Ascorbate exerts anti-proliferative effects through cell cycle inhibition and sensitizes tumor cells towards cytostatic drugs

Cancer Chemotherapy and Pharmacology

Volumn 67, Issue 5, 2011, Pages 1157-1166

  Frömberg, Anja ^a   Gutsch, Daniela ^a   Schulze, Daniel ^a   Vollbracht, Claudia ^b   Weiss, Gabriele ^b   Czubayko, Frank ^a   Aigner, Achim ^a  

^a PHILIPPS UNIVERSITY MARBURG   (Germany)

^b Pascoe Pharmazeutische Praeparate GmbH Giessen   (Germany)

Author keywords

5 FU; Ascorbate; Dehydroascorbate; Paclitaxel; Prostate carcinoma

Indexed keywords

ASCORBIC ACID; CASPASE 3; DEHYDROASCORBIC ACID; DOCETAXEL; EPIRUBICIN; FLUOROURACIL; HYDROGEN PEROXIDE; IRINOTECAN; NAVELBINE; OXALIPLATIN; PASCORBIN; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CANCER CELL CULTURE; CELL CYCLE ARREST; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL PROLIFERATION; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; DRUG EFFICACY; DRUG MECHANISM; DRUG POTENTIATION; DRUG SENSITIVITY; HUMAN; HUMAN CELL; IC 50; PRIORITY JOURNAL;

ANTINEOPLASTIC AGENTS; APOPTOSIS; ASCORBIC ACID; CAMPTOTHECIN; CELL CYCLE; CELL LINE, TUMOR; CELL PROLIFERATION; CELL SURVIVAL; DEHYDROASCORBIC ACID; DRUG SYNERGISM; EPIRUBICIN; HUMANS; MALE; ORGANOPLATINUM COMPOUNDS; PROSTATIC NEOPLASMS; TAXOIDS; VINBLASTINE;

EID: 79955550511     PISSN: 03445704     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00280-010-1418-6     Document Type: Article

References (40)

1. MM Abdel-Latif AA Raouf K Sabra D Kelleher JV Reynolds 2005 Vitamin C enhances chemosensitization of esophageal cancer cells in vitro J Chemother 17 539 549 16323444 1:CAS:528:DC%2BD2MXhtlWgtr3P (Pubitemid 41695602)
2. S Abuharbeid J Apel M Sander B Fiedler M Langer ML Zuzarte F Czubayko A Aigner 2004 Cytotoxicity of the novel anti-cancer drug rViscumin depends on HER-2 levels in SKOV-3 cells Biochem Biophys Res Commun 321 403 412 15358191 10.1016/j.bbrc.2004.06.160 1:CAS:528:DC%2BD2cXmtVajsLg%3D
3. DB Agus JC Vera DW Golde 1999 Stromal cell oxidation: a mechanism by which tumors obtain vitamin C Cancer Res 59 4555 4558 10493506 1:CAS:528:DyaK1MXmtVKksb0%3D (Pubitemid 29428957)
4. S Belin F Kaya G Duisit S Giacometti J Ciccolini M Fontes 2009 Antiproliferative effect of ascorbic acid is associated with the inhibition of genes necessary to cell cycle progression PLoS One 4 e4409 19197388 10.1371/journal.pone.0004409
5. AM Bode HQ Liang EH Green TE Meyer DJ Buckley A Norris PW Gout AR Buckley 1999 Ascorbic acid recycling in Nb2 lymphoma cells: implications for tumor progression Free Radic Biol Med 26 136 147 9890649 10.1016/S0891-5849(98)00183-X 1:CAS:528:DyaK1MXhsFym (Pubitemid 29001501)
6. E Cameron L Pauling 1978 Supplemental ascorbate in the supportive treatment of cancer: reevaluation of prolongation of survival times in terminal human cancer Proc Natl Acad Sci USA 75 4538 4542 279931 10.1073/pnas.75.9.4538 1:STN:280:DyaE1M%2Fjtlyktw%3D%3D (Pubitemid 9028392)
7. R Carosio G Zuccari I Orienti S Mangraviti PG Montaldo 2007 Sodium ascorbate induces apoptosis in neuroblastoma cell lines by interfering with iron uptake Mol Cancer 6 55 17760959 10.1186/1476-4598-6-55 (Pubitemid 47534712)
8. JJ Casciari HD Riordan JR Miranda-Massari MJ Gonzalez 2005 Effects of high dose ascorbate administration on L-10 tumor growth in guinea pigs P R Health Sci J 24 145 150 16116933
9. Q Chen MG Espey MC Krishna JB Mitchell CP Corpe GR Buettner E Shacter M Levine 2005 Pharmacologic ascorbic acid concentrations selectively kill cancer cells: action as a pro-drug to deliver hydrogen peroxide to tissues Proc Natl Acad Sci USA 102 13604 13609 16157892 10.1073/pnas.0506390102 1:CAS:528:DC%2BD2MXhtVygtr%2FP (Pubitemid 41420895)
10. Q Chen MG Espey AY Sun JH Lee MC Krishna E Shacter PL Choyke C Pooput KL Kirk GR Buettner M Levine 2007 Ascorbate in pharmacologic concentrations selectively generates ascorbate radical and hydrogen peroxide in extracellular fluid in vivo Proc Natl Acad Sci USA 104 8749 8754 17502596 10.1073/pnas. 0702854104 1:CAS:528:DC%2BD2sXmt1aktbo%3D (Pubitemid 47175383)
11. Q Chen MG Espey AY Sun C Pooput KL Kirk MC Krishna DB Khosh J Drisko M Levine 2008 Pharmacologic doses of ascorbate act as a prooxidant and decrease growth of aggressive tumor xenografts in mice Proc Natl Acad Sci USA 105 11105 11109 18678913 10.1073/pnas.0804226105 1:CAS:528:DC%2BD1cXhtVSnsLzF
12. ET Creagan CG Moertel JR O'Fallon AJ Schutt MJ O'Connell J Rubin S Frytak 1979 Failure of high-dose vitamin C (ascorbic acid) therapy to benefit patients with advanced cancer. A controlled trial N Engl J Med 301 687 690 384241 10.1056/NEJM197909273011303 1:STN:280:DyaL3c%2FhtFClsA%3D%3D (Pubitemid 10240445)
13. J Dai RS Weinberg S Waxman Y Jing 1999 Malignant cells can be sensitized to undergo growth inhibition and apoptosis by arsenic trioxide through modulation of the glutathione redox system Blood 93 268 277 9864170 1:CAS:528:DyaK1MXhvFSrtQ%3D%3D (Pubitemid 29019412)
14. Du J, Martin SM, Levine M, Wagner BA, Buettner GR, Wang SH, Taghiyev AF, Du C, Knudson CM, Cullen JJ Mechanisms of ascorbate-induced cytotoxicity in pancreatic cancer. Clin Cancer Res 16:509-520
15. MG Espey Q Chen M Levine 2009 Comment re: vitamin C antagonizes the cytotoxic effects of chemotherapy Cancer Res 69 8830 19843868 10.1158/0008-5472.CAN-08-3798 1:CAS:528:DC%2BD1MXhtl2rtr%2FI (author reply 8830-1)
16. P Gao H Zhang R Dinavahi F Li Y Xiang V Raman ZM Bhujwalla DW Felsher L Cheng J Pevsner LA Lee GL Semenza CV Dang 2007 HIF-dependent antitumorigenic effect of antioxidants in vivo Cancer Cell 12 230 238 17785204 10.1016/j.ccr.2007.08.004 1:CAS:528:DC%2BD2sXhtVKqsb3E (Pubitemid 47333417)
17. S Goutelle M Maurin F Rougier X Barbaut L Bourguignon M Ducher P Maire 2008 The Hill equation: a review of its capabilities in pharmacological modelling Fundam Clin Pharmacol 22 633 648 19049668 10.1111/j.1472-8206.2008. 00633.x 1:CAS:528:DC%2BD1MXhvV2msQ%3D%3D
18. JM Grad E Cepero LH Boise 2001 Mitochondria as targets for established and novel anti-cancer agents Drug Resist Updat 4 85 91 11512525 10.1054/drup.2001.0192 1:CAS:528:DC%2BD3MXlt12gu78%3D (Pubitemid 32619566)
19. E Hahm DH Jin JS Kang YI Kim SW Hong SK Lee HN Kim J da Jung JE Kim DH Shin YI Hwang YS Kim DY Hur Y Yang D Cho MS Lee WJ Lee 2007 The molecular mechanisms of vitamin C on cell cycle regulation in B16F10 murine melanoma J Cell Biochem 102 1002 1010 17455238 10.1002/jcb.21336 1:CAS:528: DC%2BD2sXhtlSisLrP (Pubitemid 350036939)
20. ML Heaney JR Gardner N Karasavvas DW Golde DA Scheinberg EA Smith OA O'Connor 2008 Vitamin C antagonizes the cytotoxic effects of antineoplastic drugs Cancer Res 68 8031 8038 18829561 10.1158/0008-5472.CAN-08-1490 1:CAS:528:DC%2BD1cXhtF2msLrL
21. LJ Hoffer M Levine S Assouline D Melnychuk SJ Padayatty K Rosadiuk C Rousseau L Robitaille WH Miller Jr 2008 Phase I clinical trial of i.v. ascorbic acid in advanced malignancy Ann Oncol 19 1969 1974 18544557 10.1093/annonc/ mdn377 1:STN:280:DC%2BD1cnosVClsA%3D%3D
22. SW Hong DH Jin ES Hahm SH Yim JS Lim KI Kim Y Yang SS Lee JS Kang WJ Lee WK Lee MS Lee 2007 Ascorbate (vitamin C) induces cell death through the apoptosis-inducing factor in human breast cancer cells Oncol Rep 18 811 815 17786340 1:CAS:528:DC%2BD2sXhtFygu7jO
23. CM Kurbacher U Wagner B Kolster PE Andreotti D Krebs HW Bruckner 1996 Ascorbic acid (vitamin C) improves the antineoplastic activity of doxorubicin, cisplatin, and paclitaxel in human breast carcinoma cells in vitro Cancer Lett 103 183 189 8635156 10.1016/0304-3835(96)04212-7 1:CAS:528:DyaK28Xisl2ltb8%3D (Pubitemid 26147697)
24. BD Lawenda KM Kelly EJ Ladas SM Sagar A Vickers JB Blumberg 2008 Should supplemental antioxidant administration be avoided during chemotherapy and radiation therapy? J Natl Cancer Inst 100 773 783 18505970 10.1093/jnci/djn148 1:CAS:528:DC%2BD1cXmvFWksr4%3D (Pubitemid 351809666)
25. SK Lee JS Kang J da Jung DY Hur JE Kim E Hahm S Bae HW Kim D Kim BJ Cho D Cho DH Shin YI Hwang WJ Lee 2008 Vitamin C suppresses proliferation of the human melanoma cell SK-MEL-2 through the inhibition of cyclooxygenase-2 (COX-2) expression and the modulation of insulin-like growth factor II (IGF-II) production J Cell Physiol 216 180 188 18297687 10.1002/jcp.21391 1:CAS:528:DC%2BD1cXnt1ektrs%3D (Pubitemid 351813109)
26. M Levine MG Espey Q Chen 2009 Losing and finding a way at C: new promise for pharmacologic ascorbate in cancer treatment Free Radic Biol Med 47 27 29 19361554 10.1016/j.freeradbiomed.2009.04.001 1:CAS:528:DC%2BD1MXms1yhsLY%3D
27. QQ Li ZQ Chen JD Xu XX Cao Q Chen XP Liu ZD Xu 2010 Overexpression and involvement of special AT-rich sequence binding protein 1 in multidrug resistance in human breast carcinoma cells Cancer Sci 101 80 86 19860849 10.1111/j.1349-7006.2009.01372.x 1:CAS:528:DC%2BC3cXnvVKqsQ%3D%3D
28. SY Lin WW Lai CC Chou HM Kuo TM Li JG Chung JH Yang 2006 Sodium ascorbate inhibits growth via the induction of cell cycle arrest and apoptosis in human malignant melanoma A375.S2 cells Melanoma Res 16 509 519 17119452 10.1097/01.cmr.0000232297.99160.9e (Pubitemid 44934709)
29. W Malorni U Testa G Rainaldi E Tritarelli C Peschle 1998 Oxidative stress leads to a rapid alteration of transferrin receptor intravesicular trafficking Exp Cell Res 241 102 116 9633518 10.1006/excr.1998.4020 1:CAS:528: DyaK1cXjvVGjtLg%3D (Pubitemid 28366584)
30. CG Moertel TR Fleming ET Creagan J Rubin MJ O'Connell MM Ames 1985 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 312 137 141 3880867 10.1056/NEJM198501173120301 1:STN:280:DyaL2M%2Fos1WgtQ%3D%3D (Pubitemid 15192859)
31. B Nagy I Mucsi J Molnar A Varga L Thurzo 2003 Chemosensitizing effect of vitamin C in combination with 5-fluorouracil in vitro In Vivo 17 289 292 12929582 1:CAS:528:DC%2BD3sXmvFSrs7Y%3D (Pubitemid 36958121)
32. FJ Nualart CI Rivas VP Montecinos AS Godoy VH Guaiquil DW Golde JC Vera 2003 Recycling of vitamin C by a bystander effect J Biol Chem 278 10128 10133 12435736 10.1074/jbc.M210686200 1:CAS:528:DC%2BD3sXitVCkt7c%3D (Pubitemid 36800270)
33. S Ohtani A Iwamaru W Deng K Ueda G Wu G Jayachandran S Kondo EN Atkinson JD Minna JA Roth L Ji 2007 Tumor suppressor 101F6 and ascorbate synergistically and selectively inhibit non-small cell lung cancer growth by caspase-independent apoptosis and autophagy Cancer Res 67 6293 6303 17616688 10.1158/0008-5472.CAN- 06-3884 1:CAS:528:DC%2BD2sXnsVyqt7Y%3D (Pubitemid 47037512)
34. SJ Padayatty H Sun Y Wang HD Riordan SM Hewitt A Katz RA Wesley M Levine 2004 Vitamin C pharmacokinetics: implications for oral and intravenous use Ann Intern Med 140 533 537 15068981 1:CAS:528:DC%2BD2cXjsFSqsrw%3D
35. CH Park 1985 Biological nature of the effect of ascorbic acids on the growth of human leukemic cells Cancer Res 45 3969 3973 4016763 1:CAS:528:DyaL2MXltVersL4%3D (Pubitemid 15226483)
36. CH Park BF Kimler 1991 Growth modulation of human leukemic, preleukemic, and myeloma progenitor cells by l-ascorbic acid Am J Clin Nutr 54 1241S 1246S 1962577 1:CAS:528:DyaK38XhsFahsA%3D%3D
37. X Qian J Li J Ding Z Wang W Zhang G Hu 2009 Erlotinib activates mitochondrial death pathways related to the production of reactive oxygen species in the human non-small cell lung cancer cell line A549 Clin Exp Pharmacol Physiol 36 487 494 19673930 10.1111/j.1440-1681.2008.05091.x 1:CAS:528:DC%2BD1MXlvVCksLs%3D
38. K Takara T Sakaeda T Yagami H Kobayashi N Ohmoto M Horinouchi K Nishiguchi K Okumura 2002 Cytotoxic effects of 27 anticancer drugs in HeLa and MDR1-overexpressing derivative cell lines Biol Pharm Bull 25 771 778 12081145 10.1248/bpb.25.771 1:CAS:528:DC%2BD38XkvV2gsrY%3D (Pubitemid 40036714)
39. JC Vera CI Rivas J Fischbarg DW Golde 1993 Mammalian facilitative hexose transporters mediate the transport of dehydroascorbic acid Nature 364 79 82 8316303 10.1038/364079a0 1:CAS:528:DyaK3sXks1yku7k%3D (Pubitemid 23233461)
40. JC Vera CI Rivas RH Zhang CM Farber DW Golde 1994 Human HL-60 myeloid leukemia cells transport dehydroascorbic acid via the glucose transporters and accumulate reduced ascorbic acid Blood 84 1628 1634 8068952 1:CAS:528: DyaK2cXlslKnsLo%3D (Pubitemid 24273034)