Feeding state and age dependent changes in melanin-concentrating hormone expression in the hypothalamus of broiler chickens

• Authors: Ádám Simon , József Németh , András Jávor , István Komlósi , Péter Bai , János Oláh , Béla Juhász , Rita Kiss , Zoltán Szilvássy , Levente Czeglédi
• Languages of publication: EN

Abstracts

EN

We aimed to quantify the gene expression changes of the potent orexigenic melanin-concentrating hormone (MCH) in chicken (Gallus gallus) hypothalamus with quantitative real-time polymerase chain reaction (qPCR), and for the first time determine peptide concentrations with a novel radioimmunoassay (RIA) under different feeding status. Three different experimental conditions, namely ad libitum feeding; fasting for 24 h; fasting for 24 h and then refeeding for 2 h, were applied to study changes of the aforementioned target and its receptor (MCHR4) gene expression under different nutritional status. The relative changes of MCH and MCHR4 were also studied from 7 to 35 days of age. Expression of PMCH and MCHR4 along the gastrointestinal tract (GIT) was also investigated. We found that expression of both targets was significant in the hypothalamus, while only weak expression was detected along the GIT. Different nutritional states did not affect the PMCH and MCHR4 mRNA levels. However, fasting for 24 h had significantly increased the MCH-like immunoreactivity by 25.65%. Fasting for 24 h and then refeeding for 2 h had further significantly increased the MCH peptide concentration by 32.51%, as compared to the ad libitum state. A decreasing trend with age was observable for both, the PMCH and MCHR4 mRNA levels, and also for the MCH-like immunoreactivity. Correlation analysis did not result in a significant correlation between MCH peptide concentration and abdominal fat mass in ad libitum fed birds. In conclusion, MCH peptide concentration altered in response to 24 h fasting, which indicated that this peptide may take part in feed intake regulation of broiler chickens.

Keywords

EN

chicken; feeding states; hypothalamus; MCH; qPCR; RIA

• Publisher: Polish Biochemical Society
• Journal: Acta Biochimica Polonica
• Year: 2018
• Volume: 65
• Issue: 2
• Pages: 251-258

Dates

published

2018

received

2017-11-21

revised

2018-03-02

accepted

2018-03-28

(unknown)

2018-05-30

Contributors

author

Ádám Simon

• Department of Animal Science, Faculty of Agricultural and Food Sciences and Environmental Management, University of Debrecen, Debrecen, Hungary

author

József Németh

• Department of Pharmacology and Pharmacotherapy, Faculty of Medicine, University of Debrecen, Debrecen, Hungary

author

András Jávor

• Department of Animal Science, Faculty of Agricultural and Food Sciences and Environmental Management, University of Debrecen, Debrecen, Hungary

author

István Komlósi

• Department of Animal Science, Faculty of Agricultural and Food Sciences and Environmental Management, University of Debrecen, Debrecen, Hungary

author

Péter Bai

• Department of Medical Chemistry, Faculty of Medicine, University of Debrecen, Debrecen, Hungary
• MTA-DE Lendület Laboratory of Cellular Metabolism Research Group, Debrecen, Hungary
• Research Center for Molecular Medicine, Faculty of Medicine, University of Debrecen, Debrecen, Hungary

author

János Oláh

• Farm and Regional Research Institute of Debrecen, University of Debrecen, Debrecen, Hungary

author

Béla Juhász

• Department of Pharmacology and Pharmacotherapy, Faculty of Medicine, University of Debrecen, Debrecen, Hungary

author

Rita Kiss

• Department of Pharmacology and Pharmacotherapy, Faculty of Medicine, University of Debrecen, Debrecen, Hungary

author

Zoltán Szilvássy

• Department of Pharmacology and Pharmacotherapy, Faculty of Medicine, University of Debrecen, Debrecen, Hungary

author

Levente Czeglédi

• Department of Animal Science, Faculty of Agricultural and Food Sciences and Environmental Management, University of Debrecen, Debrecen, Hungary

References

• Ando R, Bungo T, Kanwakami SI, Shimojo M, Masuda Y, Furuse M (2000) Intracerebroventricular injection of mammalian motilin, melanin-concentrating hormone or galanin does not stimulate food intake in neonatal chicks. Br Poult Sci 41: 508-511. http://www.tandfonline.com/doi/abs/10.1080/00071660050195037.
• Baile CA, Della-Fera MA, Martin RJ (2000) Regulation of metabolism and body fat mass by leptin. Annu Rev Nutr 20: 105-127.doi: 10.1146/annurev.nutr.20.1.105.
• Bittencourt J, Presse F, Arias C, Peto C, Vaughan J, Nahon J, Vale W, Sawchenko P (1992) The melanin-concentrating hormone system of the rat brain: An immuno- and hybridization histochemical characterization. J Comp Neurol 319: 218-245.doi: 10.1002/cne.903190204.
• Bradley RL, Kokkotou EG, Maratos-Flier E, Cheatham B (2000) Melanin-concentrating hormone regulates leptin synthesis and secretion in rat adipocytes. Diabetes 49: 1073.doi: 10.2337/diabetes.49.7.1073.
• Breton C, Schorpp M, Nahon J (1993) Isolation and characterization of the human melanin-concentrating hormone gene and a variant gene. Mol Brain Res 18: 297-310.doi: 10.1016/0169-328X(93)90093-5.
• Cai G, Mo C, Huang L, Li J, Wang Y (2015) Characterization of the Two CART Genes (CART1 and CART2) in Chickens (Gallus gallus). PLoS One 10: e0127107.doi: 10.1371/journal.pone.0127107.
• Chagnon YC, Bureau A, Gendron D, Bouchard RH, Merette C, Roy M, Maziade M (2007) Possible association of the pro-melanin-concentrating hormone gene with a greater body mass index as a side effect of the antipsychotic olanzapine. Am J Med Genet B Neuropsychiatr Genet 144B: 1063-1069.doi: 10.1002/ajmg.b.30554.
• Chervoneva I, Li Y, Schulz S, Croker S, Wilson C, Waldman SA, Hyslop T (2010) Selection of optimal reference genes for normalization in quantitative RT-PCR. BMC Bioinformatics 11: 253.doi: 10.1186/1471-2105-11-253.
• Chung S, Parks GS, Lee C, Civelli O (2011) Recent updates on the melanin-concentrating hormone (MCH) and its receptor system: lessons from MCH1R antagonists. J Mol Neurosci 43: 115-121.doi: 10.1007/s12031-010-9411-4.
• Cui L, Lv C, Zhang J, Mo C, Lin D, Li J, Wang Y (2017) Characterization of melanin-concentrating hormone (MCH) and its receptor in chickens: Tissue expression, functional analysis, and fasting-induced up-regulation of hypothalamic MCH expression. Gene 615: 57-67.doi: 10.1016/j.gene.2017.03.009.
• Fleige S, Pfaffl MW (2006) RNA integrity and the effect on the real-time qRT-PCR performance. Mol Aspects Med 27: 126-139.doi: 10.1016/j.mam.2005.12.003.
• Griffin C, Flouriot G, Sharp P, Greene G, Gannon F (2001) Distribution analysis of the two chicken estrogen receptor-alpha isoforms and their transcripts in the hypothalamus and anterior pituitary gland. Biol Reprod 65: 1156-1163.doi: 10.1095/biolreprod65.4.1156.
• Helgeson S, Schmutz S (2008) Genetic variation in the pro-melanin-concentrating hormone gene affects carcass traits in Bos taurus cattle. Anim Genet 39: 310-315.doi: 10.1111/j.1365-2052.2008.01717.x.
• Hervieu G, Nahon J (1995) Pro-melanin concentrating hormone messenger ribonucleic acid and peptides expression in peripheral tissues of the rat. Neuroendocrinology 61: 348-364.doi: 10.1159/000126857.
• Honda K, Saneyasu T, Aoki K, Shimatani T, Yamaguchi T, Kamisoyama H (2015) Correlation analysis of hypothalamic mRNA levels of appetite regulatory neuropeptides and several metabolic parameters in 28-day-old layer chickens. Anim Sci J 86: 517-522.doi: 10.1111/asj.12320.
• Honda K, Saneyasu T, Kamisoyama H (2017) Gut Hormones and Regulation of Food Intake in Birds. J Poult Sci 54: 103-110.doi: 10.2141/jpsa.0160100
• Huang G, Li J, Wang H, Lan X, Wang Y (2014) Discovery of a novel functional leptin protein (LEP) in zebra finches: evidence for the existence of an authentic avian leptin gene predominantly expressed in the brain and pituitary. Endocrinology 155: 3385-3396.doi: 10.1210/en.2014-1084.
• Ilnytska O, Argyropoulos G (2008) The role of the Agouti-Related Protein in energy balance regulation. Cell Mol Life Sci 65: 2721.doi: 10.1007/s00018-008-8104-4.
• Kawauchi H, Kawazoe I, Tsubokawa M, Kishida M, Baker BI (1983) Characterization of melanin-concentrating hormone in chum salmon pituitaries. Nature 305: 321-323.doi: 10.1038/305321a0.
• Lelesz B, Szilvássy Z, Tóth G, Tóth A, Enyedi A, Felszeghy E, Varga A, Juhász B, Németh J (2016) Radioanalytical methods for the measurement of melanin concentrating hormone (MCH) and detection its receptor in rat tissues. J Radioanal Nucl 310: 1325-1333.doi: 10.1007/s10967-016-4952-9
• Li Q, Wang Y, Hu X, Zhao Y, Li N (2015) Genome-wide mapping reveals conservation of promoter DNA methylation following chicken domestication. Sci Rep 5: 8748.doi: 10.1038/srep08748.
• Li W, Xue F, Li L, Li X, Yue B, Li J (2012) A triple-primer PCR approach for the sex identification of endangered Phasianidae birds. Eur J Wildl Res 58: 289-294.doi: 10.1007/s10344-011-0576-0
• Liu X, Dunn I, Sharp P, Boswell T (2007) Molecular cloning and tissue distribution of a short form chicken leptin receptor mRNA. Domest Anim Endocrinol 32: 155-166.doi: 10.1016/j.domaniend.2006.02.001.
• Malagó W Jr, Franco HM, Matheucci E Jr, Medaglia A, Henrique-Silva F (2002) Large scale sex typing of ostriches using DNA extracted from feathers. BMC Biotechnol 2: 19.doi: 10.1186/1472-6750-2-19.
• Marsh DJ, Weingarth DT, Novi DE (2002) Melanin-concentrating hormone 1 receptor-deficient mice are lean, hyperactive, and hyperphagic and have altered metabolism. Proc Natl Acad Sci USA 99: 3240-3245.doi: 10.1073/pnas.052706899.
• Naufahu J, Alzaid F, Fiuza Brito M, Doslikova B, Valencia T, Cunliffe A, Murray JF (2017) Melanin-concentrating hormone in peripheral circulation in the human. J Endocrinol 232: 513-523.doi: 10.1530/JOE-16-0240.
• Perez-Montarelo D, Madsen O, Alves E, Rodriguez MC, Folch JM, Noguera JL, Groenen MA, Fernandez AI (2014) Identification of genes regulating growth and fatness traits in pig through hypothalamic transcriptome analysis. Physiol Genomics 46: 195-206.doi: 10.1152/physiolgenomics.00151.2013.
• Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.doi: 10.1093/nar/29.9.e45.
• Pissios P, Bradley RL, Maratos-Flier E (2006) Expanding the scales: The multiple roles of MCH in regulating energy balance and other biological functions. Endocr Rev 27: 606-620.doi: 10.1210/er.2006-0021.
• Pissios P, Ozcan U, Kokkotou E, Okada T, Liew CW, Liu S, Peters JN, Dahlgren G, Karamchandani J, Kudva YC, Kurpad AJ, Kennedy RT, Maratos-Flier E, Kulkarni RN (2007) Melanin concentrating hormone is a novel regulator of islet function and growth. Diabetes 56: 311-319.doi: 10.2337/db06-0708.
• Presse F, Nahon JL (2013) Chapter 110. MCH. In Handbook of Biologically Active Peptides. Kastin A ed, pp 828-837. Academic Press.doi: 10.1016/B978-0-12-369442-3.X5001-6.
• Qu D, Ludwig D, Gammeltoft S, Piper M, Pelleymounter M, Cullen M, Mathes WF, Przypek R, Kanarek R, Maratos-Flier E (1996) A role for melanin-concentrating hormone in the central regulation of feeding behaviour. Nature 380: 243-247.doi: 10.1038/380243a0.
• Ruijter J, van der Velden S, Ilgun A (2009) LinRegPCR: Analysis of quantitative RT-PCR data [computer program]. Version 11.0. Amsterdam, the Netherlands: Heart Failure Research Center, Academic Medical Centre
• Saito Y, Nothacker H, Wang Z, Lin SH (1999) Molecular characterization of the melanin-concentrating-hormone receptor. Nature 400: 265.doi: 10.1038/22321.
• Saneyasu T, Nakanishi K, Atsuta H, Ikura A, Kamisoyama H, Hasegawa S, Honda K (2013) Age-dependent changes in the mRNA levels of neuropeptide Y, proopiomelanocortin, and corticotropin-releasing factor in the hypothalamus in growing broiler chicks. J Poult Sci 50: 364-369.doi: 10.2141/jpsa.0120188
• Seroussi E, Cinnamon Y, Yosefi S, Genin O, Smith JG, Rafati N, Bornelöv S, Andersson L, Friedman-Einat M (2016) Identification of the long-sought leptin in chicken and duck: expression pattern of the highly GC-rich avian leptin fits an autocrine/paracrine rather than endocrine function. Endocrinology 157: 737-751.doi: 10.1210/en.2015-1634.
• Shimada M, Tritos NA, Lowell BB, Flier JS, Maratos-Flier E (1998) Mice lacking melanin-concentrating hormone are hypophagic and lean. Nature 396: 670-674.doi: 10.1038/25341.
• Shiraishi J, Tanizawa H, Fujita M, Kawakami S, Bungo T (2011) Localization of hypothalamic insulin receptor in neonatal chicks: Evidence for insulinergic system control of feeding behavior. Neurosci Lett 491: 177-180.doi: 10.1016/j.neulet.2011.01.031.
• Simon Á, Jávor A, Bai P, Oláh J, Czeglédi L (2018) Reference gene selection for reverse transcription quantitative polymerase chain reaction in chicken hypothalamus under different feeding status. J Anim Physiol Anim Nutr (Berl) 102: 286-296.doi: 10.1111/jpn.12690.
• Song Z, Liu L, Yue Y, Jiao H, Lin H, Sheikhahmadi A, Everaert N, Decuypere E, Buyse J (2012) Fasting alters protein expression of AMP-activated protein kinase in the hypothalamus of broiler chicks (Gallus gallus domesticus). Gen Comp Endocrinol 178: 546-555.doi: 10.1016/j.ygcen.2012.06.026.
• Sun G, Li M, Li H, Tian Y, Chen Q, Bai Y, Kang X (2013) Molecular cloning and SNP association analysis of chicken PMCH gene. Mol Biol Rep 40: 5049-5055.doi: 10.1007/s11033-013-2606-3.
• Tokushima Y, Sulistiyanto B, Takahashi K, Akiba Y (2003) Insulin-glucose interactions characterised in newly hatched broiler chicks. Br Poult Sci 44: 746-751.doi: 10.1080/00071660310001645758.
• Uchoa ET, Silva LE, de Castro M, Antunes-Rodrigues J, Elias LL (2012) Glucocorticoids are required for meal-induced changes in the expression of hypothalamic neuropeptides. Neuropeptides 46: 119-124.doi: 10.1016/j.npep.2012.02.002.
• Vaughan J, Fischer W, Hoeger C, Rivier J, Vale W (1989) Characterization of melanin-concentrating hormone from rat hypothalamus. Endocrinology 125: 1660-1665.doi: 10.1210/endo-125-3-1660.
• Walter LJ, Gasch CA, McEvers TJ, Hutcheson JP, DeFoor P, Marquess FL, Lawrence TE (2014) Association of pro-melanin concentrating hormone genotype with beef carcass quality and yield. J Anim Sci 92: 325-331.doi: 10.2527/jas.2013-6931.
• Wang Y, Rao K, Yuan L, Everaert N, Buyse J, Grossmann R, Zhao R (2012) Chicken FTO gene: Tissue-specific expression, brain distribution, breed difference and effect of fasting. Comp Biochem Physiol A Mol Integr Physiol 163: 246-252.doi: 10.1016/j.cbpa.2012.08.009.
• Ye J, Coulouris G, Zaretskaya I, Cutcutache I, Rozen S, Madden TL (2012) Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics 13: 134.doi: 10.1186/1471-2105-13-134.
• Yi J, Gilbert ER, Siegel PB, Cline MA (2015) Fed and fasted chicks from lines divergently selected for low or high body weight have differential hypothalamic appetite-associated factor mRNA expression profiles. Behav Brain Res 286: 58-63.doi: 10.1016/j.bbr.2015.02.008.
• Yun S, Furlong M, Sim M, Cho M, Park S, Cho EB, Reyes-Alcaraz A, Hwang JI, Kim J, Seong JY (2015) Prevertebrate Local Gene Duplication Facilitated Expansion of the Neuropeptide GPCR Superfamily. Mol Biol Evol 32: 2803-2817.doi: 10.1093/molbev/msv179.
• Zhang W, Kim S, Settlage R, McMahon W, Sumners LH, Siegel PB, Dorshorst BJ, Cline MA, Gilbert ER (2015) Hypothalamic differences in expression of genes involved in monoamine synthesis and signaling pathways after insulin injection in chickens from lines selected for high and low body weight. Neurogenetics 16: 133-144. http://doi: 10.1007/s10048-014-0435-8.

Identifiers

DOI

10.18388/abp.2017_2362