The DOI matches its Crossref record.
Inhibition of mitochondrial respiration by nitric oxide rapidly stimulates cytoprotective GLUT3-mediated glucose uptake through 5′-AMP-activated protein kinase
Abstract
Recently, we have reported that the inhibition of mitochondrial respiration by nitric oxide (NO) leads to an up-regulation of glycolysis and affords cytoprotection against energy failure through the stimulation of AMPK (5′-AMP-activated protein kinase) [Almeida, Moncada and Bolaños (2004) Nat. Cell Biol. 6, 45–51]. To determine whether glucose transport contributes specifically to this effect, we have now investigated the possible role of NO in modulating glucose uptake through GLUT3, a facilitative high-affinity glucose carrier that has been suggested to afford cytoprotection against hypoglycaemic episodes. To do so, GLUT3-lacking HEK-293T cells (human embryonic kidney 293T cells) were transformed to express a plasmid construction encoding green fluorescent protein-tagged GLUT3 cDNA. This carrier was preferentially localized to the plasma membrane, was seen to be functionally active and afforded cytoprotection against low glucose-induced apoptotic death. Inhibition of mitochondrial respiration by NO triggered a rapid, cGMP-independent enhancement of GLUT3-mediated glucose uptake through a mechanism that did not involve transporter translocation. Furthermore, the functional disruption of AMPK by the RNA interference strategy rendered cells unable to respond to NO by activating GLUT3-mediated glucose uptake. These results suggest that the inhibition of mitochondrial respiration by NO activates AMPK to stimulate glucose uptake, thereby representing a novel survival pathway during pathophysiological conditions involving transient reductions in the supply of cellular glucose.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In other cell types or in conditions of overexpression, Glut3 can locate mainly at plasma membranes.
“However, in other cell types or in conditions of overexpression Glut3 can locate mainly at plasma membranes [12,35].”
From Glucose transporter 3 is a rab11-dependent trafficking cargo and its transport to the cell surface is reduced in neurons of CAG140 Huntington’s disease mice (2014) · cites this paper as [35]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
No references could be resolved yet.
Research works printed but not linked: 42
- Maher, 1994, Glucose transporter proteins in brain, FASEB J., 8, 1003, 10.1096/fasebj.8.13.7926364 · DOI
- Maher, 1996, Substrate specificity and kinetic parameters of GLUT3 in rat cerebellar granule neurons, Biochem. J., 315, 827, 10.1042/bj3150827 · DOI
- Burant, 1992, Mammalian facilitative glucose transporters: evidence for similar substrate recognition sites in functionally monomeric proteins, Biochemistry, 31, 10414, 10.1021/bi00157a032 · DOI
- Gerhart, 1992, Neurons and microvessels express the brain glucose transporter protein GLUT3, Proc. Natl. Acad. Sci. U.S.A., 89, 733, 10.1073/pnas.89.2.733 · DOI
- Gould, 1997, Introduction to the facilitative glucose transporter family, 1
- Fattoretti, 2001, Quantitative immunohistochemistry of glucose transport protein (Glut3) expression in the rat hippocampus during aging, J. Histochem. Cytochem., 49, 671, 10.1177/002215540104900518 · DOI · Paper page
- Hara, 1989, Characteristics of glucose transport in neuronal cells and astrocytes from rat brain in primary culture, J. Neurochem., 52, 902, 10.1111/j.1471-4159.1989.tb02540.x · DOI
- Cidad, 2001, Expression of glucose transporter GLUT3 by endotoxin in cultured rat astrocytes: the role of nitric oxide, J. Neurochem., 79, 17, 10.1046/j.1471-4159.2001.00523.x · DOI
- Maher, 1995, Immunolocalization of GLUT1 and GLUT3 glucose transporters in primary cultured neurons and glia, J. Neurosci. Res., 42, 459, 10.1002/jnr.490420404 · DOI
- Galea, 1992, Induction of calcium-independent nitric oxide synthase activity in primary rat glial cultures, Proc. Natl. Acad. Sci. U.S.A., 89, 10945, 10.1073/pnas.89.22.10945 · DOI
- Simmons, 1992, Induction of nitric oxide synthase in glial cells, J. Neurochem., 59, 897, 10.1111/j.1471-4159.1992.tb08328.x · DOI
- Endoh, 1994, Expression of the inducible form of nitric oxide synthase by reactive astrocytes after transient global ischemia, Brain Res., 651, 92, 10.1016/0006-8993(94)90683-1 · DOI
- Moro, 1998, Neuronal expression of inducible nitric oxide synthase after oxygen and glucose deprivation in rat forebrain slices, Eur. J. Neurosci., 10, 445, 10.1046/j.1460-9568.1998.00028.x · DOI
- Iadecola, 1997, Bright and dark sides of nitric oxide in ischemic brain injury, Trends Neurosci., 20, 132, 10.1016/S0166-2236(96)10074-6 · DOI
- Etgen, 1997, Nitric oxide stimulates skeletal muscle glucose transport through a calcium/contraction- and phosphatidylinositol-3-kinase-independent pathway, Diabetes, 46, 1915, 10.2337/diab.46.11.1915 · DOI
- Roberts, 1997, Exercise-stimulated glucose transport in skeletal muscle is nitric oxide dependent, Am. J. Physiol., 273, E220
- Fryer, 2000, Activation of glucose transport by AMP-activated protein kinase via stimulation of nitric oxide synthase, Diabetes, 49, 1978, 10.2337/diabetes.49.12.1978 · DOI
- Hardie, 1989, The AMP-activated protein kinase: a multisubstrate regulator of lipid metabolism, Trends Biochem. Sci., 14, 20, 10.1016/0968-0004(89)90084-4 · DOI
- Carling, 2004, The AMP-activated protein kinase cascade – a unifying system for energy control, Trends Biochem. Sci., 29, 18, 10.1016/j.tibs.2003.11.005 · DOI
- Chen, 1999, AMP-activated protein kinase phosphorylation of endothelial NO synthase, FEBS Lett., 443, 285, 10.1016/S0014-5793(98)01705-0 · DOI
- Shi, 1995, Modulation of GLUT1 intrinsic activity in clone 9 cells by inhibition of oxidative phosphorylation, J. Biol. Chem., 270, 21772, 10.1074/jbc.270.37.21772 · DOI
- Abbud, 2000, Stimulation of AMP-activated protein kinase (AMPK) is associated with enhancement of Glut1-mediated glucose transport, Arch. Biochem. Biophys., 380, 347, 10.1006/abbi.2000.1935 · DOI
- Barnes, 2002, Activation of GLUT1 by metabolic and osmotic stress: potential involvement of AMP-activated protein kinase (AMPK), J. Cell Sci., 115, 2433, 10.1242/jcs.115.11.2433 · DOI
- Almeida, 2004, Nitric oxide switches on glycolysis through the AMP protein kinase and 6-phosphofructo-2-kinase pathway, Nat. Cell Biol., 6, 45, 10.1038/ncb1080 · DOI
- Bolaños, 1994, Nitric oxide-mediated inhibition of the mitochondrial respiratory chain in cultured astrocytes, J. Neurochem., 63, 910, 10.1046/j.1471-4159.1994.63030910.x · DOI
- Almeida, 2001, Different responses of astrocytes and neurons to nitric oxide: the role of glycolytically-generated ATP in astrocyte protection, Proc. Natl. Acad. Sci. U.S.A., 98, 15294, 10.1073/pnas.261560998 · DOI · Paper page
- Burkhalter, 2003, Brain-derived neurotrophic factor stimulates energy metabolism in developing cortical neurons, J. Neurosci., 23, 8212, 10.1523/JNEUROSCI.23-23-08212.2003 · DOI
- Brummelkamp, 2002, A system for stable expression of short interfering RNAs in mammalian cells, Science, 296, 550, 10.1126/science.1068999 · DOI
- Sledz, 2003, Activation of the interferon system by short-interfering RNAs, Nat. Cell Biol., 9, 834, 10.1038/ncb1038 · DOI
- Ohtsuka, 2004, ASC is a Bax adaptor and regulates the p53-Bax mitochondrial apoptosis pathway, Nat. Cell Biol., 6, 121, 10.1038/ncb1087 · DOI
- Hobbs, 2003, Antiplatelet properties of a novel, non-NO-based soluble guanylate cyclase activator, BAY 41-2272, Vasc. Pharmacol., 40, 149, 10.1016/S1537-1891(03)00046-6 · DOI
- Brown, 1994, Nanomolar concentrations of nitric oxide reversibly inhibit synaptosomal respiration by competing with oxygen at cytochrome oxidase, FEBS Lett., 356, 295, 10.1016/0014-5793(94)01290-3 · DOI · Paper page
- Jaworek, 1985, Adenosine 5′-diphosphate and adenosine 5′-monophosphate. UV-method, 365
- Lowry, 1951, Protein measurement with the Folin phenol reagent, J. Biol. Chem., 193, 265, 10.1016/S0021-9258(19)52451-6 · DOI
- Suarez, 2001, A novel role of neuregulin in skeletal muscle. Neuregulin stimulates glucose uptake, glucose transporter translocation, and transporter expression in muscle cells, J. Biol. Chem., 276, 18257
- Bradford, 1976, A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding, Anal. Biochem., 72, 248, 10.1016/0003-2697(76)90527-3 · DOI · Paper page
- Cleeter, 1994, Reversible inhibition of cytochrome c oxidase, the terminal enzyme of the mitochondrial respiratory chain, by nitric oxide. Implications for neurodegenerative diseases, FEBS Lett., 345, 50, 10.1016/0014-5793(94)00424-2 · DOI · Paper page
- Schweizer, 1994, Nitric oxide potently and reversibly deenergizes mitochondria at low oxygen tension, Biochem. Biophys. Res. Commun., 204, 169, 10.1006/bbrc.1994.2441 · DOI
- Hara, 1989, Effect of glucose starvation on glucose transport in neuronal cells in primary culture from rat brain, J. Neurochem., 52, 909, 10.1111/j.1471-4159.1989.tb02541.x · DOI
- Lee, 1993, Ischemic injury induces brain glucose transporter gene expression, Endocrinology, 133, 2540, 10.1210/endo.133.6.8243275 · DOI
- Urabe, 1996, Expression of glucose transporters in rat brain following transient focal ischemic injury, J. Neurochem., 67, 265, 10.1046/j.1471-4159.1996.67010265.x · DOI
- Uehara, 1997, Chronic insulin hypoglycemia induces GLUT-3 protein in rat brain neurons, Am. J. Physiol., 272, E716
Cited by
Sorted by citations
Herrero-Mendez, A., Almeida, A., Fernández, E., Maestre, C., Moncada, S., & Bolaños, J. P. (2009) · Nature Cell Biology · doi:10.1038/ncb1881 · Cited by 844
Self-citationCommitment to glycolysis sustains survival of NO-producing inflammatory dendritic cells
Everts, B., Amiel, E., van der Windt, G. J. W., Freitas, T. C., Chott, R., Yarasheski, K. E., Pearce, E. L., & Pearce, E. J. (2012) · Blood · doi:10.1182/blood-2012-03-419747 · Cited by 532
Mantena, S. K., King, A. L., Andringa, K. K., Eccleston, H. B., & Bailey, S. M. (2008) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2007.12.029 · Cited by 429
Nitric Oxide and Mitochondrial Signaling: From Physiology to Pathophysiology
Erusalimsky, J. D., & Moncada, S. (2007) · Arteriosclerosis, Thrombosis, and Vascular Biology · doi:10.1161/atvbaha.107.151167 · Cited by 336
McClory, H., Williams, D., Sapp, E., Gatune, L. W., Wang, P., DiFiglia, M., & Li, X. (2014) · Acta Neuropathologica Communications · doi:10.1186/s40478-014-0178-7 · Cited by 60
Metadata
- Authors
- CIDAD, P., ALMEIDA, A., & BOLAÑOS, J. P.
- Affiliations
- Departamento de Bioquímica y Biología Molecular, Universidad de Salamanca, Campus Miguel de Unamuno, 37007 Salamanca, Spain
- Venue
- Biochemical Journal
- Publisher
- Portland Press Ltd.
- Published
- 2004-12-07
- Volume
- 384
- Issue
- 3
- Pages
- 629-636
- ISSN
- 0264-6021
- 1470-8728
- Cited by
- 75
- References
- 0
- Language
- en
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review