Non-MHC ligands for inhibitory immune receptors: Novel insights and implications for immune regulation

Molecular Immunology

Volumn 44, Issue 9, 2007, Pages 2153-2164

  Lebbink, Robert Jan ^a   Meyaard, Linde ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Collagen; Immune regulation; Inhibitory receptors; ITIM; Ligands

Indexed keywords

CARCINOEMBRYONIC ANTIGEN RELATED CELL ADHESION MOLECULE 1; CD100 ANTIGEN; CD200 ANTIGEN; CD200 RECEPTOR; CD47 ANTIGEN; CD48 ANTIGEN; CD72 ANTIGEN; CELL ANTIGEN; CELL PROTEIN; CELL RECEPTOR; COLLAGEN; GANGLIOSIDE; KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR; LIGAND; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; PD L1 ANTIGEN; PROTEIN 2B4; PROTEIN INHIBITOR; PROTEIN KLRB1; PROTEIN KLRG1; PROTEIN LAIR 1; PROTEIN PD 1; PROTEIN SIGLEC7; PROTEIN SIRP ALPHA; RECEPTOR PROTEIN; TUMOR PROTEIN; UNCLASSIFIED DRUG; UVOMORULIN;

EFFECTOR CELL; HUMAN; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; IMMUNOREGULATION; INFECTION RESISTANCE; LIGAND BINDING; MAJOR HISTOCOMPATIBILITY COMPLEX; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; TUMOR IMMUNITY;

ANIMALS; CELL ADHESION MOLECULES; HISTOCOMPATIBILITY ANTIGENS CLASS I; HUMANS; LIGANDS; NEOPLASMS; POLYSACCHARIDES; RECEPTORS, IMMUNOLOGIC;

EID: 33846240510     PISSN: 01615890     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molimm.2006.11.014     Document Type: Review

References (148)

1. Aldemir H., Prod'homme V., Dumaurier M.J., Retiere C., Poupon G., Cazareth J., Bihl F., and Braud V.M. Cutting edge: lectin-like transcript 1 is a ligand for the CD161 receptor. J. Immunol. 175 (2005) 7791-7795
2. Banyard J., Bao L., and Zetter B.R. Type XXIII collagen, a newtransmembrane collagen identified in metastatic tumor cells. J. Biol. Chem. 278 (2003) 20989-20994
3. Barclay A.N., and Brown M.H. The SIRP family of receptors and immune regulation. Nat. Rev. Immunol. 6 (2006) 457-464
4. Barclay A.N., Wright G.J., Brooke G., and Brown M.H. CD200 and membrane protein interactions in the control of myeloid cells. Trends Immunol. 23 (2002) 285-290
5. Basile J.R., Castilho R.M., Williams V.P., and Gutkind J.S. Semaphorin 4D provides a link between axon guidance processes and tumor-induced angiogenesis. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 9017-9022
6. Blank C., Gajewski T.F., and Mackensen A. Interaction of PD-L1 on tumor cells with PD-1 on tumor-specific T cells as a mechanism of immune evasion: implications for tumor immunotherapy. Cancer Immunol. Immunother. 15 54 (2005) 307-314
7. Blery M., Olcese L., and Vivier E. Early signaling via inhibitory and activating NK receptors. Hum. Immunol. 61 (2000) 51-64
8. Bocek Jr. P., Guthmann M.D., and Pecht I. Analysis of the genes encoding the mast cell function-associated antigen and its alternatively spliced transcripts. J. Immunol. 158 (1997) 3235-3243
9. Bolland S., and Ravetch J.V. Spontaneous autoimmune disease in Fc(gamma)RIIB-deficient mice results from strain-specific epistasis. Immunity 13 (2000) 277-285
10. + T lymphocytes. Nat. Immunol. 3 (2002) 229-236
11. Brown M.H., Boles K., van der Merwe P.A., Kumar V., Mathew P.A., and Barclay A.N. 2B4, the natural killer and T cell immunoglobulin superfamily surface protein, is a ligand for CD48. J. Exp. Med. 188 (1998) 2083-2090
12. Budt M., Michely B., Muller M.M., Reutter W., and Lucka L. Secreted CEACAM1 splice variants in rat cell lines and in vivo in rat serum. Biochem. Biophys. Res. Commun. 292 (2002) 749-755
13. Cameron C., Hota-Mitchell S., Chen L., Barrett J., Cao J.X., Macaulay C., Willer D., Evans D., and McFadden G. The complete DNA sequence of myxoma virus. Virology 264 (1999) 298-318
14. Cameron C.M., Barrett J.W., Liu L., Lucas A.R., and McFadden G. Myxoma virus M141R expresses a viral CD200 (vOX-2) that is responsible for down-regulation of macrophage and T-cell activation in vivo. J. Virol. 79 (2005) 6052-6067
15. Cameron C.M., Barrett J.W., Mann M., Lucas A., and McFadden G. Myxoma virus M128L is expressed as a cell surface CD47-like virulence factor that contributes to the downregulation of macrophage activation in vivo. Virology 337 (2005) 55-67
16. Campbell I.G., Freemont P.S., Foulkes W., and Trowsdale J. An ovarian tumor marker with homology to vaccinia virus contains an IgV-like region and multiple transmembrane domains. Cancer Res. 52 (1992) 5416-5420
17. Carreno B.M., and Collins M. BTLA: a new inhibitory receptor with a B7-like ligand. Trends Immunol. 24 (2003) 524-527
18. Cassel D.L., Keller M.A., Surrey S., Schwartz E., Schreiber A.D., Rappaport E.F., and McKenzie S.E. Differential expression of Fc gamma RIIA Fc gamma RIIB and Fc gamma RIIC in hematopoietic cells: analysis of transcripts. Mol. Immunol. 30 (1993) 451-460
19. Charalabopoulos K., Gogali A., Kostoula O.K., and Constantopoulos S.H. Cadherin superfamily of adhesion molecules in primary lung cancer. Exp. Oncol. 26 (2004) 256-260
20. Chen D., Iijima H., Nagaishi T., Nakajima A., Russell S., Raychowdhury R., Morales V., Rudd C.E., Utku N., and Blumberg R.S. Carcinoembryonic antigen-related cellular adhesion molecule 1 isoforms alternatively inhibit and costimulate human T cell function. J. Immunol. 172 (2004) 3535-3543
21. Chen R., Relouzat F., Roncagalli R., Aoukaty A., Tan R., Latour S., and Veillette A. Molecular dissection of 2B4 signaling: implications for signal transduction by SLAM-related receptors. Mol. Cell. Biol. 24 (2004) 5144-5156
22. Chen T., Zimmermann W., Parker J., Chen I., Maeda A., and Bolland S. Biliary glycoprotein (BGPa, CD66a, CEACAM1) mediates inhibitory signals. J. Leukoc. Biol. 70 (2001) 335-340
23. Cheung T.C., Humphreys I.R., Potter K.G., Norris P.S., Shumway H.M., Tran B.R., Patterson G., Jean-Jacques R., Yoon M., Spear P.G., Murphy K.M., Lurain N.S., Benedict C.A., and Ware C.F. Evolutionarily divergent herpesviruses modulate T cell activation by targeting the herpesvirus entry mediator cosignaling pathway. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 13218-13223
24. Christiansen D., Mouhtouris E., Milland J., Zingoni A., Santoni A., and Sandrin M.S. Recognition of a carbohydrate xenoepitope by human NKRP1A (CD161). Xenotransplantation 13 (2006) 440-446
25. Cicmil M., Thomas J.M., Leduc M., Bon C., and Gibbins J.M. Platelet endothelial cell adhesion molecule-1 signaling inhibits the activation of human platelets. Blood 99 (2002) 137-144
26. Colonna M. Cytolytic responses: cadherins put out the fire. J. Exp. Med. 203 (2006) 261-264
27. Connolly N.P., Jones M., and Watt S.M. Human Siglec-5: tissue distribution, novel isoforms and domain specificities for sialic acid-dependent ligand interactions. Br. J. Haematol. 119 (2002) 221-238
28. + large granular lymphocytes triggered by a tumor-expressed activating ligand. Leukemia 16 (2002) 855-860
29. Cowin P., Rowlands T.M., and Hatsell S.J. Cadherins and catenins in breast cancer. Curr. Opin. Cell Biol. 17 (2005) 499-508
30. Crocker P.R. Siglecs in innate immunity. Curr. Opin. Pharmacol. 5 (2005) 431-437
31. Crocker P.R., Mucklow S., Bouckson V., McWilliam A., Willis A.C., Gordon S., Milon G., Kelm S., and Bradfield P. Sialoadhesin, a macrophage sialic acid binding receptor for haemopoietic cells with 17 immunoglobulin-like domains. EMBO J. 13 (1994) 4490-4503
32. Duncan G.S., Andrew D.P., Takimoto H., Kaufman S.A., Yoshida H., Spellberg J., Luis D.I.P., Elia A., Wakeham A., Karan-Tamir B., Muller W.A., Senaldi G., Zukowski M.M., and Mak T.W. Genetic evidence for functional redundancy of platelet/endothelial cell adhesion molecule-1 (PECAM-1): CD31-deficient mice reveal PECAM-1-dependent and PECAM-1-independent functions. J. Immunol. 162 (1999) 3022-3030
33. Eissmann P., Beauchamp L., Wooters J., Tilton J.C., Long E.O., and Watzl C. Molecular basis for positive and negative signaling by the natural killer cell receptor 2B4 (CD244). Blood 105 (2005) 4722-4729
34. Elhabazi A., Delaire S., Bensussan A., Boumsell L., and Bismuth G. Biological activity of soluble CD100. I. The extracellular region of CD100 is released from the surface of T lymphocytes by regulated proteolysis. J. Immunol. 166 (2001) 4341-4347
35. + CD4-CD8-T cells. J. Exp. Med. 186 (1997) 109-120
36. Falati S., Patil S., Gross P.L., Stapleton M., Merrill-Skoloff G., Barrett N.E., Pixton K.L., Weiler H., Cooley B., Newman D.K., Newman P.J., Furie B.C., Furie B., and Gibbins J.M. Platelet PECAM-1 inhibits thrombus formation in vivo. Blood 107 (2006) 535-541
37. Farndale R.W., Sixma J.J., Barnes M.J., and de Groot P.G. The role of collagen in thrombosis and hemostasis. J. Thromb. Haemost. 2 (2004) 561-573
38. Foster-Cuevas M., Wright G.J., Puklavec M.J., Brown M.H., and Barclay A.N. Human herpesvirus 8 K14 protein mimics CD200 in down-regulating macrophage activation through CD200 receptor. J. Virol. 78 (2004) 7667-7676
39. Fuchs A., and Colonna M. The role of NK cell recognition of nectin and nectin-like proteins in tumor immunosurveillance. Semin. Cancer Biol. 16 5 (2006) 359-366
40. Fujiwara K. Platelet endothelial cell adhesion molecule-1 and mechanotransduction in vascular endothelial cells. J. Intern. Med. 259 (2006) 373-380
41. Gardai S.J., Xiao Y.Q., Dickinson M., Nick J.A., Voelker D.R., Greene K.E., and Henson P.M. By binding SIRPalpha or calreticulin/CD91, lung collectins act as dual function surveillance molecules to suppress or enhance inflammation. Cell 115 (2003) 13-23
42. Gelse K., Poschl E., and Aigner T. Collagens-structure, function, and biosynthesis. Adv. Drug Deliv. Rev. 55 (2003) 1531-1546
43. Gonzalez L.C., Loyet K.M., Calemine-Fenaux J., Chauhan V., Wranik B., Ouyang W., and Eaton D.L. A coreceptor interaction between the CD28 and TNF receptor family members B and T lymphocyte attenuator and herpesvirus entry mediator. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 1116-1121
44. Graesser D., Solowiej A., Bruckner M., Osterweil E., Juedes A., Davis S., Ruddle N.H., Engelhardt B., and Madri J.A. Altered vascular permeability and early onset of experimental autoimmune encephalomyelitis in PECAM-1-deficient mice. J. Clin. Invest. 109 (2002) 383-392
45. Gray-Owen S.D., and Blumberg R.S. CEACAM1: contact-dependent control of immunity. Nat. Rev. Immunol. 6 (2006) 433-446
46. Gress C.J., and Jacenko O. Growth plate compressions and altered hematopoiesis in collagen X null mice. J. Cell Biol. 149 (2000) 983-993
47. Grundemann C., Bauer M., Schweier O., von Oppen N., Lassing U., Saudan P., Becker K.F., Karp K., Hanke T., Bachmann M.F., and Pircher H. Cutting edge: identification of E-cadherin as a ligand for the murine killer cell lectin-like receptor G1. J. Immunol. 176 (2006) 1311-1315
48. Gumbiner B.M. Regulation of cadherin-mediated adhesion in morphogenesis. Nat. Rev. Mol. Cell. Biol. 6 (2005) 622-634
49. Gumbiner B.M. Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell 84 (1996) 345-357
50. Hall K.T., Boumsell L., Schultze J.L., Boussiotis V.A., Dorfman D.M., Cardoso A.A., Bensussan A., Nadler L.M., and Freeman G.J. Human CD100, a novel leukocyte semaphorin that promotes B-cell aggregation and differentiation. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 11780-11785
51. Han S., Collins B.E., Bengtson P., and Paulson J.C. Homomultimeric complexes of CD22 in B cells revealed by protein-glycan cross-linking. Nat. Chem. Biol. 1 (2005) 93-97
52. Heaney M.L., and Golde D.W. Soluble cytokine receptors. Blood 87 (1996) 847-857
53. Hemmila E., Turbide C., Olson M., Jothy S., Holmes K.V., and Beauchemin N. Ceacam1a-/- mice are completely resistant to infection by murine coronavirus mouse hepatitis virus A59. J. Virol. 78 (2004) 10156-10165
54. Henshall T.L., Jones K.L., Wilkinson R., and Jackson D.E. Src homology 2 domain-containing protein-tyrosine phosphatases, SHP-1 and SHP-2, are required for platelet endothelial cell adhesion molecule-1/CD31-mediated inhibitory signaling. J. Immunol. 166 (2001) 3098-3106
55. Hock B.D., O'Donnell J.L., Taylor K., Steinkasserer A., McKenzie J.L., Rothwell A.G., and Summers K.L. Levels of the soluble forms of CD80, CD86, and CD83 are elevated in the synovial fluid of rheumatoid arthritis patients. Tissue Antigens 67 (2006) 57-60
56. Hoek R.M., Ruuls S.R., Murphy C.A., Wright G.J., Goddard R., Zurawski S.M., Blom B., Homola M.E., Streit W.J., Brown M.H., Barclay A.N., and Sedgwick J.D. Down-regulation of the macrophage lineage through interaction with OX2 (CD200). Science 290 (2000) 1768-1771
57. Hsieh J.T., Luo W., Song W., Wang Y., Kleinerman D.I., Van N.T., and Lin S.H. Tumor suppressive role of an androgen-regulated epithelial cell adhesion molecule (C-CAM) in prostate carcinoma cell revealed by sense and antisense approaches. Cancer Res. 55 (1995) 190-197
58. Iijima H., Neurath M.F., Nagaishi T., Glickman J.N., Nieuwenhuis E.E., Nakajima A., Chen D., Fuss I.J., Utku N., Lewicki D.N., Becker C., Gallagher T.M., Holmes K.V., and Blumberg R.S. Specific regulation of T helper cell 1-mediated murine colitis by CEACAM1. J. Exp. Med. 199 (2004) 471-482
59. Iizasa T., Chang H., Suzuki M., Otsuji M., Yokoi S., Chiyo M., Motohashi S., Yasufuku K., Sekine Y., Iyoda A., Shibuya K., Hiroshima K., and Fujisawa T. Over expression of collagen XVIII is associated with poor outcome and elevated levels of circulating serum endostatin in non-small cell lung cancer. Clin. Cancer Res. 10 (2004) 5361-5366
60. Ilan N., and Madri J.A. PECAM-1: old friend, new partners. Curr. Opin. Cell Biol. 15 (2003) 515-524
61. Ito A., Handa K., Withers D.A., Satoh M., and Hakomori S. Binding specificity of Siglec7 to disialogangliosides of renal cell carcinoma: possible role of disialogangliosides in tumor progression. FEBS Lett. 504 (2001) 82-86
62. Ito M., Maruyama T., Saito N., Koganei S., Yamamoto K., and Matsumoto N. Killer cell lectin-like receptor G1 binds three members of the classical cadherin family to inhibit NK cell cytotoxicity. J. Exp. Med. 203 (2006) 289-295
63. Iwai Y., Ishida M., Tanaka Y., Okazaki T., Honjo T., and Minato N. Involvement of PD-L1 on tumor cells in the escape from host immune system and tumor immunotherapy by PD-L1 blockade. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 12293-12297
64. Jenmalm M.C., Cherwinski H., Bowman E.P., Phillips J.H., and Sedgwick J.D. Regulation of myeloid cell function through the CD200 receptor. J. Immunol. 176 (2006) 191-199
65. Jiang P., Lagenaur C.F., and Narayanan V. Integrin-associated protein is a ligand for the P84 neural adhesion molecule. J. Biol. Chem. 274 (1999) 559-562
66. Karre K., Ljunggren H.G., Piontek G., and Kiessling R. Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defence strategy. Nature 319 (1986) 675-678
67. Kolodkin A.L. Semaphorins: mediators of repulsive growth cone guidance. Trends Cell Biol. 6 (1996) 15-22
68. Kuespert K., Pils S., and Hauck C.R. CEACAMs: their role in physiology and pathophysiology. Curr. Opin. Cell Biol. 18 (2006) 565-571
69. Kumanogoh A., and Kikutani H. Biological functions and signaling of a transmembrane semaphorin CD100/Sema4D. Cell Mol. Life Sci. 61 (2004) 292-300
70. Kumanogoh A., Watanabe C., Lee I., Wang X., Shi W., Araki H., Hirata H., Iwahori K., Uchida J., Yasui T., Matsumoto M., Yoshida K., Yakura H., Pan C., Parnes J.R., and Kikutani H. Identification of CD72 as a lymphocyte receptor for the class IV semaphorin CD100: a novel mechanism for regulating B cell signaling. Immunity 13 (2000) 621-631
71. Kumaresan P.R., Stepp S.E., Bennett M., Kumar V., and Mathew P.A. Molecular cloning of transmembrane and soluble forms of a novel rat natural killer cell receptor related to 2B4. Immunogenetics 51 (2000) 306-313
72. Kunath T., Ordonez-Garcia C., Turbide C., and Beauchemin N. Inhibition of colonic tumor cell growth by biliary glycoprotein. Oncogene 11 (1995) 2375-2382
73. Kyogoku C., Dij stelbloem H.M., Tsuchiya N., Hatta Y., Kato H., Yamaguchi A., Fukazawa T., Jansen M.D., Hashimoto H., Van De Winkel J.G., Kallenberg C.G., and Tokunaga K. Fc gamma receptor gene polymorphisms in Japanese patients with systemic lupus erythematosus: contribution of FCGR2B to genetic susceptibility. Arthritis Rheum. 46 (2002) 1242-1254
74. Langlais C.L., Jones J.M., Estep R.D., and Wong S.W. Rhesus rhadinovirus R15 encodes a functional homologue of human CD200. J. Virol. 80 (2006) 3098-3103
75. Lanier L.L. NK cell receptors. Annu. Rev. Immunol. 16 (1998) 359-393
76. Lanier L.L. NK cell recognition. Annu. Rev. Immunol. (2005) 225-274
77. Lanier L.L., Chang C., and Phillips J.H. Human NKR-P1A. A disulfide-linked homodimer of the C-type lectin superfamily expressed by a subset of NK and T lymphocytes. J. Immunol. 153 (1994) 2417-2428
78. Latchman Y., McKay P.F., and Reiser H. Identification of the 2B4 molecule as a counter-receptor for CD48. J. Immunol. 161 (1998) 5809-5812
79. Lebbink R.J., de Ruiter T., Adelmeijer J., Brenkman A.B., van Helvoort J.M., Koch M., Farndale R.W., Lisman T., Sonnenberg A., Lenting P.J., and Meyaard L. Collagens are functional, high affinity ligands for the inhibitory immune receptor LAIR-1. J. Exp. Med. 203 (2006) 1419-1425
80. Leprince C., Draves K.E., Geahlen R.L., Ledbetter J.A., and Clark E.A. CD22 associates with the human surface IgM-B-cell antigen receptor complex. Proc. Natl. Acad. Sci. U.S.A. 90 (1993) 3236-3240
81. Levine S.J. Mechanisms of soluble cytokine receptor generation. J. Immunol. 173 (2004) 5343-5348
82. Lindberg F.P., Gresham H.D., Schwarz E., and Brown E.J. Molecular cloning of integrin-associated protein: an immunoglobulin family member with multiple membrane-spanning domains implicated in alpha v beta 3-dependent ligand binding. J. Cell Biol. 123 (1993) 485-496
83. Lodoen M.B., and Lanier L.L. Viral modulation of NK cell immunity. Nat. Rev. Microbiol. 3 (2005) 59-69
84. Markel G., Lieberman N., Katz G., Arnon T.I., Lotem M., Drize O., Blumberg R.S., Bar-Haim E., Mader R., Eisenbach L., and Mandelboim O. CD66a interactions between human melanoma and NK cells: a novel class I MHC-independent inhibitory mechanism of cytotoxicity. J. Immunol. 168 (2002) 2803-2810
85. Markel G., Wolf D., Hanna J., Gazit R., Goldman-Wohl D., Lavy Y., Yagel S., and Mandelboim O. Pivotal role of CEACAM1 protein in the inhibition of activated decidual lymphocyte functions. J. Clin. Invest. 110 (2002) 943-953
86. McNerney M.E., and Kumar V. The CD2 family of natural killer cell receptors. Curr. Top. Microbiol. Immunol. 298 (2006) 91-120
87. McWhirter J.R., Kretz-Rommel A., Saven A., Maruyama T., Potter K.N., Mockridge C.I., Ravey E.P., Qin F., and Bowdish K.S. Antibodies selected from combinatorial libraries block a tumor antigen that plays a key role in immunomodulation. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 1041-1046
88. Meyaard L., Adema G.J., Chang C., Woollatt E., Sutherland G.R., Lanier L.L., and Phillips J.H. LAIR-1, a novel inhibitory receptor expressed on human mononuclear leukocytes. Immunity 7 (1997) 283-290
89. Morgan A.W., Barrett J.H., Griffiths B., Subramanian D., Robinson J.I., Keyte V.H., Ali M., Jones E.A., Old R.W., Ponchel F., Boylston A.W., Situnayake R.D., Markham A.F., Emery P., and Isaacs J.D. Analysis of Fc gamma receptor haplotypes in rheumatoid arthritis: FCGR3A remains a major susceptibility gene at this locus, with an additional contribution from FCGR3B. Arthritis Res. Ther. 8 (2005) R5
90. Moser K.L., Neas B.R., Salmon J.E., Yu H., Gray-McGuire C., Asundi N., Bruner G.R., Fox J., Kelly J., Henshall S., Bacino D., Dietz M., Hogue R., Koelsch G., Nightingale L., Shaver T., Abdou N.I., Albert D.A., Carson C., Petri M., Treadwell E.L., James J.A., and Harley J.B. Genome scan of human systemic lupus erythematosus: evidence for linkage on chromosome 1q in African-American pedigrees. Proc. Natl. Acad. Sci. U.S.A. 95 (1998) 14869-14874
91. Muhlbauer M., Fleck M., Schutz C., Weiss T., Froh M., Blank C., Scholmerich J., and Hellerbrand C. PD-L1 is induced in hepatocytes by viral infection and by interferon-alpha and -gamma and mediates T cell apoptosis. J. Hepatol. 45 (2006) 520-528
92. Murphy K.M., Nelson C.A., and Sedy J.R. Balancing co-stimulation and inhibition with BTLA and HVEM. Nat. Rev. Immunol. 6 (2006) 671-681
93. Myllyharju J., and Kivirikko K.I. Collagens, modifying enzymes and their mutations in humans, flies and worms. Trends Genet. 20 (2004) 33-43
94. Newman P.J. Switched at birth: a new family for PECAM-1. J. Clin. Invest. 103 (1999) 5-9
95. Newton-Nash D.K., and Newman P.J. A new role for platelet-endothelial cell adhesion molecule-1 (CD31): inhibition of TCR-mediated signal transduction. J. Immunol. 163 (1999) 682-688
96. Nielsen C., Ohm-Laursen L., Barington T., Husby S., and Lillevang S.T. Alternative splice variants of the human PD-1 gene. Cell Immunol. 235 (2005) 109-116
97. Nielsen G.P., O'Connell J.X., Wehrli B.M., and Rosenberg A.E. Collagen-rich tumors of soft tissues: an overview. Adv. Anat. Pathol. 10 (2003) 179-199
98. Nimmerjahn F., and Ravetch J.V. Fc gamma receptors: old friends and new family members. Immunity 24 (2006) 19-28
99. Nishimura H., Nose M., Hiai H., Minato N., and Honjo T. Development of lupus-like autoimmune diseases by disruption of the PD-1 gene encoding an ITIM motif-carrying immunoreceptor. Immunity 11 (1999) 141-151
100. Nitschke L. The role of CD22 and other inhibitory co-receptors in B-cell activation. Curr. Opin. Immunol. 17 (2005) 290-297
101. O'Keefe T.L., Williams G.T., Davies S.L., and Neuberger M.S. Hyperresponsive B cells in CD22-deficient mice. Science 274 (1996) 798-801
102. Oaks M.K., Hallett K.M., Penwell R.T., Stauber E.C., Warren S.J., and Tector A.J. A native soluble form of CTLA-4. Cell Immunol. 201 (2000) 144-153
103. Ohtsubo K., and Marth J.D. Glycosylation in cellular mechanisms of health and disease. Cell 126 (2006) 855-867
104. Okazaki T., and Honjo T. The PD-1-PD-L pathway in immunological tolerance. Trends Immunol. 27 (2006) 195-201
105. Oldenborg P.A., Zheleznyak A., Fang Y.F., Lagenaur C.F., Gresham H.D., and Lindberg F.P. Role of CD47 as a marker of self on red blood cells. Science 288 (2000) 2051-2054
106. Olsson M., Nilsson A., and Oldenborg P.A. Target cell CD47 regulates macrophage activation and erythrophagocytosis. Transfus. Clin. Biol. 13 (2006) 39-43
107. Otipoby K.L., Andersson K.B., Draves K.E., Klaus S.J., Farr A.G., Kerner J.D., Perlmutter R.M., Law C.L., and Clark E.A. CD22 regulates thymus-independentresponses and the lifespan of B cells. Nature 384 (1996) 634-637
108. Ouyang W., Xue J., Liu J., Jia W., Li Z., Xie X., Liu X., Jian J., Li Q., Zhu Y., Yang A., and Jin B. Establishment of an ELISA system for determining soluble LAIR-1 levels in sera of patients with HFRS and kidney transplant. J. Immunol. Methods 292 (2004) 109-117
109. Pan C., Baumgarth N., and Parnes J.R. CD72-deficient mice reveal nonredundant roles of CD72 in B cell development and activation. Immunity 11 (1999) 495-506
110. Parikka M., Kainulainen T., Tasanen K., Vaananen A., Bruckner-Tuderman L., and Salo T. Alterations of collagen XVII expression during transformation of oral epithelium to dysplasia and carcinoma. J. Histochem. Cytochem. 51 (2003) 921-929
111. Peaker C.J., and Neuberger M.S. Association of CD22 with the B cell antigen receptor. Eur. J. Immunol. 23 (1993) 1358-1363
112. Pflugh D.L., Maher S.E., and Both well A.L. Ly-6 superfamily members Ly-6A/E, Ly-6C, and Ly-6I recognize two potential ligands expressed by B lymphocytes. J. Immunol. 169 (2002) 5130-5136
113. Pritchard N.R., and Smith K.G. B cell inhibitory receptors and autoimmunity. Immunology 108 (2003) 263-273
114. Ravetch J.V., and Bolland S. IgG Fc receptors. Annu. Rev. Immunol. 19 (2001) 275-290
115. Ravetch J.V., and Lanier L.L. Immune inhibitory receptors. Science 290 (2000) 84-89
116. Roepman P., Wessels L.F., Kettelarij N., Kemmeren P., Miles A.J., Lijnzaad P., Tilanus M.G., Koole R., Hordijk G.J., van der Vliet P.C., Reinders M.J., Slootweg P.J., and Holstege F.C. An expression profile for diagnosis of lymph node metastases from primary head and neck squamous cell carcinomas. Nat. Genet. 37 (2005) 182-186
117. Rosen D.B., Bettadapura J., Alsharifi M., Mathew P.A., Warren H.S., and Lanier L.L. Cutting edge: lectin-like transcript-1 is a ligand for the inhibitory human NKR-P1A receptor. J. Immunol. 175 (2005) 7796-7799
118. Sansom D.M., Manzotti C.N., and Zheng Y. What's the difference between CD80 and CD86?. Trends Immunol. 24 (2003) 314-319
119. Sato S., Miller A.S., Inaoki M., Bock C.B., Jansen P.J., Tang M.L., and Tedder T.F. CD22 is both a positive and negative regulator of B lymphocyte antigen receptor signal transduction: altered signaling in CD22-deficient mice. Immunity 5 (1996) 551-562
120. Sayos J., Martinez-Barriocanal A., Kitzig F., Bellon T., and Lopez-Botet M. Recruitment of C-terminal Src kinase by the leukocyte inhibitory receptor CD85j. Biochem. Biophys. Res. Commun. 324 (2004) 640-647
121. Sedy J.R., Gavrieli M., Potter K.G., Hurchla M.A., Lindsley R.C., Hildner K., Scheu S., Pfeffer K., Ware C.F., Murphy T.L., and Murphy K.M. B and T lymphocyte attenuator regulates T cell activation through interaction with herpesvirus entry mediator. Nat. Immunol. 6 (2005) 90-98
122. Seiffert M., Cant C., Chen Z., Rappold I., Brugger W., Kanz L., Brown E.J., Ullrich A., and Buhring H.J. Human signal-regulatory protein is expressed on normal, but not on subsets of leukemic myeloid cells and mediates cellular adhesion involving its counter receptor CD47. Blood 94 (1999) 3633-3643
123. Shi W., Kumanogoh A., Watanabe C., Uchida J., Wang X., Yasui T., Yukawa K., Ikawa M., Okabe M., Parnes J.R., Yoshida K., and Kikutani H. The class IV semaphorin CD100 plays nonredundant roles in the immune system: defective B and T cell activation in CD100-deficient mice. Immunity 13 (2000) 633-642
124. Short J.J., Pereboev A.V., Kawakami Y., Vasu C., Holterman M.J., and Curiel D.T. Adenovirus serotype 3 utilizes CD80 (B7.1) and CD86 (B7.2) as cellular attachment receptors. Virology 322 (2004) 349-359
125. Sidorenko S.P., and Clark E.A. The dual-function CD150 receptor subfamily: the viral attraction. Nat. Immunol. 4 (2003) 19-24
126. Simon I., Zhuo S., Corral L., Diamandis E.P., Sarno M.J., Wolfert R.L., and Kim N.W. B7-h4 is a novel membrane-bound protein and a candidate serum and tissue biomarker for ovarian cancer. Cancer Res. 66 (2006) 1570-1575
127. Smith G.M., Biggs J., Norris B., Anderson-Stewart P., and Ward R. Detection of a soluble form of the leukocyte surface antigen CD48 in plasma and its elevation in patients with lymphoid leukemias and arthritis. J. Clin. Immunol. 17 (1997) 502-509
128. Smith P., Walsh C.M., Mangan N.E., Fallon R.E., Sayers J.R., McKenzie A.N., and Fallon P.G. Schistosoma mansoni worms induce anergy of T cells via selective up-regulation of programmed death ligand 1 on macrophages. J. Immunol. 173 (2004) 1240-1248
129. Stamenkovic I., Sgroi D., Aruffo A., Sy M.S., and Anderson T. The B lymphocyte adhesion molecule CD22 interacts with leukocyte common antigen CD45RO on T cells and alpha 2-6 sialyltransferase, CD75, on B cells. Cell 66 (1991) 1133-1144
130. Stanciu L.A., Bellettato C.M., Laza-Stanca V., Coyle A.J., Papi A., and Johnston S.L. Expression of programmed death-1 ligand (PD-L) 1, PD-L2, B7-H3, and inducible costimulator ligand on human respiratory tract epithelial cells and regulation by respiratory syncytial virus and type 1 and 2 cytokines. J. Infect. Dis. 193 (2006) 404-412
131. Sun H., Norris B.J., Atkinson K., Biggs J.C., and Smith G.M. Preclinical antitumor activity of an antibody against the leukocyte antigen CD48. Clin. Cancer Res. 4 (1998) 895-900
132. Thorley-Lawson D.A., Schooley R.T., Bhan A.K., and Nadler L.M. Epstein-Barr virus superinduces a new human B cell differentiation antigen (B-LAST 1) expressed on transformed lymphoblasts. Cell 30 (1982) 415-425
133. Tridandapani S., Siefker K., Teillaud J.L., Carter J.E., Wewers M.D., and Anderson C.L. Regulated expression and inhibitory function of Fc gamma RIIb in human monocytic cells. J. Biol. Chem. 277 (2002) 5082-5089
134. Urmacher C., Cordon-Cardo C., and Houghton A.N. Tissue distribution of GD3 ganglioside detected by mouse monoclonal antibody R24. Am. J. Dermatopathol. 11 (1989) 577-581
135. Vacca, P., Pietra, G., Falco, M., Romeo, E., Bottino, C., Bellora, F., Prefumo, F., Fulcheri, E., Venturini, P.L., Costa, M., Moretta, A., Moretta, L., Mingari, M.C., 2006. Analysis of natural killer cells isolated from human decidua: evidence that 2B4 (CD244) functions as an inhibitory receptor and blocks NK cell function. Blood August 24; [Epub ahead of print].
136. Vaidya S.V., and Mathew P.A. Of mice and men: different functions of the murine and human 2B4 (CD244) receptor on NK cells. Immunol. Lett. 105 (2006) 180-184
137. Vaisanen T., Vaisanen M.R., Autio-Harmainen H., and Pihlajaniemi T. Type XIII collagen expression is induced during malignant transformation in various epithelial and mesenchymal tumours. J. Pathol. 207 (2005) 324-335
138. Varki A., and Angata T. Siglecs-the major subfamily of I-type lectins. Glycobiology 16 (2006) 1R-27R
139. Verbrugge A., Rijkers E.S., de Ruiter T., and Meyaard L. Leukocyte-associated Ig-like receptor-1 has SH2 domain-containing phosphatase-independent function and recruits C-terminal Src kinase. Eur. J. Immunol. 36 (2006) 190-198
140. Vieites J.M., de la T.R., Ortega M.A., Montero T., Peco J.M., Sanchez-Pozo A., Gil A., and Suarez A. Characterization of human cd200 glycoprotein receptor gene located on chromosome 3q12-13. Gene 311 (2003) 99-104
141. Voigt S., Sandford G.R., Hayward G.S., and Burns W.H. The English strain of rat cytomegalovirus (CMV) contains a novel captured CD200 (vOX2) gene and a spliced CC chemokine upstream from the major immediate-early region: further evidence for a separate evolutionary lineage from that of rat CMV Maastricht. J. Gen. Virol. 86 (2005) 263-274
142. Watanabe N., Gavrieli M., Sedy J.R., Yang J., Fallarino F., Loftin S.K., Hurchla M.A., Zimmerman N., Sim J., Zang X., Murphy T.L., Russell J.H., Allison J.P., and Murphy K.M. BTLA is a lymphocyte inhibitory receptor with similarities to CTLA-4 and PD-1. Nat. Immunol. 4 (2003) 670-679
143. Wilkinson R., Lyons A.B., Roberts D., Wong M.X., Bartley P.A., and Jackson D.E. Platelet endothelial cell adhesion molecule-1 (PECAM-1/CD31) acts as a regulator of B-cell development, B-cell antigen receptor (BCR)-mediated activation, and autoimmune disease. Blood 100 (2002) 184-193
144. Wright G.J., Cherwinski H., Foster-Cuevas M., Brooke G., Puklavec M.J., Bigler M., Song Y., Jenmalm M., Gorman D., McClanahan T., Liu M.R., Brown M.H., Sedgwick J.D., Phillips J.H., and Barclay A.N. Characterization of the CD200 receptor family in mice and humans and their interactions with CD200. J. Immunol. 171 (2003) 3034-3046
145. Wright G.J., Puklavec M.J., Willis A.C., Hoek R.M., Sedgwick J.D., Brown M.H., and Barclay A.N. Lymphoid/neuronal cell surface OX2 glycoprotein recognizes a novel receptor on macrophages implicated in the control of their function. Immunity 13 (2000) 233-242
146. Yada A., Ebihara S., Matsumura K., Endo S., Maeda T., Nakamura A., Akiyama K., Aiba S., and Takai T. Accelerated antigen presentation and elicitation of humoral response in vivo by Fc gammaRIIB- and Fc gammaRI/III-mediated immune complex uptake. Cell Immunol. 225 (2003) 21-32
147. Yazdani U., and Terman J.R. The semaphorins. Genome Biol. 7 (2006) 211
148. Zhang S., Cherwinski H., Sedgwick J.D., and Phillips J.H. Molecular mechanisms of CD200 inhibition of mast cell activation. J. Immunol. 173 (2004) 6786-6793