Hostname: page-component-7b9c58cd5d-nzzs5 Total loading time: 0 Render date: 2025-03-14T11:15:19.275Z Has data issue: false hasContentIssue false
  • English
  • Français

Commensal microbiome effects on mucosal immune system development in the ruminant gastrointestinal tract

Published online by Cambridge University Press:  04 July 2012

Ryan Taschuk  and
Philip J Griebel
Ryan Taschuk
Affiliation:
Vaccine and Infectious Disease Organization–International Vaccine Center, University of Saskatchewan, 120 Veterinary Road, Saskatoon, SK S7N 5E3Canada School of Public Health, University of Saskatchewan, Saskatoon, SK S7N 5E3Canada
Philip J Griebel*
Affiliation:
Vaccine and Infectious Disease Organization–International Vaccine Center, University of Saskatchewan, 120 Veterinary Road, Saskatoon, SK S7N 5E3Canada School of Public Health, University of Saskatchewan, Saskatoon, SK S7N 5E3Canada
*
*Corresponding author: E-mail: philip.griebel@usask.ca
Get access Rights & Permissions [Opens in a new window]

Abstract

Commensal microflora play many roles within the mammalian gastrointestinal tract (GIT) that benefit host physiology by way of direct or indirect interactions with mucosal surfaces. Commensal flora comprises members across all microbial phyla, although predominantly bacterial, with population dynamics varying with host species, genotype, and environmental factors. Little is known, however, about the complex mechanisms regulating host–commensal interactions that underlie this mutually beneficial relationship and how alterations in the microbiome may influence host development and susceptibility to infection. Research into the gut microbiome has intensified as it becomes increasingly evident that symbiont–host interactions have a significant impact on mucosal immunity and health. Furthermore, evidence that microbial populations vary significantly throughout the GIT suggest that regional differences in the microbiome may also influence immune function within distinct compartments of the GIT. Postpartum colonization of the GIT has been shown to have a direct effect on mucosal immune system development, but information is limited regarding regional effects of the microbiome on the development, activation, and maturation of the mucosal immune system. This review discusses factors influencing the colonization and establishment of the microbiome throughout the GIT of newborn calves and the evidence that regional differences in the microbiome influence mucosal immune system development and maturation. The implications of this complex interaction are also discussed in terms of possible effects on responses to enteric pathogens and vaccines.

Keywords

bovinegut microbiomeinnate immunitymucosal immune systemgeneticsdietecology
Type
Review Article
Information
Animal Health Research Reviews , Volume 13 , Issue 1 , June 2012 , pp. 129 - 141
Copyright
Copyright © Cambridge University Press 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abreu, MT, Vora, P, Faure, E, Thomas, LS, Arnold, ET and Arditi, M (2001). Decreased expression of Toll-like receptor-4 and MD-2 correlates with intestinal epithelial cell protection against dysregulated proinflammatory gene expression in response to bacterial lipopolysaccharide. Journal of Immunology 167: 1609–1616.CrossRefGoogle ScholarPubMed
Abreu, MT, Fukata, M and Arditi, M (2005). TLR signaling in the gut in health and disease. Journal of Immunology 174: 4453–4460.CrossRefGoogle ScholarPubMed
Alitheen, N, McClure, S and McCullagh, P (2003). Development of B cells in the gut-associated lymphoid tissue of mid-gestational fetal lambs. Developmental and Comparative Immunology 27: 639–646.CrossRefGoogle ScholarPubMed
Ata, A, Türütoğlu, H, Kale, M, Gülay, MŞ and Pehlivanoğluet, F (2010). Microbial flora of normal and abnormal cervical mucous discharge associated with reproductive performance of Cows and Heifers in Estrus. Asian-Australian Journal of Animal Sciences 8: 1007–1012.CrossRefGoogle Scholar
Barnes, EM (1979). The intestinal microflora of poultry and game birds during life and after storage. Address of the president of the Society for Applied Bacteriology delivered at a meeting of the society on 10 January 1979. Journal of Applied Bacteriology 46: 407–419.CrossRefGoogle Scholar
Barrington, GM and Parish, SM (2001). Bovine neonatal immunology. Veterinary Clinics of North America: Food Animal Practice 17: 463–476.Google Scholar
Bartley, PM, Kivar, E, Wright, S, Swales, C, Esteban-Redondo, I, Buxton, D, Maley, SW, Schock, A, Rae, AG, Hamilton, C and Innes, EA (2004). Maternal and fetal immune responses of cattle inoculated with neospora caninum at mid-gestation. Journal of Comparative Pathology 130: 81–91.Google Scholar
Benson, AK, Kelly, SA, Legge, R, Ma, F, Low, SJ, Kim, J, Zhang, M, Oh, PL, Nehrenberg, D, Hua, K, Kachman, SD, Moriyama, EN, Walter, J, Peterson, DA and Pompet, D (2010). Individuality in gut microbiota composition is a complex polygenic trait shaped by multiple environmental and host genetic factors. Proceedings of the National Academy of Sciences of the United States of America 107: 18933–18938.Google Scholar
Berge, ACB, Besser, TE, Moore, DA and Sischo, WM (2009). Evaluation of the effects of oral colostrum supplementation during the first fourteen days on the health and performance of preweaned calves. Journal of Dairy Science 92: 286–295.Google Scholar
Bevins, CL and Salzman, NH (2011). Paneth cells, antimicrobial peptides and maintenance of intestinal homeostasis. Nature Reviews Microbiology 9: 356–368.Google Scholar
Beyaz, F and Asti, RN (2004). Development of Ileal Peyer's patches and follicle associated epithelium in bovine foetuses. Anatomia, Histologia, Embryologia 33: 172–179.CrossRefGoogle ScholarPubMed
Björkstén, B, Sepp, E, Julge, K, Voor, T and Mikelsaar, M (2001). Allergy development and the intestinal microflora during the first year of life. Journal of Allergy and Clinical Immunology 108: 516–520.CrossRefGoogle ScholarPubMed
Callaway, TR, Dowd, SE, Edrington, TS, Anderson, RC, Krueger, N, Bauer, N, Kononoff, PJ and Nisbet, DJ (2010). Evaluation of bacterial diversity in the rumen and feces of cattle fed different levels of dried distillers grain plus solubles using bacterial tag-encoded FLX amplicon pyrosequencing. Journal of Animal Science 88: 3977–3983.CrossRefGoogle ScholarPubMed
Casas, E, Garcia, MD, Wells, JE and Smith, TPL (2011). Association of single nucleotide polymorphisms in the ANKRA2 and CD180 genes with bovine respiratory disease and presence of Mycobacterium avium subsp. paratuberculosis. Animal Genetics 42: 571–577.CrossRefGoogle ScholarPubMed
Cerovic, V, Jenkins, CD, Barnes, AGC, Milling, SWF, MacPherson, GG and Klavinskis, LS (2009). Hyporesponsiveness of intestinal dendritic cells to TLR stimulation is limited to TLR4. Journal of Immunology 182: 2405–2415.Google Scholar
Charavaryamath, C, Fries, P, Gomis, S, Bell, C, Doig, K, Guan, LL, Potter, A, Napper, S and Griebel, PJ (2011). Mucosal changes in a long-term bovine intestinal segment model following removal of ingesta and microflora. Gut Microbes 2: 134–144.Google Scholar
Charleston, B, Fray, MD, Baignet, S, Carr, BV and Morrison, WI (2001). Establishment of persistent infection with non-cytopathic bovine viral diarrhoea virus in cattle is associated with a failure to induce type I interferon. Journal of General Virology 82: 1893–1897.CrossRefGoogle ScholarPubMed
Chase, CCL, Hurley, DJ and Reber, AJ (2008). Neonatal immune development in the calf and its impact on vaccine response. Veterinary Clinics of North America: Food Animal Practice 24: 87–104.Google Scholar
Dominguez-Bello, MG, Blaser, MJ, Ley, RE and Knight, RE (2011). Development of the human gastrointestinal microbiota and insights from high-throughput sequencing. Gastroenterology 140: 1713–1719.CrossRefGoogle ScholarPubMed
Eckburg, PB, Bik, EM, Bernstein, CN, Purdom, E, Dethlefsen, L, Sargent, M, Gill, SR, Nelson, KE and Relman, DA (2005). Diversity of the human intestinal microbial flora. Science 308: 1635–1638.CrossRefGoogle ScholarPubMed
Ewaschuk, JB, Diaz, H, Meddings, L, Diederichs, B, Dmytrash, A, Backer, J, Looijer-van Langen, M and Madsen, KL (2008). Secreted bioactive factors from Bifidobacterium infantis enhance epithelial cell barrier function. American Journal of Physiology: Gastrointestinal and Liver Physiology 295: G1025–G1034.Google ScholarPubMed
Falk, PG, Hooper, LV, Midtvedt, T and Gordon, JI (1998). Creating and maintaining the gastrointestinal ecosystem: what we know and need to know from gnotobiology. Microbiology and Molecular Biology Reviews 62: 1157–1170.Google Scholar
Flint, HJ and Bayer, EA (2008). Plant cell wall breakdown by anaerobic microorganisms from the mammalian digestive tract. Annals of the New York Academy of Sciences 1125: 280–288.CrossRefGoogle ScholarPubMed
Foote, MR, Nonnecke, BJ, Fowler, MA, Miller, BL, Beitz, DC and Waters, WR (2005). Effects of age and nutrition on expression of CD25, CD44, and L-selectin (CD62L) on T-cells from neonatal calves. Journal of Dairy Science 88: 2718–2729.CrossRefGoogle ScholarPubMed
Fraune, S and Bosch, TCG (2007). Long-term maintenance of species-specific bacterial microbiota in the basal metazoan Hydra. Proceedings of the National Academy of Sciences of the United States of America 104: 13146–13151.CrossRefGoogle ScholarPubMed
Fries, PN, Popowych, YI, Guan, LL, Griebel, PJ (2011). Age-related changes in the distribution and frequency of myeloid and T cell populations in the small intestine of calves. Cellular Immunology 271: 428–437.Google Scholar
Gerdts, V, Uwiera, RR, Mutwiri, GK, Wilson, DJ, Bowersock, T, Kidane, A, Babiuk, LA and Griebel, PJ (2001). Multiple intestinal ‘loops’ provide an in vivo model to analyse multiple mucosal immune responses. Journal of Immunological Methods 256: 19–33.Google Scholar
Gong, J, Si, W, Forster, RJ, Huang, R, Yu, H, Yin, Y, Yang, C and Han, Y (2007). 16S rRNA gene-based analysis of mucosa-associated bacterial community and phylogeny in the chicken gastrointestinal tracts: from crops to ceca. FEMS Microbiology Ecology 59: 147–157.CrossRefGoogle ScholarPubMed
Greenblum, S, Turnbaugh, PJ and Borenstein, E (2012). Metagenomic systems biology of the human gut microbiome reveals topological shifts associated with obesity and inflammatory bowel disease. Proceedings of the National Academy of Sciences of the United States of America 109: 594–599.Google Scholar
Griebel, PJ and Hein, WR (1996). Expanding the role of Peyer's patches in B-cell ontogeny. Immunology Today 17: 30–39.Google Scholar
Griebel, PJ, Kennedy, L, Graham, T, Davis, WC and Reynolds, JD (1992). Characterization of B-cell phenotypic changes during ileal and jejunal Peyer's patch development in sheep. Immunology 77: 564.Google Scholar
Hansen, J, Gulati, A and Sartor, RB (2010). The role of mucosal immunity and host genetics in defining intestinal commensal bacteria. Current Opinion in Gastroenterology 26: 564–571.CrossRefGoogle ScholarPubMed
Harmsen, HJ, Wildeboer-Veloo, AC, Raangs, GC, Wagendorp, AA, Klijn, N, Bindels, JG and Welling, GW (2000). Analysis of intestinal flora development in breast-fed and formula-fed infants by using molecular identification and detection methods. Journal of Pediatric Gastroenterology and Nutrition 30: 61–67.Google Scholar
Hartman, AL, Lough, DM, Barupal, DK, Fiehn, O, Fishbein, T, Zasloff, M and Eisen, JA (2009). Human gut microbiome adopts an alternative state following small bowel transplantation. Proceedings of the National Academy of Sciences of the United States of America 106: 17187–17192.CrossRefGoogle ScholarPubMed
Hill, DA, Hoffmann, C, Abt, MC, Du, Y, Kobuley, D, Kirn, TJ, Bushman, FD and Artis, D (2009). Metagenomic analyses reveal antibiotic-induced temporal and spatial changes in intestinal microbiota with associated alterations in immune cell homeostasis. Mucosal Immunology 3: 148–158.Google Scholar
Hill, K, Hunsaker, B, Townsend, H, Van den Hurk, S and Griebel, PJ. (2012). Mucosal immune response of newborn Holstein calves following intransal immunization with a modified-live, multivalent viral vaccine in the face of maternal antibody. Journal of the American Veterinary Medical Association 240: 1231–1240.Google Scholar
Isolauri, E, Majamaa, H, Arvola, T, Rantala, I, Virtanen, E and Arvilommi, H (1993). Lactobacillus casei strain GG reverses increased intestinal permeability induced by cow milk in suckling rats. Gastroenterology 105: 1643–1650.Google Scholar
Iwasaki, A and Medzhitov, R (2004). Toll-like receptor control of the adaptive immune responses. Nature Immunology 5: 987–995.Google Scholar
Jacobs, AA, Bergman, JG, Theelen, RP, Jaspers, R, Helps, JM, Horspool, LJ and Paul, G (2007). Compatibility of a bivalent modified-live vaccine against Bordetella bronchiseptica and CPiV, and a trivalent modified-live vaccine against CPV, CDV and CAV-2. Veterinary Record 160: 41–45.CrossRefGoogle Scholar
Jain, L, Vidyasagar, D, Xanthou, M, Ghai, V, Shimada, S and Blend, M (1989). In vivo distribution of human milk leucocytes after ingestion by newborn baboons. Archives of Disease in Childhood 64: 930–933.Google Scholar
Jami, E and Mizrahi, I (2012). Composition and similarity of bovine rumen microbiota across individual animals. PLoS ONE 7: e33306.Google Scholar
Jensen, J, Rubino, M, Yang, WC, Cooley, AJ and Schultz, RD (1988). Ontogeny of mitogen responsive lymphocytes in the bovine fetus. Developmental and Comparative Immunology 12: 685–692.Google Scholar
Jeyanathan, J, Kirs, M, Ronimus, RS, Hoskin, SO and Janssen, PH (2011). Methanogen community structure in the rumens of farmed sheep, cattle and red deer fed different diets. FEMS Microbiology Ecology 76: 311–326.CrossRefGoogle Scholar
Jochims, K, Kaup, FJ, Drommer, W and Pickel, M (1994). An immunoelectron microscopic investigation of colostral IgG absorption across the intestine of newborn calves. Research in Veterinary Science 57: 75–80.CrossRefGoogle ScholarPubMed
Johnston, NE, Estrella, RA & Oxender, WD (1977). Resistance of neonatal calves given colostrum diet to oral challenge with a septicemia-producing Escherichia coli. American Journal of Veterinary Research 38: 1323–1326.Google ScholarPubMed
Karlsson, J, Pütsep, K, Chu, H, Kays, RJ, Bevins, CL and Andersson, M (2008). Regional variations in Paneth cell antimicrobial peptide expression along the mouse intestinal tract. BMC Immunology 9: 37.CrossRefGoogle ScholarPubMed
Kehoe, SI (2006). Colostrum components and their impact on digestive function and growth of dairy calves. Ph.D Thesis, Pennsylvania State University, USA.Google Scholar
Komatsu, M, Fujimori, Y, Sato, Y, Okamura, H, Sasaki, S, Itoh, T, Morita, M, Nakamura, R, Oe, T, Furuta, M, Yasuda, J, Kojima, T, Watanabe, T, Hayashi, T, Malau-Aduli, AEO and Takahashi, H (2010). Nucleotide polymorphisms and the 5′-UTR transcriptional analysis of the bovine growth hormone secretagogue receptor 1a (GHSR1a) gene. Animal Science Journal 81: 530–550.Google Scholar
Kovacs, A, Ben-Jacob, N, Tayem, H, Halperin, E, Iraqi, FA and Gophna, U (2011). Genotype is a stronger determinant than sex of the mouse gut microbiota. Microbial Ecology 61: 423–428.Google Scholar
Kreikemeier, KK, Harmon, DL, Peters, JP, Gross, KL, Armendariz, CK and Krehbiel, CR (1990). Influence of dietary forage and feed intake on carbohydrase activities and small intestinal morphology of calves. Journal of Animal Science 68: 2916–2929.Google Scholar
Krug, A, Rothenfusser, S, Hornung, V, Jahrsdörfer, B, Blackwell, S, Ballas, ZK, Endres, S, Krieg, AM and Hartmann, G (2001). Identification of CpG oligonucleotide sequences with high induction of IFN-alpha/beta in plasmacytoid dendritic cells. European Journal of Immunology 31: 2154–2163.Google Scholar
Kunz, C and Rudloff, S (2008). Potential anti-inflammatory and anti-infectious effects of human milk oligosaccharides. Advances in Experimental Medicine and Biology 606: 455–465.Google Scholar
Leach, RJ, O'Neill, RG, Fitzpatrick, JL, Williams, JL and Glass, EJ (2012). Quantitative trait loci associated with the immune response to a bovine respiratory syncytial virus vaccine. PLoS ONE 7: e33526.Google Scholar
Lee, A (1985). Neglected niches: the microbial ecology of the gastrointestinal tract. Advances in Microbial Ecology 8: 115–162.Google Scholar
Lejeune, A, Monahan, FJ, Moloney, AP, Earley, B, Black, AD, Campion, DP, Englishby, T, Reilly, P, O'Doherty, J and Sweeney, T (2010). Peripheral and gastrointestinal immune systems of healthy cattle raised outdoors at pasture or indoors on a concentrate-based ration. BMC Veterinary Research 6: 19.Google Scholar
Lev, M and Briggs, CAE (1956). The gut flora of the chick. II. The establishment of the flora. Journal of Applied Microbiology 19: 224–230.Google Scholar
Ley, RE, Bäckhed, F, Turnbaugh, P, Lozupone, CA, Knight, RD and Gordon, JI (2005). Obesity alters gut microbial ecology. Proceedings of the National Academy of Sciences of the United States of America 102: 11070–11075.Google Scholar
Liebler-Tenorio, EM, Riedel-Caspari, G and Pohlenz, JF (2002). Uptake of colostral leukocytes in the intestinal tract of newborn calves. Veterinary Immunology and Immunopathology 85: 33–40.Google Scholar
Lindner, JDD, Santarelli, M, Yamaguishi, CT, Soccol, CR and Neviani, E (2011). Recovery and identification of bovine colostrum microflora using traditional and molecular approaches. Food Technology and Biotechnology 49: 364–368.Google Scholar
Loh, G, Brodziak, F and Blaut, M (2008). The Toll-like receptors TLR2 and TLR4 do not affect the intestinal microbiota composition in mice. Environmental Microbiology 10: 709–715.Google Scholar
Macpherson, AJ, Geuking, MB, Slack, E, Hapfelmeier, S and McCoy, KD (2012). The habitat, double life, citizenship, and forgetfulness of IgA. Immunological Reviews 245: 132–46.CrossRefGoogle ScholarPubMed
Majamaa, H and Isolauri, E (1997). Probiotics: a novel approach in the management of food allergy. Journal of Allergy and Clinical Immunology 99: 179–185.CrossRefGoogle ScholarPubMed
Malmuthuge, N, Li, M, Chen, Y, Fries, PN, Griebel, PJ, Baurhoo, B, Zhao, X and Guan, LL (2011). Distinct commensal bacteria associated with ingesta and mucosal epithelium in the gastrointestinal tracts of calves and chickens. FEMS Microbiology Ecology 79: 337–347.Google Scholar
Malmuthuge, N, Li, M, Fries, PN, Griebel, PJ and Guan, LL (2012). Regional and age dependent changes in gene expression of Toll-like receptors and key antimicrobial defence molecules throughout the gastrointestinal tract of dairy calves. Veterinary Immunology and Immunopathology 146: 18–26.Google Scholar
Maltecca, C, Weigel, K, Khatib, H, Cowan, M and Bagnato, A (2009). Whole-genome scan for quantitative trait loci associated with birth weight, gestation length and passive immune transfer in a Holstein×Jersey crossbred population. Animal Genetics 40: 27–34.CrossRefGoogle Scholar
McGuire, K, Jones, M, Werling, D, Williams, JL, Glass, EJ and Jann, O (2006). Radiation hybrid mapping of all 10 characterized bovine Toll-like receptors. Animal Genetics 37: 47–50.Google Scholar
Mutwiri, G, Watts, T, Lew, L, Beskorwayne, T, Papp, Z, Baca-Estrada, ME and Griebel, P (1999). Ileal and jejunal Peyer's patches play distinct roles in mucosal immunity of sheep. Immunology 97: 455–461.CrossRefGoogle ScholarPubMed
Mutwiri, G, Bateman, C, Baca-Estrada, ME, Snider, M and Griebel, PJ (2000). Induction of immune responses in newborn lambs following enteric immunization with a human adenovirus vaccine vector. Vaccine 19: 1284–1293.Google Scholar
Nava, GM, Friedrichsen, HJ and Stappenbeck, TS (2011). Spatial organization of intestinal microbiota in the mouse ascending colon. ISME Journal 5: 627–638.CrossRefGoogle ScholarPubMed
Nava, GM, Carbonero, F, Croix, JA, Greenberg, E and Gaskins, HR (2012). Abundance and diversity of mucosa-associated hydrogenotrophic microbes in the healthy human colon. IMSE Journal 6: 57–70.Google Scholar
NIH HMP Working Group (2009). The NIH human microbiome project. Genome Research 19: 2317–2323.Google Scholar
Otte, J, Cario, E and Podolsky, DK (2004). Mechanisms of cross hyporesponsiveness to Toll-like receptor bacterial ligands in intestinal epithelial cells. Gastroenterology 126: 1054–1070.Google Scholar
Pakkanen, R and Aalto, J (1997). Growth factors and antimicrobial factors of bovine colostrum. International Dairy Journal 7: 285–297.Google Scholar
Pitta, DW, Pinchak, WE, Dowd, SE, Osterstock, J, Gontcharova, V, Youn, E, Dorton, K, Yoon, I, Min, BR, Fulford, JD, Wickersham, TA and Malinowski, DP (2010). Rumen bacterial diversity dynamics associated with changing from bermudagrass hay to grazed winter wheat diets. Microbial Ecology 59: 511–522.CrossRefGoogle ScholarPubMed
Poroyko, V, White, JR, Wang, M, Donovan, S, Alverdy, J, Liu, DC and Morowitz, MJ (2010). Gut microbial gene expression in mother-fed and formula-fed piglets. PLoS ONE 5: e12459.CrossRefGoogle ScholarPubMed
Possemiers, S, Bolca, S, Verstraete, W and Heyerick, A (2011). The intestinal microbiome: a separate organ inside the body with the metabolic potential to influence the bioactivity of botanicals. Fitoterapia 82: 53–66.Google Scholar
Rakoff-Nahoum, S, Paglino, J, Eslami-Varzaneh, F, Edberg, S and Medzhitov, R (2004). Recognition of commensal microflora by Toll-like receptors is required for intestinal homeostasis. Cell 118: 229–241.CrossRefGoogle ScholarPubMed
Ramsburg, E, Tigelaar, R, Craft, J and Hayday, A (2003). Age-dependent requirement for γδ T cells in the primary but not secondary protective immune response against an intestinal parasite. Journal of Experimental Medicine 198: 1403–1414.Google Scholar
Reynolds, JD and Morris, B (1984). The effect of antigen on the development of Peyer's patches in sheep. European Journal of Immunology 14: 1–6.Google Scholar
Rothkötter, HJ and Pabst, R (1989). Lymphocyte subsets in jejunal and ileal Peyer's patches of normal and gnotobiotic minipigs. Immunology 67: 103–108.Google Scholar
Round, JL and Mazmanian, SK (2010). Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proceedings of the National Academy of Sciences of the United States of America 107: 12204–12209.Google Scholar
Salzman, N, de Jong, H, Paterson, Y, Harmsen, HJM, Welling, GW and Bos, NA (2002). Analysis of 16S libraries of mouse gastrointestinal microflora reveals a large new group of mouse intestinal bacteria. Microbiology 148: 3651–3660.Google Scholar
Sansonetti, PJ (2006). The innate signaling of dangers and the dangers of innate signaling. Nature Immunology 7: 1237–1242.Google Scholar
Sansonetti, PJ (2010). To be or not to be a pathogen: that is the mucosally relevant question. Mucosal immunology 4: 8–14.Google Scholar
Schultz, RD, Dunne, HW and Heist, CE (1973). Ontogeny of the bovine immune response. Infection and Immunity 7: 981–991.Google Scholar
Schwartz, S, Friedberg, I, Ivanov, IV, Davidson, LA, Goldsby, JS, Dahl, DB, Herman, D, Wang, M, Donovan, SM and Chapkin, R (2012). A metagenomic study of diet-dependent interaction between gut microbiota and host in infants reveals differences in immune response. Genome Biology 13: pR32.Google Scholar
Spor, A, Koren, O and Ley, R (2011). Unravelling the effects of the environment and host genotype on the gut microbiome. Nature Reviews Microbiology 9: 279–290.CrossRefGoogle ScholarPubMed
Stappenbeck, TS, Hooper, LV and Gordon, JI (2002). Developmental regulation of intestinal angiogenesis by indigenous microbes via Paneth cells. Proceedings of the National Academy of Sciences of the United States of America 99: 15451–15455.Google Scholar
Stelwagen, K, Carpenter, E, Haigh, B, Hodgkinson, A and Wheeler, TT (2009). Immune components of bovine colostrum and milk. Journal of Animal Science 87: 3–9.Google Scholar
Stott, GH, Marx, DB, Menefee, BE and Nightengale, GT (1979). Colostral immunoglobulin transfer in calves I. Period of absorption. Journal of Dairy Science 62: 1632–1638.Google Scholar
Sun, C-M, Hall, JA, Blank, RB, Bouladoux, N, Oukka, M, Mora, JR and Belkaid, Y (2007). Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid. Journal of Experimental Medicine 204: 1775–1785.Google Scholar
Tanikawa, T, Shoji, N, Sonohara, N, Saito, S, Shimura, Y, Fukushima, J and Inamoto, T (2011). Aging transition of the bacterial community structure in the chick ceca. Poultry Science 90: 1004–1008.CrossRefGoogle ScholarPubMed
Tannock, GW (2005). New perceptions of the gut microbiota: implications for future research. Gastroenterology Clinics of North America 34: 361–382.Google Scholar
Thurnheer, MC, Zuercher, AW, Cebra, JJ and Bos, NA (2003). B1 cells contribute to serum IgM, but not to intestinal IgA, production in gnotobiotic Ig allotype chimeric mice. Journal of Immunology 170: 4564–4571.Google Scholar
Turnbaugh, PJ and Gordon, JI (2009). The core gut microbiome, energy balance and obesity. Journal of Physiology 587: 4153–4158.Google Scholar
Turnbaugh, PJ, Hamady, M, Yatsunenko, T, Cantarel, BL, Duncan, A, Ley, RE, Sogin, ML, Jones, WJ, Roe, BA, Affourtit, JP, Egholm, M, Henrissat, B, Heath, AC, Knight, R and Gordon, JI (2008). A core gut microbiome in obese and lean twins. Nature 457: 480–484.Google Scholar
Turnbaugh, PJ, Ridaura, VK, Faith, JJ, Rey, FE, Knight, R and Gordon, JI (2009). The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Science Translational Medicine 1: 6ra14.Google Scholar
Van Der Waaij, LA, Harmsen, HJM, Madjipour, M, Kroese, FGM, Zwiers, M, van Dullemen, HM, de Boer, NK, Welling, GW and Jansen, PLM (2005). Bacterial population analysis of human colon and terminal ileum biopsies with 16S rRNA-based fluorescent probes: Commensal bacteria live in suspension and have no direct contact with epithelial cells. Inflammatory Bowel Disease 11: 865–871.Google Scholar
Van Immerseel, F, De Buck, J, De Smet, I, Mast, J, Haesebrouck, F, Ducatelle, R (2002). The effect of vaccination with a Salmonella enteritidis aroA mutant on early cellular responses in caecal lamina propria of newly-hatched chickens. Vaccine 20: 3034–41.Google Scholar
Veenbergen, S and Samsom, JN (2012). Maintenance of small intestinal and colonic tolerance by IL-10-producing regulatory T cell subsets. Current Opinion in Immunology in press, http://dx.doi.org/10.1016/j.coi.2012.03.004.Google Scholar
Vlková, E, Trojanová, I and Rada, V (2006). Distribution of bifidobacteria in the gastrointestinal tract of calves. Folia Microbiologica 51: 325–328.Google Scholar
Walter, J and Ley, R (2011). The human gut microbiome: ecology and recent evolutionary changes. Annual Review of Microbiology 65: 41–129.Google Scholar
Wilson, RA, Zolnai, A, Rudas, P and Frenyo, LV (1996). T-cell subsets in blood and lymphoid tissues obtained from fetal calves, maturing calves, and adult bovine. Veterinary Immunology and Immunopathology 53: 49–60.CrossRefGoogle ScholarPubMed
Wlodarska, M and Finlay, BB (2010). Host immune response to antibiotic perturbation of the microbiota. Mucosal Immunology 3: 100–103.CrossRefGoogle ScholarPubMed
Wyatt, CR, Brackett, EJ, Perryman, LE and Davis, WC (1996). Identification of γδT lymphocyte subsets that populate calf ileal mucosa after birth. Veterinary Immunology and Immunopathology 52: 91–103.CrossRefGoogle Scholar
Wyatt, CR, Brackett, EJ, Perryman, LE, Rice-Ficht, AC, Brown, WC and O'Rourke, KI (1997). Activation of intestinal intraepithelial T lymphocytes in calves infected with Cryptosporidium parvum. Infection and Immunity 65: 185–190.CrossRefGoogle ScholarPubMed
Wyatt, RG, Kapikian, AZ and Mebus, CA (1983). Induction of cross-reactive serum neutralizing antibody to human rotavirus in calves after in utero administration of bovine rotavirus. Journal of Clinical Microbiology 18: 505–508.Google Scholar
Yasuda, M, Jenne, CN, Kennedy, LJ and Reynolds, JD (2006). The sheep and cattle Peyer's patch as a site of B-cell development. Veterinary Research 37: 401–415.Google Scholar
Zambrano-Nava, S, Boscán-Ocando, J and Nava, J (2011). Normal bacterial flora from vaginas of Criollo Limonero cows. Tropical Animal Health and Production 43: 291–294.Google Scholar
Zhou, M, Griebel, PJ and Guan, LL. Prevalence of methanogens in gastrointestinal tract of pre-weaned dairy calves may suggest new direction for methane mitigation and novel concept of their roles in ruminants. FEMS Microbiology Ecology (submitted).Google Scholar
Zimmermann, S, Wagner, C, Müller, W, Brenner-Weiss, G, Hug, F, Prior, B, Obst, U and Hänsch, GM (2006). Induction of neutrophil chemotaxis by the quorum-sensing molecule N-(3-Oxododecanoyl)-l-homoserine lactone. Infection and Immunity 74: 5687–5692.Google Scholar
Zoetendal, EG, Akkermans, ADL, Akkermans-van Vliet, WM, de Visser, JAGM and de Vos, WM (2001). The host genotype affects the bacterial community in the human gastronintestinal tract. Microbial Ecology in Health and Disease 13: 129–134.Google Scholar