Protein disulfide isomerases (PDIs) negatively regulate ebolavirus structural glycoprotein expression in the endoplasmic reticulum (ER) via the autophagy-lysosomal pathway

References

• Feldmann H, Sprecher A, Geisbert TW. Ebola. N Engl J Med. 2020;382(19):1832–1842.
   PubMed Web of Science ®Google Scholar
• Hoenen T, Groseth A, Feldmann H. Therapeutic strategies to target the Ebola virus life cycle. Nat Rev Microbiol. 2019;17(10):593–606.
   PubMed Web of Science ®Google Scholar
• Geisbert TW. Marburg and ebola hemorrhagic fevers (filoviruses). Mandell, Douglas, and Bennett’s principles and practice of infectious diseases. 2015 1995–9.e1.
   Google Scholar
• Francica JR, Matukonis MK, Bates P. Requirements for cell rounding and surface protein down-regulation by Ebola virus glycoprotein. Virology. 2009;383(2):237–247.
   PubMed Web of Science ®Google Scholar
• Francica JR, Varela-Rohena A, Medvec A, et al. Steric shielding of surface epitopes and impaired immune recognition induced by the ebola virus glycoprotein. PLoS Pathog. 2010;6(9):e1001098.
   PubMed Web of Science ®Google Scholar
• Simmons G, Wool-Lewis RJ, Baribaud F, et al. Ebola virus glycoproteins induce global surface protein down-modulation and loss of cell adherence. J Virol. 2002;76(5):2518–2528.
   PubMed Web of Science ®Google Scholar
• Sullivan NJ, Geisbert TW, Geisbert JB, et al. Immune protection of nonhuman primates against ebola virus with single low-dose adenovirus vectors encoding modified GPs. PLoS Med. 2006;3(6):e177.
   PubMed Web of Science ®Google Scholar
• Takada A, Watanabe S, Ito H, et al. Downregulation of beta1 integrins by Ebola virus glycoprotein: implication for virus entry. Virology. 2000;278(1):20–26.
   PubMed Web of Science ®Google Scholar
• Yang ZY, Duckers HJ, Sullivan NJ, et al. Identification of the Ebola virus glycoprotein as the main viral determinant of vascular cell cytotoxicity and injury. Nat Med. 2000;6(8):886–889.
   PubMed Web of Science ®Google Scholar
• Hacke M, Bjorkholm P, Hellwig A, et al. Inhibition of Ebola virus glycoprotein-mediated cytotoxicity by targeting its transmembrane domain and cholesterol. Nat Commun. 2015;6(1):7688.
   PubMedGoogle Scholar
• Alazard-Dany N, Volchkova V, Reynard O, et al. Ebola virus glycoprotein GP is not cytotoxic when expressed constitutively at a moderate level. J Gen Virol. 2006;87(5):1247–1257.
   PubMedGoogle Scholar
• Volchkov VE, Volchkova VA, Muhlberger E, et al. Recovery of infectious Ebola virus from complementary DNA: RNA editing of the GP gene and viral cytotoxicity. Science. 2001;291(5510):1965–1969.
   PubMed Web of Science ®Google Scholar
• Mehedi M, Falzarano D, Seebach J, et al. A new Ebola virus nonstructural glycoprotein expressed through RNA editing. J Virol. 2011;85(11):5406–5414.
   PubMed Web of Science ®Google Scholar
• Galligan JJ, Petersen DR. The human protein disulfide isomerase gene family. Hum Genomics. 2012;6(1):6.
   PubMedGoogle Scholar
• Kozlov G, Gehring K. Calnexin cycle - structural features of the ER chaperone system. FEBS J. 2020;287(20):4322–4340.
   PubMed Web of Science ®Google Scholar
• Hetz C. The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat Rev Mol Cell Biol. 2012;13(2):89–102.
   PubMed Web of Science ®Google Scholar
• Molinari M. ER-phagy responses in yeast, plants, and mammalian cells and their crosstalk with UPR and ERAD. Dev Cell. 2021;56(7):949–966.
   PubMed Web of Science ®Google Scholar
• Jeffers SA, Sanders DA, Sanchez A. Covalent modifications of the ebola virus glycoprotein. J Virol. 2002;76(24):12463–12472.
   PubMed Web of Science ®Google Scholar
• Chai Q, Li S, Collins MK, et al. HIV-1 Nef interacts with the cyclin K/CDK13 complex to antagonize SERINC5 for optimal viral infectivity. Cell Rep. 2021;36(6):109514.
   PubMed Web of Science ®Google Scholar
• Wang B, Wang Y, Frabutt DA, et al. Mechanistic understanding of N-glycosylation in Ebola virus glycoprotein maturation and function. J Biol Chem. 2017;292(14):5860–5870.
   PubMed Web of Science ®Google Scholar
• Yu C, Li S, Zhang X, et al. MARCH8 inhibits Ebola virus glycoprotein, human immunodeficiency virus type 1 envelope glycoprotein, and avian influenza virus H5N1 hemagglutinin maturation. mBio. 2020;11(5):e01882–20.
   PubMed Web of Science ®Google Scholar
• Hoenen T, Watt A, Mora A, et al. Modeling the lifecycle of Ebola virus under biosafety level 2 conditions with virus-like particles containing tetracistronic minigenomes. J Vis Exp. 2014;91:52381. DOI:10.3791/52381
   PubMed Web of Science ®Google Scholar
• Piacentini S, La Frazia S, Riccio A, et al. Nitazoxanide inhibits paramyxovirus replication by targeting the Fusion protein folding: role of glycoprotein-specific thiol oxidoreductase ERp57. Sci Rep. 2018;8(1):10425.
   PubMedGoogle Scholar
• Wu Y, Swulius MT, Moremen KW, et al. Elucidation of the molecular logic by which misfolded alpha 1-antitrypsin is preferentially selected for degradation. Proc Natl Acad Sci U S A. 2003;100(14):8229–8234.
   PubMed Web of Science ®Google Scholar
• Hebert DN, Molinari M. Flagging and docking: dual roles for N-glycans in protein quality control and cellular proteostasis. Trends Biochem Sci. 2012;37(10):404–410.
   PubMed Web of Science ®Google Scholar
• 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(1):e01690–17.
   PubMed Web of Science ®Google Scholar
• Glick D, Barth S, Macleod KF. Autophagy: cellular and molecular mechanisms. J Pathol. 2010;221(1):3–12.
   PubMed Web of Science ®Google Scholar
• Mizushima N, Yoshimori T, Ohsumi Y. The role of ATG proteins in autophagosome formation. Annu Rev Cell Dev Biol. 2011;27(1):107–132.
   PubMed Web of Science ®Google Scholar
• Grice GL, Nathan JA. The recognition of ubiquitinated proteins by the proteasome. Cell Mol Life Sci. 2016;73(18):3497–3506.
   PubMed Web of Science ®Google Scholar
• Chan SY, Ma MC, Goldsmith MA. Differential induction of cellular detachment by envelope glycoproteins of Marburg and Ebola (Zaire) viruses. J Gen Virol. 2000;81(9):2155–2159.
   PubMedGoogle Scholar
• Hudson DA, Gannon SA, Thorpe C. Oxidative protein folding: from thiol-disulfide exchange reactions to the redox poise of the endoplasmic reticulum. Free Radic Biol Med. 2015;80:171–182.
   PubMed Web of Science ®Google Scholar
• Zhou T, Frabutt DA, Moremen KW, et al. ERManI (endoplasmic reticulum class I alpha-mannosidase) is required for HIV-1 envelope glycoprotein degradation via endoplasmic reticulum-associated protein degradation pathway. J Biol Chem. 2015;290(36):22184–22192.
   PubMed Web of Science ®Google Scholar
• Johansen T, Lamark T. Selective autophagy mediated by autophagic adapter proteins. Autophagy. 2011;7(3):279–296.
   PubMed Web of Science ®Google Scholar
• Hu D, Wang B, Leng Y, et al. Genetic knockout of erp57 gene in host cells inhibits influenza virus replication. Chin J Preventive Vet Med. 2016;38. 429–433.
   Google Scholar
• Liu X, Wang B, Yao X, et al. The role of autophagy-related gene 3 in the assembly process of Ebola virus. Chin J Virol. 2019;35:888–894.
   Google Scholar