PPARγ modulated inflammatory response of human dendritic cell subsets to engulfed apoptotic neutrophils

Journal of Leukocyte Biology

Volumn 88, Issue 5, 2010, Pages 981-991

  Majai, Gyöngyike ^a,b   Gogolák, Péter ^c   Ambrus, Csilla ^c   Vereb, György ^c   Hodrea, Judit ^a   Fésüs, László ^a   Rajnavölgyi, Éva ^c  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b UNIVERSITY OF DEBRECEN   (Hungary)

^c UNIVERSITY OF DEBRECEN   (Hungary)

Author keywords

Inflammation; Phagocytosis; T lymphocyte

Indexed keywords

CD209 ANTIGEN; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 6; INTERLEUKIN 8; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; ROSIGLITAZONE; T6 ANTIGEN; TUMOR NECROSIS FACTOR ALPHA;

ANTIGEN FUNCTION; APOPTOSIS; ARTICLE; CELL INTERACTION; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOKINE RESPONSE; DENDRITIC CELL; HUMAN; HUMAN CELL; IMMUNOMODULATION; IMMUNOSTIMULATION; MACROPHAGE; MONOCYTE; NEUTROPHIL; NORMAL HUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TH1 CELL;

ANTI-INFLAMMATORY AGENTS; ANTIBODIES, MONOCLONAL; APOPTOSIS; CELL DIFFERENTIATION; COCULTURE TECHNIQUES; CYTOKINES; DENDRITIC CELLS; FLOW CYTOMETRY; HUMANS; INTERFERON-GAMMA; INTERLEUKIN-6; MACROPHAGES; MICROSCOPY, CONFOCAL; MONOCYTES; NEUTROPHILS; PHAGOCYTOSIS; PPAR GAMMA; RETINOID X RECEPTORS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 78649574843     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0310144     Document Type: Article

References (72)

1. Liu, G., Wu, C., Wu, Y., Zhao, Y. (2006) Phagocytosis of apoptotic cells and immune regulation. Scand. J. Immunol. 64, 1-9.
2. Steinman, R. M. (2007) Dendritic cells: understanding immunogenicity. Eur. J. Immunol. 37 (Suppl. 1), S53-S60.
3. Roake, J. A., Rao, A. S., Morris, P. J., Larsen, C. P., Hankins, D. F., Austyn, J. M. (1995) Dendritic cell loss from nonlymphoid tissues after systemic administration of lipopolysaccharide, tumor necrosis factor, and interleukin 1. J. Exp. Med. 181, 2237-2247.
4. Cumberbatch, M., Kimber, I. (1992) Dermal tumor necrosis factor-α induces dendritic cell migration to draining lymph nodes, and possibly provides one stimulus for Langerhans' cell migration. Immunology 75, 257-263.
5. Ravichandran, K. S., Lorenz, U. (2007) Engulfment of apoptotic cells: signals for a good meal. Nat. Rev. Immunol. 7, 964-974.
6. Majai, G., Petrovski, G., Fesus, L. (2006) Inflammation and the apoptophagocytic system. Immunol. Lett. 104, 94-101.
7. Gregory, C. D., Devitt, A. (2004) The macrophage and the apoptotic cell: an innate immune interaction viewed simplistically? Immunology 113, 1-14.
8. Savill, J., Dransfield, I., Gregory, C., Haslett, C. (2002) A blast from the past: clearance of apoptotic cells regulates immune responses. Nat. Rev. Immunol. 2, 965-975. (Pubitemid 37323217)
9. Buttiglieri, S., Galetto, A., Forno, S., De Andrea, M., Matera, L. (2003) Influence of drug-induced apoptotic death on processing and presentation of tumor antigens by dendritic cells. Int. J. Cancer 106, 516-520.
10. Ishii, S., Hiroishi, K., Eguchi, J., Mitamura, K. (2003) Dendritic cell maturation induced by delivery of ultraviolet-mediated apoptotic colorectal cancer cell lines. Anticancer Res. 23, 2457-2463.
11. Goldszmid, R. S., Idoyaga, J., Bravo, A. I., Steinman, R., Mordoh, J., Wainstok, R. (2003) Dendritic cells charged with apoptotic tumor cells induce long-lived protective CD4+ and CD8+ T cell immunity against B16 melanoma. J. Immunol. 171, 5940-5947.
12. Feng, H., Zeng, Y., Graner, M. W., Katsanis, E. (2002) Stressed apoptotic tumor cells stimulate dendritic cells and induce specific cytotoxic T cells. Blood 100, 4108-4115.
13. Hoffmann, T. K., Meidenbauer, N., Dworacki, G., Kanaya, H., Whiteside, T. L. (2000) Generation of tumor-specific T-lymphocytes by cross-priming with human dendritic cells ingesting apoptotic tumor cells. Cancer Res. 60, 3542-3549.
14. Miyasaka, K., Hanayama, R., Tanaka, M., Nagata, S. (2004) Expression of milk fat globule epidermal growth factor 8 in immature dendritic cells for engulfment of apoptotic cells. Eur. J. Immunol. 34, 1414-1422.
15. 5 and CD36, and cross-present antigens to cytotoxic T lymphocytes. J. Exp. Med. 188, 1359-1368.
16. Albert, M. L., Sauter, B., Bhardwaj, N. (1998) Dendritic cells acquire antigen from apoptotic cells and induce class I-restricted CTLs. Nature 392, 86-89.
17. Clayton, A. R., Prue, R. L., Harper, L., Drayson, M. T., Savage, C. O. (2003) Dendritic cell uptake of human apoptotic and necrotic neutrophils inhibits CD40, CD80, and CD86 expression and reduces allogeneic T cell responses: relevance to systemic vasculitis. Arthritis Rheum. 48, 2362-2374. (Pubitemid 36959219)
18. Hickman, H. D., Takeda, K., Skon, C. N., Murray, F. R., Hensley, S. E., Loomis, J., Barber, G. N., Bennink, J. R., Yewdell, J. W. (2008) Direct priming of antiviral CD8+ T cells in the peripheral interfollicular region of lymph nodes. Nat. Immunol. 9, 155-165.
19. Megiovanni, A. M., Sanchez, F., Robledo-Sarmiento, M., Morel, C., Gluckman, J. C., Boudaly, S. (2006) Polymorphonuclear neutrophils deliver activation signals and antigenic molecules to dendritic cells: a new link between leukocytes upstream of T lymphocytes. J. Leukoc. Biol. 79, 977-988.
20. Geijtenbeek, T. B., Torensma, R., van Vliet, S. J., van Duijnhoven, G. C., Adema, G. J., van Kooyk, Y., Figdor, C. G. (2000) Identification of DC-SIGN, a novel dendritic cell-specific ICAM-3 receptor that supports primary immune responses. Cell 100, 575-585.
21. Geijtenbeek, T. B., Krooshoop, D. J., Bleijs, D. A., van Vliet, S. J., van Duijnhoven, G. C., Grabovsky, V., Alon, R., Figdor, C. G., van Kooyk, Y. (2000) DC-SIGN-ICAM-2 interaction mediates dendritic cell trafficking. Nat. Immunol. 1, 353-357.
22. Bogoevska, V., Horst, A., Klampe, B., Lucka, L., Wagener, C., Nollau, P. (2006) CEACAM1, an adhesion molecule of human granulocytes, is fucosylated by fucosyltransferase IX and interacts with DC-SIGN of dendritic cells via Lewis x residues. Glycobiology 16, 197-209.
23. Van Gisbergen, K. P., Sanchez-Hernandez, M., Geijtenbeek, T. B., van Kooyk, Y. (2005) Neutrophils mediate immune modulation of dendritic cells through glycosylation-dependent interactions between Mac-1 and DC-SIGN. J. Exp. Med. 201, 1281-1292.
24. Geijtenbeek, T. B., Van Vliet, S. J., Koppel, E. A., Sanchez-Hernandez, M., Vandenbroucke-Grauls, C. M., Appelmelk, B., Van Kooyk, Y. (2003) Mycobacteria target DC-SIGN to suppress dendritic cell function. J. Exp. Med. 197, 7-17.
25. Aleman, M., de la Barrera, S., Schierloh, P., Yokobori, N., Baldini, M., Musella, R., Abbate, E., Sasiain, M. (2007) Spontaneous or Mycobacterium tuberculosis-induced apoptotic neutrophils exert opposite effects on the dendritic cell-mediated immune response. Eur. J. Immunol. 37, 1524-1537.
26. van Vliet, S. J., van Liempt, E., Geijtenbeek, T. B., van Kooyk, Y. (2006) Differential regulation of C-type lectin expression on tolerogenic dendritic cell subsets. Immunobiology 211, 577-585.
27. Kliewer, S. A., Umesono, K., Noonan, D. J., Heyman, R. A., Evans, R. M. (1992) Convergence of 9-cis retinoic acid and peroxisome proliferator signalling pathways through heterodimer formation of their receptors. Nature 358, 771-774.
28. Nagy, L., Tontonoz, P., Alvarez, J. G., Chen, H., Evans, R. M. (1998) Oxidized LDL regulates macrophage gene expression through ligand activation of PPARγ. Cell 93, 229-240.
29. Kliewer, S. A., Sundseth, S. S., Jones, S. A., Brown, P. J., Wisely, G. B., Koble, C. S., Devchand, P., Wahli, W., Willson, T. M., Lenhard, J. M., Lehmann, J. M. (1997) Fatty acids and eicosanoids regulate gene expression through direct interactions with peroxisome proliferator-activated receptors α and γ. Proc. Natl. Acad. Sci. USA 94, 4318-4323.
30. Krey, G., Braissant, O., L'Horset, F., Kalkhoven, E., Perroud, M., Parker, M. G., Wahli, W. (1997) Fatty acids, eicosanoids, and hypolipidemic agents identified as ligands of peroxisome proliferator-activated receptors by coactivator-dependent receptor ligand assay. Mol. Endocrinol. 11, 779-791.
31. Willson, T. M., Cobb, J. E., Cowan, D. J., Wiethe, R. W., Correa, I. D., Prakash, S. R., Beck, K. D., Moore, L. B., Kliewer, S. A., Lehmann, J. M. (1996) The structure-activity relationship between peroxisome proliferator-activated receptor γ agonism and the antihyperglycemic activity of thiazolidinediones. J. Med. Chem. 39, 665-668.
32. Kliewer, S. A., Lenhard, J. M., Willson, T. M., Patel, I., Morris, D. C., Lehmann, J. M. (1995) A prostaglandin J2 metabolite binds peroxisome proliferator-activated receptor γ and promotes adipocyte differentiation. Cell 83, 813-819.
33. Forman, B. M., Tontonoz, P., Chen, J., Brun, R. P., Spiegelman, B. M., Evans, R. M. (1995) 15-Deoxy-δ 12, 14-prostaglandin J2 is a ligand for the adipocyte determination factor PPAR γ. Cell 83, 803-812.
34. Lehmann, J. M., Moore, L. B., Smith-Oliver, T. A., Wilkison, W. O., Willson, T. M., Kliewer, S. A. (1995) An antidiabetic thiazolidinedione is a high affinity ligand for peroxisome proliferator-activated receptor γ (PPAR γ). J. Biol. Chem. 270, 12953-12956.
35. Beaven, S. W., Tontonoz, P. (2006) Nuclear receptors in lipid metabolism: targeting the heart of dyslipidemia. Annu. Rev. Med. 57, 313-329.
36. Gosset, P., Charbonnier, A. S., Delerive, P., Fontaine, J., Staels, B., Pestel, J., Tonnel, A. B., Trottein, F. (2001) Peroxisome proliferator-activated receptor γ activators affect the maturation of human monocyte-derived dendritic cells. Eur. J. Immunol. 31, 2857-2865.
37. Szatmari, I., Gogolak, P., Im, J. S., Dezso, B., Rajnavolgyi, E., Nagy, L. (2004) Activation of PPARγ specifies a dendritic cell subtype capable of enhanced induction of iNKT cell expansion. Immunity 21, 95-106.
38. Nencioni, A., Grunebach, F., Zobywlaski, A., Denzlinger, C., Brugger, W., Brossart, P. (2002) Dendritic cell immunogenicity is regulated by peroxisome proliferator-activated receptor γ. J. Immunol. 169, 1228-1235. (Pubitemid 34809163)
39. Gogolak, P., Rethi, B., Szatmari, I., Lanyi, A., Dezso, B., Nagy, L., Rajnavolgyi, E. (2007) Differentiation of CD1a- and CD1a+ monocyte-derived dendritic cells is biased by lipid environment and PPARγ. Blood 109, 643-652.
40. Szatmari, I., Torocsik, D., Agostini, M., Nagy, T., Gurnell, M., Barta, E., Chatterjee, K., Nagy, L. (2007) PPARγ regulates the function of human dendritic cells primarily by altering lipid metabolism. Blood 110, 3271-3280.
41. Majai, G., Sarang, Z., Csomos, K., Zahuczky, G., Fesus, L. (2007) PPARγ-dependent regulation of human macrophages in phagocytosis of apoptotic cells. Eur. J. Immunol. 37, 1343-1354.
42. Szanto, A., Nagy, L. (2005) Retinoids potentiate peroxisome proliferatoractivated receptor γ action in differentiation, gene expression, and lipid metabolic processes in developing myeloid cells. Mol. Pharmacol. 67, 1935-1943.
43. Relloso, M., Puig-Kroger, A., Pello, O. M., Rodriguez-Fernandez, J. L., de la Rosa, G., Longo, N., Navarro, J., Munoz-Fernandez, M. A., Sanchez-Mateos, P., Corbi, A. L. (2002) DC-SIGN (CD209) expression is IL-4 dependent and is negatively regulated by IFN, TGF-β, and anti-inflammatory agents. J. Immunol. 168, 2634-2643.
44. Donini, M., Zenaro, E., Tamassia, N., Dusi, S. (2007) NADPH oxidase of human dendritic cells: role in Candida albicans killing and regulation by interferons, dectin-1 and CD206. Eur. J. Immunol. 37, 1194-1203.
45. Ferguson, T. A., Herndon, J., Elzey, B., Griffith, T. S., Schoenberger, S., Green, D. R. (2002) Uptake of apoptotic antigen-coupled cells by lymphoid dendritic cells and cross-priming of CD8(+) T cells produce active immune unresponsiveness. J. Immunol. 168, 5589-5595.
46. Voll, R. E., Herrmann, M., Roth, E. A., Stach, C., Kalden, J. R., Girkontaite, I. (1997) Immunosuppressive effects of apoptotic cells. Nature 390, 350-351.
47. Henson, P. M. (2005) Dampening inflammation. Nat. Immunol. 6, 1179-1181.
48. Green, D. R., Ferguson, T., Zitvogel, L., Kroemer, G. (2009) Immunogenic and tolerogenic cell death. Nat. Rev. Immunol. 9, 353-363.
49. Shortman, K., Naik, S. H. (2007) Steady-state and inflammatory dendriticcell development. Nat. Rev. Immunol. 7, 19-30.
50. Lucas, M., Stuart, L. M., Zhang, A., Hodivala-Dilke, K., Febbraio, M., Silverstein, R., Savill, J., Lacy-Hulbert, A. (2006) Requirements for apoptotic cell contact in regulation of macrophage responses. J. Immunol. 177, 4047-4054.
51. Blander, J. M., Medzhitov, R. (2006) On regulation of phagosome maturation and antigen presentation. Nat. Immunol. 7, 1029-1035.
52. Blander, J. M., Medzhitov, R. (2004) Regulation of phagosome maturation by signals from Toll-like receptors. Science 304, 1014-1018.
53. Delamarre, L., Pack, M., Chang, H., Mellman, I., Trombetta, E. S. (2005) Differential lysosomal proteolysis in antigen-presenting cells determines antigen fate. Science 307, 1630-1634.
54. Erwig, L. P., McPhilips, K. A., Wynes, M. W., Ivetic, A., Ridley, A. J., Henson, P. M. (2006) Differential regulation of phagosome maturation in macrophages and dendritic cells mediated by Rho GTPases and ezrin-radixin-moesin (ERM) proteins. Proc. Natl. Acad. Sci. USA 103, 12825-12830.
55. Daynes, R. A., Jones, D. C. (2002) Emerging roles of PPARs in inflammation and immunity. Nat. Rev. Immunol. 2, 748-759.
56. Robinson, M. J., Sancho, D., Slack, E. C., LeibundGut-Landmann, S., Reis e Sousa, C. (2006) Myeloid C-type lectins in innate immunity. Nat. Immunol. 7, 1258-1265.
57. Bergman, M. P., Engering, A., Smits, H. H., van Vliet, S. J., van Bodegraven, A. A., Wirth, H. P., Kapsenberg, M. L., Vandenbroucke-Grauls, C. M., van Kooyk, Y., Appelmelk, B. J. (2004) Helicobacter pylori modulates the T helper cell 1/T helper cell 2 balance through phase-variable interaction between lipopolysaccharide and DC-SIGN. J. Exp. Med. 200, 979-990.
58. Wang, J., Zhang, Y., Wei, J., Zhang, X., Zhang, B., Zhu, Z., Zou, W., Wang, Y., Mou, Z., Ni, B., Wu, Y. (2007) Lewis x oligosaccharides targeting to DC-SIGN enhanced antigen-specific immune response. Immunology 121, 174-182.
59. Johansson, U., Walther-Jallow, L., Smed-Sorensen, A., Spetz, A. L. (2007) Triggering of dendritic cell responses after exposure to activated, but not resting, apoptotic PBMCs. J. Immunol. 179, 1711-1720.
60. Mariathasan, S., Weiss, D. S., Newton, K., McBride, J., O'Rourke, K., Roose-Girma, M., Lee, W. P., Weinrauch, Y., Monack, D. M., Dixit, V. M. (2006) Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 440, 228-232.
61. Martinon, F., Petrilli, V., Mayor, A., Tardivel, A., Tschopp, J. (2006) Gout-associated uric acid crystals activate the NALP3 inflammasome. Nature 440, 237-241.
62. Urban, C. F., Reichard, U., Brinkmann, V., Zychlinsky, A. (2006) Neutrophil extracellular traps capture and kill Candida albicans yeast and hyphal forms. Cell. Microbiol. 8, 668-676.
63. Brinkmann, V., Reichard, U., Goosmann, C., Fauler, B., Uhlemann, Y., Weiss, D. S., Weinrauch, Y., Zychlinsky, A. (2004) Neutrophil extracellular traps kill bacteria. Science 303, 1532-1535.
64. Fuchs, T. A., Abed, U., Goosmann, C., Hurwitz, R., Schulze, I., Wahn, V., Weinrauch, Y., Brinkmann, V., Zychlinsky, A. (2007) Novel cell death program leads to neutrophil extracellular traps. J. Cell Biol. 176, 231-241.
65. Wartha, F., Beiter, K., Normark, S., Henriques-Normark, B. (2007) Neutrophil extracellular traps: casting the NET over pathogenesis. Curr. Opin. Microbiol. 10, 52-56.
66. Ravichandran, K. S. (2003) "Recruitment signals" from apoptotic cells: invitation to a quiet meal. Cell 113, 817-820.
67. Chtanova, T., Schaeffer, M., Han, S. J., van Dooren, G. G., Nollmann, M., Herzmark, P., Chan, S. W., Satija, H., Camfield, K., Aaron, H., Striepen, B., Robey, E. A. (2008) Dynamics of neutrophil migration in lymph nodes during infection. Immunity 29, 487-496.
68. Maletto, B. A., Ropolo, A. S., Alignani, D. O., Liscovsky, M. V., Ranocchia, R. P., Moron, V. G., Pistoresi-Palencia, M. C. (2006) Presence of neutrophil-bearing antigen in lymphoid organs of immune mice. Blood 108, 3094-3102.
69. Lauber, K., Bohn, E., Krober, S. M., Xiao, Y. J., Blumenthal, S. G., Lindemann, R. K., Marini, P., Wiedig, C., Zobywalski, A., Baksh, S., Xu, Y., Autenrieth, I. B., Schulze-Osthoff, K., Belka, C., Stuhler, G., Wesselborg, S. (2003) Apoptotic cells induce migration of phagocytes via caspase-3-mediated release of a lipid attraction signal. Cell 113, 717-730.
70. Stuart, L. M., Lucas, M., Simpson, C., Lamb, J., Savill, J., Lacy-Hulbert, A. (2002) Inhibitory effects of apoptotic cell ingestion upon endotoxin-driven myeloid dendritic cell maturation. J. Immunol. 168, 1627-1635.
71. Wang, Z., Larregina, A. T., Shufesky, W. J., Perone, M. J., Montecalvo, A., Zahorchak, A. F., Thomson, A. W., Morelli, A. E. (2006) Use of the inhibitory effect of apoptotic cells on dendritic cells for graft survival via T-cell deletion and regulatory T cells. Am. J. Transplant. 6, 1297-1311.
72. Ehser, S., Chuang, J. J., Kleist, C., Sandra-Petrescu, F., Iancu, M., Wang, D., Opelz, G., Terness, P. (2008) Suppressive dendritic cells as a tool for controlling allograft rejection in organ transplantation: promises and difficulties. Hum. Immunol. 69, 165-173.