Cover Image

Vulnerability of Left Amygdala to Total Sleep Deprivation and Reversed Circadian Rhythm in Molecular Level: Glut1 as a Metabolic Biomarker

Parastou Kordestani Moghadam, Mohammad Nasehi, Fariba Khodagholi, Mohamad Reza Zarrindast

Background: 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] 

Sleep; Circadian Rhythm; Glucose Transport Protein; Amygdala

McEwen BS. Sleep deprivation as a neurobiologic and physiologic stressor: allostasis and allostatic load. Metabolism. 2006;55:S20-S3.

https://doi.org/10.1016/j.metabol.2006.07.008

PMid:16979422

Altevogt BM, Colten HR. Sleep disorders and sleep deprivation: an unmet public health problem. National Academies Press; 2006.

PMCid:PMC1360713

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.

https://doi.org/10.1080/15374416.2016.1188704

PMid:27610927

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.

https://doi.org/10.1162/jocn.2010.21526

PMid:20521852

Payne JD, Stickgold R, Swanberg K, Kensinger EA. Sleep preferentially enhances memory for emotional components of scenes. Psychological Science. 2008;19(8):781-8.

https://doi.org/10.1111/j.1467-9280.2008.02157.x

PMid:18816285 PMCid:PMC5846336

Rasch B, Born J. Maintaining memories by reactivation. Current opinion in neurobiology. 2007;17(6):698-703.

https://doi.org/10.1016/j.conb.2007.11.007

PMid:18222688

Smith C. Sleep states and memory processes. Behavioural brain research. 1995;69(1):137-45.

https://doi.org/10.1016/0166-4328(95)00024-N

Stickgold R. Sleep-dependent memory consolidation. Nature. 2005;437(7063):1272.

https://doi.org/10.1038/nature04286

PMid:16251952

Walker MP, Stickgold R. Sleep, memory, and plasticity. Annu Rev Psychol. 2006;57:139-66.

https://doi.org/10.1146/annurev.psych.56.091103.070307

PMid:16318592

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.

https://doi.org/10.1016/j.nlm.2006.03.005

PMid:16647282

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.

https://doi.org/10.1038/nrn2868

PMid:20631712

Åkerstedt T, Torsvall L. Napping in shift work. Sleep. 1985;8(2):105-9.

https://doi.org/10.1093/sleep/8.2.105

PMid:4012152

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.

https://doi.org/10.1002/dev.20026

PMid:15505801

Takahashi M. The role of prescribed napping in sleep medicine. Sleep medicine reviews. 2003;7(3):227-35.

https://doi.org/10.1053/smrv.2002.0241

PMid:12927122

Walker MP, van Der Helm E. Overnight therapy? The role of sleep in emotional brain processing. Psychological bulletin. 2009;135(5):731.

https://doi.org/10.1037/a0016570

PMid:19702380 PMCid:PMC2890316

Marcaggi P, Attwell D. Role of glial amino acid transporters in synaptic transmission and brain energetics. Glia. 2004;47(3):217-25.

https://doi.org/10.1002/glia.20027

PMid:15252810

Sofroniew MV. Molecular dissection of reactive astrogliosis and glial scar formation. Trends in neurosciences. 2009;32(12):638-47.

https://doi.org/10.1016/j.tins.2009.08.002

PMid:19782411 PMCid:PMC2787735

Sofroniew MV, Vinters HV. Astrocytes: biology and pathology. Acta neuropathologica. 2010;119(1):7-35.

https://doi.org/10.1007/s00401-009-0619-8

PMid:20012068 PMCid:PMC2799634

Morales I, Rodriguez M. Self‐induced accumulation of glutamate in striatal astrocytes and basal ganglia excitotoxicity. Glia. 2012;60(10):1481-94.

https://doi.org/10.1002/glia.22368

PMid:22715058

Featherstone DE. Intercellular glutamate signaling in the nervous system and beyond. ACS chemical neuroscience. 2009;1(1):4-12.

https://doi.org/10.1021/cn900006n

PMid:22778802 PMCid:PMC3368625

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.

https://doi.org/10.1152/jn.00510.2002

PMid:12686569

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.

https://doi.org/10.1523/JNEUROSCI.1899-04.2004

PMid:15356189

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.

https://doi.org/10.1098/rstb.2005.1764

PMid:16321804 PMCid:PMC1569585

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.

https://doi.org/10.3390/ijms161125939

PMid:26528968 PMCid:PMC4661798

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.

https://doi.org/10.1371/journal.pone.0023205

PMid:21826239 PMCid:PMC3149640

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.

https://doi.org/10.1159/000368607

PMid:25300940

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.

https://doi.org/10.1212/WNL.0b013e31822e0479

PMid:21832227

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.

https://doi.org/10.1016/j.smrv.2007.07.007

PMid:18222099

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.

https://doi.org/10.1016/j.nlm.2016.06.004

PMid:27291858

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.

https://doi.org/10.1016/0003-2697(76)90527-3

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.

https://doi.org/10.1007/s00429-008-0189-x

PMid:18704495 PMCid:PMC2522333

LeDoux J. The emotional brain, fear, and the amygdala. Cellular and molecular neurobiology. 2003;23(4-5):727-38.

https://doi.org/10.1023/A:1025048802629

PMid:14514027

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.

https://doi.org/10.1016/j.cub.2016.02.063

PMid:27112296 PMCid:PMC4864126

Ocklenburg S, Korte SM, Peterburs J, Wolf OT, Güntürkün O. Stress and laterality–The comparative perspective. Physiology & behavior. 2016;164:321-9.

https://doi.org/10.1016/j.physbeh.2016.06.020

PMid:27321757

Refbacks

  • There are currently no refbacks.