Channel catfish leukocyte immune-type receptor mediated inhibition of cellular cytotoxicity is facilitated by SHP-1-dependent and -independent mechanisms

Developmental and Comparative Immunology

Volumn 37, Issue 1, 2012, Pages 151-163

  Montgomery, Benjamin C ^a   Cortes, Herman D ^a   Burshtyn, Deborah N ^a   Stafford, James L ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

C terminal Src kinase; Channel catfish; Chimeric receptors; Cytoplasmic tails; Cytotoxicity; Immune tyrosine based inhibition motifs; Immunoglobulin superfamily; Immunoregulatory receptors; Inhibitory signaling; Leukocyte immune type receptors; Lymphokine activated killer cells; Natural killer cells; SH2 domain containing phosphatases; Src family protein tyrosine kinases; Teleosts; Vaccinia virus

Indexed keywords

KILLER CELL IMMUNOGLOBULIN LIKE RECEPTOR 2DL3; LEUKOCYTE IMMUNE TYPE RECEPTOR 1.1B; LEUKOCYTE IMMUNE TYPE RECEPTOR 1.2A; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE PHOSPHATASE SHP 1; RECOMBINANT PROTEIN; REGULATOR PROTEIN; TYROSINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL KILLING; CELL MEDIATED CYTOTOXICITY; CHANNEL CATFISH; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; INHIBITION KINETICS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; SPLEEN; VACCINIA VIRUS;

ICTALURUS PUNCTATUS; TELEOSTEI; VACCINIA VIRUS;

EID: 84859872539     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dci.2011.09.005     Document Type: Article

References (80)

1. Anderson S.K., Ortaldo J.R., McVicar D.W. The ever-expanding Ly49 gene family: repertoire and signaling. Immunol. Rev. 2001, 181:79-89.
2. Bakker A.B., Wu J., Phillips J.H., Lanier L.L. NK cell activation: distinct stimulatory pathways counterbalancing inhibitory signals. Hum. Immunol. 2000, 61:18-27.
3. Barclay A.N. Membrane proteins with immunoglobulin-like domains-a master superfamily of interaction molecules. Semin. Immunol. 2003, 14:215-223.
4. Barrow A.D., Trowsdale J. The extended leukocyte receptor complex: diverse ways of modulating immune responses. Immunol. Rev. 2008, 224:98-123.
5. Beebe K.D., Wang P., Arabaci G., Pei D.H. Determination of the binding specificity of the SH2 domains of protein tyrosine phosphatase SHP-1 through the screening of a combinatorial phosphotyrosyl peptide library. Biochemistry 2000, 39:13251-13260.
6. Biassoni R., Cantoni C., Pende D., Sivori S., Parolini S., Vitale M., et al. Human natural killer cell receptors and co-receptors. Immunol. Rev. 2001, 181:203-214.
7. Bjorge J.D., Jakymiw A., Fujita D.J. Selected glimpses into the activation and function of Src kinase. Oncogene 2000, 19:5620-5635.
8. Brdicka T., Pavlistova D., Leo A., Bruyns E., Korinek V., Angelisova P., et al. Phosphoprotein associated with glycosphingolipid-enriched microdomains (PAG), a novel ubiquitously expressed transmembrane adaptor protein, binds the protein tyrosine kinase csk and is involved in regulation of T cell activation. J. Exp. Med. 2000, 191:1591-1604.
9. Brdicková N., Brdicka T., Angelisová P., Horváth O., Spicka J., Hilgert I., et al. LIME: a new membrane Raft-associated adaptor protein involved in CD4 and CD8 coreceptor signaling. J. Exp. Med. 2003, 198:1453-1462.
10. Brown D., Trowsdale J., Allen R. The LILR family: modulators of innate and adaptive immune pathways in health and disease. Tissue Antigens 2004, 64:215-225.
11. Burshtyn D.N., Scharenberg A.M., Wagtmann N., Rajagopalan S., Berrada K., Yi T., et al. Recruitment of tyrosine phosphatase HCP by the killer cell inhibitor receptor. Immunity 1996, 4:77-85.
12. Burshtyn D.N., Yang W., Yi T., Long E.O. A novel phosphotyrosine motif with a critical amino acid at position -2 for the SH2 domain-mediated activation of the tyrosine phosphatase SHP-1. J. Biol. Chem. 1997, 272:13066-13072.
13. Burshtyn D.N., Lam A.S., Weston M., Gupta N., Warmerdam P.A., Long E.O. Conserved residues amino-terminal of cytoplasmic tyrosines contribute to the SHP-1-mediated inhibitory function of killer cell Ig-like receptors. J. Immunol. 1999, 162:897-902.
14. Carlyle J.R., Jamieson A.M., Gasser S., Clingan C.S., Arase H., Raulet D.H. Missing self-recognition of Ocil/Clr-b by inhibitory NKR-P1 natural killer cell receptors. Proc. Natl. Acad. Sci. USA 2004, 101:3527-3532.
15. Cary L.A., Cooper J.A. Molecular switches in lipid rafts. Nature 2000, 404:945-947.
16. Chemnitz J.M., Parry R.V., Nichols K.E., June C.H., Riley J.L. SHP-1 and SHP-2 associate with immunoreceptor tyrosine-based switch motif of programmed death 1 upon primary human T cell stimulation, but only receptor ligation prevents T cell activation. J. Immunol. 2004, 173:945-954.
17. Chong Y.-P., Mulhern T.D., Cheng H.-C. C-terminal kinase (Csk) and CSK-homologous kinase (CHK)-endogenous negative regulators of Src-family protein kinases. Growth Factors 2005, 23:233-244.
18. Chong Y.-P., Chan A.S., Chan K.-C., Williamson N.A., Lerner E.C., Smithgall T.E., et al. C-terminal Src kinase-homologous kinase (CHK), a unique inhibitor inactivating multiple active conformations of Src family tyrosine kinases. J. Biol. Chem. 2006, 281:32988-32999.
19. csk with protein tyrosine phosphatase PEP in T cells and other hemopoietic cells. EMBO J. 1996, 15:4909-4918.
20. Cortes H.D., Montgomery B.C., Verheijen K., García-García E., Stafford J.L. Examination of the stimulatory signaling potential of a channel catfish leukocyte immune-type receptor and associated adaptor. Dev. Comp. Immunol. 2012, 36:62-73.
21. Davidson D., Bakinowski M., Thomas M.L., Horejsi V., Veillette A. Phosphorylation-dependent regulation of T-cell activation by PAG/Cbp, a lipid raft-associated transmembrane adaptor. Mol. Cell. Biol. 2003, 23:2017-2028.
22. Earl P.L., Broder C.C., Long D., Lee S.A., Peterson J., Chakrabarti S., et al. Native oligomeric human immunodeficiency virus type 1 envelope glycoprotein elicits diverse monoclonal antibody reactivities. J. Virol. 1994, 68:3015-3026.
23. Falk N., Ravetch R.V. Fcγ receptors: old friends and new family members. Immunity 2006, 24:19-28.
24. Ford J.W., McVicar D.W. TREM and TREM-like receptors in inflammation and disease. Curr. Opin. Immunol. 2009, 21:38-46.
25. Frame M.C. Src in cancer: deregulation and consequences for cell behaviour. Biochim. Biophys. Acta. 2002, 1602:114-130.
26. Gergely J., Pecht I., Sarmay G. Immunoreceptor tyrosine-based inhibition motif bearing receptors regulate the immunotyrosine-based activation motif-induced activation of immune competent cells. Immunol. Lett. 1999, 68:3-15.
27. Gunturi A., Berg R.E., Forman J. The role of CD94/NKG2 in innate and adaptive immunity. Immunol. Res. 2004, 30:29-34.
28. Hibbs M.L., Harder K.W., Armes J., Kountouri N., Quilici C., Casagranda F., et al. Sustained activation of Lyn tyrosine kinase in vivo leads to autoimmunity. J. Exp. Med. 2002, 196:1593-1604.
29. Imhof D., Wavreille A.-S., May A., Zacharias M., Tridandapani S., Pei D. Sequence specificity of SHP-1 and SHP-2 Src homology 2 domains. Critical roles of residues beyond the pY+3 position. J. Biol Chem. 2006, 281:20271-20282.
30. Irby R.B., Yeatman T.J. Role of Src expression and activation in human cancer. Oncogene 2000, 19:5636-5642.
31. Katz H.R. Inhibition of inflammatory responses by leukocyte Ig-like receptors. Adv. Immunol. 2006, 91:251-272.
32. Kawabuchi M., Satomi Y., Takao T., Shimonishi Y., Nada S., Nagai K., et al. Transmembrane phosphoprotein Cbp regulates the activities of Src-family tyrosine kinases. Nature 2000, 404:999-1003.
33. Kim K.I.A., Mills R.D., Hossain M.I., Chan K.-C., Jarasrassamee B., Jorissen R.N., et al. Structural elements and allosteric mechanisms governing regulation and catalysis of CSK-family kinases and their inhibition of Src-family kinases. Growth Factors 2010, 28:329-350.
34. Kitaura J., Kawakami Y., Maeda-Yamamoto M., Horejsi V., Kawakami T. Dysregulation of Src family kinases in mast cells from epilepsy-resistant ASK versus epilepsy-prone EL mice. J. Immunol. 2007, 178:455-462.
35. Kuster H., Thompson H., Kinet J.P. Characterization and expression of the gene for the human Fc receptor gamma subunit: definition of a new gene family. J. Biol. Chem. 1990, 265:6448-6452.
36. Lanier L.L. Up on the tightrope: natural killer cell activation and inhibition. Nat. Immunol. 2008, 9:495-502.
37. Lanier L.L., Corliss B.C., Phillips J.H. Arousal and inhibition of human NK cells. Immunol. Rev. 1997, 155:145-154.
38. Lanier L.L., Corliss B.C., Wu J., Leong C., Phillips J.H. Immunoreceptor DAP12 bearing a tyrosine-based activation motif is involved in activating NK cells. Nature 1998, 391:703-707.
39. Long E.O. Regulation of immune responses through inhibitory receptors. Annu. Rev. Immuno. 1999, 17:875-904.
40. Long E.O. Negative signalling by inhibitory receptors: the NK cell paradigm. Immunol. Rev. 2008, 224:70-84.
41. Long E.O., Burshtyn D.N., Clark W.P., Peruzzi M., Rajagopalan S., Wagtmann N., et al. Killer cell inhibitory receptors: diversity, specificity, and function. Immunol. Rev. 1997, 155:135-144.
42. López-Botet M., Carretero M., Pérez-Villar J., Bellón T., Llano M., Navarro F. The CD94/NKG2 C-type lectin receptor complex: involvement in NK cell-mediated recognition of HLA class I molecules. Immunol. Res. 1997, 16:175-185.
43. Malek S.N., Dordai D.I., Reim J., Dintzis H., Desiderio S. Malignant transformation of early lymphoid progenitors in mice expressing an activated Blk tyrosine kinase. Proc. Natl. Acad. Sci USA 1998, 95:7351-7356.
44. Mewes J., Verheijen K., Montgomery B.C., Stafford J.L. Stimulatory catfish leukocyte immune-type receptors (IpLITRs) demonstrate a unique ability to associate with adaptor signaling proteins and participate in the formation of homo- and heterodimers. Mol. Immunol. 2009, 47:318-331.
45. Montgomery B.C., Mewes J., Davidson C., Burshtyn D.N., Stafford J.L. Cell surface expression of channel catfish leukocyte immune-type receptors (IpLITRs) and recruitment of both Src homology 2 domain-containing protein tyrosine phosphatases (SHP)-1 and SHP-2. Dev. Comp. Immunol. 2009, 33:570-582.
46. Montgomery B.C., Cortes H.D., Mewes-Ares J., Verheijen K., Stafford J.L. Teleost IgSF immunoregulatory receptors. Dev. Comp. Immunol. 2011, 35:120-134.
47. Nimmerjahn F., Ravetch J.V. Fc-receptors as regulators of immunity. Adv. Immunol. 2007, 96:179-204.
48. Nimmerjahn F., Ravetch J.V. FcγRs in health and disease. Curr. Top. Microbiol. Immunol. 2011, 350:105-125.
49. Okada M., Nada S., Yamanashi Y., Yamamoto T., Nakagawa H. Csk: a protein-tyrosine kinase involved in regulation of Src family kinases. J. Biol. Chem. 1991, 266:24249-24252.
50. Olcese L., Lang P., Vély F., Cambiaggi A., Marguet D., Bléry M., et al. Human and mouse killer-cell inhibitory receptors recruit PTP1C and PTP1D protein tyrosine phosphatases. J. Immunol. 1996, 156:4531-4534.
51. Parham P. Killer cell immunoglobulin-like receptor diversity: balancing signals in the natural killer cell response. Immunol. Lett. 2004, 92:11-13.
52. Peterson M.E., Long E.O. Inhibitory receptor signaling via tyrosine phosphorylation of the adaptor Crk. Immunity 2009, 29:578-588.
53. Ravetch J.V., Lanier L.L. Immune Inhibitory Receptor. Science 2000, 90:84-89.
54. Roussell E., Gerrard J.M., Greenberg A.H. Long-term cultures of human periperhal blood lymphocytes with recombinant human interleukin-2 generate a population of virtually pure CD3+ CD16- CD56- large granular lymphocyte LAK cells. Clin. Exp. Immunol. 1990, 82:416-421.
55. Sayos J., Martinez-Barriocanal A., Kitzig F., Bellon T., Lopez-Botet M. Recruitment of C-terminal Src kinase by the leukocyte inhibitory receptor CD85j. Biochem. Biophys. Res. Commun. 2004, 324:640-647.
56. Sidorenko S.P., Clark E.A. The dual-function CD150 receptor subfamily: the viral attraction. Nat. Immunol. 2003, 4:19-24.
57. Songyang Z., Shoelson S.E., McGlade J., Olivier P., Pawson T., Bustelo X.R., et al. Specific motifs recognized by the SH2 domains of Csk, 3BP2, fps/fes, GRB-2, HCP, SHC, Syk, and Vav. Mol. Cell. Biol. 1994, 14:2777-2785.
58. Stafford J.L., Bengtén E., Du Pasquier L., McIntosh R.D., Quiniou S.M., Clem L.W., et al. A novel family of diversified immunoregulatory receptors in teleosts is homologous to both mammalian Fc receptors and molecules encoded within the leukocyte receptor complex. Immunogenetics 2006, 58:758-773.
59. Stanietsky N., Mandelboim O. Paired NK cell receptors controlling NK cytotoxicity. FEBS Lett. 2010, 584:4895-4900.
60. Stebbins C.C., Watzl C., Billadeau D.D., Leibson P.J., Burshtyn D.N., Long E.O. Vav1 dephosphorylation by the tyrosine phosphatase SHP-1 as a mechanism for inhibition of cellular cytotoxicity. Mol. Cell. Biol. 2003, 23:6291-6299.
61. Steevels T.A.M., Meyaard L. Immune inhibitory receptors: essential regulators of phagocyte function. Eur. J. Immunol. 2011, 41:575-587.
62. Takai T. Fc receptors and their role in immune regulation and autoimmunity. J. Clin. Immunol. 2005, 25:1-18.
63. Thomas S.M., Brugge J.S. Cellular functions regulated by Src family kinases. Annu. Rev. Cell Dev. Biol. 1997, 13:513-609.
64. Thomas R., Matthias T., Witte T. Leukocyte immunoglobulin-like receptors as new players in autoimmunity. Clin. Rev. Allergy Immunol. 2010, 38:159-162.
65. Thompson A.D., Teitell M.A., Arvand A., Denny C.T. Divergent Ewing's sarcoma EWS/ETS fusions confer a common tumorigenic phenotype on NIH3T3 cells. Oncogene 1999, 30:5506-5513.
66. Tybulewicz V.L. Vav-family proteins in T-cell signalling. Curr. Opin. Immunol. 2005, 17:267-274.
67. Underhill D.M., Goodridge H.S. The many faces of ITAMs. Trends Immunol. 2007, 28:66-73.
68. Van den Herik-Oudijk I.E., Ter Bekke M.W., Tempelman M.J., Capel P.J., Van de Winkel J.G. Functional differences between two Fc receptor ITAM signaling motifs. Blood 1995, 86:3302-3307.
69. Veillette A., Thibaudeau E., Latour S. High expression of inhibitory receptor SHPS-1 and its association with protein-tyrosine phosphatase SHP-1 in macrophages. J. Biol. Chem. 1998, 273:22719-22728.
70. Verbrugge A., Rijkers E.S.K., De Ruiter T., Meyaard L. Leukocyte associated Ig-like receptor-1 has SH-2 domain-containing phosphatase independent function and recruits C-terminal Src kinase. Eur. J. Immmunol. 2006, 36:190-198.
71. Vilches C., Parham P. KIR: diverse, rapidly evolving receptors of innate and adaptive immunity. Annu. Rev. Immunol. 2002, 20:17-51.
72. Vivier E., Daeron M. Immunoreceptor tyrosine-based inhibition motifs. Immunol. Today 1997, 18:286-291.
73. Vivier E., Nunès J.A., Vély F. Natural killer cell signaling pathways. Science 2004, 306:1517-1519.
74. Weis W.I., Taylor M.E., Drickamer K. The C-type lectin superfamily in the immune system. Immunol. Rev. 1998, 163:19-34.
75. Willey R.L., Smith D.H., Lasky L.A., Theodore T.S., Earl P.L., Moss B. In vitro mutagenesis identifies a region within the envelope gene of the human immunodeficiency virus that is critical for infectivity. J. Virol. 1988, 62:139-147.
76. Wu J., Cherwinski H., Spies T., Phillips J.H., Lanier L.L. DAP10 and DAP12 form distinct, but functionally cooperative, receptor complexes in natural killer cells. J. Exp. Med. 2000, 192:1059-1068.
77. Yasuda K., Nagafuku M., Shima T., Okada M., Yagi T., Yamada T., et al. Cutting edge: Fyn is essential for tyrosine phosphorylation of Csk-binding protein/phosphoprotein associated with glycolipid-enriched microdomains in lipid rafts in resting T cells. J. Immunol. 2002, 169:2813-2817.
78. Yoder J.A., Litman G.W. The phylogenetic origins of natural killer receptors and recognition: relationships, possibilities, and realities. Immunogenetics 2011, 63:123-141.
79. Yokoyama W.M., Plougastel B.F.M. Immune functions encoded by the natural killer complex. Nat. Rev. Immunol. 2003, 3:304-316.
80. Zöller M., Price M.R., Baldwin R.W. Evaluation of 51Cr release for detecting cell-mediated cytotoxic responses to solid chemically induced rat tumours. Br. J. Cancer 1977, 25:834-843.