Redox regulation of cancer cell migration and invasion

Mitochondrion

Volumn 13, Issue 3, 2013, Pages 246-253

  Tochhawng, Lalchhandami ^a   Deng, Shuo ^a   Pervaiz, Shazib ^a,b,c,d   Yap, Celestial T ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^c DUKE NUS MEDICAL SCHOOL   (Singapore)

^d SINGAPORE MIT ALLIANCE   (Singapore)

Author keywords

Cancer; Invasion; Migration; Reactive oxygen species

Indexed keywords

INTEGRIN; MATRIX METALLOPROTEINASE; PROTEIN KINASE C; PROTEIN TYROSINE PHOSPHATASE; REACTIVE OXYGEN METABOLITE; TYROSINE KINASE RECEPTOR; UROKINASE;

ACTIN FILAMENT; CANCER CELL; CANCER GROWTH; CARCINOGENESIS; CELL ADHESION; CELL INTERACTION; CELL MIGRATION; CELLULAR, SUBCELLULAR AND MOLECULAR BIOLOGICAL PHENOMENA AND FUNCTIONS; DEGRADATION KINETICS; EPITHELIAL MESENCHYMAL TRANSITION; EXTRACELLULAR MATRIX; HUMAN; INTRACELLULAR SIGNALING; INVADOPODIA; MALIGNANT NEOPLASTIC DISEASE; MOLECULAR DYNAMICS; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; TUMOR GROWTH; TUMOR INVASION; ANIMAL; CELL MOTION; GENETICS; METABOLISM; METASTASIS; MORTALITY; NEOPLASM;

ANIMALS; CELL MOVEMENT; HUMANS; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; NEOPLASMS; OXIDATION-REDUCTION; REACTIVE OXYGEN SPECIES;

EID: 84883768176     PISSN: 15677249     EISSN: 18728278     Source Type: Journal    
DOI: 10.1016/j.mito.2012.08.002     Document Type: Review

References (134)

1. Abram C.L., Seals D.F., Pass I., Salinsky D., Maurer L., Roth T.M., Courtneidge S.A. The adaptor protein fish associates with members of the ADAMs family and localizes to podosomes of Src-transformed cells. J. Biol. Chem. 2003, 278:16844-16851.
2. Alexandrova A.Y., Kopnin P.B., Vasiliev J.M., Kopnin B.P. ROS up-regulation mediates Ras-induced changes of cell morphology and motility. Exp. Cell Res. 2006, 312:2066-2073.
3. Anastasiadis P.Z., Reynolds A.B. The p120 catenin family: complex roles in adhesion, signaling and cancer. J. Cell Sci. 2000, 113(Pt 8):1319-1334.
4. Barnett P., Arnold R.S., Mezencev R., Chung L.W., Zayzafoon M., Odero-Marah V. Snail-mediated regulation of reactive oxygen species in ARCaP human prostate cancer cells. Biochem. Biophys. Res. Commun. 2011, 404:34-39.
5. Basuroy S., Dunagan M., Sheth P., Seth A., Rao R.K. Hydrogen peroxide activates focal adhesion kinase and c-Src by a phosphatidylinositol 3 kinase-dependent mechanism and promotes cell migration in Caco-2 cell monolayers. Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 299:G186-G195.
6. Baum B., Settleman J., Quinlan M.P. Transitions between epithelial and mesenchymal states in development and disease. Semin. Cell Dev. Biol. 2008, 19:294-308.
7. Ben Mahdi M.H., Andrieu V., Pasquier C. Focal adhesion kinase regulation by oxidative stress in different cell types. IUBMB Life 2000, 50:291-299.
8. 2-production and degranulation. J. Leukoc. Biol. 1991, 49:236-244.
9. Benhar M., Engelberg D., Levitzki A. ROS, stress-activated kinases and stress signaling in cancer. EMBO Rep. 2002, 3:420-425.
10. Binker M., Binker-Cosen A., Richards D., Oliver B., Cosen-Binker L. EGF promotes invasion by PANC-1 cells through Rac1/ROS-dependent secretion and activation of MMP-2. Biochem. Biophys. Res. Commun. 2009, 379:445-450.
11. Boivin B., Yang M., Tonks N.K. Targeting the reversibly oxidized protein tyrosine phosphatase superfamily. Sci. Signal. 2010, 3:l2.
12. Brenneisen P., Sies H., Scharffetter-Kochanek K. Ultraviolet-B irradiation and matrix metalloproteinases: from induction via signaling to initial events. Ann. N. Y. Acad. Sci. 2002, 973:31-43.
13. Brooks S.A., Lomax-Browne H.J., Carter T.M., Kinch C.E., Hall D.M. Molecular interactions in cancer cell metastasis. Acta Histochem. 2010, 112:3-25.
14. Brown D.I., Griendling K.K. Nox proteins in signal transduction. Free Radic. Biol. Med. 2009, 47:1239-1253.
15. Buschman M.D., Bromann P.A., Cejudo-Martin P., Wen F., Pass I., Courtneidge S.A. The novel adaptor protein Tks4 (SH3PXD2B) is required for functional podosome formation. Mol. Biol. Cell 2009, 20:1302-1311.
16. Cadenas E., Davies K.J. Mitochondrial free radical generation, oxidative stress, and aging. Free Radic. Biol. Med. 2000, 29:222-230.
17. Cannito S., Novo E., Compagnone A., Valfrè di Bonzo L., Busletta C., Zamara E., Paternostro C., Povero D., Bandino A., Bozzo F., Cravanzola C., Bravoco V., Colombatto S., Parola M. Redox mechanisms switch on hypoxia-dependent epithelial-mesenchymal transition in cancer cells. Carcinogenesis 2008, 29:2267-2278.
18. Cannito S., Novo E., di Bonzo L.V., Busletta C., Colombatto S., Parola M. Epithelial-mesenchymal transition: from molecular mechanisms, redox regulation to implications in human health and disease. Antioxid. Redox Signal. 2010, 12:1383-1430.
19. Chae H.J., Kim H.R., Kwak Y.G., Ko J.K., Joo C.U., Chae S.W. Signal transduction of nitric oxide donor-induced protection in hydrogen peroxide-mediated apoptosis in H9C2 cardiomyoblasts. Immunopharmacol. Immunotoxicol. 2001, 23:187-204.
20. Chen W.T. Proteolytic activity of specialized surface protrusions formed at rosette contact sites of transformed cells. J. Exp. Zool. 1989, 251:167-185.
21. Chen Z.X., Pervaiz S. Bcl-2 induces pro-oxidant state by engaging mitochondrial respiration in tumor cells. Cell Death Differ. 2007, 14:1617-1627.
22. Chiarugi P., Pani G., Giannoni E., Taddei L., Colavitti R., Raugei G., Symons M., Borrello S., Galeotti T., Ramponi G. Reactive oxygen species as essential mediators of cell adhesion: the oxidative inhibition of a FAK tyrosine phosphatase is required for cell adhesion. J. Cell Biol. 2003, 161:933-944.
23. Chiu C., Maddock D.A., Zhang Q., Souza K.P., Townsend A.R., Wan Y. TGF-beta-induced p38 activation is mediated by Rac1-regulated generation of reactive oxygen species in cultured human keratinocytes. Int. J. Mol. Med. 2001, 8:251-255.
24. Chiu W., Shen S., Chow J., Lin C., Shia L., Chen Y. Contribution of reactive oxygen species to migration/invasion of human glioblastoma cells U87 via ERK-dependent COX-2/PGE(2) activation. Neurobiol. Dis. 2010, 37:118-129.
25. Comito G., Calvani M., Giannoni E., Bianchini F., Calorini L., Torre E., Migliore C., Giordano S., Chiarugi P. HIF-1α stabilization by mitochondrial ROS promotes Met-dependent invasive growth and vasculogenic mimicry in melanoma cells. Free Radic. Biol. Med. 2011, 51:893-904.
26. Curran S., Dundas S.R., Buxton J., Leeman M.F., Ramsay R., Murray G.I. Matrix metalloproteinase/tissue inhibitors of matrix metalloproteinase phenotype identifies poor prognosis colorectal cancers. Clin. Cancer Res. 2004, 10:8229-8234.
27. 2-treated actin: assembly and polymer interactions with cross-linking proteins. Biophys. J. 1995, 69:2710-2719.
28. DalleDonne I., Milzani A., Colombo R. The tert-butyl hydroperoxide-induced oxidation of actin Cys-374 is coupled with structural changes in distant regions of the protein. Biochemistry 1999, 38:12471-12480.
29. D'Autréaux B., Toledano M.B. ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat. Rev. Mol. Cell Biol. 2007, 8:813-824.
30. Day A.M., Veal E.A. Hydrogen peroxide-sensitive cysteines in the Sty1 MAPK regulate the transcriptional response to oxidative stress. J. Biol. Chem. 2010, 285:7505-7516.
31. Del Bufalo D., Biroccio A., Leonetti C., Zupi G. Bcl-2 overexpression enhances the metastatic potential of a human breast cancer line. FASEB J. 1997, 11:947-953.
32. den Hertog J., Ostman A., Böhmer F.D. Protein tyrosine phosphatases: regulatory mechanisms. FEBS J. 2008, 275:831-847.
33. Diaz B., Shani G., Pass I., Anderson D., Quintavalle M., Courtneidge S.A. Tks5-dependent, Nox-mediated generation of reactive oxygen species is necessary for invadopodia formation. Sci. Signal. 2009, 2:53.
34. Disatnik M.H., Rando T.A. Integrin-mediated muscle cell spreading. The role of protein kinase c in outside-in and inside-out signaling and evidence of integrin cross-talk. J. Biol. Chem. 1999, 274:32486-32492.
35. Disatnik M.H., Boutet S.C., Lee C.H., Mochly-Rosen D., Rando T.A. Sequential activation of individual PKC isozymes in integrin-mediated muscle cell spreading: a role for MARCKS in an integrin signaling pathway. J. Cell Sci. 2002, 115:2151-2163.
36. Dong R., Wang Q., He X.L., Chu Y.K., Lu J.G., Ma Q.J. Role of nuclear factor kappa B and reactive oxygen species in the tumor necrosis factor-alpha-induced epithelial-mesenchymal transition of MCF-7 cells. Braz. J. Med. Biol. Res. 2007, 40:1071-1078.
37. Felton V.M., Borok Z., Willis B.C. N-acetylcysteine inhibits alveolar epithelial-mesenchymal transition. Am. J. Physiol. Lung Cell. Mol. Physiol. 2009, 297:L805-L812.
38. Fiaschi T., Cozzi G., Raugei G., Formigli L., Ramponi G., Chiarugi P. Redox regulation of beta-actin during integrin-mediated cell adhesion. J. Biol. Chem. 2006, 281:22983-22991.
39. Friedl P., Gilmour D. Collective cell migration in morphogenesis, regeneration and cancer. Nat. Rev. Mol. Cell Biol. 2009, 10:445-457.
40. Gianni D., Diaz B., Taulet N., Fowler B., Courtneidge S.A., Bokoch G.M. Novel p47(phox)-related organizers regulate localized NADPH oxidase 1 (Nox1) activity. Sci. Signal. 2009, 2:54.
41. Gianni D., Taulet N., DerMardirossian C., Bokoch G.M. c-Src-mediated phosphorylation of NoxA1 and Tks4 induces the reactive oxygen species (ROS)-dependent formation of functional invadopodia in human colon cancer cells. Mol. Biol. Cell 2010, 21:4287-4298.
42. Giannoni E., Parri M., Chiarugi P. EMT and oxidative stress: a bidirectional interplay affecting tumor malignancy. Antioxid. Redox Signal. 2011, 16:1248-1263.
43. Giridharan S.S., Rohn J.L., Naslavsky N., Caplan S. Differential regulation of actin microfilaments by human MICAL proteins. J. Cell Sci. 2012, 125:614-624.
44. Gloire G., Legrand-Poels S., Piette J. NF-kappaB activation by reactive oxygen species: fifteen years later. Biochem. Pharmacol. 2006, 72:1493-1505.
45. 2 redox stress. Am. J. Respir. Cell Mol. Biol. 1998, 19:786-798.
46. Gonzalez-Rubio M., Voit S., Rodriguez-Puyol D., Weber M., Marx M. Oxidative stress induces tyrosine phosphorylation of PDGF alpha- and beta-receptors and pp 60c-src in mesangial cells. Kidney Int. 1996, 50:164-173.
47. Gopalakrishna R., Jaken S. Protein kinase C signaling and oxidative stress. Free Radic. Biol. Med. 2000, 28:1349-1361.
48. Gozin A., Franzini E., Andrieu V., Da Costa L., Rollet-Labelle E., Pasquier C. Reactive oxygen species activate focal adhesion kinase, paxillin and p130cas tyrosine phosphorylation in endothelial cells. Free Radic. Biol. Med. 1998, 25:1021-1032.
49. Granfeldt D., Dahlgren C. An intact cytoskeleton is required for prolonged respiratory burst activity during neutrophil phagocytosis. Inflammation 2001, 25:165-169.
50. Guan J.L. Role of focal adhesion kinase in integrin signaling. Int. J. Biochem. Cell Biol. 1997, 29:1085-1096.
51. 2-induced apoptosis in bovine aortic endothelial cells. Acta Pharmacol. Sin. 2000, 21:41-45.
52. Ho B.Y., Wu Y.M., Chang K.J., Pan T.M. Dimerumic acid inhibits SW620 cell invasion by attenuating HO-mediated MMP-7 expression via JNK/C-Jun and ERK/C-Fos activation in an AP-1-dependent manner. Int. J. Biol. Sci. 2011, 7:869-880.
53. Hu C.T., Wu J.R., Cheng C.C., Wang S., Wang H.T., Lee M.C., Wang L.J., Pan S.M., Chang T.Y., Wu W.S. Reactive oxygen species-mediated PKC and integrin signaling promotes tumor progression of human hepatoma HepG2. Clin. Exp. Metastasis 2011, 28:851-863.
54. Hung R.J., Pak C.W., Terman J.R. Direct redox regulation of F-actin assembly and disassembly by Mical. Science 2011, 334:1710-1713.
55. Hurd T.R., Degennaro M., Lehmann R. Redox regulation of cell migration and adhesion. Trends Cell Biol. 2011, 22:107-115.
56. Inumaru J., Nagano O., Takahashi E., Ishimoto T., Nakamura S., Suzuki Y., Niwa S., Umezawa K., Tanihara H., Saya H. Molecular mechanisms regulating dissociation of cell-cell junction of epithelial cells by oxidative stress. Genes Cells 2009, 14:703-716.
57. Kheradmand F., Werner E., Tremble P., Symons M., Werb Z. Role of Rac1 and oxygen radicals in collagenase-1 expression induced by cell shape change. Science 1998, 280:898-902.
58. Khoi P.N., Park J.S., Kim N.H., Jung Y.D. Nicotine stimulates urokinase-type plasminogen activator receptor expression and cell invasiveness through mitogen-activated protein kinase and reactive oxygen species signaling in ECV304 endothelial cells. Toxicol. Appl. Pharmacol. 2012, 259:248-256.
59. Kim M.H., Yoo H.S., Kim M.Y., Jang H.J., Baek M.K., Kim H.R., Kim K.K., Shin B.A., Ahn B.W., Jung Y.D. Helicobacter pylori stimulates urokinase plasminogen activator receptor expression and cell invasiveness through reactive oxygen species and NF-kappaB signaling in human gastric carcinoma cells. Int. J. Mol. Med. 2007, 19:689-697.
60. Kim J.S., Huang T.Y., Bokoch G.M. Reactive oxygen species regulate a slingshot-cofilin activation pathway. Mol. Biol. Cell 2009, 20:2650-2660.
61. Kim J.S., Bak E.J., Lee B.C., Kim Y.S., Park J.B., Choi I.G. Neuregulin induces HaCaT keratinocyte migration via Rac1-mediated NADPH-oxidase activation. J. Cell. Physiol. 2011, 226:3014-3021.
62. Kozma R., Ahmed S., Best A., Lim L. The Ras-related protein Cdc42Hs and bradykinin promote formation of peripheral actin microspikes and filopodia in Swiss 3T3 fibroblasts. Mol. Cell. Biol. 1995, 15:1942-1952.
63. Lai F.P., Szczodrak M., Block J., Faix J., Breitsprecher D., Mannherz H.G., Stradal T.E., Dunn G.A., Small J.V., Rottner K. Arp2/3 complex interactions and actin network turnover in lamellipodia. EMBO J. 2008, 27:982-992.
64. Lander H.M., Ogiste J.S., Teng K.K., Novogrodsky A. p21ras as a common signaling target of reactive free radicals and cellular redox stress. J. Biol. Chem. 1995, 270:21195-21198.
65. Lander H.M., Hajjar D.P., Hempstead B.L., Mirza U.A., Chait B.T., Campbell S., Quilliam L.A. A molecular redox switch on p21(ras). Structural basis for the nitric oxide-p21(ras) interaction. J. Biol. Chem. 1997, 272:4323-4326.
66. Landriscina M., Maddalena F., Laudiero G., Esposito F. Adaptation to oxidative stress, chemoresistance, and cell survival. Antioxid. Redox Signal. 2009, 11:2701-2716.
67. Lee K.H., Kim S.W., Kim J.R. Reactive oxygen species regulate urokinase plasminogen activator expression and cell invasion via mitogen-activated protein kinase pathways after treatment with hepatocyte growth factor in stomach cancer cells. J. Exp. Clin. Cancer Res. 2009, 28:73.
68. Lee E.K., Jeon W.K., Chae M.Y., Hong H.Y., Lee Y.S., Kim J.H., Kwon J.Y., Kim B.C., Park S.H. Decreased expression of glutaredoxin 1 is required for transforming growth factor-beta1-mediated epithelial-mesenchymal transition of EpRas mammary epithelial cells. Biochem. Biophys. Res. Commun. 2010, 391:1021-1027.
69. Leto T.L., Morand S., Hurt D., Ueyama T. Targeting and regulation of reactive oxygen species generation by Nox family NADPH oxidases. Antioxid. Redox Signal. 2009, 11:2607-2619.
70. Liou G.Y., Storz P. Reactive oxygen species in cancer. Free Radic. Res. 2010, 44:479-496.
71. Low I.C., Chen Z.X., Pervaiz S. Bcl-2 modulates resveratrol-induced ROS production by regulating mitochondrial respiration in tumor cells. Antioxid. Redox Signal. 2010, 13:807-819.
72. Lu T., Gabrilovich D.I. Molecular pathways: tumor infiltrating myeloid cells and reactive oxygen species in regulation of tumor microenvironment. Clin. Cancer Res. 2012, (Electronic publication ahead of print).
73. Lukaszewicz-Zajac M., Mroczko B., Szmitkowski M. Gastric cancer - the role of matrix metalloproteinases in tumor progression. Clin. Chim. Acta 2011, 412:1725-1730.
74. Meyer T., Hart I.R. Mechanisms of tumour metastasis. Eur. J. Cancer 1998, 34:214-221.
75. Moldovan L., Irani K., Moldovan N., Finkel T., Goldschmidt-Clermont P. The actin cytoskeleton reorganization induced by Rac1 requires the production of superoxide. Antioxid. Redox Signal. 1999, 1:29-43.
76. Moldovan L., Mythreye K., Goldschmidt-Clermont P., Satterwhite L. Reactive oxygen species in vascular endothelial cell motility. Roles of NAD(P)H oxidase and Rac1. Cardiovasc. Res. 2006, 71:236-246.
77. Munnamalai V., Suter D. Reactive oxygen species regulate F-actin dynamics in neuronal growth cones and neurite outgrowth. J. Neurochem. 2009, 108:644-661.
78. Mytar B., Siedlar M., Woloszyn M., Ruggiero I., Pryjma J., Zembala M. Induction of reactive oxygen intermediates in human monocytes by tumour cells and their role in spontaneous monocyte cytotoxicity. Br. J. Cancer 1999, 79:737-743.
79. Nelson K.K., Melendez J.A. Mitochondrial redox control of matrix metalloproteinases. Free Radic. Biol. Med. 2004, 37:768-784.
80. Nigam S., Weston C.E., Liu C.H., Simon E.E. The actin cytoskeleton and integrin expression in the recovery of cell adhesion after oxidant stress to a proximal tubule cell line (JTC-12). J. Am. Soc. Nephrol. 1998, 9:1787-1797.
81. Nishikawa M. Reactive oxygen species in tumor metastasis. Cancer Lett. 2008, 266:53-59.
82. Nobes C.D., Hall A. Rho, rac and cdc42 GTPases: regulators of actin structures, cell adhesion and motility. Biochem. Soc. Trans. 1995, 23:456-459.
83. Nobes C.D., Hall A. Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 1995, 81:53-62.
84. Nobes C.D., Hall A. Rho GTPases control polarity, protrusion, and adhesion during cell movement. J. Cell Biol. 1999, 144:1235-1244.
85. Novo E., Parola M. Redox mechanisms in hepatic chronic wound healing and fibrogenesis. Fibrogenesis Tissue Repair 2008, 1:5.
86. Oser M., Yamaguchi H., Mader C.C., Bravo-Cordero J.J., Arias M., Chen X., Desmarais V., van Rheenen J., Koleske A.J., Condeelis J. Cortactin regulates cofilin and N-WASp activities to control the stages of invadopodium assembly and maturation. J. Cell Biol. 2009, 186:571-587.
87. Pelicano H., Carney D., Huang P. ROS stress in cancer cells and therapeutic implications. Drug Resist. Updat. 2004, 7:97-110.
88. Pelicano H., Lu W., Zhou Y., Zhang W., Chen Z., Hu Y., Huang P. Mitochondrial dysfunction and reactive oxygen species imbalance promote breast cancer cell motility through a CXCL14-mediated mechanism. Cancer Res. 2009, 69:2375-2383.
89. Peltoniemi M., Kaarteenaho-Wiik R., Säily M., Sormunen R., Pääkkö P., Holmgren A., Soini Y., Kinnula V.L. Expression of glutaredoxin is highly cell specific in human lung and is decreased by transforming growth factor-beta in vitro and in interstitial lung diseases in vivo. Hum. Pathol. 2004, 35:1000-1007.
90. Pervaiz S. Pro-oxidant milieu blunts scissors: insight into tumor progression, drug resistance, and novel druggable targets. Curr. Pharm. Des. 2006, 12:4469-4477.
91. Pervaiz S., Clement M.V. Tumor intracellular redox status and drug resistance - serendipity or a causal relationship?. Curr. Pharm. Des. 2004, 10:1969-1977.
92. Pervaiz S., Clement M. Superoxide anion: oncogenic reactive oxygen species?. Int. J. Biochem. Cell Biol. 2007, 39:1297-1304.
93. Pinkas J., Martin S.S., Leder P. Bcl-2-mediated cell survival promotes metastasis of EpH4 betaMEKDD mammary epithelial cells. Mol. Cancer Res. 2004, 2:551-556.
94. Price J.T., Thompson E.W. Mechanisms of tumour invasion and metastasis: emerging targets for therapy. Expert Opin. Ther. Targets 2002, 6:217-233.
95. Rajagopalan S., Meng X.P., Ramasamy S., Harrison D.G., Galis Z.S. Reactive oxygen species produced by macrophage-derived foam cells regulate the activity of vascular matrix metalloproteinases in vitro. Implications for atherosclerotic plaque stability. J. Clin. Invest. 1996, 98:2572-2579.
96. Reddy S.P., Mossman B.T. Role and regulation of activator protein-1 in toxicant-induced responses of the lung. Am. J. Physiol. Lung Cell. Mol. Physiol. 2002, 283:L1161-L1178.
97. Reynaert N.L., Wouters E.F., Janssen-Heininger Y.M. Modulation of glutaredoxin-1 expression in a mouse model of allergic airway disease. Am. J. Respir. Cell Mol. Biol. 2007, 36:147-151.
98. Rhyu D.Y., Yang Y., Ha H., Lee G.T., Song J.S., Uh S.T., Lee H.B. Role of reactive oxygen species in TGF-beta1-induced mitogen-activated protein kinase activation and epithelial-mesenchymal transition in renal tubular epithelial cells. J. Am. Soc. Nephrol. 2005, 16:667-675.
99. Ridley A.J. Life at the leading edge. Cell 2011, 145:1012-1022.
100. Ridley A.J., Hall A. The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 1992, 70:389-399.
101. Robinson C.J., Sloss C.M., Plevin R. Inactivation of JNK activity by mitogen-activated protein kinase phosphatase-2 in EAhy926 endothelial cells is dependent upon agonist-specific JNK translocation to the nucleus. Cell. Signal. 2001, 13:29-41.
102. Saari H., Sorsa T., Lindy O., Suomalainen K., Halinen S., Konttinen Y.T. Reactive oxygen species as regulators of human neutrophil and fibroblast interstitial collagenases. Int. J. Tissue React. 1992, 14:113-120.
103. Salmeen A., Barford D. Functions and mechanisms of redox regulation of cysteine-based phosphatases. Antioxid. Redox Signal. 2005, 7:560-577.
104. Selvakumar B., Hess D.T., Goldschmidt-Clermont P.J., Stamler J.S. Co-regulation of constitutive nitric oxide synthases and NADPH oxidase by the small GTPase Rac. FEBS Lett. 2008, 582:2195-2202.
105. Shinohara M., Adachi Y., Mitsushita J., Kuwabara M., Nagasawa A., Harada S., Furuta S., Zhang Y., Seheli K., Miyazaki H., Kamata T. Reactive oxygen generated by NADPH oxidase 1 (Nox1) contributes to cell invasion by regulating matrix metalloprotease-9 production and cell migration. J. Biol. Chem. 2010, 285:4481-4488.
106. Sierra A., Lloveras B., Castellsague X., Moreno L., Garcia-Ramirez M., Fabra A. Bcl-2 expression is associated with lymph node metastasis in human ductal breast carcinoma. Int. J. Cancer 1995, 60:54-60.
107. 2 for platelet-derived growth factor signal transduction. Science 1995, 270:296-299.
108. Suzuki M., Kato M., Hanaka H., Izumi T., Morikawa A. Actin assembly is a crucial factor for superoxide anion generation from adherent human eosinophils. J. Allergy Clin. Immunol. 2003, 112:126-133.
109. Svineng G., Ravuri C., Rikardsen O., Huseby N.E., Winberg J.O. The role of reactive oxygen species in integrin and matrix metalloproteinase expression and function. Connect. Tissue Res. 2008, 49:197-202.
110. Taddei M.L., Parri M., Mello T., Catalano A., Levine A.D., Raugei G., Ramponi G., Chiarugi P. Integrin-mediated cell adhesion and spreading engage different sources of reactive oxygen species. Antioxid. Redox Signal. 2007, 9:469-481.
111. Tamura M., Kanno M., Endo Y. Deactivation of neutrophil NADPH oxidase by actin-depolymerizing agents in a cell-free system. Biochem. J. 2000, 349:369-375.
112. Thannickal V., Fanburg B. Reactive oxygen species in cell signaling. Am. J. Physiol. Lung Cell. Mol. Physiol. 2000, 279:L1005-L1028.
113. Thiery J.P. Epithelial-mesenchymal transitions in tumour progression. Nat. Rev. Cancer 2002, 2:442-454.
114. Thiery J.P. Epithelial-mesenchymal transitions in development and pathologies. Curr. Opin. Cell Biol. 2003, 15:740-746.
115. Thiery J.P., Sleeman J.P. Complex networks orchestrate epithelial-mesenchymal transitions. Nat. Rev. Mol. Cell Biol. 2006, 7:131-142.
116. Tobar N., Villar V., Santibanez J.F. ROS-NFkappaB mediates TGF-beta1-induced expression of urokinase-type plasminogen activator, matrix metalloproteinase-9 and cell invasion. Mol. Cell. Biochem. 2010, 340:195-202.
117. Tran H., Maurer F., Nagamine Y. Stabilization of urokinase and urokinase receptor mRNAs by HuR is linked to its cytoplasmic accumulation induced by activated mitogen-activated protein kinase-activated protein kinase 2. Mol. Cell. Biol. 2003, 23:7177-7188.
118. Usatyuk P.V., Romer L.H., He D., Parinandi N.L., Kleinberg M.E., Zhan S., Jacobson J.R., Dudek S.M., Pendyala S., Garcia J.G., Natarajan V. Regulation of hyperoxia-induced NADPH oxidase activation in human lung endothelial cells by the actin cytoskeleton and cortactin. J. Biol. Chem. 2007, 282:23284-23295.
119. Ushio-Fukai M., Tang Y., Fukai T., Dikalov S.I., Ma Y., Fujimoto M., Quinn M.T., Pagano P.J., Johnson C., Alexander R.W. Novel role of gp91(phox)-containing NAD(P)H oxidase in vascular endothelial growth factor-induced signaling and angiogenesis. Circ. Res. 2002, 91:1160-1167.
120. Velarde V., de la Cerda P.M., Duarte C., Arancibia F., Abbott E., Gonzalez A., Moreno F., Jaffa A.A. Role of reactive oxygen species in bradykinin-induced proliferation of vascular smooth muscle cells. Biol. Res. 2004, 37:419-430.
121. Vuori K., Ruoslahti E. Activation of protein kinase C precedes alpha 5 beta 1 integrin-mediated cell spreading on fibronectin. J. Biol. Chem. 1993, 268:21459-21462.
122. Wang Y., Zang Q.S., Liu Z., Wu Q., Maass D., Dulan G., Shaul P.W., Melito L., Frantz D.E., Kilgore J.A., Williams N.S., Terada L.S., Nwariaku F.E. Regulation of VEGF-induced endothelial cell migration by mitochondrial reactive oxygen species. Am. J. Physiol. Cell Physiol. 2011, 301:C695-C704.
123. Waris G., Ahsan H. Reactive oxygen species: role in the development of cancer and various chronic conditions. J. Carcinog. 2006, 5:14.
124. Werner E., Werb Z. Integrins engage mitochondrial function for signal transduction by a mechanism dependent on Rho GTPases. J. Cell Biol. 2002, 158:357-368.
125. Wu W.S. The signaling mechanism of ROS in tumor progression. Cancer Metastasis Rev. 2006, 25:695-705.
126. Wu R.F., Gu Y., Xu Y.C., Nwariaku F.E., Terada L.S. Vascular endothelial growth factor causes translocation of p47phox to membrane ruffles through WAVE1. J. Biol. Chem. 2003, 278:36830-36840.
127. Wu W.S., Tsai R.K., Chang C.H., Wang S., Wu J.R., Chang Y.X. Reactive oxygen species mediated sustained activation of protein kinase C alpha and extracellular signal-regulated kinase for migration of human hepatoma cell Hepg2. Mol. Cancer Res. 2006, 4:747-758.
128. Wu W.S., Wu J.R., Hu C.T. Signal cross talks for sustained MAPK activation and cell migration: the potential role of reactive oxygen species. Cancer Metastasis Rev. 2008, 27:303-314.
129. Yamaguchi H., Lorenz M., Kempiak S., Sarmiento C., Coniglio S., Symons M., Segall J., Eddy R., Miki H., Takenawa T., Condeelis J. Molecular mechanisms of invadopodium formation: the role of the N-WASP-Arp2/3 complex pathway and cofilin. J. Cell Biol. 2005, 168:441-452.
130. Yang J.Q., Zhao W., Duan H., Robbins M.E., Buettner G.R., Oberley L.W., Domann F.E. v-Ha-RaS oncogene upregulates the 92-kDa type IV collagenase (MMP-9) gene by increasing cellular superoxide production and activating NF-kappaB. Free Radic. Biol. Med. 2001, 31:520-529.
131. Yang S.H., Sharrocks A.D., Whitmarsh A.J. Transcriptional regulation by the MAP kinase signaling cascades. Gene 2003, 320:3-21.
132. Yap C.T., Simpson T.I., Pratt T., Price D.J., Maciver S.K. The motility of glioblastoma tumour cells is modulated by intracellular cofilin expression in a concentration-dependent manner. Cell Motil. Cytoskeleton 2005, 60:153-165.
133. Zhan Y., He D., Newburger P.E., Zhou G.W. p47(phox) PX domain of NADPH oxidase targets cell membrane via moesin-mediated association with the actin cytoskeleton. J. Cell. Biochem. 2004, 92:795-809.
134. Zhao X., Guan J.L. Focal adhesion kinase and its signaling pathways in cell migration and angiogenesis. Adv. Drug Deliv. Rev. 2011, 63:610-615.