Chapter 4 : NK Cells as a Barrier to Xenotransplantation

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The use of heterologous species for clinical transplantation has attracted increasing interest in recent years due to the shortage of human donors, resulting in significant progress toward the understanding of the mechanisms leading to recognition and rejection of xenogeneic grafts. Analysis of the leukocyte infiltrates found in tissues undergoing delayed xenograft rejection (DXR) has led to the identification of natural killer (NK) lymphocytes as an important effector cell subset. This paper focuses on the role of NK cells in xenogeneic graft rejection, on the biology of NK cells, and on NK-cell receptors in particular. NK cells contribute to the natural host defense mechanisms, both by exerting cytotoxicity on certain virally infected or tumor cells and by releasing cytokines that promote an inflammatory response, such as γ-interferon (IFN), tumor necrosis factor (TNF), granulocyte/macrophage-colony stimulating factor, and macrophage colony-stimulating factor. During NK-cell ontogeny, the CD34 surface antigen is lost and cells acquire the expression of membrane markers characteristic of mature NK cells (CD2, CD 16, CD56) . Chimerism induced by donor-specific bone marrow transplantation has been shown to produce alio- and xenotolerance, even across a discordant barrier, with evidence of NK as well as T- and B-cell tolerance. However, it seems likely that more than one of the approaches briefly outlined above might be eventually necessary to efficiently prevent NK-cell-mediated xenograft damage.

Citation: Berney T, Pileggi A, Inverardi L. 2001. NK Cells as a Barrier to Xenotransplantation, p 85-98. In Platt J (ed), Xenotransplantation. ASM Press, Washington, DC. doi: 10.1128/9781555818043.ch4
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1. Arase, H.,, N. Arase,, and T. Saito. 1995. Interferon gamma production by natural killer (NK) cells and NK1.1+ T cells upon NKR-P1 cross-linking. J. Exp. Med. 183: 2391 2396.
2. Arase, N.,, H. Arase,, S. Y. Park,, H. Ohno,, C. Ra,, and T. Saito. 1997. Association with FcRgamma is essential for activation signal through NKR-P1 (CD161) in natural killer (NK) cells and NK1.1+ T cells. J. Exp. Med. 186: 1957 1963.
3. Baquerizo, A.,, A. Mhoyan,, M. Kearns-Jonker,, W. S. Arnaout,, C. Schackleton,, R. W. Busuttil,, A. A. Demetriou,, and D. V. Cramer. 1999. Characterization of human xenoreactive antibodies in liver failure patients exposed to pig hepatocytes after bioartificial liver treatment: an ex vivo model of pig to human xenotransplantation. Transplantation 56: 5 18.
4. Barao, I.,, and J. L. Ascensao. 1998. Human natural killer cells. Arch. Immunol. Then Exp. 46: 213 229.
5. Bezouska, K.,, C. T. Yuen,, J. O'Brien,, R. A. Childs,, W. Chai,, A. M. Lawson,, K. Drbal,, A. Fiserova,, M. Pospisil,, and T. Feizi. 1994. Oligosaccharide ligands for NKR-P1 protein activate NK cells and cytotoxicity. Nature 372: 150 157.
6. Birmele, B.,, G. Thibault,, H. Nivet,, Y. Gruel,, P. Bardos,, and Y. Lebranchu. 1996. Human lymphocyte adhesion to xenogeneic porcine endothelial cells: modulation by human TNF-alpha and involvement of VLA-4 and LFA-1. Transplant. Immunol. 4: 265 270.
7. Birmele, B.,, G. Thibault,, H. Watier,, I. Vallee,, Y. Gruel,, H. Nivet,, H. Salmon,, P. Bardos,, and Y. Lebranchu. 1994. Human peripheral blood lymphocyte adhesion to xenogeneic porcine aortic endothelial cells: preferential adhesion of CD3-CD16+ NK cells. Transplant. Proc. 26: 1150 1151.
8. Bix, M.,, N. S. Liao,, M. Zijlstra,, J. Loring,, R. Jaenisch,, and D. Raulet. 1991. Rejection of class I MHC-deficient hematopoietic cells by irradiated MHC-matched mice. Nature 349: 329 331.
9. Blakely, M. L.,, W. J. Van der Werf,, M. C. Berndt,, A. P. Dalmasso,, F. H. Bach,, and W. W. Hancock. 1994. Activation of intragraft endothelial and mononuclear cells during discordant xenograft rejection. Transplantation 58: 1059 1066.
10. 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,, L. L. Lanier,, and A. J. McMichael. 1998. HLA-E binds to natural killer cell receptors CD94/NKG2A, B and C. Nature 391: 795 799.
11. Brennan, J.,, D. Mager,, W. Jefferies,, and F. Takei. 1994. Expression of different members of the Ly-49 gene family defines distinct natural killer cell subsets and cell adhesion properties. J. Exp. Med. 180: 2287 2295.
12. Brooks, A. G.,, P. E. Posch,, C. J. Scorzelli,, F. Borrego,, and J. E. Colinga. 1997. NKG2A complexed with CD94 defines a novel inhibitory natural killer cell receptor. J. Exp. Med. 185: 795 800.
13. Burshtyn, D. N.,, W. Yang,, T. Yi,, and E. O. Long. 1997. A novel phosphotyrosine motif with a critical amino acid at position -2 for the SHE2 domain-mediated activation of the tyrosine phosphatase SHP-1. J. Biol. Chem. 272: 13066 13072.
14. Candinas, D.,, S. Belliveau,, N. Koyamada,, T. Miyatake,, P. Hechenleitner,, W. Mark,, F. H. Bach,, and W. W. Hancock. 1996. T cell independence of macrophage and natural killer cell infiltration, cytokine production, and endothelial activation during delayed xenograft rejection. Transplantation 62: 1920 1927.
15. Candinas, D.,, B. A. Lesnikoski,, S. C. Robson,, T. Miyatake,, S. M. Scesney,, H. C. Marsh, Jr.,, U. S. Ryan,, A. P. Dalmasso,, W. W. Hancock,, and F. H. Bach. 1995. Effect of repetitive high-dose treatment with soluble complement receptor type 1 and cobra venom factor on discordant xenograft survival. Transplantation 62: 336 342.
16. Chan, D. V.,, and H. Auchincloss Jr.. 1996. Human anti-pig cell-mediated cytotoxicity in vivo involves non-T as well as T cell components. Xenotransplantation 3: 158 165.
17. Colonna, M.,, and J. Samaridis. 1995. Cloning of immunoglobulin-superfamily members associated with HLA-C and HLA-B recognition by human natural killer cells. Science 268: 405 408.
18. Cook, J. L.,, D. N. Ikle,, and B. A. Routes. 1995. Natural killer cell ontogeny in the athymic rat. Relationship between functional maturation and acquired resistance to E1A oncogene-expressing sarcoma cells. J. Immunol. 155: 5512 5518.
19. Dalmasso, A. P.,, G. M. Vercellotti,, R. J. Fischel,, R. M. Bolman,, F. H. Bach,, and J. L. Piatt. 1992. Mechanism of complement activation in the hyperacute rejection of porcine organs transplanted into primate recipients. Am. J. Pathol. 140: 1157 1166.
20. Fujiwara, I.,, H. Nakajima,, H. Yamagishi,, T. Matsuda,, N. Mizuta,, and T. Okta. 1998. The molecular mechanism of apoptosis induced by xenogeneic cytotoxicity. Xenotransplantation 5: 50 56.
21. Galili, U. 1993. Interaction of the natural anti-Gal antibody with alpha-galactosyl epitopes: a major obstacle for xenotransplantation in humans. Immunol. Today 14: 480 482.
22. Giorda, R.,, W. A. Rudert,, C. Vavassori,, W. H. Chambers,, J. C. Hiserodt,, and M. Trucco. 1990. NKR-P1, a signal transduction molecule on natural killer cells. Science 249: 1298 1300.
23. Goodman, D. J.,, M. Von Albertini,, A. Willson,, M. T. Millan,, and F. H. Bach. 1996. Direct activation of porcine endothelial cells by human natural killer cells. Transplantation 61: 763 771.
24. Gourlay, W. A.,, W. H. Chambers,, A. P. Monaco,, and T. Maki. 1998. Importance of natural killer cells in the rejection of hamster skin xenografts. Transplantation 65: 727 734.
25. Groth, C. G.,, O. Korsgren,, A. Tibell,, J. Tollemar,, E. Moller,, J. Bolinder,, J. Ostman,, F. P. Reinholt,, C. Hellerstrom,, and A. Andersson. 1994. Transplantation of porcine fetal pancreas to diabetic patients. Lancet 344: 1402 1404.
26. Hancock, W. W.,, M. L. Blakely,, W. Van der Werf,, and F. H. Bach. 1993. Rejection of guinea pig cardiac xenografts post-cobra venom factor therapy is associated with infiltration by mononuclear cells secreting interferon-gamma and diffuse endothelial activation. Transplant. Proc. 25: 2932.
27. Hancock, W. W.,, T. Miyatake,, N. Koyamada,, J. P. Kut,, M. Soares,, M. E. Russell,, F. H. Bach,, and M. H. Sayegh. 1997. Effects of lefiunomide and deoxyspergualin in the guinea pig ? rat cardiac model of delayed xenograft rejection: suppression of B cell and C-C chemokine responses but not induction of macrophage lectin. Transplantation 64: 696 704.
28. Hancock, W. W. 1997. Delayed xenograft rejection. World J. Surg. 21: 917 923.
29. Houchins, J. P.,, T. Yabe,, C. McSherry,, and F. H. Bach. 1991. DNA sequence analysis of NKG2, a family of related cDNA clones encoding type II integral membrane proteins on human natural killer cells. J. Exp. Med. 173: 1017 1029.
30. Inverardi, L.,, and R. Pardi,. 1996. Human natural killer cells and natural antibodies recognize overlapping molecular structures on discordant xenogeneic endothelium, p. 104 125. In E. Kemp,, K. Reemtsma,, D. White,, J. Piatt,, and D. K. C. Cooper (eds.), Xenotransplantation, Springer Scientific Publication, Berlin, Germany.
31. Inverardi, L.,, B. Clissi,, and R. Pardi. 1997. Xenorecognition by NK cells and natural antibodies: a common evolutionary pathway? Xenotransplantation 5: 9 11.
32. Inverardi, L.,, B. Clissi,, A. L. Stolzer,, J. R. Bender,, M. S. Sandrin,, and R. Pardi. 1997. Human natural killer lymphocytes directly recognize evolutionarily conserved oligosaccharide ligands expressed by xenogeneic tissues. Transplantation 63: 1318 1330.
33. Inverardi, L.,, M. Samaja,, R. Motterlini,, F. Mangili,, J. R. Bender,, and R. Pardi. 1992. Early recognition of a discordant xenogeneic organ by human circulating lymphocytes. J. Immunol. 149: 1416 1423.
34. Itescu, S.,, P. Kwiatkowski,, J. H. Artrip,, S. F. Wang,, J. Ankersmit,, O. P. Minanov,, and R. E. Michler. 1998. Role of natural killer cells, macrophages, and accessory molecule interactions in the rejection of pig-to-primate xenografts beyond the hyperacute period. Hum. Immunol. 59: 275 286.
35. Kase, A.,, M. H. Johansson,, M. Y. Olsson-Alheim,, K. Karre,, and P. Hoglund. 1998. External and internal calibration of the MHC class I-specific receptor Ly49A on murine natural killer cells. J. Immunol. 161: 6133 6138.
36. Kaufman, D. S.,, R. A. Schoon,, and P. J. Leibson. 1993. MHC class I expression on tumor targets inhibits natural killer cell-mediated cytotoxicity without interfering with target recognition. J. Immunol. 150: 1429 1436.
37. Khoo, N. K.,, L. Fahlen,, and C. L. Sentman. 1998. Modulation of Ly49A receptors on mature cells to changes in major histocompatibility complex class I molecules. Immunology 95: 126 131.
38. Kumagai-Braesch, M.,, M. Satake,, Y. Qian,, J. Holgersson,, and E. Moller. 1998. Human NK cell and ADCC reactivity against xenogeneic porcine target cells including fetal porcine islet cells. Xenotransplantation 5: 132 145.
39. Lanier, L. L.,, B. C. Corliss,, J. Wu,, C. Leong,, and J. H. Phillips. 1998. Immunoreceptor DAP12 bearing a tyrosine-based activation motif is involved in activating NK cells. Nature 391: 703 707.
40. Lanier, L. L. 1998. NK cell receptors. Annu. Rev. Immunol. 16: 359 393.
41. Lazetic, S.,, C. Chang,, J. P. Houchins,, L. L. Lanier,, and J. H. Phillips. 1996. Human natural killer cell receptors involved in MHC class I recognition are disulflde-linked heterodimers of CD94 and NKG2 subunits. J. Immunol. 157: 4741 745.
42. Leibson, P. J. 1997. Signal transduction during natural killer cell activation: inside the mind of a killer. Immunity 6: 655 661.
43. Leventhal, J. R.,, A. J. Matas,, L. H. Sun,, S. Reif,, R. M. Bolman, 3d,, A. P. Dalmasso,, and J. L. Piatt 1993. The immunopathology of cardiac xenograft rejection in the guinea pig-to-rat model. Transplantation 56: 1 8.
44. Lin, Y.,, M. Vandeputte,, and M. Waer. 1997. Contribution of activated macrophages to the process of delayed xenograft rejection. Transplantation 64: 1677 1683.
45. Lin, Y.,, M. Vandeputte,, and M. Waer. 1997. Natural killer cell- and macrophage-mediated rejection of concordant xenografts in the absence of T and B cell responses. J. Immunol. 158: 5658 5667.
46. Ljunggren, H. G.,, and K. Karre. 1985. Host resistance directed selectively against H-2-deficient lymphoma variants. Analysis of the mechanism. J. Exp. Med. 162: 1745 1759.
47. Malyguine, A. M.,, S. Saadi,, J. L. Platt,, and J. R. Dawson. 1996. Human natural killer cells induce morphologic changes in porcine endothelial cell monolayers. Transplantation 61: 161 164.
48. Mason, L. H.,, S. K. Anderson,, W. M. Yokoyama,, H. R. Smith,, R. Winkler-Pickett,, and J. R. Ortaldo. 1996. The Ly-49D receptor activates murine natural killer cells. J. Exp. Med. 184: 2119 2128.
49. Mason, L. H.,, J. Willette-Brown,, S. K. Anderson,, P. Gosselin,, E. W. Shores,, P. E. Love,, J. R. Ortaldo,, and D. W. McVicar. 1998. Characterization of an associated 16kDa tyrosine phosphoprotein required for Ly-49D signal transduction. J. Immunol. 160: 4148 4152.
50. Moretta, A.,, S. Sivori,, M. Vitale,, D. Pende,, L. Morelli,, R. Augugliaro,, C. Bottino,, and L. Moretta. 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.
51. O'Shea, J. J.,, A. M. Weissman,, I. C. Kennedy,, and J. R. Ortaldo. 1991. Engagement of the natural killer cell IgG Fc receptor results in tyrosine phosphorylation of the zeta chain. Proc. Natl. Acad. Sci. USA 88: 350 354.
52. Olcese, L.,, P. Lang,, F. Vely,, A. Cambiaggi,, D. Marguet,, M. Blery,, K. L. Hippen,, R. Biassoni,, A. Moretta,, L. Moretta,, J. C. Cambier,, and E. Vivien 1996. Human and mouse killer-cell inhibitory receptors recruit PTP1C and PTP1D protein tyrosine phosphatases. J. Immunol. 156: 4531 534.
53. Patselas, T.,, F. Thomas,, D. Araneda,, and W. Marchman. 1995. Role of natural killer and killer cells in concordant xenograft rejection. Transplant. Proc. 27: 262 263.
54. Pearse, M. J.,, E. Witort,, P. Mottram,, W. Han,, L. Murray-Segal,, M. Romanella,, E. Salvaris,, T. A. Shinkel,, D. J. Goodman,, and A. J. d'Apice. 1998. Anti-Gal antibody-mediated allograft rejection in alpha 1,3-galactosyltransferase gene knockout mice: a model of delayed xenograft rejection. Transplantation 66: 748 754.
55. Pende, D.,, R. Biassoni,, C. Cantoni,, S. Verdiani,, M. Falco,, C. di Donate,, L. Accame,, C. Bottino,, A. Moretta,, and L. Moretta. 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.
56. Phillips, J. H.,, C. Chang,, J. Mattson,, J. E. Gumperz,, P. Parham,, and L. L. Lanier. 1996. CD94 and a novel associated protein (94AP) form a NK cell receptor involved in the recognition of HLA-A, HLA-B and HLA-C allotypes. Immunity 5: 163 172.
57. Platt, J. L.,, R. J. Fischel,, A. J. Matas,, S. A. Reif,, R. M. Bolman,, and F. H. Bach. 1991. Immunopathology of hyperacute xenograft rejection in a swine-to-primate model. Transplantation 52: 214 220.
58. Pruitt, S. K.,, W. M. Baldwin, 3d,, H. C. Marsh, Jr.,, S. S. Lin,, C. G. Yeh,, and R. R. Bollinger. 1991. The effect of soluble complement receptor type 1 on hyperacute xenograft rejection. Transplantation 52: 868 873.
59. Raziuddin, A.,, D. L. Longo,, L. Mason,, J. R. Ortaldo,, and W. J. Murphy. 1996. Ly-49 G2+ NK cells are responsible for mediating the rejection of H-2b bone marrow allografts in mice. Int. Immunol. 8: 1833 1839.
60. Reynolds, C. W.,, and J. R. Ortaldo. 1987. Natural killer activity: the definition of a function rather than a cell type. Immunol. Today 8: 172 174.
61. Saadi, S.,, and J. L. Platt. 1998. Immunology of xenotransplantation. Life Sci. 62: 365 387.
62. Sanchez, M. J.,, M. O. Muench,, M. G. Roncarolo,, L. L. Lanier,, and J. H. Phillips. 1994. Identification of a common T/natural killer cell progenitor in human fetal thymus. J. Exp. Med. 180: 569 576.
63. Sanchez, M. J.,, H. Spits,, L. L. Lanier,, and J. H. Phillips. 1993. Human natural killer cell committed thymocytes and their relation to the T cell lineage. J. Exp. Med. 178: 1857 1866.
64. Sasaki, H.,, X. C. Xu,, D. M. Smith,, T. Howard,, and T. Mohanakumar. 1999. HLA-G expression protects porcine endothelial cells against natural killer cell-mediated xenogeneic cytotoxicity. Transplantation 67: 31 37.
65. Seebach, J. D.,, C. Comrack,, S. Germana,, C. LeGuern,, D. H. Sachs,, and H. DerSimonian. 1997. HLA-Cw3 expression on porcine endothelial cells protects against xenogeneic cytotoxicity mediated by a subset of human NK cells. J. Immunol. 159: 3655 3661.
66. Seebach, J. D.,, K. Yamada,, I. M. McMorrow,, D. H. Sachs,, and H. DerSimonian. 1996. Xenogeneic human anti-pig cytotoxicity mediated by activated natural killer cells. Xenotransplantation 3: 188 197.
67. Sentman, C. L.,, M. Y. Olsson,, and K. Karre. 1995. Missing self recognition by natural killer cells in MHC class I transgenic mice. A 'receptor calibration' model for how effector cells adapt to self. Semin. Immunol. 7: 109 119.
68. Sharabi, Y.,, I. Aksentijevich,, T. M. Sundt, 3d, D. H. Sachs, and M. Sykes. 1990. Specific tolerance induction across a xenogeneic barrier: production of mixed rat/mouse lymphohematopoietic chimeras using a nonlethal preparative regimen. J. Exp. Med. 172: 195 202.
69. Shimizu, Y.,, and R. DeMars. 1989. Demonstration by class I gene transfer that reduced susceptibility of human cells to natural killer cell-mediated lysis is inversely correlated with HLA class I antigen expression. Eur. J. Immunol. 19: 447 151.
70. Silver, E. T.,, J. F. Elliott,, and K. R Kane. 1995. Alternatively spliced Ly-49D and H transcripts are found in IL-2-activated NK cells. Immunogenetics 44: 478 482.
71. Sivakumar, P. V.,, I. Puzanov,, N. S. Williams,, M. Bennett,, and V. Kumar,. 1998. Ontogeny and differentiation of murine natural killer cells and their receptors, p. 161 192. In K. Karre, and M. Colonna (eds.), Specificity, Function and Development of NK Cells. Springer, Berlin, Germany.
72. Smyth, M. J.,, K. Y. T. Thia,, and M. H. Kershaw. 1997. Xenogeneic mouse anti-human NK cytotoxicity is mediated via perforin. Xenotransplantation 4: 78 84.
73. Soderstrom, K.,, B. Corliss,, L. L. Lanier,, and J. H. Phillips. 1997. CD94/NKG2 is the predominant inhibitory receptor involved in recognition of HLA-G by decidual and peripheral blood NK cells. J. Immunol. 159: 1072 1075.
74. Spritz, R. A. 1998. Genetic defects in Chediak-Higashi syndrome and the beige mouse. J. Clin. Immunol. 18: 97 105.
75. Steffens, U.,, Y. Vyas,, B. Dupont,, and A. Selvakumar. 1998. Nucleotide and amino acid sequence alignment for human killer cell inhibitory receptors (KIR). Tissue Antigens 51: 398 413.
76. Sullivan, J. A.,, H. F. Oettinger,, D. H. Sachs,, and A. S. Edge. 1997. Analysis of polymorphism in porcine MHC class I genes: alterations in signals recognized by human cytotoxic lymphocytes. J. Immunol. 159: 2318 2326.
77. Sykes, M. 1996. Hematopoietic cell transplantation for the induction of allo- and xeno-tolerance. Clin. Transplant. 10: 357 363.
78. Sykes, M.,, H. Ohdan,, J. O. Manilay,, T. Wekerle,, and Y. G. Yang. 1998. Hematopoietic chimerism and tolerance of T cells, B cells, and NK cells. Transplant. Proc. 30: 4020.
79. Tay, C. H.,, E. Szomolanyi-Tsuda,, and R. M. Welsh,. 1998. Control of infections by NK cells, p. 193 220. In K. Karre, and M. Colonna (eds.), Specificity, Function and Development of NK Cells. Springer, Berlin, Germany.
80. Vales-Gomez, M.,, H. T. Reyburn,, M. Mandelboim,, and J. L. Strominger. 1998. Kinetics of interaction of HLA-C ligands with natural killer cell inhibitory receptors. Immunity 9: 337 344.
81. Vance, R. E.,, J. R. Kraft,, J. D. Altman,, P. E. Jensen,, and D. H. Raulet. 1998. Mouse CD94/NKG2A is a natural killer cell receptor for the nonclassical major histocompatibility complex (MHC) class I molecule Qa-l(b). J. Exp. Med. 188: 1841 1848.
82. Vance, R. E.,, D. M. Tanamachi,, T. Hanke,, and D. H. Raulet. 1997. Cloning of a mouse homolog of CD94 extends the family of C-type lectins on murine natural killer cells. Eur. J. Immunol. 27: 3236 3241.
83. von Albertini, M.,, C. Ferran,, C. Brostjan,, F. H. Bach,, and D. J. Goodman. 1998. Membrane-associated lymphotoxin on natural killer cells activates endothelial cells via an NF-kappaB-dependent pathway. Transplantation 66: 1211 1219.
84. Watier, H.,, J. M. Guillaumin,, I. Vallee,, G. Thibault,, Y. Gruel,, Y. Lebranchu,, and P. Bardos. 1996. Human NK cell-mediated direct and IgG-dependent cytotoxicity against xenogeneic porcine endothelial cells. Transplant. Immunol. 4: 293 299.
85. Whiteside, T. L.,, N. L. Vujanovic,, and R. B. Herberman,. 1998. Natural killer cells and tumor therapy, p. 221 244. In K. Karre, and M. Colonna (eds.), Specificity, Function and Development of NK Cells. Springer, Berlin, Germany.
86. Winter, C. C.,, J. E. Gumperz,, P. Parham,, E. O. Long,, and N. Wagmann. 1998. Direct binding and functional transfer of NK cell inhibitory receptors reveal novel patterns of HLA-C allotype recognition. J. Immunol. 151: 571 577.
87. Wirthmueller, U.,, T. Kurosaki,, M. S. Murakami,, and J. V. Ravetch. 1992. Signal transduction by Fc gamma RIII (CD16) is mediated through the gamma chain. J. Exp. Med. 175: 1381 1390.
88. Yu, Y. Y.,, T. George,, J. R. Dorfman,, J. Roland,, V. Kumar,, and M. Bennett. 1996. The role of Ly49A and 5E6(Ly49C) molecules in hybrid resistance mediated by murine natural killer cells against normal T cell blasts. Immunity 4: 67 76.

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