Ameliorating effects of Nigella sativa oil on aggravation of inflammation, oxidative stress and cytotoxicity induced by smokeless tobacco extract in an allergic asthma model in Wistar rats
Main Article Content
Keywords
Smokeless tobacco, Experimental asthma, Nigella sativa, Airway inflammation, Oxidative stress, Wistar rats
Abstract
Background: The comparison of smokeless tobacco (ST) exposure versus Ovalbumin (Ova) sensitized rats or asthmatic patients has hardly been studied in the literature. Thus, the present study aims to investigate the aggravation of inflammation, exacerbation of asthma, oxidative stress and cytotoxicity induced by ST.
Methods: ST was given at the dose of 40 mg/kg in an allergic asthma model in Wistar rats. Furthermore, the effects of oral administration of Nigella sativa oil (NSO), at a dose of 4 mL/kg/day, were investigated.
Results: The obtained results showed that ST clearly enhanced lung inflammation through interleukin-4 (IL-4) and Nitric oxide (NO) increased production. Actually, ST was found to intensify the oxidative stress state induced by Ova-challenge in rats, which was proven not only by augmenting lipid peroxidation and protein oxidation, but also by altering the non-enzymatic and enzymatic antioxidant status. Furthermore, the aggravation of inflammation and oxidative stress was obviously demonstrated by the histopathological changes observed in lung. In contrast, NSO administration has shown anti-inflammatory effects by reducing IL-4 and NO production, restoring the antioxidant status, reducing lipid peroxidation and improving the histopathological alterations by both protein oxidation and NSO treatment.
Conclusions: Our data have proven that severe concurrent exposure to allergen and ST increases airway inflammation and oxidative stress in previously sensitized rats. They also suggest that the oral NSO treatment could be a promising treatment for asthma.
References
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16. Ellman GL. Tissue sulfhydryl groups. Arch Biochem. 1959;82:70-7.
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22. Zemmouri H, Sekiou O, Ammar S, El Feki A, Messarah M, Boumendjel A. Urtica dioica attenuates ovalbumin-induced inflammation and lipid peroxidation of lung tissues in rat asthma model. Pharm Biol. 2017;55:1561-8.
23. Vliet VD, Nguyen MN, Shigenaga MK, Eiserich JP, Marelich GP, Cross CE. Myeloperoxidase and protein oxidation in cystic fibrosis. Am J Physiol: Lung Cell Mol Physiol. 2000;279: L537-46.
24. Mahut B, Delacourt C, Zerah-Lancner F, De Blic J, Harf A, Delclaux C. Increase in alveolar nitric oxide in the presence of symptoms in childhood asthma. Chest. 2004;125:1012-8.
25. Shahzad M, Yang X, Raza Asim MB, Sun Q, Han Y, Zhang F, et al. Black seed oil ameliorates allergic airway inflammation by inhibiting T-cell proliferation in rats. Pulm Pharmacol Ther. 2009;22:37-43.
26. Jang AS, Choi IS, Jeong TK, Lee KY. The effect of cigarette smoking on the levels of nitric oxide metabolites in the sputum of patients with acute asthma. J Asthma. 2002;39:211-6.
27. Petro TM, Zhang S. The effect of smokeless tobacco extract on murine T cell cytokine production. Immunopharmacology. 1997;36:17-26.
28. Boskabady MH, Keyhanmanesh R, Khameneh S, Doostdar Y, Khakzad MR. Potential immunomodulation effect of the extract of Nigella sativa on ovalbumin sensitized guinea pigs. J Zhejiang Univ Sci B. 2011;12:201-9.
29. Mahmood MS, Gilani AH, Khwaja A, Rashid A, Ashfaq MK. The in vitro effect of aqueous extract of Nigella sativa seeds on nitric oxide production. Phytother Res. 2003;17:921-4.
30. Kujawska M, Ignatowicz E, Murias M, Ewertowska M, Mikołajczyk K, Jodynis-Liebert J. Protective effect of red beetroot against carbon tetrachloride- and N-nitrosodiethylamine induced oxidative stress in rats. J Agric Food Chem. 2009;57:2570-800.
31. Dalle-Donne I, Rossib R, Giustarinib D, Milzania A, Colombo R. Protein carbonyl groups as biomarkers of oxidative stress. Clin Chim Acta. 2003;329:23-38.
32. Ghosh MK, Chattopadhyay DJ, Chatterjee IB, Vitamin C. Prevents oxidative damage. Free Radic Res. 1996;25:173-9.
33. Sitte N. Oxidative damage to proteins. In: von Zglinicki T, editor. Aging at the molecular level. The Netherlands: Kluwer Academic Publishers; 2003. p. 27-45.
34. Bouasla I, Bouasla A, Boumendjel A, Messarah M, Abdennour C, Boulakoud MS, et al. Nigella sativa oil reduces aluminium chloride-induced oxidative injury in liver and erythrocytes of rats. Biol Trace Elem Res. 2014;162:252-61.
35. Mariod AA, Ibrahim RM, Ismail M, Ismail N. Antioxidant activity and phenolic content of phenolic rich fractions obtained from black cumin (Nigella sativa) seedcake. Food Chem. 2009;116:306-12.
36. Rahman I, MacNee W. Lung glutathione and oxidative stress: implications in cigarette smoke-induced airway disease. Am J Physiol: Lung Cell Mol Physiol. 1999;277:1067-88.
37. Cotgreave IA, Johansson U, Moldeus P, Brattsand R. The effect of acute cigarette smoke inhalation on pulmonary and systemic cysteine and glutathione redox states in the rat. Toxicology. 1987;45:203-12.
38. Krishnan N, Muthukrishnan S. Effects of Nigella sativa seed extract on carbon tetrachloride-induced hepatotoxicity in rats. J Acute Med. 2012;2:107-13.
39. Alenzi FQ, Altamimi MA, Kujan O, Tarakji B, Tamimi W, Bagader O, et al. Antioxidant properties of Nigella sativa. J Mol Genet Med. 2013;7:77-82.
40. Heffner JE, Rapine JE. Pulmonary strategies of antioxidant defense. Am Rev Respir Dis. 1989;140:531-54.
41. Ardite E, Peinado VI, Rabinivich RA, Fernandez-Checa JC, Roca J, Barberà JA. Systemic effects of cigarette smoke exposure in the guinea pig. Respir Med. 2006;100:1186-94.
42. Menezes C, Leitemperger J, Toni C, Santi A, Lopes T, Barbosa MB, et al. Comparative study on effects of dietary with diphenyl diselenide on oxidative stress in carp (Cyprinus carpio) and silver catfish (Rhamdia sp.) exposed to herbicide clomazone. Environ Toxicol Pharmacol. 2013;36:706-14.
43. Elia AC, Prearo M, Pacini N, Dorr AJ, Abete MC. Effects of selenium diets on growth, accumulation and antioxidant response in juvenile carp. Ecotoxicol Environ Saf. 2011;74:166-73.
44. Pes TS, Saccol EM, Ourique GM, Londero OP, Gressler LT, Finamor IA, et al. Effect of diets enriched with rutin on blood parameters, oxidative biomarkers and pituitary hormone expression in silver catfish (Rhamdia quelen). Fish Physiol Biochem. 2016;42:321-33.
2. Velayutharaj A, Ramesh R, Niranjan G, Kala C. Biochemical assessment of liver damage in smokeless tobacco users. Int J Curr Res Rev. 2013;5:63-9.
3. Avti PK, Kumar S, Pathak CM, Vaiphei K, Khanduja KL. Smokeless tobacco impairs the antioxidant defense in liver, lung, and kidney of rats. Toxicol Sci. 2006;89:547-53.
4. Abdel-Aziz M, Abass A, Zalata K, Abd Al-Galel T, Allam U, Karrouf G. Effect of dexamethasone and Nigella sativa on inducible nitric oxide synthase in the lungs of a murine model of allergic asthma. Iran J Allergy Asthma Immunol. 2014;13:324-34.
5. Chekchaki N, Khaldi T, Rouibah Z, Rouag M, Sekiou O, Messarah M, et al. Anti-inflammatory and antioxidant effects of two extracts from Pistacia lentiscus in liver and erythrocytes, in an experimental model of asthma. Int J Pharm Sci Rev Res. 2017;42:77-84.
6. Khan M. The translation of the meanings of Sahih Al-Bukhari (Arabic---English), vol. 7. Kingdom of Saudi Arabia: Darussalam Publishers and Distributors: Riyadh; 1997.
7. Aftab A, Asif H, Mohd M, Shah AK, Abul KN, Nasir AS, et al. A review on therapeutic potential of Nigella sativa: a miracle herb. Asian Pac J Trop Biomed. 2013;3:337-52.
8. Moerloose KB, Pauwels RA, Joos GF. Short-term cigarette smoke exposure enhances allergic airway inflammation in mice. Am J Respir Crit Care Med. 2005;172:168-72.
9. Amin B, Hosseinzadeh H. Black cumin (Nigella sativa) and its active constituent, thymoquinone: an overview on the analgesic and anti-inflammatory effects. Planta Med. 2016;82:8-16.
10. Lutterodt H, Luther M, Slavin M, Yin J-J, Parry J, Gao J-M, et al. Fatty acid profile, thymoquinone content, oxidative stability, and antioxidant properties of cold-pressed black cumin seed oils. Food Sci Technol. 2010;43:1409-13.
11. Ramadan MF. Healthy blends of high linoleic sunflower oil with selected cold-pressed oils: functionality, stability and antioxidative characteristics. Ind Crops Prod. 2013;43:65-72.
12. Balaha MF, Tanaka H, Yamashita H, Abdel Rahman MN, Inagaki N. Oral Nigella sativa oil ameliorates ovalbumin-induced bronchial asthma in mice. Int Immunopharmacol. 2012;14:224-31.
13. Temann T, Prasad B, Gallup M, Basbaum C, Ho SB, Flavell RA, et al. A novel role for murine IL-4 in vivo: induction of MUC5AC gene expression and mucin hypersecretion. Am J Respir Cell Mol Biol. 1997;16:471-8.
14. Adias TC, Ajugwo AO, Erhabor TA, Adejumo BI, Azikiwe CC. Effect of sub-lethal doses of smokeless tobacco (snuff) on some haemato rheological parameters using albino Wistar rats. Am J Med Sci Med. 2014;2:54-7.
15. Barkat L, Boumendjel A, Abdennour C, Boulakoud MS, El Feki A, Messarah M. Methidathion-induced hematological, biochemical and hepatohistological alterations in rat: ameliorative effects of selenium and zinc. Afr J Biotechnol. 2015;14:1796-806.
16. Ellman GL. Tissue sulfhydryl groups. Arch Biochem. 1959;82:70-7.
17. Levine RL, Garland D, Oliver CN, Amici A, Climent I, Lenz AG, et al. Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol. 1990;186:464-78.
18. Oswald IP, Wynn TA, Sher A, James SL. Interleukin 10 inhibits macrophage microbicidal activity by blocking the endogenous production of tumor necrosis factor-alpha required as a costimulatory factor for interferon gamma-induced activation. Proc Natl Acad Sci U S A. 1992;89:8676-80.
19. Boumendjel A, Tawk L, Malefijt RW, Boulay V, Yssel H, Pène J. IL-27 induces the production of IgG1 by human B cells. Eur Cytokine Netw. 2006;17:281-9.
20. Bochner BS, Undem BJ, Lichtenstein LM. Immunological aspects of allergic asthma. Annu Rev Immunol. 1994;12:295-335.
21. Mauser PJ, House H, Jones H, Correll G. Pharmacological characterization of the late phase reduction in lung functions and correlations with microvascular leakage and lung edema in allergen-challenged Brown Norway rats. Pulm Pharmacol Ther. 2013;26:677-84.
22. Zemmouri H, Sekiou O, Ammar S, El Feki A, Messarah M, Boumendjel A. Urtica dioica attenuates ovalbumin-induced inflammation and lipid peroxidation of lung tissues in rat asthma model. Pharm Biol. 2017;55:1561-8.
23. Vliet VD, Nguyen MN, Shigenaga MK, Eiserich JP, Marelich GP, Cross CE. Myeloperoxidase and protein oxidation in cystic fibrosis. Am J Physiol: Lung Cell Mol Physiol. 2000;279: L537-46.
24. Mahut B, Delacourt C, Zerah-Lancner F, De Blic J, Harf A, Delclaux C. Increase in alveolar nitric oxide in the presence of symptoms in childhood asthma. Chest. 2004;125:1012-8.
25. Shahzad M, Yang X, Raza Asim MB, Sun Q, Han Y, Zhang F, et al. Black seed oil ameliorates allergic airway inflammation by inhibiting T-cell proliferation in rats. Pulm Pharmacol Ther. 2009;22:37-43.
26. Jang AS, Choi IS, Jeong TK, Lee KY. The effect of cigarette smoking on the levels of nitric oxide metabolites in the sputum of patients with acute asthma. J Asthma. 2002;39:211-6.
27. Petro TM, Zhang S. The effect of smokeless tobacco extract on murine T cell cytokine production. Immunopharmacology. 1997;36:17-26.
28. Boskabady MH, Keyhanmanesh R, Khameneh S, Doostdar Y, Khakzad MR. Potential immunomodulation effect of the extract of Nigella sativa on ovalbumin sensitized guinea pigs. J Zhejiang Univ Sci B. 2011;12:201-9.
29. Mahmood MS, Gilani AH, Khwaja A, Rashid A, Ashfaq MK. The in vitro effect of aqueous extract of Nigella sativa seeds on nitric oxide production. Phytother Res. 2003;17:921-4.
30. Kujawska M, Ignatowicz E, Murias M, Ewertowska M, Mikołajczyk K, Jodynis-Liebert J. Protective effect of red beetroot against carbon tetrachloride- and N-nitrosodiethylamine induced oxidative stress in rats. J Agric Food Chem. 2009;57:2570-800.
31. Dalle-Donne I, Rossib R, Giustarinib D, Milzania A, Colombo R. Protein carbonyl groups as biomarkers of oxidative stress. Clin Chim Acta. 2003;329:23-38.
32. Ghosh MK, Chattopadhyay DJ, Chatterjee IB, Vitamin C. Prevents oxidative damage. Free Radic Res. 1996;25:173-9.
33. Sitte N. Oxidative damage to proteins. In: von Zglinicki T, editor. Aging at the molecular level. The Netherlands: Kluwer Academic Publishers; 2003. p. 27-45.
34. Bouasla I, Bouasla A, Boumendjel A, Messarah M, Abdennour C, Boulakoud MS, et al. Nigella sativa oil reduces aluminium chloride-induced oxidative injury in liver and erythrocytes of rats. Biol Trace Elem Res. 2014;162:252-61.
35. Mariod AA, Ibrahim RM, Ismail M, Ismail N. Antioxidant activity and phenolic content of phenolic rich fractions obtained from black cumin (Nigella sativa) seedcake. Food Chem. 2009;116:306-12.
36. Rahman I, MacNee W. Lung glutathione and oxidative stress: implications in cigarette smoke-induced airway disease. Am J Physiol: Lung Cell Mol Physiol. 1999;277:1067-88.
37. Cotgreave IA, Johansson U, Moldeus P, Brattsand R. The effect of acute cigarette smoke inhalation on pulmonary and systemic cysteine and glutathione redox states in the rat. Toxicology. 1987;45:203-12.
38. Krishnan N, Muthukrishnan S. Effects of Nigella sativa seed extract on carbon tetrachloride-induced hepatotoxicity in rats. J Acute Med. 2012;2:107-13.
39. Alenzi FQ, Altamimi MA, Kujan O, Tarakji B, Tamimi W, Bagader O, et al. Antioxidant properties of Nigella sativa. J Mol Genet Med. 2013;7:77-82.
40. Heffner JE, Rapine JE. Pulmonary strategies of antioxidant defense. Am Rev Respir Dis. 1989;140:531-54.
41. Ardite E, Peinado VI, Rabinivich RA, Fernandez-Checa JC, Roca J, Barberà JA. Systemic effects of cigarette smoke exposure in the guinea pig. Respir Med. 2006;100:1186-94.
42. Menezes C, Leitemperger J, Toni C, Santi A, Lopes T, Barbosa MB, et al. Comparative study on effects of dietary with diphenyl diselenide on oxidative stress in carp (Cyprinus carpio) and silver catfish (Rhamdia sp.) exposed to herbicide clomazone. Environ Toxicol Pharmacol. 2013;36:706-14.
43. Elia AC, Prearo M, Pacini N, Dorr AJ, Abete MC. Effects of selenium diets on growth, accumulation and antioxidant response in juvenile carp. Ecotoxicol Environ Saf. 2011;74:166-73.
44. Pes TS, Saccol EM, Ourique GM, Londero OP, Gressler LT, Finamor IA, et al. Effect of diets enriched with rutin on blood parameters, oxidative biomarkers and pituitary hormone expression in silver catfish (Rhamdia quelen). Fish Physiol Biochem. 2016;42:321-33.
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Khaldi, T., Chekchaki, N., Boumendjel, M., Taibi, F., Abdellaoui, M., Messarah, M., & Boumendjel, A. (2018). Ameliorating effects of Nigella sativa oil on aggravation of inflammation, oxidative stress and cytotoxicity induced by smokeless tobacco extract in an allergic asthma model in Wistar rats. Allergologia Et Immunopathologia, 46(5), 472-481. https://all-imm.com/index.php/aei/article/view/378
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Khaldi, T., Chekchaki, N., Boumendjel, M., Taibi, F., Abdellaoui, M., Messarah, M., & Boumendjel, A. (2018). Ameliorating effects of Nigella sativa oil on aggravation of inflammation, oxidative stress and cytotoxicity induced by smokeless tobacco extract in an allergic asthma model in Wistar rats. Allergologia Et Immunopathologia, 46(5), 472-481. https://all-imm.com/index.php/aei/article/view/378