Molecular basis for the integration of inositol phosphate signaling pathways via human ITPK1

Advances in Enzyme Regulation

Volumn 49, Issue 1, 2009, Pages 87-96

  Shears, Stephen B ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHLORIDE CHANNEL; INOSITOL 1,4,5-TRISPHOSPHATE 3-KINASE; INOSITOL PHOSPHATE; INOSITOL TRISPHOSPHATE 3 KINASE; PHOSPHOLIPASE C; PHOSPHOTRANSFERASE;

ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; CYTOPLASM VESICLE; GENETICS; HUMAN; METABOLISM; PH; PHYSIOLOGY; SIGNAL TRANSDUCTION;

CHLORIDE CHANNELS; CYTOPLASMIC VESICLES; HUMANS; HYDROGEN-ION CONCENTRATION; INOSITOL PHOSPHATES; MOLECULAR STRUCTURE; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); SIGNAL TRANSDUCTION; TYPE C PHOSPHOLIPASES;

EID: 66749108755     PISSN: 00652571     EISSN: None     Source Type: Book Series    
DOI: 10.1016/j.advenzreg.2008.12.008     Document Type: Article

References (80)

1. Abdullah M., Hughes P.J., Craxton A., Gigg R., Desai T., Marecek J.F., et al. Purification and characterization of inositol 1,3,4-trisphosphate 5/6-kinase from rat liver using an inositol hexakisphosphate affinity column. J Biol Chem 267 (1992) 22340-22345
2. Adelt S., Plettenburg O., Dallmann G., Ritter F.P., Shears S.B., Altenbach H.-J., et al. Regiospecific phosphohydrolases from dictyostelium as tools for the chemoenzymatic synthesis of the enantiomers d-myo-inositol 1,2,4-trisphosphate and d-myo-inositol 2,3,6-trisphosphate: non-physiological, potential analogues of biologically active d-myo-inositol 1,3,4-trisphosphate. Bioorg Med Chem Lett 11 (2001) 2705-2708
3. Alcazar-Roman A.R., and Wente S.R. Inositol polyphosphates: a new frontier for regulating gene expression. Chromosoma 117 (2008) 1-13
4. Barg S., Huang P., Eliasson L., Nelson D.J., Obermüller S., Rorsman P., et al. Priming of insulin granules for exocytosis by granular chloride uptake and acidification. J Cell Sci 114 (2001) 2145-2154
5. Barker C.J., Wong N.S., Maccallum S.M., Hunt P.A., Michell R.H., and Kirk C.J. The interrelationships of the inositol phosphates formed in WRK-1 stimulated rat mammary tumour cells. Biochem J 286 (1992) 469-474
6. Batty I.H., Currie R.A., and Downes C.P. Evidence for a model of integrated inositol phospholipid pools implies an essential role for lipid transport in the maintenance of receptor-mediated phospholipase C activity in 1321N1 cells. Biochem J 330 (1998) 1069-1077
7. Batty I.H., and Downes C.P. The inhibition of phosphoinositide synthesis and muscarinic-receptor-mediated phospholipase C activity by Li+ as secondary selective consequences of inositol depletion in 1321N1 cells. Biochem J 297 (1994) 529-537
8. Bliss T.V., and Collingridge G.L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361 (1993) 31-39
9. Brearley C.A., and Hanke D.E. Metabolic evidence for the order of addition of individual phosphate esters to the myo-inositol moiety of inositol hexakisphosphate in the duckweed Spirodela polrhiza L. Biochem J 314 (1996) 227-233
10. Chamberlain P.P., Qian X., Stiles A.R., Cho J., Jones D.H., Lesley S.A., et al. Integration of inositol phosphate signaling pathways via human ITPK1. J Biol Chem 282 (2007) 28117-28125
11. Chang S.-C., Miller A.L., Feng Y., Wente S.R., and Majerus P.W. The human homologue of the rat inositol phosphate multikinase is an inositol 1,3,4,6-tetrakisphosphate 5-kinase. J Biol Chem 277 (2002) 43836-43843
12. Clapham D. How to lose your hippocampus by working on chloride channels. Neuron 29 (2001) 1-6
13. Claud E.C., Lu J., Wang X.Q., Abe M., Petrof E.O., Sun J., et al. Platelet-activating factor induced chloride channel activation is associated with intracellular acidosis and apoptosis of intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol 294 (2008) G1191-G1200
14. Field J., Wilson M.P., Mai Z., Majerus P.W., and Samuelson J. An Entamoeba histolytica inositol 1,3,4-trisphosphate 5/6-kinase has a novel 3-kinase activity. Mol Biochem Parasitol 108 (2000) 119-123
15. Fuller C.M., Kovacs G., Anderson S.J., and Benos D.J. The CLCAs: proteins with ionchannel, cell adhesion and tumor suppressor functions. Adv Exp Med Biol 558 (2005) 83-102
16. Gentzsch M., Cui L., Mengos A., Chang X.B., Chen J.H., and Riordan J.R. The PDZ-binding chloride channel ClC-3B localizes to the Golgi and associates with cystic fibrosis transmembrane conductance regulator-interacting PDZ proteins. J Biol Chem 278 (2003) 6440-6449
17. Hara-Chikuma M., Yang B., Sonawane N.D., Sasaki S., Uchida S., and Verkman A.S. ClC-3 chloride channels facilitate endosomal acidification and chloride accumulation. J Biol Chem 280 (2005) 1241-1247
18. Ho M.W.Y., Yang X., Carew M.A., Zhang T., Hua L., Kwon Y.-U., et al. Regulation of Ins(3456)P4 signaling by a reversible kinase/phosphatase. Curr Biol 12 (2002) 477-482
19. 4. J Biol Chem 276 (2001) 18673-18680
20. Ho M.W.Y., and Shears S.B. Regulation of calcium-activated chloride channels by inositol 3,4,5,6-tetrakisphosphate. In: Fuller C.M. (Ed). "Current Topics in Membranes" (2002), Academic Press, London 345-363
21. Hunter T. When is a lipid kinase not a lipid kinase? When it is a protein kinase. Cell 83 (1995) 1-4
22. Hunyady L., Baukal A.J., Guillemette G., Balla T., and Catt K.J. Metabolism of inositol-1,3,4,6-tetrakisphosphate to inositol pentakisphosphate in adrenal glomerulosa cells. Biochem Biophys Res Commun 157 (1988) 1247-1252
23. Irvine R.F., and Schell M. Back in the water: the return of the inositol phosphates. Nat Rev Mol Cell Biol 2 (2001) 327-338
24. Ismailov Fuller II C.M., Berdiev B.K., Shlyonsky V.G., Benos D.J., and Barrett K.E. A biologic function for an "orphan" messenger: d-myo-inositol 3,4,5,6-tetrakisphosphate selectively blocks epithelial calcium-activated chloride current. Proc Nat Acad Sci USA 93 (1996) 10505-10509
25. Jentsch T.J. CLC chloride channels and transporters: from genes to protein structure, pathology and physiology. Crit Rev Biochem Mol Biol 43 (2008) 3-36
26. Jentsch TJ, Günther W. Chloride channels: an emerging molecular picture. Bioessays 1996;19:117-126.
27. Josefsen L., Bohn L., Sorensen M.B., and Rasmussen S.K. Characterization of a multifunctional inositol phosphate kinase from rice and barley belonging to the ATP-grasp superfamily. Gene 397 (2007) 114-125
28. Kilpatrick E.D., and Robertson R.P. Differentiation between glucose-induced desensitization of insulin secretion and b-cell exhaustion in the HIT-T15 cell line. Diabetes 47 (1998) 606-611
29. Leyman A., Pouillon V., Bostan A., Schurmans S., Erneux C., and 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 Signalling 19 (2007) 1497-1504
30. Li G., Pralong W.-F., Pittet D., Mayr G.W., Schlegel W., and Woolheim C.B. Inositol tetrakisphosphate isomers and elevation of cytosolic calcium in vasopressin-stimulated insulin-secreting RINm5F cells. J Biol Chem 267 (1992) 4349-4356
31. Lisal J., and Maduke M. The ClC-0 chloride channel is a 'broken' Cl(-)/H(+) antiporter. Nat Struct Mol Biol 15 (2008) 805-810
32. Majerus P.W., Zou J., Marjanovic J., Kisseleva M.V., and Wilson M.P. The role of inositol signaling in the control of apoptosis. Adv Enzym Regul 48 (2008) 10-17
33. Mao J., Chen L., Xu B., Wang L., Li H., Guo J., et al. Suppression of ClC-3 channel expression reduces migration of nasopharyngeal carcinoma cells. Biochem Pharmacol 75 (2008) 1706-1716
34. McConnell F.M., Stephens L.R., and Shears S.B. Multiple isomers of inositol pentakisphosphate in Epstein-Barr virus transformed T5-1 lymphocytes. Identification of inositol 1,3,4,5,6-pentakisphosphate, d-inositol 1,2,4,5,6-pentakisphosphate and l-inositol 1,2,4,5,6-pentakisphosphate. Biochem J 280 (1991) 323-329
35. Menniti F.S., Oliver K.G., Nogimori K., Obie J.F., Shears S.B., and Putney Jr. J.W. Origins of myo-inositol tetrakisphosphates in agonist-stimulated rat pancreatoma cells. Stimulation by bombesin of myo-inositol 1,3,4,5,6-pentakisphosphate breakdown to myo-inositol 3,4,5,6-tetrakisphosphate. J Biol Chem 265 (1990) 11167-11176
36. Meyer J., Sturis J., Katschinski M., Arnold R., Göke B., and Byrne M.M. Acute hyperglycemia alters the ability of the normal b-cell to sense and respond to glucose. Am J Physiol Endocrinol Metab 282 (2002) E917-E922
37. Miller G.J., and Hurley J.H. Crystal structure of the catalytic core of inositol 1,4,5-trisphosphate 3-kinase. Mol Cell 15 (2004) 703-711
38. Miller G.J., Wilson M.P., Majerus P.W., and Hurley J.H. Specificity determinants in inositol polyphosphate synthesis: crystal structure of inositol 1,3,4-trisphosphate 5/6-kinase. Mol Cell 18 (2005) 201-212
39. 4. through its modulation of ClC-3 function. Curr Biol 18 (2008) 1600-1605
40. Moreland J.G., Davis A.P., Bailey G., Nauseef W.M., and Lamb F.S. Anion channels, including ClC-3, are required for normal neutrophil oxidative function, phagocytosis, and transendothelial migration. J Biol Chem 281 (2006) 12277-12288
41. Mundhenk L., Alfalah M., Elble R.C., Pauli B.U., Naim H.Y., and Gruber A.D. Both cleavage products of the mCLCA3 protein are secreted soluble proteins. J Biol Chem 281 (2006) 30072-30080
42. +)-ATPases - nature's most versatile proton pumps. Nature Rev Mol Cell Biol 3 (2002) 94-103
43. Odom A.R., Stahlberg A., Wente S.R., and York J.D. A role for nuclear inositol 1,4,5-trisphosphate kinase in transcriptional control. Science 287 (2000) 2026-2029
44. Okamoto F., Kajiya H., Toh K., Uchida S., Yoshikawa M., Sasaki S., et al. Intracellular ClC-3 chloride channels promote bone resorption in vitro through organelle acidification in mouse osteoclasts. Am J Physiol Cell Physiol 294 (2008) C693-C701
45. 3 and osmotic regulation. Biochem J 335 (1998) 671-679
46. Petersen O.H. Stimulus-secretion coupling: cytoplasmic calcium signals and the control of ion channels in exocrine acinar cells. J Physiol (London) 448 (1992) 1-51
47. Picollo A., and Pusch M. Chloride/proton antiporter activity of mammalian CLC proteins ClC-4 and ClC-5. Nature 436 (2005) 420-423
48. 4 1-kinase is not a protein kinase. Biochem J 389 (2005) 389-395
49. Qin Z.X., Chen Q.J., Tong Z., and Wang X.C. The Arabidopsis inositol 1,3,4-trisphosphate 5/6 kinase, AtItpk-1, is involved in plant photomorphogenesis under red light conditions, possibly via interaction with COP9 signalosome. Plant Physiol Biochem 43 (2005) 947-954
50. Renström E., Ivarsson R., and Shears S.B. Ins(3,4,5,6)P4 inhibits insulin granule acidification and fusogenic potential. J Biol Chem 277 (2002) 26717-26720
51. 4 is not a physiologic substrate. FEBS Lett 580 (2006) 324-330
52. Robinson N.C., Huang P., Kaetzel M.A., Lamb F.S., and Nelson D.J. Identification of an N-terminal amino acid of the CLC-3 chloride channel critical in phosphorylation-dependent activation of a CaMKII-activated chloride current. J Physiol 556 (2004) 353-368
53. Rudolf M.T., Dinkel C., Traynor-Kaplan A.E., and Schultz C. Antagonists of myo-inositol 3,4,5,6-tetrakisphosphate allow repeated epithelial chloride secretion. Bioorgan Med Chem 11 (2003) 3315-3329
54. Saiardi A., Caffrey J.J., Snyder S.H., and Shears S.B. Inositol polyphosphate multikinase (ArgRIII) determines nuclear mRNA export in Saccharomyces cerevisiae. FEBS Lett 468 (2000) 28-32
55. Saiardi A., Erdjument-Bromage H., Snowman A., Tempst P., and Snyder S.H. Synthesis of diphosphoinositol pentakisphosphate by a newly identified family of higher inositol polyphosphate kinases. Curr Biol 9 (1999) 1323-1326
56. Scheel O., Zdebik A.A., Lourdel S., and Jentsch T.J. Voltage-dependent electrogenic chloride/proton exchange by endosomal CLC proteins. Nature 436 (2005) 424-427
57. Schell M.J., Letcher A.J., Brearley C.A., Biber J., Murer H., and Irvine R.F. PiUS (Pi uptake stimulator) is an inositol hexakisphosphate kinase. FEBS Lett 461 (1999) 169-172
58. Shears S.B. The pathway of myo-inositol 1,3,4-trisphosphate phosphorylation in liver. Identification of myo-inositol 1,3,4-trisphosphate 6-kinase, myo-inositol 1,3,4-trisphosphate 5-kinase, and myo-inositol 1,3,4,6-tetrakisphosphate 5-kinase. J Biol Chem 264 (1989) 19879-19886
59. Shi J., Wang H., Wu Y., Hazebroek J., Meeley R.B., and Ertl D.S. The maize low-phytic acid mutant Ipa2 is caused by mutation in an inositol phosphate kinase gene. Plant Physiol 131 (2003) 507-515
60. Stephens L.R., Hawkins P.T., Barker C.J., and Downes C.P. Synthesis of myo-inositol 1,3,4,5,6-pentakisphosphate from inositol phosphates generated by receptor activation. Biochem J 253 (1988) 721-733
61. Stiles A.R., Qian X., Shears S.B., and Grabau E.A. Metabolic and signaling properties of an Itpk gene family in Glycine max. FEBS Lett 582 (2008) 1853-1858
62. Stobrawa S.M., Breiderhoff T., Takamori S., Engel D., Schweizer M., Zdebik A.A., et al. Disruption of ClC-3, a chloride channel expressed on synaptic vesicles, leads to a loss of hippocampus. Neuron 29 (2001) 185-196
63. Sun Y., Wilson M.P., and Majerus P.W. Inositol 1,3,4-trisphosphate 5/6-kinase associates with the COP9 signalosome by binding to CSN1. J Biol Chem 277 (2002) 45759-45764
64. Suzuki M., Tanaka K., Kuwano M., and Yoshida K.T. Expression pattern of inositol phosphate-related enzymes in rice (Oryza sativa L.): implications for the phytic acid biosynthetic pathway. Gene 405 (2007) 55-64
65. Sweetman D., Stavridou I., Johnson S., Green P., Caddick S.E., and Brearley C.A. Arabidopsis thaliana inositol 1,3,4-trisphosphate 5/6-kinase 4 (AtITPK4) is an outlier to a family of ATP-grasp fold proteins from Arabidopsis. FEBS Lett 581 (2007) 4165-4171
66. 2+ in agonist-stimulated pancreatic acini of the rat. Biochem J 242 (1987) 289-292
67. Verbsky J.W., Chang S.C., Wilson M.P., Mochizuki Y., and Majerus P.W. The pathway for the production of inositol hexakisphosphate in human cells. J Biol Chem 280 (2005) 1911-1920
68. Wang X.Q., Deriy L.V., Foss S., Huang P., Lamb F.S., Kaetzel M.A., et al. CLC-3 channels modulate excitatory synaptic transmission in hippocampal neurons. Neuron 52 (2006) 321-333
69. Weylandt K.H., Nebrig M., Jansen-Rosseck N., Amey J.S., Carmena D., Wiedenmann B., et al. ClC-3 expression enhances etoposide resistance by increasing acidification of the late endocytic compartment. Mol Cancer Ther 6 (2007) 979-986
70. Wilcox R.A., Safrany S.T., Lampe D., Mills S.J., Nahorski S.R., and Potter B.V.L. Modification at C2 of myo-inositol 1,4,5-trisphosphate produces inositol trisphosphates and tetrakisphosphates with potent biological activities. Eur J Biochem 223 (1994) 115-124
71. Wilson M.P., and Majerus P.W. Characterization of a cDNA encoding Arabidopsis thaliana inositol 1,3,4-trisphosphate 5/6-kinase. Biochem Biophys Res Commun 232 (1997) 678-681
72. Wilson M.P., Sun Y., Cao L., and Majerus P.W. Inositol 1,3,4-trisphosphate 5/6-kinase is a protein kinase that phosphorylates the transcription factors c-jun and ATF-2. J Biol Chem 276 (2001) 40998-41004
73. Wong N.S., Barker C.J., Morris A.J., Craxton A., Kirk C.J., and Michell R.H. The inositol phosphates of WRK1 rat mammary tumour cells. Biochem J 286 (1992) 459-468
74. Xie W., Kaetzel M.A., Bruzik K.S., Dedman J.R., Shears S.B., and Nelson D.J. Inositol 3,4,5,6-tetrakisphosphate inhibits the calmodulin-dependent protein kinase II-activated chloride conductance inT84 colonic epithelial cells. J Biol Chem 271 (1996) 14092-14097
75. 4 and protein phosphatases. J Physiol (London) 510 (1998) 661-673
76. Yang L., Reece J., Gabriel S.E., and Shears S.B. Apical localization of ITPK1 enhances its ability to be a modifier gene product in a murine tracheal cell model of cystic fibrosis. J Cell Sci 119 (2006) 1320-1328
77. Yang X., and Shears S.B. Multitasking in signal transduction by a promiscuous human Ins(3,4,5,6)P4 1-Kinase/Ins(1,3,4)P3 5/6-kinase. Biochem J 351 (2000) 551-555
78. York J.D. Regulation of nuclear processes by inositol polyphosphates. Biochim Biophys Acta 1761 (2006) 552-559
79. Zhao Z., Li X., Hao J., Winston J.H., and Weinman S.A. The ClC-3 chloride transport protein traffics through the plasma membrane via interaction of an N-terminal dileucine cluster with clathrin. J Biol Chem 282 (2007) 29022-29031
80. Zonia L., Cordeiro S., Tupý J., and Feijó J.A. Oscillatory chloride efflux at the pollen tube apex has a role in growth and cell volume regulation and is targeted by inositol 3,4,5,6-tetrakisphosphate. Plant Cell 14 (2002) 2233-2249