Skip to main content
SpringerLink
Log in

Correlation between oxidative Stress and Alteration of Intracellular Calcium Handling in Isoproterenol-Induced Myocardial Infarction

  • Published:
Molecular and Cellular Biochemistry Aims and scope Submit manuscript

Abstract

Myocardial Ca2+ overload and oxidative stress are well documented effects associated to isoproterenol (ISO)-induced myocardial necrosis, but information correlating these two issues is scarce. Using an ISO-induced myocardial infarction model, 3 stages of myocardial damage were defined: pre-infarction (0–12 h), infarction (12–24 h) and post-infarction (24–96 h). Alterations in Ca2+ homeostasis and oxidative stress were studied in mitochondria, sarcoplasmic reticulum and plasmalemma by measuring the Ca2+ content, the activity of Ca2+ handling proteins, and by quantifying TBARs, nitric oxide (NO) and oxidative protein damage (changes in carbonyl and thiol groups). Free radicals generated system, antioxidant enzymes and oxidative stress (GSH/GSSG ratio) were also monitored at different times of ISO-induced cardiotoxicity. The Ca2+ overload induced by ISO was counterbalanced by a diminution in the ryanodine receptor activity and the Na+-Ca+2 exchanger as well as by the increase in both calcium ATPases activities (vanadate- and thapsigargine-sensitive) and mitochondrial Ca2+ uptake during pre-infarction and infarction stages. Pro-oxidative reactions and antioxidant defences during the 3 stages of cardiotoxicity were observed, with maximal oxidative stress during the infarction. Significant correlations were found among pro-oxidative reactions with plasmalemma and sarcoplasmic reticulum Ca2+ ATPases, and ryanodine receptor activities at the onset and development of ISO-induced infarction. These findings could be helpful in the design of antioxidant therapies in this pathology.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Bloom S: Reversible and irreversible injury: Calcium as a major determinant. In Cardiac Toxicology, T. Balazs (ed) vol 1Boca Ratón, CRC Press, pp 179–199, 1981

  2. Rona G, Chappel CI, Balazs T, Gaudry R: An infarct-like myocardial lesion and other toxic manifestations produced by isoproterenol in the rat. Arch Pathol 67: 443–455, 1959

    CAS  Google Scholar 

  3. Stanton HC, Brenner G, Mayfield ED: Studies on isoproterenol-induced cardiomegaly in rats. Am Heart J 77: 72–80, 1969

    Article  PubMed  CAS  Google Scholar 

  4. Chappel CI, Rona G, Balazs T: Comparison of cardiotoxic action of certain sympathomimetic amines. Can J Biochem Physiol 37: 35–42, 1959

    PubMed  CAS  Google Scholar 

  5. Pinelli A, Trivulzio S, Tomasoni L, Bertolini B, Brenna S, Bonacina E, Vignati S: Myocardial infarction non-invasively induced in rabbits by administering isoproterenol and vasopressin: protective effects exerted by verapamil. Fundam Clin Pharmacol 18: 657–667, 2004

    Article  PubMed  CAS  Google Scholar 

  6. Chagoya de Sánchez V, Hernández-Muñoz R, López-Barrera F, Yañez L, Vidrio S, Suárez J, Cota-Garza MD, Aranda-Frautro A, Cruz D: Sequential changes of energy metabolism and mitochondrial function in myocardial infarction induced by isoproterenol in rats: a long-term and integrative study. Can J Physiol Pharmacol 75: 1300–1311, 1997

    Article  PubMed  Google Scholar 

  7. Fleckenstein A, Janke J, Doring H, Leder O: Myocardial fiber necrosis due to intracellular calcium overload a new principle in cardiac pathophysiology. In Myocardial Biology, Dhalla NS (ed) University Park press, Baltimore, 4: pp 563, 1974

  8. Bloom S, Davis DL: Calcium as mediator of isoproterenol-induced myocardial necrosis. Am J Pathol 69: 459–470, 1972

    Google Scholar 

  9. Barry WH, Bridge JHB: Intracellular calcium homeostasis in cardiac myocytes. Circulation 87: 1806–1815, 1993

    PubMed  CAS  Google Scholar 

  10. Bers DM: Measurement of calcium transport in heart using modern approaches. New Horizons 4: 36–44, 1996

    PubMed  CAS  Google Scholar 

  11. Singal PK, Kapur N, Dhillonn KS, Beanish RE, Dhalla NS: Role of free radicals in catecholamine-induced cardiomyopathy. Can J Physiol Pharmacol 60: 1390–1397, 1982

    PubMed  CAS  Google Scholar 

  12. Loten EG, Redshaw-Loten JC: Preparation of rat liver plasma membrane in a high yield. Anal. Biochem 154: 183–185, 1986

    Article  PubMed  CAS  Google Scholar 

  13. Dixon IM, Hata T, Dhalla NS: Sarcolemmal calcium transport in congestive heart failure due to myocardial infarction in rats. Am J. Physiol 262: H1387–H1394, 1992

    PubMed  CAS  Google Scholar 

  14. Saborido A, Delgado J, Megías A: Measurement of sarcoplasmic reticulum Ca2+ ATPase activity and E-type Mg2+-ATPase activity in rat heart homogenates. Anal Biochem 268: 79–88, 1999

    Article  PubMed  CAS  Google Scholar 

  15. Chu A, Dickson MC, Saito A, Seiler S, Fleischer S: Isolation of sarcoplasmic reticulum fractions referable to longitudinal tubules and junctional tubules and junctional terminal cisternae from rabbit skeletal muscle. Methods Enzymol 157: 36–46, 1988

    Article  PubMed  CAS  Google Scholar 

  16. Shah KR, Matsubara T, Foerster DR, Xu YJ, Dhalla NS: Mechanisms of inotropic responses of the isolated rat hearts to vanadate. Int. J Cardiol 52: 101–113, 1995

    Article  PubMed  CAS  Google Scholar 

  17. Sharma VK, Ramesh V, Franzini-Armstrong C, Sheu SS: Transport of Ca2+ from sarcoplasmic reticulum to mitochondria in rat ventricular myocytes. J Bioenerg Biomemb 32: 97–104, 2000

    Article  CAS  Google Scholar 

  18. Hamilton SL, Mejía Alvarez R, Fill M, Hakes MJ, Brush KL, Scilling WP, Stefani E: [3H]PN200-110 and [3H] ryanodine binding and reconstitution of ion channel-activity with skeletal muscle membranes. Anal Biochem 183: 31–41, 1989

    Article  PubMed  CAS  Google Scholar 

  19. Vázquez-Martínez O, Cañedo-Merino R, Díaz-Muñoz M, Riesgo-Escovar R: Biochemical characterization, distribution and phylogenetic analisis of Drosophila melanogaster ryanodine and IP3 receptors, and thapsigargin-sensitive Ca2+ ATPase. J Cell Sci 116: 2483–2494, 2003

    Article  PubMed  CAS  Google Scholar 

  20. Furiuchi T, Simon-Chazottes D, Fujino I, Yamada N, Hasegawa M, Miyawaki A, Yoshikawa S, Guénet J, Mikoshiba K: Widespread expression of inositol 1,4,5-triphosphate receptor type 1 gene (Insp3rl) in the mouse central nervous system. Receptors & Channels 1:11–24, 1993

    Google Scholar 

  21. Brinley FJ. Jr, Tiffert T, Scarpa A: Mitochondria and other calcium buffers of squid axon studied in situ. J Gen Physiol 72: 101–127, 1978

    Article  PubMed  CAS  Google Scholar 

  22. Chavez E, Zazueta C, Cuéllar A, Reyes-Vicas H, García N: Oxygen free-radicals mediate the damaging effect of ultraviolet light on membrane mitochondria. Biochem Mol Biol Intern 46:207–214, 1998

    Google Scholar 

  23. Morita A, Kimura M, Itokawa I: The effect of aging on the mineral status of female mice. Biol Trace Elem Res 42: 165–177, 1994

    PubMed  CAS  Google Scholar 

  24. Akerboom TPM, Sies H: Assay of glutathione, glutathione disulfide and glutathione mixed disulfides in biological samples. Methods Enzymol 77: 373–382, 1981

    PubMed  CAS  Google Scholar 

  25. Buege JA, Aust SD: Microsomal lipid peroxidation. Methods Enzymol 52: 302–310, 1978

    PubMed  CAS  Google Scholar 

  26. Hernández-Muñoz R, Glender W, Diaz-Muñoz M, García-Sainz JA, Chagoya de Sánchez V: Effects of adenosine on liver cell damage induced by carbon tetrachloride. Biochem Pharmacol 33: 2599–2604, 1984

    Article  PubMed  Google Scholar 

  27. Shultz PJ, Tayeh MA, Marletta MA, Raij L: Synthesis and action of nitric oxide in rat glomerular mesangial cells. Am J Physiol 261: F600–F606, 1991

    PubMed  CAS  Google Scholar 

  28. McCord JM, Fridovich I: An enzymatic function for erythrocuprein (hemocuprein). J Biol Chem 244: 66049–66055, 1969

    Google Scholar 

  29. Stirpe F, Della Corte E: The regulation of rat liver xanthine oxidase. J Biol Chem 244: 3855–3863, 1965

    Google Scholar 

  30. Sultatos LG: Effects of acute ethanol administration on the hepatic xanthine dehydrogenase/oxidase system in the rat. J Pharmacol Exp Ther 246: 946–949, 1988

    PubMed  CAS  Google Scholar 

  31. Lùck H: Catalase In Methods of Enzymatic Analysis, HU. Bergmeyer (ed). VCH Weinheim, Germany, 885–888, 1965]

  32. Oliver CN, Alm BW, Moermann EJ, Goldstein S, Stadman ER: Age related changes in oxidized proteins. J Biol Chem 262: 5488–5491, 1987

    PubMed  CAS  Google Scholar 

  33. Sedlak J, Lindsay RH: Estimation of total protein bound and non protein sulfhydryl groups in tissue with Ellman's reagent. Anal Biochem 25: 192–205, 1968

    Article  PubMed  CAS  Google Scholar 

  34. Lowry OH, Rosebrough NL, Farr AL, Randall RJ: Protein measurement with Folin phenol reagent. J Biol Chem 193: 265–275, 1951

    PubMed  CAS  Google Scholar 

  35. Gornall AG, Bradwill CJ, David MM: Determination of serum protein by means of the biuret reaction. J Biol Chem 177: 751–766, 1949

    PubMed  CAS  Google Scholar 

  36. Choudhary G, Dudley SC Jr: Heart failure, oxidative stress, and ion channel modulation. Congest Heart Fail 8: 148–155, 2002

    PubMed  CAS  Google Scholar 

  37. Piuhola J, Hammes A, Schu K, Neyses L, Vuolteenaho O, Ruskoaho H: Overexpression of sarcolemmal calcium pump attenuates induction of cardiac gene expression in response to ET-1. Am J Physiol Regul Integr Comp Physiol 281: R699–R705, 2001

    PubMed  CAS  Google Scholar 

  38. Zhang Q, Scholz PM, He Y, Tse J, Weiss HR: Cyclic GMP signaling and regulation of SERCA activity during cardiac myocyte contraction. Cell Calcium 37: 259–266, 2005

    Article  PubMed  CAS  Google Scholar 

  39. Kaplan P, Babusikova E, Lehotsky J, Dobrota D: Free radical-induced protein modification and inhibition of Ca2+-ATPase of cardiac sarcoplasmic reticulum. Mol Cell Biochem 248: 41–47, 2003

    Article  PubMed  CAS  Google Scholar 

  40. Ray RS, MaCord JM: Ischemia-induced conversion of xanthine dehydrogenase to xanthine oxidase. Fed Proc 41: 767–773, 1982

    Google Scholar 

  41. Reimer KA, Murry CE, Richard JJ: The role of neutrophils and free radicals in the ischemia reperfused heart: Why the confusion and controversy? J Mol Cell Cardiol 21: 1225–1239, 1989

    Article  PubMed  CAS  Google Scholar 

  42. Yates JC, Beamish RE, Dhalla NS: Ventricular dysfunction and necrosis produced by adrenochrome metabolite of epinephrine: relation to pathogenesis of catecholamine cardiomyopathy. Am Heart J 102: 210–221, 1981

    Article  PubMed  CAS  Google Scholar 

  43. Tappia PS, Hata T, Hozaina L, Sandhu MS, Panagia V, Dhalla NS: Role of oxidative stress in catecholamine-induced changes in cardiac sarcolemmal Ca2+ transport. Arch Biochem Biophys 387: 85–92, 2001

    Article  PubMed  CAS  Google Scholar 

  44. Kanai AJ, Mesaros S, Finkel MS, Oddis CV, Biorder LA, Malinski T: Beta-adrenergic regulation of constitutive nitric oxide synthase in cardiac myocytes. Am J Physiol 273: C1371–C1377, 1997

    PubMed  CAS  Google Scholar 

  45. Weglicki W, Waite BM, Stam AC: Association of phospholiopase A with a myocardial membrane preparation containing (Na+−K+). Mg2+ ATPase. J Mol Cell Cardiol 4: 195–201, 1972

    Article  PubMed  CAS  Google Scholar 

  46. Reimer KA, Jennings RB: Failure of the xanthine oxidase inhibitor allopurinol to limit infarct size after inchemia and reperfusion in dogs. Circulation 71: 1069–1075, 1985

    PubMed  CAS  Google Scholar 

  47. Werns SW, Shea MJ, Mitsos SE, Dysko RC, Fantone JC, Schark MA, Abrams GD, Pitt B, Lucchesi BR: Reduction of the size of infarction by allopurinol in the ischemic-reperfused canine heart. Circulation 73: 518–524, 1986

    PubMed  CAS  Google Scholar 

  48. Goode HF, Webster NR: Free radicals and antioxidants in sepsis. Crit Care Med 21: 1770–1776, 1993

    PubMed  CAS  Google Scholar 

  49. Zahradnikova A, Minarovic I, Venema RC, Meszaros LG: Inactivation of the cardiac ryanodine receptor calcium release channel by nitric oxide. Cell Calcium 22: 447–454, 1997

    Article  PubMed  CAS  Google Scholar 

  50. Kijima Y, Saito A, Jetton TL, Magnuson MA, Fleischer S: Different intracellular localization of inositol 1,4,5-triphosphate and ryanodine receptors in cardiomyocytes. J Biol Chem 268: 3499–3506, 1993

    PubMed  CAS  Google Scholar 

  51. Schuh K, Uldrijan S, Telkamp M, Rothlein N, NeysesI: The plasmamembrane calmoduline-dependent calcium pump: a major regulator of nitric oxide synthase I. J Cell Biol 155: 201–205, 2001

    Article  PubMed  CAS  Google Scholar 

  52. Estabrook RW, Werringloer, J: Cytochrome P450, its role in oxygen activation for drug metabolism. In Drug Metabolism Concepts. Donals MJ. Roberts RG Eds. American Chem Soc pp1; 1976

Download references

Author information

Authors and Affiliations

  1. Departamento de Neurobiología Celular y Molecular, Instituto de Neurobiología, Universidad Nacional Autónoma de México, Campus Juriquilla-Querétaro, México, México

    Mauricio Díaz-Muñoz & Marco Antonio Álvarez-Pérez

  2. Departamento de Biología Celular, Instituto de Fisiología Celular, Universidad Nacional Autónoma de México, Circuito ext. s/n Ciudad Universitaria, México, D.F., 04510, México

    Lucía Yáñez, Susana Vidrio, Lidia Martínez, Gisele Rosas, Mario Yáñez, Sotero Ramírez & Victoria Chagoya de Sánchez Ph.D

Authors
  1. Mauricio Díaz-Muñoz
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marco Antonio Álvarez-Pérez
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lucía Yáñez
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Susana Vidrio
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Lidia Martínez
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Gisele Rosas
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Mario Yáñez
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Sotero Ramírez
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Victoria Chagoya de Sánchez Ph.D
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Victoria Chagoya de Sánchez Ph.D.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Díaz-Muñoz, M., Álvarez-Pérez, M.A., Yáñez, L. et al. Correlation between oxidative Stress and Alteration of Intracellular Calcium Handling in Isoproterenol-Induced Myocardial Infarction. Mol Cell Biochem 289, 125–136 (2006). https://doi.org/10.1007/s11010-006-9155-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11010-006-9155-1

Keywords

Search

Navigation