Advertisement

Progeria and Genome Instability

  • Fanbiao Meng
  • Baohua Liu
  • Zhongjun ZhouEmail author

Abstract

Aging is a process of progressive decline in physiological functions. Cells and tissues in our body are constantly exposed to a variety of endogenous and exogenous assaults that cause, DNA damages. The accumulation of unrepaired/irreparable DNA damages results in a sustained DNA damage checkpoint response and induces cellular senescence, a permanent cell cycle arrest. Studies on human premature aging syndromes have suggested that accumulated damages might lead to exhaustion of resources that are required for replacement of the damaged tissues and thus accelerate aging. In this chapter, we summarize current knowledge on DNA damage repair machinery and evidence supporting the idea that defects in genomic maintenance are behind human premature aging syndromes. We put the emphasis on Hutchinson-Gilford Progeria Syndrome.

Keywords

Premature aging DNA damage Lamin A Progerin Chromatin remodeling Epigenetics 

Notes

Acknowledgments

B.L. is an Excellent Young Researcher of National Natural Science Foundation of China (81422016), an awardee of 1000-Young Talents Program (The Organization Department of the Communist Party of China Central Committee), and supported by the Major Research plan of NSFC (91439133). Works in Z.Z.’s laboratory are supported by a NSFC Key Project grant (81330009), a National Key Basic Research Program project (2011CB964700) from Ministry of Science and Technology of China, and a RGC grant (HKU2/CRF/13G) from Hong Kong SAR.

References

  1. Ayrapetov MK, Gursoy-Yuzugullu O, Xu C, Xu Y, Price BD (2014) DNA double-strand breaks promote methylation of histone H3 on lysine 9 and transient formation of repressive chromatin. Proc Natl Acad Sci 111:9169–9174PubMedCentralCrossRefPubMedGoogle Scholar
  2. Bakkenist CJ, Kastan MB (2003) DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 421:499–506CrossRefPubMedGoogle Scholar
  3. Balajee AS, Machwe A, May A, Gray MD, Oshima J, Martin GM, Nehlin JO, Brosh R, Orren DK, Bohr VA (1999) The Werner syndrome protein is involved in RNA polymerase II transcription. Mol Biol Cell 10:2655–2668PubMedCentralCrossRefPubMedGoogle Scholar
  4. Blasco MA (2007) Telomere length, stem cells and aging. Nat Chem Biol 3:640–649CrossRefPubMedGoogle Scholar
  5. Botuyan MV, Lee J, Ward IM, Kim J-E, Thompson JR, Chen J, Mer G (2006) Structural basis for the methylation state-specific recognition of histone H4-K20 by 53BP1 and Crb2 in DNA repair. Cell 127:1361–1373PubMedCentralCrossRefPubMedGoogle Scholar
  6. Brosh RM Jr, Orren DK, Nehlin JO, Ravn PH, Kenny MK, Machwe A, Bohr VA (1999) Functional and physical interaction between WRN helicase and human replication protein A. J Biol Chem 274:18341–18350CrossRefPubMedGoogle Scholar
  7. Brosh RM Jr, von Kobbe C, Sommers JA, Karmakar P, Opresko PL, Piotrowski J, Dianova I, Dianov GL, Bohr VA (2001) Werner syndrome protein interacts with human flap endonuclease 1 and stimulates its cleavage activity. Embo J 20:5791–5801PubMedCentralCrossRefPubMedGoogle Scholar
  8. Cao K, Blair CD, Faddah DA, Kieckhaefer JE, Olive M, Erdos MR, Nabel EG, Collins FS (2011) Progerin and telomere dysfunction collaborate to trigger cellular senescence in normal human fibroblasts. J Clin Invest 121:2833–2844PubMedCentralCrossRefPubMedGoogle Scholar
  9. Chen L, Lee L, Kudlow BA, Dos Santos HG, Sletvold O, Shafeghati Y, Botha EG, Garg A, Hanson NB, Martin GM et al (2003) LMNA mutations in atypical Werner’s syndrome. Lancet 362:440–445CrossRefPubMedGoogle Scholar
  10. Chester N, Kuo F, Kozak C, O’Hara CD, Leder P (1998) Stage-specific apoptosis, developmental delay, and embryonic lethality in mice homozygous for a targeted disruption in the murine Bloom’s syndrome gene. Genes Dev 12:3382–3393PubMedCentralCrossRefPubMedGoogle Scholar
  11. Cooper MP, Machwe A, Orren DK, Brosh RM, Ramsden D, Bohr VA (2000) Ku complex interacts with and stimulates the Werner protein. Genes Dev 14:907–912PubMedCentralPubMedGoogle Scholar
  12. Csoka AB, Cao H, Sammak PJ, Constantinescu D, Schatten GP, Hegele RA (2004) Novel lamin A/C gene (LMNA) mutations in atypical progeroid syndromes. J Med Genet 41:304–308PubMedCentralCrossRefPubMedGoogle Scholar
  13. Das C, Lucia MS, Hansen KC, Tyler JK (2009) CBP/p300-mediated acetylation of histone H3 on lysine 56. Nature 459:113–117PubMedCentralCrossRefPubMedGoogle Scholar
  14. Davey CA, Sargent DF, Luger K, Maeder AW, Richmond TJ (2002) Solvent mediated interactions in the structure of the nucleosome core particle at 1.9 Å resolution. J Mol Biol 319:1097–1113CrossRefPubMedGoogle Scholar
  15. Denecke J, Brune T, Feldhaus T, Robenek H, Kranz C, Auchus RJ, Agarwal AK, Marquardt T (2006) A homozygous ZMPSTE24 null mutation in combination with a heterozygous mutation in the LMNA gene causes Hutchinson-Gilford progeria syndrome (HGPS): insights into the pathophysiology of HGPS. Hum Mutat 27:524–531CrossRefPubMedGoogle Scholar
  16. DiGiovanna AG (2000) Human aging: biological perspectives. McGraw-Hill, New YorkGoogle Scholar
  17. Downs JA, Nussenzweig MC, Nussenzweig A (2007) Chromatin dynamics and the preservation of genetic information. Nature 447:951–958CrossRefPubMedGoogle Scholar
  18. Eriksson M, Brown WT, Gordon LB, Glynn MW, Singer J, Scott L, Erdos MR, Robbins CM, Moses TY, Berglund P et al (2003) Recurrent de novo point mutations in lamin A cause Hutchinson-Gilford progeria syndrome. Nature 423:293–298CrossRefPubMedGoogle Scholar
  19. Fernandez-Capetillo O, Lee A, Nussenzweig M, Nussenzweig A (2004) H2AX: the histone guardian of the genome. DNA Repair 3:959–967CrossRefPubMedGoogle Scholar
  20. Fleck O, Nielsen O (2004) DNA repair. J Cell Sci 117:515–517CrossRefPubMedGoogle Scholar
  21. Fong LG, Ng JK, Meta M, Cote N, Yang SH, Stewart CL, Sullivan T, Burghardt A, Majumdar S, Reue K et al (2004) Heterozygosity for Lmna deficiency eliminates the progeria-like phenotypes in Zmpste24-deficient mice. Proc Natl Acad Sci U S A 101:18111–18116PubMedCentralCrossRefPubMedGoogle Scholar
  22. Fujimura-Kamada K, Nouvet FJ, Michaelis S (1997) A novel membrane-associated metalloprotease, Ste24p, is required for the first step of NH2-terminal processing of the yeast a-factor precursor. J Cell Biol 136:271–285PubMedCentralCrossRefPubMedGoogle Scholar
  23. Fukuchi K, Katsuya T, Sugimoto K, Kuremura M, Kim HD, Li L, Ogihara T (2004) LMNA mutation in a 45 year old Japanese subject with Hutchinson-Gilford progeria syndrome. J Med Genet 41:e67PubMedCentralCrossRefPubMedGoogle Scholar
  24. Gordon LB, Rothman FG, López-Otín C, Misteli T (2013) Progeria: a paradigm for translational medicine. Cell 156:400–407CrossRefGoogle Scholar
  25. Gray MD, Shen JC, Kamath-Loeb AS, Blank A, Sopher BL, Martin GM, Oshima J, Loeb LA (1997) The Werner syndrome protein is a DNA helicase. Nat Genet 17:100–103CrossRefPubMedGoogle Scholar
  26. Guo G, Wang W, Bradley A (2004) Mismatch repair genes identified using genetic screens in Blm-deficient embryonic stem cells. Nature 429:891–895CrossRefPubMedGoogle Scholar
  27. Halliwell B, Whiteman M (2004) Measuring reactive species and oxidative damage in vivo and in cell culture: how should you do it and what do the results mean? Br J Pharmacol 142:231–255PubMedCentralCrossRefPubMedGoogle Scholar
  28. Harper JW, Elledge SJ (2007) The DNA damage response: ten years after. Mol Cell 28:739–745CrossRefPubMedGoogle Scholar
  29. Hasty P (2005) The impact of DNA damage, genetic mutation and cellular responses on cancer prevention, longevity and aging: observations in humans and mice. Mech Ageing Dev 126:71–77CrossRefPubMedGoogle Scholar
  30. Hay N, Sonenberg N (2004) Upstream and downstream of mTOR. Genes Dev 18:1926–1945CrossRefPubMedGoogle Scholar
  31. Hennekam RCM (2006) Hutchinson–Gilford progeria syndrome: review of the phenotype. Am J Med Genet A 140A:2603–2624CrossRefGoogle Scholar
  32. Herranz D, Munoz-Martin M, Canamero M, Mulero F, Martinez-Pastor B, Fernandez-Capetillo O, Serrano M (2010) Sirt1 improves healthy ageing and protects from metabolic syndrome-associated cancer. Nat Commun 1:3PubMedCentralCrossRefPubMedGoogle Scholar
  33. Hickson ID (2003) RecQ helicases: caretakers of the genome. Nat Rev Cancer 3:169–178CrossRefPubMedGoogle Scholar
  34. Hoeijmakers JH (2009) DNA damage, aging, and cancer. N Engl J Med 361:1475–1485CrossRefPubMedGoogle Scholar
  35. Houtkooper RH, Williams RW, Auwerx J (2010) Metabolic networks of longevity. Cell 142:9–14Google Scholar
  36. Huang S, Li B, Gray MD, Oshima J, Mian IS, Campisi J (1998) The premature ageing syndrome protein, WRN, is a 3′-->5′ exonuclease. Nat Genet 20:114–116CrossRefPubMedGoogle Scholar
  37. Iacovoni JS, Caron P, Lassadi I, Nicolas E, Massip L, Trouche D, Legube G (2010) High resolution profiling of γH2AX around DNA double strand breaks in the mammalian genome. EMBO J 29:1446–1457PubMedCentralCrossRefPubMedGoogle Scholar
  38. Johnson RD, Liu N, Jasin M (1999) Mammalian XRCC2 promotes the repair of DNA double-strand breaks by homologous recombination. Nature 401:397–399PubMedGoogle Scholar
  39. Kamath-Loeb AS, Loeb LA, Johansson E, Burgers PM, Fry M (2001) Interactions between the Werner syndrome helicase and DNA polymerase delta specifically facilitate copying of tetraplex and hairpin structures of the d(CGG)n trinucleotide repeat sequence. J Biol Chem 276:16439–16446CrossRefPubMedGoogle Scholar
  40. Kanfi Y, Naiman S, Amir G, Peshti V, Zinman G, Nahum L, Bar-Joseph Z, Cohen HY (2012) The sirtuin SIRT6 regulates lifespan in male mice. Nature 483:218–221CrossRefPubMedGoogle Scholar
  41. Karagiannis TC, El-Osta A (2007) Chromatin modifications and DNA double-strand breaks: the current state of play. Leukemia 21:195–200CrossRefPubMedGoogle Scholar
  42. Karmakar P, Piotrowski J, Brosh RM Jr, Sommers JA, Miller SP, Cheng WH, Snowden CM, Ramsden DA, Bohr VA (2002) Werner protein is a target of DNA-dependent protein kinase in vivo and in vitro, and its catalytic activities are regulated by phosphorylation. J Biol Chem 277:18291–18302CrossRefPubMedGoogle Scholar
  43. Kenyon C, Chang J, Gensch E, Rudner A, Tabtiang R (1993) A C. elegans mutant that lives twice as long as wild type. Nature 366:461–464CrossRefPubMedGoogle Scholar
  44. Klass MR (1983) A method for the isolation of longevity mutants in the nematode Caenorhabditis elegans and initial results. Mech Ageing Dev 22:279–286CrossRefPubMedGoogle Scholar
  45. Kops GJPL, Ruiter ND, De Vries-Smits AMM, Powell DR, Bos JL, Burgering BMT (1999) Direct control of the Forkhead transcription factor AFX by protein kinase B. Nature 398:630–634CrossRefPubMedGoogle Scholar
  46. Krishnan V, Chow MZY, Wang Z, Zhang L, Liu B, Liu X, Zhou Z (2011) Histone H4 lysine 16 hypoacetylation is associated with defective DNA repair and premature senescence in Zmpste24-deficient mice. Proc Natl Acad Sci 108:12325–12330PubMedCentralCrossRefPubMedGoogle Scholar
  47. Kusumoto-Matsuo R, Opresko PL, Ramsden D, Tahara H, Bohr VA (2010) Cooperation of DNA-PKcs and WRN helicase in the maintenance of telomeric D-loops. Aging 2:274–284PubMedCentralPubMedGoogle Scholar
  48. Lebel M, Spillare EA, Harris CC, Leder P (1999) The Werner syndrome gene product co-purifies with the DNA replication complex and interacts with PCNA and topoisomerase I. J Biol Chem 274:37795–37799CrossRefPubMedGoogle Scholar
  49. Lee JH, Paull TT (2004) Direct activation of the ATM protein kinase by the Mre11/Rad50/Nbs1 complex. Science 304:93–96CrossRefPubMedGoogle Scholar
  50. Levy N, Lopez-Otin C, Hennekam RC (2005) Defective prelamin A processing resulting from LMNA or ZMPSTE24 mutations as the cause of restrictive dermopathy. Arch Dermatol 141:1473–1474, author reply 1474CrossRefPubMedGoogle Scholar
  51. Li B, Comai L (2000) Functional interaction between Ku and the werner syndrome protein in DNA end processing. J Biol Chem 275:28349–28352CrossRefPubMedGoogle Scholar
  52. Li Q, Zhou H, Wurtele H, Davies B, Horazdovsky B, Verreault A, Zhang Z (2008) Acetylation of histone H3 lysine 56 regulates replication-coupled nucleosome assembly. Cell 134:244–255PubMedCentralCrossRefPubMedGoogle Scholar
  53. Liu B, Wang J, Chan KM, Tjia WM, Deng W, Guan X, Huang J-d, Li KM, Chau PY, Chen DJ (2005) Genomic instability in laminopathy-based premature aging. Nat Med 11:780–785CrossRefPubMedGoogle Scholar
  54. Liu Y, Rusinol A, Sinensky M, Wang Y, Zou Y (2006) DNA damage responses in progeroid syndromes arise from defective maturation of prelamin A. J Cell Sci 119:4644–4649PubMedCentralCrossRefPubMedGoogle Scholar
  55. Liu Y, Wang Y, Rusinol AE, Sinensky MS, Liu J, Shell SM, Zou Y (2008) Involvement of xeroderma pigmentosum group A (XPA) in progeria arising from defective maturation of prelamin A. FASEB J 22:603–611PubMedCentralCrossRefPubMedGoogle Scholar
  56. Liu B, Ghosh S, Yang X, Zheng H, Liu X, Wang Z, Jin G, Zheng B, Kennedy BK, Suh Y (2012) Resveratrol rescues SIRT1-dependent adult stem cell decline and alleviates progeroid features in laminopathy-based progeria. Cell Metab 16:738–750CrossRefPubMedGoogle Scholar
  57. Liu B, Wang Z, Ghosh S, Zhou Z (2013a) Defective ATM-Kap-1-mediated chromatin remodeling impairs DNA repair and accelerates senescence in progeria mouse model. Aging Cell 12:316–318CrossRefPubMedGoogle Scholar
  58. Liu B, Wang Z, Zhang L, Ghosh S, Zheng H, Zhou Z (2013b) Depleting the methyltransferase Suv39h1 improves DNA repair and extends lifespan in a progeria mouse model. Nat Commun 4:1868PubMedCentralCrossRefPubMedGoogle Scholar
  59. Liu J, Yin X, Liu B, Zheng H, Zhou G, Gong L, Li M, Li X, Wang Y, Hu J et al (2014) HP1alpha mediates defective heterochromatin repair and accelerates senescence in Zmpste24-deficient cells. Cell Cycle 13:1237–1247PubMedCentralCrossRefPubMedGoogle Scholar
  60. Machwe A, Xiao L, Orren DK (2004) TRF2 recruits the Werner syndrome (WRN) exonuclease for processing of telomeric DNA. Oncogene 23:149–156CrossRefPubMedGoogle Scholar
  61. Mailand N, Bekker-Jensen S, Faustrup H, Melander F, Bartek J, Lukas C, Lukas J (2007) RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins. Cell 131:887–900CrossRefPubMedGoogle Scholar
  62. Maslov AY, Vijg J (2009) Genome instability, cancer and aging. Biochim Biophys Acta 1790:963–969PubMedCentralCrossRefPubMedGoogle Scholar
  63. Maynard S, Schurman SH, Harboe C, de Souza-Pinto NC, Bohr VA (2009) Base excision repair of oxidative DNA damage and association with cancer and aging. Carcinogenesis 30:2–10PubMedCentralCrossRefPubMedGoogle Scholar
  64. McClintock D, Ratner D, Lokuge M, Owens DM, Gordon LB, Collins FS, Djabali K (2007) The mutant form of lamin A that causes Hutchinson-Gilford progeria is a biomarker of cellular aging in human skin. PLoS One 2:e1269PubMedCentralCrossRefPubMedGoogle Scholar
  65. Melcher R, von Golitschek R, Steinlein C, Schindler D, Neitzel H, Kainer K, Schmid M, Hoehn H (2000) Spectral karyotyping of Werner syndrome fibroblast cultures. Cytogenet Cell Genet 91:180–185CrossRefPubMedGoogle Scholar
  66. Merideth MA, Gordon LB, Clauss S, Sachdev V, Smith ACM, Perry MB, Brewer CC, Zalewski C, Kim HJ, Solomon B et al (2008) Phenotype and course of Hutchinson–Gilford progeria syndrome. N Engl J Med 358:592–604PubMedCentralCrossRefPubMedGoogle Scholar
  67. Morris JZ, Tissenbaum HA, Ruvkun G (1996) A phosphatidylinositol-3-OH kinase family member regulating longevity and diapause in Caenorhabditis elegans. Nature 382:536–539CrossRefPubMedGoogle Scholar
  68. Moulson CL, Go G, Gardner JM, van der Wal AC, Smitt JH, van Hagen JM, Miner JH (2005) Homozygous and compound heterozygous mutations in ZMPSTE24 cause the laminopathy restrictive dermopathy. J Invest Dermatol 125:913–919PubMedCentralCrossRefPubMedGoogle Scholar
  69. Multani AS, Chang S (2007) WRN at telomeres: implications for aging and cancer. J Cell Sci 120:713–721CrossRefPubMedGoogle Scholar
  70. Navarro CL, De Sandre-Giovannoli A, Bernard R, Boccaccio I, Boyer A, Genevieve D, Hadj-Rabia S, Gaudy-Marqueste C, Smitt HS, Vabres P et al (2004) Lamin A and ZMPSTE24 (FACE-1) defects cause nuclear disorganization and identify restrictive dermopathy as a lethal neonatal laminopathy. Hum Mol Genet 13:2493–2503CrossRefPubMedGoogle Scholar
  71. Navarro CL, Cadinanos J, De Sandre-Giovannoli A, Bernard R, Courrier S, Boccaccio I, Boyer A, Kleijer WJ, Wagner A, Giuliano F et al (2005) Loss of ZMPSTE24 (FACE-1) causes autosomal recessive restrictive dermopathy and accumulation of Lamin A precursors. Hum Mol Genet 14:1503–1513CrossRefPubMedGoogle Scholar
  72. Osley MA, Shen X (2006) Altering nucleosomes during DNA double-strand break repair in yeast. Trends Genet 22:671–677CrossRefPubMedGoogle Scholar
  73. Osley MA, Tsukuda T, Nickoloff JA (2007) ATP-dependent chromatin remodeling factors and DNA damage repair. Mutat Res 618:65–80PubMedCentralCrossRefPubMedGoogle Scholar
  74. Pandita TK, Richardson C (2009) Chromatin remodeling finds its place in the DNA double-strand break response. Nucleic Acids Res 37:1363–1377PubMedCentralCrossRefPubMedGoogle Scholar
  75. Partridge L, Mangel M (1999) Messages from mortality: the evolution of death rates in the old. Trends Ecol Evol 14:438–442CrossRefPubMedGoogle Scholar
  76. Pendas AM, Zhou Z, Cadinanos J, Freije JM, Wang J, Hultenby K, Astudillo A, Wernerson A, Rodriguez F, Tryggvason K et al (2002) Defective prelamin A processing and muscular and adipocyte alterations in Zmpste24 metalloproteinase-deficient mice. Nat Genet 31:94–99PubMedGoogle Scholar
  77. Redon C, Pilch D, Rogakou E, Sedelnikova O, Newrock K, Bonner W (2002) Histone H2A variants h2ax and h2az. Curr Opin Genet Dev 12:162–169CrossRefPubMedGoogle Scholar
  78. Riley T, Sontag E, Chen P, Levine A (2008) Transcriptional control of human p53-regulated genes. Nat Rev Mol Cell Biol 9:402–412CrossRefPubMedGoogle Scholar
  79. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM (1998) DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273:5858–5868CrossRefPubMedGoogle Scholar
  80. Rusinol AE, Sinensky MS (2006) Farnesylated lamins, progeroid syndromes and farnesyl transferase inhibitors. J Cell Sci 119:3265–3272CrossRefPubMedGoogle Scholar
  81. Salk D, Au K, Hoehn H, Martin GM (1981) Cytogenetics of Werner’s syndrome cultured skin fibroblasts: variegated translocation mosaicism. Cytogenet Cell Genet 30:92–107CrossRefPubMedGoogle Scholar
  82. Sancar A, Lindsey-Boltz LA, Ünsal-Kaçmaz K, Linn S (2004) Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu Rev Biochem 73:39–85CrossRefPubMedGoogle Scholar
  83. Satoh A, Brace CS, Rensing N, Cliften P, Wozniak DF, Herzog ED, Yamada KA, Imai S (2013) Sirt1 extends life span and delays aging in mice through the regulation of Nk2 homeobox 1 in the DMH and LH. Cell Metab 18:416–430PubMedCentralCrossRefPubMedGoogle Scholar
  84. Scaffidi P, Misteli T (2006) Lamin A-dependent nuclear defects in human aging. Science 312:1059–1063PubMedCentralCrossRefPubMedGoogle Scholar
  85. Szilard L (1959) On the nature of the aging process. Proc Natl Acad Sci U S A 45:30–45PubMedCentralCrossRefPubMedGoogle Scholar
  86. Tam A, Nouvet FJ, Fujimura-Kamada K, Slunt H, Sisodia SS, Michaelis S (1998) Dual roles for Ste24p in yeast a-factor maturation: NH2-terminal proteolysis and COOH-terminal CAAX processing. J Cell Biol 142:635–649PubMedCentralCrossRefPubMedGoogle Scholar
  87. Tanaka T, Halicka HD, Huang X, Traganos F, Darzynkiewicz Z (2006) Constitutive histone H2AX phosphorylation and ATM activation, the reporters of DNA damage by endogenous oxidants. Cell Cycle 5:1940–1945PubMedCentralCrossRefPubMedGoogle Scholar
  88. van Attikum H, Gasser SM (2005) The histone code at DNA breaks: a guide to repair? Nat Rev Mol Cell Biol 6:757–765CrossRefPubMedGoogle Scholar
  89. Varela I, Cadinanos J, Pendas AM, Gutierrez-Fernandez A, Folgueras AR, Sanchez LM, Zhou Z, Rodriguez FJ, Stewart CL, Vega JA et al (2005) Accelerated ageing in mice deficient in Zmpste24 protease is linked to p53 signalling activation. Nature 437:564–568CrossRefPubMedGoogle Scholar
  90. Wu L, Davies SL, North PS, Goulaouic H, Riou JF, Turley H, Gatter KC, Hickson ID (2000) The Bloom’s syndrome gene product interacts with topoisomerase III. J Biol Chem 275:9636–9644CrossRefPubMedGoogle Scholar
  91. Xu Y, Ayrapetov MK, Xu C, Gursoy-Yuzugullu O, Hu Y, Price BD (2012) Histone H2A. Z controls a critical chromatin remodeling step required for DNA double-strand break repair. Mol Cell 48:723–733PubMedCentralCrossRefPubMedGoogle Scholar
  92. Yang Z, Roginskaya M, Colis LC, Basu AK, Shell SM, Liu Y, Musich PR, Harris CM, Harris TM, Zou Y (2006) Specific and efficient binding of Xeroderma pigmentosum complementation group A to double-strand/single-strand DNA junctions with 3′-and/or 5′-ssDNA branches. Biochemistry 45:15921–15930PubMedCentralCrossRefPubMedGoogle Scholar
  93. Yu CE, Oshima J, Fu YH, Wijsman EM, Hisama F, Alisch R, Matthews S, Nakura J, Miki T, Ouais S et al (1996) Positional cloning of the Werner’s syndrome gene. Science 272:258–262CrossRefPubMedGoogle Scholar

Copyright information

© Springer Japan 2015

Authors and Affiliations

  1. 1.Health Science CenterShenzhen UniversityShenzhenChina
  2. 2.Shenzhen Institute of Research and InnovationThe University of Hong KongShenzhenChina
  3. 3.Department of Biochemistry, LKS Faculty of MedicineThe University of Hong KongHong KongHong Kong

Personalised recommendations