The prolyl hydroxylase enzymes are positively associated with hypoxia-inducible factor-1α and vascular endothelial growth factor in human breast cancer and alter in response to primary systemic treatment with epirubicin and tamoxifen

Breast Cancer Research

Volumn 13, Issue 1, 2011, Pages

  Fox, Stephen B ^a   Generali, Daniele ^b   Berruti, Alfredo ^c   Brizzi, Maria P ^b   Campo, Leticia ^d   Bonardi, Simone ^b   Bersiga, Alessandra ^b   Allevi, Giovanni ^b   Milani, Manuela ^d   Aguggini, Sergio ^b   Mele, Teresa ^b,c   Dogliotti, Luigi ^c   Bottini, Alberto ^b   Harris, Adrian L ^d  

^a PETER MACCALLUM CANCER CENTRE   (Australia)

^b CREMONA HOSPITAL   (Italy)

^c SAN LUIGI GONZAGA HOSPITAL   (Italy)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CARBONATE DEHYDRATASE IX; CYCLOPHOSPHAMIDE; EPIRUBICIN; FLUOROURACIL; HYPOXIA INDUCIBLE FACTOR 1ALPHA; METHOTREXATE; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; TAMOXIFEN; VASCULOTROPIN; ANTINEOPLASTIC AGENT; EGLN1 PROTEIN, HUMAN; EGLN2 PROTEIN, HUMAN; EGLN3 PROTEIN, HUMAN; HYPOXIA INDUCIBLE FACTOR PROLINE DIOXYGENASE; TUMOR MARKER; VASCULOTROPIN A;

ARTICLE; BREAST CANCER; CANCER COMBINATION CHEMOTHERAPY; CANCER PATIENT; CANCER SURVIVAL; CONTROLLED STUDY; HUMAN; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MULTIPLE CYCLE TREATMENT; PHASE 2 CLINICAL TRIAL; PROTEIN EXPRESSION; RANDOMIZED CONTROLLED TRIAL; TISSUE MICROARRAY; TREATMENT RESPONSE; BREAST TUMOR; CONTROLLED CLINICAL TRIAL; DRUG EFFECT; ENZYMOLOGY; FEMALE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PROGNOSIS;

ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; EPIRUBICIN; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; HYPOXIA-INDUCIBLE FACTOR-PROLINE DIOXYGENASES; PROGNOSIS; PROLYL HYDROXYLASES; TAMOXIFEN; TUMOR MARKERS, BIOLOGICAL; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84860389190     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/bcr2825     Document Type: Article

References (38)

1. Harris AL. Hypoxia - a key regulatory factor in tumour growth. Nat Rev Cancer 2002, 2:38-47. 10.1038/nrc704, 11902584.
2. Generali D, Berruti A, Brizzi MP, Campo L, Bonardi S, Wigfield S, Bersiga A, Allevi G, Milani M, Aguggini S, Gandolfi V, Dogliotti L, Bottini A, Harris AL, Fox SB. Hypoxia-inducible factor-1α expression predicts a poor response to primary chemoendocrine therapy and disease-free survival in primary human breast cancer. Clin Cancer Res 2006, 12:4562-4568. 10.1158/1078-0432.CCR-05-2690, 16899602.
3. Maxwell PH. The HIF pathway in cancer. Semin Cell Dev Biol 2005, 16:523-530. 10.1016/j.semcdb.2005.03.001, 16144689.
4. Jaakkola P, Mole DR, Tian YM, Wilson MI, Gielbert J, Gaskell SJ, Kriegsheim A, Hebestreit HF, Mukherji M, Schofield CJ, Maxwell PH, Pugh CW, Ratcliffe PJ. Targeting of HIF-α to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 2001, 292:468-472. 10.1126/science.1059796, 11292861.
5. Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, Cockman ME, Wykoff CC, Pugh CW, Maher ER, Ratcliffe PJ. The tumour suppressor protein VHL targets hypoxia-inducible factors for oxygen-dependent proteolysis. Nature 1999, 399:271-275. 10.1038/20459, 10353251.
6. 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. C. elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 2001, 107:43-54. 10.1016/S0092-8674(01)00507-4, 11595184.
7. Bos R, van der Groep P, Greijer AE, Shvarts A, Meijer S, Pinedo HM, Semenza GL, van Diest PJ, van der Wall E. Levels of hypoxia-inducible factor-1α independently predict prognosis in patients with lymph node negative breast carcinoma. Cancer 2003, 97:1573-1581. 10.1002/cncr.11246, 12627523.
8. Dales JP, Garcia S, Meunier-Carpentier S, Andrac-Meyer L, Haddad O, Lavaut MN, Allasia C, Bonnier P, Charpin C. Overexpression of hypoxia-inducible factor HIF-1α predicts early relapse in breast cancer: retrospective study in a series of 745 patients. Int J Cancer 2005, 116:734-739. 10.1002/ijc.20984, 15849727.
9. Chia SK, Wykoff CC, Watson PH, Han C, Leek RD, Pastorek J, Gatter KC, Ratcliffe P, Harris AL. Prognostic significance of a novel hypoxia-regulated marker, carbonic anhydrase IX, in invasive breast carcinoma. J Clin Oncol 2001, 19:3660-3668.
10. Tan EY, Campo L, Han C, Turley H, Pezzella F, Gatter KC, Harris AL, Fox SB. BNIP3 as a progression marker in primary human breast cancer; opposing functions in in situ versus invasive cancer. Clin Cancer Res 2007, 13:467-474. 10.1158/1078-0432.CCR-06-1466, 17255267.
11. Ryan HE, Lo J, Johnson RS. HIF-1 α is required for solid tumor formation and embryonic vascularization. EMBO J 1998, 17:3005-3015. 10.1093/emboj/17.11.3005, 1170640, 9606183.
12. Ryan HE, Poloni M, McNulty W, Elson D, Gassmann M, Arbeit JM, Johnson RS. Hypoxia-inducible factor-1α is a positive factor in solid tumor growth. Cancer Res 2000, 60:4010-4015.
13. Carmeliet P, Dor Y, Herbert JM, Fukumura D, Brusselmans K, Dewerchin M, Neeman M, Bono F, Abramovitch R, Maxwell P, Koch CJ, Ratcliffe P, Moons L, Jain RK, Collen D, Keshert E. Role of HIF-1α in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis. Nature 1998, 394:485-490. 10.1038/28867, 9697772.
14. Chan DA, Kawahara TL, Sutphin PD, Chang HY, Chi JT, Giaccia AJ. Tumor vasculature is regulated by PHD2-mediated angiogenesis and bone marrow-derived cell recruitment. Cancer Cell 2009, 15:527-538. 10.1016/j.ccr.2009.04.010, 2846696, 19477431.
15. Soilleux EJ, Turley H, Tian YM, Pugh CW, Gatter KC, Harris AL. Use of novel monoclonal antibodies to determine the expression and distribution of the hypoxia regulatory factors PHD-1, PHD-2, PHD-3 and FIH in normal and neoplastic human tissues. Histopathology 2005, 47:602-610. 10.1111/j.1365-2559.2005.02280.x, 16324198.
16. Bottini A, Berruti A, Brizzi MP, Bersiga A, Generali D, Allevi G, Aguggini S, Bolsi G, Bonardi S, Tondelli B, Vana F, Tampellini M, Alquati P, Dogliotti L. Cytotoxic and antiproliferative activity of the single agent epirubicin versus epirubicin plus tamoxifen as primary chemotherapy in human breast cancer: a single-institution phase III trial. Endocr Relat Cancer 2005, 12:383-392. 10.1677/erc.1.00945, 15947110.
17. World Health Organization WHO Handbook for Reporting Results of Cancer Treatment 1978, WHO Offset Publication. Geneva, Switzerland: World Health Organisation, World Health Organization.
18. Generali D, Buffa FM, Berruti A, Brizzi MP, Campo L, Bonardi S, Bersiga A, Allevi G, Milani M, Aguggini S, Papotti M, Dogliotti L, Bottini A, Harris AL, Fox SB. Phosphorylated ERα, HIF-1α, and MAPK signaling as predictors of primary endocrine treatment response and resistance in patients with breast cancer. J Clin Oncol 2009, 27:227-234. 10.1200/JCO.2007.13.7083, 19064988.
19. Bottini A, Berruti A, Bersiga A, Brizzi MP, Brunelli A, Gorzegno G, DiMarco B, Aguggini S, Bolsi G, Cirillo F, Filippini L, Betri E, Bertoli G, Alquati P, Dogliotti L. p53 but not bcl-2 immunostaining is predictive of poor clinical complete response to primary chemotherapy in breast cancer patients. Clin Cancer Res 2000, 6:2751-2758.
20. Bottini A, Berruti A, Bersiga A, Brizzi MP, Bruzzi P, Aguggini S, Brunelli A, Bolsi G, Allevi G, Generali D, Betri E, Bertoli G, Alquati P, Dogliotti L. Relationship between tumour shrinkage and reduction in Ki67 expression after primary chemotherapy in human breast cancer. Br J Cancer 2001, 85:1106-1112. 10.1054/bjoc.2001.2048, 2375158, 11710821.
21. McCarty KS, Miller LS, Cox EB, Konrath J, McCarty KS. Estrogen receptor analyses. Correlation of biochemical and immunohistochemical methods using monoclonal antireceptor antibodies. Arch Pathol Lab Med 1985, 109:716-721.
22. Boddy JL, Fox SB, Han C, Campo L, Turley H, Kanga S, Malone PR, Harris AL. The androgen receptor is significantly associated with vascular endothelial growth factor and hypoxia sensing via hypoxia-inducible factors HIF-1a, HIF-2a, and the prolyl hydroxylases in human prostate cancer. Clin Cancer Res 2005, 11:7658-7663. 10.1158/1078-0432.CCR-05-0460, 16278385.
23. Couvelard A, O'Toole D, Turley H, Leek R, Sauvanet A, Degott C, Ruszniewski P, Belghiti J, Harris AL, Gatter K, Pezzella F. Microvascular density and hypoxia-inducible factor pathway in pancreatic endocrine tumours: negative correlation of microvascular density and VEGF expression with tumour progression. Br J Cancer 2005, 92:94-101. 10.1038/sj.bjc.6602245, 2361752, 15558070.
24. Ruan K, Song G, Ouyang G. Role of hypoxia in the hallmarks of human cancer. J Cell Biochem 2009, 107:1053-1062. 10.1002/jcb.22214, 19479945.
25. Semenza GL. Regulation of cancer cell metabolism by hypoxia-inducible factor 1. Semin Cancer Biol 2009, 19:12-16. 10.1016/j.semcancer.2008.11.009, 19114105.
26. Henze AT, Riedel J, Diem T, Wenner J, Flamme I, Pouyseggur J, Plate KH, Acker T. Prolyl hydroxylases 2 and 3 act in gliomas as protective negative feedback regulators of hypoxia-inducible factors. Cancer Res 2009, 70:357-366. 10.1158/0008-5472.CAN-09-1876, 20028863.
27. Minamishima YA, Moslehi J, Padera RF, Bronson RT, Liao R, Kaelin WG. A feedback loop involving the Phd3 prolyl hydroxylase tunes the mammalian hypoxic response in vivo. Mol Cell Biol 2009, 29:5729-5741. 10.1128/MCB.00331-09, 2772748, 19720742.
28. Appelhoff RJ, Tian YM, Raval RR, Turley H, Harris AL, Pugh CW, Ratcliffe PJ, Gleadle JM. Differential function of the prolyl hydroxylases PHD1, PHD2, and PHD3 in the regulation of hypoxia-inducible factor. J Biol Chem 2004, 279:38458-38465. 10.1074/jbc.M406026200, 15247232.
29. Tian YM, Mole DR, Ratcliffe PJ, Gleadle JM. Characterization of different isoforms of the HIF prolyl hydroxylase PHD1 generated by alternative initiation. Biochem J 2006, 397:179-186. 10.1042/BJ20051996, 1479752, 16509823.
30. Fong GH, Takeda K. Role and regulation of prolyl hydroxylase domain proteins. Cell Death Diff 2008, 15:635-641.
31. Kaelin WG, Ratcliffe PJ. Oxygen sensing by metazoans: the central role of the HIF hydroxylase pathway. Mol Cell 2008, 30:393-402. 10.1016/j.molcel.2008.04.009, 18498744.
32. Sobhanifar S, Aquino-Parsons C, Stanbridge EJ, Olive P. Reduced expression of hypoxia-inducible factor-1α in perinecrotic regions of solid tumors. Cancer Res 2005, 65:7259-7266. 10.1158/0008-5472.CAN-04-4480, 16103077.
33. Maragoudakis ME, Peristeris P, Missirlis E, Aletras A, Andriopoulou P, Haralabopoulos G. Inhibition of angiogenesis by anthracyclines and titanocene dichloride. Ann N Y Acad Sci 1994, 732:280-293. 10.1111/j.1749-6632.1994.tb24743.x, 7526759.
34. Takeda K, Ho VC, Takeda H, Duan LJ, Nagy A, Fong GH. Placental but not heart defects are associated with elevated hypoxia-inducible factor alpha levels in mice lacking prolyl hydroxylase domain protein 2. Mol Cell Biol 2006, 26:8336-8346. 10.1128/MCB.00425-06, 1636770, 16966370.
35. Lee S, Nakamura E, Yang H, Wei W, Linggi MS, Sajan MP, Farese RV, Freeman RS, Carter BD, Kaelin WG, Schlisio S. Neuronal apoptosis linked to EglN3 prolyl hydroxylase and familial pheochromocytoma genes: developmental culling and cancer. Cancer Cell 2005, 8:155-167. 10.1016/j.ccr.2005.06.015, 16098468.
36. Cummins EP, Berra E, Comerford KM, Ginouves A, Fitzgerald KT, Seeballuck F, Godson C, Nielsen JE, Moynagh P, Pouyssegur J, Taylor CT. Prolyl hydroxylase-1 negatively regulates IκB kinase-β, giving insight into hypoxia-induced NFκB activity. Proc Natl Acad Sci USA 2006, 103:18154-18159. 10.1073/pnas.0602235103, 1643842, 17114296.
37. Zhang Q, Gu J, Li L, Liu J, Luo B, Cheung HW, Boehm JS, Ni M, Geisen C, Root DE, Polyak K, Brown M, Richardson AL, Hahn WC, Kaelin WG, Bommi-Reddy A. Control of cyclin D1 and breast tumorigenesis by the EglN2 prolyl hydroxylase. Cancer Cell 2009, 16:413-424. 10.1016/j.ccr.2009.09.029, 2788761, 19878873.
38. Ginouves A, Ilc K, Macias N, Pouyssegur J, Berra E. PHDs overactivation during chronic hypoxia 'desensitizes' HIFα and protects cells from necrosis. Proc Natl Acad Sci USA 2008, 105:4745-4750. 10.1073/pnas.0705680105, 2290777, 18347341.