Chronic hypoxia reprograms human immature dendritic cells by inducing a proinflammatory phenotype and TREM-1 expression

European Journal of Immunology

Volumn 43, Issue 4, 2013, Pages 949-966

  Pierobon, Daniele ^a,b   Bosco, Maria Carla ^c   Blengio, Fabiola ^c   Raggi, Federica ^c   Eva, Alessandra ^c   Filippi, Miriam ^a,b   Musso, Tiziana ^a   Novelli, Francesco ^a,b   Cappello, Paola ^a,b   Varesio, Luigi ^c   Giovarelli, Mirella ^a,b  

^a UNIVERSITY OF TURIN   (Italy)

^b Center for Experimental Research and Medical Studies CERMS   (Italy)

^c G GASLINI INSTITUTE   (Italy)

Author keywords

Dendritic cells; Hypoxia; Immunoregulatory receptors; Innate immunity; Proinflammatory cytokines chemokines

Indexed keywords

INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 8; PATTERN RECOGNITION RECEPTOR; RANTES; THYMUS AND ACTIVATION REGULATED CHEMOKINE; TRIGGERING RECEPTOR EXPRESSED ON MYELOID CELLS 1; TUMOR NECROSIS FACTOR ALPHA;

ANTIGEN PRESENTATION; ARTICLE; BONE MARROW CELL; CELL ACTIVATION; CELL MATURATION; CELL TRANSPORT; CELLULAR IMMUNITY; CHRONIC HYPOXIA; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DOWN REGULATION; GENE CLUSTER; GENE EXPRESSION; HUMAN; HUMAN CELL; HYPOXIA; IMMUNOREGULATION; INFLAMMATION; MOLECULAR MECHANICS; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REOXYGENATION; TH1 CELL; TH17 CELL; UNINDEXED SEQUENCE; UPREGULATION;

CELL HYPOXIA; CELLS, CULTURED; CYTOKINES; DENDRITIC CELLS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; HUMANS; INFLAMMATION MEDIATORS; MEMBRANE GLYCOPROTEINS; PHENOTYPE; RECEPTORS, IMMUNOLOGIC; TH1 CELLS; TH17 CELLS;

EID: 84876442403     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201242709     Document Type: Article

References (61)

1. Rossi, M. and Young, J. W., Human dendritic cells: potent antigen-presenting cells at the crossroads of innate and adaptive immunity. J. Immunol. 2005. 175: 1373-1381.
2. Bobryshev, Y. V., Dendritic cells and their role in atherogenesis. Lab. Invest. 2010. 90: 970-984.
3. Granucci, F., Zanoni, I. and Ricciardi-Castagnoli, P., Central role of dendritic cells in the regulation and deregulation of immune responses. Cell. Mol. Life Sci. 2008. 65: 1683-1697.
4. Shortman, K. and Naik, S. H., Steady-state and inflammatory dendritic-cell development. Nat. Rev. Immunol. 2007. 7: 19-30.
5. Ueno, H., Klechevsky, E., Morita, R., Aspord, C., Cao, T., Matsui, T., Di Pucchio, T. et al., Dendritic cell subsets in health and disease. Immunol. Rev. 2007. 219: 118-142.
6. Mellman, I. and Steinman, R. M., Dendritic cells: specialized and regulated antigen processing machines. Cell 2001. 106: 255-258.
7. Cavanagh, L. L. and Von Andrian, U. H., Travellers in many guises: the origins and destinations of dendritic cells. Immunol. Cell Biol. 2002. 80: 448-462.
8. Sozzani, S., Dendritic cell trafficking: more than just chemokines. Cytokine Growth Factor Rev. 2005. 16: 581-592.
9. Lin, A., Schildknecht, A., Nguyen, L. T. and Ohashi, P. S., Dendritic cells integrate signals from the tumor microenvironment to modulate immunity and tumor growth. Immunol. Lett. 2010. 127: 77-84.
10. Rama, I., Bruene, B., Torras, J., Koehl, R., Cruzado, J. M., Bestard, O., Franquesa, M. et al., Hypoxia stimulus: an adaptive immune response during dendritic cell maturation. Kidney Int. 2008. 73: 816-825.
11. Bosco, M. C., Puppo, M., Blengio, F., Fraone, T., Cappello, P., Giovarelli, M. and Varesio, L., Monocytes and dendritic cells in a hypoxic environment: spotlights on chemotaxis and migration. Immunobiology 2008. 213: 733-749.
12. de Jong, E. C., Smits, H. H. and Kapsenberg, M. L., Dendritic cell-mediated T cell polarization. Springer Semin. Immunopathol. 2005. 26: 289-307.
13. Lanzavecchia, A. and Sallusto, F., Regulation of T cell immunity by dendritic cells. Cell 2001. 106: 263-266.
14. Forster, R., Davalos-Misslitz, A. C. and Rot, A., CCR7 and its ligands: balancing immunity and tolerance. Nat. Rev. Immunol. 2008. 8: 362-371.
15. Semenza, G. L., Hypoxia-inducible factor 1: oxygen homeostasis and disease pathophysiology. Trends Mol. Med. 2001. 7: 345-350.
16. Muz, B., Khan, M. N., Kiriakidis, S. and Paleolog, E. M., Hypoxia. The role of hypoxia and HIF-dependent signalling events in rheumatoid arthritis. Arthritis Res. Ther. 2009. 11: 201.
17. Wenger, R. H., Stiehl, D. P. and Camenisch, G., Integration of oxygen signaling at the consensus HRE. Sci. STKE 2005. 306: re12.
18. Yang, M., Ma, C., Liu, S., Sun, J., Shao, Q., Gao, W., Zhang, Y. et al., Hypoxia skews dendritic cells to a T helper type 2-stimulating phenotype and promotes tumour cell migration by dendritic cell-derived osteopontin. Immunology 2009. 128: e237-249.
19. Ricciardi, A., Elia, A. R., Cappello, P., Puppo, M., Vanni, C., Fardin, P., Eva, A. et al., Transcriptome of hypoxic immature dendritic cells: modulation of chemokine/receptor expression. Mol. Cancer Res. 2008. 6: 175-185.
20. Elia, A. R., Cappello, P., Puppo, M., Fraone, T., Vanni, C., Eva, A., Musso, T. et al., Human dendritic cells differentiated in hypoxia down-modulate antigen uptake and change their chemokine expression profile. J. Leukoc. Biol. 2008. 84: 1472-1482.
21. Jantsch, J., Chakravortty, D., Turza, N., Prechtel, A. T., Buchholz, B., Gerlach, R. G., Volke, M. et al., Hypoxia and hypoxia-inducible factor-1 alpha modulate lipopolysaccharide-induced dendritic cell activation and function. J. Immunol. 2008. 180: 4697-4705.
22. Mancino, A., Schioppa, T., Larghi, P., Pasqualini, F., Nebuloni, M., Chen, I. H., Sozzani, S. et al., Divergent effects of hypoxia on dendritic cell functions. Blood 2008. 112: 3723-3734.
23. Bosco, M. C., Pierobon, D., Blengio, F., Raggi, F., Vanni, C., Gattorno, M., Eva, A. et al., Hypoxia modulates the gene expression profile of immunoregulatory receptors in human mature dendritic cells: identification of TREM-1 as a novel hypoxic marker in vitro and in vivo. Blood 2011. 117: 2625-2639.
24. Blengio, F., Raggi, F., Pierobon, D., Cappello, P., Eva, A., Giovarelli, M., Varesio, L. and Bosco, M. C., The hypoxic environment reprograms the cytokine/chemokine expression profile of human mature dendritic cells. Immunobiology 2013. 218: 76-89.
25. Schakel, K., Dendritic cells-why can they help and hurt us. Exp. Dermatol. 2009. 18: 264-273.
26. Colonna, M., Nakajima, H. and Cella, M., A family of inhibitory and activating Ig-like receptors that modulate function of lymphoid and myeloid cells. Semin. Immunol. 2000. 12: 121-127.
27. Joffre, O., Nolte, M. A., Sporri, R. and Reis e Sousa, C., Inflammatory signals in dendritic cell activation and the induction of adaptive immunity. Immunol. Rev. 2009. 227: 234-247.
28. Klesney-Tait, J., Turnbull, I. R. and Colonna, M., The TREM receptor family and signal integration. Nat. Immunol. 2006. 7: 1266-1273.
29. Sharif, O. and Knapp, S., From expression to signaling: roles of TREM-1 and TREM-2 in innate immunity and bacterial infection. Immunobiology 2008. 213: 701-713.
30. Bouchon, A., Dietrich, J. and Colonna, M., Cutting edge: inflammatory responses can be triggered by TREM-1, a novel receptor expressed on neutrophils and monocytes. J. Immunol. 2000. 164: 4991-4995.
31. Unternaehrer, J. J., Chow, A., Pypaert, M., Inaba, K. and Mellman, I., The tetraspanin CD9 mediates lateral association of MHC class II molecules on the dendritic cell surface. Proc. Natl. Acad. Sci. USA 2007. 104: 234-239.
32. Sheng, K. C., van Spriel, A. B., Gartlan, K. H., Sofi, M., Apostolopoulos, V., Ashman, L. and Wright, M. D., Tetraspanin CD37 and CD151 differentially regulate Ag presentation and T-cell co-stimulation by DC. Eur. J. Immunol. 2009. 39: 50-55.
33. Gerber, J. S. and Mosser, D. M., Stimulatory and inhibitory signals originating from the macrophage Fcgamma receptors. Microbes. Infect. 2001. 3: 131-139.
34. Kawai, T. and Akira, S., Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 2011. 34: 637-650.
35. Chabowski, A., Gorski, J., Calles-Escandon, J., Tandon, N. N. and Bonen, A., Hypoxia-induced fatty acid transporter translocation increases fatty acid transport and contributes to lipid accumulation in the heart. FEBS Lett. 2006. 580: 3617-3623.
36. Bosco, M. C., Puppo, M., Santangelo, C., Anfosso, L., Pfeffer, U., Fardin, P., Battaglia, F. and Varesio, L., Hypoxia modifies the transcriptome of primary human monocytes: modulation of novel immune-related genes and identification of CC-chemokine ligand 20 as a new hypoxia-inducible gene. J. Immunol. 2006. 177: 1941-1955.
37. Gibot, S., Kolopp-Sarda, M. N., Bene, M. C., Bollaert, P. E., Lozniewski, A., Mory, F., Levy, B. and Faure, G. C., A soluble form of the triggering receptor expressed on myeloid cells-1 modulates the inflammatory response in murine sepsis. J. Exp. Med. 2004. 200: 1419-1426.
38. Ogino, T., Onishi, H., Suzuki, H., Morisaki, T., Tanaka, M. and Katano, M., Inclusive estimation of complex antigen presentation functions of monocyte-derived dendritic cells differentiated under normoxia and hypoxia conditions. Cancer Immunol. Immunother. 2011. 61: 409-424.
39. Kong, D., Park, E. J., Stephen, A. G., Calvani, M., Cardellina, J. H., Monks, A., Fisher, R. J. et al., Echinomycin, a small-molecule inhibitor of hypoxia-inducible factor-1 DNA-binding activity. Cancer Res. 2005. 65: 9047-9055.
40. Lebre, M. C. and Tak, P. P., Dendritic cell subsets: their roles in rheumatoid arthritis. Acta Reumatol. Port. 2008. 33: 35-45.
41. Moestrup, S. K. and Moller, H. J., CD163: a regulated hemoglobin scavenger receptor with a role in the anti-inflammatory response. Ann. Med. 2004. 36: 347-354.
42. Takamatsu, H., Okuno, T. and Kumanogoh, A., Regulation of immune cell responses by semaphorins and their receptors. Cell. Mol. Immunol. 2010. 7: 83-88.
43. Crocker, P. R., McMillan, S. J. and Richards, H. E., CD33-related siglecs as potential modulators of inflammatory responses. Ann. NY Acad. Sci. 2012. 1: 102-111.
44. Cavaillon, J. M., Monocyte TREM-1 membrane expression in non-infectious inflammation. Crit. Care 2009. 13: 152.
45. Bosco, M. C. and Varesio, L., Dendritic cell reprogramming by the hypoxic environment. Immunobiology 2012. 217: 1241-1249.
46. Prechtel, A. T., Turza, N. M., Theodoridis, A. A. and Steinkasserer, A., CD83 knockdown in monocyte-derived dendritic cells by small interfering RNA leads to a diminished T cell stimulation. J. Immunol. 2007. 178: 5454-5464.
47. Xu, G., Nie, H., Li, N., Zheng, W., Zhang, D., Feng, G., Ni, L. et al., Role of osteopontin in amplification and perpetuation of rheumatoid synovitis. J. Clin. Invest. 2005. 115: 1060-1067.
48. Scatena, M., Liaw, L. and Giachelli, C. M., Osteopontin: a multifunctional molecule regulating chronic inflammation and vascular disease. Arterioscler. Thromb. Vasc. Biol. 2007. 27: 2302-2309.
49. Baggiolini, M. and Loetscher, P., Chemokines in inflammation and immunity. Immunol. Today 2000. 21: 418-420.
50. Dinarello, C. A., Interleukin-1 in the pathogenesis and treatment of inflammatory diseases. Blood 2011. 117: 3720-3732.
51. Bosco, M. and Varesio, L., Monocytic cell gene regulation by the hypoxic environment in Juvenile Idiopathic Arthritis: implications for disease pathogenesis. Rheumatol. Musculoskelet. Med. 2010. 1: 47-55.
52. Kuai, J., Gregory, B., Hill, A., Pittman, D. D., Feldman, J. L., Brown, T., Carito, B. et al., TREM-1 expression is increased in the synovium of rheumatoid arthritis patients and induces the expression of pro-inflammatory cytokines. Rheumatology 2009. 48: 1352-1358.
53. Xu, M., Mizoguchi, I., Morishima, N., Chiba, Y., Mizuguchi, J. and Yoshimoto, T., Regulation of antitumor immune responses by the IL-12 family cytokines, IL-12, IL-23, and IL-27. Clin. Dev. Immunol. 2010. 2010: 9.
54. Wedderburn, L. R., Robinson, N., Patel, A., Varsani, H. and Woo, P., Selective recruitment of polarized T cells expressing CCR5 and CXCR3 to the inflamed joints of children with juvenile idiopathic arthritis. Arthritis Rheum. 2000. 43: 765-774.
55. Weber, C., Meiler, S., Doring, Y., Koch, M., Drechsler, M., Megens, R. T., Rowinska, Z. et al., CCL17-expressing dendritic cells drive atherosclerosis by restraining regulatory T cell homeostasis in mice. J. Clin. Invest. 2011. 121: 2898-2910.
56. Heiseke, A. F., Faul, A. C., Lehr, H. A., Forster, I., Schmid, R. M., Krug, A. B. and Reindl, W., CCL17 promotes intestinal inflammation in mice and counteracts regulatory T cell-mediated protection from colitis. Gastroenterology 2012. 142: 335-345.
57. Radstake, T. R., van der Voort, R., ten Brummelhuis, M., de Waal Malefijt, M., Looman, M., Figdor, C. G., van den Berg W. B. et al., Increased expression of CCL18, CCL19, and CCL17 by dendritic cells from patients with rheumatoid arthritis, and regulation by Fc gamma receptors. Ann. Rheum. Dis. 2005. 64: 359-367.
58. El Mezayen, R., El Gazzar, M., Seeds, M. C., McCall, C. E., Dreskin, S. C. and Nicolls, M. R., Endogenous signals released from necrotic cells augment inflammatory responses to bacterial endotoxin. Immunol. Lett. 2007. 111: 36-44.
59. Colonna, M. and Facchetti, F., TREM-1 (triggering receptor expressed on myeloid cells): a new player in acute inflammatory responses. J. Infect. Dis. 2003. 187(Suppl 2): S397-401.
60. Foell, D., Wittkowski, H. and Roth, J., Mechanisms of disease: a 'DAMP' view of inflammatory arthritis. Nat. Clin. Pract. Rheumatol. 2007. 3: 382-390.
61. Wu, J., Li, J., Salcedo, R., Mivechi, N. F., Trinchieri, G. and Horuzsko, A., The proinflammatory myeloid cell receptor TREM-1 controls Kupffer cell activation and development of hepatocellular carcinoma. Cancer Res. 2012. 72: 3977-3986.