Abstract
The calpain-1-activated apoptotic pathway plays a key role in right ventricular hypertrophy (RVH). Taurine has been shown to attenuate apoptosis by inhibiting calpain activity. This experiment aimed to determine whether taurine could prevent RVH by inhibiting the calpain-1/cytochrome c apoptotic pathway. The broilers were given 1% taurine dissolved in drinking water and were raised at 10 °C ~ 12 °C from day 21 to day 42. At 21 d, 28 d, 35 d and 42 d, the right ventricular (RV) tissues were collected. Increased RVH index, angiotensin II, norepinephrine and atrial natriuretic peptide mRNA expression were reduced by taurine in the broiler RVs. Taurine obviously inhibited cardiomyocyte apoptosis via maintaining the mitochondrial membrane potential and decreased the activation of caspase-9 and caspase-3 in the broiler RVs. The antioxidant assay demonstrated that taurine enhanced the activities of superoxide dismutase, total antioxidant capacity and glutathione peroxidase and the glutathione/glutathione disulfide ratio. Western blot results revealed that taurine also downregulated the expression of calpain-1 and cytosolic cytochrome c while upregulating the expression of Bcl-2/Bax and mitochondrial cytochrome c in broiler cardiomyocytes during RVH. In summary, we found that taurine could enhance cardiomyocyte antioxidant ability and further prevented cardiomyocyte apoptosis by inhibiting the calpain-1/cytochrome c pathway during RVH in broilers.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Adedara IA, Alake SE, Adeyemo MO et al (2018) Taurine enhances spermatogenic function and antioxidant defense mechanisms in testes and epididymis of L-NAME-induced hypertensive rats. Biomed Pharmacother 97:181–189. https://doi.org/10.1016/j.biopha.2017.10.095
Al-Abbasi F, Alghamdi E, Baghdadi M et al (2016) Gingerol synergizes the cytotoxic effects of doxorubicin against liver cancer cells and protects from its vascular toxicity. Molecules 21:886. https://doi.org/10.3390/molecules21070886
Aly HAA, Khafagy RM (2014) Taurine reverses endosulfan-induced oxidative stress and apoptosis in adult rat testis. Food Chem Toxicol 64:1–9. https://doi.org/10.1016/j.fct.2013.11.007
Arbustini E, Brega A, Narula J (2008) Ultrastructural definition of apoptosis in heart failure. Heart Fail Rev 13:121–135. https://doi.org/10.1007/s10741-007-9072-8
Azuma M, Takahashi K, Fukuda T et al (2000) Taurine attenuates hypertrophy induced by angiotensin II in cultured neonatal rat cardiac myocytes. Eur J Pharmacol 403:181–188. https://doi.org/10.1016/S0014-2999(00)00483-0
Baghbanzadeh A, Decuypere E (2008) Ascites syndrome in broilers: physiological and nutritional perspectives. Avian Pathol 37:117–126. https://doi.org/10.1080/03079450801902062
Bajaj G, Sharma RK (2006) TNF-α-mediated cardiomyocyte apoptosis involves caspase-12 and calpain. Biochem Biophys Res Commun 345:1558–1564. https://doi.org/10.1016/j.bbrc.2006.05.059
Chowdhury S, Sinha K, Banerjee S, Sil PC (2016) Taurine protects cisplatin induced cardiotoxicity by modulating inflammatory and endoplasmic reticulum stress responses: taurine protects cisplatin induced cardiotoxicity. BioFactors 42:647–664. https://doi.org/10.1002/biof.1301
Crow MT, Mani K, Nam Y-J, Kitsis RN (2004) The mitochondrial death pathway and cardiac myocyte apoptosis. Circ Res 95:957–970. https://doi.org/10.1161/01.RES.0000148632.35500.d9
de Moissac D, Gurevich RM, Zheng H et al (2000) Caspase activation and mitochondrial cytochrome C release during hypoxia-mediated apoptosis of adult ventricular myocytes. J Mol Cell Cardiol 32:53–63. https://doi.org/10.1006/jmcc.1999.1057
Dong Z, Wan L, Wang R et al (2017) (–)-Epicatechin suppresses angiotensin II-induced cardiac hypertrophy via the activation of the SP1/SIRT1 signaling pathway. Cell Physiol Biochem 41:2004–2015. https://doi.org/10.1159/000475396
Eugene B (2008) Biomarkers in heart failure. N Engl J Med 358:2148–2159. https://doi.org/10.1056/NEJMra0800239
Gill C, Mestril R, Samali A (2002) Losing heart: the role of apoptosis in heart disease—a novel therapeutic target? FASEB J 16:135–146. https://doi.org/10.1096/fj.01-0629com
Gil-Parrado S, Fernández-Montalván A, Assfalg-Machleidt I et al (2002) Ionomycin-activated calpain triggers apoptosis: a probable role For Bcl-2 family members. J Biol Chem 277:27217–27226. https://doi.org/10.1074/jbc.M202945200
Harwood SM, Yaqoob MM, Allen DA (2005) Caspase and calpain function in cell death: bridging the gap between apoptosis and necrosis. Ann Clin Biochem 42:415–431. https://doi.org/10.1258/000456305774538238
Havenstein G, Ferket P, Qureshi M (2003) Growth, livability, and feed conversion of 1957 versus 2001 broilers when fed representative 1957 and 2001 broiler diets. Poult Sci 82:1500–1508. https://doi.org/10.1093/ps/82.10.1500
He F, Ma N, Midorikawa K et al (2018) Taurine exhibits an apoptosis-inducing effect on human nasopharyngeal carcinoma cells through PTEN/Akt pathways in vitro. Amino Acids 50:1749–1758. https://doi.org/10.1007/s00726-018-2651-2
Ito T, Schaffer S, Azuma J (2014) The effect of taurine on chronic heart failure: actions of taurine against catecholamine and angiotensin II. Amino Acids 46:111–119. https://doi.org/10.1007/s00726-013-1507-z
Jong CJ, Azuma J, Schaffer S (2012) Mechanism underlying the antioxidant activity of taurine: prevention of mitochondrial oxidant production. Amino Acids 42:2223–2232. https://doi.org/10.1007/s00726-011-0962-7
Jong C, Ito T, Prentice H et al (2017) Role of mitochondria and endoplasmic reticulum in taurine-deficiency-mediated apoptosis. Nutrients 9:795. https://doi.org/10.3390/nu9080795
Julian RJ (2000) Physiological, management and environmental triggers of the ascites syndrome: a review. Avian Pathol 29:519–527. https://doi.org/10.1080/03079450020016751
Julian RJ (2007) The response of the heart and pulmonary arteries to hypoxia, pressure, and volume. Short Rev Poult Sci 86:1006–1011. https://doi.org/10.1093/ps/86.5.1006
Kalmar ID, Vanrompay D, Janssens GPJ (2013) Broiler ascites syndrome: collateral damage from efficient feed to meat conversion. Vet J 197:169–174. https://doi.org/10.1016/j.tvjl.2013.03.011
Kontny E, Grabowska A, Kowalczewski J et al (1999) Taurine chloramine inhibition of cell proliferation and cytokine production by rheumatoid arthritis fibroblast-like synoviocytes. Arthritis Rheum 42:2552–2560. https://doi.org/10.1002/1529-0131(199912)42:12%3c2552:AID-ANR7%3e3.0.CO;2-V
Kulikov AV, Shilov ES, Mufazalov IA et al (2012) Cytochrome c: the Achilles’ heel in apoptosis. Cell Mol Life Sci 69:1787–1797. https://doi.org/10.1007/s00018-011-0895-z
Li Y, Arnold J, Pampillo M et al (2009a) Taurine prevents cardiomyocyte death by inhibiting NADPH oxidase-mediated calpain activation. Free Radic Biol Med 46:51–61. https://doi.org/10.1016/j.freeradbiomed.2008.09.025
Li Y, Li Y, Feng Q et al (2009b) Calpain activation contributes to hyperglycaemia-induced apoptosis in cardiomyocytes. Cardiovasc Res 84:100–110. https://doi.org/10.1093/cvr/cvp189
Li S, Yang L, Zhang Y et al (2017a) Taurine ameliorates arsenic-induced apoptosis in the hippocampus of mice through intrinsic pathway. In: Lee D-H, Schaffer SW, Park E, Kim HW (eds) Taurine 10. Springer, Netherlands, pp 183–192
Li X, Lan Y, Wang Y et al (2017b) Telmisartan suppresses cardiac hypertrophy by inhibiting cardiomyocyte apoptosis via the NFAT/ANP/BNP signaling pathway. Mol Med Rep 15:2574–2582. https://doi.org/10.3892/mmr.2017.6318
Lyon RC, Zanella F, Omens JH, Sheikh F (2015) Mechanotransduction in cardiac hypertrophy and failure. Circ Res 116:1462–1476. https://doi.org/10.1161/CIRCRESAHA.116.304937
Maulik SK, Kumar S (2012) Oxidative stress and cardiac hypertrophy: a review. Toxicol Mech Methods 22:359–366. https://doi.org/10.3109/15376516.2012.666650
Mei M, Tang F, Lu M et al (2015) Astragaloside IV attenuates apoptosis of hypertrophic cardiomyocyte through inhibiting oxidative stress and calpain-1 activation. Environ Toxicol Pharmacol 40:764–773. https://doi.org/10.1016/j.etap.2015.09.007
Oriyanhan W, Yamazaki K, Miwa S et al (2005) Taurine prevents myocardial ischemia/reperfusion-induced oxidative stress and apoptosis in prolonged hypothermic rat heart preservation. Heart Vessels 20:278–285. https://doi.org/10.1007/s00380-005-0841-9
Pan J, Tan X, Li J et al (2008) Reduced PKCα expression in pulmonary arterioles of broiler chickens is associated with early feed restriction. Res Vet Sci 84:434–439. https://doi.org/10.1016/j.rvsc.2007.06.009
Patel SN, Pandya K, Clark GJ et al (2016) Comparison of taurine and pantoyltaurine as antioxidants in vitro and in the central nervous system of diabetic rats. Exp Toxicol Pathol 68:103–112. https://doi.org/10.1016/j.etp.2015.11.002
Polster BM, Basañez G, Etxebarria A et al (2005) Calpain I induces cleavage and release of apoptosis-inducing factor from isolated mitochondria. J Biol Chem 280:6447–6454. https://doi.org/10.1074/jbc.M413269200
Racasan S, Braam B, van der Giezen DM et al (2004) Perinatal L-arginine and antioxidant supplements reduce adult blood pressure in spontaneously hypertensive rats. Hypertension 44:83–88. https://doi.org/10.1161/01.HYP.0000133251.40322.20
Rashid K, Das J, Sil PC (2013) Taurine ameliorate alloxan induced oxidative stress and intrinsic apoptotic pathway in the hepatic tissue of diabetic rats. Food Chem Toxicol 51:317–329. https://doi.org/10.1016/j.fct.2012.10.007
Rezaee MA, Mohammadpour AH, Imenshahidi M et al (2016) Protective effect of erythropoietin on myocardial apoptosis in rats exposed to carbon monoxide. Life Sci 148:118–124. https://doi.org/10.1016/j.lfs.2016.02.007
Saleem N, Prasad A, Goswami SK (2018) Apocynin prevents isoproterenol-induced cardiac hypertrophy in rat. Mol Cell Biochem 445:79–88. https://doi.org/10.1007/s11010-017-3253-0
Samak M, Fatullayev J, Sabashnikov A et al (2016) Cardiac hypertrophy: an introduction to molecular and cellular basis. Med Sci Monit Basic Res 22:75–79. https://doi.org/10.12659/MSMBR.900437
Satoh H, Sperelakis N (1998) Review of some actions of taurine on ion channels of cardiac muscle cells and others. Gen Pharmacol Vasc Syst 30:451–463. https://doi.org/10.1016/S0306-3623(97)00309-1
Schieber M, Chandel NS (2014) ROS function in redox signaling and oxidative stress. Curr Biol 24:R453–R462. https://doi.org/10.1016/j.cub.2014.03.034
Sinha K, Das J, Pal PB, Sil PC (2013) Oxidative stress: the mitochondria-dependent and mitochondria-independent pathways of apoptosis. Arch Toxicol 87:1157–1180. https://doi.org/10.1007/s00204-013-1034-4
Smiljic S (2017) The clinical significance of endocardial endothelial dysfunction. Medicina (Mex) 53:295–302. https://doi.org/10.1016/j.medici.2017.08.003
Smith MA, Schnellmann RG (2012) Calpains, mitochondria, and apoptosis. Cardiovasc Res 96:32–37. https://doi.org/10.1093/cvr/cvs163
Sun M, Gu Y, Zhao Y, Xu C (2011) Protective functions of taurine against experimental stroke through depressing mitochondria-mediated cell death in rats. Amino Acids 40:1419–1429. https://doi.org/10.1007/s00726-010-0751-8
Takano S, Shiomoto S, Inoue KY et al (2014) Electrochemical approach for the development of a simple method for detecting cell apoptosis based on caspase-3 activity. Anal Chem 86:4723–4728. https://doi.org/10.1021/ac403394z
Takemura G, Kanoh M, Minatoguchi S, Fujiwara H (2013) Cardiomyocyte apoptosis in the failing heart—a critical review from definition and classification of cell death. Int J Cardiol 167:2373–2386. https://doi.org/10.1016/j.ijcard.2013.01.163
Takemura G, Kanamori H, Okada H et al (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 23:759–772. https://doi.org/10.1007/s10741-018-9708-x
Taylor RC, Cullen SP, Martin SJ (2008) Apoptosis: controlled demolition at the cellular level. Nat Rev Mol Cell Biol 9:231–241. https://doi.org/10.1038/nrm2312
Tham YK, Bernardo BC, Ooi JYY et al (2015) Pathophysiology of cardiac hypertrophy and heart failure: signaling pathways and novel therapeutic targets. Arch Toxicol 89:1401–1438. https://doi.org/10.1007/s00204-015-1477-x
Valko M, Leibfritz D, Moncol J et al (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39:44–84. https://doi.org/10.1016/j.biocel.2006.07.001
Wang J, Qi C, Liu L et al (2018) Taurine protects primary neonatal cardiomyocytes against apoptosis induced by hydrogen peroxide. Int Heart J 59:190–196. https://doi.org/10.1536/ihj.16-372
Wideman R (1999) Cardiac output in four-, five-, and six-week-old broilers, and hemodynamic responses to intravenous injections of epinephrine. Poult Sci 78:392–403. https://doi.org/10.1093/ps/78.3.392
Wideman RF, Erf GF, Chapman ME (2001) Intravenous endotoxin triggers pulmonary vasoconstriction and pulmonary hypertension in broiler chickens. Poult Sci 80:647–655. https://doi.org/10.1093/ps/80.5.647
Wideman RF, Rhoads DD, Erf GF, Anthony NB (2013) Pulmonary arterial hypertension (ascites syndrome) in broilers: a review. Poult Sci 92:64–83. https://doi.org/10.3382/ps.2012-02745
Wolf BB, Goldstein JC, Stennicke HR et al (1999) Calpain functions in a caspase-independent manner to promote apoptosis-like events during platelet activation. J Am Soc Hematol 94:1683–1692
Wu G, Yang J, Lv H et al (2018) Taurine prevents ethanol-induced apoptosis mediated by mitochondrial or death receptor pathways in liver cells. Amino Acids 50:863–875. https://doi.org/10.1007/s00726-018-2561-3
Xiao T, Zhang Y, Wang Y et al (2013) Activation of an apoptotic signal transduction pathway involved in the upregulation of calpain and apoptosis-inducing factor in aldosterone-induced primary cultured cardiomyocytes. Food Chem Toxicol 53:364–370. https://doi.org/10.1016/j.fct.2012.12.022
Xiong B (2012) Transforming growth factor-β1 induces glutathione peroxidase-1 and protects from H2O2-induced cell death in colon cancer cells via the Smad2/ERK1/2/HIF-1α pathway. Int J Mol Med. https://doi.org/10.3892/ijmm.2012.901
Xu J-X, Si M, Zhang H-R et al (2014) Phosphoinositide kinases play key roles in norepinephrine- and angiotensin II-induced increase in phosphatidylinositol 4,5-bisphosphate and modulation of cardiac function. J Biol Chem 289:6941–6948. https://doi.org/10.1074/jbc.M113.527952
Yan M, Chen K, He L et al (2018) Uric acid induces cardiomyocyte apoptosis via activation of calpain-1 and endoplasmic reticulum stress. Cell Physiol Biochem 45:2122–2135. https://doi.org/10.1159/000488048
Yang Q, Yang J, Wu G et al (2013) Effects of taurine on myocardial cGMP/cAMP ratio, antioxidant ability, and ultrastructure in cardiac hypertrophy rats induced by isoproterenol. In: Idrissi A, L’Amoreaux WJ (eds) Taurine 8. Springer, New York, pp 217–229
Yang J, Zong X, Wu G et al (2015a) Taurine increases testicular function in aged rats by inhibiting oxidative stress and apoptosis. Amino Acids 47:1549–1558. https://doi.org/10.1007/s00726-015-1995-0
Yang Y, Li Z, Liu H et al (2015b) Inhibitory effect of tetramethylpyrazine preconditioning on overload training-induced myocardial apoptosis in rats. Chin J Integr Med 21:423–430. https://doi.org/10.1007/s11655-014-1752-3
Yang L, Ma J, Tan Y et al (2019) Cardiac‐specific overexpression of metallothionein attenuates L‐NAME‐induced myocardial contractile anomalies and apoptosis. J Cell Mol Med. https://doi.org/10.1111/jcmm.14375
Zhang Z, Zhao L, Zhou Y et al (2017) Taurine ameliorated homocysteine-induced H9C2 cardiomyocyte apoptosis by modulating endoplasmic reticulum stress. Apoptosis 22:647–661. https://doi.org/10.1007/s10495-017-1351-9
Zorov DB, Juhaszova M, Sollott SJ (2014) Mitochondrial reactive oxygen species (ROS) and ROS-induced ROS release. Physiol Rev 94:909–950. https://doi.org/10.1152/physrev.00026.2013
Acknowledgements
This work was supported by the National Natural Science Foundation of China (Nos. 31502026)
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare that there is no conflict of interest.
Research involving human participants and/or animals
All procedures performed in research involving human participants are in accordance with the ethical standards of the institution and/or national research committee. All procedures using animals were conducted according to the requirements of the Animal Welfare Act and the Guide for the Care and Use of Laboratory Animals. The procedures were approved by the Animal Care and Use Committee of Shenyang Agricultural University (No. 201606004).
Informed consent
Informed consent was obtained from all individual participants included in the study.
Additional information
Handling Editor: S. W. Schaffer.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Li, W., Yang, J., LYU, Q. et al. Taurine prevents cardiomyocyte apoptosis by inhibiting the calpain-1/cytochrome c pathway during RVH in broilers. Amino Acids 52, 453–463 (2020). https://doi.org/10.1007/s00726-020-02824-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00726-020-02824-5