Natural killer cell tolerance persists despite significant reduction of self MHC class I on normal target cells in mice

PLoS ONE

Volumn 5, Issue 10, 2010, Pages

  Brodin, Petter ^a   Lakshmikanth, Tadepally ^a   Mehr, Ramit ^b   Johansson, Maria H ^a   Duru, Adil Doganay ^c   Achour, Adnane ^c   Salmon Divon, Mali ^b,e   Kärre, Klas ^a   Höglund, Petter ^a   Johansson, Sofia ^d  

^a KAROLINSKA INSTITUTE   (Sweden)

^b BAR ILAN UNIVERSITY   (Israel)

^c KAROLINSKA UNIVERSITY HOSPITAL   (Sweden)

^d ALBANOVA UNIVERSITY CENTER   (Sweden)

^e WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; NATURAL KILLER CELL LECTIN LIKE RECEPTOR SUBFAMILY A;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN EXPRESSION; ARTICLE; CELL INTERACTION; CELL SURFACE; CONTROLLED STUDY; HEMIZYGOTE; HOMOZYGOTE; HOST RESISTANCE; IMMUNOLOGICAL TOLERANCE; IN VIVO STUDY; MOUSE; NATURAL KILLER CELL; NONHUMAN; RECEPTOR DOWN REGULATION; TARGET CELL;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; CELL SEPARATION; FLOW CYTOMETRY; HISTOCOMPATIBILITY ANTIGENS CLASS I; KILLER CELLS, NATURAL; MICE; MICE, INBRED C57BL;

MURINAE; MUS;

EID: 78049273728     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0013174     Document Type: Article

References (54)

1. Lanier LL (2008) Up on the tightrope: natural killer cell activation and inhibition. Nat Immunol 9: 495-502.
2. Colucci F, Di Santo JP, Leibson PJ (2002) Natural killer cell activation in mice and men: different triggers for similar weapons? Nat Immunol 3: 807-813.
3. Kärre 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.
4. Cerwenka A, Bakker AB, McClanahan T, Wagner J, Wu J, et al. (2000) Retinoic acid early inducible genes define a ligand family for the activating NKG2D receptor in mice. Immunity 12: 721-727.
5. Diefenbach A, Jamieson AM, Liu SD, Shastri N, Raulet DH (2000) Ligands for the murine NKG2D receptor: expression by tumor cells and activation of NK cells and macrophages. Nat Immunol 1: 119-126.
6. Öberg L, Johansson S, Michaelsson J, Tomasello E, Vivier E, et al. (2004) Loss or mismatch of MHC class I is sufficient to trigger NK cell-mediated rejection of resting lymphocytes in vivo - role of KARAP/DAP12-dependent and - independent pathways. Eur J Immunol 34: 1646-1653.
7. Regunathan J, Chen Y, Wang D, Malarkannan S (2005) NKG2D receptormediated NK cell function is regulated by inhibitory Ly49 receptors. Blood 105: 233-240.
8. Dimasi N, Biassoni R (2005) Structural and functional aspects of the Ly49 natural killer cell receptors. Immunol Cell Biol 83: 1-8.
9. Long EO (2008) Negative signaling by inhibitory receptors: the NK cell paradigm. Immunol Rev 224: 70-84.
10. Kim S, Poursine-Laurent J, Truscott SM, Lybarger L, Song YJ, et al. (2005) Licensing of natural killer cells by host major histocompatibility complex class I molecules. Nature 436: 709-713.
11. Fernandez NC, Treiner E, Vance RE, Jamieson AM, Lemieux S, et al. (2005) A subset of natural killer cells achieve self-tolerance without expressing inhibitory receptors specific for self MHC molecules. Blood.
12. Höglund P, Ljunggren HG, öhlen C, Ahrlund-Richter L, Scangos G, et al. (1988) Natural resistance against lymphoma grafts conveyed by H-2Dd transgene to C57BL mice. J Exp Med 168: 1469-1474.
13. Öhlen C, Kling G, Höglund P, Hansson M, Scangos G, et al. (1989) Prevention of allogeneic bone marrow graft rejection by H-2 transgene in donor mice. Science 246: 666-668.
14. Held W, Raulet DH (1997) Expression of the Ly49A gene in murine natural killer cell clones is predominantly but not exclusively mono-allelic. Eur J Immunol 27: 2876-2884.
15. Johansson MH, Höglund E, Nakamura MC, Ryan JC, Höglund P (1998) Alpha1/alpha2 domains of H-2D(d), but not H-2L(d), induce ''missing self'' reactivity in vivo-no effect of H-2L(d) on protection against NK cells expressing the inhibitory receptor Ly49G2. Eur J Immunol 28: 4198-4206.
16. Johansson S, Johansson M, Rosmaraki E, Vahlne G, Mehr R, et al. (2005) Natural killer cell education in mice with single or multiple major histocompatibility complex class I molecules. J Exp Med 201: 1145-1155.
17. Brodin P, Lakshmikanth T, Johansson S, Kärre K, Höglund P (2009) The strength of inhibitory input during education quantitatively tunes the functional responsiveness of individual natural killer cells. Blood 113: 2434-2441.
18. Brodin P, Kärre K, Höglund P (2009) NK cell education: not an on-off switch but a tunable rheostat. Trends Immunol.
19. Doucey MA, Scarpellino L, Zimmer J, Guillaume P, Luescher IF, et al. (2004) Cis association of Ly49A with MHC class I restricts natural killer cell inhibition. Nat Immunol 5: 328-336.
20. Chalifour A, Scarpellino L, Back J, Brodin P, Devevre E, et al. (2009) A Role for cis Interaction between the Inhibitory Ly49A Receptor and MHC Class I for Natural Killer Cell Education. Immunity.
21. Kåse A, Johansson MH, Olsson-Alheim MY, Kä rre K, Höglund P (1998) External and internal calibration of the MHC class I-specific receptor Ly49A on murine natural killer cells. J Immunol 161: 6133-6138.
22. Andersson KE, Williams GS, Davis DM, Hoglund P (2007) Quantifying the reduction in accessibility of the inhibitory NK cell receptor Ly49A caused by binding MHC class I proteins in cis. Eur J Immunol 37: 516-527.
23. 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.
24. Nakamura MC, Hayashi S, Niemi EC, Ryan JC, Seaman WE (2000) Activating Ly-49D and inhibitory Ly-49A natural killer cell receptors demonstrate distinct requirements for interaction with H2-D(d). J Exp Med 192: 447-454.
25. Sundbäck J, Achour A, Michaëlsson J, Lindström H, Kärre K (2002) NK cell inhibitory receptor Ly-49C residues involved in MHC class I binding. J Immunol 168: 793-800.
26. Scarpellino L, Oeschger F, Guillaume P, Coudert JD, Levy F, et al. (2007) Interactions of Ly49 family receptors with MHC class I ligands in trans and cis. J Immunol 178: 1277-1284.
27. Almeida CR, Davis DM (2006) Segregation of HLA-C from ICAM-1 at NK cell immune synapses is controlled by its cell surface density. J Immunol 177: 6904-6910.
28. Storkus WJ, Alexander J, Payne JA, Dawson JR, Cresswell P (1989) Reversal of natural killing susceptibility in target cells expressing transfected class I HLA genes. Proc Natl Acad Sci U S A 86: 2361-2364.
29. Jonsson AH, Yang L, Kim S, Taffner SM, Yokoyama WM (2010) Effects of MHC class I alleles on licensing of Ly49A+ NK cells. J Immunol 184: 3424-3432.
30. Bieberich C, Scangos G, Tanaka K, Jay G (1986) Regulated expression of a murine class I gene in transgenic mice. Mol Cell Biol 6: 1339-1342.
31. Pascolo S, Bervas N, Ure JM, Smith AG, Lemonnier FA, et al. (1997) HLAA2.1-restricted education and cytolytic activity of CD8(+) T lymphocytes from beta2 microglobulin (beta2m) HLA-A2.1 monochain transgenic H-2Db beta2m double knockout mice. J Exp Med 185: 2043-2051.
32. Perarnau B, Saron MF, San Martin BR, Bervas N, Ong H, et al. (1999) Single H2Kb, H2Db and double H2KbDb knockout mice: peripheral CD8+ T cellrepertoire and anti-lymphocytic choriomeningitis virus cytolytic responses. Eur J Immunol 29: 1243-1252.
33. Vugmeyster Y, Glas R, Perarnau B, Lemonnier FA, Eisen H, et al. (1998) Major histocompatibility complex (MHC) class I KbDb -/- deficient mice possess functional CD8+ T cells and natural killer cells. Proc Natl Acad Sci U S A 95: 12492-12497.
34. Stringfellow DA, Glasgow LA (1972) Tilorone hydrochloride: an oral interferoninducing agent. Antimicrob Agents Chemother 2: 73-78.
35. Sijts AJ, De Bruijn ML, Ressing ME, Nieland JD, Mengede EA, et al. (1994) Identification of an H-2 Kb-presented Moloney murine leukemia virus cytotoxic T-lymphocyte epitope that displays enhanced recognition in H-2 Db mutant bm13 mice. J Virol 68: 6038-6046.
36. Gidlund M, Orn A, Wigzell H, Senik A, Gresser I (1978) Enhanced NK cell activity in mice injected with interferon and interferon inducers. Nature 273: 759-761.
37. Van Kaer L, Ashton-Rickardt PG, Ploegh HL, Tonegawa S (1992) TAP1 mutant mice are deficient in antigen presentation, surface class I molecules, and CD4-8+ T cells. Cell 71: 1205-1214.
38. van Stipdonk MJ, Badia-Martinez D, Sluijter M, Offringa R, van Hall T, et al. (2009) Design of agonistic altered peptides for the robust induction of CTL directed towards H-2Db in complex with the melanoma-associated epitope gp100. Cancer Res 69: 7784-7792.
39. Hanke T, Takizawa H, McMahon CW, Busch DH, Pamer EG, et al. (1999) Direct assessment of MHC class I binding by seven Ly49 inhibitory NK cell receptors. Immunity 11: 67-77.
40. Johansson S, Salmon-Divon M, Johansson MH, Pickman Y, Brodin P, et al. (2009) Probing natural killer cell education by Ly49 receptor expression analysis and computational modelling in single MHC class I mice. PLoS One 4: e6046.
41. Olsson-Alheim MY, Salcedo M, Ljunggren HG, Kärre K, Sentman CL (1997) NK cell receptor calibration: effects of MHC class I induction on killing by Ly49Ahigh and Ly49Alow NK cells. J Immunol 159: 3189-3194.
42. 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.
43. Carlyle JR, Jamieson AM, Gasser S, Clingan CS, Arase H, et al. (2004) Missing self-recognition of Ocil/Clr-b by inhibitory NKR-P1 natural killer cell receptors. Proc Natl Acad Sci U S A 101: 3527-3532.
44. Held W, Dorfman JR, Wu MF, Raulet DH (1996) Major histocompatibility complex class I-dependent skewing of the natural killer cell Ly49 receptor repertoire. Eur J Immunol 26: 2286-2292.
45. Back J, Chalifour A, Scarpellino L, Held W (2007) Stable masking by H-2Dd cis ligand limits Ly49A relocalization to the site of NK cell/target cell contact. Proc Natl Acad Sci U S A 104: 3978-3983.
46. Hoglund P, Glas R, Menard C, Kase A, Johansson MH, et al. (1998) Beta2-microglobulin-deficient NK cells show increased sensitivity to MHC class Imediated inhibition, but self tolerance does not depend upon target cell expression of H-2Kb and Db heavy chains. Eur J Immunol 28: 370-378.
47. Manilay JO, Waneck GL, Sykes M (1998) Altered expression of Ly-49 receptors on NK cells developing in mixed allogeneic bone marrow chimeras. Int Immunol 10: 1943-1955.
48. Andersson M, Freland S, Johansson MH, Wallin R, Sandberg JK, et al. (1998) MHC class I mosaic mice reveal insights into control of Ly49C inhibitory receptor expression in NK cells. J Immunol 161: 6475-6479.
49. Anfossi N, Andre P, Guia S, Falk CS, Roetynck S, et al. (2006) Human NK cell education by inhibitory receptors for MHC class I. Immunity 25: 331-342.
50. Sjöström A, Eriksson M, Cerboni C, Johansson MH, Sentman CL, et al. (2001) Acquisition of external major histocompatibility complex class I molecules by natural killer cells expressing inhibitory Ly49 receptors. J Exp Med 194: 1519-1530.
51. Zimmer J, Ioannidis V, Held W (2001) H-2D ligand expression by Ly49A+natural killer (NK) cells precludes ligand uptake from environmental cells: implications for NK cell function. J Exp Med 194: 1531-1539.
52. Back J, Malchiodi EL, Cho S, Scarpellino L, Schneider P, et al. (2009) Distinct conformations of Ly49 natural killer cell receptors mediate MHC class I recognition in trans and cis. Immunity 31: 598-608.
53. Vahlne G, Lindholm K, Meier A, Wickström S, Lakshmikanth T, et al. (2010) In vivo tumor cell rejection induced by NK cell inhibitory receptor blockade: maintained tolerance to normal cells even in the presence of IL-2. Eur J Immunol 40: 813-823.
54. Joncker NT, Raulet DH (2008) Regulation of NK cell responsiveness to achieve self-tolerance and maximal responses to diseased target cells. Immunol Rev 224: 85-97.