Lineage tracing reveals multipotent stem cells maintain human adenomas and the pattern of clonal expansion in tumor evolution

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 27, 2013, Pages

  Humphries, Adam ^a,b   Cereser, Biancastella ^c   Gay, Laura J ^c   Miller, Daniel S J ^a   Das, Bibek ^a   Gutteridge, Alice ^a,d   Elia, George ^c   Nye, Emma ^a   Jeffery, Rosemary ^a,c   Poulsom, Richard ^a,c   Novelli, Marco R ^d   Rodriguez Justo, Manuel ^d   McDonald, Stuart A C ^c   Wright, Nicholas A ^a,c   Graham, Trevor A ^a,d,e  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^b IMPERIAL COLLEGE HEALTHCARE NHS TRUST   (United Kingdom)

^c QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cancer stem cells; Intestinal adenomas; Intratumor heterogeneity; Tumor growth; Tumor life history

Indexed keywords

CYTOCHROME C OXIDASE; MITOCHONDRIAL DNA; MUCIN;

ARTICLE; CARCINOGENESIS; CELL LINEAGE; COLON POLYPOSIS; COLORECTAL ADENOMA; DNA SEQUENCE; EPIGENETICS; GENE MUTATION; HUMAN; HUMAN CELL; HUMAN TISSUE; MOLECULAR CLONING; MULTIPOTENT STEM CELL; NEUROSECRETORY CELL; PRIORITY JOURNAL; TUMOR GROWTH;

CANCER STEM CELLS; INTESTINAL ADENOMAS; INTRATUMOR HETEROGENEITY; TUMOR GROWTH; TUMOR LIFE-HISTORY;

ADENOMA; CELL DIFFERENTIATION; CELL LINEAGE; CLONE CELLS; COLORECTAL NEOPLASMS; DNA, MITOCHONDRIAL; DNA, NEOPLASM; EPIGENESIS, GENETIC; HUMANS; MODELS, BIOLOGICAL; MULTIPOTENT STEM CELLS; MUTATION; NEOPLASTIC STEM CELLS;

EID: 84879736910     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1220353110     Document Type: Article

References (51)

1. Kinzler KW, Vogelstein B (1996) Lessons from hereditary colorectal cancer. Cell 87(2):159-170. (Pubitemid 26358996)
2. Fearon ER (2011) Molecular genetics of colorectal cancer. Annu Rev Pathol 6:479-507.
3. Anonymous; Cancer Genome Atlas Network (2012) Comprehensive molecular characterization of human colon and rectal cancer. Nature 487(7407):330-337.
4. Schepers AG, et al. (2012) Lineage tracing reveals Lgr5+ stem cell activity in mouse intestinal adenomas. Science 337(6095):730-735.
5. Greaves M, Maley CC (2012) Clonal evolution in cancer. Nature 481(7381):306-313.
6. Stryker SJ, et al. (1987) Natural history of untreated colonic polyps. Gastroenterology 93(5):1009-1013. (Pubitemid 18000643)
7. Welin S, Youker J, Spratt JS, Jr. (1963) The Rates and Patterns of Growth of 375 Tumors of the Large Intestine and Rectum Observed Serially by Double Contrast Enema Study (Malmoe Technique). Am J Roentgenol Radium Ther Nucl Med 90:673-687.
8. Hofstad B, et al. (1996) Growth of colorectal polyps: Redetection and evaluation of unresected polyps for a period of three years. Gut 39(3):449-456. (Pubitemid 26338537)
9. Tada M, Misaki F, Kawai K (1984) Growth rates of colorectal carcinoma and adenoma by roentgenologic follow-up observations. Gastroenterol Jpn 19(6):550-555. (Pubitemid 15152741)
10. Jones S, et al. (2008) Comparative lesion sequencing provides insights into tumor evolution. Proc Natl Acad Sci USA 105(11):4283-4288. (Pubitemid 351754372)
11. Wong W-M, et al. (2002) Histogenesis of human colorectal adenomas and hyperplastic polyps: The role of cell proliferation and crypt fission. Gut 50(2):212-217. (Pubitemid 34087934)
12. Preston SL, et al. (2003) Bottom-up histogenesis of colorectal adenomas: Origin in the monocryptal adenoma and initial expansion by crypt fission. Cancer Res 63(13):3819-3825. (Pubitemid 36793072)
13. Greaves LC, et al. (2006) Mitochondrial DNA mutations are established in human colonic stem cells, and mutated clones expand by crypt fission. Proc Natl Acad Sci USA 103(3):714-719. (Pubitemid 43153091)
14. Thirlwell C, et al. (2010) Clonality assessment and clonal ordering of individual neoplastic crypts shows polyclonality of colorectal adenomas. Gastroenterology 138(4):1441-1454.
15. Taylor RW, et al. (2003) Mitochondrial DNA mutations in human colonic crypt stem cells. J Clin Invest 112(9):1351-1360. (Pubitemid 38057689)
16. Fellous TG, et al. (2009) A methodological approach to tracing cell lineage in human epithelial tissues. Stem Cells 27(6):1410-1420.
17. Yatabe Y, Tavaré S, Shibata D (2001) Investigating stem cells in human colon by using methylation patterns. Proc Natl Acad Sci USA 98(19):10839-10844. (Pubitemid 32884117)
18. Graham TA, et al. (2011) Use of methylation patterns to determine expansion of stem cell clones in human colon tissue. Gastroenterology 140(4):1241-1250.e1249.
19. Samowitz WS, et al. (2005) Evaluation of a large, population-based sample supports a CpG island methylator phenotype in colon cancer. Gastroenterology 129(3):837-845. (Pubitemid 41242676)
20. Weisenberger DJ, et al. (2006) CpG island methylator phenotype underlies sporadic microsatellite instability and is tightly associated with BRAF mutation in colorectal cancer. Nat Genet 38(7):787-793. (Pubitemid 43980599)
21. Ang PW, et al. (2010) Comprehensive profiling of DNA methylation in colorectal cancer reveals subgroups with distinct clinicopathological and molecular features. BMC Cancer 10:227-234.
22. Martens EA, Kostadinov R, Maley CC, Hallatschek O (2011) Spatial structure increases the waiting time for cancer. New J Phys 13:13-37.
23. Siegmund KD, Marjoram P, Tavaré S, Shibata D (2009) Many colorectal cancers are "flat" clonal expansions. Cell Cycle 8(14):2187-2193.
24. Siegmund K, Marjoram P, Woo Y, Tavaré S, Shibata D (2009) Inferring clonal expansion and cancer stem cell dynamics from DNA methylation patterns in colorectal cancers. Proc Natl Acad Sci USA 106(12):4828-4833.
25. Siegmund KD, Marjoram P, Tavaré S, Shibata D (2011) High DNA methylation pattern intratumoral diversity implies weak selection in many human colorectal cancers. PLoS ONE 6(6):e21657.
26. Bozic I, et al. (2010) Accumulation of driver and passenger mutations during tumor progression. Proc Natl Acad Sci USA 107:18545-18550.
27. Eldredge N, Gould SJ (1972) Punctuated equilibria: An alternative to phyletic gradualism. Models in Paleobiology, ed Thomas JM (Freeman, Cooper and Co, San Francisco), pp 82-115.
28. Maley CC, et al. (2004) Selectively advantageous mutations and hitchhikers in neoplasms: p16 lesions are selected in Barrett's esophagus. Cancer Res 64(10):3414-3427. (Pubitemid 38657913)
29. Fearon ER, Vogelstein B (1990) A genetic model for colorectal tumorigenesis. Cell 61(5):759-767.
30. Leonard GD, Swain SM (2004) Ductal carcinoma in situ, complexities and challenges. J Natl Cancer Inst 96(12):906-920. (Pubitemid 38868137)
31. Jin Y, Sun A, Noriki S, Imamura Y, Fukuda M (2007) Detection of cancer clones in human colorectal adenoma as revealed by increased DNA instability and other biomarkers. Eur J Histochem 51(1):1-10. (Pubitemid 351480300)
32. Leggett BA, et al. (2001) Hyperplastic polyposis: Association with colorectal cancer. Am J Surg Pathol 25(2):177-184. (Pubitemid 32167499)
33. Ahn HS, et al. (2012) Hyperplastic Polyposis Syndrome Identified with a BRAF Mutation. Gut Liver 6(2):280-283.
34. Iino H, et al. (1999) DNA microsatellite instability in hyperplastic polyps, serrated adenomas, and mixed polyps: A mild mutator pathway for colorectal cancer? J Clin Pathol 52(1):5-9. (Pubitemid 29023500)
35. Woo Y-J, Siegmund KD, Tavaré S, Shibata D (2009) Older individuals appear to acquire mitotically older colorectal cancers. J Pathol 217(4):483-488.
36. Lamlum H, et al. (2000) APC mutations are sufficient for the growth of early colorectal adenomas. Proc Natl Acad Sci USA 97(5):2225-2228. (Pubitemid 30134050)
37. Feng Y, et al. (2011) Mutant KRAS promotes hyperplasia and alters differentiation in the colon epithelium but does not expand the presumptive stem cell pool. Gastroenterology 141(3):1003-1013.
38. Sansom OJ, et al. (2006) Loss of Apc allows phenotypic manifestation of the transforming properties of an endogenous K-ras oncogene in vivo. Proc Natl Acad Sci USA 103(38):14122-14127. (Pubitemid 44452990)
39. Navin N, et al. (2011) Tumour evolution inferred by single-cell sequencing. Nature 472(7341):90-94.
40. Nik-Zainal S, et al.; Breast Cancer Working Group of the International Cancer Genome Consortium (2012) The life history of 21 breast cancers. Cell 149(5):994-1007.
41. Gerlinger M, et al. (2012) Intratumor heterogeneity and branched evolution revealed by multiregion sequencing. N Engl J Med 366(10):883-892.
42. Xu X, et al. (2012) Single-cell exome sequencing reveals single-nucleotide mutation characteristics of a kidney tumor. Cell 148(5):886-895.
43. Campbell PJ, et al. (2008) Subclonal phylogenetic structures in cancer revealed by ultra-deep sequencing. Proc Natl Acad Sci USA 105(35):13081-13086.
44. Brodie CM, Crotty PL, Gaffney EF (2004) Morphologically distinct patterns of apoptosis correlate with size and high-grade dysplasia in colonic adenomas. Histopathology 44(3):240-246. (Pubitemid 38406616)
45. Dalerba P, et al. (2011) Single-cell dissection of transcriptional heterogeneity in human colon tumors. Nat Biotechnol 29(12):1120-1127.
46. Merlos-Suárez A, et al. (2011) The intestinal stem cell signature identifies colorectal cancer stem cells and predicts disease relapse. Cell Stem Cell 8(5):511-524.
47. Kemper K, et al. (2012) Monoclonal antibodies against Lgr5 identify human colorectal cancer stem cells. Stem Cells 30(11):2378-2386.
48. Lopez-Garcia C, Klein AM, Simons BD, Winton DJ (2010) Intestinal stem cell replacement follows a pattern of neutral drift. Science 330(6005):822-825.
49. Tsao JL, et al. (1998) Tracing cell fates in human colorectal tumors from somatic microsatellite mutations: Evidence of adenomas with stem cell architecture. Am J Pathol 153(4):1189-1200.
50. Poulsom R, Longcroft JM, Jeffery RE, Rogers LA, Steel JH (1998) A robust method for isotopic riboprobe in situ hybridisation to localise mRNAs in routine pathology specimens. Eur J Histochem 42(2):121-132. (Pubitemid 28362310)
51. Galandiuk S, et al. (2012) Field cancerization in the intestinal epithelium of patients with Crohn's ileocolitis. Gastroenterology 142(4):855-864.