دورية أكاديمية
Sleep deprivation soon after recovery from synthetic torpor enhances tau protein dephosphorylation in the rat brain.
| العنوان: | Sleep deprivation soon after recovery from synthetic torpor enhances tau protein dephosphorylation in the rat brain. |
|---|---|
| المؤلفون: | Hitrec T; Department of Biomedical and NeuroMotor Sciences, University of Bologna, Piazza di Porta San Donato, 2, 40126, Bologna, Italy., Squarcio F; Department of Biomedical and NeuroMotor Sciences, University of Bologna, Piazza di Porta San Donato, 2, 40126, Bologna, Italy.; Department of Psychiatry, University of Wisconsin-Madison, Madison, WI, USA., Piscitiello E; Department of Biomedical and NeuroMotor Sciences, University of Bologna, Piazza di Porta San Donato, 2, 40126, Bologna, Italy.; Centre for Applied Biomedical Research - CRBA, University of Bologna, St. Orsola Hospital, Bologna, Italy., Cerri M; Department of Biomedical and NeuroMotor Sciences, University of Bologna, Piazza di Porta San Donato, 2, 40126, Bologna, Italy., Martelli D; Department of Biomedical and NeuroMotor Sciences, University of Bologna, Piazza di Porta San Donato, 2, 40126, Bologna, Italy.; Centre for Applied Biomedical Research - CRBA, University of Bologna, St. Orsola Hospital, Bologna, Italy., Occhinegro A; Department of Biomedical and NeuroMotor Sciences, University of Bologna, Piazza di Porta San Donato, 2, 40126, Bologna, Italy.; Centre for Applied Biomedical Research - CRBA, University of Bologna, St. Orsola Hospital, Bologna, Italy., Taddei L; Department of Biomedical and NeuroMotor Sciences, University of Bologna, Piazza di Porta San Donato, 2, 40126, Bologna, Italy.; Centre for Applied Biomedical Research - CRBA, University of Bologna, St. Orsola Hospital, Bologna, Italy., Tupone D; Department of Biomedical and NeuroMotor Sciences, University of Bologna, Piazza di Porta San Donato, 2, 40126, Bologna, Italy.; Department of Neurological Surgery, Oregon Health and Science University, Portland, OR, USA., Amici R; Department of Biomedical and NeuroMotor Sciences, University of Bologna, Piazza di Porta San Donato, 2, 40126, Bologna, Italy., Luppi M; Department of Biomedical and NeuroMotor Sciences, University of Bologna, Piazza di Porta San Donato, 2, 40126, Bologna, Italy. marco.luppi@unibo.it.; Centre for Applied Biomedical Research - CRBA, University of Bologna, St. Orsola Hospital, Bologna, Italy. marco.luppi@unibo.it. |
| المصدر: | Journal of comparative physiology. B, Biochemical, systemic, and environmental physiology [J Comp Physiol B] 2024 Jun; Vol. 194 (3), pp. 347-368. Date of Electronic Publication: 2023 Oct 09. |
| نوع المنشور: | Journal Article |
| اللغة: | English |
| بيانات الدورية: | Publisher: Springer-Verlag Country of Publication: Germany NLM ID: 8413200 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1432-136X (Electronic) Linking ISSN: 01741578 NLM ISO Abbreviation: J Comp Physiol B Subsets: MEDLINE |
| أسماء مطبوعة: | Original Publication: Berlin ; New York : Springer-Verlag, [c1984- |
| مواضيع طبية MeSH: | Sleep Deprivation*/metabolism , Sleep Deprivation*/physiopathology , tau Proteins*/metabolism , Torpor*/physiology , Brain*/metabolism , Rats, Wistar*, Animals ; Male ; Phosphorylation ; Rats ; Microglia/metabolism |
| مستخلص: | Neuronal Tau protein hyperphosphorylation (PPtau) is a hallmark of tauopathic neurodegeneration. However, a reversible brain PPtau occurs in mammals during either natural or "synthetic" torpor (ST), a transient deep hypothermic state that can be pharmacologically induced in rats. Since in both conditions a high sleep pressure builds up during the regaining of euthermia, the aim of this work was to assess the possible role of post-ST sleep in PPtau dephosphorylation. Male rats were studied at the hypothermic nadir of ST, and 3-6 h after the recovery of euthermia, after either normal sleep (NS) or total sleep deprivation (SD). The effects of SD were studied by assessing: (i) deep brain temperature (Tb); (ii) immunofluorescent staining for AT8 (phosphorylated Tau) and Tau-1 (non-phosphorylated Tau), assessed in 19 brain structures; (iii) different phosphorylated forms of Tau and the main cellular factors involved in Tau phospho-regulation, including pro- and anti-apoptotic markers, assessed through western blot in the parietal cortex and hippocampus; (iv) systemic factors which are involved in natural torpor; (v) microglia activation state, by considering morphometric variations. Unexpectedly, the reversibility of PPtau was more efficient in SD than in NS animals, and was concomitant with a higher Tb, higher melatonin plasma levels, and a higher frequency of the microglia resting phenotype. Since the reversibility of ST-induced PPtau was previously shown to be driven by a latent physiological molecular mechanism triggered by deep hypothermia, short-term SD soon after the regaining of euthermia seems to boost the possible neuroprotective effects of this mechanism. (© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.) |
| References: | Amici R, Cerri M, Ocampo-Garcés A, Baracchi F, Dentico D, Jones CA, Luppi M, Perez E, Parmeggiani PL, Zamboni G (2008) Cold exposure and sleep in the rat: REM sleep homeostasis and body size. Sleep 31:708–715. https://doi.org/10.1093/sleep/31.5.708. (PMID: 10.1093/sleep/31.5.70818517040) Arendt T, Stieler J, Holzer M (2015) Brain hypometabolism triggers PHF-like phosphorylation of tau, a major hallmark of Alzheimer’s disease pathology. J Neural Transm (vienna) 122:531–539. https://doi.org/10.1007/s00702-014-1342-8. (PMID: 10.1007/s00702-014-1342-825480630) Baldy C, Fournier S, Boisjoly-Villeneuve S, Tremblay MÈ, Kinkead R (2018) The influence of sex and neonatal stress on medullary microglia in rat pups. Exp Physiol 103:1192–1199. https://doi.org/10.1113/EP087088. (PMID: 10.1113/EP08708829920821) Billingsley ML, Kincaid RL (1997) Regulated phosphorylation and dephosphorylation of tau protein: effects on microtubule interaction, intracellular trafficking and neurodegeneration. Biochem J 323:577–591. https://doi.org/10.1042/bj3230577. (PMID: 10.1042/bj32305779169588) Blessing WW, Nalivaiko E (2001) Raphe magnus/pallidus neurons regulate tail but not mesenteric arterial blood flow in rats. Neuroscience 105:923–929. https://doi.org/10.1016/s0306-4522(01)00251-2. (PMID: 10.1016/s0306-4522(01)00251-211530230) Cerri M (2017) The Central Control of Energy Expenditure: Exploiting Torpor for Medical Applications. Annu Rev Physiol 79:167–186. https://doi.org/10.1146/annurev-physiol-022516-034133. (PMID: 10.1146/annurev-physiol-022516-03413327813827) Cerri M, Ocampo-Garces A, Amici R, Baracchi F, Capitani P, Jones CA, Luppi M, Perez E, Parmeggiani PL, Zamboni G (2005) Cold exposure and sleep in the rat: effects on sleep architecture and the electroencephalogram. Sleep 28:694–705. https://doi.org/10.1093/sleep/28.6.694. (PMID: 10.1093/sleep/28.6.69416477956) Cerri M, Mastrotto M, Tupone D, Martelli D, Luppi M, Perez E, Zamboni G, Amici R (2013) The inhibition of neurons in the central nervous pathways for thermoregulatory cold defense induces a suspended animation state in the rat. J Neurosci 33:2984–2993. https://doi.org/10.1523/JNEUROSCI.3596-12.2013. (PMID: 10.1523/JNEUROSCI.3596-12.201323407956) Cerri M, Luppi M, Tupone D, Zamboni G, Amici R (2017) REM Sleep and Endothermy: potential sites and mechanism of a reciprocal interference. Front Physiol 8:624. https://doi.org/10.3389/fphys.2017.00624. (PMID: 10.3389/fphys.2017.0062428883799) Cerri M, Hitrec T, Luppi M, Amici R (2021) Be cool to be far: Exploiting hibernation for space exploration. Neurosci Biobehav Rev 128:218–232. https://doi.org/10.1016/j.neubiorev.2021.03.037. (PMID: 10.1016/j.neubiorev.2021.03.03734144115) Chiocchetti R, Hitrec T, Giancola F, Sadeghinezhad J, Squarcio F, Galiazzo G, Piscitiello E, De Silva M, Cerri M, Amici R, Luppi M (2021) Phosphorylated Tau protein in the myenteric plexus of the ileum and colon of normothermic rats and during synthetic torpor. Cell Tissue Res 384:287–299. https://doi.org/10.1007/s00441-020-03328-0. (PMID: 10.1007/s00441-020-03328-0335114698141491) Danis C, Dupré E, Hanoulle X, Landrieu I, Lasorsa A, Neves JF, Schneider R, Smet-Nocca C (2019) Nuclear magnetic resonance spectroscopy insights into tau structure in solution: impact of post-translational modifications. In: Takashima A, WolozinB, Buee L (eds.) Tau Biology. Advances in Experimental Medicine and Biology - vol. 1184. Springer Nature, Singapore, pp 97–103. https://doi.org/10.1007/978-981-32-9358-8_3 . ISBN: 978-981-32-9357-1. Davis BM, Salinas-Navarro M, Cordeiro MF, Moons L, De Groef L (2017) Characterizing microglia activation: a spatial statistics approach to maximize information extraction. Sci Rep 7:1576. https://doi.org/10.1038/s41598-017-01747-8. (PMID: 10.1038/s41598-017-01747-828484229) Decker JM, Mandelkow EM (2019). Presynaptic Pathophysiology Encoded in Different Domains of Tau – Hyper-Versus Hypoexcitability? In: Takashima A, WolozinB, Buee L (eds.) Tau Biology. Advances in Experimental Medicine and Biology - vol. 1184. Springer Nature, Singapore, pp 97–103. doi: https://doi.org/10.1007/978-981-32-9358-8_8 . ISBN: 978–981–32–9357–1. Franken P (2002) Long-term vs. short-term processes regulating REM sleep. J Sleep Res 11:17–28. https://doi.org/10.1046/j.1365-2869.2002.00275.x. (PMID: 10.1046/j.1365-2869.2002.00275.x11869422) Franken P, Dijk DJ, Tobler I, Borbély AA (1991) Sleep deprivation in rats: effects on EEG power spectra, vigilance states, and cortical temperature. Am J Physiol 261:R198–R208. https://doi.org/10.1152/ajpregu.1991.261.1.R198. (PMID: 10.1152/ajpregu.1991.261.1.R1981858947) Gao BO, Franken P, Tobler I, Borbély AA (1995) Effect of elevated ambient temperature on sleep, EEG spectra, and brain temperature in the rat. Am J Physiol 268:R1365–R1373. https://doi.org/10.1152/ajpregu.1995.268.6.R1365. (PMID: 10.1152/ajpregu.1995.268.6.R13657611510) Giedke H, Schwärzler F (2002) Therapeutic use of sleep deprivation in depression. Sleep Med Rev 6:361–377 (PMID: 12531127). (PMID: 10.1053/smrv.2002.023512531127) Goedert M, Spillantini M.G. (2019). Ordered Assembly of Tau Protein and Neurodegeneration In: Takashima A, WolozinB, Buee L (eds.) Tau Biology. Advances in Experimental Medicine and Biology - vol. 1184. Springer Nature, Singapore, pp. 3–21. doi: https://doi.org/10.1007/978-981-32-9358-8_8 . ISBN: 978-981-32-9357-1. Guisle I, Canet G, Pétry S, Fereydouni-Forouzandeh P, Morin F, Kérauden R, Whittington RA, Calon F, Hébert SS, Planel E (2022) Sauna-like conditions or menthol treatment reduce tau phosphorylation through mild hyperthermia. Neurobiol Aging 113:118–130. https://doi.org/10.1016/j.neurobiolaging.2022.02.011. (PMID: 10.1016/j.neurobiolaging.2022.02.01135334439) Guisle I, Gratuze M, Petry S, Morin F, Keraudren R, Whittington RA, Hébert SS, Mongrain V, Planel E (2020). Circadian and sleep/wake-dependent variations in tau phosphorylation are driven by temperature. Sleep 43:zsz266. doi: https://doi.org/10.1093/sleep/zsz266 . Gutfreund H (1995) Kinetics for the life sciences: receptors, transmitters and catalysts. Cambridge University Press, Cambridge (UK). ISBN: 0-521-48027-2. Heller HC, Ruby NF (2004) Sleep and circadian rhythms in mammalian torpor. Annu Rev Physiol 66:275–289. https://doi.org/10.1146/annurev.physiol.66.032102.115313. (PMID: 10.1146/annurev.physiol.66.032102.11531314977404) Hitrec T, Squarcio F, Cerri M, Martelli D, Occhinegro A, Piscitiello E, Tupone D, Amici R, Luppi M (2021) Reversible Tau Phosphorylation Induced by Synthetic Torpor in the Spinal Cord of the Rat. Front Neuroanat 15:592288. https://doi.org/10.3389/fnana.2021.592288. (PMID: 10.3389/fnana.2021.592288336036517884466) Hu W, Wu F, Zhang Y, Gong CX, Iqbal K, Liu F (2017) Expression of Tau Pathology-Related Proteins in Different Brain Regions: A Molecular Basis of Tau Pathogenesis. Front Aging Neurosci 9:311. https://doi.org/10.3389/fnagi.2017.00311. (PMID: 10.3389/fnagi.2017.00311290217565623682) Hudson JW, Scott IM (1979) Daily Torpor in the Laboratory Mouse, Mus musculus Var. Albino. Physiol Zool 52:205–218. https://doi.org/10.1086/physzool.52.2.30152564. (PMID: 10.1086/physzool.52.2.30152564) Ittner A, Chua SW, Bertz J, Volkerling A, van der Hoven J, Gladbach A, Przybyla M, Bi M, van Hummel A, Stevens CH, Ippati S, Suh LS, Macmillan A, Sutherland G, Kril JJ, Silva AP, Mackay JP, Poljak A, Delerue F, Ke YD, Ittner LM (2016) Site-specific phosphorylation of Tau inhibits amyloid-β toxicity in Alzheimer’s mice. Science 354:904–908. https://doi.org/10.1126/science.aah6205. (PMID: 10.1126/science.aah620527856911) Kitagishi Y, Nakanishi A, Ogura Y, Matsuda S (2014) Dietary regulation of PI3K/AKT/GSK-3β pathway in Alzheimer’s disease. Alzheimers Res Ther 6:35. https://doi.org/10.1186/alzrt265. (PMID: 10.1186/alzrt265250316414075129) Kräuchi K (2007) The thermophysiological cascade leading to sleep initiation in relation to phase of entrainment. Sleep Med Rev 11:439–451. https://doi.org/10.1016/j.smrv.2007.07.001. (PMID: 10.1016/j.smrv.2007.07.00117764994) Kuhn M, Maier JG, Wolf E, Mainberger F, Feige B, Maywald S, Bredl A, Michel M, Sendelbach N, Normann C, Klöppel S, Eckert A, Riemann D, Nissen C (2020) Indices of cortical plasticity after therapeutic sleep deprivation in patients with major depressive disorder. J Affect Disord 277:425–435. https://doi.org/10.1016/j.jad.2020.08.052. (PMID: 10.1016/j.jad.2020.08.05232866801) Lew CH, Petersen C, Neylan TC, Grinberg LT (2021) Tau-driven degeneration of sleep- and wake-regulating neurons in Alzheimer’s disease. Sleep Med Rev 60:101541. https://doi.org/10.1016/j.smrv.2021.101541. (PMID: 10.1016/j.smrv.2021.10154134500400) Liu D, Wei N, Man HY, Lu Y, Zhu LQ, Wang JZ (2015) The MT2 receptor stimulates axonogenesis and enhances synaptic transmission by activating Akt signaling. Cell Death Differ 22:583–596. https://doi.org/10.1038/cdd.2014.195. (PMID: 10.1038/cdd.2014.19525501601) Lo Martire V, Berteotti C, Bastianini S, Alvente S, Valli A, Cerri M, Amici R, Silvani A, Swoap SJ, Zoccoli G (2020) The physiological signature of daily torpor is not orexin dependent. J Comp Physiol B 190:493–507. https://doi.org/10.1007/s00360-020-01281-6. (PMID: 10.1007/s00360-020-01281-632399793) Luppi M, Al-Jahmany AA, Del Vecchio F, Cerri M, Di Cristoforo A, Hitrec T, Martelli D, Perez E, Zamboni G, Amici R (2017) Wake-sleep and cardiovascular regulatory changes in rats made obese by a high-fat diet. Behav Brain Res 320:347–355. https://doi.org/10.1016/j.bbr.2016.12.024. (PMID: 10.1016/j.bbr.2016.12.02428011172) Luppi M, Hitrec T, Di Cristoforo A, Squarcio F, Stanzani A, Occhinegro A, Chiavetta P, Tupone D, Zamboni G, Amici R, Cerri M (2019) Phosphorylation and Dephosphorylation of Tau Protein During Synthetic Torpor. Front Neuroanat 13:57. https://doi.org/10.3389/fnana.2019.00057. (PMID: 10.3389/fnana.2019.0005731244617) Maeda S, Takashima A (2019). Tau Oligomers In: Takashima A, WolozinB, Buee L (eds.) Tau Biology. Advances in Experimental Medicine and Biology - vol. 1184. Springer Nature, Singapore, pp 373–380. doi: https://doi.org/10.1007/978-981-32-9358-8_8 . ISBN: 978–981–32–9357–1. Malia TJ, Teplyakov A, Ernst R, Wu SJ, Lacy ER, Liu X, Vandermeeren M, Mercken M, Luo J, Sweet RW, Gilliland GL (2016) Epitope mapping and structural basis for the recognition of phosphorylated Tau by the anti-Tau antibody AT8. Proteins 84:427–434. https://doi.org/10.1002/prot.24988. (PMID: 10.1002/prot.2498826800003) Marshall CJ (1997) Cold-adapted enzymes. Trends Biotechnol 15:359–364. https://doi.org/10.1016/S0167-7799(97)01086-X. (PMID: 10.1016/S0167-7799(97)01086-X9293034) Morrison SF, Nakamura K (2019) Central Mechanisms for Thermoregulation. Annu Rev Physiol 81:285–308. https://doi.org/10.1146/annurev-physiol-020518-114546. (PMID: 10.1146/annurev-physiol-020518-11454630256726) Nilson AN, English KC, Gerson JE, Barton Whittle T, Nicolas Crain C, Xue J, Sengupta U, Castillo-Carranza DL, Zhang W, Gupta P, Kayed R (2017) Tau Oligomers Associate with Inflammation in the Brain and Retina of Tauopathy Mice and in Neurodegenerative Diseases. J Alzheimers Dis 55:1083–1099. https://doi.org/10.3233/JAD-160912. (PMID: 10.3233/JAD-16091227716675) Paxinos G, Watson C (2007) The rat brain in stereotaxic coordinates. 6th Edition. Elsevier, San Diego. ISBN–13: 978-0-12-547612-6. Planel E, Miyasaka T, Launey T, Chui DH, Tanemura K, Sato S, Murayama O, Ishiguro K, Tatebayashi Y, Takashima A (2004) Alterations in glucose metabolism induce hypothermia leading to Tau hyperphosphorylation through differential inhibition of kinase and phosphatase activities: implications for Alzheimer’s disease. J Neurosci 24:2401–2411. https://doi.org/10.1523/JNEUROSCI.5561-03.2004. (PMID: 10.1523/JNEUROSCI.5561-03.200415014115) Planel E, Richter KE, Nolan CE, Finley JE, Liu L, Wen Y, Krishnamurthy P, Herman M, Wang L, Schachter JB, Nelson RB, Lau LF, Duff KE (2007) Anesthesia leads to tau hyperphosphorylation through inhibition of phosphatase activity by hypothermia. J Neurosci 27:3090–3097. https://doi.org/10.1523/JNEUROSCI.4854-06.2007. (PMID: 10.1523/JNEUROSCI.4854-06.200717376970) Planel E, Bretteville A, Liu L, Virag L, Du AL, Yu WH, Dickson DW, Whittington RA, Duff KE (2009) Acceleration and persistence of neurofibrillary pathology in a mouse model of tauopathy following anesthesia. FASEB J 23:2595–2604. https://doi.org/10.1096/fj.08-122424. (PMID: 10.1096/fj.08-12242419279139) Ransohoff RM (2016) How neuroinflammation contributes to neurodegeneration. Science 353:777–783. https://doi.org/10.1126/science.aag2590. (PMID: 10.1126/science.aag259027540165) Rechtschaffen A, Bergmann BM, Gilliland MA, Bauer K (1999) Effects of method, duration, and sleep stage on rebounds from sleep deprivation in the rat. Sleep 22:11–31. https://doi.org/10.1093/sleep/22.1.11. (PMID: 10.1093/sleep/22.1.119989363) Sela Y, Hoekstra MM, Franken P (2021) Sub-minute prediction of brain temperature based on sleep-wake state in the mouse. Elife 10:e62073. https://doi.org/10.7554/eLife.62073. (PMID: 10.7554/eLife.6207333683202) Squarcio F, Hitrec T, Piscitiello E, Cerri M, Giovannini C, Martelli D, Occhinegro A, Taddei L, Tupone D, Amici R, Luppi M (2023) Synthetic torpor triggers a regulated mechanism in the rat brain, favoring the reversibility of Tau protein hyperphosphorylation. Front Physiol 14:1129278. https://doi.org/10.3389/fphys.2023.1129278. (PMID: 10.3389/fphys.2023.112927836969585) Su B, Wang X, Drew KL, Perry G, Smith MA, Zhu X (2008) Physiological regulation of Tau phosphorylation during hibernation. J Neurochem 105:2098–2108. https://doi.org/10.1111/j.1471-4159.2008.05294.x. (PMID: 10.1111/j.1471-4159.2008.05294.x18284615) Szendrei GI, Lee VM, Otvos L Jr (1993) Recognition of the minimal epitope of monoclonal antibody Tau-1 depends upon the presence of a phosphate group but not its location. J Neurosci Res 34:243–249. https://doi.org/10.1002/jnr.490340212. (PMID: 10.1002/jnr.4903402127680727) Tinganelli W, Hitrec T, Romani F, Simoniello P, Squarcio F, Stanzani A, Piscitiello E, Marchesano V, Luppi M, Sioli M, Helm A, Compagnone G, Morganti AG, Amici R, Negrini M, Zoccoli A, Durante M, Cerri M (2019) Hibernation and Radioprotection: Gene Expression in the Liver and Testicle of Rats Irradiated under Synthetic Torpor. Int J Mol Sci 20:352. https://doi.org/10.3390/ijms20020352. (PMID: 10.3390/ijms20020352306544676359347) Tournissac M, Leclerc M, Valentin-Escalera J, Vandal M, Bosoi CR, Planel E, Calon F (2021) Metabolic determinants of Alzheimer’s disease: A focus on thermoregulation. Ageing Res Rev 72:101462. https://doi.org/10.1016/j.arr.2021.101462. (PMID: 10.1016/j.arr.2021.10146234534683) von der Ohe CG, Garner CC, Darian-Smith C, Heller HC (2007) Synaptic protein dynamics in hibernation. J Neurosci 27:84–92. https://doi.org/10.1523/JNEUROSCI.4385-06.2007. (PMID: 10.1523/JNEUROSCI.4385-06.2007172024756672296) Vyazovskiy VV, Palchykova S, Achermann P, Tobler I, Deboer T (2017) Different Effects of Sleep Deprivation and Torpor on EEG Slow-Wave Characteristics in Djungarian Hamsters. Cereb Cortex 27:950–961. https://doi.org/10.1093/cercor/bhx020. (PMID: 10.1093/cercor/bhx020281682945390404) Wang Y, Mandelkow E (2016) Tau in physiology and pathology. Nat Rev Neurosci 17:5–21. https://doi.org/10.1038/nrn.2015.1. (PMID: 10.1038/nrn.2015.126631930) Whittington RA, Bretteville A, Dickler MF, Planel E (2013) Anesthesia and Tau pathology. Prog Neuropsychopharmacol Biol Psychiatry 47:147–155. https://doi.org/10.1016/j.pnpbp.2013.03.004. (PMID: 10.1016/j.pnpbp.2013.03.00423535147) |
| معلومات مُعتمدة: | 2018/0370 Fondazione Cassa di Risparmio in Bologna; 4000123556 European Space Agency |
| فهرسة مساهمة: | Keywords: Brain temperature; Deep hypothermia; Gentle handling; Melatonin; Microglia; Sleep pressure |
| المشرفين على المادة: | 0 (tau Proteins) |
| تواريخ الأحداث: | Date Created: 20231009 Date Completed: 20240709 Latest Revision: 20240802 |
| رمز التحديث: | 20240802 |
| DOI: | 10.1007/s00360-023-01516-2 |
| PMID: | 37812305 |
| قاعدة البيانات: | MEDLINE |
Find this article in full text from Springer Verlag. 
Full Text Finder | تدمد: | 1432-136X |
|---|---|
| DOI: | 10.1007/s00360-023-01516-2 |