{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,6]],"date-time":"2026-10-06T13:04:55Z","timestamp":1791291895589,"version":"4.1.0"},"reference-count":67,"publisher":"Public Library of Science (PLoS)","issue":"12","license":[{"start":{"date-parts":[[2013,12,12]],"date-time":"2013-12-12T00:00:00Z","timestamp":1386806400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/3.0\/"}],"content-domain":{"domain":["www.plospathogens.org"],"crossmark-restriction":false},"short-container-title":["PLoS Pathog"],"DOI":"10.1371\/journal.ppat.1003821","type":"journal-article","created":{"date-parts":[[2013,12,13]],"date-time":"2013-12-13T01:52:33Z","timestamp":1386899553000},"page":"e1003821","update-policy":"https:\/\/doi.org\/10.1371\/journal.ppat.corrections_policy","source":"Crossref","is-referenced-by-count":110,"title":["Placental Syncytium Forms a Biophysical Barrier against Pathogen Invasion"],"prefix":"10.1371","volume":"9","author":[{"given":"Varvara B.","family":"Zeldovich","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Casper H.","family":"Clausen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Emily","family":"Bradford","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daniel A.","family":"Fletcher","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Emin","family":"Maltepe","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jennifer R.","family":"Robbins","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Anna I.","family":"Bakardjiev","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2013,12,12]]},"reference":[{"key":"ref1","doi-asserted-by":"crossref","first-page":"1500","DOI":"10.1056\/NEJM200005183422007","article-title":"Intrauterine infection and preterm delivery","volume":"342","author":"RL Goldenberg","year":"2000","journal-title":"N Engl J Med"},{"key":"ref2","doi-asserted-by":"crossref","first-page":"31","DOI":"10.2471\/BLT.08.062554","article-title":"The worldwide incidence of preterm birth: a systematic review of maternal mortality and morbidity","volume":"88","author":"S Beck","year":"2010","journal-title":"Bull World Health Organ"},{"key":"ref3","doi-asserted-by":"crossref","first-page":"36","DOI":"10.1016\/j.mib.2011.11.006","article-title":"Pathogens and the placental fortress","volume":"15","author":"JR Robbins","year":"2012","journal-title":"Curr Opin Microbiol"},{"issue":"Suppl 5","key":"ref4","doi-asserted-by":"crossref","first-page":"S405","DOI":"10.1093\/cid\/cis269","article-title":"Relative risk of listeriosis in Foodborne Diseases Active Surveillance Network (FoodNet) sites according to age, pregnancy, and ethnicity","volume":"54","author":"R Pouillot","year":"2012","journal-title":"Clin Infect Dis"},{"key":"ref5","first-page":"448","article-title":"Vital signs: Listeria illnesses, deaths, and outbreaks\u2013United States, 2009-2011","volume":"62","journal-title":"MMWR Morb Mortal Wkly Rep"},{"key":"ref6","doi-asserted-by":"crossref","first-page":"260","DOI":"10.1097\/00005792-200207000-00002","article-title":"Listeriosis during pregnancy: a case series and review of 222 cases","volume":"81","author":"E Mylonakis","year":"2002","journal-title":"Medicine (Baltimore)"},{"key":"ref7","doi-asserted-by":"crossref","first-page":"305","DOI":"10.3201\/eid0803.010195","article-title":"<italic>Listeria monocytogenes<\/italic> infection in Israel and review of cases worldwide","volume":"8","author":"Y Siegman-Igra","year":"2002","journal-title":"Emerg Infect Dis"},{"key":"ref8","first-page":"776","article-title":"<italic>Listeria<\/italic> infection during pregnancy: a 10 year experience","volume":"4","author":"A Benshushan","year":"2002","journal-title":"Isr Med Assoc J"},{"key":"ref9","doi-asserted-by":"crossref","first-page":"392","DOI":"10.1093\/oxfordjournals.aje.a115893","article-title":"The epidemiology of listeriosis in the United States\u20131986. Listeriosis Study Group","volume":"133","author":"BG Gellin","year":"1991","journal-title":"Am J Epidemiol"},{"key":"ref10","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1097\/00006454-199103000-00003","article-title":"Outbreak of neonatal listeriosis associated with mineral oil","volume":"10","author":"A Schuchat","year":"1991","journal-title":"Pediatr Infect Dis J"},{"key":"ref11","doi-asserted-by":"crossref","first-page":"244","DOI":"10.4315\/0362-028X-61.2.244","article-title":"Studies on the risk assessment of <italic>Listeria monocytogenes<\/italic>","volume":"61","author":"S Notermans","year":"1998","journal-title":"J Food Prot"},{"key":"ref12","doi-asserted-by":"crossref","first-page":"4063","DOI":"10.1172\/JCI70098","article-title":"Combinatory approaches prevent preterm birth profoundly exacerbated by gene-environment interactions","volume":"123","author":"J Cha","year":"2013","journal-title":"J Clin Invest"},{"key":"ref13","article-title":"Immunology of the Maternal-Fetal Interface","author":"A Erlebacher","year":"2013","journal-title":"Annu Rev Immunol"},{"key":"ref14","doi-asserted-by":"crossref","first-page":"e1002804","DOI":"10.1371\/journal.ppat.1002804","article-title":"Host defense and tolerance: unique challenges in the placenta","volume":"8","author":"VB Zeldovich","year":"2012","journal-title":"PLoS Pathog"},{"key":"ref15","first-page":"320","article-title":"Some immunological and endocrinological problems raised by the evolution of viviparity in vertebrates","volume":"7","author":"PB Medawar","year":"1953","journal-title":"Symp Soc Exp Biol"},{"key":"ref16","doi-asserted-by":"crossref","first-page":"80","DOI":"10.1111\/j.1749-6632.2010.05938.x","article-title":"Inflammation and pregnancy: the role of the immune system at the implantation site","volume":"1221","author":"G Mor","year":"2011","journal-title":"Ann N Y Acad Sci"},{"key":"ref17","doi-asserted-by":"crossref","first-page":"12048","DOI":"10.1073\/pnas.1304718110","article-title":"Human placental trophoblasts confer viral resistance to recipient cells","volume":"110","author":"E Delorme-Axford","year":"2013","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref18","doi-asserted-by":"crossref","first-page":"1016","DOI":"10.1172\/JCI41211","article-title":"The placenta: transcriptional, epigenetic, and physiological integration during development","volume":"120","author":"E Maltepe","year":"2010","journal-title":"J Clin Invest"},{"key":"ref19","unstructured":"Benirschke K, Kaufmann P, Baergen RN (2006) Pathology of the Human Placenta."},{"key":"ref20","doi-asserted-by":"crossref","first-page":"e1000732","DOI":"10.1371\/journal.ppat.1000732","article-title":"Placental syncytiotrophoblast constitutes a major barrier to vertical transmission of <italic>Listeria monocytogenes<\/italic>","volume":"6","author":"JR Robbins","year":"2010","journal-title":"PLoS Pathog"},{"key":"ref21","doi-asserted-by":"crossref","first-page":"418","DOI":"10.1128\/IAI.05899-11","article-title":"Tissue barriers of the human placenta to infection with <italic>Toxoplasma gondii<\/italic>","volume":"80","author":"JR Robbins","year":"2012","journal-title":"Infect Immun"},{"key":"ref22","doi-asserted-by":"crossref","first-page":"1572","DOI":"10.1095\/biolreprod.102.004325","article-title":"Syncytiotrophoblast is a barrier to maternal-fetal transmission of herpes simplex virus","volume":"67","author":"H Koi","year":"2002","journal-title":"Biol Reprod"},{"key":"ref23","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1016\/j.placenta.2008.12.001","article-title":"Adhesion molecules in human trophoblast - a review. I. Villous trophoblast","volume":"30","author":"JD Aplin","year":"2009","journal-title":"Placenta"},{"key":"ref24","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1083\/jcb.201106011","article-title":"Impenetrable barriers or entry portals? The role of cell-cell adhesion during infection","volume":"195","author":"M Bonazzi","year":"2011","journal-title":"J Cell Biol"},{"key":"ref25","doi-asserted-by":"crossref","first-page":"305","DOI":"10.1098\/rspb.1981.0041","article-title":"Morphogenesis of human placental chorionic villi: cytoskeletal, syncytioskeletal and extracellular matrix proteins","volume":"212","author":"CD Ockleford","year":"1981","journal-title":"Proc R Soc Lond B Biol Sci"},{"key":"ref26","doi-asserted-by":"crossref","first-page":"e56949","DOI":"10.1371\/journal.pone.0056949","article-title":"ECM-Dependent HIF Induction Directs Trophoblast Stem Cell Fate via LIMK1-Mediated Cytoskeletal Rearrangement","volume":"8","author":"HJ Choi","year":"2013","journal-title":"PLoS One"},{"key":"ref27","doi-asserted-by":"crossref","first-page":"2072","DOI":"10.1126\/science.282.5396.2072","article-title":"Promotion of trophoblast stem cell proliferation by FGF4","volume":"282","author":"S Tanaka","year":"1998","journal-title":"Science"},{"key":"ref28","doi-asserted-by":"crossref","first-page":"2005","DOI":"10.4049\/jimmunol.139.6.2005","article-title":"Adoptive transfer of immunity to <italic>Listeria monocytogenes<\/italic>. The influence of in vitro stimulation on lymphocyte subset requirements","volume":"139","author":"DK Bishop","year":"1987","journal-title":"J Immunol"},{"key":"ref29","doi-asserted-by":"crossref","first-page":"6152","DOI":"10.1073\/pnas.0401434101","article-title":"Targeting and crossing of the human maternofetal barrier by <italic>Listeria monocytogenes<\/italic>: role of internalin interaction with trophoblast E-cadherin","volume":"101","author":"M Lecuit","year":"2004","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref30","doi-asserted-by":"crossref","first-page":"489","DOI":"10.1128\/IAI.72.1.489-497.2004","article-title":"Listeriosis in the pregnant guinea pig: a model of vertical transmission","volume":"72","author":"AI Bakardjiev","year":"2004","journal-title":"Infect Immun"},{"key":"ref31","doi-asserted-by":"crossref","first-page":"3956","DOI":"10.1093\/emboj\/18.14.3956","article-title":"A single amino acid in E-cadherin responsible for host specificity towards the human pathogen <italic>Listeria monocytogenes<\/italic>","volume":"18","author":"M Lecuit","year":"1999","journal-title":"EMBO J"},{"key":"ref32","doi-asserted-by":"crossref","first-page":"891","DOI":"10.1016\/j.cell.2007.03.049","article-title":"Extending the host range of <italic>Listeria monocytogenes<\/italic> by rational protein design","volume":"129","author":"T Wollert","year":"2007","journal-title":"Cell"},{"key":"ref33","doi-asserted-by":"crossref","first-page":"228","DOI":"10.1103\/PhysRevLett.56.228","article-title":"Correlation between domain boundaries and surface steps: A scanning-tunneling-microscopy study on reconstructed Pt(100)","volume":"56","author":"RJ Behm","year":"1986","journal-title":"Phys Rev Lett"},{"key":"ref34","doi-asserted-by":"crossref","first-page":"495","DOI":"10.1089\/ten.tea.2010.0211","article-title":"Elastic properties of induced pluripotent stem cells","volume":"17","author":"KE Hammerick","year":"2011","journal-title":"Tissue Eng Part A"},{"key":"ref35","doi-asserted-by":"crossref","first-page":"1973","DOI":"10.1021\/bi00221a034","article-title":"Effects of cytochalasin, phalloidin, and pH on the elongation of actin filaments","volume":"30","author":"P Sampath","year":"1991","journal-title":"Biochemistry"},{"key":"ref36","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1016\/j.jbiomech.2004.11.019","article-title":"Effect of actin filament distribution on tensile properties of smooth muscle cells obtained from rat thoracic aortas","volume":"39","author":"K Nagayama","year":"2006","journal-title":"J Biomech"},{"key":"ref37","doi-asserted-by":"crossref","first-page":"445101","DOI":"10.1088\/0957-4484\/21\/44\/445101","article-title":"Stress relaxation and creep on living cells with the atomic force microscope: a means to calculate elastic moduli and viscosities of cell components","volume":"21","author":"S Moreno-Flores","year":"2010","journal-title":"Nanotechnology"},{"key":"ref38","doi-asserted-by":"crossref","first-page":"1025","DOI":"10.1242\/jcs.114.5.1025","article-title":"Effects of cytochalasin D and latrunculin B on mechanical properties of cells","volume":"114","author":"T Wakatsuki","year":"2001","journal-title":"J Cell Sci"},{"key":"ref39","doi-asserted-by":"crossref","first-page":"520","DOI":"10.1016\/S0006-3495(00)76614-8","article-title":"Drug-induced changes of cytoskeletal structure and mechanics in fibroblasts: an atomic force microscopy study","volume":"78","author":"C Rotsch","year":"2000","journal-title":"Biophys J"},{"key":"ref40","doi-asserted-by":"crossref","first-page":"1344","DOI":"10.1128\/IAI.69.3.1344-1350.2001","article-title":"<italic>Listeria monocytogenes<\/italic>-infected phagocytes can initiate central nervous system infection in mice","volume":"69","author":"DA Drevets","year":"2001","journal-title":"Infect Immun"},{"key":"ref41","doi-asserted-by":"crossref","first-page":"e66","DOI":"10.1371\/journal.ppat.0020066","article-title":"<italic>Listeria monocytogenes<\/italic> traffics from maternal organs to the placenta and back","volume":"2","author":"AI Bakardjiev","year":"2006","journal-title":"PLoS Pathog"},{"key":"ref42","doi-asserted-by":"crossref","first-page":"633","DOI":"10.1046\/j.1462-5822.2001.00143.x","article-title":"Actin-based motility is sufficient for bacterial membrane protrusion formation and host cell uptake","volume":"3","author":"DM Monack","year":"2001","journal-title":"Cell Microbiol"},{"key":"ref43","doi-asserted-by":"crossref","first-page":"1333","DOI":"10.1083\/jcb.146.6.1333","article-title":"<italic>Listeria monocytogenes<\/italic> exploits normal host cell processes to spread from cell to cell","volume":"146","author":"JR Robbins","year":"1999","journal-title":"J Cell Biol"},{"key":"ref44","doi-asserted-by":"crossref","first-page":"1597","DOI":"10.1083\/jcb.109.4.1597","article-title":"Actin filaments and the growth, movement, and spread of the intracellular bacterial parasite, <italic>Listeria monocytogenes<\/italic>","volume":"109","author":"LG Tilney","year":"1989","journal-title":"J Cell Biol"},{"key":"ref45","doi-asserted-by":"crossref","first-page":"1231","DOI":"10.1083\/jcb.131.5.1231","article-title":"Ezrin oligomers are major cytoskeletal components of placental microvilli: a proposal for their involvement in cortical morphogenesis","volume":"131","author":"M Berryman","year":"1995","journal-title":"J Cell Biol"},{"key":"ref46","doi-asserted-by":"crossref","first-page":"320","DOI":"10.1016\/S0022-5320(83)90043-6","article-title":"The organization of actin filaments in human placental villi","volume":"85","author":"BF King","year":"1983","journal-title":"J Ultrastruct Res"},{"key":"ref47","doi-asserted-by":"crossref","first-page":"2341","DOI":"10.1016\/j.bpj.2011.09.050","article-title":"Native ultrastructure of the red cell cytoskeleton by cryo-electron tomography","volume":"101","author":"A Nans","year":"2011","journal-title":"Biophys J"},{"key":"ref48","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.jbbm.2005.11.003","article-title":"Stiffness of normal and pathological erythrocytes studied by means of atomic force microscopy","volume":"66","author":"I Dulinska","year":"2006","journal-title":"J Biochem Biophys Methods"},{"key":"ref49","doi-asserted-by":"crossref","first-page":"497","DOI":"10.1111\/j.1365-2141.2008.07219.x","article-title":"Increased leukaemia cell stiffness is associated with symptoms of leucostasis in paediatric acute lymphoblastic leukaemia","volume":"142","author":"WA Lam","year":"2008","journal-title":"Br J Haematol"},{"key":"ref50","doi-asserted-by":"crossref","first-page":"112ra122","DOI":"10.1126\/scitranslmed.3002761","article-title":"Age-related intimal stiffening enhances endothelial permeability and leukocyte transmigration","volume":"3","author":"J Huynh","year":"2011","journal-title":"Sci Transl Med"},{"key":"ref51","doi-asserted-by":"crossref","first-page":"6493","DOI":"10.1073\/pnas.1031670100","article-title":"Compression forces generated by actin comet tails on lipid vesicles","volume":"100","author":"PA Giardini","year":"2003","journal-title":"Proc Natl Acad Sci U S A"},{"key":"ref52","doi-asserted-by":"crossref","first-page":"1212","DOI":"10.1038\/ncb1964","article-title":"The bacterial virulence factor InlC perturbs apical cell junctions and promotes cell-to-cell spread of <italic>Listeria<\/italic>","volume":"11","author":"T Rajabian","year":"2009","journal-title":"Nat Cell Biol"},{"key":"ref53","doi-asserted-by":"crossref","first-page":"342","DOI":"10.1016\/j.pbi.2007.05.001","article-title":"Cytoskeleton and cell wall function in penetration resistance","volume":"10","author":"AR Hardham","year":"2007","journal-title":"Curr Opin Plant Biol"},{"key":"ref54","doi-asserted-by":"crossref","first-page":"4333","DOI":"10.1242\/jcs.103648","article-title":"Toxofilin upregulates the host cortical actin cytoskeleton dynamics, facilitating <italic>Toxoplasma<\/italic> invasion","volume":"125","author":"V Delorme-Walker","year":"2012","journal-title":"J Cell Sci"},{"key":"ref55","doi-asserted-by":"crossref","first-page":"259","DOI":"10.1016\/j.chom.2009.01.011","article-title":"Host cell entry by apicomplexa parasites requires actin polymerization in the host cell","volume":"5","author":"V Gonzalez","year":"2009","journal-title":"Cell Host Microbe"},{"key":"ref56","doi-asserted-by":"crossref","first-page":"110 e111","DOI":"10.1016\/j.ajog.2007.05.044","article-title":"Detection of bacteria in placental tissues obtained from extremely low gestational age neonates","volume":"198","author":"AB Onderdonk","year":"2008","journal-title":"Am J Obstet Gynecol"},{"key":"ref57","doi-asserted-by":"crossref","first-page":"13301","DOI":"10.1128\/JVI.77.24.13301-13314.2003","article-title":"Human cytomegalovirus transmission from the uterus to the placenta correlates with the presence of pathogenic bacteria and maternal immunity","volume":"77","author":"L Pereira","year":"2003","journal-title":"J Virol"},{"key":"ref58","doi-asserted-by":"crossref","first-page":"110","DOI":"10.1111\/j.1600-0897.2010.00908.x","article-title":"Placental viral infection sensitizes to endotoxin-induced pre-term labor: a double hit hypothesis","volume":"65","author":"I Cardenas","year":"2011","journal-title":"Am J Reprod Immunol"},{"key":"ref59","doi-asserted-by":"crossref","first-page":"1248","DOI":"10.4049\/jimmunol.1000289","article-title":"Viral infection of the placenta leads to fetal inflammation and sensitization to bacterial products predisposing to preterm labor","volume":"185","author":"I Cardenas","year":"2010","journal-title":"J Immunol"},{"key":"ref60","doi-asserted-by":"crossref","first-page":"273","DOI":"10.1016\/j.placenta.2003.09.010","article-title":"Syncytiotrophoblast degradation and the pathophysiology of the malaria-infected placenta","volume":"25","author":"IP Crocker","year":"2004","journal-title":"Placenta"},{"key":"ref61","doi-asserted-by":"crossref","first-page":"154","DOI":"10.1095\/biolreprod.112.106195","article-title":"Histopathologies, immunolocalization, and a glycan binding screen provide insights into <italic>Plasmodium falciparum<\/italic> interactions with the human placenta","volume":"88","author":"BS Hromatka","year":"2013","journal-title":"Biol Reprod"},{"key":"ref62","doi-asserted-by":"crossref","first-page":"356","DOI":"10.1016\/j.placenta.2011.02.005","article-title":"<italic>Trypanosoma cruzi<\/italic> induces apoptosis in ex vivo infected human chorionic villi","volume":"32","author":"J Duaso","year":"2011","journal-title":"Placenta"},{"key":"ref63","doi-asserted-by":"crossref","first-page":"202","DOI":"10.4269\/ajtmh.2011.10-0589","article-title":"Placental malaria and mother-to-child transmission of human immunodeficiency virus-1 in rural Rwanda","volume":"85","author":"PL Bulterys","year":"2011","journal-title":"Am J Trop Med Hyg"},{"key":"ref64","doi-asserted-by":"crossref","first-page":"663","DOI":"10.1016\/j.placenta.2012.05.005","article-title":"From ancestral infectious retroviruses to bona fide cellular genes: role of the captured syncytins in placentation","volume":"33","author":"A Dupressoir","year":"2012","journal-title":"Placenta"},{"key":"ref65","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1016\/S0304-3991(00)00077-2","article-title":"Thermomechanical noise of a free v-shaped cantilever for atomic-force microscopy","volume":"86","author":"RW Stark","year":"2001","journal-title":"Ultramicroscopy"},{"key":"ref66","doi-asserted-by":"crossref","first-page":"1777","DOI":"10.1016\/S0006-3495(04)74245-9","article-title":"Quantitative analysis of the viscoelastic properties of thin regions of fibroblasts using atomic force microscopy","volume":"86","author":"RE Mahaffy","year":"2004","journal-title":"Biophys J"},{"issue":"Pt 3","key":"ref67","doi-asserted-by":"crossref","first-page":"857","DOI":"10.1242\/jcs.103.3.857","article-title":"Dynamics of three-dimensional replication patterns during the S-phase, analysed by double labelling of DNA and confocal microscopy","volume":"103","author":"EM Manders","year":"1992","journal-title":"J Cell Sci"}],"container-title":["PLoS Pathogens"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.ppat.1003821","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,7,8]],"date-time":"2023-07-08T23:22:34Z","timestamp":1688858554000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.ppat.1003821"}},"subtitle":[],"editor":[{"given":"Michael R.","family":"Wessels","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2013,12,12]]},"references-count":67,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2013,12,12]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.ppat.1003821","relation":{},"ISSN":["1553-7374"],"issn-type":[{"value":"1553-7374","type":"electronic"}],"subject":[],"published":{"date-parts":[[2013,12,12]]}}}