Abstract
Cichlasoma dimerus is a social cichlid fish capable of growing at high rates under laboratory conditions, but knowledge on somatic growth regulation is still unclear. Growth hormone (GH)/insulin-like growth factor I (IGF-I) axis is the key regulator of somatic growth in vertebrates. Two types of growth hormone receptors have been described in teleost fish, named GH receptor type 1 (GHR1) and type 2 (GHR2). In addition, isoforms of these receptors lacking part of the intracellular region have been described. The aim of this study was to evaluate the somatic growth, liver histology and changes in the GH/IGF-I axis after 4 weeks of food deprivation in C. dimerus. Four-week fasted fish showed reductions in specific growth rates in body weight (p < 0.001) and standard length (p < 0.001). Additionally, the hepatosomatic index (p < 0.001) and hepatocyte area (p < 0.001) decreased in fasted fish, while no changes in glucose levels were detected in plasma. The starvation protocol failed to induce changes in GH mRNA levels in the pituitary and IGF-I mRNA levels in liver. In contrast, IGF-I mRNA levels in muscle decreased in fasted fish (p = 0.002). On the other hand, GHR2 (detected with primer sets designed over the extracellular and intracellular region) was upregulated by starvation both in liver and muscle (p < 0.05), while GHR1 remained unchanged. These results show that a fasting period reduced somatic growth both in length and body weight concomitantly with alterations on liver and muscle GHR2 and muscle IGF-I mRNA expression.
Similar content being viewed by others
References
Alonso F, Cánepa M, Moreira RG, Pandolfi M (2011) Social and reproductive physiology and behavior of the Neotropical cichlid fish Cichlasoma dimerus under laboratory conditions. Neotrop Ichthyol 9:559–570
Baumann G (2002) Growth hormone binding protein. The soluble growth hormone receptor. Minerva Endocrinol 27:265–276
Beckman BR (2011) Perspectives on concordant and discordant relations between insulin-like growth factor 1 (IGF1) and growth in fishes. Gen Com Endocrinol 170:233–252
Beckman BR, Shimizu M, Gadberry BA, Cooper KA (2004) Response of the somatotropic axis of juvenile coho salmon to alterations in plane of nutrition with an analysis of the relationships among growth rate and circulating IGF-I and 41 kDa IGFBP. Gen Comp Endocrinol 135:334–344
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B Methodol 57:289–300
Brooks AJ, Wooh JW, Tunny KA, Waters MJ (2008) Growth hormone receptor; mechanism of action. Int J Biochem Cell Biol 40:1984–1989
Calduch-Giner JA, Duval H, Chesnel F, Boeuf G, Pérez-Sánchez J, Boujard D (2001) Fish growth hormone receptor: molecular characterization of two membrane-anchored forms. Endocrinology 142:3269–3273
Cánepa MM, Zhu Y, Fossati M, Stiller JW, Vissio PG (2012) Cloning, phylogenetic analysis and expression of somatolactin and its receptor in Cichlasoma dimerus: their role in long-term background color acclimation. Gen Comp Endocrinol 176:52–61
Duan C (1997) The insulin-like growth factor system and its biological actions in fish. Am Zool 37:491–503
Edens A, Talamantes F (1998) Alternative processing of growth hormone receptor transcripts 1. Endocr Rev 19:559–582
Ellens ER, Kittilson JD, Hall JA, Sowe, SA, Sheridan MA (2013) Evolutionary origin and divergence of the growth hormone receptor family: insight from studies on sea lamprey. Gen Com Endoc 192:222–236
Fox BK, Riley LG, Hirano T, Grau EG (2006) Effects of fasting on growth hormone, growth hormone receptor, and insulin-like growth factor-I axis in seawater-acclimated tilapia, Oreochromis mossambicus. Gen Comp Endocrinol 148:340–347
Fox BK, Breves JP, Davis LK, Pierce AL, Hirano T, Grau EG (2010) Tissue-specific regulation of the growth hormone/insulin-like growth factor axis during fasting and re-feeding: importance of muscle expression of IGF-I and IGF-II mRNA in the tilapia. Gen Comp Endocrinol 166:573–580
Fuentes EN, Einarsdottir IE, Valdes JA, Alvarez M, Molina A, Björnsson BT (2012) Inherent growth hormone resistance in the skeletal muscle of the fine flounder is modulated by nutritional status and is characterized by high contents of truncated GHR, impairment in the JAK2/STAT5 signaling pathway, and low IGF-I expression. Endocrinology 153:283–294
Fukada H, Ozaki Y, Pierce AL, Adachi S, Yamauchi K, Hara A, Dickhoff WW (2004) Salmon growth hormone receptor: molecular cloning, ligand specificity, and response to fasting. Gen Comp Endocrinol 139:61–71
Fukada H, Ozaki Y, Pierce AL, Adachi S, Yamauchi K, Hara A, Dickhoff WW (2005) Identification of the salmon somatolactin receptor, a new member of the cytokine receptor family. Endocrinology 146:2354–2361
Fukamachi S, Meyer A (2007) Evolution of receptors for growth hormone and somatolactin in fish and land vertebrates: lessons from the lungfish and sturgeon orthologues. J Mol Evol 65:359–372
Fukamachi S, Takashi Y, Hiroshi M (2005) Medaka receptors for somatolactin and growth hormone: phylogenetic paradox among fish growth hormone receptors. Genetics 171:1875–1883
Gabillard JC, Kamangar BB, Montserrat N (2006) Coordinated regulation of the GH/IGF system genes during refeeding in rainbow trout (Oncorhynchus mykiss). J Endocrinol 191:15–24
Gao FY, Lu MX, Ye X, Huang ZH, Wang H, Zhu HP, Yang LP (2011) Identification and expression analysis of two growth hormone receptors in zanzibar tilapia (Oreochromis hornorum). Fish Physiol Biochem 37:553–565
Genovese G, Da Cuña R, Towle DW, Maggese MC, Lo Nostro F (2011) Early expression of zona pellucida proteins under octylphenol exposure in Cichlasoma dimerus (Perciformes, Cichlidae). Aquat Toxicol 101:175–185
Genovese G, Regueira M, Piazza Y, Towle DW, Maggese MC, Lo Nostro F (2012) Time-course recovery of estrogen-responsive genes of a cichlid fish exposed to waterborne octylphenol. Aquat Toxicol 114:1–13
Grasl-Kraupp B, Bursch W, Ruttkay-Nedecky B, Wagner A, Lauer B, Schulte-Hermann R (1994) Food restriction eliminates preneoplastic cells through apoptosis and antagonizes carcinogenesis in rat liver. Proc Natl Acad Sci USA 91:9995–9999
Jiao B, Huang X, Chan CB, Zhang L, Wang D, Cheng CH (2006) The co-existence of two growth hormone receptors in teleost fish and their differential signal transduction, tissue distribution and hormonal regulation of expression in seabream. J Mol Endocrinol 36:23–40
Lee LT, Nong G, Chan YH, Tse DL, Cheng CH (2001) Molecular cloning of a teleost growth hormone receptor and its functional interaction with human growth hormone. Gene 270:121–129
Liao Z, Zhu SQ (2004) Identification and characterization of GH receptor and serum GH-binding protein in Chinese sturgeon (Acipenser sinensis). Acta Biochim Biophys Sin 36:811–816
Ma X, Liu X, Zhang Y, Zhu P, Ye W, Lin H (2007) Two growth hormone receptors in Nile tilapia (Oreochromis niloticus): molecular characterization, tissue distribution and expression profiles in the gonad during the reproductive cycle. Comp Biochem Physiol B 147:325–339
Mommsen TP (2001) Paradigms of growth in fish. Comp Biochem Phys B 129:207–219
Moriyama S, Ayson FG, Kawauchi H (2000) Growth regulation by insulin-like growth factor-I in fish. Biosci Biotechnol Biochem 64:1553–1562
Moutoussamy S, Kelly PA, Finidori J (1998) Growth hormone receptor and cytokine receptor family signaling. Eur J Biochem 255:1–11
Pandolfi M, Cánepa MM, Meijide FJ, Alonso F, Rey Vázquez G, Maggese MC, Vissio PG (2009) Studies on the reproductive and developmental biology of Cichlasoma dimerus (Percifomes, Cichlidae). Biocell 33:1–18
Pérez Sirkin DI, Cánepa MM, Fossati M, Fernandino JI, Delgadin T, Canosa LF, Vissio PG (2012) Melanin concentrating hormone (MCH) is involved in the regulation of growth hormone in Cichlasoma dimerus (Cichlidae, Teleostei). Gen Comp Endocrinol 176:102–111
Pérez Sirkin DI, Suzuki H, Cánepa MM, Vissio PG (2013) Orexin and neuropeptide Y: tissue specific expression and immunoreactivity in the hypothalamus and preoptic area of the cichlid fish Cichlasoma dimerus. Tissue Cell 45:452–459
Pérez-Sánchez J, Calduch-Giner JA, Mingarro M, de Celis SVR, Gómez-Requen P, Saera-Vila A, Valdivia MM (2002) Overview of fish growth hormone family. New insights in genomic organization and heterogeneity of growth hormone receptors. Fish Physiol Biochem 27:243–258
Peterson BC, Bilodeau-Bourgeois AL, Small BC (2009) Response of the somatotropic axis to alterations in feed intake of channel catfish (Ictalurus punctatus). Comp Biochem Physiol A 153:457–463
Picha ME, Turano MJ, Tipsmark CK, Borski RJ (2008a) Regulation of endocrine and paracrine sources of Igfs and Gh receptor during compensatory growth in hybrid striped bass (Morone chrysops × Morone saxatilis). J Endocrinol 199:81–94
Picha ME, Turano MJ, Beckman BR, Borski RJ (2008b) Endocrine biomarkers of growth and applications to aquaculture: a minireview of growth hormone, insulin-like growth factor (IGF)-I, and IGF Binding Proteins as Potential Growth Indicators in Fish. North Am J Aquac 70:196–211
Pierce AL, Fox BK, Davis LK, Visitacion N, Kitahashi T, Hirano T, Grau EG (2007) Prolactin receptor, growth hormone receptor, and putative somatolactin receptor in Mozambique tilapia: tissue specific expression and differential regulation by salinity and fasting. Gen Com Endocrinol 154:31–40
Ramakers C, Ruijter JM, Deprez RH, Moorman AF (2003) Assumption-free analysis of quantitative real-time PCR data. Neurosci Lett 339:62–66
Ramallo MR, Grober M, Cánepa MM, Morandini L, Pandolfi M (2012) Arginine-vasotocin expression and participation in reproduction and social behavior in males of the cichlid fish Cichlasoma dimerus. Gen Comp Endocrinol 179:221–231
Reindl M, Sheridan MA (2012) Peripheral regulation of the growth hormone-insulin-like growth factor system in fish and other vertebrates. Comp Biochem Physiol A 163:231–245
Rhee JS, Kim BM, Seo JS, Kim IC, Lee YM, Lee JS (2012) Cloning of growth hormone, somatolactin, and their receptor mRNAs, their expression in organs, during development, and on salinity stress in the hermaphroditic fish, Kryptolebias marmoratus. Comp Biochem Physiol A 16:436–442
Ruijter JM, Ramakers C, Hoogaars WMH, Karlen Y, Bakker O, Van den Hoff MJB, Moorman AFM (2009) Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res 37:e45
Saera-Vila A, Calduch-Giner JA, Pérez-Sánchez J (2005) Duplication of growth hormone receptor (GHR) in fish genome: gene organization and transcriptional regulation of GHR type I and II in gilthead sea bream (Sparus aurata). Gen Comp Endocrinol 142:193–203
Sjögren K, Liu JL, Blad K, Skrtic S, Vidal O, Wallenius V, LeRoith D, Törnell J, Isaksson OG, Jansson JO, Ohlsson C (1999) Liver-derived insulin-like growth factor I (IGF-I) is the principal source of IGF-I in blood but is not required for postnatal body growth in mice. Proc Natl Acad Sci USA 96:7088–7092
Small BC, Peterson BC (2005) Establishment of a time-resolved fluoroimmunoassay for measuring plasma insulin-like growth factor I (IGF-I) in fish: effect of fasting on plasma concentrations and tissue mRNA expression of IGF-I and growth hormone (GH) in channel catfish (Ictalurus punctatus). Domest Anim Endocrin 28:202–215
Sohm F, Manfroid I, Pezet A, Rentier-Delrue F, Rand-Weaver M, Kelly PA, Boeuf G, Postel-Vinay MC, de Luze A, Edery M (1998) Identification and modulation of a growth hormone-binding protein in rainbow trout (Oncorhynchus mykiss) plasma during seawater adaptation. Gen Comp Endocrinol 111:216–224
Uchida K, Kajimura S, Riley LG, Hirano T, Aida K, Grau EG (2003) Effects of fasting on growth hormone/insulin-like growth factor I axis in the tilapia, Oreochromis mossambicus. Comp Biochem Physiol A 134:429–439
Walock CN, Kittilson JD, Sheridan MA (2014) Characterization of a novel growth hormone receptor-encoding cDNA in rainbow trout and regulation of its expression by nutritional state. Gene 533:286–294
Wood AW, Duan C, Bern HA (2005) Insulin-like growth factor signaling in fish. Int Rev Cytol 243:215–285
Zhang Y, Marchant TA (1999) Identification of serum GH-binding proteins in the goldfish (Carassius auratus) and comparison with mammalian GH-binding proteins. J Endocrinol 161:255–262
Acknowledgments
The authors wish to thank Dr. Pablo Botta and Ignacio Simo for their assistance and Dr. Maximiliano Cánepa for his constructive comments. This work was supported by Agencia Nacional de Promoción Científica y Tecnológica (Grant Number: PICT 2005 P.V.), CONICET (Grant Number: PIP: 0276 P.V.) and Universidad de Buenos Aires (Grant Number: 20020120100280 P.V.).
Conflict of interest
The authors declare no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Delgadin, T.H., Pérez Sirkin, D.I., Di Yorio, M.P. et al. GH, IGF-I and GH receptors mRNA expression in response to growth impairment following a food deprivation period in individually housed cichlid fish Cichlasoma dimerus . Fish Physiol Biochem 41, 51–60 (2015). https://doi.org/10.1007/s10695-014-0005-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10695-014-0005-x