Bone marrow T-cell infiltration during acute GVHD is associated with delayed B-cell recovery and function after HSCT

Blood

Volumn 124, Issue 6, 2014, Pages 963-972

  Mensen, Angela ^a,b   Jöhrens, Korinna ^a   Anagnostopoulos, Ioannis ^a   Demski, Sonya ^a,b   Oey, Maike ^a   Stroux, Andrea ^a   Hemmati, Philipp ^a   Westermann, Jörg ^a   Blau, Olga ^a   Wittenbecher, Friedrich ^a   Movassaghi, Kamran ^a   Szyska, Martin ^b   Thomas, Sybill ^a   Dörken, Bernd ^a   Scheibenbogen, Carmen ^a,c   Arnold, Renate ^a   Na, Il Kang ^a,b  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b Experimental and Clinical Research Center   (Germany)

^c Berlin Brandenburg Center for Regenerative Therapies   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMSACRINE; BIOLOGICAL MARKER; BUSULFAN; CD3 ANTIGEN; CYCLOPHOSPHAMIDE; CYCLOSPORIN A; FLUDARABINE PHOSPHATE; IMMUNOGLOBULIN M; METHOTREXATE; MYCOPHENOLIC ACID 2 MORPHOLINOETHYL ESTER; PNEUMOCOCCUS POLYSACCHARIDE; RITUXIMAB; THYMOCYTE ANTIBODY;

ACUTE GRAFT VERSUS HOST DISEASE; ACUTE GRANULOCYTIC LEUKEMIA; ACUTE LYMPHOBLASTIC LEUKEMIA; ADULT; AGED; ALLOGENEIC HEMATOPOIETIC STEM CELL TRANSPLANTATION; ANTIBODY RESPONSE; ARTICLE; B LYMPHOCYTE ACTIVATION; BONE MARROW; EX VIVO STUDY; FEMALE; GRAFT VERSUS HOST REACTION; HISTOPATHOLOGY; HUMAN; HUMAN CELL; HUMAN TISSUE; KINETICS; LYMPHOCYTIC INFILTRATION; MAJOR CLINICAL STUDY; MALE; MYELOABLATIVE CONDITIONING; OSTEOBLAST; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; T LYMPHOCYTE; ACUTE DISEASE; ADVERSE EFFECTS; ALLOGRAFT; B LYMPHOCYTE; GENE REARRANGEMENT; GRAFT VS HOST DISEASE; HEMATOPOIETIC STEM CELL TRANSPLANTATION; IMMUNOLOGY; LEUKEMIA; LYMPHOCYTE ACTIVATION; MIDDLE AGED; PATHOLOGY; TIME; YOUNG ADULT;

ACUTE DISEASE; ADULT; AGED; ALLOGRAFTS; B-LYMPHOCYTE SUBSETS; BONE MARROW; FEMALE; GENE REARRANGEMENT, B-LYMPHOCYTE, LIGHT CHAIN; GRAFT VS HOST DISEASE; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; LEUKEMIA; LYMPHOCYTE ACTIVATION; MALE; MIDDLE AGED; OSTEOBLASTS; T-LYMPHOCYTES; TIME FACTORS; YOUNG ADULT;

EID: 84905730515     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2013-11-539031     Document Type: Article

References (59)

1. Storek J, Geddes M, Khan F, et al. Reconstitution of the immune system after hematopoietic stem cell transplantation in humans. Semin Immunopathol. 2008;30(4):425-437.
2. Bosch M, Khan FM, Storek J. Immune reconstitution after hematopoietic cell transplantation. Curr Opin Hematol. 2012;19(4): 324-335.
3. Corre E, Carmagnat M, Busson M, et al. Longterm immune deficiency after allogeneic stem cell transplantation: B-cell deficiency is associated with late infections. Haematologica. 2010;95(6): 1025-1029.
4. Storek J, Espino G, Dawson MA, Storer B, Flowers ME, Maloney DG. Low B-cell and monocyte counts on day 80 are associated with high infection rates between days 100 and 365 after allogeneic marrow transplantation. Blood. 2000;96(9):3290-3293.
5. Tomblyn M, Chiller T, Einsele H, et al. Guidelines for preventing infectious complications among hematopoietic cell transplant recipients: a global perspective. Preface. Bone Marrow Transplant. 2009;44(8):453-455.
6. Gratwohl A, Brand R, Frassoni F, et al; Acute and Chronic Leukemia Working Parties; Infectious Diseases Working Party of the European Group for Blood and Marrow Transplantation. Cause of death after allogeneic haematopoietic stem cell transplantation (HSCT) in early leukaemias: an EBMT analysis of lethal infectious complications and changes over calendar time. Bone Marrow Transplant. 2005;36(9):757-769. (Pubitemid 41613298)
7. Parkkali T, Ruutu T, Stenvik M, et al. Loss of protective immunity to polio, diphtheria and Haemophilus influenzae type b after allogeneic bone marrow transplantation. APMIS. 1996; 104(5):383-388. (Pubitemid 26226041)
8. Avanzini MA, Locatelli F, Dos Santos C, et al. B lymphocyte reconstitution after hematopoietic stem cell transplantation: functional immaturity and slow recovery of memory CD271 B cells. Exp Hematol. 2005;33(4):480-486. (Pubitemid 40387631)
9. D'Orsogna LJ, Wright MP, Krueger RG, et al. Allogeneic hematopoietic stem cell transplantation recipients have defects of both switched and igm memory B cells. Biol Blood Marrow Transplant. 2009;15(7):795-803.
10. Olkinuora H, von Willebrand E, Kantele JM, et al. The impact of early viral infections and graftversus- host disease on immune reconstitution following paediatric stem cell transplantation. Scand J Immunol. 2011;73(6):586-593.
11. Bemark M, Holmqvist J, Abrahamsson J, Mellgren K. Translational Mini-Review Series on B cell subsets in disease. Reconstitution after haematopoietic stem cell transplantation - revelation of B cell developmental pathways and lineage phenotypes. Clin Exp Immunol. 2012; 167(1):15-25.
12. Marie-Cardine A, Divay F, Dutot I, et al. Transitional B cells in humans: characterization and insight from B lymphocyte reconstitution after hematopoietic stem cell transplantation. Clin Immunol. 2008;127(1):14-25.
13. Cuss AK, Avery DT, Cannons JL, et al. Expansion of functionally immature transitional B cells is associated with human-immunodeficient states characterized by impaired humoral immunity. J Immunol. 2006;176(3):1506-1516. (Pubitemid 43134294)
14. Aucouturier P, Barra A, Intrator L, et al. Long lasting IgG subclass and antibacterial polysaccharide antibody deficiency after allogeneic bone marrow transplantation. Blood. 1987;70(3):779-785. (Pubitemid 18027412)
15. Rufer N, Helg C, Chapuis B, Roosnek E. Human memory T cells: lessons from stem cell transplantation. Trends Immunol. 2001;22(3): 136-141. (Pubitemid 32675260)
16. Sale GE, Alavaikko M, Schaefers KM, Mahan CT. Abnormal CD4:CD8 ratios and delayed germinal center reconstitution in lymph nodes of human graft recipients with graft-versus-host disease (GVHD): an immunohistological study. Exp Hematol. 1992;20(8):1017-1021.
17. Bulati M, Buffa S, Candore G, et al. B cells and immunosenescence: a focus on IgG1IgD-CD27- (DN) B cells in aged humans. Ageing Res Rev. 2011;10(2):274-284.
18. Anolik JH, Barnard J, Cappione A, et al. Rituximab improves peripheral B cell abnormalities in human systemic lupus erythematosus. Arthritis Rheum. 2004;50(11): 3580-3590. (Pubitemid 39488683)
19. Wei C, Anolik J, Cappione A, et al. A new population of cells lacking expression of CD27 represents a notable component of the B cell memory compartment in systemic lupus erythematosus. J Immunol. 2007;178(10): 6624-6633. (Pubitemid 46717447)
20. Colonna-Romano G, Bulati M, Aquino A, et al. A double-negative (IgD-CD27-) B cell population is increased in the peripheral blood of elderly people. Mech Ageing Dev. 2009;130(10): 681-690.
21. Weill JC, Weller S, Reynaud CA. Human marginal zone B cells. Annu Rev Immunol. 2009;27: 267-285.
22. Kuzmina Z, Greinix HT, Weigl R, et al. Significant differences in B-cell subpopulations characterize patients with chronic graft-versus-host diseaseassociated dysgammaglobulinemia. Blood. 2011; 117(7):2265-2274.
23. Storek J, Wells D, Dawson MA, Storer B, Maloney DG. Factors influencing B lymphopoiesis after allogeneic hematopoietic cell transplantation. Blood. 2001;98(2):489-491.
24. Xie M, Fu HX, Chang YJ, et al. Characteristics and influencing factors of CD191 B cell reconstitution in patients following haploidentical/ mismatched hematopoietic stem cell transplantation. Int J Hematol. 2012;96(1): 109-121.
25. Yanik G, Cooke KR. The lung as a target organ of graft-versus-host disease. Semin Hematol. 2006; 43(1):42-52. (Pubitemid 43063334)
26. Na IK, Lu SX, Yim NL, et al. The cytolytic molecules Fas ligand and TRAIL are required for murine thymic graft-versus-host disease. J Clin Invest. 2010;120(1):343-356.
27. Hartrampf S, Dudakov JA, Johnson LK, et al. The central nervous system is a target of acute graft versus host disease in mice. Blood. 2013;121(10): 1906-1910.
28. Sottini A, Ghidini C, Zanotti C, et al. Simultaneous quantification of recent thymic T-cell and bone marrow B-cell emigrants in patients with primary immunodeficiency undergone to stem cell transplantation. Clin Immunol. 2010;136(2): 217-227.
29. van Zelm MC, Szczepanski T, van der Burg M, van Dongen JJ. Replication history of B lymphocytes reveals homeostatic proliferation and extensive antigen-induced B cell expansion. J Exp Med. 2007;204(3):645-655. (Pubitemid 46457086)
30. Serana F, Sottini A, Chiarini M, et al. The different extent of B and T cell immune reconstitution after hematopoietic stem cell transplantation and enzyme replacement therapies in SCID patients with adenosine deaminase deficiency. J Immunol. 2010;185(12):7713-7722.
31. Mensen A, Ochs C, Stroux A, et al. Utilization of TREC and KREC quantification for the monitoring of early T- and B-cell neogenesis in adult patients after allogeneic hematopoietic stem cell transplantation. J Transl Med. 2013;11(1):188.
32. Zeger SL, Liang KY. Longitudinal data analysis for discrete and continuous outcomes. Biometrics. 1986;42(1):121-130.
33. Heitger A, Neu N, Kern H, et al. Essential role of the thymus to reconstitute naive (CD45RA1) T-helper cells after human allogeneic bone marrow transplantation. Blood. 1997;90(2): 850-857. (Pubitemid 27299126)
34. Mackall CL. T-cell immunodeficiency following cytotoxic antineoplastic therapy: a review. Stem Cells. 2000;18(1):10-18.
35. Mackall CL, Fleisher TA, Brown MR, et al. Distinctions between CD81 and CD41 T-cell regenerative pathways result in prolonged T-cell subset imbalance after intensive chemotherapy. Blood. 1997;89(10):3700-3707. (Pubitemid 27227093)
36. Panse JP, Heimfeld S, Guthrie KA, et al. Allogeneic peripheral blood stem cell graft composition affects early T-cell chimaerism and later clinical outcomes after non-myeloablative conditioning. Br J Haematol. 2005;128(5): 659-667. (Pubitemid 40343236)
37. Lutz E, Ward KN, Szydlo R, Goldman JM. Cytomegalovirus antibody avidity in allogeneic bone marrow recipients: evidence for primary or secondary humoral responses depending on donor immune status. J Med Virol. 1996;49(1): 61-65. (Pubitemid 26167183)
38. Lausen BF, Hougs L, Schejbel L, Heilmann C, Barington T. Human memory B cells transferred by allogenic bone marrow transplantation contribute significantly to the antibody repertoire of the recipient. J Immunol. 2004;172(5): 3305-3318. (Pubitemid 38263723)
39. Hill GR, Crawford JM, Cooke KR, Brinson YS, Pan L, Ferrara JL. Total body irradiation and acute graft-versus-host disease: the role of gastrointestinal damage and inflammatory cytokines. Blood. 1997;90(8):3204-3213. (Pubitemid 27444217)
40. Sellam J, Miceli-Richard C, Gottenberg JE, et al. Decreased B cell activating factor receptor expression on peripheral lymphocytes associated with increased disease activity in primary Sj̈ogren's syndrome and systemic lupus erythematosus. Ann Rheum Dis. 2007;66(6): 790-797. (Pubitemid 46846699)
41. Liu Z, Davidson A. BAFF and selection of autoreactive B cells. Trends Immunol. 2011;32(8): 388-394.
42. Sarantopoulos S, Stevenson KE, Kim HT, et al. Altered B-cell homeostasis and excess BAFF in human chronic graft-versus-host disease. Blood. 2009;113(16):3865-3874.
43. Abrahamsen IW, Sømme S, Heldal D, Egeland T, Kvale D, Tjønnfjord GE. Immune reconstitution after allogeneic stem cell transplantation: the impact of stem cell source and graft-versus-host disease. Haematologica. 2005;90(1):86-93. (Pubitemid 40193758)
44. Song MG, Kang B, Jeon JY, et al. In vivo imaging of differences in early donor cell proliferation in graft-versus-host disease hosts with different preconditioning doses. Mol Cells. 2012;33(1):79-86.
45. M̈ uller AM, Linderman JA, Florek M, Miklos D, Shizuru JA. Allogeneic T cells impair engraftment and hematopoiesis after stem cell transplantation. Proc Natl Acad Sci USA. 2010;107(33): 14721-14726.
46. Baker MB, Riley RL, Podack ER, Levy RB. Graft-versus-host-disease- associated lymphoid hypoplasia and B cell dysfunction is dependent upon donor T cell-mediated Fas-ligand function, but not perforin function. Proc Natl Acad Sci USA. 1997;94(4):1366-1371.
47. Shono Y, Ueha S, Wang Y, et al. Bone marrow graft-versus-host disease: early destruction of hematopoietic niche after MHC-mismatched hematopoietic stem cell transplantation. Blood. 2010;115(26):5401-5411.
48. Shono Y, Shiratori S, Kosugi-Kanaya M, et al. Bone marrow graft-versus-host disease: evaluation of its clinical impact on disrupted hematopoiesis after allogeneic hematopoietic stem cell transplantation. Biol Blood Marrow Transplant. 2013;20(4):495-500.
49. Zhu J, Garrett R, Jung Y, et al. Osteoblasts support B-lymphocyte commitment and differentiation from hematopoietic stem cells. Blood. 2007;109(9):3706-3712. (Pubitemid 46641719)
50. Wu JY, Scadden DT, Kronenberg HM. Role of the osteoblast lineage in the bone marrow hematopoietic niches. J Bone Miner Res. 2009; 24(5):759-764.
51. Tanaka Y, Morimoto I, Nakano Y, et al. Osteoblasts are regulated by the cellular adhesion through ICAM-1 and VCAM-1. J Bone Miner Res. 1995;10(10):1462-1469.
52. Ponomaryov T, Peled A, Petit I, et al. Induction of the chemokine stromal-derived factor-1 following DNA damage improves human stem cell function. J Clin Invest. 2000;106(11):1331-1339.
53. Schrum LW, Bost KL, Hudson MC, Marriott I. Bacterial infection induces expression of functional MHC class II molecules in murine and human osteoblasts. Bone. 2003;33(5):812-821. (Pubitemid 37393492)
54. Chang MK, Raggatt LJ, Alexander KA, et al. Osteal tissue macrophages are intercalated throughout human and mouse bone lining tissues and regulate osteoblast function in vitro and in vivo. J Immunol. 2008;181(2):1232-1244.
55. Qi H, Egen JG, Huang AY, Germain RN. Extrafollicular activation of lymph node B cells by antigen-bearing dendritic cells. Science. 2006; 312(5780):1672-1676. (Pubitemid 43902670)
56. Lum LG, Seigneuret MC, Storb RF, Witherspoon RP, Thomas ED. In vitro regulation of immunoglobulin synthesis after marrow transplantation. I. T-cell and B-cell deficiencies in patients with and without chronic graft-versushost disease. Blood. 1981;58(3):431-439.
57. Kruetzmann S, Rosado MM, Weber H, et al. Human immunoglobulin M memory B cells controlling Streptococcus pneumoniae infections are generated in the spleen. J Exp Med. 2003; 197(7):939-945. (Pubitemid 36437871)
58. Capolunghi F, Cascioli S, Giorda E, et al. CpG drives human transitional B cells to terminal differentiation and production of natural antibodies. J Immunol. 2008;180(2):800-808.
59. Forsl̈ow U, Mattsson J, Ringden O, Klominek J, Remberger M. Decreasing mortality rate in early pneumonia following hematopoietic stem cell transplantation. Scand J Infect Dis. 2006; 38(11-12):970-976. (Pubitemid 44869266)