Emerging Influence of the Intestinal Microbiota during Allogeneic Hematopoietic Cell Transplantation: Control the Gut and the Body Will Follow

Biology of Blood and Marrow Transplantation

Volumn 21, Issue 8, 2015, Pages 1360-1366

  Docampo, Melissa D ^a   Auletta, Jeffery J ^b   Jenq, Robert R ^c  

^a Weill Cornell Graduate School of Biomedical Sciences   (United States)

^b THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

Antimicrobial peptide; Bacteremia; Bone marrow transplant; Clostridium difficile; Dysbiosis; Enterocyte; Graft versus host disease; Gut microbiota; IL 22; Paneth cell; Regenerating islet derived III alpha; T cell; Tolerance

Indexed keywords

ALLOGENEIC HEMATOPOIETIC STEM CELL TRANSPLANTATION; GRAFT VERSUS HOST REACTION; HOMEOSTASIS; HUMAN; INTESTINE EPITHELIUM; INTESTINE FLORA; INTESTINE MUCOSA; MICROFLORA; MORBIDITY; MORTALITY; NONHUMAN; REVIEW; ALLOTRANSPLANTATION; HEMATOPOIETIC STEM CELL TRANSPLANTATION; PHYSIOLOGY; PROCEDURES; TRANSPLANTATION CONDITIONING;

GASTROINTESTINAL MICROBIOME; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; MICROBIOTA; TRANSPLANTATION CONDITIONING; TRANSPLANTATION, HOMOLOGOUS;

EID: 84937728330     PISSN: 10838791     EISSN: 15236536     Source Type: Journal    
DOI: 10.1016/j.bbmt.2015.02.016     Document Type: Review

References (82)

1. Woese C.R., Fox G.E. Phylogenetic structure of the prokaryotic domain: the primary kingdoms. Proc Natl Acad Sci USA 1977, 74:5088-5090.
2. Amann R.I., Ludwig W., Schleifer K.H. Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 1995, 59:143-169.
3. Salipante S.J., Sengupta D.J., Rosenthal C., et al. Rapid 16S rRNA next-generation sequencing of polymicrobial clinical samples for diagnosis of complex bacterial infections. PLoS One 2013, 8:e65226.
4. Murphy S., Nguyen V.H. Role of gut microbiota in graft-versus-host disease. Leuk Lymph 2011, 52:1844-1856.
5. Macpherson A.J., Slack E., Geuking M.B., McCoy K.D. The mucosal firewalls against commensal intestinal microbes. Semin Immunopathol 2009, 31:145-149.
6. van der Flier L.G., Clevers H. Stem cells, self-renewal, and differentiation in the intestinal epithelium. Annu Rev Physiol 2009, 71:241-260.
7. Specian R.D., Oliver M.G. Functional biology of intestinal goblet cells. Am J Physiol 1991, 260(2 Pt 1):C183-C193.
8. Peterson L.W., Artis D. Intestinal epithelial cells: regulators of barrier function and immune homeostasis. Nat Rev Immunol 2014, 14:141-153.
9. Bevins C.L., Salzman N.H. Paneth cells, antimicrobial peptides and maintenance of intestinal homeostasis. Nat Rev Microbiol 2011, 9:356-368.
10. Vaishnava S., Yamamoto M., Severson K.M., et al. The antibacterial lectin RegIIIgamma promotes the spatial segregation of microbiota and host in the intestine. Science 2011, 334:255-258.
11. Hill D.A., Artis D. Intestinal bacteria and the regulation of immune cell homeostasis. Annu Rev Immunol 2010, 28:623-667.
12. Rakoff-Nahoum S., Paglino J., Eslami-Varzaneh F., et al. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 2004, 118:229-241.
13. Broquet A.H., Hirata Y., McAllister C.S., Kagnoff M.F. RIG-I/MDA5/MAVS are required to signal a protective IFN response in rotavirus-infected intestinal epithelium. JImmunol 2011, 186:1618-1626.
14. Mabbott N.A., Donaldson D.S., Ohno H., et al. Microfold (M) cells: important immunosurveillance posts in the intestinal epithelium. Mucosal Immunol 2013, 6:666-677.
15. Rescigno M., Urbano M., Valzasina B., et al. Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat Immunol 2001, 2:361-367.
16. Medzhitov R. Recognition of microorganisms and activation of the immune response. Nature 2007, 449:819-826.
17. Round J.L., Mazmanian S.K. The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 2009, 9:313-323.
18. Schulz O., Jaensson E., Persson E.K., et al. Intestinal CD103+, but not CX3CR1+, antigen sampling cells migrate in lymph and serve classical dendritic cell functions. JExp Med 2009, 206:3101-3114.
19. Coombes J.L., Siddiqui K.R., Arancibia-Carcamo C.V., et al. Afunctionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF-beta and retinoic acid-dependent mechanism. JExp Med 2007, 204:1757-1764.
20. Mora J.R., Bono M.R., Manjunath N., et al. Selective imprinting of gut-homing T cells by Peyer's patch dendritic cells. Nature 2003, 424:88-93.
21. Curti A., Trabanelli S., Salvestrini V., et al. The role of indoleamine 2,3-dioxygenase in the induction of immune tolerance: focus on hematology. Blood 2009, 113:2394-2401.
22. Harrington L., Srikanth C.V., Antony R., et al. Deficiency of indoleamine 2,3-dioxygenase enhances commensal-induced antibody responses and protects against Citrobacter rodentium-induced colitis. Infect Immun 2008, 76:3045-3053.
23. Smith P.M., Howitt M.R., Panikov N., et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 2013, 341:569-573.
24. Arpaia N., Campbell C., Fan X., et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature 2013, 504:451-455.
25. Atarashi K., Tanoue T., Shima T., et al. Induction of colonic regulatory T cells by indigenous Clostridium species. Science 2011, 331:337-341.
26. Atarashi K., Tanoue T., Oshima K., et al. Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature 2013, 500:232-236.
27. Brown E.M., Sadarangani M., Finlay B.B. The role of the immune system in governing host-microbe interactions in the intestine. Nat Immunol 2013, 14:660-667.
28. Wesemann D.R., Portuguese A.J., Meyers R.M., et al. Microbial colonization influences early B-lineage development in the gut lamina propria. Nature 2013, 501:112-115.
29. Sonnenberg G.F., Artis D. Innate lymphoid cell interactions with microbiota: implications for intestinal health and disease. Immunity 2012, 37:601-610.
30. Spits H., Cupedo T. Innate lymphoid cells: emerging insights in development, lineage relationships, and function. Annu Rev Immunol 2012, 30:647-675.
31. Spits H., Di Santo J.P. The expanding family of innate lymphoid cells: regulators and effectors of immunity and tissue remodeling. Nat Immunol 2011, 12:21-27.
32. Mortha A., Chudnovskiy A., Hashimoto D., et al. Microbiota-dependent crosstalk between macrophages and ILC3 promotes intestinal homeostasis. Science 2014, 343:1477.
33. Taur Y., Pamer E.G. The intestinal microbiota and susceptibility to infection in immunocompromised patients. Curr Opin Infect Dis 2013, 26:332-337.
34. Chung H., Pamp S.J., Hill J.A., et al. Gut immune maturation depends on colonization with a host-specific microbiota. Cell 2012, 149:1578-1593.
35. Lemon K.P., Armitage G.C., Relman D.A., Fischbach M.A. Microbiota-targeted therapies: an ecological perspective. Sci Transl Med 2012, 4:137rv5.
36. Kamada N., Seo S.U., Chen G.Y., Nunez G. Role of the gut microbiota in immunity and inflammatory disease. Nat Rev Immunol 2013, 13:321-335.
37. Lupp C., Robertson M.L., Wickham M.E., et al. Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae. Cell Host Microbe 2007, 2:119-129.
38. Nicholson J.K., Holmes E., Kinross J., et al. Host-gut microbiota metabolic interactions. Science 2012, 336:1262-1267.
39. Bailey M.T. The contributing role of the intestinal microbiota in stressor-induced increases in susceptibility to enteric infection and systemic immunomodulation. Horm Behav 2012, 62:286-294.
40. Maslowski K.M., Mackay C.R. Diet, gut microbiota and immune responses. Nat Immunol 2011, 12:5-9.
41. Gordon J.I., Dewey K.G., Mills D.A., Medzhitov R.M. The human gut microbiota and undernutrition. Sci Transl Med 2012, 4:137ps12.
42. Smith M.I., Yatsunenko T., Manary M.J., et al. Gut microbiomes of Malawian twin pairs discordant for kwashiorkor. Science 2013, 339:548-554.
43. Hill G.R., Crawford J.M., Cooke K.R., et al. Total body irradiation and acute graft-versus-host disease: the role of gastrointestinal damage and inflammatory cytokines. Blood 1997, 90:3204-3213.
44. Johansson J.E., Brune M., Ekman T. The gut mucosa barrier is preserved during allogeneic, haemopoietic stem cell transplantation with reduced intensity conditioning. Bone Marrow Transplant 2001, 28:737-742.
45. Hauer-Jensen M., Denham J.W., Andreyev H.J. Radiation enteropathy-pathogenesis, treatment and prevention. Nat Rev Gastroenterol Hepatol 2014, 11:470-479.
46. Takashima S., Kadowaki M., Aoyama K., et al. The Wnt agonist R-spondin1 regulates systemic graft-versus-host disease by protecting intestinal stem cells. JExp Med 2011, 208:285-294.
47. Hanash A.M., Dudakov J.A., Hua G., et al. Interleukin-22 protects intestinal stem cells from immune-mediated tissue damage and regulates sensitivity to graft versus host disease. Immunity 2012, 37:339-350.
48. Cunliffe R.N. Alpha-defensins in the gastrointestinal tract. Mol Immunol 2003, 40:463-467.
49. Eriguchi Y., Takashima S., Oka H., et al. Graft-versus-host disease disrupts intestinal microbial ecology by inhibiting Paneth cell production of alpha-defensins. Blood 2012, 120:223-231.
50. Eriguchi Y., Uryu H., Nakamura K., et al. Reciprocal expression of enteric antimicrobial proteins in intestinal graft-versus-host disease. Biol Blood Marrow Transplant 2013, 19:1525-1529.
51. Ferrara J.L., Harris A.C., Greenson J.K., et al. Regenerating islet-derived 3-alpha is a biomarker of gastrointestinal graft-versus-host disease. Blood 2011, 118:6702-6708.
52. Jenq R.R., Ubeda C., Taur Y., et al. Regulation of intestinal inflammation by microbiota following allogeneic bone marrow transplantation. JExp Med 2012, 209:903-911.
53. Abedi M.R., Hammarstrom L., Ringden O., Smith C.I. Development of IgA deficiency after bone marrow transplantation. The influence of acute and chronic graft-versus-host disease. Transplantation 1990, 50:415-421.
54. Levine J.E., Huber E., Hammer S.T., et al. Low Paneth cell numbers at onset of gastrointestinal graft-versus-host disease identify patients at high risk for nonrelapse mortality. Blood 2013, 122:1505-1509.
55. Heimesaat M.M., Nogai A., Bereswill S., et al. MyD88/TLR9 mediated immunopathology and gut microbiota dynamics in a novel murine model of intestinal graft-versus-host disease. Gut 2010, 59:1079-1087.
56. Taur Y., Xavier J.B., Lipuma L., et al. Intestinal domination and the risk of bacteremia in patients undergoing allogeneic hematopoietic stem cell transplantation. Clin Infect Dis 2012, 55:905-914.
57. Ubeda C., Taur Y., Jenq R.R., et al. Vancomycin-resistant Enterococcus domination of intestinal microbiota is enabled by antibiotic treatment in mice and precedes bloodstream invasion in humans. JClin Invest 2010, 120:4332-4341.
58. Holler E., Butzhammer P., Schmid K., et al. Metagenomic analysis of the stool microbiome in patients receiving allogeneic stem cell transplantation: loss of diversity is associated with use of systemic antibiotics and more pronounced in gastrointestinal graft-versus-host disease. Biol Blood Marrow Transplant 2014, 20:640-645.
59. Simms-Waldrip T., Meir M., Fan D., et al. the role of gut microbiota in the development of intestinal GVHD. Biol Blood Marrow Transplant 2014, 20:S55-S56.
60. Russell W.R., Gratz S.W., Duncan S.H., et al. High-protein, reduced-carbohydrate weight-loss diets promote metabolite profiles likely to be detrimental to colonic health. Am J Clin Nutr 2011, 93:1062-1072.
61. David L.A., Maurice C.F., Carmody R.N., et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature 2014, 505:559-563.
62. Flint H.J. The impact of nutrition on the human microbiome. Nutr Rev 2012, 70(Suppl. 1):S10-S13.
63. Jones J.M., Wilson R., Bealmear P.M. Mortality and gross pathology of secondary disease in germfree mouse radiation chimeras. Radiat Res 1971, 45:577-588.
64. van Bekkum D.W., Roodenburg J., Heidt P.J., van der Waaij D. Mitigation of secondary disease of allogeneic mouse radiation chimeras by modification of the intestinal microflora. JNatl Cancer Inst 1974, 52:401-404.
65. Storb R., Prentice R.L., Buckner C.D., et al. Graft-versus-host disease and survival in patients with aplastic anemia treated by marrow grafts from HLA-identical siblings. Beneficial effect of a protective environment. NEngl J Med 1983, 308:302-307.
66. Vossen J.M., Heidt P.J., van den Berg H., et al. Prevention of infection and graft-versus-host disease by suppression of intestinal microflora in children treated with allogeneic bone marrow transplantation. Eur J Clin Microbiol Infect Dis 1990, 9:14-23.
67. Petersen F.B., Buckner C.D., Clift R.A., et al. 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 1987, 19:559-567.
68. Passweg J.R., Rowlings P.A., Atkinson K.A., et al. Influence of protective isolation on outcome of allogeneic bone marrow transplantation for leukemia. Bone Marrow Transplant 1998, 21:1231-1238.
69. Russell J.A., Chaudhry A., Booth K., et al. Early outcomes after allogeneic stem cell transplantation for leukemia and myelodysplasia without protective isolation: a 10-year experience. Biol Blood Marrow Transplant 2000, 6:109-114.
70. Vossen J.M., Guiot H.F., Lankester A.C., et al. Complete suppression of the gut microbiome prevents acute graft-versus-host disease following allogeneic bone marrow transplantation. PLoS One 2014, 9:e105706.
71. Martin P.J., McDonald G.B., Sanders J.E., et al. Increasingly frequent diagnosis of acute gastrointestinal graft-versus-host disease after allogeneic hematopoietic cell transplantation. Biol Blood Marrow Transplant 2004, 10:320-327.
72. Li H., Matte-Martone C., Tan H.S., et al. Graft-versus-host disease is independent of innate signaling pathways triggered by pathogens in host hematopoietic cells. JImmunol 2011, 186:230-241.
73. Horch M., Sahli N., Zale E., et al. Selected commensals mediate GVHD via MyD88-dependent signaling in non-hematopoietic cells. ASH Annu Meet Abstr 2012, 120:3005.
74. Nalle S.C., Aimee Kwak H., Edelblum K.L., et al. Recipient NK cell inactivation and intestinal barrier loss are required for MHC-matched graft-versus-host disease. Sci Transl Med 2014, 6:243ra87.
75. Jankovic D., Ganesan J., Bscheider M., et al. The Nlrp3 inflammasome regulates acute graft-versus-host disease. JExp Med 2013, 210:1899-1910.
76. Schwab L., Goroncy L., Palaniyandi S., et al. Neutrophil granulocytes recruited upon translocation of intestinal bacteria enhance graft-versus-host disease via tissue damage. Nat Med 2014, 20:648-654.
77. Penack O., Smith O.M., Cunningham-Bussel A., et al. NOD2 regulates hematopoietic cell function during graft-versus-host disease. JExp Med 2009, 206:2101-2110.
78. Holler E., Rogler G., Herfarth H., et al. Both donor and recipient NOD2/CARD15 mutations associate with transplant-related mortality and GVHD following allogeneic stem cell transplantation. Blood 2004, 104:889-894.
79. Gerbitz A., Schultz M., Wilke A., et al. Probiotic effects on experimental graft-versus-host disease: let them eat yogurt. Blood 2004, 103:4365-4367.
80. Storb R., Gyurkocza B., Storer B.E., et al. Allogeneic hematopoietic cell transplantation following minimal intensity conditioning: predicting acute graft-versus-host disease and graft-versus-tumor effects. Biol Blood Marrow Transplant 2013, 19:792-798.
81. Taur Y., Jenq R.R., Perales M.A., et al. The effects of intestinal tract bacterial diversity on mortality following allogeneic hematopoietic stem cell transplantation. Blood 2014, 124:1174-1182.
82. Tawara I., Liu C., Tamaki H., et al. Influence of donor microbiota on the severity of experimental graft-versus-host-disease. Biol Blood Marrow Transplant 2013, 19:164-168.