Newcastle disease virus degrades SIRT3 via PINK1-PRKN-dependent mitophagy to reprogram energy metabolism in infected cells

References

• Goodwin CM, Xu S, Munger J. Stealing the keys to the kitchen: viral manipulation of the host cell metabolic network. Trends Microbiol. 2015 Dec;23(12):789–798.
   PubMed Web of Science ®Google Scholar
• Fan S, Wu K, Zhao M, et al. LDHB inhibition induces mitophagy and facilitates the progression of CSFV infection. Autophagy. 2020 Sep 28;17(9):1–20
   Web of Science ®Google Scholar
• Sanchez EL, Lagunoff M. Viral activation of cellular metabolism. Virology. 2015 May;479–480:609–618.
   PubMed Web of Science ®Google Scholar
• Thai M, Graham NA, Braas D, et al. Adenovirus E4ORF1-induced MYC activation promotes host cell anabolic glucose metabolism and virus replication. Cell Metab. 2014 Apr 1;19(4):694–701.
   PubMed Web of Science ®Google Scholar
• Thaker SK, Chapa T, Garcia G Jr., et al. Differential metabolic reprogramming by Zika Virus promotes cell death in human versus mosquito cells. Cell Metab. 2019 May 7;29(5):1206–1216 e4.
   PubMed Web of Science ®Google Scholar
• Allonso D, Andrade IS, Conde JN, et al. Dengue Virus NS1 protein modulates cellular energy metabolism by increasing Glyceraldehyde-3-Phosphate dehydrogenase activity. J Virol. 2015 Dec;89(23):11871–11883.
   PubMed Web of Science ®Google Scholar
• Fontaine KA, Sanchez EL, Camarda R, et al. Dengue virus induces and requires glycolysis for optimal replication. J Virol. 2015 Feb;89(4):2358–2366.
   PubMed Web of Science ®Google Scholar
• Zhang J, Jia L, Tsang CM, et al. EBV infection and glucose metabolism in nasopharyngeal carcinoma. Adv Exp Med Biol. 2017;1018:75–90.
   PubMedGoogle Scholar
• Mullen PJ, Garcia G Jr., Purkayastha A, et al. SARS-CoV-2 infection rewires host cell metabolism and is potentially susceptible to mTORC1 inhibition. Nat Commun. 2021 Mar 25;12(1):1876.
   PubMed Web of Science ®Google Scholar
• Codo AC, Davanzo GG, Monteiro LB, et al. Elevated glucose levels favor SARS-CoV-2 infection and monocyte response through a HIF-1alpha/glycolysis-dependent axis. Cell Metab. 2020 Sep 1;32(3):498–499.
   PubMed Web of Science ®Google Scholar
• Sanchez EL, Pulliam TH, Dimaio TA, et al. Glycolysis, glutaminolysis, and fatty acid synthesis are required for distinct stages of Kaposi’s Sarcoma-Associated herpesvirus lytic replication. J Virol. 2017 May 15;91(10):10.
   Web of Science ®Google Scholar
• Thyrsted J, Holm CK. Virus-induced metabolic reprogramming and innate sensing hereof by the infected host. Curr Opin Biotechnol. 2020 Oct;25(68):44–50.
   Google Scholar
• Grasso D, Zampieri LX, Capeloa T, et al. Mitochondria in cancer. Cell Stress. 2020 May 11;4(6):114–146.
   PubMedGoogle Scholar
• Polyakov VY, Soukhomlinova MY, Fais D. Fusion, fragmentation, and fission of mitochondria. Biochemistry (Mosc). 2003 Aug;68(8):838–849.
   PubMed Web of Science ®Google Scholar
• de Brito OM, Scorrano L. Mitofusin 2: a mitochondria-shaping protein with signaling roles beyond fusion. Antioxid Redox Signal. 2008 Mar;10(3):621–633.
   PubMed Web of Science ®Google Scholar
• Khan M, Syed GH, Kim SJ, et al. Mitochondrial dynamics and viral infections: a close nexus. Biochim Biophys Acta. 2015 Oct;1853(10Pt B):2822–2833.
   PubMedGoogle Scholar
• Anderson CM, Macleod KF. Autophagy and cancer cell metabolism. Int Rev Cell Mol Biol. 2019;347:145–190.
   PubMed Web of Science ®Google Scholar
• Jin SM, Youle RJ. PINK1- and Parkin-mediated mitophagy at a glance. J Cell Sci. 2012 Feb 15;125(Pt 4):795–799.
   PubMed Web of Science ®Google Scholar
• Wang L, Cho YL, Tang Y, et al. PTEN-L is a novel protein phosphatase for ubiquitin dephosphorylation to inhibit PINK1-Parkin-mediated mitophagy. Cell Res. 2018 Aug;28(8):787–802.
   PubMed Web of Science ®Google Scholar
• Lin SC, Hardie DG. AMPK: sensing glucose as well as cellular energy status. Cell Metab. 2018 Feb 6;27(2):299–313.
   PubMed Web of Science ®Google Scholar
• Zhang CS, Hawley SA, Zong Y, et al. Fructose-1,6-bisphosphate and aldolase mediate glucose sensing by AMPK. Nature. 2017 Aug 3;548(7665):112–116.
   PubMed Web of Science ®Google Scholar
• Herzig S, Shaw RJ. AMPK: guardian of metabolism and mitochondrial homeostasis. Nat Rev Mol Cell Biol. 2018 Feb;19(2):121–135.
   PubMed Web of Science ®Google Scholar
• Chatel-Chaix L, Cortese M, Romero-Brey I, et al. Dengue Virus Perturbs Mitochondrial Morphodynamics to Dampen Innate Immune Responses. Cell Host Microbe. 2016 Sep 14;20(3):342–356.
   PubMed Web of Science ®Google Scholar
• McWilliams TG, Muqit MM. PINK1 and Parkin: emerging themes in mitochondrial homeostasis. Curr Opin Cell Biol. 2017 Apr;45:83–91.
   PubMed Web of Science ®Google Scholar
• Matsuda N, Tanaka K. Uncovering the roles of PINK1 and parkin in mitophagy. Autophagy. 2010 Oct;6(7):952–954.
   PubMed Web of Science ®Google Scholar
• Avia M, Rojas JM, Miorin L, et al. Virus-induced autophagic degradation of STAT2 as a mechanism for interferon signaling blockade. EMBO Rep. 2019 Nov 5;20(11):e48766.
   PubMed Web of Science ®Google Scholar
• Wang L, Xu C, Johansen T, et al. SIRT1 - a new mammalian substrate of nuclear autophagy. Autophagy. 2021 Feb;17(2):593–595.
   PubMed Web of Science ®Google Scholar
• Xu C, Wang L, Fozouni P, et al. SIRT1 is downregulated by autophagy in senescence and ageing. Nat Cell Biol. 2020 Oct;22(10):1170–1179.
   PubMed Web of Science ®Google Scholar
• Dou Z, Xu C, Donahue G, et al. Autophagy mediates degradation of nuclear lamina. Nature. 2015 Nov 5;527(7576):105–109.
   PubMed Web of Science ®Google Scholar
• Chen YY, Wang WH, Che L, et al. BNIP3L-Dependent mitophagy promotes HBx-Induced cancer stemness of hepatocellular carcinoma cells via glycolysis metabolism reprogramming. Cancers (Basel). 2020 Mar 11;12(3).
   Web of Science ®Google Scholar
• Hirschey MD, Shimazu T, Huang JY, et al. SIRT3 regulates mitochondrial protein acetylation and intermediary metabolism. Cold Spring Harb Symp Quant Biol. 2011;76:267–277.
   PubMedGoogle Scholar
• Alhazzazi TY, Kamarajan P, Verdin E, et al. Sirtuin-3 (SIRT3) and the hallmarks of cancer. Genes Cancer. 2013 Mar;4(3–4):164–171.
   PubMedGoogle Scholar
• Alhazzazi TY, Kamarajan P, Verdin E, et al. SIRT3 and cancer: tumor promoter or suppressor? Biochim Biophys Acta. 2011 Aug;1816(1):80–88.
   PubMed Web of Science ®Google Scholar
• Chalkiadaki A, Guarente L. The multifaceted functions of sirtuins in cancer. Nat Rev Cancer. 2015 Oct;15(10):608–624.
   PubMed Web of Science ®Google Scholar
• Shi T, Wang F, Stieren E, et al. SIRT3, a mitochondrial sirtuin deacetylase, regulates mitochondrial function and thermogenesis in brown adipocytes. J Biol Chem. 2005 Apr 8;280(14):13560–13567.
   PubMed Web of Science ®Google Scholar
• Finley LW, Carracedo A, Lee J, et al. SIRT3 opposes reprogramming of cancer cell metabolism through HIF1alpha destabilization. Cancer Cell. 2011 Mar 8;19(3):416–428.
   PubMed Web of Science ®Google Scholar
• Wang T, Cao Y, Zheng Q, et al. SENP1-Sirt3 signaling controls mitochondrial protein acetylation and metabolism. Mol Cell. 2019 Aug 22;75(4):823–834 e5.
   PubMed Web of Science ®Google Scholar
• Ganar K, Das M, Sinha S, et al. Newcastle disease virus: current status and our understanding. Virus Res. 2014 May;12(184):71–81.
   Google Scholar
• Tayeb S, Zakay-Rones Z, Panet A. Therapeutic potential of oncolytic newcastle disease virus: a critical review. Oncolytic Virother. 2015;4:49–62.
   PubMed Web of Science ®Google Scholar
• Zamarin D, Palese P. Oncolytic newcastle disease virus for cancer therapy: old challenges and new directions. Future Microbiol. 2012 Mar;7(3):347–367.
   PubMed Web of Science ®Google Scholar
• Meng S, Zhou Z, Chen F, et al. Newcastle disease virus induces apoptosis in cisplatin-resistant human lung adenocarcinoma A549 cells in vitro and in vivo. Cancer Lett. 2012 Apr 1;317(1):56–64.
   PubMed Web of Science ®Google Scholar
• Ren S, Ding C, Sun Y. Morphology remodeling and selective autophagy of intracellular organelles during viral infections. Int J Mol Sci. 2020 May 23;21(10):10.
   Web of Science ®Google Scholar
• Li Y, Jiang W, Niu Q, et al. eIF2alpha-CHOP-BCl-2/JNK and IRE1alpha-XBP1/JNK signaling promote apoptosis and inflammation and support the proliferation of newcastle disease virus. Cell Death Dis. 2019 Nov 26;10(12):891.
   PubMedGoogle Scholar
• Cheng JH, Sun YJ, Zhang FQ, et al. Newcastle disease virus NP and P proteins induce autophagy via the endoplasmic reticulum stress-related unfolded protein response. Sci Rep. 2016 Apr;21(6):24721.
   Google Scholar
• Sun Y, Yu S, Ding N, et al. Autophagy benefits the replication of newcastle disease virus in chicken cells and tissues. J Virol. 2014 Jan;88(1):525–537.
   PubMed Web of Science ®Google Scholar
• Santel A, Frank S. Shaping mitochondria: the complex posttranslational regulation of the mitochondrial fission protein DRP1. IUBMB Life. 2008 Jul;60(7):448–455.
   PubMed Web of Science ®Google Scholar
• Yu R, Liu T, Ning C, et al. The phosphorylation status of Ser-637 in dynamin-related protein 1 (Drp1) does not determine Drp1 recruitment to mitochondria. J Biol Chem. 2019 Nov 15;294(46):17262–17277.
   PubMed Web of Science ®Google Scholar
• Spinelli JB, Haigis MC. The multifaceted contributions of mitochondria to cellular metabolism. Nat Cell Biol. 2018 Jul;20(7):745–754.
   PubMed Web of Science ®Google Scholar
• Yu Y, Clippinger AJ, Pierciey FJ Jr., et al. Viruses and metabolism: alterations of glucose and glutamine metabolism mediated by human cytomegalovirus. Adv Virus Res. 2011;80:49–67.
   PubMed Web of Science ®Google Scholar
• Levy P, Bartosch B. Metabolic reprogramming: a hallmark of viral oncogenesis. Oncogene. 2016 Aug 11;35(32):4155–4164.
   PubMed Web of Science ®Google Scholar
• Marin-Hernandez A, Gallardo-Perez JC, Ralph SJ, et al. HIF-1alpha modulates energy metabolism in cancer cells by inducing over-expression of specific glycolytic isoforms. Mini Rev Med Chem. 2009 Aug;9(9):1084–1101.
   PubMed Web of Science ®Google Scholar
• Richardson AL, Wang ZC, De Nicolo A, et al. X chromosomal abnormalities in basal-like human breast cancer. Cancer Cell. 2006 Feb;9(2):121–132.
   PubMed Web of Science ®Google Scholar
• Ren S, Rehman ZU, Shi M, et al. Syncytia generated by hemagglutinin-neuraminidase and fusion proteins of virulent newcastle disease virus induce complete autophagy by activating AMPK-mTORC1-ULK1 signaling>. Vet Microbiol. 2019 Mar;230:283–290.
   PubMed Web of Science ®Google Scholar
• Meng C, Zhou Z, Jiang K, et al. Newcastle disease virus triggers autophagy in U251 glioma cells to enhance virus replication. Arch Virol. 2012 Jun;157(6):1011–1018.
   PubMed Web of Science ®Google Scholar
• Dikic I. Proteasomal and autophagic degradation systems. Annu Rev Biochem. 2017 Jun;20(86):193–224.
   Google Scholar
• Pohl C, Dikic I. Cellular quality control by the ubiquitin-proteasome system and autophagy. Science. 2019 Nov 15;366(6467):818–822.
   PubMed Web of Science ®Google Scholar
• Yoboue ED, Valente EM. PINK1 and Parkin: the odd couple. Neurosci Res. 2020 May 15;159:25–33.
   PubMed Web of Science ®Google Scholar
• Sugiura A, McLelland GL, Fon EA, et al. A new pathway for mitochondrial quality control: mitochondrial-derived vesicles. EMBO J. 2014 Oct 1;33(19):2142–2156.
   PubMed Web of Science ®Google Scholar
• McWilliams TG, Ganley IG. Investigating mitophagy and mitochondrial morphology in vivo using mito-QC: a comprehensive guide. Methods Mol Biol. 2019;1880:621–642.
   PubMedGoogle Scholar
• Zu Y, Chen XF, Li Q, et al. PGC-1alpha activates SIRT3 to modulate cell proliferation and glycolytic metabolism in breast cancer. Neoplasma. 2021 Mar;68(2):352–361.
   PubMed Web of Science ®Google Scholar
• Gladkova C, Maslen SL, Skehel JM, et al. Mechanism of parkin activation by PINK1. Nature. 2018 Jul;559(7714):410–414.
   PubMed Web of Science ®Google Scholar
• Yapa NMB, Lisnyak V, Reljic B, et al. Mitochondrial dynamics in health and disease. FEBS Lett. 2021 Apr;595(8):1184–1204.
   PubMed Web of Science ®Google Scholar
• Vasquez-Trincado C, Garcia-Carvajal I, Pennanen C, et al. Mitochondrial dynamics, mitophagy and cardiovascular disease. J Physiol. 2016 Feb 1;594(3):509–525.
   PubMed Web of Science ®Google Scholar
• Ozawa S, Ueda S, Imamura H, et al. Glycolysis, but not Mitochondria, responsible for intracellular ATP distribution in cortical area of podocytes. Sci Rep. 2015 Dec;18(5):18575.
   Google Scholar
• Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science. 2009 May 22;324(5930):1029–1033.
   PubMed Web of Science ®Google Scholar
• Mahmoudabadi G, Milo R, Phillips R. Energetic cost of building a virus. Proc Natl Acad Sci U S A. 2017 May 30;114(22):E4324–E4333.
   PubMed Web of Science ®Google Scholar
• Seabright AP, Fine NHF, Barlow JP, et al. AMPK activation induces mitophagy and promotes mitochondrial fission while activating TBK1 in a PINK1-Parkin independent manner. FASEB J. 2020 May;34(5):6284–6301.
   PubMed Web of Science ®Google Scholar
• Zhang CS, Lin SC. AMPK promotes autophagy by facilitating mitochondrial fission. Cell Metab. 2016 Mar 8;23(3):399–401.
   PubMed Web of Science ®Google Scholar
• Hu Y, Chen H, Zhang L, et al. The AMPK-MFN2 axis regulates MAM dynamics and autophagy induced by energy stresses. Autophagy. 2021 May;17(5):1142–1156.
   PubMed Web of Science ®Google Scholar
• Sica V, Galluzzi L, Bravo-San Pedro JM, et al. Organelle-specific initiation of autophagy. Mol Cell. 2015 Aug 20;59(4):522–539.
   PubMed Web of Science ®Google Scholar
• Toyama EQ, Herzig S, Courchet J, et al. Metabolism. AMP-activated protein kinase mediates mitochondrial fission in response to energy stress. Science. 2016 Jan 15;351(6270):275–281.
   PubMed Web of Science ®Google Scholar
• Wang X, Shen K, Wang J, et al. Hypoxic preconditioning combined with curcumin promotes cell survival and mitochondrial quality of bone marrow mesenchymal stem cells, and accelerates cutaneous wound healing via PGC-1alpha/SIRT3/HIF-1alpha signaling. Free Radic Biol Med. 2020 Nov 1;159:164–176.
   PubMed Web of Science ®Google Scholar
• Yamada T, Dawson TM, Yanagawa T, et al. SQSTM1/p62 promotes mitochondrial ubiquitination independently of PINK1 and PRKN/parkin in mitophagy. Autophagy. 2019 Nov;15(11):2012–2018.
   PubMed Web of Science ®Google Scholar
• Sun Y, Zheng H, Yu S, et al. Newcastle disease virus v protein degrades mitochondrial antiviral signaling protein to inhibit host Type I interferon production via E3 ubiquitin ligase RNF5. J Virol. 2019 Sep 15;93(18):18.
   Web of Science ®Google Scholar
• Romer-Oberdorfer A, Werner O, Veits J, et al. Contribution of the length of the HN protein and the sequence of the F protein cleavage site to Newcastle disease virus pathogenicity. J Gen Virol. 2003 Nov;84(Pt 11):3121–3129.
   PubMedGoogle Scholar