Does nicotine influence cytokine profile and subsequent cell cycling/apoptotic responses in inflammatory bowel disease?

Inflammatory Bowel Diseases

Volumn 14, Issue 11, 2008, Pages 1469-1482

  Aldhous, Marian C ^a   Prescott, Robin J ^b   Roberts, Simon ^a   Samuel, Kay ^b   Waterfall, Martin ^b   Satsangi, Jack ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Cell cycle; Cytokines; Inflammatory bowel disease

Indexed keywords

CYTOKINE; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 23; LIPOPOLYSACCHARIDE; NICOTINE; PHYTOHEMAGGLUTININ; TRANSFORMING GROWTH FACTOR ALPHA; TRANSFORMING GROWTH FACTOR BETA; BIOLOGICAL MARKER;

ADULT; AGED; APOPTOSIS; ARTICLE; CELL CYCLE; CELL CYCLE G0 PHASE; CELL CYCLE G1 PHASE; CELL PROLIFERATION; CLINICAL ARTICLE; CONTROLLED STUDY; CROHN DISEASE; CYTOKINE PRODUCTION; ENTERITIS; FEMALE; HUMAN; HUMAN CELL; MALE; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; ULCERATIVE COLITIS; ADOLESCENT; ANALYSIS OF VARIANCE; CELL CULTURE; CHILD; COMPARATIVE STUDY; DRUG EFFECT; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNOLOGY; METABOLISM; MIDDLE AGED; MONONUCLEAR CELL; MULTIVARIATE ANALYSIS; PATHOPHYSIOLOGY; PHYSIOLOGY; PROBABILITY; REFERENCE VALUE; SENSITIVITY AND SPECIFICITY; SMOKING;

ADOLESCENT; ADULT; AGED; ANALYSIS OF VARIANCE; APOPTOSIS; BIOLOGICAL MARKERS; CELL CYCLE; CELLS, CULTURED; CHILD; COLITIS, ULCERATIVE; CROHN DISEASE; CYTOKINES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; HUMANS; INFLAMMATORY BOWEL DISEASES; LEUKOCYTES, MONONUCLEAR; MALE; MIDDLE AGED; MULTIVARIATE ANALYSIS; NICOTINE; PROBABILITY; REFERENCE VALUES; SENSITIVITY AND SPECIFICITY; SMOKING; YOUNG ADULT;

EID: 59249101083     PISSN: 10780998     EISSN: 15364844     Source Type: Journal    
DOI: 10.1002/ibd.20523     Document Type: Article

References (70)

1. Rubin GP, Hungin AP, Kelly PJ, et al. Inflammatory bowel disease: epidemiology and management in an English general practice population. Aliment Pharmacol Ther. 2000;14:1553-1559.
2. Mathew CG. New links to the pathogenesis of Crohn disease provided by genome-wide association scans. Nat Rev Genet. 2008;9:9-14.
3. Armitage EL, Aldhous MC, Anderson N, et al. Incidence of juvenile-onset Crohn's disease in Scotland: association with northern latitude and affluence. Gastroenterol. 2004;127:1051-1057.
4. Halfvarson J, Jess T, Magnuson A, et al. Environmental factors in inflammatory bowel disease: a co-twin control study of a Swedish-Danish twin population. Inflamm Bowel Dis. 2006;12:925-933.
5. Xavier RJ, Podolsky DK. Unravelling the pathogenesis of inflammatory bowel disease. Nature. 2007;448:427-434.
6. Cobrin GM, Abreu MT. Defects in mucosal immunity leading to Crohn's disease. Immunol Rev. 2005;206:277-295.
7. Targan SR, Karp LC. Defects in mucosal immunity leading to ulcerative colitis. Immunol Rev. 2005;206:296-305.
8. Neurath MF. IL-23: a master regulator in Crohn disease. Nat Med. 2007;13:26-28.
9. Yen D, Cheung J, Scheerens H, et al. IL-23 is essential for T cell-mediated colitis and promotes inflammation via IL-17 and IL-6. J Clin Invest. 2006;116:1310-1316.
10. Bu P, Keshavarzian A, Stone DD, et al. Apoptosis: one of the mechanisms that maintains unresponsiveness of the intestinal mucosal immune system. J Immunol. 2001;166:6399-6403.
11. Sturm A, Leite AZA, Danese S, et al. Divergent cell cycle kinetics underlie the distinct functional capacity of mucosal T cells in Crohn's disease and ulcerative colitis. Gut. 2004;53:1624-1631.
12. Ina K, Itoh J, Fukushima K, et al. Resistance of Crohn's disease T cells to multiple apoptotic signals is associated with a bcl-2/bax mucosal imbalance. J Immunol. 1999;163:1081-1090.
13. Doering J, Begue B, Lentze MJ, et al. Induction of T lymphocyte apoptosis by sulphasalazine in patients with Crohn's disease. Gut. 2004; 53:1632-1638.
14. Fayad R, Brand MI, Stone D, et al. Apoptosis resistance in ulcerative colitis: High expression of decoy receptors by lamina propria T cells. Eur J Immunol. 2006;36:2215-2222.
15. Begue B, Wajant H, Bambou J-C, et al. Implication of TNF-related apoptosis-inducing ligand in inflammatory intestinal epithelial lesions. Gastroenterol. 2006;130:1962-1974.
16. Birrenbach T, Bocker U. Inflammatory bowel disease and smoking: a review of epidemiology, pathophysiology, and therapeutic implications. Inflamm Bowel Dis. 2004;10:848-859.
17. Aldhous MC, Drummond HE, Anderson N, et al. Does cigarette smoking influence the phenotype of Crohn's disease? Analysis using the Montreal classification. Am J Gastroenterol. 2007;102:577-588.
18. Aldhous MC, Drummond HE, Anderson N, et al. Smoking habit and load influence age at diagnosis and disease extent in ulcerative colitis. Am J Gastroenterol. 2007;102:589-597.
19. Pullan RD, Rhodes J, Ganesh S, et al. Transdermal nicotine for active ulcerative colitis. N Engl J Med. 1994;330:811-815.
20. McGrath J, McDonald JWD, McDonald JK. Transdermal nicotine for induction of remission in ulcerative colitis (Review). Cochrane Database System Rev. 2004;4:CD004722.
21. Guinet E, Yoshida K, Nouri-Shirazi M. Nicotinic environment affects the differentiation and functional maturation of monocytes derived dendritic cells (DCs). Immunol Lett. 2004;95:45-55.
22. Mamata Y, Hakki A, Yamamoto Y, et al. Nicotine modulates cytokine production by Chlamydia pneumoniae infected human peripheral blood cells. Int Immunopharmacol. 2005;5:749-756.
23. Aicher A, Heeschen C, Mohaupt M, et al. Nicotine strongly activates dendritic cell-mediated adaptive immunity: potential role for progression of atherosclerotic lesions. Circulation. 2003;107:604-611.
24. Matsunaga K, Klein TW, Friedman H, et al. Involvement of nicotinic acetylcholine receptors in suppression of antimicrobial activity and cytokine responses of alveolar macrophages to Legionella pneumophila infection by nicotine. J Immunol. 2001; 167:6518-6524.
25. Madretsma GS, Donze GJ, van Dijk APM, et al. Nicotine inhibits the in vitro production of interleukin 2 and tumour necrosis factor-α by human mononuclear cells. Immunopharmacology. 1996;35:47-51.
26. van Dijk APM, Meijssen MAC, Brouwer AJBW, et al. Transdermal nicotine inhibits interleukin 2 synthesis by mononuclear cells derived from healthy volunteers. Eur J Clin Invest. 1998;28:664-671.
27. Sugano N, Ito K. Nicotine switches the form of H2O2-induced cell death from apoptosis to necrosis in U937 cells. Immunol Lett. 2000;72:163-166.
28. Crowley-Weber CL, Dvorakova K, Crowley C, et al. Nicotine increases oxidative stress, activates NF-kappaB and GRP78, induces apoptosis and sensitizes cells to genotoxic/xenobiotic stresses by a multiple stress inducer, deoxycholate: relevance to colon carcinogenesis. Chem Biol Interact. 2003;145:53-66.
29. Eliakim R, Fan QX, Babyatsky MW. Chronic nicotine administration differentially alters jejunal and colonic inflammation in interleukin-10 deficient mice. Eur J Gastroenterol Hepatol. 2002;14:607-614.
30. Eliakim R, Karmeli F, Cohen P, et al. Dual effect of chronic nicotine administration: augmentation of jejunitis and amelioration of colitis induced by iodoacetamide in rats. Int J Colorectal Dis. 2001;16:14-21.
31. Van Dijk JPM, Madretsma GS, Keuskamp ZJ, et al. Nicotine inhibits cytokine synthesis by mouse colonic mucosa. Eur J Pharmacol. 1995; 278:R11-R12.
32. Madretsma S, Wolters LM, van Dijk JP, et al. In-vivo effect of nicotine on cytokine production by human non-adherent mononuclear cells. Eur J Gastroenterol Hepatol. 1996;8:1017-1020.
33. Sykes AP, Brampton C, Klee S, et al. An investigation into the effect and mechanisms of action of nicotine in inflammatory bowel disease. Inflamm Res. 2000;49:311-319.
34. Lennard-Jones JE. Classification of inflammatory bowel disease. Scand J Gastroenterol. 1989;24(suppl):2-6.
35. Silverberg MS, Satsangi J, Ahmad T, et al. Toward an integrated clinical, molecular and serological classification of inflammatory bowel disease: report of a Working Party of the 2005 Montreal World Congress of Gastroenterology. Can J Gastroenterol. 2005;19(suppl A):5A-36A.
36. Reddy M, Eirikis E, Davis C, et al. Comparative analysis of lymphocyte activation marker expression and cytokine secretion profile in stimulated human peripheral blood mononuclear cell cultures: an in vitro model to monitor cellular immune function. J Immunol Methods. 2004;293:127-142.
37. Geng Y, Savage SM, Johnson LJ, et al. Effects of nicotine on the immune response. I Chronic exposure to nicotine impairs antigen receptor-mediated signal transduction in lymphocytes. Toxicol Appl Pharmacol. 1995;135:268-278.
38. McGilligan VE, Wallace JMW, Heavey PM, et al. Hypothesis about mechanisms through which nicotine might exert its effect on the inter-dependence of inflammation and gut barrier function in ulcerative colitis. Inflamm Bowel Dis. 2007;13:108-115.
39. Langrish CL, McKenzie BS, Wilson NJ, et al. IL-12 and IL-23: master regulators of innate and adaptive immunity. Immunol Rev. 2004;202: 96-105.
40. Stallmach A, Giese T, Schmidt C, et al. Cytokine/chemokine transcript profiles reflect mucosal inflammation in Crohn's disease. Int J Colorectal Dis. 2004;19:308-315.
41. Schmidt C, Giese T, Ludwig B, et al. Expression of interleukin-12-related cytokine transcripts in inflammatory bowel disease: elevated interleukin-23p19 and interleukin-27p28 in Crohn's disease but not in ulcerative colitis. Inflamm Bowel Dis. 2005;11:16-23.
42. Fuss IJ, Becker C, Yang Z, et al. Both IL-12p70 and IL-23 are synthesized during active Crohn's disease and are down-regulated by treatment with anti-IL-12 p40 monoclonal antibody. Inflamm Bowel Dis. 2006;12: 9-15.
43. Mannon PJ, Fuss IJ, Mayer L, et al. Anti-interleukin-12 antibody for active Crohn's disease. N Engl J Med. 2004;351:2069-2079.
44. Gotteland M, Lopez M, Muñoz C, et al. Local and systemic liberation of proinflammatory cytokines in ulcerative colitis. Dig Dis Sci. 1999;44: 830-835.
45. Elsasser-Beile U, von Kleist S, Gerlach S, et al. Cytokine production in whole blood cell cultures of patients with Crohn's disease and ulcerative colitis. J Clin Lab Anal. 1994;8:447-451.
46. Lügering A, Schmidt M, Lügering N, et al. Infliximab induces apoptosis in monocytes from patients with chronic active Crohn's disease by using a caspase-dependent pathway. Gastroenterol. 2001;121:1145-1157.
47. di Sabatino A, Ciccocioppo R, Cinque B, et al. Defective mucosal T cell death is sustainably reverted by infliximab in a caspase dependent pathway in Crohn's disease. Gut. 2004;53:70-77.
48. Nesbitt A, Fossati G, Bergin M, et al. Mechanism of action of Certolizumab Pegol (CDP870): in vitro comparison with other anti-tumor necrosis factor α agents. Inflamm Bowel Dis. 2007; 13:1323-1332.
49. Mitoma H, Horiuchi T, Hatta N, et al. Infliximab induces potent antiinflammatory responses by outside-to-inside signals through transmembrane TNF-α. Gastroenterology. 2005;128:376-392.
50. Nilkaeo A, Bhuvanath S. Interleukin-1 modulation of human placental trophoblast proliferation. Mediators Inflamm. 2006;2:79359.
51. Kaneko N, Kudo K, Mabuchi T, et al. Suppression of cell proliferation by interferon-alpha through interleukin-1 production in adult rat dentate gyrus. Neuropsychopharmacology. 2006;31:2619-2626.
52. Heller F, Florian P, Bojarski C, et al. Interleukin-13 is the key effector Th2 cytokine in ulcerative colitis that affects epithelial tight junctions, apoptosis, and cell restitution. Gastroenterol. 2005;129:550-564.
53. Sturm A, Itoh J, Jacobberger JW, et al. p53 negatively regulates intestinal immunity by delaying mucosal T cell cycling. J Clin Invest. 2002;109:1481-1492.
54. Stio M, Treves C, Martinesi M, et al. Effect of anti-TNF therapy and vitamin D derivatives on the proliferation of peripheral blood mononuclear cells in Crohn's disease. Dig Dis Sci. 2004; 49:328-335.
55. Pérez-Machado MA, Manzano Espinosa L, De La Morena Madrigal EJ, et al. Impaired mitogenic response of peripheral blood T cells in ulcerative colitis is not due to apoptosis. Dig Dis Sci. 1999;44:2530-2537.
56. Thomas GAO, Rhodes J, Mani V, et al. Transdermal nicotine as maintenance therapy for ulcerative colitis. N Engl J Med. 1995;332:988-992.
57. McGilligan VE, Wallace JMW, Heavey PM, et al. The effect of nicotine in vitro on the integrity of tight junctions in Caco-2 cell monolayers. Food Chem Toxicol. 2007;45:1593-1598.
58. Kikuchi H, Itoh J, Fukuda S. Chronic nicotine stimulation modulates the immune response of mucosal T cells to Th1-dominant pattern via nAChR by upregulation of Th1-specific transcriptional factor. Neurosci Lett. 2008;432:217-221.
59. Afzali B, Lombardi G, Lechler RI, et al. The role of T helper 17 (Th17) and regulatory T cells (Treg) in human organ transplantation and autoimmune disease. Clin Exp Immunol. 2007;148:32-46.
60. Yoshikawa H, Kurokawa M, Ozaki N, et al. Nicotine inhibits the production of proinflammatory mediators in human monocytes by suppression of IκB phosphorylation and nuclear factor-κB transcriptional activity through nicotinic acetylcholine receptor-α7. Clin Exp Immunol. 2006;146:116-123.
61. Takahashi HK, Iwagaki H, Hamano R, et al. alpha7 Nicotinic acetylcholine receptor stimulation inhibits lipopolysaccharide-induced interleukin-18 and -12 production in monocytes. J Pharmacol Sci. 2006;102: 143-146.
62. Sato KZ, Fujii T, Watanabe Y, et al. 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. 1999;266:17-20.
63. Geng Y, Savage SM, Razani-Boroujerdi S, et al. Effects of nicotine on the immune response. II. Chronic nicotine treatment induces T cell anergy. J Immunol. 1996;156:2384-2390.
64. Ingram JR, Thomas GA, Rhodes J, et al. A randomized trial of nicotine enemas for active ulcerative colitis. Clin Gastroenterol Hepatol. 2005; 3:1107-1114.
65. Ghia JE, Blennerhassett P, Kumar-Ondiveeran H, et al. The vagus nerve: a tonic inhibitory influence associated with inflammatory bowel disease in a murine model. Gastroenterology. 2006;131:1122-1130.
66. Proulx L-I, Castonguay A, Bissonnette EY. Cytokine production by alveolar macrophages is down regulated by the a-methylhydroxylation pathway of 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone (NNK). Carcinogenesis. 2004;25:997-1003.
67. Therriault M-J, Proulx L-I, Castonguay A, et al. Immunomodulatory effects of the tobacco-specific carcinogen, NNK, on alveolar macrophages. Clin Exp Immunol. 2003;132:232-238.
68. Hegazi RA, Rao KN, Mayle A, et al. Carbon monoxide ameliorates chronic murine colitis through a heme oxygenase 1-dependent pathway. J Exp Med. 2005;202:1703-1713.
69. Bernstein CN, Blanchard JF, Rawsthorne P, et al. The prevalence of extraintestinal diseases in inflammatory bowel disease: a population-based study. Am J Gastroenterol. 2001;96:1116-1122.
70. Manguso F, Sanges M, Staiano T, et al. Cigarette smoking and appendectomy are risk factors for extraintestinal manifestations in ulcerative colitis. Am J Gastroenterol. 2004;99:327-334.