Extreme chromosomal instability forecasts improved outcome in ER-negative breast cancer: A prospective validation cohort study from the TACT trial

Annals of Oncology

Volumn 26, Issue 7, 2015, Pages 1340-1346

  Jamal Hanjani, M ^a   A'Hern, R ^b   Birkbak, N J ^a,c   Gorman, P ^a   Gronroos E ^c   Ngang, S ^a   Nicola, P ^a   Rahman, L ^a   Thanopoulou, E ^c   Kelly, G ^c   Ellis, P ^d   Barrett Lee, P ^e   Johnston, S R D ^f   Bliss, J ^b   Roylance, Rebecca ^g   Swanton, Charles ^a,c  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^c THE FRANCIS CRICK INSTITUTE   (United Kingdom)

^d GUY'S AND ST THOMAS' NHS FOUNDATION TRUST   (United Kingdom)

^e Velindre NHS Trust   (United Kingdom)

^f INSTITUTE OF CANCER RESEARCH   (United Kingdom)

^g QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

Breast cancer; Chromosomal instability; Intratumour heterogeneity; Modal centromere deviation; Prognostic biomarker

Indexed keywords

ADULT; AGED; ARTICLE; BREAST CANCER; CANCER PROGNOSIS; CANCER RISK; CANCER SURVIVAL; CELL COUNT; CENTROMERE; CHROMOSOMAL INSTABILITY; CHROMOSOME 15; CHROMOSOME 2; COHORT ANALYSIS; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE FREE SURVIVAL; ESTROGEN RECEPTOR NEGATIVE BREAST CANCER; FLUORESCENCE IN SITU HYBRIDIZATION; FOLLOW UP; HUMAN; MAJOR CLINICAL STUDY; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROSPECTIVE STUDY; VALIDATION PROCESS; BREAST NEOPLASMS; CANCER GRADING; CANCER STAGING; CLINICAL TRIAL; ENZYME IMMUNOASSAY; FEMALE; GENETICS; METABOLISM; MIDDLE AGED; MORTALITY; MULTICENTER STUDY; PATHOLOGY; PHASE 3 CLINICAL TRIAL; PROGNOSIS; RANDOMIZED CONTROLLED TRIAL; SURVIVAL RATE; VERY ELDERLY; YOUNG ADULT;

ANTHRACYCLINE; ANTINEOPLASTIC AGENT; EPIDERMAL GROWTH FACTOR RECEPTOR 2; ERBB2 PROTEIN, HUMAN; ESTROGEN RECEPTOR; PROGESTERONE RECEPTOR; TAXOID; TUMOR MARKER;

ADULT; AGED; AGED, 80 AND OVER; ANTHRACYCLINES; ANTINEOPLASTIC COMBINED CHEMOTHERAPY PROTOCOLS; BIOMARKERS, TUMOR; BREAST NEOPLASMS; CHROMOSOMAL INSTABILITY; FEMALE; FOLLOW-UP STUDIES; HUMANS; IMMUNOENZYME TECHNIQUES; IN SITU HYBRIDIZATION, FLUORESCENCE; MIDDLE AGED; NEOPLASM GRADING; NEOPLASM STAGING; PROGNOSIS; PROSPECTIVE STUDIES; RECEPTOR, ERBB-2; RECEPTORS, ESTROGEN; RECEPTORS, PROGESTERONE; SURVIVAL RATE; TAXOIDS; YOUNG ADULT;

EID: 84946730024     PISSN: 09237534     EISSN: 15698041     Source Type: Journal    
DOI: 10.1093/annonc/mdv178     Document Type: Article

References (53)

1. Gisselsson D, Pettersson L, Hoglund M et al. Chromosomal breakage-fusionbridge events cause genetic intratumor heterogeneity. Proc Natl Acad Sci USA 2000; 97: 5357-5362.
2. McGranahan N, Burrell RA, Endesfelder D et al. Cancer chromosomal instability:therapeutic and diagnostic challenges. 'Exploring aneuploidy: the significance of chromosomal imbalance' review series. EMBO Rep 2012; 13: 528-538.
3. Stewenius Y, Gorunova L, Jonson T et al. Structural and numerical chromosome changes in colon cancer develop through telomere-mediated anaphase bridges, not through mitotic multipolarity. Proc Natl Acad Sci USA 2005; 102: 5541-5546.
4. Perera SA, Maser RS, Xia H et al. Telomere dysfunction promotes genome instability and metastatic potential in a K-ras p53 mouse model of lung cancer. Carcinogenesis 2008; 29: 747-753.
5. Bailey SM, Murnane JP. Telomeres, chromosome instability and cancer. Nucleic Acids Res 2006; 34: 2408-2417.
6. Gisselsson D, Jonson T, Petersen A et al. Telomere dysfunction triggers extensive DNA fragmentation and evolution of complex chromosome abnormalities in human malignant tumors. Proc Natl Acad Sci USA 2001; 98: 12683-12688.
7. Burrell RA, McClelland SE, Endesfelder D et al. Replication stress links structural and numerical cancer chromosomal instability. Nature 2013; 494: 492-496.
8. Dereli-Oz A, Versini G, Halazonetis TD. Studies of genomic copy number changes in human cancers reveal signatures of DNA replication stress. Mol Oncol 2011; 5:308-314.
9. Grabsch H, Takeno S, Parsons WJ et al. Overexpression of the mitotic checkpoint genes BUB1, BUBR1, and BUB3 in gastric cancer--association with tumour cell proliferation. J Pathol 2003; 200: 16-22.
10. Wang X, Jin DY, Ng RW et al. Significance of MAD2 expression to mitotic checkpoint control in ovarian cancer cells. Cancer Res 2002; 62: 1662-1668.
11. Gregan J, Polakova S, Zhang L et al. Merotelic kinetochore attachment: causes and effects. Trends Cell Biol 2011; 21: 374-381.
12. Ganem NJ, Godinho SA, Pellman D. A mechanism linking extra centrosomes to chromosomal instability. Nature 2009; 460: 278-282.
13. Barber TD, McManus K, Yuen KW et al. Chromatid cohesion defects may underlie chromosome instability in human colorectal cancers. Proc Natl Acad Sci USA 2008; 105: 3443-3448.
14. Meyer R, Fofanov V, Panigrahi A et al. Overexpression and mislocalization of the chromosomal segregation protein separase in multiple human cancers. Clin Cancer Res 2009; 15: 2703-2710.
15. Zhang N, Ge G, Meyer R et al. Overexpression of Separase induces aneuploidy and mammary tumorigenesis. Proc Natl Acad Sci USA 2008; 105: 13033-13038.
16. Gisselsson D, Jin Y, Lindgren D et al. Generation of trisomies in cancer cells by multipolar mitosis and incomplete cytokinesis. Proc Natl Acad Sci USA 2010; 107:20489-20493.
17. Janssen A, van der Burg M, Szuhai K et al. Chromosome segregation errors as a cause of DNA damage and structural chromosome aberrations. Science 2011; 333: 1895-1898.
18. Crasta K, Ganem NJ, Dagher R et al. DNA breaks and chromosome pulverization from errors in mitosis. Nature 2012; 482: 53-58.
19. Carter SL, Eklund AC, Kohane IS et al. A signature of chromosomal instability inferred from gene expression profiles predicts clinical outcome in multiple human cancers. Nat Genet 2006; 38: 1043-1048.
20. Walther A, Houlston R, Tomlinson I. Association between chromosomal instability and prognosis in colorectal cancer: a meta-analysis. Gut 2008; 57: 941-950.
21. Habermann JK, Doering J, Hautaniemi S et al. The gene expression signature of genomic instability in breast cancer is an independent predictor of clinical outcome. Int J Cancer 2009; 124: 1552-1564.
22. Kronenwett U, Ploner A, Zetterberg A et al. Genomic instability and prognosis in breast carcinomas. Cancer Epidemiol Biomarkers Prev 2006; 15: 1630-1635.
23. Gerlinger M, Swanton C. How Darwinian models inform therapeutic failure initiated by clonal heterogeneity in cancer medicine. Br J Cancer 2010; 103: 1139-1143.
24. Swanton C, Nicke B, Schuett M et al. Chromosomal instability determines taxane response. Proc Natl Acad Sci USA 2009; 106: 8671-8676.
25. Duesberg P, Stindl R, Hehlmann R. Explaining the high mutation rates of cancer cells to drug and multidrug resistance by chromosome reassortments that are catalysed by aneuploidy. Proc Natl Acad Sci USA 2000; 97: 14295-14300.
26. Li R, Hehlman R, Sachs R, Duesberg P. Chromosomal alterations cause the high rates and wide ranges of drug resistance in cancer cells. Cancer Genet Cytogenet 2005; 163: 44-56.
27. Takami S, Kawasome C, Kinoshita M et al. Chromosomal instability detected by fluorescence in situ hybridization in Japanese breast cancer patients. Clin Chim Acta 2001; 308: 127-131.
28. Jonkers YM, Claessen SM, Perren A et al. Chromosomal instability predicts metastatic disease in patients with insulinomas. Endocr Relat Cancer 2005; 12:435-447.
29. Endesfelder D, Burrell RA, Kanu N et al. Chromosomal instability selects gene copy-number variants encoding core regulators of proliferation in ER+ breast cancer. Cancer Res 2014; 74: 4853-4863.
30. Torres EM, Sokolsky T, Tucker CM et al. Effects of aneuploidy on cellular physiology and cell division in haploid yeast. Science 2007; 317: 916-924.
31. Williams BR, Prabhu VR, Hunter KE et al. Aneuploidy affects proliferation and spontaneous immortalization in mammalian cells. Science 2008; 322: 703-709.
32. Loeb LA. A mutator phenotype in cancer. Cancer Res 2001; 61: 3230-3239.
33. Komarova NL, Wodarz D. The optimal rate of chromosome loss for the inactivation of tumor suppressor genes in cancer. Proc Natl Acad Sci USA 2004; 101:7017-7021.
34. Pusztai L, Ayers M, Stec J et al. Gene expression profiles obtained from fineneedle aspirations of breast cancer reliably identify routine prognostic markers and reveal large-scale molecular differences between estrogen-negative and estrogenpositive tumors. Clin Cancer Res 2003; 9: 2406-2415.
35. Birkbak NJ, Eklund AC, Li Q et al. Paradoxical relationship between chromosomal instability and survival outcome in cancer. Cancer Res 2011; 71: 3447-3452.
36. Roylance R, Endesfelder D, Gorman P et al. Relationship of extreme chromosomal instability with long-term survival in a retrospective analysis of primary breast cancer. Cancer Epidemiol Biomarkers Prev 2011; 20: 2183-2194.
37. Maley CC, Galipeau PC, Finley JC et al. Genetic clonal diversity predicts progression to esophageal adenocarcinoma. Nat Genet 2006; 38: 468-473.
38. Ellis P, Barrett-Lee P, Johnson L et al. Sequential docetaxel as adjuvant chemotherapy for early breast cancer (TACT): an open-label, phase III, randomised controlled trial. Lancet 2009; 373: 1681-1692.
39. Endesfelder D, McGranahan N, Birkbak NJ et al. A breast cancer meta-analysis of two expression measures of chromosomal instability reveals a relationship with younger age at diagnosis and high risk histopathological variables. Oncotarget 2011; 2: 529-537.
40. Bakhoum SF, Danilova OV, Kaur P et al. Chromosomal instability substantiates poor prognosis in patients with diffuse large B-cell lymphoma. Clin Cancer Res 2011; 17: 7704-7711.
41. Sheffer M, Bacolod MD, Zuk O et al. Association of survival and disease progression with chromosomal instability: a genomic exploration of colorectal cancer. Proc Natl Acad Sci USA 2009; 106: 7131-7136.
42. M'Kacher R, Andreoletti L, Flamant S et al. JC human polyomavirus is associated to chromosomal instability in peripheral blood lymphocytes of Hodgkin's lymphoma patients and poor clinical outcome. Ann Oncol 2010; 21: 826-832.
43. Sotillo R, Schvartzman JM, Socci ND, Benezra R. Mad2-induced chromosome instability leads to lung tumour relapse after oncogene withdrawal. Nature 2010; 464: 436-440.
44. Pavelka N, Rancati G, Li R. Dr Jekyll and Mr Hyde: role of aneuploidy in cellular adaptation and cancer. Curr Opin Cell Biol 2010; 22: 1-7.
45. Kops GJ, Foltz DR, Cleveland DW. Lethality to human cancer cells through massive chromosome loss by inhibition of the mitotic checkpoint. Proc Natl Acad Sci USA 2004; 101: 8699-8704.
46. Schmidt M, Budirahardja Y, Klompmaker R, Medema RH. Ablation of the spindle assembly checkpoint by a compound targeting Mps1. EMBO Rep 2005; 6: 866-872.
47. Janssen A, Kops GJ, Medema RH. Elevating the frequency of chromosome missegregation as a strategy to kill tumor cells. Proc Natl Acad Sci USA 2009; 106:19108-19113.
48. Baumbusch LO, Helland A, Wang Y et al. High levels of genomic aberrations in serous ovarian cancers are associated with better survival. PLoS One 2013; 8:e54356.
49. Roschke AV, Tonon G, Gehlhaus KS et al. Karyotypic complexity of the NCI-60 drug-screening panel. Cancer Res 2003; 63: 8634-8647.
50. Roschke AV, Lababidi S, Tonon G et al. Karyotypic "state" as a potential determinant for anticancer drug discovery. Proc Natl Acad Sci USA 2005; 102: 2964-2969.
51. Roschke AV, Kirsch IR. Targeting cancer cells by exploiting karyotypic complexity and chromosomal instability. Cell Cycle 2005; 4: 679-682.
52. Kim C, Paik S. Gene-expression-based prognostic assays for breast cancer. Nat Rev Clin Oncol 2010; 7: 340-347.
53. Pusztai L. Gene expression profiling of breast cancer. Breast Cancer Res 2009; 11(Suppl 3):S11.