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ORIGINAL RESEARCH

Contribution of N-Linked Mannosylation Pathway to Candida parapsilosis and Candida tropicalis Biofilm Formation

, ORCID Icon, , ORCID Icon & ORCID Icon
Pages 6843-6857 | Received 21 Jul 2023, Accepted 18 Oct 2023, Published online: 26 Oct 2023

References

  • McCarty TP, White CM, Pappas PG. Candidemia and invasive candidiasis. Infect Dis Clin North Am. 2021;35(2):389–413. doi:10.1016/j.idc.2021.03.007
  • Brown GD, Denning DW, Gow NA, Levitz SM, Netea MG, White TC. Hidden killers: human fungal infections. Sci Transl Med. 2012;4(165):165rv13. doi:10.1126/scitranslmed.3004404
  • Fisher MC, Gurr SJ, Cuomo CA, et al. Threats posed by the fungal kingdom to humans, wildlife, and agriculture. mBio. 2020;11(3):e00449–20. doi:10.1128/mBio.00449-20
  • Chen L, Zhang L, Xie Y, et al. Confronting antifungal resistance, tolerance, and persistence: advances in drug target discovery and delivery systems. Adv Drug Deliv Rev. 2023;200:115007. doi:10.1016/j.addr.2023.115007
  • Francisco EC, de Jong AW, Colombo AL. Candida haemulonii species complex: a mini-review. Mycopathologia. 2023. doi:10.1007/s11046-023-00748-8
  • Gómez-Gaviria M, Martínez-álvarez JA, Chávez-Santiago JO, Mora-Montes HM. Candida haemulonii complex and Candida auris: biology, virulence factors, immune response, and multidrug resistance. Infect Drug Resist. 2023;16:1455–1470. doi:10.2147/idr.S402754
  • Loh JT, Lam KP. Fungal infections: immune defense, immunotherapies and vaccines. Adv Drug Deliv Rev. 2023;196:114775. doi:10.1016/j.addr.2023.114775
  • Soriano A, Honore PM, Puerta-Alcalde P, et al. Invasive candidiasis: current clinical challenges and unmet needs in adult populations. J Antimicrob Chemother. 2023;78(7):1569–1585. doi:10.1093/jac/dkad139
  • Gómez-Gaviria M, Ramírez-Sotelo U, Mora-Montes HM. Non-albicans Candida species: immune response, evasion mechanisms, and new plant-derived alternative therapies. J Fungi. 2022;9(1):11. doi:10.3390/jof9010011
  • Parums DV. Editorial: the World Health Organization (WHO) fungal priority pathogens list in response to emerging fungal pathogens during the COVID-19 pandemic. Med Sci Monit. 2022;28:e939088. doi:10.12659/msm.939088
  • Zuza-Alves DL, Silva-Rocha WP, Chaves GM. An update on Candida tropicalis based on basic and clinical approaches. Front Microbiol. 2017;8:1927. doi:10.3389/fmicb.2017.01927
  • Toth R, Nosek J, Mora-Montes HM, et al. Candida parapsilosis: from genes to the bedside. Clin Microbiol Rev. 2019;32(2):e00111–e00118. doi:10.1128/CMR.00111-18
  • Bouza E, Guinea J, Guembe M. The role of antifungals against Candida Biofilm in catheter-related candidemia. Antibiotics. 2014;4(1):1–17. doi:10.3390/antibiotics4010001
  • Cavalheiro M, Teixeira MC. Candida biofilms: threats, challenges, and promising strategies. Front Med. 2018;5:28. doi:10.3389/fmed.2018.00028
  • Donlan RM. Biofilms and device-associated infections. Emerg Infect Dis. 2001;7(2):277–281. doi:10.3201/eid0702.010226
  • Ding C, Vidanes GM, Maguire SL, et al. Conserved and divergent roles of Bcr1 and CFEM proteins in Candida parapsilosis and Candida albicans. PLoS One. 2011;6(12):e28151. doi:10.1371/journal.pone.0028151
  • Jin Y, Samaranayake LP, Samaranayake Y, Yip HK. Biofilm formation of Candida albicans is variably affected by saliva and dietary sugars. Arch Oral Biol. 2004;49(10):789–798. doi:10.1016/j.archoralbio.2004.04.011
  • Queiroz PA, Godoy JSR, Mendonça PSB, Pedroso RB, Svidzinski TIE, Negri M. Adhesion and biofilm formation in artificial saliva and susceptibility of yeasts isolated from chronic kidney patients undergoing haemodialysis. J Med Microbiol. 2015;64(9):960–966. doi:10.1099/jmm.0.000122
  • Kleinberg ME, Rotrosen D, Malech HL. Asparagine-linked glycosylation of cytochrome b558 large subunit varies in different human phagocytic cells. J Immunol. 1989;143(12):4152–4157. doi:10.4049/jimmunol.143.12.4152
  • Pierce CG, Thomas DP, López-Ribot JL. Effect of tunicamycin on Candida albicans biofilm formation and maintenance. J Antimicrob Chemother. 2009;63(3):473–479. doi:10.1093/jac/dkn515
  • Martinez-Duncker I, Diaz-Jimenez DF, Mora-Montes HM. Comparative analysis of protein glycosylation pathways in humans and the fungal pathogen Candida albicans. Int J Microbiol. 2014;2014:267497. doi:10.1155/2014/267497
  • Mora-Montes HM, Ponce-Noyola P, Villagómez-Castro JC, Gow NAR, Flores-Carreón A, López-Romero E. Protein glycosylation in Candida. Future Microbiol. 2009;4(9):1167–1183. doi:10.2217/fmb.09.88
  • Lehle L, Strahl S, Tanner W. Protein glycosylation, conserved from yeast to man: a model organism helps elucidate congenital human diseases. Angew Chem Int Ed Engl. 2006;45(41):6802–6818. doi:10.1002/anie.200601645
  • Krshnan L, van de Weijer ML, Carvalho P. Endoplasmic reticulum-associated protein degradation. Cold Spring Harb Perspect Biol. 2022;14(12):a041247. doi:10.1101/cshperspect.a041247
  • Nagasu T, Shimma Y, Nakanishi Y, et al. Isolation of new temperature-sensitive mutants of Saccharomyces cerevisiae deficient in mannose outer chain elongation. Yeast. 1992;8(7):535–547. doi:10.1002/yea.320080705
  • Lee BN, Elion EA. The MAPKKK Ste11 regulates vegetative growth through a kinase cascade of shared signaling components. Proc Natl Acad Sci U S A. 1999;96(22):12679–12684. doi:10.1073/pnas.96.22.12679
  • Cullen PJ, Schultz J, Horecka J, Stevenson BJ, Jigami Y, Sprague GF. Defects in protein glycosylation cause SHO1-dependent activation of a STE12 signaling pathway in yeast. Genetics. 2000;155(3):1005–1018. doi:10.1093/genetics/155.3.1005
  • Hernandez-Chavez MJ, Clavijo-Giraldo DM, Novak A, et al. Role of protein mannosylation in the Candida tropicalis-host interaction. Front Microbiol. 2019;10:2743. doi:10.3389/fmicb.2019.02743
  • Perez-Garcia LA, Csonka K, Flores-Carreon A, et al. Role of protein glycosylation in Candida parapsilosis cell wall integrity and host interaction. Front Microbiol. 2016;7:306. doi:10.3389/fmicb.2016.00306
  • Laffey SF, Butler G. Phenotype switching affects biofilm formation by Candida parapsilosis. Microbiology. 2005;151(4):1073–1081. doi:10.1099/mic.0.27739-0
  • Holland LM, Schroder MS, Turner SA, et al. Comparative phenotypic analysis of the major fungal pathogens Candida parapsilosis and Candida albicans. PLoS Pathog. 2014;10(9):e1004365. doi:10.1371/journal.ppat.1004365
  • Peeters E, Nelis HJ, Coenye T. Comparison of multiple methods for quantification of microbial biofilms grown in microtiter plates. J Microbiol Methods. 2008;72(2):157–165. doi:10.1016/j.mimet.2007.11.010
  • Navarro-Arias MJ, Defosse TA, Dementhon K, et al. Disruption of protein mannosylation affects Candida guilliermondii cell wall, immune sensing, and virulence. Original Research. Front Microbiol. 2016;7(1951). doi:10.3389/fmicb.2016.01951
  • Dominguez E, Zarnowski R, Sanchez H, et al. Conservation and divergence in the Candida species biofilm matrix mannan-glucan complex structure, function, and genetic control. mBio. 2018;9(2):e00451–18. doi:10.1128/mBio.00451-18
  • Al-Fattani MA, Douglas LJ. Biofilm matrix of Candida albicans and Candida tropicalis: chemical composition and role in drug resistance. J Med Microbiol. 2006;55(8):999–1008. doi:10.1099/jmm.0.46569-0
  • Plaine A, Walker L, Da Costa G, et al. Functional analysis of Candida albicans GPI-anchored proteins: roles in cell wall integrity and caspofungin sensitivity. Fungal Genet Biol. 2008;45(10):1404–1414. doi:10.1016/j.fgb.2008.08.003
  • Mora-Montes HM, Bates S, Netea MG, et al. Endoplasmic reticulum alpha-glycosidases of Candida albicans are required for N glycosylation, cell wall integrity, and normal host-fungus interaction. Eukaryot Cell. 2007;6(12):2184–2193. doi:10.1128/EC.00350-07
  • Ramage G, Walle KV, Wickes BL, López-Ribot JL. Standardized method for in vitro antifungal susceptibility testing of Candida albicans biofilms. Antimicrob Agents Chemother. 2001;45(9):2475–2479. doi:10.1128/aac.45.9.2475-2479.2001
  • Papp C, Kocsis K, Tóth R, et al. Echinocandin-induced microevolution of Candida parapsilosis influences virulence and abiotic stress tolerance. mSphere. 2018;3(6):e00547–18. doi:10.1128/mSphere.00547-18
  • Robledo-Ortiz CI, Flores-Carreón A, Hernández-Cervantes A, et al. Isolation and functional characterization of Sporothrix schenckii ROT2, the encoding gene for the endoplasmic reticulum glucosidase II. Fungal Biol. 2012;116(8):910–918. doi:10.1016/j.funbio.2012.06.002
  • Trujillo-Esquivel E, Franco B, Flores-Martínez A, Ponce-Noyola P, Mora-Montes HM. Purification of single-stranded cDNA based on RNA degradation treatment and adsorption chromatography. Nucleosides Nucleotides Nucleic Acids. 2016;35(8):404–409. doi:10.1080/15257770.2016.1184277
  • Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001;25(4):402–408. doi:10.1006/meth.2001.1262
  • Smolenski G, Sullivan PA, Cutfield SM, Cutfield JF. Analysis of secreted aspartic proteinases from Candida albicans: purification and characterization of individual Sap1, Sap2 and Sap3 isoenzymes. Microbiology. 1997;143(2):349–356. doi:10.1099/00221287-143-2-349
  • Mora-Montes HM, Lopez-Romero E, Zinker S, Ponce-Noyola P, Flores-Carreon A. Hydrolysis of Man9GlcNAc2 and Man8GlcNAc2 oligosaccharides by a purified alpha-mannosidase from Candida albicans. Glycobiology. 2004;14(7):593–598. doi:10.1093/glycob/cwh091
  • Bates S, Hughes HB, Munro CA, et al. Outer chain N-glycans are required for cell wall integrity and virulence of Candida albicans. J Biol Chem. 2006;281(1):90–98. doi:10.1074/jbc.M510360200
  • Joly S, Pujol C, Schröppel K, Soll DR. Development of two species-specific fingerprinting probes for broad computer-assisted epidemiological studies of Candida tropicalis. J Clin Microbiol. 1996;34(12):3063–3071. doi:10.1128/jcm.34.12.3063-3071.1996
  • Lopes-Bezerra LM, Lozoya-Perez NE, Lopez-Ramirez LA, et al. Functional characterization of Sporothrix schenckii glycosidases involved in the N-linked glycosylation pathway. Med Mycol. 2015;53(1):60–68. doi:10.1093/mmy/myu057
  • Maley F, Trimble RB, Tarentino AL, Plummer TH. Characterization of glycoproteins and their associated oligosaccharides through the use of endoglycosidases. Anal Biochem. 1989;180(2):195–204. doi:10.1016/0003-2697(89)90115-2
  • Melo AS, Bizerra FC, Freymüller E, Arthington-Skaggs BA, Colombo AL. Biofilm production and evaluation of antifungal susceptibility amongst clinical Candida spp. isolates, including strains of the Candida parapsilosis complex. Med Mycol. 2011;49(3):253–262. doi:10.3109/13693786.2010.530032
  • Gácser A, Trofa D, Schäfer W, Nosanchuk JD. Targeted gene deletion in Candida parapsilosis demonstrates the role of secreted lipase in virulence. J Clin Invest. 2007;117(10):3049–3058. doi:10.1172/jci32294
  • Singh DK, Németh T, Papp A, et al. Functional characterization of secreted aspartyl proteases in Candida parapsilosis. mSphere. 2019;4(4). doi:10.1128/mSphere.00484-19
  • Lippincott-Schwartz J, Yuan L, Tipper C, Amherdt M, Orci L, Klausner RD. Brefeldin A’s effects on endosomes, lysosomes, and the TGN suggest a general mechanism for regulating organelle structure and membrane traffic. Cell. 1991;67(3):601–616. doi:10.1016/0092-8674(91)90534-6
  • Wilson IB. Glycosylation of proteins in plants and invertebrates. Curr Opin Struct Biol. 2002;12(5):569–577. doi:10.1016/s0959-440x(02)00367-6
  • Aebi M. N-linked protein glycosylation in the ER. Biochim Biophys Acta. 2013;1833(11):2430–2437. doi:10.1016/j.bbamcr.2013.04.001
  • Díaz-Jiménez DF. Fungal mannosyltransferases as fitness attributes and their contribution to virulence. Curr Protein Pept Sci. 2017;18(11):1065–1073. doi:10.2174/1389203717666160813164253
  • Hall RA, Gow NA. Mannosylation in Candida albicans: role in cell wall function and immune recognition. Mol Microbiol. 2013;90(6):1147–1161. doi:10.1111/mmi.12426
  • Gómez-Gaviria M, Vargas-Macías AP, García-Carnero LC, Martínez-Duncker I, Mora-Montes HM. Role of protein glycosylation in interactions of medically relevant fungi with the host. J Fungi. 2021;7(10):875. doi:10.3390/jof7100875
  • Gow NAR, Netea MG, Munro CA, et al. Immune recognition of Candida albicans beta-glucan by dectin-1. J Infect Dis. 2007;196(10):1565–1571. doi:10.1086/523110
  • Netea MG, Gow NA, Munro CA, et al. Immune sensing of Candida albicans requires cooperative recognition of mannans and glucans by lectin and Toll-like receptors. J Clin Invest. 2006;116(6):1642–1650. doi:10.1172/JCI27114
  • Cambi A, Netea MG, Mora-Montes HM, et al. Dendritic cell interaction with Candida albicans critically depends on N-linked mannan. J Biol Chem. 2008;283(29):20590–20599. doi:10.1074/jbc.M709334200
  • Mora-Montes HM, Bates S, Netea MG, et al. A multifunctional mannosyltransferase family in Candida albicans determines cell wall mannan structure and host-fungus interactions. J Biol Chem. 2010;285(16):12087–12095. doi:10.1074/jbc.M109.081513
  • Saijo S, Iwakura Y. Dectin-1 and Dectin-2 in innate immunity against fungi. Int Immunol. 2011;23(8):467–472. doi:10.1093/intimm/dxr046
  • Yadav B, Mora-Montes HM, Wagener J, et al. Differences in fungal immune recognition by monocytes and macrophages: n-mannan can be a shield or activator of immune recognition. Cell Surf. 2020;6:100042. doi:10.1016/j.tcsw.2020.100042
  • Heinsbroek SE, Taylor PR, Martinez FO, Martinez-Pomares L, Brown GD, Gordon S. Stage-specific sampling by pattern recognition receptors during Candida albicans phagocytosis. PLoS Pathog. 2008;4(11):e1000218. doi:10.1371/journal.ppat.1000218
  • Butler G, Rasmussen MD, Lin MF, et al. Evolution of pathogenicity and sexual reproduction in eight Candida genomes. Nature. 2009;459(7247):657–662. doi:10.1038/nature08064
  • Klis FM, de Koster CG, Brul S. A mass spectrometric view of the fungal wall proteome. Future Microbiol. 2011;6(8):941–951. doi:10.2217/fmb.11.72
  • Karkowska-Kuleta J, Kozik A. Cell wall proteome of pathogenic fungi. Acta Biochim Pol. 2015;62(3):339–351. doi:10.18388/abp.2015_1032
  • Niewiadomska M, Janik A, Perlińska-Lenart U, Piłsyk S, Palamarczyk G, Kruszewska JS. The role of Alg13 N-acetylglucosaminyl transferase in the expression of pathogenic features of Candida albicans. Biochim Biophys Acta Gen Subj. 2017;1861(4):789–801. doi:10.1016/j.bbagen.2017.01.019
  • Woods M, McAlister JA, Geddes-McAlister J. A one health approach to overcoming fungal disease and antifungal resistance. WIREs Mech Dis. 2023;15(4):e1610. doi:10.1002/wsbm.1610
  • Singh A, Singh K, Sharma A, Kaur K, Chadha R, Bedi PMS. Recent advances in antifungal drug development targeting lanosterol 14α-demethylase (CYP51): a comprehensive review with structural and molecular insights. Chem Biol Drug Des. 2023;102(3):606–639. doi:10.1111/cbdd.14266
  • Pérez-García LA, Martínez-Duncker I, Mora Montes HM. The endoplasmic reticulum alpha-glycosidases as potential targets for virus control. Curr Protein Pept Sci. 2017;18(11):1090–1097. doi:10.2174/1389203717666160813161729
  • Rothblatt J, Schekman R. A hitchhiker’s guide to analysis of the secretory pathway in yeast. Methods Cell Biol. 1989;32:3–36. doi:10.1016/s0091-679x(08)61165-6
  • Gómez-Gaviria M, Lozoya-Pérez NE, Staniszewska M, Franco B, Niño-Vega GA, Mora-Montes HM. Loss of Kex2 affects the Candida albicans cell wall and interaction with innate immune cells. J Fungi. 2020;6(2):57. doi:10.3390/jof6020057