Fisheries and Aquatic Sciences

The Korean Society of Fisheries and Aquatic Science (한국수산과학회)
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Role of the insulin-like growth factor system in gonad sexual maturation in Pacific oyster Crassostrea gigas

  • Moon, Ji-Sung (Department of Fisheries Biology, Pukyong National University) ;
  • Choi, Youn Hee (Department of Fisheries Biology, Pukyong National University)
  • Received : 2020.01.06
  • Accepted : 2020.02.13
  • Published : 2020.02.28
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Abstract

Background: The IGF system plays important roles in controlling growth, development, reproduction, and aging of organisms. Methods: To estimate maturation of the Pacific oyster Crassostrea gigas, we investigated the expression of insulin-like growth factor (IGF) system components and sex-specific genes. To determine the role of the IGF system in the growth and spawning period of female and male oysters, we examined mRNA expression levels of the C. gigas insulin receptor-related receptor (CIR), IGF binding protein complex acid labile subunit (IGFBP_ALS), and molluscan insulin-related peptide (MIP), as well as those of vitellogenin (Vg) and receptor-type guanylate cyclase (Gyc76C) in gonads of C. gigas collected between April and October, when sex can be determined visually in this species. Results: We found that MIP, IGFBP_ALS, and CIR mRNA expression levels were dependent on sex and month and were greater in males than in females. CIR and Vg mRNA expression levels were very similar among females, whereas IGF system components and Gyc76C were very similarly expressed among males. The highest expression values were observed in May, when oysters are mature; CIR and Vg mRNA expression levels were highest in females, and those of MIP, IGFBP_ALS, CIR, and Gyc76C were highest in males. Interestingly, we observed a 1:1 proportion of females to males during this period. Conclusion: Our results suggest that IGF system components, as well as Vg and Gyc76C, are associated with sexual maturation in C. gigas.

Keywords

References

  1. Ayoob JC, Yu HH, Terman JR, Kolodkin AL. The Drosophila receptor guanylyl cyclase Gyc76C is required for semaphoring-1a-plexin A-mediated axonal repulsion. J Neurosci. 2004;24:6639-49. https://doi.org/10.1523/JNEUROSCI.1104-04.2004
  2. Baxter RC. Insulin-like growth factor binding proteins in the human circulation: a review. Horm Res. 1994;42:140-4. https://doi.org/10.1159/000184186
  3. Bayne BL. Physiological components of growth differences between individual oysters (Crassostrea gigas) and a comparison with Saccostrea commercialis. Physiol Biochem Zool. 1999;72:705-13. https://doi.org/10.1086/316714
  4. Boag PR, Newton SE, Gasser RB. Molecular aspects of sexual development and reproduction in nematodes and schistosomes. Advan Parasitol. 2001;50:153-98. https://doi.org/10.1016/S0065-308X(01)50031-7
  5. Boutet I, Moraga D, Marinovic L, Obreque J, Chavez-Crooker P. Characterization of reproduction-specific genes in a marine bivalve mollusc: influence of maturation stage and sex on mRNA expression. Gene. 2008;407:130-8. https://doi.org/10.1016/j.gene.2007.10.005
  6. Brogiolo W, Stocker H, Ikeya T, Rintelen F, Fernandez R, Hafen E. An evolutionarily conserved function of the Drosophila insulin receptor and insulin-like peptides in growth control. Curr Biol. 2001;11:213-21. https://doi.org/10.1016/S0960-9822(01)00068-9
  7. Canesi L, Betti M, Ciacci C, Gallo G. Insulin-like effect of zinc in Mytilus digestive gland cells: modulation of tyrosine kinase-mediated cell signaling. Gen Comp Endocrinol. 2001;122:60-6. https://doi.org/10.1006/gcen.2001.7612
  8. Canesi L, Ciacci C, Betti M, Malatesta M, Gazzanelli G, Gallo G. Growth factors stimulate the activity of key glycolytic enzymes in isolated digestive gland cells from mussels (Mytilus galloprovincialis Lam.) through tyrosine kinase mediated signal transduction. Gen Comp Endocrinol. 1999;116:241-8. https://doi.org/10.1006/gcen.1999.7366
  9. Canesi L, Ciacci C, Orunesu M, Gallo G. Effects of epidermal growth factor on isolated digestive gland cells from mussels (Mytilus galloprovincialis Lam.). Gen Comp Endocrinol. 1997;107:221-8. https://doi.org/10.1006/gcen.1997.6918
  10. Cherif-Feildel M, Berthelin H, Adeline B, Riviere G, Favrel P, Kellner K. Molecular evolution and functional characterization of insulin related peptides in molluscs: contributions of Crassostrea gigas genomic and transcriptomicwide screening. Gen Comp Endocrinol. 2019;271:15-29. https://doi.org/10.1016/j.ygcen.2018.10.019
  11. Choi YH, Kim EY, Nam TJ. Involvement of insulin-like growth factor in intraspecific variation in growth of Pacific oyster Crassostrea gigas during winter. Fish Sci. 2018;84:1017-24. https://doi.org/10.1007/s12562-018-1232-3
  12. Choi YH, Yamaguchi K, Oda T, Nam TJ. Chemical and mass spectrometry characterization of the red alga Pyropia yezoensis chemoprotective protein (PYP): protective activity of the N-terminal fragment of PYP1 against acetaminophen-induced cell death in Chang liver cells. Int J Mol Med. 2015;35:271-6. https://doi.org/10.3892/ijmm.2014.1992
  13. Chung JS. An insulin-like growth factor found in hepatopancreas implicates carbohydrate metabolism of the blue crab Callinectes sapidus. Gen Comp Endocrinol. 2014;199:56-64. https://doi.org/10.1016/j.ygcen.2014.01.012
  14. Davis LK, Pierce AL, Hiramatsu N, Sullivan CV, Hirano T, Grau EG. Gender-specific expression of multiple estrogen receptors, growth hormone receptors, insulin-like growth factors and vitellogenins, and effects of $17{\beta}$-estradiol in the male tilapia (Oreochromis mossambicus). Gen Comp Endocrinol. 2008;156:544-51. https://doi.org/10.1016/j.ygcen.2008.03.002
  15. Deeming DC. Egg incubation: its effects on embryonic development in birds and reptiles. UK: Cambridge University Press; 1991. p. 448.
  16. Duan C. The insulin-like growth factor system and its biological actions in fish. Am Zool. 1997;37:491-503. https://doi.org/10.1093/icb/37.6.491
  17. Feng L, Li X, Yu Q, Ning X, Dou J, Zou J, Zhang L, Wang S, Hu X, Bao Z. A scallop IGF binding protein gene: molecular characterization and association of variants with growth traits. PLoS One. 2014;9:e89039. https://doi.org/10.1371/journal.pone.0089039
  18. Food and Agriculture Organization. http://www.fao.org (2020). Accessed 29 January 2020.
  19. Forbes BE, McCarthy P, Norton RS. Insulin-like growth factor binding proteins: a structural perspective. Front Endocrinol. 2012;3:1-13. https://doi.org/10.3389/fendo.2012.00001
  20. Geraerts WP. Control of growth by the neurosecretory hormone of the light green cells in the freshwater snail Lymnaea stagnalis. Gen Comp Endocrinol. 1976;29:61-71. https://doi.org/10.1016/0016-6480(76)90007-1
  21. Geraerts WP. Neurohormonal control of growth and carbohydrate metabolism by the light green cells in Lymnaea stagnalis. Gen Comp Endocrinol. 1992;86:433-44. https://doi.org/10.1016/0016-6480(92)90068-U
  22. Geraerts WP, Smit AB, Li KW, Hordijk PL. The light green cells of Lymnaea: a neuroendocrine model system for stimulus-induced expression of multiple peptide genes in a single cell type. Experientia. 1992;48:464-73. https://doi.org/10.1007/BF01928165
  23. Gigliotti S, Cavaliere V, Manzi A, Tino A, Graziani F, Malva C. A membrane guanylate cyclase Drosophila homolog gene exhibits maternal and zygotic expression. Dev Biol. 1993;159:450-61. https://doi.org/10.1006/dbio.1993.1255
  24. Gricourt L, Bonnec G, Boujard D, Mathieu M, Kellner K. 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. 2003;134:44-56. https://doi.org/10.1016/S0016-6480(03)00217-X
  25. Gronke S, Clarke DF, Broughton S, Andrews TD, Partridge L. Molecular evolution and functional characterization of Drosophila insulin-like peptides. PLoS Genet. 2010;6:e1000857. https://doi.org/10.1371/journal.pgen.1000857
  26. Hadley ME. Endocrinology: 2nd ed. Prentice-Hall, Englewood Cliffs, NJ, 1988. 550 pp. In General and Comparative Endocrinology 1988;72:329-329.
  27. Hartman D, Donald DR, Nikolaou S, Savin KW, Hasse D, J.A Presidente P, Newton SE. Analysis of developmentally regulated genes of the parasite Haemonchus contortus. Int J Parasitol. 2001;31:1236-45. https://doi.org/10.1016/S0020-7519(01)00248-X
  28. Harumi T, Watanabe T, Yamamoto T, Tanabe Y, Suzuki N. Expression of membrane-bound and soluble guanylyl cyclase mRNAs in embryonic and adult retina of the medaka fish Oryzias latipes. Zool Sci. 2003;20:133-40. https://doi.org/10.2108/zsj.20.133
  29. Huang X, Ye H, Feng B, Huang H. Insights into insulin-like peptide system in invertebrates from studies on IGF binding domain-containing proteins in the female mud crab, Scylla paramamosain. Mol Cell Endocrinol. 2015;416:36-45. https://doi.org/10.1016/j.mce.2015.08.019
  30. Jouaux A, Franco A, Heude-Berthelin C, Sourdaine P, Blin JL, Mathieu M, Kellner K. Identification of Ras, Pten and p70S6K homologs in the Pacific oyster Crassostrea gigas and diet control of insulin pathway. Gen Comp Endocrinol. 2012;176:28-38. https://doi.org/10.1016/j.ygcen.2011.12.008
  31. Krieger MJB, Jahan N, Riehle MA, Cao C, Brown MR. Molecular characterization of insulin-like peptide genes and their expression in the African malaria mosquito, Anopheles gambiae. Insect Mol Biol. 2004;13:305-15. https://doi.org/10.1111/j.0962-1075.2004.00489.x
  32. Leevers SJ. Growth control: invertebrate insulin surprises. Curr Biol. 2001;11:R209-12. https://doi.org/10.1016/S0960-9822(01)00107-5
  33. Macdonald BA, Thompson RJ. Intraspecific variation in growth and reproduction in latitudinally differentiated populations of the giant scallop Placopecten magellanicus (Gmelin). Biol Bull. 1988;175:361-71. https://doi.org/10.2307/1541727
  34. Marquez AG, Pietri JE, Smithers HM, Nuss A, Antonova Y, Drexler AL, Riehle MA, Brown MR, Luckhart S. Insulin-like peptides in the mosquito Anopheles stephensi: identification and expression in response to diet and infection with Plasmodium falciparum. Gen Comp Endocrinol. 2011;173:303-12. https://doi.org/10.1016/j.ygcen.2011.06.005
  35. Matozzo V, Gagne F, Marin MG, Ricciardi F, Christian BC. Vitellogenin as a biomarker of exposure to estrogenic compounds in aquatic invertebrates: a review. Environ Int. 2008;34:531-45. https://doi.org/10.1016/j.envint.2007.09.008
  36. Min KS, Kim BS, Kim TI, Hur YB, Chung EY. Reproductive cycle and induced sexual maturation of the Pacific oyster. Crassostrea gigas. 2004;20:75-84.
  37. Ministry of Oceans and Fisheries. http://www.mof.go.kr (2020). Accessed 29 January 2020.
  38. Myat MM, Patel U. Receptor-type guanylyl cyclase at 76C (Gyc76C) regulates De Novo lumen formation during Drosophila tracheal development. PLoS ONE. 2016;11:e0161865. https://doi.org/10.1371/journal.pone.0161865
  39. Nagasawa H, Kataoka H, Isogai A, Tamura S, Suzuki A, Mizoguchi A, Fujiwara Y, Suzuki A, Takahashi SY, Ishizaki H. Amino acid sequence of a prothoracicotropic hormone of the silkworm Bombyx mori. PNAS USA. 1986;83:5840-3. https://doi.org/10.1073/pnas.83.16.5840
  40. Nassel DR, Liu Y, Luo J. Insulin/IGF signaling and its regulation in Drosophila. Gen Comp Endocrinol. 2015;221:255-66. https://doi.org/10.1016/j.ygcen.2014.11.021
  41. Ni J, Zeng Z, Kong D, Hou L, Huang H, Ke C. Vitellogenin of Fujian oyster, Crassostrea angulata: synthesized in the ovary and controlled by estradiol-$17{\beta}$. Gen Comp Endocrinol. 2014;202:35-43. https://doi.org/10.1016/j.ygcen.2014.03.034
  42. Nisbet AJ, Gasser RB. Profiling of gender-specific gene expression for Trichostrongylus vitrinus (Nematoda: Strongylida) by microarray analysis of expressed sequence tag libraries constructed by suppressive-subtractive hybridisation. Int J Parasitol. 2004;34:633-43. https://doi.org/10.1016/j.ijpara.2003.12.007
  43. Patel U, Davies SA, Myat MM. Receptor-type guanylyl cyclase Gyc76C is required for development of the Drosophila embryonic somatic muscle. Biol Open. 2012;1:507-15. https://doi.org/10.1242/bio.2012943
  44. Qin Z, Li Y, Sun D, Shao M, Zhang Z. Cloning and expression analysis of the vitellogenin gene in the scallop Chlamys farreri and the effects of estradiol-$17{\beta}$ on its synthesis. Inverte Biol. 2012;131:312-21. https://doi.org/10.1111/ivb.12006
  45. Renteria ME, Gandhi NS, Vinuesa P, Helmerhorst E, Mancera RL. A comparative structural bioinformatics analysis of the insulin receptor family ectodomain based on phylogenetic information. 2008;3:e3667. https://doi.org/10.1371/journal.pone.0003667
  46. Roovers E, Vincent ME, van Kesteren E, Geraerts WP, Planta RJ, Vreugdenhil E, van Heerikhuizen H. Characterization of a putative molluscan insulin-related peptide receptor. Gene. 1995;11:81-8. https://doi.org/10.3390/genes11010081
  47. Schleede J, Blair SS. The Gyc76C receptor guanylyl cyclase and the foraging cGMP-dependent kinase regulate extracellular matrix organization and BMP signaling in the developing wing of Drosophila melanogaster. PLOS Gene. 2015;11:e1005576. https://doi.org/10.1371/journal.pgen.1005576
  48. Tran TQ, Boring RL, Dudenhoeffer DD, Hallbert BP, Keller MD, Anderson TM. Advantages and disadvantages of physiological assessment for next generation control room design. Hfpp HPRCT 13th Annual Meeting 2007;IEEE 8th.
  49. Ventura T, Rosen O, Sagi O. From the discovery of the crustacean androgenic gland to the insulin-like hormone in six decades. Gen Comp Endocrinol. 2011;173:381-8. https://doi.org/10.1016/j.ygcen.2011.05.018
  50. Williamson TR, Tilley DR, Campbell E. Emergy analysis to evaluate the sustainability of two oyster aquaculture systems in the Chesapeake Bay. Ecol Eng. 2015;85:103-20. https://doi.org/10.1016/j.ecoleng.2015.09.052
  51. Wu A, Brown MR. Signaling and function of insulin-like peptides in insects. Annual Review Entomol. 2006;51:1-24. https://doi.org/10.1146/annurev.ento.51.110104.151011
  52. Zheng H, Zhang Q, Liu H, Liu W, Sun Z, Li S, Zhang T. Cloning and expression of vitellogenin (Vg) gene and its correlations with total carenoids content and total antioxidant capacity in noble scallop Chlamys nobilis (Bivalve:Pectinidae). Aquaculture. 2012;366-367:46-53. https://doi.org/10.1016/j.aquaculture.2012.08.031
  53. Zhu HH, Ma GX, Luo YF, Luo YL, Yin SS, Xiong Y, Zhou RQ. Tissue distribution and functional analysis of vitellogenin-6 of Toxocara canis. Exp Parasitol. 2017;177:22-7. https://doi.org/10.1016/j.exppara.2017.03.009

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