Turning on virulence: Mechanisms that underpin the morphologic transition and pathogenicity of Blastomyces

References

• Gauthier GM. Fungal Dimorphism and Virulence: Molecular Mechanisms for Temperature Adaptation, Immune Evasion, and In Vivo Survival. Mediators Inflamm. 2017;2017:8491383.
   PubMedGoogle Scholar
• Dukik K, Muñoz JF, Jiang Y, et al. Novel taxa of thermally dimorphic systemic pathogens in the Ajellomycetaceae (Onygenales). Mycoses. 2017;60:296–309.
   PubMed Web of Science ®Google Scholar
• Wolf PL RB, Shimoda A. Practical Clinical Microbiology and Mycology: Techniques and Interpretations. In: Wolf PL RB, Shimoda A, ed. Practical Clinical Microbiology and Mycology: Techniques and Interpretations. New York: John Wiley; 1975. p. 486–8.
   Google Scholar
• McBride JA, Gauthier GM, Klein BS. Clinical Manifestations and Treatment of Blastomycosis. Clin Chest Med. 2017;38:435–49.
   PubMed Web of Science ®Google Scholar
• Klein BS, Vergeront JM, Weeks RJ, et al. Isolation of Blastomyces dermatitidis in soil associated with a large outbreak of blastomycosis in Wisconsin. N Engl J Med. 1986;314:529–34.
   PubMed Web of Science ®Google Scholar
• Klein BS, Vergeront JM, DiSalvo AF, et al. Two outbreaks of blastomycosis along rivers in Wisconsin. Isolation of Blastomyces dermatitidis from riverbank soil and evidence of its transmission along waterways. Am Rev Respir Dis. 1987;136:1333–8.
   PubMed Web of Science ®Google Scholar
• McTaggart LR, Brown EM, Richardson SE. Phylogeographic Analysis of Blastomyces dermatitidis and Blastomyces gilchristii Reveals an Association with North American Freshwater Drainage Basins. PLoS One. 2016;11:e0159396.
   PubMed Web of Science ®Google Scholar
• Gauthier GM. Dimorphism in fungal pathogens of mammals, plants, and insects. PLoS Pathog. 2015;11:e1004608.
   PubMed Web of Science ®Google Scholar
• Klotz SA, Drutz DJ, Huppert M, et al. The critical role of CO2 in the morphogenesis of Coccidioides immitis in cell-free subcutaneous chambers. J Infect Dis. 1984;150:127–34.
   PubMed Web of Science ®Google Scholar
• Pine L. Studies on the growth of Histoplasma capsulatum. I. Growth of the yeast phase in liquid media. J Bacteriol. 1954;68:671–9.
   PubMed Web of Science ®Google Scholar
• Maresca B, Lambowitz AM, Kumar VB, et al. Role of cysteine in regulating morphogenesis and mitochondrial activity in the dimorphic fungus Histoplasma capsulatum. Proc Natl Acad Sci U S A. 1981;78:4596–600.
   PubMed Web of Science ®Google Scholar
• Medoff G, Painter A, Kobayashi GS. Mycelial- to yeast-phase transitions of the dimorphic fungi Blastomyces dermatitidis and Paracoccidioides brasiliensis. J Bacteriol. 1987;169:4055–60.
   PubMed Web of Science ®Google Scholar
• Drutz DJ, Huppert M, Sun SH, et al. Human sex hormones stimulate the growth and maturation of Coccidioides immitis. Infect Immun. 1981;32:897–907.
   PubMed Web of Science ®Google Scholar
• Shankar J, Wu TD, Clemons KV, et al. Influence of 17beta-estradiol on gene expression of Paracoccidioides during mycelia-to-yeast transition. PLoS One. 2011;6:e28402.
   PubMed Web of Science ®Google Scholar
• Restrepo A, Salazar ME, Cano LE, et al. Estrogens inhibit mycelium-to-yeast transformation in the fungus Paracoccidioides brasiliensis: implications for resistance of females to paracoccidioidomycosis. Infect Immun. 1984;46:346–53.
   PubMed Web of Science ®Google Scholar
• Stover EP, Schar G, Clemons KV, et al. Estradiol-binding proteins from mycelial and yeast-form cultures of Paracoccidioides brasiliensis. Infect Immun. 1986;51:199–203.
   PubMed Web of Science ®Google Scholar
• Powell BL, Drutz DJ, Huppert M, et al. Relationship of progesterone- and estradiol-binding proteins in Coccidioides immitis to coccidioidal dissemination in pregnancy. Infect Immun. 1983;40:478–85.
   PubMed Web of Science ®Google Scholar
• Sterkel AK, Mettelman R, Wuthrich M, et al. The unappreciated intracellular lifestyle of Blastomyces dermatitidis. J Immunol. 2015;194:1796–805.
   PubMed Web of Science ®Google Scholar
• Inglis DO, Voorhies M, Hocking Murray DR, et al. Comparative transcriptomics of infectious spores from the fungal pathogen Histoplasma capsulatum reveals a core set of transcripts that specify infectious and pathogenic states. Eukaryot Cell. 2013;12:828–52.
   PubMedGoogle Scholar
• Beaman L, Benjamini E, Pappagianis D. Role of lymphocytes in macrophage-induced killing of Coccidioides immitis in vitro. Infect Immun. 1981;34:347–53.
   PubMed Web of Science ®Google Scholar
• Jimenez Mdel P, Restrepo A, Radzioch D, et al. Importance of complement 3 and mannose receptors in phagocytosis of Paracoccidioides brasiliensis conidia by Nramp1 congenic macrophages lines. FEMS Immunol Med Microbiol. 2006;47:56–66.
   PubMedGoogle Scholar
• Guzman-Beltran S, Perez-Torres A, Coronel-Cruz C, et al. Phagocytic receptors on macrophages distinguish between different Sporothrix schenckii morphotypes. Microbes Infect. 2012;14:1093–101.
   PubMed Web of Science ®Google Scholar
• Boyce KJ, Andrianopoulos A. Morphogenetic circuitry regulating growth and development in the dimorphic pathogen Penicillium marneffei. Eukaryot Cell. 2013;12:154–60.
   PubMedGoogle Scholar
• Charlier C, Nielsen K, Daou S, et al. Evidence of a role for monocytes in dissemination and brain invasion by Cryptococcus neoformans. Infect Immun. 2009;77:120–7.
   PubMed Web of Science ®Google Scholar
• Chapman SW, Dismukes WE, Proia LA, et al. Clinical practice guidelines for the management of blastomycosis: 2008 update by the Infectious Diseases Society of America. Infectious Diseases Society of America. Clin Infect Dis. 2008;46:1801–12.
   PubMed Web of Science ®Google Scholar
• Brandhorst TT, Wuthrich M, Warner T, et al. Targeted gene disruption reveals an adhesin indispensable for pathogenicity of Blastomyces dermatitidis. J Exp Med. 1999;189:1207–16.
   PubMed Web of Science ®Google Scholar
• Brandhorst TT, Roy R, Wuthrich M, et al. Structure and function of a fungal adhesin that binds heparin and mimics thrombospondin-1 by blocking T cell activation and effector function. PLoS Pathog. 2013;9:e1003464.
   PubMed Web of Science ®Google Scholar
• Beaussart A, Brandhorst T, Dufrene YF, et al. Blastomyces Virulence Adhesin-1 Protein Binding to Glycosaminoglycans Is Enhanced by Protein Disulfide Isomerase. MBio. 2015;6:e01403–15.
   PubMed Web of Science ®Google Scholar
• Brandhorst T, Wuthrich M, Finkel-Jimenez B, et al. A C-terminal EGF-like domain governs BAD1 localization to the yeast surface and fungal adherence to phagocytes, but is dispensable in immune modulation and pathogenicity of Blastomyces dermatitidis. Mol Microbiol. 2003;48:53–65.
   PubMed Web of Science ®Google Scholar
• Finkel-Jimenez B, Wuthrich M, Klein BS. BAD1, an essential virulence factor of Blastomyces dermatitidis, suppresses host TNF-alpha production through TGF-beta-dependent and -independent mechanisms. J Immunol. 2002;168:5746–55.
   PubMed Web of Science ®Google Scholar
• Finkel-Jimenez B, Wuthrich M, Brandhorst T, et al. The WI-1 adhesin blocks phagocyte TNF-alpha production, imparting pathogenicity on Blastomyces dermatitidis. J Immunol. 2001;166:2665–73.
   PubMed Web of Science ®Google Scholar
• Munoz JF, Gauthier GM, Desjardins CA, et al. The Dynamic Genome and Transcriptome of the Human Fungal Pathogen Blastomyces and Close Relative Emmonsia. PLoS Genet. 2015;11:e1005493.
   PubMed Web of Science ®Google Scholar
• Brandhorst TT, Wuthrich M, Finkel-Jimenez B, et al. Exploiting type 3 complement receptor for TNF-alpha suppression, immune evasion, and progressive pulmonary fungal infection. J Immunol. 2004;173:7444–53.
   PubMed Web of Science ®Google Scholar
• Food and Drug Administration. Tumor necrosis factor-alpha blockers (TNF blockers), Cimzia (certolizumab pegol), Enbrel (etanercept), Humira (adalimumab), and Remicade (infliximab). FDA Alert issued September 4, 2008.
   Google Scholar
• Sterkel AK, Lorenzini JL, Fites JS, et al. Fungal Mimicry of a Mammalian Aminopeptidase Disables Innate Immunity and Promotes Pathogenicity. Cell Host Microbe. 2016;19:361–74.
   PubMed Web of Science ®Google Scholar
• Kanetsuna F, Carbonell LM. Cell wall composition of the yeastlike and mycelial forms of Blastomyces dermatitidis. J Bacteriol. 1971;106:946–48.
   PubMed Web of Science ®Google Scholar
• Koneti A, Linke MJ, Brummer E, et al. Evasion of innate immune responses: evidence for mannose binding lectin inhibition of tumor necrosis factor alpha production by macrophages in response to Blastomyces dermatitidis. Infect Immun. 2008;76:994–1002.
   PubMed Web of Science ®Google Scholar
• Marty AJ, Wuthrich M, Carmen JC, et al. Isolation of Blastomyces dermatitidis yeast from lung tissue during murine infection for in vivo transcriptional profiling. Fungal Genet Biol. 2013;56:1–8.
   PubMed Web of Science ®Google Scholar
• Kujoth GC, Sullivan TD, Merkhofer R, et al. CRISPR/Cas9-Mediated Gene Disruption Reveals the Importance of Zinc Metabolism for Fitness of the Dimorphic Fungal Pathogen, Blastomyces dermatitidis. MBio. 2018;9:e00412–18.
   Google Scholar
• Hennicke F, Grumbt M, Lermann U, et al. Factors supporting cysteine tolerance and sulfite production in Candida albicans. Eukaryot Cell. 2013;12:604–13.
   PubMedGoogle Scholar
• Grumbt M, Monod M, Yamada T, et al. Keratin degradation by dermatophytes relies on cysteine dioxygenase and a sulfite efflux pump. J Invest Dermatol. 2013;133:1550–5.
   PubMed Web of Science ®Google Scholar
• Citiulo F, Jacobsen ID, Miramon P, et al. Candida albicans scavenges host zinc via Pra1 during endothelial invasion. PLoS Pathog. 2012;8:e1002777.
   PubMed Web of Science ®Google Scholar
• Mirbod-Donovan F, Schaller R, Hung CY, et al. Urease produced by Coccidioides posadasii contributes to the virulence of this respiratory pathogen. Infect Immun. 2006;74:504–15.
   PubMed Web of Science ®Google Scholar
• Singh A, Panting RJ, Varma A, et al. Factors required for activation of urease as a virulence determinant in Cryptococcus neoformans. MBio. 2013;4:e00220–13.
   PubMed Web of Science ®Google Scholar
• Nemecek JC, Wuthrich M, Klein BS. Global control of dimorphism and virulence in fungi. Science. 2006;312:583–8.
   PubMed Web of Science ®Google Scholar
• Lawry SM, Tebbets B, Kean I, et al. Fludioxonil Induces Drk1, a Fungal Group III Hybrid Histidine Kinase, To Dephosphorylate Its Downstream Target, Ypd1. Antimicrob Agents Chemother. 2017;61:e01414–16.
   PubMed Web of Science ®Google Scholar
• Boyce KJ, Schreider L, Kirszenblat L, et al. The two-component histidine kinases DrkA and SlnA are required for in vivo growth in the human pathogen Penicillium marneffei. Mol Microbiol. 2011;82:1164–84.
   PubMed Web of Science ®Google Scholar
• Hou B, Zhang Z, Zheng F, et al. Molecular cloning, characterization and differential expression of DRK1 in Sporothrix schenckii. Int J Mol Med. 2013;31:99–104.
   PubMed Web of Science ®Google Scholar
• Chaves AF, Navarro MV, Castilho DG, et al. A conserved dimorphism-regulating histidine kinase controls the dimorphic switching in Paracoccidioides brasiliensis. FEMS Yeast Res. 2016;16:
   PubMed Web of Science ®Google Scholar
• Nguyen VQ, Sil A. Temperature-induced switch to the pathogenic yeast form of Histoplasma capsulatum requires Ryp1, a conserved transcriptional regulator. Proc Natl Acad Sci U S A. 2008;105:4880–5.
   PubMed Web of Science ®Google Scholar
• Webster RH, Sil A. Conserved factors Ryp2 and Ryp3 control cell morphology and infectious spore formation in the fungal pathogen Histoplasma capsulatum. Proc Natl Acad Sci U S A. 2008;105:14573–8.
   PubMed Web of Science ®Google Scholar
• Beyhan S, Gutierrez M, Voorhies M, et al. A temperature-responsive network links cell shape and virulence traits in a primary fungal pathogen. PLoS Biol. 2013;11:e1001614.
   PubMed Web of Science ®Google Scholar
• Tao L, Du H, Guan G, et al. Discovery of a "white-gray-opaque" tristable phenotypic switching system in Candida albicans: roles of non-genetic diversity in host adaptation. PLoS Biol. 2014;12:e1001830.
   PubMed Web of Science ®Google Scholar
• Yue H, Hu J, Guan G, et al. Discovery of the gray phenotype and white-gray-opaque tristable phenotypic transitions in Candida dubliniensis. Virulence. 2016;7:230–42.
   PubMed Web of Science ®Google Scholar
• Bayram O, Krappmann S, Ni M, et al. VelB/VeA/LaeA complex coordinates light signal with fungal development and secondary metabolism. Science. 2008;320:1504–6.
   PubMed Web of Science ®Google Scholar
• Isaac DT, Berkes CA, English BC, et al. Macrophage cell death and transcriptional response are actively triggered by the fungal virulence factor Cbp1 during H. capsulatum infection Mol Microbiol. 2015;98:910–29.
   PubMed Web of Science ®Google Scholar
• Bohse ML, Woods JP. RNA interference-mediated silencing of the YPS3 gene of Histoplasma capsulatum reveals virulence defects. Infect Immun. 2007;75:2811–7.
   PubMed Web of Science ®Google Scholar
• Gauthier GM, Sullivan TD, Gallardo SS, et al. SREB, a GATA transcription factor that directs disparate fates in Blastomyces dermatitidis including morphogenesis and siderophore biosynthesis. PLoS Pathog. 2010;6:e1000846.
   PubMed Web of Science ®Google Scholar
• Marty AJ, Broman AT, Zarnowski R, et al. Fungal Morphology, Iron Homeostasis, and Lipid Metabolism Regulated by a GATA Transcription Factor in Blastomyces dermatitidis. PLoS Pathog. 2015;11:e1004959.
   PubMed Web of Science ®Google Scholar
• Hwang LH, Seth E, Gilmore SA, et al. SRE1 regulates iron-dependent and -independent pathways in the fungal pathogen Histoplasma capsulatum. Eukaryot Cell. 2012;11:16–25.
   PubMedGoogle Scholar
• Hilty J, Smulian AG, Newman SL. The Histoplasma capsulatum vacuolar ATPase is required for iron homeostasis, intracellular replication in macrophages and virulence in a murine model of histoplasmosis. Mol Microbiol. 2008;70:127–39.
   PubMed Web of Science ®Google Scholar
• Bugeja HE, Hynes MJ, Andrianopoulos A. HgrA is necessary and sufficient to drive hyphal growth in the dimorphic pathogen Penicillium marneffei. Mol Microbiol. 2013;88:998–1014.
   PubMed Web of Science ®Google Scholar
• Todd RB, Greenhalgh JR, Hynes MJ, et al. TupA, the Penicillin marneffei Tup1p homologue, represses both yeast and spore development. Mol Microbiol. 2003;48:85–94.
   PubMed Web of Science ®Google Scholar
• Gilmore SA, Naseem S, Konopka JB, et al. N-acetylglucosamine (GlcNAc) triggers a rapid, temperature-responsive morphogenetic program in thermally dimorphic fungi. PLoS Genet. 2013;9:e1003799.
   PubMed Web of Science ®Google Scholar
• Li W, Sullivan TD, Walton E, et al. Identification of the mating-type (MAT) locus that controls sexual reproduction of Blastomyces dermatitidis. Eukaryot Cell. 2013;12:109–17.
   PubMedGoogle Scholar
• Heitman J. Evolution of sexual reproduction: a view from the Fungal Kingdom supports an evolutionary epoch with sex before sexes. Fungal Biol Rev. 2015;29:108–17.
   PubMed Web of Science ®Google Scholar
• Sugar AM, Picard M, Wagner R, et al. Interactions between human bronchoalveolar macrophages and Blastomyces dermatitidis conidia: demonstration of fungicidal and fungistatic effects. J Infect Dis. 1995;171:1559–62.
   PubMed Web of Science ®Google Scholar
• Rocco NM, Carmen JC, Klein BS. Blastomyces dermatitidis yeast cells inhibit nitric oxide production by alveolar macrophage inducible nitric oxide synthase. Infect Immun. 2011;79:2385–95.
   PubMed Web of Science ®Google Scholar
• Nanjappa SG, Hernandez-Santos N, Galles K, et al. Intrinsic MyD88-Akt1-mTOR Signaling Coordinates Disparate Tc17 and Tc1 Responses during Vaccine Immunity against Fungal Pneumonia. PLoS Pathog. 2015;11:e1005161.
   PubMed Web of Science ®Google Scholar
• Wuthrich M, Gern B, Hung CY, et al. Vaccine-induced protection against 3 systemic mycoses endemic to North America requires Th17 cells in mice. J Clin Invest. 2011;121:554–68.
   PubMed Web of Science ®Google Scholar
• Klein BS, Bradsher RW, Vergeront JM, et al. Development of long-term specific cellular immunity after acute Blastomyces dermatitidis infection: assessments following a large point-source outbreak in Wisconsin. J Infect Dis. 1990;161:97–101.
   PubMed Web of Science ®Google Scholar
• Klein BS, Vergeront JM, Kaufman L, et al. Serological tests for blastomycosis: assessments during a large point-source outbreak in Wisconsin. J Infect Dis. 1987;155:262–8.
   PubMed Web of Science ®Google Scholar
• Richer SM, Smedema ML, Durkin MM, et al. Development of a highly sensitive and specific blastomycosis antibody enzyme immunoassay using Blastomyces dermatitidis surface protein BAD-1. Clin Vaccine Immunol. 2014;21:143–6.
   PubMed Web of Science ®Google Scholar
• Sidamonidze K, Peck MK, Perez M, et al. Real-time PCR assay for identification of Blastomyces dermatitidis in culture and in tissue. J Clin Microbiol. 2012;50:1783–6.
   PubMed Web of Science ®Google Scholar
• Tebbets B, Stewart D, Lawry S, et al. Identification and characterization of antifungal compounds using a Saccharomyces cerevisiae reporter bioassay. PLoS One. 2012;7:e36021.
   PubMedGoogle Scholar
• Tebbets B, Yu Z, Stewart D, et al. Identification of antifungal natural products via Saccharomyces cerevisiae bioassay: insights into macrotetrolide drug spectrum, potency and mode of action. Med Mycol. 2013;51:280–9.
   PubMed Web of Science ®Google Scholar
• Wuthrich M, Filutowicz HI, Klein BS. Mutation of the WI-1 gene yields an attenuated blastomyces dermatitidis strain that induces host resistance. J Clin Invest. 2000;106:1381–9.
   PubMed Web of Science ®Google Scholar
• Wuthrich M, Brandhorst TT, Sullivan TD, et al. Calnexin induces expansion of antigen-specific CD4(+) T cells that confer immunity to fungal ascomycetes via conserved epitopes. Cell Host Microbe. 2015;17:452–65.
   PubMed Web of Science ®Google Scholar
• Wang H, Lee TJ, Fites SJ, et al. Ligation of Dectin-2 with a novel microbial ligand promotes adjuvant activity for vaccination. PLoS Pathog. 2017;13:e1006568.
   PubMed Web of Science ®Google Scholar