Poliovirus induces autophagic signaling independent of the ULK1 complex

References

• González-Polo RA, Pizarro-Estrella E, Yakhine-Diop SMS, et al. The basics of autophagy. In: Maiuri MC, De Stefano D, editors. Autophagy networks in inflammation. New York (NY): Springer International Publishing. 2016. p. 3–20.
   Google Scholar
• Hurley JH, Young LN. Mechanisms of autophagy initiation. Annu Rev Biochem [Internet]. 2017. DOI:10.1146/annurev-biochem-061516-044820
   PubMed Web of Science ®Google Scholar
• Kim J, Kundu M, Viollet B, et al. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol. 2011;13:132–141.
   PubMed Web of Science ®Google Scholar
• Alers S, Löffler AS, Wesselborg S, et al. Role of AMPK-mTOR-Ulk1/2 in the regulation of autophagy: cross talk, shortcuts, and feedbacks. Mol Cell Biol. 2012;32:2–11.
   PubMed Web of Science ®Google Scholar
• Russell RC, Tian Y, Yuan H, et al. ULK1 induces autophagy by phosphorylating Beclin-1 and activating VPS34 lipid kinase. Nat Cell Biol. 2013;15:741–750.
   PubMed Web of Science ®Google Scholar
• Puente C, Hendrickson RC, Jiang X. Nutrient-regulated phosphorylation of ATG13 inhibits starvation-induced autophagy. J Biol Chem. 2016;291:6026–6035.
   PubMed Web of Science ®Google Scholar
• Jung CH, Jun CB, Ro S-H, et al. ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery. Mol Biol Cell. 2009;20:1992–2003.
   PubMed Web of Science ®Google Scholar
• Hosokawa N, Sasaki T, Iemura S-I, et al. Atg101, a novel mammalian autophagy protein interacting with Atg13. Autophagy. 2009;5:973–979.
   PubMed Web of Science ®Google Scholar
• Richetta C, Faure M. Autophagy in antiviral innate immunity. Cell Microbiol. 2013;15:368–376.
   PubMed Web of Science ®Google Scholar
• Jackson WT. Viruses and the autophagy pathway. Virology. 2015;479-480:450–456.
   PubMed Web of Science ®Google Scholar
• Jackson WT, Giddings TH Jr, Taylor MP, et al. Subversion of cellular autophagosomal machinery by RNA viruses. PLoS Biol. 2005;3:e156.
   PubMed Web of Science ®Google Scholar
• Richards AL, Jackson WT. Intracellular vesicle acidification promotes maturation of infectious poliovirus particles. PLoS Pathog. 2012;8:e1003046.
   PubMed Web of Science ®Google Scholar
• Taylor MP, Kirkegaard K. Modification of cellular autophagy protein LC3 by poliovirus. J Virol. 2007;81:12543–12553.
   PubMed Web of Science ®Google Scholar
• Suhy DA, Giddings TH Jr, Kirkegaard K. Remodeling the endoplasmic reticulum by poliovirus infection and by individual viral proteins: an autophagy-like origin for virus-induced vesicles. J Virol. 2000;74:8953–8965.
   PubMed Web of Science ®Google Scholar
• Gladue DP, O’Donnell V, Baker-Branstetter R, et al. Foot-and-mouth disease virus nonstructural protein 2C interacts with Beclin1, modulating virus replication. J Virol. 2012;86:12080–12090.
   PubMed Web of Science ®Google Scholar
• Too IHK, Yeo H, Sessions OM, et al. Enterovirus 71 infection of motor neuron-like NSC-34 cells undergoes a non-lytic exit pathway. Sci Rep. 2016;6:36983.
   PubMed Web of Science ®Google Scholar
• Huang S-C, Chang C-L, Wang P-S, et al. Enterovirus 71-induced autophagy detected in vitro and in vivo promotes viral replication. J Med Virol. 2009;81:1241–1252.
   PubMed Web of Science ®Google Scholar
• Alers S, Löffler AS, Wesselborg S, et al. The incredible ULKs. Cell Commun Signal. 2012;10:7.
   PubMed Web of Science ®Google Scholar
• Lee E-J, Tournier C. The requirement of uncoordinated 51-like kinase 1 (ULK1) and ULK2 in the regulation of autophagy. Autophagy. 2011;7:689–695.
   PubMed Web of Science ®Google Scholar
• Kundu M, Lindsten T, Yang C-Y, et al. Ulk1 plays a critical role in the autophagic clearance of mitochondria and ribosomes during reticulocyte maturation. Blood. 2008;112:1493–1502.
   PubMed Web of Science ®Google Scholar
• Petherick KJ, Conway OJL, Mpamhanga C, et al. Pharmacological inhibition of ULK1 kinase blocks mammalian target of rapamycin (mTOR)-dependent autophagy. J Biol Chem. 2015;290:11376–11383.
   PubMed Web of Science ®Google Scholar
• Hara T, Takamura A, Kishi C, et al. FIP200, a ULK-interacting protein, is required for autophagosome formation in mammalian cells. J Cell Biol. 2008;181:497–510.
   PubMed Web of Science ®Google Scholar
• Yamamoto A, Tagawa Y, Yoshimori T, et al. Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line, H-4-II-E cells. Cell Struct Funct. 1998;23:33–42.
   PubMed Web of Science ®Google Scholar
• Shi J, Wong J, Piesik P, et al. Cleavage of sequestosome 1/p62 by an enteroviral protease results in disrupted selective autophagy and impaired NFKB signaling. Autophagy. 2013;9:1591–1603.
   PubMed Web of Science ®Google Scholar
• Shi J, Fung G, Piesik P, et al. Dominant-negative function of the C-terminal fragments of NBR1 and SQSTM1 generated during enteroviral infection. Cell Death Differ. 2014;21:1432–1441.
   PubMed Web of Science ®Google Scholar
• Lee YH, Ko J, Joung I, et al. Immediate early response of the p62 gene encoding a non-proteasomal multiubiquitin chain binding protein. FEBS Lett. 1998;438:297–300.
   PubMed Web of Science ®Google Scholar
• Jain A, Lamark T, Sjøttem E, et al. p62/SQSTM1 is a target gene for transcription factor NRF2 and creates a positive feedback loop by inducing antioxidant response element-driven gene transcription. J Biol Chem. 2010;285:22576–22591.
   PubMed Web of Science ®Google Scholar
• Davies MV, Pelletier J, Meerovitch K, et al. The effect of poliovirus proteinase 2Apro expression on cellular metabolism. Inhibition of DNA replication, RNA polymerase II transcription, and translation. J Biol Chem. 1991;266:14714–14720.
   PubMed Web of Science ®Google Scholar
• Hirano Y, Hendil KB, Yashiroda H, et al. A heterodimeric complex that promotes the assembly of mammalian 20S proteasomes. Nature. 2005;437:1381–1385.
   PubMed Web of Science ®Google Scholar
• Chase AJ, Semler BL. Viral subversion of host functions for picornavirus translation and RNA replication. Future Virol. 2012;7:179–191.
   PubMed Web of Science ®Google Scholar
• Tamm I, Eggers HJ. Differences in the selective virus inhibitory action of 2-(alpha-hydroxybenzyl)-benzimidazole and guanidine HCl. Virology. 1962;18:439–447.
   PubMed Web of Science ®Google Scholar
• Yan J, Kuroyanagi H, Kuroiwa A, et al. Identification of mouse ULK1, a novel protein kinase structurally related to C. elegans UNC-51. Biochem Biophys Res Commun. 1998;246:222–227.
   PubMed Web of Science ®Google Scholar
• Scott RC, Juhász G, Neufeld TP. Direct induction of autophagy by Atg1 inhibits cell growth and induces apoptotic cell death. Curr Biol. 2007;17:1–11.
   PubMed Web of Science ®Google Scholar
• Cheong H, Lindsten T, Wu J, et al. Ammonia-induced autophagy is independent of ULK1/ULK2 kinases. Proc Natl Acad Sci U S A. 2011;108:11121–11126.
   PubMed Web of Science ®Google Scholar
• Zhang D, Wang W, Sun X, et al. AMPK regulates autophagy by phosphorylating BECN1 at threonine 388. Autophagy. 2016;12:1447–1459.
   PubMed Web of Science ®Google Scholar
• Xin L, Ma X, Xiao Z, et al. Coxsackievirus B3 induces autophagy in HeLa cells via the AMPK/MEK/ERK and Ras/Raf/MEK/ERK signaling pathways. Infect Genet Evol. 2015;36:46–54.
   PubMed Web of Science ®Google Scholar
• Xie W, Wang L, Dai Q, et al. Activation of AMPK restricts coxsackievirus B3 replication by inhibiting lipid accumulation. J Mol Cell Cardiol. 2015;85:155–167.
   PubMed Web of Science ®Google Scholar
• Liao -C-C, Ho M-Y, Liang S-M, et al. Recombinant protein rVP1 upregulates BECN1-independent autophagy, MAPK1/3 phosphorylation and MMP9 activity via WIPI1/WIPI2 to promote macrophage migration. Autophagy. 2013;9:5–19.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Jiao H, Su G-Q, Dong W, et al. Chaperone-like protein p32 regulates ULK1 stability and autophagy. Cell Death Differ. 2015;22:1812–1823.
   PubMed Web of Science ®Google Scholar
• Nazio F, Carinci M, Valacca C, et al. Fine-tuning of ULK1 mRNA and protein levels is required for autophagy oscillation. J Cell Biol. 2016;215:841–856.
   PubMed Web of Science ®Google Scholar
• Haller AA, Semler BL. Translation and host cell shutoff. In: Rotbart HA, editor. Human enterovirus infections. Washington (DC): ASM Press; 1995. p. 113–133.
   Google Scholar
• Rubinstein SJ, Dasgupta A. Inhibition of rRNA synthesis by poliovirus: specific inactivation of transcription factors. J Virol. 1989;63:4689–4696.
   PubMed Web of Science ®Google Scholar
• Mauthe M, Langereis M, Jung J, et al. An siRNA screen for ATG protein depletion reveals the extent of the unconventional functions of the autophagy proteome in virus replication. J Cell Biol. 2016;214:619–635.
   PubMed Web of Science ®Google Scholar
• Itakura E, Mizushima N. Characterization of autophagosome formation site by a hierarchical analysis of mammalian Atg proteins. Autophagy. 2010;6:764–776.
   PubMed Web of Science ®Google Scholar
• Richards AL, Soares-Martins JAP, Riddell GT, et al. Generation of unique poliovirus RNA replication organelles. MBio. 2014;5:e00833–13.
   PubMed Web of Science ®Google Scholar
• Wang D, Olman MA, Stewart J Jr, et al. Downregulation of FIP200 induces apoptosis of glioblastoma cells and microvascular endothelial cells by enhancing Pyk2 activity. PLoS One. 2011;6:e19629.
   PubMed Web of Science ®Google Scholar
• Xu J, Fotouhi M, McPherson PS. Phosphorylation of the exchange factor DENND3 by ULK in response to starvation activates Rab12 and induces autophagy. EMBO Rep. 2015;16:709–718.
   PubMed Web of Science ®Google Scholar
• Racaniello VR, Baltimore D. Cloned poliovirus complementary DNA is infectious in mammalian cells. Science. 1981;214:916–919.
   PubMed Web of Science ®Google Scholar