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Dietary Broccoli Sprouts Protect Against Myocardial Oxidative Damage and Cell Death During Ischemia-Reperfusion

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Abstract

Cruciferous vegetables are known for antioxidant and anti-carcinogenic effects. In the current study we asked whether dietary broccoli sprouts can protect the heart from ischemia-reperfusion. Rats were fed either control diet (sham and control groups) or a diet mixed with 2% dried broccoli sprouts for 10 days. After 10 days the isolated hearts were subjected to ischemia for 20 min and reperfusion for 2 h, and evaluated for cell death, oxidative damage, and Nrf2-regulated phase 2 enzyme activities. Broccoli sprouts feeding inhibited markers of necrosis (lactate dehydrogenase release) and apoptosis (caspase-3 activity) by 78–86%, and decreased indices of oxidative stress (thiobarbituric acid reactive substances and aconitase inactivation) by 82–116%. While broccoli sprouts increased total glutathione and activities of the phase 2 enzymes glutamate cysteine ligase and quinone reductase in liver, they did not affect these in ischemic-reperfused heart. While the mechanism is not clear, the results show that a relatively short dietary treatment with broccoli sprouts can strongly protect the heart against oxidative stress and cell death caused by ischemia-reperfusion.

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Abbreviations

DCIP:

2,6-dichloroindophenol

GCL:

glutamate cysteine ligase

GSH:

reduced glutathione

GSSG:

oxidized glutathione

IR:

ischemia-reperfusion

LDH:

lactate dehydrogenase

PMSF:

phenylmethylsulphonyl fluoride

QR:

quinone reductase

TBARS:

thiobarbituric acid reactive substances

References

  1. Nadal-Ginard B, Kajstura J, Leri A, Anversa P (2003) Myocyte death, growth, and regeneration in cardiac hypertrophy and failure. Circ Res 92:139–150

    Article  CAS  Google Scholar 

  2. Beltrami AP, Urbanek K, Kajstura J, Yan SM, Finato N, Bussani R, Nadal-Ginard B, Silvestri F, Leri A, Beltrami A, Anversa P (2001) Evidence that human cardiac myocytes divide after myocardial infarction. N Engl J Med 344:1750–1757

    Article  CAS  Google Scholar 

  3. Ahuja P, Sdek P, MacLellan WR (2007) Cardiac myocyte cell cycle control in development, disease, and regeneration. Physiol Rev 87:521–544

    Article  CAS  Google Scholar 

  4. Murphy E, Steenbergen C (2008) Mechanisms underlying acute protection from cardiac ischemia-reperfusion injury. Physiol Rev 88:581–609

    Article  CAS  Google Scholar 

  5. Dhalla NS, Elmoselhi AB, Hata T, Makino N (2000) Status of myocardial antioxidants in ischemia-reperfusion injury. Cardiovasc Res 47:446–456

    Article  CAS  Google Scholar 

  6. Tanaka M, Mokhtari GK, Terry RD, Balsam LB, Lee KH, Kofidis T, Tsao PS, Robbins RC (2004) Overexpression of human copper/zinc superoxide dismutase (SOD1) suppresses ischemia-reperfusion injury and subsequent development of graft coronary artery disease in murine cardiac grafts. Circulation 110:II200–II206

    Google Scholar 

  7. Chen SY, Hsiao G, Hwang HR, Cheng PY, Lee YM (2006) Tetramethylpyrazine induces heme oxygenase-1 expression and attenuates myocardial ischemia/reperfusion injury in rats. J Biomed Sci 13:731–740

    Article  CAS  Google Scholar 

  8. Chen XL, Kunsch C (2004) Induction of cytoprotective genes through Nrf2/antioxidant response element pathway: a new therapeutic approach for the treatment of inflammatory diseases. Curr Pharm Des 10:879–891

    Article  CAS  Google Scholar 

  9. Juurlink BH (2001) Therapeutic potential of dietary phase 2 enzyme inducers in ameliorating diseases that have an underlying inflammatory component. Can J Physiol Pharmacol 79:266–282

    Article  CAS  Google Scholar 

  10. Keck AS, Finley JW (2004) Cruciferous vegetables: cancer protective mechanisms of glucosinolate hydrolysis products and selenium. Integr Cancer Ther 3:5–12

    Article  CAS  Google Scholar 

  11. Fahey JW, Zhang Y, Talalay P (1997) Broccoli sprouts: an exceptionally rich source of inducers of enzymes that protect against chemical carcinogens. Proc Natl Acad Sci USA 94:10367–10372

    Article  CAS  Google Scholar 

  12. Liu AG, Volker SE, Jeffery EH, Erdman JW (2009) Feeding tomato and broccoli powders enriched with bioactives improves bioactivity markers in rats. J Agric Food Chem 57:7304–7310

    Article  CAS  Google Scholar 

  13. Pereira FM, Rosa E, Fahey JW, Stephenson KK, Carvalho R, Aires A (2002) Influence of temperature and ontogeny on the levels of glucosinolates in broccoli (Brassica oleracea Var. italica) sprouts and their effect on the induction of mammalian phase 2 enzymes. J Agric Food Chem 50:6239–6244

    Article  CAS  Google Scholar 

  14. Moreno DA, Carvajal M, López-Berenguer C, García-Viguera C (2006) Chemical and biological characterisation of nutraceutical compounds of broccoli. J Pharm Biomed Anal 41:1508–1522

    Article  CAS  Google Scholar 

  15. Vasanthi HR, Mukherjee S, Das DK (2009) Potential health benefits of broccoli—a chemico-biological overview. Mini Rev Med Chem 9:749–759

    Article  CAS  Google Scholar 

  16. Whanger PD (2002) Selenocompounds in plants and animals and their biological significance. J Am Coll Nutr 21:223–232

    CAS  Google Scholar 

  17. Finley JW (2003) Reduction of cancer risk by consumption of selenium-enriched plants: enrichment of broccoli with selenium increases the anticarcinogenic properties of broccoli. J Med Food 6:19–26

    Article  CAS  Google Scholar 

  18. Rayman MP, Infante HG, Sargent M (2008) Food-chain selenium and human health: spotlight on speciation. Br J Nutr 100:238–253

    CAS  Google Scholar 

  19. Keck AS, Finley JW (2004) Cruciferous vegetables: cancer protective mechanisms of glucosinolate hydrolysis products and selenium. Integr Cancer Ther 3:5–12

    Article  CAS  Google Scholar 

  20. Ribaya-Mercado JD, Blumberg JB (2004) Lutein and zeaxanthin and their potential roles in disease prevention. J Am Coll Nutr 23:567S–587S

    CAS  Google Scholar 

  21. Calvo MM (2005) Lutein: a valuable ingredient of fruit and vegetables. Crit Rev Food Sci Nutr 45:671–696

    Article  CAS  Google Scholar 

  22. Riso P, Brusamolino A, Moro M, Porrini M (2009) Absorption of bioactive compounds from steamed broccoli and their effect on plasma glutathione S-transferase activity. Int J Food Sci Nutr 60(Suppl 1):56–71

    Article  CAS  Google Scholar 

  23. Granado F, Olmedilla B, Herrero C, Pérez-Sacristán B, Blanco I, Blázquez S (2006) Bioavailability of carotenoids and tocopherols from broccoli: in vivo and in vitro assessment. Exp Biol Med (Maywood) 231:1733–1738

    CAS  Google Scholar 

  24. Eberhardt MV, Kobira K, Keck AS, Juvik JA, Jeffery EH (2005) Correlation analyses of phytochemical composition, chemical, and cellular measures of antioxidant activity of broccoli (Brassica oleracea L. Var. italica). J Agric Food Chem 53:7421–7431

    Article  CAS  Google Scholar 

  25. Cho EJ, Lee YA, Yoo HH, Yokozawa T (2006) Protective effects of broccoli (Brassica oleracea) against oxidative damage in vitro and in vivo. J Nutr Sci Vitaminol (Tokyo) 52:437–444

    Article  CAS  Google Scholar 

  26. Chu YF, Sun J, Wu X, Liu RH (2002) Antioxidant and antiproliferative activities of common vegetables. J Agric Food Chem 50:6910–6916

    Article  CAS  Google Scholar 

  27. Vinson JA, Hao Y, Su X, Zubik L (1998) Phenol antioxidant quantity and quality in foods: vegetables. J Agric Food Chem 46:3630–3634

    Article  CAS  Google Scholar 

  28. Keck AS, Finley JW (2006) Aqueous extracts of selenium-fertilized broccoli increase selenoprotein activity and inhibit DNA single-strand breaks, but decrease the activity of quinone reductase in Hepa 1c1c7 cells. Food Chem Toxicol 44:695–703

    Article  CAS  Google Scholar 

  29. Plumb GW, Lambert N, Chambers SJ, Wanigatunga S, Heaney RK, Plumb JA, Aruoma OI, Halliwell B, Miller NJ, Williamson G (1996) Are whole extracts and purified glucosinolates from cruciferous vegetables antioxidants? Free Radic Res 25:75–86

    Article  CAS  Google Scholar 

  30. Zhu CY, Loft S (2003) Effect of chemopreventive compounds from Brassica vegetables on NAD(P)H:quinone reductase and induction of DNA strand breaks in murine hepa1c1c7 cells. Food Chem Toxicol 41:455–462

    Article  CAS  Google Scholar 

  31. Gill CI, Haldar S, Porter S, Matthews S, Sullivan S, Coulter J, McGlynn H, Rowland I (2004) The effect of cruciferous and leguminous sprouts on genotoxicity, in vitro and in vivo. Cancer Epidemiol Biomarkers Prev 13:1199–1205

    Google Scholar 

  32. Hintze KJ, Keck AS, Finley JW, Jeffery EH (2003) Induction of hepatic thioredoxin reductase activity by sulforaphane, both in Hepa1c1c7 cells and in male Fisher 344 rats. J Nutr Biochem 14:173–179

    Article  CAS  Google Scholar 

  33. Wu L, Noyan Ashraf MH, Facci M, Wang R, Paterson PG, Ferrie A, Juurlink BHJ (2004) Dietary approach to attenuate oxidative stress, hypertension, and inflammation in the cardiovascular system. Proc Natl Acad Sci USA 101:7094–7099

    Article  CAS  Google Scholar 

  34. Modun D, Music I, Katalinic V, Salamunic I, Boban M (2003) Comparison of protective effects of catechin applied in vitro and in vivo on ischemia-reperfusion injury in the isolated rat hearts. Croat Med J 44:690–696

    Google Scholar 

  35. 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

    CAS  Google Scholar 

  36. Zor T, Selinger Z (1996) Linearization of the Bradford protein assay increases its sensitivity: theoretical and experimental studies. Anal Biochem 236:302–308

    Article  CAS  Google Scholar 

  37. Kornberg A (1955) Lactate dehydrogenase of muscle. Methods Enzymol 1:441–454

    Article  CAS  Google Scholar 

  38. Masini E, Pierpaoli S, Marzocca C, Mannaioni PF (2003) Protective effects of a plant histaminase in myocardial ischaemia and reperfusion injury in vivo. Biochem Biophys Res Commun 309:432–439

    Article  CAS  Google Scholar 

  39. Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358

    Article  CAS  Google Scholar 

  40. Takemoto M, Node K, Nakagami H, Liao Y, Grimm M, Takemoto Y, Kitakaze M, Liao JK (2001) Statins as antioxidant therapy for preventing cardiac myocyte hypertrophy. J Clin Invest 108:1429–1437

    CAS  Google Scholar 

  41. Tietze F (1969) Enzymic method for quantitative determination of nanogram amounts of total and oxidized glutathione: applications to mammalian blood and other tissues. Anal Biochem 27:502–522

    Article  CAS  Google Scholar 

  42. White CC, Viernes H, Krejsa CM, Botta D, Kavanagh TJ (2003) Fluorescence-based microtiter plate assay for glutamate-cysteine ligase activity. Anal Biochem 318:175–180

    Article  CAS  Google Scholar 

  43. Spencer CB, Rifkind AB (1990) NAD(P)H: quinone oxidoreductase (DT-diaphorase) in chick embryo liver. Comparison to activity in rat and guinea pig liver and differences in co-induction with 7-ethoxyresorufin deethylase by 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin. Biochem Pharmacol 39:327–335

    Article  CAS  Google Scholar 

  44. Ferrari R, Ceconi C, Curello S, Alfieri O, Visioli O (1993) Myocardial damage during ischaemia and reperfusion. Eur Heart J 14(Suppl G):25–30

    Google Scholar 

  45. Mukherjee S, Gangopadhyay H, Das DK (2008) Broccoli: a unique vegetable that protects mammalian hearts through the redox cycling of the thioredoxin superfamily. J Agric Food Chem 56:609–617

    Article  CAS  Google Scholar 

  46. Yoon HY, Kang NI, Lee HK, Jang KY, Park JW, Park BH (2008) Sulforaphane protects kidneys against ischemia-reperfusion injury through induction of the Nrf2-dependent phase 2 enzyme. Biochem Pharmacol 75:2214–2223

    Article  CAS  Google Scholar 

  47. Skrzypiec-Spring M, Grotthus B, Szelag A, Schulz R (2007) Isolated heart perfusion according to Langendorff-still viable in the new millennium. J Pharmacol Toxicol Methods 55:113–126

    Article  CAS  Google Scholar 

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Acknowledgements

This work was supported by grants from the College of Pharmacy and Nutrition, the Canadian Institutes of Health Research (CIHR), and the Natural Sciences and Engineering Research Council (NSERC). M. Akhlaghi was supported by a PhD fellowship from the Iranian Ministry of Health and Medical Education. Thanks to Dr. Bernhard H. Juurlink and Dr. Paul Lee for the broccoli seeds and helpful advice.

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Correspondence to Masoumeh Akhlaghi.

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Akhlaghi, M., Bandy, B. Dietary Broccoli Sprouts Protect Against Myocardial Oxidative Damage and Cell Death During Ischemia-Reperfusion. Plant Foods Hum Nutr 65, 193–199 (2010). https://doi.org/10.1007/s11130-010-0182-4

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