β-arrestin 2-dependent activation of ERK1/2 is required for ADP-induced paxillin phosphorylation at Ser83 and microglia chemotaxis

GLIA

Volumn 60, Issue 9, 2012, Pages 1366-1377

  Lee, Sang Hyun ^a   Hollingsworth, Ryan ^a   Kwon, Hyeok Yil ^b   Lee, Narae ^a   Chung, Chang Y ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Hallym University   (South Korea)

Author keywords

Chemotaxis; ERK1 2; Focal adhesion; Microglia; Paxillin phosphorylation

Indexed keywords

ADENOSINE DIPHOSPHATE; BETA ARRESTIN 2; GREEN FLUORESCENT PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PAXILLIN; SERINE; SHORT HAIRPIN RNA; TYROSINE;

ANIMAL CELL; ARTICLE; CHEMOTAXIS; FOCAL ADHESION; LAMELLIPODIUM; MICROGLIA; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION;

ADENOSINE DIPHOSPHATE; ANIMALS; ARRESTINS; CELL ADHESION; CELL LINE; CHEMOTAXIS; FOCAL ADHESIONS; MAP KINASE SIGNALING SYSTEM; MICE; MICROGLIA; PAXILLIN; PHOSPHORYLATION;

EID: 84864026147     PISSN: 08941491     EISSN: 10981136     Source Type: Journal    
DOI: 10.1002/glia.22355     Document Type: Article

References (49)

1. Badowski C, Pawlak G, Grichine A, Chabadel A, Oddou C, Jurdic P, Pfaff M, Albiges-Rizo C, Block MR. 2008. Paxillin phosphorylation controls invadopodia/podosomes spatiotemporal organization. Mol Biol Cell 19: 633-645.
2. Bear JE, Svitkina TM, Krause M, Schafer DA, Loureiro JJ, Strasser GA, Maly IV, Chaga OY, Cooper JA, Borisy GG, Gertler FB. 2002. Antagonism between Ena/VASP proteins and actin filament capping regulates fibroblast motility. Cell 109: 509-521.
3. Bellis SL, Miller JT, Turner CE. 1995. Characterization of tyrosine phosphorylation of paxillin in vitro by focal adhesion kinase. J Biol Chem 270: 17437-17441.
4. Bos JL. 2005. Linking Rap to cell adhesion. Curr Opin Cell Biol 17: 123-128.
5. Cai X, Li M, Vrana J, Schaller MD. 2006. Glycogen synthase kinase 3- and extracellular signal-regulated kinase-dependent phosphorylation of paxillin regulates cytoskeletal rearrangement. Mol Cell Biol 26: 2857-2868.
6. Choi CK, Zareno J, Digman MA, Gratton E, Horwitz AR. 2011. Cross-correlated fluctuation analysis reveals phosphorylation-regulated Paxillin-FAK complexes in nascent adhesions. Biophys J 100: 583-592.
7. Choi HB, Hong SH, Ryu JK, Kim SU, McLarnon JG. 2003. Differential activation of subtype purinergic receptors modulates Ca(2+) mobilization and COX-2 in human microglia. Glia 43: 95-103.
8. Deakin NO, Turner CE. 2008. Paxillin comes of age. J Cell Sci 121: 2435-2444.
9. DeFea KA, Vaughn ZD, O'Bryan EM, Nishijima D, Dery O, Bunnett NW. 2000. The proliferative and antiapoptotic effects of substance P are facilitated by formation of a beta-arrestin-dependent scaffolding complex. Proc Natl Acad Sci USA 97: 11086-11091.
10. Fong AM, Premont RT, Richardson RM, Yu YR, Lefkowitz RJ, Patel DD. 2002. Defective lymphocyte chemotaxis in beta-arrestin2- and GRK6-deficient mice. Proc Natl Acad Sci USA 99: 7478-7483.
11. Ge L, Ly Y, Hollenberg M, DeFea K. 2003. A beta-arrestin-dependent scaffold is associated with prolonged MAPK activation in pseudopodia during protease-activated receptor-2-induced chemotaxis. J Biol Chem 278: 34418-34426.
12. Gonzalez-Scarano F, Baltuch G. 1999. Microglia as mediators of inflammatory and degenerative diseases. Annu Rev Neurosci 22: 219-240.
13. Hanisch UK. 2002. Microglia as a source and target of cytokines. Glia 40: 140-155.
14. Hickey WF. 2001. Basic principles of immunological surveillance of the normal central nervous system. Glia 36: 118-124.
15. Honda S, Sasaki Y, Ohsawa K, Imai Y, Nakamura Y, Inoue K, Kohsaka S. 2001. Extracellular ATP or ADP induce chemotaxis of cultured microglia through Gi/o-coupled P2Y receptors. J Neurosci 21: 1975-1982.
16. Hu Q, Klippel A, Muslin AJ, Fantl WJ, Williams LT. 1995. Ras-dependent induction of cellular responses by constitutively active phosphatidylinositol-3 kinase. Science 268: 100-102.
17. Huang C, Borchers CH, Schaller MD, Jacobson K. 2004. Phosphorylation of paxillin by p38MAPK is involved in the neurite extension of PC-12 cells. J Cell Biol 164: 593-602.
18. Ilic D, Furuta Y, Kanazawa S, Takeda N, Sobue K, Nakatsuji N, Nomura S, Fujimoto J, Okada M, Yamamoto T. 1995. Reduced cell motility and enhanced focal adhesion contact formation in cells from FAK-deficient mice. Nature 377: 539-544.
19. Inoue K. 2002. Microglial activation by purines and pyrimidines. Glia 40: 156-163.
20. Ishibe S, Joly D, Liu ZX, Cantley LG. 2004. Paxillin serves as an ERK-regulated scaffold for coordinating FAK and Rac activation in epithelial morphogenesis. Mol Cell 16: 257-267.
21. Ishibe S, Joly D, Zhu X, Cantley LG. 2003. Phosphorylation-dependent paxillin-ERK association mediates hepatocyte growth factor-stimulated epithelial morphogenesis. Mol Cell 12: 1275-1285.
22. Klemke RL, Cai S, Giannini AL, Gallagher PJ, de Lanerolle P, Cheresh DA. 1997. Regulation of cell motility by mitogen-activated protein kinase. J Cell Biol 137: 481-492.
23. Kreutzberg GW. 1996. Microglia: A sensor for pathological events in the CNS. Trends Neurosci 19: 312-318.
24. Lee S, Chung CY. 2009. Role of VASP phosphorylation for the regulation of microglia chemotaxis via the regulation of focal adhesion formation/maturation. Mol Cell Neurosci 42: 382-390.
25. Lefkowitz RJ, Shenoy SK. 2005. Transduction of receptor signals by beta-arrestins. Science 308: 512-517.
26. Liu ZX, Yu CF, Nickel C, Thomas S, Cantley LG. 2002. Hepatocyte growth factor induces ERK-dependent paxillin phosphorylation and regulates paxillin-focal adhesion kinase association. J Biol Chem 277: 10452-10458.
27. Mitra SK, Hanson DA, Schlaepfer DD. 2005. Focal adhesion kinase: In command and control of cell motility. Nat Rev Mol Cell Biol 6: 56-68.
28. Monami G, Gonzalez EM, Hellman M, Gomella LG, Baffa R, Iozzo RV, Morrione A. 2006. Proepithelin promotes migration and invasion of 5637 bladder cancer cells through the activation of ERK1/2 and the formation of a paxillin/FAK/ERK complex. Cancer Res 66: 7103-7110.
29. O'Connor KL, Shaw LM, Mercurio AM. 1998. Release of cAMP gating by the alpha6beta4 integrin stimulates lamellae formation and the chemotactic migration of invasive carcinoma cells. J Cell Biol 143: 1749-1760.
30. 12 receptors in ATP-induced microglial chemotaxis. Glia 55: 604-616.
31. 12 receptor-mediated integrin-beta1 activation regulates microglial process extension induced by ATP. Glia 58: 790-801.
32. Schaller MD. 2001. Paxillin: A focal adhesion-associated adaptor protein. Oncogene 20: 6459-6472.
33. Sen A, O'Malley K, Wang Z, Raj GV, Defranco DB, Hammes SR. 2010. Paxillin regulates androgen- and epidermal growth factor-induced MAPK signaling and cell proliferation in prostate cancer cells. J Biol Chem 285: 28787-28795.
34. 12 receptor-mediated potentiation of thrombin-induced thromboxane A2 generation in platelets occurs through regulation of Erk1/2 activation. J Thromb Haemost 4: 638-647.
35. Shenoy SK, Drake MT, Nelson CD, Houtz DA, Xiao K, Madabushi S, Reiter E, Premont RT, Lichtarge O, Lefkowitz RJ. 2006. beta-arrestin-dependent, G protein-independent ERK1/2 activation by the beta2 adrenergic receptor. J Biol Chem 281: 1261-1273.
36. Shenoy SK, Lefkowitz RJ. 2005. Seven-transmembrane receptor signaling through beta-arrestin. Sci STKE 2005: cm10.
37. Shenoy SK, Lefkowitz RJ. 2011. beta-arrestin-mediated receptor trafficking and signal transduction. Trends Pharmacol Sci 32: 521-533.
38. Stence N, Waite M, Dailey ME. 2001. Dynamics of microglial activation: A confocal time-lapse analysis in hippocampal slices. Glia 33: 256-266.
39. Stork PJ. 2003. Does Rap1 deserve a bad Rap? Trends Biochem Sci 28: 267-275.
40. Streit WJ. 2002. Microglia as neuroprotective, immunocompetent cells of the CNS. Glia 40: 133-139.
41. Sun Y, Cheng Z, Ma L, Pei G. 2002. Beta-arrestin2 is critically involved in CXCR4-mediated chemotaxis, and this is mediated by its enhancement of p38 MAPK activation. J Biol Chem 277: 49212-49219.
42. Thomas WE. 1999. Brain macrophages: On the role of pericytes and perivascular cells. Brain Res Brain Res Rev 31: 42-57.
43. Webb DJ, Donais K, Whitmore LA, Thomas SM, Turner CE, Parsons JT, Horwitz AF. 2004. FAK-Src signalling through paxillin, ERK and MLCK regulates adhesion disassembly. Nat Cell Biol 6: 154-161.
44. Webb DJ, Schroeder MJ, Brame CJ, Whitmore L, Shabanowitz J, Hunt DF, Horwitz AR. 2005. Paxillin phosphorylation sites mapped by mass spectrometry. J Cell Sci 118(Pt 21): 4925-4929.
45. Woodrow MA, Woods D, Cherwinski HM, Stokoe D, McMahon M. 2003. Ras-induced serine phosphorylation of the focal adhesion protein paxillin is mediated by the Raf→MEK→ERK pathway. Exp Cell Res 287: 325-338.
46. Zaidel-Bar R, Ballestrem C, Kam Z, Geiger B. 2003. Early molecular events in the assembly of matrix adhesions at the leading edge of migrating cells. J Cell Sci 116(Pt 22): 4605-4613.
47. Zaidel-Bar R, Milo R, Kam Z, Geiger B. 2007. A paxillin tyrosine phosphorylation switch regulates the assembly and form of cell-matrix adhesions. J Cell Sci 120(Pt 1): 137-148.
48. Zhang Z, Baron R, Horne WC. 2000. Integrin engagement, the actin cytoskeleton, and c-Src are required for the calcitonin-induced tyrosine phosphorylation of paxillin and HEF1, but not for calcitonin-induced Erk1/2 phosphorylation. J Biol Chem 275: 37219-37223.
49. Zimerman B, Volberg T, Geiger B. 2004. Early molecular events in the assembly of the focal adhesion-stress fiber complex during fibroblast spreading. Cell Motil Cytoskeleton 58: 143-159.