SARS-CoV-2 egress from Vero cells: a morphological approach.
Coronavirus egress
Coronavirus infection
Electron microscopy
SARS-CoV-2
Virus-cell interactions
Journal
Histochemistry and cell biology
ISSN: 1432-119X
Titre abrégé: Histochem Cell Biol
Pays: Germany
ID NLM: 9506663
Informations de publication
Date de publication:
22 Sep 2023
22 Sep 2023
Historique:
accepted:
07
09
2023
medline:
22
9
2023
pubmed:
22
9
2023
entrez:
22
9
2023
Statut:
aheadofprint
Résumé
Despite being extensively studied because of the current coronavirus disease 2019 (COVID-19) pandemic, severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) interactions with mammalian cells are still poorly understood. Furthermore, little is known about this coronavirus cycle within the host cells, particularly the steps that lead to viral egress. This study aimed to shed light on the morphological features of SARS-CoV-2 egress by utilizing transmission and high-resolution scanning electron microscopy, along with serial electron tomography, to describe the route of nascent virions towards the extracellular medium. Electron microscopy revealed that the clusters of viruses in the paracellular space did not seem to result from collective virus release. Instead, virus accumulation was observed on incurved areas of the cell surface, with egress primarily occurring through individual vesicles. Additionally, our findings showed that the emission of long membrane projections, which could facilitate virus surfing in Vero cells infected with SARS-CoV-2, was also observed in non-infected cultures, suggesting that these are constitutive events in this cell lineage.
Identifiants
pubmed: 37736815
doi: 10.1007/s00418-023-02239-9
pii: 10.1007/s00418-023-02239-9
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Fundação Carlos Chagas Filho de Amparo à Pesquisa do Estado do Rio de Janeiro - FAPERJ
ID : E-26/010.000978/2019
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Alsaadi EJA, Jones IM (2019) Membrane binding proteins of coronaviruses. Future Virol 14(4):275–286
doi: 10.2217/fvl-2018-0144
Barreto-Vieira DF, da Silva MAN, Garcia CC et al (2021) Morphology and morphogenesis of SARS-CoV-2 in Vero-E6 cells. Mem Inst Oswaldo Cruz 116:e200443
Barreto-Vieira DF, da Silva MAN, de Almeida ALT et al (2022) SARS-CoV-2: ultrastructural characterization of morphogenesis in an in vitro system. Viruses 14(2):201
doi: 10.3390/v14020201
pubmed: 35215794
pmcid: 8879486
Baselga M, Moreo E, Uranga-Murillo I, Arias M, Junquera C (2023) Ultrastructural analysis and three-dimensional reconstruction of cellular structures involved in SARS-CoV-2 spread. Histochem Cell Biol 159(1):47–60
doi: 10.1007/s00418-022-02152-7
pubmed: 36175690
Blanchard E, Roingeard P et al (2015) Virus-induced double-membrane vesicles. Cell Microbiol 17:45–50
doi: 10.1111/cmi.12372
pubmed: 25287059
Caldas LA, Carneiro FA, Higa LM et al (2020) Ultrastructural analysis of SARS-CoV-2 interactions with the host cell via high resolution scanning electron microscopy. Sci Rep 10(1):16099
doi: 10.1038/s41598-020-73162-5
pubmed: 32999356
pmcid: 7528159
Caldas LA, Carneiro FA, Monteiro FL et al (2021) Intracellular host cell membrane remodelling induced by SARS-CoV-2 infection in vitro. Biol Cell 113(6):281–293
doi: 10.1111/boc.202000146
pubmed: 33600624
pmcid: 8013410
Chen D, Zheng Q, Sun L et al (2021) ORF3a of SARS-CoV-2 promotes lysosomal exocytosis-mediated viral egress. Dev Cell S1534–5807(21):00807–00808
Ducatelle R, Hoorens J (1984) Significance of lysosomes in the morphogenesis of coronaviruses. Arch Virol 79:1–12
doi: 10.1007/BF01314299
pubmed: 6320768
pmcid: 7086738
Eymieux S, Uzbekov R, Rouillé Y et al (2021a) Secretory vesicles are the principal means of SARS-CoV-2 egress. Cells 10(8):2047
doi: 10.3390/cells10082047
pubmed: 34440816
pmcid: 8393858
Eymieux S, Rouillé Y, Terrier O et al (2021b) Ultrastructural modifications induced by SARS-CoV-2 in Vero cells: a kinetic analysis of viral factory formation, viral particle morphogenesis and virion release. Cell Mol Life Sci 78(7):3565–3576
doi: 10.1007/s00018-020-03745-y
pubmed: 33449149
pmcid: 7809227
Ghosh S, Dellibovi-Ragheb TA, Kerviel A et al (2020) β-Coronaviruses use lysosomes for egress instead of the biosynthetic secretory pathway. Cell 183(6):1520-1535.e14
doi: 10.1016/j.cell.2020.10.039
pubmed: 33157038
pmcid: 7590812
Kim JM, Chung YS, Jo HJ et al (2020) Identification of coronavirus isolated from a patient in Korea with COVID-19. Osong Public Health Res Perspect 11(1):3–7
Klein S, Cortese M, Winter SL et al (2019) SARS-CoV-2 structure and replication characterized by in situ cryo-electron tomography. Nat Commun 11(1):5885
doi: 10.1038/s41467-020-19619-7
Kloc M, Uosef A, Wosik J, Kubiak JZ, Ghobrial RM (2022) Virus interactions with the actin cytoskeleton-what we know and do not know about SARS-CoV-2. Arch Virol 167(3):737–749
doi: 10.1007/s00705-022-05366-1
pubmed: 35102456
pmcid: 8803281
Kopek BG, Perkins G, Miller DJ, Ellisman MH, Ahlquist P (2007) Three-dimensional analysis of a viral RNA replication complex reveals a virus-induced mini-organelle. PLoS Biol 5(9):e220
doi: 10.1371/journal.pbio.0050220
pubmed: 17696647
pmcid: 1945040
Lehmann MJ, Sherer NM, Marks CB et al (2005) Actin and myosin driven movement of viruses along filopodia precedes their entry into cells. J Cell Biol 170:317–325. https://doi.org/10.1083/jcb.200503059
doi: 10.1083/jcb.200503059
pubmed: 16027225
pmcid: 2171413
Lu R, Zhao X, Li J et al (2020) Genomic characterisation and epidemiology of 2019 novel coronavirus: implications for virus origins and receptor binding. Lancet 395(10224):565–574
doi: 10.1016/S0140-6736(20)30251-8
pubmed: 32007145
pmcid: 7159086
Mendonça L, Howe A, Gilchrist JB et al (2021) Correlative multi-scale cryo-imaging unveils SARS-CoV-2 assembly and egress. Nat Commun 12(1):4629
doi: 10.1038/s41467-021-24887-y
pubmed: 34330917
pmcid: 8324836
Park WB, Kwon NJ, Choi SJ et al (2020) Virus isolation from the first patient with SARS-CoV-2 in Korea. J Korean Med Sci 35(7):e84
Pepe A, Pietropaoli S, Vos M et al (2022) Tunneling nanotubes provide a route for SARS-CoV-2 spreading. Sci Adv 8(29):eabo171
doi: 10.1126/sciadv.abo0171
Perlman S, Netland J (2009) Coronaviruses post-SARS: update on replication and pathogenesis. Nat Rev Microbiol 7:439–450
doi: 10.1038/nrmicro2147
pubmed: 19430490
pmcid: 2830095
Pinto AL, Rai RK, Brown JC et al (2022) Ultrastructural insight into SARS-CoV-2 entry and budding in human airway epithelium. Nat Commun 13(1):1609
doi: 10.1038/s41467-022-29255-y
pubmed: 35338134
pmcid: 8956608
Pu J, Guardia CM, Keren-Kaplan T, Bonifacino JS (2016) Mechanisms and functions of lysosome positioning. J Cell Sci 129:4329–4339
pubmed: 27799357
pmcid: 5201012
Qian Z, Travanty EA, Oko L et al (2013) Innate immune response of human alveolar type II cells infected with severe acute respiratory syndrome-coronavirus. Am J Respir Cell Mol Biol 48:742–748
doi: 10.1165/rcmb.2012-0339OC
pubmed: 23418343
pmcid: 3727876
Qinfen Z, Jinming C, Xiaojun H et al (2004) The life cycle of SARS coronavirus in Vero E6 cells. J Med Virol 73(3):332–337
doi: 10.1002/jmv.20095
pubmed: 15170625
pmcid: 7166737
Saraste J, Enyioko M, Dale H et al (2022) Evidence for the role of Rab11-positive recycling endosomes as intermediates in coronavirus egress from epithelial cells. Histochem Cell Biol 158(3):241–251
doi: 10.1007/s00418-022-02115-y
pubmed: 35604431
pmcid: 9124743
Scherer KM, Mascheroni L, Carnell GW et al (2022) SARS-CoV-2 nucleocapsid protein adheres to replication organelles before viral assembly at the Golgi/ERGIC and lysosome-mediated egress. Sci Adv 8(1):eabl4895
doi: 10.1126/sciadv.abl4895
pubmed: 34995113
Snijder EJ, Limpens RWAL, de Wilde AH et al (2020) A unifying structural and functional model of the coronavirus replication organelle: tracking down RNA synthesis. PLoS Biol 18:1–25
doi: 10.1371/journal.pbio.3000715
Sylwester A, Murphy S, Shutt D et al (1997) HIV-induced T cell syncytia are self-perpetuating and the primary cause of T cell death in culture. J Immunol 158(8):3996–4007
doi: 10.4049/jimmunol.158.8.3996
pubmed: 9103471
Wolff G, Limpens R, Zevenhoven-Dobbe JC (2020a) A molecular pore spans the double membrane of the coronavirus replication organelle. Science 369(6509):1395–1398
doi: 10.1126/science.abd3629
pubmed: 32763915
pmcid: 7665310
Wolff G, Melia CE, Snijder EJ, Bárcena M (2020b) Double-membrane vesicles as platforms for viral replication. Trends Microbiol 28(12):1022–1033
doi: 10.1016/j.tim.2020.05.009
pubmed: 32536523
pmcid: 7289118
Zhang J, Lan Y, Sanyal S (2020) Membrane heist: Coronavirus host membrane remodeling during replication. Biochimie 179:229–236
doi: 10.1016/j.biochi.2020.10.010
pubmed: 33115667
pmcid: 7585727
Zhou X, Cong Y, Veenendaal T et al (2017) Ultrastructural characterization of membrane rearrangements induced by porcine epidemic diarrhea virus infection. Viruses 9(9):251
doi: 10.3390/v9090251
pubmed: 28872588
pmcid: 5618017