intestinal integrity; tight junction; AMP-activated protein kinase; heat stress; broiler
Abstract :
[en] Dysfunction of the intestinal epithelial barrier under elevated temperatures is assumed to prompt pathological conditions and to eventually impede chickens’ growth, resulting in massive economic losses in broiler industries. The aims of this research were to determine the impact of acute heat stress on the intestinal tight junction network of broiler chicks (Gallus domesticus L.) and to elucidate whether adenosine monophosphate-activated protein kinase (AMPK) was involved in the integrated response of the broiler's gastrointestinal tract to heat stress. A total of 80 9-day-old Arbor Acres chicks were subjected to temperature treatment (thermoneutral versus heat stress) and AMPK inhibition treatment (5 mg/kg body weight intraperitoneal injection of compound C vs. sham treatment) for 72 h. In addition to monitoring growth performance, the mRNA and protein levels of key tight junction proteins, target components of the AMPK pathway, and biomarkers of intestinal inflammation and oxidative stress were assessed in the jejunum under both stressors at 24 and 72 h. An increase of the major tight junction proteins, claudin-1 and zonula occludens-1, was implemented in response to an exacerbated expression of the AMP-activated protein kinase. Heat stress did not affect zootechnical performance but was confirmed by an increased gene expression of heat shock proteins 70 and 90 as well as heat shock factor-1. In addition, hyperthermia induced significant effects on tight junction proteins, although it was independent of AMPK.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Uerlings, Julie ; Université de Liège - ULiège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Ingénierie des productions animales et nutrition
Song, Zhigang; Shandong Agricultural University > Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention
Hu, Xiji; Shandong Agricultural University > ∗Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention
Wang, Shaokun; Shandong Agricultural University > ∗Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention
Lin, Hai; Shandong Agricultural University > ∗Shandong Provincial Key Laboratory of Animal Biotechnology and Disease Control and Prevention
Buyse, Johan; KULeuven > Laboratory of Livestock Physiology, Division of Animal and Human Health
Everaert, Nadia ; Université de Liège - ULiège > Agronomie, Bio-ingénierie et Chimie (AgroBioChem) > Ingénierie des productions animales et nutrition
Language :
English
Title :
Heat exposure affects jejunal tight junction remodeling independently of adenosine monophosphate-activated protein kinase in 9-day-old broiler chicks
Altan, O., A. Altan, I. Oguz, A. Pabu,ccuoglu, and S. Konyalioglu. 2000. Effects of heat stress on growth, some blood variables and lipid oxidation in broilers exposed to high temperature at an early age. Br. Poult. Sci. 41: 489-493.
Burkholder, K. M., K. L. Thompson, M. E. Einstein, T. J. Applegate, and J. A. Patterson. 2008. Influence of stressors on normal intestinal microbiota, intestinal morphology, and susceptibility to Salmonella Enteritidis colonization in broilers. Poult. Sci. 87: 1734-1741.
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.
Corton, J. M., J. G. Gillespie, S. A. Hawley, and D. G. Hardie. 1995. 5-aminoimidazole-4-carboxamide ribonucleoside. A specific method for activating AMP-activated protein kinase in intact cells? Eur. J. Biochem. 229: 558-565.
Dokladny, K., P. L. Moseley, and T. Y. Ma. 2006. Physiologically relevant increase in temperature causes an increase in intestinal epithelial tight junction permeability. Am. J. Physiol.-Gastrointest. Liver Physiol. 290: G204-G212.
Dokladny, K., D. Ye, J. C. Kennedy, P. L. Moseley, and T. Y. Ma. 2008. Cellular and molecular mechanisms of heat stressinduced up-regulation of occludin protein expression. Am. J. Pathol. 172: 659-670.
Elamin, E. E., A. A. Masclee, J. Dekker, H.-J. Pieters, and D. M. Jonkers. 2013. Short-chain fatty acids activate AMPactivated protein kinase and ameliorate ethanol-induced intestinal barrier dysfunction in Caco-2 cell monolayers. J. Nutr. 143: 1872-1881.
Fanning, A. S., B. J. Jameson, L. A. Jesaitis, and J. M. Anderson. 1998. The tight junction protein ZO-1 establishes a link between the transmembrane protein occludin and the actin cytoskeleton. J. Biol. Chem. 273: 29745-29753.
Farquhar, M. G., and G. E. Palade. 1963. Junctional complexes in various epithelia. J. Cell Biol. 17: 375-412.
Geraert, P. A., J. C. F. Padilha, and S. Guillaumin. 1996. Metabolic and endocrine changes induced by chronic heatexposure in broiler chickens: growth performance, body composition and energy retention. Br. J. Nutr. 75: 195-204.
Groschwitz, K. R., and S. P. Hogan. 2009. Intestinal barrier function: molecular regulation and disease pathogenesis. J. Allergy Clin. Immunol. 124: 3-20.
Gu, X. H., Y. Hao, and X. L. Wang. 2012. Overexpression of heat shock protein 70 and its relationship to intestine under acute heat stress in broilers: 2. Intestinal oxidative stress. Poult. Sci. 91: 790-799.
Hall, D. M., G. R. Buettner, L. W. Oberley, L. Xu, R. D. Matthes, and C. V Gisolfi. 2001. Mechanisms of circulatory and intestinal barrier dysfunction during whole body hyperthermia. Am. J. Physiol.-Hear. Circ. Physiol. 280: H509-H521.
Hardie, D. G. 2004. The AMP-activated protein kinase pathway-new players upstream and downstream. J. Cell Sci. 117: 5479-5487
Hardie, D. G. 2011. AMP-activated protein kinase-an energy sensor that regulates all aspects of cell function. Genes Dev. 25: 1895-1908.
Hardie, D. G., and D. Carling. 1997. The AMP-activated protein kinase. Fuel gauge of the mammalian cell? Eur. J. Biochem. 246: 259-273.
Hawley, S. A., M. A. Selbert, E. G. Goldstein, A. M. Edelman, D. Carling, and D. G. Hardie. 1995. 5-AMP activates the AMPactivated protein kinase cascade, and Ca2+/calmodulin activates the calmodulin-dependent protein kinase I cascade, via three independent mechanisms. J. Biol. Chem. 270: 27186-27191.
He, S., F. Liu, L. Xu, P. Yin, D. Li, C. Mei, L. Jiang, Y. Ma, and J. Xu. 2016. Protective effects of ferulic acid against heat stressinduced intestinal epithelial barrier dysfunction in vitro and in vivo. PLoS One. 11: e0145236.
Horman, S., N. Morel, D. Vertommen, N. Hussain, D. Neumann, C. Beauloye, N. El Najjar, C. Forcet, B. Viollet, M. P. Walsh, L. Hue, and M. H. Rider. 2008. AMP-activated protein kinase phosphorylates and desensitizes smooth muscle myosin light chain kinase. J. Biol. Chem. 283: 18505-18512.
Humphrey, D. T. 2006. Are happy chickens safer chickens? Poultry welfare and disease susceptibility. Br. Poult. Sci. 47: 379-391.
Kalmar, B., and L. Greensmith. 2009. Induction of heat shock proteins for protection against oxidative stress. Adv. Drug. Deliv. Rev. 61: 310-318.
Kim, E.-K., I. Miller, S. Aja, L. E. Landree, M. Pinn, J. McFadden, F. P. Kuhajda, T. H. Moran, and G. V Ronnett. 2004. C75, a fatty acid synthase inhibitor, reduces food intake via hypothalamic AMP-activated protein kinase. J. Biol. Chem. 279: 19970-19976.
Kodiha, M., J. G. Rassi, C. M. Brown, and U. Stochaj. 2007. Localization of AMP kinase is regulated by stress, cell density, and signaling through the MEK-ERK1/2 pathway. Am. J. Physiol.-Cell Physiol. 293: C1427-C1436.
Lambert, G. P. 2009. Stress-induced gastrointestinal barrier dysfunction and its inflammatory effects. J. Anim. Sci. 87: E101-E108.
Lara, J. L., and H. M. Rostagno. 2013. Impact of heat stress on poultry production. Animals 3: 356-369.
Lei, K. Y., and S. J. Slinger. 1970. Energy utilization in the chick in relation to certain environmental stresses. Can. J. Anim. Sci. 50: 285-292.
Leon, L. R., and B. G. Helwig. 2010. Heat stroke: role of the systemic inflammatory response. J. Appl. Physiol. 109: 1980-1988.
Liu, X., H. Li, A. Lu, Y. Zhong, X. Hou, N. Wang, D. Jia, J. Zan, H. Zhao, J. Xu, and F. Liu. 2012. Reduction of intestinal mucosal immune function in heat-stressed rats and bacterial translocation. Int. J. Hyperth. 28: 756-765.
Livak, K. J., and T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-CT method. Methods 25: 402-408.
Madara, J. L. 1987. Intestinal absorptive cell tight junctions are linked to cytoskeleton. Am. J. Physiol.-Cell Physiol. 253: C171-C175.
Mandel, L. J., R. Bacallao, and G. Zampighi. 1993. Uncoupling of the molecular 'fence' and paracellular 'gate' functions in epithelial tight junctions. Nature 361: 552-555.
Moseley, P. L., C. Gapen, E. S. Wallen, M. E. Walter, and M. W. Peterson. 1994. Thermal stress induces epithelial permeability. Am. J. Physiol. Cell Physiol. 267: C425-C434.
Nalli, A. D., D. P. Kumar, S. Mahavadi, O. Al-Shboul, R. Alkahtani, J. F. Kuemmerle, J. R. Grider, and K. S. Murthy. 2014. Hypercontractility of intestinal longitudinal smooth muscle induced by cytokines is mediated by the nuclear factor-B/AMP-activated kinase/myosin light chain kinase pathway. J. Pharmacol. Exp. Ther. 350: 89-98.
Park, H.-Y., Y. Kunitake, N. Hirasaki, M. Tanaka, and T. Matsui. 2015. Theaflavins enhance intestinal barrier of Caco-2 Cell monolayers through the expression of AMP-activated protein kinase-mediated Occludin, Claudin-1, and ZO-1. Biosci. Biotechnol. Biochem. 79: 130-137.
Pearce, S. C., V. Mani, R. L. Boddicker, J. S. Johnson, T. E. Weber, J. W. Ross, R. P. Rhoads, L. H. Baumgard, and N. K. Gabler. 2013a. Heat stress reduces intestinal barrier integrity and favors intestinal glucose transport in growing pigs. PLoS One 8: e70215.
Pearce, S. C., V. Mani, T. E. Weber, R. P. Rhoads, J. F. Patience, L. H. Baumgard, and N. K. Gabler. 2013b. Heat stress and reduced plane of nutrition decreases intestinal integrity and function in pigs. J. Anim. Sci. 91: 5183-5193.
Peng, L., Z.-R. Li, R. S. Green, I. R. Holzman, and J. Lin. 2009. Butyrate enhances the intestinal barrier by facilitating tight junction assembly via activation of AMP-activated protein kinase in Caco-2 cell monolayers. J. Nutr. 139: 1619-1625.
Quinteiro-Filho, W. M., A. Ribeiro, V. Ferraz-de-Paula, M. L. Pinheiro, M. Sakai, L. R. M. Sa, A. J. P. Ferreira, and J. Palermo-Neto. 2010. Heat stress impairs performance parameters, induces intestinal injury, and decreases macrophage activity in broiler chickens. Poult. Sci. 89: 1905-1914.
Rodgers, L. S., and A. S. Fanning. 2011. Regulation of epithelial permeability by the actin cytoskeleton. Cytoskeleton 68: 653-660.
Shen, L., E. D. Black, E. D. Witkowski, W. I. Lencer, V. Guerriero, E. E. Schneeberger, and J. R. Turner. 2006. Myosin light chain phosphorylation regulates barrier function by remodeling tight junction structure. J. Cell Sci. 119: 2095-2106.
Soderholm, J. D., and M. H. Perdue. 2001. II. Stress and intestinal barrier function. Am. J. Physiol. Gastrointest. Liver Physiol. 280: G7-G13.
Sohail, M. U., M. E. Hume, J. A. Byrd, D. J. Nisbet, A. Ijaz, A. Sohail, M. Z. Shabbir, and H. Rehman. 2012. Effect of supplementation of prebiotic mannan-oligosaccharides and probiotic mixture on growth performance of broilers subjected to chronic heat stress. Poult. Sci. 91: 2235-2240.
Song, J., K. Xiao, Y. L. Ke, L. F. Jiao, C. H. Hu, Q. Y. Diao, B. Shi, and X. T. Zou. 2014. Effect of a probiotic mixture on intestinal microflora, morphology, and barrier integrity of broilers subjected to heat stress. Poult. Sci. 93: 581-588.
Turner, J. R. 2006. Molecular basis of epithelial barrier regulation. Am. J. Pathol. 169: 1901-1909.
Turner, J. R. 2009. Intestinal mucosal barrier function in health and disease. Nat. Rev. Immunol. 9: 799-809.
Umeda, K., J. Ikenouchi, S. Katahira-Tayama, K. Furuse, H. Sasaki, M. Nakayama, T. Matsui, S. Tsukita, M. Furuse, and S. Tsukita. 2006. ZO-1 and ZO-2 independently determine where claudins are polymerized in tight-junction strand formation. Cell 126: 741-754.
Varasteh, S., S. Braber, P. Akbari, J. Garssen, and J. Fink-Gremmels. 2015a. Differences in susceptibility to heat stress along the chicken intestine and the protective effects of galactooligosaccharides. PLoS One 10: e0138975.
Varasteh, S., S. Braber, J. Garssen, and J. Fink-Gremmels. 2015b. Galacto-oligosaccharides exert a protective effect against heat stress in a Caco-2 cell model. J. Funct. Foods 16: 265-277.
Voellmy, R., and F. Boellmann. 2007. Molecular Aspects of the Stress Response: Chaperones, Membranes and Networks. Pages 89-99 in P Csermely, and L. V'igh, eds. Springer, New York, NY.
Walker, J., H. B. Jijon, H. Diaz, P. Salehi, T. Churchill, and K. L. Madsen. 2005. 5-Aminoimidazole-4-carboxamide riboside (AICAR) enhances GLUT2-dependent jejunal glucose transport: a possible role for AMPK. Biochem. J. 385: 485-491.
Wang, T., Q. Yu, J. Chen, B. Deng, L. Qian, and Y. Le. 2010. PP2A mediated AMPK inhibition promotes HSP70 expression in heat shock response. PLoS One 5: e13096.
Xiao, G., L. Tang, F. Yuan, W. Zhu, S. Zhang, Z. Liu, Y. Geng, X. Qiu, Y. Zhang, and L. Su. 2013. Eicosapentaenoic acid enhances heat stress-impaired intestinal epithelial barrier function in Caco-2 cells. PLoS One 8: 1-11.
Xiao, G., F. Yuan, Y. Geng, X. Qiu, Z. Liu, J. Lu, L. Tang, Y. Zhang, and L. Su. 2015. Eicosapentaenoic acid enhances heatstroke-impared intestinal epithelial barrier function in rats. Shock 44: 348-356.
Yahav, S. 2000. Domestic fowl-strategies to confront environmental conditions. Poult. Avian Biol. Rev. 11: 81-95.
Yahav, S., and J. P. McMurtry. 2001. Thermotolerance acquisition in broiler chickens by temperature conditioning early in life-the effect of timing and ambient temperature. Poult. Sci. 80: 1662-1666.
Yang, P.-C., S.-H. He, and P.-Y. Zheng. 2007. Investigation into the signal transduction pathway via which heat stress impairs intestinal epithelial barrier function. J. Gastroenterol. Hepatol. 22: 1823-1831.
Zhang, L., J. Li, L. H. Young, and M. J. Caplan. 2006. AMPactivated protein kinase regulates the assembly of epithelial tight junctions. Proc. Natl. Acad. Sci. USA 103: 17272-17277.
Zheng, B., and L. C. Cantley. 2007. Regulation of epithelial tight junction assembly and disassembly by AMPactivated protein kinase. Proc. Natl. Acad. Sci. USA 104: 819-822.
Zhou, G., R. Myers, Y. Li, Y. Chen, X. Shen, J. Fenyk-Melody, M. Wu, J. Ventre, T. Doebber, N. Fujii, N. Musi, M. F. Hirshman, L. J. Goodyear, and D. E. Moller. 2001. Role of AMP-activated protein kinase in mechanism of metformin action. J. Clin. Invest. 108: 1167-1174.