Secreted Stress-Induced Phosphoprotein 1 Activates the ALK2-SMAD Signaling Pathways and Promotes Cell Proliferation of Ovarian Cancer Cells

Cell Reports

Volumn 2, Issue 2, 2012, Pages 283-293

  Tsai, Chia Lung ^a   Tsai, Chi Neu ^b   Lin, Chiao Yun ^a   Chen, Hsi Wen ^a,b   Lee, Yun Shien ^c,d   Chao, Angel ^a   Wang, Tzu Hao ^a,b,c   Wang, Hsin Shih ^a,b   Lai, Chyong Huey ^a  

^a CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

^b CHANG GUNG UNIVERSITY   (Taiwan)

^c CHANG GUNG MEMORIAL HOSPITAL   (Taiwan)

^d MING CHUAN UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ALK2 PROTEIN; BONE MORPHOGENETIC PROTEIN RECEPTOR; INHIBITOR OF DIFFERENTIATION 3; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHOPROTEIN; PRION PROTEIN; SMAD PROTEIN; STRESS INDUCED PHOSPHOPROTEIN 1; UNCLASSIFIED DRUG;

ARTICLE; CELL PROLIFERATION; CELL STIMULATION; CONTROLLED STUDY; EMBRYO; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; NERVOUS TISSUE; OVARY CANCER; PROTEIN BINDING; PROTEIN SECRETION; RECEPTOR BINDING; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION;

ACTIVIN RECEPTORS, TYPE I; CELL LINE, TUMOR; CELL PROLIFERATION; FEMALE; HEAT-SHOCK PROTEINS; HUMANS; INHIBITOR OF DIFFERENTIATION PROTEINS; NEOPLASM PROTEINS; OVARIAN NEOPLASMS; PROTEIN BINDING; SIGNAL TRANSDUCTION; SMAD PROTEINS;

ANIMALIA;

EID: 84865788598     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2012.07.002     Document Type: Article

References (48)

1. Alarmo E.L., Kallioniemi A. Bone morphogenetic proteins in breast cancer: dual role in tumourigenesis?. Endocr. Relat. Cancer 2010, 17:R123-R139.
2. Arbeitman M.N., Hogness D.S. Molecular chaperones activate the Drosophila ecdysone receptor, an RXR heterodimer. Cell 2000, 101:67-77.
3. Arruda-Carvalho M., Njaine B., Silveira M.S., Linden R., Chiarini L.B. Hop/STI1 modulates retinal proliferation and cell death independent of PrPC. Biochem. Biophys. Res. Commun. 2007, 361:474-480.
4. Bast R.C., Hennessy B., Mills G.B. The biology of ovarian cancer: new opportunities for translation. Nat. Rev. Cancer 2009, 9:415-428.
5. Bharadwaj S., Ali A., Ovsenek N. Multiple components of the HSP90 chaperone complex function in regulation of heat shock factor 1 In vivo. Mol. Cell. Biol. 1999, 19:8033-8041.
6. Blanco Calvo M., Bolós Fernández V., Medina Villaamil V., Aparicio Gallego G., Díaz Prado S., Grande Pulido E. Biology of BMP signalling and cancer. Clin. Transl. Oncol. 2009, 11:126-137.
7. Caetano F.A., Lopes M.H., Hajj G.N., Machado C.F., Pinto Arantes C., Magalhães A.C., Vieira Mde.P., Américo T.A., Massensini A.R., Priola S.A., et al. Endocytosis of prion protein is required for ERK1/2 signaling induced by stress-inducible protein 1. J. Neurosci. 2008, 28:6691-6702.
8. Chao A., Lin C.Y., Lee Y.S., Tsai C.L., Wei P.C., Hsueh S., Wu T.I., Tsai C.N., Wang C.J., Chao A.S., et al. Regulation of ovarian cancer progression by microRNA-187 through targeting Disabled homolog-2. Oncogene 2012, 31:764-775.
9. Ebisawa T., Tada K., Kitajima I., Tojo K., Sampath T.K., Kawabata M., Miyazono K., Imamura T. Characterization of bone morphogenetic protein-6 signaling pathways in osteoblast differentiation. J. Cell Sci. 1999, 112:3519-3527.
10. Erlich R.B., Kahn S.A., Lima F.R., Muras A.G., Martins R.A., Linden R., Chiarini L.B., Martins V.R., Moura Neto V. STI1 promotes glioma proliferation through MAPK and PI3K pathways. Glia 2007, 55:1690-1698.
11. Eustace B.K., Jay D.G. Extracellular roles for the molecular chaperone, hsp90. Cell Cycle 2004, 3:1098-1100.
12. Geisinger K.R., Kute T.E., Pettenati M.J., Welander C.E., Dennard Y., Collins L.A., Berens M.E. Characterization of a human ovarian carcinoma cell line with estrogen and progesterone receptors. Cancer 1989, 63:280-288.
13. Greenwald J., Groppe J., Gray P., Wiater E., Kwiatkowski W., Vale W., Choe S. The BMP7/ActRII extracellular domain complex provides new insights into the cooperative nature of receptor assembly. Mol. Cell 2003, 11:605-617.
14. Hardwick J.C., Kodach L.L., Offerhaus G.J., van den Brink G.R. Bone morphogenetic protein signalling in colorectal cancer. Nat. Rev. Cancer 2008, 8:806-812.
15. Hartung A., Bitton-Worms K., Rechtman M.M., Wenzel V., Boergermann J.H., Hassel S., Henis Y.I., Knaus P. Different routes of bone morphogenic protein (BMP) receptor endocytosis influence BMP signaling. Mol. Cell. Biol. 2006, 26:7791-7805.
16. Heldin C.H., Miyazono K., ten Dijke P. TGF-beta signalling from cell membrane to nucleus through SMAD proteins. Nature 1997, 390:465-471.
17. Herrera B., van Dinther M., Ten Dijke P., Inman G.J. Autocrine bone morphogenetic protein-9 signals through activin receptor-like kinase-2/Smad1/Smad4 to promote ovarian cancer cell proliferation. Cancer Res. 2009, 69:9254-9262.
18. Hu J., Toft D., Anselmo D., Wang X. In vitro reconstitution of functional hepadnavirus reverse transcriptase with cellular chaperone proteins. J. Virol. 2002, 76:269-279.
19. Johnson B.D., Schumacher R.J., Ross E.D., Toft D.O. Hop modulates Hsp70/Hsp90 interactions in protein folding. J. Biol. Chem. 1998, 273:3679-3686.
20. Karam A.K., Karlan B.Y. Ovarian cancer: the duplicity of CA125 measurement. Nat. Rev. Clin. Oncol. 2010, 7:335-339.
21. Kim S.H., Cho H.B., Nam E.J., Kim S.W., Kim Y.T., Park Y.W., Kim B.W., Kim J.H. Autoantibodies against stress-induced phosphoprotein-1 as a novel biomarker candidate for ovarian cancer. Genes Chromosomes Cancer 2010, 49:585-595.
22. Kitisin K., Saha T., Blake T., Golestaneh N., Deng M., Kim C., Tang Y., Shetty K., Mishra B., Mishra L. Tgf-Beta signaling in development. Sci. STKE 2007, 2007:cm1.
23. Lasorella A., Noseda M., Beyna M., Yokota Y., Iavarone A. Id2 is a retinoblastoma protein target and mediates signalling by Myc oncoproteins. Nature 2000, 407:592-598.
24. Lässle M., Blatch G.L., Kundra V., Takatori T., Zetter B.R. Stress-inducible, murine protein mSTI1. Characterization of binding domains for heat shock proteins and in vitro phosphorylation by different kinases. J. Biol. Chem. 1997, 272:1876-1884.
25. Lee C.T., Graf C., Mayer F.J., Richter S.M., Mayer M.P. Dynamics of the regulation of Hsp90 by the co-chaperone Sti1. EMBO J. 2012, 31:1518-1528.
26. Le Page C., Puiffe M.L., Meunier L., Zietarska M., de Ladurantaye M., Tonin P.N., Provencher D., Mes-Masson A.M. BMP-2 signaling in ovarian cancer and its association with poor prognosis. J. Ovarian Res. 2009, 2:4.
27. Li J., Richter K., Buchner J. Mixed Hsp90-cochaperone complexes are important for the progression of the reaction cycle. Nat. Struct. Mol. Biol. 2011, 18:61-66.
28. Longshaw V.M., Chapple J.P., Balda M.S., Cheetham M.E., Blatch G.L. Nuclear translocation of the Hsp70/Hsp90 organizing protein mSTI1 is regulated by cell cycle kinases. J. Cell Sci. 2004, 117:701-710.
29. Lopes M.H., Hajj G.N., Muras A.G., Mancini G.L., Castro R.M., Ribeiro K.C., Brentani R.R., Linden R., Martins V.R. Interaction of cellular prion and stress-inducible protein 1 promotes neuritogenesis and neuroprotection by distinct signaling pathways. J. Neurosci. 2005, 25:11330-11339.
30. Macia E., Ehrlich M., Massol R., Boucrot E., Brunner C., Kirchhausen T. Dynasore, a cell-permeable inhibitor of dynamin. Dev. Cell 2006, 10:839-850.
31. Macías-Silva M., Hoodless P.A., Tang S.J., Buchwald M., Wrana J.L. Specific activation of Smad1 signaling pathways by the BMP7 type I receptor, ALK2. J. Biol. Chem. 1998, 273:25628-25636.
32. Martins V.R., Graner E., Garcia-Abreu J., de Souza S.J., Mercadante A.F., Veiga S.S., Zanata S.M., Neto V.M., Brentani R.R. Complementary hydropathy identifies a cellular prion protein receptor. Nat. Med. 1997, 3:1376-1382.
33. McLean K., Gong Y., Choi Y., Deng N., Yang K., Bai S., Cabrera L., Keller E., McCauley L., Cho K.R., Buckanovich R.J. Human ovarian carcinoma-associated mesenchymal stem cells regulate cancer stem cells and tumorigenesis via altered BMP production. J. Clin. Invest. 2011, 121:3206-3219.
34. Miyazono K., Miyazawa K. Id: a target of BMP signaling. Sci. STKE 2002, 2002:pe40.
35. Niikura Y., Ohta S., Vandenbeldt K.J., Abdulle R., McEwen B.F., Kitagawa K. 17-AAG, an Hsp90 inhibitor, causes kinetochore defects: a novel mechanism by which 17-AAG inhibits cell proliferation. Oncogene 2006, 25:4133-4146.
36. Odunuga O.O., Longshaw V.M., Blatch G.L. Hop: more than an Hsp70/Hsp90 adaptor protein. Bioessays 2004, 26:1058-1068.
37. Roffé M., Beraldo F.H., Bester R., Nunziante M., Bach C., Mancini G., Gilch S., Vorberg I., Castilho B.A., Martins V.R., Hajj G.N. Prion protein interaction with stress-inducible protein 1 enhances neuronal protein synthesis via mTOR. Proc. Natl. Acad. Sci. USA 2010, 107:13147-13152.
38. Shepherd T.G., Thériault B.L., Nachtigal M.W. Autocrine BMP4 signalling regulates ID3 proto-oncogene expression in human ovarian cancer cells. Gene 2008, 414:95-105.
39. Sieber C., Kopf J., Hiepen C., Knaus P. Recent advances in BMP receptor signaling. Cytokine Growth Factor Rev. 2009, 20:343-355.
40. Taipale M., Jarosz D.F., Lindquist S. HSP90 at the hub of protein homeostasis: emerging mechanistic insights. Nat. Rev. Mol. Cell Biol. 2010, 11:515-528.
41. Thériault B.L., Shepherd T.G., Mujoomdar M.L., Nachtigal M.W. BMP4 induces EMT and Rho GTPase activation in human ovarian cancer cells. Carcinogenesis 2007, 28:1153-1162.
42. Tsai M.S., Hwang S.M., Chen K.D., Lee Y.S., Hsu L.W., Chang Y.J., Wang C.N., Peng H.H., Chang Y.L., Chao A.S., et al. Functional network analysis of the transcriptomes of mesenchymal stem cells derived from amniotic fluid, amniotic membrane, cord blood, and bone marrow. Stem Cells 2007, 25:2511-2523.
43. Waite K.A., Eng C. From developmental disorder to heritable cancer: it's all in the BMP/TGF-beta family. Nat. Rev. Genet. 2003, 4:763-773.
44. Wang T.H., Wang H.S., Ichijo H., Giannakakou P., Foster J.S., Fojo T., Wimalasena J. Microtubule-interfering agents activate c-Jun N-terminal kinase/stress-activated protein kinase through both Ras and apoptosis signal-regulating kinase pathways. J. Biol. Chem. 1998, 273:4928-4936.
45. Wang T.H., Chao A., Tsai C.L., Chang C.L., Chen S.H., Lee Y.S., Chen J.K., Lin Y.J., Chang P.Y., Wang C.J., et al. Stress-induced phosphoprotein 1 as a secreted biomarker for human ovarian cancer promotes cancer cell proliferation. Mol. Cell. Proteomics 2010, 9:1873-1884.
46. Weinmann A.S., Bartley S.M., Zhang T., Zhang M.Q., Farnham P.J. Use of chromatin immunoprecipitation to clone novel E2F target promoters. Mol. Cell. Biol. 2001, 21:6820-6832.
47. Yu P.B., Deng D.Y., Lai C.S., Hong C.C., Cuny G.D., Bouxsein M.L., Hong D.W., McManus P.M., Katagiri T., Sachidanandan C., et al. BMP type I receptor inhibition reduces heterotopic [corrected] ossification. Nat. Med. 2008, 14:1363-1369.
48. Zanata S.M., Lopes M.H., Mercadante A.F., Hajj G.N., Chiarini L.B., Nomizo R., Freitas A.R., Cabral A.L., Lee K.S., Juliano M.A., et al. Stress-inducible protein 1 is a cell surface ligand for cellular prion that triggers neuroprotection. EMBO J. 2002, 21:3307-3316.