Dominant processes during human dendritic cell maturation revealed by integration of proteome and transcriptome at the pathway level

Journal of Proteome Research

Volumn 9, Issue 4, 2010, Pages 1727-1737

  Buschow, Sonja I ^a   Lasonder, Edwin ^a   Van Deutekom, Hanneke W M ^a   Oud, MacHteld M ^a   Beltrame, Luca ^b   Huynen, Martijn A ^a   De Vries, I Jolanda M ^a   Figdor, Carl G ^a   Cavalieri, Duccio ^b  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF FLORENCE   (Italy)

Author keywords

Antigen presenting cell; Dendritic cell; Pathway analysis; Proteomics; Transcriptomics

Indexed keywords

CYTOKINE; MESSENGER RNA; PROTEOME; TRANSCRIPTOME;

ARTICLE; CELL ADHESION; CELL MATURATION; CELL MIGRATION; DENDRITIC CELL; HUMAN; HUMAN CELL; LIPID METABOLISM; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION;

CELL ADHESION; CELL DIFFERENTIATION; CELL MOVEMENT; CYTOKINES; DENDRITIC CELLS; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; HUMANS; PROTEOME; REPRODUCIBILITY OF RESULTS; RNA, MESSENGER; SIGNAL TRANSDUCTION;

EID: 77950635701     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr9008546     Document Type: Article

References (49)

1. Banchereau, J.; Steinman, R. M. Dendritic cells and the control of immunity Nature 1998, 392 (6673) 245 - 52
2. Guermonprez, P.; Valladeau, J.; Zitvogel, L.; Thery, C.; Amigorena, S. Antigen presentation and T cell stimulation by dendritic cells Annu. Rev. Immunol. 2002, 20, 621 - 67
3. Steinman, R. M.; Hawiger, D.; Nussenzweig, M. C. Tolerogenic dendritic cells Annu. Rev. Immunol. 2003, 21, 685 - 711
4. Joffre, O.; Nolte, M. A.; Sporri, R.; Reis e Sousa, C. Inflammatory signals in dendritic cell activation and the induction of adaptive immunity Immunol. Rev. 2009, 227 (1) 234 - 47
5. Steinman, R. M.; Banchereau, J. Taking dendritic cells into medicine Nature 2007, 449 (7161) 419 - 26
6. Aarntzen, E. H.; Figdor, C. G.; Adema, G. J.; Punt, C. J.; de Vries, I. J. Dendritic cell vaccination and immune monitoring Cancer Immunol. Immunother. 2008, 57 (10) 1559 - 68
7. de Vries, I. J.; Lesterhuis, W. J.; Scharenborg, N. M.; Engelen, L. P.; Ruiter, D. J.; Gerritsen, M. J.; Croockewit, S.; Britten, C. M.; Torensma, R.; Adema, G. J.; Figdor, C. G.; Punt, C. J. Maturation of dendritic cells is a prerequisite for inducing immune responses in advanced melanoma patients Clin. Cancer Res. 2003, 9 (14) 5091 - 100
8. Tang, Z.; Saltzman, A. Understanding human dendritic cell biology through gene profiling Inflamm. Res. 2004, 53 (9) 424 - 41
9. Manoli, T.; Gretz, N.; Grone, H. J.; Kenzelmann, M.; Eils, R.; Brors, B. Group testing for pathway analysis improves comparability of different microarray datasets Bioinformatics 2006, 22 (20) 2500 - 6
10. Beltrame, L.; Rizzetto, L.; Paola, R.; Rocca-Serra, P.; Gambineri, L.; Battaglia, C.; Cavalieri, D. Using pathway signatures as means of identifying similarities among microarray experiments PLoS ONE 2009, 4 (1) e4128
11. Le Naour, F.; Hohenkirk, L.; Grolleau, A.; Misek, D. E.; Lescure, P.; Geiger, J. D.; Hanash, S.; Beretta, L. Profiling changes in gene expression during differentiation and maturation of monocyte-derived dendritic cells using both oligonucleotide microarrays and proteomics J. Biol. Chem. 2001, 276 (21) 17920 - 31
12. Pereira, S. R.; Faca, V. M.; Gomes, G. G.; Chammas, R.; Fontes, A. M.; Covas, D. T.; Greene, L. J. Changes in the proteomic profile during differentiation and maturation of human monocyte-derived dendritic cells stimulated with granulocyte macrophage colony stimulating factor/interleukin-4 and lipopolysaccharide Proteomics 2005, 5 (5) 1186 - 98
13. Watarai, H.; Hinohara, A.; Nagafune, J.; Nakayama, T.; Taniguchi, M.; Yamaguchi, Y. Plasma membrane-focused proteomics: dramatic changes in surface expression during the maturation of human dendritic cells Proteomics 2005, 5 (15) 4001 - 11
14. Horlock, C.; Shakib, F.; Mahdavi, J.; Jones, N. S.; Sewell, H. F.; Ghaemmaghami, A. M. Analysis of proteomic profiles and functional properties of human peripheral blood myeloid dendritic cells, monocyte-derived dendritic cells and the dendritic cell-like KG-1 cells reveals distinct characteristics Genome Biol. 2007, 8 (3) R30
15. Gundacker, N. C.; Haudek, V. J.; Wimmer, H.; Slany, A.; Griss, J.; Bochkov, V.; Zielinski, C.; Wagner, O.; Stockl, J.; Gerner, C. Cytoplasmic proteome and secretome profiles of differently stimulated human dendritic cells J. Proteome Res. 2009, 8 (6) 2799 - 811
16. Jonuleit, H.; Kuhn, U.; Muller, G.; Steinbrink, K.; Paragnik, L.; Schmitt, E.; Knop, J.; Enk, A. H. Pro-inflammatory cytokines and prostaglandins induce maturation of potent immunostimulatory dendritic cells under fetal calf serum-free conditions Eur. J. Immunol. 1997, 27 (12) 3135 - 42
17. de Vries, I. J.; Eggert, A. A.; Scharenborg, N. M.; Vissers, J. L.; Lesterhuis, W. J.; Boerman, O. C.; Punt, C. J.; Adema, G. J.; Figdor, C. G. Phenotypical and functional characterization of clinical grade dendritic cells J. Immunother. 2002, 25 (5) 429 - 38
18. Irizarry, R. A.; Hobbs, B.; Collin, F.; Beazer-Barclay, Y. D.; Antonellis, K. J.; Scherf, U.; Speed, T. P. Exploration, normalization, and summaries of high density oligonucleotide array probe level data Biostatistics 2003, 4 (2) 249 - 64
19. Dai, M.; Wang, P.; Boyd, A. D.; Kostov, G.; Athey, B.; Jones, E. G.; Bunney, W. E.; Myers, R. M.; Speed, T. P.; Akil, H.; Watson, S. J.; Meng, F. Evolving gene/transcript definitions significantly alter the interpretation of GeneChip data Nucleic Acids Res. 2005, 33 (20) e175
20. Lasonder, E.; Ishihama, Y.; Andersen, J. S.; Vermunt, A. M.; Pain, A.; Sauerwein, R. W.; Eling, W. M.; Hall, N.; Waters, A. P.; Stunnenberg, H. G.; Mann, M. Analysis of the Plasmodium falciparum proteome by high-accuracy mass spectrometry Nature 2002, 419 (6906) 537 - 42
21. 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 (3) 663 - 70
22. Ishihama, Y.; Oda, Y.; Tabata, T.; Sato, T.; Nagasu, T.; Rappsilber, J.; Mann, M. 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 (9) 1265 - 72
23. Ishihama, Y.; Schmidt, T.; Rappsilber, J.; Mann, M.; Hartl, F. U.; Kerner, M. J.; Frishman, D. Protein abundance profiling of the Escherichia coli cytosol BMC Genomics 2008, 9, 102
24. Cavalieri, D.; Castagnini, C.; Toti, S.; Maciag, K.; Kelder, T.; Gambineri, L.; Angioli, S.; Dolara, P. Eu.Gene Analyzer a tool for integrating gene expression data with pathway databases Bioinformatics 2007, 23 (19) 2631 - 2
25. Grosu, P.; Townsend, J. P.; Hartl, D. L.; Cavalieri, D. Pathway Processor: a tool for integrating whole-genome expression results into metabolic networks Genome Res. 2002, 12 (7) 1121 - 6
26. Huang da, W.; Sherman, B. T.; Lempicki, R. A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources Nat. Protoc. 2009, 4 (1) 44 - 57
27. Dennis, G., Jr.; Sherman, B. T.; Hosack, D. A.; Yang, J.; Gao, W.; Lane, H. C.; Lempicki, R. A. DAVID: Database for Annotation, Visualization, and Integrated Discovery Genome Biol. 2003, 4 (5) P3
28. Segota, I.; Bartonicek, N.; Vlahovicek, K. MADNet: microarray database network web server Nucleic Acids Res. 2008, 36 (Web Server issue) W332 - 5
29. Benjamini, Y.; Drai, D.; Elmer, G.; Kafkafi, N.; Golani, I. Controlling the false discovery rate in behavior genetics research Behav. Brain Res. 2001, 125 (1-2) 279 - 84
30. Mathivanan, S.; Ahmed, M.; Ahn, N. G.; Alexandre, H.; Amanchy, R.; Andrews, P. C.; Bader, J. S.; Balgley, B. M.; Bantscheff, M.; Bennett, K. L.; Bjorling, E.; Blagoev, B.; Bose, R.; Brahmachari, S. K.; Burlingame, A. S.; Bustelo, X. R.; Cagney, G.; Cantin, G. T.; Cardasis, H. L.; Celis, J. E.; Chaerkady, R.; Chu, F.; Cole, P. A.; Costello, C. E.; Cotter, R. J.; Crockett, D.; DeLany, J. P.; De Marzo, A. M.; DeSouza, L. V.; Deutsch, E. W.; Dransfield, E.; Drewes, G.; Droit, A.; Dunn, M. J.; Elenitoba-Johnson, K.; Ewing, R. M.; Van Eyk, J.; Faca, V.; Falkner, J.; Fang, X.; Fenselau, C.; Figeys, D.; Gagne, P.; Gelfi, C.; Gevaert, K.; Gimble, J. M.; Gnad, F.; Goel, R.; Gromov, P.; Hanash, S. M.; Hancock, W. S.; Harsha, H. C.; Hart, G.; Hays, F.; He, F.; Hebbar, P.; Helsens, K.; Hermeking, H.; Hide, W.; Hjerno, K.; Hochstrasser, D. F.; Hofmann, O.; Horn, D. M.; Hruban, R. H.; Ibarrola, N.; James, P.; Jensen, O. N.; Jensen, P. H.; Jung, P.; Kandasamy, K.; Kheterpal, I.; Kikuno, R. F.; Korf, U.; Korner, R.; Kuster, B.; Kwon, M. S.; Lee, H. J.; Lee, Y. J.; Lefevre, M.; Lehvaslaiho, M.; Lescuyer, P.; Levander, F.; Lim, M. S.; Lobke, C.; Loo, J. A.; Mann, M.; Martens, L.; Martinez-Heredia, J.; McComb, M.; McRedmond, J.; Mehrle, A.; Menon, R.; Miller, C. A.; Mischak, H.; Mohan, S. S.; Mohmood, R.; Molina, H.; Moran, M. F.; Morgan, J. D.; Moritz, R.; Morzel, M.; Muddiman, D. C.; Nalli, A.; Navarro, J. D.; Neubert, T. A.; Ohara, O.; Oliva, R.; Omenn, G. S.; Oyama, M.; Paik, Y. K.; Pennington, K.; Pepperkok, R.; Periaswamy, B.; Petricoin, E. F.; Poirier, G. G.; Prasad, T. S.; Purvine, S. O.; Rahiman, B. A.; Ramachandran, P.; Ramachandra, Y. L.; Rice, R. H.; Rick, J.; Ronnholm, R. H.; Salonen, J.; Sanchez, J. C.; Sayd, T.; Seshi, B.; Shankari, K.; Sheng, S. J.; Shetty, V.; Shivakumar, K.; Simpson, R. J.; Sirdeshmukh, R.; Siu, K. W.; Smith, J. C.; Smith, R. D.; States, D. J.; Sugano, S.; Sullivan, M.; Superti-Furga, G.; Takatalo, M.; Thongboonkerd, V.; Trinidad, J. C.; Uhlen, M.; Vandekerckhove, J.; Vasilescu, J.; Veenstra, T. D.; Vidal-Taboada, J. M.; Vihinen, M.; Wait, R.; Wang, X.; Wiemann, S.; Wu, B.; Xu, T.; Yates, J. R.; Zhong, J.; Zhou, M.; Zhu, Y.; Zurbig, P.; Pandey, A. Human Proteinpedia enables sharing of human protein data Nat. Biotechnol. 2008, 26 (2) 164 - 7
31. Whiteside, T. L.; Odoux, C. Dendritic cell biology and cancer therapy Cancer Immunol. Immunother. 2004, 53 (3) 240 - 8
32. Lehner, M.; Morhart, P.; Stilper, A.; Petermann, D.; Weller, P.; Stachel, D.; Holter, W. Efficient chemokine-dependent migration and primary and secondary IL-12 secretion by human dendritic cells stimulated through Toll-like receptors J. Immunother. 2007, 30 (3) 312 - 22
33. Waters, K. M.; Pounds, J. G.; Thrall, B. D. Data merging for integrated microarray and proteomic analysis Brief Funct. Genomic Proteomic 2006, 5 (4) 261 - 72
34. Randolph, G. J.; Ochando, J.; Partida-Sanchez, S. Migration of dendritic cell subsets and their precursors Annu. Rev. Immunol. 2008, 26, 293 - 316
35. Tontonoz, P.; Spiegelman, B. M. Fat and beyond: the diverse biology of PPARgamma Annu. Rev. Biochem. 2008, 77, 289 - 312
36. Nencioni, A.; Grunebach, F.; Zobywlaski, A.; Denzlinger, C.; Brugger, W.; Brossart, P. Dendritic cell immunogenicity is regulated by peroxisome proliferator-activated receptor gamma J. Immunol. 2002, 169 (3) 1228 - 35
37. Szatmari, I.; Gogolak, P.; Im, J. S.; Dezso, B.; Rajnavolgyi, E.; Nagy, L. Activation of PPARgamma specifies a dendritic cell subtype capable of enhanced induction of iNKT cell expansion Immunity 2004, 21 (1) 95 - 106
38. Szatmari, I.; Nagy, L. Nuclear receptor signalling in dendritic cells connects lipids, the genome and immune function Embo J. 2008, 27 (18) 2353 - 62
39. Varga, T.; Nagy, L. Nuclear receptors, transcription factors linking lipid metabolism and immunity: the case of peroxisome proliferator-activated receptor gamma Eur. J. Clin. Invest. 2008, 38 (10) 695 - 707
40. Szatmari, I.; Torocsik, D.; Agostini, M.; Nagy, T.; Gurnell, M.; Barta, E.; Chatterjee, K.; Nagy, L. PPARgamma regulates the function of human dendritic cells primarily by altering lipid metabolism Blood 2007, 110 (9) 3271 - 80
41. Ye, J. Regulation of PPARgamma function by TNF-alpha Biochem. Biophys. Res. Commun. 2008, 374 (3) 405 - 8
42. Selenko-Gebauer, N.; Majdic, O.; Szekeres, A.; Hofler, G.; Guthann, E.; Korthauer, U.; Zlabinger, G.; Steinberger, P.; Pickl, W. F.; Stockinger, H.; Knapp, W.; Stockl, J. B7-H1 (programmed death-1 ligand) on dendritic cells is involved in the induction and maintenance of T cell anergy J. Immunol. 2003, 170 (7) 3637 - 44
43. Keir, M. E.; Butte, M. J.; Freeman, G. J.; Sharpe, A. H. PD-1 and its ligands in tolerance and immunity Annu. Rev. Immunol. 2008, 26, 677 - 704
44. Sharpe, A. H.; Wherry, E. J.; Ahmed, R.; Freeman, G. J. The function of programmed cell death 1 and its ligands in regulating autoimmunity and infection Nat. Immunol. 2007, 8 (3) 239 - 45
45. Brown, J. A.; Dorfman, D. M.; Ma, F. R.; Sullivan, E. L.; Munoz, O.; Wood, C. R.; Greenfield, E. A.; Freeman, G. J. Blockade of programmed death-1 ligands on dendritic cells enhances T cell activation and cytokine production J. Immunol. 2003, 170 (3) 1257 - 66
46. Dong, H.; Zhu, G.; Tamada, K.; Chen, L. B7-H1, a third member of the B7 family, co-stimulates T-cell proliferation and interleukin-10 secretion Nat. Med. 1999, 5 (12) 1365 - 9
47. Woodfin, A.; Voisin, M. B.; Nourshargh, S. PECAM-1: a multi-functional molecule in inflammation and vascular biology Arterioscler. Thromb. Vasc. Biol. 2007, 27 (12) 2514 - 23
48. Ostermann, G.; Weber, K. S.; Zernecke, A.; Schroder, A.; Weber, C. JAM-1 is a ligand of the beta(2) integrin LFA-1 involved in transendothelial migration of leukocytes Nat. Immunol. 2002, 3 (2) 151 - 8
49. Cera, M. R.; Del Prete, A.; Vecchi, A.; Corada, M.; Martin-Padura, I.; Motoike, T.; Tonetti, P.; Bazzoni, G.; Vermi, W.; Gentili, F.; Bernasconi, S.; Sato, T. N.; Mantovani, A.; Dejana, E. Increased DC trafficking to lymph nodes and contact hypersensitivity in junctional adhesion molecule-A-deficient mice J. Clin. Invest. 2004, 114 (5) 729 - 38