Convergent transcription through microsatellite repeat tracts induces cell death

Molecular Biology Reports

Volumn 41, Issue 9, 2014, Pages 5627-5634

  Lin, William Y ^a   Lin, Yunfu ^a   Wilson, John H ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Cell death; Convergent transcription; DNA toxicity; Tandem repeats

Indexed keywords

ARTICLE; CAG REPEAT; CELL CYCLE ARREST; CELL DEATH; CELL GROWTH; CELL LINE; CELL STRESS; CELL VIABILITY; CONTROLLED STUDY; CONVERGENT TRANSCRIPTION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MICROSATELLITE REPEAT; SHORT TANDEM REPEAT; APOPTOSIS; CELL CYCLE CHECKPOINT; GENETICS; HUMAN GENOME;

MICROSATELLITE DNA;

APOPTOSIS; CELL CYCLE CHECKPOINTS; CELL LINE; GENOME, HUMAN; HUMANS; MICROSATELLITE REPEATS; TRANSCRIPTION, GENETIC;

EID: 84906936267     PISSN: 03014851     EISSN: 15734978     Source Type: Journal    
DOI: 10.1007/s11033-014-3432-y     Document Type: Article

References (55)

1. Richard GF, Kerrest A, Dujon B (2008) Comparative genomics and molecular dynamics of DNA repeats in eukaryotes. Microbiol Mol Biol Rev 72:686-727
2. Lin Y, Dion V, Wilson JH (2006) Transcription and triplet repeat instability. In: Wells R, Ashizawa T (eds) Genetic instability and neurological diseases. Elsevier, Amsterdam, pp 691-704
3. Lopez Castel A, Cleary JD, Pearson CE (2010) Repeat instability as the basis for human diseases and as a potential target for therapy. Nat Rev Mol Cell Biol 11:165-170
4. Pearson CE, Edamura KN, Cleary JD (2005) Repeat instability: mechanisms of dynamic mutations. Nat Rev Genet 6:729-742 (Pubitemid 41400831)
5. Wells RD, Dere R, Hebert ML, Napierala M, Son LS (2005) Advances in mechanisms of genetic instability related to hereditary neurological diseases. Nucleic Acids Res 33:3785-3798 (Pubitemid 41418548)
6. Lin Y, Hubert L Jr, Wilson JH (2009) Transcription destabilizes triplet repeats. Mol Carcinog 48:350-361
7. Cleary JD, Pearson CE (2003) The contribution of cis-elements to disease-associated repeat instability: clinical and experimental evidence. Cytogenet Genome Res 100:25-55 (Pubitemid 37467789)
8. Mirkin SM (2007) Expandable DNA repeats and human disease. Nature 447:932-940
9. Wells RD (2007) Non-B DNA conformations, mutagenesis and disease. Trends Biochem Sci 32:271-278
10. Pearson CE, Sinden RR (1996) Alternative structures in duplex DNA formed within the trinucleotide repeats of the myotonic dystrophy and fragile X loci. Biochemistry 35:5041-5053 (Pubitemid 26126721)
11. Gacy AM, Goellner G, Juranic N, Macura S, McMurray CT (1995) Trinucleotide repeats that expand in human disease form hairpin structures in vitro. Cell 81:533-540
12. Wang G, Vasquez KM (2006) Non-B DNA structure-induced genetic instability. Mutat Res 598:103-119 (Pubitemid 43849854)
13. Bacolla A, Larson JE, Collins JR, Li J, Milosavljevic A, Stenson PD et al (2008) Abundance and length of simple repeats in vertebrate genomes are determined by their structural properties. Genome Res 18:1545-1553
14. Bacolla A, Wells RD (2009) Non-B DNA conformations as determinants of mutagenesis and human disease. Mol Carcinog 48:273-285
15. La Spada AR, Taylor JP (2010) Repeat expansion disease: progress and puzzles in disease pathogenesis. Nat Rev Genet 11:247-258
16. Orr HT, Zoghbi HY (2007) Trinucleotide repeat disorders. Annu Rev Neurosci 30:575-621 (Pubitemid 47218768)
17. Gatchel JR, Zoghbi HY (2005) Diseases of unstable repeat expansion: mechanisms and common principles. Nat Rev Genet 6:743-755 (Pubitemid 41400832)
18. Li LB, Yu Z, Teng X, Bonini NM (2008) RNA toxicity is a component of ataxin-3 degeneration in Drosophila. Nature 453:1107-1111 (Pubitemid 351871727)
19. Riley BE, Orr HT (2006) Polyglutamine neurodegenerative diseases and regulation of transcription: assembling the puzzle. Genes Dev 20:2183-2192
20. Ditch S, Sammarco MC, Banerjee A, Grabczyk E (2009) Progressive GAA.TTC repeat expansion in human cell lines. PLoS Genet 5:e1000704
21. Jung J, Bonini N (2007) CREB-binding protein modulates repeat instability in a Drosophila model for polyQ disease. Science 315:1857-1859 (Pubitemid 46580147)
22. Lin Y, Dion V, Wilson JH (2006) Transcription promotes contraction of CAG repeat tracts in human cells. Nat Struct Mol Biol 13:179-180 (Pubitemid 43214723)
23. Hanawalt PC, Spivak G (2008) Transcription-coupled DNA repair: two decades of progress and surprises. Nat Rev Mol Cell Biol 9:958-970
24. Kim N, Jinks-Robertson S (2012) Transcription as a source of genome instability. Nat Rev Genet 13:204-214
25. Lin Y, Wilson JH (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 (Pubitemid 47326707)
26. Dion V, Lin Y, Hubert L Jr, Waterland RA, Wilson JH (2008) Dnmt1 deficiency promotes CAG repeat expansion in the mouse germline. Hum Mol Genet 17:1306-1317 (Pubitemid 351566967)
27. Hubert L Jr, Lin Y, Dion V, Wilson JH (2011) Topoisomerase 1 and single-strand break repair modulate transcription-induced CAG repeat contraction in human cells. Mol Cell Biol 31:3105-3112
28. Lin Y, Dent SY, Wilson JH, Wells RD, Napierala M (2010) R loops stimulate genetic instability of CTG.CAG repeats. Proc Natl Acad Sci USA 107:692-697
29. Lin Y, Wilson JH (2009) Diverse effects of individual mismatch repair components on transcription-induced CAG repeat instability in human cells. DNA Repair (Amst) 8:878-885
30. Mittelman D, Sykoudis K, Hersh M, Lin Y, Wilson JH (2010) Hsp90 modulates CAG repeat instability in human cells. Cell Stress Chaperones 15:753-759
31. Lin Y, Leng M, Wan M, Wilson JH (2010) Convergent transcription through a long CAG tract destabilizes repeats and induces apoptosis. Mol Cell Biol 30:4435-4451
32. Nakamori M, Pearson CE, Thornton CA (2011) Bidirectional transcription stimulates expansion and contraction of expanded (CTG)*(CAG) repeats. Hum Mol Genet 20:580-588
33. Harper JW, Elledge SJ (2007) The DNA damage response: ten years after. Mol Cell 28:739-745 (Pubitemid 350217064)
34. Ciccia A, Elledge SJ. The DNA damage response: making it safe to play with knives. Mol Cell 40:179-204
35. Lin Y, Wilson JH (2011) Transcription-induced DNA toxicity at trinucleotide repeats: double bubble is trouble. Cell Cycle 10:611-618
36. Katayama S, Tomaru Y, Kasukawa T, Waki K, Nakanishi M, Nakamura M et al (2005) Antisense transcription in the mammalian transcriptome. Science 309:1564-1566
37. Moseley ML, Zu T, Ikeda Y, Gao W, Mosemiller AK, Daughters RS et al (2006) Bidirectional expression of CUG and CAG expansion transcripts and intranuclear polyglutamine inclusions in spinocerebellar ataxia type 8. Nat Genet 38:758-769 (Pubitemid 43980596)
38. Ladd PD, Smith LE, Rabaia NA, Moore JM, Georges SA, Hansen RS et al (2007) An antisense transcript spanning the CGG repeat region of FMR1 is upregulated in premutation carriers but silenced in full mutation individuals. Hum Mol Genet 16:3174-3187 (Pubitemid 350131334)
39. Cho DH, Thienes CP, Mahoney SE, Analau E, Filippova GN, Tapscott SJ (2005) Antisense transcription and heterochromatin at the DM1 CTG repeats are constrained by CTCF. Mol Cell 20:483-489 (Pubitemid 41572304)
40. Chen WL, Lin JW, Huang HJ, Wang SM, Su MT, Lee-Chen GJ et al (2008) SCA8 mRNA expression suggests an antisense regulation of KLHL1 and correlates to SCA8 pathology. Brain Res 1233:176-184
41. He Y, Vogelstein B, Velculescu VE, Papadopoulos N, Kinzler KW (2008) The antisense transcriptomes of human cells. Science 322:1855-1857
42. Wilburn B, Rudnicki DD, Zhao J, Weitz TM, Cheng Y, Gu X, et al. An antisense CAG repeat transcript at JPH3 locus mediates expanded polyglutamine protein toxicity in Huntington's disease-like 2 mice. Neuron 70:427-440
43. Chung DW, Rudnicki DD, Yu L, Margolis RL. A natural anti-sense transcript at the Huntington's disease repeat locus regulates HTT expression. Hum Mol Genet
44. Sopher BL, Ladd PD, Pineda VV, Libby RT, Sunkin SM, Hurley JB, et al. CTCF Regulates ataxin-7 expression through promotion of a convergently transcribed, antisense noncoding RNA. Neuron 70:1071-1084
45. Hubert L Jr, Lin Y, Dion V, Wilson JH (2011) Xpa deficiency reduces CAG trinucleotide repeat instability in neuronal tissues in a mouse model of SCA1. Hum Mol Genet 20:4822-4830
46. Owen BA, Yang Z, Lai M, Gajek M, Badger JD 2nd, Hayes JJ et al (2005) (CAG)(n)-hairpin DNA binds to Msh2-Msh3 and changes properties of mismatch recognition. Nat Struct Mol Biol 12:663-670 (Pubitemid 43086271)
47. Lin Y, Wilson JH (2012) Nucleotide excision repair, mismatch repair, and R-loops modulate convergent transcription-induced cell death and repeat instability. PLoS ONE 7:e46807
48. Ljungman M (2005) Activation of DNA damage signaling. Mutat Res 577:203-216
49. Ljungman M (2007) The transcription stress response. Cell Cycle 6:2252-2257
50. Ljungman M, Zhang F (1996) Blockage of RNA polymerase as a possible trigger for u.v. light-induced apoptosis. Oncogene 13:823-831 (Pubitemid 26312910)
51. Belotserkovskii BP, Liu R, Tornaletti S, Krasilnikova MM, Mirkin SM, Hanawalt PC. Mechanisms and implications of transcription blockage by guanine-rich DNA sequences. Proc Natl Acad Sci USA 107:12816-12821
52. Belotserkovskii BP, De Silva E, Tornaletti S, Wang G, Vasquez KM, Hanawalt PC (2007) A triplex-forming sequence from the human c-MYC promoter interferes with DNA transcription. J Biol Chem 282:32433-32441 (Pubitemid 350106421)
53. Parsons MA, Sinden RR, Izban MG (1998) Transcriptional properties of RNA polymerase II within triplet repeat-containing DNA from the human myotonic dystrophy and fragile X loci. J Biol Chem 273:26998-27008 (Pubitemid 28471723)
54. Salinas-Rios V, Belotserkovskii BP, Hanawalt PC. DNA slip-outs cause RNA polymerase II arrest in vitro: potential implications for genetic instability. Nucleic Acids Res
55. Lawlor KT, O'Keefe LV, Samaraweera SE, van Eyk CL, McLeod CJ, Maloney CA, et al (2011) Double-stranded RNA is pathogenic in Drosophila models of expanded repeat neurodegenerative diseases. Hum Mol Genet