2023
Sequence-independent activity of a predicted long disordered segment of the human papillomavirus type 16 L2 capsid protein during virus entry
Oh C, Buckley P, Choi J, Hierro A, DiMaio D. Sequence-independent activity of a predicted long disordered segment of the human papillomavirus type 16 L2 capsid protein during virus entry. Proceedings Of The National Academy Of Sciences Of The United States Of America 2023, 120: e2307721120. PMID: 37819982, PMCID: PMC10589650, DOI: 10.1073/pnas.2307721120.Peer-Reviewed Original ResearchConceptsAmino acid sequenceAcid sequenceProtein segmentsVirus traffickingUnrelated cellular proteinsSequence-independent mannerIntracellular virus traffickingActivity of proteinsAmino acid segmentComplex biological functionsVirus entryTandem arraysProtein functionTrafficking factorsCellular proteinsEndosome membraneBiological functionsHPV16 pseudovirus infectionCellular factorsDiverse sequencesL2 capsid proteinsNoncanonical Rab9a action supports retromer-mediated endosomal exit of human papillomavirus during virus entry
Choi J, DiMaio D. Noncanonical Rab9a action supports retromer-mediated endosomal exit of human papillomavirus during virus entry. PLOS Pathogens 2023, 19: e1011648. PMID: 37703297, PMCID: PMC10519607, DOI: 10.1371/journal.ppat.1011648.Peer-Reviewed Original ResearchConceptsRetromer-mediated endosomeHPV entryGTP-bound formDominant negative Rab7Intracellular vesicular transportRetrograde transport pathwayVirus entryEndosomal exitRab GTPasesRab proteinsVesicle traffickingGolgi transportCellular proteinsVesicular transportProtein cargoKnockdown cellsIntracellular traffickingRab9AIncoming virusRab7EndosomesTraffickingTransport pathwaysProteinKey roleVirology under the Microscope—a Call for Rational Discourse
Goodrum F, Lowen A, Lakdawala S, Alwine J, Casadevall A, Imperiale M, Atwood W, Avgousti D, Baines J, Banfield B, Banks L, Bhaduri-McIntosh S, Bhattacharya D, Blanco-Melo D, Bloom D, Boon A, Boulant S, Brandt C, Broadbent A, Brooke C, Cameron C, Campos S, Caposio P, Chan G, Cliffe A, Coffin J, Collins K, Damania B, Daugherty M, Debbink K, DeCaprio J, Dermody T, Dikeakos J, DiMaio D, Dinglasan R, Duprex W, Dutch R, Elde N, Emerman M, Enquist L, Fane B, Fernandez-Sesma A, Flenniken M, Frappier L, Frieman M, Frueh K, Gack M, Gaglia M, Gallagher T, Galloway D, García-Sastre A, Geballe A, Glaunsinger B, Goff S, Greninger A, Hancock M, Harris E, Heaton N, Heise M, Heldwein E, Hogue B, Horner S, Hutchinson E, Hyser J, Jackson W, Kalejta R, Kamil J, Karst S, Kirchhoff F, Knipe D, Kowalik T, Lagunoff M, Laimins L, Langlois R, Lauring A, Lee B, Leib D, Liu S, Longnecker R, Lopez C, Luftig M, Lund J, Manicassamy B, McFadden G, McIntosh M, Mehle A, Miller W, Mohr I, Moody C, Moorman N, Moscona A, Mounce B, Munger J, Münger K, Murphy E, Naghavi M, Nelson J, Neufeldt C, Nikolich J, O'Connor C, Ono A, Orenstein W, Ornelles D, Ou J, Parker J, Parrish C, Pekosz A, Pellett P, Pfeiffer J, Plemper R, Polyak S, Purdy J, Pyeon D, Quinones-Mateu M, Renne R, Rice C, Schoggins J, Roller R, Russell C, Sandri-Goldin R, Sapp M, Schang L, Schmid S, Schultz-Cherry S, Semler B, Shenk T, Silvestri G, Simon V, Smith G, Smith J, Spindler K, Stanifer M, Subbarao K, Sundquist W, Suthar M, Sutton T, Tai A, Tarakanova V, tenOever B, Tibbetts S, Tompkins S, Toth Z, van Doorslaer K, Vignuzzi M, Wallace N, Walsh D, Weekes M, Weinberg J, Weitzman M, Weller S, Whelan S, White E, Williams B, Wobus C, Wong S, Yurochko A. Virology under the Microscope—a Call for Rational Discourse. Journal Of Virology 2023, 97: e00089-23. PMID: 36700640, PMCID: PMC9972907, DOI: 10.1128/jvi.00089-23.Peer-Reviewed Original ResearchConceptsOrigin of SARS-CoV-2Evidence-based discourseRational discourseVirology researchGain-of-function approachesVirus-related researchPolicy makersField of virologyLegitimate questionsHuman pathogensDiscourseVocal groupRegulatory structureSARS-CoV-2United StatesPublic concernPublic confusionGroup of individualsVirology under the Microscope—a Call for Rational Discourse
Goodrum F, Lowen A, Lakdawala S, Alwine J, Casadevall A, Imperiale M, Atwood W, Avgousti D, Baines J, Banfield B, Banks L, Bhaduri-McIntosh S, Bhattacharya D, Blanco-Melo D, Bloom D, Boon A, Boulant S, Brandt C, Broadbent A, Brooke C, Cameron C, Campos S, Caposio P, Chan G, Cliffe A, Coffin J, Collins K, Damania B, Daugherty M, Debbink K, DeCaprio J, Dermody T, Dikeakos J, DiMaio D, Dinglasan R, Duprex W, Dutch R, Elde N, Emerman M, Enquist L, Fane B, Fernandez-Sesma A, Flenniken M, Frappier L, Frieman M, Frueh K, Gack M, Gaglia M, Gallagher T, Galloway D, García-Sastre A, Geballe A, Glaunsinger B, Goff S, Greninger A, Hancock M, Harris E, Heaton N, Heise M, Heldwein E, Hogue B, Horner S, Hutchinson E, Hyser J, Jackson W, Kalejta R, Kamil J, Karst S, Kirchhoff F, Knipe D, Kowalik T, Lagunoff M, Laimins L, Langlois R, Lauring A, Lee B, Leib D, Liu S, Longnecker R, Lopez C, Luftig M, Lund J, Manicassamy B, McFadden G, McIntosh M, Mehle A, Miller W, Mohr I, Moody C, Moorman N, Moscona A, Mounce B, Munger J, Münger K, Murphy E, Naghavi M, Nelson J, Neufeldt C, Nikolich J, O'Connor C, Ono A, Orenstein W, Ornelles D, Ou J, Parker J, Parrish C, Pekosz A, Pellett P, Pfeiffer J, Plemper R, Polyak S, Purdy J, Pyeon D, Quinones-Mateu M, Renne R, Rice C, Schoggins J, Roller R, Russell C, Sandri-Goldin R, Sapp M, Schang L, Schmid S, Schultz-Cherry S, Semler B, Shenk T, Silvestri G, Simon V, Smith G, Smith J, Spindler K, Stanifer M, Subbarao K, Sundquist W, Suthar M, Sutton T, Tai A, Tarakanova V, tenOever B, Tibbetts S, Tompkins S, Toth Z, van Doorslaer K, Vignuzzi M, Wallace N, Walsh D, Weekes M, Weinberg J, Weitzman M, Weller S, Whelan S, White E, Williams B, Wobus C, Wong S, Yurochko A. Virology under the Microscope—a Call for Rational Discourse. MBio 2023, 14: e00188-23. PMID: 36700642, PMCID: PMC9973315, DOI: 10.1128/mbio.00188-23.Peer-Reviewed Original ResearchConceptsOrigin of SARS-CoV-2Evidence-based discourseRational discourseVirology researchGain-of-function approachesVirus-related researchPolicy makersField of virologyLegitimate questionsHuman pathogensDiscourseVocal groupRegulatory structureSARS-CoV-2United StatesPublic concernPublic confusionGroup of individualsVirology under the Microscope—a Call for Rational Discourse
Goodrum F, Lowen A, Lakdawala S, Alwine J, Casadevall A, Imperiale M, Atwood W, Avgousti D, Baines J, Banfield B, Banks L, Bhaduri-McIntosh S, Bhattacharya D, Blanco-Melo D, Bloom D, Boon A, Boulant S, Brandt C, Broadbent A, Brooke C, Cameron C, Campos S, Caposio P, Chan G, Cliffe A, Coffin J, Collins K, Damania B, Daugherty M, Debbink K, DeCaprio J, Dermody T, Dikeakos J, DiMaio D, Dinglasan R, Duprex W, Dutch R, Elde N, Emerman M, Enquist L, Fane B, Fernandez-Sesma A, Flenniken M, Frappier L, Frieman M, Frueh K, Gack M, Gaglia M, Gallagher T, Galloway D, García-Sastre A, Geballe A, Glaunsinger B, Goff S, Greninger A, Hancock M, Harris E, Heaton N, Heise M, Heldwein E, Hogue B, Horner S, Hutchinson E, Hyser J, Jackson W, Kalejta R, Kamil J, Karst S, Kirchhoff F, Knipe D, Kowalik T, Lagunoff M, Laimins L, Langlois R, Lauring A, Lee B, Leib D, Liu S, Longnecker R, Lopez C, Luftig M, Lund J, Manicassamy B, McFadden G, McIntosh M, Mehle A, Miller W, Mohr I, Moody C, Moorman N, Moscona A, Mounce B, Munger J, Münger K, Murphy E, Naghavi M, Nelson J, Neufeldt C, Nikolich J, O'Connor C, Ono A, Orenstein W, Ornelles D, Ou J, Parker J, Parrish C, Pekosz A, Pellett P, Pfeiffer J, Plemper R, Polyak S, Purdy J, Pyeon D, Quinones-Mateu M, Renne R, Rice C, Schoggins J, Roller R, Russell C, Sandri-Goldin R, Sapp M, Schang L, Schmid S, Schultz-Cherry S, Semler B, Shenk T, Silvestri G, Simon V, Smith G, Smith J, Spindler K, Stanifer M, Subbarao K, Sundquist W, Suthar M, Sutton T, Tai A, Tarakanova V, tenOever B, Tibbetts S, Tompkins S, Toth Z, van Doorslaer K, Vignuzzi M, Wallace N, Walsh D, Weekes M, Weinberg J, Weitzman M, Weller S, Whelan S, White E, Williams B, Wobus C, Wong S, Yurochko A. Virology under the Microscope—a Call for Rational Discourse. MSphere 2023, 8: e00034-23. PMID: 36700653, PMCID: PMC10117089, DOI: 10.1128/msphere.00034-23.Peer-Reviewed Original ResearchConceptsOrigin of SARS-CoV-2Evidence-based discourseRational discourseVirology researchGain-of-function approachesVirus-related researchPolicy makersField of virologyLegitimate questionsHuman pathogensDiscourseVocal groupRegulatory structureSARS-CoV-2United StatesPublic concernPublic confusionGroup of individualsHPV is a cargo for the COPI sorting complex during virus entry
Harwood M, Woo T, Takeo Y, DiMaio D, Tsai B. HPV is a cargo for the COPI sorting complex during virus entry. Science Advances 2023, 9: eadc9830. PMID: 36662862, PMCID: PMC9858521, DOI: 10.1126/sciadv.adc9830.Peer-Reviewed Original ResearchConceptsCoat protein complex ITrans-Golgi networkProtein complex IGene knockdown strategyVirus entryCOPI complexProtein complexesCellular fractionationUnbiased proteomicsRetrograde traffickingCytoplasmic segmentGolgi stacksCellular cargoL2 mutantKnockdown strategyGolgi apparatusComplex IIncoming virusCell surfaceGolgiHost factorsCargoComplexesMutantsEndosomes
2022
Human Papillomavirus L2 Capsid Protein Stabilizes γ-Secretase during Viral Infection
Crite M, DiMaio D. Human Papillomavirus L2 Capsid Protein Stabilizes γ-Secretase during Viral Infection. Viruses 2022, 14: 804. PMID: 35458534, PMCID: PMC9027364, DOI: 10.3390/v14040804.Peer-Reviewed Original ResearchConceptsTM domainΓ-secretaseVirus traffickingCellular transmembrane proteinsNon-canonical rolePutative TM domainRetrograde transport pathwayΓ-secretase complexSubstrate proteinsMinor capsid protein L2Transmembrane proteinCatalytic subunitMutational studiesEndosomal membranesIntracellular traffickingProtein L2Cellular proteasesCellular factorsL2 capsid proteinsTM mutantsCapsid proteinHPV entryTraffickingL2 proteinProtein
2020
Introduction
Enquist L, Dermody T, DiMaio D. Introduction. Annual Review Of Virology 2020, 7: 1-2. PMID: 32991270, DOI: 10.1146/annurev-vi-07-070920-100011.Peer-Reviewed Original ResearchTBC1D5-Catalyzed Cycling of Rab7 Is Required for Retromer-Mediated Human Papillomavirus Trafficking during Virus Entry
Xie J, Heim EN, Crite M, DiMaio D. TBC1D5-Catalyzed Cycling of Rab7 Is Required for Retromer-Mediated Human Papillomavirus Trafficking during Virus Entry. Cell Reports 2020, 31: 107750. PMID: 32521275, PMCID: PMC7339955, DOI: 10.1016/j.celrep.2020.107750.Peer-Reviewed Original ResearchConceptsGTPase-activating proteinsRetrograde transport pathwayVirus entryRetromer activityHPV traffickingTrafficking complexMembrane recruitmentRetromer complexRab7-GTPCellular proteinsCellular compartmentsEndosome membraneRetromerRetrograde pathwayArtificial proteinsL2 capsid proteinsCapsid proteinRab7HPV entryTraffickingTBC1D5ProteinGTPTransport pathwaysPathwayIntroduction: A New Coronavirus Emerges, This Time Causing a Pandemic
DiMaio D, Enquist L, Dermody T. Introduction: A New Coronavirus Emerges, This Time Causing a Pandemic. Annual Review Of Virology 2020, 7: 1-4. PMID: 32315256, DOI: 10.1146/annurev-vi-07-042020-100001.Peer-Reviewed Original ResearchBetacoronavirusClinical Laboratory TechniquesCommunicable Disease ControlContact TracingCoronavirus InfectionsCOVID-19COVID-19 TestingHumansInfectious Disease Incubation PeriodInformation DisseminationInternational CooperationMiddle East Respiratory Syndrome CoronavirusPandemicsPneumonia, ViralPsychological DistanceQuarantineSARS-CoV-2Severe Acute Respiratory SyndromeSevere acute respiratory syndrome-related coronavirusSeverity of Illness IndexCell-penetrating peptide inhibits retromer-mediated human papillomavirus trafficking during virus entry
Zhang P, Moreno R, Lambert PF, DiMaio D. Cell-penetrating peptide inhibits retromer-mediated human papillomavirus trafficking during virus entry. Proceedings Of The National Academy Of Sciences Of The United States Of America 2020, 117: 6121-6128. PMID: 32123072, PMCID: PMC7084110, DOI: 10.1073/pnas.1917748117.Peer-Reviewed Original ResearchConceptsEssential protein-protein interactionsCellular protein complexesProtein-protein interactionsIntracellular virus traffickingRetrograde transport pathwaySites of replicationCell-penetrating sequenceProtein complexesCellular proteinsVirus replicationHPV16 pseudovirus infectionVirus traffickingL2 capsid proteinsAspects of infectionCapsid proteinHPV entryViral genomeViral proteinsIncoming virionsViral componentsHuman papillomavirus infectionProteinAntiviral targetDose-dependent blockVirus entry
2019
Introduction
Enquist L, Dermody T, DiMaio D. Introduction. Annual Review Of Virology 2019, 6: 1-2. PMID: 31567061, DOI: 10.1146/annurev-vi-06-072619-100001.Peer-Reviewed Original Research
2018
Cell-Penetrating Peptide Mediates Intracellular Membrane Passage of Human Papillomavirus L2 Protein to Trigger Retrograde Trafficking
Zhang P, da Silva G, Deatherage C, Burd C, DiMaio D. Cell-Penetrating Peptide Mediates Intracellular Membrane Passage of Human Papillomavirus L2 Protein to Trigger Retrograde Trafficking. Cell 2018, 174: 1465-1476.e13. PMID: 30122350, PMCID: PMC6128760, DOI: 10.1016/j.cell.2018.07.031.Peer-Reviewed Original ResearchMeSH KeywordsAmino Acid SequenceCapsid ProteinsCell-Penetrating PeptidesEndosomesGolgi ApparatusGreen Fluorescent ProteinsHEK293 CellsHeLa CellsHuman papillomavirus 16HumansMutagenesisOncogene Proteins, ViralProtein TransportRecombinant Fusion ProteinsSequence AlignmentVirus AttachmentVirus InternalizationConceptsCell-penetrating peptidesTrans-Golgi networkNormal cell physiologyL2 proteinRetrograde transport pathwayShort protein segmentsHPV L2 proteinTrafficking factorsRetrograde traffickingCationic cell-penetrating peptidesCell physiologyEndosomal membranesProtein segmentsC-terminusBiological roleNon-enveloped virusesRetrograde pathwayL2 capsid proteinsMembrane passageCell penetrating peptideCapsid proteinViral proteinsProteinRetromerTransport pathwaysγ-Secretase promotes membrane insertion of the human papillomavirus L2 capsid protein during virus infection
Inoue T, Zhang P, Zhang W, Goodner-Bingham K, Dupzyk A, DiMaio D, Tsai B. γ-Secretase promotes membrane insertion of the human papillomavirus L2 capsid protein during virus infection. Journal Of Cell Biology 2018, 217: 3545-3559. PMID: 30006461, PMCID: PMC6168257, DOI: 10.1083/jcb.201804171.Peer-Reviewed Original Research
2017
Single methyl groups can act as toggle switches to specify transmembrane Protein-protein interactions
He L, Steinocher H, Shelar A, Cohen EB, Heim EN, Kragelund BB, Grigoryan G, DiMaio D. Single methyl groups can act as toggle switches to specify transmembrane Protein-protein interactions. ELife 2017, 6: e27701. PMID: 28869036, PMCID: PMC5597333, DOI: 10.7554/elife.27701.Peer-Reviewed Original ResearchConceptsProtein-protein interactionsErythropoietin receptorTransmembrane proteinTransmembrane protein-protein interactionsTMD interactionsModel transmembrane proteinMouse erythropoietin receptorHuman erythropoietin receptorSingle methyl groupGrowth factor independenceSide chain methyl groupsCellular processesMouse cellsFactor independenceChain methyl groupsIntrinsic specificityToggle switchTraptamersMethyl groupProteinReceptor activitySpecific positionsReceptorsSpecificityOligomerizationTwo transmembrane dimers of the bovine papillomavirus E5 oncoprotein clamp the PDGF β receptor in an active dimeric conformation
Karabadzhak AG, Petti LM, Barrera FN, Edwards APB, Moya-Rodríguez A, Polikanov YS, Freites JA, Tobias DJ, Engelman DM, DiMaio D. Two transmembrane dimers of the bovine papillomavirus E5 oncoprotein clamp the PDGF β receptor in an active dimeric conformation. Proceedings Of The National Academy Of Sciences Of The United States Of America 2017, 114: e7262-e7271. PMID: 28808001, PMCID: PMC5584431, DOI: 10.1073/pnas.1705622114.Peer-Reviewed Original ResearchConceptsTransmembrane domainE5 proteinE5 dimerPlatelet-derived growth factor β receptorGrowth factor β receptorActive dimeric conformationPDGF β-receptorTransmembrane dimerProtein bindsMembrane environmentReceptor dimerizationDimeric conformationAtom molecular dynamics simulationsBiochemical experimentsMouse cellsMolecular mechanismsActive dimerΒ receptorBovine papillomavirusProteinSpecific interactionsMembrane modelingReceptor activationDimerizationComplexes
2016
Introduction
Enquist L, Dermody T, DiMaio D. Introduction. Annual Review Of Virology 2016, 3: 1-1. PMID: 29092671, DOI: 10.1146/annurev-vi-3-100316-100001.Peer-Reviewed Original Research
2015
Direct Binding of Retromer to Human Papillomavirus Type 16 Minor Capsid Protein L2 Mediates Endosome Exit during Viral Infection
Popa A, Zhang W, Harrison MS, Goodner K, Kazakov T, Goodwin EC, Lipovsky A, Burd CG, DiMaio D. Direct Binding of Retromer to Human Papillomavirus Type 16 Minor Capsid Protein L2 Mediates Endosome Exit during Viral Infection. PLOS Pathogens 2015, 11: e1004699. PMID: 25693203, PMCID: PMC4334968, DOI: 10.1371/journal.ppat.1004699.Peer-Reviewed Original ResearchConceptsTrans-Golgi networkRetromer cargoTransmembrane proteinGolgi apparatusDirect bindingCoat protein complexCellular transmembrane proteinsVirus entryMinor capsid proteinCarboxy-terminal segmentProtein complexesL2 minor capsid proteinMinor capsid protein L2Early endosomesVesicular transportRetromerPlasma membraneEndosomal membranesBinding motifProtein L2Capsid proteinEndosomesL2 proteinViral componentsProtein
2013
Genome-wide siRNA screen identifies the retromer as a cellular entry factor for human papillomavirus
Lipovsky A, Popa A, Pimienta G, Wyler M, Bhan A, Kuruvilla L, Guie MA, Poffenberger AC, Nelson CD, Atwood WJ, DiMaio D. Genome-wide siRNA screen identifies the retromer as a cellular entry factor for human papillomavirus. Proceedings Of The National Academy Of Sciences Of The United States Of America 2013, 110: 7452-7457. PMID: 23569269, PMCID: PMC3645514, DOI: 10.1073/pnas.1302164110.Peer-Reviewed Original ResearchConceptsTrans-Golgi networkHPV entryGenome-wide screenRetromer subunitsCellular genesScreen identifiesRetromerLate endosomesPotential antiviral targetsMultiple subunitsRetrograde pathwayTransport factorsCapsid proteinHeLa cellsCell entryAntiviral targetEndosomesGolgiVirus entryStable complexesEfficient infectionSubunitsHPV proteinsProteinImportant insights
2001
Induced senescence in HeLa cervical carcinoma cells containing elevated telomerase activity and extended telomeres.
Goodwin E, DiMaio D. Induced senescence in HeLa cervical carcinoma cells containing elevated telomerase activity and extended telomeres. Molecular Cancer Research 2001, 12: 525-34. PMID: 11714633.Peer-Reviewed Original ResearchConceptsTumor suppressor pathwayHeLa cervical carcinoma cellsExtended telomeresReplicative senescenceHTERT geneSuppressor pathwayTelomerase activityGrowth arrestCervical carcinoma cellsRepression of telomeraseElevated telomerase activitySomatic human cellsNormal somatic human cellsShort telomeresGrowth-arrested stateSenescence-associated beta-galactosidase expressionHPV E6/E7 expressionGrowth-arrested cellsHeLa cell clonesProfound growth arrestRole of telomeraseE6/E7 genesBeta-galactosidase expressionErosion of telomeresCarcinoma cells