Molecular insights into the membrane-associated phosphatidylinositol 4-kinase IIα

Nature Communications

Volumn 5, Issue , 2014, Pages

  Zhou, Qiangjun ^a,b   Li, Jiangmei ^a   Yu, Hang ^c   Zhai, Yujia ^a   Gao, Zhen ^a,b   Liu, Yanxin ^d   Pang, Xiaoyun ^a,b   Zhang, Lunfeng ^a,b   Schulten, Klaus ^c,d   Sun, Fei ^a   Chen, Chang ^a,e  

^a INSTITUTE OF BIOPHYSICS   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^d University of Illinois at Urbana Champaign   (United States)

^e BEIJING INSTITUTE FOR BRAIN DISORDERS   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; NUCLEOTIDE; PHOSPHATIDYLINOSITOL; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 4 KINASE IIALPHA; PHOSPHATIDYLINOSITOL KINASE; UNCLASSIFIED DRUG;

ALCOHOL; CRYSTAL STRUCTURE; ENZYME ACTIVITY; MEMBRANE; MOLECULAR ANALYSIS;

ANIMAL CELL; ARTICLE; BACTERIUM; CELL GROWTH; CELL MEMBRANE; CHEMICAL ANALYSIS; CRYSTAL STRUCTURE; ENZYME ACTIVITY; MEMBRANE BINDING; MOLECULAR DYNAMICS; MUTAGENESIS; NONHUMAN; NUCLEOTIDE BINDING SITE; PALMITOYLATION; PROTEIN CONFORMATION; PROTEIN EXPRESSION; PROTEIN FUNCTION;

ADENOSINE DIPHOSPHATE; AMINO ACID MOTIFS; CELL MEMBRANE; HUMANS; LIPOYLATION; PHOSPHATIDYLINOSITOLS; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT;

EID: 84897469754     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms4552     Document Type: Article

References (58)

1. Lu, D. et al. Phosphatidylinositol 4-Kinase IIalpha Is Palmitoylated by Golgi-localized Palmitoyltransferases in Cholesterol-dependent Manner. J. Biol. Chem. 287, 21856-21865 (2012
2. Minogue, S. & Waugh, M. G. The phosphatidylinositol 4-Kinases: don't call it a comeback. Subcell. Biochem. 58, 1-24 (2012
3. Salazar, G. et al. Phosphatidylinositol-4-kinase type II alpha is a component of adaptor protein-3-derived vesicles. Mol. Biol. Cell 16, 3692-3704 (2005 (Pubitemid 41077079)
4. Wang, J. et al. PI4P promotes the recruitment of the GGA adaptor proteins to the trans-Golgi network and regulates their recognition of the ubiquitin sorting signal. Mol. Biol. Cell 18, 2646-2655 (2007 (Pubitemid 47025729)
5. Wang, Y. J. et al. Phosphatidylinositol 4 phosphate regulates targeting of clathrin adaptor AP-1 complexes to the Golgi. Cell 114, 299-310 (2003 (Pubitemid 36962929)
6. Li, J. et al. PI4KIIalpha is a novel regulator of tumor growth by its action on angiogenesis and HIF-1alpha regulation. Oncogene 29, 2550-2559 (2010
7. Minogue, S. et al. Phosphatidylinositol 4-kinase is required for endosomal trafficking and degradation of the EGF receptor. J. Cell. Sci. 119, 571-581 (2006
8. Pan, W. et al. Wnt3a-mediated formation of phosphatidylinositol 4,5- bisphosphate regulates LRP6 phosphorylation. Science 321, 1350-1353 (2008
9. Pizarro-Cerda, J. et al. Type II phosphatidylinositol 4-kinases promote Listeria monocytogenes entry into target cells. Cell Microbiol. 9, 2381-2390 (2007 (Pubitemid 47365644)
10. Guo, J. et al. Phosphatidylinositol 4-kinase type IIalpha is responsible for the phosphatidylinositol 4-kinase activity associated with synaptic vesicles. Proc. Natl Acad. Sci. USA 100, 3995-4000 (2003 (Pubitemid 36418145)
11. Simons, J. P. et al. Loss of phosphatidylinositol 4-kinase 2alpha activity causes late onset degeneration of spinal cord axons. Proc. Natl Acad. Sci. USA 106, 11535-11539 (2009
12. Jovic, M. et al. Two phosphatidylinositol 4-kinases control lysosomal delivery of the Gaucher disease enzyme, beta-glucocerebrosidase. Mol. Biol. Cell 23, 1533-1545 (2012
13. Wu, B., Kitagawa, K., Zhang, N. Y., Liu, B. & Inagaki, C. Pathophysiological concentrations of amyloid beta proteins directly inhibit rat brain and recombinant human type II phosphatidylinositol 4-kinase activity. J. Neurochem. 91, 1164-1170 (2004 (Pubitemid 39587454)
14. Kang, M. S. et al. Modulation of lipid kinase PI4KIIalpha activity and lipid raft association of presenilin 1 underlies gamma-secretase inhibition by ginsenoside(20S)Rg3. J. Biol. Chem. 288, 20868-20882 (2013
15. Balla, A. & Balla, T. Phosphatidylinositol 4-kinases: old enzymes with emerging functions. Trends Cell Biol. 16, 351-361 (2006 (Pubitemid 44062315)
16. Whitman, M., Kaplan, D., Roberts, T. & Cantley, L. Evidence for two distinct phosphatidylinositol kinases in fibroblasts. Implications for cellular regulation. Biochem. J. 247, 165-174 (1987
17. Endemann, G., Dunn, S. N. & Cantley, L. C. Bovine brain contains two types of phosphatidylinositol kinase. Biochemistry 26, 6845-6852 (1987
18. Knight, Z. A. & Shokat, K. M. Chemically targeting the PI3K family. Biochem. Soc. Trans. 35, 245-249 (2007 (Pubitemid 46596480)
19. Folkes, A. J. et al. The identification of 2-(1H-indazol-4-yl)-6-(4- methanesulfonyl-piperazin-1-ylmethyl)-4-morpholin-4-yl-thieno[3,2- d]pyrimidine (GDC-0941) as a potent, selective, orally bioavailable inhibitor of class I PI3 kinase for the treatment of cancer. J. Med. Chem. 51, 5522-5532 (2008
20. Berndt, A. et al. The p110delta structure: mechanisms for selectivity and potency of new PI(3)K inhibitors. Nat. Chem. Biol. 6, 244 (2010
21. Walker, E. H., Perisic, O., Ried, C., Stephens, L. & Williams, R. L. Structural insights into phosphoinositide 3-kinase catalysis and signalling. Nature 402, 313-320 (1999 (Pubitemid 129516270)
22. Miller, S. et al. Shaping development of autophagy inhibitors with the structure of the lipid kinase Vps34. Science 327, 1638-1642 (2010
23. Pacold, M. E. et al. Crystal structure and functional analysis of Ras binding to its effector phosphoinositide 3-kinase gamma. Cell 103, 931-943 (2000
24. Rao, V. D., Misra, S., Boronenkov, I. V., Anderson, R. A. & Hurley, J. H. Structure of type IIbeta phosphatidylinositol phosphate kinase: a protein kinase fold flattened for interfacial phosphorylation. Cell 94, 829-839 (1998 (Pubitemid 28436014)
25. Wipf, P. et al. Synthesis and biological evaluation of synthetic viridins derived from C(20)-heteroalkylation of the steroidal PI-3-kinase inhibitor wortmannin. Org. Biomol. Chem. 2, 1911-1920 (2004
26. Fruman, D. A. & Rommel, C. PI3Kdelta inhibitors in cancer: rationale and serendipity merge in the clinic. Cancer Discov. 1, 562-572 (2011
27. Raynaud, F. I. et al. Pharmacologic characterization of a potent inhibitor of class I phosphatidylinositide 3-kinases. Cancer Res. 67, 5840-5850 (2007 (Pubitemid 46985018)
28. Barylko, B. et al. A novel family of phosphatidylinositol 4-kinases conserved from yeast to humans. J. Biol. Chem. 276, 7705-7708 (2001
29. Barylko, B. et al. Palmitoylation controls the catalytic activity and subcellular distribution of phosphatidylinositol 4-kinase II{alpha}. J. Biol. Chem. 284, 9994-10003 (2009
30. Minogue, S. et al. Relationship between phosphatidylinositol 4-phosphate synthesis, membrane organization, and lateral diffusion of PI4KII alpha at the trans-Golgi network. J. Lipid Res. 51, 2314-2324 (2010
31. Waugh, M. G., Minogue, S., Chotai, D., Berditchevski, F. & Hsuan, J. J. Lipid and peptide control of phosphatidylinositol 4-kinase IIalpha activity on Golgi-endosomal Rafts. J. Biol. Chem. 281, 3757-3763 (2006 (Pubitemid 43847799)
32. Banerji, S. et al. Oxysterol binding protein-dependent activation of sphingomyelin synthesis in the golgi apparatus requires phosphatidylinositol 4-kinase IIalpha. Mol. Biol. Cell 21, 4141-4150 (2010
33. Barylko, B. et al. Analysis of the catalytic domain of phosphatidylinositol 4-kinase type II. J. Biol. Chem. 277, 44366-44375 (2002 (Pubitemid 36157872)
34. Krissinel, E. & Henrick, K. Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774-797 (2007 (Pubitemid 47321791)
35. Holm, L. & Rosenstrom, P. Dali server: conservation mapping in 3D. Nucleic Acids Res. 38, W545-W549 (2010
36. Ladokhin, A. S., Jayasinghe, S. & White, S. H. How to measure and analyze tryptophan fluorescence in membranes properly, and why bother? Anal. Biochem. 285, 235-245 (2000
37. Bondeva, T. et al. Bifurcation of lipid and protein kinase signals of PI3Kgamma to the protein kinases PKB and MAPK. Science 282, 293-296 (1998 (Pubitemid 28487201)
38. Macphee, C. H. et al. The stereoselective recognition of substrates by phosphoinositide kinases. Studies using synthetic stereoisomers of dipalmitoyl phosphatidylinositol. J. Biol. Chem. 267, 11137-11143 (1992
39. Ho, B. K. & Gruswitz, F. HOLLOW: generating accurate representations of channel and interior surfaces in molecular structures. BMC Struct. Biol. 8, 49 (2008
40. Doublie, S. Preparation of selenomethionyl proteins for phase determination. Methods Enzymol. 276, 523-530 (1997 (Pubitemid 27085620)
41. Stoscheck, C. M. Quantitation of protein. Methods Enzymol. 182, 50-68 (1990 (Pubitemid 20154379)
42. Otwinowski, Z. & Minor, W. Processing of X-ray diffraction data collected in the oscillation mode. Methods Enzymol. 276, 307-326 (1997 (Pubitemid 27085611)
43. Schneider, T. R. & Sheldrick, G. M. Substructure solution with SHELXD. Acta. Crystallogr. D Biol. Crystallogr. 58, 1772-1779 (2002 (Pubitemid 35169744)
44. Pape, T. & Schneider, T. R. HKL2MAP: a graphical user interface for macromolecular phasing with SHELX programs. J. Appl. Crystallogr. 37, 843-844 (2004
45. Terwilliger, T. C. & Berendzen, J. Automated MAD and MIR structure solution. Acta Crystallogr. D Biol. Crystallogr 55, 849-861 (1999 (Pubitemid 29194533)
46. Terwilliger, T. C. Maximum-likelihood density modification. Acta Crystallogr. D Biol. Crystallogr. 56, 965-972 (2000 (Pubitemid 30622779)
47. Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta. Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (2004 (Pubitemid 41742764)
48. Murshudov, G. N., Vagin, A. A. & Dodson, E. J. Refinement of macromolecular structures by the maximum-likelihood method. Acta. Crystallogr. D Biol. Crystallogr. 53, 240-255 (1997 (Pubitemid 27235885)
49. McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Cryst. 40, 658-674 (2007 (Pubitemid 47080256)
50. Laskowski, R. A., MacArthur, M. W., Moss, D. S. & Thornton, J. M. PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Cryst. 26, 283-291 (1993
51. Chen, V. B. et al. MolProbity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66, 12-21 (2010)
52. Lasic, D. D. The mechanism of vesicle formation. Biochem. J. 256, 1-11 (1988
53. Levy, D., Bluzat, A., Seigneuret, M. & Rigaud, J. L. A systematic study of liposome and proteoliposome reconstitution involving bio-bead-mediated Triton-X-100 removal. Biochim. Biophys. Acta 1025, 179-190 (1990 (Pubitemid 20199626)
54. Tai, A. W., Bojjireddy, N. & Balla, T. A homogeneous and nonisotopic assay for phosphatidylinositol 4-kinases. Anal. Biochem. 417, 97-102 (2011
55. Jorgensen, W. L., Chandrasekhar, J., Madura, J. D., Impey, R. W. & Klein, M. L. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79, 926-935 (1983
56. Mayne, C. G., Saam, J., Schulten, K., Tajkhorshid, E. & Gumbart, J. C. Rapid parameterization of small molecules using the Force Field Toolkit. J. Comput. Chem. 34, 2757-2770 (2013
57. Phillips, J. C. et al. Scalable molecular dynamics with NAMD. J. Comput. Chem. 26, 1781-1802 (2005 (Pubitemid 43078511)
58. Humphrey, W., Dalke, A. & Schulten, K. VMD: visual molecular dynamics. J. Mol. Graph. 14, 33-38 (1996) (Pubitemid 26152973)