Nicotine-mediated signals modulate cell death and survival of T lymphocytes

Toxicology and Applied Pharmacology

Volumn 242, Issue 3, 2010, Pages 299-309

  Oloris, Silvia C S ^a,b   Frazer Abel, Ashley A ^a,c   Jubala, Cristan M ^a,d   Fosmire, Susan P ^a   Helm, Karen M ^e   Robinson, Sally R ^g   Korpela, Derek M ^g   Duckett, Megan M ^g   Baksh, Shairaz ^f   Modiano, Jaime F ^a,e,g,h  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b DEPARTAMENTO DE FÍSICA   (Brazil)

^c DEPARTMENT OF MEDICINE   (United States)

^d UNIVERSITY OF COLORADO   (United States)

^e UNIVERSITY OF COLORADO CANCER CENTER   (United States)

^f UNIVERSITY OF ALBERTA   (Canada)

^g UNIVERSITY OF MINNESOTA   (United States)

^h UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Acetylcholine receptors; Apoptosis; Calcium; Lymphocytes; Nicotine; RNA interference

Indexed keywords

CALCIUM ION; CASPASE 3; CYCLIN D2; CYCLIN DEPENDENT KINASE 4; NICOTINE; NICOTINIC RECEPTOR; TRANSCRIPTION FACTOR NFAT;

APOPTOSIS; ARTICLE; CALCIUM MOBILIZATION; CELL DEATH; CELL SURVIVAL; CELL TYPE; CONTROLLED STUDY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; LEUKEMIA CELL LINE; LYMPHOCYTE ACTIVATION; LYMPHOCYTE TRANSFORMATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

APOPTOSIS; CELL SURVIVAL; HUMANS; JURKAT CELLS; LEUKEMIA, T-CELL; NICOTINE; NICOTINIC AGONISTS; RECEPTORS, NICOTINIC; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 73449090398     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2009.10.020     Document Type: Article

References (61)

1. Abraham R.T., and Weiss A. Jurkat T cells and development of the T-cell receptor signalling paradigm. Nat. Rev. Immunol. 4 (2004) 301-308
2. Amos C.I., Wu X., Broderick P., Gorlov I.P., Gu J., Eisen T., Dong Q., Zhang Q., Gu X., Vijayakrishnan J., Sullivan K., Matakidou A., Wang Y., Mills G., Doheny K., Tsai Y.Y., Chen W.V., Shete S., Spitz M.R., and Houlston R.S. Genome-wide association scan of tag SNPs identifies a susceptibility locus for lung cancer at 15q25.1. Nat. Genet. 40 (2008) 616-622
3. Aoshiba K., Nagai A., Yasui S., and Konno K. Nicotine prolongs neutrophil survival by suppressing apoptosis. J. Lab. Clin. Med. 127 (1996) 186-194
4. Arredondo J., Nguyen V.T., Chernyavsky A.I., Bercovich D., Orr-Urtreger A., Kummer W., Lips K., Vetter D.E., and Grando S.A. Central role of alpha7 nicotinic receptor in differentiation of the stratified squamous epithelium. J. Cell Biol. 159 (2002) 325-336
5. Arredondo J., Hall L.L., Ndoye A., Nguyen V.T., Chernyavsky A.I., Bercovich D., Orr-Urtreger A., Beaudet A.L., and Grando S.A. Central role of fibroblast alpha3 nicotinic acetylcholine receptor in mediating cutaneous effects of nicotine. Lab. Invest. 83 (2003) 207-225
6. Asanuma K., Tsuji N., Endoh T., Yagihashi A., and Watanabe N. Survivin enhances Fas ligand expression via up-regulation of specificity protein 1-mediated gene transcription in colon cancer cells. J. Immunol. 172 (2004) 3922-3929
7. Benhammou K., Lee M., Strook M., Sullivan B., Logel J., Raschen K., Gotti C., and Leonard S. [(3)H]Nicotine binding in peripheral blood cells of smokers is correlated with the number of cigarettes smoked per day. Neuropharmacology 39 (2000) 2818-2829
8. Benowitz N.L., and Gourlay S.G. Cardiovascular toxicity of nicotine: implications for nicotine replacement therapy. J. Am. Coll. Cardiol. 29 (1997) 1422-1431
9. Benowitz N.L., Porchet H., Sheiner L., and Jacob P.d. Nicotine absorption and cardiovascular effects with smokeless tobacco use: comparison with cigarettes and nicotine gum. Clin. Pharmacol. Ther. 44 (1988) 23-28
10. Berrettini W., Yuan X., Tozzi F., Song K., Francks C., Chilcoat H., Waterworth D., Muglia P., and Mooser V. Alpha-5/alpha-3 nicotinic receptor subunit alleles increase risk for heavy smoking. Mol. Psychiatry 13 (2008) 368-373
11. Catassi A., Servent D., Paleari L., Cesario A., and Russo P. Multiple roles of nicotine on cell proliferation and inhibition of apoptosis: implications on lung carcinogenesis. Mutat. Res. 659 (2008) 221-231
12. Changeux J.P., and Edelstein S.J. Nicotinic acetylcholine receptors: from molecular biology to cognition (2005), Odile Jacob Publishing Corp., New York
13. Conti-Fine B.M., Navaneetham D., Lei S., and Maus A.D. Neuronal nicotinic receptors in non-neuronal cells: new mediators of tobacco toxicity?. Eur. J. Pharmacol. 393 (2000) 279-294
14. Cooke J.P. Angiogenesis and the role of the endothelial nicotinic acetylcholine receptor. Life Sci. 80 (2007) 2347-2351
15. Cordero-Erausquin M., Marubio L.M., Klink R., and Changeux J.P. Nicotinic receptor function: new perspectives from knockout mice. Trends Pharmacol. Sci. 21 (2000) 211-217
16. Dasgupta P., Kinkade R., Joshi B., Decook C., Haura E., and Chellappan S. Nicotine inhibits apoptosis induced by chemotherapeutic drugs by up-regulating XIAP and survivin. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 6332-6337
17. Fowler C.D., Arends M.A., and Kenny P.J. Subtypes of nicotinic acetylcholine receptors in nicotine reward, dependence, and withdrawal: evidence from genetically modified mice. Behav. Pharmacol. 19 (2008) 461-484
18. Frazer-Abel A.A., Baksh S., Fosmire S.P., Willis D., Pierce A.M., Meylemans H., Linthicum D.S., Burakoff S.J., Coons T., Bellgrau D., and Modiano J.F. Nicotine activates NFATc2 and prevents cell cycle entry in T cells. J. Pharmacol. Exp. Ther. 311 (2004) 758-769
19. Frost V., and Sinclair A.J. p27KIP1 is down-regulated by two different mechanisms in human lymphoid cells undergoing apoptosis. Oncogene 19 (2000) 3115-3120
20. Frost V., Al-Mehairi S., and Sinclair A.J. Exploitation of a non-apoptotic caspase to regulate the abundance of the cdkI p27(KIP1) in transformed lymphoid cells. Oncogene 20 (2001) 2737-2748
21. Garrido R., Mattson M.P., Hennig B., and Toborek M. Nicotine protects against arachidonic-acid-induced caspase activation, cytochrome c release and apoptosis of cultured spinal cord neurons. J. Neurochem. 76 (2001) 1395-1403
22. Geng Y., Savage S.M., Johnson L.J., Seagrave J., and Sopori M.L. Effects of nicotine on the immune response. I. Chronic exposure to nicotine impairs antigen receptor-mediated signal transduction in lymphocytes. Toxicol. Appl. Pharmacol. 135 (1995) 268-278
23. George J., Bais H.P., and Ravishankar G.A. Biotechnological production of plant-based insecticides. Crit. Rev. Biotechnol. 20 (2000) 49-77
24. Gritz E.R., Baer-Weiss V., Benowitz N.L., Van Vunakis H., and Jarvik M.E. Plasma nicotine and cotinine concentrations in habitual smokeless tobacco users. Clin. Pharmacol. Ther. 30 (1981) 201-209
25. Grutter T., and Changeux J.P. Nicotinic receptors in wonderland. Trends Biochem. Sci. 26 (2001) 459-463
26. Hakki A., Pennypacker K., Eidizadeh S., Friedman H., and Pross S. Nicotine inhibition of apoptosis in murine immune cells. Exp. Biol. Med. 226 (2001) 947-953
27. Hung R.J., McKay J.D., Gaborieau V., Boffetta P., Hashibe M., Zaridze D., Mukeria A., Szeszenia-Dabrowska N., Lissowska J., Rudnai P., Fabianova E., Mates D., Bencko V., Foretova L., Janout V., Chen C., Goodman G., Field J.K., Liloglou T., Xinarianos G., Cassidy A., McLaughlin J., Liu G., Narod S., Krokan H.E., Skorpen F., Elvestad M.B., Hveem K., Vatten L., Linseisen J., Clavel-Chapelon F., Vineis P., Bueno-de-Mesquita H.B., Lund E., Martinez C., Bingham S., Rasmuson T., Hainaut P., Riboli E., Ahrens W., Benhamou S., Lagiou P., Trichopoulos D., Holcatova I., Merletti F., Kjaerheim K., Agudo A., Macfarlane G., Talamini R., Simonato L., Lowry R., Conway D.I., Znaor A., Healy C., Zelenika D., Boland A., Delepine M., Foglio M., Lechner D., Matsuda F., Blanche H., Gut I., Heath S., Lathrop M., and Brennan P. A susceptibility locus for lung cancer maps to nicotinic acetylcholine receptor subunit genes on 15q25. Nature 452 (2008) 633-637
28. Jarvik M.E., Madsen D.C., Olmstead R.E., Iwamoto-Schaap P.N., Elins J.L., and Benowitz N.L. Nicotine blood levels and subjective craving for cigarettes. Pharmacol. Biochem. Behav. 66 (2000) 553-558
29. Jubala C.M., Wojcieszyn J.W., Valli V.E.O., Getzy D.M., Fosmire S.P., Coffey D., Bellgrau D., and Modiano J.F. CD20 expression in normal canine B cells and in canine non-Hodgkin's lymphoma. Vet. Pathol. 42 (2005) 468-476
30. Kane J.K., Konu O., Ma J.Z., and Li M.D. Nicotine coregulates multiple pathways involved in protein modification/degradation in rat brain. Brain Res. Mol. Brain Res. 132 (2004) 181-191
31. Kawashima K., and Fujii T. Extraneuronal cholinergic system in lymphocytes. Pharmacol. Ther. 86 (2000) 29-48
32. Khare S., Banai Y., Gokulan K., Smith III R., Linthicum D.S., and Modiano J.F. Early changes in metabolism of leukemic cell lines upon induction of apoptosis by cytotoxic drugs. Eur. J. Pharmacol. 465 (2003) 23-30
33. Lang F., Foller M., Lang K.S., Lang P.A., Ritter M., Gulbins E., Vereninov A., and Huber S.M. Ion channels in cell proliferation and apoptotic cell death. J. Membr. Biol. 205 (2005) 147-157
34. Leonard S., and Bertrand D. Neuronal nicotinic receptors: from structure to function. Nicotine Tob. Res. 3 (2001) 203-223
35. Lin P.Y., Fosmire S.P., Park S.H., Park J.Y., Baksh S., Modiano J.F., and Weiss R.H. Attenuation of PTEN increases p21 stability and cytosolic localization in kidney cancer cells: a potential mechanism of apoptosis resistance. Mol. Cancer 6 (2007) 16
36. Lindstrom J. Nicotinic acetylcholine receptors in health and disease. Mol. Neurobiol. 15 (1997) 193-222
37. Mai H., May W.S., Gao F., Jin Z., and Deng X. A functional role for nicotine in Bcl2 phosphorylation and suppression of apoptosis. J. Biol. Chem. 278 (2003) 1886-1891
38. Maneckjee R., and Minna J.D. Opioid and nicotine receptors affect growth regulation of human lung cancer cell lines. Proc. Natl. Acad. Sci. U.S.A. 87 (1990) 3294-3298
39. Mariggio M.A., Guida L., Laforgia A., Santacroce R., Curci E., Montemurro P., and Fumarulo R. Nicotine effects on polymorphonuclear cell apoptosis and lipopolysaccharide-induced monocyte functions. A possible role in periodontal disease?. J. Periodontal Res. 36 (2001) 32-39
40. Medina-Palazon C., Bernard E., Frost V., Morley S., and Sinclair A.J. KIPase activity is a novel caspase-like activity associated with cell proliferation. Eur. J. Biochem. 271 (2004) 2716-2723
41. Middlebrook A.J., Martina C., Chang Y., Lukas R.J., and DeLuca D. Effects of nicotine exposure on T cell development in fetal thymus organ culture: arrest of T cell maturation. J. Immunol. 169 (2002) 2915-2924
42. Modiano J.F., Domenico J., Szepesi A., Lucas J.J., and Gelfand E.W. Differential requirements for interleukin-2 distinguish the expression and activity of the cyclin-dependent kinases Cdk4 and Cdk2 in human T cells. J. Biol. Chem. 269 (1994) 32972-32978
43. Modiano J.F., Mayor J., Ball C., Chitko-McKown C.G., Sakata N., Domenico-Hahn J., Lucas J.J., and Gelfand E.W. Quantitative and qualitative signals determine T-cell cycle entry and progression. Cell. Immunol. 197 (1999) 19-29
44. Petro T.M., Peterson D.S., and Fung Y.K. Nicotine enhances interleukin production of rat splenic T lymphocytes. Immunopharmacol. Immunotoxicol. 14 (1992) 463-475
45. Petro T.M., Schwartzbach S.D., and Zhang S. Smokeless tobacco and nicotine bring about excessive cytokine responses of murine memory T-cells. Int. J. Immunopharmacol. 21 (1999) 103-114
46. Quick M.W., and Lester R.A. Desensitization of neuronal nicotinic receptors. J. Neurobiol. 53 (2002) 457-478
47. Rezvani K., Teng Y., Shim D., and De Biasi M. Nicotine regulates multiple synaptic proteins by inhibiting proteasomal activity. J. Neurosci. 27 (2007) 10508-10519
48. Rose J.E., Jarvik M.E., and Rose K.D. Transdermal administration of nicotine. Drug Alcohol Depend. 13 (1984) 209-213
49. Rose J.E., Herskovic J.E., Trilling Y., and Jarvik M.E. Transdermal nicotine reduces cigarette craving and nicotine preference. Clin. Pharmacol. Ther. 38 (1985) 450-456
50. Schneider N.G., Lunell E., Olmstead R.E., and Fagerstrom K.O. Clinical pharmacokinetics of nasal nicotine delivery. A review and comparison to other nicotine systems. Clin. Pharmacokinet. 31 (1996) 65-80
51. Sopori M. Effects of cigarette smoke on the immune system. Nat. Rev. Immunol. 2 (2002) 372-377
52. Sugano N., Minegishi T., Kawamoto K., and Ito K. Nicotine inhibits UV-induced activation of the apoptotic pathway. Toxicol. Lett. 125 (2001) 61-65
53. Suzuki N., Wakisaka S., Takeba Y., Mihara S., and Sakane T. Effects of cigarette smoking on Fas/Fas ligand expression of human lymphocytes. Cell. Immunol. 192 (1999) 48-53
54. Tambyrajah W.S., Bowler L.D., Medina-Palazon C., and Sinclair A.J. Cell cycle-dependent caspase-like activity that cleaves p27(KIP1) is the beta(1) subunit of the 20S proteasome. Arch. Biochem. Biophys. 466 (2007) 186-193
55. Thorgeirsson T.E., Geller F., Sulem P., Rafnar T., Wiste A., Magnusson K.P., Manolescu A., Thorleifsson G., Stefansson H., Ingason A., Stacey S.N., Bergthorsson J.T., Thorlacius S., Gudmundsson J., Jonsson T., Jakobsdottir M., Saemundsdottir J., Olafsdottir O., Gudmundsson L.J., Bjornsdottir G., Kristjansson K., Skuladottir H., Isaksson H.J., Gudbjartsson T., Jones G.T., Mueller T., Gottsater A., Flex A., Aben K.K., de Vegt F., Mulders P.F., Isla D., Vidal M.J., Asin L., Saez B., Murillo L., Blondal T., Kolbeinsson H., Stefansson J.G., Hansdottir I., Runarsdottir V., Pola R., Lindblad B., van Rij A.M., Dieplinger B., Haltmayer M., Mayordomo J.I., Kiemeney L.A., Matthiasson S.E., Oskarsson H., Tyrfingsson T., Gudbjartsson D.F., Gulcher J.R., Jonsson S., Thorsteinsdottir U., Kong A., and Stefansson K. A variant associated with nicotine dependence, lung cancer and peripheral arterial disease. Nature 452 (2008) 638-642
56. Tohgi H., Utsugisawa K., and Nagane Y. Protective effect of nicotine through nicotinic acetylcholine receptor alpha 7 on hypoxia-induced membrane disintegration and DNA fragmentation of cultured PC12 cells. Neurosci. Lett. 285 (2000) 91-94
57. Wang H., and Sun X. Desensitized nicotinic receptors in brain. Brain Res. Brain Res. Rev. 48 (2005) 420-437
58. West K.A., Brognard J., Clark A.S., Linnoila I.R., Yang X., Swain S.M., Harris C., Belinsky S., and Dennis P.A. Rapid Akt activation by nicotine and a tobacco carcinogen modulates the phenotype of normal human airway epithelial cells. J. Clin. Invest. 111 (2003) 81-90
59. Wright S.C., Zhong J., Zheng H., and Larrick J.W. Nicotine inhibition of apoptosis suggests a role in tumor promotion. FASEB J. 7 (1993) 1045-1051
60. Wu Y.P., Kita K., and Suzuki N. Involvement of human heat shock protein 90 alpha in nicotine-induced apoptosis. Int. J. Cancer 100 (2002) 37-42
61. Yoshida H., Sakagami H., Yamanaka Y., Amano Y., Yamaguchi M., Yamamura M., Fukuchi K., Gomi K., Ohata H., Momose K., and Takeda M. Induction of DNA fragmentation by nicotine in human myelogenous leukemic cell lines. Anticancer Res. 18 (1998) 2507-2511