Calcineurin-mediated intracellular organelle calcium homeostasis is required for the survival of fungal pathogens upon extracellular calcium stimuli

References

• Islam MS. Calcium signaling: from basic to bedside. Adv Exp Med Biol. 2020;1131:1–6.
   PubMed Web of Science ®Google Scholar
• Rosendo-Pineda MJ, Moreno CM, Vaca L. Role of ion channels during cell division. Cell Calcium. 2020;91:102258.
   PubMed Web of Science ®Google Scholar
• Carafoli E. Intracellular calcium homeostasis. Annu Rev Biochem. 1987;56(1):395–433.
   PubMed Web of Science ®Google Scholar
• Cyert MS, Philpott CC. Regulation of cation balance in Saccharomyces cerevisiae. Genetics. 2013;193:677–713.
   PubMed Web of Science ®Google Scholar
• Blatzer M, Latge JP. Metal-homeostasis in the pathobiology of the opportunistic human fungal pathogen Aspergillus fumigatus. Cur Opin Microbiol. 2017;40: 152–159.
   PubMed Web of Science ®Google Scholar
• Park HS, Lee SC, Cardenas ME, et al. Calcium-Calmodulin-Calcineurin signaling: a globally conserved virulence cascade in eukaryotic microbial pathogens. Cell Host Microbe. 2019;26(4):453–462.
   PubMed Web of Science ®Google Scholar
• Thewes S. Calcineurin-Crz1 signaling in lower eukaryotes. Eukaryot Cell. 2014;13(6):694–705.
   PubMedGoogle Scholar
• Cunningham KW. Acidic calcium stores of Saccharomyces cerevisiae. Cell Calcium. 2011;50(2):129–1238.
   PubMed Web of Science ®Google Scholar
• Miseta A, Fu L, Kellermayer R, et al. The golgi apparatus plays a significant role in the maintenance of Ca2+ Homeostasis in the vps33Δ Vacuolar biogenesis mutant of Saccharomyces cerevisiae. J Biol Chem. 1999a;274(9):5939–5947.
   PubMed Web of Science ®Google Scholar
• Miseta A, Kellermayer R, Aiello DP, et al. The vacuolar Ca2+/H+ exchanger Vcx1p/Hum1p tightly controls cytosolic Ca2+ levels in S. cerevisiae. FEBS Lett. 1999b;451(2):132–136.
   PubMed Web of Science ®Google Scholar
• Munoz A, Chu M, Marris PI, et al. Specific domains of plant defensins differentially disrupt colony initiation, cell fusion and calcium homeostasis in Neurospora crassa. Mol Microbiol. 2014;92(6):1357–1374.
   PubMed Web of Science ®Google Scholar
• Dolgin E. How secret conversations inside cells are transforming biology. Nature. 2019;567(7747):162–164.
   PubMed Web of Science ®Google Scholar
• La Rovere RM, Roest G, Bultynck G, et al. Intracellular Ca2+ signaling and Ca2+ microdomains in the control of cell survival, apoptosis and autophagy. Cell Calcium. 2016;60:74–87.
   PubMed Web of Science ®Google Scholar
• Dunn T, Gable K, Beeler T. Regulation of cellular Ca2+ by yeast vacuoles. J Cell Biol. 1994;269:7273–7278.
   Google Scholar
• Forster C, Kane PM. Cytosolic Ca2+ homeostasis is a constitutive function of the V-ATPase in Saccharomyces cerevisiae. J Biol Chem. 2000;275(49):38245–38253.
   PubMed Web of Science ®Google Scholar
• Kmetzsch L, Staats CC, Simon E, et al. The vacuolar Ca2+ exchanger Vcx1 is involved in Calcineurin-Dependent Ca2+ Tolerance and virulence in Cryptococcus neoformans. Eukaryot Cell. 2010a;9(11):1798–1805.
   PubMedGoogle Scholar
• Chang Y, Schlenstedt G, Flockerzi V, et al. Properties of the intracellular transient receptor potential (TRP) channel in yeast, Yvc1. FEBS Lett. 2010;584(10):2028–2032.
   PubMed Web of Science ®Google Scholar
• Denis V, Cyert MS. Internal Ca2+ release in yeast is triggered by hypertonic shock and mediated by a TRP channel homologue. J Cell Biol. 2002;156(1):29–34.
   PubMed Web of Science ®Google Scholar
• Hamamoto S, Mori Y, Yabe I, et al. In vitro and in vivo characterization of modulation of the vacuolar cation channel TRPY 1 from Saccharomyces cerevisiae. Febs J. 2018;285(6):1146–1161.
   PubMed Web of Science ®Google Scholar
• Lange I, Yamamoto S, Partida-Sanchez S, et al. TRPM2+ functions as a lysosomal Ca2+ -release channel in beta cells. Sci Signal. 2009; (71):2. 10.1126/scisignal.2000278.
   Web of Science ®Google Scholar
• Yu Q, Wang F, Zhao Q, et al. A novel role of the vacuolar calcium channel Yvc1 in stress response, morphogenesis and pathogenicity of candida albicans. Int J Med Microbiol. 2014;304(3–4):339–350.
   PubMed Web of Science ®Google Scholar
• Cunningham KW, Fink GR. Calcineurin inhibits VCX1-dependent H+/Ca2+ exchange and induces Ca2+ ATPases in Saccharomyces cerevisiae. Mol Cell Biol. 1996;16(5):2226–2237.
   PubMed Web of Science ®Google Scholar
• Dinamarco TM, Freitas FZ, Almeida RS, et al. Functional characterization of an Aspergillus fumigatus calcium transporter (PmcA) that is essential for fungal infection. PloS One. 2012;7(5):e37591.
   PubMed Web of Science ®Google Scholar
• Ferreira RT, Silva ARC, Pimentel C, et al. Arsenic stress elicits cytosolic Ca2+ bursts and Crz1 activation in Saccharomyces cerevisiae. Microbiology-Sgm. 2012;158(9):2293–2302.
   PubMed Web of Science ®Google Scholar
• Kmetzsch L, Staats CC, Simon E, et al. The vacuolar Ca2+ exchanger Vcx1 is involved in calcineurin-dependent Ca2+ tolerance and virulence in Cryptococcus neoformans. Eukaryot Cell. 2010b;9(11):1798–1805.
   PubMedGoogle Scholar
• Klionsky DJ. Cell biology – Autophagy as a regulated pathway of cellular degradation. Science. 2000;290(5497):1717–1721.
   PubMed Web of Science ®Google Scholar
• Nakatogawa H. Mechanisms governing autophagosome biogenesis. Nat RevMol Cell Biol. 2020;21:439–458.
   Web of Science ®Google Scholar
• Liu R, Li J, Zhang T, et al. Itraconazole suppresses the growth of glioblastoma through induction of autophagy: involvement of abnormal cholesterol trafficking. Autophagy. 2014;10(7):1241–1255.
   PubMed Web of Science ®Google Scholar
• Wang Y, Zhang H. Regulation of autophagy by mTOR signaling pathway. Adv Exp Med Biol. 2019;1206:67–83.
   PubMed Web of Science ®Google Scholar
• Yi C, Tong JJ, Yu L. Mitochondria: the hub of energy deprivation-induced autophagy. Autophagy. 2018;14:1084–1085.
   PubMed Web of Science ®Google Scholar
• Scarlatti F, Granata R, Meijer AJ, et al. Does autophagy have a license to kill mammalian cells?. Cell Death Differ. 2009;16(1):12–20.
   PubMed Web of Science ®Google Scholar
• White E, DiPaola RS. The double-edged sword of autophagy modulation in cancer. Clin Cancer Res. 2009;15(17):5308–5316.
   PubMed Web of Science ®Google Scholar
• Denning DW, Bromley MJ. Infectious disease. How to bolster the antifungal pipeline. Science. 2015;347(6229):1414–1416.
   PubMed Web of Science ®Google Scholar
• Juvvadi PR, Lee SC, Heitman J, et al. Calcineurin in fungal virulence and drug resistance: prospects for harnessing targeted inhibition of calcineurin for an antifungal therapeutic approach. Virulence. 2017;8(2):186–197.
   PubMed Web of Science ®Google Scholar
• Steinbach WJ, Cramer RA Jr., Perfect BZ, et al. Calcineurin controls growth, morphology, and pathogenicity in Aspergillus fumigatus. Eukaryot Cell. 2006;5(7):1091–1103.
   PubMedGoogle Scholar
• Steinbach WJ, Cramer RA Jr., Perfect BZ, et al. Calcineurin inhibition or mutation enhances cell wall inhibitors against Aspergillus fumigatus. Antimicrob Agents Chemother. 2007;51(8):2979–2981.
   PubMed Web of Science ®Google Scholar
• Fox DS, Heitman J. Good fungi gone bad: the corruption of calcineurin. Bioessays. 2002;24(10):894–903.
   PubMed Web of Science ®Google Scholar
• Park HS, Chow EW, Fu C, et al. Calcineurin targets involved in stress survival and fungal virulence. PLoS Pathog. 2016;12(9):e1005873.
   PubMed Web of Science ®Google Scholar
• Juvvadi PR, Fortwendel JR, Rogg LE, et al. Localization and activity of the calcineurin catalytic and regulatory subunit complex at the septum is essential for hyphal elongation and proper septation in aspergillus fumigatus. Mol Microbiol. 2011;82(5):1235–1259.
   PubMed Web of Science ®Google Scholar
• Nelson G, Kozlova-Zwinderman O, Collis AJ, et al. Calcium measurement in living filamentous fungi expressing codon-optimized aequorin. Mol Microbiol. 2004;52(5):1437–1550.
   PubMed Web of Science ®Google Scholar
• Kikuma T, Ohneda M, Arioka M, et al. Functional analysis of the ATG8 homologue Aoatg8 and role of autophagy in differentiation and germination in Aspergillus oryzae. Eukaryot Cell. 2006;5(8):1328–1336.
   PubMedGoogle Scholar
• Kotani T, Kirisako H, Koizumi M, et al. The Atg2-Atg18 complex tethers pre-autophagosomal membranes to the endoplasmic reticulum for autophagosome formation. Proc Natl Acad Sci U S A. 2018;115(41):10363–10368.
   PubMed Web of Science ®Google Scholar
• Tang Z, Takahashi Y, Wang HG. ATG2 regulation of phagophore expansion at mitochondria-associated ER membranes. Autophagy. 2019;15(12):2165–2166.
   PubMed Web of Science ®Google Scholar
• Wang S, Liu X, Qian H, et al. Calcineurin and Calcium channel CchA coordinate the salt stress response by regulating Cytoplasmic Ca2+ Homeostasis in Aspergillus nidulans. Appl Environ Microbiol. 2016;82(11):3420–3430.
   PubMed Web of Science ®Google Scholar
• Zhang C, Lu L. Precise and efficient in-frame integration of an exogenous GFP tag in Aspergillus fumigatus by a CRISPR system. Methods Mol Biol. 2017;1625:249–258.
   PubMedGoogle Scholar
• Greene V, Cao H, Schanne FA, et al. Oxidative stress-induced calcium signalling in Aspergillus nidulans. Cell Signaling. 2002;14(5):437–443.
   PubMed Web of Science ®Google Scholar
• Song J, Liu X, Zhai P, et al. A putative mitochondrial calcium uniporter in A. fumigatus contributes to mitochondrial Ca2+ homeostasis and stress responses. Fungal Genet Biol. 2016a;94:15–22.
   PubMed Web of Science ®Google Scholar
• Song J, Zhai P, Zhang Y, et al. The aspergillus fumigatus damage resistance protein family coordinately regulates ergosterol biosynthesis and azole susceptibility. mBio. 2016b;7(1):e01919–01915.
   PubMed Web of Science ®Google Scholar
• Zhang C, Meng XH, Wei XL, et al. Highly efficient CRISPR mutagenesis by microhomology-mediated end joining in Aspergillus fumigatus. Fungal Genet Biol. 2016a;86:47–57.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Zheng Q, Sun C, et al. Palmitoylation of the Cysteine residue in the DHHC Motif of a Palmitoyl Transferase Mediates Ca2+ Homeostasis in Aspergillus. PLoS Genet. 2016b;12(4):e1005977.
   PubMed Web of Science ®Google Scholar
• Park YJ, Yoo SA, Kim M, et al. The role of Calcium-Calcineurin-NFAT signaling pathway in health and autoimmune diseases. Front Immunol. 2020;11:195.
   PubMed Web of Science ®Google Scholar
• Blankenship JR, Heitman J. Calcineurin is required for Candida albicans to survive calcium stress in serum. Infect Immun. 2005;73(9):5767–5774.
   PubMed Web of Science ®Google Scholar
• Ma Y, Sugiura R, Koike A, et al. Transient receptor potential (TRP) and Cch1-Yam8 channels play key roles in the regulation of cytoplasmic Ca2+ in fission yeast. PLoS One. 2011;6(7):e22421.
   PubMed Web of Science ®Google Scholar
• Bonilla M, Cunningham KW. Mitogen-activated Protein Kinase Stimulation of Ca2+ Signaling is required for survival of endoplasmic reticulum stress in yeast. Mol Biol Cell. 2003;14(10):4296–4305.
   PubMed Web of Science ®Google Scholar
• Pinchai N, Juvvadi PR, Fortwendel JR, et al. The Aspergillus fumigatus P-type Golgi apparatus Ca2+/Mn2+ ATPase PmrA is involved in cation homeostasis and cell wall integrity but is not essential for pathogenesis. Eukaryot Cell. 2010;9(3):472–476.
   PubMedGoogle Scholar
• Yu Q, Wang H, Xu N, et al. Spf1 strongly influences calcium homeostasis, hyphal development, biofilm formation and virulence in Candida albicans. Microbiology. 2012;158(9):2272–2282.
   PubMed Web of Science ®Google Scholar
• Groll AH, De Lucca AJ, Walsh TJ. Emerging targets for the development of novel antifungal therapeutics. Trends Microbiol. 1998;6(3):117–124.
   PubMed Web of Science ®Google Scholar
• Juvvadi PR, Fox D 3rd, Bobay BG, et al. Harnessing calcineurin-FK506-FKBP12 crystal structures from invasive fungal pathogens to develop antifungal agents. Nature Commun. 2019;10(1):4275.
   PubMed Web of Science ®Google Scholar