Cytolytic pathways used by effector cells derived from recipient naive and memory T cells and natural killer cells in resistance to allogeneic hematopoietic cell transplantation

Biology of Blood and Marrow Transplantation

Volumn 11, Issue 12, 2005, Pages 957-971

  Zimmerman, Zachary ^a   Jones, Monica ^a   Shatry, Alwi ^a   Komatsu, Masanobu ^a   Mammolenti, Michele ^a   Levy, Robert ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

Author keywords

Conditions of transplant; Cytotoxic pathways; Effector NK; Resistance to hematopoietic transplants; T naive and T memory cells

Indexed keywords

ALLOANTIGEN; IMMUNOSUPPRESSIVE AGENT;

ALLOGENEIC HEMATOPOIETIC STEM CELL TRANSPLANTATION; CELL POPULATION; CYTOLYSIS; DONOR; EFFECTOR CELL; HISTOCOMPATIBILITY; HLA MATCHING; HOST RESISTANCE; HUMAN; IMMUNE DEFICIENCY; IMMUNOREGULATION; INFECTION; INFECTION RESISTANCE; INOCULATION; LYMPHOCYTE DEPLETION; MEMORY CELL; MYELOABLATIVE CONDITIONING; NATURAL KILLER CELL; NONHUMAN; RECIPIENT; REDUCED INTENSITY CONDITIONING; REVIEW; SENSITIZATION; T LYMPHOCYTE; TUMOR IMMUNITY;

ANIMALS; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMANS; IMMUNOLOGIC MEMORY; KILLER CELLS, NATURAL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; TRANSPLANTATION IMMUNOLOGY; TRANSPLANTATION, HOMOLOGOUS;

EID: 28744443608     PISSN: 10838791     EISSN: 15236536     Source Type: Journal    
DOI: 10.1016/j.bbmt.2005.07.006     Document Type: Review

References (118)

1. B. Lowin M. Hahne C. Mattmann J. Tschopp Cytolytic T-cell cytotoxicity is mediated through perforin and Fas lytic pathways Nature 370 1994 650-652
2. M.B. Baker E.R. Podack R.B. Levy Perforin- and Fas-mediated cytotoxic pathways are not required for allogeneic resistance to bone marrow grafts in mice Biol Blood Marrow Transplant 1 1995 69-73
3. J.A. Shizuru L. Jerabek C.T. Edwards I.L. Weissman Transplantation of purified hematopoietic stem cells requirements for overcoming the barriers of allogeneic engraftment Biol Blood Marrow Transplant 2 1996 3-14
4. T.A. Graubert J.H. Russell T.J. Ley The role of granzyme B in murine models of acute graft-versus-host disease and graft rejection Blood 87 1996 1232-1237
5. M. Bennett P.A. Taylor M. Austin et al. Cytokine and cytotoxic pathways of NK cell rejection of class I-deficient bone marrow grafts: Influence of mouse colony environment Int Immunol 10 998 85-790
6. M. Jones M. Komatsu R.B. Levy Cytotoxically impaired transplant recipients can efficiently resist major histocompatibility complex-matched bone marrow allografts Biol Blood Marrow Transplant 6 2000 456-790
7. M.A. Taylor P.M. Chaudhary J. Klem V. Kumar J.D. Schatzle M. Bennett Inhibition of the death receptor pathway by cFLIP confers partial engraftment of MHC class I-deficient stem cells and reduces tumor clearance in perforin-deficient mice J Immunol 167 2001 4230-4237
8. M.A. Taylor B. Ward J.D. Schatzle M. Bennett Perforin- and Fas-dependent mechanisms of natural killer cell mediated rejection of incompatible bone marrow cell grafts Eur J Immunol 32 2002 793-799
9. M. Komatsu M. Mammolenti M. Jones R. Jurecic T.J. Sayers R.B. Levy Antigen-primed CD8+ T cells can mediate resistance, preventing allogeneic marrow engraftment in the simultaneous absence of perforin-, CD95L-, TNFR1-, and TRAIL-dependent killing Blood 101 2003 3991-3999
10. H.L. Aguila R.J. Hershberger I.L. Weissman Transgenic mice carrying the diphtheria toxin A chain gene under the control of the granzyme A promoter: Expected depletion of cytotoxic cells and unexpected depletion of CD8 T cells Proc Natl Acad Sci U S A 92 1995 10192-10196
11. D.L. Thiele P.E. Lipsky The immunosuppressive activity of L-leucyl-L-leucine methyl ester: Selective ablation of cytotoxic lymphocytes and monocytes J Immunol 136 1986 1038-1048
12. T.P. Loughran R.F. Raff T.C. Graham et al. Tranfusion of autologous cytotoxic cells leads to failure of unrelated, DLA-nonidentical marrow grafts Exp Hematol 18 1990 1126-1131
13. Z.F. Zimmerman A.M. Shatry V. Deyev et al. Effector cells derived from host CD8 memory T cells mediate rapid resistance against minor histocompatibility antigen-mismatched allogeneic marrow grafts without participation of perforin, Fas ligand, and the simultaneous inhibition of 3 tumor necrosis factor family effector pathways Biol Blood Marrow Transplant 11 2005 576-586
14. R. Storb P.L. Weiden T.C. Graham E.D. Thomas Failure of engraftment and graft-versus-host disease after canine marrow transplantation. Two phenomena linked to but not exclusively determined by known antigens of the major histocompatibility complex Transplant Proc 10 1978 113-118
15. W.J. Murphy V. Kumar M. Bennett Rejection of bone marrow allografts by mice with severe combined immune deficiency (SCID). Evidence that natural killer cells can mediate the specificity of marrow graft rejection J Exp Med 165 1987 1212-1217
16. B. Yankelevich C. Knobloch M. Nowicki G. Dennert A novel cell type for marrow graft rejection in mice. T cells with NK phenotype cause acute rejection of marrow grafts J Immunol 165 1989 3423-3430
17. R.F. Raff H.J. Deeg T.P. Loughran Jr et al. Characterization of host cells involved in resistance to marrow grafts in dogs transplanted from unrelated DLA-nonidentical donors Blood 68 1986 861-868
18. L.A. Lee J.J. Sergio M. Sykes Natural killer cells weakly resist engraftment of allogeneic, long-term, multilineage-repopulating hematopoietic stem cells Tranplantation 61 1996 125-132
19. W.J. Murphy V. Kumar M. Bennett Acute rejection of murine bone marrow allografts by natural killer cells and T cells: Differences in kinetics and target antigens recognized J Exp Med 166 1987 1499-1550
20. K. Takeda M.W. Moore G. Dennert Acute rejection of marrow grafts in mice. Dependence on and independence of functional TcR in the rejection process J Immunol 152 1994 4407-4416
21. A.J. Barge G. Johnson R. Witherspoon B. Torok-Storb Antibody-mediated marrow failure after allogeneic bone marrow transplantation Blood 74 1989 1477-1480
22. D.B. Miklos H.T. Kim E. Zorn et al. Antibody response to DBY minor histocompatibility antigen is induced after allogeneic stem cell transplantation and in healthy female donors Blood 103 2004 353-359
23. E. Zorn D.B. Miklos B.H. Floyd et al. Minor histocompatibility antigen DBY elicits a coordinated B and T cell response after allogeneic stem cell transplantation J Exp Med 199 2004 1133-1142
24. J.M. Grayson A.J. Zajac J.D. Altman R. Ahmed Cutting edge: Increased expression of Bcl-2 in antigen-specific memory CD8+ T cells J Immunol 164 2000 3950-3954
25. R. Storb Critical issues in bone marrow transplantation Transplant Proc 19 1987 2774-2781
26. Y. Reisner I. Benbassat D. Douer A. Kaploon E. Schwartz B. Ramot Demonstration of clonable alloreactive host T cells in a primate model for bone marrow transplantation Proc Natl Acad Sci U S A 83 1986 4012-4015
27. A.B. Kraus J. Shaffer H.C. Toh et al. Early host CD8 T-cell recovery and sensitized anti-donor interleukin-2-producing and cytotoxic T-cell responses associated with marrow graft rejection following nonmyeloablative allogeneic bone marrow transplantation Exp Hematol 31 2003 609-621
28. P.A. Lowry I.A. Tabbara Peripheral hematopoietic stem cell transplantation: Current concepts Exp Hematol 20 1992 937-942
29. C.T. Jordan I.R. Lemischka Clonal and systemic analysis of long-term hematopoiesis in the mouse Genes Dev 4 1990 220-232
30. R.J. Jones J.E. Wagner P. Celano M.S. Zicha S.J. Sharkis Separation of pluripotent haematopoietic stem cells from spleen colony-forming cells Nature 347 1990 188-189
31. H.L. Aguila I.L. Weissman Hematopoietic stem cells are not direct cytotoxic targets of natural killer cells Blood 87 1996 1225-1231
32. C.Y. Koh L.A. Welniak W.J. Murphy Lack of correlation between an assay used to determine early marrow allograft rejection and long-term chimerism after murine allogeneic bone marrow transplantation: Effects of marrow dose Biol Blood Marrow Transplant 11 2005 252-259
33. C. Davenport V. Kumar M. Bennett Rapid rejection of H2k and H2k/b bone marrow cell grafts by CD8+ T cells and NK cells in irradiated mice J Immunol 155 1995 3742-3749
34. D.A. Vallera P.A. Taylor J. Sprent B.R. Blazar The role of host T-cell subsets in bone-marrow rejection directed to isolated major histocompatibility complex class-I versus class-II differences of Bm1 and Bm12 mutant mice Transplantation 57 1994 249-256
35. J. Sprent C.D. Surh D. Agus M. Hurd S. Sutton W.R. Heath Profound atrophy of the bone marrow reflecting major histocompatibility complex class II-restricted destruction of stem cells by CD4+ cells J Exp Med 180 1994 307-317
36. C.L. Sentman R. Streilein V. Kumar et al. Kinetics and location of bone marrow cell graft rejection by irradiated mice Nat Immun Cell Growth Regul 7 1988 95-105
37. A.M. Shatry M. Jones R.B. Levy The effect of the spleen on compartmental levels and distribution of donor progenitor cells after syngeneic and allogeneic bone marrow transplants Stem Cells Dev 13 2004 51-62
38. G. Dennert C.G. Anderson J. Warner T-killer cells play a role in allogeneic bone-marrow graft-rejection but not in hybrid resistance J Immunol 135 1985 3729-3734
39. C. Scheffold Y.C. Scheffold T.M. Cao J. Gworek J.A. Shizuru Cytokines and cytotoxic pathways in engraftment resistance to purified allogeneic hematopoietic stem cells Biol Blood Marrow Transplant 11 2005 1-12
40. G. Cudkowicz M. Bennett Peculiar immunobiology of bone marrow allografts. I. Graft rejection by irradiated responder mice J Exp Med 134 1971 83-102
41. R. Kiessling P.S. Hochman O. Haller G.M. Shearer H. Wigzell G. Cudkowicz Evidence for a similar or common mechanism for natural killer cell activity and resistance to hemopoietic grafts Eur J Immunol 7 1977 655-663
42. I. Barao W.J. Murphy The immunobiology of natural killer cells and bone marrow allograft rejection Biol Blood Marrow Transplant 9 2003 727-741
43. N.S. Liao M. Bix M. Zijlstra R. Jaenisch D. Raulet MHC class I deficiency: Susceptibility to natural killer (NK) cells and impaired NK activity Science 253 1991 199-202
44. H.G. Ljunggren K. Karre In search of the 'missing self' MHC molecules and NK cell recognition Immunol Today 11 1990 237-244
45. S.K. Anderson J.R. Ortaldo D.W. McVicar The ever-expanding Ly49 gene family: Repertoire and signaling Immunol Rev 181 2001 79-89
46. F.H. McLaren C.N. Svendsen P. Van der Meide E. Joly Analysis of neural stem cells by flow cytometry: Cellular differentiation modifies patterns of MHC expression J Neuroimmunol 112 2001 35-46
47. M. Modo K. Mellodew P. Rezaie In vitro expression of major histocompatibility class I and class II antigens by conditionally immortalized murine neural stem cells Neurosci Lett 337 2003 85-88
48. M. Mammolenti S. Gajavelli P. Tsoulfas R. Levy Absence of major histocompatibility complex class I on neural stem cells does not permit natural killer cell killing and prevents recognition by alloreactive cytotoxic T lymphocytes in vitro Stem Cells 22 2004 1101-1110
49. M. Drukker G. Katz A. Urbach et al. Characterization of the expression of MHC proteins in human embryonic stem cells Proc Natl Acad Sci U S A 99 2002 9864-9869
50. A. Bartholomew C. Sturgeon M. Siatskas et al. Mesenchymal stem cells suppress lymphocyte proliferation in vitro and prolong skin graft survival in vivo Exp Hematol 30 2002 42-48
51. M. Krampera S. Glennie J. Dyson et al. Bone marrow mesenchymal stem cells inhibit the response of naive and memory antigen-specific T cells to their cognate peptide Blood 101 2003 3723-3729
52. I. Scott J. O'Shea M. Bunce et al. Molecular typing shows a high level of HLA class I incompatibility in serologically well matched donor/ patient pairs: Implications for unrelated bone marrow donor selection Blood 92 1998 4864-4871
53. L. Ruggeri M. Capanni E. Urbani et al. Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants Science 295 2002 2097-2100
54. C. Koenecke J. Shaffer S.I. Alexander et al. NK cell recovery, chimerism, function and recognition in recipients of haploidentical hematopoietic cell transplantation following nonmyeloablative conditioning using a humanized anti-CD2 mAb, Medi-507 Exp Hematol 31 2003 911-923
55. J.D. Young H. Hengartner E.R. Podack Z.A. Cohn Purification and characterization of a cytolytic pore-forming protein from granules of cloned lymphocytes with natural killer activity Cell 44 1986 849-859
56. H. Arase N. Arase T. Saito Fas-mediated cytotoxicity by freshly isolated natural-killer-cells J Exp Med 181 1995 1235-1238
57. D. Kagi B. Ledermann K. Burki et al. Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforin-deficient mice Nature 369 1994 31-37
58. Y. Oshimi S. Oda Y. Honda S. Nagata S. Miyazaki Involvement of Fas ligand and Fas-mediated pathway in the cytotoxicity of human natural killer cells J Immunol 157 1996 2909-2915
59. N. Kayagaki N. Yamaguchi M. Nakayama et al. Expression and function of TNF-related apoptosis-inducing ligand on murine activated NK cells J Immunol 163 1999 1906-1913
60. G. Degliantoni M. Murphy M. Kobayashi M.K. Francis B. Perussia G. Trinchieri Natural killer (NK) cell-derived hematopoietic colony-inhibiting activity and NK cytotoxic factor. Relationship with tumor necrosis factor and synergism with immune interferon J Exp Med 162 1985 1512-1530
61. A. Thorburn Death receptor-induced cell killing Cell Signal 16 2004 139-144
62. J. Maciejewski C. Selleri S. Anderson N.S. Young Fas Antigen expression on CD34(+) human marrow-cells is induced by interferon-gamma and tumor-necrosis-factor-alpha and potentiates cytokine-mediated hematopoietic suppression in-vitro Blood 85 1995 3183-3190
63. T. Sato C. Selleri N.S. Young J.P. Maciejewski Hematopoietic inhibition by interferon-gamma is partially mediated through interferon regulatory factor-I Blood 86 1995 3373-3380
64. V.M. Eng B.D. Car B. Schnyder et al. The stimulatory effects of interleukin (IL)-12 on hematopoiesis are antagonized by IL-12-induced interferon-gamma in-vivo J Exp Med 181 1995 1893-1898
65. H.W. Snoeck S. Weekx A. Moulijn et al. Tumor necrosis factor alpha is a potent synergistic factor for the proliferation of primitive human hematopoietic progenitor cells and induces resistance to transforming growth factor beta but not to interferon gamma J Exp Med 183 1996 705-710
66. Y. Kawano Y. Takaue A. Hirao et al. Synergy among erythropoietin, interleukin-3, stem-cell factor (C-Kit ligand) and interferon-gamma on early human hematopoiesis Stem Cells 12 1994 514-520
67. P. Allavena G. Scala J.Y. Djeu et al. Production of multiple cytokines by clones of human large granular lymphocytes Cancer Immunol Immunother 19 1985 121-126
68. W.J. Murphy J.R. Keller C.L. Harrison H.A. Young D.L. Longo Interleukin-2-activated natural-killer-cells can support hematopoiesis in vitro and promote marrow engraftment in vivo Blood 80 1992 670-677
69. H. Cui S.T. Ju D.H. Sherr Functional expression of Fas (CD95) protein in autoimmune lpr mice Cell Immunol 174 1996 35-41
70. T. Lapidot Y. Faktorowich I. Lubin Y. Reisner Enhancement of T-cell-depleted bone marrow allografts in the absence of graft-versus-host disease is mediated by CD8+ CD4- and not by CD8- CD4+ thymocytes Blood 80 1992 2406-2411
71. E. Bachar-Lustig N. Rachamim H.W. Li F. Lan Y. Reisner Megadose of T cell-depleted bone marrow overcomes MHC barriers in sublethally irradiated mice Nat Med 1 1995 1268-1273
72. R. Storb H.J. Deeg F.R. Applebaum et al. Failure of anti-Ia monoclonal antibody to abrogate transfusion-induced sensitization and prevent marrow graft rejection in DLA-identical canine littermates Transplantation 45 1988 505-506
73. R. Storb H.J. Deeg Failure of allogeneic canine marrow grafts after total-body irradiation. Allogeneic "resistance" versus transfusion-induced sensitization Transplantation 42 1986 571-580
74. N.A. Kernan N. Flomenberg B. Dupont R.J. O'Reilly Graft rejection in recipients of T-cell-depleted HLA-nonidentical marrow transplants for leukemia. Identification of host-derived antidonor allocytotoxic T lymphocytes Transplantation 43 1987 842-847
75. K. Fleischhauer N.A. Kernan R.J. O'Reilly B. Dupont S.Y. Yang Bone marrow-allograft rejection by T lymphocytes recognizing a single amino acid difference in HLA-B44 N Engl J Med 323 1990 1818-1822
76. W.A.F. Marijt N.A. Kernan T. Diazbarrientos et al. Multiple minor histocompatibility antigen-specific cytotoxic T-lymphocyte clones can be generated during graft-rejection after HLA-identical bone-marrow transplantation Bone Marrow Transplant 16 1995 125-132
77. K. Fleischhauer E. Zino B. Mazzi et al. Peripheral blood stem cell allograft rejection mediated by CD4(+) T lymphocytes recognizing a single mismatch at HLA-DP beta 1*0901 Blood 98 2001 1122-1126
78. W.A. Marijt W.F. Veenhof E. Goulmy R. Willemze J.J. van Rood J.H. Falkenburg Minor histocompatibility antigens HA-1-, -2-, and -4-, and HY-specific cytotoxic T-cell clones inhibit human hematopoietic progenitor cell growth by a mechanism that is dependent on direct cell-cell contact Blood 82 1993 3778-3785
79. R. Storb R.B. Epstein R.H. Rudolph E.D. Thomas The effect of prior transfusion on marrow grafts between histocompatible canine siblings J Immunol 105 1970 627-633
80. R. Storb R.H. Rudolph T.C. Graham E.D. Thomas The influence of transfusions from unrelated donors upon marrow grafts between histocompatible canine siblings J Immunol 107 1971 409-413
81. R. Storb C.D. Buckner A. Fefer et al. Marrow transplantation in aplastic anemia Transplant Proc 6 1974 355-358
82. H.J. Deeg H.M. Shulman E. Schmidt G.C. Yee E.D. Thomas R. Storb Marrow graft rejection and veno-occlusive disease of the liver in patients with aplastic anemia conditioned with cyclophosphamide and cyclosporine Transplantation 42 1986 497-501
83. R. Storb R.L. Prentice E.D. Thomas Marrow transplantation for treatment of aplastic anemia. An analysis of factors associated with graft rejection N Engl J Med 296 1977 61-66
84. R. Storb E.D. Thomas C.D. Buckner et al. Marrow transplantation in thirty "untransfused" patients with severe aplastic anemia Ann Intern Med 92 1980 30-36
85. R. Storb R.L. Prentice E.D. Thomas et al. Factors associated with graft rejection after HLA-identical marrow transplantation for aplastic anaemia Br J Haematol 55 1983 573-585
86. R. Parkman J. Rappeport B. Camitta R.H. Levey D.G. Nathan Successful use of multiagent immunosuppression in the bone marrow transplantation of sensitized patients Blood 52 1978 1163-1169
87. R.E. Champlin M.M. Horowitz D.W. van Bekkum et al. Graft failure following bone marrow transplantation for severe aplastic anemia: Risk factors and treatment results Blood 73 1989 606-613
88. T.P. Loughran R. Storb Treatment of aplastic anemia Hematol Oncol Clin North Am 4 1990 559-575
89. N.K. Ramsay T.H. Kim P. McGlave et al. Total lymphoid irradiation and cyclophosphamide conditioning prior to bone marrow transplantation for patients with severe aplastic anemia Blood 62 1983 622-626
90. P. Levine R.E. Stetson Landmark article July 8, 1939. An unusual case of intra-group agglutination. By Philip Levine and Rufus E Stetson JAMA 251 1984 1316-1317
91. J.J. Van Rood J.G. Eernisse A. Van Leeuwen Leucocyte antibodies in sera from pregnant women Nature 181 1958 1735-1736
92. E. James J.G. Chai H. Dewchand E. Macchiarulo F. Dazzi E. Simpson Multiparity induces priming to male-specific minor histocompatibility antigen, HY, in mice and humans Blood 102 2003 388-393
93. W.A. Tekolf S. Shaw In vitro generation of cytotoxic cells specific for human minor histocompatibility antigens by lymphocytes from a normal donor potentially primed during pregnancy J Exp Med 157 1983 2172-2177
94. D.P. Singal Y.J. Wadia N. Naipaul In vitro cell-mediated cytotoxicity to the male specific (H-Y) antigen in man Hum Immunol 2 1981 45-53
95. T. Mutis G. Gillespie E. Schrama J.H. Falkenburg P. Moss E. Goulmy Tetrameric HLA class I-minor histocompatibility antigen peptide complexes demonstrate minor histocompatibility antigen-specific cytotoxic T lymphocytes in patients with graft-versus-host disease Nat Med 5 1999 839-842
96. L. Komlos D. Vardimon J. Notmann et al. Role of children's sex in mixed mother-child lymphocyte culture reactivity Am J Reprod Immunol 22 1990 4-8
97. R.M. Verdijk A. Kloosterman J. Pool et al. Pregnancy induces minor histocompatibility antigen-specific cytotoxic T cells: Implications for stem cell transplantation and immunotherapy Blood 103 2004 1961-1964
98. Gratwohl H. Baldomero L. John et al. Peripheral blood pressure cells transplants across a major histocompatibility barrier in rabbits: positive effects of a higher number of precursor cells? Acta Haematol 95 1996 176-180
99. A.B. Adams M.A. Williams T.R. Jones et al. Heterologous immunity provides a potent barrier to transplantation tolerance J Clin Invest 111 2003 1887-1895
100. H. Yang R.M. Welsh Induction of allospecific and virus-specific memory cytotoxic T cells during acute arenavirus infections Med Microbiol Immunol (Berl) 175 1986 137-139
101. H. Yang R.M. Welsh Induction of alloreactive cytotoxic T cells by acute virus infection of mice J Immunol 136 1986 1186-1193
102. R. Finberg H. Cantor B. Benacerraf S. Burakoff S. The origins of alloreactivity differentiation of prekiller cells to viral infection results in alloreactive cytolytic T lymphocytes J Immunol 124 1980 1858-1860
103. C.A. London M.P. Lodge A.K. Abbas Functional responses and costimulator dependence of memory CD4+ T cells J Immunol 164 2000 265-272
104. H. Nakamura R.E. Gress Graft-rejection by cytolytic T-cells-specificity of the effector mechanism in the rejection of allogeneic marrow Transplantation 49 1990 453-458
105. L. Luznik L.W. Engstrom R. Iannone E.J. Fuchs Posttransplantation cyclophosphamide facilitates engraftment of major histocompatibility complex-identical allogeneic marrow in mice conditioned with low-dose total body irradiation Biol Blood Marrow Transplant 8 2002 131-138
106. S.J. Baker E.P. Reddy Transducers of life and death: TNF receptor superfamily and associated proteins Oncogene 12 1996 1-9
107. A.M. Chinnaiyan K. O'Rourke G.L. Yu et al. Signal transduction by DR3, a death domain-containing receptor related to TNFR-1 and CD95 Science 274 1996 990-992
108. T.S. Migone J. Zhang X. Luo et al. TL1A is a TNF-like ligand for DR3 and TR6/DcR3 and functions as a T cell costimulator Immunity 16 2002 479-492
109. M.J. Kaplan E.E. Lewis E.A. Shelden et al. The apoptotic ligands TRAIL, TWEAK, and Fas ligand mediate monocyte death induced by autologous lupus T cells J Immunol 169 2002 6020-6029
110. M. Nakayama N. Harada K. Okumura H. Yagita Characterization of murine TWEAK and its receptor (Fn14) by monoclonal antibodies Biochem Biophys Res Commun 306 2003 819-825
111. M. Nakayama K. Ishidoh Y. Kojima et al. Fibroblast growth factor-inducible 14 mediates multiple pathways of TWEAK-induced: Cell death J Immunol 170 2003 341-348
112. M.J. Kaplan D. Ray R.L. Yung B.C. Richardson Trail and tweak mediate antigen specific and autoreactive macrophage killing by D10 cells [abstract] FASEB J 14 2000 A554
113. J.A. Madrigal I. Scott R. Arguello R. Szydlo A.M. Little J.M. Goldman Factors influencing the outcome of bone marrow transplants using unrelated donors Immunol Rev 157 1997 153-166
114. M.A. Nolte R. Arens R. van Os et al. Immune activation modulates hematopoiesis through interactions between CD27 and CD70 Nat Immunol 6 2005 412-418
115. R.Q. Hintzen S.M. Lens M.P. Beckmann R.G. Goodwin D. Lynch R.A. van Lier Characterization of the human CD27 ligand, a novel member of the TNF gene family J Immunol 152 1994 1762-1773
116. R.P. Bourette P. De Sepulveda S. Arnaud P. Dubreuil R. Rottapel G. Mouchiroud Suppressor of cytokine signaling 1 interacts with the macrophage colony-stimulating factor receptor and negatively regulates its proliferation signal J Biol Chem 276 2001 22133-22139
117. Y. Du S. Tsai J.R. Keller S.C. Williams Identification of an interleukin-3-regulated aldoketo reductase gene in myeloid cells which may function in autocrine regulation of myelopoiesis J Biol Chem 275 2000 6724-6732
118. R. Watanabe-Fukunaga C.I. Brannan N.G. Copeland N.A. Jenkins S. Nagata Lymphoproliferation disorder in mice explained by defects in Fas antigen that mediates apoptosis Nature 356 1992 314-317