Skip to main content
Erschienen in: Cardiovascular Toxicology 2/2021

25.08.2020 | Smoking and Nicotine Detoxification

Interactive Effects of Omega-3 Polyunsaturated Fatty Acids and Secondhand Smoke in Mice and Human Subjects

verfasst von: Emily Wheeler, Mary Walsh-Wilcox, Meera Shah, Abinash Achrekar, Joe R. Anderson, Mary K. Walker

Erschienen in: Cardiovascular Toxicology | Ausgabe 2/2021

Einloggen, um Zugang zu erhalten

Abstract

Active smoking and secondhand smoke (SHS) exposure increase the risk of cardiovascular morbidity and mortality. Active smoking is associated with reduced levels of omega-3 polyunsaturated fatty acids (n-3 PUFA) and studies show that n-3 PUFA supplementation can improve smoking-induced vascular dysfunction. However, the relationship between n-3 PUFA and SHS exposure has not been studied. Fat-1 transgenic mice, which convert n-6 to n-3 PUFA, were fed diets with n-3 PUFA or without (n-6 PUFA diet), exposed to air or SHS for 4 weeks, and vasoreactivity, antioxidant indices, and omega-3 index (percent eicosapentaenoic + docosahexaenoic acids in RBC) measured. Compared to air-exposed mice, SHS-enhanced aortic constriction in mice fed the n-6 PUFA diet (omega-3 index, 5.9 ± 0.2%; mean ± SE), but not in mice fed the n-3 PUFA diet (omega-3 index, 7.8 ± 0.6%). SHS also significantly induced mRNA expression of cytochrome P4501A1, NADPH:quinone oxidoreductase, heme oxygenase-1, and angiotensinogen in adipose tissue, and increased antioxidant capacity only in mice on the n-6 PUFA diet. Notably, SHS reduced the omega-3 index by 1.0 percentage point (p = 0.003), compared to air-exposed mice irrespective of diet. Additionally, we recruited human nonsmokers (NS) with and without SHS exposure (n = 40) 19–40 years old and measured the omega-3 index and antioxidant capacity. In human subjects SHS exposure was associated with a significantly lower omega-3 index (NS, 4.4 ± 1.1%; NS + SHS, 3.2 ± 1.0%; mean ± SD, p = 0.002) and higher antioxidant capacity (p < 0.001) than unexposed NS. Thus, SHS exposure is associated with lower levels of n-3 PUFA in mice and humans; however, an omega-3 index of ~ 8% in mice has vasoprotective and antioxidant properties.
Anhänge
Nur mit Berechtigung zugänglich
Literatur
1.
Zurück zum Zitat Lv, X., Sun, J., Bi, Y., Xu, M., Lu, J., Zhao, L., et al. (2015). Risk of all-cause mortality and cardiovascular disease associated with secondhand smoke exposure: a systematic review and meta-analysis. International Journal of Cardiology, 199, 106–115.PubMed Lv, X., Sun, J., Bi, Y., Xu, M., Lu, J., Zhao, L., et al. (2015). Risk of all-cause mortality and cardiovascular disease associated with secondhand smoke exposure: a systematic review and meta-analysis. International Journal of Cardiology, 199, 106–115.PubMed
2.
Zurück zum Zitat Adams, T., Wan, E., Wei, Y., Wahab, R., Castagna, F., Wang, G., et al. (2015). Secondhand smoking is associated with vascular inflammation. Chest, 148, 112–119.PubMedPubMedCentral Adams, T., Wan, E., Wei, Y., Wahab, R., Castagna, F., Wang, G., et al. (2015). Secondhand smoking is associated with vascular inflammation. Chest, 148, 112–119.PubMedPubMedCentral
3.
Zurück zum Zitat Celermajer, D. S., Adams, M. R., Clarkson, P., Robinson, J., McCredie, R., Donald, A., et al. (1996). Passive smoking and impaired endothelium-dependent arterial dilatation in healthy young adults. New England Journal of Medicine, 334, 150–154. Celermajer, D. S., Adams, M. R., Clarkson, P., Robinson, J., McCredie, R., Donald, A., et al. (1996). Passive smoking and impaired endothelium-dependent arterial dilatation in healthy young adults. New England Journal of Medicine, 334, 150–154.
4.
Zurück zum Zitat Raitakari, O. T., Adams, M. R., McCredie, R. J., Griffiths, K. A., & Celermajer, D. S. (1999). Arterial endothelial dysfunction related to passive smoking is potentially reversible in healthy young adults. Annals of Internal Medicine, 130, 578–581.PubMed Raitakari, O. T., Adams, M. R., McCredie, R. J., Griffiths, K. A., & Celermajer, D. S. (1999). Arterial endothelial dysfunction related to passive smoking is potentially reversible in healthy young adults. Annals of Internal Medicine, 130, 578–581.PubMed
5.
Zurück zum Zitat Woo, K. S., Chook, P., Leong, H. C., Huang, X. S., & Celermajer, D. S. (2000). The impact of heavy passive smoking on arterial endothelial function in modernized Chinese. Journal of the American College of Cardiology, 36, 1228–1232.PubMed Woo, K. S., Chook, P., Leong, H. C., Huang, X. S., & Celermajer, D. S. (2000). The impact of heavy passive smoking on arterial endothelial function in modernized Chinese. Journal of the American College of Cardiology, 36, 1228–1232.PubMed
6.
Zurück zum Zitat Holay, M. P., Paunikar, N. P., Joshi, P. P., Sahasrabhojney, V. S., & Tankhiwale, S. R. (2004). Effect of passive smoking on endothelial function in healthy adults. Journal of the Association of Physicians of India, 52, 114–117. Holay, M. P., Paunikar, N. P., Joshi, P. P., Sahasrabhojney, V. S., & Tankhiwale, S. R. (2004). Effect of passive smoking on endothelial function in healthy adults. Journal of the Association of Physicians of India, 52, 114–117.
7.
Zurück zum Zitat Kallio, K., Jokinen, E., Saarinen, M., Hamalainen, M., Volanen, I., Kaitosaari, T., et al. (2010). Arterial intima-media thickness, endothelial function, and apolipoproteins in adolescents frequently exposed to tobacco smoke. Circ Cardiovasc Qual Outcomes, 3, 196–203.PubMed Kallio, K., Jokinen, E., Saarinen, M., Hamalainen, M., Volanen, I., Kaitosaari, T., et al. (2010). Arterial intima-media thickness, endothelial function, and apolipoproteins in adolescents frequently exposed to tobacco smoke. Circ Cardiovasc Qual Outcomes, 3, 196–203.PubMed
8.
Zurück zum Zitat Adkins, Y., & Kelley, D. S. (2010). Mechanisms underlying the cardioprotective effects of omega-3 polyunsaturated fatty acids. Journal of Nutritional Biochemistry, 21, 781–792. Adkins, Y., & Kelley, D. S. (2010). Mechanisms underlying the cardioprotective effects of omega-3 polyunsaturated fatty acids. Journal of Nutritional Biochemistry, 21, 781–792.
9.
Zurück zum Zitat Wiest, E. F., Walsh-Wilcox, M. T., & Walker, M. K. (2017). Omega-3 polyunsaturated fatty acids protect against cigarette smoke-induced oxidative stress and vascular dysfunction. Toxicological Sciences, 156, 300–310.PubMedPubMedCentral Wiest, E. F., Walsh-Wilcox, M. T., & Walker, M. K. (2017). Omega-3 polyunsaturated fatty acids protect against cigarette smoke-induced oxidative stress and vascular dysfunction. Toxicological Sciences, 156, 300–310.PubMedPubMedCentral
10.
Zurück zum Zitat Din, J. N., Archer, R. M., Harding, S. A., Sarma, J., Lyall, K., Flapan, A. D., et al. (2012). Effect of omega-3 fatty acid supplementation on endothelial function, endogenous fibrinolysis and platelet activation in male cigarette smokers. Heart, 99, 168–174.PubMed Din, J. N., Archer, R. M., Harding, S. A., Sarma, J., Lyall, K., Flapan, A. D., et al. (2012). Effect of omega-3 fatty acid supplementation on endothelial function, endogenous fibrinolysis and platelet activation in male cigarette smokers. Heart, 99, 168–174.PubMed
11.
Zurück zum Zitat Siasos, G., Tousoulis, D., Oikonomou, E., Zaromitidou, M., Verveniotis, A., Plastiras, A., et al. (2011). Effects of Omega-3 fatty acids on endothelial function, arterial wall properties, inflammatory and fibrinolytic status in smokers: A cross over study. International Journal of Cardiology, 166, 340–346.PubMed Siasos, G., Tousoulis, D., Oikonomou, E., Zaromitidou, M., Verveniotis, A., Plastiras, A., et al. (2011). Effects of Omega-3 fatty acids on endothelial function, arterial wall properties, inflammatory and fibrinolytic status in smokers: A cross over study. International Journal of Cardiology, 166, 340–346.PubMed
12.
Zurück zum Zitat Fenton, J. I., Gurzell, E. A., Davidson, E. A., & Harris, W. S. (2016). Red blood cell PUFAs reflect the phospholipid PUFA composition of major organs. Prostaglandins Leukotrienes and Essential Fatty Acids, 112, 12–23. Fenton, J. I., Gurzell, E. A., Davidson, E. A., & Harris, W. S. (2016). Red blood cell PUFAs reflect the phospholipid PUFA composition of major organs. Prostaglandins Leukotrienes and Essential Fatty Acids, 112, 12–23.
13.
Zurück zum Zitat Harris, W. S., Pottala, J. V., Lacey, S. M., Vasan, R. S., Larson, M. G., & Robins, S. J. (2012). Clinical correlates and heritability of erythrocyte eicosapentaenoic and docosahexaenoic acid content in the Framingham Heart Study. Atherosclerosis, 225, 425–431.PubMedPubMedCentral Harris, W. S., Pottala, J. V., Lacey, S. M., Vasan, R. S., Larson, M. G., & Robins, S. J. (2012). Clinical correlates and heritability of erythrocyte eicosapentaenoic and docosahexaenoic acid content in the Framingham Heart Study. Atherosclerosis, 225, 425–431.PubMedPubMedCentral
14.
Zurück zum Zitat Flock, M. R., Skulas-Ray, A. C., Harris, W. S., Etherton, T. D., Fleming, J. A., & Kris-Etherton, P. M. (2013). Determinants of erythrocyte omega-3 fatty acid content in response to fish oil supplementation: A dose-response randomized controlled trial. Journal of American Heart Association, 2, e000513. Flock, M. R., Skulas-Ray, A. C., Harris, W. S., Etherton, T. D., Fleming, J. A., & Kris-Etherton, P. M. (2013). Determinants of erythrocyte omega-3 fatty acid content in response to fish oil supplementation: A dose-response randomized controlled trial. Journal of American Heart Association, 2, e000513.
15.
Zurück zum Zitat Block, R. C., Harris, W. S., & Pottala, J. V. (2008). Determinants of blood cell omega-3 fatty acid content. Open Biomark J, 1, 1–6.PubMedPubMedCentral Block, R. C., Harris, W. S., & Pottala, J. V. (2008). Determinants of blood cell omega-3 fatty acid content. Open Biomark J, 1, 1–6.PubMedPubMedCentral
16.
Zurück zum Zitat Murff, H. J., Tindle, H. A., Shrubsole, M. J., Cai, Q., Smalley, W., Milne, G. L., et al. (2016). Smoking and red blood cell phospholipid membrane fatty acids. Prostaglandins Leukotrienes and Essential Fatty Acids, 112, 24–31. Murff, H. J., Tindle, H. A., Shrubsole, M. J., Cai, Q., Smalley, W., Milne, G. L., et al. (2016). Smoking and red blood cell phospholipid membrane fatty acids. Prostaglandins Leukotrienes and Essential Fatty Acids, 112, 24–31.
17.
Zurück zum Zitat Simon, J. A., Fong, J., Bernert, J. T., Jr., & Browner, W. S. (1996). Relation of smoking and alcohol consumption to serum fatty acids. American Journal of Epidemiology, 144, 325–334.PubMed Simon, J. A., Fong, J., Bernert, J. T., Jr., & Browner, W. S. (1996). Relation of smoking and alcohol consumption to serum fatty acids. American Journal of Epidemiology, 144, 325–334.PubMed
18.
Zurück zum Zitat Wiest, E. F., Warneke, A., Walsh, M. T., Langsfeld, M., Anderson, J., & Walker, M. K. (2015). Association of serum aryl hydrocarbon receptor activity and RBC omega-3 polyunsaturated fatty acids with flow-mediated dilation in healthy, young Hispanic cigarette smokers. Toxicology Letters, 232, 422–428.PubMed Wiest, E. F., Warneke, A., Walsh, M. T., Langsfeld, M., Anderson, J., & Walker, M. K. (2015). Association of serum aryl hydrocarbon receptor activity and RBC omega-3 polyunsaturated fatty acids with flow-mediated dilation in healthy, young Hispanic cigarette smokers. Toxicology Letters, 232, 422–428.PubMed
19.
Zurück zum Zitat Ionescu, N., de Freitas, C., & Bueno, A. A. (2013). Perturbations in blood phosphatidylcholine and sphingomyelin fatty acid composition in a sample population of cigarette smokers. Indian Journal of Clinical Biochemistry, 28, 361–367.PubMedPubMedCentral Ionescu, N., de Freitas, C., & Bueno, A. A. (2013). Perturbations in blood phosphatidylcholine and sphingomyelin fatty acid composition in a sample population of cigarette smokers. Indian Journal of Clinical Biochemistry, 28, 361–367.PubMedPubMedCentral
20.
Zurück zum Zitat Kang, J. X., Wang, J., Wu, L., & Kang, Z. B. (2004). Transgenic mice: fat-1 mice convert n-6 to n-3 fatty acids. Nature, 427, 504.PubMed Kang, J. X., Wang, J., Wu, L., & Kang, Z. B. (2004). Transgenic mice: fat-1 mice convert n-6 to n-3 fatty acids. Nature, 427, 504.PubMed
21.
Zurück zum Zitat Superko, H. R., Superko, A. R., Lundberg, G. P., Margolis, B., Garrett, B. C., Nasir, K., et al. (2014). Omega-3 fatty acid blood levels clinical significance update. Curr Cardiovasc Risk Rep, 8, 407.PubMedPubMedCentral Superko, H. R., Superko, A. R., Lundberg, G. P., Margolis, B., Garrett, B. C., Nasir, K., et al. (2014). Omega-3 fatty acid blood levels clinical significance update. Curr Cardiovasc Risk Rep, 8, 407.PubMedPubMedCentral
22.
Zurück zum Zitat Agbor, L. N., Wiest, E. F., Rothe, M., Schunck, W. H., & Walker, M. K. (2014). Role of CYP1A1 in modulating the vascular and blood pressure benefits of omega-3 polyunsaturated fatty acids. Journal of Pharmacology and Experimental Therapeutics, 351, 688–698. Agbor, L. N., Wiest, E. F., Rothe, M., Schunck, W. H., & Walker, M. K. (2014). Role of CYP1A1 in modulating the vascular and blood pressure benefits of omega-3 polyunsaturated fatty acids. Journal of Pharmacology and Experimental Therapeutics, 351, 688–698.
23.
Zurück zum Zitat Wiest, E. F., Walsh-Wilcox, M. T., Rothe, M., Schunck, W. H., & Walker, M. K. (2016). Dietary omega-3 polyunsaturated fatty acids prevent vascular dysfunction and attenuate cytochrome P4501A1 expression by 2,3,7,8-tetrachlorodibenzo-P-dioxin. Toxicological Sciences, 154, 43–54.PubMedPubMedCentral Wiest, E. F., Walsh-Wilcox, M. T., Rothe, M., Schunck, W. H., & Walker, M. K. (2016). Dietary omega-3 polyunsaturated fatty acids prevent vascular dysfunction and attenuate cytochrome P4501A1 expression by 2,3,7,8-tetrachlorodibenzo-P-dioxin. Toxicological Sciences, 154, 43–54.PubMedPubMedCentral
24.
Zurück zum Zitat Cirera, S. (2013). Highly efficient method for isolation of total RNA from adipose tissue. BMC Research Notes, 6, 472.PubMedPubMedCentral Cirera, S. (2013). Highly efficient method for isolation of total RNA from adipose tissue. BMC Research Notes, 6, 472.PubMedPubMedCentral
25.
Zurück zum Zitat Lund, A. K., Goens, M. B., Kanagy, N. L., & Walker, M. K. (2003). Cardiac hypertrophy in aryl hydrocarbon receptor (AhR) null mice is correlated with elevated angiotensin II, endothelin-1 and mean arterial blood pressure. Toxicology and Applied Pharmacology, 193, 177–187.PubMed Lund, A. K., Goens, M. B., Kanagy, N. L., & Walker, M. K. (2003). Cardiac hypertrophy in aryl hydrocarbon receptor (AhR) null mice is correlated with elevated angiotensin II, endothelin-1 and mean arterial blood pressure. Toxicology and Applied Pharmacology, 193, 177–187.PubMed
26.
Zurück zum Zitat Pickering, T. G., Hall, J. E., Appel, L. J., Falkner, B. E., Graves, J. W., Hill, M. N., et al. (2005). Recommendations for blood pressure measurement in humans: An AHA scientific statement from the Council on High Blood Pressure Research Professional and Public Education Subcommittee. J Clin Hypertens (Greenwich), 7, 102–109. Pickering, T. G., Hall, J. E., Appel, L. J., Falkner, B. E., Graves, J. W., Hill, M. N., et al. (2005). Recommendations for blood pressure measurement in humans: An AHA scientific statement from the Council on High Blood Pressure Research Professional and Public Education Subcommittee. J Clin Hypertens (Greenwich), 7, 102–109.
27.
Zurück zum Zitat Harris, W. S., & Polreis, J. (2016). Measurement of the Omega-3 Index in dried blood spots. Annals of Clinical and Laboratory Research, 4, 137–143. Harris, W. S., & Polreis, J. (2016). Measurement of the Omega-3 Index in dried blood spots. Annals of Clinical and Laboratory Research, 4, 137–143.
28.
Zurück zum Zitat Hutchison, S. J., Glantz, S. A., Zhu, B. Q., Sun, Y. P., Chou, T. M., Chatterjee, K., et al. (1998). In-utero and neonatal exposure to secondhand smoke causes vascular dysfunction in newborn rats. Journal of the American College of Cardiology, 32, 1463–1467.PubMed Hutchison, S. J., Glantz, S. A., Zhu, B. Q., Sun, Y. P., Chou, T. M., Chatterjee, K., et al. (1998). In-utero and neonatal exposure to secondhand smoke causes vascular dysfunction in newborn rats. Journal of the American College of Cardiology, 32, 1463–1467.PubMed
29.
Zurück zum Zitat Hutchison, S. J., Sudhir, K., Sievers, R. E., Zhu, B. Q., Sun, Y. P., Chou, T. M., et al. (1999). Effects of L-arginine on atherogenesis and endothelial dysfunction due to secondhand smoke. Hypertension, 34, 44–50.PubMed Hutchison, S. J., Sudhir, K., Sievers, R. E., Zhu, B. Q., Sun, Y. P., Chou, T. M., et al. (1999). Effects of L-arginine on atherogenesis and endothelial dysfunction due to secondhand smoke. Hypertension, 34, 44–50.PubMed
30.
Zurück zum Zitat Hutchison, S. J., Sievers, R. E., Zhu, B. Q., Sun, Y. P., Stewart, D. J., Parmley, W. W., et al. (2001). Secondhand tobacco smoke impairs rabbit pulmonary artery endothelium-dependent relaxation. Chest, 120, 2004–2012.PubMed Hutchison, S. J., Sievers, R. E., Zhu, B. Q., Sun, Y. P., Stewart, D. J., Parmley, W. W., et al. (2001). Secondhand tobacco smoke impairs rabbit pulmonary artery endothelium-dependent relaxation. Chest, 120, 2004–2012.PubMed
31.
Zurück zum Zitat Kaplan, H. M., Kuyucu, Y., Polat, S., Pazarci, P., Yegani, A. A., Singirik, E., et al. (2018). Molecular basis of vascular damage caused by cigarette smoke exposure and a new approach to the treatment: Alpha-linolenic acid. Biomedicine & Pharmacotherapy, 102, 458–463. Kaplan, H. M., Kuyucu, Y., Polat, S., Pazarci, P., Yegani, A. A., Singirik, E., et al. (2018). Molecular basis of vascular damage caused by cigarette smoke exposure and a new approach to the treatment: Alpha-linolenic acid. Biomedicine & Pharmacotherapy, 102, 458–463.
32.
Zurück zum Zitat Zehr, K. R., Segovia, A., Shah, M., Walsh-Wilcox, M. T., Brumbach, B. H., Anderson, J. R., et al. (2019). Associations of medium and long chain omega-3 polyunsaturated fatty acids with blood pressure in Hispanic and non-Hispanic smokers and nonsmokers. Prostaglandins Leukotrienes and Essential Fatty Acids, 144, 10–15. Zehr, K. R., Segovia, A., Shah, M., Walsh-Wilcox, M. T., Brumbach, B. H., Anderson, J. R., et al. (2019). Associations of medium and long chain omega-3 polyunsaturated fatty acids with blood pressure in Hispanic and non-Hispanic smokers and nonsmokers. Prostaglandins Leukotrienes and Essential Fatty Acids, 144, 10–15.
33.
Zurück zum Zitat Zehr, K. R., & Walker, M. K. (2018). Omega-3 polyunsaturated fatty acids improve endothelial function in humans at risk for atherosclerosis: A review. Prostaglandins & Other Lipid Mediators, 134, 131–140. Zehr, K. R., & Walker, M. K. (2018). Omega-3 polyunsaturated fatty acids improve endothelial function in humans at risk for atherosclerosis: A review. Prostaglandins & Other Lipid Mediators, 134, 131–140.
34.
Zurück zum Zitat Leeson, C. P., Mann, A., Kattenhorn, M., Deanfield, J. E., Lucas, A., & Muller, D. P. (2002). Relationship between circulating n-3 fatty acid concentrations and endothelial function in early adulthood. European Heart Journal, 23, 216–222.PubMed Leeson, C. P., Mann, A., Kattenhorn, M., Deanfield, J. E., Lucas, A., & Muller, D. P. (2002). Relationship between circulating n-3 fatty acid concentrations and endothelial function in early adulthood. European Heart Journal, 23, 216–222.PubMed
35.
Zurück zum Zitat Li, Q., Zhang, Q., Wang, M., Liu, F., Zhao, S., Ma, J., et al. (2007). Docosahexaenoic acid affects endothelial nitric oxide synthase in caveolae. Archives of Biochemistry and Biophysics, 466, 250–259.PubMed Li, Q., Zhang, Q., Wang, M., Liu, F., Zhao, S., Ma, J., et al. (2007). Docosahexaenoic acid affects endothelial nitric oxide synthase in caveolae. Archives of Biochemistry and Biophysics, 466, 250–259.PubMed
36.
Zurück zum Zitat Li, Q., Zhang, Q., Wang, M., Zhao, S., Ma, J., Luo, N., et al. (2007). Eicosapentaenoic acid modifies lipid composition in caveolae and induces translocation of endothelial nitric oxide synthase. Biochimie, 89, 169–177.PubMed Li, Q., Zhang, Q., Wang, M., Zhao, S., Ma, J., Luo, N., et al. (2007). Eicosapentaenoic acid modifies lipid composition in caveolae and induces translocation of endothelial nitric oxide synthase. Biochimie, 89, 169–177.PubMed
37.
Zurück zum Zitat Stebbins, C. L., Stice, J. P., Hart, C. M., Mbai, F. N., & Knowlton, A. A. (2008). Effects of dietary decosahexaenoic acid (DHA) on eNOS in human coronary artery endothelial cells. Journal of Cardiovascular Pharmacology Therapeutics, 13, 261–268.PubMed Stebbins, C. L., Stice, J. P., Hart, C. M., Mbai, F. N., & Knowlton, A. A. (2008). Effects of dietary decosahexaenoic acid (DHA) on eNOS in human coronary artery endothelial cells. Journal of Cardiovascular Pharmacology Therapeutics, 13, 261–268.PubMed
38.
Zurück zum Zitat Shimokawa, H., Aarhus, L. L., & Vanhoutte, P. M. (1988). Dietary omega 3 polyunsaturated fatty acids augment endothelium-dependent relaxation to bradykinin in coronary microvessels of the pig. British Journal of Pharmacology, 95, 1191–1196.PubMedPubMedCentral Shimokawa, H., Aarhus, L. L., & Vanhoutte, P. M. (1988). Dietary omega 3 polyunsaturated fatty acids augment endothelium-dependent relaxation to bradykinin in coronary microvessels of the pig. British Journal of Pharmacology, 95, 1191–1196.PubMedPubMedCentral
39.
Zurück zum Zitat Shimokawa, H., & Vanhoutte, P. M. (1988). Dietary cod-liver oil improves endothelium-dependent responses in hypercholesterolemic and atherosclerotic porcine coronary arteries. Circulation, 78, 1421–1430.PubMed Shimokawa, H., & Vanhoutte, P. M. (1988). Dietary cod-liver oil improves endothelium-dependent responses in hypercholesterolemic and atherosclerotic porcine coronary arteries. Circulation, 78, 1421–1430.PubMed
40.
Zurück zum Zitat 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.PubMed 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.PubMed
41.
Zurück zum Zitat Tagawa, H., Shimokawa, H., Tagawa, T., Kuroiwa-Matsumoto, M., Hirooka, Y., & Takeshita, A. (1999). Long-term treatment with eicosapentaenoic acid augments both nitric oxide-mediated and non-nitric oxide-mediated endothelium-dependent forearm vasodilatation in patients with coronary artery disease. Journal of Cardiovascular Pharmacology, 33, 633–640.PubMed Tagawa, H., Shimokawa, H., Tagawa, T., Kuroiwa-Matsumoto, M., Hirooka, Y., & Takeshita, A. (1999). Long-term treatment with eicosapentaenoic acid augments both nitric oxide-mediated and non-nitric oxide-mediated endothelium-dependent forearm vasodilatation in patients with coronary artery disease. Journal of Cardiovascular Pharmacology, 33, 633–640.PubMed
42.
Zurück zum Zitat Behm, D. J., Ogbonna, A., Wu, C., Burns-Kurtis, C. L., & Douglas, S. A. (2009). Epoxyeicosatrienoic acids function as selective, endogenous antagonists of native thromboxane receptors: Identification of a novel mechanism of vasodilation. Journal of Pharmacology and Experimental Therapeutics, 328, 231–239. Behm, D. J., Ogbonna, A., Wu, C., Burns-Kurtis, C. L., & Douglas, S. A. (2009). Epoxyeicosatrienoic acids function as selective, endogenous antagonists of native thromboxane receptors: Identification of a novel mechanism of vasodilation. Journal of Pharmacology and Experimental Therapeutics, 328, 231–239.
43.
Zurück zum Zitat Hercule, H. C., Salanova, B., Essin, K., Honeck, H., Falck, J. R., Sausbier, M., et al. (2007). The vasodilator 17,18-epoxyeicosatetraenoic acid targets the pore-forming BK alpha channel subunit in rodents. Experimental Physiology, 92, 1067–1076.PubMed Hercule, H. C., Salanova, B., Essin, K., Honeck, H., Falck, J. R., Sausbier, M., et al. (2007). The vasodilator 17,18-epoxyeicosatetraenoic acid targets the pore-forming BK alpha channel subunit in rodents. Experimental Physiology, 92, 1067–1076.PubMed
44.
Zurück zum Zitat Safonova, I., Aubert, J., Negrel, R., & Ailhaud, G. (1997). Regulation by fatty acids of angiotensinogen gene expression in preadipose cells. The Biochemical Journal, 322(Pt 1), 235–239.PubMedPubMedCentral Safonova, I., Aubert, J., Negrel, R., & Ailhaud, G. (1997). Regulation by fatty acids of angiotensinogen gene expression in preadipose cells. The Biochemical Journal, 322(Pt 1), 235–239.PubMedPubMedCentral
45.
Zurück zum Zitat Siriwardhana, N., Kalupahana, N. S., Fletcher, S., Xin, W., Claycombe, K. J., Quignard-Boulange, A., et al. (2012). n-3 and n-6 polyunsaturated fatty acids differentially regulate adipose angiotensinogen and other inflammatory adipokines in part via NF-kappaB-dependent mechanisms. Journal of Nutritional Biochemistry, 23, 1661–1667. Siriwardhana, N., Kalupahana, N. S., Fletcher, S., Xin, W., Claycombe, K. J., Quignard-Boulange, A., et al. (2012). n-3 and n-6 polyunsaturated fatty acids differentially regulate adipose angiotensinogen and other inflammatory adipokines in part via NF-kappaB-dependent mechanisms. Journal of Nutritional Biochemistry, 23, 1661–1667.
46.
Zurück zum Zitat Walsh-Wilcox, M. T., Kaye, J., Rubinstein, E., & Walker, M. K. (2019). 2,3,7,8-Tetrachlorodibenzo-p-dioxin induces vascular dysfunction that is dependent on perivascular adipose and cytochrome P4501A1 expression. Cardiovascular Toxicology, 19, 565–574.PubMed Walsh-Wilcox, M. T., Kaye, J., Rubinstein, E., & Walker, M. K. (2019). 2,3,7,8-Tetrachlorodibenzo-p-dioxin induces vascular dysfunction that is dependent on perivascular adipose and cytochrome P4501A1 expression. Cardiovascular Toxicology, 19, 565–574.PubMed
47.
Zurück zum Zitat Arcand, S., Sharma, K., Al-Dissi, A. N., Cadete, V. J., Sawicki, G., & Weber, L. P. (2013). Resveratrol protects against functional impairment and cardiac structural protein degradation induced by secondhand smoke exposure. Canadian Journal of Cardiology, 29, 1320–1328. Arcand, S., Sharma, K., Al-Dissi, A. N., Cadete, V. J., Sawicki, G., & Weber, L. P. (2013). Resveratrol protects against functional impairment and cardiac structural protein degradation induced by secondhand smoke exposure. Canadian Journal of Cardiology, 29, 1320–1328.
48.
Zurück zum Zitat Conklin, D. J., Malovichko, M. V., Zeller, I., Das, T. P., Krivokhizhina, T. V., Lynch, B. H., et al. (2017). Biomarkers of chronic acrolein inhalation exposure in mice: Implications for tobacco product-induced toxicity. Toxicological Sciences, 158, 263–274.PubMedPubMedCentral Conklin, D. J., Malovichko, M. V., Zeller, I., Das, T. P., Krivokhizhina, T. V., Lynch, B. H., et al. (2017). Biomarkers of chronic acrolein inhalation exposure in mice: Implications for tobacco product-induced toxicity. Toxicological Sciences, 158, 263–274.PubMedPubMedCentral
49.
Zurück zum Zitat Scaglia, N., Chatkin, J., Chapman, K. R., Ferreira, I., Wagner, M., Selby, P., et al. (2016). The relationship between omega-3 and smoking habit: A cross-sectional study. Lipids Health Dis, 15, 61.PubMedPubMedCentral Scaglia, N., Chatkin, J., Chapman, K. R., Ferreira, I., Wagner, M., Selby, P., et al. (2016). The relationship between omega-3 and smoking habit: A cross-sectional study. Lipids Health Dis, 15, 61.PubMedPubMedCentral
50.
Zurück zum Zitat Leng, G. C., Horrobin, D. F., Fowkes, F. G., Smith, F. B., Lowe, G. D., Donnan, P. T., et al. (1994). Plasma essential fatty acids, cigarette smoking, and dietary antioxidants in peripheral arterial disease. A population-based case-control study. Arteriosclerosis and Thrombosis, 14, 471–478.PubMed Leng, G. C., Horrobin, D. F., Fowkes, F. G., Smith, F. B., Lowe, G. D., Donnan, P. T., et al. (1994). Plasma essential fatty acids, cigarette smoking, and dietary antioxidants in peripheral arterial disease. A population-based case-control study. Arteriosclerosis and Thrombosis, 14, 471–478.PubMed
51.
Zurück zum Zitat Ghezzi, S., Rise, P., Ceruti, S., & Galli, C. (2007). Effects of cigarette smoke on cell viability, linoleic acid metabolism and cholesterol synthesis, in THP-1 cells. Lipids, 42, 629–636.PubMed Ghezzi, S., Rise, P., Ceruti, S., & Galli, C. (2007). Effects of cigarette smoke on cell viability, linoleic acid metabolism and cholesterol synthesis, in THP-1 cells. Lipids, 42, 629–636.PubMed
52.
Zurück zum Zitat Marangoni, F., Colombo, C., De Angelis, L., Gambaro, V., Agostoni, C., Giovannini, M., et al. (2004). Cigarette smoke negatively and dose-dependently affects the biosynthetic pathway of the n-3 polyunsaturated fatty acid series in human mammary epithelial cells. Lipids, 39, 633–637.PubMed Marangoni, F., Colombo, C., De Angelis, L., Gambaro, V., Agostoni, C., Giovannini, M., et al. (2004). Cigarette smoke negatively and dose-dependently affects the biosynthetic pathway of the n-3 polyunsaturated fatty acid series in human mammary epithelial cells. Lipids, 39, 633–637.PubMed
53.
Zurück zum Zitat Burdge, G. C., Jones, A. E., & Wootton, S. A. (2002). Eicosapentaenoic and docosapentaenoic acids are the principal products of alpha-linolenic acid metabolism in young men. British Journal of Nutrition, 88, 355–363. Burdge, G. C., Jones, A. E., & Wootton, S. A. (2002). Eicosapentaenoic and docosapentaenoic acids are the principal products of alpha-linolenic acid metabolism in young men. British Journal of Nutrition, 88, 355–363.
54.
Zurück zum Zitat Burdge, G. C., & Wootton, S. A. (2002). Conversion of alpha-linolenic acid to eicosapentaenoic, docosapentaenoic and docosahexaenoic acids in young women. British Journal of Nutrition, 88, 411–420. Burdge, G. C., & Wootton, S. A. (2002). Conversion of alpha-linolenic acid to eicosapentaenoic, docosapentaenoic and docosahexaenoic acids in young women. British Journal of Nutrition, 88, 411–420.
55.
Zurück zum Zitat Harris, W. S., & Von Schacky, C. (2004). The Omega-3 Index: A new risk factor for death from coronary heart disease? Preventive Medicine, 39, 212–220.PubMed Harris, W. S., & Von Schacky, C. (2004). The Omega-3 Index: A new risk factor for death from coronary heart disease? Preventive Medicine, 39, 212–220.PubMed
56.
Zurück zum Zitat Harris, W. S., Del Gobbo, L., & Tintle, N. L. (2017). The Omega-3 Index and relative risk for coronary heart disease mortality: Estimation from 10 cohort studies. Atherosclerosis, 262, 51–54.PubMed Harris, W. S., Del Gobbo, L., & Tintle, N. L. (2017). The Omega-3 Index and relative risk for coronary heart disease mortality: Estimation from 10 cohort studies. Atherosclerosis, 262, 51–54.PubMed
58.
Zurück zum Zitat Rockett, B. D., Harris, M., & Raza Shaikh, S. (2012). High dose of an n-3 polyunsaturated fatty acid diet lowers activity of C57BL/6 mice. Prostaglandins Leukotrienes and Essential Fatty Acids, 86, 137–140. Rockett, B. D., Harris, M., & Raza Shaikh, S. (2012). High dose of an n-3 polyunsaturated fatty acid diet lowers activity of C57BL/6 mice. Prostaglandins Leukotrienes and Essential Fatty Acids, 86, 137–140.
Metadaten
Titel
Interactive Effects of Omega-3 Polyunsaturated Fatty Acids and Secondhand Smoke in Mice and Human Subjects
verfasst von
Emily Wheeler
Mary Walsh-Wilcox
Meera Shah
Abinash Achrekar
Joe R. Anderson
Mary K. Walker
Publikationsdatum
25.08.2020
Verlag
Springer US
Erschienen in
Cardiovascular Toxicology / Ausgabe 2/2021
Print ISSN: 1530-7905
Elektronische ISSN: 1559-0259
DOI
https://doi.org/10.1007/s12012-020-09601-6

Weitere Artikel der Ausgabe 2/2021

Cardiovascular Toxicology 2/2021 Zur Ausgabe