An insulin-like system involved in the control of Pacific oyster Crassostrea gigas reproduction: hrIGF-1 effect on germinal cell proliferation and maturation associated with expression of an homologous insulin receptor-related receptor

Aquaculture

Volumn 251, Issue 1, 2006, Pages 85-98

  Gricourt, L ^a   Mathieu, M ^a   Kellner, K ^a  

^a UNIVERSITÉ DE CAEN   (France)

Author keywords

Crassostrea gigas; Development; Gametogenesis; IGF 1; Insulin like receptor; Pacific oyster; Regulation; Reproduction

Indexed keywords

GAMETOGENESIS; MATURATION; OYSTER CULTURE; REPRODUCTION;

CRASSOSTREA GIGAS; OSTREIDAE;

EID: 29244449642     PISSN: 00448486     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.aquaculture.2005.05.015     Document Type: Article

References (90)

1. T. Adachi, S. Takiya, Y. Suzuki, M. Iwani, A. Kawakami, S.Y. Takahashi, H. Ishizaki, H. Nagasawa, and A. Suzuki cDNA structure and expression of bombyxin, an insulin-like brain secretory peptide of the silkmoth Bombyx mori J. Biol. Chem. 264 13 1989 7681 7685
2. C. Berthelin, K. Kellner, and M. Mathieu Storage metabolism in the Pacific oyster (Crassostrea gigas) in relation to summer mortalities and reproductive cycle (West coast of France) Comp. Biochem. Physiol., Part B Biochem. Mol. Biol. 125 2000 359 369
3. W. Brogiolo, H. Stocker, T. Ikeya, F. Rintelen, R. Fernandez, and E. Hafen An evolutionarily conserved function of the Drosophila insulin receptor and insulin-like peptides in growth control Curr. Biol. 11 4 2001 213 221
4. C. Cao, and M.R. Brown Localization of insulin-like peptide in brains of two flies Cell Tissue Res. 304 2 2001 317 321
5. Coulon, I., 1993. Mise au point d'un système contrôlé de culture de cellules de cœur d'huître Crassostrea gigas. Application au test de la toxicité des produits chimiques en milieu aquatique. Thèse de Doctorat, Institut National Agronomique Paris-Grignon.
6. L. Duret, N. Guex, M.C. Peitsch, and A. Bairoch New insulin-like proteins with atypical disulfide bond pattern characterized in Caenorhabditis elegans by comparative sequence analysis and homology modeling Genome Res. 8 1998 348 353
7. R. Fernandez, D. Tabarin, N. Azpiazu, M. Frasch, and J. Schlessinger The Drosophila insulin receptor homolog: a gene essential for embryonic development encodes two receptor isoforms with different signalling potential EMBO J. 14 14 1995 3373 3384
8. R. Fernandez-Almonacid, and O.M. Rosen Structure and ligand specificity of the Drosophila melanogaster insulin receptor Mol. Cell. Biol. 7 8 1987 2718 2727
9. P.D. Floyd, L. Li, S.S. Rubakhin, J.V. Sweedler, C.C. Horn, I. Kupfermann, V.Y. Alexeeva, T.A. Ellis, N.C. Dembrow, K.R. Weiss, and F.S. Vilim Insulin prohormone processing, distribution, and relation to metabolism in Aplysia californica J. Neurosci. 19 18 1999 7732 7741
10. H. Fugo, J.H. Chen, M. Nakajima, H. Nagasawa, and A. Suzuki Neurohormones in developing embryos of the silkworm Bombyx mori: the presence and characteristics of prothoracicotropic hormones J. Insect Physiol. 33 1987 245 248
11. G. Fullbright, E.R. Lacy, and E.E. Büllesbach The prothoracicotropic hormone bombyxin has specific receptors on insect ovarian cells Eur. J. Biochem. 245 1997 774 780
12. M. Gabe Masson & Co. Techniques Histologiques Paris 1968 (1113 pp.)
13. R.S. Garofalo, and O.M. Rosen Tissue localization of Drosophila melanogaster insulin receptor transcripts during development Mol. Cell. Biol. 8 1988 1638 1647
14. W.P.M. Geraerts The role of the lateral lobes in the control of growth and reproduction in the hermaphrodite freshwater snail Lymnaea stagnalis Gen. Comp. Endocrinol. 29 1976 97 108
15. P. Gomot Studies on the control of spermatogenic DNA synthesis by the mesocerebrum in the snail Helix aspersa Cell. Mol. Neurobiol. 13 5 1993 517 527
16. R. Graf, S. Neuenschwander, M.R. Brown, and U. Ackermann Insulin-mediated secretion of ecdysteroids from mosquito ovaries and molecular cloning of the insulin receptor homologue from ovaries of bloodfed Aedes aegypti Insect Mol. Biol. 6 2 1997 151 163
17. F.M. Gregoire, N. Chomiki, D. Kachinskas, and C. Warden Cloning and developmental regulation of a novel member of the insulin-like gene family in Caenorhabditis elegans Biochem. Biophys. Res. Commun. 249 2 1998 385 390
18. L. Gricourt, G. Bonnec, D. Boujard, M. Mathieu, and K. Kellner Insulin-like system and growth regulation in the Pacific oyster Crassostrea gigas: hrIGF-1 effect on protein synthesis of mantle edge cells and expression of an homologous insulin receptor-related receptor Gen. Comp. Endocrinol. 134 2003 44 56
19. P. Helbling, and R. Graf Localization of the mosquito insulin receptor homolog (MIR) in reproducing yellow fever mosquitoes (Aedes aegypti) J. Insect Physiol. 44 1998 1127 1135
20. Heude-Berthelin, C., 2000. Etude du métabolisme du glycogène chez l'huître creuse Crassostrea gigas. Impact sur la reproduction et les mortalités estivales. Thèse de Doctorat, Université de Caen.
21. C. Heude-Berthelin, J. Laisney, J. Espinosa, O. Martin, G. Hernandez, M. Mathieu, and K. Kellner Storage and reproductive strategy in Crassostrea gigas from two different growing areas (Normandy and the Atlantic coast, France) Invertebr. Reprod. Dev. 40 1 2001 79 86
22. M. Iwami, A. Kawakami, H. Ishizaki, S.Y. Takahashi, T. Adachi, Y. Suzuki, H. Nagasawa, and A. Suzuki Cloning of a gene encoding bombyxin, an insulin-like brain secretory peptide of silkmoth Bombyx mori with prothoracicotropic activity Dev. Growth Differ. 31 1 1989 31 37
23. M. Iwami, T. Adachi, H. Kondo, A. Kawakami, Y. Suzuki, H. Nagasawa, A. Suzuki, and H. Ishizaki A novel family C of the genes that encode bombyxin, an insulin-related brain secretory peptide of the silkmoth Bombyx mori: isolation and characterization of gene C-1 Insect Biochem. 20 1990 295 303
24. M. Iwami, I. Furuya, and H. Kataoka Bombyxin-related peptides: cDNA structure and expression in the brain of the hornworm Agrius convolvuli Insect Biochem. Mol. Biol. 26 1 1996 25 32
25. M. Iwami, A. Tanaka, N. Hano, and S. Sakurai Bombyxin gene expression in tissues other than brain detected by reverse transcription-polymerase chain reaction (RT-PCR) and in situ hybridization Experientia 52 9 1996 882 887
26. M. Janicot, and M.D. Lane Activation of glucose uptake by insulin and insulin-like growth factor I in Xenopus oocytes Proc. Natl. Acad. Sci. U. S. A. 86 8 1989 2642 2646
27. C. Kappler, F. Goltzené, M. Lagueux, C. Hetru, and J.A. Hoffmann Role of the follicle cells and the oocytes in ecdysone biosynthesis and esterification in vitellogenic females of Locusta migratoria Int. J. Invertebr. Reprod. Dev. 9 1986 17 34
28. A. Kawakami, M. Iwami, H. Nagasawa, A. Suzuki, and H. Ishizaki Structure and organization of four clustered genes that encode bombyxin, an insulin-related brain secretory peptide of the silkmoth Bombyx mori Proc. Natl. Acad. Sci. U. S. A. 86 1989 6843 6847
29. T. Kawano, Y. Ito, M. Ishiguro, K. Takuwa, T. Nakajima, and Y. Kimura Molecular cloning and characterization of a new insulin/IGF-like peptide of the nematode Caenorhabditis elegans Biochem. Biophys. Res. Commun. 273 2 2000 431 436
30. K.D. Kimura, H.A. Tissenbaum, Y. Liu, and G. Ruvkunt Daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans Science 277 1997 942 946
31. M. Kimura-Kawakami, M. Iwami, A. Kawakami, H. Nagasawa, A. Suzuki, and H. Ishizaki Structure and expression of bombyxin-related peptide genes of the moth Samia cynthia ricini Gen. Comp. Endocrinol. 86 2 1992 257 268
32. H. Kondo, M. Ino, A. Suzuki, H. Ishizaki, and M. Iwami Multiple gene copies for bombyxin, an insulin-related peptide of the silkmoth Bombyx mori: structural signs for gene rearrangement and duplication responsible for generation of multiple molecular forms of bombyxin J. Mol. Biol. 259 5 1996 926 937
33. C. Konrad, A. Kroner, M. Spiliotis, R. Zavala-Góngora, and K. Brehm Identification and molecular characterisation of a gene encoding a member of the insulin receptor family in Echinococcus multilocularis Int. J. Parasitol. 33 3 2003 301 312
34. E. Kromer-Metzger, and M. Lagueux Expression of the gene encoding an insulin-related peptide in Locusta (Insecta, Orthoptera). Evidence for alternative promoter usage Eur. J. Biochem. 221 1994 427 434
35. M. Lagueux, M. Him, and J.A. Hoffmann Ecdysone during ovarian development in Locusta migratoria J. Insect Physiol. 23 1 1977 109 119
36. M. Lagueux, L. Lwoff, M. Meister, F. Goltzené, and J. Hoffmann cDNAs form neurosecretory cells of brains of Locusta migratoria (Insecta, Orthoptera) encoding a novel member of the superfamily of insulins Eur. J. Biochem. 187 1990 249 254
37. V. Lardans, J.F. Coppin, J. Vicogne, E. Aroca, M. Delcroix, and C. Dissous Characterization of an insulin receptor-related receptor in Biomphalaria glabrata embryonic cells Biochim. Biophys. Acta 1510 2001 321 329
38. F. Le Gac, M. Loir, P.-Y. Le Bail, and M. Ollitrault Insulin-like growth factor (IGF-1) mRNA and IGF receptor in trout testis and in isolated spermatogenic and Sertoli cells Mol. Reprod. Dev. 44 1 1996 23 35
39. K.W. Li, and W.P.M. Geraerts Isolation and chemical characterization of a novel insulin-related neuropeptide from the freshwater snail, Lymnaea stagnalis Eur. J. Biochem. 205 1992 675 678
40. K.W. Li, W.P.M. Geraerts, R.H.M. Ebberink, and J. Joosse Purification and sequencing of molluscan insulin-related peptide I (MIP I) from the neuroendocrine light green cells of Lymnaea stagnalis Mol. Cell. Endocrinol. 85 1992 141 150
41. K.W. Li, W.P.M. Geraerts, H. Van Loenhout, and J. Joosse Biosynthesis and axonal transport of multiple molluscan insulin-related peptides by the neuroendocrine light green cells of Lymnaea stagnalis Gen. Comp. Endocrinol. 87 1992 79 86
42. Lindstrom-Dinnetz, I., Iatrou, K., 1997. Cloning and functional characterization of an insulin receptor-like mRNA expressed in the silkworm ovary. Unpublished, Genbank accession no. AF025542.
43. M. Loir, and F. Le Gac Insulin-like factor-I and -II binding and action on DNA synthesis in rainbow trout spermatogonia and spermatocytes Biol. Reprod. 51 6 1994 1154 1163
44. P. Lubet Recherches sur le cycle sexuel et l'émission des gamètes chez les Mytilidés et les Pectinidés Rev. Trav. I.S.T.P.M. 23 3 1959 387 548
45. P. Lubet, and M. Mathieu The action of internal factors on gametogenesis in Pelecypod molluscs Malacologia 22 1982 131 136
46. M.A. Maestro, E. Mendez, J.V. Planas, and J. Gutierrez Dynamics of insulin and insulin-like growth factor-I (IGF-I) ovarian receptors during maturation in the brown trout (Salmo trutta) Fish Physiol. Biochem. 20 1999 341 349
47. M. Marin-Hincapie, and R.S. Garofalo The carboxyl terminal extension of the Drosophila insulin receptor homologue binds IRS-1 and influences cell survival J. Biol. Chem. 274 35 1999 24987 24994
48. K. Maruyama, H. Nagasawa, A. Isogai, S. Tamura, H. Ishizaki, and A. Suzuki Synthesis of bombyxin-IV, an insulin-like heterodimeric peptide from the silkworm, Bombyx mori Peptides 11 1990 169 171
49. K. Maruyama, H. Nagasawa, A. Isogai, H. Ishizaki, and A. Suzuki Determination of disulfide bond arrangement in bombyxin-IV, an insulin superfamily peptide from the silkworm, Bombyx mori, by combination of thermolysin digestion of natural peptide and selective synthesis of disulfide bond isomers J. Protein Chem. 11 1 1992 13 20
50. K. Maruyama, K. Nagata, M. Tanaka, H. Nagasawa, A. Isogai, H. Ishizaki, and A. Suzuki Synthesis of bombyxin-IV, an insulin superfamily peptide from the silkworm, Bombyx mori, by stepwise and selective formation of three disulfide bridges J. Protein Chem. 11 1 1992 1 12
51. M. Mathieu, F. Lenoir, and I. Robbins A gonial mitosis stimulating factor in cerebral ganglia and hemolymph of the marine mussel Mytilus edulis Gen. Comp. Endocrinol. 72 1988 257 263
52. D.S. Miller Stimulation of RNA and protein synthesis by intracellular insulin Science 240 4851 1988 506 509
53. D.S. Miller Stimulation of protein synthesis in stage IV Xenopus oocytes by microinjected insulin J. Biol. Chem. 264 18 1989 10438 10446
54. Z. Monnier, and M. Bride In vitro effects of methionine-enkephalin, somatostatin and insulin on cultured gonadal cells of the snail Helix aspersa Experientia 51 1995 824 829
55. S. Moriyama, H. Shimma, M. Tagawa, and H. Kagawa Changes in plasma insulin-like growth factor-I levels in the precociously maturing amago salmon, Oncorhynchus masou ishikawai Fish Physiol. Biochem. 17 1997 253 259
56. T. Mosmann Rapid colorimetric assay for cellular growth and survival: application to proliferation and toxicity assays J. Immunol. Methods 65 1983 55 63
57. H. Nagasawa, H. Kataoka, Y. Hori, A. Isogai, S. Tamura, A. Suzuki, F. Guo, X.C. Zong, A. Mizoguchi, and M. Fujishita Isolation and some characterization of the prothoracicotropic hormone from Bombyx mori Gen. Comp. Endocrinol. 53 1984 143 152
58. H. Nagasawa, H. Kataoka, A. Isogai, S. Tamura, Ak. Suzuki, A. Mizoguchi, Y. Fujiwara, At. Suzuki, S.Y. Takahashi, and H. Ishizaki Amino acid sequence of a prothoracicotropic hormone of the silkworm Bombyx mori Proc. Natl. Acad. Sci. U. S. A. 83 1986 5840 5843
59. K. Nagata, K. Maruyama, K. Kojima, M. Yamamoto, M. Tanaka, H. Kataoka, H. Nagasawa, A. Isogai, H. Ishizaki, and A. Suzuki Prothoracicotropic activity of SBRPs, the insulin-like peptides of the saturniid silkworm Samia cynthia ricini Biochem. Biophys. Res. Commun. 266 2 1999 575 578
60. Y. Nishida, M. Hata, Y. Nishizuka, W.J. Rutter, and Y. Ebina Cloning of a Drosophila cDNA encoding a polypeptide similar to the human insulin receptor precursor Biochem. Biophys. Res. Commun. 141 2 1986 474 481
61. P.D. Niu, J. Perez-Sanchez, and P.Y. Le Bail Development of protein binding assay for teleost insulin-like growth factor (IGF-like): relationships between growth hormone (GH) and IGF-like in the blood of rainbow trout (Oncorhynchus mykiss) serum Fish Physiol. Biochem. 11 1993 380 391
62. C. Orikasa, H. Yamauchi, H. Nagasawa, A. Suzuki, and M. Nagata Induction of oocyte-nurse cell differentiation in the ovary by the brain during the initial stage of oogenesis in the silkworm, Bombyx mori (Lepidoptera: bombycidae) Appl. Entomol. Zool. 28 1993 303 311
63. A.J. Pazos, and M. Mathieu Effects of five natural Gonadotropin-Releasing Hormones on cell suspensions of marine bivalve gonad: stimulation of gonial DNA synthesis Gen. Comp. Endocrinol. 113 1999 112 120
64. V. Perrot, E. Borisovna, Y. Gozes, S.J. Chan, and B. Funkenstein Insulin-like Growth Factor receptors and their ligands in gonads of a hermaphroditic species, the Gilthead Seabream (Sparus aurata): expression and cellular localization Biol. Reprod. 63 2000 229 241
65. L. Petruzzelli, R. Herrera, R. Arenas-Garcia, R. Fernandez, J. Birnbaum, and O.M. Rosen Isolation of a Drosophila genomic sequence homologous to the kinase domain of the human insulin receptor and detection of the phosphorylated Drosophila receptor with an anti-peptide antibody Proc. Natl. Acad. Sci. 83 1986 4710 4714
66. S.B. Pierce, M. Costa, R. Wizotskey, S. Devadhar, S.A. Homburger, A.R. Buchman, K.C. Ferguson, J. Heller, D.M. Platt, A.A. Pasquinelli, L.X. Liu, S.K. Doberstein, and G. Ruvkun Regulation of DAF-2 receptor signaling by human insulin and ins-1, a member of the unusually large and diverse C. elegans insulin gene family Genes Dev. 15 2001 672 686
67. M.A. Riehle, and M.R. Brown Insulin stimulates ecdysteroid production through a conserved signalling cascade in the mosquito Aedes aegypti Insect Biochem. Mol. Biol. 29 1999 855 860
68. M.A. Riehle, and M.R. Brown Insulin receptor expression during development and a reproductive cycle in the ovary of the mosquito Aedes aegypti Cell Tissue Res. 308 3 2002 409 420
69. A. Robitzki, H.C. Schroder, D. Ugarkovic, K. Pfeifer, G. Uhlenbruck, and W.E.G. Muller Demonstration of an endocrine signalling circuit for insulin in the sponge Geodia cydonium EMBO J. 2 1989 2905 2909
70. E. Roovers, M.E. Vincent, E. van Kesteren, W.P.M. Geraerts, R.J. Planta, E. Vreugdenhil, and H. van Heerikhuizen Characterization of a putative molluscan insulin-related peptide receptor Gene 162 1995 181 188
71. Y. Ruan, C. Chen, Y. Cao, and R.S. Garofalo The Drosophila insulin receptor contains a novel carboxyl-terminal extension likely to play an important role in signal transduction J. Biol. Chem. 270 9 1995 4236 4243
72. S.E. Sadler, and J.L. Maller In vivo regulation of cyclic AMP phosphodiesterase in Xenopus oocytes. Stimulation by insulin and insulin-like growth factor 1 J. Biol. Chem. 262 22 1987 10644 10650
73. H. Saegusa, A. Mizoguchi, H. Kitahora, H. Nagasawa, A. Suzuki, and H. Ishizaki Changes in titer of bombyxin-immunoreactive material in hemolymph during the postembryonic development of the silkmoth Bombyx mori Dev. Growth Differ. 34 5 1992 595 605
74. G. Scavo, A.R. Shuldiner, J. Serrano, R. Dashner, J. Roth, and F. De Pablo Genes encoding receptors for insulin and insulin-like growth factor I are expressed in Xenopus oocytes and embryos Proc. Natl. Acad. Sci. U. S. A. 88 1991 6214 6218
75. H. Schäcke, H.C. Schroder, V. Gamulin, B. Rinkevich, I.M. Müller, and W.E. Müller Molecular cloning of a tyrosine kinase gene from the marine sponge Geodia cydonuim: a new member belonging to the receptor tyrosine kinase class II family Mol. Membr. Biol. 11 2 1994 101
76. V.M. Sevala, and B.G. Loughton Insulin-like peptides during oogenesis and embryogenesis in Locusta migratoria Invertebr. Reprod. Dev. 21 3 1992 187 192
77. A. Skorokhod, V. Gamulin, D. Gundacker, V. Kavsan, I.M. Müller, and W.E.G. Müller Origin of insulin receptor-like tyrosine kinases in marine sponges Biol. Bull. 197 1999 198 206
78. A.B. Smit, E. Vreugdenhil, R.H.M. Ebberink, W.P.M. Geraerts, J. Klootwijk, and J. Joosse Growth-controlling molluscan neurons produce the precursor of an insulin-related peptide Nature 331 1988 535 538
79. A.B. Smit, R.E. van Kesteren, K.W. Li, J. van Minnen, S. Spijker, H. van Heerikhuizen, and W.P.M. Geraerts Towards understanding the role of insulin in the brain: lessons from insulin-related signaling systems in the invertebrate brain Prog. Neurobiol. 54 1998 35 54
80. D. Sonetti, W.R.A. van Heumen, and E.W. Roubos Light- and electro-microscopic immunocytochemistry of a molluscan insulin-related peptide in the central nervous system of Planorbarius corneus Cell Tissue Res. 267 1992 473 481
81. R.E. Steele, P. Lieu, N.H. Mai, M.A. Shenk, and M.P. Sarras Jr. Response to insulin and the expression pattern of a gene encoding an insulin receptor homolog suggest a role for an insulin-like molecule in regulating growth and patterning in Hydra Dev. Genes Evol. 206 1996 247 259
82. M. Tanaka, H. Kataoka, K. Nagata, H. Nagasawa, and A. Suzuki Morphological changes of BM-N4 cells induced by bombyxin, an insulin-related peptide of Bombyx mori Regul. Pept. 57 1995 311 318
83. S. Tsuzuki, T. Masuta, M. Furuno, S. Sakurai, and M. Iwami Structure and expression of Bombyxin E1 gene: a novel family gene that encodes bombyxin-IV, an insect insulin-related neurosecretory peptide Comp. Biochem. Physiol., Part B Biochem. Mol. Biol. 117 3 1997 409 416
84. C. Tyler, J. Sumpter, and N. Bromage The hormonal control of vitellogenic uptake into cultured oocytes of the rainbow trout Proc. 3rd Int. Reproductive Physiology of Fish 1987 Memorial University Press St-John's, Newfoundland 142 pp.
85. J. van Minnen, and H.D.F.H. Schallig Demonstration of insulin-related substances in the central nervous systems of pulmonates and Aplysia californica Cell Tissue Res. 260 1990 381 386
86. J. Wijdenes, N.C. Schluler, L. Gomot, and H.H. Boer In the snail Helix aspersa the gonadotropic hormone-producing dorsal bodies are under inhibitory nervous control of putative growth hormone-producing neuroendocrine cells Gen. Comp. Endocrinol. 68 2 1987 224 229
87. I. Yoshida, S. Tsuzuki, S.E. Abdel Salam, M. Ino, A.M. Korayem, S. Sakurai, and M. Iwami Bombyxin F1 gene: structure and expression of a new bombyxin family gene that forms a pair with bombyxin B10 gene Zool. Sci. 14 4 1997 615 622
88. I. Yoshida, K. Moto, S. Sakurai, and M. Iwami A novel member of a bombyxin gene family: structure and expression of a bombyxin G1 gene, an insulin-related peptide gene of the silkmoth Bombyx mori Dev. Genes Evol. 208 7 1998 407 410
89. D. Zachary, F. Goltzene, F.C. Holder, J.P. Berchtold, H. Nagasawa, A. Suzuki, H. Misoguchi, H. Ishizaki, and J.A. Hoffmann Presence of bombyxin (4K-PTTH)-like molecules in neurosecretory granules of brain-corpora cardiaca complexes of Locusta migratoria: developmental aspects Int. J. Invertebr. Reprod. Dev. 14 1988 1 10
90. X.X. Zhu, and J.H. Olivier Jr. Immunocytochemical localization of an insulin-like substance in the synganglion of the tick Ornithodoros parkeri (Acari: Argasidae) Exp. Appl. Acarol. 13 1991 153 159