Mutational spectrum of Barrett's stem cells suggests paths to initiation of a precancerous lesion

Nature Communications

Volumn 7, Issue , 2016, Pages

  Yamamoto, Yusuke ^a   Wang, Xia ^b   Bertrand, Denis ^c   Kern, Florian ^c   Zhang, Ting ^c   Duleba, Marcin ^b   Srivastava, Supriya ^d   Khor, Chiea Chuen ^c   Hu, Yuanyu ^c   Wilson, Lane H ^e   Blaszyk, Hagen ^f   Rolshud, Daniil ^f   Teh, Ming ^d   Liu, Jianjun ^c   Howitt, Brooke E ^d   Vincent, Matthew ^h   Crum, Christopher P ^d   Nagarajan, Niranjan ^c   Ho, Khek Yu ⁱ   McKeon, Frank ^b,i,j   Xian, Wa ^d,g,j   more..

^a NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

^b University of Houston   (United States)

^c GENOME INSTITUTE OF SINGAPORE   (Singapore)

^d National University Health System   (Singapore)

^e UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^f MAINE MEDICAL CENTER   (United States)

^g UNIVERSITY OF TEXAS   (United States)

^h Ocata Therapeutics   (United States)

ⁱ NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^j MultiClonal Therapeutics   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN P53; PROTEIN TYROSINE KINASE;

CELLS AND CELL COMPONENTS; ENZYME ACTIVITY; GENE EXPRESSION; GENOMICS; LESION; MUTATION; SPECTRUM; TUMOR;

ADULT; ADULT STEM CELL; ARTICLE; BARRETT ESOPHAGUS; CANCER GROWTH; CANCER PATIENT; CANCER RISK; CANCER STEM CELL; CELL DIFFERENTIATION; CELL ISOLATION; COPY NUMBER VARIATION; ENDOSCOPIC BIOPSY; ESOPHAGEAL ADENOCARCINOMA; GENE AMPLIFICATION; GENE FREQUENCY; GENE MUTATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MUTATIONAL ANALYSIS; PRECANCER; PROTO ONCOGENE; SINGLE NUCLEOTIDE POLYMORPHISM; XENOGRAFT; ANIMAL; CELL CULTURE; GENETICS; MALE; METABOLISM; MOUSE; MUTATION; PATHOLOGY; STEM CELL; TUMOR CELL CULTURE;

ANIMALS; BARRETT ESOPHAGUS; CELL DIFFERENTIATION; CELLS, CULTURED; HUMANS; MALE; MICE; MUTATION; PRECANCEROUS CONDITIONS; STEM CELLS; TUMOR CELLS, CULTURED;

EID: 84955567060     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms10380     Document Type: Article

References (51)

1. Sharma, P. Clinical practice. Barrett's esophagus. N. Engl. J. Med. 361, 2548-2556 (2009).
2. Reid, B. J., Li, X., Galipeau, P. C. & Vaughan, T. L. Barrett's oesophagus and oesophageal adenocarcinoma: time for a new synthesis. Nat. Rev. Cancer 10, 87-101 (2010).
3. Edgren, G., Adami, H. O., Weiderpass, E. & Nyrén, O. A global assessment of the oesophageal adenocarcinoma epidemic. Gut 62, 1406-1414 (2013).
4. Barrett, N. R. Chronic peptic ulcer of the oesophagus and 'oesophagitis'. Br. J. Surg. 38, 175-182 (1950).
5. Naef, A. P., Savary, M. & Ozzello, L. Columnar-lined lower esophagus: an acquired lesion with malignant predisposition. Report on 140 cases of Barrett esophagus with 12 adenocarcinomas. J. Thorac. Cardiovasc. Surg. 70, 826-835 (1975).
6. Haggitt, R. C. Barrett's esophagus, dysplasia, and adenocarcinoma. Hum. Pathol. 25, 982-993 (1994).
7. Ross-Innes, C. S. et al. Evaluation of a minimally invasive cell sampling device coupled with assessment of trefoil factor 3 expression for diagnosing Barrett's esophagus: a multi-center case-control study. PLoS Med. 12, e1001780 (2015).
8. Fearon, E. R. & Vogelstein, B. A genetic model for colorectal tumorigenesis. Cell 61, 759-767 (1990).
9. Correa, P. Human gastric carcinogenesis: a multistep and multifactorial process. First American Cancer Society Award Lecture on Cancer Epidemiology and Prevention. Cancer Res. 52, 6735-6740 (1992).
10. Hvid-Jensen, F., Pedersen, L., Drewes, A. M., Sørensen, H. T. & Funch-Jensen, P. Incidence of adenocarcinoma among patients with Barrett's esophagus. N. Engl. J. Med. 365, 1375-1383 (2011).
11. Shaheen, N. J. et al. Radiofrequency ablation in Barrett's esophagus with dysplasia. N. Engl. J. Med. 360, 2277-2288 (2009).
12. Vaccaro, B. J. et al. Detection of intestinal metaplasia after successful eradication of Barrett's Esophagus with radiofrequency ablation. Dig. Dis. Sci. 56, 1996-2000 (2011).
13. Titi, M. et al. Development of subsquamous high-grade dysplasia and adenocarcinoma after successful radiofrequency ablation of Barrett's esophagus. Gastroenterology 143, 564-566 (2012).
14. Haidry, R. & Lovat, L. Long-term durability of radiofrequency ablation for Barrett's-related neoplasia. Curr. Opin. Gastroenterol. 31, 316-320 (2015).
15. Sato, T. & Clevers, H. Growing self-organizing mini-guts from a single intestinal stem cell: mechanism and applications. Science 340, 1190-1194 (2013).
16. Wang, X. et al. Cloning and variation of ground state intestinal stem cells. Nature 522, 173-178 (2015).
17. Rheinwald, J. G. & Green, H. Serial cultivation of strains of human epidermal keratinocytes: the formation of keratinizing colonies from single cells. Cell 6, 331-343 (1975).
18. Kumar, P. A. et al. Distal airway stem cells render alveoli in vitro and during lung regeneration following H1N1 influenza infection. Cell 147, 525-538 (2011).
19. Stairs, D. B. et al. Cdx1 and c-Myc foster the initiation of transdifferentiation of the normal esophageal squamous epithelium toward Barrett's esophagus. PLoS ONE 3, e3534 (2008).
20. Wang, Q., Ma, C. & Kemmner, W. Wdr66 is a novel marker for risk stratification and involved in epithelial-mesenchymal transition of esophageal squamous cell carcinoma. BMC Cancer 13, 137 (2013).
21. Seaberg, R. M. & van der Kooy, D. Stem and progenitor cells: the premature desertion of rigorous definitions. Trends Neurosci. 26, 125-131 (2003).
22. Wang, X. et al. Residual embryonic cells as precursors of a Barrett's-like metaplasia. Cell 145, 1023-1035 (2011).
23. Quante, M. et al. Bile acid and inflammation activate gastric cardia stem cells in a mouse model of Barrett-like metaplasia. Cancer Cell 21, 36-51 (2012).
24. Nicholson, A. M. et al. Barrett's metaplasia glands are clonal, contain multiple stem cells and share a common squamous progenitor. Gut 61, 1380-1389 (2012).
25. Lavery, D. L. et al. The stem cell organisation, and the proliferative and gene expression profile of Barrett's epithelium, replicates pyloric-type gastric glands. Gut 63, 1854-1863 (2014).
26. Hongo, M., Nagasaki, Y. & Shoji, T. Epidemiology of esophageal cancer: orient to occident. Effects of chronology, geography and ethnicity. J. Gastroenterol. Hepatol. 24, 729-735 (2009).
27. Hahn, W. C. et al. Creation of human tumour cells with defined genetic elements. Nature 400, 464-468 (1999).
28. Shultz, L. D., Brehm, M. A., Bavari, S. & Greiner, D. L. Humanized mice as a preclinical tool for infectious disease and biomedical research. Ann. NY Acad. Sci. 1245, 50-54 (2011).
29. Agrawal, N. et al. Comparative genomic analysis of esophageal adenocarcinoma and squamous cell carcinoma. Cancer Dis. 2, 899-905 (2012).
30. Michael, D., Beer, D. G., Wilke, C. W., Miller, D. E. & Glover, T. W. Frequent deletions of FHIT and FRA3B in Barrett's metaplasia and esophageal adenocarcinomas. Oncogene 15, 1653-1659 (1997).
31. Powell, E. L. et al. Concordant loss of MTAP and p16/CDKN2A expression in gastroesophageal carcinogenesis: evidence of homozygous deletion in esophageal noninvasive precursor lesions and therapeutic implications. Am. J. Surg. Pathol. 29, 1497-1504 (2005).
32. Lai, L. A. et al. Deletion at fragile sites is a common and early event in Barrett's esophagus. Mol. Cancer Res. 8, 1084-1094 (2010).
33. Schulmann, K. et al. Inactivation of p16, RUNX3, and HPP1 occurs early in Barrett's-associated neoplastic progression and predicts progression risk. Oncogene 24, 4138-4148 (2005).
34. Ozeri-Galai, E., Bester, A. C. & Kerem, B. The complex basis underlying common fragile site instability in cancer. Trends Genet. 28, 295-302 (2012).
35. Dulak, A. M. et al. Gastrointestinal adenocarcinomas of the esophagus, stomach, and colon exhibit distinct patterns of genome instability and oncogenesis. Cancer Res. 72, 4383-4393 (2012).
36. Nancarrow, D. J. et al. Genome-wide copy number analysis in esophageal adenocarcinoma using high-density single-nucleotide polymorphism arrays. Cancer Res. 68, 4163-4172 (2008).
37. Dulak, A. M. et al. Exome and whole-genome sequencing of esophageal adenocarcinoma identifies recurrent driver events and mutational complexity. Nat. Genet. 45, 478-486 (2013).
38. Ishimura, N. et al. Endoscopic characteristics of short-segment Barrett's esophagus, focusing on squamous islands and mucosal folds. J. Gastroenterol. Hepatol. 27(Suppl 3): 82-87 (2012).
39. Chandrasoma, P. et al. Columnar-lined esophagus without intestinal metaplasia has no proven risk of adenocarcinoma. Am. J. Surg. Pathol. 36, 1-7 (2012).
40. Sato, T. et al. Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett's epithelium. Gastroenterology 141, 1762-1772 (2011).
41. Reid, B. J., Kostadinov, R. & Maley, C. C. New strategies in Barrett's esophagus: integrating clonal evolutionary theory with clinical management. Clin. Cancer Res. 17, 3512-3519 (2011).
42. Wood, L. D. et al. The genomic landscapes of human breast and colorectal cancers. Science 318, 1108-1113 (2007).
43. Hanahan, D. & Weinberg, R. A. Hallmarks of cancer: the next generation. Cell 144, 646-674 (2011).
44. Subramanian, A. et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. USA 102, 15545-15550 (2005).
45. Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760 (2009).
46. McKenna, A. et al. The genome analysis toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20, 1297-1303 (2010).
47. Li, H. et al. The sequence alignment/map format and SAMtools. Bioinformatics 25, 2078-2079 (2009).
48. Wilm, A. et al. LoFreq: a sequence-quality aware, ultra-sensitive variant caller for uncovering cell-population heterogeneity from high-throughput sequencing datasets. Nucleic Acids Res. 40, 11189-11201 (2012).
49. Zang, Z. J. et al. Exome sequencing of gastric adenocarcinoma identifies recurrent somatic mutations in cell adhesion and chromatin remodeling genes. Nat. Genet. 44, 570-574 (2012).
50. Nagarajan, N. et al. Whole-genome reconstruction and mutational signatures in gastric cancer. Genome Biol. 13, R115 (2012).
51. Kumar, P., Henikoff, S. & Ng, P. C. Predicting the effects of coding nonsynonymous variants on protein function using the SIFT algorithm. Nat. Protoc. 4, 1073-1081 (2009).