Fish oil blunted nicotine-induced vascular endothelial abnormalities possibly via activation of PPARγ-eNOS-NO Signals

Cardiovascular Toxicology

Volumn 13, Issue 2, 2013, Pages 110-122

  Taneja, Gaurav ^a   Mahadevan, Nanjaian ^a   Balakumar, Pitchai ^a  

^a Rajendra Institute of Technology and Sciences   (India)

Author keywords

Endothelial dysfunction; eNOS; Fish oil; Nicotine; Nitric oxide; PPAR

Indexed keywords

2 CHLORO 5 NITROBENZANILIDE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; FISH OIL; N(G) NITROARGININE METHYL ESTER; NICOTINE; NITRATE; NITRIC OXIDE; NITRITE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; SUPEROXIDE; THIOBARBITURIC ACID REACTIVE SUBSTANCE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; ARTICLE; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; ENDOTHELIAL DYSFUNCTION; FEMALE; MALE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; THORACIC AORTA; VASCULAR ENDOTHELIUM; VASODILATATION;

ACETYLCHOLINE; ANILIDES; ANIMALS; AORTA, THORACIC; ENDOTHELIUM, VASCULAR; FEMALE; FISH OILS; MALE; MICROSCOPY, ELECTRON, SCANNING; NICOTINE; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; OXIDATIVE STRESS; PPAR GAMMA; RATS; RATS, WISTAR; TISSUE CULTURE TECHNIQUES; VASODILATION;

RATTUS;

EID: 84880725368     PISSN: 15307905     EISSN: 15590259     Source Type: Journal    
DOI: 10.1007/s12012-012-9190-y     Document Type: Article

References (59)

1. Furchgott, R. F.; & Zawadzki, J. V. (1980). The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine. Nature, 288, 373-376. (Pubitemid 11169009)
2. Furchgott, R. F.; & Vanhoutte, P. M. (1989). Endothelium-derived relaxing and contracting factors. FASEB Journal, 3, 2007-2018. (Pubitemid 19187609)
3. Aird, W. C. (2007). Phenotypic heterogeneity of the endothelium: I. Structure, function, and mechanisms. Circulation Research, 100, 158-173. (Pubitemid 46208717)
4. Andrew, P. J.; & Mayer, B. (1999). Enzymatic function of nitric oxide synthases. Cardiovascular Research, 43, 521-531. (Pubitemid 29369251)
5. Balakumar, P.; Kaur, T.; & Singh, M. (2008). Potential target sites to modulate vascular endothelial dysfunction: Current perspectives and future directions. Toxicology, 245, 49-64.
6. Gkaliagkousi, E.; & Ferro, A. (2011). Nitric oxide signalling in the regulation of cardiovascular and platelet function. Frontiers in Bioscience, 16, 1873-1897.
7. Laursen, J. B.; Boesgaard, S.; Trautner, S.; Rubin, I.; Poulsen, H. E.; & Aldershvile, J. (2001). Endothelium-dependent vasorelaxation in inhibited by in vivo depletion of vascular thiol levels: Role of endothelial nitric oxide synthase. Free Radical Research, 35, 387-394. (Pubitemid 32894357)
8. Montezano, A. C.; & Touyz, R. M. (2012). Reactive oxygen species and endothelial function - Role of NOS uncoupling and Nox family NADPH oxidases. Basic & Clinical Pharmacology & Toxicology, 110, 87-94.
9. Youn, J. Y.; Gao, L.; & Cai, H. (2012). The p47(phox)- and NADPH oxidase organiser 1 (NOXO1)-dependent activation of NADPH oxidase 1 (NOX1) mediates endothelial nitric oxide synthase (eNOS) uncoupling and endothelial dysfunction in a streptozotocin-induced murine model of diabetes. Diabetologia. doi: 10.1007/s00125-012-2557-6.
10. Vanhoutte, P. M. (1997). Endothelial dysfunction and atherosclerosis. European Heart Journal, 18, E19-E29. (Pubitemid 27477910)
11. Puddu, P.; Puddu, G. M.; Zaca, F.; & Muscari, A. (2000). Endothelial dysfunction in hypertension. Acta Cardiologica, 55, 221-232.
12. Kinlay, S.; & Ganz, P. (1997). Role of endothelial dysfunction in coronary artery disease and implications for therapy. American Journal of Cardiology, 80, 11I-16I. (Pubitemid 27490822)
13. Neunteufl, T.; Heher, S.; Kostner, K.; Mitulovic, G.; Lehr, S.; Khoschsorur, G.; et al. (2002). Contribution of nicotine to acute endothelial dysfunction in long-term smokers. Journal of the American College of Cardiology, 39, 251-256. (Pubitemid 34084630)
14. Catanzaro, D. F.; Zhou, Y.; Chen, R.; Yu, F.; Catanzaro, S. E.; De Lorenzo, M. S.; et al. (2007). Potentially reduced exposure cigarettes accelerate atherosclerosis: Evidence for the role of nicotine. Cardiovascular Toxicology, 7, 192-201. (Pubitemid 47575004)
15. Gupta, B. K.; Kaushik, A.; Panwar, R. B.; Chaddha, V. S.; Nayak, K. C.; Singh, V. B.; et al. (2007). Cardiovascular risk factors in tobacco-chewers: A controlled study. Journal of the Association of Physicians of India, 55, 27-31.
16. Mercado, C.; & Jaimes, E. A. (2007). Cigarette smoking as a risk factor for atherosclerosis and renal disease: Novel pathogenic insights. Current Hypertension Reports, 9, 66-72. (Pubitemid 46546700)
17. Timothy, C. O.; & Nneli, R. (2007). The effects of cigarette smoking on intraocular pressure and arterial blood pressure of normotensive young Nigerian male adults. Nigerian Journal of Physiological Sciences, 22, 33-36.
18. Kaur, J.; Reddy, K.; & Balakumar, P. (2010). The novel role of fenofibrate in preventing nicotine- and sodium arsenite-induced vascular endothelial dysfunction in the rat. Cardiovascular Toxicology, 10, 227-238.
19. Luo, H. L.; Zang, W. J.; Lu, J.; Yu, X. J.; Lin, Y. X.; & Cao, Y. X. (2006). The protective effect of captopril on nicotine-induced endothelial dysfunction in rat. Basic & Clinical Pharmacology & Toxicology, 99, 237-245. (Pubitemid 44289745)
20. Rodella, L. F.; Favero, G.; Rossini, C.; Foglio, E.; Reiter, R. J.; & Rezzani, R. (2010). Endothelin-1 as a potential marker of melatonin's therapeutic effects in smoking-induced vasculopathy. Life Sciences, 87, 558-564.
21. Celermajer, D. S.; Sorensen, K. E.; Georgakopoulos, D.; Bull, C.; Thomas, O.; Robinson, J.; et al. (1993). Cigarette smoking is associated with dose-related and potentially reversible impairment of endothelium-dependent dilation in healthy young adults. Circulation, 88, 2149-2155. (Pubitemid 23326094)
22. Giannini, D.; Leone, A.; Di Bisceglie, D.; Nuti, M.; Strata, G.; Buttitta, F.; et al. (2007). The effects of acute passive smoke exposure on endothelium-dependent brachial artery dilation in healthy individuals. Angiology, 58, 211-217. (Pubitemid 46669110)
23. Stone, N. J. (1996). Fish consumption, fish oil, lipids, and coronary heart disease. Circulation, 94, 2337-2340. (Pubitemid 26360549)
24. Warude, D.; Joshi, K.; & Harsulkar, A. (2006). Polyunsaturated fatty acids: Biotechnology. Critical Reviews in Biotechnology, 26, 83-93. (Pubitemid 43995261)
25. Balakumar, P.; & Taneja, G. (2012). Fish oil and vascular endothelial protection: Bench-to-bedside. Free Radical Biology & Medicine, 53, 271-279.
26. Nyby, M. D.; Matsumoto, K.; Yamamoto, K.; Abedi, K.; Eslami, P.; Hernandez, G.; et al. (2005). Dietary fish oil prevents vascular dysfunction and oxidative stress in hyperinsulinemic rats. American Journal of Hypertension, 18, 213-239. (Pubitemid 40332551)
27. McVeigh, G. E.; Brennan, G. M.; Johnston, G. D.; McDermott, B. J.; McGrath, L. T.; Henry, W. R.; et al. (1993). Dietary fish oil augments nitric oxide production or release in patients with type 2 (non-insulin-dependent) diabetes mellitus. Diabetologia, 36, 33-38. (Pubitemid 23018332)
28. Casós, K.; Zaragozá, M. C.; Zarkovic, N.; Zarkovic, K.; Andrisic, L.; Portero-Otín, M.; et al. (2010). A fish-oil-rich diet reduces vascular oxidative stress in apoE(-/-) mice. Free Radical Research, 44, 821-829.
29. Erdogan, H.; Fadillioglu, E.; Ozgocmen, S.; Sogut, S.; Ozyurt, B.; Akyol, O.; et al. (2004). Effect of fish oil supplementation on plasma oxidant/antioxidant status in rats. Prostaglandins Leukotrienes and Essential Fatty Acids, 71, 149-152. (Pubitemid 38903059)
30. Fahs, C. A.; Yan, H.; Ranadive, S.; Rossow, L. M.; Agiovlasitis, S.; Wilund, K. R.; et al. (2010). The effect of acute fish-oil supplementation on endothelial function and arterial stiffness following a high-fat meal. Applied Physiology, Nutrition and Metabolism, 35, 294-302.
31. Cho, D. H.; Choi, Y. J.; Jo, S. A.; & Jo, I. (2004). Nitric oxide production and regulation of endothelial nitric-oxide synthase phosphorylation by prolonged treatment with troglitazone: Evidence for involvement of peroxisome proliferator-activated receptor (PPAR) gamma-dependent and PPARgamma- independent signaling pathways. Journal of Biological Chemistry, 279, 2499-2506. (Pubitemid 38114233)
32. Polikandriotis, J. A.; Mazzella, L. J.; Rupnow, H. L.; & Hart, C. M. (2005). Peroxisome proliferator-activated receptor gamma ligands stimulate endothelial nitric oxide production through distinct peroxisome proliferator-activated receptor gamma-dependent mechanisms. Arteriosclerosis, Thrombosis, and Vascular Biology, 25, 1810-1816. (Pubitemid 41243447)
33. Wong, W. T.; Tian, X. Y.; Xu, A.; Yu, J.; Lau, C. W.; Hoo, R. L.; et al. (2011). Adiponectin is required for PPARγ-mediated improvement of endothelial function in diabetic mice. Cell Metabolism, 14, 104-115.
34. Yuen, C. Y.; Wong, W. T.; Tian, X. Y.; Wong, S. L.; Lau, C. W.; & Yu, J. (2011). Telmisartan inhibits vasoconstriction via PPARγ-dependent expression and activation of endothelial nitric oxide synthase. Cardiovascular Research, 90, 122-129.
35. Zhao, Z.; Luo, Z.; Wang, P.; Sun, J.; Yu, H.; Cao, T.; et al. (2011). Rosiglitazone restores endothelial eysfunction in a rat model of metabolic syndrome through PPARγ- and PPARδ-dependent phosphorylation of Akt and eNOS. PPAR Research, 2011, 291656.
36. Balakumar, P.; Kathuria, S.; Taneja, G.; Kalra, S.; & Mahadevan, N. (2012). Is targeting eNOS a key mechanistic insight of cardiovascular defensive potentials of statins? Journal of Molecular and Cellular Cardiology, 52, 83-92.
37. Balakumar, P.; & Kathuria, S. (2012). Submaximal PPARγ activation and endothelial dysfunction: new perspectives for the management of cardiovascular disorders. British Journal of Pharmacology, 166, 1981-1992.
38. Balakumar, P.; & Mahadevan, N. (2012). Interplay between statins and PPARs in improving cardiovascular outcomes: a double-edged sword? British Journal of Pharmacology, 165, 373-379.
39. Kleinhenz, J. M.; Kleinhenz, D. J.; You, S.; Ritzenthaler, J. D.; Hansen, J. M.; Archer, D. R.; et al. (2009). Disruption of endothelial peroxisome proliferator-activated receptor-gamma reduces vascular nitric oxide production. American Journal of Physiology: Heart and Circulatory Physiology, 297, H1647-H1654.
40. Calnek, D. S.; Mazzella, L.; Roser, S.; Roman, J.; & Hart, C. M. (2003). Peroxisome proliferator-activated receptor gamma ligands increase release of nitric oxide from endothelial cells. Arteriosclerosis, Thrombosis, and Vascular Biology, 23, 52-57. (Pubitemid 36091625)
41. Gani, O. A. (2008). Are fish oil omega-3 long-chain fatty acids and their derivatives peroxisome proliferator-activated receptor agonists? Cardiovascular Diabetology, 7, 6. (Pubitemid 351566901)
42. Mittra, S.; & Singh, M. (1998). Possible mechanism of captopril induced endothelium-dependent relaxation in isolated rabbit aorta. Molecular and Cellular Biochemistry, 183, 63-67. (Pubitemid 28263888)
43. Shah, D. I.; & Singh, M. (2006). Involvement of Rho-kinase in experimental vascular endothelial dysfunction. Molecular and Cellular Biochemistry, 283, 191-199.
44. Sastry, K. V.; Moudgal, R. P.; Mohan, J.; Tyagu, J. S.; & Rao, G. S. (2002). Spectrophotometric determination of serum nitrite and nitrate by copper-cadmium alloy. Analytical Biochemistry, 306, 79-82. (Pubitemid 34722019)
45. Kaur, T.; Goel, R. K.; & Balakumar, P. (2010). Effect of rosiglitazone in sodium arsenite-induced experimental vascular endothelial dysfunction. Archives of Pharmacal Research, 33, 611-618.
46. Sena, C. M.; Matafome, P.; Crisóstomo, J.; Rodrigues, L.; Fernandes, R.; & Pereira, P. (2012). Methylglyoxal promotes oxidative stress and endothelial dysfunction. Pharmacological Research, 65, 497-506.
47. Wang, H. D.; Pagano, P. J.; Du, Y.; Cayatte, A. J.; Quinn, M. T.; Brecher, P.; et al. (1998). Superoxide anion from the adventitia of the rat thoracic aorta inactivates nitric oxide. Circulation Research, 82, 810-818. (Pubitemid 28185849)
48. Kanie, N.; & Kamata, K. (2002). Effects of chronic administration of the novel endothelin antagonist J-104132 on endothelial dysfunction in streptozotocin-induced diabetic rat. British Journal of Pharmacology, 135, 1935-1942. (Pubitemid 34478305)
49. Ma, F. X.; Liu, L. Y.; & Xiong, X. M. (2003). Protective effects of lovastatin on vascular endothelium injured by low density lipoprotein. Acta Pharmacologica Sinica, 24, 1027-1032.
50. Hirase, T.; & Node, K. (2012). Endothelial dysfunction as a cellular mechanism for vascular failure. American Journal of Physiology Heart and Circulatory Physiology, 302, H499-505.
51. Jindal, S.; Singh, M.; & Balakumar, P. (2008). Effect of bis (maltolato) oxovanadium (BMOV) in uric acid and sodium arsenite-induced vascular endothelial dysfunction in rats. International Journal of Cardiology, 128, 383-391.
52. Balakumar, P.; Chakkarwar, V. A.; & Singh, M. (2009). Ameliorative effect of combination of benfotiamine and fenofibrate in diabetes-induced vascular endothelial dysfunction and nephropathy in the rat. Molecular and Cellular Biochemistry, 320, 149-162.
53. Sena, C. M.; Matafome, P.; Louro, T.; Nunes, E.; Fernandes, R.; & Seiça, R. M. (2011). Metformin restores endothelial function in aorta of diabetic rats. British Journal of Pharmacology, 163, 424-437.
54. Higo, K.; Karasawa, A.; & Kubo, K. (1992). Protective effects of benidipine hydrochloride (KW-3049), a calcium antagonist, against experimental arterial calcinosis and endothelial dysfunction in rats. Journal of Pharmacobio-Dynamics, 15, 113-120.
55. Kathuria, S.; Mahadevan, N.; & Balakumar, P. (2012). Possible involvement of PPARγ-associated eNOS signaling activation in rosuvastatin-mediated prevention of nicotineinduced experimental vascular endothelial abnormalities. Molecular and Cellular Biochemistry. doi: 10.1007/s11010-012-1505-6.
56. Cheng, F.; Wang, Y.; Li, J.; Su, C.; Wu, F.; Xia, W. H.; et al. (2012). Berberine improves endothelial function by reducing endothelial microparticles-mediated oxidative stress in humans. International Journal of Cardiology. doi: 10.1016/j.ijcard.2012.03.090.
57. Sena, C. M.; Nunes, E.; Louro, T.; Proença, T.; Fernandes, R.; Boarder, M. R.; et al. (2008). Effects of alpha-lipoic acid on endothelial function in aged diabetic and high-fat fed rats. British Journal of Pharmacology, 153, 894-906. (Pubitemid 351328927)
58. Chattopadhyay, K.; & Chattopadhyay, B. D. (2008). Effect of nicotine on lipid profile, peroxidation & antioxidant enzymes in female rats with restricted dietary protein. Indian Journal of Medical Research, 127, 571-576.
59. Toba, H.; Tojo, C.; Wang, J.; Noda, K.; Kobara, M.; & Nakata, T. (2012). Telmisartan inhibits vascular dysfunction and inflammation via activation of peroxisome proliferator-activated receptor-γ in subtotal nephrectomized rat. European Journal of Pharmacology, 685, 91-98.