Proteomic Characterization of Phagosomal Membrane Microdomains During Phagolysosome Biogenesis and Evolution

After their formation at the cell surface, phagosomes become fully functional through a complex maturation process involving sequential interactions with various intracellular organelles. In the last decade, series of data indicated that some of the phagosome functional properties occur in specialized membrane microdomains. The molecules associated with membrane microdomains, as well as the organization of these structures during phagolysosome biogenesis are largely unknown. In this study, we combined proteomics and bioinformatics analyses to characterize the dynamic association of proteins to maturing phagosomes. Our data indicate that groups of proteins shuffle from detergent-soluble to detergent-resistant membrane microdomains during maturation, supporting a model in which the modulation of the phagosome functional properties involves an important reorganization of the phagosome proteome by the coordinated spatial segregation of proteins. After their formation at the cell surface, phagosomes become fully functional through a complex maturation process involving sequential interactions with various intracellular organelles. In the last decade, series of data indicated that some of the phagosome functional properties occur in specialized membrane microdomains. The molecules associated with membrane microdomains, as well as the organization of these structures during phagolysosome biogenesis are largely unknown. In this study, we combined proteomics and bioinformatics analyses to characterize the dynamic association of proteins to maturing phagosomes. Our data indicate that groups of proteins shuffle from detergent-soluble to detergent-resistant membrane microdomains during maturation, supporting a model in which the modulation of the phagosome functional properties involves an important reorganization of the phagosome proteome by the coordinated spatial segregation of proteins. Phagocytosis, the mechanism by which large particles are internalized, leads to the formation of phagosomes, a specialized organelle in which the engulfed material is degraded (1Haas A. The phagosome: compartment with a license to kill.Traffic. 2007; 8: 311-330Crossref PubMed Scopus (223) Google Scholar, 2Jutras I. Laplante A. Boulais J. Brunet S. Thinakaran G. Desjardins M. Gamma-secretase is a functional component of phagosomes.J. Biol. Chem. 2005; 280: 36310-36317Abstract Full Text Full Text PDF PubMed Scopus (34) Google Scholar). In mammals, various cells including macrophages, neutrophils and dendritic cells display remarkable phagocytic activities, rapidly eliminating microorganisms, foreign inert particles, and apoptotic cells. The killing of microorganisms by professional phagocytes precludes the emergence of infectious diseases. This innate immune process is followed by the degradation of microbes in a highly concentrated mixture of hydrolases, activated by the acidic pH generated in the phagosome lumen, generating antigenic peptides that are displayed at the cell surface, enabling their recognition by T lymphocytes (3Vyas J.M. Van der Veen A.G. Ploegh H.L. The known unknowns of antigen processing and presentation.Nat Rev Immunol. 2008; 8: 607-618Crossref PubMed Scopus (445) Google Scholar). The peptides not loaded on MHC molecules are fully degraded in phagolysosomes and the end products are likely recycled from phagosomes by a variety of transporters (1Haas A. The phagosome: compartment with a license to kill.Traffic. 2007; 8: 311-330Crossref PubMed Scopus (223) Google Scholar). The establishment of these functional properties involves a complex remodeling of phagosomes, referred to as phagolysosome biogenesis (4Desjardins M. Huber L.A. Parton R.G. Griffiths G. Biogenesis of phagolysosomes proceeds through a sequential series of interactions with the endocytic apparatus.J. Cell Biol. 1994; 124: 677-688Crossref PubMed Scopus (559) Google Scholar, 5Pitt A. Mayorga L.S. Stahl P.D. Schwartz A.L. Alterations in the protein composition of maturing phagosomes.J. Clin. Invest. 1992; 90: 1978-1983Crossref PubMed Scopus (172) Google Scholar). This highly regulated process requires the fusion of nascent phagosomes with trans Golgi-derived vesicles, early endosomes, late endosomes and ultimately lysosomes (1Haas A. The phagosome: compartment with a license to kill.Traffic. 2007; 8: 311-330Crossref PubMed Scopus (223) Google Scholar, 2Jutras I. Laplante A. Boulais J. Brunet S. Thinakaran G. Desjardins M. Gamma-secretase is a functional component of phagosomes.J. Biol. Chem. 2005; 280: 36310-36317Abstract Full Text Full Text PDF PubMed Scopus (34) Google Scholar). These fusion events are believed to alter significantly the proteome of phagosomes during phagolysosome biogenesis and regulate their functional properties (6Gotthardt D. Blancheteau V. Bosserhoff A. Ruppert T. Delorenzi M. Soldati T. Proteomics fingerprinting of phagosome maturation and evidence for the role of a Galpha during uptake.Mol. Cell. Proteomics. 2006; 5: 2228-2243Abstract Full Text Full Text PDF PubMed Scopus (86) Google Scholar). The capacity to kill and degrade microbes is one of the many functions that phagosomes acquire during phagolysosome biogenesis. In a previous study, we identified more than 140 proteins associated with phagosomes (7Garin J. Diez R. Kieffer S. Dermine J.F. Duclos S. Gagnon E. Sadoul R. Rondeau C. Desjardins M. The phagosome proteome: insight into phagosome functions.J. Cell Biol. 2001; 152: 165-180Crossref PubMed Scopus (606) Google Scholar), leading to the proposal of novel mechanisms to explain phagosomal functions such as antigen cross-presentation (8Houde M. Bertholet S. Gagnon E. Brunet S. Goyette G. Laplante A. Princiotta M.F. Thibault P. Sacks D. Desjardins M. Phagosomes are competent organelles for antigen cross-presentation.Nature. 2003; 425: 402-406Crossref PubMed Scopus (602) Google Scholar). This proteomics study also shown the presence on phagosomes of proteins known to segregate into lipid rafts at the cell surface, such as flotillin-1 and prohibitin, leading to the proposal that membrane microdomains might also assemble on phagosomes. At the plasma membrane, these structures constitute foci of specialized functions, notably for signal transduction (9Simons K. Ikonen E. Functional rafts in cell membranes.Nature. 1997; 387: 569-572Crossref PubMed Scopus (8092) Google Scholar). Further biochemical and morphological analyses confirmed the presence of membrane microdomains on phagosomes (10Dermine J.F. Duclos S. Garin J. St-Louis F. Rea S. Parton R.G. Desjardins M. Flotillin-1-enriched lipid raft on maturing phagosomes.J. Biol. Chem. 2001; Full Text Full Text PDF PubMed Scopus Google Scholar). The role of membrane microdomains and the of these structures in phagosomes is data indicated that phagosomal protein and membrane microdomains as F. The on membrane microdomains for J. PubMed Scopus Google Scholar). the of phagosome microdomains in innate by the that at the and the intracellular phagosome lipid rafts as a to mechanisms A. E. A. M. phagosomal maturation on membrane PubMed Scopus Google Scholar, S. G. R. E. I. is a for intracellular Immunol. 2005; PubMed Scopus Google Scholar, J.F. Goyette G. M. Desjardins M. phagosome microdomains in 2005; PubMed Scopus Google Scholar). the of the detergent-soluble and from phagosomes into the mechanisms by to alter the functional properties of this to study membrane microdomains, including such as as well as cell to detergent-resistant membrane D. K. rafts as a PubMed Scopus Google Scholar). the that membrane microdomains are dynamic structures of than in the to of membrane microdomains, including series of M. proteomics of lipid rafts for 2003; PubMed Scopus Google Scholar, P. R. of lipid raft proteome Cell. Proteomics. 2006; 5: Full Text Full Text PDF PubMed Scopus Google Scholar, D. M. of proteins in lipid and Cell. Proteomics. Full Text Full Text PDF PubMed Scopus Google Scholar). the and the of of the membrane microdomains by the morphological and biochemical is of proteins identified in these structures D. K. rafts as a PubMed Scopus Google Scholar). In the study we proteomics to for the the of lipid rafts proteins during the biogenesis of an intracellular Our data indicate that segregation of of proteins in of the phagosome membrane the biogenesis and maturation of the that reorganization of the phagosome proteome a role in the establishment of the functional properties of this The cell in with and at in a to in to phagosomes, with in to for at for at with to and for of to early and late phagosomes. Phagosomes on as (10Dermine J.F. Duclos S. Garin J. St-Louis F. Rea S. Parton R.G. Desjardins M. Flotillin-1-enriched lipid raft on maturing phagosomes.J. Biol. Chem. 2001; Full Text Full Text PDF PubMed Scopus Google Scholar), a process generating highly organelles as by (4Desjardins M. Huber L.A. Parton R.G. Griffiths G. Biogenesis of phagolysosomes proceeds through a sequential series of interactions with the endocytic apparatus.J. Cell Biol. 1994; 124: 677-688Crossref PubMed Scopus (559) Google Scholar, E. Duclos S. Rondeau C. E. J. Desjardins M. is a mechanism of into Full Text Full Text PDF PubMed Scopus Google Scholar). phagosomes in to an and at identified as phagosomes, to the phagosomes of phagosomes from to on by an of and at to phagosomal by at and the the and the detergent-resistant phagosome to a of by of in This at the of an of and of on After of at to the of from the with to D. for the of protein in in the presence of and PubMed Scopus Google and in for an of phagosomes from on the as indicated The protein in the cell and the and of protein loaded for The and the from the from The from the of from and the from the of a from R. R. and of the membrane PubMed Scopus Google Scholar). the lipid we with from of the for protein by The proteins in which and the proteins in which the of phagosome with in and loaded on a for a After a a the in of to and in an as S. V. R. F. M. E. D. a novel protein identified through Cell Biol. PubMed Scopus Google Scholar). analyses on a with a to the the data with the data in on and and with a of in of and of phagosomes at and generated from in the data from the to a and for of by with at for and at for This and a of in which of the into an The data the protein by and the to a of of of on and The to the to and protein at than as by the A. E. R. model to the of by and Chem. PubMed Scopus Google Scholar). at than and at identified by the A. E. R. model for proteins by Chem. 2003; PubMed Scopus Google Scholar). that peptides and not on to the of These to proteins on of which we proteins of that identified by one which and of The to of in 2008; PubMed Scopus Google a protein of and at the is for the proteins and for of the proteins in this we a and a functional with the of the and of the in a as The generated T. J. a for the and of 2008; PubMed Scopus Google Scholar). a F. P.D. S. M. A. V. D. of their in PubMed Scopus Google Scholar, A. J. J. S. M. J. T. proteomics of the 2006; Full Text Full Text PDF PubMed Scopus Google Scholar). The of the from the at in and The to the of the identified proteins at the in the phagosome of and in in generated with the to the proteins one of these proteins with that of at and proteins with an at the is more than and to more than of the at the and the proteins with that of at and and proteins identified by an of for the This a of proteins for the phagosome and for the In to the and protein we the of of the the of of of the protein with from the to a by the for these analyses in and for Scholar). the phagosomal proteins for the to for the of the M. M. S. C. J. T. P. A. M. P. C. on proteins and their functional interactions in PubMed Scopus Google Scholar). The generated a of proteins in interactions with a of also interactions data from a on the a of the protein a with proteins K. V. S. I. J. in of the protein 2008; PubMed Scopus Google Scholar). the proteins identified as associated with the phagosome in this study that shown to by from we of the phagosomal proteins. this to proteins proteins in these we the in the and we a of proteins These data to a with and the M. E. A. C. R. I. M. K. R. R. S. S. S. J. K. V. A. A. M. C. I. T. of and data 2007; PubMed Scopus Google Scholar, A. J. J. R. a for and PubMed Scopus Google Scholar). the of identified rafts and phagosome and analyses as in J. M. R. Soldati T. Thibault P. Desjardins M. of the of Biol. PubMed Scopus Google that J. S. I. D. M. T. an of of and and PubMed Scopus Google and Proteomics and bioinformatics to a of the to proteins during phagolysosome biogenesis. phagosomes at of maturation including early phagosomes of maturing phagosomes of and and phagolysosomes and of analyses to the maturation of phagosomes the for study the late and during phagosome maturation (10Dermine J.F. Duclos S. Garin J. St-Louis F. 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The proteins in phagosomal membrane microdomains into a and a membrane for This to the of in and of an as by the of and the In and known of phagosomes, not in these and with the of at the of the in and proteins associated with the of the by to proteins associated with in the of phagosomal a protein to a of with at peptides than of by the and and This the of highly proteins for on these a of peptides proteins identified and with a than proteins in at some during phagosome of proteins on their in the phagosome indicated that a of proteins are in of the of phagosomal protein to at which and in of the membrane protein during phagolysosome biogenesis. the of we a F. P.D. S. M. A. V. D. of their in PubMed Scopus Google to maturation events the A. J. J. S. M. J. T. proteomics of the 2006; Full Text Full Text PDF PubMed Scopus Google Scholar). This is well to a of in a dynamic M. M. G. 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S. in the to 2007; PubMed Scopus Google that this of a variety of proteins to the phagosome for we that phagosomes from cells of of the of proteins The with the analyses to and their of at the the the in the In proteins not during maturation and as the phagosome proteins to the and In the phagosomal proteins associated with displayed important the as of the proteins in at the at the and at the These data the that are on the phagosome membrane during maturation, that membrane microdomains regulate some of the functional properties during phagosome the of groups of proteins in phagosomal functions on their during phagosome of phagosome functional groups of proteins. as in proteins by functional a of the proteins of are to the a of proteins by on the we proteins to their functional properties as well as their in and during maturation, and the to the of their a of this is in in to of the proteins and their The that a of the proteins identified on early phagosomes are to The of proteins to during phagosome maturation, that specialized foci at the phagosome membrane are likely to in the functional properties of this interactions the by data from a on the we a of the interactions with proteins K. V. S. I. J. in of the protein 2008; PubMed Scopus Google Scholar). These for the and the to and is the a of the and the of the protein which are to the and that are of the and complex for a of These interactions by with proteins are with in Further of the proteins on on and data in the modulation of phagosome functional properties during phagolysosome and the of in this Functional of proteins which to regulated by their in membrane microdomains, including intracellular and the molecules in membrane are in these data to the model of phagosome maturation that the of proteins in membrane microdomains and the proteins in and the of phagosome functions by the intracellular is also in analyses to the of the and phagosome proteins identified by by the and Our analyses indicate that the proteins of the phagosome proteome in such as that for are and In proteins that in a role in innate to as well as in to are to that a of these structures during of proteins to their functional properties the of of membrane and molecules by during analyses that the proteins of to a with proteins in of more and to a with proteins in that the protein the in is of proteins in and In the complex proteins including and that with innate is with proteins in these data that not in of interactions of proteins with proteins in data of and proteins and to the of proteins to the with proteins. indicate of interactions of proteins with indicate of interactions of phagosome proteins with proteins. of the and including and proteins are in and proteins are in The groups are in and is well that an important role in the emergence of novel functional properties by one of the to to in Google Scholar). of shown to to the of organelles during T. The of and of J. PubMed Scopus Google Scholar, of endocytic insight into the process of organelle 2008; PubMed Scopus Google Scholar). Our analyses identified of from the phagosome proteins in proteomics These analyses indicated that a significantly of the the proteins in In of the in functional of proteins in and These data that to the of the biogenesis of membrane organelles is by the of the to these structures at various of their phagosomes are for this of these organelles the of large such as particles, enabling their on a at during their biogenesis. the by phagosomes in innate and I. Desjardins M. at the of innate and Cell Biol. 2005; PubMed Scopus Google Scholar), their is of a to into the mechanisms immune The functional properties of phagosomes are through a complex maturation process by which nascent phagosomes, at the cell surface, are into biogenesis as a process through of proteins shown to with maturing phagosomes and to early late phagosomes (4Desjardins M. Huber L.A. Parton R.G. Griffiths G. Biogenesis of phagolysosomes proceeds through a sequential series of interactions with the endocytic apparatus.J. Cell Biol. 1994; 124: 677-688Crossref PubMed Scopus (559) Google Scholar, 5Pitt A. Mayorga L.S. Stahl P.D. Schwartz A.L. Alterations in the protein composition of maturing phagosomes.J. Clin. Invest. 1992; 90: 1978-1983Crossref PubMed Scopus (172) Google Scholar, M. G. A. Griffiths G. Huber L.A. of phagosomes.J. Biol. Chem. 1994; Full Text PDF PubMed Google Scholar). analyses proteomics to the of a large of proteins on phagosomes from and model (6Gotthardt D. Blancheteau V. Bosserhoff A. Ruppert T. Delorenzi M. Soldati T. Proteomics fingerprinting of phagosome maturation and evidence for the role of a Galpha during uptake.Mol. Cell. Proteomics. 2006; 5: 2228-2243Abstract Full Text Full Text PDF PubMed Scopus (86) Google Scholar, J. Diez R. Kieffer S. Dermine J.F. Duclos S. Gagnon E. Sadoul R. Rondeau C. Desjardins M. The phagosome proteome: insight into phagosome functions.J. Cell Biol. 2001; 152: 165-180Crossref PubMed Scopus (606) Google Scholar, I. M. Boulais J. Duclos S. S. E. P. Thibault P. E. P. Desjardins M. of the phagosome proteome by Cell. Proteomics. 2008; Full Text Full Text PDF PubMed Scopus Google Scholar, Boulais J. Brunet S. I. Goyette G. Rondeau C. S. P. F. C. Desjardins M. of the 2007; PubMed Scopus Google Scholar, C. T. of phagosomes of and Cell. Proteomics. 2006; 5: Full Text Full Text PDF PubMed Scopus Google Scholar, M. K. T. of in the Cell. 2005; PubMed Scopus Google Scholar, The dynamic phagosomal proteome and the of the 2007; PubMed Scopus Google Scholar, M. S. M. Desjardins M. Thibault P. The phagosomal proteome in Full Text Full Text PDF PubMed Scopus Google Scholar), into the functions of this of the novel from these that phagosomes display membrane microdomains proteins assemble (7Garin J. Diez R. Kieffer S. Dermine J.F. Duclos S. Gagnon E. Sadoul R. Rondeau C. Desjardins M. The phagosome proteome: insight into phagosome functions.J. Cell Biol. 2001; 152: 165-180Crossref PubMed Scopus (606) Google Scholar, J.F. Duclos S. Garin J. St-Louis F. Rea S. Parton R.G. Desjardins M. Flotillin-1-enriched lipid raft on maturing phagosomes.J. Biol. Chem. 2001; Full Text Full Text PDF PubMed Scopus Google Scholar, J.F. Goyette G. M. Desjardins M. phagosome microdomains in 2005; PubMed Scopus Google Scholar). This novel indicated that than an organelle and proteins are the phagosome membrane microdomains molecules are enabling specialized functions to the of phagosome functions during phagolysosome biogenesis occur not on a also through in the of proteins in of the organelle The data the of the complex modulation of the phagosome proteome during phagolysosome biogenesis. the of the detergent-soluble and of phagosomes the of the dynamic reorganization of the phagosome membrane during phagolysosome biogenesis. of the phagosome composition during phagolysosome biogenesis in previous for the of proteins to the of phagosomes to kill and degrade microorganisms for antigen J.M. through the Cell Biol. 2008; PubMed Scopus Google Scholar, M. S. M. Desjardins M. Thibault P. The phagosomal proteome in Full Text Full Text PDF PubMed Scopus Google Scholar, D. MHC molecules and antigen processing in Immunol. PubMed Scopus Google Scholar). data indicate that phagolysosome biogenesis is by the of various and phagolysosome maturation, and their in phagosomes, that these are not to phagosomes in from of the in the of the phagosome and the of also on maturing phagosomes. These are with a study the of proteins by the of The dynamic phagosomal proteome and the of the 2007; PubMed Scopus Google Scholar). of the an during phagosome that the a role in membrane fusion C. S. M. A. formation by in the of membrane 2001; PubMed Scopus Google Scholar). The of in the on and as the fusion process to the proposal these the of the lipid by of the highly C. S. M. A. formation by in the of membrane 2001; PubMed Scopus Google Scholar). confirmed that the protein in late phagosomes S. and at during Immunol. PubMed Scopus Google Scholar), supporting the that this in of the The role of the lipid as of by and that the association the by C. K. S. 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Our data also to the analyses of the of membrane microdomains. the of the proteins in and the of and the of their we to that might the of microdomains during Our data indicate that the phagosomal proteins that during to mammals, with the proteins in such as to that the of these protein of in to with proteins in the proteins that in such as a role in innate with proteins in These data also the proposal that the organization of membrane microdomains might by events that during The of in a one of the important in the of structures as an to with J. Google Scholar). large of is and are in and in is the is that the the of the of molecules and their into as an to with J. Google Scholar, in Google Scholar, and membrane from membrane to PubMed Scopus Google Scholar). is of to that from to are the that from in Google Scholar), a that to the of cells to assemble and membrane microdomains on organelles. In that analyses of the lipid molecules on phagosomes and are microdomains of this the of novel that the of membrane microdomains with with proteomics analyses indicate that phagosome microdomains are dynamic structures that assemble and during phagolysosome biogenesis. to the modulation of phagosome functional events with the emergence of novel proteins and as well as in lipid are likely to to the emergence of microdomains during R. and for their in generating the proteomics with

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