Specificity determinants in phosphoinositide dephosphorylation: Crystal structure of an archetypal inositol polyphosphate 5-phosphatase

Cell

Volumn 105, Issue 3, 2001, Pages 379-389

  Tsujishita, Yosuke ^a   Guo, Shuling ^b   Stolz, Leslie E ^b   York, John D ^b   Hurley, James H ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 0035805064     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(01)00326-9     Document Type: Article

References (53)

1. Abrahams, J.P., and Leslie, A.G.W. (1996). Methods used in the structure determination of bovine F-1 ATPase. Acta Crystallogr. D 52, 30-42.
2. Altschul, S.F., Madden, T.L, Schäffer A.A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D.J. (1997). Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402.
3. Attree, O., Olivos, I.M., Okabe, I., Bailey, L.C., Nelson, D.L., Lewis, R.A., McInnes, R.R., and Nussbaum, R.L. (1992). The Lowe's oculocerebrorenal syndrome gene encodes a protein highly homologous to inositol polyphosphate-5-phosphatase. Nature 358, 239-242.
4. Bateman, A., Birney, E., Durbin, R., Eddy, S.R., Finn, R.D., and Sonnhammer, E.L. (1999). Pfam 3.1:1313 multiple alignments match the majority of proteins. Nucleic Acids Res. 27, 260-262.
5. Berridge, M.J., and Irvine, R.F. (1989). Inositol phosphates and cell signaling. Nature 341, 197-205.
6. Brünger, A.T., Adams, P.D., Clore, G.M., DeLano, W.L., Gros, P., Grosse-Kunstleve, R.W., Jiang, J.S., Kuszewski, J., Nilges, M., Pannu, N.S., et al. (1998). Crystallography and NMR system (CNS): a new software system for macromolecular structure determination. Acta Crystallogr. D 54, 905-921.
7. Clement, S., Krause, U., Desmedt, F., Tanti, J.-F., Behrends, J., Pesesse, X., Sasaki, T., Penninger, J., Doherty, M., Malaisse, W., et al. (2001). The lipid phosphatase SHIP2 controls insulin sensitivity. Nature 409, 92-96.
8. Cremona, O., Di Paolo, G., Wenk, M.R., Luthi, A., Kim, W.T., Takei, K., Daniell, L., Nemoto, Y., Shears, S.B., Flavell, R.A., et al. (1999). Essential role of phosphoinositide metabolism in synaptic vesicle recycling. Cell 99, 179-188.
9. Dauter, Z., Dauter, M., and Rajashankar, K.R. (2000). Novel approach to phasing proteins: derivatization by short cryo-soaking with halides. Acta Crystallogr. D 56, 232-237.
10. De Camilli, P., Emr, S.D., McPherson, P.S., and Novick, P. (1996). Phosphoinositides as regulators in membrane traffic. Science 271, 1533-1539.
11. de La Fortelle, E., and Bricogne, G. (1997). Maximum-likelihood heavy-atom parameter refinement for multiple isomorphous replacement and multiwavelength anomalous diffraction methods. Methods Enzymol. 276, 472-494.
12. Dlakic, M. (2000). Functionally unrelated signalling proteins contain a fold similar to Mg2 +-dependent endonucleases. Trends Biochem. Sci. 25, 272-273.
13. Drayer, A.L., Pesesse, X., De Smedt, F., Communi, D., Moreau, C., and Erneux, C. (1996). The family of inositol and phosphatidylinositol polyphosphate 5-phosphatases. Biochem. Soc. Trans. 24, 1001-1005.
14. Gibrat, J.-F., Madej, T., and Bryant, S.H. (1996). Surprising similarities in structure comparison. Curr. Opin. Struct. Biol. 6, 377-385.
15. Gorman, M.A., Morera, S., Rothwell, D.G., de la Fortelle, E., Mol, C.D., Tainer, J.A., Hickson, I.D., and Freemont, P.S. (1997). The crystal structure of the human DNA repair endonuclease HAP1 suggests the recognition of extra-helical deoxyribose at DNA abasic sites. EMBO J. 16, 6548-6558.
16. Guo, S., Stolz, L.E., Lemrow, S.M., and York, J.D. (1999). SAC1-like domains of yeast SAC1, INP52, and INP53 and of human synaptojanin encode polyphosphoinositide phosphatases. J. Biol. Chem. 274, 12990-12995.
17. Harris, T.W., Hartwieg, E., Horvitz, H.R., and Jorgensen, E.M. (2000). Mutations in synaptojanin disrupt synaptic vesicle recycling. J. Cell Biol. 150, 589-599.
18. 3 5-phosphatase. Nature 408, 735-740.
19. Hurley, J.H., Tsujishita, Y., and Pearson, M.A. (2000). Floundering about at cell membranes: A structural view of phospholipid signaling. Curr. Opin. Struct. Biol. 10, 737-743.
20. Jefferson, A.B., and Majerus, P.W. (1996). Mutation of the conserved domains of two inositol polyphosphate 5-phosphatases. Biochemistry 35, 7890-7894.
21. Jones, T.A., Zou, J.Y., Cowan, S.W., and Kjeldgaard, M. (1991). Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47, 110-119.
22. Kisseleva, M.V., Wilson, M.P., and Majerus, P.W. (2000). The isolation and characterization of a cDNA encoding phospholipid-specific inositol polyphosphate 5-phosphatase. J. Biol. Chem. 275, 20110-20116.
23. Kraulis, P. (1991). MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24, 946-950.
24. Laskowski, R.A., MacArthur, M.W., Moss, D.S., and Thornton, J.M. (1993). PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 24, 946-950.
25. Liscovitch, M., and Cantley, L.C. (1994). Lipid second messengers. Cell 77, 329-334.
26. Liu, Q., Li, M.Z., Leibham, D., Cortez, D., and Elledge, S.J. (1998). The univector plasmid-fusion system, a method for rapid construction of recombinant DNA without restriction enzymes. Curr. Biol. 8, 1300-1309.
27. Majerus, P.W. (1992). Inositol phosphate biochemistry. Annu. Rev. Biochem. 61, 225-250.
28. Majerus, P.W., Kisseleva, M.V., and Norris, F.A. (1999). The role of phosphatases in inositol signaling reactions. J. Biol. Chem. 274, 10669-10672.
29. Matsuo, Y., Yamada, A., Tsukamoto, K., Tamura, H.-O., Ikeawa, H., Nakamura, H., and Nishikawa, K. (1996). A distant evolutionary relationship between bacterial sphingomyelinase and mammalian DNase I. Prot. Sci. 5, 2459-2467.
30. McPherson, P.S., Garcia, E.P., Slepnev, V.I., David, C., Zhang, X., Grabs, D., Sossin, W.S., Bauerfeind, R., Nemoto, Y., and De Camilli, P. (1996). A presynaptic inositol-5-phosphatase. Nature 379, 353-357.
31. Merritt, E.A., and Bacon, D.J. (1997). Raster3D version 2.0: A program for photorealistic molecular graphics. Methods Enzymol. 277, 505-524.
32. Mitchell, C.A., Brown, S., Campbell, U.K., Munday, A.D., and Speed, C.J. (1996). Regulation of second messengers by the inositol polyphosphate 5-phosphatases. Biochem Soc Trans. 24, 994-1000.
33. Mol, C.D., Kuo, C.-F., Thayer, M.M., Cunningham, R.P., and Tainer, J.A. (1995). Structure and function of the multifunctional DNA-repair enzyme exonuclease III. Nature 374, 381-386.
34. Mol, C.D., Izumi, T., Mitra, S., and Tainer, J.A. (2000). DNA-bound structures and mutants reveal abasic DNA binding by APE1 DNA repair and coordination. Nature 403, 451-456.
35. Odom, A.R., Stahlberg, A., Wente, S.R., and York, J.D. (2000). A role for nuclear inositol 1,4,5-trisphosphate kinase in transcriptional control. Science 287, 2026-2029.
36. Odorizzi, G., Babst, M., and Emr, S.D. (2000). Phosphoinositide signaling and the regulation of membrane trafficking in yeast. Trends Biochem. Sci. 25, 229-235.
37. Ono, M., Okada, H., Bolland, S., Yanagi, S., Kurosaki, T., and Ravetch, J.V. (1997). Deletion of SHIP or SHP-1 reveals two distinct pathways for inhibitory signaling. Cell 90, 293-301.
38. Otwinowski, Z., and Minor, W. (1997). Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326.
39. Rameh, L.E., and Cantley, L.C. (1999). The role of phosphoinositide 3-kinase lipid products in cell function. J. Biol. Chem. 274, 8347-8350.
40. Rao, V.D., Misra, S., Boronenkov, I.V., Anderson, R.A., and Hurley, J.H. (1998). Structure of type llβ phosphatidylinositol phosphate kinase: A protein kinase fold flattened for interfacial phosphorylation. Cell 94, 829-839.
41. Schultz, J., Milpetz, F., Bork, P., and Ponting, C.P. (1998). SMART, a simple modular architecture research tool: Identification of signaling domains. Proc. Natl. Acad. Sci. USA 95, 5857-5864.
42. Shears, S.B. (1998). The versatility of inositol phosphates as cellular signals. BBA Mol. Cell. Biol. Lipids 1436, 49-67.
43. Sheffield, P., Garrard, S., and Derewenda, Z. (1999). Overcoming expression and purification problems of RhoGDI using a family of parallel expression vectors. Protein Expr. Purification 15, 34-39.
44. Sikorski, R.S., and Hieter, P. (1989). A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122, 19-27.
45. Spiegelberg, B.D., Xiong, J.P., Smith, J.J., Gu, R.F., and York, J.D. (1999). Cloning and characterization of a mammalian lithium-sensitive bisphosphate 3′-nucleotidase inhibited by inositol 1,4-bisphosphate. J. Biol. Chem. 274, 13619-13628.
46. Srinivasan, S., Seaman, M., Nemoto, Y., Daniell, L., Suchy, S.F., Emr, S., De Camilli, P., and Nussbaum, R. (1997). Disruption of three phosphatidylinositol-polyphosphate 5-phosphatase genes from Saccharomyces cerevisiae results in pleiotropic abnormalities of vacuole morphology, cell shape, and osmohomeostasis. Eur. J. Cell Biol. 74, 350-360.
47. Stolz, L.E., Huynh, C.V., Thorner, J., and York, J.D. (1998). Identification and characterization of an essential family of inositol polyphosphate 5-phosphatases (INP51, INP52 and INP53 gene products) in the yeast Saccharomyces cerevisiae. Genetics 148, 1715-1729.
48. Suchy, S.F., Olivos-Glander, I.M., and Nussbaum, R.L. (1995). Lowe syndrome, a deficiency of a phosphatidylinotiol 4,5-bisphosphate 5-phosphatase in the Golgi apparatus. Hum. Mol. Genet. 4, 2245-2250.
49. Suck, D., and Oefner, C. (1986). Structure of DNase I at 2.0 Å resolution suggests a mechanism for binding to and cutting DNA. Nature 321,620-625.
50. Terwilliger, T.C., and Berendzen, J. (1996). Correlated phasing of multiple isomorphous replacement data. Acta Crystallogr. D 52, 749-757.
51. Whisstock, J.C., Romero, S., Gurung, R., Nandurkar, H., Ooms, L.M., Bottomley, S.P., and Mitchell, C.A. (2000). The inositol polyphosphate 5-phosphatases and the apurinic/apyrimidinic base excision repair endonucleases share a common mechanism for catalysis. J. Biol. Chem. 275, 37055-37061.
52. Woscholski, R., and Parker, P.J. (1997). Inositol lipid 5-phosphatases-traffic signals and signal traffic. Trends Biochem. Sci. 22, 427-431.
53. Zhang, X., Jefferson, A.B., Auethavekait, V., and Majerus, P.W. (1995). The protein deficient in Lowe syndrome is a phosphatidylinositol-4,5-bisphosphate 5-phosphatase. Proc. Natl. Acad. Sci. USA 92, 4853-4856.