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Feed restriction and insulin-like growth factor-I (IGF-I) affect the oocyte maturation in matrinxã Brycon amazonicus

Published online by Cambridge University Press:  08 December 2016

Luís Henrique Montrezor  and
Elisabeth Criscuolo Urbinati
Luís Henrique Montrezor*
Affiliation:
University of Araraquara, UNIARA, Department of Biological Science and Health – Medicine, Rua Voluntários da Pátria, 1309, 140801-320 – Araraquara – SP, Brazil. Medical Chemistry and Regenerative Medicine Group, QUIMMERA, UNIARA, Araraquara, São Paulo, Brazil.
Elisabeth Criscuolo Urbinati
Affiliation:
Department of Animal Morphology and Physiology/Aquaculture Center (CAUNESP), University of Estadual Paulista, UNESP, Jaboticabal, São Paulo, Brazil.
*
All correspondence to: Luís Henrique Montrezor. University of Araraquara, UNIARA, Department of Biological Science and Health – Medicine, Rua Voluntários da Pátria, 1309, 140801-320 – Araraquara – SP, Brazil. Tel: +55 16 33017300 – 7351. E-mail: [email protected]
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Summary

The feeding and nutrition of breeders are crucial aspects in the reproductive process. During the maturation period, metabolic changes occur aiming at mobilizing energy for growth and follicular development. The involvement of IGF-1 in metabolic and reproductive events is important. The aim of this work was to evaluate if alternate feed restriction and re-feeding have permissive effects on in vitro actions of IGF-1 on oocytes development of matrinxã. In vivo experiments were performed during vitellogenesis period. Females (n = 60) were fed with a commercial feed (2% of biomass) and they were divided into two treatments: fish receiving food daily (control – fed), and fish submitted to cycles of 3 days of feed restriction and 2 days of re-feeding (no-fed group). For the in vitro experiments, oocytes (n = 20) were obtained from the ovaries removed at the end of the in vivo experiment and were divided into four groups: fed –IGF-1; fed +IGF-1; no-fed –IGF-1 and no-fed +IGF-1. Fish under restriction had lower body weights, decreased plasma glucose, increased triglycerides levels, and their final maturation and mature oocyte were reduced and the atresic ones were in higher number. Moreover, IGF-1, in vitro, increased the percentage of mature oocytes in fed females and decreased the atresic ones. In no-fed females, IGF-1 increased the final maturation and mature oocytes and reduced the atresic ones. This study demonstrates the importance of the feeding management of female breeders of matrinxã during the vitellogenesis period.

Keywords

FishFood restrictionIGF-1MatrinxãOocyte development
Type
Research Article
Information
Zygote , Volume 25 , Issue 1 , February 2017 , pp. 56 - 64
Copyright
Copyright © Cambridge University Press 2016 

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References

Berishivili, G., D'Cotta, H., Baroiller, J.F., Segner, H. & Reinecke, M. (2006). Differential expression of IGF-I mRNA and peptide in the male and female gonad during early development of bony fish, the tilapia Oreochromis niloticus . Gen. Comp. Endocrinol. 146, 204–10.Google Scholar
Camargo, A.C.S. & Urbinati, E.C. (2008). Influence of food restriction on the reproduction and larval performance of matrinxã, Brycon cephalus (Spix and Agassiz, 1829). Braz. J. Biol. 68, 869–73.Google Scholar
Celik, O., Aydin, S., Celik, N. & Yilmaz, M. (2015). Peptides: basic determinants of reproductive functions. Peptides 72, 34–43.Google Scholar
Danforth, E. Jr. & Burger, A.G. (1989). The impact of nutrition on thyroid hormone physiology and action. Ann. Rev. Nutr. 9, 201–27.Google Scholar
Davoren, J.B., Kasson, B.G., Li, C.H & Hsueh, A.J.W. (1986). Specific insulin-like growth factor (IGF) I and II-binding sites on rat granulosa cells: relation to IGF action. Endocrinology 119, 2155–62.Google Scholar
Dyer, A.R., Barlow, C.G., Bransden, M.P., Carter, C.G., Glencross, B.D., Richardson, N. Thomas, P.M., Williams, K.C. & Carragher, J.F. (2004). Correlation of plasma IGF-1 concentrations and growth rat in aquaculture finfish: a tool for assessing the potential of new diets. Aquaculture 236, 583–92.Google Scholar
FAO (2012). The State of World Fisheries and Aquaculture Food and Agriculture Organization of the United Nations, Rome (209 pp).Google Scholar
Ghigo, E., Miola, C., Aimaretti, G., Valente, F., Procopio, M., Arvat, E., Yin-Zhang, W. & Cammani, F. (1992). Arginine abolishes the inhibitory effect of glucose in the growth hormone response to growth hormone-releasing hormone in man. Metab. Clin. Exp. 41, 1000–3.Google Scholar
Ginther, O.J., Beg, M.A., Bergfelt, D.R., Donadeu, F.X. & Kot, K. (2001). Follicle selection on monovular species. Biol. Reprod. 65, 638–47.Google Scholar
Hammond, J.M., Lino, J., Baranao, S., Sakaleris, D., Knight, A.B., Romanus, J.A. & Recher, R.R. (1985). Production of insulin-like growth factors by ovarian granulosa cells. Endocrinology 117, 2553–5.Google Scholar
Kagawa, H., Kobayashi, M., Hasegawa, Y. & Aida, K. (1994). Insulin and insulin-like growth factor I and II induce final maturation of oocytes of red sea bream, Pargus major, in vitro. Gen. Comp. Endocrinol. 95, 293–300.Google Scholar
Kagawa, H., Moriyama, S. & Kawauchi, H. (1995). Immunocytochemical localization of IGF-I in the ovary of the red sea bream, Pargus major. Gen. Comp. Endocrinol. 99, 307–15.Google Scholar
Kagawa, H., Gen, K. & Tanaka, H. (2003). Effects of luteinizing hormone and follicle stimulating-hormone and insulin-like growth factor-I on aromatase activity and P450 aromatase gene expression in the ovarian follicle of red sea bream, Pargus major. Biol. Reprod. 68, 1562–8.Google Scholar
Kagamar, B.B., Rasaee, M.J., Amiri, B.M., Abtahi, B. & Bahmani, M. (2007). Correlations between circulating insulin-like growth factor-I and thyroxine and cortisol hormones levels, and some biometrical traits in female brood stocks during the late stages of sex maturation and in juvenile Persian sturgeon (Acipenser persicus). Fish Physiol. Biochem. 33, 249–57.Google Scholar
Kamangar, B.B., Gabilard, J.C. & Bobe, J. (2006). Insulin-like growth factor-binding protein (IGFBP)-1, -2, -3, -4, -5, and -6 and IGFBP-related protein 1 during rainbow trout postvitellogenesis and oocyte maturation: molecular characterization, expression profiles, and hormonal regulation. Endocrinology 147, 2399–410.Google Scholar
Lubzen, E., Young, G., Bobe, J. & Cerdà, J. (2010). Oogenesis in teleosts: how fish eggs are formed. Gen. Comp. Endocrinol. 165, 367–89.CrossRefGoogle Scholar
MacKenzie, D.S., Van Putte, C.M. & Leiner, K.A. (1998). Nutrient regulation of endocrine function in fish. Aquaculture 161, 3–25.CrossRefGoogle Scholar
Maestro, M.A., Méndez, E., Párrizas, M. & Gutiérrez, J. (1997a). Characterization of insulin and insulin-like growth factor-I ovarian receptors during the reproductive cycle of carp (Cyprinus carpio). Biol. Reprod. 56, 1126–32.Google Scholar
Maestro, M.A., Planas, J.V., Moriyama, S., Gutiérrez, J., Planas, J. & Swanson, P. (1997b). Ovarian receptors for insulin-like growth factor-I (IGF-I) and effects of IGF-I on steroid production by isolated follicle layers of the preovulatory Coho salmon follicle. Gen. Comp. Endocrinol. 106, 189–201.Google Scholar
McIntosh, C.H.S. (1995). Control of gastric acid secretion and the endocrine pancreas by gastrointestinal regulatory peptides. Am. Zool. 35, 455–65.Google Scholar
Miwa, T., Yoshizaki, G., Naka, H., Nakatani, M., Sakai, K., Kobayashi, M. & Takeuchi, T. (2001). Ovarian steroid synthesis during oocyte maturation and ovulation in Japanese catfish (Silurus asotus). Aquaculture 198, 179–91.Google Scholar
Montrezor, L.H., Piccinato, C.A., Collares, C.V.A., Vireque, A.A. & Rosa e Silva, A.A.M. (2014). Comparison of medium supplementation on proliferation and hormone production of bovine granulosa cells in a defined culture system. J. Sci. Res. Rep. 3, 645–59.Google Scholar
Montrezor, L.H., Piccinato, C.A., Collares, C.V.A., Vireque, A.A. & Rosa e Silva, A.A.M. (2015). Effects of angiotensin II, atrial natriuretic peptide and endothelin-1 on proliferation and steroidogenic output of bovine granulosa cells cultured in a chemically defined system. Ann. Reprod. Sci. 152, 8–16.Google Scholar
Nakamura, I., Kusakabe, M. & Young, G. (2003). Regulation of steroidogenic enzyme mRNAs in rainbow trout (Oncorhynchus mykiss) ovarian follicles in vitro . Fish Physiol. Biochem. 28, 355–6.Google Scholar
Navarro, I. & Gutiérrez, J. (1995). Fasting and starvation. In Hochachka, P.W. & Mommsen, T.P. (Eds), Biochemistry and Molecular Biology of Fishes, vol. 4. Elsevier, Amsterdam, pp. 393–434.Google Scholar
Naylor, R.L., Goldburg, R.J., Primavera, J.H., Kautsky, N., Beveridge, M.C.M., Clay, J., Folke, C., Lubchenco, J., Mooney, H. & Troell, M. (2000). Effect of aquaculture on world fish supplies. Nature 405, 1017–24.Google Scholar
Negatu, Z., Hsiao, S.M. & Wallace, R.A. (1998). Effects of insulin-like growth factor-I on final oocyte maturation and steroid production in Fundulus heteroclitus . Fish Physiol. Biochem. 19, 13–21.Google Scholar
Pankhurst, N.W. (1997). In vitro steroid production by isolated ovarian follicles of the striped trumpeter. J. Fish Biol. 51, 669–85.Google Scholar
Patiño, R. & Kagawa, H. (1999). Regulation of gap junctions and oocyte maturational competence by gonadotropin and insulin-like growth factor-I in ovarian follicles of red sea bream. Gen. Comp. Endocrinol. 115, 454–62.CrossRefGoogle Scholar
Perrot, V., Moiseeva, E.B., Gozes, Y., Chan, S.J. & Funkenstein, B. (2000). Insulin-like growth factor receptors and their ligants in gonads of a hermaphroditic species, the gilthead sea bream (Sparus aurata): expression and cellular localization. Biol. Reprod. 63, 229–41.Google Scholar
Reindl, K.M. & Sheridan, M.A. (2012). Peripheral regulation of the growth hormone-insulin-like growth factor system in fish and other vertebrates. Comp. Biochem. Physiol. 163, 231–45.CrossRefGoogle ScholarPubMed
Roff, D.A. (1983). An allocation model of growth and reproduction in fish. Can. J. Fish Aquat. Sci. 40, 1395–403.Google Scholar
Schmid, A.C., Naef, E., Kloas, W. & Reinecke, M. (1999). IGF-I and IGF-II in the ovary of a bony fish Oreochromis mossambicus, the tilapia, in situ hybridisation, immunohistochemical localisation, northern blot and cDNA sequence. Mol. Cell. Endocrinol. 156, 141–9.Google Scholar
Urbinati, E.C., Rocha, R.M. & Carvalho, E.G. (2004). Physiological responses associated with capture and crowding stress in matrinxã Brycon cephalus (Gunther, 1869). Aquacult. Res. 35, 245–9.Google Scholar
Weber, G.M. & Sullivan, C.V. (2000). Effects of insulin-like growth factor-I on in vitro final oocyte maturation and ovarian steroidogenesis in striped bass, Morone saxatilis. Biol. Reprod. 63, 1049–57.Google Scholar
Weber, G.M. & Sullivan, C.V. (2005). Insulin-like growth factor-I induces oocyte maturational competence but not meiotic resumption in white bass (Morone chrysops) follicles in vitro: evidence for rapid evolution of insulin-like growth factor action. Biol. Reprod. 72, 1177–86.Google Scholar
Weber, G.M., Moore, A.B. & Sullivan, C.V. (2007). In vitro actions of insulin-like growth factor-I on ovarian follicle maturation in white perch (Morone americana). Gen. Comp. Endocrinol. 151, 180–7.Google Scholar
Wuertz, S., Gessner, J., Kirschbaum, F. & Kloas, W. (2007a). Expression of IGF-I and IGF-I receptor in male and female sterlet, Acipenser ruthenus – evidence for an important role in gonad maturation. Comp. Biochem. Physiol. A 147, 223–30.Google Scholar
Wuertz, S., Nitsche, A., Jastroch, M., Kesser, J., Klingenspor, M., Kirschbaum, F. & Kloas, W. (2007b). The reale of IGF-I system for vitellogenesis in maturing female sterlet, Acipenser ruthenium Linnaeus, 1758. Gen. Comp. Endocrinol. 150, 140–50.Google Scholar
Xu, Y., Zang, K., Liu, X., Shi, B., Li, C. & Shi, X. (2015). Insulin-like growth factors I and II in starry flounder (Platichthys stellatus): molecular cloning and differential expression during embryonic development. Fish Physiol. Biochem. 41, 139–52.Google Scholar