Interactions between remote ischemic conditioning and post-stroke sleep regulation

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.

Keywords

remote ischemic conditioning / sleep regulation / stroke

参考文献

[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

[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

[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

[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

[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

[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

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

[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

[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

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

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

[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

[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

[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

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

[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

[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

[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

[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 neurodegenerative disorders. Antioxid Redox Signal 2010; 13(11): 1763–1811

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

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

[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

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

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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

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

[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

[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): e12589PMID:31155748

[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

[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

[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

[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

[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

[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

[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

[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

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

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

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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

[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

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

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

[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

[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

[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

[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

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

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

[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

[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

[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

[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

[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

[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

[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

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

[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

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

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

[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

[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

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

[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

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

[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

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

[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

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

[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): 86–92PMID:27773696

[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

[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

[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

[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

[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

[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

[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

[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

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).

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.

版权

2021 Higher Education Press