Gadd45 proteins: Key players of repair-mediated DNA demethylation

Advances in Experimental Medicine and Biology

Volumn 793, Issue , 2013, Pages 35-50

  Schäfer, Andrea ^a  

^a INSTITUTE OF MOLECULAR BIOLOGY   (Armenia)

Author keywords

[No Author keywords available]

Indexed keywords

DNA METHYLTRANSFERASE 1; ESTROGEN RECEPTOR ALPHA; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 45; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR DELTA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; RETINOIC ACID RECEPTOR ALPHA; RETINOID X RECEPTOR ALPHA;

ARTICLE; DNA DEMETHYLATION; DNA METHYLATION; DNA REPAIR; ENZYME ACTIVITY; EPIGENETICS; EXCISION REPAIR; GENETIC REGULATION; HUMAN; MOLECULAR MECHANICS; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING;

EID: 84934440223     PISSN: 00652598     EISSN: None     Source Type: Book Series    
DOI: 10.1007/978-1-4614-8289-5_3     Document Type: Article

References (100)

1. Abdollahi A, Lord KA, Hoffman-Liebermann B, Liebermann DA (1991) Sequence and expression of a cDNA encoding MyD118: a novel myeloid differentiation primary response gene induced by multiple cytokines. Oncogene 6:165-167.
2. Agius F, Kapoor A, Zhu JK (2006) Role of the Arabidopsis DNA glycosylase/lyase ROS1 in active DNA demethylation. Proc Natl Acad Sci USA 103:11796-11801.
3. Azam N, Vairapandi M, Zhang W, Hoffman B, Liebermann DA (2001) Interaction of CR6 (GADD45gamma) with proliferating cell nuclear antigen impedes negative growth control. J Biol Chem 276:2766-2774.
4. Barreto G, Schäfer A, Marhold J, Stach D, Swaminathan SK, Handa V, Doderlein G, Maltry N, Wu W, Lyko F et al (2007) Gadd45a promotes epigenetic gene activation by repair-mediated DNA demethylation. Nature 445:671-675.
5. Beadling C, Johnson KW, Smith KA (1993) Isolation of interleukin 2-induced immediate-early genes. Proc Natl Acad Sci USA 90:2719-2723.
6. Bhutani N, Brady JJ, Damian M, Sacco A, Corbel SY, Blau HM (2010) Reprogramming towards pluripotency requires AID-dependent DNA demethylation. Nature 463:1042-1047.
7. Bird A (2002) DNA methylation patterns and epigenetic memory. Genes Dev 16:6-21.
8. Bruniquel D, Schwartz RH (2003) Selective, stable demethylation of the interleukin-2 gene enhances transcription by an active process. Nat Immunol 4:235-240.
9. Bulavin DV, Kovalsky O, Hollander MC, Fornace AJ Jr (2003) Loss of oncogenic H-ras-induced cell cycle arrest and p38 mitogen-activated protein kinase activation by disruption of Gadd45a. Mol Cell Biol 23:3859-3871.
10. Carrier F, Georgel PT, Pourquier P, Blake M, Kontny HU, Antinore MJ, Gariboldi M, Myers TG, Weinstein JN, Pommier Y et al (1999) Gadd45, a p53-responsive stress protein, modifies DNA accessibility on damaged chromatin. Mol Cell Biol 19:1673-1685.
11. Cedar H, Verdine GL (1999) Gene expression. The amazing demethylase. Nature 397:568-569.
12. Cheung KJ Jr, Mitchell D, Lin P, Li G (2001) The tumor suppressor candidate p33(ING1) mediates repair of UV-damaged DNA. Cancer Res 61:4974-4977.
13. Cleaver JE (2005) Cancer in xeroderma pigmentosum and related disorders of DNA repair. Nat Rev Cancer 5:564-573.
14. Cortellino S, Xu J, Sannai M, Moore R, Caretti E, Cigliano A, Le Coz M, Devarajan K, Wessels A, Soprano D et al (2011) Thymine DNA glycosylase is essential for active DNA demethylation by linked deamination-base excision repair. Cell 146:67-79.
15. D'Alessio AC, Weaver IC, Szyf M (2007) Acetylation-induced transcription is required for active DNA demethylation in methylation-silenced genes. Mol Cell Biol 27:7462-7474
16. de Boer J, Hoeijmakers JH (2000) Nucleotide excision repair and human syndromes. Carcinogenesis 21:453-460
17. Deaton AM, Bird A (2011) CpG islands and the regulation of transcription. Genes Dev 25:1010-1022.
18. Engel N, Tront JS, Erinle T, Nguyen N, Latham KE, Sapienza C, Hoffman B, Liebermann DA (2009) Conserved DNA methylation in Gadd45a(-/-) mice. Epigenetics 4:98-99.
19. Fornace AJ Jr, Alamo I Jr, Hollander MC (1988) DNA damage-inducible transcripts in mammalian cells. Proc Natl Acad Sci USA 85:8800-8804.
20. Fornace AJ Jr, Jackman J, Hollander MC, Hoffman-Liebermann B, Liebermann DA (1992) Genotoxic-stress-response genes and growth-arrest genes. gadd, MyD, and other genes induced by treatments eliciting growth arrest. Ann N Y Acad Sci 663:139-153.
21. Fromme JC, Verdine GL (2004) Base excision repair. Adv Protein Chem 69:1-41.
22. Gavin DP, Sharma RP, Chase KA, Matrisciano F, Dong E, Guidotti A (2012) Growth arrest and DNA-damage-inducible, beta (GADD45b)-mediated DNA demethylation in major psychosis. Neuropsychopharmacology 37:531-542.
23. Gjerset RA, Martin DW Jr (1982) Presence of a DNA demethylating activity in the nucleus of murine erythroleukemic cells. J Biol Chem 257:8581-8583.
24. Guo JU, Ma DK, Mo H, Ball MP, Jang MH, Bonaguidi MA, Balazer JA, Eaves HL, Xie B, Ford E et al (2011a) Neuronal activity modifies the DNA methylation landscape in the adult brain. Nat Neurosci 14:1345-1351.
25. Guo JU, Su Y, Zhong C, Ming GL, Song H (2011b) Hydroxylation of 5-methylcytosine by TET1 promotes active DNA demethylation in the adult brain. Cell 145:423-434.
26. Gupta M, Gupta SK, Balliet AG, Hollander MC, Fornace AJ, Hoffman B, Liebermann DA (2005) Hematopoietic cells from Gadd45a-and Gadd45b-deficient mice are sensitized to genotoxicstress-induced apoptosis. Oncogene 24:7170-7179.
27. Hackett JA, Surani MA (2013) DNA methylation dynamics during the mammalian life cycle. Philos Trans R Soc Lond B Biol Sci 368(1609):20110328.
28. Hackett JA, Sengupta R, Zylicz JJ, Murakami K, Lee C, Down TA, Surani MA (2013) Germline DNA demethylation dynamics and imprint erasure through 5-hydroxymethylcytosine. Science 339:448-452.
29. Hajkova P, Jeffries SJ, Lee C, Miller N, Jackson SP, Surani MA (2010) Genome-wide reprogramming in the mouse germ line entails the base excision repair pathway. Science 329:78-82.
30. He YF, Li BZ, Li Z, Liu P, Wang Y, Tang Q, Ding J, Jia Y, Chen Z, Li L et al (2011) Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 333:1303-1307.
31. Hildesheim J, Bulavin DV, Anver MR, Alvord WG, Hollander MC, Vardanian L, Fornace AJ Jr (2002) Gadd45a protects against UV irradiation-induced skin tumors, and promotes apoptosis and stress signaling via MAPK and p53. Cancer Res 62:7305-7315.
32. Hollander MC, Fornace AJ Jr (2002) Genomic instability, centrosome amplification, cell cycle checkpoints and Gadd45a. Oncogene 21:6228-6233.
33. Hollander MC, Sheikh MS, Bulavin DV, Lundgren K, Augeri-Henmueller L, Shehee R, Molinaro TA, Kim KE, Tolosa E, Ashwell JD et al (1999) Genomic instability in Gadd45a-deficient mice. Nat Genet 23:176-184.
34. Hollander MC, Kovalsky O, Salvador JM, Kim KE, Patterson AD, Haines DC, Fornace AJ Jr (2001) Dimethylbenzanthracene carcinogenesis in Gadd45a-null mice is associated with decreased DNA repair and increased mutation frequency. Cancer Res 61:2487-2491.
35. Hollander MC, Philburn RT, Patterson AD, Velasco-Miguel S, Friedberg EC, Linnoila RI, Fornace AJ Jr (2005) Deletion of XPC leads to lung tumors in mice and is associated with early events in human lung carcinogenesis. Proc Natl Acad Sci USA 102:13200-13205.
36. Hu XV, Rodrigues TM, Tao H, Baker RK, Miraglia L, Orth AP, Lyons GE, Schultz PG, Wu X (2010) Identification of RING finger protein 4 (RNF4) as a modulator of DNA demethylation through a functional genomics screen. Proc Natl Acad Sci USA 107:15087-15092.
37. Imamura T, Yamamoto S, Ohgane J, Hattori N, Tanaka S, Shiota K (2004) Non-coding RNA directed DNA demethylation of Sphk1 CpG island. Biochem Biophys Res Commun 322:593-600.
38. Inoue A, Zhang Y (2011) Replication-dependent loss of 5-hydroxymethylcytosine in mouse preimplantation embryos. Science 334:194.
39. Iqbal K, Jin SG, Pfeifer GP, Szabo PE (2011) Reprogramming of the paternal genome upon fertilization involves genome-wide oxidation of 5-methylcytosine. Proc Natl Acad Sci USA 108:3642-3647.
40. Ito S, Kuraoka I, Chymkowitch P, Compe E, Takedachi A, Ishigami C, Coin F, Egly JM, Tanaka K (2007) XPG stabilizes TFIIH, allowing transactivation of nuclear receptors: implications for Cockayne syndrome in XP-G/CS patients. Mol Cell 26:231-243.
41. Ito S, Shen L, Dai Q, Wu SC, Collins LB, Swenberg JA, He C, Zhang Y (2011) Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 333:1300-1303.
42. Jin S, Guo C, Pfeifer G (2008) GADD45A does not promote DNA demethylation. PLoS Genet 4:1-9.
43. Jones PA, Takai D (2001) The role of DNA methylation in mammalian epigenetics. Science 293:1068-1070.
44. Jost JP (1993) Nuclear extracts of chicken embryos promote an active demethylation of DNA by excision repair of 5-methyldeoxycytidine. Proc Natl Acad Sci USA 90:4684-4688.
45. Jung HJ, Kim EH, Mun JY, Park S, Smith ML, Han SS, Seo YR (2007) Base excision DNA repair defect in Gadd45a-deficient cells. Oncogene 26:7517-7525.
46. Kagiwada S, Kurimoto K, Hirota T, Yamaji M, Saitou M (2013) Replication-coupled passive DNA demethylation for the erasure of genome imprints in mice. EMBO J 32:340-353.
47. Kangaspeska S, Stride B, Metivier R, Polycarpou-Schwarz M, Ibberson D, Carmouche RP, Benes V, Gannon F, Reid G (2008) Transient cyclical methylation of promoter DNA. Nature 452:112-115.
48. Kaufmann LT, Gierl MS, Niehrs C (2011) Gadd45a, Gadd45b and Gadd45g expression during mouse embryonic development. Gene Expr Patterns 11:465-470.
49. Kearsey JM, Coates PJ, Prescott AR, Warbrick E, Hall PA (1995) Gadd45 is a nuclear cell cycle regulated protein which interacts with p21Cip1. Oncogene 11:1675-1683.
50. Kress C, Thomassin H, Grange T (2006) Active cytosine demethylation triggered by a nuclear receptor involves DNA strand breaks. Proc Natl Acad Sci USA 103:11112-11117.
51. Le May N, Egly JM, Coin F (2010a) True lies: the double life of the nucleotide excision repair factors in transcription and DNA repair. J Nucleic Acids. doi: 10.4061/2010/616342.
52. Le May N, Mota-Fernandes D, Velez-Cruz R, Iltis I, Biard D, Egly JM (2010b) NER factors are recruited to active promoters and facilitate chromatin modification for transcription in the absence of exogenous genotoxic attack. Mol Cell 38:54-66.
53. Lee B, Morano A, Porcellini A, Muller MT (2011) GADD45alpha inhibition of DNMT1 dependent DNA methylation during homology directed DNA repair. Nucleic Acids Res 40(6):2481-2493.
54. Li Y, Zhao M, Yin H, Gao F, Wu X, Luo Y, Zhao S, Zhang X, Su Y, Hu N et al (2010) Overexpression of the growth arrest and DNA damage-induced 45alpha gene contributes to autoimmunity by promoting DNA demethylation in lupus T cells. Arthritis Rheum 62:1438-1447.
55. Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, Tonti-Filippini J, Nery JR, Lee L, Ye Z, Ngo QM et al (2009) Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 462(7271):315-322.
56. Ma DK, Jang MH, Guo JU, Kitabatake Y, Chang ML, Pow-Anpongkul N, Flavell RA, Lu B, Ming GL, Song H (2009) Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science 323:1074-1077.
57. Maiti A, Drohat AC (2011) Thymine DNA glycosylase can rapidly excise 5-formylcytosine and 5-carboxylcytosine: potential implications for active demethylation of CpG sites. J Biol Chem 286:35334-35338.
58. Mak SK, Kultz D (2004) Gadd45 proteins induce G2/M arrest and modulate apoptosis in kidney cells exposed to hyperosmotic stress. J Biol Chem 279:39075-39084.
59. Matrisciano F, Dong E, Gavin DP, Nicoletti F, Guidotti A (2011) Activation of group II metabotropic glutamate receptors promotes DNA demethylation in the mouse brain. Mol Pharmacol 80:174-182.
60. Matzke M, Kanno T, Huettel B, Daxinger L, Matzke AJ (2007) Targets of RNA-directed DNA methylation. Curr Opin Plant Biol 10:512-519.
61. Mayer W, Niveleau A, Walter J, Fundele R, Haaf T (2000) Demethylation of the zygotic paternal genome. Nature 403:501-502.
62. Metivier R, Gallais R, Tiffoche C, Le Peron C, Jurkowska RZ, Carmouche RP, Ibberson D, Barath P, Demay F, Reid G et al (2008) Cyclical DNA methylation of a transcriptionally active promoter. Nature 452:45-50.
63. Mikkelsen TS, Hanna J, Zhang X, Ku M, Wernig M, Schorderet P, Bernstein BE, Jaenisch R, Lander ES, Meissner A (2008) Dissecting direct reprogramming through integrative genomic analysis. Nature 454:49-55.
64. Miller CA, Sweatt JD (2007) Covalent modification of DNA regulates memory formation. Neuron 53:857-869.
65. Niehrs C (2009) Active DNA demethylation and DNA repair. Differentiation 77:1-11.
66. Niehrs C, Schäfer A (2012) Active DNA demethylation by Gadd45 and DNA repair. Trends Cell Biol 22:220-227.
67. Oswald J, Engemann S, Lane N, Mayer W, Olek A, Fundele R, Dean W, Reik W, Walter J (2000) Active demethylation of the paternal genome in the mouse zygote. Curr Biol 10:475-478.
68. Rai K, Huggins IJ, James SR, Karpf AR, Jones DA, Cairns BR (2008) DNA demethylation in zebrafish involves the coupling of a deaminase, a glycosylase, and gadd45. Cell 135: 1201-1212.
69. Robertson AB, Klungland A, Rognes T, Leiros I (2009) DNA repair in mammalian cells: base excision repair: the long and short of it. Cell Mol Life Sci 66:981-993.
70. Santos F, Hendrich B, Reik W, Dean W (2002) Dynamic reprogramming of DNA methylation in the early mouse embryo. Dev Biol 241:172-182.
71. Santos-Rosa H, Schneider R, Bannister AJ, Sherriff J, Bernstein BE, Emre NC, Schreiber SL, Mellor J, Kouzarides T (2002) Active genes are tri-methylated at K4 of histone H3. Nature 419:407-411.
72. Schäfer A, Schomacher L, Barreto G, Doderlein G, Niehrs C (2010) Gemcitabine functions epigenetically by inhibiting repair mediated DNA demethylation. PLoS One 5:e14060.
73. Schäfer A, Karaulanov E, Stapf U, Doderlein G, Niehrs C (2013) Ing1 functions in DNA demethylation by directing Gadd45a to H3K4me3. Genes Dev 27:261-273.
74. Schmitz KM, Schmitt N, Hoffmann-Rohrer U, Schäfer A, Grummt I, Mayer C (2009) TAF12 recruits Gadd45a and the nucleotide excision repair complex to the promoter of rRNA genes leading to active DNA demethylation. Mol Cell 33:344-353.
75. Schneider R, Bannister AJ, Myers FA, Thorne AW, Crane-Robinson C, Kouzarides T (2004) Histone H3 lysine 4 methylation patterns in higher eukaryotic genes. Nat Cell Biol 6:73-77.
76. Seisenberger S, Andrews S, Krueger F, Arand J, Walter J, Santos F, Popp C, Thienpont B, Dean W, Reik W (2012) The dynamics of genome-wide DNA methylation reprogramming in mouse primordial germ cells. Mol Cell 48:849-862.
77. Sen GL, Reuter JA, Webster DE, Zhu L, Khavari PA (2010) DNMT1 maintains progenitor function in self-renewing somatic tissue. Nature 463:563-567.
78. Simonsson S, Gurdon J (2004) DNA demethylation is necessary for the epigenetic reprogramming of somatic cell nuclei. Nat Cell Biol 6:984-990.
79. Smith ML, Chen IT, Zhan Q, Bae I, Chen CY, Gilmer TM, Kastan MB, O'Connor PM, Fornace AJ Jr (1994) Interaction of the p53-regulated protein Gadd45 with proliferating cell nuclear antigen. Science 266:1376-1380.
80. Smith ML, Kontny HU, Zhan Q, Sreenath A, O'Connor PM, Fornace AJ Jr (1996) Antisense GADD45 expression results in decreased DNA repair and sensitizes cells to u.v.-irradiation or cisplatin. Oncogene 13:2255-2263.
81. Smith ML, Ford JM, Hollander MC, Bortnick RA, Amundson SA, Seo YR, Deng CX, Hanawalt PC, Fornace AJ Jr (2000) p53-mediated DNA repair responses to UV radiation: studies of mouse cells lacking p53, p21, and/or gadd45 genes. Mol Cell Biol 20:3705-3714.
82. Stadler MB, Murr R, Burger L, Ivanek R, Lienert F, Scholer A, van Nimwegen E, Wirbelauer C, Oakeley EJ, Gaidatzis D et al (2011) DNA-binding factors shape the mouse methylome at distal regulatory regions. Nature 480:490-495.
83. Sytnikova YA, Kubarenko AV, Schäfer A, Weber AN, Niehrs C (2011) Gadd45a is an RNA binding protein and is localized in nuclear speckles. PLoS One 6:e14500.
84. Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y, Agarwal S, Iyer LM, Liu DR, Aravind L et al (2009) Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324:930-935.
85. Takekawa M, Saito H (1998) A family of stress-inducible GADD45-like proteins mediate activation of the stress-responsive MTK1/MEKK4 MAPKKK. Cell 95:521-530.
86. Tian J, Huang H, Hoffman B, Liebermann DA, Ledda-Columbano GM, Columbano A, Locker J (2011) Gadd45beta is an inducible coactivator of transcription that facilitates rapid liver growth in mice. J Clin Invest 121:4491-4502.
87. Vairapandi M, Balliet AG, Fornace AJ Jr, Hoffman B, Liebermann DA (1996) The differentiation primary response gene MyD118, related to GADD45, encodes for a nuclear protein which interacts with PCNA and p21WAF1/CIP1. Oncogene 12:2579-2594.
88. Vairapandi M, Balliet AG, Hoffman B, Liebermann DA (2002) GADD45b and GADD45g are cdc2/cyclinB1 kinase inhibitors with a role in S and G2/M cell cycle checkpoints induced by genotoxic stress. J Cell Physiol 192:327-338.
89. Weiss A, Keshet I, Razin A, Cedar H (1996) DNA demethylation in vitro: involvement of RNA. Cell 86:709-718.
90. Wilks AF, Cozens PJ, Mattaj IW, Jost JP (1982) Estrogen induces a demethylation at the 5' end region of the chicken vitellogenin gene. Proc Natl Acad Sci USA 79:4252-4255.
91. Wossidlo M, Nakamura T, Lepikhov K, Marques CJ, Zakhartchenko V, Boiani M, Arand J, Nakano T, Reik W, Walter J (2011) 5-Hydroxymethylcytosine in the mammalian zygote is linked with epigenetic reprogramming. Nat Commun 2:241.
92. Wu SC, Zhang Y (2010) Active DNA demethylation: many roads lead to Rome. Nat Rev Mol Cell Biol 11:607-620.
93. Yi YW, Kim D, Jung N, Hong SS, Lee HS, Bae I (2000) Gadd45 family proteins are coactivators of nuclear hormone receptors. Biochem Biophys Res Commun 272:193-198.
94. Zhan Q, Lord KA, Alamo I Jr, Hollander MC, Carrier F, Ron D, Kohn KW, Hoffman B, Liebermann DA, Fornace AJ Jr (1994) The gadd and MyD genes define a novel set of mammalian genes encoding acidic proteins that synergistically suppress cell growth. Mol Cell Biol 14: 2361-2371.
95. Zhan Q, Fan S, Smith ML, Bae I, Yu K, Alamo I Jr, O'Connor PM, Fornace AJ Jr (1996) Abrogation of p53 function affects gadd gene responses to DNA base-damaging agents and starvation. DNA Cell Biol 15:805-815.
96. Zhan Q, Antinore MJ, Wang XW, Carrier F, Smith ML, Harris CC, Fornace AJ Jr (1999) Association with Cdc2 and inhibition of Cdc2/Cyclin B1 kinase activity by the p53-regulated protein Gadd45. Oncogene 18:2892-2900.
97. Zhang W, Bae I, Krishnaraju K, Azam N, Fan W, Smith K, Hoffman B, Liebermann DA (1999) CR6: a third member in the MyD118 and Gadd45 gene family which functions in negative growth control. Oncogene 18:4899-4907.
98. Zhang F, Pomerantz JH, Sen G, Palermo AT, Blau HM (2007) Active tissue-specific DNA demethylation conferred by somatic cell nuclei in stable heterokaryons. Proc Natl Acad Sci USA 104:4395-4400.
99. Zhang RP, Shao JZ, Xiang LX (2011) GADD45A protein plays an essential role in active DNA demethylation during terminal osteogenic differentiation of adipose-derived mesenchymal stem cells. J Biol Chem 286:41083-41094.
100. Zheng X, Pontes O, Zhu J, Miki D, Zhang F, Li WX, Iida K, Kapoor A, Pikaard CS, Zhu JK (2008) ROS3 is an RNA-binding protein required for DNA demethylation in Arabidopsis. Nature 455:1259-1262.