Characterization of the APSES-family transcriptional regulators of

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Characterization of the APSES-family transcriptional regulators of

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Characterization of the APSES-family transcriptional regulators of

FEMS Yeast Research, 18, 2018, foy087

doi: 10.1093/femsyr/foy087

Advance Access Publication Date: 7 August 2018

Research Article

RESEARCH ARTICLE

Characterization of the APSES-family transcriptional regulators ofHistoplasma capsulatum

Larissa V. G. Longo

1,

, Stephanie C. Ray

2,

, Rosana Puccia 1 and Chad A. Rappleye

2,,

1 Departamento de Microbiologia, Imunologia e Parasitologia, Escola Paulista de Medicina, Universidade Federal de Sao Paulo, Rua Botucatu, 862, Sao Paulo 04023062, Brazil and 2

Department of Microbiology, Ohio

State University, 484 W. 12th Avenue, 540 Biological Sciences Bldg., Columbus, OH 43210, USA

Corresponding author:Department of Microbiology, Ohio State University, 484 W. 12th Avenue, 540 Biological Sciences Bldg., Columbus, OH 43210, USA.

Tel:+01-(614)-247-2718; E-mail:rappleye.1@osu.edu

One sentence summary:Aspects of yeast and mycelial growth of the dimorphic fungal pathogenHistoplasma capsulatumare controlled by APSES-family

transcription factors.

Equally contributing authors.

Editor:Carol Munro

Chad A. Rappleye,http://orcid.org/0000-0001-7880-5958

ABSTRACT

The

fungal APSES protein family of transcription factors is characterized by a conserved DNA-binding motif

facilitating regulation of gene expression in fungal development and other biological processes. However, their functions in

the thermally dimorphic fungal pathogenHistoplasma capsulatumare unexplored.Histoplasma capsulatumswitches between

avirulent hyphae in the environment and virulent yeasts in mammalian hosts. We identi?ed ?ve APSES domain-containing

proteins inH. capsulatumhomologous to Swi6, Mbp1, Stu1 and Xbp1 proteins and one protein found in related

Ascomycetes (APSES-family protein 1; Afp1). Through transcriptional analyses and RNA interference-based functional

tests we explored their roles in fungal biology and virulence. Mbp1 serves an essential role and Swi6 contributes to full

yeast cell growth. Stu1 is primarily expressed in mycelia and is necessary for aerial hyphae development and conidiation.

Xbp1 is the only factor enriched speci?cally in yeast cells. The APSES proteins do not regulate conversion of conidia

into yeast and hyphal morphologies. The APSES-family transcription factors are not individually required forH. capsulatum

infection of cultured macrophages or murine infection, nor do any contribute signi?cantly to resistance to cellular stresses

including cell wall perturbation, osmotic stress, oxidative stress or antifungal treatment. Further studies of the downstream

genes regulated by the individual APSES factors will be helpful in revealing their functional roles inH. capsulatumbiology.

Keywords:APSES; transcription factor;Histoplasma capsulatum; dimorphism; pathogenesis

INTRODUCTION

The APSES domain-containing proteins constitute a family of transcription factors speci?c to fungi that share a highly conserved basic helix-loop-helix (bHLH) DNA-binding motif, referred to asthe APSES domain (Aramayoetal.1996). TheAPSES proteins from different fungi are divided into four major groups (A, B, C and D) based on relatedness of the APSES-domain (Zhao et al.2015). Group A includes the Mbp1, Swi4 and Swi6 homologs

Received:9 February 2018;Accepted:6 August 2018

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2FEMS Yeast Research, 2018, Vol. 18, No. 8

important for fungal growth and progression through the cell cycle (Kochet al.1993; Kochet al.1996; Siegmund and Nasmyth

1996). Single mutants inSaccharomyces cerevisiaeare viable but

display impaired growth and budding (Kochet al.1993;Gray et al.1997; Wijnen, Landman and Futcher2002; Bean, Siggia and Cross2006; White, Riles and Cohen2009;) and similar pheno- types are seen inCandida albicansandMagnaporthe oryzaemu- tants. InCryptococcus neoformans, the two APSES-family proteins, Mbp1 and Mbs1, belong to group A, but their functions appear to have diverged from those of Ascomycetes (Songet al.2012). Group B is comprised of the Xbp1 proteins. Group C APSES pro- teins regulate fungal differentiation. Group D includes proteins de?ned mostly by bioinformatic searches. The number of APSES proteins varies among fungal species suggesting their func- tions have specialized for the speci?c biology or niches of dif- ferent fungi;Aspergillus fumigatus,Aspergillus nidulans,C.albicans andNeurospora crassahave ?ve identi?ed APSES members each, whereasC.neoformanshasonlytwoandS.cerevisiaehassix(Zhao et al.2015). In the Hemiascomycetes (e.g.SaccharomycesandCandida species), group C-I proteins (Efg1, Efh1, Phd1 and Sok2) regulate ?lamentous versus yeast growth. InS. cerevisiae, Phd1 activates the pseudohyphal growth program in response to nitrogen star- vation(GimenoandFink1994;Hanlonetal.2011)andsuppresses ?lamentation defects (Lorenz and Heitman1998), whereas Sok2 represses pseudohyphal differentiation (Wardet al.1995;Pan and Heitman2000).Candida albicanshas two closely related group C ASPES proteins, Efg1 and Efh1, which link the regula- tion of yeast-to-hyphal transition to virulence (Loet al.1997). Efg1 plays a key role in formation of hyphae, a fungal cell type required for adherence and invasion of host cell and vir- ulence in murine models of disseminated and oral candidiasis (Loet al.1997; Stoldtet al.1997; Doedtet al.2004;Parket al.

2005).

In Euascomycetes, the group C-II proteins (StuA/Asm1 ho- mologs) are key regulators of mycelial growth and differenti- ation of sexual and/or asexual reproductive structures (Borne- man, Hynes and Andrianopoulos2002; Sheppardet al.2005; Lysoeet al.2011; Pasqualiet al.2013;Huet al.2015;Soyer et al.2015). InA. nidulans, mutants de?cient in StuA pro- duce smaller conidiophores that lack phialides and produce few conidia (Miller, Wu and Miller1992).Aspergillus fumiga- tusStuA is also required for conidiation and mutants show abnormal conidiophores that bear only a small number of