Ukr.Biochem.J. 2016; Volume 88, Issue 5, Sep-Oct, pp. 18-37

doi: https://doi.org/10.15407/ubj88.05.018

The role of the TNF receptors and apoptosis inducing ligands in tumor growth

07.11.2016   Uncategorized   No comments

O. H. Minchenko1, D. O. Tsymbal1, D. O. Minchenko1,2, О. O. Ratushna1

1Palladin Institute of Biochemistry, National Academy of Sciences of Ukraine, Kyiv;
e-mail: ominchenko@yahoo.com;
2Bohomolets National Medical University, Kyiv, Ukraine

Tumor necrosis factor (TNF) superfamily receptors and TNF apoptosis inducing ligands play an important role in the realization of TNF function and control tumor growth. The TNF-related pathways are controlled by endoplasmic reticulum stress signaling, which has a crucial role in the control of cell proliferation and tumor growth. Furthermore, the inhibition of IRE1 (inositol requiring enzyme-1), which is a central mediator of endoplasmic reticulum stress sand mainly responsible for cell proliferation and apoptosis, leads to suppression of tumor growth through specific changes in the expression of genes encoding transcription factors, tumor suppressors, angiogenesis and apoptosis related proteins, including TNF superfamily receptors and TNF apoptosis inducing ligands. Therefore, changes in the expression level of TNF-related genes encoding TNF superfamily receptors and apoptosis inducing ligands possibly reflect metabolic reprogramming of cancer cells upon inhibition of IRE1-mediated endoplasmic reticulum stress signaling and correlate with suppression of glioma cell proliferation.

Keywords: , , , ,

References:

  1. Lebrec H, Ponce R, Preston BD, Iles J, Born TL, Hooper M. Tumor necrosis factor, tumor necrosis factor inhibition, and cancer risk. Curr Med Res Opin. 2015 Mar;31(3):557-74. Review. PubMed, CrossRef
  2. Jang MK, Kim HS, Chung YH. Clinical aspects of tumor necrosis factor-α signaling in hepatocellular carcinoma. Curr Pharm Des. 2014;20(17):2799-808. Review. PubMed, CrossRef
  3. Waters JP, Pober JS, Bradley JR. Tumour necrosis factor and cancer. J Pathol. 2013 Jul;230(3):241-8. Review. PubMed, CrossRef
  4. Isaac ST, Tan TC, Polly P. Endoplasmic Reticulum Stress, Calcium Dysregulation and Altered Protein Translation: Intersection of Processes That Contribute to Cancer Cachexia Induced Skeletal Muscle Wasting. Curr Drug Targets. 2016;17(10):1140-6. Review. PubMed, CrossRef
  5. Chu WM. Tumor necrosis factor. Cancer Lett. 2013 Jan 28;328(2):222-5.  PubMed, PubMedCentral, CrossRef
  6. Song Y, Buchwald P. TNF superfamily protein-protein interactions: feasibility of small- molecule modulation. Curr Drug Targets. 2015;16(4):393-408. PubMed, PubMedCentral, CrossRef
  7. Kitson J, Raven T, Jiang YP, Goeddel DV, Giles KM, Pun KT, Grinham CJ, Brown R, Farrow SN. A death-domain-containing receptor that mediates apoptosis. Nature. 1996 Nov 28;384(6607):372-5. PubMed, CrossRef
  8. Cullen SP, Martin SJ2. Fas and TRAIL ‘death receptors’ as initiators of inflammation: Implications for cancer. Semin Cell Dev Biol. 2015 Mar;39:26-34.  PubMed, CrossRef
  9. de Miguel D, Lemke J, Anel A, Walczak H, Martinez-Lostao L. Onto better TRAILs for cancer treatment. Cell Death Differ. 2016 May;23(5):733-47. Review. PubMed, PubMedCentral, CrossRef
  10. O’Leary L, van der Sloot AM, Reis CR, Deegan S, Ryan AE, Dhami SP, Murillo LS, Cool RH, Correa de Sampaio P, Thompson K, Murphy G, Quax WJ, Serrano L, Samali A, Szegezdi E. Decoy receptors block TRAIL sensitivity at a supracellular level: the role of stromal cells in controlling tumour TRAIL sensitivity. Oncogene. 2016 Mar 10;35(10):1261-70. PubMed, CrossRef
  11. Sarhan D, D’Arcy P, Lundqvist A. Regulation of TRAIL-receptor expression by the ubiquitin-proteasome system. Int J Mol Sci. 2014 Oct 14;15(10):18557-73. Review. PubMed, PubMedCentral, CrossRef
  12. Dai X, Zhang J, Arfuso F, Chinnathambi A, Zayed ME, Alharbi SA, Kumar AP, Ahn KS, Sethi G. Targeting TNF-related apoptosis-inducing ligand (TRAIL) receptor by natural products as a potential therapeutic approach for cancer therapy. Exp Biol Med (Maywood). 2015 Jun;240(6):760-73. Review. PubMed, CrossRef
  13. Fulda S. Tumor-necrosis-factor-related apoptosis-inducing ligand (TRAIL). Adv Exp Med Biol. 2014;818:167-80. Review. PubMed, CrossRef
  14. Mahalingam D, Szegezdi E, Keane M, de Jong S, Samali A. TRAIL receptor signalling and modulation: Are we on the right TRAIL? Cancer Treat Rev. 2009 May;35(3):280-8. Review. PubMed, CrossRef
  15. Walczak H, Haas TL. Biochemical analysis of the native TRAIL death-inducing signaling complex. Methods Mol Biol. 2008;414:221-39. Review. PubMed, CrossRef
  16. Benschop R, Wei T, Na S. Tumor necrosis factor receptor superfamily member 21: TNFR-related death receptor-6, DR6. Adv Exp Med Biol. 2009;647:186-94. PubMed, CrossRef
  17. Screaton GR, Xu XN, Olsen AL, Cowper AE, Tan R, McMichael AJ, Bell JI. LARD: a new lymphoid-specific death domain containing receptor regulated by alternative pre-mRNA splicing. Proc Natl Acad Sci USA. 1997 Apr 29;94(9):4615-9. PubMed, PubMedCentral, CrossRef
  18. Lee HL, Park SH, Kim TM, Jung YY, Park MH, Oh SH, Yun HS, Jun HO, Yoo HS, Han SB, Lee US, Yoon JH, Song MJ, Hong JT. Bee venom inhibits growth of human cervical tumors in mice. Oncotarget. 2015 Mar 30;6(9):7280-92. PubMed, PubMedCentral, CrossRef
  19. Yang A, Wilson NS, Ashkenazi A. Proapoptotic DR4 and DR5 signaling in cancer cells: toward clinical translation. Curr Opin Cell Biol. 2010 Dec;22(6):837-44. Review. PubMed, CrossRef
  20. Allen JE, El-Deiry WS. Regulation of the human TRAIL gene. Cancer Biol Ther. 2012 Oct;13(12):1143-51. Review. PubMed, PubMedCentral, CrossRef
  21. Sun R, Zhang Y, Lv Q, Liu B, Jin M, Zhang W, He Q, Deng M, Liu X, Li G, Li Y, Zhou G, Xie P, Xie X, Hu J, Duan Z. Toll-like receptor 3 (TLR3) induces apoptosis via death receptors and mitochondria by up-regulating the transactivating p63 isoform alpha (TAP63alpha). J Biol Chem. 2011 May 6;286(18):15918-28. PubMed, PubMedCentral, CrossRef
  22. Twomey JD, Kim SR, Zhao L, Bozza WP, Zhang B. Spatial dynamics of TRAIL death receptors in cancer cells. Drug Resist Updat. 2015 Mar;19:13-21. Review.
    PubMed, CrossRef
  23. Holland PM. Death receptor agonist therapies for cancer, which is the right TRAIL? Cytokine Growth Factor Rev. 2014 Apr;25(2):185-93. PubMed, CrossRef
  24. Piao X, Ozawa T, Hamana H, Shitaoka K, Jin A, Kishi H, Muraguchi A. TRAIL-receptor 1 IgM antibodies strongly induce apoptosis in human cancer cells in vitro and in vivo. Oncoimmunology. 2016 May 4;5(5):e1131380. PubMed, PubMedCentral,  CrossRef
  25. Kumazaki M, Shinohara H, Taniguchi K, Takai T, Kuranaga Y, Sugito N, Akao Y. Perturbation of the Warburg effect increases the sensitivity of cancer cells to TRAIL-induced cell death. Exp Cell Res. 2016 Sep 10;347(1):133-42. PubMed, CrossRef
  26. Nogueira DR, Yaylim I, Aamir Q, Kahraman OT, Fayyaz S, Kamran-ul-Hassan Naqvi S, Farooqi AA. TRAIL mediated signaling in pancreatic cancer. Asian Pac J Cancer Prev. 2014;15(15):5977-82. PubMed, CrossRef
  27. Talekar MK, Allen JE, Dicker DT, El-Deiry WS. ONC201 induces cell death in pediatric non-Hodgkin’s lymphoma cells. Cell Cycle. 2015 Aug 3;14(15):2422-8. PubMed, PubMedCentral, CrossRef
  28. Li X, Huang JM, Wang JN, Xiong XK, Yang XF, Zou F. Combination of chrysin and cisplatin promotes the apoptosis of Hep G2 cells by up-regulating p53. Chem Biol Interact. 2015 May 5;232:12-20. PubMed, CrossRef
  29. Kollipara PS, Jeong HS, Han SB, Hong JT. (E)-2,4-bis(p-hydroxyphenyl)-2-butenal has an antiproliferative effect on NSCLC cells induced by p38 MAPK-mediated suppression of NF-κB and up-regulation of TNFRSF10B (DR5). Br J Pharmacol. 2013 Mar;168(6):1471-84.  PubMed, PubMedCentral, CrossRef
  30. Huet HA, Growney JD, Johnson JA, Li J, Bilic S, Ostrom L, Zafari M, Kowal C, Yang G, Royo A, Jensen M, Dombrecht B, Meerschaert KR, Kolkman JA, Cromie KD, Mosher R, Gao H, Schuller A, Isaacs R, Sellers WR, Ettenberg SA. Multivalent nanobodies targeting death receptor 5 elicit superior tumor cell killing through efficient caspase induction. MAbs. 2014;6(6):1560-70. PubMed, PubMedCentral, CrossRef
  31. Kobayashi E, Kishi H, Ozawa T, Hamana H, Nakagawa H, Jin A, Lin Z, Muraguchi A. A chimeric antigen receptor for TRAIL-receptor 1 induces apoptosis in various types of tumor cells. Biochem Biophys Res Commun. 2014 Oct 31;453(4):798-803. PubMed, CrossRef
  32. Zhang M, Su L, Xiao Z, Liu X, Liu X. Methyl jasmonate induces apoptosis and pro-apoptotic autophagy via the ROS pathway in human non-small cell lung cancer. Am J Cancer Res. 2016 Jan 15;6(2):187-99. PubMed, PubMedCentral
  33. Krönung SK, Beyer U, Chiaramonte ML, Dolfini D, Mantovani R, Dobbelstein M. LTR12 promoter activation in a broad range of human tumor cells by HDAC inhibition. Oncotarget. 2016 Jun 7;7(23):33484-97. PubMed, CrossRef
  34. Beyer U, Krönung SK, Leha A, Walter L, Dobbelstein M. Comprehensive identification of genes driven by ERV9-LTRs reveals TNFRSF10B as a re-activatable mediator of testicular cancer cell death. Cell Death Differ. 2016 Jan;23(1):64-75.  PubMed, PubMedCentral, CrossRef
  35. Yu R, Albarenque SM, Cool RH, Quax WJ, Mohr A, Zwacka RM. DR4 specific TRAIL variants are more efficacious than wild-type TRAIL in pancreatic cancer. Cancer Biol Ther. 2014;15(12):1658-66. PubMed, PubMedCentral, CrossRef
  36. Khan M, Bi Y, Qazi JI, Fan L, Gao H. Evodiamine sensitizes U87 glioblastoma cells to TRAIL via the death receptor pathway. Mol Med Rep. 2015 Jan;11(1):257-62. PubMed, CrossRef
  37. Wang J, Hansen K, Edwards R, Van Houten B, Qian W.  Mitochondrial division inhibitor 1 (mdivi-1) enhances death receptor-mediated apoptosis in human ovarian cancer cells. Biochem Biophys Res Commun. 2015 Jan 2;456(1):7-12. PubMed, PubMedCentral, CrossRef
  38. Tse AC, Li JW, Chan TF, Wu RS, Lai KP. Hypoxia induces miR-210, leading to anti-apoptosis in ovarian follicular cells of marine medaka Oryzias melastigma. Aquat Toxicol. 2015 Aug;165:189-96. PubMed, CrossRef
  39. Lin CM, Ma JM, Zhang L, Hao ZY, Zhou J, Zhou ZY, Shi HQ, Zhang YF, Shao EM, Liang CZ. Inhibition of Transient Receptor Potential Melastain 7 Enhances Apoptosis Induced by TRAIL in PC-3 cells. Asian Pac J Cancer Prev. 2015;16(10):4469-75. PubMed
  40. Xu K, Olsen O, Tzvetkova-Robev D, Tessier-Lavigne M, Nikolov DB. The crystal structure of DR6 in complex with the amyloid precursor protein provides insight into death receptor activation. Genes Dev. 2015 Apr 15;29(8):785-90. PubMed, PubMedCentral, CrossRef
  41. Mirzaei MR, Najafi A, Arababadi MK, Asadi MH, Mowla SJ. Altered expression of apoptotic genes in response to OCT4B1 suppression in human tumor cell lines. Tumour Biol. 2014 Oct;35(10):9999-10009.  PubMed, CrossRef
  42. Jang JY, Jeon YK, Choi Y, Kim CW. Short-hairpin RNA-induced suppression of adenine nucleotide translocase-2 in breast cancer cells restores their susceptibility to TRAIL-induced apoptosis by activating JNK and modulating TRAIL receptor expression. Mol Cancer. 2010 Sep 28;9:262. PubMed, PubMedCentral, CrossRef
  43. He Y, Yu Z, Ge D, Wang-Sattler R, Thiesen HJ, Xie L, Li Y. Cell type specificity of signaling: view from membrane receptors distribution and their downstream transduction networks. Protein Cell. 2012 Sep;3(9):701-13. PubMed, PubMedCentral, CrossRef
  44. Lalaoui N, Morlé A, Mérino D, Jacquemin G, Iessi E, Morizot A, Shirley S, Robert B, Solary E, Garrido C, Micheau O. TRAIL-R4 promotes tumor growth and resistance to apoptosis in cervical carcinoma HeLa cells through AKT. PLoS One. 2011;6(5):e19679.  PubMed, PubMedCentral, CrossRef
  45. Gottwald L, Pasz-Walczak G, Piekarski J, Szwalski J, Kubiak R, Spych M, Suzin J, Tyliński W, Sęk P, Jeziorski A. Membrane expression of trail receptors DcR1 and DcR2 in the normal endometrium, endometrial atypical hyperplasia and endometrioid endometrial cancer. J Obstet Gynaecol. 2014 May;34(4):346-9. PubMed, CrossRef
  46. Tanenbaum DG, Hall WA, Colbert LE, Bastien AJ, Brat DJ, Kong J, Kim S, Dwivedi B, Kowalski J, Landry JC, Yu DS. TNFRSF10C copy number variation is associated with metastatic colorectal cancer. J Gastrointest Oncol. 2016 Jun;7(3):306-14. PubMed, PubMedCentral, CrossRef
  47. Shin D, Kwon HY, Sohn EJ, Nam MS, Kim JH, Lee JC, Ryu SY, Park B, Kim SH. Upregulation of Death Receptor 5 and Production of Reactive Oxygen Species Mediate Sensitization of PC-3 Prostate Cancer Cells to TRAIL Induced Apoptosis by Vitisin A. Cell Physiol Biochem. 2015;36(3):1151-62.  PubMed, CrossRef
  48. Narayan G, Xie D, Ishdorj G, Scotto L, Mansukhani M, Pothuri B, Wright JD, Kaufmann AM, Schneider A, Arias-Pulido H, Murty VV. Epigenetic inactivation of TRAIL decoy receptors at 8p12-21.3 commonly deleted region confers sensitivity to Apo2L/trail-Cisplatin combination therapy in cervical cancer. Genes Chromosomes Cancer. 2016 Feb;55(2):177-89.  PubMed, CrossRef
  49. Ratzinger G, Mitteregger S, Wolf B, Berger R, Zelger B, Weinlich G, Fritsch P, Goebel G, Fiegl H. Association of TNFRSF10D DNA-methylation with the survival of melanoma patients. Int J Mol Sci. 2014 Jul 7;15(7):11984-95. PubMed, PubMedCentral, CrossRef
  50. Pei GT, Wu CW, Lin WW. Hypoxia-induced decoy receptor 2 gene expression is regulated via a hypoxia-inducible factor 1alpha-mediated mechanism. Biochem Biophys Res Commun. 2010 Jan 8;391(2):1274-9. PubMed, CrossRef
  51. Mansour NM, Bernal GM, Wu L, Crawley CD, Cahill KE, Voce DJ, Balyasnikova IV, Zhang W, Spretz R, Nunez L, Larsen GF, Weichselbaum RR, Yamini B. Decoy Receptor DcR1 Is Induced in a p50/Bcl3-Dependent Manner and Attenuates the Efficacy of Temozolomide. Cancer Res. 2015 May 15;75(10):2039-48.  PubMed, PubMedCentral, CrossRef
  52. Jiang YQ, Zhong TF, Dang YW, Zou LS, Yang L, Yang X, Chen G. Overexpression and clinicopathological contribution of DcR3 in bladder urothelial carcinoma tissues. Asian Pac J Cancer Prev. 2014;15(21):9137-42. PubMed
  53. Jiang M, Lin X, He R, Lin X, Liang L, Tang R, Xiong D, Wei K, Dang Y, Feng Z, Chen G. Decoy Receptor 3 (DcR3) as a Biomarker of Tumor Deterioration in Female Reproductive Cancers: A Meta-Analysis. Med Sci Monit. 2016 Jun 1;22:1850-7. PubMed, PubMedCentral, CrossRef
  54. Im J, Kim K, Hergert P, Nho RS. Idiopathic pulmonary fibrosis fibroblasts become resistant to Fas ligand-dependent apoptosis via the alteration of decoy receptor 3. J Pathol. 2016 Sep;240(1):25-37. PubMed, PubMedCentral, CrossRef
  55. Hu R, Liu W, Qiu X, Lin Z, Xie Y, Hong X, Paerhati R, Qi Z, Zhuang G, Liu Z. Expression of tumor necrosis factor-α-induced protein 8 in stage III gastric cancer and the correlation with DcR3 and ERK1/2. Oncol Lett. 2016 Mar;11(3):1835-1840. PubMed, PubMedCentral
  56. Zhang Y, Li D, Zhao X, Song S, Zhang L, Zhu D, Wang Z, Chen X, Zhou J. Decoy receptor 3 suppresses FasL-induced apoptosis via ERK1/2 activation in pancreatic cancer cells. Biochem Biophys Res Commun. 2015 Aug 7;463(4):1144-51. PubMed, CrossRef
  57. Goswami S, Sharma-Walia N. Osteoprotegerin rich tumor microenvironment: implications in breast cancer. Oncotarget. 2016 Apr 8. [Epub ahead of print] Review.
    PubMed, CrossRef
  58. Steagall WK, Pacheco-Rodriguez G, Glasgow CG, Ikeda Y, Lin JP, Zheng G, Moss J. Osteoprotegerin contributes to the metastatic potential of cells with a dysfunctional TSC2 tumor-suppressor gene. Am J Pathol. 2013 Sep;183(3):938-50. PubMed, PubMedCentral,  CrossRef
  59. Bosman MC, Reis CR, Schuringa JJ, Vellenga E, Quax WJ. Decreased affinity of recombinant human tumor necrosis factor-related apoptosis-inducing ligand (rhTRAIL) D269H/E195R to osteoprotegerin (OPG) overcomes TRAIL resistance mediated by the bone microenvironment. J Biol Chem. 2014 Jan 10;289(2):1071-8. PubMed, PubMedCentral, CrossRef
  60. Huang H, Ma L, Kyrkanides S. Effects of vascular endothelial growth factor on osteoblasts and osteoclasts. Am J Orthod Dentofacial Orthop. 2016 Mar;149(3):366-73.
    PubMed, CrossRef
  61. Chouchana L, Fernández-Ramos AA, Dumont F, Marchetti C, Ceballos-Picot I, Beaune P, Gurwitz D, Loriot MA.  Molecular insight into thiopurine resistance: transcriptomic signature in lymphoblastoid cell lines. Genome Med. 2015 Apr 18;7(1):37.  PubMed, PubMedCentral, CrossRef
  62. Bonazzi VF, Nancarrow DJ, Stark MS, Moser RJ, Boyle GM, Aoude LG, Schmidt C, Hayward NK. Cross-platform array screening identifies COL1A2, THBS1, TNFRSF10D and UCHL1 as genes frequently silenced by methylation in melanoma. PLoS One. 2011;6(10):e26121. PubMed, PubMedCentral, CrossRef
  63. Todorova T, Bock FJ, Chang P. PARP13 regulates cellular mRNA post-transcriptionally and functions as a pro-apoptotic factor by destabilizing TRAILR4 transcript. Nat Commun. 2014 Nov 10;5:5362. PubMed, PubMedCentral, CrossRef
  64. Todorova T, Bock FJ, Chang P. Poly(ADP-ribose) polymerase-13 and RNA regulation in immunity and cancer. Trends Mol Med. 2015 Jun;21(6):373-84. Review. PubMed, PubMedCentral, CrossRef
  65. Zuo C, Qiu X, Liu N, Yang D, Xia M, Liu J, Wang X, Zhu H, Xie H, Dan H, Li Q, Wu Q, Burns M, Liu C. Interferon-α and cyclooxygenase-2 inhibitor cooperatively mediates TRAIL-induced apoptosis in hepatocellular carcinoma. Exp Cell Res. 2015 May 1;333(2):316-26. PubMed, CrossRef
  66. Weber TG, Pöschinger T, Galbán S, Rehemtulla A, Scheuer W. Noninvasive monitoring of pharmacodynamics and kinetics of a death receptor 5 antibody and its enhanced apoptosis induction in sequential application with doxorubicin. Neoplasia. 2013 Aug;15(8):863-74. PubMed, PubMedCentral, CrossRef
  67. Haselmann V, Kurz A, Bertsch U, Hübner S, Olempska-Müller M1, Fritsch J, Häsler R, Pickl A, Fritsche H, Annewanter F, Engler C, Fleig B, Bernt A, Röder C, Schmidt H, Gelhaus C, Hauser C, Egberts JH, Heneweer C, Rohde AM, Böger C, Knippschild U, Röcken C, Adam D, Walczak H, Schütze S, Janssen O, Wulczyn FG, Wajant H, Kalthoff H, Trauzold A. Nuclear death receptor TRAIL-R2 inhibits maturation of let-7 and promotes proliferation of pancreatic and other tumor cells. Gastroenterology. 2014 Jan;146(1):278-90. PubMed, CrossRef
  68. Lim B, Allen JE, Prabhu VV, Talekar MK, Finnberg NK, El-Deiry WS. Targeting TRAIL in the treatment of cancer: new developments. Expert Opin Ther Targets. 2015;19(9):1171-85. Review. PubMed, CrossRef
  69. Minchenko OH, Kryvdiuk IV, Minchenko DO, Riabovol OO, Halkin OV. InhibitionofIRE1signalingaffectsexpression of asubset genes encoding for TNF-related factors andreceptors and modifies their hypoxic regulation in U87 glioma cells. Endoplasm Reticul Stress Dis. 2016;3(1):1-15. CrossRef
  70. Tian X, Ye J, Alonso-Basanta M, Hahn SM, Koumenis C, Dorsey JF. Modulation of CCAAT/enhancer binding protein homologous protein (CHOP)-dependent DR5 expression by nelfinavir sensitizes glioblastoma multiforme cells to tumor necrosis factor-related apoptosis-inducing ligand (TRAIL). J Biol Chem. 2011 Aug 19;286(33):29408-16.  PubMed, PubMedCentral, CrossRef
  71. Chevet E, Hetz C, Samali A. Endoplasmic reticulum stress-activated cell reprogramming in oncogenesis. Cancer Discov. 2015 Jun;5(6):586-97.  PubMed, CrossRef
  72. Wang S, Kaufman RJ. The impact of the unfolded protein response on human disease. J Cell Biol. 2012 Jun 25;197(7):857-67.  PubMed, PubMedCentral, CrossRef
  73. Hetz C, Chevet E, Harding HP. Targeting the unfolded protein response in disease. Nat Rev Drug Discov. 2013 Sep;12(9):703-19. PubMed, CrossRef
  74. Manié SN, Lebeau J, Chevet E. Cellular mechanisms of endoplasmic reticulum stress signaling in health and disease. 3. Orchestrating the unfolded protein response in oncogenesis: an update. Am J Physiol Cell Physiol. 2014 Nov 15;307(10):C901-7. PubMed, CrossRef
  75. Auf G, Jabouille A, Guérit S, Pineau R, Delugin M, Bouchecareilh M, Magnin N, Favereaux A, Maitre M, Gaiser T, von Deimling A, Czabanka M, Vajkoczy P, Chevet E, Bikfalvi A, Moenner M. Inositol-requiring enzyme 1alpha is a key regulator of angiogenesis and invasion in malignant glioma. Proc Natl Acad Sci USA. 2010 Aug 31;107(35):15553-8. PubMed, PubMedCentral, CrossRef
  76. Malhotra JD, Kaufman RJ. ER stress and its functional link to mitochondria: role in cell survival and death. Cold Spring Harb Perspect Biol. 2011 Sep 1;3(9):a004424. PubMed, PubMedCentral, CrossRef
  77. Minchenko DO, Kharkova AP, Halkin OV, Karbovskyi LL, Minchenko OH. Effect of hypoxia on the expression of genes encoding insulin-like growth factors and some related proteins in U87 glioma cells without IRE1 function. Endocr Regul. 2016 Apr;50(2):43-54. PubMed, CrossRef
  78. Minchenko OH,Tsymbal DO,Minchenko DO, Riabovol OO, Ratushna OO. Hypoxic regulation of the expressions of proliferation related genes in U87 glioma cells upon inhibition of IRE1 signaling. Ukr Biochem J. 2016;88(1):11-21.  CrossRef
  79. Minchenko OH, Kryvdiuk IV, Riabovol OO, MinchenkoDO, Danilovskyi SV, Ratushna OO. Inhibition of IRE1 modifies the hypoxic regulation of GADD family gene expressions in U87 glioma cells. Ukr Biochem J. 2016;88(2):25-34. CrossRef
  80. Auf G, Jabouille A, Delugin M, Guérit S, Pineau R, North S, Platonova N, Maitre M, Favereaux A, Vajkoczy P, Seno M, Bikfalvi A, Minchenko D, Minchenko O, Moenner M. High epiregulin expression in human U87 glioma cells relies on IRE1α and promotes autocrine growth through EGF receptor. BMC Cancer. 2013 Dec 13;13:597. PubMed, PubMedCentral, CrossRef
  81. Minchenko DO, Danilovskyi SV,Kryvdiuk IV, Bakalets TV,Lypova NM, Karbovsky LL, Minchenko OH. Inhibition of ERN1 modifies the hypoxic regulation of the expression of TP53-related genes in U87 glioma cells. Endoplasm Reticul Stress Dis. 2014; 1(1): 18-26. CrossRef
  82. Minchenko DО, Karbovskyi LL, Danilovskyi SV, Moenner M, Minchenko OH. Effect of hypoxia and glutamine or glucose deprivation on the expression of retinoblastoma and retinoblastoma-related genes in ERN1 knockdown glioma U87 cell line. Am J Mol Biol. 2012;2(1):21-31.  CrossRef
  83. Minchenko DO, Kharkova AP, Karbovskyi LL, Minchenko OH. Expression of insulin-like growth factor binding protein genes and its hypoxic regulation in U87 glioma cells depends on ERN1 mediated signaling pathway of endoplasmic reticulum stress. Endocr Regul. 2015 Apr;49(2):73-83. PubMed, CrossRef
  84. Minchenko OH, Kharkova AP, Minchenko DO, Karbovskyi LL. Effect of hypoxia on the expression of genes that encode some IGFBP and CCN proteins in U87 glioma cells depends on IRE1 signaling. Ukr Biochem J. 2015 Nov-Dec;87(6):52-63. PubMed, CrossRef
  85. Zeng L, Li T, Xu DC, Liu J, Mao G, Cui MZ, Fu X, Xu X. Death receptor 6 induces apoptosis not through type I or type II pathways, but via a unique mitochondria-dependent pathway by interacting with Bax protein. J Biol Chem. 2012 Aug 17;287(34):29125-33. PubMed, PubMedCentral,  CrossRef
  86. Li T, Su L, Lei Y, Liu X, Zhang Y, Liu X. DDIT3 and KAT2A Proteins Regulate TNFRSF10A and TNFRSF10B Expression in Endoplasmic Reticulum Stress-mediated Apoptosis in Human Lung Cancer Cells. J Biol Chem. 2015 Apr 24;290(17):11108-18.  PubMed, PubMedCentral,  CrossRef
  87. Edagawa M, Kawauchi J, Hirata M, Goshima H, Inoue M, Okamoto T, Murakami A, Maehara Y, Kitajima S. Role of activating transcription factor 3 (ATF3) in endoplasmic reticulum (ER) stress-induced sensitization of p53-deficient human colon cancer cells to tumor necrosis factor (TNF)-related apoptosis-inducing ligand (TRAIL)-mediated apoptosis through up-regulation of death receptor 5 (DR5) by zerumbone and celecoxib. J Biol Chem. 2014 Aug 1;289(31):21544-61. PubMed, PubMedCentral, CrossRef
  88. Liu J, Edagawa M, Goshima H, Inoue M, Yagita H, Liu Z, Kitajima S. Role of ATF3 in synergistic cancer cell killing by a combination of HDAC inhibitors and agonistic anti-DR5 antibody through ER stress in human colon cancer cells. Biochem Biophys Res Commun. 2014 Mar 7;445(2):320-6. PubMed, CrossRef
  89. Farooqi AA, Li KT, Fayyaz S, Chang YT, Ismail M, Liaw CC, Yuan SS, Tang JY, Chang HW. Anticancer drugs for the modulation of endoplasmic reticulum stress and oxidative stress. Tumour Biol. 2015 Aug;36(8):5743-52. PubMed, PubMedCentral, CrossRef
  90. Hu R, Du Q, Yin X1, Li J, Wang T, Zhang L. Agonist antibody activates death receptor 6 downstream signaling involving TRADD recruitment. FEBS Lett. 2014 Jan 31;588(3):401-7.  PubMed, CrossRef
  91. Johnson GG, White MC, Grimaldi M. Stressed to death: targeting endoplasmic reticulum stress response induced apoptosis in gliomas. Curr Pharm Des. 2011;17(3):284-92. PubMed, PubMedCentral, CrossRef
  92. Oikonomou E, Pintzas A. The TRAIL of oncogenes to apoptosis. Biofactors. 2013 Jul-Aug;39(4):343-54. PubMed, CrossRef
  93. Micheau O, Shirley S, Dufour F. Death receptors as targets in cancer. Br J Pharmacol. 2013 Aug;169(8):1723-44. PubMed, PubMedCentral, CrossRef
Creative CommonsThis work is licensed under a Creative Commons Attribution 4.0 International License.