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Heat Shock Protein 60, Insights to Its Importance in Histoplasma Capsulatum: from Biofilm Formation to Host-Interaction

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Heat Shock Protein 60, Insights to Its Importance in Histoplasma Capsulatum: from Biofilm Formation to Host-Interaction ORIGINAL RESEARCH published: 22 January 2021 doi: 10.3389/fcimb.2020.591950 Heat Shock Protein 60, Insights to Its Importance in Histoplasma capsulatum: From Biofilm Formation to Host-Interaction ´ 1 1 1 Edited by: Nathalia Ferreira Fregonezi , Lariane Teodoro Oliveira , Junya de Lacorte Singulani , 1 1 2 Angel Gonzalez, Caroline Maria Marcos , Claudia Tavares dos Santos , Maria Lucia Taylor , ´ 1 1 † University of Antioquia, Colombia Maria Jose Soares Mendes-Giannini , Haroldo Cesar de Oliveira * 1* Reviewed by: and Ana Marisa Fusco-Almeida Ernesto Satoshi Nakayasu, 1 Department of Clinical Analysis, School of Pharmaceutical Sciences, São Paulo State University-UNESP, Araraquara, Brazil, Pacific Northwest National Laboratory 2 Unidad de Micolog´ıa, Departamento de Microbiolog´ıa y Parasitolog´ıa, Facultad de Medicina, UNAM—Universidad Nacional (DOE), United States Auto´ noma de Me´ xico, Mexico City, Mexico Jeniel E. Nett, University of Wisconsin-Madison, United States Heat shock proteins (Hsps) are among the most widely distributed and evolutionary *Correspondence: conserved proteins, acting as essential regulators of diverse constitutive metabolic Ana Marisa Fusco-Almeida [email protected] processes. The Hsp60 of the dimorphic fungal Histoplasma capsulatum is the major Haroldo Cesar de Oliveira surface adhesin to mammalian macrophages and studies of antibody-mediated [email protected] protection against H. capsulatum have provided insight into the complexity involving † Present address: Hsp60. However, nothing is known about the role of Hsp60 regarding biofilms, a Haroldo Cesar de Oliveira, Instituto Carlos Chagas, mechanism of virulence exhibited by H. capsulatum. Considering this, the present Fundac¸ão Oswaldo Cruz (Fiocruz), study aimed to investigate the influence of the Hsp60 on biofilm features of H. Curitiba, Brazil capsulatum. Also, the non-conventional model Galleria mellonella was used to verify the Specialty section: effect of this protein during in vivo interaction. The use of invertebrate models such as G. This article was submitted to mellonella is highly proposed for the evaluation of pathogenesis, immune response, Fungal Pathogenesis, virulence mechanisms, and antimicrobial compounds. For that purpose, we used a a section of the journal Frontiers in Cellular monoclonal antibody (7B6) against Hsp60 and characterized the biofilm of two H. and Infection Microbiology capsulatum strains by metabolic activity, biomass content, and images from scanning Received: 05 August 2020 electron microscopy (SEM) and confocal laser scanning microscopy (CLSM). We also Accepted: 04 December 2020 Published: 22 January 2021 evaluated the survival rate of G. mellonella infected with both strains under blockage of Citation: Hsp60. The results showed that mAb 7B6 was effective to reduce the metabolic activity Fregonezi NF, Oliveira LT, and biomass of both H. capsulatum strains. Furthermore, the biofilms of cells treated with Singulani JL, Marcos CM, the antibody were thinner as well as presented a lower amount of cells and extracellular dos Santos CT, Taylor ML, Mendes-Giannini MJS, de Oliveira HC polymeric matrix compared to its non-treated controls. The blockage of Hsp60 before and Fusco-Almeida AM (2021) Heat fungal infection of G. mellonella larvae also resulted in a significant increase of the larvae Shock Protein 60, Insights to Its fi Importance in Histoplasma survival compared to controls. Our results highlight for the rst time the importance of the capsulatum: From Biofilm Hsp60 protein to the establishment of the H. capsulatum biofilms and the G. mellonella Formation to Host-Interaction. larvae infection. Interestingly, the results with Hsp60 mAb 7B6 in this invertebrate model Front. Cell. Infect. Microbiol. 10:591950. doi: 10.3389/fcimb.2020.591950 suggest a pattern of fungus-host interaction different from those previously found in a Frontiers in Cellular and Infection Microbiology | www.frontiersin.org1 January 2021 | Volume 10 | Article 591950 Fregonezi et al. Alternative Roles for Histoplasma capsulatum Hsp60 murine model, which can be due to the different features between insect and mammalian immune cells such as the absence of Fc receptors in hemocytes. However further studies are needed to support this hypothesis Keywords: histoplasmosis, biofilm, Hsp60, adhesins, Galleria mellonella INTRODUCTION interaction with CD11b/CD18 (CR3) Mj receptor (Long et al., 2003), therefore playing an essential role in the infection process. Histoplasma capsulatum is a dimorphic pathogenic fungus that Heat shock proteins (HSPs) are ubiquitously expressed, causes histoplasmosis, one of the most common pulmonary highly conserved proteins, known to act as molecular mycosis in the United States (US) (Armstrong et al., 2018; chaperones with important functions, such as the transport of Maiga et al., 2018; Salzer et al., 2018). Despite endemic in proteins and promotion of folding and assembly of polypeptides certain areas of the US (e.g. Ohio and Mississippi river in fungi (Kubota et al., 1995; Leach et al., 2012; Cleare et al., valleys), histoplasmosis has a worldwide distribution and is 2017). In addition to its intracellular biologic activities, Hsp60 is also one of the top AIDS-defining conditions and AIDS-related a prominent target of the humoral and cellular immune response causes of death in Latin America (Adenis et al., 2018; Papalini to H. capsulatum (Gomez A. M. et al., 1991; Gomez F. J. et al., et al., 2019). 1991). H. capsulatum Hsp60 was first identified as a 62-kDa The histoplasmosis infection occurs via inhalation of conidial protein isolated from the cell wall and membrane extract and spores that transform into yeasts within the mammalian host showed antigenic (Gomez A. M. et al., 1991) and immunogenic (Mittal et al., 2019). As a facultative intracellular fungus, H. (Gomez et al., 1995) properties. capsulatum yeasts are readily phagocytosed by resident Hsp60 is reported to be predominantly in the cytosolic macrophages, where they survive and replicate. During the fraction of cells (Kubota et al., 1995; Kalderon et al., 2015). early phases of infection, alveolar macrophages (Mj) recognize However, to act as a ligand for the host cell, in H. capsulatum, unopsonized H. capsulatum yeasts and microconidia via the Hsp60 is expressed in clusters on the cell wall (Long et al., 2003), CD18 family of adhesion-promoting glycoproteins, LFA-1 promoting recognition, adhesion, and phagocytosis of the fungi. (CD11a/CD18), complement receptor 3 (CR3; CD11b/CD18), The Hsp60/CR3 interaction results in phagocytosis without and CR4 (CD11c/CD18) (Bullock and Wright, 1987; Newman complete activation of the phagocyte, leading to a non- et al., 1990). inflammatory immunological response (Wolf et al., 1987; The adhesion capacity to host tissue is important to several Ehlers, 2000; Lin et al., 2010; Mihu and Nosanchuk, 2012). microorganisms, and a relevant mechanism of virulence is It is of great knowledge that H. capsulatum can infect described to dimorphic fungi (McMahon et al., 1995; mammals, and murine models are traditionally used for the Brandhorst and Klein, 2000; Marcos et al., 2016; Portuondo study of this fungal virulence. However, it is also known that H. et al., 2016). However, the interaction between host-pathogen is capsulatum is capable of infect G. mellonella larvae (Thomaz not the only factor involved in the infectious process, but also the et al., 2013), making this non-conventional animal model an cell-cell interaction/adhesion. The adhesion is also crucial for the important tool to understand Histoplasma-host interaction. formation of resistance structures, called biofilms (Verstrepen Invertebrate animals have emerged as alternative models to and Klis, 2006; Borges et al., 2018). Like many other pathogenic mammals because breeding is simple and inexpensive (Fuchs fungi, H. capsulatum yeasts can form biofilms in vitro (Pitangui and Mylonakis, 2006; Binder et al., 2016). In this aspect, et al., 2012; Gonçalves et al., 2020). Biofilms are defined as a the study of the pathogenesis of different microorganism dynamic community of microorganisms strongly linked with including dimorphic fungi such as Paracoccidioides spp., each other and attached to a biotic or abiotic surface, surrounded Sporothrix spp., Talaromyces marneffei (Penicillium marneffei), by a self-produced extracellular polymeric matrix (EPM) that and H. capsulatum has been evaluated in G. mellonella larvae provides protection against hostile environments and is also (Thomaz et al., 2013; Huang et al., 2015; Scorzoni et al., 2015; related to reduced antifungal activity (Costerton et al., 1995; Clavijo-Giraldo et al., 2016). The model is especially Baillie and Douglas, 2000; Brilhante et al., 2015; Zarnowski et al., advantageous for dimorphic fungi due to the possibility that 2018). In vivo H. capsulatum biofilms has never been proved. the larvae are kept at 37°C during survival assays and they However, the H. capsulatum yeasts can adhere to various present six types of immune cells called hemocytes, which have cryopreserved bat organs, such as lung, spleen, liver, and structural and functional similarities to cells of the mammalian intestine (Suarez-Alvarez et al., 2010), human epithelial cell immune system (Singulani et al., 2018). lines (Pitangui et al., 2012) and also, to endothelium and Our current work sought to understand the importance of prosthetic valves (Ledtke et al., 2012; Lorchirachonkul et al., Hsp60 in H. capsulatum biofilms formation and the fungi 2013; Riddell
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