Ukr.Biochem.J. 2015; Volume 87, Issue 6, Nov-Dec, pp. 64-75

doi: https://doi.org/10.15407/ubj87.06.064

The effect of nitric oxide on synaptic vesicle proton gradient and mitochondrial potential of brain nerve terminals

A. S. Tarasenko

Palladin Institute of Biochemistry, National Academy of Sciences of Ukraine, Kyiv;
e-mail: tas@biochem.kiev.ua

The effect of nitric oxide on synaptic vesicle proton gradient and membrane potential of rat brain nerve terminals was studied. It has been shown that nitric oxide in the form of S-nitrosothiols at nanomolar concentrations had no effect on the studied parameters, but caused a rapid dissipation of synaptic vesicle proton gradient and depolarization of mitochondrial membrane in the presence of a SH-reducing compound such as dithiothreitol. Both processes were reversible and the rate of H+-gradient restoration depended on the redox potential of nerve terminals, namely the molar ratio of reductant/oxidant. This facts, as well as insensitivity of the studied processes to the inhibitor of NO-sensitive guanylate cyclase such as ODQ, allow suggesting that post-translational modification of thiol residues of the mitochondrial and synaptic vesicle proteins underlies the effect of nitric oxide on the key functional parameters of presynaptic nerve terminals.

Keywords: , , , ,


References:

  1. Calabrese V, Mancuso C, Calvani M, Rizzarelli E, Butterfield DA, Stella AM. Nitric oxide in the central nervous system: neuroprotection versus neurotoxicity. Nat Rev Neurosci. 2007 Oct;8(10):766-75. Review. PubMed, CrossRef
  2. Guix FX, Uribesalgo I, Coma M, Muñoz FJ. The physiology and pathophysiology of nitric oxide in the brain. Prog Neurobiol. 2005 Jun;76(2):126-52. PubMedCrossRef
  3. Esplugues JV. NO as a signalling molecule in the nervous system. Br J Pharmacol. 2002 Mar;135(5):1079-95. Review. PubMed, PubMedCentral, CrossRef
  4. Herring N, Paterson DJ. Nitric oxide-cGMP pathway facilitates acetylcholine release and bradycardia during vagal nerve stimulation in the guinea-pig in vitro. J Physiol. 2001 Sep 1;535(Pt 2):507-18. PubMed, PubMedCentral, CrossRef
  5. Prast H, Tran MH, Fischer H, Philippu A. Nitric oxide-induced release of acetylcholine in the nucleus accumbens: role of cyclic GMP, glutamate, and GABA. J Neurochem. 1998 Jul;71(1):266-73. PubMed, CrossRef
  6.  Hall CN, Garthwaite J. What is the real physiological NO concentration in vivo? Nitric Oxide. 2009 Sep;21(2):92-103. Review. PubMed, PubMedCentral, CrossRef
  7. Hess DT, Matsumoto A, Kim SO, Marshall HE, Stamler JS. Protein S-nitrosylation: purview and parameters. Nat Rev Mol Cell Biol. 2005 Feb;6(2):150-66. Review. PubMed, CrossRef
  8. Foster MW, Hess DT, Stamler JS. Protein S-nitrosylation in health and disease: a current perspective. Trends Mol Med. 2009 Sep;15(9):391-404. Review. PubMed, PubMedCentral, CrossRef
  9. Zhang Y, Hogg N. S-Nitrosothiols: cellular formation and transport. Free Radic Biol Med. 2005 Apr 1;38(7):831-8. Review. PubMed, CrossRef
  10. Bishop A, Anderson JE. NO signaling in the CNS: from the physiological to the pathological. Toxicology. 2005 Mar 15;208(2):193-205. Review. PubMed, CrossRef
  11. Bellamy TC, Griffiths C, Garthwaite J. Differential sensitivity of guanylyl cyclase and mitochondrial respiration to nitric oxide measured using clamped concentrations. J Biol Chem. 2002 Aug 30;277(35):31801-7. PubMed, CrossRef
  12.  Hall CN, Attwell D. Assessing the physiological concentration and targets of nitric oxide in brain tissue. J Physiol. 2008 Aug 1;586(Pt 15):3597-615. PubMed, PubMedCentral, CrossRef
  13. Kluge I, Gutteck-Amsler U, Zollinger M, Do KQ. S-Nitrosoglutathione in rat cerebellum: identification and quantification by liquid chromatography-mass spectrometry. J Neurochem. 1997 Dec;69(6):2599-607. PubMed, CrossRef
  14. Cotman CW. Isolation of synaptosomal and synaptic plasma membrane fractions. Methods Enzymol. 1974;31:445-52. PubMed, CrossRef
  15.  Tarasenko AS, Linetska MV, Storchak LG, Himmelreich NH. Effectiveness of extracellular lactate/pyruvate for sustaining synaptic vesicle proton gradient generation and vesicular accumulation of GABA. J Neurochem. 2006 Nov;99(3):787-96. PubMed, CrossRef
  16. Larson E, Howlett B, Jagendorf A. Artificial reductant enhancement of the Lowry method for protein determination. Anal Biochem. 1986 Jun;155(2):243-8. PubMed, CrossRef
  17. DeLorenzo RJ, Freedman SD. Calcium dependent neurotransmitter release and protein phosphorylation in synaptic vesicles. Biochem Biophys Res Commun. 1978 Jan 13;80(1):183-92. PubMed, CrossRef
  18.  Zoccarato F, Cavallini L, Alexandre A. The pH-sensitive dye acridine orange as a tool to monitor exocytosis/endocytosis in synaptosomes. J Neurochem. 1999 Feb;72(2):625-33. PubMed, CrossRef
  19. Melnik VI, Bikbulatova LS, Gulyaeva NV, Bazyan AS. Synaptic vesicle acidification and exocytosis studied with acridine orange fluorescence in rat brain synaptosomes. Neurochem Res. 2001 May;26(5):549-54. PubMed
  20. Aiuchi T, Daimatsu T, Nakaya K, Nakamura Y. Fluorescence changes of rhodamine 6G associated with changes in membrane potential in synaptosomes. Biochim Biophys Acta. 1982 Mar 8;685(3):289-96. PubMed, CrossRef
  21. Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR. Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids. Anal Biochem. 1982 Oct;126(1):131-8. PubMed, CrossRef
  22. Singh RJ, Hogg N, Joseph J, Kalyanaraman B. Mechanism of nitric oxide release from S-nitrosothiols. J Biol Chem. 1996 Aug 2;271(31):18596-603. PubMed, CrossRef
  23. Matthews JR, Botting CH, Panico M, Morris HR, Hay RT. Inhibition of NF-kappaB DNA binding by nitric oxide. Nucleic Acids Res. 1996 Jun 15;24(12):2236-42. PubMed, PubMedCentral, CrossRef
  24.  Cidon S, Sihra TS. Characterization of a H+-ATPase in rat brain synaptic vesicles. Coupling to L-glutamate transport. J Biol Chem. 1989 May 15;264(14):8281-8. PubMed
  25. Forgac M. The vacuolar H+-ATPase of clathrin-coated vesicles is reversibly inhibited by S-nitrosoglutathione. J Biol Chem. 1999 Jan 15;274(3):1301-5. PubMed, CrossRef
  26.  Satoh S, Murayama T, Nomura Y. Sodium nitroprusside stimulates noradrenaline release from rat hippocampal slices in the presence of dithiothreitol. Brain Res. 1996 Sep 16;733(2):167-74. PubMed, CrossRef
  27. Satoh S, Kimura T, Toda M, Miyazaki H, Ono S, Narita H, Murayama T, Nomura Y. NO donors stimulate noradrenaline release from rat hippocampus in a calmodulin-dependent manner in the presence of L-cysteine. J Cell Physiol. 1996 Oct;169(1):87-96. PubMed, CrossRef
  28.  Scott ID, Nicholls DG. Energy transduction in intact synaptosomes. Influence of plasma-membrane depolarization on the respiration and membrane potential of internal mitochondria determined in situ. Biochem J. 1980 Jan 15;186(1):21-33. PubMed, PubMedCentral, CrossRef
  29. Brorson JR, Schumacker PT, Zhang H. Nitric oxide acutely inhibits neuronal energy production. The Committees on Neurobiology and Cell Physiology. J Neurosci. 1999 Jan 1;19(1):147-58. PubMed
  30. Solenski NJ, Kostecki VK, Dovey S, Periasamy A. Nitric-oxide-induced depolarization of neuronal mitochondria: implications for neuronal cell death. Mol Cell Neurosci. 2003 Dec;24(4):1151-69. PubMed, CrossRef
  31. Almeida A, Almeida J, Bolaños JP, Moncada S. Different responses of astrocytes and neurons to nitric oxide: the role of glycolytically generated ATP in astrocyte protection. Proc Natl Acad Sci USA. 2001 Dec 18;98(26):15294-9. PubMed, PubMedCentral, CrossRef
  32. Brown GC. Nitric oxide and mitochondrial respiration. Biochim Biophys Acta. 1999 May 5;1411(2-3):351-69. Review. PubMed, CrossRef
  33. Shen W, Hintze TH, Wolin MS. Nitric oxide. An important signaling mechanism between vascular endothelium and parenchymal cells in the regulation of oxygen consumption. Circulation. 1995 Dec 15;92(12):3505-12. PubMed
  34. Erecinńska M, Nelson D, Vanderkooi JM. Effects of NO-generating compounds on synaptosomal energy metabolism. J Neurochem. 1995 Dec;65(6):2699-705. PubMed, CrossRef
  35. Lipton SA, Choi YB, Pan ZH, Lei SZ, Chen HS, Sucher NJ, Loscalzo J, Singel DJ, Stamler JS. A redox-based mechanism for the neuroprotective and neurodestructive effects of nitric oxide and related nitroso-compounds. Nature. 1993 Aug 12;364(6438):626-32. PubMed, CrossRef

Creative CommonsThis work is licensed under a Creative Commons Attribution 4.0 International License.