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

Human Molecular Genetics

Volumn 23, Issue 18, 2014, Pages 4985-4994

  Adihe Lokanga, Rachel ^a,b   Zhao, Xiao Nan ^a   Entezam, Ali ^a   Usdin, Karen ^a  

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

^b UNIVERSITY OF CAPE TOWN   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

FRAGILE X MENTAL RETARDATION PROTEIN;

ANIMAL; DISEASE MODEL; FEMALE; FRAGILE X SYNDROME; GENE EXPRESSION REGULATION; GENE TARGETING; GENETICS; HUMAN; MALE; MOUSE; OXIDATIVE STRESS; SEXUAL DEVELOPMENT; TRINUCLEOTIDE REPEAT; X CHROMOSOME INACTIVATION;

ANIMALS; DISEASE MODELS, ANIMAL; FEMALE; FRAGILE X MENTAL RETARDATION PROTEIN; FRAGILE X SYNDROME; GENE EXPRESSION REGULATION; GENE KNOCK-IN TECHNIQUES; HUMANS; MALE; MICE; OXIDATIVE STRESS; SEX CHARACTERISTICS; TRINUCLEOTIDE REPEAT EXPANSION; X CHROMOSOME INACTIVATION;

EID: 84906242152     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddu213     Document Type: Article

References (44)

1. Chonchaiya, W., Schneider, A. and Hagerman, R.J. (2009) Fragile X: a family of disorders. Adv. Pediatr., 56, 165-186.
2. Hagerman, P. (2013) Fragile X-associated tremor/ataxia syndrome (FXTAS): pathology and mechanisms. Acta Neuropathol., 126, 1-19.
3. Sherman, S.L. (2000) Premature ovarian failure in the fragile X syndrome. Am. J. Med. Genet., 97, 189-194.
4. Murray, A., Webb, J., Grimley, S., Conway, G. and Jacobs, P. (1998) Studies of FRAXA and FRAXE in women with premature ovarian failure. J. Med. Genet., 35, 637-640.
5. Fry, M. and Usdin, K. (2006) Human Nucleotide Expansion Disorders. Springer, Heidelberg.
6. Usdin, K. (2006) Bending the rules: unusual nucleic acid structures and human disease. In Wells, R.D. and Ashizawa, T. (eds), Genetic Instabilities and Hereditary Neurological Diseases. Elsevier-Academic Press.
7. 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.
8. Entezam, A., Lokanga, A.R., Le, W., Hoffman, G. and Usdin, K. (2010) Potassium bromate, a potent DNA oxidizing agent, exacerbates germline repeat expansion in a fragile X premutation mouse model. Hum. Mutat., 31, 611-616.
9. 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.
10. 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 X-related disorders. Hum. Mutat., 35, 341-349.
11. Entezam, A. and Usdin, K. (2008) ATR protects the genome against CGG.CCG-repeat expansion in Fragile X premutation mice. Nucleic Acids Res., 36, 1050-1056.
12. 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.
13. 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 new Fragile X premutation mouse model. Gene, 395, 125-134.
14. Amos-Landgraf, J.M., Cottle, A., Plenge, R.M., Friez, M., Schwartz, C.E., Longshore, J. and Willard, H.F. (2006)Xchromosome-inactivation patterns of 1,005 phenotypically unaffected females. Am. J. Hum. Genet., 79, 493-499.
15. Tassone, F., Beilina, A., Carosi, C., Albertosi, S., Bagni, C., Li, L., Glover, K., Bentley, D. and Hagerman, P.J. (2007) Elevated FMR1 mRNA in premutation carriers is due to increased transcription. RNA, 13, 555-562.
16. Kovtun, I.V., Liu, Y., Bjoras, 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.
17. Mollersen, L., Rowe, A.D., Illuzzi, J.L., Hildrestrand, G.A., Gerhold, K.J., Tveteras, L., Bjolgerud, A., Wilson, D.M. 3rd, Bjoras, M. and Klungland, A. (2012) Neil1 is a genetic modifier of somatic and germline CAG trinucleotide repeat instability in R6/1 mice. Hum. Mol. Genet., 21, 4939-4947.
18. Ali, S.S., Xiong, C., Lucero, J., Behrens, M.M., Dugan, L.L. and Quick, K.L. (2006) Gender differences in free radical homeostasis during aging: shorter-lived female C57BL6 mice have increased oxidative stress. Aging Cell, 5, 565-574.
19. Hamilton, M.L., Van Remmen, H., Drake, J.A., Yang, H., Guo, Z.M., Kewitt, K., Walter, C.A. and Richardson, A. (2001) Does oxidative damage to DNA increase with age? Proc. Natl Acad. Sci. USA, 98, 10469-10474.
20. Ross-Inta, C., Omanska-Klusek, A., Wong, S., Barrow, C., Garcia-Arocena, D., Iwahashi, C., Berry-Kravis, E., Hagerman, R.J., Hagerman, P.J. and Giulivi, C. (2010) Evidence of mitochondrial dysfunction in fragile X-associated tremor/ataxia syndrome. Biochem. J., 429, 545-552.
21. Fu, Z.D., Csanaky, I.L. and Klaassen, C.D. (2012) Effects of aging onmRNA profiles for drug-metabolizingenzymes and transporters in livers of male and female mice. Drug Metab. Dispos., 40, 1216-1225.
22. Xu, Y.Q., Zhang, D., Jin, T., Cai, D.J., Wu, Q., Lu, Y., Liu, J. and Klaassen, C.D. (2012) Diurnal variation of hepatic antioxidant gene expression in mice. PLoS ONE, 7, e44237.
23. Dreger, H., Westphal, K., Wilck, N., Baumann, G., Stangl, V., Stangl, K. and Meiners, S. (2010) Protection of vascular cells from oxidative stress by proteasome inhibition depends on Nrf2. Cardiovasc. Res., 85, 395-403.
24. Kwak, M.K., Itoh, K., Yamamoto, M., Sutter, T.R. and Kensler, T.W. (2001) Role of transcription factor Nrf2 in the induction of hepatic phase 2 and antioxidative enzymes in vivo by the cancer chemoprotective agent, 3H-1, 2-dimethiole-3-thione. Mol. Med., 7, 135-145.
25. Fu, Z.D. and Klaassen, C.D. (2013) Short-term calorie restriction feminizes the mRNA profiles of drug metabolizing enzymes and transporters in livers of mice. Toxicol. Appl. Pharmacol., 274, 137-146.
26. Pamplona, R. and Barja, G. (2006) Mitochondrial oxidative stress, aging and caloric restriction: the protein and methionine connection. Biochim. Biophys. Acta, 1757, 496-508.
27. Glaser, D., Wohrle, D., Salat, U., Vogel, W. and Steinbach, P. (1999) Mitotic behavior of expanded CGG repeats studied on cultured cells: further evidence for methylation-mediated triplet repeat stability in fragile X syndrome. Am. J. Med. Genet., 84, 226-228.
28. Lin, Y., Hubert, L. Jr and Wilson, J.H. (2009) Transcription destabilizes triplet repeats. Mol. Carcinog., 48, 350-361.
29. Nakamori, M., Pearson, C.E. and Thornton, C.A. (2011) Bidirectional transcription stimulates expansion and contraction of expanded (CTG)*(CAG) repeats. Hum. Mol. Genet., 20, 580-588.
30. Lia, A.S., Seznec, H., Hofmann-Radvanyi, H., Radvanyi, F., Duros, C., Saquet, C., Blanche, M., Junien, C. andGourdon, G. (1998)Somatic instability of the CTGrepeat in mice transgenic for themyotonic dystrophy region is age dependent but not correlated to the relative intertissue transcription levels and proliferative capacities. Hum. Mol. Genet., 7, 1285-1291.
31. Goula, A.V., Stys, A., Chan, J.P., Trottier, Y., Festenstein, R. and Merienne, K. (2012) Transcription elongation and tissue-specific somatic CAG instability. PLoS Genet., 8, e1003051.
32. Falk, M., Lukasova, E. and Kozubek, S. (2010) Higher-order chromatin structure in DSB induction, repair and misrepair. Mutat. Res., 704, 88-100.
33. Salinas-Rios, V., Belotserkovskii, B.P. and Hanawalt, P.C. (2011) DNA slip-outs cause RNA polymerase II arrest in vitro: potential implications for genetic instability. Nucleic Acids Res., 39, 7444-7454.
34. Jung, J. and Bonini, N. (2007) CREB-binding protein modulates repeat instability in a Drosophila model for polyQ disease. Science, 315, 1857-1859.
35. Hubert, L. Jr, Lin, Y., Dion, V. and Wilson, J.H. (2011) Xpa deficiency reduces CAG trinucleotide repeat instability in neuronal tissues in a mouse model of SCA1. Hum. Mol. Genet., 20, 4822-4830.
36. Lin, Y. and Wilson, J.H. (2007) Transcription-induced CAG repeat contraction in human cells is mediated in part by transcription-coupled nucleotide excision repair. Mol. Cell. Biol., 27, 6209-6217.
37. 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.
38. Lin, Y., Dion, V. and Wilson, J.H. (2006) Transcription promotes contraction of CAG repeat tracts in human cells. Nat. Struct. Mol. Biol., 13, 179-180.
39. Hanawalt, P.C. (1987) PreferentialDNArepair in expressed genes. Environ. Health Perspect., 76, 9-14.
40. Khobta, A. and Epe, B. (2012) Interactions between DNA damage, repair, and transcription. Mutat. Res., 736, 5-14.
41. Aguilera, A. and Garcia-Muse, T. (2012) R loops: from transcription byproducts to threats to genome stability. Mol. Cell, 46, 115-124.
42. McIvor, E.I., Polak, U. and Napierala, M. (2010) New insights into repeat instability: role of RNA*DNA hybrids. RNA Biol., 7, 551-558.
43. Li, F., Mao, G., Tong, D., Huang, J., Gu, L., Yang, W. and Li, G.M. (2013) The histone mark H3K36me3 regulates human DNA mismatch repair through its interaction with MutSalpha. Cell, 153, 590-600.
44. Pluciennik, A., Burdett, V., Baitinger, C., Iyer, R.R., Shi, K. and Modrich, P. (2013) Extrahelical (CAG)/(CTG) triplet repeat elements support proliferating cell nuclear antigen loading and MutLalpha endonuclease activation. Proc. Natl Acad. Sci. USA, 110, 12277-12282.