Mutsβ generates both expansions and contractions in a mouse model of the Fragile X-associated disorders

Human Molecular Genetics

Volumn 24, Issue 24, 2015, Pages 7087-7096

  Zhao, Xiao Nan ^a   Kumari, Daman ^a   Gupta, Shikha ^a   Wu, Di ^b   Evanitsky, Maya ^a   Yang, Wei ^a   Usdin, Karen ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; MUTS BETA PROTEIN; PROTEIN MSH3; UNCLASSIFIED DRUG; MSH3 PROTEIN, MOUSE; PROTEIN; PROTEIN BINDING; PROTEIN MUTS;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; EMBRYO; FEMALE; FRAGILE X SYNDROME; GENOTYPE; GERM LINE; HYDROLYSIS; MALE; MOLECULAR MECHANICS; MOUSE; MOUSE MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN SECONDARY STRUCTURE; TEMPERATURE; ANIMAL; CELL LINE; CHROMOSOMAL INSTABILITY; CONFORMATION; DISEASE MODEL; GENETICS; GERMLINE MUTATION; MUTANT MOUSE STRAIN; PATHOPHYSIOLOGY; PHYSIOLOGY; TRINUCLEOTIDE REPEAT;

ANIMALS; CELL LINE; CHROMOSOMAL INSTABILITY; DISEASE MODELS, ANIMAL; FEMALE; FRAGILE X SYNDROME; GERM-LINE MUTATION; MALE; MICE; MICE, MUTANT STRAINS; MUTS DNA MISMATCH-BINDING PROTEIN; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; PROTEINS; TRINUCLEOTIDE REPEAT EXPANSION;

EID: 84956614647     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddv408     Document Type: Article

References (58)

1. Loesch, D. and Hagerman, R. (2012) Unstable mutations in the FMR1 gene and the phenotypes. Adv. Exp. Med. Biol., 769, 78- 114.
2. Entezam, A., Biacsi, R., Orrison, B., Saha, T., Hoffman, G.E., Grabczyk, E., Nussbaum, R.L. and Usdin, K. (2007) Regional FMRP deficits and large repeat expansions into the full mutation range in a newFragile X premutation mouse model. Gene, 395, 125-134.
3. Lokanga, R.A., Entezam, A., Kumari, D., Yudkin, D., Qin, M., Smith, C.B. and Usdin, K. (2013) Somatic expansion in mouse and human carriers of fragile X premutation alleles. Hum. Mutat., 34, 157-166.
4. Zhao, X.N. and Usdin, K. (2014) Gender and cell-type-specific effects of the transcription-coupled repair protein, ERCC6/ CSB, on repeat expansion in a mouse model of the fragile Xrelated disorders. Hum. Mutat., 35, 341-349.
5. Petek, E., Kroisel, P.M., Schuster, M., Zierler, H. andWagner, K. (1999) Mosaicism in a fragile X male including a de novo deletion in the FMR1 gene. Am. J. Med. Genet., 84, 229-232.
6. Schmucker, B. and Seidel, J. (1999) Mosaicism for a full mutation and a normal size allele in two fragile X males. Am. J. Med. Genet., 84, 221-225.
7. Todorov, T., Todorova, A., Kirov, A., Dimitrov, B., Carvalho, R., Nygren, A.O., Boneva, I. and Mitev, V. (2009) Fragile X mosaic male full mutation/normal allele detected by PCR/MS-MLPA. BMJ Case Rep., 2009, doi: 10.1136/bcr.06.2008.0139.
8. Garcia Arocena, D., de Diego, Y., Oostra, B.A., Willemsen, R. and Mirta Rodriguez, M. (2000) A fragile X case with an amplification/ deletion mosaic pattern. Hum. Genet., 106, 366-369.
9. de Graaff, E., de Vries, B.B., Willemsen, R., van Hemel, J.O., Mohkamsing, S., Oostra, B.A. and van den Ouweland, A.M. (1996) The fragile X phenotype in a mosaic male with a deletion showing expression of the FMR1 protein in 28% of the cells. Am. J. Med. Genet., 64, 302-308.
10. Fan, H., Booker, J.K., McCandless, S.E., Shashi, V., Fleming, A. and Farber, R.A. (2005) Mosaicism for an FMR1 gene deletion in a fragile X female. Am. J. Med. Genet. A, 136, 214-217.
11. Tabolacci, E., Pomponi, M.G., Pietrobono, R., Chiurazzi, P. and Neri, G. (2008) A unique case of reversion to normal size of a maternal premutation FMR1 allele in a normal boy. Eur. J. Hum. Genet., 16, 209-214.
12. Gasteiger, M., Grasbon-Frodl, E., Neitzel, B., Kooy, F. and Holinski- Feder, E. (2003) FMR1 gene deletion/reversion: a pitfall of fragile X carrier testing. Genet Test, 7, 303-308.
13. Govaerts, L.C., Smit, A.E., Saris, J.J., Van der Werf, F., Willemsen, R., Bakker, C.E., De Zeeuw, C.I. and Oostra, B.A. (2007) Exceptional good cognitive and phenotypic profile in a male carrying a mosaic mutation in the FMR1 gene. Clin. Genet., 72, 138-144.
14. Grasso, M., Faravelli, F., Lo Nigro, C., Chiurazzi, P., Sperandeo, M.P., Argusti, A., Pomponi, M.G., Lecora, M., Sebastio, G.F., Perroni, L. et al. (1999) Mosaicism for the full mutation and a microdeletion involving the CGG repeat and flanking sequences in the FMR1 gene in eight fragile X patients. Am. J. Med. Genet., 85, 311-316.
15. Mila, M., Castellvi-Bel, S., Sanchez, A., Lazaro, C., Villa, M. and Estivill, X. (1996) Mosaicism for the fragile X syndrome fullmutation and deletions within the CGG repeat of the FMR1 gene. J. Med. Genet., 33, 338-340.
16. Usdin, K. and Woodford, K.J. (1995) CGG repeats associated with DNA instability and chromosome fragility form structures that block DNA synthesis in vitro. Nucl. Acids Res., 23, 4202-4209.
17. Yu, A., Dill, J. and Mitas, M. (1995) The purine-rich trinucleotide repeat sequences d(CAG)15 and d(GAC)15 form hairpins. Nucl. Acids Res., 23, 4055-4057.
18. Mitas, M., Yu, A., Dill, J. and Haworth, I.S. (1995) The trinucleotide repeat sequence d(CGG)15 forms a heat-stable hairpin containing Gsyn. Ganti base pairs. Biochemistry, 34, 12803- 12811.
19. Mitas, M., Yu, A., Dill, J., Kamp, T.J., Chambers, E.J. and Haworth, I.S. (1995) Hairpin properties of single-stranded DNA containing a GC-rich triplet repeat: (CTG)15. Nucl. Acids Res., 23, 1050-1059.
20. Yu, A., Barron, M.D., Romero, R.M., Christy, M., Gold, B., Dai, J., Gray, D.M., Haworth, I.S. and Mitas, M. (1997) At physiological pH, d(CCG)15 forms a hairpin containing protonated cytosines and a distorted helix. Biochemistry, 36, 3687-3699.
21. Gacy, A.M., Goellner, G., Juranic, N., Macura, S. and Mcmurray, C.T. (1995) Trinucleotide repeats that expand in human-disease form hairpin structures in-vitro. Cell, 81, 533-540.
22. Gacy, A.M., Goellner, G.M., Spiro, C., Chen, X., Gupta, G., Bradbury, E.M., Dyer, R.B., Mikesell, M.J., Yao, J.Z., Johnson, A.J. et al. (1998) GAA instability in Friedreich's Ataxia shares a common, DNA-directed and intraallelic mechanism with other trinucleotide diseases. Mol. Cell, 1, 583-593.
23. Fry, M. and Loeb, L.A. (1994) The fragile X syndrome d(CGG)n nucleotide repeats form a stable tetrahelical structure. Proc. Natl Acad. Sci. USA, 91, 4950-4954.
24. Nadel, Y., Weisman-Shomer, P. and Fry, M. (1995) The fragile X syndrome single strand d(CGG)n nucleotide repeats readily fold back to form unimolecular hairpin structures. J. Biol. Chem., 270, 28970-28977.
25. Saha, T. and Usdin, K. (2001) Tetraplex formation by the progressive myoclonus epilepsy type-1 repeat: implications for instability in the repeat expansion diseases. FEBS Lett., 491, 184-187.
26. Sket, P., Pohleven, J., Kovanda, A., Stalekar, M., Zupunski, V., Zalar, M., Plavec, J. and Rogelj, B. (2015) Characterization of DNA G-quadruplex species forming from C9ORF72 G4C2- expanded repeats associated with amyotrophic lateral sclerosis and frontotemporal lobar degeneration. Neurobiol. Aging, 36, 1091-1096.
27. Latham, G.J., Coppinger, J., Hadd, A.G. and Nolin, S.L. (2014) The role of AGG interruptions in fragile X repeat expansions: a twenty-year perspective. Front Genet., 5, 244.
28. Yrigollen, C.M., Martorell, L., Durbin-Johnson, B., Naudo, M., Genoves, J., Murgia, A., Polli, R., Zhou, L., Barbouth, D., Rupchock, A. et al. (2014) AGG interruptions and maternal age affect FMR1 CGG repeat allele stability during transmission. J. Neurodev. Disord., 6, 24.
29. Nolin, S.L., Glicksman, A., Ersalesi, N., Dobkin, C., Brown, W. T., Cao, R., Blatt, E., Sah, S., Latham, G.J. and Hadd, A.G. (2015) Fragile X full mutation expansions are inhibited by one or more AGG interruptions in premutation carriers. Genet. Med., 17, 358-364.
30. Mirkin, S.M. (2007) Expandable DNA repeats and human disease. Nature, 447, 932-940.
31. Lokanga, R.A., Zhao, X.N., Entezam, A. and Usdin, K. (2014) X inactivation plays a major role in the gender bias in somatic expansion in a mouse model of the fragile X-related disorders: implications for the mechanism of repeat expansion. Hum. Mol. Genet., 23, 4985-4994.
32. Grasso, M., Boon, E.M., Filipovic-Sadic, S., van Bunderen, P.A., Gennaro, E., Cao, R., Latham, G.J., Hadd, A.G. and Coviello, D. A. (2014) A novel methylation PCR that offers standardized determination of FMR1 methylation and CGG repeat length without southern blot analysis. J. Mol. Diagn., 16, 23-31.
33. Lokanga, R.A., Zhao, X.N. and Usdin, K. (2014) The mismatch repair protein MSH2 is rate limiting for repeat expansion in a fragile X premutation mouse model. Hum. Mutat., 35, 129-136.
34. Kovtun, I.V. and McMurray, C.T. (2008) Features of trinucleotide repeat instability in vivo. Cell Res., 18, 198-213.
35. 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, 29.
36. Zhao, X.N. and Usdin, K. (2015) The transcription-coupled repair protein ERCC6/CSB also protects against repeat expansion in a mouse model of the fragile X premutation. Hum. Mutat., 36, 482-487.
37. Miller, M.J. and Yuan, B.Z. (1997) Semiautomated resolution of overlapping stutter patterns in genomic microsatellite analysis. Anal. Biochem., 251, 50-56.
38. Walsh, P.S., Fildes, N.J. and Reynolds, R. (1996) Sequence analysis and characterization of stutter products at the tetranucleotide repeat locus vWA. Nucl. Acids Res., 24, 2807-2812.
39. Shinde, D., Lai, Y., Sun, F. and Arnheim, N. (2003) Taq DNA polymerase slippage mutation rates measured by PCR and quasi-likelihood analysis: (CA/GT)n and (A/T)n microsatellites. Nucl. Acids Res., 31, 974-980.
40. Hartigan, J.A. and Hartigan, P.M. (1985) The Dip Test of Unimodality. Ann. Stat., 13, 70-84.
41. Owen, B.A., Yang, Z., Lai, M., Gajec, M., Badger, J.D. II, 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.
42. Kumar, C., Eichmiller, R., Wang, B., Williams, G.M., Bianco, P. R. and Surtees, J.A. (2014) ATP binding and hydrolysis by Saccharomyces cerevisiae Msh2-Msh3 are differentially modulated by mismatch and double-strand break repair DNA substrates. DNA Repair, 18, 18-30.
43. Lang, W.H., Coats, J.E., Majka, J., Hura, G.L., Lin, Y., Rasnik, I. and McMurray, C.T. (2011) Conformational trapping of mismatch recognition complex MSH2/MSH3 on repair-resistant DNA loops. Proc. Natl Acad. Sci. USA, 108, E837-E844.
44. Owen, B.A., W.H. Lang and McMurray, C.T. (2009) The nucleotide binding dynamics of human MSH2-MSH3 are lesion dependent. Nat. Struct. Mol. Biol., 16, 550-557.
45. Gupta, S., Gellert, M. and Yang, W. (2012) Mechanism of mismatch recognition revealed by human MutSbeta bound to unpaired DNA loops. Nat. Struct. Mol. Biol., 19, 72-78.
46. Usdin, K. (1998) NGG-triplet repeats form similar intrastrand structures: implications for the triplet expansion diseases. Nucl. Acids Res., 26, 4078-4085.
47. Amrane, S. and Mergny, J.L. (2006) Length and pH-dependent energetics of (CCG)n and (CGG)n trinucleotide repeats. Biochimie, 88, 1125-1134.
48. Kovtun, I.V., Goellner, G. and McMurray, C.T. (2001) Structural features of trinucleotide repeats associated with DNA expansion. Biochem. Cell Biol., 79, 325-336.
49. Foiry, L., Dong, L., Savouret, C., Hubert, L., te Riele, H., Junien, C. and Gourdon, G. (2006) Msh3 is a limiting factor in theformation of intergenerational CTG expansions in DM1 transgenic mice. Hum. Genet., 119, 520-526.
50. Ezzatizadeh, V., Pinto, R.M., Sandi, C., Sandi, M., Al-Mahdawi, S., Te Riele, H. and Pook, M.A. (2012) The mismatch repair system protects against intergenerational GAA repeat instability in a Friedreich ataxia mouse model. Neurobiol. Dis., 46, 165- 171.
51. Dragileva, E., Hendricks, A., Teed, A., Gillis, T., Lopez, E.T., Friedberg, E.C., Kucherlapati, R., Edelmann, W., Lunetta, K. L., MacDonald, M.E. et al. (2009) Intergenerational and striatal CAG repeat instability in Huntington's disease knock-in mice involve different DNA repair genes. Neurobiol. Dis., 33, 37-47.
52. Bourn, R.L., De Biase, I., Pinto, R.M., Sandi, C., Al-Mahdawi, S., Pook, M.A. and Bidichandani, S.I. (2012) Pms2 suppresses large expansions of the (GAA.TTC)n sequence in neuronal tissues. PLoS One, 7, e47085.
53. Du, J., Campau, E., Soragni, E., Ku, S., Puckett, J.W., Dervan, P. B. and Gottesfeld, J.M. (2012) Role of mismatch repair enzymes in GAA.TTC triplet-repeat expansion in Friedreich ataxia induced pluripotent stem cells. J. Biol. Chem., 287, 29861-29872.
54. van den Broek, W.J., Nelen, M.R., Wansink, D.G., Coerwinkel, M.M., te Riele, H., Groenen, P.J. andWieringa, B. (2002) Somatic expansion behaviour of the (CTG)n repeat in myotonic dystrophy knock-in mice is differentially affected by Msh3 and Msh6 mismatch-repair proteins. Hum. Mol. Genet., 11, 191- 198.
55. Lin, Y. and Wilson, J.H. (2009) Diverse effects of individual mismatch repair components on transcription-induced CAG repeat instability in human cells. DNA Repair, 8, 878-885.
56. Lokanga, R.A., Senejani, A.G., Sweasy, J.B. and Usdin, K. (2015) Heterozygosity for a hypomorphic polbeta mutation reduces the expansion frequency in a mouse model of the fragile x-related disorders. PLoS Genet, 11, e1005181.
57. Edelmann, W., Yang, K., Umar, A., Heyer, J., Lau, K., Fan, K., Liedtke, W., Cohen, P.E., Kane, M.F., Lipford, J.R. et al. (1997) Mutation in the mismatch repair gene Msh6 causes cancer susceptibility. Cell, 91, 467-477.
58. Edelmann, W., Umar, A., Yang, K., Heyer, J., Kucherlapati, M., Lia, M., Kneitz, B., Avdievich, E., Fan, K., Wong, E. et al. (2000) TheDNAmismatch repair genes Msh3 and Msh6 cooperate in intestinal tumor suppression. Cancer Res., 60, 803-807.