Legionella pneumophila secretes a mitochondrial carrier protein during infection

PLoS Pathogens

Volumn 8, Issue 1, 2012, Pages

  Dolezal, Pavel ^a,b   Aili, Margareta ^c,f   Tong, Janette ^a   Jiang, Jhih Hang ^a,c   Marobbio, Carlo M ^d   Lee, Sau fung ^c   Schuelein, Ralf ^c   Belluzzo, Simon ^c   Binova, Eva ^b   Mousnier, Aurelie ^e   Frankel, Gad ^e   Giannuzzi, Giulia ^d   Palmieri, Ferdinando ^d   Gabriel, Kipros ^a   Naderer, Thomas ^a   Hartland, Elizabeth L ^c   Lithgow, Trevor ^a  

^a MONASH UNIVERSITY   (Australia)

^b CHARLES UNIVERSITY   (Czech Republic)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d UNIVERSITY OF BARI   (Italy)

^e IMPERIAL COLLEGE LONDON   (United Kingdom)

^f SWEDISH UNIVERSITY OF AGRICULTURAL SCIENCES   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE NUCLEOTIDE TRANSLOCASE; LEGIONELLA NUCLEOTIDE CARRIER PROTEIN; MEMBRANE PROTEIN; MITOCHONDRIAL CARRIER FAMILY; MITOCHONDRIAL PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL MEMBRANE; BACTERIAL SECRETION SYSTEM; BACTERIAL STRAIN; BACTERIUM CULTURE; EUKARYOTE; FEMALE; FUNGAL STRAIN; HELA CELL; HIDDEN MARKOV MODEL; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; LEGIONELLA PNEUMOPHILA; LEGIONNAIRE DISEASE; MACROPHAGE; NONHUMAN; PHENOTYPE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PURIFICATION; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; SEQUENCE ANALYSIS;

ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; CARRIER PROTEINS; GENETIC COMPLEMENTATION TEST; HELA CELLS; HUMANS; LEGIONELLA PNEUMOPHILA; LEGIONNAIRES' DISEASE; MEMBRANE PROTEINS; NEORICKETTSIA SENNETSU; SACCHAROMYCES CEREVISIAE;

BACTERIA (MICROORGANISMS); EUKARYOTA; LEGIONELLA; LEGIONELLA LONGBEACHAE; LEGIONELLA PNEUMOPHILA; NEORICKETTSIA SENNETSU;

EID: 84859790802     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1002459     Document Type: Article

References (94)

1. Horwitz MA, (1983) The Legionnaires' disease bacterium (Legionella pneumophila) inhibits phagosome-lysosome fusion in human monocytes. J Exp Med 158: 2108-2126.
2. Horwitz MA, Silverstein SC, (1980) Legionnaires' disease bacterium (Legionella pneumophila) multiples intracellularly in human monocytes. J Clin Invest 66: 441-450.
3. Kagan JC, Roy CR, (2002) Legionella phagosomes intercept vesicular traffic from endoplasmic reticulum exit sites. Nat Cell Biol 4: 945-954.
4. Horwitz MA, (1983) Formation of a novel phagosome by the Legionnaires' disease bacterium (Legionella pneumophila) in human monocytes. J Exp Med 158: 1319-1331.
5. Tilney LG, Harb OS, Connelly PS, Robinson CG, Roy CR, (2001) How the parasitic bacterium Legionella pneumophila modifies its phagosome and transforms it into rough ER: implications for conversion of plasma membrane to the ER membrane. J Cell Sci 114: 4637-4650.
6. 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.
7. Roy CR, Tilney LG, (2002) The road less traveled: transport of Legionella to the endoplasmic reticulum. J Cell Biol 158: 415-419.
8. Urwyler S, Nyfeler Y, Ragaz C, Lee H, Mueller LN, et al. (2009) Proteome analysis of Legionella vacuoles purified by magnetic immunoseparation reveals secretory and endosomal GTPases. Traffic 10: 76-87.
9. Dorer MS, Kirton D, Bader JS, Isberg RR, (2006) RNA interference analysis of Legionella in Drosophila cells: exploitation of early secretory apparatus dynamics. PLoS Pathog 2: e34.
10. 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 U S A 95: 1669-1674.
11. Segal G, Shuman HA, (1997) Characterization of a new region required for macrophage killing by Legionella pneumophila. Infect Immun 65: 5057-5066.
12. Vogel JP, Andrews HL, Wong SK, Isberg RR, (1998) Conjugative transfer by the virulence system of Legionella pneumophila. Science 279: 873-876.
13. Zhu W, Banga S, Tan Y, Zheng C, Stephenson R, et al. (2011) Comprehensive identification of protein substrates of the Dot/Icm type IV transporter of Legionella pneumophila. PLoS One 6: e17638.
14. Hubber A, Roy CR, (2010) Modulation of host cell function by Legionella pneumophila type IV effectors. Annu Rev Cell Dev Biol 26: 261-283.
15. Franco IS, Shuman HA, Charpentier X, (2009) The perplexing functions and surprising origins of Legionella pneumophila type IV secretion effectors. Cell Microbiol 11: 1435-1443.
16. Newton HJ, Ang DK, van Driel IR, Hartland EL, (2010) Molecular pathogenesis of infections caused by Legionella pneumophila. Clin Microbiol Rev 23: 274-298.
17. Weber SS, Ragaz C, Hilbi H, (2009) Pathogen trafficking pathways and host phosphoinositide metabolism. Mol Microbiol 71: 1341-1352.
18. Machner MP, Isberg RR, (2007) A bifunctional bacterial protein links GDI displacement to Rab1 activation. Science 318: 974-977.
19. Shohdy N, Efe JA, Emr SD, Shuman HA, (2005) Pathogen effector protein screening in yeast identifies Legionella factors that interfere with membrane trafficking. Proc Natl Acad Sci U S A 102: 4866-4871.
20. Ingmundson A, Delprato A, Lambright DG, Roy CR, (2007) Legionella pneumophila proteins that regulate Rab1 membrane cycling. Nature 450: 365-369.
21. 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.
22. Cazalet C, Rusniok C, Bruggemann H, Zidane N, Magnier A, et al. (2004) Evidence in the Legionella pneumophila genome for exploitation of host cell functions and high genome plasticity. Nature Genet 36: 1165-1173.
23. Pan X, Luhrmann A, Satoh A, Laskowski-Arce MA, Roy CR, (2008) Ankyrin repeat proteins comprise a diverse family of bacterial type IV effectors. Science 320: 1651-1654.
24. Price CT, Al-Quadan T, Santic M, Jones SC, Abu Kwaik Y, (2010) Exploitation of conserved eukaryotic host cell farnesylation machinery by an F-box effector of Legionella pneumophila. J Exp Med 207: 1713-1726.
25. Lomma M, Dervins-Ravault D, Rolando M, Nora T, Newton HJ, et al. (2010) The Legionella pneumophila F-box protein Lpp2082 (AnkB) modulates ubiquitination of the host protein parvin B and promotes intracellular replication. Cell Microbiol 12: 1272-1291.
26. Kubori T, Hyakutake A, Nagai H, (2008) Legionella translocates an E3 ubiquitin ligase that has multiple U-boxes with distinct functions. Mol Microbiol 67: 1307-1319.
27. Degtyar E, Zusman T, Ehrlich M, Segal G, (2009) A Legionella effector acquired from protozoa is involved in sphingolipids metabolism and is targeted to the host cell mitochondria. Cell Microbiol 11: 1219-1235.
28. Alcock F, Clements A, Webb C, Lithgow T, (2010) Evolution. Tinkering inside the organelle. Science 327: 649-650.
29. Jarmuszkiewicz W, Czarna M, Swida A, Behrendt M, (2004) Uncoupling Proteins in Amoeboid Eukaryotes, Acanthamoeba castellanii, and Dictyostelium discoideum. Toxicol Mech Methods 14: 3-6.
30. Chan KW, Slotboom DJ, Cox S, Embley TM, Fabre O, et al. (2005) A novel ADP/ATP transporter in the mitosome of the microaerophilic human parasite Entamoeba histolytica. Curr Biol 15: 737-742.
31. Satre M, Mattei S, Aubry L, Gaudet P, Pelosi L, et al. (2007) Mitochondrial carrier family: repertoire and peculiarities of the cellular slime mould Dictyostelium discoideum. Biochimie 89: 1058-1069.
32. Dolezal P, Dagley MJ, Kono M, Wolynec P, Likic VA, et al. (2010) The essentials of protein import in the degenerate mitochondrion of Entamoeba histolytica. PLoS Pathog 6: e1000812.
33. Young JC, Hoogenraad NJ, Hartl FU, (2003) Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70. Cell 112: 41-50.
34. Koehler CM, (2004) New developments in mitochondrial assembly. Annu Rev Cell Dev Biol 20: 309-335.
35. Gabriel K, Pfanner N, (2007) The mitochondrial machinery for import of precursor proteins. Methods Mol Biol 390: 99-117.
36. Neupert W, Herrmann JM, (2007) Translocation of proteins into mitochondria. Annu Rev Biochem 76: 723-749.
37. Chacinska A, Koehler CM, Milenkovic D, Lithgow T, Pfanner N, (2009) Importing mitochondrial proteins: machineries and mechanisms. Cell 138: 628-644.
38. Picault N, Hodges M, Palmieri L, Palmieri F, (2004) The growing family of mitochondrial carriers in Arabidopsis. Trends Plant Sci 9: 138-146.
39. Palmieri F, Pierri CL, (2010) Mitochondrial metabolite transport. Essays Biochem 47: 37-52.
40. Palmieri F, (2004) The mitochondrial transporter family (SLC25): physiological and pathological implications. Pflugers Arch 447: 689-709.
41. Palmieri F, Pierri CL, De Grassi A, Nunes-Nesi A, Fernie AR, (2011) Evolution, structure and function of mitochondrial carriers: a review with new insights. Plant J 66: 161-181.
42. Palmieri F, Pierri CL, (2010) Structure and function of mitochondrial carriers- role of the transmembrane helix P and G residues in the gating and transport mechanism. FEBS Lett 584: 1931-1939.
43. Rikihisa Y, (2003) Mechanisms to create a safe haven by members of the family Anaplasmataceae. Ann N Y Acad Sci 990: 548-555.
44. Walker DH, (2009) Sennetsu neorickettsiosis: a potentially prevalent, treatable, acutely incapacitating tropical infectious disease. Am J Trop Med Hyg 81: 187-188.
45. Schroeder GN, Petty NK, Mousnier A, Harding CR, Vogrin AJ, et al. (2010) Legionella pneumophila strain 130b possesses a unique combination of type IV secretion systems and novel Dot/Icm secretion system effector proteins. J Bacteriol 192: 6001-6016.
46. Cazalet C, Gomez-Valero L, Rusniok C, Lomma M, Dervins-Ravault D, et al. (2010) Analysis of the Legionella longbeachae genome and transcriptome uncovers unique strategies to cause Legionnaires' disease. PLoS Genet 6: e1000851.
47. Pebay-Peyroula E, Dahout-Gonzalez C, Kahn R, Trezeguet V, Lauquin GJ, et al. (2003) Structure of mitochondrial ADP/ATP carrier in complex with carboxyatractyloside. Nature 426: 39-44.
48. Greub G, Raoult D, (2003) History of the ADP/ATP-translocase-encoding gene, a parasitism gene transferred from a Chlamydiales ancestor to plants 1 billion years ago. App Environ Microbiol 69: 5530-5535.
49. Schmitz-Esser S, Linka N, Collingro A, Beier CL, Neuhaus HE, et al. (2004) ATP/ADP translocases: a common feature of obligate intracellular amoebal symbionts related to Chlamydiae and Rickettsiae. J Bacteriol 186: 683-691.
50. Trentmann O, Horn M, van Scheltinga AC, Neuhaus HE, Haferkamp I, (2007) Enlightening energy parasitism by analysis of an ATP/ADP transporter from chlamydiae. PLoS Biol 5: e231.
51. Cambronne ED, Roy CR, (2007) The Legionella pneumophila IcmSW complex interacts with multiple Dot/Icm effectors to facilitate type IV translocation. PLoS Pathog 3: e188.
52. Nagai H, Cambronne ED, Kagan JC, Amor JC, Kahn RA, et al. (2005) A C-terminal translocation signal required for Dot/Icm-dependent delivery of the Legionella RalF protein to host cells. Proc Natl Acad Sci U S A 102: 826-831.
53. Burstein D, Zusman T, Degtyar E, Viner R, Segal G, et al. (2009) Genome-scale identification of Legionella pneumophila effectors using a machine learning approach. PLoS Pathog 5: e1000508.
54. Truscott KN, Wiedemann N, Rehling P, Muller H, Meisinger C, et al. (2002) Mitochondrial import of the ADP/ATP carrier: the essential TIM complex of the intermembrane space is required for precursor release from the TOM complex. Mol Cell Biol 22: 7780-7789.
55. Ryan MT, Muller H, Pfanner N, (1999) Functional staging of ADP/ATP carrier translocation across the outer mitochondrial membrane. J Biol Chem 274: 20619-20627.
56. Kutik S, Rissler M, Guan XL, Guiard B, Shui G, et al. (2008) The translocator maintenance protein Tam41 is required for mitochondrial cardiolipin biosynthesis. J Cell Biol 183: 1213-1221.
57. Smith CP, Thorsness PE, (2008) The molecular basis for relative physiological functionality of the ADP/ATP carrier isoforms in Saccharomyces cerevisiae. Genetics 179: 1285-1299.
58. Cavero S, Traba J, Del Arco A, Satrustegui J, (2005) The calcium-dependent ATP-Mg/Pi mitochondrial carrier is a target of glucose-induced calcium signalling in Saccharomyces cerevisiae. Biochem J 392: 537-544.
59. Traba J, Satrustegui J, del Arco A, (2009) Characterization of SCaMC-3-like/slc25a41, a novel calcium-independent mitochondrial ATP-Mg/Pi carrier. Biochem J 418: 125-133.
60. Marzo I, Brenner C, Zamzami N, Jurgensmeier JM, Susin SA, et al. (1998) Bax and adenine nucleotide translocator cooperate in the mitochondrial control of apoptosis. Science 281: 2027-2031.
61. Palmieri F, Indiveri C, Bisaccia F, Iacobazzi V, (1995) Mitochondrial metabolite carrier proteins: purification, reconstitution, and transport studies. Methods Enzymol 260: 349-369.
62. Kol S, Nouwen N, Driessen AJ, (2008) Mechanisms of YidC-mediated insertion and assembly of multimeric membrane protein complexes. J Biol Chem 283: 31269-31273.
63. Xie K, Dalbey RE, (2008) Inserting proteins into the bacterial cytoplasmic membrane using the Sec and YidC translocases. Nat Rev Microbiol 6: 234-244.
64. Ninio S, Zuckman-Cholon DM, Cambronne ED, Roy CR, (2005) The Legionella IcmS-IcmW protein complex is important for Dot/Icm-mediated protein translocation. Mol Microbiol 55: 912-926.
65. Bardill JP, Miller JL, Vogel JP, (2005) IcmS-dependent translocation of SdeA into macrophages by the Legionella pneumophila type IV secretion system. Mol Microbiol 56: 90-103.
66. Vincent CD, Vogel JP, (2006) The Legionella pneumophila IcmS-LvgA protein complex is important for Dot/Icm-dependent intracellular growth. Mol Microbiol 61: 596-613.
67. Huang L, Boyd D, Amyot WM, Hempstead AD, Luo ZQ, et al. (2011) The E Block motif is associated with Legionella pneumophila translocated substrates. Cell Microbiol 13: 227-245.
68. Tusnady GE, Simon I, (2001) The HMMTOP transmembrane topology prediction server. Bioinformatics 17: 849-850.
69. Sonnhammer EL, von Heijne G, Krogh A, (1998) A hidden Markov model for predicting transmembrane helices in protein sequences. Proc Int Conf Intell Syst Mol Biol 6: 175-182.
70. Knirsch M, Gawaz MP, Klingenberg M, (1989) The isolation and reconstitution of the ADP/ATP carrier from wild-type Saccharomyces cerevisiae. Identification of primarily one type (AAC-2). FEBS Lett 244: 427-432.
71. Gawaz M, Douglas MG, Klingenberg M, (1990) Structure-function studies of adenine nucleotide transport in mitochondria. II. Biochemical analysis of distinct AAC1 and AAC2 proteins in yeast. J Biol Chem 265: 14202-14208.
72. Heimpel S, Basset G, Odoy S, Klingenberg M, (2001) Expression of the mitochondrial ADP/ATP carrier in Escherichia coli. Renaturation, reconstitution, and the effect of mutations on 10 positive residues. J Biol Chem 276: 11499-11506.
73. Spagnoletta A, De Santis A, Palmieri F, Genchi G, (2002) Purification and characterization of the reconstitutively active adenine nucleotide carrier from mitochondria of Jerusalem artichoke (Helianthus tuberosus L.) tubers. J Bioenerg Biomembr 34: 465-472.
74. Dolce V, Scarcia P, Iacopetta D, Palmieri F, (2005) A fourth ADP/ATP carrier isoform in man: identification, bacterial expression, functional characterization and tissue distribution. FEBS Lett 579: 633-637.
75. Fiermonte G, De Leonardis F, Todisco S, Palmieri L, Lasorsa FM, et al. (2004) Identification of the mitochondrial ATP-Mg/Pi transporter. Bacterial expression, reconstitution, functional characterization, and tissue distribution. J Biol Chem 279: 30722-30730.
76. Maeno E, Ishizaki Y, Kanaseki T, Hazama A, Okada Y, (2000) Normotonic cell shrinkage because of disordered volume regulation is an early prerequisite to apoptosis. Proc Natl Acad Sci U S A 97: 9487-9492.
77. Zamaraeva MV, Sabirov RZ, Maeno E, Ando-Akatsuka Y, Bessonova SV, et al. (2005) Cells die with increased cytosolic ATP during apoptosis: a bioluminescence study with intracellular luciferase. Cell Death Differ 12: 1390-1397.
78. Tsaousis AD, Kunji ER, Goldberg AV, Lucocq JM, Hirt RP, et al. (2008) A novel route for ATP acquisition by the remnant mitochondria of Encephalitozoon cuniculi. Nature 453: 553-556.
79. Dolezal P, Dagley MJ, Kono M, Wolynec P, Likic VA, et al. (2010) The essentials of protein import in the degenerate mitochondrion of Entamoeba histolytica. PLoS Pathog 6: e1000812.
80. Fritz-Laylin LK, Prochnik SE, Ginger ML, Dacks JB, Carpenter ML, et al. (2010) The genome of Naegleria gruberi illuminates early eukaryotic versatility. Cell 140: 631-642.
81. Likic VA, Dolezal P, Celik N, Dagley M, Lithgow T, (2010) Using hidden markov models to discover new protein transport machines. Methods Mol Biol 619: 271-284.
82. Eddy SR, (1998) Profile hidden Markov models. Bioinformatics 14: 755-763.
83. Arnold K, Bordoli L, Kopp J, Schwede T, (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22: 195-201.
84. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG, (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25: 4876-4882.
85. Chan NC, Lithgow T, (2008) The peripheral membrane subunits of the SAM complex function codependently in mitochondrial outer membrane biogenesis. Mol Biol Cell 19: 126-136.
86. Daum G, Bohni PC, Schatz G, (1982) Import of proteins into mitochondria. Cytochrome b2 and cytochrome c peroxidase are located in the intermembrane space of yeast mitochondria. J Biol Chem 257: 13028-13033.
87. Vergnolle MA, Alcock FH, Petrakis N, Tokatlidis K, (2007) Mutation of conserved charged residues in mitochondrial TIM10 subunits precludes TIM10 complex assembly, but does not abolish growth of yeast cells. J Mol Biol 371: 1315-1324.
88. Foo JH, Culvenor JG, Ferrero RL, Kwok T, Lithgow T, et al. (2010) Both the p33 and p55 subunits of the Helicobacter pylori VacA toxin are targeted to mammalian mitochondria. J Mol Biol 401: 792-798.
89. Gentle I, Gabriel K, Beech P, Waller R, Lithgow T, (2004) The Omp85 family of proteins is essential for outer membrane biogenesis in mitochondria and bacteria. J Cell Biol 164: 19-24.
90. Newton HJ, Sansom FM, Bennett-Wood V, Hartland EL, (2006) 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 74: 1683-1691.
91. Newton HJ, Sansom FM, Dao J, Cazalet C, Bruggemann H, et al. (2008) Significant role for ladC in initiation of Legionella pneumophila infection. Infect Immun 76: 3075-3085.
92. Hornung V, Bauernfeind F, Halle A, Samstad EO, Kono H, et al. (2008) Silica crystals and aluminum salts activate the NALP3 inflammasome through phagosomal destabilization. Nat Immunol 9: 847-856.
93. Fiermonte G, Dolce V, Palmieri F, (1998) Expression in Escherichia coli, functional characterization, and tissue distribution of isoforms A and B of the phosphate carrier from bovine mitochondria. J Biol Chem 273: 22782-22787.
94. Drgon T, Sabova L, Nelson N, Kolarov J, (1991) ADP/ATP translocator is essential only for anaerobic growth of yeast Saccharomyces cerevisiae. FEBS Lett 289: 159-162.