Effects of the α7 nicotinic acetylcholine receptor agonist gts-21 on the innate immune response in humans

Shock

Volumn 36, Issue 1, 2011, Pages 5-11

  Kox, Matthijs ^a   Pompe, Jan C ^a   Gordinou De Gouberville, Marije C ^a   Van Der Hoeven, Johannes G ^a   Hoedemaekers, Cornelia W ^a   Pickkers, Peter ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

cytokines; Endotoxin; inflammation; innate immunity; pharmacology

Indexed keywords

3 (2,4 DIMETHOXYBENZYLIDENE)ANABASEINE; ENDOTOXIN; INTERLEUKIN 1 RECEPTOR; INTERLEUKIN 10; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; NICOTINIC RECEPTOR; PLACEBO; TUMOR NECROSIS FACTOR ALPHA;

ADULT; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BLOOD ANALYSIS; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; DOUBLE BLIND PROCEDURE; DRUG BLOOD LEVEL; ENDOTOXEMIA; HUMAN; HUMAN EXPERIMENT; IMMUNE RESPONSE; INFLAMMATION; INNATE IMMUNITY; MALE; NORMAL HUMAN;

ADOLESCENT; ADULT; ANTI-INFLAMMATORY AGENTS; BENZYLIDENE COMPOUNDS; ENDOTOXEMIA; HEMODYNAMICS; HUMANS; IMMUNITY, INNATE; INTERLEUKIN 1 RECEPTOR ANTAGONIST PROTEIN; INTERLEUKIN-10; INTERLEUKIN-6; LIPOPOLYSACCHARIDES; MALE; NICOTINIC AGONISTS; PYRIDINES; RECEPTORS, NICOTINIC; TUMOR NECROSIS FACTOR-ALPHA; YOUNG ADULT;

EID: 79959760320     PISSN: 10732322     EISSN: 15400514     Source Type: Journal    
DOI: 10.1097/SHK.0b013e3182168d56     Document Type: Article

References (40)

1. Delves PJ, Roitt IM: The immune system. First of two parts. N Engl J Med 343(1):37-49, 2000. (Pubitemid 30447991)
2. Tracey KJ, Beutler B, Lowry SF, Merryweather J, Wolpe S, Milsark IW, Hariri RJ, Fahey TJ III, Zentella A, Albert JD: Shock and tissue injury induced by recombinant human cachectin. Science 234(4775):470-474, 1986. (Pubitemid 17181429)
3. Nathan C: Points of control in inflammation. Nature 420(6917):846-852, 2002. (Pubitemid 36019637)
4. Goehler LE, Busch CR, Tartaglia N, Relton J, Sisk D, Maier SF, Watkins LR: Blockade of cytokine induced conditioned taste aversion by subdiaphragmatic vagotomy: further evidence for vagal mediation of immune-brain communication. Neurosci Lett 185(3):163-166, 1995.
5. Fleshner M, Goehler LE, Schwartz BA, McGorry M, Martin D, Maier SF, Watkins LR: Thermogenic and corticosterone responses to intravenous cytokines (IL-1beta and TNF-alpha) are attenuated by subdiaphragmatic vagotomy. J Neuroimmunol 86(2):134-141, 1998. (Pubitemid 28305354)
6. Tracey KJ: The inflammatory reflex. Nature 420(6917):853-859, 2002. (Pubitemid 36019638)
7. Wang H, Yu M, Ochani M, Amella CA, Tanovic M, Susarla S, Li JH, Wang H, Yang H, Ulloa L, et al.: Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature 421(6921):384-388, 2003. (Pubitemid 36157937)
8. Wittebole X, Hahm S, Coyle SM, Kumar A, Calvano SE, Lowry SF: Nicotine exposure alters in vivo human responses to endotoxin. Clin Exp Immunol 147(1):28-34, 2007. (Pubitemid 44915552)
9. Meyer EM, Kuryatov A, Gerzanich V, Lindstrom J, Papke RL: Analysis of 3-(4- hydroxy, 2-methoxybenzylidene)anabaseine selectivity and activity at human and rat alpha-7 nicotinic receptors. J Pharmacol Exp Ther 287(3):918-925, 1998. (Pubitemid 29131601)
10. Bruchfeld A, Goldstein RS, Chavan S, Patel NB, Rosas-Ballina M, Kohn N, Qureshi AR, Tracey KJ: Whole blood cytokine attenuation by cholinergic agonists ex vivo and relationship to vagus nerve activity in rheumatoid arthritis. J Intern Med 268(1):94-101, 2010.
11. Chatterjee PK, Al-Abed Y, Sherry B, Metz CN: Cholinergic agonists regulate JAK2/STAT3 signaling to suppress endothelial cell activation. Am J Physiol Cell Physiol 297(5):C1294YC1306, 2009.
12. Giebelen IA, van Westerloo DJ, Larosa GJ, de Vos AF, van der PT: Stimulation of alpha7 cholinergic receptors inhibits lipopolysaccharide-induced neutrophil recruitment by a tumor necrosis factor alpha-independent mechanism. Shock 27(4):443-447, 2007. (Pubitemid 46594978)
13. Giebelen IA, van Westerloo DJ, Larosa GJ, de Vos AF, van der PT: Local stimulation of alpha7 cholinergic receptors inhibits LPS-induced TNF-alpha release in the mouse lung. Shock 28(6):700-703, 2007. (Pubitemid 350135475)
14. Loram LC, Harrison JA, Chao L, Taylor FR, Reddy A, Travis CL, Giffard R, Al-Abed Y, Tracey K, Maier SF, et al.: Intrathecal injection of an alpha seven nicotinic acetylcholine receptor agonist attenuates gp120-induced mechanical allodynia and spinal pro-inflammatory cytokine profiles in rats. Brain Behav Immun 24(6):959-967, 2010.
15. Pavlov VA, Ochani M, Yang LH, Gallowitsch-Puerta M, Ochani K, Lin X, Levi J, Parrish WR, Rosas-Ballina M, Czura CJ, et al.: Selective alpha7- nicotinic acetylcholine receptor agonist GTS-21 improves survival in murine endotoxemia and severe sepsis. Crit Care Med 35(4):1139-1144, 2007. (Pubitemid 46598966)
16. Rosas-Ballina M, Goldstein RS, Gallowitsch-Puerta M, Yang L, Valdes-Ferrer SI, Patel NB, Chavan S, Al-Abed Y, Yang H, Tracey KJ: The selective alpha7 agonist GTS-21 attenuates cytokine production in human whole blood and human monocytes activated by ligands for TLR2, TLR3, TLR4, TLR9, and RAGE. Mol Med 15(7-8):195-202, 2009.
17. Yeboah MM, Xue X, Duan B, Ochani M, Tracey KJ, Susin M, Metz CN: Cholinergic agonists attenuate renal ischemia-reperfusion injury in rats. Kidney Int 74(1):62-69, 2008. (Pubitemid 351841900)
18. Freedman R, Olincy A, Buchanan RW, Harris JG, Gold JM, Johnson L, Allensworth D, Guzman-Bonilla A, Clement B, Ball MP, et al.: Initial phase 2 trial of a nicotinic agonist in schizophrenia. Am J Psychiatry 165(8):1040-1047, 2008.
19. Kitagawa H, Takenouchi T, Azuma R, Wesnes KA, Kramer WG, Clody DE, Burnett AL: Safety, pharmacokinetics, and effects on cognitive function of multiple doses of GTS-21 in healthy, male volunteers. Neuropsychopharmacology 28(3):542-551, 2003.
20. Olincy A, Harris JG, Johnson LL, Pender V, Kongs S, Allensworth D, Ellis J, Zerbe GO, Leonard S, Stevens KE, et al.: Proof-of-concept trial of an alpha7 nicotinic agonist in schizophrenia. Arch Gen Psychiatry 63(6):630-638, 2006. (Pubitemid 43848294)
21. Kox M, van Velzen JF, Pompe JC, Hoedemaekers CW, van der Hoeven JG, Pickkers P: GTS-21 inhibits proinflammatory cytokine release independent of the Toll-like receptor stimulated via a transcriptional mechanism involving JAK2 activation. Biochem Pharmacol 78(7):863-872, 2009.
22. Hirschfeld M, Ma Y, Weis JH, Vogel SN, Weis JJ: Cutting edge: repurification of lipopolysaccharide eliminates signaling through both human and murine tolllike receptor 2. J Immunol 165(2):618-622, 2000. (Pubitemid 30484724)
23. Wang H, Bloom O, Zhang M, Vishnubhakat JM, Ombrellino M, Che J, Frazier A, Yang H, Ivanova S, Borovikova L, et al.: HMG-1 as a late mediator of endotoxin lethality in mice. Science 285(5425):248-251, 1999. (Pubitemid 29329996)
24. Grebenchtchikov N, van der Ven-Jongekrijg J, Pesman GJ, Geurts-Moespot A, van der Meer JW, Sweep FC: Development of a sensitive ELISA for the quantification of human tumour necrosis factor-alpha using 4 polyclonal antibodies. Eur Cytokine Netw 16(3):215-222, 2005. (Pubitemid 46638754)
25. Lowry SF: Human endotoxemia: a model for mechanistic insight and therapeutic targeting. Shock 24(Suppl 1):94-100, 2005.
26. van Eijk LT, Pickkers P, Smits P, Bouw MP, van der Hoeven JG: Severe vagal response after endotoxin administration in humans. Intensive Care Med 30(12):2279-2281, 2004. (Pubitemid 40174267)
27. Kem WR, Mahnir VM, Prokai L, Papke RL, Cao X, LeFrancois S, Wildeboer K, Prokai-Tatrai K, Porter-Papke J, Soti F: Hydroxy metabolites of the Alzheimer's drug candidate 3-[(2,4-dimethoxy)benzylidene]-anabaseine dihydrochloride (GTS-21): their molecular properties, interactions with brain nicotinic receptors, and brain penetration. Mol Pharmacol 65(1):56-67, 2004. (Pubitemid 38113886)
28. Gabay C, Smith MF, Eidlen D, Arend WP: Interleukin 1 receptor antagonist (IL-1Ra) is an acute-phase protein. J Clin Invest 99(12):2930-2940, 1997. (Pubitemid 27278670)
29. van der PT, van Deventer SJ, ten CH, Levi M, ten Cate JW: Tumor necrosis factor is involved in the appearance of interleukin-1 receptor antagonist in endotoxemia. J Infect Dis 169(3):665-667, 1994. (Pubitemid 24063019)
30. Arzt E, Sauer J, Pollmacher T, Labeur M, Holsboer F, Reul JM, Stalla GK: Glucocorticoids suppress interleukin-1 receptor antagonist synthesis following induction by endotoxin. Endocrinology 134(2):672-677, 1994. (Pubitemid 24057209)
31. van der Poll T, Barber AE, Coyle SM, Lowry SF: Hypercortisolemia increases plasma interleukin-10 concentrations during human endotoxemiaV a clinical research center study. J Clin Endocrinol Metab 81(10):3604-3606, 1996. (Pubitemid 26339923)
32. de K, Lemaire LC, Giebelen IA, van Zoelen MA, Pater JM, van den Pangaart PS, Groot AP, de Vos AF, Elliott PJ, Meijers JC, et al.: Prednisolone dose-dependently influences inflammation and coagulation during human endotoxemia. J Immunol 178(3):1845-1851, 2007. (Pubitemid 46154657)
33. van der PT, Coyle SM, Barbosa K, Braxton CC, Lowry SF: Epinephrine inhibits tumor necrosis factor-alpha and potentiates interleukin 10 production during human endotoxemia. J Clin Invest 97(3):713-719, 1996. (Pubitemid 26057090)
34. Sloan RP, McCreath H, Tracey KJ, Sidney S, Liu K, Seeman T: RR interval variability is inversely related to inflammatory markers: the CARDIA study. Mol Med 13(3-4):178-184, 2007. (Pubitemid 46944960)
35. Thayer JF, Fischer JE: Heart rate variability, overnight urinary norepinephrine and C-reactive protein: evidence for the cholinergic anti-inflammatory pathway in healthy human adults. J Intern Med 265(4):439-447, 2009.
36. Jan BU, Coyle SM, Macor MA, Reddell M, Calvano SE, Lowry SF: Relationship of basal heart rate variability to in vivo cytokine responses after endotoxin exposure. Shock 33(4):363-368, 2010.
37. Gourlay SG, Benowitz NL, Forbes A, McNeil JJ: Determinants of plasma concentrations of nicotine and cotinine during cigarette smoking and transdermal nicotine treatment. Eur J Clin Pharmacol 51(5):407-414, 1997. (Pubitemid 27055910)
38. The FO, Boeckxstaens GE, Snoek SA, Cash JL, Bennink R, Larosa GJ, van den Wijngaard RM, Greaves DR, de Jonge WJ: Activation of the cholinergic antiinflammatory pathway ameliorates postoperative ileus in mice. Gastroenterology 133(4):1219-1228, 2007. (Pubitemid 47494458)
39. Marrero MB, Lucas R, Salet C, Hauser TA, Mazurov A, Lippiello PM, Bencherif M: An alpha7 nicotinic acetylcholine receptor-selective agonist reduces weight gain and metabolic changes in a mouse model of diabetes. J Pharmacol Exp Ther 332(1):173-180, 2010.
40. van Maanen MA, Lebre MC, van der PT, Larosa GJ, Elbaum D, Vervoordeldonk MJ, Tak PP: Stimulation of nicotinic acetylcholine receptors attenuates collagen-induced arthritis in mice. Arthritis Rheum 60(1):114-122, 2009.