Inhibitor of growth 1 (ING1) acts at early steps of multiple DNA repair pathways

Molecular and Cellular Biochemistry

Volumn 378, Issue 1-2, 2013, Pages 117-126

  Ceruti, Julieta M ^a   Ogara, María F ^a   Menéndez, Camino ^b,c   Palmero, Ignacio ^b   Cánepa, Eduardo T ^a  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b INSTITUTO DE INVESTIGACIONES BIOMÉDICAS ALBERTO SOLS   (Spain)

^c Structural Biology and Biocomputing Programme   (Spain)

Author keywords

Checkpoint kinase 1; Chromatin structure; DNA damage response; DNA repair; Genotoxic stress; ING1; P53

Indexed keywords

BETA TUBULIN; GAMMA H2AX; HISTONE H2AX; HYDROGEN PEROXIDE; INHIBITOR OF GROWTH 1 PROTEIN; MESSENGER RNA; MUTANT PROTEIN; PROTEIN ING1B; PROTEIN P16; PROTEIN P21; PROTEIN P53; TRICHOSTATIN A; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG; ZINOSTATIN; CHECKPOINT KINASE 1; GAMMA H2AX PROTEIN, MOUSE; GAMMA-H2AX PROTEIN, MOUSE; HISTONE; ING1 PROTEIN, HUMAN; ISOPROTEIN; NUCLEAR PROTEIN; PROTEIN KINASE; SIGNAL PEPTIDE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL CYCLE ARREST; CELL TYPE; CONTROLLED STUDY; DNA DAMAGE; DNA REPAIR; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; ING1B GENE; NONHUMAN; PROTEIN DOMAIN; PROTEIN EXPRESSION; SENESCENCE; TRANSCRIPTION REGULATION; TUMOR GROWTH; TUMOR SUPPRESSOR GENE; UPREGULATION; WILD TYPE; ANIMAL; GENE EXPRESSION; GENOMIC INSTABILITY; HUMAN GENOME; METABOLISM; MISSENSE MUTATION; MOUSE; PHYSIOLOGY; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; DNA DAMAGE; DNA REPAIR; GENE EXPRESSION; GENOME, HUMAN; GENOMIC INSTABILITY; HISTONES; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MUTATION, MISSENSE; NUCLEAR PROTEINS; PROTEIN ISOFORMS; PROTEIN KINASES; TUMOR SUPPRESSOR PROTEINS; UP-REGULATION;

EID: 84886768858     PISSN: 03008177     EISSN: 15734919     Source Type: Journal    
DOI: 10.1007/s11010-013-1601-2     Document Type: Article

References (55)

1. Coles AH, Jones SN (2009) The ING gene family in the regulation of cell growth and tumorigenesis. J Cell Physiol 218:45-57
2. Li X, Kikuchi K, Takano Y (2011) ING genes work as tumor suppressor genes in the carcinogenesis of head and neck squamous cell carcinoma. J Oncol. doi:10.1155/2011/963614
3. Soliman MA, Riabowol K (2007) After a decade of study-ING, a PHD for a versatile family of proteins. Trends Biochem Sci 32:509-519
4. Nouman GS, Anderson JJ, Lunec J, Angus B (2003) The role of the tumour suppressor p33 ING1b in human neoplasia. J Clin Pathol 56:491-496
5. Ythier D, Larrieu D, Brambilla C, Brambilla E, Pedeux R (2008) The new tumor suppressor genes ING: genomic structure and status in cancer. Int J Cancer 123:1483-1490
6. Champagne KS, Kutateladze TG (2009) Structural insight into histone recognition by the ING PHD fingers. Curr Drug Targets 10:432-441
7. Doyon Y, Cayrou C, Ullah M, Landry AJ, Cote V, Selleck W, Lane WS, Tan S, Yang XJ, Cote J (2006) ING tumor suppressor proteins are critical regulators of chromatin acetylation required for genome expression and perpetuation. Mol Cell 21:51-64
8. Ludwig S, Klitzsch A, Baniahmad A (2011) The ING tumor suppressors in cellular senescence and chromatin. Cell Biosci 1: 25
9. Abad M, Moreno A, Palacios A, Narita M, Blanco F, Moreno-Bueno G, Narita M and Palmero I (2011) The tumor suppressor ING1 contributes to epigenetic control of cellular senescence. Aging Cell 10: 158-171
10. Garkavtsev I, Kozin SV, Chernova O, Xu L, Winkler F, Brown E, Barnett GH, Jain RK (2004) The candidate tumour suppressor protein ING4 regulates brain tumour growth and angiogenesis. Nature 428:328-332
11. Gomez-Cabello D, Callejas S, Benguria A, Moreno A, Alonso J and Palmero I (2010) Regulation of the microRNA processor DGCR8 by the tumor suppressor ING1. Cancer Res 70: 1866-1874
12. Nozell S, Laver T, Moseley D, Nowoslawski L, De Vos M, Atkinson GP, Harrison K, Nabors LB, Benveniste EN (2008) The ING4 tumor suppressor attenuates NF-kappaB activity at the promoters of target genes. Mol Cell Biol 28:6632-6645
13. Xin H, Yoon HG, Singh PB, Wong J, Qin J (2004) Components of a pathway maintaining histone modification and heterochromatin protein 1 binding at the pericentric heterochromatin in Mammalian cells. J Biol Chem 279:9539-9546
14. Abad M, Menendez C, Fuchtbauer A, Serrano M, Fuchtbauer EM, Palmero I (2007) Ing1 mediates p53 accumulation and chromatin modification in response to oncogenic stress. J Biol Chem 282:31060-31067
15. Huertas D, Sendra R, Munoz P (2009) Chromatin dynamics coupled to DNA repair. Epigenetics 4:31-42
16. Scott M, Bonnefin P, Vieyra D, Boisvert FM, Young D, Bazett- Jones DP, Riabowol K (2001) UV-induced binding of ING1 to PCNA regulates the induction of apoptosis. J Cell Sci 114: 3455-3462
17. Wong RP, Lin H, Khosravi S, Piche B, Jafarnejad SM, Chen DW, Li G (2011) Tumour suppressor ING1b maintains genomic stability upon replication stress. Nucleic Acids Res 39: 3632-3642
18. 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
19. Kuo WH, Wang Y, Wong RP, Campos EI, Li G (2007) The ING1b tumor suppressor facilitates nucleotide excision repair by promoting chromatin accessibility to XPA. Exp Cell Res 313: 1628-1638
20. Campos EI, Martinka M, Mitchell DL, Dai DL, Li G (2004) Mutations of the ING1 tumor suppressor gene detected in human melanoma abrogate nucleotide excision repair. Int J Oncol 25: 73-80
21. Garate M, Campos EI, Bush JA, Xiao H, Li G (2007) Phosphorylation of the tumor suppressor p33(ING1b) at Ser-126 influences its protein stability and proliferation of melanoma cells. FASEB J 21:3705-3716
22. Goeman F, Thormeyer D, Abad M, Serrano M, Schmidt O, Palmero I, Baniahmad A (2005) Growth inhibition by the tumor suppressor p33ING1 in immortalized and primary cells: involvement of two silencing domains and effect of Ras. Mol Cell Biol 25:422-431
23. Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156-159
24. Palmero I, Murga M, Zubiaga A, Serrano M (2002) Activation of ARF by oncogenic stress in mouse fibroblasts is independent of E2F1 and E2F2. Oncogene 21:2939-2947
25. Gonzalez L, Freije JM, Cal S, Lopez-Otin C, Serrano M, Palmero I (2006) A functional link between the tumour suppressors ARF and p33ING1. Oncogene 25:5173-5179
26. Cheung KJ Jr., Bush JA, Jia W, Li G (2000) Expression of the novel tumour suppressor p33(ING1)is independent of p53. Br J Cancer 83: 1468-1472
27. Gunduz M, Ouchida M, Fukushima K, Hanafusa H, Etani T, Nishioka S, Nishizaki K, Shimizu K (2000) Genomic structure of the human ING1 gene and tumor-specific mutations detected in head and neck squamous cell carcinomas. Cancer Res 60: 3143-3146
28. Chen L, Matsubara N, Yoshino T, Nagasaka T, Hoshizima N, Shirakawa Y, Naomoto Y, Isozaki H, Riabowol K, Tanaka N (2001) Genetic alterations of candidate tumor suppressor ING1 in human esophageal squamous cell cancer. Cancer Res 61:4345-4349
29. Rogakou EP, Boon C, Redon C, Bonner WM (1999) Megabase chromatin domains involved in DNA double-strand breaks in vivo. J Cell Biol 146:905-916
30. Fernandez-Capetillo O, Lee A, Nussenzweig M, Nussenzweig A (2004) H2AX: the histone guardian of the genome. DNA Repair (Amst) 3:959-967
31. Kim JA, Kruhlak M, Dotiwala F, Nussenzweig A, Haber JE (2007) Heterochromatin is refractory to gamma-H2AX modification in yeast and mammals. J Cell Biol 178:209-218
32. Murga M, Jaco I, Fan Y, Soria R, Martinez-Pastor B, Cuadrado M, Yang SM, Blasco MA, Skoultchi AI, Fernandez-Capetillo O (2007) Global chromatin compaction limits the strength of the DNA damage response. J Cell Biol 178:1101-1108
33. Skowyra D, Zeremski M, Neznanov N, Li M, Choi Y, Uesugi M, Hauser CA, Gu W, Gudkov AV, Qin J (2001) Differential association of products of alternative transcripts of the candidate tumor suppressor ING1 with the mSin3/HDAC1 transcriptional corepressor complex. J Biol Chem 276:8734-8739
34. Kuzmichev A, Zhang Y, Erdjument-Bromage H, Tempst P, Reinberg D (2002) Role of the Sin3-histone deacetylase complex in growth regulation by the candidate tumor suppressor p33(ING1). Mol Cell Biol 22:835-848
35. Vieyra D, Loewith R, Scott M, Bonnefin P, Boisvert FM, Cheema P, Pastyryeva S, Meijer M, Johnston RN, Bazett-Jones DP, McMahon S, Cole MD, Young D, Riabowol K (2002) Human ING1 proteins differentially regulate histone acetylation. J Biol Chem 277:29832-29839
36. Garkavtsev I, Grigorian IA, Ossovskaya VS, Chernov MV, Chumakov PM, Gudkov AV (1998) The candidate tumour suppressor p33ING1 cooperates with p53 in cell growth control. Nature 391:295-298
37. Shiseki M, Nagashima M, Pedeux RM, Kitahama-Shiseki M, Miura K, Okamura S, Onogi H, Higashimoto Y, Appella E, Yokota J, Harris CC (2003) p29ING4 and p28ING5 bind to p53 and p300, and enhance p53 activity. Cancer Res 63:2373-2378
38. Nagashima M, Shiseki M, Miura K, Hagiwara K, Linke SP, Pedeux R, Wang XW, Yokota J, Riabowol K, Harris CC (2001) DNA damage-inducible gene p33ING2 negatively regulates cell proliferation through acetylation of p53. Proc Natl Acad Sci USA 98:9671-9676
39. Nagashima M, Shiseki M, Pedeux RM, Okamura S, Kitahama- Shiseki M, Miura K, Yokota J, Harris CC (2003) A novel PHDfinger motif protein, p47ING3, modulates p53-mediated transcription, cell cycle control, and apoptosis. Oncogene 22: 343-350
40. Pedeux R, Sengupta S, Shen JC, Demidov ON, Saito S, Onogi H, Kumamoto K, Wincovitch S, Garfield SH, McMenamin M, Nagashima M, Grossman SR, Appella E, Harris CC (2005) ING2 regulates the onset of replicative senescence by induction of p300-dependent p53 acetylation. Mol Cell Biol 25:6639-6648
41. Doyon Y, Selleck W, Lane WS, Tan S, Cote J (2004) Structural and functional conservation of the NuA4 histone acetyltransferase complex from yeast to humans. Mol Cell Biol 24:1884-1896
42. Kichina JV, Zeremski M, Aris L, Gurova KV, Walker E, Franks R, Nikitin AY, Kiyokawa H, Gudkov AV (2006) Targeted disruption of the mouse ing1 locus results in reduced body size, hypersensitivity to radiation and elevated incidence of lymphomas. Oncogene 25:857-866
43. Tsang FC, Po LS, Leung KM, Lau A, Siu WY, Poon RY (2003) ING1b decreases cell proliferation through p53-dependent and -independent mechanisms. FEBS Lett 553:277-285
44. Kataoka H, Bonnefin P, Vieyra D, Feng X, Hara Y, Miura Y, Joh T, Nakabayashi H, Vaziri H, Harris CC, Riabowol K (2003) ING1 represses transcription by direct DNA binding and through effects on p53. Cancer Res 63:5785-5792
45. Tamannai M, Farhangi S, Truss M, Sinn B, Wurm R, Bose P, Henze G, Riabowol K, von Deimling A, Tallen G (2010) The inhibitor of growth 1 (ING1) is involved in trichostatin A-induced apoptosis and caspase 3 signaling in p53-deficient glioblastoma cells. Oncol Res 18: 469-480
46. Hara Y, Zheng Z, Evans SC, Malatjalian D, Riddell DC, Guernsey DL, Wang LD, Riabowol K, Casson AG (2003) ING1 and p53 tumor suppressor gene alterations in adenocarcinomas of the esophagogastric junction. Cancer Lett 192:109-116
47. Hazra TK, Das A, Das S, Choudhury S, Kow YW, Roy R (2007) Oxidative DNA damage repair in mammalian cells: a new perspective. DNA Repair (Amst) 6:470-480
48. Hatayama T, Yukioka M (1982) Action of neocarzinostatin on cell nuclei: release of specific chromatin. Biochem Biophys Res Commun 104:889-896
49. Kappen LS, Ellenberger TE, Goldberg IH (1987) Mechanism and base specificity of DNA breakage in intact cells by neocarzinostatin. Biochemistry 26:384-390
50. Shi X, Gozani O (2005) The fellowships of the INGs. J Cell Biochem 96:1127-1136
51. Pena PV, Hom RA, Hung T, Lin H, Kuo AJ, Wong RP, Subach OM, Champagne KS, Zhao R, Verkhusha VV, Li G, Gozani O, Kutateladze TG (2008) Histone H3K4me3 binding is required for the DNA repair and apoptotic activities of ING1 tumor suppressor. J Mol Biol 380:303-312
52. Gibbons RJ, Bachoo S, Picketts DJ, Aftimos S, Asenbauer B, Bergoffen J, Berry SA, Dahl N, Fryer A, Keppler K, Kurosawa K, Levin ML, Masuno M, Neri G, Pierpont ME, Slaney SF, Higgs DR (1997) Mutations in transcriptional regulator ATRX establish the functional significance of a PHD-like domain. Nat Genet 17:146-148
53. Saugier-Veber P, Drouot N, Wolf LM, Kuhn JM, Frebourg T, Lefebvre H (2001) Identification of a novel mutation in the autoimmune regulator (AIRE-1) gene in a French family with autoimmune polyendocrinopathy-candidiasis- ectodermal dystrophy. Eur J Endocrinol 144:347-351
54. Elkin SK, Ivanov D, Ewalt M, Ferguson CG, Hyberts SG, Sun ZY, Prestwich GD, Yuan J, Wagner G, Oettinger MA, Gozani OP (2005) A PHD finger motif in the C terminus of RAG2 modulates recombination activity. J Biol Chem 280:28701-28710
55. Stark M, Puig-Butille JA, Walker G, Badenas C, Malvehy J, Hayward N, Puig S (2006) Mutation of the tumour suppressor p33ING1b is rare in melanoma. Br J Dermatol 155:94-99