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SARS-CoV-2 envelope protein and its relationship to the membrane protein

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Pages 128-150 | Received 16 Dec 2022, Accepted 24 Aug 2023, Published online: 19 Oct 2023

References

  • Huang Y, Yang C, Xu X, et al. Structural and functional properties of SARS-CoV-2 spike protein: potential antivirus drug development for COVID-19. Acta Pharmacol Sin. 2020;41:1141–1149. doi:10.1038/s41401-020-0485-4
  • Benton DJ, Wrobel AG, Xu P, et al. Receptor binding and priming of the spike protein of SARS-CoV-2 for membrane fusion. Nature. 2020;588:327–330. doi:10.1038/s41586-020-2772-0
  • Li W, Moore MJ, Vasilieva N, et al. Angiotensin-converting enzyme 2 is a functional receptor for the SARS coronavirus. Nature. 2003;426:450–454. doi:10.1038/nature02145
  • Tan CW, Chia WN, Qin X, et al. A SARS-CoV-2 surrogate virus neutralization test based on antibody-mediated blockage of ACE2–spike protein–protein interaction. Nat Biotechnol. 2020;38:1073–1078. doi:10.1038/s41587-020-0631-z
  • Chang C, Hou M-H, Chang C-F, et al. The SARS coronavirus nucleocapsid protein – forms and functions. Antiviral Res. 2014;103:39–50. doi:10.1016/j.antiviral.2013.12.009
  • McBride R, van Zyl M, Fielding B. The coronavirus nucleocapsid is a multifunctional protein. Viruses. 2014;6:2991–3018. doi:10.3390/v6082991
  • Surjit M, Liu B, Kumar P, et al. The nucleocapsid protein of the SARS coronavirus is capable of self-association through a C-terminal 209 amino acid interaction domain. Biochem Biophys Res Commun. 2004;317:1030–1036. doi:10.1016/j.bbrc.2004.03.154
  • Lu S, Ye Q, Singh D, et al. The SARS-CoV-2 nucleocapsid phosphoprotein forms mutually exclusive condensates with RNA and the membrane-associated M protein. Nat Commun. 2021;12:502. doi:10.1038/s41467-020-20768-y
  • He R, Leeson A, Ballantine M, et al. Characterization of protein–protein interactions between the nucleocapsid protein and membrane protein of the SARS coronavirus. Virus Res. 2004;105:121–125. doi:10.1016/j.virusres.2004.05.002
  • Khan A, Tahir Khan M, Saleem S, et al. Structural insights into the mechanism of RNA recognition by the N-terminal RNA-binding domain of the SARS-CoV-2 nucleocapsid phosphoprotein. Comput Struct Biotechnol J. 2020;18:2174–2184. doi:10.1016/j.csbj.2020.08.006
  • Kippes O, Thorn A, Santoni G. Structural biology of SARS-CoV-2 nucleocapsid. Crystall Rev. 2022;28:21–38. doi:10.1080/0889311X.2022.2072835
  • Kumar S, Saxena SK. Structural and molecular perspectives of SARS-CoV-2. Methods. 2021;195:23–28. doi:10.1016/j.ymeth.2021.03.007
  • Pezeshkian W, Grünewald F, Narykov O, et al. Molecular architecture and dynamics of SARS-CoV-2 envelope by integrative modeling. Structure. 2023;31:492–503.e7. doi:10.1016/j.str.2023.02.006
  • Nieto-Torres JL, Verdiá-Báguena C, Jimenez-Guardeño JM, et al. Severe acute respiratory syndrome coronavirus E protein transports calcium ions and activates the NLRP3 inflammasome. Virology. 2015;485:330–339. doi:10.1016/j.virol.2015.08.010
  • De Maio F, Lo Cascio E, Babini G, et al. Improved binding of SARS-CoV-2 envelope protein to tight junction-associated PALS1 could play a key role in COVID-19 pathogenesis. Microbes Infect. 2020;22:592–597. doi:10.1016/j.micinf.2020.08.006
  • DeDiego ML, Nieto-Torres JL, Jiménez-Guardeño JM, et al. Severe acute respiratory syndrome coronavirus envelope protein regulates cell stress response and apoptosis. PLoS Pathog. 2011;7:e1002315. doi:10.1371/journal.ppat.1002315
  • Vann KR, Acharya A, Jang SM, et al. Binding of the SARS-CoV-2 envelope E protein to human BRD4 is essential for infection. Structure. 2022;30:1224–1232.e5. doi:10.1016/j.str.2022.05.020
  • Vennema H, Godeke GJ, Rossen JW, et al. Nucleocapsid-independent assembly of coronavirus-like particles by co-expression of viral envelope protein genes. EMBO J. 1996;15:2020–2028. doi:10.1002/j.1460-2075.1996.tb00553.x
  • de Haan CAM, Rottier PJM. Molecular interactions in the assembly of coronaviruses. Advances in virus research [Internet]. Elsevier; 2005 [cited 2022 Dec 5]. p. 165–230. Available from: https://linkinghub.elsevier.com/retrieve/pii/S0065352705640067
  • Sui L, Zhao Y, Wang W, et al. SARS-CoV-2 membrane protein inhibits type I interferon production through ubiquitin-mediated degradation of TBK1. Front Immunol. 2021;12:662989. doi:10.3389/fimmu.2021.662989
  • Rahimi A, Mirzazadeh A, Tavakolpour S. Genetics and genomics of SARS-CoV-2: a review of the literature with the special focus on genetic diversity and SARS-CoV-2 genome detection. Genomics. 2021;113:1221–1232. doi:10.1016/j.ygeno.2020.09.059
  • Somberg NH, Wu WW, Medeiros-Silva J, et al. SARS-CoV-2 envelope protein forms clustered pentamers in lipid bilayers. Biochemistry. 2022;61:2280–2294. doi:10.1021/acs.biochem.2c00464
  • Surya W, Li Y, Torres J. Structural model of the SARS coronavirus E channel in LMPG micelles. Biochimica et Biophysica Acta (BBA) – Biomembranes. 2018;1860:1309–1317. doi:10.1016/j.bbamem.2018.02.017
  • Tomasello G, Armenia I, Molla G. The protein imager: a full-featured online molecular viewer interface with server-side HQ-rendering capabilities. Bioinformatics. 2020;36:2909–2911. doi:10.1093/bioinformatics/btaa009
  • Schrödinger LLC. The PyMOL molecular graphics system, Version 2.3. 2019.
  • Neuman BW, Kiss G, Kunding AH, et al. A structural analysis of M protein in coronavirus assembly and morphology. J Struct Biol. 2011;174:11–22. doi:10.1016/j.jsb.2010.11.021
  • Mahtarin R, Islam S, MdJ I, et al. Structure and dynamics of membrane protein in SARS-CoV-2. J Biomol Struct Dyn. 2022;40:4725–4738. doi:10.1080/07391102.2020.1861983
  • Heffron AS, McIlwain SJ, Amjadi MF, et al. The landscape of antibody binding in SARS-CoV-2 infection. Plos Biol. 2021;19:e3001265. doi:10.1371/journal.pbio.3001265
  • Sarkar M, Saha S. Structural insight into the role of novel SARS-CoV-2 E protein: a potential target for vaccine development and other therapeutic strategies. PLoS One. 2020;15:e0237300.
  • Westerbeck JW, Machamer CE. A coronavirus E protein is present in two distinct pools with different effects on assembly and the secretory pathway. J Virol. 2015;89:9313–9323. doi:10.1128/JVI.01237-15
  • Ortego J, Ceriani JE, Patiño C, et al. Absence of E protein arrests transmissible gastroenteritis coronavirus maturation in the secretory pathway. Virology. 2007;368:296–308. doi:10.1016/j.virol.2007.05.032
  • Venkatagopalan P, Daskalova SM, Lopez LA, et al. Coronavirus envelope (E) protein remains at the site of assembly. Virology. 2015;478:75–85. doi:10.1016/j.virol.2015.02.005
  • DeDiego ML, Alvarez E, Almazán F, et al. A severe acute respiratory syndrome coronavirus that lacks the E gene is attenuated in vitro and in vivo. J Virol. 2007;81:1701–1713. doi:10.1128/JVI.01467-06
  • Ghosh S, Dellibovi-Ragheb TA, Kerviel A, et al. β-Coronaviruses use lysosomes for egress instead of the biosynthetic secretory pathway. Cell. 2020;183:1520–1535.e14. doi:10.1016/j.cell.2020.10.039
  • Ruch TR, Machamer CE. The coronavirus E protein: assembly and beyond. Viruses. 2012;4:363–382. doi:10.3390/v4030363
  • Mehregan A, Pérez-Conesa S, Zhuang Y, et al. Probing effects of the SARS-CoV-2 E protein on membrane curvature and intracellular calcium. Biochimica et Biophysica Acta (BBA) – Biomembranes. 2022;1864:183994. doi:10.1016/j.bbamem.2022.183994
  • Kuo L, Masters PS. The small envelope protein E is not essential for murine coronavirus replication. J Virol. 2003;77:4597–4608. doi:10.1128/JVI.77.8.4597-4608.2003
  • Schoeman D, Fielding BC. Coronavirus envelope protein: current knowledge. Virol J. 2019;16:69. doi:10.1186/s12985-019-1182-0
  • Scherer KM, Mascheroni L, Carnell GW, et al. SARS-CoV-2 nucleocapsid protein adheres to replication organelles before viral assembly at the Golgi/ERGIC and lysosome-mediated egress. Sci Adv. 2022;8:eabl4895. doi:10.1126/sciadv.abl4895
  • De Haan CAM, Vennema H, Rottier PJM. Assembly of the coronavirus envelope: homotypic interactions between the M proteins. J Virol. 2000;74:4967–4978. doi:10.1128/JVI.74.11.4967-4978.2000
  • Zhang Z, Nomura N, Muramoto Y, et al. Structure of SARS-CoV-2 membrane protein essential for virus assembly. Nat Commun. 2022;13:4399. doi:10.1038/s41467-022-32019-3
  • Mandala VS, McKay MJ, Shcherbakov AA, et al. Structure and drug binding of the SARS-CoV-2 envelope protein transmembrane domain in lipid bilayers. Nat Struct Mol Biol. 2020;27:1202–1208. doi:10.1038/s41594-020-00536-8
  • Li Y, Surya W, Claudine S, et al. Structure of a conserved Golgi complex-targeting signal in coronavirus envelope proteins. J Biol Chem. 2014;289:12535–12549. doi:10.1074/jbc.M114.560094
  • Yi Z, Ling Y, Zhang X, et al. Functional mapping of B-cell linear epitopes of SARS-CoV-2 in COVID-19 convalescent population. Emerg Microbes Infect. 2020;9:1988–1996. doi:10.1080/22221751.2020.1815591
  • Javorsky A, Humbert PO, Kvansakul M. Structural basis of coronavirus E protein interactions with human PALS1 PDZ domain. Commun Biol. 2021;4:724. doi:10.1038/s42003-021-02250-7
  • Zhu Y, Alvarez F, Wolff N, et al. Interactions of severe acute respiratory syndrome coronavirus 2 protein E With cell junctions and polarity PSD-95/Dlg/ZO-1-containing proteins. Front Microbiol. 2022;13:829094. doi:10.3389/fmicb.2022.829094
  • Chai J, Cai Y, Pang C, et al. Structural basis for SARS-CoV-2 envelope protein recognition of human cell junction protein PALS1. Nat Commun. 2021;12:3433. doi:10.1038/s41467-021-23533-x
  • Teoh K-T, Siu Y-L, Chan W-L, et al. The SARS coronavirus E protein interacts with PALS1 and alters tight junction formation and epithelial morphogenesis. Mol Biol Cell. 2010;21:3838–3852. doi:10.1091/mbc.e10-04-0338
  • Duart G, García-Murria MJ, Mingarro I. The SARS-CoV-2 envelope (E) protein has evolved towards membrane topology robustness. Biochimica et Biophysica Acta (BBA) – Biomembranes. 2021;1863:183608. doi:10.1016/j.bbamem.2021.183608
  • Rahman MS, Hoque MN, Islam MR, et al. Mutational insights into the envelope protein of SARS-CoV-2. Gene Reports. 2021;22:100997. doi:10.1016/j.genrep.2020.100997
  • Corse E, Machamer CE. Infectious bronchitis virus E protein is targeted to the Golgi complex and directs release of virus-like particles. J Virol. 2000;74:4319–4326. doi:10.1128/JVI.74.9.4319-4326.2000
  • Raamsman MJ, Locker JK, de Hooge A, et al. Characterization of the coronavirus mouse hepatitis virus strain A59 small membrane protein E. J Virol. 2000;74:2333–2342. doi:10.1128/JVI.74.5.2333-2342.2000
  • Yuan Q, Liao Y, Torres J, et al. Biochemical evidence for the presence of mixed membrane topologies of the severe acute respiratory syndrome coronavirus envelope protein expressed in mammalian cells. FEBS Lett. 2006;580:3192–3200. doi:10.1016/j.febslet.2006.04.076
  • Maeda J, Repass JF, Maeda A, et al. Membrane topology of coronavirus E protein. Virology. 2001;281:163–169. doi:10.1006/viro.2001.0818
  • Godet M, L’Haridon R, Vautherot J-F, et al. TGEV corona virus ORF4 encodes a membrane protein that is incorporated into virions. Virology. 1992;188:666–675. doi:10.1016/0042-6822(92)90521-P
  • Curtis KM, Yount B, Baric RS. Heterologous gene expression from transmissible gastroenteritis virus replicon particles. J Virol. 2002;76:1422–1434. doi:10.1128/JVI.76.3.1422-1434.2002
  • Duart G, García-Murria MJ, Grau B, et al. SARS-CoV-2 envelope protein topology in eukaryotic membranes. Open Biol. 2020;10:200209. doi:10.1098/rsob.200209
  • Verdiá-Báguena C, Nieto-Torres JL, Alcaraz A, et al. Coronavirus E protein forms ion channels with functionally and structurally-involved membrane lipids. Virology. 2012;432:485–494. doi:10.1016/j.virol.2012.07.005
  • Dolan KA, Dutta M, Kern DM, et al. Structure of SARS-CoV-2 M protein in lipid nanodiscs [Internet]. bioRxiv; 2022 [cited 2022 Jul 22]. p. 2022.06.12.495841. Available from: https://www.biorxiv.org/content/10.11012022.06.12.495841v1.
  • Liu J, Sun Y, Qi J, et al. The membrane protein of severe acute respiratory syndrome coronavirus acts as a dominant immunogen revealed by a clustering region of novel functionally and structurally defined cytotoxic T-lymphocyte epitopes. J Infect Dis. 2010;202:1171–1180. doi:10.1086/656315
  • Zhang Z, Ohto U, Shimizu T. SARS-CoV-2 M protein dimer (short form) in complex with YN7717_9 Fab [Internet]. PDB; 2021. Available from: doi:10.2210/pdb7vgs/pdb
  • Zhang Z, Ohto U, Shimizu T. SARS-CoV-2 M protein dimer (long form) in complex with YN7756_1 Fab [Internet]. PDB; 2021. Available from: doi:10.2210/pdb7vgr/pdb
  • Arndt AL, Larson BJ, Hogue BG. A conserved domain in the coronavirus membrane protein tail is important for virus assembly. J Virol. 2010;84:11418–11428. doi:10.1128/JVI.01131-10
  • Boscarino JA, Logan HL, Lacny JJ, et al. Envelope protein palmitoylations are crucial for murine coronavirus assembly. J Virol. 2008;82:2989–2999. doi:10.1128/JVI.01906-07
  • Dawood AA. Glycosylation, ligand binding sites and antigenic variations between membrane glycoprotein of COVID-19 and related coronaviruses. Vacunas. 2021;22:1–9. doi:10.1016/j.vacun.2020.09.005
  • Shajahan A, Pepi LE, Rouhani DS, et al. Glycosylation of SARS-CoV-2: structural and functional insights. Anal Bioanal Chem. 2021;413:7179–7193. doi:10.1007/s00216-021-03499-x
  • Álvarez E, DeDiego ML, Nieto-Torres JL, et al. The envelope protein of severe acute respiratory syndrome coronavirus interacts with the non-structural protein 3 and is ubiquitinated. Virology. 2010;402:281–291. doi:10.1016/j.virol.2010.03.015
  • Lei J, Kusov Y, Hilgenfeld R. Nsp3 of coronaviruses: structures and functions of a large multi-domain protein. Antiviral Res. 2018;149:58. doi:10.1016/j.antiviral.2017.11.001
  • Bessa LM, Guseva S, Camacho-Zarco AR, et al. The intrinsically disordered SARS-CoV-2 nucleoprotein in dynamic complex with its viral partner nsp3a. Sci Adv. 2022;8:eabm4034. doi:10.1126/sciadv.abm4034
  • Li S, Zandi R. Biophysical modeling of SARS-CoV-2 assembly: genome condensation and budding. Viruses. 2022;14:2089. doi:10.3390/v14102089
  • Collins LT, Elkholy T, Mubin S, et al. Elucidation of SARS-Cov-2 budding mechanisms through molecular dynamics simulations of M and E protein complexes. J Phys Chem Lett. 2021;12:12249–12255. doi:10.1021/acs.jpclett.1c02955
  • Cao Y, Yang R, Wang W, et al. Probing the formation, structure and free energy relationships of M protein dimers of SARS-CoV-2. Comput Struct Biotechnol J. 2022;20:573–582. doi:10.1016/j.csbj.2022.01.007
  • Kumar P, Kumar A, Garg N, et al. An insight into SARS-CoV-2 membrane protein interaction with spike, envelope, and nucleocapsid proteins. J Biomol Struct Dyn. 2021;41:1062–1071. doi:10.1080/07391102.2021.2016490
  • Yang Y, Xiong Z, Zhang S, et al. Bcl-xL inhibits T-cell apoptosis induced by expression of SARS coronavirus E protein in the absence of growth factors. Biochem J. 2005;392:135–143. doi:10.1042/BJ20050698
  • Jimenez-Guardeño JM, Nieto-Torres JL, DeDiego ML, et al. The PDZ-binding motif of severe acute respiratory syndrome coronavirus envelope protein Is a determinant of viral pathogenesis. PLOS Pathog. 2014;10:e1004320. doi:10.1371/journal.ppat.1004320
  • Ruch TR, Machamer CE. The hydrophobic domain of infectious bronchitis virus E protein alters the host secretory pathway and is important for release of infectious virus. J Virol. 2011;85:675–685. doi:10.1128/JVI.01570-10
  • Lu W, Zheng B-J, Xu K, et al. Severe acute respiratory syndrome-associated coronavirus 3a protein forms an ion channel and modulates virus release. Proc Natl Acad Sci USA. 2006;103:12540–12545. doi:10.1073/pnas.0605402103
  • An S, Chen C-J, Yu X, et al. Induction of apoptosis in murine coronavirus-infected cultured cells and demonstration of E protein as an apoptosis inducer. J Virol. 1999;73:7853–7859. doi:10.1128/JVI.73.9.7853-7859.1999
  • Mills RJ, Humphrey SJ, Fortuna PRJ, et al. BET inhibition blocks inflammation-induced cardiac dysfunction and SARS-CoV-2 infection. Cell. 2021;184:2167–2182.e22. doi:10.1016/j.cell.2021.03.026
  • Wilson L, Gage P, Ewart G. Hexamethylene amiloride blocks E protein ion channels and inhibits coronavirus replication. Virology. 2006;353:294–306. doi:10.1016/j.virol.2006.05.028
  • Torres J, Maheswari U, Parthasarathy K, et al. Conductance and amantadine binding of a pore formed by a lysine-flanked transmembrane domain of SARS coronavirus envelope protein. Protein Sci. 2007;16:2065–2071. doi:10.1110/ps.062730007
  • Nieto-Torres JL, DeDiego ML, Verdiá-Báguena C, et al. Severe acute respiratory syndrome coronavirus envelope protein Ion channel activity promotes virus fitness and pathogenesis. PLOS Pathog. 2014;10:e1004077. doi:10.1371/journal.ppat.1004077
  • Ortego J, Escors D, Laude H, et al. Generation of a replication-competent, propagation-deficient virus vector based on the transmissible gastroenteritis coronavirus genome. J Virol. 2002;76:11518–11529. doi:10.1128/JVI.76.22.11518-11529.2002
  • Keller MD, Harris KM, Jensen-Wachspress MA, et al. SARS-CoV-2–specific T cells are rapidly expanded for therapeutic use and target conserved regions of the membrane protein. Blood. 2020;136:2905–2917. doi:10.1182/blood.2020008488
  • Khan FI, Kang T, Ali H, et al. Remdesivir strongly binds to RNA-dependent RNA polymerase, membrane protein, and main protease of SARS-CoV-2: indication from molecular modeling and simulations. Frontiers in Pharmacology [Internet]. 2021 [cited 2022 Jul 22];12. Available from: https://www.frontiersin.org/articles/10.3389fphar.2021.710778.
  • Ghosh A, Bhattacharyya D, Bhunia A. Structural insights of a self-assembling 9-residue peptide from the C-terminal tail of the SARS corona virus E-protein in DPC and SDS micelles: A combined high and low resolution spectroscopic study. Biochimica et Biophysica Acta (BBA) – Biomembranes. 2018;1860:335–346. doi:10.1016/j.bbamem.2017.10.015
  • Hurst KR, Koetzner CA, Masters PS. Characterization of a critical interaction between the coronavirus nucleocapsid protein and nonstructural protein 3 of the viral replicase-transcriptase complex. J Virol. 2013;87:9159–9172. doi:doi:10.1128/JVI.01275-13

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