Expression of CDK7, cyclin H, and MAT1 is elevated in breast cancer and is prognostic in estrogen receptor-positive breast cancer

Clinical Cancer Research

Volumn 22, Issue 23, 2016, Pages 5929-5938

  Patel, Hetal ^a   Abduljabbar, Rezvan ^b   Lai, Chun Fui ^a   Periyasamy, Manikandan ^a   Harrod, Alison ^a   Gemma, Carolina ^a   Steel, Jennifer H ^a   Patel, Naina ^a   Busonero, Claudia ^a   Jerjees, Dena ^b   Remenyi, Judit ^c   Smith, Sally ^d   Gomm, Jennifer J ^d   Magnani, Luca ^a   Gyorffy, Balázs ^e,f   Jones, Louise J ^d   Fuller Pace, Frances ^c   Shousha, Sami ^g   Buluwela, Laki ^a   Rakha, Emad A ^b   Ellis, Ian O ^b   Coombes, R Charles ^a   Ali, Simak ^a   more..

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^c UNIVERSITY OF DUNDEE   (United Kingdom)

^d QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^e INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^f SEMMELWEIS UNIVERSITY   (Hungary)

^g CHARING CROSS HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN RECEPTOR; CYCLIN DEPENDENT KINASE 7; CYCLIN DEPENDENT KINASE ACTIVATING KINASE; CYCLIN H; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ESTROGEN RECEPTOR; HEPATOCYTE NUCLEAR FACTOR 3ALPHA; MAT1 PROTEIN; MESSENGER RNA; PROGESTERONE RECEPTOR; SERINE; TRANSCRIPTION FACTOR GATA 3; UNCLASSIFIED DRUG; CARRIER PROTEIN; CCNH PROTEIN, HUMAN; CYCLIN DEPENDENT KINASE; CYCLIN-DEPENDENT KINASE-ACTIVATING KINASE; MNAT1 PROTEIN, HUMAN;

ADULT; ARTICLE; BREAST; BREAST CANCER; CANCER GRADING; CANCER PROGNOSIS; CANCER SURVIVAL; CLINICAL FEATURE; CONTROLLED STUDY; CORRELATION ANALYSIS; DISEASE ASSOCIATION; ESTROGEN RECEPTOR POSITIVE BREAST CANCER; FEMALE; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MAJOR CLINICAL STUDY; MIDDLE AGED; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TUMOR VOLUME; BREAST TUMOR; GENE EXPRESSION; GENETICS; PATHOLOGY; PHOSPHORYLATION; PROGNOSIS; SIGNAL TRANSDUCTION;

ADULT; BREAST NEOPLASMS; CARRIER PROTEINS; CYCLIN H; CYCLIN-DEPENDENT KINASES; FEMALE; GENE EXPRESSION; HUMANS; MIDDLE AGED; PHOSPHORYLATION; PROGNOSIS; RECEPTORS, ESTROGEN; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC;

EID: 85006288789     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-15-1104     Document Type: Article

References (45)

1. Malumbres M, Barbacid M. Mammalian cyclin-dependent kinases. Trends Biochem Sci 2005;30:630-41.
2. Fisher RP. Secrets of a double agent: CDK7 in cell-cycle control and transcription. J Cell Sci 2005;118:5171-80.
3. Lu H, Fisher RP, Bailey P, Levine AJ. The CDK7-cycH-p36 complex of transcription factor IIH phosphorylates p53, enhancing its sequence-specific DNA binding activity in vitro. Mol Cell Biol 1997;17:5923-34.
4. Rochette-Egly C, Adam S, Rossignol M, Egly JM, Chambon P. Stimulation of RAR alpha activation function AF-1 through binding to the general transcription factor TFIIH and phosphorylation by CDK7. Cell 1997; 90:97-107.
5. Bastien J, Adam-Stitah S, Riedl T, Egly JM, Chambon P, Rochette-Egly C. TFIIH interacts with the retinoic acid receptor gamma and phosphorylates its AF-1-activating domain through cdk7. J Biol Chem 2000; 275:21896-904.
6. Lee DK, Duan HO, Chang C. From androgen receptor to the general transcription factor TFIIH. Identification of cdk activating kinase (CAK) as an androgen receptor NH(2)-terminal associated coactivator. J Biol Chem 2000;275:9308-13.
7. Chymkowitch P, Le May N, Charneau P, Compe E, Egly JM. The phosphorylation of the androgen receptor by TFIIH directs the ubiquitin/proteasome process. EMBO J 2011;30:468-79.
8. Chen D, Riedl T, Washbrook E, Pace PE, Coombes RC, Egly JM, et al. Activation of estrogen receptor alpha by S118 phosphorylation involves a ligand-dependent interaction with TFIIH and participation of CDK7. Mol Cell 2000;6:127-37.
9. Malumbres M, Barbacid M. To cycle or not to cycle: A critical decision in cancer. Nat Rev Cancer 2001;1:222-31.
10. Lolli G, Johnson LN. CAK-Cyclin-dependent Activating Kinase: A key kinase in cell cycle control and a target for drugs? Cell Cycle 2005;4: 572-7.
11. Peyressatre M, Prevel C, Pellerano M, Morris MC. Targeting cyclin-dependent kinases in human cancers: From small molecules to Peptide inhibitors. Cancers (Basel) 2015;7:179-237.
12. Malumbres M, Barbacid M. Cell cycle, CDKs and cancer: A changing paradigm. Nat Rev Cancer 2009;9:153-66.
13. Merrick KA, Fisher RP. Why minimal is not optimal: Driving the mammalian cell cycle-and drug discovery-with a physiologic CDK control network. Cell Cycle 2012;11:2600-5.
14. DeMichele A, Clark AS, Tan KS, Heitjan DF, Gramlich K, Gallagher M, et al. CDK 4/6 inhibitor palbociclib (PD0332991) in Rb+ advanced breast cancer: phase II activity, safety, and predictive biomarker assessment. Clin Cancer Res 2015;21:995-1001.
15. Shapiro GI. Cyclin-dependent kinase pathways as targets for cancer treatment.J Clin Oncol 2006;24:1770-83.
16. Finn RS, Crown JP, Lang I, Boer K, Bondarenko IM, Kulyk SO, et al.The cyclin-dependent kinase 4/6 inhibitor palbociclib in combination with letrozole versus letrozole alone as first-line treatment of oestrogen receptor-positive, HER2-negative, advanced breast cancer (PALOMA-1/TRIO-18): A randomised phase 2 study. Lancet Oncol 2015;16:25-35.
17. Ali S, Heathcote DA, Kroll SH, Jogalekar AS, Scheiper B, Patel H, et al. The development of a selective cyclin-dependent kinase inhibitor that shows antitumor activity. Cancer Res 2009;69:6208-15.
18. Kwiatkowski N, Zhang T, Rahl PB, Abraham BJ, Reddy J, Ficarro SB, et al.Targeting transcription regulation in cancer with a covalent CDK7 inhibitor. Nature 2014;511:616-20.
19. Christensen CL, Kwiatkowski N, Abraham BJ, Carretero J, Al-Shahrour F, Zhang T, et al. Targeting transcriptional addictions in small cell lung cancer with a covalent CDK7 inhibitor. Cancer Cell 2014;26: 909-22.
20. Chipumuro E, Marco E, Christensen CL, Kwiatkowski N, Zhang T, Hatheway CM, et al. CDK7 inhibition suppresses super-enhancerlinked oncogenic transcription in MYCN-driven cancer. Cell 2014; 159:1126-39.
21. Ganuza M, Saiz-Ladera C, Canamero M, Gomez G, Schneider R, Blasco MA, et al. Genetic inactivation of Cdk7 leads to cell cycle arrest and induces premature aging due to adult stem cell exhaustion. EMBO J 2012;31:2498-510.
22. Purdie CA, Baker L, Ashfield A, Chatterjee S, Jordan LB, Quinlan P, et al. Increased mortality in HER2 positive, oestrogen receptor positive invasive breast cancer: A population-based study. Br J Cancer 2010; 103:475-81.
23. Abd El-Rehim DM, Ball G, Pinder SE, Rakha E, Paish C, Robertson JF, et al.High-throughput protein expression analysis using tissuemicroarray technology of a large well-characterised series identifies biologically distinct classes of breast cancer confirming recent cDNA expression analyses. Int J Cancer 2005;116:340-50.
24. Jerjees DA, Alabdullah M, Green AR, Alshareeda A, Macmillan RD, Ellis IO, et al. Prognostic and biological significance of proliferation and HER2 expression in the luminal class of breast cancer. Breast Cancer Res Treat 2014;145:317-30.
25. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(T)(-Delta Delta C) method.Methods 2001;25:402-8.
26. Rhodes DR, Kalyana-Sundaram S, Mahavisno V, Barrette TR, Ghosh D, Chinnaiyan AM. Mining for regulatory programs in the cancer transcriptome. Nat Genet 2005;37:579-83.
27. Sarwar N, Kim JS, Jiang J, Peston D, Sinnett HD, Madden P, et al. Phosphorylation of ERalpha at serine 118 in primary breast cancer and in tamoxifen-resistant tumours is indicative of a complex role for ERalpha phosphorylation in breast cancer progression. Endocr Relat Cancer 2006;13:851-61.
28. Camp RL, Dolled-Filhart M, Rimm DL. X-tile: A new bio-informatics tool for biomarker assessment and outcome-based cut-point optimization.Clin Cancer Res 2004;10:7252-9.
29. Abduljabbar R, Negm OH, Lai CF, Jerjees DA, Al-Kaabi M, Hamed MR, et al. Clinical and biological significance of glucocorticoid receptor (GR) expression in breast cancer. Breast Cancer Res Treat 2015; 150:335-46.
30. Habashy HO, Powe DG, Rakha EA, Ball G, Paish C, Gee J, et al. Forkheadbox A1 (FOXA1) expression in breast cancer and its prognostic significance. Eur J Cancer 2008;44:1541-51.
31. Lai CF, Flach KD, Alexi X, Fox SP, Ottaviani S, Thiruchelvam PT, et al. Coregulated gene expression by oestrogen receptor alpha and liver receptor homolog-1 is a feature of the oestrogen response in breast cancer cells.Nucleic Acids Res 2013;41:10228-40.
32. Gastl G, Spizzo G, Obrist P, Dunser M, Mikuz G. Ep-CAM overexpression in breast cancer as a predictor of survival. Lancet 2000; 356:1981-2.
33. Curtis C, Shah SP, Chin SF, TurashviliG, Rueda OM, Dunning MJ, et al. The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups. Nature 2012;486:346-52.
34. Sano M, Izumi Y, Helenius K, Asakura M, Rossi DJ, Xie M, et al. Menage-atrois 1 is critical for the transcriptional function of PPARgamma coactivator 1. Cell Metab 2007;5:129-42.
35. Lin ML, Patel H, Remenyi J, Banerji CR, Lai CF, Periyasamy M, et al. Expression profiling of nuclear receptors in breast cancer identifies TLX as a mediator of growth and invasion in triple-negative breast cancer. Oncotarget 2015;6:21685-703.
36. Peters AA, Buchanan G, Ricciardelli C, Bianco-Miotto T, Centenera MM, Harris JM, et al. Androgen receptor inhibits estrogen receptoralpha activity and is prognostic in breast cancer. Cancer Res 2009;69: 6131-40.
37. Lacroix M, Leclercq G. About GATA3, HNF3A, and XBP1, three genes coexpressed with the oestrogen receptor-alpha gene (ESR1) in breast cancer. Mol Cell Endocrinol 2004;219:1-7.
38. Ross-Innes CS, Stark R, Teschendorff AE, Holmes KA, Ali HR, Dunning MJ, et al. Differential oestrogen receptor binding is associated with clinical outcome in breast cancer. Nature 2012;481:389-93.
39. Chen D, Washbrook E, Sarwar N, Bates GJ, Pace PE, Thirunuvakkarasu V, et al. Phosphorylation of human estrogen receptor alpha at serine 118 by two distinct signal transduction pathways revealed by phosphorylation-specific antisera. Oncogene 2002;21: 4921-31.
40. Murphy LC, Seekallu SV, Watson PH. Clinical significance of estrogen receptor phosphorylation. Endocr Relat Cancer 2011;18: R1-14.
41. Bartkova J, Zemanova M, Bartek J. Expression of CDK7/CAK in normal and tumor cells of diverse histogenesis, cell-cycle position and differentiation. Int J Cancer 1996;66:732-7.
42. Zhang J, Yang X, Wang Y, Shi H, Guan C, Yao L, et al. Low expression of cyclin H and cyclin-dependent kinase 7 can decrease the proliferation of human esophageal squamous cell carcinoma. Dig Dis Sci 2013;58: 2028-37.
43. Rajbhandari P, Schalper KA, Solodin NM, Ellison-Zelski SJ, Ping Lu K, Rimm DL, et al. Pin1 modulates ERalpha levels in breast cancer through inhibition of phosphorylation-dependent ubiquitination and degradation.Oncogene 2014;33:1438-47.
44. Valley CC, Metivier R, Solodin NM, Fowler AM,Mashek MT, Hill L, et al. Differential regulation of estrogen-inducible proteolysis and transcription by the estrogen receptor alpha N terminus. Mol Cell Biol 2005; 25:5417-28.
45. Eeckhoute J, Keeton EK, Lupien M, Krum SA, Carroll JS, BrownM. Positive cross-regulatory loop ties GATA-3 to estrogen receptor alpha expression in breast cancer. Cancer Res 2007;67:6477-83.