β-Coronaviruses Use Lysosomes for Egress Instead of the Biosynthetic Secretory Pathway
Sourish Ghosh, Teegan A Dellibovi-Ragheb, Adeline Kerviel, Eowyn Pak, Qi Qiu, Matthew Fisher, Peter M Takvorian, Christopher Bleck, Victor W Hsu, Anthony R Fehr, Stanley Perlman, Sooraj R Achar, Marco R Straus, Gary R Whittaker, Cornelis A M De Haan, John Kehrl, Grégoire Altan-Bonnet, Nihal Altan-Bonnet
Cell, doi:10.1016/j.cell.2020.10.039
b-Coronaviruses are a family of positive-strand enveloped RNA viruses that includes the severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2). Much is known regarding their cellular entry and replication pathways, but their mode of egress remains uncertain. Using imaging methodologies and virus-specific reporters, we demonstrate that b-coronaviruses utilize lysosomal trafficking for egress rather than the biosynthetic secretory pathway more commonly used by other enveloped viruses. This unconventional egress is regulated by the Arf-like small GTPase Arl8b and can be blocked by the Rab7 GTPase competitive inhibitor CID1067700. Such non-lytic release of b-coronaviruses results in lysosome deacidification, inactivation of lysosomal degradation enzymes, and disruption of antigen presentation pathways. b-Coronavirus-induced exploitation of lysosomal organelles for egress provides insights into the cellular and immunological abnormalities observed in patients and suggests new therapeutic modalities.
STAR+METHODS Detailed methods are provided in the online version of this paper and include the following:
DECLARATION OF INTERESTS The authors declare no competing interests. 1 (A) Infected cells were treated with/without BFA at 8 h pi or 10 h pi. Supernatants collected at 14 h pi were reinoculated into new HeLa-mCC1a cells and TCID50/ml was calculated at 72 h .
Continued (legend continued on next page)
References
Agola, Hong, Surviladze, Ursu, Waller et al., A competitive nucleotide binding inhibitor: in vitro characterization of Rab7 GTPase inhibition, ACS Chem. Biol
Aranda-Romo, Garcia-Sepulveda, Comas-Garcı ´a, Lovato-Salas, Salgado-Bustamante et al., Killer-cell immunoglobulin-like receptors (KIR) in severe A (H1N1) 2009 influenza infections, Immunogenetics
Ballabio, Bonifacino, Lysosomes as dynamic regulators of cell and organismal homeostasis, Nat. Rev. Mol. Cell Biol
Boda, L} Orincz, Taka ´ts, Csizmadia, To ´th et al., Drosophila Arl8 is a general positive regulator of lysosomal fusion events, Biochim. Biophys. Acta Mol. Cell Res
Brazill, Caprette, Myler, Hatton, Ammann et al., A protein containing a serine-rich domain with vesicle fusing properties mediates cell cycle-dependent cytosolic pH regulation, J. Biol. Chem
Brown, Goodhouse, Farquhar, Mannose-6-phosphate receptors for lysosomal enzymes cycle between the Golgi complex and endosomes, J. Cell Biol
Bucci, Thomsen, Nicoziani, Mccarthy, Van Deurs, Rab7: a key to lysosome biogenesis, Mol. Biol. Cell
Castan ˜o-Rodriguez, Honrubia, Gutie ´rrez-A ´lvarez, Dediego, Nieto-Torres et al., Role of Severe Acute Respiratory Syndrome Coronavirus Viroporins E, 3a, and 8a in Replication and Pathogenesis, mBio
Catalano, Driscoll, Inhibiting extracellular vesicles formation and release: a review of EV inhibitors, J. Extracell. Vesicles
Channappanavar, Fehr, Vijay, Mack, Zhao et al., Dysregulated Type I Interferon and Inflammatory Monocyte-Macrophage Responses Cause Lethal Pneumonia in SARS-CoV-Infected Mice, Cell Host Microbe
Chen, Du, Hagemeijer, Takvorian, Pau et al., Phosphatidylserine vesicles enable efficient en bloc transmission of enteroviruses, Cell
Chino, Mizushima, ER-Phagy: Quality Control and Turnover of Endoplasmic Reticulum, Trends Cell Biol
Chu, Chan, Zhang, Wang, Yuan et al., Middle East respiratory syndrome coronavirus and bat coronavirus HKU9 both can utilize GRP78 for attachment onto host cells, J. Biol. Chem
Cohen, Lin, Machamer, Identification of a Golgi complex-targeting signal in the cytoplasmic tail of the severe acute respiratory syndrome coronavirus envelope protein, J. Virol
De Albuquerque, Baig, Ma, Zhang, He et al., Murine hepatitis virus strain 1 produces a clinically relevant model of severe acute respiratory syndrome in A/J mice, J. Virol
De Bouteiller, Merck, Hasan, Hubac, Benguigui et al., Recognition of double-stranded RNA by human toll-like receptor 3 and downstream receptor signaling requires multimerization and an acidic pH, J. Biol. Chem
De Haan, Kuo, Masters, Vennema, Rottier, Coronavirus particle assembly: primary structure requirements of the membrane protein, J. Virol
De Haan, Rottier, Molecular interactions in the assembly of coronaviruses, Adv. Virus Res
Ducatelle, Hoorens, Significance of lysosomes in the morphogenesis of coronaviruses, Arch. Virol
Fawcett, The Cell
Ferna ´ndez De Castro, Tenorio, Ortega-Gonza ´lez, Knowlton, Zamora et al., A modified lysosomal organelle mediates nonlytic egress of reovirus, J. Cell Biol
Fung, Liu, Human Coronavirus: Host-Pathogen Interaction, Annu. Rev. Microbiol
Fung, Liu, Post-translational modifications of coronavirus proteins: roles and function, Future Virol
Garcia-Beltran, Ho ¨lzemer, Martrus, Chung, Pacheco et al., Open conformers of HLA-F are high-affinity ligands of the activating NK-cell receptor KIR3DS1, Nat. Immunol
Goodridge, Lee, Burian, Pyo, Tykodi et al., HLA-F and MHC-I open conformers cooperate in a MHC-I antigen cross-presentation pathway, J. Immunol
Gordon, Jang, Bouhaddou, Xu, Obernier et al., A SARS-CoV-2 protein interaction map reveals targets for drug repurposing, Nature
Graham, Ford, Rickwood, Isolation of the major subcellular organelles from mouse liver using Nycodenz gradients without the use of an ultracentrifuge, Anal. Biochem
Griffiths, Burke, Lucocq, Fine structure immunocytochemistry
Ha, Van Krieken, Carlos, Lee, The stress-inducible molecular chaperone GRP78 as potential therapeutic target for coronavirus infection, J. Infect
Humphries, Payne, Imaging lysosomal enzyme activity in live cells using self-quenched substrates, Anal. Biochem
Huotari, Helenius, Endosome maturation, EMBO J
Khanolkar, Pewe, Tifrea, Perlman, Harty, Developing MHV-1 infection as an animal model for Severe Acute Respiratory Syndrome (SARS) (43.30), J. Immunol
Khatter, Sindhwani, Sharma, Arf-like GTPase Arl8: Moving from the periphery to the center of lysosomal biology, Cell. Logist
Lam, Kulp, Wang, Lou, Taylor et al., Small Molecule Inhibition of Rab7 Impairs B Cell Class Switching and Plasma Cell Survival To Dampen the Autoantibody Response in Murine Lupus, J. Immunol
Langemeyer, Fro ¨hlich, Ungermann, Rab GTPase Function in Endosome and Lysosome Biogenesis, Trends Cell Biol
Laulagnier, Schieber, Maritzen, Haucke, Parton et al., Role of AP1 and Gadkin in the traffic of secretory endo-lysosomes, Mol. Biol. Cell
Leibowitz, Kaufman, Liu, Coronaviruses: propagation, quantification, storage, and construction of recombinant mouse hepatitis virus, Curr. Protoc. Microbiol
Lie, Nixon, Lysosome trafficking and signaling in health and neurodegenerative diseases, Neurobiol. Dis
Lippincott-Schwartz, Yuan, Bonifacino, Klausner, Rapid redistribution of Golgi proteins into the ER in cells treated with brefeldin A: evidence for membrane cycling from Golgi to ER, Cell
Long, Tang, Shi, Li, Deng et al., Clinical and immunological assessment of asymptomatic SARS-CoV-2 infections, Nat. Med
Lu, Zhao, Li, Niu, Yang et al., Genomic characterisation and epidemiology of 2019 novel coronavirus: implications for virus origins and receptor binding, Lancet
Lu, Zheng, Xu, Schwarz, Du et al., Severe acute respiratory syndrome-associated coronavirus 3a protein forms an ion channel and modulates virus release, Proc. Natl. Acad. Sci. USA
Machamer, Accommodation of large cargo within Golgi cisternae, Histochem. Cell Biol
Manders, Verbeek, Aten, Measurement of co localization of objects in duaa ˚colour confocal images, J. Microsc
Martin, Gao, Lee, Nelson, Detels et al., Epistatic interaction between KIR3DS1 and HLA-B delays the progression to AIDS, Nat. Genet
Martinez, Chakrabarti, Hellevik, Morehead, Fowler et al., Synaptotagmin VII regulates Ca(2+)-dependent exocytosis of lysosomes in fibroblasts, J. Cell Biol
Mcbride, Li, Machamer, The cytoplasmic tail of the severe acute respiratory syndrome coronavirus spike protein contains a novel endoplasmic reticulum retrieval signal that binds COPI and promotes interaction with membrane protein, J. Virol
Michelet, Garg, Wolf, Tuli, Ricciardi-Castagnoli et al., MHC class II presentation is controlled by the lysosomal small GTPase, Arl8b, J. Immunol
Michelet, Tuli, Gan, Geadas, Sharma et al., Lysosome-Mediated Plasma Membrane Repair Is Dependent on the Small GTPase Arl8b and Determines Cell Death Type in Mycobacterium tuberculosis Infection, J. Immunol
Miller, Carnell, Moore, Post-Golgi membrane traffic: brefeldin A inhibits export from distal Golgi compartments to the cell surface but not recycling, J. Cell Biol
Mindell, Lysosomal acidification mechanisms, Annu. Rev. Physiol
Munro, Pelham, A C-terminal signal prevents secretion of luminal ER proteins, Cell
Narayanan, Maeda, Maeda, Makino, Characterization of the coronavirus M protein and nucleocapsid interaction in infected cells, J. Virol
Oostra, De Haan, De Groot, Rottier, Glycosylation of the severe acute respiratory syndrome coronavirus triple-spanning membrane proteins 3a and M, J. Virol
Park, Shen, Liu, Liu, Ferguson et al., Dynamin triple knockout cells reveal off target effects of commonly used dynamin inhibitors, J. Cell Sci
Perrier, Bonnin, Desmarets, Danneels, Goffard et al., The C-terminal domain of the MERS coronavirus M protein contains a trans-Golgi network localization signal, J. Biol. Chem
Pornillos, Garrus, Sundquist, Mechanisms of enveloped RNA virus budding, Trends Cell Biol
Puelles, Lu ¨tgehetmann, Lindenmeyer, Sperhake, Wong et al., Multiorgan and Renal Tropism of SARS-CoV-2, N. Engl. J. Med
Raiborg, Wenzel, Pedersen, Olsvik, Schink et al., Repeated ER-endosome contacts promote endosome translocation and neurite outgrowth, Nature
Ravindran, Bagchi, Cunningham, Tsai, Opportunistic intruders: how viruses orchestrate ER functions to infect cells, Nat. Rev. Microbiol
Robinson, Schor, Barouch-Bentov, Einav, Viral journeys on the intracellular highways, Cell. Mol. Life Sci
Rodrı ´guez, Webster, Ortego, Andrews, Lysosomes behave as Ca2+-regulated exocytic vesicles in fibroblasts and epithelial cells, J. Cell Biol
Ruch, Machamer, The coronavirus E protein: assembly and beyond, Viruses
Samarel, Ferguson, Decker, Lesch, Effects of cysteine protease inhibitors on rabbit cathepsin D maturation, Am. J. Physiol
Sanman, Van Der Linden, Verdoes, Bogyo, Bifunctional Probes of Cathepsin Protease Activity and pH Reveal Alterations in Endolysosomal pH during Bacterial Infection, Cell Chem. Biol
Siu, Teoh, Lo, Chan, Kien et al., The M, E, and N structural proteins of the severe acute respiratory syndrome coronavirus are required for efficient assembly, trafficking, and release of virus-like particles, J. Virol
Slot, Geuze, Cryosectioning and immunolabeling, Nat. Protoc
Snijder, Limpens, De Wilde, Jong, Zevenhoven-Dobbe et al., A unifying structural and functional model of the coronavirus replication organelle: Tracking down RNA synthesis, PLoS Biol
Snijder, Van Der Meer, Zevenhoven-Dobbe, Onderwater, Van Der Meulen et al., Ultrastructure and origin of membrane vesicles associated with the severe acute respiratory syndrome coronavirus replication complex, J. Virol
Stohlman, Brayton, Fleming, Weiner, Lai, Murine coronaviruses: isolation and characterization of two plaque morphology variants of the JHM neurotropic strain, J. Gen. Virol
Stroupe, This Is the End: Regulation of Rab7 Nucleotide Binding in Endolysosomal Trafficking and Autophagy, Front. Cell Dev. Biol
Strous, Van Kerkhof, Van Meer, Rijnboutt, Stoorvogel, Differential effects of brefeldin A on transport of secretory and lysosomal proteins, J. Biol. Chem
Tannous, Gaussia luciferase reporter assay for monitoring biological processes in culture and in vivo, Nat. Protoc
Tokuyasu, A technique for ultracryotomy of cell suspensions and tissues, J. Cell Biol
Tokuyasu, Immunochemistry on ultrathin frozen sections, Histochem. J
Tooze, Tooze, Fuller, Sorting of progeny coronavirus from condensed secretory proteins at the exit from the trans-Golgi network of AtT20 cells, J. Cell Biol
Tooze, Tooze, Warren, Site of addition of N-acetylgalactosamine to the E1 glycoprotein of mouse hepatitis virus-A59, J. Cell Biol
Trombetta, Mellman, Cell biology of antigen processing in vitro and in vivo, Annu. Rev. Immunol
Vanlandingham, Ceresa, Rab7 regulates late endocytic trafficking downstream of multivesicular body biogenesis and cargo sequestration, J. Biol. Chem
Vardhana, Wolchok, The many faces of the anti-COVID immune response, J. Exp. Med
Verheije, Raaben, Mari, Te Lintelo, Reggiori et al., Mouse hepatitis coronavirus RNA replication depends on GBF1-mediated ARF1 activation, PLoS Pathog
Vogel, Erez, Dichotomy of cellular inhibition by small-molecule inhibitors revealed by single-cell analysis, Nat. Commun
Westerbeck, Machamer, The Infectious Bronchitis Coronavirus Envelope Protein Alters Golgi pH To Protect the Spike Protein and Promote the Release of Infectious Virus, J. Virol
Williamson, Feldmann, Schwarz, Meade-White, Porter et al., Clinical benefit of remdesivir in rhesus macaques infected with SARS-CoV-2, Nature
Xu, Liu, Swaroop, Sun, Dehdashti et al., A phenotypic compound screening assay for lysosomal storage diseases, J. Biomol. Screen
Yue, Nabar, Shi, Kamenyeva, Xiao et al., SARS-Coronavirus Open Reading Frame-3a drives multimodal necrotic cell death, Cell Death Dis
Ziegler, Allon, Nyquist, Mbano, Miao et al., SARS-CoV-2 Receptor ACE2 Is an Interferon-Stimulated Gene in Human Airway Epithelial Cells and Is Detected in Specific Cell Subsets across Tissues, Cell
DOI record:
{
"DOI": "10.1016/j.cell.2020.10.039",
"ISSN": [
"0092-8674"
],
"URL": "http://dx.doi.org/10.1016/j.cell.2020.10.039",
"alternative-id": [
"S009286742031446X"
],
"assertion": [
{
"label": "This article is maintained by",
"name": "publisher",
"value": "Elsevier"
},
{
"label": "Article Title",
"name": "articletitle",
"value": "β-Coronaviruses Use Lysosomes for Egress Instead of the Biosynthetic Secretory Pathway"
},
{
"label": "Journal Title",
"name": "journaltitle",
"value": "Cell"
},
{
"label": "CrossRef DOI link to publisher maintained version",
"name": "articlelink",
"value": "https://doi.org/10.1016/j.cell.2020.10.039"
},
{
"label": "Content Type",
"name": "content_type",
"value": "article"
},
{
"label": "Copyright",
"name": "copyright",
"value": "Published by Elsevier Inc."
}
],
"author": [
{
"affiliation": [],
"family": "Ghosh",
"given": "Sourish",
"sequence": "first"
},
{
"affiliation": [],
"family": "Dellibovi-Ragheb",
"given": "Teegan A.",
"sequence": "additional"
},
{
"ORCID": "http://orcid.org/0000-0002-1315-9841",
"affiliation": [],
"authenticated-orcid": false,
"family": "Kerviel",
"given": "Adeline",
"sequence": "additional"
},
{
"affiliation": [],
"family": "Pak",
"given": "Eowyn",
"sequence": "additional"
},
{
"affiliation": [],
"family": "Qiu",
"given": "Qi",
"sequence": "additional"
},
{
"affiliation": [],
"family": "Fisher",
"given": "Matthew",
"sequence": "additional"
},
{
"affiliation": [],
"family": "Takvorian",
"given": "Peter M.",
"sequence": "additional"
},
{
"ORCID": "http://orcid.org/0000-0003-1029-3444",
"affiliation": [],
"authenticated-orcid": false,
"family": "Bleck",
"given": "Christopher",
"sequence": "additional"
},
{
"affiliation": [],
"family": "Hsu",
"given": "Victor W.",
"sequence": "additional"
},
{
"ORCID": "http://orcid.org/0000-0003-1560-1573",
"affiliation": [],
"authenticated-orcid": false,
"family": "Fehr",
"given": "Anthony R.",
"sequence": "additional"
},
{
"affiliation": [],
"family": "Perlman",
"given": "Stanley",
"sequence": "additional"
},
{
"affiliation": [],
"family": "Achar",
"given": "Sooraj R.",
"sequence": "additional"
},
{
"ORCID": "http://orcid.org/0000-0003-1087-2091",
"affiliation": [],
"authenticated-orcid": false,
"family": "Straus",
"given": "Marco R.",
"sequence": "additional"
},
{
"affiliation": [],
"family": "Whittaker",
"given": "Gary R.",
"sequence": "additional"
},
{
"affiliation": [],
"family": "de Haan",
"given": "Cornelis A.M.",
"sequence": "additional"
},
{
"ORCID": "http://orcid.org/0000-0002-6526-159X",
"affiliation": [],
"authenticated-orcid": false,
"family": "Kehrl",
"given": "John",
"sequence": "additional"
},
{
"affiliation": [],
"family": "Altan-Bonnet",
"given": "Grégoire",
"sequence": "additional"
},
{
"affiliation": [],
"family": "Altan-Bonnet",
"given": "Nihal",
"sequence": "additional"
}
],
"container-title": "Cell",
"container-title-short": "Cell",
"content-domain": {
"crossmark-restriction": true,
"domain": [
"cell.com",
"elsevier.com",
"sciencedirect.com"
]
},
"created": {
"date-parts": [
[
2020,
10,
27
]
],
"date-time": "2020-10-27T12:19:56Z",
"timestamp": 1603801196000
},
"deposited": {
"date-parts": [
[
2023,
10,
10
]
],
"date-time": "2023-10-10T18:01:40Z",
"timestamp": 1696960900000
},
"funder": [
{
"DOI": "10.13039/100000002",
"award": [
"R01 NS36592",
"R37GM058615",
"F32-AI113973",
"R01 A1091985-05",
"R01AI35270"
],
"doi-asserted-by": "publisher",
"id": [
{
"asserted-by": "publisher",
"id": "10.13039/100000002",
"id-type": "DOI"
}
],
"name": "National Institutes of Health"
},
{
"DOI": "10.13039/100000054",
"award": [
"R01 NS36592",
"R37GM058615",
"F32-AI113973",
"R01 A1091985-05",
"R01AI35270"
],
"doi-asserted-by": "publisher",
"id": [
{
"asserted-by": "publisher",
"id": "10.13039/100000054",
"id-type": "DOI"
}
],
"name": "National Cancer Institute"
}
],
"indexed": {
"date-parts": [
[
2024,
12,
30
]
],
"date-time": "2024-12-30T18:55:41Z",
"timestamp": 1735584941888
},
"is-referenced-by-count": 483,
"issue": "6",
"issued": {
"date-parts": [
[
2020,
12
]
]
},
"journal-issue": {
"issue": "6",
"published-print": {
"date-parts": [
[
2020,
12
]
]
}
},
"language": "en",
"license": [
{
"URL": "https://www.elsevier.com/tdm/userlicense/1.0/",
"content-version": "tdm",
"delay-in-days": 0,
"start": {
"date-parts": [
[
2020,
12,
1
]
],
"date-time": "2020-12-01T00:00:00Z",
"timestamp": 1606780800000
}
},
{
"URL": "http://www.elsevier.com/open-access/userlicense/1.0/",
"content-version": "vor",
"delay-in-days": 374,
"start": {
"date-parts": [
[
2021,
12,
10
]
],
"date-time": "2021-12-10T00:00:00Z",
"timestamp": 1639094400000
}
}
],
"link": [
{
"URL": "https://api.elsevier.com/content/article/PII:S009286742031446X?httpAccept=text/xml",
"content-type": "text/xml",
"content-version": "vor",
"intended-application": "text-mining"
},
{
"URL": "https://api.elsevier.com/content/article/PII:S009286742031446X?httpAccept=text/plain",
"content-type": "text/plain",
"content-version": "vor",
"intended-application": "text-mining"
}
],
"member": "78",
"original-title": [],
"page": "1520-1535.e14",
"prefix": "10.1016",
"published": {
"date-parts": [
[
2020,
12
]
]
},
"published-print": {
"date-parts": [
[
2020,
12
]
]
},
"publisher": "Elsevier BV",
"reference": [
{
"DOI": "10.1021/cb3001099",
"article-title": "A competitive nucleotide binding inhibitor: in vitro characterization of Rab7 GTPase inhibition",
"author": "Agola",
"doi-asserted-by": "crossref",
"first-page": "1095",
"journal-title": "ACS Chem. Biol.",
"key": "10.1016/j.cell.2020.10.039_bib1",
"volume": "7",
"year": "2012"
},
{
"DOI": "10.1007/s00251-012-0623-3",
"article-title": "Killer-cell immunoglobulin-like receptors (KIR) in severe A (H1N1) 2009 influenza infections",
"author": "Aranda-Romo",
"doi-asserted-by": "crossref",
"first-page": "653",
"journal-title": "Immunogenetics",
"key": "10.1016/j.cell.2020.10.039_bib2",
"volume": "64",
"year": "2012"
},
{
"DOI": "10.1038/s41580-019-0185-4",
"article-title": "Lysosomes as dynamic regulators of cell and organismal homeostasis",
"author": "Ballabio",
"doi-asserted-by": "crossref",
"first-page": "101",
"journal-title": "Nat. Rev. Mol. Cell Biol.",
"key": "10.1016/j.cell.2020.10.039_bib3",
"volume": "21",
"year": "2020"
},
{
"DOI": "10.1016/j.bbamcr.2018.12.011",
"article-title": "Drosophila Arl8 is a general positive regulator of lysosomal fusion events",
"author": "Boda",
"doi-asserted-by": "crossref",
"first-page": "533",
"journal-title": "Biochim. Biophys. Acta Mol. Cell Res.",
"key": "10.1016/j.cell.2020.10.039_bib4",
"volume": "4",
"year": "2019"
},
{
"DOI": "10.1074/jbc.M000900200",
"article-title": "A protein containing a serine-rich domain with vesicle fusing properties mediates cell cycle-dependent cytosolic pH regulation",
"author": "Brazill",
"doi-asserted-by": "crossref",
"first-page": "19231",
"journal-title": "J. Biol. Chem.",
"key": "10.1016/j.cell.2020.10.039_bib5",
"volume": "275",
"year": "2000"
},
{
"DOI": "10.1083/jcb.103.4.1235",
"article-title": "Mannose-6-phosphate receptors for lysosomal enzymes cycle between the Golgi complex and endosomes",
"author": "Brown",
"doi-asserted-by": "crossref",
"first-page": "1235",
"journal-title": "J. Cell Biol.",
"key": "10.1016/j.cell.2020.10.039_bib6",
"volume": "103",
"year": "1986"
},
{
"DOI": "10.1091/mbc.11.2.467",
"article-title": "Rab7: a key to lysosome biogenesis",
"author": "Bucci",
"doi-asserted-by": "crossref",
"first-page": "467",
"journal-title": "Mol. Biol. Cell",
"key": "10.1016/j.cell.2020.10.039_bib7",
"volume": "11",
"year": "2000"
},
{
"DOI": "10.1128/mBio.02325-17",
"article-title": "Role of Severe Acute Respiratory Syndrome Coronavirus Viroporins E, 3a, and 8a in Replication and Pathogenesis",
"author": "Castaño-Rodriguez",
"doi-asserted-by": "crossref",
"first-page": "e02325-17",
"journal-title": "mBio",
"key": "10.1016/j.cell.2020.10.039_bib8",
"volume": "9",
"year": "2018"
},
{
"DOI": "10.1080/20013078.2019.1703244",
"article-title": "Inhibiting extracellular vesicles formation and release: a review of EV inhibitors",
"author": "Catalano",
"doi-asserted-by": "crossref",
"first-page": "1703244",
"journal-title": "J. Extracell. Vesicles",
"key": "10.1016/j.cell.2020.10.039_bib9",
"volume": "9",
"year": "2019"
},
{
"DOI": "10.1016/j.chom.2016.01.007",
"article-title": "Dysregulated Type I Interferon and Inflammatory Monocyte-Macrophage Responses Cause Lethal Pneumonia in SARS-CoV-Infected Mice",
"author": "Channappanavar",
"doi-asserted-by": "crossref",
"first-page": "181",
"journal-title": "Cell Host Microbe",
"key": "10.1016/j.cell.2020.10.039_bib10",
"volume": "19",
"year": "2016"
},
{
"DOI": "10.1016/j.cell.2015.01.032",
"article-title": "Phosphatidylserine vesicles enable efficient en bloc transmission of enteroviruses",
"author": "Chen",
"doi-asserted-by": "crossref",
"first-page": "619",
"journal-title": "Cell",
"key": "10.1016/j.cell.2020.10.039_bib11",
"volume": "160",
"year": "2015"
},
{
"DOI": "10.1016/j.tcb.2020.02.001",
"article-title": "ER-Phagy: Quality Control and Turnover of Endoplasmic Reticulum",
"author": "Chino",
"doi-asserted-by": "crossref",
"first-page": "384",
"journal-title": "Trends Cell Biol.",
"key": "10.1016/j.cell.2020.10.039_bib12",
"volume": "30",
"year": "2020"
},
{
"DOI": "10.1074/jbc.RA118.001897",
"article-title": "Middle East respiratory syndrome coronavirus and bat coronavirus HKU9 both can utilize GRP78 for attachment onto host cells",
"author": "Chu",
"doi-asserted-by": "crossref",
"first-page": "11709",
"journal-title": "J. Biol. Chem.",
"key": "10.1016/j.cell.2020.10.039_bib13",
"volume": "293",
"year": "2018"
},
{
"DOI": "10.1128/JVI.00060-11",
"article-title": "Identification of a Golgi complex-targeting signal in the cytoplasmic tail of the severe acute respiratory syndrome coronavirus envelope protein",
"author": "Cohen",
"doi-asserted-by": "crossref",
"first-page": "5794",
"journal-title": "J. Virol.",
"key": "10.1016/j.cell.2020.10.039_bib14",
"volume": "85",
"year": "2011"
},
{
"DOI": "10.1128/JVI.00747-06",
"article-title": "Murine hepatitis virus strain 1 produces a clinically relevant model of severe acute respiratory syndrome in A/J mice",
"author": "De Albuquerque",
"doi-asserted-by": "crossref",
"first-page": "10382",
"journal-title": "J. Virol.",
"key": "10.1016/j.cell.2020.10.039_bib15",
"volume": "80",
"year": "2006"
},
{
"DOI": "10.1074/jbc.M507163200",
"article-title": "Recognition of double-stranded RNA by human toll-like receptor 3 and downstream receptor signaling requires multimerization and an acidic pH",
"author": "de Bouteiller",
"doi-asserted-by": "crossref",
"first-page": "38133",
"journal-title": "J. Biol. Chem.",
"key": "10.1016/j.cell.2020.10.039_bib16",
"volume": "280",
"year": "2005"
},
{
"DOI": "10.1016/S0065-3527(05)64006-7",
"article-title": "Molecular interactions in the assembly of coronaviruses",
"author": "de Haan",
"doi-asserted-by": "crossref",
"first-page": "165",
"journal-title": "Adv. Virus Res.",
"key": "10.1016/j.cell.2020.10.039_bib17",
"volume": "64",
"year": "2005"
},
{
"DOI": "10.1128/JVI.72.8.6838-6850.1998",
"article-title": "Coronavirus particle assembly: primary structure requirements of the membrane protein",
"author": "de Haan",
"doi-asserted-by": "crossref",
"first-page": "6838",
"journal-title": "J. Virol.",
"key": "10.1016/j.cell.2020.10.039_bib18",
"volume": "72",
"year": "1998"
},
{
"DOI": "10.1007/BF01314299",
"article-title": "Significance of lysosomes in the morphogenesis of coronaviruses",
"author": "Ducatelle",
"doi-asserted-by": "crossref",
"first-page": "1",
"journal-title": "Arch. Virol.",
"key": "10.1016/j.cell.2020.10.039_bib19",
"volume": "79",
"year": "1984"
},
{
"author": "Fawcett",
"key": "10.1016/j.cell.2020.10.039_bib20",
"series-title": "The Cell",
"year": "1966"
},
{
"DOI": "10.1083/jcb.201910131",
"article-title": "A modified lysosomal organelle mediates nonlytic egress of reovirus",
"author": "Fernández de Castro",
"doi-asserted-by": "crossref",
"first-page": "e201910131",
"journal-title": "J. Cell Biol.",
"key": "10.1016/j.cell.2020.10.039_bib21",
"volume": "219",
"year": "2020"
},
{
"DOI": "10.2217/fvl-2018-0008",
"article-title": "Post-translational modifications of coronavirus proteins: roles and function",
"author": "Fung",
"doi-asserted-by": "crossref",
"first-page": "405",
"journal-title": "Future Virol.",
"key": "10.1016/j.cell.2020.10.039_bib22",
"volume": "13",
"year": "2018"
},
{
"DOI": "10.1146/annurev-micro-020518-115759",
"article-title": "Human Coronavirus: Host-Pathogen Interaction",
"author": "Fung",
"doi-asserted-by": "crossref",
"first-page": "529",
"journal-title": "Annu. Rev. Microbiol.",
"key": "10.1016/j.cell.2020.10.039_bib23",
"volume": "73",
"year": "2019"
},
{
"DOI": "10.1038/ni.3513",
"article-title": "Open conformers of HLA-F are high-affinity ligands of the activating NK-cell receptor KIR3DS1",
"author": "Garcia-Beltran",
"doi-asserted-by": "crossref",
"first-page": "1067",
"journal-title": "Nat. Immunol.",
"key": "10.1016/j.cell.2020.10.039_bib24",
"volume": "17",
"year": "2016"
},
{
"DOI": "10.4049/jimmunol.1300080",
"article-title": "HLA-F and MHC-I open conformers cooperate in a MHC-I antigen cross-presentation pathway",
"author": "Goodridge",
"doi-asserted-by": "crossref",
"first-page": "1567",
"journal-title": "J. Immunol.",
"key": "10.1016/j.cell.2020.10.039_bib25",
"volume": "191",
"year": "2013"
},
{
"DOI": "10.1038/s41586-020-2286-9",
"article-title": "A SARS-CoV-2 protein interaction map reveals targets for drug repurposing",
"author": "Gordon",
"doi-asserted-by": "crossref",
"first-page": "459",
"journal-title": "Nature",
"key": "10.1016/j.cell.2020.10.039_bib26",
"volume": "583",
"year": "2020"
},
{
"DOI": "10.1016/0003-2697(90)90463-J",
"article-title": "Isolation of the major subcellular organelles from mouse liver using Nycodenz gradients without the use of an ultracentrifuge",
"author": "Graham",
"doi-asserted-by": "crossref",
"first-page": "318",
"journal-title": "Anal. Biochem.",
"key": "10.1016/j.cell.2020.10.039_bib27",
"volume": "187",
"year": "1990"
},
{
"author": "Griffiths",
"key": "10.1016/j.cell.2020.10.039_bib28",
"series-title": "Fine structure immunocytochemistry",
"year": "1993"
},
{
"DOI": "10.1016/j.jinf.2020.06.017",
"article-title": "The stress-inducible molecular chaperone GRP78 as potential therapeutic target for coronavirus infection",
"author": "Ha",
"doi-asserted-by": "crossref",
"first-page": "452",
"journal-title": "J. Infect.",
"key": "10.1016/j.cell.2020.10.039_bib29",
"volume": "81",
"year": "2020"
},
{
"DOI": "10.1016/j.ab.2012.02.033",
"article-title": "Imaging lysosomal enzyme activity in live cells using self-quenched substrates",
"author": "Humphries",
"doi-asserted-by": "crossref",
"first-page": "178",
"journal-title": "Anal. Biochem.",
"key": "10.1016/j.cell.2020.10.039_bib30",
"volume": "424",
"year": "2012"
},
{
"DOI": "10.1038/emboj.2011.286",
"article-title": "Endosome maturation",
"author": "Huotari",
"doi-asserted-by": "crossref",
"first-page": "3481",
"journal-title": "EMBO J.",
"key": "10.1016/j.cell.2020.10.039_bib31",
"volume": "30",
"year": "2011"
},
{
"DOI": "10.4049/jimmunol.178.Supp.43.30",
"article-title": "Developing MHV-1 infection as an animal model for Severe Acute Respiratory Syndrome (SARS) (43.30)",
"author": "Khanolkar",
"doi-asserted-by": "crossref",
"first-page": "S42",
"journal-title": "J. Immunol.",
"key": "10.1016/j.cell.2020.10.039_bib32",
"volume": "178",
"year": "2007"
},
{
"DOI": "10.1080/21592799.2015.1086501",
"article-title": "Arf-like GTPase Arl8: Moving from the periphery to the center of lysosomal biology",
"author": "Khatter",
"doi-asserted-by": "crossref",
"first-page": "e1086501",
"journal-title": "Cell. Logist.",
"key": "10.1016/j.cell.2020.10.039_bib33",
"volume": "5",
"year": "2015"
},
{
"DOI": "10.4049/jimmunol.1601427",
"article-title": "Small Molecule Inhibition of Rab7 Impairs B Cell Class Switching and Plasma Cell Survival To Dampen the Autoantibody Response in Murine Lupus",
"author": "Lam",
"doi-asserted-by": "crossref",
"first-page": "3792",
"journal-title": "J. Immunol.",
"key": "10.1016/j.cell.2020.10.039_bib34",
"volume": "197",
"year": "2016"
},
{
"DOI": "10.1016/j.tcb.2018.06.007",
"article-title": "Rab GTPase Function in Endosome and Lysosome Biogenesis",
"author": "Langemeyer",
"doi-asserted-by": "crossref",
"first-page": "957",
"journal-title": "Trends Cell Biol.",
"key": "10.1016/j.cell.2020.10.039_bib35",
"volume": "28",
"year": "2018"
},
{
"DOI": "10.1091/mbc.e11-03-0193",
"article-title": "Role of AP1 and Gadkin in the traffic of secretory endo-lysosomes",
"author": "Laulagnier",
"doi-asserted-by": "crossref",
"first-page": "2068",
"journal-title": "Mol. Biol. Cell",
"key": "10.1016/j.cell.2020.10.039_bib36",
"volume": "22",
"year": "2011"
},
{
"DOI": "10.1002/9780471729259.mc15e01s21",
"article-title": "Coronaviruses: propagation, quantification, storage, and construction of recombinant mouse hepatitis virus",
"author": "Leibowitz",
"doi-asserted-by": "crossref",
"journal-title": "Curr. Protoc. Microbiol.",
"key": "10.1016/j.cell.2020.10.039_bib37",
"year": "2011"
},
{
"DOI": "10.1016/j.nbd.2018.05.015",
"article-title": "Lysosome trafficking and signaling in health and neurodegenerative diseases",
"author": "Lie",
"doi-asserted-by": "crossref",
"first-page": "94",
"journal-title": "Neurobiol. Dis.",
"key": "10.1016/j.cell.2020.10.039_bib38",
"volume": "122",
"year": "2019"
},
{
"DOI": "10.1016/0092-8674(89)90685-5",
"article-title": "Rapid redistribution of Golgi proteins into the ER in cells treated with brefeldin A: evidence for membrane cycling from Golgi to ER",
"author": "Lippincott-Schwartz",
"doi-asserted-by": "crossref",
"first-page": "801",
"journal-title": "Cell",
"key": "10.1016/j.cell.2020.10.039_bib39",
"volume": "56",
"year": "1989"
},
{
"DOI": "10.1038/s41591-020-0965-6",
"article-title": "Clinical and immunological assessment of asymptomatic SARS-CoV-2 infections",
"author": "Long",
"doi-asserted-by": "crossref",
"first-page": "1200",
"journal-title": "Nat. Med.",
"key": "10.1016/j.cell.2020.10.039_bib40",
"volume": "26",
"year": "2020"
},
{
"DOI": "10.1073/pnas.0605402103",
"article-title": "Severe acute respiratory syndrome-associated coronavirus 3a protein forms an ion channel and modulates virus release",
"author": "Lu",
"doi-asserted-by": "crossref",
"first-page": "12540",
"journal-title": "Proc. Natl. Acad. Sci. USA",
"key": "10.1016/j.cell.2020.10.039_bib41",
"volume": "103",
"year": "2006"
},
{
"DOI": "10.1016/S0140-6736(20)30251-8",
"article-title": "Genomic characterisation and epidemiology of 2019 novel coronavirus: implications for virus origins and receptor binding",
"author": "Lu",
"doi-asserted-by": "crossref",
"first-page": "565",
"journal-title": "Lancet",
"key": "10.1016/j.cell.2020.10.039_bib42",
"volume": "395",
"year": "2020"
},
{
"DOI": "10.1007/s00418-013-1120-y",
"article-title": "Accommodation of large cargo within Golgi cisternae",
"author": "Machamer",
"doi-asserted-by": "crossref",
"first-page": "261",
"journal-title": "Histochem. Cell Biol.",
"key": "10.1016/j.cell.2020.10.039_bib43",
"volume": "140",
"year": "2013"
},
{
"DOI": "10.1111/j.1365-2818.1993.tb03313.x",
"article-title": "Measurement of co localization of objects in duaå colour confocal images",
"author": "Manders",
"doi-asserted-by": "crossref",
"first-page": "375",
"journal-title": "J. Microsc.",
"key": "10.1016/j.cell.2020.10.039_bib44",
"volume": "169",
"year": "1993"
},
{
"DOI": "10.1038/ng934",
"article-title": "Epistatic interaction between KIR3DS1 and HLA-B delays the progression to AIDS",
"author": "Martin",
"doi-asserted-by": "crossref",
"first-page": "429",
"journal-title": "Nat. Genet.",
"key": "10.1016/j.cell.2020.10.039_bib45",
"volume": "31",
"year": "2002"
},
{
"DOI": "10.1083/jcb.148.6.1141",
"article-title": "Synaptotagmin VII regulates Ca(2+)-dependent exocytosis of lysosomes in fibroblasts",
"author": "Martinez",
"doi-asserted-by": "crossref",
"first-page": "1141",
"journal-title": "J. Cell Biol.",
"key": "10.1016/j.cell.2020.10.039_bib46",
"volume": "148",
"year": "2000"
},
{
"DOI": "10.1128/JVI.02146-06",
"article-title": "The cytoplasmic tail of the severe acute respiratory syndrome coronavirus spike protein contains a novel endoplasmic reticulum retrieval signal that binds COPI and promotes interaction with membrane protein",
"author": "McBride",
"doi-asserted-by": "crossref",
"first-page": "2418",
"journal-title": "J. Virol.",
"key": "10.1016/j.cell.2020.10.039_bib47",
"volume": "81",
"year": "2007"
},
{
"DOI": "10.4049/jimmunol.1401072",
"article-title": "MHC class II presentation is controlled by the lysosomal small GTPase, Arl8b",
"author": "Michelet",
"doi-asserted-by": "crossref",
"first-page": "2079",
"journal-title": "J. Immunol.",
"key": "10.1016/j.cell.2020.10.039_bib48",
"volume": "194",
"year": "2015"
},
{
"DOI": "10.4049/jimmunol.1700829",
"article-title": "Lysosome-Mediated Plasma Membrane Repair Is Dependent on the Small GTPase Arl8b and Determines Cell Death Type in Mycobacterium tuberculosis Infection",
"author": "Michelet",
"doi-asserted-by": "crossref",
"first-page": "3160",
"journal-title": "J. Immunol.",
"key": "10.1016/j.cell.2020.10.039_bib49",
"volume": "200",
"year": "2018"
},
{
"DOI": "10.1083/jcb.118.2.267",
"article-title": "Post-Golgi membrane traffic: brefeldin A inhibits export from distal Golgi compartments to the cell surface but not recycling",
"author": "Miller",
"doi-asserted-by": "crossref",
"first-page": "267",
"journal-title": "J. Cell Biol.",
"key": "10.1016/j.cell.2020.10.039_bib50",
"volume": "118",
"year": "1992"
},
{
"DOI": "10.1146/annurev-physiol-012110-142317",
"article-title": "Lysosomal acidification mechanisms",
"author": "Mindell",
"doi-asserted-by": "crossref",
"first-page": "69",
"journal-title": "Annu. Rev. Physiol.",
"key": "10.1016/j.cell.2020.10.039_bib51",
"volume": "74",
"year": "2012"
},
{
"DOI": "10.1016/0092-8674(87)90086-9",
"article-title": "A C-terminal signal prevents secretion of luminal ER proteins",
"author": "Munro",
"doi-asserted-by": "crossref",
"first-page": "899",
"journal-title": "Cell",
"key": "10.1016/j.cell.2020.10.039_bib52",
"volume": "48",
"year": "1987"
},
{
"DOI": "10.1128/JVI.74.17.8127-8134.2000",
"article-title": "Characterization of the coronavirus M protein and nucleocapsid interaction in infected cells",
"author": "Narayanan",
"doi-asserted-by": "crossref",
"first-page": "8127",
"journal-title": "J. Virol.",
"key": "10.1016/j.cell.2020.10.039_bib53",
"volume": "74",
"year": "2000"
},
{
"DOI": "10.1128/JVI.80.5.2326-2336.2006",
"article-title": "Glycosylation of the severe acute respiratory syndrome coronavirus triple-spanning membrane proteins 3a and M",
"author": "Oostra",
"doi-asserted-by": "crossref",
"first-page": "2326",
"journal-title": "J. Virol.",
"key": "10.1016/j.cell.2020.10.039_bib54",
"volume": "80",
"year": "2006"
},
{
"article-title": "Dynamin triple knockout cells reveal off target effects of commonly used dynamin inhibitors",
"author": "Park",
"first-page": "5305",
"journal-title": "J. Cell Sci.",
"key": "10.1016/j.cell.2020.10.039_bib55",
"volume": "126",
"year": "2013"
},
{
"DOI": "10.1074/jbc.RA119.008964",
"article-title": "The C-terminal domain of the MERS coronavirus M protein contains a trans-Golgi network localization signal",
"author": "Perrier",
"doi-asserted-by": "crossref",
"first-page": "14406",
"journal-title": "J. Biol. Chem.",
"key": "10.1016/j.cell.2020.10.039_bib56",
"volume": "294",
"year": "2019"
},
{
"DOI": "10.1016/S0962-8924(02)02402-9",
"article-title": "Mechanisms of enveloped RNA virus budding",
"author": "Pornillos",
"doi-asserted-by": "crossref",
"first-page": "569",
"journal-title": "Trends Cell Biol.",
"key": "10.1016/j.cell.2020.10.039_bib57",
"volume": "12",
"year": "2002"
},
{
"DOI": "10.1056/NEJMc2011400",
"article-title": "Multiorgan and Renal Tropism of SARS-CoV-2",
"author": "Puelles",
"doi-asserted-by": "crossref",
"first-page": "590",
"journal-title": "N. Engl. J. Med.",
"key": "10.1016/j.cell.2020.10.039_bib58",
"volume": "383",
"year": "2020"
},
{
"DOI": "10.1038/nature14359",
"article-title": "Repeated ER-endosome contacts promote endosome translocation and neurite outgrowth",
"author": "Raiborg",
"doi-asserted-by": "crossref",
"first-page": "234",
"journal-title": "Nature",
"key": "10.1016/j.cell.2020.10.039_bib59",
"volume": "520",
"year": "2015"
},
{
"DOI": "10.1038/nrmicro.2016.60",
"article-title": "Opportunistic intruders: how viruses orchestrate ER functions to infect cells",
"author": "Ravindran",
"doi-asserted-by": "crossref",
"first-page": "407",
"journal-title": "Nat. Rev. Microbiol.",
"key": "10.1016/j.cell.2020.10.039_bib60",
"volume": "14",
"year": "2016"
},
{
"DOI": "10.1007/s00018-018-2882-0",
"article-title": "Viral journeys on the intracellular highways",
"author": "Robinson",
"doi-asserted-by": "crossref",
"first-page": "3693",
"journal-title": "Cell. Mol. Life Sci.",
"key": "10.1016/j.cell.2020.10.039_bib61",
"volume": "75",
"year": "2018"
},
{
"DOI": "10.1083/jcb.137.1.93",
"article-title": "Lysosomes behave as Ca2+-regulated exocytic vesicles in fibroblasts and epithelial cells",
"author": "Rodríguez",
"doi-asserted-by": "crossref",
"first-page": "93",
"journal-title": "J. Cell Biol.",
"key": "10.1016/j.cell.2020.10.039_bib62",
"volume": "137",
"year": "1997"
},
{
"DOI": "10.3390/v4030363",
"article-title": "The coronavirus E protein: assembly and beyond",
"author": "Ruch",
"doi-asserted-by": "crossref",
"first-page": "363",
"journal-title": "Viruses",
"key": "10.1016/j.cell.2020.10.039_bib63",
"volume": "4",
"year": "2012"
},
{
"DOI": "10.1152/ajpcell.1989.257.6.C1069",
"article-title": "Effects of cysteine protease inhibitors on rabbit cathepsin D maturation",
"author": "Samarel",
"doi-asserted-by": "crossref",
"first-page": "C1069",
"journal-title": "Am. J. Physiol.",
"key": "10.1016/j.cell.2020.10.039_bib64",
"volume": "257",
"year": "1989"
},
{
"DOI": "10.1016/j.chembiol.2016.05.019",
"article-title": "Bifunctional Probes of Cathepsin Protease Activity and pH Reveal Alterations in Endolysosomal pH during Bacterial Infection",
"author": "Sanman",
"doi-asserted-by": "crossref",
"first-page": "793",
"journal-title": "Cell Chem. Biol.",
"key": "10.1016/j.cell.2020.10.039_bib65",
"volume": "23",
"year": "2016"
},
{
"DOI": "10.1128/JVI.01052-08",
"article-title": "The M, E, and N structural proteins of the severe acute respiratory syndrome coronavirus are required for efficient assembly, trafficking, and release of virus-like particles",
"author": "Siu",
"doi-asserted-by": "crossref",
"first-page": "11318",
"journal-title": "J. Virol.",
"key": "10.1016/j.cell.2020.10.039_bib66",
"volume": "82",
"year": "2008"
},
{
"DOI": "10.1038/nprot.2007.365",
"article-title": "Cryosectioning and immunolabeling",
"author": "Slot",
"doi-asserted-by": "crossref",
"first-page": "2480",
"journal-title": "Nat. Protoc.",
"key": "10.1016/j.cell.2020.10.039_bib67",
"volume": "2",
"year": "2007"
},
{
"DOI": "10.1128/JVI.02501-05",
"article-title": "Ultrastructure and origin of membrane vesicles associated with the severe acute respiratory syndrome coronavirus replication complex",
"author": "Snijder",
"doi-asserted-by": "crossref",
"first-page": "5927",
"journal-title": "J. Virol.",
"key": "10.1016/j.cell.2020.10.039_bib68",
"volume": "80",
"year": "2006"
},
{
"DOI": "10.1371/journal.pbio.3000715",
"article-title": "A unifying structural and functional model of the coronavirus replication organelle: Tracking down RNA synthesis",
"author": "Snijder",
"doi-asserted-by": "crossref",
"first-page": "e3000715",
"journal-title": "PLoS Biol.",
"key": "10.1016/j.cell.2020.10.039_bib69",
"volume": "18",
"year": "2020"
},
{
"DOI": "10.1099/0022-1317-63-2-265",
"article-title": "Murine coronaviruses: isolation and characterization of two plaque morphology variants of the JHM neurotropic strain",
"author": "Stohlman",
"doi-asserted-by": "crossref",
"first-page": "265",
"journal-title": "J. Gen. Virol.",
"key": "10.1016/j.cell.2020.10.039_bib70",
"volume": "63",
"year": "1982"
},
{
"DOI": "10.3389/fcell.2018.00129",
"article-title": "This Is the End: Regulation of Rab7 Nucleotide Binding in Endolysosomal Trafficking and Autophagy",
"author": "Stroupe",
"doi-asserted-by": "crossref",
"first-page": "129",
"journal-title": "Front. Cell Dev. Biol.",
"key": "10.1016/j.cell.2020.10.039_bib71",
"volume": "6",
"year": "2018"
},
{
"DOI": "10.1016/S0021-9258(18)53781-9",
"article-title": "Differential effects of brefeldin A on transport of secretory and lysosomal proteins",
"author": "Strous",
"doi-asserted-by": "crossref",
"first-page": "2341",
"journal-title": "J. Biol. Chem.",
"key": "10.1016/j.cell.2020.10.039_bib72",
"volume": "268",
"year": "1993"
},
{
"DOI": "10.1038/nprot.2009.28",
"article-title": "Gaussia luciferase reporter assay for monitoring biological processes in culture and in vivo",
"author": "Tannous",
"doi-asserted-by": "crossref",
"first-page": "582",
"journal-title": "Nat. Protoc.",
"key": "10.1016/j.cell.2020.10.039_bib73",
"volume": "4",
"year": "2009"
},
{
"DOI": "10.1083/jcb.57.2.551",
"article-title": "A technique for ultracryotomy of cell suspensions and tissues",
"author": "Tokuyasu",
"doi-asserted-by": "crossref",
"first-page": "551",
"journal-title": "J. Cell Biol.",
"key": "10.1016/j.cell.2020.10.039_bib74",
"volume": "57",
"year": "1973"
},
{
"DOI": "10.1007/BF01011956",
"article-title": "Immunochemistry on ultrathin frozen sections",
"author": "Tokuyasu",
"doi-asserted-by": "crossref",
"first-page": "381",
"journal-title": "Histochem. J.",
"key": "10.1016/j.cell.2020.10.039_bib75",
"volume": "12",
"year": "1980"
},
{
"DOI": "10.1083/jcb.105.3.1215",
"article-title": "Sorting of progeny coronavirus from condensed secretory proteins at the exit from the trans-Golgi network of AtT20 cells",
"author": "Tooze",
"doi-asserted-by": "crossref",
"first-page": "1215",
"journal-title": "J. Cell Biol.",
"key": "10.1016/j.cell.2020.10.039_bib76",
"volume": "105",
"year": "1987"
},
{
"DOI": "10.1083/jcb.106.5.1475",
"article-title": "Site of addition of N-acetyl-galactosamine to the E1 glycoprotein of mouse hepatitis virus-A59",
"author": "Tooze",
"doi-asserted-by": "crossref",
"first-page": "1475",
"journal-title": "J. Cell Biol.",
"key": "10.1016/j.cell.2020.10.039_bib77",
"volume": "106",
"year": "1988"
},
{
"DOI": "10.1146/annurev.immunol.22.012703.104538",
"article-title": "Cell biology of antigen processing in vitro and in vivo",
"author": "Trombetta",
"doi-asserted-by": "crossref",
"first-page": "975",
"journal-title": "Annu. Rev. Immunol.",
"key": "10.1016/j.cell.2020.10.039_bib78",
"volume": "23",
"year": "2005"
},
{
"DOI": "10.1074/jbc.M809277200",
"article-title": "Rab7 regulates late endocytic trafficking downstream of multivesicular body biogenesis and cargo sequestration",
"author": "Vanlandingham",
"doi-asserted-by": "crossref",
"first-page": "12110",
"journal-title": "J. Biol. Chem.",
"key": "10.1016/j.cell.2020.10.039_bib79",
"volume": "284",
"year": "2009"
},
{
"DOI": "10.1084/jem.20200678",
"article-title": "The many faces of the anti-COVID immune response",
"author": "Vardhana",
"doi-asserted-by": "crossref",
"first-page": "e20200678",
"journal-title": "J. Exp. Med.",
"key": "10.1016/j.cell.2020.10.039_bib80",
"volume": "217",
"year": "2020"
},
{
"DOI": "10.1371/journal.ppat.1000088",
"article-title": "Mouse hepatitis coronavirus RNA replication depends on GBF1-mediated ARF1 activation",
"author": "Verheije",
"doi-asserted-by": "crossref",
"first-page": "e1000088",
"journal-title": "PLoS Pathog.",
"key": "10.1016/j.cell.2020.10.039_bib81",
"volume": "4",
"year": "2008"
},
{
"DOI": "10.1038/ncomms12428",
"article-title": "Dichotomy of cellular inhibition by small-molecule inhibitors revealed by single-cell analysis",
"author": "Vogel",
"doi-asserted-by": "crossref",
"first-page": "12428",
"journal-title": "Nat. Commun.",
"key": "10.1016/j.cell.2020.10.039_bib82",
"volume": "7",
"year": "2016"
},
{
"DOI": "10.1128/JVI.00015-19",
"article-title": "The Infectious Bronchitis Coronavirus Envelope Protein Alters Golgi pH To Protect the Spike Protein and Promote the Release of Infectious Virus",
"author": "Westerbeck",
"doi-asserted-by": "crossref",
"first-page": "e00015",
"journal-title": "J. Virol.",
"key": "10.1016/j.cell.2020.10.039_bib83",
"volume": "93",
"year": "2019"
},
{
"DOI": "10.1038/s41586-020-2423-5",
"article-title": "Clinical benefit of remdesivir in rhesus macaques infected with SARS-CoV-2",
"author": "Williamson",
"doi-asserted-by": "crossref",
"first-page": "273",
"journal-title": "Nature",
"key": "10.1016/j.cell.2020.10.039_bib84",
"volume": "585",
"year": "2020"
},
{
"DOI": "10.1177/1087057113501197",
"article-title": "A phenotypic compound screening assay for lysosomal storage diseases",
"author": "Xu",
"doi-asserted-by": "crossref",
"first-page": "168",
"journal-title": "J. Biomol. Screen.",
"key": "10.1016/j.cell.2020.10.039_bib85",
"volume": "19",
"year": "2014"
},
{
"DOI": "10.1038/s41419-018-0917-y",
"article-title": "SARS-Coronavirus Open Reading Frame-3a drives multimodal necrotic cell death",
"author": "Yue",
"doi-asserted-by": "crossref",
"first-page": "904",
"journal-title": "Cell Death Dis.",
"key": "10.1016/j.cell.2020.10.039_bib86",
"volume": "9",
"year": "2018"
},
{
"DOI": "10.1016/j.cell.2020.04.035",
"article-title": "SARS-CoV-2 Receptor ACE2 Is an Interferon-Stimulated Gene in Human Airway Epithelial Cells and Is Detected in Specific Cell Subsets across Tissues",
"author": "Ziegler",
"doi-asserted-by": "crossref",
"first-page": "1016",
"journal-title": "Cell",
"key": "10.1016/j.cell.2020.10.039_bib87",
"volume": "181",
"year": "2020"
}
],
"reference-count": 87,
"references-count": 87,
"relation": {
"has-review": [
{
"asserted-by": "object",
"id": "10.3410/f.738910917.793580494",
"id-type": "doi"
},
{
"asserted-by": "object",
"id": "10.3410/f.738910917.793580302",
"id-type": "doi"
},
{
"asserted-by": "object",
"id": "10.3410/f.738910917.793583046",
"id-type": "doi"
},
{
"asserted-by": "object",
"id": "10.3410/f.738910917.793580051",
"id-type": "doi"
}
]
},
"resource": {
"primary": {
"URL": "https://linkinghub.elsevier.com/retrieve/pii/S009286742031446X"
}
},
"score": 1,
"short-title": [],
"source": "Crossref",
"subject": [],
"subtitle": [],
"title": "β-Coronaviruses Use Lysosomes for Egress Instead of the Biosynthetic Secretory Pathway",
"type": "journal-article",
"update-policy": "http://dx.doi.org/10.1016/elsevier_cm_policy",
"volume": "183"
}