Tenascin-C-derived peptide TNIIIA2 highly enhances cell survival and Platelet-derived Growth Factor (PDGF)-dependent cell proliferation through potentiated and sustained activation of integrin α5β1

Journal of Biological Chemistry

Volumn 289, Issue 25, 2014, Pages 17699-17708

  Tanaka, Rika ^a   Seki, Yutaka ^a   Saito, Yohei ^a   Kamiya, Sadahiro ^b   Fujita, Motomichi ^a   Okutsu, Hiroaki ^a   Iyoda, Takuya ^a   Takai, Tatsuya ^a   Owaki, Toshiyuki ^a   Yajima, Hirofumi ^a   Taira, Junichi ^c   Hayashi, Ryo ^d   Kodama, Hiroaki ^d   Matsunaga, Takuya ^e   Fukai, Fumio ^a  

^a TOKYO UNIVERSITY OF SCIENCE   (Japan)

^b JOSAI INTERNATIONAL UNIVERSITY   (Japan)

^c KURUME UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^d SAGA UNIVERSITY   (Japan)

^e KAGAWA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL CULTURE; CELL PROLIFERATION; ENZYME ACTIVITY; PEPTIDES;

BIOCHEMICAL ACTIVITY; CONFLUENT MONOLAYERS; MATRIX METALLOPROTEINASE-2; MECHANISTIC ANALYSIS; MEMBRANE MICRODOMAINS; PLATELET-DERIVED GROWTH FACTORS; PROTEIN KINASE PATHWAYS; SUSTAINED ACTIVATION;

CHEMICAL ACTIVATION;

CAVEOLIN 1; MATRIX METALLOPROTEINASE INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE; PLATELET DERIVED GROWTH FACTOR; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; PROTEIN TNIIIA2; RAS PROTEIN; SYNDECAN 4; TENASCIN; UNCLASSIFIED DRUG; VERY LATE ACTIVATION ANTIGEN 5; [(4 BIPHENYLYLSULFONYL) AMINO] N HYDROXY 3 PHENYLPROPIONAMIDE;

ANIMAL CELL; ANOIKIS; ARTICLE; CELL PROLIFERATION; CELL STIMULATION; CELL SURVIVAL; CONTROLLED STUDY; FIBROBLAST; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN FUNCTION;

CELL ADHESION; CELL PROLIFERATION; EXTRACELLULAR MATRIX; INTEGRIN; PDGF; TENASCIN;

ANIMALS; CELL PROLIFERATION; CELL SURVIVAL; HUMANS; K562 CELLS; MEMBRANE MICRODOMAINS; MICE; NIH 3T3 CELLS; PEPTIDES; PLATELET-DERIVED GROWTH FACTOR; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR BETA; RECEPTORS, VITRONECTIN; SYNDECAN-4; TENASCIN;

EID: 84903467700     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.546622     Document Type: Article

References (53)

1. Chiquet-Ehrismann, R., Mackie, E. J., Pearson, C. A., and Sakakura, T. (1986) Tenascin: an extracellular matrix protein involved in tissue interactions during fetal development and oncogenesis. Cell 47, 131-139 (Pubitemid 17181535)
2. Lightner, V. A., Slemp, C. A., and Erickson, H. P. (1990) Localization and quantitation of hexabrachion (tenascin) in skin, embryonic brain, tumors, and plasma. Ann. N.Y. Acad. Sci. 580, 260-275 (Pubitemid 20170404)
3. Chiquet-Ehrismann, R., and Chiquet, M. (2003) Tenascins: regulation and putative functions during pathological stress. J. Pathol. 200, 488-499 (Pubitemid 36818249)
4. Orend, G., and Chiquet-Ehrismann, R. (2006) Tenascin-C induced signaling in cancer. Cancer Lett. 244, 143-163 (Pubitemid 44508708)
5. Chiquet-Ehrismann, R., Kalla, P., Pearson, C. A., Beck, K., and Chiquet, M. (1988) Tenascin interferes with fibronectin action. Cell 53, 383-390
6. Joshi, P., Chung, C,-Y., Aukhil, I., and Erickson, H. P. (1993) Endothelial cells adhere to the RGD domain and the fibrinogen-like terminal knob of tenascin. J. Cell Sci. 106, 389-400 (Pubitemid 23286809)
7. Murphy-Ullrich, J. E. (2001) The de-adhesive activity of matricellular proteins: is intermediate cell adhesion an adaptive state? J. Clin. Invest. 107, 785-790
8. Hsia, H. C., and Schwarzbauer, J. E. (2005) Meet the tenascins: multifunctional and mysterious. J. Biol. Chem. 280, 26641-26644 (Pubitemid 41040694)
9. Orend, G. (2005) Potential oncogenic action of tenascin-C in tumorigenesis. Int. J. Biochem. Cell Biol. 37, 1066-1083
10. Huang, W., Chiquet-Ehrismann, R., Moyano, J. V., Garcia-Pardo, A., and Orend, G. (2001) Interference of tenascin-C with syndecan-4 binding to fibronectin blocks cell adhesion and stimulates tumor cell proliferation. Cancer Res. 61, 8586-8594 (Pubitemid 33131143)
11. Midwood, K. S., Valenick, L. V., Hsia, H. C., and Schwarzbauer, J. E. (2004) Coregiulation of fibronectin signaling and matrix contraction by tenascin-C and syndecan-4. Mol. Biol. Cell 15, 5670-5677 (Pubitemid 39564757)
12. Woods, A., McCarthy, J. B., Furcht, L. T., Couchman, J. R. (1993) A synthetic peptide from the COOH-terminal heparin-binding domain of fibronectin promotes focal adhesion formation. Mol. Biol. Cell 4, 605-613 (Pubitemid 23183608)
13. Lange, K., Kammerer, M., Hegi, M. E., Grotegut, S., Dittmann, A., Huang, W., Fluri, E., Yip, G. W., Götte M., Ruiz, C., and Orend, G. (2007) Endothelin receptor type B counteracts tenascin-C-induced endothelin receptor type A-dependent focal adhesion and actin stress fiber disorganization. Cancer Res. 67, 6163-6173 (Pubitemid 47037497)
14. Lange, K., Kammerer, M., Saupe, F., Hegi, M. E., Grotegut, S., Fluri, E., and Orend, G. (2008) Combined lysophosphatidic acid/platelet-derived growth factor signaling triggers glioma cell migration in a tenascin-C microenvironment. Cancer Res. 68, 6942-6952
15. Wenk, M. B., Midwood, K. S., and Schwarzbauer, J. E. (2000) Tenascin-C suppresses Rho activation. J. Cell Biol. 150, 913-920
16. Dedhar, S., Argraves, W. S., Suzuki, S., Ruoslahti, E., and Pierschbacher, M. D., (1987) Human osteosarcoma cells resistant to detachment by an Arg-Gly-Asp-containing peptide overproduce the fibronectin receptor. J. Cell Biol. 105, 1175-1182 (Pubitemid 18029842)
17. Giancotti, F. G., and Ruoslahti, E. (1990) Elevated levels of the α5β1 fibronectin receptor suppress the transformed phenotype of Chinese hamster ovary cells. Cell 60, 849-859
18. Plantefaber, L. C., and Hynes, R. O. (1989) Changes in integrin receptors on oncogenically transformed cells. Cell 56, 281-290 (Pubitemid 19050301)
19. Tennenbaum, T., Yuspa, S. H., Grover, A., Castronovo, V., Sobel, M. E., Yamada, Y., and De Luca, L. M. (1992) Extracellular matrix receptors and mouse skin carcinogenesis: altered expression linked to appearance of early markers of tumor progression. Cancer Res. 52, 2966-2976
20. Roman, J., Ritzenthaler, J. D., Roser-Page, S., Sun, X., and Han, S. (2010) α5β1-Integrin expression is essential for tumor progression in experimental lung cancer. Am. J. Respir. Cell Mol. Biol. 43, 684-691
21. Caswell, P. T., Spence H. J., Parsons, M., White, D. P., Clark, K., Cheng, K. W., Mills, G. B., Humphries, M. J., Messent, A. J., Anderson, K. I., McCaffrey, M. W., Ozanne, B. W., and Norman, J. C. (2007) Rab25 associates with α5β1 integrin to promote invasive migration in 3D microenvironments. Dev. Cell. 13, 496-510 (Pubitemid 47514517)
22. Kita, D., Takino, T., Nakada, M., Takahashi, T., Yamashita, J., and Sato, H. (2001) Expression of dominant-negative form of Ets-1 suppresses fibronectin-stimulated cell adhesion and migration through down-regulation of integrin α5 expression in U251 glioma cell line. Cancer Res. 61, 7985-7991 (Pubitemid 33049391)
23. Nam, J. M., Onodera, Y., Bissell, M. J., and Park, C. C. (2010) Breast cancer cells in three-dimensional culture display an enhanced radioresponse after coordinate targeting of integrin α5β1 and fibronectin. Cancer Res. 70, 5238-5248
24. Adachi, M., Taki, T., Higashiyama, M., Kohno, N., Inufusa, H., Miyake, M. (2000) Significance of integrin α5 gene expression as a prognostic factor in node-negative non-small cell lung cancer. Clin. Cancer Res. 6, 96-101 (Pubitemid 30064981)
25. Lessey, B. A., Albelda, S., Buck, C. A., Castelbaum, A. J., Yeh, I., Kohler, M., and Berchuck, A. (1995) Distribution of integrin cell adhesion molecules in endometrial cancer. Am. J. Pathol. 146, 717-726
26. Maglott, A., Bartik, P., Cosgun, S., Klotz, P., Rondé, P., Fuhrmann, G., Takeda, K., Martin, S., Dontenwill, M. (2006) The small α5β1 integrin antagonist, SJ749, reduces proliferation and clonogenicity of human astrocytoma cells. Cancer Res. 66, 6002-6007
27. Sawada, K., Mitra, A. K., Radjabi, A. R., Bhaskar, V., Kistner, E. O., Tretiakova, M., Jagadeeswaran, S., Montag, A., Becker, A., Kenny, H. A., Peter, M. E., Ramakrishnan, V., Yamada, S. D., Lengyel, E. (2008) Loss of Ecadherin promotes ovarian cancer metastasis via α 5-integrin, which is a therapeutic target. Cancer Res. 68, 2329-2339 (Pubitemid 351521807)
28. Martin, S., Cosset, E. C., Terrand, J., Maglott, A., Takeda, K., Dontenwill, M. (2009) Caveolin-1 regulates glioblastoma aggressiveness through the control of α5β1 integrin expression and modulates glioblastoma responsiveness to SJ749, an α5β1 integrin antagonist. Biochim. Biophys. Acta 1793, 354-367
29. Saito, Y., Imazeki, H., Miura, S., Yoshimura, T., Okutsu, H., Harada, Y., Ohwaki, T., Nagao, O., Kamiya, S., Hayashi, R., Kodama, H., Handa, H., Yoshida, T., and Fukai, F. (2007) A peptide derived from tenascin-C induces β1 integrin activation through syndecan-4. J. Biol. Chem. 282, 34929-34937 (Pubitemid 350232444)
30. Araki, E., Momota, Y., Togo, T., Tanioka, M., Hozumi, K., Nomizu, M., Miyachi, Y., Utani, A. (2009) Clustering of syndecan-4 and integrin β1 by laminin α3 chain-derived peptide promotes keratinocyte migration. Mol. Biol. Cell 20, 3012-3024
31. Faull, R. J., and Ginsberg, M. H. (1996) Inside-out signaling through integrins. J. Am. Soc. Nephrol. 7, 1091-1097 (Pubitemid 27468259)
32. Saito, Y., Owaki, T., Matsunaga, T., Saze, M., Miura, S., Maeda, M., Eguchi, M., Tanaka, R., Taira, J., Kodama, H., Goto, S., Niitsu, Y., Terada, H., and Fukai, F. (2010) Apoptotic death of hematopoietic tumor cells through potentiated and sustained adhesion to fibronectin via VLA-4. J. Biol. Chem. 285, 7006-7015
33. Tanaka, R., Owaki, T., Kamiya, S., Matsunaga, T., Shimoda, K., Kodama, H., Hayashi, R., Abe, T., Harada, Y. P., Shimonaka, M., Yajima, H., Terada, H., and Fukai, F. (2009) VLA-5-mediated adhesion to fibronectin accelerates hemin-stimulated erythroid differentiation of K562 cells through induction of VLA-4 expression. J. Biol. Chem. 284, 19817-19825
34. Matter, M. L., and Ruoslahti, E. (2001) A signaling pathway from the α5β1 and αvβ3 integrins that elevates bcl-2 transcription. J. Biol. Chem. 276, 27757-27763
35. Riddell, D. R., Sun, X. M., Stannard, A. K., Soutar, A. K., and Owen, J. S. (2001) Localization of apolipoprotein E receptor 2 to caveolae in the plasma membrane. J. Lipid Res. 42, 998-1002 (Pubitemid 32545857)
36. Clark, G. J., Cox, A. D., Graham, S. M., and Der, C. J. (1995) Biological assays for Ras transformation. Methods Enzymol. 255, 395-412
37. Markó, K., Ligeti, M., Mezo, G., Mihala, N., Kutnyánszky, E., Kiss, E., and Hudecz, F., and Madarász, E. (2008) A novel synthetic peptide polymer with cyclicRGDmotifs supports serum-free attachment of anchorage-dependent cells. Bioconjug. Chem. 19, 1757-1766
38. Itagaki, K., Naito, T., Iwakiri, R., Haga, M., Miura, S., Saito, Y., Owaki, T., Kamiya, S., Iyoda, T., Yajima, H., Iwashita, S., Ejiri, S., and Fukai, F. (2012) Eukaryotic translation elongation factor 1A induces anoikis by triggering cell detachment. J. Biol. Chem. 287, 16037-16046
39. Ravid, D., Leser, G. P., and Lamb, R. A. (2010) A role of caveolin-1 in assembly and budding of the Paramyxovirus parainfluenza virus 5. J. Virol. 84, 9749-9759
40. Liotta, L. A., and Kohn, E. (2004) Anoikis: cancer and the homeless cell. Nature 430, 973-974
41. Jones, P. L., Crack, J., and Rabinovitch, M. (1997) Regulation of tenascin-C, a vascular smooth muscle cell survival factor that interacts with the αvβ3 integrin to promote epidermal growth factor receptor phosphorylation and growth. J. Cell Biol. 139, 279-293 (Pubitemid 27444098)
42. Castellon, R., Caballero, S., Hamdi, H. K., Atilano, S. R., Aoki, A. M., Tarnuzzer, R. W., Kenney, M. C., Grant, M. B., and Ljubimov, A. V. (2002) Effects of tenascin-C on normal and diabetic retinal endothelial cells in culture. Invest Ophthalmol. Vis. Sci. 43, 2758-2766 (Pubitemid 34809470)
43. Jones, P. L., Jones, F. S., Zhou, B., and Rabinovitch, M. (1999) Induction of vascular smooth muscle cell tenascin-C gene expression by denatured type I collagen is dependent upon a β3 integrin-mediated mitogen-activated protein kinase pathway and a 122-base pair promoter element. J. Cell Sci. 112, 435-445 (Pubitemid 29106191)
44. Perlstein, I., Connolly, J. M., Cui, X., Song, C., Li, Q., Jones, P. L., Lu, Z., DeFelice, S., Klugherz, B., Wilensky, R., and Levy, R. J. (2003) DNA delivery from an intravascular stent with a denatured collagen- polylacticpolyglycolic acid-controlled release coating: mechanisms of enhanced transfection. Gene Ther. 10, 1420-1428 (Pubitemid 36987135)
45. Ishigaki, T., Imanaka-Yoshida, K., Shimojo, N., Matsushima, S., Taki, W., and Yoshida, T. (2011) Tenascin-C enhances crosstalk signaling of integrin αvβ3/PDGFR-β complex by SRC recruitment promoting PDGF-induced proliferation and migration in smooth muscle cells. J. Cell. Physiol. 226, 2617-2624
46. Danen, E. H., Ten Berge, P. J., Van Muijen, G. N., Van't Hof-Grootenboer, A. E., Bröcker, E. B., and Ruiter, D. J. (1994) Emergence of α5β1 fibronectin- and αvβ3 vitronectin-receptor expression in melanocytic tumour progression. Histopathology 24, 249-256
47. Natali, P. G., Nicotra, M. R., Di Filippo, F., and Bigotti, A. (1995) Expression of fibronectin, fibronectin isoforms and integrin receptors in melanocytic lesions. Br. J. Cancer 71, 1243-1247
48. Schiller, J. H., and Bittner, G. (1995) Loss of the tumorigenic phenotype with in vitro, but not in vivo, passaging of a novel series of human bronchial epithelial cell lines: possible role of an α5/β1-integrin-fibronectin interaction. Cancer Res. 55, 6215-6221
49. Kanda, R., Kawahara, A., Watari, K., Murakami, Y., Sonoda, K., Maeda, M., Fujita, H., Kage, M., Uramoto, H., Costa, C., Kuwano, M., and Ono, M. (2013) Erlotinib resistance in lung cancer cells mediated by integrin β1/Src/Akt-driven bypass signaling. Cancer Res. 73, 6243-6253
50. Guo, W., and Giancotti, F. G. (2004) Integrin signalling during tumour progression. Nat. Rev. Mol. Cell Biol. 5, 816-826 (Pubitemid 39336275)
51. Soung Y. H., Clifford J. L., and Chung, J. (2010) Crosstalk between integrin and receptor tyrosine kinase signaling in breast carcinoma progression. BMB Rep. 43, 311-318
52. Fleming, T. P., Matsui, T., and Aaronson, S. A. (1992) Platelet-derived growth factor (PDGF) receptor activation in cell transformation and human malignancy. Exp. Gerontol. 27, 523-532
53. Lokker, N. A., Sullivan, C. M., Hollenbach, S. J., Israel, M. A., and Giese, N. A. (2002) Platelet-derived growth factor (PDGF) autocrine signaling regulates survival and mitogenic pathways in glioblastoma cells: evidence that the novel PDGF-C and PDGF-D ligands may play a role in the development of brain tumors. Cancer Res. 62, 3729-3735 (Pubitemid 34728854)