Formation of extracellular matrix-digesting invadopodia by primary aortic smooth muscle cells

Circulation Research

Volumn 100, Issue 9, 2007, Pages 1328-1336

  Furmaniak Kazmierczak, Emilia ^a   Crawley, Scott W ^a   Carter, Rhonda L ^a   Maurice, Donald H ^a   Côté, Graham P ^a  

^a QUEEN S UNIVERSITY   (Canada)

Author keywords

Invadopodia; Matrix metalloproteinase; PAK; Podosomes; Src; Vascular smooth muscle cells

Indexed keywords

ACTIN; CELL MARKER; CORTACTIN; GELATINASE B; MATRIX METALLOPROTEINASE 14; MITOGEN ACTIVATED PROTEIN KINASE P38; P21 ACTIVATED KINASE 1; PHORBOL ESTER; PHOSPHOTRANSFERASE; PROTEIN CDC42; RAC1 PROTEIN; TYROSINE; UROKINASE RECEPTOR;

ANIMAL CELL; ANIMAL CELL CULTURE; AORTA MEDIA; ARTICLE; CELL INVASION; CELL TYPE; CONTROLLED STUDY; EMBEDDING; ENZYME ACTIVITY; EXTRACELLULAR MATRIX; IMMUNOFLUORESCENCE MICROSCOPY; INVADOPODIA; MOLECULAR INTERACTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; RAT; SMOOTH MUSCLE FIBER; TUMOR CELL; VASCULAR SMOOTH MUSCLE;

EID: 34248338774     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.106.147744     Document Type: Article

References (41)

1. Owens GK, Kumar MS, Wamhoff BR. Molecular regulation of vascular smooth muscle cell differentiation in development and disease. Physiol Rev. 2004;84:767-801.
2. Schwartz SM. Smooth muscle migration in atherosclerosis and restenosis. J Clin Invest. 1997;99:2814-2817.
3. Indolfi C, Mongiardo A, Curcio A, Torella D. Molecular mechanisms of in-stent restenosis and approach to therapy with eluting stents. Trends Cardiovasc Med. 2003;13:142-148.
4. Buccione R, Orth JD, McNiven MA. Foot and mouth: podosomes, invadopodia and circular dorsal ruffles. Nat Rev Mol Cell Biol. 2004;5:647-657.
5. Linder S, Aepfelbacher M. Podosomes: adhesion hot-spots of invasive cells. Trends Cell Biol. 2003;13:376-385.
6. Ayala I, Baldassarre M, Caldieri G, Buccione R. Invadopodia: A guided tour. Eur J Cell Biol. 2006;85:159-164.
7. Bowden ET, Onikoyi E, Slack R, Myoui A, Yoneda T, Yamada KM, Mueller SC. Co-localization of cortactin and phosphotyrosine identifies active invadopodia in human breast cancer cells. Exp Cell Res. 2006;312:1240-1253.
8. Baldassarre M, Pompeo A, Beznoussenko G, Castaldi C, Cortellino S, McNiven MA, Luini A, Buccione R. Dynamin participates in focal extracellular matrix degradation by invasive cells. Mol Biol Cell. 2003;14:1074-1084.
9. Nitsch L, Gionti E, Cancedda R, Marchisio PC. The podosomes of Rous sarcoma virus transformed chondrocytes show a peculiar ultrastructural organization. Cell Biol Int Rep. 1989;13:919-926.
10. Ochoa GC, Slepnev VI, Neff L, Ringstad N, Takei K, Daniell L, Kim W, Cao H, McNiven M, Baron R, De Camilli P. A functional link between dynamin and the actin cytoskeleton at podosomes. J Cell Biol. 2000;150:377-389.
11. Kelly T, Mueller SC, Yeh Y, Chen WT. Invadopodia promote proteolysis of a wide variety of extracellular matrix proteins. J Cell Physiol. 1994;158:299-308.
12. Nakahara H, Howard L, Thompson EW, Sato H, Seiki M, Yeh Y, Chen WT. Transmembrane/cytoplasmic domain-mediated membrane type 1-matrix metalloprotease docking to invadopodia is required for cell invasion. Proc Natl Acad Sci U S A. 1997;94:7959-7964.
13. Ghersi G, Dong H, Goldstein LA, Yeh Y, Hakkinen L, Larjava HS, Chen WT. Regulation of fibroblast migration on collagenous matrix by a cell surface peptidase complex. J Biol Chem. 2002;277:29231-29241.
14. Webb BA, Eves R, Crawley SW, Zhou S, Cote GP, Mak AS. PAK1 induces podosome formation in A7r5 vascular smooth muscle cells in a PIX-dependent manner. Am J Physiol Cell Physiol. 2005;289:C898-C907.
15. Lener T, Burgstaller G, Crimaldi L, Lach S, Gimona M. Matrix-degrading podosomes in smooth muscle cells. Eur J Cell Biol. 2006;85:183-189.
16. Hai CM, Hahne P, Harrington EO, Gimona M. Conventional protein kinase C mediates phorbol-dibutyrate-induced cytoskeletal remodeling in a7r5 smooth muscle cells. Exp Cell Res. 2002;280:64-74.
17. Pasquet S, Thiebaud P, Faucheux C, Olive M, Fourcade S, Lalevee N, Lamaziere JM, Theze N. Characterization of a mammalian smooth muscle cell line that has retained transcriptional and posttranscriptional potencies. In Vitro Cell Dev Biol Anim. 2004;40:133-137.
18. Firulli AB, Han D, Kelly-Roloff L, Koteliansky VE, Schwartz SM, Olson EN, Miano JM. A comparative molecular analysis of four rat smooth muscle cell lines. In Vitro Cell Dev Biol Anim. 1998;34:217-226.
19. Dechert MA, Holder JM, Gerthoffer WT. p21-activated kinase 1 participates in tracheal smooth muscle cell migration by signaling to p38 Mapk. Am J Physiol Cell Physiol. 2001;281:C123-C132.
20. Hung W, Elliott B. Co-operative effect of c-Src tyrosine kinase and Stat3 in activation of hepatocyte growth factor expression in mammary carcinoma cells. J Biol Chem. 2001;276:12395-12403.
21. Bochaton-Piallat ML, Gabbiani F, Ropraz P, Gabbiani G. Cultured aortic smooth muscle cells from newborn and adult rats show distinct cytoskeletal features. Differentiation. 1992;49:175-185.
22. Vernon RB, Sage EH. A novel, quantitative model for study of endothelial cell migration and sprout formation within three-dimensional collagen matrices. Microvasc Res. 1999;57:118-133.
23. Chen WT, Olden K, Bernard BA, Chu FF Expression of transformation- associated protease(s) that degrade fibronectin at cell contact sites. J Cell Biol. 1984;98:1546-1555.
24. Weaver AM, Young ME, Lee WL, Cooper JA. Integration of signals to the Arp2/3 complex. Curr Opin Cell Biol. 2003;15:23-30.
25. Burgstaller G, Gimona M. Actin cytoskeleton remodelling via local inhibition of contractility at discrete microdomains. J Cell Sci. 2004;117:223-231.
26. Zhou S, Webb BA, Eves R, Mak AS. Effects of Tyr-phosphorylation of cortactin on podosome-formation in A7r5 vascular smooth muscle cells. Am J Physiol Cell Physiol. 2005;290:C463-C471.
27. Osiak AE, Zenner G, Linder S. Subconfluent endothelial cells form podosomes downstream of cytokine and RhoGTPase signaling. Exp Cell Res. 2005;307:342-353.
28. Johnson C, Galis ZS. Matrix metalloproteinase-2 and -9 differentially regulate smooth muscle cell migration and cell-mediated collagen organization. Arterioscler Thromb Vasc Biol. 2004;24:54-60.
29. Bourguignon LY, Gunja-Smith Z, Iida N, Zhu HB, Young LJ, Muller WJ, Cardiff RD. CD44v(3,8-10) is involved in cytoskeleton-mediated tumor cell migration and matrix metalloproteinase (MMP-9) association in metastatic breast cancer cells. J Cell Physiol. 1998;176:206-215.
30. Blasi F, Carmeliet P. uPAR: a versatile signalling orchestrator. Nat Rev Mol Cell Biol. 2002;3:932-943.
31. Chen WT. Proteolytic activity of specialized surface protrusions formed at rosette contact sites of transformed cells. J Exp Zool. 1989;251:167-185.
32. Artym VV, Zhang Y, Seillier-Moiseiwitsch F, Yamada KM, Mueller SC. Dynamic interactions of cortactin and membrane type 1 matrix metallo-proteinase at invadopodia: defining the stages of invadopodia formation and function. Cancer Res. 2006;66:3034-3043.
33. Filippov S, Koenig GC, Chun TH, Hotary KB, Ota I, Bugge TH, Roberts JD, Fay WP, Birkedal-Hansen H, Holmbeck K, Sabeh F, Allen ED, Weiss SJ. MT1-matrix metalloproteinase directs arterial wall invasion and neointima formation by vascular smooth muscle cells. J Exp Med. 2005;202:663-671.
34. Burgstaller G, Gimona M. Podosome-mediated matrix resorption and cell motility in vascular smooth muscle cells. Am J Physiol Heart Circ Physiol. 2005;288:H3001-H3005.
35. Tatin F, Varon C, Genot E, Moreau V. A signalling cascade involving PKC, Src and Cdc42 regulates podosome assembly in cultured endothelial cells in response to phorbol ester. J Cell Sci. 2006;119:769-781.
36. Brandt DT, Goerke A, Heuer M, Gimona M, Leitges M, Kremmer E, Lammers R, Haller H, Mischak H. Protein kinase C delta induces Src kinase activity via activation of the protein tyrosine phosphatase PTP alpha. J Biol Chem. 2003;278:34073-34078.
37. Gatesman A, Walker VG, Baisden JM, Weed SA, Flynn DC. Protein kinase Calpha activates c-Src and induces podosome formation via AFAP-110. Mol Cell Biol. 2004;24:7578-7597.
38. Salamanca DA, Khalil RA. Protein kinase C isoforms as specific targets for modulation of vascular smooth muscle function in hypertension. Biochem Pharmacol. 2005;70:1537-1547.
39. Sundberg-Smith LJ, Doherty JT, Mack CP, Taylor JM. Adhesion stimulates direct PAK1/ERK2 association and leads to ERK-dependent PAK1 Thr212 phosphorylation. J Biol Chem. 2005;280:2055-2064.
40. Bokoch GM. Biology of the p21-Activated Kinases. Annu Rev Biochem. 2003;72:743-781.
41. Tang DD, Bai Y, Gunst SJ. Silencing of p21-activated kinase attenuates vimentin phosphorylation on Ser-56 and reorientation of the vimentin network during stimulation of smooth muscle cells by 5-hydroxytryptamine. Biochem J. 2005;388:773-783.