Hydroxysafflor yellow A protects against angiotensin II‑induced hypertrophy

Ni,Bin; Zhou,Donglai; Jing,Yunyan; Liu,Shanxin

doi:10.3892/mmr.2018.9399

Hydroxysafflor yellow A protects against angiotensin II‑induced hypertrophy

Authors:
- Bin Ni
- Donglai Zhou
- Yunyan Jing
- Shanxin Liu
View Affiliations

Affiliations: Department of Cardiology, The Affiliated Hospital of Hangzhou Normal University, Hangzhou, Zhejiang 310015, P.R. China
Published online on: August 17, 2018 https://doi.org/10.3892/mmr.2018.9399
Pages: 3649-3656
Copyright: © Ni et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Myocardial infarction (MI) is life‑threatening and is generally accompanied by myocardial hypertrophy. Notably, Hydroxysafflor yellow A (HSYA) can prevent tissue injuries. The objective of this study was to investigate the effect of HSYA on hypertrophy after MI. Hematoxylin and eosin (H&E) staining assays were performed to measure cell area. The protein synthesis rate was assessed using the 3H Leucine incorporation assay. Reverse transcription‑quantitative polymerase chain reaction (RT‑qPCR), western blot analysis and the immunohistochemical assay were used to detect the expression of target genes. The activity of superoxide dismutase (SOD), malondialdehyde (MDA) and the reactive oxygen species (ROS) generation were examined using commercial kits. Decreased myocardial hypertrophy was observed in animals treated with HSYA. Furthermore, the expression of nuclear factor (erythroid‑derived 2)‑like 2 (Nrf2) was higher in HSYA administration groups compared with that in the MI model group. In H9c2 cardiomyocytes, the pretreatment with HSYA increased the cell viability, however, it reduced protein synthesis rate, mitigated cell surface area and decreased the expression of Brain natriuretic factor (BNP) and β‑myosin heavy chain (β‑MHC). By contrast, the downregulation of Nrf2 deteriorated and reversed the effect of Ang II and HSYA. Furthermore, oxidative stress was alleviated by HSYA via inhibiting ROS generation, modulating the activities of SOD and MDA. In addition, the expression of NAD(P)H:quinone oxidoreductase 1 (NQO1) and heme oxygenase‑1 (HO‑1) were recovered by the pretreatment of HSYA that was combated by siNrf2. In conclusion, HSYA exerted anti‑hypertrophic effects, which was pertinent with the activation of Nrf2/NQO‑1/HO‑1 signaling pathway. The findings of this study may inspire a novel strategy to combat MI.

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1	Eriksson H: Heart failure: A growing public health problem. J Intern Med. 237:135–141. 1995. View Article : Google Scholar : PubMed/NCBI
2	Dickstein K, Cohensolal A, Filippatos G, McMurray JJ, Ponikowski P, Poole-Wilson PA, Strömberg A, Van Veldhuisen DJ, Atar D, Hoes AW, et al: ESC Guidelines for the diagnosis and treatment of acute and chronic heart failure 2008: The Task Force for the diagnosis and treatment of acute and chronic heart failure 2008 of the European Society of Cardiology. Developed in collaboration with the Heart Failure Association of the ESC (HFA) and endorsed by the European Society of Intensive Care Medicine (ESICM). Eur Heart J. 29:2388–2442. 2008. View Article : Google Scholar : PubMed/NCBI
3	Frey N and Olson EN: Cardiac hypertrophy: The good, the bad and the ugly. Annu Rev Physiol. 65:452003. View Article : Google Scholar : PubMed/NCBI
4	English BA, Appalsamy M, Diedrich A, Ruggiero AM, Lund D, Wright J, Keller NR, Louderback KM, Robertson D and Blakely RD: Tachycardia, reduced vagal capacity and age-dependent ventricular dysfunction arising from diminished expression of the presynaptic choline transporter. Am J Physiol Heart Circ Physiol. 299:H799–H810. 2010. View Article : Google Scholar : PubMed/NCBI
5	Singh MV and Anderson ME: Is CaMKII a link between inflammation and hypertrophy in heart? J Mol Med. 89:537–543. 2011. View Article : Google Scholar : PubMed/NCBI
6	Molkentin JD and Dorn GW II: Cytoplasmic signaling pathways that regulate cardiac hypertrophy. Annu Rev Physiol. 63:391–426. 2001. View Article : Google Scholar : PubMed/NCBI
7	Nicol RL, Frey N and Olson EN: From the sarcomere to the nucleus: Role of genetics and signaling in structural heart disease. Annu Rev Genomics Hum Genet. 1:179–223. 2000. View Article : Google Scholar : PubMed/NCBI
8	Yang K, Xu X, Nie L, Xiao T, Guan X, He T, Yu Y, Liu L, Huang Y, Zhang J and Zhao J: Indoxyl sulfate induces oxidative stress and hypertrophy in cardiomyocytes by inhibiting the AMPK/UCP2 signaling pathway. Toxicol Lett. 234:110–119. 2015. View Article : Google Scholar : PubMed/NCBI
9	Pimentel DR, Amin JK, Xiao L, Miller T, Viereck J, Oliver-Krasinski J, Baliga R, Wang J, Siwik DA, Singh K, et al: Reactive oxygen species mediate amplitude-dependent hypertrophic and apoptotic responses to mechanical stretch in cardiac myocytes. Circ Res. 89:453–460. 2001. View Article : Google Scholar : PubMed/NCBI
10	Nakamura K, Fushimi K, Kouchi H, Mihara K, Miyazaki M, Ohe T and Namba M: Inhibitory effects of antioxidants on neonatal rat cardiac myocyte hypertrophy induced by tumor necrosis factor-alpha and angiotensin II. Circulation. 98:794–799. 1998. View Article : Google Scholar : PubMed/NCBI
11	Bendall JK, Cave AC, Heymes C, Gall N and Shah AM: Pivotal role of a gp91(phox)-containing NADPH oxidase in angiotensin II-induced cardiac hypertrophy in mice. Circulation. 105:293–296. 2002. View Article : Google Scholar : PubMed/NCBI
12	Hingtgen SD, Tian X, Yang J, Dunlay SM, Peek AS, Wu Y, Sharma RV, Engelhardt JF and Davisson RL: Nox2-containing NADPH oxidase and Akt activation play a key role in angiotensin II-induced cardiomyocyte hypertrophy. Physiol Genomics. 26:180–191. 2006. View Article : Google Scholar : PubMed/NCBI
13	Nguyen T, Nioi P and Pickett CB: The Nrf2-antioxidant response element signaling pathway and its activation by oxidative stress. J Biol Chem. 284:13291–13295. 2009. View Article : Google Scholar : PubMed/NCBI
14	Soares MP and Ribeiro AM: Nrf2 as a master regulator of tissue damage control and disease tolerance to infection. Biochem Soc Trans. 43:663–668. 2015. View Article : Google Scholar : PubMed/NCBI
15	Psaty BM, Smith NL, Siscovick DS, Koepsell TD, Weiss NS, Heckbert SR, Lemaitre RN, Wagner EH and Furberg CD: Health outcomes associated with antihypertensive therapies used as first-line agents. A systematic review and meta-analysis. JAMA. 277:739–745. 1997. View Article : Google Scholar : PubMed/NCBI
16	Wang L, Zhou GB, Liu P, Song JH, Liang Y, Yan XJ, Xu F, Wang BS, Mao JH, Shen ZX, et al: Dissection of mechanisms of Chinese medicinal formula Realgar-Indigo naturalis as an effective treatment for promyelocytic leukemia. Proc Natl Acad Sci USA. 105:pp. 4826–4831. 2008; View Article : Google Scholar : PubMed/NCBI
17	Yang J, Wang Y and Guo ML: Identification and mapping of a novel hydroxysafflor yellow A (HSYA) biosynthetic gene in Carthamus tinctorius. Biochem Genet. 49:410–415. 2011. View Article : Google Scholar : PubMed/NCBI
18	Min J and Wei C: Hydroxysafflor yellow A cardioprotection in ischemia-reperfusion (I/R) injury mainly via Akt/hexokinase II independent of ERK/GSK-3β pathway. Biomed Pharmacother. 87:419–426. 2017. View Article : Google Scholar : PubMed/NCBI
19	Nurzynska D, Meglio FD, Castaldo C, Miraglia R, Romano V, Sacco AM, Barbato V, Granato G, Belviso I, Bancone C, et al: Cardiac primitive cells in the adult human heart are influenced by Angiotensin II in chronic heart failure. Ital J Anat Embryol. 119:2014.
20	Liu SX, Zhang Y, Wang YF, Li XC, Xiang MX, Bian C and Chen P: Upregulation of heme oxygenase-1 expression by hydroxysafflor yellow A conferring protection from anoxia/reoxygenation-induced apoptosis in H9c2 cardiomyocytes. Int J Cardiol. 160:95–101. 2012. View Article : Google Scholar : PubMed/NCBI
21	Sahni A, Wang N and Alexis JD: UAP56 is an important regulator of protein synthesis and growth in cardiomyocytes. Biochem Biophys Res Commun. 393:106–110. 2010. View Article : Google Scholar : PubMed/NCBI
22	Liu Y, Jiao R, Ma ZG, Liu WEI, Wu QQ, Yang Z, Li FF, Yuan Y, Bian ZY and Tang QZ: Sanguinarine inhibits angiotensin II-induced apoptosis in H9c2 cardiac cells via restoring reactive oxygen species-mediated decreases in the mitochondrial membrane potential. Mol Med Rep. 12:3400–3408. 2015. View Article : Google Scholar : PubMed/NCBI
23	Prathapan A, Vineetha VP and Raghu KG: Protective effect of Boerhaavia diffusa L. against mitochondrial dysfunction in angiotensin II induced hypertrophy in H9c2 cardiomyoblast cells. PLoS One. 9:e962202014. View Article : Google Scholar : PubMed/NCBI
24	Kumar RR, Madhusudhanan N, Shanmugam G, Hong J, Devarajan A, Palaniappan S, Zhang J, Halade GV, Darley-Usmar VM, Hoidal JR, et al: Abrogation of Nrf2 impairs antioxidant signaling and promotes atrial hypertrophy in response to high-intensity exercise stress. J Transl Med. 14:862016. View Article : Google Scholar : PubMed/NCBI
25	Meloni M, Caporali A, Graiani G, Lagrasta C, Katare R, Van Linthout S, Spillmann F, Campesi I, Madeddu P, Quaini F and Emanueli C: Nerve growth factor promotes cardiac repair following myocardial infarction. Circ Res. 106:1275–1284. 2010. View Article : Google Scholar : PubMed/NCBI
26	Olivetti G, Quaini F, Sala R, Lagrasta C, Corradi D, Bonacina E, Gambert SR, Cigola E and Anversa P: Acute myocardial infarction in humans is associated with activation of programmed myocyte cell death in the surviving portion of the heart. J Mol Cell Cardiol. 28:2005–2016. 1996. View Article : Google Scholar : PubMed/NCBI
27	McMullen JR and Jennings GL: Differences between pathological and physiological cardiac hypertrophy: Novel therapeutic strategies to treat heart failure. Clin Exp Pharmacol Physiol. 34:255–262. 2007. View Article : Google Scholar : PubMed/NCBI
28	Neeland IJ, Drazner MH, Berry JD, Ayers CR, de Filippi C, Seliger SL, Nambi V, McGuire DK, Omland T and de Lemos JA: Biomarkers of chronic cardiac injury and hemodynamic stress identify a malignant phenotype of left ventricular hypertrophy in the general population. J Am Coll Cardiol. 61:187–195. 2013. View Article : Google Scholar : PubMed/NCBI
29	Hayashi D, Kudoh S, Shiojima I, Zou Y, Harada K, Shimoyama M, Imai Y, Monzen K, Yamazaki T, Yazaki Y, et al: Atrial natriuretic peptide inhibits cardiomyocyte hypertrophy through mitogen-activated protein kinase phosphatase-1. Biochem Biophys Res Commun. 322:310–319. 2004. View Article : Google Scholar : PubMed/NCBI
30	Li J, Ichikawa T, Villacorta L, Janicki JS, Brower GL, Yamamoto M and Cui T: Nrf2 protects against maladaptive cardiac responses to hemodynamic stress. Arterioscler Thromb Vasc Biol. 29:1843–1850. 2009. View Article : Google Scholar : PubMed/NCBI
31	Sugden PH and Clerk A: Cellular mechanisms of cardiac hypertrophy. J Mol Med. 76:725–746. 1998. View Article : Google Scholar : PubMed/NCBI
32	Tanaka K, Honda M and Takabatake T: Redox regulation of MAPK pathways and cardiac hypertrophy in adult rat cardiac myocyte. J Am Coll Cardiol. 37:676–685. 2001. View Article : Google Scholar : PubMed/NCBI
33	Todorova I, Simeonova G, Kyuchukova D, Dinev D and Gadjeva V: Reference values of oxidative stress parameters (MDA, SOD, CAT) in dogs and cats. Comp Clin Path. 13:190–194. 2005. View Article : Google Scholar
34	Omidi A, Namazi F, Jabire S, Afsar M, Honarmand M and Nazifi S: The effects of starvation and refeeding on oxidative stress parameters (MDA, SOD, GPx), lipid profile, thyroid hormones and thyroid histopathology in male wistar rats. Int Arch Med. 9(238)2016.
35	Wu CC, Hsu MC, Hsieh CW, Lin JB, Lai PH and Wung BS: Upregulation of heme oxygenase-1 by Epigallocatechin-3-gallate via the phosphatidylinositol 3-kinase/Akt and ERK pathways. Life Sci. 78:2889–2897. 2006. View Article : Google Scholar : PubMed/NCBI
36	Li P, Su L, Li X, Di W, Zhang X, Zhang C, He T, Zhu X, Zhang Y and Li Y: Remote limb ischemic postconditioning protects mouse brain against cerebral ischemia/reperfusion injury via upregulating expression of Nrf2, HO-1 and NQO-1 in mice. Int J Neurosci. September 17–2015.(Epub ahead of print). View Article : Google Scholar :
37	Tomita M, Okuyama T, Katsuyama H, Hidaka K, Otsuki T and Ishikawa T: Gene expression in rat lungs during early response to paraquat-induced oxidative stress. Int J Mol Med. 17:37–44. 2006.PubMed/NCBI
38	Wang T, Fu FH, Han B, Li GS, Zhang LM and Liu K: Hydroxysafflor yellow A reduces myocardial infarction size after coronary artery ligation in rats. Pharm Biol. 47:458–462. 2009. View Article : Google Scholar
39	Wei G, Yin Y, Duan J, Guo C, Zhu Y, Wang Y, Xi M and Wen A: Hydroxysafflor yellow A promotes neovascularization and cardiac function recovery through HO-1/VEGF-A/SDF-1α cascade. Biomed Pharmacother. 88:409–420. 2017. View Article : Google Scholar : PubMed/NCBI
40	Liu YN, Zhu JH, Xiang WU and Wang ZH: Mitochondrial mechanism of cardioprotective effect of hydroxysafflor yellow A against anoxia/reoxygenation injury in rats. J Jiangsu Univ (Medicine Edition). 23:2013.
41	Chen L, Xiang Y, Kong L, Zhang X, Sun B, Wei X and Liu H: Hydroxysafflor yellow A protects against cerebral ischemia-reperfusion injury by anti-apoptotic effect through PI3K/Akt/GSK3β pathway in rat. Neurochem Res. 38:2268–2275. 2013. View Article : Google Scholar : PubMed/NCBI
42	Zhou MX, Fu JH, Zhang Q and Wang JQ: Effect of hydroxy safflower yellow A on myocardial apoptosis after acute myocardial infarction in rats. Genet Mol Res. 14:3133–3141. 2015. View Article : Google Scholar : PubMed/NCBI