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Title: Cryptococcus neoformans Secretes Small Molecules That Inhibit IL-1β Inflammasome-Dependent Secretion

Abstract

Cryptococcus neoformans is an encapsulated yeast that causes disease mainly in immunosuppressed hosts. It is considered a facultative intracellular pathogen because of its capacity to survive and replicate inside phagocytes, especially macrophages. This ability is heavily dependent on various virulence factors, particularly the glucuronoxylomannan (GXM) component of the polysaccharide capsule. Inflammasome activation in phagocytes is usually protective against fungal infections, including cryptococcosis. Nevertheless, recognition of C. neoformans by inflammasome receptors requires specific changes in morphology or the opsonization of the yeast, impairing proper inflammasome function. In this context, we analyzed the impact of molecules secreted by C. neoformans B3501 strain and its acapsular mutant Δcap67 in inflammasome activation in an in vitro model. Our results showed that conditioned media derived from B3501 was capable of inhibiting inflammasome-dependent events (i.e., IL-1β secretion and LDH release via pyroptosis) more strongly than conditioned media from Δcap67, regardless of GXM presence. We also demonstrated that macrophages treated with conditioned media were less responsive against infection with the virulent strain H99, exhibiting lower rates of phagocytosis, increased fungal burdens, and enhanced vomocytosis. Moreover, we showed that the aromatic metabolite DL-Indole-3-lactic acid (ILA) and DL-p-Hydroxyphenyllactic acid (HPLA) were present in B3501’s conditioned media and that ILAmore » alone or with HPLA is involved in the regulation of inflammasome activation by C. neoformans. These results were confirmed by in vivo experiments, where exposure to conditioned media led to higher fungal burdens in Acanthamoeba castellanii culture as well as in higher fungal loads in the lungs of infected mice. Overall, the results presented show that conditioned media from a wild-type strain can inhibit a vital recognition pathway and subsequent fungicidal functions of macrophages, contributing to fungal survival in vitro and in vivo and suggesting that secretion of aromatic metabolites, such as ILA, during cryptococcal infections fundamentally impacts pathogenesis.« less

Authors:
 [1];  [2];  [3]; ORCiD logo [2];  [2];  [2];  [2]; ORCiD logo [4];  [5];  [6];  [6];  [7]; ORCiD logo [8];  [9]; ORCiD logo [2]; ORCiD logo [2]
+ Show Author Affiliations
  1. Univ. of Brasilia (Brazil); Univ. of Birmingham (United Kingdom)
  2. Univ. of Brasilia (Brazil)
  3. Cornell Univ., Ithaca, NY (United States)
  4. Pacific Northwest National Lab. (PNNL), Richland, WA (United States); Bruker Daltonics Inc., Billerica, MA (United States)
  5. Johns Hopkins Univ., Baltimore, MD (United States); Univ. of Aberdeen (United Kingdom); Univ. of Exeter (United Kingdom)
  6. Johns Hopkins Univ., Baltimore, MD (United States)
  7. Albert Einstein College of Medicine, Bronx, NY (United States)
  8. Johns Hopkins Univ., Baltimore, MD (United States); Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  9. Univ. of Birmingham (United Kingdom)
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1755941
Report Number(s):
PNNL-SA-140752
Journal ID: ISSN 0962-9351
Grant/Contract Number:  
AC05-76RL01830
Resource Type:
Accepted Manuscript
Journal Name:
Mediators of Inflammation
Additional Journal Information:
Journal Volume: 2020; Journal ID: ISSN 0962-9351
Publisher:
Hindawi
Country of Publication:
United States
Language:
English
Subject:
60 APPLIED LIFE SCIENCES

Citation Formats

Bürgel, Pedro Henrique, Marina, Clara Luna, Saavedra, Pedro V., Albuquerque, Patrícia, de Oliveira, Stephan Machado, Veloso Janior, Paulo Holanda, Castro, Raffael de, Heyman, Heino M., Coelho, Carolina, Cordero, Radames B., Casadevall, Arturo, Nosanchuk, Joshua D., Nakayasu, Ernesto S., May, Robin C., Tavares, Aldo Henrique, and Bocca, Anamelia Lorenzetti. Cryptococcus neoformans Secretes Small Molecules That Inhibit IL-1β Inflammasome-Dependent Secretion. United States: N. p., 2020. Web. doi:10.1155/2020/3412763.
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Bürgel, Pedro Henrique, Marina, Clara Luna, Saavedra, Pedro V., Albuquerque, Patrícia, de Oliveira, Stephan Machado, Veloso Janior, Paulo Holanda, Castro, Raffael de, Heyman, Heino M., Coelho, Carolina, Cordero, Radames B., Casadevall, Arturo, Nosanchuk, Joshua D., Nakayasu, Ernesto S., May, Robin C., Tavares, Aldo Henrique, & Bocca, Anamelia Lorenzetti. Cryptococcus neoformans Secretes Small Molecules That Inhibit IL-1β Inflammasome-Dependent Secretion. United States. https://doi.org/10.1155/2020/3412763
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Bürgel, Pedro Henrique, Marina, Clara Luna, Saavedra, Pedro V., Albuquerque, Patrícia, de Oliveira, Stephan Machado, Veloso Janior, Paulo Holanda, Castro, Raffael de, Heyman, Heino M., Coelho, Carolina, Cordero, Radames B., Casadevall, Arturo, Nosanchuk, Joshua D., Nakayasu, Ernesto S., May, Robin C., Tavares, Aldo Henrique, and Bocca, Anamelia Lorenzetti. Mon . "Cryptococcus neoformans Secretes Small Molecules That Inhibit IL-1β Inflammasome-Dependent Secretion". United States. https://doi.org/10.1155/2020/3412763. https://www.osti.gov/servlets/purl/1755941.
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@article{osti_1755941,
title = {Cryptococcus neoformans Secretes Small Molecules That Inhibit IL-1β Inflammasome-Dependent Secretion},
author = {Bürgel, Pedro Henrique and Marina, Clara Luna and Saavedra, Pedro V. and Albuquerque, Patrícia and de Oliveira, Stephan Machado and Veloso Janior, Paulo Holanda and Castro, Raffael de and Heyman, Heino M. and Coelho, Carolina and Cordero, Radames B. and Casadevall, Arturo and Nosanchuk, Joshua D. and Nakayasu, Ernesto S. and May, Robin C. and Tavares, Aldo Henrique and Bocca, Anamelia Lorenzetti},
abstractNote = {Cryptococcus neoformans is an encapsulated yeast that causes disease mainly in immunosuppressed hosts. It is considered a facultative intracellular pathogen because of its capacity to survive and replicate inside phagocytes, especially macrophages. This ability is heavily dependent on various virulence factors, particularly the glucuronoxylomannan (GXM) component of the polysaccharide capsule. Inflammasome activation in phagocytes is usually protective against fungal infections, including cryptococcosis. Nevertheless, recognition of C. neoformans by inflammasome receptors requires specific changes in morphology or the opsonization of the yeast, impairing proper inflammasome function. In this context, we analyzed the impact of molecules secreted by C. neoformans B3501 strain and its acapsular mutant Δcap67 in inflammasome activation in an in vitro model. Our results showed that conditioned media derived from B3501 was capable of inhibiting inflammasome-dependent events (i.e., IL-1β secretion and LDH release via pyroptosis) more strongly than conditioned media from Δcap67, regardless of GXM presence. We also demonstrated that macrophages treated with conditioned media were less responsive against infection with the virulent strain H99, exhibiting lower rates of phagocytosis, increased fungal burdens, and enhanced vomocytosis. Moreover, we showed that the aromatic metabolite DL-Indole-3-lactic acid (ILA) and DL-p-Hydroxyphenyllactic acid (HPLA) were present in B3501’s conditioned media and that ILA alone or with HPLA is involved in the regulation of inflammasome activation by C. neoformans. These results were confirmed by in vivo experiments, where exposure to conditioned media led to higher fungal burdens in Acanthamoeba castellanii culture as well as in higher fungal loads in the lungs of infected mice. Overall, the results presented show that conditioned media from a wild-type strain can inhibit a vital recognition pathway and subsequent fungicidal functions of macrophages, contributing to fungal survival in vitro and in vivo and suggesting that secretion of aromatic metabolites, such as ILA, during cryptococcal infections fundamentally impacts pathogenesis.},
doi = {10.1155/2020/3412763},
journal = {Mediators of Inflammation},
number = ,
volume = 2020,
place = {United States},
year = {Mon Dec 07 00:00:00 EST 2020},
month = {Mon Dec 07 00:00:00 EST 2020}
}
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