Histochemistry and Cell Biology

, Volume 134, Issue 6, pp 615–622 | Cite as

Small GTPases of the Rab family in the brain of Bombyx mori

  • Tomohide Uno
  • Keisuke Hata
  • Susumu Hiragaki
  • Yuri Isoyama
  • Le Thi Dieu Trang
  • Yuichi Uno
  • Kengo Kanamaru
  • Hiroshi Yamagata
  • Masahiko Nakamura
  • Michihiro Takagi
  • Makio Takeda
Original Paper
First Online:
Accepted:

Abstract

Small GTPases of the Rab family are key regulators of membrane trafficking. We produced antibodies against the Rab7 protein of Bombyx mori (BRab7) in rabbits, and against the Rab11 protein of B. mori (BRab11) in mice. The antibodies recognized BRab7 and BRab11 proteins, but did not recognize other Rab proteins. Immunoblotting of samples from brain tissue of B. mori revealed a single band for each antibody. Rab11 was expressed in most tissues, whereas Rab7 was expressed in the brain, ovary, and testis. Immunohistochemical reactivity of Rab7 and Rab11 in the brain of B. mori was restricted to neurons of the pars intercerebralis and dorsolateral protocerebrum. Double-labeling experiments demonstrated that immunohistochemical reactivity of Rab7 co-localized with that of Rab11 and partially with that of Rab8. Immunohistochemical reactivity of Rab11 and Rab8 co-localized with that of PERIOD, one of the proteins associated with circadian rhythm. These findings suggest that Rab7, Rab8, and Rab11 are involved in protein transport in the neurons of the brain of B. mori and might play a role in the control of circadian rhythm.

Keywords

Bombyx mori Rab Brain PERIOD Insect 
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Notes

Acknowledgments

This work was supported in part by a Grant-in-Aid for Research in Priority Areas, 20580053 and Global Center of Education and Research Program (19GCOE01), from the Ministry of Education, Science, Sports and Culture of Japan.

References

  1. Alone DP, Tiwari AK, Mandal L, Li M, Mechler BM, Roy JK (2005) Rab11 is required during Drosophila eye development. Int J Dev Biol 49:873–879CrossRefPubMedGoogle Scholar
  2. Bhuin T, Roy JK (2009a) Rab11 is required for embryonic nervous system development in Drosophila. Cell Tissue Res 335:349–356CrossRefPubMedGoogle Scholar
  3. Bhuin T, Roy JK (2009b) Rab11 is required for myoblast fusion in Drosophila. Cell Tissue Res 336:489–499CrossRefPubMedGoogle Scholar
  4. Bogard N, Lan L, Xu J, Cohen RS (2007) Rab11 maintains connections between germline stem cells and niche cells in the Drosophila ovary. Development 134:3413–3418CrossRefPubMedGoogle Scholar
  5. Boothroyd CE, Young MW (2008) The in(put)s and out(put)s of the Drosophila circadian clock. Ann NY Acad Sci 1129:350–357CrossRefPubMedGoogle Scholar
  6. Bucci C, Thomsen P, Nicoziani P, McCarthy J, van Deurs B (2000) Rab7: a key to lysosome biogenesis. Mol Biol Cell 11:467–480PubMedGoogle Scholar
  7. Coutelis JB, Ephrussi A (2007) Rab6 mediates membrane organization and determinant localization during Drosophila oogenesis. Development 134:1419–1430CrossRefPubMedGoogle Scholar
  8. Dollar G, Struckhoff E, Michaud J, Cohen RS (2002) Rab11 polarization of the Drosophila oocyte: a novel link between membrane trafficking, microtubule organization, and oskar mRNA localization and translation. Development 129:517–526PubMedGoogle Scholar
  9. Grosshans BL, Ortiz D, Novick P (2006) Rabs and their effectors: achieving specificity in membrane traffic. Proc Natl Acad Sci USA 103:11821–11827CrossRefPubMedGoogle Scholar
  10. Hall JC (2003) Genetics and molecular biology of rhythms in Drosophila and other insects. Adv Genet 48:1–280CrossRefPubMedGoogle Scholar
  11. Hartenstein V (2006) The neuroendocrine system of invertebrates: a developmental and evolutionary perspective. J Endocrinol 190:555–570Google Scholar
  12. Helfrich-Forster C (1995) The period clock gene is expressed in central nervous system neurons which also produce a neuropeptide that reveals the projections of circadian pacemaker cells within the brain of Drosophila melanogaster. Proc Natl Acad Sci USA 92:612–616CrossRefPubMedGoogle Scholar
  13. Hiragaki S, Uno T, Takeda M (2009) 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 335:607–615Google Scholar
  14. Kapfhamer D, Valladares O, Sun Y, Nolan PM, Rux JJ, Arnold SE, Veasey SC, Bucan M (2002) Mutations in Rab3a alter circadian period and homeostatic response to sleep loss in the mouse. Nat Genet 32:290–295CrossRefPubMedGoogle Scholar
  15. King DP, Takahashi JS (2000) Molecular genetics of circadian rhythms in mammals. Annu Rev Neurosci 23:713–742CrossRefPubMedGoogle Scholar
  16. Kouranti I, Sachse M, Arouche N, Goud B, Echard A (2006) Rab35 regulates an endocytic recycling pathway essential for the terminal steps of cytokinesis. Curr Biol 16:1719–1725CrossRefPubMedGoogle Scholar
  17. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685CrossRefPubMedGoogle Scholar
  18. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275PubMedGoogle Scholar
  19. Ng EL, Tang BL (2008) Rab GTPases and their roles in brain neurons and glia. Brain Res Rev 58:236–246CrossRefPubMedGoogle Scholar
  20. Okamoto A, Mori H, Tomioka K (2001) The role of the optic lobe in circadian locomotor rhythm generation in the cricket, Gryllus bimaculatus, with special reference to PDH-immunoreactive neurons. J Insect physiol 47:889–895Google Scholar
  21. Park JH, Helfrich-Forster C, Lee G, Liu L, Rosbash M, Hall JC (2000) Differential regulation of circadian pacemaker output by separate clock genes in Drosophila. Proc Natl Acad Sci USA 97:3608–3613Google Scholar
  22. Pelissier A, Chauvin JP, Lecuit T (2003) Trafficking through Rab11 endosomes is required for cellularization during Drosophila embryogenesis. Curr Biol 13:1848–1857CrossRefPubMedGoogle Scholar
  23. Pereira-Leal JB, Seabra MC (2001) Evolution of the Rab family of small GTP-binding proteins. J Mol Biol 313:889–901CrossRefPubMedGoogle Scholar
  24. Qi-miao S, Tanaka S, Takeda M (2003) Immunohistochemical localization of clock proteins (DBT and PER), and [His7]- and [Arg7]-corazonins in the cerebral ganglia of Bombyx mori: are corazonins downstream regulators of circadian clocks? Eur J Entomol 100:283–286Google Scholar
  25. Ren M, Xu G, Zeng J, De Lemos-Chiarandini C, Adesnik M, Sabatini DD (1998) Hydrolysis of GTP on rab11 is required for the direct delivery of transferrin from the pericentriolar recycling compartment to the cell surface but not from sorting endosomes. Proc Natl Acad Sci USA 95:6187–6192CrossRefPubMedGoogle Scholar
  26. Satoh AK, O’Tousa JE, Ozaki K, Ready DF (2005) Rab11 mediates post-Golgi trafficking of rhodopsin to the photosensitive apical membrane of Drosophila photoreceptors. Development 132:1487–1497CrossRefPubMedGoogle Scholar
  27. Sauman I, Reppert SM (1996a) Circadian clock neurons in the silkmoth Antheraea pernyi: novel mechanisms of Period protein regulation. Neuron 17:889–900CrossRefPubMedGoogle Scholar
  28. Sauman I, Reppert SM (1996b) 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 178:418–429CrossRefPubMedGoogle Scholar
  29. Saxena S, Bucci C, Weis J, Kruttgen A (2005) The small GTPase Rab7 controls the endosomal trafficking and neuritogenic signaling of the nerve growth factor receptor TrkA. J Neurosci 25:10930–10940CrossRefPubMedGoogle Scholar
  30. Schwartz SL, Cao C, Pylypenko O, Rak A, Wandinger-Ness A (2007) Rab GTPases at a glance. J Cell Sci 120:3905–3910CrossRefPubMedGoogle Scholar
  31. Sehadova H, Markova EP, Sehnal F, Takeda M (2004) Distribution of circadian clock-related proteins in the cephalic nervous system of the silkworm, Bombyx mori. J Biol Rhythms 19:466–482CrossRefPubMedGoogle Scholar
  32. Steel CG, Vafopoulou X (2006) Circadian orchestration of developmental hormones in the insect, Rhodnius prolixus. Comp Biochem Physiol A Mol Integr Physiol 144:351–364CrossRefPubMedGoogle Scholar
  33. Stengl M, Homberg U (1994) Pigment-dispersing hormone-immunoreactive neurons in the cockroach Leucophaea maderae share properties with circadian pacemaker neurons. J Comp Physiol A 175:203–213CrossRefPubMedGoogle Scholar
  34. Stenmark H (2009) Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 10:513–525CrossRefPubMedGoogle Scholar
  35. Thomas C, Rousset R, Noselli S (2009) JNK signalling influences intracellular trafficking during Drosophila morphogenesis through regulation of the novel target gene Rab30. Dev Biol 331:250–260CrossRefPubMedGoogle Scholar
  36. Ullrich O, Reinsch S, Urbe S, Zerial M, Parton RG (1996) Rab11 regulates recycling through the pericentriolar recycling endosome. J Cell Biol 135:913–924CrossRefPubMedGoogle Scholar
  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 61:65–76Google Scholar
  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 66:89–97CrossRefPubMedGoogle Scholar
  39. Uno T, Moriwaki T, Nakamura M, Matsubara M, Yamagata H, Kanamaru K, Takagi M (2009) Biochemical characterization of rab proteins from Bombyx mori. Arch Insect Biochem Physiol 70:77–89CrossRefPubMedGoogle Scholar
  40. Vanlandingham PA, Ceresa BP (2009) Rab7 regulates late endocytic trafficking downstream of multivesicular body biogenesis and cargo sequestration. J Biol Chem 284:12110–12124CrossRefPubMedGoogle Scholar
  41. Wilcke M, Johannes L, Galli T, Mayau V, Goud B, Salamero J (2000) Rab11 regulates the compartmentalization of early endosomes required for efficient transport from early endosomes to the trans-golgi network. J Cell Biol 151:1207–1220CrossRefPubMedGoogle Scholar
  42. Wise S, Davis NT, Tyndale E, Noveral J, Folwell MG, Bedian V, Emery IF, Siwicki KK (2002) Neuroanatomical studies of period gene expression in the hawkmoth, Manduca sexta. J Comp Neurol 447:366–380Google Scholar
  43. Zhang J, Fonovic M, Suyama K, Bogyo M, Scott MP (2009) Rab35 controls actin bundling by recruiting fascin as an effector protein. Science 325:1250–1254CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Tomohide Uno
    • 1
  • Keisuke Hata
    • 1
  • Susumu Hiragaki
    • 2
  • Yuri Isoyama
    • 1
  • Le Thi Dieu Trang
    • 3
  • Yuichi Uno
    • 4
  • Kengo Kanamaru
    • 1
  • Hiroshi Yamagata
    • 1
  • Masahiko Nakamura
    • 5
  • Michihiro Takagi
    • 6
  • Makio Takeda
    • 2
  1. 1.Laboratory of Biological Chemistry, Department of Biofunctional Chemistry, Faculty of AgricultureKobe UniversityKobeJapan
  2. 2.Graduate School of Agricultural ScienceKobe UniversityKobeJapan
  3. 3.Institute for Biotechnology and EnvironmentNong Lam UniversityHo Chi Minh CityVietnam
  4. 4.Department of Plant Resource Science, Faculty of AgricultureKobe UniversityKobeJapan
  5. 5.Department of Bioscience and Biotechnology, Faculty of Bioenvironmental ScienceKyoto Gakuen UniversityKameokaJapan
  6. 6.Research Team for Viral DiseaseNational Institute of Animal HealthTsukubaJapan

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