{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,14]],"date-time":"2026-10-14T01:46:09Z","timestamp":1791942369080,"version":"4.3.4"},"reference-count":71,"publisher":"Oxford University Press (OUP)","license":[{"start":{"date-parts":[[2026,1,2]],"date-time":"2026-01-02T00:00:00Z","timestamp":1767312000000},"content-version":"vor","delay-in-days":1,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001711","name":"Swiss National Science Foundation","doi-asserted-by":"publisher","award":["320030\u2013231940"],"award-info":[{"award-number":["320030\u2013231940"]}],"id":[{"id":"10.13039\/501100001711","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001711","name":"Swiss National Science Foundation","doi-asserted-by":"publisher","award":["17\/22\u2013087"],"award-info":[{"award-number":["17\/22\u2013087"]}],"id":[{"id":"10.13039\/501100001711","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001711","name":"Swiss National Science Foundation","doi-asserted-by":"publisher","award":["22\/27\u2013128"],"award-info":[{"award-number":["22\/27\u2013128"]}],"id":[{"id":"10.13039\/501100001711","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100002910","name":"F\u00e9d\u00e9ration Wallonie-Bruxelles","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100002910","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2026,1,5]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>The establishment of a replicative niche in the hostile environment of the host presents an enormous challenge for pathogens. Intracellular pathogens such as Brucella spp., the Gram-negative causative agents of Brucellosis, must subvert diverse host functions to ensure survival and replication. One of the key adaptations to achieve this is the translocation of effector proteins into host cells via its type 4 secretion system (T4SS). But effector identification in Brucella is particularly challenging, as previously identified effectors lack a conserved translocation signal, exhibit variable requirements for translocation, and in some cases appear to be translocated in a T4SS-independent manner. Here, we demonstrate that a subset of previously described T4SS effector proteins associates with outer membrane vesicles (OMVs) in different Brucella species. Most of these effector proteins encode predicted signal peptides for periplasmic export or transmembrane domains. Among them, BspC and VceA carry functional signal peptides that direct their export into the periplasm in a Sec-dependent manner. From the periplasm, these proteins are subsequently secreted into the extracellular milieu, likely via the formation and release of OMVs. Our findings provide new insights into protein secretion by Brucella, suggesting that OMVs may represent an alternative secretion pathway to the T4SS.<\/jats:p>","DOI":"10.1093\/femsml\/uqaf046","type":"journal-article","created":{"date-parts":[[2025,12,31]],"date-time":"2025-12-31T12:50:19Z","timestamp":1767185419000},"source":"Crossref","is-referenced-by-count":3,"title":["A subset of type 4 secretion system effectors of\n                    <i>Brucella<\/i>\n                    spp. associates to outer membrane vesicles"],"prefix":"10.1093","volume":"7","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-5157-4528","authenticated-orcid":false,"given":"Maren","family":"Ketterer","sequence":"first","affiliation":[{"name":"Biozentrum, University of Basel , 4056 Basel ,","place":["Switzerland"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Naadir","family":"Ganief","sequence":"additional","affiliation":[{"name":"Biozentrum, University of Basel , 4056 Basel ,","place":["Switzerland"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Petra","family":"Chiquet","sequence":"additional","affiliation":[{"name":"Biozentrum, University of Basel , 4056 Basel ,","place":["Switzerland"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ad\u00e9lie","family":"Lannoy","sequence":"additional","affiliation":[{"name":"Universtiy of Namur URBM and Department of Biology, Namur Research Institute for Life Sciences (NARILIS), , 5000 Namur ,","place":["Belgium"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Audrey","family":"Verhaeghe","sequence":"additional","affiliation":[{"name":"Biozentrum, University of Basel , 4056 Basel ,","place":["Switzerland"]},{"name":"Universtiy of Namur URBM and Department of Biology, Namur Research Institute for Life Sciences (NARILIS), , 5000 Namur ,","place":["Belgium"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Joanne","family":"Braunweiler","sequence":"additional","affiliation":[{"name":"Biozentrum, University of Basel , 4056 Basel ,","place":["Switzerland"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marc","family":"Dieu","sequence":"additional","affiliation":[{"name":"MaSUN, Mass Spectrometry Facility, University of Namur , 5000 Namur ,","place":["Belgium"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xavier","family":"De\u00a0Bolle","sequence":"additional","affiliation":[{"name":"Universtiy of Namur URBM and Department of Biology, Namur Research Institute for Life Sciences (NARILIS), , 5000 Namur ,","place":["Belgium"]},{"name":"WEL Research Institute (WELRI) , 1300 Wavre ,","place":["Belgium"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Maxime","family":"Qu\u00e9batte","sequence":"additional","affiliation":[{"name":"Biozentrum, University of Basel , 4056 Basel ,","place":["Switzerland"]}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christoph","family":"Dehio","sequence":"additional","affiliation":[{"name":"Biozentrum, University of Basel , 4056 Basel ,","place":["Switzerland"]}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2026,1,2]]},"reference":[{"key":"2026011210483649000_bib1","doi-asserted-by":"publisher","first-page":"420","DOI":"10.1038\/s41587-019-0036-z","article-title":"SignalP 5.0 improves signal peptide predictions using deep neural networks","volume":"37","author":"Almagro\u00a0Armenteros","year":"2019","journal-title":"Nat Biotechnol"},{"key":"2026011210483649000_bib2","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1128\/IAI.00713-17","article-title":"Brucella abortus senses the intracellular environment through the BvrR\/BvrS two-component system, which allows B. abortus to adapt to its replicative niche","volume":"86","author":"Altamirano-Silva","year":"2018","journal-title":"Infect Immun"},{"key":"2026011210483649000_bib3","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2019.02714","article-title":"Proteomic analysis of membrane blebs of Brucella abortus 2308 and RB51 and their evaluation as an acellular vaccine","volume":"10","author":"Araiza-Villanueva","year":"2019","journal-title":"Front Microbiol"},{"key":"2026011210483649000_bib4","doi-asserted-by":"crossref","first-page":"352493","DOI":"10.1155\/2012\/352493","article-title":"Characterization of outer membrane vesicles from Brucella melitensis and protection induced in mice","volume":"2012","author":"Avila-Calder\u00f3n","year":"2012","journal-title":"Clin Dev Immunol"},{"key":"2026011210483649000_bib5","doi-asserted-by":"crossref","DOI":"10.3389\/fmicb.2020.556795","article-title":"Outer membrane vesicles from Brucella melitensis modulate immune response and induce cytoskeleton rearrangement in peripheral blood mononuclear cells","volume":"11","author":"Avila-Calder\u00f3n","year":"2020","journal-title":"Front Microbiol"},{"key":"2026011210483649000_bib6","doi-asserted-by":"crossref","first-page":"D523","DOI":"10.1093\/nar\/gkac1052","article-title":"UniProt: the Universal Protein Knowledgebase in 2023","volume":"51","author":"The UniProt Consortium","year":"2023","journal-title":"Nucleic Acids Res"},{"key":"2026011210483649000_bib7","doi-asserted-by":"publisher","first-page":"3702","DOI":"10.1128\/IAI.73.6.3702-3713.2005","article-title":"Opsonized virulent Brucella abortus replicates within nonacidic, endoplasmic reticulum-negative, LAMP-1-positive phagosomes in human monocytes","volume":"73","author":"Bellaire","year":"2005","journal-title":"Infect Immun"},{"key":"2026011210483649000_bib8","doi-asserted-by":"publisher","first-page":"607610","DOI":"10.3389\/fcimb.2021.607610","article-title":"Adhesive functions or pseudogenization of type va autotransporters in Brucella species","volume":"11","author":"Bialer","year":"2021","journal-title":"Front Cell Infect Microbiol"},{"key":"2026011210483649000_bib9","doi-asserted-by":"publisher","first-page":"5693","DOI":"10.1128\/IAI.72.10.5693-5703.2004","article-title":"Release of periplasmic proteins of Brucella suis upon acidic shock involves the outer membrane protein Omp25","volume":"72","author":"Boigegrain","year":"2004","journal-title":"Infect Immun"},{"key":"2026011210483649000_bib10","doi-asserted-by":"publisher","first-page":"1544","DOI":"10.1073\/pnas.032514299","article-title":"The Brucella suis virB operon is induced intracellularly in macrophages","volume":"99","author":"Boschiroli","year":"2002","journal-title":"Proc Natl Acad Sci USA"},{"key":"2026011210483649000_bib11","doi-asserted-by":"publisher","first-page":"545","DOI":"10.1084\/jem.20030088","article-title":"Brucella evades macrophage killing via VirB-dependent sustained interactions with the endoplasmic reticulum","volume":"198","author":"Celli","year":"2003","journal-title":"J Exp Med"},{"key":"2026011210483649000_bib12","doi-asserted-by":"publisher","first-page":"159","DOI":"10.1046\/j.1462-5822.2001.00102.x","article-title":"Essential role of the VirB machinery in the maturation of the Brucella abortus-containing vacuole","volume":"3","author":"Comerci","year":"2001","journal-title":"Cell Microbiol"},{"key":"2026011210483649000_bib13","first-page":"ji1700725","article-title":"Brucella abortus triggers a cGAS-independent STING pathway to induce host protection that involves guanylate-binding proteins and inflammasome activation","volume":"200","author":"Costa\u00a0Franco","year":"2018","journal-title":"J Immunol"},{"key":"2026011210483649000_bib14","doi-asserted-by":"publisher","first-page":"1044","DOI":"10.1111\/j.1462-5822.2011.01601.x","article-title":"Identification of a Brucella spp. secreted effector specifically interacting with human small GTPase Rab2","volume":"13","author":"De\u00a0Barsy","year":"2011","journal-title":"Cell Microbiol"},{"key":"2026011210483649000_bib15","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/ncomms5366","article-title":"G1-arrested newborn cells are the predominant infectious form of the pathogen Brucella abortus","volume":"5","author":"Deghelt","year":"2014","journal-title":"Nat Commun"},{"key":"2026011210483649000_bib16","doi-asserted-by":"publisher","first-page":"1378","DOI":"10.1111\/j.1365-2958.2008.06487.x","article-title":"Identification of VceA and VceC, two members of the VjbR regulon that are translocated into macrophages by the Brucella type IV secretion system","volume":"70","author":"De\u00a0Jong","year":"2008","journal-title":"Mol Microbiol"},{"key":"2026011210483649000_bib17","doi-asserted-by":"publisher","first-page":"238","DOI":"10.1186\/s13059-019-1832-y","article-title":"OrthoFinder: phylogenetic orthology inference for comparative genomics","volume":"20","author":"Emms","year":"2019","journal-title":"Genome Biol"},{"key":"2026011210483649000_bib18","doi-asserted-by":"publisher","first-page":"3285","DOI":"10.1128\/IAI.01382-05","article-title":"Membrane vesicles shed by Legionella pneumophila inhibit fusion of phagosomes with lysosomes","volume":"74","author":"Fernandez-Moreira","year":"2006","journal-title":"Infect Immun"},{"key":"2026011210483649000_bib19","doi-asserted-by":"publisher","first-page":"220","DOI":"10.1002\/(SICI)1096-9896(199906)188:2%3c220::AID-PATH307%3e3.0.CO;2-C","article-title":"Release of Helicobacter pylori vacuolating cytotoxin by both a specific secretion pathway and budding of outer membrane vesicles","volume":"188","author":"Fiocca","year":"1999","journal-title":"J Pathol"},{"key":"2026011210483649000_bib20","doi-asserted-by":"publisher","DOI":"10.3389\/fmicb.2022.913434","article-title":"Bartonella taylorii: a model organism for studying Bartonella infection in vitro and in vivo","volume":"13","author":"Fromm","year":"2022","journal-title":"Front Microbiol"},{"key":"2026011210483649000_bib21","doi-asserted-by":"publisher","first-page":"e2310348121","DOI":"10.1073\/pnas.2310348121","article-title":"Translocation of YopJ family effector proteins through the VirB\/VirD4 T4SS of Bartonella","volume":"121","author":"Fromm","year":"2024","journal-title":"Proc Natl Acad Sci USA"},{"key":"2026011210483649000_bib22","doi-asserted-by":"publisher","first-page":"463","DOI":"10.1083\/jcb.95.2.463","article-title":"Protein translocation across the endoplasmic reticulum. I. Detection in the microsomal membrane of a receptor for the signal recognition particle","volume":"95","author":"Gilmore","year":"1982","journal-title":"J Cell Biol"},{"key":"2026011210483649000_bib23","doi-asserted-by":"crossref","first-page":"e00726","DOI":"10.1128\/mbio.00726-24","article-title":"Brucella NpeA is a secreted type IV effector containing an N-WASP-binding short linear motif that promotes niche formation","volume":"15","author":"Gim\u00e9nez","year":"2024","journal-title":"mBio"},{"key":"2026011210483649000_bib24","doi-asserted-by":"publisher","first-page":"27","DOI":"10.1038\/s41564-020-00799-3","article-title":"\u03b2-barrels covalently link peptidoglycan and the outer membrane in the \u03b1-proteobacterium Brucella abortus","volume":"6","author":"Godessart","year":"2021","journal-title":"Nat Microbiol"},{"key":"2026011210483649000_bib25","doi-asserted-by":"publisher","first-page":"2034","DOI":"10.1111\/cmi.12172","article-title":"Salmonella enterica delivers its genotoxin through outer membrane vesicles secreted from infected cells","volume":"15","author":"Guidi","year":"2013","journal-title":"Cell Microbiol"},{"key":"2026011210483649000_bib26","doi-asserted-by":"crossref","DOI":"10.1101\/2022.04.08.487609","article-title":"DeepTMHMM predicts alpha and beta transmembrane proteins using deep neural networks","author":"Hallgren","year":"2022"},{"key":"2026011210483649000_bib27","doi-asserted-by":"publisher","first-page":"637","DOI":"10.1111\/mmi.14178","article-title":"Periplasmic protein EipA determines envelope stress resistance and virulence in Brucella abortus","volume":"111","author":"Herrou","year":"2019","journal-title":"Mol Microbiol"},{"key":"2026011210483649000_bib28","doi-asserted-by":"publisher","first-page":"e00134","DOI":"10.1128\/JB.00134-19","article-title":"Brucella periplasmic protein EipB is a molecular determinant of cell envelope integrity and virulence","volume":"201","author":"Herrou","year":"2019","journal-title":"J Bacteriol"},{"key":"2026011210483649000_bib29","doi-asserted-by":"publisher","first-page":"163","DOI":"10.1016\/j.chom.2021.12.001","article-title":"Virulence factors perforate the pathogen-containing vacuole to signal efferocytosis","volume":"30","author":"Hiyoshi","year":"2022","journal-title":"Cell Host Microbe"},{"key":"2026011210483649000_bib30","doi-asserted-by":"publisher","first-page":"227","DOI":"10.1111\/j.1462-5822.2010.01531.x","article-title":"The E block motif is associated with Legionella pneumophila translocated substrates","volume":"13","author":"Huang","year":"2011","journal-title":"Cell Microbiol"},{"key":"2026011210483649000_bib31","doi-asserted-by":"publisher","first-page":"e1005592","DOI":"10.1371\/journal.ppat.1005592","article-title":"Legionella pneumophila-derived outer membrane vesicles promote bacterial replication in macrophages","volume":"12","author":"Jung","year":"2016","journal-title":"PLoS Pathog"},{"key":"2026011210483649000_bib32","doi-asserted-by":"publisher","first-page":"1027","DOI":"10.1016\/j.jmb.2004.03.016","article-title":"A combined transmembrane topology and signal peptide prediction method","volume":"338","author":"K\u00e4ll","year":"2004","journal-title":"J Mol Biol"},{"key":"2026011210483649000_bib33","doi-asserted-by":"publisher","first-page":"e00232","DOI":"10.1128\/msphere.00232-24","article-title":"The putative type 4 secretion system effector BspD is involved in maintaining envelope integrity of the pathogen Brucella","volume":"9","author":"Ketterer","year":"2024","journal-title":"mSphere"},{"key":"2026011210483649000_bib34","doi-asserted-by":"publisher","first-page":"449","DOI":"10.1016\/0022-2836(91)90724-K","article-title":"Reaction mechanism of alkaline phosphatase based on crystal structures: two-metal ion catalysis","volume":"218","author":"Kim","year":"1991","journal-title":"J Mol Biol"},{"key":"2026011210483649000_bib35","doi-asserted-by":"publisher","first-page":"863","DOI":"10.1038\/308863a0","article-title":"Signal sequence mutations disrupt feedback between secretion of an exported protein and its synthesis in E. coli","volume":"308","author":"Kumamoto","year":"1984","journal-title":"Nature"},{"key":"2026011210483649000_bib36","doi-asserted-by":"publisher","DOI":"10.1038\/s44318-025-00511-3","article-title":"A chimeric Mla-Pqi lipid transport system is required for Brucella abortus survival in macrophages","volume":"44","author":"Lannoy","year":"2025","journal-title":"EMBO J"},{"key":"2026011210483649000_bib37","doi-asserted-by":"publisher","first-page":"543","DOI":"10.1046\/j.1365-2958.2000.02150.x","article-title":"Identification and characterization of in vivo attenuated mutants of Brucella melitensis","volume":"38","author":"Lestrate","year":"2000","journal-title":"Mol Microbiol"},{"key":"2026011210483649000_bib38","doi-asserted-by":"publisher","first-page":"105536","DOI":"10.1016\/j.micpath.2022.105536","article-title":"BtpB inhibits innate inflammatory responses in goat alveolar macrophages through the TLR\/NF-\u03bab pathway and NLRP3 inflammasome during Brucella infection","volume":"166","author":"Li","year":"2022","journal-title":"Microb Pathog"},{"key":"2026011210483649000_bib39","doi-asserted-by":"publisher","first-page":"9596","DOI":"10.18632\/oncotarget.24073","article-title":"Overexpression of Cu-Zn SOD in Brucella abortus suppresses bacterial intracellular replication via down-regulation of Sar1 activity","volume":"9","author":"Liu","year":"2018","journal-title":"Oncotarget"},{"key":"2026011210483649000_bib40","doi-asserted-by":"publisher","first-page":"265","DOI":"10.1016\/S0021-9258(19)52451-6","article-title":"Protein measurement with the Folin phenol reagent","volume":"193","author":"Lowry","year":"1951","journal-title":"J Biol Chem"},{"key":"2026011210483649000_bib41","doi-asserted-by":"publisher","first-page":"e2105324118","DOI":"10.1073\/pnas.2105324118","article-title":"The Brucella effector BspL targets the ER-associated degradation (ERAD) pathway and delays bacterial egress from infected cells","volume":"118","author":"Luizet","year":"2021","journal-title":"Proc Natl Acad Sci USA"},{"key":"2026011210483649000_bib42","doi-asserted-by":"publisher","first-page":"1261","DOI":"10.1111\/j.1462-5822.2011.01618.x","article-title":"In search of Brucella abortus type IV secretion substrates: screening and identification of four proteins translocated into host cells through VirB system","volume":"13","author":"Marchesini","year":"2011","journal-title":"Cell Microbiol"},{"key":"2026011210483649000_bib43","doi-asserted-by":"publisher","DOI":"10.3389\/fcimb.2016.00153","article-title":"A T4SS effector targets host cell alpha-enolase contributing to Brucella abortus intracellular lifestyle","volume":"6","author":"Marchesini","year":"2016","journal-title":"Front Cell Infect Microbiol"},{"key":"2026011210483649000_bib44","doi-asserted-by":"publisher","first-page":"2534","DOI":"10.1074\/mcp.TIR118.000900","article-title":"Online parallel accumulation\u2013serial fragmentation (PASEF) with a novel trapped ion mobility mass spectrometer","volume":"17","author":"Meier","year":"2018","journal-title":"Mol Cell Proteomics"},{"key":"2026011210483649000_bib45","doi-asserted-by":"publisher","first-page":"e1003556","DOI":"10.1371\/journal.ppat.1003556","article-title":"Brucella modulates secretory trafficking via multiple type IV secretion effector proteins","volume":"9","author":"Myeni","year":"2013","journal-title":"PLoS Pathog"},{"key":"2026011210483649000_bib46","doi-asserted-by":"publisher","first-page":"1210","DOI":"10.1046\/j.1365-2958.1999.01569.x","article-title":"A homologue of the Agrobacterium tumefaciens VirB and Bordetella pertussis Ptl type IV secretion systems is essential for intracellular survival of Brucella suis","volume":"33","author":"O\u2019Callaghan","year":"1999","journal-title":"Mol Microbiol"},{"key":"2026011210483649000_bib47","doi-asserted-by":"publisher","first-page":"813","DOI":"10.3390\/microorganisms10040813","article-title":"The retrospective on atypical Brucella species leads to novel definitions","volume":"10","author":"Occhialini","year":"2022","journal-title":"Microorganisms"},{"key":"2026011210483649000_bib48","doi-asserted-by":"publisher","first-page":"e2321910121","DOI":"10.1073\/pnas.2321910121","article-title":"Dual membrane-spanning anti-sigma factors regulate vesiculation in Bacteroides thetaiotaomicron","volume":"121","author":"Pardue","year":"2024","journal-title":"Proc Natl Acad Sci USA"},{"key":"2026011210483649000_bib49","doi-asserted-by":"publisher","first-page":"D543","DOI":"10.1093\/nar\/gkae1011","article-title":"The PRIDE database at 20 years: 2025 update","volume":"53","author":"Perez-Riverol","year":"2025","journal-title":"Nucleic Acids Res"},{"key":"2026011210483649000_bib50","doi-asserted-by":"publisher","first-page":"5711","DOI":"10.1128\/IAI.66.12.5711-5724.1998","article-title":"Brucella abortus transits through the autophagic pathway and replicates in the endoplasmic reticulum of nonprofessional phagocytes","volume":"66","author":"Pizarro-Cerd\u00e1","year":"1998","journal-title":"Infect Immun"},{"key":"2026011210483649000_bib51","doi-asserted-by":"publisher","first-page":"2387","DOI":"10.1128\/IAI.66.5.2387-2392.1998","article-title":"Virulent Brucella abortus prevents lysosome fusion and is distributed within autophagosome-like compartments","volume":"66","author":"Pizarro-Cerd\u00e1","year":"1998","journal-title":"Infect Immun"},{"key":"2026011210483649000_bib52","doi-asserted-by":"publisher","first-page":"e50214","DOI":"10.1371\/journal.pone.0050214","article-title":"Outer membrane vesicles from Brucella abortus promote bacterial internalization by human monocytes and modulate their innate immune response","volume":"7","author":"Pollak","year":"2012","journal-title":"PLoS One"},{"key":"2026011210483649000_bib53","doi-asserted-by":"publisher","first-page":"4041","DOI":"10.1128\/IAI.67.8.4041-4047.1999","article-title":"Early acidification of phagosomes containing Brucella suis is essential for intracellular survival in murine macrophages","volume":"67","author":"Porte","year":"1999","journal-title":"Infect Immun"},{"key":"2026011210483649000_bib54","doi-asserted-by":"publisher","first-page":"1053","DOI":"10.1046\/j.1365-2958.2002.03208.x","article-title":"The VirB\/VirD4 type IV secretion system of Bartonella is essential for establishing intraerythrocytic infection","volume":"46","author":"Schulein","year":"2002","journal-title":"Mol Microbiol"},{"key":"2026011210483649000_bib55","doi-asserted-by":"publisher","first-page":"856","DOI":"10.1073\/pnas.0406796102","article-title":"A bipartite signal mediates the transfer of type IV secretion substrates of Bartonella henselae into human cells","volume":"102","author":"Schulein","year":"2005","journal-title":"Proc Natl Acad Sci USA"},{"key":"2026011210483649000_bib56","doi-asserted-by":"publisher","first-page":"jcs210799","DOI":"10.1242\/jcs.210799","article-title":"3D correlative electron microscopy reveals continuity of Brucella containing vacuoles with the endoplasmic reticulum","volume":"131","author":"Sedzicki","year":"2018","journal-title":"J Cell Sci"},{"key":"2026011210483649000_bib57","doi-asserted-by":"publisher","first-page":"e03350","DOI":"10.1128\/mBio.03350-19","article-title":"Epistatic interplay between type IV secretion effectors engages the small GTPase Rab2 in the Brucella intracellular cycle","volume":"11","author":"Smith","year":"2020","journal-title":"mBio"},{"key":"2026011210483649000_bib58","doi-asserted-by":"publisher","first-page":"1611","DOI":"10.1007\/s00203-020-02170-w","article-title":"Comparative proteomic analysis of outer membrane vesicles from Brucella suis, Brucella ovis, Brucella canis and Brucella neotomae","volume":"203","author":"Socorro\u00a0Ruiz-Palma","year":"2021","journal-title":"Arch Microbiol"},{"key":"2026011210483649000_bib59","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1016\/j.str.2016.10.010","article-title":"The BID domain of type IV Secretion Substrates forms a conserved four-helix bundle topped with a hook","volume":"25","author":"Stanger","year":"2017","journal-title":"Structure"},{"key":"2026011210483649000_bib60","doi-asserted-by":"publisher","first-page":"678","DOI":"10.1111\/j.1600-0854.2008.00718.x","article-title":"Brucella intracellular replication requires trafficking through the late endosomal\/lysosomal compartment","volume":"9","author":"Starr","year":"2008","journal-title":"Traffic"},{"key":"2026011210483649000_bib61","doi-asserted-by":"publisher","first-page":"222","DOI":"10.1186\/1471-2180-13-222","article-title":"Sec-mediated secretion by Coxiella burnetii","volume":"13","author":"Stead","year":"2013","journal-title":"BMC Microbiol"},{"key":"2026011210483649000_bib62","doi-asserted-by":"publisher","first-page":"e00312","DOI":"10.1128\/IAI.00312-18","article-title":"Transposon sequencing of Brucella abortus uncovers essential genes for growth in vitro and inside macrophages","volume":"86","author":"Sternon","year":"2018","journal-title":"Infect Immun"},{"key":"2026011210483649000_bib63","doi-asserted-by":"publisher","first-page":"e13375","DOI":"10.1111\/cmi.13375","article-title":"Galectin-3 regulates proinflammatory cytokine function and favours Brucella abortus chronic replication in macrophages and mice","volume":"23","author":"Tana","year":"2021","journal-title":"Cell Microbiol"},{"key":"2026011210483649000_bib64","doi-asserted-by":"publisher","first-page":"195","DOI":"10.1007\/BF01868635","article-title":"The signal peptide","volume":"115","author":"von\u00a0Heijne","year":"1990","journal-title":"J Membr Biol"},{"key":"2026011210483649000_bib65","doi-asserted-by":"publisher","first-page":"921","DOI":"10.3389\/fmicb.2019.00921","article-title":"Versatility of the BID domain: conserved function as type IV secretion signal and secondarily evolved effector functions within Bartonella-infected host cells","volume":"10","author":"Wagner","year":"2019","journal-title":"Front Microbiol"},{"key":"2026011210483649000_bib66","doi-asserted-by":"crossref","first-page":"545","DOI":"10.1083\/jcb.91.2.545","article-title":"Translocation of proteins across the endoplasmic reticulum. I. Signal recognition protein (SRP) binds to in-vitro-assembled polysomes synthesizing secretory protein","volume":"91","author":"Walter","year":"1981","journal-title":"J Cell Biol"},{"key":"2026011210483649000_bib67","doi-asserted-by":"publisher","first-page":"1240","DOI":"10.1111\/mmi.14490","article-title":"A NanoLuc luciferase-based assay enabling the real-time analysis of protein secretion and injection by bacterial type III secretion systems","volume":"113","author":"Westerhausen","year":"2020","journal-title":"Mol Microbiol"},{"key":"2026011210483649000_bib68","doi-asserted-by":"publisher","first-page":"359","DOI":"10.1038\/nmeth.1322","article-title":"Universal sample preparation method for proteome analysis","volume":"6","author":"Wi\u015bniewski","year":"2009","journal-title":"Nat Methods"},{"key":"2026011210483649000_bib69","doi-asserted-by":"publisher","first-page":"2182","DOI":"10.1128\/IAI.01277-10","article-title":"Discovery of Salmonella virulence factors translocated via outer membrane vesicles to murine macrophages","volume":"79","author":"Yoon","year":"2011","journal-title":"Infect Immun"},{"key":"2026011210483649000_bib70","doi-asserted-by":"publisher","first-page":"3329","DOI":"10.1038\/s41467-025-58728-z","article-title":"MSFragger-DDA+ enhances peptide identification sensitivity with full isolation window search","volume":"16","author":"Yu","year":"2025","journal-title":"Nat Commun"},{"key":"2026011210483649000_bib71","doi-asserted-by":"publisher","first-page":"100077","DOI":"10.1016\/j.mcpro.2021.100077","article-title":"IonQuant enables accurate and sensitive label-free quantification with FDR-controlled match-between-runs","volume":"20","author":"Yu","year":"2021","journal-title":"Mol Cell Proteomics"}],"container-title":["microLife"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/microlife\/advance-article-pdf\/doi\/10.1093\/femsml\/uqaf046\/66209487\/uqaf046.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/microlife\/article-pdf\/doi\/10.1093\/femsml\/uqaf046\/66209487\/uqaf046.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/microlife\/article-pdf\/doi\/10.1093\/femsml\/uqaf046\/66209487\/uqaf046.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,1,12]],"date-time":"2026-01-12T15:48:44Z","timestamp":1768232924000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/microlife\/article\/doi\/10.1093\/femsml\/uqaf046\/8408465"}},"subtitle":[],"editor":[{"given":"Carmen","family":"Buchrieser","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2026]]},"references-count":71,"URL":"https:\/\/doi.org\/10.1093\/femsml\/uqaf046","relation":{},"ISSN":["2633-6693"],"issn-type":[{"value":"2633-6693","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2026]]},"published":{"date-parts":[[2026]]},"article-number":"uqaf046"}}