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Scedosporium Cell Wall: From Carbohydrate-Containing Structures to Host–Pathogen Interactions

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Abstract

Scedosporium species are filamentous fungi usually found in sewage and soil from human-impacted areas. They cause a wide range of diseases in humans, from superficial infections, such as mycetoma, to invasive and disseminated cases, especially associated in immunocompromised patients. Scedosporium species are also related to lung colonization in individuals presenting cystic fibrosis and are considered one of the most frequent fungal pathogens associated to this pathology. Scedosporium cell wall contains glycosylated molecules involved in important biological events related to virulence and pathogenicity and represents a significant source of antigens. Polysaccharides, peptidopolysaccharides, O-linked oligosaccharides and glycosphingolipids have been identified on the Scedosporium surface. Their primary structures were determined based on a combination of techniques including gas chromatography, ESI-MS, and 1H and 13C nuclear magnetic resonance. Peptidorhamnnomannans are common cell wall components among Scedosporium species. Comparing different species, minor structural differences in the carbohydrate portions were detected which could be useful to understand variations in virulence observed among the species. N- and O-linked peptidorhamnomannans are major pathogen-associated molecular patterns and, along with α-glucans, play important roles in triggering host innate immunity. Glycosphingolipids, such as glucosylceramides, have highly conserved structures in Scedosporium species and are crucial for fungal growth and virulence. The present review presents current knowledge on structural and functional aspects of Scedosporium glycoconjugates that are relevant for understanding pathogenicity mechanisms and could contribute to the design of new agents capable of inhibiting growth and differentiation of Scedosporium species. Other cell components such as melanin and ectophosphatases will be also included.

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References

  1. Cortez KJ, Roilides E, Quiroz-Telles F, Meletiadis J, Antachopoulos C, Knudsen T, et al. Infections caused by Scedosporium spp. Clin Microbiol Rev. 2008;21(1):157–97. https://doi.org/10.1128/CMR.00039-07.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Ramirez-Garcia A, Pellon A, Rementeria A, Buldain I, Barreto-Bergter E, Rollin-Pinheiro R, et al. Scedosporium and Lomentospora: an updated overview of underrated opportunists. Med Mycol. 2018;56(1):102–25. https://doi.org/10.1093/mmy/myx113.

    Article  PubMed  Google Scholar 

  3. Rougeron A, Schuliar G, Leto J, Sitterle E, Landry D, Bougnoux ME, et al. Human-impacted areas of France are environmental reservoirs of the Pseudallescheria boydii/Scedosporium apiospermum species complex. Environ Microbiol. 2015;17(4):1039–48. https://doi.org/10.1111/1462-2920.12472.

    Article  CAS  PubMed  Google Scholar 

  4. Luplertlop N. Pseudallescheria/Scedosporium complex species: From saprobic to pathogenic fungus. J Mycol Med. 2018;28(2):249–56. https://doi.org/10.1016/j.mycmed.2018.02.015.

    Article  CAS  PubMed  Google Scholar 

  5. Guarro J, Kantarcioglu AS, Horre R, Rodriguez-Tudela JL, Cuenca Estrella M, Berenguer J, et al. Scedosporium apiospermum: changing clinical spectrum of a therapy-refractory opportunist. Med Mycol. 2006;44(4):295–32727. https://doi.org/10.1080/13693780600752507.

    Article  PubMed  Google Scholar 

  6. Harun A, Serena C, Gilgado F, Chen SC, Meyer W. Scedosporium aurantiacum is as virulent as S. prolificans, and shows strain-specific virulence differences, in a mouse model. Med Mycol. 2010;48(Suppl 1):S45–S51. https://doi.org/10.3109/13693786.2010.517224.

    Article  PubMed  Google Scholar 

  7. Husain S, Munoz P, Forrest G, Alexander BD, Somani J, Brennan K, et al. Infections due to Scedosporium apiospermum and Scedosporium prolificans in transplant recipients: clinical characteristics and impact of antifungal agent therapy on outcome. Clin Infect Dis. 2005;40(1):89–99. https://doi.org/10.1086/426445.

    Article  PubMed  Google Scholar 

  8. Lamaris GA, Chamilos G, Lewis RE, Safdar A, Raad II, Kontoyiannis DP. Scedosporium infection in a tertiary care cancer center: a review of 25 cases from 1989–2006. Clin Infect Dis. 2006;43(12):1580–4. https://doi.org/10.1086/509579.

    Article  PubMed  Google Scholar 

  9. Tammer I, Tintelnot K, Braun-Dullaeus RC, Mawrin C, Scherlach C, Schluter D, et al. Infections due to Pseudallescheria/Scedosporium species in patients with advanced HIV disease—a diagnostic and therapeutic challenge. Int J Infect Dis. 2011;15(6):e422–e429429. https://doi.org/10.1016/j.ijid.2011.03.004.

    Article  PubMed  Google Scholar 

  10. Sedlacek L, Graf B, Schwarz C, Albert F, Peter S, Wurstl B, et al. Prevalence of Scedosporium species and Lomentospora prolificans in patients with cystic fibrosis in a multicenter trial by use of a selective medium. J Cyst Fibros. 2015;14(2):237–41. https://doi.org/10.1016/j.jcf.2014.12.014.

    Article  CAS  PubMed  Google Scholar 

  11. Barreto-Bergter E, Sassaki GL, de Souza LM. Structural analysis of fungal cerebrosides. Front Microbiol. 2011;2:239. https://doi.org/10.3389/fmicb.2011.00239.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Barreto-Bergter E, Figueiredo RT. Fungal glycans and the innate immune recognition. Front Cell Infect Microbiol. 2014;4:145. https://doi.org/10.3389/fcimb.2014.00145.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Rollin-Pinheiro R, Singh A, Barreto-Bergter E, Del Poeta M. Sphingolipids as targets for treatment of fungal infections. Future Med Chem. 2016;8(12):1469–84. https://doi.org/10.4155/fmc-2016-0053.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Ghamrawi S, Gastebois A, Zykwinska A, Vandeputte P, Marot A, Mabilleau G, et al. A multifaceted study of Scedosporium boydii Cell wall changes during germination and identification of GPI-anchored proteins. PLoS ONE. 2015;10(6):e0128680. https://doi.org/10.1371/journal.pone.0128680.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Del Poeta M, Nimrichter L, Rodrigues ML, Luberto C. Synthesis and biological properties of fungal glucosylceramide. PLoS Pathog. 2014;10(1):e1003832. https://doi.org/10.1371/journal.ppat.1003832.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Barreto-Bergter E, Pinto MR, Rodrigues ML. Structure and biological functions of fungal cerebrosides. An Acad Bras Cienc. 2004;76(1):67–84.

    Article  CAS  PubMed  Google Scholar 

  17. Singh A, Del Poeta M. Sphingolipidomics: an Important mechanistic tool for studying fungal pathogens. Front Microbiol. 2016;7:501. https://doi.org/10.3389/fmicb.2016.00501.

    Article  PubMed  PubMed Central  Google Scholar 

  18. Buede R, Rinker-Schaffer C, Pinto WJ, Lester RL, Dickson RC. Cloning and characterization of LCB1, a Saccharomyces gene required for biosynthesis of the long-chain base component of sphingolipids. J Bacteriol. 1991;173(14):4325–32. https://doi.org/10.1128/jb.173.14.4325-4332.1991.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Nagiec MM, Baltisberger JA, Wells GB, Lester RL, Dickson RC. The LCB2 gene of Saccharomyces and the related LCB1 gene encode subunits of serine palmitoyltransferase, the initial enzyme in sphingolipid synthesis. Proc Natl Acad Sci USA. 1994;91(17):7899–902. https://doi.org/10.1073/pnas.91.17.7899.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Lahiri S, Futerman AH. LASS5 is a bona fide dihydroceramide synthase that selectively utilizes palmitoyl-CoA as acyl donor. J Biol Chem. 2005;280(40):33735–8. https://doi.org/10.1074/jbc.M506485200.

    Article  CAS  PubMed  Google Scholar 

  21. Sperling P, Lee M, Girke T, Zahringer U, Stymne S, Heinz E. A bifunctional delta-fatty acyl acetylenase/desaturase from the moss Ceratodon purpureus. A new member of the cytochrome b5 superfamily. Eur J Biochem. 2000;267(12):3801–11. https://doi.org/10.1046/j.1432-1327.2000.01418.x.

    Article  CAS  PubMed  Google Scholar 

  22. Ternes P, Wobbe T, Schwarz M, Albrecht S, Feussner K, Riezman I, et al. Two pathways of sphingolipid biosynthesis are separated in the yeast Pichia pastoris. J Biol Chem. 2011;286(13):11401–14. https://doi.org/10.1074/jbc.M110.193094.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Rodriguez-Cuenca S, Barbarroja N, Vidal-Puig A. Dihydroceramide desaturase 1, the gatekeeper of ceramide induced lipotoxicity. Biochim Biophys Acta. 2015;1851(1):40–50. https://doi.org/10.1016/j.bbalip.2014.09.021.

    Article  CAS  PubMed  Google Scholar 

  24. Ternes P, Sperling P, Albrecht S, Franke S, Cregg JM, Warnecke D, et al. Identification of fungal sphingolipid C9-methyltransferases by phylogenetic profiling. J Biol Chem. 2006;281(9):5582–92. https://doi.org/10.1074/jbc.M512864200.

    Article  CAS  PubMed  Google Scholar 

  25. Singh A, Wang H, Silva LC, Na C, Prieto M, Futerman AH, et al. Methylation of glycosylated sphingolipid modulates membrane lipid topography and pathogenicity of Cryptococcus neoformans. Cell Microbiol. 2012;14(4):500–16. https://doi.org/10.1111/j.1462-5822.2011.01735.x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Rittershaus PC, Kechichian TB, Allegood JC, Merrill AH Jr, Hennig M, Luberto C, et al. Glucosylceramide synthase is an essential regulator of pathogenicity of Cryptococcus neoformans. J Clin Invest. 2006;116(6):1651–9. https://doi.org/10.1172/JCI27890.

    Article  PubMed  PubMed Central  Google Scholar 

  27. Rollin-Pinheiro R, Rochetti VP, Xisto M, Liporagi-Lopes LC, Bastos B, Rella A, et al. Sphingolipid biosynthetic pathway is crucial for growth, biofilm formation and membrane integrity of Scedosporium boydii. Future Med Chem. 2019;11(22):2905–17. https://doi.org/10.4155/fmc-2019-0186.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Rollin-Pinheiro R, Liporagi-Lopes LC, de Meirelles JV, Souza LM, Barreto-Bergter E. Characterization of Scedosporium apiospermum glucosylceramides and their involvement in fungal development and macrophage functions. PLoS ONE. 2014;9(5):e98149. https://doi.org/10.1371/journal.pone.0098149.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Calixto RO, Rollin-Pinheiro R, da Silva MI, Liporagi-Lopes LC, Vieira JM, Sassaki GL, et al. Structural analysis of glucosylceramides (GlcCer) from species of the Pseudallescheria/Scedosporium complex. Fungal Biol. 2016;120(2):166–72. https://doi.org/10.1016/j.funbio.2015.05.007.

    Article  CAS  PubMed  Google Scholar 

  30. Xisto M, Henao JEM, Dias LDS, Santos GMP, Calixto ROR, Bernardino MC, et al. Glucosylceramides from Lomentospora prolificans induce a differential production of cytokines and increases the microbicidal activity of macrophages. Front Microbiol. 2019;10:554. https://doi.org/10.3389/fmicb.2019.00554.

    Article  PubMed  PubMed Central  Google Scholar 

  31. Caneppa A, de Meirelles JV, Rollin-Pinheiro R, Dutra Xisto M, Liporagi-Lopes LC, Souza L, et al. Structural differences influence biological properties of glucosylceramides from clinical and environmental isolates of Scedosporium aurantiacum and Pseudallescheria minutispora. J Fungi (Basel). 2019. https://doi.org/10.3390/jof5030062.

    Article  Google Scholar 

  32. Oura T, Kajiwara S. Disruption of the sphingolipid Delta8-desaturase gene causes a delay in morphological changes in Candida albicans. Microbiology. 2008;154(Pt 12):3795–803. https://doi.org/10.1099/mic.0.2008/018788-0.

    Article  CAS  PubMed  Google Scholar 

  33. Perdoni F, Signorelli P, Cirasola D, Caretti A, Galimberti V, Biggiogera M, et al. Antifungal activity of Myriocin on clinically relevant Aspergillus fumigatus strains producing biofilm. BMC Microbiol. 2015;15:248. https://doi.org/10.1186/s12866-015-0588-0.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Fernandes CM, de Castro PA, Singh A, Fonseca FL, Pereira MD, Vila TV, et al. Functional characterization of the Aspergillus nidulans glucosylceramide pathway reveals that LCB Delta8-desaturation and C9-methylation are relevant to filamentous growth, lipid raft localization and Psd1 defensin activity. Mol Microbiol. 2016;102(3):488–505. https://doi.org/10.1111/mmi.13474.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Pinto MR, Rodrigues ML, Travassos LR, Haido RM, Wait R, Barreto-Bergter E. Characterization of glucosylceramides in Pseudallescheria boydii and their involvement in fungal differentiation. Glycobiology. 2002;12(4):251–60.

    Article  CAS  PubMed  Google Scholar 

  36. Mor V, Rella A, Farnoud AM, Singh A, Munshi M, Bryan A, et al. Identification of a new class of antifungals targeting the synthesis of fungal sphingolipids. mBio. 2015;6(3):e00647. https://doi.org/10.1128/mBio.00647-15.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Pinto MR, Mulloy B, Haido RM, Travassos LR, Barreto BE. A peptidorhamnomannan from the mycelium of Pseudallescheria boydii is a potential diagnostic antigen of this emerging human pathogen. Microbiology. 2001;147(Pt 6):1499–506. https://doi.org/10.1099/00221287-147-6-1499.

    Article  CAS  PubMed  Google Scholar 

  38. Lopes-Bezerra LM. Sporothrix schenckii Cell Wall peptidorhamnomannans. Front Microbiol. 2011;2:243. https://doi.org/10.3389/fmicb.2011.00243.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Barreto-Bergter E, Sassaki GL, Wagner R, Souza LM, Souza MV, Pinto MR, et al. The opportunistic fungal pathogen Scedosporium prolificans: carbohydrate epitopes of its glycoproteins. Int J Biol Macromol. 2008;42(2):93–102. https://doi.org/10.1016/j.ijbiomac.2007.09.015.

    Article  CAS  PubMed  Google Scholar 

  40. Pinto MR, Gorin PA, Wait R, Mulloy B, Barreto-Bergter E. Structures of the O-linked oligosaccharides of a complex glycoconjugate from Pseudallescheria boydii. Glycobiology. 2005;15(10):895–904. https://doi.org/10.1093/glycob/cwi084.

    Article  CAS  PubMed  Google Scholar 

  41. Lopes LC, Rollin-Pinheiro R, Guimaraes AJ, Bittencourt VC, Martinez LR, Koba W, et al. Monoclonal antibodies against peptidorhamnomannans of Scedosporium apiospermum enhance the pathogenicity of the fungus. PLoS Negl Trop Dis. 2010;4(10):e853. https://doi.org/10.1371/journal.pntd.0000853.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Pinto MR, de Sa AC, Limongi CL, Rozental S, Santos AL, Barreto-Bergter E. Involvement of peptidorhamnomannan in the interaction of Pseudallescheria boydii and HEp2 cells. Microbes Infect. 2004;6(14):1259–67. https://doi.org/10.1016/j.micinf.2004.07.006.

    Article  CAS  PubMed  Google Scholar 

  43. Lopes LC, da Silva MI, Bittencourt VC, Figueiredo RT, Rollin-Pinheiro R, Sassaki GL, et al. Glycoconjugates and polysaccharides from the Scedosporium/Pseudallescheria boydii complex: structural characterisation, involvement in cell differentiation, cell recognition and virulence. Mycoses. 2011;54(Suppl 3):28–36. https://doi.org/10.1111/j.1439-0507.2011.02105.x.

    Article  CAS  PubMed  Google Scholar 

  44. Xisto MI, Bittencourt VC, Liporagi-Lopes LC, Haido RM, Mendonca MS, Sassaki G, et al. O-glycosylation in cell wall proteins in Scedosporium prolificans is critical for phagocytosis and inflammatory cytokines production by macrophages. PLoS ONE. 2015;10(4):e0123189. https://doi.org/10.1371/journal.pone.0123189.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Figueiredo RT, Fernandez PL, Dutra FF, Gonzalez Y, Lopes LC, Bittencourt VC, et al. TLR4 recognizes Pseudallescheria boydii conidia and purified rhamnomannans. J Biol Chem. 2010;285(52):40714–23. https://doi.org/10.1074/jbc.M110.181255.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Xisto MI, Liporagi-Lopes LC, Munoz JE, Bittencourt VC, Santos GM, Dias LS, et al. Peptidorhamnomannan negatively modulates the immune response in a scedosporiosis murine model. Med Mycol. 2016;54(8):846–55. https://doi.org/10.1093/mmy/myw039.

    Article  CAS  PubMed  Google Scholar 

  47. Bittencourt VC, Figueiredo RT, da Silva RB, Mourao-Sa DS, Fernandez PL, Sassaki GL, et al. An alpha-glucan of Pseudallescheria boydii is involved in fungal phagocytosis and Toll-like receptor activation. J Biol Chem. 2006;281(32):22614–23. https://doi.org/10.1074/jbc.M511417200.

    Article  CAS  PubMed  Google Scholar 

  48. Bahia MC, Vieira RP, Mulloy B, Hartmann R, Bergter EB. The structures of polysaccharides and glycolipids of Aspergillus fumigatus grown in the presence of human serum. Mycopathologia. 1997;137(1):17–25. https://doi.org/10.1023/a:1006862420963.

    Article  CAS  PubMed  Google Scholar 

  49. Wang R, Klegerman ME, Marsden I, Sinnott M, Groves MJ. An anti-neoplastic glycan isolated from Mycobacterium bovis (BCG vaccine). Biochem J. 1995;311(Pt 3):867–72. https://doi.org/10.1042/bj3110867.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Odabasi Z, Paetznick VL, Rodriguez JR, Chen E, McGinnis MR, Ostrosky-Zeichner L. Differences in beta-glucan levels in culture supernatants of a variety of fungi. Med Mycol. 2006;44(3):267–72. https://doi.org/10.1080/13693780500474327.

    Article  CAS  PubMed  Google Scholar 

  51. Gow NAR, Latge JP, Munro CA. The fungal cell wall: structure, biosynthesis, and function. Microbiol Spectr. 2017. https://doi.org/10.1128/microbiolspec.FUNK-0035-2016.

    Article  PubMed  Google Scholar 

  52. Latge JP. Tasting the fungal cell wall. Cell Microbiol. 2010;12(7):863–72. https://doi.org/10.1111/j.1462-5822.2010.01474.x.

    Article  CAS  PubMed  Google Scholar 

  53. Wheeler MH, Bell AA. Melanins and their importance in pathogenic fungi. Curr Top Med Mycol. 1988;2:338–87. https://doi.org/10.1007/978-1-4612-3730-3_10.

    Article  CAS  PubMed  Google Scholar 

  54. Langfelder K, Streibel M, Jahn B, Haase G, Brakhage AA. Biosynthesis of fungal melanins and their importance for human pathogenic fungi. Fungal Genet Biol. 2003;38(2):143–58. https://doi.org/10.1016/s1087-1845(02)00526-1.

    Article  CAS  PubMed  Google Scholar 

  55. Perez-Cuesta U, Aparicio-Fernandez L, Guruceaga X, Martin-Souto L, Abad-Diaz-de-Cerio A, Antoran A, et al. Melanin and pyomelanin in Aspergillus fumigatus: from its genetics to host interaction. Int Microbiol. 2020;23(1):55–63. https://doi.org/10.1007/s10123-019-00078-0.

    Article  CAS  PubMed  Google Scholar 

  56. Ghamrawi S, Renier G, Saulnier P, Cuenot S, Zykwinska A, Dutilh BE, et al. Cell wall modifications during conidial maturation of the human pathogenic fungus Pseudallescheria boydii. PLoS ONE. 2014;9(6):e100290. https://doi.org/10.1371/journal.pone.0100290.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Braga GU, Rangel DE, Fernandes EK, Flint SD, Roberts DW. Molecular and physiological effects of environmental UV radiation on fungal conidia. Curr Genet. 2015;61(3):405–25. https://doi.org/10.1007/s00294-015-0483-0.

    Article  CAS  PubMed  Google Scholar 

  58. Hillmann F, Novohradska S, Mattern DJ, Forberger T, Heinekamp T, Westermann M, et al. Virulence determinants of the human pathogenic fungus Aspergillus fumigatus protect against soil amoeba predation. Environ Microbiol. 2015;17(8):2858–69. https://doi.org/10.1111/1462-2920.12808.

    Article  CAS  PubMed  Google Scholar 

  59. Chai LY, Netea MG, Sugui J, Vonk AG, van de Sande WW, Warris A, et al. Aspergillus fumigatus conidial melanin modulates host cytokine response. Immunobiology. 2010;215(11):915–20. https://doi.org/10.1016/j.imbio.2009.10.002.

    Article  CAS  PubMed  Google Scholar 

  60. Jahn B, Langfelder K, Schneider U, Schindel C, Brakhage AA. PKSP-dependent reduction of phagolysosome fusion and intracellular kill of Aspergillus fumigatus conidia by human monocyte-derived macrophages. Cell Microbiol. 2002;4(12):793–803. https://doi.org/10.1046/j.1462-5822.2002.00228.x.

    Article  CAS  PubMed  Google Scholar 

  61. Amin S, Thywissen A, Heinekamp T, Saluz HP, Brakhage AA. Melanin dependent survival of Apergillus fumigatus conidia in lung epithelial cells. Int J Med Microbiol. 2014;304(5–6):626–36. https://doi.org/10.1016/j.ijmm.2014.04.009.

    Article  CAS  PubMed  Google Scholar 

  62. Pihet M, Vandeputte P, Tronchin G, Renier G, Saulnier P, Georgeault S, et al. Melanin is an essential component for the integrity of the cell wall of Aspergillus fumigatus conidia. BMC Microbiol. 2009;9:177. https://doi.org/10.1186/1471-2180-9-177.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Gravelat FN, Ejzykowicz DE, Chiang LY, Chabot JC, Urb M, Macdonald KD, et al. Aspergillus fumigatus MedA governs adherence, host cell interactions and virulence. Cell Microbiol. 2010;12(4):473–88. https://doi.org/10.1111/j.1462-5822.2009.01408.x.

    Article  CAS  PubMed  Google Scholar 

  64. Nosanchuk JD, Casadevall A. Impact of melanin on microbial virulence and clinical resistance to antimicrobial compounds. Antimicrob Agents Chemother. 2006;50(11):3519–28. https://doi.org/10.1128/AAC.00545-06.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Voelz K, May RC. Cryptococcal interactions with the host immune system. Eukaryot Cell. 2010;9(6):835–46. https://doi.org/10.1128/EC.00039-10.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Thornton CR, Ryder LS, Le Cocq K, Soanes DM. Identifying the emerging human pathogen Scedosporium prolificans by using a species-specific monoclonal antibody that binds to the melanin biosynthetic enzyme tetrahydroxynaphthalene reductase. Environ Microbiol. 2015;17(4):1023–38. https://doi.org/10.1111/1462-2920.12470.

    Article  CAS  PubMed  Google Scholar 

  67. Al-Laaeiby A, Kershaw MJ, Penn TJ, Thornton CR. Targeted disruption of melanin biosynthesis genes in the human pathogenic fungus Lomentospora prolificans and its consequences for pathogen survival. Int J Mol Sci. 2016;17(4):444. https://doi.org/10.3390/ijms17040444.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Kiffer-Moreira T, Pinheiro AA, Pinto MR, Esteves FF, Souto-Padron T, Barreto-Bergter E, et al. Mycelial forms of Pseudallescheria boydii present ectophosphatase activities. Arch Microbiol. 2007;188(2):159–66. https://doi.org/10.1007/s00203-007-0232-y.

    Article  CAS  PubMed  Google Scholar 

  69. Fernanado PH, Panagoda GJ, Samaranayake LP. The relationship between the acid and alkaline phosphatase activity and the adherence of clinical isolates of Candida parapsilosis to human buccal epithelial cells. APMIS. 1999;107(11):1034–42. https://doi.org/10.1111/j.1699-0463.1999.tb01507.x.

    Article  CAS  PubMed  Google Scholar 

  70. Bakalara N, Santarelli X, Davis C, Baltz T. Purification, cloning, and characterization of an acidic ectoprotein phosphatase differentially expressed in the infectious bloodstream form of Trypanosoma brucei. J Biol Chem. 2000;275(12):8863–71. https://doi.org/10.1074/jbc.275.12.8863.

    Article  CAS  PubMed  Google Scholar 

  71. Belanger PH, Johnston DA, Fratti RA, Zhang M, Filler SG. Endocytosis of Candida albicans by vascular endothelial cells is associated with tyrosine phosphorylation of specific host cell proteins. Cell Microbiol. 2002;4(12):805–12. https://doi.org/10.1046/j.1462-5822.2002.00232.x.

    Article  CAS  PubMed  Google Scholar 

  72. Kneipp LF, Palmeira VF, Pinheiro AA, Alviano CS, Rozental S, Travassos LR, et al. Phosphatase activity on the cell wall of Fonsecaea pedrosoi. Med Mycol. 2003;41(6):469–77. https://doi.org/10.1080/10683160310001615399.

    Article  CAS  PubMed  Google Scholar 

  73. Kneipp LF, Rodrigues ML, Holandino C, Esteves FF, Souto-Padron T, Alviano CS, et al. Ectophosphatase activity in conidial forms of Fonsecaea pedrosoi is modulated by exogenous phosphate and influences fungal adhesion to mammalian cells. Microbiology. 2004;150(Pt 10):3355–62. https://doi.org/10.1099/mic.0.27405-0.

    Article  CAS  PubMed  Google Scholar 

  74. Liu S, Hou Y, Liu W, Lu C, Wang W, Sun S. Components of the calcium-calcineurin signaling pathway in fungal cells and their potential as antifungal targets. Eukaryot Cell. 2015;14(4):324–34. https://doi.org/10.1128/EC.00271-14.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Lamoth F, Alexander BD, Juvvadi PR, Steinbach WJ. Antifungal activity of compounds targeting the Hsp90-calcineurin pathway against various mould species. J Antimicrob Chemother. 2015;70(5):1408–11. https://doi.org/10.1093/jac/dku549.

    Article  CAS  PubMed  Google Scholar 

  76. Nambu M, Covel JA, Kapoor M, Li X, Moloney MK, Numa MM, et al. A calcineurin antifungal strategy with analogs of FK506. Bioorg Med Chem Lett. 2017;27(11):2465–71. https://doi.org/10.1016/j.bmcl.2017.04.004.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

This study was financed in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) – Finance Code 001; Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) and Fundação de Amparo à Pesquisa do estado do Rio de Janeiro (Faperj).

The authors thank Walter Oelemann for English revision.

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  1. All authors contributed equally for this publication.

Authors and Affiliations

  1. Departamento de Microbiologia Geral, Instituto de Microbiologia Paulo de Góes, Universidade Federal Do Rio de Janeiro, Rio de Janeiro, 21941-902, Brazil

    Rodrigo Rollin-Pinheiro, Mariana Ingrid Dutra da Silva Xisto, Victor Pereira Rochetti & Eliana Barreto-Bergter

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  1. Rodrigo Rollin-Pinheiro
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  2. Mariana Ingrid Dutra da Silva Xisto
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  3. Victor Pereira Rochetti
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  4. Eliana Barreto-Bergter
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RRP, MIDSX, VPR and EBB equally contributed to conception, literature review, manuscript writing drawing of figures and editing.

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Correspondence to Eliana Barreto-Bergter.

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Rollin-Pinheiro, R., Xisto, M.I.D.d., Rochetti, V.P. et al. Scedosporium Cell Wall: From Carbohydrate-Containing Structures to Host–Pathogen Interactions. Mycopathologia 185, 931–946 (2020). https://doi.org/10.1007/s11046-020-00480-7

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  • DOI: https://doi.org/10.1007/s11046-020-00480-7

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