Feeding state and age dependent changes in melanin-concentrating hormone expression in the hypothalamus of broiler chickens
Abstract
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 fed, fasting for 24h, fasting for 24h then refed for 2h were applied to study the changes of the aforementioned target and its receptor (MCHR4) gene expression to different nutritional states. 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 both targets expression are restricted to the hypothalamus, only weak expression was detected along the GIT. Different nutritional states did not affect the PMCH and MCHR4 mRNA levels. However, fasting for 24h significantly increased MCH-like immunoreactivity with 25.65%. Fasting for 24h then refed for 2h further significantly increased MCH peptide concentration by 32.51% compared to ad libitum state. Decreasing trend with age was observable both for PMCH and MCHR4 mRNA levels and also for MCH-like immunoreactivity. Correlation analysis did not result significant correlation between MCH peptide concentration and abdominal fat mass in ad libitum fed birds. In conclusion, MCH peptide concentration altered with different feeding states, which indicated that this peptide takes part in feed intake regulation (short-term signalization of feed intake) of broiler chickens in a same manner as in mammals.References
Ando R, Bungo T, Kawakami 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://doi.org/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. http://doi.org/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. http://doi.org/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. http://doi.org/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. http://doi.org/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. http://doi.org/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. http://doi.org/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: 1. http://doi.org/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. http://doi.org/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. http://doi.org/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. http://doi.org/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. http://doi.org/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. http://doi.org/10.1111/j.1365-2052.2008.01717.x
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. http://doi.org/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. http://doi.org/10.2141/jpsa.0160100
Ilnytska O, Argyropoulos G (2008) The role of the Agouti-Related Protein in energy balance regulation. Cell Mol Life Sci 65: 2721. http://doi.org/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. http://doi.org/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. http://doi.org/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. Scientific Reports 5: 8748 http://doi.org/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. http://doi.org/10.1007/s10344-011-0576-0
Macneil DJ (2013) The role of melanin-concentrating hormone and its receptors in energy homeostasis. Front Endocrinol 4: 49 http://doi.org/10.3389/fendo.2013.00049
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. http://doi.org/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. http://doi.org/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. http://doi.org/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. http://doi.org/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. http://doi.org/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. http://doi.org/10.1210/er.2006-0021
Qu D, Ludwig D, Gammeltoft S, Piper M, Pelleymounter M, Cullen M, Mathes W, Przypek J, Kanarek R, MaratosFlier E (1996) A role for melanin-concentrating hormone in the central regulation of feeding behaviour. Nature 380: 243-247. http://doi.org/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. http://doi.org/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. http://doi.org/10.2141/jpsa.0120188
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. http://doi.org/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. http://doi.org/10.1016/j.neulet.2011.01.031
Simon J, Rideau N, Taouis M, Sharp P, Dunn I, Waddington D, Boswell T (2008) Chicken leptin: general and comparative endocrinology. Gen Comp Endocrinol 2-4. http://doi.org/10.1016/j.ygcen.2008.05.018
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. http://doi.org/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. http://doi.org/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. http://doi.org/10.1080/00071660310001645758
Vaughan J, Fischer W, Hoeger C, Rivier J, Vale W (1989) Characterization of melanin-concentrating hormone from rat hypothalamus. Endocrinology 125: 1660-1665. http://doi.org/10.1210/endo-125-3-1660
Walter LJ, Gasch CA, McEvers TJ, Hutcheson JP, DeFoor P, Marquess FLS, Lawrence TE (2014) Association of pro-melanin concentrating hormone genotype with beef carcass quality and yield. J Anim Sci 92: 325-331. http://doi.org/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. https://doi.org/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: 1. http://doi.org/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. http://doi.org/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. http://doi.org/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.org/10.1007/s1004
Acta Biochimica Polonica is an OpenAccess quarterly and publishes four issues a year. All contents are distributed under the Creative Commons Attribution-ShareAlike 4.0 International (CC BY 4.0) license. Everybody may use the content following terms: Attribution — You must give appropriate credit, provide a link to the license, and indicate if changes were made. You may do so in any reasonable manner, but not in any way that suggests the licensor endorses you or your use.
Copyright for all published papers © stays with the authors.
Copyright for the journal: © Polish Biochemical Society.
