Article

Inhibition of the Late Sodium Current with Ranolazine - A New Cardioprotective Mechanism

Register or Login to View PDF Permissions
Permissions× For commercial reprint enquiries please contact Springer Healthcare: ReprintsWarehouse@springernature.com.

For permissions and non-commercial reprint enquiries, please visit Copyright.com to start a request.

For author reprints, please email rob.barclay@radcliffe-group.com.
Average (ratings)
No ratings
Your rating

Disclosure:Both authors have a collaboration/grant with CV Therapeutics.

Acknowledgements:Lars S Maier and Gerd Hasenfuss are funded by the Deutsche Forschungsgemeinschaft (DFG) through grants for a clinical research group (MA 1982/2-1), and Lars S Maier is also funded by a DFG Heisenberg grant (MA 1982/3-1).

Copyright Statement:

The copyright in this work belongs to Radcliffe Medical Media. Only articles clearly marked with the CC BY-NC logo are published with the Creative Commons by Attribution Licence. The CC BY-NC option was not available for Radcliffe journals before 1 January 2019. Articles marked ‘Open Access’ but not marked ‘CC BY-NC’ are made freely accessible at the time of publication but are subject to standard copyright law regarding reproduction and distribution. Permission is required for reuse of this content.

Current Therapeutic Strategies in Stable Angina Pectoris

Current strategies of drug-induced relief of symptoms in patients with coronary heart disease aim to improve the imbalance between oxygen supply to the heart and oxygen demand, which is well known to be relevant for myocardial ischaemia and hence angina pectoris.1 The agents that reduce myocardial oxygen demand are mainly beta-blockers, calcium channel antagonists, nitrates, potassium channel openers and sinus node inhibitors. This occurs either by direct myocardial effects or indirectly by complex effects on haemodynamic determinants.2 Calcium channel antagonists, nitrates and potassium channel openers may also improve blood flow and thus oxygen supply to the heart. Ranolazine, a piperazine derivative that was recently approved in the EU, is a new anti-ischaemic drug for the treatment of angina pectoris whose mode of action is completely different from the pharmacological principles mentioned above.3

Pathophysiology of Myocardial Ischaemia and the Role of Intracellular Sodium and Calcium

Myocardial ischaemia results in reduced mitochondrial adenosine triphosphate (ATP) production in the heart and hence reduced energy supply to various key proteins for excitation–contraction coupling, leading to a dysregulation of ionic homeostasis of the individual cardiac myocyte, which is associated with contractile dysfunction and, when severe and prolonged, is followed by marked cellular depolarisation and cell death.

An early event during ischaemia with a decrease in intracellular pH is a rise in the cytosolic sodium concentration (see Figure 1). In general, there are several mechanisms by which a lack of energy increases intracellular sodium levels. A large portion of the sodium enters the cell through the cardiac sodium channel in the sarcolemma following depolarisation during the initial phase (fast upstroke) of the action potential. This sodium influx causes further rapid depolarisation, leading to the activation of voltage-gated L-type calcium channels, causing calcium influx into the cytosol from the extracellular space. Sodium channels spontaneously inactivate quickly within a few milliseconds. Channels recycle and may be activated by the next membrane depolarisation during the following action potential.4,5 It has been shown that this sodium current may be altered during pathophysiological conditions such as hypoxia, exposure to ischaemic metabolites and reactive oxygen species, as well as heart failure.

Under those conditions, there is a pronounced late opening of the sodium channel up to a few hundreds of milliseconds following depolarisation, which is referred to as persistent or late sodium current (INa,late) (see Figure 2A).6-9 INa,late may therefore represent a major source for increased intracellular sodium during ischaemia. Other mechanisms leading to disturbed sodium balance include sodium influx through the sodium-proton exchanger pump in response to intracellular acidification10 or a lack of sodium elimination through the sodium potassium ATPase.

In addition to the effects on intracellular sodium, a lack of energy and the resulting decrease in the phosphorylation potential reduce free energy available for calcium transport into the sarcoplasmic reticulum, the main intracellular source for calcium, during diastole, and therefore intracellular calcium accumulates in the cytosol. As a consequence, elevated diastolic calcium levels activate contractile proteins directly even during diastole, leading to incomplete relaxation and diastolic dysfunction.

Although altered sodium handling itself cannot activate myofilaments, this increase in intracellular sodium leads to tremendous changes in the myocytes. Disturbed sarcoplasmic reticulum calcium accumulation is severely aggravated by elevated intracellular sodium. This occurs mainly through the sarcolemmal sodium–calcium exchanger (NCX), which exchanges one calcium ion for three sodium ions per cycle (see Figure 2B). The NCX can work in two different directions. In its forward mode it eliminates calcium outside the cell to accomplish diastolic relaxation (in addition to calcium reuptake into the sarcoplasmic reticulum). In its reverse mode (usually during the action potential, i.e. systolic activation) it brings calcium into the cell in exchange for transsarcolemmal elimination of sodium. The activity and direction of transport depends on the abundance of the protein, as well as on the membrane potential, intracellular sodium and intracellular calcium concentration. Sodium accumulation following myocardial hypoxia (i.e. through INa,late) promotes reverse-mode NCX and therefore reduces the overall cellular capacity to eliminate calcium outside the cytosol. This adds to the elevated diastolic calcium due to reduced sarcoplasmic reticulum calcium pump activity and further aggravates diastolic dysfunction due to contractile protein activation. Diastolic activation of contractile proteins is associated with extra energy consumption.11

In addition, increased diastolic tone increases microcirculatory resistance and further impairs the energy balance of the ischaemic myocardium. Therefore, diastolic dysfunction following myocardial ischaemia increases energy consumption and aggravates disturbed energy balance like a vicious cycle (see Figure 3), and cellular calcium overload is believed to be a major contributor to the impairment of left ventricular relaxation caused by ischaemia/reperfusion.

However, calcium overload also has adverse consequences for myocardial electrical activity because it may lead to recurrent spontaneous releases of calcium ions from the sarcoplasmic reticulum, which, in turn, cause delayed after-depolarisations (see Figure 2C) that may lead to triggered activity, increased beat-to-beat variability of action potential duration and ventricular tachycardia. Thus, myocardial cell calcium overload has a direct role in causing mechanical and electrical dysfunction of the ischaemic myocardium.

Ranolazine has been shown to be a potent inhibitor of INa,late and therefore interrupts a major step in the pathophysiology of myocardial ischaemia and dysregulation of intracellular ion homeostasis (see Figure 3).12

Mode of Action of Ranolazine

In myocytes from dog and guinea pig hearts, ranolazine was shown to cause concentration-, voltage- and frequency-dependent inhibition of INa,late.12 Ranolazine was also shown to prevent an H2O2-induced increase in INa,late.13 Most specifically, ranolazine has been shown to reverse the sustained rise in diastolic and systolic calcium caused by a well-known enhancer of INa,late, the sea anemone toxin ATX-II.14,15 Taken together, the major mechanism of action of ranolazine is to inhibit INa,late, thus preventing sodium overloading of the cell. As a consequence, ranolazine prevents reverse-mode sodium–calcium exchange and thus diastolic accumulation of calcium, possibly resulting in improved diastolic tone, as was previously shown in vivo in 15 patients with a prior myocardial infarction.16 It was also shown recently in vitro in isolated muscle strip preparations from end-stage failing human hearts (see Figure 4).17 In addition, ranolazine has been shown to decrease post-ischaemic contracture in rabbit isolated, perfused hearts subjected to ischaemia and reperfusion.18

As an INa,late inhibitor, ranolazine was also shown to increase action potential duration and thus QT interval modestly by 2–5ms.19,20 This effect, however, is not heart rate dependent and, most importantly, cannot be exaggerated during bradycardia.21-23 In addition, ranolazine does not induce early after-depolarisations and does not increase dispersion of repolarisation across the left ventricular wall.21 According to this profile, ranolazine does not increase the risk of torsade de pointes tachycardia as is observed with many other QT interval prolonging agents. In contrast, in patients with type 3 long-QT syndrome where INa,late is increased, ranolazine shortens corrected QT (QTc) and improves diastolic relaxation.24 In addition, anti-arrhythmic effects are increasingly reported for both supraventricular25 and ventricular arrhythmias.26

Clinical Effects of Ranolazine

Ranolazine has been studied in several clinical trials. Three initial trials investigated the efficacy of immediate-release ranolazine.27–29 Two larger phase III studies examined the efficacy of sustained-release ranolazine in patients with chronic stable angina. Monotherapy Assessment of Ranolazine In Stable Angina (MARISA) randomised 191 patients to placebo or ranolazine in a crossover design with a one-week treatment period.19 Combination Assessment of Ranolazine in Stable Angina (CARISA) randomised patients to placebo or ranolazine in addition to previous anti-anginal therapy. Treatment was maintained for 12 weeks.20 MARISA showed that ranolazine monotherapy significantly improved exercise performance in patients with stable angina. This was true for exercise duration, time to angina and time to 1mm ST segment depression. More specifically, 70% of patients in the placebo group stopped their exercise test because of angina, compared with only 52% in the ranolazine group (1.5g bi-daily). CARISA improved peak and trough exercise duration, time to angina and time to 1mm ST depression. These effects were sustained through a 12-week treatment. Ranolazine also reduced the number of angina attacks from a baseline of 4.5 per week to 2.1 per week for ranolazine (1g bi-daily), compared with 3.3 per week for placebo. Most importantly, the anti-anginal effects of ranolazine in MARISA and CARISA occurred without clinically meaningful changes in heart rate or blood pressure.

In the Metabolic Efficiency with Ranolazine for Less Ischaemia in Non-ST elevation acute coronary syndrome (MERLIN) Thrombolysis In Myocardial Infarction (TIMI)-36 trial the effect of the clinical outcome of ranolazine therapy was studied in patients with acute coronary syndromes (ACS).30 MERLIN was a multinational, double-blind, randomised, placebo-controlled, parallel-group clinical trial designed to evaluate the efficacy and safety of ranolazine during acute and long-term treatment in 6,560 patients with non-ST elevation ACS treated with standard therapy. Within 48 hours of the onset of angina due to ACS, eligible hospitalised patients were enrolled in the study and randomised to receive intravenous ranolazine or placebo, followed by long-term treatment with ranolazine tablets or placebo. Although ranolazine did not significantly influence the primary combined endpoint of cardiovascular death, myocardial infarction or recurrent ischaemia, additional analyses revealed a 13% relative reduction in the risk of recurrent ischaemia. In addition, ranolazine was favourable regarding safety end-points. In particular, potential anti-arrhythmic effects of ranolzine became apparent.31 This underlines experimental data.25 Thus, inhibition of INa,late with ranolazine is safe, in particular regarding electrophysiological aspects. Although the results of MERLIN do not support the use of ranolazine for acute management of ACS, these findings support previous evidence regarding the safety and benefit of ranolazine as an anti-anginal therapy and suggest a benefit of ranolazine in a broad population of patients with established ischaemic heart disease.

Future Aspects for Clinical Applications of Ranolazine

Inhibition of enhanced INa,late by ranolazine may represent a new treatment option for cardiac diseases associated with disturbed myocardial ion homeostasis, with a focus on patients with altered intracellular sodium homeostasis. Elevated intracellular sodium has been observed in human heart failure and in several animal failure models.32,33 It has been shown recently that increased intracellular sodium in heart failure may, in part, result from calcium/calmodulin-dependent protein kinase II phosphorylation of sodium channels with a subsequent increase in INa,late.34 Therefore, ranolazine may be an interesting approach for the treatment of systolic heart failure by improving disturbed sodium homeostasis. In addition, calcium overload subsequent to disturbed sodium homeostasis may also be a major pathophysiological factor in diastolic heart failure. Therefore, we speculate that in diastolic heart failure due to disturbed sodium/calcium homeostasis, ranolazine may represent a new attractive treatment option. Even more noteworthy is that inhibition of INa,late may be a novel anti-arrhythmic approach targeting supraventricular as well as ventricular tachycardia. Accordingly, studies in heart failure with systolic and diastolic dysfunction, as well as trials in patients with atrial fibrillation, are warranted to test the broad and potential therapeutical benefit of ranolazine.

References

  1. Messerli FH, Mancia G, Conti CR, Pepine CJ, Europ Heart J, 2006;27(23):2902–3
    Crossref | PubMed
  2. Heusch G, Schulz R, Basic Res Cardiol, 2001;96:1–10.
    Crossref | PubMed
  3. Belardinelli L, Antzelevitch C, Fraser H, Europ Heart J, 2004;6 (Suppl. I):13–17.
    Crossref
  4. Maier LS, Bers DM, Cardiovasc Res, 2007;73:631–40.
    Crossref | PubMed
  5. Wagner S, Maier LS, J Cardiovasc Electrophysiol, 2006;17 (Suppl. 1):S26–33.
    Crossref | PubMed
  6. Ju YK, Saint DA, Gage PW, J Physiol, 1996;497(Pt 2):337–47.
    Crossref | PubMed
  7. Undrovians AI, Fleidervish IA, Makielski JC, Circ Res, 1992;71:1231–41.
    Crossref | PubMed
  8. Wu J, Corr PB, Am J Physiol, 1994;266:H1034≠H1046.
    PubMed
  9. Ward CA, Giles WR, J Physiol, 1997;500(Pt 3):631–42.
    Crossref | PubMed
  10. Clanachan AS, CVT Technical Report Number CVT303.093-P, 2004.
  11. Meyer M, Keweloh B, Guth K, et al., J Mol Cell Cardiol, 1998;30(8):1459–70.
    Crossref | PubMed
  12. Antzelevitch C, Belardinelli L, Zygmunt AC, et al., Circulation, 2004;110:904–10.
    Crossref | PubMed
  13. Song Y, Shryock JC, Wagner S, et al., J Pharmacol Exp Ther, 2006;318:214–22.
    Crossref | PubMed
  14. Song Y, Shryock JC, Wu L, et al., J Cardiovasc Pharmacol, 2004;44:192–9.
    Crossref | PubMed
  15. Fraser H, Belardinelli L, Wang L, et al., J Mol Cell Cardiol, 2006;41:1031–8.
    Crossref | PubMed
  16. Hayashida W, van Eyll C, Rousseau MF, Pouleur H, Cardiovasc Drugs Ther, 1994;8:741–7.
    Crossref | PubMed
  17. Sossalla SR, Rasenack ECL, Wagner S, et al., J Mol Cell Cardiol, 2008;45:32–43.
    Crossref | PubMed
  18. Gralinski MR, Black SC, Kilgore KS, et al., Cardiovasc Res, 1994;28:1231–7.
    Crossref | PubMed
  19. Chaitman BR, Skettino SL, Parker JO, et al., J Am Coll Cardiol, 2004;43:1375–82.
    Crossref | PubMed
  20. Chaitman BR, Pepine CJ, Parker JO, et al., J Am Med Assoc, 2004;291:309–16.
    Crossref | PubMed
  21. Antzelevitch C, Belardinelli L, Zygmunt AC, et al., Circulation, 2004;110:904–10.
    Crossref | PubMed
  22. Wu L, Shryock JC, Song Y, et al., J Pharmacol Exp Ther, 2004;310:599–605.
    Crossref | PubMed
  23. Okada Y, Ogawa S, Sadanaga T, et al., J Am Coll Cardiol, 1996;27:84–9.
    Crossref | PubMed
  24. Moss AJ, Zareba W, Schwarz KQ, et al., J Cardiovasc Electrophysiol, 2008 Jul 25 [Epub ahead of print].
  25. Burashnikov A, Di Diego JM, Zygmunt AC, et al., Circulation, 2007;116:1449–57.
    Crossref | PubMed
  26. Wang WQ, Robertson C, Dhalla AK, Belardinelli L, J Pharmacol Exp Ther, 2008;325(3):875–81.
    Crossref | PubMed
  27. Cocco G. Rousseau MF, Bouvy T, et al., J Cardiovasc Pharmacol, 1992;20:131–8.
    Crossref | PubMed
  28. Rousseau MF, Visser FG, Bax JJ, Eur Heart J, 1994;15(Suppl.):95.
  29. Pepine CJ, Wolff AA, Am J Cardiol, 1999;84:46–50.
    Crossref | PubMed
  30. Morrow DA, Scirica BM, Karwatoswska-Prokopczuk E, et al., JAMA, 2007;297(16):1775–83.
    Crossref | PubMed
  31. Scirica BM, Morrow DA, Hod H, et al., Circulation, 2007;116:1647–52.
    Crossref | PubMed
  32. Pieske B, Maier LS, Piacentino III V , et al., Circulation, 2002;106:447–53
    Crossref | PubMed
  33. Maier LS, Hasenfuss G. Europ Heart J, 2006;8 (Suppl. A):A6–A9.
    Crossref
  34. Wagner S, Dybkova N, Rasenack ECL, et al., J Clin Invest,2006;116:3127–38.
    Crossref | PubMed
  35. Bers DM, Kluwer Academic Publishers, Dordrecht, The Netherlands, 2001.