Differential involvement of α4β2, α7 and α9α10 nicotinic acetylcholine receptors in B lymphocyte activation in vitro

International Journal of Biochemistry and Cell Biology

Volumn 43, Issue 4, 2011, Pages 516-524

  Koval, Lyudmyla ^a   Lykhmus, Olena ^a   Zhmak, Maxim ^b   Khruschov, Alexey ^b   Tsetlin, Victor ^b   Magrini, Elena ^c   Viola, Antonella ^c   Chernyavsky, Alexander ^d   Qian, Jing ^d   Grando, Sergei ^d   Komisarenko, Sergei ^a   Skok, Maryna ^a  

^a PALLADIN INSTITUTE OF BIOCHEMISTRY   (Ukraine)

^b SHEMYAKIN OVCHINNIKOV INSTITUTE OF BIOORGANIC CHEMISTRY   (Russian Federation)

^c UNIVERSITY OF MILAN   (Italy)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

B lymphocytes; CD40; IgM; Immune synapse; Nicotinic acetylcholine receptor

Indexed keywords

ACETYLCHOLINE; ACONITINE DERIVATIVE; ALPHA CONOTOXIN MII; BUNGAROTOXIN RECEPTOR; CD40 ANTIGEN; EPIBATIDINE; IMMUNOGLOBULIN M; NICOTINIC RECEPTOR; NICOTINIC RECEPTOR ALPHA4BETA2; NICOTINIC RECEPTOR ALPHA9; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIBODY PRODUCTION; ARTICLE; B LYMPHOCYTE ACTIVATION; BAGG ALBINO MOUSE; C57BL 6 MOUSE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; GENOTYPE; LYMPHOCYTE PROLIFERATION; MALE; MITOGENESIS; MOUSE; NONHUMAN; RECEPTOR BINDING; SPLEEN LYMPHOCYTE; SYNAPSE; UPREGULATION; WILD TYPE;

ANIMALS; ANTIBODY SPECIFICITY; B-LYMPHOCYTES; GENE EXPRESSION REGULATION; HUMANS; IMMUNOLOGICAL SYNAPSES; JURKAT CELLS; LYMPHOCYTE ACTIVATION; MALE; MICE; MUTATION; PROTEIN SUBUNITS; RECEPTORS, NICOTINIC; SUBSTRATE SPECIFICITY;

MUS;

EID: 79952100582     PISSN: 13572725     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocel.2010.12.003     Document Type: Article

References (54)

1. J.F. Alcorn, K. Ckless, A.L. Brown, A.S. Guala, J.K. Kolls, and M.E. Poynter Strain-dependent activation of NF-kappaB in the airway epithelium and its role in allergic airway inflammation Am J Physiol Lung Cell Mol Physiol 298 1 2010 L57 66
2. M. Alkondon, and E.X. Albuquerque Subtype-specific inhibition of nicotinic acetylcholine receptors by choline: a regulatory pathway J Pharmacol Exp Ther 318 1 2006 268 275
3. A.S. Alm, K. Li, D. Yang, R. Andersson, Y. Lu, and X. Wang Varying susceptibility of pulmonary cytokine production to lipopolysaccharide in mice Cytokine 49 3 2010 256 263
4. J. Arredondo, L.L. Hall, A. Ndoye, V.T. Nguyen, A.I. Chernyavsky, and D. Bercovich Central role of fibroblast alpha3 nicotinic acetylcholine receptor in mediating cutaneous effects of nicotine Lab Invest 83 2 2003 207 225 (Pubitemid 36255366)
5. J. Arredondo, D. Omelchenko, A.I. Chernyavsky, M.V. Skok, and S.A. Grando Functional roles of α7 nicotinic acetylcholine receptors in human B cell lymphoma line J Exp Pharmacol 1 2009 1 7
6. E.R. Baker, R. Zwart, E. Sher, and N.S. Millar Pharmacological properties of alpha 9 alpha 10 nicotinic acetylcholine receptors revealed by heterologous expression of subunit chimeras Mol Pharmacol 65 2 2004 453 460 (Pubitemid 38134274)
7. C. Barcia, A. Gomez, V. de Pablos, E. Fernández-Villalba, C. Liu, and K.M. Kroeger CD20, CD3, and CD40 ligand microclusters segregate three-dimensionally in vivo at B-cell-T-cell immunological synapses after viral immunity in primate brain J Virol 82 20 2008 9978 9993
8. E. Battaglioli, C. Gotti, S. Terzano, A. Flora, F. Clementi, and D. Fornasari Expression and transcriptional regulation of the human alpha3 neuronal nicotinic receptor subunit in T lymphocyte cell lines J Neurochem 71 1998 1261 1270 (Pubitemid 28390281)
9. F. Borcherding, M. Nitschke, G. Hundorfean, J. Rupp, D. von Smolinski, and K. Bieber The CD40-CD40L pathway contributes to the proinflammatory function of intestinal epithelial cells in inflammatory bowel disease Am J Pathol 176 4 2010 1816 1827
10. K. Brejc, W.J. van Dijk, R.V. Klaassen, M. Schuurmans, J. van der Oost, and A.B. Smit Crystal structure of an ACh-binding protein reveals the ligand-binding domain of nicotinic receptors Nature 411 2001 269 276 (Pubitemid 32467026)
11. J.P. Changeux Nicotine addiction and nicotinic receptors: lessons from genetically modified mice Nat Rev Neurosci 11 6 2010 389 401
12. A.I. Chernyavsky, J. Arredondo, L.M. Marubio, and S.A. Grando Differential regulation of keratinocyte chemokinesis and chemotaxis through distinct nicotinic receptor subtypes J Cell Sci 117 23 2004 5665 5679 (Pubitemid 40012212)
13. B.M. Conti-Fine, D. Navaneetham, S. Lei, and A.D.J. Maus Neuronal nicotinic receptors in non-neuronal cells: new mediators of tobacco toxicity? Eur J Pharmacol 393 2000 279 294 (Pubitemid 30193427)
14. W.J. De Jonge, and L. Ulloa The alpha7 nicotinic acetylcholine receptor as a pharmacological target for inflammation Br J Pharmacol 151 2007 915 929 (Pubitemid 47195518)
15. T. Fujii An independent, non-neuronal cholinergic system in lymphocytes and its roles in regulation of immune function Nippon Yakurigaku Zasshi 123 2004 179 188 (Pubitemid 38419483)
16. Y.X. Fujii, H. Fujigaya, Y. Moriwaki, H. Misawa, T. Kasahara, and S.A. Grando Enhanced serum antigen-specific IgG1 and proinflammatory cytokine production in nicotinic acetylcholine receptor alpha7 subunit gene knockout mice J Neuroimmunol 189 2007 69 73
17. G. Galvis, K.S. Lips, and W. Kummer Expression of nicotinic acetylcholine receptors on murine alveolar macrophages J Mol Neurosci 30 1-2 2006 107 108 (Pubitemid 46035342)
18. A. Grandien, A. Brás, and C. Martinez Acquisition of CD40 expression during murine B-cell differentiation Scand J Immunol 43 1 1996 47 55 (Pubitemid 26024530)
19. V. Grau, S. Wilker, P. Hartmann, K.S. Lips, S.A. Grando, and W. Padberg Administration of keratinocyte growth factor (KGF) modulates the pulmonary expression of nicotinic acetylcholine receptor subunits alpha7, alpha9 and alpha10 Life Sci 80 24-25 2007 2290 2293 (Pubitemid 46818264)
20. C.R. Gwilt, L.E. Donnelly, and D.F. Rogers The non-neuronal cholinergic system in the airways: an unappreciated regulatory role in pulmonary inflammation? Pharmacol Ther 115 2007 208 222 (Pubitemid 47042914)
21. A. Hecker, Z. Mikulski, K.S. Lips, U. Pfeil, A. Zakrzewicz, and S. Wilker Upregulation of acetylcholine synthesis and paracrine cholinergic signaling in intravascular transplant leukocytes during rejection of rat renal allografts J Leukoc Biol 86 2009 13 22
22. E. Hellstrom-Lindahl, X. Zhang, and A. Nordberg Expression of nicotinic receptor subunit mRNAs in lymphocytes from normal and patients with Alzheimer's disease Alzheimer's Res 3 1997 29 36 (Pubitemid 27246331)
23. 2+ stores J Pharmacol Exp Ther 293 2000 166 171 (Pubitemid 30180936)
24. R. Kalra, S.P. Singh, D. Kracko, S.G. Matta, B.M. Sharp, and M.L. Sopori Chronic self-administration of nicotine in rats impairs T cell responsiveness J Pharmacol Exp Ther 302 3 2002 935 939 (Pubitemid 34920213)
25. D.O. Koroev, M.A. Titova, T.D. Volkova, M.B. Oboznaia, M.P. Filatova, and E.N. Fufacheva Induction of antibodies to particular sites of the alpha7 subunit of the nicotinic acetylcholine receptor in mice of different lines Bioorg Khim 33 2007 442 447 Russian
26. O.M. Koval, L.P. Voitenko, M.V. Skok, O.Y. Lykhmus, V.I. Tsetlin, and M.N. Zhmak The β-subunit composition of nicotinic acetylcholine receptors in the neurons of the guinea pig inferior mesenteric ganglion Neurosci Lett 365 2 2004 143 146 (Pubitemid 38881642)
27. L.M. Koval, O.Y. Lykhmus, D.M. Omelchenko, S.V. Komisarenko, and M.V. Skok The role of alpha7 nicotinic acetylcholine receptors in B lymphocyte activation Ukr Biochim Zh 81 4 2009 5 11
28. O. Lykhmus, L. Koval, S. Pavlovych, M. Zouridakis, P. Zisimopoulou, and S. Tzartos Functional effects of antibodies against non-neuronal nicotinic acetylcholine receptors Immunol Lett 128 2010 68 73
29. Lykhmus OY, Koval LM, Skok MV, Zouridakis M, Zisimopoulou P, Tzartos SJ, et al. Antibodies against extracellular domains of α4 and α7 subunits alter the levels of nicotinic receptors in the mouse brain and affect memory. Possible Relevance to Alzheimer Pathology, in press.
30. S. Malapati, and S.K. Pierce The influence of CD40 on the association of the B cell antigen receptor with lipid rafts in mature and immature cells Eur J Immunol 31 2001 3789 3797 (Pubitemid 34030993)
31. J.M. McIntosh, P.V. Plazas, M. Watkins, M.E. Gomez-Casati, B.M. Olivera, and A.B. Elgoyhen A novel alpha-conotoxin, PeIA, cloned from Conus pergrandis, discriminates between rat alpha9alpha10 and alpha7 nicotinic cholinergic receptors J Biol Chem 280 34 2005 30107 30112 (Pubitemid 41216187)
32. E.M. Nicolussi, S. Huck, H. Lassmann, and M. Bradl The cholinergic anti-inflammatory system limits T-cell infiltration into neurodegenerative CNS, but cannot counteract complex CNS inflammation Neurobiol Dis 35 2009 24 31
33. E. Nizri, M. Irony-Tur-Sinai, O. Lory, A. Orr-Urtreger, E. Lavi, and T. Brenner Activation of the cholinergic anti-inflammatory system by nicotine attenuates neuroinflammation via suppression of Th1 and Th17 responses J Immunol 183 2009 6681 6688
34. A. Orr-Urtreger, F.M. Göldner, M. Saeki, I. Lorenzo, L. Goldberg, and M. De Biasi Mice deficient in the alpha7 neuronal nicotinic receptor lack alpha-bungarotoxin binding sites and hippocampal fast nicotinic currents J Neurosci 17 1997 9165 9171 (Pubitemid 27498444)
35. M. Packiam, S.J. Veit, D.J. Anderson, R.R. Ingalls, and A.E. Jerse Mouse strain-dependent differences in susceptibility to Neisseria gonorrhoeae infection and induction of innate immune responses Infect Immun 78 1 2010 433 440
36. H. Peng, R.L. Ferris, T. Matthews, H. Hiel, A. Lopez-Albaitero, and L.R. Lustig Characterization of the human nicotinic acetylcholine receptor subunit alpha 9 (CHRNA9) and alpha 10 (CNRNA10) in lymphocytes Life Sci 76 2004 263 280 (Pubitemid 39452910)
37. M.R. Picciotto, M. Zoli, C. Léna, A. Bessis, Y. Lallemand, and N. Le Novre Abnormal avoidance learning in mice lacking functional high-affinity nicotine receptor in the brain Nature 374 1995 65 67
38. P.V. Plazas, E. Katz, M.E. Gomez-Casati, C. Bouzat, and A.B. Elgoyhen Stoichiometry of the alpha9alpha10 nicotinic cholinergic receptor J Neurosci 25 47 2005 10905 10912 (Pubitemid 41692620)
39. S. Razani-Boroujerdi, R.T. Boyd, M.I. Davila-Garci, J.S. Nandi, N.C. Mishra, and S.P. Singh T cells express alpha7-nicotinic acetylcholine receptor subunits that require a functional TCR and leukocyte-specific protein tyrosine kinase for nicotine-induced Ca2+ response J Immunol 179 5 2007 2889 2898
40. D. Richman, and B. Arnason Nicotinic acetylcholine receptor: evidence for a functionally distinct receptor on human lymphocytes Proc Natl Acad Sci USA 76 1979 4632 4635
41. M. Rosas-Ballina, and K.J. Tracey The neurology of the immune system: neural reflexes regulate immunity Neuron 64 1 2009 28 32
42. K.Z. Sato, T. Fujii, Y. Watanabe, S. Yamada, T. Ando, and F. Kazuko Diversity of mRNA expression for muscarinic acetylcholine receptor subtypes and neuronal nicotinic acetylcholine receptor subunits in human mononuclear leukocytes and leukemic cell lines Neurosci Lett 266 1999 17 20 (Pubitemid 29219745)
43. C.G.V. Sharples, and S. Wonnacott Neuronal nicotinic receptors Tocris Rev 19 2001 1 12
44. I.V. Shelukhina, E.V. Kryukova, M.V. Skok, E.Y. Lykhmus, M.N. Zhmak, and D.Y. Mordvintsev Analysis of specificity of antibodies against synthetic fragments of different neuronal nicotinic acetylcholine receptor subunits Biochemistry (Mosc) 71 7 2006 749 758 (Pubitemid 44092038)
45. F.D. Shi, W.H. Piao, Y.P. Kuo, D.I. Campagnolo, T.L. Vollmer, and R.J. Lukas Nicotine attenuation of CNS inflammation and autoimmunity J Immunol 182 2009 1730 1739
46. Skok MV To channel or not to channel? Functioning of nicotinic acetylcholine receptors in leukocytes J Leukocyte Biol 86 2009 1 3
47. M.V. Skok, L.P. Voitenko, S.V. Voitenko, E.Y. Lykhmus, E.N. Kalashnik, and T. Litvin Study of α subunit composition of nicotinic acetylcholine receptor in the neurons of autonomic ganglia of the rat with subunit-specific anti-α(181-192) peptide antibodies Neuroscience 93 4 1999 1437 1446
48. M.V. Skok, E.N. Kalashnik, L.N. Koval, V.I. Tsetlin, Y.N. Utkin, and J.P. Changeux Functional nicotinic acetylcholine receptors are expressed in B lymphocyte-derived cell lines Mol Pharmacol 64 2003 885 889 (Pubitemid 37153057)
49. M.V. Skok, R. Grailhe, and J.P. Changeux Nicotinic receptors regulate B lymphocyte activation and immune response Eur J Pharmacol 517 2005 246 251 (Pubitemid 40977902)
50. M.V. Skok, R. Grailhe, F. Agenes, and J.P. Changeux The role of nicotinic acetylcholine receptors in lymphocyte development J Neuroimmunol 171 2006 86 98 (Pubitemid 41832280)
51. M.V. Skok, R. Grailhe, F. Agenes, and J.P. Changeux The role of nicotinic receptors in B-lymphocyte development and activation Life Sci 80 2007 2334 2336 (Pubitemid 46818278)
52. A. Viola, R.L. Contento, and B. Molon Signaling amplification at the immunological synapse Curr Top Microbiol Immunol 340 2010 109 122
53. H. Wang, M. Yu, M. Ochani, C.A. Amella, M. Tanovic, and S. Susarla Nicotinic receptor α7 subunit is an essential regulator of inflammation Nature 421 2003 384 388 (Pubitemid 36157937)
54. H. Yoshikawa, M. Kurokawa, N. Ozaki, K. Nara, K. Atou, and E. Takada Nicotine inhibits the production of proinflammatory mediators in human monocytes by suppression of I-kappaB phosphorylation and nuclear factor-kappaB transcriptional activity through nicotinic acetylcholine receptor alpha7 Clin Exp Immunol 146 1 2006 116 123 (Pubitemid 44393846)