Astrocyte HIF-2α supports learning in a passive avoidance paradigm under hypoxic stress

References

• Pittman RN. Regulation of Tissue Oxygenation. San Rafael, CA: Morgan & Claypool Life Sciences; 2011.
   Google Scholar
• Bruce AS, Aloia MS, Ancoli-Israel S. Neuropsychological effects of hypoxia in medical disorders. In: Grant I, Adams KM, editors. Neuropsychological Assessment of Neuropsychiatric and Neuromedical Disorders. 3rd ed. Oxford, New York: Oxford University Press; 2009:336–349.
   Google Scholar
• Cannon JA, Moffitt P, Perez-Moreno AC, et al. Cognitive Impairment and Heart Failure: Systematic Review and Meta-Analysis. J Card Fail. 2017;23:464–475.
   PubMed Web of Science ®Google Scholar
• Yohannes AM, Chen W, Moga AM, Leroi I, Connolly MJ. Cognitive Impairment in Chronic Obstructive Pulmonary Disease and Chronic Heart Failure: A Systematic Review and Meta-analysis of Observational Studies. J Am Med Dir Assoc. 2017;18(5):451.e1–451.e11.
   Web of Science ®Google Scholar
• Schega L, Peter B, Törpel A, Mutschler H, Isermann B, Hamacher D. Effects of intermittent hypoxia on cognitive performance and quality of life in elderly adults: a pilot study. Gerontology. 2013;59(4):316–323.
   PubMed Web of Science ®Google Scholar
• Qiu C, Fratiglioni L. A major role for cardiovascular burden in age-related cognitive decline. Nat Rev Cardiol. 2015;12(5):267–277.
   PubMed Web of Science ®Google Scholar
• Popa-Wagner A, Buga A-M, Popescu B, Muresanu D. Vascular cognitive impairment, dementia, aging and energy demand. A vicious cycle. J Neural Transm. 2015;122(S1):47–54.
   Google Scholar
• Lahousse L, Tiemeier H, Ikram MA, Brusselle GG. Chronic obstructive pulmonary disease and cerebrovascular disease: A comprehensive review. Respir Med. 2015;109(11):1371–1380.
   PubMed Web of Science ®Google Scholar
• Daulatzai MA. Evidence of neurodegeneration in obstructive sleep apnea: Relationship between obstructive sleep apnea and cognitive dysfunction in the elderly. J Neurosci Res. 2015;93(12):1778–1794.
   PubMed Web of Science ®Google Scholar
• Bressler J, Knopman DS, Sharrett AR, et al. Incident Heart Failure and Cognitive Decline: The Atherosclerosis Risk in Communities Study. J Card Fail. 2017;23(1):47–55.
   PubMed Web of Science ®Google Scholar
• Suzuki H, Matsumoto Y, Ota H, et al. Hippocampal Blood Flow Abnormality Associated With Depressive Symptoms and Cognitive Impairment in Patients With Chronic Heart Failure. Circ J. 2016;80(8):1773–1780.
   PubMed Web of Science ®Google Scholar
• Kurella Tamura M, Vittinghoff E, Yang J, et al. Anemia and risk for cognitive decline in chronic kidney disease. BMC Nephrol. 2016;17(1):13.
   PubMedGoogle Scholar
• Dlugaj M, Winkler A, Weimar C, et al. Anemia and Mild Cognitive Impairment in the German General Population. J Alzheimers Dis. 2016;49:1031–1042.
   PubMed Web of Science ®Google Scholar
• Schneider ALC, Jonassaint C, Sharrett AR, et al. Hemoglobin, Anemia, and Cognitive Function: The Atherosclerosis Risk in Communities Study. J Gerontol A Biol Sci Med Sci. 2016;71(6):772–779.
   PubMed Web of Science ®Google Scholar
• Weiskopf RB, Kramer JH, Viele M, et al. Acute Severe Isovolemic Anemia Impairs Cognitive Function and Memory in Humans. Anesthesiology. 2000;92(6):1646–1652.
   PubMed Web of Science ®Google Scholar
• Weiskopf RB, Feiner J, Hopf HW, et al. Oxygen Reverses Deficits of Cognitive Function and Memory and Increased Heart Rate Induced by Acute Severe Isovolemic Anemia. Anesthesiology. 2002;96(4):871–877.
   PubMed Web of Science ®Google Scholar
• Hornbein TF. The high-altitude brain. J Exp Biol. 2001;204(Pt 18):3129–3132.
   PubMed Web of Science ®Google Scholar
• Wilson MH, Newman S, Imray CH. The cerebral effects of ascent to high altitudes. Lancet Neurol. 2009;8(2):175–191.
   PubMed Web of Science ®Google Scholar
• Neuhaus C, Hinkelbein J. Cognitive responses to hypobaric hypoxia: implications for aviation training. Psychol Res Behav Manag. 2014;7:297–302.
   PubMedGoogle Scholar
• Malle C, Quinette P, Laisney M, et al. Working Memory Impairment in Pilots Exposed to Acute Hypobaric Hypoxia. Aviat Space Environ Med. 2013;84(8):773–779.
   PubMedGoogle Scholar
• Tran PV, Carlson ES, Fretham SJB, Georgieff MK. Early-Life Iron Deficiency Anemia Alters Neurotrophic Factor Expression and Hippocampal Neuron Differentiation in Male Rats. J Nutr. 2008;138(12):2495–2501.
   PubMed Web of Science ®Google Scholar
• Hennigan A, Callaghan CK, Kealy J, Rouine J, Kelly Áine M.. Deficits in LTP and recognition memory in the genetically hypertensive rat are associated with decreased expression of neurotrophic factors and their receptors in the dentate gyrus. Behav Brain Res. 2009;197(2):371–377.
   PubMed Web of Science ®Google Scholar
• Jänicke B, Schulze G. Influence of normobaric hypoxia on learning capacity of different aged rats. Neurobiol Aging. 1987;8(6):495–500.
   PubMed Web of Science ®Google Scholar
• Li M, Bertout JA, Ratcliffe SJ, Eckenhoff MF, Simon MC, Floyd TF. Acute Anemia Elicits Cognitive Dysfunction and Evidence of Cerebral Cellular Hypoxia in Older Rats with Systemic Hypertension. Anesthesiology. 2010;113(4):845–858.
   PubMed Web of Science ®Google Scholar
• Gozal D, Row BW, Kheirandish L, et al. Increased susceptibility to intermittent hypoxia in aging rats: changes in proteasomal activity, neuronal apoptosis and spatial function. J Neurochem. 2003;86(6):1545–1552.
   PubMed Web of Science ®Google Scholar
• Ingraham JP, Forbes ME, Riddle DR, Sonntag WE. Aging Reduces Hypoxia-Induced Microvascular Growth in the Rodent Hippocampus. J Gerontol A Biol Sci Med Sci. 2008;63(1):12–20.
   PubMed Web of Science ®Google Scholar
• Dunwiddie TV. Age-related differences in the in vitro rat hippocampus. Development of inhibition and the effects of hypoxia. Dev Neurosci. 1981;4:165–175.
   PubMed Web of Science ®Google Scholar
• Larson J, Drew KL, Folkow LP, Milton SL, Park TJ. No oxygen? No problem! Intrinsic brain tolerance to hypoxia in vertebrates. J Exp Biol. 2014;217(7):1024–1039.
   PubMed Web of Science ®Google Scholar
• Wang GL, Jiang BH, Rue EA, Semenza GL. Hypoxia-inducible factor 1 is a basic-helix-loop-helix-PAS heterodimer regulated by cellular O2 tension. Proc Natl Acad Sci U S A. 1995;92(12):5510–5514.
   PubMed Web of Science ®Google Scholar
• Sharp FR, Bergeron M, Bernaudin M. Hypoxia-inducible factor in brain. Adv Exp Med Biol. 2001;502:273–291.
   PubMed Web of Science ®Google Scholar
• Lahiri S, Roy A, Baby SM, Hoshi T, Semenza GL, Prabhakar NR. Oxygen sensing in the body. Prog Biophys Mol Biol. 2006;91(3):249–286.
   PubMed Web of Science ®Google Scholar
• Kaelin WG, Ratcliffe PJ. Oxygen Sensing by Metazoans: The Central Role of the HIF Hydroxylase Pathway. Mol Cell. 2008;30(4):393–402.
   PubMed Web of Science ®Google Scholar
• Prabhakar NR, Semenza GL. Oxygen Sensing and Homeostasis. Physiology (Bethesda). 2015;30:340–348.
   PubMed Web of Science ®Google Scholar
• Mclaren AT, Mazer CD, Zhang H, Liu E, Mok L, Hare GM. A potential role for inducible nitric oxide synthase in the cerebral response to acute hemodilution. Can J Anaesth. 2009;56(7):502–509.
   PubMed Web of Science ®Google Scholar
• Powell FL, Kim BC, Johnson SR, Fu Z. Oxygen sensing in the brain-invited article. Adv Exp Med Biol. 2009;648:369–376.
   PubMed Web of Science ®Google Scholar
• Lamanna JC. Hypoxia in the central nervous system. Essays Biochem. 2007;43:138–152.
   Web of Science ®Google Scholar
• Knabe W, Knerlich F, Washausen S, et al. Expression patterns of erythropoietin and its receptor in the developing midbrain. Anat Embryol. 2004;207(6):503–512.
   PubMedGoogle Scholar
• Schodel J, Oikonomopoulos S, Ragoussis J, Pugh CW, Ratcliffe PJ, Mole DR. High-resolution genome-wide mapping of HIF-binding sites by ChIP-seq. Blood. 2011;117(23):e207–e217.
   PubMed Web of Science ®Google Scholar
• Wenger RH. Mammalian oxygen sensing, signalling and gene regulation. J Exp Biol. 2000;203(Pt 8):1253–1263.
   PubMed Web of Science ®Google Scholar
• Semenza GL. Oxygen Sensing, Hypoxia-Inducible Factors, and Disease Pathophysiology. Annu Rev Pathol. 2014;9(1):47–71.
   PubMedGoogle Scholar
• Rivard A, Berthou-Soulie L, Principe N, et al. Age-dependent defect in vascular endothelial growth factor expression is associated with reduced hypoxia-inducible factor 1 activity. J Biol Chem. 2000;275(38):29643–29647.
   PubMed Web of Science ®Google Scholar
• Chavez JC, Lamanna JC. Hypoxia-inducible factor-1alpha accumulation in the rat brain in response to hypoxia and ischemia is attenuated during aging. Adv Exp Med Biol. 2003;510:337–341.
   PubMed Web of Science ®Google Scholar
• Giulio CD, Bianchi G, Cacchio M, et al. Oxygen and life span: chronic hypoxia as a model for studying HIF-1α, VEGF and NOS during aging. Respir Physiol Neurobiol. 2005;147(1):31–38.
   PubMed Web of Science ®Google Scholar
• Bosch-Marce M, Okuyama H, Wesley JB, et al. Effects of Aging and Hypoxia-Inducible Factor-1 Activity on Angiogenic Cell Mobilization and Recovery of Perfusion After Limb Ischemia. Circ Res. 2007;101(12):1310–1318.
   PubMed Web of Science ®Google Scholar
• Katschinski D. Is there a molecular connection between hypoxia and aging? Exp Gerontol. 2006;41(5):482–484.
   PubMed Web of Science ®Google Scholar
• Ndubuizu OI, Chavez JC, Lamanna JC. Increased prolyl 4-hydroxylase expression and differential regulation of hypoxia-inducible factors in the aged rat brain. Am J Physiol Regul Integr Comp Physiol. 2009;297(1):R158–R165.
   PubMed Web of Science ®Google Scholar
• Rapino C, Bianchi G, di Giulio C, et al. HIF-1alpha cytoplasmic accumulation is associated with cell death in old rat cerebral cortex exposed to intermittent hypoxia. Aging Cell. 2005;4(4):177–185.
   PubMed Web of Science ®Google Scholar
• Frenkel-Denkberg G, Gershon D, Levy AP. The function of hypoxia-inducible factor 1 (HIF-1) is impaired in senescent mice. FEBS Lett. 1999;462(3):341–344.
   PubMed Web of Science ®Google Scholar
• Kim H, Lee D-K, Choi J-W, Kim J-S, Park SC, Youn H-D. Analysis of the effect of aging on the response to hypoxia by cDNA microarray. Mech Ageing Dev. 2003;124(8-9):941–949.
   PubMed Web of Science ®Google Scholar
• Benderro GF, Lamanna JC. Hypoxia-induced angiogenesis is delayed in aging mouse brain. Brain Res. 2011;1389:50–60.
   PubMed Web of Science ®Google Scholar
• Rabie T, Kunze R, Marti HH. Impaired hypoxic response in senescent mouse brain. Int J Dev Neurosci. 2011;29(6):655–661.
   PubMed Web of Science ®Google Scholar
• Anderson J, Sandhir R, Hamilton ES, Berman NEJ. Impaired Expression of Neuroprotective Molecules in the HIF-1α Pathway following Traumatic Brain Injury in Aged Mice. J Neurotrauma. 2009;26(9):1557–1566.
   PubMed Web of Science ®Google Scholar
• Chavez JC, Baranova O, Lin J, Pichiule P. The transcriptional activator hypoxia inducible factor 2 (HIF-2/EPAS-1) regulates the oxygen-dependent expression of erythropoietin in cortical astrocytes. J Neurosci. 2006;26(37):9471–9481.
   PubMed Web of Science ®Google Scholar
• Schousboe A, Sickmann HM, Bak LK, et al. Neuron-glia interactions in glutamatergic neurotransmission: Roles of oxidative and glycolytic adenosine triphosphate as energy source. J Neurosci Res. 2011;89(12):1926–1934.
   PubMed Web of Science ®Google Scholar
• Dienel GA. Astrocytic energetics during excitatory neurotransmission: What are contributions of glutamate oxidation and glycolysis? Neurochem Int. 2013;63(4):244–258.
   PubMed Web of Science ®Google Scholar
• Harris JJ, Jolivet R, Attwell D. Synaptic Energy Use and Supply. Neuron. 2012;75(5):762–777.
   PubMed Web of Science ®Google Scholar
• Lu B, Nagappan G, Lu Y. BDNF and synaptic plasticity, cognitive function, and dysfunction. In: Lewin GR, Carter BD, editors. Neurotrophic Factors. Berlin: Springer. 2014:223–250.
   Google Scholar
• Lum JJ, Bui T, Gruber M, et al. The transcription factor HIF-1 plays a critical role in the growth factor-dependent regulation of both aerobic and anaerobic glycolysis. Genes Dev. 2007;21(9):1037–1049.
   PubMed Web of Science ®Google Scholar
• Jelkmann W. Regulation of erythropoietin production. J Physiol. 2011;589(6):1251–1258.
   PubMed Web of Science ®Google Scholar
• Nakazawa MS, Keith B, Simon MC. Oxygen availability and metabolic adaptations. Nat Rev Cancer. 2016;16(10):663–673.
   PubMed Web of Science ®Google Scholar
• Sardinha VM, Guerra-Gomes S, Caetano I, et al. Astrocytic signaling supports hippocampal-prefrontal theta synchronization and cognitive function. Glia. 2017;65(12):1944–1960.
   PubMed Web of Science ®Google Scholar
• Holthoff K, Witte OW. Directed spatial potassium redistribution in rat neocortex. Glia. 2000;29(3):288–292.
   PubMed Web of Science ®Google Scholar
• Kofuji P, Newman EA. Potassium buffering in the central nervous system. Neuroscience. 2004;129(4):1043–1054.
   Web of Science ®Google Scholar
• Ota Y, Zanetti AT, Hallock RM. The Role of Astrocytes in the Regulation of Synaptic Plasticity and Memory Formation. Neural Plast. 2013;2013(1):11–11.
   Google Scholar
• Allen NJ. Astrocyte Regulation of Synaptic Behavior. Annu Rev Cell Dev Biol. 2014;30(1):439–463.
   PubMedGoogle Scholar
• Christopherson KS, Ullian EM, Stokes CCA, et al. Thrombospondins Are Astrocyte-Secreted Proteins that Promote CNS Synaptogenesis. Cell. 2005;120(3):421–433.
   PubMed Web of Science ®Google Scholar
• Risher WC, Eroglu C. Thrombospondins as key regulators of synaptogenesis in the central nervous system. Matrix Biology. 2012;31(3):170–177.
   PubMed Web of Science ®Google Scholar
• Pannasch U, Vargová L, Reingruber J, et al. Astroglial networks scale synaptic activity and plasticity. Proc Natl Acad Sci U S A. 2011;108(20):8467–8472.
   PubMed Web of Science ®Google Scholar
• Stogsdill JA, Eroglu C. The interplay between neurons and glia in synapse development and plasticity. Curr Opin Neurobiol. 2017;42:1–8.
   PubMed Web of Science ®Google Scholar
• Gruber M, Hu CJ, Johnson RS, Brown EJ, Keith B, Simon MC. Acute postnatal ablation of Hif-2alpha results in anemia. Proc Natl Acad Sci U S A. 2007;104(7):2301–2306.
   PubMed Web of Science ®Google Scholar
• Weidemann A, Kerdiles YM, Knaup KX, et al. The glial cell response is an essential component of hypoxia-induced erythropoiesis in mice. J Clin Invest. 2009;119:3373–3383.
   PubMed Web of Science ®Google Scholar
• Liu R, Suzuki A, Guo Z, Mizuno Y, Urabe T. Intrinsic and extrinsic erythropoietin enhances neuroprotection against ischemia and reperfusion injury in vitro. J Neurochem. 2006;96(4):1101–1110.
   PubMed Web of Science ®Google Scholar
• Petzold GC, Murthy VN. Role of Astrocytes in Neurovascular Coupling. Neuron. 2011;71(5):782–797.
   PubMed Web of Science ®Google Scholar
• Tarantini S, Tran CHT, Gordon GR, Ungvari Z, Csiszar A. Impaired neurovascular coupling in aging and Alzheimer’s disease: Contribution of astrocyte dysfunction and endothelial impairment to cognitive decline. Exp Gerontol. 2017;94:52–58.
   PubMed Web of Science ®Google Scholar
• Wang M, He Y, Sejnowski TJ, Yu X. Brain-state dependent astrocytic Ca2+ signals are coupled to both positive and negative BOLD-fMRI signals. Proc Natl Acad Sci U S A. 2018;115(7):E1647–E1656.
   Google Scholar
• Bolaños JP, Cidad P, Garcı́a-Nogales P, Delgado-Esteban M, Fernández E, Almeida A. Regulation of glucose metabolism by nitrosative stress in neural cells. Mol Aspects Med. 2004;25(1-2):61–73.
   PubMedGoogle Scholar
• Ryan HE, Poloni M, Mcnulty W, et al. Hypoxia-inducible factor-1alpha is a positive factor in solid tumor growth. Cancer Res. 2000;60:4010–4015.
   PubMed Web of Science ®Google Scholar
• Sakr HF. Abbas AM and El Samanoudy AZ. Effect of vitamin E on cerebral cortical oxidative stress and brain-derived neurotrophic factor gene expression induced by hypoxia and exercise in rats. J Physiol Pharmacol. 2015;66:191–202.
   PubMed Web of Science ®Google Scholar
• Bell M, Thake CD, Wolff CB. Effect of inspiration of 12% O2 (Balance N2) on cardiac output, respiration, oxygen saturation, and oxygen delivery. In: LaManna JC, editor. Oxygen Transport to Tissue New York. Vol. (XXXII). Berlin, Germany: Springer; 2011:327–332.
   Google Scholar
• Group TL-TOTTR. A Randomized Trial of Long-Term Oxygen for COPD with Moderate Desaturation. New England Journal of Medicine. 2016;375:1617–1627.
   PubMed Web of Science ®Google Scholar
• Kim C-H. The effects of hypoxia and exercise on physiological and cognitive performance. 2011. Available from: https://etd.ohiolink.edu/pg_10?0::NO:10:P10_ACCESSION_NUM:kent1311015088. Accessed September 05, 2018.
   Google Scholar
• Gray A, Goodacre S, Newby DE, Masson M, Sampson F, Nicholl J. Noninvasive Ventilation in Acute Cardiogenic Pulmonary Edema. N Engl J Med Overseas Ed. 2008;359(2):142–151.
   PubMed Web of Science ®Google Scholar
• Forsythe JA, Jiang BH, Iyer NV, et al. Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor 1. Mol Cell Biol. 1996;16(9):4604–4613.
   PubMed Web of Science ®Google Scholar
• Cable GG. In-flight hypoxia incidents in military aircraft: causes and implications for training. Aviat Space Environ Med. 2003;74:169–172.
   PubMed Web of Science ®Google Scholar
• Stroka DM, Burkhardt T, Desbaillets I, et al. HIF-1 is expressed in normoxic tissue and displays an organ-specific regulation under systemic hypoxia. Faseb J. 2001;15(13):2445–2453.
   PubMed Web of Science ®Google Scholar
• Vogelmeier CF, Criner GJ, Martinez FJ, et al. Global Strategy for the Diagnosis, Management, and Prevention of Chronic Obstructive Lung Disease 2017 Report. GOLD Executive Summary. Am J Respir Crit Care Med. 2017;195(5):557–582.
   Google Scholar
• Cranston JM, Crockett A, Moss J, Alpers JH, Cochrane Airways Group. Domiciliary oxygen for chronic obstructive pulmonary disease. Cochrane Database Syst Rev. 2005;14(5).
   Google Scholar
• Burman MA, Simmons CA, Hughes M, Lei L. Developing and validating trace fear conditioning protocols in C57BL/6 mice. J Neurosci Methods. 2014;222:111–117.
   PubMed Web of Science ®Google Scholar
• Mccarthy KD, de Vellis J. Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J Cell Biol. 1980;85(3):890–902.
   PubMed Web of Science ®Google Scholar
• Olney JW, Tenkova T, Dikranian K, Qin YQ, Labruyere J, Ikonomidou C. Ethanol-induced apoptotic neurodegeneration in the developing C57BL/6 mouse brain. Brain Res Dev Brain Res. 2002;133(2):115–126.
   PubMedGoogle Scholar
• Lamberty Y, Gower AJ. Age-related changes in spontaneous behavior and learning in NMRI mice from maturity to middle age. Physiol Behav. 1990;47(6):1137–1144.
   PubMed Web of Science ®Google Scholar
• Jahn-Eimermacher A, Lasarzik I, Raber J. Statistical analysis of latency outcomes in behavioral experiments. Behav Brain Res. 2011;221(1):271–275.
   PubMed Web of Science ®Google Scholar
• Tomita S, Ueno M, Sakamoto M, et al. Defective Brain Development in Mice Lacking the Hif-1 Gene in Neural Cells. Mol Cell Biol. 2003;23(19):6739–6749.
   PubMed Web of Science ®Google Scholar
• Cy K, Tsai MY, Tseng WF, et al. Integration of CNS survival and differentiation by HIF2alpha. Cell Death Differ. 2011;18:1757–1770.
   PubMed Web of Science ®Google Scholar
• Suzuki A, Stern SA, Bozdagi O, et al. Astrocyte-Neuron Lactate Transport Is Required for Long-Term Memory Formation. Cell. 2011;144(5):810–823.
   PubMed Web of Science ®Google Scholar
• Adamcio B, Sargin D, Stradomska A, et al. Erythropoietin enhances hippocampal long-term potentiation and memory. BMC Biol. 2008;6(1):37.
   PubMedGoogle Scholar
• Ögren SO, Kuteeva E, Elvander-Tottie E, Hökfelt T. Neuropeptides in learning and memory processes with focus on galanin. Eur J Pharmacol. 2010;626(1):9–17.
   PubMed Web of Science ®Google Scholar
• Detrait ER, Hanon E, Dardenne B, Lamberty Y. The inhibitory avoidance test optimized for discovery of cognitive enhancers. Behav Res Methods. 2009;41(3):805–811.
   PubMed Web of Science ®Google Scholar
• Antunes M, Biala G. The novel object recognition memory: neurobiology, test procedure, and its modifications. Cogn Process. 2012;13(2):93–110.
   PubMed Web of Science ®Google Scholar
• Krypotos A-M, Effting M, Kindt M, Beckers T. Avoidance learning: a review of theoretical models and recent developments. Front Behav Neurosci. 2015;9:189.
   PubMed Web of Science ®Google Scholar
• Pinho J, Vale R, Batalha VL, et al. Enhanced LTP in aged rats: Detrimental or compensatory? Neuropharmacology. 2017;114:12–19.
   PubMed Web of Science ®Google Scholar
• Costenla AR, de Mendonça A, Ribeiro JA. Adenosine modulates synaptic plasticity in hippocampal slices from aged rats. Brain Res. 1999; 851(1-2):228–234.
   PubMed Web of Science ®Google Scholar
• Kumar A, Foster TC. Enhanced Long-Term Potentiation During Aging Is Masked by Processes Involving Intracellular Calcium Stores. J Neurophysiol. 2004;91(6):2437–2444.
   PubMed Web of Science ®Google Scholar
• Huang Y-Y, Kandel ER. Age-related enhancement of a protein synthesis-dependent late phase of LTP induced by low frequency paired-pulse stimulation in hippocampus. Learn Mem. 2006;13(3):298–306.
   PubMed Web of Science ®Google Scholar
• Diógenes MJ, Fernandes CC, Sebastião AM, Ribeiro JA. Activation of adenosine A2A receptor facilitates brain-derived neurotrophic factor modulation of synaptic transmission in hippocampal slices. J Neurosci. 2004;24(12):2905–2913.
   PubMed Web of Science ®Google Scholar
• Kuschel A, Simon P, Tug S. Functional regulation of HIF-1α under normoxia-is there more than post-translational regulation? J Cell Physiol. 2012;227(2):514–524.
   PubMed Web of Science ®Google Scholar
• Pagé EL, Chan DA, Giaccia AJ, Levine M, Richard DE. Hypoxia-inducible factor-1alpha stabilization in nonhypoxic conditions: role of oxidation and intracellular ascorbate depletion. Mol Biol Cell. 2008;19(1):86–94.
   PubMed Web of Science ®Google Scholar
• Baek SH, Kim KI. Regulation of HIF-1α stability by lysine methylation. BMB Rep. 2016;49(5):245–246.
   PubMed Web of Science ®Google Scholar
• Mamczur P, Borsuk B, Paszko J, et al. Astrocyte-neuron crosstalk regulates the expression and subcellular localization of carbohydrate metabolism enzymes. Glia. 2015;63(2):328–340.
   PubMed Web of Science ®Google Scholar
• Tsuboi I, Yamashita T, Nagano M, Kimura K, To’a Salazar G, Ohneda O. Impaired expression of HIF-2α induces compensatory expression of HIF-1α for the recovery from anemia. J Cell Physiol. 2015;230(7):1534–1548.
   PubMed Web of Science ®Google Scholar
• Jha MK, Kim JH, Song GJ, et al. Functional dissection of astrocyte-secreted proteins: Implications in brain health and diseases. Prog Neurobiol. 2018;162:37-69.
   PubMed Web of Science ®Google Scholar
• Zhao J, du F, Shen G, Zheng F, Xu B. The role of hypoxia-inducible factor-2 in digestive system cancers. Cell Death Dis. 2015;6:e1600.
   PubMed Web of Science ®Google Scholar
• Holmquist-Mengelbier L, Fredlund E, Löfstedt T, et al. Recruitment of HIF-1alpha and HIF-2alpha to common target genes is differentially regulated in neuroblastoma: HIF-2alpha promotes an aggressive phenotype. Cancer Cell. 2006;10(5):413–423.
   PubMed Web of Science ®Google Scholar
• Filosa JA, Blanco VM. Neurovascular coupling in the mammalian brain. Exp Physiol. 2007;92(4):641–646.
   PubMed Web of Science ®Google Scholar
• Girouard H, Iadecola C. Neurovascular coupling in the normal brain and in hypertension, stroke, and Alzheimer disease. J Appl Physiol. 2006;100(1):328–335.
   PubMed Web of Science ®Google Scholar
• Iadecola C. The Neurovascular Unit Coming of Age: A Journey through Neurovascular Coupling in Health and Disease. Neuron. 2017;96(1):17–42.
   PubMed Web of Science ®Google Scholar
• Perea G, Navarrete M, Araque A. Tripartite synapses: astrocytes process and control synaptic information. Trends Neurosci. 2009;32(8):421–431.
   PubMed Web of Science ®Google Scholar
• Koehler RC, Roman RJ, Harder DR. Astrocytes and the regulation of cerebral blood flow. Trends Neurosci. 2009;32(3):160–169.
   PubMed Web of Science ®Google Scholar
• Marina N, Turovsky E, Christie IN, et al. Brain metabolic sensing and metabolic signaling at the level of an astrocyte. Glia. 2018;66(6):1185-1199.
   PubMed Web of Science ®Google Scholar
• Vallon M, Chang J, Zhang H, Kuo CJ. Developmental and pathological angiogenesis in the central nervous system. Cell Mol Life Sci. 2014;71(18):3489–3506.
   PubMed Web of Science ®Google Scholar
• Jung F, Palmer LA, Zhou N, Johns RA. Hypoxic regulation of inducible nitric oxide synthase via hypoxia inducible factor-1 in cardiac myocytes. Circ Res. 2000;86(3):319–325.
   PubMed Web of Science ®Google Scholar
• Semenza GL, Nejfelt MK, Chi SM, Antonarakis SE. Hypoxia-inducible nuclear factors bind to an enhancer element located 3’ to the human erythropoietin gene. Proceedings of the National Academy of Sciences. 1991;88(13):5680–5684.
   Google Scholar
• Esmaeili Tazangi P, Moosavi SM, Shabani M, Haghani M. Erythropoietin improves synaptic plasticity and memory deficits by decrease of the neurotransmitter release probability in the rat model of Alzheimer’s disease. Pharmacol Biochem Behav. 2015;130:15–21.
   PubMed Web of Science ®Google Scholar
• Dayyat EA, Zhang SX, Wang Y, Cheng ZJ, Gozal D. Exogenous erythropoietin administration attenuates intermittent hypoxia-induced cognitive deficits in a murine model of sleep apnea. BMC Neurosci. 2012;13:77.
   PubMed Web of Science ®Google Scholar
• Al-Qahtani JM, Abdel-Wahab BA, Abd El-Aziz SM. Long-term moderate dose exogenous erythropoietin treatment protects from intermittent hypoxia-induced spatial learning deficits and hippocampal oxidative stress in young rats. Neurochem Res. 2014;39(1):161–171.
   PubMed Web of Science ®Google Scholar
• Viviani B, Bartesaghi S, Corsini E, et al. Erythropoietin protects primary hippocampal neurons increasing the expression of brain-derived neurotrophic factor. J Neurochem. 2005;93(2):412–421.
   PubMed Web of Science ®Google Scholar
• Dzietko M, Felderhoff-Mueser U, Sifringer M, et al. Erythropoietin protects the developing brain against N-methyl-D-aspartate receptor antagonist neurotoxicity. Neurobiol Dis. 2004;15(2):177–187.
   PubMed Web of Science ®Google Scholar
• Mahmood A, Lu D, Qu C, et al. Treatment of traumatic brain injury in rats with erythropoietin and carbamylated erythropoietin. J Neurosurg. 2007;107(2):392–397.
   PubMed Web of Science ®Google Scholar
• Sönmez A, Kabakçi B, Vardar E, et al. Erythropoietin attenuates neuronal injury and potentiates the expression of pCREB in anterior horn after transient spinal cord ischemia in rats. Surg Neurol. 2007;68(3):297–303.
   PubMedGoogle Scholar
• Zhong J, Zhang T, Bloch LM. Dendritic mRNAs encode diversified functionalities in hippocampal pyramidal neurons. BMC Neurosci. 2006;7:17.
   PubMed Web of Science ®Google Scholar
• Haase VH. Regulation of erythropoiesis by hypoxia-inducible factors. Blood Rev. 2013;27(1):41–53.
   PubMed Web of Science ®Google Scholar
• Kapitsinou PP, Liu Q, Unger TL, et al. Hepatic HIF-2 regulates erythropoietic responses to hypoxia in renal anemia. Blood. 2010;116(16):3039–3048.
   PubMed Web of Science ®Google Scholar
• Yeo EJ, Cho YS, Kim MS, Park JW. Contribution of HIF-1alpha or HIF-2alpha to erythropoietin expression: in vivo evidence based on chromatin immunoprecipitation. Ann Hematol. 2008;87(1):11–17.
   PubMed Web of Science ®Google Scholar
• Uniacke J, Holterman CE, Lachance G, et al. An oxygen-regulated switch in the protein synthesis machinery. Nature. 2012;486(7401):126–129.
   PubMed Web of Science ®Google Scholar
• Sakers K, Lake AM, Khazanchi R, et al. Astrocytes locally translate transcripts in their peripheral processes. Proc Natl Acad Sci U S A. 2017;114(19):E3830–E3838.
   PubMed Web of Science ®Google Scholar
• Jessen KR, Mirsky R. Nonmyelin-forming Schwann cells coexpress surface proteins and intermediate filaments not found in myelin-forming cells: a study of Ran-2, A5E3 antigen and glial fibrillary acidic protein. J Neurocytol. 1984;13(6):923–934.
   PubMedGoogle Scholar
• Sarthy PV, Fu M. Transcriptional activation of an intermediate filament protein gene in mice with retinal dystrophy. DNA. 1989;8(6):437–446.
   PubMedGoogle Scholar
• Feinstein DL, Weinmaster GA, Milner RJ. Isolation of cDNA clones encoding rat glial fibrillary acidic protein: expression in astrocytes and in Schwann cells. J Neurosci Res. 1992;32(1):1–14.
   PubMed Web of Science ®Google Scholar
• Doetsch F. The glial identity of neural stem cells. Nat Neurosci. 2003;6(11):1127–1134.
   PubMed Web of Science ®Google Scholar
• Casper KB, Jones K, Mccarthy KD. Characterization of astrocyte-specific conditional knockouts. Genesis. 2007;45(5):292–299.
   PubMed Web of Science ®Google Scholar
• Chow LM, Zhang J, Baker SJ. Inducible Cre recombinase activity in mouse mature astrocytes and adult neural precursor cells. Transgenic Res. 2008;17(5):919–928.
   PubMed Web of Science ®Google Scholar
• Bovolenta P, Liem RK, Mason CA. Glial filament protein expression in astroglia in the mouse visual pathway. Brain Res. 1987;430(1):113–126.
   PubMedGoogle Scholar
• Bajenaru ML, Zhu Y, Hedrick NM, Donahoe J, Parada LF, Gutmann DH. Astrocyte-specific inactivation of the neurofibromatosis 1 gene (NF1) is insufficient for astrocytoma formation. Mol Cell Biol. 2002;22(14):5100–5113.
   PubMed Web of Science ®Google Scholar
• Lee Y, Messing A, Su M, Brenner M. GFAP promoter elements required for region-specific and astrocyte-specific expression. Glia. 2008;56(5):481–493.
   PubMed Web of Science ®Google Scholar
• Hirrlinger PG, Scheller A, Braun C, Hirrlinger J, Kirchhoff F. Temporal control of gene recombination in astrocytes by transgenic expression of the tamoxifen-inducible DNA recombinase variant CreERT2. Glia. 2006;54(1):11–20.
   PubMed Web of Science ®Google Scholar