β2-adrenoreceptor agonist inhibits antigen cross-presentation by dendritic cells

Journal of Immunology

Volumn 190, Issue 7, 2013, Pages 3163-3171

  Hervé, Julie ^a,b,e   Dubreil, Laurence ^b,c   Tardif, Virginie ^d   Terme, Mickael ^a,b   Pogu, Sylvie ^a,b   Anegon, Ignacio ^d   Rozec, Bertrand ^d   Gauthier, Chantal ^d   Bach, Jean Marie ^a,b   Blancou, Philippe ^a,b  

^a UNIVERSITÉ DE NANTES   (France)

^b CEMAGREF   (France)

^c La Chantrerie   (France)

^d INSERM   (France)

^e INSTITUT DE PHARMACOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BETA 2 ADRENERGIC RECEPTOR STIMULATING AGENT; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INHIBITORY GUANINE NUCLEOTIDE BINDING PROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; SALBUTAMOL; TOLL LIKE RECEPTOR 4;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; CROSS PRESENTATION; DENDRITIC CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PHAGOSOME; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PROTEIN INTERACTION;

ADRENERGIC BETA-2 RECEPTOR AGONISTS; ANIMALS; ANTIGEN PRESENTATION; CELLS, CULTURED; CROSS-PRIMING; DENDRITIC CELLS; GTP-BINDING PROTEIN ALPHA SUBUNITS, GI-GO; INTERLEUKIN-10; INTERLEUKIN-12; MICE; NF-KAPPA B; PHAGOSOMES; RECEPTORS, ADRENERGIC, BETA-2; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4;

EID: 84875450589     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1201391     Document Type: Article

References (48)

1. Loza, M. J., and R. B. Penn. 2010. Regulation of T cells in airway disease by beta-agonist. Front. Biosci. (Schol. Ed.) 2: 969-979.
2. Chamorro, A., X. Urra, and A. M. Planas. 2007. Infection after acute ischemic stroke: a manifestation of brain-induced immunodepression. Stroke 38: 1097-1103.
3. Kohm, A. P., and V. M. Sanders. 2001. Norepinephrine and β2-adrenergic receptor stimulation regulate CD4+ T and B lymphocyte function in vitro and in vivo. Pharmacol. Rev. 53: 487-525.
4. Gader, A. M., and J. D. Cash. 1975. The effect of adrenaline, noradrenaline, isoprenaline and salbutamol on the resting levels of white blood cells in man. Scand. J. Haematol. 14: 5-10.
5. Rogausch, H., A. del Rey, J. Oertel, and H. O. Besedovsky. 1999. Norepinephrine stimulates lymphoid cell mobilization from the perfused rat spleen via b-adrenergic receptors. Am. J. Physiol. 276: R724-R730.
6. Rice, P. A., G. W. Boehm, J. A. Moynihan, D. L. Bellinger, and S. Y. Stevens. 2001. Chemical sympathectomy increases the innate immune response and decreases the specific immune response in the spleen to infection with Listeria monocytogenes. J. Neuroimmunol. 114: 19-27.
7. Grebe, K. M., H. D. Hickman, K. R. Irvine, K. Takeda, J. R. Bennink, and J. W. Yewdell. 2009. Sympathetic nervous system control of anti-influenza CD8+ T cell responses. Proc. Natl. Acad. Sci. USA 106: 5300-5305.
8. Miura, T., T. Kudo, A. Matsuki, K. Sekikawa, Y. Tagawa, Y. Iwakura, and A. Nakane. 2001. Effect of 6-hydroxydopamine on host resistance against Listeria monocytogenes infection. Infect. Immun. 69: 7234-7241.
9. Cao, L., C. A. Hudson, and D. A. Lawrence. 2003. Immune changes during acute cold/restraint stress-induced inhibition of host resistance to Listeria. Toxicol. Sci. 74: 325-334.
10. Vega, J. L., H. Keino, and S. Masli. 2009. Surgical denervation of ocular sympathetic afferents decreases local transforming growth factor-beta and abolishes immune privilege. Am. J. Pathol. 175: 1218-1225.
11. Nance, D. M., and V. M. Sanders. 2007. Autonomic innervation and regulation of the immune system (1987-2007). Brain Behav. Immun. 21: 736-745.
12. Muthu, K., L. K. He, A. Szilagyi, P. Strotmon, R. L. Gamelli, and R. Shankar. 2010. β-adrenergic stimulation increases macrophage CD14 expression and E. coli phagocytosis through PKA signaling mechanisms. J. Leukoc. Biol. 88: 715-724.
13. Szelényi, J., J. P. Kiss, and E. S. Vizi. 2000. Differential involvement of sympathetic nervous system and immune system in the modulation of TNF-α production by α2- and β-adrenoceptors in mice. J. Neuroimmunol. 103: 34-40.
14. Brown, S. W., R. T. Meyers, K. M. Brennan, J. M. Rumble, N. Narasimhachari, E. F. Perozzi, J. J. Ryan, J. K. Stewart, and K. Fischer-Stenger. 2003. Catecholamines in a macrophage cell line. J. Neuroimmunol. 135: 47-55.
15. Maestroni, G. J., and P. Mazzola. 2003. Langerhans cells β2-adrenoceptors: role in migration, cytokine production, Th priming and contact hypersensitivity. J. Neuroimmunol. 144: 91-99.
16. Maestroni, G. J. 2002. Short exposure of maturing, bone marrow-derived dendritic cells to norepinephrine: impact on kinetics of cytokine production and Th development. J. Neuroimmunol. 129: 106-114.
17. Maestroni, G. J. 2000. Dendritic cell migration controlled by α1b-adrenergic receptors. J. Immunol. 165: 6743-6747.
18. Yanagawa, Y., M. Matsumoto, and H. Togashi. 2010. Enhanced dendritic cell antigen uptake via a2 adrenoceptor-mediated PI3K activation following brief exposure to noradrenaline. J. Immunol. 185: 5762-5768.
19. Wang, Z. Y., D. Yang, Q. Chen, C. A. Leifer, D. M. Segal, S. B. Su, R. R. Caspi, Z. O. Howard, and J. J. Oppenheim. 2006. Induction of dendritic cell maturation by pertussis toxin and its B subunit differentially initiate Toll-like receptor 4-dependent signal transduction pathways. Exp. Hematol. 34: 1115-1124.
20. Maderna, P., D. C. Cottell, G. Berlasconi, N. A. Petasis, H. R. Brady, and C. Godson. 2002. Lipoxins induce actin reorganization in monocytes and macrophages but not in neutrophils: differential involvement of rho GTPases. Am. J. Pathol. 160: 2275-2283.
21. Bengoechea-Alonso, M. T., B. Pelacho, J. A. Osés-Prieto, E. Santiago, N. López- Moratalla, and M. J. López-Zabalza. 2003. Regulation of NF-κB activation by protein phosphatase 2B and NO, via protein kinase A activity, in human monocytes. Nitric Oxide 8: 65-74.
22. Goyarts, E., M. Matsui, T. Mammone, A. M. Bender, J. A.Wagner, D. Maes, and R. D. Granstein. 2008. Norepinephrine modulates human dendritic cell activation by altering cytokine release. Exp. Dermatol. 17: 188-196.
23. Kockx, M., D. L. Guo, T. Huby, P. Lesnik, J. Kay, T. Sabaretnam, E. Jary, M. Hill, K. Gaus, J. Chapman, et al. 2007. Secretion of apolipoprotein E from macrophages occurs via a protein kinase A and calcium-dependent pathway along the microtubule network. Circ. Res. 101: 607-616.
24. Chruscinski, A. J., D. K. Rohrer, E. Schauble, K. H. Desai, D. Bernstein, and B. K. Kobilka. 1999. Targeted disruption of the β2 adrenergic receptor gene. J. Biol. Chem. 274: 16694-16700.
25. Rémy, S., P. Blancou, L. Tesson, V. Tardif, R. Brion, P. J. Royer, R. Motterlini, R. Foresti, M. Painchaut, S. Pogu, et al. 2009. Carbon monoxide inhibits TLRinduced dendritic cell immunogenicity. J. Immunol. 182: 1877-1884.
26. Savina, A., P. Vargas, P. Guermonprez, A. M. Lennon, and S. Amigorena. 2010. Measuring pH, ROS production, maturation, and degradation in dendritic cell phagosomes using cytofluorometry-based assays.Methods Mol. Biol. 595: 383-402.
27. Burgdorf, S., A. Kautz, V. Böhnert, P. A. Knolle, and C. Kurts. 2007. Distinct pathways of antigen uptake and intracellular routing in CD4 and CD8 T cell activation. Science 316: 612-616.
28. Ewins, B. A., M. Vassiliadou, A. M. Minihane, G. H. Rimbach, and P. D. Weinberg. 2006. Techniques for quantifying effects of dietary antioxidants on transcription factor translocation and nitric oxide production in cultured cells. Genes Nutr. 1: 125-131.
29. Benke, D., T. Krüger, A. Lang, E. E. Hamilton-Williams, and C. Kurts. 2006. Inclusion of brefeldin A during dendritic cell isolation allows in vitro detection of cross-presented self-antigens. J. Immunol. Methods 310: 12-19.
30. Amigorena, S., and A. Savina. 2010. Intracellular mechanisms of antigen cross presentation in dendritic cells. Curr. Opin. Immunol. 22: 109-117.
31. Karttunen, J., S. Sanderson, and N. Shastri. 1992. Detection of rare antigenpresenting cells by the lacZ T-cell activation assay suggests an expression cloning strategy for T-cell antigens. Proc. Natl. Acad. Sci. USA 89: 6020-6024.
32. Johnson, M. 2006. Molecular mechanisms of β2-adrenergic receptor function, response, and regulation. J. Allergy Clin. Immunol. 117: 18-24.
33. Lefkowitz, R. J., K. L. Pierce, and L. M. Luttrell. 2002. Dancing with different partners: protein kinase a phosphorylation of seven membrane-spanning receptors regulates their G protein-coupling specificity. Mol. Pharmacol. 62: 971-974.
34. Daaka, Y., L. M. Luttrell, and R. J. Lefkowitz. 1997. Switching of the coupling of the β2-adrenergic receptor to different G proteins by protein kinase A. Nature 390: 88-91.
35. Yoshimura, S., J. Bondeson, B. M. Foxwell, F. M. Brennan, and M. Feldmann. 2001. Effective antigen presentation by dendritic cells is NF-κB dependent: coordinate regulation of MHC, co-stimulatory molecules and cytokines. Int. Immunol. 13: 675-683.
36. Panina-Bordignon, P., D. Mazzeo, P. D. Lucia, D. D'Ambrosio, R. Lang, L. Fabbri, C. Self, and F. Sinigaglia. 1997. β2-agonists prevent Th1 development by selective inhibition of interleukin 12. J. Clin. Invest. 100: 1513-1519.
37. Farmer, P., and J. Pugin. 2000. β-adrenergic agonists exert their "anti-inflammatory" effects in monocytic cells through the IκB/NF-κB pathway. Am. J. Physiol. Lung Cell. Mol. Physiol. 279: L675-L682.
38. Loop, T., T. Bross, M. Humar, A. Hoetzel, R. Schmidt, H. L. Pahl, K. K. Geiger, and B. H. Pannen. 2004. Dobutamine inhibits phorbol-myristate-acetate- induced activation of nuclear factor-κB in human T lymphocytes in vitro. Anesth. Analg. 99: 1508-1515.
39. Kizaki, T., T. Izawa, T. Sakurai, S. Haga, N. Taniguchi, H. Tajiri, K. Watanabe, N. K. Day, K. Toba, and H. Ohno. 2008. β2-adrenergic receptor regulates Tolllike receptor-4-induced nuclear factor-κB activation through beta-arrestin 2. Immunology 124: 348-356.
40. Howland, S. W., and K. D. Wittrup. 2008. Antigen release kinetics in the phagosome are critical to cross-presentation efficiency. J. Immunol. 180: 1576-1583.
41. Savina, A., C. Jancic, S. Hugues, P. Guermonprez, P. Vargas, I. C. Moura, A. M. Lennon-Duménil, M. C. Seabra, G. Raposo, and S. Amigorena. 2006. NOX2 controls phagosomal pH to regulate antigen processing during crosspresentation by dendritic cells. Cell 126: 205-218.
42. Trombetta, E. S., M. Ebersold, W. Garrett, M. Pypaert, and I. Mellman. 2003. Activation of lysosomal function during dendritic cell maturation. Science 299: 1400-1403.
43. Blander, J. M., and R. Medzhitov. 2006. On regulation of phagosome maturation and antigen presentation. Nat. Immunol. 7: 1029-1035.
44. Irwin, M. R., and S. W. Cole. 2011. Reciprocal regulation of the neural and innate immune systems. Nat. Rev. Immunol. 11: 625-632.
45. Dobbs, C. M., M. Vasquez, R. Glaser, and J. F. Sheridan. 1993. Mechanisms of stress-induced modulation of viral pathogenesis and immunity. J. Neuroimmunol. 48: 151-160.
46. Sheridan, J. F., C. Dobbs, J. Jung, X. Chu, A. Konstantinos, D. Padgett, and R. Glaser. 1998. Stress-induced neuroendocrine modulation of viral pathogenesis and immunity. Ann. N. Y. Acad. Sci. 840: 803-808.
47. Elftman, M. D., C. C. Norbury, R. H. Bonneau, and M. E. Truckenmiller. 2007. Corticosterone impairs dendritic cell maturation and function. Immunology 122: 279-290.
48. Hunzeker, J. T., M. D. Elftman, J. C. Mellinger, M. F. Princiotta, R. H. Bonneau, M. E. Truckenmiller, and C. C. Norbury. 2011. A marked reduction in priming of cytotoxic CD8+ T cells mediated by stress-induced glucocorticoids involves multiple deficiencies in cross-presentation by dendritic cells. J. Immunol. 186: 183-194.