Two distinct sensing pathways allow recognition of Klebsiella pneumoniae by Dictyostelium amoebae

Cellular Microbiology

Volumn 16, Issue 3, 2014, Pages 311-323

  Lima, Wanessa C ^a   Balestrino, Damien ^b   Forestier, Christiane ^b   Cosson, Pierre ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b UNIVERSITÉ CLERMONT AUVERGNE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACILLUS SUBTILIS; BACTERIAL CAPSULES; DICTYOSTELIUM; FEEDING BEHAVIOR; KLEBSIELLA PNEUMONIAE; PHAGOCYTOSIS;

EID: 84893845430     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/cmi.12226     Document Type: Article

References (58)

1. Balestrino, D., Ghigo, J.M., Charbonnel, N., Haagensen, J.A., and Forestier, C. (2008) The characterization of functions involved in the establishment and maturation of Klebsiella pneumoniae in vitro biofilm reveals dual roles for surface exopolysaccharides. Environ Microbiol 10: 685-701.
2. Benghezal, M., Gotthardt, D., Cornillon, S., and Cosson, P. (2001) Localization of the Rh50-like protein to the contractile vacuole in Dictyostelium. Immunogenetics 52: 284-288.
3. Benghezal, M., Fauvarque, M.O., Tournebize, R., Froquet, R., Marchetti, A., Bergeret, E., etal. (2006) Specific host genes required for the killing of Klebsiella bacteria by phagocytes. Cell Microbiol 8: 139-148.
4. Bhasin, M., and Raghava, G.P. (2004) GPCRpred: an SVM-based method for prediction of families and subfamilies of G-protein coupled receptors. Nucleic Acids Res 32: W383-W389.
5. Bozzaro, S., and Eichinger, L. (2011) The professional phagocyte Dictyostelium discoideum as a model host for bacterial pathogens. Curr Drug Targets 12: 942-954.
6. Bozzaro, S., Bucci, C., and Steinert, M. (2008) Phagocytosis and host-pathogen interactions in Dictyostelium with a look at macrophages. Int Rev Cell Mol Biol 271: 253-300.
7. Burkholder, P.R., and McVeigh, I. (1942) Synthesis of vitamins by intestinal bacteria. Proc Natl Acad Sci USA 28: 285-289.
8. Carbon, S., Ireland, A., Mungall, C.J., Shu, S., Marshall, B., and Lewis, S. (2009) AmiGO: online access to ontology and annotation data. Bioinformatics 25: 288-289.
9. Carilla-Latorre, S., Calvo-Garrido, J., Bloomfield, G., Skelton, J., Kay, R.R., Ivens, A., etal. (2008) Dictyostelium transcriptional responses to Pseudomonas aeruginosa: common and specific effects from PAO1 and PA14 strains. BMC Microbiol 8: 109.
10. Charette, S.J., Mercanti, V., Letourneur, F., Bennett, N., and Cosson, P. (2006) A role for adaptor protein-3 complex in the organization of the endocytic pathway in Dictyostelium. Traffic 7: 1528-1538.
11. Cornillon, S., Pech, E., Benghezal, M., Ravanel, K., Gaynor, E., Letourneur, F., etal. (2000) Phg1p is a nine-transmembrane protein superfamily member involved in dictyostelium adhesion and phagocytosis. J Biol Chem 275: 34287-34292.
12. Cornillon, S., Gebbie, L., Benghezal, M., Nair, P., Keller, S., Wehrle-Haller, B., etal. (2006) An adhesion molecule in free-living Dictyostelium amoebae with integrin beta features. EMBO Rep 7: 617-621.
13. Cortes, G., Borrell, N., de Astorza, B., Gomez, C., Sauleda, J., and Alberti, S. (2002) Molecular analysis of the contribution of the capsular polysaccharide and the lipopolysaccharide O side chain to the virulence of Klebsiella pneumoniae in a murine model of pneumonia. Infect Immun 70: 2583-2590.
14. Cosson, P., and Soldati, T. (2008) Eat, kill or die: when amoeba meets bacteria. Curr Opin Microbiol 11: 271-276.
15. Domenico, P., Schwartz, S., and Cunha, B.A. (1989) Reduction of capsular polysaccharide production in Klebsiella pneumoniae by sodium salicylate. Infect Immun 57: 3778-3782.
16. Evrard, B., Balestrino, D., Dosgilbert, A., Bouya-Gachancard, J.L., Charbonnel, N., Forestier, C., and Tridon, A. (2010) Roles of capsule and lipopolysaccharide O antigen in interactions of human monocyte-derived dendritic cells and Klebsiella pneumoniae. Infect Immun 78: 210-219.
17. Farbrother, P., Wagner, C., Na, J., Tunggal, B., Morio, T., Urushihara, H., etal. (2006) Dictyostelium transcriptional host cell response upon infection with Legionella. Cell Microbiol 8: 438-456.
18. Favre-Bonte, S., Joly, B., and Forestier, C. (1999) Consequences of reduction of Klebsiella pneumoniae capsule expression on interactions of this bacterium with epithelial cells. Infect Immun 67: 554-561.
19. Fey, P., Gaudet, P., Curk, T., Zupan, B., Just, E.M., Basu, S., etal. (2009) dictyBase: a Dictyostelium bioinformatics resource update. Nucleic Acids Res 37: D515-D519.
20. Flannagan, R.S., Cosio, G., and Grinstein, S. (2009) Antimicrobial mechanisms of phagocytes and bacterial evasion strategies. Nat Rev Microbiol 7: 355-366.
21. Froquet, R., Cherix, N., Birke, R., Benghezal, M., Cameroni, E., Letourneur, F., etal. (2008) Control of cellular physiology by TM9 proteins in yeast and Dictyostelium. J Biol Chem 283: 6764-6772.
22. Froquet, R., Lelong, E., Marchetti, A., and Cosson, P. (2009) Dictyostelium discoideum: a model host to measure bacterial virulence. Nat Protoc 4: 25-30.
23. Hadwiger, J.A., Lee, S., and Firtel, R.A. (1994) The G alpha subunit G alpha 4 couples to pterin receptors and identifies a signaling pathway that is essential for multicellular development in Dictyostelium. Proc Natl Acad Sci USA 91: 10566-10570.
24. Herrington, M.B. (1994) Measurement of the uptake of radioactive para-aminobenzoic acid monitors folate biosynthesis in Escherichia coli K-12. Anal Biochem 216: 427-430.
25. Hilbi, H., Weber, S.S., Ragaz, C., Nyfeler, Y., and Urwyler, S. (2007) Environmental predators as models for bacterial pathogenesis. Environ Microbiol 9: 563-575.
26. Hunter, S., Jones, P., Mitchell, A., Apweiler, R., Attwood, T.K., Bateman, A., etal. (2012) InterPro in 2011: new developments in the family and domain prediction database. Nucleic Acids Res 40: D306-D312.
27. Johnson, M., Zaretskaya, I., Raytselis, Y., Merezhuk, Y., McGinnis, S., and Madden, T.L. (2008) NCBI BLAST: a better web interface. Nucleic Acids Res 36: W5-W9.
28. Kesbeke, F., Van Haastert, P.J.M., De Wit, R.J.W., and Snaar-Jagalska, B.E. (1990) Chemotaxis to cyclic AMP and folic acid is mediated by different G proteins in Dictyostelium discoideum. J Cell Sci 96: 669-673.
29. Krogh, A., Larsson, B., von Heijne, G., and Sonnhammer, E.L. (2001) Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 305: 567-580.
30. Kuspa, A. (2006) Restriction enzyme-mediated integration (REMI) mutagenesis. Methods Mol Biol 346: 201-209.
31. Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., etal. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948. PMID: 17846036.
32. Lelong, E., Marchetti, A., Gueho, A., Lima, W.C., Sattler, N., Molmeret, M., etal. (2011) Role of magnesium and a phagosomal P-type ATPase in intracellular bacterial killing. Cell Microbiol 13: 246-258.
33. Leulier, F., and Lemaitre, B. (2008) Toll-like receptors: taking an evolutionary approach. Nat Rev Genet 9: 165-178.
34. Lima, W.C., Lelong, E., and Cosson, P. (2011) What can Dictyostelium bring to the study of Pseudomonas infections? Semin Cell Dev Biol 22: 77-81.
35. March, C., Cano, V., Moranta, D., Llobet, E., Perez-Gutierrez, C., Tomas, J.M., etal. (2013) Role of bacterial surface structures on the interaction of Klebsiella pneumoniae with phagocytes. PLoS ONE 8: e56847.
36. Marchetti, A., Mercanti, V., Cornillon, S., Alibaud, L., Charette, S.J., and Cosson, P. (2004) Formation of multivesicular endosomes in Dictyostelium. J Cell Sci 117: 6053-6059.
37. Marchetti, A., Lelong, E., and Cosson, P. (2009) A measure of endosomal pH by flow cytometry in Dictyostelium. BMC Res Notes 2: 7.
38. Melendez, A.J., and Tay, H.K. (2008) Phagocytosis: a repertoire of receptors and Ca(2+) as a key second messenger. Biosci Rep 28: 287-298.
39. Mercanti, V., Charette, S.J., Bennett, N., Ryckewaert, J.J., Letourneur, F., and Cosson, P. (2006) Selective membrane exclusion in phagocytic and macropinocytic cups. J Cell Sci 119: 4079-4087.
40. Monnat, J., Hacker, U., Geissler, H., Rauchenberger, R., Neuhaus, E.M., Maniak, M., and Soldati, T. (1997) Dictyostelium discoideum protein disulfide isomerase, an endoplasmic reticulum resident enzyme lacking a KDEL-type retrieval signal. FEBS Lett 418: 357-362.
41. Nasser, W., Santhanam, B., Miranda, E.R., Parikh, A., Juneja, K., Rot, G., etal. (2013) Bacterial discrimination by dictyostelid amoebae reveals the complexity of ancient interspecies interactions. Curr Biol 23: 862-872.
42. Pan, P., Hall, E.M., and Bonner, J.T. (1972) Folic acid as second chemotactic substance in the cellular slime moulds. Nat New Biol 237: 181-182.
43. Peng, Z.L., Yang, J.Y., and Chen, X. (2010) An improved classification of G-protein-coupled receptors using sequence-derived features. BMC Bioinformatics 11: 420.
44. Petersen, T.N., Brunak, S., von Heijne, G., and Nielsen, H. (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8: 785-786.
45. Podschun, R., and Ullmann, U. (1998) Klebsiella spp. as nosocomial pathogens: epidemiology, taxonomy, typing methods, and pathogenicity factors. Clin Microbiol Rev 11: 589-603.
46. Ravanel, K., de Chassey, B., Cornillon, S., Benghezal, M., Zulianello, L., Gebbie, L., etal. (2001) Membrane sorting in the endocytic and phagocytic pathway of Dictyostelium discoideum. Eur J Cell Biol 80: 754-764.
47. Rifkin, J.L., and Goldberg, R.R. (2006) Effects of chemoattractant pteridines upon speed of D.discoideum vegetative amoebae. Cell Motil Cytoskeleton 63: 1-5.
48. Sattler, N., Monroy, R., and Soldati, T. (2013) Quantitative analysis of phagocytosis and phagosome maturation. Methods Mol Biol 983: 383-402.
49. Sengupta, P., Chou, J.H., and Bargmann, C.I. (1996) odr-10 encodes a seven transmembrane domain olfactory receptor required for responses to the odorant diacetyl. Cell 84: 899-909.
50. Sigrist, C.J., Cerutti, L., de Castro, E., Langendijk-Genevaux, P.S., Bulliard, V., Bairoch, A., and Hulo, N. (2010) PROSITE, a protein domain database for functional characterization and annotation. Nucleic Acids Res 38: D161-D166.
51. Sigrist, C.J., de Castro, E., Cerutti, L., Cuche, B.A., Hulo, N., Bridge, A., etal. (2013) New and continuing developments at PROSITE. Nucleic Acids Res 41: D344-D347.
52. Sillo, A., Bloomfield, G., Balest, A., Balbo, A., Pergolizzi, B., Peracino, B., etal. (2008) Genome-wide transcriptional changes induced by phagocytosis or growth on bacteria in Dictyostelium. BMC Genomics 9: 291.
53. Sroka, J., Madeja, Z., Michalik, M., Przestalski, S., and Korohoda, W. (2002) Folic acid, ascorbic acid and sodium selenite restore the motility of Dictyostelium discoideum inhibited by triethyllead. Toxicology 180: 275-292.
54. Steinert, M. (2011) Pathogen-host interactions in Dictyostelium, Legionella, Mycobacterium and other pathogens. Semin Cell Dev Biol 22: 70-76.
55. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M., and Kumar, S. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
56. Troemel, E.R., Chou, J.H., Dwyer, N.D., Colbert, H.A., and Bargmann, C.I. (1995) Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans. Cell 83: 207-218.
57. Underhill, D.M., and Gantner, B. (2004) Integration of Toll-like receptor and phagocytic signaling for tailored immunity. Microbes Infect 6: 1368-1373.
58. Xiao, X., Wang, P., and Chou, K.C. (2009) GPCR-CA: a cellular automaton image approach for predicting G-protein-coupled receptor functional classes. J Comput Chem 30: 1414-1423.