47
Views
40
CrossRef citations to date
0
Altmetric
Article

Tumor Necrosis Factor Alpha-Induced Hypoxia-Inducible Factor 1α–β-Catenin Axis Regulates Major Histocompatibility Complex Class I Gene Activation through Chromatin Remodeling

, &
Pages 2718-2731 | Received 12 Sep 2012, Accepted 07 May 2013, Published online: 20 Mar 2023

REFERENCES

  • Semenza GL. 2010. Defining the role of hypoxia-inducible factor 1 in cancer biology and therapeutics. Oncogene 29:625–634.
  • Semenza GL. 2003. Targeting HIF-1 for cancer therapy. Nat. Rev. Cancer 3:721–732.
  • Wang GL, Semenza GL. 1995. Purification and characterization of hypoxia-inducible factor 1. J. Biol. Chem. 270:1230–1237.
  • Wang GL, Jiang BH, Rue EA, Semenza GL. 1995. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc. Natl. Acad. Sci. U. S. A. 92:5510–5514.
  • Jung Y, Isaacs JS, Lee S, Trepel J, Liu ZG, Neckers L. 2003. Hypoxia-inducible factor induction by tumour necrosis factor in normoxic cells requires receptor-interacting protein-dependent nuclear factor kappa B activation. Biochem. J. 370:1011–1017.
  • Kaur B, Khwaja FW, Severson EA, Matheny SL, Brat DJ, Van Meir EG. 2005. Hypoxia and the hypoxia-inducible-factor pathway in glioma growth and angiogenesis. Neuro Oncol. 7:134–153.
  • Zagzag D, Zhong H, Scalzitti JM, Laughner E, Simons JW, Semenza GL. 2000. Expression of hypoxia-inducible factor 1alpha in brain tumors: association with angiogenesis, invasion, and progression. Cancer 88:2606–2618.
  • Walker PR, Calzascia T, Dietrich PY. 2002. All in the head: obstacles for immune rejection of brain tumours. Immunology 107:28–38.
  • Dunn GP, Old LJ, Schreiber RD. 2004. The immunobiology of cancer immunosurveillance and immunoediting. Immunity 21:137–148.
  • Garrido F, Ruiz-Cabello F, Cabrera T, Perez-Villar JJ, Lopez-Botet M, Duggan-Keen M, Stern PL. 1997. Implications for immunosurveillance of altered HLA class I phenotypes in human tumours. Immunol. Today 18:89–95.
  • Friese MA, Platten M, Lutz SZ, Naumann U, Aulwurm S, Bischof F, Buhring HJ, Dichgans J, Rammensee HG, Steinle A, Weller M. 2003. MICA/NKG2D-mediated immunogene therapy of experimental gliomas. Cancer Res. 63:8996–9006.
  • Sekimoto E, Ozaki S, Ohshima T, Shibata H, Hashimoto T, Abe M, Kimura N, Hattori K, Kawai S, Kinoshita Y, Yamada-Okabe H, Tsuchiya M, Matsumoto T. 2007. A single-chain Fv diabody against human leukocyte antigen-A molecules specifically induces myeloma cell death in the bone marrow environment. Cancer Res. 67:1184–1192.
  • Barsoum IB, Hamilton TK, Li X, Cotechini T, Miles EA, Siemens DR, Graham CH. 2011. Hypoxia induces escape from innate immunity in cancer cells via increased expression of ADAM10: role of nitric oxide. Cancer Res. 71:7433–7441.
  • Siemens DR, Hu N, Sheikhi AK, Chung E, Frederiksen LJ, Pross H, Graham CH. 2008. Hypoxia increases tumor cell shedding of MHC class I chain-related molecule: role of nitric oxide. Cancer Res. 68:4746–4753.
  • Drew PD, Lonergan M, Goldstein ME, Lampson LA, Ozato K, McFarlin DE. 1993. Regulation of MHC class I and beta 2-microglobulin gene expression in human neuronal cells. Factor binding to conserved cis-acting regulatory sequences correlates with expression of the genes. J. Immunol. 150:3300–3310.
  • Hallermalm K, Seki K, Wei C, Castelli C, Rivoltini L, Kiessling R, Levitskaya J. 2001. Tumor necrosis factor-alpha induces coordinated changes in major histocompatibility class I presentation pathway, resulting in increased stability of class I complexes at the cell surface. Blood 98:1108–1115.
  • Tewari R, Choudhury SR, Ghosh S, Mehta VS, Sen E. 2012. Involvement of TNFalpha-induced TLR4-NF-kappaB and TLR4-HIF-1alpha feed-forward loops in the regulation of inflammatory responses in glioma. J. Mol. Med. (Berl.) 90:67–80.
  • Sharma V, Dixit D, Koul N, Mehta VS, Sen E. 2011. Ras regulates interleukin-1beta-induced HIF-1alpha transcriptional activity in glioblastoma. J. Mol. Med. (Berl.) 89:123–136.
  • Mansky P, Brown WM, Park JH, Choi JW, Yang SY. 1994. The second kappa B element, kappa B2, of the HLA-A class I regulatory complex is an essential part of the promoter. J. Immunol. 153:5082–5090.
  • Arce L, Yokoyama NN, Waterman ML. 2006. Diversity of LEF/TCF action in development and disease. Oncogene 25:7492–7504.
  • Lee SH, Kim MH, Han HJ. 2009. Arachidonic acid potentiates hypoxia-induced VEGF expression in mouse embryonic stem cells: involvement of Notch, Wnt, and HIF-1alpha. Am. J. Physiol. Cell Physiol. 297:C207–C216.
  • Kaidi A, Williams AC, Paraskeva C. 2007. Interaction between beta-catenin and HIF-1 promotes cellular adaptation to hypoxia. Nat. Cell Biol. 9:210–217.
  • Zheng H, Ying H, Wiedemeyer R, Yan H, Quayle SN, Ivanova EV, Paik JH, Zhang H, Xiao Y, Perry SR, Hu J, Vinjamoori A, Gan B, Sahin E, Chheda MG, Brennan C, Wang YA, Hahn WC, Chin L, DePinho RA. 2010. PLAGL2 regulates Wnt signaling to impede differentiation in neural stem cells and gliomas. Cancer Cell 17:497–509.
  • Kim MJ, Kim DH, Na HK, Surh YJ. 2010. TNF-alpha induces expression of urokinase-type plasminogen activator and beta-catenin activation through generation of ROS in human breast epithelial cells. Biochem. Pharmacol. 80:2092–2100.
  • Skov S, Pedersen MT, Andresen L, Straten PT, Woetmann A, Odum N. 2005. Cancer cells become susceptible to natural killer cell killing after exposure to histone deacetylase inhibitors due to glycogen synthase kinase-3-dependent expression of MHC class I-related chain A and B. Cancer Res. 65:11136–11145.
  • Abramovitch R, Tavor E, Jacob-Hirsch J, Zeira E, Amariglio N, Pappo O, Rechavi G, Galun E, Honigman A. 2004. A pivotal role of cyclic AMP-responsive element binding protein in tumor progression. Cancer Res. 64:1338–1346.
  • Mayr B, Montminy M. 2001. Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat. Rev. Mol. Cell Biol. 2:599–609.
  • Goren I, Tavor E, Goldblum A, Honigman A. 2001. Two cysteine residues in the DNA-binding domain of CREB control binding to CRE and CREB-mediated gene expression. J. Mol. Biol. 313:695–709.
  • Gobin SJ, Peijnenburg A, Keijsers V, van den Elsen PJ. 1997. Site alpha is crucial for two routes of IFN gamma-induced MHC class I transactivation: the ISRE-mediated route and a novel pathway involving CIITA. Immunity 6:601–611.
  • Kwok RP, Lundblad JR, Chrivia JC, Richards JP, Bachinger HP, Brennan RG, Roberts SG, Green MR, Goodman RH. 1994. Nuclear protein CBP is a coactivator for the transcription factor CREB. Nature 370:223–226.
  • Arany Z, Huang LE, Eckner R, Bhattacharya S, Jiang C, Goldberg MA, Bunn HF, Livingston DM. 1996. An essential role for p300/CBP in the cellular response to hypoxia. Proc. Natl. Acad. Sci. U. S. A. 93:12969–12973.
  • Takemaru KI, Moon RT. 2000. The transcriptional coactivator CBP interacts with beta-catenin to activate gene expression. J. Cell Biol. 149:249–254.
  • Agalioti T, Lomvardas S, Parekh B, Yie J, Maniatis T, Thanos D. 2000. Ordered recruitment of chromatin modifying and general transcription factors to the IFN-beta promoter. Cell 103:667–678.
  • Bannister AJ, Kouzarides T. 1996. The CBP co-activator is a histone acetyltransferase. Nature 384:641–643.
  • Kenneth NS, Mudie S, van Uden P, Rocha S. 2009. SWI/SNF regulates the cellular response to hypoxia. J. Biol. Chem. 284:4123–4131.
  • van den Elsen PJ, Gobin SJ, van Eggermond MC, Peijnenburg A. 1998. Regulation of MHC class I and II gene transcription: differences and similarities. Immunogenetics 48:208–221.
  • Gobin SJ, van Zutphen M, Westerheide SD, Boss JM, van den Elsen PJ. 2001. The MHC-specific enhanceosome and its role in MHC class I and beta(2)-microglobulin gene transactivation. J. Immunol. 167:5175–5184.
  • Ting JP, Baldwin AS. 1993. Regulation of MHC gene expression. Curr. Opin. Immunol. 5:8–16.
  • Noman MZ, Messai Y, Carre T, Akalay I, Meron M, Janji B, Hasmim M, Chouaib S. 2011. Microenvironmental hypoxia orchestrating the cell stroma cross talk, tumor progression and antitumor response. Crit. Rev. Immunol. 31:357–377.
  • Wolf D, Rodova M, Miska EA, Calvet JP, Kouzarides T. 2002. Acetylation of beta-catenin by CREB-binding protein (CBP). J. Biol. Chem. 277:25562–25567.
  • Dixit D, Sharma V, Ghosh S, Mehta VS, Sen E. 2012. Inhibition of Casein kinase-2 induces p53-dependent cell cycle arrest and sensitizes glioblastoma cells to tumor necrosis factor (TNFalpha)-induced apoptosis through SIRT1 inhibition. Cell Death Dis. 3:e271. doi:10.1038/cddis.2012.10.
  • Biswas S, Gupta MK, Chattopadhyay D, Mukhopadhyay CK. 2007. Insulin-induced activation of hypoxia-inducible factor-1 requires generation of reactive oxygen species by NADPH oxidase. Am. J. Physiol. Heart Circ. Physiol. 292:H758–H766.
  • Mylonis I, Chachami G, Paraskeva E, Simos G. 2008. Atypical CRM1-dependent nuclear export signal mediates regulation of hypoxia-inducible factor-1alpha by MAPK. J. Biol. Chem. 283:27620–27627.
  • Khavari PA, Peterson CL, Tamkun JW, Mendel DB, Crabtree GR. 1993. BRG1 contains a conserved domain of the SWI2/SNF2 family necessary for normal mitotic growth and transcription. Nature 366:170–174.
  • Deng J, Miller SA, Wang HY, Xia W, Wen Y, Zhou BP, Li Y, Lin SY, Hung MC. 2002. Beta-catenin interacts with and inhibits NF-kappa B in human colon and breast cancer. Cancer Cell 2:323–334.
  • Mayr BM, Canettieri G, Montminy MR. 2001. Distinct effects of cAMP and mitogenic signals on CREB-binding protein recruitment impart specificity to target gene activation via CREB. Proc. Natl. Acad. Sci. U. S. A. 98:10936–10941.
  • Rock KL, Gamble S, Rothstein L, Gramm C, Benacerraf B. 1991. Dissociation of beta 2-microglobulin leads to the accumulation of a substantial pool of inactive class I MHC heavy chains on the cell surface. Cell 65:611–620.
  • Staal FJ, van Noort M, Strous GJ, Clevers HC. 2002. Wnt signals are transmitted through N-terminally dephosphorylated beta-catenin. EMBO Rep. 3:63–68.
  • van de Wetering M, Cavallo R, Dooijes D, van Beest M, van Es J, Loureiro J, Ypma A, Hursh D, Jones T, Bejsovec A, Peifer M, Mortin M, Clevers H. 1997. Armadillo coactivates transcription driven by the product of the Drosophila segment polarity gene dTCF. Cell 88:789–799.
  • Park CH, Chang JY, Hahm ER, Park S, Kim HK, Yang CH. 2005. Quercetin, a potent inhibitor against beta-catenin/Tcf signaling in SW480 colon cancer cells. Biochem. Biophys. Res. Commun. 328:227–234.
  • Naito AT, Akazawa H, Takano H, Minamino T, Nagai T, Aburatani H, Komuro I. 2005. Phosphatidylinositol 3-kinase-Akt pathway plays a critical role in early cardiomyogenesis by regulating canonical Wnt signaling. Circ. Res. 97:144–151.
  • Saegusa M, Hashimura M, Kuwata T, Hamano M, Okayasu I. 2007. Crosstalk between NF-kappaB/p65 and beta-catenin/TCF4/p300 signalling pathways through alterations in GSK-3beta expression during trans-differentiation of endometrial carcinoma cells. J. Pathol. 213:35–45.
  • Tetsu O, McCormick F. 1999. Beta-catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature 398:422–426.
  • Wang H, Wen S, Bunnett NW, Leduc R, Hollenberg MD, MacNaughton WK. 2008. Proteinase-activated receptor-2 induces cyclooxygenase-2 expression through beta-catenin and cyclic AMP-response element-binding protein. J. Biol. Chem. 283:809–815.
  • Pradeep A, Sharma C, Sathyanarayana P, Albanese C, Fleming JV, Wang TC, Wolfe MM, Baker KM, Pestell RG, Rana B. 2004. Gastrin-mediated activation of cyclin D1 transcription involves beta-catenin and CREB pathways in gastric cancer cells. Oncogene 23:3689–3699.
  • Parker D, Ferreri K, Nakajima T, LaMorte VJ, Evans R, Koerber SC, Hoeger C, Montminy MR. 1996. Phosphorylation of CREB at Ser-133 induces complex formation with CREB-binding protein via a direct mechanism. Mol. Cell. Biol. 16:694–703.
  • Ogiwara H, Ui A, Otsuka A, Satoh H, Yokomi I, Nakajima S, Yasui A, Yokota J, Kohno T. 2011. Histone acetylation by CBP and p300 at double-strand break sites facilitates SWI/SNF chromatin remodeling and the recruitment of non-homologous end joining factors. Oncogene 30:2135–2146.
  • Brockmann D, Lehmkuhler O, Schmucker U, Esche H. 2001. The histone acetyltransferase activity of PCAF cooperates with the brahma/SWI2-related protein BRG-1 in the activation of the enhancer A of the MHC class I promoter. Gene 277:111–120.
  • Zhang Y, Cheng MB, Zhang YJ, Zhong X, Dai H, Yan L, Wu NH, Shen YF. 2010. A switch from hBrm to Brg1 at IFNgamma-activated sequences mediates the activation of human genes. Cell Res. 20:1345–1360.
  • Barker N, Hurlstone A, Musisi H, Miles A, Bienz M, Clevers H. 2001. The chromatin remodelling factor Brg-1 interacts with beta-catenin to promote target gene activation. EMBO J. 20:4935–4943.
  • Wang F, Zhang R, Beischlag TV, Muchardt C, Yaniv M, Hankinson O. 2004. Roles of Brahma and Brahma/SWI2-related gene 1 in hypoxic induction of the erythropoietin gene. J. Biol. Chem. 279:46733–46741.
  • Naidu SR, Love IM, Imbalzano AN, Grossman SR, Androphy EJ. 2009. The SWI/SNF chromatin remodeling subunit BRG1 is a critical regulator of p53 necessary for proliferation of malignant cells. Oncogene 28:2492–2501.
  • Ikegame A, Ozaki S, Tsuji D, Harada T, Fujii S, Nakamura S, Miki H, Nakano A, Kagawa K, Takeuchi K, Abe M, Watanabe K, Hiasa M, Kimura N, Kikuchi Y, Sakamoto A, Habu K, Endo M, Itoh K, Yamada-Okabe H, Matsumoto T. 2012. Small molecule antibody targeting HLA class I inhibits myeloma cancer stem cells by repressing pluripotency-associated transcription factors. Leukemia 26:2124–2134.
  • Cerwenka A, Baron JL, Lanier LL. 2001. Ectopic expression of retinoic acid early inducible-1 gene (RAE-1) permits natural killer cell-mediated rejection of a MHC class I-bearing tumor in vivo. Proc. Natl. Acad. Sci. U. S. A. 98:11521–11526.
  • Nozell S, Laver T, Moseley D, Nowoslawski L, De Vos M, Atkinson GP, Harrison K, Nabors LB, Benveniste EN. 2008. The ING4 tumor suppressor attenuates NF-kappaB activity at the promoters of target genes. Mol. Cell. Biol. 28:6632–6645.
  • Christova R, Jones T, Wu PJ, Bolzer A, Costa-Pereira AP, Watling D, Kerr IM, Sheer D. 2007. P-STAT1 mediates higher-order chromatin remodelling of the human MHC in response to IFNgamma. J. Cell Sci. 120:3262–3270.
  • Gobin SJ, Peijnenburg A, van Eggermond M, van Zutphen M, van den Berg R, van den Elsen PJ. 1998. The RFX complex is crucial for the constitutive and CIITA-mediated transactivation of MHC class I and beta2-microglobulin genes. Immunity 9:531–541.
  • Yang J, Yi Q. 2010. Killing tumor cells through their surface beta(2)-microglobulin or major histocompatibility complex class I molecules. Cancer 116:1638–1645.
  • Sen E. 2011. Targeting inflammation-induced transcription factor activation: an open frontier for glioma therapy. Drug Discov. Today 16:1044–1051.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.