Acute sleep deprivation preconditions the heart against ischemia/ reperfusion injury: the role of central GABA-A receptors

Document Type : Original Article

Authors

1 Department of Physiology, School of Medicine, Tehran University of Medical Sciences, Tehran, Iran

2 Occupational Sleep Research Center, Baharloo Hospital, Tehran University of Medical Sciences, Tehran, Iran

3 Department of Physiology, School of Medicine, Ahwaz University of Medical Sciences, Ahwaz, Iran

4 Department of Genetic, School of Medicine, Tehran University of Medical Sciences, Tehran, Iran

5 Department of Anatomy, School of Medicine, Tehran University of Medical Sciences, Tehran, Iran

6 Department of Physiology, School of Medicine, Tehran University of Medical Sciences, International Campus, Tehran, Iran

Abstract

Objective(s): Central γ-aminobutyric acid (GABA) neurotransmission modulates cardiovascular functions and sleep. Acute sleep deprivation (ASD) affects functions of various body organs via different mechanisms. Here, we evaluated the effect of ASD on cardiac ischemia/reperfusion injury (IRI), and studied the role of GABA-A receptor inhibition in central nucleus of amygdala (CeA) by assessing nitric oxide (NO) and oxidative stress.
Materials and Methods: The CeA in sixty male Wistar rats was cannulated for saline or bicuculline (GABA-A receptor antagonist) administration. All animals underwent 30 min of coronary occlusion (ischemia), followed by 2 hr reperfusion (IR). The five experimental groups (n=12) included are as follows: IR: received saline; BIC+IR: received Bicuculline; MLP+IR: received saline, followed by the placement of animals in an aquarium with multiple large platforms; ASD+IR: underwent ASD in an aquarium with multiple small platforms; and BIC+ASD+IR: received bicuculline prior to ASD.
Results: Bicuculline administration increased the malondialdehyde levels and infarct size, and decreased the NO metabolites levels and endothelial nitric oxide synthase (eNOS) gene expression in infarcted and non-infarcted areas in comparison to IR group. ASD reduced malondialdehyde levels and infarct size and increased NO metabolites, corticosterone levels and eNOS expression in infarcted and non-infarcted areas as compared to the IR group. Levels of malondialdehyde were increased while levels of NO metabolites, corticosterone and eNOS expression in infarcted and non-infarcted areas were reduced in the BIC+ASD+IR as compared to the ASD+IR group.
Conclusion: Blockade of GABA-A receptors in the CeA abolishes ASD-induced cardioprotection by suppressing oxidative stress and NO production.

Keywords


1. Chen WR, Liu HB, Sha Y, Shi Y, Wang H, Dai Chen Y, et al. Effects of statin on arrhythmia and heart rate variability in healthy persons with 48‐hour sleep deprivation. J Am Heart Assoc 2016; 5:1-8.
2. Edalatyzadeh Z, Imani A, Faghihi M, Choopani S, Askari S, Aghajani M, et al. Effect of acute sleep deprivation on ischemia-induced ventricular arrhythmia in the isolated rat heart. JSS 2016; 1:38-43.
3. Pace M, Adamantidis A, Facchin L, Bassetti C. Role of REM sleep, melanin concentrating hormone and orexin/hypocretin systems in the sleep deprivation pre-ischemia. PloS one 2017; 12:1-22.
4. Tobaldini E, Covassin N, Calvin A, Singh P, Bukartyk J, Wang S, et al. Cardiac autonomic control and complexity during sleep are preserved after chronic sleep restriction in healthy subjects. Physiol Rep 2017; 5:1-8.
5. Shen X-Z, Koo MW, Cho C-H. Sleep deprivation increase the expression of inducible heat shock protein 70 in rat gastric mucosa. World J Gastroenterol 2001; 6: 273-281.
6. Weil ZM, Norman GJ, Karelina K, Morris JS, Barker JM, Su AJ, et al. Sleep deprivation attenuates inflammatory responses and ischemic cell death. Exp Neurol 2009; 218:129-136.
7. Avolio E, Mahata S, Mantuano E, Mele M, Alò R, Facciolo R, et al. Antihypertensive and neuroprotective effects of catestatin in spontaneously hypertensive rats: interaction with GABAergic transmission in amygdala and brainstem. Neuroscience 2014; 270:48-57.
8. Chen L. WW, Tan T.,Han H.,Dong Z. GABA(A) receptors in the central nucleus of the amygdala are involved in pain- and itch-related responses. J Pain 2016; 17:181-189.
9. Vaz G, Bahia A, De Figueiredo Müller-Ribeiro F, Xavier C, Patel KP, Santos R, et al. Cardiovascular and behavioral effects produced by administration of liposome-entrapped GABA into the rat central nervous system. Neuroscience 2015; 285:60-69.
10. Chanana P, Kumar A. GABA-BZD receptor modulating mechanism of panax quinquefolius against 72-h sleep deprivation induced anxiety like behavior: possible roles of oxidative stress, mitochondrial dysfunction and neuroinflammation. Front Neurosci 2016; 10:1-16.
11. Luppi P-H, Peyron C, Fort P. Not a single but multiple populations of GABAergic neurons control sleep. Sleep Med Rev 2017; 32:85-94.
12. Matsuki T, Takasu M, Hirose Y, Murakoshi N, Sinton C, Motoike T, et al. GABA A receptor-mediated input change on orexin neurons following sleep deprivation in mice. Neuroscience 2015; 284:217-224.
13. Matsuki T, Nomiyama M, Takahira H, Hirashima N, Kunita S, Takahashi S, et al. Selective loss of GABAB receptors in orexin-producing neurons results in disrupted sleep/wakefulness architecture. Proc Natl Acad Sci 2009; 106:4459-4464.
14. Modirrousta M, Mainville L, Jones BE. Dynamic changes in GABA A receptors on basal forebrain cholinergic neurons following sleep deprivation and recovery. BMC Neurosci 2007; 8:1-9.
15. Volgin DV, Kubin L. Regionally selective effects of GABA on hypothalamic GABA A receptor mRNA in vitro. Biochem Biophys Res Commun 2007; 353:726-732.
16. Chubykin AA, Atasoy D, Etherton MR, Brose N, Kavalali ET, Gibson JR, et al. Activity-dependent validation of excitatory versus inhibitory synapses by neuroligin-1 versus neuroligin-2. Neuron 2007; 54:919-931.
17. Lambert JJ, Belelli D, Peden DR, Vardy AW, Peters JA. Neurosteroid modulation of GABA A receptors. Prog Neurobiol 2003; 71:67-80.
18. Nuss P. Anxiety disorders and GABA neurotransmission: a disturbance of modulation. Neuropsychiatr Dis Treat 2015; 11: 165–175.
19. Kostin A, McGinty D, Szymusiak R, Alam M. Sleep-wake and diurnal modulation of nitric oxide in the perifornical-lateral hypothalamic area: Real-time detection in freely behaving rats. Neuroscience 2013; 254:275-284.
20. Gopalakrishnan A, Li Ji L, Cirelli C. Sleep deprivation and cellular responses to oxidative stress. Sleep 2004; 27:27-35.
21. Periasamy S, Hsu D-Z, Fu Y-H, Liu M-Y. Sleep deprivation-induced multi-organ injury: role of oxidative stress and inflammation. EXCLI J 2015; 14:672.
22. Yu D, Li M, Tian Y, Liu J, Shang J. Luteolin inhibits ROS-activated MAPK pathway in myocardial ischemia/reperfusion injury. Life Sci 2015; 122:15-25.
23. Obame FN, Zini R, Souktani R, Berdeaux A, Morin D. Peripheral benzodiazepine receptor-induced myocardial protection is mediated by inhibition of mitochondrial membrane permeabilization. J Pharmacol Exp Ther 2007; 323:336-345.
24. Del Cid-Pellitero E, Plavski A, Mainville L, Jones BE. Homeostatic changes in GABA and glutamate receptors on excitatory cortical neurons during sleep deprivation and recovery. Front Syst Neurosci 2017; 11: 1-22.
25. Paxinos G, Watson C. The rat brain in stereotaxic coordinates. 6th ed. Academic Press; 2007.
26. Riahi E, Khodagholi F, Haghparast A. Role of dorsal hippocampal orexin-1 receptors in associating morphine reward with contextual stimuli. Behav Pharmacol 2013; 24:237-248.
27. Zagaar MA, Dao AT, Alhaider IA, Alkadhi KA. Prevention by regular exercise of acute sleep deprivation-induced impairment of late phase LTP and related signaling molecules in the dentate gyrus. Mol Neurobiol 2016; 53:2900-2910.
28. Aghajani M, Faghihi M, Imani A, Vaez Mahdavi MR, Shakoori A, Rastegar T, et al. Post-infarct sleep disruption and its relation to cardiac remodeling in a rat model of myocardial infarction. Chronobiol Int 2017; 34:587-600.
29. Arthaud S, Varin C, Gay N, Libourel PA, Chauveau F, Fort P, et al. Paradoxical (REM) sleep deprivation in mice using the small‐platforms‐over‐water method: polysomnographic analyses and melanin‐concentrating hormone and hypocretin/orexin neuronal activation before, during and after deprivation. J Sleep Res 2015; 24:309-319.
30. Azizi Y, Faghihi M, Imani A, Roghani M, Zekri A, Mobasheri MB, et al. Post-infarct treatment with [Pyr 1] apelin-13 improves myocardial function by increasing neovascularization and overexpression of angiogenic growth factors in rats. Eur J Pharmacol 2015; 761:101-108.
31. Imani A, Faghihi M, Sadr SS, Niaraki SS, Alizadeh AM. Noradrenaline protects in vivo rat heart against infarction and ventricular arrhythmias via nitric oxide and reactive oxygen species. J Surg Res 2011; 169:9-15.
32. Azizi Y, Faghihi M, Imani A, Roghani M, Nazari A. Post-infarct treatment with [Pyr1]-apelin-13 reduces myocardial damage through reduction of oxidative injury and nitric oxide enhancement in the rat model of myocardial infarction. Peptides 2013; 46:76-82.
33.K hamse S, Sadr SS, Roghani M, Hasanzadeh G, Mohammadian M. Rosmarinic acid exerts a neuroprotective effect in the kainate rat model of temporal lobe epilepsy: Underlying mechanisms. Pharm Biol 2015; 53:1818-1825.
34. Grandner MA, Sands-Lincoln MR, Pak VM, Garland SN.  Sleep duration, cardiovascular disease, and proinflammatory biomarkers. Nat Sci Sleep 2013; 5:93-107.
35. Li D-P, Pan H-L. Role of γ-aminobutyric acid (GABA) A and GABAB receptors in paraventricular nucleus in control of sympathetic vasomotor tone in hypertension. J Pharmacol Exp Ther 2007; 320:615-626.
36. Gomes da Silva AQ, Xavier CH, Campagnole-santos MJ, Caligiorne SM., Baltatu OC, Bader M,  et al. Cardiovascular responses evoked by activation or blockade of GABA A receptors in the hypothalamic PVN are attenuated in transgenic rats with low brain angiotensinogen. Brain Res 2012; 1448: 101-110.
37. Kim H-W, Pandit S, Park JB. Enhanced astroglial GABA uptake in heart failure. Channels 2015; 9:225-226.
38. Carillo B, Oliveira-Sales E, Andersen M, Tufik S, Hipolide D, Santos A, et al. Changes in GABAergic inputs in the paraventricular nucleus maintain sympathetic vasomotor tone in chronic heart failure. Auton Neurosci 2012; 171:41-48.
39. Klabunde R. Cardiovascular physiology concepts. 2th ed. Lippincott Williams & Wilkins; 2011.
40. Zhang K, Patel KP. Effect of nitric oxide within the paraventricular nucleus on renal sympathetic nerve discharge: role of GABA. Am J Physiol Regul Integr Comp Physiol 1998; 275:728-734.
41. Han TH, Lee K, Park JB, Ahn D, Park J-H, Kim D-Y, et al. Reduction in synaptic GABA release contributes to target-selective elevation of PVN neuronal activity in rats with myocardial infarction. Am J Physiol Regul Integr Comp Physiol 2010; 299: 129-139.
42. Jones SP, Bolli R. The ubiquitous role of nitric oxide in cardioprotection. J Mol Cell Cardiol 2006; 40:16-23.
43. Kurian GA, Rajagopal R, Vedantham S, Rajesh M. The role of oxidative stress in myocardial ischemia and reperfusion injury and remodeling: revisited. Oxid Med Cell Longev 2016; 2016:1-15.
44. Papaharalambus CA, Griendling KK. Basic mechanisms of oxidative stress and reactive oxygen species in cardiovascular injury. Trends Cardiovasc Med 2007; 17:48-54.
45. Mateos R, Lecumberri E, Ramos S, Goya L, Bravo L. Determination of malondialdehyde (MDA) by high-performance liquid chromatography in serum and liver as a biomarker for oxidative stress: Application to a rat model for hypercholesterolemia and evaluation of the effect of diets rich in phenolic antioxidants from fruits. J Chromatogr 2005; 827:76-82.
46. Pfister HP, King MG. Adaptation of the glucocorticosterone response to novelty. Physiol Behav 1976; 17:43-46.
47. Tobler I, Murison R, Ursin R, Ursin H, Borbely A. The effect of sleep deprivation and recovery sleep on plasma corticosterone in the rat. Neurosci Lett 1983; 35:297-300.
48. Parsa H, Faghihi M, Imani A. Acute Sleep Deprivation Decreases Anxiety Behavior via γ-Aminobutyric Acid-A Receptor Activation in Central Nucleus of Amygdala. JSS 2017; 1:139-142.
49. Keim SR, Shekhar A. The effects of GABA A receptor blockade in the dorsomedial hypothalamic nucleus on corticotrophin (ACTH) and corticosterone secretion in male rats. Brain Res 1996; 739:46-51.
50. Ulrich-Lai YM, Herman JP. Neural regulation of endocrine and autonomic stress responses. Nat Rev Neurosci 2009; 10:397-409.