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

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

doi:10.1155/2020/3412763

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

Journal Article · Mon Dec 07 00:00:00 EST 2020 · Mediators of Inflammation

DOI:https://doi.org/10.1155/2020/3412763· OSTI ID:1755941

Bürgel, Pedro Henrique ^[1]; Marina, Clara Luna ^[2]; Saavedra, Pedro V. ^[3];

^[2]; de Oliveira, Stephan Machado ^[2]; Veloso Janior, Paulo Holanda ^[2]; Castro, Raffael de ^[2];

^[4]; Coelho, Carolina ^[5]; Cordero, Radames B. ^[6]; Casadevall, Arturo ^[6]; Nosanchuk, Joshua D. ^[7];

^[8]; May, Robin C. ^[9];

^[2];

^[2]

Univ. of Brasilia (Brazil); Univ. of Birmingham (United Kingdom)
Univ. of Brasilia (Brazil)
Cornell Univ., Ithaca, NY (United States)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States); Bruker Daltonics Inc., Billerica, MA (United States)
Johns Hopkins Univ., Baltimore, MD (United States); Univ. of Aberdeen (United Kingdom); Univ. of Exeter (United Kingdom)
Johns Hopkins Univ., Baltimore, MD (United States)
Albert Einstein College of Medicine, Bronx, NY (United States)
Johns Hopkins Univ., Baltimore, MD (United States); Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Univ. of Birmingham (United Kingdom)

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.

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Research Organization:: Pacific Northwest National Lab. (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC05-76RL01830

OSTI ID:: 1755941

Report Number(s):: PNNL-SA-140752

Journal Information:: Mediators of Inflammation, Vol. 2020; ISSN 0962-9351

Publisher:: HindawiCopyright Statement

Country of Publication:: United States

Language:: English

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