Modulation of membrane phosphoinositide dynamics by the phosphatidylinositide 4-kinase activity of the Legionella LepB effector

Nature Microbiology

Volumn 2, Issue , 2016, Pages

  Dong, Na ^a   Niu, Miao ^a,b   Hu, Liyan ^a   Yao, Qing ^a   Zhou, Rui ^a   Shao, Feng ^a  

^a NATIONAL INSTITUTE OF BIOLOGICAL SCIENCES   (China)

^b PEKING UNION MEDICAL COLLEGE   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; LEPB PROTEIN, LEGIONELLA PNEUMOPHILA; LIPID PHOSPHATE PHOSPHATASE; PHOSPHATIDATE PHOSPHATASE; PHOSPHATIDYLINOSITOL; PHOSPHATIDYLINOSITOL 3 PHOSPHATE; PHOSPHATIDYLINOSITOL 3,4-DIPHOSPHATE; PHOSPHATIDYLINOSITOL 4-PHOSPHATE; PHOSPHATIDYLINOSITOL KINASE; POLYPHOSPHOINOSITIDE;

CELL MEMBRANE; CHEMISTRY; HOST PATHOGEN INTERACTION; LEGIONELLA PNEUMOPHILA; METABOLISM; PROTEIN CONFORMATION; X RAY CRYSTALLOGRAPHY;

1-PHOSPHATIDYLINOSITOL 4-KINASE; BACTERIAL PROTEINS; CELL MEMBRANE; CRYSTALLOGRAPHY, X-RAY; HOST-PATHOGEN INTERACTIONS; LEGIONELLA PNEUMOPHILA; PHOSPHATIDATE PHOSPHATASE; PHOSPHATIDYLINOSITOL PHOSPHATES; PHOSPHATIDYLINOSITOLS; PROTEIN CONFORMATION;

EID: 85005973786     PISSN: None     EISSN: 20585276     Source Type: Journal    
DOI: 10.1038/nmicrobiol.2016.236     Document Type: Article

References (52)

1. Asrat, S., de Jesús, D. A., Hempstead, A. D., Ramabhadran, V., & Isberg, R. R. Bacterial pathogen manipulation of host membrane trafficking. Annu. Rev. Cell Dev. Biol. 30, 79-109 (2014
2. Dong, N., et al. Structurally distinct bacterial TBC-like GAPs link Arf GTPase to Rab1 inactivation to counteract host defenses. Cell 150, 1029-1041 (2012
3. Finsel, I., & Hilbi, H. Formation of a pathogen vacuole according to Legionella pneumophila: how to kill one bird with many stones. Cell Microbiol. 17, 935-950 (2015
4. Hubber, A., & Roy, C. R. Modulation of host cell function by Legionella pneumophila type IV effectors. Annu. Rev. Cell Dev. Biol. 26, 261-283 (2010
5. Ge, J., & Shao, F. Manipulation of host vesicular trafficking and innate immune defence by Legionella Dot/Icm effectors. Cell. Microbiol. 13, 1870-1880 (2011
6. Muller, M. P., et al. The Legionella effector protein DrrA AMPylates the membrane traffic regulator Rab1b. Science 329, 946-949 (2010
7. Machner, M. P., & Isberg, R. R. Targeting of host Rab GTPase function by the intravacuolar pathogen Legionella pneumophila. Dev. Cell 11, 47-56 (2006
8. Murata, T., et al. The Legionella pneumophila effector protein DrrA is a Rab1 guanine nucleotide-exchange factor. Nat. Cell Biol. 8, 971-977 (2006
9. Schoebel, S., Oesterlin, L. K., Blankenfeldt, W., Goody, R. S., & Itzen, A. RabGDI displacement by DrrA from Legionella is a consequence of its guanine nucleotide exchange activity. Mol. Cell 36, 1060-1072 (2009
10. Suh, H. Y., et al. Structural insights into the dual nucleotide exchange and GDI displacement activity of SidM/DrrA. EMBO J. 29, 496-504 (2010
11. Zhu, Y., et al. Structural mechanism of host Rab1 activation by the bifunctional Legionella type IV effector SidM/DrrA. Proc. Natl Acad. Sci. USA 107, 4699-4704 (2010
12. Brombacher, E., et al. Rab1 guanine nucleotide exchange factor SidM is a major phosphatidylinositol 4-phosphate-binding effector protein of Legionella pneumophila. J. Biol. Chem. 284, 4846-4856 (2009
13. Ingmundson, A., Delprato, A., Lambright, D. G., & Roy, C. R. Legionella pneumophila proteins that regulate Rab1 membrane cycling. Nature 450, 365-369 (2007
14. Neunuebel, M. R., et al. De-AMPylation of the small GTPase Rab1 by the pathogen Legionella pneumophila. Science 333, 453-456 (2011
15. Tan, Y., & Luo, Z. Q. Legionella pneumophila SidD is a deAMPylase that modifies Rab1. Nature 475, 506-509 (2011
16. Tan, Y., Arnold, R. J., & Luo, Z. Q. Legionella pneumophila regulates the small GTPase Rab1 activity by reversible phosphorylcholination. Proc. Natl Acad. Sci. USA 108, 21212-21217 (2011
17. Niebuhr, K., et al. Conversion of PtdIns(4,5)P(2) into PtdIns(5)P by the S. flexneri effector ipgD reorganizes host cell morphology. EMBO J. 21, 5069-5078 (2002
18. Norris, F. A., Wilson, M. P., Wallis, T. S., Galyov, E. E., & Majerus, P. W. Sopb, a protein required for virulence of Salmonella dublin, is an inositol phosphate phosphatase. Proc. Natl Acad. Sci. USA 95, 14057-14059 (1998
19. Broberg, C. A., Zhang, L., Gonzalez, H., Laskowski-Arce, M. A., & Orth, K. A Vibrio effector protein is an inositol phosphatase and disrupts host cell membrane integrity. Science 329, 1660-1662 (2010
20. Weber, S. S., Ragaz, C., Reus, K., Nyfeler, Y., & Hilbi, H. Legionella pneumophila exploits PI(4)P to anchor secreted effector proteins to the replicative vacuole. PLoS Pathog. 2, e46 (2006
21. Mihai Gazdag, E., et al. Mechanism of Rab1b deactivation by the Legionella pneumophila GAP LepB. EMBO Rep. 14, 199-205 (2013
22. Mishra, A. K., Del Campo, C. M., Collins, R. E., Roy, C. R., & Lambright, D. G. The Legionella pneumophila GTPase activating protein LepB accelerates Rab1 deactivation by a non-canonical hydrolytic mechanism. J. Biol. Chem. 288, 24000-24011 (2013
23. Yu, Q., et al. Structural analyses of Legionella LepB reveal a new GAP fold that catalytically mimics eukaryotic RasGAP. Cell Res. 23, 775-787 (2013
24. Heidtman, M., Chen, E. J., Moy, M. Y., & Isberg, R. R. Large-scale identification of Legionella pneumophila Dot/Icm substrates that modulate host cell vesicle trafficking pathways. Cell. Microbiol. 11, 230-248 (2009
25. Storrie, B., et al. Recycling of Golgi-resident glycosyltransferases through the ER reveals a novel pathway and provides an explanation for nocodazole-induced Golgi scattering. J. Cell Biol. 143, 1505-1521 (1998
26. Presley, J. F., et al. ER-to-Golgi transport visualized in living cells. Nature 389, 81-85 (1997
27. Kim, D. J., et al. Helicobacter pylori proinflammatory protein up-regulates NF-?B as a cell-translocating Ser/Thr kinase. Proc. Natl Acad. Sci. USA 107, 21418-21423 (2010
28. Steinbacher, S., et al. The crystal structure of the Physarum polycephalum actinfragmin kinase: an atypical protein kinase with a specialized substrate-binding domain. EMBO J. 18, 2923-2929 (1999
29. 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
30. Levine, T. P., & Munro, S. The pleckstrin homology domain of oxysterol-binding protein recognises a determinant specific to Golgi membranes. Curr. Biol. 8, 729-739 (1998
31. Halet, G. Imaging phosphoinositide dynamics using GFP-tagged protein domains. Biol. Cell 97, 501-518 (2005
32. Tai, A. W., Bojjireddy, N., & Balla, T. A homogeneous and nonisotopic assay for phosphatidylinositol 4-kinases. Anal. Biochem. 417, 97-102 (2011
33. Hsu, F., et al. Structural basis for substrate recognition by a unique Legionella phosphoinositide phosphatase. Proc. Natl Acad. Sci. USA 109, 13567-13572 (2012
34. Rudge, S. A., Anderson, D. M., & Emr, S. D. Vacuole size control: regulation of PtdIns(3,5)P2 levels by the vacuole-Associated Vac14-Fig4 complex, a PtdIns (3,5)P2-specific phosphatase. Mol. Biol. Cell 15, 24-36 (2004
35. Balla, A., & Balla, T. Phosphatidylinositol 4-kinases: old enzymes with emerging functions. Trends Cell Biol. 16, 351-361 (2006
36. Baumlova, A., et al. The crystal structure of the phosphatidylinositol 4-kinase IIa. EMBO Rep. 15, 1085-1092 (2014
37. Burke, J. E., et al. Structures of PI4KIIIβ complexes show simultaneous recruitment of Rab11 and its effectors. Science 344, 1035-1038 (2014
38. Zhou, Q., et al. Molecular insights into the membrane-Associated phosphatidylinositol 4-kinase IIa. Nat. Commun. 5, 3552 (2014
39. Toulabi, L., Wu, X., Cheng, Y., & Mao, Y. Identification and structural characterization of a Legionella phosphoinositide phosphatase. J. Biol. Chem. 288, 24518-24527 (2013
40. Hubber, A., et al. The machinery at endoplasmic reticulum-plasma membrane contact sites contributes to spatial regulation of multiple Legionella effector proteins. PLoS Pathog. 10, e1004222 (2014
41. Ragaz, C., et al. The Legionella pneumophila phosphatidylinositol-4 phosphatebinding type IV substrate SidC recruits endoplasmic reticulum vesicles to a replication-permissive vacuole. Cell. Microbiol. 10, 2416-2433 (2008
42. Gaspar, A. H., & Machner, M. P. Vipd is a Rab5-Activated phospholipase A1 that protects Legionella pneumophila from endosomal fusion. Proc. Natl Acad. Sci. USA 111, 4560-4565 (2014
43. Ku, B., et al. Vipd of Legionella pneumophila targets activated Rab5 and Rab22 to interfere with endosomal trafficking in macrophages. PLoS Pathog. 8, e1003082 (2012
44. Pizarro-Cerdá, J., Kühbacher, A., & Cossart, P. Phosphoinositides and host- pathogen interactions. Biochim. Biophys. Acta 1851, 911-918 (2015
45. Cazalet, C., et al. Analysis of the Legionella longbeachae genome and transcriptome uncovers unique strategies to cause Legionnaires disease. PLoS Genet. 6, e1000851 (2010
46. Vergne, I., et al. Mechanism of phagolysosome biogenesis block by viable Mycobacterium tuberculosis. Proc. Natl Acad. Sci. USA 102, 4033-4038 (2005
47. Rao, V. D., Misra, S., Boronenkov, I. V., Anderson, R. A., & Hurley, J. H. Structure of type IIβ phosphatidylinositol phosphate kinase: a protein kinase fold flattened for interfacial phosphorylation. Cell 94, 829-839 (1998
48. Fiume, R., et al. PIP4K and the role of nuclear phosphoinositides in tumour suppression. Biochim. Biophys. Acta 1851, 898-910 (2015
49. de Graaf, P., et al. Phosphatidylinositol 4-kinaseβ is critical for functional association of rab11 with the Golgi complex. Mol. Biol. Cell 15, 2038-2047 (2004
50. Levine, T. P., & Munro, S. Targeting of Golgi-specific pleckstrin homology domains involves both PtdIns 4-kinase-dependent and -independent components. Curr. Biol. 12, 695-704 (2002
51. Adams, P. D., et al. Phenix: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D 66, 213-221 (2010
52. Emsley, P., & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D 60, 2126-2132 (2004