Massively parallel sequencing of phyllodes tumours of the breast reveals actionable mutations, and TERT promoter hotspot mutations and TERT gene amplification as likely drivers of progression

Journal of Pathology

Volumn 238, Issue 4, 2016, Pages 508-518

  Piscuoglio, Salvatore ^a   Ng, Charlotte K Y ^a   Murray, Melissa ^a   Burke, Kathleen A ^a   Edelweiss, Marcia ^a   Geyer, Felipe C ^a,b   MacEdo, Gabriel S ^a   Inagaki, Akiko ^a   Papanastasiou, Anastasios D ^a,c   Martelotto, Luciano G ^a   Marchio, Caterina ^a,d   Lim, Raymond S ^a   Ioris, Rafael A ^a   Nahar, Pooja K ^a   Bruijn, Ino De ^a   Smyth, Lillian ^a   Akram, Muzaffar ^a   Ross, Dara ^a   Petrini, John H ^a   Norton, Larry ^a   Solit, David B ^a   Baselga, Jose ^a   Brogi, Edi ^a   Ladanyi, Marc ^a   Weigelt, Britta ^a   Reis Filho, Jorge S ^a   more..

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b HOSPITAL ISRAELITA ALBERT EINSTEIN   (Brazil)

^c UNIVERSITY GENERAL HOSPITAL OF PATRAS   (Greece)

^d UNIVERSITY OF TURIN   (Italy)

Author keywords

gene amplification; massively parallel sequencing; mutation; phyllodes tumour; promoter; telomerase

Indexed keywords

CYCLIN DEPENDENT KINASE INHIBITOR 2A; EPIDERMAL GROWTH FACTOR RECEPTOR; MESSENGER RNA; PROTEIN P53; TELOMERASE REVERSE TRANSCRIPTASE; TELOMERASE; TERT PROTEIN, HUMAN;

AMPLICON; ARTICLE; COPY NUMBER VARIATION; CYSTOSARCOMA PHYLLOIDES; DIFFERENTIAL DIAGNOSIS; EXON; FIBROADENOMA; FLUORESCENCE IN SITU HYBRIDIZATION; GENE AMPLIFICATION; GENE DOSAGE; GENE MUTATION; GENE SEQUENCE; HETEROZYGOSITY LOSS; HUMAN; LASER CAPTURE MICRODISSECTION; MAJOR CLINICAL STUDY; MASSIVELY PARALLEL SEQUENCING; ONCOGENE N RAS; PREDICTIVE VALUE; PRIORITY JOURNAL; PROMOTER REGION; SOMATIC MUTATION; TUMOR GENE; BREAST TUMOR; FEMALE; GENETICS; HIGH THROUGHPUT SEQUENCING; MUTATION; PATHOLOGY; PHYLLODES TUMOR; PROCEDURES; TUMOR RECURRENCE;

BREAST NEOPLASMS; DIAGNOSIS, DIFFERENTIAL; FEMALE; FIBROADENOMA; GENE AMPLIFICATION; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; MUTATION; NEOPLASM RECURRENCE, LOCAL; PHYLLODES TUMOR; PROMOTER REGIONS, GENETIC; TELOMERASE;

EID: 84959127806     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4672     Document Type: Article

References (57)

1. Tan PH, Tse G, Lee A, et al., Fibroepithelial tumours. In WHO Classification of Tumours of the Breast, 4th edn, Lakhani SR, Ellis IO, Schnitt SJ, et al (eds). IARC Press: Lyon, France, 2012.
2. Tan PH, Thike AA, Tan WJ, et al., Predicting clinical behaviour of breast phyllodes tumours: a nomogram based on histological criteria and surgical margins. J Clin Pathol 2012; 65: 69-76.
3. Barth RJ Jr., Histologic features predict local recurrence after breast conserving therapy of phyllodes tumors. Breast Cancer Res Treat 1999; 57: 291-295.
4. Ben Hassouna J, Damak T, Gamoudi A, et al., Phyllodes tumors of the breast: a case series of 106 patients. Am J Surg 2006; 192: 141-147.
5. Belkacemi Y, Bousquet G, Marsiglia H, et al., Phyllodes tumor of the breast. Int J Radiat Oncol Biol Phys 2008; 70: 492-500.
6. Asoglu O, Ugurlu MM, Blanchard K, et al., Risk factors for recurrence and death after primary surgical treatment of malignant phyllodes tumors. Ann Surg Oncol 2004; 11: 1011-1017.
7. Mishra SP, Tiwary SK, Mishra M, et al., Phyllodes tumor of breast: a review article. ISRN Surg 2013; 2013: 361469.
8. Khazai L, Middleton LP, Goktepe N, et al., Breast pathology second review identifies clinically significant discrepancies in over 10% of patients. J Surg Oncol 2015; 111: 192-197.
9. Cheng SP, Chang YC, Liu TP, et al., Phyllodes tumor of the breast: the challenge persists. World J Surg 2006; 30: 1414-1421.
10. Tan J, Ong CK, Lim WK, et al., Genomic landscapes of breast fibroepithelial tumors. Nat Genet 2015; 47: 1341-1345.
11. Cani AK, Hovelson DH, McDaniel AS, et al., Next-gen sequencing exposes frequent MED12 mutations and actionable therapeutic targets in phyllodes tumors. Mol Cancer Res 2015; 13: 613-619.
12. Yoshida M, Ogawa R, Yoshida H, et al., TERT promoter mutations are frequent and show association with MED12 mutations in phyllodes tumors of the breast. Br J Cancer 2015; 113: 1244-1248.
13. Weinreb I, Piscuoglio S, Martelotto LG, et al., Hotspot activating PRKD1 somatic mutations in polymorphous low-grade adenocarcinomas of the salivary glands. Nat Genet 2014; 46: 1166-1169.
14. Cheng DT, Mitchell TN, Zehir A, et al., Memorial Sloan Kettering-Integrated Mutation Profiling of Actionable Cancer Targets (MSK-IMPACT): a hybridization capture-based next-generation sequencing clinical assay for solid tumor molecular oncology. J Mol Diagn 2015; 17: 251-264.
15. Li H, Durbin R,. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009; 25: 1754-1760.
16. DePristo MA, Banks E, Poplin R, et al., A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 2011; 43: 491-498.
17. Cibulskis K, Lawrence MS, Carter SL, et al., Sensitive detection of somatic point mutations in impure and heterogeneous cancer samples. Nat Biotechnol 2013; 31: 213-219.
18. Saunders CT, Wong WS, Swamy S, et al., Strelka: accurate somatic small-variant calling from sequenced tumor-normal sample pairs. Bioinformatics 2012; 28: 1811-1817.
19. Koboldt DC, Zhang Q, Larson DE, et al., VarScan 2: somatic mutation and copy number alteration discovery in cancer by exome sequencing. Genome Res 2012; 22: 568-576.
20. De Mattos-Arruda L, Weigelt B, Cortes J, et al., Capturing intra-tumor genetic heterogeneity by de novo mutation profiling of circulating cell-free tumor DNA: a proof of principle. Ann Oncol 2014; 25: 1729-1735.
21. Robinson JT, Thorvaldsdottir H, Winckler W, et al., Integrative genomics viewer. Nat Biotechnol 2011; 29: 24-26.
22. McKenna A, Hanna M, Banks E, et al., The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res 2010; 20: 1297-1303.
23. Young SR, Pilarski RT, Donenberg T, et al., The prevalence of BRCA1 mutations among young women with triple-negative breast cancer. BMC Cancer 2009; 9: 86.
24. Ronglai S, Seshan V,. FACETS: Fraction and allele-specific copy number estimates from tumor sequencing. Memorial Sloan-Kettering Cancer Center, Department of Epidemiology and Biostatistics Working Paper Series, 2015; Working Paper 29.
25. Schwarz JM, Rödelsperger C, Schuelke M, et al., MutationTaster evaluates disease-causing potential of sequence alterations. Nat Methods 2010; 7: 575-576.
26. Carter H, Chen S, Isik L, et al., Cancer-specific high-throughput annotation of somatic mutations: computational prediction of driver missense mutations. Cancer Res 2009; 69: 6660-6667.
27. Shihab HA, Gough J, Cooper DN, et al., Predicting the functional, molecular, and phenotypic consequences of amino acid substitutions using hidden Markov models. Hum Mutat 2013; 34: 57-65.
28. Choi Y, Sims GE, Murphy S, et al., Predicting the functional effect of amino acid substitutions and indels. PLoS One 2012; 7: e46688.
29. Martelotto LG, Ng C, De Filippo MR, et al., Benchmarking mutation effect prediction algorithms using functionally validated cancer-related missense mutations. Genome Biol 2014; 15: 484.
30. Kandoth C, McLellan MD, Vandin F, et al., Mutational landscape and significance across 12 major cancer types. Nature 2013; 502: 333-339.
31. Futreal PA, Coin L, Marshall M, et al., A census of human cancer genes. Nat Rev Cancer 2004; 4: 177-183.
32. Lawrence MS, Stojanov P, Mermel CH, et al., Discovery and saturation analysis of cancer genes across 21 tumour types. Nature 2014; 505: 495-501.
33. Carter SL, Cibulskis K, Helman E, et al., Absolute quantification of somatic DNA alterations in human cancer. Nat Biotechnol 2012; 30: 413-421.
34. Landau DA, Carter SL, Stojanov P, et al., Evolution and impact of subclonal mutations in chronic lymphocytic leukemia. Cell 2013; 152: 714-726.
35. Curtis C, Shah SP, Chin SF, et al., The genomic and transcriptomic architecture of 2000 breast tumours reveals novel subgroups. Nature 2012; 486: 346-352.
36. Weigelt B, Geyer FC, Natrajan R, et al., The molecular underpinning of lobular histological growth pattern: a genome-wide transcriptomic analysis of invasive lobular carcinomas and grade- and molecular subtype-matched invasive ductal carcinomas of no special type. J Pathol 2010; 220: 45-57.
37. Arriola E, Marchio C, Tan DS, et al., Genomic analysis of the HER2/TOP2A amplicon in breast cancer and breast cancer cell lines. Lab Invest 2008; 88: 491-503.
38. O'Callaghan NJ, Fenech M,. A quantitative PCR method for measuring absolute telomere length. Biol Proced Online 2011; 13: 3.
39. Kannan K, Inagaki A, Silber J, et al., Whole-exome sequencing identifies ATRX mutation as a key molecular determinant in lower-grade glioma. Oncotarget 2012; 3: 1194-1203.
40. Wu KD, Orme LM, Shaughnessy J Jr, et al., Telomerase and telomere length in multiple myeloma: correlations with disease heterogeneity, cytogenetic status, and overall survival. Blood 2003; 101: 4982-4989.
41. Julious SA,. Two-sided confidence intervals for the single proportion: comparison of seven methods by Robert G. Newcombe, Statistics in Medicine 1998; 17: 857-872. Stat Med 2005; 24: 3383-3384.
42. Wilson EB,. Probable inference, the law of succession, and statistical inference. J Am Statist Assoc 1927; 22: 209-212.
43. Piscuoglio S, Murray M, Fusco N, et al., MED12 somatic mutations in fibroadenomas and phyllodes tumours of the breast. Histopathology 2015; 67: 719-729.
44. Weinhold N, Jacobsen A, Schultz N, et al., Genome-wide analysis of noncoding regulatory mutations in cancer. Nat Genet 2014; 46: 1160-1165.
45. Heidenreich B, Rachakonda PS, Hemminki K, et al., TERT promoter mutations in cancer development. Curr Opin Genet Dev 2014; 24: 30-37.
46. Borah S, Xi L, Zaug AJ, et al., Cancer. TERT promoter mutations and telomerase reactivation in urothelial cancer. Science 2015; 347: 1006-1010.
47. Vinagre J, Almeida A, Populo H, et al., Frequency of TERT promoter mutations in human cancers. Nat Commun 2013; 4: 2185.
48. Nault JC, Zucman-Rossi J,. TERT promoter mutations in primary liver tumors. Clin Res Hepatol Gastroenterol 2015; DOI: 10.1016/j.clinre.2015.07.006.
49. Li C, Wu S, Wang H, et al., The C228T mutation of TERT promoter frequently occurs in bladder cancer stem cells and contributes to tumorigenesis of bladder cancer. Oncotarget 2015; 6: 19542-19551.
50. Heidenreich B, Rachakonda PS, Hosen I, et al., TERT promoter mutations and telomere length in adult malignant gliomas and recurrences. Oncotarget 2015; 6: 10617-10633.
51. de Biase D, Gandolfi G, Ragazzi M, et al., TERT promoter mutations in papillary thyroid microcarcinomas. Thyroid 2015; 25: 1013-1019.
52. Chiba K, Johnson JZ, Vogan JM, et al., Cancer-associated TERT promoter mutations abrogate telomerase silencing. Elife 2015; 4: e07918.
53. Liu T, Brown TC, Juhlin CC, et al., The activating TERT promoter mutation C228T is recurrent in subsets of adrenal tumors. Endocr Relat Cancer 2014; 21: 427-434.
54. Hosen I, Rachakonda PS, Heidenreich B, et al., TERT promoter mutations in clear cell renal cell carcinoma. Int J Cancer 2015; 136: 2448-2452.
55. Lim WK, Ong CK, Tan J, et al., Exome sequencing identifies highly recurrent MED12 somatic mutations in breast fibroadenoma. Nat Genet 2014; 46: 877-880.
56. Clynes D, Jelinska C, Xella B, et al., Suppression of the alternative lengthening of telomere pathway by the chromatin remodelling factor ATRX. Nat Commun 2015; 6: 7538.
57. Napier CE, Huschtscha LI, Harvey A, et al., ATRX represses alternative lengthening of telomeres. Oncotarget 2015; 6: 16543-16558.