TCR-independent killing of B cell malignancies by anti-third-party CTLs: The critical role of MHC-CD8 engagement

Journal of Immunology

Volumn 187, Issue 4, 2011, Pages 2006-2014

  Lask, Assaf ^a   Goichberg, Polina ^a   Cohen, Adva ^a   Goren Arbel, Rinat ^a   Milstein, Oren ^a   Aviner, Shraga ^a   Feine, Ilan ^a   Ophir, Eran ^a   Reich Zeliger, Shlomit ^a   Hagin, David ^a   Klein, Tirza ^b   Nagler, Arnon ^c   Berrebi, Alain ^d   Reisner, Yair ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b RABIN MEDICAL CENTER   (Israel)

^c SHEBA MEDICAL CENTER   (Israel)

^d KAPLAN MEDICAL CENTER   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CD8 ANTIGEN; INTERCELLULAR ADHESION MOLECULE 1; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; T LYMPHOCYTE RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTI THIRD PARTY CYTOTOXIC T LYMPHOCYTE; ANTIGEN BINDING; APOPTOSIS; ARTICLE; B LYMPHOCYTE; CELL KILLING; CELL MUTANT; CONJUGATION; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DAUDI CELL; FEMALE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LYMPHOMA CELL; MOUSE; NONHODGKIN LYMPHOMA; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING;

ANIMALS; ANTIGENS, CD8; APOPTOSIS; B-LYMPHOCYTES; CELL LINE, TUMOR; FEMALE; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; IMMUNITY, CELLULAR; INTERCELLULAR ADHESION MOLECULE-1; LYMPHOCYTE FUNCTION-ASSOCIATED ANTIGEN-1; LYMPHOMA, B-CELL; MALE; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; MICE, SCID; MUTATION; T-LYMPHOCYTES, CYTOTOXIC;

EID: 80051924951     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1100095     Document Type: Article

References (47)

1. Bachar-Lustig, E., S. Reich-Zeliger, H. Gur, Y. Zhao, R. Krauthgamer, and Y. Reisner. 2001. Bone marrow transplantation across major genetic barriers: The role of megadose stem cells and nonalloreactive donor anti-third party CTLS. Transplant. Proc. 33: 2099-2100. (Pubitemid 33762647)
2. Bachar-Lustig, E., S. Reich-Zeliger, and Y. Reisner. 2003. Anti-third-party veto CTLs overcome rejection of hematopoietic allografts: Synergism with rapamycin and BM cell dose. Blood 102: 1943-1950. (Pubitemid 37122364)
3. Aviner, S., X. Yao, R. Krauthgamer, Y. Gan, R. Goren-Arbel, T. Klein, A. Tabilio, J. D. McMannis, R. Champlin, M. F. Martelli, et al. 2005. Large-scale preparation of human anti-third-party veto cytotoxic T lymphocytes depleted of graft-versus-host reactivity: A new source for graft facilitating cells in bone marrow transplantation. Hum. Immunol. 66: 644-652. (Pubitemid 40922553)
4. Reich-Zeliger, S., Y. Zhao, R. Krauthgamer, E. Bachar-Lustig, and Y. Reisner. 2000. Anti-third party CD8+ CTLs as potent veto cells: Coexpression of CD8 and FasL is a prerequisite. Immunity 13: 507-515.
5. Milstein, O., D. Hagin, A. Lask, S. Reich-Zeliger, E. Shezen, E. Ophir, Y. Eidelstein, R. Afik, Y. E. Antebi, M. L. Dustin, and Y. Reisner. 2011. CTLs respond with activation and granule secretion when serving as targets for T-cell recognition. Blood 117: 1042-1052.
6. Arditti, F. D., S. Aviner, B. Dekel, R. Krauthgamer, J. Gan, A. Nagler, A. Tabilio, M. Martelli, A. Berrebi, and Y. Reisner. 2005. Eradication of B-CLL by autologous and allogeneic host nonreactive anti-third-party CTLs. Blood 105: 3365-3371.
7. Agrawal, S., and M. C. Kishore. 2000. MHC class I gene expression and regulation. J. Hematother. Stem Cell Res. 9: 795-812. (Pubitemid 32110279)
8. König, R. 2002. Interactions between MHC molecules and co-receptors of the TCR. Curr. Opin. Immunol. 14: 75-83. (Pubitemid 34085109)
9. Gao, G. F., and B. K. Jakobsen. 2000. Molecular interactions of coreceptor CD8 and MHC class I: The molecular basis for functional coordination with the T-cell receptor. Immunol. Today 21: 630-636. (Pubitemid 32044020)
10. Skov, S., P. Klausen, and M. H. Claesson. 1997. Ligation of major histocompatability complex (MHC) class I molecules on human T cells induces cell death through PI-3 kinase-induced c-Jun NH2-terminal kinase activity: A novel apoptotic pathway distinct from Fas-induced apoptosis. J. Cell Biol. 139: 1523-1531. (Pubitemid 28013672)
11. Skov, S., S. Bregenholt, and M. H. Claesson. 1997. MHC class I ligation of human T cells activates the ZAP70 and p56lck tyrosine kinases, leads to an alternative phenotype of the TCR/CD3 zeta-chain, and induces apoptosis. J. Immunol. 158: 3189-3196. (Pubitemid 127484033)
12. Pedersen, A. E., S. Bregenholt, B. Johansen, S. Skov, and M. H. Claesson. 1999. MHC-I-induced apoptosis in human B-lymphoma cells is dependent on protein tyrosine and serine/threonine kinases. Exp. Cell Res. 251: 128-134. (Pubitemid 29406526)
13. Rubio, G., X. Férez, M. Sánchez-Campillo, J. Gálvez, S. Martí, R. Verdú, T. Hernández-Caselles, and P. García-Peñarrubia. 2004. Cross-linking of MHC class I molecules on human NK cells inhibits NK cell function, segregates MHC I from the NK cell synapse, and induces intracellular phosphotyrosines. J. Leukoc. Biol. 76: 116-124. (Pubitemid 38857178)
14. Gur, H., F. el-Zaatari, T. D. Geppert, M. C. Wacholtz, J. D. Taurog, and P. E. Lipsky. 1990. Analysis of T cell signaling by class I MHC molecules: The cytoplasmic domain is not required for signal transduction. J. Exp. Med. 172: 1267-1270. (Pubitemid 20343229)
15. Gur, H., T. D. Geppert, M. C. Wacholtz, and P. E. Lipsky. 1999. The cytoplasmic and the transmembrane domains are not sufficient for class I MHC signal transduction. Cell. Immunol. 191: 105-116. (Pubitemid 29091844)
16. Tector, M., Q. Zhang, and R. D. Salter. 1997. Beta 2-microglobulin and calnexin can independently promote folding and disulfide bond formation in class I histocompatibility proteins. Mol. Immunol. 34: 401-408. (Pubitemid 27368336)
17. Demaria, S., L. D. DeVito-Haynes, R. D. Salter, W. J. Burlingham, and Y. Bushkin. 1999. Peptide-conformed beta2m-free class I heavy chains are intermediates in generation of soluble HLA by the membrane-bound metalloproteinase. Hum. Immunol. 60: 1216-1226. (Pubitemid 30017504)
18. Baxter, T. K., S. J. Gagnon, R. L. Davis-Harrison, J. C. Beck, A. K. Binz, R. V. Turner, W. E. Biddison, and B. M. Baker. 2004. Strategic mutations in the class I major histocompatibility complex HLA-A2 independently affect both peptide binding and T cell receptor recognition. J. Biol. Chem. 279: 29175-29184. (Pubitemid 38915791)
19. Aiuti, A., I. J. Webb, C. Bleul, T. Springer, and J. C. Gutierrez-Ramos. 1997. The chemokine SDF-1 is a chemoattractant for human CD34+ hematopoietic progenitor cells and provides a new mechanism to explain the mobilization of CD34+ progenitors to peripheral blood. J. Exp. Med. 185: 111-120. (Pubitemid 27039446)
20. Hauss, P., F. Selz, and A. Fischer. 1996. Comparative analysis of CD4-mediated down-regulation of T cell adhesion to B cells by flow cytometry and fluorescence microscopy. Cytometry 23: 39-47.
21. Koopman, G., C. P. Reutelingsperger, G. A. Kuijten, R. M. Keehnen, S. T. Pals, and M. H. Van Oers. 1994. Annexin V for flow cytometric detection of phosphatidylserine expression on B cells undergoing apoptosis. Blood 84: 1415-1420. (Pubitemid 24273007)
22. Yustein, J. T., and C. V. Dang. 2007. Biology and treatment of Burkitt's lymphoma. Curr. Opin. Hematol. 14: 375-381. (Pubitemid 46842812)
23. Martin, P., A. Chadburn, P. Christos, R. Furman, J. Ruan, M. A. Joyce, E. Fusco, P. Glynn, R. Elstrom, R. Niesvizky, et al. 2008. Intensive treatment strategies may not provide superior outcomes in mantle cell lymphoma: overall survival exceeding 7 years with standard therapies. Ann. Oncol. 19: 1327-1330.
24. Gagnon, S. J., O. Y. Borbulevych, R. L. Davis-Harrison, T. K. Baxter, J. R. Clemens, K. M. Armstrong, R. V. Turner, M. Damirjian, W. E. Biddison, and B. M. Baker. 2005. Unraveling a hotspot for TCR recognition on HLA-A2: Evidence against the existence of peptide-independent TCR binding determinants. J. Mol. Biol. 353: 556-573. (Pubitemid 41417737)
25. Matsui, M., C. E. Hioe, and J. A. Frelinger. 1993. Roles of the six peptide-binding pockets of the HLA-A2 molecule in allorecognition by human cytotoxic T-cell clones. Proc. Natl. Acad. Sci. USA 90: 674-678. (Pubitemid 23028926)
26. Kim, K. J., C. Kanellopoulos-Langevin, R. M. Merwin, D. H. Sachs, and R. Asofsky. 1979. Establishment and characterization of BALB/c lymphoma lines with B cell properties. J. Immunol. 122: 549-554.
27. Good, K. L., D. T. Avery, and S. G. Tangye. 2009. Resting human memory B cells are intrinsically programmed for enhanced survival and responsiveness to diverse stimuli compared to naive B cells. J. Immunol. 182: 890-901.
28. Sambhara, S. R., and R. G. Miller. 1991. Programmed cell death of T cells signaled by the T cell receptor and the alpha 3 domain of class I MHC. Science 252: 1424-1427. (Pubitemid 21917060)
29. Reich-Zeliger, S., J. Gan, E. Bachar-Lustig, and Y. Reisner. 2004. Tolerance induction by veto CTLs in the TCR transgenic 2C mouse model. II. Deletion of effector cells by Fas-Fas ligand apoptosis. J. Immunol. 173: 6660-6666. (Pubitemid 39541050)
30. Somersalo, K., N. Anikeeva, T. N. Sims, V. K. Thomas, R. K. Strong, T. Spies, T. Lebedeva, Y. Sykulev, and M. L. Dustin. 2004. Cytotoxic T lymphocytes form an antigen-independent ring junction. J. Clin. Invest. 113: 49-57. (Pubitemid 38541631)
31. Purbhoo, M. A., D. J. Irvine, J. B. Huppa, and M. M. Davis. 2004. T cell killing does not require the formation of a stable mature immunological synapse. Nat. Immunol. 5: 524-530. (Pubitemid 38660465)
32. De Fougerolles, A. R., S. A. Stacker, R. Schwarting, and T. A. Springer. 1991. Characterization of ICAM-2 and evidence for a third counter-receptor for LFA-1. J. Exp. Med. 174: 253-267.
33. Dustin, M. L., R. Rothlein, A. K. Bhan, C. A. Dinarello, and T. A. Springer. 1986. Induction by IL 1 and interferon-gamma: Tissue distribution, biochemistry, and function of a natural adherence molecule (ICAM-1). J. Immunol. 137: 245-254. (Pubitemid 16100296)
34. Pedersen, A. E., S. Bregenholt, S. Skov, M. L. Vrang, and M. H. Claesson. 1998. Protein tyrosine kinases p53/56lyn and p72syk in MHC class I-mediated signal transduction in B lymphoma cells. Exp. Cell Res. 240: 144-150. (Pubitemid 28366618)
35. Woodle, E. S., D. M. Smith, J. A. Bluestone, W. M. Kirkman, III, D. R. Green, and E. W. Skowronski. 1997. Anti-human class I MHC antibodies induce apoptosis by a pathway that is distinct from the Fas antigen-mediated pathway. J. Immunol. 158: 2156-2164. (Pubitemid 127469998)
36. Wallén-Ohman, M., and C. A. Borrebaeck. 1994. A cell surface antigen (BAL) defined by a mouse monoclonal antibody inducing apoptosis in a human lymphocytic leukemia cell line. Int. J. Cancer 57: 544-552. (Pubitemid 24173101)
37. Yang, J., J. Qian, M. Wezeman, S. Wang, P. Lin, M. Wang, S. Yaccoby, L. W. Kwak, B. Barlogie, and Q. Yi. 2006. Targeting beta2-microglobulin for induction of tumor apoptosis in human hematological malignancies. Cancer Cell 10: 295-307. (Pubitemid 44512192)
38. Yang, J., X. Zhang, J. Wang, J. Qian, L. Zhang, M. Wang, L. W. Kwak, and Q. Yi. 2007. Anti beta2-microglobulin monoclonal antibodies induce apoptosis in myeloma cells by recruiting MHC class I to and excluding growth and survival cytokine receptors from lipid rafts. Blood 110: 3028-3035. (Pubitemid 350006957)
39. Amirayan, N., E. Furrie, F. Deleuil, A. Mellor, L. Leserman, and P. Machy. 1995. Influence of MHC class I molecules on T-cell proliferation induced by CD3 or Thy-1 stimulation. Immunology 86: 71-78.
40. Lapidot, T., A. Terenzi, T. S. Singer, O. Salomon, and Y. Reisner. 1989. Enhancement by dimethyl myleran of donor type chimerism in murine recipients of bone marrow allografts. Blood 73: 2025-2032. (Pubitemid 19145141)
41. Bachar-Lustig, E., N. Rachamim, H. W. Li, F. Lan, and Y. Reisner. 1995. Megadose of T cell-depleted bone marrow overcomes MHC barriers in sublethally irradiated mice. Nat. Med. 1: 1268-1273.
42. Pedrazzini, A., A. S. Freedman, J. Andersen, L. Heflin, K. Anderson, T. Takvorian, G. P. Canellos, J. Whitman, F. Coral, J. Ritz, et al. 1989. Anti-Bcell monoclonal antibody-purged autologous bone marrow transplantation for Bcell non-Hodgkin's lymphoma: Phenotypic reconstitution and B-cell function. Blood 74: 2203-2211. (Pubitemid 19269131)
43. Kasamon, Y. L., R. J. Jones, R. A. Brodsky, E. J. Fuchs, W. Matsui, L. Luznik, J. D. Powell, A. L. Blackford, A. Goodrich, C. D. Gocke, et al. 2010. Immunologic recovery following autologous stem-cell transplantation with pre- and posttransplantation rituximab for low-grade or mantle cell lymphoma. Ann. Oncol. 21: 1203-1210.
44. Van Besien, K., F. R. Loberiza, Jr., R. Bajorunaite, J. O. Armitage, A. Bashey, L. J. Burns, C. O. Freytes, J. Gibson, M. M. Horowitz, D. J. Inwards, et al. 2003. Comparison of autologous and allogeneic hematopoietic stem cell transplantation for follicular lymphoma. Blood 102: 3521-3529. (Pubitemid 37409366)
45. Verdonck, L. F., A. W. Dekker, H. M. Lokhorst, E. J. Petersen, and H. K. Nieuwenhuis. 1997. Allogeneic versus autologous bone marrow transplantation for refractory and recurrent low-grade non-Hodgkin's lymphoma. Blood 90: 4201-4205. (Pubitemid 27484077)
46. Glass, B., M. Nickelsen, P. Dreger, A. Claviez, J. Hasenkamp, G. Wulf, L. Trümper, and N. Schmitz. 2004. Reduced-intensity conditioning prior to allogeneic transplantation of hematopoietic stem cells: The need for T cells early after transplantation to induce a graft-versus-lymphoma effect. Bone Marrow Transplant. 34: 391-397. (Pubitemid 39232367)
47. Morris, E., K. Thomson, C. Craddock, P. Mahendra, D. Milligan, G. Cook, G. M. Smith, A. Parker, S. Schey, R. Chopra, et al. 2004. Outcomes after alemtuzumab-containing reduced-intensity allogeneic transplantation regimen for relapsed and refractory non-Hodgkin lymphoma. Blood 104: 3865-3871. (Pubitemid 39620131)