Importance of intracellular pH in determining the uptake and efficacy of the weakly basic chemotherapeutic drug, doxorubicin

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Swietach, Pawel ^a   Hulikova, Alzbeta ^a   Patiar, Shalini ^b   Vaughan Jones, Richard D ^a   Harris, Adrian L ^b  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b JOHN RADCLIFFE HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DOXORUBICIN; ANTINEOPLASTIC ANTIBIOTIC;

ARTICLE; BINDING SITE; CARCINOMA CELL; CELL MEMBRANE; CELL PH; CELL PROLIFERATION; COLON CARCINOMA; CONTROLLED STUDY; CYTOPLASM; DRUG EFFICACY; DRUG SENSITIVITY; DRUG UPTAKE; HUMAN; HUMAN CELL; MATHEMATICAL MODEL; MEMBRANE POTENTIAL; STEADY STATE; CELL NUCLEUS; CELL STRAIN HCT116; CHEMICAL MODEL; DRUG EFFECT; METABOLISM; PH;

ANTIBIOTICS, ANTINEOPLASTIC; BINDING SITES; CELL NUCLEUS; CELL PROLIFERATION; DOXORUBICIN; HCT116 CELLS; HUMANS; HYDROGEN-ION CONCENTRATION; MODELS, CHEMICAL;

EID: 84860372850     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0035949     Document Type: Article

References (34)

1. Raghunand N, He X, van Sluis R, Mahoney B, Baggett B, et al. (1999) Enhancement of chemotherapy by manipulation of tumour pH. Br J Cancer 80: 1005-1011.
2. Gerweck LE, Kozin SV, Stocks SJ, (1999) The pH partition theory predicts the accumulation and toxicity of doxorubicin in normal and low-pH-adapted cells. Br J Cancer 79: 838-842.
3. Gerweck LE, Seetharaman K, (1996) Cellular pH gradient in tumor versus normal tissue: potential exploitation for the treatment of cancer. Cancer Res 56: 1194-1198.
4. Stubbs M, McSheehy PM, Griffiths JR, Bashford CL, (2000) Causes and consequences of tumour acidity and implications for treatment. Mol Med Today 6: 15-19.
5. Vaupel P, Kallinowski F, Okunieff P, (1989) Blood flow, oxygen and nutrient supply, and metabolic microenvironment of human tumors: a review. Cancer Res 49: 6449-6465.
6. Raghunand N, Zhang S, Sherry AD, Gillies RJ, (2002) In vivo magnetic resonance imaging of tissue pH using a novel pH-sensitive contrast agent, GdDOTA-4AmP. Acad Radiol 9 (Suppl 2): S481-483.
7. Smalley RV, Lefante J, Bartolucci A, Carpenter J, Vogel C, et al. (1983) A comparison of cyclophosphamide, adriamycin, and 5-fluorouracil (CAF) and cyclophosphamide, methotrexate, 5-fluorouracil, vincristine, and prednisone (CMFVP) in patients with advanced breast cancer. Breast Cancer Res Treat 3: 209-220.
8. Gerweck LE, Vijayappa S, Kozin S, (2006) Tumor pH controls the in vivo efficacy of weak acid and base chemotherapeutics. Mol Cancer Ther 5: 1275-1279.
9. Mahoney BP, Raghunand N, Baggett B, Gillies RJ, (2003) Tumor acidity, ion trapping and chemotherapeutics. I. Acid pH affects the distribution of chemotherapeutic agents in vitro. Biochem Pharmacol 66: 1207-1218.
10. Raghunand N, Mahoney BP, Gillies RJ, (2003) Tumor acidity, ion trapping and chemotherapeutics. II. pH-dependent partition coefficients predict importance of ion trapping on pharmacokinetics of weakly basic chemotherapeutic agents. Biochem Pharmacol 66: 1219-1229.
11. Noel G, Peterson C, Trouet A, Tulkens P, (1978) Uptake and subcellular localization of daunorubicin and adriamycin in cultured fibroblasts. Eur J Cancer 14: 363-368.
12. Schindler M, Grabski S, Hoff E, Simon SM, (1996) Defective pH regulation of acidic compartments in human breast cancer cells (MCF-7) is normalized in adriamycin-resistant cells (MCF-7adr). Biochemistry 35: 2811-2817.
13. Lee CM, Tannock IF, (2006) Inhibition of endosomal sequestration of basic anticancer drugs: influence on cytotoxicity and tissue penetration. Br J Cancer 94: 863-869.
14. Boron WF, (2004) Regulation of intracellular pH. Adv Physiol Educ 28: 160-179.
15. Cutts SM, Nudelman A, Rephaeli A, Phillips DR, (2005) The power and potential of doxorubicin-DNA adducts. IUBMB Life 57: 73-81.
16. Cullinane C, Cutts SM, van Rosmalen A, Phillips DR, (1994) Formation of adriamycin-DNA adducts in vitro. Nucleic Acids Res 22: 2296-2303.
17. Swietach P, Patiar S, Supuran CT, Harris AL, Vaughan-Jones RD, (2009) The role of carbonic anhydrase 9 in regulating extracellular and intracellular ph in three-dimensional tumor cell growths. J Biol Chem 284: 20299-20310.
18. Swietach P, Wigfield S, Cobden P, Supuran CT, Harris AL, et al. (2008) Tumor-associated carbonic anhydrase 9 spatially coordinates intracellular pH in three-dimensional multicellular growths. J Biol Chem 283: 20473-20483.
19. Long BH, Wang L, Lorico A, Wang RC, Brattain MG, et al. (1991) Mechanisms of resistance to etoposide and teniposide in acquired resistant human colon and lung carcinoma cell lines. Cancer Res 51: 5275-5283.
20. Wu L, Smythe AM, Stinson SF, Mullendore LA, Monks A, et al. (1992) Multidrug-resistant phenotype of disease-oriented panels of human tumor cell lines used for anticancer drug screening. Cancer Res 52: 3029-3034.
21. Aouida M, Poulin R, Ramotar D, (2010) The human carnitine transporter SLC22A16 mediates high affinity uptake of the anticancer polyamine analogue bleomycin-A5. J Biol Chem 285: 6275-6284.
22. Hulikova A, Vaughan-Jones RD, Swietach P, (2011) Dual role of CO2/HCO3(-) formula buffer in the regulation of intracellular pH of three-dimensional tumor growths. J Biol Chem 286: 13815-13826.
23. Rzymski T, Milani M, Pike L, Buffa F, Mellor HR, et al. (2010) Regulation of autophagy by ATF4 in response to severe hypoxia. Oncogene 29: 4424-4435.
24. Thomas JA, Buchsbaum RN, Zimniak A, Racker E, (1979) Intracellular pH measurements in Ehrlich ascites tumor cells utilizing spectroscopic probes generated in situ. Biochemistry 18: 2210-2218.
25. Gewirtz DA, (1999) A critical evaluation of the mechanisms of action proposed for the antitumor effects of the anthracycline antibiotics adriamycin and daunorubicin. Biochem Pharmacol 57: 727-741.
26. Durand RE, Olive PL, (1981) Flow cytometry studies of intracellular adriamycin in single cells in vitro. Cancer Res 41: 3489-3494.
27. Luk CK, Tannock IF, (1989) Flow cytometric analysis of doxorubicin accumulation in cells from human and rodent cell lines. J Natl Cancer Inst 81: 55-59.
28. Schneider YJ, Baurain R, Zenebergh A, Trouet A, (1979) DNA-binding parameters of daunorubicin and doxorubicin in the conditions used for studying the interaction of anthracycline-DNA complexes with cells in vitro. Cancer Chemother Pharmacol 2: 7-10.
29. Bryn SR, Dolch GD, (1978) Analysis of binding of daunorubicin and doxorubicin to DNA using computerized curve-fitting procedures. J Pharm Sci 67: 688-693.
30. Okabe M, Unno M, Harigae H, Kaku M, Okitsu Y, et al. (2005) Characterization of the organic cation transporter SLC22A16: a doxorubicin importer. Biochem Biophys Res Commun 333: 754-762.
31. Roninson IB, Chin JE, Choi KG, Gros P, Housman DE, et al. (1986) Isolation of human mdr DNA sequences amplified in multidrug-resistant KB carcinoma cells. Proc Natl Acad Sci U S A 83: 4538-4542.
32. Karukstis KK, Thompson EH, Whiles JA, Rosenfeld RJ, (1998) Deciphering the fluorescence signature of daunomycin and doxorubicin. Biophys Chem 73: 249-263.
33. Huber V, De Milito A, Harguindey S, Reshkin SJ, Wahl ML, et al. (2010) Proton dynamics in cancer. J Transl Med 8: 57.
34. Luciani F, Spada M, De Milito A, Molinari A, Rivoltini L, et al. (2004) Effect of proton pump inhibitor pretreatment on resistance of solid tumors to cytotoxic drugs. J Natl Cancer Inst 96: 1702-1713.