Martinez Barrera Stephani, Hatchell Emma, Byrum Stephanie D, Mackintosh Samuel G, Kozubowski Lukasz
Department of Genetics and Biochemistry, Eukaryotic Pathogens Innovation Center, Clemson University, Clemson, SC, United States of America.
Department of Biochemistry and Molecular Biology, University of Arkansas for Medical Sciences, Little Rock, AR, United States of America.
PLoS One. 2024 Dec 17;19(12):e0313444. doi: 10.1371/journal.pone.0313444. eCollection 2024.
Cryptococcus neoformans is a pathogenic basidiomycetous yeast that primarily infects immunocompromised individuals. Fatal outcome of cryptococcosis depends on the ability of C. neoformans to sense and adapt to 37°C. A complex of conserved filament forming GTPases, called septins, composed of Cdc3, Cdc10, Cdc11, and Cdc12, assembles at the mother-bud neck in C. neoformans. Septins Cdc3 and Cdc12 are essential for proliferation of C. neoformans at 37°C and for virulence in the Galleria mellonella model of infection, presumably due to their requirement for septin complex formation, and the involvement in cytokinesis. However, how exactly Cdc3, and Cdc12 contribute to C. neoformans growth at 37°C remains unknown. Based on studies investigating roles of septins in Saccharomyces cerevisiae, septin complex at the mother-bud neck of C. neoformans is predicted to interact with proteins involved in cell cycle control, morphogenesis, and cytokinesis, but the septin-associated proteome in C. neoformans has not been investigated. Here, we utilized tandem mass spectrometry to define C. neoformans proteins that associate with either Cdc3 or Cdc10 at ∼25°C or after the shift to 37°C. Our findings unveil a diverse array of septin-associated proteins, highlighting potential roles of septins in cell division, and stress response. Two proteins, identified as associated with both Cdc3 and Cdc10, the actin-binding protein profilin, which was detected at both temperatures, and ATP-binding multi-drug transporter Afr1, which was detected exclusively at 37°C, were further confirmed by co-immunoprecipitation. We also confirmed that association of Cdc3 with Afr1 was enhanced at 37°C. Upon shift to 37°C, septins Cdc3 and Cdc10 exhibited altered localization and Cdc3 partially co-localized with Afr1. In addition, we also investigated changes to levels of individual C. neoformans proteins upon shift from ∼25 to 37°C in exponentially grown culture and when cells entered stationary phase at ∼25°C. Our study reveals changes to C. neoformans proteome associated with heat and nutrient deprivation stresses and provides a landscape of septin-associated C. neoformans proteome, which will facilitate elucidating the biology of septins and mechanisms of stress response in this fungal pathogen.
新型隐球菌是一种致病性担子菌酵母,主要感染免疫功能低下的个体。隐球菌病的致命后果取决于新型隐球菌感知并适应37°C的能力。由Cdc3、Cdc10、Cdc11和Cdc12组成的一组保守的丝状形成GTP酶(称为隔膜蛋白)在新型隐球菌的母细胞-芽颈处组装。隔膜蛋白Cdc3和Cdc12对于新型隐球菌在37°C下的增殖以及在感染的大蜡螟模型中的毒力至关重要,这可能是由于它们对隔膜蛋白复合物形成的需求以及参与胞质分裂。然而,Cdc3和Cdc12究竟如何促进新型隐球菌在37°C下的生长仍不清楚。基于对酿酒酵母中隔膜蛋白作用的研究,预计新型隐球菌母细胞-芽颈处的隔膜蛋白复合物会与参与细胞周期控制、形态发生和胞质分裂的蛋白质相互作用,但尚未对新型隐球菌中与隔膜蛋白相关的蛋白质组进行研究。在这里,我们利用串联质谱法来确定在约25°C或转移至37°C后与Cdc3或Cdc10相关的新型隐球菌蛋白质。我们的研究结果揭示了一系列与隔膜蛋白相关的蛋白质,突出了隔膜蛋白在细胞分裂和应激反应中的潜在作用。通过免疫共沉淀进一步证实了两种与Cdc3和Cdc10都相关的蛋白质,即肌动蛋白结合蛋白丝切蛋白,在两个温度下均被检测到,以及ATP结合多药转运蛋白Afr1,仅在37°C时被检测到。我们还证实,在37°C时Cdc3与Afr1的结合增强。转移至37°C后,隔膜蛋白Cdc3和Cdc10表现出定位改变,且Cdc3与Afr1部分共定位。此外,我们还研究了在指数生长培养中从约25°C转移至37°C以及细胞在约25°C进入稳定期时新型隐球菌单个蛋白质水平的变化。我们的研究揭示了与热应激和营养剥夺应激相关的新型隐球菌蛋白质组的变化,并提供了与隔膜蛋白相关的新型隐球菌蛋白质组图谱,这将有助于阐明该真菌病原体中隔膜蛋白的生物学特性和应激反应机制。