Skip to main content
Log in

Interactions between remote ischemic conditioning and post-stroke sleep regulation

  • Review
  • Published:
Frontiers of Medicine Aims and scope Submit manuscript

Abstract

Sleep disturbances are common in patients with stroke, and sleep quality has a critical role in the onset and outcome of stroke. Poor sleep exacerbates neurological injury, impedes nerve regeneration, and elicits serious complications. Thus, exploring a therapy suitable for patients with stroke and sleep disturbances is imperative. As a multi-targeted nonpharmacological intervention, remote ischemic conditioning can reduce the ischemic size of the brain, improve the functional outcome of stroke, and increase sleep duration. Preclinical/clinical evidence showed that this method can inhibit the inflammatory response, mediate the signal transductions of adenosine, activate the efferents of the vagal nerve, and reset the circadian clocks, all of which are involved in sleep regulation. In particular, cytokines tumor necrosis factor α (TNFα) and adenosine are sleep factors, and electrical vagal nerve stimulation can improve insomnia. On the basis of the common mechanisms of remote ischemic conditioning and sleep regulation, a causal relationship was proposed between remote ischemic conditioning and post-stroke sleep quality.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Wang W, Jiang B, Sun H, Ru X, Sun D, Wang L, Wang L, Jiang Y, Li Y, Wang Y, Chen Z, Wu S, Zhang Y, Wang D, Wang Y, Feigin VL; NESS-China Investigators. Prevalence, incidence, and mortality of stroke in China: results from a nationwide population-based survey of 480 687 adults. Circulation 2017; 135(8): 759–771

    Article  PubMed  Google Scholar 

  2. Dirnagl U, Endres M. Found in translation: preclinical stroke research predicts human pathophysiology, clinical phenotypes, and therapeutic outcomes. Stroke 2014; 45(5): 1510–1518

    Article  PubMed  Google Scholar 

  3. Baylan S, Griffiths S, Grant N, Broomfield NM, Evans JJ, Gardani M. Incidence and prevalence of post-stroke insomnia: a systematic review and meta-analysis. Sleep Med Rev 2020; 49: 101222

    Article  PubMed  Google Scholar 

  4. Morin CM, Edinger JD, Beaulieu-Bonneau S, Ivers H, Krystal AD, Guay B, Bélanger L, Cartwright A, Simmons B, Lamy M, Busby M. Effectiveness of sequential psychological and medication therapies for insomnia disorder: a randomized clinical trial. JAMA Psychiatry 2020; 77(11): 1107–1115

    Article  PubMed  Google Scholar 

  5. Morin CM, Vallières A, Guay B, Ivers H, Savard J, Mérette C, Bastien C, Baillargeon L. Cognitive behavioral therapy, singly and combined with medication, for persistent insomnia: a randomized controlled trial. JAMA 2009; 301(19): 2005–2015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Ibáñez B, Heusch G, Ovize M, Van de Werf F. Evolving therapies for myocardial ischemia/reperfusion injury. J Am Coll Cardiol 2015; 65(14): 1454–1471

    Article  PubMed  Google Scholar 

  7. Kleinbongard P, Skyschally A, Heusch G. Cardioprotection by remote ischemic conditioning and its signal transduction. Pflugers Arch 2017; 469(2): 159–181

    Article  CAS  PubMed  Google Scholar 

  8. Pace M, Camilo MR, Seiler A, Duss SB, Mathis J, Manconi M, Bassetti CL. Rapid eye movements sleep as a predictor of functional outcome after stroke: a translational study. Sleep (Basel) 2018; 41(10): zsy138

    Google Scholar 

  9. Terzoudi A, Vorvolakos T, Heliopoulos I, Livaditis M, Vadikolias K, Piperidou H. Sleep architecture in stroke and relation to outcome. Eur Neurol 2009; 61(1): 16–22

    Article  CAS  PubMed  Google Scholar 

  10. Bassetti CL, Aldrich MS. Sleep electroencephalogram changes in acute hemispheric stroke. Sleep Med 2001; 2(3): 185–194

    Article  PubMed  Google Scholar 

  11. Mims KN, Kirsch D. Sleep and stroke. Sleep Med Clin 2016; 11(1): 39–51

    Article  PubMed  Google Scholar 

  12. McAlpine CS, Kiss MG, Rattik S, He S, Vassalli A, Valet C, Anzai A, Chan CT, Mindur JE, Kahles F, Poller WC, Frodermann V, Fenn AM, Gregory AF, Halle L, Iwamoto Y, Hoyer FF, Binder CJ, Libby P, Tafti M, Scammell TE, Nahrendorf M, Swirski FK. Sleep modulates haematopoiesis and protects against atherosclerosis. Nature 2019; 566(7744): 383–387

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Gao B, Cam E, Jaeger H, Zunzunegui C, Sarnthein J, Bassetti CL. Sleep disruption aggravates focal cerebral ischemia in the rat. Sleep 2010; 33(7): 879–887

    Article  PubMed  PubMed Central  Google Scholar 

  14. Zunzunegui C, Gao B, Cam E, Hodor A, Bassetti CL. Sleep disturbance impairs stroke recovery in the rat. Sleep (Basel) 2011; 34(9): 1261–1269

    Article  Google Scholar 

  15. Hermann DM, Bassetti CL. Sleep-related breathing and sleep-wake disturbances in ischemic stroke. Neurology 2009; 73(16): 1313–1322

    Article  PubMed  Google Scholar 

  16. Nguyen S, Wong D, McKay A, Rajaratnam SMW, Spitz G, Williams G, Mansfield D, Ponsford JL. Cognitive behavioural therapy for post-stroke fatigue and sleep disturbance: a pilot randomised controlled trial with blind assessment. Neuropsychol Rehabil 2019; 29(5): 723–738

    Article  PubMed  Google Scholar 

  17. Hodor A, Palchykova S, Baracchi F, Noain D, Bassetti CL. Baclofen facilitates sleep, neuroplasticity, and recovery after stroke in rats. Ann Clin Transl Neurol 2014; 1(10): 765–777

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Dirnagl U, Becker K, Meisel A. Preconditioning and tolerance against cerebral ischaemia: from experimental strategies to clinical use. Lancet Neurol 2009; 8(4): 398–412

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Calabrese V, Cornelius C, Dinkova-Kostova AT, Calabrese EJ, Mattson MP. Cellular stress responses, the hormesis paradigm, and vitagenes: novel targets for therapeutic intervention in neurode-generative disorders. Antioxid Redox Signal 2010; 13(11): 1763–1811

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Stebbing AR. Hormesis—the stimulation of growth by low levels of inhibitors. Sci Total Environ 1982; 22(3): 213–234

    Article  CAS  PubMed  Google Scholar 

  21. Heusch G. Myocardial ischaemia-reperfusion injury and cardioprotection in perspective. Nat Rev Cardiol 2020; 17(12): 773–789

    Article  PubMed  Google Scholar 

  22. Calabrese V, Renis M, Calderone A, Russo A, Barcellona ML, Rizza V. Stress proteins and SH-groups in oxidant-induced cell damage after acute ethanol administration in rat. Free Radic Biol Med 1996; 20(3): 391–397

    Article  CAS  PubMed  Google Scholar 

  23. Siracusa R, Scuto M, Fusco R, Trovato A, Ontario ML, Crea R, Di Paola R, Cuzzocrea S, Calabrese V. Anti-inflammatory and antioxidant activity of Hidrox® in rotenone-induced Parkinson’s disease in mice. Antioxidants 2020; 9(9): 824

    Article  CAS  PubMed Central  Google Scholar 

  24. Dirnagl U, Meisel A. Endogenous neuroprotection: mitochondria as gateways to cerebral preconditioning?. Neuropharmacology 2008; 55(3): 334–344

    Article  CAS  PubMed  Google Scholar 

  25. Hausenloy DJ, Barrabes JA, Bøtker HE, Davidson SM, Di Lisa F, Downey J, Engstrom T, Ferdinandy P, Carbrera-Fuentes HA, Heusch G, Ibanez B, Iliodromitis EK, Inserte J, Jennings R, Kalia N, Kharbanda R, Lecour S, Marber M, Miura T, Ovize M, Perez-Pinzon MA, Piper HM, Przyklenk K, Schmidt MR, Redington A, Ruiz-Meana M, Vilahur G, Vinten-Johansen J, Yellon DM, Garcia-Dorado D. Ischaemic conditioning and targeting reperfusion injury: a 30 year voyage of discovery. Basic Res Cardiol 2016; 111(6): 70

    Article  PubMed  PubMed Central  Google Scholar 

  26. Cheng X, Zhao H, Yan F, Tao Z, Wang R, Han Z, Li G, Luo Y, Ji X. Limb remote ischemic post-conditioning mitigates brain recovery in a mouse model of ischemic stroke by regulating reactive astrocytic plasticity. Brain Res 2018; 1686: 94–100

    Article  CAS  PubMed  Google Scholar 

  27. Ren C, Li N, Li S, Han R, Huang Q, Hu J, Jin K, Ji X. Limb ischemic conditioning improved cognitive deficits via eNOS-dependent augmentation of angiogenesis after chronic cerebral hypoperfusion in rats. Aging Dis 2018; 9(5): 869–879

    Article  PubMed  PubMed Central  Google Scholar 

  28. Zhao W, Meng R, Ma C, Hou B, Jiao L, Zhu F, Wu W, Shi J, Duan Y, Zhang R, Zhang J, Sun Y, Zhang H, Ling F, Wang Y, Feng W, Ding Y, Ovbiagele B, Ji X. Safety and efficacy of remote ischemic preconditioning in patients with severe carotid artery stenosis before carotid artery stenting: a proof-of-concept, randomized controlled trial. Circulation 2017; 135(14): 1325–1335

    Article  PubMed  PubMed Central  Google Scholar 

  29. Meng R, Asmaro K, Meng L, Liu Y, Ma C, Xi C, Li G, Ren C, Luo Y, Ling F, Jia J, Hua Y, Wang X, Ding Y, Lo EH, Ji X. Upper limb ischemic preconditioning prevents recurrent stroke in intracranial arterial stenosis. Neurology 2012; 79(18): 1853–1861

    Article  PubMed  Google Scholar 

  30. Zhao W, Jiang F, Zhang Z, Zhang J, Ding Y, Ji X. Remote ischemic conditioning: a novel non-invasive approach to prevent post-stroke depression. Front Aging Neurosci 2017; 9: 270

    Article  PubMed  PubMed Central  Google Scholar 

  31. Liu ZJ, Chen C, Li XR, Ran YY, Xu T, Zhang Y, Geng XK, Zhang Y, Du HS, Leak RK, Ji XM, Hu XM. Remote ischemic preconditioning-mediated neuroprotection against stroke is associated with significant alterations in peripheral immune responses. CNS Neurosci Ther 2016; 22(1): 43–52

    Article  CAS  PubMed  Google Scholar 

  32. Brager AJ, Yang T, Ehlen JC, Simon RP, Meller R, Paul KN. Sleep is critical for remote preconditioning-induced neuroprotection. Sleep (Basel) 2016; 39(11): 2033–2040

    Article  Google Scholar 

  33. Macleod MR, O’Collins T, Horky LL, Howells DW, Donnan GA. Systematic review and meta-analysis of the efficacy of melatonin in experimental stroke. J Pineal Res 2005; 38(1): 35–41

    Article  CAS  PubMed  Google Scholar 

  34. Chang YS, Lin MH, Lee JH, Lee PL, Dai YS, Chu KH, Sun C, Lin YT, Wang LC, Yu HH, Yang YH, Chen CA, Wan KS, Chiang BL. Melatonin supplementation for children with atopic dermatitis and sleep disturbance: a randomized clinical trial. JAMA Pediatr 2016; 170(1): 35–42

    Article  PubMed  Google Scholar 

  35. Reiter RJ, Sainz RM, Lopez-Burillo S, Mayo JC, Manchester LC, Tan DX. Melatonin ameliorates neurologic damage and neuro-physiologic deficits in experimental models of stroke. Ann N Y Acad Sci 2003; 993(1): 35–53

    Article  CAS  PubMed  Google Scholar 

  36. Feng D, Wang B, Wang L, Abraham N, Tao K, Huang L, Shi W, Dong Y, Qu Y. Pre-ischemia melatonin treatment alleviated acute neuronal injury after ischemic stroke by inhibiting endoplasmic reticulum stress-dependent autophagy via PERK and IRE1 signalings. J Pineal Res 2017; 62(3): e12395

    Article  Google Scholar 

  37. Gul-Kahraman K, Yilmaz-Bozoglan M, Sahna E. Physiological and pharmacological effects of melatonin on remote ischemic perconditioning after myocardial ischemia-reperfusion injury in rats: role of Cybb, Fas, NfκB, Irisin signaling pathway. J Pineal Res 2019; 67(2): e12589

    Article  PubMed  Google Scholar 

  38. Hausenloy DJ, Garcia-Dorado D, Erik Bøtker H, Davidson SM, Downey J, Engel FB, Jennings R, Lecour S, Leor J, Madonna R, Ovize M, Perrino C, Prunier F, Schulz R, Sluijter JPG, Van Laake LW, Vinten-Johansen J, Yellon DM, Ytrehus K, Heusch G, Ferdinandy P. Melatonin as a cardioprotective therapy following ST-segment elevation myocardial infarction: is it really promising? Reply. Cardiovasc Res 2017; 113(11): 1418–1419

    Article  PubMed  Google Scholar 

  39. Karikó K, Weissman D, Welsh FA. Inhibition of Toll-like receptor and cytokine signaling—a unifying theme in ischemic tolerance. J Cereb Blood Flow Metab 2004; 24(11): 1288–1304

    Article  PubMed  Google Scholar 

  40. Pace M, Baracchi F, Gao B, Bassetti C. Identification of sleep-modulated pathways involved in neuroprotection from stroke. Sleep (Basel) 2015; 38(11): 1707–1718

    Article  Google Scholar 

  41. Konstantinov IE, Arab S, Kharbanda RK, Li J, Cheung MM, Cherepanov V, Downey GP, Liu PP, Cukerman E, Coles JG, Redington AN. The remote ischemic preconditioning stimulus modifies inflammatory gene expression in humans. Physiol Genomics 2004; 19(1): 143–150

    Article  CAS  PubMed  Google Scholar 

  42. Hsu JC, Lee YS, Chang CN, Ling EA, Lan CT. Sleep deprivation prior to transient global cerebral ischemia attenuates glial reaction in the rat hippocampal formation. Brain Res 2003; 984(1–2): 170–181

    Article  CAS  PubMed  Google Scholar 

  43. Moldovan M, Constantinescu AO, Balseanu A, Oprescu N, Zagrean L, Popa-Wagner A. Sleep deprivation attenuates experimental stroke severity in rats. Exp Neurol 2010; 222(1): 135–143

    Article  PubMed  Google Scholar 

  44. Cam E, Gao B, Imbach L, Hodor A, Bassetti CL. Sleep deprivation before stroke is neuroprotective: a pre-ischemic conditioning related to sleep rebound. Exp Neurol 2013; 247: 673–679

    Article  CAS  PubMed  Google Scholar 

  45. Morin CM, Drake CL, Harvey AG, Krystal AD, Manber R, Riemann D, Spiegelhalder K. Insomnia disorder. Nat Rev Dis Primers 2015; 1(1): 15026

    Article  PubMed  Google Scholar 

  46. Porkka-Heiskanen T, Kalinchuk AV. Adenosine, energy metabolism and sleep homeostasis. Sleep Med Rev 2011; 15(2): 123–135

    Article  PubMed  Google Scholar 

  47. McAlpine CS, Swirski FK. Circadian influence on metabolism and inflammation in atherosclerosis. Circ Res 2016; 119(1): 131–141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Imeri L, Opp MR. How (and why) the immune system makes us sleep. Nat Rev Neurosci 2009; 10(3): 199–210

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Granger JI, Ratti PL, Datta SC, Raymond RM, Opp MR. Sepsis-induced morbidity in mice: effects on body temperature, body weight, cage activity, social behavior and cytokines in brain. Psychoneuroendocrinology 2013; 38(7): 1047–1057

    Article  CAS  PubMed  Google Scholar 

  50. Castillo J, Moro MA, Blanco M, Leira R, Serena J, Lizasoain I, Dávalos A. The release of tumor necrosis factor-α is associated with ischemic tolerance in human stroke. Ann Neurol 2003; 54(6): 811–819

    Article  CAS  PubMed  Google Scholar 

  51. Gedik N, Kottenberg E, Thielmann M, Frey UH, Jakob H, Peters J, Heusch G, Kleinbongard P. Potential humoral mediators of remote ischemic preconditioning in patients undergoing surgical coronary revascularization. Sci Rep 2017; 7(1): 12660

    Article  PubMed  PubMed Central  Google Scholar 

  52. Meng XL, Zhang DL, Sui SH. Acute remote ischemic preconditioning alleviates free radical injury and inflammatory response in cerebral ischemia/reperfusion rats. Exp Ther Med 2019; 18(3): 1953–1960

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Offner H, Subramanian S, Parker SM, Afentoulis ME, Vandenbark AA, Hurn PD. Experimental stroke induces massive, rapid activation of the peripheral immune system. J Cereb Blood Flow Metab 2006; 26(5): 654–665

    Article  CAS  PubMed  Google Scholar 

  54. Chapman KZ, Dale VQ, Dénes A, Bennett G, Rothwell NJ, Allan SM, McColl BW. A rapid and transient peripheral inflammatory response precedes brain inflammation after experimental stroke. J Cereb Blood Flow Metab 2009; 29(11): 1764–1768

    Article  PubMed  Google Scholar 

  55. Cai ZP, Parajuli N, Zheng X, Becker L. Remote ischemic preconditioning confers late protection against myocardial ischemia-reperfusion injury in mice by upregulating interleukin-10. Basic Res Cardiol 2012; 107(4): 277

    Article  PubMed  PubMed Central  Google Scholar 

  56. Heusch G. Adenosine and maximum coronary vasodilation in humans: myth and misconceptions in the assessment of coronary reserve. Basic Res Cardiol 2010; 105(1): 1–5

    Article  PubMed  Google Scholar 

  57. Huang ZL, Urade Y, Hayaishi O. The role of adenosine in the regulation of sleep. Curr Top Med Chem 2011; 11(8): 1047–1057

    Article  CAS  PubMed  Google Scholar 

  58. Grover GJ, Sleph PG, Dzwonczyk S. Role of myocardial ATP-sensitive potassium channels in mediating preconditioning in the dog heart and their possible interaction with adenosine A1-receptors. Circulation 1992; 86(4): 1310–1316

    Article  CAS  PubMed  Google Scholar 

  59. Leesar MA, Stoddard MF, Xuan YT, Tang XL, Bolli R. Nonelectrocardiographic evidence that both ischemic preconditioning and adenosine preconditioning exist in humans. J Am Coll Cardiol 2003; 42(3): 437–445

    Article  CAS  PubMed  Google Scholar 

  60. Schulz R, Rose J, Post H, Heusch G. Involvement of endogenous adenosine in ischaemic preconditioning in swine. Pflugers Arch 1995; 430(2): 273–282

    Article  CAS  PubMed  Google Scholar 

  61. Kitakaze M, Hori M, Takashima S, Sato H, Inoue M, Kamada T. Ischemic preconditioning increases adenosine release and 5′-nucleotidase activity during myocardial ischemia and reperfusion in dogs. Implications for myocardial salvage. Circulation 1993; 87(1): 208–215

    Article  CAS  PubMed  Google Scholar 

  62. Elmenhorst D, Elmenhorst EM, Hennecke E, Kroll T, Matusch A, Aeschbach D, Bauer A. Recovery sleep after extended wakefulness restores elevated A1 adenosine receptor availability in the human brain. Proc Natl Acad Sci USA 2017; 114(16): 4243–4248

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Bjorness TE, Kelly CL, Gao T, Poffenberger V, Greene RW. Control and function of the homeostatic sleep response by adenosine A1 receptors. J Neurosci 2009; 29(5): 1267–1276

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Hu S, Dong H, Zhang H, Wang S, Hou L, Chen S, Zhang J, Xiong L. Noninvasive limb remote ischemic preconditioning contributes neuroprotective effects via activation of adenosine A1 receptor and redox status after transient focal cerebral ischemia in rats. Brain Res 2012; 1459: 81–90

    Article  CAS  PubMed  Google Scholar 

  65. Gross GJ, Auchampach JA. Blockade of ATP-sensitive potassium channels prevents myocardial preconditioning in dogs. Circ Res 1992; 70(2): 223–233

    Article  CAS  PubMed  Google Scholar 

  66. Auchampach JA, Gross GJ. Adenosine A1 receptors, KATP channels, and ischemic preconditioning in dogs. Am J Physiol 1993; 264(5): H1327–H1336

    CAS  PubMed  Google Scholar 

  67. Lieder HR, Kleinbongard P, Skyschally A, Hagelschuer H, Chilian WM, Heusch G. Vago-splenic axis in signal transduction of remote ischemic preconditioning in pigs and rats. Circ Res 2018; 123(10): 1152–1163

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Irwin M, Thompson J, Miller C, Gillin JC, Ziegler M. Effects of sleep and sleep deprivation on catecholamine and interleukin-2 levels in humans: clinical implications. J Clin Endocrinol Metab 1999; 84(6): 1979–1985

    CAS  PubMed  Google Scholar 

  69. Vgontzas AN, Fernandez-Mendoza J, Liao D, Bixler EO. Insomnia with objective short sleep duration: the most biologically severe phenotype of the disorder. Sleep Med Rev 2013; 17(4): 241–254

    Article  PubMed  PubMed Central  Google Scholar 

  70. Vgontzas AN, Bixler EO, Papanicolaou DA, Kales A, Stratakis CA, Vela-Bueno A, Gold PW, Chrousos GP. Rapid eye movement sleep correlates with the overall activities of the hypothalamic-pituitary-adrenal axis and sympathetic system in healthy humans. J Clin Endocrinol Metab 1997; 82(10): 3278–3280

    Article  CAS  PubMed  Google Scholar 

  71. Seravalle G, Mancia G, Grassi G. Sympathetic nervous system, sleep, and hypertension. Curr Hypertens Rep 2018; 20(9): 74

    Article  PubMed  Google Scholar 

  72. Dorrance AM, Fink G. Effects of stroke on the autonomic nervous system. Compr Physiol 2015; 5(3): 1241–1263

    Article  PubMed  Google Scholar 

  73. Dutta P, Courties G, Wei Y, Leuschner F, Gorbatov R, Robbins CS, Iwamoto Y, Thompson B, Carlson AL, Heidt T, Majmudar MD, Lasitschka F, Etzrodt M, Waterman P, Waring MT, Chicoine AT, van der Laan AM, Niessen HW, Piek JJ, Rubin BB, Butany J, Stone JR, Katus HA, Murphy SA, Morrow DA, Sabatine MS, Vinegoni C, Moskowitz MA, Pittet MJ, Libby P, Lin CP, Swirski FK, Weissleder R, Nahrendorf M. Myocardial infarction accelerates atherosclerosis. Nature 2012; 487(7407): 325–329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Lambert EA, Thomas CJ, Hemmes R, Eikelis N, Pathak A, Schlaich MP, Lambert GW. Sympathetic nervous response to ischemia-reperfusion injury in humans is altered with remote ischemic preconditioning. Am J Physiol Heart Circ Physiol 2016; 311(2): H364–H370

    Article  PubMed  Google Scholar 

  75. Miura T, Kawamura S, Tatsuno H, Ikeda Y, Mikami S, Iwamoto H, Okamura T, Iwatate M, Kimura M, Dairaku Y, Maekawa T, Matsuzaki M. Ischemic preconditioning attenuates cardiac sympathetic nerve injury via ATP-sensitive potassium channels during myocardial ischemia. Circulation 2001; 104(9): 1053–1058

    Article  CAS  PubMed  Google Scholar 

  76. Tsutsui H, Tanaka R, Yamagata M, Yukimura T, Ohkita M, Matsumura Y. Protective effect of ischemic preconditioning on ischemia/reperfusion-induced acute kidney injury through sympathetic nervous system in rats. Eur J Pharmacol 2013; 718(1–3): 206–212

    Article  CAS  PubMed  Google Scholar 

  77. Irwin MR, Valladares EM, Motivala S, Thayer JF, Ehlers CL. Association between nocturnal vagal tone and sleep depth, sleep quality, and fatigue in alcohol dependence. Psychosom Med 2006; 68(1): 159–166

    Article  PubMed  Google Scholar 

  78. Zhao B, Li L, Jiao Y, Luo M, Xu K, Hong Y, Cao JD, Zhang Y, Fang JL, Rong PJ. Transcutaneous auricular vagus nerve stimulation in treating post-stroke insomnia monitored by resting-state fMRI: the first case report. Brain Stimul 2019; 12(3): 824–826

    Article  PubMed  Google Scholar 

  79. Buchholz B, Kelly J, Muñoz M, Bernatené EA, Méndez Diodati N, González Maglio DH, Dominici FP, Gelpi RJ. Vagal stimulation mimics preconditioning and postconditioning of ischemic myocardium in mice by activating different protection mechanisms. Am J Physiol Heart Circ Physiol 2018; 314(6): H1289–H1297

    Article  CAS  PubMed  Google Scholar 

  80. Heusch G. Vagal cardioprotection in reperfused acute myocardial infarction. JACC Cardiovasc Interv 2017; 10(15): 1521–1522

    Article  PubMed  Google Scholar 

  81. Basalay MV, Mastitskaya S, Mrochek A, Ackland GL, Del Arroyo AG, Sanchez J, Sjoquist PO, Pernow J, Gourine AV, Gourine A. Glucagon-like peptide-1 (GLP-1) mediates cardioprotection by remote ischaemic conditioning. Cardiovasc Res 2016; 112(3): 669–676

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Challet E. The circadian regulation of food intake. Nat Rev Endocrinol 2019; 15(7): 393–405

    Article  PubMed  Google Scholar 

  83. Reinke H, Asher G. Crosstalk between metabolism and circadian clocks. Nat Rev Mol Cell Biol 2019; 20(4): 227–241

    Article  CAS  PubMed  Google Scholar 

  84. Ehlen JC, Brager AJ, Baggs J, Pinckney L, Gray CL, DeBruyne JP, Esser KA, Takahashi JS, Paul KN. Bmal1 function in skeletal muscle regulates sleep. eLife 2017; 6: e26557

    Article  PubMed  PubMed Central  Google Scholar 

  85. van den Buuse M. Circadian rhythms of blood pressure and heart rate in conscious rats: effects of light cycle shift and timed feeding. Physiol Behav 1999; 68(1–2): 9–15

    Article  CAS  PubMed  Google Scholar 

  86. Durgan DJ, Young ME. The cardiomyocyte circadian clock: emerging roles in health and disease. Circ Res 2010; 106(4): 647–658

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Depner CM, Melanson EL, McHill AW, Wright KP Jr. Mistimed food intake and sleep alters 24-hour time-of-day patterns of the human plasma proteome. Proc Natl Acad Sci USA 2018; 115(23): E5390–E5399

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Wolff G, Esser KA. Scheduled exercise phase shifts the circadian clock in skeletal muscle. Med Sci Sports Exerc 2012; 44(9): 1663–1670

    Article  PubMed  PubMed Central  Google Scholar 

  89. Cai Z, Zhong H, Bosch-Marce M, Fox-Talbot K, Wang L, Wei C, Trush MA, Semenza GL. Complete loss of ischaemic preconditioning-induced cardioprotection in mice with partial deficiency of HIF-1α Cardiovasc Res 2008; 77(3): 463–470

    Article  CAS  PubMed  Google Scholar 

  90. Semenza GL. Hypoxia-inducible factor 1: oxygen homeostasis and disease pathophysiology. Trends Mol Med 2001; 7(8): 345–350

    Article  CAS  PubMed  Google Scholar 

  91. Kalakech H, Tamareille S, Pons S, Godin-Ribuot D, Carmeliet P, Furber A, Martin V, Berdeaux A, Ghaleh B, Prunier F. Role of hypoxia inducible factor-1α in remote limb ischemic preconditioning. J Mol Cell Cardiol 2013; 65: 98–104

    Article  CAS  PubMed  Google Scholar 

  92. Heusch G. HIF-1 and paradoxical phenomena in cardioprotection: expert’s perspective. Cardiovasc Res 2012; 96(2): 214–215

    Article  CAS  PubMed  Google Scholar 

  93. Peek CB, Levine DC, Cedernaes J, Taguchi A, Kobayashi Y, Tsai SJ, Bonar NA, McNulty MR, Ramsey KM, Bass J. Circadian clock interaction with HIF1α mediates oxygenic metabolism and anaerobic glycolysis in skeletal muscle. Cell Metab 2017; 25(1): 86–92

    Article  CAS  PubMed  Google Scholar 

  94. Wu Y, Tang D, Liu N, Xiong W, Huang H, Li Y, Ma Z, Zhao H, Chen P, Qi X, Zhang EE. Reciprocal regulation between the circadian clock and hypoxia signaling at the genome level in mammals. Cell Metab 2017; 25(1): 73–85

    Article  CAS  PubMed  Google Scholar 

  95. Adamovich Y, Ladeuix B, Golik M, Koeners MP, Asher G. Rhythmic oxygen levels reset circadian clocks through HIF1α. Cell Metab 2017; 25(1): 93–101

    Article  CAS  PubMed  Google Scholar 

  96. Basalay MV, Davidson SM, Gourine AV, Yellon DM. Neural mechanisms in remote ischaemic conditioning in the heart and brain: mechanistic and translational aspects. Basic Res Cardiol 2018; 113(4): 25

    Article  PubMed  PubMed Central  Google Scholar 

  97. Schibler U, Gotic I, Saini C, Gos P, Curie T, Emmenegger Y, Sinturel F, Gosselin P, Gerber A, Fleury-Olela F, Rando G, Demarque M, Franken P. Clock-talk: interactions between central and peripheral circadian oscillators in mammals. Cold Spring Harb Symp Quant Biol 2015; 80: 223–232

    Article  PubMed  Google Scholar 

  98. Kung TA, Egbejimi O, Cui J, Ha NP, Durgan DJ, Essop MF, Bray MS, Shaw CA, Hardin PE, Stanley WC, Young ME. Rapid attenuation of circadian clock gene oscillations in the rat heart following ischemia-reperfusion. J Mol Cell Cardiol 2007; 43(6): 744–753

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Beker MC, Caglayan B, Yalcin E, Caglayan AB, Turkseven S, Gurel B, Kelestemur T, Sertel E, Sahin Z, Kutlu S, Kilic U, Baykal AT, Kilic E. Time-of-day dependent neuronal injury after ischemic stroke: implication of circadian clock transcriptional factor Bmal1 and survival kinase AKT. Mol Neurobiol 2018; 55(3): 2565–2576

    Article  CAS  PubMed  Google Scholar 

  100. Liu ZJ, Chen C, Li XR, Ran YY, Xu T, Zhang Y, Geng XK, Zhang Y, Du HS, Leak RK, Ji XM, Hu XM. Remote ischemic preconditioning-mediated neuroprotection against stroke is associated with significant alterations in peripheral immune responses. CNS Neurosci Ther 2016; 22(1): 43–52

    Article  CAS  PubMed  Google Scholar 

  101. Zhang Y, Ma L, Ren C, Liu K, Tian X, Wu D, Ding Y, Li J, Borlongan CV, Ji X. Immediate remote ischemic postconditioning reduces cerebral damage in ischemic stroke mice by enhancing leptomeningeal collateral circulation. J Cell Physiol 2019; 234(8): 12637–12645

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Key R&D Program of China (No. 2017YFC1308401) and the Talent Introduction Project of the Beijing Bureau of Foreign Expert (No. BJ2018001).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Xunming Ji.

Additional information

Compliance with ethics guidelines

Xian Wang and Xunming Ji declare that they have no conflict of interest. This manuscript is a review article and does not involve a research protocol requiring approval by the relevant institutional review board or ethics committee.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, X., Ji, X. Interactions between remote ischemic conditioning and post-stroke sleep regulation. Front. Med. 15, 867–876 (2021). https://doi.org/10.1007/s11684-021-0887-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11684-021-0887-9

Keywords

Navigation