Hic-5 promotes invadopodia formation and invasion during TGF-β-induced epithelial-mesenchymal transition

Journal of Cell Biology

Volumn 197, Issue 3, 2012, Pages 421-437

  Pignatelli, Jeanine ^a   Tumbarello, David A ^a,b   Schmidt, Ronald P ^a   Turner, Christopher E ^a  

^a SUNY UPSTATE MEDICAL UNIVERSITY   (United States)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN; PROTEIN HIC 5; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; CYTOSKELETON PROTEIN; DNA BINDING PROTEIN; LIM PROTEIN; PROTEIN TYROSINE KINASE; SMALL INTERFERING RNA; TGFB1I1 PROTEIN, MOUSE;

ARTICLE; CELL INVASION; CELL MIGRATION; CONTROLLED STUDY; EPITHELIAL MESENCHYMAL TRANSITION; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; ANIMAL; BREAST; CELL ADHESION; CELL CULTURE; CELL MOTION; CELL SURFACE; DRUG ANTAGONISM; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PHYSIOLOGY; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; BREAST; CELL ADHESION; CELL MOVEMENT; CELL SURFACE EXTENSIONS; CELLS, CULTURED; CYTOSKELETAL PROTEINS; DNA-BINDING PROTEINS; EPITHELIAL-MESENCHYMAL TRANSITION; EXTRACELLULAR MATRIX; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; HUMANS; LIM DOMAIN PROTEINS; MICE; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; RHOA GTP-BINDING PROTEIN; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; TRANSFORMING GROWTH FACTOR BETA;

EID: 84862629472     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201108143     Document Type: Article

References (65)

1. Albiges-Rizo, C., O. Destaing, B. Fourcade, E. Planus, and M.R. Block. 2009. Actin machinery and mechanosensitivity in invadopodia, podosomes and focal adhesions. J. Cell Sci. 122:3037-3049. http://dx.doi.org/10.1242/jcs.052704
2. Alexander, N.R., K.M. Branch, A. Parekh, E.S. Clark, I.C. Iwueke, S.A. Guelcher, and A.M. Weaver. 2008. Extracellular matrix rigidity promotes invadopodia activity. Curr. Biol. 18:1295-1299. http://dx.doi.org/10.1016/j.cub.2008.07.090
3. Badowski, C., G. Pawlak, A. Grichine, A. Chabadel, C. Oddou, P. Jurdic, M. Pfaff, C. Albigès-Rizo, and M.R. Block. 2008. Paxillin phosphorylation controls invadopodia/podosomes spatiotemporal organization. Mol. Biol. Cell. 19:633-645. http://dx.doi.org/10.1091/mbc.E06-01-0088
4. Bakin, A.V., C. Rinehart, A.K. Tomlinson, and C.L. Arteaga. 2002. p38 mitogenactivated protein kinase is required for TGFbeta-mediated fibroblastic transdifferentiation and cell migration. J. Cell Sci. 115:3193-3206.
5. Bellovin, D.I., K.J. Simpson, T. Danilov, E. Maynard, D.L. Rimm, P. Oettgen, and A.M. Mercurio. 2006. Reciprocal regulation of RhoA and RhoC characterizes the EMT and identifies RhoC as a prognostic marker of colon carcinoma. Oncogene. 25:6959-6967. http://dx.doi.org/10.1038/sj.onc.1209682
6. Bharti, S., H. Inoue, K. Bharti, D.S. Hirsch, Z. Nie, H.Y. Yoon, V. Artym, K.M. Yamada, S.C. Mueller, V.A. Barr, and P.A. Randazzo. 2007. Src-dependent phosphorylation of ASAP1 regulates podosomes. Mol. Cell. Biol. 27: 8271-8283. http://dx.doi.org/10.1128/MCB.01781-06
7. Bhowmick, N.A., M. Ghiassi, A. Bakin, M. Aakre, C.A. Lundquist, M.E. Engel, C.L. Arteaga, and H.L. Moses. 2001a. Transforming growth factor-beta1 mediates epithelial to mesenchymal transdifferentiation through a RhoA-dependent mechanism. Mol. Biol. Cell. 12:27-36.
8. Bhowmick, N.A., R. Zent, M. Ghiassi, M. McDonnell, and H.L. Moses. 2001b. Integrin beta 1 signaling is necessary for transforming growth factorbeta activation of p38MAPK and epithelial plasticity. J. Biol. Chem. 276:46707-46713. http://dx.doi.org/10.1074/jbc.M106176200
9. Bowden, E.T., P.J. Coopman, and S.C. Mueller. 2001. Invadopodia: unique methods for measurement of extracellular matrix degradation in vitro. Methods Cell Biol. 63:613-627. http://dx.doi.org/10.1016/S0091-679X(01)63033-4
10. Bowden, E.T., E. Onikoyi, R. Slack, A. Myoui, T. Yoneda, K.M. Yamada, and S.C. Mueller. 2006. Co-localization of cortactin and phosphotyrosine identifies active invadopodia in human breast cancer cells. Exp. Cell Res. 312:1240-1253. http://dx.doi.org/10.1016/j.yexcr.2005.12.012
11. Bravo-Cordero, J.J., M. Oser, X. Chen, R. Eddy, L. Hodgson, and J. Condeelis. 2011. A novel spatiotemporal RhoC activation pathway locally regulates cofilin activity at invadopodia. Curr. Biol. 21:635-644. http://dx.doi.org/10.1016/j.cub.2011.03.039
12. Brown, M.C., and C.E. Turner. 2004. Paxillin: adapting to change. Physiol. Rev. 84:1315-1339. http://dx.doi.org/10.1152/physrev.00002.2004
13. Buccione, R., G. Caldieri, and I. Ayala. 2009. Invadopodia: specialized tumor cell structures for the focal degradation of the extracellular matrix. Cancer Metastasis Rev. 28:137-149. http://dx.doi.org/10.1007/s10555-008-9176-1
14. Buschman, M.D., P.A. Bromann, P. Cejudo-Martin, F. Wen, I. Pass, and S.A. Courtneidge. 2009. The novel adaptor protein Tks4 (SH3PXD2B) is required for functional podosome formation. Mol. Biol. Cell. 20:1302-1311. http://dx.doi.org/10.1091/mbc.E08-09-0949
15. Cary, L.A., R.A. Klinghoffer, C. Sachsenmaier, and J.A. Cooper. 2002. SRC catalytic but not scaffolding function is needed for integrin-regulated tyrosine phosphorylation, cell migration, and cell spreading. Mol. Cell. Biol. 22:2427-2440. http://dx.doi.org/10.1128/MCB.22.8.2427-2440.2002
16. Cheng, J.C., C. Klausen, and P.C. Leung. 2010. Hydrogen peroxide mediates EGF-induced down-regulation of E-cadherin expression via p38 MAPK and snail in human ovarian cancer cells. Mol. Endocrinol. 24:1569-1580. http://dx.doi.org/10.1210/me.2010-0034
17. Christiansen, J.J., and A.K. Rajasekaran. 2006. Reassessing epithelial to mesenchymal transition as a prerequisite for carcinoma invasion and metastasis. Cancer Res. 66:8319-8326. http://dx.doi.org/10.1158/0008-5472.CAN-06-0410
18. Cicchini, C., I. Laudadio, F. Citarella, M. Corazzari, C. Steindler, A. Conigliaro, A. Fantoni, L. Amicone, and M. Tripodi. 2008. TGFbeta-induced EMT requires focal adhesion kinase (FAK) signaling. Exp. Cell Res. 314:143-152. http://dx.doi.org/10.1016/j.yexcr.2007.09.005
19. Clark, E.A., T.R. Golub, E.S. Lander, and R.O. Hynes. 2000. Genomic analysis of metastasis reveals an essential role for RhoC. Nature. 406:532-535. http://dx.doi.org/10.1038/35020106
20. Dabiri, G., D.A. Tumbarello, C.E. Turner, and L. Van de Water. 2008. Hic-5 promotes the hypertrophic scar myofibroblast phenotype by regulating the TGF-beta1 autocrine loop. J. Invest. Dermatol. 128:2518-2525. http://dx.doi.org/10.1038/jid.2008.90
21. Davies, M., M. Robinson, E. Smith, S. Huntley, S. Prime, and I. Paterson. 2005. Induction of an epithelial to mesenchymal transition in human immortal and malignant keratinocytes by TGF-beta1 involves MAPK, Smad and AP-1 signalling pathways. J. Cell. Biochem. 95:918-931. http://dx.doi.org/10.1002/jcb.20458
22. Deakin, N.O., and C.E. Turner. 2008. Paxillin comes of age. J. Cell Sci. 121:2435-2444. http://dx.doi.org/10.1242/jcs.018044
23. Deakin, N.O., and C.E. Turner. 2011. Distinct roles for paxillin and Hic-5 in regulating breast cancer cell morphology, invasion, and metastasis. Mol. Biol. Cell. 22:327-341. http://dx.doi.org/10.1091/mbc.E10-09-0790
24. Destaing, O., M.R. Block, E. Planus, and C. Albiges-Rizo. 2011. Invadosome regulation by adhesion signaling. Curr. Opin. Cell Biol. 23:597-606. http://dx.doi.org/10.1016/j.ceb.2011.04.002
25. Dumont, N., and C.L. Arteaga. 2000. Transforming growth factor-beta and breast cancer: Tumor promoting effects of transforming growth factorbeta. Breast Cancer Res. 2:125-132. http://dx.doi.org/10.1186/bcr44
26. Fujimoto, N., S. Yeh, H.Y. Kang, S. Inui, H.C. Chang, A. Mizokami, and C. Chang. 1999. Cloning and characterization of androgen receptor coactivator, ARA55, in human prostate. J. Biol. Chem. 274:8316-8321. http://dx.doi.org/10.1074/jbc.274.12.8316
27. Fujita, H., K. Kamiguchi, D. Cho, M. Shibanuma, C. Morimoto, and K. Tachibana. 1998. Interaction of Hic-5, A senescence-related protein, with focal adhesion kinase. J. Biol. Chem. 273:26516-26521. http://dx.doi.org/10.1074/jbc.273.41.26516
28. Gimona, M., and R. Buccione. 2006. Adhesions that mediate invasion. Int. J. Biochem. Cell Biol. 38:1875-1892. http://dx.doi.org/10.1016/j.biocel.2006.05.003
29. Head, J.A., D. Jiang, M. Li, L.J. Zorn, E.M. Schaefer, J.T. Parsons, and S.A. Weed. 2003. Cortactin tyrosine phosphorylation requires Rac1 activity and association with the cortical actin cytoskeleton. Mol. Biol. Cell. 14:3216-3229. http://dx.doi.org/10.1091/mbc.E02-11-0753
30. Hetey, S.E., D.P. Lalonde, and C.E. Turner. 2005. Tyrosine-phosphorylated Hic-5 inhibits epidermal growth factor-induced lamellipodia formation. Exp. Cell Res. 311:147-156. http://dx.doi.org/10.1016/j.yexcr.2005.08.011
31. Hutchison, N., B.M. Hendry, and C.C. Sharpe. 2009. Rho isoforms have distinct and specific functions in the process of epithelial to mesenchymal transition in renal proximal tubular cells. Cell. Signal. 21:1522-1531. http://dx.doi.org/10.1016/j.cellsig.2009.05.012
32. Ishino, M., H. Aoto, H. Sasaski, R. Suzuki, and T. Sasaki. 2000. Phosphorylation of Hic-5 at tyrosine 60 by CAKbeta and Fyn. FEBS Lett. 474:179-183. http://dx.doi.org/10.1016/S0014-5793(00)01597-0
33. Kim, E.S., M.S. Kim, and A. Moon. 2004. TGF-beta-induced upregulation of MMP-2 and MMP-9 depends on p38 MAPK, but not ERK signaling in MCF10A human breast epithelial cells. Int. J. Oncol. 25:1375-1382.
34. Kim, E.S., M.S. Kim, and A. Moon. 2005. Transforming growth factor (TGF)-beta in conjunction with H-ras activation promotes malignant progression of MCF10A breast epithelial cells. Cytokine. 29:84-91. http://dx.doi.org/10.1016/j.cyto.2004.10.001
35. Legate, K.R., E. Montañez, O. Kudlacek, and R. Fässler. 2006. ILK, PINCH and parvin: the tIPP of integrin signalling. Nat. Rev. Mol. Cell Biol. 7:20-31. http://dx.doi.org/10.1038/nrm1789
36. Linder, S. 2007. The matrix corroded: podosomes and invadopodia in extracellular matrix degradation. Trends Cell Biol. 17:107-117. http://dx.doi.org/10.1016/j.tcb.2007.01.002
37. Linder, S. 2009. Invadosomes at a glance. J. Cell Sci. 122:3009-3013. http://dx.doi.org/10.1242/jcs.032631
38. Linder, S., D. Nelson, M. Weiss, and M. Aepfelbacher. 1999. Wiskott-Aldrich syndrome protein regulates podosomes in primary human macrophages. Proc. Natl. Acad. Sci. USA. 96:9648-9653. http://dx.doi.org/10.1073/pnas.96.17.9648
39. Litvinov, I.V., L. Antony, S.L. Dalrymple, R. Becker, L. Cheng, and J.T. Isaacs. 2006. PC3, but not DU145, human prostate cancer cells retain the coregulators required for tumor suppressor ability of androgen receptor. Prostate. 66:1329-1338. http://dx.doi.org/10.1002/pros.20483
40. Loesch, M., H.Y. Zhi, S.W. Hou, X.M. Qi, R.S. Li, Z. Basir, T. Iftner, A. Cuenda, and G. Chen. 2010. p38gamma MAPK cooperates with c-Jun in transactivating matrix metalloproteinase 9. J. Biol. Chem. 285:15149-15158. http://dx.doi.org/10.1074/jbc.M110.105429
41. Mandal, S., K.R. Johnson, and M.J. Wheelock. 2008. TGF-beta induces formation of F-actin cores and matrix degradation in human breast cancer cells via distinct signaling pathways. Exp. Cell Res. 314:3478-3493. http://dx.doi.org/10.1016/j.yexcr.2008.09.013
42. Matsuya, M., H. Sasaki, H. Aoto, T. Mitaka, K. Nagura, T. Ohba, M. Ishino, S. Takahashi, R. Suzuki, and T. Sasaki. 1998. Cell adhesion kinase beta forms a complex with a new member, Hic-5, of proteins localized at focal adhesions. J. Biol. Chem. 273:1003-1014. http://dx.doi.org/10.1074/jbc.273.2.1003
43. Miyoshi, Y., H. Ishiguro, H. Uemura, K. Fujinami, H. Miyamoto, Y. Miyoshi, H. Kitamura, and Y. Kubota. 2003. Expression of AR associated protein 55 (ARA55) and androgen receptor in prostate cancer. Prostate. 56:280-286. http://dx.doi.org/10.1002/pros.10262
44. Munshi, H.G., Y.I. Wu, S. Mukhopadhyay, A.J. Ottaviano, A. Sassano, J.E. Koblinski, L.C. Platanias, and M.S. Stack. 2004. Differential regulation of membrane type 1-matrix metalloproteinase activity by ERK 1/2- and p38 MAPK-modulated tissue inhibitor of metalloproteinases 2 expression controls transforming growth factor-beta1-induced pericellular collagenolysis. J. Biol. Chem. 279:39042-39050. http://dx.doi.org/10.1074/jbc.M404958200
45. Nakamura, K., H. Yano, H. Uchida, S. Hashimoto, E. Schaefer, and H. Sabe. 2000. Tyrosine phosphorylation of paxillin alpha is involved in temporospatial regulation of paxillin-containing focal adhesion formation and F-actin organization in motile cells. J. Biol. Chem. 275:27155-27164.
46. Nikolopoulos, S.N., and C.E. Turner. 2000. Actopaxin, a new focal adhesion protein that binds paxillin LD motifs and actin and regulates cell adhesion. J. Cell Biol. 151:1435-1448. http://dx.doi.org/10.1083/jcb.151.7.1435
47. Pankov, R., Y. Endo, S. Even-Ram, M. Araki, K. Clark, E. Cukierman, K. Matsumoto, and K.M. Yamada. 2005. A Rac switch regulates random versus directionally persistent cell migration. J. Cell Biol. 170:793-802. http://dx.doi.org/10.1083/jcb.200503152
48. Parekh, A., and A.M. Weaver. 2009. Regulation of cancer invasiveness by the physical extracellular matrix environment. Cell Adh. Migr. 3:288-292. http://dx.doi.org/10.4161/cam.3.3.8888
49. Provenzano, P.P., and P.J. Keely. 2009. The role of focal adhesion kinase in tumor initiation and progression. Cell Adh. Migr. 3:347-350. http://dx.doi.org/10.4161/cam.3.4.9458
50. Sahai, E., and C.J. Marshall. 2002. RHO-GTPases and cancer. Nat. Rev. Cancer. 2:133-142. http://dx.doi.org/10.1038/nrc725
51. Sakurai-Yageta, M., C. Recchi, G. Le Dez, J.B. Sibarita, L. Daviet, J. Camonis, C. D'Souza-Schorey, and P. Chavrier. 2008. The interaction of IQGAP1 with the exocyst complex is required for tumor cell invasion downstream of Cdc42 and RhoA. J. Cell Biol. 181:985-998. http://dx.doi.org/10.1083/jcb.200709076
52. Schmalhofer, O., S. Brabletz, and T. Brabletz. 2009. E-cadherin, beta-catenin, and ZEB1 in malignant progression of cancer. Cancer Metastasis Rev. 28:151-166. http://dx.doi.org/10.1007/s10555-008-9179-y
53. Sebe, A., A. Masszi, M. Zulys, T. Yeung, P. Speight, O.D. Rotstein, H. Nakano, I. Mucsi, K. Szászi, and A. Kapus. 2008. Rac, PAK and p38 regulate cell contact-dependent nuclear translocation of myocardinrelated transcription factor. FEBS Lett. 582:291-298. http://dx.doi.org/10.1016/j.febslet.2007.12.021
54. Shibanuma, M., J. Mashimo, T. Kuroki, and K. Nose. 1994. Characterization of the TGF beta 1-inducible hic-5 gene that encodes a putative novel zinc finger protein and its possible involvement in cellular senescence. J. Biol. Chem. 269:26767-26774.
55. Shibanuma, M., E. Mochizuki, R. Maniwa, J. Mashimo, N. Nishiya, S. Imai, T. Takano, M. Oshimura, and K. Nose. 1997. Induction of senescencelike phenotypes by forced expression of hic-5, which encodes a novel LIM motif protein, in immortalized human fibroblasts. Mol. Cell. Biol. 17:1224-1235.
56. Thiery, J.P., H. Acloque, R.Y. Huang, and M.A. Nieto. 2009. Epithelialmesenchymal transitions in development and disease. Cell. 139:871-890. http://dx.doi.org/10.1016/j.cell.2009.11.007
57. Thomas, S.M., M. Hagel, and C.E. Turner. 1999. Characterization of a focal adhesion protein, Hic-5, that shares extensive homology with paxillin. J. Cell Sci. 112:181-190.
58. Tian, M., J.R. Neil, and W.P. Schiemann. 2011. Transforming growth factor-β and the hallmarks of cancer. Cell. Signal. 23:951-962. http://dx.doi.org/10.1016/j.cellsig.2010.10.015
59. Tumbarello, D.A., and C.E. Turner. 2007. Hic-5 contributes to epithelialmesenchymal transformation through a RhoA/ROCK-dependent pathway. J. Cell. Physiol. 211:736-747. http://dx.doi.org/10.1002/jcp.20991
60. Tumbarello, D.A., M.C. Brown, S.E. Hetey, and C.E. Turner. 2005. Regulation of paxillin family members during epithelial-mesenchymal transformation: a putative role for paxillin delta. J. Cell Sci. 118:4849-4863. http://dx.doi.org/10.1242/jcs.02615
61. Wendt, M.K., and W.P. Schiemann. 2009. Therapeutic targeting of the focal adhesion complex prevents oncogenic TGF-beta signaling and metastasis. Breast Cancer Res. 11:R68. http://dx.doi.org/10.1186/bcr2360
62. Wendt, M.K., J.A. Smith, and W.P. Schiemann. 2010. Transforming growth factor-β-induced epithelial-mesenchymal transition facilitates epidermal growth factor-dependent breast cancer progression. Oncogene. 29:6485-6498. http://dx.doi.org/10.1038/onc.2010.377
63. Wickström, S.A., A. Lange, E. Montanez, and R. Fässler. 2010. The ILK/PINCH/parvin complex: the kinase is dead, long live the pseudokinase! EMBO J. 29:281-291. http://dx.doi.org/10.1038/emboj.2009.376
64. Xu, J., S. Lamouille, and R. Derynck. 2009. TGF-beta-induced epithelial to mesenchymal transition. Cell Res. 19:156-172. http://dx.doi.org/10.1038/cr.2009.5
65. Yilmaz, M., and G. Christofori. 2009. EMT, the cytoskeleton, and cancer cell invasion. Cancer Metastasis Rev. 28:15-33. http://dx.doi.org/10.1007/s10555-008-9169-0