Biology of Blood and Marrow Transplantation
Volume 15, Issue 9 , Pages 1066-1076 , September 2009

Up-Regulation of α4β7 Integrin on Peripheral T Cell Subsets Correlates with the Development of Acute Intestinal Graft-versus-Host Disease following Allogeneic Stem Cell Transplantation

  • Yi-Bin Chen

      Affiliations

    • Department of Hematology/Oncology, Division of Bone Marrow Transplantation, Massachusetts General Hospital, Boston, MA
    • Corresponding Author InformationCorrespondence and reprint requests: Yi-Bin Chen, MD, Division of Bone Marrow Transplantation, Department of Hematology/Oncology, Massachusetts General Hospital, 55 Fruit Street, Boston, MA 02114.
    • ,
  • Haesook T. Kim

      Affiliations

    • Department of Biostatistics and Computational Biology, Dana-Farber Cancer Institute, Boston, MA
    • ,
  • Sean McDonough

      Affiliations

    • Department of Medical Oncology, Division of Hematologic Malignancies, Dana-Farber Cancer Institute, Boston, MA
    • ,
  • Robert D. Odze

      Affiliations

    • Department of Pathology, Brigham and Women's Hospital, Boston, MA
    • ,
  • Xiaopan Yao

      Affiliations

    • Department of Biostatistics and Computational Biology, Dana-Farber Cancer Institute, Boston, MA
    • ,
  • Suzan Lazo-Kallanian

      Affiliations

    • Department of Medical Oncology, Division of Hematologic Malignancies, Dana-Farber Cancer Institute, Boston, MA
    • ,
  • Thomas R. Spitzer

      Affiliations

    • Department of Hematology/Oncology, Division of Bone Marrow Transplantation, Massachusetts General Hospital, Boston, MA
    • ,
  • Robert Soiffer

      Affiliations

    • Department of Medical Oncology, Division of Hematologic Malignancies, Dana-Farber Cancer Institute, Boston, MA
    • ,
  • Joseph H. Antin

      Affiliations

    • Department of Medical Oncology, Division of Hematologic Malignancies, Dana-Farber Cancer Institute, Boston, MA
    • ,
  • Jerome Ritz

      Affiliations

    • Department of Medical Oncology, Division of Hematologic Malignancies, Dana-Farber Cancer Institute, Boston, MA
    • Harvard Stem Cell Institute, Boston, MA

Received 19 February 2009 ,Accepted 5 May 2009.

References 

  1. Ferrara JL, Deeg HJ. Graft-versus-host disease. N Engl J Med. 1991;324:667–674
  2. Hill GR, Ferrara JL. The primacy of the gastrointestinal tract as a target organ of acute graft-versus-host disease: rationale for the use of cytokine shields in allogeneic bone marrow transplantation. Blood. 2000;95:2754–2759
  3. Wysocki CA, Panoskaltsis-Mortari A, Blazar BR, et al. Leukocyte migration and graft-versus-host disease. Blood. 2005;105:4191–4199
  4. Johansson-Lindbom B, Svensson M, Wurbel MA, et al. Selective generation of gut tropic T cells in gut-associated lymphoid tissue (GALT): requirement for GALT dendritic cells and adjuvant. J Exp Med. 2003;198:963–969
  5. Mora JR, Bono MR, Manjunath N, et al. Selective imprinting of gut-homing T cells by Peyer's patch dendritic cells. Nature. 2003;424:88–93
  6. Iwata M, Hirakiyama A, Eshima Y, et al. Retinoic acid imprints gut-homing specificity on T cells. Immunity. 2004;21:527–538
  7. Svensson M, Johansson-Lindbom B, Wurbel MA, et al. Selective generation of gut-tropic T cells in gut-associated lymphoid tissues: requirement for GALT dendritic cells and adjuvant. Ann N Y Acad Sci. 2004;1029:405–407
  8. Beilhack A, Schulz S, Baker J, et al. Prevention of acute graft-versus-host disease by blocking T-cell entry to secondary lymphoid organs. Blood. 2008;111:2919–2928
  9. Guy-Grand D, Vassalli P. Gut intraepithelial lymphocyte development. Curr Opin Immunol. 2002;14:255–259
  10. Hayday A, Theodoridis E, Ramsburg E, et al. Intraepithelial lymphocytes: exploring the third way in immunology. Nat Immunol. 2001;2:997–1003
  11. Butcher EC, Picker LJ. Lymphocyte homing and homeostasis. Science. 1996;272:60–66
  12. Springer TA. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm. Cell. 1994;76:301–314
  13. von Andrian UH, Mackay CR. T-cell function and migration: two sides of the same coin. N Engl J Med. 2000;343:1020–1034
  14. Bargatze RF, Jutila MA, Butcher EC. Distinct roles of L-selectin and integrins alpha 4 beta 7 and LFA-1 in lymphocyte homing to Peyer's patch-HEV in situ: the multistep model confirmed and refined. Immunity. 1995;3:99–108
  15. Farstad IN, Halstensen TS, Kvale D, et al. Topographic distribution of homing receptors on B and T cells in human gut-associated lymphoid tissue: relation of L-selectin and integrin alpha 4 beta 7 to naive and memory phenotypes. Am J Pathol. 1997;150:187–199
  16. Rott LS, Briskin MJ, Andrew DP, et al. A fundamental subdivision of circulating lymphocytes defined by adhesion to mucosal addressin cell adhesion molecule-1: comparison with vascular cell adhesion molecule-1 and correlation with beta 7 integrins and memory differentiation. J Immunol. 1996;156:3727–3736
  17. Berlin C, Berg EL, Briskin MJ, et al. Alpha 4 beta 7 integrin mediates lymphocyte binding to the mucosal vascular addressin MAdCAM-1. Cell. 1993;74:185–195
  18. Nakache M, Berg EL, Streeter PR, et al. The mucosal vascular addressin is a tissue-specific endothelial cell adhesion molecule for circulating lymphocytes. Nature. 1989;337:179–181
  19. Streeter PR, Berg EL, Rouse BT, et al. A tissue-specific endothelial cell molecule involved in lymphocyte homing. Nature. 1988;331:41–46
  20. Briskin M, Winsor-Hines D, Shyjan A, et al. Human mucosal addressin cell adhesion molecule-1 is preferentially expressed in intestinal tract and associated lymphoid tissue. Am J Pathol. 1997;151:97–110
  21. Campbell JJ, Hedrick J, Zlotnik A, et al. Chemokines and the arrest of lymphocytes rolling under flow conditions. Science. 1998;279:381–384
  22. Cyster JG. Chemokines and cell migration in secondary lymphoid organs. Science. 1999;286:2098–2102
  23. Luster AD. Chemokines: chemotactic cytokines that mediate inflammation. N Engl J Med. 1998;338:436–445
  24. Uehara S, Grinberg A, Farber JM, et al. A role for CCR9 in T lymphocyte development and migration. J Immunol. 2002;168:2811–2819
  25. Wurbel MA, Malissen B, Campbell JJ. Complex regulation of CCR9 at multiple discrete stages of T cell development. Eur J Immunol. 2006;36:73–81
  26. Kunkel EJ, Campbell JJ, Haraldsen G, et al. Lymphocyte CC chemokine receptor 9 and epithelial thymus-expressed chemokine (TECK) expression distinguish the small intestinal immune compartment: epithelial expression of tissue-specific chemokines as an organizing principle in regional immunity. J Exp Med. 2000;192:761–768
  27. Zabel BA, Agace WW, Campbell JJ, et al. Human G protein–coupled receptor GPR-9-6/CC chemokine receptor 9 is selectively expressed on intestinal homing T lymphocytes, mucosal lymphocytes, and thymocytes and is required for thymus-expressed chemokine-mediated chemotaxis. J Exp Med. 1999;190:1241–1256
  28. Przepiorka D, Weisdorf D, Martin P, et al. 1994 Consensus Conference on Acute GVHD Grading. Bone Marrow Transplant. 1995;15:825–828
  29. Beilhack A, Schulz S, Baker J, et al. In vivo analyses of early events in acute graft-versus-host disease reveal sequential infiltration of T-cell subsets. Blood. 2005;106:1113–1122
  30. Panoskaltsis-Mortari A, Price A, Hermanson JR, et al. In vivo imaging of graft-versus-host-disease in mice. Blood. 2004;103:3590–3598
  31. Hadeiba H, Sato T, Habtezion A, et al. CCR9 expression defines tolerogenic plasmacytoid dendritic cells able to suppress acute graft-versus-host disease. Nat Immunol. 2008;9:1253–1260
  32. Sale GE, Shulman HM, McDonald GB, et al. Gastrointestinal graft-versus-host disease in man: a clinicopathologic study of the rectal biopsy. Am J Surg Pathol. 1979;3:291–299
  33. Woodruff JM, Hansen JA, Good RA, et al. The pathology of the graft-versus-host reaction (GVHR) in adults receiving bone marrow transplants. Transplant Proc. 1976;8:675–684
  34. Kobayashi S, Hashino S, Tanaka J, et al. Increased adhesion molecule expression during graft-versus-host disease. Transplant Proc. 2000;32:2452–2453
  35. Yakoub-Agha I, Saule P, Depil S, et al. A high proportion of donor CD4+ T cells expressing the lymph node–homing chemokine receptor CCR7 increases incidence and severity of acute graft-versus-host disease in patients undergoing allogeneic stem cell transplantation for hematological malignancy. Leukemia. 2006;20:1557–1565
  36. Jaksch M, Remberger M, Mattsson J. Increased gene expression of chemokine receptors is correlated with acute graft-versus-host disease after allogeneic stem cell transplantation. Biol Blood Marrow Transplant. 2005;11:280–287
  37. Piper KP, Horlock C, Curnow SJ, et al. CXCL10–CXCR3 interactions play an important role in the pathogenesis of acute graft-versus-host disease in the skin following allogeneic stem cell transplantation. Blood. 2007;110:3827–3832
  38. Murai M, Yoneyama H, Ezaki T, et al. Peyer's patch is the essential site in initiating murine acute and lethal graft-versus-host reaction. Nat Immunol. 2003;4:154–160
  39. Petrovic A, Alpdogan O, Willis LM, et al. LPAM (alpha 4 beta 7 integrin) is an important homing integrin on alloreactive T cells in the development of intestinal graft-versus-host disease. Blood. 2004;103:1542–1547
  40. Waldman E, Lu SX, Hubbard VM, et al. Absence of beta7 integrin results in less graft-versus-host disease because of decreased homing of alloreactive T cells to intestine. Blood. 2006;107:1703–1711
  41. Dutt S, Ermann J, Tseng D, et al. L-selectin and beta7 integrin on donor CD4 T cells are required for the early migration to host mesenteric lymph nodes and acute colitis of graft-versus-host disease. Blood. 2005;106:4009–4015
  42. Anderson BE, Taylor PA, McNiff JM, et al. Effects of donor T-cell trafficking and priming site on graft-versus-host disease induction by naive and memory phenotype CD4 T cells. Blood. 2008;111:5242–5251
  43. Chakraverty R, Cote D, Buchli J, et al. An inflammatory checkpoint regulates recruitment of graft-versus-host reactive T cells to peripheral tissues. J Exp Med. 2006;203:2021–2031
  44. Mapara MY, Leng C, Kim YM, et al. Expression of chemokines in GVHD target organs is influenced by conditioning and genetic factors and amplified by GVHR. Biol Blood Marrow Transplant. 2006;12:623–634
  45. Feagan BG, Greenberg GR, Wild G, et al. Treatment of ulcerative colitis with a humanized antibody to the alpha4beta7 integrin. N Engl J Med. 2005;352:2499–2507

 Financial disclosure: See Acknowledgments on page 1075.

PII: S1083-8791(09)00227-4

doi: 10.1016/j.bbmt.2009.05.003

Biology of Blood and Marrow Transplantation
Volume 15, Issue 9 , Pages 1066-1076 , September 2009

Article Tools

* Image Usage & Resolution