Skip to main content

A Sexy Moth Model – The Molecular Basis of Sex Pheromone Biosynthesis in the Silkmoth Bombyx mori

  • Chapter
  • First Online:

Part of the book series: Entomology Monographs ((ENTMON))

Abstract

The reproductive behaviors of many insects are coordinated by the synthesis and release of species-specific volatiles that communicate the location of potential mates. Given their biological importance, structural elucidation of these compounds (i.e., sex pheromones) and molecular determination of the underlying biosynthetic pathways have been the focus of numerous studies. Among the various model species that have been examined, the silkmoth (Bombyx mori) has had an outsized impact on the research field. Indeed, it was Adolf Butenandt’s pioneering publication in 1959 on chemical characterization of the silkmoth sex pheromone (E,Z)-10,12-hexadecadien-1-ol (i.e., bombykol) that ushered in a new era of chemical ecology. Since then, B. mori has been at the forefront of each new advancement in our understanding of the pre- and postadult eclosion processes that culminate in pheromone production – from demonstration of hormonal regulation by a neuropeptide to identification of the cognate receptors and characterization of the genes comprising the biosynthetic and regulatory pathways. In honor of the 60th anniversary of bombykol’s elucidation, we provide a perspective on the spectrum of studies that have made Butenandt’s “sexy” moth one of the principal models for sex pheromone biosynthesis.

This is a preview of subscription content, log in via an institution.

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   139.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   179.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   179.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Allison JD, Cardé RT (2016) Pheromone communication in moths: evolution, behavior, and application. University of California Press

    Google Scholar 

  • Altstein M (2001) Insect neuropeptide antagonists. Biopolymers 60:460–473

    Article  CAS  PubMed  Google Scholar 

  • Altstein M, Hariton A (2009) Rational design of insect control agents: the PK/PBAN family as a study case. In: Biorational control of arthropod pests. Springer, Dordrecht, pp 49–81

    Chapter  Google Scholar 

  • Altstein M, Gazit Y, Aziz OB et al (1996) Induction of cuticular melanization in Spodoptera littoralis larvae by PBAN/MRCH: development of a quantitative bioassay and structure function analysis. Arch Insect Biochem Physiol 31:355–370

    Article  CAS  Google Scholar 

  • Altstein M, Ben-Aziz O, Zeltser I et al (2007) Inhibition of PK/PBAN-mediated functions in insects: discovery of selective and non-selective inhibitors. Peptides 28:574–584

    Article  CAS  PubMed  Google Scholar 

  • Ando T, Arima R, Uchiyama M et al (1988a) Pheromone biosynthesis activating neuropeptide hormone in heads of the silkworm moth. Agric Biol Chem 52:881–883

    CAS  Google Scholar 

  • Ando T, Hase T, Arima R, Uchiyama M (1988b) Biosynthetic pathway of bombykol, the sex pheromone of the female silkworm moth. Agric Biol Chem 52:473–478

    CAS  Google Scholar 

  • Ando T, Hase T, Funayoshi A et al (1988c) Sex pheromone biosynthesis from14C-Hexadecanoic acid in the silkworm moth. Agric Biol Chem 52:141–147

    CAS  Google Scholar 

  • Ando T, Inomata SI, Yamamoto M (2004) Lepidopteran sex pheromones. In: Schulz S (ed) The chemistry of pheromones and other semiochemicals I. Springer-Verlag, Berlin Heidelberg, pp 51–96

    Chapter  Google Scholar 

  • Antony B, Fujii T, Moto K et al (2009) Pheromone-gland-specific fatty-acyl reductase in the adzuki bean borer, Ostrinia scapulalis (Lepidoptera: Crambidae). Insect Biochem Mol Biol 39:90–95

    Article  CAS  PubMed  Google Scholar 

  • Arima R, Takahara K, Kadoshima T et al (1991) Hormonal regulation of pheromone biosynthesis in the silkworm moth, Bombyx mori (Lepidoptera: Bombycidae). Appl Entomol Zool 26:137–147

    Article  CAS  Google Scholar 

  • Audsley N, Down RE (2015) G protein coupled receptors as targets for next generation pesticides. Insect Biochem Mol Biol 67:1–32

    Article  CAS  Google Scholar 

  • Bai H, Palli SR (2013) G protein-coupled receptors as target sites for insecticide discovery. In: Advanced technologies for managing insect pests. Springer, Dordrecht, pp 57–82

    Chapter  Google Scholar 

  • Barak LS, Ménard L, Ferguson SS et al (1995) The conserved seven-transmembrane sequence NP(X)2,3Y of the G-protein-coupled receptor superfamily regulates multiple properties of the beta 2-adrenergic receptor. Biochemistry 34:15407–15414

    Article  CAS  PubMed  Google Scholar 

  • Barbosa AD, Savage DB, Siniossoglou S (2015) Lipid droplet–organelle interactions: emerging roles in lipid metabolism. Curr Opin Cell Biol 35:91–97

    Article  CAS  PubMed  Google Scholar 

  • Berridge MJ, Lipp P, Bootman MD (2000) The versatility and universality of calcium signalling. Nat Rev Mol Cell Biol 1:11–21

    Article  CAS  PubMed  Google Scholar 

  • Berridge MJ, Bootman MD, Roderick HL (2003) Calcium signalling: dynamics, homeostasis and remodelling. Nat Rev Mol Cell Biol 4:517–529

    Article  CAS  PubMed  Google Scholar 

  • Bjostad LB, Wolf WA, Roelofs WL (1987) Pheromone biosynthesis in lepidopterans: desaturation and chain shortening. In: Pheromone biochemistry. Academic Press, Orlando, pp 77–120

    Google Scholar 

  • Bober R, Rafaeli A (2010) Gene-silencing reveals the functional significance of pheromone biosynthesis activating neuropeptide receptor (PBAN-R) in a male moth. Proc Natl Acad Sci 107:16858–16862

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bouley R, Sun T-X, Chenard M et al (2003) Functional role of the NPxxY motif in internalization of the type 2 vasopressin receptor in LLC-PK1 cells. Am J Physiol Cell Physiol 285:C750–C762

    Article  CAS  PubMed  Google Scholar 

  • Butenandt A, Beckmann R, Stamm D, Hecker ET (1959) Uber den sexual-lockstoff des seidenspinners Bombyx mori -reindarstellung und konstitution. Zeitschrift Fur Naturforschung Part B-Chemie Biochemie Biophysik Biologie Und Verwandten Gebiete 14:283–284

    Google Scholar 

  • Byers DM, Gong H (2007) Acyl carrier protein: structure–function relationships in a conserved multifunctional protein family. Biochem Cell Biol 85:649–662

    Article  CAS  PubMed  Google Scholar 

  • Calebiro D, Godbole A (2018) Internalization of G-protein-coupled receptors: implication in receptor function, physiology and diseases. Best Pract Res Clin Endocrinol Metab 32:83–91

    Article  CAS  PubMed  Google Scholar 

  • Cha WH, Jung JK, Lee D-W (2018) Identification of G protein-coupled receptors in the pheromone gland of Maruca vitrata by transcriptomic analysis. J Asia-Pacific Entomol 21:1203–1210

    Article  Google Scholar 

  • Chabre M, le Maire M (2005) Monomeric G-protein-coupled receptor as a functional unit. Biochemistry 44:9395–9403

    Article  CAS  PubMed  Google Scholar 

  • Chan DI, Vogel HJ (2010) Current understanding of fatty acid biosynthesis and the acyl carrier protein. Biochem J 430:1–19

    Article  CAS  PubMed  Google Scholar 

  • Chang J-C, Ramasamy S (2014) Identification and expression analysis of diapause hormone and pheromone biosynthesis activating neuropeptide (DH-PBAN) in the legume pod borer, Maruca vitrata Fabricius. PLoS One 9:e84916–e84911

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cheng Y, Luo L, Jiang X et al (2010) Expression of pheromone biosynthesis activating neuropeptide and its receptor (PBANR) mRNA in adult female Spodoptera exigua (Lepidoptera: Noctuidae). Arch Insect Biochem Physiol 75:13–27

    Article  CAS  PubMed  Google Scholar 

  • Choi M-Y, Jurenka RA (2004) PBAN stimulation of pheromone biosynthesis by inducing calcium influx in pheromone glands of Helicoverpa zea. J Insect Physiol 50:555–560

    Article  CAS  PubMed  Google Scholar 

  • Choi M-Y, Jurenka RA (2006) Role of extracellular Ca2+ and calcium channel activated by a G protein-coupled receptor regulating pheromone production in Helicoverpa zea (Lepidoptera: Noctuidae). Ann Entomol Soc Am 99:905–909

    Google Scholar 

  • Choi M-Y, Vander Meer RK (2012) Ant trail pheromone biosynthesis is triggered by a neuropeptide hormone. PLoS One 7:e50400

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choi M-Y, Fuerst E-J, Rafaeli A, Jurenka RA (2003) Identification of a G protein-coupled receptor for pheromone biosynthesis activating neuropeptide from pheromone glands of the moth Helicoverpa zea. Proc Natl Acad Sci U S A 100:9721–9726

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choi M-Y, Fuerst E-J, Rafaeli A, Jurenka R (2007) Role of extracellular domains in PBAN/pyrokinin GPCRs from insects using chimera receptors. Insect Biochem Mol Biol 37:296–306

    Article  CAS  PubMed  Google Scholar 

  • Chow KBS, Sun J, Chu KM et al (2012) The truncated ghrelin receptor polypeptide (GHS-R1b) is localized in the endoplasmic reticulum where it forms heterodimers with ghrelin receptors (GHS-R1a) to attenuate their cell surface expression. Mol Cell Endocrinol 348:247–254

    Article  PubMed  CAS  Google Scholar 

  • Collawn JF, Stangel M, Kuhn LA et al (1990) Transferrin receptor internalization sequence YXRF implicates a tight turn as the structural recognition motif for endocytosis. Cell 63:1061–1072

    Article  CAS  PubMed  Google Scholar 

  • Cong X, Topin J, Golebiowski J (2017) Class A GPCRs: structure, function, modeling and structure-based ligand design. Curr Pharm Des 23:4390–4409

    Article  CAS  PubMed  Google Scholar 

  • Congreve M, Langmead CJ, Mason JS, Marshall FH (2011) Progress in structure-based drug design for G protein-coupled receptors. J Med Chem 54:4283–4311

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • D'Andrea S (2016) Lipid droplet mobilization: the different ways to loosen the purse strings. Biochimie 120:17–27

    Article  CAS  PubMed  Google Scholar 

  • Davis NT, Homberg U, Teal PEA et al (1996) Neuroanatomy and immunocytochemistry of the median neuroendocrine cells of the subesophageal ganglion of the tobacco hawkmoth, Manduca sexta: immunoreactivities to PBAN and other neuropeptides. Microsc Res Tech 35:201–229

    Article  CAS  PubMed  Google Scholar 

  • Derler I, Jardín I, Romanin C (2016) Molecular mechanisms of STIM/Orai communication. Am J Physiol Cell Physiol 310:C643–C662

    Article  PubMed  PubMed Central  Google Scholar 

  • Ding B-J, Löfstedt C (2015) Analysis of the Agrotis segetum pheromone gland transcriptome in the light of sex pheromone biosynthesis. BMC Genomics:1–21

    Google Scholar 

  • Donaldson LF, Beazley-Long N (2016) Alternative RNA splicing: contribution to pain and potential therapeutic strategy. Drug Discov Today 21:1787–1798

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dong C, Filipeanu CM, Duvernay MT, Wu G (2007) Regulation of G protein-coupled receptor export trafficking. Biochim Biophys Acta 1768:853–870

    Article  CAS  PubMed  Google Scholar 

  • Du M, Yin X, Zhang S et al (2012a) Identification of lipases involved in PBAN stimulated pheromone production in Bombyx mori using the DGE and RNAi approaches. PLoS One 7:e31045

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Du M, Zhang S, Zhu B et al (2012b) Identification of a diacylglycerol acyltransferase 2 gene involved in pheromone biosynthesis activating neuropeptide stimulated pheromone production in Bombyx mori. J Insect Physiol 58:699–703

    Article  CAS  PubMed  Google Scholar 

  • Du M, Liu X, Liu X et al (2015) Glycerol-3-phosphate O-acyltransferase is required for PBAN-induced sex pheromone biosynthesis in Bombyx mori. Sci Rep 5:8110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Du M, Liu X, Ma N et al (2017a) Calcineurin-mediated dephosphorylation of acetyl-coA carboxylase is required for pheromone biosynthesis activating neuropeptide (PBAN)-induced sex pheromone biosynthesis in Helicoverpa armigera. Mol Cell Proteomics 16:2138–2152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Du M, Zhao W, Jurenka R et al (2017b) Transcriptome analysis of Helicoverpa armigera male hairpencils: alcohol biosynthesis and requirement for mating success. Insect Biochem Mol Biol 87:154–164

    Article  CAS  PubMed  Google Scholar 

  • Duc NM, Kim HR, Chung KY (2015) Structural mechanism of G protein activation by G protein-coupled receptor. Eur J Pharmacol 763:214–222

    Article  PubMed  CAS  Google Scholar 

  • Duvernay MT, Filipeanu CM, Wu G (2005) The regulatory mechanisms of export trafficking of G protein-coupled receptors. Cell Signal 17:1457–1465

    Article  CAS  PubMed  Google Scholar 

  • El-Sayed AM (2018) The Pherobase: database of Pheromones and Semiochemicals www.pherobase.com

  • Fang N, Teal PE, Tumlinson JH (1996) Effects of decapitation and PBAN injection on amounts of triacylglycerols in the sex pheromone gland of Manduca sexta (L.). Arch Insect Biochem Physiol 32:249–260

    Article  CAS  Google Scholar 

  • Ferguson S (2001) Evolving concepts in G protein-coupled receptor endocytosis: the role in receptor desensitization and signaling. Pharmacol Rev 53:1–24

    CAS  PubMed  Google Scholar 

  • Ferré S, Casadó V, Devi LA et al (2014) G protein-coupled receptor oligomerization revisited: functional and pharmacological perspectives. Pharmacol Rev 66:413–434

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fodor J, Köblös G, Kákai et al (2017) Molecular cloning, mRNA expression and biological activity of the pheromone biosynthesis activating neuropeptide (PBAN) from the European corn borer, Ostrinia nubilalis. Insect Mol Biol 31:355–317

    Google Scholar 

  • Fodor J, Hull JJ, Köblös G et al (2018) Identification and functional characterization of the pheromone biosynthesis activating neuropeptide receptor isoforms from Mamestra brassicae. Gen Comp Endocrinol 258:60–69

    Article  CAS  PubMed  Google Scholar 

  • Fónagy A, Matsumoto S, Schoofs L et al (1992a) In vivo and in vitro pheromonotropic activity of two locustatachykinin peptides in Bombyx mori. Biosci Biotechnol Biochem 56:1692–1693

    Article  PubMed  Google Scholar 

  • Fónagy A, Matsumoto S, Uchiumi K et al (1992b) Action of pheromone biosynthesis activating neuropeptide on pheromone glands of Bombyx mori and Spodoptera litura. J Pest Sci 17:47–54

    Article  Google Scholar 

  • Fónagy A, Matsumoto S, Uchiumi K, Mitsui T (1992c) Role of calcium ion and cyclic nucleotides in pheromone production in Bombyx mori. J Pest Sci 17:115–121

    Article  Google Scholar 

  • Fónagy A, Schoofs L, Matsumoto S et al (1992d) Functional cross-reactivities of some locustamyotropins and Bombyx pheromone biosynthesis activating neuropeptide. J Insect Physiol 38:651–657

    Article  Google Scholar 

  • Fónagy A, Yokoyama N, Ozawa R et al (1999) Involvement of calcineurin in the signal transduction of PBAN in the silkworm, Bombyx mori (Lepidoptera). Comp Biochem Physiol B 124:51–60

    Article  PubMed  Google Scholar 

  • Fónagy A, Yokoyama N, Okano K et al (2000) Pheromone-producing cells in the silkmoth, Bombyx mori: identification and their morphological changes in response to pheromonotropic stimuli. J Insect Physiol 46:735–744

    Article  PubMed  Google Scholar 

  • Fónagy A, Yokoyama N, Matsumoto S (2001) Physiological status and change of cytoplasmic lipid droplets in the pheromone-producing cells of the silkmoth, Bombyx mori (Lepidoptera, Bombycidae). Arthropod Struct Dev 30:113–123

    Article  PubMed  Google Scholar 

  • Fónagy A, Ohnishi A, Esumi Y et al (2005) Further studies of lipid droplets in the bombykol-producing pheromone gland of Bombyx mori. Ann N Y Acad Sci 1040:310–314

    Article  PubMed  CAS  Google Scholar 

  • Foster SP (2001) Fatty acyl pheromone analogue-containing lipids and their roles in sex pheromone biosynthesis in the lightbrown apple moth, Epipyhas postvittana (Walker). J Insect Physiol 47:433–443

    Article  CAS  PubMed  Google Scholar 

  • Foster SP (2005) Lipid analysis of the sex pheromone gland of the moth Heliothis virescens. Arch Insect Biochem Physiol 59:80–90

    Article  CAS  PubMed  Google Scholar 

  • Fotiadis D, Jastrzebska B, Philippsen A et al (2006) Structure of the rhodopsin dimer: a working model for G-protein-coupled receptors. Curr Opin Struct Biol 16:252–259

    Article  CAS  PubMed  Google Scholar 

  • Fujii T, Sakurai T, Ito K et al (2018) Lipid droplets in the pheromone gland of wild silkmoth Bombyx mandarina. J Insect Biotechnol Sericol 87:2029–2034

    Google Scholar 

  • Gao Q, Goodman JM (2015) The lipid droplet—a well-connected organelle. Front Cell Dev Biol 3:49

    Article  PubMed  PubMed Central  Google Scholar 

  • Gossett RE, Frolov AA, Roths JB et al (1996) Acyl-CoA binding proteins: multiplicity and function. Lipids 31:895–918

    Article  CAS  PubMed  Google Scholar 

  • Gripentrog JM (2000) A single amino acid substitution (N297A) in the conserved NPXXY sequence of the human N-formyl peptide receptor results in inhibition of desensitization and endocytosis, and a dose-dependent shift in p42/44 mitogen-activated protein kinase activation and chemotaxis. Biochem J 352:399–407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Groot AT (2014) Circadian rhythms of sexual activities in moths: a review. Front Ecol Evol 2:43

    Article  Google Scholar 

  • Groot AT, Dekker T, Heckel DG (2015) The genetic basis of pheromone evolution in moths. Annu Rev Entomol 61:99–117

    Article  PubMed  CAS  Google Scholar 

  • Guo Y, Cordes KR, Farese RV, Walther TC (2009) Lipid droplets at a glance. J Cell Sci 122:749–752

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hagino A, Kitagawa N, Imai K et al (2010) Immunoreactive intensity of FXPRL amide neuropeptides in response to environmental conditions in the silkworm, Bombyx mori. Cell Tissue Res 342:459–469

    Article  CAS  PubMed  Google Scholar 

  • Hagström AK, Liénard MA, Groot AT et al (2012) Semi-selective fatty acyl reductases from four heliothine moths influence the specific pheromone composition. PLoS One 7:e37230

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hardie RC (2007) TRP channels and lipids: from Drosophila to mammalian physiology. J Physiol Lond 578:9–24

    Article  CAS  PubMed  Google Scholar 

  • Hariton A, Ben-Aziz O, Davidovitch M, Altstein M (2010) Bioavailability of backbone cyclic PK/PBAN neuropeptide antagonists--inhibition of sex pheromone biosynthesis elicited by the natural mechanism in Heliothis peltigera females. FEBS J 277:1035–1044

    Article  CAS  PubMed  Google Scholar 

  • Hasegawa K, Shimizu I (1990) GABAergic control of the release of diapause hormone from the suboesophageal ganglion of the silkworm, Bombyx mori. J Insect Physiol 36:909–915

    Article  CAS  Google Scholar 

  • Hayashi T, Ito U (1933) Histological observations of the alluring gland of the female silkmoth. J Seric Sci 4:308–314

    Google Scholar 

  • He R, Browning DD, Ye RD (2001) Differential roles of the NPXXY motif in formyl peptide receptor signaling. J Immunol 166:4099–4105

    Article  CAS  PubMed  Google Scholar 

  • Holman GM, Cook BJ, Nachman RJ (1986) Primary structure and synthesis of a blocked myotropic neuropeptide isolated from the cockroach, Leucophaea maderae. Comp Biochem Physiol Part C: Comp Pharmacol 85:219–224

    Article  CAS  Google Scholar 

  • Holst B, Nygaard R, Valentin-Hansen L et al (2010) A conserved aromatic lock for the tryptophan rotameric switch in TM-VI of seven-transmembrane receptors. J Biol Chem 285:3973–3985

    Article  CAS  PubMed  Google Scholar 

  • Homma T, Watanabe K, Tsurumaru S et al (2006) G protein-coupled receptor for diapause hormone, an inducer of Bombyx embryonic diapause. Biochem Biophys Res Commun 344:386–393

    Article  CAS  PubMed  Google Scholar 

  • Hong B, Zhang Z-F, Tang S-M et al (2006) Protein–DNA interactions in the promoter region of the gene encoding diapause hormone and pheromone biosynthesis activating neuropeptide of the cotton bollworm, Helicoverpa armigera. Biochim Biophys Acta Gene Struct Expr 1759:177–185

    Article  CAS  Google Scholar 

  • Hull JJ, Ohnishi A, Moto K et al (2004) Cloning and characterization of the pheromone biosynthesis activating neuropeptide receptor from the silkmoth, Bombyx mori. Significance of the carboxyl terminus in receptor internalization. J Biol Chem 279:51500–51507

    Article  CAS  PubMed  Google Scholar 

  • Hull JJ, Ohnishi A, Matsumoto S (2005) Regulatory mechanisms underlying pheromone biosynthesis activating neuropeptide (PBAN)-induced internalization of the Bombyx mori PBAN receptor. Biochem Biophys Res Commun 334:69–78

    Article  CAS  PubMed  Google Scholar 

  • Hull JJ, Kajigaya R, Imai K, Matsumoto S (2007a) The Bombyx mori sex pheromone biosynthetic pathway is not mediated by cAMP. J Insect Physiol 53:782–793

    Article  CAS  PubMed  Google Scholar 

  • Hull JJ, Kajigaya R, Imai K, Matsumoto S (2007b) Sex pheromone production in the silkworm, Bombyx mori, is mediated by store-operated Ca2+ channels. Biosci Biotechnol Biochem 71:1993–2001

    Article  CAS  PubMed  Google Scholar 

  • Hull JJ, Lee JM, Kajigaya R, Matsumoto S (2009) Bombyx mori homologs of STIM1 and Orai1 are essential components of the signal transduction cascade that regulates sex pheromone production. J Biol Chem 284:31200–31213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hull JJ, Lee JM, Matsumoto S (2010) Gqalpha-linked phospholipase Cbeta1 and phospholipase Cgamma are essential components of the pheromone biosynthesis activating neuropeptide (PBAN) signal transduction cascade. Insect Mol Biol 19:553–566

    CAS  PubMed  Google Scholar 

  • Hull JJ, Lee JM, Matsumoto S (2011) Identification of specific sites in the third intracellular loop and carboxyl terminus of the Bombyx mori pheromone biosynthesis activating neuropeptide receptor crucial for ligand-induced internalization. Insect Mol Biol 20:801–811

    Article  CAS  PubMed  Google Scholar 

  • Hulme EC (2013) GPCR activation: a mutagenic spotlight on crystal structures. Trends Pharmacol Sci 34:67–84

    Article  CAS  PubMed  Google Scholar 

  • Hussain MM (2014) Intestinal lipid absorption and lipoprotein formation. Curr Opin Lipidol 25:200–206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ichikawa T (1998) Activity patterns of neurosecretory cells releasing pheromonotropic neuropeptides in the moth Bombyx mori. Proc Natl Acad Sci U S A 95:4055–4060

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ichikawa T, Kamimoto S (2003) Firing activities of neurosecretory cells producing diapause hormone and its related peptides in the female silkmoth, Bombyx mori. II. Mandibular and maxillary cells. Zool Sci 20:979–983

    Article  CAS  Google Scholar 

  • Ichikawa T, Suenobu A (2003) Firing activity of “diapause hormone” producing cells in the male silkmoth, Bombyx mori. Zool Sci 20:957–962

    Article  Google Scholar 

  • Ichikawa T, Hasegawa K, Shimizu I et al (1995) Structure of neurosecretory cells with immunoreactive diapause hormone and pheromone biosynthesis activating neuropeptide in the silkworm, Bombyx mori. Zool Sci 12:703–712

    Article  CAS  Google Scholar 

  • Ichikawa T, Shiota T, Shimizu I, Kataoka H (1996) Functional differentiation of neurosecretory cells with immunoreactive diapause hormone and pheromone biosynthesis activating neuropeptide of the moth, Bombyx mori. Zool Sci 13:21–25

    Article  CAS  Google Scholar 

  • Ichikawa T, Aoki S, Shimizu I (1997) Neuroendocrine control of diapause hormone secretion in the silkworm, Bombyx mori. J Insect Physiol 43:1101–1109

    Article  CAS  PubMed  Google Scholar 

  • Imai K, Konno T, Nakazawa Y et al (1991) Isolation and structure of diapause hormone of the silkworm, Bombyx mori. Proc Jpn Acad Ser B Phys Biol Sci 67:98–101

    Article  CAS  Google Scholar 

  • Iwanaga M, Dohmae N, Francke A et al (1998) Isolation and characterization of calmodulin in the pheromone gland of the silkworm, Bombyx mori. Comp Biochem Physiol B Biochem Mol Biol 120:761–767

    Article  CAS  PubMed  Google Scholar 

  • Jiang L, Zhang F, Hou Y et al (2018) Isolation and functional characterization of the pheromone biosynthesis activating neuropeptide receptor of Chinese oak silkworm, Antheraea pernyi. Int J Biol Macromol 117:42–50

    Article  CAS  PubMed  Google Scholar 

  • Jing T-Z, Wang Z-Y, Qi F-H, Liu K-Y (2007) Molecular characterization of diapause hormone and pheromone biosynthesis activating neuropeptide from the black-back prominent moth, Clostera anastomosis (L.) (Lepidoptera, Notodontidae). Insect Biochem Mol Biol 37:1262–1271

    Article  CAS  PubMed  Google Scholar 

  • Jurenka R (1996) Signal transduction in the stimulation of sex pheromone biosynthesis in moths. Arch Insect Biochem Physiol 33:245–258

    Article  CAS  Google Scholar 

  • Jurenka R (2015) The PRXamide neuropeptide signalling system: conserved in animals. In: Jurenka R (ed) Advances in insect physiology. Academic Press, Oxford, pp 123–170

    Google Scholar 

  • Jurenka R (2017) Regulation of pheromone biosynthesis in moths. Curr Opin Insect Sci 24:29–35

    Article  PubMed  Google Scholar 

  • Jurenka R, Nusawardani T (2011) The pyrokinin/ pheromone biosynthesis-activating neuropeptide (PBAN) family of peptides and their receptors in Insecta: evolutionary trace indicates potential receptor ligand-binding domains. Insect Mol Biol 20:323–334

    Article  CAS  PubMed  Google Scholar 

  • Jurenka RA, Jacquin E, Roelofs WL (1991a) Stimulation of pheromone biosynthesis in the moth Helicoverpa zea: action of a brain hormone on pheromone glands involves Ca2+ and cAMP as second messengers. Proc Natl Acad Sci U S A 88:8621–8625

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jurenka RA, Jacquin E, Roelofs WL (1991b) Control of the pheromone biosynthetic pathway in Helicoverpa zea by the pheromone biosynthesis activating neuropeptide. Arch Insect Biochem Physiol 17:81–91

    Article  CAS  Google Scholar 

  • Jurenka RA, Fabriás G, DeVoe L, Roelofs WL (1994) Action of PBAN and related peptides on pheromone biosynthesis in isolated pheromone glands of the redbanded leafroller moth, Argyrotaenia velutinana. Comp Biochem Physiol Pharmacol Toxicol Endocrinol 108:153–160

    Article  CAS  PubMed  Google Scholar 

  • Kawai T, Hull JJ, Matsumoto S et al (2010) Studies on the structure-activity relationship of pheromone biosynthesis-activating neuropeptide (PBAN). In: Okamoto K (ed) Peptide science 2009: proceedings of the 46th Japanese peptide symposium. The Japanese Peptide Society Press, Osaka, pp 231–234

    Google Scholar 

  • Kawai T, Nagata K, Okada K et al (2011) Structure-activity relationship studies of the pheromone biosynthesis-activating neuropeptide of the silkworm, Bombyx mori. In: Fujii N, Kiso Y (eds) Peptide SCIENCE 2010: proceedings of the fifth international peptide symposium. The Japanese Peptide Society Press, Osaka, p 126

    Google Scholar 

  • Kawai T, Lee JM, Nagata K et al (2012) The arginine residue within the C-terminal active core of Bombyx mori pheromone biosynthesis-activating neuropeptide is essential for receptor binding and activation. Front Endocrinol 3:42

    Article  Google Scholar 

  • Kawai T, Katayama Y, Guo L et al (2014) Identification of functionally important residues of the silkmoth pheromone biosynthesis-activating neuropeptide receptor, an insect ortholog of the vertebrate neuromedin U receptor. J Biol Chem 289:19150–19163

    Article  CAS  PubMed  Google Scholar 

  • Kawano T, Kataoka H, Nagasawa H, Isogai A (1992) cDNA cloning and sequence determination of the pheromone biosynthesis activating neuropeptide of the silkworm, Bombyx mori. Biochem Biophys Res Commun 189:221–226

    Article  CAS  PubMed  Google Scholar 

  • Kim Y-J, Nachman R, Aimanova K et al (2008) The pheromone biosynthesis activating neuropeptide (PBAN) receptor of Heliothis virescens: identification, functional expression, and structure-activity relationships of ligand analogs. Peptides 29:268–275

    Article  CAS  PubMed  Google Scholar 

  • Kingan TG, Blackburn MB, Raina AK (1992) The distribution of pheromone-biosynthesis-activating neuropeptide (PBAN) immunoreactivity in the central nervous system of the corn earworm moth, Helicoverpa zea. Cell Tissue Res 270:229–240

    Article  CAS  Google Scholar 

  • Kitamura A, Nagasawa H, Kataoka H et al (1989) Amino acid sequence of pheromone-biosynthesis-activating neuropeptide (PBAN) of the silkworm, Bombyx mori. Biochem Biophys Res Commun 163:520–526

    Article  CAS  PubMed  Google Scholar 

  • Kitamura A, Nagasawa H, Kataoka H et al (1990) Amino acid sequence of pheromone biosynthesis activating neuropeptide-II (PBAN-II) of the silkmoth, Bombyx mori. Agric Biol Chem 54:2495–2497

    CAS  PubMed  Google Scholar 

  • Kleinau G, Jaeschke H, Worth CL et al (2010) Principles and determinants of G-protein coupling by the rhodopsin-like thyrotropin receptor. PLoS One 5:e9745

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kristiansen K (2004) Molecular mechanisms of ligand binding, signaling, and regulation within the superfamily of G-protein-coupled receptors: molecular modeling and mutagenesis approaches to receptor structure and function. Pharmacol Ther 103:21–80

    Article  CAS  PubMed  Google Scholar 

  • Kuniyoshi H, Kitamura A, Nagasawa H et al (1991a) Structure-activity relationship of pheromone biosynthesis activating neuropeptide (PBAN) from the silkmoth, Bombyx mori. Pept Chem 1990:251–254

    Google Scholar 

  • Kuniyoshi H, Nagasawa H, Ando T, Suzuki A (1991b) Structure-activity relationship and metabolism of pheromone biosynthesis activating neuropeptide (PBAN) from the silkmoth Bombyx mori. Pept Chem:221–226

    Google Scholar 

  • Kuniyoshi H, Nagasawa H, Ando T et al (1992a) Cross-activity between pheromone biosynthesis activating neuropeptide (PBAN) and myotropic pyrokinin insect peptides. Biosci Biotechnol Biochem 56:167–168

    Article  CAS  PubMed  Google Scholar 

  • Kuniyoshi H, Nagasawa H, Ando T, Suzuki A (1992b) N-terminal modified analogs of C-terminal fragments of PBAN with pheromonotropic activity. Insect Biochem Mol Biol 22:399–403

    Article  CAS  Google Scholar 

  • Lassance J-M, Liénard MA, Antony B et al (2013) Functional consequences of sequence variation in the pheromone biosynthetic gene pgFAR for Ostrinia moths. Proc Natl Acad Sci U S A 110:3967–3972

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee JM, Hull JJ, Kawai T et al (2012a) Re-evaluation of the PBAN receptor molecule: characterization of PBANR variants expressed in the pheromone glands of moths. Front Endocrinol 3:6

    Article  CAS  Google Scholar 

  • Lee JM, Hull JJ, Kawai T et al (2012b) Establishment of Sf9 transformants constitutively expressing PBAN receptor variants: application to functional evaluation. Front Endocrinol 3:56

    Google Scholar 

  • Liénard MA, Hagström AK, Lassance J-M, Löfstedt C (2010) Evolution of multicomponent pheromone signals in small ermine moths involves a single fatty-acyl reductase gene. Proc Natl Acad Sci U S A 107:10955–10960

    Article  PubMed  PubMed Central  Google Scholar 

  • Ma PW, Ramaswamy SB (2003) Biology and ultrastructure of sex pheromone-producing tissue. In: Insect pheromone biochemistry and molecular biology. Academic Press, Boston, pp 19–51

    Chapter  Google Scholar 

  • Ma PWK, Roelofs WL (1995a) Sites of synthesis and release of PBAN-like factor in the female European corn borer, Ostrinia nubilalis. J Insect Physiol 41:339–350

    Article  CAS  Google Scholar 

  • Ma PWK, Roelofs WL (1995b) Calcium involvement in the stimulation of sex pheromone production by PBAN in the European corn borer, Ostrinia nubilalis (Lepidoptera: Pyralidae). Insect Biochem Mol Biol 25:467–473

    Article  CAS  Google Scholar 

  • Maggio R, Fasciani I, Rossi M et al (2016) Variants of G protein-coupled receptors: a reappraisal of their role in receptor regulation. Biochem Soc Trans 44:589–594

    Article  CAS  PubMed  Google Scholar 

  • Markovic D, Challiss RAJ (2009) Alternative splicing of G protein-coupled receptors: physiology and pathophysiology. Cell Mol Life Sci 66:3337–3352

    Article  CAS  PubMed  Google Scholar 

  • Matoušková P, Pichová I, Svatos A (2007) Functional characterization of a desaturase from the tobacco hornworm moth (Manduca sexta) with bifunctional Z11-and 10, 12-desaturase activity. Insect Biochem Mol Biol 37:601–610

    Article  PubMed  CAS  Google Scholar 

  • Matsumoto S, Isogai A, Suzuki A (1986) Isolation and amino terminal sequence of melanization and reddish coloration hormone (MRCH) from the silkworm, Bombyx mori. Insect Biochem 16:775–779

    Article  CAS  Google Scholar 

  • Matsumoto S, Kitamura A, Nagasawa H et al (1990) Functional diversity of a neurohormone produced by the suboesophageal ganglion: molecular identity of melanization and reddish colouration hormone and pheromone biosynthesis activating neuropeptide. J Insect Physiol 36:427–432

    Article  CAS  Google Scholar 

  • Matsumoto S, Fónagy A, Kurihara M, Uchiumi K (1992a) Isolation and primary structure of a novel pheromonotropic neuropeptide structurally related to leucopyrokinin from the armyworm larvae, Pseudaletia separata. Biochem Biophys Res Commun 182:534–539

    Article  CAS  PubMed  Google Scholar 

  • Matsumoto S, Yamashita O, Fónagy A (1992b) Functional diversity of a pheromonotropic neuropeptide: induction of cuticular melanization and embryonic diapause in lepidopteran insects by Pseudaletia pheromonotropin. J Insect Physiol 38:847–851

    Article  CAS  Google Scholar 

  • Matsumoto S, Ozawa R, Nagamine T et al (1995a) Intracellular transduction in the regulation of pheromone biosynthesis of the silkworm, Bombyx mori: suggested involvement of calmodulin and phosphoprotein phosphatase. Biosci Biotechnol Biochem 59:560–562

    Article  CAS  PubMed  Google Scholar 

  • Matsumoto S, Ozawa R, Uchiumi K et al (1995b) Intracellular signal transduction of PBAN action in the common cutworm, Spodoptera litura: effects of pharmacological agents on sex pheromone production in vitro. Insect Biochem Mol Biol 25:1055–1059

    Article  CAS  PubMed  Google Scholar 

  • Matsumoto S, Yoshiga T, Yokoyama N et al (2001) Characterization of acyl-CoA-binding protein (ACBP) in the pheromone gland of the silkworm, Bombyx mori. Insect Biochem Mol Biol 31:603–609

    Article  CAS  PubMed  Google Scholar 

  • Matsumoto S, Fónagy A, Yamamoto M (2002) Chemical characterization of cytoplasmic lipid droplets in the pheromone-producing cells of the silkmoth, Bombyx mori. Insect Biochem Mol Biol 32:1447–1455

    Article  CAS  PubMed  Google Scholar 

  • Matsutani K, Sonobe H (1987) Control of diapause-factor secretion from the suboesophageal ganglion in the silkworm, Bombyx mori: the roles of the protocerebrum and tritocerebrum. J Insect Physiol 33:279–285

    Article  CAS  Google Scholar 

  • McDowell DG, Burns NA, Parkes HC (1998) Localised sequence regions possessing high melting temperatures prevent the amplification of a DNA mimic in competitive PCR. Nucleic Acids Res 26:3340–3347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mobarec JC, Sanchez R, Filizola M (2009) Modern homology modeling of G-protein coupled receptors: which structural template to use? J Med Chem 52:5207–5216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Morita A, Niimi T, Yamashita O (2003) Physiological differentiation of DH-PBAN-producing neurosecretory cells in the silkworm embryo. J Insect Physiol 49:1093–1102

    Article  CAS  PubMed  Google Scholar 

  • Moto K-I, Matsumoto S (2012) Construction of an in vivo system for functional analysis of the genes involved in sex pheromone production in the silkmoth, Bombyx mori. Front Endocrinol 3:30

    Article  Google Scholar 

  • Moto K, Yoshiga T, Yamamoto M et al (2003) Pheromone gland-specific fatty-acyl reductase of the silkmoth, Bombyx mori. Proc Natl Acad Sci U S A 100:9156–9161

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moto K, Suzuki MG, Hull JJ et al (2004) Involvement of a bifunctional fatty-acyl desaturase in the biosynthesis of the silkmoth, Bombyx mori, sex pheromone. Proc Natl Acad Sci U S A 101:8631–8636

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mount SM (1982) A catalogue of splice junction sequences. Nucleic Acids Res 10:459–472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nachman RJ (2009) Agonists/antagonists of the insect kinin and pyrokinin/PBAN neuropeptide classes as tools for rational pest control. In: Biorational control of arthropod pests: application and resistance management. Springer, Dordrecht, pp 21–48

    Chapter  Google Scholar 

  • Nachman RJ (2014) Peptidomics applied: a new strategy for development of selective antagonists/agonists of insect pyrokinin (FXPRLamide) family using a novel conformational-mimetic motif. EuPA Open Proteom 3:138–142

    Article  CAS  Google Scholar 

  • Nachman RJ, Kuniyoshi H, Roberts VA et al (1993) Active conformation of the pyrokinin/PBAN neuropeptide family for pheromone biosynthesis in the silkworm. Biochem Biophys Res Commun 193:661–666

    Article  CAS  PubMed  Google Scholar 

  • Nagasawa H, Kitamura A, Inoue T et al (1988) Isolation of pheromone biosynthesis activating neuropeptide of the silkworm, Bombyx mori. Agric Biol Chem 52:2985–2987

    CAS  Google Scholar 

  • Nagasawa H, Kuniyoshi H, Arima R et al (1994) Structure and activity of Bombyx PBAN. Arch Insect Biochem Physiol 25:261–270

    Article  CAS  PubMed  Google Scholar 

  • Noguchi H, Hayakawa Y (2001) Dopamine is a key factor for the induction of egg diapause of the silkworm, Bombyx mori. Eur J Biochem 268:774–780

    Article  CAS  PubMed  Google Scholar 

  • Nusawardani T, Kroemer JA, Choi M-Y, Jurenka RA (2013) Identification and characterization of the pyrokinin/pheromone biosynthesis activating neuropeptide family of G protein-coupled receptors from Ostrinia nubilalis. Insect Mol Biol 22:331–340

    Article  CAS  PubMed  Google Scholar 

  • Nwokonko RM, Cai X, Loktionova NA et al (2017) The STIM-Orai pathway: conformational coupling between STIM and Orai in the activation of store-operated Ca2+ entry. In: Store-operated Ca2+ entry (SOCE) pathways. Springer, Cham, pp 83–98

    Chapter  Google Scholar 

  • Ohguchi Y, Tatsuki S, Usui K, Arai K (1985) Hormone-like substance present in the cephalic organs of the female moth, Chilo suppressalis (Walker)(Lepidoptera:Pyralidae) and controlling sex pheromone production. Jpn J Appl Entomol Zool 29:265–269

    Article  CAS  Google Scholar 

  • Ohnishi A, Koshino H, Takahashi S et al (2005) Isolation and characterization of a humoral factor that stimulates transcription of the acyl-CoA-binding protein in the pheromone gland of the silkmoth, Bombyx mori. J Biol Chem 280:4111–4116

    Article  CAS  PubMed  Google Scholar 

  • Ohnishi A, Hull JJ, Matsumoto S (2006) Targeted disruption of genes in the Bombyx mori sex pheromone biosynthetic pathway. Proc Natl Acad Sci U S A 103:4398–4403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ohnishi A, Hashimoto K, Imai K, Matsumoto S (2009) Functional characterization of the Bombyx mori fatty acid transport protein (BmFATP) within the silkmoth pheromone gland. J Biol Chem 284:5128–5136

    Article  CAS  PubMed  Google Scholar 

  • Ohnishi A, Hull JJ, Kaji M et al (2011a) Hormone signaling linked to silkmoth sex pheromone biosynthesis involves Ca2+/calmodulin-dependent protein kinase II-mediated phosphorylation of the insect PAT family protein Bombyx mori lipid storage droplet protein-1 (BmLsd1). J Biol Chem 286:24101–24112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ohnishi A, Kaji M, Hashimoto K, Matsumoto S (2011b) Screening for the genes involved in bombykol biosynthesis: identification and functional characterization of Bombyx mori acyl carrier protein. Front Endocrinol 2:92

    Article  Google Scholar 

  • Okada A, Kawai T, Sugisaka A, Ohtsuka J, Hull JJ, Moto K, Matsumoto S, Nagasawa H, Nagata K, Tanokura M (2009) Structural analysis of the active and inactive fragments of pheromone biosynthesis-activating neuropeptide (PBAN) from the silkmoth Bombyx mori. In: Peptide science: proceedings of the Japanese peptide symposium, pp 535–538

    Google Scholar 

  • Ozawa R, Matsumoto S (1996) Intracellular signal transduction of PBAN action in the silkworm, Bombyx mori: involvement of acyl CoA reductase. Insect Biochem Mol Biol 26:259–265

    Article  CAS  PubMed  Google Scholar 

  • Ozawa AR, Ando T, Nagasawa H et al (1993) Reduction of the acyl group: the critical step in bombykol biosynthesis that is regulated in vitro by the neuropeptide hormone in the pheromone gland of Bombyx mori. Biosci Biotechnol Biochem 57:2144–2147

    Article  CAS  Google Scholar 

  • Ozawa R, Matsumoto S, Kim GH et al (1995) Intracellular signal transduction of PBAN action in lepidopteran insects: inhibition of sex pheromone production by compactin, an HMG CoA reductase inhibitor. Regul Pept 57:319–327

    Article  CAS  PubMed  Google Scholar 

  • Paing MM, Temple BRS, Trejo J (2004) A tyrosine-based sorting signal regulates intracellular trafficking of protease-activated receptor-1: multiple regulatory mechanisms for agonist-induced G protein-coupled receptor internalization. J Biol Chem 279:21938–21947

    Article  CAS  PubMed  Google Scholar 

  • Pandey KN (2009) Functional roles of short sequence motifs in the endocytosis of membrane receptors. Front Biosci 14:5339–5360

    Article  CAS  Google Scholar 

  • Parekh AB (2006) On the activation mechanism of store-operated calcium channels. Pflugers Arch 453:303–311

    Article  CAS  PubMed  Google Scholar 

  • Park Y, Kim Y-J, Adams ME (2002) Identification of G protein-coupled receptors for Drosophila PRXamide peptides, CCAP, corazonin, and AKH supports a theory of ligand-receptor coevolution. Proc Natl Acad Sci U S A 99:11423–11428

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Patel RT, Soulages JL, Hariharasundaram B, Arrese EL (2005) Activation of the lipid droplet controls the rate of lipolysis of triglycerides in the insect fat body. J Biol Chem 280:22624–22631

    Article  CAS  PubMed  Google Scholar 

  • Patterson R, Vanrossum D, Nikolaidis N et al (2005) Phospholipase C-γ: diverse roles in receptor-mediated calcium signaling. Trends Biochem Sci 30:688–697

    Article  CAS  PubMed  Google Scholar 

  • Percy-Cunningham JE, MacDonald JA (1987) Biology and ultrastructure of sex pheromone-producing glands. In: Blomquist GJ, Prestwich GD (eds) Pheromone biochemistry. Academic Press, Orlando, pp 27–75

    Google Scholar 

  • Pol A, Gross SP, Parton RG (2014) Biogenesis of the multifunctional lipid droplet: lipids, proteins, and sites. J Cell Biol 204:635–646

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quentien MH, Manfroid I, Moncet D et al (2002) Pitx factors are involved in basal and hormone-regulated activity of the human prolactin promoter. J Biol Chem (46):44408–44416

    Article  CAS  PubMed  Google Scholar 

  • Rafaeli A (1994) Pheromonotropic stimulation of moth pheromone gland cultures in vitro. Arch Insect Biochem Physiol 25:287–299

    Article  CAS  Google Scholar 

  • Rafaeli A, Gileadi C (1996) Down regulation of pheromone biosynthesis: cellular mechanisms of pheromonostatic responses. Insect Biochem Mol Biol 26:797–807

    Article  CAS  Google Scholar 

  • Rafaeli A, Gileadi C (1997) Neuroendocrine control of pheromone production in moths. Invertebr Neurosci 3:223–229

    Article  CAS  Google Scholar 

  • Rafaeli A, Soroker V (1989) Cyclic AMP mediation of the hormonal stimulation of 14C-acetate incorporation by Heliothis armigera pheromone glands in vitro. Mol Cell Endocrinol 65:43–48

    Article  CAS  PubMed  Google Scholar 

  • Rafaeli A, Soroker V, Kamensky B, Raina AK (1990) Action of pheromone biosynthesis activating neuropeptide on in vitro pheromone glands of Heliothis armigera females. J Insect Physiol 36:641–646

    Article  CAS  Google Scholar 

  • Rafaeli A, Zakharova T, Lapsker Z, Jurenka RA (2003) The identification of an age- and female-specific putative PBAN membrane-receptor protein in pheromone glands of Helicoverpa armigera: possible up-regulation by juvenile hormone. Insect Biochem Mol Biol 33:371–380

    Article  CAS  PubMed  Google Scholar 

  • Rafaeli A, Bober R, Becker L et al (2007) Spatial distribution and differential expression of the PBAN receptor in tissues of adult Helicoverpa spp. (Lepidoptera: Noctuidae). Insect Mol Biol 16:287–293

    Article  CAS  PubMed  Google Scholar 

  • Raina AK, Klun JA (1984) Brain factor control of sex pheromone production in the female corn earworm moth. Science 225:531–533

    Article  CAS  PubMed  Google Scholar 

  • Raina AK, Jaffe H, Klun JA et al (1987) Characteristics of a neurohormone that controls sex pheromone production in Heliothis zea. J Insect Physiol 33:809–814

    Article  CAS  Google Scholar 

  • Raina A, Jaffe H, Kempe T et al (1989) Identification of a neuropeptide hormone that regulates sex pheromone production in female moths. Science 244:796–798

    Article  CAS  PubMed  Google Scholar 

  • Raina AK, Kingan TG, Kochansky JP (2003) A pheromonotropic peptide of Helicoverpa zea, with melanizing activity, interaction with PBAN, and distribution of immunoreactivity. Arch Insect Biochem Physiol 53:147–157

    Article  CAS  PubMed  Google Scholar 

  • Riddiford LM, Williams CM (1971) Role of the corpora cardiaca in the behavior of saturniid moths. I. Release of sex pheromone. Biol Bull 140:1–7

    Article  CAS  PubMed  Google Scholar 

  • Roelofs WL, Liu W, Hao G et al (2002) Evolution of moth sex pheromones via ancestral genes. Proc Natl Acad Sci U S A 99:13621–13626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sabio M, Jones K, Topiol S (2008) Use of the X-ray structure of the beta2-adrenergic receptor for drug discovery. Part 2: identification of active compounds. Bioorg Med Chem Lett 18:5391–5395

    Article  CAS  PubMed  Google Scholar 

  • Sakurai T, Namiki S, Kanzaki R (2014) Molecular and neural mechanisms of sex pheromone reception and processing in the silkmoth Bombyx mori. Front Physiol 5:125

    Article  PubMed  PubMed Central  Google Scholar 

  • Sato Y, Oguchi M, Menjo N et al (1993) Precursor polyprotein for multiple neuropeptides secreted from the suboesophageal ganglion of the silkworm Bombyx mori: characterization of the cDNA encoding the diapause hormone precursor and identification of additional peptides. Proc Natl Acad Sci U S A 90:3251–3255

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sato Y, Ikeda M, Yamashita O (1994) Neurosecretory cells expressing the gene for common precursor for diapause hormone and pheromone biosynthesis-activating neuropeptide in the suboesophageal ganglion of the silkworm, Bombyx mori. Gen Comp Endocrinol 96:27–36

    Article  CAS  PubMed  Google Scholar 

  • Sato Y, Shiomi K, Saito H et al (1998) Phe-X-Pro-Arg-Leu-NH2 peptide producing cells in the central nervous system of the silkworm, Bombyx mori. J Insect Physiol 44:333–342

    Article  CAS  PubMed  Google Scholar 

  • Scherkenbeck J, Zdobinsky T (2009) Insect neuropeptides: structures, chemical modifications and potential for insect control. Bioorganic Med Chem 17:4071–4084

    Article  CAS  Google Scholar 

  • Schoofs L, Vanden Broeck J, De Loof A (1993) The myotropic peptides of Locusta migratoria: structures, distribution, functions and receptors. Insect Biochem Mol Biol 23:859–881

    Article  CAS  PubMed  Google Scholar 

  • Schoofs L, De Loof A, Van Hiel MB (2017) Neuropeptides as regulators of behavior in insects. Annu Rev Entomol 62:35–52

    Article  CAS  PubMed  Google Scholar 

  • Seck T, Pellegrini M, Florea AM et al (2005) The delta e13 isoform of the calcitonin receptor forms a six-transmembrane domain receptor with dominant-negative effects on receptor surface expression and signaling. Mol Endocrinol 19:2132–2144

    Article  CAS  PubMed  Google Scholar 

  • Senthilkumar R, Srinivasan R (2019) Sex-specific spatial and temporal gene expressions of pheromone biosynthesis activating neuropeptide (PBAN) and binding proteins (PBP/OBP) in Spoladea recurvalis. Sci Rep 9:3515

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Serra M, Gauthier LT, Fabrias G, Buist PH (2006a) Delta11 desaturases of Trichoplusia ni and Spodoptera littoralis exhibit dual catalytic behaviour. Insect Biochem Mol Biol 36:822–825

    Article  CAS  PubMed  Google Scholar 

  • Serra M, Piña B, Bujons J et al (2006b) Biosynthesis of 10, 12-dienoic fatty acids by a bifunctional Δ11desaturase in Spodoptera littoralis. Insect Biochem Mol Biol 36:634–641

    Article  CAS  PubMed  Google Scholar 

  • Serra M, Piña B, Abad JL et al (2007) A multifunctional desaturase involved in the biosynthesis of the processionary moth sex pheromone. Proc Natl Acad Sci U S A 104:16444–16449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shapiro JP, Law JH, Wells MA (1988) Lipid transport in insects. Annu Rev Entomol 33:297–318

    Article  CAS  PubMed  Google Scholar 

  • Sharma RK, Parameswaran S (2018) Calmodulin-binding proteins: a journey of 40 years. Cell Calcium 75:89–100

    Article  CAS  PubMed  Google Scholar 

  • Shimizu I, Matsui T, Hasegawa K (1989) Possible involvement of GABAergic neurons in regulation of diapause hormone secretion in the silkworm, Bombyx mori. Zool Sci 6:809–812

    CAS  Google Scholar 

  • Shimomura M, Minami H, Suetsugu Y et al (2009) KAIKObase: an integrated silkworm genome database and data mining tool. BMC Genomics 10:486

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Shiomi K, Kajiura Z, Nakagaki M, Yamashita O (2003) Baculovirus-mediated efficient gene transfer into the central nervous system of the silkworm, Bombyx mori. J Insect Biotech Sericology 72:149–155

    CAS  Google Scholar 

  • Shiomi K, Fujiwara Y, Yasukochi Y et al (2007) The Pitx homeobox gene in Bombyx mori: regulation of DH-PBAN neuropeptide hormone gene expression. Mol Cell Neurosci 34:209–218

    Article  CAS  PubMed  Google Scholar 

  • Shiomi K, Takasu Y, Kunii M et al (2015) Disruption of diapause induction by TALEN-based gene mutagenesis in relation to a unique neuropeptide signaling pathway in Bombyx. Sci Rep:1–10

    Google Scholar 

  • Shuttleworth TJ, Thompson JL, Mignen O (2004) ARC channels: a novel pathway for receptor-activated calcium entry. Physiology (Bethesda) 19:355–361

    CAS  Google Scholar 

  • Slice LW, Wong HC, Sternini C et al (1994) The conserved NPXnY motif present in the gastrin-releasing peptide receptor is not a general sequestration sequence. J Biol Chem 269:21755–21761

    CAS  PubMed  Google Scholar 

  • Soroker V, Rafaeli A (1989) In vitro hormonal stimulation of [14C]acetate incorporation by Heliothis armigera pheromone glands. Insect Biochemistry 19:1–5

    Article  CAS  Google Scholar 

  • Soroker V, Rafaeli A (1995) Multi-signal transduction of the pheromonotropic response by pheromone gland incubations of Helicoverpa armigera. Insect Biochem Mol Biol 25:1–9

    Article  CAS  Google Scholar 

  • Stahl A (2004) A current review of fatty acid transport proteins (SLC27). Pflugers Arch 447:722–727

    Article  CAS  PubMed  Google Scholar 

  • Steinbrecht RA (1964) Feinstruktur und Histochemie der Sexualduftdrüse des Seidenspinners Bombyx mori L. Z Zellforsch Mikrosk Anat 64:227–261

    CAS  Google Scholar 

  • Stern PS, Yu L, Choi M-Y et al (2007) Molecular modeling of the binding of pheromone biosynthesis activating neuropeptide to its receptor. J Insect Physiol 53:803–818

    Article  CAS  PubMed  Google Scholar 

  • Sztalryd C, Brasaemle DL (2017) The perilipin family of lipid droplet proteins: gatekeepers of intracellular lipolysis. Biochim Biophyis Acta - Mol Cell Biol Lipids 1862:1221–1232

    Article  CAS  Google Scholar 

  • Takeuchi K, Reue K (2009) Biochemistry, physiology, and genetics of GPAT, AGPAT, and lipin enzymes in triglyceride synthesis. Am J Physiol Endocrinol Metab 296:E1195–E1209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tang JD, Charlton RE, Jurenka RA et al (1989) Regulation of pheromone biosynthesis by a brain hormone in two moth species. Proc Natl Acad Sci U S A 86:1806–1810

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tawata M, Ichikawa T (2001) Circadian firing activities of neurosecretory cells releasing pheromonotropic neuropeptides in the silkmoth, Bombyx mori. Zool Sci 18:645–649

    Article  CAS  Google Scholar 

  • Teal PEA, Tumlinson JH, Oberlander H (1989) Neural regulation of sex pheromone biosynthesis in Heliothis moths. Proc Natl Acad Sci U S A 86:2488–2492

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tehan BG, Bortolato A, Blaney FE et al (2014) Unifying family A GPCR theories of activation. Pharmacol Ther 143:51–60

    Article  CAS  Google Scholar 

  • Tips A, Schoofs L, Paemen L et al (1993) Co-localization of locustamyotropin-like and pheromone biosynthesis activating neuropeptide-like immunoreactivity in the central-nervous-system of five insect species. Comp Biochem Physiol A Comp Physiol 106:195–207

    Article  Google Scholar 

  • Tremblay JJ, Drouin J (1999) Egr-1 is a downstream effector of GnRH and synergizes by direct interaction with Ptx1 and SF-1 to enhance luteinizing hormone beta gene transcription. Mol Cell Biol 19:2567–2576

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trzaskowski B, Latek D, Yuan S et al (2012) Action of molecular switches in GPCRs--theoretical and experimental studies. Curr Med Chem 19:1090–1109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsfadia O, Azrielli A, Falach L et al (2008) Pheromone biosynthetic pathways: PBAN-regulated rate-limiting steps and differential expression of desaturase genes in moth species. Insect Biochem Mol Biol 38:552–567

    Article  CAS  PubMed  Google Scholar 

  • Uehara H, Senoh Y, Yoneda K et al (2011) An FXPRLamide neuropeptide induces seasonal reproductive polyphenism underlying a life-history tradeoff in the tussock moth. PLoS One 6:e24213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Urrutia J, Aguado A, Muguruza-Montero A et al (2019) The crossroad of ion channels and calmodulin in disease. Int J Mol Sci 20:400–422

    Article  PubMed Central  CAS  Google Scholar 

  • Van Hiel MB, Van Loy T, Poels J et al (2010) Neuropeptide receptors as possible targets for development of insect pest control agents. Adv Exp Med Biol 692:211–226

    Article  PubMed  Google Scholar 

  • Veenstra JA (2000) Mono- and dibasic proteolytic cleavage sites in insect neuroendocrine peptide precursors. Arch Insect Biochem Physiol 43:49–63

    Article  CAS  PubMed  Google Scholar 

  • Waku Y, Sumimoto K-I (1969) Ultrastructure and secretory mechanism of the alluring gland cell in the silkworm, Bombyx mori L. (Lepidoptera: Bombycidae). Appl Entomol Zool 4:135–146

    Article  Google Scholar 

  • Wang W, Qiao Y, Li Z (2018) New insights into modes of GPCR activation. Trends Pharmacol Sci 39:367–386

    Article  CAS  PubMed  Google Scholar 

  • Watanabe K (1924) Studies on the voltinism of the silkworm, Bombyx mori. Bull Sericult Exp Sta (Tokyo) 6:411–455

    Google Scholar 

  • Watanabe K, Hull JJ, Niimi T et al (2007) FXPRL-amide peptides induce ecdysteroidogenesis through a G-protein coupled receptor expressed in the prothoracic gland of Bombyx mori. Mol Cell Endocrinol 273:51–58

    Article  CAS  PubMed  Google Scholar 

  • Whorton MR, Jastrzebska B, PS-H P et al (2008) Efficient coupling of transducin to monomeric rhodopsin in a phospholipid bilayer. J Biol Chem 283:4387–4394

    Article  CAS  PubMed  Google Scholar 

  • Wu SF, Yu HY, Jiang TT et al (2015) Superfamily of genes encoding G protein-coupled receptors in the diamondback moth Plutella xylostella (Lepidoptera: Plutellidae). Insect Mol Biol 24:442–453

    Article  CAS  PubMed  Google Scholar 

  • Xu W-H, Denlinger DL (2003) Molecular characterization of prothoracicotropic hormone and diapause hormone in Heliothis virescens during diapause, and a new role for diapause hormone. Insect Mol Biol 12:509–516

    Article  CAS  PubMed  Google Scholar 

  • Xu W-H, Sato Y, Ikeda M, Yamashita O (1995a) Stage-dependent and temperature-controlled expression of the gene encoding the precursor protein of diapause hormone and pheromone biosynthesis activating neuropeptide in the silkworm, Bombyx mori. J Biol Chem 270:3804–3808

    Article  CAS  PubMed  Google Scholar 

  • Xu W-H, Sato Y, Ikeda M, Yamashita O (1995b) Molecular characterization of the gene encoding the precursor protein of diapause hormone and pheromone biosynthesis activating neuropeptide (DH-PBAN) of the silkworm, Bombyx mori and its distribution in some insects. Biochim Biophys Acta Gene Struct Expr 1261:83–89

    Article  Google Scholar 

  • Yaginuma T, Niimi T (2015) FXPRLamide peptide family. In: handbook of hormones: comparative endocrinology for basic and. Clin Res:395

    Google Scholar 

  • Yamaoka R, Taniguchi Y, Hayashiya K (1984) Bombykol biosynthesis from deuterium-labeled (Z)-11-hexadecenoic acid. Experientia 40:80–81

    Article  CAS  Google Scholar 

  • Yang M, Wang W, Zhong M et al (2002) Lysine 270 in the third intracellular domain of the oxytocin receptor is an important determinant for G alpha(q) coupling specificity. Mol Endocrinol 16:814–823

    CAS  PubMed  Google Scholar 

  • Yew JY, Chung H (2015) Insect pheromones: an overview of function, form, and discovery. Prog Lipid Res 59:88–105

    Article  CAS  PubMed  Google Scholar 

  • Yokoyama N, Francke A, Tatsuki S et al (2003) Ultrastructural studies on the pheromone-producing cells in the silkmoth, Bombyx mori: formation of cytoplasmic lipid droplets before adult eclosion. Acta Biol Hung 54:299–311

    Article  CAS  PubMed  Google Scholar 

  • Yoshiga T, Okano K, Mita K et al (2000) cDNA cloning of acyl-CoA desaturase homologs in the silkworm, Bombyx mori. Gene 246:339–345

    Article  CAS  PubMed  Google Scholar 

  • Yoshiga T, Yokoyama N, Imai N et al (2002) cDNA cloning of calcineurin heterosubunits from the pheromone gland of the silkmoth, Bombyx mori. Insect Biochem Mol Biol 32:477–486

    Article  CAS  PubMed  Google Scholar 

  • Ždárek J, Nachman RJ, Hayes TK (1998) Structure-activity relationships of insect neuropeptides of the pyrokinin/PBAN family and their selective action on pupariation in fleshfly (Neobelleria bullata) larvae (Diptera:Sarcophagidae). Eur J Entomol 95:9–16

    Google Scholar 

  • Ždárek J, Verleyen P, Mares M et al (2004) Comparison of the effects of pyrokinins and related peptides identified from arthropods on pupariation behaviour in flesh fly (Sarcophaga bullata) larvae (Diptera: Sarcophagidae). J Insect Physiol 50:233–239

    Article  PubMed  CAS  Google Scholar 

  • Zhang Q, Denlinger DL (2012) Dynamics of diapause hormone and prothoracicotropic hormone transcript expression at diapause termination in pupae of the corn earworm, Helicoverpa zea. Peptides 34:120–126

    Article  CAS  PubMed  Google Scholar 

  • Zhang T-Y, Kang L, Zhang Z-F, Xu W-H (2004) Identification of a POU factor involved in regulating the neuron-specific expression of the gene encoding diapause hormone and pheromone biosynthesis-activating neuropeptide in Bombyx mori. Biochem J 380:255–263

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang T-Y, Sun J-S, Liu W-Y et al (2005) Structural characterization and transcriptional regulation of the gene encoding diapause hormone and pheromone biosynthesis activating neuropeptide in the cotton bollworm, Helicoverpa armigera. Biochim Biophys Acta 1728:44–52

    Article  CAS  PubMed  Google Scholar 

  • Zhang S, Li X, Bin Z et al (2013) Molecular identification of a pancreatic lipase-like gene involved in sex pheromone biosynthesis of Bombyx mori. Insect Sci 21:459–468

    Article  PubMed  CAS  Google Scholar 

  • Zhang S, Liu X, Zhu B et al (2014) Identification of differentially expressed genes in the pheromone glands of mated and virgin Bombyx mori by digital gene expression profiling. PLoS One 9:e111003

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang J, Walker WB, Wang G (2015) Pheromone reception in moths: from molecules to behaviors. Prog Mol Biol Trans Sci 130:109–128

    Article  CAS  Google Scholar 

  • Zhao C-H, Li Q, Gao W (2002) Stimulation of sex pheromone production by PBAN-like substance in the pine caterpillar moth, Dendrolimus punctatus (Lepidoptera: Lasiocampidae). Arch Insect Biochem Physiol 49:137–148

    Article  CAS  PubMed  Google Scholar 

  • Zhao W, Li L, Zhang Y et al (2018) Calcineurin is required for male sex pheromone biosynthesis and female acceptance. Insect Mol Biol 72:173–110

    Google Scholar 

  • Zheng L, Lytle C, Njauw C-N et al (2007) Cloning and characterization of the pheromone biosynthesis activating neuropeptide receptor gene in Spodoptera littoralis larvae. Gene 393:20–30

    Article  CAS  PubMed  Google Scholar 

  • Zmijewski MA, Slominski AT (2009) CRF1 receptor splicing in epidermal keratinocytes: potential biological role and environmental regulations. J Cell Physiol 218:593–602

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

We are grateful to Dr. József Fodor for critical reading of the text and insightful comments. We also thank Dr. Shogo Matsumoto (retired; RIKEN Advanced Science Institute) for his support of the Japan Society for the Promotion of Science which played a pivotal role in our respective careers. In addition, we thank the many members of the former Molecular Entomology Laboratory at the RIKEN Advanced Science Institute and the numerous colleagues and peers who have contributed to advancing our understanding of the cellular processes that govern biosynthesis of the pheromone that first piqued Butenstadt’s interest 60 years ago. Mention of trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the United States Department of Agriculture (USDA). USDA is an equal opportunity provider and employer.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to J. Joe Hull .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2020 Springer Nature Singapore Pte Ltd.

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Hull, J.J., Fónagy, A. (2020). A Sexy Moth Model – The Molecular Basis of Sex Pheromone Biosynthesis in the Silkmoth Bombyx mori. In: Ishikawa, Y. (eds) Insect Sex Pheromone Research and Beyond. Entomology Monographs. Springer, Singapore. https://doi.org/10.1007/978-981-15-3082-1_6

Download citation

Publish with us

Policies and ethics