DOI QR코드

DOI QR Code

Effect of 24 h Fasting on Gene Expression of AMPK, Appetite Regulation Peptides and Lipometabolism Related Factors in the Hypothalamus of Broiler Chicks

  • Lei, Liu ;
  • Lixian, Zhu
  • Received : 2012.03.22
  • Accepted : 2012.06.02
  • Published : 2012.09.01

Abstract

The 5'-adenosine monophosphate-activated protein kinase (AMPK) is a key part of a kinase-signaling cascade that acts to maintain energy homeostasis. The objective of this experiment was to investigate the possible effects of fasting and refeeding on the gene expression of hypothalamic AMPK, some appetitive regulating peptides and lipid metabolism related enzymes. Seven-day-old male broiler (Arbor Acres) chicks were allocated into three equal treatments: fed ad libitum (control); fasted for 24 h; fasted for 24 h and then refed for 24 h. Compared with the control, the hypothalamic gene expression of $AMPK{\alpha}2$, $AMPK{\beta}1$, $AMPK{\beta}2$, $AMPK{\gamma}1$, Ste20-related adaptor protein ${\beta}$ ($STRAD{\beta}$), mouse protein $25{\alpha}$ ($MO25{\alpha}$) and agouti-related peptide (AgRP) were increased after fasting for 24 h. No significant difference among treatments was observed in mRNA levels of $AMPK{\alpha}1$, $AMPK{\gamma}2$, LKB1 and neuropeptide Y (NPY). However, the expression of $MO25{\beta}$, pro-opiomelanocortin (POMC), corticotropin-releasing hormone (CRH), ghrelin, fatty acid synthase (FAS), acetyl-CoA carboxylase ${\alpha}$ ($ACC{\alpha}$), carnitine palmitoyltransferase 1 (CPT-1) and sterol regulatory element binding protein-1 (SREBP-1) were significantly decreased. The present results indicated that 24 h fasting altered gene expression of AMPK subunits, appetite regulation peptides and lipometabolism related factors in chick's hypothalamus; the hypothalamic FAS signaling pathway might be involved in the AMPK regulated energy homeostasis and/or appetite regulation in poultry.

Keywords

Metabolism;Nutrition;Peptides;Lipid;Hypothalamus;Broiler

References

  1. Bass, A. F., J. Boudeau, G. P. Sapkota, L. Smit, R. Medema, N. A. Morrice, D. R. Alessi and H. C. Clevers. 2003. Activation of the tumor suppressor kinase LKB1 by the STE20-like pseudokinase STRAD. EMBO J. 22:3062-3072. https://doi.org/10.1093/emboj/cdg292
  2. Bennett, M., Y. Seo, S. Datta, D. Shin and T. Osborne. 2008. Selective binding of sterol regulatory element-binding protein isoforms and co-regulatory proteins to promoters for lipid metabolic genes in liver. J. Biol. Chem. 283:15628-15637. https://doi.org/10.1074/jbc.M800391200
  3. Boudeau, J., A. F. Bass, M. Deak, N. A. Morrice, A. Kieloch, M. Schutkowski, A. R. Prescott, H. C. Clevers and D. R. Alessi. 2003. MO25 ${\alpha}/{\beta}$ interact with STRAD ${\alpha}/{\beta}$ enhancing their ability to bind, activate and localize LKB1 in the cytoplasm. EMBO J. 22:5102-5114. https://doi.org/10.1093/emboj/cdg490
  4. Carling, D., M. Sanders and A. Woods. 2008. The regulation of AMP-activated protein kinase by upstream kinases. Int. J. Obes. (Lond). 32:S55-S59.
  5. Cheung, P., I. Salt, S. Davies, D. Hardie and D. Carling.2000. Characterization of AMP-activated protein kinase gamma-subunit isoforms and their role in AMP binding. Biochem. J. 346:659-669. https://doi.org/10.1042/0264-6021:3460659
  6. Claret, M., M. A. Smith, R. L. Batterham, C. Selman, A. I. Choudhury, L. G. Fryer, M. Clements, H. Al-Qassab, H. Heffron, A. W. Xu, J. R. Speakman, G. S. Barsh, B. Viollet, S. Vaulont, M. L. Ashford, D. Carling and D. J. Withers. 2007. AMPK is essential for energy homeostasis regulation and glucose sensing by POMC and AgRP neurons. J. Clin. Invest. 117:2325-2336. https://doi.org/10.1172/JCI31516
  7. Close, B., K. Banister, V. Baumans, E. M. Bernoth, N. Bromage, J. Bunyan, W. Erhardt, P. Flecknell, N. Gregory, H. Hackbarth, D. Morton and C. Warwick. 1997. Recommendations for euthanasia of experimental animals: Part 2. DGXT of the European Commission. Lab. Anim. 31:1-32. https://doi.org/10.1258/002367797780600297
  8. Corton, J. M., J. G. Gillespie and D. G. Hardie. 1994. Role of the AMP-activated protein kinase in the cellular stress response. Curr. Biol. 4:315-324. https://doi.org/10.1016/S0960-9822(00)00070-1
  9. Cowley, M., J. L. Smart, M. Rubinstein, M. G. Cerdán, S. Diano, T. L. Horvath, R. D. Cone and M. L. Low. 2001. Leptin activates anorexigenic POMC neurons through a neural network in the arcuate nucleus. Nature 411:480-484. https://doi.org/10.1038/35078085
  10. da Silva Xavier, G., I. Leclerc, I. P. Salt, B. Doiron, D. G. Hardie, A. Kahn and G. A. Rutter. 2000. Role of AMP-activated protein kinase in the regulation by glucose of islet beta cell gene expression. Proc. Natl. Acad. Sci. USA. 97:4023-4028. https://doi.org/10.1073/pnas.97.8.4023
  11. Date, Y., N. Murakami, K. Toshinai, S. Matsukura, A. Niijima, H. Matsuo, K. Kangawa and M. Nakazato. 2002. The role of the gastric afferent vagal nerve in ghrelin-induced feeding and growth hormone secretion in rats. Gastroenterology 123:1120-1128. https://doi.org/10.1053/gast.2002.35954
  12. Dridi, S., C. Ververken, F. B. Hillgartner, A. Lutgarde, E. Van der Gucht, L. Cnops, E. Decuypere and J. Buyse. 2006. FAS inhibitor cerulenin reduces food intake and melanocortin receptor gene expression without modulating the other (an)orexigenic neuropeptides in chickens. Am. J. Physiol. Regul. Integr. Comp. Physiol. 291:R138-R147. https://doi.org/10.1152/ajpregu.00899.2005
  13. Dzamko, N., B. J. van Denderen, A. L. Hevener, S. B. Jørgensen, J. Honeyman, S. Galic, Z. P. Chen, M. J. Watt, D. J. Campbell, G. R. Steinberg and B. E. Kemp. 2010. AMPK beta1 deletion reduces appetite, preventing obesity and hepatic insulin resistance. J. Biol. Chem. 285:115-122. https://doi.org/10.1074/jbc.M109.056762
  14. Foretz, M., N. Ancellin, F. Andreelli, Y. Saintillan, P. Grondin, A. Kahn, B. Thorens, S. Vaulont and B. Viollet. 2005. Short-term overexpression of a constitutively active form of AMP-activated protein kinase in the liver leads to mild hypoglycemia and fatty liver. Diabetes 54:1331-1339. https://doi.org/10.2337/diabetes.54.5.1331
  15. Hahn, T., J. Breininger, D. Baskin and M. Schwartz. 1998. Coexpression of Agrp and NPY in fasting-activated hypothalamic neurons. Nat. Neurosci. 1:271-272. https://doi.org/10.1038/1082
  16. Hardie, D. and S. Hawley. 2001. AMP-activated protein kinase: the energy charge hypothesis revisited. Bioessays 23:1112-1119. https://doi.org/10.1002/bies.10009
  17. Hardie, D. G., J. W. Scott, D. A. Pan and E. R. Hudson. 2003. Management of cellular energy by the AMP-activated protein kinase system. FEBS Lett. 546:113-120. https://doi.org/10.1016/S0014-5793(03)00560-X
  18. Hawley, S. A., M. Davison, A. Woods, S. P. Davies, R. K. Beri, D. Carling and D. G. Hardie. 1996. Characterization of the AMP-activated protein kinase from rat liver and identification of threonine-172 as the major site at which it phosphorylates AMP-activated protein kinase. J. Biol. Chem. 271:27879-27887. https://doi.org/10.1074/jbc.271.44.27879
  19. Hawley, S. A., D. A. Pan, K. J. Mustard, L. Ross, J. Bain, A. M. Edelman, B. G. Frenguelli and D. G. Hardie. 2005. Calmodulin-dependent protein kinase kinase-beta is an alternative upstream kinase for AMP-activated protein kinase. Cell Metab. 2:9-19. https://doi.org/10.1016/j.cmet.2005.05.009
  20. Hemminki, A., D. Markie, I. Tomlinson, E. Avizienyte, S. Roth, A. Loukola, G. Bignell, W. Warren, M. Aminoff, P. Hoglund, H. Järvinen, P. Kristo, K. Pelin, M. Ridanpaa, R. Salovaara, T. Toro, W. Bodmer, S. Olschwang, A. S. Olsen, M. R. Stratton, A. de la Chapelle and L. A. Aaltonen. 1998. A serine/threonine kinase gene defective in Peutz-Jeghers syndrome. Nature 391: 184-187. https://doi.org/10.1038/34432
  21. He, W., T. Lam, S. Obici and L. Rossetti. 2006. Molecular disruption of hypothalamic nutrient sensing induces obesity. Nat. Neurosci. 9:227-233. https://doi.org/10.1038/nn1626
  22. Hong, S. P., F. C. Leiper, A. Woods, D. Carling and M. Carlson. 2003. Activation of yeast Snf1 and mammalian AMP-activated protein kinase by upstream kinases. Proc. Natl. Acad. Sci. USA. 100:8839-8843. https://doi.org/10.1073/pnas.1533136100
  23. Hurley, R., K. A. Anderson, J. M. Franzone, B. E. Kemp, A. R. Means and L. A. Witters. 2005. The $Ca^{2+}$/calmodulin-dependent protein kinase kinases are AMP-activated protein kinase kinases. J. Biol. Chem. 280:29060-29066. https://doi.org/10.1074/jbc.M503824200
  24. Jenne, D. E., H. Reimann, J. Nezu, W. Friedel, S. Loff, R. Jeschke, O. Müller, W. Back and M. Zimmer. 1998. Puetz-Jeghers syndrome is caused by mutation in a novel serine threonine kinase. Nat. Genet. 18:38-43. https://doi.org/10.1038/ng0198-38
  25. Khan, M., K. Dodo, K. Yahata, S. Nishimoto, H. Ueda, T. Taneike, T. Kitazawa and Y. Hosaka. 2006. Intracerebroventricular administration of growth hormone releasing peptide-6 (GHRP-6) inhibits food intake, but not food retention of crop and stomach in neonatal chicks. J. Poult. Sci. 43:35-40. https://doi.org/10.2141/jpsa.43.35
  26. Kola, B. 2008. Role of AMP-activated protein kinase in the control of appetite. J. Neuroendocrinol. 20:942-951. https://doi.org/10.1111/j.1365-2826.2008.01745.x
  27. Kola, B., M. Boscaro, G. A. Rutter, A. B. Grossman and M.Korbonits. 2006. Expanding role of AMPK in endocrinology. Trends Endocrinol. Metab. 17:205-215. https://doi.org/10.1016/j.tem.2006.05.006
  28. Lam, T. K., G. J. Schwartz and L. Rossetti. 2005. Hypothalamic sensing of fatty acids. Nat. Neurosci. 8:579-584. https://doi.org/10.1038/nn1456
  29. Lane, M. D., Z. Hu, S. H. Cha, Y. Dai, M. Wolfgang and A. Sidhaye. 2005. Role of malonyl-CoA in the hypothalamic control of food intake and energy expenditure. Biochem. Soc. Trans. 33:1063-1067. https://doi.org/10.1042/BST20051063
  30. Lopez, M., R. Lage, A. K. Saha, D. Perez-Tilve, M. J. Vazquez, L. Varela, S. Sangiao-Alvarellos, S. Tovar, K. Raghay, S. Rodríguez-Cuenca, R. M. Deoliveira, T. Castaneda, R. Datta, J. Z. Dong, M. Culler, M. W. Sleeman, C. V. Alvarez, R. Gallego, C. J. Lelliott, D. Carling, M. H. Tschop, C. Diéguez and A. Vidal-Puig. 2008. Hypothalamic fatty acid metabolism mediates the orexigenic action of ghrelin. Cell Metab. 7:389-399. https://doi.org/10.1016/j.cmet.2008.03.006
  31. Lage, R., C. Dieguez, A. Vidal-Puig and M. Lopez. 2008. AMPK: a metabolic gauge regulating whole-body energy homeostasis. Trends Mol. Med. 14:539-549. https://doi.org/10.1016/j.molmed.2008.09.007
  32. Lim, C. T., B. Kola and M. Korbonits. 2010. AMPK as a mediator of hormonal signalling. J. Mol. Endocrinol. 44:87-97. https://doi.org/10.1677/JME-09-0063
  33. Livak, K. J. and T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-[Delta][Delta]CT method. Methods 25:402-408. https://doi.org/10.1006/meth.2001.1262
  34. Marsin, A. S., L. Bertrand, M. H. Rider, J. Deprez, C. Beauloye, M. F. Vincent, G. Van den Berghe, D. Carling and L. Hue. 2000. Phosphorylation and activation of heart PFK-2 by AMPK has a role in the stimulation of glycolysis during ischaemia. Curr. Biol. 10:1247-1255. https://doi.org/10.1016/S0960-9822(00)00742-9
  35. Minokoshi, Y., T. Alquier, N. Furukawa, Y. B. Kim, A. Lee, B. Xue, J. Mu, F. Foufelle, P. Ferre, M. J. Birnbaum, B. J. Stuck and B. B. Kahn. 2004. AMP-kinase regulates food intake by responding to hormonal and nutrient signals in the hypothalamus. Nature 428:569-574. https://doi.org/10.1038/nature02440
  36. Mitchelhill, K. I., D. Stapleton, G. Gao, C. House, B. Michell, F. Katsis, L. A. Witters and B. E. Kemp. 1994. Mammalian AMP-activated protein kinase shares structural and functional homology with the catalytic domain of yeast Snf1 protein kinase. J. Biol. Chem. 269:2361-2364.
  37. Momcilovic, M., S. P. Hong and M. Carlson. 2006. Mammalian TAK1 activates Snf1 protein kinase in yeast and phosphorylates AMP-activated protein kinase in vitro. J. Biol. Chem. 281:25336-25343. https://doi.org/10.1074/jbc.M604399200
  38. Morton, G. J., D. E. Cummings, D. G. Baskin, G. S. Barsh and M. W. Schwartz. 2006. Central nervous system control of food intake and body weight. Nature 443:289-295. https://doi.org/10.1038/nature05026
  39. Mu, J., J. T. Brozinick, O. Valladares, M. Bucan and M. J. Birnbaum. 2001. A role for AMP-activated protein kinase in contraction-and hypoxia-regulated glucose transport in skeletal muscle. Mol. Cell 7:1085-1094. https://doi.org/10.1016/S1097-2765(01)00251-9
  40. Musi, N., N. Fujii, M. F. Hirshman, I. Ekberg, S. Fröberg, O. Ljungqvist, A. Thorell and L. J. Goodyear. 2001. AMP-activated protein kinase (AMPK) is activated in muscle of subjects with type 2 diabetes during exercise. Diabetes 50: 921-927. https://doi.org/10.2337/diabetes.50.5.921
  41. Nakazato, M., N. Murakami, Y. Date, M. Kojima, H. Matsuo, K. Kangawa and S. Matsukura. 2001. A role for ghrelin in the central regulation of feeding. Nature 409:194-198. https://doi.org/10.1038/35051587
  42. Obici, S., Z. Feng, A. Arduini, R. Conti and L. Rossetti. 2003. Inhibition of hypothalamic carnitine palmitoyltransferase-1 decreases food intake and glucose production. Nat. Med. 9: 756-761. https://doi.org/10.1038/nm873
  43. Olfert, E. D., B. M. Cross and A. A. McWilliam. 1993. Guide to the care and use of experimental animals. Canadian Council on Animal Care, 1000-151 Slater Street, Ottawa, Ontario K1P 5H3.
  44. Ollmann, M. M., B. D. Wilson, Y. K. Yang, J. A. Kerns, Y. Chen, I. Gantz and G. S. Barsh.1997. Antagonism of central melanocortin receptors in vitro and in vivo by agouti-related protein. Science 278:135-138. https://doi.org/10.1126/science.278.5335.135
  45. Proszkowiec-Weglarz, M., M. P. Richards, B. D. Humphrey, R. W. Rosebrough and J. P. McMurtry. 2009. AMP-activated protein kinase and carbohydrate response element binding protein: a study of two potential regulatory factors in the hepatic lipogenic program of broiler chickens. Comp. Biochem. Physiol. B. Biochem. Mol. Biol. 154:68-79. https://doi.org/10.1016/j.cbpb.2009.05.003
  46. Proszkowiec-Weglarz, M., M. P. Richards, R. Ramachandran and J. McMurtry. 2006. Characterization of the AMP-activated protein kinase pathway in chickens. Comp. Biochem. Physiol. B. Biochem. Mol. Biol. 143:92-106. https://doi.org/10.1016/j.cbpb.2005.10.009
  47. Proszkowiec-Weglarz, M. and M. P. Richards. 2009. Expression and activity of the 5'-adenosine monophosphate-activated protein kinase pathway in selected tissues during chicken embryonic development. Poult. Sci. 88:159-178. https://doi.org/10.3382/ps.2008-00262
  48. Richards, M. P., R. W. Rosebrough, C. N. Coon and J. P. Mcmurtry. 2010. Feed intake regulation for the female broiler breeder: In theory and in practice. J. Appl. Poult. Res. 19:182-193. https://doi.org/10.3382/japr.2010-00167
  49. Richards, M. P. and M. Proszkowiec-Weglarz. 2007. Mechanisms regulating feed intake, energy expenditure, and body weight in poultry. Poult. Sci. 86:1478-1490. https://doi.org/10.1093/ps/86.7.1478
  50. Roseberry, A. G., H. Liu, A. C. Jackson, X. Cai and J. M. Friedman. 2004. Neuropeptide Y-mediated inhibition of proopiomelanocortin neurons in the arcuate nucleus shows enhanced desensitization in ob/ob mice. Neuron 41:711-722. https://doi.org/10.1016/S0896-6273(04)00074-1
  51. Saito, E., H. Kaiya, T. Tachibana, S. Tomonaga, D. Denbow, K. Kangawa and M. Furuse. 2005. Inhibitory effect of ghrelin on food intake is mediated by the corticotropin-releasing factor system in neonatal chickens. Regul. Pept. 125:201-208. https://doi.org/10.1016/j.regpep.2004.09.003
  52. Scott, J. W., S. A. Hawley, K. A. Green, M. Anis, G. Stewart, G. A. Scullion, D. G. Norman and D. G. Hardie. 2004. CBS domains form energy-sensing modules whose binding of adenosine ligands is disrupted by disease mutations. J. Clin. Invest. 113: 274-284. https://doi.org/10.1172/JCI19874
  53. Shaw, R. J., K. A. Lamia, D. Vasquez, S. H. Koo, N. Bardeesy, R. A. DePinho, M. Montminy and L. C. Cantley. 2005. The kinase LKB1 mediates glucose homeostasis in liver and therapeutic effects of metformin. Science 310:1642-1646. https://doi.org/10.1126/science.1120781
  54. Stapleton, D., K. I. Mitchelhill, G. Gao, J. Widmer, B. J. Michell, T. The, C. M. House, C. S. Fernandez, T. Cox, L. A. Witters and B. E. Kemp. 1996. Mammalian AMP-activated protein kinase subfamily. J. Biol. Chem. 271:611-614. https://doi.org/10.1074/jbc.271.2.611
  55. Stapleton, D., E. Woollatt, K. I. Mitchelhill, J. K. Nicholl, C. S. Fernandez, B. J. Michell, L. A. Witters, D. A. Power, G. R. Sutherland and B. E. Kemp. 1997. AMP-activated protein kinase isoenzyme family: subunit structure and chromosomal location. FEBS Lett. 409:452-456. https://doi.org/10.1016/S0014-5793(97)00569-3
  56. Takahashi, K. A. and R. D. Cone. 2005. Fasting induces a large, leptin-dependent increase in the intrinsic action potential frequency of orexigenic arcuate nucleus neuropeptide Y/Agouti-related protein neurons. Endocrinology 146:1043-1047. https://doi.org/10.1210/en.2004-1397
  57. Toshinai, K., Y. Date, N. Murakami, M. Shimada, M. S. Mondal, T. Shimbara, J. L. Guan, Q. P. Wang, H. Funahashi, T. Sakurai, S. Shioda, S. Matsukura, K. Kangawa and M. Nakazato. 2003. Ghrelin-induced food intake is mediated via the orexin pathway. Endocrinology 144:1506-1512. https://doi.org/10.1210/en.2002-220788
  58. Tsujii, S., and G. A. Bray. 1989. Acetylation alters the feeding response to MSH and beta-endorphin. Brain Res. Bull. 23: 165-169. https://doi.org/10.1016/0361-9230(89)90142-1
  59. Turnley, A. M., D. Stapleton, R. J. Mann, L. A. Witters, B. E. Kemp and P. F. Bartlett. 1999. Cellular distribution and developmental expression of AMP-activated protein kinase isoforms in mouse central nervous system. J. Neurochem. 72: 1707-1716.
  60. Xue, B. and B. Kahn. 2006. AMPK integrates nutrient and hormonal signals to regulate food intake and energy balance through effects in the hypothalamus and peripheral tissues. J. Physiol. 574:73-83. https://doi.org/10.1113/jphysiol.2006.113217
  61. Xu, P., C. J. Denbow, N. Meiri and D. M. Denbow. 2011. Fasting of 3-day-old chickens leads to changes in histone H3 methylation status. Physiol. Behav. 105:276-282.
  62. Xu, P., P. B. Siegel and D. M. Denbow. 2011. Genetic selection for body weight in chickens has altered responses of the brain's AMPK system to food intake regulation effect of ghrelin, but not obestatin. Behav. Brain Res. 221:216-226. https://doi.org/10.1016/j.bbr.2011.02.034
  63. Yaswen, L., N. Diehl, M. Brennan and U. Hochgeschwender. 1999. Obesity in the mouse model of pro-opiomelanocortin deficiency responds to peripheral melanocortin. Nat. Med. 5: 1066-1070. https://doi.org/10.1038/12506

Cited by

  1. Differential gene expression pattern in hypothalamus of chickens during fasting-induced metabolic reprogramming: Functions of glucose and lipid metabolism in the feed intake of chickens vol.93, pp.11, 2014, https://doi.org/10.3382/ps.2014-04047
  2. Effect of dexamethasone on hypothalamic expression of appetite-related genes in chickens under different diet and feeding conditions vol.7, pp.1, 2016, https://doi.org/10.1186/s40104-016-0084-x
  3. genes in chicken preadipocytes vol.88, pp.3, 2016, https://doi.org/10.1111/asj.12722
  4. Regulation of Agouti-Related Protein and Pro-Opiomelanocortin Gene Expression in the Avian Arcuate Nucleus vol.8, pp.1664-2392, 2017, https://doi.org/10.3389/fendo.2017.00075
  5. Hypothalamic AMPK as a Regulator of Energy Homeostasis vol.2016, pp.1687-5443, 2016, https://doi.org/10.1155/2016/2754078
  6. Sex differences in basal hypothalamic anorectic and orexigenic gene expression and the effect of quantitative and qualitative food restriction vol.9, pp.1, 2018, https://doi.org/10.1186/s13293-018-0178-6