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Research Paper

Radiation induces EIF2AK3/PERK and ERN1/IRE1 mediated pro-survival autophagy

ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon, ORCID Icon & ORCID Icon
Pages 1391-1406 | Received 11 Mar 2018, Accepted 29 Jan 2019, Published online: 20 Mar 2019

References

  • Kiang JG, Garrison BR, Gorbunov NV. Radiation combined injury: DNA damage, apoptosis and autophagy. Adapt Med. 2010;2(1):1–10.
  • Gorbunov NV, Kiang JG. Up-regulation of autophagy in small intestine Paneth cells in response to total-body gamma-irradiation. J Pathol. 2009 Oct;219(2):242–252. PubMed PMID: 19681094.
  • Kiang JG, Smith JT, Agravante NG. Geldanamycin analog 17-DMAG inhibits iNOS and caspases in gamma-irradiated human T cells. Radiat Res. 2009 Sep;172(3):321–330. PubMed PMID: 19708781.
  • Mikkelsen RB, Wardman P. Biological chemistry of reactive oxygen and nitrogen and radiation-induced signal transduction mechanisms. Oncogene. 2003 Sep 1;22(37):5734–5754. PubMed PMID: 12947383.
  • Chaurasia M, Bhatt AN, Das A, et al. Radiation-induced autophagy: mechanisms and consequences. Free Radic Res. 2016;50(3):273–290. PubMed PMID: 26764568.
  • Buytaert E, Dewaele M, Agostinis P. Molecular effectors of multiple cell death pathways initiated by photodynamic therapy. Biochim Biophys Acta. 2007 Sep;1776(1):86–107. PubMed PMID: 17693025.
  • Farrukh MR, Nissar UA, Afnan Q, et al. Oxidative stress mediated Ca(2+) release manifests endoplasmic reticulum stress leading to unfolded protein response in UV-B irradiated human skin cells. J Dermatol Sci. 2014 Jul;75(1):24–35. PubMed PMID: 24794973.
  • Nakai A, Yamaguchi O, Takeda T, et al. The role of autophagy in cardiomyocytes in the basal state and in response to hemodynamic stress. Nat Med. 2007 May;13(5):619–624. PubMed PMID: 17450150.
  • Chen Y, Azad MB, Gibson SB. Superoxide is the major reactive oxygen species regulating autophagy. Cell Death Differ. 2009 Jul;16(7):1040–1052. PubMed PMID: 19407826.
  • Fulda S, Gorman AM, Hori O, et al. Cellular stress responses: cell survival and cell death. Int J Cell Biol. 2010;2010:214074. PubMed PMID: 20182529; PubMed Central PMCID: PMCPMC2825543.
  • Zhang Y, Qi H, Taylor R, et al. The role of autophagy in mitochondria maintenance: characterization of mitochondrial functions in autophagy-deficient S. cerevisiae strains. Autophagy. 2007 Jul-Aug;3(4):337–346. PubMed PMID: 17404498.
  • Mizushima N. Autophagy: process and function. Genes Dev. 2007 Nov 15;21(22):2861–2873. PubMed PMID: 18006683.
  • Marino G, Niso-Santano M, Baehrecke EH, et al. Self-consumption: the interplay of autophagy and apoptosis. Nat Rev Mol Cell Biol. 2014 Feb;15(2):81–94. PubMed PMID: 24401948; PubMed Central PMCID: PMCPMC3970201.
  • Yang Z, Xu Y, Xu L, et al. Regulation of autophagy via PERK-eIF2alpha effectively relieve the radiation myelitis induced by iodine-125. PLoS One. 2013;8(11):e76819. PubMed PMID: 24223705; PubMed Central PMCID: PMCPMC3818370.
  • Kim KW, Moretti L, Mitchell LR, et al. Endoplasmic reticulum stress mediates radiation-induced autophagy by perk-eIF2alpha in caspase-3/7-deficient cells. Oncogene. 2010 Jun 3;29(22):3241–3251. PubMed PMID: 20348950; PubMed Central PMCID: PMCPMC2953962.
  • Kong EY, Cheng SH, Yu KN. Induction of autophagy and interleukin 6 secretion in bystander cells: metabolic cooperation for radiation-induced rescue effect? J Radiat Res. 2018 Mar 1;59(2):129–140. PubMed PMID: 29385614; PubMed Central PMCID: PMCPMC5951087.
  • Wang F, Tang J, Li P, et al. Chloroquine enhances the radiosensitivity of bladder cancer cells by inhibiting autophagy and activating apoptosis. Cell Physiol Biochem. 2018;45(1):54–66. PubMed PMID: 29316551.
  • Chen Y, Li X, Guo L, et al. Combining radiation with autophagy inhibition enhances suppression of tumor growth and angiogenesis in esophageal cancer. Mol Med Rep. 2015 Aug;12(2):1645–1652. PubMed PMID: 25891159; PubMed Central PMCID: PMCPMC4464360.
  • Hu JL, He GY, Lan XL, et al. Inhibition of ATG12-mediated autophagy by miR-214 enhances radiosensitivity in colorectal cancer. Oncogenesis. 2018 Feb 20;7(2):16. PubMed PMID: 29459645; PubMed Central PMCID: PMCPMC5833763.
  • Paglin S, Hollister T, Delohery T, et al. A novel response of cancer cells to radiation involves autophagy and formation of acidic vesicles. Cancer Res. 2001 Jan 15;61(2):439–444. PubMed PMID: 11212227.
  • Sailaja GS, Bhoopathi P, Gorantla B, et al. The secreted protein acidic and rich in cysteine (SPARC) induces endoplasmic reticulum stress leading to autophagy-mediated apoptosis in neuroblastoma. Int J Oncol. 2013 Jan;42(1):188–196. PubMed PMID: 23123816; PubMed Central PMCID: PMCPMC3538858.
  • Scriven P, Brown NJ, Pockley AG, et al. The unfolded protein response and cancer: a brighter future unfolding? J Mol Med (Berl). 2007 Apr;85(4):331–341. PubMed PMID: 17216204.
  • Black HS. ROS: a step closer to elucidating their role in the etiology of light-induced skin disorders. J Invest Dermatol. 2004 Jun;122(6):xiii–xiv. PubMed PMID: 15175053.
  • Briganti S, Picardo M. Antioxidant activity, lipid peroxidation and skin diseases. What’s new. J Eur Acad Dermatol Venereol. 2003 Nov;17(6):663–669. PubMed PMID: 14761133.
  • Ding W, Yang L, Zhang M, et al. Reactive oxygen species-mediated endoplasmic reticulum stress contributes to aldosterone-induced apoptosis in tubular epithelial cells. Biochem Biophys Res Commun. 2012 Feb 17;418(3):451–456. PubMed PMID: 22281495.
  • Ron D, Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol. 2007 Jul;8(7):519–529. PubMed PMID: 17565364.
  • Malhotra JD, Kaufman RJ. Endoplasmic reticulum stress and oxidative stress: a vicious cycle or a double-edged sword? Antioxid Redox Signal. 2007 Dec;9(12):2277–2293. PubMed PMID: 17979528.
  • Moretti L, Cha YI, Niermann KJ, et al. Switch between apoptosis and autophagy: radiation-induced endoplasmic reticulum stress? Cell Cycle. 2007 Apr 1;6(7):793–798. PubMed PMID: 17377498.
  • Castino R, Davies J, Beaucourt S, et al. Autophagy is a prosurvival mechanism in cells expressing an autosomal dominant familial neurohypophyseal diabetes insipidus mutant vasopressin transgene. FASEB J. 2005 Jun;19(8):1021–1023. PubMed PMID: 15781609.
  • Alnasser HA, Guan Q, Zhang F, et al. Requirement of clusterin expression for prosurvival autophagy in hypoxic kidney tubular epithelial cells. Am J Physiol Renal Physiol. 2016 Jan 15;310(2): F160–73. PubMed PMID: 26561650.
  • Hsieh CH, Pai PY, Hsueh HW, et al. Complete induction of autophagy is essential for cardioprotection in sepsis. Ann Surg. 2011 Jun;253(6):1190–1200. PubMed PMID: 21412148.
  • Li J, Qin Z, Liang Z. The prosurvival role of autophagy in Resveratrol-induced cytotoxicity in human U251 glioma cells. BMC Cancer. 2009 Jun 30;9:215. PubMed PMID: 19566920; PubMed Central PMCID: PMCPMC2717978.
  • Dalby KN, Tekedereli I, Lopez-Berestein G, et al. Targeting the prodeath and prosurvival functions of autophagy as novel therapeutic strategies in cancer. Autophagy. 2010 Apr;6(3):322–329. PubMed PMID: 20224296; PubMed Central PMCID: PMCPMC2914492.
  • Klionsky DJ, Abdalla FC, Abeliovich H, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy. 2012 Apr;8(4):445–544. PubMed PMID: 22966490; PubMed Central PMCID: PMCPMC3404883.
  • Lin JH, Walter P, Yen TS. Endoplasmic reticulum stress in disease pathogenesis. Annu Rev Pathol. 2008;3:399–425. PubMed PMID: 18039139; PubMed Central PMCID: PMCPMC3653419.
  • Ogata M, Hino S, Saito A, et al. Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol Cell Biol. 2006 Dec;26(24):9220–9231. PubMed PMID: 17030611; PubMed Central PMCID: PMCPMC1698520.
  • Yorimitsu T, Nair U, Yang Z, et al. Endoplasmic reticulum stress triggers autophagy. J Biol Chem. 2006 Oct 6;281(40):30299–30304. PubMed PMID: 16901900; PubMed Central PMCID: PMCPMC1828866.
  • Li T, Su L, Zhong N, et al. Salinomycin induces cell death with autophagy through activation of endoplasmic reticulum stress in human cancer cells. Autophagy. 2013 Jul;9(7):1057–1068. PubMed PMID: 23670030; PubMed Central PMCID: PMCPMC3722315.
  • Cao SS, Kaufman RJ. Endoplasmic reticulum stress and oxidative stress in cell fate decision and human disease. Antioxid Redox Signal. 2014 Jul 20;21(3):396–413. PubMed PMID: 24702237; PubMed Central PMCID: PMCPMC4076992.
  • Xue X, Piao JH, Nakajima A, et al. Tumor necrosis factor alpha (TNFalpha) induces the unfolded protein response (UPR) in a reactive oxygen species (ROS)-dependent fashion, and the UPR counteracts ROS accumulation by TNFalpha. J Biol Chem. 2005 Oct 7;280(40):33917–33925. PubMed PMID: 16107336.
  • Yen YP, Tsai KS, Chen YW, et al. Arsenic induces apoptosis in myoblasts through a reactive oxygen species-induced endoplasmic reticulum stress and mitochondrial dysfunction pathway. Arch Toxicol. 2012 Jun;86(6):923–933. PubMed PMID: 22622864.
  • Kouroku Y, Fujita E, Tanida I, et al. ER stress (PERK/eIF2alpha phosphorylation) mediates the polyglutamine-induced LC3 conversion, an essential step for autophagy formation. Cell Death Differ. 2007 Feb;14(2):230–239. PubMed PMID: 16794605.
  • Sun WT, Wang XC, Mak SK, et al. Activation of PERK branch of ER stress mediates homocysteine-induced BKCa channel dysfunction in coronary artery via FoxO3a-dependent regulation of atrogin-1. Oncotarget. 2017 Aug 1;8(31):51462–51477. PubMed PMID: 28881660; PubMed Central PMCID: PMCPMC5584261.
  • Huo Y, Fan L, Yin S, et al. Involvement of unfolded protein response, p53 and Akt in modulation of porcine reproductive and respiratory syndrome virus-mediated JNK activation. Virology. 2013 Sep;444( 1–2):233–240. PubMed PMID: 23850458.
  • Volkmann K, Lucas JL, Vuga D, et al. Potent and selective inhibitors of the inositol-requiring enzyme 1 endoribonuclease. J Biol Chem. 2011 Apr 8;286(14):12743–12755. PubMed PMID: 21303903; PubMed Central PMCID: PMCPMC3069474.
  • Komatsu M, Waguri S, Ueno T, et al. Impairment of starvation-induced and constitutive autophagy in Atg7-deficient mice. J Cell Biol. 2005 May 9;169(3):425–434. PubMed PMID: 15866887; PubMed Central PMCID: PMCPMC2171928.
  • Kuma A, Hatano M, Matsui M, et al. The role of autophagy during the early neonatal starvation period. Nature. 2004 Dec 23;432(7020):1032–1036. PubMed PMID: 15525940.
  • Mizushima N, Noda T, Yoshimori T, et al. A protein conjugation system essential for autophagy. Nature. 1998 Sep 24;395(6700):395–398. PubMed PMID: 9759731.
  • Komatsu M, Wang QJ, Holstein GR, et al. Essential role for autophagy protein Atg7 in the maintenance of axonal homeostasis and the prevention of axonal degeneration. Proc Natl Acad Sci U S A. 2007 Sep 4;104(36):14489–14494. PubMed PMID: 17726112; PubMed Central PMCID: PMCPMC1964831.
  • Fan XY, Tian C, Wang H, et al. Activation of the AMPK-ULK1 pathway plays an important role in autophagy during prion infection. Sci Rep. 2015 Oct 1;5:14728. PubMed PMID: 26423766; PubMed Central PMCID: PMCPMC4589734.
  • Yang ZJ, Chee CE, Huang S, et al. The role of autophagy in cancer: therapeutic implications. Mol Cancer Ther. 2011 Sep;10(9):1533–1541. PubMed PMID: 21878654; PubMed Central PMCID: PMCPMC3170456.
  • Zong Y, Feng S, Cheng J, et al. Up-regulated ATF4 expression increases cell sensitivity to apoptosis in response to radiation. Cell Physiol Biochem. 2017;41(2):784–794. PubMed PMID: 28214891.
  • Wang K, Klionsky DJ. Mitochondria removal by autophagy. Autophagy. 2011 Mar;7(3):297–300. PubMed PMID: 21252623; PubMed Central PMCID: PMCPMC3359476.
  • Reggiori F, Komatsu M, Finley K, et al. Selective types of autophagy. Int J Cell Biol. 2012;2012:156272. PubMed PMID: 22956958; PubMed Central PMCID: PMCPMC3432363.
  • Avivar-Valderas A, Bobrovnikova-Marjon E, Alan Diehl J, et al. Regulation of autophagy during ECM detachment is linked to a selective inhibition of mTORC1 by PERK. Oncogene. 2013 Oct 10;32(41):4932–4940. PubMed PMID: 23160380; PubMed Central PMCID: PMCPMC3600386.
  • Lee H, Noh JY, Oh Y, et al. IRE1 plays an essential role in ER stress-mediated aggregation of mutant huntingtin via the inhibition of autophagy flux. Hum Mol Genet. 2012 Jan 1;21(1):101–114. PubMed PMID: 21954231.
  • Inoki K, Zhu T, Guan KL. TSC2 mediates cellular energy response to control cell growth and survival. Cell. 2003 Nov 26;115(5):577–590. PubMed PMID: 14651849.
  • Qin L, Wang Z, Tao L, et al. ER stress negatively regulates AKT/TSC/mTOR pathway to enhance autophagy. Autophagy. 2010 Feb;6(2):239–247. PubMed PMID: 20104019.
  • Marquez RT, Xu L. Bcl-2:beclin1 complex: multiple, mechanisms regulating autophagy/apoptosis toggle switch. Am J Cancer Res. 2012;2(2):214–221. PubMed PMID: 22485198; PubMed Central PMCID: PMCPMC3304572.
  • Liang J, Shao SH, Xu ZX, et al. The energy sensing LKB1-AMPK pathway regulates p27(kip1) phosphorylation mediating the decision to enter autophagy or apoptosis. Nat Cell Biol. 2007 Feb;9(2):218–224. PubMed PMID: 17237771.
  • Stansborough RL, Bateman EH, Al-Dasooqi N, et al. Fractionated abdominal irradiation induces intestinal microvascular changes in an in vivo model of radiotherapy-induced gut toxicity. Support Care Cancer. 2017 Jun;25(6):1973–1983. PubMed PMID: 28175996.

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