Tks5-dependent, nox-mediated generation of reactive oxygen species is necessary for invadopodia formation

Science Signaling

Volumn 2, Issue 88, 2009, Pages

  Diaz, Begoña ^a   Shani, Gidon ^a   Pass, Ian ^a   Anderson, Diana ^a   Quintavalle, Manuela ^a   Courtneidge, Sara A ^a  

^a BURNHAM INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN P22; PROTEIN TYROSINE KINASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; CYTOCHROME B; FISH PROTEIN, MOUSE; P22(PHOX) PROTEIN, MOUSE; PHOSPHOPROTEIN; SH3PXD2A PROTEIN, HUMAN; SMALL INTERFERING RNA; VESICULAR TRANSPORT ADAPTOR PROTEIN;

ANIMAL CELL; ARTICLE; CANCER CELL; CELL FUNCTION; CELL STRUCTURE; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME SUBSTRATE; HUMAN; HUMAN CELL; INVADOPODIA; MOUSE; NONHUMAN; POSITIVE FEEDBACK; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; ANIMAL; CELL LINE; CELL SURFACE; DRUG ANTAGONISM; FEEDBACK SYSTEM; GENETIC TRANSFECTION; GENETICS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; TUMOR CELL LINE;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; CELL LINE; CELL LINE, TUMOR; CELL SURFACE EXTENSIONS; CYTOCHROME B GROUP; FEEDBACK, PHYSIOLOGICAL; HUMANS; MICE; NADPH OXIDASE; PHOSPHOPROTEINS; PHOSPHORYLATION; REACTIVE OXYGEN SPECIES; RNA, SMALL INTERFERING; TRANSFECTION;

EID: 73949101383     PISSN: 19450877     EISSN: 19379145     Source Type: Journal    
DOI: 10.1126/scisignal.2000368     Document Type: Article

References (82)

1. S. Linder, P. Kopp, Podosomes at a glance. J. Cell Sci. 118, 2079-2082 (2005). (Pubitemid 40872830)
2. A. M. Weaver, Invadopodia: Specialized cell structures for cancer invasion. Clin. Exp. Metastasis 23, 97-105 (2006). (Pubitemid 44440169)
3. J. G. Evans, P. Matsudaira, Structure and dynamics of macrophage podosomes. Eur. J. Cell Biol. 85, 145-149 (2006).
4. S. Linder, The matrix corroded: Podosomes and invadopodia in extracellular matrix degradation. Trends Cell Biol. 17, 107-117 (2007). (Pubitemid 46341826)
5. M. Gimona, R. Buccione, S. A. Courtneidge, S. Linder, Assembly and biological role of podosomes and invadopodia. Curr. Opin. Cell Biol. 20, 235-241 (2008).
6. W. L. Monsky, C. Y. Lin, A. Aoyama, T. Kelly, S. K. Akiyama, S. C. Mueller, W. T. Chen, A potential marker protease of invasiveness, seprase, is localized on invadopodia of human malignant melanoma cells. Cancer Res. 54, 5702-5710 (1994). (Pubitemid 24346270)
7. H. Nakahara, L. Howard, E. W. Thompson, H. Sato, M. Seiki, Y. Yeh, W. T. Chen, Transmembrane/cytoplasmic domain-mediated membrane type 1-matrix metalloprotease docking to invadopodia is required for cell invasion. Proc. Natl. Acad. Sci. U.S.A. 94, 7959-7964 (1997). (Pubitemid 27343757)
8. W. T. Chen, J. Y. Wang, Specialized surface protrusions of invasive cells, invadopodia and lamellipodia, have differential MT1-MMP, MMP-2, and TIMP-2 localization. Ann. N. Y. Acad. Sci. 878, 361-371 (1999).
9. V. V. Artym, A. L. Kindzelskii, W. T. Chen, H. R. Petty, Molecular proximity of seprase and the urokinase-type plasminogen activator receptor on malignant melanoma cell membranes: Dependence on b1 integrins and the cytoskeleton. Carcinogenesis 23, 1593-1601 (2002).
10. C. Tu, C. F. Ortega-Cava, G. Chen, N. D. Fernandes, D. Cavallo-Medved, B. F. Sloane, V. Band, H. Band, Lysosomal cathepsin B participates in the podosome-mediated extracellular matrix degradation and invasion via secreted lysosomes in v-Src fibroblasts. Cancer Res. 68, 9147-9156 (2008).
11. P. J. Coopman, M. T. Do, E. W. Thompson, S. C. Mueller, Phagocytosis of cross-linked gelatin matrix by human breast carcinoma cells correlates with their invasive capacity. Clin. Cancer Res. 4, 507-515 (1998).
12. T. Kelly, Y. Yan, R. L. Osborne, A. B. Athota, T. L. Rozypal, J. C. Colclasure, W. S. Chu, Proteolysis of extracellular matrix by invadopodia facilitates human breast cancer cell in-vasion and is mediated by matrix metalloproteinases. Clin. Exp. Metastasis 16, 501-512 (1998). (Pubitemid 29009586)
13. Y. Y. Chuang, N. L. Tran, N. Rusk, M. Nakada, M. E. Berens, M. Symons, Role of synaptojanin 2 in glioma cell migration and invasion. Cancer Res. 64, 8271-8275 (2004). (Pubitemid 39491764)
14. E. T. Bowden, E. Onikoyi, R. Slack, A. Myoui, T. Yoneda, K. M. Yamada, S. C. Mueller, Co-localization of cortactin and phosphotyrosine identifies active invadopodia in human breast cancer cells. Exp. Cell Res. 312, 1240-1253 (2006).
15. S. E. Tague, V. Muralidharan, C. D'Souza-Schorey, ADP-ribosylation factor 6 regulates tumor cell invasion through the activation of the MEK/ERK signaling pathway. Proc. Natl. Acad. Sci. U.S.A. 101, 9671-9676 (2004). (Pubitemid 38869294)
16. R. Vishnubhotla, S. Sun, J. Huq, M. Bulic, A. Ramesh, G. Guzman, M. Cho, S. C. Glover, ROCK-IImediates colon cancer invasion via regulation of MMP-2 and MMP-13 at the site of invadopodia as revealed by multiphoton imaging. Lab. Invest. 87, 1149-1158 (2007). (Pubitemid 47609026)
17. J. M. Nam, Y. Onodera, Y. Mazaki, H. Miyoshi, S. Hashimoto, H. Sabe, CIN85, a Cblinteracting protein, is a component of AMAP1-mediated breast cancer invasion machinery. EMBO J. 26, 647-656 (2007). (Pubitemid 46253844)
18. B. Blouw, D. F. Seals, I. Pass, B. Diaz, S. A. Courtneidge, A role for the podosome/ invadopodia scaffold protein Tks5 in tumor growth in vivo. Eur. J. Cell Biol. 87, 555-567 (2008).
19. T. Finkel, Oxidant signals and oxidative stress. Curr. Opin. Cell Biol. 15, 247-254 (2003). (Pubitemid 36332201)
20. A. A. Starkov, The role of mitochondria in reactive oxygen species metabolism and signaling. Ann. N. Y. Acad. Sci. 1147, 37-52 (2008).
21. A. Görlach, P. Klappa, T. Kietzmann, The endoplasmic reticulum: Folding, calcium homeostasis, signaling, and redox control. Antioxid. Redox Signal. 8, 1391-1418 (2006). (Pubitemid 44726319)
22. S. Kawanishi, Y. Hiraku, Oxidative and nitrative DNA damage as biomarker for carcinogenesis with special reference to inflammation. Antioxid. Redox Signal. 8, 1047-1058 (2006). (Pubitemid 44036521)
23. A. Federico, F. Morgillo, C. Tuccillo, F. Ciardiello, C. Loguercio, Chronic inflammation and oxidative stress in human carcinogenesis. Int. J. Cancer 121, 2381-2386 (2007). (Pubitemid 350022406)
24. J. M. Matés, J. A. Segura, F. J. Alonso, J. Márquez, Intracellular redox status and oxidative stress: Implications for cell proliferation, apoptosis, and carcinogenesis. Arch. Toxicol. 82, 273-299 (2008).
25. B.M. Babior, J. D. Lambeth, W.Nauseef, The neutrophil NADPH oxidase. Arch. Biochem. Biophys. 397, 342-344 (2002). (Pubitemid 34852301)
26. M. R. Abid, Z. Kachra, K. C. Spokes, W. C. Aird, NADPH oxidase activity is required for endothelial cell proliferation and migration. FEBS Lett. 486, 252-256 (2000).
27. phox-containing NAD(P)H oxidase in vascular endothelial growth factor-induced signaling and angiogenesis. Circ. Res. 91, 1160-1167 (2002). (Pubitemid 36076365)
28. S. Devadas, L. Zaritskaya, S. G. Rhee, L. Oberley, M. S. Williams, Discrete generation of superoxide and hydrogen peroxide by T cell receptor stimulation: Selective regulation of mitogen-activated protein kinase activation and fas ligand expression. J. Exp. Med. 195, 59-70 (2002). (Pubitemid 34074497)
29. P. Chiarugi,G. Pani, E.Giannoni, L. Taddei, R. Colavitti,G. Raugei,M. Symons, S. Borrello, T. Galeotti,G. Ramponi, Reactive oxygen species as essentialmediators of cell adhesion: The oxidative inhibition of a FAK tyrosine phosphatase is required for cell adhesion. J. Cell Biol. 161, 933-944 (2003). (Pubitemid 36718426)
30. H. ten Freyhaus, M. Huntgeburth, K. Wingler, J. Schnitker, A. T. Baumer, M. Vantler, M. M. Bekhite, M. Wartenberg, H. Sauer, S. Rosenkranz, Novel Nox inhibitor VAS2870 attenuates PDGF-dependent smooth muscle cell chemotaxis, but not proliferation. Cardiovasc. Res. 71, 331-341 (2006). (Pubitemid 43913722)
31. J. Mitsushita, J. D. Lambeth, T. Kamata, The superoxide-generating oxidase Nox1 is functionally required for Ras oncogene transformation. Cancer Res. 64, 3580-3585 (2004). (Pubitemid 38657935)
32. D. Ferraro, S. Corso, E. Fasano, E. Panieri, R. Santangelo, S. Borrello, S. Giordano, G. Pani, T. Galeotti, Pro-metastatic signaling by c-Met through RAC-1 and reactive oxygen species (ROS). Oncogene 25, 3689-3698 (2006). (Pubitemid 43980490)
33. D. Gianni, B. Bohl, S. A. Courtneidge, G. M. Bokoch, The involvement of the tyrosine kinase c-Src in the regulation of reactive oxygen species generation mediated by NADPH oxidase-1. Mol. Biol. Cell 19, 2984-2994 (2008).
34. M. G. Binker, A. A. Binker-Cosen, D. Richards, B. Oliver, L. I. Cosen-Binker, EGF promotes invasion by PANC-1 cells through Rac1/ROS-dependent secretion and activation of MMP-2. Biochem. Biophys. Res. Commun. 379, 445-450 (2009).
35. N. K. Tonks, Redox redux: Revisiting PTPs and the control of cell signaling. Cell 121, 667-670 (2005).
36. W. S. Wu, The signaling mechanism of ROS in tumor progression. Cancer Metastasis Rev. 25, 695-705 (2006).
37. W. S. Wu, J. R. Wu, C. T. Hu, Signal cross talks for sustained MAPK activation and cell migration: The potential role of reactive oxygen species. Cancer Metastasis Rev. 27, 303-314 (2008).
38. G. Svineng, C. Ravuri, O. Rikardsen, N. E. Huseby, J. O. Winberg, The role of reactive oxygen species in integrin andmatrix metalloproteinase expression and function. Connect. Tissue Res. 49, 197-202 (2008).
39. G. M. Bokoch, U. G. Knaus, NADPH oxidases: Not just for leukocytes anymore! Trends Biochem. Sci. 28, 502-508 (2003). (Pubitemid 38340415)
40. J. D. Lambeth, NOX enzymes and the biology of reactive oxygen. Nat. Rev. Immunol. 4, 181-189 (2004).
41. K. Bedard, K.H. Krause, The NOX family of ROS-generating NADPH oxidases: Physiology and pathophysiology. Physiol. Rev. 87, 245-313 (2007). (Pubitemid 46209993)
42. G. Cheng, Z. Cao, X. Xu, E. G. van Meir, J. D. Lambeth, Homologs of gp91phox: Cloning and tissue expression of Nox3, Nox4, and Nox5. Gene 269, 131-140 (2001). (Pubitemid 32488913)
43. T. Kawahara, M. T. Quinn, J. D. Lambeth, Molecular evolution of the reactive oxygengenerating NADPH oxidase (Nox/Duox) family of enzymes. BMC Evol. Biol. 7, 109 (2007).
44. J. D. Lambeth, T. Kawahara, B. Diebold, Regulation of Nox and Duox enzymatic activity and expression. Free Radic. Biol. Med. 43, 319-331 (2007).
45. T. Kawahara, J. D. Lambeth, Molecular evolution of Phox-related regulatory subunits for NADPH oxidase enzymes. BMC Evol. Biol. 7, 178 (2007).
46. M. Geiszt, K. Lekstrom, J. Witta, T. L. Leto, Proteins homologous to p47phox and p67phox support superoxide production by NAD(P)H oxidase 1 in colon epithelial cells. J. Biol. Chem. 278, 20006-20012 (2003).
47. I. Szanto, L. Rubbia-Brandt, P. Kiss, K. Steger, B. Banfi, E. Kovari, F. Herrmann, A. Hadengue, K. H. Krause, Expression of NOX1, a superoxide-generating NADPH oxidase, in colon cancer and inflammatory bowel disease. J. Pathol. 207, 164-176 (2005).
48. M. Fukuyama, K. Rokutan, T. Sano, H. Miyake, M. Shimada, S. Tashiro, Overexpression of a novel superoxide-producing enzyme, NADPH oxidase 1, in adenoma and well differentiated adenocarcinoma of the human colon. Cancer Lett. 221, 97-104 (2005).
49. S. D. Lim, C. Sun, J. D. Lambeth, F. Marshall, M. Amin, L.Chung, J. A. Petros,R. S. Arnold, Increased Nox1 and hydrogen peroxide in prostate cancer. Prostate 62, 200-207 (2005).
50. M. Ushio-Fukai, Y. Nakamura, Reactive oxygen species and angiogenesis: NADPH oxidase as target for cancer therapy. Cancer Lett. 266, 37-52 (2008).
51. S. S. Brar, T. P. Kennedy, A. B. Sturrock, T. P. Huecksteadt, M. T. Quinn, A. R. Whorton, J. R. Hoidal, An NAD(P)H oxidase regulates growth and transcription in melanoma cells. Am. J. Physiol. Cell Physiol. 282, C1212-C1224 (2002).
52. J. K. Maranchie, Y. Zhan, Nox4 is critical for hypoxia-inducible factor 2-α transcriptional activity in von Hippel-Lindau-deficient renal cell carcinoma. Cancer Res. 65, 9190-9193 (2005).
53. T. Mochizuki, S. Furuta, J. Mitsushita, W. H. Shang, M. Ito, Y. Yokoo, M. Yamaura, S. Ishizone, J. Nakayama, A. Konagai, K. Hirose, K. Kiyosawa, T. Kamata, Inhibition of NADPH oxidase 4 activates apoptosis via the AKT/apoptosis signal-regulating kinase 1 pathway in pancreatic cancer PANC-1 cells. Oncogene 25, 3699-3707 (2006).
54. P. Lock, C. L. Abram, T. Gibson, S. A. Courtneidge, A new method for isolating tyrosine kinase substrates used to identify fish, an SH3 and PX domain-containing protein, and Src substrate. EMBO J. 17, 4346-4357 (1998).
55. C. L. Abram, D. F. Seals, I. Pass, D. Salinsky, L. Maurer, T. M. Roth, S. A. Courtneidge, The adaptor protein fish associates with members of the ADAMs family and localizes to podosomes of Src-transformed cells. J. Biol. Chem. 278, 16844-16851 (2003).
56. D. F. Seals, E. F. Azucena Jr., I. Pass, L. Tesfay, R. Gordon, M. Woodrow, J. H. Resau, S. A. Courtneidge, The adaptor protein Tks5/Fish is required for podosome formation and function, and for the protease-driven invasion of cancer cells. Cancer Cell 7, 155-165 (2005).
57. M. D. Buschman, P. A. Bromann, P. Cejudo-Martin, F. Wen, I. Pass, S. A. Courtneidge, The novel adaptor protein Tks4 (SH3PXD2B) is required for functional podosome formation. Mol. Biol. Cell 20, 1302-1311 (2009).
58. S. A. Courtneidge, E. F. Azucena, I. Pass, D. F. Seals, L. Tesfay, The SRC substrate Tks5, podosomes (invadopodia), and cancer cell invasion. Cold Spring Harb. Symp. Quant. Biol. 70, 167-171 (2005).
59. Y. Groemping, K. Lapouge, S. J. Smerdon, K. Rittinger, Molecular basis of phosphorylation induced activation of the NADPH oxidase. Cell 113, 343-355 (2003).
60. phox is required for activation of the NADPH oxidase. J. Biol. Chem. 271, 22152-22158 (1996).
61. 2-integrin ligation. Cell Motil. Cytoskeleton 47, 174-188 (2000).
62. R. K. Ambasta, P. Kumar, K. K. Griendling, H. H. Schmidt, R. Busse, R. P. Brandes, Direct interaction of the novel Nox proteins with p22phox is required for the formation of a functionally active NADPH oxidase. J. Biol. Chem. 279, 45935-45941 (2004).
63. N. Ueno, R. Takeya, K. Miyano, H. Kikuchi, H. Sumimoto, The NADPH oxidase Nox3 constitutively produces superoxide in a p22phox-dependent manner: Its regulation by oxidase organizers and activators. J. Biol. Chem. 280, 23328-23339 (2005).
64. L. L. Hilenski, R. E. Clempus, M. T. Quinn, J. D. Lambeth, K. K. Griendling, Distinct subcellular localizations of Nox1 and Nox4 in vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 24, 677-683 (2004).
65. K. Chen, M. T. Kirber, H. Xiao, Y. Yang, J. F. Keaney Jr., Regulation of ROS signal transduction by NADPH oxidase 4 localization. J. Cell Biol. 181, 1129-1139 (2008). (Pubitemid 351915488)
66. phox-related organizers regulate localized NADPH oxidase 1 (Nox1) activity. Sci. Signal. 2, ra54 (2009).
67. K. D.Martyn, L. M. Frederick, K. von Loehneysen,M. C. Dinauer, U.G. Knaus, Functional analysis of Nox4 reveals unique characteristics compared to other NADPH oxidases. Cell. Signal. 18, 69-82 (2006). (Pubitemid 41415716)
68. phox, thereby activating the oxidase. J. Biol. Chem. 274, 33644-33653 (1999). (Pubitemid 129511677)
69. T. Kawahara, D. Ritsick, G. Cheng, J. D. Lambeth, Point mutations in the proline-rich region of p22phox are dominant inhibitors of Nox1- and Nox2-dependent reactive oxygen generation. J. Biol. Chem. 280, 31859-31869 (2005). (Pubitemid 41291936)
70. T. C. Meng, T. Fukada, N. K. Tonks, Reversible oxidation and inactivation of protein tyrosine phosphatases in vivo. Mol. Cell 9, 387-399 (2002). (Pubitemid 34195563)
71. S. S. Stylli, T. T. Stacey, A. M. Verhagen, S. S. Xu, I. Pass, S. A. Courtneidge, P. Lock, Nck adaptor proteins link Tks5 to invadopodia actin regulation and ECM degradation. J. Cell Sci. 122, 2727-2740 (2009).
72. T. Oikawa, T. Itoh, T. Takenawa, Sequential signals toward podosome formation in NIH-src cells. J. Cell Biol. 182, 157-169 (2008). (Pubitemid 352008629)
73. G. Cheng, J. D. Lambeth, NOXO1, regulation of lipid binding, localization, and activation of Nox1 by the Phox homology (PX) domain. J. Biol. Chem. 279, 4737-4742 (2004). (Pubitemid 38199068)
74. M. A. Chellaiah, R. S. Biswas, D. Yuen, U. M. Alvarez, K. A. Hruska, Phosphatidylinositol 3,4,5-trisphosphate directs association of Src homology 2-containing signaling proteins with gelsolin. J. Biol. Chem. 276, 47434-47444 (2001). (Pubitemid 37373125)
75. A. Angers-Loustau, J. F. Cote, A. Charest, D. Dowbenko, S. Spencer, L. A. Lasky, M. L. Tremblay, Protein tyrosine phosphatase-PEST regulates focal adhesion disassembly, migration, and cytokinesis in fibroblasts. J. Cell Biol. 144, 1019-1031 (1999). (Pubitemid 29238975)
76. S. K. Sastry, P. D. Lyons, M. D. Schaller, K. Burridge, PTP-PEST controls motility through regulation of Rac1. J. Cell Sci. 115, 4305-4316 (2002). (Pubitemid 35460701)
77. R. F. Wu, Y. C. Xu, Z. Ma, F. E. Nwariaku, G. A. Sarosi Jr., L. S. Terada, Subcellular targeting of oxidants during endothelial cell migration. J. Cell Biol. 171, 893-904 (2005). (Pubitemid 41746590)
78. J. H. Brumell, A. L. Burkhardt, J. B. Bolen, S. Grinstein, Endogenous reactive oxygen intermediates activate tyrosine kinases in human neutrophils. J. Biol. Chem. 271, 1455-1461 (1996). (Pubitemid 26028630)
79. T. Shono, N. Yokoyama, T. Uesaka, J. Kuroda, R. Takeya, T. Yamasaki, T. Amano, M. Mizoguchi, S. O. Suzuki, H. Niiro, K. Miyamoto, K. Akashi, T. Iwaki, H. Sumimoto, T. Sasaki, Enhanced expression of NADPH oxidase Nox4 in human gliomas and its roles in cell proliferation and survival. Int. J. Cancer 123, 787-792 (2008). (Pubitemid 352032403)
80. E. Laurent, J. W. McCoy III, R. A. Macina, W. Liu, G. Cheng, S. Robine, J. Papkoff, J. D. Lambeth, Nox1 is over-expressed in human colon cancers and correlates with activating mutations in K-Ras. Int. J. Cancer 123, 100-107 (2008). (Pubitemid 351705197)
81. R. L. Berdeaux, B. Diaz, L. Kim, G. S. Martin, Active Rho is localized to podosomes induced by oncogenic Src and is required for their assembly and function. J. Cell Biol. 166, 317-323 (2004). (Pubitemid 39031235)
82. We thank G. Bokoch and D. Gianni for helpful discussions and suggestions, U. Knaus for advice and p22 reagents, T. Mustelin for antibodies to PTP-PEST, and A. Weaver for SCC61 cells. We thank Y. Altman, J. Russo, and E. Monosov for help with ROS measurements. We are especially grateful to E. Azucena, P. Bromann, and M. Peterman for their help in the early stages of this project. Research in the Courtneidge laboratory was supported by the National Cancer Institute and the Mathers Foundation.