Yeast phosphatidylinositol 4-kinase, Pik1, has essential roles at the Golgi and in the nucleus

Journal of Cell Biology

Volumn 171, Issue 6, 2005, Pages 967-979

  Strahl, Thomas ^a   Hama, Hiroko ^b,c   DeWald, Daryll B ^b   Thorner, Jeremy ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UTAH STATE UNIVERSITY   (United States)

^c MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL PROTEIN; PHOSPHATIDYLINOSITOL KINASE; PIK1 PROTEIN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; BIOACCUMULATION; CATALYSIS; CELL FUNCTION; CELL VIABILITY; CHIMERA; CONTROLLED STUDY; ENZYME LOCALIZATION; GENE EXPRESSION; GENE OVEREXPRESSION; GOLGI COMPLEX; NONHUMAN; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL;

1-PHOSPHATIDYLINOSITOL 4-KINASE; ACTIVE TRANSPORT, CELL NUCLEUS; CALCIUM-BINDING PROTEINS; CELL NUCLEUS; CYTOSOL; GOLGI APPARATUS; GREEN FLUORESCENT PROTEINS; KARYOPHERINS; MICROSCOPY, FLUORESCENCE; RECOMBINANT PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 29144458344     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200504104     Document Type: Article

References (74)

1. Aitchison, J.D., G. Blobel, and M.P. Rout. 1996. Kap104p: a karyopherin involved in the nuclear transport of messenger RNA binding proteins. Science. 274:624-627.
2. Albertini, M., L.F. Pemberton, J.S. Rosenblum, and G. Blobel. 1998. A novel nuclear import pathway for the transcription factor TFIIS. J. Cell Biol. 143:1447-1455.
3. Ames, J.B., K.B. Hendricks, T. Strahl, I.G. Huttner, N. Hamasaki, and J. Thorner. 2000. Structure and calcium-binding properties of Frq1, a novel calcium sensor in the yeast Saccharomyces cerevisiae. Biochemistry. 39:12149-12161.
4. Audhya, A., and S.D. Emr. 2002. Stt4 PI 4-kinase localizes to the plasma membrane and functions in the Pkc1-mediated MAP kinase cascade. Dev. Cell. 2:593-605.
5. Audhya, A., and S.D. Emr. 2003. Regulation of PI4,5P2 synthesis by nuclearcytoplasmic shuttling of the Mss4 lipid kinase. EMBO J. 22:4223-4236.
6. Audhya, A., M. Foti, and S.D. Emr. 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.
7. Begley, M.J., G.S. Taylor, S.-A. Kim, D.M. Veine, J.E. Dixon, and J.A. Stuckey. 2003. Crystal structure of a phosphoinositide phosphatase, MTMR 2, insights into myotubular myopathy and Charcot-Marie Tooth Syndrome. Mol. Cell. 12:1391-1402.
8. Bourne, Y., J. Dannenberg, V. Pollmann, P. Marchot, and O. Pongs. 2001. Immunocytochemical localization and crystal structure of human frequenin (neuronal calcium sensor 1). J. Biol. Chem. 276:11949-11955.
9. Brachmann, C.B., A. Davies, G.J. Cost, E. Caputo, J. Li, P. Hieter, and J.D. Boeke. 1998. Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast. 14:115-132.
10. Brickner, J.H., and P. Walter. 2004. Gene recruitment of the activated INO1 locus to the nuclear membrane. PLoS Biol. 10.1371/journal.pbio.0020342.
11. Chang, F.S., G.-S. Han, G.M. Carman, and K.J. Blumer. 2005. A WASp-binding type II phosphatidylinositol 4-kinase required for actin polymerization-driven endosome motility. J. Cell Biol. 171:133-142.
12. Chang, H.J., S.A. Jesch, M.L. Gaspa, and S.A. Henry. 2004. Role of the unfolded protein response pathway in secretory stress and regulation of INO1 expression in Saccharomyces cerevisiae. Genetics. 168:1899-1913.
13. de Graaf, P., W.T. Zwart, R.A.J. van Dijken, M. Deneka, T.K.F. Schulz, N. Geijsen, P.J. Coffer, B.M. Gadella, A.J. Verkleij, P. van der Sluijs, and P.M van Bergen en Henegouwen. 2004. Phosphatidylinositol 4-kinase is critical for association of rab11 with the golgi complex. Mol. Biol. Cell. 15:2038-2047.
14. Desrivieres, S., F.T. Cooke, P.J. Parker, and M.N. Hall. 1998. MSS4, a phosphatidylinositol-4-phosphate 5-kinase required for organization of the actin cytoskeleton in Saccharomyces cerevisiae. J. Biol. Chem. 273:15787-15793.
15. Doerks, T., M. Strauss, M. Brendel, and P. Bork. 2000. GRAM, a novel domain in glucosyltransferases, myotubularins, and other putative membraneassociated proteins. Trends Biochem. Sci. 25:483-485.
16. Enenkel, C., G. Blobel, and M. Rexach. 1995. Identification of a yeast karyopherin heterodimer that targets import substrate to mammalian nuclear pore complexes. J. Biol. Chem. 270:16499-16502.
17. Esmon, B., P. Novick, and R. Schekman. 1981. Compartmentalized assembly of oligosaccharides on exported glycoproteins in yeast. Cell. 25:451-460.
18. Flanagan, C.A., and J. Thorner. 1992. Purification and characterization of a soluble phosphatidylinositol 4-kinase from the yeast Saccharomyces cerevisiae. J. Biol. Chem. 267:24117-24125.
19. Flanagan, C.A., E.A. Schnieders, A.W. Emerick, R. Kunisawa, A. Admon, and J. Thorner. 1993. Phosphatidylinositol 4-kinase: gene structure and requirement for yeast cell viability. Science. 262:1444-1448.
20. Flick, J.S., and J. Thorner. 1993. Genetic and biochemical characterization of a phosphatidylinositol-specific phospholipase C in Saccharomyces cerevisiae. Mol. Cell. Biol. 13:5861-5876.
21. Franzusoff, A., K. Redding, J. Crosby, R.S. Fuller, and R. Schekman. 1991. Localization of components involved in protein transport and processing through the yeast Golgi apparatus. J. Cell Biol. 112:27-37.
22. Garcia-Bustos, J.F., F. Marini, I. Stevenson, C. Frei, and M.N. Hall. 1994. PIK1, an essential phosphatidylinositol 4-kinase associated with the yeast nucleus. EMBO J. 13:2352-2361.
23. Godi, A., P. Pertile, R. Meyers, P. Marra, G. Di Tullio, C. Iurisci, A. Luini, D. Corda, and M.A. De Matteis. 1999. ARF mediates recruitment of PtdIns-4-OH kinase-beta and stimulates synthesis of PtdIns(4,5)P-2 on the Golgi complex. Nat. Cell Biol. 1:280-287.
24. Gozani, O., P. Karuman, D.R. Jones, D. Ivanov, J. Cha, A.A. Lugovskoy, C.L. Baird, H. Zhu, S.J. Field, S.L. Lessnick, et al. 2003. The PHD finger of the chromatin-associated protein ING2 functions as a nuclear phosphoinositide receptor. Cell. 114:99-111.
25. Guthrie, C., and G.R. Fink. 1991. Guide to yeast genetics and molecular biology. Methods in Enzymology, vol. 194, ed. J.N. Abelson and M.I. Simon. New York: Academic Press, Inc.
26. Ha, S.A., J. Torabinejad, D.B. DeWald, M.R. Wenk, L. Lucast, P. De Camilli, R.A. Newitt, R. Aebersold, and S.F. Nothwehr. 2003. The synaptojaninlike protein Inp53/Sjl3 functions with clathrin in a yeast TGN-to-endosome pathway distinct from the GGA protein-dependent pathway. Mol. Biol. Cell. 14:1319-1333.
27. Hama, H., E.A. Schnieders, J. Thorner, J.Y. Takemoto, and D.B. DeWald. 1999. Direct involvement of phosphatidylinositol 4-phosphate in secretion in the yeast Saccharomyces cerevisiae. J. Biol. Chem. 274:34294-34300.
28. Han, G.S., A. Audhya, D.J. Markley, S.D. Emr, and G.M. Carman. 2002. The Saccharomyces cerevisiae LSB6 gene encodes phosphatidylinositol 4-kinase activity. J. Biol. Chem. 277:47709-47718.
29. Hancock, J.F. 2003. Ras proteins: different signals from different locations. Nat. Rev. Mol. Cell Biol. 4:373-384.
30. Haynes, L.P., G.M. Thomas, and R.D. Burgoyne. 2005. Interaction of neuronal calcium sensor-1 and ADP-ribosylation factor 1 allows bidirectional control of phosphatidylinositol 4-kinase beta and trans-Golgi network-plasma membrane traffic. J. Biol. Chem. 280:6047-6054.
31. Heilmeyer, L.M., Jr., G. Vereb Jr., G. Vereb, A. Kakuk, and I. Szivak. 2003. Mammalian phosphatidylinositol 4-kinases. IUBMB Life. 55:59-65.
32. Hendricks, K.B., B.Q. Wang, E.A. Schnieders, and J. Thorner. 1999. Yeast homologue of neuronal frequenin is a regulator of phosphatidylinositol-4-OH kinase. Nat. Cell Biol. 1:234-241.
33. Huh, W.K., J.V. Falvo, L.C. Gerke, A.S. Carroll, R.W. Howson, J.S. Weissman, and E.K. O'Shea. 2003. Global analysis of protein localization in budding yeast. Nature. 425:686-691.
34. Huttner, I.G., T. Strahl, M. Osawa, D.S. King, J.B. Ames, and J. Thorner. 2003. Molecular interactions of yeast frequenin (Frq1) with the phosphatidylinositol 4-kinase isoform, Pik1. J. Biol. Chem. 278:4862-4874.
35. Huynh, C.V. 1998. Molecular genetic analysis of a phosphoinositide- specific phospholipase C (PLC1 gene product) in the yeast Saccharomyces cerevisiae. Ph.D. thesis. University of California, Berkeley, Berkeley, CA. 173 pp.
36. Iovine, M.K., and S.R. Wente. 1997. A nuclear export signal in Kap95p is required for both recycling the import factor and interaction with the nucleoporin GLFG repeat regions of Nup116p and Nup100p. J. Cell Biol. 137:797-811.
37. Irvine, R.F. 2003. Nuclear lipid signaling. Nat. Rev. Mol. Cell Biol. 4:349-360.
38. Jones, E.W. 1991. Tackling the protease problem in yeast. Methods Enzymol. 194:428-435.
39. Kamada, Y., H. Qadota, C.P. Python, Y. Anraku, Y. Ohya, and D.E. Levin. 1996. Activation of yeast protein kinase C by Rho1 GTPase. J. Biol. Chem. 271:9193-9196.
40. Kapp-Barnea, Y., S. Melnikov, I. Shefler, A. Jeromin, and R. Sagi-Eisenberg. 2003. Neuronal calcium sensor-1 and phosphatidylinositol 4-kinase beta regulate IgE receptor-triggered exocytosis in cultured mast cells. J. Immunol. 171:5320-5327.
41. Levin, D.E., F.O. Fields, R. Kunisawa, J.M. Bishop, and J. Thorner. 1990. A candidate protein kinase C gene, PKC1, is required for the S. cerevisiae cell cycle. Cell. 62:213-224.
42. Levine, T.P., and S. Munro. 2002. Targeting of Golgi-specific pleckstrin homology domains involves both PtdIns 4-kinase-dependent and -independent components. Curr. Biol. 12:695-704.
43. Li, X., M.P. Rivas, M. Fang, J. Marchena, B. Mehrotra, A. Chaudhary, L. Feng, G.D. Prestwich, and V.A. Bankaitis. 2002. Analysis of oxysterol binding protein homologue Kes1p function in regulation of Sec14p-dependent protein transport from the yeast Golgi complex. J. Cell Biol. 157:63-77.
44. Li, Y., R.D. Moir, I.K. Sethy-Coraci, J.R. Warner, and I.M. Willis. 2000. Repression of ribosome and tRNA synthesis in secretion-defective cells is signaled by a novel branch of the cell integrity pathway. Mol. Cell. Biol. 20:3843-3851.
45. Loeb, J.D., G. Schlenstedt, D. Pellman, D. Kornitzer, P.A. Silver, and G.R. Fink. 1995. The yeast nuclear import receptor is required for mitosis. Proc. Natl. Acad. Sci. USA. 92:7647-7651.
46. Longtine, M.S., A. McKenzie III, D.J. Demarini, N.G. Shah, A. Wach, A. Brachat, A. Philippsen, and J.R. Pringle. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast. 14:953-961.
47. Martin, T.F. 1998. Phosphoinositide lipids as signaling molecules: common themes for signal transduction, cytoskeletal regulation, and membrane trafficking. Annu. Rev. Cell Dev. Biol. 14:231-264.
48. Michell, R.H., N.M. Perera, and S.K. Dove. 2003. New insights into the roles of phosphoinositides and inositol polyphosphates in yeast. Biochem. Soc. Trans. 31:11-15.
49. Miller, A.L., M. Suntharalingam, S.L. Johnson, A. Audhya, S.D. Emr, and S.R. Wente. 2004. Cytoplasmic inositol hexakisphosphate production is sufficient for mediating the Gle1-mRNA export pathway. J. Biol. Chem. 279:51022-51032.
50. Nanduri, J., and A.M. Tartakoff. 2001. The arrest of secretion response in yeast: signaling from the secretory path to the nucleus via Wsc proteins and Pkc1p. Mol. Cell. 8:281-289.
51. Nanduri, J., S. Mitra, C. Andrei, Y. Liu, Y. Yu, M. Hitomi, and A.M. Tartakoff. 1999. An unexpected link between the secretory path and the organization of the nucleus. J. Biol. Chem. 274:33785-33789.
52. Nikolaev, I., M.F. Cochet, and B. Felenbok. 2003. Nuclear import of zinc binuclear cluster proteins proceeds through multiple, overlapping transport pathways. Eukaryot. Cell. 2:209-221.
53. Odom, A.R., A. Stahlberg, S.R. Wente, and J.D. York. 2000. A role for nuclear inositol 1,4,5-trisphosphate kinase in transcriptional control. Science. 287:2026-2029.
54. Pryciak, P.M., and F.A. Huntress. 1998. Membrane recruitment of the kinase cascade scaffold protein Ste5 by the Gβ-γ complex underlies activation of the yeast pheromone response pathway. Genes Dev. 12:2684-2697.
55. Rao, V.D., S. Misra, I.V. Boronenkov, R.A. Anderson, and J.H. Hurley. 1998. Structure of type IIβ phosphatidylinositol phosphate kinase: a protein kinase fold flattened for interfacial phosphorylation. Cell. 94:829-839.
56. Reinke, C.A., P. Kozik, and B.S. Glick. 2004. Golgi inheritance in small buds of Saccharomyces cerevisiae is linked to endoplasmic reticulum inheritance. Proc. Natl. Acad. Sci. USA. 101:18018-18023.
57. Sata, M., J.G. Donaldson, J. Moss, and M. Vaughan. 1998. Brefeldin A-inhibited guanine nucleotide-exchange activity of Sec7 domain from yeast Sec7 with yeast and mammalian ADP ribosylation factors. Proc. Natl. Acad. Sci. USA. 95:4204-4208.
58. Schnieders, E.A. 1996. Biochemical and genetic analysis of a phosphatidylinositol 4-kinase (PIK1 gene product) in the yeast Saccharomyces cerevisiae. Ph.D. thesis. University of California, Berkeley, Berkeley, CA. 185 pp.
59. Sciorra, V.A., A. Audhya, A.B. Parsons, N. Segev, and C. Boone. 2005. Synthetic genetic array analysis of the PtdIns 4-kinase Pik1p identifies components in a Golgi-specific Ypt31/rab-GTPase signaling pathway. Mol. Biol. Cell. 16:776-793.
60. Shelton, S.N., B. Barylko, D.D. Binns, B.F. Horazdovsky, J.P. Albanesi, and J.M. Goodman. 2003. Saccharomyces cerevisiae contains a Type II phosphoinositide 4-kinase. Biochem. J. 371:533-540.
61. Shen, X., H. Xiao, R. Ranallo, W.H. Wu, and C. Wu. 2003. Modulation of ATP-dependent chromatin-remodeling complexes by inositol polyphosphates. Science. 299:112-114.
62. Sherman, F., G.R. Fink, and J.A. Hicks. 1986. Appendix A. In Laboratory Course Manual for Methods in Yeast Genetics. Cold Spring Harbor Laboratory Press. Cold Spring Harbor, NY. 163-167.
63. Shulewitz, M.J., C.J. Inouye, and J. Thorner. 1999. Hsl7 localizes to a septin ring and serves as an adapter in a regulatory pathway that relieves tyrosine phosphorylation of Cdc28 protein kinase in Saccharomyces cerevisiae. Mol. Cell. Biol. 19:7123-7137.
64. Sikorski, R.S., and P. Hieter. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics. 122:19-27.
65. Stade, K., C.S. Ford, C. Guthrie, and K. Weis. 1997. Exportin 1 (Crm1p) is an essential nuclear export factor. Cell. 90:1041-1050.
66. Steger, D.J., E.S. Haswell, A.L. Miller, S.R. Wente, and E.K. O'Shea. 2003. Regulation of chromatin remodeling by inositol polyphosphates. Science. 299:114-116.
67. Strahl, T., B. Grafelmann, J. Dannenberg, J. Thorner, and O. Pongs. 2003. Conservation of regulatory function in calcium-binding proteins: Human frequenin (neuronal calcium sensor-1) associates productively with yeast phosphatidylinositol 4-kinase isoform, Pik1. J. Biol. Chem. 278:49589-49599.
68. Strom, A.C., and K. Weis. 2001. Importin-beta-like nuclear transport receptors. Genome Biol 10.1186/gb-2001-2-6-reviews3008.
69. Walch-Solimena, C., and P. Novick. 1999. The yeast phosphatidylinositol- 4-OH kinase Pik1 regulates secretion at the Golgi. Nat. Cell Biol. 1:523-525.
70. Wang, Y.J., J. Wang, H.Q. Sun, M. Martinez, Y.X. Sun, E. Macia, T. Kirchhausen, J.P. Albanesi, M.G. Roth, and H.L. Yin. 2003. Phosphatidylinositol 4 phosphate regulates targeting of clathrin adaptor AP-1 complexes to the Golgi. Cell. 114:299-310.
71. Xiao, Z., J.T. McGrew, A.J. Schroeder, and M. Fitzgerald-Hayes. 1993. CSE1 and CSE2, two new genes required for accurate mitotic chromosome segregation in Saccharomyces cerevisiae. Mol. Cell. Biol. 13:4691-4702.
72. York, J.D., A.R. Odom, R. Murphy, E.B. Ives, and S.R. Wente. 1999. A phospholipase C-dependent inositol polyphosphate kinase pathway required for efficient messenger RNA export. Science. 285:96-100.
73. York, S.J., B.N. Armbruster, P. Greenwell, T.D. Petes, and J.D. York. 2005. Inositol diphosphate signaling regulates telomere length. J. Biol. Chem. 280:4264-4269.
74. Yoshida, S., Y. Ohya, M. Goebl, A. Nakano, and Y. Anraku. 1994. A novel gene, STT4, encodes a phosphatidylinositol 4-kinase in the PKC1 protein kinase pathway of Saccharomyces cerevisiae. J. Biol. Chem. 269:1166-1172.