Effects of Tobacco smoking on immune response: A Review

Debkumar Sahoo; Biplab Mandal; Sudipta Ghorai

doi:10.48001/veethika.2022.08.01.004

Debkumar Sahoo Coastal Ecology Research laboratory, Egra, Pin 721429, Purba Medinipur, West Bengal
Biplab Mandal Department of Zoology, Vidyasagar University, Medinipur, Pin 721102, West Bengal
Sudipta Ghorai Department of Zoology, Egra Sarada Shashi Bhusan College, Egra, Purba Medinipur, West Bengal https://orcid.org/0000-0003-3478-3632

DOI: https://doi.org/10.48001/veethika.2022.08.01.004

Keywords: Chronic obstructive pulmonary disease, free radicals and oxidizing agents, adaptive immune systems, innate immune systems

Abstract

Tobacco smoking causes a variety of illnesses, the most common of which is ''Chronic Obstructive Pulmonary Disease'' (COPD), and has a severe influence on one's health.Tobacco consists of nearly 7000 toxic chemicals, including free radicals and oxidizing agents. The impact of smoking on research is being done on both the innate and adaptive immune responses. Adaptive and innate immune systems affected by smoking include T helper cells, regulatory cells, memory T/B lymphocytes and DCs, macrophages, NK cells, respectively. Smokers are showing highly different values of parameters like several NK cells, cytokines, leukocytes, granulocytes, monocytes etc., from controls. As a result, immunological responses are impeded and cellular and molecular processes are permanently impaired.

Downloads

Download data is not yet available.

References

Ahmed R, Gray D. Immunological memory and protective immunity: understanding their relation. Science. 1996; 272: 54-60.

Arnson Y, Shoenfeld Y, Amital H. Effects of tobacco smoke on immunity, inflammation and autoimmunity. J. Autoimmun. 2010; 34: J258-265.

Barcelo B, Pons J, Ferrer JM, Sauleda J, Fuster A, Agusti AG. Phenotypic characterisation of T-lymphocytes in COPD: abnormal CD4+, CD25+ regulatory T-lymphocyte response to Tobacco smoking. Eur. Respir. J. 2008; 31: 555-562.

Barlow, D. and Durand, V. (2005). Abnormal Psychology: An Integrative Approach. Thomson Wadsworth, Belmont, CA.

Bartal, M. (2005). COPD and tobacco smoke. Monaldi. Arch. Chest. Dis. 63(4): 213- 225.

Bell, S. and Lee, C. (2006). Does timing and sequencing of transitions to adulthood make a difference? Stress, smoking, and physical activity among young Australian women. International Journal of Behavioral Medicine. 13: 265–274.

Beutler, B. (1990). The complex regulation and biology of TNF (cachectin). Crit. Rev. Oncog 2(1): 9-18.

Boirivant M, Fuss IJ, Chu A, Strober W. Oxazolone colitis: A murine model of T helper cell type 2 colitis treatable with antibodies to interleukin 4. J. Exp. Med. 1998; 188:1929-1939.

Brandsma CA, Hylkema MN, Geerlings M, van Geffen WH, Postma DS, Timens W, Kerstjens HA. Increased levels of (class switched) memory B cells in peripheral blood of current smokers. Respir Res. 2009; 10:108.

Calapai G, Caputi AP, Mannucci C, Gregg EO, Pieratti A, Russo GA, Chaudhary N, Puntoni R,Lowe F, McEwan M, Bassi A, Morandi S, Nunziata A. A cross-sectional investigation of biomarkers of risk after a decade of smoking. Inhal. Toxicol. 2009; 21:1138-1143.

Cataldo JK, Prochaska JJ, Glantz SA. Cigarette smoking is a risk factor for Alzheimer's Disease: an analysis controlling for tobacco industry affiliation. J Alzheimers Dis. 2010; 19: 465-480.

Centers for Disease C, Prevention. Annual smoking attributable mortality, years of potential life lost, and economic costs--United States, 1995-1999. MMWR Morb Mortal Wkly Rep. 2002; 51:300-303.

Cesar-Neto JB, Duarte PM, de Oliveira MC, Casati MZ, Tambeli CH, Parada CA, Sallum EA, Nociti FH, Jr. Smoking modulates interferon-gamma expression in the gingival tissue of patients with chronic periodontitis. Eur. J. Oral. Sci. 2006; 114:403-408.

Chang, W. H., Thai, P. , Xu, J. , Yang, D. C. , Wu, R. and Chen, C. H. (2017). Cigarette Smoke Regulates the Competitive Interactions between NRF2 and BACH1 for Heme Oxygenase-1 Induction. Int. J. Mol. Sci. 18(11): 2386.

Chavance M, Perrot JY, Annesi I. Smoking, CD45R0+ (memory), and CD45RA+ (naive) CD4+ T cells. Am Rev Respir Dis. 1993; 148: 237-240.

Chen, Q., Kang, J. and Fu, C. (2018). The independence of and associations among apoptosis, autophagy, and necrosis. Sig. Transduct. Target. Ther. 3: 18.

Chen, Y., McMillan-Ward, E., Kong, J., Israels, S. J. and Gibson, S. B. (2008). Oxidative stress induces autophagic cell death independent of apoptosis in transformed and cancer cells. Cell Death Differ. 15: 171-182.

Chen, Z. H., Kim, H. P., Sciurba, F. C., Lee, S. J., Feghali-Bostwick, C., Stolz, D. B., Dhir, R., Landreneau, R. J., Schuchert, M. J., Yousem, S. A., Nakahira, K., Pilewski, J. M., Lee, J. S., Zhang, Y., Ryter, S. W. and Choi, A. M. (2008). Egr-1 regulates autophagy in cigarette smoke-induced chronic obstructive pulmonary disease. PLoS One. 3: e3316.

Chiappori A, Folli C, Balbi F, Caci E, Riccio AM, De Ferrari L, Melioli G, Braido F, Canonica GW. CD4(+) CD25 (high) CD127(-) regulatory T-cells in COPD: smoke and drugs effect. World Allergy Organ J. 2016; 9: 5.

Church, D. F. and Pryor, W. A. (1985). Freeradical chemistry of cigarette smoke and its toxicological implications. Environ. Health. Perspect. 64: 111-126.

Cullinan, S. B. and Diehl, J. A. (2006). Coordination of ER and oxidative stress signaling: the PERK/Nrf2 signaling pathway. Int J Biochem Cell Biol. 38(3): 317-332.

Dalbey, W. E., Nettesheim, P., Griesemer, R., Caton, J.E. and Guerin, M. R. (1980). Chronic inhalation of cigarette smoke by F344 rats. J. Natl. Cancer Inst. 64: 383-390.

Das, D. and Das, S. (2021). Endocrine Disruptor—A threat to the animal world. International Journal of Experimental Research and Review. 24: 10-23.

Das, M., Chattopadhayay, A. and Basu, R. (2017). Flood hazard and damage assessment in former Jalpaiguri district of West Bengal, India. International Journal of Experimental Research and Review. 11: 43-51.

Dey, S. and Guha, P. (2020). A brief review on cigarette induced cellular damage. International Journal of Experimental Research and Review. 23: 18-26.

Doll R, Peto R, Boreham J, Sutherland I. Mortality in relation to smoking: 50 years' observations on male British doctors. BMJ. 2004; 328:1519.

Duan MC, Tang HJ, Zhong XN, Huang Y. Persistence of Th17/Tc17 Cell Expression upon Smoking Cessation in Mice with Cigarette Smoke-Induced Emphysema. Clin Dev Immunol. 2013; 2013:350727.

Dutton RW, Bradley LM, Swain SL. T cell memory. Annu Rev Immunol. 1998; 16:201-223.

Eliakim R, Karmeli F, Cohen P, Heyman SN, Rachmilewitz D. Dual effect of chronic nicotine administration: augmentation of jejunitis and amelioration of colitis induced by odoacetamide inrats. Int J Colorectal Dis. 2001; 16:14-21.

Ferson, M., Edwards, A., Lind, A., Milton, G. W. and Hersey, P. (1979). Low natural killer-

Forsslund H, Mikko M, Karimi R, Grunewald J, Wheelock AM, Wahlstrom J, Skold CM. Distribution of T-cell subsets in BAL fluid of patients with mild to moderate COPD depends on current smoking status and not airway obstruction. Chest. 2014; 145: 711-722.

Friedrichs B, Neumann U, Schuller J, Peck MJ. Cigarettesmoke-induced priming of neutrophils from smokers and non-smokers for increased oxidative burst response is mediated by TNF-alpha. Toxicol In Vitro. 2014; 28:1249-1258.

Fujino S, Andoh A, Bamba S, Ogawa A, Hata K, Araki Y, Bamba T, Fujiyama Y. Increased expression of interleukin 17 in inflammatory bowel disease. Gut. 2003; 52: 65-70.

Fusby JS, Kassmeier MD, Palmer VL, Perry GA, Anderson DK, Hackfort BT, Alvarez GK, Cullen DM, Akhter MP, Swanson PC. Cigarette smoke-induced effects on bone marrow B- cell subsets and CD4+:CD8+ T-cell ratios are reversed by smoking cessation: influence of bone mass on immune cell response to and recovery from smoke exposure. Inhal Toxicol. 2010; 22:785-796.

Galitovskiy V, Qian J, Chernyavsky AI, Marchenko S, Gindi V, Edwards RA, Grando SA. Cytokine-induced alterations of alpha7 nicotinic receptor in colonic CD4 T cells mediate dichotomous response to nicotine in murine models of Th1/Th17- versus Th2-mediated colitis. J Immunol. 2011; 187:2677-2687.

Giuca MR, Pasini M, Tecco S, Giuca G, Marzo G. Levels of salivary immunoglobulins and periodontal evaluation in smoking patients. BMC Immunol. 2014; 15: 5.

Goncalves RB, Coletta RD, Silverio KG, Benevides L, Casati MZ, da Silva JS, Nociti FH, Jr.Impact of smoking on inflammation: overview of molecular mechanisms. Inflamm Res. 2011; 60:409-424.

Good-Jacobson KL, Tarlinton DM. Multiple routes to B-cell memory. Int Immunol. 2012; 24:403-408.

Hagh LG, Zakavi F, Ansarifar S, Ghasemzadeh O, Solgi G. Association of dental caries and salivary IgA with tobacco smoking. Aust Dent J. 2013; 58:219-223.

Hagiwara E, Takahashi KI, Okubo T, Ohno S, Ueda A, Aoki A, Odagiri S, Ishigatsubo Y. Cigarette smoking depletes cells spontaneously secreting Th(1) cytokines in the human airway. Cytokine. 2001; 14:121-126.

Harrison OJ, Foley J, Bolognese BJ, Long E, 3rd, Podolin PL, Walsh PT. Airway infiltration of CD4+, CCR6+ Th17 type cells associated with chronic cigarette smoke induced airspace enlargement. Immunol Lett. 2008; 121: 13-21.

Hecht, S. S. (1999). Tobacco Smoke Carcinogens and Lung Cancer, JNCI: J. Natl. Cancer Inst. 91 (14): 1194–1210.

Henson, P. M. and Tuder, R. M. (2008). Apoptosis in the lung: induction, clearance and detection. Am J. Physiol. Lung Cell Mol. Physiol. 294(4): L601-11.

Hogg JC, Timens W. The Pathology of Chronic Obstructive Pulmonary Disease. Annual Review of PathologyMechanisms Of Disease. 2009; 4:435-434.

Hou J, Sun YC, Hao Y, Zhuo J, Liu XF, Bai P, Han JY, Zheng XW, Zeng H. Imbalance between subpopulations of regulatory T cells in COPD. Thorax. 2013; 68: 1131-1139.

Hwang, J. W., Chung, S., Sundar, I. K., Yao, H., Arunachalam, G., McBurney, M. W. and Rahman, I. (2010). Cigarette smoke-induced autophagy is regulated by SIRT1-PARP-1-dependentmechanism: implication in pathogenesis of COPD. Arch. Biochem. Biophys. 500: 203-209.

Kaech SM, Wherry EJ, Ahmed R. Effector and memory T-cell differentiation: implications for vaccine development. Nat Rev Immunol. 2002; 2: 251-262.

Kasahara, Y., Tuder, R. M, Cool, C, D,, Lynch, D, A,, Flores, S. C, and Voelkel, N. F. (2001). Endothelial cell death and decreased expression of vascular endothelial growth factor and vascular endothelial growth factor receptor 2 in emphysema. Am. J. Respir. Crit. Care Med. 163: 737–744.

Kelsen, S. G., Duan, X., Ji, R., Perez, O., Liu, C. and Merali, S. (2008). Cigarette smoke induces an unfolded protein response in the human lung: a proteomic approach. Am. J. Respir. Cell Mol. Biol. 38: 541–550.

Kim, H. P., Wang, X., Chen, Z. H., Lee, S. J., Huang, M. H., Wang, Y., Ryter, S. W. and Choi, A. M. (2008). Autophagic proteins regulate cigarette smoke induced apoptosis: protective role of heme oxygenase-1. Autophagy. 4: 887- 895.

Kishimoto, T. (1989). The biology of interleukin-6. Blood. 74: 1-10.

Kitani A, Fuss IJ, Nakamura K, Schwartz OM, Usui T, Strober W. Treatment of experimental (Trinitrobenzene sulfonic acid) colitis by intranasal administration of transforming growth factor (TGF)-beta1 plasmid: TGFbeta1-mediated suppression of T helper cell type 1 response occurs by interleukin (IL)-10 induction and IL-12 receptor beta2 chain downregulation. J Exp. Med. 2000; 192: 41-52.

Koch A, Gaczkowski M, Sturton G, Staib P, Schinkothe T, Klein E, Rubbert A, Bacon K, Wassermann K, Erdmann E. Modification of surface antigens in blood CD8+ T-lymphocytes in COPD: effects of smoking. Eur Respir J. 2007; 29: 42-50.

Kondo M. Lymphoid and myeloid lineage commitment in multipotent hematopoietic progenitors. Immunol Rev. 2010; 238: 37-46.

Lazarus, R. S. and Folkman, S. (1984). Stress, Appraisal and Coping. Springer, New York. Lee J, Taneja V, Vassallo R. Cigarette Smoking and Inflammation: Cellular and Molecular Mechanisms. J Dent Res. 2012; 91:142-149.

Leigh, N. J., Palumbo, M. N. and Marino, A. M. (2018). Tobacco-specific nitrosamines (TSNA) in heated tobacco product IQOS. Tobacco Control. 27: s37-s38.

Li G, Wulan H, Song ZC, Paik PA, Tsao ML, Goodman GM, MacEachern PT, Downey RS, Jankowska AJ, Rabinowitz YM, Learch TB, Song DZ, Yuan JJ, Zheng SH, Zheng ZD. Regulatory B Cell Function Is Suppressed by Smoking and Obesity in H-pylori-Infected Subjects and Is Correlated with Elevated Risk of Gastric Cancer. PLoS One. 2015; 10:e0134591.

MacNee, W. (2005). Pulmonary and systemic oxidant/antioxidant imbalance in chronic obstructive pulmonary disease. Proc. Am. Thorac Soc. 2(1): 50-60.

Maeno T, Houghton AM, Quintero PA, Grumelli S, Owen CA, Shapiro SD. CD8(+) T cells are required for inflammation and destruction in cigarette smoke-induced emphysema in mice. J Immunol. 2007; 178:8090-8096.

Mainali P, Pant S, Rodriguez AP, Deshmukh A, Mehta JL. Tobacco and cardiovascular health. Cardiovasc Toxicol. 2015; 15:107-116.

Maiti, M. and Samanta, G. C. (2018). Relationship between physical activity and smoking behavior among college students. International Journal of Experimental Research and Review. 15: 39-43.

Masdottir, B., Jónsson, T., Manfredsdottir, V., Víkingsson, A., Brekkan, A. and Valdimarsson, H. (2000). Smoking, rheumatoid factor isotypes and severity of rheumatoid arthritis. Rheumatol. (Oxford) 39: 1202-1205.

Mathews, J. D., Whittingham, S., Hooper, B. M., Mackay, I. R. and Stenhouse, N. S. (1973). Association of autoantibodies with smoking, cardiovascular morbidity, and death in the Busselton population. Lancet. 2: 754-758.

Meuronen A, Majuri ML, Alenius H, Mantyla T, Wolff H, Piirila P, Laitinen A. Decreased cytokine and chemokine mRNA expression in bronchoalveolar lavage in asymptomatic smoking subjects. Respiration. 2008; 75:450-458.

Mishra, A., Chaturvedi, P., Datta, S., Sinukumar, S., Joshi, P., Garg, A. (2005). Harmful effects of nicotine. Indian J. Med. Paediatr. Oncol. 36(1): 24-31.

Mitchell, R. S., Vincent, T. N. and Filley, G. F. (1964). Cigarette Smoking, Chronic Bronchitis, and Emphysema. JAMA. 188(1): 12–16.

Miyara M, Yoshioka Y, Kitoh A, Shima T, Wing K, Niwa A, Parizot C, Taflin C, Heike T, Valeyre D, Mathian A, Nakahata T, Yamaguchi T, Nomura T, Ono M, Amoura Z, et al. Functional delineation and differentiation dynamics of human CD4+ T cells expressing the FoxP3 transcription factor. Immunity. 2009; 30: 899-911.

Montbarbon M, Pichavant M, Langlois A, Erdual E, Maggiotto F, Neut C, Mallevaey T, Dharancy S, Dubuquoy L, Trottein F, Cortot A, Desreumaux P, Gosset P, Bertin B. Colonic Inflammation in Mice Is Improved by Cigarette Smoke through iNKT Cells Recruitment. PLoS One. 2013; 8:e62208.

Moreira DM, Nickel JC, Gerber L, Muller RL, Andriole GL, Castro-Santamaria R, Freedland SJ. Smoking Is Associated with Acute and Chronic Prostatic Inflammation: Results from the REDUCE Study. Cancer Prevention Research. 2015; 8:312-317.

Nadigel J, Prefontaine D, Baglole CJ, Maltais F, Bourbeau J, Eidelman DH, Hamid Q. Cigarette smoke increases TLR4 and TLR9 expression and induces cytokine production from CD8(+) T cells in chronic obstructive pulmonary disease. Respir Res. 2011; 12:149.

Nakamura Y, Miyata M, Ohba T, Ando T, Hatsushika K, Suenaga F, Shimokawa N, Ohnuma Y, Katoh R, Ogawa H, Nakao A. Cigarette smoke extract induces thymic stromal lymphopoietin expression, leading to T(H)2-type immune responses and airway inflammation. J Allergy Clin Immunol. 2008; 122:1208-1214.

Namujju PB, Pajunen E, Simen-Kapeu A, Hedman L, Merikukka M, Surcel HM, Kirnbauer R, Apter D, Paavonen J, Hedman K, Lehtinen M. Impact of smoking on the quantity and quality of antibodies induced by human papillomavirus type 16 and 18 AS04-adjuvanted virus-like- particle vaccine - a pilot study. BMC Res Notes. 2014; 7:445.

Nguyen NT, Nakahama T, Kishimoto T. Aryl hydrocarbon receptor and experimental autoimmune arthritis. Semin Immunopathol. 2013; 35:637-644.

Nyunoya, T., Monick, M. M., Klingelhutz, A., Yarovinsky, T. O., Cagley, J. R. and Hunninghake, G. W. (2006). Cigarette smoke induces cellular senescence. Am. J. Respir. Cell Mol. Biol. 35(6): 681-688.

Onozaki K. Etiological and biological aspects of cigarette smoking in rheumatoid arthritis. Inflamm Allergy Drug Targets. 2009; 8:364-368.

Palmer VL, Kassmeier MD, Willcockson J, Akhter MP, Cullen DM, Swanson PC. N- acetylcysteine increases the frequency of bone marrow pro-B/pre-B cells, but does not reverse cigarette smoking-induced loss of this subset. PLoS One. 2011; 6:e24804.

Papathanasiou, G., Papandreou, M., Galanos, A., Kortianou, E., Tsepis, E., Kalfakakou, V. and Kalfakakou, A. (2012). Smoking and Physical Activity Interrelations in Health Science Students. Is Smoking Associated with Physical Inactivity in Young Adults? Hellenic. J. Cardiol. 53: 17-25.

Parkes GC, Whelan K, Lindsay JO. Smoking in inflammatory bowel disease: Impact on disease course and insights into the aetiology of its effect. Journal Of Crohns & Colitis. 2014; 8:717- 725.

Perricone C, Versini M, Ben-Ami D, Gertel S, Watad A, Segel MJ, Ceccarelli F, Conti F, Cantarini L, Bogdanos DP, Antonelli A, Amital H, Valesini G, Shoenfeld Y. Smoke and autoimmunity: The fire behind the disease. Autoimmun Rev. 2016; 15:354-374.

Petrache, I., Natarajan, V., Zhen, L., Medler, T . R., Richter, A. T., Cho, C., Hubbard, W. C., Berdyshev, E. V. and Tuder, R. M. (2005). Ceramide upregulation causes pulmonary cell apoptosis and emphysema-like disease in mice. Nat. Med. 11: 491-498.

Pramanik, B. (2018). A comparative study on the knowledge, attitude and risk perception regarding complications of type-2 diabetes mellitus between male and female diabetic patients attending diabetic clinics in selected hospital of West Bengal, India. International Journal of Experimental Research and Review. 15: 16-27.

Prueitt RL, Wallace TA, Glynn SA, Yi M, Tang W, Luo J, Dorsey TH, Stagliano KE, Gillespie JW, Hudson RS, Terunuma A, Shoe JL, Haines DC, Yfantis HG, Han M, Martin DN, et al. An Immune-Inflammation Gene Expression Signature in Prostate Tumors of Smokers. Cancer Res. 2016; 76:1055-1065.

Qin S, Cobbold SP, Pope H, Elliott J, Kioussis D, Davies J, Waldmann H. “Infectious” transplantation tolerance. Science. 1993; 259:974-977.

Qiu. F, Liang, C. L., Liu, H., Zeng, Y. Q., Hou, S., Huang, S., Lai, X. and Dai, Z. (2017). Impacts of cigarette smoking on immune responsiveness: Up and down or upside down? Oncotarget. 8(1): 268- 284.

Rahman, I. and MacNee, W. (1996) Oxidant/antioxidant imbalance in smokers and chronic obstructive pulmonary disease. Thorax. 51: 348- 350.

Raphael I, Nalawade S, Eagar TN, Forsthuber TG. T cell subsets and their signature cytokines in autoimmune and inflammatory diseases. Cytokine. 2015; 74:5-17.

Rennard SI. Cigarette smoke in research. Am J Respir Cell Mol Biol. 2004; 31:479-480.

Reynolds, H. Y. (1987) Bronchoalveolar lavage. Am. Rev. Respir. Dis. 135: 250-263.

Ridner, S. H. (2004). Psychological distress: concept analysis. Journal of Advanced Nursing. 45: 536–545.

Roos-Engstrand E, Ekstrand-Hammarstrom B, Pourazar J, Behndig AF, Bucht A, Blomberg A. Influence of smoking cessation on airway T lymphocyte subsets in COPD. COPD. 2009; 6:112-120.

Rubin DT, Hanauer SB. Smoking and inflammatory bowel disease. Eur J Gastroenterol Hepatol. 2000; 12:855-862.

Rutgers, S. R., Timens, W., Kauffman, H. F. and Postma, D. S.. (2001). Markers of active airway inflammation and remodelling in chronic obstructive pulmonary disease. Clin Exp Allergy. 31(2): 193-205.

Ryter, S. W. and Choi, A. M. (2010). Autophagy in the lung. Proc. Am. Thorac. Soc. 7: 13-21.

Saetta M, Di Stefano A, Turato G, Facchini FM, Corbino L, Mapp CE, Maestrelli P, Ciaccia A, Fabbri LM. CD8+ T-lymphocytes in peripheral airways of smokers with chronic obstructive pulmonary disease. Am J Respir Crit Care Med. 1998; 157:822-826.

Saha, S. P., Bhalla, D. K., Whayne, T. F. Jr. and Gairola, C. (2007). Cigarette smoke and adverse health effects: An overview of research trends and future needs. Int. J. Angiol. 16(3): 77-83. Sander L, Gilman, Xun Z. Smoke: A Global History of Smoking. London: Reaktion Books. 2004.

Sakaguchi S, Sakaguchi N, Asano M, Itoh M, Toda M. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25): Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J Immunol. 1995;155: 1151-1164.

Sarkar, S. (2016). Livelihood Strategies of Street children using the urban space: A case study at Sealdah station area, Kolkata. International Journal of Experimental Research and Review. 7: 44-52.

Sartor RB. Mechanisms of disease: pathogenesis of Crohn's disease and ulcerative colitis. Nat Clin Pract Gastroenterol Hepatol. 2006; 3: 390-407.

Schmidt C, Giese T, Ludwig B, Mueller-Molaian I, Marth T, Zeuzem S, Meuer SC, Stallmach A. Expression of interleukin-12-related cytokine transcripts in inflammatory bowel disease: Elevated interleukin-23p19 and interleukin27p28 in Crohn's disease but not in ulcerative colitis. Inflamm Bowel Dis. 2005; 11:16-23.

Shan M, Yuan X, Song LZ, Roberts L, Zarinkamar N, Seryshev A, Zhang Y, Hilsenbeck S, Chang SH, Dong C, Corry DB, Kheradm and F. Cigarette smoke induction of osteopontin (SPP1) mediates T(H)17 inflammation in human and experimental emphysema. Sci Transl Med. 2012; 4: 117ra119.

Shintani, T. and Klionsky, D. J. (2004) Autophagy in health and disease: a double-edgedsword. Science. 306: 990- 995.

Singh SP, Gundavarapu S, Pena-Philippides JC, Rir-sima-ah J, Mishra NC, Wilder JA, Langley RJ, Smith KR, Sopori ML. Prenatal Secondhand Cigarette Smoke Promotes Th2 Polarization and Impairs Goblet Cell Differentiation and Airway Mucus Formation. J Immunol. 2011; 187:4542-4552.

Skok MV, Kalashnik EN, Koval LN, Tsetlin VI, Utkin YN, Changeux JP, Grailhe R. Functional nicotinic acetylcholine receptors are expressed in B lymphocyte-derived cell lines. Mol Pharmacol. 2003; 64: 885-889.

Slebos, D. J., Ryter, S. W., van der Toorn, M. Liu, F., Guo, F., Baty, C. J., Karlsson, J. M.,Watkins, S. C., Kim, H. P., Wang, X., Lee, J. S., Postma, D. S., Kauffman, H. F. and Choi, A. M. K. (2007). Mitochondrial localization and function of heme oxygenase-1 in cigarette smoke induced cell death. Am. J. Respir. Cell Mol. Biol. 36(4): 409-417.

Smyth LJ, Starkey C, Vestbo J, Singh D. CD4-regulatory cells in COPD patients. Chest. 2007; 132:156-163.

Sopori, M. (2002) Effects of cigarette smoke on the immune system. Nat. Rev. Immunol. 2: 372-377.

Stepanov, I. and Hecht, S. S. (2005). Tobacco Specific Nitrosamines and Their Pyridine-N- glucuronides in the Urine of Smokers and Smokeless Tobacco Cancer Epidemiol. Biomarkers Prev. 14(4): 885-891.

Sun Z, Xiao Z. 4-(Methylnitrosamino)-1-(3-pyridyl)-1- butanone (NNK) regulates CTL activation and memory programming. Biochem Biophys Res Commun. 2013; 435:472-476.

Takeuchi, M., Nagai, S., Nakajima, A., Shinya, M., Tsukano, C., Asada, H., Yoshikawa, K., Yoshimura, M. and Izumi, T. (2001). Inhibition of lung natural killer cell activity by smoking: the role of alveolar macrophages. Respiration. 68: 262–267.

Talhout R, Schulz T, Florek E, van Benthem J, Wester P, Opperhuizen A. Hazardous compounds in tobacco smoke. Int J Environ Res Public Health. 2011; 8:613-628.

Tanigawa T, Araki S, Nakata A, Kitamura F, Yasumoto M, Sakurai S, Kiuchi T. Increase in memory (CD4+, CD29+ and CD4+, CD45, RO+) T and naive (CD4+, CD45, RA+) T-cell subpopulations in smokers. Arch Environ Health. 1998; 53:378-383.

Thomson, N. C., Chaudhuri, R. and Livingston, E. (2004). Asthma and cigarette smoking. Eur. Resp. J. 24 (5): 822-833.

Thorburn, A. (2008). Apoptosis and autophagy: regulatory connections between two supposedly different processes. Apoptosis. 13(1): 1-9.

Torii K, Saito C, Furuhashi T, Nishioka A, Shintani Y, Kawashima K, Kato H, Morita A. Tobacco smoke is related to Th17 generation with clinical implications for psoriasis patients. Exp Dermatol. 2011; 20:371-373.

Touyz, R. M., Rios, F. J., Alves-Lopes, R., Neves, K. B., Camargo, L. L. and Montezano, A. C. (2020). Oxidative Stress: A Unifying Paradigm in Hypertension. Can. J. Cardiol. 36(5): 659– 670.

Tuder, R. M., Petrache, I., Elias, J. A., Voelkel, N. F. and Henson, P. M. (2003). Apoptosis andemphysema: the missing link. Am. J. Respir. Cell. Mol. Biol. 28: 551-554.

Van Hove CL, Moerloose K, Maes T, Joos GF, Tournoy KG. Cigarette smoke enhances Th-2 driven airway inflammation and delays inhalational tolerance. Respir Res. 2008; 9: 42.

Vardavas CI, Plada M, Tzatzarakis M, Marcos A, Warnberg J, Gomez-Martinez S, Breidenassel C, Gonzalez-Gross M, Tsatsakis AM, Saris WH, Moreno LA, Kafatos AG, Group HHS. Passive smoking alters circulating naive/memory lymphocyte T-cell subpopulations in children. Pediatr Allergy Immunol. 2010; 21:1171-1178.

Vargas-Rojas MI, Ramirez-Venegas A, Limon-Camacho L, Ochoa L, Hernandez-Zenteno R, Sansores RH. Increase of Th17 cells in peripheral blood of patients with chronic obstructive pulmonary disease. Respir Med. 2011; 105:1648-1654.

Wan F, Dai H, Zhang S, Moore Y, Wan N, Dai Z. Cigarette smoke exposure hinders long-term allograft survival by suppressing indoleamine 2, 3-dioxygenase expression. Am J Transplant. 2012; 12:610-619.

Wang H, Peng W, Weng Y, Ying H, Li H, Xia D, Yu W. Imbalance of Th17/Treg cells in mice with chronic cigarette smoke exposure. Int Immuno-pharmacol. 2012; 14:504-512.

Warren GW, Cummings KM. Tobacco and lung cancer: risks, trends, and outcomes in patients with cancer. Am Soc Clin Oncol Educ Book. 2013: 359-364.

Wichianson, J. R., Bughi, S. A., Unger, J. B., Spruijt-Metz, D. and Nguyen-Rodriguez, S. T. (2009). Perceived stress, coping and night-eating in college students. Stress Health. 25: 235–240.

World Health Organization (WHO) (2011). World Health Report on Reducing Risks and Promoting Healthy Life.

World Health Organization (WHO). (2008). Report on the Global Tobacco Epidemic.

Yen D, Cheung J, Scheerens H, Poulet F, McClanahan T, Mckenzie B, Kleinschek MA, Owyang A, Mattson J, Blumenschein W, Murphy E, Sathe M, Cua DJ, Kastelein RA, Rennick D. 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.

Yoshida, T. and Tuder, R. M. (2007). Pathobiology of cigarette smokeinduced chronic obstructive pulmonary disease. Physiol. Rev. 87(3): 1047-1082.

Yu MQ, Liu XS, Wang JM, Xu YJ. CD8(+) Tc-lymphocytes immunodeviation in peripheral blood and airway from patients of chronic obstructive pulmonary disease and changes after short-term smoking cessation. Chin Med J. 2013; 126:3608-3615.

Zhang MQ, Wan Y, Jin Y, Xin JB, Zhang JC, Xiong XZ, Chen L, Chen G. Cigarette smoking promotes inflammation in patients with COPD by affecting the polarization and survival of Th/Tregs through up-regulation of muscarinic receptor 3 and 5 expression. PLoS One. 2014; 9:e112350.

Zhou HB, Hua W, Jin Y, Zhang C, Che LQ, Xia LX, Zhou JS, Chen ZH, Li W, Shen HH. Tc17 cells are associated with cigarette smoke-induced lung inflammation and emphysema. Respirology. 2015; 20:426-433.