Low expression levels of ATM may substitute for CHEK2 /TP53 mutations predicting resistance towards anthracycline and mitomycin chemotherapy in breast cancer

Breast Cancer Research

Volumn 14, Issue 2, 2012, Pages

  Knappskog, Stian ^a,b   Chrisanthar, Ranjan ^a,b,i   Løkkevik, Erik ^c   Anker, Gun ^a,b   Østenstad, Bjørn ^d   Lundgren, Steinar ^e,f   Risberg, Terje ^g   Mjaaland, Ingvil ^h   Leirvaag, Beryl ^a,b   Miletic, Hrvoje ^a,b   Lønning, Per E ^a,b  

^a UNIVERSITY OF BERGEN   (Norway)

^b HAUKELAND UNIVERSITY HOSPITAL   (Norway)

^c OSLO UNIVERSITY HOSPITAL   (Norway)

^d ULLEVÅL UNIVERSITY HOSPITAL   (Norway)

^e TRONDHEIM UNIVERSITY HOSPITAL   (Norway)

^f NORWEGIAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Norway)

^g UNIVERSITY HOSPITAL OF NORTH NORWAY   (Norway)

^h STAVANGER UNIVERSITY HOSPITAL   (Norway)

ⁱ OSLO UNIVERSITY HOSPITAL   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

ANTHRACYCLINE; ATM PROTEIN; CHECKPOINT KINASE 2; DOXORUBICIN; EPIRUBICIN; FLUOROURACIL; MITOMYCIN; PROTEIN P53; ANTINEOPLASTIC AGENT; ANTINEOPLASTIC ANTIBIOTIC; CELL CYCLE PROTEIN; DNA BINDING PROTEIN; PACLITAXEL; PROTEIN SERINE THREONINE KINASE; TUMOR SUPPRESSOR PROTEIN;

ADJUVANT CHEMOTHERAPY; ADJUVANT THERAPY; ADVANCED CANCER; ARTICLE; BREAST BIOPSY; BREAST CANCER; CANCER CHEMOTHERAPY; CANCER RESISTANCE; CLINICAL ARTICLE; COHORT ANALYSIS; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; MONOTHERAPY; NUCLEOTIDE SEQUENCE; PREDICTION; PROSPECTIVE STUDY; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; BREAST TUMOR; CONTROLLED CLINICAL TRIAL; DRUG RESISTANCE; FEMALE; GENE EXPRESSION REGULATION; GENETICS; MORTALITY; MUTATION; PREDICTIVE VALUE; PROMOTER REGION; RANDOMIZED CONTROLLED TRIAL;

ANTHRACYCLINES; ANTIBIOTICS, ANTINEOPLASTIC; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; BREAST NEOPLASMS; CELL CYCLE PROTEINS; COHORT STUDIES; DNA-BINDING PROTEINS; DOXORUBICIN; DRUG RESISTANCE, NEOPLASM; EPIRUBICIN; FEMALE; FLUOROURACIL; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MITOMYCIN; MUTATION; PACLITAXEL; PREDICTIVE VALUE OF TESTS; PROMOTER REGIONS, GENETIC; PROSPECTIVE STUDIES; PROTEIN-SERINE-THREONINE KINASES; TUMOR SUPPRESSOR PROTEIN P53; TUMOR SUPPRESSOR PROTEINS;

EID: 84858144480     PISSN: 14655411     EISSN: 1465542X     Source Type: Journal    
DOI: 10.1186/bcr3147     Document Type: Article

References (44)

1. Lonning PE. Breast cancer prognostication and prediction: are we making progress?. Ann Oncol 2007, 18(Suppl 8):viii3-7.
2. Bartlett JM, Munro AF, Dunn JA, McConkey C, Jordan S, Twelves CJ, Cameron DA, Thomas J, Campbell FM, Rea DW, Provenzano E, Caldas C, Pharoah P, Hiller L, Earl H, Poole CJ. Predictive markers of anthracycline benefit: a prospectively planned analysis of the UK National Epirubicin Adjuvant Trial (NEAT/BR9601). Lancet Oncol 2010, 11:266-274. 10.1016/S1470-2045(10)70006-1, 20079691.
3. Knoop AS, Knudsen H, Balslev E, Rasmussen BB, Overgaard J, Nielsen KV, Schonau A, Gunnarsdottir K, Olsen KE, Mouridsen H, Ejlertsen B. retrospective analysis of topoisomerase IIa amplifications and deletions as predictive markers in primary breast cancer patients randomly assigned to cyclophosphamide, methotrexate, and fluorouracil or cyclophosphamide, epirubicin, and fluorouracil: Danish Breast Cancer Cooperative Group. J Clin Oncol 2005, 23:7483-7490. 10.1200/JCO.2005.11.007, 16234514.
4. Muss HB, Thor AD, Berry DA, Kute T, Liu ET, Koerner F, Cirrincione CT, Budman DR, Wood WC, Barcos M, et al. c-erbB-2 expression and response to adjuvant therapy in women with node-positive early breast cancer. N Engl J Med 1994, 330:1260-1266. Erratum in: N Engl J Med 1994, 331:211, 10.1056/NEJM199405053301802, 7908410.
5. Pritchard KI, Shepherd LE, O'Malley FP, Andrulis IL, Tu D, Bramwell VH, Levine MN. HER2 and responsiveness of breast cancer to adjuvant chemotherapy. N Engl J Med 2006, 354:2103-2111. 10.1056/NEJMoa054504, 16707747.
6. Schmitt CA, Fridman JS, Yang M, Lee S, Baranov E, Hoffman RM, Lowe SW. A senescence program controlled by p53 and p16INK4a contributes to the outcome of cancer therapy. Cell 2002, 109:335-346. 10.1016/S0092-8674(02)00734-1, 12015983.
7. Vogelstein B, Lane D, Levine AJ. Surfing the p53 network. Nature 2000, 408:307-310. 10.1038/35042675, 11099028.
8. Chrisanthar R, Knappskog S, Lokkevik E, Anker G, Ostenstad B, Lundgren S, Berge EO, Risberg T, Mjaaland I, Maehle L, Engebretsen LF, Lillehaug JR, Lonning PE. CHEK2 mutations affecting kinase activity together with mutations in TP53 indicate a functional pathway associated with resistance to epirubicin in primary breast cancer. PLoS ONE 2008, 3:e3062. 10.1371/journal.pone.0003062, 2518116, 18725978.
9. Geisler S, Borresen-Dale AL, Johnsen H, Aas T, Geisler J, Akslen LA, Anker G, Lonning PE. TP53 gene mutations predict the response to neoadjuvant treatment with 5-fluorouracil and mitomycin in locally advanced breast cancer. Clin Cancer Res 2003, 9:5582-5588.
10. Geisler S, Lonning PE, Aas T, Johnsen H, Fluge O, Haugen DF, Lillehaug JR, Akslen LA, Borresen-Dale AL. Influence of TP53 gene alterations and c-erbB-2 expression on the response to treatment with doxorubicin in locally advanced breast cancer. Cancer Res 2001, 61:2505-2512.
11. Lonning PE. Genes causing inherited cancer as beacons to identify the mechanisms of chemoresistance. Trends Mol Med 2004, 10:113-118. 10.1016/j.molmed.2004.01.005, 15102353.
12. Lonning PE, Knappskog S, Staalesen V, Chrisanthar R, Lillehaug JR. Breast cancer prognostication and prediction in the postgenomic era. Ann Oncol 2007, 18:1293-1306. 10.1093/annonc/mdm013, 17317675.
13. Knappskog S, Chrisanthar R, Staalesen V, Borresen-Dale AL, Gram IT, Lillehaug JR, Lonning PE. Mutations and polymorphisms of the p21B transcript in breast cancer. Int J Cancer 2007, 121:908-910. 10.1002/ijc.22777, 17443496.
14. Staalesen V, Leirvaag B, Lillehaug JR, Lonning PE. Genetic and epigenetic changes in p21 and p21B do not correlate with resistance to doxorubicin or mitomycin and 5-fluorouracil in locally advanced breast cancer. Clin Cancer Res 2004, 10:3438-3443. 10.1158/1078-0432.CCR-03-0796, 15161699.
15. Staalesen V, Falck J, Geisler S, Bartkova J, Borresen-Dale AL, Lukas J, Lillehaug JR, Bartek J, Lonning PE. Alternative splicing and mutation status of CHEK2 in stage III breast cancer. Oncogene 2004, 23:8535-8544. 10.1038/sj.onc.1207928, 15361853.
16. Hirao A, Kong YY, Matsuoka S, Wakeham A, Ruland J, Yoshida H, Liu D, Elledge SJ, Mak TW. DNA damage-induced activation of p53 by the checkpoint kinase Chk2. Science 2000, 287:1824-1827. 10.1126/science.287.5459.1824, 10710310.
17. Toledo F, Wahl GM. Regulating the p53 pathway: in vitro hypotheses, in vivo veritas. Nat Rev Cancer 2006, 6:909-923. 10.1038/nrc2012, 17128209.
18. Ahn JY, Schwarz JK, Piwnica-Worms H, Canman CE. Threonine 68 phosphorylation by ataxia telangiectasia mutated is required for efficient activation of Chk2 in response to ionizing radiation. Cancer Res 2000, 60:5934-5936.
19. Matsuoka S, Huang M, Elledge SJ. Linkage of ATM to cell cycle regulation by the Chk2 protein kinase. Science 1998, 282:1893-1897.
20. Canman CE, Lim DS, Cimprich KA, Taya Y, Tamai K, Sakaguchi K, Appella E, Kastan MB, Siliciano JD. Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science 1998, 281:1677-1679.
21. Siliciano JD, Canman CE, Taya Y, Sakaguchi K, Appella E, Kastan MB. DNA damage induces phosphorylation of the amino terminus of p53. Genes Dev 1997, 11:3471-3481. 10.1101/gad.11.24.3471, 316806, 9407038.
22. Jiang H, Reinhardt HC, Bartkova J, Tommiska J, Blomqvist C, Nevanlinna H, Bartek J, Yaffe MB, Hemann MT. The combined status of ATM and p53 link tumor development with therapeutic response. Genes Dev 2009, 23:1895-1909. 10.1101/gad.1815309, 2725944, 19608766.
23. Chrisanthar R, Knappskog S, lokkevik E, Anker G, Ostenstad B, Lundgren S, Risberg T, Mjaaland I, Skjonsberg G, Aas T, Schlichting E, Fjosne HE, Nysted A, Lillehaug JR, Lonning PE. Predictive and prognostic impact of TP53 mutations and MDM2 promoter genotype in primary breast cancer patients treated with epirubicin or paclitaxel. PLoS ONE 2011, 6:e19249. 10.1371/journal.pone.0019249, 3083424, 21556366.
24. Berge EO, Knappskog S, Geisler S, Staalesen V, Pacal M, Borresen-Dale AL, Puntervoll P, Lillehaug JR, Lonning PE. Identification and characterization of retinoblastoma gene mutations disturbing apoptosis in human breast cancers. Mol Cancer 2010, 9:173. 10.1186/1476-4598-9-173, 2908580, 20594292.
25. Ai L, Vo QN, Zuo C, Li L, Ling W, Suen JY, Hanna E, Brown KD, Fan CY. Ataxia-telangiectasia-mutated (ATM) gene in head and neck squamous cell carcinoma: promoter hypermethylation with clinical correlation in 100 cases. Cancer Epidemiol Biomarkers Prev 2004, 13:150-156. 10.1158/1055-9965.EPI-082-3, 14744748.
26. Bretsky P, Haiman CA, Gilad S, Yahalom J, Grossman A, Paglin S, Van Den Berg D, Kolonel LN, Skaliter R, Henderson BE. The relationship between twenty missense ATM variants and breast cancer risk: the Multiethnic Cohort. Cancer Epidemiol Biomarkers Prev 2003, 12:733-738.
27. Dork T, Bendix R, Bremer M, Rades D, Klopper K, Nicke M, Skawran B, Hector A, Yamini P, Steinmann D, Weise S, Stuhrmann M, Karstens JH. Spectrum of ATM gene mutations in a hospital-based series of unselected breast cancer patients. Cancer Res 2001, 61:7608-7615.
28. Thorstenson YR, Roxas A, Kroiss R, Jenkins MA, Yu KM, Bachrich T, Muhr D, Wayne TL, Chu G, Davis RW, Wagner TM, Oefner PJ. Contributions of ATM mutations to familial breast and ovarian cancer. Cancer Res 2003, 63:3325-3333.
29. LOVD v.2.0 - Leiden Open Variation Database - online gene-centered collection and display of DNA variations. , http://www.lovd.nl
30. Hayward JL, Carbone PP, Heusen JC, Kumaoka S, Segaloff A, Rubens RD. Assessment of response to therapy in advanced breast cancer. Br J Cancer 1977, 35:292-298. 10.1038/bjc.1977.42, 2025288, 856236.
31. Aas T, Borresen AL, Geisler S, Smith-Sorensen B, Johnsen H, Varhaug JE, Akslen LA, Lonning PE. Specific P53 mutations are associated with de novo resistance to doxorubicin in breast cancer patients. Nat Med 1996, 2:811-814. 10.1038/nm0796-811, 8673929.
32. Byrd PJ, Cooper PR, Stankovic T, Kullar HS, Watts GDJ, Robinson PJ, Taylor AMR. A gene transcribed from the bidirectional ATM promoter coding for a serine rich protein: amino acid sequence, structure and expression studies. Hum Mol Genet 1996, 5:1785-1791. 10.1093/hmg/5.11.1785, 8923007.
33. Hu H, Du L, Nagabayashi G, Seeger RC, Gatti RA. ATM is down-regulated by N-Myc-regulated microRNA-421. Proc Natl Acad Sci USA 2010, 107:1506-1511. 10.1073/pnas.0907763107, 2824372, 20080624.
34. Sorlie T, Perou CM, Fan C, Geisler S, Aas T, Nobel A, Anker G, Akslen LA, Botstein D, Borresen-Dale AL, Lonning PE. Gene expression profiles do not consistently predict the clinical treatment response in locally advanced breast cancer. Mol Cancer Ther 2006, 5:2914-2918. 10.1158/1535-7163.MCT-06-0126, 17121939.
35. Sorlie T, Perou CM, Tibshirani R, Aas T, Geisler S, Johnsen H, Hastie T, Eisen MB, van de Rijn M, Jeffrey SS, Thorsen T, Quist H, Matese JC, Brown PO, Botstein D, Eystein Lonning P, Borresen-Dale AL. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci USA 2001, 98:10869-10874. 10.1073/pnas.191367098, 58566, 11553815.
36. Penault-Llorca F, Andre F, Sagan C, Lacroix-Triki M, Denoux Y, Verriele V, Jacquemier J, Baranzelli MC, Bibeau F, Antoine M, Lagarde N, Martin AL, Asselain B, Roche H. Ki67 expression and docetaxel efficacy in patients with estrogen receptor-positive breast cancer. J Clin Oncol 2009, 27:2809-2815. 10.1200/JCO.2008.18.2808, 19380452.
37. Albain KS, Barlow WE, Shak S, Hortobagyi GN, Livingston RB, Yeh IT, Ravdin P, Bugarini R, Baehner FL, Davidson NE, Sledge GW, Winer EP, Hudis C, Ingle JN, Perez EA, Pritchard KI, Shepherd L, Gralow JR, Yoshizawa C, Allred DC, Osborne CK, Hayes DF. Prognostic and predictive value of the 21-gene recurrence score assay in postmenopausal women with node-positive, oestrogen-receptor-positive breast cancer on chemotherapy: a retrospective analysis of a randomised trial. Lancet Oncol 2010, 11:55-65. 10.1016/S1470-2045(09)70314-6, 3058239, 20005174.
38. Paik S, Tang G, Shak S, Kim C, Baker J, Kim W, Cronin M, Baehner FL, Watson D, Bryant J, Costantino JP, Geyer CE, Wickerham DL, Wolmark N. Gene expression and benefit of chemotherapy in women with node-negative, estrogen receptor-positive breast cancer. J Clin Oncol 2006, 24:3726-3734. 10.1200/JCO.2005.04.7985, 16720680.
39. Hayward JL, Carbone PP, Heuson JC, Kumaoka S, Segaloff A, Rubens RD. Assessment of response to therapy in advanced breast cancer: a project of the Programme on Clinical Oncology of the International Union Against Cancer, Geneva, Switzerland. Cancer 1977, 39:1289-1294. 10.1002/1097-0142(197703)39:3<1289::AID-CNCR2820390340>3.0.CO;2-F, 912660.
40. Chipuk JE, Kuwana T, Bouchier-Hayes L, Droin NM, Newmeyer DD, Schuler M, Green DR. Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science 2004, 303:1010-1014. 10.1126/science.1092734, 14963330.
41. Moll UM, Wolff S, Speidel D, Deppert W. Transcription-independent pro-apoptotic functions of p53. Curr Opin Cell Biol 2005, 17:631-636. 10.1016/j.ceb.2005.09.007, 16226451.
42. Nister M, Tang M, Zhang XQ, Yin C, Beeche M, Hu X, Enblad G, van Dyke T, Wahl GM. p53 must be competent for transcriptional regulation to suppress tumor formation. Oncogene 2005, 24:3563-3573. 10.1038/sj.onc.1208354, 15750633.
43. Ryan KM, Vousden KH. Characterization of structural p53 mutants which show selective defects in apoptosis but not cell cycle arrest. Mol Cell Biol 1998, 18:3692-3698. 108951, 9632751.
44. Villunger A, Michalak EM, Coultas L, Mullauer F, Bock G, Ausserlechner MJ, Adams JM, Strasser A. p53- and drug-induced apoptotic responses mediated by BH3-only proteins puma and noxa. Science 2003, 302:1036-1038. 10.1126/science.1090072, 14500851.