Recipient expression of ligands for donor inhibitory KIRs enhances NK-cell function to control leukemic relapse after haploidentical transplantation

European Journal of Immunology

Volumn 45, Issue 8, 2015, Pages 2396-2408

  Zhao, Xiang Yu ^a   Chang, Ying Jun ^a   Zhao, Xiao Su ^a   Xu, Lan Ping ^a   Zhang, Xiao Hui ^a   Liu, Kai Yan ^a   Li, Dan ^a   Huang, Xiao Jun ^a,b  

^a PEKING UNIVERSITY PEOPLE S HOSPITAL   (China)

^b Tsinghua University   (China)

Author keywords

Haploidentica; HSCT; KIR; Leukemia; NK cells; T cell replete

Indexed keywords

CD107 ALPHA PROTEIN; GAMMA INTERFERON; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR; LIGAND; PROTEIN; UNCLASSIFIED DRUG; IFNG PROTEIN, HUMAN; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1;

ADOLESCENT; ADULT; ARTICLE; CHILD; COHORT ANALYSIS; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOMEGALOVIRUS INFECTION; CYTOTOXICITY; DISEASE FREE SURVIVAL; DISEASE SEVERITY; FEMALE; FOLLOW UP; HLA SYSTEM; HUMAN; HUMAN CELL; K562 CELL LINE; LEUKEMIA CELL; LEUKEMIA RELAPSE; LONGITUDINAL STUDY; LYMPHATIC LEUKEMIA; LYMPHOCYTE FUNCTION; MAJOR CLINICAL STUDY; MALE; MORTALITY; MYELOID LEUKEMIA; NATURAL KILLER CELL; OVERALL SURVIVAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RECURRENCE RISK; STEM CELL TRANSPLANTATION; UVEITIS; VIRUS REACTIVATION; ALLOGRAFT; CASE CONTROL STUDY; CLINICAL TRIAL; GENE EXPRESSION REGULATION; IMMUNOLOGY; LEUKEMIA; MIDDLE AGED; PATHOLOGY; PROSPECTIVE STUDY; RECURRENT DISEASE;

ADOLESCENT; ADULT; ALLOGRAFTS; CASE-CONTROL STUDIES; CHILD; FEMALE; GENE EXPRESSION REGULATION, LEUKEMIC; HUMANS; INTERFERON-GAMMA; K562 CELLS; KILLER CELLS, NATURAL; LEUKEMIA; LYSOSOMAL-ASSOCIATED MEMBRANE PROTEIN 1; MALE; MIDDLE AGED; PROSPECTIVE STUDIES; RECEPTORS, KIR; RECURRENCE; STEM CELL TRANSPLANTATION;

EID: 84938988549     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201445057     Document Type: Article

References (42)

1. Parham, P. and McQueen, K. L., Alloreactive killer cells: hindrance and help for haematopoietic transplants. Nat. Rev. Immunol. 2003. 3: 108-122.
2. Ruggeri, L., Capanni, M., Urbani, E., Perruccio, K., Shlomchik, W. D., Tosti, A., Posati, S. et al., Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science 2002. 295: 2097-2100.
3. Leung, W., Iyengar, R., Turner, V., Lang, P., Bader, P., Conn, P., Niethammer, D. and Handgretinger, R., Determinants of antileukemia effects of allogeneic NK cells. J. Immunol. 2004. 172: 644-650.
4. Ruggeri, L., Capanni, M., Casucci, M., Volpi, I., Tosti, A., Perruccio, K., Urbani, E. et al., Role of natural killer cell alloreactivity in HLA-mismatched hematopoietic stem cell transplantation. Blood 1999. 94: 333-339.
5. Ruggeri, L., Mancusi, A., Capanni, M., Urbani, E., Carotti, A., Aloisi, T., Stern, M. et al., Donor natural killer cell allorecognition of missing self in haploidentical hematopoietic transplantation for acute myeloid leukemia: challenging its predictive value. Blood 2007. 110: 433-440.
6. Zhao, X. Y., Chang, Y. J. and Huang, X. J., Conflicting impact of alloreactive NK cells on transplantation outcomes after haploidentical transplantation: do the reconstitution kinetics of natural killer cells create these differences? Biol. Blood Marrow Transplant. 2011. 17: 1436-1442.
7. Zhao, X. Y., Huang, X. J., Liu, K. Y., Xu, L. P. and Liu, D. H., Reconstitution of natural killer cell receptor repertoires after unmanipulated HLA-mismatched/haploidentical blood and marrow transplantation: analyses of CD94:NKG2A and killer immunoglobulin-like receptor expression and their associations with clinical outcome. Biol. Blood Marrow Transplant. 2007. 13: 734-744.
8. Pfeiffer, M. M., Feuchtinger, T., Teltschik, H. M., Schumm, M., Muller, I., Handgretinger, R. and Lang, P., Reconstitution of natural killer cell receptors influences natural killer activity and relapse rate after haploidentical transplantation of T- and B-cell depleted grafts in children. Haematologica 2010. 95: 1381-1388.
9. Triplett, B. M., Horwitz, E. M., Iyengar, R., Turner, V., Holladay, M. S., Gan, K., Behm, F. G. et al., Effects of activating NK cell receptor expression and NK cell reconstitution on the outcomes of unrelated donor hematopoietic cell transplantation for hematologic malignancies. Leukemia 2009. 23: 1278-1287.
10. Vago, L., Forno, B., Sormani, M. P., Crocchiolo, R., Zino, E., Di Terlizzi, S., Lupo Stanghellini. et al., Temporal, quantitative, and functional characteristics of single-KIR-positive alloreactive natural killer cell recovery account for impaired graft-versus-leukemia activity after haploidentical hematopoietic stem cell transplantation. Blood 2008. 112: 3488-3499.
11. Bjorklund, A. T., Schaffer, M., Fauriat, C., Ringden, O., Remberger, M., Hammarstedt, C., Barrett, A. J. et al., NK cells expressing inhibitory KIR for non-self-ligands remain tolerant in HLA-matched sibling stem cell transplantation. Blood 2010. 115: 2686-2694.
12. Yu, J., Venstrom, J. M., Liu, X. R., Pring, J., Hasan, R. S., O'Reilly, R. J. and Hsu, K. C., Breaking tolerance to self, circulating natural killer cells expressing inhibitory KIR for non-self HLA exhibit effector function after T cell-depleted allogeneic hematopoietic cell transplantation. Blood 2009. 113: 3875-3884.
13. Foley, B., Cooley, S., Verneris, M. R., Curtsinger, J., Luo, X., Waller, E. K., Weisdorf, D. J. and Miller, J. S., NK cell education after allogeneic transplantation: dissociation between recovery of cytokine-producing and cytotoxic functions. Blood 2011. 118: 2784-2792.
14. Huang, X. J., Liu, D. H., Liu, K. Y., Xu, L. P., Chen, H., Han, W., Chen, Y. H. et al., Haploidentical hematopoietic stem cell transplantation without in vitro T-cell depletion for the treatment of hematological malignancies. Bone Marrow Transplant. 2006. 38: 291-297.
15. Lu, D. P., Dong, L., Wu, T., Huang, X. J., Zhang, M. J., Han, W., Chen, H. et al., Conditioning including antithymocyte globulin followed by unmanipulated HLA-mismatched/haploidentical blood and marrow transplantation can achieve comparable outcomes with HLA-identical sibling transplantation. Blood 2006. 107: 3065-3073.
16. Wang, Y., Liu, D. H., Liu, K. Y., Xu, L. P., Zhang, X. H., Han, W., Chen, H. et al., Long-term follow-up of haploidentical hematopoietic stem cell transplantation without in vitro T cell depletion for the treatment of leukemia: nine years of experience at a single center. Cancer 2013. 119: 978-985.
17. Huang, X. J., Zhao, X. Y., Liu, D. H., Liu, K. Y. and Xu, L. P., Deleterious effects of KIR ligand incompatibility on clinical outcomes in haploidentical hematopoietic stem cell transplantation without in vitro T-cell depletion. Leukemia 2007. 21: 848-851.
18. Zhao, X. Y., Huang, X. J., Liu, K. Y., Xu, L. P. and Liu, D. H., Prognosis after unmanipulated HLA-haploidentical blood and marrow transplantation is correlated to the numbers of KIR ligands in recipients. Eur. J. Haematol. 2007. 78: 338-346.
19. Zhao, X. Y., Chang, Y. J., Xu, L. P., Zhang, X. H., Liu, K. Y., Li, D. and Huang, X. J., HLA and KIR genotyping correlates with relapse after T-cell-replete haploidentical transplantation in chronic myeloid leukaemia patients. Br. J. Cancer 2014. 111: 1080-1088.
20. Miller, J. S. and Blazar, B. R., Control of acute myeloid leukemia relapse-dance between KIRs and HLA. N Engl J Med 2012. 367: 866-868.
21. Kim, S., Poursine-Laurent, J., Truscott, S. M., Lybarger, L., Song, Y. J., Yang, L., French, A. R. et al., Licensing of natural killer cells by host major histocompatibility complex class I molecules. Nature 2005. 436: 709-713.
22. Elliott, J. M., Wahle, J. A. and Yokoyama, W. M., MHC class I-deficient natural killer cells acquire a licensed phenotype after transfer into an MHC class I-sufficient environment. J. Exp. Med. 2010. 207: 2073-2079.
23. Hendricks, D. W., Balfour, H. H., Jr., Dunmire, S. K., Schmeling, D. O., Hogquist, K. A. and Lanier, L. L., Cutting Edge: NKG2ChiCD57+ NK cells respond specifically to acute infection with cytomegalovirus and not Epstein-Barr virus. J. Immunol. 2014. 192: 4492-4496.
24. Della Chiesa, M., Falco, M., Bertaina, A., Muccio, L., Alicata, C., Frassoni, F., Locatelli, F. et al., Human cytomegalovirus infection promotes rapid maturation of NK cells expressing activating killer Ig-like receptor in patients transplanted with NKG2C-/- umbilical cord blood. J. Immunol. 2014. 192: 1471-1479.
25. Charoudeh, H. N., Terszowski, G., Czaja, K., Gonzalez, A., Schmitter, K. and Stern, M., Modulation of the natural killer cell KIR repertoire by cytomegalovirus infection. Eur. J. Immunol. 2013. 43: 480-487.
26. Beziat, V., Liu, L. L., Malmberg, J. A., Ivarsson, M. A., Sohlberg, E., Bjorklund, A. T., Retiere, C. et al., NK cell responses to cytomegalovirus infection lead to stable imprints in the human KIR repertoire and involve activating KIRs. Blood 2013. 121: 2678-2688.
27. Foley, B., Cooley, S., Verneris, M. R., Pitt, M., Curtsinger, J., Luo, X., Lopez-Verges, S. et al., Cytomegalovirus reactivation after allogeneic transplantation promotes a lasting increase in educated NKG2C+ natural killer cells with potent function. Blood 2012. 119: 2665-2674.
28. Bjorkstrom, N. K., Riese, P., Heuts, F., Andersson, S., Fauriat, C., Ivarsson, M. A., Bjorklund, A. T. et al., Expression patterns of NKG2A, KIR, and CD57 define a process of CD56dim NK-cell differentiation uncoupled from NK-cell education. Blood 2010. 116: 3853-3864.
29. Kulkarni, S., Martin, M. P. and Carrington, M., The Yin and Yang of HLA and KIR in human disease. Semin. Immunol. 2008. 20: 343-352.
30. Yawata, M., Yawata, N., Draghi, M., Little, A. M., Partheniou, F. and Parham, P., Roles for HLA and KIR polymorphisms in natural killer cell repertoire selection and modulation of effector function. J. Exp. Med. 2006. 203: 633-645.
31. Elliott, J. M. and Yokoyama, W. M., Unifying concepts of MHC-dependent natural killer cell education. Trends Immunol. 2011. 32: 364-372.
32. Hsu, K. C., Keever-Taylor, C. A., Wilton, A., Pinto, C., Heller, G., Arkun, K., O'Reilly, R. J. et al., Improved outcome in HLA-identical sibling hematopoietic stem-cell transplantation for acute myelogenous leukemia predicted by KIR and HLA genotypes. Blood 2005. 105: 4878-4884.
33. Cooley, S., McCullar, V., Wangen, R., Bergemann, T. L., Spellman, S., Weisdorf, D. J. and Miller, J. S., KIR reconstitution is altered by T cells in the graft and correlates with clinical outcomes after unrelated donor transplantation. Blood 2005. 106: 4370-4376.
34. Bessoles, S., Angelov, G. S., Back, J., Leclercq, G., Vivier, E. and Held, W., Education of murine NK cells requires both cis and trans recognition of MHC class I molecules. J. Immunol. 2013. 191: 5044-5051.
35. Sungur, C. M., Tang-Feldman, Y. J., Zamora, A. E., Alvarez, M., Pomeroy, C. and Murphy, W. J., Murine NK-cell licensing is reflective of donor MHC-I following allogeneic hematopoietic stem cell transplantation in murine cytomegalovirus responses. Blood 2013. 122: 1518-1521.
36. Sungur, C. M., Tang-Feldman, Y. J., Ames, E., Alvarez, M., Chen, M., Longo, D. L., Pomeroy, C. et al., Murine natural killer cell licensing and regulation by T regulatory cells in viral responses. Proc. Natl. Acad. Sci. U S A 2013. 110: 7401-7406.
37. Orr, M. T., Murphy, W. J. and Lanier, L. L., 'Unlicensed' natural killer cells dominate the response to cytomegalovirus infection. Nat. Immunol. 2010. 11: 321-327.
38. Gardiner, C. M., Guethlein, L. A., Shilling, H. G., Pando, M., Carr, W. H., Rajalingam, R., Vilches, C. et al., Different NK cell surface phenotypes defined by the DX9 antibody are due to KIR3DL1 gene polymorphism. J. Immunol. 2001. 166: 2992-3001.
39. O'Connor, G. M., Guinan, K. J., Cunningham, R. T., Middleton, D., Parham, P. and Gardiner, C. M., Functional polymorphism of the KIR3DL1/S1 receptor on human NK cells. J. Immunol. 2007. 178: 235-241.
40. O'Connor, G. M., Vivian, J. P., Widjaja, J. M., Bridgeman, J. S., Gostick, E., Lafont, B. A., Anderson, S. K. et al., Mutational and structural analysis of KIR3DL1 reveals a lineage-defining allotypic dimorphism that impacts both HLA and peptide sensitivity. J. Immunol. 2014. 192: 2875-2884.
41. Thananchai, H., Gillespie, G., Martin, M. P., Bashirova, A., Yawata, N., Yawata, M., Easterbrook, P. et al., Cutting edge: allele-specific and peptide-dependent interactions between KIR3DL1 and HLA-A and HLA-B. J. Immunol. 2007. 178: 33-37.
42. Boudreau, J. E., Le Luduec, J. B. and Hsu, K. C., Development of a novel multiplex PCR assay to detect functional subtypes of KIR3DL1 alleles. PLoS One 2014. 9: e99543.