Proteomic characterization of phagosomal membrane microdomains during phagolysosome biogenesis and evolution

Molecular and Cellular Proteomics

Volumn 11, Issue 11, 2012, Pages 1365-1377

  Goyette, Guillaume ^a   Boulais, Jonathan ^a,f   Carruthers, Nicholas J ^b   Landry, Christian R ^a,c   Jutras, Isabelle ^a   Duclos, Sophie ^a   Dermine, Jean François ^a   Michnick, Stephen W ^a   LaBoissière, Sylvie ^e   Lajoie, Gilles ^b   Barreiro, Luis ^f   Thibault, Pierre ^d   Desjardins, Michel ^a  

^a UNIVERSITÉ DE MONTRÉAL   (Canada)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

^c UNIVERSITÉ LAVAL   (Canada)

^d INSTITUTE FOR RESEARCH IN IMMUNOLOGY AND CANCER   (Canada)

^e MCGILL UNIVERSITY   (Canada)

^f UNIVERSITY OF MONTREAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

DETERGENT;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BIOGENESIS; CELL FUNCTION; CELL MATURATION; CELL MEMBRANE; CELL ORGANELLE; CONTROLLED STUDY; LIPID RAFT; MOLECULAR DYNAMICS; MOLECULAR EVOLUTION; MOUSE; NONHUMAN; PHAGOLYSOSOME; PHAGOSOME; PRIORITY JOURNAL; PROTEIN STRUCTURE; PROTEOMICS;

ANIMALS; CELL LINE; DETERGENTS; EVOLUTION, MOLECULAR; LYSOSOMES; MEMBRANE MICRODOMAINS; MICE; PEPTIDES; PHAGOSOMES; PROTEOME; PROTEOMICS; REPRODUCIBILITY OF RESULTS; SEQUENCE HOMOLOGY, AMINO ACID; TIME FACTORS;

EID: 84869205080     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M112.021048     Document Type: Article

References (69)

1. Haas, A. (2007) The phagosome: compartment with a license to kill. Traffic 8, 311-330
2. Jutras, I., Laplante, A., Boulais, J., Brunet, S., Thinakaran, G., and Desjardins, M. (2005) Gamma-secretase is a functional component of phagosomes. J. Biol. Chem. 280, 36310-36317
3. Vyas, J. M., Van der Veen, A. G., and Ploegh, H. L. (2008) The known unknowns of antigen processing and presentation. Nat Rev Immunol. 8, 607-618
4. Desjardins, M., Huber, L. A., Parton, R. G., and Griffiths, G. (1994) Biogenesis of phagolysosomes proceeds through a sequential series of interactions with the endocytic apparatus. J. Cell Biol. 124, 677-688 (Pubitemid 24085778)
5. Pitt, A., Mayorga, L. S., Stahl, P. D., and Schwartz, A. L. (1992) Alterations in the protein composition of maturing phagosomes. J. Clin. Invest. 90, 1978-1983
6. Gotthardt, D., Blancheteau, V., Bosserhoff, A., Ruppert, T., Delorenzi, M., and Soldati, T. (2006) Proteomics fingerprinting of phagosome maturation and evidence for the role of a Galpha during uptake. Mol. Cell. Proteomics 5, 2228-2243 (Pubitemid 46040630)
7. Garin, J., Diez, R., Kieffer, S., Dermine, J. F., Duclos, S., Gagnon, E., Sadoul, R., Rondeau, C., and Desjardins, M. (2001) The phagosome proteome: insight into phagosome functions. J. Cell Biol. 152, 165-180 (Pubitemid 32102445)
8. Houde, M., Bertholet, S., Gagnon, E., Brunet, S., Goyette, G., Laplante, A., Princiotta, M. F., Thibault, P., Sacks, D., and Desjardins, M. (2003) Phagosomes are competent organelles for antigen cross-presentation. Nature 425, 402-406 (Pubitemid 37187269)
9. Simons, K., and Ikonen, E. (1997) Functional rafts in cell membranes. Nature 387, 569-572 (Pubitemid 27248754)
10. Dermine, J. F., Duclos, S., Garin, J., St-Louis, F., Rea, S., Parton, R. G., and Desjardins, M. (2001) Flotillin-1-enriched lipid raft domains accumulate on maturing phagosomes. J. Biol. Chem. 276, 18507-18512
11. Vilhardt, F., and van Deurs, B. (2004) The phagocyte NADPH oxidase depends on cholesterol-enriched membrane microdomains for assembly. EMBO J. 23, 739-748 (Pubitemid 38418741)
12. Winberg, M. E., Holm, A., Särndahl, E., Vinet, A. F., Descoteaux, A., Magnusson, K. E., Rasmusson, B., and Lerm, M. (2009) Leishmania donovani lipophosphoglycan inhibits phagosomal maturation via action on membrane rafts. Microbes Infect. 11, 215-222
13. Arellano-Reynoso, B., Lapaque, N., Salcedo, S., Briones, G., Ciocchini, A. E., Ugalde, R., Moreno, E., Moriyón, I., and Gorvel, J. P. (2005) Cyclic beta-1,2-glucan is a Brucella virulence factor required for intracellular survival. Nat. Immunol. 6, 618-625 (Pubitemid 41710733)
14. Dermine, J. F., Goyette, G., Houde, M., Turco, S. J., and Desjardins, M. (2005) Leishmania donovani lipophosphoglycan disrupts phagosome microdomains in J774 macrophages. Cell Microbiol. 7, 1263-1270 (Pubitemid 41179419)
15. Lingwood, D., and Simons, K. (2010) Lipid rafts as a membrane-organizing principle. Science. 327, 46-50
16. Foster, L. J., De Hoog, C. L., and Mann, M. (2003) Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors. Proc. Natl. Acad. Sci. 100, 5813-5818 (Pubitemid 36576890)
17. Mannová, P., Fang, R., Wang, H., Deng, B., McIntosh, M. W., Hanash, S. M., and Beretta, L. (2006) Modification of host lipid raft proteome upon hepatitis C virus replication. Mol. Cell. Proteomics 5, 2319-2325 (Pubitemid 46040636)
18. Yang, W., Di Vizio, D., Kirchner, M., Steen, H., and Freeman, M. R. (2010) Proteome scale characterization of human S-acylated proteins in lipid raft-enriched and non-raft membranes. Mol. Cell. Proteomics 9, 54-70
19. Gagnon, E., Duclos, S., Rondeau, C., Chevet, E., Cameron, P. H., Steele-Mortimer, O., Paiement, J., Bergeron, J. J., and Desjardins, M. (2002) Endoplasmic reticulum-mediated phagocytosis is a mechanism of entry into macrophages. Cell 110, 119-131 (Pubitemid 34874611)
20. Wessel, D., and Flügge, U. I. (1984) A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal. Biochem. 138, 141-143 (Pubitemid 14146660)
21. Hiebl-Dirschmied, C. M., Adolf, G. R., and Prohaska, R. (1991) Isolation and partial characterization of the human erythrocyte band 7 integral membrane protein. Biochim. Biophys. Acta 1065, 195-202
22. Wasiak, S., Legendre-Guillemin, V., Puertollano, R., Blondeau, F., Girard, M., de Heuvel, E., Boismenu, D., Bell, A. W., Bonifacino, J. S., and McPherson, P. S. (2002) Enthoprotin: a novel clathrin-associated protein identified through subcellular proteomics. J. Cell Biol. 158, 855-862 (Pubitemid 35001077)
23. Keller, A., Nesvizhskii, A. I., Kolker, E., and Aebersold, R. (2002) Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal. Chem. 74, 5383-5392 (Pubitemid 35215372)
24. Nesvizhskii, A. I., Keller, A., Kolker, E., and Aebersold, R. (2003) A statistical model for identifying proteins by tandem mass spectrometry. Anal. Chem. 75, 4646-4658 (Pubitemid 37082259)
25. Choi, H., and Nesvizhskii, A. I. (2008) Semisupervised model-based validation of peptide identifications in mass spectrometry-based proteomics. J. Proteome Res. 7, 254-265 (Pubitemid 351171138)
26. Hulsen, T., de Vlieg, J., and Alkema, W. (2008) BioVenn - a web application for the comparison and visualization of biological lists using area-proportional Venn diagrams. BMC Genomics 9, 488
27. Blondeau, F., Ritter, B., Allaire, P. D., Wasiak, S., Girard, M., Hussain, N. K., Angers, A., Legendre-Guillemin, V., Roy, L., Boismenu, D., Kearney, R. E., Bell, A. W., Bergeron, J. J., and McPherson, P. S. (2004) Tandem MS analysis of brain clathrin-coated vesicles reveals their critical involvement in synaptic vesicle recycling. Proc. Natl. Acad. Sci. 101, 3833-3838 (Pubitemid 38381064)
28. Gilchrist, A., Au, C. E., Hiding, J., Bell, A. W., Fernandez-Rodriguez, J., Lesimple, S., Nagaya, H., Roy, L., Gosline, S. J., Hallett, M., Paiement, J., Kearney, R. E., Nilsson, T., and Bergeron, J. J. (2006) Quantitative proteomics analysis of the secretory pathway. Cell 127, 1265-1281 (Pubitemid 44914006)
29. R-Team, R. D. C. (2009) R: A language and environment for statistical computing. In: Computing, R. F. f. S., ed., Vienna, Austria
30. Tarassov, K., Messier, V., Landry, C. R., Radinovic, S., Serna Molina, M. M., Shames, I., Malitskaya, Y., Vogel, J., Bussey, H., and Michnick, S. W. (2008) An in vivo map of the yeast protein interactome. Science 320, 1465-1470 (Pubitemid 351929421)
31. Cline, M. S., Smoot, M., Cerami, E., Kuchinsky, A., Landys, N., Workman, C., Christmas, R., Avila-Campilo, I., Creech, M., Gross, B., Hanspers, K., Isserlin, R., Kelley, R., Killcoyne, S., Lotia, S., Maere, S., Morris, J., Ono, K., Pavlovic, V., Pico, A. R., Vailaya, A., Wang, P. L., Adler, A., Conklin, B. R., Hood, L., Kuiper, M., Sander, C., Schmulevich, I., Schwikowski, B., Warner, G. J., Ideker, T., and Bader, G. D. (2007) Integration of biological networks and gene expression data using Cytoscape. Nat. Protoc. 2, 2366-2382
32. Martin, A., Ochagavia, M. E., Rabasa, L. C., Miranda, J., Fernandez-de-Cossio, J., and Bringas, R. (2010) BisoGenet: a new tool for gene network building, visualization and analysis. BMC Bioinformatics 11, 91
33. Boulais, J., Trost, M., Landry, C. R., Dieckmann, R., Levy, E. D., Soldati, T., Michnick, S. W., Thibault, P., and Desjardins, M. (2010) Molecular characterization of the evolution of phagosomes. Mol. Syst. Biol. 6, 423
34. Huerta-Cepas, J., Capella-Gutierrez, S., Pryszcz, L. P., Denisov, I., Kormes, D., Marcet-Houben, M., and Gabaldon, T. (2011) PhylomeDB v3.0: an expanding repository of genome-wide collections of trees, alignments and phylogeny-based orthology and paralogy predictions. Nucleic Acids Res. 39, D556-560
35. Jutras, I., Houde, M., Currier, N., Boulais, J., Duclos, S., LaBoissiere, S., Bonneil, E., Kearney, P., Thibault, P., Paramithiotis, E., Hugo, P., and Desjardins, M. (2008) Modulation of the phagosome proteome by interferon-gamma. Mol. Cell. Proteomics 7, 697-715
36. Bantscheff, M., Schirle, M., Sweetman, G., Rick, J., and Kuster, B. (2007) Quantitative mass spectrometry in proteomics: a critical review. Anal. Bioanal. Chem. 389, 1017-1031 (Pubitemid 47482251)
37. Kinchen, J. M., and Ravichandran, K. S. (2008) Phagosome maturation: going through the acid test. Nat. Rev. Mol. Cell Biol. 9, 781-795
38. Pike, L. J. (2008) The challenge of lipid rafts. J. Lipid Res. 50 Suppl, S323-S328
39. Feuk-Lagerstedt, E., Movitz, C., Pellmé, S., Dahlgren, C., and Karlsson, A. (2007) Lipid raft proteome of the human neutrophil azurophil granule. Proteomics 7, 194-205 (Pubitemid 46184083)
40. Stuart, L. M., Boulais, J., Charriere, G. M., Hennessy, E. J., Brunet, S., Jutras, I., Goyette, G., Rondeau, C., Letarte, S., Huang, H., Ye, P., Morales, F., Kocks, C., Bader, J. S., Desjardins, M., and Ezekowitz, R. A. (2007) A systems biology analysis of the Drosophila phagosome. Nature 445, 95-101 (Pubitemid 46067308)
41. Shui, W., Sheu, L., Liu, J., Smart, B., Petzold, C. J., Hsieh, T. Y., Pitcher, A., Keasling, J. D., and Bertozzi, C. R. (2008) Membrane proteomics of phagosomes suggests a connection to autophagy. Proc. Natl. Acad. Sci. 105, 16952-16957
42. Sanjuan, M. A., Dillon, C. P., Tait, S. W., Moshiach, S., Dorsey, F., Connell, S., Komatsu, M., Tanaka, K., Cleveland, J. L., Withoff, S., and Green, D. R. (2007) Toll-like receptor signalling in macrophages links the autophagy pathway to phagocytosis. Nature 450, 1253-1257
43. Jutras, I., and Desjardins, M. (2005) Phagocytosis: at the crossroads of innate and adaptive immunity. Annu. Rev. Cell Dev. Biol. 21, 511-527 (Pubitemid 41740644)
44. Desjardins, M., Celis, J. E., van Meer, G., Dieplinger, H., Jahraus, A., Griffiths, G., and Huber, L. A. (1994) Molecular characterization of phagosomes. J. Biol. Chem. 269, 32194-32200
45. Burlak, C., Whitney, A. R., Mead, D. J., Hackstadt, T., and Deleo, F. R. (2006) Maturation of human neutrophil phagosomes includes incorporation of molecular chaperones and endoplasmic reticulum quality control machinery. Mol. Cell. Proteomics 5, 620-634
46. Okada, M., Huston, C. D., Mann, B. J., Petri, W. A., Jr., Kita, K., and Nozaki, T. (2005) Proteomic analysis of phagocytosis in the enteric protozoan parasite Entamoeba histolytica. Eukaryot. Cell 4, 827-831 (Pubitemid 40600435)
47. Rogers, L. D., and Foster, L. J. (2007) The dynamic phagosomal proteome and the contribution of the endoplasmic reticulum. Proc. Natl. Acad. Sci. 104, 18520-18525 (Pubitemid 350210729)
48. Trost, M., English, L., Lemieux, S., Courcelles, M., Desjardins, M., and Thibault, P. (2009) The phagosomal proteome in interferon-gamma-activated macrophages. Immunity 30, 143-154
49. Ramachandra, L., Simmons, D., and Harding, C. V. (2009) MHC molecules and microbial antigen processing in phagosomes. Curr Opin Immunol. 21, 98-104
50. Peters, C., Bayer, M. J., Bühler, S., Andersen, J. S., Mann, M., and Mayer, A. (2001) Trans-complex formation by proteolipid channels in the terminal phase of membrane fusion. Nature 409, 581-588 (Pubitemid 32154803)
51. Collins, R. F., Schreiber, A. D., Grinstein, S., and Trimble, W. S. (2002) Syntaxins 13 and 7 function at distinct steps during phagocytosis. J. Immunol. 169, 3250-3256 (Pubitemid 35013172)
52. Lafourcade, C., Sobo, K., Kieffer-Jaquinod, S., Garin, J., and van der Goot, F. G. (2008) Regulation of the V-ATPase along the endocytic pathway occurs through reversible subunit association and membrane localization. PLoS ONE 3, e2758
53. Fatimathas, L., and Moss, S. E. (2010) Annexins as disease modifiers. Histol. Histopathol. 25, 527-532
54. Gerke, V., Creutz, C. E., and Moss, S. E. (2005) Annexins: linking Ca2+ signalling to membrane dynamics. Nat. Rev. Mol. Cell Biol. 6, 449-461 (Pubitemid 40780557)
55. Kobayashi, T., Stang, E., Fang, K. S., de Moerloose, P., Parton, R. G., and Gruenberg, J. (1998) A lipid associated with the antiphospholipid syndrome regulates endosome structure and function. Nature 392, 193-197 (Pubitemid 28162794)
56. Taute, A., Wätzig, K., Simons, B., Lohaus, C., Meyer, H., and Hasilik, A. (2002) Presence of detergent-resistant microdomains in lysosomal membranes. Biochem. Biophys. Res. Commun. 298, 5-9 (Pubitemid 35205379)
57. Antonin, W., Fasshauer, D., Becker, S., Jahn, R., and Schneider, T. R. (2002) Crystal structure of the endosomal SNARE complex reveals common structural principles of all SNAREs. Nat. Struct. Biol. 9, 107-111 (Pubitemid 34132411)
58. Flowerdew, S. E., and Burgoyne, R. D. (2009) A VAMP7/Vti1a SNARE complex distinguishes a non-conventional traffic route to the cell surface used by KChIP1 and Kv4 potassium channels. Biochem. J. 418, 529-540
59. Mallard, F., Tang, B. L., Galli, T., Tenza, D., Saint-Pol, A., Yue, X., Antony, C., Hong, W., Goud, B., and Johannes, L. (2002) Early/recycling endosomes-to-TGN transport involves two SNARE complexes and a Rab6 isoform. J. Cell Biol. 156, 653-664 (Pubitemid 34839881)
60. Welin, A., Winberg, M. E., Abdalla, H., Särndahl, E., Rasmusson, B., Stendahl, O., and Lerm, M. (2008) Incorporation of Mycobacterium tuberculosis lipoarabinomannan into macrophage membrane rafts is a prerequisite for the phagosomal maturation block. Infect. Immun. 76, 2882-2887
61. Desjardins, M., and Descoteaux, A. (1997) Inhibition of phagolysosomal biogenesis by the Leishmania lipophosphoglycan. J. Exp. Med. 185, 2061-2068 (Pubitemid 27265989)
62. Lodge, R., and Descoteaux, A. (2008) Leishmania invasion and phagosome biogenesis. Subcell. Biochem. 47, 174-181
63. Vinet, A. F., Fukuda, M., Turco, S. J., and Descoteaux, A. (2009) The Leishmania donovani lipophosphoglycan excludes the vesicular proton-ATPase from phagosomes by impairing the recruitment of synaptotagmin V. PLoS Pathog. 5, e1000628
64. Brown, A. J., and Galea, A. M. (2010) Cholesterol as an evolutionary response to living with oxygen. Evolution; Int. J. Organic Evolution 64, 2179-2183
65. Nes, W. R. N. a. W. D. (1980) Lipids in evolution, 1st Ed., Plenum Press
66. Barenholz, Y. (2002) Cholesterol and other membrane active sterols: from membrane evolution to "rafts". Progress Lipid Res. 41, 1-5
67. Jensen, L. J., Kuhn, M., Stark, M., Chaffron, S., Creevey, C., Muller, J., Doerks, T., Julien, P., Roth, A., Simonovic, M., Bork, P., and von Mering, C. (2009) STRING 8-a global view on proteins and their functional interactions in 630 organisms. Nucleic Acids Res. 37, D412-D416
68. Cavalier-Smith, T. (2002) The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. Int. J. Syst. Evol. Microbiol. 52, 297-354
69. Dacks, J. B., Poon, P. P., and Field, M. C. (2008) Phylogeny of endocytic components yields insight into the process of nonendosymbiotic organelle evolution. Proc. Natl. Acad. Sci. 105, 588-593 (Pubitemid 351171752)