A molecular portrait of microsatellite instability across multiple cancers

Nature Communications

Volumn 8, Issue , 2017, Pages

  Cortes Ciriano, Isidro ^a,b   Lee, Sejoon ^c   Park, Woong Yang ^c   Kim, Tae Min ^a   Park, Peter J ^a,d  

^a HARVARD MEDICAL SCHOOL   (United States)

^b HARVARD UNIVERSITY   (United States)

^c Samsung Medical Center   (South Korea)

^d The Catholic University of Korea   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

MICROSATELLITE DNA;

CANCER; DNA; FREQUENCY ANALYSIS; GENETIC MARKER; GENOME; MOLECULAR ANALYSIS; MUTATION; TUMOR;

ADRENAL CORTEX CARCINOMA; ARTICLE; BLADDER CANCER; BREAST CANCER; CANCER IMMUNOTHERAPY; CANCER PATIENT; COLON ADENOCARCINOMA; CONTROLLED STUDY; COPY NUMBER VARIATION; CUTANEOUS MELANOMA; DNA REPAIR; ENDOMETRIUM CARCINOMA; ESOPHAGUS CARCINOMA; EXOME; FRAMESHIFT MUTATION; GENE EXPRESSION; GERMLINE MUTATION; GLIOBLASTOMA; GLIOMA; HEAD AND NECK SQUAMOUS CELL CARCINOMA; HUMAN; KIDNEY CARCINOMA; LIVER CELL CARCINOMA; LUNG ADENOCARCINOMA; MICROSATELLITE INSTABILITY; MITOCHONDRIAL GENOME; MULTIPLE CANCER; OVARY CANCER; PANCREAS CANCER; PARAGANGLIOMA; PHEOCHROMOCYTOMA; PROMOTER REGION; PROSTATE ADENOCARCINOMA; RECTUM CARCINOMA; SOMATIC MUTATION; SQUAMOUS CELL CARCINOMA; SQUAMOUS CELL LUNG CARCINOMA; STOMACH ADENOCARCINOMA; THYROID CANCER; UNTRANSLATED REGION; WHOLE EXOME SEQUENCING; WHOLE GENOME SEQUENCING; CLASSIFICATION; GENETICS; MUTATION; NEOPLASM; ONCOGENE; PHENOTYPE;

DNA REPAIR; GENOME, MITOCHONDRIAL; HUMANS; MICROSATELLITE INSTABILITY; MUTATION; NEOPLASMS; ONCOGENES; PHENOTYPE; WHOLE EXOME SEQUENCING; WHOLE GENOME SEQUENCING;

EID: 85020420753     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms15180     Document Type: Article

References (57)

1. Aaltonen, L. A. et al. Clues to the pathogenesis of familial colorectal cancer. Science 260, 812-816 (1993).
2. Hendriks, Y. M. C. et al. Diagnostic approach and management of Lynch syndrome (hereditary nonpolyposis colorectal carcinoma): a guide for clinicians. CA. Cancer J. Clin. 56, 213-225 (2006).
3. Herman, J. G. et al. Incidence and functional consequences of hMLH1 promoter hypermethylation in colorectal carcinoma. Proc. Natl Acad. Sci. USA 95, 6870-6875 (1998).
4. Ligtenberg, M. J. L. et al. Heritable somatic methylation and inactivation of MSH2 in families with Lynch syndrome due to deletion of the 3 exons of TACSTD1. Nat. Genet. 41, 112-117 (2009).
5. Volinia, S. et al. A microRNA expression signature of human solid tumors defines cancer gene targets. Proc. Natl Acad. Sci. USA 103, 2257-2261 (2006).
6. Jiricny, J. The multifaceted mismatch-repair system. Nat. Rev. Mol. Cell Biol. 7, 335-346 (2006).
7. Vilar, E. & Gruber, S. B. Microsatellite instability in colorectal cancer-the stable evidence. Nat. Rev. Clin. Oncol. 7, 153-162 (2010).
8. Dudley, J. C., Lin, M.-T., Le, D. T. & Eshleman, J. R. Microsatellite instability as a biomarker for PD-1 blockade. Clin. Cancer Res. 22, 813-820 (2016).
9. Gryfe, R. et al. Tumor microsatellite instability and clinical outcome in young patients with colorectal cancer. N. Engl. J. Med. 342, 69-77 (2000).
10. Bodmer, W., Bishop, T. & Karran, P. Genetic steps in colorectal cancer. Nat. Genet. 6, 217-219 (1994).
11. Rizvi, N. A. et al. Cancer immunology. Mutational landscape determines sensitivity to PD-1 blockade in non-small cell lung cancer. Science 348, 124-128 (2015).
12. Snyder, A. et al. Genetic basis for clinical response to CTLA-4 blockade in melanoma. N. Engl. J. Med. 371, 2189-2199 (2014).
13. Le, D. T. et al. PD-1 blockade in tumors with mismatch-repair deficiency. N. Engl. J. Med. 372, 2509-2520 (2015).
14. Weinstein, J. N. et al. The cancer genome atlas pan-cancer analysis project. Nat. Genet. 45, 1113-1120 (2013).
15. Kim, T.-M., Laird, P. W. & Park, P. J. The landscape of microsatellite instability in colorectal and endometrial cancer genomes. Cell 155, 858-868 (2013).
16. Hause, R. J., Pritchard, C. C., Shendure, J. & Salipante, S. J. Classification and characterization of microsatellite instability across 18 cancer types. Nat. Med. 22, 1342-1350 (2016).
17. Bass, A. J. et al. Comprehensive molecular characterization of gastric adenocarcinoma. Nature 513, 202-209 (2014).
18. The Cancer Genome Atlas Research Network. Integrated genomic characterization of endometrial carcinoma. Nature 497, 67-73 (2013).
19. Cancer Genome Atlas Research Network. Comprehensive molecular characterization of human colon and rectal cancer. Nature 487, 330-337 (2012).
20. Lawrence, M. S. et al. Mutational heterogeneity in cancer and the search for new cancer-associated genes. Nature 499, 214-218 (2013).
21. Kang, J., D'Andrea, A. D. & Kozono, D. A DNA repair pathway-focused score for prediction of outcomes in ovarian cancer treated with platinum-based chemotherapy. J. Natl Cancer Inst. 104, 670-681 (2012).
22. Lynch, H. T., Snyder, C. L., Shaw, T. G., Heinen, C. D. & Hitchins, M. P. Milestones of Lynch syndrome: 1895-2015. Nat. Rev. Cancer 15, 181-194 (2015).
23. Hayward, B. E. et al. Extensive gene conversion at the PMS2 DNA mismatch repair locus. Hum. Mutat. 28, 424-430 (2007).
24. Brogna, S. & Wen, J. Nonsense-mediated mRNA decay (NMD) mechanisms. Nat. Struct. Mol. Biol. 16, 107-113 (2009).
25. de la Chapelle, A. Genetic predisposition to colorectal cancer. Nat. Rev. Cancer 4, 769-780 (2004).
26. Kandoth, C. et al. Mutational landscape and significance across 12 major cancer types. Nature 502, 333-339 (2013).
27. Huang, J. et al. APC mutations in colorectal tumours with mismatch repair deficiency. Proc. Natl Acad. Sci. USA 93, 9049-9054 (1996).
28. Giannakis, M. et al. RNF43 is frequently mutated in colorectal and endometrial cancers. Nat. Genet. 46, 1264-1266 (2014).
29. Tougeron, D. et al. Tumor-infiltrating lymphocytes in colorectal cancers with microsatellite instability are correlated with the number and spectrum of frameshift mutations. Mod. Pathol. 22, 1186-1195 (2009).
30. Yoshida, Y. et al. ALPK2 is crucial for luminal apoptosis and DNA repair-related gene expression in a three-dimensional colonic-crypt model. Anticancer Res. 32, 2301-2308 (2012).
31. Katainen, R. et al. CTCF/cohesin-binding sites are frequently mutated in cancer. Nat. Genet. 47, 818-821 (2015).
32. Weinhold, N., Jacobsen, A., Schultz, N., Sander, C. & Lee, W. Genome-wide analysis of noncoding regulatory mutations in cancer. Nat. Genet. 46, 1160-1165 (2014).
33. Aran, D., Sirota, M. & Butte, A. J. Systematic pan-cancer analysis of tumour purity. Nat. Commun. 6, 8971 (2015).
34. Mayr, C. & Bartel, D. P. Widespread shortening of 3UTRs by alternative cleavage and polyadenylation activates oncogenes in cancer cells. Cell 138, 673-684 (2009).
35. Yoon, K. et al. Comprehensive genome-and transcriptome-wide analyses of mutations associated with microsatellite instability in Korean gastric cancers. Genome Res. 23, 1109-1117 (2013).
36. Pal, T., Permuth-Wey, J., Kumar, A. & Sellers, T. A. Systematic review and meta-analysis of ovarian cancers: estimation of microsatellite-high frequency and characterization of mismatch repair deficient tumor histology. Clin. Cancer Res. 14, 6847-6854 (2008).
37. Altavilla, G., Fassan, M., Busatto, G., Orsolan, M. & Giacomelli, L. Microsatellite instability and hMLH1 and hMSH2 expression in renal tumors. Oncol. Rep. 24, 927-932 (2010).
38. Watson, M. M. C., Berg, M. & Søreide, K. Prevalence and implications of elevated microsatellite alterations at selected tetranucleotides in cancer. Br. J. Cancer 111, 823-827 (2014).
39. Ernst, J. & Kellis, M. Large-scale imputation of epigenomic datasets for systematic annotation of diverse human tissues. Nat. Biotechnol. 33, 364-376 (2015).
40. Larman, T. C. et al. Spectrum of somatic mitochondrial mutations in five cancers. Proc. Natl Acad. Sci. USA 109, 14087-14091 (2012).
41. Schwartz, S. & Perucho, M. Somatic mutations in mitochondrial DNA do not associate with nuclear microsatellite instability in gastrointestinal cancer. Gastroenterology 119, 1806-1807 (2000).
42. Breiman, L. Random forests. Mach. Learn. 45, 5-32 (2001).
43. Norinder, U., Carlsson, L., Boyer, S. & Eklund, M. Introducing conformal prediction in predictive modeling. a transparent and flexible alternative to applicability domain determination. J. Chem. Inf. Model. 54, 1596-1603 (2014).
44. Murphy, M. A. & Wentzensen, N. Frequency of mismatch repair deficiency in ovarian cancer: a systematic review. Int. J. Cancer 129, 1914-1922 (2011).
45. Supek, F. & Lehner, B. Differential DNA mismatch repair underlies mutation rate variation across the human genome. Nature 521, 81-84 (2015).
46. Kuismanen, S. A. et al. Endometrial and colorectal tumors from patients with hereditary nonpolyposis colon cancer display different patterns of microsatellite instability. Am. J. Pathol. 160, 1953-1958 (2002).
47. Miller, S. L., Antico, G., Raghunath, P. N., Tomaszewski, J. E. & Clevenger, C. V. Nek3 kinase regulates prolactin-mediated cytoskeletal reorganization and motility of breast cancer cells. Oncogene 26, 4668-4678 (2007).
48. Niu, B. et al. MSIsensor: microsatellite instability detection using paired tumor-normal sequence data. Bioinformatics 30, 1015-1016 (2014).
49. Huang, M. N. et al. MSIseq: software for assessing microsatellite instability from catalogs of somatic mutations. Sci. Rep. 5, 13321 (2015).
50. Dohm, J. C., Lottaz, C., Borodina, T. & Himmelbauer, H. Substantial biases in ultra-short read data sets from high-throughput DNA sequencing. Nucleic Acids Res. 36, e105-e105 (2008).
51. Bacher, J. W. et al. Development of a fluorescent multiplex assay for detection of MSI-high tumors. Dis. Markers 20, 237-250 (2004).
52. Cibulskis, K. et al. Sensitive detection of somatic point mutations in impure and heterogeneous cancer samples. Nat. Biotechnol. 31, 213-219 (2013).
53. 1000 Genomes Project Consortium. A global reference for human genetic variation. Nature 526, 68-74 (2015).
54. DePristo, M. A. et al. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet. 43, 491-498 (2011).
55. Wang, K., Li, M. & Hakonarson, H. ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res. 38, e164 (2010).
56. Consortium, R. E. et al. Integrative analysis of 111 reference human epigenomes. Nature 518, 317-330 (2015).
57. Kuhn, M. & Johnson, K. Applied Predictive Modeling (Springer, 2013)