AMPK; appetite; broiler; diet energy level; stress; General Veterinary
Abstract :
[en] This study aimed to characterize the effects of diets with different energy levels on the growth performance, plasma parameters, and central AMPK signaling pathway in broilers under dexamethasone (DEX)-induced stress. A total of 216 1-day-old male broiler chickens were allocated to groups fed with high (HED), National Research Council-recommended (control), or low (LED) energy diets. At 10 days old, chickens were treated with or without dexamethasone (DEX, 2 mg/kg body weight) for 3 consecutive days. HED increased broiler average daily gain (ADG) at 10 days old, compared with the LED (P < 0.05), while average daily feed intake (ADFI) and feed conversion rate (FCR) decreased as the dietary energy level increased (P < 0.05). Chickens fed a HED had higher total protein (TP) content, albumin (ALB), glucose (GLU), total cholesterol (TCHO), high-density lipoprotein (HDL) cholesterol, and low-density lipoprotein (LDL) cholesterol, compared with the control group (P < 0.05). At 13 days old, DEX decreased ADG and increased FCR in broilers fed with different energy diets (P < 0.05). The DEX-HED group had a higher ADFI than non-DEX treated HED group chickens. In addition, TP, ALB, triglycerides (TG), TCHO, HDL, and LDL content levels in the DEX group were higher than those in the control group (P < 0.05). The uric acid (UA) content of the LED group was higher than that of the HED group (P < 0.05). Further, gene expression levels of liver kinase B1, AMP-activated protein kinase α1, neuropeptide Y, and GC receptor in the hypothalamus were increased in chickens treated with DEX (P < 0.05). There was a trend toward interaction between plasma TCHO and hypothalamic LKB1 expression (0.05 < P < 0.1). In conclusion, this study suggests that HED improves growth performance, plasma glucose and total cholesterol at 10 days old broilers, but had no significant effect on performance, plasma parameters, and central AMPK in stressed broilers.
Disciplines :
Agriculture & agronomy
Author, co-author :
Hu, Xiyi; Department of Animal Science, Shandong Agricultural University, Taian, China
Li, Xianlei; Department of Animal Science, Shandong Agricultural University, Taian, China
Xiao, Chuanpi ; Université de Liège - ULiège > TERRA Research Centre ; Department of Animal Science, Shandong Agricultural University, Taian, China
Kong, Linglian; Department of Animal Science, Shandong Agricultural University, Taian, China
Zhu, Qidong; Department of Animal Science, Shandong Agricultural University, Taian, China
Song, Zhigang; Department of Animal Science, Shandong Agricultural University, Taian, China
Language :
English
Title :
Effects of Dietary Energy Level on Performance, Plasma Parameters, and Central AMPK Levels in Stressed Broilers.
Yuan L, Lin H, Jiang KJ, Jiao H. C., Song ZG., Corticosterone administration and high-energy feed results in enhanced fat accumulation and insulin resistance in broiler chickens. Br Poult Sci. (2008) 49:487–95. 10.1080/0007166080225173118704796
Elenkov IJ, Chrousos GP. Stress Hormones, Th1/Th2 patterns, pro/anti-inflammatory cytokines and susceptibility to disease. Trends Endocrinol Metab. (1999) 10:359–68. 10.1016/S1043-2760(99)00188-510511695
Trinchieri G. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat Rev Immunol. (2003) 3:133–46. 10.1038/nri100112563297
Yang J, Liu L, Sheikhahmadi A. Effects of corticosterone and dietary energy on immune function of broiler chickens. PLoS One. (2015) 10:e0119750. 10.1371/journal.pone.011975025803644
Liu L, Wang X, Jiao H, Zhao J, Lin H. Glucocorticoids inhibited hypothalamic target of rapamycin in high fat diet-fed chicks. Poult Sci. (2015) 94:2221–7. 10.3382/ps/pev16826188033
Chrousos GP, Kino T. Glucocorticoid action networks and complex psychiatric and/or somatic disorders. Stress. (2007) 10:213–9. 10.1080/1025389070129211917514590
Kino T, Chrousos GP. Glucocorticoid effects on gene expression. Tech Behav Neural Sci. (2005) 15:295–311. 10.1016/S0921-0709(05)80017-3
Adam TC, Epel ES. Stress, eating and the reward system. Physiol Behav. (2007) 91:449–58. 10.1016/j.physbeh.2007.04.011
Das TK, Mondal MK, Biswas P, Bairagi B, Samanta CC. Influence of level of dietary inorganic and organic copper and energy level on the performance and nutrient utilization of broiler chickens. Asian-Australas J Anim Sci. (2010) 23:82–9. 10.5713/ajas.2010.60150
Alabi OJ, Ng'Ambi JW, Norris D. Dietary energy level for optimum productivity and carcass characteristics of indigenous Venda chickens raised in closed confinement. S Afr J Anim Sci. (2014) 43:75–80. 10.4314/sajas.v43i5.14
O'Connor DB, O'Connor RC. Perceived changes in food intake in response to stress: the role of conscientiousness. Stress Health. (2004) 20:279–91. 10.1002/smi.1028
Fernandes SS, Koth AP, Parfitt GM. Enhanced cholinergic-tone during the stress induce a depressive-like state in mice. Behav Brain Res. (2018) 347:17–25. 10.1016/j.bbr.2018.02.04429501509
Epel E, Lapidus R, McEwen B, Brownell K. Stress may add bite to appetite in women: a laboratory study of stress-induced cortisol and eating behavior. Psychoneuroendocrinology. (2001) 26:37–49. 10.1016/S0306-4530(00)00035-411070333
Pecoraro N, Reyes F, Gomez F, Bhargava A, Dallman MF. Chronic stress promotes palatable feeding, which reduces signs of stress: feedforward and feedback effects of chronic stress. Endocrinology. (2004) 145:3754–62. 10.1210/en.2004-030515142987
Coccurello R, Romano A, Giacovazzo G. Increased intake of energy-dense diet and negative energy balance in a mouse model of chronic psychosocial defeat. Eur J Nutr. (2018) 57:1485–98. 10.1007/s00394-017-1434-y28314964
Zellner DA, Loaiza S, Gonzalez Z. Food selection changes under stress. Physiol Behav. (2006) 87:789–93. 10.1016/j.physbeh.2006.01.01416519909
Auvinen HE, Romijn J.A, Biermasz NR. Effects of high fat diet on the Basal activity of the hypothalamus-pituitary-adrenal axis in mice: a systematic review. Horm Metab Res. (2011) 43:899–906. 10.1055/s-0031-129130522068812
la Fleur SE, Houshyar H, Roy M, Dallman MF. Choice of lard, but not total lard calories, damps adrenocorticotropin responses to restraint. Endocrinology. (2005) 146:2193–9. 10.1210/en.2004-160315705773
Covasa M, Forbes JM. Selection of foods by broiler chickens following corticosterone administration. Br Poult Sci. (1995) 36:489–501. 10.1080/000716695084177947583379
Wang XJ, Xu SH, Liu L, Song ZG, Jiao HC, Lin H. Dietary fat alters the response of hypothalamic neuropeptide Y to subsequent energy intake in broiler chickens. J Exp Biol. (2016) 220:607–14. 10.1242/jeb.14379227903700
Lu Q, Yang Y, Jia S. SRC1 deficiency in hypothalamic arcuate nucleus increases appetite and body weight [published online ahead of print, 2018 Oct 1]. J Mol Endocrinol. (2018) 62:37–46. 10.1530/JME-18-0075
Boswell T, Li Q, Takeuchi S. Neurons expressing neuropeptide Y mRNA in the infundibular hypothalamus of Japanese quail are activated by fasting and co-express agouti-related protein mRNA. Brain Res Mol Brain Res. (2002) 100:31–42. 10.1016/S0169-328X(02)00145-612008019
Richards MP. Genetic regulation of feed intake and energy balance in poultry. Poult Sci. (2003) 82:907–16. 10.1093/ps/82.6.90712817445
Chen C, Wang H, Jiao H, Wang X, Zhao J, Lin H. Feed habituation alleviates decreased feed intake after feed replacement in broilers. Poult Sci. (2018) 97:733–42. 10.3382/ps/pex35829253224
Saha AK, Ruderman NB. Malonyl-CoA and AMP-activated protein kinase: An expanding partnership. Mol Cell Biochem. (2003) 253:65–70. 10.1023/A:102605330203614619957
Proszkowiec-Weglarz M, Richards MP, Ramachandran R, McMurtry JP. Characterization of the AMP-activated protein kinase pathway in chickens. Comp Biochem Physiol B Biochem Mol Biol. (2006) 143:92–106. 10.1016/j.cbpb.2005.10.00916343965
Liu L, Wang X, Jiao H. Glucocorticoids induced high fat diet preference via activating hypothalamic AMPK signaling in chicks. Gen Comp Endocrinol. (2017) 249:40–7. 10.1016/j.ygcen.2017.02.01828263818
Cai Y, Song Z, Zhang X, Wang X, Jiao H, Lin H. Increased de novo lipogenesis in liver contributes to the augmented fat deposition in dexamethasone exposed broiler chickens (Gallus gallus domesticus). Comp Biochem Physiol C Toxicol Pharmacol. (2009) 150:164–9. 10.1016/j.cbpc.2009.04.00519393339
Cai Y, Song Z, Wang X, Jiao H, Lin H. Dexamethasone-induced hepatic lipogenesis is insulin dependent in chickens (Gallus gallus domesticus). Stress. (2011) 14:273–81. 10.3109/10253890.2010.54344421294661
Wang X, Lin H, Song Z, Jiao H. Dexamethasone facilitates lipid accumulation and mild feed restriction improves fatty acids oxidation in skeletal muscle of broiler chicks (Gallus gallus domesticus). Comp Biochem Physiol C Toxicol Pharmacol. (2010) 151:447–54. 10.1016/j.cbpc.2010.01.01020138241
Song Z, Zhao T, Liu L, Jiao H, Lin H. Effect of copper on antioxidant ability and nutrient metabolism in broiler chickens stimulated by lipopolysaccharides. Arch Anim Nutr. (2011) 65:366–75. 10.1080/1745039X.2011.60975322164958
Liu SQ, Zhao JP, Fan XX. Rapamycin, a specific inhibitor of the target of rapamycin complex 1, disrupts intestinal barrier integrity in broiler chicks. J Anim Physiol Anim Nutr (Berl). (2016) 100:323–30. 10.1111/jpn.1237526249793
Huang C, Jiao H, Song Z, Zhao J, Wang X, Lin H. Heat stress impairs mitochondria functions and induces oxidative injury in broiler chickens. J Anim Sci. (2015) 93:2144–53. 10.2527/jas.2014-873926020310
Zhao JP, Cui DP, Zhang ZY, Jiao HC, Song ZG, Lin H. Live performance, carcass characteristic and blood metabolite responses of broilers to two distinct corn types with different extent of grinding. J Anim Physiol Anim Nutr (Berl). (2017) 101:378–88. 10.1111/jpn.1245127080870
Liu L, Xu S, Wang X, Jiao H, Lin H. Peripheral insulin doesn't alter appetite of broiler chicks. Asian-Australas J Anim Sci. (2016) 29:1294–9. 10.5713/ajas.15.067426954230
Higgins SE, Ellestad LE, Trakooljul N. Transcriptional and pathway analysis in the hypothalamus of newly hatched chicks during fasting and delayed feeding. BMC Genomics. (2010) 11:162. 10.1186/1471-2164-11-16220214824
Tang D, Wu J, Jiao H, Wang X, Zhao J, Lin H. The development of antioxidant system in the intestinal tract of broiler chickens. Poult Sci. (2019) 98:664–678. 10.3382/ps/pey41530289502
Uerlings J, Song ZG, Hu XY. Heat exposure affects jejunal tight junction remodeling independently of adenosine monophosphate-activated protein kinase in 9-day-old broiler chicks. Poult Sci. (2018) 97:3681–90. 10.3382/ps/pey22929901744
Zhao JP, Bao J, Wang XJ, Jiao HC, Song ZG, Lin H. Altered gene and protein expression of glucose transporter1 underlies dexamethasone inhibition of insulin-stimulated glucose uptake in chicken muscles. J Anim Sci. (2012) 90:4337–45. 10.2527/jas.2012-510022859751
Zhao PY, Kim IH. Effect of diets with different energy and lysophospholipids levels on performance, nutrient metabolism, and body composition in broilers. Poult Sci. (2016) 96:1341–7. 10.3382/ps/pew46928204735
Hu X, Wang Y, Sheikhahmadi A. Effects of dietary energy level on appetite and central adenosine monophosphate-activated protein kinase (AMPK) in broilers. J Anim Sci. (2019) 97:4488–95. 10.1093/jas/skz31231586423
West DB, York B. Dietary fat, genetic predisposition, and obesity: lessons from animal models. Am J Clin Nutr. (1998) 67:505S−12S. 10.1093/ajcn/67.3.505S9497161
Murtaugh MA, Herrick JS, Sweeney C. Diet composition and risk of overweight and obesity in women living in the southwestern United States. J Am Diet Assoc. (2007) 107:1311–21. 10.1016/j.jada.2007.05.00817659896
Niu ZY, Shi JS, Liu FZ, Wang XH, Gao CQ, Yao LK. Effects of dietary energy and protein on growth performance and carcass quality of broilers during starter phase. Int J Poult Sci. (2009) 8:508–11. 10.3923/ijps.2009.508.511
Wang JP, Zhang ZF, Yan L, Kim IH. Effects of dietary supplementation of emulsifier and carbohydrase on the growth performance, serum cholesterol and breast meat fatty acids profile of broiler chickens. Anim Sci J. (2015) 87:250–6. 10.1111/asj.1241226278708
Saxena R, Saxena VK, Tripathi V. Dynamics of gene expression of hormones involved in the growth of broiler chickens in response to the dietary protein and energy changes. Gen Comp Endocrinol. (2020) 288:113377. 10.1016/j.ygcen.2019.11337731881203
Maiorka A, Dahlke F, Santin E, Kessler A, Penz AM, Jr. Effect of energy levels of diets formulated on total or digestible amino acid basis on broiler performance. Rev Bras Cienc Avic. (2004) 6:87–91. 10.1590/S1516-635X200400020000319086597
Ge XK, Wang AA, Ying ZX. Effects of diets with different energy and bile acids levels on growth performance and lipid metabolism in broilers. Poult Sci. (2019) 98:887–95. 10.3382/ps/pey43430239873
Lv ZP, Peng YZ, Zhang BB, Fan H, Liu D, Guo YM. Glucose and lipid metabolism disorders in the chickens with dexamethasone-induced oxidative stress. J Anim Physiol Anim Nutr (Berl). (2018) 102:e706–e17. 10.1111/jpn.1282329098735
Dong H, Lin H, Jiao HC, Song ZG, Zhao JP, Jiang KJ. Altered development and protein metabolism in skeletal muscles of broiler chickens (Gallus gallus domesticus) by corticosterone. Comp Biochem Physiol A Mol Integr Physiol. (2007) 147:189–95. 10.1016/j.cbpa.2006.12.03417289413
Hu XF, Guo YM, Huang BY, Bun S, Zhang LB, Li JH. The effect of glucagon-like peptide 2 injection on performance, small intestinal morphology, and nutrienttransporter expression of stressed broiler chickens. Poult Sci. (2010) 89:1967–74. 10.3382/ps.2009-0054720709983
Limdi JK, Hyde GM. Evaluation of abnormal liver function tests. Postgrad Med J. (2003) 79:307–12. 10.1136/pmj.79.932.307
Okumura JI, Tasaki I. Effect of fasting, refeeding and dietary protein level on uric acid and ammonia content of blood, liver and kidney in chickens. J Nutr. (1969) 97:316–20. 10.1093/jn/97.3.3165773332
Uyeda K, Repa JJ. Carbohydrate response element binding protein, ChREBP, a transcription factor coupling hepatic glucose utilization and lipid synthesis. Cell Metab. (2006) 4:107–10. 10.1016/j.cmet.2006.06.00816890538
Prola L, Nery J, Lauwaerts A. Effects of N,N-dimethylglycine sodium salt on apparent digestibility, vitamin E absorption, and serum proteins in broiler chickens fed a high- or low-fat diet. Poult Sci. (2013) 92:1221–6. 10.3382/ps.2012-0246523571331
Helkin A, Stein JJ, Lin S, Siddiqui S, Maier KG, Gahtan V. Dyslipidemia part 1–review of lipid metabolism and vascular cell physiology. Vasc Endovascular Surg. (2016) 50:107–18. 10.1177/153857441662865426983667
Song D, Wang YW, Hou YJ. The effects of dietary supplementation of microencapsulated Enterococcus faecalis and the extract of Camellia oleifera seed on growth performance, immune functions, and serum biochemical parameters in broiler chickens1. J Anim Sci. (2016) 94:3271–7. 10.2527/jas.2016-0286
Lai W, Huang W, Dong B. Effects of dietary supplemental bile acids on performance, carcass characteristics, serum lipid metabolites and intestinal enzyme activities of broiler chickens. Poult Sci. (2018) 97:196–202. 10.3382/ps/pex28829136214
Siritarino PW. Effects of diet on high-density lipoprotein cholesterol. Curr Atheroscler Rep. (2011) 13:453–60. 10.1007/s11883-011-0207-y
Khan TJ, Kuerban A, Razvi SS. In vivo evaluation of hypolipidemic and antioxidative effect of ‘Ajwa’ (Phoenix dactylifera L.) date seed-extract in high-fat diet-induced hyperlipidemic rat model. Biomed Pharmacother. (2018) 107:675–80. 10.1016/j.biopha.2018.07.13430125841
Miller GJ, Miller NE. Plasma-high-density-lipoprotein concentration and development of ischaemic heart-disease. Lancet. (1975) 1:16–9. 10.1016/S0140-6736(75)92376-446338
Hermier D. Lipoprotein metabolism and fattening in poultry. J Nutr. (1997) 127:S805–S8. 10.1093/jn/127.5.805S9164241
Mantha L, Palacios E, Deshaies Y. Modulation of triglyceride metabolism by glucocorticoids in diet-induced obesity. Am J Physiol. (1999) 277:R455–R64. 10.1152/ajpregu.1999.277.2.R45510444552
Denis RG, Joly-Amado A, Cansell C. Central orchestration of peripheral nutrient partitioning and substrate utilization: implications for the metabolic syndrome. Diabetes Metab. (2014) 40:191–7. 10.1016/j.diabet.2013.11.00224332017
Morton GJ, Cummings DE, Baskin DG, Barsh GS, Schwartz MW. Central nervous system control of food intake and body weight. Nature. (2006) 443:289–95. 10.1038/nature0502616988703
Kuenzel WJ, Beck MM, Teruyama R. Neural sites and pathways regulating food intake in birds: a comparative analysis to mammalian systems. J Exp Zool. (1999) 283:348–64. 10.1002/(SICI)1097-010X(19990301/01)283:4/5<348::AID-JEZ5>3.0.CO12474867
Kalra SP, Dube MG, Sahu A, Phelps CP, Kalra PS. Neuropeptide Y secretion increases in the paraventricular nucleus in association with increased appetite for food. Proc Natl Acad Sci U S A. (1991) 88:10931–5. 10.1073/pnas.88.23.109311961764
Hahn TM, Breininger JF, Baskin DG, Schwartz MW. Coexpression of Agrp and NPY in fasting-activated hypothalamic neurons. Nat Neurosci. (1998) 1:271–2. 10.1038/108210195157
Larsen PJ, Jessop DS, Chowdrey HS, Lightman SL, Mikkelsen JD. Chronic administration of glucocorticoids directly upregulates prepro-neuropeptide Y and Y1-receptor mRNA levels in the arcuate nucleus of the rat. J Neuroendocrinol. (1994) 6:153–9. 10.1111/j.1365-2826.1994.tb00566.x8049712
Kino T, De Martino MU, Charmandari E, Mirani M, Chrousos GP. Tissue glucocorticoid resistance/hypersensitivity syndromes. J Steroid Biochem Mol Biol. (2003) 85:457–67. 10.1016/S0960-0760(03)00218-812943736
Chrousos GP, Kino T. Intracellular glucocorticoid signaling: a formerly simple system turns stochastic. Sci STKE. (2005) 304:pe48. 10.1126/stke.3042005pe4816204701
Kahn BB, Alquier T, Carling D, Hardie DG. AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism. Cell Metab. (2005) 1:15–25. 10.1016/j.cmet.2004.12.00316054041
Scerif M, Füzesi T, Thomas JD. CB1 receptor mediates the effects of glucocorticoids on AMPK activity in the hypothalamus. J Endocrinol. (2013) 219:79–88. 10.1530/JOE-13-019223884964
Spasic MR, Callaerts P, Norga KK. AMP-activated protein kinase (AMPK) molecular crossroad for metabolic control and survival of neurons. Neuroscientist. (2009) 15:309–16. 10.1177/107385840832780519359670
Lim CT, Kola B, Korbonits M. AMPK as a mediator of hormonal signalling. J Mol Endocrinol. (2010) 44:87–97. 10.1677/JME-09-0063
Liu F, Benashski SE, Persky R, Xu Y, Li J, McCullough LD. Age-related changes in AMP-activated protein kinase after stroke. Age (Dordr). (2012) 34:157–68. 10.1007/s11357-011-9214-821360073
Minokoshi Y, Alquier T, Furukawa N, Kim YB, Lee A, Xue B. AMP-kinase regulates food intake by responding to hormonal and nutrient signals in the hypothalamus. Nature. (2004) 428:569–74. 10.1038/nature0244015058305
Yi CO, Jeon BT, Shin HJ, Jeong EA, Chang KC, Lee JE. Resveratrol activates AMPK and suppresses LPS-induced NF-κB-dependent COX-2 activation in RAW 264.7 macrophage cells. Anat Cell Biol. (2011) 44:194–203. 10.5115/acb.2011.44.3.19422025971
Viollet B, Andreelli F, Jorgensen SB, Perrin C, Flamez D, Mu J. Physiological role of AMP-activated protein kinase (AMPK): insights from knockout mouse models. Biochem Soc Trans. (2003) 31:216–9. 10.1042/bst031021612546688
Christ-Crain M, Kola B, Lolli F. AMP-activated protein kinase mediates glucocorticoid-induced metabolic changes: a novel mechanism in Cushing's syndrome. FASEB J. (2008) 22:1672–83. 10.1096/fj.07-09414418198220
Shimizu H, Arima H, Watanabe M, Goto M, Banno R, Sato I, et al. Glucocorticoids increase neuropeptide Y and agouti-related peptide gene expression via adenosine monophosphateactivated protein kinase signaling in the arcuate nucleus of rats. Endocrinology. (2008) 149:4544–53. 10.1210/en.2008-0229
Tataranni PA, Larson DE, Snitker S. Effects of glucocorticoids on energy metabolism and food intake in humans. Am J Physiol. (1996) 271:E317–E25. 10.1152/ajpendo.1996.271.2.E3178770026
