Peri/epicellular protein disulfide isomerase-A1 acts as an upstream organizer of cytoskeletal mechanoadaptation in vascular smooth muscle cells

Página do item simplificado
dc.contributorSistema FMUSP-HC: Faculdade de Medicina da Universidade de São Paulo (FMUSP) e Hospital das Clínicas da FMUSP
dc.contributor.authorTANAKA, Leonardo Y.
dc.contributor.authorARAUJO, Thais L. S.
dc.contributor.authorI, Andres Rodriguez
dc.contributor.authorFERRAZ, Mariana S.
dc.contributor.authorPELEGATI, Vitor B.
dc.contributor.authorMORAIS, Mauro C. C.
dc.contributor.authorSANTOS, Aline M. dos
dc.contributor.authorCESAR, Carlos L.
dc.contributor.authorRAMOS, Alexandre F.
dc.contributor.authorALENCAR, Adriano M.
dc.contributor.authorLAURINDO, Francisco R. M.
dc.date.accessioned2019-05-30T13:46:24Z
dc.date.available2019-05-30T13:46:24Z
dc.date.issued2019
dc.description.abstractAlthough redox processes closely interplay with mechanoresponses to control vascular remodeling, redox pathways coupling mechanostimulation to cellular cytoskeletal organization remain unclear. The peri/epicellular pool of protein disulfide isomerase-A1 (pecPDIA1) supports postinjury vessel remodeling. Using distinct models, we investigated whether pecPDIA1 could work as a redox-dependent organizer of cytoskeletal mechanoresponses. In vascular smooth muscle cells (VSMCs), pecPDIA1 immunoneutralization impaired stress fiber assembly in response to equibiaxial stretch and, under uniaxial stretch, significantly perturbed cell repositioning perpendicularly to stretch orientation. During cyclic stretch, pecPDIA1 supported thiol oxidation of the known mechanosensor beta(1)-integrin and promoted polarized compartmentalization of suifenylated proteins. Using traction force microscopy, we showed that pecPDIA1 organizes intracellular force distribution. The net contractile moment ratio of platelet-derived growth factor-exposed to basal VSMCs decreased from 0.90 +/- 0.09 (IgG-exposed controls) to 0.70 +/- 0.08 after pecPDIA1 neutralization (P < 0.05), together with an enhanced coefficient of variation for distribution of force modules, suggesting increased noise. Moreover, in a single cell model, pecPDIA1 neutralization impaired migration persistence without affecting total distance or velocity, whereas siRNA-mediated total PDIA1 silencing disabled all such variables of VSMC migration. Neither expression nor total activity of the master mechanotransmitter/regulator RhoA was affected by pecPDIA1 neutralization. However, cyclic stretch-induced focal distribution of membrane-bound RhoA was disrupted by pecPDI inhibition, which promoted a nonpolarized pattern of RhoA/caveolin-3 cluster colocalization. Accordingly, FRET biosensors showed that pecPDIA1 supports localized RhoA activity at cell protrusions versus perinuclear regions. Thus. pecPDI acts as a thiol redox-dependent organizer and noise reducer mechanism of cytoskeletal repositioning, oxidant generation, and localized RhoA activation during a variety of VSMC mechanoresponses. NEW & NOTEWORTHY Effects of a peri/epicellular pool of protein disulfide isomerase-A1 (pecPDIA1) during mechanoregulation in vascular smooth muscle cells (VSMCs) were highlighted using approaches such as equibiaxial and uniaxial stretch, random single cell migration, and traction force microscopy. pecPDIA1 regulates organization of the cytoskeleton and minimizes the noise of cell alignment, migration directionality, and persistence. pecPDIA1 mechanisms involve redox control of beta(1)-integrin and localized RhoA activation. pecPDIA1 acts as a novel organizer of mechanoadaptation responses in VSMCs.eng
dc.description.indexMEDLINEeng
dc.description.sponsorshipCentros de Pesquisa, Inovacao e Difusao Redoxoma-Fundacao de Amparo a Pesquisa do Estado de Sao Paulo (FAPESP) [2013/07937-8]
dc.description.sponsorshipFundacao Zerbini
dc.description.sponsorshipPrograma de Pos-Graduacao em Oncologia, Instituto do Cancer do Estado de Sao Paulo
dc.description.sponsorshipCoordenacao de Aperfeicoamento de Pessoal de Nivel Superior (CAPES)
dc.description.sponsorshipPrograma Nacional de Pos-Doutoramento
dc.description.sponsorshipCAPES
dc.description.sponsorshipFAPESP [2013/17115-5, 2015/06210-2, 2013/06241-0]
dc.identifier.citationAMERICAN JOURNAL OF PHYSIOLOGY-HEART AND CIRCULATORY PHYSIOLOGY, v.316, n.3, p.H566-H579, 2019
dc.identifier.doi10.1152/ajpheart.00379.2018
dc.identifier.eissn1522-1539
dc.identifier.issn0363-6135
dc.identifier.urihttps://observatorio.fm.usp.br/handle/OPI/31958
dc.language.isoeng
dc.publisherAMER PHYSIOLOGICAL SOCeng
dc.relation.ispartofAmerican Journal of Physiology-Heart and Circulatory Physiology
dc.rightsrestrictedAccesseng
dc.rights.holderCopyright AMER PHYSIOLOGICAL SOCeng
dc.subjectcytoskeletoneng
dc.subjectmechanobiologyeng
dc.subjectprotein disulfide isomeraseeng
dc.subjectredoxeng
dc.subjectvascular smooth muscle cellseng
dc.subject.otheroxidaseeng
dc.subject.otherrhoaeng
dc.subject.otheractivationeng
dc.subject.othermigrationeng
dc.subject.otherexpressioneng
dc.subject.otheroxidationeng
dc.subject.othercofilineng
dc.subject.wosCardiac & Cardiovascular Systemseng
dc.subject.wosPhysiologyeng
dc.subject.wosPeripheral Vascular Diseaseeng
dc.titlePeri/epicellular protein disulfide isomerase-A1 acts as an upstream organizer of cytoskeletal mechanoadaptation in vascular smooth muscle cellseng
dc.typearticleeng
dc.type.categoryoriginal articleeng
dc.type.versionpublishedVersioneng
dspace.entity.typePublication
hcfmusp.affiliation.countryChile
hcfmusp.affiliation.countryisocl
hcfmusp.author.externalI, Andres Rodriguez:Univ Sao Paulo, Sch Med, Heart Inst, Vasc Biol Lab, Sao Paulo, Brazil; Univ Bio Bio, Fac Sci, Dept Basic Sci, Grp Res & Innovat Vasc Hlth, Chillan, Chile
hcfmusp.author.externalFERRAZ, Mariana S.:Univ Sao Paulo, Inst Phys, Sao Paulo, Brazil
hcfmusp.author.externalPELEGATI, Vitor B.:Univ Estadual Campinas, Gleb Wataghin Inst Phys, Campinas, SP, Brazil
hcfmusp.author.externalSANTOS, Aline M. dos:Univ Estadual Campinas, Inst Biol, Dept Struct & Funct Biol, Campinas, SP, Brazil
hcfmusp.author.externalCESAR, Carlos L.:Univ Estadual Campinas, Gleb Wataghin Inst Phys, Campinas, SP, Brazil
hcfmusp.author.externalALENCAR, Adriano M.:Univ Sao Paulo, Inst Phys, Sao Paulo, Brazil
hcfmusp.citation.scopus17
hcfmusp.contributor.author-fmusphcLEONARDO YUJI TANAKA
hcfmusp.contributor.author-fmusphcTHAIS LARISSA ARAUJO DE OLIVEIRA SILVA
hcfmusp.contributor.author-fmusphcMAURO CESAR CAFUNDO DE MORAIS
hcfmusp.contributor.author-fmusphcALEXANDRE FERREIRA RAMOS
hcfmusp.contributor.author-fmusphcFRANCISCO RAFAEL MARTINS LAURINDO
hcfmusp.description.beginpageH566
hcfmusp.description.endpageH579
hcfmusp.description.issue3
hcfmusp.description.volume316
hcfmusp.origemWOS
hcfmusp.origem.pubmed30499716
hcfmusp.origem.scopus2-s2.0-85061485653
hcfmusp.origem.wosWOS:000460561200013
hcfmusp.publisher.cityBETHESDAeng
hcfmusp.publisher.countryUSAeng
hcfmusp.relation.referenceAraujo TLS, 2017, FREE RADICAL BIO MED, V103, P199, DOI 10.1016/j.freeradbiomed.2016.12.021eng
hcfmusp.relation.referenceBenham AM, 2012, ANTIOXID REDOX SIGN, V16, P781, DOI 10.1089/ars.2011.4439eng
hcfmusp.relation.referenceBurgess A, 2010, P NATL ACAD SCI USA, V107, P12564, DOI 10.1073/pnas.0914191107eng
hcfmusp.relation.referenceButler JP, 2002, AM J PHYSIOL-CELL PH, V282, pC595, DOI 10.1152/ajpcell.00270.2001eng
hcfmusp.relation.referenceCameron JM, 2015, CURR BIOL, V25, P1520, DOI 10.1016/j.cub.2015.04.020eng
hcfmusp.relation.referenceCrescente M, 2016, ARTERIOSCL THROM VAS, V36, P1164, DOI 10.1161/ATVBAHA.116.307461eng
hcfmusp.relation.referenceDajnowiec D, 2007, CLIN SCI, V113, P15, DOI 10.1042/CS200602337eng
hcfmusp.relation.referenceDamughatla AR, 2015, J MAGN RESON IMAGING, V41, P44, DOI 10.1002/jmri.24506eng
hcfmusp.relation.referenceDatla SR, 2014, AM J PHYSIOL-HEART C, V307, pH945, DOI 10.1152/ajpheart.00918.2013eng
hcfmusp.relation.referenceDOBRIN PB, 1978, PHYSIOL REV, V58, P397eng
hcfmusp.relation.referenceDovas A, 2005, BIOCHEM J, V390, P1, DOI 10.1042/BJ20050104eng
hcfmusp.relation.referenceEble JA, 2014, ANTIOXID REDOX SIGN, V20, P1977, DOI 10.1089/ars.2013.5294eng
hcfmusp.relation.referenceFernandes DC, 2007, AM J PHYSIOL-CELL PH, V292, pC413, DOI 10.1152/ajpcell.00188.2006eng
hcfmusp.relation.referenceFernandes DC, 2009, ARCH BIOCHEM BIOPHYS, V484, P197, DOI 10.1016/j.abb.2009.01.022eng
hcfmusp.relation.referenceFlaumenhaft R, 2016, BLOOD, V128, P893, DOI 10.1182/blood-2016-04-636456eng
hcfmusp.relation.referenceGoldyn AM, 2009, J CELL SCI, V122, P3644, DOI 10.1242/jcs.054866eng
hcfmusp.relation.referenceHahn C, 2009, NAT REV MOL CELL BIO, V10, P53, DOI 10.1038/nrm2596eng
hcfmusp.relation.referenceJaniszewski M, 2005, J BIOL CHEM, V280, P40813, DOI 10.1074/jbc.M509255200eng
hcfmusp.relation.referenceKawamura S, 2003, J BIOL CHEM, V278, P31111, DOI 10.1074/jbc.M300725200eng
hcfmusp.relation.referenceKrishnan R, 2011, AM J PHYSIOL-CELL PH, V300, pC146, DOI 10.1152/ajpcell.00195.2010eng
hcfmusp.relation.referenceLahav J, 2002, BLOOD, V100, P2472, DOI 10.1182/blood-2002-12-0339eng
hcfmusp.relation.referenceLaurindo FRM, 2012, FREE RADICAL BIO MED, V52, P1954, DOI 10.1016/j.freeradbiomed.2012.02.037eng
hcfmusp.relation.referenceMontenegro MF, 2015, FREE RADICAL BIO MED, V85, P288, DOI 10.1016/j.freeradbiomed.2015.05.011eng
hcfmusp.relation.referenceMoretti AIS, 2017, SCI REP-UK, V7, DOI 10.1038/s41598-017-16947-5eng
hcfmusp.relation.referenceOchoa CD, 2008, AM J RESP CELL MOL, V39, P105, DOI 10.1165/rcmb.2007-0283OCeng
hcfmusp.relation.referencePeixoto AS, 2018, J BIOL CHEM, V293, P1450, DOI 10.1074/jbc.M117.807016eng
hcfmusp.relation.referencePereira MBM, 2015, NAT COMMUN, V6, DOI 10.1038/ncomms7508eng
hcfmusp.relation.referencePereira MBM, 2014, NAT COMMUN, V5, DOI 10.1038/ncomms6159eng
hcfmusp.relation.referencePertz O, 2006, NATURE, V440, P1069, DOI 10.1038/nature04665eng
hcfmusp.relation.referencePescatore LA, 2012, J BIOL CHEM, V287, P29290, DOI 10.1074/jbc.M112.394551eng
hcfmusp.relation.referenceRodriguez AI, 2015, ARTERIOSCL THROM VAS, V35, P430, DOI 10.1161/ATVBAHA.114.304936eng
hcfmusp.relation.referenceSadok A, 2009, MOL CELL BIOL, V29, P3915, DOI 10.1128/MCB.01199-08eng
hcfmusp.relation.referenceSathyanesan A, 2012, J NEUROSCI METH, V206, P165, DOI 10.1016/j.jneumeth.2012.02.019eng
hcfmusp.relation.referenceSchad JF, 2011, VASC CELL, V3, DOI 10.1186/2045-824X-3-21eng
hcfmusp.relation.referenceMoretti AIS, 2017, ARCH BIOCHEM BIOPHYS, V617, P106, DOI 10.1016/j.abb.2016.11.007eng
hcfmusp.relation.referenceTanaka LY, 2017, FREE RADICAL BIO MED, V109, P11, DOI 10.1016/j.freeradbiomed.2017.01.025eng
hcfmusp.relation.referenceTanaka LY, 2016, HYPERTENSION, V67, P613, DOI 10.1161/HYPERTENSIONAHA.115.06177eng
hcfmusp.relation.referenceWang C, 2012, J BIOL CHEM, V287, P1139, DOI 10.1074/jbc.M111.303149eng
hcfmusp.relation.referenceZhang WW, 2012, J BIOL CHEM, V287, P33996, DOI 10.1074/jbc.M112.369603eng
hcfmusp.scopus.lastupdate2024-05-10
relation.isAuthorOfPublication2dd31d46-e17e-49fc-b4f7-35ec3c057da4
relation.isAuthorOfPublicationf98e9e81-ce05-43ed-a417-ef7787254873
relation.isAuthorOfPublicationc938ebbc-934d-4887-8b84-c6196008921f
relation.isAuthorOfPublication8e2158f8-af61-4104-9d42-c82b5e8efc1a
relation.isAuthorOfPublicationda503f9f-63c6-457e-8bca-832eafee1091
relation.isAuthorOfPublication.latestForDiscovery2dd31d46-e17e-49fc-b4f7-35ec3c057da4
Arquivos
Pacote Original
Agora exibindo 1 - 1 de 1
Nenhuma Miniatura disponível
Nome:
art_TANAKA_Periepicellular_protein_disulfide_isomeraseA1_acts_as_an_upstream_2019.PDF
Tamanho:
4.41 MB
Formato:
Adobe Portable Document Format
Descrição:
publishedVersion (English)
Baixar
Coleções
Artigos e Materiais de Revistas Científicas - HC/InCor
Artigos e Materiais de Revistas Científicas - LIM/24
Artigos e Materiais de Revistas Científicas - LIM/64