Role played by paxillin and paxillin tyrosine phosphorylation in hepatocyte growth factor/sphingosine-1-phosphate-mediated reactive oxygen species generation, lamellipodia formation, and endothelial barrier function

Pulmonary Circulation

Volumn 5, Issue 4, 2015, Pages 619-630

  Fu, Panfeng ^a   Usatyuk, Peter V ^a   Jacobson, Jeffrey ^b   Cress, Anne E ^c   Garcia, Joe G N ^c   Salgia, Ravi ^d   Natarajan, Viswanathan ^a,b  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b UNIVERSITY OF ILLINOIS   (United States)

^c UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF CHICAGO   (United States)

Author keywords

C Abl; Endothelial barrier; Lamellipodia; Paxillin; Reactive oxygen species; Tyrosine phosphorylation of paxillin

Indexed keywords

EID: 85026339258     PISSN: 20458932     EISSN: 20458940     Source Type: Journal    
DOI: 10.1086/683693     Document Type: Article

References (58)

1. Bates DO. Vascular endothelial growth factors and vascular permeability. Cardiovasc Res 2010;87(2):262-271.
2. Breslin JW, Pappas PJ, Cerveira JJ, Hobson RW 2nd, Duran WN. VEGF increases endothelial permeability by separate signaling pathways involving ERK-1/2 and nitric oxide. Am J Physiol Heart Circ Physiol 2003;284 (1):H92-H100.
3. Gavard J, Gutkind JS. VEGF controls endothelial-cell permeability by promoting the β-arrestin-dependent endocytosis of VE-cadherin. Nat Cell Biol 2006;8(11):1223-1234.
4. Marumo T, Noll T, Schini-Kerth VB, Harley EA, Duhault J, Piper HM, Busse R. Significance of nitric oxide and peroxynitrite in permeability changes of the retinal microvascular endothelial cell monolayer induced by vascular endothelial growth factor. J Vasc Res 1999;36 (6):510-515.
5. Qian Y, Ducatman A, Ward R, Leonard S, Bukowski V, Lan Guo N, Shi X, Vallyathan V, Castranova V. Perfluorooctane sulfonate (PFOS) induces reactive oxygen species (ROS) production in human microvascular endothelial cells: role in endothelial permeability. J Toxicol Environ Health A 2010;73(12):819-836.
6. Garcia JG, Liu F, Verin AD, Birukova A, Dechert MA, Gerthoffer WT, Bamberg JR, English D. Sphingosine 1-phosphate promotes endothelial cell barrier integrity by Edg-dependent cytoskeletal rearrangement. J Clin Invest 2001;108(5):689-701.
7. McVerry BJ, Garcia JG. Endothelial cell barrier regulation by sphingosine 1-phosphate. J Cell Biochem 2004;92(6):1075-1085.
8. Birukova AA, Alekseeva E, Mikaelyan A, Birukov KG. HGF attenuates thrombin-induced endothelial permeability by Tiam1-mediated activation of the Rac pathway and by Tiam1/Rac-dependent inhibition of the Rho pathway. FASEB J 2007;21(11):2776-2786.
9. Gille J, Khalik M, Konig V, Kaufmann R. Hepatocyte growth factor/scatter factor (HGF/SF) induces vascular permeability factor (VPF/VEGF) expression by cultured keratinocytes. J Invest Dermatol 1998;111(6): 1160-1165.
10. Martin TA, Mansel RE, Jiang WG. Antagonistic effect of NK4 on HGF/SF induced changes in the transendothelial resistance (TER) and paracellular permeability of human vascular endothelial cells. J Cell Physiol 2002;192 (3):268-275.
11. Ragette R, Fu C, Bhattacharya J. Barrier effects of hyperosmolar signaling in microvascular endothelium of rat lung. J Clin Invest 1997;100 (3):685-692.
12. Safdar Z, Wang P, Ichimura H, Issekutz AC, Quadri S, Bhattacharya J. Hyperosmolarity enhances the lung capillary barrier. J Clin Invest 2003; 112(10):1541-1549.
13. Usatyuk PV, Natarajan V. Regulation of reactive oxygen species-induced endothelial cell-cell and cell-matrix contacts by focal adhesion kinase and adherens junction proteins. Am J Physiol Lung Cell Mol Physiol 2005;289(6):L999-L1010.
14. Usatyuk PV, Parinandi NL, Natarajan V. Redox regulation of 4-hydroxy-2-nonenal-mediated endothelial barrier dysfunction by focal adhesion, adherens, and tight junction proteins. J Biol Chem 2006;281 (46):35554-35566.
15. Pan Q, Qiu WY, Huo YN, Yao YF, Lou MF. Low levels of hydrogen peroxide stimulate corneal epithelial cell adhesion, migration, and wound healing. Invest Ophthalmol Vis Sci 2011;52(3):1723-1734.
16. Yang S, Yip R, Polena S, Sharma M, Rao S, Griciene P, Gintautas J, Jerome H. Reactive oxygen species increased focal adhesion kinase production in pulmonary microvascular endothelial cells. Proc West Pharmacol Soc 2004;47:54-56.
17. Lee JF, Ozaki H, Zhan X, Wang E, Hla T, Lee MJ. Sphingosine-1-phosphate signaling regulates lamellipodia localization of cortactin complexes in endothelial cells. Histochem Cell Biol 2006;126(3):297-304.
18. Maceyka M, Alvarez SE, Milstien S, Spiegel S. Filamin A links sphingosine kinase 1 and sphingosine-1-phosphate receptor 1 at lamellipodia to orchestrate cell migration. Mol Cell Biol 2008;28(18):5687-5697.
19. Morimura S, Suzuki K, Takahashi K. β PIX and GIT1 regulate HGFinduced lamellipodia formation and WAVE2 transport. Biochem Biophys Res Commun 2009;382(3):614-619.
20. Usatyuk PV, Fu P, Mohan V, Epshtein Y, Jacobson JR, Gomez-Cambronero J, Wary KK, et al. Role of c-Met/phosphatidylinositol 3-kinase (PI3k)/Akt signaling in hepatocyte growth factor (HGF)-mediated lamellipodia formation, reactive oxygen species (ROS) generation, and motility of lung endothelial cells. J Biol Chem 2014;289(19): 13476-13491.
21. Belvitch P, Dudek SM. Role of FAK in S1P-regulated endothelial permeability. Microvasc Res 2011;83(1):22-30.
22. Birukova AA, Cokic I, Moldobaeva N, Birukov KG. Paxillin is involved in the differential regulation of endothelial barrier by HGF and VEGF. Am J Respir Cell Mol Biol 2009;40(1):99-107.
23. Deakin NO, Turner CE. Paxillin comes of age. J Cell Sci 2008;121:2435-2444.
24. Brown MC, Cary LA, Jamieson JS, Cooper JA, Turner CE. Src and FAK kinases cooperate to phosphorylate paxillin kinase linker, stimulate its focal adhesion localization, and regulate cell spreading and protrusiveness. Mol Biol Cell 2005;16(9):4316-4328.
25. Roy S, Ruest PJ, Hanks SK. FAK regulates tyrosine phosphorylation of CAS, paxillin, and PYK2 in cells expressing v-Src, but is not a critical determinant of v-Src transformation. J Cell Biochem 2002;84(2):377-388.
26. Takayama Y, Tanaka S, Nagai K, Okada M. Adenovirus-mediated overexpression of C-terminal Src kinase (Csk) in type I astrocytes interferes with cell spreading and attachment to fibronectin: correlation with tyrosine phosphorylations of paxillin and FAK. J Biol Chem 1999;274(4):2291-2297.
27. Webb DJ, Donais K, Whitmore LA, Thomas SM, Turner CE, Parsons JT, Horwitz AF. FAK-Src signalling through paxillin, ERK and MLCK regulates adhesion disassembly. Nat Cell Biol 2004;6(2):154-161.
28. Iwasaki T, Nakata A, Mukai M, Shinkai K, Yano H, Sabe H, Schaefer E, et al. Involvement of phosphorylation of Tyr-31 and Tyr-118 of paxillin in MM1 cancer cell migration. Int J Cancer 2002;97(3):330-335.
29. Petit V, Boyer B, Lentz D, Turner CE, Thiery JP, Valles AM. Phosphorylation of tyrosine residues 31 and 118 on paxillin regulates cell migration through an association with CRK in NBT-II cells. J Cell Biol 2000;148(5):957-970.
30. Chen GC, Turano B, Ruest PJ, Hagel M, Settleman J, Thomas SM. Regulation of Rho and Rac signaling to the actin cytoskeleton by paxillin during Drosophila development. Mol Cell Biol 2005;25(3):979-987.
31. Wang F, Nobes CD, Hall A, Spiegel S. Sphingosine 1-phosphate stimulates rho-mediated tyrosine phosphorylation of focal adhesion kinase and paxillin in Swiss 3T3 fibroblasts. Biochem J 1997;324:481-488.
32. Chen DL, Wang DS, Wu WJ, Zeng ZL, Luo HY, Qiu MZ, Ren C, et al. Overexpression of paxillin induced by miR-137 suppression promotes tumor progression and metastasis in colorectal cancer. Carcinogenesis 2013;34(4):803-811.
33. Chen DL, Wang ZQ, Ren C, Zeng ZL, Wang DS, Luo HY, Wang F, et al. Abnormal expression of paxillin correlates with tumor progression and poor survival in patients with gastric cancer. J Transl Med 2013; 11:277.
34. German AE, Mammoto T, Jiang E, Ingber DE, Mammoto A. Paxillin controls endothelial cell migration and tumor angiogenesis by altering neuropilin 2 expression. J Cell Sci 2014;127:1672-1683.
35. Salgia R, Li JL, Ewaniuk DS, Wang YB, Sattler M, Chen WC, Richards W, et al. Expression of the focal adhesion protein paxillin in lung cancer and its relation to cell motility. Oncogene 1999;18(1):67-77.
36. Usatyuk PV, Burns M, Mohan V, Pendyala S, He D, Ebenezer DL, Harijith A, et al. Coronin 1B regulates S1P-induced human lung endothelial cell chemotaxis: role of PLD2, protein kinase C and Rac1 signal transduction. PLoS ONE 2013;8(5):e63007.
37. Fu P, Usatyuk PV, Lele A, Harijith A, Gregorio CC, Garcia JG, Salgia R, Natarajan V. c-Abl mediated tyrosine phosphorylation of paxillin regulates LPS-induced endothelial dysfunction and lung injury. Am J Physiol Lung Cell Mol Physiol 2015;308(10):L1025-L1038.
38. Romanova LY, Hashimoto S, Chay KO, Blagosklonny MV, Sabe H, Mushinski JF. Phosphorylation of paxillin tyrosines 31 and 118 controls polarization and motility of lymphoid cells and is PMA-sensitive. J Cell Sci 2004;117:3759-3768.
39. Usatyuk PV, Romer LH, He D, Parinandi NL, Kleinberg ME, Zhan S, Jacobson JR, et al. Regulation of hyperoxia-induced NADPH oxidase activation in human lung endothelial cells by the actin cytoskeleton and cortactin. J Biol Chem 2007;282(32):23284-23295.
40. Frigault MM, Naujokas MA, Park M. Gab2 requires membrane targeting and the Met binding motif to promote lamellipodia, cell scatter, and epithelial morphogenesis downstream from the Met receptor. J Cell Physiol 2008;214(3):694-705.
41. Khurana S, Tomar A, George SP, Wang Y, Siddiqui MR, Guo H, Tigyi G, Mathew S. Autotaxin and lysophosphatidic acid stimulate intestinal cell motility by redistribution of the actin modifying protein villin to the developing lamellipodia. Exp Cell Res 2008;314(3):530-542.
42. Majumder S, Sowden MP, Gerber SA, Thomas T, Christie CK, Mohan A, Yin G, Lord EM, Berk BC, Pang J. G-protein-coupled receptor-2-interacting protein-1 is required for endothelial cell directional migration and tumor angiogenesis via cortactin-dependent lamellipodia formation. Arterioscler Thromb Vasc Biol 2014;34(2):419-426.
43. McDougall AR, Hooper SB, Zahra VA, Cole TJ, Lo CY, Doran T, Wallace MJ. Trop2 regulates motility and lamellipodia formation in cultured fetal lung fibroblasts. Am J Physiol Lung Cell Mol Physiol 2013;305 (7):L508-L521.
44. Yang Y, Lundquist EA. The actin-binding protein UNC-115/abLIM controls formation of lamellipodia and filopodia and neuronal morphogenesis in Caenorhabditis elegans. Mol Cell Biol 2005;25(12):5158-5170.
45. Chen S, Wang R, Li QF, Tang DD. Abl knockout differentially affects p130 Crk-associated substrate, vinculin, and paxillin in blood vessels of mice. Am J Physiol Heart Circ Physiol 2009;297(2):H533-H539.
46. Flinn HM, Ridley AJ. Rho stimulates tyrosine phosphorylation of focal adhesion kinase, p130 and paxillin. J Cell Sci 1996;109:1133-1141.
47. Lamorte L, Rodrigues S, Sangwan V, Turner CE, Park M. Crk associates with a multimolecular Paxillin/GIT2/β-PIX complex and promotes Racdependent relocalization of paxillin to focal contacts. Mol Biol Cell 2003;14(7):2818-2831.
48. Valles AM, Beuvin M, Boyer B. Activation of Rac1 by paxillin-Crk-DOCK180 signaling complex is antagonized by Rap1 in migrating NBT-II cells. J Biol Chem 2004;279(43):44490-44496.
49. Yano H, Uchida H, Iwasaki T, Mukai M, Akedo H, Nakamura K, Hashimoto S, Sabe H. Paxillin α and Crk-associated substrate exert opposing effects on cell migration and contact inhibition of growth through tyrosine phosphorylation. Proc Natl Acad Sci USA 2000;97(16):9076-9081.
50. Ito A, Kataoka TR, Watanabe M, Nishiyama K, Mazaki Y, Sabe H, Kitamura Y, Nojima H. A truncated isoform of the PP2A B56 subunit promotes cell motility through paxillin phosphorylation. EMBO J 2000;19 (4):562-571.
51. Huang Y, Comiskey EO, Dupree RS, Li S, Koleske AJ, Burkhardt JK. The c-Abl tyrosine kinase regulates actin remodeling at the immune synapse. Blood 2008;112(1):111-119.
52. Sossey-Alaoui K, Li X, Cowell JK. c-Abl-mediated phosphorylation of WAVE3 is required for lamellipodia formation and cell migration. J Biol Chem 2007;282(36):26257-26265.
53. Jin H, Wang JY. Abl tyrosine kinase promotes dorsal ruffles but restrains lamellipodia extension during cell spreading on fibronectin. Mol Biol Cell 2007;18(10):4143-4154.
54. Bryce NS, Clark ES, Leysath JL, Currie JD, Webb DJ, Weaver AM. Cortactin promotes cell motility by enhancing lamellipodial persistence. Curr Biol 2005;15(14):1276-1285.
55. Gov NS, Bernheim-Groswasser A. Releasing the brakes while hanging on: cortactin effects on actin-driven motility. Bioarchitecture 2012;2(1):11-14.
56. Siton O, Ideses Y, Albeck S, Unger T, Bershadsky AD, Gov NS, Bernheim-Groswasser A. Cortactin releases the brakes in actin-based motility by enhancing WASP-VCA detachment from Arp2/3 branches. Curr Biol 2011;21(24):2092-2097.
57. Usatyuk PV, He D, Bindokas V, Gorshkova IA, Berdyshev EV, Garcia JG, Natarajan V. Photolysis of caged sphingosine-1-phosphate induces barrier enhancement and intracellular activation of lung endothelial cell signaling pathways. Am J Physiol Lung Cell Mol Physiol 2011;300 (6):L840-L850.
58. de Rooij J. Cadherin adhesion controlled by cortical actin dynamics. Nat Cell Biol 2014;16(6):508-510.