Skip to main content

Advertisement

SpringerLink
Log in

Stromal-cell regulation of natural killer cell differentiation

  • Review
  • Published:
Journal of Molecular Medicine Aims and scope Submit manuscript

Abstract

Natural killer (NK) cells are bone-marrow-derived lymphocytes that play a crucial role in host defense against some viral and bacterial infections, as well as against tumors. Their phenotypic and functional maturation requires intimate interactions between the bone marrow stroma and committed precursors. In parallel to the identification of several phenotypic and functional stages of NK cell development, recent studies have shed new light on the role of stromal cells in driving functional maturation of NK cells. In this review, we provide an overview of the role of bone marrow microenvironment in NK cell differentiation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  1. Herberman RB, Nunn ME, Holden HT, Lavrin DH (1975) Natural cytotoxic reactivity of mouse lymphoid cells against syngeneic and allogeneic tumors. II. Characterization of effector cells. Int J Cancer 16:230–239

    PubMed  CAS  Google Scholar 

  2. French AR, Yokoyama WM (2003) Natural killer cells and viral infections. Curr Opin Immunol 15:45–51

    PubMed  CAS  Google Scholar 

  3. Lodoen MB, Lanier LL (2006) Natural killer cells as an initial defense against pathogens. Curr Opin Immunol 18:391–398

    PubMed  CAS  Google Scholar 

  4. Ruggeri L, Aversa F, Martelli MF, Velardi A (2006) Allogeneic hematopoietic transplantation and natural killer cell recognition of missing self. Immunol Rev 214:202–218

    PubMed  CAS  Google Scholar 

  5. Moffett-King A (2002) Natural killer cells and pregnancy. Nat Rev Immunol 2:656–663

    PubMed  CAS  Google Scholar 

  6. Anne Croy B, van den Heuvel MJ, Borzychowski AM, Tayade C (2006) Uterine natural killer cells: a specialized differentiation regulated by ovarian hormones. Immunol Rev 214:161–185

    PubMed  CAS  Google Scholar 

  7. Screpanti V, Wallin RP, Ljunggren HG, Grandien A (2001) A central role for death receptor-mediated apoptosis in the rejection of tumors by NK cells. J Immunol 167:2068–2073

    PubMed  CAS  Google Scholar 

  8. Smyth MJ, Cretney E, Kelly JM, Westwood JA, Street SE, Yagita H, Takeda K, van Dommelen SL, Degli-Esposti MA, Hayakawa Y (2005) Activation of NK cell cytotoxicity. Mol Immunol 42:501–510

    PubMed  CAS  Google Scholar 

  9. Takeda K, Cretney E, Hayakawa Y, Ota T, Akiba H, Ogasawara K, Yagita H, Kinoshita K, Okumura K, Smyth MJ (2005) TRAIL identifies immature natural killer cells in newborn mice and adult mouse liver. Blood 105:2082–2089

    PubMed  CAS  Google Scholar 

  10. Anegon I, Cuturi MC, Trinchieri G, Perussia B (1988) Interaction of Fc receptor (CD16) ligands induces transcription of interleukin 2 receptor (CD25) and lymphokine genes and expression of their products in human natural killer cells. J Exp Med 167:452–472

    PubMed  CAS  Google Scholar 

  11. Arase H, Arase N, Saito T (1996) Interferon gamma production by natural killer (NK) cells and NK1.1+ T cells upon NKR-P1 cross-linking. J Exp Med 183:2391–2396

    PubMed  CAS  Google Scholar 

  12. Kim S, Yokoyama WM (1998) NK cell granule exocytosis and cytokine production inhibited by Ly-49A engagement. Cell Immunol 183:106–112

    PubMed  CAS  Google Scholar 

  13. Ho EL, Carayannopoulos LN, Poursine-Laurent J, Kinder J, Plougastel B, Smith HR, Yokoyama WM (2002) Costimulation of multiple NK cell activation receptors by NKG2D. J Immunol 169:3667–3675

    PubMed  CAS  Google Scholar 

  14. Gosselin P, Mason LH, Willette-Brown J, Ortaldo JR, McVicar DW, Anderson SK (1999) Induction of DAP12 phosphorylation, calcium mobilization, and cytokine secretion by Ly49H. J Leukoc Biol 66:165–171

    PubMed  CAS  Google Scholar 

  15. Ortaldo JR, Young HA (2003) Expression of IFN-gamma upon triggering of activating Ly49D NK receptors in vitro and in vivo: costimulation with IL-12 or IL-18 overrides inhibitory receptors. J Immunol 170:1763–1769

    PubMed  CAS  Google Scholar 

  16. Smith HR, Heusel JW, Mehta IK, Kim S, Dorner BG, Naidenko OV, Iizuka K, Furukawa H, Beckman DL, Pingel JT, Scalzo AA, Fremont DH, Yokoyama WM (2002) Recognition of a virus-encoded ligand by a natural killer cell activation receptor. Proc Natl Acad Sci USA 99:8826–8831

    PubMed  CAS  Google Scholar 

  17. Raulet DH, Vance RE, McMahon CW (2001) Regulation of the natural killer cell receptor repertoire. Annu Rev Immunol 19:291–330

    PubMed  CAS  Google Scholar 

  18. Vivier E, Nunes JA, Vely F (2004) Natural killer cell signaling pathways. Science 306:1517–1519

    PubMed  CAS  Google Scholar 

  19. Lanier LL (2005) NK cell recognition. Annu Rev Immunol 23:225–274

    PubMed  CAS  Google Scholar 

  20. Karre K, Ljunggren HG, Piontek G, Kiessling R (1986) Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defence strategy. Nature 319:675–678

    PubMed  CAS  Google Scholar 

  21. Iizuka K, Naidenko OV, Plougastel BF, Fremont DH, Yokoyama WM (2003) Genetically linked C-type lectin-related ligands for the NKRP1 family of natural killer cell receptors. Nat Immunol 4:801–807

    PubMed  CAS  Google Scholar 

  22. Carlyle JR, Jamieson AM, Gasser S, Clingan CS, Arase H, Raulet DH (2004) Missing self-recognition of Ocil/Clr-b by inhibitory NKR-P1 natural killer cell receptors. Proc Natl Acad Sci USA 101:3527–3532

    PubMed  CAS  Google Scholar 

  23. Brown MH, Boles K, van der Merwe PA, Kumar V, Mathew PA, Barclay AN (1998) 2B4, the natural killer and T cell immunoglobulin superfamily surface protein, is a ligand for CD48. J Exp Med 188:2083–2090

    PubMed  CAS  Google Scholar 

  24. McNerney ME, Guzior D, Kumar V (2005) 2B4 (CD244) - CD48 interactions provide a novel MHC class I-independent system for NK cell self-tolerance in mice. Blood 106:1337–1340

    PubMed  CAS  Google Scholar 

  25. Diefenbach A, Raulet DH (2002) The innate immune response to tumors and its role in the induction of T-cell immunity. Immunol Rev 188:9–21

    PubMed  CAS  Google Scholar 

  26. Yokoyama WM, Plougastel BF (2003) Immune functions encoded by the natural killer gene complex. Nat Rev Immunol 3:304–316

    PubMed  CAS  Google Scholar 

  27. Raulet DH (2003) Roles of the NKG2D immunoreceptor and its ligands. Nat Rev Immunol 3:781–790

    PubMed  CAS  Google Scholar 

  28. Carayannopoulos LN, Yokoyama WM (2004) Recognition of infected cells by natural killer cells. Curr Opin Immunol 16:26–33

    PubMed  CAS  Google Scholar 

  29. Di Santo JP (2006) Natural killer cell developmental patways: A Question of Balance. Annu Rev Immunol 24:257–286

    PubMed  Google Scholar 

  30. Huard B, Tournier M, Triebel F (1998) LAG-3 does not define a specific mode of natural killing in human. Immunol Lett 61:109–112

    PubMed  CAS  Google Scholar 

  31. Cooper MA, Fehniger TA, Caligiuri MA (2001) The biology of human natural killer-cell subsets. Trends Immunol 22:633–640

    PubMed  CAS  Google Scholar 

  32. Haller O, Wigzell H (1977) Suppression of natural killer cell activity with radioactive strontium: effector cells are marrow dependent. J Immunol 118:1503–1506

    PubMed  CAS  Google Scholar 

  33. Kumar V, Ben-Ezra J, Bennett M, Sonnenfeld G (1979) Natural killer cells in mice treated with 89strontium: normal target-binding cell numbers but inability to kill even after interferon administration. J Immunol 123:1832–1838

    PubMed  CAS  Google Scholar 

  34. Moore T, Bennett M, Kumar V (1995) Transplantable NK cell progenitors in murine bone marrow. J Immunol 154:1653–1663

    PubMed  CAS  Google Scholar 

  35. Dorshkind K, Pollack SB, Bosma MJ, Phillips RA (1985) Natural killer (NK) cells are present in mice with severe combined immunodeficiency (SCID). J Immunol 134:3798–3801

    PubMed  CAS  Google Scholar 

  36. Hackett J Jr, Bosma GC, Bosma MJ, Bennett M, Kumar V (1986) Transplantable progenitors of natural killer cells are distinct from those of T and B lymphocytes. Proc Natl Acad Sci USA 83:3427–3431

    PubMed  Google Scholar 

  37. Mombaerts P, Iacomini J, Johnson RS, Herrup K, Tonegawa S, Papaioannou VE (1992) RAG-1-deficient mice have no mature B and T lymphocytes. Cell 68:869–877

    PubMed  CAS  Google Scholar 

  38. Shinkai Y, Rathbun G, Lam KP, Oltz EM, Stewart V, Mendelsohn M, Charron J, Datta M, Young F, Stall AM et al (1992) RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement. Cell 68:855–867

    PubMed  CAS  Google Scholar 

  39. Lian RH, Kumar V (2002) Murine natural killer cell progenitors and their requirements for development. Semin Immunol 14:453–460

    PubMed  CAS  Google Scholar 

  40. Moretta A, Bottino C, Vitale M, Pende D, Cantoni C, Mingari MC, Biassoni R, Moretta L (2001) Activating receptors and coreceptors involved in human natural killer cell-mediated cytolysis. Annu Rev Immunol 19:197–223

    PubMed  CAS  Google Scholar 

  41. Kim S, Iizuka K, Kang HS, Dokun A, French AR, Greco S, Yokoyama WM (2002) In vivo developmental stages in murine natural killer cell maturation. Nat Immunol 3:523–528

    PubMed  Google Scholar 

  42. Fernandez NC, Treiner E, Vance RE, Jamieson AM, Lemieux S, Raulet DH (2005) A subset of natural killer cells achieve self-tolerance without expressing inhibitory receptors specific for self MHC molecules. Blood 105:4416–4423

    PubMed  CAS  Google Scholar 

  43. Raulet DH, Vance RE (2006) Self-tolerance of natural killer cells. Nat Rev Immunol 6:520–531

    PubMed  CAS  Google Scholar 

  44. Kim S, Poursine-Laurent J, Truscott SM, Lybarger L, Song YJ, Yang L, French AR, Sunwoo JB, Lemieux S, Hansen TH, Yokoyama WM (2005) Licensing of natural killer cells by host major histocompatibility complex class I molecules. Nature 436:709–713

    PubMed  CAS  Google Scholar 

  45. Yokoyama WM, Kim S (2006) How do natural killer cells find self to achieve tolerance? Immunity 24:249–257

    PubMed  CAS  Google Scholar 

  46. Rodewald HR, Moingeon P, Lucich JL, Dosiou C, Lopez P, Reinherz EL (1992) A population of early fetal thymocytes expressing Fc gamma RII/III contains precursors of T lymphocytes and natural killer cells. Cell 69:139–150

    PubMed  CAS  Google Scholar 

  47. Carlyle JR, Michie AM, Furlonger C, Nakano T, Lenardo MJ, Paige CJ, Zuniga-Pflucker JC (1997) Identification of a novel developmental stage marking lineage commitment of progenitor thymocytes. J Exp Med 186:173–182

    PubMed  CAS  Google Scholar 

  48. Carlyle JR, Michie AM, Cho SK, Zuniga-Pflucker JC (1998) Natural killer cell development and function precede alpha beta T cell differentiation in mouse fetal thymic ontogeny. J Immunol 160:744–753

    PubMed  CAS  Google Scholar 

  49. Carlyle JR, Zuniga-Pflucker JC (1998) Requirement for the thymus in alphabeta T lymphocyte lineage commitment. Immunity 9:187–197

    PubMed  CAS  Google Scholar 

  50. Michie AM, Carlyle JR, Schmitt TM, Ljutic B, Cho SK, Fong Q, Zuniga-Pflucker JC (2000) Clonal characterization of a bipotent T cell and NK cell progenitor in the mouse fetal thymus. J Immunol 164:1730–1733

    PubMed  CAS  Google Scholar 

  51. Douagi I, Colucci F, Di Santo JP, Cumano A (2002) Identification of the earliest prethymic bipotent T/NK progenitor in murine fetal liver. Blood 99:463–471

    PubMed  CAS  Google Scholar 

  52. Schmitt TM, Ciofani M, Petrie HT, Zuniga-Pflucker JC (2004) Maintenance of T cell specification and differentiation requires recurrent notch receptor-ligand interactions. J Exp Med 200:469–479

    PubMed  CAS  Google Scholar 

  53. Porritt HE, Rumfelt LL, Tabrizifard S, Schmitt TM, Zuniga-Pflucker JC, Petrie HT (2004) Heterogeneity among DN1 prothymocytes reveals multiple progenitors with different capacities to generate T cell and non-T cell lineages. Immunity 20:735–745

    PubMed  CAS  Google Scholar 

  54. Franki AS, Van Beneden K, Dewint P, Meeus I, Veys E, Deforce D, Elewaut D (2005) Lymphotoxin alpha 1 beta 2: a critical mediator in V alpha 14i NKT cell differentiation. Mol Immunol 42:413–417

    PubMed  CAS  Google Scholar 

  55. Freud AG, Becknell B, Roychowdhury S, Mao HC, Ferketich AK, Nuovo GJ, Hughes TL, Marburger TB, Sung J, Baiocchi RA, Guimond M, Caligiuri MA (2005) A human CD34(+) subset resides in lymph nodes and differentiates into CD56bright natural killer cells. Immunity 22:295–304

    PubMed  CAS  Google Scholar 

  56. Vosshenrich CA, Samson-Villeger SI, Di Santo JP (2005) Distinguishing features of developing natural killer cells. Curr Opin Immunol 17:151–158

    PubMed  CAS  Google Scholar 

  57. Vosshenrich CA, Garcia-Ojeda ME, Samson-Villeger SI, Pasqualetto V, Enault L, Goff OR, Corcuff E, Guy-Grand D, Rocha B, Cumano A, Rogge L, Ezine S, Di Santo JP (2006) A thymic pathway of mouse natural killer cell development characterized by expression of GATA-3 and CD127. Nat Immunol 7:1217–1224

    PubMed  CAS  Google Scholar 

  58. Smyth MJ, Nutt SL (2006) IL-7 and the thymus dictate the NK cell ‘labor market’. Nat Immunol 7:1134–1136

    PubMed  CAS  Google Scholar 

  59. Samson SI, Richard O, Tavian M, Ranson T, Vosshenrich CA, Colucci F, Buer J, Grosveld F, Godin I, Di Santo JP (2003) GATA-3 promotes maturation, IFN-gamma production, and liver-specific homing of NK Cells. Immunity 19:701–711

    PubMed  CAS  Google Scholar 

  60. Hayakawa Y, Smyth MJ (2006) CD27 Dissects mature NK cells into two subsets with distinct responsiveness and migratory capacity. J Immunol 176:1517–1524

    PubMed  CAS  Google Scholar 

  61. Martin-Fontecha A, Thomsen LL, Brett S, Gerard C, Lipp M, Lanzavecchia A, Sallusto F (2004) Induced recruitment of NK cells to lymph nodes provides IFN-gamma for T(H)1 priming. Nat Immunol 5:1260–1265

    PubMed  CAS  Google Scholar 

  62. Seaman WE, Gindhart TD, Greenspan JS, Blackman MA, Talal N (1979) Natural killer cells, bone, and the bone marrow: studies in estrogen-treated mice and in congenitally osteopetrotic (mi/mi) mice. J Immunol 122:2541–2547

    PubMed  CAS  Google Scholar 

  63. Hackett J Jr, Bennett M, Kumar V (1985) Origin and differentiation of natural killer cells. I. Characteristics of a transplantable NK cell precursor. J Immunol 134:3731–3738

    PubMed  Google Scholar 

  64. Hackett J Jr, Bennett M, Koo GC, Kumar V (1986) Origin and differentiation of natural killer cells. III. Relationship between the precursors and effectors of natural killer and natural cytotoxic activity. Immunol Res 5:16–24

    Article  PubMed  Google Scholar 

  65. Medina KL, Garrett KP, Thompson LF, Rossi MI, Payne KJ, Kincade PW (2001) Identification of very early lymphoid precursors in bone marrow and their regulation by estrogen. Nat Immunol 2:718–724

    PubMed  CAS  Google Scholar 

  66. Igarashi H, Gregory SC, Yokota T, Sakaguchi N, Kincade PW (2002) Transcription from the RAG1 locus marks the earliest lymphocyte progenitors in bone marrow. Immunity 17:117–130

    PubMed  CAS  Google Scholar 

  67. Adolfsson J, Mansson R, Buza-Vidas N, Hultquist A, Liuba K, Jensen CT, Bryder D, Yang L, Borge OJ, Thoren LA, Anderson K, Sitnicka E, Sasaki Y, Sigvardsson M, Jacobsen SE (2005) Identification of Flt3+ lympho-myeloid stem cells lacking erythro-megakaryocytic potential a revised road map for adult blood lineage commitment. Cell 121:295–306

    PubMed  CAS  Google Scholar 

  68. Kondo M, Weissman IL, Akashi K (1997) Identification of clonogenic common lymphoid progenitors in mouse bone marrow. Cell 91:661–672

    PubMed  CAS  Google Scholar 

  69. Waskow C, Paul S, Haller C, Gassmann M, Rodewald HR (2002) Viable c-Kit(W/W) mutants reveal pivotal role for c-kit in the maintenance of lymphopoiesis. Immunity 17:277–288

    PubMed  CAS  Google Scholar 

  70. Waskow C, Rodewald HR (2002) Lymphocyte development in neonatal and adult c-Kit-deficient (c-KitW/W) mice. Adv Exp Med Biol 512:1–10

    PubMed  CAS  Google Scholar 

  71. Iizuka K, Chaplin DD, Wang Y, Wu Q, Pegg LE, Yokoyama WM, Fu YX (1999) Requirement for membrane lymphotoxin in natural killer cell development. Proc Natl Acad Sci USA 96:6336–6340

    PubMed  CAS  Google Scholar 

  72. Rosmaraki EE, Douagi I, Roth C, Colucci F, Cumano A, Di Santo JP (2001) Identification of committed NK cell progenitors in adult murine bone marrow. Eur J Immunol 31:1900–1909

    PubMed  CAS  Google Scholar 

  73. Yokoyama WM, Kim S, French AR (2004) The dynamic life of natural killer cells. Annu Rev Immunol 22:405–429

    PubMed  CAS  Google Scholar 

  74. Hayakawa Y, Huntington ND, Nutt SL, Smyth MJ (2006) Functional subsets of mouse natural killer cells. Immunol Rev 214:47–55

    PubMed  CAS  Google Scholar 

  75. Freud AG, Caligiuri MA (2006) Human natural killer cell development. Immunol Rev 214:56–72

    PubMed  CAS  Google Scholar 

  76. Jamieson AM, Isnard P, Dorfman JR, Coles MC, Raulet DH (2004) Turnover and proliferation of NK cells in steady state and lymphopenic conditions. J Immunol 172:864–870

    PubMed  CAS  Google Scholar 

  77. Vosshenrich CA, Ranson T, Samson SI, Corcuff E, Colucci F, Rosmaraki EE, Di Santo JP (2005) Roles for common cytokine receptor gamma-chain-dependent cytokines in the generation, differentiation, and maturation of NK cell precursors and peripheral NK cells in vivo. J Immunol 174:1213–1221

    PubMed  CAS  Google Scholar 

  78. Miller JS, Alley KA, McGlave P (1994) Differentiation of natural killer (NK) cells from human primitive marrow progenitors in a stroma-based long-term culture system: identification of a CD34+7+ NK progenitor. Blood 83:2594–2601

    PubMed  CAS  Google Scholar 

  79. Delfino DV, Patrene KD, Lu J, Deleo A, Deleo R, Herberman RB, Boggs SS (1996) Natural killer cell precursors in the CD44neg/dim T-cell receptor population of mouse bone marrow. Blood 87:2394–2400

    PubMed  CAS  Google Scholar 

  80. Wu Q, Sun Y, Wang J, Lin X, Wang Y, Pegg LE, Futterer A, Pfeffer K, Fu YX (2001) Signal via lymphotoxin-beta R on bone marrow stromal cells is required for an early checkpoint of NK cell development. J Immunol 166:1684–1689

    PubMed  CAS  Google Scholar 

  81. Lee KN, Kang HS, Jeon JH, Kim EM, Yoon SR, Song H, Lyu CY, Piao ZH, Kim SU, Han YH, Song SS, Lee YH, Song KS, Kim YM, Yu DY, Choi I (2005) VDUP1 is required for the development of natural killer cells. Immunity 22:195–208

    PubMed  CAS  Google Scholar 

  82. Townsend MJ, Weinmann AS, Matsuda JL, Salomon R, Farnham PJ, Biron CA, Gapin L, Glimcher LH (2004) T-bet regulates the terminal maturation and homeostasis of NK and Valpha14i NKT cells. Immunity 20:477–494

    PubMed  CAS  Google Scholar 

  83. Taki S, Nakajima S, Ichikawa E, Saito T, Hida S (2005) IFN regulatory factor-2 deficiency revealed a novel checkpoint critical for the generation of peripheral NK cells. J Immunol 174:6005–6012

    PubMed  CAS  Google Scholar 

  84. Lacorazza HD, Miyazaki Y, Di Cristofano A, Deblasio A, Hedvat C, Zhang J, Cordon-Cardo C, Mao S, Pandolfi PP, Nimer SD (2002) The ETS protein MEF plays a critical role in perforin gene expression and the development of natural killer and NK-T cells. Immunity 17:437–449

    PubMed  CAS  Google Scholar 

  85. Ito A, Kataoka TR, Kim DK, Koma Y, Lee YM, Kitamura Y (2001) Inhibitory effect on natural killer activity of microphthalmia transcription factor encoded by the mutant mi allele of mice. Blood 97:2075–2083

    PubMed  CAS  Google Scholar 

  86. Kaisho T, Tsutsui H, Tanaka T, Tsujimura T, Takeda K, Kawai T, Yoshida N, Nakanishi K, Akira S (1999) Impairment of natural killer cytotoxic activity and interferon gamma production in CCAAT/enhancer binding protein gamma-deficient mice. J Exp Med 190:1573–1582

    PubMed  CAS  Google Scholar 

  87. Roth C, Carlyle JR, Takizawa H, Raulet DH (2000) Clonal acquisition of inhibitory Ly49 receptors on developing NK cells is successively restricted and regulated by stromal class I MHC. Immunity 13:143–153

    PubMed  CAS  Google Scholar 

  88. Williams NS, Kubota A, Bennett M, Kumar V, Takei F (2000) Clonal analysis of NK cell development from bone marrow progenitors in vitro: orderly acquisition of receptor gene expression. Eur J Immunol 30:2074–2082

    PubMed  CAS  Google Scholar 

  89. Dorfman JR, Raulet DH (1998) Acquisition of Ly49 receptor expression by developing natural killer cells. J Exp Med 187:609–618

    PubMed  CAS  Google Scholar 

  90. Stevenaert F, Van Beneden K, De Creus A, Debacker V, Plum J, Leclercq G (2003) Ly49E expression points toward overlapping, but distinct, natural killer (NK) cell differentiation kinetics and potential of fetal versus adult lymphoid progenitors. J Leukoc Biol 73:731–738

    PubMed  CAS  Google Scholar 

  91. Tanamachi DM, Moniot DC, Cado D, Liu SD, Hsia JK, Raulet DH (2004) Genomic Ly49A transgenes: basis of variegated Ly49A gene expression and identification of a critical regulatory element. J Immunol 172:1074–1082

    PubMed  CAS  Google Scholar 

  92. Saleh A, Davies GE, Pascal V, Wright PW, Hodge DL, Cho EH, Lockett SJ, Abshari M, Anderson SK (2004) Identification of probabilistic transcriptional switches in the Ly49 gene cluster: a eukaryotic mechanism for selective gene activation. Immunity 21:55–66

    PubMed  CAS  Google Scholar 

  93. Pascal V, Stulberg MJ, Anderson SK (2006) Regulation of class I major histocompatibility complex receptor expression in natural killer cells: one promoter is not enough! Immunol Rev 214:9–21

    PubMed  CAS  Google Scholar 

  94. Held W, Kunz B, Lowin-Kropf B, van de Wetering M, Clevers H (1999) Clonal acquisition of the Ly49A NK cell receptor is dependent on the trans-acting factor TCF-1. Immunity 11:433–442

    PubMed  CAS  Google Scholar 

  95. Kunz B, Held W (2001) Positive and negative roles of the trans-acting T cell factor-1 for the acquisition of distinct Ly-49 MHC class I receptors by NK cells. J Immunol 166:6181–6187

    PubMed  CAS  Google Scholar 

  96. Held W, Clevers H, Grosschedl R (2003) Redundant functions of TCF-1 and LEF-1 during T and NK cell development, but unique role of TCF-1 for Ly49 NK cell receptor acquisition. Eur J Immunol 33:1393–1398

    PubMed  CAS  Google Scholar 

  97. Kennedy MK, Glaccum M, Brown SN, Butz EA, Viney JL, Embers M, Matsuki N, Charrier K, Sedger L, Willis CR, Brasel K, Morrissey PJ, Stocking K, Schuh JC, Joyce S, Peschon JJ (2000) Reversible defects in natural killer and memory CD8 T cell lineages in interleukin 15-deficient mice. J Exp Med 191:771–780

    PubMed  CAS  Google Scholar 

  98. Cooper MA, Bush JE, Fehniger TA, VanDeusen JB, Waite RE, Liu Y, Aguila HL, Caligiuri MA (2002) In vivo evidence for a dependence on interleukin 15 for survival of natural killer cells. Blood 100:3633–3638

    PubMed  CAS  Google Scholar 

  99. Prlic M, Blazar BR, Farrar MA, Jameson SC (2003) In vivo survival and homeostatic proliferation of natural killer cells. J Exp Med 197:967–976

    PubMed  CAS  Google Scholar 

  100. Koka R, Burkett PR, Chien M, Chai S, Chan F, Lodolce JP, Boone DL, Ma A (2003) Interleukin (IL)-15R{alpha}-deficient natural killer cells survive in normal but not IL-15R{alpha}-deficient mice. J Exp Med 197:977–984

    PubMed  CAS  Google Scholar 

  101. Dubois S, Mariner J, Waldmann TA, Tagaya Y (2002) IL-15Ralpha recycles and presents IL-15 In trans to neighboring cells. Immunity 17:537–547

    PubMed  CAS  Google Scholar 

  102. Kawamura T, Koka R, Ma A, Kumar V (2003) Differential roles for IL-15R alpha-chain in NK cell development and Ly-49 induction. J Immunol 171:5085–5090

    PubMed  CAS  Google Scholar 

  103. Lian RH, Chin RK, Nemeth HE, Libby SL, Fu YX, Kumar V (2004) A role for lymphotoxin in the acquisition of Ly49 receptors during NK cell development. Eur J Immunol 34:2699–2707

    PubMed  CAS  Google Scholar 

  104. Stevenaert F, Van Beneden K, De Colvenaer V, Franki AS, Debacker V, Boterberg T, Deforce D, Pfeffer K, Plum J, Elewaut D, Leclercq G (2005) Ly49 and CD94/NKG2 receptor acquisition by NK cells does not require lymphotoxin-{beta} receptor expression. Blood 106:956–962

    PubMed  CAS  Google Scholar 

  105. Liao NS, Bix M, Zijlstra M, Jaenisch R, Raulet D (1991) MHC class I deficiency: susceptibility to natural killer (NK) cells and impaired NK activity. Science 253:199–202

    PubMed  CAS  Google Scholar 

  106. Zimmer J, Donato L, Hanau D, Cazenave JP, Tongio MM, Moretta A, de la Salle H (1998) Activity and phenotype of natural killer cells in peptide transporter (TAP)-deficient patients (type I bare lymphocyte syndrome). J Exp Med 187:117–122

    PubMed  CAS  Google Scholar 

  107. Dorfman JR, Zerrahn J, Coles MC, Raulet DH (1997) The basis for self-tolerance of natural killer cells in beta2-microglobulin- and TAP-1- mice. J Immunol 159:5219–5225

    PubMed  CAS  Google Scholar 

  108. Anfossi N, Andre P, Guia S, Falk CS, Roetynck S, Stewart CA, Breso V, Frassati C, Reviron D, Middleton D, Romagne F, Ugolini S, Vivier E (2006) Human NK cell education by inhibitory receptors for MHC class I. Immunity 25:331–342

    PubMed  CAS  Google Scholar 

  109. Yokoyama WM, Kim S (2006) Licensing of natural killer cells by self-major histocompatibility complex class I. Immunol Rev 214:143–154

    PubMed  CAS  Google Scholar 

  110. Tassi I, Presti R, Kim S, Yokoyama WM, Gilfillan S, Colonna M (2005) Phospholipase C-gamma 2 is a critical signaling mediator for murine NK cell activating receptors. J Immunol 175:749–754

    PubMed  CAS  Google Scholar 

  111. Caraux A, Kim N, Bell SE, Zompi S, Ranson T, Lesjean-Pottier S, Garcia-Ojeda ME, Turner M, Colucci F (2006) Phospholipase C-gamma2 is essential for NK cell cytotoxicity and innate immunity to malignant and virally infected cells. Blood 107:994–1002

    PubMed  CAS  Google Scholar 

  112. Caraux A, Lu Q, Fernandez N, Riou S, Di Santo JP, Raulet DH, Lemke G, Roth C (2006) Natural killer cell differentiation driven by Tyro3 receptor tyrosine kinases. Nat Immunol 7:747–754

    PubMed  CAS  Google Scholar 

  113. Stitt TN, Conn G, Gore M, Lai C, Bruno J, Radziejewski C, Mattsson K, Fisher J, Gies DR, Jones PF et al (1995) The anticoagulation factor protein S and its relative, Gas6, are ligands for the Tyro 3/Axl family of receptor tyrosine kinases. Cell 80:661–670

    PubMed  CAS  Google Scholar 

  114. Lai C, Lemke G (1991) An extended family of protein-tyrosine kinase genes differentially expressed in the vertebrate nervous system. Neuron 6:691–704

    PubMed  CAS  Google Scholar 

  115. Lai C, Gore M, Lemke G (1994) Structure, expression, and activity of Tyro 3, a neural adhesion-related receptor tyrosine kinase. Oncogene 9:2567–2578

    PubMed  CAS  Google Scholar 

  116. Graham DK, Dawson TL, Mullaney DL, Snodgrass HR, Earp HS (1994) Cloning and mRNA expression analysis of a novel human protooncogene, c-mer. Cell Growth Differ 5:647–657

    PubMed  CAS  Google Scholar 

  117. Lu Q, Lemke G (2001) Homeostatic regulation of the immune system by receptor tyrosine kinases of the Tyro 3 family. Science 293:306–311

    PubMed  CAS  Google Scholar 

  118. Lemke G, Lu Q (2003) Macrophage regulation by Tyro 3 family receptors. Curr Opin Immunol 15:31–36

    PubMed  CAS  Google Scholar 

  119. Hafizi S, Dahlback B (2006) Gas6 and protein S. Vitamin K-dependent ligands for the Axl receptor tyrosine kinase subfamily. FEBS J 273:5231–5244

    PubMed  CAS  Google Scholar 

  120. Walzer T, Vivier E (2006) NK cell development: gas matters. Nat Immunol 7:702–704

    PubMed  CAS  Google Scholar 

  121. Budagian V, Bulanova E, Orinska Z, Thon L, Mamat U, Bellosta P, Basilico C, Adam D, Paus R, Bulfone-Paus S (2005) A promiscuous liaison between IL-15 receptor and Axl receptor tyrosine kinase in cell death control. EMBO J 24:4260–4270

    PubMed  CAS  Google Scholar 

  122. Hafizi S, Dahlback B (2006) Signalling and functional diversity within the Axl subfamily of receptor tyrosine kinases. Cytokine Growth Factor Rev 17:295–304

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratoire Immunité Cellulaire Antivirale, Département d’Immunologie, Institut Pasteur, 75724, Paris Cedex 15, France

    Claude Roth & Sylvain Riou

  2. Molecular Neurobiology Laboratory, The Salk Institute, La Jolla, CA, 92037, USA

    Carla Rothlin & Greg Lemke

  3. Department of Molecular and Cell Biology and Cancer Research Laboratory, University of California Berkeley, Berkeley, CA, 94720-3200, USA

    David H. Raulet

  4. Cancer Research Laboratory, University of California Berkeley, Berkeley, CA, 94720-3200, USA

    David H. Raulet

Authors
  1. Claude Roth
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Carla Rothlin
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sylvain Riou
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. David H. Raulet
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Greg Lemke
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Claude Roth.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Roth, C., Rothlin, C., Riou, S. et al. Stromal-cell regulation of natural killer cell differentiation. J Mol Med 85, 1047–1056 (2007). https://doi.org/10.1007/s00109-007-0195-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00109-007-0195-0

Keywords

Search

Navigation