Histamine regulates autoreactive T cell activation and adhesiveness in inflamed brain microcirculation

Journal of Leukocyte Biology

Volumn 89, Issue 2, 2011, Pages 259-267

  Lapilla, Marilena ^a   Gallo, Barbara ^a   Martinello, Marianna ^b   Procaccini, Claudio ^c   Costanza, Massimo ^a   Musio, Silvia ^a   Rossi, Barbara ^b   Angiari, Stefano ^b   Farina, Cinthia ^a   Steinman, Lawrence ^d   Matarese, Giuseppe ^c   Constantin, Gabriela ^b   Pedotti, Rosetta ^a  

^a DEPARTMENT OF NEUROSURGERY   (Italy)

^b UNIVERSITY OF VERONA   (Italy)

^c CNR   (Italy)

^d STANFORD UNIVERSITY   (United States)

Author keywords

Autoimmunity; Chemokine; Cytokine; EAE; MS

Indexed keywords

CHEMOKINE; CYCLIN DEPENDENT KINASE INHIBITOR 1B; DIMAPRIT; GAMMA INTERFERON; HISTAMINE; HISTAMINE AGONIST; HISTAMINE H1 RECEPTOR; HISTAMINE H1 RECEPTOR AGONIST; HISTAMINE H2 RECEPTOR; HISTAMINE H2 RECEPTOR AGONIST; HISTAMINERGIC RECEPTOR AFFECTING AGENT; INTERCELLULAR ADHESION MOLECULE 1; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MYELIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOIMMUNE DISEASE; BRAIN MICROCIRCULATION; CELL ADHESION; CELL MIGRATION; CONTROLLED STUDY; ENCEPHALITIS; ENZYME ACTIVATION; FEMALE; FLOW CYTOMETRY; HISTOPATHOLOGY; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE PROLIFERATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; T LYMPHOCYTE ACTIVATION;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN; CELL ADHESION; CELL PROLIFERATION; CELLS, CULTURED; CHEMOTAXIS, LEUKOCYTE; FEMALE; HISTAMINE; HISTAMINE AGONISTS; INFLAMMATION MEDIATORS; LYMPHOCYTE ACTIVATION; MICE; MICROCIRCULATION; RECEPTORS, HISTAMINE; SIGNAL TRANSDUCTION; T-LYMPHOCYTE SUBSETS;

ANIMALIA;

EID: 79951839901     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0910486     Document Type: Article

References (52)

1. Dy, M., Schneider, E. (2004) Histamine-cytokine connection in immunity and hematopoiesis. Cytokine Growth Factor Rev. 15, 393-410. (Pubitemid 39140701)
2. Jutel, M., Watanabe, T., Akdis, M., Blaser, K., Akdis, C. A. (2002) Immune regulation by histamine. Curr. Opin. Immunol. 14, 735-740.
3. Pedotti, R., Steinman, L. (2005) Histamine in immune regulation: possible roles in autoimmune demyelinating disease of the central nervous system. Curr. Med. Chem. Anti-Inflammatory and Anti-Allergy Agents 4, 637-643. (Pubitemid 41722368)
4. Elenkov, I. J., Webster, E., Papanicolaou, D. A., Fleisher, T. A., Chrousos, G. P., Wilder, R. L. (1998) Histamine potently suppresses human IL-12 and stimulates IL-10 production via H2 receptors. J. Immunol. 161, 2586-2593. (Pubitemid 28397078)
5. Van der Pouw Kraan, T. C., Snijders, A., Boeije, L. C., de Groot, E. R., Alewijnse, A. E., Leurs, R., Aarden, L. A. (1998) Histamine inhibits the production of interleukin-12 through interaction with H2 receptors. J. Clin. Invest. 102, 1866-1873. (Pubitemid 28533834)
6. Idzko, M., la Sala, A., Ferrari, D., Panther, E., Herouy, Y., Dichmann, S., Mockenhaupt, M., Di Virgilio, F., Girolomoni, G., Norgauer, J. (2002) Expression and function of histamine receptors in human monocyte-derived dendritic cells. J. Allergy Clin. Immunol. 109, 839-846. (Pubitemid 34499519)
7. Caron, G., Delneste, Y., Roelandts, E., Duez, C., Bonnefoy, J. Y., Pestel, J., Jeannin, P. (2001) Histamine polarizes human dendritic cells into Th2 cell-promoting effector dendritic cells. J. Immunol. 167, 3682-3686. (Pubitemid 32910811)
8. Mazzoni, A., Young, H. A., Spitzer, J. H., Visintin, A., Segal, D. M. (2001) Histamine regulates cytokine production in maturing dendritic cells, resulting in altered T cell polarization. J. Clin. Invest. 108, 1865-1873. (Pubitemid 34015132)
9. Vannier, E., Miller, L. C., Dinarello, C. A. (1991) Histamine suppresses gene expression and synthesis of tumor necrosis factor α via histamine H2 receptors. J. Exp. Med. 174, 281-284.
10. Osna, N., Elliott, K., Khan, M. M. (2001) The effects of histamine on interferon γ production are dependent on the stimulatory signals. Int. Immunopharmacol. 1, 135-145. (Pubitemid 32193608)
11. Banu, Y., Watanabe, T. (1999) Augmentation of antigen receptor-mediated responses by histamine H1 receptor signaling. J. Exp. Med. 189, 673-682. (Pubitemid 29193368)
12. Jutel, M., Watanabe, T., Klunker, S., Akdis, M., Thomet, O. A., Malolepszy, J., Zak-Nejmark, T., Koga, R., Kobayashi, T., Blaser, K., Akdis, C. A. (2001) Histamine regulates T-cell and antibody responses by differential expression of H1 and H2 receptors. Nature 413, 420-425. (Pubitemid 32928596)
13. Ma, R. Z., Gao, J., Meeker, N. D., Fillmore, P. D., Tung, K. S., Watanabe, T., Zachary, J. F., Offner, H., Blankenhorn, E. P., Teuscher, C. (2002) Identification of Bphs, an autoimmune disease locus, as histamine receptor H1. Science 297, 620-623. (Pubitemid 34815349)
14. Park, H., Li, Z., Yang, X. O., Chang, S. H., Nurieva, R., Wang, Y. H., Wang, Y., Hood, L., Zhu, Z., Tian, Q., Dong, C. (2005) A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat. Immunol. 6, 1133-1141. (Pubitemid 41541791)
15. Steinman, L. (2008) A rush to judgment on Th17. J. Exp. Med. 205, 1517-1522.
16. Pedotti, R., De Voss, J. J., Steinman, L., Galli, S. J. (2003) Involvement of both "allergic" and "autoimmune" mechanisms in EAE, MS and other autoimmune diseases. Trends Immunol. 24, 479-484. (Pubitemid 37088150)
17. Pedotti, R., DeVoss, J. J., Youssef, S., Mitchell, D., Wedemeyer, J., Madanat, R., Garren, H., Fontoura, P., Tsai, M., Galli, S. J., Sobel, R. A., Steinman, L. (2003) Multiple elements of the allergic arm of the immune response modulate autoimmune demyelination. Proc. Natl. Acad. Sci. USA 100, 1867-1872. (Pubitemid 36254540)
18. Noubade, R., Milligan, G., Zachary, J. F., Blankenhorn, E. P., del Rio, R., Rincon, M., Teuscher, C. (2007) Histamine receptor H1 is required for TCR-mediated p38 MAPK activation and optimal IFN-γ production in mice. J. Clin. Invest. 117, 3507-3518. (Pubitemid 350097006)
19. Noubade, R., Saligrama, N., Spach, K., Del Rio, R., Blankenhorn, E. P., Kantidakis, T., Milligan, G., Rincon, M., Teuscher, C. (2008) Autoimmune disease-associated histamine receptor H1 alleles exhibit differential protein trafficking and cell surface expression. J. Immunol. 180, 7471-7479.
20. El Behi, M., Zephir, H., Lefranc, D., Dutoit, V., Dussart, P., Devos, P., Dessaint, J. P., Vermersch, P., Prin, L. (2007) Changes in self-reactive IgG antibody repertoire after treatment of experimental autoimmune encephalomyelitis with anti-allergic drugs. J. Neuroimmunol. 182, 80-88. (Pubitemid 46039760)
21. Dimitriadou, V., Pang, X., Theoharides, T. C. (2000) Hydroxyzine inhibits experimental allergic encephalomyelitis (EAE) and associated brain mast cell activation. Int. J. Immunopharmacol. 22, 673-684. (Pubitemid 30407021)
22. Musio, S., Gallo, B., Scabeni, S., Lapilla, M., Poliani, P. L., Matarese, G., Ohtsu, H., Galli, S. J., Mantegazza, R., Steinman, L., Pedotti, R. (2006) A key regulatory role for histamine in experimental autoimmune encephalomyelitis: disease exacerbation in histidine decarboxylase-deficient mice. J. Immunol. 176, 17-26. (Pubitemid 43023244)
23. Emerson, M. R., Orentas, D. M., Lynch, S. G., LeVine, S. M. (2002) Activation of histamine H2 receptors ameliorates experimental allergic encephalomyelitis. Neuroreport 13, 1407-1410.
24. Pedotti, R., Mitchell, D., Wedemeyer, J., Karpuj, M., Chabas, D., Hattab, E. M., Tsai, M., Galli, S. J., Steinman, L. (2001) An unexpected version of horror autotoxicus: anaphylactic shock to a self-peptide. Nat. Immunol. 2, 216-222. (Pubitemid 33705997)
25. Scabeni, S., Lapilla, M., Musio, S., Gallo, B., Ciusani, E., Steinman, L., Mantegazza, R., Pedotti, R. (2008) CD4+CD25+ regulatory T cells specific for a thymus-expressed antigen prevent the development of anaphylaxis to self. J. Immunol. 180, 4433-4440.
26. De Rosa, V., Procaccini, C., Cali, G., Pirozzi, G., Fontana, S., Zappacosta, S., La Cava, A., Matarese, G. (2007) A key role of leptin in the control of regulatory T cell proliferation. Immunity 26, 241-255. (Pubitemid 46329441)
27. Constantin, G., Laudanna, C., Brocke, S., Butcher, E. C. (1999) Inhibition of experimental autoimmune encephalomyelitis by a tyrosine kinase inhibitor. J. Immunol. 162, 1144-1149. (Pubitemid 29035446)
28. Laudanna, C., Campbell, J. J., Butcher, E. C. (1996) Role of Rho in chemoattractant-activated leukocyte adhesion through integrins. Science 271, 981-983. (Pubitemid 26066394)
29. Piccio, L., Rossi, B., Scarpini, E., Laudanna, C., Giagulli, C., Issekutz, A. C., Vestweber, D., Butcher, E. C., Constantin, G. (2002) Molecular mechanisms involved in lymphocyte recruitment in inflamed brain microvessels: critical roles for P-selectin glycoprotein ligand-1 and heterotrimeric G(i)-linked receptors. J. Immunol. 168, 1940-1949. (Pubitemid 34135797)
30. George, T. C., Fanning, S. L., Fitzgeral-Bocarsly, P., Medeiros, R. B., Highfill, S., Shimizu, Y., Hall, B. E., Frost, K., Basiji, D., Ortyn, W. E., Morrissey, P. J., Lynch, D. H. (2006) Quantitative measurement of nuclear translocation events using similarity analysis of multispectral cellular images obtained in flow. J. Immunol. Methods 311, 117-129.
31. Constantin, G., Marconi, S., Rossi, B., Angiari, S., Calderan, L., Anghileri, E., Gini, B., Dorothea Bach, S., Martinello, M., Bifari, F., Galiè, M., Turano, E., Budui, S., Sbarbati, A., Krampera, M., Bonetti, B. (2009) Adipose-derived mesenchymal stem cells ameliorate chronic experimental autoimmune encephalomyelitis. Stem Cells 27, 2624-2635.
32. Boussiotis, V. A., Freeman, G. J., Taylor, P. A., Berezovskaya, A., Grass, I., Blazar, B. R., Nadler, L. M. (2000) p27Kip1 functions as an anergy factor inhibiting interleukin 2 transcription and clonal expansion of alloreactive human and mouse helper T lymphocytes. Nat. Med. 6, 290-297. (Pubitemid 30148621)
33. Wells, A. D., Walsh, M. C., Bluestone, J. A., Turka, L. A. (2001) Signaling through CD28 and CTLA-4 controls two distinct forms of T cell anergy. J. Clin. Invest. 108, 895-903.
34. Baron, J. L., Madri, J. A., Ruddle, N. H., Hashim, G., Janeway Jr., C. A. (1993) Surface expression of α 4 integrin by CD4 T cells is required for their entry into brain parenchyma. J. Exp. Med. 177, 57-68.
35. Constantin, G., Majeed, M., Giagulli, C., Piccio, L., Kim, J. Y., Butcher, E. C., Laudanna, C. (2000) Chemokines trigger immediate β2 integrin affinity and mobility changes: differential regulation and roles in lymphocyte arrest under flow. Immunity 13, 759-769. (Pubitemid 32041799)
36. Ley, K., Laudanna, C., Cybulsky, M. I., Nourshargh, S. (2007) Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat. Rev. Immunol. 7, 678-689. (Pubitemid 47327397)
37. Sonobe, Y., Nakane, H., Watanabe, T., Nakano, K. (2004) Regulation of Con A-dependent cytokine production from CD4+ and CD8+ T lymphocytes by autosecretion of histamine. Inflamm. Res. 53, 87-92. (Pubitemid 38372943)
38. Saito, H., Shimizu, H., Mita, H., Maeda, Y., Akiyama, K. (1996) Histamine augments VCAM-1 expression on IL-4- and TNF-α-stimulated human umbilical vein endothelial cells. Int. Arch. Allergy Immunol. 111, 126-132. (Pubitemid 26319373)
39. Miki, I., Kusano, A., Ohta, S., Hanai, N., Otoshi, M., Masaki, S., Sato, S., Ohmori, K. (1996) Histamine enhanced the TNF-α-induced expression of E-selectin and ICAM-1 on vascular endothelial cells. Cell. Immunol. 171, 285-288. (Pubitemid 26268486)
40. Leurs, R., Church, M. K., Taglialatela, M. (2002) H1-antihistamines: inverse agonism, anti-inflammatory actions and cardiac effects. Clin. Exp. Allergy 32, 489-498. (Pubitemid 34429565)
41. Abbott, N. J. (2000) Inflammatory mediators and modulation of bloodbrain barrier permeability. Cell. Mol. Neurobiol. 20, 131-147.
42. Hirasawa, N., Ohtsu, H., Watanabe, T., Ohuchi, K. (2002) Enhancement of neutrophil infiltration in histidine decarboxylase-deficient mice. Immunology 107, 217-221. (Pubitemid 35279048)
43. Cairo, C. W., Mirchev, R., Golan, D. E. (2006) Cytoskeletal regulation couples LFA-1 conformational changes to receptor lateral mobility and clustering. Immunity 25, 297-308. (Pubitemid 44224146)
44. Giagulli, C., Ottoboni, L., Caveggion, E., Rossi, B., Lowell, C., Constantin, G., Laudanna, C., Berton, G. (2006) The Src family kinases Hck and Fgr are dispensable for inside-out, chemoattractant-induced signaling regulating β 2 integrin affinity and valency in neutrophils, but are required for β 2 integrin-mediated outside-in signaling involved in sustained adhesion. J. Immunol. 177, 604-611. (Pubitemid 43939174)
45. Hershenson, M. B., Chao, T. S., Abe, M. K., Gomes, I., Kelleher, M. D., Solway, J., Rosner, M. R. (1995) Histamine antagonizes serotonin and growth factor-induced mitogen-activated protein kinase activation in bovine tracheal smooth muscle cells. J. Biol. Chem. 270, 19908-19913.
46. Sakhalkar, S. P., Patterson, E. B., Khan, M. M. (2005) Involvement of histamine H1 and H2 receptors in the regulation of STAT-1 phosphorylation: inverse agonism exhibited by the receptor antagonists. Int. Immunopharmacol. 5, 1299-1309. (Pubitemid 40725723)
47. Moniri, N. H., Booth, R. G. (2006) Role of PKA and PKC in histamine H1 receptor-mediated activation of catecholamine neurotransmitter synthesis. Neurosci. Lett. 407, 249-253. (Pubitemid 44402876)
48. Laudanna, C., Campbell, J. J., Butcher, E. C. (1997) Elevation of intracellular cAMP inhibits RhoA activation and integrin-dependent leukocyte adhesion induced by chemoattractants. J. Biol. Chem. 272, 24141-24144. (Pubitemid 27418609)
49. Lovenberg, T. W., Roland, B. L., Wilson, S. J., Jiang, X., Pyati, J., Huvar, A., Jackson, M. R., Erlander, M. G. (1999) Cloning and functional expression of the human histamine H3 receptor. Mol. Pharmacol. 55, 1101-1107. (Pubitemid 29252378)
50. Teuscher, C., Subramanian, M., Noubade, R., Gao, J. F., Offner, H., Zachary, J. F., Blankenhorn, E. P. (2007) Central histamine H3 receptor signaling negatively regulates susceptibility to autoimmune inflammatory disease of the CNS. Proc. Natl. Acad. Sci. USA 104, 10146-10151. (Pubitemid 47175277)
51. Dunford, P. J., O'Donnell, N., Riley, J. P., Williams, K. N., Karlsson, L., Thurmond, R. L. (2006) The histamine H4 receptor mediates allergic airway inflammation by regulating the activation of CD4+ T cells. J. Immunol. 176, 7062-7070. (Pubitemid 43787887)
52. Cowden, J. M., Riley, J. P., Ma, J. Y., Thurmond, R. L., Dunford, P. J. (2010) Histamine H4 receptor antagonism diminishes existing airway inflammation and dysfunction via modulation of Th2 cytokines. Respir. Res. 11, 86.