Please wait a minute...
Frontiers of Medicine

ISSN 2095-0217

ISSN 2095-0225(Online)

CN 11-5983/R

Postal Subscription Code 80-967

2018 Impact Factor: 1.847

Front. Med.    2021, Vol. 15 Issue (6) : 867-876    https://doi.org/10.1007/s11684-021-0887-9
REVIEW
Interactions between remote ischemic conditioning and post-stroke sleep regulation
Xian Wang1, Xunming Ji1,2()
1. Beijing Institute of Brain Disorders, Laboratory of Brain Disorders, Ministry of Science and Technology, Collaborative Innovation Center for Brain Disorders, Capital Medical University, Beijing 100069, China
2. Beijing Key Laboratory of Hypoxia Conditioning Translational Medicine, Beijing 100069, China
 Download: PDF(448 KB)   HTML
 Export: BibTeX | EndNote | Reference Manager | ProCite | RefWorks
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     
Corresponding Author(s): Xunming Ji   
Just Accepted Date: 29 October 2021   Online First Date: 19 November 2021    Issue Date: 27 December 2021
 Cite this article:   
Xian Wang,Xunming Ji. Interactions between remote ischemic conditioning and post-stroke sleep regulation[J]. Front. Med., 2021, 15(6): 867-876.
 URL:  
https://academic.hep.com.cn/fmd/EN/10.1007/s11684-021-0887-9
https://academic.hep.com.cn/fmd/EN/Y2021/V15/I6/867
Fig.1  Evidence that links stroke, remote ischemic conditioning (RIC) and sleep. Stroke and sleep disturbances have mutually adverse effects. Stress, brain edema, severity, comorbidities, and lesion location that are resulted from stroke induce sleep disturbances, while poor sleep facilitates atherogenesis, endothelial dysfunction, extended edema, and infarct region. RIC and good sleep have similarly neuroprotective effects, such as reducing ischemia/reperfusion (I/R) injury, increasing neurogenesis, axonal sprouting, and cerebral perfusion. Furthermore, RIC involves in sleep regulation, by impacting melatonin, sleep homeostasis, and circadian system, as well as by the shared mechanisms of sleep deprivation (SD) preconditioning.
Fig.2  Putative pathways linking remote ischemic conditioning to sleep regulation (sleep homeostasis and circadian system). RIC increases sleep propensity by the pre-activating immune system, mimicking/strengthening the effects of the adenosine system and vagal activity. It reduces sleep fragmentation by inhibiting the hyperactivation of inflammatory response and sympathetic activity. In addition, RIC plays a regulatory role in the circadian system, through increasing HIF1α, balancing neural activities, and decreasing ischemia/reperfusion (I/R) injury.
1 W Wang, B Jiang, H Sun, X Ru, D Sun, L Wang, L Wang, Y Jiang, Y Li, Y Wang, Z Chen, S Wu, Y Zhang, D Wang, Y Wang, VL; NESS-China Investigators Feigin. 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
https://doi.org/10.1161/CIRCULATIONAHA.116.025250 pmid: 28052979
2 U Dirnagl, M Endres. Found in translation: preclinical stroke research predicts human pathophysiology, clinical phenotypes, and therapeutic outcomes. Stroke 2014; 45(5): 1510–1518
https://doi.org/10.1161/STROKEAHA.113.004075 pmid: 24652307
3 S Baylan, S Griffiths, N Grant, NM Broomfield, JJ Evans, M Gardani. Incidence and prevalence of post-stroke insomnia: a systematic review and meta-analysis. Sleep Med Rev 2020; 49: 101222
https://doi.org/10.1016/j.smrv.2019.101222 pmid: 31739180
4 CM Morin, JD Edinger, S Beaulieu-Bonneau, H Ivers, AD Krystal, B Guay, L Bélanger, A Cartwright, B Simmons, M Lamy, M Busby. Effectiveness of sequential psychological and medication therapies for insomnia disorder: a randomized clinical trial. JAMA Psychiatry 2020; 77(11): 1107–1115
https://doi.org/10.1001/jamapsychiatry.2020.1767 pmid: 32639561
5 CM Morin, A Vallières, B Guay, H Ivers, J Savard, C Mérette, C Bastien, L Baillargeon. Cognitive behavioral therapy, singly and combined with medication, for persistent insomnia: a randomized controlled trial. JAMA 2009; 301(19): 2005–2015
https://doi.org/10.1001/jama.2009.682 pmid: 19454639
6 B Ibáñez, G Heusch, M Ovize, F Van de Werf. Evolving therapies for myocardial ischemia/reperfusion injury. J Am Coll Cardiol 2015; 65(14): 1454–1471
https://doi.org/10.1016/j.jacc.2015.02.032 pmid: 25857912
7 P Kleinbongard, A Skyschally, G Heusch. Cardioprotection by remote ischemic conditioning and its signal transduction. Pflugers Arch 2017; 469(2): 159–181
https://doi.org/10.1007/s00424-016-1922-6 pmid: 27928644
8 M Pace, MR Camilo, A Seiler, SB Duss, J Mathis, M Manconi, CL Bassetti. Rapid eye movements sleep as a predictor of functional outcome after stroke: a translational study. Sleep (Basel) 2018; 41(10): zsy138
https://doi.org/10.1093/sleep/zsy138 pmid: 30032306
9 A Terzoudi, T Vorvolakos, I Heliopoulos, M Livaditis, K Vadikolias, H Piperidou. Sleep architecture in stroke and relation to outcome. Eur Neurol 2009; 61(1): 16–22
https://doi.org/10.1159/000165344 pmid: 18948695
10 CL Bassetti, MS Aldrich. Sleep electroencephalogram changes in acute hemispheric stroke. Sleep Med 2001; 2(3): 185–194
https://doi.org/10.1016/S1389-9457(00)00071-X pmid: 11311681
11 KN Mims, D Kirsch. Sleep and stroke. Sleep Med Clin 2016; 11(1): 39–51
https://doi.org/10.1016/j.jsmc.2015.10.009 pmid: 26972032
12 CS McAlpine, MG Kiss, S Rattik, S He, A Vassalli, C Valet, A Anzai, CT Chan, JE Mindur, F Kahles, WC Poller, V Frodermann, AM Fenn, AF Gregory, L Halle, Y Iwamoto, FF Hoyer, CJ Binder, P Libby, M Tafti, TE Scammell, M Nahrendorf, FK Swirski. Sleep modulates haematopoiesis and protects against atherosclerosis. Nature 2019; 566(7744): 383–387
https://doi.org/10.1038/s41586-019-0948-2 pmid: 30760925
13 B Gao, E Cam, H Jaeger, C Zunzunegui, J Sarnthein, CL Bassetti. Sleep disruption aggravates focal cerebral ischemia in the rat. Sleep 2010; 33(7): 879–887
https://doi.org/10.1093/sleep/33.7.879 pmid: 20614848
14 C Zunzunegui, B Gao, E Cam, A Hodor, CL Bassetti. Sleep disturbance impairs stroke recovery in the rat. Sleep (Basel) 2011; 34(9): 1261–1269
https://doi.org/10.5665/SLEEP.1252 pmid: 21886364
15 DM Hermann, CL Bassetti. Sleep-related breathing and sleep–wake disturbances in ischemic stroke. Neurology 2009; 73(16): 1313–1322
https://doi.org/10.1212/WNL.0b013e3181bd137c pmid: 19841384
16 S Nguyen, D Wong, A McKay, SMW Rajaratnam, G Spitz, G Williams, D Mansfield, JL Ponsford. 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
https://doi.org/10.1080/09602011.2017.1326945 pmid: 28521579
17 A Hodor, S Palchykova, F Baracchi, D Noain, CL Bassetti. Baclofen facilitates sleep, neuroplasticity, and recovery after stroke in rats. Ann Clin Transl Neurol 2014; 1(10): 765–777
https://doi.org/10.1002/acn3.115 pmid: 25493268
18 U Dirnagl, K Becker, A Meisel. Preconditioning and tolerance against cerebral ischaemia: from experimental strategies to clinical use. Lancet Neurol 2009; 8(4): 398–412
https://doi.org/10.1016/S1474-4422(09)70054-7 pmid: 19296922
19 V Calabrese, C Cornelius, AT Dinkova-Kostova, EJ Calabrese, MP Mattson. Cellular stress responses, the hormesis paradigm, and vitagenes: novel targets for therapeutic intervention in neurodegenerative disorders. Antioxid Redox Signal 2010; 13(11): 1763–1811
https://doi.org/10.1089/ars.2009.3074 pmid: 20446769
20 AR Stebbing. Hormesis—the stimulation of growth by low levels of inhibitors. Sci Total Environ 1982; 22(3): 213–234
https://doi.org/10.1016/0048-9697(82)90066-3 pmid: 7043732
21 G Heusch. Myocardial ischaemia-reperfusion injury and cardioprotection in perspective. Nat Rev Cardiol 2020; 17(12): 773–789
https://doi.org/10.1038/s41569-020-0403-y pmid: 32620851
22 V Calabrese, M Renis, A Calderone, A Russo, ML Barcellona, V Rizza. 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
https://doi.org/10.1016/0891-5849(95)02095-0 pmid: 8720910
23 R Siracusa, M Scuto, R Fusco, A Trovato, ML Ontario, R Crea, R Di Paola, S Cuzzocrea, V Calabrese. Anti-inflammatory and anti-oxidant activity of Hidrox® in rotenone-induced Parkinson’s disease in mice. Antioxidants 2020; 9(9): 824
https://doi.org/10.3390/antiox9090824 pmid: 32899274
24 U Dirnagl, A Meisel. Endogenous neuroprotection: mitochondria as gateways to cerebral preconditioning? Neuropharmacology 2008; 55(3): 334–344
https://doi.org/10.1016/j.neuropharm.2008.02.017 pmid: 18402985
25 DJ Hausenloy, JA Barrabes, HE Bøtker, SM Davidson, F Di Lisa, J Downey, T Engstrom, P Ferdinandy, HA Carbrera-Fuentes, G Heusch, B Ibanez, EK Iliodromitis, J Inserte, R Jennings, N Kalia, R Kharbanda, S Lecour, M Marber, T Miura, M Ovize, MA Perez-Pinzon, HM Piper, K Przyklenk, MR Schmidt, A Redington, M Ruiz-Meana, G Vilahur, J Vinten-Johansen, DM Yellon, D Garcia-Dorado. Ischaemic conditioning and targeting reperfusion injury: a 30 year voyage of discovery. Basic Res Cardiol 2016; 111(6): 70
https://doi.org/10.1007/s00395-016-0588-8 pmid: 27766474
26 X Cheng, H Zhao, F Yan, Z Tao, R Wang, Z Han, G Li, Y Luo, X Ji. 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
https://doi.org/10.1016/j.brainres.2018.02.019 pmid: 29462606
27 C Ren, N Li, S Li, R Han, Q Huang, J Hu, K Jin, X Ji. 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
https://doi.org/10.14336/AD.2017.1106 pmid: 30271664
28 W Zhao, R Meng, C Ma, B Hou, L Jiao, F Zhu, W Wu, J Shi, Y Duan, R Zhang, J Zhang, Y Sun, H Zhang, F Ling, Y Wang, W Feng, Y Ding, B Ovbiagele, X Ji. 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
https://doi.org/10.1161/CIRCULATIONAHA.116.024807 pmid: 28174194
29 R Meng, K Asmaro, L Meng, Y Liu, C Ma, C Xi, G Li, C Ren, Y Luo, F Ling, J Jia, Y Hua, X Wang, Y Ding, EH Lo, X Ji. Upper limb ischemic preconditioning prevents recurrent stroke in intracranial arterial stenosis. Neurology 2012; 79(18): 1853–1861
https://doi.org/10.1212/WNL.0b013e318271f76a pmid: 23035060
30 W Zhao, F Jiang, Z Zhang, J Zhang, Y Ding, X Ji. Remote ischemic conditioning: a novel non-invasive approach to prevent post-stroke depression. Front Aging Neurosci 2017; 9: 270
https://doi.org/10.3389/fnagi.2017.00270 pmid: 28848427
31 ZJ Liu, C Chen, XR Li, YY Ran, T Xu, Y Zhang, XK Geng, Y Zhang, HS Du, RK Leak, XM Ji, XM Hu. Remote ischemic preconditioning-mediated neuroprotection against stroke is associated with significant alterations in peripheral immune responses. CNS Neurosci Ther 2016; 22(1): 43–52
https://doi.org/10.1111/cns.12448 pmid: 26384716
32 AJ Brager, T Yang, JC Ehlen, RP Simon, R Meller, KN Paul. Sleep is critical for remote preconditioning-induced neuroprotection. Sleep (Basel) 2016; 39(11): 2033–2040
https://doi.org/10.5665/sleep.6238 pmid: 27568798
33 MR Macleod, T O’Collins, LL Horky, DW Howells, GA Donnan. Systematic review and meta-analysis of the efficacy of melatonin in experimental stroke. J Pineal Res 2005; 38(1): 35–41
https://doi.org/10.1111/j.1600-079X.2004.00172.x pmid: 15617535
34 YS Chang, MH Lin, JH Lee, PL Lee, YS Dai, KH Chu, C Sun, YT Lin, LC Wang, HH Yu, YH Yang, CA Chen, KS Wan, BL Chiang. Melatonin supplementation for children with atopic dermatitis and sleep disturbance: a randomized clinical trial. JAMA Pediatr 2016; 170(1): 35–42
https://doi.org/10.1001/jamapediatrics.2015.3092 pmid: 26569624
35 RJ Reiter, RM Sainz, S Lopez-Burillo, JC Mayo, LC Manchester, DX Tan. Melatonin ameliorates neurologic damage and neurophysiologic deficits in experimental models of stroke. Ann N Y Acad Sci 2003; 993(1): 35–53
https://doi.org/10.1111/j.1749-6632.2003.tb07509.x pmid: 12853293
36 D Feng, B Wang, L Wang, N Abraham, K Tao, L Huang, W Shi, Y Dong, Y Qu. 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
https://doi.org/10.1111/jpi.12395 pmid: 28178380
37 K Gul-Kahraman, M Yilmaz-Bozoglan, E Sahna. 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 PMID:31155748
https://doi.org/10.1111/jpi.12589
38 DJ Hausenloy, D Garcia-Dorado, H Erik Bøtker, SM Davidson, J Downey, FB Engel, R Jennings, S Lecour, J Leor, R Madonna, M Ovize, C Perrino, F Prunier, R Schulz, JPG Sluijter, LW Van Laake, J Vinten-Johansen, DM Yellon, K Ytrehus, G Heusch, P Ferdinandy. Melatonin as a cardioprotective therapy following ST-segment elevation myocardial infarction: is it really promising? Reply. Cardiovasc Res 2017; 113(11): 1418–1419
https://doi.org/10.1093/cvr/cvx137 pmid: 28859295
39 K Karikó, D Weissman, FA Welsh. Inhibition of Toll-like receptor and cytokine signaling—a unifying theme in ischemic tolerance. J Cereb Blood Flow Metab 2004; 24(11): 1288–1304
https://doi.org/10.1097/01.WCB.0000145666.68576.71 pmid: 15545925
40 M Pace, F Baracchi, B Gao, C Bassetti. Identification of sleep-modulated pathways involved in neuroprotection from stroke. Sleep (Basel) 2015; 38(11): 1707–1718
https://doi.org/10.5665/sleep.5148 pmid: 26085290
41 IE Konstantinov, S Arab, RK Kharbanda, J Li, MM Cheung, V Cherepanov, GP Downey, PP Liu, E Cukerman, JG Coles, AN Redington. The remote ischemic preconditioning stimulus modifies inflammatory gene expression in humans. Physiol Genomics 2004; 19(1): 143–150
https://doi.org/10.1152/physiolgenomics.00046.2004 pmid: 15304621
42 JC Hsu, YS Lee, CN Chang, EA Ling, CT Lan. Sleep deprivation prior to transient global cerebral ischemia attenuates glial reaction in the rat hippocampal formation. Brain Res 2003; 984(1–2): 170–181
https://doi.org/10.1016/S0006-8993(03)03128-7 pmid: 12932851
43 M Moldovan, AO Constantinescu, A Balseanu, N Oprescu, L Zagrean, A Popa-Wagner. Sleep deprivation attenuates experimental stroke severity in rats. Exp Neurol 2010; 222(1): 135–143
https://doi.org/10.1016/j.expneurol.2009.12.023 pmid: 20045410
44 E Cam, B Gao, L Imbach, A Hodor, CL Bassetti. Sleep deprivation before stroke is neuroprotective: a pre-ischemic conditioning related to sleep rebound. Exp Neurol 2013; 247: 673–679
https://doi.org/10.1016/j.expneurol.2013.03.003 pmid: 23499829
45 CM Morin, CL Drake, AG Harvey, AD Krystal, R Manber, D Riemann, K Spiegelhalder. Insomnia disorder. Nat Rev Dis Primers 2015; 1(1): 15026
https://doi.org/10.1038/nrdp.2015.26 pmid: 27189779
46 T Porkka-Heiskanen, AV Kalinchuk. Adenosine, energy metabolism and sleep homeostasis. Sleep Med Rev 2011; 15(2): 123–135
https://doi.org/10.1016/j.smrv.2010.06.005 pmid: 20970361
47 CS McAlpine, FK Swirski. Circadian influence on metabolism and inflammation in atherosclerosis. Circ Res 2016; 119(1): 131–141
https://doi.org/10.1161/CIRCRESAHA.116.308034 pmid: 27340272
48 L Imeri, MR Opp. How (and why) the immune system makes us sleep. Nat Rev Neurosci 2009; 10(3): 199–210
https://doi.org/10.1038/nrn2576 pmid: 19209176
49 JI Granger, PL Ratti, SC Datta, RM Raymond, MR Opp. 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
https://doi.org/10.1016/j.psyneuen.2012.10.010 pmid: 23146654
50 J Castillo, MA Moro, M Blanco, R Leira, J Serena, I Lizasoain, A Dávalos. The release of tumor necrosis factor-α is associated with ischemic tolerance in human stroke. Ann Neurol 2003; 54(6): 811–819
https://doi.org/10.1002/ana.10765 pmid: 14681891
51 N Gedik, E Kottenberg, M Thielmann, UH Frey, H Jakob, J Peters, G Heusch, P Kleinbongard. Potential humoral mediators of remote ischemic preconditioning in patients undergoing surgical coronary revascularization. Sci Rep 2017; 7(1): 12660
https://doi.org/10.1038/s41598-017-12833-2 pmid: 28978919
52 XL Meng, DL Zhang, SH Sui. Acute remote ischemic preconditioning alleviates free radical injury and inflammatory response in cerebral ischemia/reperfusion rats. Exp Ther Med 2019; 18(3): 1953–1960
https://doi.org/10.3892/etm.2019.7797 pmid: 31410157
53 H Offner, S Subramanian, SM Parker, ME Afentoulis, AA Vandenbark, PD Hurn. Experimental stroke induces massive, rapid activation of the peripheral immune system. J Cereb Blood Flow Metab 2006; 26(5): 654–665
https://doi.org/10.1038/sj.jcbfm.9600217 pmid: 16121126
54 KZ Chapman, VQ Dale, A Dénes, G Bennett, NJ Rothwell, SM Allan, BW McColl. A rapid and transient peripheral inflammatory response precedes brain inflammation after experimental stroke. J Cereb Blood Flow Metab 2009; 29(11): 1764–1768
https://doi.org/10.1038/jcbfm.2009.113 pmid: 19654587
55 ZP Cai, N Parajuli, X Zheng, L Becker. Remote ischemic preconditioning confers late protection against myocardial ischemia-reperfusion injury in mice by upregulating interleukin-10. Basic Res Cardiol 2012; 107(4): 277
https://doi.org/10.1007/s00395-012-0277-1 pmid: 22752341
56 G Heusch. Adenosine and maximum coronary vasodilation in humans: myth and misconceptions in the assessment of coronary reserve. Basic Res Cardiol 2010; 105(1): 1–5
https://doi.org/10.1007/s00395-009-0074-7 pmid: 19941145
57 ZL Huang, Y Urade, O Hayaishi. The role of adenosine in the regulation of sleep. Curr Top Med Chem 2011; 11(8): 1047–1057
https://doi.org/10.2174/156802611795347654 pmid: 21401496
58 GJ Grover, PG Sleph, S Dzwonczyk. 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
https://doi.org/10.1161/01.CIR.86.4.1310 pmid: 1394937
59 MA Leesar, MF Stoddard, YT Xuan, XL Tang, R Bolli. Nonelectrocardiographic evidence that both ischemic preconditioning and adenosine preconditioning exist in humans. J Am Coll Cardiol 2003; 42(3): 437–445
https://doi.org/10.1016/S0735-1097(03)00658-2 pmid: 12906969
60 R Schulz, J Rose, H Post, G Heusch. Involvement of endogenous adenosine in ischaemic preconditioning in swine. Pflugers Arch 1995; 430(2): 273–282
https://doi.org/10.1007/BF00374659 pmid: 7675637
61 M Kitakaze, M Hori, S Takashima, H Sato, M Inoue, T Kamada. 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
https://doi.org/10.1161/01.CIR.87.1.208 pmid: 8419009
62 D Elmenhorst, EM Elmenhorst, E Hennecke, T Kroll, A Matusch, D Aeschbach, A Bauer. 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
https://doi.org/10.1073/pnas.1614677114 pmid: 28373571
63 TE Bjorness, CL Kelly, T Gao, V Poffenberger, RW Greene. Control and function of the homeostatic sleep response by adenosine A1 receptors. J Neurosci 2009; 29(5): 1267–1276
https://doi.org/10.1523/JNEUROSCI.2942-08.2009 pmid: 19193874
64 S Hu, H Dong, H Zhang, S Wang, L Hou, S Chen, J Zhang, L Xiong. 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
https://doi.org/10.1016/j.brainres.2012.04.017 pmid: 22560096
65 GJ Gross, JA Auchampach. Blockade of ATP-sensitive potassium channels prevents myocardial preconditioning in dogs. Circ Res 1992; 70(2): 223–233
https://doi.org/10.1161/01.RES.70.2.223 pmid: 1310443
66 JA Auchampach, GJ Gross. Adenosine A1 receptors, KATP channels, and ischemic preconditioning in dogs. Am J Physiol 1993; 264(5): H1327–H1336
pmid: 8498546
67 HR Lieder, P Kleinbongard, A Skyschally, H Hagelschuer, WM Chilian, G Heusch. Vago-splenic axis in signal transduction of remote ischemic preconditioning in pigs and rats. Circ Res 2018; 123(10): 1152–1163
https://doi.org/10.1161/CIRCRESAHA.118.313859 pmid: 30359199
68 M Irwin, J Thompson, C Miller, JC Gillin, M Ziegler. 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
https://doi.org/10.1210/jc.84.6.1979 pmid: 10372697
69 AN Vgontzas, J Fernandez-Mendoza, D Liao, EO Bixler. Insomnia with objective short sleep duration: the most biologically severe phenotype of the disorder. Sleep Med Rev 2013; 17(4): 241–254
https://doi.org/10.1016/j.smrv.2012.09.005 pmid: 23419741
70 AN Vgontzas, EO Bixler, DA Papanicolaou, A Kales, CA Stratakis, A Vela-Bueno, PW Gold, GP Chrousos. 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
https://doi.org/10.1210/jcem.82.10.4307 pmid: 9329353
71 G Seravalle, G Mancia, G Grassi. Sympathetic nervous system, sleep, and hypertension. Curr Hypertens Rep 2018; 20(9): 74
https://doi.org/10.1007/s11906-018-0874-y pmid: 29980938
72 AM Dorrance, G Fink. Effects of stroke on the autonomic nervous system. Compr Physiol 2015; 5(3): 1241–1263
https://doi.org/10.1002/cphy.c140016 pmid: 26140717
73 P Dutta, G Courties, Y Wei, F Leuschner, R Gorbatov, CS Robbins, Y Iwamoto, B Thompson, AL Carlson, T Heidt, MD Majmudar, F Lasitschka, M Etzrodt, P Waterman, MT Waring, AT Chicoine, AM van der Laan, HW Niessen, JJ Piek, BB Rubin, J Butany, JR Stone, HA Katus, SA Murphy, DA Morrow, MS Sabatine, C Vinegoni, MA Moskowitz, MJ Pittet, P Libby, CP Lin, FK Swirski, R Weissleder, M Nahrendorf. Myocardial infarction accelerates atherosclerosis. Nature 2012; 487(7407): 325–329
https://doi.org/10.1038/nature11260 pmid: 22763456
74 EA Lambert, CJ Thomas, R Hemmes, N Eikelis, A Pathak, MP Schlaich, GW Lambert. 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
https://doi.org/10.1152/ajpheart.00369.2016 pmid: 27288436
75 T Miura, S Kawamura, H Tatsuno, Y Ikeda, S Mikami, H Iwamoto, T Okamura, M Iwatate, M Kimura, Y Dairaku, T Maekawa, M Matsuzaki. Ischemic preconditioning attenuates cardiac sympathetic nerve injury via ATP-sensitive potassium channels during myocardial ischemia. Circulation 2001; 104(9): 1053–1058
https://doi.org/10.1161/hc3501.093800 pmid: 11524401
76 H Tsutsui, R Tanaka, M Yamagata, T Yukimura, M Ohkita, Y Matsumura. 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
https://doi.org/10.1016/j.ejphar.2013.08.032 pmid: 24036256
77 MR Irwin, EM Valladares, S Motivala, JF Thayer, CL Ehlers. Association between nocturnal vagal tone and sleep depth, sleep quality, and fatigue in alcohol dependence. Psychosom Med 2006; 68(1): 159–166
https://doi.org/10.1097/01.psy.0000195743.60952.00 pmid: 16449427
78 B Zhao, L Li, Y Jiao, M Luo, K Xu, Y Hong, JD Cao, Y Zhang, JL Fang, PJ Rong. 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
https://doi.org/10.1016/j.brs.2019.02.016 pmid: 30871845
79 B Buchholz, J Kelly, M Muñoz, EA Bernatené, N Méndez Diodati, DH González Maglio, FP Dominici, RJ Gelpi. 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
https://doi.org/10.1152/ajpheart.00286.2017 pmid: 29631370
80 G Heusch. Vagal cardioprotection in reperfused acute myocardial infarction. JACC Cardiovasc Interv 2017; 10(15): 1521–1522
https://doi.org/10.1016/j.jcin.2017.05.063 pmid: 28797428
81 MV Basalay, S Mastitskaya, A Mrochek, GL Ackland, AG Del Arroyo, J Sanchez, PO Sjoquist, J Pernow, AV Gourine, A Gourine. Glucagon-like peptide-1 (GLP-1) mediates cardioprotection by remote ischaemic conditioning. Cardiovasc Res 2016; 112(3): 669–676
https://doi.org/10.1093/cvr/cvw216 pmid: 27702763
82 E Challet. The circadian regulation of food intake. Nat Rev Endocrinol 2019; 15(7): 393–405
https://doi.org/10.1038/s41574-019-0210-x pmid: 31073218
83 H Reinke, G Asher. Crosstalk between metabolism and circadian clocks. Nat Rev Mol Cell Biol 2019; 20(4): 227–241
https://doi.org/10.1038/s41580-018-0096-9 pmid: 30635659
84 JC Ehlen, AJ Brager, J Baggs, L Pinckney, CL Gray, JP DeBruyne, KA Esser, JS Takahashi, KN Paul. Bmal1 function in skeletal muscle regulates sleep. eLife 2017; 6: e26557
https://doi.org/10.7554/eLife.26557 pmid: 28726633
85 M van den Buuse. 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
https://doi.org/10.1016/S0031-9384(99)00148-1 pmid: 10627056
86 DJ Durgan, ME Young. The cardiomyocyte circadian clock: emerging roles in health and disease. Circ Res 2010; 106(4): 647–658
https://doi.org/10.1161/CIRCRESAHA.109.209957 pmid: 20203314
87 CM Depner, EL Melanson, AW McHill, KP Wright 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
https://doi.org/10.1073/pnas.1714813115 pmid: 29784788
88 G Wolff, KA Esser. Scheduled exercise phase shifts the circadian clock in skeletal muscle. Med Sci Sports Exerc 2012; 44(9): 1663–1670
https://doi.org/10.1249/MSS.0b013e318255cf4c pmid: 22460470
89 Z Cai, H Zhong, M Bosch-Marce, K Fox-Talbot, L Wang, C Wei, MA Trush, GL Semenza. Complete loss of ischaemic preconditioning-induced cardioprotection in mice with partial deficiency of HIF-1α. Cardiovasc Res 2008; 77(3): 463–470
https://doi.org/10.1093/cvr/cvm035 pmid: 18006459
90 GL Semenza. Hypoxia-inducible factor 1: oxygen homeostasis and disease pathophysiology. Trends Mol Med 2001; 7(8): 345–350
https://doi.org/10.1016/S1471-4914(01)02090-1 pmid: 11516994
91 H Kalakech, S Tamareille, S Pons, D Godin-Ribuot, P Carmeliet, A Furber, V Martin, A Berdeaux, B Ghaleh, F Prunier. Role of hypoxia inducible factor-1α in remote limb ischemic preconditioning. J Mol Cell Cardiol 2013; 65: 98–104
https://doi.org/10.1016/j.yjmcc.2013.10.001 pmid: 24140799
92 G Heusch. HIF-1 and paradoxical phenomena in cardioprotection: expert’s perspective. Cardiovasc Res 2012; 96(2): 214–215
https://doi.org/10.1093/cvr/cvs145 pmid: 22822099
93 CB Peek, DC Levine, J Cedernaes, A Taguchi, Y Kobayashi, SJ Tsai, NA Bonar, MR McNulty, KM Ramsey, J Bass. Circadian clock interaction with HIF1α mediates oxygenic metabolism and anaerobic glycolysis in skeletal muscle. Cell Metab 2017; 25(1): 86–92 PMID:27773696
https://doi.org/10.1016/j.cmet.2016.09.010
94 Y Wu, D Tang, N Liu, W Xiong, H Huang, Y Li, Z Ma, H Zhao, P Chen, X Qi, EE Zhang. Reciprocal regulation between the circadian clock and hypoxia signaling at the genome level in mammals. Cell Metab 2017; 25(1): 73–85
https://doi.org/10.1016/j.cmet.2016.09.009 pmid: 27773697
95 Y Adamovich, B Ladeuix, M Golik, MP Koeners, G Asher. Rhythmic oxygen levels reset circadian clocks through HIF1α. Cell Metab 2017; 25(1): 93–101
https://doi.org/10.1016/j.cmet.2016.09.014 pmid: 27773695
96 MV Basalay, SM Davidson, AV Gourine, DM Yellon. Neural mechanisms in remote ischaemic conditioning in the heart and brain: mechanistic and translational aspects. Basic Res Cardiol 2018; 113(4): 25
https://doi.org/10.1007/s00395-018-0684-z pmid: 29858664
97 U Schibler, I Gotic, C Saini, P Gos, T Curie, Y Emmenegger, F Sinturel, P Gosselin, A Gerber, F Fleury-Olela, G Rando, M Demarque, P Franken. Clock-talk: interactions between central and peripheral circadian oscillators in mammals. Cold Spring Harb Symp Quant Biol 2015; 80: 223–232
https://doi.org/10.1101/sqb.2015.80.027490 pmid: 26683231
98 TA Kung, O Egbejimi, J Cui, NP Ha, DJ Durgan, MF Essop, MS Bray, CA Shaw, PE Hardin, WC Stanley, ME Young. Rapid attenuation of circadian clock gene oscillations in the rat heart following ischemia-reperfusion. J Mol Cell Cardiol 2007; 43(6): 744–753
https://doi.org/10.1016/j.yjmcc.2007.08.018 pmid: 17959196
99 MC Beker, B Caglayan, E Yalcin, AB Caglayan, S Turkseven, B Gurel, T Kelestemur, E Sertel, Z Sahin, S Kutlu, U Kilic, AT Baykal, E Kilic. 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
https://doi.org/10.1007/s12035-017-0524-4 pmid: 28421530
100 ZJ Liu, C Chen, XR Li, YY Ran, T Xu, Y Zhang, XK Geng, Y Zhang, HS Du, RK Leak, XM Ji, XM Hu. Remote ischemic preconditioning-mediated neuroprotection against stroke is associated with significant alterations in peripheral immune responses. CNS Neurosci Ther 2016; 22(1): 43–52
https://doi.org/10.1111/cns.12448 pmid: 26384716
101 Y Zhang, L Ma, C Ren, K Liu, X Tian, D Wu, Y Ding, J Li, CV Borlongan, X Ji. Immediate remote ischemic postconditioning reduces cerebral damage in ischemic stroke mice by enhancing leptomeningeal collateral circulation. J Cell Physiol 2019; 234(8): 12637–12645
https://doi.org/10.1002/jcp.27858 pmid: 30536714
[1] Long Chen, Bin Gu, Zhongpeng Wang, Lei Zhang, Minpeng Xu, Shuang Liu, Feng He, Dong Ming. EEG-controlled functional electrical stimulation rehabilitation for chronic stroke: system design and clinical application[J]. Front. Med., 2021, 15(5): 740-749.
[2] Nikolay V. Tsygan, Alexandr P. Trashkov, Igor V. Litvinenko, Viktoriya A. Yakovleva, Alexandr V. Ryabtsev, Andrey G. Vasiliev, Leonid P. Churilov. Autoimmunity in acute ischemic stroke and the role of blood--brain barrier: the dark side or the light one?[J]. Front. Med., 2019, 13(4): 420-426.
[3] Xiaohan Yang, Tiezheng Zheng, Hao Hong, Nan Cai, Xiaofeng Zhou, Changkai Sun, Liying Wu, Shuhong Liu, Yongqi Zhao, Lingling Zhu, Ming Fan, Xuezhong Zhou, Fengxie Jin. Neuroprotective effects of Ginkgo biloba extract and Ginkgolide B against oxygen–glucose deprivation/reoxygenation and glucose injury in a new in vitro multicellular network model[J]. Front. Med., 2018, 12(3): 307-318.
[4] Yufeng Zhao, Bo Liu, Liyun He, Wenjing Bai, Xueyun Yu, Xinyu Cao, Lin Luo, Peijing Rong, Yuxue Zhao, Guozheng Li, Baoyan Liu. A novel classification method for aid decision of traditional Chinese patent medicines for stroke treatment[J]. Front. Med., 2017, 11(3): 432-439.
[5] Yingchen Li,Guoheng Hu,Qilai Cheng. Implantation of human umbilical cord mesenchymal stem cells for ischemic stroke: perspectives and challenges[J]. Front. Med., 2015, 9(1): 20-29.
[6] Marie-Germaine Bousser. Stroke prevention: an update[J]. Front Med, 2012, 6(1): 22-34.
[7] Wei-Li ZHANG MD, PhD, Ru-Tai HUI MD, PhD, . Genetics of ischemic and hemorrhagic stroke in Chinese population[J]. Front. Med., 2010, 4(1): 21-28.
[8] Chen WANG PhD, MD, Zhen-Guo ZHAI PhD, MD, Ying H. SHEN PhD, MD, Lan ZHAO PhD, MD, . Clinical and genetic risk factors for venous thromboembolism in Chinese population[J]. Front. Med., 2010, 4(1): 29-35.
[9] Jiangtao YAN, Rutai HUI, Daowen WANG. Elevated C-reactive protein levels predict worsening prognosis in Chinese patients with first-onset stroke[J]. Front Med Chin, 2009, 3(1): 30-35.
[10] YAN Jiangtao, SHAO Jiaomei, WANG Daowen, YUE Zhengliang, HUI Rutai. Predication of increased plasma homocysteine level on the prognosis of Chinese patients with first-onset ischemic stroke[J]. Front. Med., 2008, 2(4): 352-355.
[11] HUANG Jiuyi, WANG Guiqing, GUO Jiping, CAO Yifeng, WANG Yan, YANG Yongju, YU Xuehai. Evaluation of the relative risk of stroke in patients with hypertension using cerebrovascular hemodynamic accumulative score[J]. Front. Med., 2007, 1(3): 274-278.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed