The prognostic impact of a combined carbonic anhydrase IX and Ki67 signature in oral squamous cell carcinoma

British Journal of Cancer

Volumn 109, Issue 7, 2013, Pages 1859-1866

  Klimowicz, A C ^a,b,d   Bose, P ^a   Petrillo, S K ^b   Magliocco, A M ^a,b,e   Dort, J C ^a   Brockton, N T ^a,c  

^a UNIVERSITY OF CALGARY   (Canada)

^b TOM BAKER CANCER CENTRE   (Canada)

^c ALBERTA HEALTH SERVICES   (Canada)

^d BOEHRINGER INGELHEIM PHARMACEUTICALS INC   (United States)

^e H LEE MOFFITT CANCER CENTER AND RESEARCH INSTITUTE   (United States)

Author keywords

AQUA; CAIX; head and neck squamous cell carcinoma; hypoxia; Ki67; oral squamous cell carcinoma

Indexed keywords

ANTINEOPLASTIC AGENT; CARBONATE DEHYDRATASE IX; KI 67 ANTIGEN; PROTEIN BAX;

ADULT; ARTICLE; CANCER CHEMOTHERAPY; CANCER PROGNOSIS; CANCER RADIOTHERAPY; CANCER SURGERY; CANCER SURVIVAL; DISEASE SPECIFIC SURVIVAL; FEMALE; FLUORESCENCE; HUMAN; IMMUNOHISTOCHEMISTRY; LYMPH NODE METASTASIS; MAJOR CLINICAL STUDY; MALE; MOUTH SQUAMOUS CELL CARCINOMA; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETROSPECTIVE STUDY; SMOKING;

ANTIGENS, NEOPLASM; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; CARBONIC ANHYDRASES; CARCINOMA, SQUAMOUS CELL; CELL HYPOXIA; DRUG RESISTANCE, NEOPLASM; FEMALE; HUMANS; KI-67 ANTIGEN; MALE; MIDDLE AGED; MOUTH NEOPLASMS; PROGNOSIS; SURVIVAL; TREATMENT OUTCOME; TUMOR MARKERS, BIOLOGICAL;

EID: 84885174952     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/bjc.2013.533     Document Type: Article

References (44)

1. BelAiba RS, Bonello S, Zahringer C, Schmidt S, Hess J, Kietzmann T, Gorlach A (2007) Hypoxia up-regulates hypoxia-inducible factor-1 alpha transcription by involving phosphatidylinositol 3-kinase and nuclear factor kappa B in pulmonary artery smooth muscle cells. Mol Biol Cell 18(12): 4691-4697.
2. Bose P, Brockton NT, Dort JC (2013) Head and neck cancer: from anatomy to biology. Int J Cancer 133(9): 2013-2023.
3. Bose P, Klimowicz AC, Kornaga E, Petrillo SK, Matthews TW, Chandarana S, Magliocco AM, Brockton NT, Dort JC (2012) Bax expression measured by AQUAnalysis is an independent prognostic marker in oral squamous cell carcinoma. BMC Cancer 12: 332.
4. Brockton N, Dort J, Lau H, Hao D, Brar S, Klimowicz A, Petrillo S, Diaz R, Doll C, Magliocco A (2011) High stromal carbonic anhydrase IX expression is associated with decreased survival in p16-negative head-andneck tumors. Int J Radiat Oncol Biol Phys 80: 249-257.
5. Brockton NT, Klimowicz AC, Bose P, Petrillo SK, Konno M, Rudmik L, Dean M, Nakoneshny SC, Matthews TW, Chandarana S, Lau HY, Magliocco AM, Dort JC (2012) High stromal carbonic anhydrase IX expression is associated with nodal metastasis and decreased survival in patients with surgically-treated oral cavity squamous cell carcinoma. Oral Oncol 48(7): 615-622.
6. Camp RL, Chung GG, Rimm DL (2002) Automated subcellular localization and quantification of protein expression in tissue microarrays. Nat Med 8(11): 1323-1327.
7. Camp RL, Neumeister V, Rimm DL (2008) A decade of tissue microarrays: progress in the discovery and validation of cancer biomarkers. J Clin Oncol 26(34): 5630-5637.
8. Campana JP, Meyers AD (2006) The surgical management of oral cancer. Otolaryngol Clin North Am 39(2): 331-348.
9. Chen L, Gajendrareddy PK, DiPietro LA (2012) Differential expression of HIF-1 alpha in skin and mucosal wounds. J Dent Res 91(9): 871-876.
10. Chi JT, Wang Z, Nuyten DS, Rodriguez EH, Schaner ME, Salim A, Wang Y, Kristensen GB, Helland A, Borresen-Dale AL, Giaccia A, Longaker MT, Hastie T, Yang GP, van dV, Brown PO (2006) Gene expression programs in response to hypoxia: cell type specificity and prognostic significance in human cancers. PLoS Med 3(3): e47.
11. Chrastina A (2003) High cell density-mediated pericellular hypoxia is a crucial factor inducing expression of the intrinsic hypoxia marker CA IX in vitro in HeLa cells. Neoplasma 50(4): 251-256.
12. Cuzick J, Dowsett M, Pineda S, Wale C, Salter J, Quinn E, Zabaglo L, Mallon E, Green AR, Ellis IO, Howell A, Buzdar AU, Forbes JF (2011) Prognostic value of a combined estrogen receptor, progesterone receptor, Ki-67, and human epidermal growth factor receptor 2 immunohistochemical score and comparison with the genomic health recurrence score in early breast cancer. J Clin Oncol 29(32): 4273-4278.
13. Erler JT, Cawthorne CJ, Williams KJ, Koritzinsky M, Wouters BG, Wilson C, Miller C, Demonacos C, Stratford IJ, Dive C (2004) Hypoxia-mediated down-regulation of bid and bax in tumors occurs via hypoxia-inducible factor 1-dependent and-independent mechanisms and contributes to drug resistance. Mol Cell Biol 24(7): 2875-2889.
14. Gustavson MD, Bourke-Martin B, Reilly DM, Cregger M, Williams C, Tedeschi G, Pinard R, Christiansen J (2009) Development of an unsupervised pixel-based clustering algorithm for compartmentalization of immunohistochemical expression using Automated QUantitative Analysis. Appl Immunohistochem Mol Morphol 17(4): 329-337.
15. Harris AL (2002) Hypoxia-a key regulatory factor in tumour growth. Nat Rev Cancer 2(1): 38-47.
16. Hoogsteen IJ, Marres HA, Wijffels KI, Rijken PF, Peters JP, van den Hoogen FJ, Oosterwijk E, van der Kogel AJ, Kaanders JH (2005) Colocalization of carbonic anhydrase 9 expression and cell proliferation in human head and neck squamous cell carcinoma. Clin Cancer Res 11(1): 97-106.
17. Hoogsteen IJ, Marres HAM, Bussink J, van der Kogel AJ, Kaanders JHAM (2007) Tumor microenvironment in head and neck squamous cell carcinomas: Predictive value and clinical relevance of hypoxic markers. A review. Head Neck 29(6): 591-604.
18. Ivanov SV, Kuzmin I, Wei MH, Pack S, Geil L, Johnson BE, Stanbridge EJ, Lerman MI (1998) Down-regulation of transmembrane carbonic anhydrases in renal cell carcinoma cell lines by wild-type von Hippel-Lindau transgenes. Proc Natl Acad Sci USA 95(21): 12596-12601.
19. Janssen HL, Haustermans KM, Balm AJ, Begg AC (2005) Hypoxia in head and neck cancer: How much, how important? Head Neck 27(7): 622-638.
20. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D (2011) Global cancer statistics. CA Cancer J Clin 61(2): 69-90.
21. Jubb AM, Buffa FM, Harris AL (2010) Assessment of tumour hypoxia for prediction of response to therapy and cancer prognosis. J Cell Mol Med 14(1-2): 18-29.
22. Kaanders JHAM, Wijffels KIEM, Marres HAM, Ljungkvist ASE, Pop LAM, van den Hoogen FJA, De Wilde PCM, Bussink J, Raleigh JA, van der Kogel AJ (2002) Pimonidazole binding and tumor vascularity predict for treatment outcome in head and neck cancer. Cancer Res 62(23): 7066-7074.
23. Kaluz S, Kaluzova M, Chrastina A, Olive PL, Pastorekova S, Pastorek J, Lerman MI, Stanbridge EJ (2002) Lowered oxygen tension induces expression of the hypoxia marker MN/carbonic anhydrase IX in the absence of hypoxia-inducible factor 1 alpha stabilization: A role for phosphatidylinositol 3 '-kinase. Cancer Res 62(15): 4469-4477.
24. Kaluz S, Kaluzova M, Liao SY, Lerman M, Stanbridge EJ (2009) Transcriptional control of the tumor-and hypoxia-marker carbonic anhydrase 9: a one transcription factor (HIF-1) show? Biochim Biophys Acta 1795(2): 162-172.
25. Klimowicz AC, Bose P, Nakoneshny SC, Dean M, Huang LL, Chandarana S, Magliocco AM, Matthews TW, Brockton NT, Dort JC (2012) Basal Ki67 expression measured by digital image analysis is optimal for prognostication in oral squamous cell carcinoma. Eur J Cancer 48(14): 2166-2174.
26. Kondo Y, Yoshikawa K, Omura Y, Shinohara A, Kazaoka Y, Sano J, Mizuno Y, Yokoi T, Yamada S (2011) Clinicopathological significance of carbonic anhydrase 9, glucose transporter-1, Ki-67 and p53 expression in oral squamous cell carcinoma. Oncol Rep 25(5): 1227-1233.
27. Laughner E, Taghavi P, Chiles K, Mahon PC, Semenza GL (2001) HER2 (neu) signaling increases the rate of hypoxia-inducible factor 1 alpha (HIF-1 alpha) synthesis: novel mechanism for HIF-1-mediated vascular endothelial growth factor expression. Mol Cell Biol 21(12): 3995-4004.
28. Ljungkvist ASE, Bussink J, Rijken P, Kaanders J, van der Kogel AJ, Denekamp J (2002) Vascular architecture, hypoxia, and proliferation in first generation xenografts of human head-and-neck squamous cell carcinomas. Int J Radiat Oncol Biol Phys 54(1): 215-228.
29. Mayer A, Hockel M, Vaupel P (2005) Carbonic anhydrase IX expression and tumor oxygenation status do not correlate at the microregional level in locally-advanced cancers of the uterine cervix. Clin Cancer Res 11(20): 7220-7225.
30. McDonald PC, Winum JY, Supuran CT, Dedhar S (2012) Recent developments in targeting carbonic anhydrase IX for cancer therapeutics. Oncotarget 3(1): 84-97.
31. McShane LM, Altman DG, Sauerbrei W, Taube SE, Gion M, Clark GM (2005) Reporting recommendations for tumor marker prognostic studies. J Clin Oncol 23(36): 9067-9072.
32. Nelson DA, Tan TT, Rabson AB, Anderson D, Degenhardt K, White E (2004) Hypoxia and defective apoptosis drive genomic instability and tumorigenesis. Genes Dev 18(17): 2095-2107.
33. Pastorekova S, Ratcliffe PJ, Pastorek J (2008) Molecular mechanisms of carbonic anhydrase IX-mediated pH regulation under hypoxia. BJU Int 101: 8-15.
34. Pore N, Jiang ZB, Shu HK, Bernhard E, Kao GD, Maity A (2006) Akt1 activation can augment hypoxia-inducible factor-1 alpha expression by increasing protein translation through a mammalian target of rapamycin-independent pathway. Mol Cancer Res 4(7): 471-479.
35. Ross JS, Hatzis C, Symmans WF, Pusztai L, Hortobagyi GN (2008) Commercialized multigene predictors of clinical outcome for breast cancer. Oncologist 13(5): 477-493.
36. Sobhanifar S, Aquino-Parsons C, Stanbridge EJ, Olive P (2005) Reduced Expression of Hypoxia-inducible factor-1a in perinecrotic regions of solid tumors. Cancer Res 65(16): 7259-7266.
37. Sorensen BS, Hao J, Overgaard J, Vorum H, Honore B, Alsner J, Horsman MR (2005) Influence of oxygen concentration and pH on expression of hypoxia induced genes. Radiother Oncol 76(2): 187-193.
38. Sowter HM, Raval RR, Moore JW, Ratcliffe PJ, Harris AL (2003) Predominant role of hypoxia-inducible transcription factor (Hif)-1alpha versus Hif-2alpha in regulation of the transcriptional response to hypoxia. Cancer Res 63(19): 6130-6134.
39. Sparano A, Quesnelle KM, Kumar MS, Wang Y, Sylvester AJ, Feldman M, Sewell DA, Weinstein GS, Brose MS (2006) Genome-wide profiling of oral squamous cell carcinoma by array-based comparative genomic hybridization. Laryngoscope 116(5): 735-741.
40. Sullivan R, Graham CH (2007) Hypoxia-driven selection of the metastatic phenotype. Cancer Metastasis Rev 26(2): 319-331.
41. Toustrup K, Sorensen BS, Alsner J, Overgaard J (2012) Hypoxia gene expression signatures as prognostic and predictive markers in head and neck radiotherapy. Semin Radiat Oncol 22(2): 119-127.
42. Vaupel P, Mayer A (2007) Hypoxia in cancer: significance and impact on clinical outcome. Cancer Metastasis Rev 26(2): 225-239.
43. Wilson WR, Hay MP (2011) Targeting hypoxia in cancer therapy. Nat Rev Cancer 11(6): 393-410.
44. Wykoff CC, Beasley NJP, Watson PH, Turner KJ, Pastorek J, Sibtain A, Wilson GD, Turley H, Talks KL, Maxwell PH, Pugh CW, Ratcliffe PJ, Harris AL (2000) Hypoxia-inducible expression of tumor-associated carbonic anhydrases. Cancer Res 60(24): 7075-7083.