Extracellular heat shock protein HSP90β secreted by MG63 osteosarcoma cells inhibits activation of latent TGF-β1

Biochemical and Biophysical Research Communications

Volumn 398, Issue 3, 2010, Pages 525-531

  Suzuki, Shigeki ^a   Kulkarni, Ashok B ^a  

^a NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

Author keywords

Extracellular HSP90 ; Latent TGF activation; MG63 cell; Osteosarcoma; TGF 1

Indexed keywords

CELL SURFACE PROTEIN; HEAT SHOCK PROTEIN 90; HEAT SHOCK PROTEIN 90BETA; LATENCY ASSOCIATED PEPTIDE; TRANSFORMING GROWTH FACTOR BETA1; UNCLASSIFIED DRUG;

ARTICLE; CELL PROLIFERATION; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; HUMAN; HUMAN CELL; OSTEOSARCOMA; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; SIGNAL TRANSDUCTION;

AMINO ACID SEQUENCE; ANIMALS; CELL LINE, TUMOR; CELL PROLIFERATION; GENE EXPRESSION REGULATION; HSP90 HEAT-SHOCK PROTEINS; MOLECULAR SEQUENCE DATA; TRANSCRIPTION, GENETIC; TRANSFORMING GROWTH FACTOR BETA;

EID: 77955282106     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2010.06.112     Document Type: Article

References (34)

1. Kulkarni A.B., Huh C.G., Becker D., Geiser A., Lyght M., Flanders K.C., Roberts A.B., Sporn M.B., Ward J.M., Karlsson S. Transforming growth factor beta 1 null mutation in mice causes excessive inflammatory response and early death. Proc. Natl. Acad. Sci. USA 1993, 90:770-774.
2. Moses H.L., Serra R. Regulation of differentiation by TGF-beta. Curr. Opin. Genet. Dev. 1996, 6:581-586.
3. Massagué J., Blain S.W., Lom R.S. TGFbeta signaling in growth control, cancer, and heritable disorders. Cell 2000, 13:295-309.
4. Verrecchia F., Mauviel A. Transforming growth factor-β signaling through the SMAD pathway: role in extracellular matrix gene expression and regulation. J. Invest. Dermatol. 2002, 118:211-215.
5. Siegel P.M., Massagué J. Cytostatic and apoptotic actions of TGF-beta in homeostasis and cancer. Nat. Rev. Cancer 2003, 3:807-821.
6. Seyedin S.M., Thomas T.C., Thompson A.Y., Rosen D.M., Piez K.A. Purification and characterization of two cartilage-inducing factors from bovine demineralized bone. Proc. Natl. Acad. Sci. USA 1985, 82:2267-2271.
7. Janssens K., ten Dijke P., Janssens S., Van H.W. Transforming growth factor-beta1 to the bone. Endocr. Rev. 2005, 26:743-774.
8. Franchi A., Arganini L., Baroni G., Calzolari A., Capanna R., Campanacci D., Caldora P., Masi L., Brand M.L., Zampi G. Expression of transforming growth factor beta isoforms in osteosarcoma variants: association of TGF beta 1 with high-grade osteosarcomas. J. Pathol. 1998, 185:284-289.
9. Kloen P., Gebhardt M.C., Perez-Atayde A., Rosenberg A.E., Springfield D.S., Gold L.I., Mankin H.J. Expression of transforming growth factor-beta (TGF-beta) isoforms in osteosarcomas: TGF-beta3 is related to disease progression. Cancer 1997, 80:2230-2239.
10. Gentry L.E., Lioubin M.N., Purchio A.F., Marquardt H. Molecular events in the processing of recombinant type 1 pre-pro-transforming growth factor beta to the mature polypeptide. Mol. Cell. Biol. 1988, 8:4162-4168.
11. Miyazono K., Hellman U., Wernstedt C., Heldin C.H. Latent high molecular weight complex of transforming growth factor beta 1. Purification from human platelets and structural characterization. J. Biol. Chem. 1988, 263:6407-6415.
12. Wakefield L.M., Smith D.M., Flanders K.C., Sporn M.B. Latent transforming growth factor-beta from human platelets. A high molecular weight complex containing precursor sequences. J. Biol. Chem. 1988, 263:7646-7654.
13. Annes J.P., Munger J.S., Rifkin D.B. Making sense of latent TGFbeta activation. J. Cell Sci. 2003, 116:217-224.
14. Blakytny R., Ludlow A., Martin G.E., Ireland G., Lundm L.R., Ferguson M.W., Brunner G. Latent TGF-β1 activation by platelets. J. Cell Physiol. 2004, 199:67-76.
15. Annes J.P., Chen Y., Munger J.S., Rifkin D.B. Integrin alphaVbeta6-mediated activation of latent TGF-beta requires the latent TGF-beta binding protein-1. J. Cell Biol. 2004, 165:723-734.
16. Hozumi K., Suzuki N., Nielsen P.K., Nomizu M., Yamada Y. Laminin alpha1 chain LG4 module promotes cell attachment through syndecans and cell spreading through integrin alpha2beta1. J. Biol. Chem. 2006, 281:32929-32940.
17. de Vega S., Iwamoto T., Nakamura T., Hozumi K., McKnight D.A., Fisher L.W., Fukumoto S., Yamada Y. TM14 is a new member of the fibulin family (fibulin-7) that interacts with extracellular matrix molecules and is active for cell binding. J. Biol. Chem. 2007, 282:30878-30888.
18. Dennler S., Itoh S., Vivien D., ten Dijke P., Huet S., Gauthier J.M. Direct binding of Smad3 and Smad4 to critical TGF beta-inducible elements in the promoter of human plasminogen activator inhibitor-type 1 gene. EMBO J. 1998, 17:3091-3100.
19. Pearl L.H., Prodromou C. Structure, function, and mechanism of the Hsp90 molecular chaperone. Adv. Protein Chem. 2001, 59:157-186.
20. Young J.C., Moarefi I., Hartl F.U. Hsp90: a specialized but essential protein-folding tool. J. Cell Biol. 2001, 154:267-273.
21. Wrighton K.H., Lin X., Feng X.H. Critical role of chaperone HSP90 in TGF-β signaling. Proc. Natl. Acad. Sci. USA 2008, 105:9244-9249.
22. Eustace B.K., Sakurai T., Stewart J.K., Yimlamai D., Unger C., Zehetmeier C., Lain B., Torella C., Henning S.W., Beste G., Scroggins B.T., Neckers L., Ilag L.L., Jay D.G. Functional proteomic screens reveal an essential extracellular role for hsp90 alpha in cancer cell invasiveness. Nat. Cell Biol. 2004, 6:507-514.
23. Sidera K., Samiotaki M., Yfanti E., Panayotou G., Pastsavoudi E. Involvement of cell surface HSP90 in cell migration reveals a novel role in the developing nervous system. J. Biol. Chem. 2004, 279:45379-45388.
24. Becker B., Multhoff G., Farkas B., Wild P.J., Landthaler M., Stolz W., Vogt T. Induction of Hsp90 protein expression in malignant melanomas and melanoma metastases. Exp. Dermatol. 2004, 13:27-32.
25. Calderwood S.K., Mambula S.S., Gray P.J., Theriault J.R. Extracellular heat shock proteins in cell signaling. FEBS Lett. 2007, 581:3689-3694.
26. Cheng C.F., Fan J., Fedesco M., Guan S., Li Y., Bandyopadhyay B., Bright A.M., Yerushalmi D., Liang M., Chen M., Han Y.P., Woodley D.T., Li W. Transforming growth factor alpha (TGFalpha)-stimulated secretion of HSP90alpha: using the receptor LRP-1/CD91 to promote human skin cell migration against a TGF beta-rich environment during wound healing. Mol. Cell. Biol. 2008, 28:3344-3358.
27. Becker T., Hartl F.U., Wieland F. CD40, an extracellular receptor for binding and uptake of Hsp70-peptide complexes. J. Cell Biol. 2002, 158:1277-1285.
28. Matsuyama S., Iwadate M., Kondo M., Saitoh M., Hanyu A., Shimizu K., Aburatani H., Mishima H.K., Imamura T., Miyazono K., Miyazawa K. SB-431542 and Gleevec inhibit transforming growth factor-beta-induced proliferation of human osteosarcoma cells. Cancer Res. 2003, 63:7791-7798.
29. Young G.D., Murphy-Ullrich J.E. The tryptophan-rich motifs of the thrombospondin type 1 repeats bind VLAL motifs in the latent transforming growth factor-beta complex. J. Biol. Chem. 2004, 279:47633-47642.
30. Yang Z., Mu Z., Dabovic B., Jurukovski V., Yu D., Sung J., Xiong X., Mungerm J.S. Absence of integrin-mediated TGFbeta1 activation in vivo recapitulates the phenotype of TGFbeta1-null mice. J. Cell Biol. 2007, 176:787-793.
31. Nakao A., Afrakhte M., Morén A., Nakayama T., Christian J.L., Heuchei R., Itoh S., Kawabata M., Heldin N.E., Heldin C.H., ten Dijke P. Identification of Smad7, a TGF-β-inducible antagonist of TGF-β signaling. Nature 1997, 389:631-635.
32. Nakajima M., Kizawa H., Saitoh M., Kou I., Miyazono K., Ikegawa S. Mechanisms for asporin function and regulation in articular cartilage. J. Biol. Chem. 2007, 282:32185-32192.
33. Yu X., Harris S.L., Levine A.J. The regulation of exosome secretion: a novel function of the p53 protein. Cancer Res. 2006, 66:4795-4801.
34. Amzallag N., Passer B.J., Allanic D., Segura E., Théry C., Goud B., Amson R., Telerman A. TSAP6 facilitates the secretion of translationally controlled tumor protein/histamine-releasing factor via a nonclassical pathway. J. Biol. Chem. 2004, 279:46104-46112.