1887

Abstract

The metabolism of inositol 1,4,5-trisphosphate [Ins(1,4,5)P] was examined in yeast cells and germ tubes of Methods have been developed for analysis of the two key metabolic enzymes, Ins(1,4,5)P kinase and phosphatase. ATP-dependent Ins(1,4,5)P kinase activity was detected predominantly in the soluble fraction of cell extracts and exhibited a of approximately 9 μM. The apparent of Ins(1,4,5)P phosphatase for Ins(1,4,5)P was approximately 480 μM. The slow rate of dephosphorylation of Ins(1,4,5)P to inositol bisphosphate suggests a lower importance of the phosphatase within cells compared to the kinase. Since both yeast cells and germ tubes of rapidly phosphorylated Ins(1,4,5)P to inositol tetrakisphosphate and inositol penta/hexakisphosphate, it is suggested that Ins(1,4,5)P has an important role as a precursor for production of these compounds. A sustained increase in cellular Ins(1,4,5)P levels was observed during germ tube formation and, prior to the onset of germination between 1 and 2 h incubation, the Ins(1,4,5)P content increased up to eightfold. Transien increases in the level of Ins(1,4,5)P were also observed during yeast-like growth of The possible role and relative importance of Ins(1,4,5)P as a precursor for inositol polyphosphates and in signal transduction involving Ca release from internal stores is discussed.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-143-2-437
1997-02-01
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/micro/143/2/mic-143-2-437.html?itemId=/content/journal/micro/10.1099/00221287-143-2-437&mimeType=html&fmt=ahah

References

  1. Anraku Y., Ohya Y., Iida H. 1991; Cell cycle control by calcium and calmodulin in Saccharomyces cerevisiae.. Biochim Biophys Acta 1093:169–177
    [Google Scholar]
  2. Bedell G., Werth A., Soli D.R. 1980; The regulation of nuclear migration and division during synchronous bud formation in released stationary phase cultures of the yeast Candida albicans.. Exp Cell Res 127:103–113
    [Google Scholar]
  3. Belde P.J.M., Vossen J.H., Borst-Pauwels G.W.F.H., Theuvenet A.P.R. 1993; Inositol 1,4,5-trisphosphate releases? Ca2+ from vacuolar membrane-vesicles of Saccharomyces cerevisiae.. FEBS Lett 323:113–118
    [Google Scholar]
  4. Berridge M.J. 1987; Inositol trisphosphate and diacylglycerol: two interacting second messengers.. Annu Rev Biochem 56:159–193
    [Google Scholar]
  5. Berridge M.J. 1993; Inositol trisphosphate and calcium signalling.. Nature 361:315–325
    [Google Scholar]
  6. Berridge M.J., Irvine R.F. 1989; Inositol phosphates and cell signalling.. Nature 341:197–205
    [Google Scholar]
  7. Bertl A., Slayman C.L. 1990; Cation-selective channels in the vacuolar membrane of Saccharomyces cerevisiae: dependence on Ca2+, redox state and voltage.. Proc Natl Acad Sci USA 877824–7828
    [Google Scholar]
  8. Bertl A., Slayman C.L. 1992; Complex modulation of cation channels in the tonoplast and plasma membrane of Saccharomyces cerevisiae - single-channel studies.. J Exp Biol 172:271–287
    [Google Scholar]
  9. Brummel M., Soll D.R. 1982; The temporal regulation of protein synthesis during synchronous bud or mycelium formation in the dimorphic yeast Candida albicans.. Dev Biol 89:211–224
    [Google Scholar]
  10. Brunton A.H., Gadd G.M. 1989; The effect of exogenously-supplied nucleosides and nucleotides and the involvement of adenosine 3̓ :5̓-cyclic monophosphate (cyclic AMP) in the yeast- mycelium transition of Ceratocystis (= Ophiostoma) ulmi.. FEMS Microbiol Lett 60:49–54
    [Google Scholar]
  11. Brunton A.H., Gadd G.M. 1991; Evidence for an inositol lipid signal pathway in the yeast-mycelium transition of Ophiostoma(Ceratocystis) ulmi, the Dutch elm disease fungus.. Mycol Res 95:484–491
    [Google Scholar]
  12. Buffo J., Herman M.A., Soll D.R. 1984; A characterization of pH regulated dimorphism in Candida albicans.. Mycopathologia 85:21–30
    [Google Scholar]
  13. Calvert C.M., Sanders D. 1995; Inositol trisphosphate-dependent and -independent Ca2+ mobilization pathways at the vacuolar membrane of Candida albicans.. J Biol Chem 270:7272–7280
    [Google Scholar]
  14. Cohen P., Hardie D.G. 1991; The actions of cyclic AMP on biosynthetic processes are mediated indirectly by cyclic AMP-dependent protein kinase.. Biochim Biophys Acta 1094:292–299
    [Google Scholar]
  15. Cooper L.A., Edwards S.W., Gadd G.M. 1985; Involvement of adenosine 3̓:5̓-cyclic monophosphate in the yeast-mycelium transition of Aureobasidium pullulans.. J Gen Microbiol 131:1589–1593
    [Google Scholar]
  16. Cornelius G., Nakashima H. 1987; Vacuoles play a decisive role in calcium homeostasis in Neurospora crassa.. J Gen Microbiol 133:2341–2347
    [Google Scholar]
  17. Cornelius G., Gebauer G., Techel D. 1989; Inositol trisphosphate induces calcium release from Neurospora crassa vacuoles.. Biochem Biophys Res Commun 162:852–856
    [Google Scholar]
  18. Crombie T., Gow N.A.R., Gooday G.W. 1990; Influence of applied electrical fields on yeast and hyphal growth of Candida albicans.. J Gen Microbiol 136:311–317
    [Google Scholar]
  19. Cunningham K.W., Fink G.R. 1994; Calcineurin-dependent growth control in Saccharomyces cerevisiae mutants lacking PCM1, a homolog of plasma membrane Ca2+ ATPases.. J Cell Biol 124:351–363
    [Google Scholar]
  20. Eilam Y., Lavi H., Grossowicz N. 1985; Cytoplasmic Ca2+homeostasis maintained by a vacuolar Ca2+ transport system in the yeast Saccharomyces cerevisiae.. J Gen Microbiol 31:623–629
    [Google Scholar]
  21. Estevez F., Pulford D., Stark M.J., Carter A.N., Downes C.P. 1994; Inositol trisphosphate metabolism in Saccharomyces cerevisiae; identification, purification and properties of inositol 1,4,5-trisphosphate 6-kinase.. Biochem J 302:709–716
    [Google Scholar]
  22. Flanagan C.A., Thorner J. 1992; Purification and characterization of a soluble phosphatidylinositol 4-kinase from the yeast Saccharomyces cerevisiae.. J Biol Chem 267:24117–24125
    [Google Scholar]
  23. Gadd G.M. 1995; Signal transduction in fungi.. In The Growing Fungus pp. 183–210 Gow N.A.R., Gadd G.M. Edited by London:: Chapman & Hall.;
    [Google Scholar]
  24. Gadd G.M., Brunton A.H. 1992; Calcium involvement in dimorphism of Ophiostoma ulmi, the Dutch elm disease fungus, and characterization of calcium uptake by yeast cells and germ tubes.. J Gen Microbiol 138:1561–1571
    [Google Scholar]
  25. Gancedo J.M., Mazon M.J., Eraso P. 1985; Biological roles of cyclic AMP: similarities and differences between organisms.. Trends Biochem Sci 10:210–212
    [Google Scholar]
  26. Gani D., Downes C.P., Batty I., Bramham J. 1993; Lithium and myo-inositol homeostasis.. Biochim Biophys Acta 1177:253–269
    [Google Scholar]
  27. Gibson D.M., Ullah A.B.J. 1990; Phytases and their action on phytic acid.. In Inositol Metabolism in Plants pp. 72–92 Morre D.J., Boss W.F., Loewus F.A. Edited by New York:: Wiley-Liss.;
    [Google Scholar]
  28. Goffeau A., Ghislain M., Navarre C., Purnelle B., Supply P. 1990; Novel transport ATPases in yeast.. Biochim Biophys Acta 1018:200–202
    [Google Scholar]
  29. Gow N.A.R. 1994; Growth and guidance of the fungal hypha.. Microbiology 140:3193–3205
    [Google Scholar]
  30. Gow N.A.R. 1995; Yeast-hyphal dimorphism.. In The Growing Fungus pp. 403–422 Gow N.A.R., Gadd G.M. Edited by London:: Chapman & Hall.;
    [Google Scholar]
  31. Graf E., Mahoney J.R., Bryant R.G., Eaton J.W. 1984; Iron-catalyzed hydroxyl radical formation - stringent requirement for free iron coordination site.. J Biol Chem 259:3620–3624
    [Google Scholar]
  32. Halachmi D., Ghislain M., Eilam Y. 1992; An intracellular ATP-dependent calcium pump within the yeast Schizosaccharomyces pombe, encoded by the gene cta3.. Eur J Biochem 207:1003–1008
    [Google Scholar]
  33. Hansbro P.M., Foster P.S., Liu C., Potter B.V.L., Denborough M.A. 1994; Kinetic analysis of novel inhibitors of inositol polyphosphate metabolism.. Biochem Biophys Res Commun 200:8–15
    [Google Scholar]
  34. Hanson B.A. 1991; The effects of lithium on the phosphoinositides and inositol phosphates of Neurospora crassa.. Exp Mycol 15:76–90
    [Google Scholar]
  35. Hawkins P.T., Stephens L.R., Piggot J.R. 1993; Analysis of inositol metabolites produced by Saccharomyces cerevisiae in response to glucose stimulation.. J Biol Chem 268:3374–3383
    [Google Scholar]
  36. Holmes A.R., Cannon R.D., Shepherd M.G. 1991; Effect of calcium ion uptake on Candida albicans morphology.. FEMS Microbiol Lett 77:187–194
    [Google Scholar]
  37. Hubbard M., Bradley M., Sullivan P., Shepherd M., Forrester I. 1982; Evidence for the occurrence of calmodulin in the yeasts Candida albicans and Saccharomyces cerevisiae.. FEBS Lett 137:85–88
    [Google Scholar]
  38. Iida H., Yagawa Y., Anraku Y. 1990; Essential role for induced Ca2+ influx followed by [Ca2+]1 rise in maintaining viability of yeast cells late in the mating pheromone response pathway.. J Biol Chem 265:13391–13399
    [Google Scholar]
  39. Irvine R.F. 1992; Inositol phosphates and Ca2+ entry: toward a proliferation or a simplification?. FASEB J 6:3085–3091
    [Google Scholar]
  40. Jackson S.L., Heath I.B. 1993; Roles of calcium ions in hyphal tip growth.. Microbiol Rev 57:367–382
    [Google Scholar]
  41. Kaibuchi K., Miyajima A., Arai K.-I., Matsumoto K. 1986; Possible involvement of RAS-encoded proteins in glucose-induced inositol phospholipid turnover in Saccharomyces cerevisiae.. Proc Natl Acad Sci USA 838172–8176
    [Google Scholar]
  42. Kamihara T., Omi K. 1989; Increase in cyclic AMP content with enhanced phosphatidylinositol turnover in the cells of Candida tropicalis during mycelial growth caused by ethanol.. Yeast 5:437–440
    [Google Scholar]
  43. Kato H., Uno I., Ishikawa T., Takenawa T. 1989; Activation of phosphatidylinositol kinase and phosphatidylinositol-4-phosphate kinase by cAMP in Saccharomyces cerevisiae.. J Biol Chem 264:3116–3121
    [Google Scholar]
  44. Kinney A.J., Carman G.M. 1990; Enzymes of phosphoinositide synthesis in secretory vesicles destined for the plasma membrane in Saccharomyces cerevisiae.. J Bacteriol 172:4115–4117
    [Google Scholar]
  45. Knight H., Trewavas A.J., Read N.D. 1993; Confocal microscopy of living fungal hyphae microinjected with Ca2+-sensitive fluorescent dyes.. Mycol Res 97:1505–1515
    [Google Scholar]
  46. Lakin-Thomas P.L. 1993a; Evidence against a direct role for inositol phosphate metabolism in the circadian oscillator and the blue-light signal transduction pathway in Neurospora crassa.. Biochem J 292:813–818
    [Google Scholar]
  47. Lakin-Thomas P.L. 1993b; Effects of inositol starvation on the levels of inositol phosphates and inositol lipids in Neurospora crassa.. Biochem J 292:805–811
    [Google Scholar]
  48. Lampe D., Liu C., Potter B.V.L. 1994; Synthesis of selective non-Ca2+-mobilizing inhibitors of D-myo-inositol 1,4,5-trisphosphate 5-phosphatase.. J Med Chem 37:907–912
    [Google Scholar]
  49. Lever M.C., Robertson B.E.M., Buchan A.D.B., Miller P.F.P., Gooday G.W., Gow N.A.R. 1994; pH and Ca2+ dependent galvanotropism of filamentous fungi: implications and mechanisms.. Mycol Res 98:301–306
    [Google Scholar]
  50. Liu Y., Ohki Y.A., Azuma Y., Tachikawa Y., Tsuchiya E., Fukui S., Miyakawa T. 1990; Calmodulin and calmodulin-binding proteins of Rhodosporidium toruloides, a basidiomycetous yeast.. J Gen Microbiol 136:131–136
    [Google Scholar]
  51. Menniti F.S., Oliver K.G., Putney J.W., Shears S.B. 1993; Inositol phosphates and cell signaling-new views of InsP5 and InsP6.. Trends Biochem Sci 18:53–56
    [Google Scholar]
  52. Miller A.J., Vogg G., Sanders D. 1990; Cytosolic calcium homeostasis in fungi: roles of plasma membrane transport and intracellular sequestration of calcium.. Proc Natl Acad Sci USA 879348–9352
    [Google Scholar]
  53. Morris A.J., Murray K., England P.J., Downes C.P., Michell R.H. 1988; Partial purification and some properties of rat-brain inositol 1,4,5-trisphosphate 3-kinase.. Biochem J 251:157–163
    [Google Scholar]
  54. Muthukumar G., Nickerson K.W. 1984; Ca(II)-calmodulin regulation of fungal dimorphism in Ceratocystis ulmi.. FEMS Microbiol Lett 159:390–392
    [Google Scholar]
  55. Muthukumar G., Luby M.T., Nickerson K.W. 1986; Calmodulin activity in yeast and mycelial phases of Ceratocystis ulmi.. FEMS Microbiol Lett 37:313–316
    [Google Scholar]
  56. Nishizuka Y. 1984; Protein kinases in signal transduction.. Trends Biochem Sci 4:163–166
    [Google Scholar]
  57. Nishizuka Y. 1992; Intracellular signalling by hydrolysis of phospholipids and activation of protein kinase C.. Science 258:607–614
    [Google Scholar]
  58. O̓Day D.H. 1990; Calcium as an intracellular messenger in eucaryotic microbes.. In Calcium as an Intracellular Messenger in Eucaryotic Microbes pp. 3–13 O̓Day D.H. Edited by Washington, DC:: American Society for Microbiology.;
    [Google Scholar]
  59. Ohsumi Y., Kitamoto K., Anraku Y. 1988; Changes induced in the permeability barrier of the yeast plasma membrane by cupric ion.. J Bacteriol 170:2676–2682
    [Google Scholar]
  60. Okorokov L.A. 1994; Several compartments of Saccharomyces cerevisiae are equipped with Ca2+-ATPases.. FEMS Microbiol Lett 117:311–318
    [Google Scholar]
  61. Omi K., Kamihara T. 1989; Accumulation of cAMP in the cells of Candida tropicalis at an early stage of ethanol-induced filamentous growth and its prevention by myo-inositol.. Biochem Biophys Res Commun 162:646–650
    [Google Scholar]
  62. Pall M.L. 1981; Adenosine 3̓:5̓-monophosphate in fungi.. Microbiol Rev 45:462–480
    [Google Scholar]
  63. Paranjape V.8cDatta. 1990; Role of calcium and calmodulin in morphogenesis of Candida albicans. . In Calcium as an Intracellular Messenger in Eucaryotic Microbes pp. 362–374 O̓Day D.H. Edited by Washington, DC:: American Society for Microbiology.;
    [Google Scholar]
  64. Paranjape V., Roy B.G., Datta A. 1990; Involvement of calcium, calmodulin and protein phosphorylation in morphogenesis of Candida albicans.. J Gen Microbiol 136:2149–2154
    [Google Scholar]
  65. Pitt D., Barnes J.C. 1993; Calcium homeostasis, signalling and protein phosphorylation during calcium-induced conidiation in Penicillium notatum.. J Gen Microbiol 139:3053–3063
    [Google Scholar]
  66. Pitt D., Kaile A. 1989; Transduction of the calcium signal with special reference to Ca2+ induced conidiation in Penicillium notatum. . In Biochemistry of Cell Walls and Membranes of Fungi pp. 283–298 Kuhn P.J., Trinci A.P.J., Jung M., Goosey M., Copping L.G. Edited by Berlin:: Springer-Verlag.;
    [Google Scholar]
  67. Prior S.L., Cundiffe B.W., Robson G.D., Trind A.P.J. 1993; Multiple isomers of phosphatidyl inositol monophosphate and inositol bis- and trisphosphates from filamentous fungi.. FEMS Microbiol Lett 110:147–152
    [Google Scholar]
  68. Prior S.L., Robson G.D., Trinci A.P.J. 1994; Phosphoinositide turnover does not mediate the effects of light or choline, or the relief of derepression of glucose metabolism in filamentous fungi.. Mycol Res 93:291–294
    [Google Scholar]
  69. Robson G.D., Wiebe M.G., Trinci A.P.J. 1991a; Involvement of Ca2+ in the regulation of hyphal extension and branching in Fusarium graminearum A3/5.. Exp Mycol 15:263–272
    [Google Scholar]
  70. Robson G.D., Wiebe M.G., Trinci A.P.J. 1991b; Exogenous cAMP and cGMP modulate branching in Fusarium graminearum.. J Gen Microbiol 137:963–969
    [Google Scholar]
  71. Rudolph H.K., Antebi A., Fink G.R., Buckley C.M., Dorman T.E., LeVitre J., Davidow L.S., Mao J.-I., Moir D.T. 1989; The yeast secretory pathway is perturbed by mutations in μMR1, a member of a Ca2+-ATPase family.. Cell 58:133–145
    [Google Scholar]
  72. Sabie F.T., Gadd G.M. 1989; Involvement of a Ca2+- calmodulin interaction in the yeast-mycelial transition of Candida albicans.. Mycopathologia 108:47–54
    [Google Scholar]
  73. Sabie F.T., Gadd G.M. 1992; Effect of nucleosides and nucleotides and the relationship between cellular adenosine 3̓: 5̓-cyclic monophosphate (cyclic AMP) and germ tube formation in Candida albicans.. Mycopathologia 119:147–156
    [Google Scholar]
  74. Schomerus C., Kuntzel H. 1992; CDC25-dependent induction of inositol 1,4,5-trisphosphate and diacylglycerol in Saccharomyces cerevisiae by nitrogen.. FEBS Lett 307:249–252
    [Google Scholar]
  75. Sherwood J., Gow N.A.R., Gooday G.W., Gregory G.W., Marshall D. 1992; Contact sensing in Candida albicans: a possible aid to epithelial penetration.. J Med Vet Mycol 30:461–469
    [Google Scholar]
  76. Sillence D.J., Downes C.P. 1992; Lithium treatment of affective disorders: effects of lithium on the inositol phospholipid and cyclic AMP signalling pathways.. Biochim Biophys Acta 1138:46–52
    [Google Scholar]
  77. Stewart E., Gow N.A.R., Bowen D.V. 1988; Cytoplasmic alkalinization during germ tube formation in Candida albicans.. J Gen Microbiol 134:1079–1087
    [Google Scholar]
  78. Trinci A.P.J., Robson G.D., Wiebe M.G., Cunliffe B., Naylor T.W. 1990; Growth and morphology of Fusarium graminearumand other fungi in batch and continuous culture.. In Microbial Growth Dynamics pp. 17–38 Poole R.K., Bazin M.J., Keevil C.W. Edited by Oxford:: IRL Press.;
    [Google Scholar]
  79. Uejima Y., Koga T., Kamihara T. 1987; Enhanced metabolism of phosphatidylinositol in Candida tropicalis in association with filamentous growth caused by ethanol.. FEBS Lett 214:127–129
    [Google Scholar]
  80. Uno I., Fukami K., Kato H., Takenawa T., Ishikawa T. 1988; Essential role for phosphatidylinositol 4,5-bisphosphate in yeast cell proliferation.. Nature 333:188–190
    [Google Scholar]
  81. Yoko-o T., Matsui Y., Yagisawa H., Nojima H., Uno I., Toh-e A. 1993; The putative phosphoinositide-specific phospholipase C gene, PLCl, of the yeast Saccharomyces cerevisiae is important for cell growth.. Proc Natl Acad Sci USA 901804–1808
    [Google Scholar]
  82. Youatt J. 1993; Calcium and microorganisms.. Crit Rev Microbiol 19:83–97
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-143-2-437
Loading
/content/journal/micro/10.1099/00221287-143-2-437
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error