Discovery of a functional immunoreceptor tyrosine-based switch motif in a 7-transmembrane-spanning receptor: Role in the orexin receptor OX1R-driven apoptosis

FASEB Journal

Volumn 23, Issue 12, 2009, Pages 4069-4080

  El Firar, Aadil ^b   Voisin, Thierry ^a   Rouyer Fessard, Christiane ^b   Ostuni, Mariano A ^b   Couvineau, Alain ^b   Laburthe, Marc ^a  

^a CENTRE DE RECHERCHE BIOMÉDICALE BICHAT BEAUJON CRB3   (France)

^b NONE

Author keywords

G protein coupled receptor; Neuropeptide; Protein tyrosine phosphatase; SHP 2; Tyrosine based motifs

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN; INOSITOL PHOSPHATE; MEMBRANE RECEPTOR; OREXIN; OREXIN 1 RECEPTOR; PHENYLALANINE; PHOSPHOTYROSINE; PROTEIN TYROSINE PHOSPHATASE SHP 2; TYROSINE;

AMINO ACID SEQUENCE; ANIMAL CELL; APOPTOSIS; ARTICLE; CALCIUM TRANSPORT; CANCER CELL; CHO CELL; CONTROLLED STUDY; GENE MUTATION; MOLECULAR MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION;

AMINO ACID MOTIFS; ANIMALS; APOPTOSIS; CELL MEMBRANE; CHO CELLS; CRICETINAE; CRICETULUS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MODELS, MOLECULAR; NEUROPEPTIDES; PROTEIN CONFORMATION; RECEPTORS, G-PROTEIN-COUPLED; RECEPTORS, NEUROPEPTIDE; RECOMBINANT PROTEINS;

EID: 72749110288     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.09-131367     Document Type: Article

References (45)

1. Sakurai, T., Amemiya, A., Ishii, M., Matsuzaki, I., Chemelli, R. M., Tanaka, H., Williams, S. C., Richardson, J. A., Kozlowski, G. P., Wilson, S., Arch, J. R., Buckingham, R. E., Haynes, A. C., Carr, S. A., Annan, R. S., McNulty, D. E., Liu, W. S., Terrett, J. A., Elshourbagy, N. A., Bergsma, D. J., and Yanagisawa, M. (1998) Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 92, 573-585 (Pubitemid 28101119)
2. De Lecea, L., Kilduff, T. S., Peyron, C., Gao, X., Foye, P. E., Danielson, P. E., Fukuhara, C., Battenberg, E. L., Gautvik, V. T., Bartlett, F. S., Frankel, W. N., van den Pol, A. N., Bloom, F. E., Gautvik, K. M., and Sutcliffe, J. G. (1998) The hypocretins: hypothalamus-specific peptides with neuroexcitatory activity. Proc. Natl. Acad. Sci. U. S. A. 95, 322-327 (Pubitemid 28103952)
3. Nishino, S. (2007) Clinical and neurobiological aspects of narcolepsy. Sleep Med. 8, 373-399
4. Williams, R. H., and Burdakov, D. (2008) Hypothalamic orexins/hypocretins as regulators of breathing. Expert Rev. Mol. Med. 10, e28
5. Harris, G. C., and Aston-Jones, G. (2006) Arousal and reward: a dichotomy in orexin function. Trends Neurosci. 29, 571-577
6. Boutrel, B., Kenny, P. J., Specio, S. E., Martin-Fardon, R., Markou, A., Koob, G. F., and De Lecea, L. (2005) Role for hypocretin in mediating stress-induced reinstatement of cocaine-seeking behavior. Proc. Natl. Acad. Sci. U. S. A. 102, 19168-19173 (Pubitemid 43049584)
7. Boutrel, B., and De Lecea, L. (2008) Addiction and arousal: the hypocretin connection. Physiol. Behav. 93, 947-951
8. Voisin, T., Rouet-Benzineb, P., Reuter, N., and Laburthe, M. (2003) Orexins and their receptors: structural aspects and role in peripheral tissues. Cell. Mol. Life Sci. 60, 72-87 (Pubitemid 36223118)
9. Heinonen, M. V., Purhonen, A. K., Makela, K. A., and Herzig, K. H. (2008) Functions of orexins in peripheral tissues. Acta Physiol. (Oxf.) 192, 471-485
10. Zhu, Y., Miwa, Y., Yamanaka, A., Yada, T., Shibahara, M., Abe, Y., Sakurai, T., and Goto, K. (2003) Orexin receptor type-1 couples exclusively to pertussis toxin-insensitive G-proteins, while orexin receptor type-2 couples to both pertussis toxin-sensitive and -insensitive G-proteins. J. Pharmacol. Sci. 92, 259-266 (Pubitemid 36992313)
11. 2+ signalling by the orexin receptor type 1. Biochem. Pharmacol. 71, 827-836
12. 1 receptor suppress cell growth by inducing apoptosis. J. Biol. Chem. 279, 45875-45886
13. Voisin, T., Firar, A. E., Avondo, V., and Laburthe, M. (2006) Orexin-induced apoptosis: the key role of the seven-transmembrane domain orexin type 2 receptor. Endocrinology 147, 4977-4984 (Pubitemid 44402205)
14. Voisin, T., El Firar, A., Rouyer-Fessard, C., Gratio, V., and Laburthe, M. (2008) A hallmark of immunoreceptor, the tyrosine-based inhibitory motif ITIM, is present in the G protein-coupled receptor OX1R for orexins and drives apoptosis: a novel mechanism. FASEB J. 22, 1993-2002 (Pubitemid 351811475)
15. Daeron, M., Jaeger, S., Du, P. L., and Vivier, E. (2008) Immunoreceptor tyrosine-based inhibition motifs: a quest in the past and future. Immunol. Rev. 224, 11-43
16. Ravetch, J. V., and Lanier, L. L. (2000) Immune inhibitory receptors. Science 290, 84-89
17. Bruhns, P., Marchetti, P., Fridman, W. H., Vivier, E., and Daeron, M. (1999) Differential roles of N- and C-terminal immunoreceptor tyrosine-based inhibition motifs during inhibition of cell activation by killer cell inhibitory receptors. J. Immunol. 162, 3168-3175 (Pubitemid 29313562)
18. Eissmann, P., Beauchamp, L., Wooters, J., Tilton, J. C., Long, E. O., and Watzl, C. (2005) Molecular basis for positive and negative signaling by the natural killer cell receptor 2B4 (CD244). Blood 105, 4722-4729 (Pubitemid 40807295)
19. Ostrakhovitch, E. A., and Li, S. S. (2006) The role of SLAM family receptors in immune cell signaling. Biochem. Cell Biol. 84, 832-843 (Pubitemid 46450684)
20. Shlapatska, L. M., Mikhalap, S. V., Berdova, A. G., Zelensky, O. M., Yun, T. J., Nichols, K. E., Clark, E. A., and Sidorenko, S. P. (2001) CD150 association with either the SH2-containing inositol phosphatase or the SH2-containing protein tyrosine phosphatase is regulated by the adaptor protein SH2D1A. J. Immunol. 166, 5480-5487
21. Sidorenko, S. P., and Clark, E. A. (2003) The dual-function CD150 receptor subfamily: the viral attraction. Nat. Immunol. 4, 19-24
22. Chen, L., Sung, S. S., Yip, M. L., Lawrence, H. R., Ren, Y., Guida, W. C., Sebti, S. M., Lawrence, N. J., and Wu, J. (2006) Discovery of a novel Shp2 protein tyrosine phosphatase inhibitor. Mol. Pharmacol. 70, 562-570 (Pubitemid 44092317)
23. Duchesne, C., Charland, S., Asselin, C., Nahmias, C., and Rivard, N. (2003) Negative regulation of β-catenin signaling by tyrosine phosphatase SHP-1 in intestinal epithelial cells. J. Biol. Chem. 278, 14274-14283 (Pubitemid 36799976)
24. Pei, D., Lorenz, U., Klingmuller, U., Neel, B. G., and Walsh, C. T. (1994) Intramolecular regulation of protein tyrosine phosphatase SH-PTP1: a new function for Src homology 2 domains. Biochemistry 33, 15483-15493
25. Pei, D., Wang, J., and Walsh, C. T. (1996) Differential functions of the two Src homology 2 domains in protein tyrosine phosphatase SH-PTP1. Proc. Natl. Acad. Sci. U. S. A. 93, 1141-1145 (Pubitemid 26052854)
26. 2-adrenergic G protein-coupled receptor. Science 318, 1258-1265
27. Couvineau, A., Fabre, C., Gaudin, P., Maoret, J. J., and Laburthe, M. (1996) Mutagenesis of N-glycosylation sites in the human vasoactive intestinal peptide 1 receptor: evidence that asparagine 58 or 69 is crucial for correct delivery of the receptor to plasma membrane. Biochemistry 35, 1745-1752 (Pubitemid 26062623)
28. 2+ channels. Neuroreport 12, 2017-2020
29. Barrow, A. D., and Trowsdale, J. (2006) You say ITAM and I say ITIM, let's call the whole thing off: the ambiguity of immunoreceptor signalling. Eur. J. Immunol. 36, 1646-1653
30. Palczewski, K., Kumasaka, T., Hori, T., Behnke, C. A., Motoshima, H., Fox, B. A., Le Trong, I., Teller, D. C., Okada, T., Stenkamp, R. E., Yamamoto, M., and Miyano, M. (2000) Crystal structure of rhodopsin: a G protein-coupled receptor. Science 289, 739-745 (Pubitemid 30650186)
31. Gether, U., Asmar, F., Meinild, A. K., and Rasmussen, S. G. (2002) Structural basis for activation of G-protein-coupled receptors. Pharmacol. Toxicol. 91, 304-312 (Pubitemid 36132435)
32. Hof, P., Pluskey, S., Dhe-Paganon, S., Eck, M. J., and Shoelson, S. E. (1998) Crystal structure of the tyrosine phosphatase SHP-2. Cell 92, 441-450 (Pubitemid 28101108)
33. Lee, C. H., Kominos, D., Jacques, S., Margolis, B., Schlessinger, J., Shoelson, S. E., and Kuriyan, J. (1994) Crystal structures of peptide complexes of the amino-terminal SH2 domain of the Syp tyrosine phosphatase. Structure 2, 423-438 (Pubitemid 2085245)
34. Ferjoux, G., Lopez, F., Esteve, J. P., Ferrand, A., Vivier, E., Vely, F., Saint-Laurent, N., Pradayrol, L., Buscail, L., and Susini, C. (2003) Critical role of Src and SHP-2 in sst2 somatostatin receptor-mediated activation of SHP-1 and inhibition of cell proliferation. Mol. Biol. Cell 14, 3911-3928 (Pubitemid 37151636)
35. Gentili, C., Boland, R., and Russo de Boland, A. (2006) Implication of Gβγ proteins and c-SRC tyrosine kinase in parathyroid hormone-induced signal transduction in rat enterocytes. J. Endocrinol. 188, 69-78
36. Neel, B. G., Gu, H., and Pao, L. (2003) The 'Shp'ing news: SH2 domain-containing tyrosine phosphatases in cell signaling. Trends Biochem. Sci. 28, 284-293 (Pubitemid 36776291)
37. Imhof, D., Wavreille, A. S., May, A., Zacharias, M., Tridandapani, S., and Pei, D. (2006) Sequence specificity of SHP-1 and SHP-2 Src homology 2 domains: critical roles of residues beyond the pY+3 position. J. Biol. Chem. 281, 20271-20282 (Pubitemid 44065802)
38. Songyang, Z., Shoelson, S. E., McGlade, J., Olivier, P., Pawson, T., Bustelo, X. R., Barbacid, M., Sabe, H., Hanafusa, H., and Yi, T. (1994) Specific motifs recognized by the SH2 domains of Csk, 3BP2, fps/fes, GRB-2, HCP, SHC, Syk, and Vav. Mol. Cell. Biol. 14, 2777-2785 (Pubitemid 24108258)
39. Sayos, J., Wu, C., Morra, M., Wang, N., Zhang, X., Allen, D., van Schaik, S., Notarangelo, L., Geha, R., Roncarolo, M. G., Oettgen, H., De Vries, J. E., Aversa, G., and Terhorst, C. (1998) The X-linked lymphoproliferative-disease gene product SAP regulates signals induced through the co-receptor SLAM. Nature 395, 462-469 (Pubitemid 28462434)
40. Chemnitz, J. M., Parry, R. V., Nichols, K. E., June, C. H., and Riley, J. L. (2004) 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. 173, 945-954
41. Kumaresan, P. R., Lai, W. C., Chuang, S. S., Bennett, M., and Mathew, P. A. (2002) CS1, a novel member of the CD2 family, is homophilic and regulates NK cell function. Mol. Immunol. 39, 1-8 (Pubitemid 35245377)
42. Burshtyn, D. N., Scharenberg, A. M., Wagtmann, N., Rajagopalan, S., Berrada, K., Yi, T., Kinet, J. P., and Long, E. O. (1996) Recruitment of tyrosine phosphatase HCP by the killer cell inhibitor receptor. Immunity 4, 77-85 (Pubitemid 26056459)
43. Eck, M. J., Pluskey, S., Trub, T., Harrison, S. C., and Shoelson, S. E. (1996) Spatial constraints on the recognition of phosphoproteins by the tandem SH2 domains of the phosphatase SH-PTP2. Nature 379, 277-280 (Pubitemid 26025216)
44. Duchene, J., Schanstra, J. P., Pecher, C., Pizard, A., Susini, C., Esteve, J. P., Bascands, J. L., and Girolami, J. P. (2002) A novel protein-protein interaction between a G protein-coupled receptor and the phosphatase SHP-2 is involved in bradykinin-induced inhibition of cell proliferation. J. Biol. Chem. 277, 40375-40383 (Pubitemid 35215611)
45. Vatinel, S., Ferrand, A., Lopez, F., Kowalski-Chauvel, A., Esteve, J. P., Fourmy, D., Dufresne, M., and Seva, C. (2006) An ITIM-like motif within the CCK2 receptor sequence required for interaction with SHP-2 and the activation of the AKT pathway. Biochim. Biophys. Acta 1763, 1098-1107 (Pubitemid 44466114)