Abstract
| Original language | English |
|---|---|
| Pages (from-to) | 3121-3131 |
| Number of pages | 11 |
| Journal | Molecular and Cellular Biology |
| Volume | 32 |
| Issue number | 15 |
| DOIs | |
| Publication status | Published - Aug 2012 |
| Externally published | Yes |
Fingerprint
Keywords
- acyltransferase
- cyclin D
- histone methyltransferase
- histone methyltransferase mmset
- histone methyltransferase nsd2
- immunoglobulin enhancer binding protein
- interleukin 6
- interleukin 8
- methyltransferase
- protein bcl 2
- protein p300
- survivin
- tumor necrosis factor alpha
- unclassified drug
- vasculotropin A
- acetylation
- article
- autocrine effect
- cancer cell
- castration resistant prostate cancer
- cell proliferation
- cell survival
- chromatin
- controlled study
- enzyme activity
- gene targeting
- human
- human cell
- positive feedback
- priority journal
- promoter region
- protein expression
- protein interaction
- tumor growth
- Acetylation
- Animals
- Autocrine Communication
- Cell Line, Tumor
- Cell Proliferation
- Cell Survival
- Chromatin
- Cyclin D
- Gene Expression Regulation, Neoplastic
- Histone-Lysine N-Methyltransferase
- Histones
- Humans
- Inhibitor of Apoptosis Proteins
- Interleukin-6
- Interleukin-8
- Male
- Mice
- Mice, Inbred BALB C
- Neoplasm Transplantation
- NF-kappa B
- p300-CBP Transcription Factors
- Promoter Regions, Genetic
- Prostatic Neoplasms
- Proto-Oncogene Proteins c-bcl-2
- Repressor Proteins
- RNA Interference
- RNA, Small Interfering
- Signal Transduction
- Transplantation, Heterologous
- Tumor Necrosis Factor-alpha
- Vascular Endothelial Growth Factor A
Cite this
Histone methyltransferase NSD2/MMSET mediates constitutive NF-kb signaling for cancer cell proliferation, survival, and tumor growth via a feed-forward loop. / Yang, P.; Guo, L.; Duan, Z.J.; Tepper, C.G.; Xue, L.; Chen, X.; Kung, H.-J.; Gao, A.C.; Zou, J.X.; Chena, H.-W.
In: Molecular and Cellular Biology, Vol. 32, No. 15, 08.2012, p. 3121-3131.Research output: Contribution to journal › Article
}
TY - JOUR
T1 - Histone methyltransferase NSD2/MMSET mediates constitutive NF-kb signaling for cancer cell proliferation, survival, and tumor growth via a feed-forward loop
AU - Yang, P.
AU - Guo, L.
AU - Duan, Z.J.
AU - Tepper, C.G.
AU - Xue, L.
AU - Chen, X.
AU - Kung, H.-J.
AU - Gao, A.C.
AU - Zou, J.X.
AU - Chena, H.-W.
N1 - 引用次數:51 Export Date: 5 March 2018 CODEN: MCEBD 通訊地址: Zou, J.X.; UC Davis Cancer Center/Basic Sciences, University of California at Davis, Sacramento, CA, United States; 電子郵件: jxzou@ucdavis.edu 化學物質/CAS: acyltransferase, 9012-30-0, 9054-54-0; cyclin D, 146587-97-5; interleukin 8, 114308-91-7; methyltransferase, 9033-25-4; protein bcl 2, 219306-68-0; survivin, 195263-98-0; vasculotropin A, 489395-96-2; BIRC5 protein, human; Chromatin; Cyclin D; Histone-Lysine N-Methyltransferase, 2.1.1.43; Histones; Inhibitor of Apoptosis Proteins; Interleukin-6; Interleukin-8; NF-kappa B; Proto-Oncogene Proteins c-bcl-2; RNA, Small Interfering; Repressor Proteins; Tumor Necrosis Factor-alpha; Vascular Endothelial Growth Factor A; WHSC1 protein, human, 2.1.1.43; p300-CBP Transcription Factors, 2.3.1.48; p300-CBP-associated factor, 2.3.1.48 參考文獻: Agoulnik, I.U., Role of SRC-1 in the promotion of prostate cancer cell growth and tumor progression (2005) Cancer Res, 65, pp. 7959-7967; Barish, G.D., Bcl-6 and NF-kappaB cistromes mediate opposing regulation of the innate immune response (2010) Genes Dev, 24, pp. 2760-2765; Caron, C., Functional characterization of ATAD2 as a new cancer/testis factor and a predictor of poor prognosis in breast and lung cancers (2010) Oncogene, 29, pp. 5171-5181; Carrozza, M.J., Histone H3 methylation by Set2 directs deacetylation of coding regions by Rpd3S to suppress spurious intragenic transcription (2005) Cell, 123, pp. 581-592; Chaturvedi, M.M., Sung, B., Yadav, V.R., Kannappan, R., Aggarwal, B.B., NF-kappaB addiction and its role in cancer: 'one size does not fit all. ' (2011) Oncogene, 30, pp. 1615-1630; Chen, C.D., Sawyers, C.L., NF- kappa B activates prostate-specific antigen expression and is upregulated in androgen-independent prostate cancer (2002) Mol. Cell. Biol., 22, pp. 2862-2870; Chen, L.F., NF- kappaB RelA phosphorylation regulates RelA acetylation (2005) Mol. Cell. Biol., 25, pp. 7966-7975; Ciro, M., ATAD2 is a novel cofactor for MYC, overexpressed and amplified in aggressive tumors (2009) Cancer Res, 69, pp. 8491-8498; Dan, H.C., Akt-dependent regulation of NF-{kappa}B is controlled by mTOR and Raptor in association with IKK (2008) Genes Dev, 22, pp. 1490-1500; De Santa, F., The histone H3 lysine-27 demethylase Jmjd3 links inflammation to inhibition of polycomb-mediated gene silencing (2007) Cell, 130, pp. 1083-1094; Heinz, S., Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities (2010) Mol. Cell, 38, pp. 576-589; Huang, B., Yang, X.D., Zhou, M.M., Ozato, K., Chen, L.F., Brd4 coactivates transcriptional activation of NF-kappaB via specific binding to acetylated RelA (2009) Mol. Cell. Biol., 29, pp. 1375-1387; Hudlebusch, H.R., The histone methyltransferase and putative oncoprotein MMSET is overexpressed in a large variety of human tumors (2011) Clin. Cancer Res., 17, pp. 2919-2933; Jin, R.J., The nuclear factor-kappaB pathway controls the progression of prostate cancer to androgen-independent growth (2008) Cancer Res, 68, pp. 6762-6769; Kalashnikova, E.V., ANCCA/ATAD2 overexpression identifies breast cancer patients with poor prognosis, acting to drive proliferation and survival of triple-negative cells through control of B-Myb and EZH2 (2010) Cancer Res, 70, pp. 9402-9412; Kim, J.Y., Multiple-myeloma-related WHSC1/MMSET isoform RE-IIBP is a histone methyltransferase with transcriptional repression activity (2008) Mol. Cell. Biol., 28, pp. 2023-2034; Kuo, A.J., NSD2 links dimethylation of histone H3 at lysine 36 to oncogenic programming (2011) Mol. Cell, 44, pp. 609-620; Lamont, K.R., Tindall, D.J., Minireview: alternative activation pathways for the androgen receptor in prostate cancer (2011) Mol. Endocrinol., 25, pp. 897-907; Lauring, J., The multiple myeloma associated MMSET gene contributes to cellular adhesion, clonogenic growth, and tumorigenicity (2008) Blood, 111, pp. 856-864; Lee, L.F., Interleukin-8 confers androgen-independent growth and migration of LNCaP: differential effects of tyrosine kinases Src and FAK (2004) Oncogene, 23, pp. 2197-2205; Lessard, L., Nuclear localization of nuclear factor-kappaB p65 in primary prostate tumors is highly predictive of pelvic lymph node metastases (2006) Clin. Cancer Res., 12, pp. 5741-5745; Li, Y., Role of the histone H3 lysine 4 methyltransferase, SET7/9, in the regulation of NF-kappaB-dependent inflammatory genes Relevance to diabetes and inflammation (2008) J. Biol. Chem., 283, pp. 26771-26781; Li, Y., The target of the NSD family of histone lysine methyltransferases depends on the nature of the substrate (2009) J. Biol. Chem., 284, pp. 34283-34295; Louie, M.C., Androgen-induced recruitment of RNA polymerase II to a nuclear receptor-p160 coactivator complex (2003) Proc. Natl. Acad. Sci. U. S. A., 100, pp. 2226-2230; Lu, T., Regulation of NF-kappaB by NSD1/FBXL11-dependent reversible lysine methylation of p65 (2010) Proc. Natl. Acad. Sci. U. S. A., 107, pp. 46-51; Malinowska, K., Interleukin-6 stimulation of growth of prostate cancer in vitro and in vivo through activation of the androgen receptor (2009) Endocr. Relat. Cancer, 16, pp. 155-169; Marango, J., The MMSET protein is a histone methyltransferase with characteristics of a transcriptional corepressor (2008) Blood, 111, pp. 3145-3154; Martinez-Garcia, E., The MMSET histone methyl transferase switches global histone methylation and alters gene expression in t(4;14) multiple myeloma cells (2011) Blood, 117, pp. 211-220; Min, J., An oncogene-tumor suppressor cascade drives metastatic prostate cancer by coordinately activating Ras and nuclear factorkappaB (2010) Nat. Med., 16, pp. 286-294; Nadiminty, N., Aberrant activation of the androgen receptor by NF-kappaB2/p52 in prostate cancer cells (2010) Cancer Res, 70, pp. 3309-3319; Ndlovu, M.N., Hyperactivated NF-{kappa}B and AP-1 transcription factors promote highly accessible chromatin and constitutivetranscription across the interleukin-6 gene promoter in metastatic breast cancer cells (2009) Mol. Cell. Biol., 29, pp. 5488-5504; Nimura, K., A histone H3 lysine 36 trimethyltransferase links Nkx2-5 to Wolf-Hirschhorn syndrome (2009) Nature, 460, pp. 287-291; Niu, Y., Differential androgen receptor signals in different cells explain why androgen-deprivation therapy of prostate cancer fails (2010) Oncogene, 29, pp. 3593-3604; Norris, J.D., The homeodomain protein HOXB13 regulates the cellular response to androgens (2009) Mol. Cell, 36, pp. 405-416; Nowak, D.E., RelA Ser276 phosphorylation is required for activation of a subset of NF-kappaB-dependent genes by recruiting cyclindependent kinase 9/cyclin T1 complexes (2008) Mol. Cell. Biol., 28, pp. 3623-3638; Pei, H., MMSET regulates histone H4K20 methylation and 53BP1 accumulation at DNA damage sites (2011) Nature, 470, pp. 124-128; Perkins, N.D., The diverse and complex roles of NF-kappaB subunits in cancer (2012) Nat. Rev. Cancer, 12, pp. 121-132; Pradhan, M., Baumgarten, S.C., Bembinster, L.A., Frasor, J., CBP mediates NF-kappaB-dependent histone acetylation and estrogen receptor recruitment to an estrogen response element in the BIRC3 promoter (2012) Mol. Cell. Biol., 32, pp. 569-575; Ramadoss, S., Li, J., Ding, X., Al Hezaimi, K., Wang, C.Y., Transducin beta-like protein 1 recruits nuclear factor kappaB to the target gene promoter for transcriptional activation (2011) Mol. Cell. Biol., 31, pp. 924-934; Revenko, A.S., Kalashnikova, E.V., Gemo, A.T., Zou, J.X., Chen, H.W., Chromatin loading of E2F-MLL complex by cancer-associated coregulator ANCCA via reading a specific histone mark (2010) Mol. Cell. Biol., 30, pp. 5260-5272; Rojas, A., IL-6 promotes prostate tumorigenesis and progression through autocrine cross-activation of IGF-IR (2011) Oncogene, 30, pp. 2345-2355; Ross, J.S., Expression of nuclear factor-kappa B and I kappa B alpha proteins in prostatic adenocarcinomas: correlation of nuclear factor-kappa B immunoreactivity with disease recurrence (2004) Clin. Cancer Res., 10, pp. 2466-2472; Schmitges, F.W., Histone methylation by PRC2 is inhibited by active chromatin marks (2011) Mol. Cell, 42, pp. 330-341; Seaton, A., Interleukin-8 signaling promotes androgenindependent proliferation of prostate cancer cells via induction of androgen receptor expression and activation (2008) Carcinogenesis, 29, pp. 1148-1156; Setlur, S.R., Integrative microarray analysis of pathways dysregulated in metastatic prostate cancer (2007) Cancer Res, 67, pp. 10296-10303; Sheppard, K.A., Transcriptional activation by NF-kappaB requires multiple coactivators (1999) Mol. Cell. Biol., 19, pp. 6367-6378; Smale, S.T., Hierarchies of NF-kappaB target-gene regulation (2011) Nat. Immunol., 12, pp. 689-694; van Essen, D., Zhu, Y., Saccani, S., A feed-forward circuit controlling inducible NF-kappaB target gene activation by promoter histone demethylation (2010) Mol. Cell, 39, pp. 750-760; Varambally, S., Integrative genomic and proteomic analysis of prostate cancer reveals signatures of metastatic progression (2005) Cancer Cell, 8, pp. 393-406; Wang, J., Activation of NF-{kappa}B by TMPRSS2/ERG fusion isoforms through Toll-like receptor-4 (2011) Cancer Res, 71, pp. 1325-1333; Wissmann, M., Cooperative demethylation by JMJD2C and LSD1 promotes androgen receptor-dependent gene expression (2007) Nat. Cell Biol., 9, pp. 347-353; Wolter, S., c-Jun controls histone modifications, NF-kappaB recruitment, and RNA polymerase II function to activate the ccl2 gene (2008) Mol. Cell. Biol., 28, pp. 4407-4423; Wright, C.W., Duckett, C.S., The aryl hydrocarbon nuclear translocator alters CD30-mediated NF-kappaB-dependent transcription (2009) Science, 323, pp. 251-255; Wu, R.C., Selective phosphorylations of the SRC-3/AIB1 coactivator integrate genomic responses to multiple cellular signaling pathways (2004) Mol. Cell, 15, pp. 937-949; Xu, Y., RelB enhances prostate cancer growth: implications for the role of the nuclear factor-kappaB alternative pathway in tumorigenicity (2009) Cancer Res, 69, pp. 3267-3271; Yang, X.D., Negative regulation of NF-kappaB action by Set9-mediated lysine methylation of the RelA subunit (2009) EMBO J, 28, pp. 1055-1066; Yang, X.D., Tajkhorshid, E., Chen, L.F., Functional interplay between acetylation and methylation of the RelA subunit of NF-kappaB (2010) Mol. Cell. Biol., 30, pp. 2170-2180; Yemelyanov, A., Effects of IKK inhibitor PS1145 on NF-kappaB function, proliferation, apoptosis and invasion activity in prostate carcinoma cells (2006) Oncogene, 25, pp. 387-398; Yu, J., The neuronal repellent SLIT2 is a target for repression by EZH2 in prostate cancer (2010) Oncogene, 29, pp. 5370-5380; Zhang, L., NF-kappaB regulates androgen receptor expression and prostate cancer growth (2009) Am. J. Pathol., 175, pp. 489-499; Zhong, H., May, M.J., Jimi, E., Ghosh, S., The phosphorylation status of nuclear NF-kappa B determines its association with CBP/p300 or HDAC-1 (2002) Mol. Cell, 9, pp. 625-636; Zhou, H.J., SRC-3 is required for prostate cancer cell proliferation and survival (2005) Cancer Res, 65, pp. 7976-7983; Zou, J.X., Androgen-induced coactivator ANCCA mediates specific androgen receptor signaling in prostate cancer (2009) Cancer Res, 69, pp. 3339-3346; Zou, J.X., Revenko, A.S., Li, L.B., Gemo, A.T., Chen, H.W., ANCCA, an estrogen-regulated AAA_ATPase coactivator for ERalpha, is required for coregulator occupancy and chromatin modification (2007) Proc. Natl. Acad. Sci. U. S. A., 104, pp. 18067-18072; Zou, J.X., ACTR/AIB1/SRC-3 and androgen receptor control prostate cancer cell proliferation and tumor growth through direct control of cell cycle genes (2006) Prostate, 66, pp. 1474-1486
PY - 2012/8
Y1 - 2012/8
N2 - Constitutive NF-kB activation by proinflammatory cytokines plays a major role in cancer progression. However, the underlying mechanism is still unclear. We report here that histone methyltransferase NSD2 (also known as MMSET or WHSC1), a target of bromodomain protein ANCCA/ATAD2, acts as a strong coactivator of NF-kB by directly interacting with NF-kB for activation of target genes, including those for interleukin-6 (IL-6), IL-8, vascular endothelial growth factor A (VEGFA), cyclin D, Bcl-2, and survivin, in castration-resistant prostate cancer (CRPC) cells. NSD2 is recruited to the target gene promoters upon induction and mediates NF-kB activation-associated elevation of histone H3K36me2 and H3K36me3 marks at the promoter, which involves its methylase activity. Interestingly, we found that NSD2 is also critical for cytokine-induced recruitment of NF-kB and acetyltransferase p300 and histone hyperacetylation. Importantly, NSD2 is overexpressed in prostate cancer tumors, and its overexpression correlates with NF-kB activation. Furthermore, NSD2 expression is strongly induced by tumor necrosis factor alpha (TNF-α) and IL-6 via NF-kB and plays a crucial role in tumor growth. These results identify NSD2 to be a key chromatin regulator of NF-kB and mediator of the cytokine autocrine loop for constitutive NF-kB activation and emphasize the important roles played by NSD2 in cancer cell proliferation and survival and tumor growth. © 2012, American Society for Microbiology.
AB - Constitutive NF-kB activation by proinflammatory cytokines plays a major role in cancer progression. However, the underlying mechanism is still unclear. We report here that histone methyltransferase NSD2 (also known as MMSET or WHSC1), a target of bromodomain protein ANCCA/ATAD2, acts as a strong coactivator of NF-kB by directly interacting with NF-kB for activation of target genes, including those for interleukin-6 (IL-6), IL-8, vascular endothelial growth factor A (VEGFA), cyclin D, Bcl-2, and survivin, in castration-resistant prostate cancer (CRPC) cells. NSD2 is recruited to the target gene promoters upon induction and mediates NF-kB activation-associated elevation of histone H3K36me2 and H3K36me3 marks at the promoter, which involves its methylase activity. Interestingly, we found that NSD2 is also critical for cytokine-induced recruitment of NF-kB and acetyltransferase p300 and histone hyperacetylation. Importantly, NSD2 is overexpressed in prostate cancer tumors, and its overexpression correlates with NF-kB activation. Furthermore, NSD2 expression is strongly induced by tumor necrosis factor alpha (TNF-α) and IL-6 via NF-kB and plays a crucial role in tumor growth. These results identify NSD2 to be a key chromatin regulator of NF-kB and mediator of the cytokine autocrine loop for constitutive NF-kB activation and emphasize the important roles played by NSD2 in cancer cell proliferation and survival and tumor growth. © 2012, American Society for Microbiology.
KW - acyltransferase
KW - cyclin D
KW - histone methyltransferase
KW - histone methyltransferase mmset
KW - histone methyltransferase nsd2
KW - immunoglobulin enhancer binding protein
KW - interleukin 6
KW - interleukin 8
KW - methyltransferase
KW - protein bcl 2
KW - protein p300
KW - survivin
KW - tumor necrosis factor alpha
KW - unclassified drug
KW - vasculotropin A
KW - acetylation
KW - article
KW - autocrine effect
KW - cancer cell
KW - castration resistant prostate cancer
KW - cell proliferation
KW - cell survival
KW - chromatin
KW - controlled study
KW - enzyme activity
KW - gene targeting
KW - human
KW - human cell
KW - positive feedback
KW - priority journal
KW - promoter region
KW - protein expression
KW - protein interaction
KW - tumor growth
KW - Acetylation
KW - Animals
KW - Autocrine Communication
KW - Cell Line, Tumor
KW - Cell Proliferation
KW - Cell Survival
KW - Chromatin
KW - Cyclin D
KW - Gene Expression Regulation, Neoplastic
KW - Histone-Lysine N-Methyltransferase
KW - Histones
KW - Humans
KW - Inhibitor of Apoptosis Proteins
KW - Interleukin-6
KW - Interleukin-8
KW - Male
KW - Mice
KW - Mice, Inbred BALB C
KW - Neoplasm Transplantation
KW - NF-kappa B
KW - p300-CBP Transcription Factors
KW - Promoter Regions, Genetic
KW - Prostatic Neoplasms
KW - Proto-Oncogene Proteins c-bcl-2
KW - Repressor Proteins
KW - RNA Interference
KW - RNA, Small Interfering
KW - Signal Transduction
KW - Transplantation, Heterologous
KW - Tumor Necrosis Factor-alpha
KW - Vascular Endothelial Growth Factor A
U2 - 10.1128/MCB.00204-12
DO - 10.1128/MCB.00204-12
M3 - Article
VL - 32
SP - 3121
EP - 3131
JO - Molecular and Cellular Biology
JF - Molecular and Cellular Biology
SN - 0270-7306
IS - 15
ER -