Functional role of α-actinin, Pl 3-kinase and MEK1/2 in insulin-like growth factor I receptor kinase regulated motility of human breast carcinoma cells

Journal of Cell Science

Volumn 115, Issue 21, 2002, Pages 4149-4165

  Guvakova, Marina A ^a   Adams, Josephine C ^b,c   Bettiger, David ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c LERNER RESEARCH INSTITUTE   (United States)

Author keywords

actinin; Actin cytoskeleton; Breast cancer cell migration; IGF IR signaling

Indexed keywords

ACTIN; ALPHA ACTININ; GREEN FLUORESCENT PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MUTANT PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHOLIPID; PHOSPHOTRANSFERASE; SOMATOMEDIN C RECEPTOR; ACTININ; DIAGNOSTIC AGENT; HYBRID PROTEIN; MAP2K1 PROTEIN, HUMAN; MITOGEN ACTIVATED PROTEIN KINASE KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; PHOTOPROTEIN; PROTEIN SERINE THREONINE KINASE; SOMATOMEDIN C;

AMINO TERMINAL SEQUENCE; BREAST CARCINOGENESIS; BREAST CARCINOMA; BREAST DEVELOPMENT; CARBOXY TERMINAL SEQUENCE; CARCINOMA CELL; CELL CONTACT; CELL JUNCTION; CELL MIGRATION; CELL MOTILITY; CELL SEPARATION; CHEMICAL LABELING; CONTROLLED STUDY; ENZYME ACTIVITY; GENE DELETION; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION; SPIKE; ARTICLE; BREAST TUMOR; CARCINOMA; CELL ADHESION; CELL COMMUNICATION; CELL CULTURE; CELL MOTION; DRUG EFFECT; ELECTRON MICROSCOPY; ENZYMOLOGY; EPITHELIUM CELL; FEMALE; GENETICS; METABOLISM; METASTASIS; PROTEIN TERTIARY STRUCTURE; PSEUDOPODIUM; ULTRASTRUCTURE;

MINK CELL FOCUS-FORMING VIRUS;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ACTININ; ACTINS; BREAST NEOPLASMS; CARCINOMA; CELL ADHESION; CELL COMMUNICATION; CELL MOVEMENT; EPITHELIAL CELLS; FEMALE; GREEN FLUORESCENT PROTEINS; HUMANS; INSULIN-LIKE GROWTH FACTOR I; INTERCELLULAR JUNCTIONS; LUMINESCENT PROTEINS; MAP KINASE KINASE 1; MICROSCOPY, ELECTRON; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; NEOPLASM METASTASIS; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; PSEUDOPODIA; RECEPTOR, IGF TYPE 1; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; TUMOR CELLS, CULTURED;

EID: 1842833905     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.00104     Document Type: Review

References (76)

1. Andre, F., Rigot, V., Remacle-Bonnet, M., Luis, J., Pommier, G. and Marvaldi, J. (1999). Protein kinase C-gamma and -delta are involved in insulin-like growth factor I-induced migration of colonic epithelial cells. Gastroenterology 116, 64-77.
2. Baron, M. D., Davison, M. D., Jones, P. and Critchley, D. R. (1987). The sequence of chick α-actinin reveals homologies to spectrin and calmodulin. J. Biol. Chem. 262, 17623-17629.
3. Baserga, R. (1999). The IGF-I receptor in cancer research. Exp. Cell Res. 253, 1-6.
4. Boyer, B. and Thiery, J.-P. (1993). Epithelium-mesenchyme interconversions as example of epithelial plasticity. APMIS 101, 257-268.
5. Chausovsky, A., Tsarfaty, I., Kam, Z., Yarden, Y., Geiger, B. and Bershadsky, A. D. (1998). Morphogenetic effects of neuregulin (neu differentiation factor) in cultured epithelial cells. Mol. Biol. Cell 9, 3195-3209.
6. Chernicky, C. L., Yi, L., Tan, H., Gan, S. U. and Ilan, J. (2000). Treatment of human breast cancer cells with antisense RNA to the type I insulin-like growth receptor inhibits cell growth, suppresses tumorigenesis, alters the metastatic potential, and prolongs survival in vivo. Cancer Gene Ther. 7, 384-395.
7. Christerson, L. B., Vanderbilt, C. A. and Cobb, M. H. (1999). MEKK1 interacts with alpha-actinin and localizes to stress fibers and focal adhesions. Cell Motil. Cytoskeleton 43, 186-198.
8. Cowin, P. and Burke, B. (1996). Cytoskeleton-membrane interactions. Curr. Opin. Cell Biol. 8, 56-65.
9. Crawford, A. W., Michelsen, J. W. and Beckerle, M. C. (1992). An interaction between zyxin and α-actinin. J. Cell Biol. 116, 1381-1393.
10. Davies, J. A. and Garrod, D. R. (1997). Molecular aspects of the epithelial phenotype. BioEssays 19, 699-704.
11. Dabiri, G. A., Turnacioglu, K. K., Sanger, J. M. and Sanger, J. M. (1997). Myofibrillogenes, is visualized in living embryonic cardiomyocytes. Proc. Natl. Acad. Sci. USA 94, 9493-9498.
12. Doerr, M. E. and Jones, J. I. (1996). The roles of integrins and extracellular matrix proteins in the insulin-like growth factor I-stimulated chemotaxis of human breast cancer cells. J. Biol. Chem. 271, 2443-2447.
13. Dubreuil, R. R. and Wang, P. (2000). Genetic analysis of the requirements for α-actinin function. J. Muscle Res. Cell Motil. 21, 705-713.
14. Edwards, R. A. and Bryan, J. (1995). Fascins, a family of actin bundling proteins. Cell Motil. Cytoskeleton 32, 1-9.
15. Firon, M., Shahrabany, M., Altstock, R. T., Horev, J., Abramovici, A., Resau, J. H., Vande Woude, G. F., and Tsarfaty, I. (2000). Dominant negative Met reduces tumorigenicity-metastasis and increases tubule formation in mammary cells. Oncogene 19, 2386-2397.
16. Furge, K. A., Zhang, Y. W. and Vande Woude, G. F. (2000). Met receptor tyrosine kinase: enhanced signaling through adapter proteins. Oncogene 19, 5582-5589.
17. Fukami, K., Sawada, N., Endo, T. and Takenawa, T. (1996). Identification of a phosphatidylinositol 4,5-bisphosphate-binding site in chicken skeletal muscle α-actinin. J. Biol. Chem. 271, 2646-2650.
18. 3 binding to α-actinin. J. Cell Biol. 150, 627-641.
19. Gumbiner, B. M. (1996). Cell adhesion: the molecular basis of tissue architecture and morphogenesis. Cell 84, 345-357.
20. Gumbiner, B. M. (2000). Regulation of cadherin adhesive activity. J. Cell Biol. 148, 399-404.
21. Guvakova, M. A. and Surmacz, E. (1997). Overexpressed IGF-I receptors reduce estrogen growth requirements, enhance survival, and promote E-cadherin-mediated cell-cell adhesion in human breast cancer cells. Exp. Cell Res. 231, 149-162.
22. Guvakova, M. A. and Surmacz, E. (1999). The activated insulin-like growth factor I receptor induces depolarization in breast epithelial cells characterized by actin filament disassembly and tyrosine dephosphorylation of FAK, Cas, and paxillin. Exp. Cell Res. 251, 244-255.
23. Guvakova, M. A., Boettiger, D. and Adams, J. C. (2002). Induction of fascin spikes in breast cancer cells by activation of the insulin-like growth factor-I receptor. Int. J. Biochem. Cell. Biol, 34, 685-698.
24. Happerfield, L. C., Miles, D. W., Barnes, D. M., Thomsen, L. L., Smith, P, and Hanby, A. (1997). The localization of the insulin-like growth factor receptor I (IGFR- 1) in benign and malignant breast tissue. J. Pathology 183, 412-417.
25. Hay, E. D. (1995). An overview of epithelio-mesenchymal transformation. Acta Anatomica 154, 8-20.
26. Hazan, R. B. and Norton, L. (1998). The epidermal growth factor receptor modulates the interaction of E-cadherin with the actin cytoskeleton. J. Biol. Chem. 273, 9078-9084.
27. Hemmings, L., Kuhlman, P. A. and Critchley, D. (1992). Analysis of the actin-binding domain of α-actinin by mutagenesis and demonstration that dystrophin contains a functionally homologous domain. J. Cell Biol. 116, 1369-1380.
28. Herrera, R. (1998). Modulation of hepatocyte growth factor-induced scattering of HT29 colon carcinoma cells. Involvement of the MAPK pathway. J. Cell Sci. 111, 1039-1049.
29. Hijikata, T., Lin, Z. X., Holtzer, S., Choi, J., Sweeney, H. L. and Holtzer, H. (1997). Unanticipated temporal and spatial effects of sarcomeric α-actinin peptides expressed in PtK2 cells. Cell Motil. Cytosleteton 38, 54-74.
30. Hu, Y., Qiao, L., Wang, S., Rong, S., Meuillet, E. J., Berggren, M., Gallegos, A., Powis, G. and Kozikowski, A. P. (2000). 3-(Hydroxymethyl)-bearing phophatidylinositol ether lipid analogous and carbonate surrogates block PI3-K, Akt, and cancer cell growth. J. Med. Chem. 43, 3045-3051.
31. Isumi, T., Saeki, Y., Akanuma, Y., Takaku, F. and Kasuga, M. (1988). Requirement for receptor-intrinsic tyrosine kinase activities during ligand-induced membrane ruffling of KB cells. J. Biol. Chem. 263, 10386-10393.
32. Izaguirre, G., Aguirre, L., Hu, Y. P., Lee, H. Y., Schlaepfer, D., Aneskievich, B. J. and Haimovich, B. (2001). The cytosleletal/non-muscle isoform of α-actinin is phosphorylated on its actin-binding domain by the focal adhesion kinase. J. Biol. Chem. 276, 28676-28685.
33. Kadowaki, T., Koyasu, S., Nishida, E., Sakai, H., Takaku, E, Yahara, I. and Kasuga, M. (1986). Insulin-like growth factors, insulin, and epidermal growth factor cause rapid cytoskeletal reorganization in KB cells. J. Biol. Chem. 261, 16141-16147.
34. Kato, H., Faria, T. N., Stannard, B., Roberts, C. T., Jr and LeRoith, D. (1994). Essential role of tyrosine residues 1131, 1135, 1136 of the insulin-like growth factor-I (IGF-I) receptor on IGF-I action. Mol. Endocrinol. 8, 40-50.
35. Kleinberg, D. L., Feldman, M. and Ruan, W. (2000). IGF-I: an essential factor in terminal end bud formation and ductal morphogenesis. J. Mamm. Gland Biol. Neoplasia 5, 7-17.
36. Klemke, R. L., Cai, S., Giannini, A. L., Gallagher, P. J., de Lanerolle, P. and Cheresh, D. A. (1997). Regulation of cell motility by mitogen-activated protein kinase. J. Cell Biol. 137, 481-492.
37. Knudsen, K. A., Peralta Soler, A., Johnson, K. R. and Wheellock, M. J. (1995). Interactions of α-actinin with the cadherin/catenin cell-cell adhesion complex via α-catenin. J. Cell. Sci. 130, 67-77.
38. Kohn, E. C., Francis, E. A., Liotta, L. A. and Schiffmann, E. (1990). Heterogeneity of the motility responses in malignant tumor cells: a biological basis for the diversity and homing of metastatic cells. Int. J. Cancer 46, 287-292.
39. Kroemker, M., Rüdiger, A. H., Jockusch, B. M. and Rüdiger, M. (1994). Intramolecular interactions in vinculin control α-actinin binding to the vinculin head. FEBS Lett. 355, 259-262.
40. Kureishy, N., Sapountzi, A., Prag, S., Anilkumar, N. and Adams, J. C. (2002). Fascins, and their roles in cell structure and function. BioEssays 24, 350-361.
41. Kusumi, A., Suzuki, K. and Koyasako, K. (1999). Mobility and cytoskeletal interactions of cell adhesion receptors. Curr Opin. Cell. Biol. 11, 582-590.
42. Lee, A. V., Hilsenbeck, S. G. and Yee, D. (1998). IGF system components as prognostic markers in breast cancer. Breast Cancer Res. Treat. 47, 295-302.
43. LeRoith, D. (2000). Insulin-like growth factor I receptor signaling-Overlapping or redundant pathways. Endocrinol. 141, 1287-1288.
44. Leventhal, P. S. and Feldman, E. L. (1997). Insulin-like growth factors as regulators of cell motility: Signaling mechanisms. Trends. Endocrinol. Metab. 8, 1-6.
45. Liang, T. J., Reid, A. E., Xavier, R., Cardiff, R. D. and Wang, T. C. (1996). Transgenic expressions of tpr-met oncogene leads to development of mammary hyperplasia and tumors. J. Clin. Invest. 97, 2872-2877.
46. Manes, S., Mira, E., Gomes-Mouton, C., Zhao, Z. J., Lacalle, R. A. and Martinez-A, C. (1999). Concerted activity of tyrosine phosphatase SHP-2 and focal adhesion kinase in regulation of cell motility. Mol. Cell. Biol. 19, 3125-3135.
47. Matsudaira, P. (1994). Actin crosslinking proteins at the leading edge. Semin. Cell Biol. 5, 165-174.
48. McGregor, A., Blanchard, A. D., Rowe, A. J. and Critchley, D. R. (1994). Identification of the vinculin-binding site in the cytoskeletal protein alpha-actinin. Biochem. J. 301, 225-233.
49. Mira, E., Manes, S., Lacalle, R. A., Marquez, G. and Martinez-A, C. (1999). Insulin-like growth factor I-triggered cell migration and invasion are mediated by matrix metalloproteinase-9. Endocrinol. 140, 1657-1664.
50. Morali, O. G., Delmas, V., Moore, R., Jeanney, C., Thiery, J. P. and Larue, L. (2001). IGFII induces rapid β-catenin relocation to the nucleus during epithelium to mesenchyme transition. Oncogene 20, 4942-4950.
51. Müller, T., Choidas, A., Reichmann, E. and Ullrich, A. (1999). Phosphorylation and free pool of β-catenin are regulated by tyrosine kinases and tyrosine phosphatases during epithelial cell migration. J. Biol Chem. 274, 10173-10183.
52. Nieset, J. E., Redfield, A. R., Jin, F., Knudsen, K. A., Johnson, K. R. and Wheelock, M. J. (1997). Characterization of the interactions of alpha-catenin with alpha-actinin and beta-catenin/plakoglobin. J. Cell Sci. 110, 1013-1022.
53. Nobes, C. D., Hawkins, P., Stephens, L. and Hall, A. (1995). Activation of the small GTP-binding proteins rho and rac by growth factor receptors. J. Cell Sci. 108, 225-233.
54. Otey, C. A., Vasquez, G. B., Burridge, K. and Erickson, B. W. (1993). Mapping of the α-actinin binding site with β1 integrin cytoplasmic domain. J. Biol. Chem. 268, 21193-21197.
55. Potempa, S. and Ridley, A. J. (1998). Activation of both MAP kinsase and phosphatidylinositide 3-kinase by Ras is required for hepatocyte growth factor/scatter factor-induced adherens junction disassembly. Mol. Biol. Cell 9, 2185-2200.
56. Resnik, J. L., Reichart, D. B., Huey, K., Webster, N. J. G. and Seely, B. L. (1998). Elevated insulin-like growth factor I receptor autophosphorylation and kinase activity in human breast cancer. Cancer Res. 58, 1159-1164.
57. Royal, I. and Park, M. (1995). Hepatocyte growth factor-induced scatter of Madin-Darby Canine kidney cells requires phosphatidylinositol-3 kinse. J. Biol. Chem. 270, 27780-27787.
58. Sachs, M., Weidner, K. M., Brinkmann, V., Walther, L., Obermeier, A., Ullrich, A. and Birchmeier, W. (1996). Motogenic and morphogenic activity of epithelial receptor tyrosine kinases. J. Cell Biol. 133, 1095-1107.
59. Savagner, P. (2001). Leaving the neighborhood: molecular mechanisms involved during epithelial-mesenchymal transition. BioEssays 23, 912-923.
60. Savagner, P., Yamada, K. M. and Thiery, J. P. (1997). The zinc-finger protein slug causes desmosome dissociation, an initial and necessary step for growth factor-induced epithelial-mesenchymal transition. J. Cell Biol. 137, 1403-1419.
61. Schultheiss, T., Choi, J., Lin, Z. X., DiLullo, C., Cohen-Gould, L., Fischman, D. and Holtzer, H. (1992). A sarcomeric alpha-actinin truncated at the carboxyl end induced the breakdown of stress fibers in PtK2 cells and the formation of nemaline-like bodies and breakdown of myofibrils in myotubes. Proc. Natl. Acad. Sci. USA 89, 9282-9286.
62. Shibasaki, F., Fukami, K., Fukui, Y., and Takenawa, T. (1994). Phosphatidylinositol 3-kinase binds to alpha-actinin through the p85 subunit. Biochem. J. 302, 551-557.
63. Spencer, K. S. R., Graus-Porta, D., Leng, J., Hynes, N. E. and Klemke, R. L. (2000). ErbB2 is necessary for induction of carcinoma cell invasion by ErbB family receptor tyrosine kinases. J. Cell Biol. 148, 385-397.
64. Stoker, M. and Perryman, M. (1985). An epithelial scatter factor released by embroy fibroblasts. J. Cell Sci. 77, 209-223.
65. Stoker, M., Gherardi, E., Perryman, M. and Gray, J. (1987). Scatter factor is a fibroblast-derived modulator of epithelial cell mobility. Nature 327, 239-242.
66. Thiery, J. P. and Chopin, D. (1999). Epithelial cell plasticity in development and tumor progression. Cancer Metastasis Rev. 18, 31-42.
67. Tilney, L. G. and Tilney, M. S. (1994). Methods to visualize actin polymerization associated with bacterial invasion. Methods Enzymol. 236, 476-481.
68. Tsarfaty, I., Resau, J. H., Rulong, S., Keydar, I., Faletto, D. L. and Vande Woude, G. F. (1992). The met proto-oncogene receptor and lumen formation. Science 257, 1258-1261.
69. Tseng, Y., Fedorov, E., McCaffery, J. M., Almo, S. and Wirtz, D. (2001). Micromechanics and ultrastructure of actin filament networks crosslinked by human fascin: a comparison with α-actinin. J. Mol. Biol. 310, 351-366.
70. Tsukatani, Y., Sizuki, I. and Takahashi, K. (1997). Loss of density-dependent growth inhibition and dissociation of alpha-catenin from E-cadherin. J. Cell. Physiol. 173, 54-63.
71. Vasioukhin, V., Bauer, C., Yin, M. and Fuchs, E. (2000). Directed actin polymeriation in the driving force for epithelial cell-cell adhesion. Cell 100, 209-219.
72. Weidner, K. M., Behrens, J., Vanderkerckhove, J. and Birchmeier, W. (1990). Scatter Factor: Molecular characteristics and effect on the invasiveness of epithelial cells. J. Cell Biol. 111, 2097-2108.
73. 2+-binding domains in non-muscle type alpha-actinin: biochemical and genetic analysis. J. Cell Biol. 121, 599-606.
74. Wong, V., Ching, D., McCrea, P. D. and Firestone, G. L. (1999). Glucocorticoid down-regulation of fascin protein expressions is required for the steroid-induced formation of tight junctions and cell-cell interactions in rat mammary epithelial tumor cells. J. Biol. Chem. 274, 5443-5453.
75. Xu, J., Wirtz, D. and Pollard, T. D. (1998). Dynamic cross-linking by α-actinin determines the mechanical properties of actin filament networks. J. Biol. Chem. 273, 9570-9576.
76. Yamashiro, S., Yamakita, Y., Ono, S. and Matsumura, F. (1998) Fascin, an actin-bundling protein, induces membrane protusions and increases cell motility of epithelial cells. Mol. Biol. Cell 9, 993-1006.