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Calcium Cation Cycling and Signaling Pathways in Fungi

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Biology of the Fungal Cell

Part of the book series: The Mycota ((MYCOTA,volume 8))

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Abstract

As in other eukaryotic cells, fungal cytosolic calcium cation concentrations are maintained at extreme low level to function as the second messenger. On the contrary, high concentrations of Ca2+ are immediately available for influx from outside of the cell into the cytoplasm and the intracellular Ca2+ stores, to transmit a variety of intracellular or extracellular cues. The Ca2+ channels, pumps, exchangers, and antiporters localized in the membrane as well as Ca2+ sensors with their signal effectors in the cytoplasm are highly networked to regulate, conduct, and translate various signals. Here, we retrospect the relative knowledge and advantages on Ca2+ cycling and signaling pathways, especially in the fungal kingdom.

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References

  • Adiele RC, Stevens D, Kamunde C (2012) Features of cadmium and calcium uptake and toxicity in rainbow trout (Oncorhynchus mykiss) mitochondria. Toxicol In Vitro 26(1):164–173

    Article  CAS  PubMed  Google Scholar 

  • Aguilar PS, Engel A, Walter P (2007) The plasma membrane proteins Prm1 and Fig1 ascertain fidelity of membrane fusion during yeast mating. Mol Biol Cell 18(2):547–556

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Antebi A, Fink GR (1992) The yeast Ca(2+)-ATPase homologue, PMR1, is required for normal Golgi function and localizes in a novel Golgi-like distribution. Mol Biol Cell 3(6):633–654

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baksh S, Burakoff SJ (2000) The role of calcineurin in lymphocyte activation. Semin Immunol 12(4):405–415

    Article  CAS  PubMed  Google Scholar 

  • Bates S, MacCallum DM, Bertram G, Munro CA, Hughes HB, Buurman ET, Brown AJ, Odds FC, Gow NA (2005) Candida albicans Pmr1p, a secretory pathway P-type Ca2+/Mn2+-ATPase, is required for glycosylation and virulence. J Biol Chem 280(24):23408–23415

    Article  CAS  PubMed  Google Scholar 

  • Batistic O, Kudla J (2012) Analysis of calcium signaling pathways in plants. Biochim Biophys Acta 1820(8):1283–1293

    Article  CAS  PubMed  Google Scholar 

  • Bazil JN, Dash RK (2011) A minimal model for the mitochondrial rapid mode of Ca(2)+ uptake mechanism. PLoS One 6(6):e21324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bentivoglio M, Jones EG, Mazzarello P, Ribak CE, Shepherd GM, Swanson LW (2011) Camillo Golgi and modern neuroscience. Brain Res Rev 66(1–2):1–4

    Article  PubMed  Google Scholar 

  • Bernardi P, Di Lisa F (2014) The mitochondrial permeability transition pore: molecular nature and role as a target in cardioprotection. J Mol Cell Cardiol 78:100–106

    Article  PubMed  CAS  Google Scholar 

  • Bezprozvanny I (2005) The inositol 1,4,5-trisphosphate receptors. Cell Calcium 38(3–4):261–272

    Article  CAS  PubMed  Google Scholar 

  • Blomeyer CA, Bazil JN, Stowe DF, Pradhan RK, Dash RK, Camara AK (2013) Dynamic buffering of mitochondrial Ca2+ during Ca2+ uptake and Na+-induced Ca2+ release. J Bioenerg Biomembr 45(3):189–202

    Article  CAS  PubMed  Google Scholar 

  • Bowman BJ, Draskovic M, Freitag M, Bowman EJ (2009) Structure and distribution of organelles and cellular location of calcium transporters in Neurospora crassa. Eukaryot Cell 8(12):1845–1855

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bowman BJ, Abreu S, Margolles-Clark E, Draskovic M, Bowman EJ (2011) Role of four calcium transport proteins, encoded by nca-1, nca-2, nca-3, and cax, in maintaining intracellular calcium levels in Neurospora crassa. Eukaryot Cell 10(5):654–661

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brand A, Shanks S, Duncan VM, Yang M, Mackenzie K, Gow NA (2007) Hyphal orientation of Candida albicans is regulated by a calcium-dependent mechanism. Curr Biol 17(4):347–352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brini M, Carafoli E (2009) Calcium pumps in health and disease. Physiol Rev 89(4):1341–1378

    Article  CAS  PubMed  Google Scholar 

  • Brunner JM, Plattet P, Doucey MA, Rosso L, Curie T, Montagner A, Wittek R, Vandelvelde M, Zurbriggen A, Hirling H, Desvergne B (2012) Morbillivirus glycoprotein expression induces ER stress, alters Ca2+ homeostasis and results in the release of vasostatin. PLoS One 7(3):e32803

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bublitz M, Poulsen H, Morth JP, Nissen P (2010) In and out of the cation pumps: P-type ATPase structure revisited. Curr Opin Struct Biol 20(4):431–439

    Article  CAS  PubMed  Google Scholar 

  • Buntinas L, Gunter KK, Sparagna GC, Gunter TE (2001) The rapid mode of calcium uptake into heart mitochondria (RaM): comparison to RaM in liver mitochondria. Biochim Biophys Acta 1504(2–3):248–261

    Article  CAS  PubMed  Google Scholar 

  • Buttner S, Faes L, Reichelt WN, Broeskamp F, Habernig L, Benke S, Kourtis N, Ruli D, Carmona-Gutierrez D, Eisenberg T, D’Hooge P, Ghillebert R, Franssens V, Harger A, Pieber TR, Freudenberger P, Kroemer G, Sigrist SJ, Winderickx J, Callewaert G, Tavernarakis N, Madeo F (2013) The Ca2+/Mn2+ ion-pump PMR1 links elevation of cytosolic Ca(2+) levels to alpha-synuclein toxicity in Parkinson’s disease models. Cell Death Differ 20(3):465–477

    Article  CAS  PubMed  Google Scholar 

  • Calvert CM, Sanders D (1995) Inositol trisphosphate-dependent and -independent Ca2+ mobilization pathways at the vacuolar membrane of Candida albicans. J Biol Chem 270(13):7272–7280

    Article  CAS  PubMed  Google Scholar 

  • Carafoli E, Brini M (2000) Calcium pumps: structural basis for and mechanism of calcium transmembrane transport. Curr Opin Chem Biol 4(2):152–161

    Article  CAS  PubMed  Google Scholar 

  • Carafoli E, Santella L, Branca D, Brini M (2001) Generation, control, and processing of cellular calcium signals. Crit Rev Biochem Mol Biol 36(2):107–260

    Article  CAS  PubMed  Google Scholar 

  • Cavinder B, Hamam A, Lew RR, Trail F (2011) Mid1, a mechanosensitive calcium ion channel, affects growth, development, and ascospore discharge in the filamentous fungus Gibberella zeae. Eukaryot Cell 10(6):832–841

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chakraborty S, Hasan G (2012) IP3R, store-operated Ca2+ entry and neuronal Ca2+ homoeostasis in Drosophila. Biochem Soc Trans 40(1):279–281

    Article  CAS  PubMed  Google Scholar 

  • Chang Y, Schlenstedt G, Flockerzi V, Beck A (2010) Properties of the intracellular transient receptor potential (TRP) channel in yeast, Yvc1. FEBS Lett 584(10):2028–2032

    Article  CAS  PubMed  Google Scholar 

  • Chatfield-Reed K, Vachon L, Kwon EJ, Chua G (2016) Conserved and diverged functions of the calcineurin-activated Prz1 transcription factor in fission yeast. Genetics 202(4):1365–1375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cho JH, Ko KM, Singaravelu G, Ahnn J (2005) Caenorhabditis elegans PMR1, a P-type calcium ATPase, is important for calcium/manganese homeostasis and oxidative stress response. FEBS Lett 579(3):778–782

    Article  CAS  PubMed  Google Scholar 

  • Chow EW, Clancey SA, Billmyre RB, Averette AF, Granek JA, Mieczkowski P, Cardenas ME, Heitman J (2017) Elucidation of the calcineurin-Crz1 stress response transcriptional network in the human fungal pathogen Cryptococcus neoformans. PLoS Genet 13(4):e1006667

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cifuentes F, Gonzalez CE, Fiordelisio T, Guerrero G, Lai FA, Hernandez-Cruz A (2001) A ryanodine fluorescent derivative reveals the presence of high-affinity ryanodine binding sites in the Golgi complex of rat sympathetic neurons, with possible functional roles in intracellular Ca(2+) signaling. Cell Signal 13(5):353–362

    Article  CAS  PubMed  Google Scholar 

  • Coe H, Michalak M (2009) Calcium binding chaperones of the endoplasmic reticulum. Gen Physiol Biophys 28 Spec No Focus:F96–F103

    PubMed  Google Scholar 

  • Cronin SR, Rao R, Hampton RY (2002) Cod1p/Spf1p is a P-type ATPase involved in ER function and Ca2+ homeostasis. J Cell Biol 157(6):1017–1028

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cui J, Kaandorp JA, Ositelu OO, Beaudry V, Knight A, Nanfack YF, Cunningham KW (2009) Simulating calcium influx and free calcium concentrations in yeast. Cell Calcium 45(2):123–132

    Article  CAS  PubMed  Google Scholar 

  • Cunningham KW (2011) Acidic calcium stores of Saccharomyces cerevisiae. Cell Calcium 50(2):129–138

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cunningham KW, Fink GR (1994) Calcineurin-dependent growth control in Saccharomyces cerevisiae mutants lacking PMC1, a homolog of plasma membrane Ca2+ ATPases. J Cell Biol 124(3):351–363

    Article  CAS  PubMed  Google Scholar 

  • Cunningham KW, Fink GR (1996) Calcineurin inhibits VCX1-dependent H+/Ca2+ exchange and induces Ca2+ ATPases in Saccharomyces cerevisiae. Mol Cell Biol 16(5):2226–2237

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cyert MS (2003) Calcineurin signaling in Saccharomyces cerevisiae: how yeast go crazy in response to stress. Biochem Biophys Res Commun 311(4):1143–1150

    Article  CAS  PubMed  Google Scholar 

  • Day KJ, Staehelin LA, Glick BS (2013) A three-stage model of Golgi structure and function. Histochem Cell Biol 140(3):239–249

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Marchi E, Bonora M, Giorgi C, Pinton P (2014) The mitochondrial permeability transition pore is a dispensable element for mitochondrial calcium efflux. Cell Calcium 56(1):1–13

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Denton RM (2009) Regulation of mitochondrial dehydrogenases by calcium ions. Biochim Biophys Acta 1787(11):1309–1316

    Article  CAS  PubMed  Google Scholar 

  • Ding X, Yu Q, Xu N, Wang Y, Cheng X, Qian K, Zhao Q, Zhang B, Xing L, Li M (2013) Ecm7, a regulator of HACS, functions in calcium homeostasis maintenance, oxidative stress response and hyphal development in Candida albicans. Fungal Genet Biol 57:23–32

    Article  CAS  PubMed  Google Scholar 

  • Docampo R, Moreno SN (2011) Acidocalcisomes. Cell Calcium 50(2):113–119

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dominguez DC (2004) Calcium signalling in bacteria. Mol Microbiol 54(2):291–297

    Article  CAS  PubMed  Google Scholar 

  • Dong XP, Shen D, Wang X, Dawson T, Li X, Zhang Q, Cheng X, Zhang Y, Weisman LS, Delling M, Xu H (2010) PI(3,5)P(2) controls membrane trafficking by direct activation of mucolipin Ca(2+) release channels in the endolysosome. Nat Commun 1:38

    Article  PubMed  CAS  Google Scholar 

  • Dunn T, Gable K, Beeler T (1994) Regulation of cellular Ca2+ by yeast vacuoles. J Biol Chem 269(10):7273–7278

    CAS  PubMed  Google Scholar 

  • Durr G, Strayle J, Plemper R, Elbs S, Klee SK, Catty P, Wolf DH, Rudolph HK (1998) The medial-Golgi ion pump Pmr1 supplies the yeast secretory pathway with Ca2+ and Mn2+ required for glycosylation, sorting, and endoplasmic reticulum-associated protein degradation. Mol Biol Cell 9(5):1149–1162

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ermak G, Davies KJ (2002) Calcium and oxidative stress: from cell signaling to cell death. Mol Immunol 38(10):713–721

    Article  CAS  PubMed  Google Scholar 

  • Fischer M, Schnell N, Chattaway J, Davies P, Dixon G, Sanders D (1997) The Saccharomyces cerevisiae CCH1 gene is involved in calcium influx and mating. FEBS Lett 419(2–3):259–262

    Article  CAS  PubMed  Google Scholar 

  • Flegg MB, Rudiger S, Erban R (2013) Diffusive spatio-temporal noise in a first-passage time model for intracellular calcium release. J Chem Phys 138(15):154103

    Article  PubMed  CAS  Google Scholar 

  • Forster C, Kane PM (2000) Cytosolic Ca2+ homeostasis is a constitutive function of the V-ATPase in Saccharomyces cerevisiae. J Biol Chem 275(49):38245–38253

    Article  CAS  PubMed  Google Scholar 

  • Ganitkevich VY (2003) The role of mitochondria in cytoplasmic Ca2+ cycling. Exp Physiol 88(1):91–97

    Article  CAS  PubMed  Google Scholar 

  • Groenendyk J, Lynch J, Michalak M (2004) Calreticulin, Ca2+, and calcineurin – signaling from the endoplasmic reticulum. Mol Cells 17(3):383–389

    CAS  PubMed  Google Scholar 

  • Gunter TE, Gunter KK (2001) Uptake of calcium by mitochondria: transport and possible function. IUBMB Life 52(3–5):197–204

    Article  CAS  PubMed  Google Scholar 

  • Haiech J, Moreau M (2011) The calcium signal: a universal carrier to code, decode and transduce information. Biochimie 93(12):v

    Article  CAS  PubMed  Google Scholar 

  • Hartwig C, Bahre H, Wolter S, Beckert U, Kaever V, Seifert R (2014) cAMP, cGMP, cCMP and cUMP concentrations across the tree of life: high cCMP and cUMP levels in astrocytes. Neurosci Lett 579:183–187

    Article  CAS  PubMed  Google Scholar 

  • Hashimoto K, Kudla J (2011) Calcium decoding mechanisms in plants. Biochimie 93(12):2054–2059

    Article  CAS  PubMed  Google Scholar 

  • He W, Hu Z (2012) The role of the Golgi-resident SPCA Ca(2)(+)/Mn(2)(+) pump in ionic homeostasis and neural function. Neurochem Res 37(3):455–468

    Article  CAS  PubMed  Google Scholar 

  • Herchuelz A, Nguidjoe E, Jiang L, Pachera N (2013) Na(+)/Ca(2+) exchange and the plasma membrane Ca(2+)-ATPase in beta-cell function and diabetes. Adv Exp Med Biol 961:385–394

    Article  CAS  PubMed  Google Scholar 

  • Hernandez-Cruz A, Escobar AL, Jimenez N (1997) Ca(2+)-induced Ca2+ release phenomena in mammalian sympathetic neurons are critically dependent on the rate of rise of trigger Ca2+. J Gen Physiol 109(2):147–167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hohendanner F, McCulloch AD, Blatter LA, Michailova AP (2014) Calcium and IP3 dynamics in cardiac myocytes: experimental and computational perspectives and approaches. Front Pharmacol 5:35

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Horikawa Y, Goel A, Somlyo AP, Somlyo AV (1998) Mitochondrial calcium in relaxed and tetanized myocardium. Biophys J 74(3):1579–1590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iida H, Nakamura H, Ono T, Okumura MS, Anraku Y (1994) MID1, a novel Saccharomyces cerevisiae gene encoding a plasma membrane protein, is required for Ca2+ influx and mating. Mol Cell Biol 14(12):8259–8271

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ji G, Feldman M, Doran R, Zipfel W, Kotlikoff MI (2006) Ca2+-induced Ca2+ release through localized Ca2+ uncaging in smooth muscle. J Gen Physiol 127(3):225–235

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang H, Liu F, Zhang S, Lu L (2014a) Putative PmrA and PmcA are important for normal growth, morphogenesis and cell wall integrity, but not for viability in Aspergillus nidulans. Microbiology 160(Pt 11):2387–2395

    Article  CAS  PubMed  Google Scholar 

  • Jiang H, Shen Y, Liu W, Lu L (2014b) Deletion of the putative stretch-activated ion channel Mid1 is hypervirulent in Aspergillus fumigatus. Fungal Genet Biol 62:62–70

    Article  CAS  PubMed  Google Scholar 

  • Kakinuma Y, Ohsumi Y, Anraku Y (1981) Properties of H+-translocating adenosine triphosphatase in vacuolar membranes of Saccharomyces cerevisiae. J Biol Chem 256(21):10859–10863

    CAS  PubMed  Google Scholar 

  • Kanzaki M, Nagasawa M, Kojima I, Sato C, Naruse K, Sokabe M, Iida H (1999) Molecular identification of a eukaryotic, stretch-activated nonselective cation channel. Science 285(5429):882–886

    Article  CAS  PubMed  Google Scholar 

  • Katoh I, Sato S, Fukunishi N, Yoshida H, Imai T, Kurata S (2008) Apaf-1-deficient fog mouse cell apoptosis involves hypo-polarization of the mitochondrial inner membrane, ATP depletion and citrate accumulation. Cell Res 18(12):1210–1219

    Article  CAS  PubMed  Google Scholar 

  • Kellermayer R, Aiello DP, Miseta A, Bedwell DM (2003) Extracellular Ca(2+) sensing contributes to excess Ca(2+) accumulation and vacuolar fragmentation in a pmr1Delta mutant of S. cerevisiae. J Cell Sci 116.(Pt 8:1637–1646

    Article  CAS  PubMed  Google Scholar 

  • Kmetzsch L, Staats CC, Simon E, Fonseca FL, de Oliveira DL, Sobrino L, Rodrigues J, Leal AL, Nimrichter L, Rodrigues ML, Schrank A, Vainstein MH (2010) The vacuolar Ca(2)(+) exchanger Vcx1 is involved in calcineurin-dependent Ca(2)(+) tolerance and virulence in Cryptococcus neoformans. Eukaryot Cell 9(11):1798–1805

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kovacs-Bogdan E, Sancak Y, Kamer KJ, Plovanich M, Jambhekar A, Huber RJ, Myre MA, Blower MD, Mootha VK (2014) Reconstitution of the mitochondrial calcium uniporter in yeast. Proc Natl Acad Sci USA 111(24):8985–8990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Krizanova O, Ondrias K (2003) The inositol 1,4,5-trisphosphate receptor–transcriptional regulation and modulation by phosphorylation. Gen Physiol Biophys 22(3):295–311

    CAS  PubMed  Google Scholar 

  • Lanner JT, Georgiou DK, Joshi AD, Hamilton SL (2010) Ryanodine receptors: structure, expression, molecular details, and function in calcium release. Cold Spring Harb Perspect Biol 2(11):a003996

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li X, Qian J, Wang C, Zheng K, Ye L, Fu Y, Han N, Bian H, Pan J, Wang J, Zhu M (2011) Regulating cytoplasmic calcium homeostasis can reduce aluminum toxicity in yeast. PLoS One 6(6):e21148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li LH, Tian XR, Jiang Z, Zeng LW, He WF, Hu ZP (2013) The Golgi apparatus: panel point of cytosolic Ca(2+) regulation. Neurosignals 21(3–4):272–284

    Article  CAS  PubMed  Google Scholar 

  • Lissandron V, Podini P, Pizzo P, Pozzan T (2010) Unique characteristics of Ca2+ homeostasis of the trans-Golgi compartment. Proc Natl Acad Sci USA 107(20):9198–9203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu M, Du P, Heinrich G, Cox GM, Gelli A (2006) Cch1 mediates calcium entry in Cryptococcus neoformans and is essential in low-calcium environments. Eukaryot Cell 5(10):1788–1796

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu S, Hou Y, Liu W, Lu C, Wang W, Sun S (2015) Components of the calcium-calcineurin signaling pathway in fungal cells and their potential as antifungal targets. Eukaryot Cell 14(4):324–334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Locke EG, Bonilla M, Liang L, Takita Y, Cunningham KW (2000) A homolog of voltage-gated Ca(2+) channels stimulated by depletion of secretory Ca(2+) in yeast. Mol Cell Biol 20(18):6686–6694

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Losev E, Papanikou E, Rossanese OW, Glick BS (2008) Cdc1p is an endoplasmic reticulum-localized putative lipid phosphatase that affects Golgi inheritance and actin polarization by activating Ca2+ signaling. Mol Cell Biol 28(10):3336–3343

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Loukin S, Zhou X, Kung C, Saimi Y (2008) A genome-wide survey suggests an osmoprotective role for vacuolar Ca2+ release in cell wall-compromised yeast. FASEB J 22(7):2405–2415

    Article  CAS  PubMed  Google Scholar 

  • Luan S (2009) The CBL-CIPK network in plant calcium signaling. Trends Plant Sci 14(1):37–42

    Article  CAS  PubMed  Google Scholar 

  • Lustoza AC, Palma LM, Facanha AR, Okorokov LA, Okorokova-Facanha AL (2011) P(5A)-type ATPase Cta4p is essential for Ca2+ transport in the endoplasmic reticulum of Schizosaccharomyces pombe. PLoS One 6(11):e27843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marchi V, Sorin A, Wei Y, Rao R (1999) Induction of vacuolar Ca2+-ATPase and H+/Ca2+ exchange activity in yeast mutants lacking Pmr1, the Golgi Ca2+-ATPase. FEBS Lett 454(3):181–186

    Article  CAS  PubMed  Google Scholar 

  • Martin DC, Kim H, Mackin NA, Maldonado-Baez L, Evangelista CC Jr, Beaudry VG, Dudgeon DD, Naiman DQ, Erdman SE, Cunningham KW (2011) New regulators of a high affinity Ca2+ influx system revealed through a genome-wide screen in yeast. J Biol Chem 286(12):10744–10754

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Matheos DP, Kingsbury TJ, Ahsan US, Cunningham KW (1997) Tcn1p/Crz1p, a calcineurin-dependent transcription factor that differentially regulates gene expression in Saccharomyces cerevisiae. Genes Dev 11(24):3445–3458

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Micaroni M, Mironov AA (2010) Roles of Ca and secretory pathway Ca-ATPase pump type 1 (SPCA1) in intra-Golgi transport. Commun Integr Biol 3(6):504–507

    Article  PubMed  PubMed Central  Google Scholar 

  • Michalak M, Robert Parker JM, Opas M (2002) Ca2+ signaling and calcium binding chaperones of the endoplasmic reticulum. Cell Calcium 32(5–6):269–278

    Article  CAS  PubMed  Google Scholar 

  • Michelangeli F, Ogunbayo OA, Wootton LL (2005) A plethora of interacting organellar Ca2+ stores. Curr Opin Cell Biol 17(2):135–140

    Article  CAS  PubMed  Google Scholar 

  • Miseta A, Fu L, Kellermayer R, Buckley J, Bedwell DM (1999a) The Golgi apparatus plays a significant role in the maintenance of Ca2+ homeostasis in the vps33Delta vacuolar biogenesis mutant of Saccharomyces cerevisiae. J Biol Chem 274(9):5939–5947

    Article  CAS  PubMed  Google Scholar 

  • Miseta A, Kellermayer R, Aiello DP, Fu L, Bedwell DM (1999b) The vacuolar Ca2+/H+ exchanger Vcx1p/Hum1p tightly controls cytosolic Ca2+ levels in S. cerevisiae. FEBS Lett 451(2):132–136

    Article  CAS  PubMed  Google Scholar 

  • Molinaro P, Cantile M, Cuomo O, Secondo A, Pannaccione A, Ambrosino P, Pignataro G, Fiorino F, Severino B, Gatta E, Sisalli MJ, Milanese M, Scorziello A, Bonanno G, Robello M, Santagada V, Caliendo G, Di Renzo G, Annunziato L (2013) Neurounina-1, a novel compound that increases Na+/Ca2+ exchanger activity, effectively protects against stroke damage. Mol Pharmacol 83(1):142–156

    Article  CAS  PubMed  Google Scholar 

  • Moreno SN, Docampo R (2009) The role of acidocalcisomes in parasitic protists. J Eukaryot Microbiol 56(3):208–213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Muller EM, Locke EG, Cunningham KW (2001) Differential regulation of two Ca(2+) influx systems by pheromone signaling in Saccharomyces cerevisiae. Genetics 159(4):1527–1538

    CAS  PubMed  PubMed Central  Google Scholar 

  • Muller EM, Mackin NA, Erdman SE, Cunningham KW (2003) Fig1p facilitates Ca2+ influx and cell fusion during mating of Saccharomyces cerevisiae. J Biol Chem 278(40):38461–38469

    Article  CAS  PubMed  Google Scholar 

  • Nakano A (2004) Yeast Golgi apparatus–dynamics and sorting. Cell Mol Life Sci 61(2):186–191

    Article  CAS  PubMed  Google Scholar 

  • Okamura H, Denawa M, Ohniwa R, Takeyasu K (2003) P-type ATPase superfamily: evidence for critical roles for kingdom evolution. Ann N Y Acad Sci 986:219–223

    Article  CAS  PubMed  Google Scholar 

  • Onyewu C, Wormley FL Jr, Perfect JR, Heitman J (2004) The calcineurin target, Crz1, functions in azole tolerance but is not required for virulence of Candida albicans. Infect Immun 72(12):7330–7333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palmer CP, Zhou XL, Lin J, Loukin SH, Kung C, Saimi Y (2001) A TRP homolog in Saccharomyces cerevisiae forms an intracellular Ca(2+)-permeable channel in the yeast vacuolar membrane. Proc Natl Acad Sci USA 98(14):7801–7805

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pan Y, Mansfield KD, Bertozzi CC, Rudenko V, Chan DA, Giaccia AJ, Simon MC (2007) Multiple factors affecting cellular redox status and energy metabolism modulate hypoxia-inducible factor prolyl hydroxylase activity in vivo and in vitro. Mol Cell Biol 27(3):912–925

    Article  CAS  PubMed  Google Scholar 

  • Parlati F, Dominguez M, Bergeron JJ, Thomas DY (1995) Saccharomyces cerevisiae CNE1 encodes an endoplasmic reticulum (ER) membrane protein with sequence similarity to calnexin and calreticulin and functions as a constituent of the ER quality control apparatus. J Biol Chem 270(1):244–253

    Article  CAS  PubMed  Google Scholar 

  • Perrino BA, Fong YL, Brickey DA, Saitoh Y, Ushio Y, Fukunaga K, Miyamoto E, Soderling TR (1992) Characterization of the phosphatase activity of a baculovirus-expressed calcineurin A isoform. J Biol Chem 267(22):15965–15969

    CAS  PubMed  Google Scholar 

  • Pfeiffer DR, Gunter TE, Eliseev R, Broekemeier KM, Gunter KK (2001) Release of Ca2+ from mitochondria via the saturable mechanisms and the permeability transition. IUBMB Life 52(3–5):205–212

    Article  CAS  PubMed  Google Scholar 

  • Pittman JK (2011) Vacuolar Ca(2+) uptake. Cell Calcium 50(2):139–146

    Article  CAS  PubMed  Google Scholar 

  • Pivovarova NB, Hongpaisan J, Andrews SB, Friel DD (1999) Depolarization-induced mitochondrial Ca accumulation in sympathetic neurons: spatial and temporal characteristics. J Neurosci 19(15):6372–6384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pizzo P, Lissandron V, Capitanio P, Pozzan T (2011) Ca(2+) signalling in the Golgi apparatus. Cell Calcium 50(2):184–192

    Article  CAS  PubMed  Google Scholar 

  • Prole DL, Taylor CW (2012) Identification and analysis of cation channel homologues in human pathogenic fungi. PLoS One 7(8):e42404

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Raeymaekers L, Wuytack E, Willems I, Michiels CW, Wuytack F (2002) Expression of a P-type Ca(2+)-transport ATPase in Bacillus subtilis during sporulation. Cell Calcium 32(2):93

    Article  CAS  PubMed  Google Scholar 

  • Roome CJ, Empson RM (2013) The contribution of the sodium-calcium exchanger (NCX) and plasma membrane Ca(2+) ATPase (PMCA) to cerebellar synapse function. Adv Exp Med Biol 961:251–263

    Article  CAS  PubMed  Google Scholar 

  • Rudolph HK, Antebi A, Fink GR, Buckley CM, Dorman TE, LeVitre J, Davidow LS, Mao JI, Moir DT (1989) The yeast secretory pathway is perturbed by mutations in PMR1, a member of a Ca2+ ATPase family. Cell 58(1):133–145

    Article  CAS  PubMed  Google Scholar 

  • Rueda CB, Llorente-Folch I, Amigo I, Contreras L, Gonzalez-Sanchez P, Martinez-Valero P, Juaristi I, Pardo B, del Arco A, Satrustegui J (2014) Ca(2+) regulation of mitochondrial function in neurons. Biochim Biophys Acta 1837(10):1617–1624

    Article  CAS  PubMed  Google Scholar 

  • Rusnak F, Mertz P (2000) Calcineurin: form and function. Physiol Rev 80(4):1483–1521

    Article  CAS  PubMed  Google Scholar 

  • Samanta K, Douglas S, Parekh AB (2014) Mitochondrial calcium uniporter MCU supports cytoplasmic Ca2+ oscillations, store-operated Ca2+ entry and Ca2+-dependent gene expression in response to receptor stimulation. PLoS One 9(7):e101188

    Article  PubMed  PubMed Central  Google Scholar 

  • Samarao SS, Teodoro CE, Silva FE, Ribeiro CC, Granato TM, Bernardes NR, Retamal CA, Facanha AR, Okorokova-Facanha AL, Okorokov LA (2009) V H+-ATPase along the yeast secretory pathway: energization of the ER and Golgi membranes. Biochim Biophys Acta 1788(2):303–313

    Article  CAS  PubMed  Google Scholar 

  • Santo-Domingo J, Demaurex N (2010) Calcium uptake mechanisms of mitochondria. Biochim Biophys Acta 1797(6–7):907–912

    Article  CAS  PubMed  Google Scholar 

  • Schwaller B (2010) Cytosolic Ca2+ buffers. Cold Spring Harb Perspect Biol 2(11):a004051

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shnyder SD, Mangum JE, Hubbard MJ (2008) Triplex profiling of functionally distinct chaperones (ERp29/PDI/BiP) reveals marked heterogeneity of the endoplasmic reticulum proteome in cancer. J Proteome Res 7(8):3364–3372

    Article  CAS  PubMed  Google Scholar 

  • Silverman-Gavrila LB, Lew RR (2002) An IP3-activated Ca2+ channel regulates fungal tip growth. J Cell Sci 115.(Pt 24:5013–5025

    Article  CAS  PubMed  Google Scholar 

  • Song J, Liu X, Zhai P, Huang J, Lu L (2016) A putative mitochondrial calcium uniporter in A. fumigatus contributes to mitochondrial Ca(2+) homeostasis and stress responses. Fungal Genet Biol 94:15–22

    Article  CAS  PubMed  Google Scholar 

  • Squizani ED, Oliveira NK, Reuwsaat JCV, Marques BM, Lopes W, Gerber AL, de Vasconcelos ATR, Lev S, Djordjevic JT, Schrank A, Vainstein MH, Staats CC, Kmetzsch L (2018) Cryptococcal dissemination to the central nervous system requires the vacuolar calcium transporter Pmc1. Cell Microbiol 20(2):e12803

    Article  CAS  Google Scholar 

  • Stemmer PM, Klee CB (1994) Dual calcium ion regulation of calcineurin by calmodulin and calcineurin B. Biochemistry 33(22):6859–6866

    Article  CAS  PubMed  Google Scholar 

  • Suda Y, Nakano A (2012) The yeast Golgi apparatus. Traffic 13(4):505–510

    Article  CAS  PubMed  Google Scholar 

  • Takeuchi A, Kim B, Matsuoka S (2015) The destiny of Ca released by mitochondria. J Physiol Sci 65:11–24

    Article  CAS  PubMed  Google Scholar 

  • Tanida I, Hasegawa A, Iida H, Ohya Y, Anraku Y (1995) Cooperation of calcineurin and vacuolar H(+)-ATPase in intracellular Ca2+ homeostasis of yeast cells. J Biol Chem 270(17):10113–10119

    Article  CAS  PubMed  Google Scholar 

  • Ton VK, Mandal D, Vahadji C, Rao R (2002) Functional expression in yeast of the human secretory pathway Ca(2+), Mn(2+)-ATPase defective in Hailey-Hailey disease. J Biol Chem 277(8):6422–6427

    Article  CAS  PubMed  Google Scholar 

  • Tsai MF, Jiang D, Zhao L, Clapham D, Miller C (2014) Functional reconstitution of the mitochondrial Ca2+/H+ antiporter Letm1. J Gen Physiol 143(1):67–73

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tuteja N, Mahajan S (2007) Calcium signaling network in plants: an overview. Plant Signal Behav 2(2):79–85

    Article  PubMed  PubMed Central  Google Scholar 

  • Ueda Y, Ishitsuka R, Hullin-Matsuda F, Kobayashi T (2014) Regulation of the transbilayer movement of diacylglycerol in the plasma membrane. Biochimie 107:43–50

    Article  CAS  PubMed  Google Scholar 

  • Uemura S, Kihara A, Iwaki S, Inokuchi J, Igarashi Y (2007) Regulation of the transport and protein levels of the inositol phosphorylceramide mannosyltransferases Csg1 and Csh1 by the Ca2+-binding protein Csg2. J Biol Chem 282(12):8613–8621

    Article  CAS  PubMed  Google Scholar 

  • Van Baelen K, Vanoevelen J, Missiaen L, Raeymaekers L, Wuytack F (2001) The Golgi PMR1 P-type ATPase of Caenorhabditis elegans. Identification of the gene and demonstration of calcium and manganese transport. J Biol Chem 276(14):10683–10691

    Article  PubMed  Google Scholar 

  • Van Baelen K, Dode L, Vanoevelen J, Callewaert G, De Smedt H, Missiaen L, Parys JB, Raeymaekers L, Wuytack F (2004) The Ca2+/Mn2+ pumps in the Golgi apparatus. Biochim Biophys Acta 1742(1–3):103–112

    Article  PubMed  CAS  Google Scholar 

  • von Blume J, Alleaume AM, Cantero-Recasens G, Curwin A, Carreras-Sureda A, Zimmermann T, van Galen J, Wakana Y, Valverde MA, Malhotra V (2011) ADF/cofilin regulates secretory cargo sorting at the TGN via the Ca2+ ATPase SPCA1. Dev Cell 20(5):652–662

    Article  CAS  Google Scholar 

  • Wada Y, Anraku Y (1994) Chemiosmotic coupling of ion transport in the yeast vacuole: its role in acidification inside organelles. J Bioenerg Biomembr 26(6):631–637

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Cao J, Liu X, Hu H, Shi J, Zhang S, Keller NP, Lu L (2012) Putative calcium channels CchA and MidA play the important roles in conidiation, hyphal polarity and cell wall components in Aspergillus nidulans. PLoS One 7(10):e46564

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • White PJ, Broadley MR (2003) Calcium in plants. Ann Bot 92(4):487–511

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wuytack F, Raeymaekers L, Missiaen L (2003) PMR1/SPCA Ca2+ pumps and the role of the Golgi apparatus as a Ca2+ store. Pflugers Arch 446(2):148–153

    Article  CAS  PubMed  Google Scholar 

  • Yagodin S, Pivovarova NB, Andrews SB, Sattelle DB (1999) Functional characterization of thapsigargin and agonist-insensitive acidic Ca2+ stores in Drosophila melanogaster S2 cell lines. Cell Calcium 25(6):429–438

    Article  CAS  PubMed  Google Scholar 

  • Yang M, Brand A, Srikantha T, Daniels KJ, Soll DR, Gow NA (2011) Fig1 facilitates calcium influx and localizes to membranes destined to undergo fusion during mating in Candida albicans. Eukaryot Cell 10(3):435–444

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu Q, Wang F, Zhao Q, Chen J, Zhang B, Ding X, Wang H, Yang B, Lu G, Li M (2014) A novel role of the vacuolar calcium channel Yvc1 in stress response, morphogenesis and pathogenicity of Candida albicans. Int J Med Microbiol 304(3–4):339–350

    Article  CAS  PubMed  Google Scholar 

  • Zhang S, Zheng H, Long N, Carbo N, Chen P, Aguilar PS, Lu L (2014) FigA, a putative homolog of low-affinity calcium system member Fig1 in Saccharomyces cerevisiae, is involved in growth and asexual and sexual development in Aspergillus nidulans. Eukaryot Cell 13(2):295–303

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhang Y, Zheng Q, Sun C, Song J, Gao L, Zhang S, Munoz A, Read ND, Lu L (2016) Palmitoylation of the cysteine residue in the DHHC motif of a palmitoyl transferase mediates Ca2+ homeostasis in Aspergillus. PLoS Genet 12(4):e1005977

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhou XL, Batiza AF, Loukin SH, Palmer CP, Kung C, Saimi Y (2003) The transient receptor potential channel on the yeast vacuole is mechanosensitive. Proc Natl Acad Sci USA 100(12):7105–7110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Zhang, Y., Jiang, H., Lu, L. (2019). Calcium Cation Cycling and Signaling Pathways in Fungi. In: Hoffmeister, D., Gressler, M. (eds) Biology of the Fungal Cell. The Mycota, vol 8. Springer, Cham. https://doi.org/10.1007/978-3-030-05448-9_7

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