{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,23]],"date-time":"2026-04-23T14:30:12Z","timestamp":1776954612633,"version":"3.51.4"},"reference-count":109,"publisher":"MDPI AG","issue":"16","license":[{"start":{"date-parts":[[2020,8,13]],"date-time":"2020-08-13T00:00:00Z","timestamp":1597276800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["GM081498"],"award-info":[{"award-number":["GM081498"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000002","name":"National Institutes of Health","doi-asserted-by":"publisher","award":["DK067494"],"award-info":[{"award-number":["DK067494"]}],"id":[{"id":"10.13039\/100000002","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>In addition to providing invaluable insights to the host response to viral infection, adenovirus continues to be an important model system for discovering basic aspects of cell biology. This is especially true for products of early region three (E3), which have provided the foundation for understanding many new mechanisms regulating intracellular trafficking of host cell proteins involved in the host immune response. Cholesterol homeostasis is vital for proper cellular physiology, and disturbances in cholesterol balance are increasingly recognized as important factors in human disease. Despite its central role in numerous aspects of cellular functions, the mechanisms responsible for delivery of dietary cholesterol to the endoplasmic reticulum, where the lipid metabolic and regulatory machinery reside, remain poorly understood. In this review, we describe a novel intracellular pathway for cholesterol trafficking that has been co-opted by an adenovirus E3 gene product. We describe what is known about the molecular regulation of this pathway, how it might benefit viral replication, and its potential involvement in normal cell physiology. Finally, we make a case that adenovirus has co-opted a cellular pathway that may be dysregulated in various human diseases.<\/jats:p>","DOI":"10.3390\/ijms21165808","type":"journal-article","created":{"date-parts":[[2020,8,13]],"date-time":"2020-08-13T09:23:44Z","timestamp":1597310624000},"page":"5808","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":6,"title":["Adenovirus Reveals New Pathway for Cholesterol Egress from the Endolysosomal System"],"prefix":"10.3390","volume":"21","author":[{"given":"Cathleen","family":"Carlin","sequence":"first","affiliation":[{"name":"Department of Molecular Biology and Microbiology, Case Comprehensive Cancer Center, School of Medicine, Case Western Reserve University, Cleveland, OH 44106, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Danny","family":"Manor","sequence":"additional","affiliation":[{"name":"Department of Nutrition, Department of Pharmacology, Case Comprehensive Cancer Center, School of Medicine, Case Western Reserve University, Cleveland, OH 44106, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2020,8,13]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"43","DOI":"10.1042\/bse0570043","article-title":"Cholesterol trafficking and distribution","volume":"57","author":"Iaea","year":"2015","journal-title":"Essays Biochem."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1016\/j.ceb.2018.06.002","article-title":"Mechanisms of cellular cholesterol compartmentalization: Recent insights","volume":"53","author":"Ikonen","year":"2018","journal-title":"Curr. Opin. Cell Biol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"281","DOI":"10.1038\/nrm.2017.138","article-title":"Understanding the diversity of membrane lipid composition","volume":"19","author":"Harayama","year":"2018","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"841362","DOI":"10.1155\/2012\/841362","article-title":"Endoplasmic reticulum stress and lipid metabolism: Mechanisms and therapeutic potential","volume":"2012","author":"Basseri","year":"2012","journal-title":"Biochem. Res. Int."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"431","DOI":"10.1161\/ATVBAHA.108.179564","article-title":"The LDL receptor","volume":"29","author":"Goldstein","year":"2009","journal-title":"Arterioscler. Thromb. Vasc. Biol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"759","DOI":"10.1083\/jcb.201401126","article-title":"Bridging the gap: Membrane contact sites in signaling, metabolism, and organelle dynamics","volume":"205","author":"Prinz","year":"2015","journal-title":"J. Cell Biol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"1848","DOI":"10.15252\/embj.201591481","article-title":"ER-endosome contact sites: Molecular compositions and functions","volume":"34","author":"Raiborg","year":"2015","journal-title":"EMBO J."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"2439","DOI":"10.1038\/emboj.2013.170","article-title":"An ER-peroxisome tether exerts peroxisome population control in yeast","volume":"32","author":"Knoblach","year":"2013","journal-title":"EMBO J."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"E458","DOI":"10.1073\/pnas.1215232110","article-title":"Endoplasmic reticulum-associated mitochondria-cortex tether functions in the distribution and inheritance of mitochondria","volume":"110","author":"Lackner","year":"2013","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"450","DOI":"10.1016\/j.devcel.2014.01.012","article-title":"Mitochondrial ER contacts are crucial for mitophagy in yeast","volume":"28","author":"Bockler","year":"2014","journal-title":"Dev. Cell"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1038\/nature11910","article-title":"Autophagosomes form at ER-mitochondria contact sites","volume":"495","author":"Hamasaki","year":"2013","journal-title":"Nature"},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"358","DOI":"10.1126\/science.1207385","article-title":"ER tubules mark sites of mitochondrial division","volume":"334","author":"Friedman","year":"2011","journal-title":"Science"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1030","DOI":"10.1091\/mbc.e12-10-0733","article-title":"Endoplasmic reticulum-endosome contact increases as endosomes traffic and mature","volume":"24","author":"Friedman","year":"2013","journal-title":"Mol. Biol. Cell"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"2364","DOI":"10.1128\/JVI.02249-10","article-title":"Phosphatidylinositol 4-kinase III beta is a target of enviroxime-like compounds for antipoliovirus activity","volume":"85","author":"Arita","year":"2011","journal-title":"J. Virol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"3163","DOI":"10.1105\/tpc.108.060053","article-title":"An inositolphosphorylceramide synthase is involved in regulation of plant programmed cell death associated with defense in Arabidopsis","volume":"20","author":"Wang","year":"2008","journal-title":"Plant Cell"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"e01462-18","DOI":"10.1128\/JVI.01462-18","article-title":"A single point mutation in the rhinovirus 2B protein reduces the requirement for phosphatidylinositol 4-kinase class III beta in viral replication","volume":"92","author":"Roulin","year":"2018","journal-title":"J. Virol."},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Dorobantu, C.M., Albulescu, L., Harak, C., Feng, Q., van Kampen, M., Strating, J.R.P.M., Gorbalenya, A.E., Lohmann, V., van der Schaar, H.M., and van Kuppeveld, F.J.M. (2014). Modulation of the host lipid landscape to promote RNA virus replication: The picornavirus encephalomyocarditis virus converges on the pathway used by hepatitis C virus. PLoS Pathog., 11.","DOI":"10.1371\/journal.ppat.1005185"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"6586","DOI":"10.1128\/JVI.00208-14","article-title":"A complex comprising phosphatidylinositol 4-Kinase III, ACBD3, and Aichi virus proteins enhances phosphatidylinositol 4-phosphate synthesis and is critical for formation of the viral replication complex","volume":"88","author":"Sasaki","year":"2014","journal-title":"J. Virol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"340","DOI":"10.1038\/nature10348","article-title":"Ebola virus entry requires the cholesterol transporter Niemann-Pick C1","volume":"477","author":"Carette","year":"2011","journal-title":"Nature"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"458","DOI":"10.1016\/j.ceb.2011.04.006","article-title":"Lipid transfer and signaling at organelle contact sites: The tip of the iceberg","volume":"23","author":"Toulmay","year":"2011","journal-title":"Curr. Opin. Cell Biol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"504","DOI":"10.1038\/35080071","article-title":"How proteins move lipids and lipids move proteins","volume":"2","author":"Sprong","year":"2001","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_22","first-page":"87","article-title":"Is spontaneous translocation of polar lipids between cellular organelles negligible?","volume":"8","author":"Somerharju","year":"2016","journal-title":"Lipid Insights"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"85","DOI":"10.1038\/s41580-018-0071-5","article-title":"Lipid transfer proteins: The lipid commute via shuttles, bridges and tubes","volume":"20","author":"Wong","year":"2019","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"419","DOI":"10.1042\/BST20150182","article-title":"The role of phosphatidylinositol-transfer proteins at membrane contact sites","volume":"44","author":"Selitrennik","year":"2016","journal-title":"Biochem. Soc. Trans."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1465","DOI":"10.1042\/BST20140143","article-title":"Building lipid PIPelines throughout the cell by ORP\/Osh proteins","volume":"42","author":"Mesmin","year":"2014","journal-title":"Biochem. Soc. Trans."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1083\/jcb.200510084","article-title":"Nonvesicular sterol movement from plasma membrane to ER requires oxysterol-binding protein-related proteins and phosphoinositides","volume":"173","author":"Raychaudhuri","year":"2006","journal-title":"J. Cell Biol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"17797","DOI":"10.1074\/jbc.M800121200","article-title":"Mechanisms of ligand transfer by the hepatic tocopherol transfer protein","volume":"283","author":"Morley","year":"2008","journal-title":"J. Biol. Chem."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"809","DOI":"10.1146\/annurev-biochem-061516-044924","article-title":"The oxysterol-binding protein cycle: Burning off PI (4) P to transport cholesterol","volume":"87","author":"Antonny","year":"2018","journal-title":"Ann. Rev. Biochem."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"516","DOI":"10.1016\/j.tibs.2017.05.001","article-title":"Advances on the transfer of lipids by lipid transfer proteins","volume":"42","author":"Wong","year":"2017","journal-title":"Trends Biochem. Sci."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"329","DOI":"10.1016\/S0022-2275(20)42093-0","article-title":"Disposition of intracellular cholesterol in human fibroblasts","volume":"32","author":"Lange","year":"1991","journal-title":"J. Lipid Res."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"839","DOI":"10.1016\/j.biochi.2004.09.018","article-title":"SREBP transcription factors: Master regulators of lipid homeostasis","volume":"86","author":"Eberle","year":"2004","journal-title":"Biochimie"},{"key":"ref_32","unstructured":"Brown, M.S., and Goldstein, J.S. (1985). A receptor-mediated pathway for cholesterol homeostasis. Nobel Lectures, Physiology or Medicine 1981\u20131990, World Scientific Publishing Co."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"27871","DOI":"10.1074\/jbc.M801463200","article-title":"Lysobisphosphatidic acid controls endosomal cholesterol levels","volume":"283","author":"Chevallier","year":"2008","journal-title":"J. Biol. Chem."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1609","DOI":"10.1194\/jlr.R047837","article-title":"Niemann-Pick C disease and mobilization of lysosomal cholesterol by cyclodextrin","volume":"55","author":"Vance","year":"2014","journal-title":"J. Lipid Res."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1706","DOI":"10.1074\/jbc.TM118.004165","article-title":"NPC intracellular cholesterol transporter 1 (NPC1)-mediated cholesterol export from lysosomes","volume":"294","author":"Pfeffer","year":"2019","journal-title":"J. Biol. Chem."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"23525","DOI":"10.1074\/jbc.M703848200","article-title":"Structural basis of sterol binding by NPC2, a lysosomal protein deficient in Niemann-Pick Type C2 disease","volume":"282","author":"Xu","year":"2007","journal-title":"J. Biol. Chem."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"e50832","DOI":"10.7554\/eLife.50832","article-title":"Intracellular cholesterol trafficking is dependent upon NPC2 interaction with lysobisphosphatidic acid","volume":"8","author":"McCauliff","year":"2019","journal-title":"eLife"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"8212","DOI":"10.1073\/pnas.1607795113","article-title":"Structure of human Niemann Pick C1 protein","volume":"113","author":"Li","year":"2016","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"258","DOI":"10.1016\/j.cell.2015.12.044","article-title":"Ebola viral glycoprotein bound to its endosomal receptor Niemann-Pick C1","volume":"164","author":"Wang","year":"2016","journal-title":"Cell"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1213","DOI":"10.1016\/j.cell.2009.03.049","article-title":"Structure of N-terminal domain of NPC1 reveals distinct subdomains for binding and transfer of cholesterol","volume":"137","author":"Kwon","year":"2009","journal-title":"Cell"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"15287","DOI":"10.1073\/pnas.0807328105","article-title":"NPC2 facilitates bidirectional transfer of cholesterol between NPC1 and lipid bilayers, a step in cholesterol egress from lysosomes","volume":"105","author":"Infante","year":"2008","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"1023","DOI":"10.1194\/jlr.M002345","article-title":"MLN64 mediates egress of cholesterol from endosomes to mitochondria in the absence of functional Niemann-Pick Type C1 protein","volume":"51","author":"Charman","year":"2010","journal-title":"J. Lipid Res."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"14876","DOI":"10.1073\/pnas.1520490112","article-title":"Glycosylation inhibition reduces cholesterol accumulation in NPC1 protein-deficient cells","volume":"112","author":"Li","year":"2015","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1083\/jcb.201004142","article-title":"A role for oxysterol-binding protein-related protein 5 in endosomal cholesterol trafficking","volume":"192","author":"Du","year":"2011","journal-title":"J. Cell Biol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"4276","DOI":"10.1038\/s41467-019-12152-2","article-title":"NPC1 regulates ER contacts with endocytic organelles to mediate cholesterol egress","volume":"10","author":"Hoglinger","year":"2019","journal-title":"Nat. Commun."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"428","DOI":"10.1126\/science.aab1370","article-title":"PI4P\/phosphatidylserine countertransport at ORP5- and ORP8-mediated ER-plasma membrane contacts","volume":"349","author":"Chung","year":"2015","journal-title":"Science"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"2093","DOI":"10.1073\/pnas.0812934106","article-title":"Unraveling the sterol-trafficking defect in Niemann-Pick C disease","volume":"106","author":"Sturley","year":"2009","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"129","DOI":"10.1146\/annurev.cellbio.22.010305.104656","article-title":"Cholesterol sensing, trafficking, and esterification","volume":"22","author":"Chang","year":"2006","journal-title":"Annu. Rev. Cell Dev. Biol."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"e01904","DOI":"10.1128\/JVI.01904-16","article-title":"Adenovirus modulates Toll-like receptor 4 signaling by reprogramming ORP1L-VAP protein contacts for cholesterol transport from endosomes to the endoplasmic reticulum","volume":"91","author":"Cianciola","year":"2017","journal-title":"J. Virol."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"3309","DOI":"10.1091\/mbc.e12-10-0760","article-title":"Adenovirus RIDa uncovers a novel pathway requiring ORP1L for lipid droplet formation independent of NPC1","volume":"24","author":"Cianciola","year":"2013","journal-title":"Mol. Biol. Cell"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"13838","DOI":"10.1016\/S0021-9258(19)85179-7","article-title":"Role of the plasma membrane in cholesterol esterification in rat hepatoma cells","volume":"268","author":"Lange","year":"1993","journal-title":"J. Biol. Chem."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"281","DOI":"10.1016\/j.chom.2013.08.002","article-title":"Enteroviruses harness the cellular endocytic machinery to remodel the host cell cholesterol landscape for effective viral replication","volume":"14","author":"Ilnytska","year":"2013","journal-title":"Cell Host Microbe"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"724","DOI":"10.1016\/j.bbalip.2008.08.006","article-title":"Different kinetics of cholesterol delivery to components of the cholesterol homeostatic machinery: Implications for cholesterol trafficking to the endoplasmic reticulum","volume":"1781","author":"Kristiana","year":"2008","journal-title":"Biochim. Biophys. Acta Mol. Cell Biol. Lipids"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"46414","DOI":"10.1074\/jbc.M108099200","article-title":"Cholesterol overload promotes morphogenesis of a Niemann-Pick C (NPC)-like compartment independent of inhibition of NPC1 or HE1\/NPC2 function","volume":"276","author":"Frolov","year":"2001","journal-title":"J. Biol. Chem."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"128","DOI":"10.1161\/01.ATV.0000148323.94021.e5","article-title":"ACAT1 deficiency disrupts cholesterol efflux and alters cellular morphology in macrophages","volume":"25","author":"Dove","year":"2005","journal-title":"Arterioscler. Thromb. Vasc. Biol."},{"key":"ref_56","doi-asserted-by":"crossref","unstructured":"Sobo, K., Le Blanc, I., Luyet, P.-P., Fivaz, M., Ferguson, C., Parton, R.G., Gruenberg, J., and van der Goot, F.G. (2007). Late endosomal cholesterol accumulation leads to impaired intra-endosomal trafficking. PLoS ONE, 2.","DOI":"10.1371\/journal.pone.0000851"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"e26","DOI":"10.1017\/S146239940800080X","article-title":"The pathogenesis of Niemann-Pick type C disease: A role for autophagy?","volume":"10","author":"Pacheco","year":"2008","journal-title":"Expert Rev. Mol. Med."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"17890","DOI":"10.1074\/jbc.M601679200","article-title":"Cholesterol accumulation sequesters Rab9 and disrupts late endosome function in NPC1-deficient cells","volume":"281","author":"Ganley","year":"2006","journal-title":"J. Biol. Chem."},{"key":"ref_59","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":"Sem. Cell Dev. Biol."},{"key":"ref_60","doi-asserted-by":"crossref","unstructured":"Guerra, F., and Bucci, C. (2016). Multiple Roles of the Small GTPase Rab7. Cells, 5.","DOI":"10.3390\/cells5030034"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"1209","DOI":"10.1083\/jcb.200811005","article-title":"Cholesterol sensor ORP1L contacts the ER protein VAP to control Rab7-RILP-p150Glued and late endosome positioning","volume":"185","author":"Rocha","year":"2009","journal-title":"J. Cell Biol."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"459","DOI":"10.1083\/jcb.200606077","article-title":"Activation of endosomal dynein motors by stepwise assembly of Rab7-RILP-p150Glued, ORP1L, and the receptor {beta}lll spectrin","volume":"12","author":"Johansson","year":"2007","journal-title":"J. Cell Biol."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"1289","DOI":"10.1093\/emboj\/21.6.1289","article-title":"Late endosome motility depends on lipids via the small GTPase Rab7","volume":"21","author":"Lebrand","year":"2002","journal-title":"EMBO J."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1016\/j.coph.2006.11.014","article-title":"Adenovirus infections and lung disease","volume":"7","author":"Hayashi","year":"2007","journal-title":"Curr. Opin. Pharm."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"S152","DOI":"10.1002\/jgm.553","article-title":"Adenovirus endocytosis","volume":"6","author":"Meier","year":"2004","journal-title":"J. Gene Med."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1016\/j.chom.2015.06.006","article-title":"Co-option of membrane wounding enables virus penetration into cells","volume":"18","author":"Luisoni","year":"2016","journal-title":"Cell Host Microbe"},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1016\/j.chom.2011.07.006","article-title":"Drifting motions of the adenovirus receptor CAR and immobile integrins initiate virus uncoating and membrane lytic protein exposure","volume":"10","author":"Burckhardt","year":"2011","journal-title":"Cell Host Microbe"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"734","DOI":"10.1016\/j.tcb.2014.07.008","article-title":"Damage control: Cellular mechanisms of plasma membrane repair","volume":"24","author":"Andrews","year":"2014","journal-title":"Trends Cell Biol."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"265","DOI":"10.1089\/hum.2014.001","article-title":"Innate immunity to adenovirus","volume":"25","author":"Hendrickx","year":"2014","journal-title":"Hum. Gene Ther."},{"key":"ref_70","doi-asserted-by":"crossref","unstructured":"Carlin, C.R. (2019). New insights to adenovirus-directed innate immunity in respiratory epithelial cells. Microorganisms, 7.","DOI":"10.3390\/microorganisms7080216"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"1310","DOI":"10.1093\/emboj\/20.6.1310","article-title":"Adenovirus-activated PKA and p38\/MAPK pathways boost microtubule-mediated nuclear targeting of virus","volume":"20","author":"Suomalainen","year":"2001","journal-title":"EMBO J."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"163","DOI":"10.1083\/jcb.201307116","article-title":"PKA-dependent dynein switching from lysosomes to adenovirus: A novel form of host-virus competition","volume":"205","author":"Scherer","year":"2014","journal-title":"J. Cell Biol."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1513\/pats.200909-101JS","article-title":"Autophagy in the lung","volume":"7","author":"Ryter","year":"2010","journal-title":"Proc. Am. Thorac. Soc."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"2307","DOI":"10.1128\/JVI.02014-12","article-title":"Host cell autophagy modulates early stages of adenovirus infections in airway epithelial cells","volume":"87","author":"Zeng","year":"2013","journal-title":"J. Virol."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"1472","DOI":"10.1038\/s41564-018-0293-5","article-title":"An ATG16L1-dependent pathway promotes plasma membrane repair and limits Listeria monocytogenes cell-to-cell spread","volume":"3","author":"Tan","year":"2018","journal-title":"Nat. Microbiol."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"3089","DOI":"10.1128\/JVI.78.6.3089-3098.2004","article-title":"Cholesterol is required for endocytosis and endosomal escape of adenovirus type 2","volume":"78","author":"Imelli","year":"2004","journal-title":"J. Virol."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"137","DOI":"10.1038\/s41580-018-0085-z","article-title":"Dynamics and functions of lipid droplets","volume":"20","author":"Olzmann","year":"2019","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"96","DOI":"10.1016\/j.micinf.2006.10.015","article-title":"Lipid rafts play an important role in the early stage of severe acute respiratory syndrome-coronavirus life cycle","volume":"9","author":"Li","year":"2007","journal-title":"Microbes Infect."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"344","DOI":"10.1016\/j.bbrc.2008.02.023","article-title":"Lipid rafts are involved in SARS-CoV entry into Vero E6 cells","volume":"369","author":"Lu","year":"2008","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"10654","DOI":"10.1021\/acs.jpcb.9b08455","article-title":"Membrane cholesterol modulates oligomeric status and peptide-membrane interaction of severe acute respiratory syndrome coronavirus fusion peptide","volume":"123","author":"Meher","year":"2019","journal-title":"J. Phys. Chem. B"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"485","DOI":"10.5114\/aoms.2020.94503","article-title":"Lipid-lowering therapy and renin-angiotensin-aldosterone system inhibitors in the era of the COVID-19 pandemic","volume":"16","author":"Katsiki","year":"2020","journal-title":"Arch. Med. Sci."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"1061","DOI":"10.1001\/jama.2020.1585","article-title":"Clinical Characteristics of 138 Hospitalized Patients With 2019 Novel Coronavirus-Infected Pneumonia in Wuhan, China","volume":"323","author":"Wang","year":"2020","journal-title":"JAMA"},{"key":"ref_83","first-page":"3695","article-title":"Adenovirus E3 protein causes constitutively internalized EGF receptors to accumulate in a prelysosomal compartment, resulting in enhanced degradation","volume":"14","author":"Hoffman","year":"1994","journal-title":"Mol. Cell Biol."},{"key":"ref_84","doi-asserted-by":"crossref","unstructured":"Zeng, X., and Carlin, C.R. (2019). Adenovirus early region 3 RIDa protein limits NFkB signaling through stress-activated EGF receptors. PLoS Pathog., 15.","DOI":"10.1371\/journal.ppat.1008017"},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"965","DOI":"10.1083\/jcb.200702187","article-title":"Adenovirus RIDa regulates endosome maturation by mimicking GTP-Rab7","volume":"179","author":"Shah","year":"2007","journal-title":"J. Cell Biol."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"537","DOI":"10.1083\/jcb.200903039","article-title":"Adenovirus RID-a activates an autonomous cholesterol regulatory mechanism that rescues defects linked to Niemann-Pick disease type C","volume":"187","author":"Cianciola","year":"2009","journal-title":"J. Cell Biol."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"154","DOI":"10.1038\/nature03923","article-title":"Structural mechanism for sterol sensing and transport by OSBP-related proteins","volume":"437","author":"Im","year":"2005","journal-title":"Nature"},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1042\/bj2480237","article-title":"Movement of plasma-membrane sterols to the endoplasmic reticulum in cultured cells","volume":"248","author":"Slotte","year":"1987","journal-title":"Biochem. J."},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"8299","DOI":"10.1128\/jvi.71.11.8299-8306.1997","article-title":"The adenovirus E3-10.4K\/14.5K complex mediates loss of cell surface Fas (CD95) and resistance to Fas-induced apoptosis","volume":"71","author":"Shisler","year":"1997","journal-title":"J. Virol."},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"726","DOI":"10.1038\/33712","article-title":"Forced degradation of Fas inhibits apoptosis in adenovirus-infected cells","volume":"392","author":"Tollefson","year":"1997","journal-title":"Nature"},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"1879","DOI":"10.1523\/JNEUROSCI.5282-06.2007","article-title":"Endosomal accumulation of Toll-like receptor 4 causes constitutive secretion of cytokines and activation of signal transducers and activators of transcription in Niemann-Pick disease type C (NPC) fibroblasts: A potential basis for glial cell activation in the NPC brain","volume":"27","author":"Suzuki","year":"2007","journal-title":"J. Neurosci."},{"key":"ref_92","doi-asserted-by":"crossref","first-page":"118","DOI":"10.4161\/auto.5260","article-title":"Adenovirus\u2019s last trick","volume":"4","author":"Jiang","year":"2008","journal-title":"Autophagy"},{"key":"ref_93","doi-asserted-by":"crossref","first-page":"136","DOI":"10.1016\/j.yexcr.2015.03.028","article-title":"Phosphatidylinositol 4-kinases: Function, structure, and inhibition","volume":"337","author":"Boura","year":"2015","journal-title":"Exp. Cell Res."},{"key":"ref_94","doi-asserted-by":"crossref","first-page":"799","DOI":"10.1016\/j.cell.2010.03.050","article-title":"Viral reorganization of the secretory pathway generates distinct organelles for RNA replication","volume":"141","author":"Hsu","year":"2010","journal-title":"Cell"},{"key":"ref_95","doi-asserted-by":"crossref","unstructured":"Kobuna, H., Inoue, T., Shibata, M., Gengyo-Ando, K., Yamamoto, A., Mitani, S., and Arai, H. (2010). Multivesicular body formation requires OSBP-related proteins and cholesterol. PLoS Genet., 6.","DOI":"10.1371\/journal.pgen.1001055"},{"key":"ref_96","doi-asserted-by":"crossref","first-page":"473","DOI":"10.1016\/j.devcel.2016.05.005","article-title":"Annexin A1 tethers membrane contact sites that mediate ER to endosome cholesterol transport","volume":"37","author":"Eden","year":"2016","journal-title":"Dev. Cell"},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"514","DOI":"10.1016\/j.tcb.2006.08.003","article-title":"Intra-endosomal membrane traffic","volume":"16","author":"Gruenberg","year":"2006","journal-title":"Trends Cell Biol."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"1807","DOI":"10.1016\/j.celrep.2017.05.028","article-title":"Oxysterol-binding protein-related protein 1L regulates cholesterol egress from the endo-lysosomal system","volume":"19","author":"Zhao","year":"2017","journal-title":"Cell Rep."},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"829","DOI":"10.1038\/s41467-019-08791-0","article-title":"Allosteric enhancement of ORP1-mediated cholesterol transport by PI(4,5)P2\/PI(3,4)P2","volume":"10","author":"Dong","year":"2019","journal-title":"Nat. Commun."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"7673","DOI":"10.1038\/sj.onc.1209040","article-title":"Recent lessons in gene expression, cell cycle control, and cell biology from adenovirus","volume":"24","author":"Berk","year":"2005","journal-title":"Oncogene"},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"1163","DOI":"10.1016\/j.it.2019.10.002","article-title":"Foam cells: One size doesn\u2019t fit all","volume":"40","author":"Guerrini","year":"2019","journal-title":"Trends Immunol."},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"dmm034272","DOI":"10.1242\/dmm.034272","article-title":"Immunometabolism in cancer at a glance","volume":"11","author":"Singer","year":"2018","journal-title":"Dis. Models Mech."},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1016\/j.cca.2013.06.006","article-title":"Foam cells in atherosclerosis","volume":"424","author":"Yu","year":"2013","journal-title":"Clin. Chim. Acta"},{"key":"ref_104","doi-asserted-by":"crossref","first-page":"740","DOI":"10.5551\/jat.4416","article-title":"Association of ACAT1-positive vesicles with late endosomes\/lysosomes in cholesterol-rich human macrophages","volume":"17","author":"Lei","year":"2010","journal-title":"J. Atheroscler. Thromb."},{"key":"ref_105","doi-asserted-by":"crossref","first-page":"1263","DOI":"10.1194\/jlr.M900288-JLR200","article-title":"Cholesterol loading in macrophages stimulates formation of ER-derived vesicles with elevated ACAT1 activity","volume":"51","author":"Sakashita","year":"2010","journal-title":"J. Lipid Res."},{"key":"ref_106","doi-asserted-by":"crossref","first-page":"e12177","DOI":"10.7554\/eLife.12177","article-title":"Identification of NPC1 as the target of U18666A, an inhibitor of lysosomal cholesterol export and Ebola infection","volume":"4","author":"Lu","year":"2015","journal-title":"eLife"},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"5480","DOI":"10.1091\/mbc.e05-03-0189","article-title":"The oxysterol-binding protein homologue ORP1L interacts with Rab7 and alters functional properties of late endocytic compartments","volume":"16","author":"Johansson","year":"2005","journal-title":"Mol. Biol. Cell"},{"key":"ref_108","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1038\/s41419-020-2297-3","article-title":"Lipid droplets: Platforms with multiple functions in cancer hallmarks","volume":"11","author":"Cruz","year":"2020","journal-title":"Cell Death Dis."},{"key":"ref_109","doi-asserted-by":"crossref","first-page":"268","DOI":"10.1016\/j.tem.2010.01.001","article-title":"The Akt-SREBP nexus: Cell signaling meets lipid metabolism","volume":"21","author":"Krycer","year":"2010","journal-title":"Trends Endocrin. Metab."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/21\/16\/5808\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T10:00:00Z","timestamp":1760176800000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/21\/16\/5808"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,8,13]]},"references-count":109,"journal-issue":{"issue":"16","published-online":{"date-parts":[[2020,8]]}},"alternative-id":["ijms21165808"],"URL":"https:\/\/doi.org\/10.3390\/ijms21165808","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,8,13]]}}}