Flavonoids in prevention of diseases with respect to modulation of Ca-pump function

Horáková, Ľubica

doi:10.2478/v10102-011-0019-5

Abstract

Flavonoids, natural phenolic compounds, are known as agents with strong antioxidant properties. In many diseases associated with oxidative/nitrosative stress and aging they provide multiple biological health benefits. Ca²⁺-ATPases belong to the main calcium regulating proteins involved in the balance of calcium homeostasis, which is impaired in oxidative/nitrosative stress and related diseases or aging. The mechanisms of Ca²⁺-ATPases dysfunction are discussed, focusing on cystein oxidation and tyrosine nitration. Flavonoids act not only as antioxidants but are also able to bind directly to Ca²⁺-ATPases, thus changing their conformation, which results in modulation of enzyme activity.

Dysfunction of Ca²⁺-ATPases is summarized with respect to their posttranslational and conformational changes in diseases related to oxidative/nitrosative stress and aging. Ca²⁺-ATPases are discussed as a therapeutic tool and the possible role of flavonoids in this process is suggested.

References

Adachi T, Matsui R, Weisbrod RM, Najibi S, Cohen RA. (2001). Reduced sarco/endoplasmic reticulum Ca(2+) uptake activity can account for the reduced response to NO, but not sodium nitroprusside, in hypercholesterolemic rabbit aorta. Circulation 104: 1040-5.
Search in Google Scholar
Adachi T, Matsui R, Xu S, Kirber M, Lazar HL, Sharov VS, Schöneich C, Cohen RA. (2002). Antioxidant improves smooth muscle sarco/endoplasmic reticulum Ca(2+)-ATPase function and lowers tyrosine nitration in hypercholesterolemia and improves nitric oxide-induced relaxation. Circ Res 90: 1114-1121.
Search in Google Scholar
Adachi T, Weisbrod RM, Pimentel DR, Ying J, Sharov VS, Schöneich C, Cohen RA. (2004). S-Glutathiolation by peroxynitrite activates SERCA during arterial relaxation by nitric oxide. Nat Med 10: 1200-1207.
Search in Google Scholar
Adachi T. (2010). Modulation of vascular sarco/endoplasmic reticulum calcium ATPase in cardiovascular pathophysiology. Adv Pharmacol 59: 165-95. Review.
Search in Google Scholar
Amić D, Davidović-Amić D, Beslo D, Rastija V, Lucić B, Trinajstić N. (2007). SAR and QSAR of the antioxidant activity of flavonoids. Curr Med Chem 14: 827-45. Review.
Search in Google Scholar
Bast A, Haenen GR, Bruynzeel AM, Van der Vijgh WJ. (2007). Protection by flavonoids against anthracycline cardiotoxicity: from chemistry to clinical trials. Cardiovasc Toxicol 7: 154-159. Review.
Search in Google Scholar
Bettuzzi S, Brausi M, Rizzi F, Castagnetti G, Peracchia G, Corti A. (2006). Chemoprevention of human prostate cancer by oral administration of green tea catechins in volunteers with high-grade prostate intraepithelial neoplasia: a preliminary report from a one-year proof-of-principle study. Cancer Res 66: 1234-40.
Search in Google Scholar
Bigelow DJ. (2009). Nitrotyrosine-modified SERCA2: a cellular sensor of reactive nitrogen species. Pflugers Arch 457: 701-710.
Search in Google Scholar
Bilmen JG, Khan SZ, Javed MH, Michelangeli F. (2001). Inhibition of the SERCA Ca2+ pumps by curcumin. Curcumin putatively stabilizes the interaction between the nucleotide-binding and phosphorylation domains in the absence of ATP. Eur J Biochem 268: 6318-6327.
Search in Google Scholar
Burda S, Oleszek W. (2001). Antioxidant and antiradical activities of flavonoids. J Agric Food Chem 49: 2774-2779.
Search in Google Scholar
Cao G, Sofic E, Prior RL. (1997). Antioxidant and prooxidant behavior of flavonoids: structure-activity relationships. Free Radic Biol Med 22: 749-60.
Search in Google Scholar
Clement Y. (2009). Can green tea do that? A literature review of the clinical evidence. Prev Med 49: 83-87. Review.
Search in Google Scholar
Chen B, Jones TE, Bigelow DJ. (1999). The nucleotide-binding site of the sarcoplasmic reticulum Ca-ATPase is conformationally altered in aged skeletal muscle. Biochemistry 38:14887-14896.
Search in Google Scholar
Choi EH, Chang HJ, Cho JY, Chun HS. (2007). Cytoprotective effect of anthocyanins against doxorubicin-induced toxicity in H9c2 cardiomyocytes in relation to their antioxidant activities. Food Chem Toxicol 45: 1873-1881.
Search in Google Scholar
Chyu KY, Babbidge SM, Zhao X, Dandillaya R, Rietveld AG, Yano J, Dimayuga P, Cercek B, Shah PK. (2004). Differential effects of green tea-derived catechin on developing versus established atherosclerosis in apolipoprotein E-null mice. Circulation 109: 2448-2453.
Search in Google Scholar
Cohen RA and Adachi T. (2006). Nitric-oxide-induced vasodilatation: Regulation by Physiologic S-glutathiolation and pathologic oxidation of the sarcoplasmic endoplasmic reticulum calcium ATPase. TCM 16: 109-114.
Search in Google Scholar
Croft KD. (2006). The chemistry and biological effects of flavonoids and phenolic acids. Ann NY Acad Sci 854: 435-442.
Search in Google Scholar
Dremina ES, Sharov VS, Davies MJ, Schöneich C. (2007). Oxidation and inactivation of SERCA by selective reaction of cysteine residues with amino acid peroxides. Chem Res Toxicol 20: 1462-1469.
Search in Google Scholar
Drieu K. (1986). Preparation and definition of the extract of Ginkgo biloba. Presse Médicale 15: 1455-1457.
Search in Google Scholar
Dyer JL, Khan SZ, Bilmen JG, Hawtin SR, Wheatley M, Javed MU, Michelangeli F. (2002). Curcumin: a new cell-permeant inhibitor of the inositol 1,4,5-trisphosphate receptor. Cell Calcium 31: 45-52.
Search in Google Scholar
East JM. (2000). Sarco(endo)plasmic reticulum calcium pumps: recent advances in our understanding of structure/function and biology. Mol Membr Biol 17: 189-200.
Search in Google Scholar
Erlund I, Silaste ML, Alfthan G, Rantala M, Kesäniemi YA, Aro A. (2002). Plasma concentrations of the flavonoids hesperetin, naringenin and quercetin in human subjects following their habitual diets, and diets high or low in fruit and vegetables. Eur J Clin Nutr 56: 891-898.
Search in Google Scholar
Hagerman AE, Dean RT, Davies MJ. (2003). Radical chemistry of epigallocatechin gallate and its relevance to protein damage. Arch Biochem Biophys 14: 115-120.
Search in Google Scholar
Hanasaki Y, Ogawa S, Fukui S. (1994). The correlation between active oxygens scavenging and antioxidative effects of flavonoids. Free Radic Biol Med 16: 845-50.
Search in Google Scholar
Heim KE, Tagliaferro AR, Bobilya DJ. (2002). Flavonoid antioxidants: chemistry, metabolism and structure-activity relationships. J Nutr Biochem 13: 572-584.
Search in Google Scholar
Hodgson JM, Croft KD. (2010). Tea flavonoids and cardiovascular health. Mol Aspects Med 31: 495-502. Review.
Search in Google Scholar
Inesi G, Hua S, Xu C, Ma H, Seth M, Prasad AM, Sumbilla C. (2005). Studies of Ca2+ ATPase (SERCA) inhibition. J Bioenerg Biomembr 37: 365-8. Review.
Search in Google Scholar
Ishige K, Schubert D, Sagara Y. (2001). Flavonoids protect neuronal cells from oxidative stress by three distinct mechanisms. Free Radical Biology & Medicine 30: 433-446.
Search in Google Scholar
Kamihira M, Nakazawa H, Kira A, Mizutani Y, Nakamura M, Nakayama T. (2008). Interaction of tea catechins with lipid bilayers investigated by a quartz-crystal microbalance analysis. Biosci Biotechnol Biochem 72: 1372-1375.
Search in Google Scholar
Knyushko TV, Sharov VS, Williams TD, Schöneich C. and Bigelow DJ. (2005). 3-Nitrotyrosine-modification of SERCA2a in the aging heart: a distinct signature of cellular redox environment. Biochemistry 44: 13071-13081.
Search in Google Scholar
Kuhar M, Sen S, Singh N. (2006). Role of mitochondria in quercetin-enhanced chemotherapeutic response in human non-small cell lung carcinoma H-520 cells. Anticancer Res 26: 1297-1303.
Search in Google Scholar
Lancel S, Qin F, Lennon SL, Zhang J, Tong X, Mazzini MJ, Kang YJ, Siwik DA, Cohen RA, Colucci WS. (2010). Oxidative posttranslational modifications mediate decreased SERCA activity and myocyte dysfunction in Galphaq-overexpressing mice. Circ Res 107: 228-232.
Search in Google Scholar
Leung HW, Kuo CL, Yang WH, Lin CH, Lee HZ. (2006). Antioxidant enzymes activity involvement in luteolin-induced human lung squamous carcinoma CH27 cell apoptosis. Eur J Pharmacol 534: 12-18.
Search in Google Scholar
MacLennan DH, Rice W J. and Green NM. (1997). The mechanism of Ca2+ transport by sarco(endo)plasmic reticulum Ca2+-ATPases. J Biol Chem 272: 28815-28828.
Search in Google Scholar
Mandel SA, Amit T, Weinreb O, Youdim MB. (2011). Understanding the broad-spectrum neuroprotective action profile of green tea polyphenols in aging and neurodegenerative diseases. J Alzheimers Dis 25(2): 187-208.
Search in Google Scholar
Martín MA, Serrano AB, Ramos S, Pulido MI, Bravo L, Goya L. (2010). Cocoa flavonoids up-regulate antioxidant enzyme activity via the ERK1/2 pathway to protect against oxidative stress-induced apoptosis in HepG2 cells. J Nutr Biochem 21: 196-205.
Search in Google Scholar
Mulvihill EE, Huff MW. (2010). Antiatherogenic properties of flavonoids: implications for cardiovascular health. Can J Cardiol 26(Suppl A): 17A-21A. Review.
Search in Google Scholar
Nagata H, Takekoshi S, Takagi T, Honma T, Watanabe K. (1999). Antioxidative action of flavonoids, quercetin and catechin, mediated by the activation of glutathione peroxidase. Tokai J Exp Clin Med 24: 1-11.
Search in Google Scholar
Ochiai H, Takeda K, Soeda S, Tahara Y, Takenaka H, Abe K, Hayashi Y, Noguchi S, Inoue M, Schwarz S, Schwarz W, Kawamura M. (2009). Epigallocatechin-3-gallate is an inhibitor of Na+, K(+)-ATPase by favoring the E1 conformation. Biochem Pharmacol 78: 1069-74.
Search in Google Scholar
Ogunbayo OA, Harris RM, Waring RH, Kirk CJ, Michelangeli F. (2008). Inhibition of the sarcoplasmic/endoplasmic reticulum Ca2+-ATPase by flavonoids: a quantitative structure-activity relationship study. IUBMB Life 60: 853-858.
Search in Google Scholar
Pacher P, Beckman JS, Liaudet L. (2007). Nitric oxide and peroxynitrite in health and disease. Physiol Rev 87: 315-424. Review.
Search in Google Scholar
Packer L, Rimbach G, Virgili F. (1999). Antioxidant activity and biologic properties of a procyanidin-rich extract from pine (Pinus maritima) bark, pycnogenol. Free Radical Biology & Medicine 27: 704-724.
Search in Google Scholar
Procházková D, Boušová I, Wilhelmová N. (2011). Antioxidant and prooxidant properties of flavonoids. Fitoterapia 82: 513-523.
Search in Google Scholar
Ramos S. (2007). Effects of dietary flavonoids on apoptotic pathways related to cancer chemoprevention. J Nutr Biochem 18: 427-442.
Search in Google Scholar
Randriamboavonjy V, Pistrosch F, Bölck B, Schwinger RH, Dixit M, Badenhoop K, Cohen RA, Busse R, Fleming I. (2008). Platelet sarcoplasmic endoplasmic reticulum Ca2+-ATPase and mu-calpain activity are altered in type 2 diabetes mellitus and restored by rosiglitazone. Circulation 117: 52-60.
Search in Google Scholar
Restall CJ, Coke M, Phillips E, Chapman D. (1986). Derivative spectroscopy of tryptophan fluorescence used to study conformational transitions in the (Ca2+Mg2+)-adenosine triphosphatase of sarcoplasmic reticulum. Biochim Biophys Acta 874: 305-311.
Search in Google Scholar
Rice-Evans CA, Miller NJ, Paganga G. (1996). Structure-antioxidant activity relationships of flavonoids and phenolic acids. Free Radic Biol Med 20: 933-956.
Search in Google Scholar
Rizvi SI, Zaid MA. (2005). Impairment of sodium pump and Na/H exchanger in erythrocytes from non-insulin dependent diabetes mellitus patients: effect of tea catechins. Clin Chim Acta 354: 59-67.
Search in Google Scholar
Rohdewald P. (2002). A review of the French maritime pine bark extract (Pycnogenol), a herbal medication with a diverse clinical pharmacology. Review. International Journal of Clinical Pharmacology and Therapeutics 40: 158-168.
Search in Google Scholar
Sastre J, Millan A, De La Asuncion JG, Pla JG, Pallardo FV, O' Connor E, Martin JA, Droy-Lefaix MT, Viña J. (1998). A Ginkgo biloba extract (EGb 761) prevents mitochondrial aging by protecting against oxidative stress. Free Radical Biology & Medicine 24: 298-304.
Search in Google Scholar
Schroeter H, Williams RJ, Matin R, Iversen L, Rice-Evans CA. (2000). Phenolic antioxidants attenuate neuronal cell death following uptake of oxidized low-density lipoprotein. Free Radical Biology & Medicine 29: 1222-1233.
Search in Google Scholar
Schimmel KJ, Richel DJ, van den Brink RB, Guchelaar HJ. (2004). Cardiotoxicity of cytotoxic drugs. Cancer Treat Rev 30: 181-191. Review.
Search in Google Scholar
Selvendiran K, Koga H, Ueno T, Yoshida T, Maeyama M, Torimura T, Yano H, Kojiro M, Sata M. (2006). Luteolin promotes degradation in signal transducer and activator of transcription 3 in human hepatoma cells: an implication for the antitumor potential of flavonoids. Cancer Res 66: 4826-4834.
Search in Google Scholar
Sharov VS, Dremina ES, Galeva NA, Williams TD, Schöneich C. (2006). Quantitative mapping of oxidation-sensitive cysteine residues in SERCA in vivo and in vitro by HPLC-electrospray-tandem MS: selective protein oxidation during biological aging. Biochem J 394: 605-615.
Search in Google Scholar
Sheng R, Gu ZL, Xie ML, Zhou WX, Guo CY. (2007). EGCG inhibits cardiomyocyte apoptosis in pressure overload-induced cardiac hypertrophy and protects cardiomyocytes from oxidative stress in rats. Acta Pharmacol Sin 28: 191-201.
Search in Google Scholar
Shoshan V, MacLennan DH. (1981). Quercetin interaction with the (Ca2+ + Mg2+)-ATPase of sarcoplasmic reticulum. J Biol Chem 256: 887-892.
Search in Google Scholar
Štrosová M, Karlovská J, Balgavý P, Horáková L. (2006). Effect of some antioxidants on sarcoplasmic reticulum Ca2+-ATPase activity from rabbit skeletal muscle. Neuroendocrinology Letters 27: 164-167.
Search in Google Scholar
Štrosová MK, Karlovská J, Žižková P, Kwolek-Mirek M, Poništ S, Spickett CM, Horáková Ľ. (2011). Modulation of sarcoplasmic/endoplasmic reticulum Ca(2+)-ATPase activity and oxidative modification during the development of adjuvant arthritis. Arch Biochem Biophys 511: 40-47.
Search in Google Scholar
Štrosová M, Škuciová M., Horáková L. (2005). Oxidative damage to Ca2+-ATPase sarcoplasmic reticulum by HOCl and HNE and protective effect of some antioxidants. Biofactors 23: 111-116.
Search in Google Scholar
Suganuma M, Saha A, Fujiki H. (2011). New cancer treatment strategy using combination of green tea catechins and anticancer drugs. Cancer Sci 102: 317-323. Review.
Search in Google Scholar
Sun C, Fu J, Chen J, Jiang L, Pan Y. (2010). On-line HPLC method for screening of antioxidants against superoxide anion radical from complex mixtures. J Sep Sci 33: 1018-23.
Search in Google Scholar
Taguchi K, Kobayashi T, Hayashi Y, Matsumoto T, Kamata K. (2007). Enalapril improves impairment of SERCA-derived relaxation and enhancement of tyrosine nitration in diabetic rat aorta. Eur J Pharmacol 556: 121-128.
Search in Google Scholar
Taubert D, Breitenbach T, Lazar A, Censarek P, Harlfinger S, Berkels R, Klaus W, Roesen R. (2003). Reaction rate constants of superoxide scavenging by plant antioxidants. Free Radic Biol Med 35: 1599-1607.
Search in Google Scholar
Tipoe GL, Leung TM, Hung MW, Fung ML. (2007). Green tea polyphenols as an antioxidant and anti-inflammatory agent for cardiovascular protection. Cardiovasc Hematol Disord Drug Targets 7: 135-144. Review.
Search in Google Scholar
Tong X, Evangelista A, Cohen RA. (2010). Targeting the redox regulation of SERCA in vascular physiology and disease. Curr Opin Pharmacol 10: 133-138.
Search in Google Scholar
Tsujimoto I, Hikoso S, Yamaguchi O, Kashiwase K, Nakai A, Takeda T, Watanabe T, Taniike M, Matsumura Y, Nishida K, Hori M, Kogo M, Otsu K. (2005). The antioxidant edaravone attenuates pressure overload-induced left ventricular hypertrophy. Hypertension 45: 921-926.
Search in Google Scholar
Townsend PA, Scarabelli TM, Pasini E, Gitti G, Menegazzi M, Suzuki H, Knight RA, Latchman DS, Stephanou A. (2004). Epigallocatechin-3-gallate inhibits STAT-1 activation and protects cardiac myocytes from ischemia/reperfusion-induced apoptosis. FASEB J 18:1621-1623.
Search in Google Scholar
Tupling R, Green H, Senisterra G, Lepock J, McKee N. (2001). Ischemia-induced structural change in SR Ca2+-ATPase is associated with reduced enzyme activity in rat muscle. Am J Physiol Regul Integr Comp Physiol 281: R1681-1688.
Search in Google Scholar
Vanoverberghe K, Vanden Abeele F, Mariot P, Lepage G, Roudbaraki M, Bonnal JL, Mauroy B, Shuba Y, Skryma R. and Prevarskaya N. (2004). Ca2+ homeostasis and apoptotic resistance of neuroendocrine-differentiated prostate cancer cells. Cell Death Differ 11: 321-330.
Search in Google Scholar
Viner, R. I., Ferrington, D. A., Williams, T. D., Bigelow, D. J. and Schöneich, C (1999a) Protein modification during biological aging: selective tyrosine nitration of the SERCA2a isoform of the sarcoplasmic reticulum Ca2+-ATPase in skeletal muscle. Biochem J 340: 657-669.10.1042/bj3400657
Search in Google Scholar
Viner RI, Williams TD. and Schöneich C (1999b) Peroxynitrite modification of protein thiols: oxidation, nitrosilation, and S-glutathiolation of functionally important cysteine residue(s) in the sarcoplasmic reticulum Ca-ATPase. Biochemistry 38: 12408-12415.10.1021/bi990944510493809
Search in Google Scholar
Viskupičová J, Štrosová M, Šturdík E, Horáková Ľ. (2009). Modulating effect of flavonoids and their derivatives on sarcoplasmic reticulum Ca2+-ATPase oxidized by hypochloric acid and peroxinitrite. Neuroendocrinology Letters 30: 148-151.
Search in Google Scholar
Voss P, Engels M, Štrosova M, Grune T, Horakova Ľ. (2008). Protective effect of antioxidants against sarcoplasmic reticulum (SR) oxidation by Fenton reaction, however without prevention of Ca-pump activity. Toxicology In vitro 22: 1726-1733.
Search in Google Scholar
Wictome M, Michelangeli F, Lee AG, East JM. (1992). The inhibitors thapsigargin and 2,5-di(tert-butyl)-1,4-benzohydroquinone favour the E2 form of the Ca2+,Mg(2+)-ATPase. FEBS Lett 304: 109-13.
Search in Google Scholar
Williams SB, Cusco JA, Roddy MA, Johnstone MT, Creager MA. (1996). Impaired nitric oxide-mediated vasodilation in patients with non-insulin-dependent diabetes mellitus. J Am Coll Cardiol 27: 567-74.
Search in Google Scholar
Winkel-Shirley B. (2001). Flavonoid biosynthesis: a colorful model for genetics, biochemistry, cell biology and biotechnology. Plant Physiol 126: 485-493.
Search in Google Scholar
Yang CS, Wang X. (2010). Green tea and cancer prevention. Nutr Cancer 62: 931-937. Review.
Search in Google Scholar
Ying J, Sharov V, Xu S, Jiang B, Gerrity R, Schöneich C, Cohen RA. (2008). Cysteine-674 oxidation and degradation of sarcoplasmic reticulum Ca(2+) ATPase in diabetic pig aorta. Free Radic Biol Med 45: 756-62.
Search in Google Scholar
Zheng J, Lee HC, Bin Sattar MM, Huang Y, Bian JS. (2011). Cardioprotective effects of epigallocatechin-3-gallate against doxorubicin-induced cardiomyocyte injury. Eur J Pharmacol 652: 82-88.
Search in Google Scholar

Flavonoids in prevention of diseases with respect to modulation of Ca-pump function

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