Advertisement

The CRaZy Calcium Cycle

  • Eduardo A. EspesoEmail author
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 892)

Abstract

Calcium is an essential cation for a cell. This cation participates in the regulation of numerous processes in either prokaryotes or eukaryotes, from bacteria to humans. Saccharomyces cerevisiae has served as a model organism to understand calcium homeostasis and calcium-dependent signaling in fungi. In this chapter it will be reviewed known and predicted transport mechanisms that mediate calcium homeostasis in the yeast. How and when calcium enters the cell, how and where it is stored, when is reutilized, and finally secreted to the environment to close the cycle. As a second messenger, maintenance of a controlled free intracellular calcium concentration is important for mediating transcriptional regulation. Many environmental stimuli modify the concentration of cytoplasmic free calcium generating the “calcium signal”. This is sensed and transduced through the calmodulin/calcineurin pathway to a transcription factor, named calcineurin-responsive zinc finger, CRZ, also known as “crazy”, to mediate transcriptional regulation of a large number of genes of diverse pathways including a negative feedback regulation of the calcium homeostasis system.

Keywords

Crz1 Calcineurin signaling Calcium pump Calcium channel P-type ATPase Magnesium homeostasis 

Notes

Acknowledgements

Work at the laboratory of Dr. Espeso at the Centro de Investigaciones Biológicas (CIB), from the Spanish Research Council, CSIC, is supported by the Spanish Ministerio de Economía y Competitividad through grant BFU2012-33142.

Bibliography

  1. Adams AE, Johnson DI, Longnecker RM, Sloat BF, Pringle JR (1990) CDC42 and CDC43, two additional genes involved in budding and the establishment of cell polarity in the yeast Saccharomyces cerevisiae. J Cell Biol 111:131–142CrossRefPubMedGoogle Scholar
  2. Aiello DP, Fu L, Miseta A, Bedwell DM (2002) Intracellular glucose 1-phosphate and glucose 6-phosphate levels modulate Ca2+ homeostasis in Saccharomyces cerevisiae. J Biol Chem 277:45751–45758CrossRefPubMedGoogle Scholar
  3. Anraku Y, Ohya Y, Iida H (1991) Cell cycle control by calcium and calmodulin in Saccharomyces cerevisiae. Biochim Biophys Acta 1093:169–177CrossRefPubMedGoogle Scholar
  4. 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 3:633–654CrossRefPubMedPubMedCentralGoogle Scholar
  5. Beeler T, Gable K, Zhao C, Dunn T (1994) A novel protein, CSG2p, is required for Ca2+ regulation in Saccharomyces cerevisiae. J Biol Chem 269:7279–7284PubMedGoogle Scholar
  6. Beeler TJ, Fu D, Rivera J, Monaghan E, Gable K, Dunn TM (1997) SUR1 (CSG1/BCL21), a gene necessary for growth of Saccharomyces cerevisiae in the presence of high Ca2+ concentrations at 37 degrees C, is required for mannosylation of inositolphosphorylceramide. Mol Gen Genet 255:570–579CrossRefPubMedGoogle Scholar
  7. Birchwood CJ, Saba JD, Dickson RC, Cunningham KW (2001) Calcium influx and signaling in yeast stimulated by intracellular sphingosine 1-phosphate accumulation. J Biol Chem 276:11712–11718CrossRefPubMedGoogle Scholar
  8. Bonilla M, Cunningham KW (2003) Mitogen-activated protein kinase stimulation of Ca(2+) signaling is required for survival of endoplasmic reticulum stress in yeast. Mol Biol Cell 14:4296–4305CrossRefPubMedPubMedCentralGoogle Scholar
  9. Bonilla M, Nastase KK, Cunningham KW (2002) Essential role of calcineurin in response to endoplasmic reticulum stress. EMBO J 21:2343–2353CrossRefPubMedPubMedCentralGoogle Scholar
  10. Borrelly G, Boyer JC, Touraine B, Szponarski W, Rambier M, Gibrat R (2001) The yeast mutant vps5Delta affected in the recycling of Golgi membrane proteins displays an enhanced vacuolar Mg2+/H+ exchange activity. Proc Natl Acad Sci U S A 98:9660–9665CrossRefPubMedPubMedCentralGoogle Scholar
  11. Boustany LM, Cyert MS (2002) Calcineurin-dependent regulation of Crz1p nuclear export requires Msn5p and a conserved calcineurin docking site. Genes Dev 16:608–619CrossRefPubMedPubMedCentralGoogle Scholar
  12. Cagnac O, Leterrier M, Yeager M, Blumwald E (2007) Identification and characterization of Vnx1p, a novel type of vacuolar monovalent cation/H+ antiporter of Saccharomyces cerevisiae. J Biol Chem 282:24284–24293CrossRefPubMedGoogle Scholar
  13. Cagnac O, Aranda-Sicilia MN, Leterrier M, Rodriguez-Rosales MP, Venema K (2010) Vacuolar cation/H+ antiporters of Saccharomyces cerevisiae. J Biol Chem 285:33914–33922CrossRefPubMedPubMedCentralGoogle Scholar
  14. Catterall WA (2000) Structure and regulation of voltage-gated Ca2+ channels. Annu Rev Cell Dev Biol 16:521–555CrossRefPubMedGoogle Scholar
  15. Connolly S, Kingsbury T (2012) Regulatory subunit myristoylation antagonizes calcineurin phosphatase activation in yeast. J Biol Chem 287:39361–39368CrossRefPubMedPubMedCentralGoogle Scholar
  16. Courchesne WE, Ozturk S (2003) Amiodarone induces a caffeine-inhibited, MID1-dependent rise in free cytoplasmic calcium in Saccharomyces cerevisiae. Mol Microbiol 47:223–234CrossRefPubMedGoogle Scholar
  17. Cronin SR, Rao R, Hampton RY (2002) Cod1p/Spf1p is a P-type ATPase involved in ER function and Ca2+ homeostasis. J Cell Biol 157:1017–1028CrossRefPubMedPubMedCentralGoogle Scholar
  18. Cui J, Kaandorp JA (2006) Mathematical modeling of calcium homeostasis in yeast cells. Cell Calcium 39:337–348CrossRefPubMedGoogle Scholar
  19. Cui J, Kaandorp JA, Ositelu OO, Beaudry V, Knight A, Nanfack YF, Cunningham KW (2009a) Simulating calcium influx and free calcium concentrations in yeast. Cell Calcium 45:123–132CrossRefPubMedGoogle Scholar
  20. Cui J, Kaandorp JA, Sloot PM, Lloyd CM, Filatov MV (2009b) Calcium homeostasis and signaling in yeast cells and cardiac myocytes. FEMS Yeast Res 9:1137–1147CrossRefPubMedGoogle Scholar
  21. Culotta VC, Yang M, Hall MD (2005) Manganese transport and trafficking: lessons learned from Saccharomyces cerevisiae. Eukaryot Cell 4:1159–1165CrossRefPubMedPubMedCentralGoogle Scholar
  22. Cunningham KW (2005) Calcium signaling networks in yeast. In: Putney JW (ed) Calcium signaling, 2nd edn. Taylor & Francis Group/CRC Press, Florida, pp 107–201Google Scholar
  23. Cunningham KW, Fink GR (1994a) Ca2+ transport in Saccharomyces cerevisiae. J Exp Biol 196:157–166Google Scholar
  24. Cunningham KW, Fink GR (1994b) Calcineurin-dependent growth control in Saccharomyces cerevisiae mutants lacking PMC1, a homolog of plasma membrane Ca2+ ATPases. J Cell Biol 124:351–363CrossRefPubMedGoogle Scholar
  25. Cunningham KW, Fink GR (1996) Calcineurin inhibits VCX1-dependent H+/Ca2+ exchange and induces Ca2+ ATPases in Saccharomyces cerevisiae. Mol Cell Biol 16:2226–2237CrossRefPubMedPubMedCentralGoogle Scholar
  26. Cyert MS (2001) Genetic analysis of calmodulin and its targets in Saccharomyces cerevisiae. Annu Rev Genet 35:647–672CrossRefPubMedGoogle Scholar
  27. Cyert MS (2003) Calcineurin signaling in Saccharomyces cerevisiae: how yeast go crazy in response to stress. Biochem Biophys Res Commun 311:1143–1150CrossRefPubMedGoogle Scholar
  28. Cyert MS, Thorner J (1992) Regulatory subunit (CNB1 gene product) of yeast Ca2+/calmodulin-dependent phosphoprotein phosphatases is required for adaptation to pheromone. Mol Cell Biol 12:3460–3469CrossRefPubMedPubMedCentralGoogle Scholar
  29. Cyert MS, Kunisawa R, Kaim D, Thorner J (1991) Yeast has homologs (CNA1 and CNA2 gene products) of mammalian calcineurin, a calmodulin-regulated phosphoprotein phosphatase. Proc Natl Acad Sci U S A 88:7376–7380CrossRefPubMedPubMedCentralGoogle Scholar
  30. Dalal CK, Cai L, Lin Y, Rahbar K, Elowitz MB (2014) Pulsatile dynamics in the yeast proteome. Curr Biol 24:2189–2194CrossRefPubMedPubMedCentralGoogle Scholar
  31. Davis TN, Urdea MS, Masiarz FR, Thorner J (1986) Isolation of the yeast calmodulin gene: calmodulin is an essential protein. Cell 47:423–431CrossRefPubMedGoogle Scholar
  32. Demaegd D, Foulquier F, Colinet AS, Gremillon L, Legrand D, Mariot P, Peiter E, Van SE, Matthijs G, Morsomme P (2013) Newly characterized Golgi-localized family of proteins is involved in calcium and pH homeostasis in yeast and human cells. Proc Natl Acad Sci U S A 110:6859–6864CrossRefPubMedPubMedCentralGoogle Scholar
  33. Denis V, Cyert MS (2002) Internal Ca(2+) release in yeast is triggered by hypertonic shock and mediated by a TRP channel homologue. J Cell Biol 156:29–34CrossRefPubMedPubMedCentralGoogle Scholar
  34. Desfarges L, Durrens P, Juguelin H, Cassagne C, Bonneu M, Aigle M (1993) Yeast mutants affected in viability upon starvation have a modified phospholipid composition. Yeast 9:267–277CrossRefPubMedGoogle Scholar
  35. Dickson RC, Lester RL (2002) Sphingolipid functions in Saccharomyces cerevisiae. Biochim Biophys Acta 1583:13–25CrossRefPubMedGoogle Scholar
  36. Dunn T, Gable K, Beeler T (1994) Regulation of cellular Ca2+ by yeast vacuoles. J Biol Chem 269:7273–7278PubMedGoogle Scholar
  37. 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 9:1149–1162CrossRefPubMedPubMedCentralGoogle Scholar
  38. Fu D, Beeler T, Dunn T (1994) Sequence, mapping and disruption of CCC1, a gene that cross-complements the Ca(2+)-sensitive phenotype of csg1 mutants. Yeast 10:515–521CrossRefPubMedGoogle Scholar
  39. Grabarek Z (2011) Insights into modulation of calcium signaling by magnesium in calmodulin, troponin C and related EF-hand proteins. Biochim Biophys Acta 1813:913–921CrossRefPubMedPubMedCentralGoogle Scholar
  40. Graschopf A, Stadler JA, Hoellerer MK, Eder S, Sieghardt M, Kohlwein SD, Schweyen RJ (2001) The yeast plasma membrane protein Alr1 controls Mg2+ homeostasis and is subject to Mg2+-dependent control of its synthesis and degradation. J Biol Chem 276:16216–16222CrossRefPubMedGoogle Scholar
  41. Halachmi D, Eilam Y (1996) Elevated cytosolic free Ca2+ concentrations and massive Ca2+ accumulation within vacuoles, in yeast mutant lacking PMR1, a homolog of Ca2+-ATPase. FEBS Lett 392:194–200CrossRefPubMedGoogle Scholar
  42. Hilioti Z, Gallagher DA, Low-Nam ST, Ramaswamy P, Gajer P, Kingsbury TJ, Birchwood CJ, Levchenko A, Cunningham KW (2004) GSK-3 kinases enhance calcineurin signaling by phosphorylation of RCNs. Genes Dev 18:35–47CrossRefPubMedPubMedCentralGoogle Scholar
  43. Hoekstra MF, Liskay RM, Ou AC, DeMaggio AJ, Burbee DG, Heffron F (1991) HRR25, a putative protein kinase from budding yeast: association with repair of damaged DNA. Science 253:1031–1034CrossRefPubMedGoogle Scholar
  44. Hu Z, Killion PJ, Iyer VR (2007) Genetic reconstruction of a functional transcriptional regulatory network. Nat Genet 39:683–687CrossRefPubMedGoogle Scholar
  45. Iida H, Yagawa Y, Anraku Y (1990) Essential role for induced Ca2+ influx followed by [Ca2+]i rise in maintaining viability of yeast cells late in the mating pheromone response pathway. A study of [Ca2+]i in single Saccharomyces cerevisiae cells with imaging of fura-2. J Biol Chem 265:13391–13399PubMedGoogle Scholar
  46. 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 14:8259–8271CrossRefPubMedPubMedCentralGoogle Scholar
  47. Kafadar KA, Zhu H, Snyder M, Cyert MS (2003) Negative regulation of calcineurin signaling by Hrr25p, a yeast homolog of casein kinase I. Genes Dev 17:2698–2708CrossRefPubMedPubMedCentralGoogle Scholar
  48. 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 285:882–886CrossRefPubMedGoogle Scholar
  49. Kingsbury TJ, Cunningham KW (2000) A conserved family of calcineurin regulators. Genes Dev 14:1595–1604PubMedPubMedCentralGoogle Scholar
  50. Lapinskas PJ, Lin SJ, Culotta VC (1996) The role of the Saccharomyces cerevisiae CCC1 gene in the homeostasis of manganese ions. Mol Microbiol 21:519–528CrossRefPubMedGoogle Scholar
  51. 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 20:6686–6694CrossRefPubMedPubMedCentralGoogle Scholar
  52. Macdiarmid CW, Gardner RC (1998) Overexpression of the Saccharomyces cerevisiae magnesium transport system confers resistance to aluminum ion. J Biol Chem 273:1727–1732CrossRefPubMedGoogle Scholar
  53. Mandal D, Woolf TB, Rao R (2000) Manganese selectivity of pmr1, the yeast secretory pathway ion pump, is defined by residue gln783 in transmembrane segment 6. Residue Asp778 is essential for cation transport. J Biol Chem 275:23933–23938CrossRefPubMedGoogle Scholar
  54. 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 454:181–186CrossRefPubMedGoogle Scholar
  55. 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 11:3445–3458CrossRefPubMedPubMedCentralGoogle Scholar
  56. Matsumoto TK, Ellsmore AJ, Cessna SG, Low PS, Pardo JM, Bressan RA, Hasegawa PM (2002) An osmotically induced cytosolic Ca2+ transient activates calcineurin signaling to mediate ion homeostasis and salt tolerance of Saccharomyces cerevisiae. J Biol Chem 277:33075–33080CrossRefPubMedGoogle Scholar
  57. Mehlgarten C, Schaffrath R (2003) Mutant casein kinase I (Hrr25p/Kti14p) abrogates the G1 cell cycle arrest induced by Kluyveromyces lactiszymocin in budding yeast. Mol Genet Genomics 269:188–196PubMedGoogle Scholar
  58. Mehta S, Li H, Hogan PG, Cunningham KW (2009) Domain architecture of the regulators of calcineurin (RCANs) and identification of a divergent RCAN in yeast. Mol Cell Biol 29:2777–2793CrossRefPubMedPubMedCentralGoogle Scholar
  59. Mendizabal I, Pascual-Ahuir A, Serrano R, de Larrinoa IF (2001) Promoter sequences regulated by the calcineurin-activated transcription factor Crz1 in the yeast ENA1 gene. Mol Genet Genomics 265:801–811CrossRefPubMedGoogle Scholar
  60. Miseta A, Kellermayer R, Aiello DP, Fu L, Bedwell DM (1999) The vacuolar Ca2+/H+ exchanger Vcx1p/Hum1p tightly controls cytosolic Ca2+ levels in S. cerevisiae. FEBS Lett 451:132–136CrossRefPubMedGoogle Scholar
  61. O’Donnell AF, Huang L, Thorner J, Cyert MS (2013) A calcineurin-dependent switch controls the trafficking function of alpha-arrestin Aly1/Art6. J Biol Chem 288:24063–24080CrossRefPubMedPubMedCentralGoogle Scholar
  62. Ohya Y, Ohsumi Y, Anraku Y (1984) Genetic study of the role of calcium ions in the cell division cycle of Saccharomyces cerevisiae: a calcium-dependent mutant and its trifluoperazine-dependent pseudorevertants. Mol Gen Genet 193:389–394CrossRefPubMedGoogle Scholar
  63. Ohya Y, Ohsumi Y, Anraku Y (1986) Isolation and characterization of Ca2+-sensitive mutants of Saccharomyces cerevisiae. J Gen Microbiol 132:979–988PubMedGoogle Scholar
  64. Ozeki-Miyawaki C, Moriya Y, Tatsumi H, Iida H, Sokabe M (2005) Identification of functional domains of Mid1, a stretch-activated channel component, necessary for localization to the plasma membrane and Ca2+ permeation. Exp Cell Res 311:84–95CrossRefPubMedGoogle Scholar
  65. Paidhungat M, Garrett S (1997) A homolog of mammalian, voltage-gated calcium channels mediates yeast pheromone-stimulated Ca2+ uptake and exacerbates the cdc1(Ts) growth defect. Mol Cell Biol 17:6339–6347CrossRefPubMedPubMedCentralGoogle Scholar
  66. 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 U S A 98:7801–7805CrossRefPubMedPubMedCentralGoogle Scholar
  67. Peiter E, Fischer M, Sidaway K, Roberts SK, Sanders D (2005) The Saccharomyces cerevisiae Ca2+ channel Cch1pMid1p is essential for tolerance to cold stress and iron toxicity. FEBS Lett 579:5697–5703CrossRefPubMedGoogle Scholar
  68. Pinton P, Pozzan T, Rizzuto R (1998) The Golgi apparatus is an inositol 1,4,5-trisphosphate-sensitive Ca2+ store, with functional properties distinct from those of the endoplasmic reticulum. EMBO J 17:5298–5308CrossRefPubMedPubMedCentralGoogle Scholar
  69. Pisat NP, Pandey A, Macdiarmid CW (2009) MNR2 regulates intracellular magnesium storage in Saccharomyces cerevisiae. Genetics 183:873–884CrossRefPubMedPubMedCentralGoogle Scholar
  70. Polizotto RS, Cyert MS (2001) Calcineurin-dependent nuclear import of the transcription factor Crz1p requires Nmd5p. J Cell Biol 154:951–960CrossRefPubMedPubMedCentralGoogle Scholar
  71. Pozos TC, Sekler I, Cyert MS (1996) The product of HUM1, a novel yeast gene, is required for vacuolar Ca2+/H+ exchange and is related to mammalian Na+/Ca2+ exchangers. Mol Cell Biol 16:3730–3741CrossRefPubMedPubMedCentralGoogle Scholar
  72. Prezant TR, Chaltraw WE Jr, Fischel-Ghodsian N (1996) Identification of an overexpressed yeast gene which prevents aminoglycoside toxicity. Microbiology 142(Pt 12):3407–3414CrossRefPubMedGoogle Scholar
  73. Ripmaster TL, Vaughn GP, Woolford JL Jr (1993) DRS1 to DRS7, novel genes required for ribosome assembly and function in Saccharomyces cerevisiae. Mol Cell Biol 13:7901–7912CrossRefPubMedPubMedCentralGoogle Scholar
  74. Rodriguez A, Roy J, Martinez-Martinez S, Lopez-Maderuelo MD, Nino-Moreno P, Orti L, Pantoja-Uceda D, Pineda-Lucena A, Cyert MS, Redondo JM (2009) A conserved docking surface on calcineurin mediates interaction with substrates and immunosuppressants. Mol Cell 33:616–626CrossRefPubMedPubMedCentralGoogle Scholar
  75. Roy J, Li H, Hogan PG, Cyert MS (2007) A conserved docking site modulates substrate affinity for calcineurin, signaling output, and in vivo function. Mol Cell 25:889–901CrossRefPubMedPubMedCentralGoogle Scholar
  76. 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 58:133–145CrossRefPubMedGoogle Scholar
  77. Schlingmann KP, Gudermann T (2005) A critical role of TRPM channel-kinase for human magnesium transport. J Physiol 566:301–308CrossRefPubMedPubMedCentralGoogle Scholar
  78. Schmitz C, Perraud AL, Johnson CO, Inabe K, Smith MK, Penner R, Kurosaki T, Fleig A, Scharenberg AM (2003) Regulation of vertebrate cellular Mg2+ homeostasis by TRPM7. Cell 114:191–200CrossRefPubMedGoogle Scholar
  79. Shaker JL, Deftos L (2000) Calcium and phosphate homeostasis (De Groot LJ, Beck-Peccoz P, Chrousos G, Dungan K, Grossman A, Hershman JM, Koch C, McLachlan R, New M, Rebar R, Singer F, Vinik A, Weickert MO, eds). MDText.com, Inc., South Dartmouth. PMID: 25905252Google Scholar
  80. Sopko R, Huang D, Preston N, Chua G, Papp B, Kafadar K, Snyder M, Oliver SG, Cyert M, Hughes TR, Boone C, Andrews B (2006) Mapping pathways and phenotypes by systematic gene overexpression. Mol Cell 21:319–330CrossRefPubMedGoogle Scholar
  81. Sorin A, Rosas G, Rao R (1997) PMR1, a Ca2+-ATPase in yeast Golgi, has properties distinct from sarco/endoplasmic reticulum and plasma membrane calcium pumps. J Biol Chem 272:9895–9901CrossRefPubMedGoogle Scholar
  82. Starovasnik MA, Davis TN, Klevit RE (1993) Similarities and differences between yeast and vertebrate calmodulin: an examination of the calcium-binding and structural properties of calmodulin from the yeast Saccharomyces cerevisiae. Biochemistry 32:3261–3270CrossRefPubMedGoogle Scholar
  83. Stathopoulos AM, Cyert MS (1997) Calcineurin acts through the CRZ1/TCN1-encoded transcription factor to regulate gene expression in yeast. Genes Dev 11:3432–3444CrossRefPubMedPubMedCentralGoogle Scholar
  84. Stathopoulos-Gerontides A, Guo JJ, Cyert MS (1999) Yeast calcineurin regulates nuclear localization of the Crz1p transcription factor through dephosphorylation. Genes Dev 13:798–803CrossRefPubMedPubMedCentralGoogle Scholar
  85. Strayle J, Pozzan T, Rudolph HK (1999) Steady-state free Ca(2+) in the yeast endoplasmic reticulum reaches only 10 microM and is mainly controlled by the secretory pathway pump pmr1. EMBO J 18:4733–4743CrossRefPubMedPubMedCentralGoogle Scholar
  86. Takita Y, Engstrom L, Ungermann C, Cunningham KW (2001) Inhibition of the Ca(2+)-ATPase Pmc1p by the v-SNARE protein Nyv1p. J Biol Chem 276:6200–6206CrossRefPubMedGoogle Scholar
  87. Tanida I, Takita Y, Hasegawa A, Ohya Y, Anraku Y (1996) Yeast Cls2p/Csg2p localized on the endoplasmic reticulum membrane regulates a non-exchangeable intracellular Ca2+ pool cooperatively with calcineurin. FEBS Lett 379:38–42CrossRefPubMedGoogle Scholar
  88. Tomar P, Sinha H (2014) Conservation of PHO pathway in ascomycetes and the role of Pho84. J Biosci 39:525–536CrossRefPubMedGoogle Scholar
  89. Viladevall L, Serrano R, Ruiz A, Domenech G, Giraldo J, Barcelo A, Arino J (2004) Characterization of the calcium-mediated response to alkaline stress in Saccharomyces cerevisiae. J Biol Chem 279:43614–43624CrossRefPubMedGoogle Scholar
  90. Wachek M, Aichinger MC, Stadler JA, Schweyen RJ, Graschopf A (2006) Oligomerization of the Mg2+-transport proteins Alr1p and Alr2p in yeast plasma membrane. FEBS J 273:4236–4249CrossRefPubMedGoogle Scholar
  91. Wei Y, Marchi V, Wang R, Rao R (1999) An N-terminal EF hand-like motif modulates ion transport by Pmr1, the yeast Golgi Ca(2+)/Mn(2+)-ATPase. Biochemistry 38:14534–14541CrossRefPubMedGoogle Scholar
  92. Wiesenberger G, Steinleitner K, Malli R, Graier WF, Vormann J, Schweyen RJ, Stadler JA (2007) Mg2+ deprivation elicits rapid Ca2+ uptake and activates Ca2+/calcineurin signaling in Saccharomyces cerevisiae. Eukaryot Cell 6:592–599CrossRefPubMedPubMedCentralGoogle Scholar
  93. Yoshimura H, Tada T, Iida H (2004) Subcellular localization and oligomeric structure of the yeast putative stretch-activated Ca2+ channel component Mid1. Exp Cell Res 293:185–195CrossRefPubMedGoogle Scholar
  94. Zhou Y, Meraner P, Kwon HT, Machnes D, Oh-hora M, Zimmer J, Huang Y, Stura A, Rao A, Hogan PG (2010a) STIM1 gates the store-operated calcium channel ORAI1 in vitro. Nat Struct Mol Biol 17:112–116CrossRefPubMedGoogle Scholar
  95. Zhou Y, Ramachandran S, Oh-hora M, Rao A, Hogan PG (2010b) Pore architecture of the ORAI1 store-operated calcium channel. Proc Natl Acad Sci U S A 107:4896–4901CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Department of Cellular and Molecular BiologyCentro de Investigaciones Biológicas, CSICMadridSpain

Personalised recommendations