The guanine-nucleotide-exchange factor P-Rex1 is activated by protein phosphatase 1α

Biochemical Journal

Volumn 443, Issue 1, 2012, Pages 173-183

  Barber, Mark A ^a   Hendrickx, Annick ^b   Beullens, Monique ^b   Ceulemans, Hugo ^b   Oxley, David ^a   Thelen, Sylvia ^c   Thelen, Marcus ^c   Bollen, Mathieu ^b   Welch, Heidi C E ^a  

^a BABRAHAM INSTITUTE   (United Kingdom)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Switzerland)

Author keywords

Dephosphorylation; Guanine nucleotide exchange factor (GEF) P Rex1; Mechanism of regulation; P Rex family; Serine threonine protein phosphatase PP1; Small G protein (GTPase) Rac

Indexed keywords

ALANINE; GUANINE NUCLEOTIDE EXCHANGE FACTOR; LYSOPHOSPHATIDIC ACID; PHOSPHOPROTEIN PHOSPHATASE; PHOSPHOPROTEIN PHOSPHATASE 1ALPHA; PLATELET DERIVED GROWTH FACTOR; PROTEIN P REX1; RAC PROTEIN; SERINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING KINETICS; CELL STRUCTURE; CONTROLLED STUDY; DEPHOSPHORYLATION; ENDOTHELIUM CELL; ENZYME ACTIVITY; EXPRESSION VECTOR; HUMAN; HUMAN CELL; IN VITRO STUDY; MOLECULAR DOCKING; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SITE DIRECTED MUTAGENESIS; TANDEM MASS SPECTROMETRY; WILD TYPE;

AMINO ACID MOTIFS; ANIMALS; AORTA; CELL SHAPE; CELLS, CULTURED; ENDOTHELIAL CELLS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; PHOSPHORYLATION; PLATELET-DERIVED GROWTH FACTOR; PROTEIN BINDING; PROTEIN PHOSPHATASE 1; PROTEIN STRUCTURE, TERTIARY; RABBITS; RAC1 GTP-BINDING PROTEIN; SWINE;

EID: 84858318015     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20112078     Document Type: Article

References (46)

1. Wennerberg, K., Rossman, K. L. and Der, C. J. (2005) The Ras superfamily at a glance. J. Cell Sci. 118, 843-846 (Pubitemid 40484876)
2. Welch, H. C., Coadwell, W. J., Ellson, C. D., Ferguson, G. J., Andrews, S. R., Erdjument-Bromage, H., Tempst, P., Hawkins, P. T. and Stephens, L. R. (2002) P-Rex1, a PtdIns(3,4,5)P 3- and Gβγ-regulated guanine-nucleotide exchange factor for Rac. Cell 108, 809-821 (Pubitemid 34327532)
3. Donald, S., Hill, K., Lecureuil, C., Barnouin, R., Krugmann, S., Coadwell, W. J., Andrews, S. R., Walker, S. A., Hawkins, P. T., Stephens, L. R. and Welch, H. C. (2004) P-Rex2, a new guanine-nucleotide exchange factor for Rac. FEBS Lett. 572, 172-176 (Pubitemid 39092531)
4. Rosenfeldt, H., Vazquez-Prado, J. and Gutkind, J. S. (2004) P-Rex2, a novel PI-3-kinase sensitive Rac exchange factor. FEBS Lett. 572, 167-171 (Pubitemid 39092530)
5. Donald, S., Humby, T., Fyfe, I., Segonds-Pichon, A., Walker, S. A., Andrews, S. R., Coadwell, W. J., Emson, P., Wilkinson, L. S. and Welch, H.C.E. (2008) P-Rex2 regulates Purkinje cell dendrite morphology and motor coordination. Proc. Natl. Acad. Sci. U.S.A. 105, 4483-4488 (Pubitemid 351754406)
6. Yoshizawa, M., Kawauchi, T., Sone, M., Nishimura, Y. V., Terao, M., Chihama, K., Nabeshima, Y. and Hoshino, M. (2005) Involvement of a Rac activator, P-Rex1, in neurotrophin-derived signaling and neuronal migration. J. Neurosci. 25, 4406-4419 (Pubitemid 40628785)
7. Li, Z., Paik, J. H., Wang, Z., Hla, T. and Wu, D. (2005) Role of guanine nucleotide exchange factor P-Rex2b in sphingosine 1-phosphate-induced Rac1 activation and cell migration in endothelial cells. Prostaglandins Other Lipid Mediators 76, 95-104 (Pubitemid 40720406)
8. Dong, X., Mo, Z., Bokoch, G., Guo, C., Li, Z. and Wu, D. (2005) P-Rex1 is a primary Rac2 guanine nucleotide exchange factor in mouse neutrophils. Curr. Biol. 15, 1874-1879 (Pubitemid 41501524)
9. Wang, Z., Dong, X., Li, Z., Smith, J. D. and Wu, D. (2008) Lack of a significant role of P-Rex1, a major regulator of macrophage Rac1 activation and chemotaxis, in atherogenesis. Prostaglandins Other Lipid Mediators 87, 9-13
10. Welch, H. C., Condliffe, A. M., Milne, L. J., Ferguson, G. J., Hill, K., Webb, L. M., Okkenhaug, K., Coadwell, W. J., Andrews, S. R., Thelen, M. et al. (2005) P-Rex1 regulates neutrophil function. Curr. Biol. 15, 1867-1873 (Pubitemid 41501523)
11. Waters, J. E., Astle, M. V., Ooms, L. M., Balamatsias, D., Gurung, R. and Mitchell, C. A. (2008) P-Rex1: a multidomain protein that regulates neurite differentiation. J. Cell Sci. 121, 2892-2903
12. Lawson, C., Donald, S., Anderson, K., Patton, D. and Welch, H. (2011) P-Rex1 and Vav1 cooperate in the regulation of fMLF-dependent neutrophil responses. J. Immunol. 186, 1467-1476
13. Ledezma-Sánchez, B. A., García-Regalado, A., Guzmán-Hernández, M. L. and Vázquez-Prado, J. (2010) Sphingosine-1-phosphate receptor S1P1 is regulated by direct interactions with P-Rex1, a Rac guanine nucleotide exchange factor. Biochem. Biophys. Res. Commun. 391, 1647-1652
14. Carretero-Ortega, J., Walsh, C. T., Hernández-García, R., Reyes-Cruz, G., Brown, J. H. and Vázquez-Prado, J. (2010) Phosphatidylinositol 3,4,5-triphosphate-dependent Rac exchanger 1 (P-Rex-1), a guanine nucleotide exchange factor for Rac, mediates angiogenic responses to stromal cell-derived factor-1/chemokine stromal cell derived factor-1 (SDF-1/CXCL-12) linked to Rac activation, endothelial cell migration, and in vitro angiogenesis. Mol. Pharmacol. 77, 435-442
15. Jackson, C., Welch, H. C. and Bellamy, T. C. (2010) Control of cerebellar long-term potentiation by P-Rex-family guanine-nucleotide exchange factors and phosphoinositide 3-kinase. PLoS ONE 5, e11962
16. Lindsay, C. R., Lawn, S., Campbell, A. D., Faller, W. J., Rambow, F., Mort, R. L., Timpson, P., Li, A., Cammareri, P., Ridgway, R. A. et al. (2011) P-Rex1 is required for efficient melanoblast migration and melanoma metastasis. Nat. Commun. 2, 555
17. Montero, J. C., Seoane, S., Ocana, A. and Pandiella, A. (2010) P-Rex1 participates in Neuregulin-ErbB signal transduction and its expression correlates with patient outcome in breast cancer. Oncogene 30, 1059-1071
18. Qin, J., Xie, Y., Wang, B., Hoshino, M., Wolff, D. W., Zhao, J., Scofield, M. A., Dowd, F. J., Lin, M. F. and Tu, Y. (2009) Upregulation of PIP3-dependent Rac exchanger 1 (P-Rex1) promotes prostate cancer metastasis. Oncogene 28, 1853-1863
19. Sosa, M. S., Lopez-Haber, C., Yang, C., Wang, H., Lemmon, M. A., Busillo, J. M., Luo, J., Benovic, J. L., Klein-Szanto, A., Yagi, H. et al. (2010) Identification of the Rac-GEF P-Rex1 as an essential mediator of ErbB signaling in breast cancer. Mol. Cell 40, 877-892
20. Fine, B., Hodakoski, C., Koujak, S., Su, T., Saal, L. H., Maurer, M., Hopkins, B., Keniry, M., Sulis, M. L., Mense, S. et al. (2009) Activation of the PI3K pathway in cancer through inhibition of PTEN by exchange factor P-Rex2a. Science 325, 1261-1265
21. Hill, K., Krugmann, S., Andrews, S. R., Coadwell, W. J., Finan, P., Welch, H. C., Hawkins, P. T. and Stephens, L. R. (2005) Regulation of P-Rex1 by phosphatidylinositol (3,4,5)-trisphosphate and Gβγ subunits. J. Biol. Chem. 280, 4166-4173 (Pubitemid 40288581)
22. Barber, M. A., Donald, S., Thelen, S., Anderson, K. E., Thelen, M. and Welch, H.C.E. (2007) Membrane translocation of P-Rex1 is mediated by G protein βγ subunits and phosphoinositide 3-kinase. J. Biol. Chem. 282, 29967-29976 (Pubitemid 350035293)
23. Mayeenuddin, L. H., McIntire, W. E. and Garrison, J. C. (2006) Differential sensitivity of P-Rex1 to isoforms of G protein βγ dimers. J. Biol. Chem. 281, 1913-1920 (Pubitemid 43845776)
24. Urano, D., Nakata, A., Mizuno, N., Tago, K. and Itoh, H. (2008) Domain-domain interaction of P-Rex1 is essential for the activation and inhibition by G protein βγ subunits and PKA. Cell. Signaling 20, 1545-1554
25. Mayeenuddin, L. H. and Garrison, J. C. (2006) Phosphorylation of P-Rex1 by the cyclic AMP-dependent protein kinase inhibits the phosphatidylinositiol (3,4,5)-trisphosphate and Gβγ-mediated regulation of its activity. J. Biol. Chem. 281, 1921-1928 (Pubitemid 43845777)
26. Zhao, T., Nalbant, P., Hoshino, M., Dong, X., Wu, D. and Bokoch, G. M. (2007) Signaling requirements for translocation of P-Rex1, a key Rac2 exchange factor involved in chemoattractant-stimulated human neutrophil function. J. Leukocyte Biol. 81, 1127-1136 (Pubitemid 46495662)
27. phox cells. Cell. Signalling 22, 770-782
28. Bollen, M., Peti, W., Ragusa, M. J. and Beullens, M. (2010) The extended PP1 toolkit: designed to create specificity. Trends Biochem. Sci. 35, 450-458
29. Virshup, D. M. and Shenolikar, S. (2009) From promiscuity to precision: protein phosphatases get a makeover. Mol. Cell 33, 537-545
30. Wakula, P., Beullens, M., Ceulemans, H., Stalmans, W. and Bollen, M. (2003) Degeneracy and function of the ubiquitous RVXF motif that mediates binding to protein phosphatase-1. J. Biol. Chem. 278, 18817-18823 (Pubitemid 36799263)
31. Hendrickx, A., Beullens, M., Ceulemans, H., Den Abt, T., Van Eynde, A., Nicolaescu, E., Lesage, B. and Bollen, M. (2009) Docking motif-guided mapping of the interactome of protein phosphatase-1. Chem. Biol. 16, 365-371
32. Roy, J. and Cyert, M. S. (2009) Cracking the phosphatase code: docking interactions determine substrate specificity. Sci. Signaling 2, re9
33. Beullens, M., Vulsteke, V., Van Eynde, A., Jagiello, I., Stalmans, W. and Bollen, M. (2000) The C-terminus of NIPP1 (nuclear inhibitor of protein phosphatase-1) contains a novel binding site for protein phosphatase-1 that is controlled by tyrosine phosphorylation and RNA binding. Biochem. J. 352, 651-658 (Pubitemid 32015019)
34. Hill, K. and Welch, H. C. (2006) Purification of P-Rex1 from neutrophils and nucleotide exchange assay. Methods Enzymol. 406, 26-41 (Pubitemid 43207429)
35. DeGuzman, A. and Lee, E. Y. (1988) Preparation of low-molecular-weight forms of rabbit muscle protein phosphatase. Methods Enzymol. 159, 356-368
36. Welch, H., Eguinoa, A., Stephens, L. R. and Hawkins, P. T. (1998) Protein kinase B and Rac are activated in parallel within a phosphatidylinositide 3OH-kinase-controlled signaling pathway. J. Biol. Chem. 273, 11248-11256 (Pubitemid 28204977)
37. Wakula, P., Beullens, M., van Eynde, A., Ceulemans, H., Stalmans, W. and Bollen, M. (2006) The translation initation factor eIF2β is an interactor of protein phosphatase-1. Biochem. J. 400, 377-383 (Pubitemid 44852050)
38. Sander, E. E., van Delft, S., ten Klooster, J. P., Reid, T., van der Kammen, R. A., Michiels, F. and Collard, J. G. (1998) Matrix-dependent Tiam1/Rac signaling in epithelial cells promotes either cell-cell adhesion or cell migration and is regulated by phosphatidylinositol 3-kinase. J. Cell Biol. 143, 1385-1398 (Pubitemid 28559838)
39. Lesage, B., Beullens, M., Nuytten, M., Van Eynde, A., Keppens, S., Himpens, B. and Bollen, M. (2004) Interactor-mediated nuclear translocation and retention of protein phosphatase-1. J. Biol. Chem. 279, 55978-55984 (Pubitemid 40066605)
40. Dawson, J. and Holmes, C. (1999) Molecular mechanisms underlying inhibition of protein phosphatases my marine toxins. Front. Biosci. 1, 646-658
41. Haystead, T.A.J., Sim, A.T.R., Carling, D., Honnor, R. C., Tsukitani, Y., Cohen, P. and Hardie, D. G. (1989) Effects of the tumour promoter okadaic acid on intracellular protein phosphorylation and metabolism. Nature 337, 78-81 (Pubitemid 19022553)
42. Ceulemans, H. and Bollen, M. (2004) Functional diversity of protein phosphatase-1, a cellular economizer and reset button. Physiol. Rev. 84, 1-39 (Pubitemid 38049874)
43. Hawkins, P. T., Eguinoa, A., Qiu, R.-G., Stokoe, D., Cooke, F. T., Walters, R., Wennström, S., Claesson-Welsh, L., Evans, T., Symons, M. and Stephens, L. (1995) PDGF stimulates an increase in GTP-Rac via activation of phosphoinositide 3-kinase. Curr. Biol. 5, 393-403
44. Imami, K., Sugiyama, N., Kyono, Y., Tomita, M. and Ishihama, Y. (2008) Automated phosphoproteome analysis for cultured cancer cells by two-dimensional nanoLC-MS using a calcined titania/C18 biphasic column. Anal. Sci. 24, 161-166
45. Kuroda, F., Moss, J. and Vaughan, M. (2007) Regulation of brefeldin A-inhibited guanine nucleotide-exchange protein 1 (BIG1) and BIG2 activity via PKA and protein phosphatase 1γ. Proc. Natl. Acad. Sci. U.S.A. 104, 3201-3206 (Pubitemid 46364137)
46. Martín-Encabo, S., Santos, E. and Guerrero, C. (2007) C3G mediated suppression of malignant transformation involves activation of PP2A phosphatases at the subcortical actin cytoskeleton. Exp. Cell Res. 313, 3881-3891 (Pubitemid 47561894)