Enterocyte proliferation and apoptosis in the caudal small intestine is influenced by the composition of colonizing commensal bacteria in the neonatal gnotobiotic pig

Journal of Animal Science

Volumn 85, Issue 12, 2007, Pages 3256-3266

  Willing, B P ^a   Van Kessel, A G ^a  

^a UNIVERSITY OF SASKATCHEWAN   (Canada)

Author keywords

Commensal bacteria; Enterocyte turnover; Gnotobiotic pig

Indexed keywords

CASPASE; FAS LIGAND; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL; ANIMAL DISEASE; APOPTOSIS; ARTICLE; CELL DIVISION; ERYTHROCYTE; ESCHERICHIA COLI; FECES; GERMFREE ANIMAL; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; LACTOBACILLUS FERMENTUM; METABOLISM; METHODOLOGY; MICROBIOLOGY; PATHOLOGY; PHYSIOLOGY; POLYMERASE CHAIN REACTION; RANDOMIZATION; SIGNAL TRANSDUCTION; SMALL INTESTINE; SWINE;

ANIMALS; APOPTOSIS; CASPASES; CELL DIVISION; ERYTHROCYTES; ESCHERICHIA COLI; FAS LIGAND PROTEIN; FECES; GERM-FREE LIFE; INTESTINE, SMALL; LACTOBACILLUS FERMENTUM; POLYMERASE CHAIN REACTION; RANDOM ALLOCATION; SIGNAL TRANSDUCTION; SWINE; TOLL-LIKE RECEPTORS; TUMOR NECROSIS FACTOR-ALPHA;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; LACTOBACILLUS FERMENTUM; SUIDAE;

EID: 37049028329     PISSN: 00218812     EISSN: None     Source Type: Journal    
DOI: 10.2527/jas.2007-0320     Document Type: Article

References (49)

1. Abrams, G. D., H. Bauer, and H. Sprinz. 1963. Influence of the normal flora on mucosal morphology and cellular renewal in the ileum. A comparison of germ-free and conventional mice. Lab. Invest. 12:355-364.
2. Abreu, M. T., E. T. Arnold, L. S. Thomas, R. Gonsky, Y. Zhou, B. Hu, and M. Arditi. 2002. TLR4 and MD-2 expression is regulated by immune-mediated signals inhuman intestinal epithelial cells. J. Biol. Chem. 277:20431-20437.
3. Aderem, A., and R. J. Ulevitch. 2000. Toll-like receptors in the induction of the innate immune response. Nature 406:782-787.
4. An, H., Y. Yu, M. Zhang, H. Xu, R. Qi, X. Yan, S. Liu, W. Wang, Z. Guo, J. Guo, Z. Qin, and X. Cao. 2002. Involvement of ERK, p38 and NF-κB signal transduction in regulation of TLR2, TLR4 and TLR9 gene expression induced by lipopolysaccharide in mouse dendritic cells. Immunology 106:38-45.
5. Canadian Council on Animal Care. 1993. Guide to the care and use of experimental animals. Volume 1. E. D. Olfert, B. M. Cross, and A. A. McWilliams, ed. CCAC, Ottawa, Ontario, Canada.
6. Coates, M. E. 1973. Gnotobiotic animals in nutrition research. Proc. Nutr. Soc. 32:53-58.
7. Coles, H. S. R., J. F. Burne, and M. C. Raff. 1993. Large-scale normal-cell death in the developing rat kidney and its reduction by epidermal growth factor. Development 118:777-784.
8. Corredor, J., F. Yan, C. C. Shen, W. Tong, S. K. John, G. Wilson, R. Whitehead, and D. B. Polk. 2003. Tumor necrosis factor regulates intestinal epithelial cell migration by receptor-dependent mechanisms. Am. J. Physiol. Cell Physiol. 284:C953-C961.
9. Delneste, Y., A. Donnet-Hughes, and E. J. Schiffrin. 1998. Functional foods: Mechanisms of action on immunocompetent cells. Nutr. Rev. 56:S93-S98.
10. Durkin, E., A. P. Moran, and P. J. Hanson. 2006. Apoptosis induction in gastric mucous cells in vitro: Lesser potency of Helicobacter pylori than Escherichia coli lipopolysaccharide, but positive interaction with ibuprofen. J. Endotoxin Res. 12:47-56.
11. Ellis, J., L. Hassard, E. Clark, J. Harding, G. Allan, P. Willson, J. Strokappe, K. Martin, F. Mcneilly, B. Meehan, D. Todd, and D. Haines. 1998. Isolation of circovirus from lesions of pigs with postweaning multisystemic wasting syndrome. Can. Vet. J. 39:44-51.
12. Embury-Hyatt, C. K., G. Wobeser, E. Simko, and M. R. Woodbury. 2005. Investigation of a syndrome of sudden death, splenomegaly, and small intestinal hemorrhage in farmed deer. Can. Vet. J. 46:702-708.
13. Erickson, K., and N. Hubbard. 2000. Probiotic immunomodulation in health and disease. J. Nutr. 130:403S-409S.
14. Fan, M., B. Stoll, R. Jiang, and D. Burrin. 2001. Enterocyte digestive enzyme activity along the crypt-villus and longitudinal axes in the neonatal pig small intestine. J. Anim. Sci. 79:371-381.
15. Furuse, M., and J. Okumura. 1994. Nutritional and physiological characteristics in germ-free chickens. Comp. Biochem. Physiol. A Physiol. 109:547-556.
16. Galdeano, C. M., and G. Perdigon. 2006. The probiotic bacterium Lactobacillus casei induces activation of the gut mucosal immune system through innate immunity. Clin. Vaccine Immunol. 13:219-226.
17. Haines, D. M., and B. J. Chelack. 1991. Technical considerations for developing enzyme immunohistochemical staining procedures on formalin-fixed paraffin-embedded tissues for diagnostic pathology. J. Vet. Diagn. Invest. 3:101-112.
18. Hall, P. A., P. J. Coates, B. Ansari, and D. Hopwood. 1994. Regulation of cell number in the mammalian gastrointestinal tract: The importance of apoptosis. J. Cell Sci. 107:3569-3577.
19. Hill, J. E., R. P. Seipp, M. Betts, L. Hawkins, A. G. Van Kessel, W. L. Crosby, and S. M. Hemmingsen. 2002. Extensive profiling of a complex microbial community by high-throughput sequencing. Appl. Environ. Microbiol. 68:3055-3066.
20. Hooper, L. V. 2004. Bacterial contributions to mammalian gut development. Trends Microbiol. 12:129-134.
21. Hooper, L. V., M. H. Wong, A. Thelin, L. Hansson, P. G. Falk, and J. I. Gordon. 2001. Molecular analysis of commensal host-microbial relationships in the intestine. Science 291:881-884.
22. Le Floc'h, N., and B. Seve. 2000. Protein and amino acid metabolism in the intestine of the pig: From digestion to appearance in the portal vein. Prod. Anim. 13:303-314.
23. Leschelle, X., V. Robert, S. Delpal, B. Mouille, C. Mayeur, P. Martel, and F. Blachier. 2002. Isolation of pig colonic crypts for cytotoxic assay of luminal compounds: Effects of hydrogen sulfide, ammonia, and deoxycholic acid. Cell Biol. Toxicol. 18:193-203.
24. Mariadason, J. M., C. Nicholas, K. E. L'italien, M. Zhuang, H. J. M. Smartt, B. G. Heerdt, W. C. Yang, G. A. Corner, A. J. Wilson, L. Klampfer, D. Arango, and L. H. Augenlicht. 2005. Gene expression profiling of intestinal epithelial cell maturation along the crypt-villus axis. Gastroenterology 128:1081-1088.
25. Medzhitov, R. 2001. Toll-like receptors and innate immunity. Nat. Rev. Immunol. 1:135-145.
26. Nyachoti, C., C. De Lange, B. Mcbride, S. Leeson, and V. Gabert. 2000. Endogenous gut nitrogen losses in growing pigs are not caused by increased protein synthesis rates in the small intestine. J. Nutr. 130:566-572.
27. Oshikawa, K., and Y. Sugiyama. 2003. Regulation of toll-like receptor 2 and 4 gene expression in murine alveolar macrophages. Exp. Lung Res. 29:401-412.
28. Oswald, I. P. 2006. Role of intestinal epithelial cells in the innate immune defence of the pig intestine. Vet. Res. 37:359-368.
29. Pfaffl, M. W. 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29:e45.
30. Potten, C. S., and M. Loeffler. 1990. Stem-cells: attributes, cycles, spirals, pitfalls and uncertainties. Lessons for and from the crypt. Development 110:1001-1020.
31. Rakoff-Nahoum, S., J. Paglino, F. Eslami-Varzaneh, S. Edberg, and R. Medzhitov. 2004. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118:229-241.
32. Roediger, W., and W. Babidge. 1997. Human colonocyte detoxification. Gut 41:731-734.
33. Rothkotter, H. J., H. Ulrich, and R. Pabst. 1991. The postnatal development of gut lamina propria lymphocytes: Number, proliferation, and T and B cell subsets in conventional and germfree pigs. Pediatr. Res. 29:237-242.
34. Ruemmele, F. M., J. F. Beaulieu, S. Dionne, E. Levy, E. G. Seidman, N. Cerf-Bensussan, and M. J. Lentze. 2002. Lipopolysaccharide modulation of normal enterocyte turnover by toll-like receptors is mediated by enclogenously produced tumour necrosis factor α. Gut 51:842-848.
35. Ruemmele, F., P. Russo, J. Beaulieu, S. Dionne, E. Levy, M. Lentze, and E. Seidman. 1999. Susceptibility to FAS-induced apoptosis in human nontumoral enterocytes: Role of costimulatory factors. J. Cell. Physiol. 181:45-54.
36. Saegusa, S., M. Totsuka, S. Kaminogawa, and T. Hosol. 2004. Candida albicans and Saccharomyces cerevisiae induce interleukin-8 production from intestinal epithelial-like Caco-2 cells in the presence of butyric acid. FEMS Immunol. Med. Microbiol. 41:227-235.
37. Sakata, T. 1987. Stimulatory effect of short-chain fatty acids on epithelial cell proliferation in the rat intestine: A possible explanation for trophic effects of fermentable fibre, gut microbes and luminal trophic factors. Br. J. Nutr. 58:95-103.
38. Savage, D., J. Siegel, J. Snellen, and D. Whitt. 1981. Transit time of epithelial cells in the small intestines of germ-free mice and ex-germfree mice associated with indigenous microorganisms. Appl. Environ. Microbiol. 42:996-1001.
39. Schauser, K., J. Olsen, and L. I. Larsson. 2005. Salmonella Typhimurium infection in the porcine intestine: Evidence for caspase-3-dependent and -independent programmed cell death. Histochem. Cell Biol. 123:43-50.
40. Shirkey, T. W., R. H. Siggers, B. G. Goldade, J. K. Marshall, M. D. Drew, B. Laarveld, and A. G. Van Kessel. 2006. Effects of commensal bacteria on intestinal morphology and expression of proinflammatory cytokines in the gnotobiotic pig. Exp. Biol. Med. 231:1333-1345.
41. Siggers, R. H., J. K. Marshall, T. W. Shirkey, M. D. Drew, B. Laarveld, and A. G. Van Kessel. 2003. Cloning of porcine proglucagon and effect of commensal bacteria on relative expression in intestine of gnotobiotic pigs. Pages 13-15 in Proc. 9th Int. Symp. Digest. Physiol. Pig, Banff, Alberta, Canada. Univ. Alberta, Edmonton, Alberta, Canada.
42. Stappenbeck, T., L. Hooper, and J. Gordon. 2002. Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells. Proc. Natl. Acad. Sci. USA 99:15451-15455.
43. Strater, J., and P. Moller. 2000. Expression and function of death receptors and their natural ligands in the intestine. Epithelial Transp. Barrier Funct. 915:162-170.
44. Suzuki, H., A. Yanaka, T. Shibahara, H. Matsui, A. Nakahara, N. Tanaka, H. Muto, T. Momoi, and Y. Uchiyama. 2002. Ammonia-induced apoptosis is accelerated at higher pH in gastric surface mucous cells. Am. J. Physiol. Gastrointest. Liver Physiol. 283:G986-G995.
45. Tappenden, K. A., D. M. Albin, A. L. Bartholome, and H. F. Mangian. 2003. Glucagon-like peptide-2 and short-chain fatty acids: A new twist to an old story. J. Nutr. 133:3717-3720.
46. Thompson, G., and P. Trexler. 1971. Gastrointestinal structure and function in germ-free or gnotobiotic animals. Gut 12:230-235.
47. Tsukahara, T., H. Koyama, M. Okada, and K. Ushida. 2002. Stimulation of butyrate production by gluconic acid in batch culture of pig cecal digesta and identification of butyrate-producing bacteria. J. Nutr. 132:2229-2234.
48. Vinderola, G., C. Matar, and G. Perdigon. 2005. Role of intestinal epithelial cells in immune effects mediated by gram-positive probiotic bacteria: Involvement of Toll-like receptors. Clin. Diagn. Lab. Immunol. 12:1075-1084.
49. Visek, W. J. 1978. Diet and cell growth modulation by ammonia. Am. J. Clin. Nutr. 31:8216-8220.