PLEKHG2 Promotes Heterotrimeric G Protein βγ-Stimulated Lymphocyte Migration via Rac and Cdc42 Activation and Actin Polymerization

Molecular and Cellular Biology

Volumn 33, Issue 21, 2013, Pages 4294-4307

  Runne, Caitlin ^a   Chen, Songhai ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; CELL PROTEIN PLEKHG2; GUANINE NUCLEOTIDE BINDING PROTEIN BETA SUBUNIT; GUANINE NUCLEOTIDE BINDING PROTEIN GAMMA SUBUNIT; PROTEIN CDC42; RAC PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; SMALL INTERFERING RNA; UNCLASSIFIED DRUG;

ACTIN POLYMERIZATION; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL CULTURE; CONTROLLED STUDY; DOWN REGULATION; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; LYMPHOCYTE MEMBRANE; LYMPHOCYTE MIGRATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEQUENCE HOMOLOGY; T LYMPHOCYTE; UPREGULATION;

ACTINS; AMINO ACID SUBSTITUTION; BINDING SITES; CDC42 GTP-BINDING PROTEIN; CHEMOKINE CXCL12; CHEMOTAXIS, LEUKOCYTE; ENZYME ACTIVATION; GTP-BINDING PROTEIN BETA SUBUNITS; GTP-BINDING PROTEIN GAMMA SUBUNITS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HEK293 CELLS; HL-60 CELLS; HUMANS; JURKAT CELLS; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN MULTIMERIZATION; RAC GTP-BINDING PROTEINS;

EID: 84886886499     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00879-13     Document Type: Article

References (47)

1. Sit ST, Manser E. 2011. Rho GTPases and their role in organizing the actin cytoskeleton. J. Cell Sci. 124:679-683.
2. Rossman KL, Der CJ, Sondek J. 2005. GEF means go: turning on RHO GTPases with guanine nucleotide-exchange factors. Nat. Rev. Mol. Cell Biol. 6:167-180.
3. Heasman SJ, Ridley AJ. 2008. Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat. Rev. Mol. Cell Biol. 9:690-701.
4. Mulloy JC, Cancelas JA, Filippi MD, Kalfa TA, Guo F, Zheng Y. 2010. Rho GTPases in hematopoiesis and hemopathies. Blood 115:936-947.
5. Zheng Y. 2001. Dbl family guanine nucleotide exchange factors. Trends Biochem. Sci. 26:724-732.
6. Aittaleb M, Boguth CA, Tesmer JJ. 2010. Structure and function of heterotrimericGprotein-regulated Rho guanine nucleotide exchange factors. Mol. Pharmacol. 77:111-125.
7. Himmel KL, Bi F, Shen H, Jenkins NA, Copeland NG, Zheng Y, Largaespada DA. 2002. Activation of clg, a novel dbl family guanine nucleotide exchange factor gene, by proviral insertion at evi24, a common integration site in B cell and myeloid leukemias. J. Biol. Chem. 277:13463-13472.
8. Ueda H, Nagae R, Kozawa M, Morishita R, Kimura S, Nagase T, Ohara O, Yoshida S, Asano T. 2008. Heterotrimeric G protein betagamma subunits stimulate FLJ00018, a guanine nucleotide exchange factor for Rac1 and Cdc42. J. Biol. Chem. 283:1946-1953.
9. Rickert P, Weiner OD, Wang F, Bourne HR, Servant G. 2000. Leukocytes navigate by compass: roles of PI3Kgamma and its lipid products. Trends Cell Biol. 10:466-473.
10. Runne C, Chen S. 2013. WD40-repeat proteins control the flow of Gbetagamma signaling for directional cell migration. Cell Adh. Migr. 7:214-218.
11. Arai H, Tsou CL, Charo IF. 1997. Chemotaxis in a lymphocyte cell line transfected with C-C chemokine receptor 2B: evidence that directed migration is mediated by betagamma dimers released by activation of Galphai-coupled receptors. Proc. Natl. Acad. Sci. U. S. A. 94:14495-14499.
12. Neptune ER, Bourne HR. 1997. Receptors induce chemotaxis by releasing the betagamma subunit of Gi, not by activating Gq or Gs. Proc. Natl. Acad. Sci. U. S. A. 94:14489-14494.
13. Dong X, Mo Z, Bokoch G, Guo C, Li Z, Wu D. 2005. P-Rex1 is a primary Rac2 guanine nucleotide exchange factor in mouse neutrophils. Curr. Biol. 15:1874-1879.
14. Fukui Y, Hashimoto O, Sanui T, Oono T, Koga H, Abe M, Inayoshi A, Noda M, Oike M, Shirai T, Sasazuki T. 2001. Haematopoietic cellspecific CDM family protein DOCK2 is essential for lymphocyte migration. Nature 412:826-831.
15. Li Z, Hannigan M, Mo Z, Liu B, Lu W, Wu Y, Smrcka AV, Wu G, Li L, Liu M, Huang CK, Wu D. 2003. Directional sensing requires G beta gamma-mediated PAK1 and PIX alpha-dependent activation of Cdc42. Cell 114:215-227.
16. Nishikimi A, Fukuhara H, Su W, Hongu T, Takasuga S, Mihara H, Cao Q, Sanematsu F, Kanai M, Hasegawa H, Tanaka Y, Shibasaki M, Kanaho Y, Sasaki T, Frohman MA, Fukui Y. 2009. Sequential regulation ofDOCK2dynamics by two phospholipids during neutrophil chemotaxis. Science 324:384-387.
17. Wang Z, Kumamoto Y, Wang P, Gan X, Lehmann D, Smrcka AV, Cohn L, Iwasaki A, Li L, Wu D. 2009. Regulation of immature dendritic cell migration by RhoA guanine nucleotide exchange factor Arhgef5. J. Biol. Chem. 284:28599-28606.
18. Welch HC, Condliffe AM, Milne LJ, Ferguson GJ, Hill K, Webb LM, Okkenhaug K, Coadwell WJ, Andrews SR, Thelen M, Jones GE, Hawkins PT, Stephens LR. 2005. P-Rex1 regulates neutrophil function. Curr. Biol. 15:1867-1873.
19. Chen S, Lin F, Shin ME, Wang F, Shen L, Hamm HE. 2008. RACK1 regulates directional cell migration by acting on G betagamma at the interface with its effectors PLC beta and PI3K gamma. Mol. Biol. Cell 19: 3909-3922.
20. Sun Z, Tang X, Lin F, Chen S. 2011. The WD40 repeat protein WDR26 binds Gbetagamma and promotes Gbetagamma-dependent signal transduction and leukocyte migration. J. Biol. Chem. 286:43902-43912.
21. Sun Z, Runne C, Tang X, Lin F, Chen S. 2012. The Gbeta3 splice variant associated with the C825T gene polymorphism is an unstable and functionally inactive protein. Cell Signal. 24:2349-2359.
22. Benard V, Bokoch GM. 2002. Assay of Cdc42, Rac, and Rho GTPase activation by affinity methods. Methods Enzymol. 345:349-359.
23. Condeelis J, Hall AL. 1991. Measurement of actin polymerization and cross-linking in agonist-stimulated cells. Methods Enzymol. 196:486-496.
24. Hampf M, Gossen M. 2006. A protocol for combined Photinus and Renilla luciferase quantification compatible with protein assays. Anal. Biochem. 356:94-99.
25. Sotsios Y, Whittaker GC, Westwick J, Ward SG. 1999. The CXC chemokine stromal cell-derived factor activates a Gi-coupled phosphoinositide 3-kinase in T lymphocytes. J. Immunol. 163:5954-5963.
26. Nishita M, Aizawa H, Mizuno K. 2002. Stromal cell-derived factor 1alpha activates LIM kinase 1 and induces cofilin phosphorylation for T-cell chemotaxis. Mol. Cell. Biol. 22:774-783.
27. Riedl J, Crevenna AH, Kessenbrock K, Yu JH, Neukirchen D, Bista M, Bradke F, Jenne D, Holak TA, Werb Z, Sixt M, Wedlich-Soldner R.2008. Lifeact: a versatile marker to visualize F-actin. Nat. Methods 5:605-607.
28. Thompson G, Owen D, Chalk PA, Lowe PN. 1998. Delineation of the Cdc42/Rac-binding domain of p21-activated kinase. Biochemistry 37: 7885-7891.
29. Srinivasan S, Wang F, Glavas S, Ott A, Hofmann F, Aktories K, Kalman D, Bourne HR. 2003. Rac and Cdc42 play distinct roles in regulating PI(3,4,5)P3 and polarity during neutrophil chemotaxis. J. Cell Biol. 160: 375-385.
30. Strack S, Wilson TJ, Cribbs JT. 2013. Cyclin-dependent kinases regulate splice-specific targeting of dynamin-related protein 1 to microtubules. J. Cell Biol. 201:1037-1051.
31. Hill CS, Wynne J, Treisman R. 1995. The Rho family GTPases RhoA, Rac1, and CDC42Hs regulate transcriptional activation by SRF. Cell 81: 1159-1170.
32. Nobes CD, Hall A. 1995. Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81:53-62.
33. Katz E, Sims AH, Sproul D, Caldwell H, Dixon MJ, Meehan RR, Harrison DJ. 2012. Targeting of Rac GTPases blocks the spread of intact human breast cancer. Oncotarget 3:608-619.
34. Chen HY, Yang YM, Stevens BM, Noble M. 2013. Inhibition of redox/Fyn/c-Cbl pathway function by Cdc42 controls tumour initiation capacity and tamoxifen sensitivity in basal-like breast cancer cells. EMBO Mol. Med. 5:723-736.
35. Shutes A, Onesto C, Picard V, Leblond B, Schweighoffer F, Der CJ. 2007. Specificity and mechanism of action of EHT 1864, a novel small molecule inhibitor of Rac family small GTPases. J. Biol. Chem. 282: 35666-35678.
36. Smrcka AV. 2008. G protein betagamma subunits: central mediators of G protein-coupled receptor signaling. Cell. Mol. Life Sci. 65:2191-2214.
37. Davis TL, Bonacci TM, Sprang SR, Smrcka AV. 2005. Structural and molecular characterization of a preferred protein interaction surface on G protein beta gamma subunits. Biochemistry 44:10593-10604.
38. Ford CE, Skiba NP, Bae H, Daaka Y, Reuveny E, Shekter LR, Rosal R, Weng G, Yang CS, Iyengar R, Miller RJ, Jan LY, Lefkowitz RJ, Hamm HE. 1998. Molecular basis for interactions of G protein betagamma subunits with effectors. Science 280:1271-1274.
39. Yoshikawa DM, Bresciano K, Hatwar M, Smrcka AV. 2001. Characterization of a phospholipase C beta 2-binding site near the amino-terminal coiled-coil of G protein beta gamma subunits. J. Biol. Chem. 276:11246-11251.
40. Scott JK, Huang SF, Gangadhar BP, Samoriski GM, Clapp P, Gross RA, Taussig R, Smrcka AV. 2001. Evidence that a protein-protein interaction 'hot spot' on heterotrimeric G protein betagamma subunits is used for recognition of a subclass of effectors. EMBO J. 20:767-776.
41. Sato K, Handa H, Kimura M, Okano Y, Nagaoka H, Nagase T, Sugiyama T, Kitade Y, Ueda H. 2013. Identification of a Rho family specific guanine nucleotide exchange factor, FLJ00018, as a novel actinbinding protein. Cell Signal. 25:41-49.
42. Welch HC, Coadwell WJ, Ellson CD, Ferguson GJ, Andrews SR, Erdjument-Bromage H, Tempst P, Hawkins PT, Stephens LR. 2002. PRex1, a PtdIns(3,4,5)P3-and Gbetagamma-regulated guanine-nucleotide exchange factor for Rac. Cell 108:809-821.
43. Hill K, Krugmann S, Andrews SR, Coadwell WJ, Finan P, Welch HC, Hawkins PT, Stephens LR. 2005. Regulation of P-Rex1 by phosphatidylinositol (3,4,5)-trisphosphate and Gbetagamma subunits. J. Biol. Chem. 280:4166-4173.
44. Barber MA, Donald S, Thelen S, Anderson KE, Thelen M, Welch HC. 2007. Membrane translocation of P-Rex1 is mediated by G protein betagamma subunits and phosphoinositide 3-kinase. J. Biol. Chem. 282: 29967-29976.
45. Yohe ME, Rossman K, Sondek J. 2008. Role of the C-terminal SH3 domain and N-terminal tyrosine phosphorylation in regulation of Tim and related Dbl-family proteins. Biochemistry 47:6827-6839.
46. Yohe ME, Rossman KL, Gardner OS, Karnoub AE, Snyder JT, Gershburg S, Graves LM, Der CJ, Sondek J. 2007. Auto-inhibition of the Dbl family protein Tim by an N-terminal helical motif. J. Biol. Chem. 282: 13813-13823.
47. Sondek J, Bohm A, Lambright DG, Hamm HE, Sigler PB. 1996. Crystal structure of a G-protein beta gamma dimer at 2.1A resolution. Nature 379:369-374.