Adhesins in the virulence of opportunistic fungal pathogens of human

Figures & data

Table 1. List of characterised adhesins from opportunistic fungal pathogens

Fungus	Adhesin	Morphotype	Ligand	References
Aspergillus fumigatus	RodA	Conidia	Collagen	Thau et al. (1994)
	37 and 72-kDa proteins	Conidia	Laminin	Tronchin et al. (1997)
	32-kDa protein	Conidia	Fucose	Mendes-Giannini et al. (2000)
	Mp1 (Galactomannoprotein)	Swollen conidia	ECM	Upadhyay et al. (2008)
	Extracellular Thaumatin domain protein (AfCalAp)	Swollen conidia	Laminin, Fibrinogen, Mice Lung cells	Upadhyay et al. (2009); Liu et al.(2016)
	Hydrophobins	Conidia	ECM	Abad et al. (2010)
	CspA	Conidia	ECM	Levdansky et al. (2010)
	Alpha-mannosidase	Swollen conidia	Fibrinogen	Upadhyay et al.(2012)
	Amidase familyprotein, putative
	Beta-glucosidase, putative
	Hypothetical protein
	Pectate lyase A
	Oryzin precursor (Alkaline proteinase) (Elastase)
A. niger	HF-extractable cell wall putative GPI-anchored mannoprotein – cwpA	Conidia	ECM	Damveld et al. (2005)
Blastomyces dermatitidis	120-kDa protein (WI1)/BAD1g	Yeast form	ECM proteins	Brandhorst et al. (1999)
Candida albicans	55- and 105-kDa proteins	Yeast form	Fibronectin (RGD domain)	Sa et al. (1992)
	37-kDa	Yeast form	Laminin	Lo´pez-Ribot et al. (1994)
	60- and 105-kDa glycoproteins	Yeast form	Fibronectin	Klotz et al.(1994)
	68-, 62- and 60-kDa proteins	Yeast form	Laminin	Lo´pez-Ribot et al. (1994)
	Glyceraldehyde-3-phosphate dehydrogenase (GAPDH)	Yeast form	fibronectin and laminin	Gil-Navarro et al. (1997); Gozalbo et al. (1998)
	Als1p, Ala1p/Als5p	Yeast form	ECM proteins	Sundstrom (1999)
	Hwp1	Yeast form	Mammalian transglutaminases	Staab et al. (1999)
	EAP1g	Yeast form	Epithelial cells	Li and Palecek (2003)
	Int1	Yeast form	ECM proteins	de Groot et al. 2004; Zhao et al. 2004
	ALS (Als 1p-Als9p),	Yeast form	ECM proteins	de Groot et al. 2004; Zhao et al. 2004
	EPA and GPI dependent CWPs	Yeast form	ECM proteins	de Groot et al. 2004; Zhao et al. 2004
	CaIff4	Yeast form	Epithelial cells; Plastic surface	Kempf et al. 2007
	Alcohol dehydrogenase (Adh1)	hyphae	Vitronectin, fibronectin, laminin	Kozik et al. 2015
	Phosphoglycerate mutase (Gpm1)	hyphae	Vitronectin	Kozik et al. 2015
Candida glabrata	Epa1p/EPA1g	Yeast form	Host-cell carbohydrates	Cormack et al. 1999
Candida tropicalis	Surface expressed integrin analogue (putative fibronectin receptor)	Yeast form	Fibronectin	Cm and Hostetter 1993
	105-kDa surface expressed fibronectin-binding protein	Yeast form	ECM proteins	Gp and Hostetter 1996
	Fibronectin-binding proteins gi|255722,852 gi|255,728,333 gi|255,727,881 gi|255,732,698 gi|255,722,021	Pseudohyphae	fibrinogen	Kozik et al. 2015
	Vitronectin-binding proteins gi|255,722,852 gi|240,134,900 gi|255,728,333 gi|255,727,881 gi|255,732,698 gi|255,722,021	Pseudohyphae	Vitronectin	Kozik et al. 2015
	Laminin-binding proteins gi|255,722,852 gi|240,134,900 gi|255,728,333 gi|240,132,975 gi|255,727,881 gi|255,732,698 gi|255,722,021	Pseudohyphae	Laminin	Kozik et al. 2015
Candida parapsilosis	Surface Als like proteins	Pseudohyphae	ECM proteins	Kozik et al. 2015
	Fibronectin-binding proteins gi|354,547,941, gi|354,547,939 gi|354,547,813 gi|354,545,198 gi|354,545,113 gi|354,544,475 gi|354,546,116 gi|354,545,980 gi|354,546,805	Pseudohyphae	Fibronectin	Kozik et al. 2015
	Vitronectin-binding protein gi|8,927,048 gi|354,545,198 gi|354,545,113 gi|354,544,475 gi|354,546,116 gi|354,545,980 gi|354,546,348 gi|354,545,888	Pseudohyphae	Vitronectin	Kozik et al. 2015
	Laminin-binding proteins gi|354,547,939 gi|354,545,113 gi|354,544,475 gi|354,546,805	Pseudohyphae	Laminin	Kozik et al. 2015
Cryptococcus neoformans	MP 15, 98, 88 and 84 kDa proteins	Yeast cells	Lung epithelial cells	Teixeira et al. 2014
	Cfl1	Hyphae	Plastic surface	Wang et al. 2012
Coccidioides immitis	SOWgpg/rSOWp	Parasitic phase	ECM proteins	Hung et al. 2002
Fusarium oxysporum	β-1,6 glycosyated GPI-CWP -Fem1p (60-kDa)	Microconidia	ECM	Schoffelmeer et al. 2001
Fonsecaea pedrosoi	50-kDa protein	Conidia	Manose and N-acetilglycosamine	Limongi et al. 2001
Histoplasma capsulatum	50-kDa protein	Yeast cells	Laminin	McMahon et al. 1995
	Heat shock protein (Hsp60)	Yeast cells	CD18 receptors on Macrophage cells, CHO cells	Long et al. 2003
Metarhizium anisopliae	MAD1 and MAD2	Conidia	ECM	Wang et al. 2007
Penicillium marneffei	20-kDa protein	conidia	Laminin and Fibronectin	Hamilton et al. 1998
	Cell Wall Mannoprotein Mp1p (58-kDa)	Yeast cells	Concanavalin A (a type of lectin purified from jack beans, binds with mannse residues of glycoproteins)	Cao et al. 1998
	Glyceraldehyde-3-phosphate dehydrogenase (GAPDH)	Conidia	A549 pneumocytes, fibronectin and laminin	Lau et al. 2013
Phytophthora cinnamomi	220 kDa-proteins with thrombospondin type 1 repeats	Zoospores	ECM	Robold and Hardham 2005
Paracoccidioides brasiliensis	30-kDa; 19- and 32-kDa proteins	Yeast cells	Laminin and ECM proteins	Andreotti et al. 2005
	Glyceraldehyde-3-phosphate dehydrogenase (GAPDH)	Yeast cells	fibronectin, laminin, and type I collagen	Barbosa et al. 2006
	43-kDa protein	Yeast cells	Laminin	Vicentini et al. 1994
	Pb 14-3-3 protein	Yeast phase	S. cerevisiae cells expressing Pb 14-3-3 adhere to epithelial cell-line A549	de Oliveira et al. 2015
Pseudallescheria boydii	Peptidorhamnomannan (PRM)	Conidia	HEp2 cells (human larynx carcinoma cells)	Pinto et al. 2004
Pneumocystis jirovecii	Msg protein	Yeast cells	A549 cell-line	Kutty et al. 2013
Rhizopus oryzae	Conidial surface adhesins	Spores and germ tube	HUVECs, ECM proteins, endothelial cells	Ibrahim et al. 2005
Sporothrix schenckii	Cell wall proteins with MW 90 and 135 kDa	Yeast cells	Human umbilical vein endothelial cells (HUVECs)	Figueiredo et al. 2004
	Gp70, Unidentified proteins in 37–92 kDa range	Yeast cells	Fibronectin	Teixeira et al. 2009
	Gp70 glycoprotein	conidia	Dermis of mouse tail	Ruiz-Baca et al. 2009
	Cell surface glycoconjugates with carbohydrate or peptide moieties	Yeast and conidia	Fibronectin	Lima et al. 2001
	Cell wall proteins with MW ≥ 190, 180, 115, 90 and 80 kDa	Yeast form	Epithelial cells	Sandoval-Bernal et al. 2011
Trichophyton mentagrophytes	Carbohydrate specific adhesins on microconidial surface	Microconidia	Mannose residues on Chinese hamster ovary (CHO) cells	Esquenazi et al. 2003
Trichophyton rubrum	Lectin-like adhesins on microconidial surface	Microconidia	CHO cells, epithelial and macrophages cells.	D. Esquenazi et al. 2004

Figure 1. Estimated global burden of fungal diseases annually (in millions)

Figure 2. Extracellular matrix (ECM) accessible at the damaged epithelial sites facilitate more pronounced adhesion of fungal morphotypes to host-tissue(s)

Figure 3. Combination of host and pathogen factors determine the tissue tropism of fungal pathogens

Figure 4. Various phases of biofilm formation by fungi

Thau N, Monod M, Crestani B, Rolland C, Tronchin G, Latgé JP, Paris S. 1994. rodletless mutants of aspergillus fumigatus. Infect Immun. 62(10):4380–4388. doi:https://doi.org/10.1128/IAI.62.10.4380-4388.1994.

 PubMed Web of Science ®Google Scholar

Tronchin G, Esnault K, Renier G, Filmon R, Chabasse D, Bouchara JP. 1997. Expression and identification of a laminin-binding protein in aspergillus fumigatus conidia. Infect Immun. 65(1):9–15. doi:https://doi.org/10.1128/IAI.65.1.9-15.1997.

 PubMedGoogle Scholar

Mendes-Giannini MJ, Taylor ML, Bouchara JB, Burger E, Calich VL, Escalante ED, Hanna SA, Lenzi HL, Machado MP, Miyaji M, et al. 2000. Pathogenesis II: fungal responses to host responses: interaction of host cells with fungi. Medical Mycology. 38(Suppl s1):113–123. doi:https://doi.org/10.1080/mmy.38.s1.113.123.

 PubMed Web of Science ®Google Scholar

Upadhyay SK, Basir SF & Madan T. 2008. Characterization of cell wall galactomannoprotein (Mp1) as a potential adhesin of Aspergillus fumigatus. Journal of Allergy and Clinical Immunology, 121(2), S14.

 Web of Science ®Google Scholar

Upadhyay SK, Mahajan L, Ramjee S, Singh Y, Basir SF, Madan T. 2009. Identification and characterization of a laminin-binding protein of aspergillus fumigatus: extracellular thaumatin domain protein (AfCalAp). J Med Microbiol. 58(6):714–722. doi:https://doi.org/10.1099/jmm.0.005991-0.

 PubMed Web of Science ®Google Scholar

Liu H, Lee MJ, Solis NV, Phan QT, Swidergall M, Ralph B, Filler SG. 2016. Aspergillus fumigatus CalA binds to integrin α 5 β 1 and mediates host cell invasion. Nature Microbiology. 2(2):1–10.

 Web of Science ®Google Scholar

Abad A, Jv F-M, Bikandi J, Ramírez A, Margareto J, Sendino J, Fl H, Pontón J, Garaizar J, Rementeria A. 2010. What makes aspergillus fumigatus a successful pathogen? genes and molecules involved in invasive aspergillosis. Rev Iberoam Micol. 27(4):155–182.

 PubMed Web of Science ®Google Scholar

Levdansky E, Kashi O, Sharon H, Shadkchan Y, Osherov N. 2010. The aspergillus fumigatus cspA gene encoding a repeat-rich cell wall protein is important for normal conidial cell wall architecture and interaction with host cells. Eukaryotic Cell. 9(9):1403–1415. doi:https://doi.org/10.1128/EC.00126-10.

 PubMedGoogle Scholar

Damveld RA, Arentshorst M, VanKuyk PA, Klis FM, van den Hondel CA, Ram AF. 2005. Characterisation of CwpA, a putative glycosylphosphatidylinositol-anchored cell wall mannoprotein in the filamentous fungus aspergillus niger. Fungal Genetics and Biology : FG & B. 42(10):873–885. doi:https://doi.org/10.1016/j.fgb.2005.06.006.

 PubMed Web of Science ®Google Scholar

Brandhorst TT, Wüthrich M, Warner T, Klein B. 1999. Targeted gene disruption reveals an adhesin indispensable for pathogenicity of blastomyces dermatitidis. J Exp Med. 189(8):1207–1216. doi:https://doi.org/10.1084/jem.189.8.1207.

 PubMed Web of Science ®Google Scholar

Sa K, RL S, BW S. 1992. Effect of an arginine-glycine-aspartic acid-containing peptide on hematogenous candidal infections in rabbits. Antimicrob Agents Chemother. 36(1):132–136. doi:https://doi.org/10.1128/AAC.36.1.132.

 PubMedGoogle Scholar

López-Ribot JL, Casanova M, Monteagudo C, Sepúlveda P, Martínez JP. 1994. Evidence for the presence of a high-affinity laminin receptor-like molecule on the surface of Candida albicans yeast cells. Infection and Immunity. 62(2):742–6. doi: https://doi.org/10.1128/iai.62.2.742-746.1994. PMID: 8300236; PMCID: PMC186171.

 Google Scholar

Klotz SA, Hein RC, Smith RL, & Rouse JB. 1994. The fibronectin adhesin of Candida albicans. Infection and immunity. 62(10):4679–4681.

 PubMed Web of Science ®Google Scholar

Gil-Navarro I, Gil ML, Casanova M, O'Connor JE, Martinez JP & Gozalbo D. 1997. The glycolytic enzyme glyceraldehyde-3-phosphate dehydrogenase of Candida albicans is a surface antigen. Journal of Bacteriology, 179(16), 4992–4999.

 Google Scholar

Gozalbo D, Gil-Navarro I, Azorín I, Renau-Piqueras J, Martínez JP, Gil ML. 1998. The cell wall-associated glyceraldehyde-3-phosphate dehydrogenase of candida albicans is also a fibronectin and laminin binding protein. Infect Immun. 66(5):2052–2059. doi:https://doi.org/10.1128/IAI.66.5.2052-2059.1998.

 PubMed Web of Science ®Google Scholar

Sundstrom P. 1999. Adhesins in candida albicans. Curr Opin Microbiol. 2(4):353–357. doi:https://doi.org/10.1016/S1369-5274(99)80062-9.

 PubMedGoogle Scholar

Staab JF, Bradway SD, Fidel PL, Sundstrom P. 1999. Adhesive and mammalian transglutaminase substrate properties of candida albicans Hwp1. Science (New York, N Y). 283(5407):1535–1538. doi:https://doi.org/10.1126/science.283.5407.1535.

 PubMed Web of Science ®Google Scholar

Li F, Palecek SP. 2003. EAP1, a candida albicans gene involved in binding human epithelial cells. Eukaryotic Cell. 2(6):1266–1273. doi:https://doi.org/10.1128/EC.2.6.1266-1273.2003.

 PubMedGoogle Scholar

de Groot PW, De Boer AD, Cunningham J, Dekker HL, de Jong L, Hellingwerf KJ, de Koster C, Klis FM. 2004. Proteomic analysis of candida albicans cell walls reveals covalently bound carbohydrate-active enzymes and adhesins. Eukaryotic Cell. 3(4):955–965. doi:https://doi.org/10.1128/EC.3.4.955-965.2004.

 PubMedGoogle Scholar

Zhao X, Oh SH, Cheng G, Green CB, Nuessen JA, Yeater K, Leng RP, Brown A, Hoyer LL. 2004. ALS3 and ALS8 represent a single locus that encodes a candida albicans adhesin; functional comparisons between Als3p and Als1p. Microbiology (Reading, England). 150(8):2415–2428. doi:https://doi.org/10.1099/mic.0.26943-0.

 PubMed Web of Science ®Google Scholar

Kempf M, Apaire-Marchais V, Saulnier P, Licznar P, Lefrançois C, Robert R, Cottin J. 2007. Disruption of candida albicans IFF4 gene involves modifications of the cell electrical surface properties. Colloids Surf B Biointerfaces. 58(2):250–255. doi:https://doi.org/10.1016/j.colsurfb.2007.03.017.

 PubMed Web of Science ®Google Scholar

Kozik A, Karkowska-Kuleta J, Zajac D, Bochenska O, Kedracka-Krok S, Jankowska U, Rapala-Kozik M. 2015. Fibronectin-, vitronectin- and laminin-binding proteins at the cell walls of candida parapsilosis and candida tropicalis pathogenic yeasts. BMC Microbiol. 15(1):197. doi:https://doi.org/10.1186/s12866-015-0531-4.

 PubMed Web of Science ®Google Scholar

Cormack BP, Ghori N, Falkow S. 1999. An adhesin of the yeast pathogen candida glabrata mediating adherence to human epithelial cells. Science (New York, N Y). 285(5427):578–582. doi:https://doi.org/10.1126/science.285.5427.578.

 PubMed Web of Science ®Google Scholar

Cm B, Hostetter MK. 1993. Distinct mechanisms of epithelial adhesion for candida albicans and candida tropicalis.Identification of the participating ligands and development of inhibitory peptides. J Clin Invest. 92(4):1840–1849. doi:https://doi.org/10.1172/JCI116775.

 PubMed Web of Science ®Google Scholar

Gp D, Hostetter MK. 1996. Evidence for a beta 1 integrin fibronectin receptor in candida tropicalis. J Infect Dis. 174(1):127–132. doi:https://doi.org/10.1093/infdis/174.1.127.

 PubMed Web of Science ®Google Scholar

Teixeira PA, Penha LL, Mendonça-Previato L, Previato JO. 2014. Mannoprotein MP84 mediates the adhesion of cryptococcus neoformans to epithelial lung cells. Front Cell Infect Microbiol. 4:106. doi:https://doi.org/10.3389/fcimb.2014.00106.

 PubMedGoogle Scholar

Wang L, Zhai B, Lin X. 2012. The link between morphotype transition and virulence in cryptococcus neoformans. PLoS Pathog. 8(6):e1002765. doi:https://doi.org/10.1371/journal.ppat.1002765.

 PubMedGoogle Scholar

Hung CY, Yu JJ, Seshan KR, Reichard U, Cole GT. 2002. A parasitic phase-specific adhesin of coccidioides immitis contributes to the virulence of this respiratory fungal pathogen. Infect Immun. 70(7):3443–3456. doi:https://doi.org/10.1128/IAI.70.7.3443-3456.2002.

 PubMed Web of Science ®Google Scholar

Schoffelmeer EA, Vossen JH, Van Doorn AA, Cornelissen BJ, Haring MA. 2001. FEM1, a Fusarium oxysporum glycoprotein that is covalently linked to the cell wall matrix and is conserved in filamentous fungi. Molecular Genetics and Genomics: MGG. 265(1):143–152.

 PubMed Web of Science ®Google Scholar

Limongi CL, Alviano CS, De Souza W, Rozental S. 2001. Isolation and partial characterization of an adhesin from fonsecaea pedrosoi. Medical Mycology. 39(5):429–437. doi:https://doi.org/10.1080/mmy.39.5.429.437.

 PubMed Web of Science ®Google Scholar

McMahon JP, Wheat J, Sobel ME, Pasula R, Downing JF, Martin WJ 2nd.1995. Murine laminin binds to Histoplasma capsulatum. A possible mechanism of dissemination. J Clin Invest. 96(2):1010–7. doi: https://doi.org/10.1172/JCI118086. PMID: 7635937; PMCID: PMC286381

 Google Scholar

Long KH, Gomez FJ, Morris RE, Newman SL. 2003. Identification of heat shock protein 60 as the ligand on histoplasma capsulatum that mediates binding to CD18 receptors on human macrophages. Journal of Immunology (Baltimore, Md : 1950). 170(1):487–494. doi:https://doi.org/10.4049/jimmunol.170.1.487.

 PubMed Web of Science ®Google Scholar

Wang Y, Liu T, Gong H, Zhou Q, Wang Y, Sun S, Xie L. 2007. Gene profiling in murine corneas challenged with aspergillus fumigatus. Mol Vis. 13:1226–1233.

 PubMed Web of Science ®Google Scholar

Hamilton AJ, Jeavons L, Youngchim S, Vanittanakom N, Hay RJ. 1998. Sialic Acid-dependent recognition of Laminin byPenicillium marneffei conidia. Infect Immun. 66(10):6024–6026. doi:https://doi.org/10.1128/IAI.66.12.6024-6026.1998.

 PubMed Web of Science ®Google Scholar

Cao L, Chan CM, Lee C, Wong SS, Yuen KY. 1998. MP1 encodes an abundant and highly antigenic cell wall mannoprotein in the pathogenic fungus penicillium marneffei. Infect Immun. 66(3):966–973. doi:https://doi.org/10.1128/IAI.66.3.966-973.1998.

 PubMed Web of Science ®Google Scholar

Lau SK, Tse H, Chan JS, Zhou AC, Curreem SO, Lau CC, Yuen KY, Woo PC. 2013. Proteome profiling of the dimorphic fungus penicillium marneffei extracellular proteins and identification of glyceraldehyde-3-phosphate dehydrogenase as an important adhesion factor for conidial attachment. FEBS J. 280(24):6613–6626. doi:https://doi.org/10.1111/febs.12566.

 PubMed Web of Science ®Google Scholar

Robold AV, Hardham AR. 2005. During attachment phytophthora spores secrete proteins containing thrombospondin type 1 repeats. Curr Genet. 47(5):307–315. doi:https://doi.org/10.1007/s00294-004-0559-8.

 PubMed Web of Science ®Google Scholar

Andreotti PF, Monteiro da Silva JL, Am B, Cm S, Benard G, Cp S, MJ M-G. 2005. Isolation and partial characterization of a 30 kDa adhesin from paracoccidioides brasiliensis. Microbes and Infection. 7(5–6):875–881. doi:https://doi.org/10.1016/j.micinf.2005.02.005.

 PubMed Web of Science ®Google Scholar

Barbosa MS, Báo SN, Andreotti PF, de Faria FP, Felipe MS, dos Santos Feitosa L, MJ M-G, Cm S. 2006. Glyceraldehyde-3-phosphate dehydrogenase of paracoccidioides brasiliensis is a cell surface protein involved in fungal adhesion to extracellular matrix proteins and interaction with cells. Infect Immun. 74(1):382–389. doi:https://doi.org/10.1128/IAI.74.1.382-389.2006.

 PubMed Web of Science ®Google Scholar

Vicentini AP, Gesztesi JL, Franco MF, de Souza W, de Moraes JZ, Travassos LR, Lopes JD. 1994. Binding of paracoccidioides brasiliensis to laminin through surface glycoprotein gp43 leads to enhancement of fungal pathogenesis. Infect Immun. 62(4):1465–1469. doi:https://doi.org/10.1128/IAI.62.4.1465-1469.1994.

 PubMedGoogle Scholar

de Oliveira HC, JDF DS, Scorzoni L, Marcos CM, Rossi SA, Ac DPES, Pa A, Ra DS, Fusco-Almeida AM, Mendes-Giannini MJ. 2015. Importance of adhesins in virulence of paracoccidioides spp. Front Microbiol. 6:303.

 PubMed Web of Science ®Google Scholar

Pinto MR, de Sá AC, Limongi CL, Rozental S, Santos AL, Barreto-Bergter E. 2004. Involvement of peptidorhamnomannan in the interaction of pseudallescheria boydii and HEp2 cells. Microbes and Infection. 6(14):1259–1267. doi:https://doi.org/10.1016/j.micinf.2004.07.006.

 PubMed Web of Science ®Google Scholar

Kutty G, England KJ, & Kovacs JA. 2013. Expression of Pneumocystis jirovecii major surface glycoprotein in Saccharomyces cerevisiae. The Journal of infectious diseases, 208(1), 170–179. doi:https://doi.org/10.1093/infdis/jit131.

 Google Scholar

Ibrahim AS, Spellberg BJ, Avenissian V, Fu Y, Filler SG, Edwards JE. 2005. Vaccination with recombinant N-terminal domain of Als1p improves survival during murine disseminated candidiasis by enhancing cell-mediated, not humoral, immunity. Infect Immun. 73(2):999–1005. doi:https://doi.org/10.1128/IAI.73.2.999-1005.2005.

 PubMed Web of Science ®Google Scholar

Lima OC, Figueiredo CC, Previato JO, Mendonça-Previato L, Morandi V, Lopes Bezerra LM. 2001. Involvement of fungal cell wall components in adhesion of sporothrix schenckii to human fibronectin. Infect Immun. 69(11):6874–6880. doi:https://doi.org/10.1128/IAI.69.11.6874-6880.2001.

 PubMed Web of Science ®Google Scholar

Esquenazi D, De Souza W, Sales Alviano C, Rozental S. 2003. The role of surface carbohydrates on the interaction of microconidia of trichophyton mentagrophytes with epithelial cells. FEMS Immunol Med Microbiol. 35(2):113–123. doi:https://doi.org/10.1016/S0928-8244(03)00007-5.

 PubMedGoogle Scholar

Esquenazi D, Alviano CS, de Souza W, Rozental S. 2004. The influence of surface carbohydrates during in vitro infection of mammalian cells by the dermatophyte trichophyton rubrum. Res Microbiol. 155(3):144–153. doi:https://doi.org/10.1016/j.resmic.2003.12.002.

 PubMed Web of Science ®Google Scholar