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Erschienen in: Journal of Cancer Research and Clinical Oncology 2/2017

20.08.2016 | Review – Cancer Research

INGs are potential drug targets for cancer

verfasst von: Runyun Zhang, Jianhua Jin, Juanjuan Shi, Yongzhong Hou

Erschienen in: Journal of Cancer Research and Clinical Oncology | Ausgabe 2/2017

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Abstract

Purpose

The inhibitor of growth (ING) family consists of ING1, ING2, ING3, ING4 and ING5, which function as the type II tumor suppressors. INGs regulate cell proliferation, senescence, apoptosis, differentiation, angiogenesis, DNA repair, metastasis, and invasion by multiple pathways. In addition, INGs increase cancer cell sensitivity for chemotherapy and radiotherapy, while clinical observations show that INGs are frequently lost in some types of cancers. The aim of the study was to summarize the recent progress regarding INGs regulating tumor progression.

Methods

The literatures of INGs regulating tumor progression were searched and assayed.

Results

The regulating signaling pathways of ING1, ING2, ING3 or ING4 on tumor progression were shown. The mechanisms of INGs on tumor suppression were also assayed.

Conclusions

This review better summarized the signaling mechanism of INGs on tumor suppression, which provides a candidate therapy strategy for cancers.
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Zurück zum Zitat 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 22:835–848PubMedPubMedCentralCrossRef 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 22:835–848PubMedPubMedCentralCrossRef
Zurück zum Zitat Larrieu D, Ythier D, Brambilla C, Pedeux R (2010) ING2 controls the G1 to S-phase transition by regulating p21 expression. Cell Cycle 9:3984–3990PubMedCrossRef Larrieu D, Ythier D, Brambilla C, Pedeux R (2010) ING2 controls the G1 to S-phase transition by regulating p21 expression. Cell Cycle 9:3984–3990PubMedCrossRef
Zurück zum Zitat Li J, Li G (2010) Cell cycle regulator ING4 is a suppressor of melanoma angiogenesis that is regulated by the metastasis suppressor BRMS1. Cancer Res 70:10445–10453PubMedCrossRef Li J, Li G (2010) Cell cycle regulator ING4 is a suppressor of melanoma angiogenesis that is regulated by the metastasis suppressor BRMS1. Cancer Res 70:10445–10453PubMedCrossRef
Zurück zum Zitat Li X, Nishida T, Noguchi A, Zheng Y, Takahashi H, Yang X, Masuda S, Takano Y (2010) Decreased nuclear expression and increased cytoplasmic expression of ING5 may be linked to tumorigenesis and progression in human head and neck squamous cell carcinoma. J Cancer Res Clin Oncol 136:1573–1583PubMedCrossRef Li X, Nishida T, Noguchi A, Zheng Y, Takahashi H, Yang X, Masuda S, Takano Y (2010) Decreased nuclear expression and increased cytoplasmic expression of ING5 may be linked to tumorigenesis and progression in human head and neck squamous cell carcinoma. J Cancer Res Clin Oncol 136:1573–1583PubMedCrossRef
Zurück zum Zitat Li XH, Noguchi A, Nishida T, Takahashi H, Zheng Y, Yang XH, Masuda S, Kikuchi K, Takano Y (2011a) Cytoplasmic expression of p33ING1b is correlated with tumorigenesis and progression of head and neck squamous cell carcinoma. Histol Histopathol 26:597–607PubMed Li XH, Noguchi A, Nishida T, Takahashi H, Zheng Y, Yang XH, Masuda S, Kikuchi K, Takano Y (2011a) Cytoplasmic expression of p33ING1b is correlated with tumorigenesis and progression of head and neck squamous cell carcinoma. Histol Histopathol 26:597–607PubMed
Zurück zum Zitat Li N, Li Q, Cao X, Zhao G, Xue L, Tong T (2011b) The tumor suppressor p33ING1b upregulates p16INK4a expression and induces cellular senescence. FEBS Lett 585:3106–3112PubMedCrossRef Li N, Li Q, Cao X, Zhao G, Xue L, Tong T (2011b) The tumor suppressor p33ING1b upregulates p16INK4a expression and induces cellular senescence. FEBS Lett 585:3106–3112PubMedCrossRef
Zurück zum Zitat 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:e283PubMedPubMedCentralCrossRef 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:e283PubMedPubMedCentralCrossRef
Zurück zum Zitat Li S, Fan T, Liu H, Chen J, Qin C, Ren X (2013) Tumor suppressor ING4 overexpression contributes to proliferation and invasion inhibition in gastric carcinoma by suppressing the NF-kappaB signaling pathway. Mol Biol Rep 40:5723–5732PubMedCrossRef Li S, Fan T, Liu H, Chen J, Qin C, Ren X (2013) Tumor suppressor ING4 overexpression contributes to proliferation and invasion inhibition in gastric carcinoma by suppressing the NF-kappaB signaling pathway. Mol Biol Rep 40:5723–5732PubMedCrossRef
Zurück zum Zitat Li Y, Deng H, Lv L, Zhang C, Qian L, Xiao J, Zhao W, Liu Q, Zhang D, Wang Y, Yan J, Zhang H et al (2015) The miR-193a-3p-regulated ING5 gene activates the DNA damage response pathway and inhibits multi-chemoresistance in bladder cancer. Oncotarget 6:10195–10206PubMedPubMedCentralCrossRef Li Y, Deng H, Lv L, Zhang C, Qian L, Xiao J, Zhao W, Liu Q, Zhang D, Wang Y, Yan J, Zhang H et al (2015) The miR-193a-3p-regulated ING5 gene activates the DNA damage response pathway and inhibits multi-chemoresistance in bladder cancer. Oncotarget 6:10195–10206PubMedPubMedCentralCrossRef
Zurück zum Zitat Ling C, Xie Y, Zhao D, Zhu Y, Xiang J, Yang J (2012) Enhanced radiosensitivity of non-small-cell lung cancer (NSCLC) by adenovirus-mediated ING4 gene therapy. Cancer Gene Ther 19:697–706PubMedCrossRef Ling C, Xie Y, Zhao D, Zhu Y, Xiang J, Yang J (2012) Enhanced radiosensitivity of non-small-cell lung cancer (NSCLC) by adenovirus-mediated ING4 gene therapy. Cancer Gene Ther 19:697–706PubMedCrossRef
Zurück zum Zitat Liu Y, Yu L, Wang Y, Zhang Y, Wang Y, Zhang G (2012) Expression of tumor suppressor gene ING4 in ovarian carcinoma is correlated with microvessel density. J Cancer Res Clin Oncol 138:647–655PubMedCrossRef Liu Y, Yu L, Wang Y, Zhang Y, Wang Y, Zhang G (2012) Expression of tumor suppressor gene ING4 in ovarian carcinoma is correlated with microvessel density. J Cancer Res Clin Oncol 138:647–655PubMedCrossRef
Zurück zum Zitat Liu N, Wang J, Wang J, Wang R, Liu Z, Yu Y, Lu H (2013) ING5 is a Tip60 cofactor that acetylates p53 in response to DNA damage. Cancer Res 73:3749–3760PubMedCrossRef Liu N, Wang J, Wang J, Wang R, Liu Z, Yu Y, Lu H (2013) ING5 is a Tip60 cofactor that acetylates p53 in response to DNA damage. Cancer Res 73:3749–3760PubMedCrossRef
Zurück zum Zitat Lou C, Jiang S, Guo X, Dong XS (2012) ING4 is negatively correlated with microvessel density in colon cancer. Tumour Biol J Int Soc Oncodev Biol Med 33:2357–2364CrossRef Lou C, Jiang S, Guo X, Dong XS (2012) ING4 is negatively correlated with microvessel density in colon cancer. Tumour Biol J Int Soc Oncodev Biol Med 33:2357–2364CrossRef
Zurück zum Zitat Lu M, Chen F, Wang Q, Wang K, Pan Q, Zhang X (2012) Downregulation of inhibitor of growth 3 is correlated with tumorigenesis and progression of hepatocellular carcinoma. Oncol Lett 4:47–52PubMedPubMedCentral Lu M, Chen F, Wang Q, Wang K, Pan Q, Zhang X (2012) Downregulation of inhibitor of growth 3 is correlated with tumorigenesis and progression of hepatocellular carcinoma. Oncol Lett 4:47–52PubMedPubMedCentral
Zurück zum Zitat Lu M, Pan C, Zhang L, Ding C, Chen F, Wang Q, Wang K, Zhang X (2013) ING4 inhibits the translation of proto-oncogene MYC by interacting with AUF1. FEBS Lett 587:1597–1604PubMedCrossRef Lu M, Pan C, Zhang L, Ding C, Chen F, Wang Q, Wang K, Zhang X (2013) ING4 inhibits the translation of proto-oncogene MYC by interacting with AUF1. FEBS Lett 587:1597–1604PubMedCrossRef
Zurück zum Zitat Luo J, Shah S, Riabowol K, Mains PE (2009) The Caenorhabditis elegans ing-3 gene regulates ionizing radiation-induced germ-cell apoptosis in a p53-associated pathway. Genetics 181:473–482PubMedPubMedCentralCrossRef Luo J, Shah S, Riabowol K, Mains PE (2009) The Caenorhabditis elegans ing-3 gene regulates ionizing radiation-induced germ-cell apoptosis in a p53-associated pathway. Genetics 181:473–482PubMedPubMedCentralCrossRef
Zurück zum Zitat Lv Y, Purbey BK, Huang Y, Li S, Radha G, Hao Z (2012) Adenovirus-mediated expression of p33(ING1b) induces apoptosis and inhibits proliferation in gastric adenocarcinoma cells in vitro. Gastric Cancer Off J Int Gastric Cancer Assoc Jpn Gastric Cancer Assoc 15:355–362 Lv Y, Purbey BK, Huang Y, Li S, Radha G, Hao Z (2012) Adenovirus-mediated expression of p33(ING1b) induces apoptosis and inhibits proliferation in gastric adenocarcinoma cells in vitro. Gastric Cancer Off J Int Gastric Cancer Assoc Jpn Gastric Cancer Assoc 15:355–362
Zurück zum Zitat Mao ZL, He SB, Sheng WH, Dong XQ, Yang JC (2013) Adenovirus-mediated ING4 expression reduces multidrug resistance of human gastric carcinoma cells in vitro and in vivo. Oncol Rep 30:2187–2194PubMed Mao ZL, He SB, Sheng WH, Dong XQ, Yang JC (2013) Adenovirus-mediated ING4 expression reduces multidrug resistance of human gastric carcinoma cells in vitro and in vivo. Oncol Rep 30:2187–2194PubMed
Zurück zum Zitat Moreno A, Soleto I, Garcia-Sanz P, Moreno-Bueno G, Palmero I (2014) ING4 regulates a secretory phenotype in primary fibroblasts with dual effects on cell proliferation and tumor growth. Oncogene 33:1945–1953PubMedCrossRef Moreno A, Soleto I, Garcia-Sanz P, Moreno-Bueno G, Palmero I (2014) ING4 regulates a secretory phenotype in primary fibroblasts with dual effects on cell proliferation and tumor growth. Oncogene 33:1945–1953PubMedCrossRef
Zurück zum Zitat Nabbi A, Almami A, Thakur S, Suzuki K, Boland D, Bismar TA, Riabowol K (2015) ING3 protein expression profiling in normal human tissues suggest its role in cellular growth and self-renewal. Eur J Cell Biol 94:214–222PubMedCrossRef Nabbi A, Almami A, Thakur S, Suzuki K, Boland D, Bismar TA, Riabowol K (2015) ING3 protein expression profiling in normal human tissues suggest its role in cellular growth and self-renewal. Eur J Cell Biol 94:214–222PubMedCrossRef
Zurück zum Zitat 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 98:9671–9676PubMedPubMedCentralCrossRef 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 98:9671–9676PubMedPubMedCentralCrossRef
Zurück zum Zitat 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 22:343–350PubMedCrossRef 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 22:343–350PubMedCrossRef
Zurück zum Zitat Nanding A, Tang L, Cai L, Chen H, Geng J, Liu X, Ning X, Li X, Zhang Q (2014) Low ING4 protein expression detected by paraffin-section immunohistochemistry is associated with poor prognosis in untreated patients with gastrointestinal stromal tumors. Gastric Cancer Off J Int Gastric Cancer Assoc Jpn Gastric Cancer Assoc 17:87–96 Nanding A, Tang L, Cai L, Chen H, Geng J, Liu X, Ning X, Li X, Zhang Q (2014) Low ING4 protein expression detected by paraffin-section immunohistochemistry is associated with poor prognosis in untreated patients with gastrointestinal stromal tumors. Gastric Cancer Off J Int Gastric Cancer Assoc Jpn Gastric Cancer Assoc 17:87–96
Zurück zum Zitat 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 584:3005–3012PubMedCrossRef 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 584:3005–3012PubMedCrossRef
Zurück zum Zitat 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 28:6632–6645PubMedPubMedCentralCrossRef 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 28:6632–6645PubMedPubMedCentralCrossRef
Zurück zum Zitat Ozer A, Bruick RK (2005) Regulation of HIF by prolyl hydroxylases: recruitment of the candidate tumor suppressor protein ING4. Cell Cycle 4:1153–1156PubMedCrossRef Ozer A, Bruick RK (2005) Regulation of HIF by prolyl hydroxylases: recruitment of the candidate tumor suppressor protein ING4. Cell Cycle 4:1153–1156PubMedCrossRef
Zurück zum Zitat Palacios A, Munoz IG, Pantoja-Uceda D, Marcaida MJ, Torres D, Martin-Garcia JM, Luque I, Montoya G, Blanco FJ (2008) Molecular basis of histone H3K4me3 recognition by ING4. J Biol Chem 283:15956–15964PubMedPubMedCentralCrossRef Palacios A, Munoz IG, Pantoja-Uceda D, Marcaida MJ, Torres D, Martin-Garcia JM, Luque I, Montoya G, Blanco FJ (2008) Molecular basis of histone H3K4me3 recognition by ING4. J Biol Chem 283:15956–15964PubMedPubMedCentralCrossRef
Zurück zum Zitat Pan YQ, Zhang X, Xu DP, Bao WG, Lin AF, Xu HH, Yan WH (2014) Decreased expression of ING2 gene and its clinicopathological significance in Chinese NSCLC patients. Neoplasma 61:468–475PubMedCrossRef Pan YQ, Zhang X, Xu DP, Bao WG, Lin AF, Xu HH, Yan WH (2014) Decreased expression of ING2 gene and its clinicopathological significance in Chinese NSCLC patients. Neoplasma 61:468–475PubMedCrossRef
Zurück zum Zitat Pedeux R, Sengupta S, Shen JC, Demidov ON, Saito S, Onogi H, Kumamoto K, Wincovitch S, Garfield SH, McMenamin M, Nagashima M, Grossman SR et al (2005) ING2 regulates the onset of replicative senescence by induction of p300-dependent p53 acetylation. Mol Cell Biol 25:6639–6648PubMedPubMedCentralCrossRef Pedeux R, Sengupta S, Shen JC, Demidov ON, Saito S, Onogi H, Kumamoto K, Wincovitch S, Garfield SH, McMenamin M, Nagashima M, Grossman SR et al (2005) ING2 regulates the onset of replicative senescence by induction of p300-dependent p53 acetylation. Mol Cell Biol 25:6639–6648PubMedPubMedCentralCrossRef
Zurück zum Zitat Pena PV, Hom RA, Hung T, Lin H, Kuo AJ, Wong RP, Subach OM, Champagne KS, Zhao R, Verkhusha VV, Li G, Gozani O et al (2008) Histone H3K4me3 binding is required for the DNA repair and apoptotic activities of ING1 tumor suppressor. J Mol Biol 380:303–312PubMedPubMedCentralCrossRef Pena PV, Hom RA, Hung T, Lin H, Kuo AJ, Wong RP, Subach OM, Champagne KS, Zhao R, Verkhusha VV, Li G, Gozani O et al (2008) Histone H3K4me3 binding is required for the DNA repair and apoptotic activities of ING1 tumor suppressor. J Mol Biol 380:303–312PubMedPubMedCentralCrossRef
Zurück zum Zitat Qi L, Zhang Y (2014) Truncation of inhibitor of growth family protein 5 effectively induces senescence, but not apoptosis in human tongue squamous cell carcinoma cell line. Tumour Biol J Int Soc Oncodev Biol Med 35:3139–3144CrossRef Qi L, Zhang Y (2014) Truncation of inhibitor of growth family protein 5 effectively induces senescence, but not apoptosis in human tongue squamous cell carcinoma cell line. Tumour Biol J Int Soc Oncodev Biol Med 35:3139–3144CrossRef
Zurück zum Zitat Rajarajacholan UK, Thalappilly S, Riabowol K (2013) The ING1a tumor suppressor regulates endocytosis to induce cellular senescence via the Rb-E2F pathway. PLoS Biol 11:e1001502PubMedPubMedCentralCrossRef Rajarajacholan UK, Thalappilly S, Riabowol K (2013) The ING1a tumor suppressor regulates endocytosis to induce cellular senescence via the Rb-E2F pathway. PLoS Biol 11:e1001502PubMedPubMedCentralCrossRef
Zurück zum Zitat Rotte A, Li G, Bhandaru M (2014) Tumor suppressor Ing1b facilitates DNA repair and prevents oxidative stress induced cell death. Apoptosis Int J Program Cell Death 19:518–526CrossRef Rotte A, Li G, Bhandaru M (2014) Tumor suppressor Ing1b facilitates DNA repair and prevents oxidative stress induced cell death. Apoptosis Int J Program Cell Death 19:518–526CrossRef
Zurück zum Zitat Russell M, Berardi P, Gong W, Riabowol K (2006) Grow-ING, Age-ING and Die-ING: ING proteins link cancer, senescence and apoptosis. Exp Cell Res 312:951–961PubMedCrossRef Russell M, Berardi P, Gong W, Riabowol K (2006) Grow-ING, Age-ING and Die-ING: ING proteins link cancer, senescence and apoptosis. Exp Cell Res 312:951–961PubMedCrossRef
Zurück zum Zitat 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 374:490–495PubMedCrossRef 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 374:490–495PubMedCrossRef
Zurück zum Zitat Saha A, Bamidele A, Murakami M, Robertson ES (2011) EBNA3C attenuates the function of p53 through interaction with inhibitor of growth family proteins 4 and 5. J Virol 85:2079–2088PubMedCrossRef Saha A, Bamidele A, Murakami M, Robertson ES (2011) EBNA3C attenuates the function of p53 through interaction with inhibitor of growth family proteins 4 and 5. J Virol 85:2079–2088PubMedCrossRef
Zurück zum Zitat Saito M, Kumamoto K, Robles AI, Horikawa I, Furusato B, Okamura S, Goto A, Yamashita T, Nagashima M, Lee TL, Baxendale VJ, Rennert OM et al (2010) Targeted disruption of Ing2 results in defective spermatogenesis and development of soft-tissue sarcomas. PLoS One 5:e15541PubMedPubMedCentralCrossRef Saito M, Kumamoto K, Robles AI, Horikawa I, Furusato B, Okamura S, Goto A, Yamashita T, Nagashima M, Lee TL, Baxendale VJ, Rennert OM et al (2010) Targeted disruption of Ing2 results in defective spermatogenesis and development of soft-tissue sarcomas. PLoS One 5:e15541PubMedPubMedCentralCrossRef
Zurück zum Zitat 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 283:13269–13279PubMedPubMedCentralCrossRef 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 283:13269–13279PubMedPubMedCentralCrossRef
Zurück zum Zitat Schafer A, Karaulanov E, Stapf U, Doderlein G, Niehrs C (2013) Ing1 functions in DNA demethylation by directing Gadd45a to H3K4me3. Genes Dev 27:261–273PubMedPubMedCentralCrossRef Schafer A, Karaulanov E, Stapf U, Doderlein G, Niehrs C (2013) Ing1 functions in DNA demethylation by directing Gadd45a to H3K4me3. Genes Dev 27:261–273PubMedPubMedCentralCrossRef
Zurück zum Zitat Shah S, Smith H, Feng X, Rancourt DE, Riabowol K (2009) ING function in apoptosis in diverse model systems. Biochem Cell Biol 87:117–125PubMedCrossRef Shah S, Smith H, Feng X, Rancourt DE, Riabowol K (2009) ING function in apoptosis in diverse model systems. Biochem Cell Biol 87:117–125PubMedCrossRef
Zurück zum Zitat Shi X, Hong T, Walter KL, Ewalt M, Michishita E, Hung T, Carney D, Pena P, Lan F, Kaadige MR, Lacoste N, Cayrou C et al (2006) ING2 PHD domain links histone H3 lysine 4 methylation to active gene repression. Nature 442:96–99PubMedPubMedCentralCrossRef Shi X, Hong T, Walter KL, Ewalt M, Michishita E, Hung T, Carney D, Pena P, Lan F, Kaadige MR, Lacoste N, Cayrou C et al (2006) ING2 PHD domain links histone H3 lysine 4 methylation to active gene repression. Nature 442:96–99PubMedPubMedCentralCrossRef
Zurück zum Zitat 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 21:1208–1216PubMedCrossRef 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 21:1208–1216PubMedCrossRef
Zurück zum Zitat 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 63:2373–2378PubMed 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 63:2373–2378PubMed
Zurück zum Zitat 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 17:65–74PubMedPubMedCentralCrossRef 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 17:65–74PubMedPubMedCentralCrossRef
Zurück zum Zitat Suzuki S, Nozawa Y, Tsukamoto S, Kaneko T, Imai H, Minami N (2013) ING3 is essential for asymmetric cell division during mouse oocyte maturation. PLoS One 8:e74749PubMedPubMedCentralCrossRef Suzuki S, Nozawa Y, Tsukamoto S, Kaneko T, Imai H, Minami N (2013) ING3 is essential for asymmetric cell division during mouse oocyte maturation. PLoS One 8:e74749PubMedPubMedCentralCrossRef
Zurück zum Zitat Tallen G, Farhangi S, Tamannai M, Holtkamp N, Mangoldt D, Shah S, Suzuki K, Truss M, Henze G, Riabowol K, von Deimling A (2009) The inhibitor of growth 1 (ING1) proteins suppress angiogenesis and differentially regulate angiopoietin expression in glioblastoma cells. Oncol Res 18:95–105PubMedCrossRef Tallen G, Farhangi S, Tamannai M, Holtkamp N, Mangoldt D, Shah S, Suzuki K, Truss M, Henze G, Riabowol K, von Deimling A (2009) The inhibitor of growth 1 (ING1) proteins suppress angiogenesis and differentially regulate angiopoietin expression in glioblastoma cells. Oncol Res 18:95–105PubMedCrossRef
Zurück zum Zitat 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 18:469–480PubMedCrossRef 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 18:469–480PubMedCrossRef
Zurück zum Zitat 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:e43671PubMedPubMedCentralCrossRef 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:e43671PubMedPubMedCentralCrossRef
Zurück zum Zitat Thakur S, Singla AK, Chen J, Tran U, Yang Y, Salazar C, Magliocco A, Klimowicz A, Jirik F, Riabowol K (2014) Reduced ING1 levels in breast cancer promotes metastasis. Oncotarget 5:4244–4256PubMedPubMedCentralCrossRef Thakur S, Singla AK, Chen J, Tran U, Yang Y, Salazar C, Magliocco A, Klimowicz A, Jirik F, Riabowol K (2014) Reduced ING1 levels in breast cancer promotes metastasis. Oncotarget 5:4244–4256PubMedPubMedCentralCrossRef
Zurück zum Zitat 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:e21065PubMedPubMedCentralCrossRef 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:e21065PubMedPubMedCentralCrossRef
Zurück zum Zitat Wang Y, Wang J, Li G (2006a) Leucine zipper-like domain is required for tumor suppressor ING2-mediated nucleotide excision repair and apoptosis. FEBS Lett 580:3787–3793PubMedCrossRef Wang Y, Wang J, Li G (2006a) Leucine zipper-like domain is required for tumor suppressor ING2-mediated nucleotide excision repair and apoptosis. FEBS Lett 580:3787–3793PubMedCrossRef
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Metadaten
Titel
INGs are potential drug targets for cancer
verfasst von
Runyun Zhang
Jianhua Jin
Juanjuan Shi
Yongzhong Hou
Publikationsdatum
20.08.2016
Verlag
Springer Berlin Heidelberg
Erschienen in
Journal of Cancer Research and Clinical Oncology / Ausgabe 2/2017
Print ISSN: 0171-5216
Elektronische ISSN: 1432-1335
DOI
https://doi.org/10.1007/s00432-016-2219-z

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