Exposure to nicotine adversely affects the dendritic cell system and compromises host response to vaccination

Journal of Immunology

Volumn 188, Issue 5, 2012, Pages 2359-2370

  Nouri Shirazi, Mahyar ^a   Guinet, Elisabeth ^a  

^a FLORIDA ATLANTIC UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADJUVANT; INTERLEUKIN 4; NICOTINE; PROTEIN BASED VACCINE; UNCLASSIFIED DRUG; VACCINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY PRODUCTION; ANTIGEN SPECIFICITY; ARTICLE; CELL DIFFERENTIATION; CELL FUNCTION; CELL ISOLATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; EFFECTOR CELL; IMMUNE RESPONSE; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; TH1 CELL; VACCINATION;

ANIMALS; ANTIBODY FORMATION; CELL LINE, TUMOR; CELL PROLIFERATION; CELLS, CULTURED; COCULTURE TECHNIQUES; DENDRITIC CELLS; EPITOPES, T-LYMPHOCYTE; HUMANS; IMMUNOLOGIC MEMORY; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, TRANSGENIC; NICOTINE; OVALBUMIN; TH1 CELLS; VACCINATION;

EID: 84857479709     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1102552     Document Type: Article

References (77)

1. Ambrosino, D. M., and D. C. Molrine. 1993. Critical appraisal of immunization strategies for prevention of infection in the compromised host. Hematol. Oncol. Clin. North Am. 7: 1027-1050. (Pubitemid 23294241)
2. Kumar, R., and E. A. Burns. 2008. Age-related decline in immunity: implications for vaccine responsiveness. Expert Rev. Vaccines 7: 467-479. (Pubitemid 351681640)
3. Arcavi, L., and N. L. Benowitz. 2004. Cigarette smoking and infection. Arch. Intern. Med. 164: 2206-2216. (Pubitemid 39452980)
4. Kuehn, B. M. 2008. CDC panel recommends vaccine for smokers; reviews HPV safety data. JAMA 300: 2713-2714.
5. Sopori, M. 2002. Effects of cigarette smoke on the immune system. Nat. Rev. Immunol. 2: 372-377. (Pubitemid 37328760)
6. Stämpfli, M. R., and G. P. Anderson. 2009. How cigarette smoke skews immune responses to promote infection, lung disease and cancer. Nat. Rev. Immunol. 9: 377-384.
7. Finklea, J. F., V. Hasselblad, W. B. Riggan, W. C. Nelson, D. I. Hammer, and V. A. Newill. 1971. Cigarette smoking and hemagglutination inhibition response to influenza after natural disease and immunization. Am. Rev. Respir. Dis. 104: 368-376.
8. MacKenzie, J. S., I. H. MacKenzie, and P. G. Holt. 1976. The effect of cigarette smoking on susceptibility to epidemic influenza and on serological responses to live attenuated and killed subunit influenza vaccines. J. Hyg. (Lond.) 77: 409-417.
9. Winter, A. P., E. A. Follett, J. McIntyre, J. Stewart, and I. S. Symington. 1994. Influence of smoking on immunological responses to hepatitis B vaccine. Vaccine 12: 771-772. (Pubitemid 24190555)
10. Rennard, S. I. 2004. Cigarette smoke in research. Am. J. Respir. Cell Mol. Biol. 31: 479-480. (Pubitemid 39463394)
11. Smith, C. J., and C. Hansch. 2000. The relative toxicity of compounds in mainstream cigarette smoke condensate. Food Chem. Toxicol. 38: 637-646. (Pubitemid 30624144)
12. Sopori, M. L., and W. Kozak. 1998. Immunomodulatory effects of cigarette smoke. J. Neuroimmunol. 83: 148-156. (Pubitemid 28280961)
13. Holt, P. G., J. E. Chalmer, L. M. Roberts, J. M. Papadimitriou, W. R. Thomas, and D. Keast. 1976. Low-tar and high-tar cigarettes. Arch. Environ. Health 31: 258-265.
14. Geng, Y., S. M. Savage, L. J. Johnson, J. Seagrave, and M. L. Sopori. 1995. Effects of nicotine on the immune response. I. Chronic exposure to nicotine impairs antigen receptor-mediated signal transduction in lymphocytes. Toxicol. Appl. Pharmacol. 135: 268-278. (Pubitemid 26031878)
15. Geng, Y., S. M. Savage, S. Razani-Boroujerdi, and M. L. Sopori. 1996. Effects of nicotine on the immune response. II. Chronic nicotine treatment induces T cell anergy. J. Immunol. 156: 2384-2390. (Pubitemid 26091561)
16. Steinman, R. M. 1991. The dendritic cell system and its role in immunogenicity. Annu. Rev. Immunol. 9: 271-296.
17. Banchereau, J., F. Briere, C. Caux, J. Davoust, S. Lebecque, Y. J. Liu, B. Pulendran, and K. Palucka. 2000. Immunobiology of dendritic cells. Annu. Rev. Immunol. 18: 767-811. (Pubitemid 30365397)
18. Guinet, E., K. Yoshida, and M. Nouri-Shirazi. 2004. Nicotinic environment affects the differentiation and functional maturation of monocytes derived dendritic cells (DCs). Immunol. Lett. 95: 45-55. (Pubitemid 39119899)
19. Nouri-Shirazi, M., and E. Guinet. 2003. Evidence for the immunosuppressive role of nicotine on human dendritic cell functions. Immunology 109: 365-373. (Pubitemid 36783262)
20. Nouri-Shirazi, M., and E. Guinet. 2006. A possible mechanism linking cigarette smoke to higher incidence of respiratory infection and asthma. Immunol. Lett. 103: 167-176. (Pubitemid 43162932)
21. Nouri-Shirazi, M., R. Tinajero, and E. Guinet. 2007. Nicotine alters the biological activities of developing mouse bone marrow-derived dendritic cells (DCs). Immunol. Lett. 109: 155-164. (Pubitemid 46452751)
22. Zeng, M., E. Guinet, and M. Nouri-Shirazi. 2009. B7-1 and B7-2 differentially control peripheral homeostasis of CD4(+)CD25(+)Foxp3(+) regulatory T cells. Transpl. Immunol. 20: 171-179.
23. Asavaroengchai, W., Y. Kotera, and J. J. Mulé. 2002. Tumor lysate-pulsed dendritic cells can elicit an effective antitumor immune response during early lymphoid recovery. Proc. Natl. Acad. Sci. USA 99: 931-936. (Pubitemid 34106613)
24. Taieb, A., J. J. Breitinger, J. V. Unadkat, W. J. Shufesky, A. E. Morelli, A. W. Thomson, W. P. Lee, and M. Feili-Hariri. 2007. Intrinsic ability of GM+IL-4 but not Flt3L-induced rat dendritic cells to promote allogeneic T cell hyporesponsiveness. Clin. Immunol. 123: 176-189. (Pubitemid 46590068)
25. Paul, W. E., and R. A. Seder. 1994. Lymphocyte responses and cytokines. Cell 76: 241-251. (Pubitemid 24046687)
26. Kaech, S. M., J. T. Tan, E. J. Wherry, B. T. Konieczny, C. D. Surh, and R. Ahmed. 2003. Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nat. Immunol. 4: 1191-1198. (Pubitemid 37540688)
27. Brasel, K., H. J. McKenna, P. J. Morrissey, K. Charrier, A. E. Morris, C. C. Lee, D. E. Williams, and S. D. Lyman. 1996. Hematologic effects of flt3 ligand in vivo in mice. Blood 88: 2004-2012. (Pubitemid 26307902)
28. Maraskovsky, E., K. Brasel, M. Teepe, E. R. Roux, S. D. Lyman, K. Shortman, and H. J. McKenna. 1996. Dramatic increase in the numbers of functionally mature dendritic cells in Flt3 ligand-treated mice: multiple dendritic cell subpopulations identified. J. Exp. Med. 184: 1953-1962. (Pubitemid 26404485)
29. McKenna, H. J., K. L. Stocking, R. E. Miller, K. Brasel, T. De Smedt, E. Maraskovsky, C. R. Maliszewski, D. H. Lynch, J. Smith, B. Pulendran, et al. 2000. Mice lacking flt3 ligand have deficient hematopoiesis affecting hematopoietic progenitor cells, dendritic cells, and natural killer cells. Blood 95: 3489-3497. (Pubitemid 30428482)
30. Chang, E., E. C. Forsberg, J. Wu, Bingyin Wang, S. S. Prohaska, R. Allsopp, I. L. Weissman, and J. P. Cooke. 2010. Cholinergic activation of hematopoietic stem cells: role in tobacco-related disease? Vasc. Med. 15: 375-385.
31. Moore, M. W., F. R. Carbone, and M. J. Bevan. 1988. Introduction of soluble protein into the class I pathway of antigen processing and presentation. Cell 54: 777-785.
32. Bleifuss, E., T. Kammertoens, A. Hutloff, D. Quarcoo, M. Dorner, P. Straub, W. Uckert, and E. Hildt. 2006. The translocation motif of hepatitis B virus improves protein vaccination. Cell. Mol. Life Sci. 63: 627-635.
33. Buonocore, S., N. O. Haddou, F. Moore, S. Florquin, F. Paulart, C. Heirman, K. Thielemans, M. Goldman, and V. Flamand. 2008. Neutrophil-dependent tumor rejection and priming of tumoricidal CD8+ T cell response induced by dendritic cells overexpressing CD95L. J. Leukoc. Biol. 84: 713-720.
34. Galea-Lauri, J., J. W. Wells, D. Darling, P. Harrison, and F. Farzaneh. 2004. Strategies for antigen choice and priming of dendritic cells influence the polarization and efficacy of antitumor T-cell responses in dendritic cell-based cancer vaccination. Cancer Immunol. Immunother. 53: 963-977. (Pubitemid 39371741)
35. Hao, S., O. Bai, J. Yuan, M. Qureshi, and J. Xiang. 2006. Dendritic cell-derived exosomes stimulate stronger CD8+ CTL responses and antitumor immunity than tumor cell-derived exosomes. Cell. Mol. Immunol. 3: 205-211.
36. Johnston, D., B. Zaidi, and J. C. Bystryn. 2007. TLR7 imidazoquinoline ligand 3M-019 is a potent adjuvant for pure protein prototype vaccines. Cancer Immunol. Immunother. 56: 1133-1141. (Pubitemid 46763928)
37. Karan, D., A. M. Krieg, and D. M. Lubaroff. 2007. Paradoxical enhancement of CD8 T cell-dependent anti-tumor protection despite reduced CD8 T cell responses with addition of a TLR9 agonist to a tumor vaccine. Int. J. Cancer 121: 1520-1528. (Pubitemid 47328711)
38. Krishnan, L., S. Sad, G. B. Patel, and G. D. Sprott. 2003. Archaeosomes induce enhanced cytotoxic T lymphocyte responses to entrapped soluble protein in the absence of interleukin 12 and protect against tumor challenge. Cancer Res. 63: 2526-2534. (Pubitemid 36605193)
39. Mizukami, S., C. Kajiwara, H. Ishikawa, I. Katayama, K. Yui, and H. Udono. 2008. Both CD4+ and CD8+ T cell epitopes fused to heat shock cognate protein 70 (hsc70) can function to eradicate tumors. Cancer Sci. 99: 1008-1015. (Pubitemid 351997605)
40. Kellermann, S. A., S. Hudak, E. R. Oldham, Y. J. Liu, and L. M. McEvoy. 1999. The CC chemokine receptor-7 ligands 6Ckine and macrophage inflammatory protein-3 beta are potent chemoattractants for in vitro- and in vivo-derived dendritic cells. J. Immunol. 162: 3859-3864. (Pubitemid 29314763)
41. Robbins, C. S., F. Franco, M. Mouded, M. Cernadas, and S. D. Shapiro. 2008. Cigarette smoke exposure impairs dendritic cell maturation and T cell proliferation in thoracic lymph nodes of mice. J. Immunol. 180: 6623-6628.
42. Feng, Y., Y. Kong, P. F. Barnes, F. F. Huang, P. Klucar, X. Wang, B. Samten, M. Sengupta, B. Machona, R. Donis, et al. 2011. Exposure to cigarette smoke inhibits the pulmonary T-cell response to influenza virus and Mycobacterium tuberculosis. Infect. Immun. 79: 229-237.
43. Pape, K. A., A. Khoruts, A. Mondino, and M. K. Jenkins. 1997. Inflammatory cytokines enhance the in vivo clonal expansion and differentiation of antigen-activated CD4+ T cells. J. Immunol. 159: 591-598. (Pubitemid 127484207)
44. Steinman, R. M., and J. Banchereau. 2007. Taking dendritic cells into medicine. Nature 449: 419-426. (Pubitemid 47509552)
45. Aicher, A., C. Heeschen, M. Mohaupt, J. P. Cooke, A. M. Zeiher, and S. Dimmeler. 2003. Nicotine strongly activates dendritic cell-mediated adaptive immunity: potential role for progression of atherosclerotic lesions. Circulation 107: 604-611. (Pubitemid 36176812)
46. Hughes, D. A., P. L. Haslam, P. J. Townsend, and M. Turner-Warwick. 1985. Numerical and functional alterations in circulatory lymphocytes in cigarette smokers. Clin. Exp. Immunol. 61: 459-466. (Pubitemid 15247775)
47. Vassallo, R., K. Tamada, J. S. Lau, P. R. Kroening, and L. Chen. 2005. Cigarette smoke extract suppresses human dendritic cell function leading to preferential induction of Th-2 priming. J. Immunol. 175: 2684-2691. (Pubitemid 41113884)
48. Zavitz, C. C., G. J. Gaschler, C. S. Robbins, F. M. Botelho, P. G. Cox, and M. R. Stampfli. 2008. Impact of cigarette smoke on T and B cell responsiveness. Cell. Immunol. 253: 38-44.
49. Hallquist, N., A. Hakki, L. Wecker, H. Friedman, and S. Pross. 2000. Differential effects of nicotine and aging on splenocyte proliferation and the production of Th1- versus Th2-type cytokines. Proc. Soc. Exp. Biol. Med. 224: 141-146. (Pubitemid 30439068)
50. Petersen, B. H., L. F. Steimel, and J. T. Callaghan. 1983. Suppression of mitogen- induced lymphocyte transformation in cigarette smokers. Clin. Immunol. Immunopathol. 27: 135-140. (Pubitemid 13120958)
51. Bevan, M. J. 2004. Helping the CD8(+) T-cell response. Nat. Rev. Immunol. 4: 595-602.
52. Obar, J. J., E. R. Jellison, B. S. Sheridan, D. A. Blair, Q. M. Pham, J. M. Zickovich, and L. Lefrançois. 2011. Pathogen-induced inflammatory environment controls effector and memory CD8(+) T cell differentiation. J. Immunol. 187: 4967-4978.
53. Nimmerjahn, F., and J. V. Ravetch. 2005. Divergent immunoglobulin g subclass activity through selective Fc receptor binding. Science 310: 1510-1512. (Pubitemid 41746349)
54. Langenkamp, A., M. Messi, A. Lanzavecchia, and F. Sallusto. 2000. Kinetics of dendritic cell activation: impact on priming of TH1, TH2 and nonpolarized T cells. Nat. Immunol. 1: 311-316.
55. Amsen, D., J. M. Blander, G. R. Lee, K. Tanigaki, T. Honjo, and R. A. Flavell. 2004. Instruction of distinct CD4 T helper cell fates by different notch ligands on antigen-presenting cells. Cell 117: 515-526. (Pubitemid 38610236)
56. Flavell, R. A., S. Sanjabi, S. H. Wrzesinski, and P. Licona-Limón. 2010. The polarization of immune cells in the tumour environment by TGFbeta. Nat. Rev. Immunol. 10: 554-567.
57. Stavnezer, J. 1995. Regulation of antibody production and class switching by TGF-beta. J. Immunol. 155: 1647-1651.
58. Burrows, B., M. Halonen, R. A. Barbee, and M. D. Lebowitz. 1981. The relationship of serum immunoglobulin E to cigarette smoking. Am. Rev. Respir. Dis. 124: 523-525. (Pubitemid 12236671)
59. Ronchetti, R., F. Macri, G. Ciofetta, L. Indinnimeo, R. Cutrera, E. Bonci, G. Antognoni, and F. D. Martinez. 1990. Increased serum IgE and increased prevalence of eosinophilia in 9-year-old children of smoking parents. J. Allergy Clin. Immunol. 86: 400-407. (Pubitemid 20305644)
60. Byron, K. A., G. A. Varigos, and A. M. Wootton. 1994. IL-4 production is increased in cigarette smokers. Clin. Exp. Immunol. 95: 333-336. (Pubitemid 24207149)
61. Blanchet, M. R., E. Israël-Assayag, and Y. Cormier. 2004. Inhibitory effect of nicotine on experimental hypersensitivity pneumonitis in vivo and in vitro. Am. J. Respir. Crit. Care Med. 169: 903-909.
62. Kalra, R., S. P. Singh, J. C. Pena-Philippides, R. J. Langley, S. Razani-Boroujerdi, and M. L. Sopori. 2004. Immunosuppressive and anti-inflammatory effects of nicotine administered by patch in an animal model. Clin. Diagn. Lab. Immunol. 11: 563-568. (Pubitemid 38661424)
63. Murrin, L. C., J. R. Ferrer, W. Y. Zeng, and N. J. Haley. 1987. Nicotine administration to rats: methodological considerations. Life Sci. 40: 1699-1708. (Pubitemid 17055482)
64. Sopori, M. L., W. Kozak, S. M. Savage, Y. Geng, and M. J. Kluger. 1998. Nicotine-induced modulation of T Cell function. Implications for inflammation and infection. Adv. Exp. Med. Biol. 437: 279-289.
65. Singh, S. P., R. Kalra, P. Puttfarcken, A. Kozak, J. Tesfaigzi, and M. L. Sopori. 2000. Acute and chronic nicotine exposures modulate the immune system through different pathways. Toxicol. Appl. Pharmacol. 164: 65-72. (Pubitemid 30198545)
66. Navarro, H. A., P. V. Basta, F. J. Seidler, and T. A. Slotkin. 2003. Short-term adolescent nicotine exposure in rats elicits immediate and delayed deficits in T-lymphocyte function: critical periods, patterns of exposure, dose thresholds. Nicotine Tob. Res. 5: 859-868. (Pubitemid 38029081)
67. Razani-Boroujerdi, S., S. P. Singh, C. Knall, F. F. Hahn, J. C. Peña-Philippides, R. Kalra, R. J. Langley, and M. L. Sopori. 2004. Chronic nicotine inhibits inflammation and promotes influenza infection. Cell. Immunol. 230: 1-9. (Pubitemid 39482356)
68. Benowitz, N. L., A. Hansson, and P. Jacob, III. 2002. Cardiovascular effects of nasal and transdermal nicotine and cigarette smoking. Hypertension 39: 1107-1112. (Pubitemid 34620132)
69. Milhorn, H. T., Jr. 1989. Nicotine dependence. Am. Fam. Physician 39: 214-224.
70. Ebert, R. V., M. E. McNabb, K. T. McCusker, and S. L. Snow. 1983. Amount of nicotine and carbon monoxide inhaled by smokers of low-tar, low-nicotine cigarettes. JAMA 250: 2840-2842. (Pubitemid 14234132)
71. Zevin, S., S. G. Gourlay, and N. L. Benowitz. 1998. Clinical pharmacology of nicotine. Clin. Dermatol. 16: 557-564. (Pubitemid 29372788)
72. Slotkin, T. A. 1998. Fetal nicotine or cocaine exposure: which one is worse? J. Pharmacol. Exp. Ther. 285: 931-945. (Pubitemid 28277888)
73. Trauth, J. A., F. J. Seidler, and T. A. Slotkin. 2000. An animal model of adolescent nicotine exposure: effects on gene expression and macromolecular constituents in rat brain regions. Brain Res. 867: 29-39. (Pubitemid 30317378)
74. Matta, S. G., D. J. Balfour, N. L. Benowitz, R. T. Boyd, J. J. Buccafusco, A. R. Caggiula, C. R. Craig, A. C. Collins, M. I. Damaj, E. C. Donny, et al. 2007. Guidelines on nicotine dose selection for in vivo research. Psychopharmacology (Berl.) 190: 269-319. (Pubitemid 46156883)
75. Kalra, R., S. P. Singh, S. M. Savage, G. L. Finch, and M. L. Sopori. 2000. Effects of cigarette smoke on immune response: chronic exposure to cigarette smoke impairs antigen-mediated signaling in T cells and depletes IP3-sensitive Ca(2+) stores. J. Pharmacol. Exp. Ther. 293: 166-171. (Pubitemid 30180936)
76. Mishra, N. C., J. Rir-Sima-Ah, R. J. Langley, S. P. Singh, J. C. Peña-Philippides, T. Koga, S. Razani-Boroujerdi, J. Hutt, M. Campen, K. C. Kim, et al. 2008. Nicotine primarily suppresses lung Th2 but not goblet cell and muscle cell responses to allergens. J. Immunol. 180: 7655-7663.
77. Hukkanen, J., P. Jacob, III, and N. L. Benowitz. 2005. Metabolism and disposition kinetics of nicotine. Pharmacol. Rev. 57: 79-115. (Pubitemid 40283970)