Structural basis for substrate recognition by a unique Legionella phosphoinositide phosphatase

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 34, 2012, Pages 13567-13572

  Hsu, FoSheng ^a,b   Zhu, Wenhan ^c   Brennan, Lucy ^b   Tao, Lili ^c   Luo, Zhao Qing ^c   Mao, Yuxin ^a,b  

^a School of Integrative Plant Sciences   (United States)

^b Department of Obstetrics Gynecology   (United States)

^c PURDUE UNIVERSITY   (United States)

Author keywords

Membrane trafficking; Phagocytosis; Phosphoinositide signaling; Type IV secretion system; Virulence factor

Indexed keywords

PHOSPHATIDYLINOSITIDE; SIDF PROTEIN; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ARTICLE; CATALYSIS; CONFORMATION; CRYSTAL STRUCTURE; ENZYME ACTIVITY; LEGIONELLA PNEUMOPHILA; NONHUMAN; PHAGOSOME; PRIORITY JOURNAL;

BACTERIAL PROTEINS; CATALYSIS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; HYDROLYSIS; LEGIONELLA PNEUMOPHILA; LIPIDS; MOLECULAR CONFORMATION; OXIDATION-REDUCTION; PHAGOCYTOSIS; PHAGOSOMES; PHOSPHATIDYLINOSITOLS; PHOSPHORIC MONOESTER HYDROLASES; PROTEIN STRUCTURE, TERTIARY; SUBSTRATE SPECIFICITY;

EID: 84865303538     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1207903109     Document Type: Article

References (42)

1. McDade JE, et al. (1977) Legionnaires' disease: Isolation of a bacterium and demonstration of its role in other respiratory disease. N Engl J Med 297:1197-1203.
2. Fraser DW, et al. (1977) Legionnaires' disease: Description of an epidemic of pneumonia. N Engl J Med 297:1189-1197.
3. McKinney RM, et al. (1981) Legionella longbeachae species nova, another etiologic agent of human pneumonia. Ann Intern Med 94:739-743.
4. Fields BS, Benson RF, Besser RE (2002) Legionella and Legionnaires' disease: 25 years of investigation. Clin Microbiol Rev 15:506-526.
5. Segal G, Purcell M, Shuman HA (1998) Host cell killing and bacterial conjugation require overlapping sets of genes within a 22-kb region of the Legionella pneumophila genome. Proc Natl Acad Sci USA 95:1669-1674.
6. Vogel JP, Andrews HL, Wong SK, Isberg RR (1998) Conjugative transfer by the virulence system of Legionella pneumophila. Science 279:873-876.
7. Isberg RR, O'Connor TJ, Heidtman M (2009) The Legionella pneumophila replication vacuole: Making a cosy niche inside host cells. Nat Rev Microbiol 7:13-24.
8. Hubber A, Roy CR (2010) Modulation of host cell function by Legionella pneumophila type IV effectors. Annu Rev Cell Dev Biol 26:261-283.
9. Odorizzi G, Babst M, Emr SD (2000) Phosphoinositide signaling and the regulation of membrane trafficking in yeast. Trends Biochem Sci 25:229-235.
10. De Matteis MA, Godi A (2004) PI-loting membrane traffic. Nat Cell Biol 6:487-492.
11. Di Paolo G, De Camilli P (2006) Phosphoinositides in cell regulation and membrane dynamics. Nature 443:651-657.
12. Ham H, Sreelatha A, Orth K (2011) Manipulation of host membranes by bacterial effectors. Nat Rev Microbiol 9:635-646.
13. Pizarro-Cerdá J, Cossart P (2004) Subversion of phosphoinositide metabolism by intracellular bacterial pathogens. Nat Cell Biol 6:1026-1033.
14. Niebuhr K, et al. (2002) 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.
15. House D, Bishop A, Parry C, Dougan G, Wain J (2001) Typhoid fever: Pathogenesis and disease. Curr Opin Infect Dis 14:573-578.
16. Bakowski MA, Braun V, Brumell JH (2008) Salmonella-containing vacuoles: Directing traffic and nesting to grow. Traffic 9:2022-2031.
17. Patel JC, Hueffer K, Lam TT, Galán JE (2009) Diversification of a Salmonella virulence protein function by ubiquitin-dependent differential localization. Cell 137:283-294.
18. Weber SS, Ragaz C, Reus K, Nyfeler Y, Hilbi H (2006) Legionella pneumophila exploits PI(4)P to anchor secreted effector proteins to the replicative vacuole. PLoS Pathog 2: e46.
19. Ragaz C, et al. (2008) The Legionella pneumophila phosphatidylinositol-4 phosphatebinding type IV substrate SidC recruits endoplasmic reticulum vesicles to a replicationpermissive vacuole. Cell Microbiol 10:2416-2433.
20. Weber SS, Ragaz C, Hilbi H (2009) The inositol polyphosphate 5-phosphatase OCRL1 restricts intracellular growth of Legionella, localizes to the replicative vacuole and binds to the bacterial effector LpnE. Cell Microbiol 11:442-460.
21. Norris FA, Wilson MP, Wallis TS, Galyov EE, Majerus PW (1998) SopB, a protein required for virulence of Salmonella dublin, is an inositol phosphate phosphatase. Proc Natl Acad Sci USA 95:14057-14059.
22. ZhuW, et al. (2011) Comprehensive identification of protein substrates of the Dot/Icm type IV transporter of Legionella pneumophila. PLoS ONE 6:e17638.
23. Maehama T, Taylor GS, Slama JT, Dixon JE (2000) A sensitive assay for phosphoinositide phosphatases. Anal Biochem 279:248-250.
24. Banga S, et al. (2007) Legionella pneumophila inhibits macrophage apoptosis by targeting pro-death members of the Bcl2 protein family. Proc Natl Acad Sci USA 104:5121-5126.
25. Taylor GS, Dixon JE (2001) An assay for phosphoinositide phosphatases utilizing fluorescent substrates. Anal Biochem 295:122-126.
26. Taylor GS, Maehama T, Dixon JE (2000) Myotubularin, a protein tyrosine phosphatase mutated in myotubular myopathy, dephosphorylates the lipid second messenger, phosphatidylinositol 3-phosphate. Proc Natl Acad Sci USA 97:8910-8915.
27. Guo S, Stolz LE, Lemrow SM, York JD (1999) SAC1-like domains of yeast SAC1, INP52, and INP53 and of human synaptojanin encode polyphosphoinositide phosphatases. J Biol Chem 274:12990-12995.
28. Erdmann KS, et al. (2007) A role of the Lowe syndrome protein OCRL in early steps of the endocytic pathway. Dev Cell 13:377-390.
29. Kamen LA, Levinsohn J, Swanson JA (2007) Differential association of phosphatidylinositol 3-kinase, SHIP-1, and PTEN with forming phagosomes. Mol Biol Cell 18:2463-2472.
30. Vieira OV, et al. (2001) Distinct roles of class I and class III phosphatidylinositol 3- kinases in phagosome formation and maturation. J Cell Biol 155:19-25.
31. Brombacher E, et al. (2009) Rab1 guanine nucleotide exchange factor SidM is a major phosphatidylinositol 4-phosphate-binding effector protein of Legionella pneumophila. J Biol Chem 284:4846-4856.
32. Manford A, et al. (2010) Crystal structure of the yeast Sac1: Implications for its phosphoinositide phosphatase function. EMBO J 29:1489-1498.
33. Holm L, Sander C (1995) Dali: A network tool for protein structure comparison. Trends Biochem Sci 20:478-480.
34. Barford D, Flint AJ, Tonks NK (1994) Crystal structure of human protein tyrosine phosphatase 1B. Science 263:1397-1404.
35. Stuckey JA, et al. (1994) Crystal structure of Yersinia protein tyrosine phosphatase at 2.5 A and the complex with tungstate. Nature 370:571-575.
36. Lee JO, et al. (1999) Crystal structure of the PTEN tumor suppressor: Implications for its phosphoinositide phosphatase activity and membrane association. Cell 99:323-334.
37. Begley MJ, et al. (2006) Molecular basis for substrate recognition by MTMR2, a myotubularin family phosphoinositide phosphatase. Proc Natl Acad Sci USA 103:927-932.
38. Begley MJ, et al. (2003) Crystal structure of a phosphoinositide phosphatase, MTMR2: Insights into myotubular myopathy and Charcot-Marie-Tooth syndrome. Mol Cell 12: 1391-1402.
39. Shin HW, et al. (2005) An enzymatic cascade of Rab5 effectors regulates phosphoinositide turnover in the endocytic pathway. J Cell Biol 170:607-618.
40. Vergne I, Chua J, Deretic V (2003) Mycobacterium tuberculosis phagosome maturation arrest: Selective targeting of PI3P-dependent membrane trafficking. Traffic 4:600-606.
41. Flannagan RS, Cosío G, Grinstein S (2009) Antimicrobial mechanisms of phagocytes and bacterial evasion strategies. Nat Rev Microbiol 7:355-366.
42. Puius YA, et al. (1997) Identification of a second aryl phosphate-binding site in protein- tyrosine phosphatase 1B: A paradigm for inhibitor design. Proc Natl Acad Sci USA 94:13420-13425.