An unusual CD56brightCD16low NK cell subset dominates the early posttransplant period following HLA-matched hematopoietic stem cell transplantation

Journal of Immunology

Volumn 181, Issue 3, 2008, Pages 2227-2237

  Dulphy, Nicolas ^a,b,c   Haas, Philippe ^a   Busson, Marc ^a   Belhadj, Stéphanie ^a   De Latour, Régis Peffault ^c   Robin, Marie ^c   Carmagnat, Maryvonnick ^a,c   Loiseau, Pascale ^a,b   Tamouza, Ryad ^a,c   Scieux, Catherine ^c   Rabian, Claire ^a,b,c   Di Santo, James P ^d,e   Charron, Dominique ^a,b,c   Janin, Anne ^a,b   Socié, Gérard ^a,c   Toubert, Antoine ^a,b,c  

^a INSERM   (France)

^b UNIVERSITÉ PARIS DIDEROT   (France)

^c SAINT LOUIS HOSPITAL   (France)

^d INSTITUT PASTEUR   (France)

^e INSTITUT PASTEUR   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD16 ANTIGEN; CD56 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 15; NATURAL KILLER CELL RECEPTOR NKG2A; NATURAL KILLER CELL RECEPTOR NKG2D; PERFORIN; PROTEIN P46; FC RECEPTOR; GEM PROTEIN, HUMAN; HLA ANTIGEN; LECTIN; MONOMERIC GUANINE NUCLEOTIDE BINDING PROTEIN;

ACUTE GRANULOCYTIC LEUKEMIA; ACUTE LYMPHOBLASTIC LEUKEMIA; ADOLESCENT; ADULT; AGED; ALLOGENEIC HEMATOPOIETIC STEM CELL TRANSPLANTATION; ARTICLE; CELL EXPANSION; CELL FUNCTION; CELL MATURATION; CELL SUBPOPULATION; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; DEGRANULATION; DONOR SELECTION; FEMALE; FLOW CYTOMETRY; GRAFT VERSUS HOST REACTION; HEMATOLOGIC MALIGNANCY; HLA MATCHING; HODGKIN DISEASE; HUMAN; HUMAN TISSUE; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; MALE; MYELOMA; MYELOPROLIFERATIVE DISORDER; NATURAL KILLER CELL; NONHODGKIN LYMPHOMA; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCHOOL CHILD; T CELL DEPLETION; ALLOTRANSPLANTATION; BIOSYNTHESIS; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; CYTOLOGY; CYTOTOXICITY; GENOTYPE; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HOMEOSTASIS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; MIDDLE AGED; TIME;

ADOLESCENT; ADULT; ANTIGENS, CD56; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; CHILD; CYTOTOXICITY, IMMUNOLOGIC; FEMALE; GENOTYPE; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HLA ANTIGENS; HOMEOSTASIS; HUMANS; INTERFERON TYPE II; KILLER CELLS, NATURAL; LECTINS; LYMPHOCYTE ACTIVATION; MALE; MIDDLE AGED; MONOMERIC GTP-BINDING PROTEINS; PHENOTYPE; RECEPTORS, IGG; TIME FACTORS; TRANSPLANTATION, HOMOLOGOUS;

EID: 49649107807     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.3.2227     Document Type: Article

References (55)

1. Karre, K., H. G. Ljunggren, G. Piontek, and R. Kiessling. 1986. Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defence strategy. Nature 319: 675-678.
2. bright natural killer cells are present in human lymph nodes and are activated by T cell-derived IL-2: a potential new link between adaptive and innate immunity. Blood 101: 3052-3057.
3. Ruggeri, L., M. Capanni, E. Urbani, K. Perruccio, W. D. Shlomchik, A. Tosti, S. Posati, D. Rogaia, F. Frassoni, F. Aversa, et al. 2002. Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science 295: 2097-2100.
4. Lanier, L. L. 2005. NK cell recognition. Annu. Rev. Immunol. 23: 225-274.
5. Kumar, V., and M. E. McNerney. 2005. A new self: MHC-class-I-independent natural-killer-cell self-tolerance. Nat. Rev. Immunol. 5: 363-374.
6. Parham, P. 2005. MHC class I molecules and KIRs in human history, health and survival. Nat. Rev. Immunol. 5: 201-214.
7. Braud, V. M., D. S. Allan, C. A. O'Callaghan, K. Soderstrom, A. D'Andrea, G. S. Ogg, S. Lazetic, N. T. Young, J. I. Bell, J. H. Phillips, et al. 1998. HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature 391: 795-799.
8. Moretta, A., C. Bottino, M. Vitale, D. Pende, C. Cantoni, M. C. Mingari, R. Biassoni, and L. Moretta. 2001. Activating receptors and coreceptors involved in human natural killer cell-mediated cytolysis. Annu. Rev. Immunol. 19: 197-223.
9. Sivori, S., D. Pende, C. Bottino, E. Marcenaro, A. Pessino, R. Biassoni, L. Moretta, and A. Moretta. 1999. 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: 1656-1666.
10. Pende, D., S. Parolini, A. Pessino, S. Sivori, R. Augugliaro, L. Morelli, E. Marcenaro, L. Accame, A. Malaspina, R. Biassoni, 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.
11. Hayakawa, Y., J. M. Kelly, J. A. Westwood, P. K. Darcy, A. Diefenbach, D. Raulet, and M. J. Smyth. 2002. Cutting edge: Tumor rejection mediated by NKG2D receptor-ligand interaction is dependent upon perforin. J. Immunol. 169: 5377-5381.
12. Pende, D., P. Rivera, S. Marcenaro, C. C. Chang, R. Biassoni, R. Conte, M. Kubin, D. Cosman, S. Ferrone, L. Moretta, and A. Moretta. 2002. 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: 6178-6186.
13. Salih, H. R., H. Antropius, F. Gieseke, S. Z. Lutz, L. Kanz, H. G. Rammensee, and A. Steinle. 2003. Functional expression and release of ligands for the activating immunoreceptor NKG2D in leukemia. Blood 102: 1389-1396.
14. Sconocchia, G., M. Lau, M. Provenzano, K. Rezvani, W. Wongsena, H. Fujiwara, N. Hensel, J. Melenhorst, J. Li, S. Ferrone, and A. J. Barrett. 2005. The antileukemia effect of HLA-matched NK and NK-T cells in chronic myelogenous leukemia involves NKG2D-target-cell interactions. Blood 106: 3666-3672.
15. Cooper, M. A., T. A. Fehniger, and M. A. Caligiuri. 2001. The biology of human natural killer-cell subsets. Trends Immunol. 22: 633-640.
16. Cooley, S., F. Xiao, M. Pitt, M. Gleason, V. McCullar, T. Bergemann, K. L. McQueen, L. A. Guethlein, P. Parham, and J. S. Miller. 2007. A subpopulation of human peripheral blood NK cells that lacks inhibitory receptors for self MHC is developmentally immature. Blood 110: 578-586.
17. dim NK cells upon activation. J. Immunol. 178: 4947-4955.
18. dim cells: role of contact with peripheral fibroblasts. J. Immunol. 179: 89-94.
19. Nguyen, S., N. Dhedin, J. P. Vernant, M. Kuentz, A. Al Jijakli, N. Rouas-Freiss, E. D. Carosella, A. Boudifa, P. Debre, and V. Vieillard. 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.
20. Shilling, H. G., K. L. McQueen, N. W. Cheng, J. A. Shizuru, R. S. Negrin, and P. Parham. 2003. Reconstitution of NK cell receptor repertoire following HLA-matched hematopoietic cell transplantation. Blood 101: 3730-3740.
21. Cooley, S., V. McCullar, R. Wangen, T. L. Bergemann, S. Spellman, D. J. Weisdorf, and J. S. Miller. 2005. KIR reconstitution is altered by T cells in the graft and correlates with clinical outcomes after unrelated donor transplantation. Blood 106: 4370-4376.
22. Uhrberg, M., P. Parham, and P. Wernet. 2002. Definition of gene content for nine common group B haplotypes of the Caucasoid population: KIR haplotypes contain between seven and eleven KIR genes. Immunogenetics 54: 221-229.
23. Chen, C., M. Busson, V. Rocha, M. L. Appert, V. Lepage, N. Dulphy, P. Haas, G. Socie, A. Toubert, D. Charron, and P. Loiseau. 2006. Activating KIR genes are associated with CMV reactivation and survival after non-T-cell depleted HLA-identical sibling bone marrow transplantation for malignant disorders. Bone Marrow Transplant. 38: 437-444.
24. + T cells in Crohn's disease mediate inflammatory and cytotoxic responses through MICA interactions. Gastroenterology 132: 2346-2358.
25. Bryceson, Y. T., M. E. March, D. F. Barber, H. G. Ljunggren, and E. O. Long. 2005. Cytolytic granule polarization and degranulation controlled by different receptors in resting NK cells. J. Exp. Med. 202: 1001-1012.
26. Bryceson, Y. T., M. E. March, H. G. Ljunggren, and E. O. Long. 2006. Synergy among receptors on resting NK cells for the activation of natural cytotoxicity and cytokine secretion. Blood 107: 159-166.
27. Farag, S. S., and M. A. Caligiuri. 2006. Human natural killer cell development and biology. Blood Rev. 20: 123-137.
28. Yawata, M., N. Yawata, M. Draghi, A. M. Little, F. Partheniou, and P. Parham. 2006. Roles for HLA and KIR polymorphisms in natural killer cell repertoire selection and modulation of effector function. J. Exp. Med. 203: 633-645.
29. Huntington, N. D., C. A. Vosshenrich, and J. P. Di Santo. 2007. Developmental pathways that generate natural-killer-cell diversity in mice and humans. Nat. Rev. Immunol. 7: 703-714.
30. Carson, W. E., T. A. Fehniger, S. Haldar, K. Eckhert, M. J. Lindemann, C. F. Lai, C. M. Croce, H. Baumann, and M. A. Caligiuri. 1997. A potential role for interleukin-15 in the regulation of human natural killer cell survival. J. Clin. Invest. 99: 937-943.
31. Blom, B., and H. Spits. 2006. Development of human lymphoid cells. Annu. Rev. Immunol. 24: 287-320.
32. Di Santo, J. P. 2006. Natural killer cell developmental pathways: a question of balance. Annu. Rev. Immunol. 24: 257-286.
33. Freud, A. G., and M. A. Caligiuri. 2006. Human natural killer cell development. Immunol. Rev. 214: 56-72.
34. Blaser, B. W., S. Roychowdhury, D. J. Kim, N. R. Schwind, D. Bhatt, W. Yuan, D. F. Kusewitt, A. K. Ferketich, M. A. Caligiuri, and M. Guimond. 2005. Donor-derived IL-15 is critical for acute allogeneic graft-versus-host disease. Blood 105: 894-901.
35. Blaser, B. W., N. R. Schwind, S. Karol, D. Chang, S. Shin, S. Roychowdhury, B. Becknell, A. K. Ferketich, D. F. Kusewitt, B. R. Blazar, and M. A. Caligiuri. 2006. Trans-presentation of donor-derived interleukin 15 is necessary for the rapid onset of acute graft-versus-host disease but not for graft-versus-tumor activity. Blood 108: 2463-2469.
36. Sutherland, C. L., N. J. Chalupny, K. Schooley, T. VandenBos, M. Kubin, and D. Cosman. 2002. UL16-binding proteins, novel MHC class I-related proteins, bind to NKG2D and activate multiple signaling pathways in primary NK cells. J. Immunol. 168: 671-679.
37. + memory T cells. Proc. Natl. Acad. Sci. USA 99: 6192-6197.
38. Cook, M. A., D. W. Milligan, C. D. Fegan, P. J. Darbyshire, P. Mahendra, C. F. Craddock, P. A. Moss, and D. C. Briggs. 2004. The impact of donor KIR and patient HLA-C genotypes on outcome following HLA-identical sibling hematopoietic stem cell transplantation for myeloid leukemia. Blood 103: 1521-1526.
39. bright natural killer cells. Immunity 22: 295-304.
40. Freud, A. G., A. Yokohama, B. Becknell, M. T. Lee, H. C. Mao, A. K. Ferketich, and M. A. Caligiuri. 2006. Evidence for discrete stages of human natural killer cell differentiation in vivo. J. Exp. Med. 203: 1033-1043.
41. Bajenoff, M., B. Breart, A. Y. Huang, H. Qi, J. Cazareth, V. M. Braud, R. N. Germain, and N. Glaichenhaus. 2006. Natural killer cell behavior in lymph nodes revealed by static and real-time imaging. J. Exp. Med. 203: 619-631.
42. Vosshenrich, C. A., M. E. Garcia-Ojeda, S. I. Samson-Villeger, V. Pasqualetto, L. Enault, O. Richard-Le Goff, E. Corcuff, D. Guy-Grand, B. Rocha, A. Cumano, et al. 2006. A thymic pathway of mouse natural killer cell development characterized by expression of GATA-3 and CD127. Nat. Immunol. 7: 1217-1224.
43. Di Santo, J. P., and C. A. Vosshenrich. 2006. Bone marrow versus thymic pathways of natural killer cell development. Immunol. Rev. 214: 35-46.
44. Waldmann, T. A. 2006. The biology of interleukin-2 and interleukin-15: implications for cancer therapy and vaccine design. Nat. Rev. Immunol. 6: 595-601.
45. + T cell homeostasis. J. Exp. Med. 200: 825-834.
46. Dubois, S., J. Mariner, T. A. Waldmann, and Y. Tagaya. 2002. IL-15Rα recycles and presents IL-15 in trans to neighboring cells. Immunity 17: 537-547.
47. Carson, W. E., M. E. Ross, R. A. Baiocchi, M. J. Marien, N. Boiani, K. Grabstein, and M. A. Caligiuri. 1995. Endogenous production of interleukin 15 by activated human monocytes is critical for optimal production of interferon-γ by natural killer cells in vitro. J. Clin. Invest. 96: 2578-2582.
48. Fehniger, T. A., M. H. Shah, M. J. Turner, J. B. VanDeusen, S. P. Whitman, M. A. Cooper, K. Suzuki, M. Wechser, F. Goodsaid, and M. A. Caligiuri. 1999. Differential cytokine and chemokine gene expression by human NK cells following activation with IL-18 or IL-15 in combination with IL-12: implications for the innate immune response. J. Immunol. 162: 4511-4520.
49. Sato, N., H. J. Patel, T. A. Waldmann, and Y. Tagaya. 2007. The IL-15/IL-15Rα on cell surfaces enables sustained IL-15 activity and contributes to the long survival of CD8 memory T cells. Proc. Natl. Acad. Sci. USA 104: 588-593.
50. Alpdogan, O., J. M. Eng, S. J. Muriglan, L. M. Willis, V. M. Hubbard, K. H. Tjoe, T. H. Terwey, A. Kochman, and M. R. van den Brink. 2005. Interleukin-15 enhances immune reconstitution after allogeneic bone marrow transplantation. Blood 105: 865-873.
51. Lucas, M., W. Schachterle, K. Oberle, P. Aichele, and A. Diefenbach. 2007. Dendritic cells prime natural killer cells by trans-presenting interleukin 15. Immunity 26: 503-517.
52. Martin-Fontecha, A., L. L. Thomsen, S. Brett, C. Gerard, M. Lipp, A. Lanzavecchia, and F. Sallusto. 2004. Induced recruitment of NK cells to lymph nodes provides IFN-γ for Th1 priming. Nat. Immunol. 5: 1260-1265.
53. Morandi, B., G. Bougras, W. A. Muller, G. Ferlazzo, and C. Munz. 2006. NK cells of human secondary lymphoid tissues enhance T cell polarization via IFN-γ secretion. Eur. J. Immunol. 36: 2394-2400.
54. Miller, J. S., Y. Soignier, A. Panoskaltsis-Mortari, S. A. McNearney, G. H. Yun, S. K. Fautsch, D. McKenna, C. Le, T. E. Defor, L. J. Burns, et al. 2005. Successful adoptive transfer and in vivo expansion of human haploidentical NK cells in patients with cancer. Blood 105: 3051-3057.
55. Pages, F., A. Berger, M. Camus, F. Sanchez-Cabo, A. Costes, R. Molidor, B. Mlecnik, A. Kirilovsky, M. Nilsson, D. Damotte, et al. 2005. Effector memory T cells, early metastasis, and survival in colorectal cancer. N. Engl. J. Med. 353: 2654-2666.