The Pseudomonas aeruginosa patatin-like protein PlpD is the archetype of a novel Type V secretion system

Environmental Microbiology

Volumn 12, Issue 6, 2010, Pages 1498-1512

  Salacha, Richard ^a   Kovačić, Filip ^b   Brochier Armanet, Céline ^a   Wilhelm, Susanne ^b   Tommassen, Jan ^c   Filloux, Alain ^a,d   Voulhoux, Romé ^a   Bleves, Sophie ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

^b HEINRICH HEINE UNIVERSITY   (Germany)

^c UTRECHT UNIVERSITY   (Netherlands)

^d IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CARBOXYLESTERASE; PATATIN PROTEIN, SOLANUM TUBEROSUM; VEGETABLE PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; CHEMICAL STRUCTURE; CHEMISTRY; CLASSIFICATION; ENZYMOLOGY; EXOCYTOSIS; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; PSEUDOMONAS AERUGINOSA; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; CARBOXYLIC ESTER HYDROLASES; EXOCYTOSIS; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PLANT PROTEINS; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; PSEUDOMONAS AERUGINOSA; SEQUENCE ALIGNMENT;

EID: 77957956351     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/j.1462-2920.2010.02174.x     Document Type: Article

References (63)

1. Arpigny, J.L., and Jaeger, K.E. (1999) Bacterial lipolytic enzymes: classification and properties. Biochem J 343 (Part 1): 177-183.
2. Banerji, S., and Flieger, A. (2004) Patatin-like proteins: a new family of lipolytic enzymes present in bacteria? Microbiology 150: 522-525.
3. Bendtsen, J.D., Nielsen, H., von Heijne, G., and Brunak, S (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340
4. Berven, F.S., Flikka, K., Jensen, H.B., and Eidhammer, I. (2004) BOMP: a program to predict integral beta-barrel outer membrane proteins encoded within genomes of Gramnegative bacteria. Nucleic Acids Res 32: W394-W399.
5. Bleves, S., Gerard-Vincent, M., Lazdunski, A., and Filloux, A. (1999) Structure-function analysis of XcpP, a component involved in general secretory pathway-dependent protein secretion in Pseudomonas aeruginosa. J Bacteriol 181: 4012-4019.
6. Bos, M.P., Robert, V., and Tommassen, J. (2007) Functioning of outer membrane protein assembly factor Omp85 requires a single POTRA domain. EMBO Rep 8: 1149-1154.
7. Clantin, B., Hodak, H., Willery, E., Locht, C., Jacob-Dubuisson, F., and Villeret, V. (2004) The crystal structure of filamentous hemagglutinin secretion domain and its implications for the two-partner secretion pathway. Proc Natl Acad Sci USA 101: 6194-6199.
8. Clantin, B., Delattre, A.S., Rucktooa, P., Saint, N., Meli, A.C., Locht, C., et al. (2007) Structure of the membrane protein FhaC: a member of the Omp85-TpsB transporter superfamily. Science 317: 957-961.
9. Coutte, L., Willery, E., Antoine, R., Drobecq, H., Locht, C., and Jacob-Dubuisson, F. (2003) Surface anchoring of bacterial subtilisin important for maturation function. Mol Microbiol 49: 529-539.
10. Dautin, N., and Bernstein, H.D. (2007) Protein secretion in gram-negative bacteria via the autotransporter pathway. Annu Rev Microbiol 61: 89-112.
11. Dekker, N., Merck, K., Tommassen, J., and Verheij, H.M. (1995) In vitro folding of Escherichia coli outer-membrane phospholipase A. Eur J Biochem 232: 214-219.
12. Dhondt, S., Geoffroy, P., Stelmach, B.A., Legrand, M., and Heitz, T. (2000) Soluble phospholipase A2 activity is induced before oxylipin accumulation in tobacco mosaic virus-infected tobacco leaves and is contributed by patatinlike enzymes. Plant J 23: 431-440.
13. Economou, A., Christie, P.J., Fernandez, R.C., Palmer, T., Plano, G.V., and Pugsley, A.P. (2006) Secretion by numbers: protein traffic in prokaryotes. Mol Microbiol 62: 308-319.
14. Filloux, A., Hachani, A., and Bleves, S. (2008) The bacterial type VI secretion machine: yet another player for protein transport across membranes. Microbiology 154: 1570-1583.
15. Finck-Barbancon, V., Goranson, J., Zhu, L., Sawa, T., Wiener-Kronish, J.P., Fleiszig, S.M., et al. (1997) ExoU expression by Pseudomonas aeruginosa correlates with acute cytotoxicity and epithelial injury. Mol Microbiol 25: 547-557.
16. Gardy, J.L., Spencer, C., Wang, K., Ester, M., Tusnady, G.E., Simon, I., et al. (2003) PSORT-B: improving protein subcellular localization prediction for Gram-negative bacteria. Nucleic Acids Res 31: 3613-3617.
17. Gentle, I.E., Burri, L., and Lithgow, T. (2005) Molecular architecture and function of the Omp85 family of proteins. Mol Microbiol 58: 1216-1225.
18. Guindon, S., and Gascuel, O. (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52: 696-704.
19. Hardie, K.R., Pommier, S., and Wilhelm, S. (2009) The secreted proteins of Pseudomonas aeruginosa: their export machineries and how they contribute to pathogenesis. In Bacterial Secreted Proteins, Vol. 1. Karl Wooldridge Centre for Biomolecular Sciences, U.o.N., UK (ed.). Nottingham, UK: Caister Academic Press, pp. 451-478.
20. Hauser, A.R., Kang, P.J., and Engel, J.N. (1998) PepA, a secreted protein of Pseudomonas aeruginosa, is necessary for cytotoxicity and virulence. Mol Microbiol 27: 807-818.
21. Henderson, I.R., Navarro-Garcia, F., Desvaux, M., Fernandez, R.C., and Ala'Aldeen, D. (2004) Type V protein secretion pathway: the autotransporter story. Microbiol Mol Biol Rev 68: 692-744.
22. Hendrixson, D.R., de la Morena, M.L., Stathopoulos, C., and St Geme, J.W., 3rd (1997) Structural determinants of processing and secretion of the Haemophilus influenzae hap protein. Mol Microbiol 26: 505-518.
23. Hirschberg, H.J., Simons, J.W., Dekker, N., and Egmond, M.R. (2001) Cloning, expression, purification and characterization of patatin, a novel phospholipase A. Eur J Biochem 268: 5037-5044.
24. Hodak, H., and Jacob-Dubuisson, F. (2007) Current challenges in autotransport and two-partner protein secretion pathways. Res Microbiol 158: 631-637.
25. Jacob-Dubuisson, F., Buisine, C., Mielcarek, N., Clement, E., Menozzi, F.D., and Locht, C. (1996) Amino-terminal maturation of the Bordetella pertussis filamentous haemagglutinin. Mol Microbiol 19: 65-78.
26. Jain, S., and Goldberg, M.B. (2007) Requirement for YaeT in the outer membrane assembly of autotransporter proteins. J Bacteriol 189: 5393-5398.
27. Kim, S., Malinverni, J.C., Sliz, P., Silhavy, T.J., Harrison, S.C., and Kahne, D. (2007) Structure and function of an essential component of the outer membrane protein assembly machine. Science 317: 961-964.
28. Konieczny, M.P.J., Benz, I., Hollinderbaumer, B., Beinke, C., Niederweis, M., and Schmidt, M.A. (2001) Modular organization of the AIDA autotransporter translocator: the N-terminal beta1-domain is surface-exposed and stabilizes the transmembrane beta2-domain. Antonie Van Leeuwenhoek 80: 19-34.
29. Kulasekara, B.R., Kulasekara, H.D., Wolfgang, M.C., Stevens, L., Frank, D.W., and Lory, S. (2006) Acquisition and evolution of the exoU locus in Pseudomonas aeruginosa. J Bacteriol 188: 4037-4050.
30. Labaer, J., Qiu, Q., Anumanthan, A., Mar, W., Zuo, D., Murthy, T.V., et al. (2004) The Pseudomonas aeruginosa PA01 gene collection. Genome Res 14: 2190-2200.
31. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
32. Liberati, N.T., Urbach, J.M., Miyata, S., Lee, D.G., Drenkard, E., Wu, G., et al. (2006) An ordered, nonredundant library of Pseudomonas aeruginosa strain PA14 transposon insertion mutants. Proc Natl Acad Sci USA 103: 2833-2838.
33. Linke, D., Riess, T., Autenrieth, I.B., Lupas, A., and Kempf, V.A. (2006) Trimeric autotransporter adhesins: variable structure, common function. Trends Microbiol 14: 264-270.
34. Ma, Q., Zhai, Y., Schneider, J.C., Ramseier, T.M., and Saier, M.H., Jr (2003) Protein secretion systems of Pseudomonas aeruginosa and P. fluorescens. Biochim Biophys Acta 1611: 223-233.
35. Mazar, J., and Cotter, P.A. (2007) New insight into the molecular mechanisms of two-partner secretion. Trends Microbiol 15: 508-515.
36. Michel, G.P.F., and Voulhoux, R. (2009) The type II secretory system (T2SS) in Gram negative bacteria: a molecular nanomachine for secretion of Sec and Tat-dependent extracellular proteins. In Bacterial Secreted Proteins, Vol. 1. Karl Wooldridge Centre for Biomolecular Sciences, U.o.N., UK (ed.). Nottingham, UK: Caister Academic Press, pp. 67-92.
37. Moraleda-Munoz, A., and Shimkets, L.J. (2007) Lipolytic enzymes in Myxococcus xanthus. J Bacteriol 189: 3072-3080.
38. Nielsen, H., Engelbrecht, J., Brunak, S., and von Heijne, G. (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 10: 1-6.
39. Oomen, C.J., van Ulsen, P., van Gelder, P., Feijen, M., Tommassen, J., and Gros, P. (2004) Structure of the translocator domain of a bacterial autotransporter. EMBO J 23: 1257-1266.
40. Pettersen, E.F., Goddard, T.D., Huang, C.C., Couch, G.S., Greenblatt, D.M., Meng, E.C., and Ferrin, T.E. (2004) UCSF Chimera -a visualization system for exploratory research and analysis. J Comput Chem 25: 1605-1612.
41. Philippe, H. (1993) MUST, a computer package of Management Utilities for Sequences and Trees. Nucleic Acids Res 21: 5264-5272.
42. Ronquist, F., and Huelsenbeck, J.P. (2003) MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
43. Ruer, S., Ball, G., Filloux, A., and de Bentzmann, S. (2008) The 'P-usher', a novel protein transporter involved in fimbrial assembly and TpsA secretion. EMBO J 27: 2669-2680.
44. Rydel, T.J., Williams, J.M., Krieger, E., Moshiri, F., Stallings, W.C., Brown, S.M., et al. (2003) The crystal structure, mutagenesis, and activity studies reveal that patatin is a lipid acyl hydrolase with a Ser-Asp catalytic dyad. Biochemistry 42: 6696-6708.
45. Sato, H., Frank, D.W., Hillard, C.J., Feix, J.B., Pankhaniya, R.R., Moriyama, K., et al. (2003) The mechanism of action of the Pseudomonas aeruginosa-encoded type III cytotoxin, ExoU. EMBO J 22: 2959-2969.
46. Sato, H., Feix, J.B., Hillard, C.J., and Frank, D.W. (2005) Characterization of phospholipase activity of the Pseudomonas aeruginosa type III cytotoxin, ExoU. J Bacteriol 187: 1192-1195
47. Sato, H., Feix, J.B., and Frank, D.W. (2006) Identification of superoxide dismutase as a cofactor for the pseudomonas type III toxin, ExoU. Biochemistry 45: 10368-10375.
48. Schonherr, R., Tsolis, R., Focareta, T., and Braun, V. (1993) Amino acid replacements in the Serratia marcescens haemolysin ShIA define sites involved in activation and secretion. Mol Microbiol 9: 1229-1237.
49. Shaver, C.M., and Hauser, A.R. (2004) Relative contributions of Pseudomonas aeruginosa ExoU, ExoS, and ExoT to virulence in the lung. Infect Immun 72: 6969-6977.
50. Shere, K.D., Sallustio, S., Manessis, A., D'Aversa, T.G., and Goldberg, M.B. (1997) Disruption of IcsP, the major Shigella protease that cleaves IcsA, accelerates actin-based motility. Mol Microbiol 25: 451-462. Shewry, P.R. (2003) Tuber storage proteins. Ann Bot (Lond) 91: 755-769.
51. Shewry, P.R. (2003) Tuber storage proteins. Ann Bot (Lond) 91: 755-769
52. Skillman, K.M., Barnard, T.J., Peterson, J.H., Ghirlando, R., and Bernstein, H.D. (2005) Efficient secretion of a folded protein domain by a monomeric bacterial autotransporter. Mol Microbiol 58: 945-958.
53. Stirling, F.R., Cuzick, A., Kelly, S.M., Oxley, D., and Evans, T.J. (2006) Eukaryotic localization, activation and ubiquitinylation of a bacterial type III secreted toxin. Cell Microbiol 8: 1294-1309.
54. Struyve, M., Moons, M., and Tommassen, J. (1991) Carboxyterminal phenylalanine is essential for the correct assembly of a bacterial outer membrane protein. J Mol Biol 218: 141-148.
55. Thompson, J.D., Higgins, D.G., and Gibson, T.J. (1994) Improved sensitivity of profile searches through the use of sequence weights and gap excision. Comput Appl Biosci 10: 19-29.
56. van Ulsen, P., van Alphen, L., Hove, J., Fransen, F., van der Ley, P., and Tommassen, J. (2003) A Neisserial autotransporter NalP modulating the processing of other autotransporters. Mol Microbiol 50: 1017-1030.
57. VanRheenen, S.M., Luo, Z.Q., O'Connor, T., and Isberg, R.R. (2006) Members of a Legionella pneumophila family of proteins with ExoU (phospholipase A) active sites are translocated to target cells. Infect Immun 74: 3597-3606.
58. Voulhoux, R., Bos, M.P., Geurtsen, J., Mols, M., and Tommassen, J. (2003) Role of a highly conserved bacterial protein in outer membrane protein assembly. Science 299: 262-265.
59. Walker, G., Hertle, R., and Braun, V. (2004) Activation of Serratia marcescens hemolysin through a conformational change. Infect Immun 72: 611-614.
60. Winkler, U.K., and Stuckmann, M. (1979) Glycogen, hyaluronate, and some other polysaccharides greatly enhance the formation of exolipase by Serratia marcescens. J Bacteriol 138: 663-670.
61. Wolfgang, M.C., Kulasekara, B.R., Liang, X., Boyd, D., Wu, K., Yang, Q., et al. (2003) Conservation of genome content and virulence determinants among clinical and environmental isolates of Pseudomonas aeruginosa. Proc Natl Acad Sci USA 100: 8484-8489.
62. Yoshihara, E., Gotoh, N., Nishino, T., and Nakae, T. (1996) Protein D2 porin of the Pseudomonas aeruginosa outer membrane bears the protease activity. FEBS Lett 394: 179-182.
63. Yoshihara, E., Gotoh, N., Nishino, T., and Nakae, T. (1996) Protein D2 porin of the Pseudomonas aeruginosa outer membrane bears the protease activity. FEBS Lett 394: 179-182.