The altered schaedler flora: Continued applications of a defined murine microbial community

ILAR Journal

Volumn 56, Issue 2, 2015, Pages 169-178

  Brand, Meghan Wymore ^a   Wannemuehler, Michael J ^a   Phillips, Gregory J ^a   Proctor, Alexandra ^a   Overstreet, Anne Marie ^b   Jergens, Albert E ^a   Orcutt, Roger P ^c   Fox, James G ^d  

^a IOWA STATE UNIVERSITY   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Biomedical Research Associates   (United States)

^d USA   (United States)

Author keywords

ASF; Gnotobiotic; Microbiota

Indexed keywords

ANIMAL; BACTERIUM; GENETICS; GERMFREE ANIMAL; HUMAN; INTESTINE FLORA; METABOLISM; MOUSE; PHYSIOLOGY;

ANIMALS; BACTERIA; GASTROINTESTINAL MICROBIOME; GERM-FREE LIFE; HUMANS; MICE;

EID: 84941771586     PISSN: 10842020     EISSN: 19306180     Source Type: Journal    
DOI: 10.1093/ilar/ilv012     Document Type: Article

References (63)

1. Alexander AD, Orcutt RP, Henry JC, Baker J Jr., Bissahoyo AC, Threadgill DW. 2006. Quantitative PCR assays for mouse enteric flora reveal strain-dependent differences in composition that are influenced by the microenvironment. Mamm Genome 17:1093-1104.
2. Baker DE. 1966. The commercial production of mice with a spec-ified flora. Natl Cancer Inst Monogr 20:161-166.
3. Bauer H, Horowitz RE, Levenson SM, Popper H. 1963. The response of the lymphatic tissue to the microbial flora. Studies on germfree mice. Am J Pathol 42:471-483.
4. Berry D, Stecher B, Schintlmeister A, Reichert J, Brugiroux S, WildB, Wanek W, RichterA, Rauch I, Decker T, LoyA, Wagner M. 2013. Host-compound foraging by intestinal microbiota revealed by single-cell stable isotope probing. Proc Natl Acad Sci USA 110:4720-4725.
5. Cahill RJ, Foltz CJ, Fox JG, Dangler CA, Powrie F, Schauer DB. 1997. Inflammatory bowel disease: an immunity-mediated condition triggered by bacterial infection with Helicobacter hepaticus. Infect Immun 65:3126-3131.
6. Collins J, Borojevic R, Verdu EF, Huizinga JD, Ratcliffe EM. 2014. Intestinal microbiota influence the early postnatal development of the enteric nervous system. Neurogastroenterol Motil 26:98-107.
7. Cong Y, Feng T, Fujihashi K, Schoeb TR, Elson CO. 2009. A dominant, coordinated T regulatory cell-IgA response to the intestinal microbiota. Proc Natl Acad Sci USA 106:19256-19261.
8. Dethlefsen L, McFall-Ngai M, Relman DA. 2007. An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature 449:811-818.
9. Dewhirst FE, Chien CC, Paster BJ, Ericson RL, Orcutt RP, Schauer DB, Fox JG. 1999. Phylogeny of the defined murine microbiota: altered Schaedler flora. Appl Environ Microbiol 65:3287-3292.
10. Doolittle DJ, Sherrill JM, Butterworth BE. 1983. Influence of intestinal bacteria, sex of the animal, and position of the nitro group on the hepatic genotoxicity of nitrotoluene isomers in vivo. Cancer Res 43:2836-2842.
11. Dubos R, Schaedler RW, Costello R, Hoet P. 1965. Indigenous, normal, and autochthonous flora of the gastrointestinal tract. J Exp Med 122:67-76.
12. Dubos RJ, Schaedler RW. 1962. The effect of diet on the fecal bacterial flora of mice and on their resistance to infection. J Exp Med 115:1161-1172.
13. Duca FA, Sakar Y, Lepage P, Devime F, Langelier B, Dore J, Covasa M. 2014. Replication of obesity and associated signaling pathways through transfer of microbiota from obese-prone rats. Diabetes 63:1624-1636.
14. Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, Gill SR, Nelson KE, Relman DA. 2005. Diversity of the human intestinal microbial flora. Science 308:1635-1638.
15. Faith JJ, Guruge JL, Charbonneau M, Subramanian S, Seedorf H, Goodman AL, Clemente JC, Knight R, Heath AC, Leibel RL, Rosenbaum M, Gordon JI. 2013. The long-term stability of the human gut microbiota. Science 341:1237439.
16. Feng T, Wang L, Schoeb TR, Elson CO, Cong Y. 2010. Microbiota innate stimulation is a prerequisite for T cell spontaneous proliferation and induction of experimental colitis. J Exp Med 207:1321-1332.
17. Ge Z, Feng Y, Taylor NS, Ohtani M, Polz MF, Schauer DB, Fox JG. 2006. Colonization dynamics of altered Schaedler flora is in-fluenced by gender, aging, and Helicobacter hepaticus infection in the intestines of Swiss Webster mice. Appl Environ Microbiol 72:5100-5103.
18. Geuking MB, Cahenzli J, Lawson MA, Ng DC, Slack E, Hapfelmeier S, McCoy KD, Macpherson AJ. 2011. Intestinal bacterial colonization induces mutualistic regulatory T cell responses. Immunity 34:794-806.
19. Hapfelmeier S, Lawson MA, SlackE, Kirundi JK, Stoel M, Heikenwalder M, Cahenzli J, Velykoredko Y, Balmer ML, Endt K, Geuking MB, Curtiss R 3rd, McCoy KD, Macpherson AJ. 2010. Reversible microbial colonization of germ-free mice reveals the dynamics of IgA immune responses. Science 328:1705-1709.
20. Horowitz RE, Bauer H, Paronetto F, Abrams GD, Watkins KC, Popper H. 1964. The response of the lymphatic tissue to bacterial antigen. Studies in germfree mice. Am J Pathol 44:747-761.
21. Ivanov II, Frutos Rde L, Manel N, Yoshinaga K, Rifkin DB, Sartor RB, Finlay BB, Littman DR. 2008. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 4:337-349.
22. Jergens AE, Dorn A, Wilson J, Dingbaum K, Henderson A, Liu Z, Hostetter J, Evans RB, Wannemuehler MJ. 2006. Induction of differential immune reactivity to members of the flora of gnotobiotic mice following colonization with Helicobacter bilis or Brachyspira hyodysenteriae. Microbes Infect 8:1602-1610.
23. Jergens AE, Wilson-Welder JH, Dorn A, Henderson A, Liu Z, Evans RB, Hostetter J, Wannemuehler MJ. 2007. Helicobacter bilis triggers persistent immune reactivity to antigens derived from the commensal bacteria in gnotobiotic C3H/HeN mice. Gut 56:934-940.
24. Jostins L, Ripke S, Weersma RK, Duerr RH, McGovern DP, Hui KY, Lee JC, Schumm LP, Sharma Y, Anderson CA, Essers J, Mitrovic M, Ning K, Cleynen I, Theatre E, Spain SL, Raychaudhuri S, Goyette P, Wei Z, Abraham C, Achkar JP, Ahmad T, Amininejad L, Ananthakrishnan AN, Andersen V, Andrews JM, Baidoo L, Balschun T, Bampton PA, Bitton A, Boucher G, Brand S, Buning C, Cohain A, Cichon S, D'Amato M, De Jong D, Devaney KL, Dubinsky M, Edwards C, Ellinghaus D, Ferguson LR, Franchimont D, Fransen K, Gearry R, Georges M, Gieger C, Glas J, Haritunians T, Hart A, Hawkey C, Hedl M, Hu X, Karlsen TH, Kupcinskas L, Kugathasan S, Latiano A, Laukens D, Lawrance IC, Lees CW, LouisE, Mahy G, Mansfield J, Morgan AR, Mowat C, Newman W, Palmieri O, Ponsioen CY, Potocnik U, Prescott NJ, Regueiro M, Rotter JI, Russell RK, Sanderson JD, Sans M, Satsangi J, Schreiber S, Simms LA, Sventoraityte J, Targan SR, Taylor KD, Tremelling M, Verspaget HW, De Vos M, Wijmenga C, Wilson DC, Winkelmann J, Xavier RJ, Zeissig S, Zhang B, Zhang CK, Zhao H, Silverberg MS, Annese V, Hakonarson H, Brant SR, Radford-Smith G, Mathew CG, Rioux JD, Schadt EE, Daly MJ, Franke A, Parkes M, Vermeire S, Barrett JC, Cho JH. 2012. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature 491:119-124.
25. Kuhn R, Lohler J, Rennick D, Rajewsky K, Muller W. 1993. Interleukin-10-deficient mice develop chronic enterocolitis. Cell 75:263-274.
26. Laycock G, Sait L, Inman C, Lewis M, Smidt H, van Diemen P, Jorgensen F, Stevens M, Bailey M. 2012. A defined intestinal colonization microbiota for gnotobiotic pigs. Vet Immunol Immunopathol 149(3-4):216-224.
27. Lertpiriyapong K, Whary MT, Muthupalani S, Lofgren JL, Gamazon ER, Feng Y, Ge Z, Wang TC, Fox JG. 2014. Gastric colonisation with a restricted commensal microbiota replicates the promotion of neoplastic lesions by diverse intestinal microbiota in the Helicobacter pylori INS-GAS mouse model of gastric carcinogenesis. Gut 63:54-63.
28. Lesher S, Walburg HE Jr., Sacher GA Jr. 1964. Generation cycle in the duodenal crypt cells of germ-free and conventional mice. Nature 202:884-886.
29. Ley RE, Peterson DA, Gordon JI. 2006. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell 124:837-848.
30. Liu Z, Henderson AL, Nettleton D, Wilson-Welder JH, Hostetter JM, Ramer-Tait A, Jergens AE, Wannemuehler MJ. 2009. Mucosal gene expression profiles following the colonization of immunocompetent defined-flora C3H mice with Helicobacter bilis: a prelude to typhlocolitis. Microbes Infect 11:374-383.
31. Liu Z, Ramer-Tait AE, Henderson AL, Demirkale CY, Nettleton D, Wang C, Hostetter JM, Jergens AE, Wannemuehler MJ. 2011. Helicobacter bilis colonization enhances susceptibility to typhlocolitis following an inflammatory trigger. Dig Dis Sci 56:2838-2848.
32. Luckey TD. 1972. Introduction to intestinal microecology. Am J Clin Nutr 25:1292-1294.
33. McCafferty J, Muhlbauer M, Gharaibeh RZ, Arthur JC, Perez-Chanona E, Sha W, Jobin C, Fodor AA. 2013. Stochastic changes over time and not founder effects drive cage effects in microbial community assembly in a mouse model. Isme J 7:2116-2125.
34. Momose Y, Park SH, Miyamoto Y, Itoh K. 2011. Design of species-specific oligonucleotide probes for the detection of Bacteroides and Parabacteroides by fluorescence in situ hybridization and their application to the analysis of mouse caecal BacteroidesParabacteroides microbiota. J Appl Microbiol 111:176-184.
35. Mosconi I, Geuking MB, Zaiss MM, Massacand JC, Aschwanden C, Kwong Chung CK, McCoy KD, Harris NL. 2013. Intestinal bacteria induce TSLP to promote mutualistic T-cell responses. Mucosal Immunol 6:1157-1167.
36. Natividad JM, Hayes CL, Motta JP, Jury J, Galipeau HJ, Philip V, Garcia-Rodenas CL, Kiyama H, Bercik P, Verdu EF. 2013. Differential induction of antimicrobial REGIII by the intestinal microbiota and Bifidobacterium breve NCC2950. Appl Environ Microbiol 79:7745-7754.
37. -/-mice. Inflamm Bowel Dis 18:1434-1446.
38. Norin E, Midtvedt T. 2010. Intestinal microflora functions in laboratory mice claimed to harbor a "normal" intestinal microflora. Is the SPF concept running out of date? Anaerobe 16:311-313.
39. O'Hara AM, Shanahan F. 2006. The gut flora as a forgotten organ. EMBO Rep 7:688-693.
40. Orcutt RP, Gianni FJ, Judge RJ. 1987. Development of an "altered Schaedler flora" for NCI gnotobiotic rodents. Microecology and Therapy 17:59.
41. Park SH, Itoh K. 2005. Species-specific oligonucleotide probes for the detection and identification of Lactobacillus isolated from mouse faeces. J Appl Microbiol 99:51-57.
42. Rath HC, Herfarth HH, Ikeda JS, Grenther WB, Hamm TE Jr., Balish E, Taurog JD, Hammer RE, Wilson KH, Sartor RB. 1996. Normal luminal bacteria, especially Bacteroides species, mediate chronic colitis, gastritis, and arthritis in HLA-B27/human ß2 microglobulin transgenic rats. J Clin Invest 98:945-953.
43. Robertson BR, O'Rourke JL, Neilan BA, Vandamme P, On SL, Fox JG, Lee A. 2005. Mucispirillum schaedleri gen. nov., sp. nov., a spiral-shaped bacterium colonizing the mucus layer of the gastrointestinal tract of laboratory rodents. Int J Syst Evol Microbiol 55:1199-1204.
44. Round JL, Mazmanian SK. 2010. Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc Natl Acad Sci USA 107:12204-12209.
45. Sarma-Rupavtarm RB, Ge Z, Schauer DB, Fox JG, Polz MF. 2004. Spatial distribution and stability of the eight microbial species of the altered schaedler flora in the mouse gastrointestinal tract. Appl Environ Microbiol 70:2791-2800.
46. Savage DC. 1977. Microbial ecology of the gastrointestinal tract. Annu Rev Microbiol 31:107-133.
47. Savage DC, Dubos R, Schaedler RW. 1968. The gastrointestinal epithelium and its autochthonous bacterial flora. J Exp Med 127:67-76.
48. Savage DC, McAllister JS, Davis CP. 1971. Anaerobic bacteria on the mucosal epithelium of the murine large bowel. Infect Immun 1971:492-502.
49. Schaedler RW, Dubs R, Costello R. 1965. Association of germfree mice with bacteria isolated from normal mice. J Exp Med 122:77-82.
50. Schmitz JM, Durham CG, Schoeb TR, Soltau TD, Wolf KJ, Tanner SM, McCracken VJ, Lorenz RG. 2011. Helicobacter felis-associated gastric disease in microbiota-restricted mice. J Histochem Cytochem 59:826-841.
51. Schoeb TR, Bullard DC. 2012. Microbial and histopathologic considerations in the use of mouse models of inflammatory bowel diseases. Inflamm Bowel Dis 18:1558-1565.
52. Smith PM, Howitt MR, Panikov N, Michaud M, Gallini CA, Bohlooly YM, Glickman JN, Garrett WS. 2013. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 341:569-573.
53. Stecher B, Chaffron S, Kappeli R, Hapfelmeier S, Freedrich S, WeberTC, KirundiJ, Suar M, McCoy KD, von Mering C, Macpherson AJ, Hardt WD. 2010. Like will to like: abundances of closely related species can predict susceptibility to intestinal colonization by pathogenic and commensal bacteria. PLoS Pathog 6:e1000711.
54. Stehr M, Greweling MC, Tischer S, Singh M, Blocker H, Monner DA, Muller W. 2009. Charles River altered Schaedler flora (CRASF) remained stable for four years in a mouse colony housed in individually ventilated cages. Lab Anim 43:362-370.
55. Thompson GR, Trexler PC. 1971. Gastrointestinal structure and function in germ-free or gnotobiotic animals. Gut 12:230-235.
56. Trexler PC, Orcutt RP. 1999. Development of gnotobiotics and contamination control in laboratory animal science. In: Macpherson CW, Mattingly SF, eds. 50 Years of Laboratory Animal Science. Memphis: American Association for Laboratory Animal Science. p. 121-128.
57. Turnbaugh PJ, Ridaura VK, Faith JJ, Rey FE, Knight R, Gordon JI. 2009. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci Transl Med 1:6-14.
58. Wannemuehler MJ, Overstreet AM, Ward DV, Phillips GJ. 2014. Draft genome sequences of the altered schaedler flora, a de-fined bacterial community from gnotobiotic mice. Genome Announc 2:e00287-14.
59. Wen L, Ley RE, Volchkov PY, Stranges PB, Avanesyan L, Stonebraker AC, Hu C, Wong FS, Szot GL, Bluestone JA, Gordon JI, Chervonsky AV. 2008. Innate immunity and intestinal microbiota in the development of Type 1 diabetes. Nature 455:1109-1113.
60. -/-) mice infected with Helicobacter trogontum is associated with decreased colonization by altered Schaedler's flora. Infect Immun 74: 6615-6623.
61. WharyM T, MuthupalaniS, Ge Z, Feng Y, Lofgren J, ShiHN, Taylor NS, Correa P, Versalovic J, Wang TC, Fox JG. 2014. Helminth co-infection in Helicobacter pylori infected INS-GAS mice attenuates gastric premalignant lesions of epithelial dysplasia and glandular atrophy and preserves colonization resistance of the stomach to lower bowel microbiota. Microbes Infect 16:345-355.
62. Whitman WB, Coleman DC, Wiebe WJ. 1998. Prokaryotes: the unseen majority. Proc Natl Acad Sci USA 95:6578-6583.
63. Zoetendal EG, von Wright A, Vilpponen-Salmela T, Ben-Amor K, Akkermans AD, de Vos WM. 2002. Mucosa-associated bacteria in the human gastrointestinal tract are uniformly distributed along the colon and differ from the community recovered from feces. Appl Environ Microbiol 68:3401-3407.