Increased protein kinase or decreased PP2A activity bypasses sphingoid base requirement in endocytosis

EMBO Journal

Volumn 19, Issue 12, 2000, Pages 2834-2844

  Friant, Sylvie ^a   Zanolari, Bettina ^a   Riezman, Howard ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Casein kinase I; Endocytosis; Protein kinase C; Protein phosphatase 2A; Sphingoid base

Indexed keywords

ACTIN; PHOSPHOPROTEIN PHOSPHATASE 2A; PROTEIN KINASE; SPHINGOLIPID; SPHINGOSINE;

ARTICLE; CONTROLLED STUDY; CYTOSKELETON; ENDOCYTOSIS; ENZYME ACTIVITY; GENE MUTATION; INTERNALIZATION; MEMBRANE TRANSPORT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SYNTHESIS; YEAST;

SPHINGIODEA;

EID: 0034660458     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/19.12.2834     Document Type: Article

References (78)

1. Anderson, R.G. (1998) The caveolae membrane system. Annu. Rev. Biochem., 67, 199-225.
2. Antonsson, B., Montessuit, S., Friedli, L., Payton, M.A. and Paravicini, G. (1994) Protein kinase C in yeast. Characteristics of the Saccharomyces cerevisiae PKC1 gene product. J. Biol. Chem., 269, 16821-16828.
3. Bankaitis, V.A., Aitken, J.R., Cleves, A.E. and Dowhan, W. (1990) An essential role for a phospholipid transfer protein in yeast Golgi function. Nature, 347, 561-562.
4. Benedetti, H., Raths, S., Crausaz, F. and Riezman, H. (1994) The END3 gene encodes a protein that is required for the internalization step of endocytosis and for actin cytoskeleton organization in yeast. Mol. Biol. Cell, 5, 1023-1037.
5. Bokoch, G.M., Reilly, A.M., Daniels, R.H., King, C.C., Olivera, A., Spiegel, S. and Knaus, U.G. (1998) A GTPase-independent mechanism of p21-activated kinase activation. Regulation by sphingosine and other biologically active lipids. J. Biol. Chem., 273, 8137-8144.
6. Camps, M., Nichols, A., Gillieron, C., Antonsson, B., Muda, M., Chabert, C., Boschert, U. and Arkinstall, S. (1998) Catalytic activation of the phosphatase MKP-3 by ERK2 mitogen-activated protein kinase. Science, 280, 1262-1265.
7. Chen, P., Lee, K.S. and Levin, D.E. (1993) A pair of putative protein kinase genes (YPK1 and YPK2) is required for cell growth in Sacharomyces cerevisiae. Mol. Gen. Genet., 236, 443-447.
8. Cuvillier, O., Pirianov, G., Kleuser, B., Vanek, P.G., Coso, O.A., Gutkind, S. and Spiegel, S. (1996) Suppression of ceramide-mediated programmed cell death by sphingosine-1-phosphate. Nature, 381, 800-803.
9. Delley, P.A. and Hall, M.N. (1999) Cell wall stress depolarizes cell growth via hyperactivation of RHO1. J. Cell Biol., 147, 163-174.
10. Desrivières, S., Cooke, F.T., Parker, P.J. and 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.
11. Dickson, R.C., Nagiec, E.E., Skrzypek, M., Tillman, P., Wells, G.B. and Lester, R.L. (1997) Sphingolipids are potential heat stress signals in Saccharomyces. J. Biol. Chem., 272, 30196-30200.
12. Dobrowsky, R.T., Kamibayashi, C., Mumby, M.C. and Hannun, Y.A. (1993) Ceramide activates heterotrimeric protein phosphatase 2A. J. Biol. Chem., 268, 15523-15530.
13. Dulic, V., Egerton, M., Elguindi, I., Raths, S., Singer, B. and Riezman, H. (1991) Yeast endocytosis assays. Methods Enzymol., 194, 697-710.
14. Fishbein, J.D., Dobrowsky, R.T., Bielawska, A., Garrett, S. and Hannun, Y.A. (1993) Ceramide-mediated growth inhibition and CAPP are conserved in Saccharomyces cerevisiae. J. Biol. Chem., 268, 9255-9261.
15. Geli, M.I. and Riezman, H. (1998) Endocytic internalization in yeast and animal cells: similar and different. J. Cell Sci., 111, 1031-1037.
16. Geli, M.I., Wesp, A. and Riezman, H. (1998) Distinct functions of calmodulin are required for the uptake step of receptor-mediated endocytosis in yeast: the type 1 myosin Myo5p is one of the calmodulin targets. EMBO J., 17, 635-647.
17. Hannun, Y.A. (1994) The sphingomyelin cycle and the second messenger function of ceramide. J. Biol. Chem., 269, 3125-3128.
18. Hannun, Y.A. (1996) Functions of ceramide in coordinating cellular responses to stress. Science, 274, 1855-1859.
19. Hannun, Y.A., Loomis, C.R., Merrill, A.H.,Jr and Bell, R.M. (1986) Sphingosine inhibition of protein kinase C activity and of phorbol dibutyrate binding in vitro and in human platelets. J. Biol. Chem., 261, 12604-12609.
20. Healy, A.M., Zolnierowicz, S., Stapleton, A.E., Goebl, M., DePaoli-Roach, A.A. and Pringle, J.R. (1991) CDC55. a Saccharomyces cerevisiae gene involved in cellular morphogenesis: identification, characterization and homology to the B subunit of mammalian type 2A protein phosphatase. Mol. Cell. Biol., 11, 5767-5780.
21. Helliwell, S.B., Howald, I., Barbet, N. and Hall, M.N. (1998a) TOR2 is part of two related signaling pathways coordinating cell growth in Saccharomyces cerevisiae. Genetics, 148, 99-112.
22. Helliwell, S.B., Schmidt, A., Ohya, Y. and Hall, M.N. (1998b) The Rho1 effector Pkc1, but not Bni1, mediates signalling from Tor2 to the actin cytoskeleton. Curr. Biol., 8, 1211-1214.
23. Herskowitz, I. (1995) MAP kinase pathways in yeast: for mating and more. Cell, 80, 187-197.
24. Hicke, L., Zanolari, B. and Riezman, H. (1998) Cytoplasmic tail phosphorylation of the α-factor receptor is required for its ubiquitination and internalization. J. Cell Biol., 141, 349-358.
25. Hill, J., Donald, K.A., Griffiths, D.E. and Donald, G. (1991) DMSO-enhanced whole cell yeast transformation. Nucleic Acids Res., 19, 5791.
26. Horvath, A., Sütterlin, C., Manning-Krieg, U., Movva, N.R. and Riezman, H. (1994) Ceramide synthesis enhances transport of GPI-anchored proteins to the Golgi apparatus in yeast. EMBO J., 13, 3687-3695.
27. Hunter, T. and Plowman, G.D. (1997) The protein kinases of budding yeast: six score and more. Trends Biochem. Sci., 22, 18-22.
28. Irie, K., Takase, M., Lee, K.S., Levin, D.E., Araki, H., Matsumoto, K. and Oshima, Y. (1993) MKK1 and MKK2, which encode Saccharomyces cerevisiae mitogen-activated protein kinase-kinase homologs, function in the pathway mediated by protein kinase C. Mol. Cell. Biol., 13, 3076-3083.
29. Jayadev, S. and Hannun, Y.A. (1996) Ceramide: role in growth inhibitory cascades. J. Lipid Mediat. Cell Signal., 14, 295-301.
30. Jenkins, G.M., Richards, A., Wahl, T., Mao, C., Obeid, L. and Hannun, Y. (1997) Involvement of yeast sphingolipids in the heat stress response of Saccharomyces cerevisiae. J. Biol. Chem., 272, 32566-32572.
31. Kamada, Y., Jung, U.S., Piotrowski, J. and Levin, D.E. (1995) The protein kinase C-activated MAP kinase pathway of Saccharomyces cerevisiae mediates a novel aspect of the heat shock response. Genes Dev., 9, 1559-1571.
32. Kearns, B.G., McGee, T.P., Mayinger, P., Gedvilaite, A., Phillips, S.E., Kagiwada, S. and Bankaitis, V.A. (1997) Essential role for diacylglycerol in protein transport from the yeast Golgi complex. Nature, 387, 101-105.
33. King, C.C., Zenke, F.T., Dawson, P.E., Dutil, E.M., Newton, A.C., Hemmings, B.A. and Bokoch, G.M. (2000) Sphingosine is a novel activator of 3-phosphoinositide-dependent kinase-1. J. Biol. Chem., 29, in press.
34. Kobayashi, T., Gu, F. and Gruenberg, J. (1998) Lipids, lipid domains and lipid-protein interactions in endocytic membrane traffic. Semin. Cell Dev. Biol., 9, 517-526.
35. Kolesnick, R. and Hannun, Y.A. (1999) Ceramide and apoptosis. Trends Biochem. Sci., 24, 224-225.
36. Kübler, E. and Riezman, H. (1993) Actin and fimbrin are required for the internalization step of endocytosis in yeast. EMBO J., 12, 2855-2862.
37. Kübler, E., Schimmöller, F. and Riezman, H. (1994) Calcium-independent calmodulin requirement for endocytosis in yeast. EMBO J., 13, 5539-5546.
38. Lee, K.S. and Levin, D.E. (1992) Dominant mutations in a gene encoding a putative protein kinase (BCK1) bypass the requirement for a Saccharomyces cerevisiae protein kinase C homolog. Mol. Cell. Biol., 12, 172-182.
39. Lee, K.S., Irie, K., Gotoh, Y., Watanabe, Y., Araki, H., Nishida, E., Matsumoto, K. and Levin, D.E. (1993) A yeast mitogen-activated protein kinase homolog (Mpk1p) mediates signalling by protein kinase C. Mol. Cell. Biol., 13, 3067-3075.
40. Lin, F.C. and Arndt, K.T. (1995) The role of Saccharomyces cerevisiae type 2A phosphatase in the actin cytoskeleton and in entry into mitosis. EMBO J., 14, 2745-2759.
41. Mandala, S.M., Thornton, R., Tu, Z., Kurtz, M.B., Nickels, J., Broach, J., Menzeleev, R. and Spiegel, S. (1998) Sphingoid base 1-phosphate phosphatase: a key regulator of sphingolipid metabolism and stress response. Proc. Natl Acad. Sci. USA, 95, 150-155.
42. Mao, C., Saba, J.D. and Obeid, L.M. (1999) The dihydrosphingosine-1-phosphate phosphatases of Saccharomyces cerevisiae are important regulators of cell proliferation and heat stress responses. Biochem. J., 342, 667-675.
43. Marchal, C., Haguenauer-Tsapis, R. and Urban-Grimal, D. (1998) A PEST-like sequence mediates phosphorylation and efficient ubiquitination of yeast uracil permease. Mol. Cell. Biol., 18, 314-321.
44. Mazzoni, C., Zarov, P., Rambourg, A. and Mann, C. (1993) The SLT2 (MPK1) MAP kinase homolog is involved in polarized cell growth in Saccharomyces cerevisiae. J. Cell Biol., 123, 1821-1833.
45. McDonald, O.B., Hannun, Y.A., Reynolds, C.H. and Sahyoun, N. (1991) Activation of casein kinase II by sphingosine. J. Biol. Chem., 266, 21773-21776.
46. Muller, G., Ayoub, M., Storz, P., Rennecke, J., Fabbro, D. and Pfizenmaier, K. (1995) PKCζ is a molecular switch in signal transduction of TNF-α, bifunctionally regulated by ceramide and arachidonic acid. EMBO J., 14, 1961-1969.
47. +-ATPase-defective yeast: identification of six new END genes. J. Cell Biol., 127, 373-386.
48. Munn, A.L., Stevenson, B.J., Geli, M.I. and Riezman, H. (1995) end5, end6 and end7: mutations that cause actin delocalization and block the internalization step of endocytosis in Saccharomyces cerevisiae. Mol. Biol. Cell, 6, 1721-1742.
49. Munn, A.L., Heese-Peck, A., Stevenson, B.J., Pichler, H. and Riezman, H. (1999) Specific sterols required for the internalization step of endocytosis in yeast. Mol. Biol. Cell, 10, 3943-3957.
50. Nagiec, M.M., Baltisberger, J.A., Wells, G.B., Lester, R.L. and Dickson, R.C. (1994) The LCB2 gene of Saccharomyces and the related LCB1 gene encode subunits of serine palmitoyltransferase, the initial enzyme in sphingolipid synthesis. Proc. Natl Acad. Sci. USA, 91, 7899-7902.
51. 1 arrest of Saccharomyces cerevisiae. Genes Dev., 10, 382-394.
52. Nonaka, H., Tanaka, K., Hirano, H., Fujiwara, T., Kohno, H., Umikawa, M., Mino, A. and Takai, Y. (1995) A downstream target of RHO1 small GTP-binding protein is PKC1, a homolog of protein kinase C, which leads to activation of the MAP kinase cascade in Saccharomyces cerevisiae. EMBO J., 14, 5931-5938.
53. Ono, Y., Fujii, T., Ogita, K., Kikkawa, U., Igarashi, K. and Nishizuka, Y. (1989) Protein kinase C ζ subspecies from rat brain: its structure, expression and properties. Proc. Natl Acad. Sci. USA, 86, 3099-3103.
54. Panek, H.R., Stepp, J.D., Engle, H.M., Marks, K.M., Tan, P.K., Lemmon, S.K. and Robinson, L.C. (1997) Suppressors of YCK-encoded yeast casein kinase 1 deficiency define the four subunits of a novel clathrin AP-like complex. EMBO J., 16, 4194-4204.
55. Pushkareva, M., Khan, W.A., Alessenko, A.V., Sahyoun, N. and Hannun, Y.A. (1992) Sphingosine activation of protein kinases in Jurkat T cells. In vitro phosphorylation of endogenous protein substrates and specificity of action. J. Biol. Chem., 267, 15246-15251.
56. Pushkareva, M., Bielawska, A., Menaldiv, D., Liotta, D. and Hannun, Y.A. (1993) Regulation of sphingosine-activated protein kinases: selectivity of activation by sphingoid bases and inhibition by non-esterified fatty acids. Biochem. J., 294, 699-703.
57. Raths, S., Rohrer, J., Crausaz, F. and Riezman, H. (1993) end3 and end4: two mutants defective in receptor-mediated and fluid-phase endocytosis in Saccharomyces cerevisiae. J. Cell Biol., 120, 55-65.
58. Riezman, H. (1998) Down regulation of yeast G protein-coupled receptors. Semin. Cell Dev. Biol., 9, 129-134.
59. Riezman, H., Munn, A., Geli, M.I. and Hicke, L. (1996) Actin-, myosin-and ubiquitin-dependent endocytosis. Experientia, 52, 1033-1041.
60. Robinson, L.C. et al. (1992) Yeast casein kinase I homologues: an essential gene pair. Proc. Natl Acad Sci. USA, 89, 28-32.
61. Robinson, L.C., Menold, M.M., Garrett, S. and Culbertson, M.R. (1993) Casein kinase I-like protein kinases encoded by YCK1 and YCK2 are required for yeast morphogenesis. Mol. Cell. Biol., 13, 2870-2881.
62. Robinson, L.C., Bradley, C., Bryan, J.D., Jerome, A., Kweon, Y. and Panek, H.R. (1999) The yck2 yeast casein kinase 1 isoform shows cell cycle-specific localization to sites of polarized growth and is required for proper septin organization. Mol. Biol. Cell, 10, 1077-1092.
63. Rodal, S.K., Skretting, G., Garred, O., Vilhardt, F., van Deurs, B. and Sandvig, K. (1999) Extraction of cholesterol with methyl-β-cyclodextrin perturbs formation of clathrin-coated endocytic vesicles. Mol. Biol. Cell, 10, 961-974.
64. Ronne, H., Carlberg, M., Hu, G.Z. and Nehlin, J.O. (1991) Protein phosphatase 2A in Saccharomyces cerevisiae: effects on cell growth and bud morphogenesis. Mol. Cell. Biol., 11, 4876-4884.
65. Schiestl, R.H. and Gietz, R.D. (1989) High efficiency transformation of intact yeast cells using single stranded nucleic acids as a carrier. Curr. Genet., 16, 339-346.
66. Schmidt, A., Beck, T., Koller, A., Kunz, J. and Hall, M.N. (1998) The TOR nutrient signalling pathway phosphorylates NPR1 and inhibits turnover of the tryptophan permease. EMBO J., 17, 6924-6931.
67. Schu, P.V., Takegawa, K., Fry, M.J., Stack, J.H., Waterfield, M.D. and Emr, S.D. (1993) Phosphatidylinositol 3-kinase encoded by yeast VPS34 gene essential for protein sorting. Science, 260, 88-91.
68. Sherman, F., Fink, G. and Hicks, J.B. (1983) Methods in Yeast Genetics: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
69. Skrzypek, M.S., Nagiec, M.M., Lester, R.L. and Dickson, R.C. (1999) Analysis of phosphorylated sphingolipid long-chain bases reveals potential roles in heat stress and growth control in Saccharomyces. J. Bacteriol., 181, 1134-1140.
70. Sneddon, A.A., Cohen, P.T. and Stark, M.J. (1990) Saccharomyces cerevisiae protein phosphatase 2A performs an essential cellular function and is encoded by two genes. EMBO J., 9, 4339-4346.
71. Subtil, A., Gaidarov, I., Kobylarz, K., Lampson, M.A., Keen. J.H. and McGraw, T.E. (1999) Acute cholesterol depletion inhibits clathrin-coated pit budding. Proc. Natl Acad. Sci. USA, 96, 6775-6780.
72. 1 for progression into S phase. Mol. Cell. Biol., 11, 2133-2148.
73. van Blitterswijk, W.J. (1998) Hypothesis: ceramide conditionally activates atypical protein kinases C, Raf-1 and KSR through binding to their cysteine-rich domains. Biochem. J., 331, 679-680.
74. van Zyl, W., Huang, W., Sneddon, A.A., Stark, M., Camier, S., Werner, M., Marck, C., Sentenac, A. and Broach, J.R. (1992) Inactivation of the protein phosphatase 2A regulatory subunit A results in morphological and transcriptional defects in Saccharomyces cerevisiae. Mol. Cell. Biol., 12, 4946-4959.
75. Wang, X., Hoekstra, M.F., DeMaggio, A.J., Dhillon, N., Vancura, A., Kuret, J., Johnston, G.C. and Singer, R.A. (1996) Prenylated isoforms of yeast casein kinase I, including the novel Yck3p. suppress the gcs1 blockage of cell proliferation from stationary phase. Mol. Cell. Biol., 16, 5375-5385.
76. 2+-calmodulin-dependent protein kinase IV and protein phosphatase 2A. Science, 280, 1258-1261.
77. Wolff, R.A., Dobrowsky, R.T., Bielawska, A., Obeid, L.M. and Hannun, Y.A. (1994) Role of ceramide-activated protein phosphatase in ceramide-mediated signal transduction. J. Biol. Chem., 269, 19605-19609.
78. Zanolari, B., Friant, S., Funato, K., Sütterlin, C., Stevenson, B.J. and Riezman, H. (2000) Sphingoid base synthesis requirement for endocytosis in Saccharomyces cerevisiae. EMBO J., 19, 2824-2833.