The enzymes of human diphosphoinositol polyphosphate metabolism

FEBS Journal

Volumn 281, Issue 1, 2014, Pages 14-33

  Thomas, Mark P ^a   Potter, Barry V L ^a  

^a University of Bath   (United Kingdom)

Author keywords

diphosphoinositol polyphosphate phosphohydrolase; inositol hexakisphosphate and diphosphoinositol pentakisphosphate kinase; inositol hexakisphosphate kinase; inositol pyrophosphate

Indexed keywords

BETA INTERFERON; CASEIN KINASE II; DIPHOSPHOINOSITOL PENTAKISPHOSPHATE KINASE; DIPHOSPHOINOSITOL POLYPHOSPHATE; DIPHOSPHOINOSITOL POLYPHOSPHATE PHOSPHOHYDROLASE; GLYCOGEN SYNTHASE KINASE 3; HEAT SHOCK PROTEIN 90; INOSITOL HEXAKISPHOSPHATE KINASE; INOSITOL PHOSPHATE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE; PHOSPHORIC ACID DERIVATIVE; PHYTIC ACID; PLECKSTRIN; PROTEIN P53; RAB PROTEIN; RIBOSOME PROTEIN; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 2; UNCLASSIFIED DRUG;

APOPTOSIS; BINDING KINETICS; CATALYSIS; CELL MEMBRANE; DIABETES MELLITUS; ENZYME ACTIVITY; ENZYME BINDING; ENZYME METABOLISM; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; EXOCYTOSIS; HUMAN; INFECTION; MEMBRANE TRANSPORT; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN TRANSPORT; REVIEW; UBIQUITINATION;

EID: 84891827868     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12575     Document Type: Review

References (139)

1. Mayr GW, Radenberg T, Thiel U, Vogel G, &, Stephens LR, (1992) Phosphoinositol diphosphates: non-enzymic formation in vitro and occurrence in vivo in the cellular slime mold Dictyostelium. Carbohydr Res 234, 247-262.
2. Menniti FS, Miller RN, Putney JW Jr, &, Shears SB, (1993) Turnover of inositol polyphosphate pyrophosphates in pancreatoma cells. J Biol Chem 268, 3850-3856.
3. Stephens L, Radenberg T, Thiel U, Vogel G, Khoo K-H, Dell A, Jackson TR, Hawkins PT, &, Mayr GW, (1993) The detection, purification, structural characterization, and metabolism of diphosphoinositol pentakisphosphate(s) and bisdiphosphoinositol tetrakisphosphate(s). J Biol Chem 268, 4009-4015.
4. Saiardi A, Resnick AC, Snowman AM, Wendland B, &, Snyder SH, (2005) Inositol pyrophosphates regulate cell death and telomere length through phosphoinositide 3-kinase-related protein kinases. Proc Natl Acad Sci USA 102, 1911-1914.
5. York SJ, Armbruster BN, Greenwell P, Petes TD, &, York JD, (2005) Inositol diphosphate signaling regulates telomere length. J Biol Chem 280, 4264-4269.
6. Lee Y-S, Mulugu S, York JD, &, O'Shea EK, (2007) Regulation of a cyclin-CDK-CDK inhibitor complex by inositol pyrophosphates. Science 316, 109-112.
7. Lee Y-S, Huang K, Quiocho FA, &, O'Shea EK, (2008) Molecular basis of cyclin-CDK-CKI regulation by reversible binding of an inositol pyrophosphate. Nat Chem Biol 4, 25-32.
8. 8') is selectively activated by hyperosmotic stress. J Biol Chem 279, 43378-43381.
9. Safrany ST, (2004) Protocols for regulation and study of diphosphoinositol polyphosphates. Mol Pharmacol 66, 1585-1591.
10. Choi JH, Williams J, Cho J, Falck JR, &, Shears SB, (2007) Purification, sequencing, and molecular identification of a mammalian PP-InsP5 kinase that is activated when cells are exposed to hyperosmotic stress. J Biol Chem 282, 30763-30775.
11. +-selective channels gated by, inositol polyphosphate. J Biol Chem 269, 17826-17832.
12. Ye W, Ali N, Bembenek ME, Shears SB, &, Lafer EM, (1995) Inhibition of clathrin assembly by high affinity binding of specific inositol polyphosphates to the synapse-specific clathrin assembly protein AP-3. J Biol Chem 270, 1564-1568.
13. Morrison BH, Bauer JA, Kalvakolanu DV, &, Lindner DJ, (2001) Inositol hexakisphosphate kinase 2 mediates growth suppressive and apoptotic effects of interferon-β in ovarian carcinoma cells. J Biol Chem 276, 24965-24970.
14. Nagata E, Luo HR, Saiardi A, Bae B-I, Suzuki N, &, Snyder SH, (2005) Inositol hexakisphosphate kinase-2, a physiologic mediator of cell death. J Biol Chem 280, 1634-1640.
15. Luo HR, Saiardi A, Nagata E, Ye K, Yu H, Jung TS, Luo X, Jain S, Sawa A, &, Snyder SH, (2003) Inositol pyrophosphates mediate chemotaxis in Dictyostelium via pleckstrin homology domain-PtdIns(3,4,5)P3 interactions. Cell 114, 559-572.
16. 3 for polyphosphoinositide-binding domains. Biochem J 453, 413-426.
17. Bennett M, Onnebo SMN, Azevedo C, &, Saiardi A, (2006) Inositol pyrophosphates: metabolism and signaling. Cell Mol Life Sci 63, 552-564.
18. Barker CJ, Illies C, Gaboardi GC, &, Berggren P-O, (2009) Inositol pyrophosphates: structure, enzymology and function. Cell Mol Life Sci 66, 3851-3871.
19. Burton A, Hu X, &, Saiardi A, (2009) Are inositol pyrophosphates signalling molecules? J Cell Physiol 220, 8-15.
20. Shears SB, (2009) Diphosphoinositol polyphosphates: metabolic messengers? Mol Pharmacol 76, 236-252.
21. Azevedo C, Szijgyarto Z, &, Saiardi A, (2011) The signaling role of inositol hexakisphosphate kinases (IP6Ks). Adv Enzyme Regul 51, 74-82.
22. Shears SB, Gokhale NA, Wang H, &, Zaremba A, (2011) Diphosphoinositol polyphosphates: what are the mechanisms? Adv Enzyme Regul 51, 13-25.
23. Wundenberg T, &, Mayr GW, (2012) Synthesis and biological actions of diphosphoinositol phosphates (inositol pyrophosphates), regulators of cell homeostasis. Biol Chem 393, 979-998.
24. Wilson MSC, Livermore TM, &, Saiardi A, (2013) Inositol pyrophosphates: between signalling and metabolism. Biochem J 452, 369-379.
25. Shears SB, Weaver JD, &, Wang H, (2013) Structural insight into inositol pyrophosphate turnover. Adv Biol Regul 53, 19-27.
26. Parys JB, &, De Smedt H, (2012) Inositol 1,4,5-trisphosphate and its receptors. Adv Exp Med Biol 740, 255-279.
27. Shears SB, Ganapathi SB, Gokhale NA, Schenk TMH, Wang H, Weaver JD, Zaremba A, &, Zhou Y, (2012) Defining signal transduction by inositol phosphates. Subcell Biochem 59, 389-412.
28. Saiardi A, (2012) How inositol pyrophosphates control cellular phosphate homeostasis? Adv Biol Regul 52, 351-359.
29. Alcázar-Román AR, &, Wente SR, (2008) Inositol polyphosphates: a new frontier for regulating gene expression. Chromosoma 117, 1-13.
30. Tsui MM, &, York JD, (2010) Roles of inositol phosphates and inositol pyrophosphates in development, cell signalling and nuclear processes. Adv Enzyme Regul 50, 324-337.
31. Antonsson B, (1997) Phosphatidylinositol synthase from mammalian tissues. Biochim Biophys Acta 1348, 179-186.
32. Irvine RF, &, Schell MJ, (2001) Back in the water: the return of the inositol phosphates. Nat Rev Mol Cell Biol 2, 327-338.
33. Best MD, Zhang H, &, Prestwich GD, (2010) Inositol polyphosphates, diphosphoinositol polyphosphates and phosphatidylinositol polyphosphate lipids: structure, synthesis, and development of probes for studying biological activity. Nat Prod Rep 27, 1403-1430.
34. Hatch AJ, &, York JD, (2010) SnapShot: inositol phosphates. Cell 143, 1030.
35. Chakraborty A, Kim S, &, Snyder SH, (2011) Inositol pyrophosphates as mammalian cell signals. Sci Signal 4, re1.
36. Lee J-Y, Kim Y, Park J, &, Kim S, (2012) Inositol polyphosphate multikinase signaling in the regulation of metabolism. Ann N Y Acad Sci 1271, 68-74.
37. Martin J-B, Laussmann T, Bakker-Grunwald T, Vogel G, &, Klein G, (2000) neo-Inositol polyphosphates in the amoeba Entamoeba histolytica. J Biol Chem 275, 10134-10140.
38. Draškovič P, Saiardi A, Bhandari R, Burton A, Ilc G, Kovačevič M, Snyder SH, &, Podobnik M, (2008) Inositol hexakisphosphate kinase products contain diphosphate and triphosphate groups. Chem Biol 15, 274-286.
39. Laussmann T, Reddy KM, Reddy KK, Falck JR, &, Vogel G, (1997) Diphospho-myo-inositol phosphates from Dictyostelium identified as D-6-diphospho-myo-inositol pentakisphosphate and D-5,6-bisdiphospho-myo- inositol tetrakisphosphate. Biochem J 322, 31-33.
40. Laussmann T, Hansen A, Reddy KM, Reddy KK, Falck JR, &, Vogel G, (1998) Diphospho-myo-inositol phosphates in Dictyostelium and Polysphondylium: identification of a new bisdiphospho-myo-inositol tetrakisphosphate. FEBS Lett 426, 145-150.
41. Mulugu S, Bai W, Fridy PC, Bastidas RJ, Otto JC, Dollins DE, Haystead TA, Ribeiro AA, &, York JD, (2007) A conserved family of enzymes that phosphorylate inositol hexakisphosphate. Science 316, 106-109.
42. Glennon MC, &, Shears SB, (1993) Turnover of inositol pentakisphosphates, inositol hexakisphosphate and diphosphoinositol polyphosphates in primary cultured hepatocytes. Biochem J 283, 583-590.
43. Shears SB, Ali N, Craxton A, &, Bembenek ME, (1995) Synthesis and metabolism of bis-diphosphoinositol tetrakisphosphate in vitro and in vivo. J Biol Chem 270, 10489-10497.
44. Saiardi A, Nagata E, Luo HR, Sawa A, Luo X, Snowman AM, &, Snyder SH, (2001) Mammalian inositol polyphosphate multikinase synthesizes inositol 1,4,5-trisphosphate and an inositol pyrophosphate. Proc Natl Acad Sci USA 98, 2306-2311.
45. Zhang T, Caffrey JJ, &, Shears SB, (2001) The transcriptional regulator, Arg82, is a hybrid kinase with both monophosphoinositol and diphosphoinositol polyphosphate synthase activity. FEBS Lett 494, 208-212.
46. Voglmaier SM, Bembenek ME, Kaplin AI, Dormán G, Olszewski JD, Prestwich GD, &, Snyder SH, (1996) Purified inositol hexakisphosphate kinase is an ATP synthase: diphosphoinositol pentakisphosphate as a high-energy phosphate donor. Proc Natl Acad Sci USA 93, 4305-4310.
47. 5 kinase. Chem Commun 48, 11292-11294.
48. Weaver JD, Wang H, &, Shears SB, (2013) The kinetic properties of a human PPIP5K reveal that its kinase activities are protected against the consequences of a deteriorating cellular bioenergetic environment. Biosci Rep 33, art:000222.
49. Saiardi A, Bhandari R, Resnick AC, Snowman AM, &, Snyder SH, (2004) Inositol pyrophosphate: physiologic phosphorylation of proteins. Science 306, 2101-2105.
50. Bhandari R, Saiardi A, Ahmadibeni Y, Snowman AM, Resnick AC, Kristiansen TZ, Molina H, Pandey A, Werner JK Jr, Juluri KR, et al,. (2007) Protein pyrophosphorylation by inositol pyrophosphates is a posttranslational event. Proc Natl Acad Sci USA 104, 15305-15310.
51. Brehm MA, Schenk TMH, Zhou X, Fanick W, Lin H, Windhorst S, Nalaskowski MM, Kobras M, Shears SB, &, Mayr GW, (2007) Intracellular localization of human inositol 1,3,4,5,6- pentakisphosphate 2-kinase. Biochem J 408, 335-345.
52. Otto JC, Kelly P, Chiou S-T, &, York JD, (2007) Alterations in an inositol phosphate code through synergistic activation of a G protein and inositol phosphate kinases. Proc Natl Acad Sci USA 104, 15653-15658.
53. Saiardi A, Erdjument-Bromage H, Snowman AM, Tempst P, &, Snyder SH, (1999) Synthesis of diphosphoinositol pentakisphosphate by a newly identified family of higher inositol polyphosphate kinases. Curr Biol 9, 1323-1326.
54. Saiardi A, Nagata E, Luo HR, Snowman AM, &, Snyder SH, (2001) Identification and characterization of a novel inositol hexakisphosphate kinase. J Biol Chem 276, 39179-39185.
55. Padmanabhan U, Dollins DE, Fridy PC, York JD, &, Downes CP, (2009) Characterization of a selective inhibitor of inositol hexakisphosphate kinases: use in defining biological roles and metabolic relationships of inositol pyrophosphates. J Biol Chem 284, 10571-10582.
56. González B, Schell MJ, Letcher AJ, Veprintsev DB, Irvine RF, &, Williams RL, (2004) Structure of a human inositol 1,4,5-trisphosphate 3-kinase: substrate binding reveals why it is not a phosphoinositide 3-kinase. Mol Cell 15, 689-701.
57. Miller GJ, &, Hurley JH, (2004) Crystal structure of the catalytic core of inositol 1,4,5-trisphosphate 3-kinase. Mol Cell 15, 703-711.
58. Holmes W, &, Jogl G, (2006) Crystal structure of inositol phosphate multikinase 2 and implications for substrate specificity. J Biol Chem 281, 38109-38116.
59. Endo-Streeter S, Tsui M-KM, Odom AR, Block J, &, York JD, (2012) Structural studies and protein engineering of inositol phosphate multikinase. J Biol Chem 287, 35360-35369.
60. Saiardi A, Caffrey JJ, Snyder SH, &, Shears SB, (2000) The inositol hexakisphosphate kinase family. Catalytic flexibility and function in yeast vacuole biogenesis. J Biol Chem 275, 24686-24692.
61. Lin H, Fridy PC, Ribeiro AA, Choi JH, Barma DK, Vogel G, Falck JR, Shears SB, York JD, &, Mayr GW, (2009) Structural analysis and detection of biological inositol pyrophosphates reveal that the family of VIP/diphosphoinositol pentakisphosphate kinases are 1/3-kinases. J Biol Chem 284, 1863-1872.
62. Dephoure N, Zhou C, Villén Beausoleil SA, Bakalarski CE, Elledge SJ, &, Gygi SP, (2008) A quantitative atlas of mitotic phosphorylation. Proc Natl Acad Sci USA 105, 10762-10767.
63. Rual J-F, Venkatesan K, Hao T, Hirozane-Kishikawa T, Dricot A, Li N, Berriz GF, Gibbons FD, Dreze M, Ayivi-Guedehoussou N, et al,. (2005) Towards a proteome-scale map of the human protein-protein interaction network. Nature 437, 1173-1178.
64. Venkatesan K, Rual J-F, Vazquez A, Stelzl U, Lemmens I, Hirozane-Kishikawa T, Hao T, Zenkner M, Xin X, Goh K-I, et al,. (2009) An empirical framework for binary interactome mapping. Nat Methods 6, 83-90.
65. Yu H, Tardivo L, Tam S, Weiner E, Gebreab F, Fan C, Svrzikapa N, Hirozane-Kishikawa T, Rietman E, Yang X, et al,. (2011) Next-generation sequencing to generate interactome datasets. Nat Methods 8, 478-480.
66. Houseley J, LaCava J, &, Tollervey D, (2006) RNA-quality control by the exosome. Nat Rev Mol Cell Biol 7, 529-539.
67. Kerrien S, Aranda B, Breuza L, Bridge A, Broackes-Carter F, Chen C, Duesbury M, Dumousseau M, Feuermann M, Hinz U, et al,. (2012) The IntAct molecular interaction database in 2012. Nucleic Acids Res 40, D841-D846.
68. Bianchin MM, Londero RG, Lima JE, &, Bigal ME, (2010) Migraine and epilepsy: a focus on overlapping clinical, pathophysiological, molecular and therapeutic aspects. Curr Pain Headache Rep 14, 276-283.
69. Luo HR, Huang YE, Chen JC, Saiardi A, Iijima M, Ye K, Huang Y, Nagata E, Devreotes P, &, Snyder SH, (2001) GRAB: a physiologic guanine nucleotide exchange factor for Rab3A, which interacts with inositol hexakisphosphate kinase. Neuron 31, 439-451.
70. Illies C, Gromada J, Fiume R, Leibiger B, Yu J, Juhl K, Yang S-N, Barma DK, Falck JR, Saiardi A, et al,. (2007) Requirement of inositol pyrophosphates for full exocytotic capacity in pancreatic β cells. Science 318, 1299-1302.
71. Kamimura J, Wakui K, Kadowaki H, Watanabe Y, Miyake K, Harada N, Sakamoto M, Kinoshita A, Yoshiura K, Ohta T, et al,. (2004) The IHPK1 gene is disrupted at the 3p21.31 breakpoint of t(3;9) in a family with type 2 diabetes mellitus. J Hum Genet 49, 360-365.
72. Bhandari R, Juluri KR, Resnick AC, &, Snyder SH, (2008) Gene deletion of inositol hexakisphosphate kinase 1 reveals inositol pyrophosphate regulation of insulin secretion, growth, and spermiogenesis. Proc Natl Acad Sci USA 105, 2349-2353.
73. Chakraborty A, Koldobskiy MA, Bello NT, Maxwell M, Potter JJ, Juluri KR, Maag D, Kim S, Huang AS, Dailey MJ, et al,. (2010) Inositol pyrophosphates inhibit Akt signaling, thereby regulating insulin sensitivity and weight gain. Cell 143, 897-910.
74. Rayasam GV, Tulasi VK, Sodhi R, Davis JA, &, Ray A, (2009) Glycogen synthase kinase 3: more than a namesake. Br J Pharmacol 156, 885-898.
75. Chakraborty A, Latapy C, Xu J, Snyder SH, &, Beaulieu J-M, (2013) Inositol hexakisphosphate kinase-1 regulates behavioural responses via GSK3 signaling pathways. Mol Psychiatry, doi: 10.1038/mp.2013.21.
76. Prasad A, Jia Y, Chakraborty A, Li Y, Jain SK, Zhong J, Roy SG, Loison F, Mondal S, Sakai J, et al,. (2011) Inositol hexakisphosphate kinase 1 regulates neutrophil function in innate immunity by inhibiting phosphatidylinositol-(3,4, 5)-trisphosphate signaling. Nat Immunol 12, 752-760.
77. Onnebo SMN, &, Saiardi A, (2009) Inositol pyrophosphates modulate hydrogen peroxide signalling. Biochem J 423, 109-118.
78. Jadav RS, Chanduri MVL, Sengupta S, &, Bhandari R, (2013) Inositol pyrophosphate synthesis by inositol hexakisphosphate kinase 1 is required for homologous recombination repair. J Biol Chem 288, 3312-3321.
79. Ghosh S, Shukla D, Suman K, Lakshmi BJ, Manorama R, Kumar S, &, Bhandari R, (2013) Inositol hexakisphosphate kinase 1 maintains hemostasis in mice by regulating platelet polyphosphate levels. Blood 122, 1478-1486.
80. Ye C, Bandara WMMS, &, Greenberg ML, (2013) Regulation of inositol metabolism is fine-tuned by inositol pyrophosphates in Saccharomyces cerevisiae. J Biol Chem 288, 24898-24908.
81. Morrison BH, Tang Z, Jacobs BS, Bauer JA, &, Lindner DJ, (2005) Apo2L/TRAIL induction and nuclear translocation of inositol hexakisphosphate kinase 2 during IFN-β-induced apoptosis in ovarian carcinoma. Biochem J 385, 595-603.
82. Nagata E, Saiardi A, Tsukamoto H, Okada Y, Itoh Y, Satoh T, Itoh J, Margolis RL, Takizawa S, Sawa A, et al,. (2011) Inositol hexakisphosphate kinases induce cell death in Huntington disease. J Biol Chem 286, 26680-26686.
83. Morrison BH, Bauer JA, Hu J, Grane RW, Ozdemir AM, Chawla-Sarkar M, Gong B, Almasan A, Kalvakoluna DV, &, Lindner DJ, (2002) Inositol hexakisphosphate kinase 2 sensitizes ovarian carcinoma cells to multiple cancer therapeutics. Oncogene 21, 1882-1889.
84. Nagata E, Saiardi A, Tsukamoto H, Satoh T, Itoh Y, Itoh J, Shibata M, Takizawa S, &, Takagi S, (2010) Inositol hexakisphosphate kinases promote autophagy. Int J Biochem Cell Biol 42, 2065-2071.
85. Schmelzle T, &, Hall MN, (2000) TOR, a central controller of cell growth. Cell 103, 253-262.
86. Morrison BH, Bauer JA, Lupica JA, Tang Z, Schmidt H, DiDonato JA, &, Lindner DJ, (2007) Effect of inositol hexakisphosphate kinase 2 on transforming growth factor β-activated kinase 1 and NF-κB activation. J Biol Chem 282, 15349-15356.
87. Chakraborty A, Werner JK Jr, Koldobskiy MA, Mustafa AK, Juluri KR, Pietropaoli J, Snowman AM, &, Snyder SH, (2011) Casein kinase-2 mediates cell survival through phosphorylation and degradation of inositol hexakisphosphate kinase-2. Proc Natl Acad Sci USA 108, 2205-2209.
88. Chakraborty A, Koldobskiy MA, Sixt KM, Juluri KR, Mustafa AK, Snowman AM, van Rossum DB, Patterson RL, &, Snyder SH, (2008) HSP90 regulates cell survival via inositol hexakisphosphate kinase-2. Proc Natl Acad Sci USA 105, 1134-1139.
89. Koldobskiy MA, Chakraborty A, Werner JK Jr, Snowman AM, Juluri KR, Vandiver MS, Kim S, Heletz S, &, Snyder SH, (2010) p53-Mediated apoptosis requires inositol hexakisphosphate kinase-2. Proc Natl Acad Sci USA 107, 20947-20951.
90. Rice DS, Northcutt GM, &, Kurschner C, (2001) The Lnx family proteins function as molecular scaffolds for numb family proteins. Mol Cell Neurosci 18, 525-540.
91. 2+-dependent transbilayer movement of phospholipids. J Biol Chem 271, 17205-17210.
92. Dong B, Zhou Q, Zhao J, Zhou A, Harty RN, Bose S, Banerjee A, Slee R, Guenther J, Williams BRG, et al,. (2004) Phospholipid scramblase 1 potentiates the antiviral activity of interferon. J Virol 78, 8983-8993.
93. Sarmah B, &, Wente SR, (2010) Inositol hexakisphosphate kinase-2 acts as an effector of the vertebrate Hedgehog pathway. Proc Natl Acad Sci USA 107, 19921-19926.
94. Morrison BH, Haney R, Lamarre E, Drazba J, Prestwich GD, &, Lindner DJ, (2009) Gene deletion of inositol hexakisphosphate kinase 2 predisposes to aerodigestive tract carcinoma. Oncogene 28, 2383-2392.
95. Imami K, Sugiyama N, Kyono Y, Tomita M, &, Ishihama Y, (2008) Automated phosphoproteome analysis for cultured cancer cells by two-dimensional nanoLC-MS using a calcined titania/C18 biphasic column. Anal Sci 24, 161-166.
96. Togashi S, Takazawa K, Endo T, Erneux C, &, Onaya T, (1997) Structural identification of the myo-inositol 1,4,5-trisphosphate-binding domain in rat brain inositol 1,4,5-trisphosphate 3-kinase. Biochem J 326, 221-225.
97. Fridy PC, Otto JC, Dollins DE, &, York JD, (2007) Cloning and characterization of two human VIP1-like inositol hexakisphosphate and diphosphoinositol pentakisphosphate kinases. J Biol Chem 282, 30754-30762.
98. Wang H, Falck JR, Tanaka Hall TM, &, Shears SB, (2012) Structural basis for an inositol pyrophosphate kinase surmounting phosphate crowding. Nat Chem Biol 8, 111-116.
99. Gokhale NA, Zaremba A, &, Shears SB, (2011) Receptor-dependent compartmentalization of PPIP5K1, a kinase with a cryptic polyphosphoinositide binding domain. Biochem J 434, 415-426.
100. Barbe L, Lundberg E, Oksvold P, Stenius A, Lewin E, Björling E, Asplund A, Pontén F, Brismar H, Uhlén M, et al,. (2008) Toward a confocal subcellular atlas of the human proteome. Mol Cell Proteomics 7, 499-508.
101. Olsen JV, Blagoev B, Gnad F, Macek B, Kumar C, Mortensen P, &, Mann M, (2006) Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127, 635-648.
102. Cantin GT, Yi W, Lu B, Park SK, Xu T, Lee J-D, &, Yates JR III, (2008) Combining protein-based IMAC, peptide-based IMAC, and MudPIT for efficient phosphoproteomic analysis. J Proteome Res 7, 1346-1351.
103. Gauci S, Helbig AO, Slijper M, Krijgsveld J, Heck AJR, &, Mohammed S, (2009) Lys-N and trypsin cover complementary parts of the phosphoproteome in a refined SCX-based approach. Anal Chem 81, 4493-4501.
104. Beausoleil SA, Villén J, Gerber SA, Rush J, &, Gygi SP, (2006) A probability-based approach for high-throughput protein phosphorylation analysis and site localization. Nat Biotechnol 24, 1285-1292.
105. Yu L-R, Zhu Z, Chan KC, Issaq HJ, Dimitrov DS, &, Veenstra TD, (2007) Improved titanium dioxide enrichment of phosphopeptides from HeLa cells and high confident phosphopeptide identification by cross-validation of MS/MS and MS/MS/MS spectra. J Proteome Res 6, 4150-4162.
106. Mayya V, Lundgren DH, Hwang S-I, Rezaul K, Wu L, Eng JK, Rodionov V, &, Han DK, (2009) Quantitative phosphoproteomic analysis of T cell receptor signaling reveals system-wide modulation of protein-protein interactions. Sci Signal 2, RA46.
107. Alekseev AE, Reyes S, Selivanov VA, Dzeja PP, &, Terzic A, (2012) Compartmentation of membrane processes and nucleotide dynamics in diffusion-restricted cardiac cell microenvironment. J Mol Cell Cardiol 52, 401-409.
108. Erneux C, &, Elong Edimo W, (2013) When worlds collide: inositol pyrophosphates and phosphoinositides intersect at the plasma membrane. Biochem J 453, e3-e4.
109. - as a transition state analog of phosphoryl transfer. Chem Biol 9, 375-381.
110. Dang CV, (2012) MYC on the path to cancer. Cell 149, 22-35.
111. Safrany ST, Caffrey JJ, Yang X, Bembenek ME, Moyer MB, Burkhart WA, &, Shears SB, (1998) A novel context for the 'MutT' module, a guardian of cell integrity, in a diphosphoinositol polyphosphate phosphohydrolase. EMBO J 17, 6599-6607.
112. Caffrey JJ, Safrany ST, Yang X, &, Shears SB, (2000) Discovery of molecular and catalytic diversity among human diphosphoinositol-polyphosphate phosphohydrolases: an expanding NUDT family. J Biol Chem 275, 12730-12736.
113. Caffrey JJ, &, Shears SB, (2001) Genetic rationale for microheterogeneity of human diphosphoinositol polyphosphate phosphohydrolase type 2. Gene 269, 53-60.
114. Fisher DI, Safrany ST, Strike P, McLennan AG, &, Cartwright JL, (2002) Nudix hydrolases that degrade dinucleoside and diphosphoinositol polyphosphates also have 5-phosphoribosyl 1-pyrophosphate (PRPP) pyrophosphatase activity that generates the glycolytic activator ribose 1,5-bisphosphate. J Biol Chem 277, 47313-47317.
115. Hidaka K, Caffrey JJ, Hua L, Zhang T, Falck JR, Nickel GC, Carrel L, Barnes LD, &, Shears SB, (2002) An adjacent pair of human NUDT genes on chromosome X are preferentially expressed in testis and encode two new isoforms of diphosphoinositol polyphosphate phosphohydrolase. J Biol Chem 277, 32730-32738.
116. Leslie NR, McLennan AG, &, Safrany ST, (2002) Cloning and characterisation of hAps1 and hAps2, human diadenosine polyphosphate- metabolising Nudix hydrolases. BMC Biochem 3, 20.
117. Safrany ST, Ingram SW, Cartwright JL, Falck JR, McLennan AG, Barnes LD, &, Shears SB, (1999) The diadenosine hexaphosphate hydrolases from Schizosaccharomyces pombe and Saccharomyces cerevisiae are homologues of the human diphosphoinositol polyphosphate phosphohydrolase. Overlapping substrate specificities in a MutT-type protein. J Biol Chem 274, 21735-21740.
118. Kilari RS, Weaver JD, Shears SB, &, Safrany ST, (2013) Understanding inositol pyrophosphate metabolism and function: kinetic characterization of the DIPPs. FEBS Lett 587, 3464-3470.
119. Thorsell A-G, Persson C, Gräslund S, Hammarström M, Busam RD, &, Hallberg BM, (2009) Crystal structure of human diphosphoinositol phosphatase 1. Proteins 77, 242-246.
120. McLennan AG, (2006) The Nudix hydrolase superfamily. Cell Mol Life Sci 63, 123-143.
121. Yang X, Safrany ST, &, Shears SB, (1999) Site-directed mutagenesis of diphosphoinositol polyphosphate phosphohydrolase, a dual specificity NUDT enzyme that attacks diadenosine polyphosphates and diphosphoinositol polyphosphates. J Biol Chem 274, 35434-35440.
122. Chu C, Alapat D, Wen X, Timo K, Burstein D, Lisanti M, Shears S, &, Kohtz DS, (2004) Ectopic expression of murine diphosphoinositol polyphosphate phosphohydrolase 1 attenuates signaling through the ERK1/2 pathway. Cell Signal 16, 1045-1059.
123. Hua LV, Green M, Warsh JJ, &, Li PP, (2001) Molecular cloning of a novel isoform of diphosphoinositol polyphosphate phosphohydrolase: a potential target of lithium therapy. Neuropsychopharmacology 24, 640-651.
124. Hunziker W, &, Peters PJ, (1998) Rab17 localizes to recycling endosomes and regulates receptor-mediated transcytosis in epithelial cells. J Biol Chem 273, 15734-15741.
125. Zacchi P, Stenmark H, Parton RG, Orioli D, Lim F, Giner A, Mellman I, Zerial M, &, Murphy C, (1998) Rab17 regulates membrane trafficking through apical recycling endosomes in polarized epithelial cells. J Cell Biol 140, 1039-1053.
126. Linossi EM, &, Nicholson SE, (2012) The SOCS box-adapting proteins for ubiquitination and proteasomal degradation. IUBMB Life 64, 316-323.
127. Otto EA, Loeys B, Khanna H, Hellemans J, Sudbrak R, Fan S, Muerb U, O'Toole JF, Helou J, Attanasio M, et al,. (2005) Nephrocystin-5, a ciliary IQ domain protein, is mutated in Senior-Loken syndrome and interacts with RPGR and calmodulin. Nat Genet 37, 282-288.
128. Richter AM, Pfeifer GP, &, Dammann RH, (2009) The RASSF proteins in cancer; from epigenetic silencing to functional characterization. Biochim Biophys Acta 1796, 114-128.
129. Bradley JR, &, Pober JS, (2001) Tumor necrosis factor receptor-associated factors (TRAFs). Oncogene 20, 6482-6491.
130. Wang J, Huo K, Ma L, Tang L, Li D, Huang X, Yuan Y, Li C, Wang W, Guan W, et al,. (2011) Toward an understanding of the protein interaction network of the human liver. Mol Syst Biol 7, 536.
131. Stelzl U, Worm U, Lalowski M, Haenig C, Brembeck FH, Goehler H, Stroedicke M, Zenker M, Schoenherr A, Koeppen S, et al,. (2005) A human protein-protein interaction network: a resource for annotating the proteome. Cell 122, 957-968.
132. Roland BP, Stuchul KA, Larsen SB, Amrich CG, VanDemark AP, Celotto AM, &, Palladino MJ, (2013) Evidence of a triosephosphate isomerase non-catalytic function crucial to behavior and longevity. J Cell Sci 126, 3151-3158.
133. Falcon SC, Hudson CS, Huang Y, Mortimore M, Golec JM, Charlton PA, Weber P, &, Sundaram H, (2013) A non-catalytic role of choline kinase alpha is important in promoting cancer cell survival. Oncogenesis 2, e38.
134. Rauch J, Volinsky N, Romano D, &, Kolch W, (2011) The secret life of kinases: functions beyond catalysis. Cell Commun Signal 9, 23.
135. Saini C, Suter DM, Liani A, Gos P, &, Schibler U, (2011) The mammalian circadian timing system: synchronization of peripheral clocks. Cold Spring Harb Symp Quant Biol 76, 39-47.
136. Logue JS, &, Morrison DK, (2012) Complexity in the signaling network: insights from the use of targeted inhibitors in cancer therapy. Genes Dev 26, 641-650.
137. Tran PV, Lachke SA, &, Stottmann RW, (2013) Towards a systems-level understanding of the Hedgehog signaling pathway: defining the complex, robust, and fragile. Wiley Interdiscip Rev Syst Biol Med 5, 83-100.
138. ChemBioDraw Ultra, Version 12.0.2.1076, http://www.cambridgesoft.com/ software/chembiodraw.
139. The PyMOL Molecular Graphics System, Version 1.5.0.4. Schrodinger, LLC. http://www.pymol.org.