2024
Cross-regulations of two connected domains form a mechanical circuit for steady force transmission during clathrin-mediated endocytosis
Ren Y, Yang J, Fujita B, Zhang Y, Berro J. Cross-regulations of two connected domains form a mechanical circuit for steady force transmission during clathrin-mediated endocytosis. Cell Reports 2024, 43: 114725. PMID: 39276354, PMCID: PMC11476202, DOI: 10.1016/j.celrep.2024.114725.Peer-Reviewed Original ResearchClathrin-mediated endocytosisF-actinActin cytoskeletonFission yeast Schizosaccharomyces pombeYeast Schizosaccharomyces pombeCell adhesion complexAdhesion complexesMembrane localizationPN forcesStable bindingEnd4pCross-regulationCytoskeletonActinEndocytosisMembraneBindingMechanical forcesTalinTransmission of forcesThatchForce transmissionDomainCellsFissionLipid osmosis, membrane tension, and other mechanochemical driving forces of lipid flow
Zhang Y, Lin C. Lipid osmosis, membrane tension, and other mechanochemical driving forces of lipid flow. Current Opinion In Cell Biology 2024, 88: 102377. PMID: 38823338, PMCID: PMC11193448, DOI: 10.1016/j.ceb.2024.102377.Peer-Reviewed Reviews, Practice Guidelines, Standards, and Consensus StatementsMembrane tensionLipid transportNonvesicular lipid transportLipid transfer proteinsOrganelle biogenesisLipid transferMembrane proteinsMembrane domainsLipid homeostasisBiological functionsLipid flowMembrane protein densityTransfer proteinMembrane regionsProtein densityProteinMembraneLipidBiogenesisOrganellesTomosyns attenuate SNARE assembly and synaptic depression by binding to VAMP2-containing template complexes
Meijer M, Öttl M, Yang J, Subkhangulova A, Kumar A, Feng Z, van Voorst T, Groffen A, van Weering J, Zhang Y, Verhage M. Tomosyns attenuate SNARE assembly and synaptic depression by binding to VAMP2-containing template complexes. Nature Communications 2024, 15: 2652. PMID: 38531902, PMCID: PMC10965968, DOI: 10.1038/s41467-024-46828-1.Peer-Reviewed Original ResearchConceptsSynaptobrevin-2/VAMP2SNARE assemblySNARE motifC-terminal polybasic regionSNAP-25 bindingSNARE complex assemblyTemplate complexStructure-function analysisMunc18-1Syntaxin-1Polybasic regionTomosynSNAP-25Membrane fusionSynaptic vesiclesSingle-molecule force measurementsEssential intermediateSNAREMotifInhibitory functionAssemblyMouse modelMunc18Synaptic transmissionSynaptic strength
2023
Force redistribution in clathrin-mediated endocytosis revealed by coiled-coil force sensors
Ren Y, Yang J, Fujita B, Jin H, Zhang Y, Berro J. Force redistribution in clathrin-mediated endocytosis revealed by coiled-coil force sensors. Science Advances 2023, 9: eadi1535. PMID: 37831774, PMCID: PMC10575576, DOI: 10.1126/sciadv.adi1535.Peer-Reviewed Original ResearchConceptsActin cytoskeletonPlasma membraneHuntingtin Interacting Protein 1Clathrin-mediated endocytosisCountless cellular processesEndocytic machineryCellular processesClathrin latticesProtein condensationCytoskeletonEnd4pProtein 1Membrane deformationPiconewton forcesEndocytosisVivo force measurementsMembranePiconewtonsClathrinMachineryProteinCoatMolecular scale
2022
A dynamic template complex mediates Munc18-chaperoned SNARE assembly
Yang J, Jin H, Liu Y, Guo Y, Zhang Y. A dynamic template complex mediates Munc18-chaperoned SNARE assembly. Proceedings Of The National Academy Of Sciences Of The United States Of America 2022, 119: e2215124119. PMID: 36454760, PMCID: PMC9894263, DOI: 10.1073/pnas.2215124119.Peer-Reviewed Original ResearchConceptsSoluble N-ethylmaleimide-sensitive factor attachment protein receptorsSNARE assemblyMunc18-3Munc18-1N-ethylmaleimide-sensitive factor attachment protein receptorsFactor attachment protein receptorsSNAP-25SNAP-25 bindingAttachment protein receptorsFour-helix bundleSynaptic vesicle fusionGlucose transporter translocationSNARE motifSNARE bundleSNAP-23Syntaxin 4GLUT4 translocationSyntaxin-1Transporter translocationPlasma membraneLinker regionMembrane fusionTemplate complexVesicle fusionMolecular mechanismsPolybasic patches in both C2 domains of synaptotagmin-1 are required for evoked neurotransmitter release
Wu Z, Tsemperouli M, Ma L, Courtney N, Zhu J, Zhang Y, Chapman E, Karatekin E. Polybasic patches in both C2 domains of synaptotagmin-1 are required for evoked neurotransmitter release. Biophysical Journal 2022, 121: 293a. DOI: 10.1016/j.bpj.2021.11.1283.Peer-Reviewed Original Research
2019
Synaptic vesicle fusion: today and beyond
Brose N, Brunger A, Cafiso D, Chapman ER, Diao J, Hughson FM, Jackson MB, Jahn R, Lindau M, Ma C, Rizo J, Shin YK, Söllner TH, Tamm L, Yoon TY, Zhang Y. Synaptic vesicle fusion: today and beyond. Nature Structural & Molecular Biology 2019, 26: 663-668. PMID: 31384060, DOI: 10.1038/s41594-019-0277-z.Peer-Reviewed Original ResearchAnimalsCalciumCryoelectron MicroscopyEndocytosisExocytosisHumansMacromolecular SubstancesMembrane FusionMembrane LipidsMembrane ProteinsNerve Tissue ProteinsNeurophysiologyNeurotransmitter AgentsOptical TweezersProtein Interaction MappingSingle Molecule ImagingSNARE ProteinsSynaptic TransmissionSynaptic Vesicles
2018
Munc18-1 catalyzes neuronal SNARE assembly by templating SNARE association
Jiao J, He M, Port SA, Baker RW, Xu Y, Qu H, Xiong Y, Wang Y, Jin H, Eisemann TJ, Hughson FM, Zhang Y. Munc18-1 catalyzes neuronal SNARE assembly by templating SNARE association. ELife 2018, 7: e41771. PMID: 30540253, PMCID: PMC6320071, DOI: 10.7554/elife.41771.Peer-Reviewed Original ResearchConceptsSNARE assemblyMunc18-1Sec1/Munc18-family (SM) proteinsSM protein Munc18-1Membrane fusionMunc18-1 mutationsNeuronal SNARE assemblyFour-helix bundleC-terminal regionN-terminal regionSingle-molecule force spectroscopySNARE motifSm proteinsSynaptic SNAREsMunc18-3SNARE zipperingProtein mechanismsTemplate complexForce spectroscopySnareZipperingProteinAssemblyComplexesVps33Single-Molecule Optical Tweezers Study of Regulated SNARE Assembly
Ma L, Jiao J, Zhang Y. Single-Molecule Optical Tweezers Study of Regulated SNARE Assembly. Methods In Molecular Biology 2018, 1860: 95-114. PMID: 30317500, PMCID: PMC6441361, DOI: 10.1007/978-1-4939-8760-3_6.Peer-Reviewed Original ResearchConceptsSoluble N-ethylmaleimide-sensitive factor attachment protein receptorsSNARE assemblyHigh-resolution optical tweezersN-ethylmaleimide-sensitive factor attachment protein receptorsMembrane fusionFactor attachment protein receptorsOptical tweezers studiesNeuronal SNARE assemblyIntracellular membrane fusionAttachment protein receptorsOptical tweezersΑ-SNAPDetailed experimental protocolCellular compartmentsRegulatory proteinsProtein receptorsDifferent cellsSpatiotemporal resolutionProteinAssemblyFusion processManipulation approachTweezersExperimental approachFusion
2017
Editorial Overview: Single-Molecule Approaches up to Difficult Challenges in Folding and Dynamics
Zhang Y, Ha T, Marqusee S. Editorial Overview: Single-Molecule Approaches up to Difficult Challenges in Folding and Dynamics. Journal Of Molecular Biology 2017, 430: 405-408. PMID: 29288633, PMCID: PMC5858691, DOI: 10.1016/j.jmb.2017.12.019.Peer-Reviewed Original ResearchSingle-molecule force spectroscopy of protein-membrane interactions
Ma L, Cai Y, Li Y, Jiao J, Wu Z, O'Shaughnessy B, De Camilli P, Karatekin E, Zhang Y. Single-molecule force spectroscopy of protein-membrane interactions. ELife 2017, 6: e30493. PMID: 29083305, PMCID: PMC5690283, DOI: 10.7554/elife.30493.Peer-Reviewed Original ResearchConceptsProtein-membrane interactionsC2 domainPlasma membraneMultiple C2 domainsSingle-molecule force spectroscopy approachSingle-molecule force spectroscopyOptical tweezersE-SytsUnprecedented spatiotemporal resolutionForce spectroscopyMembrane bindingMembrane fusionSingle proteinSynaptotagmin-1Biological processesEndoplasmic reticulumSpectroscopy approachLipid exchangeSynaptic vesiclesSynaptotagmin 2ProteinSilica beadsMechanical forcesHigh-resolution methodsSpatiotemporal resolutionTwo Disease-Causing SNAP-25B Mutations Selectively Impair SNARE C-terminal Assembly
Rebane AA, Wang B, Ma L, Qu H, Coleman J, Krishnakumar S, Rothman JE, Zhang Y. Two Disease-Causing SNAP-25B Mutations Selectively Impair SNARE C-terminal Assembly. Journal Of Molecular Biology 2017, 430: 479-490. PMID: 29056461, PMCID: PMC5805579, DOI: 10.1016/j.jmb.2017.10.012.Peer-Reviewed Original ResearchConceptsSoluble N-ethylmaleimide-sensitive factor attachment receptorSNARE assemblySynaptic exocytosisMembrane fusionSingle-molecule optical tweezersT-SNARE complexVesicle-associated SNAREsTarget plasma membraneC-terminal assemblyFour-helix bundleC-terminal regionSNARE complexPlasma membraneMolecular mechanismsZipperingMutationsNumerous diseasesAssembly energyNeurotransmitter releaseExocytosisAttachment receptorAssemblyNeurological disordersOptical tweezersComplexesEnergetics, kinetics, and pathway of SNARE folding and assembly revealed by optical tweezers
Zhang Y. Energetics, kinetics, and pathway of SNARE folding and assembly revealed by optical tweezers. Protein Science 2017, 26: 1252-1265. PMID: 28097727, PMCID: PMC5477538, DOI: 10.1002/pro.3116.Peer-Reviewed Original ResearchConceptsSoluble N-ethylmaleimide-sensitive factor attachment protein receptorsSynaptic soluble N-ethylmaleimide-sensitive factor attachment protein receptorSNARE assemblyMembrane fusionSNARE complexN-ethylmaleimide-sensitive factor attachment protein receptorsFactor attachment protein receptorsFast calcium-triggered fusionAttachment protein receptorsHigh-resolution optical tweezersCalcium-triggered fusionC-terminal domainFour-helix bundleNeurotransmitter-containing vesiclesLinker domainPlasma membraneDomain associationProtein receptorsMolecular engineDifferent functionsPathwayAssemblyMembraneOptical tweezersSynaptic transmission
2016
Stability, folding dynamics, and long-range conformational transition of the synaptic t-SNARE complex
Zhang X, Rebane AA, Ma L, Li F, Jiao J, Qu H, Pincet F, Rothman JE, Zhang Y. Stability, folding dynamics, and long-range conformational transition of the synaptic t-SNARE complex. Proceedings Of The National Academy Of Sciences Of The United States Of America 2016, 113: e8031-e8040. PMID: 27911771, PMCID: PMC5167175, DOI: 10.1073/pnas.1605748113.Peer-Reviewed Original ResearchMeSH KeywordsAmino Acid SequenceAnimalsMembrane FusionMiceMicroscopy, Atomic ForceMolecular Dynamics SimulationMunc18 ProteinsOptical TweezersProtein ConformationProtein DomainsProtein FoldingProtein StabilityQa-SNARE ProteinsSNARE ProteinsSynaptic TransmissionSynaptosomal-Associated Protein 25Vesicle-Associated Membrane Protein 2ConceptsSynaptic soluble N-ethylmaleimide-sensitive factor attachment protein receptorT-SNARE complexC-terminal domainN-terminal domainSNARE zipperingPlasma membraneN-ethylmaleimide-sensitive factor attachment protein receptorsSoluble N-ethylmaleimide-sensitive factor attachment protein receptorsFactor attachment protein receptorsTarget plasma membraneAttachment protein receptorsFour-helix bundleThree-helix bundleSynaptic vesicle fusionSingle-molecule force spectroscopyV-SNARESNARE assemblySNARE complexHelical bundleConformational switchC-terminusMembrane fusionVesicle fusionProtein receptorsZipperingSingle-Molecule Protein Folding Experiments Using High-Precision Optical Tweezers
Jiao J, Rebane AA, Ma L, Zhang Y. Single-Molecule Protein Folding Experiments Using High-Precision Optical Tweezers. Methods In Molecular Biology 2016, 1486: 357-390. PMID: 27844436, PMCID: PMC5508109, DOI: 10.1007/978-1-4939-6421-5_14.Peer-Reviewed Original ResearchConceptsOptical tweezersProtein complexesHigh-resolution optical tweezersSingle-molecule manipulationFolding of proteinsFundamental biological problemOptical trapSingle-molecule measurementsUnprecedented spatiotemporal resolutionThree-dimensional structureTweezersSingle proteinSpontaneous foldingDetailed protocolAmino acidsMolecule proteinProteinBiological problemsPowerful approachMechanical forcesFoldingSpatiotemporal resolutionEnergyTransition kineticsLinear chainsHidden Markov Modeling with Detailed Balance and Its Application to Single Protein Folding
Zhang Y, Jiao J, Rebane AA. Hidden Markov Modeling with Detailed Balance and Its Application to Single Protein Folding. Biophysical Journal 2016, 111: 2110-2124. PMID: 27851936, PMCID: PMC5112951, DOI: 10.1016/j.bpj.2016.09.045.Peer-Reviewed Original ResearchConceptsDetailed balanceThermodynamic equilibriumOptical tweezersIndependent fitting parametersDegenerate statesSingle-molecule trajectoriesSatisfies detailed balanceExtension trajectoriesEnergy landscapeFitting parametersShort trajectoriesProtein foldingExperimental dataTransition stateSNARE zipperingTweezersFree energyRegulation of DNA Translocation Efficiency within the Chromatin Remodeler RSC/Sth1 Potentiates Nucleosome Sliding and Ejection
Clapier CR, Kasten MM, Parnell TJ, Viswanathan R, Szerlong H, Sirinakis G, Zhang Y, Cairns BR. Regulation of DNA Translocation Efficiency within the Chromatin Remodeler RSC/Sth1 Potentiates Nucleosome Sliding and Ejection. Molecular Cell 2016, 62: 453-461. PMID: 27153540, PMCID: PMC5291166, DOI: 10.1016/j.molcel.2016.03.032.Peer-Reviewed Original ResearchMeSH KeywordsAdenosine TriphosphateBinding SitesBiological TransportCell Cycle ProteinsChromatin Assembly and DisassemblyDNA-Binding ProteinsDNA, FungalHydrolysisMicrofilament ProteinsMutationNuclear ProteinsNucleosomesProtein BindingProtein Interaction Domains and MotifsSaccharomyces cerevisiaeSaccharomyces cerevisiae ProteinsTime FactorsTranscription Factorsα-SNAP Enhances SNARE Zippering by Stabilizing the SNARE Four-Helix Bundle
Ma L, Kang Y, Jiao J, Rebane AA, Keun HK, Xi Z, Qu H, Zhang Y. α-SNAP Enhances SNARE Zippering by Stabilizing the SNARE Four-Helix Bundle. Cell Reports 2016, 15: 531-539. PMID: 27068468, PMCID: PMC4838522, DOI: 10.1016/j.celrep.2016.03.050.Peer-Reviewed Original ResearchConceptsSoluble N-ethylmaleimide-sensitive factor attachment protein receptorsC-terminal domainN-terminal domainMembrane fusionLinker domainΑ-SNAPSynaptic soluble N-ethylmaleimide-sensitive factor attachment protein receptorN-ethylmaleimide-sensitive factor attachment protein receptorsFactor attachment protein receptorsIntracellular membrane fusionAttachment protein receptorsConformational selection mechanismFour-helix bundleSNARE assemblySNARE complexProtein receptorsDynamic assemblyStepwise assemblyAssemblyDomainFusionZipperingOptical tweezersRecent experimentsReceptorsStructure-Based Derivation of Protein Folding Intermediates and Energies from Optical Tweezers
Rebane AA, Ma L, Zhang Y. Structure-Based Derivation of Protein Folding Intermediates and Energies from Optical Tweezers. Biophysical Journal 2016, 110: 441-454. PMID: 26789767, PMCID: PMC4724646, DOI: 10.1016/j.bpj.2015.12.003.Peer-Reviewed Original ResearchConceptsOptical tweezersSingle-molecule manipulation experimentsProtein Folding IntermediatesSingle-molecule trajectoriesAbsence of forceCorresponding experimental measurementsRepresentative protein complexesStructure‐based derivationIntrinsic extensionTransition ratesEnergy of proteinsPrevious data analysisTweezersExperimental measurementsEnergySynaptic SNARE proteinsSingle macromoleculeFolding intermediatesExperimental dataProtein structureFunction of forceTransition stateHigh-resolution structuresDifferent folding statesFolding statesAlpha-SNAP enhances SNARE zippering by stabilizing the SNARE four-helix bundle
L. Ma, Y. Kang, J. Y. Jiao, A. A. Rebane, H. K. Cha, Z. Xi, H. Qu, Y. L. Zhang, Alpha-SNAP enhances SNARE zippering by stabilizing the SNARE four-helix bundle. Cell Reports 15: 531-539 (2016).Peer-Reviewed Original Research