-
Články
- Časopisy
- Kurzy
- Témy
- Kongresy
- Videa
- Podcasty
The Fungal Exopolysaccharide Galactosaminogalactan Mediates Virulence by Enhancing Resistance to Neutrophil Extracellular Traps
The ubiquitous mold A. fumigatus is isolated in over 80% of all patients with invasive aspergillosis (IA). A. nidulans is a relatively non-pathogenic species that rarely causes IA except in patients with chronic granulomatous disease (CGD), a hereditary disease characterized by impaired neutrophil function due to mutations in the NADPH oxidase complex. Here, we demonstrate that one factor underlying the differences in the intrinsic virulence between A. fumigatus and A. nidulans is the amount of the exopolysaccharide galactosaminogalactan that is associated with the cell wall of these species. A. fumigatus produces higher amounts of cell wall-associated galactosaminogalactan and is more resistant than A. nidulans to neutrophil killing by NADPH-oxidase dependent extracellular traps (NETs). Increasing cell wall-associated galactosaminogalactan in A. nidulans enhanced resistance to NETs and increased the virulence of this species to the same level as A. fumigatus in mice with intact NET formation. Collectively, these data suggest that A. nidulans is more sensitive than A. fumigatus to NADPH-oxidase dependent NETosis due to lower levels of cell wall-associated GAG.
Vyšlo v časopise: The Fungal Exopolysaccharide Galactosaminogalactan Mediates Virulence by Enhancing Resistance to Neutrophil Extracellular Traps. PLoS Pathog 11(10): e32767. doi:10.1371/journal.ppat.1005187
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1005187Souhrn
The ubiquitous mold A. fumigatus is isolated in over 80% of all patients with invasive aspergillosis (IA). A. nidulans is a relatively non-pathogenic species that rarely causes IA except in patients with chronic granulomatous disease (CGD), a hereditary disease characterized by impaired neutrophil function due to mutations in the NADPH oxidase complex. Here, we demonstrate that one factor underlying the differences in the intrinsic virulence between A. fumigatus and A. nidulans is the amount of the exopolysaccharide galactosaminogalactan that is associated with the cell wall of these species. A. fumigatus produces higher amounts of cell wall-associated galactosaminogalactan and is more resistant than A. nidulans to neutrophil killing by NADPH-oxidase dependent extracellular traps (NETs). Increasing cell wall-associated galactosaminogalactan in A. nidulans enhanced resistance to NETs and increased the virulence of this species to the same level as A. fumigatus in mice with intact NET formation. Collectively, these data suggest that A. nidulans is more sensitive than A. fumigatus to NADPH-oxidase dependent NETosis due to lower levels of cell wall-associated GAG.
Zdroje
1. Garcia-Vidal C, Upton A, Kirby KA, Marr KA (2008) Epidemiology of invasive mold infections in allogeneic stem cell transplant recipients: biological risk factors for infection according to time after transplantation. Clinical infectious diseases: an official publication of the Infectious Diseases Society of America 47 : 1041–1050.
2. Geiser DM, Klich MA, Frisvad JC, Peterson SW, Varga J, et al. (2007) The current status of species recognition and identification in Aspergillus. Studies in Mycology 59 : 1–10. doi: 10.3114/sim.2007.59.01 18490947
3. Lucas GM, Tucker P, Merz WG (1999) Primary Cutaneous Aspergillus nidulans Infection Associated with a Hickman Catheter in a Patient with Neutropenia. Clinical Infectious Diseases 29 : 1594–1596. 10585834
4. Henriet SS, Verweij PE, Warris A (2012) Aspergillus nidulans and chronic granulomatous disease: a unique host-pathogen interaction. J Infect Dis 206 : 1128–1137. doi: 10.1093/infdis/jis473 22829648
5. Song E, Jaishankar GB, Saleh H, Jithpratuck W, Sahni R, et al. (2011) Chronic granulomatous disease: a review of the infectious and inflammatory complications. Clin Mol Allergy 9 : 10. doi: 10.1186/1476-7961-9-10 21624140
6. Henriet S, Verweij PE, Holland SM, Warris A (2013) Invasive fungal infections in patients with chronic granulomatous disease. Adv Exp Med Biol 764 : 27–55. 23654055
7. Abad A, Fernandez-Molina JV, Bikandi J, Ramirez A, Margareto J, et al. (2010) What makes Aspergillus fumigatus a successful pathogen? Genes and molecules involved in invasive aspergillosis. Rev Iberoam Micol 27 : 155–182. doi: 10.1016/j.riam.2010.10.003 20974273
8. Sales-Campos H, Tonani L, Cardoso CR, Kress MR (2013) The immune interplay between the host and the pathogen in Aspergillus fumigatus lung infection. Biomed Res Int 2013 : 693023. doi: 10.1155/2013/693023 23984400
9. Fontaine T, Delangle A, Simenel C, Coddeville B, van Vliet SJ, et al. (2011) Galactosaminogalactan, a new immunosuppressive polysaccharide of Aspergillus fumigatus. PLoS Pathog. pp. e1002372. doi: 10.1371/journal.ppat.1002372 22102815
10. Gravelat FN, Beauvais A, Liu H, Lee MJ, Snarr BD, et al. (2013) Aspergillus Galactosaminogalactan Mediates Adherence to Host Constituents and Conceals Hyphal β-Glucan from the Immune System. PLoS pathogens. doi: 10.1371/journal.ppat.1003575 23990787
11. Lee MJ, Gravelat FN, Cerone RP, Baptista SD, Campoli PV, et al. (2014) Overlapping and distinct roles of Aspergillus fumigatus UDP-glucose 4-epimerases in galactose metabolism and the synthesis of galactose-containing cell wall polysaccharides. J Biol Chem 289 : 1243–1256. doi: 10.1074/jbc.M113.522516 24257745
12. Gravelat FN, Ejzykowicz DE, Chiang LY, Chabot JC, Urb M, et al. (2010) Aspergillus fumigatus MedA governs adherence, host cell interactions and virulence. Cell Microbiol 12 : 473–488. doi: 10.1111/j.1462-5822.2009.01408.x 19889083
13. Robinet P, Baychelier F, Fontaine T, Picard C, Debre P, et al. (2014) A Polysaccharide Virulence Factor of a Human Fungal Pathogen Induces Neutrophil Apoptosis via NK Cells. J Immunol. doi: 10.4049/jimmunol.1303180 24790151
14. Gresnigt MS, Bozza S, Becker KL, Joosten LA, Abdollahi-Roodsaz S, et al. (2014) A polysaccharide virulence factor from Aspergillus fumigatus elicits anti-inflammatory effects through induction of Interleukin-1 receptor antagonist. PLoS Pathog 10: e1003936. doi: 10.1371/journal.ppat.1003936 24603878
15. Ruperez P, Leal JA (1981) Extracellular galactosaminogalactan from Aspergillus parasiticus. Transactions of the British Mycological Society 77 : 621–625.
16. Bardalaye PC, Nordin JH (1976) Galactosaminogalactan from cell walls of Aspergillus niger. Journal of bacteriology 125 : 655–669. 173713
17. Gorin PAJ, Eveleigh DE (1970) Extracellular 2-acetamido-2-deoxy-D-galacto-D-galactan from Aspergillus nidulans. Biochemistry 9 : 5023–5027. 5480165
18. Leal JA, Ruperez P (1978) Extracellular polysaccharide production by Aspergillus nidulans. Transactions of the British Mycological Society 70 : 115–120.
19. Hedayati MT, Pasqualotto AC, Warn PA, Bowyer P, Denning DW (2007) Aspergillus flavus: human pathogen, allergen and mycotoxin producer. Microbiology (Reading, England) 153 : 1677–1692.
20. Rao VS, Lam K, Qasba PK (1998) Three dimensional structure of the soybean agglutinin Gal/GalNAc complexes by homology modeling. Journal of biomolecular structure & dynamics 15 : 853–860.9619508
21. Dam TK, Gerken TA, Cavada BS, Nascimento KS, Moura TR, et al. (2007) Binding studies of alpha-GalNAc-specific lectins to the alpha-GalNAc (Tn-antigen) form of porcine submaxillary mucin and its smaller fragments. The Journal of biological chemistry 282 : 28256–28263. 17652089
22. Paul BC, El-Ganiny AM, Abbas M, Kaminskyj SGW, Dahms TES (2011) Quantifying the importance of galactofuranose in Aspergillus nidulans hyphal wall surface organization by atomic force microscopy. Eukaryotic cell 10 : 646–653. doi: 10.1128/EC.00304-10 21335527
23. Reeves EP, Lu H, Jacobs HL, Messina CG, Bolsover S, et al. (2002) Killing activity of neutrophils is mediated through activation of proteases by K+ flux. Nature 416 : 291–297. 11907569
24. Segal AW (2005) How neutrophils kill microbes. Annu Rev Immunol 23 : 197–223. 15771570
25. Segal BH, Han W, Bushey JJ, Joo M, Bhatti Z, et al. (2010) NADPH oxidase limits innate immune responses in the lungs in mice. PLoS One 5: e9631. doi: 10.1371/journal.pone.0009631 20300512
26. Bianchi M, Hakkim A, Brinkmann V, Siler U, Seger RA, et al. (2009) Restoration of NET formation by gene therapy in CGD controls aspergillosis. Blood 114 : 2619–2622. doi: 10.1182/blood-2009-05-221606 19541821
27. Bruns S, Kniemeyer O, Hasenberg M, Aimanianda V, Nietzsche S, et al. (2010) Production of extracellular traps against Aspergillus fumigatus in vitro and in infected lung tissue is dependent on invading neutrophils and influenced by hydrophobin RodA. PLoS Pathog 6: e1000873. doi: 10.1371/journal.ppat.1000873 20442864
28. Rohm M, Grimm MJ, D'Auria AC, Almyroudis NG, Segal BH, et al. (2014) NADPH oxidase promotes neutrophil extracellular trap formation in pulmonary aspergillosis. Infect Immun 82 : 1766–1777. doi: 10.1128/IAI.00096-14 24549323
29. Urban CF, Ermert D, Schmid M, Abu-Abed U, Goosmann C, et al. (2009) Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathog 5: e1000639. doi: 10.1371/journal.ppat.1000639 19876394
30. Lamarre C, Beau R, Balloy V, Fontaine T, Wong Sak Hoi J, et al. (2009) Galactofuranose attenuates cellular adhesion of Aspergillus fumigatus. Cellular microbiology 11 : 1612–1623. doi: 10.1111/j.1462-5822.2009.01352.x 19563461
31. Kwon-Chung KJ, Sugui JA (2013) Aspergillus fumigatus—what makes the species a ubiquitous human fungal pathogen? PLoS Pathog 9: e1003743 doi: 10.1371/journal.ppat.1003743 24348239
32. Schaffner A (1985) Therapeutic concentrations of glucocorticoids suppress the antimicrobial activity of human macrophages without impairing their responsiveness to gamma interferon. J Clin Invest 76 : 1755–1764. 3932471
33. Brummer E, Maqbool A, Stevens DA (2001) In vivo GM-CSF prevents dexamethasone suppression of killing of Aspergillus fumigatus conidia by bronchoalveolar macrophages. J Leukoc Biol 70 : 868–872. 11739548
34. Lamarre C, Beau R, Balloy V, Fontaine T, Wong Sak Hoi J, et al. (2009) Galactofuranose attenuates cellular adhesion of Aspergillus fumigatus. Cellular microbiology 11 : 1612–1623. doi: 10.1111/j.1462-5822.2009.01352.x 19563461
35. Henriet SS, Hermans PW, Verweij PE, Simonetti E, Holland SM, et al. (2011) Human leukocytes kill Aspergillus nidulans by reactive oxygen species-independent mechanisms. Infect Immun 79:: 767–773. doi: 10.1128/IAI.00921-10 21078850
36. Campos MA, Vargas MA, Regueiro V, Llompart CM, Alberti S, et al. (2004) Capsule polysaccharide mediates bacterial resistance to antimicrobial peptides. Infect Immun 72 : 7107–7114. 15557634
37. Liu HZ M.; Zhu S. (2011) Persistence of Antibiotic Resistance and Capsule in E. coli B23 after Removal from Sublethal Kanamycin Treatment JEMI 15 : 43–46.
38. Bales PM, Renke EM, May SL, Shen Y, Nelson DC (2013) Purification and Characterization of Biofilm-Associated EPS Exopolysaccharides from ESKAPE Organisms and Other Pathogens. PLoS One 8: e67950. 23805330
39. Lee MJ, Geller AM, Gravelat FN, Liu H, Snarr BD, et al. Deacetylation of Aspergillus fumigatu galactosaminogalactan is required for adherence and virulence; 2014; Madrid, Spain.
40. Vuong C, Kocianova S, Voyich JM, Yao Y, Fischer ER, et al. (2004) A crucial role for exopolysaccharide modification in bacterial biofilm formation, immune evasion, and virulence. J Biol Chem 279 : 54881–54886. 15501828
41. Sheppard DC, Doedt T, Chiang LY, Kim HS, Chen D, et al. (2005) The Aspergillus fumigatus StuA protein governs the up-regulation of a discrete transcriptional program during the acquisition of developmental competence. Mol Biol Cell 16 : 5866–5879. 16207816
42. Campoli P, Al Abdallah Q, Robitaille R, Solis NV, Fielhaber JA, et al. (2011) Concentration of antifungal agents within host cell membranes: a new paradigm governing the efficacy of prophylaxis. Antimicrob Agents Chemother 55 : 5732–5739. doi: 10.1128/AAC.00637-11 21930891
43. Twumasi-Boateng K, Yu Y, Chen D, Gravelat FN, Nierman WC, et al. (2009) Transcriptional profiling identifies a role for BrlA in the response to nitrogen depletion and for StuA in the regulation of secondary metabolite clusters in Aspergillus fumigatus. Eukaryot Cell 8 : 104–115. doi: 10.1128/EC.00265-08 19028996
44. Choe SI, Gravelat FN, Al Abdallah Q, Lee MJ, Gibbs BF, et al. (2012) Role of Aspergillus niger acrA in arsenic resistance and its use as the basis for an arsenic biosensor. Appl Environ Microbiol 78 : 3855–3863. doi: 10.1128/AEM.07771-11 22467499
45. Gravelat FN, Askew DS, Sheppard DC (2012) Targeted gene deletion in Aspergillus fumigatus using the hygromycin-resistance split-marker approach. Methods in molecular biology (Clifton, NJ) 845 : 119–130.
46. Sheppard DC, Rieg G, Chiang LY, Filler SG, Edwards JE Jr., et al. (2004) Novel inhalational murine model of invasive pulmonary aspergillosis. Antimicrob Agents Chemother 48 : 1908–1911. 15105158
47. Vinh DC, Sugui JA, Hsu AP, Freeman AF, Holland SM (2010) Invasive fungal disease in autosomal-dominant hyper-IgE syndrome. J Allergy Clin Immunol 125 : 1389–1390. doi: 10.1016/j.jaci.2010.01.047 20392475
48. Pierce CG, Uppuluri P, Tristan AR, Wormley FL Jr., Mowat E, et al. (2008) A simple and reproducible 96-well plate-based method for the formation of fungal biofilms and its application to antifungal susceptibility testing. Nat Protoc 3 : 1494–1500. doi: 10.1038/nport.2008.141 18772877
49. Sheppard DC, Rieg G, Chiang LY, Filler SG, Edwards JE Jr., et al. (2004) Novel inhalational murine model of invasive pulmonary aspergillosis. Antimicrob Agents Chemother 48 : 1908–1911. 15105158
Štítky
Hygiena a epidemiológia Infekčné lekárstvo Laboratórium
Článek TRIM21 Promotes cGAS and RIG-I Sensing of Viral Genomes during Infection by Antibody-Opsonized VirusČlánek Effector OspB Activates mTORC1 in a Manner That Depends on IQGAP1 and Promotes Cell ProliferationČlánek Fundamental Roles of the Golgi-Associated Aspartyl Protease, ASP5, at the Host-Parasite InterfaceČlánek Modulation of the Surface Proteome through Multiple Ubiquitylation Pathways in African Trypanosomes
Článok vyšiel v časopisePLOS Pathogens
Najčítanejšie tento týždeň
2015 Číslo 10- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
-
Všetky články tohto čísla
- Expression of Concern: Misregulation of Underlies the Developmental Abnormalities Caused by Three Distinct Viral Silencing Suppressors in Arabidopsis
- Preparing for the Next Epidemic with Basic Virology
- Effectively Communicating the Uncertainties Surrounding Ebola Virus Transmission
- Translating Basic Research into Clinical Applications: Malaria Research at an NIH Lab
- A Gut Odyssey: The Impact of the Microbiota on Spore Formation and Germination
- Papillomavirus E6 Oncoproteins Take Common Structural Approaches to Solve Different Biological Problems
- Chronobiomics: The Biological Clock as a New Principle in Host–Microbial Interactions
- Dimensions of Horizontal Gene Transfer in Eukaryotic Microbial Pathogens
- Addressing the Complications of Ebola and Other Viral Hemorrhagic Fever Infections: Using Insights from Bacterial and Fungal Sepsis
- Time for Chocolate: Current Understanding and New Perspectives on Cacao Witches’ Broom Disease Research
- Ganglioside and Non-ganglioside Mediated Host Responses to the Mouse Polyomavirus
- Crosslinking of a Peritrophic Matrix Protein Protects Gut Epithelia from Bacterial Exotoxins
- Structure Elucidation of Coxsackievirus A16 in Complex with GPP3 Informs a Systematic Review of Highly Potent Capsid Binders to Enteroviruses
- CD39 Expression Identifies Terminally Exhausted CD8 T Cells
- Abiotic Stresses Antagonize the Rice Defence Pathway through the Tyrosine-Dephosphorylation of OsMPK6
- Dissociation of Tissue Destruction and Bacterial Expansion during Bubonic Plague
- Interferon-γ: The Jekyll and Hyde of Malaria
- CCR2 Inflammatory Dendritic Cells and Translocation of Antigen by Type III Secretion Are Required for the Exceptionally Large CD8 T Cell Response to the Protective YopE Epitope during Infection
- A New Glycan-Dependent CD4-Binding Site Neutralizing Antibody Exerts Pressure on HIV-1
- The Suramin Derivative NF449 Interacts with the 5-fold Vertex of the Enterovirus A71 Capsid to Prevent Virus Attachment to PSGL-1 and Heparan Sulfate
- Trans-generational Immune Priming Protects the Eggs Only against Gram-Positive Bacteria in the Mealworm Beetle
- Peripheral Vγ9Vδ2 T Cells Are a Novel Reservoir of Latent HIV Infection
- Respiratory Syncytial Virus Disease Is Mediated by Age-Variable IL-33
- TRIM21 Promotes cGAS and RIG-I Sensing of Viral Genomes during Infection by Antibody-Opsonized Virus
- Modeling the Effects of Vorinostat Reveals both Transient and Delayed HIV Transcriptional Activation and Minimal Killing of Latently Infected Cells
- Identification of a Novel Lipoprotein Regulator of Spore Germination
- Calcium Regulation of Hemorrhagic Fever Virus Budding: Mechanistic Implications for Host-Oriented Therapeutic Intervention
- Antigen-Specific Th17 Cells Are Primed by Distinct and Complementary Dendritic Cell Subsets in Oropharyngeal Candidiasis
- Comparative Life Cycle Transcriptomics Revises Genome Annotation and Links a Chromosome Duplication with Parasitism of Vertebrates
- The Autophagy Receptor TAX1BP1 and the Molecular Motor Myosin VI Are Required for Clearance of Salmonella Typhimurium by Autophagy
- Carcinogenic Parasite Secretes Growth Factor That Accelerates Wound Healing and Potentially Promotes Neoplasia
- Effector OspB Activates mTORC1 in a Manner That Depends on IQGAP1 and Promotes Cell Proliferation
- Dengue Virus Infection of Requires a Putative Cysteine Rich Venom Protein
- Distinct Viral and Mutational Spectrum of Endemic Burkitt Lymphoma
- Fundamental Roles of the Golgi-Associated Aspartyl Protease, ASP5, at the Host-Parasite Interface
- Phenotypic and Functional Alterations in Circulating Memory CD8 T Cells with Time after Primary Infection
- Systematic Identification of Cyclic-di-GMP Binding Proteins in Reveals a Novel Class of Cyclic-di-GMP-Binding ATPases Associated with Type II Secretion Systems
- Influenza Transmission in the Mother-Infant Dyad Leads to Severe Disease, Mammary Gland Infection, and Pathogenesis by Regulating Host Responses
- Myeloid Cell Arg1 Inhibits Control of Arthritogenic Alphavirus Infection by Suppressing Antiviral T Cells
- The White-Nose Syndrome Transcriptome: Activation of Anti-fungal Host Responses in Wing Tissue of Hibernating Little Brown Myotis
- Influenza Virus Reassortment Is Enhanced by Semi-infectious Particles but Can Be Suppressed by Defective Interfering Particles
- Identification of the Mechanisms Causing Reversion to Virulence in an Attenuated SARS-CoV for the Design of a Genetically Stable Vaccine
- Differentiation-Dependent KLF4 Expression Promotes Lytic Epstein-Barr Virus Infection in Epithelial Cells
- The Histone Acetyltransferase Hat1 Regulates Stress Resistance and Virulence via Distinct Chromatin Assembly Pathways
- C-di-GMP Regulates Motile to Sessile Transition by Modulating MshA Pili Biogenesis and Near-Surface Motility Behavior in
- Modulation of the Surface Proteome through Multiple Ubiquitylation Pathways in African Trypanosomes
- Crystal Structure of the Human Cytomegalovirus Glycoprotein B
- Depletion of . GlmU from Infected Murine Lungs Effects the Clearance of the Pathogen
- Immunologic Control of Papillomavirus Type 1
- Requires Host Rab1b for Survival in Macrophages
- Structure Analysis Uncovers a Highly Diverse but Structurally Conserved Effector Family in Phytopathogenic Fungi
- PD-L1 Expression on Retrovirus-Infected Cells Mediates Immune Escape from CD8 T Cell Killing
- Phospho-dependent Regulation of SAMHD1 Oligomerisation Couples Catalysis and Restriction
- IL-4 Induced Innate CD8 T Cells Control Persistent Viral Infection
- Crystal Structures of a Piscine Betanodavirus: Mechanisms of Capsid Assembly and Viral Infection
- BCG Skin Infection Triggers IL-1R-MyD88-Dependent Migration of EpCAM CD11b Skin Dendritic cells to Draining Lymph Node During CD4+ T-Cell Priming
- Antigenic Characterization of the HCMV gH/gL/gO and Pentamer Cell Entry Complexes Reveals Binding Sites for Potently Neutralizing Human Antibodies
- Rescue of a Plant Negative-Strand RNA Virus from Cloned cDNA: Insights into Enveloped Plant Virus Movement and Morphogenesis
- Geminivirus Activates to Accelerate Cytoplasmic DCP2-Mediated mRNA Turnover and Weakens RNA Silencing in
- Disruption of Sphingolipid Biosynthesis Blocks Phagocytosis of
- The Fungal Exopolysaccharide Galactosaminogalactan Mediates Virulence by Enhancing Resistance to Neutrophil Extracellular Traps
- The Timing of Stimulation and IL-2 Signaling Regulate Secondary CD8 T Cell Responses
- Structural and Functional Analysis of Murine Polyomavirus Capsid Proteins Establish the Determinants of Ligand Recognition and Pathogenicity
- The Dual Role of an ESCRT-0 Component HGS in HBV Transcription and Naked Capsid Secretion
- PLOS Pathogens
- Archív čísel
- Aktuálne číslo
- Informácie o časopise
Najčítanejšie v tomto čísle- Chronobiomics: The Biological Clock as a New Principle in Host–Microbial Interactions
- Interferon-γ: The Jekyll and Hyde of Malaria
- Crosslinking of a Peritrophic Matrix Protein Protects Gut Epithelia from Bacterial Exotoxins
- Antigen-Specific Th17 Cells Are Primed by Distinct and Complementary Dendritic Cell Subsets in Oropharyngeal Candidiasis
Prihlásenie#ADS_BOTTOM_SCRIPTS#Zabudnuté hesloZadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.
- Časopisy