Prometastatic NEDD9 regulates individual cell migration via caveolin-1-dependent trafficking of integrins

Molecular Cancer Research

Volumn 13, Issue 3, 2015, Pages 423-438

  Kozyulina, Polina Y ^a,b   Loskutov, Yuriy V ^a   Kozyreva, Varvara K ^a   Rajulapati, Anuradha ^a   Ice, Ryan J ^a   Jones, Brandon C ^a   Pugacheva, Elena N ^a  

^a WEST VIRGINIA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INSTITUTE OF CYTOLOGY   (Russian Federation)

Author keywords

[No Author keywords available]

Indexed keywords

CAVEOLIN 1; INTEGRIN; PROTEIN; PROTEIN NEDD9; TYROSINE; UNCLASSIFIED DRUG; NEDD9 PROTEIN, HUMAN; PHOSPHOPROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ARTICLE; BREAST CANCER CELL LINE; CELL ADHESION; CELL MIGRATION; CELL VACUOLE; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; METASTASIS; MOLECULAR BIOLOGY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; REGULATORY MECHANISM; BREAST TUMOR; CELL MOTION; FEMALE; GENETICS; HUMAN; METABOLISM; PATHOLOGY; TUMOR CELL LINE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; BREAST NEOPLASMS; CAVEOLIN 1; CELL ADHESION; CELL LINE, TUMOR; CELL MOVEMENT; ENDOSOMES; FEMALE; HUMANS; INTEGRINS; PHOSPHOPROTEINS; PROTEIN TRANSPORT;

EID: 84928014692     PISSN: 15417786     EISSN: 15573125     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-14-0353     Document Type: Article

References (47)

1. Pugacheva EN, Golemis EA. The focal adhesion scaffolding protein HEF1 regulates activation of the Aurora-A and Nek2 kinases at the centrosome. Nat Cell Biol 2005;7:937-46.
2. Zhong J, Baquiran JB, Bonakdar N, Lees J, Ching YW, Pugacheva E, et al. NEDD9 stabilizes focal adhesions, increases binding to the extra-cellular matrix and differentially effects 2D versus 3D cell migration. PLoS ONE 2012;7:e35058.
3. Jin Y, Li F, Zheng C, Wang Y, Fang Z, Guo C, et al. NEDD9 promotes lung cancer metastasis through epithelial-mesenchymal transition. Int J Cancer 2014;134:2294-304.
4. Ahn J, Sanz-Moreno V, Marshall CJ. The metastasis gene NEDD9 product acts through integrin beta3 and Src to promotemesenchymal motility and inhibit amoeboid motility. J Cell Sci 2012;125(Pt 7):1814-26.
5. ONeill GM, Seo S, Serebriiskii IG, Lessin SR, Golemis EA. A new central scaffold for metastasis: parsing HEF1/Cas-L/NEDD9. Cancer Res 2007; 67:8975-9.
6. Singh MK, Izumchenko E, Klein-Szanto AJ, Egleston BL, Wolfson M, Golemis EA. Enhanced genetic instability and dasatinib sensitivity in mammary tumor cells lacking NEDD9. Cancer Res 2010;70: 8907-16.
7. McLaughlin SL, Ice RJ, Rajulapati A, Kozyulina PY, Livengood RH, Kozyreva VK, et al. NEDD9 depletion leads to MMP14 inactivation by TIMP2 and prevents invasion and metastasis. Mol Cancer Res 2014;12:69-81.
8. Izumchenko E, Singh MK, Plotnikova OV, Tikhmyanova N, Little JL, Serebriiskii IG, et al. NEDD9 promotes oncogenic signaling in mammary tumor development. Cancer Res 2009;69:7198-206.
9. Kong C, Wang C, Wang L, Ma M, Niu C, Sun X, et al. NEDD9 is a positive regulator of epithelial-mesenchymal transition and promotes invasion in aggressive breast cancer. PLoS ONE 2011;6:e22666.
10. Sima N, Cheng X, Ye F, Ma D, Xie X, Lu W. The overexpression of scaffolding protein NEDD9 promotes migration and invasion in cervical cancer via tyrosine phosphorylated FAK and SRC. PLoS ONE 2013;8:e74594.
11. Patani N, Martin LA, Reis-Filho JS, Dowsett M. The role of caveolin-1 in human breast cancer. Breast Cancer Res Treat 2012;131:1-15.
12. Pellinen T, Ivaska J. Integrin traffic. J Cell Sci 2006;119(Pt 18):3723-31.
13. Salanueva IJ, Cerezo A, Guadamillas MC, del Pozo MA. Integrin regulation of caveolin function. J Cell Mol Med 2007;11:969-80.
14. Aoki T, Nomura R, Fujimoto T. Tyrosine phosphorylation of caveolin-1 in the endothelium. Exp Cell Res 1999;253:629-36.
15. Irschick R, Trost T, Karp G, Hausott B, Auer M, Claus P, et al. Sorting of the FGF receptor 1 in a human glioma cell line. Histochem Cell Biol 2013; 139:135-48.
16. Schmidt-Glenewinkel H, Vacheva I, Hoeller D, Dikic I, Eils R. An ultrasensitive sorting mechanism for EGF receptor endocytosis. BMC Syst Biol 2008;2:32.
17. Echarri A, Muriel O, Del Pozo MA. Intracellular trafficking of raft/caveolae domains: insights from integrin signaling. Semin Cell Dev Biol 2007;18: 627-37.
18. Cao H, Courchesne WE, Mastick CC. A phosphotyrosine-dependent protein interaction screen reveals a role for phosphorylation of caveolin-1 on tyrosine 14: recruitment of C-terminal Src kinase. J Biol Chem 2002; 277:8771-4.
19. Corn PG, Thompson TC. Identification of a novel prostate cancer biomarker, caveolin-1: Implications and potential clinical benefit. Cancer Manag Res 2010;2:111-22.
20. Wehrle-Haller B. Assembly and disassembly of cell matrix adhesions. Curr Opin Cell Biol 2012;24:569-81.
21. Luo BH, Carman CV, Springer TA. Structural basis of integrin regulation and signaling. Annu Rev Immunol 2007;25:619-47.
22. Cabodi S, del Pilar Camacho-Leal M, Di Stefano P, Defilippi P. Integrin signalling adaptors: not only figurants in the cancer story. Nat Rev Cancer 2010;10:858-70.
23. Arjonen A, Alanko J, Veltel S, Ivaska J. Distinct recycling of active and inactive beta1 integrins. Traffic 2012;13:610-25.
24. Arora PD, Manolson MF, Downey GP, Sodek J, McCulloch CA. A novel model system for characterization of phagosomal maturation, acidification, and intracellular collagen degradation in fibroblasts. J Biol Chem 2000;275:35432-41.
25. del Pozo MA, Balasubramanian N, Alderson NB, Kiosses WB, Grande- Garcia A, Anderson RG, et al. Phospho-caveolin-1 mediates integrinregulated membrane domain internalization. Nat Cell Biol 2005;7: 901-8.
26. Pugacheva EN, Jablonski SA, Hartman TR, Henske EP, Golemis EA. HEF1- dependent Aurora A activation induces disassembly of the primary cilium. Cell 2007;129:1351-63.
27. Ice RJ, McLaughlin SL, Livengood RH, Culp MV, Eddy ER, Ivanov AV, et al. NEDD9 depletion destabilizes Aurora A kinase and heightens the efficacy of Aurora A inhibitors: implications for treatment of metastatic solid tumors. Cancer Res 2013;73:3168-80.
28. Macdonald JL, Pike LJ. A simplified method for the preparation of detergent- free lipid rafts. J Lipid Res 2005;46:1061-7.
29. Carter WG, Wayner EA, Bouchard TS, Kaur P. The role of integrins alpha 2 beta 1 and alpha 3 beta 1 in cell-cell and cell-substrate adhesion of human epidermal cells. J Cell Biol 1990;110:1387-404.
30. Wegener J, Keese CR, Giaever I. Electric cell-substrate impedance sensing (ECIS) as a noninvasive means to monitor the kinetics of cell spreading to artificial surfaces. Exp Cell Res 2000;259:158-66.
31. Chan CM, Huang JH, Chiang HS, Wu WB, Lin HH, Hong JY, et al. Effects of (-)-epigallocatechin gallate on RPE cell migration and adhesion. Mol Vis 2010;16:586-95.
32. Nethe M, Anthony EC, Fernandez-Borja M, Dee R, Geerts D, Hensbergen PJ, et al. Focal-adhesion targeting links caveolin-1 to a Rac1-degradation pathway. J Cell Sci 2010;123(Pt 11):1948-58.
33. Gorshkova I, He D, Berdyshev E, Usatuyk P, Burns M, Kalari S, et al. Protein kinase C-epsilon regulates sphingosine 1-phosphate-mediated migration of human lung endothelial cells through activation of phospholipase D2, protein kinase C-zeta, and Rac1. J Biol Chem 2008; 283:11794-806.
34. Glukhova MA, Streuli CH.Howintegrins control breast biology. Curr Opin Cell Biol 2013;25:633-41.
35. Hanein D, Horwitz AR. The structure of cell-matrix adhesions: the new frontier. Curr Opin Cell Biol 2012;24:134-40.
36. Yamamoto M, Yamato M, Aoyagi M, Yamamoto K. Identification of integrins involved in cell adhesion to native and denatured type I collagens and the phenotypic transition of rabbit arterial smooth muscle cells. Exp Cell Res 1995;219:249-56.
37. Mould AP, Akiyama SK, Humphries MJ. The inhibitory anti-beta1 integrin monoclonal antibody 13 recognizes an epitope that is attenuated by ligand occupancy. Evidence for allosteric inhibition of integrin function. J Biol Chem 1996;271:20365-74.
38. Mould AP, Garratt AN, Askari JA, Akiyama SK, Humphries MJ. Identification of a novel anti-integrin monoclonal antibody that recognises a ligandinduced binding site epitope on the beta 1 subunit. FEBS Lett 1995;363: 118-22.
39. Shi F, Sottile J. Caveolin-1-dependent beta1 integrin endocytosis is a critical regulator of fibronectin turnover. J Cell Sci 2008;121(Pt 14):2360-71.
40. Barczyk M, Carracedo S, Gullberg D. Integrins. Cell Tissue Res 2010;339: 269-80.
41. Valdembri D, Serini G. Regulation of adhesion site dynamics by integrin traffic. Curr Opin Cell Biol 2012;24:582-91.
42. Dozynkiewicz MA, Jamieson NB, Macpherson I, Grindlay J, van den Berghe PV, von Thun A, et al. Rab25 and CLIC3 collaborate to promote integrin recycling from late endosomes/lysosomes and drive cancer progression. Dev Cell 2012;22:131-45.
43. Bass MD, Williamson RC, Nunan RD, Humphries JD, Byron A, Morgan MR, et al. A syndecan-4 hair trigger initiates wound healing through caveolin- and RhoG-regulated integrin endocytosis. Dev Cell 2011;21: 681-93.
44. Roberts M, Barry S, Woods A, van der Sluijs P, Norman J. PDGFregulated rab4-dependent recycling of alphavbeta3 integrin from early endosomes is necessary for cell adhesion and spreading. Curr Biol 2001;11:1392-402.
45. Margadant C, Monsuur HN, Norman JC, Sonnenberg A. Mechanisms of integrin activation and trafficking. Curr Opin Cell Biol 2011;23:607-14.
46. Boyd ND, Chan BM, Petersen NO. Adaptor protein-2 exhibits alpha 1 beta 1 or alpha 6 beta 1 integrin-dependent redistribution in rhabdomyosarcoma cells. Biochemistry 2002;41:7232-40.
47. Boscher C, Nabi IR. Galectin-3- and phospho-caveolin-1-dependent outside- in integrin signaling mediates the EGF motogenic response in mammary cancer cells. Mol Biol Cell 2013;24:2134-45.