Effect of the acute heat stress on serum endotoxin concentration and the expression of TLR4 mRNA in liver of Arbor Acres broiler chickens
Shu-cheng Huang A B , Ya-Fen Fu A , Mujeeb Ur Rehman B , Kun Li B , Yan-fang Lan B , Wei Liu A , Hou-qiang Luo B , Hui Zhang B , Li-hong Zhang B , Ya-nan Hao B and Zong-xi Tong A C
+ Author Affiliations
- Author Affiliations
A College of Animal Science and Veterinary Medicine, Henan Agricultural University, Zhengzhou 450002, China.
B College of Veterinary Medicine, Huazhong Agricultural University, Wuhan 430070, China.
C Corresponding author. Email: 2578032310@qq.com
Animal Production Science 58(12) 2200-2206 https://doi.org/10.1071/AN16423
Submitted: 2 July 2016 Accepted: 23 July 2017 Published: 21 February 2018
Abstract
This study was undertaken to investigate the relationship between gut-derived endotoxin and the Toll-like receptor 4 (TLR4) expression in the liver of broilers under acute heat stress (AHS). For this purpose, 120 Arbor Acres chicks were randomised into two groups: control temperature group (CT group, 22 ± 1°C) and high temperature group (HT group, 38 ± 1°C). The chicks received AHS at Day 28 and their small intestine, liver and blood samples were collected after 2 h, 5 h and 10 h to examine the histopathology, biochemical parameters, endotoxin concentrations and TLR4 expression. The results showed that damaged intestinal villi and severe congestion of the hepatic sinusoids were observed, especially after 10 h of AHS in the HT group. In addition, the levels of alanine transferase, aspartate transaminase, and direct bilirubin, except alkaline phosphataseafter were significantly elevated (P < 0.05) and total bilirubin (P < 0.01) and albumin (P < 0.05) were decreased after 10 h of AHS as compared with the CT group, which are associated with liver function. Moreover, the mRNA expression of TLR4 in the liver was noticeably upregulated (P < 0.05) during AHS with significantly increased in endotoxin concentration (P < 0.01) of broilers. Altogether, these findings suggest that the upregulated expression of TLR4 mRNA was triggered via gut-derived endotoxin in heat stress-induced liver injury.
Additional keyword: liver injury.
References
Aderem A, Ulevitch RJ (2000) Toll-like receptors in the induction of the innate immune response. Nature 406, 782–787.| Toll-like receptors in the induction of the innate immune response.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3cvjtVOhuw%3D%3D&md5=a874dcf6ae314ae441db8a3e18538cb4CAS |
Amar J, Burcelin R, Ruidavets J, Cani P, Fauvel J, Alessi MC, Chamontin B, Ferrieres J (2008) Energy intake is associated with endotoxemia in apparently healthy men. The American Journal of Clinical Nutrition 87, 1219–1223.
Bangen JM, Ulrich S, Flohé SB (2007) Diverse regulatory activity of human heat shock proteins 60 and 70 on endotoxin-induced inflammation. Biochemical and Biophysical Research Communications 359, 709–715.
| Diverse regulatory activity of human heat shock proteins 60 and 70 on endotoxin-induced inflammation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmsFyktbo%3D&md5=557ca8c275b07b6f8ac239221c505c47CAS |
Berg RD (1992) Bacterial translocation from the gastrointestinal tract. Advances in Experimental Medicine and Biology 3, 11–30.
Dokladny K, Moseley PL, Ma TY (2006) Physiologically relevant increase in temperature causes an increase in intestinal epithelial tight junction permeability. American Journal of Physiology. Gastrointestinal and Liver Physiology 290, G204–G212.
| Physiologically relevant increase in temperature causes an increase in intestinal epithelial tight junction permeability.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhsFKht7o%3D&md5=41043f0c0487c4d514155228a5dfdfa8CAS |
Douhara A, Moriya K, Yoshiji H, Noguchi R, Namisaki T, Kitade M, Kaji K, Aihara Y, Nishimura N, Takeda K, Okura Y, Kawaratani H, Fukui H (2015) Reduction of endotoxin attenuates liver fibrosis through suppression of hepatic stellate cell activation and remission of intestinal permeability in a rat non-alcoholic steatohepatitis model. Molecular Medicine Reports 11, 1693–1700.
| Reduction of endotoxin attenuates liver fibrosis through suppression of hepatic stellate cell activation and remission of intestinal permeability in a rat non-alcoholic steatohepatitis model.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXltVWitL8%3D&md5=08182aa314709620ac7622cc2330e9a2CAS |
Fisher JE, Mckenzie TJ, Lillegard JB, Yue Y, Juskewitch JE, Nedredal GI, Brunn GJ, Yi ES, Smyrk TC, Nyberg SL (2013) Role of kupffer cells and toll-like receptor 4 in acetaminophen-induced acute liver failure. The Journal of Surgical Research 180, 147–155.
| Role of kupffer cells and toll-like receptor 4 in acetaminophen-induced acute liver failure.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvFWht7zF&md5=8e9d3a6679023314a2370afcb62b488aCAS |
Flanagan SW, Ryan AJ, Gisolfi CV, Moseley PL (1995) Tissue-specific hsp70 response in animals undergoing heat stress. The American Journal of Physiology 268, R28–R32.
Gao ZM, Liu FH, Yin P, Wan CR, He SS, Liu XX, Zhao H, Liu T, Xu JQ, Guo SN (2013) Inhibition of heat-induced apoptosis in rat small intestine and IEC-6 cells through the AKT signaling pathway. BMC Veterinary Research 9, 241
| Inhibition of heat-induced apoptosis in rat small intestine and IEC-6 cells through the AKT signaling pathway.Crossref | GoogleScholarGoogle Scholar |
Garcia-Martinez R, Caraceni P, Bernardi M, Gines P, Arroyo V, Jalan R (2013) Albumin: pathophysiologic basis of its role in the treatment of cirrhosis and its complications. Hepatology (Baltimore, Md.) 58, 1836–1846.
| Albumin: pathophysiologic basis of its role in the treatment of cirrhosis and its complications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhslWqsLnK&md5=5a55a2aa901481520992bb8216692b06CAS |
Geraert PA, Guillaumin S, Leclercq B (1993) Are genetically lean broilers more resistant to hot climate. British Poultry Science 34, 643–653.
| Are genetically lean broilers more resistant to hot climate.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2c%2FmtFGruw%3D%3D&md5=88241436e06151f16eb74b6149378312CAS |
Guo SH, Alsadi R, Said HM, Ma TY (2012) Lipopolysaccharide causes an increase in intestinal tight junction permeability in vitro and in vivo by inducing enterocyte membrane expression and localization of TLR-4 and CD14. The Korean Journal of Physiology & Pharmacology; Official Journal of the Korean Physiological Society and the Korean Society of Pharmacology 182, 447–453.
Hall DM, Buettner GR, Oberley LW, Xu LJ, Matthes RD, Gisolfi CV (2001) Mechanisms of circulatory and intestinal barrier dysfunction during whole body hyperthermia. American Journal of Physiology. Heart and Circulatory Physiology 280, H509–H521.
Kregel KC, Moseley PL, Skidmore R, Gutierrez JA, Guerriero V (1995) Hsp70 accumulation in tissues of heat-stressed rats is blunted with advancing age. Journal of Applied Physiology (Bethesda, Md.) 79, 1673–1678.
Lambert GP (2009) Stress-induced gastrointestinal barrier dysfunction and its inflammatory effects. Journal of Animal Science 87, E101–E108.
| Stress-induced gastrointestinal barrier dysfunction and its inflammatory effects.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1M3mtVSrug%3D%3D&md5=90ce249586dd0e7ce13f7a43ffe6a301CAS |
Lee KCL, Baker LA, Stanzani G, Alibhai H, Chang YM, Palacios CJ, Leckie PJ, Giordano P, Priestnall SL, Antoine DJ, Jenkins RE, Goldring CE, Kevin Park B, Andreola F, Agarwal B, Mookerjee RP, Davies NA, Jalan R (2015) Extracorporeal liver assist device to exchange albumin and remove endotoxin in acute liver failure: results of a pivotal pre-clinical study. Journal of Hepatology 63, 634–642.
| Extracorporeal liver assist device to exchange albumin and remove endotoxin in acute liver failure: results of a pivotal pre-clinical study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtVKmt7vI&md5=88c132f9fe90a4997d97a742fed7b340CAS |
Li YB (2005) Effects of heat stressing on broiler immune parameter. Chinese Journal of Agricultural Biotechnology 13, 394–395.
Lina AT, Axelrod JH, Sarit D, Yossi O, Valery K, Eithan G, Johnny A, Rifaat S (2013) Natural killer cell-dependent anti-fibrotic pathway in liver injury via toll-like receptor-9. PLoS One 8, 1611–1614.
Liu CP, Fu J, Xu FP, Wang XS, Li S (2015) The role of heat shock proteins in oxidative stress damage induced by se deficiency in chicken livers. Biometals 28, 163–173.
| The role of heat shock proteins in oxidative stress damage induced by se deficiency in chicken livers.Crossref | GoogleScholarGoogle Scholar |
Moreira APB, Texeira TFS, Alessandra Barbosa F, Peluzio MDCG (2012) Influence of a high-fat diet on gut microbiota, intestinal permeability and metabolic endotoxaemia. British Journal of Nutrition 108, 801–809.
| Influence of a high-fat diet on gut microbiota, intestinal permeability and metabolic endotoxaemia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1yqtb3F&md5=6d3d1e742e9edc2c630a92daf6158578CAS |
Park CY, Jung SH, Bak JP, Lee SS, Rhee DK (2005) Comparison of the rabbit pyrogen test and limulus amoebocyte lysate assay for endotoxin in hepatitis b vaccines and the effect of aluminum hydroxide. Biologicals 33, 145–151.
| Comparison of the rabbit pyrogen test and limulus amoebocyte lysate assay for endotoxin in hepatitis b vaccines and the effect of aluminum hydroxide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXpslygt7w%3D&md5=505e78e2a71830cf217e10ea09e58ae2CAS |
Pearce SC, Mani V, Boddicker RL, Johnson JS, Weber TE, Ross JW, Rhoads RP, Baumgard LH, Gabler NK (2013) Heat stress reduces intestinal barrier integrity and favors intestinal glucose transport in growing pigs. PLoS One 8, e70215
| Heat stress reduces intestinal barrier integrity and favors intestinal glucose transport in growing pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXht1yqu7vL&md5=5aefb393e14e616b453e35f3036f1fa0CAS |
Ryan AJ, Matthes RD, Mitros FA, Gisolfi CV (1994) Heat stress does not sensitize rats to the toxic effects of bacterial lipopolysaccharide. Medicine and Science in Sports and Exercise 26, 687–694.
| Heat stress does not sensitize rats to the toxic effects of bacterial lipopolysaccharide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXltlajtb4%3D&md5=e954c781b8cc5f9952d0ec88fef6da3bCAS |
Shah N, Oca MMD, Jover-Cobos M, Tanamoto KI, Muroi M, Sugiyama KI, Davies NA, Mookerjee RP, Dhar DK, Jalan R (2013) Role of Toll-like receptor 4 in mediating multiorgan dysfunction in mice with acetaminophen induced acute liver failure. Liver Transplantation 19, 751–761.
| Role of Toll-like receptor 4 in mediating multiorgan dysfunction in mice with acetaminophen induced acute liver failure.Crossref | GoogleScholarGoogle Scholar |
Shahzad M, Liu JY, Gao JF, Wang Z, Zhang D, Nabi F, Li JK (2014) Hsp-90 inhibitor geldanamycin attenuates liver oxidative stress and toxicity in thiram-induced tibial dyschondroplasia. Pakistan Veterinary Journal 4, 545–547.
Shannon CH, Shaw W, Lowry SF, Calvano SE, Daniel R (2010) Acute inflammatory response to endotoxin in mice and humans. Clinical and Diagnostic Laboratory Immunology 12, 60–67.
Su GL, Hoesel LM, Bayliss J, Hemmila MR, Wang S (2010) Lipopolysaccharide binding protein inhibitory peptide protects against acetaminophen-induced hepatotoxicity. Am J Physiol-Gastr L 299, G1319–G1325.
Tokuda Y, Miura N, Kobayashi M, Hoshinaga Y, Murai A, Aoyama H, Ito H, Horio F (2015) Ascorbic acid deficiency increases endotoxin influx to portal blood and liver inflammatory gene expressions in ods rats. Nutrition (Burbank, Los Angeles County, Calif.) 31, 373–379.
| Ascorbic acid deficiency increases endotoxin influx to portal blood and liver inflammatory gene expressions in ods rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtFGrtrs%3D&md5=bac004b2879b3a7bb2dfee73ae2e9cabCAS |
Wang L, Xue B, Wang K, Li S, Li Z (2011) Effect of heat stress on endotoxin flux across mesenteric-drained and portal-drained viscera of dairy goat. Journal of Animal Physiology and Animal Nutrition 95, 468–477.
| Effect of heat stress on endotoxin flux across mesenteric-drained and portal-drained viscera of dairy goat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtVOntLbJ&md5=e23b3fa2a839961bb502d65ab1ee1599CAS |
Wang LF, Zhao ZW, Yang GQ, Wang YY, Zhu HS, Han LQ, Zhang Z, Yang GY (2012) Effects of acute lipopolysaccharide injury on liver nutrition metabolism in dairy goats. Chi J Anim Nutr 12, 2366–2374.
Yan Y, Zhao Y, Wang H, Fan M (2006) Pathophysiological factors underlying heatstroke. Medical Hypotheses 67, 609–617.
| Pathophysiological factors underlying heatstroke.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmtlGlsL4%3D&md5=1098e2b8856a712541ba18f2c00068d8CAS |
Yu J, Bao E (2008) Effect of acute heat stress on heat shock protein 70 and its corresponding mRNA expression in the heart, liver, and kidney of broilers. Asian-Australasian Journal of Animal Sciences 21, 1116–1126.
| Effect of acute heat stress on heat shock protein 70 and its corresponding mRNA expression in the heart, liver, and kidney of broilers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFaru7bK&md5=81cb95acfb19b5d6a3d5291634dc9073CAS |
Zhang HJ, Xu L, Drake VJ, Oberley LW, Kregel KC (2003) Heat-induced liver injury in old rats is associated with exaggerated oxidative stress and altered transcription factor activation. The FASEB Journal 17, 2293–2295.
