{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,3]],"date-time":"2026-06-03T01:42:16Z","timestamp":1780450936040,"version":"3.54.1"},"reference-count":64,"publisher":"MDPI AG","issue":"9","license":[{"start":{"date-parts":[[2018,9,14]],"date-time":"2018-09-14T00:00:00Z","timestamp":1536883200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100003042","name":"Else Kr\u00f6ner-Fresenius-Stiftung","doi-asserted-by":"publisher","award":["2014-A45 and 2016-A126"],"award-info":[{"award-number":["2014-A45 and 2016-A126"]}],"id":[{"id":"10.13039\/501100003042","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Viruses"],"abstract":"<jats:p>Immunoglobulins are only moderately effective for the treatment of human cytomegalovirus (HCMV) infections, possibly due to ineffectiveness against cell-associated virus spread. To overcome this limitation, we aimed to identify individuals with exceptional antibodies in their plasma that can efficiently block the cell-associated spread of HCMV. A Gaussia luciferase-secreting mutant of the cell-associated HCMV strain Merlin was generated, and luciferase activity evaluated as a readout for the extent of cell-associated focal spread. This reporter virus-based assay was then applied to screen plasma samples from 8400 HCMV-seropositive individuals for their inhibitory effect, including direct-acting antiviral drugs as positive controls. None of the plasmas reduced virus spread to the level of these controls. Even the top-scoring samples that partially reduced luciferase activity in the screening assay failed to inhibit focal growth when reevaluated with a more accurate, immunofluorescence-based assay. Selected sera with high neutralizing capacity against free viruses were analyzed separately, and none of them prevented the focal spread of three recent clinical HCMV isolates nor reduced the number of particles transmitted, as demonstrated with a fluorescent Merlin mutant. We concluded that donors with cell-to-cell-spread-inhibiting plasma are nonexistent or extremely rare, emphasizing cell-associated spread as a highly efficient immune escape mechanism of HCMV.<\/jats:p>","DOI":"10.3390\/v10090500","type":"journal-article","created":{"date-parts":[[2018,9,14]],"date-time":"2018-09-14T10:57:59Z","timestamp":1536922679000},"page":"500","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":23,"title":["Large-Scale Screening of HCMV-Seropositive Blood Donors Indicates that HCMV Effectively Escapes from Antibodies by Cell-Associated Spread"],"prefix":"10.3390","volume":"10","author":[{"given":"Jessica Julia","family":"Falk","sequence":"first","affiliation":[{"name":"Institute for Virology, Ulm University Medical Center, 89081 Ulm, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Martina","family":"Winkelmann","sequence":"additional","affiliation":[{"name":"Institute for Transfusion Medicine, Ulm University Medical Center, 89081 Ulm, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kerstin","family":"Laib Sampaio","sequence":"additional","affiliation":[{"name":"Institute for Virology, Ulm University Medical Center, 89081 Ulm, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Caroline","family":"Paal","sequence":"additional","affiliation":[{"name":"Institute for Virology, Ulm University Medical Center, 89081 Ulm, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hubert","family":"Schrezenmeier","sequence":"additional","affiliation":[{"name":"Institute for Transfusion Medicine, Ulm University Medical Center, 89081 Ulm, Germany"},{"name":"Institute for Clinical Transfusion Medicine and Immunogenetics Ulm, German Red Cross Blood Transfusion Service Baden-W\u00fcrttemberg\u2013Hessen and Ulm University Medical Center, 89081 Ulm, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mira","family":"Alt","sequence":"additional","affiliation":[{"name":"Institute for Virology, University Hospital Essen, University of Duisburg-Essen, 45147 Essen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6799-1182","authenticated-orcid":false,"given":"Richard","family":"Stanton","sequence":"additional","affiliation":[{"name":"Division of Infection and Immunity, Cardiff University School of Medicine, Cardiff CF14 4XN, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9502-9903","authenticated-orcid":false,"given":"Adalbert","family":"Krawczyk","sequence":"additional","affiliation":[{"name":"Institute for Virology, University Hospital Essen, University of Duisburg-Essen, 45147 Essen, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8125-0591","authenticated-orcid":false,"given":"Ramin","family":"Lotfi","sequence":"additional","affiliation":[{"name":"Institute for Transfusion Medicine, Ulm University Medical Center, 89081 Ulm, Germany"},{"name":"Institute for Clinical Transfusion Medicine and Immunogenetics Ulm, German Red Cross Blood Transfusion Service Baden-W\u00fcrttemberg\u2013Hessen and Ulm University Medical Center, 89081 Ulm, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9282-1783","authenticated-orcid":false,"given":"Christian","family":"Sinzger","sequence":"additional","affiliation":[{"name":"Institute for Virology, Ulm University Medical Center, 89081 Ulm, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2018,9,14]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"2105","DOI":"10.1016\/S0140-6736(05)66553-1","article-title":"Antiviral medications to prevent cytomegalovirus disease and early death in recipients of solid-organ transplants: A systematic review of randomised controlled trials","volume":"365","author":"Hodson","year":"2005","journal-title":"Lancet"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"466","DOI":"10.1097\/MOH.0000000000000085","article-title":"The role of cytomegalovirus serostatus on outcome of hematopoietic stem cell transplantation","volume":"21","author":"Ljungman","year":"2014","journal-title":"Curr. Opin. Hematol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"6465","DOI":"10.1182\/blood-2009-02-203307","article-title":"Impact of donor CMV status on viral infection and reconstitution of multifunction CMV-specific T cells in CMV-positive transplant recipients","volume":"113","author":"Zhou","year":"2009","journal-title":"Blood"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"333","DOI":"10.1097\/TP.0b013e31829df29d","article-title":"Updated International Consensus Guidelines on the Management of Cytomegalovirus in Solid-Organ Transplantation","volume":"96","author":"Kotton","year":"2013","journal-title":"Transplantation"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"e609","DOI":"10.1542\/peds.2013-2217","article-title":"Incidence and Impact of CMV Infection in Very Low Birth Weight Infants","volume":"133","author":"Turner","year":"2014","journal-title":"Pediatrics"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1128\/CMR.00062-12","article-title":"The \u201csilent\u201d global burden of congenital cytomegalovirus","volume":"26","author":"Manicklal","year":"2013","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"S178","DOI":"10.1093\/cid\/cit629","article-title":"Congenital Cytomegalovirus Infection: Clinical Outcome","volume":"57","author":"Boppana","year":"2013","journal-title":"Clin. Infect. Dis."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1904","DOI":"10.1001\/jama.1986.03380140074025","article-title":"Primary cytomegalovirus infection in pregnancy. Incidence, transmission to fetus, and clinical outcome","volume":"256","author":"Stagno","year":"1986","journal-title":"JAMA"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1159","DOI":"10.1182\/blood.V99.4.1159","article-title":"Infectious Diseases Working Party of the European Group for Blood and Marrow Transplantation Randomized multicenter trial of foscarnet versus ganciclovir for preemptive therapy of cytomegalovirus infection after allogeneic stem cell transplantation","volume":"99","author":"Reusser","year":"2002","journal-title":"Blood"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"388","DOI":"10.1182\/blood.V97.2.388","article-title":"Cidofovir for cytomegalovirus infection and disease in allogeneic stem cell transplant recipients. The Infectious Diseases Working Party of the European Group for Blood and Marrow Transplantation","volume":"97","author":"Ljungman","year":"2001","journal-title":"Blood"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"1009","DOI":"10.4065\/mcp.2011.0309","article-title":"Antiviral drugs for viruses other than human immunodeficiency virus","volume":"86","author":"Razonable","year":"2011","journal-title":"Mayo Clin. Proc."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"153","DOI":"10.1016\/j.csbj.2015.01.003","article-title":"Antiviral Drug- and Multidrug Resistance in Cytomegalovirus Infected SCT Patients","volume":"13","author":"Hamprecht","year":"2015","journal-title":"Comput. Struct. Biotechnol. J."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"2433","DOI":"10.1056\/NEJMoa1706640","article-title":"Letermovir Prophylaxis for Cytomegalovirus in Hematopoietic-Cell Transplantation","volume":"377","author":"Marty","year":"2017","journal-title":"N. Engl. J. Med."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"215","DOI":"10.1093\/infdis\/jir718","article-title":"Immunoglobulin therapy of fetal cytomegalovirus infection occurring in the first half of pregnancy-A case-control study of the outcome in children","volume":"205","author":"Nigro","year":"2012","journal-title":"J. Infect. Dis."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"439","DOI":"10.1515\/jpm-2011-0257","article-title":"Use of cytomegalovirus hyperimmunoglobulin for prevention of congenital cytomegalovirus disease: A retrospective analysis","volume":"40","author":"Buxmann","year":"2012","journal-title":"J. Perinat. Med."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1316","DOI":"10.1056\/NEJMoa1310214","article-title":"A Randomized Trial of Hyperimmune Globulin to Prevent Congenital Cytomegalovirus","volume":"370","author":"Revello","year":"2014","journal-title":"N. Engl. J. Med."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1007\/s00404-017-4380-2","article-title":"Cytomegalovirus infection in pregnancy","volume":"296","author":"Kagan","year":"2017","journal-title":"Arch. Gynecol. Obstet."},{"key":"ref_18","first-page":"273","article-title":"Efficacy of immune globulin in preventing complications of bone marrow transplantation: A meta-analysis","volume":"12","author":"Bass","year":"1993","journal-title":"Bone Marrow Transplant."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1049","DOI":"10.1056\/NEJM198710223171703","article-title":"Use of cytomegalovirus immune globulin to prevent cytomegalovirus in renal-transplant recipients","volume":"317","author":"Snydman","year":"1987","journal-title":"N. Engl. J. Med."},{"key":"ref_20","first-page":"17","article-title":"Meta-analysis of CMVIG studies for the prevention and treatment of CMV infection in transplant patients","volume":"28","author":"Wittes","year":"1996","journal-title":"Transplant. Proc."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"4919","DOI":"10.1128\/AAC.00523-15","article-title":"Phase 1 Randomized, Double-Blind, Placebo-Controlled Study of RG7667, an Anticytomegalovirus Combination Monoclonal Antibody Therapy, in Healthy Adults","volume":"59","author":"Ishida","year":"2015","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Ishida, J.H., Patel, A., Mehta, A.K., Gatault, P., McBride, J.M., Burgess, T., Derby, M.A., Snydman, D.R., Emu, B., and Feierbach, B. (2017). Phase 2 Randomized, Double-Blind, Placebo-Controlled Trial of RG7667, a Combination Monoclonal Antibody, for Prevention of Cytomegalovirus Infection in High-Risk Kidney Transplant Recipients. Antimicrob. Agents Chemother., 61.","DOI":"10.1128\/AAC.01794-16"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"6273","DOI":"10.1073\/pnas.1800224115","article-title":"Protection from cytomegalovirus viremia following glycoprotein B vaccination is not dependent on neutralizing antibodies","volume":"115","author":"Baraniak","year":"2018","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1191","DOI":"10.1056\/NEJMoa0804749","article-title":"Vaccine prevention of maternal cytomegalovirus infection","volume":"360","author":"Pass","year":"2009","journal-title":"N. Engl. J. Med."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1256","DOI":"10.1016\/S0140-6736(11)60136-0","article-title":"Cytomegalovirus glycoprotein-B vaccine with MF59 adjuvant in transplant recipients: A phase 2 randomised placebo-controlled trial","volume":"377","author":"Griffiths","year":"2011","journal-title":"Lancet"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1016\/0264-410X(83)90008-7","article-title":"Supernatant virus release as a differentiating marker between low passage and vaccine strains of human cytomegalovirus","volume":"1","author":"Yamane","year":"1983","journal-title":"Vaccine"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"2867","DOI":"10.1099\/0022-1317-80-11-2867","article-title":"Modification of human cytomegalovirus tropism through propagation in vitro is associated with changes in the viral genome","volume":"80","author":"Sinzger","year":"1999","journal-title":"J. Gen. Virol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"3191","DOI":"10.1172\/JCI42955","article-title":"Reconstruction of the complete human cytomegalovirus genome in a BAC reveals RL13 to be a potent inhibitor of replication","volume":"120","author":"Stanton","year":"2010","journal-title":"J. Clin. Investig."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1535","DOI":"10.1099\/vir.0.018994-0","article-title":"Sequential mutations associated with adaptation of human cytomegalovirus to growth in cell culture","volume":"91","author":"Dargan","year":"2010","journal-title":"J. Gen. Virol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"112","DOI":"10.1016\/j.jcv.2006.11.009","article-title":"Effect of serum and CTL on focal growth of human cytomegalovirus","volume":"38","author":"Sinzger","year":"2007","journal-title":"J. Clin. Virol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1558","DOI":"10.1128\/AAC.04295-14","article-title":"A high-affinity native human antibody neutralizes human cytomegalovirus infection of diverse cell types","volume":"59","author":"Kauvar","year":"2015","journal-title":"Antimicrob. Agents Chemother."},{"key":"ref_32","doi-asserted-by":"crossref","unstructured":"Cui, X., Freed, D.C., Wang, D., Qiu, P., Li, F., Fu, T.-M., Kauvar, L.M., and McVoy, M.A. (2017). Impact of Antibodies and Strain Polymorphisms on Cytomegalovirus Entry and Spread in Fibroblasts and Epithelial Cells. J. Virol., 91.","DOI":"10.1128\/JVI.01650-16"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"2145","DOI":"10.1007\/s00705-011-1105-x","article-title":"UL74 of human cytomegalovirus reduces the inhibitory effect of gH-specific and gB-specific antibodies","volume":"156","author":"Jiang","year":"2011","journal-title":"Arch. Virol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"2802","DOI":"10.1128\/JVI.01550-07","article-title":"UL74 of human cytomegalovirus contributes to virus release by promoting secondary envelopment of virions","volume":"82","author":"Jiang","year":"2008","journal-title":"J. Virol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"853","DOI":"10.1099\/vir.0.83523-0","article-title":"Human cytomegalovirus serum neutralizing antibodies block virus infection of endothelial\/epithelial cells, but not fibroblasts, early during primary infection","volume":"89","author":"Gerna","year":"2008","journal-title":"J. Gen. Virol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"6104","DOI":"10.1073\/pnas.1704809114","article-title":"The pentameric complex drives immunologically covert cell-cell transmission of wild-type human cytomegalovirus","volume":"114","author":"Murrell","year":"2017","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"876","DOI":"10.1093\/infdis\/jiy229","article-title":"Identification of \u201celite\u201d blood donors with broad and potent neutralizing activity against the human cytomegalovirus","volume":"218","author":"Falk","year":"2018","journal-title":"J. Infect. Dis."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"9075","DOI":"10.1016\/j.vaccine.2011.09.056","article-title":"Quantitative analysis of neutralizing antibody response to human cytomegalovirus in natural infection","volume":"29","author":"Wang","year":"2011","journal-title":"Vaccine"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"3598","DOI":"10.1182\/blood.V86.9.3598.bloodjournal8693598","article-title":"A comparison of filtered leukocyte-reduced and cytomegalovirus (CMV) seronegative blood products for the prevention of transfusion-associated CMV infection after marrow transplant","volume":"86","author":"Bowden","year":"1995","journal-title":"Blood"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"52","DOI":"10.1309\/PVFR-DDWE-302T-WFA1","article-title":"Cytomegalovirus infectivity in whole blood following leukocyte reduction by filtration","volume":"116","author":"Lipson","year":"2001","journal-title":"Am. J. Clin. Pathol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1094","DOI":"10.1093\/infdis\/jix069","article-title":"Determination of the Biological Form of Human Cytomegalovirus DNA in the Plasma of Solid-Organ Transplant Recipients","volume":"215","author":"Tong","year":"2017","journal-title":"J. Infect. Dis."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"568","DOI":"10.1093\/infdis\/132.5.568","article-title":"Comparative serial virologic and serologic studies of symptomatic and subclinical congenitally and natally acquired cytomegalovirus infections","volume":"132","author":"Stagno","year":"1975","journal-title":"J. Infect. Dis."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1016\/S1386-6532(03)00074-X","article-title":"Rapid detection and quantification of cell free cytomegalovirus by a high-speed centrifugation-based microculture assay: Comparison to longitudinally analyzed viral DNA load and pp67 late transcript during lactation","volume":"28","author":"Hamprecht","year":"2003","journal-title":"J. Clin. Virol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"7337","DOI":"10.1128\/JVI.00110-09","article-title":"Human immunodeficiency virus type 1 elite neutralizers: Individuals with broad and potent neutralizing activity identified by using a high-throughput neutralization assay together with an analytical selection algorithm","volume":"83","author":"Simek","year":"2009","journal-title":"J. Virol."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1126\/science.1178746","article-title":"Broad and potent neutralizing antibodies from an African donor reveal a new HIV-1 vaccine target","volume":"326","author":"Walker","year":"2009","journal-title":"Science"},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1016\/j.chom.2017.07.013","article-title":"Principles of Broad and Potent Antiviral Human Antibodies: Insights for Vaccine Design","volume":"22","author":"Crowe","year":"2017","journal-title":"Cell Host Microbe"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1038\/nm.4268","article-title":"Antibody 10-1074 suppresses viremia in HIV-1-infected individuals","volume":"23","author":"Caskey","year":"2017","journal-title":"Nat. Med."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"441","DOI":"10.1089\/ten.tea.2009.0184","article-title":"Synthetic gene regulation circuits for control of cell expansion","volume":"16","author":"May","year":"2010","journal-title":"Tissue Eng. Part. A"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"127","DOI":"10.2144\/000114326","article-title":"A permanently growing human endothelial cell line supports productive infection with human cytomegalovirus under conditional cell growth arrest","volume":"59","author":"Lieber","year":"2015","journal-title":"Biotechniques"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"359","DOI":"10.1099\/vir.0.83286-0","article-title":"Cloning and sequencing of a highly productive, endotheliotropic virus strain derived from human cytomegalovirus TB40\/E","volume":"89","author":"Sinzger","year":"2008","journal-title":"J. Gen. Virol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"3929","DOI":"10.1128\/JVI.02858-15","article-title":"Genetic Stability of Bacterial Artificial Chromosome-Derived Human Cytomegalovirus during Culture In Vitro","volume":"90","author":"Murrell","year":"2016","journal-title":"J. Virol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"182","DOI":"10.1016\/j.jviromet.2016.06.008","article-title":"Generation of a Gaussia luciferase-expressing endotheliotropic cytomegalovirus for screening approaches and mutant analyses","volume":"235","author":"Falk","year":"2016","journal-title":"J. Virol. Methods"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"421","DOI":"10.1007\/978-1-60761-652-8_30","article-title":"En passant mutagenesis: A two step markerless red recombination system","volume":"634","author":"Tischer","year":"2010","journal-title":"Methods Mol. Biol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"2699","DOI":"10.1099\/0022-1317-73-10-2699","article-title":"Monoclonal antibody E-13 (M-810) to human cytomegalovirus recognizes an epitope encoded by exon 2 of the major immediate early gene","volume":"73","author":"Mazeron","year":"1992","journal-title":"J. Gen. Virol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"19755","DOI":"10.1073\/pnas.1115861108","article-title":"High-resolution human cytomegalovirus transcriptome","volume":"108","author":"Gatherer","year":"2011","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1016\/j.coviro.2012.11.004","article-title":"Cell-to-cell transmission of viruses","volume":"3","author":"Zhong","year":"2013","journal-title":"Curr. Opin. Virol."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"8360","DOI":"10.1128\/JVI.00443-10","article-title":"Virus cell-to-cell transmission","volume":"84","author":"Mothes","year":"2010","journal-title":"J. Virol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"140","DOI":"10.1016\/j.virol.2013.06.002","article-title":"Neutralizing antibodies are unable to inhibit direct viral cell-to-cell spread of human cytomegalovirus","volume":"444","author":"Jacob","year":"2013","journal-title":"Virology"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"7720","DOI":"10.1128\/JVI.74.17.7720-7729.2000","article-title":"Fast screening procedures for random transposon libraries of cloned herpesvirus genomes: Mutational analysis of human cytomegalovirus envelope glycoprotein genes","volume":"74","author":"Hobom","year":"2000","journal-title":"J. Virol."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"12396","DOI":"10.1073\/pnas.1635160100","article-title":"Functional map of human cytomegalovirus AD169 defined by global mutational analysis","volume":"100","author":"Yu","year":"2003","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"14223","DOI":"10.1073\/pnas.2334032100","article-title":"Functional profiling of a human cytomegalovirus genome","volume":"100","author":"Dunn","year":"2003","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"201","DOI":"10.1007\/978-1-62703-601-6_14","article-title":"Applications for a dual fluorescent human cytomegalovirus in the analysis of viral entry","volume":"1064","author":"Jahn","year":"2013","journal-title":"Methods Mol. Biol."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"e1006273","DOI":"10.1371\/journal.ppat.1006273","article-title":"A derivative of platelet-derived growth factor receptor alpha binds to the trimer of human cytomegalovirus and inhibits entry into fibroblasts and endothelial cells","volume":"13","author":"Stegmann","year":"2017","journal-title":"PLoS Pathog."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"471","DOI":"10.1016\/j.it.2017.05.003","article-title":"Novel Approaches to Analyze Immunoglobulin Repertoires","volume":"38","author":"Wardemann","year":"2017","journal-title":"Trends Immunol."}],"container-title":["Viruses"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1999-4915\/10\/9\/500\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T15:20:34Z","timestamp":1760196034000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1999-4915\/10\/9\/500"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,9,14]]},"references-count":64,"journal-issue":{"issue":"9","published-online":{"date-parts":[[2018,9]]}},"alternative-id":["v10090500"],"URL":"https:\/\/doi.org\/10.3390\/v10090500","relation":{},"ISSN":["1999-4915"],"issn-type":[{"value":"1999-4915","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,9,14]]}}}