Chronic insulinopenia/hyperglycemia decreases cannabinoid CB1 receptor density and impairs glucose uptake in the mouse forebrain

Abdul-Ghani, 2007, Effect of insulin on 3H-deoxy-glucose uptake into brain slices and synaptosomal preparations from different brain regions, Eur. J. Sci. Res., 18, 532 Araya, 2007, Role of cannabinoid CB1 receptors and Gi/o protein activation in the modulation of synaptosomal Na+,K+-ATPase activity by WIN55,212-2 and delta(9)-THC, Eur. J. Pharmacol., 572, 32, 10.1016/j.ejphar.2007.06.013 Astrup, 1981, Oxygen and glucose consumption related to Na+-K+ transport in canine brain, Stroke, 12, 726, 10.1161/01.STR.12.6.726 Attwell, 2001, An energy budget for signaling in the grey matter of the brain, J. Cereb. Blood Flow Metab., 21, 1133, 10.1097/00004647-200110000-00001 Bakirtzi, 2009, Cerebellar neurons possess a vesicular compartment structurally and functionally similar to Glut4-storage vesicles from peripheral insulin-sensitive tissues, J. Neurosci., 29, 5193, 10.1523/JNEUROSCI.0858-09.2009 Baptista, 2011, Diabetes induces early transient changes in the content of vesicular transporters and no major effects in neurotransmitter release in hippocampus and retina, Brain Res., 1383, 257, 10.1016/j.brainres.2011.01.071 Baydas, 2003, Altered expression of NCAM in hippocampus and cortex may underlie memory and learning deficits in rats with streptozotocin-induced diabetes mellitus, Life Sci., 73, 1907, 10.1016/S0024-3205(03)00561-7 Bénard, 2012, Mitochondrial CB1 receptors regulate neuronal energy metabolism, Nat. Neurosci., 15, 558, 10.1038/nn.3053 Bermúdez-Silva, 2016, The cannabinoid CB1 receptor and mTORC1 signalling pathways interact to modulate glucose homeostasis in mice, Dis Model Mech., 9, 51, 10.1242/dmm.020750 Blázquez, 1999, The stimulation of ketogenesis by cannabinoids in cultured astrocytes defines carnitine palmitoyltransferase I as a new ceramide-activated enzyme, J. Neurochem., 72, 1759, 10.1046/j.1471-4159.1999.721759.x Bouaboula, 1997, ). A selective inverse agonist for central cannabinoid receptor inhibits mitogen-activated protein kinase activation stimulated by insulin or insulin-like growth factor 1. Evidence for a new model of receptor/ligand interactions, J. Biol. Chem., 272, 22330, 10.1074/jbc.272.35.22330 Brands, 2004, Cerebral dysfunction in type 1 diabetes: effects of insulin, vascular risk factors and blood-glucose levels, Eur. J. Pharmacol., 490, 159, 10.1016/j.ejphar.2004.02.053 Callén, 2012, Cannabinoid receptors CB1 and CB2 form functional heteromers in brain, J. Biol. Chem., 287, 20851, 10.1074/jbc.M111.335273 Catanzaro, 2013, Bradykinin B₁ antagonism inhibits oxidative stress and restores Na+K+ ATPase activity in diabetic rat peripheral nervous system, Peptides, 44, 100, 10.1016/j.peptides.2013.01.019 Chen, 2009, Upregulation of myostatin gene expression in streptozotocin-induced type 1 diabetes mice is attenuated by insulin, Biochem. Biophys. Res. Commun., 388, 112, 10.1016/j.bbrc.2009.07.129 Chenal, 2008, Insulin and IGF-1 enhance the expression of the neuronal monocarboxylate transporter MCT2 by translational activation via stimulation of the phosphoinositide 3-kinase-Akt-mammalian target of rapamycin pathway, Eur. J. Neurosci., 27, 53, 10.1111/j.1460-9568.2007.05981.x Clarke, 1999, Circulation and Energy Metabolism of the Brain, 637 Clarke, 1984, Insulin binds to specific receptors and stimulates 2-deoxy-D-glucose uptake in cultured glial cells from rat brain, J. Biol. Chem., 259, 11672, 10.1016/S0021-9258(20)71260-3 Cota, 2003, The endogenous cannabinoid system affects energy balance via central orexigenic drive and peripheral lipogenesis, J. Clin. Invest., 112, 423, 10.1172/JCI17725 Cranston, 2001, Changes in regional brain (18)F-fluorodeoxyglucose uptake at hypoglycemia in type 1 diabetic men associated with hypoglycemia unawareness and counter-regulatory failure, Diabetes, 50, 2329, 10.2337/diabetes.50.10.2329 Curtis, 2015, Experimental design and analysis and their reporting: new guidance for publication in BJP, Br. J. Pharmacol., 172, 3461, 10.1111/bph.12856 Dalton, 2012, Cannabinoid CB1 receptors transactivate multiple receptor tyrosine kinases and regulate serine/threonine kinases to activate ERK in neuronal cells, Br. J. Pharmacol., 165, 2497, 10.1111/j.1476-5381.2011.01455.x de Ceballos, 2017, Boosting brain glucose metabolism to fight neurodegeneration?, Oncotarget, 8, 14273, 10.18632/oncotarget.15131 de Morais, 2016, Anandamide reverses depressive-like behavior, neurochemical abnormalities and oxidative-stress parameters in streptozotocin-diabetic rats: Role of CB1 receptors, Eur. Neuropsychopharmacol., 26, 1590, 10.1016/j.euroneuro.2016.08.007 Di Marzo, 2011, Cannabinoids and Endocannabinoids in Metabolic Disorders with Focus on Diabetes, 75 Díaz-Asensio, 2008, Type 1 diabetes alters brain cannabinoid receptor expression and phosphorylation status in rats, Horm. Metab. Res., 40, 454, 10.1055/s-2008-1065323 Detka, 2013, Neuroendocrine link between stress, depression and diabetes, Pharmacol. Rep., 65, 1591, 10.1016/S1734-1140(13)71520-2 Duarte, 2015, Metabolic Alterations Associated to Brain Dysfunction in Diabetes, Aging Dis, 6, 304, 10.14336/AD.2014.1104 Duarte, 2012, CB1 receptor activation inhibits neuronal and astrocytic intermediary metabolism in the rat hippocampus, Neurochem. Int., 60, 1, 10.1016/j.neuint.2011.10.019 Duarte, 2007, Increase of cannabinoid CB1 receptor density in the hippocampus of streptozotocin-induced diabetic rats, Exp. Neurol., 204, 479, 10.1016/j.expneurol.2006.11.013 Elahi, 2016, Region-Specific Vulnerability to Oxidative Stress, Neuroinflammation, and Tau Hyperphosphorylation in Experimental Diabetes Mellitus Mice, J. Alzheimers Dis., 51, 1209, 10.3233/JAD-150820 Ghasemi, 2013, Insulin in the brain: sources, localization and functions, Mol. Neurobiol., 47, 145, 10.1007/s12035-012-8339-9 Greene, 1983, Impaired rat sciatic nerve sodium-potassium adenosine triphosphatase in acute streptozocin diabetes and its correction by dietary myo-inositol supplementation, J. Clin. Invest., 72, 1058, 10.1172/JCI111030 Guven, 2009, Central nervous system complications of diabetes in streptozotocin-induced diabetic rats: a histopathological and immunohistochemical examination, Int. J. Neurosci., 119, 1155, 10.1080/00207450902841723 Harkany, 2017, (S)Pot on Mitochondria: Cannabinoids Disrupt Cellular Respiration to Limit Neuronal Activity, Cell Metab., 25, 8, 10.1016/j.cmet.2016.12.020 Hatou, 2010, Role of insulin in regulation of Na+-/K+-dependent ATPase activity and pump function in corneal endothelial cells, Invest. Ophthalmol. Vis. Sci., 51, 3935, 10.1167/iovs.09-4027 Havrankova, 1979, Concentrations of insulin and insulin receptors in the brain are independent of peripheral insulin levels. Studies of obese and streptozotocin-treated rodents, J. Clin. Invest., 64, 636, 10.1172/JCI109504 Hawkins, 1986, Regional ketone body utilization by rat brain in starvation and diabetes, Am. J. Physiol., 250, 169 Jakobsen, 1987, Cation permeability of the blood-brain barrier in streptozotocin-diabetic rats, Diabetologia, 30, 409, 10.1007/BF00292543 Jakobsen, 1990, Regional brain glucose metabolism and blood flow in streptozocin-induced diabetic rats, Diabetes, 39, 437, 10.2337/diab.39.4.437 Jourdan, 2017, Decreasing CB1 receptor signaling in Kupffer cells improves insulin sensitivity in obese mice, Mol. Metab., 6, 1517, 10.1016/j.molmet.2017.08.011 Kilkenny, 2010, Animal research: reporting in vivo experiments: the ARRIVE guidelines, Br. J. Pharmacol., 160, 1577, 10.1111/j.1476-5381.2010.00872.x Kim, 2012, Cannabinoids induce pancreatic β-cell death by directly inhibiting insulin receptor activation, Sci. Signal., 5, ra23, 10.1126/scisignal.2002519 Köfalvi, 2016, Stimulation of brain glucose uptake by cannabinoid CB2 receptors and its therapeutic potential in Alzheimer’s disease, Neuropharmacology, 110, 519, 10.1016/j.neuropharm.2016.03.015 Labouèbe, 2013, Insulin induces long-term depression of ventral tegmental area dopamine neurons via endocannabinoids, Nat. Neurosci., 16, 300, 10.1038/nn.3321 Ledent, 1999, Unresponsiveness to cannabinoids and reduced addictive effects of opiates in CB1 receptor knockout mice, Science, 283, 401, 10.1126/science.283.5400.401 Lemos, 2012, Impaired hippocampal glucoregulation in the cannabinoid CB1 receptor knockout mice as revealed by an optimized in vitro experimental approach, J. Neurosci. Methods, 204, 366, 10.1016/j.jneumeth.2011.11.028 Marco, 2009, The critical role of the endocannabinoid system in emotional homeostasis: avoiding excess and deficiencies, Mini Rev. Med. Chem., 9, 1407, 10.2174/138955709789957468 Matias, 2008, Endocannabinoids in Energy Homeostasis and Metabolic Disorders, 277 McGrath, 2010, Guidelines for reporting experiments involving animals: the ARRIVE guidelines, Br. J. Pharmacol., 160, 1573, 10.1111/j.1476-5381.2010.00873.x Miles, 1922, Psychologic tests applied to diabetic patients, Arch. Intern. Med. (Chic.), 30, 767, 10.1001/archinte.1922.00110120086003 Molnár, 2014, GABAergic neurogliaform cells represent local sources of insulin in the cerebral cortex, J. Neurosci., 34, 1133, 10.1523/JNEUROSCI.4082-13.2014 Mooradian, 1991, Brain uptake of glucose in diabetes mellitus: the role of glucose transporters, Am. J. Med. Sci., 301, 173, 10.1097/00000441-199103000-00004 Moura, 2014, Neurotensin-loaded collagen dressings reduce inflammation and improve wound healing in diabetic mice, Biochim. Biophys. Acta, 1842, 32, 10.1016/j.bbadis.2013.10.009 Pearson-Leary, 2018, Insulin modulates hippocampally-mediated spatial working memory via glucose transporter-4, Behav. Brain Res., 338, 32, 10.1016/j.bbr.2017.09.033 Piazza, 2017, The CB1 Receptor as the Cornerstone of Exostasis, Neuron, 93, 1252, 10.1016/j.neuron.2017.02.002 Pillion, 1988, Paradoxical organ-specific adaptations to streptozotocin diabetes mellitus in adult rats, Am. J. Physiol., 254, 749 Pinheiro, 2016, Hierarchical glucocorticoid-endocannabinoid interplay regulates the activation of the nucleus accumbens by insulin, Brain Res. Bull., 124, 222, 10.1016/j.brainresbull.2016.05.009 Price, 1996, Muscle wasting in insulinopenic rats results from activation of the ATP-dependent, ubiquitin-proteasome proteolytic pathway by a mechanism including gene transcription, J. Clin. Invest., 98, 1703, 10.1172/JCI118968 Ramana, 2005, Requirement of aldose reductase for the hyperglycemic activation of protein kinase C and formation of diacylglycerol in vascular smooth muscle cells, Diabetes, 54, 818, 10.2337/diabetes.54.3.818 Ravinet Trillou, 2004, CB1 cannabinoid receptor knockout in mice leads to leanness, resistance to diet-induced obesity and enhanced leptin sensitivity, Int. J. Obes. Relat. Metab. Disord., 28, 640, 10.1038/sj.ijo.0802583 Reske-Nielsen, 1966, Pathological changes in the central and peripheral nervous system of young long-term diabetics : I. Diabetic encephalopathy, Diabetologia, 1, 233, 10.1007/BF01257917 Rossini, 1977, Studies of streptozotocin-induced insulitis and diabetes, Proc. Natl. Acad. Sci. U.S.A., 74, 2485, 10.1073/pnas.74.6.2485 Ruderman, 1974, Regulation of glucose and ketone-body metabolism in brain of anaesthetized rats, Biochem. J., 138, 1, 10.1042/bj1380001 Sidibeh, 2017, Role of cannabinoid receptor 1 in human adipose tissue for lipolysis regulation and insulin resistance, Endocrine, 55, 839, 10.1007/s12020-016-1172-6 Sima, 2008, The effects of C-peptide on type 1 diabetic polyneuropathies and encephalopathy in the BB/Wor-rat, Exp. Diabetes. Res., 10.1155/2008/230458 Smith, 1985, Measurement of protein using bicinchoninic acid, Anal. Biochem., 150, 76, 10.1016/0003-2697(85)90442-7 Solymosi, 2017, Cannabis: A Treasure Trove or Pandora’s Box?, Mini Rev. Med. Chem, 17, 1223, 10.2174/1389557516666161004162133 Stranahan, 2008, Diabetes impairs hippocampal function through glucocorticoid-mediated effects on new and mature neurons, Nat. Neurosci., 11, 309, 10.1038/nn2055 Uemura, 2006, Insulin regulates neuronal glucose uptake by promoting translocation of glucose transporter GLUT3, Exp. Neurol., 198, 48, 10.1016/j.expneurol.2005.10.035 Valente-Silva, 2015, Ketone bodies effectively compete with glucose for neuronal acetyl-CoA generation in rat hippocampal slices, NMR Biomed, 28, 1111, 10.1002/nbm.3355 Végh, 2017, Effects of articaine on [3H]noradrenaline release from cortical and spinal cord slices prepared from normal and streptozotocin-induced diabetic rats and compared to lidocaine, Brain Res. Bull., 135, 157, 10.1016/j.brainresbull.2017.10.011 Zhang, 2007, Expression of cannabinoid CB1 receptors in models of diabetic neuropathy, J. Pharmacol. Exp. Ther., 323, 508, 10.1124/jpet.107.128272 Zilberter, 2017, The vicious circle of hypometabolism in neurodegenerative diseases: Ways and mechanisms of metabolic correction, J. Neurosci. Res., 95, 2217, 10.1002/jnr.24064