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11.06.2019

The Protective Effect of Crataegus aronia Against High-Fat Diet-Induced Vascular Inflammation in Rats Entails Inhibition of the NLRP-3 Inflammasome Pathway

verfasst von: Abdullah S. Shatoor, Suliman Al Humayed

Erschienen in: Cardiovascular Toxicology

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Abstract

This study investigated whether the whole-plant aqueous extract of Crataegus aronia (C. aronia) could protect against or alleviate high-fat diet (HFD)-induced aortic vascular inflammation in rats by inhibiting the NLRP-3 inflammasome pathway and examined some mechanisms of action with respect to its antioxidant and hypolipidemic effects. Adult male Wistar rats were divided into five groups (n = 6/each): standard diet (10% fat) fed to control rats, control + C. aronia (200 mg/kg), HFD (40% fat), HFD + C. aronia, and HFD post-treated with C. aronia. The HFD was fed for 8 weeks and C. aronia was administered orally for 4 weeks. In addition, isolated macrophages from control rats were pre-incubated with two doses of C. aronia (25 and 50 μg/mL) with or without lipopolysaccharide (LPS) stimulation. Only in HFD-fed rats, co- and post-C. aronia therapy lowered circulatory levels of LDL-C and ox-LDL-c and aortic protein levels of LOX-1 and CD36. C. aronia also inhibited the nuclear accumulation of NF-κB and lowered protein levels of NLRP-3, caspase-1, and mature IL-1β. In vitro, in the absence of ox-LDL-c, C. aronia led to reduced nuclear levels of NF-κB, ROS generation, and protein NLRP-3 levels, in both LPS-stimulated and unstimulated macrophages, in a dose-dependent manner. However, protein levels of LOX-1 were not affected by C. aronia in unstimulated cells. In conclusion, C. aronia inhibits the NLRP-3 inflammasome pathway, induced by HFD feeding in the aorta of rats, mainly by its hypolipidemic effect and in vitro, in LPS-stimulated macrophages, by its antioxidant effect.

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Literatur
1.
Zurück zum Zitat Packard, R. R., & Libby, P. (2008). Inflammation in atherosclerosis: From vascular biology to biomarker discovery and risk prediction. Clinical Chemistry,54, 24–38.PubMed Packard, R. R., & Libby, P. (2008). Inflammation in atherosclerosis: From vascular biology to biomarker discovery and risk prediction. Clinical Chemistry,54, 24–38.PubMed
2.
Zurück zum Zitat Anogeianaki, A., Angelucci, D., Cianchetti, E., D’Alessandro, M., Maccauro, G., Saggini, A., et al. (2011). Atherosclerosis: A classic inflammatory disease. International Journal of Immunopathology and Pharmacology,24(4), 817–825.PubMed Anogeianaki, A., Angelucci, D., Cianchetti, E., D’Alessandro, M., Maccauro, G., Saggini, A., et al. (2011). Atherosclerosis: A classic inflammatory disease. International Journal of Immunopathology and Pharmacology,24(4), 817–825.PubMed
3.
Zurück zum Zitat Tedgui, A., & Mallat, Z. (2006). Cytokines in atherosclerosis: Pathogenic and regulatory pathways. Physiological Reviews,86(2), 515–581.PubMed Tedgui, A., & Mallat, Z. (2006). Cytokines in atherosclerosis: Pathogenic and regulatory pathways. Physiological Reviews,86(2), 515–581.PubMed
4.
Zurück zum Zitat Baldrighi, M., Malla, Z., & Li, X. (2017). NLRP-3 inflammasome pathways in atherosclerosis. Atherosclerosis,267, 127–138.PubMed Baldrighi, M., Malla, Z., & Li, X. (2017). NLRP-3 inflammasome pathways in atherosclerosis. Atherosclerosis,267, 127–138.PubMed
5.
Zurück zum Zitat Libby, P. (2017). Interleukin-1 beta as a target for atherosclerosis therapy biological basis of CANTOS and beyond. Journal of the American College of Cardiology,70, 2278–2289.PubMedPubMedCentral Libby, P. (2017). Interleukin-1 beta as a target for atherosclerosis therapy biological basis of CANTOS and beyond. Journal of the American College of Cardiology,70, 2278–2289.PubMedPubMedCentral
6.
Zurück zum Zitat Shi, X., Xie, W. L., Kong, W. W., Chen, D., & Qu, P. (2015). Expression of the NLRP-3 inflammasome in carotid atherosclerosis. Journal of Stroke and Cerebrovascular Diseases,24, 2455–2466.PubMed Shi, X., Xie, W. L., Kong, W. W., Chen, D., & Qu, P. (2015). Expression of the NLRP-3 inflammasome in carotid atherosclerosis. Journal of Stroke and Cerebrovascular Diseases,24, 2455–2466.PubMed
7.
Zurück zum Zitat Paramel Varghese, G., Folkersen, L., Strawbridge, R. J., Halvorsen, B., Yndestad, A., Ranheim, T., et al. (2016). NLRP-3 inflammasome expression and activation in human atherosclerosis. Journal of the American Heart Association,5, e003031.PubMedPubMedCentral Paramel Varghese, G., Folkersen, L., Strawbridge, R. J., Halvorsen, B., Yndestad, A., Ranheim, T., et al. (2016). NLRP-3 inflammasome expression and activation in human atherosclerosis. Journal of the American Heart Association,5, e003031.PubMedPubMedCentral
8.
Zurück zum Zitat Xing, Q. (2014). Silence of NLRP-3 suppresses atherosclerosis and stabilizes plaques in apolipoprotein E-deficient mice. Mediators of Inflammation,2014, 507208.PubMedPubMedCentral Xing, Q. (2014). Silence of NLRP-3 suppresses atherosclerosis and stabilizes plaques in apolipoprotein E-deficient mice. Mediators of Inflammation,2014, 507208.PubMedPubMedCentral
9.
Zurück zum Zitat Kirichenko, T. V., Sobenin, I. A., Nikolic, D., Rizzo, M., & Orekhov, A. N. (2016). Anticytokine therapy for prevention of atherosclerosis. Phytomedicine,23(11), 1198–1210.PubMed Kirichenko, T. V., Sobenin, I. A., Nikolic, D., Rizzo, M., & Orekhov, A. N. (2016). Anticytokine therapy for prevention of atherosclerosis. Phytomedicine,23(11), 1198–1210.PubMed
10.
Zurück zum Zitat Ridker, P. M., Everett, B. M., Thuren, T., MacFadyen, J. G., Chang, W. H., Ballantyne, C., et al. (2017). Antiinflammatory therapy with canakinumab for atherosclerotic disease. New England Journal of Medicine,377(12), 1119–1131.PubMed Ridker, P. M., Everett, B. M., Thuren, T., MacFadyen, J. G., Chang, W. H., Ballantyne, C., et al. (2017). Antiinflammatory therapy with canakinumab for atherosclerotic disease. New England Journal of Medicine,377(12), 1119–1131.PubMed
11.
Zurück zum Zitat Zheng, H., Fletcher, D., Kozak, W., Jiang, M., Hofmann, K. J., Conn, C. A., et al. (1995). Resistance to fever induction and impaired acute-phase response in interleukin-1 beta-deficient mice. Immunity,3(1), 9–19.PubMed Zheng, H., Fletcher, D., Kozak, W., Jiang, M., Hofmann, K. J., Conn, C. A., et al. (1995). Resistance to fever induction and impaired acute-phase response in interleukin-1 beta-deficient mice. Immunity,3(1), 9–19.PubMed
12.
Zurück zum Zitat Abderrazak, A., Couchie, D., Mahmood, D. F., Elhage, R., Vindis, C., Laffargue, M., et al. (2015). Antiinflammatory and antiatherogenic effects of the NLRP-3 inflammasome inhibitor arglabin in ApoE2.Ki mice fed a high-fat diet. Circulation,131(12), 1061–1070.PubMed Abderrazak, A., Couchie, D., Mahmood, D. F., Elhage, R., Vindis, C., Laffargue, M., et al. (2015). Antiinflammatory and antiatherogenic effects of the NLRP-3 inflammasome inhibitor arglabin in ApoE2.Ki mice fed a high-fat diet. Circulation,131(12), 1061–1070.PubMed
13.
Zurück zum Zitat Chang, W. T., Dao, J., & Shao, Z. H. (2005). Hawthorn: Potential roles in cardiovascular disease. The American Journal of Chinese Medicine,33(1), 1–10.PubMed Chang, W. T., Dao, J., & Shao, Z. H. (2005). Hawthorn: Potential roles in cardiovascular disease. The American Journal of Chinese Medicine,33(1), 1–10.PubMed
14.
Zurück zum Zitat Wang, J., Xiong, X., & Feng, B. (2013). Effect of crataegus usage in cardiovascular disease prevention: An evidence-based approach. Evidence-Based Complement Alternat Med.,2013, 149363. Wang, J., Xiong, X., & Feng, B. (2013). Effect of crataegus usage in cardiovascular disease prevention: An evidence-based approach. Evidence-Based Complement Alternat Med.,2013, 149363.
15.
Zurück zum Zitat Nabavi, S. F., Habtemariam, S., Ahmed, T., Sureda, A., Daglia, M., Sobarzo-Sánchez, E., et al. (2015). Polyphenolic composition of Crataegus monogyna Jacq: From chemistry to medical applications. Nutrients,7(9), 708–728. Nabavi, S. F., Habtemariam, S., Ahmed, T., Sureda, A., Daglia, M., Sobarzo-Sánchez, E., et al. (2015). Polyphenolic composition of Crataegus monogyna Jacq: From chemistry to medical applications. Nutrients,7(9), 708–728.
16.
Zurück zum Zitat Gao, P., Li, S., Liu, K., Sun, C., Song, S., & Li, L. (2019). Antiplatelet aggregation and antithrombotic benefits of terpenes and flavones from hawthorn leaf extract isolated using the activity-guided Method. Food and Function,10(20), 859–866.PubMed Gao, P., Li, S., Liu, K., Sun, C., Song, S., & Li, L. (2019). Antiplatelet aggregation and antithrombotic benefits of terpenes and flavones from hawthorn leaf extract isolated using the activity-guided Method. Food and Function,10(20), 859–866.PubMed
17.
Zurück zum Zitat Liu, P., Yang, B., & Kallio, H. (2010). Characterization of phenolic compounds in Chinese hawthorn (Crataegus pinnatifida Bge. var. major) fruit by high-performance liquid chromatography–electrospray ionization mass spectrometry. Food Chemistry,121(4), 1188–1197. Liu, P., Yang, B., & Kallio, H. (2010). Characterization of phenolic compounds in Chinese hawthorn (Crataegus pinnatifida Bge. var. major) fruit by high-performance liquid chromatography–electrospray ionization mass spectrometry. Food Chemistry,121(4), 1188–1197.
18.
Zurück zum Zitat Fong, H. H. S., & Bauman, J. L. (2002). Hawthorn. The Journal of Cardiovascular Nursing,16(4), 1–8.PubMed Fong, H. H. S., & Bauman, J. L. (2002). Hawthorn. The Journal of Cardiovascular Nursing,16(4), 1–8.PubMed
19.
Zurück zum Zitat Attard, E., & Attard, H. (2006). The potential angiotensin-converting enzyme inhibitory activity of oleanolic acid in the hydroethanolic extract of Crataegus monogyna Jacq. Natural Product Communications,1, 381–386. Attard, E., & Attard, H. (2006). The potential angiotensin-converting enzyme inhibitory activity of oleanolic acid in the hydroethanolic extract of Crataegus monogyna Jacq. Natural Product Communications,1, 381–386.
20.
Zurück zum Zitat Petkov, E., Nikolov, N., & Uzunov, P. (1981). Inhibitory effect of some flavonoids and flavonoid mixtures on cyclic AMP phosphodiesterase activity of rat heart. Planta Medica,43(2), 183–186.PubMed Petkov, E., Nikolov, N., & Uzunov, P. (1981). Inhibitory effect of some flavonoids and flavonoid mixtures on cyclic AMP phosphodiesterase activity of rat heart. Planta Medica,43(2), 183–186.PubMed
21.
Zurück zum Zitat Schwinger, R. H., Pietsch, M., Frank, K., & Brixius, K. (2000). Crataegus special extract WS 1442 increases force of contraction in human myocardium cAMP-independently. Journal of Cardiovascular Pharmacology,35(5), 700–707.PubMed Schwinger, R. H., Pietsch, M., Frank, K., & Brixius, K. (2000). Crataegus special extract WS 1442 increases force of contraction in human myocardium cAMP-independently. Journal of Cardiovascular Pharmacology,35(5), 700–707.PubMed
22.
Zurück zum Zitat Chen, Z. Y., Zhang, Z. S., Kwan, K. Y., Zhu, M., Ho, W. K., & Huang, Y. (1998). Endothelium-dependent relaxation induced by hawthorn extract in rat mesenteric artery. Life Sciences,63(22), 1983–1991.PubMed Chen, Z. Y., Zhang, Z. S., Kwan, K. Y., Zhu, M., Ho, W. K., & Huang, Y. (1998). Endothelium-dependent relaxation induced by hawthorn extract in rat mesenteric artery. Life Sciences,63(22), 1983–1991.PubMed
23.
Zurück zum Zitat Kim, S. H., Kang, K. W., Kim, K. W., & Kim, N. D. (2000). Procyanidins in crataegus extract evoke endothelium-dependent vasorelaxation in rat aorta. Life Sciences,67(2), 121–131.PubMed Kim, S. H., Kang, K. W., Kim, K. W., & Kim, N. D. (2000). Procyanidins in crataegus extract evoke endothelium-dependent vasorelaxation in rat aorta. Life Sciences,67(2), 121–131.PubMed
24.
Zurück zum Zitat Pittler, M. H., Schmidt, K., & Ernst, E. (2008). Hawthorn extract for treating chronic heart failure. Cochrane Database of Systematic Reviews,23(1), CD005312. Pittler, M. H., Schmidt, K., & Ernst, E. (2008). Hawthorn extract for treating chronic heart failure. Cochrane Database of Systematic Reviews,23(1), CD005312.
25.
Zurück zum Zitat Veveris, M., Koch, E., & Chatterjee, S. S. (2004). Crataegus special extract WS 1442 improves cardiac function and reduces infarct size in a rat model of prolonged coronary ischemia and reperfusion. Life Sciences,74, 1945–1955.PubMed Veveris, M., Koch, E., & Chatterjee, S. S. (2004). Crataegus special extract WS 1442 improves cardiac function and reduces infarct size in a rat model of prolonged coronary ischemia and reperfusion. Life Sciences,74, 1945–1955.PubMed
26.
Zurück zum Zitat Müller, A., Linke, W., Zhao, Y., & Klaus, W. (1996). Crataegus extract prolongs action potential duration in guinea-pig papillary muscle. Phytomedicine,3(3), 257–261.PubMed Müller, A., Linke, W., Zhao, Y., & Klaus, W. (1996). Crataegus extract prolongs action potential duration in guinea-pig papillary muscle. Phytomedicine,3(3), 257–261.PubMed
27.
Zurück zum Zitat Müller, A., Linke, W., & Klaus, W. (1999). Crataegus extract blocks potassium currents in guinea pig ventricular cardiac myocytes. Planta Medica,65(4), 335–339.PubMed Müller, A., Linke, W., & Klaus, W. (1999). Crataegus extract blocks potassium currents in guinea pig ventricular cardiac myocytes. Planta Medica,65(4), 335–339.PubMed
28.
Zurück zum Zitat Garjani, A., Nazemiyeh, H., Maleki, N., & Valizadeh, H. (2000). Effects of extracts from flowering tops of Crataegus meyeri A. Pojark. on ischaemic arrhythmias in anaesthetized rats. Phytotherapy Research,14(6), 428–431.PubMed Garjani, A., Nazemiyeh, H., Maleki, N., & Valizadeh, H. (2000). Effects of extracts from flowering tops of Crataegus meyeri A. Pojark. on ischaemic arrhythmias in anaesthetized rats. Phytotherapy Research,14(6), 428–431.PubMed
29.
Zurück zum Zitat Rajendran, S., Deepalakshm, P. D., Parasakthy, K., Devaraj, H., & Devaraj, S. N. (1996). Effect of tincture of Crataegus on the LDL-receptor activity of hepatic plasma membrane of rats fed an atherogenic diet. Atherosclerosis.,123(1–2), 235–241.PubMed Rajendran, S., Deepalakshm, P. D., Parasakthy, K., Devaraj, H., & Devaraj, S. N. (1996). Effect of tincture of Crataegus on the LDL-receptor activity of hepatic plasma membrane of rats fed an atherogenic diet. Atherosclerosis.,123(1–2), 235–241.PubMed
30.
Zurück zum Zitat Zhang, Z., Ho, W. K., Huang, Y., James, A. E., Lam, L. W., & Chen, Z. Y. (2002). Hawthorn fruit is hypolipidemic in rabbits fed a high cholesterol diet. The Journal of Nutrition,132(1), 5–10.PubMed Zhang, Z., Ho, W. K., Huang, Y., James, A. E., Lam, L. W., & Chen, Z. Y. (2002). Hawthorn fruit is hypolipidemic in rabbits fed a high cholesterol diet. The Journal of Nutrition,132(1), 5–10.PubMed
31.
Zurück zum Zitat Shih, C. C., Lin, C. H., Lin, Y. J., & Wu, J. B. (2013). Validation of the antidiabetic and hypolipidemic effects of hawthorn by assessment of gluconeogenesis and lipogenesis related genes and AMP-activated protein kinase phosphorylation. Evidence-Based Complementary and Alternative Medicine.,2013, 597067.PubMedPubMedCentral Shih, C. C., Lin, C. H., Lin, Y. J., & Wu, J. B. (2013). Validation of the antidiabetic and hypolipidemic effects of hawthorn by assessment of gluconeogenesis and lipogenesis related genes and AMP-activated protein kinase phosphorylation. Evidence-Based Complementary and Alternative Medicine.,2013, 597067.PubMedPubMedCentral
32.
Zurück zum Zitat Kao, E., Wang, C., Lin, W., Yin, Y., Wang, C., & Tseng, T. (2005). Anti-inflammatory potential of flavonoid contents from dried fruit of Crataegus pinnatifida in vitro and in vivo. Journal of Agricultural and Food Chemistry,53(2), 430–436.PubMed Kao, E., Wang, C., Lin, W., Yin, Y., Wang, C., & Tseng, T. (2005). Anti-inflammatory potential of flavonoid contents from dried fruit of Crataegus pinnatifida in vitro and in vivo. Journal of Agricultural and Food Chemistry,53(2), 430–436.PubMed
33.
Zurück zum Zitat Chu, C., Lee, M., Liao, C., Lin, W., Yin, Y., & Tseng, T. (2003). Inhibitory effect of hot water extract from dried fruit of Crataegus pinnatifida on low-density lipoprotein (LDL) oxidation in cell and cell-free systems. Journal of Agricultural and Food Chemistry,51(26), 7583.PubMed Chu, C., Lee, M., Liao, C., Lin, W., Yin, Y., & Tseng, T. (2003). Inhibitory effect of hot water extract from dried fruit of Crataegus pinnatifida on low-density lipoprotein (LDL) oxidation in cell and cell-free systems. Journal of Agricultural and Food Chemistry,51(26), 7583.PubMed
34.
Zurück zum Zitat Fu, J. H., Zheng, Y. Q., Li, P., Li, X. Z., Shang, X. H., & Liu, J. X. (2013). Hawthorn leaves flavonoids decreases inflammation related to acute myocardialischemia/reperfusion in anesthetized dogs. Chinese Journal of Integrative Medicine,19(8), 582–588.PubMed Fu, J. H., Zheng, Y. Q., Li, P., Li, X. Z., Shang, X. H., & Liu, J. X. (2013). Hawthorn leaves flavonoids decreases inflammation related to acute myocardialischemia/reperfusion in anesthetized dogs. Chinese Journal of Integrative Medicine,19(8), 582–588.PubMed
35.
Zurück zum Zitat Ljubuncic, P., Portnaya, I., Cogan, U., Azaizeh, H., & Bomzon, A. (2005). Antioxidant activity of Crataegus aronia aqueous extract used in traditional Arab medicine in Israel. Journal of Ethnopharmacology,101(1–3), 153–161.PubMed Ljubuncic, P., Portnaya, I., Cogan, U., Azaizeh, H., & Bomzon, A. (2005). Antioxidant activity of Crataegus aronia aqueous extract used in traditional Arab medicine in Israel. Journal of Ethnopharmacology,101(1–3), 153–161.PubMed
36.
Zurück zum Zitat Shatoor, A. S. (2011). Acute and sub-acute toxicity of Crataegus aronia syn Azarolus (L.) whole plant aqueous extract in wistar rats. American Journal of Pharmacology Toxicology.,6, 37–45. Shatoor, A. S. (2011). Acute and sub-acute toxicity of Crataegus aronia syn Azarolus (L.) whole plant aqueous extract in wistar rats. American Journal of Pharmacology Toxicology.,6, 37–45.
37.
Zurück zum Zitat Shatoor, A. S. (2013). In vivo hemodynamic and electrocardiographic changes following Crataegus aronia syn. Azarolus (L.) administration to normotensive Wistar rats. Saudi Medical Journal,34(2), 123–134.PubMed Shatoor, A. S. (2013). In vivo hemodynamic and electrocardiographic changes following Crataegus aronia syn. Azarolus (L.) administration to normotensive Wistar rats. Saudi Medical Journal,34(2), 123–134.PubMed
38.
Zurück zum Zitat Humayed, S. (2017). Protective and therapeutic effects of Crataegus aronia in non-alcoholic fatty liver disease. Archives of Physiology and Biochemistry,123(1), 23–30.PubMed Humayed, S. (2017). Protective and therapeutic effects of Crataegus aronia in non-alcoholic fatty liver disease. Archives of Physiology and Biochemistry,123(1), 23–30.PubMed
39.
Zurück zum Zitat Dallak, M. (2018). Crataegus aronia enhances sperm parameters and preserves testicular architecture in both control and non-alcoholic fatty liver disease-induced rats. Pharmaceutical Biology,56(1), 535–547.PubMedPubMedCentral Dallak, M. (2018). Crataegus aronia enhances sperm parameters and preserves testicular architecture in both control and non-alcoholic fatty liver disease-induced rats. Pharmaceutical Biology,56(1), 535–547.PubMedPubMedCentral
40.
Zurück zum Zitat Mostafa, D. G., Khaleel, E. F., & Abdel-Aleem, G. A. (2018). Inhibition of the hepatic glucose output is responsible for the hypoglycemic effect of Crataegus aronia against type 2 diabetes mellitus in rats. Archives of Biological Sciences,70(2), 277–287. Mostafa, D. G., Khaleel, E. F., & Abdel-Aleem, G. A. (2018). Inhibition of the hepatic glucose output is responsible for the hypoglycemic effect of Crataegus aronia against type 2 diabetes mellitus in rats. Archives of Biological Sciences,70(2), 277–287.
41.
Zurück zum Zitat Shatoor, A. S., Al Humayed, S., Alkhateeb, M. A., Shatoor, A. K., Aldera, H., Alassiri, M., et al. (2019). Crataegus Aronia protects and reverses vascular inflammation in a high-fat diet rat model by an antioxidant mechanism and modulating serum levels of oxidized low-density lipoprotein. Pharmaceutical Biology,57(1), 38–48.PubMedPubMedCentral Shatoor, A. S., Al Humayed, S., Alkhateeb, M. A., Shatoor, A. K., Aldera, H., Alassiri, M., et al. (2019). Crataegus Aronia protects and reverses vascular inflammation in a high-fat diet rat model by an antioxidant mechanism and modulating serum levels of oxidized low-density lipoprotein. Pharmaceutical Biology,57(1), 38–48.PubMedPubMedCentral
42.
Zurück zum Zitat Begue, G., Douillard, A., Galbes, O., Rossano, B., Vernus, B., Candau, R., et al. (2013). Activation of rat skeletal muscle IL-6/STAT1/STAT3 dependent gene expression in resistance exercise linked to hypertrophy. PLoS ONE,8, e57141.PubMedPubMedCentral Begue, G., Douillard, A., Galbes, O., Rossano, B., Vernus, B., Candau, R., et al. (2013). Activation of rat skeletal muscle IL-6/STAT1/STAT3 dependent gene expression in resistance exercise linked to hypertrophy. PLoS ONE,8, e57141.PubMedPubMedCentral
43.
Zurück zum Zitat Boaru, S. G., Borkham-Kamphorst, E., Tihaa, L., Haas, U., & Weiskirchen, R. (2012). Expression analysis of inflammasomes in experimental models of inflammatory and fibrotic liver disease. Journal of Inflammation,9(1), 49.PubMed Boaru, S. G., Borkham-Kamphorst, E., Tihaa, L., Haas, U., & Weiskirchen, R. (2012). Expression analysis of inflammasomes in experimental models of inflammatory and fibrotic liver disease. Journal of Inflammation,9(1), 49.PubMed
44.
Zurück zum Zitat Veres-Székely, A., Pap, D., Sziksz, E., Jávorszky, E., Rokonay, R., Lippai, R., et al. (2017). Selective measurement of α smooth muscle actin: Why β-actin can not be used as a housekeeping gene when tissue fibrosis occurs. BMC Molecular Biology,18(1), 12.PubMedPubMedCentral Veres-Székely, A., Pap, D., Sziksz, E., Jávorszky, E., Rokonay, R., Lippai, R., et al. (2017). Selective measurement of α smooth muscle actin: Why β-actin can not be used as a housekeeping gene when tissue fibrosis occurs. BMC Molecular Biology,18(1), 12.PubMedPubMedCentral
45.
Zurück zum Zitat Xie, S., Xie, S., Liu, B., Fu, S., Wang, W., Yin, Y., et al. (2014). GLP-2 suppresses LPS-induced inflammation in macrophages by inhibiting ERK phosphorylation and NF-κB activation. Cellular Physiology and Biochemistry,34(2), 590–602.PubMed Xie, S., Xie, S., Liu, B., Fu, S., Wang, W., Yin, Y., et al. (2014). GLP-2 suppresses LPS-induced inflammation in macrophages by inhibiting ERK phosphorylation and NF-κB activation. Cellular Physiology and Biochemistry,34(2), 590–602.PubMed
46.
Zurück zum Zitat Soromou, L. W., Zhang, Z., Li, R., Chen, N., Guo, W., Huo, M., et al. (2012). Regulation of inflammatory cytokines in lipopolysaccharide-stimulated RAW 264.7 murine macrophage by 7-O-methyl-naringenin. Molecules,17(3), 3574–3585.PubMedPubMedCentral Soromou, L. W., Zhang, Z., Li, R., Chen, N., Guo, W., Huo, M., et al. (2012). Regulation of inflammatory cytokines in lipopolysaccharide-stimulated RAW 264.7 murine macrophage by 7-O-methyl-naringenin. Molecules,17(3), 3574–3585.PubMedPubMedCentral
47.
Zurück zum Zitat Sheehan, D. C., & Hrapchak, B. B. (1987). Theory and practice of histotechnology (2nd ed.). Columbus: Battelle Memorial Institute. Sheehan, D. C., & Hrapchak, B. B. (1987). Theory and practice of histotechnology (2nd ed.). Columbus: Battelle Memorial Institute.
48.
Zurück zum Zitat Li, D., & Mehta, J. L. (2000). Upregulation of endothelial receptor for oxidized LDL (LOX-1) by oxidized LDL and implications in apoptosis of coronary artery endothelial cells: Evidence from use of antisense LOX-1 mRNA and chemical inhibitors. Arteriosclerosis, Thrombosis, and Vascular Biology,20(4), 1116–1122.PubMed Li, D., & Mehta, J. L. (2000). Upregulation of endothelial receptor for oxidized LDL (LOX-1) by oxidized LDL and implications in apoptosis of coronary artery endothelial cells: Evidence from use of antisense LOX-1 mRNA and chemical inhibitors. Arteriosclerosis, Thrombosis, and Vascular Biology,20(4), 1116–1122.PubMed
49.
Zurück zum Zitat Ding, Z., Liu, S., Wang, X., Dai, Y., Khaidakov, M., Deng, X., et al. (2014). LOX-1, mtDNA damage, and NLRP-3 inflammasome activation in macrophages: Implications in atherogenesis. Cardiovascular Research,103(4), 619–628.PubMedPubMedCentral Ding, Z., Liu, S., Wang, X., Dai, Y., Khaidakov, M., Deng, X., et al. (2014). LOX-1, mtDNA damage, and NLRP-3 inflammasome activation in macrophages: Implications in atherogenesis. Cardiovascular Research,103(4), 619–628.PubMedPubMedCentral
50.
Zurück zum Zitat Ferreiro, D. U., & Komives, E. A. (2010). Molecular mechanisms of system control of NF-κB signaling by IκBα. Biochemistry,49(8), 1560–1567.PubMedPubMedCentral Ferreiro, D. U., & Komives, E. A. (2010). Molecular mechanisms of system control of NF-κB signaling by IκBα. Biochemistry,49(8), 1560–1567.PubMedPubMedCentral
51.
Zurück zum Zitat Groot, P. H., van Vlijmen, B. J., Benson, G. M., Hofker, M. H., Schiffelers, R., Vidgeon-Hart, M., et al. (1996). Quantitative assessment of aortic atherosclerosis in APOE3 Leiden transgenic mice and its relationship to serum cholesterol exposure. Arteriosclerosis, Thrombosis, and Vascular Biology,16(8), 926–933.PubMed Groot, P. H., van Vlijmen, B. J., Benson, G. M., Hofker, M. H., Schiffelers, R., Vidgeon-Hart, M., et al. (1996). Quantitative assessment of aortic atherosclerosis in APOE3 Leiden transgenic mice and its relationship to serum cholesterol exposure. Arteriosclerosis, Thrombosis, and Vascular Biology,16(8), 926–933.PubMed
52.
Zurück zum Zitat Jawien, J., Csanyi, G., Gajda, M., Mateuszuk, L., Lomnicka, M., Korbut, R., et al. (2007). Ticlopidine attenuates progression of atherosclerosis in apolipoprotein E and low density lipoprotein receptor double knockout mice. European Journal of Pharmacology,556(1–3), 129–135.PubMed Jawien, J., Csanyi, G., Gajda, M., Mateuszuk, L., Lomnicka, M., Korbut, R., et al. (2007). Ticlopidine attenuates progression of atherosclerosis in apolipoprotein E and low density lipoprotein receptor double knockout mice. European Journal of Pharmacology,556(1–3), 129–135.PubMed
53.
Zurück zum Zitat Wrobel, P. T., Mateuszuk, L., Chlopicki, S., Malek, K., & Baranska, M. (2011). Imaging of lipids in atherosclerotic lesion in aorta from ApoE/LDLR-/- mice by FT-IR spectroscopy and hierarchical cluster analysis. Analyst.,136(24), 5247–5255. Wrobel, P. T., Mateuszuk, L., Chlopicki, S., Malek, K., & Baranska, M. (2011). Imaging of lipids in atherosclerotic lesion in aorta from ApoE/LDLR-/- mice by FT-IR spectroscopy and hierarchical cluster analysis. Analyst.,136(24), 5247–5255.
54.
Zurück zum Zitat Lloyd, D. J., Helmering, J., Kaufman, S. A., Turk, J., Silva, M., Vasquez, S., et al. (2011). A volumetric method for quantifying atherosclerosis in mice by using microCT:comparison to en face. PLoS ONE,6(4), e18800.PubMedPubMedCentral Lloyd, D. J., Helmering, J., Kaufman, S. A., Turk, J., Silva, M., Vasquez, S., et al. (2011). A volumetric method for quantifying atherosclerosis in mice by using microCT:comparison to en face. PLoS ONE,6(4), e18800.PubMedPubMedCentral
55.
Zurück zum Zitat Mackness, M. I., Arrol, S., & Durrington, P. N. (1991). Paraoxonase prevents accumulation of lipoperoxides in low-density lipoprotein. FEBS Letters,286(1–2), 152–154.PubMed Mackness, M. I., Arrol, S., & Durrington, P. N. (1991). Paraoxonase prevents accumulation of lipoperoxides in low-density lipoprotein. FEBS Letters,286(1–2), 152–154.PubMed
56.
Zurück zum Zitat Khalil, R., Abuharfeil, N., & Shabsoug, B. (2008). The effect of Crataegus Aronica aqueous extract in rabbits fed with high cholesterol diet. European Journal of Scientific Research.,22(3), 352–360. Khalil, R., Abuharfeil, N., & Shabsoug, B. (2008). The effect of Crataegus Aronica aqueous extract in rabbits fed with high cholesterol diet. European Journal of Scientific Research.,22(3), 352–360.
57.
Zurück zum Zitat Pirillo, A., Norata, G. D., & Catapano, A. L. (2013). LOX-1, oxLDL, and atherosclerosis. Mediators of Inflammation,2013, 152786.PubMedPubMedCentral Pirillo, A., Norata, G. D., & Catapano, A. L. (2013). LOX-1, oxLDL, and atherosclerosis. Mediators of Inflammation,2013, 152786.PubMedPubMedCentral
58.
Zurück zum Zitat Kotla, S., Singh, N. K., & Rao, G. N. (2017). ROS via BTK-p300-STAT1-PPARg signaling activation mediates cholesterol crystals-induced CD36 expression and foam cell formation. Redox Biology,11, 350–364.PubMed Kotla, S., Singh, N. K., & Rao, G. N. (2017). ROS via BTK-p300-STAT1-PPARg signaling activation mediates cholesterol crystals-induced CD36 expression and foam cell formation. Redox Biology,11, 350–364.PubMed
59.
Zurück zum Zitat Thacker, S. G., Zarzour, A., Chen, Y., Alcicek, M. S., Freeman, L. A., Sviridov, D. O., et al. (2016). High-density lipoprotein reduces inflammation from cholesterol crystals by inhibiting inflammasome activation. Immunology,149(3), 306–319.PubMedPubMedCentral Thacker, S. G., Zarzour, A., Chen, Y., Alcicek, M. S., Freeman, L. A., Sviridov, D. O., et al. (2016). High-density lipoprotein reduces inflammation from cholesterol crystals by inhibiting inflammasome activation. Immunology,149(3), 306–319.PubMedPubMedCentral
60.
Zurück zum Zitat Zhang, Z., Chang, Q., Zhu, M., Huang, Y., Ho, W. K., & Chen, Z. (2001). Characterization of antioxidants present in hawthorn fruits. The Journal of Nutritional Biochemistry,12(3), 144–152.PubMed Zhang, Z., Chang, Q., Zhu, M., Huang, Y., Ho, W. K., & Chen, Z. (2001). Characterization of antioxidants present in hawthorn fruits. The Journal of Nutritional Biochemistry,12(3), 144–152.PubMed
61.
Zurück zum Zitat Bahri-Sahloul, R., Ben Fredj, R., Boughalleb, N., Shriaa, J., Saguem, S., Hilbert, J. L., et al. (2014). Phenolic composition and antioxidant and antimicrobial activities of extracts obtained from Crataegus azarolus L. var. aronia (Willd.) Batt Ovaries Calli. Journal of Botany.,2014, 623651. Bahri-Sahloul, R., Ben Fredj, R., Boughalleb, N., Shriaa, J., Saguem, S., Hilbert, J. L., et al. (2014). Phenolic composition and antioxidant and antimicrobial activities of extracts obtained from Crataegus azarolus L. var. aronia (Willd.) Batt Ovaries Calli. Journal of Botany.,2014, 623651.
62.
Zurück zum Zitat Liu, P., Kallio, H., & Yang, B. (2011). Phenolic compounds in hawthorn (Crataegus grayana) fruits and leaves and changes during fruit ripening. Journal of Agricultural and Food Chemistry,59(20), 11141–11149.PubMed Liu, P., Kallio, H., & Yang, B. (2011). Phenolic compounds in hawthorn (Crataegus grayana) fruits and leaves and changes during fruit ripening. Journal of Agricultural and Food Chemistry,59(20), 11141–11149.PubMed
63.
Zurück zum Zitat Gao, P. Y., Li, L. Z., Liu, L. C., Sun, C., Sun, X., Wu, T. N., et al. (2017). Natural terpenoid glycosides with in vitro/vivo antithrombotic profiles from the leaves of Crataegus pinnatifida. RSC Advances,76, 48466–48474. Gao, P. Y., Li, L. Z., Liu, L. C., Sun, C., Sun, X., Wu, T. N., et al. (2017). Natural terpenoid glycosides with in vitro/vivo antithrombotic profiles from the leaves of Crataegus pinnatifida. RSC Advances,76, 48466–48474.
64.
Zurück zum Zitat Lin, Y., Vermeer, M. A., & Trautwein, E. A. (2011). Triterpenic acids present in hawthorn lower plasma cholesterol by inhibiting intestinal ACAT activity in hamsters. Evidence-Based Complementary and Alternative Medicine.,2011, 801272.PubMed Lin, Y., Vermeer, M. A., & Trautwein, E. A. (2011). Triterpenic acids present in hawthorn lower plasma cholesterol by inhibiting intestinal ACAT activity in hamsters. Evidence-Based Complementary and Alternative Medicine.,2011, 801272.PubMed
65.
Zurück zum Zitat de Whalley, C. V., Rankin, S. M., Hoult, J. R., Jessup, W., & Leake, D. S. (1990). Flavonoids inhibit the oxidative modification of low density lipoproteins by macrophages. Biochemical Pharmacology,39(11), 1743–1750.PubMed de Whalley, C. V., Rankin, S. M., Hoult, J. R., Jessup, W., & Leake, D. S. (1990). Flavonoids inhibit the oxidative modification of low density lipoproteins by macrophages. Biochemical Pharmacology,39(11), 1743–1750.PubMed
66.
Zurück zum Zitat Bahri-Sahloul, R., Ammar, S., Fredj, R. B., Saguem, S., Grec, S., Trotin, F., et al. (2009). Polyphenol contents and antioxidant activities of extracts from flowers of two Crataegus azarolus L. varieties. Pakistan Journal of Biological Sciences,12(9), 660–668.PubMed Bahri-Sahloul, R., Ammar, S., Fredj, R. B., Saguem, S., Grec, S., Trotin, F., et al. (2009). Polyphenol contents and antioxidant activities of extracts from flowers of two Crataegus azarolus L. varieties. Pakistan Journal of Biological Sciences,12(9), 660–668.PubMed
67.
Zurück zum Zitat Meng, S., Cao, J., Feng, Q., Peng, J., & Hu, Y. (2013). Roles of chlorogenic acid in regulating glucose and lipids metabolism: A review. Evidence-Based Complementary and Alternative Medicine,801457, 31. Meng, S., Cao, J., Feng, Q., Peng, J., & Hu, Y. (2013). Roles of chlorogenic acid in regulating glucose and lipids metabolism: A review. Evidence-Based Complementary and Alternative Medicine,801457, 31.
68.
Zurück zum Zitat Quettier-Deleu, C., Voiselle, G., Fruchart, J. C., Duriez, P., Teissier, E., Bailleul, F., et al. (2003). Hawthorn extracts inhibit LDL oxidation. Pharmazie.,58(8), 577–581.PubMed Quettier-Deleu, C., Voiselle, G., Fruchart, J. C., Duriez, P., Teissier, E., Bailleul, F., et al. (2003). Hawthorn extracts inhibit LDL oxidation. Pharmazie.,58(8), 577–581.PubMed
Metadaten
Titel
The Protective Effect of Crataegus aronia Against High-Fat Diet-Induced Vascular Inflammation in Rats Entails Inhibition of the NLRP-3 Inflammasome Pathway
verfasst von
Abdullah S. Shatoor
Suliman Al Humayed
Publikationsdatum
11.06.2019
Verlag
Springer US
Erschienen in
Cardiovascular Toxicology
Print ISSN: 1530-7905
Elektronische ISSN: 1559-0259
DOI
https://doi.org/10.1007/s12012-019-09534-9