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Evolutionarily Conserved, Multitasking TRP Channels: Lessons from Worms and Flies

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Mammalian Transient Receptor Potential (TRP) Cation Channels

Part of the book series: Handbook of Experimental Pharmacology ((HEP,volume 223))

Abstract

The Transient Receptor Potential (TRP) channel family is comprised of a large group of cation-permeable channels, which display an extraordinary diversity of roles in sensory signaling. TRPs allow animals to detect chemicals, mechanical force, light, and changes in temperature. Consequently, these channels control a plethora of animal behaviors. Moreover, their functions are not limited to the classical senses, as they are cellular sensors, which are critical for ionic homeostasis and metabolism. Two genetically tractable invertebrate model organisms, Caenorhabditis elegans and Drosophila melanogaster, have led the way in revealing a wide array of sensory roles and behaviors that depend on TRP channels. Two overriding themes have emerged from these studies. First, TRPs are multitasking proteins, and second, many functions and modes of activation of these channels are evolutionarily conserved, including some that were formerly thought to be unique to invertebrates, such as phototransduction. Thus, worms and flies offer the potential to decipher roles for mammalian TRPs, which would otherwise not be suspected.

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References

  • Acharya JK, Jalink K, Hardy RW, Hartenstein V, Zuker CS (1997) InsP3 receptor essential for growth and differentiation but not for vision in Drosophila. Neuron 18:881–887

    CAS  PubMed  Google Scholar 

  • Al-Anzi B, Tracey WD Jr, Benzer S (2006) Response of Drosophila to wasabi is mediated by painless, the fly homolog of mammalian TRPA1/ANKTM1. Curr Biol 16:1034–1040

    CAS  PubMed  Google Scholar 

  • Al-Anzi B, Sapin V, Waters C, Zinn K, Wyman RJ, Benzer S (2009) Obesity-blocking neurons in Drosophila. Neuron 63:329–341

    CAS  PubMed Central  PubMed  Google Scholar 

  • Allada R, Chung BY (2010) Circadian organization of behavior and physiology in Drosophila. Annu Rev Physiol 72:605–624

    CAS  PubMed Central  PubMed  Google Scholar 

  • Badsha F, Kain P, Prabhakar S, Sundaram S, Padinjat R, Rodrigues V, Hasan G (2012) Mutants in Drosophila TRPC channels reduce olfactory sensitivity to carbon dioxide. PLoS One 7:e49848

    CAS  PubMed Central  PubMed  Google Scholar 

  • Bandell M, Story GM, Hwang SW, Viswanath V, Eid SR, Petrus MJ, Earley TJ, Patapoutian A (2004) Noxious cold ion channel TRPA1 is activated by pungent compounds and bradykinin. Neuron 41:849–857

    CAS  PubMed  Google Scholar 

  • Bargal R, Avidan N, Ben-Asher E, Olender Z, Zeigler M, Frumkin A, Raas-Rothschild A, Glusman G, Lancet D, Bach G (2000) Identification of the gene causing mucolipidosis type IV. Nat Genet 26:118–123

    CAS  PubMed  Google Scholar 

  • Barr MM, Sternberg PW (1999) A polycystic kidney-disease gene homologue required for male mating behaviour in C. elegans. Nature 401:386–389

    CAS  PubMed  Google Scholar 

  • Barr MM, DeModena J, Braun D, Nguyen CQ, Hall DH, Sternberg PW (2001) The Caenorhabditis elegans autosomal dominant polycystic kidney disease gene homologs lov-1 and pkd-2 act in the same pathway. Curr Biol 11:1341–1346

    CAS  PubMed  Google Scholar 

  • Bassi MT, Manzoni M, Monti E, Pizzo MT, Ballabio A, Borsani G (2000) Cloning of the gene encoding a novel integral membrane protein, mucolipidin-and identification of the two major founder mutations causing mucolipidosis type IV. Am J Hum Genet 67:1110–1120

    CAS  PubMed Central  PubMed  Google Scholar 

  • Benton R, Vannice KS, Gomez-Diaz C, Vosshall LB (2009) Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila. Cell 136:149–162

    CAS  PubMed Central  PubMed  Google Scholar 

  • Berson DM, Dunn FA, Takao M (2002) Phototransduction by retinal ganglion cells that set the circadian clock. Science 295:1070–1073

    CAS  PubMed  Google Scholar 

  • Bloomquist BT, Shortridge RD, Schneuwly S, Perdew M, Montell C, Steller H, Rubin G, Pak WL (1988) Isolation of a putative phospholipase C gene of Drosophila, norpA, and its role in phototransduction. Cell 54:723–733

    CAS  PubMed  Google Scholar 

  • Caterina MJ (2007) Transient receptor potential ion channels as participants in thermosensation and thermoregulation. Am J Physiol Regul Integr Comp Physiol 292:R64–R76

    CAS  PubMed  Google Scholar 

  • Caterina MJ, Rosen TA, Tominaga M, Brake AJ, Julius D (1999) A capsaicin-receptor homologue with a high threshold for noxious heat. Nature 398:436–441

    CAS  PubMed  Google Scholar 

  • Cheng LE, Song W, Looger LL, Jan LY, Jan YN (2010) The role of the TRP channel NompC in Drosophila larval and adult locomotion. Neuron 67:373–380

    CAS  PubMed Central  PubMed  Google Scholar 

  • Christensen AP, Corey DP (2007) TRP channels in mechanosensation: direct or indirect activation? Nat Rev Neurosci 8:510–521

    CAS  PubMed  Google Scholar 

  • Chyb S, Raghu P, Hardie RC (1999) Polyunsaturated fatty acids activate the Drosophila light-sensitive channels TRP and TRPL. Nature 397:255–259

    CAS  PubMed  Google Scholar 

  • Clyne PJ, Warr CG, Freeman MR, Lessing D, Kim J, Carlson JR (1999) A novel family of divergent seven-transmembrane proteins: candidate odorant receptors in Drosophila. Neuron 22:327–338

    CAS  PubMed  Google Scholar 

  • Colbert HA, Smith TL, Bargmann CI (1997) OSM-9, a novel protein with structural similarity to channels, is required for olfaction, mechanosensation, and olfactory adaptation in Caenorhabditis elegans. J Neurosci 17:8259–8269

    CAS  PubMed  Google Scholar 

  • Conti B (2008) Considerations on temperature, longevity and aging. Cell Mol Life Sci 65:1626–1630

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cosens DJ, Manning A (1969) Abnormal electroretinogram from a Drosophila mutant. Nature 224:285–287

    CAS  PubMed  Google Scholar 

  • Darszon A, Sanchez-Cardenas C, Orta G, Sanchez-Tusie AA, Beltran C, Lopez-Gonzalez I, Granados-Gonzalez G, Trevino CL (2012) Are TRP channels involved in sperm development and function? Cell Tissue Res 349:749–764

    CAS  PubMed  Google Scholar 

  • de Bono M, Bargmann CI (1998) Natural variation in a neuropeptide Y receptor homolog modifies social behavior and food response in C. elegans. Cell 94:679–689

    PubMed  Google Scholar 

  • de Bono M, Tobin DM, Davis MW, Avery L, Bargmann CI (2002) Social feeding in Caenorhabditis elegans is induced by neurons that detect aversive stimuli. Nature 419:899–903

    PubMed Central  PubMed  Google Scholar 

  • Dhaka A, Viswanath V, Patapoutian A (2006) TRP ion channels and temperature sensation. Annu Rev Neurosci 29:135–161

    CAS  PubMed  Google Scholar 

  • Dong XP, Shen D, Wang X, Dawson T, Li X, Zhang Q, Cheng X, Zhang Y, Weisman LS, Delling M, Xu H (2010) PI(3,5)P2 controls membrane traffic by direct activation of mucolipin Ca2+ release channels in the endolysosome. Nat Commun 1:38. doi:10.1038/ncomms1037

    PubMed Central  PubMed  Google Scholar 

  • Dwoskin LP, Crooks PA, Teng L, Green TA, Bardo MT (1999) Acute and chronic effects of nornicotine on locomotor activity in rats: altered response to nicotine. Psychopharmacology (Berlin) 145:442–451

    CAS  Google Scholar 

  • Eberl DF, Hardy RW, Kernan MJ (2000) Genetically similar transduction mechanisms for touch and hearing in Drosophila. J Neurosci 20:5981–5988

    CAS  PubMed  Google Scholar 

  • Effertz T, Wiek R, Gopfert MC (2011) NompC TRP channel is essential for Drosophila sound receptor function. Curr Biol 21:592–597

    CAS  PubMed  Google Scholar 

  • Effertz T, Nadrowski B, Piepenbrock D, Albert JT, Gopfert MC (2012) Direct gating and mechanical integrity of Drosophila auditory transducers require TRPN1. Nat Neurosci 15:1198–1200

    CAS  PubMed  Google Scholar 

  • Fares H, Greenwald I (2001) Regulation of endocytosis by CUP-5, the Caenorhabditis elegans mucolipin-1 homolog. Nat Genet 28:64–68

    CAS  PubMed  Google Scholar 

  • Feng Z, Li W, Ward A, Piggott BJ, Larkspur ER, Sternberg PW, Xu XZ (2006) A C. elegans model of nicotine-dependent behavior: regulation by TRP-family channels. Cell 127:621–633

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fowler MA, Montell C (2013) Drosophila TRP channels and animal behavior. Life Sci 92:394–403

    CAS  PubMed Central  PubMed  Google Scholar 

  • Fu Y, Yau KW (2007) Phototransduction in mouse rods and cones. Pflugers Arch 454:805–819

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gallagher AR, Germino GG, Somlo S (2010) Molecular advances in autosomal dominant polycystic kidney disease. Adv Chronic Kidney Dis 17:118–130

    PubMed Central  PubMed  Google Scholar 

  • Gallio M, Ofstad TA, Macpherson LJ, Wang JW, Zuker CS (2011) The coding of temperature in the Drosophila brain. Cell 144:614–624

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gao Q, Chess A (1999) Identification of candidate Drosophila olfactory receptors from genomic DNA sequence. Genomics 60:31–39

    CAS  PubMed  Google Scholar 

  • Gao Z, Ruden DM, Lu X (2003) PKD2 cation channel is required for directional sperm movement and male fertility. Curr Biol 13:2175–2178

    CAS  PubMed  Google Scholar 

  • Georgiev P, Okkenhaug H, Drews A, Wright D, Lambert S, Flick M, Carta V, Martel C, Oberwinkler J, Raghu P (2010) TRPM channels mediate zinc homeostasis and cellular growth during Drosophila larval development. Cell Metab 12:386–397

    CAS  PubMed  Google Scholar 

  • Glaser FT, Stanewsky R (2007) Synchronization of the Drosophila circadian clock by temperature cycles. Cold Spring Harb Symp Quant Biol 72:233–242

    CAS  PubMed  Google Scholar 

  • Glauser DA, Chen WC, Agin R, Macinnis BL, Hellman AB, Garrity PA, Tan MW, Goodman MB (2011) Heat avoidance is regulated by transient receptor potential (TRP) channels and a neuropeptide signaling pathway in Caenorhabditis elegans. Genetics 188:91–103

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gong Z, Son W, Chung YD, Kim J, Shin DW, McClung CA, Lee Y, Lee HW, Chang DJ, Kaang BK, Cho H, Oh U, Hirsh J, Kernan MJ, Kim C (2004) Two interdependent TRPV channel subunits, Inactive and Nanchung, mediate hearing in Drosophila. J Neurosci 24:9059–9066

    CAS  PubMed  Google Scholar 

  • Göpfert MC, Albert JT, Nadrowski B, Kamikouchi A (2006) Specification of auditory sensitivity by Drosophila TRP channels. Nat Neurosci 9:999–1000

    PubMed  Google Scholar 

  • Gracheva EO, Ingolia NT, Kelly YM, Cordero-Morales JF, Hollopeter G, Chesler AT, Sanchez EE, Perez JC, Weissman JS, Julius D (2010) Molecular basis of infrared detection by snakes. Nature 464:1006–1011

    CAS  PubMed Central  PubMed  Google Scholar 

  • Gruninger TR, LeBoeuf B, Liu Y, Garcia LR (2007) Molecular signaling involved in regulating feeding and other motivated behaviors. Mol Neurobiol 35:1–20

    CAS  PubMed  Google Scholar 

  • Hamada FN, Rosenzweig M, Kang K, Pulver SR, Ghezzi A, Jegla TJ, Garrity PA (2008) An internal thermal sensor controlling temperature preference in Drosophila. Nature 454:217–220

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hardie RC, Franze K (2012) Photomechanical responses in Drosophila photoreceptors. Science 338:260–263

    CAS  PubMed  Google Scholar 

  • Hardie RC, Minke B (1992) The trp gene is essential for a light-activated Ca2+ channel in Drosophila photoreceptors. Neuron 8:643–651

    CAS  PubMed  Google Scholar 

  • Hardin PE (2011) Molecular genetic analysis of circadian timekeeping in Drosophila. Adv Genet 74:141–173

    CAS  PubMed  Google Scholar 

  • Harteneck C, Obukhov AG, Zobel A, Kalkbrenner F, Schultz G (1995) The Drosophila cation channel trpl expressed in Sf9 cells is stimulated by agonists of G-protein-coupled receptors. FEBS Lett 358:297–300

    CAS  PubMed  Google Scholar 

  • Hersh BM, Hartwieg E, Horvitz HR (2002) The Caenorhabditis elegans mucolipin-like gene cup-5 is essential for viability and regulates lysosomes in multiple cell types. Proc Natl Acad Sci U S A 99:4355–4360

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hilliard MA, Bergamasco C, Arbucci S, Plasterk RH, Bazzicalupo P (2004) Worms taste bitter: ASH neurons, QUI-1, GPA-3 and ODR-3 mediate quinine avoidance in Caenorhabditis elegans. EMBO J 23:1101–1111

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hinman A, Chuang HH, Bautista DM, Julius D (2006) TRP channel activation by reversible covalent modification. Proc Natl Acad Sci U S A 103:19564–19568

    CAS  PubMed Central  PubMed  Google Scholar 

  • Hofmann T, Chubanov V, Chen X, Dietz AS, Gudermann T, Montell C (2010) Drosophila TRPM channel is essential for the control of extracellular magnesium levels. PLoS One 5:e10519

    PubMed Central  PubMed  Google Scholar 

  • Howard J, Bechstedt S (2004) Hypothesis: a helix of ankyrin repeats of the NOMPC-TRP ion channel is the gating spring of mechanoreceptors. Curr Biol 14:R224–R226

    CAS  PubMed  Google Scholar 

  • Hu Y, Vaca L, Zhu X, Birnbaumer L, Kunze DL, Schilling WP (1994) Appearance of a novel Ca2+ influx pathway in Sf9 insect cells following expression of the transient potential-like (trpl) protein of Drosophila. Biochem Biophys Res Commun 201:1050–1056

    CAS  PubMed  Google Scholar 

  • Huang J, Liu CH, Hughes SA, Postma M, Schwiening CJ, Hardie RC (2010) Activation of TRP channels by protons and phosphoinositide depletion in Drosophila photoreceptors. Curr Biol 20:189–197

    CAS  PubMed  Google Scholar 

  • Hwang RY, Stearns NA, Tracey WD (2012) The ankyrin repeat domain of the TRPA protein Painless is important for thermal nociception but not mechanical nociception. PLoS One 7:e30090

    CAS  PubMed Central  PubMed  Google Scholar 

  • Inoue H, Yoshioka T, Hotta Y (1985) A genetic study of inositol trisphosphate involvement in phototransduction using Drosophila mutants. Biochem Biophys Res Commun 132:513–519

    CAS  PubMed  Google Scholar 

  • Johnson WA, Carder JW (2012) Drosophila nociceptors mediate larval aversion to dry surface environments utilizing both the Painless TRP channel and the DEG/ENaC subunit, PPK1. PLoS One 7:e32878

    CAS  PubMed Central  PubMed  Google Scholar 

  • Jordt SE, Bautista DM, Chuang HH, McKemy DD, Zygmunt PM, Hogestätt ED, Meng ID, Julius D (2004) Mustard oils and cannabinoids excite sensory nerve fibres through the TRP channel ANKTM1. Nature 427:260–265

    CAS  PubMed  Google Scholar 

  • Jungnickel MK, Marrero H, Birnbaumer L, Lemos JR, Florman HM (2001) Trp2 regulates entry of Ca2+ into mouse sperm triggered by egg ZP3. Nat Cell Biol 3:499–502

    CAS  PubMed  Google Scholar 

  • Kahn-Kirby AH, Bargmann CI (2006) TRP channels in C. elegans. Annu Rev Physiol 68:719–736

    CAS  PubMed  Google Scholar 

  • Kamikouchi A (2013) Auditory neuroscience in fruit flies. Neurosci Res 76:113–118

    PubMed  Google Scholar 

  • Kamikouchi A, Inagaki HK, Effertz T, Hendrich O, Fiala A, Gopfert MC, Ito K (2009) The neural basis of Drosophila gravity-sensing and hearing. Nature 458:165–171

    CAS  PubMed  Google Scholar 

  • Kang K, Pulver SR, Panzano VC, Chang EC, Griffith LC, Theobald DL, Garrity PA (2010a) Analysis of Drosophila TRPA1 reveals an ancient origin for human chemical nociception. Nature 464:597–600

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kang L, Gao J, Schafer WR, Xie Z, Xu XZ (2010b) C. elegans TRP family protein TRP-4 is a pore-forming subunit of a native mechanotransduction channel. Neuron 67:381–391

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kang K, Panzano VC, Chang EC, Ni L, Dainis AM, Jenkins AM, Regna K, Muskavitch MA, Garrity PA (2012) Modulation of TRPA1 thermal sensitivity enables sensory discrimination in Drosophila. Nature 481:76–80

    CAS  Google Scholar 

  • Karashima Y, Talavera K, Everaerts W, Janssens A, Kwan KY, Vennekens R, Nilius B, Voets T (2009) TRPA1 acts as a cold sensor in vitro and in vivo. Proc Natl Acad Sci U S A 106:1273–1278

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kernan MJ (2007) Mechanotransduction and auditory transduction in Drosophila. Pflugers Arch 454:703–720

    CAS  PubMed  Google Scholar 

  • Kim J, Chung YD, Park DY, Choi S, Shin DW, Soh H, Lee HW, Son W, Yim J, Park CS, Kernan MJ, Kim C (2003) A TRPV family ion channel required for hearing in Drosophila. Nature 424:81–84

    CAS  PubMed  Google Scholar 

  • Kim SH, Lee Y, Akitake B, Woodward OM, Guggino WB, Montell C (2010) Drosophila TRPA1 channel mediates chemical avoidance in gustatory receptor neurons. Proc Natl Acad Sci U S A 107:8440–8445

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kindt KS, Viswanath V, Macpherson L, Quast K, Hu H, Patapoutian A, Schafer WR (2007) Caenorhabditis elegans TRPA-1 functions in mechanosensation. Nat Neurosci 10:568–577

    CAS  PubMed  Google Scholar 

  • Köttgen M, Hofherr A, Li W, Chu K, Cook S, Montell C, Watnick T (2011) Drosophila sperm swim backwards in the female reproductive tract and are activated via TRPP2 ion channels. PLoS One 6:e20031

    PubMed Central  PubMed  Google Scholar 

  • Kwan KY, Allchorne AJ, Vollrath MA, Christensen AP, Zhang DS, Woolf CJ, Corey DP (2006) TRPA1 contributes to cold, mechanical, and chemical nociception but is not essential for hair-cell transduction. Neuron 50:277–289

    CAS  PubMed  Google Scholar 

  • Kwon Y, Shim HS, Wang X, Montell C (2008) Control of thermotactic behavior via coupling of a TRP channel to a phospholipase C signaling cascade. Nat Neurosci 11:871–873

    CAS  PubMed  Google Scholar 

  • Kwon Y, Kim SH, Ronderos DS, Lee Y, Akitake B, Woodward OM, Guggino WB, Smith DP, Montell C (2010a) Drosophila TRPA1 channel is required to avoid the naturally occurring insect repellent citronellal. Curr Biol 20:1672–1678

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kwon Y, Shen WL, Shim HS, Montell C (2010b) Fine thermotactic discrimination between the optimal and slightly cooler temperatures via a TRPV channel in chordotonal neurons. J Neurosci 30:10465–10471

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kwon I, Choe HK, Son GH, Kim K (2011) Mammalian molecular clocks. Exp Neurobiol 20:18–28

    PubMed Central  PubMed  Google Scholar 

  • Lee BH, Ashrafi K (2008) A TRPV channel modulates C. elegans neurosecretion, larval starvation survival, and adult lifespan. PLoS Genet 4:e1000213

    PubMed Central  PubMed  Google Scholar 

  • Lee Y, Montell C (2013) Drosophila TRPA1 functions in temperature control of circadian rhythm in pacemaker neurons. J Neurosci 33:6716–6725

    CAS  PubMed Central  PubMed  Google Scholar 

  • Lee Y, Lee Y, Lee J, Bang S, Hyun S, Kang J, Hong ST, Bae E, Kaang BK, Kim J (2005) Pyrexia is a new thermal transient receptor potential channel endowing tolerance to high temperatures in Drosophila melanogaster. Nat Genet 37:305–310

    CAS  PubMed  Google Scholar 

  • Lehnert BP, Baker AE, Gaudry Q, Chiang AS, Wilson RI (2013) Distinct roles of TRP channels in auditory transduction and amplification in Drosophila. Neuron 77:115–128

    CAS  PubMed  Google Scholar 

  • Li W, Feng Z, Sternberg PW, Xu XZ (2006) A C. elegans stretch receptor neuron revealed by a mechanosensitive TRP channel homologue. Nature 440:684–687

    CAS  PubMed Central  PubMed  Google Scholar 

  • Liu KS, Sternberg PW (1995) Sensory regulation of male mating behavior in Caenorhabditis elegans. Neuron 14:79–89

    CAS  PubMed  Google Scholar 

  • Liu CH, Wang T, Postma M, Obukhov AG, Montell C, Hardie RC (2007a) In vivo identification and manipulation of the Ca2+ selectivity filter in the Drosophila transient receptor potential channel. J Neurosci 27:604–615

    CAS  PubMed  Google Scholar 

  • Liu L, Li Y, Wang R, Yin C, Dong Q, Hing H, Kim C, Welsh MJ (2007b) Drosophila hygrosensation requires the TRP channels water witch and nanchung. Nature 450:294–298

    CAS  PubMed  Google Scholar 

  • Liu J, Ward A, Gao J, Dong Y, Nishio N, Inada H, Kang L, Yu Y, Ma D, Xu T, Mori I, Xie Z, Xu XZ (2010) C. elegans phototransduction requires a G protein-dependent cGMP pathway and a taste receptor homolog. Nat Neurosci 13:715–722

    CAS  PubMed Central  PubMed  Google Scholar 

  • Macpherson LJ, Dubin AE, Evans MJ, Marr F, Schultz PG, Cravatt BF, Patapoutian A (2007) Noxious compounds activate TRPA1 ion channels through covalent modification of cysteines. Nature 445:541–545

    CAS  PubMed  Google Scholar 

  • Magalhaes CP, de Freitas MF, Nogueira MI, Campina RC, Takase LF, de Souza SL, de Castro RM (2010) Modulatory role of serotonin on feeding behavior. Nutr Neurosci 13:246–255

    CAS  PubMed  Google Scholar 

  • Matsuura H, Sokabe T, Kohno K, Tominaga M, Kadowaki T (2009) Evolutionary conservation and changes in insect TRP channels. BMC Evol Biol 9:228

    PubMed Central  PubMed  Google Scholar 

  • Montell C (2001) Physiology, phylogeny and functions of the TRP superfamily of cation channels. Sci STKE 2001(90):re1

    CAS  PubMed  Google Scholar 

  • Montell C (2005) The TRP superfamily of cation channels. Sci STKE 2005(272):re3

    PubMed  Google Scholar 

  • Montell C (2009) A taste of the Drosophila gustatory receptors. Curr Opin Neurobiol 19:345–353

    CAS  PubMed Central  PubMed  Google Scholar 

  • Montell C (2011) The history of TRP channels, a commentary and reflection. Pflugers Arch 461:499–506

    CAS  PubMed  Google Scholar 

  • Montell C, Rubin GM (1989) Molecular characterization of the Drosophila trp locus: a putative integral membrane protein required for phototransduction. Neuron 2:1313–1323

    CAS  PubMed  Google Scholar 

  • Neckameyer WS (2010) A trophic role for serotonin in the development of a simple feeding circuit. Dev Neurosci 32:217–237

    CAS  PubMed  Google Scholar 

  • Neely GG, Keene AC, Duchek P, Chang EC, Wang QP, Aksoy YA, Rosenzweig M, Costigan M, Woolf CJ, Garrity PA, Penninger JM (2011) TrpA1 regulates thermal nociception in Drosophila. PLoS One 6:e24343

    CAS  PubMed Central  PubMed  Google Scholar 

  • Niemeyer BA, Suzuki E, Scott K, Jalink K, Zuker CS (1996) The Drosophila light-activated conductance is composed of the two channels TRP and TRPL. Cell 85:651–659

    CAS  PubMed  Google Scholar 

  • Pérez CA, Huang L, Rong M, Kozak JA, Preuss AK, Zhang H, Max M, Margolskee RF (2002) A transient receptor potential channel expressed in taste receptor cells. Nat Neurosci 5:1169–1176

    PubMed  Google Scholar 

  • Peschel N, Helfrich-Förster C (2011) Setting the clock–by nature: circadian rhythm in the fruitfly Drosophila melanogaster. FEBS Lett 585:1435–1442

    CAS  PubMed  Google Scholar 

  • Petersen LK, Stowers RS (2011) A Gateway MultiSite recombination cloning toolkit. PLoS One 6:e24531

    CAS  PubMed Central  PubMed  Google Scholar 

  • Phillips AM, Bull A, Kelly LE (1992) Identification of a Drosophila gene encoding a calmodulin-binding protein with homology to the trp phototransduction gene. Neuron 8:631–642

    CAS  PubMed  Google Scholar 

  • Provencio I, Rodriguez IR, Jiang G, Hayes WP, Moreira EF, Rollag MD (2000) A novel human opsin in the inner retina. J Neurosci 20:600–605

    CAS  PubMed  Google Scholar 

  • Raghu P, Colley NJ, Webel R, James T, Hasan G, Danin M, Selinger Z, Hardie RC (2000) Normal phototransduction in Drosophila photoreceptors lacking an InsP3 receptor gene. Mol Cell Neurosci 15:429–445

    CAS  PubMed  Google Scholar 

  • Reppert SM, Weaver DR (2002) Coordination of circadian timing in mammals. Nature 418:935–941

    CAS  PubMed  Google Scholar 

  • Robertson HM, Warr CG, Carlson JR (2003) Molecular evolution of the insect chemoreceptor gene superfamily in Drosophila melanogaster. Proc Natl Acad Sci U S A 100(Suppl 2):14537–14542

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rogers C, Persson A, Cheung B, de Bono M (2006) Behavioral motifs and neural pathways coordinating O2 responses and aggregation in C. elegans. Curr Biol 16:649–659

    CAS  PubMed  Google Scholar 

  • Rosenzweig M, Brenman KM, Taylor TD, Phelps P, Patapoutian A, Garrity PA (2005) The Drosophila ortholog of vertebrate TRPA1 regulates thermotaxis. Genes Dev 19:419–424

    CAS  PubMed Central  PubMed  Google Scholar 

  • Rosenzweig M, Kang K, Garrity PA (2008) Distinct TRP channels are required for warm and cool avoidance in Drosophila melanogaster. Proc Natl Acad Sci U S A 105:14668–14673

    CAS  PubMed Central  PubMed  Google Scholar 

  • Saito S, Fukuta N, Shingai R, Tominaga M (2011) Evolution of vertebrate transient receptor potential vanilloid 3 channels: opposite temperature sensitivity between mammals and western clawed frogs. PLoS Genet 7:e1002041

    CAS  PubMed Central  PubMed  Google Scholar 

  • Saito S, Nakatsuka K, Takahashi K, Fukuta N, Imagawa T, Ohta T, Tominaga M (2012) Analysis of transient receptor potential ankyrin 1 (TRPA1) in frogs and lizards illuminates both nociceptive heat and chemical sensitivities and coexpression with TRP vanilloid 1 (TRPV1) in ancestral vertebrates. J Biol Chem 287:30743–30754

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sakai T, Kasuya J, Kitamoto T, Aigaki T (2009) The Drosophila TRPA channel, Painless, regulates sexual receptivity in virgin females. Genes Brain Behav 8:546–557

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sayeed O, Benzer S (1996) Behavioral genetics of thermosensation and hygrosensation in Drosophila. Proc Natl Acad Sci U S A 93:6079–6084

    CAS  PubMed Central  PubMed  Google Scholar 

  • Schaheen L, Dang H, Fares H (2006) Basis of lethality in C. elegans lacking CUP-5, the Mucolipidosis Type IV orthologue. Dev Biol 293:382–391

    PubMed  Google Scholar 

  • Schlingmann KP, Weber S, Peters M, Niemann Nejsum L, Vitzthum H, Klingel K, Kratz M, Haddad E, Ristoff E, Dinour D, Syrrou M, Nielsen S, Sassen M, Waldegger S, Seyberth HW, Konrad M (2002) Hypomagnesemia with secondary hypocalcemia is caused by mutations in TRPM6, a new member of the TRPM gene family. Nat Genet 31:166–170

    CAS  PubMed  Google Scholar 

  • Schmidt TM, Chen SK, Hattar S (2011) Intrinsically photosensitive retinal ganglion cells: many subtypes, diverse functions. Trends Neurosci 34:572–580

    CAS  PubMed Central  PubMed  Google Scholar 

  • Senatore S, Rami Reddy V, Semeriva M, Perrin L, Lalevee N (2010) Response to mechanical stress is mediated by the TRPA channel painless in the Drosophila heart. PLoS Genet 6:e1001088

    PubMed Central  PubMed  Google Scholar 

  • Sharif-Naeini R, Dedman A, Folgering JH, Duprat F, Patel A, Nilius B, Honore E (2008) TRP channels and mechanosensory transduction: insights into the arterial myogenic response. Pflugers Arch 456:529–540

    CAS  PubMed  Google Scholar 

  • Shen WL, Kwon Y, Adegbola AA, Luo J, Chess A, Montell C (2011) Function of rhodopsin in temperature discrimination in Drosophila. Science 331:1333–1336

    CAS  PubMed  Google Scholar 

  • Sidi S, Friedrich RW, Nicolson T (2003) NompC TRP channel required for vertebrate sensory hair cell mechanotransduction. Science 301:96–99

    CAS  PubMed  Google Scholar 

  • Silvert DJ, Doctor J, Quesada L, Fristrom JW (1984) Pupal and larval cuticle proteins of Drosophila melanogaster. Biochemistry 23:5767–5774

    CAS  PubMed  Google Scholar 

  • Sokabe T, Tsujiuchi S, Kadowaki T, Tominaga M (2008) Drosophila Painless is a Ca2+-requiring channel activated by noxious heat. J Neurosci 28:9929–9938

    CAS  PubMed  Google Scholar 

  • Sokolchik I, Tanabe T, Baldi PF, Sze JY (2005) Polymodal sensory function of the Caenorhabditis elegans OCR-2 channel arises from distinct intrinsic determinants within the protein and is selectively conserved in mammalian TRPV proteins. J Neurosci 25:1015–1023

    CAS  PubMed  Google Scholar 

  • Sprecher SG, Desplan C (2008) Switch of rhodopsin expression in terminally differentiated Drosophila sensory neurons. Nature 454:533–537

    CAS  PubMed Central  PubMed  Google Scholar 

  • Stanley BG, Leibowitz SF, Eppel N, St-Pierre S, Hoebel BG (1985) Suppression of norepinephrine-elicited feeding by neurotensin: evidence for behavioral, anatomical and pharmacological specificity. Brain Res 343:297–304

    CAS  PubMed  Google Scholar 

  • Störtkuhl KF, Hovemann BT, Carlson JR (1999) Olfactory adaptation depends on the Trp Ca2+ channel in Drosophila. J Neurosci 19:4839–4846

    PubMed  Google Scholar 

  • Story GM, Peier AM, Reeve AJ, Eid SR, Mosbacher J, Hricik TR, Earley TJ, Hergarden AC, Andersson DA, Hwang SW, McIntyre P, Jegla T, Bevan S, Patapoutian A (2003) ANKTM1, a TRP-like channel expressed in nociceptive neurons, is activated by cold temperatures. Cell 112:819–829

    CAS  PubMed  Google Scholar 

  • Sun M, Goldin E, Stahl S, Falardeau JL, Kennedy JC, Acierno JS Jr, Bove C, Kaneski CR, Nagle J, Bromley MC, Colman M, Schiffmann R, Slaugenhaupt SA (2000) Mucolipidosis type IV is caused by mutations in a gene encoding a novel transient receptor potential channel. Hum Mol Genet 9:2471–2478

    CAS  PubMed  Google Scholar 

  • Sun Y, Liu L, Ben-Shahar Y, Jacobs JS, Eberl DF, Welsh MJ (2009) TRPA channels distinguish gravity sensing from hearing in Johnston’s organ. Proc Natl Acad Sci U S A 106:13606–13611

    CAS  PubMed Central  PubMed  Google Scholar 

  • Sze JY, Victor M, Loer C, Shi Y, Ruvkun G (2000) Food and metabolic signalling defects in a Caenorhabditis elegans serotonin-synthesis mutant. Nature 403:560–564

    CAS  PubMed  Google Scholar 

  • Takahashi N, Kuwaki T, Kiyonaka S, Numata T, Kozai D, Mizuno Y, Yamamoto S, Naito S, Knevels E, Carmeliet P, Oga T, Kaneko S, Suga S, Nokami T, Yoshida J, Mori Y (2011) TRPA1 underlies a sensing mechanism for O2. Nat Chem Biol 7:701–711

    CAS  PubMed  Google Scholar 

  • Talavera K, Gees M, Karashima Y, Meseguer VM, Vanoirbeek JA, Damann N, Everaerts W, Benoit M, Janssens A, Vennekens R, Viana F, Nemery B, Nilius B, Voets T (2009) Nicotine activates the chemosensory cation channel TRPA1. Nat Neurosci 12:1293–1299

    CAS  PubMed  Google Scholar 

  • Teramoto T, Lambie EJ, Iwasaki K (2005) Differential regulation of TRPM channels governs electrolyte homeostasis in the C. elegans intestine. Cell Metab 1:343–354

    CAS  PubMed Central  PubMed  Google Scholar 

  • Teramoto T, Sternick LA, Kage-Nakadai E, Sajjadi S, Siembida J, Mitani S, Iwasaki K, Lambie EJ (2010) Magnesium excretion in C. elegans requires the activity of the GTL-2 TRPM channel. PLoS One 5:e9589

    PubMed Central  PubMed  Google Scholar 

  • Tobin D, Madsen D, Kahn-Kirby A, Peckol E, Moulder G, Barstead R, Maricq A, Bargmann C (2002) Combinatorial expression of TRPV channel proteins defines their sensory functions and subcellular localization in C. elegans neurons. Neuron 35:307–318

    CAS  PubMed  Google Scholar 

  • Tomaszuk A, Simpson C, Williams G (1996) Neuropeptide Y, the hypothalamus and the regulation of energy homeostasis. Horm Res 46:53–58

    CAS  PubMed  Google Scholar 

  • Tracey WD, Wilson RI, Laurent G, Benzer S (2003) painless, a Drosophila gene essential for nociception. Cell 113:261–273

    CAS  PubMed  Google Scholar 

  • Treusch S, Knuth S, Slaugenhaupt SA, Goldin E, Grant BD, Fares H (2004) Caenorhabditis elegans functional orthologue of human protein h-mucolipin-1 is required for lysosome biogenesis. Proc Natl Acad Sci U S A 101:4483–4488

    CAS  PubMed Central  PubMed  Google Scholar 

  • Tsubouchi A, Caldwell JC, Tracey WD (2012) Dendritic filopodia, Ripped Pocket, NOMPC, and NMDARs contribute to the sense of touch in Drosophila larvae. Curr Biol 22:2124–2134

    CAS  PubMed Central  PubMed  Google Scholar 

  • Vaca L, Sinkins WG, Hu Y, Kunze DL, Schilling WP (1994) Activation of recombinant trp by thapsigargin in Sf9 insect cells. Am J Physiol 266:C1501–C1505

    Google Scholar 

  • Venkatachalam K, Montell C (2007) TRP channels. Annu Rev Biochem 76:387–417

    CAS  PubMed  Google Scholar 

  • Venkatachalam K, Long A, Elsaesser R, Nikolaeva D, Broadie K, Montell C (2008) Motor deficit in a Drosophila model of mucolipidosis type IV due to defective clearance of apoptotic cells. Cell 135:838–851

    CAS  PubMed Central  PubMed  Google Scholar 

  • Venkatachalam K, Wong CO, Montell C (2013) Feast or famine: role of TRPML in preventing cellular amino acid starvation. Autophagy 9:98–100

    CAS  PubMed Central  PubMed  Google Scholar 

  • Viswanath V, Story GM, Peier AM, Petrus MJ, Lee VM, Hwang SW, Patapoutian A, Jegla T (2003) Opposite thermosensor in fruitfly and mouse. Nature 423:822–823

    CAS  PubMed  Google Scholar 

  • Vosshall LB, Stocker RF (2007) Molecular architecture of smell and taste in Drosophila. Annu Rev Neurosci 30:505–533

    CAS  PubMed  Google Scholar 

  • Vosshall LB, Amrein H, Morozov PS, Rzhetsky A, Axel R (1999) A spatial map of olfactory receptor expression in the Drosophila antenna. Cell 96:725–736

    CAS  PubMed  Google Scholar 

  • Walder RY, Landau D, Meyer P, Shalev H, Tsolia M, Borochowitz Z, Boettger MB, Beck GE, Englehardt RK, Carmi R, Sheffield VC (2002) Mutation of TRPM6 causes familial hypomagnesemia with secondary hypocalcemia. Nat Genet 31:171–174

    CAS  PubMed  Google Scholar 

  • Walker RG, Willingham AT, Zuker CS (2000) A Drosophila mechanosensory transduction channel. Science 287:2229–2234

    CAS  PubMed  Google Scholar 

  • Wang T, Wang X, Xie Q, Montell C (2008) The SOCS box protein STOPS Is required for phototransduction through its effects on phospholipase C. Neuron 57:56–68

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wang G, Qiu YT, Lu T, Kwon HW, Pitts RJ, Van Loon JJ, Takken W, Zwiebel LJ (2009) Anopheles gambiae TRPA1 is a heat-activated channel expressed in thermosensitive sensilla of female antennae. Eur J Neurosci 30:967–974

    PubMed Central  PubMed  Google Scholar 

  • Wang K, Guo Y, Wang F, Wang Z (2011) Drosophila TRPA channel painless inhibits male-male courtship behavior through modulating olfactory sensation. PLoS One 6:e25890

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ward A, Liu J, Feng Z, Xu XZ (2008) Light-sensitive neurons and channels mediate phototaxis in C. elegans. Nat Neurosci 11:916–922

    CAS  PubMed Central  PubMed  Google Scholar 

  • Watnick TJ, Jin Y, Matunis E, Kernan MJ, Montell C (2003) A flagellar polycystin-2 homolog required for male fertility in Drosophila. Curr Biol 13:2179–2184

    CAS  PubMed  Google Scholar 

  • Wes PD, Chevesich J, Jeromin A, Rosenberg C, Stetten G, Montell C (1995) TRPC1, a human homolog of a Drosophila store-operated channel. Proc Natl Acad Sci U S A 92:9652–9656

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wolfgang W, Simoni A, Gentile C, Stanewsky R (2013) The Pyrexia transient receptor potential channel mediates circadian clock synchronization to low temperature cycles in Drosophila melanogaster. Proc Biol Sci 280:20130959

    PubMed  Google Scholar 

  • Wolstenholme AJ, Williamson SM, Reaves BJ (2011) TRP channels in parasites. Adv Exp Med Biol 704:359–371

    CAS  PubMed  Google Scholar 

  • Wong CO, Li R, Montell C, Venkatachalam K (2012) Drosophila TRPML is required for TORC1 activation. Curr Biol 22:1616–1621

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wu Q, Wen T, Lee G, Park JH, Cai HN, Shen P (2003) Developmental control of foraging and social behavior by the Drosophila neuropeptide Y-like system. Neuron 39:147–161

    CAS  PubMed  Google Scholar 

  • Wu LJ, Sweet TB, Clapham DE (2010) International union of basic and clinical pharmacology. LXXVI. Current progress in the mammalian TRP ion channel family. Pharmacol Rev 62:381–404

    CAS  PubMed Central  PubMed  Google Scholar 

  • Xiang Y, Yuan Q, Vogt N, Looger LL, Jan LY, Jan YN (2010) Light-avoidance-mediating photoreceptors tile the Drosophila larval body wall. Nature 468:921–926

    CAS  PubMed Central  PubMed  Google Scholar 

  • Xiao R, Xu XZ (2009) Function and regulation of TRP family channels in C. elegans. Pflugers Arch 458:851–860

    CAS  PubMed Central  PubMed  Google Scholar 

  • Xiao R, Xu XZ (2011) C. elegans TRP channels. Adv Exp Med Biol 704:323–339

    CAS  PubMed Central  PubMed  Google Scholar 

  • Xiao R, Zhang B, Dong Y, Gong J, Xu T, Liu J, Xu XZ (2013) A genetic program promotes C. elegans longevity at cold temperatures via a thermosensitive TRP channel. Cell 152:806–817

    CAS  PubMed Central  PubMed  Google Scholar 

  • Xu XZ, Sternberg PW (2003) A C. elegans sperm TRP protein required for sperm-egg interactions during fertilization. Cell 114:285–297

    CAS  PubMed  Google Scholar 

  • Xu XZ, Li HS, Guggino WB, Montell C (1997) Coassembly of TRP and TRPL produces a distinct store-operated conductance. Cell 89:1155–1164

    CAS  PubMed  Google Scholar 

  • Xu J, Sornborger AT, Lee JK, Shen P (2008) Drosophila TRPA channel modulates sugar-stimulated neural excitation, avoidance and social response. Nat Neurosci 11:676–682

    CAS  PubMed  Google Scholar 

  • Xue T, Do MT, Riccio A, Jiang Z, Hsieh J, Wang HC, Merbs SL, Welsbie DS, Yoshioka T, Weissgerber P, Stolz S, Flockerzi V, Freichel M, Simon MI, Clapham DE, Yau KW (2011) Melanopsin signalling in mammalian iris and retina. Nature 479:67–73

    CAS  PubMed Central  PubMed  Google Scholar 

  • Yan Z, Zhang W, He Y, Gorczyca D, Xiang Y, Cheng LE, Meltzer S, Jan LY, Jan YN (2013) Drosophila NOMPC is a mechanotransduction channel subunit for gentle-touch sensation. Nature 493:221–225

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang Y, Hoon MA, Chandrashekar J, Mueller KL, Cook B, Wu D, Zuker CS, Ryba NJ (2003) Coding of sweet, bitter, and umami tastes: different receptor cells sharing similar signaling pathways. Cell 112:293–301

    CAS  PubMed  Google Scholar 

  • Zhang S, Sokolchik I, Blanco G, Sze JY (2004) Caenorhabditis elegans TRPV ion channel regulates 5HT biosynthesis in chemosensory neurons. Development 131:1629–1638

    CAS  PubMed  Google Scholar 

  • Zhang HJ, Anderson AR, Trowell SC, Luo AR, Xiang ZH, Xia QY (2011) Topological and functional characterization of an insect gustatory receptor. PLoS One 6:e24111

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang W, Yan Z, Jan LY, Jan YN (2013a) Sound response mediated by the TRP channels NOMPC, NANCHUNG, and INACTIVE in chordotonal organs of Drosophila larvae. Proc Natl Acad Sci U S A 110:13612–13617

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhang YV, Ni J, Montell C (2013b) The molecular basis for attractive salt-taste coding in Drosophila. Science 340:1334–1338

    CAS  PubMed  Google Scholar 

  • Zhang YV, Raghuwanshi RP, Shen WL, Montell C (2013c) Food-experience induced taste desensitization modulated by the Drosophila TRPL channel. Nat Neurosci 16:1468–1476

    CAS  PubMed Central  PubMed  Google Scholar 

  • Zhong L, Bellemer A, Yan H, Honjo K, Robertson J, Hwang RY, Pitt GS, Tracey WD (2012) Thermosensory and non-thermosensory isoforms of Drosophila melanogaster TRPA1 reveal heat sensor domains of a thermoTRP channel. Cell Rep 1:43–55

    CAS  PubMed Central  PubMed  Google Scholar 

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Authors and Affiliations

  1. Department of Integrative Biology and Pharmacology, University of Texas School of Medicine, Houston, TX, 77030, USA

    Kartik Venkatachalam

  2. Department of Biological Chemistry, The Johns Hopkins University School of Medicine, Baltimore, MD, 21205, USA

    Junjie Luo

  3. Department of Molecular, Cellular, and Developmental Biology, Neuroscience Research Institute, University of California at Santa Barbara, Santa Barbara, CA, 93106, USA

    Junjie Luo & Craig Montell

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  1. Kartik Venkatachalam
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  2. Junjie Luo
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  3. Craig Montell
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Correspondence to Kartik Venkatachalam or Craig Montell .

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Editors and Affiliations

  1. Laboratory Ion Channel Research, Campus Gasthuisberg, KU Leuven Department, Cell Mol Medicin, Leuven, Belgium

    Bernd Nilius

  2. Pharmakologie und Toxikologie, Universität des Saarlandes, Institut für Experimentelle u. Klinische, Homburg, Germany

    Veit Flockerzi

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Venkatachalam, K., Luo, J., Montell, C. (2014). Evolutionarily Conserved, Multitasking TRP Channels: Lessons from Worms and Flies. In: Nilius, B., Flockerzi, V. (eds) Mammalian Transient Receptor Potential (TRP) Cation Channels. Handbook of Experimental Pharmacology, vol 223. Springer, Cham. https://doi.org/10.1007/978-3-319-05161-1_9

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