Crypt base columnar stem cells in small intestines of mice are radioresistant

Gastroenterology

Volumn 143, Issue 5, 2012, Pages 1266-1276

  Hua, Guoqiang ^a   Thin, Tin Htwe ^a   Feldman, Regina ^a   Haimovitz Friedman, Adriana ^a   Clevers, Hans ^b   Fuks, Zvi ^a   Kolesnick, Richard ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

BrdU; Cancer Treatment; GI Syndrome; Radioresistance

Indexed keywords

BRCA1 PROTEIN; CASPASE 3; DNA; HISTONE H2AX; RAD51 PROTEIN;

ADULT STEM CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL ASSAY; CELL CYCLE ARREST; CELL GROWTH; CELL POPULATION; CELL PROTECTION; CELL REGENERATION; CELL SURVIVAL; CONTROLLED STUDY; CRYPT BASE COLUMNAR CELL; CRYPT CELL; DNA REPAIR; DOUBLE STRANDED DNA BREAK; GENOTOXICITY; HOMOLOGOUS RECOMBINATION; INTESTINE INJURY; JEJUNUM; MITOSIS; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; RADIATION DOSE; RADIATION INJURY; RADIATION INJURY REPAIR; RADIOSENSITIVITY; SMALL INTESTINE; STEM CELL;

EID: 84868109646     PISSN: 00165085     EISSN: 15280012     Source Type: Journal    
DOI: 10.1053/j.gastro.2012.07.106     Document Type: Article

References (40)

1. M. Mohrin, E. Bourke, D. Alexander Hematopoietic stem cell quiescence promotes error-prone DNA repair and mutagenesis Cell Stem Cell 7 2010 174 185
2. P.A. Sotiropoulou, A. Candi, G. Mascre Bcl-2 and accelerated DNA repair mediates resistance of hair follicle bulge stem cells to DNA-damage-induced cell death Nat Cell Biol 12 2010 572 582
3. E.D. Tichy, R. Pillai, L. Deng Mouse embryonic stem cells, but not somatic cells, predominantly use homologous recombination to repair double-strand DNA breaks Stem Cells Dev 19 2010 1699 1711
4. C.S. Potten, R. Gandara, Y.R. Mahida The stem cells of small intestinal crypts: where are they? Cell Prolif 42 2009 731 750
5. C.S. Potten Radiation, the ideal cytotoxic agent for studying the cell biology of tissues such as the small intestine Radiat Res 161 2004 123 136
6. J.A. Rotolo, J.G. Maj, R. Feldman Bax and Bak do not exhibit functional redundancy in mediating radiation-induced endothelial apoptosis in the intestinal mucosa Int J Radiat Oncol Biol Phys 70 2008 804 815
7. P. Kaur, C.S. Potten Cell migration velocities in the crypts of the small intestine after cytotoxic insult are not dependent on mitotic activity Cell Tissue Kinet 19 1986 601 610
8. C.S. Potten A comprehensive study of the radiobiological response of the murine (BDF1) small intestine Int J Radiat Biol 58 1990 925 973
9. C.S. Potten, Y. Taylor, J.H. Hendry The doubling time of regenerating clonogenic cells in the crypts of the irradiated mouse small intestine Int J Radiat Biol 54 1988 1041 1051
10. H.R. Withers Regeneration of intestinal mucosa after irradiation Cancer 28 1971 75 81
11. J.S. Bedford, J.B. Mitchell, H.G. Griggs Radiation-induced cellular reproductive death and chromosome aberrations Radiat Res 76 1978 573 586
12. A. Ciccia, S.J. Elledge The DNA damage response: making it safe to play with knives Mol Cell 40 2010 179 204
13. S. Bekker-Jensen, N. Mailand Assembly and function of DNA double-strand break repair foci in mammalian cells DNA Repair (Amst) 9 2010 1219 1228
14. A. Kinner, W. Wu, C. Staudt Gamma-H2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin Nucleic Acids Res 36 2008 5678 5694
15. D.W. Chan, B.P. Chen, S. Prithivirajsingh Autophosphorylation of the DNA-dependent protein kinase catalytic subunit is required for rejoining of DNA double-strand breaks Genes Dev 16 2002 2333 2338
16. H. Cheng, C.P. Leblond Origin, differentiation and renewal of the four main epithelial cell types in the mouse small intestine V. Unitarian theory of the origin of the four epithelial cell types Am J Anat 141 1974 537 561
17. N. Barker, J.H. van Es, J. Kuipers Identification of stem cells in small intestine and colon by marker gene Lgr5 Nature 449 2007 1003 1007
18. T. Sato, R.G. Vries, H.J. Snippert Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche Nature 459 2009 262 265
19. W. Bocker, G. Iliakis Computational methods for analysis of foci: validation for radiation-induced gamma-H2AX foci in human cells Radiat Res 165 2006 113 124
20. A.G. Schepers, R. Vries, M. van den Born Lgr5 intestinal stem cells have high telomerase activity and randomly segregate their chromosomes EMBO J 30 2011 1104 1109
21. H.R. Withers, M.M. Elkind Microcolony survival assay for cells of mouse intestinal mucosa exposed to radiation Int J Radiat Biol Relat Stud Phys Chem Med 17 1970 261 267
22. N.H. Terry, E.L. Travis The influence of bone marrow depletion on intestinal radiation damage Int J Radiat Oncol Biol Phys 17 1989 569 573
23. J.H. Hendry, C.S. Potten, N.P. Roberts The gastrointestinal syndrome and mucosal clonogenic cells: relationships between target cell sensitivities, LD50 and cell survival, and their modification by antibiotics Radiat Res 96 1983 100 112
24. J.G. Maj, F. Paris, A. Haimovitz-Friedman Microvascular function regulates intestinal crypt response to radiation Cancer Res 63 2003 4338 4341
25. D. Booth, C.S. Potten Protection against mucosal injury by growth factors and cytokines JNCI Monographs 29 2001 16 20
26. T. Sato, J.H. van Es, H.J. Snippert Paneth cells constitute the niche for Lgr5 stem cells in intestinal crypts Nature 469 2011 415 418
27. H.J. Ch'ang, J.G. Maj, F. Paris ATM regulates target switching to escalating doses of radiation in the intestines Nat Med 11 2005 477 478
28. S. Itzkovitz, A. Lyubimova, I.C. Blat Single-molecule transcript counting of stem-cell markers in the mouse intestine Nat Cell Biol 14 2011 106 114
29. E. Riballo, M. Kuhne, N. Rief A pathway of double-strand break rejoining dependent upon ATM, Artemis, and proteins locating to gamma-H2AX foci Mol Cell 16 2004 715 724
30. W. Qiu, B. Leibowitz, L. Zhang Growth factors protect intestinal stem cells from radiation-induced apoptosis by suppressing PUMA through the PI3K/AKT/p53 axis Oncogene 29 2010 1622 1632
31. A. Merlos-Suarez, F.M. Barriga, P. Jung The intestinal stem cell signature identifies colorectal cancer stem cells and predicts disease relapse Cell Stem Cell 8 2011 511 524
32. N. Takeda, R. Jain, M.R. LeBoeuf Interconversion between intestinal stem cell populations in distinct niches Science 334 2011 1420 1424
33. K.S. Yan, L.A. Chia, X. Li The intestinal stem cell markers Bmi1 and Lgr5 identify two functionally distinct populations Proc Natl Acad Sci U S A 109 2012 466 471
34. L. Van Landeghem, M.A. Santoro, A.E. Krebs Activation of two distinct Sox9-EGFP-expressing intestinal stem cell populations during crypt regeneration after irradiation Am J Physiol Gastrointest Liver Physiol 302 2012 G1111 G1132
35. J. Denekamp Cell kinetics and radiation biology Int J Radiat Biol Relat Stud Phys Chem Med 49 1986 357 380
36. H.R. Withers, K. Mason, B.O. Reid Response of mouse intestine to neutrons and gamma rays in relation to dose fractionation and division cycle Cancer 34 1974 39 47
37. S.N. Powell, L.A. Kachnic Roles of BRCA1 and BRCA2 in homologous recombination, DNA replication fidelity and the cellular response to ionizing radiation Oncogene 22 2003 5784 5791
38. J.A. Rotolo, J. Mesicek, J. Maj Regulation of ceramide synthase-mediated crypt epithelium apoptosis by DNA damage repair enzymes Cancer Res 70 2010 957 967
39. N. Barker, R.A. Ridgway, J.H. van Es Crypt stem cells as the cells-of-origin of intestinal cancer Nature 457 2009 608 611
40. H. Takahashi, H. Ishii, N. Nishida Significance of Lgr5(+ve) cancer stem cells in the colon and rectum Ann Surg Oncol 18 2010 1166 1174