ING1 and ING2: Multifaceted tumor suppressor genes

Cellular and Molecular Life Sciences

Volumn 70, Issue 20, 2013, Pages 3753-3772

  Guérillon, Claire ^a,b   Larrieu, Delphine ^d   Pedeux, Rémy ^a,b,c  

^a INSERM U917   (France)

^b UNIVERSITÉ DE RENNES 1   (France)

^c ETABLISSEMENT FRANÇAIS DU SANG   (France)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

H3K4Me3; ING1; ING2; p53; Tumor suppressor gene

Indexed keywords

INHIBITOR OF GROWTH 1 PROTEIN; INHIBITOR OF GROWTH 2 PROTEIN; ISOPROTEIN; ONCOPROTEIN; PROTEIN P53; PROTEIN P73; PROTEIN P73 ALPHA; UNCLASSIFIED DRUG;

ACETYLATION; ALTERNATIVE RNA SPLICING; APOPTOSIS; CELL AGING; CELL CYCLE; DNA REPAIR; DNA REPLICATION; EXON; EXPERIMENTAL MODEL; GENE EXPRESSION; GENE FREQUENCY; GENE FUNCTION; GENE MUTATION; GENOMIC INSTABILITY; HETEROZYGOSITY LOSS; HUMAN; INHIBITOR OF GROWTH 1 GENE; INHIBITOR OF GROWTH 2 GENE; KNOCKOUT MOUSE; MALIGNANT NEOPLASTIC DISEASE; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REVIEW; SEQUENCE ANALYSIS; STRUCTURE ACTIVITY RELATION; TELOMERE; TRANSCRIPTION REGULATION; TUMOR SUPPRESSOR GENE; ULTRAVIOLET RADIATION;

AMINO ACID SEQUENCE; ANIMALS; APOPTOSIS; BASE SEQUENCE; DNA REPAIR; DNA REPLICATION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENOMIC INSTABILITY; HOMEODOMAIN PROTEINS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; MICE, KNOCKOUT; MOLECULAR SEQUENCE DATA; NUCLEAR PROTEINS; RECEPTORS, CYTOPLASMIC AND NUCLEAR; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEINS;

MUS;

EID: 84884903165     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-013-1270-z     Document Type: Review

References (130)

1. Kinzler KW, Vogelstein B (1997) Cancer-susceptibility genes. Gatekeepers and caretakers. Nature 386 (6627):761, 763. doi: 10.1038/386761a0
2. Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144(5):646-674. doi: 10.1016/j.cell.2011.02.013
3. Garkavtsev I, Kazarov A, Gudkov A, Riabowol K (1996) Suppression of the novel growth inhibitor p33ING1 promotes neoplastic transformation. Nat Genet 14(4):415-420. doi: 10.1038/ng1296-415
4. 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(17):9671-9676. doi: 10.1073/pnas.161151798
5. Nagashima M, Shiseki M, Pedeux RM, Okamura S, Kitahama-Shiseki M, Miura K, Yokota J, Harris CC (2003) A novel PHD-finger motif protein, p47ING3, modulates p53-mediated transcription, cell cycle control, and apoptosis. Oncogene 22(3):343-350. doi: 10.1038/sj.onc.1206115
6. Shimada Y, Saito A, Suzuki M, Takahashi E, Horie M (1998) Cloning of a novel gene (ING1L) homologous to ING1, a candidate tumor suppressor. Cytogenet Cell Genet 83(3-4):232-235. doi: ccg83232
7. 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(10):2373-2378
8. Loewith R, Meijer M, Lees-Miller SP, Riabowol K, Young D (2000) Three yeast proteins related to the human candidate tumor suppressor p33(ING1) are associated with histone acetyltransferase activities. Mol Cell Biol 20(11):3807-3816
9. He GH, Helbing CC, Wagner MJ, Sensen CW, Riabowol K (2005) Phylogenetic analysis of the ING family of PHD finger proteins. Mol Biol Evol 22(1):104-116. doi: 10.1093/molbev/msh256msh256
10. Soliman MA, Riabowol K (2007) After a decade of study-ING, a PHD for a versatile family of proteins. Trends Biochem Sci 32(11):509-519. doi: 10.1016/j.tibs.2007.08.006
11. Lee WY, Lee D, Chung WI, Kwon CS (2009) Arabidopsis ING and Alfin1-like protein families localize to the nucleus and bind to H3K4me3/2 via plant homeodomain fingers. Plant J 58(3):511-524. doi: 10.1111/j.1365-313X.2009.03795. x
12. Wagner MJ, Gogela-Spehar M, Skirrow RC, Johnston RN, Riabowol K, Helbing CC (2001) Expression of novel ING variants is regulated by thyroid hormone in the Xenopus laevis tadpole. J Biol Chem 276(50):47013-47020. doi: 10.1074/jbc.M106965200M106965200
13. 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(7):1483-1490. doi: 10.1002/ijc.23790
14. 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(6):857-866. doi: 10.1038/sj.onc.1209118
15. Coles AH, Liang H, Zhu Z, Marfella CG, Kang J, Imbalzano AN, Jones SN (2007) Deletion of p37Ing1 in mice reveals a p53-independent role for Ing1 in the suppression of cell proliferation, apoptosis, and tumorigenesis. Cancer Res 67(5):2054-2061. doi: 10.1158/0008-5472.CAN-06-3558
16. Coles AH, Marfella CG, Imbalzano AN, Steinman HA, Garlick DS, Gerstein RM, Jones SN (2008) p37Ing1b regulates B-cell proliferation and cooperates with p53 to suppress diffuse large B-cell lymphomagenesis. Cancer Res 68(21):8705-8714. doi: 10.1158/0008-5472.CAN-08-0923
17. Saito M, Kumamoto K, Robles AI, Horikawa I, Furusato B, Okamura S, Goto A, Yamashita T, Nagashima M, Lee TL, Baxendale VJ, Rennert OM, Takenoshita S, Yokota J, Sesterhenn IA, Trivers GE, Hussain SP, Harris CC (2010) Targeted disruption of ing2 results in defective spermatogenesis and development of soft-tissue sarcomas. PLoS ONE 5(11):e15541. doi: 10.1371/journal.pone.0015541
18. Zeremski M, Hill JE, Kwek SS, Grigorian IA, Gurova KV, Garkavtsev IV, Diatchenko L, Koonin EV, Gudkov AV (1999) Structure and regulation of the mouse ing1 gene. Three alternative transcripts encode two phd finger proteins that have opposite effects on p53 function. J Biol Chem 274(45):32172-32181
19. Walzak AA, Veldhoen N, Feng X, Riabowol K, Helbing CC (2008) Expression profiles of mRNA transcript variants encoding the human inhibitor of growth tumor suppressor gene family in normal and neoplastic tissues. Exp Cell Res 314(2):273-285. doi: 10.1016/j.yexcr.2007.07.029
20. 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(11):1468-1472. doi: 10.1054/bjoc.2000.1464
21. Unoki M, Kumamoto K, Robles AI, Shen JC, Zheng ZM, Harris CC (2008) A novel ING2 isoform, ING2b, synergizes with ING2a to prevent cell cycle arrest and apoptosis. FEBS Lett 582(28):3868-3874. doi: 10.1016/j.febslet.2008.10.024
22. Kumamoto K, Spillare EA, Fujita K, Horikawa I, Yamashita T, Appella E, Nagashima M, Takenoshita S, Yokota J, Harris CC (2008) Nutlin-3a activates p53 to both down-regulate inhibitor of growth 2 and up-regulate mir-34a, mir-34b, and mir-34c expression, and induce senescence. Cancer Res 68(9):3193-3203. doi: 10.1158/0008-5472.CAN-07-2780
23. Kumamoto K, Fujita K, Kurotani R, Saito M, Unoki M, Hagiwara N, Shiga H, Bowman ED, Yanaihara N, Okamura S, Nagashima M, Miyamoto K, Takenoshita S, Yokota J, Harris CC (2009) ING2 is upregulated in colon cancer and increases invasion by enhanced MMP13 expression. Int J Cancer 125(6):1306-1315. doi: 10.1002/ijc.24437
24. Eapen SA, Netherton SJ, Sarker KP, Deng L, Chan A, Riabowol K, Bonni S (2012) Identification of a novel function for the chromatin remodeling protein ING2 in muscle differentiation. PLoS ONE 7(7):e40684. doi: 10.1371/journal.pone. 0040684
25. Gozani O, Karuman P, Jones DR, Ivanov D, Cha J, Lugovskoy AA, Baird CL, Zhu H, Field SJ, Lessnick SL, Villasenor J, Mehrotra B, Chen J, Rao VR, Brugge JS, Ferguson CG, Payrastre B, Myszka DG, Cantley LC, Wagner G, Divecha N, Prestwich GD, Yuan J (2003) The PHD finger of the chromatin-associated protein ING2 functions as a nuclear phosphoinositide receptor. Cell 114(1):99-111. doi: S009286740300480X
26. Pena PV, Davrazou F, Shi X, Walter KL, Verkhusha VV, Gozani O, Zhao R, Kutateladze TG (2006) Molecular mechanism of histone H3K4me3 recognition by plant homeodomain of ING2. Nature 442(7098):100-103. doi: 10.1038/nature04814
27. Shi X, Hong T, Walter KL, Ewalt M, Michishita E, Hung T, Carney D, Pena P, Lan F, Kaadige MR, Lacoste N, Cayrou C, Davrazou F, Saha A, Cairns BR, Ayer DE, Kutateladze TG, Shi Y, Cote J, Chua KF, Gozani O (2006) ING2 PHD domain links histone H3 lysine 4 methylation to active gene repression. Nature 442(7098):96-99. doi: 10.1038/nature04835
28. 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(3):835-848
29. 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(2):303-312. doi: 10.1016/j.jmb.2008.04.061
30. 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(12):8734-8739. doi: 10.1074/jbc.M007664200
31. Yaffe MB, Rittinger K, Volinia S, Caron PR, Aitken A, Leffers H, Gamblin SJ, Smerdon SJ, Cantley LC (1997) The structural basis for 14-3-3:phosphopeptide binding specificity. Cell 91(7):961-971
32. Gong W, Russell M, Suzuki K, Riabowol K (2006) Subcellular targeting of p33ING1b by phosphorylation-dependent 14-3-3 binding regulates p21WAF1 expression. Mol Cell Biol 26(8):2947-2954. doi: 10.1128/MCB.26.8.2947-2954.2006
33. Russell MW, Soliman MA, Schriemer D, Riabowol K (2008) ING1 protein targeting to the nucleus by karyopherins is necessary for activation of p21. Biochem Biophys Res Commun 374(3):490-495. doi: 10.1016/j.bbrc.2008.07.076
34. 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(Pt 19):3455-3462
35. Han X, Feng X, Rattner JB, Smith H, Bose P, Suzuki K, Soliman MA, Scott MS, Burke BE, Riabowol K (2008) Tethering by lamin A stabilizes and targets the ING1 tumour suppressor. Nat Cell Biol 10(11):1333-1340. doi: 10.1038/ncb1792
36. Feng X, Hara Y, Riabowol K (2002) Different HATS of the ING1 gene family. Trends Cell Biol 12(11):532-538
37. Coles AH, Jones SN (2009) The ING gene family in the regulation of cell growth and tumorigenesis. J Cell Physiol 218(1):45-57. doi: 10.1002/jcp.21583
38. Culurgioni S, Munoz IG, Moreno A, Palacios A, Villate M, Palmero I, Montoya G, Blanco FJ (2012) The crystal structure of the inhibitor of growth 4 (ING4) dimerization domain reveals the functional organization of the ING family of chromatin binding proteins. J Biol Chem. doi: 10.1074/jbc.M111.330001
39. Palacios A, Moreno A, Oliveira BL, Rivera T, Prieto J, Garcia P, Fernandez-Fernandez MR, Bernado P, Palmero I, Blanco FJ (2010) The dimeric structure and the bivalent recognition of H3K4me3 by the tumor suppressor ING4 suggests a mechanism for enhanced targeting of the HBO1 complex to chromatin. J Mol Biol 396(4):1117-1127. doi: 10.1016/j.jmb.2009.12.049
40. 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(13):3705-3716. doi: 10.1096/fj.07-8069com
41. Garate M, Wong RP, Campos EI, Wang Y, Li G (2008) NAD(P)H quinone oxidoreductase 1 inhibits the proteasomal degradation of the tumour suppressor p33(ING1b). EMBO Rep 9(6):576-581. doi: 10.1038/embor.2008.48
42. Nie J, Liu L, Wu M, Xing G, He S, Yin Y, Tian C, He F, Zhang L (2010) HECT ubiquitin ligase Smurf1 targets the tumor suppressor ING2 for ubiquitination and degradation. FEBS Lett 584(14):3005-3012. doi: 10.1016/j.febslet.2010.05.033
43. Chen C, Matesic LE (2007) The Nedd4-like family of E3 ubiquitin ligases and cancer. Cancer Metastas Rev 26(3-4):587-604. doi: 10.1007/s10555-007-9091-x
44. Kwei KA, Shain AH, Bair R, Montgomery K, Karikari CA, van de Rijn M, Hidalgo M, Maitra A, Bashyam MD, Pollack JR (2011) SMURF1 amplification promotes invasiveness in pancreatic cancer. PLoS ONE 6(8):e23924. doi: 10.1371/journal.pone.002392
45. Ythier D, Brambilla E, Binet R, Nissou D, Vesin A, de Fraipont F, Moro-Sibilot D, Lantuejoul S, Brambilla C, Gazzeri S, Pedeux R (2010) Expression of candidate tumor suppressor gene ING2 is lost in non-small cell lung carcinoma. Lung Cancer 69(2):180-186. doi: 10.1016/j.lungcan.2009.11.006
46. Gunduz M, Gunduz E, Rivera RS, Nagatsuka H (2008) The inhibitor of growth (ING) gene family: potential role in cancer therapy. Curr Cancer Drug Targets 8(4):275-284
47. 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(11):4345-4349
48. Tokunaga E, Maehara Y, Oki E, Kitamura K, Kakeji Y, Ohno S, Sugimachi K (2000) Diminished expression of ING1 mRNA and the correlation with p53 expression in breast cancers. Cancer Lett 152(1):15-22
49. Toyama T, Iwase H, Watson P, Muzik H, Saettler E, Magliocco A, DiFrancesco L, Forsyth P, Garkavtsev I, Kobayashi S, Riabowol K (1999) Suppression of ING1 expression in sporadic breast cancer. Oncogene 18(37):5187-5193. doi: 10.1038/sj.onc.1202905
50. Chen B, Campos EI, Crawford R, Martinka M, Li G (2003) Analyses of the tumour suppressor ING1 expression and gene mutation in human basal cell carcinoma. Int J Oncol 22(4):927-931
51. Nouman GS, Anderson JJ, Crosier S, Shrimankar J, Lunec J, Angus B (2003) Downregulation of nuclear expression of the p33(ING1b) inhibitor of growth protein in invasive carcinoma of the breast. J Clin Pathol 56(7):507-511
52. Takahashi M, Ozaki T, Todo S, Nakagawara A (2004) Decreased expression of the candidate tumor suppressor gene ING1 is associated with poor prognosis in advanced neuroblastomas. Oncol Rep 12(4):811-816
53. Zhang HK, Pan K, Wang H, Weng DS, Song HF, Zhou J, Huang W, Li JJ, Chen MS, Xia JC (2008) Decreased expression of ING2 gene and its clinicopathological significance in hepatocellular carcinoma. Cancer Lett 261(2):183-192. doi: 10.1016/j.canlet.2007.11.019
54. Borkosky SS, Gunduz M, Nagatsuka H, Beder LB, Gunduz E, Ali MA, Rodriguez AP, Cilek MZ, Tominaga S, Yamanaka N, Shimizu K, Nagai N (2009) Frequent deletion of ING2 locus at 4q35.1 associates with advanced tumor stage in head and neck squamous cell carcinoma. J Cancer Res Clin Oncol 135(5):703-713. doi: 10.1007/s00432-008-0507-y
55. Sironi E, Cerri A, Tomasini D, Sirchia SM, Porta G, Rossella F, Grati FR, Simoni G (2004) Loss of heterozygosity on chromosome 4q32-35 in sporadic basal cell carcinomas: evidence for the involvement of p33ING2/ING1L and SAP30 genes. J Cutan Pathol 31(4):318-322. doi: 187
56. Zhang H, Ma H, Wang Q, Chen M, Weng D, Wang H, Zhou J, Li Y, Sun J, Chen Y, Liang X, Zhao J, Pan K, Xia J (2010) Analysis of loss of heterozygosity on chromosome 4q in hepatocellular carcinoma using high-throughput SNP array. Oncol Rep 23(2):445-455
57. Okano T, Gemma A, Hosoya Y, Hosomi Y, Nara M, Kokubo Y, Yoshimura A, Shibuya M, Nagashima M, Harris CC, Kudoh S (2006) Alterations in novel candidate tumor suppressor genes, ING1 and ING2 in human lung cancer. Oncol Rep 15(3):545-549
58. Lu F, Dai DL, Martinka M, Ho V, Li G (2006) Nuclear ING2 expression is reduced in human cutaneous melanomas. Br J Cancer 95(1):80-86. doi: 10.1038/sj.bjc.6603205
59. Vieyra D, Senger DL, Toyama T, Muzik H, Brasher PM, Johnston RN, Riabowol K, Forsyth PA (2003) Altered subcellular localization and low frequency of mutations of ING1 in human brain tumors. Clin Cancer Res 9(16 Pt 1):5952-5961
60. Engelmann D, Putzer BM (2012) The dark side of E2F1: in transit beyond apoptosis. Cancer Res 72(3):571-575. doi: 10.1158/0008-5472.CAN-11-2575
61. Guo XB, Jing CQ, Li LP, Zhang L, Shi YL, Wang JS, Liu JL, Li CS (2011) Down-regulation of miR-622 in gastric cancer promotes cellular invasion and tumor metastasis by targeting ING1 gene. World J Gastroenterol 17(14):1895-1902. doi: 10.3748/wjg.v17.i14.1895
62. Bannister AJ, Kouzarides T (2004) Histone methylation: recognizing the methyl mark. Methods Enzymol 376:269-288. doi: 10.1016/S0076-6879(03)76018-2
63. Abad M, Moreno A, Palacios A, Narita M, Blanco F, Moreno-Bueno G, Palmero I (2011) The tumor suppressor ING1 contributes to epigenetic control of cellular senescence. Aging Cell 10(1):158-171. doi: 10.1111/j.1474-9726.2010. 00651.x
64. 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(33):29832-29839. doi: 10.1074/jbc.M200197200
65. Gomez-Cabello D, Callejas S, Benguria A, Moreno A, Alonso J, Palmero I (2010) Regulation of the microRNA processor DGCR8 by the tumor suppressor ING1. Cancer Res 70(5):1866-1874. doi: 10.1158/0008-5472.CAN-09-2088
66. Shi XB, Tepper CG, deVere White RW (2008) Cancerous miRNAs and their regulation. Cell Cycle 7(11):1529-1538
67. Takahashi M, Seki N, Ozaki T, Kato M, Kuno T, Nakagawa T, Watanabe K, Miyazaki K, Ohira M, Hayashi S, Hosoda M, Tokita H, Mizuguchi H, Hayakawa T, Todo S, Nakagawara A (2002) Identification of the p33(ING1)-regulated genes that include cyclin B1 and proto-oncogene DEK by using cDNA microarray in a mouse mammary epithelial cell line NMuMG. Cancer Res 62(8):2203-2209
68. Li N, Li Q, Cao X, Zhao G, Xue L, Tong T (2011) The tumor suppressor p33ING1b upregulates p16INK4a expression and induces cellular senescence. FEBS Lett 585(19):3106-3112. doi: 10.1016/j.febslet.2011.08.044
69. 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(18):5785-5792
70. Shimada H, Liu TL, Ochiai T, Shimizu T, Haupt Y, Hamada H, Abe T, Oka M, Takiguchi M, Hiwasa T (2002) Facilitation of adenoviral wild-type p53-induced apoptotic cell death by overexpression of p33(ING1) in T.Tn human esophageal carcinoma cells. Oncogene 21(8):1208-1216. doi: 10.1038/sj.onc.1205176
71. 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(6664):295-298. doi: 10.1038/34675
72. Helbing CC, Veillette C, Riabowol K, Johnston RN, Garkavtsev I (1997) A novel candidate tumor suppressor, ING1, is involved in the regulation of apoptosis. Cancer Res 57(7):1255-1258
73. Soliman MA, Berardi P, Pastyryeva S, Bonnefin P, Feng X, Colina A, Young D, Riabowol K (2008) ING1a expression increases during replicative senescence and induces a senescent phenotype. Aging Cell 7(6):783-794. doi: 10.1111/j.1474-9726.2008.00427.x
74. Vieyra D, Toyama T, Hara Y, Boland D, Johnston R, Riabowol K (2002) ING1 isoforms differentially affect apoptosis in a cell age-dependent manner. Cancer Res 62(15):4445-4452
75. 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(42):31060-31067. doi: 10.1074/jbc.M701639200
76. 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(3):277-285
77. Leung KM, Po LS, Tsang FC, Siu WY, Lau A, Ho HT, Poon RY (2002) The candidate tumor suppressor ING1b can stabilize p53 by disrupting the regulation of p53 by MDM2. Cancer Res 62(17):4890-4893
78. Zawacka-Pankau J, Kostecka A, Sznarkowska A, Hedstrom E, Kawiak A (2010) p73 tumor suppressor protein: a close relative of p53 not only in structure but also in anti-cancer approach? Cell Cycle 9(4):720-728
79. Melino G (2011) p63 is a suppressor of tumorigenesis and metastasis interacting with mutant p53. Cell Death Differ 18(9):1487-1499. doi: 10.1038/cdd.2011.81
80. Allocati N, Di Ilio C, De Laurenzi V (2012) p63/p73 in the control of cell cycle and cell death. Exp Cell Res 318(11):1285-1290. doi: 10.1016/j.yexcr.2012.01.023
81. Binda O, Nassif C, Branton PE (2008) SIRT1 negatively regulates HDAC1-dependent transcriptional repression by the RBP1 family of proteins. Oncogene 27(24):3384-3392. doi: 10.1038/sj.onc.1211014
82. Shieh SY, Ikeda M, Taya Y, Prives C (1997) DNA damage-induced phosphorylation of p53 alleviates inhibition by MDM2. Cell 91(3):325-334
83. Thalappilly S, Feng X, Pastyryeva S, Suzuki K, Muruve D, Larocque D, Richard S, Truss M, von Deimling A, Riabowol K, Tallen G (2011) The p53 tumor suppressor is stabilized by inhibitor of growth 1 (ING1) by blocking polyubiquitination. PLoS ONE 6(6):e21065. doi: 10.1371/journal.pone.0021065
84. 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(37):5173-5179. doi: 10.1038/sj.onc.1209526
85. Tallen UG, Truss M, Kunitz F, Wellmann S, Unryn B, Sinn B, Lass U, Krabbe S, Holtkamp N, Hagemeier C, Wurm R, Henze G, Riabowol KT, von Deimling A (2008) Down-regulation of the inhibitor of growth 1 (ING1) tumor suppressor sensitizes p53-deficient glioblastoma cells to cisplatin-induced cell death. J Neurooncol 86(1):23-30. doi: 10.1007/s11060-007-9436-x
86. Feng X, Bonni S, Riabowol K (2006) HSP70 induction by ING proteins sensitizes cells to tumor necrosis factor alpha receptor-mediated apoptosis. Mol Cell Biol 26(24):9244-9255. doi: 10.1128/MCB.01538-06
87. Shi Y, Tu Z, Tang D, Zhang H, Liu M, Wang K, Calderwood SK, Xiao X (2006) The inhibition of LPS-induced production of inflammatory cytokines by HSP70 involves inactivation of the NF-kappaB pathway but not the MAPK pathways. Shock 26(3):277-284. doi: 10.1097/01.shk.0000223134.17877.ad
88. Ran R, Lu A, Zhang L, Tang Y, Zhu H, Xu H, Feng Y, Han C, Zhou G, Rigby AC, Sharp FR (2004) Hsp70 promotes TNF-mediated apoptosis by binding IKK gamma and impairing NF-kappa B survival signaling. Genes Dev 18(12):1466-1481. doi: 10.1101/gad.1188204
89. Ma L, Chang N, Guo S, Li Q, Zhang Z, Wang W, Tong T (2008) CSIG inhibits PTEN translation in replicative senescence. Mol Cell Biol 28(20):6290-6301. doi: 10.1128/MCB.00142-08
90. Li N, Zhao G, Chen T, Xue L, Ma L, Niu J, Tong T (2012) Nucleolar protein CSIG is required for p33ING1 function in UV-induced apoptosis. Cell Death Dis 3:e283. doi: 10.1038/cddis.2012.22
91. 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(13):4974-4977
92. Niehrs C, Schafer A (2012) Active DNA demethylation by Gadd45 and DNA repair. Trends Cell Biol 22(4):220-227. doi: 10.1016/j.tcb.2012.01.002
93. 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(1):73-80
94. 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(8):1628-1638. doi: 10.1016/j.yexcr.2007. 02.010
95. 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(9):3632-3642. doi: 10.1093/nar/gkq1337
96. Watanabe K, Tateishi S, Kawasuji M, Tsurimoto T, Inoue H, Yamaizumi M (2004) Rad18 guides poleta to replication stalling sites through physical interaction and PCNA monoubiquitination. EMBO J 23(19):3886-3896. doi: 10.1038/sj.emboj.7600383
97. Hoege C, Pfander B, Moldovan GL, Pyrowolakis G, Jentsch S (2002) RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419(6903):135-141. doi: 10.1038/nature00991
98. Yu P, Huang B, Shen M, Lau C, Chan E, Michel J, Xiong Y, Payan DG, Luo Y (2001) p15(PAF), a novel PCNA associated factor with increased expression in tumor tissues. Oncogene 20(4):484-489. doi: 10.1038/sj.onc.1204113
99. Krishna TS, Kong XP, Gary S, Burgers PM, Kuriyan J (1994) Crystal structure of the eukaryotic DNA polymerase processivity factor PCNA. Cell 79(7):1233-1243
100. Gulbis JM, Kelman Z, Hurwitz J, O'Donnell M, Kuriyan J (1996) Structure of the C-terminal region of p21(WAF1/CIP1) complexed with human PCNA. Cell 87(2):297-306
101. Simpson F, Lammerts van Bueren K, Butterfield N, Bennetts JS, Bowles J, Adolphe C, Simms LA, Young J, Walsh MD, Leggett B, Fowles LF, Wicking C (2006) The PCNA-associated factor KIAA0101/p15(PAF) binds the potential tumor suppressor product p33ING1b. Exp Cell Res 312(1):73-85. doi: 10.1016/j.yexcr.2005.09.020
102. Pena PV, Musselman CA, Kuo AJ, Gozani O, Kutateladze TG (2009) NMR assignments and histone specificity of the ING2 PHD finger. Magn Reson Chem 47(4):352-358. doi: 10.1002/mrc.2390
103. Smith KT, Martin-Brown SA, Florens L, Washburn MP, Workman JL (2010) Deacetylase inhibitors dissociate the histone-targeting ING2 subunit from the Sin3 complex. Chem Biol 17(1):65-74. doi: 10.1016/j.chembiol.2009.12.010
104. 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(1):51-64. doi: 10.1016/j.molcel.2005.12.007
105. Ryan RJ, Bernstein BE (2012) Molecular biology. Genetic events that shape the cancer epigenome. Science 336(6088):1513-1514. doi: 10.1126/science.1223730
106. Ythier D, Larrieu D, Binet R, Binda O, Brambilla C, Gazzeri S, Pedeux R (2010) Sumoylation of ING2 regulates the transcription mediated by Sin3A. Oncogene 29(44):5946-5956. doi: 10.1038/onc.2010.325
107. Larrieu D, Ythier D, Brambilla C, Pedeux R (2010) ING2 controls the G1 to S-phase transition by regulating p21 expression. Cell Cycle 9(19):3984-3990. doi: 13208
108. Tian M, Neil JR, Schiemann WP (2011) Transforming growth factor-beta and the hallmarks of cancer. Cell Signal 23(6):951-962. doi: 10.1016/j.cellsig.2010. 10.015
109. Sarker KP, Kataoka H, Chan A, Netherton SJ, Pot I, Huynh MA, Feng X, Bonni A, Riabowol K, Bonni S (2008) ING2 as a novel mediator of transforming growth factor-beta-dependent responses in epithelial cells. J Biol Chem 283(19):13269-13279. doi: 10.1074/jbc.M708834200
110. 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(15):6639-6648. doi: 10.1128/MCB.25.15.6639-6648.2005
111. Kaadige MR, Ayer DE (2006) The polybasic region that follows the plant homeodomain zinc finger 1 of Pf1 is necessary and sufficient for specific phosphoinositide binding. J Biol Chem 281(39):28831-28836. doi: 10.1074/jbc.M605624200
112. Jones DR, Bultsma Y, Keune WJ, Halstead JR, Elouarrat D, Mohammed S, Heck AJ, D'Santos CS, Divecha N (2006) Nuclear PtdIns5P as a transducer of stress signaling: an in vivo role for PIP4Kbeta. Mol Cell 23(5):685-695. doi: 10.1016/j.molcel.2006.07.014
113. Gozani O, Field SJ, Ferguson CG, Ewalt M, Mahlke C, Cantley LC, Prestwich GD, Yuan J (2005) Modification of protein sub-nuclear localization by synthetic phosphoinositides: evidence for nuclear phosphoinositide signaling mechanisms. Adv Enzyme Regul 45:171-185. doi: 10.1016/j.advenzreg.2005.02.010
114. Huang W, Zhang H, Davrazou F, Kutateladze TG, Shi X, Gozani O, Prestwich GD (2007) Stabilized phosphatidylinositol-5-phosphate analogues as ligands for the nuclear protein ING2: chemistry, biology, and molecular modeling. J Am Chem Soc 129(20):6498-6506. doi: 10.1021/ja070195b
115. Costanzo A, Merlo P, Pediconi N, Fulco M, Sartorelli V, Cole PA, Fontemaggi G, Fanciulli M, Schiltz L, Blandino G, Balsano C, Levrero M (2002) DNA damage-dependent acetylation of p73 dictates the selective activation of apoptotic target genes. Mol Cell 9(1):175-186
116. Zeng X, Lee H, Zhang Q, Lu H (2001) p300 does not require its acetylase activity to stimulate p73 function. J Biol Chem 276(1):48-52. doi: 10.1074/jbc.C000722200
117. Chen J, Ghazawi FM, Li Q (2010) Interplay of bromodomain and histone acetylation in the regulation of p300-dependent genes. Epigenetics 5(6):509-515
118. Kalkhoven E (2004) CBP and p300: HATs for different occasions. Biochem Pharmacol 68(6):1145-1155. doi: 10.1016/j.bcp.2004.03.045
119. Larrieu D, Ythier D, Binet R, Brambilla C, Brambilla E, Sengupta S, Pedeux R (2009) ING2 controls the progression of DNA replication forks to maintain genome stability. EMBO Rep 10(10):1168-1174. doi: 10.1038/embor.2009. 180
120. Hasan S, Hassa PO, Imhof R, Hottiger MO (2001) Transcription coactivator p300 binds PCNA and may have a role in DNA repair synthesis. Nature 410(6826):387-391. doi: 10.1038/35066610
121. Larrieu D, Pedeux R (2009) SharING out the roles in replicatING DNA. Cell Cycle 8(22):3623-3624. doi: 9947
122. Wang J, Chin MY, Li G (2006) The novel tumor suppressor p33ING2 enhances nucleotide excision repair via inducement of histone H4 acetylation and chromatin relaxation. Cancer Res 66(4):1906-1911. doi: 10.1158/0008-5472.CAN-05- 3444
123. Wang Y, Wang J, Li G (2006) Leucine zipper-like domain is required for tumor suppressor ING2-mediated nucleotide excision repair and apoptosis. FEBS Lett 580(16):3787-3793. doi: 10.1016/j.febslet.2006.05.065
124. Kim MK, Shin JM, Eun HC, Chung JH (2009) The role of p300 histone acetyltransferase in UV-induced histone modifications and MMP-1 gene transcription. PLoS ONE 4(3):e4864. doi: 10.1371/journal.pone.0004864
125. Loewith R, Smith JS, Meijer M, Williams TJ, Bachman N, Boeke JD, Young D (2001) Pho23 is associated with the Rpd3 histone deacetylase and is required for its normal function in regulation of gene expression and silencing in Saccharomyces cerevisiae. J Biol Chem 276(26):24068-24074. doi: 10.1074/jbc.M102176200
126. Garkavtsev I, Riabowol K (1997) Extension of the replicative life span of human diploid fibroblasts by inhibition of the p33ING1 candidate tumor suppressor. Mol Cell Biol 17(4):2014-2019
127. Sun G, Jin S, Baskaran R (2009) MMR/c-Abl-dependent activation of ING2/p73alpha signaling regulates the cell death response to N-methyl-N'-nitro-N-nitrosoguanidine. Exp Cell Res 315(18):3163-3175. doi: 10.1016/j.yexcr.2009.09.010
128. De Biasio A, Campos-Olivas R, Sanchez R, Lopez-Alonso JP, Pantoja-Uceda D, Merino N, Villate M, Martin-Garcia JM, Castillo F, Luque I, Blanco FJ (2012) Proliferating cell nuclear antigen (PCNA) interactions in solution studied by NMR. PLoS ONE 7(11):e48390. doi: 10.1371/journal.pone.0048390
129. Stratton MR, Campbell PJ, Futreal PA (2009) The cancer genome. Nature 458(7239):719-724. doi: 10.1038/nature07943
130. Thakur S, Feng X, Qiao Shi Z, Ganapathy A, Kumar Mishra M, Atadja P, Morris D, Riabowol K (2012) ING1 and 5-azacytidine act synergistically to block breast cancer cell growth. PLoS ONE 7(8):e43671. doi: 10.1371/journal.pone. 0043671