Increased tumor ascorbate is associated with extended disease-free survival and decreased hypoxia-inducible factor-1 activation in human colorectal cancer

Frontiers in Oncology

Volumn 4 FEB, Issue , 2014, Pages

  Kuiper, Caroline ^a   Dachs, Gabi U ^a   Munn, Delwyn ^a   Currie, Margaret J ^a   Robinson, Bridget A ^a,b   Pearson, John F ^a   Vissers, Margreet C M ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b CHRISTCHURCH HOSPITAL   (New Zealand)

Author keywords

Ascorbate; BNIP3; Colorectal cancer; Hydroxylation; Hypoxia inducible factor; VEGF

Indexed keywords

ASCORBIC ACID; CAPECITABINE; FLUOROURACIL; FOLINIC ACID; GLUCOSE TRANSPORTER 1; HYPOXIA INDUCIBLE FACTOR 1; OXALIPLATIN; PROTEIN BNIP3; VASCULOTROPIN;

ARTICLE; CANCER STAGING; CANCER SURVIVAL; CLINICAL ARTICLE; COLORECTAL CANCER; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE FREE SURVIVAL; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; FOLLOW UP; HUMAN; HUMAN TISSUE; MALE; OBSERVATIONAL STUDY; RETROSPECTIVE STUDY; SCORING SYSTEM; TUMOR VOLUME; WESTERN BLOTTING;

EID: 84896737068     PISSN: None     EISSN: 2234943X     Source Type: Journal    
DOI: 10.3389/fonc.2014.00010     Document Type: Article

References (50)

1. Maxwell PH, Dachs GU, Gleadle JM, Nicholls LG, Harris AL, Stratford IJ, et al. Hypoxia-inducible factor-1 modulates gene expression in solid tumors and influences both angiogenesis and tumor growth. Proc Natl Acad Sci U S A (1997) 94(15):8104-9. doi: 10.1073/pnas.94.15.8104
2. Semenza GL. Targeting HIF-1 for cancer therapy. Nat Rev Cancer (2003) 3(10):721-32. doi:10.1038/nrc1187
3. Baba Y, Nosho K, Shima K, Irahara N, Chan AT, Meyerhardt JA, et al. HIF1A overexpression is associated with poor prognosis in a cohort of 731 colorectal cancers. Am J Pathol (2010) 176(5):2292-301. doi:10.2353/ajpath.2010.090972
4. Liu L, Ning X, Sun L, Zhang H, Shi Y, Guo C, et al. Hypoxia-inducible factor-1 alpha contributes to hypoxia-induced chemoresistance in gastric cancer. Cancer Sci (2008) 99(1):121-8.
5. Vaupel P, Mayer A. Hypoxia in cancer: significance and impact on clinical outcome. Cancer Metastasis Rev (2007) 26(2):225-39. doi:10.1007/s10555-007-9055-1
6. Yamamoto Y, Ibusuki M, Okumura Y, Kawasoe T, Kai K, Iyama K, et al. Hypoxia-inducible factor 1 alpha is closely linked to an aggressive phenotype in breast cancer. Breast Cancer Res Treat (2008) 110(3):465-75. doi:10.1007/s10549-007-9742-1
7. Rohwer N, Cramer T. Hypoxia-mediated drug resistance: novel insights on the functional interaction of HIFs and cell death pathways. Drug Resist Updat (2011) 14:191-201. doi:10.1016/j.drup.2011.03.001
8. Wong CC, Gilkes DM, Zhang H, Chen J, Wei H, Chaturvedi P, et al. Hypoxia-inducible factor 1 is a master regulator of breast cancer metastatic niche formation. Proc Natl Acad Sci U S A (2011) 108(39):16369-74. doi:10.1073/pnas.1113483108
9. Zhang H, Wong CC, Wei H, Gilkes DM, Korangath P, Chaturvedi P, et al. HIF-1-dependent expression of angiopoietin-like 4 and L1CAM mediates vascular metastasis of hypoxic breast cancer cells to the lungs. Oncogene (2012) 31(14):1757-70. doi:10.1038/onc.2011.365
10. Hu Y, Liu J, Huang H. Recent agents targeting HIF-1alpha for cancer therapy. J Cell Biochem (2013) 114(3):498-509. doi:10.1002/jcb.24390
11. Ward C, Langdon SP, Mullen P, Harris AL, Harrison DJ, Supuran CT, et al. New strategies for targeting the hypoxic tumor microenvironment in breast cancer. Cancer Treat Rev (2013) 39(2):171-9. doi:10.1016/j.ctrv.2012.08.004
12. Ozer A, Bruick RK. Non-heme dioxygenases: cellular sensors and regulators jelly rolled into one? Nat Chem Biol (2007) 3(3):144-53. doi:10.1038/nchembio863
13. Loenarz C, Schofield CJ. Physiological and biochemical aspects of hydroxylations and demethylations catalyzed by human 2-oxoglutarate oxygenases. Trends Biochem Sci (2011) 36(1):7-18. doi:10.1016/j.tibs.2010.07.002
14. Myllyla R, Kuutti-Savolainen ER, Kivirikko KI. The role of ascorbate in the prolyl hydroxylase reaction. Biochem Biophys Res Commun (1978) 83(2):441-8. doi:10.1016/0006-291X(78)91010-0
15. Clifton IJ, McDonough MA, Ehrismann D, Kershaw NJ, Granatino N, Schofield CJ. Structural studies on 2-oxoglutarate oxygenases and related double-stranded beta-helix fold proteins. J Inorg Biochem (2006) 100(4):644-69. doi:10.1016/j.jinorgbio.2006.01.024
16. Knowles HJ, Raval RR, Harris AL, Ratcliffe PJ. Effect of ascorbate on the activity of hypoxia-inducible factor in cancer cells. Cancer Res (2003) 63(8):1764-8.
17. Vissers MC, Gunningham SP, Morrison MJ, Dachs GU, Currie MJ. Modulation of hypoxia-inducible factor-1 alpha in cultured primary cells by intracellular ascorbate. Free Radic Biol Med (2007) 42(6):765-72. doi:10.1016/j.freeradbiomed.2006.11.023
18. Vissers MC, Wilkie RP. Ascorbate deficiency results in impaired neutrophil apoptosis and clearance and is associated with up-regulation of hypoxia-inducible factor 1 alpha. J Leukoc Biol (2007) 81(5):1236-44. doi:10.1189/jlb.0806541
19. Du J, Cullen JJ, Buettner GR. Ascorbic acid: chemistry, biology and the treatment of cancer. Biochim Biophys Acta (2012) 1826(2):443-57. doi:10.1016/j.bbcan.2012.06.003
20. Hornig D. Distribution of ascorbic acid, metabolites and analogues in man and animals. Ann N Y Acad Sci (1975) 258:103-18. doi:10.1111/j.1749-6632.1975.tb29271.x
21. Levine M, Conry-Cantilena C, Wang Y, Welch RW, Washko PW, Dhariwal KR, et al. Vitamin C pharmacokinetics in healthy volunteers: evidence for a recommended dietary allowance. Proc Natl Acad Sci U S A (1996) 93(8):3704-9. doi:10.1073/pnas.93.8.3704
22. Anthony HM, Schorah CJ. Severe hypovitaminosis C in lung-cancer patients: the utilization of vitamin C in surgical repair and lymphocyte-related host resistance. Br J Cancer (1982) 46(3):354-67. doi:10.1038/bjc.1982.211
23. Mayland CR, Bennett MI, Allan K. Vitamin C deficiency in cancer patients. Palliat Med (2005) 19(1):17-20. doi:10.1191/0269216305pm970oa
24. Chen H, Costa M. Iron- and 2-oxoglutarate-dependent dioxygenases: an emerging group of molecular targets for nickel toxicity and carcinogenicity. Biometals (2009) 22:191-6. doi:10.1007/s10534-008-9190-3
25. Gao P, Zhang H, Dinavahi R, Li F, Xiang Y, Raman V, et al. HIF-dependent antitumorigenic effect of antioxidants in vivo. Cancer Cell (2007) 12(3):230-8. doi:10.1016/j.ccr.2007.08.004
26. Kuiper C, Molenaar IG, Dachs GU, Currie MJ, Sykes PH, Vissers MC. Low ascorbate levels are associated with increased hypoxia-inducible factor-1 activity and an aggressive tumor phenotype in endometrial cancer. Cancer Res (2010) 70(14):5749-58. doi:10.1158/0008-5472.CAN-10-0263
27. Hawk ET, Limburg PJ, Viner JL. Epidemiology and prevention of colorectal cancer. Surg Clin North Am (2002) 82(5):905-41. doi:10.1016/S0039-6109(02)00046-4
28. Cao D, Hou M, Guan YS, Jiang M, Yang Y, Gou HF. Expression of HIF-1alpha and VEGF in colorectal cancer: association with clinical outcomes and prognostic implications. BMC Cancer (2009) 9:432. doi:10.1186/1471-2407-9-432
29. Kwon HC, Kim SH, Oh SY, Lee S, Kwon KA, Choi HJ, et al. Clinicopathological significance of p53, hypoxia-inducible factor 1 alpha, and vascular endothelial growth factor expression in colorectal cancer. Anticancer Res (2010) 30(10):4163-8.
30. Liang WJ, Johnson D, Jarvis SM. Vitamin C transport systems of mammalian cells. Mol Membr Biol (2001) 18(1):87-95. doi:10.1080/09687680110033774
31. Harris HR, Bergkvist L, Wolk A. Vitamin C intake and breast cancer mortality in a cohort of Swedish women. Br J Cancer (2013) 109(1):257-64. doi:10.1038/bjc.2013.269
32. Chen C, Sun J, Liu G, Chen J. Effect of small interference RNA targeting HIF-1alpha mediated by rAAV combined L: ascorbate on pancreatic tumors in athymic mice. Pathol Oncol Res (2009) 15(1):109-14. doi:10.1007/s12253-008-9063-7
33. Welsh JL, Wagner BA, van't Erve TJ, Zehr PS, Berg DJ, Halfdanarson TR, et al. Pharmacological ascorbate with gemcitabine for the control of metastatic and node-positive pancreatic cancer (PACMAN): results from a phase I clinical trial. Cancer Chemother Pharmacol (2013) 71(3):765-75. doi:10.1007/s00280-013-2070-8
34. Lu H, Dalgard CL, Mohyeldin A, McFate T, Tait AS, Verma A. Reversible inactivation of HIF-1 prolyl hydroxylases allows cell metabolism to control basal HIF-1. J Biol Chem (2005) 280(51):41928-39. doi:10.1074/jbc.M508718200
35. Qiao H, Li L, Qu ZC, May JM. Cobalt-induced oxidant stress in cultured endothelial cells: prevention by ascorbate in relation to HIF-1alpha. Biofactors (2009) 35(3):306-13. doi:10.1002/biof.43
36. Cha J, Roomi MW, Ivanov V, Kalinovsky T, Niedzwiecki A, Rath M. Ascorbate depletion increases growth and metastasis of melanoma cells in vitamin C deficient mice. Exp Oncol (2011) 33(4):226-30.
37. Cha J, Roomi MW, Ivanov V, Kalinovsky T, Niedzwiecki A, Rath M. Ascorbate supplementation inhibits growth and metastasis of B16FO melanoma and 4T1 breast cancer cells in vitamin C-deficient mice. Int J Oncol (2013) 42(1):55-64. doi:10.3892/ijo.2012.1712
38. Padayatty SJ, Sun AY, Chen Q, Espey MG, Drisko J, Levine M. Vitamin C: intravenous use by complementary and alternative medicine practitioners and adverse effects. PLoS One (2010) 5(7):e11414. doi:10.1371/journal.pone.0011414
39. Padayatty SJ, Sun H, Wang Y, Riordan HD, Hewitt SM, Katz A, et al. Vitamin C pharmacokinetics: implications for oral and intravenous use. Ann Intern Med (2004) 140(7):533-7. doi:10.7326/0003-4819-140-7-200404060-00010
40. Moertel CG, Fleming TR, Creagan ET, Rubin J, O'Connell MJ, Ames MM. High-dose vitamin C versus placebo in the treatment of patients with advanced cancer who have had no prior chemotherapy. A randomized double-blind comparison. N Engl J Med (1985) 312(3):137-41. doi:10.1056/NEJM198501173120301
41. Cameron E, Pauling L. Experimental studies designed to evaluate the management of patients with incurable cancer. Proc Natl Acad Sci U S A (1978) 75(12):6252. doi:10.1073/pnas.75.12.6252
42. Cameron E, Pauling L. Supplemental ascorbate in the supportive treatment of cancer: reevaluation of prolongation of survival times in terminal human cancer. Proc Natl Acad Sci U S A (1978) 75(9):4538-42. doi:10.1073/pnas.75.9.4538
43. Chen Q, Espey MG, Sun AY, Lee JH, Krishna MC, Shacter E, et al. Ascorbate in pharmacologic concentrations selectively generates ascorbate radical and hydrogen peroxide in extracellular fluid in vivo. Proc Natl Acad Sci U S A (2007) 104(21):8749-54. doi:10.1073/pnas.0702854104
44. Chen Q, Espey MG, Sun AY, Pooput C, Kirk KL, Krishna MC, et al. Pharmacologic doses of ascorbate act as a prooxidant and decrease growth of aggressive tumor xenografts in mice. Proc Natl Acad Sci U S A (2008) 105(32):11105-9. doi:10.1073/pnas.0804226105
45. (2)-mediated cytotoxicity of pharmacologic ascorbate concentrations to neuroblastoma cells: potential role of lactate and ferritin. Cell Physiol Biochem (2010) 25(6):767-74. doi:10.1159/000315098
46. Verrax J, Calderon PB. Pharmacologic concentrations of ascorbate are achieved by parenteral administration and exhibit antitumoral effects. Free Radic Biol Med (2009) 47(1):32-40. doi:10.1016/j.freeradbiomed.2009.02.016
47. May JM. The SLC23 family of ascorbate transporters: ensuring that you get and keep your daily dose of vitamin C. Br J Pharmacol (2011) 164(7):1793-801. doi:10.1111/j.1476-5381.2011.01350.x
48. Dewhirst MW, Tso CY, Oliver R, Gustafson CS, Secomb TW, Gross JF. Morphologic and hemodynamic comparison of tumor and healing normal tissue microvasculature. Int J Radiat Oncol Biol Phys (1989) 17(1):91-9. doi:10.1016/0360-3016(89)90375-1
49. Wu Y, Jin M, Xu H, Shimin Z, He S, Wang L, et al. Clinicopathologic significance of HIF-1alpha, CXCR4, and VEGF expression in colon cancer. Clin Dev Immunol (2010) 2010:10. doi:10.1155/2010/537531
50. Kuwai T, Kitadai Y, Tanaka S, Onogawa S, Matsutani N, Kaio E, et al. Expression of hypoxia-inducible factor-1 alpha is associated with tumor vascularization in human colorectal carcinoma. Int J Cancer (2003) 105(2):176-81. doi:10.1002/ijc.11068