22,942
Views
0
CrossRef citations to date
0
Altmetric
Special Focus on Autophagy in host-pathogen interactions

The roles of apoptosis, autophagy and unfolded protein response in arbovirus, influenza virus, and HIV infections

ORCID Icon, , ORCID Icon, , , , ORCID Icon, , , & ORCID Icon show all
Pages 376-413 | Received 14 Dec 2018, Accepted 08 Apr 2019, Published online: 30 Apr 2019

References

  • Baltimore D. Expression of animal virus genomes. Bacteriol Rev. 1971;35:235–241.
  • Mendez II, Swanson MS, Coombs KM. Introduction to virus structure, classification, replication, and hosts. In: Nath A, Berger JR, editors. Clinical neurovirology, in clinical neurovirology. New York (NY): Marcel-Dekker; 2003. p. 1–19.
  • Lefkowitz EJ, Dempsey DM, Hendrickson RC, et al. Virus taxonomy: the database of the international committee on taxonomy of viruses (ICTV). Nucleic Acids Res. 2018;46:D708–D717.
  • Fauquet CM, Mayo MA, Maniloff J, et al., Virus taxonomy. 8th Report of the International Committee on Taxonomy of Viruses. 2005.
  • WHO. Deaths by cause, age, sex, by country and by region, 2000–2016, global health estimates. Geneva: World Health Organization; 2018.
  • Gong J, Sachdev E, Mita AC, et al. Clinical development of reovirus for cancer therapy: an oncolytic virus with immune-mediated antitumor activity. World J Methodol. 2016;6:25–42.
  • Vitaliti G, Pratico AD, Cimino C, et al. Hepatitis B vaccine in celiac disease: yesterday, today and tomorrow. World J Gastroenterol. 2013;19:838–845.
  • Lin D, Koskella B, Ritz NL, et al. Perturbation of gut microbiome leads to fluctuations in phage population density. Gastroenterology. 2017;152:S819–S820.
  • Clem RJ, Passarelli AL. Baculoviruses: sophisticated pathogens of insects. PLoS Pathog. 2013;9:e1003729.
  • Voirol LRP, Frago E, Kaltenpoth M, et al. Bacterial symbionts in lepidoptera: their diversity, transmission, and impact on the host. Front Microbiol. 2018;9:556.
  • Weger-Lucarelli J, Auerswald H, Vignuzzi M, et al. Taking a bite out of nutrition and arbovirus infection. PLoS Negl Trop Dis. 2018;12:e0006247.
  • Bhatt S, Gething PW, Brady OJ, et al. The global distribution and burden of dengue. Nature. 2013;496:504–507.
  • Heymann DL, Hodgson A, Sall AA, et al. Zika virus and microcephaly: why is this situation a PHEIC? Lancet. 2016;387:719–721.
  • Sacramento CQ, de Melo GR, de Freitas CS, et al. The clinically approved antiviral drug sofosbuvir inhibits Zika virus replication. Sci Rep. 2017;7:40920.
  • Duffy MR, Chen TH, Hancock WT, et al. Zika virus outbreak on yap Island, federated states of micronesia. N Engl J Med. 2009;360:2536–2543.
  • Palese P, Shaw ML. Orthomyxoviridae: the viruses and their replication. In: Knipe DM, Howley PM, editors. Fields Virology. Philadelphia: Lippincott Williams & Wilkins; 2007. p. 1647–1689.
  • Tong SX, Li Y, Rivailler P, et al. A distinct lineage of influenza A virus from bats. Proceedings of the National Academy of Sciences. 109 (2012) 4269–4274
  • Prevention CfDCa. Types of influenza viruses. 2016 2016 Jun 17]; Available from: http://www.cdc.gov/flu/about/viruses/types.htm.
  • Sellers SA, Hagan RS, Hayden FG, et al. The hidden burden of influenza: A review of the extra-pulmonary complications of influenza infection. Influenza Other Respir Viruses. 2017;11:372–393.
  • Kwong JC, Schwartz KL, Campitelli MA. Acute myocardial infarction after laboratory-confirmed influenza infection REPLY. N Engl J Med. 2018;378:2540–2541.
  • Bresee J, Fitzner J, Campbell H, et al. Progress and remaining gaps in estimating the global disease burden of influenza. Emerg Infect Dis. 2018;24:1173–1177.
  • Sautto GA, Kirchenbaum GA, Ross TM. Towards a universal influenza vaccine: different approaches for one goal. Virol J. 2018;15:17.
  • Freed EO, Martin MA. Human immunodeficiency viruses: replication. In: Knipe D, Howley PM, editors. Fields Virology. Philadelphia: Lippincott Williams & Wilkins; 2013. p. 1502–1560.
  • WHO. Estimated number of people dying from HIV-related causes, Global Health Observatory (GHO), 2017. Available from: www.who.int/gho/hiv/epidemic_status/deaths_text/en/.
  • Haynes BF, Burton DR. HIV developing an HIV vaccine What are the paths and obstacles to a practical vaccine? Science. 2017;355:1129–1130.
  • Liu MQ, Zhao M, Kong WH, et al. Combination antiretroviral therapy (cART) restores HIV-1 infection-mediated impairment of JAK-STAT signaling pathway. Oncotarget. 2017;8:22524–22533.
  • Fulda S, Gorman AM, Hori O, et al. Cellular stress responses: cell survival and cell death. Int J Cell Biol. 2010;2010:214074.
  • Hooper PL, Hightower LE, Hooper PL. Loss of stress response as a consequence of viral infection: implications for disease and therapy. Cell Stress Chaperones. 2012;17:647–655.
  • Burnett HF, Audas TE, Liang GQ, et al. Herpes simplex virus-1 disarms the unfolded protein response in the early stages of infection. Cell Stress Chaperones. 2012;17:473–483.
  • Zhang LR, Wang AM. Virus-induced ER stress and the unfolded protein response. Front Plant Sci. 2012;3:293.
  • Liu MM, Chen FZ, Liu T, et al. The role of oxidative stress in influenza virus infection. Microbes Infect. 2017;19:580–586.
  • Ong HK, Soo BPC, Chu KL, et al. XBP-1, a cellular target for the development of novel anti-viral strategies. Curr Protein Pept Sci. 2018;19:145–154.
  • Gladwyn-Ng I, Cordon-Barris L, Alfano C, et al. Stress-induced unfolded protein response contributes to Zika virus-associated microcephaly. Nat Neurosci. 2018;21:63-+.
  • Preston CM, Nicholl MJ. Induction of cellular stress overcomes the requirement of herpes simplex virus type 1 for immediate-early protein ICP0 and reactivates expression from quiescent viral genomes. J Virol. 2008;82:11775–11783.
  • Zhang ZW, Li ZL, Yuan S. The role of secretory autophagy in zika virus transfer through the placental barrier. Front Cell Infect Microbiol. 2017;6:206.
  • Kerr JF, Wyllie AH, Currie AR. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer. 1972;26:239–257.
  • Mokarram P, Albokashy M, Zarghooni M, et al. New frontiers in the treatment of colorectal cancer: autophagy and the unfolded protein response as promising targets. Autophagy. 2017;13:781–819.
  • Rashedi I, Panigrahi S, Ezzati P, et al. Autoimmunity and apoptosis–therapeutic implications. Curr Med Chem. 2007;14:3139–3151.
  • Wilson NS, Dixit V, Ashkenazi A. Death receptor signal transducers: nodes of coordination in immune signaling networks. Nat Immunol. 2009;10:348–355.
  • Ghavami S, Hashemi M, Ande SR, et al. Apoptosis and cancer: mutations within caspase genes. J Med Genet. 2009;46:497–510.
  • Cory S, Adams JM. The Bcl2 family: regulators of the cellular life-or-death switch. Nat Rev Cancer. 2002;2:647–656.
  • Strasser A, Vaux DL. Viewing BCL2 and cell death control from an evolutionary perspective. Cell Death Differ. 2018;25:13–20.
  • Dai H, Meng XW, Kaufmann SH. Mitochondrial apoptosis and BH3 mimetics. F1000Res. 2016;5:2804.
  • Sarosiek KA, Letai A. Directly targeting the mitochondrial pathway of apoptosis for cancer therapy using BH3 mimetics - recent successes, current challenges and future promise. FEBS J. 2016;283:3523–3533.
  • Sochalska M, Tuzlak S, Egle A, et al. Lessons from gain- and loss-of-function models of pro-survival Bcl2 family proteins: implications for targeted therapy. FEBS J. 2015;282:834–849.
  • Meier P, Finch A, Evan G. Apoptosis in development. Nature. 2000;407:796–801.
  • Tuzlak S, Kaufmann T, Villunger A. Interrogating the relevance of mitochondrial apoptosis for vertebrate development and postnatal tissue homeostasis. Genes Dev. 2016;30:2133–2151.
  • Vaux DL Toward an understanding of the molecular mechanisms of physiological cell death. Proceedings of the National Academy of Sciences of the United States of America. 90 (1993) 786–789
  • Nagata S, Tanaka M. Programmed cell death and the immune system. Nat Rev Immunol. 2017;17:333–340.
  • Kaczanowski S. Apoptosis: its origin, history, maintenance and the medical implications for cancer and aging. Phys Biol. 2016;13:031001.
  • Fadeel B, Orrenius S, Zhivotovsky B. Apoptosis in human disease: a new skin for the old ceremony? Biochem Biophys Res Commun. 1999;266:699–717.
  • Richardson H, Kumar S. Death to flies: drosophila as a model system to study programmed cell death. J Immunol Methods. 2002;265:21–38.
  • Cikala M, Wilm B, Hobmayer E, et al. Identification of caspases and apoptosis in the simple metazoan Hydra. Curr Biol. 1999;9:959–962.
  • Liu QA, Hengartner MO. The molecular mechanism of programmed cell death in C elegans. Ann N Y Acad Sci. 1999;887:92–104.
  • Solomon M, Belenghi B, Delledonne M, et al. The involvement of cysteine proteases and protease inhibitor genes in the regulation of programmed cell death in plants. Plant Cell. 1999;11:431–444.
  • Sueldo DJ, van der Hoorn RAL. Plant life needs cell death, but does plant cell death need Cys proteases? FEBS J. 2017;284:1577–1585.
  • Kabbage M, Kessens R, Bartholomay LC, et al. The life and death of a plant cell. Annu Rev Plant Biol. 2017;68:375–404.
  • Madeo F, Frohlich E, Ligr M, et al. Oxygen stress: a regulator of apoptosis in yeast. J Cell Biol. 1999;145:757–767.
  • Alizadeh J, Glogowska A, Thliveris J, et al. Autophagy modulates transforming growth factor beta 1 induced epithelial to mesenchymal transition in non-small cell lung cancer cells. Biochim Biophys Acta, Mol Cell Res. 2018;1865:749–768.
  • Hombach-Klonisch S, Mehrpour M, Shojaei S, et al. Glioblastoma and chemoresistance to alkylating agents: involvement of apoptosis, autophagy, and unfolded protein response. Pharmacol Ther. 2018;184:13–41.
  • Omatsu-Kanbe M, Yamamoto T, Matsuura H. Autophagy is constitutively active in normal mouse sino-atrial nodal cells. Acta Histochem Cytochem. 2011;44:223–231.
  • Klionsky DJ, Abdelmohsen K, Abe A, et al. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy. 2016;12:1–222.
  • Klionsky DJ, Abdalla FC, Abeliovich H, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy. 2012;8:445–544.
  • Deretic V, Kimura T, Timmins G, et al. Immunologic manifestations of autophagy. J Clin Invest. 2015;125:75–84.
  • Jiang P, Mizushima N. Autophagy and human diseases. Cell Res. 2014;24:69–79.
  • Jiang X, Overholtzer M, Thompson CB. Autophagy in cellular metabolism and cancer. J Clin Investig. 2015;125:47–54.
  • Kuballa P, Nolte WM, Castoreno AB, et al. Autophagy and the immune system. Annu Rev Immunol. 2012;30:611–646.
  • Nixon RA. The role of autophagy in neurodegenerative disease. Nat Med. 2013;19:983–997.
  • Alizadeh J, Shojaei S, Sepanjnia A, et al. Simultaneous detection of autophagy and epithelial to mesenchymal transition in the non-small cell lung cancer cells. Methods Mol Biol. 2019;1854:87–103.
  • Novikoff AB, Beaufay H, De Duve C. Electron microscopy of lysosomerich fractions from rat liver. J Biophys Biochem Cytol. 1956;2:179–184.
  • Kaur J, Debnath J. Autophagy at the crossroads of catabolism and anabolism. Nat Rev Mol Cell Biol. 2015;16:461–472.
  • Ghavami S, Yeganeh B, Stelmack GL, et al. Apoptosis, autophagy and ER stress in mevalonate cascade inhibition-induced cell death of human atrial fibroblasts. Cell Death Dis. 2012;3:e330.
  • Mizushima N, Komatsu M. Autophagy: renovation of cells and tissues. Cell. 2011;147:728–741.
  • Li WW, Li J, Bao JK. Microautophagy: lesser-known self-eating. Cell Mol Life Sci. 2012;69:1125–1136.
  • Cuervo AM, Wong E. Chaperone-mediated autophagy: roles in disease and aging. Cell Res. 2014;24:92–104.
  • Ghavami S, Shojaei S, Yeganeh B, et al. Autophagy and apoptosis dysfunction in neurodegenerative disorders. Prog Neurobiol. 2014;112:24–49.
  • Jin M, Liu X, Klionsky DJ. SnapShot: selective autophagy. Cell. 2013;152:368–368 e2.
  • Yeganeh B, Rezaei Moghadam A, Alizadeh J, et al. Hepatitis B and C virus-induced hepatitis: apoptosis, autophagy, and unfolded protein response. World J Gastroenterol. 2015;21:13225–13239.
  • Alavian SM, Ande SR, Coombs KM, et al. Virus-triggered autophagy in viral hepatitis - possible novel strategies for drug development. J Viral Hepat. 2011;18:821–830.
  • Singh A, Kendall SL, Campanella M. Common traits spark the mitophagy/xenophagy interplay. Front Physiol. 2018;9:1172.
  • Ktistakis NT, Tooze SA. Digesting the expanding mechanisms of autophagy. Trends Cell Biol. 2016;26:624–635.
  • Gallagher LE, Williamson LE, Chan EY. Advances in autophagy regulatory mechanisms. Cells. 2016;5:pii:E24.
  • Nakatogawa H, Suzuki K, Kamada Y, et al. Dynamics and diversity in autophagy mechanisms: lessons from yeast. Nat Rev Mol Cell Biol. 2009;10:458–467.
  • Yang Z, Klionsky DJ. An overview of the molecular mechanism of autophagy. Curr Top Microbiol Immunol. 2009;335:1–32.
  • Klionsky DJ, Cregg JM, Dunn WA Jr., et al. A unified nomenclature for yeast autophagy-related genes. Dev Cell. 2003;5:539–545.
  • Ragusa MJ, Stanley RE, Hurley JH. Architecture of the Atg17 complex as a scaffold for autophagosome biogenesis. Cell. 2012;151:1501–1512.
  • Diao J, Liu R, Rong Y, et al. ATG14 promotes membrane tethering and fusion of autophagosomes to endolysosomes. Nature. 2015;520:563–566.
  • Tooze SA, Yoshimori T. The origin of the autophagosomal membrane. Nat Cell Biol. 2010;12:831–835.
  • Huang R, Xu Y, Wan W, et al. Deacetylation of nuclear LC3 drives autophagy initiation under starvation. Mol Cell. 2015;57:456–466.
  • Bednarczyk M, Zmarzly N, Grabarek B, et al. Genes involved in the regulation of different types of autophagy and their participation in cancer pathogenesis. Oncotarget. 2018;9:34413–34428.
  • White E, Mehnert JM, Chan CS. Autophagy, Metabolism, and Cancer. Clin Cancer Res. 2015;21:5037–5046.
  • Kim J, Huang WP, Stromhaug PE, et al. Convergence of multiple autophagy and cytoplasm to vacuole targeting components to a perivacuolar membrane compartment prior to de novo vesicle formation. J Biol Chem. 2002;277:763–773.
  • Suzuki K, Kirisako T, Kamada Y, et al. The pre-autophagosomal structure organized by concerted functions of APG genes is essential for autophagosome formation. Embo J. 2001;20:5971–5981.
  • Hamasaki M, Furuta N, Matsuda A, et al. Autophagosomes form at ER-mitochondria contact sites. Nature. 2013;495:389–393.
  • Lamb CA, Yoshimori T, Tooze SA. The autophagosome: origins unknown, biogenesis complex. Nat Rev Mol Cell Biol. 2013;14:759–774.
  • Sica V, Galluzzi L, Bravo-San Pedro José M, et al. Organelle-specific initiation of autophagy. Mol Cell. 2015;59:522–539.
  • Park C, Cuervo AM. Selective autophagy: talking with the UPS. Cell Biochem Biophys. 2013;67:3–13.
  • Okamoto K. Organellophagy: eliminating cellular building blocks via selective autophagy. J Cell Biol. 2014;205:435–445.
  • Randow F, Youle RJ. Self and nonself: how autophagy targets mitochondria and bacteria. Cell Host Microbe. 2014;15:403–411.
  • Rogov V, Dotsch V, Johansen T, et al. Interactions between autophagy receptors and ubiquitin-like proteins form the molecular basis for selective autophagy. Mol Cell. 2014;53:167–178.
  • Wild P, McEwan DG, Dikic I. The LC3 interactome at a glance. J Cell Sci. 2014;127:3–9.
  • Hjerpe R, Bett John S, Keuss Matthew J, et al. UBQLN2 mediates autophagy-independent protein aggregate clearance by the proteasome. Cell. 2016;166:935–949.
  • Youle RJ, Narendra DP. Mechanisms of mitophagy. Nat Rev Mol Cell Biol. 2011;12:9–14.
  • Liu L, Feng D, Chen G, et al. Mitochondrial outer-membrane protein FUNDC1 mediates hypoxia-induced mitophagy in mammalian cells. Nat Cell Biol. 2012;14:177–185.
  • Novak I, Kirkin V, McEwan DG, et al. Nix is a selective autophagy receptor for mitochondrial clearance. EMBO Rep. 2010;11:45–51.
  • Sandoval H, Thiagarajan P, Dasgupta SK, et al. Essential role for Nix in autophagic maturation of erythroid cells. Nature. 2008;454:232–235.
  • Aoki Y, Kanki T, Hirota Y, et al. Phosphorylation of Serine 114 on Atg32 mediates mitophagy. Mol Biol Cell. 2011;22:3206–3217.
  • Loos B, Du Toit A, Hofmeyr J-HS. Defining and measuring autophagosome flux—concept and reality. Autophagy. 2014;10:2087–2096.
  • Green DR, Galluzzi L, Kroemer G. Mitochondria and the autophagy-inflammation-cell death axis in organismal aging. Science. 2011;333:1109–1112.
  • Mizushima N, Levine B, Cuervo AM, et al. Autophagy fights disease through cellular self-digestion. Nature. 2008;451:1069–1075.
  • McAlinden KD, Deshpande DA, Ghavami S, et al. Autophagy activation in asthma airways remodeling. Am J Respir Cell Mol Biol. 2018.
  • Kroemer G, Marino G, Levine B. Autophagy and the integrated stress response. Mol Cell. 2010;40:280–293.
  • Masiero E, Agatea L, Mammucari C, et al. Autophagy is required to maintain muscle mass. Cell Metab. 2009;10:507–515.
  • Ding WX, Ni HM, Gao W, et al. Differential effects of endoplasmic reticulum stress-induced autophagy on cell survival. J Biol Chem. 2007;282:4702–4710.
  • Levy JMM, Towers CG, Thorburn A. Targeting autophagy in cancer. Nat Rev Cancer. 2017;17:528–542.
  • Kaushik S, Bandyopadhyay U, Sridhar S, et al. Chaperone-mediated autophagy at a glance. J Cell Sci. 2011;124:495–499.
  • Yordy B, Iwasaki A. Autophagy in the control and pathogenesis of viral infection. Curr Opin Virol. 2011;1:196–203.
  • Deretic V, Saitoh T, Akira S. Autophagy in infection, inflammation and immunity. Nat Rev Immunol. 2013;13:722–737.
  • Romao S, Gannage M, Münz C. Checking the garbage bin for problems in the house, or how autophagy assists in antigen presentation to the immune system. Semin Cancer Biol. 2013;23:391–396.
  • Choi Y, Bowman JW, Jung JU. Autophagy during viral infection — a double-edged sword. Nature Rev Microbiol. 2018;16:341–354.
  • Loo Y-M, Fornek J, Crochet N, et al. Distinct RIG-I and MDA5 signaling by RNA viruses in innate immunity. J Virol. 2008;82:335–345.
  • Yang Q, Liu TT, Lin HC, et al. TRIM32-TAX1BP1-dependent selective autophagic degradation of TRIF negatively regulates TLR3/4-mediated innate immune responses. PLoS Pathog. 2017;13:e1006600.
  • Orvedahl A, MacPherson S, Sumpter RJ, et al. Autophagy protects against Sindbis virus infection of the central nervous system. Cell Host Microbe. 2010;7:115–127.
  • Gannagé M, Dormann D, Albrecht R, et al. Matrix protein 2 of influenza A virus blocks autophagosome fusion with lysosomes. Cell Host Microbe. 2009;6:367–380.
  • Zhirnov OP, Klenk HD. Influenza A virus proteins NS1 and hemagglutinin along with M2 are involved in stimulation of autophagy in infected cells. J Virol. 2013;87:13107–13114.
  • Kyei GB, Dinkins C, Davis AS, et al. Autophagy pathway intersects with HIV-1 biosynthesis and regulates viral yields in macrophages. J Cell Biol. 2009;186:255–268.
  • Samsa MM, Mondotte JA, Iglesias NG, et al. Dengue virus capsid protein usurps lipid droplets for viral particle formation. PLoS Pathog. 2009;5:e1000632.
  • Heaton NS, Randall G. Dengue virus-induced autophagy regulates lipid metabolism. Cell Host Microbe. 2010;8:422–432.
  • Metz P, Chiramel A, Chatel-Chaix L, et al. Dengue Virus inhibition of autophagic flux and dependency of viral replication on proteasomal degradation of the autophagy receptor p62. J Virol. 2015;89:8026.
  • Sovolyova N, Healy S, Samali A, et al. Stressed to death - mechanisms of ER stress-induced cell death. J Biol Chem. 2014; 395: 1–13.
  • Iranpour M, Moghadam AR, Yazdi M, et al. Apoptosis, autophagy and unfolded protein response pathways in Arbovirus replication and pathogenesis. Expert Rev Mol Med. 2016;18:e1.
  • Almanza A, Carlesso A, Chintha C, et al. Endoplasmic reticulum stress signalling - from basic mechanisms to clinical applications. FEBS J. 2019;286:241–278.
  • Hetz C, Chevet E, Harding HP. Targeting the unfolded protein response in disease. Nat Rev Drug Discov. 2013;12:703–719.
  • McGrath EP, Logue SE, Mnich K, et al. The unfolded protein response in breast cancer. Cancers (Basel). 2018;10:10.
  • Dejeans N, Barroso K, Fernandez-Zapico ME, et al. Novel roles of the unfolded protein response in the control of tumor development and aggressiveness. Seminars in Cancer Biology. 33 (2015) 67–73
  • Lhomond S, Avril T, Dejeans N, et al. Dual IRE1 RNase functions dictate glioblastoma development. EMBO Mol Med. 2018;10.
  • Sovolyova N, Healy S, Samali A, et al. Stressed to death - mechanisms of ER stress-induced cell death. J Biol Chem. 2014;395:1–13.
  • Ghavami S, Yeganeh B, Zeki AA, et al. Autophagy and the unfolded protein response promote profibrotic effects of TGF-beta1 in human lung fibroblasts. Am J Physiol Lung Cell Mol Physiol. 2018;314:L493–L504.
  • Hetz C. The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat Rev Mol Cell Biol. 2012;13:89–102.
  • Lin JH, Li H, Yasumura D, et al. IRE1 signaling affects cell fate during the unfolded protein response. Science. 2007;318:944–949.
  • Deegan S, Koryga I, Glynn SA, et al. A close connection between the PERK and IRE arms of the UPR and the transcriptional regulation of autophagy. Biochem Biophys Res Commun. 2015;456:305–311.
  • Yoshida H, Matsui T, Yamamoto A, et al. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell. 2001;107:881–891.
  • Novoa I, Zeng H, Harding HP, et al. Feedback inhibition of the unfolded protein response by GADD34-mediated dephosphorylation of eIF2alpha. J Cell Biol. 2001;153:1011–1022.
  • Cullinan SB, Zhang D, Hannink M, et al. Nrf2 is a direct PERK substrate and effector of PERK-dependent cell survival. Mol Cell Biol. 2003;23:7198–7209.
  • Verfaillie T, Rubio N, Garg AD, et al. PERK is required at the ER-mitochondrial contact sites to convey apoptosis after ROS-based ER stress. Cell Death Differ. 2012;19:1880–1891.
  • Lee Y-R, Lei H-Y, Liu M-T, et al. Autophagic machinery activated by dengue virus enhances virus replication. Virology. 2008;374:240–248.
  • Meng S, Jiang K, Zhang X, et al. Avian reovirus triggers autophagy in primary chicken fibroblast cells and Vero cells to promote virus production. Arch Virol. 2012;157:661–668.
  • Krejbich-Trotot P, Gay B, Li-Pat-Yuen G, et al. Chikungunya triggers an autophagic process which promotes viral replication. Virol J. 2011;8:432.
  • Shai B, Schmukler E, Yaniv R, et al. Epizootic hemorrhagic disease virus induces and benefits from cell stress, autophagy, and apoptosis. J Virol. 2013;87:13397–13408.
  • Chi PI, Huang WR, Lai IH, et al. The p17 nonstructural protein of avian reovirus triggers autophagy enhancing virus replication via activation of phosphatase and tensin deleted on chromosome 10 (PTEN) and AMP-activated protein kinase (AMPK), as well as dsRNA-dependent protein kinase (PKR)/eIF2α signaling pathways. J Biol Chem. 2013;288:3571–3584.
  • American Mosquito Control Association, Den Boon JA, Ahlquist P. Organelle-like membrane compartmentalization of positive-strand RNA virus replication factories. Annu Rev Microbiol. 2010;64:241–256.
  • Panyasrivanit M, Khakpoor A, Wikan N, et al. Co-localization of constituents of the dengue virus translation and replication machinery with amphisomes. J Gen Virol. 2009;90:448–456.
  • Sharma M, Bhattacharyya S, Nain M, et al. Japanese encephalitis virus replication is negatively regulated by autophagy and occurs on LC3-I- and EDEM1-containing membranes. Autophagy. 2014;10:1637–1651.
  • Heaton NS, Randall G. Dengue virus and autophagy. Viruses. 2011;3:1332–1341.
  • Blázquez AB, Escribano-Romero E, Merino-Ramos T, et al. Stress responses in flavivirus-infected cells: activation of unfolded protein response and autophagy. Front Microbiol. 2014;5.
  • Panyasrivanit M, Greenwood MP, Murphy D, et al. Induced autophagy reduces virus output in dengue infected monocytic cells. Virology. 2011;418:74–84.
  • Vandergaast R, Fredericksen BL. West Nile Virus (WNV) replication is independent of autophagy in mammalian cells. PLoS ONE. 2012;7:e45800.
  • Beatman E, Oyer R, Shives KD, et al. West Nile Virus growth is independent of autophagy activation. Virology. 2012;433:262–272.
  • Kobayashi S, Orba Y, Yamaguchi H, et al. Autophagy inhibits viral genome replication and gene expression stages in West Nile virus infection. Virus Res. 2014;191:83–91.
  • Blázquez AB, Martín-Acebes MA, Saiz J-C. Amino acid substitutions in the non-structural proteins 4A or 4B modulate the induction of autophagy in West Nile virus infected cells independently of the activation of the unfolded protein response. Front Microbiol. 2015;5.
  • Sharma M, Bhattacharyya S, Sharma KB, et al. Japanese encephalitis virus activates autophagy through XBP1 and ATF6 ER stress sensors in neuronal cells. J Gen Virol. 2017;98:1027–1039.
  • Lee Y-R, Hu H-Y, Kuo S-H, et al. Dengue virus infection induces autophagy: an in vivo study. J Biomed Sci. 2013;20:65.
  • Jackson WT, Giddings TH Jr, Taylor MP, et al. Subversion of cellular autophagosomal machinery by RNA viruses. PLoS Biol. 2005;3:e156.
  • Panyasrivanit M, Khakpoor A, Wikan N, et al. Linking dengue virus entry and translation/replication through amphisomes. Autophagy. 2009;5:434–435.
  • Jin R, Zhu W, Cao S, et al. Japanese Encephalitis Virus Activates Autophagy as a Viral Immune Evasion Strategy. PLoS ONE. 2013;8:e52909.
  • Miller S, Kastner S, Krijnse-Locker J, et al. The non-structural protein 4A of dengue virus is an integral membrane protein inducing membrane alterations in a 2K-regulated manner. J Biol Chem. 2007;282:8873–8882.
  • McLean JE, Wudzinska A, Datan E, et al. Flavivirus NS4A-induced autophagy protects cells against death and enhances virus replication. J Biol Chem. 2011;286:22147–22159.
  • Joubert P-E, Werneke SW, de la Calle C, et al. Chikungunya virus–induced autophagy delays caspase-dependent cell death. J Exp Med. 2012;209:1029–1047.
  • Avila-Bonilla RG, Yocupicio-Monroy M, Marchat LA, et al. Analysis of the miRNA profile in C6/36 cells persistently infected with dengue virus type 2. Virus Res. 2017;232:139–151.
  • Hou F, Sun L, Zheng H, et al. MAVS forms functional prion-like aggregates to activate and propagate antiviral innate immune response. Cell. 2011;146:448–461.
  • Jounai N, Takeshita F, Kobiyama K, et al. The Atg5–atg12 conjugate associates with innate antiviral immune responses. Proceedings of the National Academy of Sciences. 104 (2007) 14050–14055
  • Hamel R, Dejarnac O, Wichit S, et al. Biology of Zika Virus infection in human skin cells. J Virol. 2015;89:8880–8896.
  • Cugola FR, Fernandes IR, Russo FB, et al. The Brazilian Zika virus strain causes birth defects in experimental models. Nature. 2016;534:267.
  • Brackney DE. Implications of autophagy on arbovirus infection of mosquitoes. Curr Opin Insect Sci. 2017;22:1–6.
  • Liu Y, Gordesky-Gold B, Leney-Greene M, et al. Inflammation-induced, STING-dependent autophagy restricts zika virus infection in the drosophila brain. Cell Host Microbe. 2018;24:57–68.e3.
  • Hirano M, Yoshii K, Sakai M, et al. Tick-borne flaviviruses alter membrane structure and replicate in dendrites of primary mouse neuronal cultures. J Gen Virol. 2014;95:849–861.
  • Bílý T, Palus M, Eyer L, et al. Electron tomography analysis of Tick-Borne Encephalitis Virus infection in human neurons. Sci Rep. 2015;5:10745.
  • Lewis J, Wesselingh SL, Griffin DE, et al. Alphavirus-induced apoptosis in mouse brains correlates with neurovirulence. J Virol. 1996;70:1828–1835.
  • Samuel MA, Morrey JD, Diamond MS. Caspase 3-dependent cell death of neurons contributes to the pathogenesis of West Nile virus encephalitis. J Virol. 2007;81:2614–2623.
  • Sun J, Yu Y, Deubel V. Japanese encephalitis virus NS1′ protein depends on pseudoknot secondary structure and is cleaved by caspase during virus infection and cell apoptosis. Microbes Infect. 2012;14:930–940.
  • Stollar V, Shenk TE, Stollar BD. Double-stranded RNA in hamster, chick, and mosquito cells infected with Sindbis virus. Virology. 1972;47:122–132.
  • Stollar BD, Stollar V. Immunofluorescent demonstration of double-stranded RNA in the cytoplasm of Sindbis virus-infected cells. Virology. 1970;42:276–280.
  • Domingo-Gil E, Toribio R, Nájera JL, et al. Diversity in viral anti-PKR mechanisms: a remarkable case of evolutionary convergence. PLoS ONE. 2011;6:e16711.
  • Akgul C. Mcl-1 is a potential therapeutic target in multiple types of cancer. Cell Mol Life Sci. 2009;66:1326–1336.
  • Venticinque L, Meruelo D. Sindbis viral vector induced apoptosis requires translational inhibition and signaling through Mcl-1 and Bak. Mol Cancer. 2010;9:37.
  • Krejbich-Trotot P, Denizot M, Hoarau -J-J-J, et al. Chikungunya virus mobilizes the apoptotic machinery to invade host cell defenses. FASEB J. 2011;25:314–325.
  • Rodrigues R, Paranhos-Baccalà G, Vernet G, et al. Crimean-Congo hemorrhagic fever virus-infected hepatocytes induce ER-stress and apoptosis crosstalk. PLoS ONE. 2012;7:e29712.
  • Medin CL, Rothman AL. Cell type–specific mechanisms of interleukin-8 induction by dengue virus and differential response to drug treatment. J Infect Dis. 2006;193:1070–1077.
  • Li A, Dubey S, Varney ML, et al. IL-8 directly enhanced endothelial cell survival, proliferation, and matrix metalloproteinases production and regulated angiogenesis. J Immunol. 2003;170:3369–3376.
  • Lee C-J, Liao C-L, Lin Y-L. Flavivirus activates phosphatidylinositol 3-kinase signaling to block caspase-dependent apoptotic cell death at the early stage of virus infection. J Virol. 2005;79:8388–8399.
  • van Marle G, Antony J, Ostermann H, et al. West Nile virus-induced neuroinflammation: glial infection and capsid protein-mediated neurovirulence. J Virol. 2007;81:10933–10949.
  • Jan J-T, Griffin DE. Induction of apoptosis by Sindbis virus occurs at cell entry and does not require virus replication. J Virol. 1999;73:10296–10302.
  • Abraham R, Singh S, Nair SR, et al. Nucleophosmin (NPM1)/B23 in the proteome of human astrocytic cells restricts chikungunya virus replication. J Proteome Res. 2017;16:4144–4155.
  • Chiam CW, Chan YF, Ong KC, et al. Neurovirulence comparison of Chikungunya virus isolates of the Asian and East/Central/South African genotypes from Malaysia. J Gen Virol. 2015;96:3243–3254.
  • Urbanowski MD, Hobman TC. The West Nile virus capsid protein blocks apoptosis through a phosphatidylinositol 3-kinase-dependent mechanism. J Virol. 2013;87:872–881.
  • Del Carmen Parquet M, Kumatori A, Hasebe F, et al. West Nile virus-induced bax-dependent apoptosis. FEBS Lett. 2001;500:17–24.
  • Fujikura D, Ito M, Chiba S, et al. CLIPR-59 regulates TNF-α-induced apoptosis by controlling ubiquitination of RIP1. Cell Death Dis. 2012;3:e264.
  • Chu J, Ng M. The mechanism of cell death during West Nile virus infection is dependent on initial infectious dose. J Gen Virol. 2003;84:3305–3314.
  • Yang MR, Lee SR, Oh W, et al. West Nile virus capsid protein induces p53‐mediated apoptosis via the sequestration of HDM2 to the nucleolus. Cell Microbiol. 2008;10:165–176.
  • Medigeshi GR, Lancaster AM, Hirsch AJ, et al. West Nile virus infection activates the unfolded protein response, leading to CHOP induction and apoptosis. J Virol. 2007;81:10849–10860.
  • Smith JL, Grey FE, Uhrlaub JL, et al. Induction of the cellular microRNA, Hs_154, by West Nile virus contributes to virus-mediated apoptosis through repression of antiapoptotic factors. J Virol. 2012;86:5278–5287.
  • Yang T-C, Lai -C-C, Shiu S-L, et al. Japanese encephalitis virus down-regulates thioredoxin and induces ROS-mediated ASK1-ERK/p38 MAPK activation in human promonocyte cells. Microbes Infect. 2010;12:643–651.
  • Lin R-J, Liao C-L, Lin Y-L. Replication-incompetent virions of Japanese encephalitis virus trigger neuronal cell death by oxidative stress in a culture system. J Gen Virol. 2004;85:521–533.
  • Melian EB, Hinzman E, Nagasaki T, et al. NS1′ of flaviviruses in the Japanese encephalitis virus serogroup is a product of ribosomal frameshifting and plays a role in viral neuroinvasiveness. J Virol. 2010;84:1641–1647.
  • Liao C-L, Lin Y-L, Shen S-C, et al. Antiapoptotic but not antiviral function of Human bcl-2 assists establishment of Japanese encephalitis virus persistence in cultured cells. J Virol. 1998;72:9844–9854.
  • Al-Obaidi MMJ, Bahadoran A, Har LS, et al. Japanese encephalitis virus disrupts blood-brain barrier and modulates apoptosis proteins in THBMEC cells. Virus Res. 2017;233:17–28.
  • Myint KSA, Kipar A, Jarman RG, et al. Neuropathogenesis of Japanese Encephalitis in a primate model. PLoS Negl Trop Dis. 2014;8:e2980.
  • Silveira GF, Meyer F, Delfraro A, et al. Dengue virus type 3 isolated from a fatal case with visceral complications induces enhanced proinflammatory responses and apoptosis of human dendritic cells. J Virol. 2011;85:5374–5383.
  • Palmer DR, Sun P, Celluzzi C, et al. Differential effects of dengue virus on infected and bystander dendritic cells. J Virol. 2005;79:2432–2439.
  • Nasirudeen A, Liu DX. Gene expression profiling by microarray analysis reveals an important role for caspase‐1 in dengue virus‐induced p53‐mediated apoptosis. J Med Virol. 2009;81:1069–1081.
  • Austin D, Baer A, Lundberg L, et al. p53 activation following rift valley fever virus infection contributes to cell death and viral production. PLoS ONE. 2012;7:e36327.
  • Won S, Ikegami T, Peters C, et al. NSm protein of rift valley fever virus suppresses virus-induced apoptosis. J Virol. 2007;81:13335–13345.
  • Ikegami T, Narayanan K, Won S, et al. Rift valley fever virus NSs protein promotes post-transcriptional downregulation of protein kinase PKR and inhibits eIF2α phosphorylation. PLoS Pathog. 2009;5:e1000287.
  • Kohl A, Clayton RF, Weber F, et al. Bunyamwera virus nonstructural protein NSs counteracts interferon regulatory factor 3-mediated induction of early cell death. J Virol. 2003;77:7999–8008.
  • Mortola E, Noad R, Roy P. Bluetongue virus outer capsid proteins are sufficient to trigger apoptosis in mammalian cells. J Virol. 2004;78:2875–2883.
  • Stassen L, Huismans H, Theron J. African horse sickness virus induces apoptosis in cultured mammalian cells. Virus Res. 2012;163:385–389.
  • Sakinah S, Priya SP, Kumari S, et al. Impact of dengue virus (serotype DENV-2) infection on liver of BALB/c mice: A histopathological analysis. Tissue Cell. 2017;49:86–94.
  • Carter JR, Taylor S, Fraser TS, et al. Suppression of the arboviruses Dengue and Chikungunya using a dual-acting group-I intron coupled with conditional expression of the Bax C-terminal domain. PLoS ONE. 2015;10:e0139899.
  • Yen PS, James A, Li JC, et al. Synthetic miRNAs induce dual arboviral-resistance phenotypes in the vector mosquito Aedes aegypti. Commun Biol. 2018;1:11.
  • Frumence E, Roche M, Krejbich-Trotot P, et al. The south pacific epidemic strain of Zika virus replicates efficiently in human epithelial A549 cells leading to IFN-β production and apoptosis induction. Virology. 2016;493:217–226.
  • Dang J, Tiwari SK, Lichinchi G, et al. Zika virus depletes neural progenitors in human cerebral organoids through activation of the innate immune receptor TLR3. Cell Stem Cell. 2016;19:258–265.
  • Bos S, Viranaicken W, Turpin J, et al. The structural proteins of epidemic and historical strains of Zika virus differ in their ability to initiate viral infection in human host cells. Virology. 2018;516:265–273.
  • Rivarola ME, de Olmos S, Albrieu-Llinás G, et al. Neuronal degeneration in mice induced by an epidemic strain of Saint Louis encephalitis virus isolated in Argentina. Front Microbiol. 2018;9.
  • Wang H, Gort T, Boyle DL, et al. Effects of manipulating apoptosis on Sindbis Virus infection of Aedes aegypti mosquitoes. J Virol. 2012;86:6546–6554.
  • O’Neill K, Olson BJ, Huang N, et al. Rapid selection against arbovirus-induced apoptosis during infection of a mosquito vector. Proceedings of the National Academy of Sciences of the United States of America. 112 (2015) E1152–E1161
  • Feng L, Liu H, Li X, et al. Identification of AaCASPS7, an effector caspase in Aedes albopictus. Gene. 2016;593:117–125.
  • Clem RJ. Arboviruses and apoptosis: the role of cell death in determining vector competence. J Gen Virol. 2016;97:1033–1036.
  • Troupin A, Londono-Renteria B, Conway MJ, et al. A novel mosquito ubiquitin targets viral envelope protein for degradation and reduces virion production during dengue virus infection. Biochim Biophys Acta, Mol Cell Res. (2016);1860:1898–1909.
  • Ambrose RL, Mackenzie JM. West Nile virus differentially modulates the unfolded protein response to facilitate replication and immune evasion. J Virol. 2011;85:2723–2732.
  • Ambrose RL, Mackenzie JM. ATF6 signaling is required for efficient West Nile virus replication by promoting cell survival and inhibition of innate immune responses. J Virol. 2013;87:2206–2214.
  • Rathore AP, Ng ML, Vasudevan SG. Differential unfolded protein response during Chikungunya and Sindbis virus infection: CHIKV nsP4 suppresses eIF2alpha phosphorylation. Virol J. 2013;10:36.
  • Yu CY, Hsu YW, Liao CL, et al. Flavivirus infection activates the XBP1 pathway of the unfolded protein response to cope with endoplasmic reticulum stress. J Virol. 2006;80:11868–11880.
  • Sayce AC, Alonzi DS, Killingbeck SS, et al. Iminosugars inhibit dengue virus production via inhibition of ER alpha-glucosidases-Not glycolipid processing enzymes. PLoS Negl Trop Dis. 2016;10:e0004524–e0004524.
  • Whitby K, Pierson TC, Geiss B, et al. Castanospermine, a potent inhibitor of dengue virus infection in vitro and in vivo. J Virol. 2005;79:8698–8706.
  • Umareddy I, Pluquet O, Wang QY, et al. Dengue virus serotype infection specifies the activation of the unfolded protein response. Virol J. 2007;4:91.
  • Albornoz A, Carletti T, Corazza G, et al. The stress granule component TIA-1 binds tick-borne encephalitis virus RNA and is recruited to perinuclear sites of viral replication to inhibit viral translation. J Virol. 2014;88:6611–6622.
  • Yu CY, Achazi K, Niedrig M. Tick-borne encephalitis virus triggers inositol-requiring enzyme 1 (IRE1) and transcription factor 6 (ATF6) pathways of unfolded protein response. Virus Res. 2013;178:471–477.
  • Baer A, Lundberg L, Swales D, et al. Venezuelan Equine Encephalitis Virus induces apoptosis through the unfolded protein response activation of EGR1. J Virol. 2016;90:3558–3572.
  • Zhou Z, Jiang X, Liu D, et al. Autophagy is involved in influenza A virus replication. Autophagy. 2009;5:321–328.
  • Yeganeh B, Ghavami S, Kroeker AL, et al. Suppression of influenza a virus replication in human lung epithelial cells by noncytotoxic concentrations bafilomycin A1. Am J Physiol Gastrointest Liver Physiol. 2015;308:L270–L286.
  • Law AH-Y, Lee DC-W, Yuen K-Y, et al. Cellular response to influenza virus infection: a potential role for autophagy in CXCL10 and interferon-alpha induction. Cell Mol Immunol. 2010;7:263–270.
  • Pattingre S, Tassa A, Qu X, et al. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell. 2005;122:927–939.
  • Ghavami S, Mutawe MM, Hauff K, et al. Statin-triggered cell death in primary human lung mesenchymal cells involves p53-PUMA and release of Smac and Omi but not cytochrome c. Biochim Biophys Acta, Mol Cell Res. 2010;1803:452–467.
  • Codogno P, Meijer AJ. Autophagy and signaling: their role in cell survival and cell death. Cell Death Differ. 2005;12:1509–1518.
  • Cheng J, Ohsaki Y, Tauchi-Sato K, et al. Cholesterol depletion induces autophagy. Biochem Biophys Res Commun. 2006;351:246–252.
  • Sumpter R, Levine B. Autophagy and innate immunity: triggering, targeting and tuning. In: Seminars in cell & developmental biology. Elsevier; 2010;21: 699–711.
  • Rossman JS, Lamb RA. Autophagy, apoptosis, and the influenza virus M2 protein. Cell Host Microbe. 2009;6:367–380.
  • Schmid D. Autophagy delivers viral antigens for MHC class II presentation and is regulated by viral infection. The Rockefeller University; 2007. p. 205.
  • Ochiai H, Sakai S, Hirabayashi T, et al. Inhibitory effect of bafilomycin A1, a specific inhibitor of vacuolar-type proton pump, on the growth of influenza A and B viruses in MDCK cells. Antiviral Res. 1995;27:425–430.
  • Mehrbod P, Hair-Bejo M, Ibrahim TAT, et al. Simvastatin modulates cellular components in influenza A virus-infected cells. Int J Mol Med. 2014;34:61–73.
  • Comber JD, Robinson TM, Siciliano NA, et al. Functional macroautophagy induction by influenza A virus without a contribution to major histocompatibility complex class II-restricted presentation. J Virol. 2011;85:6453–6463.
  • Zhu H-Y, Han L, Shi X-L, et al. Baicalin inhibits autophagy induced by influenza A virus H3N2. Antiviral Res. 2015;113:62–70.
  • Hale BG, Jackson D, Chen YH, et al. Influenza A virus NS1 protein binds p85β and activates phosphatidylinositol-3-kinase signaling. Proceedings of the National Academy of Sciences. 103 (2006) 14194–14199
  • Ren Y, Li C, Feng L, et al. Proton channel activity of influenza A virus matrix protein 2 contributes to autophagy arrest. J Virol. 2016;90:591–598.
  • Fletcher K, Ulferts R, Jacquin E, et al. The WD40 domain of ATG16L1 is required for its non‐canonical role in lipidation of LC3 at single membranes. Embo J. 2018;37:e97840.
  • Su WC, Yu WY, Huang SH, et al. Ubiquitination of the cytoplasmic domain of influenza A virus M2 protein is crucial for production of infectious virus particles. J Virol. 2018;92:e01972–17.
  • Egan DF, Kim J, Shaw RJ, et al. The autophagy initiating kinase ULK1 is regulated via opposing phosphorylation by AMPK and mTOR. Autophagy. 2011;7:645–646.
  • Liu G, Zhong M, Guo C, et al. Autophagy is involved in regulating influenza A virus RNA and protein synthesis associated with both modulation of Hsp90 induction and mTOR/p70S6K signaling pathway. Int J Biochem Cell Biol. 2016;72:100–108.
  • Klionsky DJ, Emr SD. Autophagy as a regulated pathway of cellular degradation. Science. 2000;290:1717–1721.
  • Ma J, Sun Q, Mi R, et al. Avian influenza A virus H5N1 causes autophagy-mediated cell death through suppression of mTOR signaling. J Genet Genome. 2011;38:533–537.
  • Sun Y, Li C, Shu Y, et al. Inhibition of autophagy ameliorates acute lung injury caused by avian influenza A H5N1 infection. Sci Signal. 2012;5:1r16.
  • Ehrhardt C, Marjuki H, Wolff T, et al. Bivalent role of the phosphatidylinositol-3-kinase (PI3K) during influenza virus infection and host cell defence. Cell Microbiol. 2006;8:1336–1348.
  • Datan E, Shirazian A, Benjamin S, et al. mTOR/p70S6K signaling distinguishes routine, maintenance-level autophagy from autophagic cell death during influenza A infection. Virology. 2014;452–453:175–190.
  • Puleston DJ, Zhang H, Powell TJ, et al. Autophagy is a critical regulator of memory CD8(+) T cell formation. eLife. 2014;3:e03706.
  • Lu Q, Yokoyama CC, Williams JW, et al. Homeostatic control of innate lung inflammation by Vici Syndrome Gene Epg5 and additional autophagy genes promotes influenza pathogenesis. Cell Host Microbe. 2016;19:102–113.
  • Zhao H, Zhao YG, Wang X, et al. Mice deficient in EPG5 exhibit selective neuronal vulnerability to degeneration. J Cell Biol. 2013;200:731.
  • Perot BP, Boussier J, Yatim N, et al. Autophagy diminishes the early interferon-β response to influenza A virus resulting in differential expression of interferon-stimulated genes. Cell Death Dis. 2018;9:539.
  • Jung KL, Pyo CW, Choi SY. Influenza A virus-induced autophagy contributes to enhancement of virus infectivity by SOD1 downregulation in alveolar epithelial cells. Biochem Biophys Res Commun. 2018;498:960–966.
  • Nakahira K, Haspel JA, Rathinam VAK, et al. Autophagy proteins regulate innate immune response by inhibiting NALP3 inflammasome-mediated mitochondrial DNA release. Nat Immunol. 2011;12:222–230.
  • Lupfer C, Thomas PG, Anand PK, et al. Receptor interacting protein kinase 2-mediated mitophagy regulates inflammasome activation during virus infection. Nat Immunol. 2013;14:480–488.
  • Feizi N, Mehrbod P, Romani B, et al. Autophagy induction regulates influenza virus replication in a time-dependent manner. J Med Microbiol. 2017;66:536–541.
  • Sparrer KMJ, Gableske S, Zurenski MA, et al. TRIM23 mediates virus-induced autophagy via activation of TBK1. Nat Microbiol. 2017;2:1543–1557.
  • Moon HJ, Nikapitiya C, Lee H-C, et al. Inhibition of highly pathogenic avian influenza (HPAI) virus by a peptide derived from vFLIP through its direct destabilization of viruses. Sci Rep. 2017;7:4875.
  • Georgi A, Mottola-Hartshorn C, Warner A, et al. Detection of individual fluorescently labeled reovirions in living cells. Proc Nat Acad Sci. 1990;87:6579.
  • Wu QM, Liu SL, Chen G, et al. Uncovering the Rab5-independent autophagic trafficking of influenza A virus by quantum-dot-based single-virus tracking. Small. 2018;14:e1702841.
  • Mori I, Komatsu T, Takeuchi K, et al. In vivo induction of apoptosis by influenza virus. J Gen Virol. 1995;76:2869–2873.
  • Yang N, Hong X, Yang P, et al. The 2009 pandemic A/Wenshan/01/2009 H1N1 induces apoptotic cell death in human airway epithelial cells. J Mol Cell Biol. 2011;3:221–229.
  • Tran AT, Cortens JP, Du Q, et al. Influenza virus induces apoptosis via BAD-mediated mitochondrial dysregulation. J Virol. 2013;87:1049–1060.
  • Yeganeh B, Ghavami S, Rahim MN, et al. Autophagy activation is required for influenza A virus-induced apoptosis and replication. Biochim Biophys Acta, Mol Cell Res. 2018;1865:364–378.
  • McLean JE, Datan E, Matassov D, et al. Lack of Bax prevents influenza A virus-induced apoptosis and causes diminished viral replication. J Virol. 2009;83:8233–8246.
  • Hinshaw VS, Olsen CW, Dybdahl-Sissoko N, et al. Apoptosis: a mechanism of cell killing by influenza A and B viruses. J Virol. 1994;68:3667–3673.
  • Olsen CW, Kehren JC, Dybdahl-Sissoko NR, et al. bcl-2 alters influenza virus yield, spread, and hemagglutinin glycosylation. J Virol. 1996;70:663–666.
  • Guan Z, Shi N, Song Y, et al. Induction of the cellular microRNA-29c by influenza virus contributes to virus-mediated apoptosis through repression of antiapoptotic factors BCL2L2. Biochem Biophys Res Commun. 2012;425:662–667.
  • Ludwig S, Wang X, Ehrhardt C, et al. The influenza A virus NS1 protein inhibits activation of Jun N-Terminal Kinase and AP-1 transcription factors. J Virol. 2002;76:11166–11171.
  • Lu X, Masic A, Li Y, et al. The PI3K/Akt pathway inhibits influenza A virus-induced Bax-mediated apoptosis by negatively regulating the JNK pathway via ASK1. J Gen Virol. 2010;91:1439–1449.
  • Chung M, Cho SY, Lee YS. Construction of a transcriptome-driven network at the early stage of infection with influenza A H1N1 in human lung alveolar epithelial cells. Biomol Ther (Seoul). 2018;26:290–297.
  • Elbim C, Katsikis PD, Estaquier J. Neutrophil apoptosis during viral infections. Open Virol J. 2009;3:52–59.
  • Mao H, Liu Y, Sia SF, et al. Avian influenza virus directly infects human natural killer cells and inhibits cell activity. Virol Sin. 2017;32:122–129.
  • Stasakova J, Ferko B, Kittel C, et al. Influenza A mutant viruses with altered NS1 protein function provoke caspase-1 activation in primary human macrophages, resulting in fast apoptosis and release of high levels of interleukins 1β and 18. J Gen Virol. 2005;86:185–195.
  • Jordan A, Hadfield JA, Lawrence NJ, et al. Tubulin as a target for anticancer drugs: agents which interact with the mitotic spindle. Med Res Rev. 1998;18:259–296.
  • Han X, Li Z, Chen H, et al. Influenza virus A/Beijing/501/2009(H1N1) NS1 interacts with β-tubulin and induces disruption of the microtubule network and apoptosis on A549 cells. PLoS ONE. 2012;7:e48340.
  • Yang P, Deng J, Li C, et al. Characterization of the 2009 pandemic A/Beijing/501/2009 H1N1 influenza strain in human airway epithelial cells and ferrets. PLoS ONE. 2012;7:e46184.
  • Zhang C, Yang Y, Zhou X, et al. Highly pathogenic avian influenza A virus H5N1 NS1 protein induces caspase-dependent apoptosis in human alveolar basal epithelial cells. Virol J. 2010;7:51.
  • Pauli EK, Schmolke M, Wolff T, et al. Influenza A virus inhibits type I IFN signaling via NF-kappaB-dependent induction of SOCS-3 expression. PLoS Pathog. 2008;4:e1000196.
  • Shiozaki T, Iwai A, Kawaoka Y, et al. Requirement for Siva-1 for replication of influenza A virus through apoptosis induction. J Gen Virol. 2011;92:315–325.
  • Tripathi S, Batra J, Cao W, et al. Influenza A virus nucleoprotein induces apoptosis in human airway epithelial cells: implications of a novel interaction between nucleoprotein and host protein Clusterin. Cell Death Dis. 2013;4:e562.
  • Husain M, Harrod KS. Influenza A virus-induced caspase-3 cleaves the histone deacetylase 6 in infected epithelial cells. FEBS Lett. 2009;583:2517–2520.
  • Tinoco R, Carrette F, Henriquez ML, et al. Fucosyltransferase induction during influenza virus infection is required for the generation of functional memory CD4+T Cells. J Immunol. 2018;200:2690–2702.
  • Chida J, Hara H, Yano M, et al. Prion protein protects mice from lethal infection with influenza A viruses. PLoS Pathog. 2018;14:e1007049.
  • Yang W, Qu S, Liu Q, et al. Avian influenza virus A/chicken/Hubei/489/2004 (H5N1) induces caspase-dependent apoptosis in a cell-specific manner. Mol Cell Biochem. 2009;332:233–241.
  • Ekchariyawat P, Thitithanyanont A, Sirisinha S, et al. Apoptosis induced by avian H5N1 virus in human monocyte-derived macrophages involves TRAIL-inducing caspase-10 activation. Innate Immun. 2012;18:390–397.
  • Gao H, Sun Y, Hu J, et al. The contribution of PA-X to the virulence of pandemic 2009 H1N1 and highly pathogenic H5N1 avian influenza viruses. Sci Rep. 2015;5:8262.
  • Gao Z, Hu J, Wang X, et al. The PA-interacting host protein nucleolin acts as an antiviral factor during highly pathogenic H5N1 avian influenza virus infection. Arch Virol. 2018;163:2775–2786..
  • Stawowczyk M, Van Scoy S, Kumar KP, et al. The interferon stimulated gene 54 promotes apoptosis. J Biol Chem. 2011;286:7257–7266.
  • Rong E, Hu J, Yang C, et al. Broad-spectrum antiviral functions of duck interferon-induced protein with tetratricopeptide repeats (AvIFIT). Dev Comp Immunol. 2018;84:71–81.
  • Wein AN, Dunbar PR, McMaster SR, et al. IL-36γ protects against severe influenza infection by promoting lung alveolar macrophage survival and limiting viral replication. J Immunol. 2018;201:573–582.
  • Lee S, Hirohama M, Noguchi M, et al. Influenza A virus infection triggers pyroptosis and apoptosis of respiratory epithelial cells through type I IFN signaling pathway in a mutually exclusive manner. J Virol. 2018;92:e00396–18.
  • Keshtkar-Jahromi M, Ouyang M, Keshtkarjahromi M, et al. Effect of influenza vaccine on tumor necrosis factor-like Weak inducer of apoptosis (TWEAK) in older population. Vaccine. 2016;36:2220–2225.
  • Mata M, Morcillo E, Gimeno C, et al. N-acetyl-l-cysteine (NAC) inhibit mucin synthesis and pro-inflammatory mediators in alveolar type II epithelial cells infected with influenza virus A and B and with respiratory syncytial virus (RSV). Biochem Pharmacol. 2011;82:548–555.
  • Ma LL, Sun ZH, Xu YL, et al. Screening host proteins required for bacterial adherence after H9N2 virus infection. Vet Microbiol. 2018;213:5–14.
  • Coombs KM, Berard A, Xu W, et al. Quantitative proteomic analyses of influenza virus-infected cultured human lung cells. J Virol. 2010;84:10888–10906.
  • Simon PF, de La Vega MA, Paradis E, et al. Avian influenza viruses that cause highly virulent infections in humans exhibit distinct replicative properties in contrast to human H1N1 viruses. Sci Rep. 2016;6:24154.
  • Ranadheera C, Coombs KM, Kobasa D. Comprehending a killer: the Akt/mTOR signaling pathways are temporally high-jacked by the highly pathogenic 1918 influenza virus. EBioMedicine. 2018;32:142–163.
  • Kroeker AL, Ezzati P, Halayko AJ, et al. Response of primary human airway epithelial cells to influenza infection: a quantitative proteomic study. J Proteome Res. 2012;11:4132–4146.
  • Kroeker AL, Ezzati P, Coombs KM, et al. Influenza A infection of primary human airway epithelial cells up-regulates proteins related to purine metabolism and ubiquitin-related signaling. J Proteome Res. 2013;12:3139–3151.
  • Nailwal H, Sharma S, Mayank AK, et al. The nucleoprotein of influenza A virus induces p53 signaling and apoptosis via attenuation of host ubiquitin ligase RNF43. Cell Death Dis. 2015;6:e1768.
  • Li Y, Lin Z, Guo M, et al. Inhibition of H1N1 influenza virus-induced apoptosis by functionalized selenium nanoparticles with amantadine through ROS-mediated AKT signaling pathways. Int J Nanomedicine. 2018;13:2005–2016.
  • Hassan IH, Zhang MS, Powers LS, et al. Influenza A viral replication is blocked by inhibition of the inositol-requiring enzyme 1 (IRE1) stress pathway. J Biol Chem. 2012;287:4679–4689.
  • Numajiri Haruki A, Naito T, Nishie T, et al. Interferon-inducible antiviral protein MxA enhances cell death triggered by endoplasmic reticulum stress. J Interferon Cytokine Res. 2011;31:847–856.
  • Roberson EC, Tully JE, Guala AS, et al. Influenza induces endoplasmic reticulum stress, caspase-12-dependent apoptosis, and c-Jun N-terminal kinase-mediated transforming growth factor-β release in lung epithelial cells. Am J Respir Cell Mol Biol. 2012;46:573–581.
  • Yan W, Frank CL, Korth MJ, et al. Control of PERK eIF2α kinase activity by the endoplasmic reticulum stress-induced molecular chaperone P58IPK. Proceedings of the National Academy of Sciences. 99 (2002) 15920–15925
  • Goodman AG, Smith JA, Balachandran S, et al. The cellular protein P58IPK regulates influenza virus mRNA translation and replication through a PKR-mediated mechanism. J Virol. 2007;81:2221–2230.
  • Frabutt DA, Wang B, Riaz S, et al. Innate sensing of influenza A virus hemagglutinin glycoproteins by the host endoplasmic reticulum (ER) stress pathway triggers a potent antiviral response via ER-associated protein degradation. J Virol. 2018;92): e01690:-17.
  • Nardacci R, Ciccosanti F, Marsella C, et al. Role of autophagy in HIV infection and pathogenesis. J Intern Med. 2017;281:422–432.
  • Jackson WT. Viruses and the autophagy pathway. Virology. 2015;479–480:450–456.
  • Badley AD, Pilon AA, Landay A, et al. Mechanisms of HIV-associated lymphocyte apoptosis. Blood. 2000;96:2951–2964.
  • Ahr B, Robert-Hebmann V, Devaux C, et al. Apoptosis of uninfected cells induced by HIV envelope glycoproteins. Retrovirology. 2004;1:1–12.
  • Ethell DW, Buhler LA. Fas ligand-mediated apoptosis in degenerative disorders of the brain. J Clin Immunol. 2003;23:439–446.
  • Perfettini JL, Castedo M, Roumier T, et al. Mechanisms of apoptosis induction by the HIV-1 envelope. Cell Death Differ. 2005;12(Suppl 1):916–923.
  • Clever JL, Tam SM, Rold CJ, et al. Nef deletion in HIV-1 eliminates peripheral CD4 T-cell loss in a humanized BLT mouse model of HIV disease. Int J Drug Dev Res. 2016;8:058–064.
  • Andersen JL, DeHart JL, Zimmerman ES, et al. HIV-1 Vpr-induced apoptosis is cell cycle dependent and requires Bax but not ANT. PLoS Pathog. 2006;2:e127.
  • Murakami T, Aida Y. Visualizing Vpr-induced G2 arrest and apoptosis. PLoS ONE. 2014;9:e86840–e86840.
  • Fan Y, He JJ. HIV-1 tat induces unfolded protein response and endoplasmic reticulum stress in astrocytes and causes neurotoxicity through glial fibrillary acidic protein (GFAP) activation and aggregation. J Biol Chem. 2016;291:22819–22829.
  • Borsa M, Ferreira PL, Petry A, et al. HIV infection and antiretroviral therapy lead to unfolded protein response activation. Virol J. 2015;12:77.
  • Peymani P, Ghavami S, Yeganeh B, et al. Effect of chloroquine on some clinical and biochemical parameters in non-response chronic hepatitis C virus infection patients: pilot clinical trial. Acta Biomed. 2016;87:46–53.
  • Logue SE, McGrath EP, Cleary P, et al. Inhibition of IRE1 RNase activity modulates the tumor cell secretome and enhances response to chemotherapy. Nat Commun. 2018;9:3267.
  • Abdoli A, Alirezaei M, Mehrbod P, et al. Autophagy: the multi-purpose bridge in viral infections and host cells. Rev Med Virol. 2018;28:e1973.
  • Colamussi ML, White MR, Crouch E, et al. Influenza A virus accelerates neutrophil apoptosis and markedly potentiates apoptotic effects of bacteria. Blood. 1999;93:2395–2403.