Vulnerability of Left Amygdala to Total Sleep Deprivation and Reversed Circadian Rhythm in Molecular Level: Glut1 as a Metabolic Biomarker
AbstractBackground: Sleep deprivation (SD) in the long term can cause multi-organ dysfunction as well as neurocognitive disorders. Daytime sleep or napping is a biological compensate due to insomnia or sleep deprivation. Metabolic responses to this biological rhythm may being as a biological indicator or biomarker to compare the effect of them. Glucose transporter type 1 (Glut-1) is one of the metabolic biomarkers that is affected by several conditions such as stress, seizure, malignancy, and neurocognitive disorders. We studied the effect of SD, circadian reversed (R) and napping models on the Glut-1 expression level in the right and left amygdala. Materials and Methods: Sixty-four Wistar rats were divided into eight groups as follow: Intact group that rats were placed in a cage without any intervention. In the sham group, rats were on the stable pedal of the SD apparatus (turn off). Experimental groups include total SD48, total SD48- (plus short nap), total SD48+ (plus long nap), R48, R48- (plus short nap), and R48+ (plus long nap).The Glut-1 expression level in the right and left amygdala were measured by western blotting. Results: Our findings demonstrated the significant effect of both SD for 48 hours and reversed circadian on the expression of Glut-1 from sham and intact groups. The long nap plus them could decrease the elevation of Glut-1 in the left amygdala. However, the short nap could not reduce this elevation of Glut-1. Conclusion: Left amygdala is vulnerable to the fluctuation of hypothalamic-pituitary-adrenal axis and stress. In other words, sleep disorders are affecting by Glut-1 as a metabolic biomarker in left amygdala alone. [GMJ.2019;8:e970]
McEwen BS. Sleep deprivation as a neurobiologic and physiologic stressor: allostasis and allostatic load. Metabolism. 2006;55:S20-S3.
Altevogt BM, Colten HR. Sleep disorders and sleep deprivation: an unmet public health problem. National Academies Press; 2006.
Palmer CA, Alfano CA. Sleep Architecture Relates to Daytime Affect and Somatic Complaints in Clinically Anxious but Not Healthy Children. Journal of Clinical Child & Adolescent Psychology. 2017;46(2):175-87.
Payne JD, Kensinger EA. Sleep leads to changes in the emotional memory trace: evidence from FMRI. Journal of Cognitive Neuroscience. 2011;23(6):1285-97.
Payne JD, Stickgold R, Swanberg K, Kensinger EA. Sleep preferentially enhances memory for emotional components of scenes. Psychological Science. 2008;19(8):781-8.
Rasch B, Born J. Maintaining memories by reactivation. Current opinion in neurobiology. 2007;17(6):698-703.
Smith C. Sleep states and memory processes. Behavioural brain research. 1995;69(1):137-45.
Stickgold R. Sleep-dependent memory consolidation. Nature. 2005;437(7063):1272.
Walker MP, Stickgold R. Sleep, memory, and plasticity. Annu Rev Psychol. 2006;57:139-66.
Tucker MA, Hirota Y, Wamsley EJ, Lau H, Chaklader A, Fishbein W. A daytime nap containing solely non-REM sleep enhances declarative but not procedural memory. Neurobiology of learning and memory. 2006;86(2):241-7.
Wulff K, Gatti S, Wettstein JG, Foster RG. Sleep and circadian rhythm disruption in psychiatric and neurodegenerative disease. Nature reviews Neuroscience. 2010;11(8):589.
Åkerstedt T, Torsvall L. Napping in shift work. Sleep. 1985;8(2):105-9.
Watamura SE, Donzella B, Kertes DA, Gunnar MR. Developmental changes in baseline cortisol activity in early childhood: Relations with napping and effortful control. Developmental Psychobiology. 2004;45(3):125-33.
Takahashi M. The role of prescribed napping in sleep medicine. Sleep medicine reviews. 2003;7(3):227-35.
Walker MP, van Der Helm E. Overnight therapy? The role of sleep in emotional brain processing. Psychological bulletin. 2009;135(5):731.
Marcaggi P, Attwell D. Role of glial amino acid transporters in synaptic transmission and brain energetics. Glia. 2004;47(3):217-25.
Sofroniew MV. Molecular dissection of reactive astrogliosis and glial scar formation. Trends in neurosciences. 2009;32(12):638-47.
Sofroniew MV, Vinters HV. Astrocytes: biology and pathology. Acta neuropathologica. 2010;119(1):7-35.
Morales I, Rodriguez M. Self‐induced accumulation of glutamate in striatal astrocytes and basal ganglia excitotoxicity. Glia. 2012;60(10):1481-94.
Featherstone DE. Intercellular glutamate signaling in the nervous system and beyond. ACS chemical neuroscience. 2009;1(1):4-12.
Darby M, Kuzmiski JB, Panenka W, Feighan D, MacVicar BA. ATP released from astrocytes during swelling activates chloride channels. Journal of neurophysiology. 2003;89(4):1870-7.
Starkov AA, Fiskum G, Chinopoulos C, Lorenzo BJ, Browne SE, Patel MS et al. Mitochondrial α-ketoglutarate dehydrogenase complex generates reactive oxygen species. Journal of Neuroscience. 2004;24(36):7779-88.
Tretter L, Adam-Vizi V. Alpha-ketoglutarate dehydrogenase: a target and generator of oxidative stress. Philosophical Transactions of the Royal Society of London B: Biological Sciences. 2005;360(1464):2335-45.
Falkowska A, Gutowska I, Goschorska M, Nowacki P, Chlubek D, Baranowska-Bosiacka I. Energy metabolism of the brain, including the cooperation between astrocytes and neurons, especially in the context of glycogen metabolism. International journal of molecular sciences. 2015;16(11):25959-81.
Young CD, Lewis AS, Rudolph MC, Ruehle MD, Jackman MR, Yun UJ et al. Modulation of glucose transporter 1 (GLUT1) expression levels alters mouse mammary tumor cell growth in vitro and in vivo. PloS one. 2011;6(8):e23205.
Detka J, Kurek A, Basta-Kaim A, Kubera M, Lasoń W, Budziszewska B. Elevated brain glucose and glycogen concentrations in an animal model of depression. Neuroendocrinology. 2014;100(2-3):178-90.
Weber Y, Kamm C, Suls A, Kempfle J, Kotschet K, Schüle R et al. Paroxysmal choreoathetosis/spasticity (DYT9) is caused by a GLUT1 defect. Neurology. 2011;77(10):959-64.
Meerlo P, Sgoifo A, Suchecki D. Restricted and disrupted sleep: effects on autonomic function, neuroendocrine stress systems and stress responsivity. Sleep medicine reviews. 2008;12(3):197-210.
Norozpour Y, Nasehi M, Sabouri-Khanghah V, Torabi-Nami M, Zarrindast M-R. The effect of CA1 α2 adrenergic receptors on memory retention deficit induced by total sleep deprivation and the reversal of circadian rhythm in a rat model. Neurobiology of learning and memory. 2016;133:53-60.
Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical biochemistry. 1976;72(1-2):248-54.
Drevets WC, Price JL, Furey ML. Brain structural and functional abnormalities in mood disorders: implications for neurocircuitry models of depression. Brain structure and function. 2008;213(1-2):93-118.
LeDoux J. The emotional brain, fear, and the amygdala. Cellular and molecular neurobiology. 2003;23(4-5):727-38.
Tamaki M, Bang JW, Watanabe T, Sasaki Y. Night watch in one brain hemisphere during sleep associated with the first-night effect in humans. Current biology. 2016;26(9):1190-4.
Ocklenburg S, Korte SM, Peterburs J, Wolf OT, Güntürkün O. Stress and laterality–The comparative perspective. Physiology & behavior. 2016;164:321-9.
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution 4.0 International License that allows others to share the work with an acknowledgment of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgment of its initial publication in this journal.
- Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).