Acidic pH of Early Endosomes Governs SARS-CoV-2 Transport in Host Cells
Perla Fares, Mariam Duhaini, Suvranta K Tripathy, Ali Srour, Ph.D Kalyan C Kondapalli
Journal of Biological Chemistry, doi:10.1016/j.jbc.2024.108144
Endocytosis is a prominent mechanism for SARS-CoV-2 entry into host cells. Upon internalization into early endosomes (EEs), the virus is transported to late endosomes (LEs), where acidic conditions facilitate spike protein processing and viral genome release. Dynein and kinesin motors drive EE transport along microtubules; dynein moves EEs to the perinuclear region, while kinesins direct them towards the plasma membrane, creating a tug-ofwar over the direction of transport. Here, we identify that luminal pH of EEs is a key factor regulating the outcome of this tug-of-war. Among the known endosomal pH regulators, only the sodium-proton exchanger NHE9 has so far been genetically linked to severe COVID-19 risk. NHE9 functions as a proton leak pathway specifically on endosomes. We show that limiting acidification of EEs by increasing the expression of NHE9 leads to decreased infectivity of the SARS-CoV-2 spike-bearing virus in host cells. Our investigation identified the EE membrane lipid phosphatidylinositol-3-phosphate (PI3P) as a link between luminal pH changes and EE transport. Normally, as EEs mature, PI3P depletes. However, in cells with high NHE9 expression, PI3P persists longer on EEs. PI3P plays a pivotal role in the recruitment of motor proteins and the subsequent movement of EEs. Consistently, we observed NHE9 mediated alkalization of EEs hindered perinuclear movement. Specifically, EE speed and run-length were negatively impacted, ultimately leading to EEs falling off microtubules and impairing the delivery of viral cargo to LEs. NHE9 thus offers a unique opportunity as a viable therapeutic target to impede SARS-CoV-2 host cell entry.
Conflict of Interest The authors declare that they have no conflicts of interest with the contents of the article.
Author Contributions Conception and design: K.C.K; Acquisition of data: P.F., M.D. , and A.S.; Analysis of data: P.F., M.D., S.K.T., A.S., and KCK ; Writing the manuscript: K.C.K. and P.F. ; All authors approved the final version of the manuscript.
Conflict of Interest The authors declare that they have no conflicts of interest with the contents of the article. J o u r n a l P r e -p r o o f
References
Bayati, Kumar, Francis, Mcpherson, SARS-CoV-2 infects cells after viral entry via clathrin-mediated endocytosis, J Biol Chem
Beydoun, Hamood, Gomez Zubieta, Kondapalli, Na(+)/h(+) exchanger 9 regulates iron mobilization at the blood-brain barrier in response to iron starvation, J Biol Chem
Bourdoncle, Laummonerie, Mutterer, Colocalization finder Institut Jacques Monod
Bright, Gratian, Luzio, Endocytic delivery to lysosomes mediated by concurrent fusion and kissing events in living cells, Curr Biol
Daczkowski, Dzimianski, Clasman, Goodwin, Mesecar, Structural insights into the interaction of coronavirus papain-like proteases and interferon-stimulated gene product 15 from different species, J Mol Biol
Di Paolo, Camilli, Phosphoinositides in cell regulation and membrane dynamics, Nature
Dolman, A review of reagents for fluorescence microscopy of cellular compartments and structures, part i: Bacmam labeling and reagents for vesicular structures, Curr Protoc
Dowling, Vreede, Low, Gibbs, Kuwada et al., Loss of myotubularin function results in T-tubule disorganization in zebrafish and human myotubular myopathy, PLoS Genet
Esposito, Sorosina, Ottoboni, Lim, Replogle et al., A pharmacogenetic study implicates SLC9a9 in multiple sclerosis disease activity, Ann Neurol
Flessner, Orlowski, Na+/H+ exchangers In Encyclopedia of Molecular Pharmacology
Freeman, Grinstein, Orlowski, Determinants, maintenance, and function of organellar pH, Physiol Rev
Gomez Zubieta, Hamood, Beydoun, Pall, Kondapalli, MicroRNA-135a regulates NHE9 to inhibit proliferation and migration of glioblastoma cells, Cell Commun Signal
Granger, Mcnee, Allan, The role of the cytoskeleton and molecular motors in endosomal dynamics, Semin Cell Dev Biol
Gruenberg, Lipids in endocytic membrane transport and sorting, Curr Opin Cell Biol
Hammond, DepHining membrane identity, J Cell Biol
Hoffmann, Kleine-Weber, Schroeder, Kruger, Herrler et al., SARS-COV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor, Cell
Jackson, Farzan, Chen, Mechanisms of SARS-CoV-2 entry into cells, Nat Rev Mol Cell Biol
Jaqaman, Loerke, Mettlen, Kuwata, Grinstein et al., Robust single-particle tracking in live-cell time-lapse sequences, Nat Methods
Katze, He, Jr, Viruses and interferon: a fight for supremacy, Nat Rev Immunol
Kondapalli, Hack, Schushan, Landau, Ben-Tal et al., Functional evaluation of autism-associated mutations in NHE9, Nat Commun
Kondapalli, Llongueras, Capilla-Gonzalez, Prasad, Hack et al., A leak pathway for luminal protons in endosomes drives oncogenic signalling in glioblastoma, Nat Commun
Kondapalli, Prasad, Rao, An inside job: how endosomal Na(+)/H(+) exchangers link to autism and neurological disease, Front Cell Neurosci
Kreutzberger, Sanyal, Saminathan, Bloyet, Stumpf et al., SARS-CoV-2 requires acidic pH to infect cells, Proc Natl Acad Sci U S A
Lee, Kang, Von Ballmoos, Newstead, Uzdavinys et al., A two-domain elevator mechanism for sodium/proton antiport, Nature
Li, Guan, Wu, Wang, Zhou et al., Early transmission dynamics in Wuhan, China, of Novel Coronavirus-Infected Pneumonia, N Engl J Med
Li, Stolz, Characterization of endocytic vesicles using magnetic microbeads coated with signaling ligands, Traffic,
doi:115010.1111/tra.12424Li, Zhu, Fan, Zhang, Peng et al., Dependence of SARS-CoV-2 infection on cholesterol-rich lipid raft and endosomal acidification, Comput Struct Biotechnol J
Masre, Jufri, Ibrahim, Andabdul Raub, Classical and alternative receptors for SARS-CoV-2 therapeutic strategy, Rev Med Virol
Maxson, Grinstein, The vacuolar-type h(+)-atpase at a glance -more than a proton pump, J Cell Sci
Naufer, Hipolito, Ganesan, Prashar, Zaremberg et al., pH of endophagosomes controls association of their membranes with Vps34 and PtdIns(3)P levels, J Cell Biol
Nobukuni, Joaquin, Roccio, Dann, Kim et al., Amino acids mediate mTOR/raptor signaling through activation of class 3 phosphatidylinositol 3OHkinase, Proc Natl Acad Sci U S A
Pall, Juratli, Guntur, Bandyopadhyay, Kondapalli, A gain of function paradox: Targeted therapy for glioblastoma associated with abnormal NHE9 expression, J Cell Mol Med
Pathak, Mallik, Lipid -motor interactions: Soap opera or symphony?, Curr Opin Cell Biol
Pedersen, The SLC9A-C mammalian Na(+)/H(+) Exchanger family: Molecules, mechanisms, and physiology, Physiol Rev
Posey, Blaisdell-Pijuan, Knoll, Saif, Small-scale displacement fluctuations of vesicles in fibroblasts, Sci Rep
Prasad, Protons to Patients: targeting endosomal Na(+) /H(+) exchangers against COVID-19 and other viral diseases, FEBS J
Rai, Pathak, Thakur, Singh, Dubey et al., Dynein Clusters into Lipid Microdomains on Phagosomes to Drive Rapid Transport toward Lysosomes, Cell
Schneider, Rasband, Eliceiri, NIH image to ImageJ: 25 years of image analysis, Nat Methods
Shamroukh, Lone, Akhtar, Altayib, Sutliff et al., The sodium proton exchanger NHE9 regulates phagosome maturation and bactericidal activity in macrophages, J Biol Chem
Shang, Wan, Luo, Ye, Geng et al., Cell entry mechanisms of SARS-CoV-2, Proc Natl Acad Sci U S A
Steinberg, Grinstein, Pathogen destruction versus intracellular survival: the role of lipids as phagosomal fate determinants, J Clin Invest
Tinevez, Perry, Schindelin, Hoopes, Reynolds et al., TrackMate: An open and extensible platform for single-particle tracking, Methods
Tirumala, Redpath, Skerhut, Dolai, Kapoor-Kaushik et al., Single-molecule imaging of stochastic interactions that drive dynein activation and cargo movement in cells, J Cell Biol
Tirumala, Visualization of single dynein molecules in mammalian cells, Methods Mol Biol
Tokunaga, Imamoto, Sakata-Sogawa, Highly inclined thin illumination enables clear single-molecule imaging in cells, Nat Methods
Velazquez-Salinas, The complex evolutionary dynamics of SARS-CoV-2, a big challenge to control the pandemic of COVID-19, J Med Virol
Wang, Horby, Hayden, A novel coronavirus outbreak of global health concern, Lancet
Wassmer, Attar, Harterink, Van Weering, Traer et al., The retromer coat complex coordinates endosomal sorting and dynein-mediated transport, with carrier recognition by the trans-Golgi network, Dev Cell
Wen, Zhang, Lin, Shi, Cytoskeleton-a crucial key in host cell for coronavirus infection, J Mol Cell Biol
Winklemann, Matsuoka, Meier, Shutin, Zhang et al., Structure and elevator mechanism of the mammalian sodium/proton exchanger NHE9, EMBO J
Yang, Jia, Meng, Xue, Liu et al., SNX27 suppresses SARS-CoV-2 infection by inhibiting viral lysosome/late endosome entry, Proc Natl Acad Sci U S A
Yoshikawa, Hill, Yoshikawa, Popov, Galindo et al., Dynamic innate immune responses of human bronchial epithelial cells to severe acute respiratory syndrome-associated coronavirus infection, PLoS One
Zornetta, Brandi, Janowiak, Dal Molin, Tonello et al., Imaging the cell entry of the anthrax oedema and lethal toxins with fluorescent protein chimeras, Cell Microbiol
{ 'indexed': { 'date-parts': [[2024, 12, 27]],
'date-time': '2024-12-27T00:10:35Z',
'timestamp': 1735258235524,
'version': '3.32.0'},
'reference-count': 54,
'publisher': 'Elsevier BV',
'license': [ { 'start': { 'date-parts': [[2024, 12, 1]],
'date-time': '2024-12-01T00:00:00Z',
'timestamp': 1733011200000},
'content-version': 'tdm',
'delay-in-days': 0,
'URL': 'https://www.elsevier.com/tdm/userlicense/1.0/'},
{ 'start': { 'date-parts': [[2024, 12, 1]],
'date-time': '2024-12-01T00:00:00Z',
'timestamp': 1733011200000},
'content-version': 'tdm',
'delay-in-days': 0,
'URL': 'https://www.elsevier.com/legal/tdmrep-license'},
{ 'start': { 'date-parts': [[2024, 12, 25]],
'date-time': '2024-12-25T00:00:00Z',
'timestamp': 1735084800000},
'content-version': 'vor',
'delay-in-days': 24,
'URL': 'http://creativecommons.org/licenses/by/4.0/'}],
'content-domain': { 'domain': ['jbc.org', 'elsevier.com', 'sciencedirect.com'],
'crossmark-restriction': True},
'published-print': {'date-parts': [[2024, 12]]},
'DOI': '10.1016/j.jbc.2024.108144',
'type': 'journal-article',
'created': { 'date-parts': [[2024, 12, 26]],
'date-time': '2024-12-26T23:52:41Z',
'timestamp': 1735257161000},
'page': '108144',
'update-policy': 'https://doi.org/10.1016/elsevier_cm_policy',
'source': 'Crossref',
'is-referenced-by-count': 0,
'title': 'Acidic pH of Early Endosomes Governs SARS-CoV-2 Transport in Host Cells',
'prefix': '10.1016',
'author': [ {'given': 'Perla', 'family': 'Fares', 'sequence': 'first', 'affiliation': []},
{'given': 'Mariam', 'family': 'Duhaini', 'sequence': 'additional', 'affiliation': []},
{ 'ORCID': 'https://orcid.org/0000-0002-6658-1691',
'authenticated-orcid': False,
'given': 'Suvranta K.',
'family': 'Tripathy',
'sequence': 'additional',
'affiliation': []},
{'given': 'Ali', 'family': 'Srour', 'sequence': 'additional', 'affiliation': []},
{ 'ORCID': 'https://orcid.org/0000-0003-1242-9990',
'authenticated-orcid': False,
'given': 'Kalyan C.',
'family': 'Kondapalli',
'sequence': 'additional',
'affiliation': []}],
'member': '78',
'reference': [ { 'key': '10.1016/j.jbc.2024.108144_bib1',
'doi-asserted-by': 'crossref',
'first-page': '1199',
'DOI': '10.1056/NEJMoa2001316',
'article-title': 'Early transmission dynamics in Wuhan, China, of Novel '
'Coronavirus-Infected',
'volume': '382',
'author': 'Li',
'year': '2020',
'journal-title': 'Pneumonia N Engl J Med'},
{ 'key': '10.1016/j.jbc.2024.108144_bib2',
'doi-asserted-by': 'crossref',
'first-page': '470',
'DOI': '10.1016/S0140-6736(20)30185-9',
'article-title': 'A novel coronavirus outbreak of global health concern',
'volume': '395',
'author': 'Wang',
'year': '2020',
'journal-title': 'Lancet'},
{ 'key': '10.1016/j.jbc.2024.108144_bib3',
'doi-asserted-by': 'crossref',
'first-page': '5082',
'DOI': '10.1002/jmv.27979',
'article-title': 'The complex evolutionary dynamics of SARS-CoV-2, a big challenge to '
'control the pandemic of COVID-19',
'volume': '94',
'author': 'Velazquez-Salinas',
'year': '2022',
'journal-title': 'J Med Virol'},
{ 'key': '10.1016/j.jbc.2024.108144_bib4',
'doi-asserted-by': 'crossref',
'first-page': '3',
'DOI': '10.1038/s41580-021-00418-x',
'article-title': 'Mechanisms of SARS-CoV-2 entry into cells',
'volume': '23',
'author': 'Jackson',
'year': '2022',
'journal-title': 'Nat Rev Mol Cell Biol'},
{ 'key': '10.1016/j.jbc.2024.108144_bib5',
'doi-asserted-by': 'crossref',
'unstructured': 'Hoffmann, M., Kleine-Weber, H., Schroeder, S., Kruger, N., Herrler, T., '
'Erichsen, S. et al. (2020) SARS-COV-2 cell entry depends on ACE2 and '
'TMPRSS2 and is blocked by a clinically proven protease inhibitor Cell '
'181, 271-280e278 10.1016/j.cell.2020.02.052',
'DOI': '10.1016/j.cell.2020.02.052'},
{ 'key': '10.1016/j.jbc.2024.108144_bib6',
'doi-asserted-by': 'crossref',
'first-page': '11727',
'DOI': '10.1073/pnas.2003138117',
'article-title': 'Cell entry mechanisms of SARS-CoV-2',
'volume': '117',
'author': 'Shang',
'year': '2020',
'journal-title': 'Proc Natl Acad Sci U S A'},
{ 'key': '10.1016/j.jbc.2024.108144_bib7',
'article-title': 'SNX27 suppresses SARS-CoV-2 infection by inhibiting viral lysosome/late '
'endosome entry',
'volume': '119',
'author': 'Yang',
'year': '2022',
'journal-title': 'Proc Natl Acad Sci U S A'},
{ 'key': '10.1016/j.jbc.2024.108144_bib8',
'doi-asserted-by': 'crossref',
'DOI': '10.1073/pnas.2209514119',
'article-title': 'SARS-CoV-2 requires acidic pH to infect cells',
'volume': '119',
'author': 'Kreutzberger',
'year': '2022',
'journal-title': 'Proc Natl Acad Sci U S A'},
{ 'key': '10.1016/j.jbc.2024.108144_bib9',
'doi-asserted-by': 'crossref',
'DOI': '10.1016/j.jbc.2021.100306',
'article-title': 'SARS-CoV-2 infects cells after viral entry via clathrin-mediated '
'endocytosis',
'volume': '296',
'author': 'Bayati',
'year': '2021',
'journal-title': 'J Biol Chem'},
{ 'key': '10.1016/j.jbc.2024.108144_bib10',
'doi-asserted-by': 'crossref',
'first-page': '968',
'DOI': '10.1093/jmcb/mjaa042',
'article-title': 'Cytoskeleton-a crucial key in host cell for coronavirus infection',
'volume': '12',
'author': 'Wen',
'year': '2020',
'journal-title': 'J Mol Cell Biol'},
{ 'key': '10.1016/j.jbc.2024.108144_bib11',
'doi-asserted-by': 'crossref',
'DOI': '10.1016/j.jbc.2022.102150',
'article-title': 'The sodium proton exchanger NHE9 regulates phagosome maturation and '
'bactericidal activity in macrophages',
'volume': '298',
'author': 'Shamroukh',
'year': '2022',
'journal-title': 'J Biol Chem'},
{ 'key': '10.1016/j.jbc.2024.108144_bib12',
'doi-asserted-by': 'crossref',
'first-page': '1933',
'DOI': '10.1016/j.csbj.2021.04.001',
'article-title': 'Dependence of SARS-CoV-2 infection on cholesterol-rich lipid raft and '
'endosomal acidification',
'volume': '19',
'author': 'Li',
'year': '2021',
'journal-title': 'Comput Struct Biotechnol J'},
{ 'key': '10.1016/j.jbc.2024.108144_bib13',
'doi-asserted-by': 'crossref',
'first-page': '4987',
'DOI': '10.1242/jcs.158550',
'article-title': 'The vacuolar-type h(+)-atpase at a glance - more than a proton pump',
'volume': '127',
'author': 'Maxson',
'year': '2014',
'journal-title': 'J Cell Sci'},
{ 'key': '10.1016/j.jbc.2024.108144_bib14',
'doi-asserted-by': 'crossref',
'first-page': '515',
'DOI': '10.1152/physrev.00009.2022',
'article-title': 'Determinants, maintenance, and function of organellar pH',
'volume': '103',
'author': 'Freeman',
'year': '2023',
'journal-title': 'Physiol Rev'},
{ 'key': '10.1016/j.jbc.2024.108144_bib15',
'article-title': 'Structure and elevator mechanism of the mammalian sodium/proton '
'exchanger NHE9',
'volume': '39',
'author': 'Winklemann',
'year': '2020',
'journal-title': 'EMBO J'},
{ 'key': '10.1016/j.jbc.2024.108144_bib16',
'doi-asserted-by': 'crossref',
'first-page': '2015',
'DOI': '10.1152/physrev.00028.2018',
'article-title': 'The SLC9A-C mammalian Na(+)/H(+) Exchanger family: Molecules, '
'mechanisms, and physiology',
'volume': '99',
'author': 'Pedersen',
'year': '2019',
'journal-title': 'Physiol Rev'},
{ 'key': '10.1016/j.jbc.2024.108144_bib17',
'doi-asserted-by': 'crossref',
'first-page': '4293',
'DOI': '10.1074/jbc.M116.769240',
'article-title': 'Na(+)/h(+) exchanger 9 regulates iron mobilization at the blood-brain '
'barrier in response to iron starvation',
'volume': '292',
'author': 'Beydoun',
'year': '2017',
'journal-title': 'J Biol Chem'},
{ 'key': '10.1016/j.jbc.2024.108144_bib18',
'doi-asserted-by': 'crossref',
'first-page': '6289',
'DOI': '10.1038/ncomms7289',
'article-title': 'A leak pathway for luminal protons in endosomes drives oncogenic '
'signalling in glioblastoma',
'volume': '6',
'author': 'Kondapalli',
'year': '2015',
'journal-title': 'Nat Commun'},
{ 'key': '10.1016/j.jbc.2024.108144_bib19',
'doi-asserted-by': 'crossref',
'first-page': '172',
'DOI': '10.3389/fncel.2014.00172',
'article-title': 'An inside job: how endosomal Na(+)/H(+) exchangers link to autism and '
'neurological disease',
'volume': '8',
'author': 'Kondapalli',
'year': '2014',
'journal-title': 'Front Cell Neurosci'},
{ 'key': '10.1016/j.jbc.2024.108144_bib20',
'doi-asserted-by': 'crossref',
'first-page': '5071',
'DOI': '10.1111/febs.16163',
'article-title': 'Protons to Patients: targeting endosomal Na(+) /H(+) exchangers against '
'COVID-19 and other viral diseases',
'volume': '288',
'author': 'Prasad',
'year': '2021',
'journal-title': 'FEBS J'},
{ 'key': '10.1016/j.jbc.2024.108144_bib21',
'doi-asserted-by': 'crossref',
'unstructured': 'Li, H. S., Stolz, D. B., and Romero, G. (2016) Characterization of '
'endocytic vesicles using magnetic microbeads coated with signaling '
'ligands Traffic 17, 1150 10.1111/tra.12424',
'DOI': '10.1111/tra.12424'},
{ 'key': '10.1016/j.jbc.2024.108144_bib22',
'doi-asserted-by': 'crossref',
'first-page': '573',
'DOI': '10.1038/nature12484',
'article-title': 'A two-domain elevator mechanism for sodium/proton antiport',
'volume': '501',
'author': 'Lee',
'year': '2013',
'journal-title': 'Nature'},
{ 'key': '10.1016/j.jbc.2024.108144_bib23',
'doi-asserted-by': 'crossref',
'first-page': '2510',
'DOI': '10.1038/ncomms3510',
'article-title': 'Functional evaluation of autism-associated mutations in NHE9',
'volume': '4',
'author': 'Kondapalli',
'year': '2013',
'journal-title': 'Nat Commun'},
{ 'key': '10.1016/j.jbc.2024.108144_bib24',
'doi-asserted-by': 'crossref',
'unstructured': 'Flessner, R., and Orlowski, J. (2021) Na+/H+ exchangers In Encyclopedia '
'of Molecular Pharmacology, Offermanns S, Rosenthal W, eds. Springer '
'International Publishing, Cham 1047-1062',
'DOI': '10.1007/978-3-030-57401-7_193'},
{ 'key': '10.1016/j.jbc.2024.108144_bib25',
'doi-asserted-by': 'crossref',
'first-page': '360',
'DOI': '10.1016/j.cub.2005.01.049',
'article-title': 'Endocytic delivery to lysosomes mediated by concurrent fusion and '
'kissing events in living cells',
'volume': '15',
'author': 'Bright',
'year': '2005',
'journal-title': 'Curr Biol'},
{ 'key': '10.1016/j.jbc.2024.108144_bib26',
'doi-asserted-by': 'crossref',
'unstructured': 'Dolman, N. J., and Kilgore, J. A. (2023) A review of reagents for '
'fluorescence microscopy of cellular compartments and structures, part i: '
'Bacmam labeling and reagents for vesicular structures Curr Protoc 3, '
'e751 10.1002/cpz1.751',
'DOI': '10.1002/cpz1.751'},
{ 'key': '10.1016/j.jbc.2024.108144_bib27',
'doi-asserted-by': 'crossref',
'first-page': '651',
'DOI': '10.1038/nature05185',
'article-title': 'Phosphoinositides in cell regulation and membrane dynamics',
'volume': '443',
'author': 'Di Paolo',
'year': '2006',
'journal-title': 'Nature'},
{ 'key': '10.1016/j.jbc.2024.108144_bib28',
'doi-asserted-by': 'crossref',
'first-page': '382',
'DOI': '10.1016/S0955-0674(03)00078-4',
'article-title': 'Lipids in endocytic membrane transport and sorting',
'volume': '15',
'author': 'Gruenberg',
'year': '2003',
'journal-title': 'Curr Opin Cell Biol'},
{ 'key': '10.1016/j.jbc.2024.108144_bib29',
'doi-asserted-by': 'crossref',
'DOI': '10.1242/jcs.259689',
'article-title': 'Choreographing the motor-driven endosomal dance',
'volume': '136',
'author': 'Jongsma',
'year': '2023',
'journal-title': 'J Cell Sci'},
{ 'key': '10.1016/j.jbc.2024.108144_bib30',
'doi-asserted-by': 'crossref',
'first-page': '79',
'DOI': '10.1016/j.ceb.2016.09.005',
'article-title': 'Lipid - motor interactions: Soap opera or symphony?',
'volume': '44',
'author': 'Pathak',
'year': '2017',
'journal-title': 'Curr Opin Cell Biol'},
{ 'key': '10.1016/j.jbc.2024.108144_bib31',
'doi-asserted-by': 'crossref',
'first-page': '329',
'DOI': '10.1083/jcb.201702179',
'article-title': 'pH of endophagosomes controls association of their membranes with Vps34 '
'and PtdIns(3)P levels',
'volume': '217',
'author': 'Naufer',
'year': '2018',
'journal-title': 'J Cell Biol'},
{ 'key': '10.1016/j.jbc.2024.108144_bib32',
'doi-asserted-by': 'crossref',
'first-page': '19',
'DOI': '10.1083/jcb.201711134',
'article-title': 'DepHining membrane identity',
'volume': '217',
'author': 'Hammond',
'year': '2018',
'journal-title': 'J Cell Biol'},
{ 'key': '10.1016/j.jbc.2024.108144_bib33',
'doi-asserted-by': 'crossref',
'first-page': '159',
'DOI': '10.1038/nmeth1171',
'article-title': 'Highly inclined thin illumination enables clear single-molecule imaging '
'in cells',
'volume': '5',
'author': 'Tokunaga',
'year': '2008',
'journal-title': 'Nat Methods'},
{ 'key': '10.1016/j.jbc.2024.108144_bib34',
'doi-asserted-by': 'crossref',
'DOI': '10.1083/jcb.202210026',
'article-title': 'Single-molecule imaging of stochastic interactions that drive dynein '
'activation and cargo movement in cells',
'volume': '223',
'author': 'Tirumala',
'year': '2024',
'journal-title': 'J Cell Biol'},
{ 'key': '10.1016/j.jbc.2024.108144_bib35',
'doi-asserted-by': 'crossref',
'DOI': '10.1038/s41598-018-31656-3',
'article-title': 'Small-scale displacement fluctuations of vesicles in fibroblasts',
'volume': '8',
'author': 'Posey',
'year': '2018',
'journal-title': 'Sci Rep'},
{ 'key': '10.1016/j.jbc.2024.108144_bib36',
'doi-asserted-by': 'crossref',
'first-page': '675',
'DOI': '10.1038/nri888',
'article-title': 'Viruses and interferon: a fight for supremacy',
'volume': '2',
'author': 'Katze',
'year': '2002',
'journal-title': 'Nat Rev Immunol'},
{ 'key': '10.1016/j.jbc.2024.108144_bib37',
'doi-asserted-by': 'crossref',
'first-page': '115',
'DOI': '10.1002/ana.24429',
'article-title': 'A pharmacogenetic study implicates SLC9a9 in multiple sclerosis disease '
'activity',
'volume': '78',
'author': 'Esposito',
'year': '2015',
'journal-title': 'Ann Neurol'},
{ 'key': '10.1016/j.jbc.2024.108144_bib38',
'doi-asserted-by': 'crossref',
'first-page': '1661',
'DOI': '10.1016/j.jmb.2017.04.011',
'article-title': 'Structural insights into the interaction of coronavirus papain-like '
'proteases and interferon-stimulated gene product 15 from different '
'species',
'volume': '429',
'author': 'Daczkowski',
'year': '2017',
'journal-title': 'J Mol Biol'},
{ 'key': '10.1016/j.jbc.2024.108144_bib39',
'doi-asserted-by': 'crossref',
'DOI': '10.1371/journal.pone.0008729',
'article-title': 'Dynamic innate immune responses of human bronchial epithelial cells to '
'severe acute respiratory syndrome-associated coronavirus infection',
'volume': '5',
'author': 'Yoshikawa',
'year': '2010',
'journal-title': 'PLoS One'},
{ 'key': '10.1016/j.jbc.2024.108144_bib40',
'doi-asserted-by': 'crossref',
'first-page': '1',
'DOI': '10.1002/rmv.2207',
'article-title': 'Classical and alternative receptors for SARS-CoV-2 therapeutic strategy',
'volume': '31',
'author': 'Masre',
'year': '2021',
'journal-title': 'Rev Med Virol'},
{ 'key': '10.1016/j.jbc.2024.108144_bib41',
'doi-asserted-by': 'crossref',
'first-page': '20',
'DOI': '10.1016/j.semcdb.2014.04.011',
'article-title': 'The role of the cytoskeleton and molecular motors in endosomal dynamics',
'volume': '31',
'author': 'Granger',
'year': '2014',
'journal-title': 'Semin Cell Dev Biol'},
{ 'key': '10.1016/j.jbc.2024.108144_bib42',
'doi-asserted-by': 'crossref',
'first-page': '2002',
'DOI': '10.1172/JCI35433',
'article-title': 'Pathogen destruction versus intracellular survival: the role of lipids '
'as phagosomal fate determinants',
'volume': '118',
'author': 'Steinberg',
'year': '2008',
'journal-title': 'J Clin Invest'},
{ 'key': '10.1016/j.jbc.2024.108144_bib43',
'doi-asserted-by': 'crossref',
'first-page': '110',
'DOI': '10.1016/j.devcel.2009.04.016',
'article-title': 'The retromer coat complex coordinates endosomal sorting and '
'dynein-mediated transport, with carrier recognition by the trans-Golgi '
'network',
'volume': '17',
'author': 'Wassmer',
'year': '2009',
'journal-title': 'Dev Cell'},
{ 'key': '10.1016/j.jbc.2024.108144_bib44',
'doi-asserted-by': 'crossref',
'first-page': '722',
'DOI': '10.1016/j.cell.2015.12.054',
'article-title': 'Dynein Clusters into Lipid Microdomains on Phagosomes to Drive Rapid '
'Transport toward Lysosomes',
'volume': '164',
'author': 'Rai',
'year': '2016',
'journal-title': 'Cell'},
{ 'key': '10.1016/j.jbc.2024.108144_bib45',
'doi-asserted-by': 'crossref',
'first-page': '55',
'DOI': '10.1186/s12964-017-0209-7',
'article-title': 'MicroRNA-135a regulates NHE9 to inhibit proliferation and migration of '
'glioblastoma cells',
'volume': '15',
'author': 'Gomez Zubieta',
'year': '2017',
'journal-title': 'Cell Commun Signal'},
{ 'key': '10.1016/j.jbc.2024.108144_bib46',
'doi-asserted-by': 'crossref',
'DOI': '10.1111/jcmm.14665',
'article-title': 'A gain of function paradox: Targeted therapy for glioblastoma '
'associated with abnormal NHE9 expression',
'author': 'Pall',
'year': '2019',
'journal-title': 'J Cell Mol Med'},
{ 'key': '10.1016/j.jbc.2024.108144_bib47',
'doi-asserted-by': 'crossref',
'first-page': '671',
'DOI': '10.1038/nmeth.2089',
'article-title': 'NIH image to ImageJ: 25 years of image analysis',
'volume': '9',
'author': 'Schneider',
'year': '2012',
'journal-title': 'Nat Methods'},
{ 'key': '10.1016/j.jbc.2024.108144_bib48',
'doi-asserted-by': 'crossref',
'DOI': '10.1371/journal.pgen.1000372',
'article-title': 'Loss of myotubularin function results in T-tubule disorganization in '
'zebrafish and human myotubular myopathy',
'volume': '5',
'author': 'Dowling',
'year': '2009',
'journal-title': 'PLoS Genet'},
{ 'key': '10.1016/j.jbc.2024.108144_bib49',
'doi-asserted-by': 'crossref',
'first-page': '14238',
'DOI': '10.1073/pnas.0506925102',
'article-title': 'Amino acids mediate mTOR/raptor signaling through activation of class 3 '
'phosphatidylinositol 3OH-kinase',
'volume': '102',
'author': 'Nobukuni',
'year': '2005',
'journal-title': 'Proc Natl Acad Sci U S A'},
{ 'key': '10.1016/j.jbc.2024.108144_bib50',
'doi-asserted-by': 'crossref',
'unstructured': 'Zornetta, I., Brandi, L., Janowiak, B., Dal Molin, F., Tonello, F., '
'Collier, R. J. et al. (2010) Imaging the cell entry of the anthrax '
'oedema and lethal toxins with fluorescent protein chimeras Cell '
'Microbiol 12, 1435-1445 10.1111/j.1462-5822.2010.01480.x',
'DOI': '10.1111/j.1462-5822.2010.01480.x'},
{ 'key': '10.1016/j.jbc.2024.108144_bib51',
'unstructured': 'Bourdoncle, P., Laummonerie, C., Mutterer, J. (2003) Colocalization '
'finder Institut Jacques Monod, Service Imagerie, CNRS, University Paris '
'Diderot, Paris, France.'},
{ 'key': '10.1016/j.jbc.2024.108144_bib52',
'first-page': '87',
'article-title': 'Visualization of single dynein molecules in mammalian cells Methods',
'volume': '2623',
'author': 'Tirumala',
'year': '2023',
'journal-title': 'Mol Biol'},
{ 'key': '10.1016/j.jbc.2024.108144_bib53',
'doi-asserted-by': 'crossref',
'first-page': '695',
'DOI': '10.1038/nmeth.1237',
'article-title': 'Robust single-particle tracking in live-cell time-lapse sequences',
'volume': '5',
'author': 'Jaqaman',
'year': '2008',
'journal-title': 'Nat Methods'},
{ 'key': '10.1016/j.jbc.2024.108144_bib54',
'doi-asserted-by': 'crossref',
'first-page': '80',
'DOI': '10.1016/j.ymeth.2016.09.016',
'article-title': 'TrackMate: An open and extensible platform for single-particle tracking',
'volume': '115',
'author': 'Tinevez',
'year': '2017',
'journal-title': 'Methods'}],
'container-title': 'Journal of Biological Chemistry',
'original-title': [],
'language': 'en',
'link': [ { 'URL': 'https://api.elsevier.com/content/article/PII:S0021925824026462?httpAccept=text/xml',
'content-type': 'text/xml',
'content-version': 'vor',
'intended-application': 'text-mining'},
{ 'URL': 'https://api.elsevier.com/content/article/PII:S0021925824026462?httpAccept=text/plain',
'content-type': 'text/plain',
'content-version': 'vor',
'intended-application': 'text-mining'}],
'deposited': { 'date-parts': [[2024, 12, 26]],
'date-time': '2024-12-26T23:52:54Z',
'timestamp': 1735257174000},
'score': 1,
'resource': {'primary': {'URL': 'https://linkinghub.elsevier.com/retrieve/pii/S0021925824026462'}},
'subtitle': [],
'short-title': [],
'issued': {'date-parts': [[2024, 12]]},
'references-count': 54,
'alternative-id': ['S0021925824026462'],
'URL': 'http://dx.doi.org/10.1016/j.jbc.2024.108144',
'relation': {},
'ISSN': ['0021-9258'],
'subject': [],
'container-title-short': 'Journal of Biological Chemistry',
'published': {'date-parts': [[2024, 12]]},
'assertion': [ {'value': 'Elsevier', 'name': 'publisher', 'label': 'This article is maintained by'},
{ 'value': 'Acidic pH of Early Endosomes Governs SARS-CoV-2 Transport in Host Cells',
'name': 'articletitle',
'label': 'Article Title'},
{ 'value': 'Journal of Biological Chemistry',
'name': 'journaltitle',
'label': 'Journal Title'},
{ 'value': 'https://doi.org/10.1016/j.jbc.2024.108144',
'name': 'articlelink',
'label': 'CrossRef DOI link to publisher maintained version'},
{'value': 'article', 'name': 'content_type', 'label': 'Content Type'},
{ 'value': '© 2024 THE AUTHORS. Published by Elsevier Inc on behalf of American Society for '
'Biochemistry and Molecular Biology.',
'name': 'copyright',
'label': 'Copyright'}],
'article-number': '108144'}
