S100A4 downregulates filopodia formation through increased dynamic instability

Cell Adhesion and Migration

Volumn 5, Issue 5, 2011, Pages

  Sin, Connie Goh Then ^a   Hersch, Nils ^c   Rudland, Philip S ^b   Barraclough, Roger ^b   Hoffmann, Bernd ^c   Gross, Stephane R ^a  

^a ASTON UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF LIVERPOOL   (United Kingdom)

^c FORSCHUNGSZENTRUM JÜLICH   (Germany)

Author keywords

Cancer progression; Cell migration; Filopodia; Focal adhesion; Myosin IIA; S100A4

Indexed keywords

CALVASCULIN; MYOSIN IIA; CELL ADHESION MOLECULE; PROTEIN S 100; S100A4 PROTEIN, RAT;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELL ASSAY; CELL MIGRATION; CELL MOTILITY; CELL ORGANELLE; CONTROLLED STUDY; DOWN REGULATION; FILOPODIUM; GENE OVEREXPRESSION; LAMELLIPODIUM; NONHUMAN; PROTEIN BINDING; PROTEIN FUNCTION; RAT; TUMOR CELL LINE; ANIMAL; CELL LINE; CELL MOTION; CHEMISTRY; FOCAL ADHESION; GENETICS; METABOLISM; PHYSIOLOGY; PSEUDOPODIUM;

RATTUS;

ANIMALS; CELL ADHESION MOLECULES; CELL LINE; CELL MOVEMENT; DOWN-REGULATION; FOCAL ADHESIONS; NONMUSCLE MYOSIN TYPE IIA; PSEUDOPODIA; RATS; S100 PROTEINS;

EID: 80053435531     PISSN: 19336918     EISSN: 19336926     Source Type: Journal    
DOI: None     Document Type: Article

References (50)

1. Kirfel G, Rigort A, Borm B, Herzog V. Cell migration: mechanisms of rear detachment and the formation of migration tracks. Eur J Cell Biol 2004; 83:717-24; PMID:15679116; http://dx.doi.org/10.1078/0171- 9335-00421.
2. Pollard TD, Borisy GG. Cellular motility driven by assembly and disassembly of actin filaments. Cell 2003; 112:453-65; PMID:12600310; http://dx.doi. org/10.1016/S0092-8674(03)00120-X.
3. Mallavarapu A, Mitchison T. Regulated actin cytoskeleton assembly at filopodium tips controls their extension and retraction. J Cell Biol 1999; 146:1097- 106; PMID:10477762; http://dx.doi.org/10.1083/ jcb.146.5.1097.
4. Vignjevic D, Kojima S, Aratyn Y, Danciu O, Svitkina T, Borisy GG. Role of fascin in filopodial protrusion. J Cell Biol 2006; 174:863-75; PMID:16966425; http:// dx.doi.org/10.1083/jcb.200603013.
5. Partridge MA, Marcantonio EE. Initiation of attachment and generation of mature focal adhesions by integrin-containing filopodia in cell spreading. Mol Biol Cell 2006; 17:4237-48; PMID:16855018; http:// dx.doi.org/10.1091/mbc.E06- 06-0496.
6. Schäfer C, Borm B, Born S, Mohl C, Eibl EM, Hoffmann B. One step ahead: role of filopodia in adhesion formation during cell migration of keratinocytes. Exp Cell Res 2009; 315:1212-24; PMID:19100734; http://dx.doi.org/10.1016/j.yexcr.2008.11.008.
7. Schäfer C, Born S, Mohl C, Houben S, Kirchgessner N, Merkel R, et al. The key feature for early migratory processes: Dependence of adhesion, actin bundles, force generation and transmission on filopodia. Cell Adh Migr 2010; 4:215-25; PMID:20179423; http:// dx.doi.org/10.4161/cam.4.2.10745.
8. Nemethova M, Auinger S, Small JV. Building the actin cytoskeleton: filopodia contribute to the construction of contractile bundles in the lamella. J Cell Biol 2008; 180:1233-44; PMID:18362182; http://dx.doi. org/10.1083/jcb.200709134.
9. Zaidel-Bar R, Itzkovitz S, Ma'ayan A, Iyengar R, Geiger B. Functional atlas of the integrin adhesome. Nat Cell Biol 2007; 9:858-67; PMID:17671451; http://dx.doi. org/10.1038/ncb0807-858.
10. Wolfenson H, Bershadsky A, Henis YI, Geiger B. Actomyosin-generated tension controls the molecular kinetics of focal adhesions. J Cell Sci 2011; 124:1425- 32; PMID:21486952; http://dx.doi.org/10.1242/ jcs.077388.
11. Parsons JT, Horwitz AR, Schwartz MA. Cell adhesion: integrating cytoskeletal dynamics and cellular tension. Nat Rev Mol Cell Biol 2010; 11:633-43; PMID:20729930; http://dx.doi.org/10.1038/ nrm2957.
12. Cohen DM, Kutscher B, Chen H, Murphy DB, Craig SW. A conformational switch in vinculin drives formation and dynamics of a talin-vinculin complex at focal adhesions. J Biol Chem 2006; 281:16006- 15; PMID:16608855; http://dx.doi.org/10.1074/jbc. M600738200.
13. Vicente-Manzanares M, Koach MA, Whitmore L, Lamers ML, Horwitz AF. Segregation and activation of myosin IIB creates a rear in migrating cells. J Cell Biol 2008; 183:543-54; PMID:18955554; http://dx.doi. org/10.1083/jcb. 200806030.
14. Totsukawa G, Yamakita Y, Yamashiro S, Hartshorne DJ, Sasaki Y, Matsumura F. Distinct roles of ROCK (Rho-kinase) and MLCK in spatial regulation of MLC phosphorylation for assembly of stress fibers and focal adhesions in 3T3 fibroblasts. J Cell Biol 2000; 150:797-806; PMID:10953004; http://dx.doi. org/10.1083/jcb.150.4.797.
15. Totsukawa G, Wu Y, Sasaki Y, Hartshorne DJ, Yamakita Y, Yamashiro S, et al. Distinct roles of MLCK and ROCK in the regulation of membrane protrusions and focal adhesion dynamics during cell migration of fibroblasts. J Cell Biol 2004; 164:427-39; PMID:14757754; http://dx.doi.org/10.1083/jcb.200306172.
16. Ford HL, Salim MM, Chakravarty R, Aluiddin V, Zain SB. Expression of Mts1, a metastasis-associated gene, increases motility but not invasion of a nonmetastatic mouse mammary adenocarcinoma cell line. Oncogene 1995; 11:2067-75; PMID:7478526.
17. Ford HL, Silver DL, Kachar B, Sellers JR, Zain SB. Effect of Mts1 on the structure and activity of nonmuscle myosin II. Biochemistry 1997; 36:16321- 7; PMID:9405067; http://dx.doi.org/10.1021/ bi971182l.
18. Kriajevska MV, Cardenas MN, Grigorian MS, Ambartsumian NS, Georgiev GP, Lukanidin EM. Non-muscle myosin heavy chain as a possible target for protein encoded by metastasis-related mts-1 gene. J Biol Chem 1994; 269:19679-82; PMID:8051043.
19. Zhang S, Wang G, Fernig DG, Rudland PS, Webb SE, Barraclough R, et al. Interaction of metastasis-inducing S100A4 protein in vivo by fluorescence lifetime imaging microscopy. Eur Biophys J 2005; 34:19-27; PMID:15289939; http://dx.doi.org/10.1007/s00249- 004-0428-x.
20. Li ZH, Spektor A, Varlamova O, Bresnick AR. Mts1 regulates the assembly of nonmuscle myosin-IIA. Biochemistry 2003; 42:14258-66; PMID:14640694; http://dx.doi.org/10.1021/bi0354379.
21. Dulyaninova NG, Malashkevich VN, Almo SC, Bresnick AR. Regulation of myosin-IIA assembly and Mts1 binding by heavy chain phosphorylation. Biochemistry 2005; 44:6867-76; PMID:15865432; http://dx.doi.org/10.1021/ bi0500776.
22. Jenkinson SR, Barraclough R, West CR, Rudland PS. S100A4 regulates cell motility and invasion in an in vitro model for breast cancer metastasis. Br J Cancer 2004; 90:253-62; PMID:14710237; http://dx.doi. org/10.1038/sj.bjc. 6601483.
23. Li ZH, Bresnick AR. The S100A4 metastasis factor regulates cellular motility via a direct interaction with myosin-IIA. Cancer Res 2006; 66:5173-80; PMID:16707441; http://dx.doi.org/10.1158/0008-.CAN-05-3087.
24. Ismail TM, Fernig DG, Rudland PS, Terry CJ, Wang G, Barraclough R. The basic C-terminal amino acids of calcium-binding protein S100A4 promote metastasis. Carcinogenesis 2008; 29:2259-66; PMID:18784356; http://dx.doi.org/ 10.1093/carcin/bgn217.
25. Ismail TM, Zhang S, Fernig DG, Gross S, Martin- Fernandez ML, See V, et al. Self-association of calciumbinding protein S100A4 and metastasis. J Biol Chem 2010; 285:914-22; PMID:19917604; http://dx.doi. org/10.1074/jbc.M109. 010892.
26. Helfman DM, Kim EJ, Lukanidin E, Grigorian M. The metastasis associated protein S100A4: role in tumour progression and metastasis. Br J Cancer 2005; 92:1955-8; PMID:15900299; http://dx.doi. org/10.1038/sj.bjc.6602613.
27. Rudland PS, Platt-Higgins A, El-Tanani M, De Silva Rudland S, Barraclough R, Winstanley JH, et al. Prognostic significance of the metastasis-associated protein osteopontin in human breast cancer. Cancer Res 2002; 62:3417-27; PMID:12067984.
28. Davies BR, Davies MP, Gibbs FE, Barraclough R, Rudland PS. Induction of the metastatic phenotype by transfection of a benign rat mammary epithelial cell line with the gene for p9Ka, a rat calcium-binding protein, but not with the oncogene EJ-ras-1. Oncogene 1993; 8:999-1008; PMID:8455951.
29. Lloyd BH, Platt-Higgins A, Rudland PS, Barraclough R. Human S100A4 (p9Ka) induces the metastatic phenotype upon benign tumour cells. Oncogene 1998; 17:465-73; PMID:9696040; http://dx.doi. org/10.1038/sj.onc.1201948.
30. Zhang S, Wang G, Liu D, Bao Z, Fernig DG, Rudland PS, et al. The C-terminal region of S100A4 is important for its metastasis-inducing properties. Oncogene 2005; 24:4401-11; PMID:15856021; http://dx.doi. org/10.1038/sj.onc. 1208663.
31. Dunnington DJ, Hughes CM, Monaghan P, Rudland PS. Phenotypic instability of rat mammary tumor epithelial cells. J Natl Cancer Inst 1983; 71:1227-40; PMID:6418941.
32. Andersen K, Nesland JM, Holm R, Florenes VA, Fodstad O, Maelandsmo GM. Expression of S100A4 combined with reduced E-cadherin expression predicts patient outcome in malignant melanoma. Mod Pathol 2004; 17:990-7; PMID:15133476; http://dx.doi. org/10.1038/modpathol.3800151.
33. Kimura K, Endo Y, Yonemura Y, Heizmann CW, Schafer BW, Watanabe Y, et al. Clinical significance of S100A4 and E-cadherin-related adhesion molecules in non-small cell lung cancer. Int J Oncol 2000; 16:1125- 31; PMID:10811984.
34. Rudland PS, Platt-Higgins A, Renshaw C, West CR, Winstanley JH, Robertson L, et al. Prognostic significance of the metastasis-inducing protein S100A4 (p9Ka) in human breast cancer. Cancer Res 2000; 60:1595-603; PMID:10749128.
35. Yonemura Y, Endou Y, Kimura K, Fushida S, Bandou E, Taniguchi K, et al. Inverse expression of S100A4 and E-cadherin is associated with metastatic potential in gastric cancer. Clin Cancer Res 2000; 6:4234-42; PMID:11106237.
36. Ambartsumian NS, Grigorian MS, Larsen IF, Karlstrom O, Sidenius N, Rygaard J, et al. Metastasis of mammary carcinomas in GRS/A hybrid mice transgenic for the mts1 gene. Oncogene 1996; 13:1621-30; PMID:8895507.
37. Takenaga K, Nakamura Y, Endo H, Sakiyama S. Involvement of S100-related calcium-binding protein pEL98 (or mts1) in cell motility and tumor cell invasion. Jpn J Cancer Res 1994; 85:831-9; PMID:7928629.
38. Takenaga K, Nakamura Y, Sakiyama S. Expression of antisense RNA to S100A4 gene encoding an S100- related calcium-binding protein suppresses metastatic potential of high-metastatic Lewis lung carcinoma cells. Oncogene 1997; 14:331-7; PMID:9018119; http:// dx.doi.org/10.1038/sj.onc.1200820.
39. Bjørnland K, Winberg JO, Odegaard OT, Hovig E, Loennechen T, Aasen AO, et al. S100A4 involvement in metastasis: deregulation of matrix metalloproteinases and tissue inhibitors of matrix metalloproteinases in osteosarcoma cells transfected with an anti-S100A4 ribozyme. Cancer Res 1999; 59:4702-8; PMID:10493528.
40. Kim EJ, Helfman DM. Characterization of the metastasis-associated protein, S100A4. Roles of calcium binding and dimerization in cellular localization and interaction with myosin. J Biol Chem 2003; 278:30063-73; PMID:12756252; http://dx.doi. org/10.1074/jbc.M304909200.
41. Hotulainen P, Lappalainen P. Stress fibers are generated by two distinct actin assembly mechanisms in motile cells. J Cell Biol 2006; 173:383-94; PMID:16651381; http://dx.doi.org/10.1083/jcb.200511093.
42. Medeiros NA, Burnette DT, Forscher P. Myosin II functions in actin-bundle turnover in neuronal growth cones. Nat Cell Biol 2006; 8:216-26; PMID:16501565; http://dx.doi.org/10.1038/ncb1367.
43. Betapudi V. Myosin II motor proteins with different functions determine the fate of lamellipodia extension during cell spreading. PLoS ONE 2010; 5:8560; PMID:20052411; http://dx.doi.org/10.1371/journal. pone.0008560.
44. Tokuo H, Mabuchi K, Ikebe M. The motor activity of myosin-X promotes actin fiber convergence at the cell periphery to initiate filopodia formation. J Cell Biol 2007; 179:229-38; PMID:17954606; http://dx.doi. org/10.1083/jcb. 200703178.
45. Schäfer C, Born S, Mohl C, Houben S, Kirchgessner N, Merkel R, et al. The key feature for early migratory processes: Dependence of adhesion, actin bundles, force generation and transmission on filopodia. Cell Adh Migr 2010; 4:215-25; PMID:20179423; http:// dx.doi.org/10.4161/cam.4.2.10745.
46. Takenaga K, Nakamura Y, Sakiyama S, Hasegawa Y, Sato K, Endo H. Binding of pEL98 protein, an S100-related calcium-binding protein, to nonmuscle tropomyosin. J Cell Biol 1994; 124:757- 68; PMID:8120097; http://dx.doi.org/10. 1083/ jcb.124.5.757.
47. Watanabe Y, Usada N, Minami H, Morita T, Tsugane S, Ishikawa R, et al. Calvasculin, as a factor affecting the microfilament assemblies in rat fibroblasts transfected by src gene. FEBS Lett 1993; 324:51-5; PMID:8504859; http://dx.doi.org/10.1016/0014- 5793(93)81530-D
48. Creed SJ, Desouza M, Bamburg JR, Gunning P, Stehn J. Tropomyosin isoform 3 promotes the formation of filopodia by regulating the recruitment of actinbinding proteins to actin filaments. Exp Cell Res 2011; 317:249-61; PMID:21036167; http://dx.doi. org/10.1016/j.yexcr.2010.10.019.
49. Gupton SL, Anderson KL, Kole TP, Fischer RS, Ponti A, Hitchcock-DeGregori SE, et al. Cell migration without a lamellipodium: translation of actin dynamics into cell movement mediated by tropomyosin. J Cell Biol 2005; 168:619-31; PMID:15716379; http://dx.doi. org/10.1083/jcb.200406063.
50. Bach CT, Schevzov G, Bryce NS, Gunning PW, O'Neill GM. Tropomyosin isoform modulation of focal adhesion structure and cell migration. Cell Adh Migr 2010; 4:226-34; PMID:20305380; http://dx.doi. org/10.4161/cam.4.2.10888.