Trichothiodystrophy view from the molecular basis of DNA repair/transcription factor TFIIH

Human Molecular Genetics

Volumn 18, Issue R2, 2009, Pages

  Hashimoto, Satoru ^a   Egly, Jean Marc ^a  

^a INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR IIH;

ANIMAL; DNA REPAIR; GENETIC TRANSCRIPTION; GENETICS; HUMAN; METABOLISM; PATHOLOGY; REVIEW; TRICHOTHIODYSTROPHY;

ANIMALS; DNA REPAIR; HUMANS; TRANSCRIPTION FACTOR TFIIH; TRANSCRIPTION, GENETIC; TRICHOTHIODYSTROPHY SYNDROMES;

EID: 77956985370     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddp390     Document Type: Article

References (75)

1. McKinnon, P.J. (2009) DNA repair deficiency and neurological disease. Nat. Rev. Neurosci., 10, 100-112.
2. Lehmann, A.R. (2003) DNA repair-deficient diseases, xeroderma pigmentosum, Cockayne syndrome and trichothiodystrophy. Biochimie, 85, 1101-1111.
3. Kraemer, K.H. (2004) From proteomics to disease. Nat. Genet., 36, 677-678.
4. Jaspers, N.G., Raams, A., Silengo, M.C., Wijgers, N., Niedernhofer, L.J., Robinson, A.R., Giglia-Mari, G., Hoogstraten, D., Kleijer, W.J., Hoeijmakers, J.H. et al. (2007) First reported patient with human ERCC1 deficiency has cerebro-oculo-facio-skeletal syndrome with a mild defect in nucleotide excision repair and severe developmental failure. Am. J. Hum. Genet., 80, 457-466.
5. Lehmann, A.R. (2001) The xeroderma pigmentosum group D (XPD) gene: one gene, two functions, three diseases. Genes Dev., 15, 15-23.
6. Price, V.H., Odom, R.B., Ward, W.H. and Jones, F.T. (1980) Trichothiodystrophy: sulfur-deficient brittle hair as a marker for a neuroectodermal symptom complex. Arch. Dermatol., 116, 1375-1384.
7. Itin, P.H., Sarasin, A. and Pittelkow, M.R. (2001) Trichothiodystrophy: update on the sulfur-deficient brittle hair syndromes. J. Am. Acad. Dermatol., 44, 891-920.
8. Petrin, J.H., Meckler, K.A. and Sybert, V.P. (1998) A new variant of trichothiodystrophy with recurrent infections, failure to thrive, and death. Pediatr. Dermatol., 15, 31-34.
9. Liang, C., Morris, A., Schlucker, S., Imoto, K., Price, V.H., Menefee, E., Wincovitch, S.M., Levin, I.W., Tamura, D., Strehle, K.R. et al. (2006) Structural and molecular hair abnormalities in trichothiodystrophy. J. Invest. Dermatol., 126, 2210-2216.
10. Faghri, S., Tamura, D., Kraemer, K.H. and Digiovanna, J.J. (2008) Trichothiodystrophy: a systematic review of 112 published cases characterises a wide spectrum of clinical manifestations. J. Med. Genet., 45, 609-621.
11. Kleijer, W.J., Laugel, V., Berneburg, M., Nardo, T., Fawcett, H., Gratchev, A., Jaspers, N.G., Sarasin, A., Stefanini, M. and Lehmann, A.R. (2008) Incidence of DNA repair deficiency disorders in western Europe: xeroderma pigmentosum, Cockayne syndrome and trichothiodystrophy. DNA Repair (Amst), 7, 744-750.
12. Moriwaki, S. and Kraemer, K.H. (2001) Xeroderma pigmentosum- bridging a gap between clinic and laboratory. Photodermatol. Photoimmunol. Photomed., 17, 47-54.
13. Hirai, Y., Kodama, Y., Moriwaki, S., Noda, A., Cullings, H.M., Macphee, D.G., Kodama, K., Mabuchi, K., Kraemer, K.H., Land, C.E. et al. (2006) Heterozygous individuals bearing a founder mutation in the XPA DNA repair gene comprise nearly 1% of the Japanese population. Mutat. Res., 601, 171-178.
14. Stefanini, M., Lagomarsini, P., Arlett, C.F., Marinoni, S., Borrone, C., Crovato, F., Trevisan, G., Cordone, G. and Nuzzo, F. (1986) Xeroderma pigmentosum (complementation group D) mutation is present in patients affected by trichothiodystrophy with photosensitivity. Hum. Genet., 74, 107-112.
15. Leibeling, D., Laspe, P. and Emmert, S. (2006) Nucleotide excision repair and cancer. J. Mol. Histol., 37, 225-238.
16. Kraemer, K.H., Patronas, N.J., Schiffmann, R., Brooks, B.P., Tamura, D. and DiGiovanna, J.J. (2007) Xeroderma pigmentosum, trichothiodystrophy and Cockayne syndrome: a complex genotype-phenotype relationship. Neuroscience, 145, 1388-1396.
17. Westerveld, A., Hoeijmakers, J.H., van Duin, M., de Wit, J., Odijk, H., Pastink, A., Wood, R.D. and Bootsma, D. (1984) Molecular cloning of a human DNA repair gene. Nature, 310, 425-429.
18. Botta, E., Nardo, T., Lehmann, A.R., Egly, J.M., Pedrini, A.M. and Stefanini, M. (2002) Reduced level of the repair/transcription factor TFIIH in trichothiodystrophy. Hum. Mol. Genet., 11, 2919-2928.
19. Vermeulen, W., Bergmann, E., Auriol, J., Rademakers, S., Frit, P., Appeldoorn, E., Hoeijmakers, J.H. and Egly, J.M. (2000) Sublimiting concentration of TFIIH transcription/DNA repair factor causes TTD-A trichothiodystrophy disorder. Nat. Genet., 26, 307-313.
20. Cleaver, J.E., Thompson, L.H., Richardson, A.S. and States, J.C. (1999) A summary of mutations in the UV-sensitive disorders: xeroderma pigmentosum, Cockayne syndrome, and trichothiodystrophy. Hum. Mutat., 14, 9-22.
21. Botta, E., Nardo, T., Orioli, D., Guglielmino, R., Ricotti, R., Bondanza, S., Benedicenti, F., Zambruno, G. and Stefanini, M. (2009) Genotype-phenotype relationships in trichothiodystrophy patients with novel splicing mutations in the XPD gene. Hum. Mutat., 30, 438-445.
22. Taylor, E.M., Broughton, B.C., Botta, E., Stefanini, M., Sarasin, A., Jaspers, N.G., Fawcett, H., Harcourt, S.A., Arlett, C.F. and Lehmann, A.R. (1997) Xeroderma pigmentosum and trichothiodystrophy are associated with different mutations in the XPD (ERCC2) repair/transcription gene. Proc. Natl Acad. Sci. USA, 94, 8658-8663.
23. Andressoo, J.O., Jans, J., de Wit, J., Coin, F., Hoogstraten, D., van de Ven, M., Toussaint, W., Huijmans, J., Thio, H.B., van Leeuwen, W.J. et al. (2006) Rescue of progeria in trichothiodystrophy by homozygous lethal Xpd alleles. PLoS Biol., 4, e322.
24. Laine, J.P., Mocquet, V., Bonfanti, M., Braun, C., Egly, J.M. and Brousset, P. (2007) Common XPD (ERCC2) polymorphisms have no measurable effect on nucleotide excision repair and basal transcription. DNA Repair (Amst), 6, 1264-1270.
25. Giglia-Mari, G., Coin, F., Ranish, J.A., Hoogstraten, D., Theil, A., Wijgers, N., Jaspers, N.G., Raams, A., Argentini, M., van der Spek, P.J. et al. (2004) A new, tenth subunit of TFIIH is responsible for the DNA repair syndrome trichothiodystrophy group A. Nat. Genet., 36, 714-719.
26. Nakabayashi, K., Amann, D., Ren, Y., Saarialho-Kere, U., Avidan, N., Gentles, S., MacDonald, J.R., Puffenberger, E.G., Christiano, A.M., Martinez-Mir, A. et al. (2005) Identification of C7orf11 (TTDN1) gene mutations and genetic heterogeneity in nonphotosensitive trichothiodystrophy. Am. J. Hum. Genet., 76, 510-516.
27. Botta, E., Offman, J., Nardo, T., Ricotti, R., Zambruno, G., Sansone, D., Balestri, P., Raams, A., Kleijer, W.J., Jaspers, N.G. et al. (2007) Mutations in the C7orf11 (TTDN1) gene in six nonphotosensitive trichothiodystrophy patients: no obvious genotype-phenotype relationships. Hum. Mutat., 28, 92-96.
28. Zhang, Y., Tian, Y., Chen, Q., Chen, D., Zhai, Z. and Shu, H.B. (2007) TTDN1 is a Plk1-interacting protein involved in maintenance of cell cycle integrity. Cell Mol. Life Sci., 64, 632-640.
29. Hanawalt, P.C. and Spivak, G. (2008) Transcription-coupled DNA repair: two decades of progress and surprises. Nat. Rev. Mol. Cell Biol., 9, 958-970.
30. Mocquet, V., Laine, J.P., Riedl, T., Yajin, Z., Lee, M.Y. and Egly, J.M. (2008) Sequential recruitment of the repair factors during NER: the role of XPG in initiating the resynthesis step. EMBO J., 27, 155-167.
31. Riedl, T., Hanaoka, F. and Egly, J. (2003) The comings and goings of nucleotide excision repair factors on damaged DNA. EMBO J, 22, 5293-5303.
32. Schultz, P., Fribourg, S., Poterszman, A., Mallouh, V., Moras, D. and Egly, J.M. (2000) Molecular structure of human TFIIH. Cell, 102, 599-607.
33. Sijbers, A.M., de Laat, W.L., Ariza, R.R., Biggerstaff, M., Wei, Y.F., Moggs, J.G., Carter, K.C., Shell, B.K., Evans, E., de Jong, M.C. et al. (1996) Xeroderma pigmentosum group F caused by a defect in a structure-specific DNA repair endonuclease. Cell, 86, 811-822.
34. O'Donovan, A., Scherly, D., Clarkson, S.G. and Wood, R.D. (1994) Isolation of active recombinant XPG protein, a human DNA repair endonuclease. J. Biol. Chem., 269, 15965-15968.
35. Coin, F., Oksenych, V., Mocquet, V., Groh, S., Blattner, C. and Egly, J.M. (2008) Nucleotide excision repair driven by the dissociation of CAK from TFIIH. Mol. Cell, 31, 9-20.
36. Akhtar, M.S., Heidemann, M., Tietjen, J.R., Zhang, D.W., Chapman, R.D., Eick, D. and Ansari, A.Z. (2009) TFIIH kinase places bivalent marks on the carboxy-terminal domain of RNA polymerase II. Mol. Cell, 34, 387-393.
37. Keriel, A., Stary, A., Sarasin, A., Rochette-Egly, C. and Egly, J.M. (2002) XPD mutations prevent TFIIH-dependent transactivation by nuclear receptors and phosphorylation of RARalpha. Cell, 109, 125-135.
38. Guzder, S.N., Sung, P., Bailly, V., Prakash, L. and Prakash, S. (1994) RAD25 is a DNA helicase required for DNA repair and RNA polymerase II transcription. Nature, 369, 578-581.
39. Coin, F., Oksenych, V. and Egly, J.M. (2007) Distinct roles for the XPB/ p52 and XPD/p44 subcomplexes of TFIIH in damaged DNA opening during nucleotide excision repair. Mol. Cell, 26, 245-256.
40. Fan, L., Arvai, A.S., Cooper, P.K., Iwai, S., Hanaoka, F. and Tainer, J.A. (2006) Conserved XPB core structure and motifs for DNA unwinding: implications for pathway selection of transcription or excision repair. Mol. Cell, 22, 27-37.
41. Oksenych, V., Bernardes de Jesus, B., Zhovmer, A., Egly, J.M. and Coin, F. (2009) Molecular insights into the recruitment of TFIIH to the sites of DNA damage. EMBO J, in press.
42. Jawhari, A., Laine, J.P., Dubaele, S., Lamour, V., Poterszman, A., Coin, F., Moras, D. and Egly, J.M. (2002) p52 Mediates XPB function within the transcription/repair factor TFIIH. J. Biol. Chem., 277, 31761-31767.
43. Fregoso, M., Laine, J.P., Aguilar-Fuentes, J., Mocquet, V., Reynaud, E., Coin, F., Egly, J.M. and Zurita, M. (2007) DNA repair and transcriptional deficiencies caused by mutations in the Drosophila p52 subunit of TFIIH generate developmental defects and chromosome fragility. Mol. Cell Biol., 27, 3640-3650.
44. Guzder, S.N., Sung, P., Prakash, S. and Prakash, L. (1995) Lethality in yeast of trichothiodystrophy (TTD) mutations in the human xeroderma pigmentosum group D gene. Implications for transcriptional defect in TTD. J. Biol. Chem., 270, 17660-17663.
45. Dubaele, S., Proietti De Santis, L., Bienstock, R.J., Keriel, A., Stefanini, M., Van Houten, B. and Egly, J.M. (2003) Basal transcription defect discriminates between xeroderma pigmentosum and trichothiodystrophy in XPD patients. Mol. Cell, 11, 1635-1646.
46. Coin, F., Marinoni, J.C., Rodolfo, C., Fribourg, S., Pedrini, A.M. and Egly, J.M. (1998) Mutations in the XPD helicase gene result in XP and TTD phenotypes, preventing interaction between XPD and the p44 subunit of TFIIH. Nat. Genet., 20, 184-188.
47. Liu, H., Rudolf, J., Johnson, K.A., McMahon, S.A., Oke, M., Carter, L., McRobbie, A.M., Brown, S.E., Naismith, J.H. and White, M.F. (2008) Structure of the DNA repair helicase XPD. Cell, 133, 801-812.
48. Wolski, S.C., Kuper, J., Hanzelmann, P., Truglio, J.J., Croteau, D.L., Van Houten, B. and Kisker, C. (2008) Crystal structure of the FeS cluster-containing nucleotide excision repair helicase XPD. PLoS Biol., 6, e149.
49. Fan, L., Fuss, J.O., Cheng, Q.J., Arvai, A.S., Hammel, M., Roberts, V.A., Cooper, P.K. and Tainer, J.A. (2008) XPD helicase structures and activities: insights into the cancer and aging phenotypes from XPD mutations. Cell, 133, 789-800.
50. Boyle, J., Ueda, T., Oh, K.S., Imoto, K., Tamura, D., Jagdeo, J., Khan, S.G., Nadem, C., Digiovanna, J.J. and Kraemer, K.H. (2008) Persistence of repair proteins at unrepaired DNA damage distinguishes diseases with ERCC2 (XPD) mutations: cancer-prone xeroderma pigmentosum vs non-cancer-prone trichothiodystrophy. Hum. Mutat., 29, 1194-1208.
51. Nishiwaki, T., Kobayashi, N., Iwamoto, T., Yamamoto, A., Sugiura, S., Liu, Y.C., Sarasin, A., Okahashi, Y., Hirano, M., Ueno, S. et al. (2008) Comparative study of nucleotide excision repair defects between XPD-mutated fibroblasts derived from trichothiodystrophy and xeroderma pigmentosum patients. DNA Repair (Amst), 7, 1990-1998.
52. Chigancas, V., Lima-Bessa, K.M., Stary, A., Menck, C.F. and Sarasin, A. (2008) Defective transcription/repair factor IIH recruitment to specific UV lesions in trichothiodystrophy syndrome. Cancer Res., 68, 6074-6083.
53. Humbert, S., van Vuuren, H., Lutz, Y., Hoeijmakers, J.H., Egly, J.M. and Moncollin, V. (1994) p44 and p34 subunits of the BTF2/TFIIH transcription factor have homologies with SSL1, a yeast protein involved in DNA repair. EMBO J., 13, 2393-2398.
54. Takagi, Y., Masuda, C.A., Chang, W.H., Komori, H., Wang, D., Hunter, T., Joazeiro, C.A. and Kornberg, R.D. (2005) Ubiquitin ligase activity of TFIIH and the transcriptional response to DNA damage. Mol. Cell, 18, 237-243.
55. Burglen, L., Seroz, T., Miniou, P., Lefebvre, S., Burlet, P., Munnich, A., Pequignot, E.V., Egly, J.M. and Melki, J. (1997) The gene encoding p44, a subunit of the transcription factor TFIIH, is involved in large-scale deletions associated with Werdnig-Hoffmann disease. Am. J. Hum. Genet., 60, 72-79.
56. Ranish, J.A., Hahn, S., Lu, Y., Yi, E.C., Li, X.J., Eng, J. and Aebersold, R. (2004) Identification of TFB5, a new component of general transcription and DNA repair factor IIH. Nat. Genet., 36, 707-713.
57. Coin, F., Proietti De Santis, L., Nardo, T., Zlobinskaya, O., Stefanini, M. and Egly, J.M. (2006) p8/TTD-A as a repair-specific TFIIH subunit. Mol. Cell, 21, 215-226.
58. Aguilar-Fuentes, J., Fregoso, M., Herrera, M., Reynaud, E., Braun, C., Egly, J.M. and Zurita, M. (2008) p8/TTDA overexpression enhances UV-irradiation resistance and suppresses TFIIH mutations in a Drosophila trichothiodystrophy model. PLoS Genet., 4, e1000253.
59. Giglia-Mari, G., Miquel, C., Theil, A.F., Mari, P.O., Hoogstraten, D., Ng, J.M., Dinant, C., Hoeijmakers, J.H. and Vermeulen, W. (2006) Dynamic interaction of TTDA with TFIIH is stabilized by nucleotide excision repair in living cells. PLoS Biol., 4, e156.
60. Vitorino, M., Coin, F., Zlobinskaya, O., Atkinson, R.A., Moras, D., Egly, J.M., Poterszman, A. and Kieffer, B. (2007) Solution structure and self-association properties of the p8 TFIIH subunit responsible for trichothiodystrophy. J. Mol. Biol., 368, 473-480.
61. Kainov, D.E., Vitorino, M., Cavarelli, J., Poterszman, A. and Egly, J.M. (2008) Structural basis for group A trichothiodystrophy. Nat. Struct. Mol. Biol., 15, 980-984.
62. Sugasawa, K., Okuda, Y., Saijo, M., Nishi, R., Matsuda, N., Chu, G., Mori, T., Iwai, S., Tanaka, K. and Hanaoka, F. (2005) UV-induced ubiquitylation of XPC protein mediated by UV-DDB-ubiquitin ligase complex. Cell, 121, 387-400.
63. Weeda, G., Rossignol, M., Fraser, R.A., Winkler, G.S., Vermeulen, W., van 't Veer, L.J., Ma, L., Hoeijmakers, J.H. and Egly, J.M. (1997) The XPB subunit of repair/transcription factor TFIIH directly interacts with SUG1, a subunit of the 26S proteasome and putative transcription factor. Nucleic Acids Res., 25, 2274-2283.
64. He, Q., Peng, H., Collins, S.J., Triche, T.J. and Wu, L. (2004) Retinoid-modulated MAT1 ubiquitination and CAK activity. FASEB J., 18, 1734-1736.
65. Coin, F., Auriol, J., Tapias, A., Clivio, P., Vermeulen, W. and Egly, J.M. (2004) Phosphorylation of XPB helicase regulates TFIIH nucleotide excision repair activity. EMBO J., 23, 4835-4846.
66. Subba Rao, K. (2007) Mechanisms of disease: DNA repair defects and neurological disease. Nat. Clin. Pract. Neurol., 3, 162-172.
67. Nouspikel, T. (2007) DNA repair in differentiated cells: some new answers to old questions. Neuroscience, 145, 1213-1221.
68. de Gruijl, F.R. (1999) Skin cancer and solar UV radiation. Eur. J. Cancer, 35, 2003-2209.
69. Brooks, P.J., Cheng, T.F. and Cooper, L. (2008) Do all of the neurologic diseases in patients with DNA repair gene mutations result from the accumulation of DNA damage? DNA Repair (Amst), 7, 834-848.
70. Offman, J., Jina, N., Theron, T., Pallas, J., Hubank, M. and Lehmann, A. (2008) Transcriptional changes in trichothiodystrophy cells. DNA Repair (Amst), 7, 1364-1371.
71. de Boer, J., de Wit, J., van Steeg, H., Berg, R.J., Morreau, H., Visser, P., Lehmann, A.R., Duran, M., Hoeijmakers, J.H. and Weeda, G. (1998) A mouse model for the basal transcription/DNA repair syndrome trichothiodystrophy. Mol. Cell, 1, 981-990.
72. Compe, E., Malerba, M., Soler, L., Marescaux, J., Borrelli, E. and Egly, J.M. (2007) Neurological defects in trichothiodystrophy reveal a coactivator function of TFIIH. Nat. Neurosci., 10, 1414-1422.
73. Compe, E., Drane, P., Laurent, C., Diderich, K., Braun, C., Hoeijmakers, J.H. and Egly, J.M. (2005) Dysregulation of the peroxisome proliferator-activated receptor target genes by XPD mutations. Mol. Cell Biol., 25, 6065-6076.
74. Drane, P., Compe, E., Catez, P., Chymkowitch, P. and Egly, J.M. (2004) Selective regulation of vitamin D receptor-responsive genes by TFIIH. Mol. Cell, 16, 187-197.
75. Chen, D., Riedl, T., Washbrook, E., Pace, P.E., Coombes, R.C., Egly, J.M. and Ali, S. (2000) Activation of estrogen receptor alpha by S118 phosphorylation involves a ligand-dependent interaction with TFIIH and participation of CDK7. Mol. Cell, 6, 127-137.