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Citations to this article

Hypoglycemic neuronal death is triggered by glucose reperfusion and activation of neuronal NADPH oxidase
Sang Won Suh, … , Pak H. Chan, Raymond A. Swanson
Sang Won Suh, … , Pak H. Chan, Raymond A. Swanson
Published April 2, 2007
Citation Information: J Clin Invest. 2007;117(4):910-918. https://doi.org/10.1172/JCI30077.
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Hypoglycemic neuronal death is triggered by glucose reperfusion and activation of neuronal NADPH oxidase

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Abstract

Hypoglycemic coma and brain injury are potential complications of insulin therapy. Certain neurons in the hippocampus and cerebral cortex are uniquely vulnerable to hypoglycemic cell death, and oxidative stress is a key event in this cell death process. Here we show that hypoglycemia-induced oxidative stress and neuronal death are attributable primarily to the activation of neuronal NADPH oxidase during glucose reperfusion. Superoxide production and neuronal death were blocked by the NADPH oxidase inhibitor apocynin in both cell culture and in vivo models of insulin-induced hypoglycemia. Superoxide production and neuronal death were also blocked in studies using mice or cultured neurons deficient in the p47phox subunit of NADPH oxidase. Chelation of zinc with calcium disodium EDTA blocked both the assembly of the neuronal NADPH oxidase complex and superoxide production. Inhibition of the hexose monophosphate shunt, which utilizes glucose to regenerate NADPH, also prevented superoxide formation and neuronal death, suggesting a mechanism linking glucose reperfusion to superoxide formation. Moreover, the degree of superoxide production and neuronal death increased with increasing glucose concentrations during the reperfusion period. These results suggest that high blood glucose concentrations following hypoglycemic coma can initiate neuronal death by a mechanism involving extracellular zinc release and activation of neuronal NADPH oxidase.

Authors

Sang Won Suh, Elizabeth T. Gum, Aaron M. Hamby, Pak H. Chan, Raymond A. Swanson

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Critical illness-induced dysglycemia and the brain
R Sonneville, I Vanhorebeek, HM Hertog, F Chrétien, D Annane, T Sharshar, GV Berghe
Intensive Care Medicine 2014
Mitochondrial Dysfunction Induced by Nuclear Poly(ADP-Ribose) Polymerase-1: a Treatable Cause of Cell Death in Stroke
P Baxter, Y Chen, Y Xu, RA Swanson
Translational Stroke Research 2013
Antecedent glycemic control reduces severe hypoglycemia-induced neuronal damage in diabetic rats
CM Reno, T Tanoli, A Bree, D Daphna-Iken, C Cui, SE Maloney, DF Wozniak, SJ Fisher
American journal of physiology. Endocrinology and metabolism 2013
Impairment of autophagic flux promotes glucose reperfusion-induced neuro2A cell death after glucose deprivation
BG Jang, BY Choi, JH Kim, MJ Kim, M Sohn, SW Suh
PloS one 2013
Vitamin C further improves the protective effect of GLP-1 on the ischemia-reperfusion-like effect induced by hyperglycemia post-hypoglycemia in type 1 diabetes
A Ceriello, A Novials, E Ortega, S Canivell, G Pujadas, LL Sala, L Bucciarelli, M Rondinelli, S Genovese
Cardiovascular Diabetology 2013
Severe hypoglycemia in a juvenile diabetic rat model: presence and severity of seizures are associated with mortality
M Maheandiran, S Mylvaganam, C Wu, Y El-Hayek, S Sugumar, L Hazrati, M Campo, A Giacca, L Zhang, PL Carlen
PloS one 2013
Pyruvate administration reduces recurrent/moderate hypoglycemia-induced cortical neuron death in diabetic rats
BY Choi, JH Kim, HJ Kim, JH Yoo, HK Song, M Sohn, SJ Won, SW Suh
PloS one 2013
Recurrent/moderate hypoglycemia induces hippocampal dendritic injury, microglial activation, and cognitive impairment in diabetic rats
SJ Won, BH Yoo, TM Kauppinen, BY Choi, JH Kim, BG Jang, MW Lee, M Sohn, J Liu, RA Swanson, SW Suh
Journal of Neuroinflammation 2012
NADPH oxidases as therapeutic targets in ischemic stroke
T Kahles, RP Brandes
Cellular and Molecular Life Sciences 2012
Prevention of acute/severe hypoglycemia-induced neuron death by lactate administration
SJ Won, BG Jang, BH Yoo, M Sohn, MW Lee, BY Choi, JH Kim, HK Song, SW Suh
Journal of Cerebral Blood Flow & Metabolism 2012
Regulation of NADPH Oxidase Gene Expression with PKA and Cytokine IL-4 in Neurons and Microglia
VL Savchenko
Neurotoxicity Research 2012
Hypoglycemia and Death in Mice Following Experimental Exposure to an Extract of Trogia venenata Mushrooms
GQ Shi, J He, T Shen, RE Fontaine, L Yang, ZY Zhou, H Gao, YF Xu, C Qin, ZL Yang, JK Liu, WL Huang, G Zeng
PloS one 2012
Targeting NOX enzymes in the central nervous system: therapeutic opportunities
S Sorce, KH Krause, V Jaquet
Cellular and Molecular Life Sciences 2012
The 1027th target candidate in stroke: Will NADPH oxidase hold up?
KA Radermacher, K Wingler, P Kleikers, S Altenhöfer, JJ Hermans, C Kleinschnitz, HH Schmidt
Experimental & translational stroke medicine 2012
Impact of Hypoglycemia in Hospitalized Patients
M Carey, L Boucai, J Zonszein
Current Diabetes Reports 2012
Prevention of hypoglycemia-induced neuronal death by minocycline
SJ Won, JH Kim, BH Yoo, M Sohn, TM Kauppinen, MS Park, HJ Kwon, J Liu, SW Suh
Journal of Neuroinflammation 2012
Prevention of traumatic brain injury-induced neuron death by intranasal delivery of nicotinamide adenine dinucleotide
SJ Won, BY Choi, BH Yoo, M Sohn, W Ying, RA Swanson, SW Suh
Journal of Neurotrauma 2012
Evidence that hyperglycemia after recovery from hypoglycemia worsens endothelial function and increases oxidative stress and inflammation in healthy control subjects and subjects with type 1 diabetes
A Ceriello, A Novials, E Ortega, LL Sala, G Pujadas, R Testa, AR Bonfigli, K Esposito, D Giugliano
Diabetes 2012
Activation of neuronal NMDA receptors induces superoxide-mediated oxidative stress in neighboring neurons and astrocytes
RC Reyes, AM Brennan, Y Shen, Y Baldwin, RA Swanson
The Journal of neuroscience : the official journal of the Society for Neuroscience 2012
The neuroprotective effects of apocynin
Simonyi A, Serfozo P, Lehmidi TM, Cui J, Gu Z, Lubahn DB, Sun AY, Sun GY
Frontiers in bioscience (Elite edition) 2012
Prediction and Prevention of Treatment-Related Inpatient Hypoglycemia
Elliott MB, Schafers SJ, McGill JB, Tobin GS
Journal of diabetes science and technology 2012
Glycemic Control in the Pediatric Intensive Care Unit of Leuven: Two Years of Experience
Van Herpe T, Vanhonsebrouck K, Mesotten D, De Moor B, Van den Berghe G
Journal of diabetes science and technology 2012
Acute hypoglycemia induces retinal cell death in mouse
M Emery, DF Schorderet, R Roduit
PloS one 2011
Insight into glutamate excitotoxicity from synaptic zinc homeostasis
A Takeda
International Journal of Alzheimer's Disease 2011
Dynamic optical imaging of metabolic and NADPH oxidase-derived superoxide in live mouse brain using fluorescence lifetime unmixing
DJ Hall, SH Han, A Chepetan, EG Inui, M Rogers, LL Dugan
Journal of Cerebral Blood Flow & Metabolism 2011
Oxidative Stress in Ischemic Brain Damage: Mechanisms of Cell Death and Potential Molecular Targets for Neuroprotection
H Chen, H Yoshioka, GS Kim, JE Jung, N Okami, H Sakata, CM Maier, P Narasimhan, CE Goeders, PH Chan
Antioxidants & Redox Signaling 2011
Hyperglycemia promotes tissue plasminogen activator-induced hemorrhage by Increasing superoxide production
SJ Won, XN Tang, SW Suh, MA Yenari, RA Swanson
Annals of Neurology 2011
Pharmacologic amelioration of Severe Hypoglycemia-induced Neuronal Damage
JM Silverstein, D Musikantow, EC Puente, D Daphna-Iken, AJ Bree, SJ Fisher
Neuroscience Letters 2011
Hypoglycemia in critically ill adults--association yes, causation not proven
S Finfer
Critical Care 2011
Phosphatidylinositol-3-Kinase Gamma Plays a Central Role in Blood–Brain Barrier Dysfunction in Acute Experimental Stroke
R Jin, Z Song, S Yu, A Piazza, A Nanda, JM Penninger, DN Granger, G Li
Stroke; a journal of cerebral circulation 2011
Pyruvate administered to newborn rats with insulin-induced hypoglycemic brain injury reduces neuronal death and cognitive impairment.
Zhou D, Qian J, Chang H, Xi B, Sun RP
European Journal of Pediatrics 2011
Recurrent moderate hypoglycemia ameliorates brain damage and cognitive dysfunction induced by severe hypoglycemia
EC Puente, J Silverstein, AJ Bree, DR Musikantow, DF Wozniak, S Maloney, D Daphna-Iken, SJ Fisher
Diabetes 2010
Bench-to-bedside review: Glucose and stress conditions in the intensive care unit
MR Losser, C Damoisel, D Payen
Critical Care 2010
Clinical review: Strict or loose glycemic control in critically ill patients--implementing best available evidence from randomized controlled trials
MJ Schultz, RE Harmsen, PE Spronk
Critical Care 2010
Hypoglycemia induced changes in cholinergic receptor expression in the cerebellum of diabetic rats
S Antony, TP Kumar, J Mathew, TR Anju, CS Paulose
Journal of Biomedical Science 2010
Mini-review: impact of recurrent hypoglycemia on cognitive and brain function
EC McNay, VE Cotero
Physiology & Behavior 2010
Use of NAD(P)H and flavoprotein autofluorescence transients to probe neuron and astrocyte responses to synaptic activation
CW Shuttleworth
Neurochemistry International 2010
Serum or Target Deprivation Induced Neuronal Death Cause Oxidative Neuronal Accumulation of Zn2+ and Loss of NAD+
CT Sheline, AL Cai, J Zhu, C Shi
The European journal of neuroscience 2010
EAAC1 Gene Deletion Alters Zinc Homeostasis and Exacerbates Neuronal Injury after Transient Cerebral Ischemia
SJ Won, BH Yoo, AM Brennan, BS Shin, TM Kauppinen, AE Berman, RA Swanson, SW Suh
The Journal of neuroscience : the official journal of the Society for Neuroscience 2010
International recommendations for glucose control in adult non diabetic critically ill patients
C Ichai, JC Preiser
Critical Care 2010
Chronic social isolation compromises the activity of both glutathione peroxidase and catalase in hippocampus of male wistar rats.
Djordjevic J, Djordjevic A, Adzic M, Radojcic MB
Cellular and Molecular Neurobiology 2010
Zinc signaling in the hippocampus and its relation to pathogenesis of depression.
Takeda A
Molecular Neurobiology 2010
NADPH oxidase is the primary source of superoxide induced by NMDA receptor activation
AM Brennan, SW Suh, SJ Won, P Narasimhan, TM Kauppinen, H Lee, Y Edling, PH Chan, RA Swanson
Nature Neuroscience 2009
Inhibition of NADPH oxidase is neuroprotective after ischemia-reperfusion
H Chen, YS Song, PH Chan
Journal of Cerebral Blood Flow & Metabolism 2009
Optimum serum glucose levels for patients with severe traumatic brain injury
DW Marion
F1000 medicine reports 2009
Hypoglycemia aggravates critical illness-induced neurocognitive dysfunction
T Duning, I Heuvel, A Dickmann, T Volkert, C Wempe, J Reinholz, H Lohmann, H Freise, B Ellger
Diabetes care 2009
Prevention of hypoglycemia-induced neuronal death by hypothermia
BS Shin, SJ Won, BH Yoo, TM Kauppinen, SW Suh
Journal of Cerebral Blood Flow & Metabolism 2009
Postnatal age influences hypoglycemia-induced poly(ADP-ribose) polymerase-1 activation in the brain regions of rats
R Rao, D Sperr, K Ennis, P Tran
Pediatric Research 2009
Diabetes increases brain damage caused by severe hypoglycemia
AJ Bree, EC Puente, D Daphna-Iken, SJ Fisher
American journal of physiology. Endocrinology and metabolism 2009
Cocaine and human immunodeficiency virus type 1 gp120 mediate neurotoxicity through overlapping signaling pathways
H Yao, JE Allen, X Zhu, S Callen, S Buch
Journal of Neurovirology 2009
An Overview of Hypoglycemia in the Critically Ill
Lacherade JC, Jacqueminet S, Preiser JC
Journal of diabetes science and technology 2009
Regulation of apoptotic and inflammatory cell signaling in cerebral ischemia: the complex roles of heat shock protein 70
RG Giffard, RQ Han, JF Emery, M Duan, JF Pittet
Anesthesiology 2008
Is "safe effective glucose control" effective and safe?
MJ Schultz, GV Berghe
Critical Care 2008
Levofloxacin-associated hypoglycaemia complicated by pontine myelinolysis and quadriplegia
S Vallurupalli, G Huesmann, J Gregory, MG 4th
Diabetic medicine : a journal of the British Diabetic Association 2008
Postnatal age influences hypoglycemia-induced neuronal injury in the rat brain
K Ennis, PV Tran, ER Seaquist, R Rao
Brain Research 2008
Zinc triggers microglial activation
TM Kauppinen, Y Higashi, SW Suh, C Escartin, K Nagasawa, RA Swanson
The Journal of neuroscience : the official journal of the Society for Neuroscience 2008
Glucose and NADPH oxidase drive neuronal superoxide formation in stroke
SW Suh, BS Shin, H Ma, MV Hoecke, AM Brennan, MA Yenari, RA Swanson
Annals of Neurology 2008
Glycemic Control and Hypoglycemia: Is the loser the winner?
LC Perlmuter, BP Flanagan, PH Shah, SP Singh
Diabetes care 2008
Hypoglycemia, functional brain failure, and brain death
Philip E. Cryer
Journal of Clinical Investigation 2007
Enhanced [3H] glutamate binding in the cerebellum of insulin-induced hypoglycaemic and streptozotocin-induced diabetic rats.
Joseph A, Robinson R, Paulose CS
Cellular and Molecular Neurobiology 2007

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