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Inhibition of mitochondrial respiration by nitric oxide rapidly stimulates cytoprotective GLUT3-mediated glucose uptake through 5′-AMP-activated protein kinase

CIDAD, Pilar, ALMEIDA, Angeles, BOLAÑOS, Juan P.·2004·Biochemical Journal

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.

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Research works printed but not linked: 42

  1. Maher, 1994, Glucose transporter proteins in brain, FASEB J., 8, 1003, 10.1096/fasebj.8.13.7926364 · DOI
  2. Maher, 1996, Substrate specificity and kinetic parameters of GLUT3 in rat cerebellar granule neurons, Biochem. J., 315, 827, 10.1042/bj3150827 · DOI
  3. Burant, 1992, Mammalian facilitative glucose transporters: evidence for similar substrate recognition sites in functionally monomeric proteins, Biochemistry, 31, 10414, 10.1021/bi00157a032 · DOI
  4. 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
  5. Gould, 1997, Introduction to the facilitative glucose transporter family, 1
  6. 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
  7. 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
  8. 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
  9. 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
  10. 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
  11. Simmons, 1992, Induction of nitric oxide synthase in glial cells, J. Neurochem., 59, 897, 10.1111/j.1471-4159.1992.tb08328.x · DOI
  12. 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
  13. 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
  14. 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
  15. 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
  16. Roberts, 1997, Exercise-stimulated glucose transport in skeletal muscle is nitric oxide dependent, Am. J. Physiol., 273, E220
  17. 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
  18. 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
  19. 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
  20. Chen, 1999, AMP-activated protein kinase phosphorylation of endothelial NO synthase, FEBS Lett., 443, 285, 10.1016/S0014-5793(98)01705-0 · DOI
  21. 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
  22. 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
  23. 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
  24. 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
  25. 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
  26. 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
  27. 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
  28. Brummelkamp, 2002, A system for stable expression of short interfering RNAs in mammalian cells, Science, 296, 550, 10.1126/science.1068999 · DOI
  29. Sledz, 2003, Activation of the interferon system by short-interfering RNAs, Nat. Cell Biol., 9, 834, 10.1038/ncb1038 · DOI
  30. Ohtsuka, 2004, ASC is a Bax adaptor and regulates the p53-Bax mitochondrial apoptosis pathway, Nat. Cell Biol., 6, 121, 10.1038/ncb1087 · DOI
  31. 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
  32. 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
  33. Jaworek, 1985, Adenosine 5′-diphosphate and adenosine 5′-monophosphate. UV-method, 365
  34. Lowry, 1951, Protein measurement with the Folin phenol reagent, J. Biol. Chem., 193, 265, 10.1016/S0021-9258(19)52451-6 · DOI
  35. 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
  36. 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
  37. 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
  38. 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
  39. 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
  40. Lee, 1993, Ischemic injury induces brain glucose transporter gene expression, Endocrinology, 133, 2540, 10.1210/endo.133.6.8243275 · DOI
  41. 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
  42. Uehara, 1997, Chronic insulin hypoglycemia induces GLUT-3 protein in rat brain neurons, Am. J. Physiol., 272, E716

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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
Published
2004-12-07
Volume
384
Issue
3
Pages
629-636
ISSN
  • 0264-6021
  • 1470-8728
Cited by
75
References
0
Language
en

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