Hypoxia-inducible factor-1α and -2α are expressed in most rectal cancers but only hypoxia-inducible factor-1α is associated with prognosis

British Journal of Cancer

Volumn 100, Issue 10, 2009, Pages 1666-1673

  Rasheed, S ^a   Harris, A L ^b   Tekkis, P P ^a,c   Turley, H ^b   Silver, A ^d   McDonald, P J ^a   Talbot, I C ^a   Glynne Jones, R ^a   Northover, J M A ^a   Guenther, T ^a  

^a ST MARK S HOSPITAL   (United Kingdom)

^b JOHN RADCLIFFE HOSPITAL   (United Kingdom)

^c CHELSEA AND WESTMINSTER HOSPITAL   (United Kingdom)

^d QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Angiogenesis; HIF 1a and HIF 2a; Hypoxia; Microvessel density; Rectal cancer

Indexed keywords

CD34 ANTIBODY; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; PROTEIN ANTIBODY;

ADULT; ADVANCED CANCER; ARTICLE; CANCER INVASION; CANCER RECURRENCE; CANCER SURGERY; CANCER SURVIVAL; CONTROLLED STUDY; DISEASE FREE SURVIVAL; DISEASE MARKER; FEMALE; FOLLOW UP; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MALE; MICROVASCULATURE; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; RECTUM CARCINOMA; RECTUM SURGERY; SURVIVAL RATE; SURVIVAL TIME;

ADENOCARCINOMA; ADULT; AGED; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; DISEASE PROGRESSION; FEMALE; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MALE; MIDDLE AGED; NEOPLASM STAGING; NEOVASCULARIZATION, PATHOLOGIC; PROGNOSIS; RECTAL NEOPLASMS; SURVIVAL ANALYSIS;

EID: 66149119317     PISSN: 00070920     EISSN: 15321827     Source Type: Journal    
DOI: 10.1038/sj.bjc.6605026     Document Type: Article

References (50)

1. American Cancer Society (2006) Cancer Facts and Figures. American Cancer Society: Atlanta
2. Aprelikova O, Chandramouli GV, Wood M, Vasselli JR, Riss J, Maranchie JK, Linehan WM, Barrett JC (2004) Regulation of HIF prolyl hydroxylases by hypoxia-inducible factors. J Cell Biochem 92: 491-501
3. Birner P, Schindl M, Obermair A, Plank C, Breitenecker G, Oberhuber G (2000) Overexpression of hypoxia-inducible factor 1alpha is a marker for an unfavorable prognosis in early-stage invasive cervical cancer. Cancer Res 60: 4693-4696
4. Blancher C, Moore JW, Talks KL, Houlbrook S, Harris AL (2000) Relationship of hypoxia-inducible factor (HIF)-1alpha and HIF-2alpha expression to vascular endothelial growth factor induction and hypoxia survival in human breast cancer cell lines. Cancer Res 60: 7106-7113
5. Bossi P, Viale G, Lee AK, Alfano R, Coggi G, Bosari S (1995) Angiogenesis in colorectal tumors: microvessel quantitation in adenomas and carcinomas with clinicopathological correlations. Cancer Res 55: 5049-5053
6. 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, Keshet E (1998) Role of HIF-1alpha in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis. Nature 394: 485-490
7. Carracedo A, Lorente M, Egia A, Blazquez C, Garcia S, Giroux V, Malicet C, Villuendas R, Gironella M, Gonzalez-Feria L, Piris MA, Iovanna JL, Guzman M, Velasco G (2006) The stress-regulated protein p8 mediates cannabinoid-induced apoptosis of tumor cells. Cancer Cell 9: 301-312
8. Chen YB, Wan DS, Zhan YQ, Zhou ZW, Li W, Chen G (2004) Correlation of tumor microvessel density to metastasis and recurrence of rectal cancer. Ai Zheng 23: 1203-1206
9. Choi HJ, Hyun MS, Jung GJ, Kim SS, Hong SH (1998) Tumor angiogenesis as a prognostic predictor in colorectal carcinoma with special reference to mode of metastasis and recurrence. Oncology 55: 575-581
10. Chua YJ, Cunningham D (2006) Emerging therapies for rectal cancer. Colorectal Dis 8(Suppl 3): 18-20
11. Cleven AH, van Engeland M, Wouters BG, de Bruine AP (2007) Stromal expression of hypoxia-regulated proteins is an adverse prognostic factor in colorectal carcinomas. Cell Oncol 29: 229-240
12. Conway EM, Collen D, Carmeliet P (2001) Molecular mechanisms of blood vessel growth. Cardiovasc Res 49: 507-521
13. Dahlberg M, Pahlman L, Bergstrom R, Glimelius B (1998) Improved survival in patients with rectal cancer: a population-based register study. Br J Surg 85: 515-520
14. Giatromanolaki A, Harris AL (2001) Tumour hypoxia, hypoxia signaling pathways and hypoxia inducible factor expression in human cancer. Anticancer Res 21: 4317-4324
15. Gulubova M, Vlaykova T (2007) Prognostic significance of mast cell number and microvascular density for the survival of patients with primary colorectal cancer. J Gastroenterol Hepatol [E-pub ahead of print July 2007]
16. Iyer NV, Kotch LE, Agani F, Leung SW, Laughner E, Wenger RH, Gassmann M, Gearhart JD, Lawler AM, Yu AY, Semenza GL (1998) Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1 alpha. Genes Dev 12: 149-162
17. Jiang CQ, Liu ZS, Qian Q, He YM, Yuan YF, Ai ZL (2003a) [Relationship of hypoxia-inducible factor 1 alpha (HIF-1alpha) gene expression with vascular endothelial growth factor (VEGF) and microvessel density (MVD) in human colorectal adenoma and adenocarcinoma]. Ai Zheng 22: 1170-1174
18. Jiang YA, Fan LF, Jiang CQ, Zhang YY, Luo HS, Tang ZJ, Xia D, Wang M (2003b) Expression and significance of PTEN, hypoxia-inducible factor-1 alpha in colorectal adenoma and adenocarcinoma. World J Gastroenterol 9: 491-494
19. Kaidi A, Williams AC, Paraskeva C (2007) Interaction between beta-catenin and HIF-1 promotes cellular adaptation to hypoxia. Nat Cell Biol 9: 210-217
20. Kivela AJ, Parkkila S, Saarnio J, Karttunen TJ, Kivela J, Parkkila AK, Bartosova M, Mucha V, Novak M, Waheed A, Sly WS, Rajaniemi H, Pastorekova S, Pastorek J (2005) Expression of von Hippel-Lindau tumor suppressor and tumor-associated carbonic anhydrases IX and XII in normal and neoplastic colorectal mucosa. World J Gastroenterol 11: 2616-2625
21. Klatte T, Seligson DB, Riggs SB, Leppert JT, Berkman MK, Kleid MD, Yu H, Kabbinavar FF, Pantuck AJ, Belldegrun AS (2007) Hypoxia-inducible factor 1 alpha in clear cell renal cell carcinoma. Clin Cancer Res 13: 7388-7393
22. Kmietowicz Z (2004) British cancer death rates fell by 12% between 1972 and 2002. Bmj 328: 303
23. Koukourakis MI, Giatromanolaki A, Sivridis E, Simopoulos C, Turley H, Talks K, Gatter KC, Harris AL (2002) Hypoxia-inducible factor (HIF1A and HIF2A), angiogenesis, and chemoradiotherapy outcome of squamous cell head-and-neck cancer. Int J Radiat Oncol Biol Phys 53: 1192-1202
24. Kuwai T, Kitadai Y, Tanaka S, Onogawa S, Matsutani N, Kaio E, Ito M, Chayama K (2003) Expression of hypoxia-inducible factor-1alpha is associated with tumor vascularization in human colorectal carcinoma. Int J Cancer 105: 176-181
25. Leek RD, Talks KL, Pezzella F, Turley H, Campo L, Brown NS, Bicknell R, Taylor M, Gatter KC, Harris AL (2002) Relation of hypoxia-inducible factor-2 alpha (HIF-2 alpha) expression in tumor-infiltrative macro-phages to tumor angiogenesis and the oxidative thymidine phosphory-lase pathway in Human breast cancer. Cancer Res 62: 1326-1329
26. Li C, Gardy R, Seon BK, Duff SE, Abdalla S, Renehan A, O'Dwyer ST, Haboubi N, Kumar S (2003) Both high intratumoral microvessel density determined using CD105 antibody and elevated plasma levels of CD105 in colorectal cancer patients correlate with poor prognosis. Br J Cancer 88: 1424-1431
27. Lindmark G, Gerdin B, Pahlman L, Bergstrom R, Glimelius B (1994) Prognostic predictors in colorectal cancer. Dis Colon Rectum 37: 1219-1227
28. Lu XG, Xing CG, Feng YZ, Chen J, Deng C (2006) Clinical significance of immunohistochemical expression of hypoxia-inducible factor-1alpha as a prognostic marker in rectal adenocarcinoma. Clin Colorectal Cancer 5: 350-353
29. Mackay H, Hedley D, Major P, Townsley C, Mackenzie M, Vincent M, Degendorfer P, Tsao MS, Nicklee T, Birle D, Wright J, Siu L, Moore M, Oza A (2005) A phase II trial with pharmacodynamic endpoints of the proteasome inhibitor bortezomib in patients with metastatic colorectal cancer. Clin Cancer Res 11: 5526-5533
30. Maynard MA, Ohh M (2007) The role of hypoxia-inducible factors in cancer. Cell Mol Life Sci 64: 2170-2180
31. Palit V, Phillips RM, Puri R, Shah T, Bibby MC (2005) Expression of HIF-1alpha and Glut-1 in human bladder cancer. Oncol Rep 14: 909-913
32. Pugh CW, Ratcliffe PJ (2003) Regulation of angiogenesis by hypoxia: role of the HIF system. Nat Med 9: 677-684
33. Rasheed S, Harris AL, Tekkis PP, Turley H, Silver A, McDonald PJ, Talbot IC, Glynne-Jones R, Northover JM, Guenther T (2009) Assessment of microvessel density and carbonic anhydrase-9 (CA-9) expression in rectal cancer. Pathol Res Pract 205(1): 1-9
34. Rasheed S, McDonald PJ, Northover JM, Guenther T (2008) Angiogenesis and hypoxic factors in colorectal cancer. Pathol Res Pract 204: 501-510
35. Ratcliffe PJ, Ebert BL, Firth JD, Gleadle JM, Maxwell PH, Nagao M, O'Rourke JF, Pugh CW, Wood SM (1997) Oxygen regulated gene expression: erythropoietin as a model system. Kidney Int 51: 514-526
36. Sagar P, Pemberton J (1996) Surgical management of locally recurrent rectal cancer. Br J Surg 83: 293-304
37. Semenza GL (2001) Hypoxia-inducible factor 1: control of oxygen homeostasis in health and disease. Pediatr Res 49: 614-617
38. Shibaji T, Nagao M, Ikeda N, Kanehiro H, Hisanaga M, Ko S, Fukumoto A, Nakajima Y (2003) Prognostic significance of HIF-1 alpha overexpres-sion in human pancreatic cancer. Anticancer Res 23: 4721-4727
39. Singh RP, Gu M, Agarwal R (2008) Silibinin inhibits colorectal cancer growth by inhibiting tumor cell proliferation and angiogenesis. Cancer Res 68: 2043-2050
40. Talks KL, Turley H, Gatter KC, Maxwell PH, Pugh CW, Ratcliffe PJ, Harris AL (2000) The expression and distribution of the hypoxia-inducible factors HIF-1alpha and HIF-2alpha in normal human tissues, cancers, and tumor-associated macrophages. Am J Pathol 157: 411-421
41. Theodoropoulos GE, Lazaris AC, Theodoropoulos VE, Papatheodosiou K, Gazouli M, Bramis J, Patsouris E, Panoussopoulos D (2006) Hypoxia, angiogenesis and apoptosis markers in locally advanced rectal cancer. Int J Colorectal Dis 21: 248-257
42. Theodoropoulos VE, Lazaris AC, Kastriotis I, Spiliadi C, Theodoropoulos GE, Tsoukala V, Patsouris E, Sofras F (2005) Evaluation of hypoxia-inducible factor 1alpha overexpression as a predictor of tumour recurrence and progression in superficial urothelial bladder carcinoma. BJU Int 95: 425-431
43. Tomisaki S, Ohno S, Ichiyoshi Y, Kuwano H, Maehara Y, Sugimachi K (1996) Microvessel quantification and its possible relation with liver metastasis in colorectal cancer. Cancer 77: 1722-1728
44. Trastour C, Benizri E, Ettore F, Ramaioli A, Chamorey E, Pouyssegur J, Berra E (2007) HIF-1alpha and CA IX staining in invasive breast carcinomas: prognosis and treatment outcome. Int J Cancer 120: 1451-1458
45. Vermeulen PB, Van den Eynden GG, Huget P, Goovaerts G, Weyler J, Lardon F, Van Marck E, Hubens G, Dirix LY (1999) Prospective study of intratumoral microvessel density, p53 expression and survival in colorectal cancer. Br J Cancer 79: 316-322
46. Willett CG, Boucher Y, di Tomaso E, Duda DG, Munn LL, Tong RT, Chung DC, Sahani DV, Kalva SP, Kozin SV, Mino M, Cohen KS, Scadden DT, Hartford AC, Fischman AJ, Clark JW, Ryan DP, Zhu AX, Blaszkowsky LS, Chen HX, Shellito PC, Lauwers GY, Jain RK (2004) Direct evidence that the VEGF-specific antibody bevacizumab has antivascular effects in human rectal cancer. Nat Med 10: 145-147
47. Willett CG, Kozin SV, Duda DG, di Tomaso E, Kozak KR, Boucher Y, Jain RK (2006) Combined vascular endothelial growth factor-targeted therapy and radiotherapy for rectal cancer: theory and clinical practice. Semin Oncol 33: S35-S40
48. Wykoff CC, Pugh CW, Harris AL, Maxwell PH, Ratcliffe PJ (2001) The HIF pathway: implications for patterns of gene expression in cancer. Novartis Found Symp 240: 212-225; discussion 225-231)
49. Yoshimura H, Dhar DK, Kohno H, Kubota H, Fujii T, Ueda S, Kinugasa S, Tachibana M, Nagasue N (2004) Prognostic impact of hypoxia-inducible factors 1alpha and 2alpha in colorectal cancer patients: correlation with tumor angiogenesis and cyclooxygenase-2 expression. Clin Cancer Res 10: 8554-8560
50. Zhu B, Lu L, Cai W, Yang X, Li C, Yang Z, Zhan W, Ma JX, Gao G (2007) Kallikrein-binding protein inhibits growth of gastric carcinoma by reducing vascular endothelial growth factor production and angio-genesis. Mol Cancer Ther 6: 3297-3306