Induction of 1C aldoketoreductases and other drug dose-dependent genes upon acquisition of anthracycline resistance

Pharmacogenetics and Genomics

Volumn 19, Issue 6, 2009, Pages 477-488

  Veitch, Zachary W ^a,c   Guo, Baoqing ^c   Hembruff, Stacey L ^c   Bewick, Adam J ^c   Heibein, Allan D ^a   Eng, Jamei ^e   Cull, Stephanie ^b   MacLean, David A ^b,d   Parissenti, Amadeo M ^a,c,d,e  

^a SUDBURY REGIONAL HOSPITAL   (Canada)

^b LAURENTIAN UNIVERSITY   (Canada)

^c Sudbury Regional Hospital   (Canada)

^d NORTHERN ONTARIO SCHOOL OF MEDICINE   (Canada)

^e UNIVERSITY OF OTTAWA   (Canada)

Author keywords

5b cholanic acid; Abcb1; Aldoketoreductase; Breast cancer; CDNA microarray; Doxorubicin; Drug resistance; Epirubicin; Quantitative polymerase chain reaction

Indexed keywords

ANTHRACYCLINE; DNA; DOXORUBICIN; DOXORUBICINOL; EPIRUBICIN; MULTIDRUG RESISTANCE PROTEIN 1; OSTEOGENIC PROTEIN 1; 15 HYDROXYPROSTAGLANDIN DEHYDROGENASE; 3(OR 17)BETA HYDROXYSTEROID DEHYDROGENASE; AKR1C2 PROTEIN, HUMAN; AKR1C3 PROTEIN, HUMAN; ANTINEOPLASTIC ANTIBIOTIC; ENZYME INHIBITOR; HYDROXYSTEROID DEHYDROGENASE;

ALDOKETOREDUCTASE 1C1 GENE; ALDOKETOREDUCTASE 1C3 GENE; ANTIBIOTIC RESISTANCE; APOPTOSIS; ARTICLE; BREAST TUMOR; CELL ACTIVITY; CELL COMMUNICATION; CELL PROLIFERATION; CONTROLLED STUDY; DNA MICROARRAY; DOSE RESPONSE; DRUG TRANSPORT; GENE EXPRESSION; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; GENOTYPE; HUMAN; HUMAN CELL; IMMUNE SYSTEM; OXIDATION REDUCTION REACTION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN STRUCTURE; QUANTITATIVE ANALYSIS; WILD TYPE; DRUG ANTAGONISM; DRUG RESISTANCE; FEMALE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; TUMOR CELL LINE;

3-HYDROXYSTEROID DEHYDROGENASES; ANTIBIOTICS, ANTINEOPLASTIC; BREAST NEOPLASMS; CELL LINE, TUMOR; DOXORUBICIN; DRUG RESISTANCE, NEOPLASM; ENZYME INHIBITORS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; HYDROXYPROSTAGLANDIN DEHYDROGENASES; HYDROXYSTEROID DEHYDROGENASES; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS;

EID: 70149116449     PISSN: 17446872     EISSN: 17446880     Source Type: Journal    
DOI: 10.1097/FPC.0b013e32832c484b     Document Type: Article

References (56)

1. Gottesman MM, Pastan I. Resistance to multiple chemotherapeutic agents in human cancer cells. Trends Pharmacol Sci 1988; 9:54-58.
2. Cole SP, Bhardwaj G, Gerlach JH, Mackie JE, Grant CE, Almquist KC, et al. Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science 1992; 258:1650-1654.
3. Manoharan TH, Welch PJ, Gulick AM, Puchalski RB, Lathrop AL, Fahl WE. Expression of tandem glutathione S-transferase recombinant genes in COS cells for analysis of efficiency of protein expression and associated drug resistance. Mol Pharmacol 1991; 39:461-467.
4. Giaccone G, Gazdar AF, Beck H, Zunino F, Capranico G. Multidrug sensitivity phenotype of human lung cancer cells associated with topoisomerase II expression. Cancer Res 1992; 52:1666-1674.
5. Lee MS, Wang JC, Beran M. Two independent amsacrine-resistant human myeloid leukemia cell lines share an identical point mutation in the 170 kDa form of human topoisomerase II. J Mol Biol 1992; 223:837-843.
6. Hurwitz SJ, Terashima M, Mizunuma N, Slapak CA. Vesicular anthracycline accumulation in doxorubicin-selected U-937 cells: participation of lysosomes. Blood 1997; 89:3745-3754.
7. Lam V, McPherson JP, Salmena L, Lees J, Chu W, Sexsmith E, et al. p53 gene status and chemosensitivity of childhood acute lymphoblastic leukemia cells to adriamycin. Leuk Res 1999; 23:871-880.
8. Baer MR, George SL, Dodge RK, O'Loughlin KL, Minderman H, Caligiuri MA, et al. Phase 3 study of the multidrug resistance modulator PSC-833 in previously untreated patients 60 years of age and older with acute myeloid leukemia: cancer and leukemia group B study 9720. Blood 2002; 100:1224-1232.
9. Pusztai L, Wagner P, Ibrahim N, Rivera E, Theriault R, Booser D, et al. Phase II study of tariquidar, a selective P-glycoprotein inhibitor, in patients with chemotherapy-resistant, advanced breast carcinoma. Cancer 2005; 104:682-691.
10. Parissenti AM, Hembruff SL, Villeneuve DJ, Veitch Z, Guo B, Eng J. Gene expression profiles as biomarkers for the prediction of chemotherapy drug response in human tumour cells. Anticancer Drugs 2007; 18:499-523.
11. Liscovitch M, Ravid D. A case study in misidentification of cancer cell lines: MCF-7/AdrR cells (re-designated NCI/ADR-RES) are derived from OVCA R-8 human ovarian carcinoma cells. Cancer Lett 2006; 245:350-352.
12. Ozols RF, Willson JK, Weltz MD, Grotzinger KR, Myers CE, Young RC. Inhibition of human ovarian cancer colony formation by adriamycin and its major metabolites. Cancer Res 1980; 40:4109-4112.
13. Reed K, Hembruff SL, Laberge ML, Villeneuve DJ, Cote GB, Parissenti AM. Hypermethylation of the ABCB1 downstream gene promoter accompanies ABCB1 gene amplification and increased expression in docetaxel-resistant MCF-7 breast tumor cells. Epigenetics 2008; 3:1-11.
14. Guo B, Hembruff SL, Villeneuve DJ, Kirwan AF, Parissenti AM. Potent killing of paclitaxel-and doxorubicin-resistant breast cancer cells by calphostin C accompanied by cytoplasmic vacuolization. Breast Cancer Res Treat 2003; 82:125-141.
15. Guo B, Villeneuve DJ, Hembruff SL, Kirwan AF, Blais DE, Bonin M, et al. Cross-resistance studies of isogenic drug-resistant breast tumor cell lines support recent clinical evidence suggesting that sensitivity to paclitaxel may be strongly compromised by prior doxorubicin exposure. Breast Cancer Res Tr e a t 2004; 85:31-51.
16. Brazma A, Hingamp P, Quackenbush J, Sherlock G, Spellman P, Stoeckert C, et al. Minimum information about a microarray experiment (MIAME)-toward standards for microarray data. Nat Genet 2001; 29:365-371.
17. Villeneuve DJ, Hembruff SL, Veitch Z, Cecchetto M, Dew WA, Parissenti AM. cDNA microarray analysis of isogenic paclitaxel-and doxorubicin-resistant breast tumor cell lines reveals distinct drug-specific genetic signatures of resistance. Breast Cancer Res Treat 2006; 96:17-39.
18. Villeneuve DJ, Parissenti AM. The use of DNA microarrays to investigate the pharmacogenomics of drug response in living systems. Curr Top Med Chem 2004; 4:1329-1345.
19. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 2001; 98:5116-5121.
20. Hembruff SL, Villeneuve DJ, Parissenti AM. The optimization of quantitative reverse transcription PCR for verification of cDNA microarray data. Anal Biochem 2005; 345:237-249.
21. Stoffel-Wagner B, Watzka M, Steckelbroeck S, Ludwig M, Clusmann H, Bidlingmaier F, et al. Allopregnanolone serum levels and expression of 5 alpha-reductase and 3 alpha-hydroxysteroid dehydrogenase isoforms in hippocampal and temporal cortex of patients with epilepsy. Epilepsy Res 2003; 54:11-19.
22. Cusack BJ, Tesnohlidek DA, Loseke VL, Vestal RE, Brenner DE, Olson RD. Effect of phenytoin on the pharmacokinetics of doxorubicin and doxorubicinol in the rabbit. Cancer Chemother Pharmacol 1988; 22:294-298.
23. Behnia K, Boroujerdi M. Inhibition of aldo-keto reductases by phenobarbital alters metabolism, pharmacokinetics and toxicity of doxorubicin in rats. J Pharm Pharmacol 1999; 51:1275-1282.
24. Bains OS, Takahashi RH, Pfeifer TA, Grigliatti TA, Reid RE, Riggs KW. Two allelic variants of aldo-keto reductase 1A1 exhibit reduced in vitro metabolism of daunorubicin. Drug Metab Dispos 2008; 36:904-910.
25. Fogli S, Danesi R, Innocenti F, Di PA, Bocci G, Barbara C, et al. An improved HPLC method for therapeutic drug monitoring of daunorubicin, idarubicin, doxorubicin, epirubicin, and their 13-dihydro metabolites in human plasma. Ther Drug Monit 1999; 21:367-375.
26. Steckelbroeck S, Oyesanmi B, Jin Y, Lee SH, Kloosterboer HJ, Penning TM. Tibolone metabolism in human liver is catalyzed by 3alpha/ 3beta-hydroxysteroid dehydrogenase activities of the four isoforms of the aldo-keto reductase (AKR)1C subfamily. J Pharmacol Exp Ther 2006; 316:1300-1309.
27. Chang JC, Wooten EC, Tsimelzon A, Hilsenbeck SG, Gutierrez MC, Elledge R, et al. Gene expression profiling for the prediction of therapeutic response to docetaxel in patients with breast cancer. Lancet 2003; 362:362-369.
28. Iwao-Koizumi K, Matoba R, Ueno N, Kim SJ, Ando A, Miyoshi Y, et al. Prediction of docetaxel response in human breast cancer by gene expression profiling. J Clin Oncol 2005; 23:422-431.
29. Andre F, Mazouni C, Hortobagyi GN, Pusztai L. DNA arrays as predictors of efficacy of adjuvant/neoadjuvant chemotherapy in breast cancer patients: current data and issues on study design. Biochim Biophys Acta 2006; 1766:197-204.
30. Bar-Joseph Z, Gerber G, Simon I, Gifford DK, Jaakkola TS. Comparing the continuous representation of time-series expression profiles to identify differentially expressed genes. Proc Natl Acad Sci U S A 2003; 100:10146-10151.
31. Nueda MJ, Conesa A, Westerhuis JA, Hoefsloot HC, Smilde AK, Talon M, et al. Discovering gene expression patterns in Time Course Microarray Experiments by ANOVA-SCA. Bioinformatics 2007; 23:1792-1800.
32. Szakacs G, Annereau JP, Lababidi S, Shankavaram U, Arciello A, Bussey KJ, et al. Predicting drug sensitivity and resistance: profiling ABC transporter genes in cancer cells. Cancer Cell 2004; 6:129-137.
33. Hembruff SL, Laberge ML, Villeneuve DJ, Guo B, Veitch Z, Cecchetto M, et al. Role of drug transporters and drug accumulation in the temporal acquisition of drug resistance. BMC Cancer 2008; 8:318.
34. Plebuch M, Soldan M, Hungerer C, Koch L, Maser E. Increased resistance of tumor cells to daunorubicin after transfection of cDNAs coding for anthracycline inactivating enzymes. Cancer Lett 2007; 255:49-56.
35. Annereau JP, Szakacs G, Tucker CJ, Arciello A, Cardarelli C, Collins J, et al. Analysis of ATP-binding cassette transporter expression in drug-selected cell lines by a microarray dedicated to multidrug resistance. Mol Pharmacol 2004; 66:1397-1405.
36. Dan S, Tsunoda T, Kitahara O, Yanagawa R, Zembutsu H, Katagiri T, et al. An integrated database of chemosensitivity to 55 anticancer drugs and gene expression profiles of 39 human cancer cell lines. Cancer Res 2002; 62:1139-1147. (Pubitemid 34160300)
37. Hung JJ, Chow KC, Wang HW, Wang LS. Expression of dihydrodiol dehydrogenase and resistance to chemotherapy and radiotherapy in adenocarcinoma cells of lung. Anticancer Res 2006; 26:2949-2955.
38. Tai HL, Lin TS, Huang HH, Lin TY, Chou MC, Chiou SH, et al. Overexpression of aldo-keto reductase 1C2 as a high-risk factor in bladder cancer. Oncol Rep 2007; 17:305-311.
39. Penning TM, Burczynski ME, Jez JM, Hung CF, Lin HK, Ma H, et al. Human 3alpha-hydroxysteroid dehydrogenase isoforms (AKR1C1-AKR1C4) of the aldo-keto reductase superfamily: functional plasticity and tissue distribution reveals roles in the inactivation and formation of male and female sex hormones. Biochem J 2000; 351:67-77.
40. Albini A, Graf J, Kitten GT, Kleinman HK, Martin GR, Veillette A, et al. 17 beta-estradiol regulates and v-Ha-ras transfection constitutively enhances MCF7 breast cancer cell interactions with basement membrane. Proc Natl Acad Sci U S A 1986; 83:8182-8186.
41. Rajah TT, Pento JT. Influence of antiestrogens on the invasiveness and laminin attachment of breast cancer cells. Cancer Invest 1999; 17:10-18.
42. Jin Y, Penning TM. Aldo-keto reductases and bioactivation/detoxication. Annu Rev Pharmacol Toxicol 2007; 47:263-292.
43. Ax W, Soldan M, Koch L, Maser E. Development of daunorubicin resistance in tumour cells by induction of carbonyl reduction. Biochem Pharmacol 2000; 59:293-300.
44. Keizer HG, Schuurhuis GJ, Broxterman HJ, Lankelma J, Schoonen WG, van RJ, et al. Correlation of multidrug resistance with decreased drug accumulation, altered subcellular drug distribution, and increased P-glycoprotein expression in cultured SW-1573 human lung tumor cells. Cancer Res 1989; 49:2988-2993.
45. Schuurhuis GJ, Broxterman HJ, de Lange JH, Pinedo HM, van Heijningen TH, Kuiper CM, et al. Early multidrug resistance, defined by changes in intracellular doxorubicin distribution, independent of P-glycoprotein. Br J Cancer 1991; 64:857-861.
46. Coley HM, Amos WB, Twentyman PR, Workman P. Examination by laser scanning confocal fluorescence imaging microscopy of the subcellular localisation of anthracyclines in parent and multidrug resistant cell lines. Br J Cancer 1993; 67:1316-1323.
47. Bachur NR, Gordon SL, Gee MV. Anthracycline antibiotic augmentation of microsomal electron transport and free radical formation. Mol Pharmacol 1977; 13:901-910.
48. Lou H, Du S, Ji Q, Stolz A. Induction of AKR1C2 by phase II inducers: identification of a distal consensus antioxidant response element regulated by NRF2. Mol Pharmacol 2006; 69:1662-1672.
49. Penning TM, Drury JE. Human aldo-keto reductases: function, gene regulation, and single nucleotide polymorphisms. Arch Biochem Biophys 2007; 464:241-250.
50. Pietsch EC, Chan JY, Torti FM, Torti SV. Nrf2 mediates the induction of ferritin H in response to xenobiotics and cancer chemopreventive dithiolethiones. J Biol Chem 2003; 278:2361-2369.
51. Kim YC, Yamaguchi Y, Kondo N, Masutani H, Yodoi J. Thioredoxin-dependent redox regulation of the antioxidant responsive element (ARE) in electrophile response. Oncogene 2003; 22:1860-1865.
52. Andrews GK. Regulation of metallothionein gene expression by oxidative stress and metalions. Biochem Pharmacol 2000; 59:95-104.
53. Zhu H, Cai C, Chen J. Suppression of P-glycoprotein gene expression in Hs578T/Dox by the overexpression of caveolin-1. FEBS Lett 2004; 576:369-374. (Pubitemid 39388630)
54. Arumugam T, Simeone DM, Schmidt AM, Logsdon CD. S100P stimulates cell proliferation and survival via receptor for activated glycation end products (RAGE). J Biol Chem 2004; 279:5059-5065.
55. Yang S, Lim M, Pham LK, Kendall SE, Reddi AH, Altieri DC, et al. Bone morphogenetic protein 7 protects prostate cancer cells from stress-induced apoptosis via both Smad and c-Jun NH2-terminal kinase pathways. Cancer Res 2006; 66:4285-4290.
56. Alarmo EL, Kuukasjarvi T, Karhu R, Kallioniemi A. A comprehensive expression survey of bone morphogenetic proteins in breast cancer highlights the importance of BMP4 and BMP7. Breast Cancer Res Treat 2007; 103:239-246.