Yeast mismatch repair components are required for stable inheritance of gene silencing


Autoři: Qian Liu aff001;  Xuefeng Zhu aff002;  Michelle Lindström aff001;  Yonghong Shi aff002;  Ju Zheng aff001;  Xinxin Hao aff001;  Claes M. Gustafsson aff002;  Beidong Liu aff001
Působiště autorů: Department of Chemistry and Molecular Biology, University of Gothenburg, Medicinaregatan, Goteborg, Sweden aff001;  Institute of Biomedicine, University of Gothenburg, Goteborg, Sweden aff002;  Department of Biology, Functional Biology, KU Leuven, Heverlee, Belgium aff003;  Center for Large-scale cell-based screening, Faculty of Science, University of Gothenburg, Medicinaregatan, Goteborg, Sweden aff004
Vyšlo v časopise: Yeast mismatch repair components are required for stable inheritance of gene silencing. PLoS Genet 16(5): e32767. doi:10.1371/journal.pgen.1008798
Kategorie: Research Article
doi: 10.1371/journal.pgen.1008798

Souhrn

Alterations in epigenetic silencing have been associated with ageing and tumour formation. Although substantial efforts have been made towards understanding the mechanisms of gene silencing, novel regulators in this process remain to be identified. To systematically search for components governing epigenetic silencing, we developed a genome-wide silencing screen for yeast (Saccharomyces cerevisiae) silent mating type locus HMR. Unexpectedly, the screen identified the mismatch repair (MMR) components Pms1, Mlh1, and Msh2 as being required for silencing at this locus. We further found that the identified genes were also required for proper silencing in telomeres. More intriguingly, the MMR mutants caused a redistribution of Sir2 deacetylase, from silent mating type loci and telomeres to rDNA regions. As a consequence, acetylation levels at histone positions H3K14, H3K56, and H4K16 were increased at silent mating type loci and telomeres but were decreased in rDNA regions. Moreover, knockdown of MMR components in human HEK293T cells increased subtelomeric DUX4 gene expression. Our work reveals that MMR components are required for stable inheritance of gene silencing patterns and establishes a link between the MMR machinery and the control of epigenetic silencing.

Klíčová slova:

Deletion mutagenesis – Epigenetics – Gene silencing – Genetic loci – Phenotypes – Small interfering RNAs – Telomeres – Yeast


Zdroje

1. Gong C, Qu S, Lv XB, Liu B, Tan W, Nie Y, et al. BRMS1L suppresses breast cancer metastasis by inducing epigenetic silence of FZD10. Nat Commun. 2014;5:5406. doi: 10.1038/ncomms6406 25406648.

2. Jones PA, Baylin SB. The epigenomics of cancer. Cell. 2007;128(4):683–92. Epub 2007/02/27. S0092-8674(07)00127-4 [pii] doi: 10.1016/j.cell.2007.01.029 17320506; PubMed Central PMCID: PMC3894624.

3. Ronsch K, Jagle S, Rose K, Seidl M, Baumgartner F, Freihen V, et al. SNAIL1 combines competitive displacement of ASCL2 and epigenetic mechanisms to rapidly silence the EPHB3 tumor suppressor in colorectal cancer. Mol Oncol. 2015;9(2):335–54. doi: 10.1016/j.molonc.2014.08.016 25277775.

4. Fox CA, McConnell KH. Toward biochemical understanding of a transcriptionally silenced chromosomal domain in Saccharomyces cerevisiae. Journal of Biological Chemistry. 2005;280(10):8629–32. doi: 10.1074/jbc.R400033200 15623501

5. Guarente L. Sirtuins and calorie restriction. Nature reviews Molecular cell biology. 2012;13(4):207–.

6. Moretti P, Freeman K, Coodly L, Shore D. Evidence that a complex of SIR proteins interacts with the silencer and telomere-binding protein RAP1. Genes & Development. 1994;8(19):2257–69. doi: 10.1101/gad.8.19.2257 7958893

7. Pirrotta V, Gross DS. Epigenetic silencing mechanisms in budding yeast and fruit fly: different paths, same destinations. Mol Cell. 2005;18(4):395–8. doi: 10.1016/j.molcel.2005.04.013 15893722.

8. Gotta M, Laroche T, Formenton A, Maillet L, Scherthan H, Gasser SM. The clustering of telomeres and colocalization with Rap1, Sir3, and Sir4 proteins in wild-type Saccharomyces cerevisiae. J Cell Biol. 1996;134(6):1349–63. doi: 10.1083/jcb.134.6.1349 8830766; PubMed Central PMCID: PMC2121006.

9. Cockell M, Palladino F, Laroche T, Kyrion G, Liu C, Lustig AJ, et al. The carboxy termini of Sir4 and Rap1 affect Sir3 localization: evidence for a multicomponent complex required for yeast telomeric silencing. J Cell Biol. 1995;129(4):909–24. doi: 10.1083/jcb.129.4.909 7744964; PubMed Central PMCID: PMC2120499.

10. Huang Y. Transcriptional silencing in Saccharomyces cerevisiae and Schizosaccharomyces pombe. Nucleic Acids Research. 2002;30(7):1465–82. doi: 10.1093/nar/30.7.1465 WOS:000174654200002. 11917007

11. Imai S, Armstrong CM, Kaeberlein M, Guarente L. Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature. 2000;403(6771):795–800. WOS:000085423100058. doi: 10.1038/35001622 10693811

12. Rusche LN, Kirchmaier AL, Rine J. The establishment, inheritance, and function of silenced chromatin in Saccharomyces cerevisiae. Annual Review of Biochemistry. 2003;72:481–516. doi: 10.1146/annurev.biochem.72.121801.161547 WOS:000185092500016. 12676793

13. Rine J, Strathern JN, Hicks JB, Herskowitz I. A suppressor of mating-type locus mutations in Saccharomyces cerevisiae: evidence for and identification of cryptic mating-type loci. Genetics. 1979;93(4):877–901. 397913

14. Rine J, Herskowitz I. Four genes responsible for a position effect on expression from HML and HMR in Saccharomyces cerevisiae. Genetics. 1987;116(1):9–22. 3297920

15. Loo S, Laurenson P, Foss M, Dillin A, Rine J. Roles of ABF1, NPL3, and YCL54 in silencing in Saccharomyces cerevisiae. Genetics. 1995;141(3):889–902. 8582634; PubMed Central PMCID: PMC1206852.

16. Tong AHY, Lesage G, Bader GD, Ding H, Xu H, Xin X, et al. Global Mapping of the Yeast Genetic Interaction Network. Science. 2004;303(5659):808–13. doi: 10.1126/science.1091317 14764870

17. Tong AH, Evangelista M, Parsons AB, Xu H, Bader GD, Page N, et al. Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science. 2001;294(5550):2364–8. doi: 10.1126/science.1065810 11743205.

18. Pillus L, Rine J. Epigenetic inheritance of transcriptional states in S. cerevisiae. Cell. 1989;59(4):637–47. doi: 10.1016/0092-8674(89)90009-3 2684414

19. Goellner EM, Smith CE, Campbell CS, Hombauer H, Desai A, Putnam CD, et al. PCNA and Msh2-Msh6 activate an Mlh1-Pms1 endonuclease pathway required for Exo1-independent mismatch repair. Mol Cell. 2014;55(2):291–304. doi: 10.1016/j.molcel.2014.04.034 24981171; PubMed Central PMCID: PMC4113420.

20. Leite M, Corso G, Sousa S, Milanezi F, Afonso LP, Henrique R, et al. MSI phenotype and MMR alterations in familial and sporadic gastric cancer. Int J Cancer. 2011;128(7):1606–13. doi: 10.1002/ijc.25495 20533283.

21. Hirai Y, Banno K, Suzuki M, Ichikawa Y, Udagawa Y, Sugano K, et al. Molecular epidemiological and mutational analysis of DNA mismatch repair (MMR) genes in endometrial cancer patients with HNPCC-associated familial predisposition to cancer. Cancer Sci. 2008;99(9):1715–9. doi: 10.1111/j.1349-7006.2008.00886.x 18624996.

22. Avdievich E, Reiss C, Scherer SJ, Zhang Y, Maier SM, Jin B, et al. Distinct effects of the recurrent Mlh1G67R mutation on MMR functions, cancer, and meiosis. Proc Natl Acad Sci U S A. 2008;105(11):4247–52. doi: 10.1073/pnas.0800276105 18337503; PubMed Central PMCID: PMC2393764.

23. Costanzo M, VanderSluis B, Koch EN, Baryshnikova A, Pons C, Tan G, et al. A global genetic interaction network maps a wiring diagram of cellular function. Science. 2016;353(6306). doi: 10.1126/science.aaf1420 27708008.

24. Liu B, Larsson L, Caballero A, Hao X, Öling D, Grantham J, et al. The Polarisome Is Required for Segregation and Retrograde Transport of Protein Aggregates. Cell. 2010;140(2):257–67. doi: 10.1016/j.cell.2009.12.031 WOS:000273826500016. 20141839

25. Bitterman KJ, Anderson RM, Cohen HY, Latorre-Esteves M, Sinclair DA. Inhibition of silencing and accelerated aging by nicotinamide, a putative negative regulator of yeast sir2 and human SIRT1. J Biol Chem. 2002;277(47):45099–107. doi: 10.1074/jbc.M205670200 12297502.

26. Gallo CM, Smith DL Jr., Smith JS. Nicotinamide clearance by Pnc1 directly regulates Sir2-mediated silencing and longevity. Mol Cell Biol. 2004;24(3):1301–12. doi: 10.1128/mcb.24.3.1301-1312.2004 14729974; PubMed Central PMCID: PMC321434.

27. Breitkreutz BJ, Stark C, Reguly T, Boucher L, Breitkreutz A, Livstone M, et al. The BioGRID Interaction Database: 2008 update. Nucleic Acids Res. 2008;36(Database issue):D637–40. doi: 10.1093/nar/gkm1001 18000002.

28. Johnson RE, Kovvali GK, Prakash L, Prakash S. Requirement of the yeast MSH3 and MSH6 genes for MSH2-dependent genomic stability. J Biol Chem. 1996;271(13):7285–8. doi: 10.1074/jbc.271.13.7285 8631743.

29. Supek F, Lehner B. Differential DNA mismatch repair underlies mutation rate variation across the human genome. Nature. 2015;521(7550):81–4. doi: 10.1038/nature14173 25707793; PubMed Central PMCID: PMC4425546.

30. Rodriguez GP, Romanova NV, Bao G, Rouf NC, Kow YW, Crouse GF. Mismatch repair-dependent mutagenesis in nondividing cells. Proc Natl Acad Sci U S A. 2012;109(16):6153–8. doi: 10.1073/pnas.1115361109 22474380; PubMed Central PMCID: PMC3341054.

31. Serero A, Jubin C, Loeillet S, Legoix-Ne P, Nicolas AG. Mutational landscape of yeast mutator strains. Proc Natl Acad Sci U S A. 2014;111(5):1897–902. doi: 10.1073/pnas.1314423111 24449905; PubMed Central PMCID: PMC3918763.

32. Anderson MZ, Gerstein AC, Wigen L, Baller JA, Berman J. Silencing is noisy: population and cell level noise in telomere-adjacent genes is dependent on telomere position and sir2. PLoS Genet. 2014;10(7):e1004436. doi: 10.1371/journal.pgen.1004436 25057900; PubMed Central PMCID: PMC4109849.

33. Hou Z, Bernstein DA, Fox CA, Keck JL. Structural basis of the Sir1-origin recognition complex interaction in transcriptional silencing. Proc Natl Acad Sci U S A. 2005;102(24):8489–94. doi: 10.1073/pnas.0503525102 15932939; PubMed Central PMCID: PMC1150864.

34. Gottschling DE, Aparicio OM, Billington BL, Zakian VA. Position effect at S. cerevisiae telomeres: Reversible repression of Pol II transcription. Cell. 1990;63(4):751–62. doi: 10.1016/0092-8674(90)90141-z 2225075

35. Bühler M, Gasser SM. Silent chromatin at the middle and ends: lessons from yeasts. The EMBO Journal. 2009;28(15):2149–61. doi: 10.1038/emboj.2009.185 19629038

36. Tham W-H, Zakian VA. Transcriptional silencing at Saccharomyces telomeres: implications for other organisms. Oncogene. 2002;21(4):512–21. doi: 10.1038/sj.onc.1205078 11850776

37. Mondoux MA, Zakian VA. Subtelomeric Elements Influence But Do Not Determine Silencing Levels at Saccharomyces cerevisiae Telomeres. Genetics. 2007;177(4):2541–6. doi: 10.1534/genetics.107.079806 18073447

38. Chien CT, Buck S, Sternglanz R, Shore D. Targeting of SIR1 protein establishes transcriptional silencing at HM loci and telomeres in yeast. Cell. 1993;75(3):531–41. doi: 10.1016/0092-8674(93)90387-6 8221892.

39. Rusche LN, Kirchmaier AL, Rine J. Ordered nucleation and spreading of silenced chromatin in Saccharomyces cerevisiae. Mol Biol Cell. 2002;13(7):2207–22. doi: 10.1091/mbc.e02-03-0175 12134062; PubMed Central PMCID: PMC117306.

40. Triolo T, Sternglanz R. Role of interactions between the origin recognition complex and SIR1 in transcriptional silencing. Nature. 1996;381(6579):251–3. doi: 10.1038/381251a0 8622770.

41. Iglesias N, Redon S, Pfeiffer V, Dees M, Lingner J, Luke B. Subtelomeric repetitive elements determine TERRA regulation by Rap1/Rif and Rap1/Sir complexes in yeast. EMBO Rep. 2011;12(6):587–93. doi: 10.1038/embor.2011.73 21525956; PubMed Central PMCID: PMC3128280.

42. Smith JA, Bannister LA, Bhattacharjee V, Wang Y, Waldman BC, Waldman AS. Accurate homologous recombination is a prominent double-strand break repair pathway in mammalian chromosomes and is modulated by mismatch repair protein Msh2. Mol Cell Biol. 2007;27(22):7816–27. doi: 10.1128/MCB.00455-07 17846123; PubMed Central PMCID: PMC2169143.

43. Nowosielska A, Marinus MG. DNA mismatch repair-induced double-strand breaks. DNA Repair (Amst). 2008;7(1):48–56. doi: 10.1016/j.dnarep.2007.07.015 17827074; PubMed Central PMCID: PMC2175267.

44. Surtees JA, Alani E. Mismatch repair factor MSH2-MSH3 binds and alters the conformation of branched DNA structures predicted to form during genetic recombination. J Mol Biol. 2006;360(3):523–36. doi: 10.1016/j.jmb.2006.05.032 16781730.

45. Elliott B, Jasin M. Repair of double-strand breaks by homologous recombination in mismatch repair-defective mammalian cells. Mol Cell Biol. 2001;21(8):2671–82. doi: 10.1128/MCB.21.8.2671-2682.2001 11283247; PubMed Central PMCID: PMC86898.

46. Habraken Y, Jolois O, Piette J. Differential involvement of the hMRE11/hRAD50/NBS1 complex, BRCA1 and MLH1 in NF-kappaB activation by camptothecin and X-ray. Oncogene. 2003;22(38):6090–9. doi: 10.1038/sj.onc.1206893 12955088.

47. Sugawara N, Pâques F, Colaiácovo M, Haber JE. Role of Saccharomyces cerevisiae Msh2 and Msh3 repair proteins in double-strand break-induced recombination. Proceedings of the National Academy of Sciences. 1997;94(17):9214–9. doi: 10.1073/pnas.94.17.9214 9256462

48. Martin SG, Laroche T, Suka N, Grunstein M, Gasser SM. Relocalization of telomeric Ku and SIR proteins in response to DNA strand breaks in yeast. Cell. 1999;97(5):621–33. doi: 10.1016/s0092-8674(00)80773-4 10367891.

49. McAinsh AD, Scott-Drew S, Murray JA, Jackson SP. DNA damage triggers disruption of telomeric silencing and Mec1p-dependent relocation of Sir3p. Curr Biol. 1999;9(17):963–6. doi: 10.1016/s0960-9822(99)80424-2 10508591.

50. Larcher MV, Pasquier E, MacDonald RS, Wellinger RJ. Ku Binding on Telomeres Occurs at Sites Distal from the Physical Chromosome Ends. PLoS Genet. 2016;12(12):e1006479. doi: 10.1371/journal.pgen.1006479 27930670; PubMed Central PMCID: PMC5145143.

51. Kitada T, Kuryan BG, Tran NN, Song C, Xue Y, Carey M, et al. Mechanism for epigenetic variegation of gene expression at yeast telomeric heterochromatin. Genes Dev. 2012;26(21):2443–55. doi: 10.1101/gad.201095.112 23124068; PubMed Central PMCID: PMC3490002.

52. Huang J, Moazed D. Association of the RENT complex with nontranscribed and coding regions of rDNA and a regional requirement for the replication fork block protein Fob1 in rDNA silencing. Genes Dev. 2003;17(17):2162–76. doi: 10.1101/gad.1108403 12923057; PubMed Central PMCID: PMC196457.

53. Machin F, Paschos K, Jarmuz A, Torres-Rosell J, Pade C, Aragon L. Condensin regulates rDNA silencing by modulating nucleolar Sir2p. Curr Biol. 2004;14(2):125–30. 14738734.

54. Straight AF, Shou W, Dowd GJ, Turck CW, Deshaies RJ, Johnson AD, et al. Net1, a Sir2-associated nucleolar protein required for rDNA silencing and nucleolar integrity. Cell. 1999;97(2):245–56. doi: 10.1016/s0092-8674(00)80734-5 10219245.

55. Li YC, Cheng TH, Gartenberg MR. Establishment of transcriptional silencing in the absence of DNA replication. Science. 2001;291(5504):650–3. doi: 10.1126/science.291.5504.650 11158677.

56. Straatman KR, Louis EJ. Localization of telomeres and telomere-associated proteins in telomerase-negative Saccharomyces cerevisiae. Chromosome Research. 2007;15(8):1033. doi: 10.1007/s10577-007-1178-2 18075778

57. Matecic M, Martins-Taylor K, Hickman M, Tanny J, Moazed D, Holmes SG. New alleles of SIR2 define cell-cycle-specific silencing functions. Genetics. 2006;173(4):1939–50. doi: 10.1534/genetics.106.055491 16783021; PubMed Central PMCID: PMC1569706.

58. Lau A, Blitzblau H, Bell SP. Cell-cycle control of the establishment of mating-type silencing in S. cerevisiae. Genes Dev. 2002;16(22):2935–45. doi: 10.1101/gad.764102 12435634; PubMed Central PMCID: PMC187485.

59. Kirchmaier AL, Rine J. Cell cycle requirements in assembling silent chromatin in Saccharomyces cerevisiae. Mol Cell Biol. 2006;26(3):852–62. doi: 10.1128/MCB.26.3.852-862.2006 16428441; PubMed Central PMCID: PMC1347038.

60. Simon I, Barnett J, Hannett N, Harbison CT, Rinaldi NJ, Volkert TL, et al. Serial regulation of transcriptional regulators in the yeast cell cycle. Cell. 2001;106(6):697–708. doi: 10.1016/s0092-8674(01)00494-9 11572776.

61. Gotta M, Strahl-Bolsinger S, Renauld H, Laroche T, Kennedy BK, Grunstein M, et al. Localization of Sir2p: the nucleolus as a compartment for silent information regulators. EMBO J. 1997;16(11):3243–55. doi: 10.1093/emboj/16.11.3243 9214640; PubMed Central PMCID: PMC1169941.

62. Huh WK, Falvo JV, Gerke LC, Carroll AS, Howson RW, Weissman JS, et al. Global analysis of protein localization in budding yeast. Nature. 2003;425(6959):686–91. doi: 10.1038/nature02026 14562095.

63. Ha CW, Huh WK. Rapamycin increases rDNA stability by enhancing association of Sir2 with rDNA in Saccharomyces cerevisiae. Nucleic Acids Res. 2011;39(4):1336–50. doi: 10.1093/nar/gkq895 20947565; PubMed Central PMCID: PMC3045593.

64. Oppikofer M, Kueng S, Martino F, Soeroes S, Hancock SM, Chin JW, et al. A dual role of H4K16 acetylation in the establishment of yeast silent chromatin. EMBO J. 2011;30(13):2610–21. doi: 10.1038/emboj.2011.170 21666601; PubMed Central PMCID: PMC3155304.

65. Johnson A, Li G, Sikorski TW, Buratowski S, Woodcock CL, Moazed D. Reconstitution of heterochromatin-dependent transcriptional gene silencing. Mol Cell. 2009;35(6):769–81. doi: 10.1016/j.molcel.2009.07.030 19782027; PubMed Central PMCID: PMC2842978.

66. Das C, Lucia MS, Hansen KC, Tyler JK. CBP/p300-mediated acetylation of histone H3 on lysine 56. Nature. 2009;459(7243):113–7. doi: 10.1038/nature07861 19270680; PubMed Central PMCID: PMC2756583.

67. Schwer B, Schumacher B, Lombard DB, Xiao C, Kurtev MV, Gao J, et al. Neural sirtuin 6 (Sirt6) ablation attenuates somatic growth and causes obesity. Proc Natl Acad Sci U S A. 2010;107(50):21790–4. doi: 10.1073/pnas.1016306107 21098266; PubMed Central PMCID: PMC3003110.

68. Alper BJ, Job G, Yadav RK, Shanker S, Lowe BR, Partridge JF. Sir2 is required for Clr4 to initiate centromeric heterochromatin assembly in fission yeast. EMBO J. 2013;32(17):2321–35. doi: 10.1038/emboj.2013.143 23771057; PubMed Central PMCID: PMC3770337.

69. Stadler G, Rahimov F, King OD, Chen JC, Robin JD, Wagner KR, et al. Telomere position effect regulates DUX4 in human facioscapulohumeral muscular dystrophy. Nat Struct Mol Biol. 2013;20(6):671–8. doi: 10.1038/nsmb.2571 23644600; PubMed Central PMCID: PMC3711615.

70. Nielsen SV, Stein A, Dinitzen AB, Papaleo E, Tatham MH, Poulsen EG, et al. Predicting the impact of Lynch syndrome-causing missense mutations from structural calculations. PLOS Genetics. 2017;13(4):e1006739. doi: 10.1371/journal.pgen.1006739 28422960

71. Huang S, Zhou H, Katzmann D, Hochstrasser M, Atanasova E, Zhang Z. Rtt106p is a histone chaperone involved in heterochromatin-mediated silencing. Proceedings of the National Academy of Sciences of the United States of America. 2005;102(38):13410–5. doi: 10.1073/pnas.0506176102 16157874

72. Miller AM, Nasmyth KA. Role of DNA replication in the repression of silent mating type loci in yeast. Nature. 1984;312(5991):247–51. doi: 10.1038/312247a0 6390211.

73. Rivier DH, Rine J. An origin of DNA replication and a transcription silencer require a common element. Science. 1992;256(5057):659–63. doi: 10.1126/science.1585179 1585179.

74. Bell SP, Kobayashi R, Stillman B. Yeast origin recognition complex functions in transcription silencing and DNA replication. Science. 1993;262(5141):1844–9. doi: 10.1126/science.8266072 8266072.

75. Foss M, McNally FJ, Laurenson P, Rine J. Origin recognition complex (ORC) in transcriptional silencing and DNA replication in S. cerevisiae. Science. 1993;262(5141):1838–44. doi: 10.1126/science.8266071 8266071.

76. Li JJ, Herskowitz I. Isolation of ORC6, a component of the yeast origin recognition complex by a one-hybrid system. Science. 1993;262(5141):1870–4. doi: 10.1126/science.8266075 8266075.

77. Douglas NL, Dozier SK, Donato JJ. Dual roles for Mcm10 in DNA replication initiation and silencing at the mating-type loci. Mol Biol Rep. 2005;32(4):197–204. doi: 10.1007/s11033-005-2312-x 16328881.

78. Singh J, Goel V, Klar AJ. A novel function of the DNA repair gene rhp6 in mating-type silencing by chromatin remodeling in fission yeast. Mol Cell Biol. 1998;18(9):5511–22. doi: 10.1128/mcb.18.9.5511 9710635; PubMed Central PMCID: PMC109136.

79. Liu J, Ren X, Yin H, Wang Y, Xia R, Wang Y, et al. Mutation in the catalytic subunit of DNA polymerase alpha influences transcriptional gene silencing and homologous recombination in Arabidopsis. Plant J. 2010;61(1):36–45. doi: 10.1111/j.1365-313X.2009.04026.x 19769574.

80. Hombauer H, Campbell CS, Smith CE, Desai A, Kolodner RD. Visualization of eukaryotic DNA mismatch repair reveals distinct recognition and repair intermediates. Cell. 2011;147(5):1040–53. doi: 10.1016/j.cell.2011.10.025 22118461; PubMed Central PMCID: PMC3478091.

81. Bishop DK, Williamson MS, Fogel S, Kolodner RD. The role of heteroduplex correction in gene conversion in Saccharomyces cerevisiae. Nature. 1987;328(6128):362–4. doi: 10.1038/328362a0 3299108

82. Kunkel TA, Erie DA. DNA MISMATCH REPAIR. Annual Review of Biochemistry. 2005;74(1):681–710. doi: 10.1146/annurev.biochem.74.082803.133243 15952900.

83. Yu S, Owen-Hughes T, Friedberg EC, Waters R, Reed SH. The yeast Rad7/Rad16/Abf1 complex generates superhelical torsion in DNA that is required for nucleotide excision repair. DNA Repair. 2004;3(3):277–87. doi: 10.1016/j.dnarep.2003.11.004 15177043

84. Reed SH, Akiyama M, Stillman B, Friedberg EC. Yeast autonomously replicating sequence binding factor is involved in nucleotide excision repair. Genes & development. 1999;13(23):3052–8. doi: 10.1101/gad.13.23.3052 10601031.

85. Berera S, Koru-Sengul T, Miao F, Carrasquillo O, Nadji M, Zhang Y, et al. Colorectal Tumors From Different Racial and Ethnic Minorities Have Similar Rates of Mismatch Repair Deficiency. Clin Gastroenterol Hepatol. 2016;14(8):1163–71. doi: 10.1016/j.cgh.2016.03.037 27046481.

86. Lamba AR, Moore AY, Moore T, Rhees J, Arnold MA, Boland CR. Defective DNA mismatch repair activity is common in sebaceous neoplasms, and may be an ineffective approach to screen for Lynch syndrome. Fam Cancer. 2015;14(2):259–64. doi: 10.1007/s10689-015-9782-3 25637498.

87. Nguyen A, Bougeard G, Koob M, Chenard MP, Schneider A, Maugard C, et al. MSI detection and its pitfalls in CMMRD syndrome in a family with a bi-allelic MLH1 mutation. Fam Cancer. 2016. doi: 10.1007/s10689-016-9894-4 27017609.

88. Murphy MA, Wentzensen N. Frequency of mismatch repair deficiency in ovarian cancer: a systematic review This article is a US Government work and, as such, is in the public domain of the United States of America. Int J Cancer. 2011;129(8):1914–22. doi: 10.1002/ijc.25835 21140452; PubMed Central PMCID: PMC3107885.

89. Carethers JM, Stoffel EM. Lynch syndrome and Lynch syndrome mimics: The growing complex landscape of hereditary colon cancer. World J Gastroenterol. 2015;21(31):9253–61. doi: 10.3748/wjg.v21.i31.9253 26309352; PubMed Central PMCID: PMC4541378.

90. Kucherlapati M, Nguyen A, Kuraguchi M, Yang K, Fan K, Bronson R, et al. Tumor progression in Apc(1638N) mice with Exo1 and Fen1 deficiencies. Oncogene. 2007;26(43):6297–306. doi: 10.1038/sj.onc.1210453 17452984.

91. Dixit M, Ansseau E, Tassin A, Winokur S, Shi R, Qian H, et al. DUX4, a candidate gene of facioscapulohumeral muscular dystrophy, encodes a transcriptional activator of PITX1. Proc Natl Acad Sci U S A. 2007;104(46):18157–62. doi: 10.1073/pnas.0708659104 17984056; PubMed Central PMCID: PMC2084313.

92. Snider L, Asawachaicharn A, Tyler AE, Geng LN, Petek LM, Maves L, et al. RNA transcripts, miRNA-sized fragments and proteins produced from D4Z4 units: new candidates for the pathophysiology of facioscapulohumeral dystrophy. Hum Mol Genet. 2009;18(13):2414–30. doi: 10.1093/hmg/ddp180 19359275; PubMed Central PMCID: PMC2694690.

93. Lemmers RJ, van der Vliet PJ, Klooster R, Sacconi S, Camano P, Dauwerse JG, et al. A unifying genetic model for facioscapulohumeral muscular dystrophy. Science. 2010;329(5999):1650–3. doi: 10.1126/science.1189044 20724583; PubMed Central PMCID: PMC4677822.

94. Kazakov V, Rudenko D, Schulev J, Pozdnyakov A. Unusual association of FSHD and extramedullary thoracic tumour in the same patient: a case report. Acta Myol. 2009;28(2):76–9. 20128141; PubMed Central PMCID: PMC2858950.

95. Yazici O, Aksoy S, Ozdemir N, Sendur MA, Dogan M, Zengin N. A rare coincidence: facioscapulohumeral muscular dystrophy and breast cancer. Exp Oncol. 2013;35(4):311–2. 24382443.

96. Wagih O, Usaj M, Baryshnikova A, VanderSluis B, Kuzmin E, Costanzo M, et al. SGAtools: one-stop analysis and visualization of array-based genetic interaction screens. Nucleic Acids Res. 2013;41(Web Server issue):W591–6. doi: 10.1093/nar/gkt400 23677617; PubMed Central PMCID: PMC3692131.

97. Ugolini S, Bruschi CV. The red/white colony color assay in the yeast Saccharomyces cerevisiae: epistatic growth advantage of white ade8-18, ade2 cells over red ade2 cells. Current Genetics. 1996;30(6):485–92. doi: 10.1007/s002940050160 8939809

98. Studamire B, Price G, Sugawara N, Haber JE, Alani E. Separation-of-function mutations in Saccharomyces cerevisiae MSH2 that confer mismatch repair defects but do not affect nonhomologous-tail removal during recombination. Molecular and cellular biology. 1999;19(11):7558–67. doi: 10.1128/mcb.19.11.7558 10523644.

99. Boyle EI, Weng S, Gollub J, Jin H, Botstein D, Cherry JM, et al. GO::TermFinder—open source software for accessing Gene Ontology information and finding significantly enriched Gene Ontology terms associated with a list of genes. Bioinformatics. 2004;20(18):3710–5. doi: 10.1093/bioinformatics/bth456 15297299

100. Breitkreutz B-J, Stark C, Tyers M. Osprey: a network visualization system. Genome Biology. 2003;4(3):R22. doi: 10.1186/gb-2003-4-3-r22 12620107

101. Zhu X, Wiren M, Sinha I, Rasmussen NN, Linder T, Holmberg S, et al. Genome-wide occupancy profile of mediator and the Srb8-11 module reveals interactions with coding regions. Mol Cell. 2006;22(2):169–78. doi: 10.1016/j.molcel.2006.03.032 16630887.

102. Teytelman L, Osborne Nishimura EA, Ozaydin B, Eisen MB, Rine J. The enigmatic conservation of a Rap1 binding site in the Saccharomyces cerevisiae HMR-E silencer. G3 (Bethesda). 2012;2(12):1555–62. doi: 10.1534/g3.112.004077 23275878; PubMed Central PMCID: PMC3516477.

103. Song J, Yang Q, Yang J, Larsson L, Hao X, Zhu X, et al. Essential Genetic Interactors of SIR2 Required for Spatial Sequestration and Asymmetrical Inheritance of Protein Aggregates. PLoS genetics. 2014;10(7):e1004539. doi: 10.1371/journal.pgen.1004539 25079602

Štítky
Genetika Reprodukční medicína

Článek vyšel v časopise

PLOS Genetics


2020 Číslo 5

Nejčtenější v tomto čísle

Tomuto tématu se dále věnují…


Kurzy Doporučená témata Časopisy
Přihlášení
Zapomenuté heslo

Nemáte účet?  Registrujte se

Zapomenuté heslo

Zadejte e-mailovou adresu se kterou jste vytvářel(a) účet, budou Vám na ni zaslány informace k nastavení nového hesla.

Přihlášení

Nemáte účet?  Registrujte se

VIRTUÁLNÍ ČEKÁRNA ČR Jste praktický lékař nebo pediatr? Zapojte se! Jste praktik nebo pediatr? Zapojte se!

×