The tumour hypoxia marker pimonidazole reflects a transcriptional programme associated with aggressive prostate cancer

British Journal of Cancer

Volumn 112, Issue 2, 2015, Pages 382-390

  Ragnum, H B ^a   Vlatkovic, L ^a   Lie, A K ^a   Axcrona, K ^a   Julin, C H ^a   Frikstad, K M ^a   Hole, K H ^a   Seierstad, T ^a   Lyng, H ^a  

^a OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

Biomarker; Gene expression; Hypoxia; Pimonidazole; Proliferation; Prostate cancer

Indexed keywords

KI 67 ANTIGEN; PIMONIDAZOLE; PROSTATE SPECIFIC ANTIGEN; NITROIMIDAZOLE DERIVATIVE; TRANSCRIPTOME;

ABSENCE OF SIDE EFFECTS; ARTICLE; CANCER AGGRESSIVENESS; CANCER PROGNOSIS; CANCER STAGING; CANCER SURGERY; CANCER SURVIVAL; CELL HYPOXIA; CELL PROLIFERATION; CORRELATION ANALYSIS; DNA REPAIR; DRUG MEGADOSE; ENDOPLASMIC RETICULUM; ESSENTIAL GENE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; GLEASON SCORE; HIGH RISK PATIENT; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LABELING INDEX; LYMPH NODE METASTASIS; MAJOR CLINICAL STUDY; MALE; NUCLEAR MAGNETIC RESONANCE IMAGING; ONCOLOGICAL PARAMETERS; PHENOTYPE; PRIORITY JOURNAL; PROSTATE CANCER; PROSTATECTOMY; PROTEIN PROCESSING; ROBOTIC SURGICAL PROCEDURE; TUMOR BIOPSY; UPREGULATION; DIAGNOSTIC USE; KAPLAN MEIER METHOD; METABOLISM; MORTALITY; PATHOLOGY; PROPORTIONAL HAZARDS MODEL; PROSTATE TUMOR; STAINING; TISSUE DISTRIBUTION;

CELL HYPOXIA; HUMANS; KAPLAN-MEIER ESTIMATE; LYMPHATIC METASTASIS; MALE; NITROIMIDAZOLES; PROPORTIONAL HAZARDS MODELS; PROSTATIC NEOPLASMS; STAINING AND LABELING; TISSUE DISTRIBUTION; TRANSCRIPTOME;

EID: 84921981432     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2014.604     Document Type: Article

References (49)

1. Axcrona K, Vlatkovic L, Hovland J, Brennhovd B, Kongsgaard U, Giercksky KE (2012) Robot-assisted laparoscopic prostatectomy in a 68-year-old patient with previous heart transplantation and pelvic irradiation. J Robot Surg 6: 81-83.
2. Barentsz JO, Richenberg J, Clements R, Choyke P, Verma S, Villeirs G, Rouviere O, Logager V, Futterer JJ (2012) ESUR prostate MR guidelines 2012. Eur Radiol 22: 746-757.
3. Buffa FM, Harris AL, West CM, Miller CJ (2010) Large meta-analysis of multiple cancers reveals a common, compact and highly prognostic hypoxia metagene. Br J Cancer 102: 428-435.
4. Cai Y, Balli D, Ustiyan V, Fulford L, Hiller A, Misetic V, Zhang Y, Paluch AM, Waltz SE, Kasper S, Kalin TV (2013) Foxm1 expression in prostate epithelial cells is essential for prostate carcinogenesis. J Biol Chem 288: 22527-22541.
5. Carnell DM, Smith RE, Daley FM, Saunders MI, Bentzen SM, Hoskin PJ (2006) An immunohistochemical assessment of hypoxia in prostate carcinoma using pimonidazole: implications for radioresistance. Int J Radiat Oncol Biol Phys 65: 91-99.
6. Chandran UR, Ma C, Dhir R, Bisceglia M, Lyons-Weiler M, Liang W, Michalopoulos G, Becich M, Monzon FA (2007) Gene expression profiles of prostate cancer reveal involvement of multiple molecular pathways in the metastatic process. BMC Cancer 7: 64.
7. Chiang DY, Villanueva A, Hoshida Y, Peix J, Newell P, Minguez B, LeBlanc AC, Donovan DJ, Thung SN, Sole M, Tovar V, Alsinet C, Ramos AH, Barretina J, Roayaie S, Schwartz M, Waxman S, Bruix J, Mazzaferro V, Ligon AH, Najfeld V, Friedman SL, Sellers WR, Meyerson M, Llovet JM (2008) Focal gains of VEGFA and molecular classification of hepatocellular carcinoma. Cancer Res 68: 6779-6788.
8. Ciccia A, Elledge SJ (2010) The DNA damage response: making it safe to play with knives. Mol Cell 40: 179-204.
9. D'Amico AV, Whittington R, Malkowicz SB, Schultz D, Blank K, Broderick GA, Tomaszewski JE, Renshaw AA, Kaplan I, Beard CJ, Wein A (1998) Biochemical outcome after radical prostatectomy, external beam radiation therapy, or interstitial radiation therapy for clinically localized prostate cancer. JAMA 280: 969-974.
10. Damber JE, Aus G (2008) Prostate cancer. Lancet 371: 1710-1721.
11. Dinu I, Potter JD, Mueller T, Liu Q, Adewale AJ, Jhangri GS, Einecke G, Famulski KS, Halloran P, Yasui Y (2007) Improving gene set analysis of microarray data by SAM-GS. BMC Bioinform 8: 242.
12. Epstein JI (2010) An update of the gleason grading system. J Urol 183: 433-440.
13. Eustace A, Mani N, Span PN, Irlam JJ, Taylor J, Betts GN, Denley H, Miller CJ, Homer JJ, Rojas AM, Hoskin PJ, Buffa FM, Harris AL, Kaanders JH, West CM (2013) A 26-gene hypoxia signature predicts benefit from hypoxia-modifying therapy in laryngeal cancer but not bladder cancer. Clin Cancer Res 19: 4879-4888.
14. Fraser M, Berlin A, Bristow RG, van der Kwast T (2014) Genomic, pathological, and clinical heterogeneity as drivers of personalized medicine in prostate cancer. Urol Oncol 32 : S1078-S1439.
15. Gilkes DM, Bajpai S, Chaturvedi P, Wirtz D, Semenza GL (2013) Hypoxia-inducible factor 1 (HIF-1) promotes extracellular matrix remodeling under hypoxic conditions by inducing P4HA1, P4HA2, and PLOD2 expression in fibroblasts. J Biol Chem 288: 10819-10829.
16. Gross MW, Karbach U, Groebe K, Franko AJ, Mueller-Klieser W (1995) Calibration of misonidazole labeling by simultaneous measurement of oxygen tension and labeling density in multicellular spheroids. Int J Cancer 61: 567-573.
17. Halle C, Andersen E, Lando M, Aarnes EK, Hasvold G, Holden M, Syljuasen RG, Sundfor K, Kristensen GB, Holm R, Malinen E, Lyng H (2012) Hypoxia-induced gene expression in chemoradioresistant cervical cancer revealed by dynamic contrast-enhanced MRI. Cancer Res 72: 5285-5295.
18. Hoskin PJ, Carnell DM, Taylor NJ, Smith RE, Stirling JJ, Daley FM, Saunders MI, Bentzen SM, Collins DJ, D'Arcy JA, Padhani AP (2007) Hypoxia in prostate cancer: correlation of BOLD-MRI with pimonidazole immunohistochemistry-initial observations. Int J Radiat Oncol Biol Phys 68: 1065-1071.
19. Huang dW, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57.
20. Kim SJ, Choi H, Park SS, Chang C, Kim E (2011) Stearoyl CoA desaturase (SCD) facilitates proliferation of prostate cancer cells through enhancement of androgen receptor transactivation. Mol Cells 31: 371-377.
21. Kizaka-Kondoh S, Konse-Nagasawa H (2009) Significance of nitroimidazole compounds and hypoxia-inducible factor-1 for imaging tumor hypoxia. Cancer Sci 100: 1366-1373.
22. Koukourakis MI, Giatromanolaki A, Panteliadou M, Pouliliou SE, Chondrou PS, Mavropoulou S, Sivridis E (2014) Lactate dehydrogenase 5 isoenzyme overexpression defines resistance of prostate cancer to radiotherapy. Br J Cancer 110: 2217-2223.
23. Kuner R, Falth M, Pressinotti NC, Brase JC, Puig SB, Metzger J, Gade S, Schafer G, Bartsch G, Steiner E, Klocker H, Sultmann H (2013) The maternal embryonic leucine zipper kinase (MELK) is upregulated in high-grade prostate cancer. J Mol Med (Berl) 91: 237-248.
24. Larkin SE, Holmes S, Cree IA, Walker T, Basketter V, Bickers B, Harris S, Garbis SD, Townsend PA, ukim-Hastie C (2012) Identification of markers of prostate cancer progression using candidate gene expression. Br J Cancer 106: 157-165.
25. Lee HY, Yang EG, Park H (2013) Hypoxia enhances the expression of prostate-specific antigen by modifying the quantity and catalytic activity of Jumonji C domain-containing histone demethylases. Carcinogenesis 34: 2706-2715.
26. Markert EK, Levine AJ, Vazquez A (2012) Proliferation and tissue remodeling in cancer: the hallmarks revisited. Cell Death Dis 3: e397.
27. Massie CE, Lynch A, Ramos-Montoya A, Boren J, Stark R, Fazli L, Warren A, Scott H, Madhu B, Sharma N, Bon H, Zecchini V, Smith DM, Denicola GM, Mathews N, Osborne M, Hadfield J, Macarthur S, Adryan B, Lyons SK, Brindle KM, Griffiths J, Gleave ME, Rennie PS, Neal DE, Mills IG (2011) The androgen receptor fuels prostate cancer by regulating central metabolism and biosynthesis. EMBO J 30: 2719-2733.
28. Mense SM, Sengupta A, Zhou M, Lan C, Bentsman G, Volsky DJ, Zhang L (2006) Gene expression profiling reveals the profound upregulation of hypoxia-responsive genes in primary human astrocytes. Physiol Genom 25: 435-449.
29. Milosevic M, Warde P, Menard C, Chung P, Toi A, Ishkanian A, McLean M, Pintilie M, Sykes J, Gospodarowicz M, Catton C, Hill RP, Bristow R (2012) Tumor hypoxia predicts biochemical failure following radiotherapy for clinically localized prostate cancer. Clin Cancer Res 18: 2108-2114.
30. Mitani T, Yamaji R, Higashimura Y, Harada N, Nakano Y, Inui H (2011) Hypoxia enhances transcriptional activity of androgen receptor through hypoxia-inducible factor-1alpha in a low androgen environment. J Steroid Biochem Mol Biol 123: 58-64.
31. Park C, Kim Y, Shim M, Lee Y (2012) Hypoxia enhances ligand-occupied androgen receptor activity. Biochem Biophys Res Commun 418: 319-323.
32. Ragnum HB, Roe K, Holm R, Vlatkovic L, Nesland JM, Aarnes EK, Ree AH, Flatmark K, Seierstad T, Lilleby W, Lyng H (2013) Hypoxia-independent downregulation of hypoxia-inducible factor 1 targets by androgen deprivation therapy in prostate cancer. Int J Radiat Oncol Biol Phys 87: 753-760.
33. Sartori DA, Chan DW (2014) Biomarkers in prostate cancer: what's new? Curr Opin Oncol 26: 259-264.
34. Sboner A, Demichelis F, Calza S, Pawitan Y, Setlur SR, Hoshida Y, Perner S, Adami HO, Fall K, Mucci LA, Kantoff PW, Stampfer M, Andersson SO, Varenhorst E, Johansson JE, Gerstein MB, Golub TR, Rubin MA, Andren O (2010) Molecular sampling of prostate cancer: a dilemma for predicting disease progression. BMC Med Genom 3: 8.
35. Shariat SF, Lotan Y, Saboorian H, Khoddami SM, Roehrborn CG, Slawin KM, Ashfaq R (2004) Survivin expression is associated with features of biologically aggressive prostate carcinoma. Cancer 100: 751-757.
36. Sobin LH, Gospodarowicz MK, Wittekind C (2009) TNM Classification of Malignant Tumours. 7th ed, John Wiley & Sons Ltd: West Sussex, UK.
37. Sonn GA, Margolis DJ, Marks LS (2014) Target detection: magnetic resonance imaging-ultrasound fusion-guided prostate biopsy. Urol Oncol 32: S1078-S1439.
38. Srigley JR (2006) Key issues in handling and reporting radical prostatectomy specimens. Arch Pathol Lab Med 130: 303-317.
39. Starmans MH, Krishnapuram B, Steck H, Horlings H, Nuyten DS, van d V, Seigneuric R, Buffa FM, Harris AL, Wouters BG, Lambin P (2008) Robust prognostic value of a knowledge-based proliferation signature across large patient microarray studies spanning different cancer types. Br J Cancer 99: 1884-1890.
40. Toubaji A, Sutcliffe S, Chaux A, Lecksell K, Hicks J, De Marzo AM, Platz EA, Netto GJ (2012) Immunohistochemical expression of minichromosome maintenance complex protein 2 predicts biochemical recurrence in prostate cancer: a tissue microarray and digital imaging analysis-based study of 428 cases. Hum Pathol 43: 1852-1865.
41. Toustrup K, Sorensen BS, Nordsmark M, Busk M, Wiuf C, Alsner J, Overgaard J (2011) Development of a hypoxia gene expression classifier with predictive impact for hypoxic modification of radiotherapy in head and neck cancer. Cancer Res 71: 5923-5931.
42. Turaka A, Buyyounouski MK, Hanlon AL, Horwitz EM, Greenberg RE, Movsas B (2012) Hypoxic prostate/muscle PO2 ratio predicts for outcome in patients with localized prostate cancer: long-term results. Int J Radiat Oncol Biol Phys 82: e433-e439.
43. Urbanucci A, Sahu B, Seppala J, Larjo A, Latonen LM, Waltering KK, Tammela TL, Vessella RL, Lahdesmaki H, Janne OA, Visakorpi T (2012) Overexpression of androgen receptor enhances the binding of the receptor to the chromatin in prostate cancer. Oncogene 31: 2153-2163.
44. van der Kwast TH, Amin MB, Billis A, Epstein JI, Griffiths D, Humphrey PA, Montironi R, Wheeler TM, Srigley JR, Egevad L, Delahunt B (2011) International Society of Urological Pathology (ISUP) Consensus Conference on Handling and Staging of Radical Prostatectomy Specimens. Working group 2: T2 substaging and prostate cancer volume. Mod Pathol 24: 16-25.
45. van Laarhoven HW, Kaanders JH, Lok J, Peeters WJ, Rijken PF, Wiering B, Ruers TJ, Punt CJ, Heerschap A, van der Kogel AJ (2006) Hypoxia in relation to vasculature and proliferation in liver metastases in patients with colorectal cancer. Int J Radiat Oncol Biol Phys 64: 473-482.
46. Verhoven B, Yan Y, Ritter M, Khor LY, Hammond E, Jones C, Amin M, Bahary JP, Zeitzer K, Pollack A (2013) Ki-67 is an independent predictor of metastasis and cause-specific mortality for prostate cancer patients treated on Radiation Therapy Oncology Group (RTOG) 94-08. Int J Radiat Oncol Biol Phys 86: 317-323.
47. Wijffels KI, Marres HA, Peters JP, Rijken PF, van der Kogel AJ, Kaanders JH (2008) Tumour cell proliferation under hypoxic conditions in human head and neck squamous cell carcinomas. Oral Oncol 44: 335-344.
48. Winter SC, Buffa FM, Silva P, Miller C, Valentine HR, Turley H, Shah KA, Cox GJ, Corbridge RJ, Homer JJ, Musgrove B, Slevin N, Sloan P, Price P, West CM, Harris AL (2007) Relation of a hypoxia metagene derived from head and neck cancer to prognosis of multiple cancers. Cancer Res 67: 3441-3449.
49. Xia L, Mo P, Huang W, Zhang L, Wang Y, Zhu H, Tian D, Liu J, Chen Z, Zhang Y, Chen Z, Hu H, Fan D, Nie Y, Wu K (2012) The TNF-alpha/ROS/HIF-1-induced upregulation of FoxMI expression promotes HCC proliferation and resistance to apoptosis. Carcinogenesis 33: 2250-2259.