Aspergillus fumigatus : Principles of Pathogenesis and Host Defense

Hohl, Tobias M.; Feldmesser, Marta

doi:10.1128/ec.00274-07

Cited by 237Antifungal resistance and susceptibilityFungal and yeast genetics researchFungal Infections and Studies

Aspergillus fumigatus : Principles of Pathogenesis and Host Defense

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Hohl, Tobias M., Feldmesser, Marta·2007·Eukaryotic Cell

DOI 10.1128/ec.00274-07PMC PMC2168400

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Abstract

Aspergillus fumigatus is a ubiquitous saprophytic mold (67) that forms airborne spores (conidia). Humans inhale, on average, hundreds of these infectious propagules daily. In immune competent hosts, these encounters are of no further significance—conidia are killed and cleared by cells of the pulmonary immune system. However, disease occurs when the host response is either too strong or too weak. Thus, understanding how the host interacts with the organism to define this balance is a critical goal, the successful pursuit of which requires recognition of the dynamic nature of both fungal and host molecular participants. In immunocompromised hosts, A. fumigatus represents a major cause of morbidity and mortality. This patient population is expanding due to the increasing use of transplantation for end organ disease, the development of immunosuppressive and myeloablative therapies for autoimmune and neoplastic disease, and the human immunodeficiency virus/AIDS pandemic (38). A. fumigatus is the most common invasive mold infection in these patients, and mortality rates exceed 50% in high-risk groups, such as leukemic patients and hematopoietic stem cell transplant recipients (74). Sensitivity to A. fumigatus antigens is associated with asthma, the prevalence of which is increasing in the developed world, though proving causation has been difficult (49, 54). Regardless, this increased prevalence brings a parallel rise in the number of individuals predisposed to allergic bronchopulmonary aspergillosis, a disease associated with aberrant responses to Aspergillus antigens in the setting of chronic inflammation. The spectrum of invasive, semi-invasive, and allergic disease caused by A. fumigatus is reviewed in several outstanding articles (9, 94). The study of A. fumigatus molecules involved in virulence has been hampered by the lack of an identifiable sexual cycle, limiting classical genetic analysis (21). A recent study, however, indicates that A. fumigatus encodes distinct mating-type loci and the pheromone machinery required for sexual mating (103). Nonetheless, within the past decade, researchers have developed and refined experimental tools to generate mutant strains by homologous recombination (21, 35, 62, 152, 154), utilized RNA interference to repress endogenous transcripts (95), and expressed heterologous genes in A. fumigatus under the control of drug-inducible regulatory elements (145). The completion of the A. fumigatus genome (98) has accelerated gene structure and function studies and made possible comparative genomic analyses with other sequenced Aspergillus species (Aspergillus oryzae and Aspergillus nidulans), as well as other genera of pathogenic (e.g., Candida albicans and Cryptococcus neoformans) and nonpathogenic (e.g., Saccharomyces cerevisiae) fungi. An important insight from the genomes has been that A. fumigatus does not share a common set of genes with other fungal pathogens (98). The types of hosts that are susceptible to invasive aspergillosis and the lack of unique pathways conserved among pathogenic fungi underscore the importance of the host contribution to pathogenesis. Damage from A. fumigatus can result from fungal growth and tissue invasion or from inflammatory cells recruited to sites of infection (130). Included in the latter are responses that are ineffective in clearing the organism, occur in the process of immune reconstitution, or are associated with allergy. For example, in a murine model of chronic granulomatous disease, in which mice have defective phagocyte oxidase systems, administration of killed hyphae results in chronic inflammation due to persistence of fungal elements (92). From the perspective of the mammalian immune system, A. fumigatus represents an organism with continuous respiratory tract exposure that must be cleared from terminal airways with an immune response calibrated to avoid fungal tissue invasion, as well as inflammation-induced tissue damage. Here, we review our growing understanding of the interface between A. fumigatus and host defense mechanisms, with an emphasis on invasive disease in humans and small animal models.

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The mechanisms utilized by A. fumigatus to survive and cause disease in immunocompromised hosts are not fully understood.
“Yet, the mechanisms utilized by A. fumigatus to survive and cause disease in immunocompromised hosts are not fully understood [4].”
From A Sterol-Regulatory Element Binding Protein Is Required for Cell Polarity, Hypoxia Adaptation, Azole Drug Resistance, and Virulence in Aspergillus fumigatus (2008) · cites this paper as [4]

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MEASUREMENT OF HUMORAL ANTIBODIES TO ASPERGILLI *
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Identification of genes of Aspergillus fumigatus up-regulated during growth on endothelial cells
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1,4-Oligoglucosides Inhibit the Binding of Aspergillus fumigatus Conidia to Human Monocytes
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The Aspergillus fumigatus mepB gene encodes an 82 kDa intracellular metalloproteinase structurally related to mammalian thimet oligopeptidases
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Characterization of a Monoclonal Antibody Against Concanavalin A Binding Antigen of Aspergillus Fumigatus
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Monocyte recruitment during infection and inflammation
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IRF4 Transcription Factor-Dependent CD11b+ Dendritic Cells in Human and Mouse Control Mucosal IL-17 Cytokine Responses
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Aspergillus fumigatus—What Makes the Species a Ubiquitous Human Fungal Pathogen?
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What makes Aspergillus fumigatus a successful pathogen? Genes and molecules involved in invasive aspergillosis
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A Sterol-Regulatory Element Binding Protein Is Required for Cell Polarity, Hypoxia Adaptation, Azole Drug Resistance, and Virulence in Aspergillus fumigatus
Willger, S. D., Puttikamonkul, S., Kim, K.-H., Burritt, J. B., Grahl, N., Metzler, L. J., Barbuch, R., Bard, M., Lawrence, C. B., & Cramer, R. A. (2008) · PLoS Pathogens · doi:10.1371/journal.ppat.1000200 · Cited by 345 · see citing works
Inflammatory Monocytes Facilitate Adaptive CD4 T Cell Responses during Respiratory Fungal Infection
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Production of nanoparticles using organisms
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Aspergillusand aspergilloses in wild and domestic animals: a global health concern with parallels to human disease
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Essential Role for Neutrophils but not Alveolar Macrophages at Early Time Points followingAspergillus fumigatusInfection
Mircescu, M. M., Lipuma, L., van Rooijen, N., Pamer, E. G., & Hohl, T. M. (2009) · The Journal of Infectious Diseases · doi:10.1086/600380 · Cited by 216 · see citing works
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The role of acute and chronic respiratory colonization and infections in the pathogenesis of COPD
Leung, J. M., Tiew, P. Y., Aogáin, M. M., Budden, K. F., Yong, V. F. L., Thomas, S. S., Pethe, K., Hansbro, P. M., & Chotirmall, S. H. (2017) · Respirology · doi:10.1111/resp.13032 · Cited by 196 · see citing works
Strain-Dependent Variation in 18S Ribosomal DNA Copy Numbers in Aspergillus fumigatus
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Distinct Roles for Dectin-1 and TLR4 in the Pathogenesis of Aspergillus fumigatus Keratitis
Leal, S. M., Cowden, S., Hsia, Y. C., Ghannoum, M. A., Momany, M., & Pearlman, E. M. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1000976 · Cited by 179 · see citing works
Master and Commander in Fungal Pathogens: the Two-Component System and the HOG Signaling Pathway
Bahn, Y. (2008) · Eukaryotic Cell · doi:10.1128/ec.00323-08 · Cited by 175 · see citing works
Inflammatory Monocytes Orchestrate Innate Antifungal Immunity in the Lung
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Recognition of Aspergillus fumigatus Hyphae by Human Plasmacytoid Dendritic Cells Is Mediated by Dectin-2 and Results in Formation of Extracellular Traps
Loures, F. V., Röhm, M., Lee, C. K., Santos, E., Wang, J. P., Specht, C. A., Calich, V. L. G., Urban, C. F., & Levitz, S. M. (2015) · PLOS Pathogens · doi:10.1371/journal.ppat.1004643 · Cited by 165 · see citing works
Metabolomics ofAspergillus fumigatus
Frisvad, J. C., Rank, C., Nielsen, K. F., & Larsen, T. O. (2008) · Medical Mycology · doi:10.1080/13693780802307720 · Cited by 162 · see citing works
Differences in pathogenicity and clinical syndromes due toAspergillus fumigatusandAspergillus flavus
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Dectin-1 diversifies Aspergillus fumigatus–specific T cell responses by inhibiting T helper type 1 CD4 T cell differentiation
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Toll-Like Receptor 9-Dependent Immune Activation by Unmethylated CpG Motifs in Aspergillus fumigatus DNA
Ramirez‐Ortiz, Z. G., Specht, C. A., Wang, J. P., Lee, C. K., Bartholomeu, D. C., Gazzinelli, R. T., & Levitz, S. M. (2008) · Infection and Immunity · doi:10.1128/iai.00047-08 · Cited by 151 · see citing works
The innate immune response to Aspergillus fumigatus at the alveolar surface
Margalit, A., & Kavanagh, K. A. (2015) · FEMS Microbiology Reviews · doi:10.1093/femsre/fuv018 · Cited by 129 · see citing works
Molecular Mechanisms of Conidial Germination in Aspergillus spp
Baltussen, T. J. H., Zoll, J., Verweij, P. E., & Melchers, W. J. G. (2019) · Microbiology and Molecular Biology Reviews · doi:10.1128/mmbr.00049-19 · Cited by 129 · see citing works
Expression of Innate and Adaptive Immune Mediators in Human Corneal Tissue Infected With Aspergillus or Fusarium
Karthikeyan, R. S. G., Leal, S. M., Prajna, N. V., Dharmalingam, K., Geiser, D. M., Pearlman, E. M., & Lalitha, P. (2011) · The Journal of Infectious Diseases · doi:10.1093/infdis/jir426 · Cited by 125 · see citing works
A Nonredundant Role for Plasmacytoid Dendritic Cells in Host Defense against the Human Fungal Pathogen Aspergillus fumigatus
Ramirez-Ortiz, Z. G., Lee, C. K., Wang, J. P., Boon, L., Specht, C. A., & Levitz, S. M. (2011) · Cell Host & Microbe · doi:10.1016/j.chom.2011.04.007 · Cited by 121 · see citing works
Pathophysiological aspects of Aspergillus colonization in disease.
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Rapid Host Defense against Aspergillus fumigatus Involves Alveolar Macrophages with a Predominance of Alternatively Activated Phenotype
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The role of fungi in fungal keratitis
Mills, B., Radhakrishnan, N., Karthikeyan, R. S. G., Rameshkumar, G., Lalitha, P., & Prajna, N. V. (2020) · Experimental Eye Research · doi:10.1016/j.exer.2020.108372 · Cited by 118 · see citing works
Invasive aspergillosis in glucocorticoid-treated patients
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Coevolution of TH1, TH2, and TH17 Responses during Repeated Pulmonary Exposure toAspergillus fumigatusConidia
Murdock, B. J., Shreiner, A. B., McDonald, R. A., Osterholzer, J. J., White, E. S., Toews, G. B., & Huffnagle, G. B. (2010) · Infection and Immunity · doi:10.1128/iai.00508-10 · Cited by 105 · see citing works
Immune responses against Aspergillus fumigatus
Cramer, R. A., Rivera, A., & Hohl, T. M. (2011) · Current Opinion in Infectious Diseases · doi:10.1097/qco.0b013e328348b159 · Cited by 99 · see citing works
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The cryptic sexual strategies of human fungal pathogens
Ene, I. V., & Bennett, R. J. (2014) · Nature Reviews Microbiology · doi:10.1038/nrmicro3236 · Cited by 99 · see citing works
Azole Resistance In Aspergillus Fumigatus : A New Challenge In The Management Of Invasive Aspergillosis?
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Aspergillus fumigatus CalA Binds to Integrin α5β1 and Mediates Host Cell Invasion
Liu, H., Lee, M. J., Solis, N., Phan, Q., Swidergall, M., Ralph, B., Ibrahim, A., Sheppard, D., & Filler, S. (2016) · Nature Microbiology · doi:10.1038/nmicrobiol.2016.211 · Cited by 88 · see citing works
Targeting CBLB as a potential therapeutic approach for disseminated candidiasis
Xiao, Y., Tang, J., Guo, H., Zhao, Y., Tang, R., Ouyang, S., Zeng, Q., Rappleye, C. A., Rajaram, M. V. S., Schlesinger, L. S., et al. (2016) · Nature Medicine · doi:10.1038/nm.4141 · Cited by 92 · see citing works
Hidden killers: persistence of opportunistic fungal pathogens in the human host
d’Enfert, C. (2009) · Current Opinion in Microbiology · doi:10.1016/j.mib.2009.05.008 · Cited by 90 · see citing works
Aspergillus fumigatus: virulence genes in a street-smart mold
Askew, D. S. (2008) · Current Opinion in Microbiology · doi:10.1016/j.mib.2008.05.009 · Cited by 89 · see citing works
Phagocytosis of melanized Aspergillus conidia by macrophages exerts cytoprotective effects by sustained PI3K/Akt signalling
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Synthesis of a PEGylated Dopamine Ester with Enhanced Antibacterial and Antifungal Activity
Thakur, A., Ranote, S., Kumar, D., Bhardwaj, K. K., Gupta, R., & Chauhan, G. S. (2018) · ACS Omega · doi:10.1021/acsomega.8b01099 · Cited by 88 · see citing works
Phylogenetic analyses of eurotiomycetous endophytes reveal their close affinities to Chaetothyriales, Eurotiales, and a new order – Phaeomoniellales
Chen, K., Miądlikowska, J., Molnár, K., Arnold, A. E., U’Ren, J. M., Gaya, E., Gueidan, C., & Lutzoni, F. M. (2015) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2015.01.008 · Cited by 83 · see citing works
VeA Regulates Conidiation, Gliotoxin Production, and Protease Activity in the Opportunistic Human Pathogen Aspergillus fumigatus
Dhingra, S., Andes, D. R., & Calvo, A. M. (2012) · Eukaryotic Cell · doi:10.1128/ec.00222-12 · Cited by 83 · see citing works
Allergic bronchopulmonary aspergillosis and Aspergillus infection in cystic fibrosis
Moss, R. B. (2010) · Current Opinion in Pulmonary Medicine · doi:10.1097/mcp.0b013e32833e24a6 · Cited by 81 · see citing works
Embryonated Eggs as an Alternative Infection Model To InvestigateAspergillus fumigatusVirulence
Jacobsen, I. D., Große, K., Slesiona, S., Hube, B., Berndt, A., & Brock, M. (2010) · Infection and Immunity · doi:10.1128/iai.00268-10 · Cited by 78 · see citing works
First Line of Defense: Innate Cell-Mediated Control of Pulmonary Aspergillosis
Espinosa, V., & Rivera, A. (2016) · Frontiers in Microbiology · doi:10.3389/fmicb.2016.00272 · Cited by 77 · see citing works
Eosinophils Are Recruited in Response to Chitin Exposure and Enhance Th2-Mediated Immune Pathology in Aspergillus fumigatus Infection
O’Dea, E. M., Amarsaikhan, N., Li, H., Downey, J., Steele, E., Dyken, S. J. V., Locksley, R. M., & Templeton, S. P. (2014) · Infection and Immunity · doi:10.1128/iai.01990-14 · Cited by 73 · see citing works
The Fumagillin Gene Cluster, an Example of Hundreds of Genes under veA Control in Aspergillus fumigatus
Dhingra, S., Lind, A., Lin, H., Tang, Y., Rokas, A., & Calvo, A. M. (2013) · PLoS ONE · doi:10.1371/journal.pone.0077147 · Cited by 71 · see citing works
Developmental regulators in Aspergillus fumigatus
Park, H.-S., & Yu, J. (2016) · The Journal of Microbiology · doi:10.1007/s12275-016-5619-5 · Cited by 71 · see citing works
Distinct Responses of Human Monocyte Subsets to Aspergillus fumigatus Conidia
Serbina, N. V., Cherny, M., Shi, C., Bleau, S. A., Collins, N. H., Young, J. W., & Pamer, E. G. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0803398 · Cited by 70 · see citing works
The Multifaceted Role of T-Helper Responses in Host Defense against Aspergillus fumigatus
Dewi, I., Van de Veerdonk, F., & Gresnigt, M. (2017) · Journal of Fungi · doi:10.3390/jof3040055 · Cited by 69 · see citing works
Allergic bronchopulmonary aspergillosis in patients with cystic fibrosis
Janahi, I. A., Rehman, A., & Al-Naimi, A. R. (2017) · Annals of Thoracic Medicine · doi:10.4103/atm.atm_231_16 · Cited by 67 · see citing works
Fast-track development of an in vitro 3D lung/immune cell model to study Aspergillus infections
Chandorkar, P., Posch, W., Zaderer, V., Blatzer, M., Steger, M., Ammann, C. G., Binder, U., Hermann, M., Hörtnagl, P., Lass‐Flörl, C., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-11271-4 · Cited by 67 · see citing works
The Aspergillus fumigatus conidial melanin production is regulated by the bifunctional bHLH DevR and MADS‐box RlmA transcription factors
Valiante, V., Baldin, C., Hortschansky, P., Jain, R., Thywißen, A., Straßburger, M., Shelest, E., Heinekamp, T., & Brakhage, A. A. (2016) · Molecular Microbiology · doi:10.1111/mmi.13462 · Cited by 63 · see citing works
Noninvasive Pulmonary Aspergillus Infections
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Causes of Death in a Contemporary Cohort of Patients with Invasive Aspergillosis
García‐Vidal, C., Peghin, M., Cervera, C., Gudiol, C., Ruíz-Camps, I., Moreno, A., Royo, C., Roselló, E., de la Bellacasa, J. P., Ayats, J., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0120370 · Cited by 63 · see citing works
Regulation of hypoxia adaptation: an overlooked virulence attribute of pathogenic fungi?
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Tissue-Resident Macrophages in Fungal Infections
Xu, S., & Shinohara, M. L. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01798 · Cited by 57 · see citing works
Pyomelanin Formation in Aspergillus fumigatus Requires HmgX and the Transcriptional Activator HmgR but Is Dispensable for Virulence
Keller, S., Macheleidt, J., Scherlach, K., Schmaler-Ripcke, J., Jacobsen, I. D., Heinekamp, T., & Brakhage, A. A. (2011) · PLoS ONE · doi:10.1371/journal.pone.0026604 · Cited by 57 · see citing works
Neutropenia Enhances Lung Dendritic Cell Recruitment in Response to Aspergillus via a Cytokine-to-Chemokine Amplification Loop
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Comparative systems analysis of the secretome of the opportunistic pathogen Aspergillus fumigatus and other Aspergillus species
Vivek-Ananth, R. P., Mohanraj, K., Vandanashree, M., Jhingran, A., Craig, J. P., & Samal, A. (2018) · Scientific Reports · doi:10.1038/s41598-018-25016-4 · Cited by 57 · see citing works
Fungal Aflatoxins Reduce Respiratory Mucosal Ciliary Function
Lee, R. J., Workman, A., Carey, R., Chen, B., Rosen, P. L., Doghramji, L., Adappa, N., Palmer, J., Kennedy, D., & Cohen, N. (2016) · Scientific Reports · doi:10.1038/srep33221 · Cited by 60 · see citing works
Menacing Mold: Recent Advances in Aspergillus Pathogenesis and Host Defense
Tischler, B. Y., & Hohl, T. M. (2019) · Journal of Molecular Biology · doi:10.1016/j.jmb.2019.03.027 · Cited by 55 · see citing works
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The Small GTPase RacA Mediates Intracellular Reactive Oxygen Species Production, Polarized Growth, and Virulence in the Human Fungal Pathogen Aspergillus fumigatus
Li, H., Barker, B. M., Grahl, N., Puttikamonkul, S., Bell, J. D., Craven, K. D., & Cramer, R. A. (2010) · Eukaryotic Cell · doi:10.1128/ec.00288-10 · Cited by 55 · see citing works
CD4+T Cells Mediate the Protective Effect of the Recombinant Asp f3-Based Anti-Aspergillosis Vaccine
Díaz-Arévalo, D., Bagramyan, K. A., Hong, T., Ito, J. I., & Kalkum, M. (2011) · Infection and Immunity · doi:10.1128/iai.01311-10 · Cited by 53 · see citing works
Immuno-Reactive Molecules Identified from the Secreted Proteome of Aspergillus fumigatus
Singh, B., Oellerich, M., Kumar, R. P., Kumar, M., Bhadoria, D. P., Reichard, U., Gupta, V. K., Sharma, G. L., & Asif, A. R. (2010) · Journal of Proteome Research · doi:10.1021/pr100604x · Cited by 53 · see citing works
Klebsiella pneumoniae prevents spore germination and hyphal development of Aspergillus species
Nogueira, F., Pereira, L., Jenull, S., Kuchler, K., & Lion, T. (2019) · Scientific Reports · doi:10.1038/s41598-018-36524-8 · Cited by 50 · see citing works
Citizen science reveals landscape-scale exposures to multiazole-resistant Aspergillus fumigatus bioaerosols
Shelton, J., Rhodes, J. L., Uzzell, C. B., Hemmings, S., Brackin, A. P., Sewell, T. R., Alghamdi, A., Dyer, P. S., Fraser, M., Borman, A. M., et al. (2023) · Science Advances · doi:10.1126/sciadv.adh8839 · Cited by 50 · see citing works
Post-Translational Modifications Drive Success and Failure of Fungal–Host Interactions
Retanal, C., Ball, B., & Geddes‐McAlister, J. (2021) · Journal of Fungi · doi:10.3390/jof7020124 · Cited by 49 · see citing works
Citizen Science Surveillance of Triazole-Resistant Aspergillus fumigatus in United Kingdom Residential Garden Soils
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Authors: Hohl, T. M., & Feldmesser, M.
Affiliations: Memorial Sloan Kettering Cancer Center (US)
Albert Einstein College of Medicine (US)
ORCID: Hohl, Tobias M.
Venue: Eukaryotic Cell
Publisher: American Society for Microbiology
Published: 2007-11
Volume: 6
Issue: 11
Pages: 1953-1963
ISSN: 1535-9778 (ISSN-L)
1535-9786
DOI: 10.1128/ec.00274-07
PMC: PMC2168400
OpenAlex: W2096728005
Cited by: 237
References: 163
Citations by year: 2026: 8 · 2025: 7 · 2024: 9 · 2023: 9 · 2022: 12 · 2021: 13 · 2020: 6 · 2019: 16 · 2018: 12 · 2017: 17 · 2016: 15 · 2015: 13 · 2014: 21 · 2013: 13 · 2012: 12
FWCI: 1.41
Type: journal article
Language: en
Open access: diamond
doi.org
Licence: journals.asm.org/non-commercial-tdm-license (tdm)
Locations: Eukaryotic Cell (publishedVersion)
PubMed Central (publishedVersion)
PubMed (publishedVersion)
Funders: Charles H. Revson Foundation
National Institutes of Health
National Institute of Allergy and Infectious Diseases (R01AI059663)
Topics: Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
Health Sciences › Medicine › Epidemiology › Fungal Infections and Studies
Keywords: Aspergillus fumigatus, pathogenesis, host defense, immunocompromised patients, invasive aspergillosis, allergic bronchopulmonary aspergillosis, fungal virulence factors, conidia, pulmonary immune response, antifungal resistance, antifungal susceptibility testing, antifungal therapy, immunosuppression
MeSH terms: Animals, Aspergillus fumigatus, Host-Parasite Interactions, Humans, Mammals

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Aspergillus fumigatus : Principles of Pathogenesis and Host Defense

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