Allosteric activation of the phosphoinositide phosphatase Sac1 by anionic phospholipids

Biochemistry

Volumn 51, Issue 15, 2012, Pages 3170-3177

  Zhong, Shurong ^a,c   Hsu, Fosheng ^a   Stefan, Christopher J ^a   Wu, Xiaochun ^a   Patel, Anamika ^b   Cosgrove, Michael S ^b   Mao, Yuxin ^a  

^a School of Integrative Plant Sciences   (United States)

^b SYRACUSE UNIVERSITY   (United States)

^c KUNMING MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOSTERIC ACTIVATION; ALLOSTERIC ENZYMES; ANIONIC PHOSPHOLIPIDS; CATALYTIC SITES; CONFORMATIONAL CHANGE; LIPID COMPOSITION; PHOSPHATASE ACTIVITY; PHOSPHATIDYLINOSITOL; PHOSPHATIDYLSERINE; PHOSPHOINOSITIDE PHOSPHATASE; POSITIVELY CHARGED; SUBSTRATE MEMBRANES;

PHOSPHOLIPIDS;

PHOSPHATASES;

DNA; MEMBRANE PHOSPHOLIPID; PHOSPHATASE; PHOSPHATIDYLINOSITIDE; PHOSPHATIDYLSERINE; PHOSPHOINOSITIDE PHOSPHATASE SAC1; PHOSPHOLIPID; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

ALLOSTERISM; ARTICLE; CATALYSIS; DNA SEQUENCE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME KINETICS; EUKARYOTE; FLUORESCENCE MICROSCOPY; LIPID ANALYSIS; MEMBRANE VESICLE; MUTAGENESIS; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PURIFICATION; YEAST;

ALLOSTERIC REGULATION; CATALYTIC DOMAIN; KINETICS; PHOSPHOLIPIDS; PHOSPHORIC MONOESTER HYDROLASES; PROTEIN CONFORMATION; SACCHAROMYCES CEREVISIAE PROTEINS;

EUKARYOTA;

EID: 84859885284     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi300086c     Document Type: Article

References (45)

1. 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 (Pubitemid 30236220)
2. De Matteis, M. A. and Godi, A. (2004) PI-loting membrane traffic Nat. Cell Biol. 6, 487-492 (Pubitemid 38786590)
3. Di Paolo, G. and De Camilli, P. (2006) Phosphoinositids in cell regulation and membrane dynamics Nature 443, 651-657 (Pubitemid 44564702)
4. Novick, P., Osmond, B. C., and Botstein, D. (1989) Suppressors of yeast actin mutations Genetics 121, 659-674 (Pubitemid 19105484)
5. Cleves, A. E., Novick, P. J., and Bankaitis, V. A. (1989) Mutations in the SAC1 gene suppress defects in yeast Golgi and yeast actin function J. Cell Biol. 109, 2939-2950 (Pubitemid 20011920)
6. Foti, M., Audhya, A., and Emr, S. D. (2001) Sac1 lipid phosphatase and Stt4 phosphatidylinositol 4-kinase regulate a pool of phosphatidylinositol 4-phosphate that functions in the control of the actin cytoskeleton and vacuole morphology Mol. Biol. Cell 12, 2396-2411 (Pubitemid 33051964)
7. 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
8. Rivas, M. P., Kearns, B. G., Xie, Z., Guo, S., Sekar, M. C., Hosaka, K., Kagiwada, S., York, J. D., and Bankaitis, V. A. (1999) Pleiotropic alterations in lipid metabolism in yeast sac1 mutants: Relationship to "bypass Sec14p" and inositol auxotrophy Mol. Biol. Cell 10, 2235-2250 (Pubitemid 29343132)
9. Wei, H. C., Sanny, J., Shu, H., Baillie, D. L., Brill, J. A., Price, J. V., and Harden, N. (2003) The Sac1 lipid phosphatase regulates cell shape change and the JNK cascade during dorsal closure in Drosophila Curr. Biol. 13, 1882-1887 (Pubitemid 37347931)
10. Liu, Y., Boukhelifa, M., Tribble, E., Morin-Kensicki, E., Uetrecht, A., Bear, J. E., and Bankaitis, V. A. (2008) The Sac1 phosphoinositide phosphatase regulates Golgi membrane morphology and mitotic spindle organization in mammals Mol. Biol. Cell 19, 3080-3096
11. Blagoveshchenskaya, A., Cheong, F. Y., Rohde, H. M., Glover, G., Knodler, A., Nicolson, T., Boehmelt, G., and Mayinger, P. (2008) Integration of Golgi trafficking and growth factor signaling by the lipid phosphatase SAC1 J. Cell Biol. 180, 803-812 (Pubitemid 351397779)
12. Zhong, R., Burk, D. H., Nairn, C. J., Wood-Jones, A., Morrison, W. H., III, and Ye, Z. H. (2005) Mutation of SAC1, an Arabidopsis SAC domain phosphoinositide phosphatase, causes alterations in cell morphogenesis, cell wall synthesis, and actin organization Plant Cell 17, 1449-1466 (Pubitemid 43138197)
13. Tahirovic, S., Schorr, M., and Mayinger, P. (2005) Regulation of intracellular phosphatidylinositol-4-phosphate by the Sac1 lipid phosphatase Traffic 6, 116-130
14. Liu, Y., Boukhelifa, M., Tribble, E., and Bankaitis, V. A. (2009) Functional studies of the mammalian Sac1 phosphoinositide phosphatase Adv. Enzyme Regul. 49, 75-86
15. Strahl, T. and Thorner, J. (2007) Synthesis and function of membrane phosphoinositides in budding yeast, Saccharomyces cerevisiae Biochim. Biophys. Acta 1771, 353-404 (Pubitemid 46428617)
16. Manford, A., Xia, T., Saxena, A. K., Stefan, C., Hu, F., Emr, S. D., and Mao, Y. (2010) Crystal structure of the yeast Sac1: Implications for its phosphoinositide phosphatase function EMBO J. 29, 1489-1498
17. Lee, J. O., Yang, H., Georgescu, M. M., Di Cristofano, A., Maehama, T., Shi, Y., Dixon, J. E., Pandolfi, P., and Pavletich, N. P. (1999) Crystal structure of the PTEN tumor suppressor: Implications for its phosphoinositide phosphatase activity and membrane association Cell 99, 323-334 (Pubitemid 29519911)
18. Begley, M. J., Taylor, G. S., Kim, S. A., Veine, D. M., Dixon, J. E., and Stuckey, J. A. (2003) Crystal structure of a phosphoinositide phosphatase, MTMR2: Insights into myotubular myopathy and Charcot-Marie-Tooth syndrome Mol. Cell 12, 1391-1402 (Pubitemid 38037009)
19. Stefan, C. J., Manford, A. G., Baird, D., Yamada-Hanff, J., Mao, Y., and Emr, S. D. (2011) Osh Proteins Regulate Phosphoinositide Metabolism at ER-Plasma Membrane Contact Sites Cell 144, 389-401
20. 31P-NMR spectroscopy Biophys. J. 83, 994-1003 (Pubitemid 34803632)
21. Wang, Y. K., Chen, W., Blair, D., Pu, M., Xu, Y., Miller, S. J., Redfield, A. G., Chiles, T. C., and Roberts, M. F. (2008) Insights into the structural specificity of the cytotoxicity of 3-deoxyphosphatidylinositols J. Am. Chem. Soc. 130, 7746-7755 (Pubitemid 351842138)
22. Kuzmic, P. (1996) Program DYNAFIT for the analysis of enzyme kinetic data: Application to HIV proteinase Anal. Biochem. 237, 260-273 (Pubitemid 26177089)
23. Schuck, P. (2000) Size-distribution analysis of macromolecules by sedimentation velocity ultracentrifugation and Lamm equation modeling Biophys. J. 78, 1606-1619 (Pubitemid 30141584)
24. Laue, T. M., Ridgeway, and T. M., and Pelletier, S. L. (1991) in Analytical Ultracentrifugation in Biochemistry and Polymer Science (Harding, S. E., Rowe, A. J., and Horton, J. C., Eds.) pp 90-125, Royal Society of Chemistry, Cambridge, U.K.
25. Baird, D., Stefan, C., Audhya, A., Weys, S., and Emr, S. D. (2008) Assembly of the PtdIns 4-kinase Stt4 complex at the plasma membrane requires Ypp1 and Efr3 J. Cell Biol. 183, 1061-1074
26. Hughes, W. E., Cooke, F. T., and Parker, P. J. (2000) Sac phosphatase domain proteins Biochem. J. 350 (Part 2) 337-352
27. Hughes, W. E., Woscholski, R., Cooke, F. T., Patrick, R. S., Dove, S. K., McDonald, N. Q., and Parker, P. J. (2000) SAC1 encodes a regulated lipid phosphoinositide phosphatase, defects in which can be suppressed by the homologous Inp52p and Inp53p phosphatases J. Biol. Chem. 275, 801-808 (Pubitemid 30051118)
28. Andersen, J. F. and Ribeiro, J. M. (2006) A secreted salivary inositol polyphosphate 5-phosphatase from a blood-feeding insect: Allosteric activation by soluble phosphoinositides and phosphatidylserine Biochemistry 45, 5450-5457 (Pubitemid 43673176)
29. Nemoto, Y., Kearns, B. G., Wenk, M. R., Chen, H., Mori, K., Alb, J. G., Jr., De Camilli, P., and Bankaitis, V. A. (2000) Functional characterization of a mammalian Sac1 and mutants exhibiting substrate-specific defects in phosphoinositide phosphatase activity J. Biol. Chem. 275, 34293-34305
30. Maehama, T., Taylor, G. S., Slama, J. T., and Dixon, J. E. (2000) A sensitive assay for phosphoinositide phosphatases Anal. Biochem. 279, 248-250 (Pubitemid 30165015)
31. Rabin, B. R. (1967) Co-operative effects in enzyme catalysis: A possible kinetic model based on substrate-induced conformation isomerization Biochem. J. 102, 22C-23C
32. Qian, H. (2008) Cooperativity and specificity in enzyme kinetics: A single-molecule time-based perspective Biophys. J. 95, 10-17
33. Campbell, R. B., Liu, F., and Ross, A. H. (2003) Allosteric activation of PTEN phosphatase by phosphatidylinositol 4,5-bisphosphate J. Biol. Chem. 278, 33617-33620 (Pubitemid 37553192)
34. Schaletzky, J., Dove, S. K., Short, B., Lorenzo, O., Clague, M. J., and Barr, F. A. (2003) Phosphatidylinositol-5-phosphate activation and conserved substrate specificity of the myotubularin phosphatidylinositol 3-phosphatases Curr. Biol. 13, 504-509 (Pubitemid 36345726)
35. Atkinson, K., Fogel, S., and Henry, S. A. (1980) Yeast mutant defective in phosphatidylserine synthesis J. Biol. Chem. 255, 6653-6661 (Pubitemid 10014091)
36. Roy, A. and Levine, T. P. (2004) Multiple pools of phosphatidylinositol 4-phosphate detected using the pleckstrin homology domain of Osh2p J. Biol. Chem. 279, 44683-44689 (Pubitemid 39430877)
37. Cornish-Bowden, A. and Cardenas, M. L. (1987) Co-operativity in monomeric enzymes J. Theor. Biol. 124, 1-23 (Pubitemid 17002610)
38. McConnachie, G., Pass, I., Walker, S. M., and Downes, C. P. (2003) Interfacial kinetic analysis of the tumour suppressor phosphatase, PTEN: Evidence for activation by anionic phospholipids Biochem. J. 371, 947-955 (Pubitemid 36578893)
39. Leventis, P. A. and Grinstein, S. (2010) The distribution and function of phosphatidylserine in cellular membranes Annu. Rev. Biophys. 39, 407-427
40. Cockcroft, S. (2009) Phosphatidic acid regulation of phosphatidylinositol 4-phosphate 5-kinases Biochim. Biophys. Acta 1791, 905-912
41. Moritz, A., De Graan, P. N., Gispen, W. H., and Wirtz, K. W. (1992) Phosphatidic acid is a specific activator of phosphatidylinositol-4-phosphate kinase J. Biol. Chem. 267, 7207-7210
42. Jenkins, G. H., Fisette, P. L., and Anderson, R. A. (1994) Type I phosphatidylinositol 4-phosphate 5-kinase isoforms are specifically stimulated by phosphatidic acid J. Biol. Chem. 269, 11547-11554 (Pubitemid 24200376)
43. Yeung, T., Gilbert, G. E., Shi, J., Silvius, J., Kapus, A., and Grinstein, S. (2008) Membrane phosphatidylserine regulates surface charge and protein localization Science 319, 210-213
44. Tani, M. and Kuge, O. (2010) Requirement of a specific group of sphingolipid-metabolizing enzyme for growth of yeast Saccharomyces cerevisiae under impaired metabolism of glycerophospholipids Mol. Microbiol. 78, 395-413
45. Kennedy, E. P. and Weiss, S. B. (1956) The function of cytidine coenzymes in the biosynthesis of phospholipides J. Biol. Chem. 222, 193-214