Skip to main content
Top
Published in: Tumor Biology 4/2016

01-04-2016 | Review

Inhibitor of growth-4 is a potential target for cancer therapy

Authors: Shuping Yuan, Jianhua Jin, Juanjuan Shi, Yongzhong Hou

Published in: Tumor Biology | Issue 4/2016

Login to get access

Abstract

The inhibitor of growth-4 (ING-4) belongs to the inhibitor of growth (ING) family that is a type II tumor suppressor gene including five members (ING1-5). As a tumor suppressor, ING4 inhibits tumor growth, invasion, and metastasis by multiple signaling pathways. In addition to that, ING4 can facilitate cancer cell sensitivity to chemotherapy and radiotherapy. Although ING4 loss is observed for many types of cancers, increasing evidences show that ING4 can be used for gene therapy. In this review, the recent progress of ING4 regulating tumorigenesis is discussed.
Literature
1.
go back to reference Feng X, Hara Y, Riabowol K. Different HATS of the ING1 gene family. Trends Cell Biol. 2002;12:532–8.CrossRefPubMed Feng X, Hara Y, Riabowol K. Different HATS of the ING1 gene family. Trends Cell Biol. 2002;12:532–8.CrossRefPubMed
2.
go back to reference He GH, Helbing CC, Wagner MJ, Sensen CW, Riabowol K. Phylogenetic analysis of the ING family of PHD finger proteins. Mol Biol Evol. 2005;22:104–16.CrossRefPubMed He GH, Helbing CC, Wagner MJ, Sensen CW, Riabowol K. Phylogenetic analysis of the ING family of PHD finger proteins. Mol Biol Evol. 2005;22:104–16.CrossRefPubMed
3.
go back to reference Russell M, Berardi P, Gong W, Riabowol K. Grow-ING, Age-ING and Die-ING: ING proteins link cancer, senescence and apoptosis. Exp Cell Res. 2006;312:951–61.CrossRefPubMed Russell M, Berardi P, Gong W, Riabowol K. Grow-ING, Age-ING and Die-ING: ING proteins link cancer, senescence and apoptosis. Exp Cell Res. 2006;312:951–61.CrossRefPubMed
4.
go back to reference Hu RM, Han ZG, Song HD, Peng YD, Huang QH, Ren SX, et al. Gene expression profiling in the human hypothalamus-pituitary-adrenal axis and full-length cDNA cloning. Proc Natl Acad Sci U S A. 2000;97:9543–8.CrossRefPubMedPubMedCentral Hu RM, Han ZG, Song HD, Peng YD, Huang QH, Ren SX, et al. Gene expression profiling in the human hypothalamus-pituitary-adrenal axis and full-length cDNA cloning. Proc Natl Acad Sci U S A. 2000;97:9543–8.CrossRefPubMedPubMedCentral
5.
go back to reference Garkavtsev I, Kozin SV, Chernova O, Xu L, Winkler F, Brown E, et al. The candidate tumour suppressor protein ING4 regulates brain tumour growth and angiogenesis. Nature. 2004;428:328–32.CrossRefPubMed Garkavtsev I, Kozin SV, Chernova O, Xu L, Winkler F, Brown E, et al. The candidate tumour suppressor protein ING4 regulates brain tumour growth and angiogenesis. Nature. 2004;428:328–32.CrossRefPubMed
6.
go back to reference Gunduz M, Ouchida M, Fukushima K, Ito S, Jitsumori Y, Nakashima T, et al. Allelic loss and reduced expression of the ING3, a candidate tumor suppressor gene at 7q31, in human head and neck cancers. Oncogene. 2002;21:4462–70.CrossRefPubMed Gunduz M, Ouchida M, Fukushima K, Ito S, Jitsumori Y, Nakashima T, et al. Allelic loss and reduced expression of the ING3, a candidate tumor suppressor gene at 7q31, in human head and neck cancers. Oncogene. 2002;21:4462–70.CrossRefPubMed
7.
go back to reference Unoki M, Shen JC, Zheng ZM, Harris CC. Novel splice variants of ING4 and their possible roles in the regulation of cell growth and motility. J Biol Chem. 2006;281:34677–86.CrossRefPubMed Unoki M, Shen JC, Zheng ZM, Harris CC. Novel splice variants of ING4 and their possible roles in the regulation of cell growth and motility. J Biol Chem. 2006;281:34677–86.CrossRefPubMed
8.
go back to reference Shiseki M, Nagashima M, Pedeux RM, Kitahama-Shiseki M, Miura K, Okamura S, et al. p29ING4 and p28ING5 bind to p53 and p300, and enhance p53 activity. Cancer Res. 2003;63:2373–8.PubMed Shiseki M, Nagashima M, Pedeux RM, Kitahama-Shiseki M, Miura K, Okamura S, et al. p29ING4 and p28ING5 bind to p53 and p300, and enhance p53 activity. Cancer Res. 2003;63:2373–8.PubMed
9.
go back to reference Doyon Y, Cayrou C, Ullah M, Landry AJ, Cote V, Selleck W, et al. ING tumor suppressor proteins are critical regulators of chromatin acetylation required for genome expression and perpetuation. Mol Cell. 2006;21:51–64.CrossRefPubMed Doyon Y, Cayrou C, Ullah M, Landry AJ, Cote V, Selleck W, et al. ING tumor suppressor proteins are critical regulators of chromatin acetylation required for genome expression and perpetuation. Mol Cell. 2006;21:51–64.CrossRefPubMed
10.
go back to reference Kim S, Chin K, Gray JW, Bishop JM. A screen for genes that suppress loss of contact inhibition: identification of ING4 as a candidate tumor suppressor gene in human cancer. Proc Natl Acad Sci U S A. 2004;101:16251–6.CrossRefPubMedPubMedCentral Kim S, Chin K, Gray JW, Bishop JM. A screen for genes that suppress loss of contact inhibition: identification of ING4 as a candidate tumor suppressor gene in human cancer. Proc Natl Acad Sci U S A. 2004;101:16251–6.CrossRefPubMedPubMedCentral
11.
go back to reference Moreno A, Soleto I, Garcia-Sanz P, Moreno-Bueno G, Palmero I. ING4 regulates a secretory phenotype in primary fibroblasts with dual effects on cell proliferation and tumor growth. Oncogene. 2014;33:1945–53.CrossRefPubMed Moreno A, Soleto I, Garcia-Sanz P, Moreno-Bueno G, Palmero I. ING4 regulates a secretory phenotype in primary fibroblasts with dual effects on cell proliferation and tumor growth. Oncogene. 2014;33:1945–53.CrossRefPubMed
12.
go back to reference Mathema VB, Koh YS. Inhibitor of growth-4 mediates chromatin modification and has a suppressive effect on tumorigenesis and innate immunity. Tumour Biol. 2012;33:1–7.CrossRefPubMed Mathema VB, Koh YS. Inhibitor of growth-4 mediates chromatin modification and has a suppressive effect on tumorigenesis and innate immunity. Tumour Biol. 2012;33:1–7.CrossRefPubMed
13.
go back to reference Sun J, Shen Q, Lu H, Jiang Z, Xu W, Feng L, et al. Oncogenic Ras suppresses ING4-TDG-Fas axis to promote apoptosis resistance. Oncotarget. 2015;6:41997–2007.PubMedPubMedCentral Sun J, Shen Q, Lu H, Jiang Z, Xu W, Feng L, et al. Oncogenic Ras suppresses ING4-TDG-Fas axis to promote apoptosis resistance. Oncotarget. 2015;6:41997–2007.PubMedPubMedCentral
14.
go back to reference Yan R, He L, Li Z, Han X, Liang J, Si W, et al. SCF(JFK) is a bona fide E3 ligase for ING4 and a potent promoter of the angiogenesis and metastasis of breast cancer. Genes Dev. 2015;29:672–85.CrossRefPubMedPubMedCentral Yan R, He L, Li Z, Han X, Liang J, Si W, et al. SCF(JFK) is a bona fide E3 ligase for ING4 and a potent promoter of the angiogenesis and metastasis of breast cancer. Genes Dev. 2015;29:672–85.CrossRefPubMedPubMedCentral
15.
go back to reference Yao H, Wang K, Wang Y, Wang S, Li J, Lou J, et al. Enhanced blood–brain barrier penetration and glioma therapy mediated by a new peptide modified gene delivery system. Biomaterials. 2015;37:345–52.CrossRefPubMed Yao H, Wang K, Wang Y, Wang S, Li J, Lou J, et al. Enhanced blood–brain barrier penetration and glioma therapy mediated by a new peptide modified gene delivery system. Biomaterials. 2015;37:345–52.CrossRefPubMed
16.
go back to reference Xu M, Xie Y, Sheng W, Miao J, Yang J. Adenovirus-mediated ING4 gene transfer in osteosarcoma suppresses tumor growth via induction of apoptosis and inhibition of tumor angiogenesis. Technol Cancer Res Treat. 2015;14:369–78.CrossRefPubMed Xu M, Xie Y, Sheng W, Miao J, Yang J. Adenovirus-mediated ING4 gene transfer in osteosarcoma suppresses tumor growth via induction of apoptosis and inhibition of tumor angiogenesis. Technol Cancer Res Treat. 2015;14:369–78.CrossRefPubMed
17.
go back to reference Zhao Y, Li Z, Sheng W, Miao J, Yang J. Radiosensitivity by ING4-IL-24 bicistronic adenovirus-mediated gene cotransfer on human breast cancer cells. Cancer Gene Ther. 2013;20:38–45.CrossRefPubMed Zhao Y, Li Z, Sheng W, Miao J, Yang J. Radiosensitivity by ING4-IL-24 bicistronic adenovirus-mediated gene cotransfer on human breast cancer cells. Cancer Gene Ther. 2013;20:38–45.CrossRefPubMed
18.
go back to reference Gunduz M, Nagatsuka H, Demircan K, Gunduz E, Cengiz B, Ouchida M, et al. Frequent deletion and down-regulation of ING4, a candidate tumor suppressor gene at 12p13, in head and neck squamous cell carcinomas. Gene. 2005;356:109–17.CrossRefPubMed Gunduz M, Nagatsuka H, Demircan K, Gunduz E, Cengiz B, Ouchida M, et al. Frequent deletion and down-regulation of ING4, a candidate tumor suppressor gene at 12p13, in head and neck squamous cell carcinomas. Gene. 2005;356:109–17.CrossRefPubMed
19.
go back to reference Mao ZL, He SB, Sheng WH, Dong XQ, Yang JC. Adenovirus-mediated ING4 expression reduces multidrug resistance of human gastric carcinoma cells in vitro and in vivo. Oncol Rep. 2013;30:2187–94.PubMed Mao ZL, He SB, Sheng WH, Dong XQ, Yang JC. Adenovirus-mediated ING4 expression reduces multidrug resistance of human gastric carcinoma cells in vitro and in vivo. Oncol Rep. 2013;30:2187–94.PubMed
20.
go back to reference Ling C, Xie Y, Zhao D, Zhu Y, Xiang J, Yang J. Enhanced radiosensitivity of non-small-cell lung cancer (NSCLC) by adenovirus-mediated ING4 gene therapy. Cancer Gene Ther. 2012;19:697–706.CrossRefPubMed Ling C, Xie Y, Zhao D, Zhu Y, Xiang J, Yang J. Enhanced radiosensitivity of non-small-cell lung cancer (NSCLC) by adenovirus-mediated ING4 gene therapy. Cancer Gene Ther. 2012;19:697–706.CrossRefPubMed
21.
go back to reference Li J, Li G. Cell cycle regulator ING4 is a suppressor of melanoma angiogenesis that is regulated by the metastasis suppressor BRMS1. Cancer Res. 2010;70:10445–53.CrossRefPubMed Li J, Li G. Cell cycle regulator ING4 is a suppressor of melanoma angiogenesis that is regulated by the metastasis suppressor BRMS1. Cancer Res. 2010;70:10445–53.CrossRefPubMed
22.
go back to reference Xu Y, Jin J, Zhang W, Zhang Z, Gao J, Liu Q, et al. EGFR/MDM2 signaling promotes NFkappaB activation via PPARgamma degradation. Carcinogenesis. 2015. Xu Y, Jin J, Zhang W, Zhang Z, Gao J, Liu Q, et al. EGFR/MDM2 signaling promotes NFkappaB activation via PPARgamma degradation. Carcinogenesis. 2015.
23.
go back to reference Gao J, Liu Q, Xu Y, Gong X, Zhang R, Zhou C, et al. PPARalpha induces cell apoptosis by destructing Bcl2. Oncotarget. 2015. Gao J, Liu Q, Xu Y, Gong X, Zhang R, Zhou C, et al. PPARalpha induces cell apoptosis by destructing Bcl2. Oncotarget. 2015.
24.
go back to reference Hou Y, Gao J, Xu H, Xu Y, Zhang Z, Xu Q, et al. PPARgamma E3 ubiquitin ligase regulates MUC1-C oncoprotein stability. Oncogene. 2013. Hou Y, Gao J, Xu H, Xu Y, Zhang Z, Xu Q, et al. PPARgamma E3 ubiquitin ligase regulates MUC1-C oncoprotein stability. Oncogene. 2013.
25.
go back to reference Yan A, Yang C, Chen Z, Li C, Cai L. MiR-761 promotes progression and metastasis of non-small cell lung cancer by targeting ING4 and TIMP2. Cell Physiol Biochem. 2015;37:55–66.CrossRefPubMed Yan A, Yang C, Chen Z, Li C, Cai L. MiR-761 promotes progression and metastasis of non-small cell lung cancer by targeting ING4 and TIMP2. Cell Physiol Biochem. 2015;37:55–66.CrossRefPubMed
26.
go back to reference Cao L, Chen S, Zhang C, Chen C, Lu N, Jiang Y, et al. ING4 enhances paclitaxel’s effect on colorectal cancer growth in vitro and in vivo. Int J Clin Exp Pathol. 2015;8:2919–27.PubMedPubMedCentral Cao L, Chen S, Zhang C, Chen C, Lu N, Jiang Y, et al. ING4 enhances paclitaxel’s effect on colorectal cancer growth in vitro and in vivo. Int J Clin Exp Pathol. 2015;8:2919–27.PubMedPubMedCentral
27.
go back to reference Kim S, Welm AL, Bishop JM. A dominant mutant allele of the ING4 tumor suppressor found in human cancer cells exacerbates MYC-initiated mouse mammary tumorigenesis. Cancer Res. 2010;70:5155–62.CrossRefPubMedPubMedCentral Kim S, Welm AL, Bishop JM. A dominant mutant allele of the ING4 tumor suppressor found in human cancer cells exacerbates MYC-initiated mouse mammary tumorigenesis. Cancer Res. 2010;70:5155–62.CrossRefPubMedPubMedCentral
28.
go back to reference Byron SA, Min E, Thal TS, Hostetter G, Watanabe AT, Azorsa DO, et al. Negative regulation of NF-kappaB by the ING4 tumor suppressor in breast cancer. PLoS One. 2012;7, e46823.CrossRefPubMedPubMedCentral Byron SA, Min E, Thal TS, Hostetter G, Watanabe AT, Azorsa DO, et al. Negative regulation of NF-kappaB by the ING4 tumor suppressor in breast cancer. PLoS One. 2012;7, e46823.CrossRefPubMedPubMedCentral
29.
go back to reference Berger PL, Frank SB, Schulz VV, Nollet EA, Edick MJ, Holly B, et al. Transient induction of ING4 by Myc drives prostate epithelial cell differentiation and its disruption drives prostate tumorigenesis. Cancer Res. 2014;74:3357–68.CrossRefPubMedPubMedCentral Berger PL, Frank SB, Schulz VV, Nollet EA, Edick MJ, Holly B, et al. Transient induction of ING4 by Myc drives prostate epithelial cell differentiation and its disruption drives prostate tumorigenesis. Cancer Res. 2014;74:3357–68.CrossRefPubMedPubMedCentral
30.
go back to reference Nanding A, Tang L, Cai L, Chen H, Geng J, Liu X, et al. Low ING4 protein expression detected by paraffin-section immunohistochemistry is associated with poor prognosis in untreated patients with gastrointestinal stromal tumors. Gastric Cancer. 2014;17:87–96.CrossRefPubMed Nanding A, Tang L, Cai L, Chen H, Geng J, Liu X, et al. Low ING4 protein expression detected by paraffin-section immunohistochemistry is associated with poor prognosis in untreated patients with gastrointestinal stromal tumors. Gastric Cancer. 2014;17:87–96.CrossRefPubMed
31.
go back to reference Zhang H, Zhou X, Xu C, Yang J, Xiang J, Tao M, et al. Synergistic tumor suppression by adenovirus-mediated ING4/PTEN double gene therapy for gastric cancer. Cancer Gene Ther. 2015. Zhang H, Zhou X, Xu C, Yang J, Xiang J, Tao M, et al. Synergistic tumor suppression by adenovirus-mediated ING4/PTEN double gene therapy for gastric cancer. Cancer Gene Ther. 2015.
32.
go back to reference Lou C, Jiang S, Guo X, Dong XS. ING4 is negatively correlated with microvessel density in colon cancer. Tumour Biol. 2012;33:2357–64.CrossRefPubMed Lou C, Jiang S, Guo X, Dong XS. ING4 is negatively correlated with microvessel density in colon cancer. Tumour Biol. 2012;33:2357–64.CrossRefPubMed
33.
go back to reference Liu Y, Yu L, Wang Y, Zhang Y, Wang Y, Zhang G. Expression of tumor suppressor gene ING4 in ovarian carcinoma is correlated with microvessel density. J Cancer Res Clin Oncol. 2012;138:647–55.CrossRefPubMed Liu Y, Yu L, Wang Y, Zhang Y, Wang Y, Zhang G. Expression of tumor suppressor gene ING4 in ovarian carcinoma is correlated with microvessel density. J Cancer Res Clin Oncol. 2012;138:647–55.CrossRefPubMed
34.
go back to reference Wang QS, Li M, Zhang LY, Jin Y, Tong DD, Yu Y, et al. Down-regulation of ING4 is associated with initiation and progression of lung cancer. Histopathology. 2010;57:271–81.CrossRefPubMed Wang QS, Li M, Zhang LY, Jin Y, Tong DD, Yu Y, et al. Down-regulation of ING4 is associated with initiation and progression of lung cancer. Histopathology. 2010;57:271–81.CrossRefPubMed
35.
go back to reference Klironomos G, Bravou V, Papachristou DJ, Gatzounis G, Varakis J, Parassi E, et al. Loss of inhibitor of growth (ING-4) is implicated in the pathogenesis and progression of human astrocytomas. Brain Pathol. 2010;20:490–7.CrossRefPubMed Klironomos G, Bravou V, Papachristou DJ, Gatzounis G, Varakis J, Parassi E, et al. Loss of inhibitor of growth (ING-4) is implicated in the pathogenesis and progression of human astrocytomas. Brain Pathol. 2010;20:490–7.CrossRefPubMed
36.
go back to reference Fang F, Luo LB, Tao YM, Wu F, Yang LY. Decreased expression of inhibitor of growth 4 correlated with poor prognosis of hepatocellular carcinoma. Cancer Epidemiol Biomark Prev. 2009;18:409–16.CrossRef Fang F, Luo LB, Tao YM, Wu F, Yang LY. Decreased expression of inhibitor of growth 4 correlated with poor prognosis of hepatocellular carcinoma. Cancer Epidemiol Biomark Prev. 2009;18:409–16.CrossRef
37.
go back to reference Xie Y, Zhang H, Sheng W, Xiang J, Ye Z, Yang J. Adenovirus-mediated ING4 expression suppresses lung carcinoma cell growth via induction of cell cycle alteration and apoptosis and inhibition of tumor invasion and angiogenesis. Cancer Lett. 2008;271:105–16.CrossRefPubMed Xie Y, Zhang H, Sheng W, Xiang J, Ye Z, Yang J. Adenovirus-mediated ING4 expression suppresses lung carcinoma cell growth via induction of cell cycle alteration and apoptosis and inhibition of tumor invasion and angiogenesis. Cancer Lett. 2008;271:105–16.CrossRefPubMed
38.
go back to reference Xie YF, Sheng W, Xiang J, Zhang H, Ye Z, Yang J. Adenovirus-mediated ING4 expression suppresses pancreatic carcinoma cell growth via induction of cell-cycle alteration, apoptosis, and inhibition of tumor angiogenesis. Cancer Biother Radiopharm. 2009;24:261–9.CrossRefPubMed Xie YF, Sheng W, Xiang J, Zhang H, Ye Z, Yang J. Adenovirus-mediated ING4 expression suppresses pancreatic carcinoma cell growth via induction of cell-cycle alteration, apoptosis, and inhibition of tumor angiogenesis. Cancer Biother Radiopharm. 2009;24:261–9.CrossRefPubMed
39.
go back to reference Wang Y, Yang J, Sheng W, Xie Y, Liu J. Adenovirus-mediated ING4/PTEN double tumor suppressor gene co-transfer modified by RGD enhances antitumor activity in human nasopharyngeal carcinoma cells. Int J Oncol. 2015;46:1295–303.PubMed Wang Y, Yang J, Sheng W, Xie Y, Liu J. Adenovirus-mediated ING4/PTEN double tumor suppressor gene co-transfer modified by RGD enhances antitumor activity in human nasopharyngeal carcinoma cells. Int J Oncol. 2015;46:1295–303.PubMed
40.
go back to reference Wu J, Zhu Y, Xu C, Xu H, Zhou X, Yang J, et al. Adenovirus-mediated p53 and ING4 gene cotransfer elicits synergistic antitumor effects through enhancement of p53 acetylation in breast cancer. Oncol Rep. 2016;35:243–52.PubMed Wu J, Zhu Y, Xu C, Xu H, Zhou X, Yang J, et al. Adenovirus-mediated p53 and ING4 gene cotransfer elicits synergistic antitumor effects through enhancement of p53 acetylation in breast cancer. Oncol Rep. 2016;35:243–52.PubMed
41.
go back to reference Han Z, Zhou C, Sun B, Yan Q, Zhang J. Experimental studies on the inhibition of adenovirus-ING4-OSM therapy on nasopharyngeal carcinoma proliferation in vitro and in vivo. Cell Biochem Biophys. 2014;70:1573–8.CrossRefPubMed Han Z, Zhou C, Sun B, Yan Q, Zhang J. Experimental studies on the inhibition of adenovirus-ING4-OSM therapy on nasopharyngeal carcinoma proliferation in vitro and in vivo. Cell Biochem Biophys. 2014;70:1573–8.CrossRefPubMed
42.
go back to reference Conner J, Braidwood L. Expression of inhibitor of growth 4 by HSV1716 improves oncolytic potency and enhances efficacy. Cancer Gene Ther. 2012;19:499–507.CrossRefPubMed Conner J, Braidwood L. Expression of inhibitor of growth 4 by HSV1716 improves oncolytic potency and enhances efficacy. Cancer Gene Ther. 2012;19:499–507.CrossRefPubMed
45.
go back to reference Stancovski I, Baltimore D. NF-kappaB activation: the I kappaB kinase revealed? Cell. 1997;91:299–302.CrossRefPubMed Stancovski I, Baltimore D. NF-kappaB activation: the I kappaB kinase revealed? Cell. 1997;91:299–302.CrossRefPubMed
46.
go back to reference Ghosh S, Baltimore D. Activation in vitro of NF-kappa B by phosphorylation of its inhibitor I kappa B. Nature. 1990;344:678–82.CrossRefPubMed Ghosh S, Baltimore D. Activation in vitro of NF-kappa B by phosphorylation of its inhibitor I kappa B. Nature. 1990;344:678–82.CrossRefPubMed
47.
go back to reference Hou Y, Mortimer L, Chadee K. Entamoeba histolytica cysteine proteinase 5 binds integrin on colonic cells and stimulates NFkappaB-mediated pro-inflammatory responses. J Biol Chem. 2010;285:35497–504.CrossRefPubMedPubMedCentral Hou Y, Mortimer L, Chadee K. Entamoeba histolytica cysteine proteinase 5 binds integrin on colonic cells and stimulates NFkappaB-mediated pro-inflammatory responses. J Biol Chem. 2010;285:35497–504.CrossRefPubMedPubMedCentral
48.
go back to reference Xu H, You M, Shi H, Hou Y. Ubiquitin-mediated NFkappaB degradation pathway. Cell Mol Immunol. 2014. Xu H, You M, Shi H, Hou Y. Ubiquitin-mediated NFkappaB degradation pathway. Cell Mol Immunol. 2014.
49.
go back to reference Hou Y, Moreau F, Chadee K. PPARgamma is an E3 ligase that induces the degradation of NFkappaB/p65. Nat Commun. 2012;3:1300.CrossRefPubMed Hou Y, Moreau F, Chadee K. PPARgamma is an E3 ligase that induces the degradation of NFkappaB/p65. Nat Commun. 2012;3:1300.CrossRefPubMed
50.
go back to reference Hou Y, Zhang Z, Xu Q, Wang H, Xu Y, Chen K. Inhibitor of growth 4 induces NFkappaB/p65 ubiquitin-dependent degradation. Oncogene. 2014;33:1997–2003.CrossRefPubMed Hou Y, Zhang Z, Xu Q, Wang H, Xu Y, Chen K. Inhibitor of growth 4 induces NFkappaB/p65 ubiquitin-dependent degradation. Oncogene. 2014;33:1997–2003.CrossRefPubMed
51.
go back to reference Nozell S, Laver T, Moseley D, Nowoslawski L, De Vos M, Atkinson GP, et al. The ING4 tumor suppressor attenuates NF-kappaB activity at the promoters of target genes. Mol Cell Biol. 2008;28:6632–45.CrossRefPubMedPubMedCentral Nozell S, Laver T, Moseley D, Nowoslawski L, De Vos M, Atkinson GP, et al. The ING4 tumor suppressor attenuates NF-kappaB activity at the promoters of target genes. Mol Cell Biol. 2008;28:6632–45.CrossRefPubMedPubMedCentral
52.
go back to reference Tang Y, Cheng Y, Martinka M, Ong CJ, Li G. Prognostic significance of KAI1/CD82 in human melanoma and its role in cell migration and invasion through the regulation of ING4. Carcinogenesis. 2014;35:86–95.CrossRefPubMed Tang Y, Cheng Y, Martinka M, Ong CJ, Li G. Prognostic significance of KAI1/CD82 in human melanoma and its role in cell migration and invasion through the regulation of ING4. Carcinogenesis. 2014;35:86–95.CrossRefPubMed
53.
go back to reference Coles AH, Gannon H, Cerny A, Kurt-Jones E, Jones SN. Inhibitor of growth-4 promotes IkappaB promoter activation to suppress NF-kappaB signaling and innate immunity. Proc Natl Acad Sci U S A. 2010;107:11423–8.CrossRefPubMedPubMedCentral Coles AH, Gannon H, Cerny A, Kurt-Jones E, Jones SN. Inhibitor of growth-4 promotes IkappaB promoter activation to suppress NF-kappaB signaling and innate immunity. Proc Natl Acad Sci U S A. 2010;107:11423–8.CrossRefPubMedPubMedCentral
54.
go back to reference Li S, Fan T, Liu H, Chen J, Qin C, Ren X. Tumor suppressor ING4 overexpression contributes to proliferation and invasion inhibition in gastric carcinoma by suppressing the NF-kappaB signaling pathway. Mol Biol Rep. 2013;40:5723–32.CrossRefPubMed Li S, Fan T, Liu H, Chen J, Qin C, Ren X. Tumor suppressor ING4 overexpression contributes to proliferation and invasion inhibition in gastric carcinoma by suppressing the NF-kappaB signaling pathway. Mol Biol Rep. 2013;40:5723–32.CrossRefPubMed
55.
go back to reference Raho G, Miranda C, Tamborini E, Pierotti MA, Greco A. Detection of novel mRNA splice variants of human ING4 tumor suppressor gene. Oncogene. 2007;26:5247–57.CrossRefPubMed Raho G, Miranda C, Tamborini E, Pierotti MA, Greco A. Detection of novel mRNA splice variants of human ING4 tumor suppressor gene. Oncogene. 2007;26:5247–57.CrossRefPubMed
56.
go back to reference Loginov VI, Maliukova AV, Seregin Iu A, Khodyrev DS, Kazubskaia TP, Ermilova VD, et al. Methylation of the promoter region of the RASSF1A gene, a candidate tumor suppressor, in primary epithelial tumors. Mol Biol. 2004;38:654–67.CrossRef Loginov VI, Maliukova AV, Seregin Iu A, Khodyrev DS, Kazubskaia TP, Ermilova VD, et al. Methylation of the promoter region of the RASSF1A gene, a candidate tumor suppressor, in primary epithelial tumors. Mol Biol. 2004;38:654–67.CrossRef
57.
go back to reference Iizuka M, Stillman B. Histone acetyltransferase HBO1 interacts with the ORC1 subunit of the human initiator protein. J Biol Chem. 1999;274:23027–34.CrossRefPubMed Iizuka M, Stillman B. Histone acetyltransferase HBO1 interacts with the ORC1 subunit of the human initiator protein. J Biol Chem. 1999;274:23027–34.CrossRefPubMed
58.
59.
go back to reference Avvakumov N, Cote J. The MYST family of histone acetyltransferases and their intimate links to cancer. Oncogene. 2007;26:5395–407.CrossRefPubMed Avvakumov N, Cote J. The MYST family of histone acetyltransferases and their intimate links to cancer. Oncogene. 2007;26:5395–407.CrossRefPubMed
60.
go back to reference Saksouk N, Avvakumov N, Champagne KS, Hung T, Doyon Y, Cayrou C, et al. HBO1 HAT complexes target chromatin throughout gene coding regions via multiple PHD finger interactions with histone H3 tail. Mol Cell. 2009;33:257–65.CrossRefPubMedPubMedCentral Saksouk N, Avvakumov N, Champagne KS, Hung T, Doyon Y, Cayrou C, et al. HBO1 HAT complexes target chromatin throughout gene coding regions via multiple PHD finger interactions with histone H3 tail. Mol Cell. 2009;33:257–65.CrossRefPubMedPubMedCentral
61.
go back to reference Palacios A, Munoz IG, Pantoja-Uceda D, Marcaida MJ, Torres D, Martin-Garcia JM, et al. Molecular basis of histone H3K4me3 recognition by ING4. J Biol Chem. 2008;283:15956–64.CrossRefPubMedPubMedCentral Palacios A, Munoz IG, Pantoja-Uceda D, Marcaida MJ, Torres D, Martin-Garcia JM, et al. Molecular basis of histone H3K4me3 recognition by ING4. J Biol Chem. 2008;283:15956–64.CrossRefPubMedPubMedCentral
62.
go back to reference Shi X, Hong T, Walter KL, Ewalt M, Michishita E, Hung T, et al. ING2 PHD domain links histone H3 lysine 4 methylation to active gene repression. Nature. 2006;442:96–9.CrossRefPubMedPubMedCentral Shi X, Hong T, Walter KL, Ewalt M, Michishita E, Hung T, et al. ING2 PHD domain links histone H3 lysine 4 methylation to active gene repression. Nature. 2006;442:96–9.CrossRefPubMedPubMedCentral
63.
go back to reference Hung T, Binda O, Champagne KS, Kuo AJ, Johnson K, Chang HY, et al. ING4 mediates crosstalk between histone H3 K4 trimethylation and H3 acetylation to attenuate cellular transformation. Mol Cell. 2009;33:248–56.CrossRefPubMedPubMedCentral Hung T, Binda O, Champagne KS, Kuo AJ, Johnson K, Chang HY, et al. ING4 mediates crosstalk between histone H3 K4 trimethylation and H3 acetylation to attenuate cellular transformation. Mol Cell. 2009;33:248–56.CrossRefPubMedPubMedCentral
64.
go back to reference Foy RL, Song IY, Chitalia VC, Cohen HT, Saksouk N, Cayrou C, et al. Role of Jade-1 in the histone acetyltransferase (HAT) HBO1 complex. J Biol Chem. 2008;283:28817–26.CrossRefPubMedPubMedCentral Foy RL, Song IY, Chitalia VC, Cohen HT, Saksouk N, Cayrou C, et al. Role of Jade-1 in the histone acetyltransferase (HAT) HBO1 complex. J Biol Chem. 2008;283:28817–26.CrossRefPubMedPubMedCentral
65.
go back to reference Zhang X, Wang KS, Wang ZQ, Xu LS, Wang QW, Chen F, et al. Nuclear localization signal of ING4 plays a key role in its binding to p53. Biochem Biophys Res Commun. 2005;331:1032–8.CrossRefPubMed Zhang X, Wang KS, Wang ZQ, Xu LS, Wang QW, Chen F, et al. Nuclear localization signal of ING4 plays a key role in its binding to p53. Biochem Biophys Res Commun. 2005;331:1032–8.CrossRefPubMed
66.
go back to reference Guo Y, Meng X, Wang Q, Wang Y, Shang H. The ING4 binding with p53 and induced p53 acetylation were attenuated by human papillomavirus 16 E6. PLoS One. 2013;8, e71453.CrossRefPubMedPubMedCentral Guo Y, Meng X, Wang Q, Wang Y, Shang H. The ING4 binding with p53 and induced p53 acetylation were attenuated by human papillomavirus 16 E6. PLoS One. 2013;8, e71453.CrossRefPubMedPubMedCentral
67.
go back to reference Guo Q, Fast W. Citrullination of inhibitor of growth 4 (ING4) by peptidylarginine deminase 4 (PAD4) disrupts the interaction between ING4 and p53. J Biol Chem. 2011;286:17069–78.CrossRefPubMedPubMedCentral Guo Q, Fast W. Citrullination of inhibitor of growth 4 (ING4) by peptidylarginine deminase 4 (PAD4) disrupts the interaction between ING4 and p53. J Biol Chem. 2011;286:17069–78.CrossRefPubMedPubMedCentral
68.
go back to reference Liao B, Hu Y, Brewer G. Competitive binding of AUF1 and TIAR to MYC mRNA controls its translation. Nat Struct Mol Biol. 2007;14:511–8.CrossRefPubMed Liao B, Hu Y, Brewer G. Competitive binding of AUF1 and TIAR to MYC mRNA controls its translation. Nat Struct Mol Biol. 2007;14:511–8.CrossRefPubMed
69.
go back to reference Lu M, Pan C, Zhang L, Ding C, Chen F, Wang Q, et al. ING4 inhibits the translation of proto-oncogene MYC by interacting with AUF1. FEBS Lett. 2013;587:1597–604.CrossRefPubMed Lu M, Pan C, Zhang L, Ding C, Chen F, Wang Q, et al. ING4 inhibits the translation of proto-oncogene MYC by interacting with AUF1. FEBS Lett. 2013;587:1597–604.CrossRefPubMed
70.
go back to reference Ozer A, Bruick RK. Regulation of HIF by prolyl hydroxylases: recruitment of the candidate tumor suppressor protein ING4. Cell Cycle. 2005;4:1153–6.CrossRefPubMed Ozer A, Bruick RK. Regulation of HIF by prolyl hydroxylases: recruitment of the candidate tumor suppressor protein ING4. Cell Cycle. 2005;4:1153–6.CrossRefPubMed
71.
go back to reference Colla S, Tagliaferri S, Morandi F, Lunghi P, Donofrio G, Martorana D, et al. The new tumor-suppressor gene inhibitor of growth family member 4 (ING4) regulates the production of proangiogenic molecules by myeloma cells and suppresses hypoxia-inducible factor-1 alpha (HIF-1alpha) activity: involvement in myeloma-induced angiogenesis. Blood. 2007;110:4464–75.CrossRefPubMed Colla S, Tagliaferri S, Morandi F, Lunghi P, Donofrio G, Martorana D, et al. The new tumor-suppressor gene inhibitor of growth family member 4 (ING4) regulates the production of proangiogenic molecules by myeloma cells and suppresses hypoxia-inducible factor-1 alpha (HIF-1alpha) activity: involvement in myeloma-induced angiogenesis. Blood. 2007;110:4464–75.CrossRefPubMed
72.
go back to reference Lu J, Tang Y, Cheng Y, Zhang G, Yip A, Martinka M, et al. ING4 regulates JWA in angiogenesis and their prognostic value in melanoma patients. Br J Cancer. 2013;109:2842–52.CrossRefPubMedPubMedCentral Lu J, Tang Y, Cheng Y, Zhang G, Yip A, Martinka M, et al. ING4 regulates JWA in angiogenesis and their prognostic value in melanoma patients. Br J Cancer. 2013;109:2842–52.CrossRefPubMedPubMedCentral
73.
74.
75.
go back to reference Zhang X, Zhu W, Zhang J, Huo S, Zhou L, Gu Z, et al. MicroRNA-650 targets ING4 to promote gastric cancer tumorigenicity. Biochem Biophys Res Commun. 2010;395:275–80.CrossRefPubMed Zhang X, Zhu W, Zhang J, Huo S, Zhou L, Gu Z, et al. MicroRNA-650 targets ING4 to promote gastric cancer tumorigenicity. Biochem Biophys Res Commun. 2010;395:275–80.CrossRefPubMed
76.
go back to reference Huang JY, Cui SY, Chen YT, Song HZ, Huang GC, Feng B, et al. MicroRNA-650 was a prognostic factor in human lung adenocarcinoma and confers the docetaxel chemoresistance of lung adenocarcinoma cells via regulating Bcl-2/Bax expression. PLoS One. 2013;8, e72615.CrossRefPubMedPubMedCentral Huang JY, Cui SY, Chen YT, Song HZ, Huang GC, Feng B, et al. MicroRNA-650 was a prognostic factor in human lung adenocarcinoma and confers the docetaxel chemoresistance of lung adenocarcinoma cells via regulating Bcl-2/Bax expression. PLoS One. 2013;8, e72615.CrossRefPubMedPubMedCentral
77.
go back to reference Mraz M, Dolezalova D, Plevova K, Stano Kozubik K, Mayerova V, Cerna K, et al. MicroRNA-650 expression is influenced by immunoglobulin gene rearrangement and affects the biology of chronic lymphocytic leukemia. Blood. 2012;119:2110–3.CrossRefPubMed Mraz M, Dolezalova D, Plevova K, Stano Kozubik K, Mayerova V, Cerna K, et al. MicroRNA-650 expression is influenced by immunoglobulin gene rearrangement and affects the biology of chronic lymphocytic leukemia. Blood. 2012;119:2110–3.CrossRefPubMed
78.
go back to reference Loesch K, Galaviz S, Hamoui Z, Clanton R, Akabani G, Deveau M, et al. Functional genomics screening utilizing mutant mouse embryonic stem cells identifies novel radiation-response genes. PLoS One. 2015;10, e0120534.CrossRefPubMedPubMedCentral Loesch K, Galaviz S, Hamoui Z, Clanton R, Akabani G, Deveau M, et al. Functional genomics screening utilizing mutant mouse embryonic stem cells identifies novel radiation-response genes. PLoS One. 2015;10, e0120534.CrossRefPubMedPubMedCentral
79.
go back to reference Zhao Y, Su C, Zhai H, Tian Y, Sheng W, Miao J, et al. Synergistic antitumor effect of adenovirus-mediated hING4 gene therapy and (125)I radiation therapy on pancreatic cancer. Cancer Lett. 2012;316:211–8.CrossRefPubMed Zhao Y, Su C, Zhai H, Tian Y, Sheng W, Miao J, et al. Synergistic antitumor effect of adenovirus-mediated hING4 gene therapy and (125)I radiation therapy on pancreatic cancer. Cancer Lett. 2012;316:211–8.CrossRefPubMed
80.
go back to reference Huang JH, Ling CH, Yang JC, Zhao DG, Xie YF, Sheng WH. The in vitro and in vivo effects of adenovirus-mediated inhibitor of growth 4 and interleukin-24 co-expression on the radiosensitivity of human lung adenocarcinoma. Zhonghua Jie He He Hu Xi Za Zhi. 2011;34:413–8.PubMed Huang JH, Ling CH, Yang JC, Zhao DG, Xie YF, Sheng WH. The in vitro and in vivo effects of adenovirus-mediated inhibitor of growth 4 and interleukin-24 co-expression on the radiosensitivity of human lung adenocarcinoma. Zhonghua Jie He He Hu Xi Za Zhi. 2011;34:413–8.PubMed
81.
go back to reference Wang R, Huang J, Feng B, De W, Chen L. Identification of ING4 (inhibitor of growth 4) as a modulator of docetaxel sensitivity in human lung adenocarcinoma. Mol Med. 2012;18:874–86.PubMedPubMedCentral Wang R, Huang J, Feng B, De W, Chen L. Identification of ING4 (inhibitor of growth 4) as a modulator of docetaxel sensitivity in human lung adenocarcinoma. Mol Med. 2012;18:874–86.PubMedPubMedCentral
Metadata
Title
Inhibitor of growth-4 is a potential target for cancer therapy
Authors
Shuping Yuan
Jianhua Jin
Juanjuan Shi
Yongzhong Hou
Publication date
01-04-2016
Publisher
Springer Netherlands
Published in
Tumor Biology / Issue 4/2016
Print ISSN: 1010-4283
Electronic ISSN: 1423-0380
DOI
https://doi.org/10.1007/s13277-016-4842-3

Other articles of this Issue 4/2016

Tumor Biology 4/2016 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine