Inositol phosphate synthesis and the nuclear processes they affect

Current Opinion in Cell Biology

Volumn 22, Issue 3, 2010, Pages 365-373

  Monserrate, Jessica P ^a   York, John D ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GENE PRODUCT; INOSITOL 1,3,4 TRIPHOSPHATE 5 KINASE; INOSITOL PHOSPHATE; INOSITOL PHOSPHATE 6; INOSITOL PHOSPHATE 7; INOSITOL PHOSPHATE 8; INOSITOL TRISPHOSPHATE 3 KINASE; INOSITOL TRISPHOSPHATE 6 KINASE; MESSENGER RNA; PHOSPHATIDYLINOSITOL 4 PHOSPHATE KINASE; PHOSPHATIDYLINOSITOL KINASE; PHOSPHOTRANSFERASE; UNCLASSIFIED DRUG;

CHROMATIN ASSEMBLY AND DISASSEMBLY; CHROMOSOME SIZE; ENZYME ACTIVITY; ENZYME SYNTHESIS; EUKARYOTE; GENE CONTROL; GENE EXPRESSION; GENOMIC INSTABILITY; HUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; REVIEW; SEQUENCE HOMOLOGY; TELOMERE; TRANSCRIPTION REGULATION; ANIMAL; BIOSYNTHESIS; CELL NUCLEUS; GENE EXPRESSION REGULATION; METABOLISM; RNA TRANSPORT;

ANIMALS; CELL NUCLEUS; GENE EXPRESSION REGULATION; GENOMIC INSTABILITY; HUMANS; INOSITOL PHOSPHATES; RNA TRANSPORT; TELOMERE;

EUKARYOTA;

EID: 77954818764     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ceb.2010.03.006     Document Type: Review

References (91)

1. Saiardi A., Nagata E., Luo H.R., Sawa A., Luo X., Snowman A.M., Snyder S.H. Mammalian inositol polyphosphate multikinase synthesizes inositol 1,4,5-trisphosphate and an inositol pyrophosphate. Proc Natl Acad Sci U S A 2001, 98:2306-2311.
2. Nalaskowski M.M., Deschermeier C., Fanick W., Mayr G.W. The human homologue of yeast ArgRIII protein is an inositol phosphate multikinase with predominantly nuclear localization. Biochem J 2002, 366:549-556.
3. Fujii M., York J.D. A role for rat inositol polyphosphate kinases rIPK2 and rIPK1 in inositol pentakisphosphate and inositol hexakisphosphate production in rat-1 cells. J Biol Chem 2005, 280:1156-1164.
4. Otto J.C., Kelly P., Chiou S.T., York J.D. Alterations in an inositol phosphate code through synergistic activation of a G protein and inositol phosphate kinases. Proc Natl Acad Sci U S A 2007, 104:15653-15658.
5. Frederick J.P., Mattiske D., Wofford J.A., Megosh L.C., Drake L.Y., Chiou S.T., Hogan B.L., York J.D. An essential role for an inositol polyphosphate multikinase, Ipk2, in mouse embryogenesis and second messenger production. Proc Natl Acad Sci U S A 2005, 102:8454-8459.
6. Chang S.C., Miller A.L., Feng Y., Wente S.R., Majerus P.W. The human homolog of the rat inositol phosphate multikinase is an inositol 1,3,4,6-tetrakisphosphate 5-kinase. J Biol Chem 2002, 277:43836-43843.
7. Stevenson-Paulik J., Odom A.R., York J.D. Molecular and biochemical characterization of two plant inositol polyphosphate 6-/3-/5-kinases. J Biol Chem 2002, 277:42711-42718.
8. Seeds A.M., Sandquist J.C., Spana E.P., York J.D. A molecular basis for inositol polyphosphate synthesis in Drosophila melanogaster. J Biol Chem 2004, 279:47222-47232.
9. Resnick A.C., Snowman A.M., Kang B.N., Hurt K.J., Snyder S.H., Saiardi A. Inositol polyphosphate multikinase is a nuclear PI3-kinase with transcriptional regulatory activity. Proc Natl Acad Sci U S A 2005, 102:12783-12788.
10. Verbsky J.W., Chang S.C., Wilson M.P., Mochizuki Y., Majerus P.W. The pathway for the production of inositol hexakisphosphate in human cells. J Biol Chem 2005, 280:1911-1920.
11. Irvine R.F., Letcher A.J., Heslop J.P., Berridge M.J. The inositol tris/tetrakisphosphate pathway-demonstration of Ins(1,4,5)P3 3-kinase activity in animal tissues. Nature 1986, 320:631-634.
12. Choi K.Y., Kim H.K., Lee S.Y., Moon K.H., Sim S.S., Kim J.W., Chung H.K., Rhee S.G. Molecular cloning and expression of a complementary DNA for inositol 1,4,5-trisphosphate 3-kinase. Science 1990, 248:64-66.
13. Takazawa K., Perret J., Dumont J.E., Erneux C. Molecular cloning and expression of a new putative inositol 1,4,5-trisphosphate 3-kinase isoenzyme. Biochem J 1991, 278(Pt 3):883-886.
14. Abdullah M., Hughes P.J., Craxton A., Gigg R., Desai T., Marecek J.F., Prestwich G.D., Shears S.B. Purification and characterization of inositol-1,3,4-trisphosphate 5/6-kinase from rat liver using an inositol hexakisphosphate affinity column. J Biol Chem 1992, 267:22340-22345.
15. Wilson M.P., Majerus P.W. Isolation of inositol 1,3,4-trisphosphate 5/6-kinase, cDNA cloning and expression of the recombinant enzyme. J Biol Chem 1996, 271:11904-11910.
16. Yang X., Shears S.B. Multitasking in signal transduction by a promiscuous human Ins(3,4,5,6)P(4) 1-kinase/Ins(1,3,4)P(3) 5/6-kinase. Biochem J 2000, 351(Pt 3):551-555.
17. Connolly T.M., Bansal V.S., Bross T.E., Irvine R.F., Majerus P.W. The metabolism of tris- and tetraphosphates of inositol by 5-phosphomonoesterase and 3-kinase enzymes. J Biol Chem 1987, 262:2146-2149.
18. Damen J.E., Liu L., Rosten P., Humphries R.K., Jefferson A.B., Majerus P.W., Krystal G. The 145-kDa protein induced to associate with Shc by multiple cytokines is an inositol tetraphosphate and phosphatidylinositol 3,4,5-triphosphate 5-phosphatase. Proc Natl Acad Sci U S A 1996, 93:1689-1693.
19. York J.D., Odom A.R., Murphy R., Ives E.B., Wente S.R. A phospholipase C-dependent inositol polyphosphate kinase pathway required for efficient messenger RNA export. Science 1999, 285:96-100.
20. Ives E.B., Nichols J., Wente S.R., York J.D. Biochemical and functional characterization of inositol 1,3,4,5,6-pentakisphosphate 2-kinases. J Biol Chem 2000, 275:36575-36583.
21. Verbsky J.W., Wilson M.P., Kisseleva M.V., Majerus P.W., Wente S.R. The synthesis of inositol hexakisphosphate. Characterization of human inositol 1,3,4,5,6-pentakisphosphate 2-kinase. J Biol Chem 2002, 277:31857-31862.
22. Seeds A.M., Bastidas R.J., York J.D. Molecular definition of a novel inositol polyphosphate metabolic pathway initiated by inositol 1,4,5-trisphosphate 3-kinase activity in Saccharomyces cerevisiae. J Biol Chem 2005, 280:27654-27661.
23. Stevenson-Paulik J., Bastidas R.J., Chiou S.T., Frye R.A., York J.D. Generation of phytate-free seeds in Arabidopsis through disruption of inositol polyphosphate kinases. Proc Natl Acad Sci U S A 2005, 102:12612-12617.
24. Verbsky J., Lavine K., Majerus P.W. Disruption of the mouse inositol 1,3,4,5,6-pentakisphosphate 2-kinase gene, associated lethality, and tissue distribution of 2-kinase expression. Proc Natl Acad Sci U S A 2005, 102:8448-8453.
25. Sun Y., Thompson M., Lin G., Butler H., Gao Z., Thornburgh S., Yau K., Smith D.A., Shukla V.K. Inositol 1,3,4,5,6-pentakisphosphate 2-kinase from maize: molecular and biochemical characterization. Plant Physiol 2007, 144:1278-1291.
26. Leyman A., Pouillon V., Bostan A., Schurmans S., Erneux C., Pesesse X. The absence of expression of the three isoenzymes of the inositol 1,4,5-trisphosphate 3-kinase does not prevent the formation of inositol pentakisphosphate and hexakisphosphate in mouse embryonic fibroblasts. Cell Signal 2007, 19:1497-1504.
27. Voglmaier S.M., Bembenek M.E., Kaplin A.I., Dorman G., Olszewski J.D., Prestwich G.D., Snyder S.H. Purified inositol hexakisphosphate kinase is an ATP synthase: diphosphoinositol pentakisphosphate as a high-energy phosphate donor. Proc Natl Acad Sci U S A 1996, 93:4305-4310.
28. Saiardi A., Erdjument-Bromage H., Snowman A.M., Tempst P., Snyder S.H. Synthesis of diphosphoinositol pentakisphosphate by a newly identified family of higher inositol polyphosphate kinases. Curr Biol 1999, 9:1323-1326.
29. Schell M.J., Letcher A.J., Brearley C.A., Biber J., Murer H., Irvine R.F. PiUS (Pi uptake stimulator) is an inositol hexakisphosphate kinase. FEBS Lett 1999, 461:169-172.
30. Mulugu S., Bai W., Fridy P.C., Bastidas R.J., Otto J.C., Dollins D.E., Haystead T.A., Ribeiro A.A., York J.D. A conserved family of enzymes that phosphorylate inositol hexakisphosphate. Science 2007, 316:106-109.
31. Draskovic P., Saiardi A., Bhandari R., Burton A., Ilc G., Kovacevic M., Snyder S.H., Podobnik M. Inositol hexakisphosphate kinase products contain diphosphate and triphosphate groups. Chem Biol 2008, 15:274-286.
32. York S.J., Armbruster B.N., Greenwell P., Petes T.D., York J.D. Inositol diphosphate signaling regulates telomere length. J Biol Chem 2005, 280:4264-4269.
33. Saiardi A., Sciambi C., McCaffery J.M., Wendland B., Snyder S.H. Inositol pyrophosphates regulate endocytic trafficking. Proc Natl Acad Sci U S A 2002, 99:14206-14211.
34. Lin H., Fridy P.C., Ribeiro A.A., Choi J.H., Barma D.K., Vogel G., Falck J.R., Shears S.B., York J.D., Mayr G.W. Structural analysis and detection of biological inositol pyrophosphates reveal that the family of VIP/diphosphoinositol pentakisphosphate kinases are 1/3-kinases. J Biol Chem 2009, 284:1863-1872.
35. Choi J.H., Williams J., Cho J., Falck J.R., Shears S.B. Purification, sequencing, and molecular identification of a mammalian PP-InsP5 kinase that is activated when cells are exposed to hyperosmotic stress. J Biol Chem 2007, 282:30763-30775.
36. Fridy P.C., Otto J.C., Dollins D.E., York J.D. Cloning and characterization of two human VIP1-like inositol hexakisphosphate and diphosphoinositol pentakisphosphate kinases. J Biol Chem 2007, 282:30754-30762.
37. Padmanabhan U., Dollins D.E., Fridy P.C., York J.D., Downes C.P. Characterization of a selective inhibitor of inositol hexakisphosphate kinases: use in defining biological roles and metabolic relationships of inositol pyrophosphates. J Biol Chem 2009, 284:10571-10582.
38. Odom A.R., Stahlberg A., Wente S.R., York J.D. A role for nuclear inositol 1,4,5-trisphosphate kinase in transcriptional control. Science 2000, 287:2026-2029.
39. Saiardi A., Caffrey J.J., Snyder S.H., Shears S.B. Inositol polyphosphate multikinase (ArgRIII) determines nuclear mRNA export in Saccharomyces cerevisiae. FEBS Lett 2000, 468:28-32.
40. Dubois E., Messenguy F. Integration of the multiple controls regulating the expression of the arginase gene CAR1 of Saccharomyces cerevisiae in response to different nitrogen signals: role of Gln3p, ArgRp-Mcm1p, and Ume6p. Mol Gen Genet 1997, 253:568-580.
41. El Bakkoury M., Dubois E., Messenguy F. Recruitment of the yeast MADS-box proteins, ArgRI and Mcm1 by the pleiotropic factor ArgRIII is required for their stability. Mol Microbiol 2000, 35:15-31.
42. Yoon S., Govind C.K., Qiu H., Kim S.J., Dong J., Hinnebusch A.G. Recruitment of the ArgR/Mcm1p repressor is stimulated by the activator Gcn4p: a self-checking activation mechanism. Proc Natl Acad Sci U S A 2004, 101:11713-11718.
43. Xia H.J., Brearley C., Elge S., Kaplan B., Fromm H., Mueller-Roeber B. Arabidopsis inositol polyphosphate 6-/3-kinase is a nuclear protein that complements a yeast mutant lacking a functional ArgR-Mcm1 transcription complex. Plant Cell 2003, 15:449-463.
44. Caddick S.E., Harrison C.J., Stavridou I., Johnson S., Brearley C.A. A lysine accumulation phenotype of ScIpk2Delta mutant yeast is rescued by Solanum tuberosum inositol phosphate multikinase. Biochem J 2007, 403:381-389.
45. Guzinska K., Varghese R., Vancura A. Role of Plc1p in regulation of Mcm1p-dependent genes. FEMS Microbiol Lett 2009, 295:245-250.
46. Steger D.J., Haswell E.S., Miller A.L., Wente S.R., O'Shea E.K. Regulation of chromatin remodeling by inositol polyphosphates. Science 2003, 299:114-116.
47. Shen X., Xiao H., Ranallo R., Wu W.H., Wu C. Modulation of ATP-dependent chromatin-remodeling complexes by inositol polyphosphates. Science 2003, 299:112-114.
48. Desai P., Guha N., Galdieri L., Hadi S., Vancura A. Plc1p is required for proper chromatin structure and activity of the kinetochore in Saccharomyces cerevisiae by facilitating recruitment of the RSC complex. Mol Genet Genomics 2009, 281:511-523.
49. Letcher A.J., Schell M.J., Irvine R.F. Do mammals make all their own inositol hexakisphosphate?. Biochem J 2008, 416:263-270.
50. Sarmah B., Latimer A.J., Appel B., Wente S.R. Inositol polyphosphates regulate zebrafish left-right asymmetry. Dev Cell 2005, 9:133-145.
51. Iglesias N., Stutz F. Regulation of mRNP dynamics along the export pathway. FEBS Lett 2008, 582:1987-1996.
52. Moore M.J. From birth to death: the complex lives of eukaryotic mRNAs. Science 2005, 309:1514-1518.
53. Rout M.P., Aitchison J.D., Suprapto A., Hjertaas K., Zhao Y., Chait B.T. The yeast nuclear pore complex: composition, architecture, and transport mechanism. J Cell Biol 2000, 148:635-651.
54. Hodge C.A., Colot H.V., Stafford P., Cole C.N. Rat8p/Dbp5p is a shuttling transport factor that interacts with Rat7p/Nup159p and Gle1p and suppresses the mRNA export defect of xpo1-1 cells. EMBO J 1999, 18:5778-5788.
55. Alcazar-Roman A.R., Tran E.J., Guo S., Wente S.R. Inositol hexakisphosphate and Gle1 activate the DEAD-box protein Dbp5 for nuclear mRNA export. Nat Cell Biol 2006, 8:711-716.
56. Weirich C.S., Erzberger J.P., Flick J.S., Berger J.M., Thorner J., Weis K. Activation of the DExD/H-box protein Dbp5 by the nuclear-pore protein Gle1 and its coactivator InsP6 is required for mRNA export. Nat Cell Biol 2006, 8:668-676.
57. Rocak S., Linder P. DEAD-box proteins: the driving forces behind RNA metabolism. Nat Rev Mol Cell Biol 2004, 5:232-241.
58. Zhao J., Jin S.B., Bjorkroth B., Wieslander L., Daneholt B. The mRNA export factor Dbp5 is associated with Balbiani ring mRNP from gene to cytoplasm. EMBO J 2002, 21:1177-1187.
59. Estruch F., Cole C.N. An early function during transcription for the yeast mRNA export factor Dbp5p/Rat8p suggested by its genetic and physical interactions with transcription factor IIH components. Mol Biol Cell 2003, 14:1664-1676.
60. Tran E.J., Zhou Y., Corbett A.H., Wente S.R. The DEAD-box protein Dbp5 controls mRNA export by triggering specific RNA:protein remodeling events. Mol Cell 2007, 28:850-859.
61. Dossani Z.Y., Weirich C.S., Erzberger J.P., Berger J.M., Weis K. Structure of the C-terminus of the mRNA export factor Dbp5 reveals the interaction surface for the ATPase activator Gle1. Proc Natl Acad Sci U S A 2009, 106:16251-16256.
62. Bolger T.A., Folkmann A.W., Tran E.J., Wente S.R. The mRNA export factor Gle1 and inositol hexakisphosphate regulate distinct stages of translation. Cell 2008, 134:624-633.
63. Gross T., Siepmann A., Sturm D., Windgassen M., Scarcelli J.J., Seedorf M., Cole C.N., Krebber H. The DEAD-box RNA helicase Dbp5 functions in translation termination. Science 2007, 315:646-649.
64. Macbeth M.R., Schubert H.L., Vandemark A.P., Lingam A.T., Hill C.P., Bass B.L. Inositol hexakisphosphate is bound in the ADAR2 core and required for RNA editing. Science 2005, 309:1534-1539.
65. Smith G.C., Jackson S.P. The DNA-dependent protein kinase. Genes Dev 1999, 13:916-934.
66. Walker J.R., Corpina R.A., Goldberg J. Structure of the Ku heterodimer bound to DNA and its implications for double-strand break repair. Nature 2001, 412:607-614.
67. Hanakahi L.A., Bartlet-Jones M., Chappell C., Pappin D., West S.C. Binding of inositol phosphate to DNA-PK and stimulation of double-strand break repair. Cell 2000, 102:721-729.
68. Cheung J.C., Salerno B., Hanakahi L.A. Evidence for an inositol hexakisphosphate-dependent role for Ku in mammalian nonhomologous end joining that is independent of its role in the DNA-dependent protein kinase. Nucleic Acids Res 2008, 36:5713-5726.
69. Hanakahi L.A., West S.C. Specific interaction of IP6 with human Ku70/80, the DNA-binding subunit of DNA-PK. EMBO J 2002, 21:2038-2044.
70. Shrivastav M., De Haro L.P., Nickoloff J.A. Regulation of DNA double-strand break repair pathway choice. Cell Res 2008, 18:134-147.
71. Ma Y., Lieber M.R. Binding of inositol hexakisphosphate (IP6) to Ku but not to DNA-PKcs. J Biol Chem 2002, 277:10756-10759.
72. Saiardi A., Resnick A.C., Snowman A.M., Wendland B., Snyder S.H. Inositol pyrophosphates regulate cell death and telomere length through phosphoinositide 3-kinase-related protein kinases. Proc Natl Acad Sci U S A 2005, 102:1911-1914.
73. Ponnusamy S., Alderson N.L., Hama H., Bielawski J., Jiang J.C., Bhandari R., Snyder S.H., Jazwinski S.M., Ogretmen B. Regulation of telomere length by fatty acid elongase 3 in yeast. Involvement of inositol phosphate metabolism and Ku70/80 function. J Biol Chem 2008, 283:27514-27524.
74. Feoktistova A., McCollum D., Ohi R., Gould K.L. Identification and characterization of Schizosaccharomyces pombe asp1(+), a gene that interacts with mutations in the Arp2/3 complex and actin. Genetics 1999, 152:895-908.
75. Mullaney E.J., Ullah A.H. The term phytase comprises several different classes of enzymes. Biochem Biophys Res Commun 2003, 312:179-184.
76. Lee Y.S., Mulugu S., York J.D., O'Shea E.K. Regulation of a cyclin-CDK-CDK inhibitor complex by inositol pyrophosphates. Science 2007, 316:109-112.
77. O'Neill E.M., Kaffman A., Jolly E.R., O'Shea E.K. Regulation of PHO4 nuclear localization by the PHO80-PHO85 cyclin-CDK complex. Science 1996, 271:209-212.
78. Kaffman A., Herskowitz I., Tjian R., O'Shea E.K. Phosphorylation of the transcription factor PHO4 by a cyclin-CDK complex, PHO80-PHO85. Science 1994, 263:1153-1156.
79. Lee Y.S., Huang K., Quiocho F.A., O'Shea E.K. Molecular basis of cyclin-CDK-CKI regulation by reversible binding of an inositol pyrophosphate. Nat Chem Biol 2008, 4:25-32.
80. Schneider K.R., Smith R.L., O'Shea E.K. Phosphate-regulated inactivation of the kinase PHO80-PHO85 by the CDK inhibitor PHO81. Science 1994, 266:122-126.
81. Ogawa N., Noguchi K., Sawai H., Yamashita Y., Yompakdee C., Oshima Y. Functional domains of Pho81p, an inhibitor of Pho85p protein kinase, in the transduction pathway of Pi signals in Saccharomyces cerevisiae. Mol Cell Biol 1995, 15:997-1004.
82. Ogawa N., Noguchi K., Yamashita Y., Yasuhara T., Hayashi N., Yoshida K., Oshima Y. Promoter analysis of the PHO81 gene encoding a 134kDa protein bearing ankyrin repeats in the phosphatase regulon of Saccharomyces cerevisiae. Mol Gen Genet 1993, 238:444-454.
83. Irvine R.F. Nuclear lipid signalling. Nat Rev Mol Cell Biol 2003, 4:349-360.
84. Martelli A.M., Fala F., Faenza I., Billi A.M., Cappellini A., Manzoli L., Cocco L. Metabolism and signaling activities of nuclear lipids. Cell Mol Life Sci 2004, 61:1143-1156.
85. Mellman D.L., Gonzales M.L., Song C., Barlow C.A., Wang P., Kendziorski C., Anderson R.A. A PtdIns4,5P2-regulated nuclear poly(A) polymerase controls expression of select mRNAs. Nature 2008, 451:1013-1017.
86. Huang Y.H., Grasis J.A., Miller A.T., Xu R., Soonthornvacharin S., Andreotti A.H., Tsoukas C.D., Cooke M.P., Sauer K. Positive regulation of Itk PH domain function by soluble IP4. Science 2007, 316:886-889.
87. Illies C., Gromada J., Fiume R., Leibiger B., Yu J., Juhl K., Yang S.N., Barma D.K., Falck J.R., Saiardi A., et al. Requirement of inositol pyrophosphates for full exocytotic capacity in pancreatic beta cells. Science 2007, 318:1299-1302.
88. Bhandari R., Juluri K.R., Resnick A.C., Snyder S.H. Gene deletion of inositol hexakisphosphate kinase 1 reveals inositol pyrophosphate regulation of insulin secretion, growth, and spermiogenesis. Proc Natl Acad Sci U S A 2008, 105:2349-2353.
89. Saiardi A., Bhandari R., Resnick A.C., Snowman A.M., Snyder S.H. Phosphorylation of proteins by inositol pyrophosphates. Science 2004, 306:2101-2105.
90. Bhandari R., Saiardi A., Ahmadibeni Y., Snowman A.M., Resnick A.C., Kristiansen T.Z., Molina H., Pandey A., Werner J.K., Juluri K.R., et al. Protein pyrophosphorylation by inositol pyrophosphates is a posttranslational event. Proc Natl Acad Sci U S A 2007, 104:15305-15310.
91. Azevedo C., Burton A., Ruiz-Mateos E., Marsh M., Saiardi A. Inositol pyrophosphate mediated pyrophosphorylation of AP3B1 regulates HIV-1 Gag release. Proc Natl Acad Sci U S A 2009, 106:21161-21166.