Sprouty4 negatively regulates protein kinase C activation by inhibiting phosphatidylinositol 4,5-biphosphate hydrolysis

Oncogene

Volumn 28, Issue 8, 2009, Pages 1076-1088

  Ayada, T ^a,b   Taniguchi, K ^a   Okamoto, F ^a   Kato, R ^a   Komune, S ^b   Takaesu, G ^a   Yoshimura, A ^a,c  

^a KYUSHU UNIVERSITY   (Japan)

^b KYUSHU UNIVERSITY   (Japan)

^c KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

ERK; Phosphatidylinositol; Phospholipase C; Ras; VEGF

Indexed keywords

CALCIUM; CYSTEINE; FIBROBLAST GROWTH FACTOR; G PROTEIN COUPLED RECEPTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INOSITOL 1,4,5 TRISPHOSPHATE; LYSOPHOSPHATIDIC ACID; MARCKS PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PHOSPHOLIPASE C BETA; PHOSPHOLIPASE C GAMMA1; PROTEIN KINASE C; PROTEIN KINASE D; SPROUTY PROTEIN; VASCULOTROPIN A;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CALCIUM MOBILIZATION; CARBOXY TERMINAL SEQUENCE; CELL STRAIN HEK293; COMPETITIVE INHIBITION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME MECHANISM; GENE DELETION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; LIPID HYDROLYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM;

ANIMALS; CALCIUM; CELLS, CULTURED; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FIBROBLAST GROWTH FACTORS; FIBROBLASTS; GENES, RAS; HUMANS; HYDROLYSIS; INOSITOL 1,4,5-TRISPHOSPHATE; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LYSOPHOSPHOLIPIDS; MEMBRANE PROTEINS; MICE; MITOGEN-ACTIVATED PROTEIN KINASES; NERVE TISSUE PROTEINS; NF-KAPPA B; PHOSPHATIDYLINOSITOL 4,5-DIPHOSPHATE; PHOSPHATIDYLINOSITOLS; PHOSPHOINOSITIDE PHOSPHOLIPASE C; PHOSPHOLIPASE C BETA; PHOSPHORYLATION; PROTEIN KINASE C; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 61349098467     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2008.464     Document Type: Article

References (45)

1. Abe M, Naski MC. (2004). Regulation of sprouty expression by PLCγ and calcium-dependent signals. Biochem Biophys Res Commun 323: 1040-1047.
2. Angrist M, Bolk S, Halushka M, Lapchak PA, Chakravarti A. (1996). Germline mutations in glial cell line-derived neurotrophic factor (GDNF) and RET in a Hirschsprung disease patient. Nat Genet 14: 341-344.
3. Armesilla AL, Lorenzo E, Gomez del Arco P, Martinez-Martinez S, Alfranca A, Redondo JM. (1999). Vascular endothelial growth factor activates nuclear factor of activated T cells in human endothelial cells: a role for tissue factor gene expression. Mol Cell Biol 19: 2032-2043.
4. Basson MA, Akbulut S, Watson-Johnson J, Simon R, Carroll TJ, Shakya R et al. (2005). Sprouty1 is a critical regulator of GDNF/ RET-mediated kidney induction. Dev Cell 8: 229-239.
5. Basson MA, Watson-Johnson J, Shakya R, Akbulut S, Hyink D, Costantini FD et al. (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. Brems H, Chmara M, Sahbatou M, Denayer E, Taniguchi K, Kato R et al. (2007). Germline loss-of-function mutations in SPRED1 cause a neurofibromatosis 1-like phenotype. Nat Genet 39: 1120-1126.
7. Byers DM, Palmer FB, Spence MW, Cook HW. (1993). Dissociation of phosphorylation and translocation of a myristoylated protein kinase C substrate (MARCKS protein) in C6 glioma and N1E-115 neuroblastoma cells. J Neurochem 60: 1414-1421.
8. Casci T, Vinos J, Freeman M. (1999). Sprouty, an intracellular inhibitor of Ras signaling. Cell 96: 655-665.
9. Fong CW, Chua MS, McKie AB, Ling SH, Mason V, Li R et al. (2006). Sprouty 2, an inhibitor of mitogen-activated protein kinase signaling, is down-regulated in hepatocellular carcinoma. Cancer Res 66: 2048-2058.
10. Fujita T, Nolan GP, Liou HC, Scott ML, Baltimore D. (1993). The candidate proto-oncogene bcl-3 encodes a transcriptional coactivator that activates through NF-κB p50 homodimers. Genes Dev 7: 1354-1363.
11. Fukunaga K, Ishii S, Asano K, Yokomizo T, Shiomi T, Shimizu T et al. (2001). Single nucleotide polymorphism of human platelet-activating factor receptor impairs G-protein activation. J Biol Chem 276: 43025-43030.
12. Gaudreau R, Le Gouill C, Metaoui S, Lemire S, Stankova J, Rola-Pleszczynski M. (1998). Signalling through the leukotriene B4 receptor involves both αi and α16, but not αq or α11 G-protein subunits. Biochem J 335(Part 1): 15-18.
13. Gross I, Bassit B, Benezra M, Licht JD. (2001). Mammalian sprouty proteins inhibit cell growth and differentiation by preventing ras activation. J Biol Chem 276: 46460-46468.
14. Guy GR, Wong ES, Yusoff P, Chandramouli S, Lo TL, Lim J et al. (2003). Sprouty: how does the branch manager work? J Cell Sci 116: 3061-3068.
15. Hacohen N, Kramer S, Sutherland D, Hiromi Y, Krasnow MA. (1998). Sprouty encodes a novel antagonist of FGF signaling that patterns apical branching of the Drosophila airways. Cell 92: 253-263.
16. Hanafusa H, Torii S, Yasunaga T, Nishida E. (2002). Sprouty1 and Sprouty2 provide a control mechanism for the Ras/MAPK signalling pathway. Nat Cell Biol 4: 850-858.
17. Hempstead BL. (2004). Sculpting organ innervation. J Clin Invest 113: 811-813.
18. Impagnatiello MA, Weitzer S, Gannon G, Compagni A, Cotten M, Christofori G. (2001). Mammalian sprouty-1 and -2 are membrane-anchored phosphoprotein inhibitors of growth factor signaling in endothelial cells. J Cell Biol 152: 1087-1098.
19. Kato R, Nonami A, Taketomi T, Wakioka T, Kuroiwa A, Matsuda Y et al. (2003). Molecular cloning of mammalian Spred-3 which suppresses tyrosine kinase-mediated Erk activation. Biochem Biophys Res Commun 302: 767-772.
20. Kelley GG, Kaproth-Joslin KA, Reks SE, Smrcka AV, Wojcikiewicz RJ. (2006). G-protein-coupled receptor agonists activate endogenous phospholipase Cepsilon and phospholipase Cβ3 in a temporally distinct manner. J Biol Chem 281: 2639-2648.
21. Kramer S, Okabe M, Hacohen N, Krasnow MA, Hiromi Y. (1999). Sprouty: a common antagonist of FGF and EGF signaling pathways in Drosophila. Development 126: 2515-2525.
22. Kuriyama M, Taniguchi T, Shirai Y, Sasaki A, Yoshimura A, Saito N. (2004). Activation and translocation of PKCδ is necessary for VEGF-induced ERK activation through KDR in HEK293T cells. Biochem Biophys Res Commun 325: 843-851.
23. Lee SH, Schloss DJ, Jarvis L, Krasnow MA, Swain JL. (2001). Inhibition of angiogenesis by a mouse sprouty protein. J Biol Chem 276: 4128-4133.
24. Lemmon MA, Ferguson KM, O'Brien R, Sigler PB, Schlessinger J. (1995). Specific and high-affinity binding of inositol phosphates to an isolated pleckstrin homology domain. Proc Natl Acad Sci USA 92: 10472-10476.
25. Lim J, Yusoff P, Wong ES, Chandramouli S, Lao DH, Fong CW et al. (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.
26. Lo TL, Fong CW, Yusoff P, McKie AB, Chua MS, Leung HY et al. (2006). Sprouty and cancer: the first terms report. Cancer Lett 242: 141-150.
27. Maeng YS, Min JK, Kim JH, Yamagishi A, Mochizuki N, Kwon JY et al. (2006). ERK is an anti-inflammatory signal that suppresses expression of NF-κB-dependent inflammatory genes by inhibiting IKK activity in endothelial cells. Cell Signal 18: 994-1005.
28. Minowada G, Jarvis LA, Chi CL, Neubuser A, Sun X, Hacohen N et al. (1999). Vertebrate Sprouty genes are induced by FGF signaling and can cause chondrodysplasia when overexpressed. Development 126: 4465-4475.
29. Ohmori S, Sakai N, Shirai Y, Yamamoto H, Miyamoto E, Shimizu N et al. (2000). Importance of protein kinase C targeting for the phosphorylation of its substrate, myristoylated alanine-rich C-kinase substrate. J Biol Chem 275: 26449-26457.
30. Ozdener F, Dangelmaier C, Ashby B, Kunapuli SP, Daniel JL. (2002). Activation of phospholipase Cγ2 by tyrosine phosphorylation. Mol Pharmacol 62: 672-679.
31. Qin L, Zeng H, Zhao D. (2006). Requirement of protein kinase D tyrosine phosphorylation for VEGF-A165-induced angiogenesis through its interaction and regulation of phospholipase Cγ phosphorylation. J Biol Chem 281: 32550-32558.
32. Reich A, Sapir A, Shilo B. (1999). Sprouty is a general inhibitor of receptor tyrosine kinase signaling. Development 126: 4139-4147.
33. Sasaki A, Taketomi T, Kato R, Saeki K, Nonami A, Sasaki M et al. (2003). Mammalian Sprouty4 suppresses Ras-independent ERK activation by binding to Raf1. Nat Cell Biol 5: 427-432.
34. Sasaki A, Taketomi T, Wakioka T, Kato R, Yoshimura A. (2001). Identification of a dominant negative mutant of Sprouty that potentiates fibroblast growth factor but not epidermal growth factor-induced ERK activation. J Biol Chem 276: 36804-36808.
35. Sivak JM, Petersen LF, Amaya E. (2005). FGF signal interpretation is directed by Sprouty and Spred proteins during mesoderm formation. Dev Cell 8: 689-701.
36. Stauffer TP, Ahn S, Meyer T. (1998). Receptor-induced transient reduction in plasma membrane PtdIns(4,5)P2 concentration monitored in living cells. Curr Biol 8: 343-346.
37. Swierczynski SL, Blackshear PJ. (1995). Membrane association of the myristoylated alanine-rich C kinase substrate (MARCKS) protein. Mutational analysis provides evidence for complex interactions. J Biol Chem 270: 13436-13445.
38. Taketomi T, Yoshiga D, Taniguchi K, Kobayashi T, Nonami A, Kato R et al. (2005). Loss of mammalian Sprouty2 leads to enteric neuronal hyperplasia and esophageal achalasia. Nat Neurosci 8: 855-857.
39. Taniguchi K, Kohno R, Ayada T, Kato R, Ichiyama K, Morisada T et al. (2007). Spreds are essential for embryonic lymphangiogenesis by regulating vascular endothelial growth factor receptor 3 signaling. Mol Cell Biol 27: 4541-4550.
40. Tefft JD, Lee M, Smith S, Leinwand M, Zhao J, Bringas Jr P et al. (1999). Conserved function of mSpry-2, a murine homolog of Drosophila sprouty, which negatively modulates respiratory organogenesis. Curr Biol 9: 219-222.
41. Wang Y, Janicki P, Koster I, Berger CD, Wenzl C, Grosshans J et al. (2008). Xenopus paraxial protocadherin regulates morphogenesis by antagonizing Sprouty. Genes Dev 22: 878-883.
42. Wong C, Jin ZG. (2005). Protein kinase C-dependent protein kinase D activation modulates ERK signal pathway and endothelial cell proliferation by vascular endothelial growth factor. J Biol Chem 280: 33262-33269.
43. Yao YG, Duh EJ. (2004). VEGF selectively induces Down syndrome critical region 1 gene expression in endothelial cells: a mechanism for feedback regulation of angiogenesis? Biochem Biophys Res Commun 321: 648-656.
44. Yigzaw Y, Cartin L, Pierre S, Scholich K, Patel TB. (2001). The C terminus of sprouty is important for modulation of cellular migration and proliferation. J Biol Chem 276: 22742-22747.
45. Yusoff P, Lao DH, Ong SH, Wong ES, Lim J, Lo TL et al. (2002). Sprouty2 inhibits the Ras/MAP kinase pathway by inhibiting the activation of Raf. J Biol Chem 277: 3195-3201.