Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Putative regulatory mechanism of prothoracicotropic hormone (PTTH) secretion in the American cockroach, Periplaneta americana as inferred from co-localization of Rab8, PTTH, and protein kinase C in neurosecretory cells

Abstract

Small GTPases of the Rab family act as essential regulators of vesicle transport pathways, including the exocytosis of neurohormones. These processes are not well-understood in insects. To address the physiological function of Rab proteins and their phosphorylation in insect neurosecretion, Rab8-like, prothoracicotropic hormone (PTTH)-like, and protein kinase C (PKC)-like immunohistochemical reactivities (-ir) were investigated in the brain of the American cockroach, Periplaneta americana. All the antibodies tested reacted with neurons in the pars intercerebralis, corpora cardiaca, and nervi corporis allati I. Double-labeling experiments demonstrated that all PTTH-ir were colocalized with Rab8-ir and PKC-ir in the pars intercerebralis, although exclusive reactivity was present to antisera against Rab8 or PKC. These findings support the notion that Rab8-like antigen is phosphorylated by PKC, and that this phosphorylation is involved in the axonal transport and secretion of PTTH in this species.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Amadio M, Battaini F, Pascale A (2006) The different facets of protein kinases C: old and new players in neuronal signal transduction pathways. Pharmacol Res 54:317–325

  2. Baldini G, Wang G, Weber M, Zweyer M, Bareggi R, Witkin JW, Martelli AM (1998) Expression of Rab3D N135I inhibits regulated secretion of ACTH in AtT-20 cells. J Cell Biol 140:305–313

  3. Chiariello M, Bruni CB, Bucci C (1999) The small GTPases Rab5a, Rab5b and Rab5c are differentially phosphorylated in vitro. FEBS Lett 453:20–24

  4. Deneka M, Neeft M, Sluijs P van der (2003) Regulation of membrane transport by rab GTPases. Crit Rev Biochem Mol Biol 38:121–142

  5. Deretic D, Huber LA, Ransom N, Mancini M, Simons K, Papermaster DS (1995) Rab8 in retinal photoreceptors may participate in rhodopsin transport and in rod outer segment disk morphogenesis. J Cell Sci 108:215–224

  6. Ding J, Soule G, Overmeyer JH, Maltese WA (2003) Tyrosine phosphorylation of the Rab24 GTPase in cultured mammalian cells. Biochem Biophys Res Commun 312:670–675

  7. Fitzgerald ML, Reed GL (1999) Rab6 is phosphorylated in thrombin-activated platelets by a protein kinase C-dependent mechanism: effects on GTP/GDP binding and cellular distribution. Biochem J 342:353–360

  8. Goltzené F, Holder F, Charlet M, Meister M, Oka T (1992) Immunocytochemical localization of Bombyx-PTTH-like molecules in neurosecretory cells of the brain of the migratory locust, Locusta migratoria. A comparison with neuroparsin and insulin-related peptide. Cell Tissue Res 269:133–140

  9. Griner EM, Kazanietz MG (2007) Protein kinase C and other diacylglycerol effectors in cancer. Nat Rev Cancer 7:281–294

  10. Gurkan C, Lapp H, Alory C, Su AI, Hogenesch JB, Balch WE (2005) Large-scale profiling of Rab GTPase trafficking networks: the membrome. Mol Biol Cell 16:3847–3864

  11. Gurkan C, Koulov AV, Balch WE (2007) An evolutionary perspective on eukaryotic membrane trafficking. Adv Exp Med Biol 607:73–83

  12. Hartenstein V (2006) The neuroendocrine system of invertebrates: a developmental and evolutionary perspective. J Endocrinol 190:555–570

  13. Hattula K, Furuhjelm J, Arffman A, Peranen J (2002) A Rab8-specific GDP/GTP exchange factor is involved in actin remodeling and polarized membrane transport. Mol Biol Cell 13:3268–3280

  14. Huber LA, Hoop MJ de, Dupree P, Zerial M, Simons K, Dotti C (1993) Protein transport to the dendritic plasma membrane of cultured neurons is regulated by rab8p. J Cell Biol 123:47–55

  15. Huber LA, Dupree P, Dotti CG (1995) A deficiency of the small GTPase rab8 inhibits membrane traffic in developing neurons. Mol Cell Biol 15:918–924

  16. Ishizaki H, Suzuki A (1994) The brain secretory peptides that control moulting and metamorphosis of the silkmoth, Bombyx mori. Int J Dev Biol 38:301–310

  17. Karniguian A, Zahraoui A, Tavitian A (1993) Identification of small GTP-binding rab proteins in human platelets: thrombin-induced phosphorylation of rab3B, rab6, and rab8 proteins. Proc Natl Acad Sci USA 90:7647–7651

  18. Krauthamer V (1985) Morphology of identified neurosecretory and non-neurosecretory cells in the cockroach pars intercerebralis. J Exp Zool 234:221–230

  19. Mizoguchi A, Oka T, Kataoka H, Nagasawa H, Suzuk A, Ishizaki H (1990) Immunohistochemical localization of prothoracicotropic hormone-producing neurosecretory cells in the brain of Bombyx mori. Dev Growth Differ 32:591–598

  20. Moritz OL, Tam BM, Hurd LL, Peränen J, Deretic D, Papermaster DS (2001) Mutant rab8 impairs docking and fusion of rhodopsin-bearing post-Golgi membranes and causes cell death of transgenic Xenopus rods. Mol Biol Cell 12:2341–2351

  21. Nishizuka Y (1995) Protein kinase C and lipid signaling for sustained cellular responses. FASEB J 9:484–496

  22. Noguti T, Adachi-Yamada T, Katagiri T, Kawakami A, Iwami M, Ishibashi J, Kataoka H, Suzuki A, Go M, Ishizaki H (1995) Insect prothoracicotropic hormone: a new member of the vertebrate growth factor superfamily. FEBS Lett 376:251–256

  23. Pfeffer S, Aivazian D (2004) Targeting Rab GTPases to distinct membrane compartments. Nat Rev Mol Cell Biol 5:886–896

  24. Pipa RL (1978) Locations and central projections of neurons associated with the retrocerebral neuroendocrine complex of the cockroach Periplaneta americana (L.). Cell Tissue Res 30:443–455

  25. Richter K, Böhm GA (1997) The molting gland of the cockroach Periplaneta americana: secretory activity and its regulation. Gen Pharmacol 29:17–21

  26. Richter K, Peschke E, Peschke D (2000) A neuroendocrine releasing effect of melatonin in the brain of an insect, Periplaneta americana (L.). J Pineal Res 28:129–135

  27. Sauman I, Reppert SM (1996) Molecular characterization of prothoracicotropic hormone (PTTH) from the giant silkmoth Antheraea pernyi: developmental appearance of PTTH-expressing cells and relationship to circadian clock cells in central brain. Dev Biol 178:418–429

  28. Schaeffer E, Smith D, Mardon G, Quinn W, Zuker C (1989) Isolation and characterization of two new Drosophila protein kinase C genes, including one specifically expressed in photoreceptor cells. Cell 57:403–412

  29. Shirai Y, Iwasaki T, Matsubara F, Aizono Y (1994) The carbachol-induced release of prothoracicotropic hormone from brain-corpus cardiacum-corpus allatum complex of the silkworm, Bombyx mori. J Insect Physiol 40:469–473

  30. Shirai Y, Shimazaki K, Iwasaki T, Matsubara F, Aizono Y (1995) The in situ release of prothoracicotropic hormone (PTTH) in the brain-corpus cardiacum-corpus allatum complex of silkworm, Bombyx mori. Comp Biochem Physiol [C] 110:143–148

  31. Shirai Y, Sumida M, Sakamura Y, Aizono Y (1997) Carbachol-induced protein phosphorylation in the brain-corpus cardiacum-corpus allatum complex of the silkworm, Bombyx mori. Appl Entomol Zool 32:573–581

  32. Shirai Y, Uno T, Aizono Y (1998) Small GTP-binding proteins in the brain-corpus cardiacum-corpus allatum complex of the silkworm, Bombyx mori: involvement in the secretion of prothoracicotropic hormone. Arch Insect Biochem Physiol 38:177–184

  33. Steel CG, Vafopoulou X (2006) Circadian orchestration of developmental hormones in the insect, Rhodnius prolixus. Comp Biochem Physiol [A] Mol Integr Physiol 144:351–364

  34. Tasaka K, Masumoto N, Mizuki J, Ikebuchi Y, Ohmichi M, Kurachi H, Miyake A, Murata Y (1998) Rab3B is essential for GnRH-induced gonadotrophin release from anterior pituitary cells. J Endocrinol 157:267–274

  35. Ullrich O, Stenmark H, Alexandrov K, Huber LA, Kaibuchi K, Sasaki T, Takai Y, Zerial M (1993) Rab GDP dissociation inhibitor as a general regulator for the membrane association of rab proteins. J Biol Chem 268:18143–18150

  36. Uno T, Nakao A, Katsurauma C (2004) Phosphorylation of Rab proteins from the brain of Bombyx mori. Arch Insect Biochem Physiol 57:68–77

  37. Uno T, Nakao A, Fujiwara Y, Katsurauma C, Nakada T, Itoh O (2006) Molecular cloning and expression of protein kinase C from Bombyx mori. Arch Insect Biochem Physiol 61:65–76

  38. Uno T, Nakada T, Okamaoto S, Nakamura M, Matsubara M, Imaishi H, Yamagata H, Kanamaru K, Takagi M (2007) Determination of phosphorylated amino acid residues of Rab8 from Bombyx mori. Arch Insect Biochem Physiol 66:89–97

  39. Vafopoulou X, Steel CG, Terry KL (2007) Neuroanatomical relations of prothoracicotropic hormone neurons with the circadian timekeeping system in the brain of larval and adult Rhodnius prolixus (Hemiptera). J Comp Neurol 503:511–524

  40. Zerial M, McBride H (2001) Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2:107–117

  41. Zhao S, Torii S, Yokota-Hashimoto H, Takeuchi T, Izumi T (2002) Involvement of Rab27b in the regulated secretion of pituitary hormones. Endocrinology 143:1817–1824

Download references

Acknowledgments

We thank Dr. I. Sauman for providing the anti-PTTH antibody. We also thank Dr. M. Takagi who helped us with the production of the anti-Rab8 antibody.

Author information

Correspondence to Makio Takeda.

Additional information

This work was supported by a Grant-in-Aid for Scientific Research (B) 1838043, (C) 20580053, and Global Center of Education and Research Program (19GCOE01) from the Japan Society for the Promotion of Science.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Hiragaki, S., Uno, T. & Takeda, M. Putative regulatory mechanism of prothoracicotropic hormone (PTTH) secretion in the American cockroach, Periplaneta americana as inferred from co-localization of Rab8, PTTH, and protein kinase C in neurosecretory cells. Cell Tissue Res 335, 607–615 (2009). https://doi.org/10.1007/s00441-008-0747-9

Download citation

Keywords

  • Rab protein
  • Neurosecretion
  • Protein kinase C
  • Prothoracicotropic hormone
  • Periplaneta americana (Insecta)