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The protective effects of procyanidin supplementation on PM2.5-induced acute cardiac injury in rats

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Abstract

Objective

Numerous epidemiological and experimental studies have indicated that ambient fine particulate matter (PM2.5) exposure can lead to myocardial injury by inhibiting oxidative stress and apoptosis. The effects of procyanidin (PC) on PM2.5-induced cardiovascular diseases (CVDs) are still unknown. The purpose of this study was to explore the protective effect of PC supplementation on PM2.5-induced oxidative stress and cardiomyocyte apoptosis in rats.

Method

Rats were treated by gavage with three different PC concentrations (50, 100 and 200 mg/kg) for 21 days prior to exposure to 10 mg/kg PM2.5 suspension liquid by intratracheal instillation every other day for three times. We determined myocardial reactive oxygen species (ROS) and malondialdehyde (MDA) levels. Superoxide dismutase (SOD) and glutathione peroxidase (GSH-Px) activities in the myocardium were measured. The expression levels of apoptosis-related proteins, including p-Akt/Akt, Bcl-2, caspase-3 and Bax, were determined. In addition, histopathological examination was used to evaluate cardiac injury.

Results

PM2.5 exposure noticeably elevated the contents of MDA and ROS and decreased the activities of GSH-Px and SOD. PM2.5 exposure inhibited Bcl-2 expression and up-regulated caspase-3 and Bax expression in the myocardium of rats. The anti-apoptosis–related index p-Akt/Akt was reduced. Moreover, pretreatment with PC could attenuate these PM2.5-induced changes. However, remarkable differences in the protective effect of different PC doses did not exist.

Conclusions

The results indicated that PC supplementation could effectively attenuate the oxidative stress and apoptosis induced by PM2.5 in rat myocardial tissue.

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Data availability

All data generated or analysed during this study are included in this published article.

References

  • Al-Saad S, Donnem T, Al-Shibli K, Persson M, Bremnes RM, Busund LT (2009) Diverse prognostic roles of Akt isoforms, PTEN and PI3K in tumor epithelial cells and stromal compartment in non-small cell lung cancer. Anticancer Res 29:4175–83

    Google Scholar 

  • Azimzadeh O, Sievert W, Sarioglu H, Merl-Pham J, Yentrapalli R, Bakshi MV, Janik D, Ueffing M, Atkinson MJ, Multhoff G, Tapio S (2015) Integrative proteomics and targeted transcriptomics analyses in cardiac endothelial cells unravel mechanisms of long-term radiation-induced vascular dysfunction. J Proteome Res 14:1203–19

    Article  CAS  Google Scholar 

  • Bo L, Jiang S, **e Y, Kan H, Song W, Zhao J (2016) Effect of vitamin E and omega-3 fatty acids on protecting ambient PM2.5-induced inflammatory response and oxidative stress in vascular endothelial cells. PLoS One 11:e0152216

    Article  Google Scholar 

  • Burt S (2004) Essential oils: their antibacterial properties and potential applications in foods–a review. Int J Food Microbiol 94:223–53

    Article  CAS  Google Scholar 

  • Chen DM, Cai X, Kwik-Uribe CL, Zeng R, Zhu XZ (2006) Inhibitory effects of procyanidin B(2) dimer on lipid-laden macrophage formation. J Cardiovasc Pharmacol 48:54–70

    Article  CAS  Google Scholar 

  • Chen Y, Wang L, Liu T, Qiu Z, Qiu Y, Liu D (2021) Inhibitory effects of Panax ginseng glycoproteins in models of doxorubicin-induced cardiac toxicity in vivo and in vitro. Food Funct 12:10862–74

    Article  CAS  Google Scholar 

  • Crobeddu B, Aragao-Santiago L, Bui LC, Boland S, BaezaSquiban A (2017) Oxidative potential of particulate matter 2.5 as predictive indicator of cellular stress. Environ Pollut 230:125–33

    Article  CAS  Google Scholar 

  • Del Re DP, Amgalan D, Linkermann A, Liu Q, Kitsis RN (2019) Fundamental Mechanisms of Regulated Cell Death and Implications for Heart Disease. Physiol Rev 99:1765–817

    Article  Google Scholar 

  • Du X, Jiang S, Bo L, Liu J, Zeng X, **e Y, He Q, Ye X, Song W, Zhao J (2017) Combined effects of vitamin E and omega-3 fatty acids on protecting ambient PM2.5-induced cardiovascular injury in rats. Chemosphere 173:14–21

    Article  CAS  Google Scholar 

  • Fang J, Tang Y, Cheng X, Wang L, Cai C, Zhang X, Liu S, Li P (2019) Exenatide alleviates adriamycin-induced heart dysfunction in mice: modulation of oxidative stress, apoptosis and inflammation. Chem Biol Interact 304:186–93

    Article  CAS  Google Scholar 

  • Fukai T, Ushio-Fukai M (2011) Superoxide dismutases: role in redox signaling, vascular function, and diseases. Antioxid Redox Signal 15:1583–606

    Article  CAS  Google Scholar 

  • Galiana-Simal A, Olivares-Alvaro E, Klett-Mingo M, Ruiz-Roso MB, Ballesteros S, de Las Heras N, Fuller PJ, Lahera V, Martin-Fernandez B (2016) Proanthocyanidins block aldosterone-dependent up-regulation of cardiac gamma ENaC and Nedd4–2 inactivation via SGK1. J Nutr Biochem 37:13–19

    Article  CAS  Google Scholar 

  • Garrido C, Galluzzi L, Brunet M, Puig PE, Didelot C, Kroemer G (2006) Mechanisms of cytochrome c release from mitochondria. Cell Death Differ 13:1423–33

    Article  CAS  Google Scholar 

  • Gorr MW, Velten M, Nelin TD, Youtz DJ, Sun Q, Wold LE (2014) Early life exposure to air pollution induces adult cardiac dysfunction. Am J Physiol Heart Circ Physiol 307:H1353-60

    Article  CAS  Google Scholar 

  • Huang RJ, Zhang Y, Bozzetti C, Ho KF, Cao JJ, Han Y, Daellenbach KR, Slowik JG, Platt SM, Canonaco F, Zotter P, Wolf R, Pieber SM, Bruns EA, Crippa M, Ciarelli G, Piazzalunga A, Schwikowski M, Abbaszade G, Schnelle-Kreis J, Zimmermann R, An Z, Szidat S, Baltensperger U, El Haddad I, Prevot AS (2014) High secondary aerosol contribution to particulate pollution during haze events in China. Nature 514:218–22

    Article  CAS  Google Scholar 

  • Huang K, Shi C, Min J, Li L, Zhu T, Yu H, Deng H (2019) Study on the mechanism of curcumin regulating lung injury induced by outdoor fine particulate matter (PM2.5). Mediators Inflamm 2019:8613523

    Article  Google Scholar 

  • Jiang Y, Wang C, Lin Z, Niu Y, **a Y, Liu C, Chen C, Ge Y, Wang W, Yin G, Cai J, Chen B, Chen R, Kan H (2019) Alleviated systemic oxidative stress effects of combined atmospheric oxidant capacity by fish oil supplementation: a randomized, double-blinded, placebo-controlled trial. Ecotoxicol Environ Saf 184

  • Karimi GK, Antoniades C, Nicholls SJ, Channon KM, Figtree GA (2015) Redox biomarkers in cardiovascular medicine. Eur Heart J 36.1576–82, 82a-b.

  • Karthikeyan K, Bai BR, Devaraj SN (2007) Efficacy of grape seed proanthocyanidins on serum and heart tissue lipids in rats subjected to isoproterenol-induced myocardial injury. Vascul Pharmacol 47:295–301

    Article  CAS  Google Scholar 

  • Kim R (2005) Unknotting the roles of Bcl-2 and Bcl-xL in cell death. Biochem Biophys Res Commun 333:336–43

    Article  CAS  Google Scholar 

  • Lawrence SP, Holman GD, Koumanov F (2010) Translocation of the Na+/H+ exchanger 1 (NHE1) in cardiomyocyte responses to insulin and energy-status signalling. Biochem J 432:515–23

    Article  CAS  Google Scholar 

  • Li R, Kou X, Geng H, **e J, Tian J, Cai Z, Dong C (2015) Mitochondrial damage: an important mechanism of ambient PM2.5 exposure-induced acute heart injury in rats. J Hazard Mater 287:392–401

    Article  CAS  Google Scholar 

  • Li J, Li H, Li H, Guo W, An Z, Zeng X, Li W, Li H, Song J, Wu W (2019) Amelioration of PM2.5-induced lung toxicity in rats by nutritional supplementation with fish oil and Vitamin E. Respir Res 20:76

    Article  Google Scholar 

  • Liang CS, Duan FK, He KB, Ma YL (2016) Review on recent progress in observations, source identifications and countermeasures of PM2.5. Environ Int 86:150–70

    Article  CAS  Google Scholar 

  • Lin HH, Chen JH, Huang CC, Wang CJ (2007) Apoptotic effect of 3,4-dihydroxybenzoic acid on human gastric carcinoma cells involving JNK/p38 MAPK signaling activation. Int J Cancer 120:2306–16

    Article  CAS  Google Scholar 

  • Lin Z, Chen R, Jiang Y, **a Y, Niu Y, Wang C, Liu C, Chen C, Ge Y, Wang W, Yin G, Cai J, Clement V, Xu X, Chen B, Chen H, Kan H (2019) Cardiovascular benefits of fish-oil supplementation against fine particulate air pollution in China. J Am Coll Cardiol 73:2076–85

    Article  CAS  Google Scholar 

  • Long MH, Zhu XM, Wang Q, Chen Y, Gan XD, Li F, Fu WL, **ng WW, Xu DQ, Xu DG (2020) PM2.5 exposure induces vascular dysfunction via NO generated by iNOS in lung of ApoE-/- mouse. Int J Biol Sci 16:49–60

    Article  CAS  Google Scholar 

  • LoPiccolo J, Blumenthal GM, Bernstein WB, Dennis PA (2008) Targeting the PI3K/Akt/mTOR pathway: effective combinations and clinical considerations. Drug Resist Updat 11:32–50

    Article  CAS  Google Scholar 

  • Mantena SK, Katiyar SK (2006) Grape seed proanthocyanidins inhibit UV-radiation-induced oxidative stress and activation of MAPK and NF-kappaB signaling in human epidermal keratinocytes. Free Radic Biol Med 40:1603–14

    Article  CAS  Google Scholar 

  • Pang Y, Abeysinghe IS, He J, He X, Huhman D, Mewan KM, Sumner LW, Yun J, Dixon RA (2013) Functional characterization of proanthocyanidin pathway enzymes from tea and their application for metabolic engineering. Plant Physiol 161:1103–16

    Article  CAS  Google Scholar 

  • Rajagopalan S, Al-Kindi SG, Brook RD (2018) Air pollution and cardiovascular disease: JACC state-of-the-art review. J Am Coll Cardiol 72:2054–70

    Article  CAS  Google Scholar 

  • Rauf A, Imran M, Abu-Izneid T, Ul HI, Patel S, Pan X, Naz S, Sanches Silva A, Saeed F, Rasul Suleria HA (2019) Proanthocyanidins: a comprehensive review. Biomed Pharmacother 116:108999

    Article  CAS  Google Scholar 

  • Reed J (2002) Cranberry flavonoids, atherosclerosis and cardiovascular health. Crit Rev Food Sci Nutr 42:301–16

    Article  CAS  Google Scholar 

  • Ren JY, Yin BW, Li X, Zhu SQ, Deng JL, Sun YT, Zhang ZA, Guo ZH, Pei HT, Zhang F, Li RQ, Chen FG, Ma YX (2021) Sesamin attenuates PM2.5-induced cardiovascular injury by inhibiting ferroptosis in rats. Food Funct 12:12671–82

    Article  CAS  Google Scholar 

  • Ren J, Liang J, Wang J, Yin B, Zhang F, Li X, Zhu S, Tian H, Cui Q, Song J, Liu G, Ling W, Ma Y (2022) Vascular benefits of vitamin C supplementation against fine particulate air pollution in healthy adults: a double-blind randomised crossover trial. Ecotoxicol Environ Saf 241:113735

    Article  CAS  Google Scholar 

  • Sancini G, Farina F, Battaglia C, Cifola I, Mangano E, Mantecca P, Camatini M, Palestini P (2014) Health risk assessment for air pollutants: alterations in lung and cardiac gene expression in mice exposed to Milano winter fine particulate matter (PM2.5). PLoS One 9:e109685

    Article  Google Scholar 

  • Senoner T, Dichtl W (2019) Oxidative stress in cardiovascular diseases: still a therapeutic target? Nutrients 11.

  • Singh T, Sharma SD, Katiyar SK (2011) Grape proanthocyanidins induce apoptosis by loss of mitochondrial membrane potential of human non-small cell lung cancer cells in vitro and in vivo. PLoS One 6:e27444

    Article  CAS  Google Scholar 

  • Su X, Tian J, Li B, Zhou L, Kang H, Pei Z, Zhang M, Li C, Wu M, Wang Q, Han B, Chu C, Pang Y, Ning J, Zhang B, Niu Y, Zhang R (2020) Ambient PM2.5 caused cardiac dysfunction through FoxO1-targeted cardiac hypertrophy and macrophage-activated fibrosis in mice. Chemosphere 247:125881

    Article  CAS  Google Scholar 

  • Sun Y, **u C, Liu W, Tao Y, Wang J, Qu YI (2016) Grape seed proanthocyanidin extract protects the retina against early diabetic injury by activating the Nrf2 pathway. Exp Ther Med 11:1253–58

    Article  CAS  Google Scholar 

  • Takemura G, Kanamori H, Okada H, Miyazaki N, Watanabe T, Tsujimoto A, Goto K, Maruyama R, Fujiwara T, Fujiwara H (2018) Anti-apoptosis in nonmyocytes and pro-autophagy in cardiomyocytes: two strategies against postinfarction heart failure through regulation of cell death/degeneration. Heart Fail Rev 23:759–72

    Article  Google Scholar 

  • van der Pol A, van Gilst WH, Voors AA, van der Meer P (2019) Treating oxidative stress in heart failure: past, present and future. Eur J Heart Fail 21:425–35

    Article  Google Scholar 

  • Wei FX, Hu XF, Sa RN, Liu FZ, Li SY, Sun QY (2014) Antioxidant capacity and meat quality of broilers exposed to different ambient humidity and ammonia concentrations. Genet Mol Res 13:3117–27

    Article  CAS  Google Scholar 

  • Weichenthal SA, Godri-Pollitt K, Villeneuve PJ (2013) PM2.5, oxidant defence and cardiorespiratory health: a review. Environ Health 12:40

    Article  Google Scholar 

  • Wolfram R, Oguogho A, Palumbo B, Sinzinger H (2005) Enhanced oxidative stress in coronary heart disease and chronic heart failure as indicated by an increased 8-epi-PGF(2alpha). Eur J Heart Fail 7:167–72

    Article  CAS  Google Scholar 

  • Wu Y, Wang Y, Nabi X (2019) Protective effect of Ziziphora clinopodioides flavonoids against H2O2-induced oxidative stress in HUVEC cells. Biomed Pharmacother 117:109156

    Article  CAS  Google Scholar 

  • **ao Y, Ding L, Gu YH (2017) Progress of acupuncture and moxibustion research on the signal transduction pathways involved in cell apoptosis in myocardial ischemia reperfusion injury. Zhen Ci Yan Jiu 42:463–6

    CAS  Google Scholar 

  • Yang L, **an D, **ong X, Lai R, Song J, Zhong J (2018) Proanthocyanidins against oxidative stress: from molecular mechanisms to clinical applications. Biomed Res Int 2018:8584136

    Google Scholar 

  • Zeng X, Liu J, Du X, Zhang J, Pan K, Shan W, **e Y, Song W, Zhao J (2018) The protective effects of selenium supplementation on ambient PM2.5-induced cardiovascular injury in rats. Environ Sci Pollut Res Int 25:22153–62

    Article  CAS  Google Scholar 

  • Zhang LM, Lv SS, Fu SR, Wang JQ, Liang LY, Li RQ, Zhang F, Ma YX (2021) Procyanidins inhibit fine particulate matter-induced vascular smooth muscle cells apoptosis via the activation of the Nrf2 signaling pathway. Ecotoxicol Environ Saf 223:112586

    Article  CAS  Google Scholar 

  • Zhao L, Qi Y, Xu L, Tao X, Han X, Yin L, Peng J (2018) MicroRNA-140–5p aggravates doxorubicin-induced cardiotoxicity by promoting myocardial oxidative stress via targeting Nrf2 and Sirt2. Redox Biol 15:284–96

    Article  CAS  Google Scholar 

  • Zhu F (2018) Proanthocyanidins in cereals and pseudocereals. Crit Rev Food Sci Nutr 59:1521–33

    Article  Google Scholar 

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Funding

This paper was funded by the National Natural Science Foundation of China (no. 81874264).

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Authors and Affiliations

Authors

Contributions

Bowen Yin: conceptualisation, methodology, software, writing—original draft, formal analysis, writing—review and editing, project administration, resources. **ao Zhang: conceptualisation, methodology, formal analysis, investigation, data curation, writing—original draft. **gyi Ren: formal analysis, investigation, data curation. Fengge Chen: conceptualisation, methodology, resources. Hanning Zhang: methodology, software, investigation. Jufeng Liang: methodology, validation, investigation. Huanting Pei: software, investigation. Zhaohui Hu: investigation. Yan Wang: investigation. Wei Xue: investigation. **nyue Yu: investigation. Rui Zhang: investigation. Yuxia Ma: conceptualisation, methodology, investigation, writing—review and editing, funding acquisition.

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Correspondence to Yuxia Ma.

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Yin, B., Zhang, X., Ren, J. et al. The protective effects of procyanidin supplementation on PM2.5-induced acute cardiac injury in rats. Environ Sci Pollut Res 30, 10890–10900 (2023). https://doi.org/10.1007/s11356-022-22938-5

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