Cellular and molecular basis of haploidentical hematopoietic stem cell transplantation in the successful treatment of high-risk leukemias: Role of alloreactive NK cells

Frontiers in Immunology

Volumn 4, Issue FRB, 2013, Pages

  Locatelli, Franco ^a,b   Pende, Daniela ^c   Mingari, Maria C ^c,d   Bertaina, Alice ^a,b   Falco, Michela ^e   Moretta, Alessandro ^d   Moretta, Lorenzo ^e  

^a BAMBINO GESÙ CHILDREN S HOSPITAL   (Italy)

^b UNIVERSITY OF PAVIA   (Italy)

^c UNIVERSITY OF GENOA   (Italy)

^d UNIVERSITY OF GENOA   (Italy)

^e G GASLINI INSTITUTE   (Italy)

Author keywords

Acute lymphoblastic leukemia; Acute myeloid leukemia; Graft vs host disease; Haploidentical hemopoietic stem cell transplantation; Killer Ig like receptors; Natural killer cells; NK alloreactivity

Indexed keywords

KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR; NATURAL KILLER CELL RECEPTOR; NATURAL KILLER CELL RECEPTOR NKG2A; T LYMPHOCYTE RECEPTOR;

ACUTE LYMPHOBLASTIC LEUKEMIA; CELL FUNCTION; CYTOFLUOROMETRY; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; IMMUNE RESPONSE; IMMUNOREGULATION; LEUKEMIA; NATURAL KILLER CELL; NONHUMAN; PROTEIN EXPRESSION; REVIEW; SURVIVAL RATE; TREATMENT OUTCOME;

EID: 84883723997     PISSN: None     EISSN: 16643224     Source Type: Journal    
DOI: 10.3389/fimmu.2013.00015     Document Type: Review

References (82)

1. Antoine, C., Müller, S., Cant, A., Cavazzana-Calvo, M., Veys, P., Vossen, J., et al. (2003). Long-term survival and transplantation of haemopoietic stem cells for immunodeficiencies: report of the European experience 1968-99. Lancet 361, 553-560.
2. Asai, O., Longo, D. L., Tian, Z. G., Hornung, R. L., Taub, D. D., Ruscetti, F. W., et al. (1998). Suppression of graft-versus-host disease and amplification of graft-versus-tumor effects by activated natural killer cells after allogeneic bone marrow transplantation. J. Clin. Invest. 101, 1835-1842.
3. Aversa, F., Tabilio, A., Terenzi, A., Velardi, A., Falzetti, F., Giannoni, C., et al. (1994). Successful engraftment of T-cell-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, 3948-3955.
4. Aversa, F., Tabilio, A., Velardi, A., Cunningham, I., Terenzi, A., Falzetti, F., et al. (1998). Treatment of high risk acute leukaemia with T-depleted stem cells from related donors with one fully mismatched HLA haplotype. N. Eng. J. Med. 339, 1186-1193.
5. Bachar-Lustig, E., Rachamim, N., Li, H. W., Lan, F., and Reisner, Y. (1995). Megadose of T-depleted bone marrow overcomes MHC barriers in sublethally irradiated mice. Nat. Med. 1, 1268-1273.
6. Bennet, M. (1987). Biology and genetics of hybrid resistance. Adv. Immunol. 41, 333-445.
7. Biassoni, R., Falco, M., Cambiaggi, A., Costa, P., Verdiani, S., Pende, D., et al. (1995). Amino acid substitutions can influence the natural killer (NK)-mediated recognition of HLA-C molecules. Role of serine-77 and lysine-80 in the target cell protection from lysis mediated by "group 2" or "group 1" NK clones. J. Exp. Med. 182, 605-609.
8. Bottino, C., Castriconi, R., Pende, D., Rivera, P., Nanni, M., Carnemolla, B., et al. (2003). Identification of PVR (CD155) and Nectin-2 (CD112) as cell surface ligands for the human DNAM-1 (CD226) activating molecule. J. Exp. Med. 198, 557-567.
9. Bottino, C., Falco, M., Parolini, S., Marcenaro, E., Augugliaro, R., Sivori, S., et al. (2001). NTB-A, a novel SH2D1A-associated surface molecule contributing to the inability of natural killer cells to kill Epstein-Barr virus-infected B cells in X-linked lymphoproliferative diseases. J. Exp. Med. 194, 235-246.
10. Brandt, C. S., Bléry, M., Chaix, J., Fuseri, N., Chasson, L., Robbins, S. H., et al. (2009). The B7 family member B7-H6 is a tumor cell ligand for the activating natural killer cell receptor NKp30 in humans. J. Exp. Med. 20, 1495-1503.
11. Cantoni, C., Bottino, C., Vitale, M., Pessino, A., Augugliaro, R., Malaspina, A., et al. (1999). NKp44, a triggering receptor involved in tumor cell lysis by activated human natural killer cells, is a novel member of the immunoglobulin superfamily. J. Exp. Med. 189, 787-796.
12. Chaleff, S., Otto, M., Barfield, R. C., Leimig, T., Iyengar, R., Martin, J., et al. (2007). A large-scale method for the selective depletion of alphabeta T lymphocytes from PBSC for allogeneic transplantation. Cytotherapy 9, 746-754.
13. Chewning, J. H., Gudme, C. N., Hsu, K. C., Selvakumar, A., and Dupont, B. (2007). KIR2DS1-positive NK cells mediate alloresponse against the C2 HLA-KIR ligand group in vitro. J. Immunol. 179, 854-868.
14. Ciccone, E., Pende, D., Viale, O., Di Donato, C., Tripodi, G., Orengo, A. M., et al. (1992a). 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, 709-718.
15. Ciccone, E., Pende, D., Viale, O., Than, A., Di Donato, C., Orengo, A. M., et al. (1992b). Involvement of HLA class I alleles in NK cell specific function: expression of HLA-Cw3 confers selective protection from lysis by alloreactive NK clones displaying a defined specificity (specificity 2). J. Exp. Med. 176, 963-971.
16. Ciccone, E., Pende, D., Vitale, M., Nanni, L., Di Donato, C., Bottino, C., et al. (1994). Self class I molecules protect normal cells from lysis mediated by autologous natural killer cells. Eur. J. Immunol. 24, 1003-1006.
17. Colonna, M., Navarro, F., Bellón, T., Llano, M., García, P., Samaridis, J., et al. (1997). A common inhibitory receptor for major histocompatibility complex class I molecules on human lymphoid and myelomonocytic cells. J. Exp. Med. 186, 1809-1818.
18. Colonna, M., and Samaridis, J. (1995). Cloning of immunoglobulin-superfamily members associated with HLA-C and HLA-B recognition by human natural killer cells. Science 268, 405-408.
19. Cooley, S., Weisdorf, D. J., Guethlein, L. A., Klein, J. P., Wang, T., Le, C. T., et al. (2010). Donor selection for natural killer cell receptor genes leads to superior survival after unrelated transplantation for acute myelogenous leukemia. Blood 116, 2411-2419.
20. Copelan, E. A. (2006). Hematopoietic stem cell transplantation N Engl. J. Med. 354, 1813-1826.
21. Cosman, D., Fanger, N., Borges, L., Kubin, M., Chin, W., Peterson, L., et al. (1997). A novel immunoglobulin superfamily receptor for cellular and viral MHC class I molecules. Immunity 7, 273-282.
22. Costello, R. J., Sivori, S., Marcenaro, E., Lafage-Pochitaloff, M., Mozziconacci, M. J., Reviron, D., et al. (2002). Defective expression and function of natural killer cell triggering receptors in patients with acute myeloid leukemia. Blood 99, 3661-3667.
23. Della Chiesa, M., Falco, M., Podestá, M., Locatelli, F., Moretta, L., Frassoni, F., et al. (2012). Phenotypic and functional heterogeneity of human NK cells developing after umbilical cord blood transplantation: a role for human cytomegalovirus? Blood 119, 399-410.
24. Döhring, C., Scheidegger, D., Samaridis, J., Cella, M., and Colonna, M. (1996). A human killer inhibitory receptor specific for HLA-A. J. Immunol. 156, 3098-3101.
25. Foley, B., Cooley, S., Verneris, M. R., Pitt, M., Curtsinger, J., Luo, X., et al. (2012). Cytomegalovirus reactivation after allogeneic transplantation promotes a lasting increase in educated NKG2C+ natural killer cells with potent function. Blood 119, 2665-2674.
26. Gluckman, E. (2006). Cord blood transplantation. Biol. Blood Marrow Transplant. 12, 808-812.
27. Graef, T., Moesta, A. K., Norman, P. J., Abi-Rached, L., Vago, L., Older Aguilar, A. M., et al. (2009). KIR2DS4 is a product of gene conversion with KIR3DL2 that introduced specificity for HLA-A*11 while diminishing avidity for HLA-C. J. Exp. Med. 206, 2557-2572.
28. Gumá, M., Angulo, A., Vilches, C., Gómez-Lozano, N., and Malats, N., López-Botet, M. (2004). Imprint of human cytomegalovirus infection on the NK cell receptor repertoire. Blood 104, 3664-3671.
29. Gumperz, J. E., Barber, L. D., Valiante, N. M., Percival, L., Phillips, J. H., Lanier, L. L., et al. (1997). Conserved and variable residues within the Bw4 motif of HLA-B make separable contributions to recognition by the NKB1 killer cell-inhibitory receptor. J. Immunol. 158, 5237-5241.
30. Handgretinger, R. (2012). New approaches to graft engineering for haploidentical bone marrow transplantation. Semin. Oncol. 39, 664-673.
31. Horowitz, M. M., Gale, R. P., Sondel, P. M., Goldman, J. M., Kersey, J., Kolb, H. J., et al. (1990). Graft-versus-leukemia reactions after bone marrow transplantation. Blood 75, 555-562.
32. Janeway, C. A. Jr., and Medzhitov, R. (2002). Innate immune recognition. Annu. Rev. Immunol. 20, 197-216.
33. Lanier, L. L. (1998). NK cell receptors. Annu. Rev. Immunol. 16, 359-393.
34. Leung, W., Iyengar, R., Turner, V., Lang, P., Bader, P., Conn, P., et al. (2004). Determinants of antileukemia effects of allogeneic NK cells. J. Immunol. 172, 644-650.
35. Locatelli, F, Pende, D., Maccario, R., Mingari, M. C., Moretta, A., and Moretta, L. (2009). Haploidentical hemopoietic stem cell transplantation for the treatment of high-risk leukemias: how NK cells make the difference. Clin. Immunol. 133, 171-178.
36. Long, E. O. (1999). Regulation of immune responses through inhibitory receptors. Annu. Rev. Immunol. 17, 875-904.
37. Lopez-Botet, M., Llano, M., Navarro, F., and Bellón, T. (2000). NK cell recognition of non-classical HLA class I molecules. Semin. Immunol. 12, 109-219.
38. Martelli, M. F., Aversa, F., Bachar-Lustig, E., Velardi, A., Reich-Zelicher, S., Tabilio, A., et al. (2002). Transplants across human leukocyte antigen barriers. Semin. Hematol. 39, 48-56.
39. Martin, M. P., Gao, X., Lee, J. H., Nelson, G. W., Detels, R., Goedert, J. J., et al. (2002). Epistatic interaction between KIR3DS1 and HLA-B delays the progression to AIDS. Nat. Genet. 31, 429-434.
40. Miller, J. S., Soignier, Y., Panoskaltsis-Mortari, A., McNearney, S. A., Yun, G. H., Fautsch, S. K., et al. (2005). Successful adoptive transfer and in vivo expansion of human haploidentical NK cells in patients with cancer. Blood 105, 3051-3057.
41. Moesta, A. K., Norman, P. J., Yawata, M., Yawata, N., Gleimer, M., and Parham, P. (2008). Synergistic polymorphism at two positions distal to the ligand-binding site makes KIR2DL2 a stronger receptor for HLA-C than KIR2DL3. J. Immunol. 180, 3969-3979.
42. Moretta, A., Bottino, C., Pende, D., Tripodi, G., Tambussi, G., Viale, O., et al. (1990a). Identification of four subsets of human CD3-CD16+ NK cells by the expression of clonally distributed functional surface molecules. Correlation between subset assignment of NK clones and ability to mediate specific alloantigen recognition. J. Exp. Med. 172, 1589-1598.
43. Moretta, A., Tambussi, G., Bottino, C., Tripodi, G., Merli, A., Ciccone, E., et al. (1990b). A novel surface antigen expressed by a subset of human CD3-CD16+ Natural Killer cells. Role in cell activation and regulation of cytolytic function. J. Exp. Med. 171, 695-714.
44. Moretta, A., Bottino, C., Tripodi, G., Vitale, M., Pende, D., Morelli, L., et al. (1992). Novel surface molecules involved in human NK cell activation and triggering of the lytic machinery. Int. J. Cancer Suppl. 7, 6-10.
45. Moretta, A., Bottino, C., Vitale, M., Pende, D., Biassoni, R., Mingari, M. C., et al. (1996). Receptors for HLA-class I molecules in human natural killer cells. Annu. Rev. Immunol. 14, 619-648.
46. Moretta, A., Locatelli, F., and Moretta, L. (2008). Human NK cells: from HLA class I-specific Ig-like receptors to the therapy of acute leukemias. Immunol. Rev. 224, 58-69.
47. Moretta, A., Sivori, S., Vitale, M., Pende, D., Morelli, L., Augugliaro, R., et al. (1995). Existence of both inhibitory (p58) and activatory (p50) receptors for HLA-C molecules in human natural killer cells. J. Exp. Med. 182, 875-884.
48. Moretta, A., Vitale, M., Bottino, C., Orengo, A. M., Morelli, L., Augugliaro, R., et al. (1993). p58 molecules as putative receptors for MHC class I molecules in human natural killer (NK) cells. Anti-p58 antibodies reconstitute lysis of MHC class I-protected cells in NK clones displaying different specificities. J. Exp. Med. 178, 597-604.
49. Moretta, L., Bottino, C., Pende, D., Castriconi, R., Mingari, M. C., and Moretta, A. (2006). Surface NK receptors and their ligands on tumor cells. Semin. Immunol. 18, 151-158.
50. Moretta, L., Ciccone, E., Mingari, M. C., Biassoni, R. and Moretta, A. (1994). Human NK cells: origin, clonality, specificity and receptors. Adv. Immunol. 55, 341-380.
51. Moretta, L., Locatelli, F., Pende, D., Marcenaro, E., Mingari, M. C., and Moretta, A. (2011). Killer Ig-like receptor-mediated control of natural killer cell alloreactivity in haploidentical hematopoietic stem cell transplantation. Blood 117, 764-771.
52. Moretta, L., and Moretta, A. (2004). Unravelling natural killer cell function: triggering and inhibitory human NK receptors. EMBO J. 23, 255-259.
53. Nguyen, S., Dhedin, N., Vernant, J. P., Kuentz, M., Al Jijakli, A., Rouas-Freiss, N., et al. (2005). NK-cell reconstitution after haploidentical hematopoietic stem-cell transplantations: immaturity of NK cells and inhibitory effect of NKG2A override GvL effect. Blood 105, 4135-4142.
54. Pende, D., Biassoni, R., Cantoni, C., Verdiani, S., Falco, M., di Donato, C., et al. (1996). The natural killer cell receptor specific for HLA-A allotypes: a novel member of the p58/p70 family of inhibitory receptors that is characterized by three immunoglobulin-like domains and is expressed as a 140-kD disulphide-linked dimer. J. Exp. Med. 184, 505-518.
55. Pende, D., Marcenaro, S., Falco, M., Martini, S., Bernardo, M. E., Montagna, D., et al. (2009). Anti-leukemia activity of alloreactive NK cells in KIR ligand-mismatched haploidentical HSCT for pediatric patients: evaluation of the functional role of activating KIR and redefinition of inhibitory KIR specificity. Blood 113, 3119-3129.
56. Pende, D., Parolini, S., Pessino, A., Sivori, S., Augugliaro, R., Morelli, L., et al. (1999). Identification and molecular characterization of NKp30, a novel triggering receptor involved in natural cytotoxicity mediated by human natural killer cells. J. Exp. Med. 190, 1505-1516.
57. Pende, D., Spaggiari, G. M., Marcenaro, S., Martini, S., Rivera, P., Capobianco, A., et al. (2005). Analysis of the receptor-ligand interactions in the natural killer-mediated lysis of freshly isolated myeloid or lymphoid leukemias. Evidence for the involvement of the poliovirus receptor (CD155) and Nectin-2 (CD122). Blood 105, 2066-2073.
58. Pessino, A., Sivori, S., Bottino, C., Malaspina, A., Morelli, L., Moretta, L., et al. (1998). Molecular cloning of NKp46: a novel member of the immunoglobulin superfamily involved in triggering of natural cytotoxicity. J. Exp. Med. 188, 953-960.
59. Rajagopalan, S., Fu, J., and Long, E. O. (2001). Cutting edge: induction of IFN-gamma production but not cytotoxicity by the killer cell Ig-like receptor KIR2DL4 (CD158d) in resting NK cells. J. Immunol. 167, 1877-1881.
60. Raulet, D. H. (2003). Roles of the NKG2D immunoreceptor and its ligands. Nat. Rev. Immunol. 3, 781-790.
61. Reisner, Y., Kapoor, N., Kirkpatrick, D., Pollack, M. S., Cunningham-Rundles, S., Dupont, B., et al. (1983). Transplantation for severe combined immunodeficiency with HLA-A,B,D,DR incompatible parental marrow cells fractionated by soybean agglutinin and sheep red blood cells. Blood 61, 341-348.
62. Reisner, Y., and Martelli, F. (1999). Stem cell escalation enables HLA-disparate hematopoietic transplants in leukemia patients. Immunol. Today 20, 343-347.
63. Reymond, N., Castriconi, R., Pende, D., Rivera, P., Nanni, M., Carnemolla, B., et al. (2004). DNAM-1 and PVR regulate of monocyte migration through endothelial junctions. J. Exp. Med. 199, 1331-1341.
64. Rocha, V., and Locatelli, F. (2008). Searching for alternative donors of haematopoietic stem cell for paediatric patients. Bone Marrow Transplant. 41, 207-214.
65. Romagné, F., André, P., Spee, P., Zahn, S., Anfossi, N., Gauthier, L., et al. (2009). Preclinical characterization of 1-7F9, a novel human anti-KIR receptor therapeutic antibody that augments natural killer-mediated killing of tumor cells. Blood 114, 2667-2677.
66. Rubnitz, J. E., Inaba, H., Ribeiro, R. C., Pounds, S., Rooney, B., Bell, T., Pui, C. H., et al. (2010). NKAML: a pilot study to determine the safety and feasibility of haploidentical natural killer cell transplantation in childhood acute myeloid leukemia. J. Clin. Oncol. 28, 955-959.
67. Ruggeri, L., Capanni, M., Urbani, E., Perruccio, K., Shlomchik, W. D., Tosti, A., et al. (2002). Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science 295, 2097-2100.
68. Shibuya, A., Campbell, D., Hannum, C., Yssel, H., Franz-Bacon, K., McClanahan, T., et al. (1996). DNAM-1, a novel adhesion molecule involved in the cytolytic function of T lymphocytes. Immunity 4, 573-581.
69. Shlomchik, W. D., Couzens, M. S., Tang, C. B., McNiff, J., Robert, M. E., Liu, J., et al. (1999). Prevention of graft versus host disease by inactivation of host antigen-presenting cells. Science 285, 412-415.
70. Sivori, S., Vitale, M., Morelli, L., Sanseverino, L., Augugliaro, R., Bottino, C., et al. (1997). p46, a novel natural killer cell-specific surface molecule which mediates cell activation. J. Exp. Med. 186, 1129-1136.
71. Stern, M., Ruggeri, L., Capanni, M., Mancusi, A., and Velardi, A. (2008). Human leukocyte antigens A23, A24, and A32 but not A25 are ligands for KIR3DL1. Blood 112, 708-710.
72. Stewart, C. A., Laugier-Anfossi, F., Vély, F., Saulquin, X., Riedmuller, J., Tisserant, A., et al. (2005). Recognition of peptide-MHC class I complexes by activating killer immunoglobulin-like receptors. Proc. Natl. Acad. Sci. U.S.A. 102, 13224-13229.
73. Symons, H. J., Leffell, M. S., Rossiter, N. D., Zahurak, M., Jones, R. J., and Fuchs, E. J. (2010). Improved survival with inhibitory killer immunoglobulin receptor (KIR) gene mismatches and KIR haplotype B donors after nonmyeloablative, HLA-haploidentical bone marrow transplantation. Biol. Blood Marrow Transplant. 16, 533-542.
74. Trinchieri, G. (1989). Biology of natural killer cells. Adv. Immunol. 47, 187-376.
75. Vago, L., Forno, B., Sormani, M. P., Crocchiolo, R., Zino, E., Di Terlizzi, S., et al. (2008). 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 112, 3488-3499.
76. Valiante, N. M., and Trinchieri, G. (1993). Identification of a novel signal transduction surface molecule on human cytotoxic lymphocytes. J. Exp. Med. 178, 1397-1406.
77. Vitale, M., Bottino, C., Sivori, S., Sanseverino, L., Castriconi, R., Marcenaro, E., et al. (1998). NKp44, a novel triggering surface molecule specifically expressed by activated natural killer cells is involved in non-MHC restricted tumor cell lysis. J. Exp. Med. 187, 2065-2072.
78. Vitale, M., Falco, M., Castriconi, R., Parolini, S., Zambello, R., Semenzato, G., et al. (2001). Identification of NKp80, a novel triggering molecule expressed by human natural killer cells. Eur. J. Immunol. 31, 233-242.
79. Wagtmann, N., Biassoni, R., Cantoni, C., Verdiani, S., Malnati, M. S., Vitale, M., et al. (1995). Molecular clones of the p58 natural killer cell receptor reveal Ig-related molecules with diversity in both the extra- and intracellular domains. Immunity 2, 439-449.
80. Walzer, T., Bléry, M., Chaix, J., Fuseri, N., Chasson, L., Robbins, S. H., et al. (2007). Identification, activation, and selective in vivo ablation of mouse NK cells via NKp46. Proc. Natl. Acad. Sci. U.S.A. 104, 3384-3389.
81. Welte, S., Kuttruff, S., Waldhauer, I., and Steinle, A. (2006). Mutual activation of natural killer cells and monocytes mediated by NKp80-AICL interaction. Nat. Immunol. 12, 1334-1342.
82. Wu, J., Song, Y., Bakker, A. B., Bauer, S., Spies, T., Lanier, L. L., et al. (1999). An activating immunoreceptor complex formed by NKG2D and DAP10. Science 285, 730-732.