An immunoreceptor tyrosine-based inhibitory motif, with serine at site Y-2, binds SH2-domain-containing phosphatases

European Journal of Biochemistry

Volumn 267, Issue 3, 2000, Pages 703-711

  Philosof Oppenheimer, Rachel ^a   Hampe, Christiane S ^a   Schlessinger, Karni ^a   Fridkin, Mati ^a   Pecht, Israel ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

Author keywords

MAFA; Mast cells; Transmembranal signaling

Indexed keywords

AMINO ACID; EPITOPE; ISOENZYME; LEUKOCYTE ANTIGEN; MAST CELL FUNCTION ASSOCIATED ANTIGEN; PHOSPHATASE; PROTEIN TYROSINE PHOSPHATASE; SERINE; TYROSINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTIGEN BINDING; ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; ENZYME BINDING; MAST CELL; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; RAT; REACTION ANALYSIS; STRUCTURE ACTIVITY RELATION;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, MONOCLONAL; BINDING SITES; CELL LINE; LECTINS, C-TYPE; MAST CELLS; MEMBRANE GLYCOPROTEINS; MOLECULAR SEQUENCE DATA; PHOSPHORIC MONOESTER HYDROLASES; RATS; RECEPTORS, IGE; SRC HOMOLOGY DOMAINS; TYROSINE;

ANIMALIA;

EID: 0033965088     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1327.2000.01044.x     Document Type: Article

References (66)

1. 1. Conrad, D.H. & Froese, A. (1978) Characterization of the target cell receptor for IgE. III. Properties of the receptor isolated from rat basophilic leukemia cells by affinity chromatography. J. Immunol. 120, 429-437.
2. 2. Kulczycki, A.J. & Metzger, H. (1974) The interaction of IgE with rat basophilic leukemia cells. II: Quantitative aspects of the binding reaction. J. Exp. Med. 140, 1676-1695.
3. 3. Sterk, A. & Ishizaka, K. (1982) Binding properties of IgE receptors on normal mouse mast cells. J. Immunol. 128, 838-843.
4. 4. Keegan, A.D. & Paul, W.E. (1992) Multi-chain immune recognition receptors: similarities in structure and signaling pathways. Immunol. Today 13, 63-68.
5. 5. Reth, M. (1989) Antigen receptor tail clue. Nature 338, 383-386.
6. 6. Cambier, J.C. (1995) New nomenclature for the Reth motif (or ARH1/TAM/ARAM/YXXL). Immunol. Today 16, 110-112.
7. 7. Weiss, A. (1993) T cell antigen receptor signal transduction: a tail of tails and cytoplasmic protein-tyrosine kinases. Cell 73, 209-212.
8. 8. Pleinman, C., D'Ambrosio, D. & Cambier, J.C. (1994) The B cell antigen receptor complex: structure and signal transduction. Immunol. Today 15, 393-399.
9. 9. Amigorena, S., Bonnerot, C., Drake, J., Choqet, D., Hunziker, W., Guillet, J.G., Webster, P., Sautes, C., Mellman, I. & Fridman, W.H. (1992) Cytoplasmic domain heterogeneity and functions of IgG Fc receptors in B lymphocytes. Science 256, 1808-1812.
10. gRIIB modulates B-bell signaling. Nature 368, 70-73.
11. 11. Daeron, M., Latour, S., Malbec, O., Espinosa, E., Pina, P., Pasmans, S. & Fridman, W.H. (1995) The same tyrosine-based inhibition motif in the intracytoplasmic domain of FcRIIB, regulates negatively BCR-, TCR-, and Fc-dependent cell activation. Immunity 3, 635-646.
12. 12. Daeron, M., Malbec, O., Latour, S., Arock, M. & Fridman, W.H. (1995) Regulation of high-affinity IgE receptor-mediated mast cell activation by murine low-affinity IgG receptors. J. Clin. Invest. 95, 577-585.
13. 13. Rennard, V., Cambiaggi, A., Vely, F., Blery, M., Olcese, L., Olivero, S., Bouchet, M. & Vivier, E. (1997) Transduction of cytotoxic signals in natural killer cells: a general model of fine tuning between activatory and inhibitory pathways in lymphocytes. Immunol. Rev. 155, 205-221.
14. 14. Lanier, L.L. & Phillips, J.H. (1995) NK cell recognition of major histocompatibility complex class I molecules. Semin. Immunol. 7, 75-82.
15. 15. Raulet, D.H., Correa, L., Dorfman, J. & Wu, M.F. (1995) Inhibitory effects of class I molecules on murine NK cells: speculations on function, specificity and self-tolerance. Semin. Immunol. 7, 103-107.
16. 16. Yokoyama, W.M., Daniels, B.F., Seaman, W.E., Hunriker, R., Margulies, D.H. & Smith, H.R.C. (1995) A family of murine NK cell receptors specific for target cell MHC class I molecules. Semin. Immunol. 7, 89-101.
17. 17. Correa, I., Corral, L. & Raulet, D.H. (1994) Multiple natural killer cell-activating signals are inhibited by major histocompatibility complex class I expression in target cells. Eur. J. Immunol. 24, 1323-1331.
18. 18. Leibson, P.J. (1995) MHC-recognizing receptors: they're not just for T cells anymore. Immunity 3, 5-8.
19. 19. Phillips, J.H., Gumperz, J.E., Parham, P. & Lanier, L.L. (1995) Superantigen-dependent cell-mediated cytotoxicity inhibited by MHC class I receptors on T lymphocytes. Science 268, 403-405.
20. 20. Mingari, M.C., Cambiaggi, A., Schiavetti, F., Melioli, G., Ferrini, S. & Poggi, A. (1995) Cytolytic T lymphocytes displaying natural killer (NK)-like activity: expression of NK-related functional receptors for HLA class I molecules (p58 and CD49) and inhibitory effect on the TCR-mediated target cell lysis or lymphokine production. Int. Immunol. 7, 697-703.
21. + lymphoproliferative diseases of granular lymphocytes displays either inhibitory or stimulatory functions. Blood 87, 2369-2375.
22. 22. D'Ambrosio, D., Hippen, K.H., Minskoff, S.A., Mellman, I., Pani, G., Siminovitch, K.A. & Cambier, J.C. (1995) Recruitment and activation of PTP1C in negatine regulation of antigen receptor signalling by FcRIIB1. Science 268, 293-296.
23. 23. Burshtyn, D.N., Scharenberg, A.M., Wagtmann, N., Rajogopalan, S., Berrada, K., Yi, T., Kinet, J.P. & Long, E.O. (1996) Recruitment of tyrosine phosphatase HCP by the killer cell inhibitory receptor. Immunity 4, 77-85.
24. 24. Olcese, L., Lang, P., Vely, F., Cambiaggi, A., Marguet, D., Blery, M., Hippen, K.L., Biassoni, R., Moretta, L., Cambier, J.C. & Vivier, E. (1996) Human and mouse killer-cell inhibitory receptors recruit PTP1C. J. Immunol. 156, 4531-4535.
25. 25. Ono, M., Bolland, S., Tempst, P. & Ravetch, J.V. (1996) Role of the inositol phosphatase SHIP in the negative regulation of the immune system by the receptor FcRIIB. Nature 383, 263-266.
26. 26. D'Ambrosio, D., Fong, D.C. & Cambier, J.C. (1996) The SHIP phosphatase becomes associated with FcRIIB1 and is tyrosine phosphorylated during 'negative' signaling. Immunol. Lett. 54, 77-82.
27. 27. Fong, D.C., Malbec, O., Arock, M., Cambier, J.C., Fridman, W.H. & Daeron, M. (1996) Selective in vivo recruitment of phosphatidylinositol phosphatase SHIP by phosphorylated FcRIIB during negative regulation of IgE-dependent mouse mast cell activation. Immunol. Lett. 54, 83-91.
28. 28. Cambier, J.C. (1997) Inhibitory receptors abound? Proc. Natl Acad. Sci. USA 94, 5993-5995.
29. 29. Daeron, M. (1996) Building up the family of ITIM-bearing negative co-receptors. Immunol. Lett. 54, 73-76.
30. 30. Brooks, A.G., Posch, P.E., Scorzelli, C.J., Borrego, F. & Coligan, J.E. (1997) NKG2A complexed with CD94 defines a novel inhibitory natural killer cell receptor. J. Exp. Med. 185, 795-800.
31. 31. Le Drean, E., Vely, F., Olcese, L., Cambiaggi, A., Guia, S., Krystal, G., Gervois, N., Moretta, A., Jotereau, F. & Vivier, E. (1998) Inhibition of antigen-induced T cell response and antibody-induced NK cell cytotoxicity by NKG2A: association of NKG2A with SHP-1 and SHP-2 protein-tyrosine phosphatases. Eur. J. Immunol. 28, 264-276.
32. 32. Kubagawa, H., Burrows, P.D. & Cooper, M.D. (1997) A novel pair of immunoglobulin-like receptor expressed by B cells and myeloid cells. Proc. Natl Acad. Sci. USA 94, 5261-5266.
33. 33. Blery, M., Kubagawa, H., Chen, C.-C., Vely, F., Cooper, M. & Vivier. E. (1998) The paired Ig-like receptor PIR-B is an inhibitory receptor that recruits the protein tyrosine phosphatase SHP-1. Proc. Natl Acad. Sci. USA 95, 2446-2451.
34. 34. Ortega, E. & Pecht, I. (1988) A monoclonal antibody that inhibits secretion from rat basophilic leukemia cells and binds to a novel membrane component. J. Immunol. 141, 4324-4332.
35. 35. Guthman, M., Tal, M. & Pecht, I. (1995) A new member of the C-type lectin family is a modulator of the mast cell secretory response. J. Arch. Allerg. Immunol. 107, 82-86.
36. 36. Guthman, M., Tal, M. & Pecht, I. (1995) A secretion inhibitory signal transduction molecule on mast cells is another C-type lectin. Proc. Natl Acad. Sci. USA 92, 9397-9401.
37. 37. Binsack, R. & Pecht, I. (1997) The mast cell function-associated antigen (MAFA) exhibits saccharide binding capacity. Eur. J. Immunol. 27, 2557-2561.
38. 38. Kitas, E., Kung, E. & Bannwarth, W. (1994) Chemical synthesis of O-thiophosphotyrosyl peptides. Int. J. Peptide Protein Res. 43, 146-153.
39. 39. Eisen, H.N., Kern, M., Newton, W. & Helmreich, E. (1959) A study of the distribution of 2,4-dinitrobenzene sensitizers between isolated lymph nodes cells and extracellular medium in relation to induction of contact skin sensitivity. J. Exp. Med. 110, 187-206.
40. 40. Hardy, R. (1986) Handbook of Experimental Immunology (Weir, D.M., ed), p. 405. Blackwell Scientific, Palo Alto, CA.
41. b heavy chain haplotype. Eur. J. Immunol. 11, 527-529.
42. 42. Atherton, E. & Sheppared, R.C. (1989) Solid Phase Peptide Synthesis, A Practical Approach. Oxford University Press, Oxford, UK.
43. 43. Wilchek, M. & Miron, T. (1982) Immobilization of enzymes and affinity ligands onto agarose via stable and uncharged carbamate linkage. Biochem. Int. 4, 629-635.
44. 44. Bernatowicz, M.S. & Matsueda, G.R. (1986) Preparation of peptide-protein immunogens using N-succinimidyl bromoacetate as a heterobifunctional crosslinking reagent. Anal. Biochem. 155, 95-102.
45. 45. Miron, T. & Wilchek, M. (1981) Polyacrylhydrazido-agarose: preparation via periodate oxidation and use for immobilization and affinity chromatography. J. Chromat. 215, 55-63.
46. 46. Ellman, G.L. (1959) Tissue sulfhydryl groups. Arch. Biochem. Biophys. 82, 70-77.
47. 47. Barsumian, E.L., Isersky, C., Petrino, M.G. & Siraganian, R.P. (1981) IgE-induced histamine release from rat basophilic leukemia cell lines: isolation of releasing and non-releasing clones. Eur. J. Immunol. 11, 317-323.
48. 48. Mitchell, C.A., Connolly, T.M. & Majerus, P.W. (1989) Identification and isolation of a 75-kDa polyphosphate-5-phosphatase from human platelets. J. Biol. Chem. 264, 8873-8877.
49. 49. Crowley, M.T., Harmer, S.L. & DeFranco, A.L. (1996) Activation-induced association of a 145-kDa tyrosine-phosphorylated protein with Shc and Syk in B lymphocytes and macrophages. J. Biol. Chem. 271, 1145-1152.
50. 50. Kimura, T., Sakamoto, H., Appella, E. & Siraganian, R.P. (1997) The negative signaling molecule SH2 domain containing inositol polyphosphate 5-phosphatase (SHIP) binds to tyrosine-phosphorylated β subunit of the high affinity IgE receptor. J. Biol. Chem. 272, 13991-13996.
51. 51. Famiglietti, S.J., Nakamura, K. & Cambier, J.C. (1999) Unique features of SHIP, SHP-1 and SHP-2 binding to FcRIIb revealed by surface plasmon resonance analysis. Immunol. Lett. 68, 35-40.
52. 52. Anderson, C.A. & Sinclair, R.St C. (1998) FcR-mediated inhibition of cell activation and other forms of coinhibition. Crit. Rev. Immunol. 18, 525-544.
53. 53. Vely, F., Olivero, S., Olcese, L., Moretta, A., Damen, J.J., Liu, L., Krystal, G., Cambier, J.C., Daeron, M. & Vivier, E. (1997) Differential association of phosphatases with hematopoietic co-receptors bearing tyrosine-based inhibition motifs. Eur. J. Immunol. 27, 1994-2000.
54. 54. Huyer, G., Min Li, Z., Adam, M., Huckle, W.R. & Ramachandran, C. (1995) Direct determination of the sequence recognition requirements of the SH2 domains of SH-PTP2. Biochem. 34, 1040-1049.
55. 55. Songyang, Z., Shelson, S.E., Mcglade, J., Oliver, P., Pawson, T., Bustelo, X.R., Barbacid, M., Sabe, H., Hanafusa, H., Yi, T., Ren, R., Baltimore, D., Ratnofsky, S., Feldman, R.A. & Cantley, L.C. (1994) Specific motifs recognized by SH2 domains of Csk, 3 BP2, fps/fes, Grb-2, HCP, SHC, Syk, and Vav. Mol. Cell. Biol. 14, 2777-2785.
56. 56. Thomas, M.L. (1995) Of ITAMs and ITIMs: turning of and on B-cell antigen receptor. J. Exp. Med. 181, 1953-1956.
57. 57. Doody, G.M., Justement, L.B., Delibrias, C.C., Matthewes, R.J., Thomas, M.C. & Fearon, D.T. (1995) A role in B cell activation for CD22 and the protein tyrosine phosphatase SHP. Science 259, 242-245.
58. 58. Kimura, T., Zhang, J., Sagawa, K., Appella, E. & Siraganian, R.P. (1997) Syk-independent tyrosine phosphorylation and association of the protein tyrosine phosphatases SHP-1 and SHP-2 with the high affinity IgE receptor. J. Immunol. 159, 4426-4434.
59. 59. Damen, J.E., Liu, L., Rosten, P., Humphries, R.K., Jefferson, A.B., Majerus, P.W. & Krystal, G. (1996) The 145-kDa protein induced to associate with SHC by multiple cytokines is an inositol tetraphosphate and phosphatidylinositol 3,4,5-triphosphate 5-phosphatase. Proc. Natl Acad. Sci. USA 93, 1689-1693.
60. 60. Osborne, M.A., Zenner, G., Lubinus, M., Zhang, Z., Songyang, Z., Cantley, L.C., Majerus, P., Burn, P. & Kochan, J.P. (1996) The inositol 5′-phosphatase SHIP binds to immunoreceptor signaling motif and responds to high affinity IgE receptor aggregation. J. Biol. Chem. 271, 29271-29278.
61. 61. Berridge, M.J. (1993) Inositol triphosphate and calcium signaling. Nature 361, 315-325.
62. 62. Miyazaki, S. (1995) Inositol triphosphate receptor mediated spatiotemporal calcium signaling. Curr. Opin. Cell Biol. 7, 190-196.
63. 3)/ Tec kinase-dependent calcium signaling pathway: a target for SHIP-mediated inhibitory signals. EMBO J. 17, 1961-1972.
64. 64. Bolland, S., Pearse, R.N., Kurosaki, T. & Ravetch, J.V. (1998) SHIP modulates immune receptor responses by regulating membrane association of Btk. Immunity 8, 509-516.
65. 65. Li, H.C., Simmoneli, P.F. & Huan, L.J. (1988) Preparation of protein phosphatase-resistant substrates using adenosine 5′-O-(γ-thio) triphosphate. In Methods in Enzymology (Corbin, J.D. & Johnson, R.A., eds), Vol. 159, p. 346. Academic Press, San Diego, CA.
66. 66. Jurgens, L., Jovin, D.A., Pecht, I. & Jovin, T.M. (1996) Proximity relationship between the type I receptor for Fc (FcRI) and the mast cell function-associated antigen (MAFA) studied by donor photobleaching fluorescence resonance energy transfer. Eur. J. Immunol. 269, 84-91.