Regulation of intestinal inflammation by microbiota following allogeneic bone marrow transplantation

Journal of Experimental Medicine

Volumn 209, Issue 5, 2012, Pages 903-911

  Jenq, Robert R ^a,b   Ubeda, Carles ^a,f   Taur, Ying ^a,b   Menezes, Clarissa C ^c   Khanin, Raya ^a   Dudakov, Jarrod A ^a   Liu, Chen ^d   West, Mallory L ^a   Singer, Natalie V ^a   Equinda, Michele J ^a   Gobourne, Asia ^a   Lipuma, Lauren ^a   Young, Lauren F ^a   Smith, Odette M ^a   Ghosh, Arnab ^a   Hanash, Alan M ^a,b   Goldberg, Jenna D ^a,b   Aoyama, Kazutoshi ^e   Blazar, Bruce R ^e   Pamer, Eric G ^a,b,c   van den Brink, Marcel R M ^a,b,c   more..

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

^c Weill Graduate School of Medical Sciences of Cornell University   (United States)

^d UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

^e UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^f Center for Advanced Research in Public Health   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

BUDESONIDE; CALCINEURIN INHIBITOR; METHOTREXATE; METHYLPREDNISOLONE; METRONIDAZOLE; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; QUINOLINE DERIVED ANTIINFECTIVE AGENT; RAPAMYCIN; AMPICILLIN; DEXTRAN SULFATE; RNA 16S;

ALLOGENIC BONE MARROW TRANSPLANTATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBIOTIC PROPHYLAXIS; ARTICLE; CLOSTRIDIALES; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE SEVERITY; ENTERITIS; ENTEROCOCCUS; FEMALE; GRAFT RECIPIENT; GRAFT VERSUS HOST REACTION; HUMAN; HUMAN TISSUE; INTESTINE FLORA; LACTOBACILLALES; MALE; MOUSE; NONHUMAN; PANETH CELL; PRIORITY JOURNAL; RISK FACTOR; STREPTOCOCCUS; TREATMENT OUTCOME; ALLOTRANSPLANTATION; ANIMAL; BIODIVERSITY; BONE MARROW TRANSPLANTATION; DNA SEQUENCE; ENTEROCOLITIS; FECES; GENETICS; GRAM POSITIVE BACTERIUM; ISOLATION AND PURIFICATION; METAGENOME; MICROBIOLOGY; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PATHOLOGY; PHYLOGENY; SPECIES DIFFERENCE;

AMPICILLIN; ANIMALS; BASE SEQUENCE; BIODIVERSITY; BONE MARROW TRANSPLANTATION; DEXTRAN SULFATE; ENTEROCOLITIS; FECES; GRAFT VS HOST DISEASE; GRAM-POSITIVE BACTERIA; HUMANS; METAGENOME; MICE; MOLECULAR SEQUENCE DATA; PHYLOGENY; RNA, RIBOSOMAL, 16S; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY; TRANSPLANTATION, HOMOLOGOUS;

EID: 84861539347     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20112408     Document Type: Article

References (37)

1. Beelen, D.W., A. Elmaagacli, K.D. Müller, H. Hirche, and U.W. Schaefer. 1999. Influence of intestinal bacterial decontamination using metronidazole and ciprofloxacin or ciprofloxacin alone on the development of acute graft-versus-host disease after marrow transplantation in patients with hematologic malignancies: final results and long-term follow-up of an open-label prospective randomized trial. Blood. 93:3267-3275.
2. Blazar, B.R., P.A. Taylor, M.W. Boyer, A. Panoskaltsis-Mortari, J.P. Allison, and D.A. Vallera. 1997. CD28/B7 interactions are required for sustaining the graft-versus-leukemia effect of delayed post-bone marrow transplantation splenocyte infusion in murine recipients of myeloid or lymphoid leukemia cells. J. Immunol. 159:3460-3473.
3. Blazar, B.R., C.J. Lees, P.J. Martin, R.J. Noelle, B. Kwon, W. Murphy, and P.A. Taylor. 2000. Host T cells resist graft-versus-host disease mediated by donor leukocyte infusions. J. Immunol. 165:4901-4909.
4. Buhnik-Rosenblau, K., Y. Danin-Poleg, and Y. Kashi. 2011. Predominant effect of host genetics on levels of Lactobacillus johnsonii bacteria in the mouse gut. Appl. Environ. Microbiol. 77:6531-6538. http://dx.doi.org/ 10.1128/AEM.00324-11
5. Cooke, K.R., L. Kobzik, T.R. Martin, J. Brewer, J. Delmonte Jr., J.M. Crawford, and J.L. Ferrara. 1996. An experimental model of idiopathic pneumonia syndrome after bone marrow transplantation: I. The roles of minor H antigens and endotoxin. Blood. 88: 3230-3239.
6. Dethlefsen, L., S. Huse, M.L. Sogin, and D.A. Relman. 2008. The pervasive effects of an antibiotic on the human gut microbiota, as revealed by deep 16S rRNA sequencing. PLoS Biol. 6:e280. http://dx.doi.org/10.1371/ journal.pbio.0060280
7. Dubberke, E.R., J.M. Hollands, P. Georgantopoulos, K. Augustin, J.F. DiPersio, L.M. Mundy, and H.J. Khoury. 2006. Vancomycin-resistant enterococcal bloodstream infections on a hematopoietic stem cell transplant unit: are the sick getting sicker? Bone Marrow Transplant. 38:813- 819. http://dx.doi.org/10.1038/sj.bmt.1705530
8. Ferrara, J.L., J.E. Levine, P. Reddy, and E. Holler. 2009. Graft-versus-host disease. Lancet. 373:1550-1561. http://dx.doi.org/10.1016/S0140-6736(09)60237-3
9. Gerbitz, A., M. Schultz, A. Wilke, H.J. Linde, J. Schölmerich, R. Andreesen, and E. Holler. 2004. Probiotic effects on experimental graft-versus-host disease: let them eat yogurt. Blood. 103:4365-4367. http://dx.doi .org/10.1182/blood-2003-11-3769
10. Heimesaat, M.M., A. Nogai, S. Bereswill, R. Plickert, A. Fischer, C. Loddenkemper, U. Steinhoff, S. Tchaptchet, E. Thiel, M.A. Freudenberg, et al. 2010. MyD88/TLR9 mediated immunopathology and gut microbiota dynamics in a novel murine model of intestinal graftversus-host disease. Gut. 59:1079-1087. http://dx.doi.org/10.1136/gut.2009.197434
11. Hill, G.R., J.M. Crawford, K.R. Cooke, Y.S. Brinson, L. Pan, and J.L. Ferrara. 1997. Total body irradiation and acute graft-versus-host disease: the role of gastrointestinal damage and inflammatory cytokines. Blood. 90:3204-3213.
12. Jones, J.M., R. Wilson, and P.M. Bealmear. 1971. Mortality and gross pathology of secondary disease in germfree mouse radiation chimeras. Radiat. Res. 45:577-588. http://dx.doi.org/10.2307/3573066
13. Kau, A.L., P.P. Ahern, N.W. Griffin, A.L. Goodman, and J.I. Gordon. 2011. Human nutrition, the gut microbiome and the immune system. Nature. 474:327-336. http://dx.doi.org/10.1038/nature10213
14. Kim, S.O., H.I. Sheikh, S.D. Ha, A. Martins, and G. Reid. 2006. G-CSFmediated inhibition of JNK is a key mechanism for Lactobacillus rhamnosusinduced suppression of TNF production in macrophages. Cell. Microbiol. 8:1958-1971. http://dx.doi.org/10.1111/j.1462-5822.2006.00763.x
15. Korngold, R., and J. Sprent. 1978. Lethal graft-versus-host disease after bone marrow transplantation across minor histocompatibility barriers in mice. Prevention by removing mature T cells from marrow. J. Exp. Med. 148:1687-1698. http://dx.doi.org/10.1084/jem.148.6.1687
16. Lozupone, C., M. Hamady, and R. Knight. 2006. UniFrac-an online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinformatics. 7:371. http://dx.doi.org/10.1186/1471-2105-7-371
17. Magurran, A.E. 2004. Measuring Biological Diversity. Blackwell Pub., Malden, Ma. 256 pages.
18. Maloy, K.J., and F. Powrie. 2011. Intestinal homeostasis and its breakdown in inflammatory bowel disease. Nature. 474:298-306. http://dx.doi.org/10.1038/nature10208
19. Manson, J.M., M. Rauch, and M.S. Gilmore. 2008. The commensal microbiology of the gastrointestinal tract. Adv. Exp. Med. Biol. 635:15-28. http://dx.doi.org/10.1007/978-0-387-09550-9_2
20. Passweg, J.R., P.A. Rowlings, K.A. Atkinson, A.J. Barrett, R.P. Gale, A. Gratwohl, N. Jacobsen, J.P. Klein, P. Ljungman, J.A. Russell, et al. 1998. Influence of protective isolation on outcome of allogeneic bone marrow transplantation for leukemia. Bone Marrow Transplant. 21:1231- 1238. http://dx.doi.org/10.1038/sj.bmt.1701238
21. Penack, O., O.M. Smith, A. Cunningham-Bussel, X. Liu, U. Rao, N. Yim, I.K. Na, A.M. Holland, A. Ghosh, S.X. Lu, et al. 2009. NOD2 regulates hematopoietic cell function during graft-versus-host disease. J. Exp. Med. 206:2101-2110. http://dx.doi.org/10.1084/jem.20090623
22. Penack, O., E. Henke, D. Suh, C.G. King, O.M. Smith, I.K. Na, A.M. Holland, A. Ghosh, S.X. Lu, R.R. Jenq, et al. 2010. Inhibition of neovascularization to simultaneously ameliorate graft-vs-host disease and decrease tumor growth. J. Natl. Cancer Inst. 102:894-908. http://dx.doi.org/10.1093/jnci/djq172
23. Petersen, F.B., C.D. Buckner, R.A. Clift, N. Nelson, G.W. Counts, J.D. Meyers, and E.D. Thomas. 1987. Infectious complications in patients undergoing marrow transplantation: a prospective randomized study of the additional effect of decontamination and laminar air flow isolation among patients receiving prophylactic systemic antibiotics. Scand. J. Infect. Dis. 19:559-567. http://dx.doi.org/10.3109/ 00365548709032423
24. Pridmore, R.D., B. Berger, F. Desiere, D. Vilanova, C. Barretto, A.C. Pittet, M.C. Zwahlen, M. Rouvet, E. Altermann, R. Barrangou, et al. 2004. The genome sequence of the probiotic intestinal bacterium Lactobacillus johnsonii NCC 533. Proc. Natl. Acad. Sci. USA. 101:2512-2517. http:// dx.doi.org/10.1073/pnas.0307327101
25. Reddy, P., and J.L.M. Ferrara. 2008. Mouse models of graft-versus-host disease. In StemBook. Lisa Gerard, editor. StemBook, Cambridge, MA. http://www.stembook.org/node/548
26. Russell, J.A., A. Chaudhry, K. Booth, C. Brown, R.C. Woodman, K. Valentine, D. Stewart, J.D. Ruether, B.A. Ruether, A.R. Jones, et al. 2000. Early outcomes after allogeneic stem cell transplantation for leukemia and myelodysplasia without protective isolation: a 10-year experience. Biol. Blood Marrow Transplant. 6:109-114. http://dx.doi.org/ 10.1016/S1083-8791(00)70073-5
27. Sayegh, M.H., Z. Wu, W.W. Hancock, P.B. Langmuir, M. Mata, S. Sandner, K. Kishimoto, M. Sho, E. Palmer, R.N. Mitchell, and L.A. Turka. 2003. Allograft rejection in a new allospecific CD4+ TCR transgenic mouse. Am. J. Transplant. 3:381-389. http://dx.doi.org/10.1034/ j.1600-6143.2003.00062.x
28. Schloss, P.D., S.L. Westcott, T. Ryabin, J.R. Hall, M. Hartmann, E.B. Hollister, R.A. Lesniewski, B.B. Oakley, D.H. Parks, C.J. Robinson, et al. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75:7537-7541. http://dx.doi.org/10.1128/AEM.01541-09
29. Schroeder, M.A., and J.F. DiPersio. 2011. Mouse models of graft-versus-host disease: advances and limitations. Dis Model Mech. 4:318-333. http:// dx.doi.org/10.1242/dmm.006668
30. Sekirov, I., S.L. Russell, L.C. Antunes, and B.B. Finlay. 2010. Gut microbiota in health and disease. Physiol. Rev. 90:859-904. http://dx.doi.org/10.1152/physrev.00045.2009
31. Steck, N., M. Hoffmann, I.G. Sava, S.C. Kim, H. Hahne, S.L. Tonkonogy, K. Mair, D. Krueger, M. Pruteanu, F. Shanahan, et al. 2011. Enterococcus faecalis metalloprotease compromises epithelial barrier and contributes to intestinal inflammation. Gastroenterology. 141:959-971. http://dx.doi.org/10.1053/j.gastro.2011.05.035
32. Storb, R., R.L. Prentice, C.D. Buckner, R.A. Clift, F. Appelbaum, J. Deeg, K. Doney, J.A. Hansen, M. Mason, J.E. Sanders, et al. 1983. Graftversus-host disease and survival in patients with aplastic anemia treated by marrow grafts from HLA-identical siblings. Beneficial effect of a protective environment. N. Engl. J. Med. 308:302-307. http://dx.doi.org/10.1056/NEJM198302103080602
33. Ubeda, C., Y. Taur, R.R. Jenq, M.J. Equinda, T. Son, M. Samstein, A. Viale, N.D. Socci, M.R.M. van den Brink, M. Kamboj, and E.G. Pamer. 2010. Intestinal domination by Vancomycin-resistant Enterococcus precedes bloodstream invasion in humans. J. Clin. Invest. In press.
34. van Bekkum, D.W., J. Roodenburg, P.J. Heidt, and D. van der Waaij. 1974. Mitigation of secondary disease of allogeneic mouse radiation chimeras by modification of the intestinal microflora. J. Natl. Cancer Inst. 52:401-404.
35. Wang, Q., G.M. Garrity, J.M. Tiedje, and J.R. Cole. 2007. Naive Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73:5261-5267. http://dx.doi.org/10.1128/AEM.00062-07
36. Willing, B.P., S.L. Russell, and B.B. Finlay. 2011. Shifting the balance: antibiotic effects on host-microbiota mutualism. Nat. Rev. Microbiol. 9:233-243. http://dx.doi.org/10.1038/nrmicro2536
37. Woodmansey, E.J. 2007. Intestinal bacteria and ageing. J. Appl. Microbiol. 102:1178-1186. http://dx.doi.org/10.1111/j.1365-2672.2007.03400.x