1887

Abstract

Phosphoinositides are important lipid signalling molecules in eukaryotic cells. Phosphatidylinositol-4-phosphate 5-kinase (PI4P5K) catalyses the production of phosphatidylinositol 4,5-bisphosphate (PIP), which stimulates phospholipase D1 (PLD1) activity in mammalian and yeast cells. PLD1 catalyses the formation of phosphatidic acid (PA), which has been shown to activate PI4P5Ks in mammalian and cells. In the present study, PI4P5K activity in the opportunistic pathogen was identified. A gene with significant sequence homology to the PI4P5K was cloned and designated . This gene was demonstrated to encode a functional PI4P5K by expression in . This enzyme was found to be membrane-associated and was stimulated by PA. Within the first 20 min after induction of polarized hyphal growth induced by a shift to elevated temperature, PI4P5K activity increased 25-fold. This stimulation was not observed when hyphae were induced by a combination of elevated temperature and serum. A lack of PLD1 activity resulted in the loss of induction of PI4P5K activity during the morphogenetic switch. Furthermore, the addition of propranolol attenuated the stimulation of PI4P5K activity during morphogenesis. These results suggest that PA derived from PLD1 activity stimulates PI4P5K during the switch to the hyphal form under some conditions.

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2002-06-01
2024-12-12
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References

  1. Amsterdam A., Dantes A., Liscovitch M. 1994; Role of phospholipase-D and phosphatidic acid in mediating gonadotropin-releasing hormone-induced inhibition of preantral granulosa cell differentiation. Endocrinology 135:1205–1211
    [Google Scholar]
  2. Anderson R. A., Boronenkov I. V., Doughman S. D., Kunz J., Loijens J. C. 1999; Phosphatidylinositol phosphate kinases, a multifaceted family of signaling enzymes. J Biol Chem 274:9907–9910 [CrossRef]
    [Google Scholar]
  3. Athenstaedt K., Weys S., Paltauf F., Daum G. 1999; Redundant systems of phosphatidic acid biosynthesis via acylation of glycerol-3-phosphate or dihydroxyacetone phosphate in the yeast Saccharomyces cerevisiae . J Bacteriol 181:1458–1463
    [Google Scholar]
  4. Audhya A., Foti M., Emr S. D. 2000; Distinct roles for the yeast phosphatidylinositol 4-kinases, Stt4p and Pik1p, in secretion, cell growth, and organelle membrane dynamics. Mol Biol Cell 11:2673–2689 [CrossRef]
    [Google Scholar]
  5. Bligh E. C., Dyer W. J. 1959; A rapid method of total lipid extraction and purification. Can J Biochem Physiol 37:911–917 [CrossRef]
    [Google Scholar]
  6. Chong L. D., Traynor-Kaplan A., Bokoch G. M., Schwartz M. A. 1994; The small GTP-binding protein Rho regulates a phosphatidylinositol 4-phosphate 5-kinase in mammalian cells. Cell 79:507–513 [CrossRef]
    [Google Scholar]
  7. Cochet C., Chambaz E. M. 1986; Catalytic properties of a purified phosphatidylinositol-4-phosphate kinase from rat brain. Biochem J 237:25–31
    [Google Scholar]
  8. Cutler J. E. 1991; Putative virulence factors of Candida albicans . Annu Rev Microbiol 45:187–218 [CrossRef]
    [Google Scholar]
  9. Desrivieres S., Cooke F. T., Parker P. J., Hall M. N. 1998; MSS4, a phosphatidylinositol-4-phosphate 5-kinase required for organization of the actin cytoskeleton in Saccharomyces cerevisiae . J Biol Chem 273:15787–15793 [CrossRef]
    [Google Scholar]
  10. DiNubile M. J., Huang S. 1997a; Capping of the barbed ends of actin filaments by a high-affinity profilin-actin complex. Cell Motil Cytoskeleton 37:211–225 [CrossRef]
    [Google Scholar]
  11. DiNubile M. J., Huang S. 1997b; High concentrations of phosphatidylinositol-4,5-bisphosphate may promote actin filament growth by three potential mechanisms: inhibiting capping by neutrophil lysates, severing actin filaments and removing capping protein-beta2 from barbed ends. Biochim Biophys Acta 1358:261–278 [CrossRef]
    [Google Scholar]
  12. Dove S. K., Cooke F. T., Douglas M. R., Sayers L. G., Parker P. J., Michell R. H. 1997; Osmotic stress activates phosphatidylinositol-3,5-bisphosphate synthesis. Nature 390:187–192 [CrossRef]
    [Google Scholar]
  13. Ella K. M., Dolan J. W., Meier K. E. 1995; Characterization of a regulated form of phospholipase D in the yeast Saccharomyces cerevisiae . Biochem J 307:799–805
    [Google Scholar]
  14. Ernst J. F. 2000; Regulation of dimorphism in Candida albicans . Contrib Microbiol 5:98–111
    [Google Scholar]
  15. Fruman D. A., Meyers R. E., Cantley L. C. 1998; Phosphoinositide kinases. Annu Rev Biochem 67:481–507 [CrossRef]
    [Google Scholar]
  16. Fukami K., Furuhashi K., Inagaki M., Endo T., Hatano S., Takenawa T. 1992; Requirement of phosphatidylinositol 4,5-bisphosphate for alpha-actinin function. Nature 359:150–152 [CrossRef]
    [Google Scholar]
  17. Gietz R. D., Woods R. A. 2001; Genetic transformation of yeast. Biotechniques 30:816–820 822–826, 828 passim
    [Google Scholar]
  18. Ha K. S., Exton J. H. 1993; Activation of actin polymerization by phosphatidic acid derived from phosphatidylcholine in IIC9 fibroblasts. J Cell Biol 123:1789–1796 [CrossRef]
    [Google Scholar]
  19. Heiss S. G., Cooper J. A. 1991; Regulation of CapZ, an actin capping protein of chicken muscle, by anionic phospholipids. Biochemistry 30:8753–8758 [CrossRef]
    [Google Scholar]
  20. Homma K., Terui S., Minemura M., Qadota H., Anraku Y., Kanaho Y., Ohya Y. 1998; Phosphatidylinositol-4-phosphate 5-kinase localized on the plasma membrane is essential for yeast cell morphogenesis. J Biol Chem 273:15779–15786 [CrossRef]
    [Google Scholar]
  21. Honda A., Nogami M., Yokozeki T. 8 other authors 1999; Phosphatidylinositol 4-phosphate 5-kinase alpha is a downstream effector of the small G protein ARF6 in membrane ruffle formation. Cell 99:521–532 [CrossRef]
    [Google Scholar]
  22. Hube B., Hess D., Baker C. A., Schaller M., Schafer W., Dolan J. W. 2001; The role and relevance of phospholipase D1 during growth and dimorphism of Candida albicans . Microbiology 147:879–889
    [Google Scholar]
  23. Isakoff S. J., Cardozo T., Andreev J., Li Z., Ferguson K. M., Abagyan R., Lemmon M. A., Aronheim A., Skolnik E. Y. 1998; Identification and analysis of PH domain-containing targets of phosphatidylinositol 3-kinase using a novel in vivo assay in yeast. EMBO J 17:5374–5387 [CrossRef]
    [Google Scholar]
  24. Ishihara H., Shibasaki Y., Kizuki N., Katagiri H., Yazaki Y., Asano T., Oka Y. 1996; Cloning of cDNAs encoding two isoforms of 68-kDa type I phosphatidylinositol-4-phosphate 5-kinase. J Biol Chem 271:23611–23614 [CrossRef]
    [Google Scholar]
  25. Ishihara H., Shibasaki Y., Kizuki N., Wada T., Yazaki Y., Asano T., Oka Y. 1998; Type I phosphatidylinositol-4-phosphate 5-kinases. Cloning of the third isoform and deletion/substitution analysis of members of this novel lipid kinase family. J Biol Chem 273:8741–8748 [CrossRef]
    [Google Scholar]
  26. Janmey P. A. 1994; Phosphoinositides and calcium as regulators of cellular actin assembly and disassembly. Annu Rev Physiol 56:169–191 [CrossRef]
    [Google Scholar]
  27. Janmey P. A., Stossel T. P. 1987; Modulation of gelsolin function by phosphatidylinositol 4, 5-bisphosphate. Nature 325:362–364 [CrossRef]
    [Google Scholar]
  28. Janmey P. A., Iida K., Yin H. L., Stossel T. P. 1987; Polyphosphoinositide micelles and polyphosphoinositide-containing vesicles dissociate endogenous gelsolin-actin complexes and promote actin assembly from the fast-growing end of actin filaments blocked by gelsolin. J Biol Chem 262:12228–12236
    [Google Scholar]
  29. Jenkins G. H., Fisette P. L., Anderson R. A. 1994; Type I phosphatidylinositol 4-phosphate 5-kinase isoforms are specifically stimulated by phosphatidic acid. J Biol Chem 269:11547–11554
    [Google Scholar]
  30. Kaszkin M., Richards J., Kinzel V. 1996; Phosphatidic acid mobilized by phospholipase D is involved in the phorbol 12-myristate 13-acetate-induced G2 delay of A431 cells. Biochem J 314:129–138
    [Google Scholar]
  31. Knighton D. R., Zheng J. H., Ten Eyck L. F., Ashford V. A., Xuong N. H., Taylor S. S., Sowadski J. M. 1991; Crystal structure of the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase. Science 253:407–414 [CrossRef]
    [Google Scholar]
  32. Leberer E., Ziegelbauer K., Schmidt A., Harcus D., Dignard D., Ash J., Johnson L., Thomas D. Y. 1997; Virulence and hyphal formation of Candida albicans require the Ste20p-like protein kinase CaCla4p. Curr Biol 7:539–546 [CrossRef]
    [Google Scholar]
  33. Liscovitch M., Chalifa V., Pertile P., Chen C. S., Cantley L. C. 1994; Novel function of phosphatidylinositol 4,5-bisphosphate as a cofactor for brain membrane phospholipase D. J Biol Chem 269:21403–21406
    [Google Scholar]
  34. Liscovitch M., Czarny M., Fiucci G., Lavie Y., Tang X. 1999; Localization and possible functions of phospholipase D isozymes. Biochim Biophys Acta 1439245–263 [CrossRef]
    [Google Scholar]
  35. Loijens J. C., Anderson R. A. 1996; Type I phosphatidylinositol-4-phosphate 5-kinases are distinct members of this novel lipid kinase family. J Biol Chem 271:32937–32943 [CrossRef]
    [Google Scholar]
  36. Loijens J. C., Boronenkov I. V., Parker G. J., Anderson R. A. 1996; The phosphatidylinositol 4-phosphate 5-kinase family. Adv Enzyme Regul 36:115–140 [CrossRef]
    [Google Scholar]
  37. Majerus P. W. 1992; Inositol phosphate biochemistry. Annu Rev Biochem 61:225–250 [CrossRef]
    [Google Scholar]
  38. McLain N., Dolan J. W. 1997; Phospholipase D activity is required for dimorphic transition in Candida albicans . Microbiology 143:3521–3526 [CrossRef]
    [Google Scholar]
  39. Meier K. E., Gause K. C., Wisehart-Johnson A. E., Gore A. C., Finley E. L., Jones L. G., Bradshaw C. D., McNair A. F., Ella K. M. 1998; Effects of propranolol on phosphatidate phosphohydrolase and mitogen-activated protein kinase activities in A7r5 vascular smooth muscle cells. Cell Signal 10:415–426 [CrossRef]
    [Google Scholar]
  40. Moritz A., De Graan P. N., Gispen W. H., Wirtz K. W. 1992; Phosphatidic acid is a specific activator of phosphatidylinositol-4-phosphate kinase. J Biol Chem 267:7207–7210
    [Google Scholar]
  41. Morlock K. R., McLaughlin J. J., Lin Y. P., Carman G. M. 1991; Phosphatidate phosphatase from Saccharomyces cerevisiae . Isolation of 45- and 104-kDa forms of the enzyme that are differentially regulated by inositol. J Biol Chem 266:3586–3593
    [Google Scholar]
  42. Navarro-Garcia F., Sanchez M., Nombela C., Pla J. 2001; Virulence genes in the pathogenic yeast Candida albicans . FEMS Microbiol Rev 25:245–268 [CrossRef]
    [Google Scholar]
  43. Odds F. C. 1988 Candida and Candidosis, 2nd edn. Philadelphia, PA: Bailliere Tindall;
    [Google Scholar]
  44. Odorizzi G., Babst M., Emr S. D. 2000; Phosphoinositide signaling and the regulation of membrane trafficking in yeast. Trends Biochem Sci 25:229–235 [CrossRef]
    [Google Scholar]
  45. Ohama T., Suzuki T., Mori M., Osawa S., Ueda T., Watanabe K., Nakase T. 1993; Non-universal decoding of the leucine codon CUG in several Candida species. Nucleic Acids Res 21:4039–4045 [CrossRef]
    [Google Scholar]
  46. Rameh L. E., Tolias K. F., Duckworth B. C., Cantley L. C. 1997; A new pathway for synthesis of phosphatidylinositol-4,5-bisphosphate. Nature 390:192–196 [CrossRef]
    [Google Scholar]
  47. Rex J. H., Rinaldi M. G., Pfaller M. A. 1995; Resistance of Candida species to fluconazole. Antimicrob Agents Chemother 39:1–8 [CrossRef]
    [Google Scholar]
  48. Rose K., Rudge S. A., Frohman M. A., Morris A. J., Engebrecht J. 1995; Phospholipase D signaling is essential for meiosis. Proc Natl Acad Sci USA 92:12151–12155 [CrossRef]
    [Google Scholar]
  49. Santos M. A., Keith G., Tuite M. F. 1993; Non-standard translational events in Candida albicans mediated by an unusual seryl-tRNA with a 5′-CAG-3(leucine) anticodon. EMBO J 12:607–616
    [Google Scholar]
  50. Sherman F. 1991; Getting started with yeast. Methods Enzymol 194:3–21
    [Google Scholar]
  51. Siddhanta A., Shields D. 1998; Secretory vesicle budding from the trans-Golgi network is mediated by phosphatidic acid levels. J Biol Chem 273:17995–17998 [CrossRef]
    [Google Scholar]
  52. Surewicz W. K., Leyko W. 1981; Interaction of propranolol with model phospholipid membranes. Monolayer, spin label and fluorescent spectroscopy studies. Biochim Biophys Acta 643:387–397 [CrossRef]
    [Google Scholar]
  53. Tolias K. F., Hartwig J. H., Ishihara H., Shibasaki Y., Cantley L. C., Carpenter C. L. 2000; Type I alpha phosphatidylinositol-4-phosphate 5-kinase mediates Rac-dependent actin assembly. Curr Biol 10:153–156
    [Google Scholar]
  54. Vancurova I., Choi J. H., Lin H., Kuret J., Vancura A. 1999; Regulation of phosphatidylinositol 4-phosphate 5-kinase from Schizosaccharomyces pombe by casein kinase I. J Biol Chem 274:1147–1155 [CrossRef]
    [Google Scholar]
  55. Varnai P., Balla T. 1998; Visualization of phosphoinositides that bind pleckstrin homology domains: calcium-and agonist-induced dynamic changes and relationship to myo-[3H]inositol-labeled phosphoinositide pools. J Cell Biol 143:501–510 [CrossRef]
    [Google Scholar]
  56. Waksman M., Eli Y., Liscovitch M., Gerst J. E. 1996; Identification and characterization of a gene encoding phospholipase D activity in yeast. J Biol Chem 271:2361–2364 [CrossRef]
    [Google Scholar]
  57. Wu W. I., Lin Y. P., Wang E., Merrill A. H. Jr, Carman G. M. 1993; Regulation of phosphatidate phosphatase activity from the yeast Saccharomyces cerevisiae by sphingoid bases. J Biol Chem 268:13830–13837
    [Google Scholar]
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