Prognostic impact of multidrug resistance gene expression on the management of breast cancer in the context of adjuvant therapy based on a series of 171 patients

British Journal of Cancer

Volumn 94, Issue 4, 2006, Pages 473-480

  Moureau Zabotto, L ^a,c   Ricci, S ^a   Lefranc, J P ^b   Coulet, F ^a,d   Genestie, C ^b   Antoine, M ^a   Uzan, S ^a   Lotz, J P ^a   Touboul, E ^a   Lacave, R ^a  

^a HÔPITAL TENON   (France)

^b ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

^c INSTITUT PAOLI CALMETTES   (France)

^d Centre de Génétique   (France)

Author keywords

Breast cancer; GSTPI; MDRI; MRPI; Prognosis; rt PCR

Indexed keywords

GLUTATHIONE TRANSFERASE P1; MULTIDRUG RESISTANCE PROTEIN 1;

ADULT; AGED; ARTICLE; BREAST CANCER; CANCER ADJUVANT THERAPY; CANCER RADIOTHERAPY; CANCER STAGING; CANCER SURGERY; CANCER SURVIVAL; CANCER TISSUE; CONTROLLED STUDY; CORRELATION ANALYSIS; DISEASE FREE SURVIVAL; FEMALE; FOLLOW UP; GENE EXPRESSION; HORMONAL THERAPY; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; MULTIDRUG RESISTANCE; MULTIVARIATE ANALYSIS; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; STATISTICAL SIGNIFICANCE; UNIVARIATE ANALYSIS;

ADULT; AGED; BREAST NEOPLASMS; CHEMOTHERAPY, ADJUVANT; DISEASE-FREE SURVIVAL; FEMALE; GENE EXPRESSION PROFILING; GENES, MDR; GLUTATHIONE S-TRANSFERASE PI; HUMANS; MIDDLE AGED; MULTIDRUG RESISTANCE-ASSOCIATED PROTEINS; MULTIVARIATE ANALYSIS; P-GLYCOPROTEIN; PROGNOSIS; RADIOTHERAPY, ADJUVANT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 33344456074     PISSN: 00070920     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.bjc.6602958     Document Type: Article

References (60)

1. Adler V, Yin Z, Fuchs SY, Benezra M, Rosario L, Tew KD, Pincus MR, Sardana M, Henderson CJ, Wolf CR, Davis RJ, Ronai Z (1999) Regulation of JNK signaling by GSTp. EMBO J 18: 1321-1334
2. Akiyama S, Fojo A, Hanover JA, Pastan I, Gottesman MM (1985) Isolation and genetic characterization of human KB cell lines resistant to multiple drugs. Somat Cell Mol Genet 11: 117-126
3. Beck WT, Grogan TM, Willman CL, Cordon-Cardo C, Parham DM, Kuttesch JF, Andreeff M, Bates SE, Berard CW, Boyett JM, Brophy NA, Broxterman HJ, Chan HS, Dalton WS, Dietel M, Fojo AT, Gascoyne RD, Head D, Houghton PJ, Srivastava DK, Lehnert M, Leith CP, Paietta E, Pavelic ZP, Weinstein R (1996) Methods to detect P-glycoprotein-associated multidrug resistance in patients' tumors: consensus recommendations. Cancer Res 56: 3010-3020
4. Benard J, Da Silva J, De Blois MC, Boyer P, Duvillard P, Chiric E, Riou G (1985) Characterization of a human ovarian adenocarcinoma line, IGROV1, in tissue culture and in nude mice. Cancer Res 45: 4970-4979
5. Bennaceur-Griscelli A, Bosq J, Koscielny S, Lefrere F, Turhan A, Brousse N, Hermine O, Ribrag V (2004) High level of glutathione-S-transferase pi expression in mantle cell lymphomas. Clin Cancer Res 10: 3029-3034
6. Boku N, Chin K, Hosokawa K, Ohtsu A, Tajiri H, Yoshida S, Yamao T, Kondo H, Shirao K, Shimada Y, Saito D, Hasebe T, Mukai K, Seki S, Saito H, Johnston PG (1998) Biological markers as a predictor for response and prognosis of unresectable gastric cancer patients treated with 5-fluorouracil and cis-platinum. Clin Cancer Res 4: 1469-1474
7. Bonadonna G, Veronesi U, Brambilla C, Ferrari L, Luini A, Greco M, Bartoli C, Coopmans de Yoldi G, Zucali R, Rilke F (1990) Primary chemotherapy to avoid mastectomy in tumors with diameters of three centimeters or more. J Natl Cancer Inst 82: 1539-1545
8. Burger H, Foekens JA, Look MP, Meijer-van Gelder ME, Klijn JG, Wiemer EA, Stoter G, Nooter K (2003) RNA expression of breast cancer resistance protein, lung resistance-related protein, multidrug resistance-associated proteins 1 and 2, and multidrug resistance gene 1 in breast cancer: correlation with chemotherapeutic response. Clin Cancer Res 9: 827-836
9. Buser K, Joncourt F, Altermatt HJ, Bacchi M, Oberli A, Cerny T (1997) Breast cancer: pretreatment drug resistance parameters (GSH-system, ATase, P-glycoprotein) in tumor tissue and their correlation with clinical and prognostic characteristics. Ann Oncol 8: 335-341
10. Chassevent A, Jourdan ML, Romain S, Descotes F, Colonna M, Martin PM, Bolla M, Spyratos F (2001) S-Phase Fraction and DNA Ploidy in 633 T1T2 breast cancers a standardized flow cytometric study. Clin Cancer Res 7: 909-917
11. Chevillard S, Pouillart P, Beldjord C, Asselain B, Beuzeboc P, Magdelenat H, Vielh P (1996) Sequential assessment of multidrug phenotype and measurement of S-phase fraction as predictive markers of breast cancer response to neoadjuvant chemotherapy. Cancer 77: 292-300
12. Cole SP, Sparks KE, Fraser K, Loe DW, Grant CE, Wilson GM, Deeley RG (1994) Pharmacological characterization of multidrug resistant MRP-transfected human tumor cells. Cancer Res 54: 5902-5910
13. Cox DR (1972) Regression models and life tables. J R Statist Soc B 34: 187-220
14. Cullen KJ, Newkirk KA, Schumaker LM, Aldosari N, Rone JD, Haddad BR (2003) Glutathione S-transferase pi amplification is associated with cisplatin resistance in head and neck squamous cell carcinoma cell lines and primary tumors. Cancer Res 63: 8097-8102
15. Das PM, Singal R (2004) DNA methylation and cancer. J Clin Oncol 22: 4632-4642
16. Dean M, Hamon Y, Chimini G (2001) The human ATP-binding cassette (ABC) transporter superfamily. J Lipid Res 42: 1007-1017
17. Depeille P, Cuq P, Mary S, Passagne I, Evrard A, Cupissol D, Vian L (2004) Glutathione S-transferase M1 and multidrug resistance protein 1 act in synergy to protect melanoma cells from vincristine effects. Mol Pharmacol 65: 897-905
18. Depeille P, Cuq P, Passagne I, Evrard A, Vian L (2005) Combined effects of GSTP1 and MRP1 in melanoma drug resistance. Br J Cancer 93: 216-223
19. Elsby R, Kitteringham NR, Goldring CE, Lovatt CA, Chamberlain M, Henderson CJ, Wolf CR, Park BK (2003) Increased constitutive c-Jun N-terminal kinase signaling in mice lacking glutathione S-transferase Pi. J Biol Chem 278: 22243-22249
20. Endicott JA, Ling V (1989) The biochemistry of P-glycoprotein-mediated multidrug resistance. Annu Rev Biochem 58: 137-171
21. Esteller M, Corn PG, Urena JM, Gabrielson E, Baylin SB, Herman JG (1998) Inactivation of glutathione S-transferase P1 gene by promoter hypermethylation in human neoplasia. Cancer Res 58: 4515-4518
22. Ferrandina G, Scambia G, Damia G, Tagliabue G, Fagotti A, Benedetti Panici P, Mangioni C, Mancuso S, D'Incalci M (1997) Glutathione S-transferase activity in epithelial ovarian cancer: association with response to chemotherapy and disease outcome. Ann Oncol 8: 343-350
23. Ferrero JM, Etienne MC, Formento JL, Francoual M, Rostagno P, Peyrottes I, Ettore F, Teissier E, Leblanc-Talent P, Namer M, Milano G (2000) Application of an original RT-PCR-ELISA multiplex assay for MDR1 and MRP, along with p53 determination in node-positive breast cancer patients. Br J Cancer 82: 171-177
24. Frassoldati A, Adami F, Banzi C, Criscuolo M, Piccinini L, Silingardi V (1997) Changes of biological features in breast cancer cells determined by primary chemotherapy. Breast Cancer Res Treat 44: 185-192
25. Galimberti S, Testi R, Guerrini F, Fazzi R, Petrini M (2003) The clinical relevance of the expression of several multidrug-resistant-related genes in patients with primary acute myeloid leukemia. J Chemother 15: 374-379
26. Goasguen JE, Lamy T, Bergeron C, Ly Sunaram B, Mordelet E, Gorre G, Dossot JM, Le Gall E, Grosbois B, Le Prise PY, Fauchet R (1996) Multifactorial drug-resistance phenomenon in acute leukemias: impact of P170-MDR1, LRP56 protein, glutathione-transferases and metallothionein systems on clinical outcome. Leuk Lymphoma 23: 567-576
27. Gottesman MM, Pastan I (1993) Biochemistry of multidrug resistance mediated by the multidrug transporter. Annu Rev Biochem 62: 385-427
28. Howells RE, Redman CW, Dhar KK, Sarhanis P, Musgrove C, Jones PW, Alldersea J, Fryer AA, Hoban PR, Strange RC (1998) Association of glutathione S-transferase GSTM1 and GSTT1 null genotypes with clinical outcome in epithelial ovarian cancer. Clin Cancer Res 4: 2439-2445
29. Ito K, Fujimori M, Nakata S, Hama Y, Shingu K, Kobayashi S, Tsuchiya S, Kohno K, Kuwano M, Amano J (1998) Clinical significance of the increased multidrug resistance-associated protein (MRP) gene expression in patients with primary breast cancer. Oncol Res 10: 99-109
30. Jhaveri MS, Morrow CS (1998) Methylation-mediated regulation of the glutathione S-transferase P1 gene in human breast cancer cells. Gene 210: 1-7
31. Jones PA, Baylin SB (2002) The fundamental role of epigenetic events in cancer. Nat Rev Genet 3: 415-428
32. Kanzaki A, Toi M, Nakayama K, Bando H, Mutoh M, Uchida T, Fukumoto M, Takebayashi Y (2001) Expression of multidrug resistance-related transporters in human breast carcinoma. Jpn J Cancer Res 92: 452-458
33. Kaplan ES, Meier P (1958) Non parametric estimation from incomplete observations. Am Stat Assoc J 53: 457-480
34. Kearns PR, Pieters R, Rottier MM, Pearson AD, Hall AG (2001) Raised blast glutathione levels are associated with an increased risk of relapse in childhood acute lymphocytic leukemia. Blood 97: 393-398
35. Keith WN, Stallard S, Brown R (1990) Expression of mdr1 and gst-pi in human breast tumours: comparison to in vitro chemosensitivity. Br J Cancer 61: 712-716
36. Lacave R, Coulet F, Ricci S, Touboul E, Flahault A, Rateau JG, Cesari D, Lefranc JP, Bernaudin JF (1998) Comparative evaluation by semiquantitative reverse transcriptase polymerase chain reaction of MDR1, MRP and GSTp gene expression in breast carcinomas. Br J Cancer 77: 694-702
37. Leonessa F, Clarke R (2003) ATP binding cassette transporters and drug resistance in breast cancer. Endocr Relat Cancer 10: 43-73
38. Lin X, Nelson WG (2003) Methyl-CpG-binding domain protein-2 mediates transcriptional repression associated with hypermethylated GSTP1 CpG islands in MCF-7 breast cancer cells. Cancer Res 63: 498-504
39. Morales MC, Perez-Yarza G, Nieto-Rementeria N, Boyano MD, Jangi M, Atencia R, Asumendi A (2005) Intracellular glutathione levels determine cell sensitivity to apoptosis induced by the antineoplasic agent N-(4-hydroxyphenyl) retinamide. Anticancer Res 25: 1945-1951
40. Morrow CS, Smitherman PK, Diah SK, Schneider E, Townsend AJ (1998) Coordinated action of glutathione S-transferases (GSTs) and multidrug resistance protein 1 (MRP1) in antineoplastic drug detoxification. Mechanism of GST A1-1- and MRP1-associated resistance to chlorambucil in MCF7 breast carcinoma cells. J Biol Chem 273: 20114-20120
41. Muller M, Meijer C, Zaman GJ, Borst P, Scheper RJ, Mulder NH, de Vries EG, Jansen PL (1994) Overexpression of the gene encoding the multidrug resistance-associated protein results in increased ATP-dependent glutathione S-conjugate transport. Proc Natl Acad Sci USA 91: 13033-13037
42. O'Brien M, Kruh GD, Tew KD (2000) The influence of coordinate overexpression of glutathione phase II detoxification gene products on drug resistance. J Pharmacol Exp Ther 294: 480-487
43. Oudard S, Levalois C, Andrieu JM, Bougaran J, Validire P, Thiounn N, Poupon MF, Fourme E, Chevillard S (2002) Expression of genes involved in chemoresistance, proliferation and apoptosis in clinical samples of renal cell carcinoma and correlation with clinical outcome. Anticancer Res 22: 121-128
44. Raitano AB, Halpern JR, Hambuch TM, Sawyers CL (1995) The Bcr-Abl leukemia oncogene activates Jun kinase and requires Jun for transformation. Proc Natl Acad Sci USA 92: 11746-11750
45. Rappa G, Lorico A, Flavell RA, Sartorelli AC (1997) Evidence that the multidrug resistance protein (MRP) functions as a co-transporter of glutathione and natural product toxins. Cancer Res 57: 5232-5237
46. Ruscoe JE, Rosario LA, Wang T, Gate L, Arifoglu P, Wolf CR, Henderson CJ, Ronai Z, Tew KD (2001) Pharmacologic or genetic manipulation of glutathione S-transferase P1-1 (GSTpi) influences cell proliferation pathways. J Pharmacol Exp Ther 298: 339-345
47. Scholl SM, Fourquet A, Asselain B, Pierga JY, Vilcoq JR, Durand JC, Dorval T, Palangie T, Jouve M, Beuzeboc P (1994) Neoadjuvant vs adjuvant chemotherapy in premenopausal patients with tumours considered too large for breast conserving surgery: preliminary results of a randomised trial: S6. Eur J Cancer 30: 645-652
48. Shinozaki M, Hoon DS, Giuliano AE, Hansen NM, Wang HJ, Turner R, Taback B (2005) Distinct hypermethylation profile of primary breast cancer is associated with sentinel lymph node metastasis. Clin Cancer Res 11: 2156-2162
49. Silvestrini R, Veneroni S, Benini E, Daidone MG, Luisi A, Leutner M, Maucione A, Kenda R, Zucali R, Veronesi U (1997) Expression of p53, glutathione S-transferase-pi, and Bcl-2 proteins and benefit from adjuvant radiotherapy in breast cancer. J Natl Cancer Inst 89: 639-645
50. Simon SM, Schindler M (1994) Cell biological mechanisms of multidrug resistance in tumors. Proc Natl Acad Sci USA 91: 3497-3504
51. Soule HD, Vazguez J, Long A, Albert S, Brennan M (1973) A human cell line from a pleural effusion derived from a breast carcinoma. J Natl Cancer Inst 51: 1409-1416
52. Stoehlmacher J, Park DJ, Zhang W, Groshen S, Tsao-Wei DD, Yu MC, Lenz HJ (2002) Association between glutathione S-transferase P1, T1, and M1 genetic polymorphism and survival of patients with metastatic colorectal cancer. J Natl Cancer Inst 94: 936-942
53. Surowiak P, Materna V, Matkowski R, Szczuraszek K, Kornafel J, Wojnar A, Pudelko M, Dietel M, Denkert C, Zabel M, Lage H (2005) Relationship between the expression of cyclooxygenase 2 and MDR1/P-glycoprotein in invasive breast cancers and their prognostic significance. Breast Cancer Res 7: 862-870
54. Takahashi M, Sato T, Shinohara F, Echigo S, Rikiishi H (2005) Possible role of glutathione in mitochondrial apoptosis of human oral squamous cell carcinoma caused by inorganic selenium compounds. Int J Oncol 27: 489-495
55. Timokhina I, Kissel H, Stella G, Besmer P (1998) Kit signaling through PI 3-kinase and Src kinase pathways: an essential role for Rac1 and JNK activation in mast cell proliferation. EMBO J 17: 6250-6262
56. Tournier C, Hess P, Yang DD, Xu J, Turner TK, Nimnual A, Bar-Sagi D, Jones SN, Flavell RA, Davis RJ (2000) Requirement of JNK for stress-induced activation of the cytochrome c-mediated death pathway. Science 288: 870-874
57. Trock BJ, Leonessa F, Clarke R (1997) Multidrug resistance in breast cancer: a meta-analysis of MDR1/gp170 expression and its possible functional significance. J Natl Cancer Inst 89: 917-931
58. Verma M, Maruvada P, Srivastava S (2004) Epigenetics and cancer. Crit Rev Clin Lab Sci 41: 585-607
59. Widschwendter M, Jones PA (2002) DNA methylation and breast carcinogenesis. Oncogene 21: 5462-5482
60. Xiao L, Lang W (2000) A dominant role for the c-Jun NH2-terminal kinase in oncogenic ras-induced morphologic transformation of human lung carcinoma cells. Cancer Res 60: 400-408