An Xpb mouse model for combined xeroderma pigmentosum and cockayne syndrome reveals progeroid features upon further attenuation of DNA repair

Molecular and Cellular Biology

Volumn 29, Issue 5, 2009, Pages 1276-1290

  Andressoo, Jaan Olle ^a,c   Weeda, Geert ^a   De Wit, Jan ^a   Mitchell, James R ^a,d   Beems, Rudolf B ^b   Van Steeg, Harry ^b   Van Der Horst, Gijsbertus T J ^a   Hoeijmakers, Jan H ^a  

^a ERASMUS MEDICAL CENTER   (Netherlands)

^b NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

^c UNIVERSITY OF HELSINKI   (Finland)

^d HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HELICASE; TRANSCRIPTION FACTOR IIH;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATTENUATION; COCKAYNE SYNDROME; DNA DAMAGE; DNA REPAIR; EMBRYO DEVELOPMENT; EXCISION REPAIR; GENE MUTATION; GENETIC VARIABILITY; GENOTYPE; IMMUNOBLOTTING; IMMUNOFLUORESCENCE; MOUSE; NONHUMAN; OXIDATIVE STRESS; POINT MUTATION; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; XERODERMA PIGMENTOSUM; ANIMAL; DISEASE MODEL; GENETICS; MUTATION;

ANIMALS; COCKAYNE SYNDROME; DISEASE MODELS, ANIMAL; DNA HELICASES; DNA REPAIR; MICE; MUTATION; OXIDATIVE STRESS; TRANSCRIPTION FACTOR TFIIH; XERODERMA PIGMENTOSUM;

ANIMALIA; MUS;

EID: 61749093727     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01229-08     Document Type: Article

References (73)

1. Andressoo, J. O., and J. H. Hoeijmakers. 2005. Transcription-coupled repair and premature ageing. Mutat. Res. 577:179-194.
2. Andressoo, J. O., J. Jans, J. de Wit, F. Coin, D. Hoogstraten, M. van de Ven, W. Toussaint, J. Huijmans, H. B. Thio, W. J. van Leeuwen, J. de Boer, J. M. Egly, J. H. Hoeijmakers, G. T. van der Horst, and J. R. Mitchell. 2006. Rescue of progeria in trichothiodystrophy by homozygous lethal Xpd alleles. PLoS Biol. 4:e322.
3. Andressoo, J. O., J. R. Mitchell, J. de Wit, D. Hoogstraten, M. Volker, W. Toussaint, E. Speksnijder, R. B. Beems, H. van Steeg, J. Jans, C. I. de Zeeuw, N. G. Jaspers, A. Raams, A. R. Lehmann, W. Vermeulen, J. H. Hoeijmakers, and G. T. van der Horst. 2006. An Xpd mouse model for the combined xeroderma pigmentosum/Cockayne syndrome exhibiting both cancer predisposition and segmental progeria. Cancer Cell 10:121-132.
4. Bahar, R., C. H. Hartmann, K. A. Rodriguez, A. D. Denny, R. A. Busuttil, M. E. Dolle, R. B. Calder, G. B. Chisholm, B. H. Pollock, C. A. Klein, and J. Vijg. 2006. Increased cell-to-cell variation in gene expression in ageing mouse heart. Nature 441:1011-1014.
5. Bartke, A. 2005. Minireview: role of the growth hormone/insulin-like growth factor system in mammalian aging. Endocrinology 146:3718-3723.
6. Bauer, M., A. C. Hamm, M. Bonaus, A. Jacob, J. Jaekel, H. Schorle, M. J. Pankratz, and J. D. Katzenberger. 2004. Starvation response in mouse liver shows strong correlation with life-span-prolonging processes. Physiol. Genomics 17:230-244.
7. Bootsma, D., K. H. Kraemer, J. E. Cleaver, and J. H. Hoeijmakers. 2002. The genetic basis of human cancer. McGraw-Hill Medical Publishing Division, New York, NY.
8. Botta, E., T. Nardo, A. R. Lehmann, J. M. Egly, A. M. Pedrini, and M. Stefanini. 2002. Reduced level of the repair/transcription factor TFIIH in trichothiodystrophy. Hum. Mol. Genet. 11:2919-2928.
9. Bradsher, J., J. Auriol, L. Proietti de Santis, S. Iben, J. L. Vonesch, I. Grummt, and J. M. Egly. 2002. CSB is a component of RNA pol I transcription. Mol. Cell 10:819-829.
10. Brooks, P. J. 2007. The case for 8,5′-cyclopurine-2′- deoxynucleosides as endogenous DNA lesions that cause neurodegeneration in xeroderma pigmentosum. Neuroscience 145:1407-1417.
11. Brooks, P. J., T. F. Cheng, and L. Cooper. 2008. Do all of the neurologic diseases in patients with DNA repair gene mutations result from the accumulation of DNA damage? DNA Repair 7:834-848.
12. Broughton, B. C., M. Berneburg, H. Fawcett, E. M. Taylor, C. F. Arlett, T. Nardo, M. Stefanini, E. Menefee, V. H. Price, S. Queille, A. Sarasin, E. Bohnert, J. Krutmann, R. Davidson, K. H. Kraemer, and A. R. Lehmann. 2001. Two individuals with features of both xeroderma pigmentosum and trichothiodystrophy highlight the complexity of the clinical outcomes of mutations in the XPD gene. Hum. Mol. Genet. 10:2539-2547.
13. Charlet-Berguerand, N., S. Feuerhahn, S. E. Kong, H. Ziserman, J. W. Conaway, R. Conaway, and J. M. Egly. 2006. RNA polymerase II bypass of oxidative DNA damage is regulated by transcription elongation factors. EMBO J. 25:5481-5491.
14. Citterio, E., V. Van Den Boom, G. Schnitzler, R. Kanaar, E. Bonte, R. E. Kingston, J. H. Hoeijmakers, and W. Vermeulen. 2000. ATP-dependent chromatin remodeling by the Cockayne syndrome B DNA repair-transcription- coupling factor. Mol. Cell. Biol. 20:7643-7653.
15. Cleaver, J. E., E. Hefner, R. R. Laposa, D. Karentz, and T. Marti. 2007. Cockayne syndrome exhibits dysregulation of p21 and other gene products that may be independent of transcription-coupled repair. Neuroscience 145:1300-1308.
16. Cleaver, J. E., L. H. Thompson, A. S. Richardson, and J. C. States. 1999. A summary of mutations in the UV-sensitive disorders: xeroderma pigmentosum, Cockayne syndrome, and trichothiodystrophy. Hum. Mutat. 14:9-22.
17. Coin, F., E. Bergmann, A. Tremeau-Bravard, and J. M. Egly. 1999. Mutations in XPB and XPD helicases found in xeroderma pigmentosum patients impair the transcription function of TFIIH. EMBO J. 18:1357-1366.
18. Compe, E., M. Malerba, L. Soler, J. Marescaux, E. Borrelli, and J. M. Egly. 2007. Neurological defects in trichothiodystrophy reveal a coactivator function of TFIIH. Nat. Neurosci. 10:1414-1422.
19. de Boer, J., J. O. Andressoo, J. de Wit, J. Huijmans, R. B. Beems, H. van Steeg, G. Weeda, G. T. van der Horst, W. van Leeuwen, A. P. Themmen, M. Meradji, and J. H. Hoeijmakers. 2002. Premature aging in mice deficient in DNA repair and transcription. Science 296:1276-1279.
20. de Boer, J., J. de Wit, H. van Steeg, R. J. W. Berg, M. Morreau, P. Visser, A. R. Lehmann, M. Duran, J. H. J. Hoeijmakers, and G. Weeda. 1998. A mouse model for the basal transcription/DNA repair syndrome trichothiodystrophy. Mol. Cell 1:981-990.
21. de Boer, J., I. Donker, J. de Wit, J. H. J. Hoeijmakers, and G. Weeda. 1998. Disruption of the mouse xeroderma pigmentosum group D DNA repair/basal transcription gene results in preimplantation lethality. Cancer Res. 58:89-94.
22. D'Errico, M., E. Parlanti, M. Teson, P. Degan, T. Lemma, A. Calcagnile, I. Iavarone, P. Jaruga, M. Ropolo, A. M. Pedrini, D. Orioli, G. Frosina, G. Zambruno, M. Dizdaroglu, M. Stefanini, and E. Dogliotti. 2007. The role of CSA in the response to oxidative DNA damage in human cells. Oncogene 26:4336-4343.
23. D'Errico, M., M. Teson, A. Calcagnile, T. Nardo, N. De Luca, C. Lazzari, S. Soddu, G. Zambruno, M. Stefanini, and E. Dogliotti. 2005. Differential role of transcription-coupled repair in UVB-induced response of human fibroblasts and keratinocytes. Cancer Res. 65:432-438.
24. de Vries, A., C. T. M. van Oostrom, F. M. A. Hofhuis, P. M. Dortant, R. J. W. Berg, F. R. de Gruijl, P. W. Wester, C. F. van Kreijl, P. J. A. Capel, H. van Steeg, and S. J. Verbeek. 1995. Increased susceptibility to ultraviolet-B and carcinogens of mice lacking the DNA excision repair gene XPA. Nature 377:169-173.
25. de Waard, H., J. de Wit, J. O. Andressoo, C. T. van Oostrom, B. Riis, A. Weimann, H. E. Poulsen, H. van Steeg, J. H. Hoeijmakers, and G. T. van der Horst. 2004. Different effects of CSA and CSB deficiency on sensitivity to oxidative DNA damage. Mol. Cell. Biol. 24:7941-7948.
26. de Waard, H., J. de Wit, T. G. Gorgels, G. van den Aardweg, J. O. Andressoo, M. Vermeij, H. van Steeg, J. H. Hoeijmakers, and G. T. van der Horst. 2003. Cell type-specific hypersensitivity to oxidative damage in CSB and XPA mice. DNA Repair 2:13-25.
27. Dollé, M. E., R. A. Busuttil, A. M. Garcia, S. Wijnhoven, E. van Drunen, L. J. Niedernhofer, G. van der Horst, J. H. Hoeijmakers, H. van Steeg, and J. Vijg. 2006. Increased genomic instability is not a prerequisite for shortened lifespan in DNA repair deficient mice. Mutat. Res. 596:22-35.
28. Dubaele, S., L. Proietti De Santis, R. J. Bienstock, A. Keriel, M. Stefanini, B. Van Houten, and J. M. Egly. 2003. Basal transcription defect discriminates between xeroderma pigmentosum and trichothiodystrophy in XPD patients. Mol. Cell 11:1635-1646.
29. Fousteri, M., and L. H. Mullenders. 2008. Transcription-coupled nucleotide excision repair in mammalian cells: molecular mechanisms and biological effects. Cell Res. 18:73-84.
30. Fousteri, M., W. Vermeulen, A. A. van Zeeland, and L. H. Mullenders. 2006. Cockayne syndrome A and B proteins differentially regulate recruitment of chromatin remodeling and repair factors to stalled RNA polymerase II in vivo. Mol. Cell 23:471-482.
31. Friedberg, E. C., and L. B. Meira. 2004. Database of mouse strains carrying targeted mutations in genes affecting biological responses to DNA damage (Version 6). DNA Repair 3:1617-1638.
32. Garinis, G. A., G. T. van der Horst, J. Vijg, and J. H. Hoeijmakers. 2008. DNA damage and ageing: new-age ideas for an age-old problem. Nat. Cell Biol. 10:1241-1247.
33. Hanawalt, P. C. 2002. Subpathways of nucleotide excision repair and their regulation. Oncogene 21:8949-8956.
34. Harada, Y. N., N. Shiomi, M. Koike, M. Ikawa, M. Okabe, S. Hirota, Y. Kitamura, M. Kitagawa, T. Matsunaga, O. Nikaido, and T. Shiomi. 1999. Postnatal growth failure, short life span, and early onset of cellular senescence and subsequent immortalization in mice lacking the xeroderma pigmentosum group G gene. Mol. Cell. Biol. 19:2366-2372.
35. Keriel, A., A. Stary, A. Sarasin, C. Rochette-Egly, and J. M. Egly. 2002. XPD mutations prevent TFIIH-dependent transactivation by nuclear receptors and phosphorylation of RARα. Cell 109:125-135.
36. Kraemer, K. H., N. J. Patronas, R. Schiffmann, B. P. Brooks, D. Tamura, and J. J. DiGiovanna. 2007. Xeroderma pigmentosum, trichothiodystrophy and Cockayne syndrome: a complex genotype-phenotype relationship. Neuroscience 145:1388-1396.
37. Laposa, R. R., E. J. Huang, and J. E. Cleaver. 2007. Increased apoptosis, p53 up-regulation, and cerebellar neuronal degeneration in repair-deficient Cockayne syndrome mice. Proc. Natl. Acad. Sci. USA 104:1389-1394.
38. Lindenbaum, Y., D. Dickson, P. Rosenbaum, K. Kraemer, I. Robbins, and I. Rapin. 2001. Xeroderma pigmentosum/cockayne syndrome complex: first neuropathological study and review of eight other cases. Eur. J. Paediatr. Neurol. 5:225-242.
39. Marietta, C., and P. J. Brooks. 2007. Transcriptional bypass of bulky DNA lesions causes new mutant RNA transcripts in human cells. EMBO Rep. 8:388-393.
40. McWhir, J., J. Seldridge, D. J. Harrison, S. Squires, and D. W. Melton. 1993. Mice with DNA repair gene (ERCC-1) deficiency have elevated levels of p53, liver nuclear abnormalities and die before weaning. Nat. Gen. 5:217-223.
41. Murai, M., Y. Enokido, N. Inamura, M. Yoshino, Y. Nakatsu, G. T. van der Horst, J. H. Hoeijmakers, K. Tanaka, and H. Hatanaka. 2001. Early postnatal ataxia and abnormal cerebellar development in mice lacking xeroderma pigmentosum Group A and Cockayne syndrome Group B DNA repair genes. Proc. Natl. Acad. Sci. USA 98:13379-13384.
42. Nakane, H., S. Takeuchi, S. Yuba, M. Saijo, Y. Nakatsu, H. Murai, Y. Nakatsuru, T. Ishikawa, S. Hirota, Y. Kitamura, et al. 1995. High incidence of ultraviolet-B- or chemical-carcinogen-induced skin tumours in mice lacking the xeroderma pigmentosum group A gene. Nature 377:165-168.
43. Nance, M. A., and S. A. Berry. 1992. Cockayne syndrome: review of 140 cases. Am. J. Med. Genet. 42:68-84.
44. Niedernhofer, L. J. 2008. Tissue-specific accelerated aging in nucleotide excision repair deficiency. Mech. Ageing Dev. 129:408-415.
45. Niedernhofer, L. J., G. A. Garinis, A. Raams, A. S. Lalai, A. R. Robinson, E. Appeldoorn, H. Odijk, R. Oostendorp, A. Ahmad, W. van Leeuwen, A. F. Theil, W. Vermeulen, G. T. van der Horst, P. Meinecke, W. J. Kleijer, J. Vijg, N. G. Jaspers, and J. H. Hoeijmakers. 2006. A new progeroid syndrome reveals that genotoxic stress suppresses the somatotroph axis. Nature 444:1038-1043.
46. Niedernhofer, L. J., A. S. Lalai, and J. H. Hoeijmakers. 2005. Fanconi anemia (cross)linked to DNA repair. Cell 123:1191-1198.
47. Nouspikel, T. 2008. Nucleotide excision repair and neurological diseases. DNA Repair 7:1155-1167.
48. Oh, K. S., S. G. Khan, N. G. Jaspers, A. Raams, T. Ueda, A. Lehmann, P. S. Friedmann, S. Emmert, A. Gratchev, K. Lachlan, A. Lucassan, C. C. Baker, and K. H. Kraemer. 2006. Phenotypic heterogeneity in the XPB DNA helicase gene (ERCC3): xeroderma pigmentosum without and with Cockayne syndrome. Hum. Mutat. 27:1092-1103.
49. Randerath, E., G. D. Zhou, and K. Randerath. 1997. Organ-specific oxidative DNA damage associated with normal birth in rats. Carcinogenesis 18:859-866.
50. Robbins, J. H., K. H. Kraemer, M. A. Lutzner, B. W. Festoff, and H. G. Coon. 1974. Xeroderma pigmentosum. An inherited disease with sun sensitivity, multiple cutaneous neoplasms and abnormal repair. Ann. Intern. Med. 80:221-248.
51. Sands, A. T., A. Abuin, A. Sanchez, C. J. Conti, and A. Bradley. 1995. High susceptibility to ultraviolet-induced carcinogenesis in mice lacking XPC. Nature 377:162-165.
52. Schaeffer, L., R. Roy, S. Humbert, V. Moncollin, W. Vermeulen, J. H. J. Hoeijmakers, P. Chambon, and J. Egly. 1993. DNA repair helicase: a component of BTF2 (TFIIH) basic transcription factor. Science 260:58-63.
53. Shiomi, N., S. Kito, M. Oyama, T. Matsunaga, Y. N. Harada, M. Ikawa, M. Okabe, and T. Shiomi. 2004. Identification of the XPG region that causes the onset of Cockayne syndrome by using Xpg mutant mice generated by the cDNA-mediated knock-in method. Mol. Cell. Biol. 24:3712-3719.
54. Shiomi, N., M. Mori, S. Kito, Y. N. Harada, K. Tanaka, and T. Shiomi. 2005. Severe growth retardation and short life span of double-mutant mice lacking Xpa and exon 15 of Xpg. DNA Repair 4:351-357.
55. Shuck, S. C., E. A. Short, and J. J. Turchi. 2008. Eukaryotic nucleotide excision repair: from understanding mechanisms to influencing biology. Cell Res. 18:64-72.
56. Spivak, G., and P. C. Hanawalt. 2006. Host cell reactivation of plasmids containing oxidative DNA lesions is defective in Cockayne syndrome but normal in UV-sensitive syndrome fibroblasts. DNA Repair 5:13-22.
57. Sun, X. Z., Y. N. Harada, S. Takahashi, N. Shiomi, and T. Shiomi. 2001. Purkinje cell degeneration in mice lacking the xeroderma pigmentosum group G gene. J. Neurosci. Res. 64:348-354.
58. Tian, M., R. Shinkura, N. Shinkura, and F. W. Alt. 2004. Growth retardation, early death, and DNA repair defects in mice deficient for the nucleotide excision repair enzyme XPF. Mol. Cell. Biol. 24:1200-1205.
59. Tuo, J., P. Jaruga, H. Rodriguez, V. A. Bohr, and M. Dizdaroglu. 2003. Primary fibroblasts of Cockayne syndrome patients are defective in cellular repair of 8-hydroxyguanine and 8-hydroxyadenine resulting from oxidative stress. FASEB J. 17:668-674.
60. van der Horst, G. T., L. Meira, T. G. Gorgels, J. de Wit, S. Velasco-Miguel, J. A. Richardson, Y. Kamp, M. P. Vreeswijk, B. Smit, D. Bootsma, J. H. Hoeijmakers, and E. C. Friedberg. 2002. UVB radiation-induced cancer predisposition in Cockayne syndrome group A (Csa) mutant mice. DNA Repair 1:143-157.
61. van der Horst, G. T. J., H. van Steeg, R. J. W. Berg, A. van Gool, J. de Wit, G. Weeda, H. Morreau, R. B. Beems, C. F. van Kreijl, F. R. de Gruijl, D. Bootsma, and J. H. J. Hoeijmakers. 1997. Defective transcription-coupled repair in Cockayne syndrome B mice is associated with skin cancer predisposition. Cell 89:425-435.
62. van der Pluijm, I., G. A. Garinis, R. M. Brandt, T. G. Gorgels, S. W. Wijnhoven, K. E. Diderich, J. de Wit, J. R. Mitchell, C. van Oostrom, R. Beems, L. J. Niedernhofer, S. Velasco, E. C. Friedberg, K. Tanaka, H. van Steeg, J. H. Hoeijmakers, and G. T. van der Horst. 2007. Impaired genome maintenance suppresses the growth hormone - insulin-like growth factor 1 axis in mice with Cockayne syndrome. PLoS Biol. 5:e2.
63. van de Ven, M., J. O. Andressoo, V. B. Holcomb, P. Hasty, Y. Suh, H. van Steeg, G. A. Garinis, J. H. Hoeijmakers, and J. R. Mitchell. 2006. Extended longevity mechanisms in short-lived progeroid mice: identification of a preservative stress response associated with successful aging. Mech. Ageing Dev. 218:58-63.
64. van de Ven, M., J. O. Andressoo, V. B. Holcomb, M. von Lindern, W. M. Jong, C. I. Zeeuw, Y. Suh, P. Hasty, J. H. Hoeijmakers, G. T. van der Horst, and J. R. Mitchell. 2006. Adaptive stress response in segmental progeria resembles long-lived dwarfism and calorie restriction in mice. PLoS Genet. 2:e192.
65. Vermeulen, W., E. Bergmann, J. Auriol, S. Rademakers, P. Frit, E. Appeldoorn, J. H. Hoeijmakers, and J. M. Egly. 2000. Sublimiting concentration of TFIIH transcription/DNA repair factor causes TTD-A trichothiodystrophy disorder. Nat. Genet. 26:307-313.
66. Vermeulen, W., S. Rademakers, N. G. Jaspers, E. Appeldoorn, A. Raams, B. Klein, W. J. Kleijer, L. K. Hansen, and J. H. Hoeijmakers. 2001. A temperature-sensitive disorder in basal transcription and DNA repair in humans. Nat. Genet. 27:299-303.
67. Vermeulen, W., R. J. Scott, S. Potger, H. J. Muller, J. Cole, C. F. Arlett, W. J. Kleijer, D. Bootsma, J. H. J. Hoeijmakers, and G. Weeda. 1994. Clinical heterogeneity within xeroderma pigmentosum associated with mutations in the DNA repair and transcription gene ERCC3. Am. J. Hum. Gen. 54:191-200.
68. Volker, M., M. J. Mone, P. Karmakar, A. van Hoffen, W. Schul, W. Vermeulen, J. H. Hoeijmakers, R. van Driel, A. A. van Zeeland, and L. H. Mullenders. 2001. Sequential assembly of the nucleotide excision repair factors in vivo. Mol. Cell 8:213-224.
69. Weeda, G., I. Donker, J. de Wit, H. Morreau, R. Janssens, C. J. Vissers, A. Nigg, H. van Steeg, D. Bootsma, and J. H. J. Hoeijmakers. 1997. Disruption of mouse ERCC1 results in a novel repair syndrome with growth failure, nuclear abnormalities and senescence. Curr. Biol. 7:427-439.
70. Weeda, G., R. C. A. Van Ham, W. Vermeulen, D. Bootsma, A. J. Van der Eb, and J. H. J. Hoeijmakers. 1990. A presumed DNA helicase encoded by ERCC-3 is involved in the human repair disorders xeroderma pigmentosum and Cockayne's syndrome. Cell 62:777-791.
71. Wijnhoven, S. W., R. B. Beems, M. Roodbergen, J. van den Berg, P. H. Lohman, K. Diderich, G. T. van der Horst, J. Vijg, J. H. Hoeijmakers, and H. van Steeg. 2005. Accelerated aging pathology in ad libitum fed Xpd(TTD) mice is accompanied by features suggestive of caloric restriction. DNA Repair 4:1314-1324.
72. Wijnhoven, S. W., E. M. Hoogervorst, H. de Waard, G. T. van der Horst, and H. van Steeg. 2007. Tissue specific mutagenic and carcinogenic responses in NER defective mouse models. Mutat. Res. 614:77-94.
73. Winkler, G. S., S. J. Araujo, U. Fiedler, W. Vermeulen, F. Coin, J. M. Egly, J. H. Hoeijmakers, R. D. Wood, H. T. Timmers, and G. Weeda. 2000. TFIIH with inactive XPD helicase functions in transcription initiation but is defective in DNA repair. J. Biol. Chem. 275:4258-4266.