Loss of dna mismatch repair imparts a selective advantage in planarian adult stem cells

PLoS ONE

Volumn 6, Issue 7, 2011, Pages

  Hollenbach, Jessica P ^a   Resch, Alissa M ^a   Palakodeti, Dasaradhi ^a,b   Graveley, Brenton R ^a   Heinen, Christopher D ^a  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b TATA INSTITUTE OF FUNDAMENTAL RESEARCH   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ALKYLATING AGENT; CELL DNA; MESSENGER RNA; MISMATCH REPAIR PROTEIN; PROTEIN MLH1; PROTEIN MSH2; PROTEIN MSH6; DNA BINDING PROTEIN;

ADULT STEM CELL; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; DNA DAMAGE; GENE EXPRESSION; IN VIVO STUDY; MISMATCH REPAIR; NONHUMAN; NUCLEOTIDE SEQUENCE; RNA INTERFERENCE; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; CYTOLOGY; DRUG EFFECT; GENETIC SELECTION; GENETICS; HUMAN; METABOLISM; MITOSIS; MOLECULAR EVOLUTION; MOLECULAR GENETICS; MOUSE; PHYSIOLOGY; REGENERATION; SEQUENCE HOMOLOGY; TURBELLARIA;

ANIMALIA; PLANARIA; SCHMIDTEA MEDITERRANEA;

ADULT STEM CELLS; ALKYLATING AGENTS; AMINO ACID SEQUENCE; ANIMALS; DNA DAMAGE; DNA MISMATCH REPAIR; DNA-BINDING PROTEINS; EVOLUTION, MOLECULAR; HUMANS; MICE; MITOSIS; MOLECULAR SEQUENCE DATA; PLANARIANS; REGENERATION; RNA INTERFERENCE; SELECTION, GENETIC; SEQUENCE HOMOLOGY, NUCLEIC ACID;

EID: 79959828354     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0021808     Document Type: Article

References (42)

1. Lynch HT, Lynch J, Shaw T, Lubinski J, (2003) HNPCC (Lynch Syndrome): Differential Diagnosis, Molecular Genetics and Management - a Review. Hereditary Cancer in Clincial Practice 1: 7-18.
2. Fishel R, Kolodner RD, (1995) Identification of mismatch repair genes and their role in the development of cancer. Curr Opin Genet Dev 5: 382-395.
3. Jiricny J, (2006) The multifaceted mismatch-repair system. Nat Rev Mol Cell Biol 7: 335-346.
4. Lobo NA, Shimono Y, Qian D, Clarke MF, (2007) The biology of cancer stem cells. Annu Rev Cell Dev Biol 23: 675-699.
5. Pardal R, Clarke MF, Morrison SJ, (2003) Applying the principles of stem-cell biology to cancer. Nat Rev Cancer 3: 895-902.
6. Sanchez Alvarado A, Newmark PA, (1999) Double-stranded RNA specifically disrupts gene expression during planarian regeneration. Proc Natl Acad Sci USA 96: 5049-5054.
7. Reddien PW, Sánchez Alvarado A, (2004) Fundamentals of planarian regeneration. Annu Rev Cell Dev Biol 20: 725-757.
8. Peltomäki P, Vasen HF, (1997) Mutations predisposing to hereditary nonpolyposis colorectal cancer: database and results of a collaborative study. The International Collaborative Group on Hereditary Nonpolyposis Colorectal Cancer. Gastroenterology 113: 1146-1158.
9. Hsieh P, Yamane K, (2008) DNA mismatch repair: Molecular mechanism, cancer, and ageing. Mechanisms of Ageing and Development 129: 391-407.
10. Stojic L, Brun R, Jiricny J, (2004) Mismatch repair and DNA damage signalling. DNA Repair 3: 1091-1101.
11. Robb S, Ross E, Sánchez Alvarado A, (2007) SmedGD: the Schmidtea mediterranea genome database. Nucleic Acids Res 36: D599-606.
12. Gertz EM, Yu Y-K, Agarwala R, Schaffer A, Altschul S, (2006) Composition-based statistics and translated nucleotide searches: Improving the TBLASTN module of BLAST. BMC Biology 4: 41.
13. Ashburner M, Ball C, Blake J, Botstein D, Butler H, et al. (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25: 25-29.
14. Reddien PW, Oviedo NJ, Jennings JR, Jenkin JC, Sánchez Alvarado A, (2005) SMEDWI-2 is a PIWI-like protein that regulates planarian stem cells. Science 310: 1327-1330.
15. Orii H, Sakurai T, Watanabe K, (2005) Distribution of the stem cells (neoblasts) in the planarian Dugesia japonica. Dev Genes Evol 215: 143-157.
16. Eisenhoffer GT, Kang H, Alvarado AS, (2008) Molecular analysis of stem cells and their descendants during cell turnover and regeneration in the planarian Schmidtea mediterranea. Cell Stem Cell 3: 327-339.
17. Hayashi T, Asami M, Higuchi S, Shibata N, Agata K, (2006) Isolation of planarian X-ray-sensitive stem cells by fluorescence-activated cell sorting. Dev Growth Differ 48: 371-380.
18. Newmark PA, Reddien PW, Cebrià F, Sánchez Alvarado A, (2003) Ingestion of bacterially expressed double-stranded RNA inhibits gene expression in planarians. Proc Natl Acad Sci U S A 100 (Suppl 1): 11861-11865.
19. Mette Handberg-Thorsager EF, Emili Salo, (2008) Stem cells and regeneration in planarians. Frontiers Bioscience 13: 6374-6394.
20. Edelmann L, Edelmann W, (2004) Loss of DNA mismatch repair function and cancer predisposition in the mouse: animal models for human hereditary nonpolyposis colorectal cancer. Am J Med Genet C Semin Med Genet 129: 91-99.
21. de Wind N, Dekker M, van Rossum A, van der Valk M, te Riele H, (1998) Mouse models for hereditary nonpolyposis colorectal cancer. Cancer Res 58: 248-255.
22. Mastrocola AS, Heinen CD, (2010) Lynch syndrome-associated mutations in MSH2 alter DNA repair and checkpoint response functions in vivo. Hum Mutat 31: E1699-1708.
23. Stojic L, Mojas N, Cejka P, Di Pietro M, Ferrari S, et al. (2004) Mismatch repair-dependent G2 checkpoint induced by low doses of SN1 type methylating agents requires the ATR kinase. Genes Dev 18: 1331-1344.
24. Toft NJ, Winton DJ, Kelly J, Howard LA, Dekker M, et al. (1999) Msh2 status modulates both apoptosis and mutation frequency in the murine small intestine. Proc Natl Acad Sci U S A 96: 3911-3915.
25. Zhang H, Richards B, Wilson T, Lloyd M, Cranston A, et al. (1999) Apoptosis induced by overexpression of hMSH2 or hMLH1. Cancer Res 59: 3021-3027.
26. Wyatt MD, Pittman DL, (2006) Methylating Agents and DNA Repair Responses: Methylated Bases and Sources of Strand Breaks. Chemical Research in Toxicology 19: 1580-1594.
27. Hendzel MJ, Wei Y, Mancini MA, Van Hooser A, Ranalli T, et al. (1997) Mitosis-specific phosphorylation of histone H3 initiates primarily within pericentromeric heterochromatin during G2 and spreads in an ordered fashion coincident with mitotic chromosome condensation. Chromosoma 106: 348-360.
28. Bartkova J, Horejsí Z, Koed K, Krämer A, Tort F, et al. (2005) DNA damage response as a candidate anti-cancer barrier in early human tumorigenesis. Nature 434: 864-870.
29. Gorgoulis VG, Vassiliou L-VF, Karakaidos P, Zacharatos P, Kotsinas A, et al. (2005) Activation of the DNA damage checkpoint and genomic instability in human precancerous lesions. Nature 434: 907-913.
30. Lin DP, Wang Y, Scherer SJ, Clark AB, Yang K, et al. (2004) An Msh2 point mutation uncouples DNA mismatch repair and apoptosis. Cancer Res 64: 517-522.
31. Yang G, Scherer SJ, Shell SS, Yang K, Kim M, et al. (2004) Dominant effects of an Msh6 missense mutation on DNA repair and cancer susceptibility. Cancer Cell 6: 139-150.
32. Heinen CD, Schmutte C, Fishel R, (2002) DNA repair and tumorigenesis: lessons from hereditary cancer syndromes. Cancer Biol Ther 1: 477-485.
33. Stojic L, P C, Jiricny J, (2005) High doses of SN1 type methylating agents activate DNA damage signaling cascades that are largely independent of mismatch repair. Cell Cycle 4: 473-477.
34. Foster JA, (1963) Induction of Neoplasms in Planarians with Carcinogens. Cancer Res 23: 300-303.
35. Newmark PA, Alvarado AS, (2002) Not your father's planarian: a classic model enters the era of functional genomics. Nat Rev Genetics 3: 210-219.
36. Oviedo NJ, Nicolas CL, Adams DS, Levin M, (2008) Planarians: A Versatile and Powerful Model System for Molecular Studies of Regeneration, Adult Stem Cell Regulation, Aging, and Behavior. Cold Spring Harbor Protocols 2008.
37. Langmead B, Trapnell C, Pop M, Salzberg S, (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.
38. Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, et al. (2010) Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotech 28: 511-515.
39. Lu Y, Smielewska M, Palakodeti D, Lovci M, Aigner S, et al. (2009) Deep sequencing identifies new and regulated microRNAs in Schmidtea mediterranea. RNA 15: 1483-1491.
40. Reddien PW, Bermange AL, Murfitt KJ, Jennings JR, Sánchez Alvarado A, (2005) Identification of genes needed for regeneration, stem cell function, and tissue homeostasis by systematic gene perturbation in planaria. Dev Cell 8: 635-649.
41. Zayas RM, Hernández A, Habermann B, Wang Y, Stary JM, et al. (2005) The planarian Schmidtea mediterranea as a model for epigenetic germ cell specification: analysis of ESTs from the hermaphroditic strain. Proc Natl Acad Sci USA 102: 18491-18496.
42. Pearson BJ, Eisenhoffer GT, Gurley KA, Rink JC, Miller DE, et al. (2009) Formaldehyde-based whole-mount in situ hybridization method for planarians. Dev Dyn 238: 443-450.