{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,2]],"date-time":"2026-07-02T03:31:49Z","timestamp":1782963109461,"version":"3.54.5"},"reference-count":89,"publisher":"MDPI AG","issue":"8","license":[{"start":{"date-parts":[[2023,4,20]],"date-time":"2023-04-20T00:00:00Z","timestamp":1681948800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100001659","name":"DFG","doi-asserted-by":"publisher","award":["FL 168\/5-1"],"award-info":[{"award-number":["FL 168\/5-1"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100001659","name":"DFG","doi-asserted-by":"publisher","award":["HE 1383\/13-1"],"award-info":[{"award-number":["HE 1383\/13-1"]}],"id":[{"id":"10.13039\/501100001659","id-type":"DOI","asserted-by":"publisher"}]},{"name":"J\u00fcrgen Manchot Stiftung","award":["FL 168\/5-1"],"award-info":[{"award-number":["FL 168\/5-1"]}]},{"name":"J\u00fcrgen Manchot Stiftung","award":["HE 1383\/13-1"],"award-info":[{"award-number":["HE 1383\/13-1"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Bacterial pathogens have evolved intricate ways to manipulate the host to support infection. Here, we systematically assessed the importance of the microtubule cytoskeleton for infection by Chlamydiae, which are obligate intracellular bacteria that are of great importance for human health. The elimination of microtubules in human HEp-2 cells prior to C. pneumoniae infection profoundly attenuated the infection efficiency, demonstrating the need for microtubules for the early infection processes. To identify microtubule-modulating C. pneumoniae proteins, a screen in the model yeast Schizosaccharomyces pombe was performed. Unexpectedly, among 116 selected chlamydial proteins, more than 10%, namely, 13 proteins, massively altered the yeast interphase microtubule cytoskeleton. With two exceptions, these proteins were predicted to be inclusion membrane proteins. As proof of principle, we selected the conserved CPn0443 protein, which caused massive microtubule instability in yeast, for further analysis. CPn0443 bound and bundled microtubules in vitro and co-localized partially with microtubules in vivo in yeast and human cells. Furthermore, CPn0443-transfected U2OS cells had a significantly reduced infection rate by C. pneumoniae EBs. Thus, our yeast screen identified numerous proteins encoded using the highly reduced C. pneumoniae genome that modulated microtubule dynamics. Hijacking of the host microtubule cytoskeleton must be a vital part of chlamydial infection.<\/jats:p>","DOI":"10.3390\/ijms24087618","type":"journal-article","created":{"date-parts":[[2023,4,21]],"date-time":"2023-04-21T03:01:48Z","timestamp":1682046108000},"page":"7618","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["A Functional Yeast-Based Screen Identifies the Host Microtubule Cytoskeleton as a Target of Numerous Chlamydia pneumoniae Proteins"],"prefix":"10.3390","volume":"24","author":[{"given":"Carolin","family":"Wevers","sequence":"first","affiliation":[{"name":"Eukaryotic Microbiology, Institute of Functional Microbial Genomics, Heinrich-Heine-University, 40225 D\u00fcsseldorf, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3573-953X","authenticated-orcid":false,"given":"Mona","family":"H\u00f6hler","sequence":"additional","affiliation":[{"name":"Eukaryotic Microbiology, Institute of Functional Microbial Genomics, Heinrich-Heine-University, 40225 D\u00fcsseldorf, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Abel R.","family":"Alc\u00e1zar-Rom\u00e1n","sequence":"additional","affiliation":[{"name":"Eukaryotic Microbiology, Institute of Functional Microbial Genomics, Heinrich-Heine-University, 40225 D\u00fcsseldorf, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Johannes H.","family":"Hegemann","sequence":"additional","affiliation":[{"name":"Institute of Functional Microbial Genomics, Heinrich-Heine-University, 40225 D\u00fcsseldorf, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0270-0970","authenticated-orcid":false,"given":"Ursula","family":"Fleig","sequence":"additional","affiliation":[{"name":"Eukaryotic Microbiology, Institute of Functional Microbial Genomics, Heinrich-Heine-University, 40225 D\u00fcsseldorf, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,4,20]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Hohmann, T., and Dehghani, F. (2019). The Cytoskeleton-A Complex Interacting Meshwork. Cells, 8.","DOI":"10.3390\/cells8040362"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"a022608","DOI":"10.1101\/cshperspect.a022608","article-title":"Microtubules and Microtubule-Associated Proteins","volume":"10","author":"Goodson","year":"2018","journal-title":"Cold Spring Harb. Perspect. Biol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"a018267","DOI":"10.1101\/cshperspect.a018267","article-title":"The Actin Cytoskeleton and Actin-Based Motility","volume":"10","author":"Svitkina","year":"2018","journal-title":"Cold Spring Harb. Perspect. Biol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"a018242","DOI":"10.1101\/cshperspect.a018242","article-title":"Intermediate Filaments: Structure and Assembly","volume":"8","author":"Herrmann","year":"2016","journal-title":"Cold Spring Harb. Perspect. Biol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1016\/j.ceb.2020.10.007","article-title":"The state of the septin cytoskeleton from assembly to function","volume":"68","author":"Woods","year":"2021","journal-title":"Curr. Opin. Cell Biol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"487","DOI":"10.1038\/nrmicro2592","article-title":"Bacterial protein toxins that modify host regulatory GTPases","volume":"9","author":"Aktories","year":"2011","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"3658","DOI":"10.1002\/1873-3468.13173","article-title":"Actin dynamics in host-pathogen interaction","volume":"592","author":"Stradal","year":"2018","journal-title":"FEBS Lett."},{"key":"ref_8","doi-asserted-by":"crossref","unstructured":"Alqassim, S.S. (2022). Functional Mimicry of Eukaryotic Actin Assembly by Pathogen Effector Proteins. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms231911606"},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"571","DOI":"10.1515\/bmc-2012-0030","article-title":"Modulation of host microtubule dynamics by pathogenic bacteria","volume":"3","author":"Radhakrishnan","year":"2012","journal-title":"Biomol. Concepts"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"S1","DOI":"10.1111\/j.1469-0691.1998.tb00697.x","article-title":"Epidemiology of Chlamydia pneumoniae","volume":"4","author":"Blasi","year":"1998","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"237","DOI":"10.1615\/ForumImmunDisTher.2017020161","article-title":"Chlamydia pneumoniae Infection and Inflammatory Diseases","volume":"7","author":"Porritt","year":"2016","journal-title":"Forum Immunopathol. Dis. Ther."},{"key":"ref_12","unstructured":"Tran, M., Hegemann, J.H., and S\u00fctterlin, C. (2020). Chlamydia Biology: From Genome to Disease, Caister Academic Press."},{"key":"ref_13","doi-asserted-by":"crossref","unstructured":"Stephens, R.S. (1999). Chlamydia: Intracellular Biology, Pathogenesis, and Immunity, ASM Press.","DOI":"10.1128\/9781555818203"},{"key":"ref_14","unstructured":"Tran, M., Hegemann, J.H., and S\u00fctterlin, C. (2020). Chlamydia Biology: From Genome to Disease, Caister Academic Press."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"385","DOI":"10.1038\/nrmicro.2016.30","article-title":"Chlamydia cell biology and pathogenesis","volume":"14","author":"Elwell","year":"2016","journal-title":"Nat. Rev. Microbiol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"11430","DOI":"10.1073\/pnas.0703218104","article-title":"Mechanisms of host cell exit by the intracellular bacterium Chlamydia","volume":"104","author":"Hybiske","year":"2007","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_17","first-page":"193","article-title":"Control mechanisms governing the infectivity of Chlamydia trachomatis for HeLa cells: The role of calmodulin","volume":"130","author":"Murray","year":"1984","journal-title":"J. Gen. Microbiol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"324","DOI":"10.1128\/iai.63.1.324-332.1995","article-title":"Cytoskeletal requirements in Chlamydia trachomatis infection of host cells","volume":"63","author":"Schramm","year":"1995","journal-title":"Infect. Immun."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"4465","DOI":"10.1128\/iai.59.12.4465-4472.1991","article-title":"Mobilization of F-actin and clathrin during redistribution of Chlamydia trachomatis to an intracellular site in eucaryotic cells","volume":"59","author":"Majeed","year":"1991","journal-title":"Infect. Immun."},{"key":"ref_20","first-page":"1765","article-title":"Control mechanisms governing the infectivity of Chlamydia trachomatis for HeLa cells: Mechanisms of endocytosis","volume":"130","author":"Ward","year":"1984","journal-title":"J. Gen. Microbiol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"3793","DOI":"10.1242\/jcs.00695","article-title":"Chlamydia trachomatis uses host cell dynein to traffic to the microtubule-organizing center in a p50 dynamitin-independent process","volume":"116","author":"Grieshaber","year":"2003","journal-title":"J. Cell Sci."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"441","DOI":"10.1046\/j.1365-2958.1997.4591832.x","article-title":"Chlamydia trachomatis utilizes the host cell microtubule network during early events of infection","volume":"25","author":"Clausen","year":"1997","journal-title":"Mol. Microbiol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1016\/j.chom.2008.05.018","article-title":"Actin and intermediate filaments stabilize the Chlamydia trachomatis vacuole by forming dynamic structural scaffolds","volume":"4","author":"Kumar","year":"2008","journal-title":"Cell Host Microbe"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"e01802","DOI":"10.1128\/mBio.01802-14","article-title":"Septins arrange F-actin-containing fibers on the Chlamydia trachomatis inclusion and are required for normal release of the inclusion by extrusion","volume":"5","author":"Volceanov","year":"2014","journal-title":"mBio"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1285","DOI":"10.1111\/mmi.12829","article-title":"Chlamydia trachomatis remodels stable microtubules to coordinate Golgi stack recruitment to the chlamydial inclusion surface","volume":"94","author":"Kerr","year":"2014","journal-title":"Mol. Microbiol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"10166","DOI":"10.1073\/pnas.0402829101","article-title":"A chlamydial type III translocated protein is tyrosine-phosphorylated at the site of entry and associated with recruitment of actin","volume":"101","author":"Clifton","year":"2004","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"1423","DOI":"10.1111\/j.1365-2958.2009.06732.x","article-title":"Evidence that CT694 is a novel Chlamydia trachomatis T3S substrate capable of functioning during invasion or early cycle development","volume":"72","author":"Hower","year":"2009","journal-title":"Mol. Microbiol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"511","DOI":"10.3389\/fcimb.2017.00511","article-title":"The Chlamydia pneumoniae Tarp Ortholog CPn0572 Stabilizes Host F-Actin by Displacement of Cofilin","volume":"7","author":"Zrieq","year":"2017","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"jcs260185","DOI":"10.1242\/jcs.260185","article-title":"Distinct roles of the Chlamydia trachomatis effectors TarP and TmeA in the regulation of formin and Arp2\/3 during entry","volume":"135","author":"Romero","year":"2022","journal-title":"J. Cell Sci."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1016\/j.bbrc.2015.04.116","article-title":"Chlamydia trachomatis inclusion membrane protein CT850 interacts with the dynein light chain DYNLT1 (Tctex1)","volume":"462","author":"Mital","year":"2015","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"1235","DOI":"10.1111\/j.1462-5822.2010.01465.x","article-title":"Specific chlamydial inclusion membrane proteins associate with active Src family kinases in microdomains that interact with the host microtubule network","volume":"12","author":"Mital","year":"2010","journal-title":"Cell. Microbiol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"542","DOI":"10.1016\/j.ijmm.2014.03.005","article-title":"Chlamydia psittaci inclusion membrane protein IncB associates with host protein Snapin","volume":"304","author":"Heurich","year":"2014","journal-title":"Int. J. Med. Microbiol."},{"key":"ref_33","first-page":"3420","article-title":"A Chlamydia effector recruits CEP170 to reprogram host microtubule organization","volume":"128","author":"Dumoux","year":"2015","journal-title":"J. Cell Sci."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"2058","DOI":"10.12688\/f1000research.12316.1","article-title":"Taking control: Reorganization of the host cytoskeleton by Chlamydia","volume":"6","author":"Wesolowski","year":"2017","journal-title":"F1000Res"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"e0239721","DOI":"10.1128\/mBio.02397-21","article-title":"Cross Talk between ARF1 and RhoA Coordinates the Formation of Cytoskeletal Scaffolds during Chlamydia Infection","volume":"12","author":"Haines","year":"2021","journal-title":"mBio"},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Sherry, J., Dolat, L., McMahon, E., Swaney, D.L., Bastidas, R.J., Johnson, J.R., Valdivia, R.H., Krogan, N.J., Elwell, C.A., and Engel, J.N. (2022). Chlamydia trachomatis effector Dre1 interacts with dynactin to reposition host organelles during infection. bioRxiv, 2022.2004.2015.488217.","DOI":"10.1101\/2022.04.15.488217"},{"key":"ref_37","unstructured":"Tran, M., Hegemann, J.H., and S\u00fctterlin, C. (2020). Chlamydia Biology: From Genome to Disease, Caister Academic Press."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"46896","DOI":"10.1074\/jbc.M407227200","article-title":"Conservation of the biochemical properties of IncA from Chlamydia trachomatis and Chlamydia caviae: Oligomerization of IncA mediates interaction between facing membranes","volume":"279","author":"Delevoye","year":"2004","journal-title":"J. Biol. Chem."},{"key":"ref_39","doi-asserted-by":"crossref","unstructured":"Dehoux, P., Flores, R., Dauga, C., Zhong, G., and Subtil, A. (2011). Multi-genome identification and characterization of chlamydiae-specific type III secretion substrates: The Inc proteins. BMC Genom., 12.","DOI":"10.1186\/1471-2164-12-109"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"33992","DOI":"10.1074\/jbc.M111.258426","article-title":"The Chlamydia effector chlamydial outer protein N (CopN) sequesters tubulin and prevents microtubule assembly","volume":"286","author":"Archuleta","year":"2011","journal-title":"J. Biol. Chem."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"25199","DOI":"10.1074\/jbc.M114.568436","article-title":"Biochemical and Structural Insights into Microtubule Perturbation by CopN from Chlamydia pneumoniae","volume":"289","author":"Nawrotek","year":"2014","journal-title":"J. Biol. Chem."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1016\/j.devcel.2007.01.020","article-title":"Organization of interphase microtubules in fission yeast analyzed by electron tomography","volume":"12","author":"Hoog","year":"2007","journal-title":"Dev. Cell"},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Loiodice, I., Janson, M.E., Tavormina, P., Schaub, S., Bhatt, D., Cochran, R., Czupryna, J., Fu, C., and Tran, P.T. (2019). Quantifying Tubulin Concentration and Microtubule Number Throughout the Fission Yeast Cell Cycle. Biomolecules, 9.","DOI":"10.3390\/biom9030086"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1001","DOI":"10.1002\/yea.1404","article-title":"Cytoplasmic microtubule organization in fission yeast","volume":"23","author":"Sawin","year":"2006","journal-title":"Yeast"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"362104","DOI":"10.1155\/2012\/362104","article-title":"Evolution and conservation of predicted inclusion membrane proteins in chlamydiae","volume":"2012","author":"Lutter","year":"2012","journal-title":"Comp. Funct. Genom."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"51","DOI":"10.1111\/j.1365-2958.2006.05074.x","article-title":"Multifunctional analysis of Chlamydia-specific genes in a yeast expression system","volume":"60","author":"Sisko","year":"2006","journal-title":"Mol. Microbiol."},{"key":"ref_47","unstructured":"Herbst, F. (2011). Identifizierung und Charakterisierung Potentieller Neuer Effektorproteine aus Chlamydia pneumoniae, Heinreich-Heine-Universit\u00e4t."},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Maurer, A.P., Mehlitz, A., Mollenkopf, H.J., and Meyer, T.F. (2007). Gene expression profiles of Chlamydophila pneumoniae during the developmental cycle and iron depletion-mediated persistence. PLoS Pathog., 3.","DOI":"10.1371\/journal.ppat.0030083"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"861","DOI":"10.1002\/1097-0061(20000630)16:9<861::AID-YEA577>3.0.CO;2-9","article-title":"A family of multifunctional thiamine-repressible expression vectors for fission yeast","volume":"16","author":"Moreno","year":"2000","journal-title":"Yeast"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1016\/S0022-2836(83)80017-5","article-title":"Cold-sensitive nuclear division arrest mutants of the fission yeast Schizosaccharomyces pombe","volume":"168","author":"Toda","year":"1983","journal-title":"J. Mol. Biol."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"3389","DOI":"10.1093\/emboj\/20.13.3389","article-title":"Fission yeast ch-TOG\/XMAP215 homologue Alp14 connects mitotic spindles with the kinetochore and is a component of the Mad2-dependent spindle checkpoint","volume":"20","author":"Garcia","year":"2001","journal-title":"EMBO J."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"2441","DOI":"10.1091\/mbc.e06-08-0738","article-title":"The conserved Spc7 protein is required for spindle integrity and links kinetochore complexes in fission yeast","volume":"18","author":"Kerres","year":"2007","journal-title":"Mol. Biol. Cell"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"343","DOI":"10.1242\/jcs.89.3.343","article-title":"The use of cell division cycle mutants to investigate the control of microtubule distribution in the fission yeast Schizosaccharomyces pombe","volume":"89","author":"Hagan","year":"1988","journal-title":"J. Cell Sci."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"647","DOI":"10.1038\/35089520","article-title":"A journey into space","volume":"2","author":"Hayles","year":"2001","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"717","DOI":"10.1083\/jcb.139.3.717","article-title":"Mal3, the fission yeast homologue of the human APC-interacting protein EB-1 is required for microtubule integrity and the maintenance of cell form","volume":"139","author":"Beinhauer","year":"1997","journal-title":"J. Cell Biol."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"2381","DOI":"10.1007\/s00018-017-2476-2","article-title":"Regulation of end-binding protein EB1 in the control of microtubule dynamics","volume":"74","author":"Nehlig","year":"2017","journal-title":"Cell. Mol. Life Sci."},{"key":"ref_57","doi-asserted-by":"crossref","unstructured":"Erent, M., Drummond, D.R., and Cross, R.A.S. (2012). pombe kinesins-8 promote both nucleation and catastrophe of microtubules. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0030738"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"2360","DOI":"10.1091\/mbc.02-01-0603","article-title":"A fourth component of the fission yeast gamma-tubulin complex, Alp16, is required for cytoplasmic microtubule integrity and becomes indispensable when gamma-tubulin function is compromised","volume":"13","author":"Fujita","year":"2002","journal-title":"Mol. Biol. Cell"},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"e74535","DOI":"10.7554\/eLife.74535","article-title":"Phosphoregulation accommodates Type III secretion and assembly of a tether of ER-Chlamydia inclusion membrane contact sites","volume":"11","author":"Ende","year":"2022","journal-title":"eLife"},{"key":"ref_60","doi-asserted-by":"crossref","unstructured":"Flor-Parra, I., Sabido-Bozo, S., Ikeda, A., Hanaoka, K., Aguilera-Romero, A., Funato, K., Muniz, M., and Lucena, R. (2021). The Ceramide Synthase Subunit Lac1 Regulates Cell Growth and Size in Fission Yeast. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms23010303"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"931","DOI":"10.1038\/s41467-019-08862-2","article-title":"The Cep57-pericentrin module organizes PCM expansion and centriole engagement","volume":"10","author":"Watanabe","year":"2019","journal-title":"Nat. Commun."},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"487","DOI":"10.1016\/j.tranon.2015.11.004","article-title":"Prognostic Significance and Functional Role of CEP57 in Prostate Cancer","volume":"8","author":"Mang","year":"2015","journal-title":"Transl. Oncol."},{"key":"ref_63","doi-asserted-by":"crossref","unstructured":"Zhou, H., Zheng, T., Wang, T., Li, Q., Wang, F., Liang, X., Chen, J., and Teng, J. (2019). CCDC74A\/B are K-fiber crosslinkers required for chromosomal alignment. BMC Biol., 17.","DOI":"10.1186\/s12915-019-0694-9"},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"115","DOI":"10.1016\/bs.mcb.2017.06.015","article-title":"Measuring Tau-microtubule affinity through cosedimentation assays","volume":"141","author":"Alberico","year":"2017","journal-title":"Methods Cell Biol."},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"1175","DOI":"10.1083\/jcb.200111052","article-title":"PRC1 is a microtubule binding and bundling protein essential to maintain the mitotic spindle midzone","volume":"157","author":"Mollinari","year":"2002","journal-title":"J. Cell Biol."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"359","DOI":"10.1089\/dna.1995.14.359","article-title":"Schizosaccharomyces pombe: A model for molecular studies of eukaryotic genes","volume":"14","author":"Zhao","year":"1995","journal-title":"DNA Cell Biol."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"112","DOI":"10.2119\/molmed.2016.00189","article-title":"A Journey in Science: Cell-Cycle Control","volume":"22","author":"Nurse","year":"2017","journal-title":"Mol. Med."},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"351","DOI":"10.1016\/bs.pmbts.2019.07.001","article-title":"Yeast models of neurodegenerative diseases","volume":"168","author":"Tuite","year":"2019","journal-title":"Prog. Mol. Biol. Transl. Sci."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1002\/cm.970180203","article-title":"Microtubules in the fission yeast Schizosaccharomyces pombe contain only the tyrosinated form of alpha-tubulin","volume":"18","author":"Alfa","year":"1991","journal-title":"Cell Motil. Cytoskelet."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"e02280-16","DOI":"10.1128\/mBio.02280-16","article-title":"Chlamydia Hijacks ARF GTPases To Coordinate Microtubule Posttranslational Modifications and Golgi Complex Positioning","volume":"8","author":"Wesolowski","year":"2017","journal-title":"mBio"},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"R98","DOI":"10.1186\/gb-2011-12-10-r98","article-title":"The transcriptional landscape of Chlamydia pneumoniae","volume":"12","author":"Albrecht","year":"2011","journal-title":"Genome Biol."},{"key":"ref_72","unstructured":"Murra, G. (2009). Identifizierung und Charakterisierung von Adh\u00e4sionsproteinen des Humanpathogenen Erregers Chlamydia pneumoniae, Heinrich-Heine-Universit\u00e4t D\u00fcsseldorf."},{"key":"ref_73","doi-asserted-by":"crossref","unstructured":"Luo, J., Liu, G., Zhong, Y., Jia, T., Liu, K., Chen, D., and Zhong, G. (2007). Characterization of hypothetical proteins Cpn0146, 0147, 0284 & 0285 that are predicted to be in the Chlamydia pneumoniae inclusion membrane. BMC Microbiol., 7.","DOI":"10.1186\/1471-2180-7-38"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"777","DOI":"10.1099\/mic.0.2006\/002956-0","article-title":"Characterization of the hypothetical protein Cpn1027, a newly identified inclusion membrane protein unique to Chlamydia pneumoniae","volume":"153","author":"Flores","year":"2007","journal-title":"Microbiology"},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"e46196","DOI":"10.15252\/embr.201846196","article-title":"Opposing kinesin complexes queue at plus tips to ensure microtubule catastrophe at cell ends","volume":"19","author":"Meadows","year":"2018","journal-title":"EMBO Rep."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"12039","DOI":"10.1073\/pnas.1709060114","article-title":"IncV, a FFAT motif-containing Chlamydia protein, tethers the endoplasmic reticulum to the pathogen-containing vacuole","volume":"114","author":"Stanhope","year":"2017","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"132","DOI":"10.1038\/s41586-021-04204-9","article-title":"ER proteins decipher the tubulin code to regulate organelle distribution","volume":"601","author":"Zheng","year":"2022","journal-title":"Nature"},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"653","DOI":"10.1111\/j.1567-1364.2011.00752.x","article-title":"Versatile use of Schizosaccharomyces pombe plasmids in Saccharomyces cerevisiae","volume":"11","author":"Jakopec","year":"2011","journal-title":"FEMS Yeast Res."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"367","DOI":"10.1016\/S1286-4579(00)00335-X","article-title":"Type III secretion system in Chlamydia species: Identified members and candidates [letter]","volume":"2","author":"Subtil","year":"2000","journal-title":"Microbes Infect."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"620","DOI":"10.1128\/jcm.35.3.620-623.1997","article-title":"Antigenic and molecular analyses of different Chlamydia pneumoniae strains","volume":"35","author":"Jantos","year":"1997","journal-title":"J. Clin. Microbiol."},{"key":"ref_81","doi-asserted-by":"crossref","unstructured":"Weinmaier, T., Hoser, J., Eck, S., Kaufhold, I., Shima, K., Strom, T.M., Rattei, T., and Rupp, J. (2015). Genomic factors related to tissue tropism in Chlamydia pneumoniae infection. BMC Genom., 16.","DOI":"10.1186\/s12864-015-1377-8"},{"key":"ref_82","doi-asserted-by":"crossref","unstructured":"Masumoto, H., and Matsuyama, S. (2018). The combination of NAD+-dependent deacetylase gene deletion and the interruption of gluconeogenesis causes increased glucose metabolism in budding yeast. PLoS ONE, 13.","DOI":"10.1371\/journal.pone.0194942"},{"key":"ref_83","doi-asserted-by":"crossref","unstructured":"Molleken, K., and Hegemann, J.H. (2017). Acquisition of Rab11 and Rab11-Fip2-A novel strategy for Chlamydia pneumoniae early survival. PLoS Pathog., 13.","DOI":"10.1371\/journal.ppat.1006556"},{"key":"ref_84","doi-asserted-by":"crossref","first-page":"795","DOI":"10.1016\/0076-6879(91)94059-L","article-title":"Molecular genetic analysis of fission yeast Schizosaccharomyces pombe","volume":"194","author":"Moreno","year":"1991","journal-title":"Methods Enzymol."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"220","DOI":"10.1016\/j.ymeth.2003.11.017","article-title":"Imaging green fluorescent protein fusions in living fission yeast cells","volume":"33","author":"Tran","year":"2004","journal-title":"Methods"},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"792","DOI":"10.1046\/j.1365-2958.2001.02272.x","article-title":"Secretion of predicted Inc proteins of Chlamydia pneumoniae by a heterologous type III machinery","volume":"39","author":"Subtil","year":"2001","journal-title":"Mol. Microbiol."},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"35","DOI":"10.1046\/j.1462-5822.2000.00029.x","article-title":"A secondary structure motif predictive of protein localization to the chlamydial inclusion membrane","volume":"2","author":"Bannantine","year":"2000","journal-title":"Cell. Microbiol."},{"key":"ref_88","doi-asserted-by":"crossref","first-page":"1636","DOI":"10.1111\/j.1365-2958.2005.04647.x","article-title":"A directed screen for chlamydial proteins secreted by a type III mechanism identifies a translocated protein and numerous other new candidates","volume":"56","author":"Subtil","year":"2005","journal-title":"Mol Microbiol"},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"497","DOI":"10.1128\/IAI.00935-06","article-title":"Hypothetical Protein Cpn0308 Is Localized in the Chlamydia pneumoniae Inclusion Membrane","volume":"75","author":"Luo","year":"2007","journal-title":"Infect. Immun."}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/8\/7618\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T19:20:14Z","timestamp":1760124014000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/24\/8\/7618"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,4,20]]},"references-count":89,"journal-issue":{"issue":"8","published-online":{"date-parts":[[2023,4]]}},"alternative-id":["ijms24087618"],"URL":"https:\/\/doi.org\/10.3390\/ijms24087618","relation":{},"ISSN":["1422-0067"],"issn-type":[{"value":"1422-0067","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,4,20]]}}}