Natural killer cell recognition of missing self and haploidentical hematopoietic transplantation

Seminars in Cancer Biology

Volumn 16, Issue 5, 2006, Pages 404-411

  Ruggeri, Loredana ^a   Mancusi, Antonella ^a   Burchielli, Emanuela ^a   Perruccio, Katia ^a   Aversa, Franco ^a   Martelli, Massimo F ^a   Velardi, Andrea ^a  

^a UNIVERSITY OF PERUGIA   (Italy)

Author keywords

Allogeneic hematopoietic transplantation; Immunotherapy; KIR; Leukemia; NK cell alloreactivity

Indexed keywords

CYCLOPHOSPHAMIDE; FLUDARABINE; HLA ANTIGEN CLASS 1; HLA B ANTIGEN; HLA C ANTIGEN; IMMUNOSUPPRESSIVE AGENT; THIOTEPA; THYMOCYTE ANTIBODY;

ACUTE LEUKEMIA; ADOPTIVE IMMUNOTHERAPY; ALLELE; ALLOGENEIC HEMATOPOIETIC STEM CELL TRANSPLANTATION; ALLOIMMUNITY; CANCER RELAPSE; CANCER RISK; CANCER SURVIVAL; CELL TRANSPLANTATION; CLINICAL TRIAL; DONOR; GRAFT VERSUS HOST REACTION; HAPLOIDY; HAPLOTYPE; HEMATOLOGIC DISEASE; HEMATOPOIESIS; HUMAN; IMMUNOTHERAPY; LEUKEMIA; LYMPHOCYTOPENIA; LYSIS; NATURAL KILLER CELL; NONHUMAN; RECIPIENT; REVIEW;

ANIMALS; AUTOANTIGENS; CELL DEATH; CLINICAL TRIALS; CLINICAL TRIALS AS TOPIC; GRAFT VS HOST DISEASE; GRAFT VS LEUKEMIA EFFECT; HAPLOTYPES; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HLA ANTIGENS; HUMANS; IMMUNOTHERAPY, ADOPTIVE; KILLER CELLS, NATURAL; MICE; NEOPLASMS; RECEPTORS, IMMUNOLOGIC; RECEPTORS, KIR; TRANSPLANTATION TOLERANCE; TRANSPLANTATION, HOMOLOGOUS;

EID: 33748204462     PISSN: 1044579X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.semcancer.2006.07.007     Document Type: Review

References (68)

1. Kärre K., Ljunggren H.G., Piontek G., and Kiessling R. Selective rejection of H-2 deficient lymphoma variants suggests alternative immune defence strategy. Nature 319 (1986) 675-678
2. Ljunggren H.G., and Kärre K. In search of the 'missing self'. MHC molecules and NK cell recognition. Immunol Today 11 (1990) 237-244
3. Moretta L., Ciccone E., Moretta A., et al. Allorecognition by NK cells: non-self or no self?. Immunol Today 13 (1992) 300-306
4. Ciccone E., Pende D., Viale O., Hoglund P., Ohlen C., and Karre K. Evidence of a natural killer (NK) cell repertoire for (allo) antigen recognition: definition of five distinct NK-determined allospecificities in humans. J Exp Med 175 (1992) 709-718
5. Colonna M., Brooks E.G., Falco M., Ferrara G.B., and Strominger J.L. Generation of allospecific natural killer cells by stimulation across a polymorphism of HLA-C. Science 260 (1993) 1121-1124
6. Colonna M., and Samaridis J. Cloning of immunoglobulin-superfamily members associated with HLA-C and HLA-B recognition by human natural killer cells. Science 268 (1995) 405-408
7. Valiante N.M., Uhrberg M., Shilling H.G., Lienert-Weidenbach K., Arnett K.L., D'Andrea A., et al. Functionally and structurally distinct NK cell receptor repertoires in the peripheral blood of two human donors. Immunity 7 (1997) 739-751
8. Uhrberg M., Valiante N.M., Shum B.P., Shilling H.G., Lienert-Weidenbach K., Corliss B., et al. Human diversity in killer cell inhibitory receptor genes. Immunity 7 (1997) 753-760
9. Long E.O. Regulation of immune responses through inhibitory receptors. Annu Rev Immunol 17 (1999) 875-904
10. Lanier L.L. Face off-the interplay between activating and inhibitory immune receptors. Curr Opin Immunol 13 (2001) 326-331
11. Moretta L., and Moretta A. Killer immunoglobulin-like receptors. Curr Opin Immunol 16 (2004) 626-633
12. Lopez-Botet M., Perez-Villar J.J., Carretero M., Rodriguez A., Melero I., Bellon T., et al. Structure and function of the CD94 C-type lectin receptor complex involved in the recognition of HLA class I molecules. Immunol Rev 155 (1997) 165-174
13. Vilches C., and Parham P. KIR: diverse, rapidly evolving receptors of innate and adaptive immunity. Annu Rev Imunol 20 (2002) 217-251
14. Shilling H.G., Young N., Guethlein L.A., Cheng N.W., Gardiner C.M., Tyan D., et al. Genetic control of human NK cell repertoire. J Immunol 169 (2002) 239-247
15. Lanier L.L. On guard-activating NK cell receptors. Nat Immunol 2 (2001) 23-27
16. Moretta A., Bottino C., Vitale M., Pende D., Cantoni C., Mingari M.C., et al. Activating receptors and coreceptors involved in human natural killer cell-mediated cytolysis. Annu Rev Immunol 19 (2001) 197-223
17. Wu J., Song Y., Bakker A.B., Bauer S., Spies T., Lanier L.L., et al. An activating immunoreceptor complex formed by NKG2D and DAP10. Science 285 (1999) 730-732
18. Jamieson A.M., Diefenbach A., McMahon C.W., Xiong N., Carlyle J.R., and Raulet D.H. The role of the NKG2D immunoreceptor in immune cell activation and natural killing. Immunity 17 (2002) 19-29
19. Bauer S., Groh V., Wu J., Steinle A., Phillips J.H., Lanier L.L., et al. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science 285 (1999) 727-729
20. Cosman D., Mullberg J., Sutherland C.L., Chin W., Armitage R., Fanslow W., et al. ULBPs, novel MHC class I-related molecules, bind to CMV glycoprotein UL16 and stimulate NK cytotoxicity through the NKG2D receptor. Immunity 14 (2001) 123-133
21. Diefenbach A., Jamieson A.M., Liu S.D., Shastri N., and Raulet D.H. Ligands for the murine NKG2D receptor: expression by tumor cells and activation of NK cells and macrophages. Nat Immunol 1 (2000) 119-126
22. Diefenbach A., Jensen E.R., Jamieson A.M., and Raulet D.H. Rae1 and H60 ligands of the NKG2D receptor stimulate tumour immunity. Nature 413 (2001) 165-171
23. Cerwenka A., Bakker A.B., McClanahan T., Wagner J., Wu J., Phillips J.H., et al. Retinoic acid early inducible genes define a ligand family for the activating NKG2D receptor in mice. Immunity 12 (2000) 721-727
24. Groh V., Rhinehart R., Secrist H., Bauer S., Grabstein K.H., Spies T., et al. Broad tumor-associated expression and recognition by tumor-derived gamma delta T cells of MICA and MICB. Proc Natl Acad Sci USA 96 (1999) 6879-6884
25. Sutherland C.L., Chalupny N.J., Schooley K., VandenBos T., Kubin M., Cosman D., et al. UL16-binding proteins, novel MHC class I-related proteins, bind to NKG2D and activate multiple signaling pathways in primary NK cells. J Immunol 168 (2002) 671-679
26. Kubin M., Cassiano L., Chalupny J., Chin W., Cosman D., Fanslow W., et al. ULBP1, 2, 3: novel MHC class I-related molecules that bind to human cytomegalovirus glycoprotein UL16, activate NK cells. Eur J Immunol 31 (2001) 1428-1437
27. Pende D., Rivera P., Marcenaro S., Chang C.C., Biassoni R., Conte R., et al. Major histocompatibility complex class I-related chain A and UL16-binding protein expression on tumor cell lines of different histotypes: analysis of tumor susceptibility to NKG2D-dependent natural killer cell cytotoxicity. Cancer Res 62 (2002) 6178-6186
28. Moretta A., Biassoni R., Bottino C., Mingari M.C., and Moretta L. Natural cytotoxicity receptors that trigger human NK cell-mediated cytolysis. Immunol Today 21 (2000) 228-234
29. Sivori S., Pende D., Bottino C., Marcenaro E., Pessino A., Biassoni R., et al. NKp46 is the major triggering receptor involved in the natural cytotoxicity of fresh or cultured human NK cells. Correlation between surface density of NKp46 and natural cytotoxicity against autologous, allogeneic or xenogeneic target cells. Eur J Immunol 29 (1999) 1656-1666
30. Moretta L., and Moretta A. Unravelling natural killer cell function: triggering and inhibitory human NK receptors. EMBO J 23 (2004) 255-259
31. Parham P. MHC class I molecules and KIRs in human history, health and survival. Nat Rev Immunol 5 (2005) 201-214
32. Saulquin X., Gastinel L.N., and Vivier E. Crystal structure of the human natural killer cell activating receptor KIR2DS2 (CD158j). J Exp Med 197 (2004) 933-938
33. Velardi A., Ruggeri L., Moretta A., and Moretta L. NK-cells: a lesson from mismatched haematopoietic transplantation. Trends Immunol 23 (2002) 438-444
34. Farag S.S., Fehniger T.A., Ruggeri L., Velardi A., and Caligiuri M.A. Natural killer cell receptors: new biology and insights into the graft versus leukemia effect. Blood 100 (2002) 1935-1947
35. Cudkowicz G., and Bennett M. Peculiar immunobiology of bone-marrow allografts. II. Rejection of parental grafts by resistant F1 hybrid mice. J Exp Med 135 (1972) 1028-1036
36. Yu Y.Y., George T., Dorfman J.R., Roland J., Kumar V., and Bennett M. The role of Ly49A and 5E6 (Ly49C) molecules in hybrid resistance mediated by murine natural killer cells against normal T cell blasts. Immunity 4 (1996) 67-76
37. Ruggeri L., Capanni M., Urbani E., Perruccio K., Shlomchik W.D., Tosti A., et al. Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science 295 (2002) 2097-2100
38. Kärre K. A perfect mismatch. Science 295 (2002) 2029-2031
39. Shlomchik W.D., Couzens M.S., Tang C.B., McNiff J., Robert M.E., Liu J., et al. Prevention of graft versus host disease by inactivation of host antigen-presenting cells. Science 285 (1999) 412-415
40. Caligiuri M.A., Velardi A., Scheinberg D.A., and Borrello I.M. Immunotherapeutic approaches for haematological malignancies. Hematology 2004, ASH education program book (2004), American Society of Hematology, Washington, WA p. 337-53
41. Ruggeri L., Capanni M., Casucci M., Volpi I., Tosti A., Perruccio K., et al. Role of natural killer cell alloreactivity in HLA-mismatched hematopoietic stem cell transplantation. Blood 94 (1999) 333-339
42. Igarashi T., Wynberg J., Srinivasan R., Becknell B., McCoy Jr. J.P., Takahashi Y., et al. Enhanced cytotoxicity of allogeneic NK cells with killer immunoglobulin-like receptor ligand incompatibility against melanoma and renal cell carcinoma cells. Blood 104 (2004) 170-177
43. Blume K.G., Forman S.J., and Appelbaum F.R. Hematopoietic cell transplantation. 3rd ed. (2004), Blackwell Science, Malden, MA
44. Anasetti C., and Velardi A. Hematopoietic cell transplantation from HLA partially matched related donors. In: Blume K.G., Forman S.J., and Appelbaum F.R. (Eds). Hematopoietic cell transplantation. 3rd ed. (2004), Blackwell Science, Malden, MA
45. Bachar-Lustig E., Rachamim N., Li H.W., Lan F., and Reisner Y. Megadose of T-depleted bone marrow overcomes MHC barriers in sublethally irradiated mice. Nat Med 1 (1995) 1268-1273
46. Aversa F., Tabilio A., Terenzi A., Velardi A., Falzetti F., Giannoni C., et al. Successful engraftment of T-depleted haploidentical "three-loci" incompatible transplants in leukemia patients by addition of recombinant human granulocyte colony-stimulating factor-mobilized peripheral blood progenitor cells to bone marrow inoculum. Blood 84 (1994) 3948-3955
47. Aversa F., Tabilio A., Velardi A., Cunningham I., Terenzi A., Falzetti F., et al. Treatment of high risk acute leukaemia with T-depleted stem cells from related donors with one fully mismatched HLA haplotype. N Engl J Med 339 (1998) 1186-1193
48. Aversa F., Terenzi A., Tabilio A., Falzetti F., Carotti A., Ballanti S., et al. Full haplotype-mismatched hematopoietic stem-cell transplantation: a phase II study in patients with acute leukemia at high risk of relapse. J Clin Oncol 23 (2005) 3447-3454
49. Leung W., Iyengar R., Turner V., Lang P., Bader P., Conn P., et al. Determinants of antileukemia effects of allogeneic NK cells. J Immunol 172 (2004) 644-650
50. Ruggeri L., Mancusi A., Capanni M., Martelli M.F., and Velardi A. Exploitation of alloreactive natural killer cells in adoptive immunotherapy of cancer. Curr Opin Immunol 17 (2005) 211-217
51. Hsu K.C., Keever-Taylor C.A., Wilton A., Pinto C., Heller G., Arkun K., et al. Improved outcome in HLA-identical sibling hematopoietic stem-cell transplantation for acute myelogenous leukemia predicted by KIR and HLA genotypes. Blood 105 (2005) 4878-4884
52. Salcedo M., Andersson M., Lemieux S., Van Kaer L., Chambers B.J., and Ljunggren H.G. Fine tuning of natural killer cell specificity and maintenance of self-tolerance in MHC class I-deficient mice. Eur J Immunol 28 (1998) 1315-1321
53. Johansson M.H., Bieberich C., Jay G., Karre K., and Hoglund P. Natural killer cell tolerance in mice with mosaic expression of histocompatibility complex class I transgene. J Exp Med 186 (1997) 353-364
54. Raulet D.H., Vance R.E., and McMahon C.W. Regulation of the natural killer cell receptor repertoire. Annu Rev Immunol 19 (2001) 291-330
55. Raulet D.H. Interplay of natural killer cells and their receptors with the adaptive immune response. Nat Immunol 5 (2004) 996-1002
56. Davies S.M., Ruggieri L., DeFor T., Wagner J.E., Weisdorf D.J., Miller J.S., et al. Evaluation of KIR ligand incompatibility in mismatched unrelated donor hematopoietic transplants. Blood 100 (2002) 3825-3827
57. Giebel S., Locatelli F., Lamparelli T., Velardi A., Davies S., Frumento G., et al. Survival advantage with KIR ligand incompatibility in hematopoietic stem cell transplantation from unrelated donors. Blood 102 (2003) 814-819
58. Lowe E.J., Turner V., Handgretinger R., Horwitz E.M., Benaim E., Hale G.A., et al. T-cell alloreactivity dominates natural killer cell alloreactivity in minimally T-cell-depleted HLA-non-identical paediatric bone marrow transplantation. Br J Haematol 123 (2003) 323-326
59. Morishima Y., Yabe T., and Inoko H. Clinical significance of killer Ig-like receptor (KIR) on acute GvHD, rejection and leukemia relapse in patients transplanted non-T cell depleted marrow from unrelated donors; roles of inhibitory KIR epitope matching and activating KIR genotype. Blood 102 (2003) 526a
60. Elmaagacli A.H., Ottinger H., and Koldehoff M. Reduced risk of molecular and haematological relapse in patients with CML after KIR-mismatched hematopoietic stem cell transplantation. Bone Marrow Transpl 33 (2004) S59
61. Bornhauser M., Schwerdtfeger R., Martin H., Frank K.H., Theuser C., and Ehninger G. Role of KIR ligand incompatibility in hematopoietic stem cell transplantation using unrelated donors. Blood 103 (2005) 2860-2861
62. Beelen D.W., Ottinger H.D., Ferencik S., Elmaagacli A.H., Peceny R., Trenschel R., et al. Genotypic inhibitory killer immunoglobulin-like receptor ligand incompatibility enhances the long-term antileukemic effect of unmodified allogeneic hematopoietic stem cell transplantation in patients with myeloid leukemias. Blood 105 (2005) 2594-2600
63. Shilling H.G., McQueen K.L., Cheng N.W., Shizuru J.A., Negrin R.S., and Parham P. Reconstitution of NK cell receptor repertoire following HLA-matched hematopoietic cell transplantation. Blood 101 (2003) 3730-3740
64. Cooley S., McCullar V., Wangen R., Bergemann T.L., Spellman S., Weisdorf D.J., et al. KIR reconstitution is altered by T cells in the graft and correlates with clinical outcomes after unrelated donor transplantation. Blood 106 (2005) 4370-4376
65. Miller J.S., Soignier Y., Panoskaltsis-Mortari A., McNearney S.A., Yun G.H., Fautsch S.K., et al. Successful adoptive transfer and in vivo expansion of human haploidentical NK cells in cancer patients. Blood 105 (2005) 3051-3057
66. Dudley M.E., Wunderlich J.R., Robbins P.F., Yang J.C., Hwu P., Schwartzentruber D.J., et al. Cancer regression and autoimmunity in patients after clonal repopulation with antitumor lymphocytes. Science 298 (2002) 850-854
67. Cooper M.A., Bush J.E., Fehniger T.A., VanDeusen J.B., Waite R.E., Liu Y., et al. In vivo evidence for a dependence on interleukin 15 for survival of natural killer cells. Blood 100 (2002) 3633-3638
68. Imai C., Iwamoto S., and Campana D. Genetic modification of primary natural killer cells overcomes inhibitory signals and induces specific killing of leukemic cells. Blood 106 (2005) 376-383