Nuclear HIF1A expression is strongly prognostic in sporadic but not familial male breast cancer

Modern Pathology

Volumn 27, Issue 9, 2014, Pages 1223-1230

  Deb, Siddhartha ^a,b   Johansson, Ida ^c   Byrne, David ^a   Nilsson, Cecilia ^d   Constable, Leonie ^e   Fjällskog, Marie Louise ^f   Dobrovic, Alexander ^a,b   Hedenfalk, Ingrid ^c   Fox, Stephen B ^a,b  

^a PETER MACCALLUM CANCER CENTRE   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c LUND UNIVERSITY   (Sweden)

^d CENTRAL HOSPITAL   (Sweden)

^e MELBOURNE PATHOLOGY   (Australia)

^f UPPSALA UNIVERSITY   (Sweden)

Author keywords

BRCA1; BRCA2; BRCAX; CA9; Familial; HIF1A; Male breast cancer

Indexed keywords

BRCA1 PROTEIN; BRCA2 PROTEIN; CARBONATE DEHYDRATASE IX; HYPOXIA INDUCIBLE FACTOR 1ALPHA; CA9 PROTEIN, HUMAN; CARBONATE DEHYDRATASE; TUMOR ANTIGEN; TUMOR MARKER;

AGED; ARTICLE; AUSTRALIAN; CANCER PROGNOSIS; CANCER STAGING; COHORT ANALYSIS; COMPARATIVE STUDY; DISEASE SPECIFIC SURVIVAL; FAMILIAL MALE BREAST CANCER; FEMALE; GENE MUTATION; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MALE; MALE BREAST CANCER; NEW ZEALAND; ONCOLOGICAL PARAMETERS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SPORADIC MALE BREAST CANCER; TUMOR MICROENVIRONMENT; TUMOR VOLUME; BREAST NEOPLASMS, MALE; BREAST TUMOR; DISEASE FREE SURVIVAL; GENETIC PREDISPOSITION; GENETICS; GERMLINE MUTATION; METABOLISM; MORTALITY; PATHOLOGY; PROGNOSIS; TISSUE MICROARRAY;

AGED; ANTIGENS, NEOPLASM; BRCA1 PROTEIN; BRCA2 PROTEIN; BREAST NEOPLASMS; BREAST NEOPLASMS, MALE; CARBONIC ANHYDRASES; DISEASE-FREE SURVIVAL; FEMALE; GENETIC PREDISPOSITION TO DISEASE; GERM-LINE MUTATION; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; IMMUNOHISTOCHEMISTRY; MALE; PROGNOSIS; TISSUE ARRAY ANALYSIS; TUMOR MARKERS, BIOLOGICAL;

EID: 84925228811     PISSN: 08933952     EISSN: 15300285     Source Type: Journal    
DOI: 10.1038/modpathol.2013.231     Document Type: Article

References (38)

1. Deb S, Jene N, Kconfab I, et al. Genotypic and phenotypic analysis of male breast cancer shows under representation of the HER2 and basal subtypes in BRCA-associated carcinomas. BMC cancer 2012;12:510.
2. Johansson I, Nilsson C, Berglund P, et al. Gene expression profiling of primary male breast cancers reveals two unique subgroups and identifies N-acetyltransferase-1 (NAT1) as a novel prognostic biomarker. Breast Cancer Res: BCR 2012;14:R31.
3. Ottini L, Silvestri V, Rizzolo P, et al. Clinical and pathologic characteristics of BRCA-positive and BRCA-negative male breast cancer patients: results from a collaborative multicenter study in Italy. Breast Cancer Res Treat 2012;134:411-418.
4. Deb S, Do H, Byrne D, et al. PIK3CA mutations are frequently observed in BRCAX but not BRCA2 - associated male breast cancer. Breast Cancer Res 2013;15:R69.
5. Harris AL. Hypoxia-a key regulatory factor in tumour growth. Nat Rev Cancer 2002;2:38-47.
6. Tan EY, Yan M, Campo L, et al. The key hypoxia regulated gene CAIX is upregulated in basal-like breast tumours and is associated with resistance to chemotherapy. Br J Cancer 2009;100:405-411.
7. Vaapil M, Helczynska K, Villadsen R, et al. Hypoxic conditions induce a cancer-like phenotype in human breast epithelial cells. PloS One 2012;7:e46543.
8. Wang GL, Jiang BH, Rue EA, et al. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc Natl Acad Sci USA 1995;92:5510-5514.
9. Srinivas V, Zhang LP, Zhu XH, et al. Characterization of an oxygen/redox-dependent degradation domain of hypoxia-inducible factor alpha (HIF-alpha) proteins. BiochemBiophy Res Commun 1999;260:557-561.
10. Huang LE, Arany Z, Livingston DM, et al. Activation of hypoxia-inducible transcription factor depends primarily upon redox-sensitive stabilization of its alpha subunit. J Biol Chem 1996;271:32253-32259.
11. Kallio PJ, Pongratz I, Gradin K, et al. Activation of hypoxia-inducible factor 1alpha: post-transcriptional regulation and conformational change by recruitment of the Arnt transcription factor. Proc Natl Acad Sci USA 1997;94:5667-5672.
12. Vaupel P. The role of hypoxia-induced factors in tumor progression. Oncologist 2004;9(Suppl 5):10-17.
13. Ke Q, Costa M. Hypoxia-inducible factor-1 (HIF-1). Mol Pharmacol 2006;70:1469-1480.
14. Dales JP, Garcia S, Meunier-Carpentier S, et al. Overexpression of hypoxia-inducible factor HIF-1alpha predicts early relapse in breast cancer: retrospective study in a series of 745 patients. Int J Cancer 2005;116:734-739.
15. Generali D, Berruti A, Brizzi MP, et al. Hypoxia-inducible factor-1alpha 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.
16. Yan M, Rayoo M, Takano EA, et al. BRCA1 tumours correlate with a HIF-1alpha phenotype and have a poor prognosis through modulation of hydroxylase enzyme profile expression. Br J Cancer 2009;101:1168-1174.
17. Neumeister VM, Sullivan CA, Lindner R, et al. Hypoxia-induced protein CAIX is associated with somatic loss of BRCA1 protein and pathway activity in triple negative breast cancer. Breast Cancer Res Treat 2012;136:67-75.
18. Kornegoor R, Verschuur-Maes AH, Buerger H, et al. Fibrotic focus and hypoxia in male breast cancer. Mod Pathol 2012;25:1397-1404.
19. Nilsson C, Koliadi A, Johansson I, et al. High proliferation is associated with inferior outcome in male breast cancer patients. Mod Pathol 2013;26:87-94.
20. Lakhani SR, Ellis IO, Schnitt SJ, et al. WHO classification of tumours of the breast. IARC: Lyon, 2012.
21. McShane LM, Altman DG, Sauerbrei W, et al. REporting recommendations for tumor MARKer prognostic studies (REMARK). Breast Cancer Res Treat 2006;100:229-235.
22. Boddy JL, Fox SB, Han C, et 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.
23. Couvelard A, Deschamps L, Rebours V, et al. Overexpression of the oxygen sensors PHD-1, PHD-2, PHD-3, and FIH Is associated with tumor aggressiveness in pancreatic endocrine tumors. Clin Cancer Res 2008;14:6634-6639.
24. Soilleux EJ, Turley H, Tian YM, et 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.
25. Bos R, Zhong H, Hanrahan CF, et al. Levels of hypoxia-inducible factor-1 alpha during breast carcinogenesis. J Natl Cancer Inst 2001;93:309-314.
26. van der Groep P, Bouter A, Menko FH, et al. High frequency of HIF-1alpha overexpression in BRCA1 related breast cancer. Breast Cancer Res Treat 2008;111:475-480.
27. Vleugel MM, Greijer AE, Shvarts A, et al. Differential prognostic impact of hypoxia induced and diffuse HIF-1alpha expression in invasive breast cancer. J Clin Pathol 2005;58:172-177.
28. Jiang BH, Semenza GL, Bauer C, et al. Hypoxia-inducible factor 1 levels vary exponentially over a physiologically relevant range of O2 tension. Am J Physiol 1996;271:C1172-C1180.
29. Rafajova M, Zatovicova M, Kettmann R, et al. Induction by hypoxia combined with low glucose or low bicarbonate and high posttranslational stability upon reoxygenation contribute to carbonic anhydrase IX expression in cancer cells. Int J Oncol 2004;24:995-1004.
30. Turner KJ, Crew JP, Wykoff CC, et al. The hypoxia-inducible genes VEGF and CA9 are differentially regulated in superficial vs invasive bladder cancer. Br J Cancer 2002;86:1276-1282.
31. Currie MJ, Hanrahan V, Gunningham SP, et al. Expression of vascular endothelial growth factor D is associated with hypoxia inducible factor (HIF-1alpha) and the HIF-1alpha target gene DEC1, but not lymph node metastasis in primary human breast carcinomas. J Clin Pathol 2004;57:829-834.
32. van Diest PJ, Vleugel MM, van der Groep P, et al. VEGF-D and HIF-1alpha in breast cancer. J Clin Pathol 2005;58:335 author reply 6.
33. Maity A, Sall W, Koch CJ, et al. Low pO2 and beta-estradiol induce VEGF in MCF-7 and MCF-7-5C cells: relationship to in vivo hypoxia. Breast Cancer Res Treat 2001;67:51-60.
34. Marchal F, Salou M, Marchal C, et al. Men with breast cancer have same disease-specific and event-free survival as women. Ann Surg Oncol 2009;16:972-978.
35. Ding YC, Steele L, Kuan CJ, et al. Mutations in BRCA2 and PALB2 in male breast cancer cases from the United States. Breast Cancer Res Treat 2011;126:771-778.
36. Fox SB, Generali D, Berruti A, et al. The prolyl hydroxylase enzymes are positively associated with hypoxia-inducible factor-1alpha and vascular endothelial growth factor in human breast cancer and alter in response to primary systemic treatment with epirubicin and tamoxifen. Breast Cancer Res: BCR 2011;13:R16.
37. Lundgren K, Holm C, Landberg G. Hypoxia and breast cancer: prognostic and therapeutic implications. Cell Mol Life Sci 2007;64:3233-3247.
38. Milani M, Harris AL. Targeting tumour hypoxia in breast cancer. Eur J Cancer (Oxford, England: 1990) 2008;44:2766-2773.