Translational Activation of HIF1α by YB-1 Promotes Sarcoma Metastasis

Cancer Cell

Volumn 27, Issue 5, 2015, Pages 682-697

  El Naggar, Amal M ^a,b   Veinotte, Chansey J ^c   Cheng, Hongwei ^d   Grunewald, Thomas G P ^e   Negri, Gian Luca ^a,b   Somasekharan, Syam Prakash ^b   Corkery, Dale P ^c   Tirode, Franck ^f   Mathers, Joan ^b   Khan, Debjit ^b   Kyle, Alastair H ^b   Baker, Jennifer H ^b   LePard, Nancy E ^b   McKinney, Steven ^b   Hajee, Shamil ^b   Bosiljcic, Momir ^a,b   Leprivier, Gabriel ^b   Tognon, Cristina E ^b   Minchinton, Andrew I ^b   Bennewith, Kevin L ^a,b   Delattre, Olivier ^f   Wang, Yuzhuo ^d   Dellaire, Graham ^g   Berman, Jason N ^c,g   Sorensen, Poul H ^a,b   more..

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b BRITISH COLUMBIA CANCER RESEARCH CENTRE   (Canada)

^c IWK HEALTH CENTRE   (Canada)

^d UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^e UNIVERSITY OF MUNICH   (Germany)

^f INSTITUT CURIE   (France)

^g DALHOUSIE UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1ALPHA; Y BOX BINDING PROTEIN 1; HIF1A PROTEIN, HUMAN; VHL PROTEIN, HUMAN; VON HIPPEL LINDAU PROTEIN; YBX1 PROTEIN, HUMAN;

ANIMAL EXPERIMENT; ARTICLE; CELL INVASION; CONTROLLED STUDY; GENE EXPRESSION; HIGH RISK PATIENT; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA TRANSLATION; SARCOMA CELL; GENETICS; PATHOLOGY; PHYSIOLOGY; PROTEIN SYNTHESIS; SARCOMA; TUMOR INVASION;

ANIMALIA;

HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; NEOPLASM INVASIVENESS; NEOPLASM METASTASIS; PROTEIN BIOSYNTHESIS; SARCOMA; VON HIPPEL-LINDAU TUMOR SUPPRESSOR PROTEIN; Y-BOX-BINDING PROTEIN 1;

EID: 84929169233     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccell.2015.04.003     Document Type: Article

References (48)

1. Belaiba R.S., Bonello S., Zähringer C., Schmidt S., Hess J., Kietzmann T., Görlach A. Hypoxia up-regulates hypoxia-inducible factor-1alpha transcription by involving phosphatidylinositol 3-kinase and nuclear factor kappaB in pulmonary artery smooth muscle cells. Mol. Biol. Cell 2007, 18:4691-4697.
2. Bert A.G., Grépin R., Vadas M.A., Goodall G.J. Assessing IRES activity in the HIF-1alpha and other cellular 5' UTRs. RNA 2006, 12:1074-1083.
3. Bogden A.E., Haskell P.M., LePage D.J., Kelton D.E., Cobb W.R., Esber H.J. Growth of human tumor xenografts implanted under the renal capsule of normal immunocompetent mice. Exp. Cell Biol. 1979, 47:281-293.
4. Braunstein S., Karpisheva K., Pola C., Goldberg J., Hochman T., Yee H., Cangiarella J., Arju R., Formenti S.C., Schneider R.J. A hypoxia-controlled cap-dependent to cap-independent translation switch in breast cancer. Mol. Cell 2007, 28:501-512.
5. Chaffer C.L., Weinberg R.A. A perspective on cancer cell metastasis. Science 2011, 331:1559-1564.
6. Corkery D.P., Dellaire G., Berman J.N. Leukaemia xenotransplantation in zebrafish-chemotherapy response assay in vivo. Br. J. Haematol. 2011, 153:786-789.
7. Cutz J.C., Guan J., Bayani J., Yoshimoto M., Xue H., Sutcliffe M., English J., Flint J., LeRiche J., Yee J., et al. Establishment in severe combined immunodeficiency mice of subrenal capsule xenografts and transplantable tumor lines from a variety of primary human lung cancers: potential models for studying tumor progression-related changes. Clin. Cancer Res. 2006, 12:4043-4054.
8. Eisinger-Mathason T.S., Zhang M., Qiu Q., Skuli N., Nakazawa M.S., Karakasheva T., Mucaj V., Shay J.E., Stangenberg L., Sadri N., Pure E., Yoon S.S., Kirsch D.G., Simon M.C. Hypoxia-dependent modification of collagen networks promotes sarcoma metastasis. Cancer Discov. 2013, 3:1190-1205.
9. El Naggar A., Clarkson P., Zhang F., Mathers J., Tognon C., Sorensen P.H. Expression and stability of hypoxia inducible factor 1α in osteosarcoma. Pediatr. Blood Cancer 2012, 59:1215-1222.
10. Eliseeva I.A., Kim E.R., Guryanov S.G., Ovchinnikov L.P., Lyabin D.N. Y-box-binding protein 1 (YB-1) and its functions. Biochemistry Mosc. 2011, 76:1402-1433.
11. Evdokimova V.M., Ovchinnikov L.P. Translational regulation by Y-box transcription factor: involvement of the major mRNA-associated protein, p50. Int. J. Biochem. Cell Biol. 1999, 31:139-149.
12. Evdokimova V., Ovchinnikov L.P., Sorensen P.H. Y-box binding protein 1: providing a new angle on translational regulation. Cell Cycle 2006, 5:1143-1147.
13. Evdokimova V., Ruzanov P., Anglesio M.S., Sorokin A.V., Ovchinnikov L.P., Buckley J., Triche T.J., Sonenberg N., Sorensen P.H. Akt-mediated YB-1 phosphorylation activates translation of silent mRNA species. Mol. Cell. Biol. 2006, 26:277-292.
14. Evdokimova V., Tognon C., Ng T., Ruzanov P., Melnyk N., Fink D., Sorokin A., Ovchinnikov L.P., Davicioni E., Triche T.J., Sorensen P.H. Translational activation of snail1 and other developmentally regulated transcription factors by YB-1 promotes an epithelial-mesenchymal transition. Cancer Cell 2009, 15:402-415.
15. Finger E.C., Giaccia A.J. Hypoxia, inflammation, and the tumor microenvironment in metastatic disease. Cancer Metastasis Rev. 2010, 29:285-293.
16. Fraser D.J., Phillips A.O., Zhang X., van Roeyen C.R., Muehlenberg P., En-Nia A., Mertens P.R. Y-box protein-1 controls transforming growth factor-beta1 translation in proximal tubular cells. Kidney Int. 2008, 73:724-732.
17. Fujiwara-Okada Y., Matsumoto Y., Fukushi J., Setsu N., Matsuura S., Kamura S., Fujiwara T., Iida K., Hatano M., Nabeshima A., et al. Y-box binding protein-1 regulates cell proliferation and is associated with clinical outcomes of osteosarcoma. Br. J. Cancer 2013, 108:836-847.
18. Galbán S., Kuwano Y., Pullmann R., Martindale J.L., Kim H.H., Lal A., Abdelmohsen K., Yang X., Dang Y., Liu J.O., et al. RNA-binding proteins HuR and PTB promote the translation of hypoxia-inducible factor 1alpha. Mol. Cell. Biol. 2008, 28:93-107.
19. Giménez-Bonafé P., Fedoruk M.N., Whitmore T.G., Akbari M., Ralph J.L., Ettinger S., Gleave M.E., Nelson C.C. YB-1 is upregulated during prostate cancer tumor progression and increases P-glycoprotein activity. Prostate 2004, 59:337-349.
20. Gluz O., Mengele K., Schmitt M., Kates R., Diallo-Danebrock R., Neff F., Royer H.D., Eckstein N., Mohrmann S., Ting E., et al. Y-box-binding protein YB-1 identifies high-risk patients with primary breast cancer benefiting from rapidly cycled tandem high-dose adjuvant chemotherapy. J. Clin. Oncol. 2009, 27:6144-6151.
21. Gupta G.P., Massagué J. Cancer metastasis: building a framework. Cell 2006, 127:679-695.
22. HaDuong J.H., Martin A.A., Skapek S.X., Mascarenhas L. Sarcomas. Pediatr. Clin. North Am. 2015, 62:179-200.
23. Höckel M., Vaupel P. Tumor hypoxia: definitions and current clinical, biologic, and molecular aspects. J. Natl. Cancer Inst. 2001, 93:266-276.
24. Hsieh A.C., Liu Y., Edlind M.P., Ingolia N.T., Janes M.R., Sher A., Shi E.Y., Stumpf C.R., Christensen C., Bonham M.J., et al. The translational landscape of mTOR signalling steers cancer initiation and metastasis. Nature 2012, 485:55-61.
25. Hui A.S., Bauer A.L., Striet J.B., Schnell P.O., Czyzyk-Krzeska M.F. Calcium signaling stimulates translation of HIF-alpha during hypoxia. FASEB J. 2006, 20:466-475.
26. Ivan M., Kondo K., Yang H., Kim W., Valiando J., Ohh M., Salic A., Asara J.M., Lane W.S., Kaelin W.G. HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science 2001, 292:464-468.
27. Jaakkola P., Mole D.R., Tian Y.M., Wilson M.I., Gielbert J., Gaskell S.J., von Kriegsheim A., Hebestreit H.F., Mukherji M., Schofield C.J., et al. Targeting of HIF-alpha to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 2001, 292:468-472.
28. Kaelin W.G. Cancer and altered metabolism: potential importance of hypoxia-inducible factor and 2-oxoglutarate-dependent dioxygenases. Cold Spring Harb. Symp. Quant. Biol. 2011, 76:335-345.
29. Kohno K., Izumi H., Uchiumi T., Ashizuka M., Kuwano M. The pleiotropic functions of the Y-box-binding protein, YB-1. Bioessays 2003, 25:691-698.
30. Lagarde P., Przybyl J., Brulard C., Pérot G., Pierron G., Delattre O., Sciot R., Wozniak A., Schöffski P., Terrier P., et al. Chromosome instability accounts for reverse metastatic outcomes of pediatric and adult synovial sarcomas. J. Clin. Oncol. 2013, 31:608-615.
31. Lee S.L., Rouhi P., Dahl Jensen L., Zhang D., Ji H., Hauptmann G., Ingham P., Cao Y. Hypoxia-induced pathological angiogenesis mediates tumor cell dissemination, invasion, and metastasis in a zebrafish tumor model. Proc. Natl. Acad. Sci. USA 2009, 106:19485-19490.
32. Man T.K., Chintagumpala M., Visvanathan J., Shen J., Perlaky L., Hicks J., Johnson M., Davino N., Murray J., Helman L., et al. Expression profiles of osteosarcoma that can predict response to chemotherapy. Cancer Res. 2005, 65:8142-8150.
33. Masson N., Willam C., Maxwell P.H., Pugh C.W., Ratcliffe P.J. Independent function of two destruction domains in hypoxia-inducible factor-alpha chains activated by prolyl hydroxylation. EMBO J. 2001, 20:5197-5206.
34. Maxwell P.H., Wiesener M.S., Chang G.W., Clifford S.C., Vaux E.C., Cockman M.E., Wykoff C.C., Pugh C.W., Maher E.R., Ratcliffe P.J. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 1999, 399:271-275.
35. Mendoza-Naranjo A., El-Naggar A., Wai D.H., Mistry P., Lazic N., Ayala F.R., da Cunha I.W., Rodriguez-Viciana P., Cheng H., Tavares Guerreiro Fregnani J.H., et al. ERBB4 confers metastatic capacity in Ewing sarcoma. EMBO Mol. Med. 2013, 5:1019-1034.
36. Minchinton A.I., Wendt K.R., Clow K.A., Fryer K.H. Multilayers of cells growing on a permeable support. An in vitro tumour model. Acta Oncol. 1997, 36:13-16.
37. Peppel K., Baglioni C. A simple and fast method to extract RNA from tissue culture cells. Biotechniques 1990, 9:711-713.
38. Piccinin S., Tonin E., Sessa S., Demontis S., Rossi S., Pecciarini L., Zanatta L., Pivetta F., Grizzo A., Sonego M., et al. A "twist box" code of p53 inactivation: twist box: p53 interaction promotes p53 degradation. Cancer Cell 2012, 22:404-415.
39. Postel-Vinay S., Véron A.S., Tirode F., Pierron G., Reynaud S., Kovar H., Oberlin O., Lapouble E., Ballet S., Lucchesi C., et al. Common variants near TARDBP and EGR2 are associated with susceptibility to Ewing sarcoma. Nat. Genet. 2012, 44:323-327.
40. Semenza G.L. Targeting HIF-1 for cancer therapy. Nat. Rev. Cancer 2003, 3:721-732.
41. Semenza G.L. Hypoxia-inducible factor 1 and cancer pathogenesis. IUBMB Life 2008, 60:591-597.
42. Semenza G.L. Oxygen sensing, hypoxia-inducible factors, and disease pathophysiology. Annu. Rev. Pathol. 2014, 9:47-71.
43. Somasekharan S.P., Stoynov N., Rotblat B., Leprivier G., Galpin J.D., Ahern C.A., Foster L.J., Sorensen P.H. Identification and quantification of newly synthesized proteins translationally regulated by YB-1 using a novel Click-SILAC approach. J. Proteomics 2012, 77:e1-e10.
44. Taylor M.A., Sossey-Alaoui K., Thompson C.L., Danielpour D., Schiemann W.P. TGF-β upregulates miR-181a expression to promote breast cancer metastasis. J. Clin. Invest. 2013, 123:150-163.
45. Thoreen C.C., Chantranupong L., Keys H.R., Wang T., Gray N.S., Sabatini D.M. A unifying model for mTORC1-mediated regulation of mRNA translation. Nature 2012, 485:109-113.
46. Wykoff C.C., Beasley N.J., Watson P.H., Turner K.J., Pastorek J., Sibtain A., Wilson G.D., Turley H., Talks K.L., Maxwell P.H., et al. Hypoxia-inducible expression of tumor-associated carbonic anhydrases. Cancer Res. 2000, 60:7075-7083.
47. Xu M., Jin H., Xu C.X., Sun B., Song Z.G., Bi W.Z., Wang Y. miR-382 inhibits osteosarcoma metastasis and relapse by targeting Y box-binding protein 1. Mol. Ther. 2014, 23:89-98.
48. Yang M.H., Wu M.Z., Chiou S.H., Chen P.M., Chang S.Y., Liu C.J., Teng S.C., Wu K.J. Direct regulation of TWIST by HIF-1alpha promotes metastasis. Nat. Cell Biol. 2008, 10:295-305.