Sprouty proteins inhibit receptor-mediated activation of phosphatidylinositol-specific phospholipase C

Molecular Biology of the Cell

Volumn 21, Issue 19, 2010, Pages 3487-3496

  Akbulut, Simge ^a   Reddi, Alagarsamy L ^b   Aggarwal, Priya ^b   Ambardekar, Charuta ^b   Canciani, Barbara ^b   Kim, Marianne K H ^b   Hix, Laura ^b   Vilimas, Tomas ^b   Mason, Jacqueline ^c   Basson, M Albert ^d   Lovatt, Matthew ^e   Powell, Jonathan ^f   Collins, Samuel ^f   Quatela, Steven ^g   Phillips, Mark ^g   Licht, Jonathan D ^a,b  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c PRINCESS MARGARET HOSPITAL   (Canada)

^d KING'S COLLEGE LONDON   (United Kingdom)

^e NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^f JOHNS HOPKINS UNIVERSITY   (United States)

^g NEW YORK UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD69 ANTIGEN; DIACYLGLYCEROL; GROWTH FACTOR; INOSITOL 1,4,5 TRISPHOSPHATE; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL; PHOSPHOLIPASE C GAMMA; PHOSPHOLIPASE C GAMMA1; PHOSPHOLIPASE C GAMMA2; PROTEIN TYROSINE PHOSPHATASE SHP 2; RAS PROTEIN; SMALL INTERFERING RNA; SPROUTY PROTEIN; SPROUTY PROTEIN 1; SPROUTY PROTEIN 2; T LYMPHOCYTE RECEPTOR; TYROSINE; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CALCIUM SIGNALING; CALCIUM TRANSPORT; CONTROLLED STUDY; DOWNSTREAM PROCESSING; ENZYME ACTIVITY; GENE ACTIVITY; GENE OVEREXPRESSION; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; REPORTER GENE; T LYMPHOCYTE; TRANSCRIPTION TERMINATION;

ANIMALS; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, T-LYMPHOCYTE; BIOLOGICAL MARKERS; CALCIUM; DIGLYCERIDES; ENZYME ACTIVATION; IMMUNOPRECIPITATION; INOSITOL 1,4,5-TRISPHOSPHATE; INTRACELLULAR SPACE; LECTINS, C-TYPE; MEMBRANE PROTEINS; MICE; MITOGEN-ACTIVATED PROTEIN KINASES; NIH 3T3 CELLS; PHOSPHOLIPASE C GAMMA; PHOSPHOPROTEINS; PROTEIN BINDING; RAS PROTEINS; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTES; TRANSCRIPTION, GENETIC;

MUS;

EID: 77958071242     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E10-02-0123     Document Type: Article

References (71)

1. Abe, M., and Naski, M. C. (2004). Regulation of sprouty expression by PLCγ and calcium-dependent signals. Biochem. Biophys. Res. Commun. 323, 1040-1047.
2. Ayada, T., Taniguchi, K., Okamoto, F., Kato, R., Komune, S., Takaesu, G., and Yoshimura, A. (2009). Sprouty4 negatively regulates protein kinase C activation by inhibiting phosphatidylinositol 4,5-biphosphate hydrolysis. Oncogene 28, 1076-1088.
3. Barker, S. A., Caldwell, K. K., Pfeiffer, J. R., and Wilson, B. S. (1998). Wortmannin-sensitive phosphorylation, translocation, and activation of PLCgamma1, but not PLCgamma2, in antigen-stimulated RBL-2H3 mast cells. Mol. Biol. Cell 9, 483-496.
4. Basson, M. A., et al. (2005). Sprouty1 is a critical regulator of GDNF/RETmediated kidney induction. Dev. Cell 8, 229-239.
5. Basson, M. A., Watson-Johnson, J., Shakya, R., Akbulut, S., Hyink, D., Costantini, F. D., Wilson, P. D., Mason, I. J., and Licht, J. D. (2006). Branching morphogenesis of the ureteric epithelium during kidney development is coordinated by the opposing functions of GDNF and Sprouty1. Dev. Biol. 299, 466-477.
6. Bivona, T. G., Perez De Castro, I., Ahearn, I. M., Grana, T. M., Chiu, V. K., Lockyer, P. J., Cullen, P. J., Pellicer, A., Cox, A. D., and Philips, M. R. (2003). Phospholipase Cgamma activates Ras on the Golgi apparatus by means of RasGRP1. Nature 424, 694-698.
7. Cabrita, M. A., and Christofori, G. (2008). Sprouty proteins, masterminds of receptor tyrosine kinase signaling. Angiogenesis 11, 53-62.
8. Carpenter, G., and Ji, Q. (1999). Phospholipase C-gamma as a signal-transducing element. Exp. Cell Res. 253, 15-24.
9. Casci, T., Vinos, J., and Freeman, M. (1999). Sprouty, an intracellular inhibitor of Ras signaling. Cell 96, 655-665.
10. Choi, H., Cho, S. Y., Schwartz, R. H., and Choi, K. (2006). Dual effects of Sprouty1 on TCR signaling depending on the differentiation state of the T cell. J. Immunol. 176, 6034-6045.
11. Crabtree, G. R., and Olson, E. N. (2002). NFAT signaling: choreographing the social lives of cells. Cell 109 (suppl), S67-S79.
12. Dumont, F. J., Staruch, M. J., Fischer, P., DaSilva, C., and Camacho, R. (1998). Inhibition of T cell activation by pharmacologic disruption of the MEK1/ERK MAP kinase or calcineurin signaling pathways results in differential modulation of cytokine production. J. Immunol. 160, 2579-2589.
13. Edwin, F., Anderson, K., Ying, C., and Patel, T. B. (2009). Intermolecular interactions of Sprouty proteins and their implications in development and disease. Mol. Pharmacol. 76, 679-691.
14. Fantl, W. J., Johnson, D. E., and Williams, L. T. (1993). Signalling by receptor tyrosine kinases. Annu. Rev. Biochem. 62, 453-481.
15. Feske, S., Giltnane, J., Dolmetsch, R., Staudt, L. M., and Rao, A. (2001). Gene regulation mediated by calcium signals in T lymphocytes. Nat. Immunol. 2, 316-324.
16. Fong, C. W., Leong, H. F., Wong, E. S., Lim, J., Yusoff, P., and Guy, G. R. (2003). Tyrosine phosphorylation of Sprouty2 enhances its interaction with c-Cbl and is crucial for its function. J. Biol. Chem. 278, 33456-33464.
17. Foskett, J. K., White, C., Cheung, K. H., and Mak, D. O. (2007). Inositol trisphosphate receptor Ca2+ release channels. Physiol. Rev. 87, 593-658.
18. Griner, E. M., and Kazanietz, M. G. (2007). Protein kinase C and other diacylglycerol effectors in cancer. Nat. Rev. Cancer 7, 281-294.
19. Gross, I., Bassit, B., Benezra, M., and Licht, J. D. (2001). Mammalian sprouty proteins inhibit cell growth and differentiation by preventing ras activation. J. Biol. Chem. 276, 46460-46468.
20. Hacohen, N., Kramer, S., Sutherland, D., Hiromi, Y., and Krasnow, M. A. (1998). Sprouty encodes a novel antagonist of FGF signaling that patterns apical branching of the Drosophila airways. Cell 92, 253-263.
21. Haglund, K., Schmidt, M. H., Wong, E. S., Guy, G. R., and Dikic, I. (2005). Sprouty2 acts at the Cbl/CIN85 interface to inhibit epidermal growth factor receptor downregulation. EMBO Rep. 6, 635-641.
22. Hall, A. B., Jura, N., DaSilva, J., Jang, Y. J., Gong, D., and Bar-Sagi, D. (2003). hSpry2 is targeted to the ubiquitin-dependent proteasome pathway by c-Cbl. Curr. Biol. 13, 308-314.
23. Hanafusa, H., Torii, S., Yasunaga, T., and Nishida, E. (2002). Sprouty1 and Sprouty2 provide a control mechanism for the Ras/MAPK signalling pathway. Nat. Cell Biol. 4, 850-858.
24. Hanafusa, H., Torii, S., Yasunaga, T., Matsumoto, K., and Nishida, E. (2004). Shp2, an SH2-containing protein-tyrosine phosphatase, positively regulates receptor tyrosine kinase signaling by dephosphorylating and inactivating the inhibitor Sprouty. J. Biol. Chem. 279, 22992-22995.
25. Hardingham, G. E., and Bading, H. (1999). Calcium as a versatile second messenger in the control of gene expression. Microsc. Res. Tech. 46, 348-355.
26. Ji, Q. S., Ermini, S., Baulida, J., Sun, F. L., and Carpenter, G. (1998). Epidermal growth factor signaling and mitogenesis in Plcg1 null mouse embryonic fibroblasts. Mol. Biol. Cell 9, 749-757.
27. Klein, O. D., Lyons, D. B., Balooch, G., Marshall, G. W., Basson, M. A., Peterka, M., Boran, T., Peterkova, R., and Martin, G. R. (2008). An FGF signaling loop sustains the generation of differentiated progeny from stem cells in mouse incisors. Development 135, 377-385.
28. Klein, O. D., Minowada, G., Peterkova, R., Kangas, A., Yu, B. D., Lesot, H., Peterka, M., Jernvall, J., and Martin, G. R. (2006). Sprouty genes control diastema tooth development via bidirectional antagonism of epithelial- mesenchymal FGF signaling. Dev. Cell 11, 181-190.
29. Kramer, S., Okabe, M., Hacohen, N., Krasnow, M. A., and Hiromi, Y. (1999). Sprouty: a common antagonist of FGF and EGF signaling pathways in Drosophila. Development 126, 2515-2525.
30. Kurosaki, T., Maeda, A., Ishiai, M., Hashimoto, A., Inabe, K., and Takata, M. (2000). Regulation of the phospholipase C-gamma2 pathway in B cells. Immunol. Rev. 176, 19-29.
31. Lao, D. H., Yusoff, P., Chandramouli, S., Philp, R. J., Fong, C. W., Jackson, R. A., Saw, T. Y., Yu, C. Y., and Guy, G. R. (2007). Direct binding of PP2A to Sprouty2 and phosphorylation changes are a prerequisite for ERK inhibition downstream of fibroblast growth factor receptor stimulation. J. Biol. Chem. 282, 9117-9126.
32. Le Good, J. A., Ziegler, W. H., Parekh, D. B., Alessi, D. R., Cohen, P., and Parker, P. J. (1998). Protein kinase C isotypes controlled by phosphoinositide 3-kinase through the protein kinase PDK1. Science 281, 2042-2045.
33. Ledda, F., and Paratcha, G. (2007). Negative regulation of receptor tyrosine kinase (RTK) signaling: a developing field. Biomark Insights 2, 45-58.
34. Lee, J. S., Lee, J. E., Oh, Y. M., Park, J. B., Choi, H., Choi, C. Y., Kim, I. H., Lee, S. H., and Choi, K. (2009). Recruitment of Sprouty1 to immune synapse regulates T cell receptor signaling. J. Immunol. 183, 7178-7186.
35. Lim, J., Yusoff, P., Wong, E. S., Chandramouli, S., Lao, D. H., Fong, C. W., and Guy, G. R. (2002). The cysteine-rich sprouty translocation domain targets mitogen-activated protein kinase inhibitory proteins to phosphatidylinositol 4,5-bisphosphate in plasma membranes. Mol. Cell. Biol. 22, 7953-7966.
36. Macian, F., Im, S. H., Garcia-Cozar, F. J., and Rao, A. (2004). T-cell anergy. Curr. Opin. Immunol. 16, 209-216.
37. Marais, R., Light, Y., Mason, C., Paterson, H., Olson, M. F., and Marshall, C. J. (1998). Requirement of Ras-GTP-Raf complexes for activation of Raf-1 by protein kinase C. Science 280, 109-112.
38. Mason, J. M., Morrison, D. J., Bassit, B., Dimri, M., Band, H., Licht, J. D., and Gross, I. (2004). Tyrosine phosphorylation of Sprouty proteins regulates their ability to inhibit growth factor signaling: a dual feedback loop. Mol. Biol. Cell 15, 2176-2188.
39. Mason, J. M., Morrison, D. J., Basson, M. A., and Licht, J. D. (2006). Sprouty proteins: multifaceted negative-feedback regulators of receptor tyrosine kinase signaling. Trends Cell Biol. 16, 45-54.
40. Masuda, E. S., Imamura, R., Amasaki, Y., Arai, K., and Arai, N. (1998). Signalling into the T-cell nucleus: NFAT regulation. Cell Signal. 10, 599-611.
41. Middlemas, D. S., Meisenhelder, J., and Hunter, T. (1994). Identification of TrkB autophosphorylation sites and evidence that phospholipase C-gamma 1 is a substrate of the TrkB receptor. J. Biol. Chem. 269, 5458-5466.
42. Minowada, G., Jarvis, L. A., Chi, C. L., Neubuser, A., Sun, X., Hacohen, N., Krasnow, M. A., and Martin, G. R. (1999). Vertebrate Sprouty genes are induced by FGF signaling and can cause chondrodysplasia when overexpressed. Development 126, 4465-4475.
43. Nutt, S. L., Dingwell, K. S., Holt, C. E., and Amaya, E. (2001). Xenopus Sprouty2 inhibits FGF-mediated gastrulation movements but does not affect mesoderm induction and patterning. Genes Dev. 15, 1152-1166.
44. Oancea, E., Teruel, M. N., Quest, A. F., and Meyer, T. (1998). Green fluorescent protein (GFP)-tagged cysteine-rich domains from protein kinase C as fluorescent indicators for diacylglycerol signaling in living cells. J. Cell Biol. 140, 485-498.
45. Oliva, J. L., Griner, E. M., and Kazanietz, M. G. (2005). PKC isozymes and diacylglycerol-regulated proteins as effectors of growth factor receptors. Growth Factors 23, 245-252.
46. Ozaki, K., Kadomoto, R., Asato, K., Tanimura, S., Itoh, N., and Kohno, M. (2001). ERK pathway positively regulates the expression of Sprouty genes. Biochem. Biophys. Res. Commun. 285, 1084-1088.
47. Paris, S., and Pouyssegur, J. (1987). Further evidence for a phospholipase C-coupled G protein in hamster fibroblasts. Induction of inositol phosphate formation by fluoroaluminate and vanadate and inhibition by pertussis toxin. J. Biol. Chem. 262, 1970-1976.
48. Perez de Castro, I., Bivona, T. G., Philips, M. R., and Pellicer, A. (2004). Ras activation in Jurkat T cells following low-grade stimulation of the T-cell receptor is specific to N-Ras and occurs only on the Golgi apparatus. Mol. Cell. Biol. 24, 3485-3496.
49. Peters, K. G., Marie, J., Wilson, E., Ives, H. E., Escobedo, J., Del Rosario, M., Mirda, D., and Williams, L. T. (1992). Point mutation of an FGF receptor abolishes phosphatidylinositol turnover and Ca2+ flux but not mitogenesis. Nature 358, 678-681.
50. Reddi, A. L., Ying, G., Duan, L., Chen, G., Dimri, M., Douillard, P., Druker, B. J., Naramura, M., Band, V., and Band, H. (2007). Binding of Cbl to a phospholipase Cgamma1-docking site on platelet-derived growth factor receptor beta provides a dual mechanism of negative regulation. J. Biol. Chem. 282, 29336-29347.
51. Reich, A., Sapir, A., and Shilo, B. (1999). Sprouty is a general inhibitor of receptor tyrosine kinase signaling. Development 126, 4139-4147.
52. Rhee, S. G. (2001). Regulation of phosphoinositide-specific phospholipase C. Annu. Rev. Biochem. 70, 281-312.
53. Ronnstrand, L., Mori, S., Arridsson, A. K., Eriksson, A., Wernstedt, C., Hellman, U., Claesson-Welsh, L., and Heldin, C. H. (1992). Identification of two C-terminal autophosphorylation sites in the PDGF beta-receptor: involvement in the interaction with phospholipase C-gamma. EMBO J. 11, 3911-3919.
54. Roose, J. P., Mollenauer, M., Gupta, V. A., Stone, J., and Weiss, A. (2005). A diacylglycerol-protein kinase C-RasGRP1 pathway directs Ras activation upon antigen receptor stimulation of T cells. Mol. Cell. Biol. 25, 4426-4441.
55. Rotin, D., Margolis, B., Mohammadi, M., Daly, R. J., Daum, G., Li, N., Fischer, E. H., Burgess, W. H., Ullrich, A., and Schlessinger, J. (1992). SH2 domains prevent tyrosine dephosphorylation of the EGF receptor: identification of Tyr992 as the high-affinity binding site for SH2 domains of phospholipase C gamma. EMBO J. 11, 559-567.
56. Rozen, E. J., Schmidt, H., Dolcet, X., Basson, M. A., Jain, S., and Encinas, M. (2009). Loss of Sprouty1 rescues renal agenesis caused by Ret mutation. J. Am. Soc. Nephrol. 20, 255-259.
57. Rubin, C., Litvak, V., Medvedovsky, H., Zwang, Y., Lev, S., and Yarden, Y. (2003). Sprouty fine-tunes EGF signaling through interlinked positive and negative feedback loops. Curr. Biol. 13, 297-307.
58. Sasaki, A., Taketomi, T., Kato, R., Saeki, K., Nonami, A., Sasaki, M., Kuriyama, M., Saito, N., Shibuya, M., and Yoshimura, A. (2003). Mammalian Sprouty4 suppresses Ras-independent ERK activation by binding to Raf1. Nat. Cell Biol. 5, 427-432.
59. Saunders, B., Lyon, S., Day, M., Riley, B., Chenette, E., Subramaniam, S., and Vadivelu, I. (2008). The Molecule Pages database. Nucleic Acids Res. 36, D700-706.
60. Schlessinger, J. (2000). Cell signaling by receptor tyrosine kinases. Cell 103, 211-225.
61. Schonwasser, D. C., Marais, R. M., Marshall, C. J., and Parker, P. J. (1998). Activation of the mitogen-activated protein kinase/extracellular signal-regulated kinase pathway by conventional, novel, and atypical protein kinase C isotypes. Mol. Cell. Biol. 18, 790-798.
62. Shim, K., Minowada, G., Coling, D. E., and Martin, G. R. (2005). Sprouty2, a mouse deafness gene, regulates cell fate decisions in the auditory sensory epithelium by antagonizing FGF signaling. Dev. Cell 8, 553-564.
63. Sivak, J. M., Petersen, L. F., and Amaya, E. (2005). FGF signal interpretation is directed by Sprouty and Spred proteins during mesoderm formation. Dev. Cell 8, 689-701.
64. Smith, M. R., Liu, Y. L., Kim, H., Rhee, S. G., and Kung, H. F. (1990). Inhibition of serum- and ras-stimulated DNA synthesis by antibodies to phospholipase C. Science 247, 1074-1077.
65. Strathdee, C. A., McLeod, M. R., and Hall, J. R. (1999). Efficient control of tetracycline-responsive gene expression from an autoregulated bi-directional expression vector. Gene 229, 21-29.
66. Tefft, D., Lee, M., Smith, S., Crowe, D. L., Bellusci, S., and Warburton, D. (2002). mSprouty2 inhibits FGF10-activated MAP kinase by differentially binding to upstream target proteins. Am. J. Physiol. Lung Cell Mol. Physiol. 283, L700-L706.
67. Testi, R., D'Ambrosio, D., De Maria, R., and Santoni, A. (1994). The CD69 receptor: a multipurpose cell-surface trigger for hematopoietic cells. Immunol. Today 15, 479-483.
68. Wang, D., et al. (2000). Phospholipase Cgamma2 is essential in the functions of B cell and several Fc receptors. Immunity 13, 25-35.
69. Wells, A. D., Liu, Q. H., Hondowicz, B., Zhang, J., Turka, L. A., and Freedman, B. D. (2003). Regulation of T cell activation and tolerance by phospholipase C gamma-1-dependent integrin avidity modulation. J. Immunol. 170, 4127-4133.
70. Wilde, J. I., and Watson, S. P. (2001). Regulation of phospholipase C gamma isoforms in haematopoietic cells: why one, not the other? Cell Signal. 13, 691-701.
71. Wong, E. S., Lim, J., Low, B. C., Chen, Q., and Guy, G. R. (2001). Evidence for direct interaction between Sprouty and Cbl. J. Biol. Chem. 276, 5866-5875.