{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,4,3]],"date-time":"2026-04-03T16:38:26Z","timestamp":1775234306403,"version":"3.50.1"},"reference-count":39,"publisher":"Public Library of Science (PLoS)","issue":"2","license":[{"start":{"date-parts":[[2019,2,14]],"date-time":"2019-02-14T00:00:00Z","timestamp":1550102400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"CONICET Fundaci\u00f3n CRICYT","award":["BID PICT 2016-0443"],"award-info":[{"award-number":["BID PICT 2016-0443"]}]},{"name":"Agencia-CONICET","award":["PICT2013-0305"],"award-info":[{"award-number":["PICT2013-0305"]}]}],"content-domain":{"domain":["www.plosone.org"],"crossmark-restriction":false},"short-container-title":["PLoS ONE"],"DOI":"10.1371\/journal.pone.0212202","type":"journal-article","created":{"date-parts":[[2019,2,14]],"date-time":"2019-02-14T18:37:59Z","timestamp":1550169479000},"page":"e0212202","update-policy":"https:\/\/doi.org\/10.1371\/journal.pone.corrections_policy","source":"Crossref","is-referenced-by-count":7,"title":["The cAMP effectors, Rap2b and EPAC, are involved in the regulation of the development of the Coxiella burnetii containing vacuole by altering the fusogenic capacity of the vacuole"],"prefix":"10.1371","volume":"14","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-4387-2995","authenticated-orcid":true,"given":"Mar\u00eda Eugenia","family":"Mansilla Pareja","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4717-277X","authenticated-orcid":true,"given":"Maria Celeste","family":"Gaur\u00f3n","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Esteban","family":"Robledo","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Milton Osmar","family":"Aguilera","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5788-9256","authenticated-orcid":true,"given":"Mar\u00eda Isabel","family":"Colombo","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2019,2,14]]},"reference":[{"key":"ref1","doi-asserted-by":"crossref","first-page":"829","DOI":"10.1111\/j.1462-5822.2007.00901.x","article-title":"Lounging in a lysosome: The intracellular lifestyle of Coxiella burnetii","author":"DE Voth","year":"2007","journal-title":"Cellular Microbiology"},{"key":"ref2","doi-asserted-by":"crossref","first-page":"981","DOI":"10.1111\/j.1462-5822.2005.00527.x","article-title":"Autophagy induction favours the generation and maturation of the Coxiella-replicative vacuoles","volume":"7","author":"MG Gutierrez","year":"2005","journal-title":"Cell Microbiol"},{"key":"ref3","doi-asserted-by":"crossref","first-page":"5816","DOI":"10.1128\/IAI.70.10.5816-5821.2002","article-title":"Coxiella burnetii localizes in a Rab7-labeled compartment with autophagic characteristics","volume":"70","author":"W Ber\u00f3n","year":"2002","journal-title":"Infect Immun"},{"key":"ref4","doi-asserted-by":"crossref","first-page":"891","DOI":"10.1111\/j.1462-5822.2006.00838.x","article-title":"The autophagic pathway is actively modulated by phase II Coxiella burnetii to efficiently replicate in the host cell","volume":"9","author":"PS Romano","year":"2007","journal-title":"Cell Microbiol"},{"key":"ref5","doi-asserted-by":"crossref","first-page":"7344","DOI":"10.1128\/JB.186.21.7344-7352.2004","article-title":"Temporal Analysis of Coxiella burnetii Morphological Differentiation","author":"SA Coleman","year":"2004","journal-title":"J Bacteriol"},{"key":"ref6","doi-asserted-by":"crossref","first-page":"3914","DOI":"10.1128\/JB.00071-13","article-title":"Identification of Coxiella burnetii Type IV Secretion Substrates Required for Intracellular Replication and Coxiella-Containing Vacuole Formation","volume":"195","author":"MM Weber","year":"2013","journal-title":"J Bacteriol"},{"key":"ref7","doi-asserted-by":"crossref","first-page":"922","DOI":"10.1111\/cmi.12087","article-title":"Endocytic SNAREs are involved in optimal Coxiella burnetii vacuole development","volume":"15","author":"EM Campoy","year":"2013","journal-title":"Cell Microbiol"},{"key":"ref8","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1128\/IAI.00688-10","article-title":"The early secretory pathway contributes to the growth of the Coxiella-replicative niche","volume":"79","author":"EM Campoy","year":"2011","journal-title":"Infect Immun"},{"key":"ref9","first-page":"1","article-title":"Host Pathways Important for Coxiella burnetii Infection Revealed by Genome-Wide RNA Interference Screening","author":"JA Mcdonough","year":"2013","journal-title":"Host Pathways Important for Coxiella burnetii Infection Revealed by Genome-Wide RNA Interference Screening"},{"key":"ref10","doi-asserted-by":"crossref","first-page":"463","DOI":"10.1016\/S1534-5807(04)00099-1","article-title":"Development by self-digestion: molecular mechanisms and biological functions of autophagy","volume":"6","author":"B Levine","year":"2004","journal-title":"Dev Cell"},{"key":"ref11","doi-asserted-by":"crossref","first-page":"1246","DOI":"10.1111\/j.1600-0854.2010.01086.x","article-title":"Autophagosome formation depends on the small GTPase Rab1 and functional ER exit sites","volume":"11","author":"FCM Zoppino","year":"2010","journal-title":"Traffic"},{"key":"ref12","doi-asserted-by":"crossref","first-page":"197","DOI":"10.2174\/156652411795243441","article-title":"A membrane is born: origin of the autophagosomal compartment","volume":"11","author":"RD Militello","year":"2011","journal-title":"Curr Mol Med"},{"key":"ref13","first-page":"54","article-title":"Autophagic clearance of bacterial pathogens: molecular recognition of intracellular microorganisms","volume":"3","author":"MEM Pareja","year":"2013","journal-title":"Front Cell Infect Microbiol"},{"key":"ref14","first-page":"265","article-title":"The role of Epac proteins, novel cAMP mediators, in the regulation of immune, lung and neuronal function","author":"M Grandoch","year":"2010","journal-title":"Abbreviations"},{"key":"ref15","doi-asserted-by":"crossref","first-page":"3686","DOI":"10.1242\/jcs.03091","article-title":"cAMP synthesis and degradation by phagosomes regulate actin assembly and fusion events: consequences for mycobacteria","volume":"119","author":"SA Kalamidas","year":"2006","journal-title":"J Cell Sci"},{"key":"ref16","doi-asserted-by":"crossref","first-page":"533","DOI":"10.1083\/jcb.201002108","article-title":"Regulation of the autophagy protein LC3 by phosphorylation","volume":"190","author":"SJ Cherra","year":"2010","journal-title":"J Cell Biol"},{"key":"ref17","first-page":"345","article-title":"Epac: effectors and biological functions","author":"SS Roscioni","year":"2008","journal-title":"Epac: effectors and biological functions"},{"key":"ref18","doi-asserted-by":"crossref","first-page":"24825","DOI":"10.1074\/jbc.M109.015362","article-title":"Epac activates the small G proteins Rap1 and Rab3A to achieve exocytosis","volume":"284","author":"MT Branham","year":"2009","journal-title":"J Biol Chem"},{"key":"ref19","doi-asserted-by":"crossref","first-page":"680","DOI":"10.1016\/j.tibs.2006.10.002","article-title":"Epac proteins: multi-purpose cAMP targets","volume":"31","author":"JL Bos","year":"2006","journal-title":"Trends Biochem Sci"},{"key":"ref20","doi-asserted-by":"crossref","first-page":"790","DOI":"10.1016\/j.bbamem.2008.12.010","article-title":"Cell-cell junction formation: the role of Rap1 and Rap1 guanine nucleotide exchange factors","volume":"1788","author":"W-J Pannekoek","year":"2009","journal-title":"Biochim Biophys Acta"},{"key":"ref21","doi-asserted-by":"crossref","first-page":"5145","DOI":"10.1074\/jbc.M111.257634","article-title":"Ras-related GTPases Rap1 and RhoA Collectively Induce the Phagocytosis of Serum-opsonized Zymosan Particles in Macrophages","volume":"287","author":"J-G Kim","year":"2012","journal-title":"J Biol Chem"},{"key":"ref22","doi-asserted-by":"crossref","first-page":"295","DOI":"10.1038\/nchembio.79","article-title":"Novel targets for Huntington\u2019s disease in an mTOR-independent autophagy pathway","volume":"4","author":"A Williams","year":"2008","journal-title":"Nat Chem Biol"},{"key":"ref23","doi-asserted-by":"crossref","first-page":"e1002664","DOI":"10.1371\/journal.ppat.1002664","article-title":"cAMP and EPAC are key players in the regulation of the signal transduction pathway involved in the \u03b1-hemolysin autophagic response","volume":"8","author":"MB Mestre","year":"2012","journal-title":"PLoS Pathog"},{"key":"ref24","doi-asserted-by":"crossref","first-page":"891","DOI":"10.1111\/j.1462-5822.2006.00838.x","article-title":"The autophagic pathway is actively modulated by phase II Coxiella burnetii to efficiently replicate in the host cell","volume":"9","author":"PS Romano","year":"2007","journal-title":"Cell Microbiol"},{"key":"ref25","doi-asserted-by":"crossref","first-page":"112","DOI":"10.3389\/fcimb.2017.00112","article-title":"Alterations of the Coxiella burnetii Replicative Vacuole Membrane Integrity and Interplay with the Autophagy Pathway","volume":"7","author":"ME Mansilla Pareja","year":"2017","journal-title":"Front Cell Infect Microbiol"},{"key":"ref26","first-page":"295","article-title":"UKPMC Funders Group Novel targets for Huntington \u2018 s disease in an mTOR-independent autophagy pathway","volume":"4","author":"A Williams","year":"2009","journal-title":"UKPMC Funders Group Novel targets for Huntington \u2018 s disease in an mTOR-independent autophagy pathway"},{"key":"ref27","doi-asserted-by":"crossref","first-page":"26581","DOI":"10.1074\/jbc.M203571200","article-title":"Cell cycle-dependent subcellular localization of exchange factor directly activated by cAMP","volume":"277","author":"J Qiao","year":"2002","journal-title":"J Biol Chem"},{"key":"ref28","doi-asserted-by":"crossref","first-page":"753","DOI":"10.1016\/j.cell.2004.11.038","article-title":"Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages","volume":"119","author":"MG Gutierrez","year":"2004","journal-title":"Cell"},{"key":"ref29","first-page":"1661","article-title":"Association of Rap1a and Rap1b proteins with late endocytic \/ phagocytic compartments and Rap2a with the Golgi complex","volume":"1670","author":"V Pizon","year":"1994","journal-title":"Association of Rap1a and Rap1b proteins with late endocytic \/ phagocytic compartments and Rap2a with the Golgi complex"},{"key":"ref30","doi-asserted-by":"crossref","first-page":"732","DOI":"10.1016\/j.bbrc.2008.11.107","article-title":"Rap2 function requires palmitoylation and recycling endosome localization","volume":"378","author":"Y Uechi","year":"2009","journal-title":"Biochem Biophys Res Commun"},{"key":"ref31","doi-asserted-by":"crossref","first-page":"e106687","DOI":"10.1371\/journal.pone.0106687","article-title":"Mechanisms of isoform specific Rap2 signaling during enterocytic brush border formation","volume":"9","author":"LJM Bruurs","year":"2014","journal-title":"PLoS One"},{"key":"ref32","doi-asserted-by":"crossref","first-page":"R563","DOI":"10.1016\/j.cub.2005.07.010","article-title":"Signaling interplay in Ras superfamily function","volume":"15","author":"N Mitin","year":"2005","journal-title":"Curr Biol"},{"key":"ref33","doi-asserted-by":"crossref","first-page":"396","DOI":"10.3390\/cells1030396","article-title":"LC3-Associated Phagocytosis (LAP): Connections with Host Autophagy","volume":"1","author":"S-C Lai","year":"2012","journal-title":"Cells"},{"key":"ref34","article-title":"Effector Protein Translocation by the Coxiella burnetii Dot \/ Icm Type IV Secretion System Requires Endocytic Maturation of the Pathogen-Occupied Vacuole","author":"HJ Newton","year":"2013","journal-title":"Effector Protein Translocation by the Coxiella burnetii Dot \/ Icm Type IV Secretion System Requires Endocytic Maturation of the Pathogen-Occupied Vacuole"},{"key":"ref35","first-page":"1","article-title":"Effector Protein Cig2 Decreases Host Tolerance of Infection by Directing Constitutive Fusion of Autophagosomes with the Coxiella\u2014Containing Vacuole","volume":"7","author":"L Kohler","year":"2016","journal-title":"Effector Protein Cig2 Decreases Host Tolerance of Infection by Directing Constitutive Fusion of Autophagosomes with the Coxiella\u2014Containing Vacuole"},{"key":"ref36","doi-asserted-by":"crossref","first-page":"2229","DOI":"10.1128\/IAI.01236-13","article-title":"Coxiella burnetii type IV secretion-dependent recruitment of macrophage autophagosomes","volume":"82","author":"CG Winchell","year":"2014","journal-title":"Infect Immun"},{"key":"ref37","doi-asserted-by":"crossref","first-page":"e1004286","DOI":"10.1371\/journal.ppat.1004286","article-title":"A screen of Coxiella burnetii mutants reveals important roles for Dot\/Icm effectors and host autophagy in vacuole biogenesis","volume":"10","author":"HJ Newton","year":"2014","journal-title":"PLoS Pathog"},{"key":"ref38","first-page":"1","article-title":"Host Pathways Important for Coxiella burnetii Infection Revealed by","author":"JA Mcdonough","year":"2013","journal-title":"Host Pathways Important for Coxiella burnetii Infection Revealed by"},{"key":"ref39","doi-asserted-by":"crossref","first-page":"1901","DOI":"10.1016\/j.bbamcr.2009.09.011","article-title":"TI-VAMP\/VAMP7 and VAMP3\/cellubrevin: two v-SNARE proteins involved in specific steps of the autophagy\/multivesicular body pathways","volume":"1793","author":"CM Fader","year":"2009","journal-title":"Biochim Biophys Acta"}],"container-title":["PLOS ONE"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/dx.plos.org\/10.1371\/journal.pone.0212202","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,5,9]],"date-time":"2020-05-09T02:37:22Z","timestamp":1588991842000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pone.0212202"}},"subtitle":[],"editor":[{"given":"Zhao-Qing","family":"Luo","sequence":"first","affiliation":[],"role":[{"role":"editor","vocabulary":"crossref"}]}],"short-title":[],"issued":{"date-parts":[[2019,2,14]]},"references-count":39,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2019,2,14]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pone.0212202","relation":{},"ISSN":["1932-6203"],"issn-type":[{"value":"1932-6203","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,2,14]]}}}