An integrin binding-defective mutant of insulin-like growth factor-1 (R36E/R37E IGF1) acts as a dominant-negative antagonist of the IGF1 receptor (IGF1R) and suppresses tumorigenesis but still binds to IGF1R

Journal of Biological Chemistry

Volumn 288, Issue 27, 2013, Pages 19593-19603

  Fujita, Masaaki ^a   Ieguchi, Katsuaki ^a   Cedano Prieto, Dora M ^a   Fong, Andrew ^a   Wilkerson, Charles ^a   Chen, Jane Q ^a   Wu, Mac ^a   Lo, Su Hao ^a   Cheung, Anthony T W ^a   Wilson, MacHelle D ^a   Cardiff, Robert D ^a   Borowsky, Alexander D ^a   Takada, Yoko K ^a   Takada, Yoshikazu ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CANCER CELL LINES; CELL VIABILITY; IGF1 RECEPTOR; INDUCED SIGNAL; INSULIN-LIKE GROWTH FACTOR-1; TERNARY COMPLEX; THERAPEUTIC TARGETS; TUMORIGENESIS;

ANCHORAGES (FOUNDATIONS); CELL CULTURE; CELL MEMBRANES; INSULIN; SIGNALING;

CELL SIGNALING;

INSULIN; INSULIN RECEPTOR; INTEGRIN; SOMATOMEDIN C; SOMATOMEDIN C RECEPTOR;

ANCHORAGE INDEPENDENT GROWTH; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL; CANCER CELL CULTURE; CARCINOGENESIS; CELL SURFACE; CELL VIABILITY; COMPLEX FORMATION; CONTROLLED STUDY; FEMALE; GENE REPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

CANCER; DRUG DISCOVERY; EXTRACELLULAR MATRIX; GROWTH FACTORS; INSULIN-LIKE GROWTH FACTOR (IGF); INTEGRINS; MUTANT; SIGNAL TRANSDUCTION;

AMINO ACID SUBSTITUTION; ANIMALS; CELL LINE, TUMOR; CELL SURVIVAL; CELL TRANSFORMATION, NEOPLASTIC; HUMANS; INSULIN; INSULIN-LIKE GROWTH FACTOR I; INTEGRINS; MICE; MODELS, BIOLOGICAL; MUTATION, MISSENSE; NIH 3T3 CELLS; PROTEIN BINDING; PROTEIN STRUCTURE, QUATERNARY; RECEPTOR, IGF TYPE 1; SIGNAL TRANSDUCTION;

EID: 84880047955     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.470872     Document Type: Article

References (30)

1. Stewart, C. E., and Rotwein, P. (1996) Growth, differentiation, and survival: multiple physiological functions for insulin-like growth factors. Physiol. Rev. 76, 1005-1026
2. Clemmons, D. R., Maile, L. A., Ling, Y., Yarber, J., and Busby, W. H. (2007) Role of the integrin αVβ3 in mediating increased smooth muscle cell responsiveness to IGF-I in response to hyperglycemic stress. Growth Horm. IGF Res. 17, 265-270
3. Clemmons, D. R., and Maile, L. A. (2005) Interaction between insulin-like growth factor-I receptor and αVβ3 integrin linked signaling pathways: cellular responses to changes in multiple signaling inputs. Mol. Endocrinol. 19, 1-11
4. Chaves, J., and Saif, M. W. (2011) IGF system in cancer: from bench to clinic. Anticancer Drugs 22, 206-212
5. Hynes, R. O. (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110, 673-687
6. Takada, Y., Ye, X., and Simon, S. (2007) The integrins. Genome Biol. 8, 215
7. Jones, J. I., Doerr, M. E., and Clemmons, D. R. (1995) Cell migration: interactions among integrins, IGFs and IGFBPs. Prog. Growth Factor Res. 6, 319-327
8. Zheng, B., and Clemmons, D. R. (1998) Blocking ligand occupancy of the αVβ3 integrin inhibits insulin-like growth factor I signaling in vascular smooth muscle cells. Proc. Natl. Acad. Sci. U.S.A. 95, 11217-11222
9. Saegusa, J., Yamaji, S., Ieguchi, K., Wu, C. Y., Lam, K. S., Liu, F. T., Takada, Y. K., and Takada, Y. (2009) The direct binding of insulin-like growth factor-1 (IGF-1) to integrin αVβ3 is involved in IGF-1 signaling. J. Biol. Chem. 284, 24106-24114
10. Fujita, M., Takada, Y. K., and Takada, Y. (2013) Insulin-like growth factor (IGF) signaling requires αVβ3-IGF1-IGF type 1 receptor (IGF1R) ternary complex formation in anchorage independence, and the complex formation does not require IGF1R and Src activation. J. Biol. Chem. 288, 3059-3069
11. Fujita, M., Ieguchi, K., Davari, P., Yamaji, S., Taniguchi, Y., Sekiguchi, K., Takada, Y. K., and Takada, Y. (2012) Cross-talk between integrin α6β4 and insulin-like growth factor-1 receptor (IGF1R) through direct α6β4 binding to IGF1 and subsequent α6β4-IGF1-IGF1R ternary complex formation in anchorage-independent conditions. J. Biol. Chem. 287, 12491-12500
12. Fukazawa, H., Mizuno, S., and Uehara, Y. (1995) A microplate assay for quantitation of anchorage-independent growth of transformed cells. Anal. Biochem. 228, 83-90
13. Akakura, N., Hoogland, C., Takada, Y. K., Saegusa, J., Ye, X., Liu, F. T., Cheung, A. T., and Takada, Y. (2006) The COOH-terminal globular domain of fibrinogen μ chain suppresses angiogenesis and tumor growth. Cancer Res. 66, 9691-9697
14. Feldman, J. P., Goldwasser, R., Mark, S., Schwartz, J., and Orion, I. (2009) A mathematical model for tumor volume evaluation using two-dimensions. J. Appl. Quant. Methods 4, 455-462
15. Ieguchi, K., Fujita, M., Ma, Z., Davari, P., Taniguchi, Y., Sekiguchi, K., Wang, B., Takada, Y. K., and Takada, Y. (2010) Direct binding of the EGF-like domain of neuregulin-1 to integrins (αVβ3 andα6β4) is involved in neuregulin-1/ErbB signaling. J. Biol. Chem. 285, 31388-31398
16. Mira, E., Mañes, S., Lacalle, R. A., Márquez, G., and Martínez-A, C. (1999) Insulin-like growth factor I-triggered cell migration and invasion are mediated by matrix metalloproteinase-9. Endocrinology 140, 1657-1664
17. Lu, C., Shimaoka, M., Ferzly, M., Oxvig, C., Takagi, J., and Springer, T. A. (2001) An isolated, surface-expressed I domain of the integrin αLβ2 is sufficient for strong adhesive function when locked in the open conformation with a disulfide bond. Proc. Natl. Acad. Sci. U.S.A. 98, 2387-2392
18. Perks, C. M., Vernon, E. G., Rosendahl, A. H., Tonge, D., and Holly, J. M. (2007) IGF-II and IGFBP-2 differentially regulate PTEN in human breast cancer cells. Oncogene 26, 5966-5972
19. Guy, C. T., Cardiff, R. D., and Muller, W. J. (1992) Induction of mammary tumors by expression of polyomavirus middle T oncogene: a transgenic mouse model for metastatic disease. Mol. Cell. Biol. 12, 954-961
20. Cheung, A., Young, L., and Chen, P. (1997) Microcirculation and metastasis in a new mouse mammary tumor model system. Int. J. Oncol. 11, 69-77
21. Pandini, G., Vigneri, R., Costantino, A., Frasca, F., Ippolito, A., Fujita-Yamaguchi, Y., Siddle, K., Goldfine, I. D., and Belfiore, A. (1999) Insulin and insulin-like growth factor-I (IGF-I) receptor overexpression in breast cancers leads to insulin/IGF-I hybrid receptor overexpression: evidence for a second mechanism of IGF-I signaling. Clin. Cancer Res. 5, 1935-1944
22. Fox, E. M., Miller, T. W., Balko, J. M., Kuba, M. G., Sánchez, V., Smith, R. A., Liu, S., González-Angulo, A. M., Mills, G. B., Ye, F., Shyr, Y., Manning, H. C., Buck, E., and Arteaga, C. L. (2011) A kinome-wide screen identifies the insulin/IGF-I receptor pathway as a mechanism of escape from hormone dependence in breast cancer. Cancer Res. 71, 6773-6784
23. Papa, V., Gliozzo, B., Clark, G. M., McGuire, W. L., Moore, D., Fujita-Yamaguchi, Y., Vigneri, R., Goldfine, I. D., and Pezzino, V. (1993) Insulinlike growth factor-I receptors are overexpressed and predict a low risk in human breast cancer. Cancer Res. 53, 3736-3740
24. Vella, V., Sciacca, L., Pandini, G., Mineo, R., Squatrito, S., Vigneri, R., and Belfiore, A. (2001) The IGF system in thyroid cancer: new concepts. Mol. Pathol. 54, 121-124
25. Girnita, A., Girnita, L., del Prete, F., Bartolazzi, A., Larsson, O., and Axelson, M. (2004) Cyclolignans as inhibitors of the insulin-like growth factor- 1 receptor and malignant cell growth. Cancer Res. 64, 236-242
26. Mizushima, H., Wang, X., Miyamoto, S., and Mekada, E. (2009) Integrin signal masks growth-promotion activity of HB-EGF in monolayer cell cultures. J. Cell Sci. 122, 4277-4286
27. Mori, S., Wu, C. Y., Yamaji, S., Saegusa, J., Shi, B., Ma, Z., Kuwabara, Y., Lam, K. S., Isseroff, R. R., Takada, Y. K., and Takada, Y. (2008) Direct binding of integrin αVβ3 to FGF1 plays a role in FGF1 signaling. J. Biol. Chem. 283, 18066-18075
28. Fujita, M., Takada, Y. K., and Takada, Y. (2012) Integrins αVβ3 and α4β1 act as coreceptors for fractalkine, and the integrin-binding defective mutant of fractalkine is an antagonist of CX3CR1. J. Immunol. 189, 5809-5819
29. Yamaji, S., Saegusa, J., Ieguchi, K., Fujita, M., Mori, S., Takada, Y. K., and Takada, Y. (2010) A novel fibroblast growth factor-1 (FGF1) mutant that acts as an FGF antagonist. PLoS One 5, e10273
30. Mori, S., Tran, V., Nishikawa, K., Kaneda, T., Hamada, Y., Kawaguchi, N., Fujita, M., Takada, Y. K., Matsuura, N., Zhao, M., and Takada, Y. (2013) A dominant-negative FGF1 mutant (the R50E mutant) suppresses tumorigenesis and angiogenesis. PLoS One 8, e57927