Cyclin E overexpression as a biomarker for combination treatment strategies in inflammatory breast cancer

Oncotarget

Volumn 8, Issue 9, 2017, Pages 14897-14911

  Alexander, Angela ^a,e   Karakas, Cansu ^a   Chen, Xian ^a   Carey, Jason P W ^a   Yi, Min ^a   Bondy, Melissa ^b   Thompson, Patricia ^c   Cheung, Kwok Leung ^d   Ellis, Ian O ^d   Gong, Yun ^a   Krishnamurthy, Savitri ^a,e   Alvarez, Ricardo H ^a,e   Ueno, Naoto T ^a,e   Hunt, Kelly K ^a   Keyomarsi, Khandan ^a  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c STONY BROOK UNIVERSITY   (United States)

^d UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^e Department of Breast Medical Oncology   (United States)

Author keywords

CDK2; Cell cycle; Cyclin E; Inflammatory breast cancer; Treatment

Indexed keywords

CARBOPLATIN; CYCLIN DEPENDENT KINASE 2; CYCLIN DEPENDENT KINASE 2 INHIBITOR; CYCLIN E; DINACICLIB; EPIRUBICIN; ETOPOSIDE; MERIOLIN 5; PACLITAXEL; UNCLASSIFIED DRUG; AMINE OXIDE; CCNE1 PROTEIN, HUMAN; CDK2 PROTEIN, HUMAN; FUSED HETEROCYCLIC RINGS; INDOLIZINE DERIVATIVE; ONCOPROTEIN; PYRIDINIUM DERIVATIVE; TUMOR MARKER;

ADULT; AGED; APOPTOSIS; ARTICLE; CANCER COMBINATION CHEMOTHERAPY; CANCER PROGNOSIS; CANCER SURVIVAL; CONTROLLED STUDY; DNA DAMAGE; DOWN REGULATION; FEMALE; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INFLAMMATORY BREAST CANCER; MAJOR CLINICAL STUDY; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; CANCER GRADING; CANCER STAGING; CELL CYCLE; CELL PROLIFERATION; FOLLOW UP; GENE EXPRESSION REGULATION; METABOLISM; MIDDLE AGED; MULTIMODALITY CANCER THERAPY; PATHOLOGY; PROGNOSIS; SURVIVAL RATE; TUMOR CELL CULTURE; TUMOR INVASION; VERY ELDERLY; YOUNG ADULT;

ADULT; AGED; AGED, 80 AND OVER; APOPTOSIS; BIOMARKERS, TUMOR; BRIDGED BICYCLO COMPOUNDS, HETEROCYCLIC; CELL CYCLE; CELL PROLIFERATION; COMBINED MODALITY THERAPY; CYCLIC N-OXIDES; CYCLIN E; CYCLIN-DEPENDENT KINASE 2; FEMALE; FOLLOW-UP STUDIES; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; INDOLIZINES; INFLAMMATORY BREAST NEOPLASMS; MIDDLE AGED; NEOPLASM GRADING; NEOPLASM INVASIVENESS; NEOPLASM STAGING; ONCOGENE PROTEINS; PROGNOSIS; PYRIDINIUM COMPOUNDS; SURVIVAL RATE; TUMOR CELLS, CULTURED; YOUNG ADULT;

EID: 85014059970     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.14689     Document Type: Article

References (44)

1. Dawood S, Ueno NT, Valero V, Woodward WA, Buchholz TA, Hortobagyi GN, Gonzalez-Angulo AM, Cristofanilli M. Differences in survival among women with stage III inflammatory and noninflammatory locally advanced breast cancer appear early: a large populationbased study. Cancer. 2011; 117:1819-1826.
2. Dawood S, Merajver SD, Viens P, Vermeulen PB, Swain SM, Buchholz TA, Dirix LY, Levine PH, Lucci A, Krishnamurthy S, Robertson FM, Woodward WA, Yang WT, et al. International expert panel on inflammatory breast cancer: consensus statement for standardized diagnosis and treatment. Ann Oncol. 2011; 22:515-523.
3. Dawood S, Lei X, Dent R, Gupta S, Sirohi B, Cortes J, Cristofanilli M, Buchholz T, Gonzalez-Angulo AM. Survival of women with inflammatory breast cancer: a large population-based study. Ann Oncol. 2014; 25:1143-1151.
4. Masuda H, Brewer TM, Liu DD, Iwamoto T, Shen Y, Hsu L, Willey JS, Gonzalez-Angulo AM, Chavez-MacGregor M, Fouad TM, Woodward WA, Reuben JM, Valero V, et al. Long-term treatment efficacy in primary inflammatory breast cancer by hormonal receptor-and HER2-defined subtypes. Ann Oncol. 2014; 25:384-391.
5. Sørlie 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, et al. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc Natl Acad Sci USA. 2001; 98:10869-10874.
6. Bertucci F, Ueno NT, Finetti P, Vermeulen P, Lucci A, Robertson FM, Marsan M, Iwamoto T, Krishnamurthy S, Masuda H, Van Dam P, Woodward WA, Cristofanilli M, et al. Gene expression profiles of inflammatory breast cancer: correlation with response to neoadjuvant chemotherapy and metastasis-free survival. Ann Oncol. 2014; 25:358-365.
7. Porter DC, Zhang N, Danes C, McGahren MJ, Harwell RM, Faruki S, Keyomarsi K. Tumor-specific proteolytic processing of cyclin E generates hyperactive lower-molecular-weight forms. Mol Cell Biol. 2001; 21:6254-6269.
8. Bagheri-Yarmand R, Nanos-Webb A, Biernacka A, Bui T, Keyomarsi K. Cyclin E deregulation impairs mitotic progression through premature activation of Cdc25C. Cancer Res. 2010; 70:5085-5095.
9. Bagheri-Yarmand R, Biernacka A, Hunt KK, Keyomarsi K. Low molecular weight cyclin E overexpression shortens mitosis, leading to chromosome missegregation and centrosome amplification. Cancer Res. 2010; 70:5074-5084.
10. Duong MT, Akli S, Wei C, Wingate HF, Liu W, Lu Y, Yi M, Mills GB, Hunt KK, Keyomarsi K. LMW-E/CDK2 deregulates acinar morphogenesis, induces tumorigenesis, and associates with the activated b-Raf-ERK1/2-mTOR pathway in breast cancer patients. PLoS Genet. 2012; 8:e1002538.
11. Duong MT, Akli S, Macalou S, Biernacka A, Debeb BG, Yi M, Hunt KK, Keyomarsi K. Hbo1 is a cyclin E/CDK2 substrate that enriches breast cancer stem-like cells. Cancer Res. 2013; 73:5556-5568.
12. Keyomarsi K, Tucker SL, Buchholz TA, Callister M, Ding Y, Hortobagyi GN, Bedrosian I, Knickerbocker C, Toyofuku W, Lowe M, Herliczek TW, Bacus SS. Cyclin E and survival in patients with breast cancer. N Engl J Med. 2002; 347:1566-1575.
13. Delk NA, Hunt KK, Keyomarsi K. Altered subcellular localization of tumor-specific cyclin E isoforms affects cyclin-dependent kinase 2 complex formation and proteasomal regulation. Cancer Res. 2009; 69:2817-2825.
14. Akli S, Van Pelt CS, Bui T, Meijer L, Keyomarsi K. Cdk2 is required for breast cancer mediated by the low-molecularweight isoform of cyclin E. Cancer Res. 2011; 71:3377-3386.
15. Hunt KK, Karakas C, Ha MJ, Biernacka A, Yi M, Sahin A, Adjapong O, Hortobogyi GN, Bondy ML, Thompson PA, Cheung KL, Ellis IO, Bacus S, et al. Cytoplasmic Cyclin E Predicts Recurrence in Patients with Breast Cancer. Clin Cancer Res. 2016.
16. Karakas C, Biernacka A, Bui T, Sahin AA, Yi M, Akli S, Schafer J, Alexander A, Adjapong O, Hunt KK, Keyomarsi K. Cytoplasmic Cyclin E, Phospho-Cyclin-Dependent Kinase 2 Are Biomarkers of Aggressive Breast Cancer. Am J Pathol. 2016; 186:1900-1912.
17. Lim JS, Turner NC, Yap TA. CDK4/6 Inhibitors: Promising Opportunities beyond Breast Cancer. Cancer Discov. 2016; 6:697-699.
18. O'Leary B, Finn RS, Turner NC. Treating cancer with selective CDK4/6 inhibitors. Nat Rev Clin Oncol. 2016; 13:417-430.
19. Bruyere C, Meijer L. Targeting cyclin-dependent kinases in anti-neoplastic therapy. Current opinion in cell biology. 2013; 25:772-779.
20. Echalier A, Bettayeb K, Ferandin Y, Lozach O, Clement M, Valette A, Liger F, Marquet B, Morris JC, Endicott JA, Joseph B, Meijer L. Meriolins (3-(pyrimidin-4-yl)-7-azaindoles): synthesis, kinase inhibitory activity, cellular effects, and structure of a CDK2/cyclin A/meriolin complex. Journal of medicinal chemistry. 2008; 51:737-751.
21. Lehmann BD, Bauer JA, Chen X, Sanders ME, Chakravarthy AB, Shyr Y, Pietenpol JA. Identification of human triple-negative breast cancer subtypes and preclinical models for selection of targeted therapies. J Clin Invest. 2011; 121:2750-2767.
22. Nanos-Webb A, Jabbour NA, Multani AS, Wingate H, Oumata N, Galons H, Joseph B, Meijer L, Hunt KK, Keyomarsi K. Targeting low molecular weight cyclin E (LMW-E) in breast cancer. Breast Cancer Res Treat. 2012; 132:575-588.
23. Chou TC, Talalay P. Analysis of combined drug effects: a new look at a very old problem. Trends in Pharmacological Sciences. 1983; 4:450-454.
24. Tenzer A, Pruschy M. Potentiation of DNA-damageinduced cytotoxicity by G2 checkpoint abrogators. Curr Med Chem Anticancer Agents. 2003; 3:35-46.
25. O'Connor MJ, Martin NM, Smith GC. Targeted cancer therapies based on the inhibition of DNA strand break repair. Oncogene. 2007; 26:7816-7824.
26. Batey MA, Zhao Y, Kyle S, Richardson C, Slade A, Martin NM, Lau A, Newell DR, Curtin NJ. Preclinical evaluation of a novel ATM inhibitor, KU59403, in vitro and in vivo in p53 functional and dysfunctional models of human cancer. Mol Cancer Ther. 2013; 12:959-967.
27. Biddlestone-Thorpe L, Sajjad M, Rosenberg E, Beckta JM, Valerie NC, Tokarz M, Adams BR, Wagner AF, Khalil A, Gilfor D, Golding SE, Deb S, Temesi DG, et al. ATM kinase inhibition preferentially sensitizes p53-mutant glioma to ionizing radiation. Clin Cancer Res. 2013; 19:3189-3200.
28. Kwok M, Davies N, Agathanggelou A, Smith E, Oldreive C, Petermann E, Stewart G, Brown J, Lau A, Pratt G, Parry H, Taylor M, Moss P, et al. ATR inhibition induces synthetic lethality and overcomes chemoresistance in TP53-or ATMdefective chronic lymphocytic leukemia cells. Blood. 2016; 127:582-595.
29. Min J, Guo K, Suryadevara PK, Zhu F, Holbrook G, Chen Y, Feau C, Young BM, Lemoff A, Connelly MC, Kastan MB, Guy RK. Optimization of a Novel Series of Ataxia-Telangiectasia Mutated Kinase Inhibitors as Potential Radiosensitizing Agents. J Med Chem. 2016; 59:559-577.
30. Vendetti FP, Lau A, Schamus S, Conrads TP, O'Connor MJ, Bakkenist CJ. The orally active and bioavailable ATR kinase inhibitor AZD6738 potentiates the anti-tumor effects of cisplatin to resolve ATM-deficient non-small cell lung cancer in vivo. Oncotarget. 2015; 6:44289-44305. doi: 10.18632/oncotarget.6247.
31. Alagpulinsa DA, Ayyadevara S, Yaccoby S, Shmookler Reis RJ. A Cyclin-Dependent Kinase Inhibitor, Dinaciclib, Impairs Homologous Recombination and Sensitizes Multiple Myeloma Cells to PARP Inhibition. Mol Cancer Ther. 2016; 15:241-250.
32. Gregory GP, Hogg SJ, Kats LM, Vidacs E, Baker AJ, Gilan O, Lefebure M, Martin BP, Dawson MA, Johnstone RW, Shortt J. CDK9 inhibition by dinaciclib potently suppresses Mcl-1 to induce durable apoptotic responses in aggressive MYC-driven B-cell lymphoma in vivo. Leukemia. 2015; 29:1437-1441.
33. Li JP, Yang YX, Liu QL, Pan ST, He ZX, Zhang X, Yang T, Chen XW, Wang D, Qiu JX, Zhou SF. The investigational Aurora kinase A inhibitor alisertib (MLN8237) induces cell cycle G2/M arrest, apoptosis, and autophagy via p38 MAPK, Akt/mTOR signaling pathways in human breast cancer cells. Drug Des Devel Ther. 2015; 9:1627-1652.
34. Hu S, Danilov AV, Godek K, Orr B, Tafe LJ, Rodriguez-Canales J, Behrens C, Mino B, Moran CA, Memoli VA, Mustachio LM, Galimberti F, Ravi S, et al. CDK2 Inhibition Causes Anaphase Catastrophe in Lung Cancer through the Centrosomal Protein CP110. Cancer Res. 2015; 75:2029-2038.
35. Opyrchal M, Salisbury JL, Iankov I, Goetz MP, McCubrey J, Gambino MW, Malatino L, Puccia G, Ingle JN, Galanis E, D'Assoro AB. Inhibition of Cdk2 kinase activity selectively targets the CD44+/CD24-/Low stem-like subpopulation and restores chemosensitivity of SUM149PT triple-negative breast cancer cells. Int J Oncol. 2014; 45:1193-1199.
36. Nemunaitis JJ, Small KA, Kirschmeier P, Zhang D, Zhu Y, Jou YM, Statkevich P, Yao SL, Bannerji R. A first-in-human, phase 1, dose-escalation study of dinaciclib, a novel cyclindependent kinase inhibitor, administered weekly in subjects with advanced malignancies. J Transl Med. 2013; 11:259.
37. Mitri Z, Karakas C, Wei C, Briones B, Simmons H, Ibrahim N, Alvarez R, Murray JL, Keyomarsi K, Moulder S. A phase 1 study with dose expansion of the CDK inhibitor dinaciclib (SCH 727965) in combination with epirubicin in patients with metastatic triple negative breast cancer. Invest New Drugs. 2015; 33:890-894.
38. Mita MM, Joy AA, Mita A, Sankhala K, Jou YM, Zhang D, Statkevich P, Zhu Y, Yao SL, Small K, Bannerji R, Shapiro CL. Randomized phase II trial of the cyclin-dependent kinase inhibitor dinaciclib (MK-7965) versus capecitabine in patients with advanced breast cancer. Clin Breast Cancer. 2014; 14:169-176.
39. Barry SP, Townsend PA, Knight RA, Scarabelli TM, Latchman DS, Stephanou A. STAT3 modulates the DNA damage response pathway. Int J Exp Pathol. 2010; 91:506-514.
40. Jhaveri K, Teplinsky E, Silvera D, Valeta-Magara A, Arju R, Giashuddin S, Sarfraz Y, Alexander M, Darvishian F, Levine PH, Hashmi S, Zolfaghari L, Hoffman HJ, et al. Hyperactivated mTOR, JAK2/STAT3 Pathways: Molecular Drivers and Potential Therapeutic Targets of Inflammatory and Invasive Ductal Breast Cancers After Neoadjuvant Chemotherapy. Clin Breast Cancer. 2016; 16:113-122.e111.
41. Courapied S, Sellier H, de Carné Trécesson S, Vigneron A, Bernard AC, Gamelin E, Barré B, Coqueret O. The cdk5 kinase regulates the STAT3 transcription factor to prevent DNA damage upon topoisomerase I inhibition. J Biol Chem. 2010; 285:26765-26778.
42. Tian B, Yang Q, Mao Z. Phosphorylation of ATM by Cdk5 mediates DNA damage signalling and regulates neuronal death. Nat Cell Biol. 2009; 11:211-218.
43. Hudis CA, Barlow WE, Costantino JP, Gray RJ, Pritchard KI, Chapman JA, Sparano JA, Hunsberger S, Enos RA, Gelber RD, Zujewski JA. Proposal for standardized definitions for efficacy end points in adjuvant breast cancer trials: the STEEP system. J Clin Oncol. 2007; 25:2127-2132.
44. Lucenay KS, Doostan I, Karakas C, Bui T, Ding Z, Mills GB, Hunt KK, Keyomarsi K. Cyclin E associates with the lipogenic enzyme ATP-citrate lyase to enable malignant growth of breast cancer cells. Cancer Res. 2016.