The Mnn2 Mannosyltransferase Family Modulates Mannoprotein Fibril Length, Immune Recognition and Virulence of Candida albicans

Hall, Rebecca A.; Bates, Steven; Lenardon, Megan D.; MacCallum, Donna M.; Wagener, Jeanette; Lowman, Douglas W.; Kruppa, Michael D.; Williams, David L.; Odds, Frank C.; Brown, Alistair J. P.; Gow, Neil A. R.

doi:10.1371/journal.ppat.1003276

Cited by 128Fungal and yeast genetics researchGlycosylation and Glycoproteins ResearchAntifungal resistance and susceptibility

The Mnn2 Mannosyltransferase Family Modulates Mannoprotein Fibril Length, Immune Recognition and Virulence of Candida albicans

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Hall, Rebecca A., Bates, Steven, Lenardon, Megan D., MacCallum, Donna M., Wagener, Jeanette, Lowman, Douglas W., Kruppa, Michael D., Williams, David L. +3 more·2013·PLoS Pathogens

DOI 10.1371/journal.ppat.1003276PMC PMC3636026

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Abstract

The fungal cell wall is the first point of interaction between an invading fungal pathogen and the host immune system. The outer layer of the cell wall is comprised of GPI anchored proteins, which are post-translationally modified by both N- and O-linked glycans. These glycans are important pathogen associated molecular patterns (PAMPs) recognised by the innate immune system. Glycan synthesis is mediated by a series of glycosyl transferases, located in the endoplasmic reticulum and Golgi apparatus. Mnn2 is responsible for the addition of the initial α1,2-mannose residue onto the α1,6-mannose backbone, forming the N-mannan outer chain branches. In Candida albicans, the MNN2 gene family is comprised of six members (MNN2, MNN21, MNN22, MNN23, MNN24 and MNN26). Using a series of single, double, triple, quintuple and sextuple mutants, we show, for the first time, that addition of α1,2-mannose is required for stabilisation of the α1,6-mannose backbone and hence regulates mannan fibril length. Sequential deletion of members of the MNN2 gene family resulted in the synthesis of lower molecular weight, less complex and more uniform N-glycans, with the sextuple mutant displaying only un-substituted α1,6-mannose. TEM images confirmed that the sextuple mutant was completely devoid of the outer mannan fibril layer, while deletion of two MNN2 orthologues resulted in short mannan fibrils. These changes in cell wall architecture correlated with decreased proinflammatory cytokine induction from monocytes and a decrease in fungal virulence in two animal models. Therefore, α1,2-mannose of N-mannan is important for both immune recognition and virulence of C. albicans.

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Cell wall and extracellular matrix polysaccharides have mechanistic roles implicated in protection of Candida species from host response and drug therapies.
“Cell wall and extracellular matrix polysaccharides have mechanistic roles implicated in the protection of Candida species from host response and drug therapies (13–16).”
From Dual function of Candida auris mannosyltransferase, MNT5, in biofilm community protection from antifungal therapy and the host (2025) · cites this paper as [14]
The Discussion (page not provided) describes cell-wall N-mannan as a shield that masks a pro-inflammatory β-glucan layer and links increased β-glucan exposure to enhanced macrophage recognition. This supports a mechanism involving protection from the host response in C. albicans, but the paper does not establish the claimed roles for extracellular-matrix polysaccharides, protection from drug therapies, or Candida species generally. (LLM, conf=0.87)
Experimental — accuracy not yet measured
C. albicans has a well-characterized cell wall composed of an inner layer of chitin, β-1,3-glucan, and β-1,6-glucan, and an outer layer composed of proteins modified with N- and O-linked mannans and phosphomannans.
“C. albicans has a well-characterized cell wall composed of an inner layer of chitin, β−1,3-glucan, and β−1,6-glucan, and an outer layer composed of proteins modified with N- and O-linked mannans and phosphomannans, called mannoproteins34,35.”
From Distinct echinocandin responses of Candida albicans and Candida auris cell walls revealed by solid-state NMR (2025) · cites this paper as [34]

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[18]Netea MG, Gow NAR, Joosten LAB, Verschueren I, van der Meer JWM, et al (2010) Variable recognition of Candida albicans strains by TLR4 and lectin recognition receptors. Med Mycol 48: 897– 903. 20166865

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Lactate signalling regulates fungal β-glucan masking and immune evasion
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Metabolism impacts upon Candida immunogenicity and pathogenicity at multiple levels
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Draft genome of a commonly misdiagnosed multidrug resistant pathogen Candida auris
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Mannosylation in C andida albicans : role in cell wall function and immune recognition
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Antimicrobial activity, improved cell selectivity and mode of action of short PMAP-36-derived peptides against bacteria and Candida
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Adaptation of Candida albicans to environmental pH induces cell wall remodelling and enhances innate immune recognition
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Candida albicans, plasticity and pathogenesis
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The Viscoelastic Properties of the Fungal Cell Wall Allow Traffic of AmBisome as Intact Liposome Vesicles
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Candida albicans Hypha Formation and Mannan Masking of β-Glucan Inhibit Macrophage Phagosome Maturation
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Targeting the Fungal Cell Wall: Current Therapies and Implications for Development of Alternative Antifungal Agents
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Activity and Mechanism of Action of Antifungal Peptides from Microorganisms: A Review
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Scalar nanostructure of the Candida albicans cell wall; a molecular, cellular and ultrastructural analysis and interpretation
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Divergent Approaches to Virulence in C. albicans and C. glabrata: Two Sides of the Same Coin
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Mannan detecting C-type lectin receptor probes recognise immune epitopes with diverse chemical, spatial and phylogenetic heterogeneity in fungal cell walls
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Mannan Molecular Substructures Control Nanoscale Glucan Exposure in Candida
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Role of Protein Glycosylation in Candida parapsilosis Cell Wall Integrity and Host Interaction
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Medical mycology and fungal immunology: new research perspectives addressing a major world health challenge
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Dressed to impress: impact of environmental adaptation on the C andida albicans cell wall
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Nature of β-1,3-Glucan-Exposing Features on Candida albicans Cell Wall and Their Modulation
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High-Throughput Screening Identifies Genes Required for Candida albicans Induction of Macrophage Pyroptosis
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Differences in fungal immune recognition by monocytes and macrophages: N-mannan can be a shield or activator of immune recognition
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Inhibition of Classical and Alternative Modes of Respiration in Candida albicans Leads to Cell Wall Remodeling and Increased Macrophage Recognition
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“Wheat germ agglutinin (WGA) binds chitin in fungal cell walls but, due to its large size, cannot penetrate the cell wall to stain chitin in the innermost layers where it is usually found (41).”
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Biosynthesis of cell wall mannan in the conidium and the mycelium ofAspergillusfumigatus
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Candida albicans enhances meropenem tolerance of Pseudomonas aeruginosa in a dual-species biofilm
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An Acquired and Endogenous Glycocalyx Forms a Bidirectional “Don’t Eat” and “Don’t Eat Me” Barrier to Phagocytosis
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Yeast species-specific, differential inhibition of β-1,3-glucan synthesis by poacic acid and caspofungin
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Distinct echinocandin responses of Candida albicans and Candida auris cell walls revealed by solid-state NMR
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Disruption of Protein Mannosylation Affects Candida guilliermondii Cell Wall, Immune Sensing, and Virulence
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Contribution of Fdh3 and Glr1 to Glutathione Redox State, Stress Adaptation and Virulence in Candida albicans
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Alpha‐ and beta‐mannan utilization by marine Bacteroidetes
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Two KTR Mannosyltransferases Are Responsible for the Biosynthesis of Cell Wall Mannans and Control Polarized Growth in Aspergillus fumigatus
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Fungal cell wall components modulate our immune system
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Mnn10 Maintains Pathogenicity in Candida albicans by Extending α-1,6-Mannose Backbone to Evade Host Dectin-1 Mediated Antifungal Immunity
Zhang, S. Q., Zou, Z., Shen, H., Shuai, S. S., Miao, Q., Huang, X., Liu, W., Li, L. P., Chen, S. M., Yan, L., et al. (2016) · PLoS Pathogens · doi:10.1371/journal.ppat.1005617 · Cited by 41 · see citing works
Targeted gene disruption in Candida parapsilosis demonstrates a role for CPAR2_404800 in adhesion to a biotic surface and in a murine model of ascending urinary tract infection
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Phosphomannosylation and the Functional Analysis of the Extended Candida albicans MNN4-Like Gene Family
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Phosphoric Metabolites Link Phosphate Import and Polysaccharide Biosynthesis for Candida albicans Cell Wall Maintenance
Liu, N., Acosta‐Zaldívar, M., Qi, W., Diray‐Arce, J., Walker, L. A., Kottom, T. J., Kelly, R., Yuan, M., Asara, J. M., Lasky-Su, J. A., et al. (2020) · mBio · doi:10.1128/mbio.03225-19 · Cited by 33 · see citing works
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Transcriptomics and Phenotyping Define Genetic Signatures Associated with Echinocandin Resistance in Candida auris
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“tions (51) and alterations in the abundances of cell wall-modulating enzymes (52, 53)”
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The Role of Secretory Pathways in Candida albicans Pathogenesis
Rollenhagen, C., Mamtani, S. S., Ma, D., Dixit, R., Eszterhas, S. K., & Lee, S. A. (2020) · Journal of Fungi · doi:10.3390/jof6010026 · Cited by 32 · see citing works
Accessibility and contribution to glucan masking of natural and genetically tagged versions of yeast wall protein 1 of Candida albicans
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Toll-like receptor 4 (TLR4) is the major pattern recognition receptor triggering the protective effect of a Candida albicans extracellular vesicle-based vaccine prototype in murine systemic candidiasis
Honorato, L., Bonilla, J. J. A., Valdez, A. F., Frasés, S., Araújo, G. R. D. S., Sabino, A. L. R. D. N., da Silva, N. M., Ribeiro, L., Ferreira, M. D. S., Kornetz, J., et al. (2024) · mSphere · doi:10.1128/msphere.00467-24 · Cited by 30 · see citing works
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Dependence on Dectin-1 Varies With Multiple Candida Species
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Impact of the Environment upon the Candida albicans Cell Wall and Resultant Effects upon Immune Surveillance
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High molecular weight chitosan oligosaccharide exhibited antifungal activity by misleading cell wall organization via targeting PHR transglucosidases
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Comparative Analysis of Protein Glycosylation Pathways in Humans and the Fungal PathogenCandida albicans
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Role of the Candida albicans MNN1 gene family in cell wall structure and virulence
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β-1,6-Glucan plays a central role in the structure and remodeling of the bilaminate fungal cell wall
Bekirian, C., Valsecchi, I., Bachellier-Bassi, S., Scandola, C., Guijarro, J. I., Chauvel, M., Mourer, T., Gow, N. A., Aimanianda, V. K., d'Enfert, C., et al. (2024) · eLife · doi:10.7554/elife.100569.3 · Cited by 28 · see citing works
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Candida albicans N-Linked Mannans Potentiate the Induction of Trained Immunity via Dectin-2
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Role of protein phosphomannosylation in the Candida tropicalis–macrophage interaction
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Silencing of OCH1 unveils the role of Sporothrix schenckii N-linked glycans during the host–fungus interaction
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Cell Wall N-Linked Mannoprotein Biosynthesis Requires Goa1p, a Putative Regulator of Mitochondrial Complex I in Candida albicans
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Core N -Glycan Structures Are Critical for the Pathogenicity of Cryptococcus neoformans by Modulating Host Cell Death
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Role of Protein Glycosylation in Interactions of Medically Relevant Fungi with the Host
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Mannosylation of fungal glycoconjugates in the Golgi apparatus
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Candida albicans β-Glucan-Containing Particles Increase HO-1 Expression in Oral Keratinocytes via a Reactive Oxygen Species/p38 Mitogen-Activated Protein Kinase/Nrf2 Pathway
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Antifungal peptides: Therapeutic potential and challenges before their commercial success
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Identification of Membrane Proteome of Paracoccidioides Lutzii and its Regulation by Zinc
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Evolutionarily Conserved and Divergent Roles of Unfolded Protein Response (UPR) in the Pathogenic Cryptococcus Species Complex
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Antifungal mechanism of p-anisaldehyde against Aspergillus flavus based on transcriptome analysis
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Role of Protein Mannosylation in the Candida tropicalis-Host Interaction
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Mannose-Binding Lectin: A Potential Therapeutic Candidate against Candida Infection
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β-1,2-Mannosyltransferases 1 and 3 Participate in Yeast and Hyphae O- and N-Linked Mannosylation and Alter Candida albicans Fitness During Infection
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Impaired amino acid uptake leads to global metabolic imbalance of Candida albicans biofilms
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The ER stress response and host temperature adaptation in the human fungal pathogenCryptococcus neoformans
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The role of manganese in morphogenesis and pathogenesis of the opportunistic fungal pathogen Candida albicans
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Bst1 is required for Candida albicans infecting host via facilitating cell wall anchorage of Glycosylphosphatidyl inositol anchored proteins
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Revisiting the Vital Drivers and Mechanisms of β-Glucan Masking in Human Fungal Pathogen, Candida albicans
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A Candida albicans regulator of disseminated infection operates primarily as a repressor and governs cell surface remodeling
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The MNN2 Gene Knockout Modulates the Antifungal Resistance of Biofilms of Candida glabrata
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Importance of Candida Antigenic Factors: Structure-Driven Immunomodulation Properties of Synthetically Prepared Mannooligosaccharides in RAW264.7 Macrophages
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A CO 2 sensing module modulates β-1,3-glucan exposure in Candida albicans
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Effects of altered N-glycan structures of Cryptococcus neoformans mannoproteins, MP98 (Cda2) and MP84 (Cda3), on interaction with host cells
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Authors: Hall, R. A., Bates, S., Lenardon, M. D., MacCallum, D. M., Wagener, J., Lowman, D. W., Kruppa, M. D., Williams, D. L., Odds, F. C., Brown, A. J. P., & Gow, N. A. R.
Affiliations: University of Aberdeen (GB)
University of Exeter (GB)
East Tennessee State University (US)
Corresponding author: Gow, Neil A. R.
ORCID: Hall, Rebecca A.
Bates, Steven
Lenardon, Megan D.
MacCallum, Donna M.
Wagener, Jeanette
Lowman, Douglas W.
Kruppa, Michael D.
Williams, David L.
Brown, Alistair J. P.
Gow, Neil A. R.
Venue: PLoS Pathogens
Publisher: Public Library of Science (PLoS)
Published: 2013-04-25
Volume: 9
Issue: 4
Pages: e1003276
ISSN: 1553-7366 (ISSN-L)
1553-7374
DOI: 10.1371/journal.ppat.1003276
PMC: PMC3636026
OpenAlex: W2086193922
Cited by: 128
References: 60
Citations by year: 2026: 8 · 2025: 9 · 2024: 13 · 2023: 4 · 2022: 12 · 2021: 6 · 2020: 9 · 2019: 10 · 2018: 16 · 2017: 9 · 2016: 11 · 2015: 9 · 2014: 6 · 2013: 6
FWCI: 4.78
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (unspecified)
Locations: PLoS Pathogens (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Kent Academic Repository (University of Kent) (acceptedVersion)
Aberdeen University Research Archive (Aberdeen University) (submittedVersion)
Digital Commons - East Tennessee State University (East Tennessee State University) (submittedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Figshare (submittedVersion, cc-by)
Open Research Exeter (University of Exeter) (submittedVersion)
University of Birmingham Research Portal (University of Birmingham) (submittedVersion, cc-by)
University of Birmingham Research Portal (University of Birmingham) (submittedVersion, other-oa)
Funders: Wellcome Trust (099215, 086827, 080088, 075470)
European Commission (260338)
Medical Research Council (MR/J008230/1)
Biotechnology and Biological Sciences Research Council (BB/F00513X/1)
National Institute of General Medical Sciences (R01GM053522)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Glycosylation and Glycoproteins Research
Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
Keywords: Candida albicans, fungal cell wall, glycosyltransferases, pathogen-associated molecular patterns, innate immune recognition, inflammatory cytokines, fungal virulence, GPI-anchored proteins, N-glycans
MeSH terms: Animals, Candida albicans, Candidiasis, Cell Wall, Female, Fungal Proteins, Humans, Mannans, Mannose, Mannosyltransferases, Membrane Glycoproteins, Mice, Inbred BALB C, Polysaccharides, Sequence Alignment, Sequence Deletion, Receptors, Pattern Recognition, Mice

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The Mnn2 Mannosyltransferase Family Modulates Mannoprotein Fibril Length, Immune Recognition and Virulence of Candida albicans

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