3β1 integrins regulate CD151 complex assembly and membrane dynamics in carcinoma cells within 3D environments

Oncogene

Volumn 32, Issue 34, 2013, Pages 3965-3979

  Scales, T M E ^a   Jayo, A ^a   Obara, B ^b   Holt, M R ^a   Hotchin, N A ^c   Berditchevski, F ^c   Parsons, M ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

3 integrin; 3D ECM; Actin cytoskeleton; CD151; Migration; protrusion

Indexed keywords

CD151 ANTIGEN; HOMODIMER; LAMININ; MATRIGEL; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; VERY LATE ACTIVATION ANTIGEN 3; PHOTOPROTEIN; PROTEIN BINDING;

ARTICLE; BREAST CARCINOMA; CARCINOMA CELL; CELL INVASION; CELL MEMBRANE; CELL MIGRATION; CELL POLARITY; CONTROLLED STUDY; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; BREAST TUMOR; CELL MOTION; CELL STRAIN HEK293; CHEMISTRY; CULTURE TECHNIQUE; FEMALE; GENETIC TRANSFECTION; GENETICS; KINETICS; METABOLISM; METHODOLOGY; PATHOLOGY; PROTEIN MULTIMERIZATION; RNA INTERFERENCE; TUMOR CELL LINE; WESTERN BLOTTING; HEK293 CELL LINE; PROCEDURES;

ANTIGENS, CD151; BLOTTING, WESTERN; BREAST NEOPLASMS; CELL CULTURE TECHNIQUES; CELL LINE, TUMOR; CELL MEMBRANE; CELL MOVEMENT; FEMALE; FLUORESCENCE RESONANCE ENERGY TRANSFER; HEK293 CELLS; HUMANS; INTEGRIN ALPHA3BETA1; KINETICS; LUMINESCENT PROTEINS; PROTEIN BINDING; PROTEIN MULTIMERIZATION; RHO GTP-BINDING PROTEINS; RNA INTERFERENCE; TRANSFECTION;

EID: 84883136971     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.415     Document Type: Article

References (57)

1. Hynes RO. Integrins: bidirectional, allosteric signaling machines. Cell 2002; 110: 673-687.
2. Turner FE, Broad S, Khanim FL, Jeanes A, Talma S, Hughes S et al. Slug regulates integrin expression and cell proliferation in human epidermal keratinocytes. J Biol Chem 2006; 281: 21321-21331.
3. Nguyen BP, Gil SG, Carter WG. Deposition of laminin 5 by keratinocytes regulates integrin adhesion and signaling. J Biol Chem 2000; 275: 31896-31907.
4. Stipp CS. Laminin-binding integrins and their tetraspanin partners as potential antimetastatic targets. Expert Rev Mol Med 2010; 12: e3.
5. Reynolds LE, Conti FJ, Silva R, Robinson SD, Iyer V, Rudling R et al. Alpha3beta1 integrin-controlled Smad7 regulates reepithelialization during wound healing in mice. J Clin Invest 2008; 118: 965-974.
6. Morini M, Mottolese M, Ferrari N, Ghiorzo F, Buglioni S, Mortarini R et al. The alpha 3 beta 1 integrin is associated with mammary carcinoma cell metastasis, invasion, and gelatinase B (MMP-9) activity. Int J Cancer 2000; 87: 336-342.
7. Fukushima Y, Ohnishi T, Arita N, Hayakawa T, Sekiguchi K. Integrin alpha3beta1-mediated interaction with laminin-5 stimulates adhesion, migration and invasion of malignant glioma cells. Int J Cancer 1998; 76: 63-72.
8. Melchiori A, Mortarini R, Carlone S, Marchisio PC, Anichini A, Noonan DM et al. The alpha 3 beta 1 integrin is involved in melanoma cell migration and invasion. Exp Cell Res 1995; 219: 233-242.
9. Okada T, Okuno H, Mitsui Y. A novel in vitro assay system for transendothelial tumor cell invasion: significance of E-selectin and alpha 3 integrin in the transendothelial invasion by HT1080 fibrosarcoma cells. Clin Exp Metastasis 1994; 12: 305-314.
10. Yanez-Mo M, Barreiro O, Gordon-Alonso M, Sala-Valdes M, Sanchez-Madrid F. Tetraspanin-enriched microdomains: a functional unit in cell plasma membranes. Trends Cell Biol 2009; 19: 434-446.
11. Claas C, Stipp CS, Hemler ME. Evaluation of prototype transmembrane 4 superfamily protein complexes and their relation to lipid rafts. J Biol Chem 2001; 276: 7974-7984.
12. Hemler ME. Tetraspanin functions and associated microdomains. Nat Rev Mol Cell Biol 2005; 6: 801-811.
13. Yauch RL, Berditchevski F, Harler MB, Reichner J, Hemler ME. Highly stoichiometric, stable, and specific association of integrin alpha3beta1 with CD151 provides a major link to phosphatidylinositol 4-kinase, and may regulate cell migration. Mol Biol Cell 1998; 9: 2751-2765.
14. Stipp CS, Kolesnikova TV, Hemler ME. Functional domains in tetraspanin proteins. Trends Biochem Sci 2003; 28: 106-112.
15. Zhang XA, Bontrager AL, Hemler ME. Transmembrane-4 superfamily proteins associate with activated protein kinase C (PKC) and link PKC to specific beta(1) integrins. J Biol Chem 2001; 276: 25005-25013.
16. Sadej R, Romanska H, Baldwin G, Gkirtzimanaki K, Novitskaya V, Filer AD et al. CD151 regulates tumorigenesis by modulating the communication between tumor cells and endothelium. Mol Cancer Res 2009; 7: 787-798.
17. Yang XH, Richardson AL, Torres-Arzayus MI, Zhou P, Sharma C, Kazarov AR et al. CD151 accelerates breast cancer by regulating alpha 6 integrin function, signaling, and molecular organization. Cancer Res 2008; 68: 3204-3213.
18. Zijlstra A, Lewis J, Degryse B, Stuhlmann H, Quigley JP. The inhibition of tumor cell intravasation and subsequent metastasis via regulation of in vivo tumor cell motility by the tetraspanin CD151. Cancer Cell 2008; 13: 221-234.
19. Tokuhara T, Hasegawa H, Hattori N, Ishida H, Taki T, Tachibana S et al. Clinical significance of CD151 gene expression in non-small cell lung cancer. Clin Cancer Res 2001; 7: 4109-4114.
20. Hashida H, Takabayashi A, Tokuhara T, Hattori N, Taki T, Hasegawa H et al. Clinical significance of transmembrane 4 superfamily in colon cancer. Br J Cancer 2003; 89: 158-167.
21. Ang J, Lijovic M, Ashman LK, Kan K, Frauman AG. CD151 protein expression predicts the clinical outcome of low-grade primary prostate cancer better than histologic grading: a new prognostic indicator? Cancer Epidemiol Biomarkers Prev 2004; 13(Pt 1): 1717-1721.
22. Winterwood NE, Varzavand A, Meland MN, Ashman LK, Stipp CS. A critical role for tetraspanin CD151 in alpha3beta1 and alpha6beta4 integrin-dependent tumor cell functions on laminin-5. Mol Biol Cell 2006; 17: 2707-2721.
23. Baldwin G, Novitskaya V, Sadej R, Pochec E, Litynska A, Hartmann C et al. Tetraspanin CD151 regulates glycosylation of (alpha)3(beta)1 integrin. J Biol Chem 2008; 283: 35445-35454.
24. Liu L, He B, Liu WM, Zhou D, Cox JV, Zhang XA. Tetraspanin CD151 promotes cell migration by regulating integrin trafficking. J Biol Chem 2007; 282: 31631-31642.
25. Sugiura T, Berditchevski F. Function of alpha3beta1-tetraspanin protein complexes in tumor cell invasion. Evidence for the role of the complexes in production of matrix metalloproteinase 2 (MMP-2). J Cell Biol 1999; 146: 1375-1389.
26. Zhou H, Kramer RH. Integrin engagement differentially modulates epithelial cell motility by RhoA/ROCK and PAK1. J Biol Chem 2005; 280: 10624-10635.
27. Frank DE, Carter WG. Laminin 5 deposition regulates keratinocyte polarization and persistent migration. J Cell Sci 2004; 117: 1351-1363.
28. Yauch RL, Kazarov AR, Desai B, Lee RT, Hemler ME. Direct extracellular contact between integrin alpha(3)beta(1) and TM4SF protein CD151. J Biol Chem 2000; 275: 9230-9238.
29. Sterk LM, Geuijen CA, van den Berg JG, Claessen N, Weening JJ, Sonnenberg A. Association of the tetraspanin CD151 with the laminin-binding integrins alpha3beta1, alpha6beta1, alpha6beta4 and alpha7beta1 in cells in culture and in vivo. J Cell Sci 2002; 115: 1161-1173.
30. Morton PE, Parsons M. Measuring FRET using time-resolved FLIM. Methods Mol Biol 2011; 769: 403-413.
31. Worth DC, Parsons M. Adhesion dynamics: mechanisms and measurements. Int J Biochem Cell Biol 2008; 40: 2397-2409.
32. Parsons M, Messent AJ, Humphries JD, Deakin NO, Humphries MJ. Quantification of integrin receptor agonism by fluorescence lifetime imaging. J Cell Sci 2008; 121: 265-271.
33. Yang X, Claas C, Kraeft SK, Chen LB, Wang Z, Kreidberg JA et al. Palmitoylation of tetraspanin proteins: modulation of CD151 lateral interactions, subcellular distribution, and integrin-dependent cell morphology. Mol Biol Cell 2002; 13: 767-781.
34. Berditchevski F, Gilbert E, Griffiths MR, Fitter S, Ashman L, Jenner SJ. Analysis of the CD151-alpha3beta1 integrin and CD151-tetraspanin interactions by mutagenesis. J Biol Chem 2001; 276: 41165-41174.
35. Hodivala-Dilke KM, DiPersio CM, Kreidberg JA, Hynes RO. Novel roles for alpha3beta1 integrin as a regulator of cytoskeletal assembly and as a transdominant inhibitor of integrin receptor function in mouse keratinocytes. J Cell Biol 1998; 142: 1357-1369.
36. Wang Z, Symons JM, Goldstein SL, McDonald A, Miner JH, Kreidberg JA. (Alpha)3(beta)1 integrin regulates epithelial cytoskeletal organization . J Cell Sci 1999; 112: Pt 17 2925-2935.
37. Nakamura T, Kurokawa K, Kiyokawa E, Matsuda M. Analysis of the spatiotemporal activation of rho GTPases using Raichu probes. Methods Enzymol 2006; 406: 315-332.
38. Carmona-Fontaine C, Matthews HK, Kuriyama S, Moreno M, Dunn GA, Parsons M et al. Contact inhibition of locomotion in vivo controls neural crest directional migration. Nature 2008; 456: 957-961.
39. Lichtner RB, Howlett AR, Lerch M, Xuan JA, Brink J, Langton-Webster B et al. Negative cooperativity between alpha 3 beta 1 and alpha 2 beta 1 integrins in human mammary carcinoma MDA MB 231 cells. Exp Cell Res 1998; 240: 368-376.
40. Kazarov AR, Yang X, Stipp CS, Sehgal B, Hemler ME. An extracellular site on tetraspanin CD151 determines alpha 3 and alpha 6 integrin-dependent cellular morphology. J Cell Biol 2002; 158: 1299-1309.
41. Vicente-Manzanares M, Ma X, Adelstein RS, Horwitz AR. Non-muscle myosin II takes centre stage in cell adhesion and migration. Nat Rev Mol Cell Biol 2009; 10: 778-790.
42. Nishiya N, Kiosses WB, Han J, Ginsberg MH. An alpha4 integrin-paxillin- Arf-GAP complex restricts Rac activation to the leading edge of migrating cells. Nat Cell Biol 2005; 7: 343-352.
43. Sarmiento C, Wang W, Dovas A, Yamaguchi H, Sidani M, El-Sibai M et al. WASP family members and formin proteins coordinate regulation of cell protrusions in carcinoma cells. J Cell Biol 2008; 180: 1245-1260.
44. Egeblad M, Rasch MG, Weaver VM. Dynamic interplay between the collagen scaffold and tumor evolution. Curr Opin Cell Biol 2010; 22: 697-706.
45. Mitchell K, Svenson KB, Longmate WM, Gkirtzimanaki K, Sadej R, Wang X et al. Suppression of integrin alpha3beta1 in breast cancer cells reduces cyclooxygenase-2 gene expression and inhibits tumorigenesis, invasion, and cross-talk to endothelial cells. Cancer Res 2010; 70: 6359-6367.
46. Arthur WT, Burridge K. RhoA inactivation by p190RhoGAP regulates cell spreading and migration by promoting membrane protrusion and polarity. Mol Biol Cell 2001; 12: 2711-2720.
47. Sah VP, Seasholtz TM, Sagi SA, Brown JH. The role of Rho in G proteincoupled receptor signal transduction. Annu Rev Pharmacol Toxicol 2000; 40: 459-489.
48. Takeda Y, Li Q, Kazarov AR, Epardaud M, Elpek K, Turley SJ et al. Diminished metastasis in tetraspanin CD151-knockout mice. Blood 2011; 118: 464-472.
49. Gu J, Sumida Y, Sanzen N, Sekiguchi K. Laminin-10/11 and fibronectin differentially regulate integrin-dependent Rho and Rac activation via p130(Cas)-CrkIIDOCK180 pathway. J Biol Chem 2001; 276: 27090-27097.
50. Ridley AJ. Life at the leading edge. Cell 2011; 145: 1012-1022.
51. Nobes CD, 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.
52. Ramirez NE, Zhang Z, Madamanchi A, Boyd KL, O'Rear LD, Nashabi A et al. The alphabeta integrin is a metastasis suppressor in mouse models and human cancer. J Clin Invest 2011; 121: 226-237.
53. Calderwood DA, Tai V, Di Paolo G, De Camilli P, Ginsberg MH. Competition for talin results in trans-dominant inhibition of integrin activation. J Biol Chem 2004; 279: 28889-28895.
54. Latysheva N, Muratov G, Rajesh S, Padgett M, Hotchin NA, Overduin M et al. Syntenin-1 is a new component of tetraspanin-enriched microdomains: mechanisms and consequences of the interaction of syntenin-1 with CD63. Mol Cell Biol 2006; 26: 7707-7718.
55. Parsons M, Monypenny J, Ameer-Beg SM, Millard TH, Machesky LM, Peter M et al. Spatially distinct binding of Cdc42 to PAK1 and N-WASP in breast carcinoma cells. Mol Cell Biol 2005; 25: 1680-1695.
56. Worth DC, Hodivala-Dilke K, Robinson SD, King SJ, Morton PE, Gertler FB et al. Alpha v beta3 integrin spatially regulates VASP and RIAM to control adhesion dynamics and migration. J Cell Biol 2010; 189: 369-383.
57. Matthews HK, Marchant L, Carmona-Fontaine C, Kuriyama S, Larrain J, Holt MR et al. Directional migration of neural crest cells in vivo is regulated by Syndecan-4/Rac1 and non-canonical Wnt signaling/RhoA. Development 2008; 135: 1771-1780.