The Legionella pneumophila F-box protein Lpp2082 (AnkB) modulates ubiquitination of the host protein parvin B and promotes intracellular replication

Cellular Microbiology

Volumn 12, Issue 9, 2010, Pages 1272-1291

  Lomma, M ^a,b   Dervins Ravault, D ^a,b   Rolando, M ^a,b   Nora, T ^a,b   Newton, H J ^c   Sansom, F M ^c   Sahr, T ^c   Gomez Valero, L ^a,b   Jules, M ^a,b   Hartland, E L ^c   Buchrieser, C ^a,b  

^a INSTITUT PASTEUR   (France)

^b CNRS   (France)

^c UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

F BOX PROTEIN; UBIQUITIN PROTEIN LIGASE E3;

ACANTHAMOEBA CASTELLANII; ACANTHAMOEBA INFECTION; ARTICLE; BACTERIAL INFECTION; BACTERIAL STRAIN; BACTERIAL SURVIVAL; CELL DIVISION; CELL VACUOLE; EPITHELIUM CELL; EUKARYOTE; FLUORESCENCE ANALYSIS; FOCAL ADHESION; FRANCE; HUMAN; HUMAN CELL; HYBRID; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; IN VIVO STUDY; LAMELLIPODIUM; LEGIONELLA; LEGIONELLA PNEUMOPHILA; LUNG ALVEOLUS CELL; MACROPHAGE; MAMMAL CELL; MOUSE; MUTANT; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN INTERACTION; UBIQUITINATION; YEAST;

ACANTHAMOEBA CASTELLANII; ACTININ; ANIMALS; CELL LINE; EPITHELIAL CELLS; F-BOX PROTEINS; FEMALE; HOST-PATHOGEN INTERACTIONS; HUMANS; LEGIONELLA PNEUMOPHILA; LEGIONNAIRES' DISEASE; LUNG; MACROPHAGES; MICE; PHOSPHOPROTEINS; S-PHASE KINASE-ASSOCIATED PROTEINS; UBIQUITINATED PROTEINS; UBIQUITINATION;

ACANTHAMOEBA CASTELLANII; BACTERIA (MICROORGANISMS); EUKARYOTA; LEGIONELLA; LEGIONELLA PNEUMOPHILA; MAMMALIA; MUS;

EID: 77953704524     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2010.01467.x     Document Type: Article

References (90)

1. Abu-Zant A, Jones S, Asare R, Suttles J, Price C, Graham J, Kwaik YA. Anti-apoptotic signalling by the Dot/Icm secretion system of L. pneumophila. Cell Microbiol 2006, 9:246-264.
2. Albert-Weissenberger C, Cazalet C, Buchrieser C. Legionella pneumophila - a human pathogen that co-evolved with fresh water protozoa. Cell Mol Life Sci 2007, 64:432-448.
3. Al-Khodor S, Price CT, Habyarimana F, Kalia A, Abu Kwaik Y. A Dot/Icm-translocated ankyrin protein of Legionella pneumophila is required for intracellular proliferation within human macrophages and protozoa. Mol Microbiol 2008, 70:908-923.
4. Angot A, Peeters N, Lechner E, Vailleau F, Baud C, Gentzbittel L. Ralstonia solanacearum requires F-box-like domain-containing type III effectors to promote disease on several host plants. Proc Natl Acad Sci USA 2006, 103:14620-14625.
5. Aravind L, Koonin EV. The U box is a modified RING finger - a common domain in ubiquitination. Curr Biol 2000, 10:R132-R134.
6. Ardley HC, Robinson PA. E3 ubiquitin ligases. Essays Biochem 2005, 41:15-30.
7. d'Azzo A, Bongiovanni A, Nastasi T. E3 ubiquitin ligases as regulators of membrane protein trafficking and degradation. Traffic 2005, 6:429-441.
8. Bardill JP, Miller JL, Vogel JP. IcmS-dependent translocation of SdeA into macrophages by the Legionella pneumophila type IV secretion system. Mol Microbiol 2005, 56:90-103.
9. Bartel PL. Using the two-hybrid system to detect protein-protein interactions. Cellular Interactions in Development: A Practical Approach 1993, 153-179. Hartley DA. ed., Oxford, Oxford University Press, pp.
10. Bartfeld S, Engels C, Bauer B, Aurass P, Flieger A, Brüggemann H, Meyer TF. Temporal resolution of two-tracked NF-kappaB activation by Legionella pneumophila. Cell Microbiol 2009, 11:1638-1651.
11. Bonazzi M, Veiga E, Pizarro-Cerdá J, Cossart P. Successive post-translational modifications of E-cadherin are required for InlA-mediated internalization of Listeria monocytogenes. Cell Microbiol 2008, 10:2208-2222.
12. Brüggemann H, Hagman A, Jules M, Sismeiro O, Dillies M, Gouyette C. Virulence strategies for infecting phagocytes deduced from the in vivo transcriptional program of Legionella pneumophila. Cell Microbiol 2006, 8:1228-1240.
13. Cardozo T, Pagano M. The SCF ubiquitin ligase: insights into a molecular machine. Nat Rev Mol Cell Biol 2004, 5:739-751.
14. Cazalet C, Rusniok C, Bruggemann H, Zidane N, Magnier A, Ma L. Evidence in the Legionella pneumophila genome for exploitation of host cell functions and high genome plasticity. Nat Genet 2004, 36:1165-1173.
15. Cazalet C, Jarraud S, Ghavi-Helm Y, Kunst F, Glaser P, Etienne J, Buchrieser C. Multigenome analysis identifies a worldwide distributed epidemic Legionella pneumophila clone that emerged within a highly diverse species. Genome Res 2008, 18:431-441.
16. Chen J, de Felipe KS, Clarke M, Lu H, Anderson OR, Segal G, Shuman HA. Legionella effectors that promote nonlytic release from protozoa. Science 2004, 303:1358-1361.
17. Craig KL, Tyers M. The F-box: a new motif for ubiquitin dependent proteolysis in cell cycle regulation and signal transduction. Prog Biophys Mol Biol 1999, 72:299-328.
18. Dorer MS, Kirton D, Bader JS, Isberg RR. RNA interference analysis of Legionella in Drosophila cells: exploitation of early secretory apparatus dynamics. PLoS Pathog 2006, 2:e34.
19. Doye A, Boyer L, Mettouchi A, Lemichez E. Ubiquitin-mediated proteasomal degradation of Rho proteins by the CNF1 toxin. Methods Enzymol 2006, 406:447-456.
20. Feeley JC, Gibson RJ, Gorman GW, Langford NC, Rasheed JK, Mackel DC, Baine WB. Charcoal-yeast extract agar: primary isolation medium for Legionella pneumophila. J Clin Microbiol 1979, 10:437-441.
21. de Felipe KS, Pampou S, Jovanovic OS, Pericone CD, Ye SF, Kalachikov S, Shuman HA. Evidence for acquisition of Legionella type IV secretion substrates via interdomain horizontal gene transfer. J Bacteriol 2005, 187:7716-7726.
22. de Felipe KS, Glover RT, Charpentier X, Anderson OR, Reyes M, Pericone CD, Shuman HA. Legionella eukaryotic-like type IV substrates interfere with organelle trafficking. PLoS Pathog 2008, 4:e1000117.
23. Fields BS, Benson RF, Besser RE. Legionella and Legionnaires' disease: 25 years of investigation. Clin Microbiol Rev 2002, 15:506-526.
24. Filipenko NR, Attwell S, Roskelley C, Dedhar S. Integrin-linked kinase activity regulates Rac- and Cdc42-mediated actin cytoskeleton reorganization via alpha-PIX. Oncogene 2005, 24:5837-5849.
25. Formstecher E, Aresta S, Collura V, Hamburger A, Meil A, Trehin A. Protein interaction mapping: a Drosophila case study. Genome Res 2005, 15:376-384.
26. Fraser DW, Tsai TR, Orenstein W, Parkin WE, Beecham HJ, Sharrar RG. Legionnaires' disease: description of an epidemic of pneumonia. N Engl J Med 1977, 297:1189-1197.
27. Fromont-Racine M, Rain JC, Legrain P. Toward a functional analysis of the yeast genome through exhaustive two-hybrid screens. Nat Genet 1997, 16:277-282.
28. Fukuda T, Chen K, Shi X, Wu C. PINCH-1 is an obligate partner of integrin-linked kinase (ILK) functioning in cell shape modulation, motility, and surviva. J Biol Chem 2003, 278:51324-51333.
29. Gimona M, Djinovic-Carugo K, Kranewitter WJ, Winder SJ. Functional plasticity of CH domains. FEBS Lett 2002, 13:98-106.
30. Glaser P, Sakamoto H, Bellalou J, Ullmann A, Danchin A. Secretion of cyclolysin, the calmodulin-sensitive adenylate cyclase-haemolysin bifunctional protein of Bordetella pertussis. EMBO J 1988, 7:3997-4004.
31. Heo K, Kim B, Kim K, Choi J, Kim H, Zhan Y. Isolation and characterization of proteins associated with histone H3 tails in vivo. J Biol Chem 2007, 282:15476-15483.
32. Hershko A, Ciechanover A. The ubiquitin system. Annu Rev Biochem 1998, 67:425-479.
33. Horwitz MA. Formation of a novel phagosome by the Legionnaires' disease bacterium (Legionella pneumophila) in human monocytes. J Exp Med 1983, 158:1319-1331.
34. Isberg RR, O'Connor TJ, Heidtman M. The Legionella pneumophila replication vacuole: making a cosy niche inside host cells. Nat Rev Microbiol 2009, 7:13-24.
35. Ivanov SS, Roy CR. Modulation of ubiquitin dynamics and suppression of DALIS formation by the Legionella pneumophila Dot/Icm system. Cell Microbiol 2008, 11:261-278.
36. Janjusevic R, Abramovitch RB, Martin GB, Stebbins CE. A bacterial inhibitor of host programmed cell death defenses is an E3 ubiquitin ligase. Science 2006, 311:222-226.
37. Kagan JC, Roy CR. Legionella phagosomes intercept vesicular traffic from endoplasmic reticulum exit sites. Nat Cell Biol 2002, 4:945-954.
38. Kim DW, Lenzen G, Page AL, Legrain P, Sansonetti PJ, Parsot C. The Shigella flexneri effector OspG interferes with innate immune responses by targeting ubiquitin-conjugating enzymes. Proc Natl Acad Sci USA 2005, 102:14046-14051.
39. Kim M, Ogawa M, Fujita Y, Yoshikawa Y, Nagai T, Koyama T. Bacteria hijack integrin-linked kinase to stabilize focal adhesions and block cell detachment. Nature 2009, 459:578-582.
40. Kipreos ET, Pagano M. The F-box protein family. Genome Biol 2000, 1:3002.1-3002.7.
41. Korenbaum E, Olski TM, Noegel AA. Genomic organization and expression profile of the parvin family of focal adhesion proteins in mice and humans. Gene 2001, 279:69-79.
42. Krek W. BTB proteins as henchmen of Cul3-based ubiquitin ligases. Nat Cell Biol 2003, 5:950-951.
43. Kubori T, Galan JE. Temporal regulation of Salmonella virulence effector function by proteasome-dependent protein degradation. Cell 2003, 115:333-342.
44. Kubori T, Hyakutake A, Nagai H. Legionella translocates an E3 ubiquitin ligase that has multiple U-boxes with distinct functions. Mol Microbiol 2008, 67:1307-1319.
45. Legate KR, Montañez E, Kudlacek O, Fässler R. ILK, PINCH and parvin: the tIPP of integrin signalling. Nat Rev Mol Cell Biol 2006, 7:20-31.
46. Li W, Bengtson MH, Ulbrich A, Matsuda A, Reddy VA, Orth A. Genome-wide and functional annotation of human E3 ubiquitin ligases identifies MULAN, a mitochondrial E3 that regulates the organelle's dynamics and signaling. PLoS One 2008, 3:e1487.
47. Losick VP, Isberg RR. NF-kappaB translocation prevents host cell death after low-dose challenge by Legionella pneumophila. J Exp Med 2006, 203:2177-2189.
48. McDade JE, Shepard CC, Fraser DW, Tsai TR, Redus MA, Dowdle WR. Legionnaires' disease: isolation of a bacterium and demonstration of its role in other respiratory disease. N Engl J Med 1977, 297:1197-1203.
49. Matsuda C, Kameyama K, Suzuki A, Mishima W, Yamaji S, Okamoto H. Affixin activates Rac1 via betaPIX in C2C12 myoblast. FEBS Lett 2008, 582:1189-1196.
50. Munro P, Flatau G, Lemichez E. Bacteria and the ubiquitin pathway. Curr Opin Microbiol 2007, 10:39-46.
51. Nagai H, Kagan JC, Zhu X, Kahn RA, Roy CR. A bacterial guanine nucleotide exchange factor activates ARF on Legionella phagosomes. Science 2002, 295:679-682.
52. Nagai H, Cambronne ED, Kagan JC, Amor JC, Kahn RA, Roy CR. A C-terminal translocation signal required for Dot/Icm-dependent delivery of the Legionella RalF protein to host cells. Proc Natl Acad Sci USA 2005, 102:826-831.
53. Newton HJ, Sansom FM, Bennett-Wood V, Hartland EL. Identification of Legionella pneumophila-specific genes by genomic subtractive hybridization with Legionella micdadei and identification of lpnE, a gene required for efficient host cell entry. Infect Immun 2006, 74:1683-1691.
54. Newton HJ, Sansom FM, Dao J, Cazalet C, Bruggemann H, Albert-Weissenberger C. Significant role for ladC in initiation of Legionella pneumophila infection. Infect Immun 2008, 76:3075-3085.
55. Nora T, Lomma M, Gomez-Valero L, Buchrieser C. Molecular mimicry: an important virulence strategy employed by Legionella pneumophila to subvert host functions. Future Microbiol 2009, 4:691-701.
56. Ohi MD, Vander Kooi CW, Rosenberg JA, Chazin WJ, Gould KL. Structural insights into the U-box, a domain associated with multi-ubiquitination. Nat Struct Biol 2003, 10:250-255.
57. Olski TM, Noegel AA, Korenbaum E. Parvin, a 42 kDa focal adhesion protein, related to the alpha-actinin superfamily. J Cell Sci 2001, 114:525-538.
58. Pan X, Lührmann A, Satoh A, Laskowski-Arce MA, Roy CR. Ankyrin repeat proteins comprise a diverse family of bacterial type IV effectors. Science 2008, 320:1651-1654.
59. Price CT, Al-Khodor S, Al-Quadan T, Santic M, Habyarimana F, Kalia A, Kwaik YA. Molecular mimicry by an F-Box effector of Legionella pneumophila hijacks a conserved polyubiquitination machinery within macrophages and protozoa. PLoS Pathog 2009, 5:e1000704.
60. Randow F, Lehner PJ. Viral avoidance and exploitation of the ubiquitin system. Nat Cell Biol 2009, 11:527-534.
61. Rohde JR, Breitkreutz A, Chenal A, Sansonetti PJ, Parsot C. Type III secretion effectors of the IpaH family are E3 ubiquitin ligases. Cell Host Microbe 2007, 1:77-83.
62. Rolando M, Stefani C, Flatau G, Auberger P, Mettouchi A, Mhlanga M, Rapp U, Galmiche A, Lemichez E. Transcriptome dysregulation by anthrax lethal toxin plays a key role in induction of human endothelial cell cytotoxicity: Cell Microbiol 2010, 2010 Jan 20 [Epub ahead of print]. DOI 10.1111/j.1462-5822.2010.01438.x
63. Rytkonen A, Poh J, Garmendia J, Boyle C, Thompson A, Liu M. SseL, a Salmonella deubiquitinase required for macrophage killing and virulence. Proc Natl Acad Sci USA 2007, 104:3502-3507.
64. Sahr T, Bruggemann H, Jules M, Lomma M, Albert-Weissenberger C, Cazalet C, Buchrieser C. Two small ncRNAs jointly govern virulence and transmission in Legionella pneumophila. Mol Microbiol 2009, 72:741-762.
65. Schulman BA, Carrano AC, Jeffrey PD, Bowen Z, Kinnucan ER, Finnin MS. Insights into SCF ubiquitin ligases from the structure of the Skp1-Skp2 complex. Nature 2000, 408:381-386.
66. Sepulveda JL, Wu C. The parvins. Cell Mol Life Sci 2006, 63:25-35.
67. Shin S, Roy CR. Host cell processes that influence the intracellular survival of Legionella pneumophila. Cell Microbiol 2008, 10:1209-1220.
68. Singer AU, Rohde JR, Lam R, Skarina T, Kagan O, Dileo R. Structure of the Shigella T3SS effector IpaH defines a new class of E3 ubiquitin ligases. Nat Struct Mol Biol 2008, 15:1293-1301.
69. Skaar JR, D'Angiolella V, Pagan JK, Pagano M. SnapShot: F box proteins II. Cell 2009a, 137:1358-1358 e1351.
70. Skaar JR, Pagan JK, Pagano M. SnapShot: F box proteins I. Cell 2009b, 137:1160-1160 e1161.
71. Skaug B, Jiang X, Chen ZJ. The role of ubiquitin in NF-kappaB regulatory pathways. Annu Rev Biochem 2009, 78:769-796.
72. Sonnberg S, Seet BT, Pawson T, Fleming SB, Mercer AA. Poxvirus ankyrin repeat proteins are a unique class of F-box proteins that associate with cellular SCF1 ubiquitin ligase complexes. Proc Natl Acad Sci USA 2008, 105:10955-10960.
73. Sory MP, Cornelis GR. Translocation of a hybrid YopE-adenylate cyclase from Yersinia enterocolitica into HeLa cells. Mol Microbiol 1994, 14:583-594.
74. Steinert M, Heuner K, Buchrieser C, Albert-Weissenberger C, Glöckner G. Legionella pathogenicity: genome structure, regulatory networks and the host cell response. Int J Med Microbiol 2007, 297:577-587.
75. Stogios PJ, Downs GS, Jauhal JJ, Nandra SK, Privé GG. Sequence and structural analysis of BTB domain proteins. Genome Biol 2005, 6:R82.
76. Tiaden A, Spirig T, Weber SS, Brüggemann H, Bosshard R, Buchrieser C, Hilbi H. The Legionella pneumophila response regulator LqsR promotes virulence as an element of the regulatory network controlled by RpoS and LetA. Cell Microbiol 2007, 9:2903-2920.
77. Vojtek AB, Hollenberg SM. Ras-Raf interaction: two-hybrid analysis. Methods Enzymol 1995, 255:331-342.
78. Weber SS, 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 2006, 2:e46.
79. Willems AR, Schwab M, Tyers M. A hitchhiker's guide to the cullin ubiquitin ligases: SCF and its kin. Biochem Biophys Acta 2004, 1695:133-170.
80. Wilson K. Preparation of Genomic DNA from Bacteria 1997, New York, John Wiley and Sons, Inc
81. Wojcik J, Boneca IG, Legrain P. Prediction, assessment and validation of protein interaction maps in bacteria. J Mol Biol 2002, 323:763-770.
82. Wu C. The PINCH-ILK-parvin complexes: assembly, functions and regulation. Biochim Biophys Acta 2004, 1692:55-62.
83. Xu L, Wei Y, Reboul J, Vaglio P, Shin TH, Vidal M. BTB proteins are substrate-specific adaptors in an SCF-like modular ubiquitin ligase containing CUL-3. Nature 2003, 425:316-321.
84. Yamaji S, Suzuki A, Sugiyama Y, Koide Y, Yoshida M, Kanamori H. A novel integrin-linked kinase-binding protein, affixin, is involved in the early stage of cell-substrate interaction. J Cell Biol 2001, 153:1251-1264.
85. Yamaji S, Suzuki A, Kanamori H, Mishima W, Yoshimi R, Takasaki H. Affixin interacts with alpha-actinin and mediates integrin signaling for reorganization of F-actin induced by initial cell-substrate interaction. J Cell Biol 2004, 165:539-551.
86. Zhang L, Villa NY, McFadden G. Interplay between poxviruses and the cellular ubiquitin/ubiquitin-like pathways. FEBS Lett 2009, 583:607-614.
87. Zhang Y, Chen K, Tu Y, Wu C. Distinct roles of two structurally closely related focal adhesion proteins, alpha-parvins and beta-parvins, in regulation of cell morphology and survival. J Biol Chem 2004, 279:41695-41705.
88. Zhang Y, Higashide WM, McCormick BA, Chen J, Zhou D. The inflammation-associated Salmonella SopA is a HECT-like E3 ubiquitin ligase. Mol Microbiol 2006, 62:786-793.
89. Zheng N, Wang P, Jeffrey PD, Pavletich NP. Structure of a c-Cbl-UbcH7 complex: RING domain function in ubiquitin-protein ligases. Cell 2000, 102:533-539.
90. Zhou H, Monack DM, Kayagaki N, Wertz I, Yin J, Wolf B, Dixit VM. Yersinia virulence factor YopJ acts as a deubiquitinase to inhibit NF-kappa B activation. J Exp Med 2005, 202:1327-1332.