Intestinal integrity, endotoxin transport and detoxification in pigs divergently selected for residual feed intake

Journal of Animal Science

Volumn 91, Issue 5, 2013, Pages 2141-2150

  Mani, V ^a   Harris, A J ^a   Keating, A F ^a   Weber, T E ^a   Dekkers, J C M ^a   Gabler, N K ^a  

^a IOWA STATE UNIVERSITY   (United States)

Author keywords

Endotoxin; Feed efficiency; Intestinal integrity; Pig

Indexed keywords

EID: 84882727283     PISSN: 00218812     EISSN: 15253163     Source Type: Journal    
DOI: 10.2527/jas.2012-6053     Document Type: Article

References (51)

1. Albin, D. M., J. E. Wubben, J. M. Rowlett, K. A. Tappenden, and R. A. Nowak. 2007. Changes in small intestinal nutrient transport and barrier function after lipopolysaccharide exposure in two pig breeds. J. Anim Sci 85: 2517-2523.
2. Barbe, F., K. Atanasova, and K. Van Reeth. 2011. Cytokines and acute phase proteins associated with acute swine influenza infection in pigs. Vet J 187: 48-53.
3. Barea, R. et al. 2010. Energy utilization in pigs selected for high and low residual feed intake. J. Anim Sci 88: 2062-2072.
4. Bates, J. M., J. Akerlund, E. Mittge, and K. Guillemin. 2007. Intestinal Alkaline Phosphatase Detoxifies Lipopolysaccharide and Prevents Inflammation in Zebrafish in Response to the Gut Microbiota. Cell Host & Microbe 2: 371-382.
5. Boddicker, N., N. K. Gabler, M. E. Spurlock, D. Nettleton, and J. C. Dekkers. 2011. Effects of ad libitum and restricted feed intake on growth performance and body composition of Yorkshire pigs selected for reduced residual feed intake. J. Anim Sci 89: 40-51.
6. Bol-Schoenmakers, M. et al. 2010. Intestinal alkaline phosphatase contributes to the reduction of severe intestinal epithelial damage. European Journal of Pharmacology 633: 71-77.
7. Bottje, W., N. R. Pumford, C. Ojano-Dirain, M. Iqbal, and K. Lassiter. 2006. Feed efficiency and mitochondrial function. Poultry science 85: 8-14.
8. Cai, W., D. S. Casey, and J. C. Dekkers. 2008. Selection response and genetic parameters for residual feed intake in Yorkshire swine. J. Anim Sci 86: 287-298.
9. Cani, P. D., and N. M. Delzenne. 2010. Gut Microbiota, Diet, Endotoxemia, and Diseases. Wiley-VCH Verlag GmbH & Co. KGaA.
10. de La Serre, C. B. et al. 2010. Propensity to high-fat diet-induced obesity in rats is associated with changes in the gut microbiota and gut inflammation. American Journal of Physiology-Gastrointestinal and Liver Physiology 299: G440-G448.
11. Diack, A. B., C. D. Gladney, M. A. Mellencamp, M. J. Stear, and P. D. Eckersall. 2011. Characterisation of plasma acute phase protein concentrations in a high health boar herd. Veterinary Immunology and Immunopathology 139: 107-112.
12. Dritz, S. S. et al. 1996. Influence of lipopolysaccharide-induced immune challenge and diet complexity on growth performance and acute-phase protein production in segregated early-weaned pigs. J. Anim Sci 74: 1620-1628.
13. Elsbach, P. 2000. Mechanisms of disposal of bacterial lipopolysaccharides by animal hosts. Microbes and Infection 2: 1171-1180.
14. Erridge, C., T. Attina, C. M. Spickett, and D. J. Webb. 2007. A high-fat meal induces low-grade endotoxemia: Evidence of a novel mechanism of postprandial inflammation. Am J Clin Nutr 86: 1286-1292.
15. Feulner, J. A. et al. 2004. Identification of acyloxyacyl hydrolase, a lipopolysaccharide-detoxifying enzyme, in the murine urinary tract. Infection and immunity 72: 3171-3178.
16. Gabler, N. K., J. S. Radcliffe, J. D. Spencer, D. M. Webel, and M. E. Spurlock. 2009. Feeding long-chain n-3 polyunsaturated fatty acids during gestation increases intestinal glucose absorption potentially via the acute activation of AMPK. J. Nutr Biochem 20: 17-25.
17. Gabler, N. K., J. D. Spencer, D. M. Webel, and M. E. Spurlock. 2008. n-3 PUFA attenuate lipopolysaccharide-induced down-regulation of toll-like receptor 4 expression in porcine adipose tissue but does not alter the expression of other immune modulators. J. Nutr Biochem 19: 8-15.
18. Gardiner, K. R. et al. 1995. Significance of systemic endotoxaemia in inflammatory bowel disease. Gut 36: 897-901.
19. Gilbert, H. et al. 2007. Genetic parameters for residual feed intake in growing pigs, with emphasis on genetic relationships with carcass and meat quality traits. J. Anim Sci 85: 3182-3188.
20. Hall, W. F., T. E. Eurell, R. D. Hansen, and L. G. Herr. 1992. Serum haptoglobin concentration in swine naturally or experimentally infected with Actinobacillus pleuropneumoniae. J. Am Vet Med Assoc 201: 1730-1733.
21. Herd, R. M., and P. F. Arthur. 2009. Physiological basis for residual feed intake. J. Anim Sci 87: E64-71.
22. Kimball, S. R. et al. 2003. Endotoxin induces differential regulation of mTOR-dependent signaling in skeletal muscle and liver of neonatal pigs. Am J Physiol Endocrinol Metab 285: E637-644.
23. Lackeyram, D., C. Yang, T. Archbold, K. C. Swanson, and M. Z. Fan. 2010. Early weaning reduces small intestinal alkaline phosphatase expression in pigs. J. Nutr 140: 461-468.
24. Lallès, J.-P. 2010. Intestinal alkaline phosphatase: Multiple biological roles in maintenance of intestinal homeostasis and modulation by diet. Nutrition Reviews 68: 323-332.
25. Livak, K. J., and T. D. Schmittgen. 2001. Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2-ΔΔCT Method. Methods 25: 402-408.
26. Lu, M. et al. 2005. Lipopolysaccharide deacylation by an endogenous lipase controls innate antibody responses to Gram-negative bacteria. Nat Immunol 6: 989-994.
27. May, K. D., J. E. Wells, C. V. Maxwell, and W. T. Oliver. 2012. Granulated lysozyme as an alternative to antibiotics improves growth performance and small intestinal morphology of 10-dayold pigs. J. Anim Sci 90: 1118-1125.
28. McDermott, C., and B. Fenwick. 1992. Neutrophil activation associated with increased neutrophil acyloxyacyl hydrolase activity during inflammation in cattle. Am J Vet Res 53: 803-807.
29. Moeser, A. J., L. B. Borst, B. L. Overman, and J. S. Pittman. 2012. Defects in small intestinal epithelial barrier function and morphology associated with peri-weaning failure to thrive syndrome (PFTS) in swine. Research in veterinary science 93: 975-982.
30. Munford, R., M. Lu, and A. Varley. 2009. Chapter 2 Kill the Bacteria and Also Their Messengers? In: W. A. Frederick (ed.) Advances in Immunology No. Volume 103. p. 29-48. Academic Press.
31. Murata, H., N. Shimada, and M. Yoshioka. 2004. Current research on acute phase proteins in veterinary diagnosis: An overview. Vet J 168: 28-40.
32. Nyachoti, C. M., E. Kiarie, S. K. Bhandari, G. Zhang, and D. O. Krause. 2012. Weaned pig responses to Escherichia coli K88 oral challenge when receiving a lysozyme supplement. J. Anim Sci 90: 252-260.
33. Orellana, R. A. et al. 2007. Insulin stimulates muscle protein synthesis in neonates during endotoxemia despite repression of translation initiation. Am J Physiol Endocrinol Metab 292: E629-636.
34. Pineiro, C., M. Piñeiro, J. Morales, M. Andrés, E. Lorenzo, M. D. Pozo, M. A. Alava, and F. Lampreave. 2009. Pig-MAP and haptoglobin concentration reference values in swine from commercial farms. Vet J 179:78-84.
35. Pineiro, M., C. Piñeiro, R. Carpintero, J. Morales, F. M. Campbell, P. D. Eckersall, M. J. M. Toussaint, and F. Lampreave. 2007. Characterisation of the pig acute phase protein response to road transport. Vet J 173: 669-674.
36. Pinton, P., C. Braicu, J.-P. Nougayrede, J. Laffitte, I. Taranu, and I. P. Oswald. 2010. Deoxynivalenol impairs porcine intestinal barrier function and decreases the protein expression of claudin-4 through a mitogen-activated protein kinase-dependent mechanism. J. Nutr. 140:1956-1962.
37. Poelstra, K. et al. 1997. Dephosphorylation of endotoxin by alkaline phosphatase in vivo. Am J Pathol 151: 1163-1169.
38. Rakhshandeh, A., and C. F. de Lange. 2012. Evaluation of chronic immune system stimulation models in growing pigs. Animal: An international journal of animal bioscience 6: 305-310.
39. Ravin, H. A., D. Rowley, C. Jenkins, and J. Fine. 1960. On the absorption of bacterial endotoxin from the gastro-intestinal tract of the normal and shocked animal. J. Exp Med 112: 783-792.
40. Sandelin, B. A. 2005. Association of mitochondrial biochemistry and electron transport chain protein expression with feed efficiency in Angus cattle. PhD. Dissertation, Univ. Arkansas, Fayetteville
41. Schinckel, A. P. et al. 1995. Effects of antigenic challenge on growth and composition of segregated early-weaned pigs. Swine Health and Production 3: 228-234.
42. Suzuki, K., H. Ota, S. Sasagawa, T. Sakatani, and T. Fujikura. 1983. Assay method for myeloperoxidase in human polymorphonuclear leukocytes. Analytical Biochemistry 132: 345-352.
43. Takada, K., N. Ohno, and T. Yadomae. 1994. Detoxification of lipopolysaccharide (LPS) by egg white lysozyme. FEMS Immunology & Medical Microbiology 9: 255-263.
44. Tomita, M., R. Ohkubo, and M. Hayashi. 2004. Lipopolysaccharide transport system across colonic epithelial cells in normal and infective rat. Drug Metab Pharmacokinet 19: 33-40.
45. Van Gucht, S. et al. 2006. Effect of porcine respiratory coronavirus infection on lipopolysaccharide recognition proteins and haptoglobin levels in the lungs. Microbes Infect 8: 1492-1501.
46. Wang, Q., C. H. Fang, and P.-O. Hasselgren. 2001. Intestinal permeability is reduced and IL-10 levels are increased in septic IL-6 knockout mice. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology 281: R1013-R1023.
47. Webel, D. M., B. N. Finck, D. H. Baker, and R. W. Johnson. 1997. Time course of increased plasma cytokines, cortisol, and urea nitrogen in pigs following intraperitoneal injection of lipopolysaccharide. J. Anim. Sci. 75: 1514-1520.
48. Weber, T. E., and B. J. Kerr. 2008. Effect of sodium butyrate on growth performance and response to lipopolysaccharide in weanling pigs. J. Anim Sci 86: 442-450.
49. Williams, P. N., C. T. Collier, J. A. Carroll, T. H. Welsh, Jr., and J. C. Laurenz. 2009. Temporal pattern and effect of sex on lipopolysaccharide-induced stress hormone and cytokine response in pigs. Domest Anim Endocrinol 37: 139-147.
50. Wright, K. J. et al. 2000. Integrated adrenal, somatotropic, and immune responses of growing pigs to treatment with lipopolysaccharide. J. Anim. Sci. 78: 1892-1899.
51. Young, J. M., W. Cai, and J. C. Dekkers. 2011. Effect of selection for residual feed intake on feeding behavior and daily feed intake patterns in Yorkshire swine. J. Anim Sci 89: 639-647.