{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,14]],"date-time":"2025-10-14T00:46:57Z","timestamp":1760402817647,"version":"build-2065373602"},"reference-count":36,"publisher":"MDPI AG","issue":"4","license":[{"start":{"date-parts":[[2020,4,17]],"date-time":"2020-04-17T00:00:00Z","timestamp":1587081600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Pathogens"],"abstract":"<jats:p>Background. Previous works suggest that sugars can have a beneficial effect on C. trachomatis (CT) survival and virulence. In this study, we investigated the effect of different sugars on CT infectivity, elucidating some of the molecular mechanisms behind CT-sugar interaction. Methods. CT infectivity was investigated on HeLa cells after 2 hour-incubation of elementary bodies (EBs) with glucose, sucrose, or mannitol solutions (0.5, 2.5, 5.0 mM). The effect of sugars on EB membrane fluidity was investigated by fluorescence anisotropy measurement, whereas the changes in lipopolysaccharide (LPS) exposure were examined by cytofluorimetric analysis. By means of a Western blot, we explored the phosphorylation state of Focal Adhesion Kinase (FAK) in HeLa cells infected with EBs pre-incubated with sugars. Results. All sugar solutions significantly increased CT infectivity on epithelial cells, acting directly on the EB structure. Sugars induced a significant increase of EB membrane fluidity, leading to changes in LPS membrane exposure. Especially after incubation with sucrose and mannitol, EBs led to a higher FAK phosphorylation, enhancing the activation of anti-apoptotic and proliferative signals in the host cells. Conclusions. Sugars can increase CT infectivity and virulence, by modulating the expression\/exposure of chlamydial membrane ligands. Further in-depth studies are needed to better understand the molecular mechanisms involved.<\/jats:p>","DOI":"10.3390\/pathogens9040298","type":"journal-article","created":{"date-parts":[[2020,4,21]],"date-time":"2020-04-21T04:49:38Z","timestamp":1587444578000},"page":"298","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Effect of Sugars on Chlamydia trachomatis Infectivity"],"prefix":"10.3390","volume":"9","author":[{"given":"Giacomo","family":"Marziali","sequence":"first","affiliation":[{"name":"FaBiT Department, University of Bologna, Via Irnerio 42, 40126 Bologna, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Antonella","family":"Marangoni","sequence":"additional","affiliation":[{"name":"Microbiology, DIMES, University of Bologna, St. Orsola Hospital, Via Massarenti, 9, 40138 Bologna, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7253-8799","authenticated-orcid":false,"given":"Claudio","family":"Foschi","sequence":"additional","affiliation":[{"name":"Microbiology, DIMES, University of Bologna, St. Orsola Hospital, Via Massarenti, 9, 40138 Bologna, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Maria Carla","family":"Re","sequence":"additional","affiliation":[{"name":"Microbiology, DIMES, University of Bologna, St. Orsola Hospital, Via Massarenti, 9, 40138 Bologna, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Natalia","family":"Calonghi","sequence":"additional","affiliation":[{"name":"FaBiT Department, University of Bologna, Via Irnerio 42, 40126 Bologna, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2020,4,17]]},"reference":[{"key":"ref_1","unstructured":"European Centre for Disease Prevention and Control (2015). Sexually Transmitted Infection in Europe 2013, ECDC."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"969","DOI":"10.1128\/CMR.00035-15","article-title":"Human and Pathogen Factors Associated with Chlamydia trachomatis-Related Infertility in Women","volume":"28","author":"Menon","year":"2015","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1128\/mr.55.1.143-190.1991","article-title":"Interaction of chlamydiae and host cells in vitro","volume":"55","author":"Moulder","year":"1991","journal-title":"Microbiol. Rev."},{"key":"ref_4","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_5","doi-asserted-by":"crossref","first-page":"19781","DOI":"10.1073\/pnas.1212831109","article-title":"Developmental stage-specific metabolic and transcriptional activity of Chlamydia trachomatis in an axenic medium","volume":"109","author":"Omsland","year":"2012","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"e00065-18","DOI":"10.1128\/JB.00065-18","article-title":"Impact of Active Metabolism on Chlamydia trachomatis Elementary Body Transcript Profile and Infectivity","volume":"200","author":"Grieshaber","year":"2018","journal-title":"J. Bacteriol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"ftx108","DOI":"10.1093\/femspd\/ftx108","article-title":"Orchestration of the mammalian host cell glucose transporter proteins-1 and 3 by Chlamydia contributes to intracellular growth and infectivity","volume":"75","author":"Wang","year":"2017","journal-title":"Pathog. Dis."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1004","DOI":"10.1111\/mmi.13603","article-title":"Metabolic adaptation of Chlamydia trachomatis to mammalian host cells","volume":"103","author":"Mehlitz","year":"2017","journal-title":"Mol. Microbiol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"29024","DOI":"10.1038\/srep29024","article-title":"Lactobacillus crispatus inhibits the infectivity of Chlamydia trachomatis elementary bodies, in vitro study","volume":"6","author":"Nardini","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Foschi, C., Laghi, L., D\u2019Antuono, A., Gaspari, V., Zhu, C., Dellarosa, N., Salvo, M., and Marangoni, A. (2018). Urine metabolome in women with Chlamydia trachomatis infection. PLoS ONE, 13.","DOI":"10.1371\/journal.pone.0194827"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"17","DOI":"10.3389\/fcimb.2011.00017","article-title":"Major host factors involved in epithelial cell invasion of Campylobacter jejuni: Role of fibronectin, integrin \u03b21, FAK, Tiam-1, and DOCK180 in activating Rho GTPase Rac1","volume":"1","author":"Boehm","year":"2011","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"278","DOI":"10.1186\/1476-4598-9-278","article-title":"Dasatinib reduces FAK phosphorylation increasing the effects of RPI-1 inhibition in a RET\/PTC1-expressing cell line","volume":"9","author":"Caccia","year":"2010","journal-title":"Mol. Cancer"},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"368","DOI":"10.1038\/sj.bjc.6603884","article-title":"Downstream signalling and specific inhibition of c-MET\/HGF pathway in small cell lung cancer: Implications for tumour invasion","volume":"97","author":"Ma","year":"2007","journal-title":"Br. J. Cancer"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"167","DOI":"10.1016\/0163-7827(90)90002-3","article-title":"The role of alterations in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment","volume":"29","author":"Hazel","year":"1990","journal-title":"Prog. Lipid. Res."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"87","DOI":"10.3109\/07388559709146608","article-title":"Effect of some environmental factors on the content and composition of microbial membrane lipids","volume":"17","author":"Sajbidor","year":"1997","journal-title":"Crit. Rev. Biotechnol."},{"key":"ref_16","first-page":"255","article-title":"Influence of the environment on microbial lipid composition","volume":"Volume 2","author":"Ratledge","year":"1990","journal-title":"Microbial Lipids"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1553","DOI":"10.1021\/mp900110q","article-title":"Biophysical and stabilization studies of the Chlamydia trachomatis mouse pneumonitis major outer membrane protein","volume":"6","author":"Cai","year":"2009","journal-title":"Mol. Pharm."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"7068","DOI":"10.1002\/chem.201600533","article-title":"Accessible Mannitol-Based Amphiphiles (MNAs) for Membrane Protein Solubilisation and Stabilisation","volume":"22","author":"Hussain","year":"2016","journal-title":"Chemistry"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"330","DOI":"10.3390\/nu2030330","article-title":"Pilot-scale production and viability analysis of freeze-dried probiotic bacteria using different protective agents","volume":"2","author":"Savini","year":"2010","journal-title":"Nutrients"},{"key":"ref_20","doi-asserted-by":"crossref","unstructured":"Campbell, R., Tasevska, N., Jackson, K.G., Sagi-Kiss, V., di Paolo, N., Mindell, J.S., Lister, S.J., Khaw, K.T., and Kuhnle, G.G.C. (2017). Association between urinary biomarkers of total sugar intake and measures of obesity in a cross-sectional study. PLoS ONE, 12.","DOI":"10.1101\/099556"},{"key":"ref_21","doi-asserted-by":"crossref","unstructured":"Bouatra, S., Aziat, F., Mandal, R., Guo, A.C., Wilson, M.R., Knox, C., Bjorndahl, T.C., Krishnamurthy, R., Saleem, F., and Liu, P. (2013). The human urine metabolome. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0073076"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"261","DOI":"10.1099\/jmm.0.47237-0","article-title":"Is lipopolysaccharide a factor in infectivity of Chlamydia trachomatis?","volume":"57","author":"Fadel","year":"2008","journal-title":"J. Med. Microbiol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"593","DOI":"10.1042\/CBI20090227","article-title":"CFTR is required for cellular entry and internalization of Chlamydia trachomatis","volume":"34","author":"Ajonuma","year":"2010","journal-title":"Cell. Biol. Int."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"10284","DOI":"10.1073\/pnas.1107478108","article-title":"Lipooligosaccharide is required for the generation of infectious elementary bodies in Chlamydia trachomatis","volume":"108","author":"Nguyen","year":"2011","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"e00595-19","DOI":"10.1128\/mBio.00595-19","article-title":"Chlamydia trachomatis Lipopolysaccharide Evades the Canonical and Noncanonical Inflammatory Pathways To Subvert Innate Immunity","volume":"10","author":"Yang","year":"2019","journal-title":"mBio"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"126","DOI":"10.1177\/0968051907079122","article-title":"Investigation on the agonistic and antagonistic biological activities of synthetic Chlamydia lipid A and its use in in vitro enzymatic assays","volume":"13","author":"Heine","year":"2007","journal-title":"J. Endotoxin Res."},{"key":"ref_27","doi-asserted-by":"crossref","unstructured":"Slanina, H., Hebling, S., Hauck, C.R., and Schubert-Unkmeir, A. (2012). Cell invasion by Neisseria meningitidis requires a functional interplay between the focal adhesion kinase, Src and cortactin. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0039613"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1826","DOI":"10.1128\/IAI.00142-16","article-title":"Role of Host Type IA Phosphoinositide 3-Kinase Pathway Components in Invasin-Mediated Internalization of Yersinia enterocolitica","volume":"84","author":"Dowd","year":"2016","journal-title":"Infect. Immun."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"4698","DOI":"10.1091\/mbc.e06-06-0492","article-title":"Invasion of host cells by Salmonella typhimurium requires focal adhesion kinase and p130Cas","volume":"17","author":"Shi","year":"2006","journal-title":"Mol. Biol. Cell"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"2630","DOI":"10.3389\/fmicb.2018.02630","article-title":"Lactobacillus crispatus BC5 Interferes With Chlamydia trachomatis Infectivity Through Integrin Modulation in Cervical Cells","volume":"9","author":"Parolin","year":"2018","journal-title":"Front. Microbiol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"447","DOI":"10.1046\/j.1462-5822.2002.00203.x","article-title":"Identification of MEK- and phosphoinositide 3-kinase-dependent signalling as essential events during Chlamydia pneumoniae invasion of HEp2 cells","volume":"4","author":"Coombes","year":"2002","journal-title":"Cell. Microbiol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"30426","DOI":"10.1074\/jbc.M114.604876","article-title":"The Chlamydia effector TarP mimics the mammalian leucine-aspartic acid motif of paxillin to subvert the focal adhesion kinase during invasion","volume":"289","author":"Thwaites","year":"2014","journal-title":"J. Biol. Chem."},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Foschi, C., Bortolotti, M., Marziali, G., Polito, L., Marangoni, A., and Bolognesi, A. (2019). Survival and death of intestinal cells infected by Chlamydia trachomatis. PLoS ONE, 14.","DOI":"10.1371\/journal.pone.0215956"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"471","DOI":"10.1016\/j.atherosclerosis.2015.05.023","article-title":"Chlamydia pneumoniae acute liver infection affects hepatic cholesterol and triglyceride metabolism in mice","volume":"241","author":"Marangoni","year":"2015","journal-title":"Atherosclerosis"},{"key":"ref_35","first-page":"215","article-title":"Chlamydia trachomatis serovar distribution and other sexually transmitted coinfections in subjects attending an STD outpatients clinic in Italy","volume":"35","author":"Marangoni","year":"2012","journal-title":"New Microbiol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"508","DOI":"10.1021\/bi00570a021","article-title":"Differential polarized phase fluorometric investigations of diphenylhexatriene in lipid bilayers. Quantitation of hindered depolarizing rotations","volume":"18","author":"Lakowicz","year":"1979","journal-title":"Biochemistry"}],"container-title":["Pathogens"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-0817\/9\/4\/298\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,13]],"date-time":"2025-10-13T14:08:59Z","timestamp":1760364539000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-0817\/9\/4\/298"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,4,17]]},"references-count":36,"journal-issue":{"issue":"4","published-online":{"date-parts":[[2020,4]]}},"alternative-id":["pathogens9040298"],"URL":"https:\/\/doi.org\/10.3390\/pathogens9040298","relation":{},"ISSN":["2076-0817"],"issn-type":[{"type":"electronic","value":"2076-0817"}],"subject":[],"published":{"date-parts":[[2020,4,17]]}}}