The prolyl 3-hydroxylases P3H2 and P3H3 are novel targets for epigenetic silencing in breast cancer

British Journal of Cancer

Volumn 100, Issue 10, 2009, Pages 1687-1696

  Shah, R ^a   Smith, P ^a   Purdie, C ^b   Quinlan, P ^b   Baker, L ^b   Aman, P ^c   Thompson, A M ^b   Crook, T ^a  

^a INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^b UNIVERSITY OF DUNDEE   (United Kingdom)

^c UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

Breast cancer; Epigenetics; Prolyl hydroxylase

Indexed keywords

ESTROGEN RECEPTOR;

ARTICLE; BREAST CARCINOMA; CANCER INHIBITION; COLONY FORMATION; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; DOWN REGULATION; EPIGENETICS; GENE EXPRESSION; GENE INACTIVATION; GENE SILENCING; GENE TARGETING; HUMAN; HUMAN CELL; P3H2 GENE; P3H3 GENE; PRIMARY TUMOR; PRIORITY JOURNAL; PROGNOSIS; TRANSCRIPTION REGULATION; TUMOR SUPPRESSOR GENE;

BREAST NEOPLASMS; CARCINOMA; CELL LINE, TUMOR; CELLS, CULTURED; CPG ISLANDS; DNA METHYLATION; DOWN-REGULATION; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; GENES, TUMOR SUPPRESSOR; HUMANS; PROCOLLAGEN-PROLINE DIOXYGENASE; RECEPTORS, ESTROGEN; TUMOR STEM CELL ASSAY;

EID: 66149118937     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/sj.bjc.6605042     Document Type: Article

References (41)

1. Baldridge D, Schwarze U, Morello R, Lennington J, Bertin TK, Pace JM, Pepin MG, Weis M, Eyre DR, Walsh J, Lambert D, Green A, Robinson H, Michelson M, Houge G, Lindman C, Martin J, Ward J, Lemyre E, Mitchell JJ, Krakow D, Rimoin DL, Cohn DH, Byers PH, Lee B (2008) CRTAP and LEPRE1 mutations in recessive osteogenesis imperfecta. Hum Mutat 29: 1435 - 1442
2. Baylin SB (2005) DNA methylation and gene silencing in cancer. Nat Clin Pract Oncol 2 Suppl (1): S4-S11
3. Baylin SB, Ohm JE (2006) Epigenetic gene silencing in cancer - a mechanism for early oncogenic pathway addiction? Nat Rev Cancer 6: 107-116
4. Bruick RK, McKnight SL (2001) A conserved family of prolyl-4-hydroxylases that modify HIF. Science 294: 1337-1340
5. Cabral WA, Chang W, Barnes AM, Weis M, Scott MA, Leikin S, Makareeva E, Kuznetsova NV, Rosenbaum KN, Tifft CJ, Bulas DI, Kozma C, Smith PA, Eyre DR, Marini JC (2007) Prolyl 3-hydroxylase 1 deficiency causes a recessive metabolic bone disorder resembling lethal/severe osteogenesis imperfecta. Nat Genet 39: 359 - 365
6. Crook T, Marston NJ, Sara EA, Vousden KH (1994) Transcriptional activation by p53 correlates with suppression of growth but not transformation. Cell 79: 817-827
7. Desmedt C, Piette F, Loi S, Wang Y, Lallemand F, Haibe-Kains B, Viale G, Delorenzi M, Zhang Y, d'Assignies MS, Bergh J, Lidereau R, Ellis P, Harris AL, Klijn JG, Foekens JA, Cardoso F, Piccart MJ, Buyse M, Sotiriou C (2007) Strong time dependence of the 76-gene prognostic signature for node-negative breast cancer patients in the TRANSBIG multicenter independent validation series. Clin Cancer Res 13: 3207-3214
8. Epstein AC, Gleadle JM, McNeill LA, Hewitson KS, O'Rourke J, Mole DR, Mukherji M, Metzen E, Wilson MI, Dhanda A, Tian YM, Masson N, Hamilton DL, Jaakkola P, Barstead R, Hodgkin J, Maxwell PH, Pugh CW, Schofield CJ, Ratcliffe PJ (2001) C elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 107: 43-54
9. Fähling M, Mrowka R, Steege A, Nebrich G, Perlewitz A, Persson PB, Thiele BJ (2006) Translational control of collagen prolyl 4-hydroxylase- α(I) gene expression under hypoxia. J Biol Chem 281: 26089-26101
10. Farmer P, Bonnefoi H, Becette V, Tubiana-Hulin M, Fumoleau P, Larsimont D, Macgrogan G, Bergh J, Cameron D, Goldstein D, Duss S, Nicoulaz AL, Brisken C, Fiche M, Delorenzi M, Iggo R (2005) Identification of molecular apocrine breast tumours by microarray analysis. Oncogene 24: 4660-4671
11. Ginestier C, Cervera N, Finetti P, Esteyries S, Esterni B, Adelaide J, Xerri L, Viens P, Jacquemier J, Charafe-Jauffret E, Chaffanet M, Birnbaum D, Bertucci F (2006) Prognosis and gene expression profiling of 20ql3-amplified breast cancers. Clin Cancer Res 12: 4533-4544
12. Gryder RM, Lamon M, Adams E (1975) Sequence position of 3-hydroxyproline in basement membrane collagen. Isolation of glycyl-3-hydroxyprolyl-4- hydroxyproline from swine kidney. J Biol Chem 250: 2470-2474
13. Herman JG, Baylin SB (2003) Gene silencing in cancer in association with promoter hypermethylation. N Engl J Med 349: 2042 - 2054
14. Hess KR, Anderson K, Symmans WF, Valero V, Ibrahim N, Mejia JA, Booser D, Theriault RL, Buzdar AU, Dempsey PJ, Rouzier R, Sneige N, Ross JS, Vidaurre T, Gomez HL, Hortobagyi GN, Pusztai L (2006) Pharmacogenomic predictor of sensitivity to preoperative chemotherapy with paclitaxel and fluorouracil, doxorubicin, and cyclophosphamide in breast cancer. J Clin Oncol 24: 4236 - 4244
15. Hofbauer KH, Gess B, Lohaus C, Meyer HE, Katschinski D, Kurtz A (2003) Oxygen tension regulates the expression of a group of procollagen hydroxylases. Eur J Bio chem 270: 4515-4522
16. Ikeda K, Iyama K, Ishikawa N, Egami H, Nakao M, Sado Y, Ninomiya Y, Baba H (2006) Loss of expression of type IV collagen alpha5 and alpha6 chains in colorectal cancer associated with the hypermethylation of their promoter region. Am J Pathol 168: 856-865
17. Ivan M, Kondo K, Yang H, Kim W, Valiando J, Ohh M, Salic A, Asara JM, Lane WS, Kaelin Jr WG (2001) HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for 02 sensing. Science 292: 464-468
18. Ivshina AV, George J, Senko O, Mow B, Putti TC, Smeds J, Lindahl T, Pawitan Y, Hall P, Nordgren H, Wong JE, Liu ET, Bergh J, Kuznetsov VA, Miller LD (2004) Genetic reclassification of histologic grade delineates new clinical subtypes of breast cancer. Cancer Res 66: 10292-10301
19. Jarnum S, Kjellman C, Darabi A, Nilsson I, Edvardsen K, Aman P (2004) Leprell, a novel ER and Golgi resident member of the Leprecan family. Biochem Biophys Res Commun 317: 342-351
20. Jenkins CL, Bretscher LE, Guzei IA, Raines RT (2003) Effect of 3-hydroxyproline residues on collagen stability. J Am Chem Soc 125: 6422-6427
21. Jones PA, Baylin SB (2002) The fundamental role of epigenetic events in cancer. Nat Rev Genet 3: 415-428
22. Raul SC, Sugihara T, Yoshida A, Nomura H, Wadhwa R (2000) Grosl, a potential growth suppressor on chromosome 1: its identity to basement membrane-associated proteoglycan, leprecan. Oncogene 19: 3576-3583
23. Kivirikko KI, Myllylä R, Pihlajaniemi T (1989) Protein hydroxylation: prolyl 4-hydroxylase, an enzyme with four co-substrates and a multifunctional subunit. FASEB J 3: 1609-1617
24. Ma XJ, Wang Z, Ryan PD, Isakoff SJ, Barmettler A, Fuller A, Muir B, Mohapatra G, Salunga R, Tuggle JT, Tran Y, Tran D, Tassin A, Amon P, Wang W, Wang W, Enright E, Stecker K, Estepa-Sabal E, Smith B, Younger J, Balis U, Michaelson J, Bhan A, Habin K, Baer TM, Brugge J, Haber DA, Erlander MG, Sgroi DC (2004) A two-gene expression ratio predicts clinical outcome in breast cancer patients treated with tamoxifen. Cancer Cell 5: 607-616
25. Miller LD, Smeds J, George J, Vega VB, Vergara L, Ploner A, Pawitan Y, Hall P, Klaar S, Liu ET, Bergh J (2005) An expression signature for p53 status in human breast cancer predicts mutation status, transcriptional effects, and patient survival. Proc Natl Acad Sci 102: 13550-13555
26. Minn AJ, Gupta GP, Siegel PM, Bos PD, Shu W, Giri DD, Viale A, Olshen AB, Gerald WL, Massague J (2005) Genes that mediate breast cancer metastasis to lung. Nature 436: 518-524
27. Mizuno K, Hayashi T, Peyton DH, Bachinger HP (2004) The peptides acetyl-(Gly-3(S)Hyp-4(R)Hyp)10-NH2 and acetyl-(Gly-Pro-3(S)Hyp)10-NH2 do not form a collagen triple helix. J Biol Chem 279: 282-287
28. Myllyharju J (2003) Prolyl 4-hydroxylases, the key enzymes of collagen biosynthesis. Matrix Biol 22: 15-24
29. Myllyharju J (2005) Intracellular Post-Translational Modifications of Collagens. Springer: Berlin/Heidelberg 2005; 247: 115-147
30. Neve RM, Chin K, Fridlyand J, Yeh J, Baehner FL, Fevr T, Clark L, Bayani N, Coppe JP, Tong F, Speed T, Spellman PT, DeVries S, Lapuk A, Wang NJ, Kuo WL, Stilwell JL, Pinkel D, Albertson DG, Waldman FM, McCormick F, Dickson RB, Johnson MD, Lippman M, Ethier S, Gazdar A, Gray JW (2006) A collection of breast cancer cell lines for the study of functionally distinct cancer subtypes. Cancer Cell 10: 515-527
31. Pawitan Y, Bjöhle J, Amler L, Borg AL, Egyhazi S, Hall P, Han X, Holmberg L, Huang F, Klaar S, Liu ET, Miller L, Nordgren H, Ploner A, Sandelin K, Shaw PM, Smeds J, Skoog L, Wedren S, Bergh J (2006) Gene expression profiling spares early breast cancer patients from adjuvant therapy: derived and validated in two population-based cohorts. Breast Cancer Res 7: R953 - R964
32. Radvanyi L, Singh-Sandhu D, Gallichan S, Lovitt C, Pedyczak A, Mallo G, Gish K, Kwok K, Hanna W, Zubovits J, Armes J, Venter D, Hakimi J, Shortreed J, Donovan M, Parrington M, Dunn P, Oomen R, Tartaglia J, Berinstein NL (2005) The gene associated with trichorhinophalangeal syndrome in humans is overexpressed in breast cancer. Proc Natl Acad Sci USA 102: 11005-11100
33. Richardson AL, Wang ZC, De Nicolo A, Lu X, Brown M, Miron A, Liao X, Iglehart JD, Livingston DM, Ganesan S (2006) X chromosomal abnormalities in basal-like human breast cancer. Cancer Cell 9: 121 - 132
34. Sengupta PK, Smith EM, Kim K, Murnane MJ, Smith BD (2003) DNA hypermethylation near the transcription start site of collagen alpha2(I) gene occurs in both cancer cell lines and primary colorectal cancers. Cancer Res 63: 1789-1797
35. Tiainen P, Pasanen A, Sormunen R, Myllyharju J (2008) Characterization of recombinant human prolyl 3-hydroxylase isoenzyme 2, an enzyme modifying the basement membrane collagen IV. J Biol Chem 283: 19432-19439
36. van de Vijver MJ, He YD, van't Veer LJ, Dai H, Hart AA, Voskuil DW, Schreiber GJ, Peterse JL, Roberts C, Marton MJ, Parrish M, Atsma D, Witteveen A, Glas A, Delahaye L, van der Velde T, Bartelink H, Rodenhuis S, Rutgers ET, Friend SH, Bernards R (2002) A gene-expression signature as a predictor of survival in breast cancer. N Engl J Med 347: 1999-2009
37. van't Veer LJ, Dai H, van de Vijver MJ, He YD, Hart AA, Mao M, Peterse HL, van der Kooy K, Marton MJ, Witteveen AT, Schreiber GJ, Kerkhoven RM, Roberts C, Linsley PS, Bernards R, Friend SH (2002) Gene expression profiling predicts clinical outcome of breast cancer. Nature 415: 530-536
38. Vranka JA, Sakai LY, Bachinger HP (2004) Prolyl 3-hydroxylase 1, enzyme characterisation and identification of a novel family of enzymes. J Biol Chem 279: 23615-23621
39. Wang Y, Klijn JG, Zhang Y, Sieuwerts AM, Look MP, Yang F, Talantov D, Timmermans M, Meijer-van Gelder ME, Yu J, Jafkoe T, Berns EM, Atkins D, Foekens JA (2005) Gene-expression profiles to predict distant metastasis of lymph-node-negative primary breast cancer. Lancet 365: 671-679
40. Wassenhove-McCarthy DJ, McCarthy KJ (1999) Molecular characterization of a novel basement membrane-associated proteoglycan, leprecan. J Biol Chem 274: 25004-25017
41. Zhao H, Langerod A, Ji Y, Nowels KW, Nesland JM, Tibshirani R, Bukholm IK, Käresen R, Botstein D, Borresen-Dale AL, Jeffrey SS (2004) Different gene expression patterns in invasive lobular and ductal carcinomas of the breast. Mol Biol Cell 15: 2523-253