Neil1 is a genetic modifier of somatic and germline CAG trinucleotide repeat instability in R6/1 mice

Human Molecular Genetics

Volumn 21, Issue 22, 2012, Pages 4939-4947

  Møllersen, Linda ^a   Rowe, Alexander D ^a   Illuzzi, Jennifer L ^b   Hildrestrand, Gunn A ^a   Gerhold, Katharina J ^c   Tveterås, Linda ^a   Bjølgerud, Anja ^d   Wilson III, David M ^b   Bjørås, Magnar ^a   Klungland, Arne ^a  

^a OSLO UNIVERSITY HOSPITAL   (Norway)

^b NATIONAL INSTITUTE ON AGING   (United States)

^c MEDICAL UNIVERSITY OF VIENNA   (Austria)

^d UNIVERSITY OF OSLO   (Norway)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOSINE; DOUBLE STRANDED DNA; NEIL1 PROTEIN; PROTEIN; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; BRAIN REGION; CAG REPEAT; DNA MODIFICATION; EXON; FEMALE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; TRINUCLEOTIDE REPEAT;

ANIMALS; BASE SEQUENCE; DISEASE MODELS, ANIMAL; DNA GLYCOSYLASES; FEMALE; GENOMIC INSTABILITY; GERM-LINE MUTATION; HUNTINGTON DISEASE; MALE; MICE; MICE, KNOCKOUT; MUTATION; TRINUCLEOTIDE REPEAT EXPANSION;

MUS;

EID: 84868115310     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/dds337     Document Type: Article

References (39)

1. The Huntington's Disease Collaborative Research Group. (1993) A novel gene containing a trinucleotide repeat that is expanded and unstable on Huntington's disease chromosomes. Cell, 72, 971-983.
2. Duyao, M., Ambrose, C., Myers, R., Novelletto, A., Persichetti, F., Frontali, M., Folstein, S., Ross, C., Franz, M. and Abbott, M. (1993) Trinucleotide repeat length instability and age of onset in Huntington's disease. Nat. Genet., 4, 387-392.
3. Swami, M., Hendricks, A.E., Gillis, T., Massood, T., Mysore, J., Myers, R.H. and Wheeler, V.C. (2009) Somatic expansion of the Huntington's disease CAG repeat in the brain is associated with an earlier age of disease onset. Hum. Mol. Genet., 18, 3039-3047.
4. Shelbourne, P.F., Keller-McGandy, C., Bi, W.L., Yoon, S.R., Dubeau, L., Veitch, N.J., Vonsattel, J.P., Wexler, N.S., Arnheim, N. and Augood, S.J. (2007) Triplet repeat mutation length gains correlate with cell-type specific vulnerability in Huntington disease brain. Hum. Mol. Genet., 16, 1133-1142.
5. Møllersen, L., Rowe, A.D., Larsen, E., Rognes, T. and Klungland, A. (2010) Continuous and periodic expansion of CAG repeats in Huntington's disease R6/1 mice. PLoS Genet., 6, e1001242.
6. Kovtun, I.V., Liu, Y., Bjørås, M., Klungland, A., Wilson, S.H. and McMurray, C.T. (2007) OGG1 initiates age-dependent CAG trinucleotide expansion in somatic cells. Nature, 447, 447-452.
7. Manley, K., Shirley, T.L., Flaherty, L. and Messer, A. (1999) Msh2 deficiency prevents in vivo somatic instability of the CAG repeat in Huntington disease transgenic mice. Nat. Genet., 23, 471-473.
8. Owen, B.A., Yang, Z., Lai, M., Gajek, M., Badger, J.D., Hayes, J.J., Edelmann, W., Kucherlapati, R., Wilson, T.M. and McMurray, C.T. (2005) (CAG)(n)-hairpin DNA binds to Msh2-Msh3 and changes properties of mismatch recognition. Nat. Struct. Mol. Biol., 12, 663-670.
9. Wheeler, V.C., Lebel, L.A., Vrbanac, V., Teed, A., te Riele, R.H. and MacDonald, M.E. (2003) Mismatch repair gene Msh2 modifies the timing of early disease in Hdh(Q111) striatum. Hum. Mol. Genet., 12, 273-281.
10. Goula, A.V., Berquist, B.R., Wilson, D.M. III, Wheeler, V.C., Trottier, Y. and Merienne, K. (2009) Stoichiometry of base excision repair proteins correlates with increased somatic CAG instability in striatum over cerebellum In Huntington's disease transgenic mice. PLoS Genet., 5, e1000749.
11. Hazra, T.K., Das, A., Das, S., Choudhury, S., Kow, Y.W. and Roy, R. (2007) Oxidative DNA damage repair in mammalian cells: a new perspective. DNA Repair (Amst.), 6, 470-480.
12. Klungland, A. and Lindahl, T. (1997) Second pathway for completion of human DNA base excision-repair: reconstitution with purified proteins and requirement for DNase IV (FEN1). EMBO J., 16, 3341-3348.
13. Morland, I., Rolseth, V., Luna, L., Rognes, T., Bjørås, M. and Seeberg, E. (2002) Human DNA glycosylases of the bacterial Fpg/MutM superfamily: an alternative pathway for the repair of 8-oxoguanine and other oxidation products in DNA. Nucleic Acids Res., 30, 4926-4936.
14. Hazra, T.K., Izumi, T., Boldogh, I., Imhoff, B., Kow, Y.W., Jaruga, P., Dizdaroglu, M. and Mitra, S. (2002) Identification and characterization of a human DNA glycosylase for repair of modified bases in oxidatively damaged DNA. Proc. Natl Acad. Sci. USA, 99, 3523-3528.
15. Takao, M., Kanno, S., Kobayashi, K., Zhang, Q.M., Yonei, S., van der Horst, G.T. and Yasui, A. (2002) A back-up glycosylase in Nth1 knock-out mice is a functional Nei (endonuclease VIII) homologue. J. Biol. Chem., 277, 42205-42213.
16. Dou, H., Mitra, S. and Hazra, T.K. (2003) Repair of oxidized bases in DNA bubble structures by human DNA glycosylases NEIL1 and NEIL2. J. Biol. Chem., 278, 49679-49684.
17. Jaruga, P., Birincioglu, M., Rosenquist, T.A. and Dizdaroglu, M. (2004) Mouse NEIL1 protein is specific for excision of 2,6-diamino-4-hydroxy-5-formamidopyrimidine and 4,6-diamino-5-formamidopyrimidine from oxidatively damaged DNA. Biochemistry, 43, 15909-15914.
18. Hailer, M.K., Slade, P.G., Martin, B.D., Rosenquist, T.A. and Sugden, K.D. (2005) Recognition of the oxidized lesions spiroiminodihydantoin and guanidinohydantoin in DNA by the mammalian base excision repair glycosylases NEIL1 and NEIL2. DNA Repair (Amst.), 4, 41-50.
19. Krishnamurthy, N., Zhao, X., Burrows, C.J. and David, S.S. (2008) Superior removal of hydantoin lesions relative to other oxidized bases by the human DNA glycosylase hNEIL1. Biochemistry, 47, 7137-7146.
20. Rolseth, V., Runden-Pran, E., Luna, L., McMurray, C., Bjørås, M. and Ottersen, O.P. (2008) Widespread distribution of DNA glycosylases removing oxidative DNA lesions in human and rodent brains. DNA Repair (Amst.), 7, 1578-1588.
21. Parsons, J.L., Kavli, B., Slupphaug, G. and Dianov, G.L. (2007) NEIL1 is the major DNA glycosylase that processes 5-hydroxyuracil in the proximity of a DNA single-strand break. Biochemistry, 46, 4158-4163.
22. Dobbs, T.A., Palmer, P., Maniou, Z., Lomax, M.E. and O'Neill, P. (2008) Interplay of two major repair pathways in the processing of complex double-strand DNA breaks. DNA Repair (Amst.), 7, 1372-1383.
23. Mangiarini, L., Sathasivam, K., Mahal, A., Mott, R., Seller, M. and Bates, G.P. (1997) Instability of highly expanded CAG repeats in mice transgenic for the Huntington's disease mutation. Nat. Genet., 15, 197-200.
24. Wheeler, V.C., Auerbach, W., White, J.K., Srinidhi, J., Auerbach, A., Ryan, A., Duyao, M.P., Vrbanac, V., Weaver, M., Gusella, J.F. et al. (1999) Length-dependent gametic CAG repeat instability in the Huntington's disease knock-in mouse. Hum. Mol. Genet., 8, 115-122.
25. Kovtun, I.V., Therneau, T.M. and McMurray, C.T. (2000) Gender of the embryo contributes to CAG instability in transgenic mice containing a Huntington's disease gene. Hum. Mol. Genet., 9, 2767-2775.
26. Lee, J.M., Zhang, J., Su, A.I., Walker, J.R., Wiltshire, T., Kang, K., Dragileva, E., Gillis, T., Lopez, E.T., Boily, M.J. et al. (2010) A novel approach to investigate tissue-specific trinucleotide repeat instability. BMC. Syst. Biol., 4, doi:10.1186/1752-0509-4-29.
27. Kovtun, I.V., Johnson, K.O. and McMurray, C.T. (2011) Cockayne syndrome B protein antagonizes OGG1 in modulating CAG repeat length in vivo. Aging (Albany NY), 3, 509-514.
28. Kovtun, I.V., Thornhill, A.R. and McMurray, C.T. (2004) Somatic deletion events occur during early embryonic development and modify the extent of CAG expansion in subsequent generations. Hum. Mol. Genet., 13, 3057-3068.
29. Telenius, H., Kremer, B., Goldberg, Y.P., Theilmann, J., Andrew, S.E., Zeisler, J., Adam, S., Greenberg, C., Ives, E.J. and Clarke, L.A. (1994) Somatic and gonadal mosaicism of the Huntington disease gene CAG repeat in brain and sperm. Nat. Genet., 6, 409-414.
30. Kennedy, L., Evans, E., Chen, C.M., Craven, L., Detloff, P.J., Ennis, M. and Shelbourne, P.F. (2003) Dramatic tissue-specific mutation length increases are an early molecular event in Huntington disease pathogenesis. Hum. Mol. Genet., 12, 3359-3367.
31. Kennedy, L. and Shelbourne, P.F. (2000) Dramatic mutation instability in HD mouse striatum: does polyglutamine load contribute to cell-specific vulnerability in Huntington's disease? Hum. Mol. Genet., 9, 2539-2544.
32. Sampath, H., Batra, A.K., Vartanian, V., Carmical, J.R., Prusak, D., King, I.B., Lowell, B., Earley, L.F., Wood, T.G., Marks, D.L. et al. (2011) Variable penetrance of metabolic phenotypes and development of high-fat diet-induced adiposity in NEIL1-deficient mice. Am. J. Physiol. Endocrinol. Metab., 300, E724-E734.
33. O'Brien, P.J. and Ellenberger, T. (2004) Dissecting the broad substrate specificity of human 3-methyladenine-DNA glycosylase. J. Biol. Chem., 279, 9750-9757.
34. Jarem, D.A., Wilson, N.R. and Delaney, S. (2009) Structure-dependent DNA damage and repair in a trinucleotide repeat sequence. Biochemistry, 48, 6655-6663.
35. Goula, A.V., Pearson, C.E., Della, M.J., Trottier, Y., Tomkinson, A.E., Wilson, D.M. III and Merienne, K. (2012) The nucleotide sequence, DNA damage location, and protein stoichiometry influence the base excision repair outcome at CAG/CTG repeats. Biochemistry, 51, 3919-3932.
36. Chan, M.K., Ocampo-Hafalla, M.T., Vartanian, V., Jaruga, P., Kirkali, G., Koenig, K.L., Brown, S., Lloyd, R.S., Dizdaroglu, M. and Teebor, G.W. (2009) Targeted deletion of the genes encoding NTH1 and NEIL1 DNA N-glycosylases reveals the existence of novel carcinogenic oxidative damage to DNA. DNA Repair (Amst.), 8, 786-794.
37. Smith, K.M., Matson, S., Matson, W.R., Cormier, K., Del Signore, S.J., Hagerty, S.W., Stack, E.C., Ryu, H. and Ferrante, R.J. (2006) Dose ranging and efficacy study of high-dose coenzyme Q10 formulations in Huntington's disease mice. Biochim. Biophys. Acta, 1762, 616-626.
38. Mangiarini, L., Sathasivam, K., Seller, M., Cozens, B., Harper, A., Hetherington, C., Lawton, M., Trottier, Y., Lehrach, H., Davies, S.W. et al. (1996) Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice. Cell, 87, 493-506.
39. Berquist, B.R., McNeill, D.R. and Wilson, D.M. III (2008) Characterization of abasic endonuclease activity of human Ape1 on alternative substrates, as well as effects of ATP and sequence context on AP site incision. J. Mol. Biol., 379, 17-27.