Structural basis for phosphoinositide substrate recognition, catalysis, and membrane interactions in human inositol polyphosphate 5-phosphatases

Structure

Volumn 22, Issue 5, 2014, Pages 744-755

  Trésaugues, Lionel ^a   Silvander, Camilla ^a   Flodin, Susanne ^a   Welin, Martin ^a   Nyman, Tomas ^a   Gräslund, Susanne ^a   Hammarström, Martin ^a   Berglund, Helena ^a   Nordlund, Pär ^a,b  

^a KAROLINSKA INSTITUTE   (Sweden)

^b NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

INPP5B PROTEIN; OCRL PROTEIN; PHOSPHATIDYLINOSITIDE; SHIP2 PROTEIN; SYNAPTOJANIN; UNCLASSIFIED DRUG; INOSITOL PHOSPHATE; INPPL1 PROTEIN, HUMAN; OCRL PROTEIN, HUMAN; PHOSPHATASE; PHOSPHATIDYLINOSITOL; PHOSPHOINOSITIDE 5-PHOSPHATASE;

ARTICLE; CATALYSIS; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME BINDING; ENZYME SPECIFICITY; ENZYME SUBSTRATE; HUMAN; MEMBRANE BINDING; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN STRUCTURE; CELL MEMBRANE; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; X RAY CRYSTALLOGRAPHY;

CATALYTIC DOMAIN; CELL MEMBRANE; CRYSTALLOGRAPHY, X-RAY; HUMANS; INOSITOL PHOSPHATES; MODELS, MOLECULAR; PHOSPHATIDYLINOSITOLS; PHOSPHORIC MONOESTER HYDROLASES; SUBSTRATE SPECIFICITY;

EID: 84899861049     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2014.01.013     Document Type: Article

References (71)

1. L. Amoasii, K. Hnia, and J. Laporte Myotubularin phosphoinositide phosphatases in human diseases. Curr. Top Microbiol. Immunol. 362 2012 209 233
2. D.A. Annis, C.C. Cheng, C.C. Chuang, J.D. McCarter, H.M. Nash, N. Nazef, T. Rowe, R.J. Kurzeja, and G.W. Shipps Jr. Inhibitors of the lipid phosphatase SHIP2 discovered by high-throughput affinity selection-mass spectrometry screening of combinatorial libraries Comb. Chem. High Throughput Screen. 12 2009 760 771
3. M.V. Astle, G. Seaton, E.M. Davies, C.G. Fedele, P. Rahman, L. Arsala, and C.A. Mitchell Regulation of phosphoinositide signaling by the inositol polyphosphate 5-phosphatases IUBMB Life 58 2006 451 456
4. M.V. Astle, K.A. Horan, L.M. Ooms, and C.A. Mitchell The inositol polyphosphate 5-phosphatases: traffic controllers, waistline watchers and tumour suppressors? Biochem. Soc. Symp. 2007 161 181
5. O. Attree, I.M. Olivos, I. Okabe, L.C. Bailey, D.L. Nelson, R.A. Lewis, R.R. McInnes, and R.L. Nussbaum The Lowe's oculocerebrorenal syndrome gene encodes a protein highly homologous to inositol polyphosphate-5-phosphatase Nature 358 1992 239 242
6. H. Azzedine, A. Bolino, T. Taïeb, N. Birouk, M. Di Duca, A. Bouhouche, S. Benamou, A. Mrabet, T. Hammadouche, and T. Chkili et al. Mutations in MTMR13, a new pseudophosphatase homologue of MTMR2 and Sbf1, in two families with an autosomal recessive demyelinating form of Charcot-Marie-Tooth disease associated with early-onset glaucoma Am. J. Hum. Genet. 72 2003 1141 1153
7. P.T. Beernink, B.W. Segelke, M.Z. Hadi, J.P. Erzberger, D.M. Wilson 3rd, and B. Rupp Two divalent metal ions in the active site of a new crystal form of human apurinic/apyrimidinic endonuclease, Ape1: implications for the catalytic mechanism J. Mol. Biol. 307 2001 1023 1034
8. S.L. Bielas, J.L. Silhavy, F. Brancati, M.V. Kisseleva, L. Al-Gazali, L. Sztriha, R.A. Bayoumi, M.S. Zaki, A. Abdel-Aleem, and R.O. Rosti et al. Mutations in INPP5E, encoding inositol polyphosphate-5-phosphatase E, link phosphatidyl inositol signaling to the ciliopathies Nat. Genet. 41 2009 1032 1036
9. M.D. Blunt, and S.G. Ward Targeting PI3K isoforms and SHIP in the immune system: new therapeutics for inflammation and leukemia Curr. Opin. Pharmacol. 12 2012 444 451
10. A. Bolino, M. Muglia, F.L. Conforti, E. LeGuern, M.A. Salih, D.M. Georgiou, K. Christodoulou, I. Hausmanowa-Petrusewicz, P. Mandich, and A. Schenone et al. Charcot-Marie-Tooth type 4B is caused by mutations in the gene encoding myotubularin-related protein-2 Nat. Genet. 25 2000 17 19
11. V.B. Chen, W.B. Arendall 3rd, J.J. Headd, D.A. Keedy, R.M. Immormino, G.J. Kapral, L.W. Murray, J.S. Richardson, and D.C. Richardson MolProbity: all-atom structure validation for macromolecular crystallography Acta Crystallogr. D Biol. Crystallogr. 66 2010 12 21
12. Y. Chi, B. Zhou, W.Q. Wang, S.K. Chung, Y.U. Kwon, Y.H. Ahn, Y.T. Chang, Y. Tsujishita, J.H. Hurley, and Z.Y. Zhang Comparative mechanistic and substrate specificity study of inositol polyphosphate 5-phosphatase Schizosaccharomyces pombe Synaptojanin and SHIP2 J. Biol. Chem. 279 2004 44987 44995
13. D. Communi, R. Lecocq, and C. Erneux Arginine 343 and 350 are two active residues involved in substrate binding by human Type I D-myo-inositol 1,4,5,-trisphosphate 5-phosphatase J. Biol. Chem. 271 1996 11676 11683
14. S.E. Conduit, J.M. Dyson, and C.A. Mitchell Inositol polyphosphate 5-phosphatases; new players in the regulation of cilia and ciliopathies FEBS Lett. 586 2012 2846 2857
15. G. Di Paolo, and P. De Camilli Phosphoinositides in cell regulation and membrane dynamics Nature 443 2006 651 657
16. J.M. Dyson, A.M. Kong, F. Wiradjaja, M.V. Astle, R. Gurung, and C.A. Mitchell The SH2 domain containing inositol polyphosphate 5-phosphatase-2: SHIP2 Int. J. Biochem. Cell Biol. 37 2005 2260 2265
17. D.A. Eberhard, C.L. Cooper, M.G. Low, and R.W. Holz Evidence that the inositol phospholipids are necessary for exocytosis. Loss of inositol phospholipids and inhibition of secretion in permeabilized cells caused by a bacterial phospholipase C and removal of ATP Biochem. J. 268 1990 15 25
18. K.S. Erdmann, Y. Mao, H.J. McCrea, R. Zoncu, S. Lee, S. Paradise, J. Modregger, D. Biemesderfer, D. Toomre, and P. De Camilli A role of the Lowe syndrome protein OCRL in early steps of the endocytic pathway Dev. Cell 13 2007 377 390
19. G.M. Fuhler, R. Brooks, B. Toms, S. Iyer, E.A. Gengo, M.Y. Park, M. Gumbleton, D.R. Viernes, J.D. Chisholm, and W.G. Kerr Therapeutic potential of SH2 domain-containing inositol-5′-phosphatase 1 (SHIP1) and SHIP2 inhibition in cancer Mol. Med. 18 2012 65 75
20. N. Gamper, and M.S. Shapiro Regulation of ion transport proteins by membrane phosphoinositides Nat. Rev. Neurosci. 8 2007 921 934
21. M.A. Gorman, S. Morera, D.G. Rothwell, E. de La Fortelle, C.D. Mol, J.A. Tainer, I.D. Hickson, and P.S. Freemont The crystal structure of the human DNA repair endonuclease HAP1 suggests the recognition of extra-helical deoxyribose at DNA abasic sites EMBO J. 16 1997 6548 6558
22. S. Gräslund, J. Sagemark, H. Berglund, L.G. Dahlgren, A. Flores, M. Hammarström, I. Johansson, T. Kotenyova, M. Nilsson, P. Nordlund, and J. Weigelt The use of systematic N- and C-terminal deletions to promote production and structural studies of recombinant proteins Protein Expr. Purif. 58 2008 210 221
23. S. Hakim, M.C. Bertucci, S.E. Conduit, D.L. Vuong, and C.A. Mitchell Inositol polyphosphate phosphatases in human disease Curr. Top. Microbiol. Immunol. 362 2012 247 314
24. J.H. Hartwig, G.M. Bokoch, C.L. Carpenter, P.A. Janmey, L.A. Taylor, A. Toker, and T.P. Stossel Thrombin receptor ligation and activated Rac uncap actin filament barbed ends through phosphoinositide synthesis in permeabilized human platelets Cell 82 1995 643 653
25. E. Hellsten, J.P. Evans, D.J. Bernard, P.A. Jänne, and R.L. Nussbaum Disrupted sperm function and fertilin beta processing in mice deficient in the inositol polyphosphate 5-phosphatase Inpp5b Dev. Biol. 240 2001 641 653
26. R.R. Hoopes Jr., A.E. Shrimpton, S.J. Knohl, P. Hueber, B. Hoppe, J. Matyus, A. Simckes, V. Tasic, B. Toenshoff, and S.F. Suchy et al. Dent Disease with mutations in OCRL1 Am. J. Hum. Genet. 76 2005 260 267
27. Y. Ichihara, R. Fujimura, H. Tsuneki, T. Wada, K. Okamoto, H. Gouda, S. Hirono, K. Sugimoto, Y. Matsuya, T. Sasaoka, and N. Toyooka Rational design and synthesis of 4-substituted 2-pyridin-2-ylamides with inhibitory effects on SH2 domain-containing inositol 5′-phosphatase 2 (SHIP2) Eur. J. Med. Chem. 62 2013 649 660
28. P.A. Jänne, S.F. Suchy, D. Bernard, M. MacDonald, J. Crawley, A. Grinberg, A. Wynshaw-Boris, H. Westphal, and R.L. Nussbaum Functional overlap between murine Inpp5b and Ocrl1 may explain why deficiency of the murine ortholog for OCRL1 does not cause Lowe syndrome in mice J. Clin. Invest. 101 1998 2042 2053
29. A.B. Jefferson, and P.W. Majerus Mutation of the conserved domains of two inositol polyphosphate 5-phosphatases Biochemistry 35 1996 7890 7894
30. A. Koch, A. Mancini, O. El Bounkari, and T. Tamura The SH2-domian-containing inositol 5-phosphatase (SHIP)-2 binds to c-Met directly via tyrosine residue 1356 and involves hepatocyte growth factor (HGF)-induced lamellipodium formation, cell scattering and cell spreading Oncogene 24 2005 3436 3447
31. J. Laporte, L.J. Hu, C. Kretz, J.L. Mandel, P. Kioschis, J.F. Coy, S.M. Klauck, A. Poustka, and N. Dahl A gene mutated in X-linked myotubular myopathy defines a new putative tyrosine phosphatase family conserved in yeast Nat. Genet. 13 1996 175 182
32. G. Ligresti, L. Militello, L.S. Steelman, A. Cavallaro, F. Basile, F. Nicoletti, F. Stivala, J.A. McCubrey, and M. Libra PIK3CA mutations in human solid tumors: role in sensitivity to various therapeutic approaches Cell Cycle 8 2009 1352 1358
33. 25Mg NMR spectroscopy J. Am. Chem. Soc. 130 2008 9332 9341
34. P. Liu, H. Cheng, T.M. Roberts, and J.J. Zhao Targeting the phosphoinositide 3-kinase pathway in cancer Nat. Rev. Drug Discov. 8 2009 627 644
35. A.L. Lomize, I.D. Pogozheva, M.A. Lomize, and H.I. Mosberg Positioning of proteins in membranes: a computational approach Protein Sci. 15 2006 1318 1333
36. M.A. Lomize, I.D. Pogozheva, H. Joo, H.I. Mosberg, and A.L. Lomize OPM database and PPM web server: resources for positioning of proteins in membranes Nucleic Acids Res. 40 Database issue 2012 D370 D376
37. T. Maffucci An introduction to phosphoinositides Curr. Top. Microbiol. Immunol. 362 2012 1 42
38. Y. Mao, D.M. Balkin, R. Zoncu, K.S. Erdmann, L. Tomasini, F. Hu, M.M. Jin, M.E. Hodsdon, and P. De Camilli A PH domain within OCRL bridges clathrin-mediated membrane trafficking to phosphoinositide metabolism EMBO J. 28 2009 1831 1842
39. T.F. Martin PI(4,5)P(2) regulation of surface membrane traffic Curr. Opin. Cell Biol. 13 2001 493 499
40. H.J. McCrea, and P. De Camilli Mutations in phosphoinositide metabolizing enzymes and human disease Physiology (Bethesda) 24 2009 8 16
41. R.H. Michell Inositol derivatives: evolution and functions Nat. Rev. Mol. Cell Biol. 9 2008 151 161
42. S.J. Mills, C. Persson, G. Cozier, M.P. Thomas, L. Trésaugues, C. Erneux, A.M. Riley, P. Nordlund, and B.V. Potter A synthetic polyphosphoinositide headgroup surrogate in complex with SHIP2 provides a rationale for drug discovery ACS Chem. Biol. 7 2012 822 828
43. C.D. Mol, T. Izumi, S. Mitra, and J.A. Tainer DNA-bound structures and mutants reveal abasic DNA binding by APE1 and DNA repair coordination [corrected] Nature 403 2000 451 456
44. S.A. Moses, M.A. Ali, S. Zuohe, L. Du-Cuny, L.L. Zhou, R. Lemos, N. Ihle, A.G. Skillman, S. Zhang, and E.A. Mash et al. In vitro and in vivo activity of novel small-molecule inhibitors targeting the pleckstrin homology domain of protein kinase B/AKT Cancer Res. 69 2009 5073 5081
45. N. Oezguen, C.H. Schein, S.R. Peddi, T.D. Power, T. Izumi, and W. Braun A "moving metal mechanism" for substrate cleavage by the DNA repair endonuclease APE-1 Proteins 68 2007 313 323
46. + binding at the B site in human AP endonuclease 1 Bioinformation 7 2011 184 198
47. L.M. Ooms, K.A. Horan, P. Rahman, G. Seaton, R. Gurung, D.S. Kethesparan, and C.A. Mitchell The role of the inositol polyphosphate 5-phosphatases in cellular function and human disease Biochem. J. 419 2009 29 49
48. X. Pesesse, C. Moreau, A.L. Drayer, R. Woscholski, P. Parker, and C. Erneux The SH2 domain containing inositol 5-phosphatase SHIP2 displays phosphatidylinositol 3,4,5-trisphosphate and inositol 1,3,4,5-tetrakisphosphate 5-phosphatase activity FEBS Lett. 437 1998 301 303
49. M. Pirruccello, and P. De Camilli Inositol 5-phosphatases: insights from the Lowe syndrome protein OCRL Trends Biochem. Sci. 37 2012 134 143
50. D. Poccia, and B. Larijani Phosphatidylinositol metabolism and membrane fusion Biochem. J. 418 2009 233 246
51. N. Prasad, R.S. Topping, and S.J. Decker SH2-containing inositol 5′-phosphatase SHIP2 associates with the p130(Cas) adapter protein and regulates cellular adhesion and spreading Mol. Cell. Biol. 21 2001 1416 1428
52. Y. Samuels, Z. Wang, A. Bardelli, N. Silliman, J. Ptak, S. Szabo, H. Yan, A. Gazdar, S.M. Powell, and G.J. Riggins et al. High frequency of mutations of the PIK3CA gene in human cancers Science 304 2004 554
53. T. Sasaoka, T. Wada, and H. Tsuneki Lipid phosphatases as a possible therapeutic target in cases of type 2 diabetes and obesity Pharmacol. Ther. 112 2006 799 809
54. A.C. Schmid, H.M. Wise, C.A. Mitchell, R. Nussbaum, and R. Woscholski Type II phosphoinositide 5-phosphatases have unique sensitivities towards fatty acid composition and head group phosphorylation FEBS Lett. 576 2004 9 13
55. J. Senderek, C. Bergmann, S. Weber, U.P. Ketelsen, H. Schorle, S. Rudnik-Schöneborn, R. Büttner, E. Buchheim, and K. Zerres Mutation of the SBF2 gene, encoding a novel member of the myotubularin family, in Charcot-Marie-Tooth neuropathy type 4B2/11p15 Hum. Mol. Genet. 12 2003 349 356
56. M.W. Sleeman, K.E. Wortley, K.M. Lai, L.C. Gowen, J. Kintner, W.O. Kline, K. Garcia, T.N. Stitt, G.D. Yancopoulos, S.J. Wiegand, and D.J. Glass Absence of the lipid phosphatase SHIP2 confers resistance to dietary obesity Nat. Med. 11 2005 199 205
57. G.R. Stenton, L.F. Mackenzie, P. Tam, J.L. Cross, C. Harwig, J. Raymond, J. Toews, D. Chernoff, T. MacRury, and C. Szabo Characterization of AQX-1125, a small-molecule SHIP1 activator: Part 2. Efficacy studies in allergic and pulmonary inflammation models in vivo Br. J. Pharmacol. 168 2013 1519 1529
58. G.R. Stenton, L.F. Mackenzie, P. Tam, J.L. Cross, C. Harwig, J. Raymond, J. Toews, J. Wu, N. Ogden, T. MacRury, and C. Szabo Characterization of AQX-1125, a small-molecule SHIP1 activator: Part 1. Effects on inflammatory cell activation and chemotaxis in vitro and pharmacokinetic characterization in vivo Br. J. Pharmacol. 168 2013 1506 1518
59. A. Suwa, T. Yamamoto, A. Sawada, K. Minoura, N. Hosogai, A. Tahara, T. Kurama, T. Shimokawa, and I. Aramori Discovery and functional characterization of a novel small molecule inhibitor of the intracellular phosphatase, SHIP2 Br. J. Pharmacol. 158 2009 879 887
60. A. Suwa, T. Kurama, and T. Shimokawa SHIP2 and its involvement in various diseases Expert Opin. Ther. Targets 14 2010 727 737
61. A. Suwa, T. Kurama, T. Yamamoto, A. Sawada, T. Shimokawa, and I. Aramori Glucose metabolism activation by SHIP2 inhibitors via up-regulation of GLUT1 gene in L6 myotubes Eur. J. Pharmacol. 642 2010 177 182
62. K.F. Tolias, J.H. Hartwig, H. Ishihara, Y. Shibasaki, L.C. Cantley, and C.L. Carpenter Type Ialpha phosphatidylinositol-4-phosphate 5-kinase mediates Rac-dependent actin assembly Curr. Biol. 10 2000 153 156
63. Y. Tsujishita, S. Guo, L.E. Stolz, J.D. York, and J.H. Hurley Specificity determinants in phosphoinositide dephosphorylation: crystal structure of an archetypal inositol polyphosphate 5-phosphatase Cell 105 2001 379 389
64. S.E. Tsutakawa, D.S. Shin, C.D. Mol, T. Izumi, A.S. Arvai, A.K. Mantha, B. Szczesny, I.N. Ivanov, D.J. Hosfield, and B. Maiti et al. Conserved structural chemistry for incision activity in structurally non-homologous apurinic/apyrimidinic endonuclease APE1 and endonuclease IV DNA repair enzymes J. Biol. Chem. 288 2013 8445 8455
65. A. Ungewickell, M.E. Ward, E. Ungewickell, and P.W. Majerus The inositol polyphosphate 5-phosphatase Ocrl associates with endosomes that are partially coated with clathrin Proc. Natl. Acad. Sci. USA 101 2004 13501 13506
66. B. Vanhaesebroeck, S.J. Leevers, G. Panayotou, and M.D. Waterfield Phosphoinositide 3-kinases: a conserved family of signal transducers Trends Biochem. Sci. 22 1997 267 272
67. M.G. Waugh Phosphatidylinositol 4-kinases, phosphatidylinositol 4-phosphate and cancer Cancer Lett. 325 2012 125 131
68. J.C. Whisstock, S. Romero, R. Gurung, H. Nandurkar, L.M. Ooms, S.P. Bottomley, and C.A. Mitchell The inositol polyphosphate 5-phosphatases and the apurinic/apyrimidinic base excision repair endonucleases share a common mechanism for catalysis J. Biol. Chem. 275 2000 37055 37061
69. D. Wisniewski, A. Strife, S. Swendeman, H. Erdjument-Bromage, S. Geromanos, W.M. Kavanaugh, P. Tempst, and B. Clarkson A novel SH2-containing phosphatidylinositol 3,4,5-trisphosphate 5-phosphatase (SHIP2) is constitutively tyrosine phosphorylated and associated with src homologous and collagen gene (SHC) in chronic myelogenous leukemia progenitor cells Blood 93 1999 2707 2720
70. Y. Yin, and W.H. Shen PTEN: a new guardian of the genome Oncogene 27 2008 5443 5453
71. Y.Q. Zhang, F. Wang, J. Ding, H. Yan, and Y.L. Yang Novel OCRL mutations in Chinese children with Lowe syndrome World J. Pediatr. 9 2013 53 57