{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,23]],"date-time":"2026-10-23T06:12:21Z","timestamp":1792735941575,"version":"4.5.0"},"reference-count":53,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2015,7,29]],"date-time":"2015-07-29T00:00:00Z","timestamp":1438128000000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2015,7,29]],"date-time":"2015-07-29T00:00:00Z","timestamp":1438128000000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Nat Commun"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>The intracellular pathogen, <jats:italic>Legionella pneumophila<\/jats:italic>, secretes \u223c300 effector proteins to modulate the host environment. Given the intimate interaction between <jats:italic>L. pneumophila<\/jats:italic> and the endoplasmic reticulum, we investigated the role of the host unfolded protein response (UPR) during <jats:italic>L. pneumophila<\/jats:italic> infection. Interestingly, we show that the host identifies <jats:italic>L. pneumophila<\/jats:italic> infection as a form of endoplasmic reticulum stress and the sensor pATF6 is processed to generate pATF6(N), a transcriptional activator of downstream UPR genes. However, <jats:italic>L. pneumophila<\/jats:italic> is able to suppress the UPR and block the translation of prototypical UPR genes, BiP and CHOP. Furthermore, biochemical studies reveal that <jats:italic>L. pneumophila<\/jats:italic> uses two effectors (Lgt1 and Lgt2) to inhibit the splicing of XBP1u mRNA to spliced XBP1 (XBP1s), an UPR response regulator. Thus, we demonstrate that <jats:italic>L. pneumophila<\/jats:italic> is able to inhibit the UPR by multiple mechanisms including blocking XBP1u splicing and causing translational repression. This observation highlights the utility of <jats:italic>L. pneumophila<\/jats:italic> as a powerful tool for studying a critical protein homeostasis regulator.<\/jats:p>","DOI":"10.1038\/ncomms8887","type":"journal-article","created":{"date-parts":[[2015,7,29]],"date-time":"2015-07-29T09:25:59Z","timestamp":1438161959000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":66,"title":["Legionella suppresses the host unfolded protein response via multiple mechanisms"],"prefix":"10.1038","volume":"6","author":[{"given":"Sean","family":"Treacy-Abarca","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shaeri","family":"Mukherjee","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2015,7,29]]},"reference":[{"key":"BFncomms8887_CR1","doi-asserted-by":"publisher","first-page":"1669","DOI":"10.1073\/pnas.95.4.1669","volume":"95","author":"G Segal","year":"1998","unstructured":"Segal, G., Purcell, M. & Shuman, H. A. Host cell killing and bacterial conjugation require overlapping sets of genes within a 22-kb region of the Legionella pneumophila genome. Proc. Natl Acad. Sci. USA 95, 1669\u20131674 (1998) .","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"BFncomms8887_CR2","doi-asserted-by":"publisher","first-page":"873","DOI":"10.1126\/science.279.5352.873","volume":"279","author":"JP Vogel","year":"1998","unstructured":"Vogel, J. P., Andrews, H. L., Wong, S. K. & Isberg, R. R. Conjugative transfer by the virulence system of Legionella pneumophila. Science 279, 873\u2013876 (1998) .","journal-title":"Science"},{"key":"BFncomms8887_CR3","doi-asserted-by":"publisher","first-page":"743","DOI":"10.1093\/jb\/mvp166","volume":"146","author":"K Mori","year":"2009","unstructured":"Mori, K. Signalling pathways in the unfolded protein response: development from yeast to mammals. J. Biochem. 146, 743\u2013750 (2009) .","journal-title":"J. Biochem."},{"key":"BFncomms8887_CR4","doi-asserted-by":"publisher","first-page":"1081","DOI":"10.1126\/science.1209038","volume":"334","author":"P Walter","year":"2011","unstructured":"Walter, P. & Ron, D. The unfolded protein response: from stress pathway to homeostatic regulation. Science 334, 1081\u20131086 (2011) .","journal-title":"Science"},{"key":"BFncomms8887_CR5","doi-asserted-by":"publisher","first-page":"271","DOI":"10.1038\/16729","volume":"397","author":"HP Harding","year":"1999","unstructured":"Harding, H. P., Zhang, Y. & Ron, D. Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397, 271\u2013274 (1999) .","journal-title":"Nature"},{"key":"BFncomms8887_CR6","doi-asserted-by":"publisher","first-page":"944","DOI":"10.1126\/science.1146361","volume":"318","author":"JH Lin","year":"2007","unstructured":"Lin, J. H. et al. IRE1 signaling affects cell fate during the unfolded protein response. Science 318, 944\u2013949 (2007) .","journal-title":"Science"},{"key":"BFncomms8887_CR7","first-page":"289","volume":"71","author":"LM Hendershot","year":"2004","unstructured":"Hendershot, L. M. The ER chaperone BiP is a master regulator of ER function. Mt. Sinai J. Med. 71, 289\u2013297 (2004) .","journal-title":"Mt. Sinai J. Med."},{"key":"BFncomms8887_CR8","doi-asserted-by":"publisher","first-page":"4196","DOI":"10.1128\/MCB.9.10.4196","volume":"9","author":"AJ Fornace Jr","year":"1989","unstructured":"Fornace, A. J. Jr et al. Mammalian genes coordinately regulated by growth arrest signals and DNA-damaging agents. Mol. Cell. Biol. 9, 4196\u20134203 (1989) .","journal-title":"Mol. Cell. Biol."},{"key":"BFncomms8887_CR9","doi-asserted-by":"crossref","first-page":"20465","DOI":"10.1016\/S0021-9258(19)88725-2","volume":"267","author":"JD Bartlett","year":"1992","unstructured":"Bartlett, J. D., Luethy, J. D., Carlson, S. G., Sollott, S. J. & Holbrook, N. J. Calcium ionophore A23187 induces expression of the growth arrest and DNA damage inducible CCAAT\/enhancer-binding protein (C\/EBP)-related gene, gadd153. Ca2+ increases transcriptional activity and mRNA stability. J. Biol. Chem. 267, 20465\u201320470 (1992) .","journal-title":"J. Biol. Chem."},{"key":"BFncomms8887_CR10","doi-asserted-by":"publisher","first-page":"4736","DOI":"10.1128\/MCB.13.8.4736","volume":"13","author":"SG Carlson","year":"1993","unstructured":"Carlson, S. G., Fawcett, T. W., Bartlett, J. D., Bernier, M. & Holbrook, N. J. Regulation of the C\/EBP-related gene gadd153 by glucose deprivation. Mol. Cell. Biol. 13, 4736\u20134744 (1993) .","journal-title":"Mol. Cell. Biol."},{"key":"BFncomms8887_CR11","doi-asserted-by":"publisher","first-page":"6890","DOI":"10.1128\/JVI.79.11.6890-6899.2005","volume":"79","author":"JA Isler","year":"2005","unstructured":"Isler, J. A., Skalet, A. H. & Alwine, J. C. Human cytomegalovirus infection activates and regulates the unfolded protein response. J. Virol. 79, 6890\u20136899 (2005) .","journal-title":"J. Virol."},{"key":"BFncomms8887_CR12","doi-asserted-by":"publisher","first-page":"e1003544","DOI":"10.1371\/journal.ppat.1003544","volume":"9","author":"S Stahl","year":"2013","unstructured":"Stahl, S. et al. Cytomegalovirus downregulates IRE1 to repress the unfolded protein response. PLoS Pathog. 9, e1003544 (2013) .","journal-title":"PLoS Pathog."},{"key":"BFncomms8887_CR13","doi-asserted-by":"publisher","first-page":"e00418","DOI":"10.1128\/mBio.00418-12","volume":"4","author":"MF de Jong","year":"2013","unstructured":"de Jong, M. F. et al. Sensing of bacterial type IV secretion via the unfolded protein response. mBio 4, e00418 (2013) .","journal-title":"mBio"},{"key":"BFncomms8887_CR14","doi-asserted-by":"publisher","first-page":"e1003556","DOI":"10.1371\/journal.ppat.1003556","volume":"9","author":"S Myeni","year":"2013","unstructured":"Myeni, S. et al. Brucella modulates secretory trafficking via multiple type IV secretion effector proteins. PLoS Pathog. 9, e1003556 (2013) .","journal-title":"PLoS Pathog."},{"key":"BFncomms8887_CR15","doi-asserted-by":"publisher","first-page":"e1003785","DOI":"10.1371\/journal.ppat.1003785","volume":"9","author":"JA Smith","year":"2013","unstructured":"Smith, J. A. et al. Brucella induces an unfolded protein response via TcpB that supports intracellular replication in macrophages. PLoS Pathog. 9, e1003785 (2013) .","journal-title":"PLoS Pathog."},{"key":"BFncomms8887_CR16","doi-asserted-by":"publisher","first-page":"921","DOI":"10.1111\/j.1462-5822.2007.01094.x","volume":"10","author":"N Morinaga","year":"2008","unstructured":"Morinaga, N., Yahiro, K., Matsuura, G., Moss, J. & Noda, M. Subtilase cytotoxin, produced by Shiga-toxigenic Escherichia coli, transiently inhibits protein synthesis of Vero cells via degradation of BiP and induces cell cycle arrest at G1 by downregulation of cyclin D1. Cell. Microbiol. 10, 921\u2013929 (2008) .","journal-title":"Cell. Microbiol."},{"key":"BFncomms8887_CR17","doi-asserted-by":"publisher","first-page":"770","DOI":"10.1111\/j.1462-5822.2007.01083.x","volume":"10","author":"SY Lee","year":"2008","unstructured":"Lee, S. Y., Lee, M. S., Cherla, R. P. & Tesh, V. L. Shiga toxin 1 induces apoptosis through the endoplasmic reticulum stress response in human monocytic cells. Cell. Microbiol. 10, 770\u2013780 (2008) .","journal-title":"Cell. Microbiol."},{"key":"BFncomms8887_CR18","doi-asserted-by":"publisher","first-page":"548","DOI":"10.1038\/nature05124","volume":"443","author":"AW Paton","year":"2006","unstructured":"Paton, A. W. et al. AB5 subtilase cytotoxin inactivates the endoplasmic reticulum chaperone BiP. Nature 443, 548\u2013552 (2006) .","journal-title":"Nature"},{"key":"BFncomms8887_CR19","doi-asserted-by":"publisher","first-page":"112","DOI":"10.1038\/labinvest.2012.131","volume":"93","author":"M Baird","year":"2013","unstructured":"Baird, M. et al. The unfolded protein response is activated in Helicobacter-induced gastric carcinogenesis in a non-cell autonomous manner. Lab. Invest. 93, 112\u2013122 (2013) .","journal-title":"Lab. Invest."},{"key":"BFncomms8887_CR20","doi-asserted-by":"publisher","first-page":"949","DOI":"10.1111\/j.1462-5822.2012.01769.x","volume":"14","author":"H Pillich","year":"2012","unstructured":"Pillich, H., Loose, M., Zimmer, K. P. & Chakraborty, T. Activation of the unfolded protein response by Listeria monocytogenes. Cell. Microbiol. 14, 949\u2013964 (2012) .","journal-title":"Cell. Microbiol."},{"key":"BFncomms8887_CR21","doi-asserted-by":"publisher","first-page":"558","DOI":"10.1016\/j.chom.2013.03.011","volume":"13","author":"JA Cho","year":"2013","unstructured":"Cho, J. A. et al. The unfolded protein response element IRE1alpha senses bacterial proteins invading the ER to activate RIG-I and innate immune signaling. Cell Host Microbe 13, 558\u2013569 (2013) .","journal-title":"Cell Host Microbe"},{"key":"BFncomms8887_CR22","doi-asserted-by":"publisher","first-page":"898","DOI":"10.1002\/eji.201141497","volume":"41","author":"M Dalod","year":"2011","unstructured":"Dalod, M. & Pierre, P. Integration of ER stress and viral nucleotide sensing in DCs: mounting a response commensurate to the threat? Eur. J. Immunol. 41, 898\u2013901 (2011) .","journal-title":"Eur. J. Immunol."},{"key":"BFncomms8887_CR23","doi-asserted-by":"publisher","first-page":"455","DOI":"10.1038\/nature07203","volume":"454","author":"K Zhang","year":"2008","unstructured":"Zhang, K. & Kaufman, R. J. From endoplasmic-reticulum stress to the inflammatory response. Nature 454, 455\u2013462 (2008) .","journal-title":"Nature"},{"key":"BFncomms8887_CR24","doi-asserted-by":"publisher","first-page":"900","DOI":"10.1016\/j.cell.2010.02.034","volume":"140","author":"GS Hotamisligil","year":"2010","unstructured":"Hotamisligil, G. S. Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell 140, 900\u2013917 (2010) .","journal-title":"Cell"},{"key":"BFncomms8887_CR25","doi-asserted-by":"publisher","first-page":"260","DOI":"10.1038\/icb.2011.112","volume":"90","author":"SZ Hasnain","year":"2012","unstructured":"Hasnain, S. Z., Lourie, R., Das, I., Chen, A. C. & McGuckin, M. A. The interplay between endoplasmic reticulum stress and inflammation. Immunol. Cell Biol. 90, 260\u2013270 (2012) .","journal-title":"Immunol. Cell Biol."},{"key":"BFncomms8887_CR26","doi-asserted-by":"publisher","first-page":"1224","DOI":"10.1111\/cmi.12278","volume":"16","author":"A Mehlitz","year":"2014","unstructured":"Mehlitz, A. et al. The chlamydial organism Simkania negevensis forms ER vacuole contact sites and inhibits ER-stress. Cell. Microbiol. 16, 1224\u20131243 (2014) .","journal-title":"Cell. Microbiol."},{"key":"BFncomms8887_CR27","doi-asserted-by":"publisher","first-page":"1440","DOI":"10.1126\/science.1229556","volume":"338","author":"TJ O'Connor","year":"2012","unstructured":"O'Connor, T. J., Boyd, D., Dorer, M. S. & Isberg, R. R. Aggravating genetic interactions allow a solution to redundancy in a bacterial pathogen. Science 338, 1440\u20131444 (2012) .","journal-title":"Science"},{"key":"BFncomms8887_CR28","doi-asserted-by":"publisher","first-page":"229","DOI":"10.1016\/0014-5793(93)80638-B","volume":"332","author":"F DeJesus","year":"1993","unstructured":"DeJesus, F., Girardet, J. L. & Dupont, Y. Characterisation of ATP binding inhibition to the sarcoplasmic reticulum Ca(2+)-ATPase by thapsigargin. FEBS Lett. 332, 229\u2013232 (1993) .","journal-title":"FEBS Lett."},{"key":"BFncomms8887_CR29","doi-asserted-by":"publisher","first-page":"2807","DOI":"10.1089\/ars.2009.2466","volume":"11","author":"F Hatahet","year":"2009","unstructured":"Hatahet, F. & Ruddock, L. W. Protein disulfide isomerase: a critical evaluation of its function in disulfide bond formation. Antioxid. Redox Signal. 11, 2807\u20132850 (2009) .","journal-title":"Antioxid. Redox Signal."},{"key":"BFncomms8887_CR30","doi-asserted-by":"publisher","first-page":"3153","DOI":"10.1128\/AAC.42.12.3153","volume":"42","author":"AL Baltch","year":"1998","unstructured":"Baltch, A. L., Smith, R. P., Franke, M. A. & Michelsen, P. B. Antibacterial effects of levofloxacin, erythromycin, and rifampin in a human monocyte system against Legionella pneumophila. Antimicrob. Agents Chemother. 42, 3153\u20133156 (1998) .","journal-title":"Antimicrob. Agents Chemother."},{"key":"BFncomms8887_CR31","doi-asserted-by":"publisher","first-page":"1219","DOI":"10.1038\/ni.2740","volume":"14","author":"SS Ivanov","year":"2013","unstructured":"Ivanov, S. S. & Roy, C. R. Pathogen signatures activate a ubiquitination pathway that modulates the function of the metabolic checkpoint kinase mTOR. Nat. Immunol. 14, 1219\u20131228 (2013) .","journal-title":"Nat. Immunol."},{"key":"BFncomms8887_CR32","doi-asserted-by":"publisher","first-page":"1932","DOI":"10.1038\/sj.onc.1209990","volume":"26","author":"X Wan","year":"2007","unstructured":"Wan, X., Harkavy, B., Shen, N., Grohar, P. & Helman, L. J. Rapamycin induces feedback activation of Akt signaling through an IGF-1R-dependent mechanism. Oncogene 26, 1932\u20131940 (2007) .","journal-title":"Oncogene"},{"key":"BFncomms8887_CR33","doi-asserted-by":"publisher","first-page":"16953","DOI":"10.1073\/pnas.0601562103","volume":"103","author":"Y Belyi","year":"2006","unstructured":"Belyi, Y. et al. Legionella pneumophila glucosyltransferase inhibits host elongation factor 1A. Proc. Natl Acad. Sci. USA 103, 16953\u201316958 (2006) .","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"BFncomms8887_CR34","doi-asserted-by":"publisher","first-page":"e1001289","DOI":"10.1371\/journal.ppat.1001289","volume":"7","author":"MF Fontana","year":"2011","unstructured":"Fontana, M. F. et al. Secreted bacterial effectors that inhibit host protein synthesis are critical for induction of the innate immune response to virulent Legionella pneumophila. PLoS Pathog. 7, e1001289 (2011) .","journal-title":"PLoS Pathog."},{"key":"BFncomms8887_CR35","doi-asserted-by":"publisher","first-page":"92","DOI":"10.1038\/415092a","volume":"415","author":"M Calfon","year":"2002","unstructured":"Calfon, M. et al. IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature 415, 92\u201396 (2002) .","journal-title":"Nature"},{"key":"BFncomms8887_CR36","doi-asserted-by":"publisher","first-page":"1031","DOI":"10.1016\/S0092-8674(00)80369-4","volume":"90","author":"C Sidrauski","year":"1997","unstructured":"Sidrauski, C. & Walter, P. The transmembrane kinase Ire1p is a site-specific endonuclease that initiates mRNA splicing in the unfolded protein response. Cell 90, 1031\u20131039 (1997) .","journal-title":"Cell"},{"key":"BFncomms8887_CR37","doi-asserted-by":"publisher","first-page":"881","DOI":"10.1016\/S0092-8674(01)00611-0","volume":"107","author":"H Yoshida","year":"2001","unstructured":"Yoshida, H., Matsui, T., Yamamoto, A., Okada, T. & Mori, K. XBP1 mRNA is induced by ATF6 and spliced by IRE1 in response to ER stress to produce a highly active transcription factor. Cell 107, 881\u2013891 (2001) .","journal-title":"Cell"},{"key":"BFncomms8887_CR38","doi-asserted-by":"publisher","first-page":"565","DOI":"10.1083\/jcb.200508145","volume":"172","author":"H Yoshida","year":"2006","unstructured":"Yoshida, H., Oku, M., Suzuki, M. & Mori, K. pXBP1(U) encoded in XBP1 pre-mRNA negatively regulates unfolded protein response activator pXBP1(S) in mammalian ER stress response. J. Cell Biol. 172, 565\u2013575 (2006) .","journal-title":"J. Cell Biol."},{"key":"BFncomms8887_CR39","doi-asserted-by":"publisher","first-page":"382","DOI":"10.1016\/j.ymeth.2004.10.011","volume":"35","author":"J Shen","year":"2005","unstructured":"Shen, J. & Prywes, R. ER stress signaling by regulated proteolysis of ATF6. Methods 35, 382\u2013389 (2005) .","journal-title":"Methods"},{"key":"BFncomms8887_CR40","doi-asserted-by":"publisher","first-page":"75","DOI":"10.1247\/csf.07044","volume":"33","author":"Y Adachi","year":"2008","unstructured":"Adachi, Y. et al. ATF6 is a transcription factor specializing in the regulation of quality control proteins in the endoplasmic reticulum. Cell Struct. Funct. 33, 75\u201389 (2008) .","journal-title":"Cell Struct. Funct."},{"key":"BFncomms8887_CR41","doi-asserted-by":"publisher","first-page":"543","DOI":"10.1016\/j.bbrc.2007.02.004","volume":"355","author":"T Namba","year":"2007","unstructured":"Namba, T., Ishihara, T., Tanaka, K., Hoshino, T. & Mizushima, T. Transcriptional activation of ATF6 by endoplasmic reticulum stressors. Biochem Biophys. Res. Commun. 355, 543\u2013548 (2007) .","journal-title":"Biochem Biophys. Res. Commun."},{"key":"BFncomms8887_CR42","doi-asserted-by":"publisher","first-page":"1279","DOI":"10.1016\/j.celrep.2013.03.024","volume":"3","author":"MD Shoulders","year":"2013","unstructured":"Shoulders, M. D. et al. Stress-independent activation of XBP1s and\/or ATF6 reveals three functionally diverse ER proteostasis environments. Cell Rep. 3, 1279\u20131292 (2013) .","journal-title":"Cell Rep."},{"key":"BFncomms8887_CR43","doi-asserted-by":"publisher","first-page":"99","DOI":"10.1016\/S1534-5807(02)00203-4","volume":"3","author":"J Shen","year":"2002","unstructured":"Shen, J., Chen, X., Hendershot, L. & Prywes, R. ER stress regulation of ATF6 localization by dissociation of BiP\/GRP78 binding and unmasking of Golgi localization signals. Dev. Cell 3, 99\u2013111 (2002) .","journal-title":"Dev. Cell"},{"key":"BFncomms8887_CR44","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/S1534-5807(02)00210-1","volume":"3","author":"T Sommer","year":"2002","unstructured":"Sommer, T. & Jarosch, E. BiP binding keeps ATF6 at bay. Dev. Cell 3, 1\u20132 (2002) .","journal-title":"Dev. Cell"},{"key":"BFncomms8887_CR45","doi-asserted-by":"publisher","first-page":"945","DOI":"10.1038\/ncb883","volume":"4","author":"JC Kagan","year":"2002","unstructured":"Kagan, J. C. & Roy, C. R. Legionella phagosomes intercept vesicular traffic from endoplasmic reticulum exit sites. Nat. Cell Biol. 4, 945\u2013954 (2002) .","journal-title":"Nat. Cell Biol."},{"key":"BFncomms8887_CR46","doi-asserted-by":"publisher","first-page":"545","DOI":"10.1084\/jem.20030088","volume":"198","author":"J Celli","year":"2003","unstructured":"Celli, J. et al. Brucella evades macrophage killing via VirB-dependent sustained interactions with the endoplasmic reticulum. J. Exp. Med. 198, 545\u2013556 (2003) .","journal-title":"J. Exp. Med."},{"key":"BFncomms8887_CR47","doi-asserted-by":"publisher","first-page":"a007526","DOI":"10.1101\/cshperspect.a007526","volume":"3","author":"K Araki","year":"2011","unstructured":"Araki, K. & Nagata, K. Protein folding and quality control in the ER. Cold Spring Harb. Perspect. Biol. 3, a007526 (2011) .","journal-title":"Cold Spring Harb. Perspect. Biol."},{"key":"BFncomms8887_CR48","doi-asserted-by":"publisher","first-page":"910","DOI":"10.1038\/ni.2991","volume":"15","author":"S Janssens","year":"2014","unstructured":"Janssens, S., Pulendran, B. & Lambrecht, B. N. Emerging functions of the unfolded protein response in immunity. Nat. Immunol. 15, 910\u2013919 (2014) .","journal-title":"Nat. Immunol."},{"key":"BFncomms8887_CR49","doi-asserted-by":"crossref","first-page":"3609","DOI":"10.1128\/iai.63.9.3609-3620.1995","volume":"63","author":"MS Swanson","year":"1995","unstructured":"Swanson, M. S. & Isberg, R. R. Association of Legionella pneumophila with the macrophage endoplasmic reticulum. Infect. Immun. 63, 3609\u20133620 (1995) .","journal-title":"Infect. Immun."},{"key":"BFncomms8887_CR50","doi-asserted-by":"publisher","first-page":"28","DOI":"10.4161\/sgtp.18704","volume":"3","author":"MR Neunuebel","year":"2012","unstructured":"Neunuebel, M. R. & Machner, M. P. The taming of a Rab GTPase by Legionella pneumophila. Small GTPases 3, 28\u201333 (2012) .","journal-title":"Small GTPases"},{"key":"BFncomms8887_CR51","first-page":"117","volume":"376","author":"RS Goody","year":"2013","unstructured":"Goody, R. S. & Itzen, A. Modulation of small GTPases by Legionella. Curr. Top. Microbiol. Immunol. 376, 117\u2013133 (2013) .","journal-title":"Curr. Top. Microbiol. Immunol."},{"key":"BFncomms8887_CR52","doi-asserted-by":"publisher","first-page":"103","DOI":"10.1038\/nature10335","volume":"477","author":"S Mukherjee","year":"2011","unstructured":"Mukherjee, S. et al. Modulation of Rab GTPase function by a protein phosphocholine transferase. Nature 477, 103\u2013106 (2011) .","journal-title":"Nature"},{"key":"BFncomms8887_CR53","doi-asserted-by":"publisher","first-page":"14733","DOI":"10.1073\/pnas.1111678108","volume":"108","author":"TJ O'Connor","year":"2011","unstructured":"O'Connor, T. J., Adepoju, Y., Boyd, D. & Isberg, R. R. Minimization of the Legionella pneumophila genome reveals chromosomal regions involved in host range expansion. Proc. Natl Acad. Sci. USA 108, 14733\u201314740 (2011) .","journal-title":"Proc. Natl Acad. Sci. USA"}],"container-title":["Nature Communications"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/ncomms8887.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/ncomms8887","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/ncomms8887.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,1,5]],"date-time":"2023-01-05T11:03:07Z","timestamp":1672916587000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/ncomms8887"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2015,7,29]]},"references-count":53,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2015,11,24]]}},"alternative-id":["BFncomms8887"],"URL":"https:\/\/doi.org\/10.1038\/ncomms8887","relation":{},"ISSN":["2041-1723"],"issn-type":[{"value":"2041-1723","type":"electronic"}],"subject":[],"published":{"date-parts":[[2015,7,29]]},"assertion":[{"value":"26 November 2014","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"22 June 2015","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"29 July 2015","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing financial interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"7887"}}