Integrin β4 regulates SPARC protein to promote invasion

Journal of Biological Chemistry

Volumn 287, Issue 13, 2012, Pages 9835-9844

  Gerson, Kristin D ^a   Shearstone, Jeffrey R ^a   Maddula, V S R Krishna ^b   Seligmann, Bruce E ^b   Mercurio, Arthur M ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b High Throughput Genomics Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AFFYMETRIX GENECHIP; BREAST CARCINOMA CELLS; CYTOSKELETAL DYNAMICS; INTEGRINS; MATRIX REMODELING; MICRORNAS; SECRETED PROTEIN; SIGNALING PATHWAYS;

AMINO ACIDS;

GLYCOPROTEINS;

ALPHA6BETA4 INTEGRIN; BETA4 INTEGRIN; GLYCOPROTEIN; MICRORNA; MICRORNA 29A; OSTEONECTIN; UNCLASSIFIED DRUG;

ARTICLE; BREAST CARCINOGENESIS; BREAST CARCINOMA; CANCER INVASION; CARCINOMA CELL; CONTROLLED STUDY; CYTOSKELETON; GENE EXPRESSION REGULATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; SIGNAL TRANSDUCTION; TUMOR PROMOTION;

CELL LINE, TUMOR; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INTEGRIN BETA4; MICRORNAS; NEOPLASM INVASIVENESS; NEOPLASM PROTEINS; NEOPLASMS; OSTEONECTIN; PROTEIN BIOSYNTHESIS;

EID: 84858980393     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.317727     Document Type: Article

References (79)

1. Hynes, R. O. (1999) Cell adhesion. Old and new questions. Trends Cell Biol. 9, M33-M37
2. van der Flier, A., and Sonnenberg, A. (2001) Function and interactions of integrins. Cell Tissue Res. 305, 285-298
3. Lipscomb, E. A., and Mercurio, A. M. (2005) Mobilization and activation of a signaling-competent α6β4 integrin underlies its contribution to carcinoma progression. Cancer Metastasis Rev. 24, 413-423 (Pubitemid 41569981)
4. de Pereda, J. M., Ortega, E., Alonso-García, N., Gómez-Hernández, M., and Sonnenberg, A. (2009) Advances and perspectives of the architecture of hemidesmosomes. Lessons from structural biology. Cell Adh. Migr. 3, 361-364
5. Borradori, L., and Sonnenberg, A. (1999) Structure and function of hemidesmosomes. More than simple adhesion complexes. J. Invest. Dermatol. 112, 411-418 (Pubitemid 29171928)
6. Lee, E. C., Lotz, M. M., Steele, G. D., Jr., and Mercurio, A. M. (1992) The integrin α6β4 is a laminin receptor. J. Cell Biol. 117, 671-678
7. Santoro, M. M., Gaudino, G., and Marchisio, P. C. (2003) The MSP receptor regulates α6β4 and α3β1 integrins via 14-3-3 proteins in keratinocyte migration. Dev. Cell 5, 257-271 (Pubitemid 37006470)
8. Rabinovitz, I., and Mercurio, A. M. (1997) The integrin α6β4 functions in carcinoma cell migration on laminin-1 by mediating the formation and stabilization of actin-containing motility structures. J. Cell Biol. 139, 1873-1884 (Pubitemid 28079249)
9. Rabinovitz, I., Toker, A., and Mercurio, A. M. (1999) Protein kinase C-dependent mobilization of the α6β4 integrin from hemidesmosomes and its association with actin-rich cell protrusions drive the chemotactic migration of carcinoma cells. J. Cell Biol. 146, 1147-1160
10. Sehgal, B. U., DeBiase, P. J., Matzno, S., Chew, T. L., Claiborne, J. N., Hopkinson, S. B., Russell, A., Marinkovich, M. P., and Jones, J. C. (2006) Integrin β4 regulates migratory behavior of keratinocytes by determining laminin-332 organization. J. Biol. Chem. 281, 35487-35498 (Pubitemid 46036585)
11. Yang, X. H., Richardson, A. L., Torres-Arzayus, M. I., Zhou, P., Sharma, C., Kazarov, A. R., Andzelm, M. M., Strominger, J. L., Brown, M., and Hemler, M. E. (2008) CD151 accelerates breast cancer by regulating α6 integrin function, signaling, and molecular organization. Cancer Res. 68, 3204-3213
12. Lu, S., Simin, K., Khan, A., and Mercurio, A. M. (2008) Analysis of integrin β4 expression in human breast cancer. Association with basal-like tumors and prognostic significance. Clin. Cancer Res. 14, 1050-1058 (Pubitemid 351302550)
13. Yang, X., Kovalenko, O. V., Tang, W., Claas, C., Stipp, C. S., and Hemler, M. E. (2004) Palmitoylation supports assembly and function of integrin-tetraspanin complexes. J. Cell Biol. 167, 1231-1240 (Pubitemid 40066636)
14. Guo, W., Pylayeva, Y., Pepe, A., Yoshioka, T., Muller, W. J., Inghirami, G., and Giancotti, F. G. (2006) β4 integrin amplifies ErbB2 signaling to promote mammary tumorigenesis. Cell 126, 489-502 (Pubitemid 44163602)
15. O'Connor, K. L., Nguyen, B. K., and Mercurio, A. M. (2000) RhoA function in lamellae formation and migration is regulated by the α6β4 integrin and cAMP metabolism. J. Cell Biol. 148, 253-258 (Pubitemid 30078237)
16. O'Connor, K. L., Shaw, L. M., and Mercurio, A. M. (1998) Release ofcAMP gating by the α6β4 integrin stimulates lamellae formation and the chemotactic migration of invasive carcinoma cells. J. Cell Biol. 143, 1749-1760 (Pubitemid 29006517)
17. Shaw, L. M., Rabinovitz, I., Wang, H. H., Toker, A., and Mercurio, A. M. (1997) Activation of phosphoinositide 3-OH kinase by the α6β4 integrin promotes carcinoma invasion. Cell 91, 949-960 (Pubitemid 28027828)
18. Zahir, N., Lakins, J. N., Russell, A., Ming, W., Chatterjee, C., Rozenberg, G. I., Marinkovich, M. P., and Weaver, V. M. (2003) Autocrine laminin-5 ligates α6β4 integrin and activates RAC and NFκB to mediate anchorage-independent survival of mammary tumors. J. Cell Biol. 163, 1397-1407 (Pubitemid 38032099)
19. Chen, M., Sinha, M., Luxon, B. A., Bresnick, A. R., and O'Connor, K. L. (2009) Integrin α6β4 controls the expression of genes associated with cell motility, invasion, and metastasis, including S100A4/metastasin. J. Biol. Chem. 284, 1484-1494
20. Clark, C. J., and Sage, E. H. (2008)Aprototypic matricellular protein in the tumor microenvironment. Where there's SPARC, there's fire. J. Cell Biochem. 104, 721-732 (Pubitemid 351830824)
21. Kapinas, K., Kessler, C. B., and Delany, A. M. (2009) miR-29 suppression of osteonectin in osteoblasts. Regulation during differentiation and by canonical Wnt signaling. J. Cell Biochem. 108, 216-224
22. Bartel, D. P. (2004) MicroRNAs. Genomics, biogenesis, mechanism, and function. Cell 116, 281-297
23. Bartel, D. P. (2009) MicroRNAs. Target recognition and regulatory functions. Cell 136, 215-233
24. Shaw, L. M., Lotz, M. M., and Mercurio, A. M. (1993) Inside-out integrin signaling in macrophages. Analysis of the role of the α 6Aβ1 and α6Bβ1 integrin variants in laminin adhesion by cDNA expression in an α6 integrin- deficient macrophage cell line. J. Biol. Chem. 268, 11401-11408 (Pubitemid 23162339)
25. Irizarry, R. A., Bolstad, B. M., Collin, F., Cope, L. M., Hobbs, B., and Speed, T. P. (2003) Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res. 31, e15
26. Lewis, B. P., Burge, C. B., and Bartel, D. P. (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120, 15-20 (Pubitemid 40094598)
27. Grimson, A., Farh, K. K., Johnston, W. K., Garrett-Engele, P., Lim, L. P., and Bartel, D. P. (2007) MicroRNA targeting specificity in mammals. Determinants beyond seed pairing. Mol. Cell 27, 91-105 (Pubitemid 46991392)
28. Subramanian, A., Tamayo, P., Mootha, V. K., Mukherjee, S., Ebert, B. L., Gillette, M. A., Paulovich, A., Pomeroy, S. L., Golub, T. R., Lander, E. S., and Mesirov, J. P. (2005) Gene set enrichment analysis. A knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. U.S.A. 102, 15545-15550 (Pubitemid 41528093)
29. Subramanian, A., Kuehn, H., Gould, J., Tamayo, P., and Mesirov, J. P. (2007) GSEA-P. A desktop application for Gene Set Enrichment Analysis. Bioinformatics 23, 3251-3253 (Pubitemid 350187532)
30. Ellison, G., Klinowska, T., Westwood, R. F., Docter, E., French, T., and Fox, J. C. (2002) Further evidence to support the melanocytic origin of MDAMB- 435. Mol. Pathol. 55, 294-299 (Pubitemid 35193254)
31. Garraway, L. A., Widlund, H. R., Rubin, M. A., Getz, G., Berger, A. J., Ramaswamy, S., Beroukhim, R., Milner, D. A., Granter, S. R., Du, J., Lee, C., Wagner, S. N., Li, C., Golub, T. R., Rimm, D. L., Meyerson, M. L., Fisher, D. E., and Sellers, W. R. (2005) Integrative genomic analyses identify MITF as a lineage survival oncogene amplified in malignant melanoma. Nature 436, 117-122 (Pubitemid 40966196)
32. Rae, J. M., Creighton, C. J., Meck, J. M., Haddad, B. R., and Johnson, M. D. (2007) MDA-MB-435 cells are derived from M14 melanoma cells. A loss for breast cancer but a boon for melanoma research. Breast Cancer Res. Treat. 104, 13-19 (Pubitemid 46976633)
33. Chambers, A. F. (2009) MDA-MB-435 and M14 cell lines. Identical but not M14 melanoma? Cancer Res. 69, 5292-5293
34. Montel, V., Suzuki, M., Galloy, C., Mose, E. S., and Tarin, D. (2009) Expression of melanocyte-related genes in human breast cancer and its implications. Differentiation 78, 283-291
35. Sellappan, S., Grijalva, R., Zhou, X., Yang, W., Eli, M. B., Mills, G. B., and Yu, D. (2004) Lineage infidelity of MDA-MB-435 cells. Expression of melanocyte proteins in a breast cancer cell line. Cancer Res. 64, 3479-3485 (Pubitemid 38657921)
36. Hollestelle, A., and Schutte, M. (2009) Comment re: MDA-MB-435 and M14 cell lines. Identical but not M14 Melanoma? Cancer Res. 69, 7893
37. Zhang, Q., Fan, H., Shen, J., Hoffman, R. M., and Xing, H. R. (2010) Human breast cancer cell lines co-express neuronal, epithelial, and melanocytic differentiation markers in vitro and in vivo. PLoS One 5, e9712
38. Hemler, M. E., Crouse, C., and Sonnenberg, A. (1989) Association of the VLA α6 subunit with a novel protein. A possible alternative to the common VLA β1 subunit on certain cell lines. J. Biol. Chem. 264, 6529-6535 (Pubitemid 19106739)
39. Shaw, L. M., Chao, C., Wewer, U. M., and Mercurio, A. M. (1996) Function of the integrin α6β1 in metastatic breast carcinoma cells assessed by expression of a dominant-negative receptor. Cancer Res. 56, 959-963 (Pubitemid 26065385)
40. Wewer, U. M., Shaw, L. M., Albrechtsen, R., and Mercurio, A. M. (1997) The integrin α6β1 promotes the survival of metastatic human breast carcinoma cells in mice. Am. J. Pathol. 151, 1191-1198 (Pubitemid 27479747)
41. Hwang, H. W., Wentzel, E. A., and Mendell, J. T. (2007) A hexanucleotide element directs microRNA nuclear import. Science 315, 97-100 (Pubitemid 46196987)
42. Sano, M., Aoyagi, K., Takahashi, H., Kawamura, T., Mabuchi, T., Igaki, H., Tachimori, Y., Kato, H., Ochiai, A., Honda, H., Nimura, Y., Nagino, M., Yoshida, T., and Sasaki, H. (2010) Forkhead box A1 transcriptional pathway in KRT7-expressing esophageal squamous cell carcinomas with extensive lymph node metastasis. Int. J. Oncol. 36, 321-330
43. Schietke, R., Warnecke, C., Wacker, I., Schödel, J., Mole, D. R., Campean, V., Amann, K., Goppelt-Struebe, M., Behrens, J., Eckardt, K. U., and Wiesener, M. S. (2010) The lysyl oxidases LOX and LOXL2 are necessary and sufficient to repress E-cadherin in hypoxia. Insights into cellular transformation processes mediated by HIF-1. J. Biol. Chem. 285, 6658-6669
44. Kirschmann, D. A., Seftor, E. A., Fong, S. F., Nieva, D. R., Sullivan, C. M., Edwards, E. M., Sommer, P., Csiszar, K., and Hendrix, M. J. (2002) A molecular role for lysyl oxidase in breast cancer invasion. Cancer Res. 62, 4478-4483 (Pubitemid 34827311)
45. Brekhman, V., and Neufeld, G. (2009) A novel asymmetric three-dimensional in vitro assay for the study of tumor cell invasion. BMC Cancer 9, 415
46. Barker, H. E., Chang, J., Cox, T. R., Lang, G., Bird, D., Nicolau, M., Evans, H. R., Gartland, A., and Erler, J. T. (2011) LOXL2-mediated matrix remodeling in metastasis and mammary gland involution. Cancer Res. 71, 1561-1572
47. Abiatari, I., Gillen, S., DeOliveira, T., Klose, T., Bo, K., Giese, N. A., Friess, H., and Kleeff, J. (2009) The microtubule-associated protein MAPRE2 is involved in perineural invasion of pancreatic cancer cells. Int. J. Oncol. 35, 1111-1116
48. Ramaswamy, S., Ross, K. N., Lander, E. S., and Golub, T. R. (2003) A molecular signature of metastasis in primary solid tumors. Nat. Genet. 33, 49-54 (Pubitemid 36068681)
49. Egeblad, M., Rasch, M. G., and Weaver, V. M. (2010) Dynamic interplay between the collagen scaffold and tumor evolution. Curr. Opin. Cell Biol. 22, 697-706
50. Trusolino, L., Bertotti, A., and Comoglio, P. M. (2001) A signaling adapter function for α6β4 integrin in the control of HGF-dependent invasive growth. Cell 107, 643-654 (Pubitemid 34014865)
51. Chung, J., Bachelder, R. E., Lipscomb, E. A., Shaw, L. M., and Mercurio, A. M. (2002) Integrin (α6β4) regulation of eIF-4E activity and VEGF translation. A survival mechanism for carcinoma cells. J. Cell Biol. 158, 165-174
52. Lipscomb, E. A., Simpson, K. J., Lyle, S. R., Ring, J. E., Dugan, A. S., and Mercurio, A. M. (2005) The α6β4 integrin maintains the survival of human breast carcinoma cells in vivo. Cancer Res. 65, 10970-10976 (Pubitemid 41713366)
53. Ledda, M. F., Adris, S., Bravo, A. I., Kairiyama, C., Bover, L., Chernajovsky, Y., Mordoh, J., and Podhajcer, O. L. (1997) Suppression of SPARC expression by antisense RNA abrogates the tumorigenicity of human melanoma cells. Nat. Med. 3, 171-176 (Pubitemid 27064701)
54. Gilles, C., Bassuk, J. A., Pulyaeva, H., Sage, E. H., Foidart, J. M., and Thompson, E. W. (1998) SPARC/osteonectin induces matrix metalloproteinase 2 activation in human breast cancer cell lines. Cancer Res. 58, 5529-5536 (Pubitemid 28551141)
55. Jacob, K., Webber, M., Benayahu, D., and Kleinman, H. K. (1999) Osteonectin promotes prostate cancer cell migration and invasion. A possible mechanism for metastasis to bone. Cancer Res. 59, 4453-4457 (Pubitemid 29418768)
56. Schultz, C., Lemke, N., Ge, S., Golembieski, W. A., and Rempel, S. A. (2002) Secreted protein acidic and rich in cysteine promotes glioma invasion and delays tumor growth in vivo. Cancer Res. 62, 6270-6277 (Pubitemid 35244481)
57. Kunigal, S., Gondi, C. S., Gujrati, M., Lakka, S. S., Dinh, D. H., Olivero, W. C., and Rao, J. S. (2006) SPARC-induced migration of glioblastoma cell lines via uPA-uPAR signaling and activation of small GTPase RhoA. Int. J. Oncol. 29, 1349-1357
58. Campo McKnight, D. A., Sosnoski, D. M., Koblinski, J. E., and Gay, C. V. (2006) Roles of osteonectin in the migration of breast cancer cells into bone. J. Cell Biochem. 97, 288-302 (Pubitemid 43167146)
59. Shi, Q., Bao, S., Song, L., Wu, Q., Bigner, D. D., Hjelmeland, A. B., and Rich, J. N. (2007) Targeting SPARC expression decreases glioma cellular survival and invasion associated with reduced activities of FAK and ILK kinases. Oncogene 26, 4084-4094 (Pubitemid 46920166)
60. Girotti, M. R., Fernández, M., López, J. A., Camafeita, E., Fernández, E. A., Albar, J. P., Benedetti, L. G., Valacco, M. P., Brekken, R. A., Podhajcer, O. L., and Llera, A. S. (2011) SPARC promotes cathepsin B-mediated melanoma invasiveness through a collagen I/α2β1 integrin axis. J. Invest. Dermatol. 131, 2438-2447
61. Sarrió, D., Rodriguez-Pinilla, S. M., Hardisson, D., Cano, A., Moreno- Bueno, G., and Palacios, J. (2008) Epithelial-mesenchymal transition in breast cancer relates to the basal-like phenotype. Cancer Res. 68, 989-997 (Pubitemid 351272216)
62. Koblinski, J. E., Kaplan-Singer, B. R., VanOsdol, S. J., Wu, M., Engbring, J. A., Wang, S., Goldsmith, C. M., Piper, J. T., Vostal, J. G., Harms, J. F., Welch, D. R., and Kleinman, H. K. (2005) Endogenous osteonectin/ SPARC/BM-40 expression inhibits MDA-MB-231 breast cancer cell metastasis. Cancer Res. 65, 7370-7377 (Pubitemid 41161270)
63. Wong, S. Y., Crowley, D., Bronson, R. T., and Hynes, R. O. (2008) Analyses of the role of endogenous SPARC in mouse models of prostate and breast cancer. Clin. Exp. Metastasis 25, 109-118
64. Kupprion, C., Motamed, K., and Sage, E. H. (1998) SPARC (BM-40, osteonectin) inhibits the mitogenic effect of vascular endothelial growth factor on microvascular endothelial cells. J. Biol. Chem. 273, 29635-29640 (Pubitemid 28509972)
65. Raines, E. W., Lane, T. F., Iruela-Arispe, M. L., Ross, R., and Sage, E. H. (1992) The extracellular glycoprotein SPARC interacts with platelet-derived growth factor (PDGF)-AB and -BB and inhibits the binding of PDGF to its receptors. Proc. Natl. Acad. Sci. U.S.A. 89, 1281-1285
66. Barker, T. H., Baneyx, G., Cardó-Vila, M., Workman, G. A., Weaver, M., Menon, P. M., Dedhar, S., Rempel, S. A., Arap, W., Pasqualini, R., Vogel, V., and Sage, E. H. (2005) SPARC regulates extracellular matrix organization through its modulation of integrin-linked kinase activity. J. Biol. Chem. 280, 36483-36493 (Pubitemid 41633922)
67. Nie, J., Chang, B., Traktuev, D. O., Sun, J., March, K., Chan, L., Sage, E. H., Pasqualini, R., Arap, W., and Kolonin, M. G. (2008) IFATS collection. Combinatorial peptides identify α5β1 integrin as a receptor for the matricellular protein SPARC on adipose stromal cells. Stem. Cells 26, 2735-2745
68. Weaver, M. S., Workman, G., and Sage, E. H. (2008) The copper binding domain of SPARC mediates cell survival in vitro via interaction with integrin β1 and activation of integrin-linked kinase. J. Biol. Chem. 283, 22826-22837
69. Thomas, S. L., Alam, R., Lemke, N., Schultz, L. R., Gutiérrez, J. A., and Rempel, S. A. (2010) PTEN augments SPARC suppression of proliferation and inhibits SPARC-induced migration by suppressing SHC-RAF-ERK and AKT signaling. Neuro Oncol. 12, 941-955
70. Rivera, L. B., Bradshaw, A. D., and Brekken, R. A. (2011) The regulatory function of SPARC in vascular biology. Cell. Mol. Life Sci. 68, 3165-3173
71. Tian, M., and Schiemann, W. P. (2009) The TGF-β paradox in human cancer. An update. Future Oncol. 5, 259-271
72. Francki, A., Bradshaw, A. D., Bassuk, J. A., Howe, C. C., Couser, W. G., and Sage, E. H. (1999) SPARC regulates the expression of collagen type I and transforming growth factor-β1 in mesangial cells. J. Biol. Chem. 274, 32145-32152
73. Francki, A., McClure, T. D., Brekken, R. A., Motamed, K., Murri, C., Wang, T., and Sage, E. H. (2004) SPARC regulates TGF-β1-dependent signaling in primary glomerular mesangial cells. J. Cell Biochem. 91, 915-925
74. Schiemann, B. J., Neil, J. R., and Schiemann, W. P. (2003) SPARC inhibits epithelial cell proliferation in part through stimulation of the transforming growth factor-β-signaling system. Mol. Biol. Cell 14, 3977-3988 (Pubitemid 37186302)
75. Chlenski, A., Guerrero, L. J., Yang, Q., Tian, Y., Peddinti, R., Salwen, H. R., and Cohn, S. L. (2007) SPARC enhances tumor stroma formation and prevents fibroblast activation. Oncogene 26, 4513-4522 (Pubitemid 47037046)
76. Rivera, L. B., and Brekken, R. A. (2011) SPARC promotes pericyte recruitment via inhibition of endoglin-dependent TGF-β1 activity. J. Cell Biol. 193, 1305-1319
77. Jauliac, S., López-Rodriguez, C., Shaw, L. M., Brown, L. F., Rao, A., and Toker, A. (2002) The role of NFAT transcription factors in integrin-mediated carcinoma invasion. Nat. Cell Biol. 4, 540-544 (Pubitemid 34752442)
78. Pullar, C. E., Baier, B. S., Kariya, Y., Russell, A. J., Horst, B. A., Marinkovich, M. P., and Isseroff, R. R. (2006) β4 integrin and epidermal growth factor coordinately regulate electric field-mediated directional migration via Rac1. Mol. Biol. Cell 17, 4925-4935 (Pubitemid 44665760)
79. Friedland, J. C., Lakins, J. N., Kazanietz, M. G., Chernoff, J., Boettiger, D., and Weaver, V. M. (2007) α6β4 integrin activates Rac-dependent p21- activated kinase 1 to drive NF-κB-dependent resistance to apoptosis in three-dimensional mammary acini. J. Cell Sci. 120, 3700-3712 (Pubitemid 350120961)