Phosphoinositide signaling pathways in nuclei are associated with nuclear speckles containing Pre-mRNA processing factors

Molecular Biology of the Cell

Volumn 9, Issue 12, 1998, Pages 3547-3560

  Boronenkov, Igor V ^a   Loijens, Joost C ^a   Umeda, Masato ^b   Anderson, Richard A ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA PRECURSOR; PHOSPHATIDYLINOSITOL 4 PHOSPHATE KINASE; POLYPHOSPHOINOSITIDE;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL FRACTIONATION; ENZYME ASSAY; ENZYME LOCALIZATION; ENZYME SUBSTRATE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; NONHUMAN; PRIORITY JOURNAL; RAT; RNA PROCESSING; SIGNAL TRANSDUCTION;

ANIMALIA; MAMMALIA;

EID: 0031771547     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.9.12.3547     Document Type: Article

References (75)

1. Asano, M., Tamiya-Koizumi, K., Homma, Y., Takenawa, T., Nimura, Y., Kojima, K., and Yoshida, S. (1994). Purification and characterization of nuclear phospholipase C specific for phosphoinositides. J. Biol. Chem. 269, 12360-12366.
2. Balboa, M.A., and Insel, P.A. (1995). Nuclear phospholipase D in Madin-Darby canine kidney cells. Guanosine 5′-O-(thiotriphosphate)-stimulated activation is mediated by RhoA and is downstream of protein kinase C. J. Biol. Chem. 270, 29843-29847.
3. Bazenet, C.E., Ruano, A.R., Brockman, J.L., and Anderson, R.A. (1990). The human erythrocyte contains two forms of phosphatidylinositol-4-phosphate 5-kinase which are differentially active toward membranes. J. Biol. Chem. 265, 18012-18022.
4. Boronenkov, I.V., and Anderson, R.A. (1995). The sequence of phosphatidylinositol-4-phosphate 5-kinase defines a novel family of lipid kinases. J. Biol. Chem. 270, 2881-2884.
5. Brockman, J.L., and Anderson, R.A. (1991). Casein kinase I is regulated by phosphatidylinositol 4,5-bisphosphate in native membranes. J. Biol. Chem. 266, 2508-2512.
6. Carmo-Fonseca, M., Pepperkok, R., Carvalho, M.T., and Lamond, A.I. (1992). Transcription-dependent colocalization of the U1, U2, U4/U6, and U5 snRNPs in coiled bodies. J. Cell Biol. 117, 1-14.
7. Castellino, A.M., Parker, G.J., Boronenkov, I.V., Anderson, R.A., and Chao, M.V. (1997). A novel interaction between the juxtamembrane region of the p55 tumor necrosis factor receptor and phosphatidylinositol-4-phosphate 5-kinase. J. Biol. Chem. 272, 5861-5870.
8. Cocco, L., Gilmour, R.S., Ognibene, A., Letcher, A.J., Manzoli, F.A., and Irvine, R.F. (1987). Synthesis of polyphosphoinositides in nuclei of Friend cells. Evidence for polyphosphoinositide metabolism inside the nucleus which changes with cell differentiation. Biochem. J. 248, 765-770.
9. Cockcroft, S. (1998). Phosphatidylinositol transfer proteins: a requirement in signal transduction and vesicle traffic. Bioessays 20, 423-432.
10. Collas, P., Thompson, L., Fields, A.P., Poccia, D.L., and Courvalin, J.C. (1997). Protein kinase C-mediated interphase lamin B phosphorylation and solubilization. J. Biol. Chem. 272, 21274-21280.
11. Colwill, K., Feng, L.L., Yeakley, J.M., Gish, G.D., Caceres, J.F., Pawson, T., and Fu, X.D. (1996). SRPK1 and C1k/Sty protein kinases show distinct substrate specificities for serine/arginine-rich splicing factors. J. Biol. Chem. 271, 24569-24575.
12. Davis, L., Cadrin, M., Brown, D.L., and Chaly, N. (1993). Reversible disassembly of transcription domains in lymphocyte nuclei during inhibition of RNA synthesis by DRB. Biol. Cell 78, 163-180.
13. De Vries, K.J., Westerman, J., Bastiaens, P.I., Jovin, T.M., Wirtz, K.W., and Snoek, G.T. (1996). Fluorescently labeled phosphatidylinositol transfer protein isoforms (alpha and beta), microinjected into fetal bovine heart endothelial cells, are targeted to distinct intracellular sites. Exp. Cell Res. 227, 33-39.
14. Dignam, J.D., Lebovitz, R.M., and Roeder, R.G. (1983). Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11, 1475-1489.
15. Divecha, N., Banfic, H., and Irvine, R.F. (1991). The polyphosphoinositide cycle exists in the nuclei of Swiss 3T3 cells under the control of a receptor (for IGF-I) in the plasma membrane, and stimulation of the cycle increases nuclear diacylglycerol and apparently induces translocation of protein kinase C to the nucleus. EMBO J. 10, 3207-3214.
16. Divecha, N., Banfic, H., and Irvine, R.F. (1993). Inositides and the nucleus and inositides in the nucleus. Cell 74, 405-407.
17. Divecha, N., Banfic, H., Treagus, J.E., Vann, L., Irvine, R.F., and D'Santos, C. (1997). Nuclear diacylglycerol, the cell cycle, the enzymes and a red herring (or how we came to love phosphatidylcholine). Biochem. Soc. Trans. 25, 571-575.
18. Divecha, N., Truong, O., Hsuan, J.J., Hinchliffe, K.A., and Irvine, R.F. (1995). The cloning and sequence of the C isoform of PtdIns4P 5-kinase. Biochem. J. 309, 715-719.
19. Dove, S.K., Cooke, F.T., Douglas, M.R., Savers, L.G., Parker, P.J., and Michell, R.H. (1997). Osmotic stress activates phosphatidylinositol-3,5-bisphosphate synthesis. Nature 390, 187-192.
20. Fakan, S., Leser, G., and Martin, T.E. (1984). Ultrastructural distribution of nuclear ribonucleoproteins as visualized by immunocytochemistry on thin sections. J. Cell Biol. 98, 358-363.
21. Fricker, M., Hollinshead, M., White, N., and Vaux, D. (1997). Interphase nuclei of many mammalian cell types contain deep, dynamic, tubular membrane-bound invaginations of the nuclear envelope. J. Cell Biol. 136, 531-544.
22. Fu, X.D., and Maniatis, T. (1990). Factor required for mammalian spliceosome assembly is localized to discrete regions in the nucleus. Nature 343, 437-441.
23. Fukami, K., Matsuoka, K., Nakanishi, O., Yamakawa, A., Kawai, S., and Takenawa, T. (1988). Antibody to phosphatidylinositol 4,5-bisphosphate inhibits oncogene-induced mitogenesis. Proc. Natl. Acad. Sci. USA 85, 9057-9061.
24. Fukami, K., and Takenawa, T. (1989). Quantitative changes in polyphosphoinositides 1,2-diacylglycerol and inositol 1,4,5-trisphosphate by platelet-derived growth factor and prostaglandin F2 alpha. J. Biol. Chem. 264, 14985-14989.
25. Goss, V.L., Hocevar, B.A., Thompson, L.J., Stratton, C.A., Burns, D.J., and Fields, A.P. (1994). Identification of nuclear beta II protein kinase C as a mitotic lamin kinase. J. Biol. Chem. 269, 19074-19080.
26. Gui, J.F., Lane, W.S., and Fu, X.D. (1994). A serine kinase regulates intracellular localization of splicing factors in the cell cycle. Nature 369, 678-682.
27. Hardin, J.A., Lerner, M.R., Lerner, E.A., and Steitz, J.A. (1982). New directions in antinuclear antibody research: the Sm, RNP, Ro, and La antigens are found on small-RNA protein particles. Am. J. Kidney Dis. 2, 98-100.
28. Huang, S., and Spector, D.L. (1996). Intron-dependent recruitment of pre-mRNA splicing factors to sites of transcription. J. Cell Biol. 133, 719-732.
29. Iida, K., Matsumoto, S., and Yahara, I. (1992). The KKRKK sequence is involved in heat shock-induced nuclear translocation of the 18-kDa actin-binding protein, cofilin. Cell. Struct. Funct. 17, 39-46.
30. Ishihara, H., Shibasaki, Y., Kizuki, N., Wada, T., Yazaki, Y., Asano, T., and 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.
31. Itoh, T., Takeshi, I., and Takenawa, T. (1998). A novel phosphatidylinositol-5-phosphate 4-kinase (phosphatidylinositol-phosphate kinase IIγ) is phosphorylated in the endoplasmic reticulum in response to mitogenic signals. J. Biol. Chem. 273, 20292-20299.
32. Jackson, D.A., Hassan, A.B., Errington, R.J., and Cook, P.R. (1993). Visualization of focal sites of transcription within human nuclei. EMBO J. 12, 1059-1065.
33. Janmey, P.A. (1994). Phosphoinositides and calcium as regulators of cellular actin assembly and disassembly. Annu. Rev. Physiol. 56, 169-191.
34. Jenkins, G.H., Fisette, P.L., and Anderson, R.A. (1994). Type I phosphatidylinositol 4-phosphate 5-kinase isoforms are specifically stimulated by phosphatidic acid. J. Biol. Chem. 269, 11547-11554.
35. Kuriki, H., Tamiya-Koizumi, K., Asano, M., Yoshida, S., Kojima, K., and Nimura, Y. (1992). Existence of phosphoinositide-specific phospholipase C in rat liver nuclei and its change during liver regeneration. J. Biochem. 111, 283-286.
36. Lamond, A.I., and Earnshaw, W.C. (1998). Structure and function in the nucleus. Science 280, 547-553.
37. Liu, N., Fukami, K., Yu, H., and Takenawa, T. (1996). A new phospholipase C delta 4 is induced at S-phase of the cell cycle and appears in the nucleus. J. Biol. Chem. 272, 355-360.
38. Loijens, J.C., and 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.
39. Loijens, J.C., Boronenkov, I.V., Parker, G.J., and Anderson, R.A. (1996). The phosphatidylinositol 4-phosphate 5-kinase family. Adv. Enzyme Regul. 36, 115-140.
40. Lu, P.J., Hsu, A.L., Wang, D.S., Yan, H.Y., Yin, H.L., and Chen, C.S. (1998). Phosphoinositide 3-kinase in rat liver nuclei. Biochemistry 37, 5738-5745.
41. Malviya, A.N., and Rogue, P.J. (1998). "Tell me where is calcium bred": clarifying the roles of nuclear calcium. Cell 92, 17-23.
42. Maraldi, N.M., Cocco, L., Capitani, S., Mazzotti, G., Barnabei, O., and Manzoli, F.A. (1994). Lipid-dependent nuclear signalling: morphological and functional features. Adv. Enzyme Regul. 34, 129-143.
43. Maraldi, N.M., Zini, N., Ognibene, A., Martelli, A.M., Barbieri, M., Mazzotti, G., and Manzoli, F.A. (1995). Immunocytochemical detection of the intranuclear variations of phosphatidylinositol 4,5-bisphosphate amount associated with changes of activity and amount of phospholipase C beta 1 in cells exposed to mitogenic or differentiating agonists. Biol. Cell 83, 201-210.
44. Martelli, A.M., Gilmour, R.S., Bertagnolo, V., Neri, L.M., Manzoli, L., and Cocco, L. (1992). Nuclear localization and signalling activity of phosphoinositidase C beta in Swiss 3T3 cells. Nature 358, 242-245.
45. Matter, N., Ritz, M.F., Freyermuth, S., Rogue, P., and Malviya, A.N. (1993). Stimulation of nuclear protein kinase C leads to phosphorylation of nuclear inositol 1,4,5-trisphosphate receptor and accelerated calcium release by inositol 1,4,5-trisphosphate from isolated rat liver nuclei. J. Biol. Chem. 268, 732-736.
46. Matuoka, K., Fukami, K., Nakanishi, O., Kawai, S., and Takenawa, T. (1988). Mitogenesis in response to PDGF and bombesin abolished by microinjection of antibody to PIP2. Science 239, 640-643.
47. Meier, R., Alessi, D.R., Cron, P., Andjelkovic, M., and Hemmings, B.A. (1997). Mitogenic activation, phosphorylation, and nuclear translocation of protein kinase B beta. J. Biol. Chem. 272, 30491-30497.
48. Misteli, T., and Spector, D.L. (1996). Serine/threonine phosphatase 1 modulates the subnuclear distribution of pre-mRNA splicing factors. Mol. Biol. Cell 7, 1559-1572.
49. Misteli, T., Caceres, J.F., and Spector, D.L. (1997). The dynamics of a pre-mRNA splicing factor in living cells. Nature 387, 523-527.
50. Miyazawa, A., Umeda, M., Horikoshi, T., Yanagisawa, K., Yoshioka, T., and Inoue, K. (1988). Production and characterization of monoclonal antibodies that bind to phosphatidylinositol 4,5-bisphosphate. Mol. Immunol. 25, 1025-1031.
51. Mortillaro, M.J., Blencowe, B.J., Wei, X., Nakayasu, H., Du, L., Warren, S.L., Sharp, P.A., and Berezney, R. (1996). A hyperphosphorylated form of the large subunit of RNA polymerase II is associated with splicing complexes and the nuclear matrix. Proc. Natl. Acad. Sci. USA 93, 8253-8257.
52. Neugebauer, K.M., and Roth, M.B. (1997). Distribution of pre-mRNA splicing factors at sites of RNA polymerase II transcription. Genes & Dev. 11, 1148-1159.
53. Nickerson, J.A., Blencowe, B.J., and Penman, S. (1995). The architectural organization of nuclear metabolism. Int. Rev. Cytol. 162A, 67-123.
54. Onoda, K., and Yin, H.L. (1993). gCap39 is phosphorylated. Stimulation by okadaic acid and preferential association with nuclei. J. Biol. Chem. 268, 4106-4112.
55. Payrastre, B., Nievers, M., Boonstra, J., Breton, M., Verkleij, A.J., and Van Bergen en Henegouwen, P.M. (1992). A differential location of phosphoinositide kinases, diacylglycerol kinase, and phospholipase C in the nuclear matrix. J. Biol. Chem. 267, 5078-5084.
56. Pombo, A., and Cook, P.R. (1996). The localization of sites containing nascent RNA and splicing factors. Exp. Cell Res. 229, 201-203.
57. Rameh, L.E., Tolias, K.F., Duckworth, B.C., and Cantley, L.C. (1997). A new pathway for synthesis of phosphatidylinositol-4,5-bisphosphate (see comments). Nature 390, 192-196.
58. Roth, M.B., Murphy, C., and Gall, J.G. (1990). A monoclonal antibody that recognizes a phosphorylated epitope stains lampbrush chromosome loops and small granules in the amphibian germinal vesicle. J. Cell Biol, 111, 2217-2223.
59. Singer, R.H., and Green, M.R. (1997). Compartmentalization of eukaryotic gene expression: causes and effects. Cell 91, 291-294.
60. Smith, C.D., and Wells, W.W. (1983). Phosphorylation of rat liver nuclear envelopes. II. Characterization of in vitro lipid phosphorylation. J. Biol. Chem. 258, 9368-9373.
61. Spector, D.L. (1996). Nuclear organization and gene expression. Exp. Cell Res. 229, 189-197.
62. Spector, D.L., Fu, X.D., and Maniatis, T. (1991). Associations between distinct pre-mRNA splicing components and the cell nucleus. EMBO J. 10, 3467-3481.
63. Spector, D.L., Schrier, W.H., and Busch, H. (1983). Immunoelectron microscopic localization of snRNPs. Biol. Cell 49, 1-10.
64. Sun, B., Murray, N.R., and Fields, A.P. (1997). A role for nuclear phosphatidylinositol-specific phospholipase C in the G2/M phase transition. J. Biol. Chem. 272, 26313-26324.
65. Tolias, K.F., Rameh, L.E., Ishihara, H., Shibasaki, Y., Chen, J., Prestwich, G.D., Cantley, L.C., and Carpenter, C.L. (1998). Type I phosphatidylinositol-4-phosphate 5-kinases synthesize the novel lipids phosphatidylinositol 3,5-bisphosphate and phosphatidylinositol 5-phosphate. J. Biol. Chem. 273, 18040-18046.
66. Vann, L.R., Wooding, F.B., Irvine, R.F., and Divecha, N. (1997). Metabolism and possible compartmentalization of inositol lipids in isolated rat-liver nuclei. Biochem. J. 327, 569-576.
67. Wan, K.M., Nickerson, J.A., Krockmalnic, G., and Penman, S. (1994). The B1C8 protein is in the dense assemblies of the nuclear matrix and relocates to the spindle and pericentriolar filaments at mitosis. Proc. Natl. Acad. Sci. USA 91, 594-598.
68. York, J.D., and Majerus, P.W. (1994). Nuclear phosphatidylinositols decrease during S-phase of the cell cycle in HeLa cells. J. Biol. Chem. 269, 7847-7850.
69. York, J.D., Saffitz, J.E., and Majerus, P.W. (1994). Inositol polyphosphate 1-phosphatase is present in the nucleus and inhibits DNA synthesis. J. Biol. Chem. 269, 19992-19999.
70. Yu, H., Fukami, K., Watanabe, Y., Ozaki, C., and Takenawa, T. (1998). Phosphatidylinositol 4,5-bisphosphate reverses the inhibition of RNA transcription caused by histone H1. Eur. J. Biochem. 251, 281-287.
71. Zeng, C., Kim, E., Warren, S.L., and Berget, S.M. (1997). Dynamic relocation of transcription and splicing factors dependent upon transcriptional activity. EMBO J. 16, 1401-1412.
72. Zhang, X., Loijens, J.C., Boronenkov, I.V., Parker, G.J., Morris, F.A., Chen, J., Thum, O., Prestwich, G.D., Majerus, P.W., and Anderson, R.A. (1997). Phosphatidylinositol-4-phosphate 5-kinase isozymes catalyze the synthesis of 3-phosphate-containing phosphatidylinositol signaling molecules. J. Biol. Chem. 272, 17756-17761.
73. Zini, N., Martelli, A.M., Cocco, L., Manzoli, F.A., and Maraldi, N.M. (1993). Phosphoinositidase C isoforms are specifically localized in the nuclear matrix and cytoskeleton of Swiss 3T3 cells. Exp. Cell Res. 208, 257-269.
74. Zini, N., Ognibene, A., Bavelloni, A., Santi, S., Sabatelli, P., Baldini, N., Scotlandi, K., Serra, M., and Maraldi, N.M. (1996a). Cytoplasmic and nuclear localization sites of phosphatidylinositol 3-kinase in human osteosarcoma sensitive and multidrug-resistant Saos-2 cells. Histochem. Cell Biol. 106, 457-464.
75. Zini, N., Sabatelli, P., Faenza, I., Ognibene, A., and Maraldi, N.M. (1996b). Interleukin-1 alpha induces variations of the intranuclear amount of phosphatidylinositol 4,5-bisphosphate and phospholipase C beta 1 in human osteosarcoma Saos-2 cells. Histochem. J. 28, 495-504.