High mobility group protein-mediated transcription requires DNA damage marker γ-H2AX

Cell Research

Volumn 25, Issue 7, 2015, Pages 837-850

  Singh, Indrabahadur ^a   Ozturk, Nihan ^a   Cordero, Julio ^a   Mehta, Aditi ^a   Hasan, Diya ^a   Cosentino, Claudia ^b   Sebastian, Carlos ^b   Krüger, Marcus ^a   Looso, Mario ^a   Carraro, Gianni ^c   Bellusci, Saverio ^d,e,f   Seeger, Werner ^a,f   Braun, Thomas ^a,f   Mostoslavsky, Raul ^b   Barreto, Guillermo ^a,e,f  

^a MAX PLANCK INSTITUTE FOR HEART AND LUNG RESEARCH   (Germany)

^b HARVARD MEDICAL SCHOOL   (United States)

^c CEDARS SINAI MEDICAL CENTER   (United States)

^d JUSTUS LIEBIG UNIVERSITY   (Germany)

^e KAZAN FEDERAL UNIVERSITY   (Russian Federation)

^f JUSTUS LIEBIG UNIVERSITY GIESSEN   (Germany)

Author keywords

ATM; Chromatin associated proteins; DNA damage; Gata6; HMGA2; TGF 1; Transcription; H2AX

Indexed keywords

CELL CYCLE PROTEIN; H2AFX PROTEIN, HUMAN; H2AFX PROTEIN, MOUSE; HIGH MOBILITY GROUP PROTEIN; HISTONE;

ANIMAL; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; HUMAN; METABOLISM; MOUSE; PHYSIOLOGY; PROCEDURES; PROTEOMICS; SIGNAL TRANSDUCTION;

ANIMALS; CELL CYCLE PROTEINS; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; HIGH MOBILITY GROUP PROTEINS; HISTONES; HUMANS; MICE; PROTEOMICS; SIGNAL TRANSDUCTION;

EID: 84940899075     PISSN: 10010602     EISSN: 17487838     Source Type: Journal    
DOI: 10.1038/cr.2015.67     Document Type: Article

References (58)

1. Bustin M, Catez F, Lim JH. The dynamics of histone H1 function in chromatin. Mol Cell 2005; 17:617-620.
2. Catez F, Hock R. Binding and interplay of HMG proteins on chromatin: lessons from live cell imaging. Biochim Biophys Acta 2010; 1799:15-27.
3. Ozturk N, Singh I, Mehta A, Braun T, Barreto G. HMGA proteins as modulators of chromatin structure during transcriptional activation. Front Cell Dev Biol 2014; 2:5.
4. Reeves R. Nuclear functions of the HMG proteins. Biochim Biophys Acta 2010; 1799:3-14.
5. Thuault S, Valcourt U, Petersen M, Manfioletti G, Heldin CH, Moustakas A. Transforming growth factor-beta employs HMGA2 to elicit epithelial-mesenchymal transition. J Cell Biol 2006; 174:175-183.
6. Lavin MF. Ataxia-telangiectasia: from a rare disorder to a paradigm for cell signalling and cancer. Nat Rev Mol Cell Biol 2008; 9:759-769.
7. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 1998; 273:5858-5868.
8. Redon CE, Nakamura AJ, Martin OA, Parekh PR, Weyemi US, Bonner WM. Recent developments in the use of gamma-H2AX as a quantitative DNA double-strand break biomarker. Aging 2011; 3:168-174.
9. Economopoulou M, Langer HF, Celeste A, et al. Histone H2AX is integral to hypoxia-driven neovascularization. Nat Med 2009; 15:553-558.
10. Steinel NC, Lee BS, Tubbs AT, et al. The ataxia telangiectasia mutated kinase controls Igkappa allelic exclusion by inhibiting secondary Vkappa-to-Jkappa rearrangements. J Exp Med 2013; 210:233-239.
11. Turinetto V, Orlando L, Sanchez-Ripoll Y, et al. High basal gammaH2AX levels sustain self-renewal of mouse embryonic and induced pluripotent stem cells. Stem Cells 2012; 30:1414-1423.
12. McManus KJ, Hendzel MJ. ATM-dependent DNA damage-independent mitotic phosphorylation of H2AX in normally growing mammalian cells. Mol Biol Cell 2005; 16:5013-5025.
13. Xiang X, Benson KF, Chada K. Mini-mouse: disruption of the pygmy locus in a transgenic insertional mutant. Science 1990; 247:967-969.
14. Bakkenist CJ, Kastan MB. DNA damage activates ATM through intermolecular autophosphorylation and dimer dissociation. Nature 2003; 421:499-506.
15. Mukherjee P, Winter SL, Alexandrow MG. Cell cycle arrest by transforming growth factor beta1 near G1/S is mediated by acute abrogation of prereplication complex activation involving an Rb-MCM interaction. Mol Cell Biol 2010; 30:845-856.
16. Singh I, Mehta A, Contreras A, et al. Hmga2 is required for canonical WNT signaling during lung development. BMC Biol 2014; 12:21.
17. Zhou X, Benson KF, Ashar HR, Chada K. Mutation responsible for the mouse pygmy phenotype in the developmentally regulated factor HMGI-C. Nature 1995; 376:771-774.
18. Gagou ME, Zuazua-Villar P, Meuth M. Enhanced H2AX phosphorylation, DNA replication fork arrest, and cell death in the absence of Chk1. Mol Biol Cell 2010; 21:739-752.
19. Bonner WM, Redon CE, Dickey JS, et al. GammaH2AX and cancer. Nat Rev Cancer 2008; 8:957-967.
20. Szuts D, Krude T. Cell cycle arrest at the initiation step of human chromosomal DNA replication causes DNA damage. J Cell Sci 2004; 117:4897-4908.
21. Chung LC, Tsui KH, Feng TH, Lee SL, Chang PL, Juang HH. L-Mimosine blocks cell proliferation via upregulation of B-cell translocation gene 2 and N-myc downstream regulated gene 1 in prostate carcinoma cells. Am J Physiol Cell Physiol 2012; 302:C676-685.
22. Ikeda K, Mason PJ, Bessler M. 3UTR-truncated Hmga2 cDNA causes MPN-like hematopoiesis by conferring a clonal growth advantage at the level of HSC in mice. Blood 2011; 117:5860-5869.
23. Chen J, Herrup K. Glutamine acts as a neuroprotectant against DNA damage, beta-amyloid and H2O2-induced stress. PloS One 2012; 7:e33177.
24. Knobel PA, Belotserkovskaya R, Galanty Y, Schmidt CK, Jackson SP, Stracker TH. USP28 is recruited to sites of DNA damage by the tandem BRCT domains of 53BP1 but plays a minor role in double-strand break metabolism. Mol Cell Biol 2014; 34:2062-2074.
25. Smith JJ, Cole ES, Romero DP. Transcriptional control of RAD51 expression in the ciliate Tetrahymena thermophila. Nucleic Acids Res 2004; 32:4313-4321.
26. Youn CK, Song PI, Kim MH, et al. Human 8-oxoguanine DNA glycosylase suppresses the oxidative stress induced apoptosis through a p53-mediated signaling pathway in human fibroblasts. Mol Cancer Res 2007; 5:1083-1098.
27. Ma Z, Yao G, Zhou B, Fan Y, Gao S, Feng X. The Chk1 inhibitor AZD7762 sensitises p53 mutant breast cancer cells to radiation in vitro and in vivo. Mol Med Rep 2012; 6:897-903.
28. Jin C, Zang C, Wei G, et al. H3. 3/H2A. Z double variant-containing nucleosomes mark 'nucleosome-free regions' of active promoters and other regulatory regions. Nat Genet 2009; 41:941-945.
29. Li A, Yu Y, Lee SC, Ishibashi T, Lees-Miller SP, Ausio J. Phosphorylation of histone H2A. X by DNA-dependent protein kinase is not affected by core histone acetylation, but it alters nucleosome stability and histone H1 binding. J Biol Chem 2010; 285:17778-17788.
30. Kishi Y, Fujii Y, Hirabayashi Y, Gotoh Y. HMGA regulates the global chromatin state and neurogenic potential in neocortical precursor cells. Nat Neurosci 2012; 15:1127-1133.
31. Catez F, Yang H, Tracey KJ, Reeves R, Misteli T, Bustin M. Network of dynamic interactions between histone H1 and high-mobility-group proteins in chromatin. Mol Cell Biol 2004; 24:4321-4328.
32. Vicent GP, Nacht AS, Font-Mateu J, et al. Four enzymes cooperate to displace histone H1 during the first minute of hormonal gene activation. Genes Dev 2011; 25:845-862.
33. Heo K, Kim H, Choi SH, et al. FACT-mediated exchange of histone variant H2AX regulated by phosphorylation of H2AX and ADP-ribosylation of Spt16. Mol Cell 2008; 30:86-97.
34. Ransom M, Williams SK, Dechassa ML, et al. FACT and the proteasome promote promoter chromatin disassembly and transcriptional initiation. J Biol Chem 2009; 284:23461-23471.
35. Formosa T, Eriksson P, Wittmeyer J, Ginn J, Yu Y, Stillman DJ. Spt16-Pob3 and the HMG protein Nhp6 combine to form the nucleosome-binding factor SPN. EMBO J 2001; 20:3506-3517.
36. Natarajan S, Hombach-Klonisch S, Droge P, Klonisch T. HMGA2 inhibits apoptosis through interaction with ATRCHK1 signaling complex in human cancer cells. Neoplasia 2013; 15:263-280.
37. Shanbhag NM, Rafalska-Metcalf IU, Balane-Bolivar C, Janicki SM, Greenberg RA. ATM-dependent chromatin changes silence transcription in cis to DNA double-strand breaks. Cell 2010; 141:970-981.
38. Ju BG, Lunyak VV, Perissi V, et al. A topoisomerase IIbeta-mediated dsDNA break required for regulated transcription. Science 2006; 312:1798-1802.
39. Lin C, Yang L, Tanasa B, et al. Nuclear receptor-induced chromosomal proximity and DNA breaks underlie specific translocations in cancer. Cell 2009; 139:1069-1083.
40. Hamperl S, Cimprich KA. The contribution of co-transcriptional RNA:DNA hybrid structures to DNA damage and genome instability. DNA Rep 2014; 19:84-94.
41. Li AY, Boo LM, Wang SY, et al. Suppression of nonhomologous end joining repair by overexpression of HMGA2. Cancer Res 2009; 69:5699-5706.
42. Barlow C, Hirotsune S, Paylor R, et al. Atm-deficient mice: A paradigm of ataxia telangiectasia. Cell 1996; 86:159-171.
43. Celeste A, Petersen S, Romanienko PJ, et al. Genomic instability in mice lacking histone H2AX. Science 2002; 296:922-927.
44. Kari V, Shchebet A, Neumann H, Johnsen SA. The H2B ubiquitin ligase RNF40 cooperates with SUPT16H to induce dynamic changes in chromatin structure during DNA double-strand break repair. Cell Cycle 2011; 10:3495-3504.
45. Minsky N, Shema E, Field Y, Schuster M, Segal E, Oren M. Monoubiquitinated H2B is associated with the transcribed region of highly expressed genes in human cells. Nat Cell Biol 2008; 10:483-488.
46. Summer H, Li O, Bao Q, et al. HMGA2 exhibits dRP/AP site cleavage activity and protects cancer cells from DNA-damage-induced cytotoxicity during chemotherapy. Nucleic Acids Res 2009; 37:4371-4384.
47. Winslow MM, Dayton TL, Verhaak RG, et al. Suppression of lung adenocarcinoma progression by Nkx2-1. Nature 2011; 473:101-104.
48. Mehta A, Dobersch S, Dammann RH, et al. Validation of Tuba1a as appropriate internal control for normalization of gene expression analysis during mouse lung development. Int J Mol Sci 2015; 16:4492-4511.
49. Metivier R, Penot G, Hubner MR, et al. Estrogen receptor-alpha directs ordered, cyclical, and combinatorial recruitment of cofactors on a natural target promoter. Cell 2003; 115:751-763.
50. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods 2012; 9:357-359.
51. Zhang Y, Liu T, Meyer CA, et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol 2008; 9:R137.
52. Jagla B, Wiswedel B, Coppee JY. Extending KNIME for next-generation sequencing data analysis. Bioinformatics 2011; 27:2907-2909.
53. Shen L, Shao N, Liu X, Nestler E. ngs. plot: Quick mining and visualization of next-generation sequencing data by integrating genomic databases. BMC Genomics 2014; 15:284.
54. Shevchenko A, Jensen ON, Podtelejnikov AV, et al. Linking genome and proteome by mass spectrometry: large-scale identification of yeast proteins from two dimensional gels. Proc Natl Acad Sci USA 1996; 93:14440-14445.
55. Mukhametshina RT, Ruhs A, Singh I, et al. Quantitative proteome analysis of alveolar type-II cells reveals a connection of integrin receptor subunits beta 2/6 and WNT Signaling. J Proteome Res 2013; 12:5598-5608.
56. Cox J, Mann M. MaxQuant enables high peptide identification rates, individualized p. p. b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol 2008; 26:1367-1372.
57. Cox J, Matic I, Hilger M, et al. A practical guide to the Max-Quant computational platform for SILAC-based quantitative proteomics. Nat Protoc 2009; 4:698-705.
58. Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 2002; 30:207-210.