{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,14]],"date-time":"2026-02-14T11:14:12Z","timestamp":1771067652052,"version":"3.50.1"},"reference-count":124,"publisher":"MDPI AG","issue":"11","license":[{"start":{"date-parts":[[2019,10,30]],"date-time":"2019-10-30T00:00:00Z","timestamp":1572393600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Cells"],"abstract":"<jats:p>Invasive fungal infections (IFI) are an increasing threat to the developing world, with fungal spores being ubiquitous and inhaled every day. Some fungal species are commensal organisms that are part of the normal human microbiota, and, as such, do not pose a threat to the immune system. However, when the natural balance of this association is disturbed or the host\u2019s immune system is compromised, these fungal pathogens overtake the organism, and cause IFI. To understand the invasiveness of these pathogens and to address the growing problem of IFI, it is essential to identify the cellular processes of the invading organism and their virulence. In this review, we will discuss the prevalence and current options available to treat IFI, including recent reports of drug resistance. Nevertheless, the main focus of this review is to describe the glycobiology of human fungal pathogens and how various components of the fungal cell wall, particularly cell wall polysaccharides and glycoconjugates, are involved in fungal pathogenicity, their biosynthesis and how they can be potentially exploited to develop novel antifungal treatment options. We will specifically describe the nucleotide sugar transporters (NSTs) that are important in fungal survival and suggest that the inhibition of fungal NSTs may potentially be useful to prevent the establishment of fungal infections.<\/jats:p>","DOI":"10.3390\/cells8111348","type":"journal-article","created":{"date-parts":[[2019,10,31]],"date-time":"2019-10-31T05:18:26Z","timestamp":1572499106000},"page":"1348","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":17,"title":["Glycobiology of Human Fungal Pathogens: New Avenues for Drug Development"],"prefix":"10.3390","volume":"8","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-2077-5634","authenticated-orcid":false,"given":"Danielle J.","family":"Lee","sequence":"first","affiliation":[{"name":"Institute for Glycomics, Griffith University, Gold Coast Campus, Queensland, 4222, Australia; Member of Fraunhofer International Consortium for Anti-Infective Research (iCAIR), Nikolai-Fuchs Strasse 1, 30625 Hannover, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-9636-2342","authenticated-orcid":false,"given":"Holly","family":"O\u2019Donnell","sequence":"additional","affiliation":[{"name":"Institute for Glycomics, Griffith University, Gold Coast Campus, Queensland, 4222, Australia; Member of Fraunhofer International Consortium for Anti-Infective Research (iCAIR), Nikolai-Fuchs Strasse 1, 30625 Hannover, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7163-0590","authenticated-orcid":false,"given":"Fran\u00e7oise H.","family":"Routier","sequence":"additional","affiliation":[{"name":"Department of Clinical Biochemistry OE4340, Hannover Medical School, Carl-Neuberg-Strasse 1, 30625 Hannover, Germany; Member of Fraunhofer International Consortium for Anti-Infective Research (iCAIR), Nikolai-Fuchs Strasse 1, 30625 Hannover, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Joe","family":"Tiralongo","sequence":"additional","affiliation":[{"name":"Institute for Glycomics, Griffith University, Gold Coast Campus, Queensland, 4222, Australia; Member of Fraunhofer International Consortium for Anti-Infective Research (iCAIR), Nikolai-Fuchs Strasse 1, 30625 Hannover, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-3373-8680","authenticated-orcid":false,"given":"Thomas","family":"Haselhorst","sequence":"additional","affiliation":[{"name":"Institute for Glycomics, Griffith University, Gold Coast Campus, Queensland, 4222, Australia; Member of Fraunhofer International Consortium for Anti-Infective Research (iCAIR), Nikolai-Fuchs Strasse 1, 30625 Hannover, Germany"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2019,10,30]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"2261","DOI":"10.1007\/s00018-015-1860-z","article-title":"Opportunistic yeast pathogens: Reservoirs, virulence mechanisms, and therapeutic strategies","volume":"72","author":"Polvi","year":"2015","journal-title":"Cell. Mol. Life Sci."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1016\/j.bcp.2016.11.019","article-title":"Antifungals","volume":"133","author":"Campoy","year":"2017","journal-title":"Biochem. Pharmacol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"2037","DOI":"10.1099\/mic.0.2008\/017483-0","article-title":"Two GDP-mannose transporters contribute to hyphal form and cell wall integrity in Aspergillus nidulans","volume":"154","author":"Hill","year":"2008","journal-title":"Microbiology"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"70","DOI":"10.1016\/j.mib.2018.02.005","article-title":"Antifungal drug resistance: Evolution, mechanisms and impact","volume":"45","author":"Revie","year":"2018","journal-title":"Curr. Opin. Microbiol."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1007\/s12275-016-0647-8","article-title":"Human fungal pathogens: Why should we learn?","volume":"54","author":"Kim","year":"2016","journal-title":"J. Microbiol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"358","DOI":"10.1016\/j.mib.2009.05.008","article-title":"Hidden killers: Persistence of opportunistic fungal pathogens in the human host","volume":"12","year":"2009","journal-title":"Curr. Opin. Microbiol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"S612","DOI":"10.1093\/cid\/civ791","article-title":"Echinocandin Resistance in Candida","volume":"61","author":"Perlin","year":"2015","journal-title":"Clin. Infect Dis."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1498","DOI":"10.1111\/jam.13301","article-title":"Fungal cell membrane-promising drug target for antifungal therapy","volume":"121","author":"Sant","year":"2016","journal-title":"J. Appl. Microbiol."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Bongomin, F., Gago, S., Oladele, R.O., and Denning, D.W. (2017). Global and Multi-National Prevalence of Fungal Diseases-Estimate Precision. J. Fungi (Basel), 3.","DOI":"10.3390\/jof3040057"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"S3","DOI":"10.1086\/504490","article-title":"Invasive Fungal Pathogens: Current Epidemiological Trends","volume":"43","author":"Pfaller","year":"2006","journal-title":"Clin. Infect. Dis."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"281","DOI":"10.1128\/CMR.17.2.281-310.2004","article-title":"Surface glycans of Candida albicans and other pathogenic fungi: Physiological roles, clinical uses, and experimental challenges","volume":"17","author":"Masuoka","year":"2004","journal-title":"Clin. Microbiol. Rev."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"521","DOI":"10.1086\/432060","article-title":"Emerging fungal diseases","volume":"41","author":"Nucci","year":"2005","journal-title":"Clin. Infect. Dis."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1024","DOI":"10.3389\/fmicb.2017.01024","article-title":"Azole Resistance in Aspergillus fumigatus: A Consequence of Antifungal Use in Agriculture?","volume":"8","author":"Berger","year":"2017","journal-title":"Front. Microbiol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"1567","DOI":"10.2165\/00003495-200767110-00004","article-title":"Invasive aspergillosis: Epidemiology, diagnosis and management in immunocompromised patients","volume":"67","author":"Maschmeyer","year":"2007","journal-title":"Drugs"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"165rv13","DOI":"10.1126\/scitranslmed.3004404","article-title":"Hidden killers: Human fungal infections","volume":"4","author":"Brown","year":"2012","journal-title":"Sci. Transl. Med."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"420","DOI":"10.1111\/myc.12628","article-title":"Improving outcome of fungal diseases\u2014Guiding experts and patients towards excellence","volume":"60","author":"Cornely","year":"2017","journal-title":"Mycoses"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"214","DOI":"10.3389\/fmicb.2019.00214","article-title":"The Still Underestimated Problem of Fungal Diseases Worldwide","volume":"10","author":"Almeida","year":"2019","journal-title":"Front. Microbiol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"26","DOI":"10.3389\/fmicb.2013.00026","article-title":"Receptor-mediated signaling in Aspergillus fumigatus","volume":"4","author":"Grice","year":"2013","journal-title":"Front. Microbiol."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Kohler, J.R., Hube, B., Puccia, R., Casadevall, A., and Perfect, J.R. (2017). Fungi that Infect Humans. Microbiol. Spectr., 5.","DOI":"10.1128\/microbiolspec.FUNK-0014-2016"},{"key":"ref_20","unstructured":"LIFE (2019, May 10). How Common Are Fungal Disease?. Available online: https:\/\/www.fungalinfectiontrust.org\/How%20Common%20are%20Fungal%20Diseases5.pdf."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"284","DOI":"10.1016\/j.tim.2018.01.007","article-title":"Dynamic Fungal Cell Wall Architecture in Stress Adaptation and Immune Evasion","volume":"26","author":"Hopke","year":"2018","journal-title":"Trends Microbiol."},{"key":"ref_22","doi-asserted-by":"crossref","unstructured":"Clark, C., and Drummond, R.A. (2019). The Hidden Cost of Modern Medical Interventions: How Medical Advances Have Shaped the Prevalence of Human Fungal Disease. Pathogens, 8.","DOI":"10.3390\/pathogens8020045"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"719","DOI":"10.1093\/glycob\/cwy030","article-title":"Unraveling synthesis of the cryptococcal cell wall and capsule","volume":"28","author":"Wang","year":"2018","journal-title":"Glycobiology"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.idc.2015.10.004","article-title":"The Global Burden of Fungal Diseases","volume":"30","author":"Vallabhaneni","year":"2016","journal-title":"Infect. Dis. Clin. N. Am."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"107352","DOI":"10.1016\/j.biotechadv.2019.02.008","article-title":"The fungal cell wall as a target for the development of new antifungal therapies","volume":"37","author":"Cortes","year":"2019","journal-title":"Biotechnol. Adv."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"66","DOI":"10.3410\/B2-66","article-title":"Fungal echinocandin resistance","volume":"2","author":"Munro","year":"2010","journal-title":"F1000 Biol. Rep."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1016\/j.ijid.2003.05.001","article-title":"Burden of hospitalization of patients with Candida and Aspergillus infections in Australia","volume":"8","author":"Slavin","year":"2004","journal-title":"Int. J. Infect. Dis."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1791","DOI":"10.1093\/cid\/ciy776","article-title":"Estimation of Direct Healthcare Costs of Fungal Diseases in the United States","volume":"68","author":"Benedict","year":"2019","journal-title":"Clin. Infect. Dis."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"186","DOI":"10.1038\/nature10947","article-title":"Emerging fungal threats to animal, plant and ecosystem health","volume":"484","author":"Fisher","year":"2012","journal-title":"Nature"},{"key":"ref_30","unstructured":"GAFFI (2019, May 13). Fungal Disease Frequency. Available online: https:\/\/www.gaffi.org\/why\/fungal-disease-frequency\/."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"325","DOI":"10.3389\/fmicb.2015.00325","article-title":"The Aspergillus fumigatus cell wall integrity signaling pathway: Drug target, compensatory pathways, and virulence","volume":"6","author":"Valiante","year":"2015","journal-title":"Front. Microbiol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"308","DOI":"10.1111\/j.1751-7915.2008.00070.x","article-title":"The role of the cell wall in fungal pathogenesis","volume":"2","author":"Arana","year":"2009","journal-title":"Microb. Biotechnol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"377","DOI":"10.1146\/annurev-micro-091313-103507","article-title":"Fungal membrane organization: The eisosome concept","volume":"68","author":"Douglas","year":"2014","journal-title":"Annu. Rev. Microbiol."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"e27564","DOI":"10.1002\/pbc.27564","article-title":"Epidemiology of invasive fungal infections in immunocompromised children; an Australian national 10-year review","volume":"66","author":"Bartlett","year":"2019","journal-title":"Pediatr. Blood Cancer"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1146\/annurev.micro.62.081307.162753","article-title":"How sweet it is! Cell wall biogenesis and polysaccharide capsule formation in Cryptococcus neoformans","volume":"63","author":"Doering","year":"2009","journal-title":"Annu. Rev. Microbiol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"776","DOI":"10.1128\/EC.00015-07","article-title":"The pathogenic fungus Cryptococcus neoformans expresses two functional GDP-mannose transporters with distinct expression patterns and roles in capsule synthesis","volume":"6","author":"Cottrell","year":"2007","journal-title":"Eukaryot. Cell"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"e02319-17","DOI":"10.1128\/mBio.02319-17","article-title":"UDP-Glucuronic Acid Transport Is Required for Virulence of Cryptococcus neoformans","volume":"9","author":"Li","year":"2018","journal-title":"MBio"},{"key":"ref_38","unstructured":"CDC (2019, May 13). How Common Are C.neoformans Infection?, Available online: https:\/\/www.cdc.gov\/fungal\/diseases\/cryptococcosis-neoformans\/statistics.html."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"e334","DOI":"10.1016\/S1473-3099(17)30303-1","article-title":"Fungal infections in HIV\/AIDS","volume":"17","author":"Limper","year":"2017","journal-title":"Lancet Infect. Dis."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1007\/s12281-018-0317-x","article-title":"A Call to Action for Mycetoma","volume":"12","author":"Beer","year":"2018","journal-title":"Curr. Fungal Infect. Rep."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"646","DOI":"10.1111\/eci.12448","article-title":"Diagnosis of invasive aspergillosis: Recent developments and ongoing challenges","volume":"45","author":"Arvanitis","year":"2015","journal-title":"Eur. J. Clin. Investig."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"FSO199","DOI":"10.4155\/fsoa-2017-0030","article-title":"Galactofuranose antigens, a target for diagnosis of fungal infections in humans","volume":"3","author":"Marino","year":"2017","journal-title":"Future Sci. OA"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1093\/mmy\/myw134","article-title":"7th Advances Against Aspergillosis: Basic, diagnostic, clinical and therapeutic studies","volume":"55","author":"Cramer","year":"2017","journal-title":"Med. Mycol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1175","DOI":"10.1001\/jama.2017.10661","article-title":"Aspergillus Galactomannan for Diagnosing Invasive Aspergillosis","volume":"318","author":"Miceli","year":"2017","journal-title":"JAMA"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"e1","DOI":"10.1093\/cid\/ciw326","article-title":"Practice Guidelines for the Diagnosis and Management of Aspergillosis: 2016 Update by the Infectious Diseases Society of America","volume":"63","author":"Patterson","year":"2016","journal-title":"Clin. Infect. Dis."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1417","DOI":"10.1086\/503427","article-title":"Diagnosis of invasive aspergillosis using a galactomannan assay: A meta-analysis","volume":"42","author":"Pfeiffer","year":"2006","journal-title":"Clin. Infect. Dis."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"e357","DOI":"10.1016\/S1473-3099(17)30309-2","article-title":"Pulmonary and sinus fungal diseases in non-immunocompromised patients","volume":"17","author":"Denning","year":"2017","journal-title":"Lancet Infect. Dis."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"214","DOI":"10.1016\/j.drudis.2008.11.013","article-title":"Targeting virulence: A new paradigm for antifungals","volume":"14","author":"Gauwerky","year":"2009","journal-title":"Drug Discov. Today"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"333","DOI":"10.1016\/j.ijantimicag.2017.09.002","article-title":"The antifungal arsenal: Alternative drugs and future targets","volume":"51","author":"Wiederhold","year":"2018","journal-title":"Int. J. Antimicrob. Agents"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"739","DOI":"10.1126\/science.aap7999","article-title":"Worldwide emergence of resistance to antifungal drugs challenges human health and food security","volume":"360","author":"Fisher","year":"2018","journal-title":"Science"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"e1","DOI":"10.1016\/j.cmi.2018.01.002","article-title":"Diagnosis and management of Aspergillus diseases: Executive summary of the 2017 ESCMID-ECMM-ERS guideline","volume":"24","author":"Ullmann","year":"2018","journal-title":"Clin. Microbiol. Infect."},{"key":"ref_52","doi-asserted-by":"crossref","unstructured":"Wagener, J., and Loiko, V. (2017). Recent Insights into the Paradoxical Effect of Echinocandins. J. Fungi (Basel), 4.","DOI":"10.3390\/jof4010005"},{"key":"ref_53","first-page":"271","article-title":"Invasive Fungal Infection","volume":"116","author":"Wagener","year":"2019","journal-title":"Dtsch. Arztebl. Int."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"84","DOI":"10.1093\/glycob\/cwm122","article-title":"Glycosylinositolphosphoceramides in Aspergillus fumigatus","volume":"18","author":"Simenel","year":"2008","journal-title":"Glycobiology"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"51869","DOI":"10.1074\/jbc.M405232200","article-title":"GPI7 involved in glycosylphosphatidylinositol biosynthesis is essential for yeast cell separation","volume":"279","author":"Fujita","year":"2004","journal-title":"J. Biol. Chem."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1194\/jlr.R063313","article-title":"Biosynthesis of GPI-anchored proteins: Special emphasis on GPI lipid remodeling","volume":"57","author":"Kinoshita","year":"2016","journal-title":"J. Lipid Res."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"6991","DOI":"10.1021\/bi8006324","article-title":"The glycosylphosphatidylinositol anchor: A complex membrane-anchoring structure for proteins","volume":"47","author":"Paulick","year":"2008","journal-title":"Biochemistry"},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"1132","DOI":"10.1128\/EC.2.5.1132-1136.2003","article-title":"Biosynthesis of glycosylphosphatidylinositol is essential to the survival of the protozoan parasite Toxoplasma gondii","volume":"2","author":"Wichroski","year":"2003","journal-title":"Eukaryot. Cell"},{"key":"ref_59","doi-asserted-by":"crossref","unstructured":"Beauvais, A., and Latge, J.P. (2018). Special Issue: Fungal Cell Wall. J. Fungi (Basel), 4.","DOI":"10.3390\/jof4030091"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"2812","DOI":"10.1002\/1522-2683(200108)22:13<2812::AID-ELPS2812>3.0.CO;2-Q","article-title":"Proteome analysis of Aspergillus fumigatus identifies glycosylphosphatidylinositol-anchored proteins associated to the cell wall biosynthesis","volume":"22","author":"Bruneau","year":"2001","journal-title":"Electrophoresis"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"279","DOI":"10.1111\/j.1365-2958.2007.05872.x","article-title":"The cell wall: A carbohydrate armour for the fungal cell","volume":"66","author":"Latge","year":"2007","journal-title":"Mol. Microbiol."},{"key":"ref_62","first-page":"30","article-title":"Aspergillus fumigatus Cap59-like protein A is involved in alpha1,3-mannosylation of GPI-anchors","volume":"26","author":"Kruger","year":"2016","journal-title":"Glycobiology"},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"44418","DOI":"10.1074\/jbc.M112.398321","article-title":"Biosynthesis of the fungal cell wall polysaccharide galactomannan requires intraluminal GDP-mannose","volume":"287","author":"Engel","year":"2012","journal-title":"J. Biol. Chem."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"e00397-19","DOI":"10.1128\/mSphere.00397-19","article-title":"The Glycosylphosphatidylinositol-Anchored DFG Family Is Essential for the Insertion of Galactomannan into the beta-(1,3)-Glucan-Chitin Core of the Cell Wall of Aspergillus fumigatus","volume":"4","author":"Muszkieta","year":"2019","journal-title":"mSphere"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1080\/mmy.39.1.9.17","article-title":"Aspergillus fumigatus cell wall: Composition and biosynthesis","volume":"39","author":"Bernard","year":"2001","journal-title":"Med. Mycol."},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1128\/microbiolspec.FUNK-0035-2016","article-title":"The Fungal Cell Wall: Structure, Biosynthesis, and Function","volume":"5","author":"Gow","year":"2017","journal-title":"Microbiol. Spectr."},{"key":"ref_67","doi-asserted-by":"crossref","first-page":"456","DOI":"10.1093\/glycob\/cwr144","article-title":"Galactofuranose in eukaryotes: Aspects of biosynthesis and functional impact","volume":"22","author":"Tefsen","year":"2012","journal-title":"Glycobiology"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"S15","DOI":"10.1080\/13693780400029155","article-title":"Specific molecular features in the organization and biosynthesis of the cell wall of Aspergillus fumigatus","volume":"43","author":"Latge","year":"2005","journal-title":"Med. Mycol."},{"key":"ref_69","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1016\/S0065-2164(09)01204-0","article-title":"The capsule of the fungal pathogen Cryptococcus neoformans","volume":"68","author":"Zaragoza","year":"2009","journal-title":"Adv. Appl. Microbiol."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"583","DOI":"10.2217\/fmb.09.29","article-title":"Aspergillus fumigatus: Cell wall polysaccharides, their biosynthesis and organization","volume":"4","author":"Gastebois","year":"2009","journal-title":"Future Microbiol."},{"key":"ref_71","doi-asserted-by":"crossref","first-page":"458","DOI":"10.1111\/mmi.12877","article-title":"Aspergillus fumigatus devoid of cell wall beta-1,3-glucan is viable, massively sheds galactomannan and is killed by septum formation inhibitors","volume":"95","author":"Dichtl","year":"2015","journal-title":"Mol. Microbiol."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"e00619-17","DOI":"10.1128\/mBio.00619-17","article-title":"The Dual Activity Responsible for the Elongation and Branching of beta-(1,3)-Glucan in the Fungal Cell Wall","volume":"8","author":"Aimanianda","year":"2017","journal-title":"MBio"},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"855","DOI":"10.1128\/EC.00399-06","article-title":"Chitosan, the deacetylated form of chitin, is necessary for cell wall integrity in Cryptococcus neoformans","volume":"6","author":"Baker","year":"2007","journal-title":"Eukaryot. Cell"},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.fbr.2016.03.002","article-title":"The importance of subclasses of chitin synthase enzymes with myosin-like domains for the fitness of fungi","volume":"30","author":"Fernandes","year":"2016","journal-title":"Fungal Biol. Rev."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"26","DOI":"10.1128\/EC.05270-11","article-title":"alpha1,3 glucans are dispensable in Aspergillus fumigatus","volume":"11","author":"Henry","year":"2012","journal-title":"Eukaryot. Cell"},{"key":"ref_76","doi-asserted-by":"crossref","unstructured":"Beauvais, A., Bozza, S., Kniemeyer, O., Formosa, C., Balloy, V., Henry, C., Roberson, R.W., Dague, E., Chignard, M., and Brakhage, A.A. (2013). Deletion of the alpha-(1,3)-glucan synthase genes induces a restructuring of the conidial cell wall responsible for the avirulence of Aspergillus fumigatus. PLoS Pathog., 9.","DOI":"10.1371\/annotation\/05c0ca66-4ed9-4c04-96c6-3addac835e04"},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"1385","DOI":"10.1111\/j.1365-2958.2006.05551.x","article-title":"Loss of cell wall alpha(1-3) glucan affects Cryptococcus neoformans from ultrastructure to virulence","volume":"63","author":"Reese","year":"2007","journal-title":"Mol. Microbiol."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1093\/glycob\/cwu091","article-title":"Significant structural change in both O- and N-linked carbohydrate moieties of the antigenic galactomannan from Aspergillus fumigatus grown under different culture conditions","volume":"25","author":"Kudoh","year":"2015","journal-title":"Glycobiology"},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"523","DOI":"10.1016\/j.ijmm.2011.02.003","article-title":"Studies on galactofuranose-containing glycostructures of the pathogenic mold Aspergillus fumigatus","volume":"301","author":"Heesemann","year":"2011","journal-title":"Int. J. Med. Microbiol."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"S104","DOI":"10.1080\/13693780802258832","article-title":"Galactofuranose containing molecules in Aspergillus fumigatus","volume":"47","author":"Latge","year":"2009","journal-title":"Med. Mycol."},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"657","DOI":"10.1515\/BC.2005.076","article-title":"Identification and partial characterization of two eukaryotic UDP-galactopyranose mutases","volume":"386","author":"Bakker","year":"2005","journal-title":"Biol. Chem."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"1147","DOI":"10.1128\/EC.4.6.1147-1154.2005","article-title":"Eukaryotic UDP-galactopyranose mutase (GLF gene) in microbial and metazoal pathogens","volume":"4","author":"Beverley","year":"2005","journal-title":"Eukaryot. Cell"},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"896","DOI":"10.1016\/j.fgb.2011.06.001","article-title":"Roles of the Aspergillus nidulans UDP-galactofuranose transporter, UgtA in hyphal morphogenesis, cell wall architecture, conidiation, and drug sensitivity","volume":"48","author":"Afroz","year":"2011","journal-title":"Fungal Genet. Biol."},{"key":"ref_84","doi-asserted-by":"crossref","unstructured":"Park, J., Tefsen, B., Heemskerk, M.J., Lagendijk, E.L., van den Hondel, C.A., van Die, I., and Ram, A.F. (2015). Identification and functional analysis of two Golgi-localized UDP-galactofuranose transporters with overlapping functions in Aspergillus niger. BMC Microbiol., 15.","DOI":"10.1186\/s12866-015-0541-2"},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"568","DOI":"10.1093\/glycob\/cwx028","article-title":"GfsA is a beta1,5-galactofuranosyltransferase involved in the biosynthesis of the galactofuran side chain of fungal-type galactomannan in Aspergillus fumigatus","volume":"27","author":"Katafuchi","year":"2017","journal-title":"Glycobiology"},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"1268","DOI":"10.1128\/EC.00109-08","article-title":"Contribution of galactofuranose to the virulence of the opportunistic pathogen Aspergillus fumigatus","volume":"7","author":"Schmalhorst","year":"2008","journal-title":"Eukaryot. Cell"},{"key":"ref_87","doi-asserted-by":"crossref","first-page":"1054","DOI":"10.1111\/mmi.12416","article-title":"GfsA encodes a novel galactofuranosyltransferase involved in biosynthesis of galactofuranose antigen of O-glycan in Aspergillus nidulans and Aspergillus fumigatus","volume":"90","author":"Komachi","year":"2013","journal-title":"Mol. Microbiol."},{"key":"ref_88","doi-asserted-by":"crossref","unstructured":"Arentshorst, M., de Lange, D., Park, J., Lagendijk, E.L., Alazi, E., van den Hondel, C., and Ram, A.F.J. (2019). Functional analysis of three putative galactofuranosyltransferases with redundant functions in galactofuranosylation in Aspergillus niger. Arch. Microbiol., 1\u20137.","DOI":"10.1007\/s00203-019-01709-w"},{"key":"ref_89","doi-asserted-by":"crossref","first-page":"e02647-18","DOI":"10.1128\/mBio.02647-18","article-title":"Two KTR Mannosyltransferases Are Responsible for the Biosynthesis of Cell Wall Mannans and Control Polarized Growth in Aspergillus fumigatus","volume":"10","author":"Henry","year":"2019","journal-title":"MBio"},{"key":"ref_90","doi-asserted-by":"crossref","first-page":"16918","DOI":"10.1038\/s41598-018-35059-2","article-title":"Identification of Two Mannosyltransferases Contributing to Biosynthesis of the Fungal-type Galactomannan alpha-Core-Mannan Structure in Aspergillus fumigatus","volume":"8","author":"Onoue","year":"2018","journal-title":"Sci. Rep."},{"key":"ref_91","doi-asserted-by":"crossref","first-page":"501","DOI":"10.1016\/j.micinf.2018.01.011","article-title":"Fungal extracellular vesicles: Modulating host-pathogen interactions by both the fungus and the host","volume":"20","author":"Nimrichter","year":"2018","journal-title":"Microbes Infect"},{"key":"ref_92","doi-asserted-by":"crossref","unstructured":"Li, L.X., Rautengarten, C., Heazlewood, J.L., and Doering, T.L. (2018). Xylose donor transport is critical for fungal virulence. PLoS Pathog., 14.","DOI":"10.1371\/journal.ppat.1006765"},{"key":"ref_93","first-page":"582","article-title":"Distribution of the O-acetyl groups and beta-galactofuranose units in galactoxylomannans of the opportunistic fungus Cryptococcus neoformans","volume":"27","author":"Previato","year":"2017","journal-title":"Glycobiology"},{"key":"ref_94","first-page":"44","article-title":"Editorial: Glycan diversity in fungi, bacteria, and sea organisms","volume":"5","year":"2015","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"ref_95","doi-asserted-by":"crossref","first-page":"626","DOI":"10.1093\/glycob\/cwn044","article-title":"Protein glycosylation pathways in filamentous fungi","volume":"18","author":"Deshpande","year":"2008","journal-title":"Glycobiology"},{"key":"ref_96","doi-asserted-by":"crossref","unstructured":"Tiralongo, J., and Martinez-Duncker, I. (2013). Introduction to sialic acid structure, occurrence, biosynthesis and function. Sialobiology: Structure, Biosynthesis and Function. Sialic Acid Glycoconjugates in Health and Disease, Bentham Science Publishers. [1st ed.].","DOI":"10.2174\/97816080538651130101"},{"key":"ref_97","doi-asserted-by":"crossref","first-page":"4937","DOI":"10.1128\/iai.65.12.4937-4942.1997","article-title":"Identification of N-acetylneuraminic acid and its 9-O-acetylated derivative on the cell surface of Cryptococcus neoformans: Influence on fungal phagocytosis","volume":"65","author":"Rodrigues","year":"1997","journal-title":"Infect. Immun."},{"key":"ref_98","doi-asserted-by":"crossref","first-page":"262","DOI":"10.1016\/S0304-4165(00)00003-9","article-title":"Identification of sialic acids on the cell surface of Candida albicans","volume":"1474","author":"Soares","year":"2000","journal-title":"Biochim. Biophys. Acta"},{"key":"ref_99","doi-asserted-by":"crossref","first-page":"145","DOI":"10.1080\/02681218680000211","article-title":"Identification of sialic acids on the cell surface of hyphae and conidia of the human pathogen Fonsecaea pedrosoi","volume":"24","author":"Souza","year":"1986","journal-title":"J. Med. Vet. Mycol."},{"key":"ref_100","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1111\/j.1574-6968.1993.tb06069.x","article-title":"Identification of sialic acids on the cell surface of hyphae and yeast forms of the human pathogen Paracoccidioides brasiliensis","volume":"108","author":"Soares","year":"1993","journal-title":"FEMS Microbiol. Lett."},{"key":"ref_101","doi-asserted-by":"crossref","first-page":"401","DOI":"10.1093\/glycob\/cwl085","article-title":"Structure and role of sialic acids on the surface of Aspergillus fumigatus conidiospores","volume":"17","author":"Warwas","year":"2007","journal-title":"Glycobiology"},{"key":"ref_102","doi-asserted-by":"crossref","first-page":"3100","DOI":"10.1099\/mic.0.026997-0","article-title":"Inhibition of Aspergillus fumigatus conidia binding to extracellular matrix proteins by sialic acids: A pH effect?","volume":"155","author":"Tiralongo","year":"2009","journal-title":"Microbiology"},{"key":"ref_103","doi-asserted-by":"crossref","first-page":"869","DOI":"10.1099\/00221287-147-4-869","article-title":"Differences in sialic acid density in pathogenic and non-pathogenic Aspergillus species","volume":"147","author":"Wasylnka","year":"2001","journal-title":"Microbiology"},{"key":"ref_104","doi-asserted-by":"crossref","unstructured":"Speth, C., Rambach, G., Lass-Florl, C., Howell, P.L., and Sheppard, D.C. (2019). Galactosaminogalactan (GAG) and its multiple roles in Aspergillus pathogenesis. Virulence, 1\u20138.","DOI":"10.1080\/21505594.2019.1568174"},{"key":"ref_105","first-page":"145","article-title":"Fungal glycans and the innate immune recognition","volume":"4","author":"Figueiredo","year":"2014","journal-title":"Front. Cell. Infect. Microbiol."},{"key":"ref_106","doi-asserted-by":"crossref","unstructured":"Samar, D., Kieler, J.B., and Klutts, J.S. (2015). Identification and deletion of Tft1, a predicted glycosyltransferase necessary for cell wall beta-1,3;1,4-glucan synthesis in Aspergillus fumigatus. PLoS ONE, 10.","DOI":"10.1371\/journal.pone.0117336"},{"key":"ref_107","doi-asserted-by":"crossref","first-page":"805","DOI":"10.1021\/ar0400239","article-title":"Nucleotide sugar transporters of the Golgi apparatus: From basic science to diseases","volume":"39","author":"Caffaro","year":"2006","journal-title":"Acc. Chem. Res."},{"key":"ref_108","doi-asserted-by":"crossref","first-page":"1149","DOI":"10.1590\/S0100-879X2006000900002","article-title":"Nucleotide-sugar transporters: Structure, function and roles in vivo","volume":"39","author":"Handford","year":"2006","journal-title":"Braz. J. Med. Biol. Res."},{"key":"ref_109","doi-asserted-by":"crossref","first-page":"3150","DOI":"10.1016\/j.jmb.2016.05.021","article-title":"Overview of Nucleotide Sugar Transporter Gene Family Functions Across Multiple Species","volume":"428","author":"Orellana","year":"2016","journal-title":"J. Mol. Biol."},{"key":"ref_110","doi-asserted-by":"crossref","first-page":"521","DOI":"10.1038\/nature24464","article-title":"Structural basis of nucleotide sugar transport across the Golgi membrane","volume":"551","author":"Parker","year":"2017","journal-title":"Nature"},{"key":"ref_111","doi-asserted-by":"crossref","first-page":"127","DOI":"10.1016\/j.sbi.2019.03.019","article-title":"Gateway to the Golgi: Molecular mechanisms of nucleotide sugar transporters","volume":"57","author":"Parker","year":"2019","journal-title":"Curr. Opin. Struct. Biol."},{"key":"ref_112","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1016\/j.csbj.2014.05.003","article-title":"Structure and function of nucleotide sugar transporters: Current progress","volume":"10","author":"Hadley","year":"2014","journal-title":"Comput. Struct. Biotechnol. J."},{"key":"ref_113","doi-asserted-by":"crossref","first-page":"832","DOI":"10.1128\/EC.00054-14","article-title":"Cryptococcus neoformans dual GDP-mannose transporters and their role in biology and virulence","volume":"13","author":"Wang","year":"2014","journal-title":"Eukaryot. Cell"},{"key":"ref_114","doi-asserted-by":"crossref","first-page":"542","DOI":"10.1016\/S0959-440X(00)00128-7","article-title":"Nucleotide sugar transporters of the Golgi apparatus","volume":"10","author":"Berninsone","year":"2000","journal-title":"Curr. Opin. Struct. Biol."},{"key":"ref_115","doi-asserted-by":"crossref","first-page":"24600","DOI":"10.1074\/jbc.M110.134544","article-title":"Inhibition of Golgi apparatus glycosylation causes endoplasmic reticulum stress and decreased protein synthesis","volume":"285","author":"Xu","year":"2010","journal-title":"J. Biol. Chem."},{"key":"ref_116","doi-asserted-by":"crossref","first-page":"5687","DOI":"10.1242\/jcs.01491","article-title":"Localization of GDP-mannose transporter in the Golgi requires retrieval to the endoplasmic reticulum depending on its cytoplasmic tail and coatomer","volume":"117","author":"Abe","year":"2004","journal-title":"J. Cell Sci."},{"key":"ref_117","doi-asserted-by":"crossref","first-page":"600","DOI":"10.1016\/j.semcdb.2010.02.002","article-title":"The role of nucleotide sugar transporters in development of eukaryotes","volume":"21","author":"Liu","year":"2010","journal-title":"Semin. Cell. Dev. Biol."},{"key":"ref_118","doi-asserted-by":"crossref","first-page":"1123","DOI":"10.1016\/j.csbj.2019.08.002","article-title":"Nucleotide Sugar Transporter SLC35 Family Structure and Function","volume":"17","author":"Hadley","year":"2019","journal-title":"Comput. Struct. Biotechnol. J."},{"key":"ref_119","doi-asserted-by":"crossref","first-page":"305","DOI":"10.3852\/09-138","article-title":"GDP-mannose transporter paralogues play distinct roles in polarized growth of Aspergillus nidulans","volume":"102","author":"Hill","year":"2010","journal-title":"Mycologia"},{"key":"ref_120","doi-asserted-by":"crossref","first-page":"1612","DOI":"10.1111\/j.1462-5822.2009.01352.x","article-title":"Galactofuranose attenuates cellular adhesion of Aspergillus fumigatus","volume":"11","author":"Lamarre","year":"2009","journal-title":"Cell. Microbiol."},{"key":"ref_121","doi-asserted-by":"crossref","first-page":"33859","DOI":"10.1074\/jbc.M109.070219","article-title":"A single UDP-galactofuranose transporter is required for galactofuranosylation in Aspergillus fumigatus","volume":"284","author":"Engel","year":"2009","journal-title":"J. Biol. Chem."},{"key":"ref_122","doi-asserted-by":"crossref","first-page":"10994","DOI":"10.1074\/jbc.M112.441998","article-title":"Unusual galactofuranose modification of a capsule polysaccharide in the pathogenic yeast Cryptococcus neoformans","volume":"288","author":"Heiss","year":"2013","journal-title":"J. Biol. Chem."},{"key":"ref_123","doi-asserted-by":"crossref","first-page":"1601","DOI":"10.1128\/EC.3.6.1601-1608.2004","article-title":"UGD1, encoding the Cryptococcus neoformans UDP-glucose dehydrogenase, is essential for growth at 37 degrees C and for capsule biosynthesis","volume":"3","author":"Moyrand","year":"2004","journal-title":"Eukaryot. Cell."},{"key":"ref_124","doi-asserted-by":"crossref","first-page":"51669","DOI":"10.1074\/jbc.M408889200","article-title":"UDP-glucose dehydrogenase plays multiple roles in the biology of the pathogenic fungus Cryptococcus neoformans","volume":"279","author":"Griffith","year":"2004","journal-title":"J. Biol. Chem."}],"container-title":["Cells"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4409\/8\/11\/1348\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T13:30:25Z","timestamp":1760189425000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4409\/8\/11\/1348"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2019,10,30]]},"references-count":124,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2019,11]]}},"alternative-id":["cells8111348"],"URL":"https:\/\/doi.org\/10.3390\/cells8111348","relation":{},"ISSN":["2073-4409"],"issn-type":[{"value":"2073-4409","type":"electronic"}],"subject":[],"published":{"date-parts":[[2019,10,30]]}}}