So Many Roads: the Multifaceted Regulation of Autophagy Induction

REFERENCES

• Ohsumi Y. 2014. Historical landmarks of autophagy research. Cell Res 24:9–23. https://doi.org/10.1038/cr.2013.169.
   PubMed Web of Science ®Google Scholar
• Tanida I. 2011. Autophagy basics. Microbiol Immunol 55:1–11. https://doi.org/10.1111/j.1348-0421.2010.00271.x.
   PubMed Web of Science ®Google Scholar
• White E, Mehnert JM, Chan CS. 2015. Autophagy, metabolism, and cancer. Clin Cancer Res 21:5037–5046. https://doi.org/10.1158/1078-0432.CCR-15-0490.
   PubMed Web of Science ®Google Scholar
• Romao S, Gasser N, Becker AC, Guhl B, Bajagic M, Vanoaica D, Ziegler U, Roesler J, Dengjel J, Reichenbach J, Münz C. 2013. Autophagy proteins stabilize pathogen-containing phagosomes for prolonged MHC II antigen processing. J Cell Biol 203:757–766. https://doi.org/10.1083/jcb.201308173.
   PubMed Web of Science ®Google Scholar
• Klionsky DJ, et al.. 2016. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy 12:1–222. https://doi.org/10.1080/15548627.2015.1100356.
   PubMed Web of Science ®Google Scholar
• Kimura S, Fujita N, Noda T, Yoshimori T. 2009. Monitoring autophagy in mammalian cultured cells through the dynamics of LC3. Methods Enzymol 452:1–12. https://doi.org/10.1016/S0076-6879(08)03601-X.
   PubMed Web of Science ®Google Scholar
• Jiang P, Mizushima N. 2015. LC3- and p62-based biochemical methods for the analysis of autophagy progression in mammalian cells. Methods 75:13–18. https://doi.org/10.1016/j.ymeth.2014.11.021.
   PubMed Web of Science ®Google Scholar
• Thost A-K, Dönnes P, Kohlbacher O, Proikas-Cezanne T. 2015. Fluorescence-based imaging of autophagy progression by human WIPI protein detection. Methods 75:69–78. https://doi.org/10.1016/j.ymeth.2014.11.011.
   PubMed Web of Science ®Google Scholar
• Noda T, Ohsumi Y. 1998. Tor, a phosphatidylinositol kinase homologue, controls autophagy in yeast. J Biol Chem 273:3963–3966. https://doi.org/10.1074/jbc.273.7.3963.
   PubMed Web of Science ®Google Scholar
• Chan TF, Carvalho J, Riles L, Zheng XF. 2000. A chemical genomics approach toward understanding the global functions of the target of rapamycin protein (TOR). Proc Natl Acad Sci U S A 97:13227–13232. https://doi.org/10.1073/pnas.240444197.
   PubMed Web of Science ®Google Scholar
• Matsuura A, Tsukada M, Wada Y, Ohsumi Y. 1997. Apg1p, a novel protein kinase required for the autophagic process in Saccharomyces cerevisiae. Gene 192:245–250. https://doi.org/10.1016/S0378-1119(97)00084-X.
   PubMed Web of Science ®Google Scholar
• Kametaka S, Matsuura A, Wada Y, Ohsumi Y. 1996. Structural and functional analyses of APG5, a gene involved in autophagy in yeast. Gene 178:139–143. https://doi.org/10.1016/0378-1119(96)00354-X.
   PubMed Web of Science ®Google Scholar
• Funakoshi T, Matsuura A, Noda T, Ohsumi Y. 1997. Analyses of APG13 gene involved in autophagy in yeast, Saccharomyces cerevisiae. Gene 192:207–213. https://doi.org/10.1016/S0378-1119(97)00031-0.
   PubMed Web of Science ®Google Scholar
• Papinski D, Kraft C. 2014. Atg1 kinase organizes autophagosome formation by phosphorylating Atg9. Autophagy 10:1338–1340. https://doi.org/10.4161/auto.28971.
   PubMed Web of Science ®Google Scholar
• Chang Y-Y, Neufeld TP. 2009. An Atg1/Atg13 complex with multiple roles in TOR-mediated autophagy regulation. Mol Biol Cell 20:2004–2014. https://doi.org/10.1091/mbc.e08-12-1250.
   PubMed Web of Science ®Google Scholar
• Yan J, Kuroyanagi H, Kuroiwa A, Matsuda Y, Tokumitsu H, Tomoda T, Shirasawa T, Muramatsu M. 1998. Identification of mouse ULK1, a novel protein kinase structurally related to C. elegans UNC-51. Biochem Biophys Res Commun 246:222–227. https://doi.org/10.1006/bbrc.1998.8546.
   PubMed Web of Science ®Google Scholar
• Kuroyanagi H, Yan J, Seki N, Yamanouchi Y, Suzuki Y, Takano T, Muramatsu M, Shirasawa T. 1998. Human ULK1, a novel serine/threonine kinase related to UNC-51 kinase of Caenorhabditis elegans: cDNA cloning, expression, and chromosomal assignment. Genomics 51:76–85. https://doi.org/10.1006/geno.1998.5340.
   PubMed Web of Science ®Google Scholar
• Yan J, Kuroyanagi H, Tomemori T, Okazaki N, Asato K, Matsuda Y, Suzuki Y, Ohshima Y, Mitani S, Masuho Y, Shirasawa T, Muramatsu M. 1999. Mouse ULK2, a novel member of the UNC-51-like protein kinases: unique features of functional domains. Oncogene 18:5850–5859. https://doi.org/10.1038/sj.onc.1202988.
   PubMedGoogle Scholar
• Chan EYW, Kir S, Tooze SA. 2007. siRNA screening of the kinome identifies ULK1 as a multidomain modulator of autophagy. J Biol Chem 282:25464–25474. https://doi.org/10.1074/jbc.M703663200.
   PubMed Web of Science ®Google Scholar
• Lee E-J, Tournier C. 2011. The requirement of uncoordinated 51-like kinase 1 (ULK1) and ULK2 in the regulation of autophagy. Autophagy 7:689–695. https://doi.org/10.4161/auto.7.7.15450.
   PubMed Web of Science ®Google Scholar
• Nath S, Dancourt J, Shteyn V, Puente G, Fong WM, Nag S, Bewersdorf J, Yamamoto A, Antonny B, Melia TJ. 2014. Lipidation of the LC3/GABARAP family of autophagy proteins relies on a membrane-curvature-sensing domain in Atg3. Nat Cell Biol 16:415–424. https://doi.org/10.1038/ncb2940.
   PubMed Web of Science ®Google Scholar
• Nguyen TN, Padman BS, Usher J, Oorschot V, Ramm G, Lazarou M. 2016. Atg8 family LC3/GABARAP proteins are crucial for autophagosome-lysosome fusion but not autophagosome formation during PINK1/Parkin mitophagy and starvation. J Cell Biol 215:857–874.
   PubMed Web of Science ®Google Scholar
• Ganley IG, Lam DH, Wang J, Ding X, Chen S, Jiang X. 2009. ULK1.ATG13.FIP200 complex mediates mTOR signaling and is essential for autophagy. J Biol Chem 284:12297–12305. https://doi.org/10.1074/jbc.M900573200.
   PubMed Web of Science ®Google Scholar
• Hara T, Mizushima N. 2009. Role of ULK-FIP200 complex in mammalian autophagy: FIP200, a counterpart of yeast Atg17? Autophagy 5:85–87. https://doi.org/10.4161/auto.5.1.7180.
   PubMed Web of Science ®Google Scholar
• Hara T, Takamura A, Kishi C, Iemura S-I, Natsume T, Guan J-L, Mizushima N. 2008. FIP200, a ULK-interacting protein, is required for autophagosome formation in mammalian cells. J Cell Biol 181:497–510. https://doi.org/10.1083/jcb.200712064.
   PubMed Web of Science ®Google Scholar
• Hosokawa N, Sasaki T, Iemura S, Natsume T, Hara T, Mizushima N. 2009. Atg101, a novel mammalian autophagy protein interacting with Atg13. Autophagy 5:973–979. https://doi.org/10.4161/auto.5.7.9296.
   PubMed Web of Science ®Google Scholar
• Kim J, Kundu M, Viollet B, Guan K-L. 2011. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol 13:132–141. https://doi.org/10.1038/ncb2152.
   PubMed Web of Science ®Google Scholar
• Hosokawa N, Hara T, Kaizuka T, Kishi C, Takamura A, Miura Y, Iemura S, Natsume T, Takehana K, Yamada N, Guan J-L, Oshiro N, Mizushima N. 2009. Nutrient-dependent mTORC1 association with the ULK1-Atg13-FIP200 complex required for autophagy. Mol Biol Cell 20:1981–1991. https://doi.org/10.1091/mbc.e08-12-1248.
   PubMed Web of Science ®Google Scholar
• Jung CH, Jun CB, Ro S-H, Kim Y-M, Otto NM, Cao J, Kundu M, Kim D-H. 2009. ULK-Atg13-FIP200 complexes mediate mTOR signaling to the autophagy machinery. Mol Biol Cell 20:1992–2003. https://doi.org/10.1091/mbc.e08-12-1249.
   PubMed Web of Science ®Google Scholar
• Chen S, Wang C, Yeo S, Liang C-C, Okamoto T, Sun S, Wen J, Guan J-L. 2016. Distinct roles of autophagy-dependent and -independent functions of FIP200 revealed by generation and analysis of a mutant knock-in mouse model. Genes Dev 30:856–869. https://doi.org/10.1101/gad.276428.115.
   PubMed Web of Science ®Google Scholar
• Qi S, Kim DJ, Stjepanovic G, Hurley JH. 2015. Structure of the human Atg13-Atg101 HORMA heterodimer: an interaction hub within the ULK1 complex. Structure 23:1848–1857.
   PubMed Web of Science ®Google Scholar
• Alemu EA, Lamark T, Torgersen KM, Birgisdottir AB, Larsen KB, Jain A, Olsvik H, Øvervatn A, Kirkin V, Johansen T. 2012. ATG8 family proteins act as scaffolds for assembly of the ULK complex: sequence requirements for LC3-interacting region (LIR) motifs. J Biol Chem 287:39275–39290. https://doi.org/10.1074/jbc.M112.378109.
   PubMed Web of Science ®Google Scholar
• Okazaki N, Yan J, Yuasa S, Ueno T, Kominami E, Masuho Y, Koga H, Muramatsu M. 2000. Interaction of the Unc-51-like kinase and microtubule-associated protein light chain 3 related proteins in the brain: possible role of vesicular transport in axonal elongation. Brain Res Mol Brain Res 85:1–12. https://doi.org/10.1016/S0169-328X(00)00218-7.
   PubMedGoogle Scholar
• Suzuki H, Tabata K, Morita E, Kawasaki M, Kato R, Dobson RCJ, Yoshimori T, Wakatsuki S. 2014. Structural basis of the autophagy-related LC3/Atg13 LIR complex: recognition and interaction mechanism. Structure 22:47–58. https://doi.org/10.1016/j.str.2013.09.023.
   PubMed Web of Science ®Google Scholar
• Kim D-H, Sarbassov DD, Ali SM, King JE, Latek RR, Erdjument-Bromage H, Tempst P, Sabatini DM. 2002. mTOR interacts with raptor to form a nutrient-sensitive complex that signals to the cell growth machinery. Cell 110:163–175. https://doi.org/10.1016/S0092-8674(02)00808-5.
   PubMed Web of Science ®Google Scholar
• Kim D-H, Sarbassov DD, Ali SM, Latek RR, Guntur KVP, Erdjument-Bromage H, Tempst P, Sabatini DM. 2003. GbetaL, a positive regulator of the rapamycin-sensitive pathway required for the nutrient-sensitive interaction between raptor and mTOR. Mol Cell 11:895–904. https://doi.org/10.1016/S1097-2765(03)00114-X.
   PubMed Web of Science ®Google Scholar
• Wullschleger S, Loewith R, Hall MN. 2006. TOR signaling in growth and metabolism. Cell 124:471–484. https://doi.org/10.1016/j.cell.2006.01.016.
   PubMed Web of Science ®Google Scholar
• Lee JW, Park S, Takahashi Y, Wang H-G. 2010. The association of AMPK with ULK1 regulates autophagy. PLoS One 5:e15394. https://doi.org/10.1371/journal.pone.0015394.
   PubMed Web of Science ®Google Scholar
• Rourke JL, Hu Q, Screaton RA. 2018. AMPK and friends: central regulators of β cell biology. Trends Endocrinol Metab 29:111–122. https://doi.org/10.1016/j.tem.2017.11.007.
   PubMedGoogle Scholar
• Cordero MD, Williams MR, Ryffel B. 2018. AMP-activated protein kinase regulation of the NLRP3 inflammasome during aging. Trends Endocrinol Metab 29:8–17. https://doi.org/10.1016/j.tem.2017.10.009.
   PubMed Web of Science ®Google Scholar
• Herzig S, Shaw RJ. 2018. AMPK: guardian of metabolism and mitochondrial homeostasis. Nat Rev Mol Cell Biol 19:121–135. https://doi.org/10.1038/nrn.2018.14.
   PubMed Web of Science ®Google Scholar
• Puente C, Hendrickson RC, Jiang X. 2016. Nutrient-regulated phosphorylation of ATG13 inhibits starvation-induced autophagy. J Biol Chem 291:6026–6035. https://doi.org/10.1074/jbc.M115.689646.
   PubMed Web of Science ®Google Scholar
• Dunlop EA, Hunt DK, Acosta-Jaquez HA, Fingar DC, Tee AR. 2011. ULK1 inhibits mTORC1 signaling, promotes multisite Raptor phosphorylation and hinders substrate binding. Autophagy 7:737–747. https://doi.org/10.4161/auto.7.7.15491.
   PubMed Web of Science ®Google Scholar
• Löffler AS, Alers S, Dieterle AM, Keppeler H, Franz-Wachtel M, Kundu M, Campbell DG, Wesselborg S, Alessi DR, Stork B. 2011. Ulk1-mediated phosphorylation of AMPK constitutes a negative regulatory feedback loop. Autophagy 7:696–706. https://doi.org/10.4161/auto.7.7.15451.
   PubMed Web of Science ®Google Scholar
• Russell RC, Tian Y, Yuan H, Park HW, Chang Y-Y, Kim J, Kim H, Neufeld TP, Dillin A, Guan K-L. 2013. ULK1 induces autophagy by phosphorylating Beclin-1 and activating VPS34 lipid kinase. Nat Cell Biol 15:741–750. https://doi.org/10.1038/ncb2757.
   PubMed Web of Science ®Google Scholar
• Fogel AI, Dlouhy BJ, Wang C, Ryu S-W, Neutzner A, Hasson SA, Sideris DP, Abeliovich H, Youle RJ. 2013. Role of membrane association and Atg14-dependent phosphorylation in beclin-1-mediated autophagy. Mol Cell Biol 33:3675–3688. https://doi.org/10.1128/MCB.00079-13.
   PubMed Web of Science ®Google Scholar
• Park J-M, Seo M, Jung CH, Grunwald D, Stone M, Otto NM, Toso E, Ahn Y, Kyba M, Griffin TJ, Higgins L, Kim D-H. 2018. ULK1 phosphorylates Ser30 of BECN1 in association with ATG14 to stimulate autophagy induction. Autophagy 14:584–597. https://doi.org/10.1080/15548627.2017.1422851.
   PubMed Web of Science ®Google Scholar
• Dooley HC, Razi M, Polson HEJ, Girardin SE, Wilson MI, Tooze SA. 2014. WIPI2 links LC3 conjugation with PI3P, autophagosome formation, and pathogen clearance by recruiting Atg12-5-16L1. Mol Cell 55:238–252. https://doi.org/10.1016/j.molcel.2014.05.021.
   PubMed Web of Science ®Google Scholar
• Grotemeier A, Alers S, Pfisterer SG, Paasch F, Daubrawa M, Dieterle A, Viollet B, Wesselborg S, Proikas-Cezanne T, Stork B. 2010. AMPK-independent induction of autophagy by cytosolic Ca2+ increase. Cell Signal 22:914–925. https://doi.org/10.1016/j.cellsig.2010.01.015.
   PubMed Web of Science ®Google Scholar
• Thastrup O, Cullen PJ, Drøbak BK, Hanley MR, Dawson AP. 1990. Thapsigargin, a tumor promoter, discharges intracellular Ca2+ stores by specific inhibition of the endoplasmic reticulum Ca2(+)-ATPase. Proc Natl Acad Sci U S A 87:2466–2470.
   PubMed Web of Science ®Google Scholar
• Bernales S, McDonald KL, Walter P. 2006. Autophagy counterbalances endoplasmic reticulum expansion during the unfolded protein response. PLoS Biol 4:e423. https://doi.org/10.1371/journal.pbio.0040423.
   PubMed Web of Science ®Google Scholar
• Ganley IG, Wong P-M, Gammoh N, Jiang X. 2011. Distinct autophagosomal-lysosomal fusion mechanism revealed by thapsigargin-induced autophagy arrest. Mol Cell 42:731–743. https://doi.org/10.1016/j.molcel.2011.04.024.
   PubMed Web of Science ®Google Scholar
• Mauvezin C, Nagy P, Juhász G, Neufeld TP. 2015. Autophagosome-lysosome fusion is independent of V-ATPase-mediated acidification. Nat Commun 6:7007. https://doi.org/10.1038/ncomms8007.
   PubMed Web of Science ®Google Scholar
• Moruno-Manchón JF, Pérez-Jiménez E, Knecht E. 2013. Glucose induces autophagy under starvation conditions by a p38 MAPK-dependent pathway. Biochem J 449:497–506. https://doi.org/10.1042/BJ20121122.
   PubMed Web of Science ®Google Scholar
• Yamamoto A, Mizushima N, Tsukamoto S. 2014. Fertilization-induced autophagy in mouse embryos is independent of mTORC1. Biol Reprod 91:7. https://doi.org/10.1095/biolreprod.113.115816.
   PubMed Web of Science ®Google Scholar
• Watanabe-Asano T, Kuma A, Mizushima N. 2014. Cycloheximide inhibits starvation-induced autophagy through mTORC1 activation. Biochem Biophys Res Commun 445:334–339. https://doi.org/10.1016/j.bbrc.2014.01.180.
   PubMed Web of Science ®Google Scholar
• Choi H, Merceron C, Mangiavini L, Seifert EL, Schipani E, Shapiro IM, Risbud MV. 2016. Hypoxia promotes noncanonical autophagy in nucleus pulposus cells independent of MTOR and HIF1A signaling. Autophagy 12:1631–1646. https://doi.org/10.1080/15548627.2016.1192753.
   PubMed Web of Science ®Google Scholar
• Nwadike C, Williamson LE, Gallagher LE, Guan J-L, Chan EYW. 2018. AMPK inhibits ULK1-dependent autophagosome formation and lysosomal acidification via distinct mechanisms. Mol Cell Biol 38:e00023-18. https://doi.org/10.1128/MCB.00023-18.
   Google Scholar
• Pfisterer SG, Mauthe M, Codogno P, Proikas-Cezanne T. 2011. Ca2+/calmodulin-dependent kinase (CaMK) signaling via CaMKI and AMP-activated protein kinase contributes to the regulation of WIPI-1 at the onset of autophagy. Mol Pharmacol 80:1066–1075. https://doi.org/10.1124/mol.111.071761.
   PubMed Web of Science ®Google Scholar
• Williams T, Forsberg LJ, Viollet B, Brenman JE. 2009. Basal autophagy induction without AMP-activated protein kinase under low glucose conditions. Autophagy 5:1155–1165. https://doi.org/10.4161/auto.5.8.10090.
   PubMed Web of Science ®Google Scholar
• Yazawa T, Imamichi Y, Miyamoto K, Khan MRI, Uwada J, Umezawa A, Taniguchi T. 2016. Induction of steroidogenic cells from adult stem cells and pluripotent stem cells. Endocr J 63:943–951. https://doi.org/10.1507/endocrj.EJ16-0373.
   PubMedGoogle Scholar
• Ugland H, Naderi S, Brech A, Collas P, Blomhoff HK. 2011. cAMP induces autophagy via a novel pathway involving ERK, cyclin E and Beclin 1. Autophagy 7:1199–1211. https://doi.org/10.4161/auto.7.10.16649.
   PubMed Web of Science ®Google Scholar
• Cheong H, Lindsten T, Wu J, Lu C, Thompson CB. 2011. Ammonia-induced autophagy is independent of ULK1/ULK2 kinases. Proc Natl Acad Sci U S A 108:11121–11126. https://doi.org/10.1073/pnas.1107969108.
   PubMed Web of Science ®Google Scholar
• Alers S, Löffler AS, Paasch F, Dieterle AM, Keppeler H, Lauber K, Campbell DG, Fehrenbacher B, Schaller M, Wesselborg S, Stork B. 2011. Atg13 and FIP200 act independently of Ulk1 and Ulk2 in autophagy induction. Autophagy 7:1423–1433. https://doi.org/10.4161/auto.7.12.18027.
   PubMed Web of Science ®Google Scholar
• Niso-Santano M, Malik SA, Pietrocola F, Bravo-San Pedro JM, Mariño G, Cianfanelli V, Ben-Younès A, Troncoso R, Markaki M, Sica V, Izzo V, Chaba K, Bauvy C, Dupont N, Kepp O, Rockenfeller P, Wolinski H, Madeo F, Lavandero S, Codogno P, Harper F, Pierron G, Tavernarakis N, Cecconi F, Maiuri MC, Galluzzi L, Kroemer G. 2015. Unsaturated fatty acids induce non-canonical autophagy. EMBO J 34:1025–1041. https://doi.org/10.15252/embj.201489363.
   PubMed Web of Science ®Google Scholar
• Kim J, Kim YC, Fang C, Russell RC, Kim JH, Fan W, Liu R, Zhong Q, Guan K-L. 2013. Differential regulation of distinct Vps34 complexes by AMPK in nutrient stress and autophagy. Cell 152:290–303. https://doi.org/10.1016/j.cell.2012.12.016.
   PubMed Web of Science ®Google Scholar
• Zhang D, Wang W, Sun X, Xu D, Wang C, Zhang Q, Wang H, Luo W, Chen Y, Chen H, Liu Z. 2016. AMPK regulates autophagy by phosphorylating BECN1 at threonine 388. Autophagy 12:1447–1459. https://doi.org/10.1080/15548627.2016.1185576.
   PubMed Web of Science ®Google Scholar
• Li X, Wu X-Q, Deng R, Li D-D, Tang J, Chen W-D, Chen J-H, Ji J, Jiao L, Jiang S, Yang F, Feng G-K, Senthilkumar R, Yue F, Zhang H-L, Wu R-Y, Yu Y, Xu X-L, Mai J, Li Z-L, Peng X-D, Huang Y, Huang X, Ma N-F, Tao Q, Zeng Y-X, Zhu X-F. 2017. CaMKII-mediated Beclin 1 phosphorylation regulates autophagy that promotes degradation of Id and neuroblastoma cell differentiation. Nat Commun 8:1159. https://doi.org/10.1038/s41467-017-01272-2.
   PubMed Web of Science ®Google Scholar
• Qian X, Li X, Lu Z. 2017. Protein kinase activity of the glycolytic enzyme PGK1 regulates autophagy to promote tumorigenesis. Autophagy 13:1246–1247. https://doi.org/10.1080/15548627.2017.1313945.
   PubMed Web of Science ®Google Scholar
• Cheng Z, Zhu Q, Dee R, Opheim Z, Mack CP, Cyr DM, Taylor JM. 2017. Focal adhesion kinase-mediated phosphorylation of beclin1 protein suppresses cardiomyocyte autophagy and initiates hypertrophic growth. J Biol Chem 292:2065–2079. https://doi.org/10.1074/jbc.M116.758268.
   PubMed Web of Science ®Google Scholar
• Zalckvar E, Berissi H, Mizrachy L, Idelchuk Y, Koren I, Eisenstein M, Sabanay H, Pinkas-Kramarski R, Kimchi A. 2009. DAP-kinase-mediated phosphorylation on the BH3 domain of beclin 1 promotes dissociation of beclin 1 from Bcl-XL and induction of autophagy. EMBO Rep 10:285–292. https://doi.org/10.1038/embor.2008.246.
   PubMed Web of Science ®Google Scholar
• Fujiwara N, Usui T, Ohama T, Sato K. 2016. Regulation of Beclin 1 protein phosphorylation and autophagy by protein phosphatase 2A (PP2A) and death-associated protein kinase 3 (DAPK3). J Biol Chem 291:10858–10866. https://doi.org/10.1074/jbc.M115.704908.
   PubMed Web of Science ®Google Scholar
• Wei Y, An Z, Zou Z, Sumpter R, Su M, Zang X, Sinha S, Gaestel M, Levine B. 2015. The stress-responsive kinases MAPKAPK2/MAPKAPK3 activate starvation-induced autophagy through Beclin 1 phosphorylation. Elife 4:e05289. https://doi.org/10.7554/eLife.05289.
   PubMed Web of Science ®Google Scholar
• Wang J, Zhou J-Y, Kho D, Reiners JJ, Wu GS. 2016. Role for DUSP1 (dual-specificity protein phosphatase 1) in the regulation of autophagy. Autophagy 12:1791–1803. https://doi.org/10.1080/15548627.2016.1203483.
   PubMed Web of Science ®Google Scholar
• Wang RC, Wei Y, An Z, Zou Z, Xiao G, Bhagat G, White M, Reichelt J, Levine B. 2012. Akt-mediated regulation of autophagy and tumorigenesis through Beclin 1 phosphorylation. Science 338:956–959. https://doi.org/10.1126/science.1225967.
   PubMed Web of Science ®Google Scholar
• Birmingham CL, Higgins DE, Brumell JH. 2008. Avoiding death by autophagy: interactions of Listeria monocytogenes with the macrophage autophagy system. Autophagy 4:368–371. https://doi.org/10.4161/auto.5594.
   PubMed Web of Science ®Google Scholar
• Alirezaei M, Flynn CT, Wood MR, Harkins S, Whitton JL. 2015. Coxsackievirus can exploit LC3 in both autophagy-dependent and -independent manners in vivo. Autophagy 11:1389–1407. https://doi.org/10.1080/15548627.2015.1063769.
   PubMed Web of Science ®Google Scholar
• Jackson WT. 2015. Viruses and the autophagy pathway. Virology 479-480:450–456.
   PubMed Web of Science ®Google Scholar
• Chen X, Wang K, Xing Y, Tu J, Yang X, Zhao Q, Li K, Chen Z. 2014. Coronavirus membrane-associated papain-like proteases induce autophagy through interacting with Beclin1 to negatively regulate antiviral innate immunity. Protein Cell 5:912–927. https://doi.org/10.1007/s13238-014-0104-6.
   PubMed Web of Science ®Google Scholar
• Zhong L, Shu W, Dai W, Gao B, Xiong S. 2017. Reactive oxygen species-mediated c-Jun NH2-terminal kinase activation contributes to hepatitis B virus X protein-induced autophagy via regulation of the Beclin-1/Bcl-2 interaction. J Virol 91:e00001-17. https://doi.org/10.1128/JVI.00001-17.
   Google Scholar
• Corona Velazquez A, Corona A, Klein KA, Jackson WT. 2018. Poliovirus induces autophagic signaling independent of the ULK1 complex. Autophagy 14:1201–1213. https://doi.org/10.1080/15548627.2018.1458805.
   PubMed Web of Science ®Google Scholar
• Corona AK, Saulsbery HM, Corona Velazquez AF, Jackson WT. 2018. Enteroviruses remodel autophagic trafficking through regulation of host SNARE proteins to promote virus replication and cell exit. Cell Rep 22:3304–3314. https://doi.org/10.1016/j.celrep.2018.03.003.
   PubMed Web of Science ®Google Scholar
• Shi J, Wong J, Piesik P, Fung G, Zhang J, Jagdeo J, Li X, Jan E, Luo H. 2013. Cleavage of sequestosome 1/p62 by an enteroviral protease results in disrupted selective autophagy and impaired NFKB signaling. Autophagy 9:1591–1603. https://doi.org/10.4161/auto.26059.
   PubMed Web of Science ®Google Scholar
• Jakhar R, Paul S, Bhardwaj M, Kang SC. 2016. Astemizole-histamine induces Beclin-1-independent autophagy by targeting p53-dependent crosstalk between autophagy and apoptosis. Cancer Lett 372:89–100. https://doi.org/10.1016/j.canlet.2015.12.024.
   PubMed Web of Science ®Google Scholar
• Athamneh K, Hasasna HE, Samri HA, Attoub S, Arafat K, Benhalilou N, Rashedi AA, Dhaheri YA, AbuQamar S, Eid A, Iratni R. 2017. Rhus coriaria increases protein ubiquitination, proteasomal degradation and triggers noncanonical Beclin-1-independent autophagy and apoptotic cell death in colon cancer cells. Sci Rep 7:11633. https://doi.org/10.1038/s41598-017-11202-3.
   PubMedGoogle Scholar