Relationship between the expression of Rab family GTPases and neuropeptide hormones in the brain of Bombyx mori

Histochemistry and Cell Biology

Volumn 139, Issue 2, 2013, Pages 299-308

  Uno, Tomohide ^a   Sakamoto, Kazuki ^a   Isoyama, Yuri ^a   Hiragaki, Susumu ^a   Uno, Yuichi ^a   Kanamaru, Kengo ^a   Yamagata, Hiroshi ^a   Takagi, Michihiro ^b   Mizoguchi, Akira ^c   Takeda, Makio ^a  

^a KOBE UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF ANIMAL HEALTH   (Japan)

^c NAGOYA UNIVERSITY   (Japan)

Author keywords

Bombyx mori; Bombyxin; Brain; Eclosion hormone; Insect; Rab

Indexed keywords

GUANOSINE TRIPHOSPHATASE; NEUROPEPTIDE; PROTHORACICOTROPIC HORMONE; RAB PROTEIN; RAB14 PROTEIN; RAB7 PROTEIN; UNCLASSIFIED DRUG; INSECT HORMONE;

ANIMAL TISSUE; ARTICLE; BOMBYX MORI; BRAIN TISSUE; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RABBIT; ANIMAL; BIOSYNTHESIS; BOMBYX; BRAIN; ENZYMOLOGY; ISOLATION AND PURIFICATION; METABOLISM;

BOMBYX MORI; HEXAPODA; ORYCTOLAGUS CUNICULUS;

ANIMALS; BOMBYX; BRAIN; IMMUNOHISTOCHEMISTRY; INSECT HORMONES; RAB GTP-BINDING PROTEINS;

EID: 84877143370     PISSN: 09486143     EISSN: 1432119X     Source Type: Journal    
DOI: 10.1007/s00418-012-1021-5     Document Type: Article

References (57)

1. Agui N, Granger NA, Gilbert LI, Bollenbacher WE (1979) Cellular localization of the insect prothoracicotropic hormone: in vitro assay of a single neurosecretory cell. Proc Natl Acad Sci USA 76:5694-5698
2. Bucci C, Thomsen P, Nicoziani P, McCarthy J, van Deurs B (2000) Rab7: a key to lysosome biogenesis. Mol Biol Cell 11:467-480
3. Copenhaver PF, Truman JW (1986a) Control of neurosecretion in the moth Manduca sexta: physiological regulation of the eclosion hormone cells. J Comp Physiol A 158:445-455
4. Copenhaver PF, Truman JW (1986b) Identification of the cerebral neurosecretory cells that contain eclosion hormone in the moth Manduca sexta. J Neurosci 6:1738-1747
5. Coutelis JB, Ephrussi A (2007) Rab6 mediates membrane organization and determinant localization during Drosophila oogenesis. Development 134:1419-1430
6. Ewer J (2005) Behavioral actions of neuropeptides in invertebrates: insights from Drosophila. Horm Behav 48:418-429
7. Ewer J, De Vente J, Truman JW (1994) Neuropeptide induction of cyclic GMP increases in the insect CNS: resolution at the level of single identifiable neurons. J Neurosci 14:7704-7712
8. Feng Y, Press B, Wandinger-Ness A (1995) Rab 7: an important regulator of late endocytic membrane traffic. J Cell Biol 131:1435-1452
9. Gammie SC, Truman JW (1999) Eclosion hormone provides a link between ecdysis-triggering hormone and crustacean cardioactive peptide in the neuroendocrine cascade that controls ecdysis behavior. J Exp Biol 202:343-352
10. Gilbert LI, Rybczynski R, Song Q, Mizoguchi A, Morreale R, Smith WA, Matubayashi H, Shionoya M, Nagata S, Kataoka H (2000) Dynamic regulation of prothoracic gland ecdysteroidogenesis: Manduca sexta recombinant prothoracicotropic hormone and brain extracts have identical effects. Insect Biochem Mol Biol 30:1079-1089
11. Grosshans BL, Ortiz D, Novick P (2006) Rabs and their effectors: achieving specificity in membrane traffic. Proc Natl Acad Sci USA 103:11821-11827
12. Harrison RE, Bucci C, Vieira OV, Schroer TA, Grinstein S (2003) Phagosomes fuse with late endosomes and/or lysosomes by extension of membrane protrusions along microtubules: role of Rab7 and RILP. Mol Cell Biol 23:6494-6506
13. Hartenstein V (2006) The neuroendocrine system of invertebrates: a developmental and evolutionary perspective. J Endocrinol 190:555-570
14. 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 335:607-615
15. Hou L, Wang JX, Zhao XF (2011) Rab32 and the remodeling of the imaginal midgut in Helicoverpa armigera. Amino Acids 40:953-961
16. Iwami M, Furuya I, Kataoka H (1996) Bombyxin-related peptides: cDNA structure and expression in the brain of the hornworm Agrius convolvuli [corrected]. Insect Biochem Mol Biol 26:25-32
17. Junutula JR, De Maziere AM, Peden AA, Ervin KE, Advani RJ, van Dijk SM, Klumperman J, Scheller RH (2004) Rab14 is involved in membrane trafficking between the Golgi complex and endosomes. Mol Biol Cell 15:2218-2229
18. Kawakami A, Kataoka H, Oka T, Mizoguchi A, Kimura-Kawakami M, Adachi T, Iwami M, Nagasawa H, Suzuki A, Ishizaki H (1990) Molecular cloning of the Bombyx mori prothoracicotropic hormone. Science 247:1333-1335
19. Kono T, Nagasawa H, Kataoka H, Isogai A, Fugo H, Suzuki A (1990) Eclosion hormone of the silkworm Bombyx mori. Expression in Escherichia coli and location of disulfide bonds. FEBS Lett 263:358-360
20. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685
21. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265-275
22. Marti T, Takio K, Walsh KA, Terzi G, Truman JW (1987) Microanalysis of the amino acid sequence of the eclosion hormone from the tobacco hornworm Manduca sexta. FEBS Lett 219:415-418
23. Masumura M, Satake S, Saegusa H, Mizoguchi A (2000) Glucose stimulates the release of bombyxin, an insulin-related peptide of the silkworm Bombyx mori. Gen Comp Endocrinol 118:393-399
24. McNabb SL, Truman JW (2008) Light and peptidergic eclosion hormone neurons stimulate a rapid eclosion response that masks circadian emergence in Drosophila. J Exp Biol 211:2263-2274
25. Mizoguchi A, Ishizaki H, Nagasawa H, Kataoka H, Isogai A, Tamura S, Suzuki A, Fujino M, Kitada C (1987) A monoclonal antibody against a synthetic fragment of bombyxin (4K-prothoracicotropic hormone) from the silkmoth, Bombyx mori: characterization and immunohistochemistry. Mol Cell Endocrinol 51:227-235
26. Mizoguchi A, Dedos SG, Fugo H, Kataoka H (2002) Basic pattern of fluctuation in hemolymph PTTH titers during larval-pupal and pupal-adult development of the silkworm, Bombyx mori. Gen Comp Endocrinol 127:181-189
27. Nagasawa H, Kataoka H, Isogai A, Tamura S, Suzuki A, Mizoguchi A, Fujiwara Y, Takahashi SY, Ishizaki H (1986) Amino acid sequence of a prothoracicotropic hormone of the silkworm Bombyx mori. Proc Natl Acad Sci USA 83:5840-5843
28. Nagata K, Maruyama K, Nagasawa H, Urushibata I, Isogai A, Ishizaki H, Suzuki A (1992) Bombyxin-II and its disulfide bond isomers: synthesis and activity. Peptides 13:653-662
29. Nassel DR, Homberg U (2006) Neuropeptides in interneurons of the insect brain. Cell Tissue Res 326:1-24
30. Nassel DR, Winther AM (2010) Drosophila neuropeptides in regulation of physiology and behavior. Prog Neurobiol 92:42-104
31. Nijhout HF, Grunert LW (2002) Bombyxin is a growth factor for wing imaginal disks in Lepidoptera. Proc Natl Acad Sci USA 99:15446-15450
32. Nijhout HF, Smith WA, Schachar I, Subramanian S, Tobler A, Grunert LW (2007) The control of growth and differentiation of the wing imaginal disks of Manduca sexta. Dev Biol 302:569-576
33. Pereira-Leal JB, Seabra MC (2001) Evolution of the Rab family of small GTP-binding proteins. J Mol Biol 313:889-901
34. Plutner H, Schwaninger R, Pind S, Balch WE (1990) Synthetic peptides of the Rab effector domain inhibit vesicular transport through the secretory pathway. EMBO J 9:2375-2383
35. Plutner H, Cox AD, Pind S, Khosravi-Far R, Bourne JR, Schwaninger R, Der CJ, Balch WE (1991) Rab1b regulates vesicular transport between the endoplasmic reticulum and successive Golgi compartments. J Cell Biol 115:31-43
36. Proikas-Cezanne T, Gaugel A, Frickey T, Nordheim A (2006) Rab14 is part of the early endosomal clathrin-coated TGN microdomain. FEBS Lett 580:5241-5246
37. Satake S, Masumura M, Ishizaki H, Nagata K, Kataoka H, Suzuki A, Mizoguchi A (1997) Bombyxin, an insulin-related peptide of insects, reduces the major storage carbohydrates in the silkworm Bombyx mori. Comp Biochem Physiol B Biochem Mol Biol 118:349-357
38. Satoh A, Tokunaga F, Kawamura S, Ozaki K (1997) In situ inhibition of vesicle transport and protein processing in the dominant negative Rab1 mutant of Drosophila. J Cell Sci 110(Pt 23):2943-2953
39. 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
40. Schwartz SL, Cao C, Pylypenko O, Rak A, Wandinger-Ness A (2007) Rab GTPases at a glance. J Cell Sci 120:3905-3910
41. 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
42. Stenmark H (2009) Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 10:513-525
43. Tobler A, Nijhout HF (2010) A switch in the control of growth of the wing imaginal disks of Manduca sexta. PLoS One 5:e10723
44. Tong C, Ohyama T, Tien AC, Rajan A, Haueter CM, Bellen HJ (2011) Rich regulates target specificity of photoreceptor cells and N-cadherin trafficking in the Drosophila visual system via Rab6. Neuron 71:447-459
45. Uno T, Ueno M, Nakajima A, Shirai Y, Aizono Y (1998) Molecular cloning of cDNA for BRab from the brain of Bombyx mori and biochemical properties of BRab expressed in Escherichia coli. Biosci Biotechnol Biochem 62:1885-1891
46. 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
47. Uno T, Hata K, Trang TD, Hiragaki S, Nakada T, Nakamura M, Uno Y, Yamagata H, Kanamru K, Takeda M, Matsubara M (2009) Phosphorylation of small GTPase Rab proteins from Bombyx mori (Lepidoptera: Bombycidae). Eur J Entomol 106:499-506
48. Uno T, Hata K, Hiragaki S, Isoyama Y, le Trang TD, Uno Y, Kanamaru K, Yamagata H, Nakamura M, Takagi M, Takeda M (2010a) Small GTPases of the Rab family in the brain of Bombyx mori. Histochem Cell Biol 134:615-622
49. Uno T, Moriwaki T, Isoyama Y, Uno Y, Kanamaru K, Yamagata H, Nakamura M, Takagi M (2010b) Rab14 from Bombyx mori (Lepidoptera: Bombycidae) shows ATPase activity. Biol Lett 6:379-381
50. 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
51. Vafopoulou X, Cardinal-Aucoin M, Steel CG (2012) Rhythmic release of prothoracicotropic hormone from the brain of an adult insect during egg development. Comp Biochem Physiol A Mol Integr Physiol 161:193-200
52. Westbrook AL, Bollenbacher WE (1990) The development of identified neurosecretory cells in the tobacco hornworm, Manduca sexta. Dev Biol 140:291-299
53. Wilkin M, Tongngok P, Gensch N, Clemence S, Motoki M, Yamada K, Hori K, Taniguchi-Kanai M, Franklin E, Matsuno K, Baron M (2008) Drosophila HOPS and AP-3 complex genes are required for a Deltex-regulated activation of notch in the endosomal trafficking pathway. Dev Cell 15:762-772
54. 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 447:366-380
55. Zavodska R, Sauman I, Sehnal F (2003) Distribution of PER protein, pigment-dispersing hormone, prothoracicotropic hormone, and eclosion hormone in the cephalic nervous system of insects. J Biol Rhythms 18:106-122
56. Zhang M, Xu WH (2006) Isolation of an eclosion hormone gene from the cotton bollworm, Helicoverpa armigera: temporal and spatial distribution of transcripts. Comp Biochem Physiol B Biochem Mol Biol 143:351-359
57. Zhang J, Schulze KL, Hiesinger PR, Suyama K, Wang S, Fish M, Acar M, Hoskins RA, Bellen HJ, Scott MP (2007) Thirty-one flavors of Drosophila rab proteins. Genetics 176:1307-1322