Main Article Content
Abstract
Insulin-like growth factor 1 (IGF1) is involved in various physiological functions that are regulated by somatotropic (GH-IGF1) axis. To decipher the role of IGF1 in the HPG-L axis gene encoding igf1 cDNA of female catfish, Heteropneustes fossilis, has been sequenced followed by in silico analysis as well as seasonal expression of igf1 in brain, liver and ovary organs. The mRNA expression of igf1 gene in these three organs elucidates that it plays a pivotal role in the HPG-L axis. In ovary, igf1 gene expression exhibits a direct correlation with gonadosomatic index, whereas, an inverse relationship has been observed in brain and liver tissues. Hence upregulation of igf1 in brain and liver, during the post-spawning phase and downregulation in ovary shows the shift from gonadal growth to somatic growth in resting phase. In silico analysis depicts that IGF1 is stable and hydrophilic in nature with 159 amino acid (aa) and molecular weight of 17.65 kDa. Secondary structure shows the presence of maximum random coils and alpha-helix. It is secretory protein showing maximum interaction with IGF1R, estrogen receptor alpha and GH. Protein structures of IGF1, luteinizing hormone beta (LHβ), follicle stimulating hormone beta (FSHβ) and growth hormone (GH) have been constructed and interaction among them has been docked which suggests that gonadal and somatic axes are probably interlinked and may regulate the neuroendocrine system of fish.
Keywords
Article Details
This work is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.
The authors transfer the copyrights of their papers to the Iranian Society of Ichthyology. However, the information could be used in accordance with the Creative Commons licence (Attribution-NonCommercial 4.0 International (CC BY-NC 4.0)
References
- Arukwe, A. 2001. Cellular and molecular responses to endocrine-modulators and the impact on fish reproduction. Marine Pollution Bulletin 42(8): 643-655.
- Baker, D.M.; Davies, B.; Dickhoff, W.W. & Swanson, P. 2000. Insulin-like growth factor I increases follicle-stimulating hormone (FSH) content and gonadotropin-releasing hormone-stimulated FSH release from coho salmon pituitary cells in vitro. Biology of Reproduction 63(3): 865-871.
- Berishvili, G.; Baroiller, J.F.; Eppler, E. & Reinecke, M. 2010. Insulin-like growth factor-3 (IGF-3) in male and female gonads of the tilapia: Development and regulation of gene expression by growth hormone (GH) and 17α-ethinylestradiol (EE2). General and Comparative Endocrinology 167(1): 128-134.
- Berishvili, 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 a bony fish, the tilapia Oreochromis niloticus. General and Comparative Endocrinology 146(3): 204-210.
- Berishvili, G.; Shved, N.; Eppler, E.; Clota, F.; Baroiller, J.F. & Reinecke, M. 2006b. Organ-specific expression of IGF-I during early development of bony fish as revealed in the tilapia, Oreochromis niloticus, by in situ hybridization and immunohistochemistry: indication for the particular importance of local IGF-I. Cell and Tissue Research 325(2): 287-301.
- Biran, J., & Levavi-Sivan, B. 2018. Endocrine control of reproduction. Fish Encyclopedia of Reproduction pp: 362–368.
- Boan, A.F.; Delgadin, T.H.; Canosa, L.F. & Fernandino, J. I. 2024. Loss of function in somatostatin receptor 5 has no impact on the growth of medaka fish due to compensation by the other paralogs. General and Comparative Endocrinology 351: 114478.
- Campbell, B.; Dickey, J.; Beckman, B.; Young, G.; Pierce, A.; Fukada, H. & Swanson, P. 2006. Previtellogenic oocyte growth in salmon: relationships among body growth, plasma insulin-like growth factor-1, estradiol-17beta, follicle-stimulating hormone and expression of ovarian genes for insulin-like growth factors, steroidogenic-acute regulatory protein and receptors for gonadotropins, growth hormone, and somatolactin. Biology of Reproduction 75(1): 34-44.
- Carnevali, O.; Cardinali, M.; Maradonna, F.; Parisi, M.; Olivotto, I.; Polzonetti-Magni, A.M.; Mosconi, G. & Funkenstein, B. 2005. Hormonal regulation of hepatic IGF-I and IGF-II gene expression in the marine teleost Sparus aurata. Molecular Reproduction and Development, 71(1): 12–18.
- Chaube, R.; Sharma, S.; Senthilkumaran, B.; Bhat, S.G. & Joy, K.P. 2022. Kisspeptins stimulate the hypothalamus-pituitary-ovarian axis and induce final oocyte maturation and ovulation in female stinging catfish (Heteropneustes fossilis): Evidence from in vivo and in vitro studies. Aquaculture 548: 737734.
- Chomczynski, P. & Sacchi, N. 2006. The single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction: Twenty-something years on. Nature Protocols, 1(2): 581–585.
- Cleveland, B.M. & Weber, G.M. 2015. Effects of sex steroids on expression of genes regulating growth-related mechanisms in rainbow trout (Oncorhynchus mykiss). General and Comparative Endocrinology 216: 103-115.
- Colovos, C. & Yeates, T. O. 1993. Verification of protein structures: patterns of nonbonded atomic interactions. Protein Science 2(9): 1511-1519.
- Das, D.; Khan, P.P. & Maitra, S. 2017. Endocrine and paracrine regulation of meiotic cell cycle progression in teleost oocytes: cAMP at the centre of complex intra-oocyte signalling events. General and Comparative Endocrinology 241:33-40.
- Davis, L.K.; Hiramatsu, N.; Hiramatsu, K.; Reading, B.J.; Matsubara, T.; Hara, A.; Sullivan, C.V.; Pierce, A.L.; Hirano, T. & Grau, E.G. 2007. Induction of three vitellogenins by 17beta-estradiol with concurrent inhibition of the growth hormone-insulin-like growth factor 1 axis in a euryhaline teleost, the tilapia (Oreochromis mossambicus). Biology of Reproduction 77(4): 614-625.
- Denley, A.; Cosgrove, L.J.; Booker, G.W.; Wallace, J.C. & Forbes, B.E. 2005. Molecular interactions of the IGF system. Cytokine and Growth Factor Reviews 16(4-5): 421–439.
- Duan, C.; Ren, H. & Gao, S. 2010. Insulin-like growth factors (IGFs), IGF receptors, and IGF-binding proteins: Roles in skeletal muscle growth and differentiation. General and Comparative Endocrinology 167(3): 344-351.
- Duan, C. & Xu, Q. 2005. Roles of insulin-like growth factor (IGF) binding proteins in regulating IGF actions. General and Comparative Endocrinology 142(1-2): 44-52.
- Escobar, S.; Fuentes, E.N.; Poblete, E.; Valdés, J.A.; Safian, D.; Reyes, A.E.; Álvarez, M. & Molina, A. 2011. Molecular cloning of IGF-1 and IGF-1 receptor and their expression pattern in the Chilean flounder (Paralichthys adspersus). Comparative Biochemistry and Physiology - B Biochemistry and Molecular Biology 159(3): 140-147.
- Filby, A.L.; Thorp, K.L. & Tyler, C.R. 2006. Multiple molecular effect pathways of an environmental oestrogen in fish. Journal of Molecular Endocrinology 37(1): 121-134.
- Goswami, S.V. & Sundararaj, B. I. 1968. Compensatory hypertrophy of the remaining ovary after unilateral ovariectomy at various phases of the reproductive cycle of catfish, Heteropneustes fossilis (Bloch). General and Comparative Endocrinology 11(2): 401-413.
- Gu, W.; Yang, Y.; Ning, C.; Wang, Y.; Hu, J.; Zhang, M.; Kuang, S.; Sun, Y.; Li, Y.; Zhang, Y.; Sun, J.; Ying, D. & Xu, S. 2021. Identification and characteristics of insulin-like growth factor system in the brain, liver, and gonad during development of a seasonal breeding teleost, Pampus argenteus. General and Comparative Endocrinology 300: 113645.
- Hanson, A.M.; Kittilson, J.D.; McCormick, S.D. & Sheridan, M. A. 2012. Effects of 17β-estradiol, 4-nonylphenol, and β-sitosterol on the growth hormone-insulin-like growth factor system and seawater adaptation of rainbow trout (Oncorhynchus mykiss). Aquaculture 362: 241-247.
- Hanson, S., Steeves, K., Bagatim, T., Hogan, N., Wiseman, S., Hontela, A., & Hecker, M. 2021. Health status of fathead minnow (Pimephales promelas) populations in a municipal wastewater effluent-dominated stream in the Canadian prairies, Wascana Creek, Saskatchewan. Aquatic Toxicology, 238: 105933.
- Hara, A.; Hiramatsu, N. & Fujita, T. 2016. Vitellogenesis and choriogenesis in fishes. Fisheries science 82: 187-202.
- Hober, S.; Uhlén, M. & Nilsson, B. 1997. Disulfide exchange folding of disulfide mutants of insulin-like growth factor I in vitro. Biochemistry 36(15): 4616-4622.
- Hollander-Cohen, L.; Golan, M. & Levavi-Sivan, B. 2021. Differential regulation of gonadotropins as revealed by transcriptomes of distinct LH and FSH cells of fish pituitary. International Journal of Molecular Sciences 22(12): 6478.
- Jones, J.I. 1995. Insulin-like growth factors and their binding proteins: biological actions. Endocrine Reviews 16(1): 3-34.
- Kagawa, H.; Gen, K.; Okuzawa, 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 follicles of red seabream, Pagrus major. Biology of Reproduction 68(5): 1562-1568.
- Kagawa, H.; Kobayashi, M.; Hasegawa, Y. & Aida, K. 1994. Insulin and insulin-like growth factors I and II induce final maturation of oocytes of red seabream, Pagrus major, in vitro. General and Comparative Endocrinology 95(2): 293-300.
- Krieger, E.; Joo, K.; Lee, J.; Lee, J.; Raman, S.; Thompson, J. & Karplus, K. 2009. Improving physical realism, stereochemistry, and side‐chain accuracy in homology modeling: four approaches that performed well in CASP8. Proteins: Structure, Function, and Bioinformatics 77(S9): 114-122.
- Kumari, P.; Kumar, M.; Sehgal, N. & Aggarwal, N. 2020. In silico analysis of kiss2, expression studies and protein–protein interaction with gonadotropin-releasing hormone 2 (GnRH2) and luteinizing hormone beta (LHβ) in Heteropneustes fossilis. Journal of Biomolecular Structure and Dynamics 40(10): 4543–4557.
- Kumari, P.; Sehgal, N.; Goswami, S.V. & Aggarwal, N. 2021. Multifactorial control of gonadotropin release for induction of oocyte maturation: Influence of gonadotropin-releasing hormone, gonadotropin release-inhibiting factor and dopamine receptors in the catfish, Heteropneustes fossilis. Journal of Applied and Natural Science 13(2): 686-699.
- Lamba, V.J.; Goswami, S.V. & Sundararaj, B.I. 1983. Circannual and circadian variations in plasma levels of steroids (cortisol, estradiol-17β estrone, and testosterone) correlated with the annual gonadal cycle in the catfish, Heteropneustes fossilis (Bloch). General and Comparative Endocrinology 50(2): 205-225.
- Laskowski, R.A.; MacArthur, M.W.; Moss, D.S. & Thornton, J.M. 1993. PROCHECK: a program to check the stereochemical quality of protein structures. Journal of Applied Crystallography 26(2): 283-291.
- Le Roith, D.; Bondy, C.; Yakar, S.; Liu, J.L. & Butler, A. 2001. The somatomedin hypothesis: 2001. Endocrine Reviews 22(1): 53-74.
- Levavi-Sivan, B.; Bogerd, J.; Mañanós, E.L.; Gómez, A. & Lareyre, J.J. 2010. Perspectives on fish gonadotropins and their receptors. General and Comparative Endocrinology 165(3): 412-437.
- Li, J.; Liu, Z.; Kang, T.; Li, M.; Wang, D. & Cheng, C.H. 2021. Igf3: a novel player in fish reproduction. Biology of Reproduction, 104(6): 1194-1204.
- Lin, S.W. & Ge, W. 2009. Differential regulation of gonadotropins (FSH and LH) and growth hormone (GH) by neuroendocrine, endocrine, and paracrine factors in the zebrafish-An in vitro approach. General and Comparative Endocrinology 160(2): 183-193.
- Liu, H.; Guo, Q.; Zhang, L.; Tian, X.; Ma, X.; Zhang, J.X. & Li, X. 2022. The insulin-like growth factor 1 stimulates ovarian steroidogenesis and oocyte maturation in spotted steed Hemibarbus maculatus. Journal of Steroid Biochemistry and Molecular Biology 224: 106159.
- Livak, K.J. & Schmittgen, T.D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25(4): 402-408.
- Lokman, P.M.; George, K.A.N.; Divers, S.L.; Algie, M. & Young, G. 2007. 11-Ketotestosterone and IGF-I increse the size of previttelogenic oocytes from shortfinned eel, Anguilla australis, in vitro. Reproduction 133(5): 955-967.
- Lubzens, E.; Young, G.; Bobe, J. & Cerdà, J. 2010. Oogenesis in teleosts: How fish eggs are formed. General and Comparative Endocrinology 165(3): 367-389.
- Luckenbach, J.A.; Dickey, J.T. & Swanson, P. 2010. Regulation of pituitary GnRH receptor and gonadotropin subunits by IGF1 and GnRH in prepubertal male coho salmon. General and Comparative Endocrinology 167(3): 387-396.
- Maestro, M.A.; Planas, J.V.; Moriyama, S.; Gutiérrez, J.; Planas, J. & Swanson, P. 1997. Ovarian receptors for insulin and insulin-like growth factor I (IGF-I) and effects of IGF-I on steroid production by isolated follicular layers of the preovulatory coho salmon ovarian follicle. General and Comparative Endocrinology 106(2): 189-201.
- Magee, B.A.; Shooter, G.K.; Wallace, J. C. & Francis, G. L. 1999. Insulin-like growth factor I and its binding proteins: A study of the binding interface using B-domain analogues. Biochemistry 38(48): 15863-15870.
- Mahardini, A.; Yamauchi, C.; Takeuchi, Y.; Rizky, D.; Takekata, H. & Takemura, A. 2018. Changes in mRNA abundance of insulin-like growth factors in the brain and liver of a tropical damselfish, Chrysiptera cyanea, in relation to seasonal and food-manipulated reproduction. General and Comparative Endocrinology 269: 112-121.
- Mcbride, R.S.; Somarakis, S.; Fitzhugh, G.R.; Albert, A.; Yaragina, N.A.; Wuenschel, M.J.; Alonso-Fernández, A. & Basilone, G. 2015. Energy acquisition and allocation to egg production in relation to fish reproductive strategies. Fish and Fisheries 16(1): 23-57.
- Messaoudi, A.; Belguith, H. & Ben Hamida, J. 2013. Homology modeling and virtual screening approaches to identify potent inhibitors of VEB-1 β-lactamase. Theoretical Biology and Medical Modelling 10: 1-10.
- Mittal, S., Saluja, D. 2015. Protein Post-translational Modifications: Role in Protein Structure, Function and Stability. In: Singh, L.R., Dar, T.A., Ahmad, P. (eds) Proteostasis and Chaperone Surveillance. Springer, New Delhi.
- Moriyama, S.; Ayson, F.G. & Kawauchi, H. 2000. Growth regulation by insulin-like growth factor-1 in fish. Bioscience, Biotechnology and Biochemistry 64(8): 1553-1562.
- Mukherjee, D., Majumder, S., Moulik, S. R., Pal, P., Gupta, S., Guha, P., & Kumar, D. 2017. Membrane receptor cross talk in gonadotropin-, IGF-I, and insulin-mediated steroidogenesis in fish ovary: an overview. General and Comparative Endocrinology 240: 10-18.
- Nagahama, Y. & Yamashita, M. 2008. Regulation of oocyte maturation in fish. Development, growth and differentiation 50: S195-S219.
- Nakamura, I.; Kusakabe, M.; Swanson, P. & Young, G. 2016. Regulation of sex steroid production and mRNAs encoding gonadotropin receptors and steroidogenic proteins by gonadotropins, cyclic AMP and insulin-like growth factor-I in ovarian follicles of rainbow trout (Oncorhynchus mykiss) at two stages of vitellogenesis. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 201: 132-140.
- Ndandala, C.B.; Dai, M.; Mustapha, U.F.; Li, X.; Liu, J.; Huang, H. & Chen, H. 2022. Current research and future perspectives of GH and IGFs family genes in somatic growth and reproduction of teleost fish. Aquaculture Reports 26: 101289.
- 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 Physiology and Biochemistry 19: 13-21.
- Neirijnck, Y.; Papaioannou, M.D. & Nef, S. 2019. The insulin/IGF system in mammalian sexual development and reproduction. International Journal of Molecular Sciences 20(18): 4440.
- Nipkow, M.; Wirthgen, E.; Luft, P.; Rebl, A.; Hoeflich, A. & Goldammer, T. 2018. Characterization of igf1 and igf2 genes during maraena whitefish (Coregonus maraena) ontogeny and the effect of temperature on embryogenesis and igf expression. Growth Hormone & IGF Research 40: 32-43.
- Nooren, I.M.A. & Thornton, J.M. 2003. Structural characterisation and functional significance of transient protein-protein interactions. Journal of Molecular Biology, 325(5): 991-1018.
- Pant, D.R.; Ila, K.; Sahu, U.B. & Sehgal, N. 2023. Temporal expression of thyroid hormone regulating genes (tsh-b, tsh-r, dio2 and dio3) and their correlation with annual reproductive cycle of the Indian freshwater catfish, Heteropneustes fossilis (Bloch). Journal of Applied and Natural Science 15(1): 41-56.
- Philippou, A.; Maridaki, M.; Pneumaticos, S. & Koutsilieris, M. 2014. The complexity of the IGF1 gene splicing, posttranslational modification and bioactivity. Molecular Medicine, 20: 202-214.
- Pipil, S., Kumar, V., Rawat, V. S., Sharma, L., & Sehgal, N. 2015. In silico and in vivo analysis of binding affinity of estrogens with estrogen receptor alpha in Channa punctatus (Bloch). Fish Physiology and Biochemistry, 41: 31–40.
- Qin, Q.; Chen, X.; Zhu, X.; Li, X.; Zhao, Y.; Xu, Z. & Liu, W. 2020. Insulin-like growth factor I of Yellow catfish (Pelteobagrus fulvidraco): cDNA characterization, tissue distribution, and expressions in response to starvation and refeeding. Fish Physiology and Biochemistry 46: 177-186.
- Rawat, V.S.; Rani, K.V.; Phartyal, R. & Sehgal, N. 2013. Vitellogenin genes in fish: Differential expression on exposure to estradiol. Fish Physiology and Biochemistry, 39: 39–46.
- Reinecke, M. 2010. Insulin-like growth factors and fish reproduction. Biology of Reproduction 82(4): 656-661.
- Reinecke, M.; Björnsson, B.T.; Dickhoff, W.W.; McCormick, S.D.; Navarro, I.; Power, D.M. & Gutiérrez, J. 2005. Growth hormone and insulin-like growth factors in fish: Where we are and where to go. General and Comparative Endocrinology 142(1-2): 20-24.
- Reinecke, M.; Schmid, A.; Ermatinger, R. & Loffing-Cueni, D. 1997. Insulin-like growth factor I in the teleost Oreochromis mossambicus, the tilapia: Gene sequence, tissue expression, and cellular localization. Endocrinology 138(9): 3613-3619.
- Riley, L.G.; Hirano, T. & Grau, E.G. 2002. Disparate effects of gonadal steroid hormones on plasma and liver mRNA levels of insulin-like growth factor-I and vitellogenin in the tilapia, Oreochromis mossambicus. Fish Physiology and Biochemistry 26: 223-230.
- Roy, A.K. 2017. Analysis of Insulin-Like Growth Factor I and Its Receptor of an Indian Major Carp Labeo rohita: An In silico Approach. MOJ Proteomics & Bioinformatics 6(3): 00195.
- Roy, A.; Kucukural, A. & Zhang, Y. 2010. I-TASSER: A unified platform for automated protein structure and function prediction. Nature Protocols 5(4): 725-738.
- Sarang, M. K., & Lal, B. 2005. Effect of piscine GH/IGF-I on final oocyte maturation in vitro in Heteropneustes fossilis. Fish Physiology and Biochemistry 31: 231-233.
- Steinkampf, M.P.; Mendelson, C.R. & Simpson, E.R. 1988. Effects of epidermal growth factor and insulin-like growth factor I on the levels of mRNA encoding aromatase cytochrome P-450 of human ovarian granulosa cells. Molecular and Cellular Endocrinology, 59(1-2): 93-99.
- Suskiewicz, M. J. 2024. The logic of protein post‐translational modifications (PTMs): Chemistry, mechanisms and evolution of protein regulation through covalent attachments. BioEssays 46(3): 2300178.
- Torre, S.; Della Benedusi, V.; Fontana, R. & Maggi, A. 2014. Energy metabolism and fertility - A balance preserved for female health. Nature Reviews Endocrinology 10(1): 13-23.
- Triantaphyllopoulos, K.A.; Cartas, D. & Miliou, H. 2020. Factors influencing GH and IGF‐I gene expression on growth in teleost fish: how can aquaculture industry benefit?. Reviews in Aquaculture 12(3): 1637-1662.
- Vasal, S. & Sundararaj, B.I. 1976. Response of the ovary in the catfish, Heteropneustes fossilis (Bloch), to various combinations of photoperiod and temperature. Journal of Experimental Zoology 197(2): 247-263.
- Vriend, G. 1990. WHAT IF: A molecular modeling and drug design program. Journal of Molecular Graphics 8(1): 52-56.
- Wang, D.S.; Jiao, B.; Hu, C.; Huang, X.; Liu, Z. & Cheng, C.H.K. 2008. Discovery of a gonad-specific IGF subtype in teleost. Biochemical and Biophysical Research Communications 367(2): 336-341.
- Weil, C.; Carré, F.; Blaise, O.; Breton, B. & Le Bail, P.Y. 1999. Differential effect of insulin-like growth factor I on in vitro gonadotropin (I and II) and growth hormone secretions in rainbow trout (Oncorhynchus mykiss) at different stages of the reproductive cycle. Endocrinology 140(5): 2054-2062.
- Wiederstein, M. & Sippl, M.J. 2007. ProSA-web: Interactive web service for the recognition of errors in three-dimensional structures of proteins. Nucleic Acids Research 35(Suppl_2): W407-W410.
- Wood, A.W.; Duan, C. & Bern, H.A. 2005. Insulin-like growth factor signaling in fish. International Review of Cytology 243(1): 215-285.
- Xie, L.; Tang, Q.; Yang, L. & Chen, L. 2016. Insulin-like growth factor I promotes oocyte maturation through increasing the expression and phosphorylation of epidermal growth factor receptor in the zebrafish ovary. Molecular and Cellular Endocrinology 419: 198-207.
- 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 Physiology and Biochemistry 41: 139-152.
- Yang, J. & Zhang, Y. 2015. I-TASSER server: New development for protein structure and function predictions. Nucleic Acids Research 43(W1): W174-W181.
- Yuan, C.; Chen, K.; Zhu, Y.; Yuan, Y. & Li, M. 2018. Medaka igf1 identifies somatic cells and meiotic germ cells of both sexes. Gene 642: 423-429.
- Zhang, Y. 2008. I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9(40): 1-8.
- Zheng, W.; Zhang, C.; Li, Y.; Pearce, R.; Bell, E.W. & Zhang, Y. 2021. Folding non-homologous proteins by coupling deep-learning contact maps with I-TASSER assembly simulations. Cell Reports Methods 1(3): 100014.
- Zhou, R.; Yu, S.M.Y.; & Ge, W. 2016. Expression and functional characterization of intrafollicular GH–IGF system in the zebrafish ovary. General and Comparative Endocrinology 232: 32-42.
- Zhou, X.; Zheng, W.; Li, Y.; Pearce, R.; Zhang, C.; Bell, E.W.; Zhang, G. & Zhang, Y. 2022. I-TASSER-MTD: a deep-learning-based platform for multi-domain protein structure and function prediction. Nature Protocols 17(10): 2326-2353.
- Zohar, Y.; Muñoz-Cueto, J.A.; Elizur, A. & Kah, O. 2010. Neuroendocrinology of reproduction in teleost fish. General and Comparative Endocrinology 165(3): 438-455.
References
Arukwe, A. 2001. Cellular and molecular responses to endocrine-modulators and the impact on fish reproduction. Marine Pollution Bulletin 42(8): 643-655.
Baker, D.M.; Davies, B.; Dickhoff, W.W. & Swanson, P. 2000. Insulin-like growth factor I increases follicle-stimulating hormone (FSH) content and gonadotropin-releasing hormone-stimulated FSH release from coho salmon pituitary cells in vitro. Biology of Reproduction 63(3): 865-871.
Berishvili, G.; Baroiller, J.F.; Eppler, E. & Reinecke, M. 2010. Insulin-like growth factor-3 (IGF-3) in male and female gonads of the tilapia: Development and regulation of gene expression by growth hormone (GH) and 17α-ethinylestradiol (EE2). General and Comparative Endocrinology 167(1): 128-134.
Berishvili, 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 a bony fish, the tilapia Oreochromis niloticus. General and Comparative Endocrinology 146(3): 204-210.
Berishvili, G.; Shved, N.; Eppler, E.; Clota, F.; Baroiller, J.F. & Reinecke, M. 2006b. Organ-specific expression of IGF-I during early development of bony fish as revealed in the tilapia, Oreochromis niloticus, by in situ hybridization and immunohistochemistry: indication for the particular importance of local IGF-I. Cell and Tissue Research 325(2): 287-301.
Biran, J., & Levavi-Sivan, B. 2018. Endocrine control of reproduction. Fish Encyclopedia of Reproduction pp: 362–368.
Boan, A.F.; Delgadin, T.H.; Canosa, L.F. & Fernandino, J. I. 2024. Loss of function in somatostatin receptor 5 has no impact on the growth of medaka fish due to compensation by the other paralogs. General and Comparative Endocrinology 351: 114478.
Campbell, B.; Dickey, J.; Beckman, B.; Young, G.; Pierce, A.; Fukada, H. & Swanson, P. 2006. Previtellogenic oocyte growth in salmon: relationships among body growth, plasma insulin-like growth factor-1, estradiol-17beta, follicle-stimulating hormone and expression of ovarian genes for insulin-like growth factors, steroidogenic-acute regulatory protein and receptors for gonadotropins, growth hormone, and somatolactin. Biology of Reproduction 75(1): 34-44.
Carnevali, O.; Cardinali, M.; Maradonna, F.; Parisi, M.; Olivotto, I.; Polzonetti-Magni, A.M.; Mosconi, G. & Funkenstein, B. 2005. Hormonal regulation of hepatic IGF-I and IGF-II gene expression in the marine teleost Sparus aurata. Molecular Reproduction and Development, 71(1): 12–18.
Chaube, R.; Sharma, S.; Senthilkumaran, B.; Bhat, S.G. & Joy, K.P. 2022. Kisspeptins stimulate the hypothalamus-pituitary-ovarian axis and induce final oocyte maturation and ovulation in female stinging catfish (Heteropneustes fossilis): Evidence from in vivo and in vitro studies. Aquaculture 548: 737734.
Chomczynski, P. & Sacchi, N. 2006. The single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction: Twenty-something years on. Nature Protocols, 1(2): 581–585.
Cleveland, B.M. & Weber, G.M. 2015. Effects of sex steroids on expression of genes regulating growth-related mechanisms in rainbow trout (Oncorhynchus mykiss). General and Comparative Endocrinology 216: 103-115.
Colovos, C. & Yeates, T. O. 1993. Verification of protein structures: patterns of nonbonded atomic interactions. Protein Science 2(9): 1511-1519.
Das, D.; Khan, P.P. & Maitra, S. 2017. Endocrine and paracrine regulation of meiotic cell cycle progression in teleost oocytes: cAMP at the centre of complex intra-oocyte signalling events. General and Comparative Endocrinology 241:33-40.
Davis, L.K.; Hiramatsu, N.; Hiramatsu, K.; Reading, B.J.; Matsubara, T.; Hara, A.; Sullivan, C.V.; Pierce, A.L.; Hirano, T. & Grau, E.G. 2007. Induction of three vitellogenins by 17beta-estradiol with concurrent inhibition of the growth hormone-insulin-like growth factor 1 axis in a euryhaline teleost, the tilapia (Oreochromis mossambicus). Biology of Reproduction 77(4): 614-625.
Denley, A.; Cosgrove, L.J.; Booker, G.W.; Wallace, J.C. & Forbes, B.E. 2005. Molecular interactions of the IGF system. Cytokine and Growth Factor Reviews 16(4-5): 421–439.
Duan, C.; Ren, H. & Gao, S. 2010. Insulin-like growth factors (IGFs), IGF receptors, and IGF-binding proteins: Roles in skeletal muscle growth and differentiation. General and Comparative Endocrinology 167(3): 344-351.
Duan, C. & Xu, Q. 2005. Roles of insulin-like growth factor (IGF) binding proteins in regulating IGF actions. General and Comparative Endocrinology 142(1-2): 44-52.
Escobar, S.; Fuentes, E.N.; Poblete, E.; Valdés, J.A.; Safian, D.; Reyes, A.E.; Álvarez, M. & Molina, A. 2011. Molecular cloning of IGF-1 and IGF-1 receptor and their expression pattern in the Chilean flounder (Paralichthys adspersus). Comparative Biochemistry and Physiology - B Biochemistry and Molecular Biology 159(3): 140-147.
Filby, A.L.; Thorp, K.L. & Tyler, C.R. 2006. Multiple molecular effect pathways of an environmental oestrogen in fish. Journal of Molecular Endocrinology 37(1): 121-134.
Goswami, S.V. & Sundararaj, B. I. 1968. Compensatory hypertrophy of the remaining ovary after unilateral ovariectomy at various phases of the reproductive cycle of catfish, Heteropneustes fossilis (Bloch). General and Comparative Endocrinology 11(2): 401-413.
Gu, W.; Yang, Y.; Ning, C.; Wang, Y.; Hu, J.; Zhang, M.; Kuang, S.; Sun, Y.; Li, Y.; Zhang, Y.; Sun, J.; Ying, D. & Xu, S. 2021. Identification and characteristics of insulin-like growth factor system in the brain, liver, and gonad during development of a seasonal breeding teleost, Pampus argenteus. General and Comparative Endocrinology 300: 113645.
Hanson, A.M.; Kittilson, J.D.; McCormick, S.D. & Sheridan, M. A. 2012. Effects of 17β-estradiol, 4-nonylphenol, and β-sitosterol on the growth hormone-insulin-like growth factor system and seawater adaptation of rainbow trout (Oncorhynchus mykiss). Aquaculture 362: 241-247.
Hanson, S., Steeves, K., Bagatim, T., Hogan, N., Wiseman, S., Hontela, A., & Hecker, M. 2021. Health status of fathead minnow (Pimephales promelas) populations in a municipal wastewater effluent-dominated stream in the Canadian prairies, Wascana Creek, Saskatchewan. Aquatic Toxicology, 238: 105933.
Hara, A.; Hiramatsu, N. & Fujita, T. 2016. Vitellogenesis and choriogenesis in fishes. Fisheries science 82: 187-202.
Hober, S.; Uhlén, M. & Nilsson, B. 1997. Disulfide exchange folding of disulfide mutants of insulin-like growth factor I in vitro. Biochemistry 36(15): 4616-4622.
Hollander-Cohen, L.; Golan, M. & Levavi-Sivan, B. 2021. Differential regulation of gonadotropins as revealed by transcriptomes of distinct LH and FSH cells of fish pituitary. International Journal of Molecular Sciences 22(12): 6478.
Jones, J.I. 1995. Insulin-like growth factors and their binding proteins: biological actions. Endocrine Reviews 16(1): 3-34.
Kagawa, H.; Gen, K.; Okuzawa, 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 follicles of red seabream, Pagrus major. Biology of Reproduction 68(5): 1562-1568.
Kagawa, H.; Kobayashi, M.; Hasegawa, Y. & Aida, K. 1994. Insulin and insulin-like growth factors I and II induce final maturation of oocytes of red seabream, Pagrus major, in vitro. General and Comparative Endocrinology 95(2): 293-300.
Krieger, E.; Joo, K.; Lee, J.; Lee, J.; Raman, S.; Thompson, J. & Karplus, K. 2009. Improving physical realism, stereochemistry, and side‐chain accuracy in homology modeling: four approaches that performed well in CASP8. Proteins: Structure, Function, and Bioinformatics 77(S9): 114-122.
Kumari, P.; Kumar, M.; Sehgal, N. & Aggarwal, N. 2020. In silico analysis of kiss2, expression studies and protein–protein interaction with gonadotropin-releasing hormone 2 (GnRH2) and luteinizing hormone beta (LHβ) in Heteropneustes fossilis. Journal of Biomolecular Structure and Dynamics 40(10): 4543–4557.
Kumari, P.; Sehgal, N.; Goswami, S.V. & Aggarwal, N. 2021. Multifactorial control of gonadotropin release for induction of oocyte maturation: Influence of gonadotropin-releasing hormone, gonadotropin release-inhibiting factor and dopamine receptors in the catfish, Heteropneustes fossilis. Journal of Applied and Natural Science 13(2): 686-699.
Lamba, V.J.; Goswami, S.V. & Sundararaj, B.I. 1983. Circannual and circadian variations in plasma levels of steroids (cortisol, estradiol-17β estrone, and testosterone) correlated with the annual gonadal cycle in the catfish, Heteropneustes fossilis (Bloch). General and Comparative Endocrinology 50(2): 205-225.
Laskowski, R.A.; MacArthur, M.W.; Moss, D.S. & Thornton, J.M. 1993. PROCHECK: a program to check the stereochemical quality of protein structures. Journal of Applied Crystallography 26(2): 283-291.
Le Roith, D.; Bondy, C.; Yakar, S.; Liu, J.L. & Butler, A. 2001. The somatomedin hypothesis: 2001. Endocrine Reviews 22(1): 53-74.
Levavi-Sivan, B.; Bogerd, J.; Mañanós, E.L.; Gómez, A. & Lareyre, J.J. 2010. Perspectives on fish gonadotropins and their receptors. General and Comparative Endocrinology 165(3): 412-437.
Li, J.; Liu, Z.; Kang, T.; Li, M.; Wang, D. & Cheng, C.H. 2021. Igf3: a novel player in fish reproduction. Biology of Reproduction, 104(6): 1194-1204.
Lin, S.W. & Ge, W. 2009. Differential regulation of gonadotropins (FSH and LH) and growth hormone (GH) by neuroendocrine, endocrine, and paracrine factors in the zebrafish-An in vitro approach. General and Comparative Endocrinology 160(2): 183-193.
Liu, H.; Guo, Q.; Zhang, L.; Tian, X.; Ma, X.; Zhang, J.X. & Li, X. 2022. The insulin-like growth factor 1 stimulates ovarian steroidogenesis and oocyte maturation in spotted steed Hemibarbus maculatus. Journal of Steroid Biochemistry and Molecular Biology 224: 106159.
Livak, K.J. & Schmittgen, T.D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25(4): 402-408.
Lokman, P.M.; George, K.A.N.; Divers, S.L.; Algie, M. & Young, G. 2007. 11-Ketotestosterone and IGF-I increse the size of previttelogenic oocytes from shortfinned eel, Anguilla australis, in vitro. Reproduction 133(5): 955-967.
Lubzens, E.; Young, G.; Bobe, J. & Cerdà, J. 2010. Oogenesis in teleosts: How fish eggs are formed. General and Comparative Endocrinology 165(3): 367-389.
Luckenbach, J.A.; Dickey, J.T. & Swanson, P. 2010. Regulation of pituitary GnRH receptor and gonadotropin subunits by IGF1 and GnRH in prepubertal male coho salmon. General and Comparative Endocrinology 167(3): 387-396.
Maestro, M.A.; Planas, J.V.; Moriyama, S.; Gutiérrez, J.; Planas, J. & Swanson, P. 1997. Ovarian receptors for insulin and insulin-like growth factor I (IGF-I) and effects of IGF-I on steroid production by isolated follicular layers of the preovulatory coho salmon ovarian follicle. General and Comparative Endocrinology 106(2): 189-201.
Magee, B.A.; Shooter, G.K.; Wallace, J. C. & Francis, G. L. 1999. Insulin-like growth factor I and its binding proteins: A study of the binding interface using B-domain analogues. Biochemistry 38(48): 15863-15870.
Mahardini, A.; Yamauchi, C.; Takeuchi, Y.; Rizky, D.; Takekata, H. & Takemura, A. 2018. Changes in mRNA abundance of insulin-like growth factors in the brain and liver of a tropical damselfish, Chrysiptera cyanea, in relation to seasonal and food-manipulated reproduction. General and Comparative Endocrinology 269: 112-121.
Mcbride, R.S.; Somarakis, S.; Fitzhugh, G.R.; Albert, A.; Yaragina, N.A.; Wuenschel, M.J.; Alonso-Fernández, A. & Basilone, G. 2015. Energy acquisition and allocation to egg production in relation to fish reproductive strategies. Fish and Fisheries 16(1): 23-57.
Messaoudi, A.; Belguith, H. & Ben Hamida, J. 2013. Homology modeling and virtual screening approaches to identify potent inhibitors of VEB-1 β-lactamase. Theoretical Biology and Medical Modelling 10: 1-10.
Mittal, S., Saluja, D. 2015. Protein Post-translational Modifications: Role in Protein Structure, Function and Stability. In: Singh, L.R., Dar, T.A., Ahmad, P. (eds) Proteostasis and Chaperone Surveillance. Springer, New Delhi.
Moriyama, S.; Ayson, F.G. & Kawauchi, H. 2000. Growth regulation by insulin-like growth factor-1 in fish. Bioscience, Biotechnology and Biochemistry 64(8): 1553-1562.
Mukherjee, D., Majumder, S., Moulik, S. R., Pal, P., Gupta, S., Guha, P., & Kumar, D. 2017. Membrane receptor cross talk in gonadotropin-, IGF-I, and insulin-mediated steroidogenesis in fish ovary: an overview. General and Comparative Endocrinology 240: 10-18.
Nagahama, Y. & Yamashita, M. 2008. Regulation of oocyte maturation in fish. Development, growth and differentiation 50: S195-S219.
Nakamura, I.; Kusakabe, M.; Swanson, P. & Young, G. 2016. Regulation of sex steroid production and mRNAs encoding gonadotropin receptors and steroidogenic proteins by gonadotropins, cyclic AMP and insulin-like growth factor-I in ovarian follicles of rainbow trout (Oncorhynchus mykiss) at two stages of vitellogenesis. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 201: 132-140.
Ndandala, C.B.; Dai, M.; Mustapha, U.F.; Li, X.; Liu, J.; Huang, H. & Chen, H. 2022. Current research and future perspectives of GH and IGFs family genes in somatic growth and reproduction of teleost fish. Aquaculture Reports 26: 101289.
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 Physiology and Biochemistry 19: 13-21.
Neirijnck, Y.; Papaioannou, M.D. & Nef, S. 2019. The insulin/IGF system in mammalian sexual development and reproduction. International Journal of Molecular Sciences 20(18): 4440.
Nipkow, M.; Wirthgen, E.; Luft, P.; Rebl, A.; Hoeflich, A. & Goldammer, T. 2018. Characterization of igf1 and igf2 genes during maraena whitefish (Coregonus maraena) ontogeny and the effect of temperature on embryogenesis and igf expression. Growth Hormone & IGF Research 40: 32-43.
Nooren, I.M.A. & Thornton, J.M. 2003. Structural characterisation and functional significance of transient protein-protein interactions. Journal of Molecular Biology, 325(5): 991-1018.
Pant, D.R.; Ila, K.; Sahu, U.B. & Sehgal, N. 2023. Temporal expression of thyroid hormone regulating genes (tsh-b, tsh-r, dio2 and dio3) and their correlation with annual reproductive cycle of the Indian freshwater catfish, Heteropneustes fossilis (Bloch). Journal of Applied and Natural Science 15(1): 41-56.
Philippou, A.; Maridaki, M.; Pneumaticos, S. & Koutsilieris, M. 2014. The complexity of the IGF1 gene splicing, posttranslational modification and bioactivity. Molecular Medicine, 20: 202-214.
Pipil, S., Kumar, V., Rawat, V. S., Sharma, L., & Sehgal, N. 2015. In silico and in vivo analysis of binding affinity of estrogens with estrogen receptor alpha in Channa punctatus (Bloch). Fish Physiology and Biochemistry, 41: 31–40.
Qin, Q.; Chen, X.; Zhu, X.; Li, X.; Zhao, Y.; Xu, Z. & Liu, W. 2020. Insulin-like growth factor I of Yellow catfish (Pelteobagrus fulvidraco): cDNA characterization, tissue distribution, and expressions in response to starvation and refeeding. Fish Physiology and Biochemistry 46: 177-186.
Rawat, V.S.; Rani, K.V.; Phartyal, R. & Sehgal, N. 2013. Vitellogenin genes in fish: Differential expression on exposure to estradiol. Fish Physiology and Biochemistry, 39: 39–46.
Reinecke, M. 2010. Insulin-like growth factors and fish reproduction. Biology of Reproduction 82(4): 656-661.
Reinecke, M.; Björnsson, B.T.; Dickhoff, W.W.; McCormick, S.D.; Navarro, I.; Power, D.M. & Gutiérrez, J. 2005. Growth hormone and insulin-like growth factors in fish: Where we are and where to go. General and Comparative Endocrinology 142(1-2): 20-24.
Reinecke, M.; Schmid, A.; Ermatinger, R. & Loffing-Cueni, D. 1997. Insulin-like growth factor I in the teleost Oreochromis mossambicus, the tilapia: Gene sequence, tissue expression, and cellular localization. Endocrinology 138(9): 3613-3619.
Riley, L.G.; Hirano, T. & Grau, E.G. 2002. Disparate effects of gonadal steroid hormones on plasma and liver mRNA levels of insulin-like growth factor-I and vitellogenin in the tilapia, Oreochromis mossambicus. Fish Physiology and Biochemistry 26: 223-230.
Roy, A.K. 2017. Analysis of Insulin-Like Growth Factor I and Its Receptor of an Indian Major Carp Labeo rohita: An In silico Approach. MOJ Proteomics & Bioinformatics 6(3): 00195.
Roy, A.; Kucukural, A. & Zhang, Y. 2010. I-TASSER: A unified platform for automated protein structure and function prediction. Nature Protocols 5(4): 725-738.
Sarang, M. K., & Lal, B. 2005. Effect of piscine GH/IGF-I on final oocyte maturation in vitro in Heteropneustes fossilis. Fish Physiology and Biochemistry 31: 231-233.
Steinkampf, M.P.; Mendelson, C.R. & Simpson, E.R. 1988. Effects of epidermal growth factor and insulin-like growth factor I on the levels of mRNA encoding aromatase cytochrome P-450 of human ovarian granulosa cells. Molecular and Cellular Endocrinology, 59(1-2): 93-99.
Suskiewicz, M. J. 2024. The logic of protein post‐translational modifications (PTMs): Chemistry, mechanisms and evolution of protein regulation through covalent attachments. BioEssays 46(3): 2300178.
Torre, S.; Della Benedusi, V.; Fontana, R. & Maggi, A. 2014. Energy metabolism and fertility - A balance preserved for female health. Nature Reviews Endocrinology 10(1): 13-23.
Triantaphyllopoulos, K.A.; Cartas, D. & Miliou, H. 2020. Factors influencing GH and IGF‐I gene expression on growth in teleost fish: how can aquaculture industry benefit?. Reviews in Aquaculture 12(3): 1637-1662.
Vasal, S. & Sundararaj, B.I. 1976. Response of the ovary in the catfish, Heteropneustes fossilis (Bloch), to various combinations of photoperiod and temperature. Journal of Experimental Zoology 197(2): 247-263.
Vriend, G. 1990. WHAT IF: A molecular modeling and drug design program. Journal of Molecular Graphics 8(1): 52-56.
Wang, D.S.; Jiao, B.; Hu, C.; Huang, X.; Liu, Z. & Cheng, C.H.K. 2008. Discovery of a gonad-specific IGF subtype in teleost. Biochemical and Biophysical Research Communications 367(2): 336-341.
Weil, C.; Carré, F.; Blaise, O.; Breton, B. & Le Bail, P.Y. 1999. Differential effect of insulin-like growth factor I on in vitro gonadotropin (I and II) and growth hormone secretions in rainbow trout (Oncorhynchus mykiss) at different stages of the reproductive cycle. Endocrinology 140(5): 2054-2062.
Wiederstein, M. & Sippl, M.J. 2007. ProSA-web: Interactive web service for the recognition of errors in three-dimensional structures of proteins. Nucleic Acids Research 35(Suppl_2): W407-W410.
Wood, A.W.; Duan, C. & Bern, H.A. 2005. Insulin-like growth factor signaling in fish. International Review of Cytology 243(1): 215-285.
Xie, L.; Tang, Q.; Yang, L. & Chen, L. 2016. Insulin-like growth factor I promotes oocyte maturation through increasing the expression and phosphorylation of epidermal growth factor receptor in the zebrafish ovary. Molecular and Cellular Endocrinology 419: 198-207.
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 Physiology and Biochemistry 41: 139-152.
Yang, J. & Zhang, Y. 2015. I-TASSER server: New development for protein structure and function predictions. Nucleic Acids Research 43(W1): W174-W181.
Yuan, C.; Chen, K.; Zhu, Y.; Yuan, Y. & Li, M. 2018. Medaka igf1 identifies somatic cells and meiotic germ cells of both sexes. Gene 642: 423-429.
Zhang, Y. 2008. I-TASSER server for protein 3D structure prediction. BMC Bioinformatics 9(40): 1-8.
Zheng, W.; Zhang, C.; Li, Y.; Pearce, R.; Bell, E.W. & Zhang, Y. 2021. Folding non-homologous proteins by coupling deep-learning contact maps with I-TASSER assembly simulations. Cell Reports Methods 1(3): 100014.
Zhou, R.; Yu, S.M.Y.; & Ge, W. 2016. Expression and functional characterization of intrafollicular GH–IGF system in the zebrafish ovary. General and Comparative Endocrinology 232: 32-42.
Zhou, X.; Zheng, W.; Li, Y.; Pearce, R.; Zhang, C.; Bell, E.W.; Zhang, G. & Zhang, Y. 2022. I-TASSER-MTD: a deep-learning-based platform for multi-domain protein structure and function prediction. Nature Protocols 17(10): 2326-2353.
Zohar, Y.; Muñoz-Cueto, J.A.; Elizur, A. & Kah, O. 2010. Neuroendocrinology of reproduction in teleost fish. General and Comparative Endocrinology 165(3): 438-455.