Unraveling the human dendritic cell phagosome proteome by organellar enrichment ranking

Journal of Proteomics

Volumn 75, Issue 5, 2012, Pages 1547-1562

  Buschow, Sonja I ^a   Lasonder, Edwin ^a   Szklarczyk, Radek ^a   Oud, Machteld M ^a   de Vries, I Jolanda M ^a   Figdor, Carl G ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Antigen presentation; Dendritic cell; Galectin 9; Phagocytosis; Phagosome interaction network; Proteomics

Indexed keywords

ADENOSINE TRIPHOSPHATASE; CELL SURFACE RECEPTOR; ECALECTIN; LYSOSOME ENZYME; RAB PROTEIN; SNARE PROTEIN;

ANTIGEN PRESENTATION; ARTICLE; CONFOCAL MICROSCOPY; DENDRITIC CELL; ENDOSOME; ENZYME ACTIVITY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; IN VITRO STUDY; LIQUID CHROMATOGRAPHY; ORGANELLAR ENRICHMENT RANKING; PHAGOSOME; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PURIFICATION; PROTEIN STRUCTURE; PROTEOMICS; TANDEM MASS SPECTROMETRY; WESTERN BLOTTING;

ANTIGEN PRESENTATION; CELLS, CULTURED; DENDRITIC CELLS; HUMANS; MASS SPECTROMETRY; MONOCYTES; PHAGOCYTOSIS; PHAGOSOMES; PROTEOME;

EID: 84856317475     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2011.11.024     Document Type: Article

References (64)

1. Banchereau J., Steinman R.M. Dendritic cells and the control of immunity. Nature 1998, 392:245-252.
2. Savina A., Amigorena S. Phagocytosis and antigen presentation in dendritic cells. Immunol Rev 2007, 219:143-156.
3. Stuart L.M., Ezekowitz R.A. Phagocytosis: elegant complexity. Immunity 2005, 22:539-550.
4. Blander J.M. Signalling and phagocytosis in the orchestration of host defence. Cell Microbiol 2007, 9:290-299.
5. Underhill D.M., Gantner B. Integration of Toll-like receptor and phagocytic signaling for tailored immunity. Microbes Infect 2004, 6:1368-1373.
6. Rogers L.D., Foster L.J. Contributions of proteomics to understanding phagosome maturation. Cell Microbiol 2008, 10:1405-1412.
7. Li Q., Jagannath C., Rao P.K., Singh C.R., Lostumbo G. Analysis of phagosomal proteomes: from latex-bead to bacterial phagosomes. Proteomics 2010, 10:4098-4116.
8. Boulais J., Trost M., Landry C.R., Dieckmann R., Levy E.D., Soldati T., et al. Molecular characterization of the evolution of phagosomes. Mol Syst Biol 2010, 6:423.
9. Ishihama Y., Oda Y., Tabata T., Sato T., Nagasu T., Rappsilber J., et al. Exponentially modified protein abundance index (emPAI) for estimation of absolute protein amount in proteomics by the number of sequenced peptides per protein. Mol Cell Proteomics 2005, 4:1265-1272.
10. Rogers L.D., Foster L.J. The dynamic phagosomal proteome and the contribution of the endoplasmic reticulum. Proc Natl Acad Sci U S A 2007, 104:18520-18525.
11. Foster L.J., de Hoog C.L., Zhang Y., Zhang Y., Xie X., Mootha V.K., et al. A mammalian organelle map by protein correlation profiling. Cell 2006, 125:187-199.
12. Borner G.H., Harbour M., Hester S., Lilley K.S., Robinson M.S. Comparative proteomics of clathrin-coated vesicles. J Cell Biol 2006, 175:571-578.
13. Zheng Y.Z., Berg K.B., Foster L.J. Mitochondria do not contain lipid rafts, and lipid rafts do not contain mitochondrial proteins. J Lipid Res 2009, 50:988-998.
14. Gilchrist A., Au C.E., Hiding J., Bell A.W., Fernandez-Rodriguez J., Lesimple S., et al. Quantitative proteomics analysis of the secretory pathway. Cell 2006, 127:1265-1281.
15. Jonuleit H., Kuhn U., Muller G., Steinbrink K., Paragnik L., Schmitt E., et al. Pro-inflammatory cytokines and prostaglandins induce maturation of potent immunostimulatory dendritic cells under fetal calf serum-free conditions. Eur J Immunol 1997, 27:3135-3142.
16. Desjardins M., Celis J.E., van Meer G., Dieplinger H., Jahraus A., Griffiths G., et al. Molecular characterization of phagosomes. J Biol Chem 1994, 269:32194-32200.
17. Bolte S., Cordelieres F.P. A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 2006, 224:213-232.
18. Tacken P.J., de Vries I.J., Gijzen K., Joosten B., Wu D., Rother R.P., et al. Effective induction of naive and recall T-cell responses by targeting antigen to human dendritic cells via a humanized anti-DC-SIGN antibody. Blood 2005, 106:1278-1285.
19. Lasonder E., Ishihama Y., Andersen J.S., Vermunt A.M., Pain A., Sauerwein R.W., et al. Analysis of the Plasmodium falciparum proteome by high-accuracy mass spectrometry. Nature 2002, 419:537-542.
20. Rappsilber J., Ishihama Y., Mann M. Stop and go extraction tips for matrix-assisted laser desorption/ionization, nanoelectrospray, and LC/MS sample pretreatment in proteomics. Anal Chem 2003, 75:663-670.
21. Cox J., Mann M. MaxQuant enables high peptide identification rates, individualized p.p.b.-range mass accuracies and proteome-wide protein quantification. Nat Biotechnol 2008, 26:1367-1372.
22. Ishihama Y., Schmidt T., Rappsilber J., Mann M., Hartl F.U., Kerner M.J., et al. Protein abundance profiling of the Escherichia coli cytosol. BMC Genomics 2008, 9:102.
23. Buschow S.I., Lasonder E., van Deutekom H.W., Oud M.M., Beltrame L., Huynen M.A., et al. Dominant processes during human dendritic cell maturation revealed by integration of proteome and transcriptome at the pathway level. J Proteome Res 2010, 9:1727-1737.
24. Dennis G., Sherman B.T., Hosack D.A., Yang J., Gao W., Lane H.C., et al. DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 2003, 4:P3.
25. Hosack D.A., Dennis G., Sherman B.T., Lane H.C., Lempicki R.A. Identifying biological themes within lists of genes with EASE. Genome Biol 2003, 4:R70.
26. Burlak C., Whitney A.R., Mead D.J., Hackstadt T., Deleo F.R. Maturation of human neutrophil phagosomes includes incorporation of molecular chaperones and endoplasmic reticulum quality control machinery. Mol Cell Proteomics 2006, 5:620-634.
27. Lee B.Y., Jethwaney D., Schilling B., Clemens D.L., Gibson B.W., Horwitz M.A. The Mycobacterium bovis bacille Calmette-Guerin phagosome proteome. Mol Cell Proteomics 2010, 9:32-53.
28. Trost M., English L., Lemieux S., Courcelles M., Desjardins M., Thibault P. The phagosomal proteome in interferon-gamma-activated macrophages. Immunity 2009, 30:143-154.
29. Szklarczyk D., Franceschini A., Kuhn M., Simonovic M., Roth A., Minguez P., et al. The STRING database in 2011: functional interaction networks of proteins, globally integrated and scored. Nucleic Acids Res 2011, 39:D561-D568.
30. Engering A., Geijtenbeek T.B., van Vliet S.J., Wijers M., van Liempt E., Demaurex N., et al. The dendritic cell-specific adhesion receptor DC-SIGN internalizes antigen for presentation to T cells. J Immunol 2002, 168:2118-2126.
31. Cambi A., Gijzen K., de Vries J.M., Torensma R., Joosten B., Adema G.J., et al. The C-type lectin DC-SIGN (CD209) is an antigen-uptake receptor for Candida albicans on dendritic cells. Eur J Immunol 2003, 33:532-538.
32. Gringhuis S.I., den Dunnen J., Litjens M., van der Vlist M., Geijtenbeek T.B. Carbohydrate-specific signaling through the DC-SIGN signalosome tailors immunity to Mycobacterium tuberculosis, HIV-1 and Helicobacter pylori. Nat Immunol 2009, 10:1081-1088.
33. Gringhuis S.I., den Dunnen J., Litjens M., van Het Hof B., van Kooyk Y., Geijtenbeek T.B. C-type lectin DC-SIGN modulates Toll-like receptor signaling via Raf-1 kinase-dependent acetylation of transcription factor NF-kappaB. Immunity 2007, 26:605-616.
34. Heil F., Hemmi H., Hochrein H., Ampenberger F., Kirschning C., Akira S., et al. Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science 2004, 303:1526-1529.
35. Mantegazza A.R., Savina A., Vermeulen M., Perez L., Geffner J., Hermine O., et al. NADPH oxidase controls phagosomal pH and antigen cross-presentation in human dendritic cells. Blood 2008, 112:4712-4722.
36. Rabinovich G.A., Toscano M.A. Turning 'sweet' on immunity: galectin-glycan interactions in immune tolerance and inflammation. Nat Rev 2009, 9:338-352.
37. Sato S., St-Pierre C., Bhaumik P., Nieminen J. Galectins in innate immunity: dual functions of host soluble beta-galactoside-binding lectins as damage-associated molecular patterns (DAMPs) and as receptors for pathogen-associated molecular patterns (PAMPs). Immunol Rev 2009, 230:172-187.
38. Katoh S., Ishii N., Nobumoto A., Takeshita K., Dai S.Y., Shinonaga R., et al. Galectin-9 inhibits CD44-hyaluronan interaction and suppresses a murine model of allergic asthma. Am J Respir Crit Care Med 2007, 176:27-35.
39. Tanikawa R., Tanikawa T., Hirashima M., Yamauchi A., Tanaka Y. Galectin-9 induces osteoblast differentiation through the CD44/Smad signaling pathway. Biochem Biophys Res Commun 2010, 394:317-322.
40. Vachon E., Martin R., Plumb J., Kwok V., Vandivier R.W., Glogauer M., et al. CD44 is a phagocytic receptor. Blood 2006, 107:4149-4158.
41. Dunkley T.P., Watson R., Griffin J.L., Dupree P., Lilley K.S. Localization of organelle proteins by isotope tagging (LOPIT). Mol Cell Proteomics 2004, 3:1128-1134.
42. Haas A. The phagosome: compartment with a license to kill. Traffic 2007, 8:311-330.
43. Gagnon E., Duclos S., Rondeau C., Chevet E., Cameron P.H., Steele-Mortimer O., et al. Endoplasmic reticulum-mediated phagocytosis is a mechanism of entry into macrophages. Cell 2002, 110:119-131.
44. Guermonprez P., Saveanu L., Kleijmeer M., Davoust J., Van Endert P., Amigorena S. ER-phagosome fusion defines an MHC class I cross-presentation compartment in dendritic cells. Nature 2003, 425:397-402.
45. Ackerman A.L., Giodini A., Cresswell P. A role for the endoplasmic reticulum protein retrotranslocation machinery during crosspresentation by dendritic cells. Immunity 2006, 25:607-617.
46. Touret N., Paroutis P., Terebiznik M., Harrison R.E., Trombetta S., Pypaert M., et al. Quantitative and dynamic assessment of the contribution of the ER to phagosome formation. Cell 2005, 123:157-170.
47. Ehlers M.R. CR3: a general purpose adhesion-recognition receptor essential for innate immunity. Microbes Infect 2000, 2:289-294.
48. Vachon E., Martin R., Kwok V., Cherepanov V., Chow C.W., Doerschuk C.M., et al. CD44-mediated phagocytosis induces inside-out activation of complement receptor-3 in murine macrophages. Blood 2007, 110:4492-4502.
49. van Helden S.F., Krooshoop D.J., Broers K.C., Raymakers R.A., Figdor C.G., van Leeuwen F.N. A critical role for prostaglandin E2 in podosome dissolution and induction of high-speed migration during dendritic cell maturation. J Immunol 2006, 177:1567-1574.
50. Brown D.P., Jones D.C., Anderson K.J., Lapaque N., Buerki R.A., Trowsdale J., et al. The inhibitory receptor LILRB4 (ILT3) modulates antigen presenting cell phenotype and, along with LILRB2 (ILT4), is upregulated in response to Salmonella infection. BMC Immunol 2009, 10:56.
51. Akashi-Takamura S., Miyake K. TLR accessory molecules. Curr Opin Immunol 2008, 20:420-425.
52. Chapuis F., Rosenzwajg M., Yagello M., Ekman M., Biberfeld P., Gluckman J.C. Differentiation of human dendritic cells from monocytes in vitro. Eur J Immunol 1997, 27:431-441.
53. Baumann C.L., Aspalter I.M., Sharif O., Pichlmair A., Bluml S., Grebien F., et al. CD14 is a coreceptor of Toll-like receptors 7 and 9. J Exp Med 2010, 207:2689-2701.
54. Jialin G., Xuefan G., Huiwen Z. SID1 transmembrane family, member 2 (Sidt2): a novel lysosomal membrane protein. Biochem Biophys Res Commun 2010, 402:588-594.
55. Eberle H.B., Serrano R.L., Fullekrug J., Schlosser A., Lehmann W.D., Lottspeich F., et al. Identification and characterization of a novel human plant pathogenesis-related protein that localizes to lipid-enriched microdomains in the Golgi complex. J Cell Sci 2002, 115:827-838.
56. Chiampanichayakul S., Khunkaewla P., Pata S., Kasinrerk W. Na, K ATPase beta3 subunit (CD298): association with alpha subunit and expression on peripheral blood cells. Tissue Antigens 2006, 68:509-517.
57. Hebert S.C., Mount D.B., Gamba G. Molecular physiology of cation-coupled Cl- cotransport: the SLC12 family. Pflugers Arch 2004, 447:580-593.
58. Matsumoto R., Matsumoto H., Seki M., Hata M., Asano Y., Kanegasaki S., et al. Human ecalectin, a variant of human galectin-9, is a novel eosinophil chemoattractant produced by T lymphocytes. J Biol Chem 1998, 273:16976-16984.
59. Dai S.Y., Nakagawa R., Itoh A., Murakami H., Kashio Y., Abe H., et al. Galectin-9 induces maturation of human monocyte-derived dendritic cells. J Immunol 2005, 175:2974-2981.
60. Tanikawa R., Tanikawa T., Okada Y., Nakano K., Hirashima M., Yamauchi A., et al. Interaction of galectin-9 with lipid rafts induces osteoblast proliferation through the c-Src/ERK signaling pathway. J Bone Miner Res 2008, 23:278-286.
61. Wada J., Ota K., Kumar A., Wallner E.I., Kanwar Y.S. Developmental regulation, expression, and apoptotic potential of galectin-9, a beta-galactoside binding lectin. J Clin Invest 1997, 99:2452-2461.
62. Nobumoto A., Nagahara K., Oomizu S., Katoh S., Nishi N., Takeshita K., et al. Galectin-9 suppresses tumor metastasis by blocking adhesion to endothelium and extracellular matrices. Glycobiology 2008, 18:735-744.
63. Tanikawa R., Tanikawa T., Hirashima M., Yamauchi A., Tanaka Y. Galectin-9 induces osteoblast differentiation through the CD44/Smad signaling pathway. Biochem Biophys Res Commun 2010, 394:317-322.
64. Lipkowitz M.S., Leal-Pinto E., Cohen B.E., Abramson R.G. Galectin 9 is the sugar-regulated urate transporter/channel UAT. Glycoconj J 2004, 19:491-498.