Brain damage led to decrease of nitric oxide content in the hippocampus of rats: Investigation by EPR spectroscopy

G.G. Yafarova a,b, V.V. Andrianov a,b, S.G. Pashkevich c, Ju.P. Stukach c, M.O. Dosina c, T.Kh. Bogodvid a,d, V.A. Kulchitsky c, Kh.L. Gainutdinov a,b

a Kazan Federal University, Kazan, 420008 Russia

b Zavoisky Physical-Technical Institute, FRC Kazan Scientific Center of Russian Academy of Sciences, Kazan, 420034 Russia

c Institute of Physiology of National Academy of Sciences of Belarus, Minsk, 220072 Republic of Belarus

d Volga Region State Academy of Physical Culture, Kazan, 420010 Russia

Received May 17, 2018

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Abstract

Direct measurements of the content of nitric oxide (NO) by the method of spectroscopy of electron paramagnetic resonance were performed. It was found that NO production in hippocampus tissues decreased to 46% after 5 h of ischemic stroke as compared to the control group and remained at the same level after 72 h. Following the hemorrhagic stroke, the level of NO production in the hippocampus decreased to 32% after 5 h of hemorrhagic stroke of the control level. After 72 hours of hemorrhagic stroke NO production was higher than after 5 h and amounted to 48% of the level of intact animals.

Keywords: nitric oxide, ischemic brain stroke, hemorrhagic brain stroke, hippocampus, electron paramagnetic resonance

Acknowledgments. The study was supported by the Russian Foundation for Basic Research (project no. 18-515-00003) and by the Belarusian Republican Foundation for Fundamental Research (project no. B18R-227).

References

  1. Doyle K.P., Simon R.P., Stenzel-Poore M.P. Mechanisms of ischemic brain damage. Neuro­phrmacology, 2008, vol. 55, no. 3, pp. 310–318. doi: 10.1016/j.neuropharm.2008.01.005.
  2. Steinert J.R., Chernova T., Forsythe I.D. Nitric oxide signaling in brain function, dysfunction, and dementia. Neuroscientist, 2010, vol. 16, no. 4, pp. 435–452. doi: 10.1177/1073858410366481.
  3. Gainutdinov Kh.L., Gavrilova S.A., Iyudin V.S., Golubeva A.V., Davydova M.P., Jafarova G.G., Andrianov V.V., Koshelev V.B. EPR study of the intensity of the nitric oxide production in rat brain after ischemic stroke. Appl. Magn. Reson., 2011, vol. 40, no. 3, pp. 267–278. doi: 10.1007/s00723-011-0207-7.
  4. Terpolilli N.A., Moskowitz M.A., Plesnila N. Nitric oxide: Considerations for the treatment of ischemic stroke. J. Cereb. Blood Flow Metab., 2012, vol. 32, no. 7, pp. 1332–1346. doi: 10.1038/jcbfm.2012.12.
  5. Vanin A.F., Huisman A., Van Faassen E.E. Iron dithiocarbamate as spin trap for nitric oxide detection: Pitfalls and successes. Methods Enzymol., 2003, vol. 359, pp. 27–42. doi: 10.1016/S0076-6879(02)59169-2.
  6. Godínez-Rubí M., Rojas-Mayorquín A.E., Ortuño-Sahagún D. Nitric oxide donors as neuroprotective agents after an ischemic stroke-related inflammatory reaction. Oxid. Med. Cell. Longevity, 2013, vol. 2013, art. 297357, pp. 1–16. doi: 10.1155/2013/297357.
  7. Roch M., Messlinger K., Kulchitsky V.A., Tichonovich O.G., Azev O.A., Koulchitsky S.V. Ongoing activity in trigeminal wide-dynamic range neurons is driven from the periphery. Neuroscience, 2007, vol. 150, no. 3, pp. 681–691. doi: 10.1016/j.neuroscience.2007.09.032.
  8. Kulchitsky V., Semenik T., Kaliadzich Z., Andrianova T., Tsishkevich K. The analysis of chemosensitive structures contribution to obstructive sleep apnea development. Clin. Neu­rophysiol., 2014, vol. 125, suppl. 1, pp. S330–S331. doi: 10.1016/S1388-2457(14)51089-9.
  9. Gainutdinov Kh.L., Andrianov V.V., Iyudin V.S., Yurtaeva S.V., Jafarova G.G., Faisul­lina R.I., Sitdikov F.G. EPR study of nitric oxide production in rat tissues under hypokinesia. Biophysics, 2013, vol. 58, no. 2, pp. 203–205. doi: 10.1134/S0006350913020073.
  10. Nagendran J., Michelakis E.D. Mitochondrial NOS is upregulated in the hypoxic heart: Implications for the function of the hypertrophied right ventricle. Am. J. Physiol., 2009, vol. 296, no. 6, pp. H1723–H1726. doi: 10.1152/ajpheart.00380.2009.
  11. Samdani A.F., Dawson T.M., Dawson V.L. Nitric oxide synthase in models of focal ischemia. Stroke, 1997, vol. 28, no. 6, pp. 1283–1288. doi: 10.1161/01.str.28.6.1283.
  12. Iadecola C., Zhang F., Casey R., Nagayama M., Ross M.E. Delayed reduction of ischemic brain injury and neurological deficits in mice lacking the inducible nitric oxide synthase gene. J. Neurosci., 1997, vol. 17, no. 23, pp. 9157–9164. doi: 10.1523/JNEUROSCI.17-23-09157.1997.
  13. Yafarova G.G., Andrianov V.V., Yagudin R.K., I.I. Shaikhytdinov, Gainutdinov K.L. Effects of NO synthase blocker L-NAME on functional state of the neuromotor system during traumatic disease of the spinal cord. Bull. Exp. Biol. Med., 2017, vol. 162, no. 3, pp. 316–319. doi: 10.1007/s10517-017-3604-6.
  14. Dawson D.A., Kusumoto K., Graham D.I., McCulloch J., Macrae I.M. Inhibition of nitric oxide synthesis does not reduce infarct volume in a rat model of focal cerebral ischaemia. Neurosci. Lett., 1992, vol. 142, no. 2, pp. 151–154. doi: 10.1016/0304-3940(92)90361-A.
  15. Yamamoto S., Golanov E.V., Berger S.B., Reis D.J. Inhibition of nitric oxide synthesis increases focal ischemic infarction in rat. J. Cereb. Blood Flow Metab., 1992, vol. 12, no. 5, pp. 717–726. doi: 10.1038/jcbfm.1992.102.
  16. Abu-Soud H.M., Rousseau D.L., Stuehr D.J. Nitric oxide binding to the heme of neuronal nitric-oxide synthase links its activity to changes in oxygen tension. J. Biol. Chem., 1996, vol. 271, no. 51, pp. 32515–32518. doi: 10.1074/jbc.271.51.32515.
  17. Le Cras T.D., McMur-ry I.F. Nitric oxide production in the hypoxic lung. Am. J. Physiol.-Lung Cell Mol. Physiol., 2001, vol. 280, no. 4, pp. L575–L582. doi: 10.1152/ajplung.2001.280.4.L575.
  18. Hampl V., Herget J. Role of nitric oxide in the pathogenesis of chronic pulmonary hypertension. Physiol. Rev., 2000, vol. 80, no. 4, pp. 1337–1372. doi: 10.1152/physrev.2000.80.4.1337.
  19. Manukhina E.B., Malyshev I.Y., Smirin B.V., Mashina S.Y., Saltykova V.A., Vanin A.F. Production and storage of nitric oxide in adaptation to hypoxia. Nitric Oxide, 1999, vol. 3, no. 5, pp. 393–401. doi: 10.1006/niox.1999.0244.


For citation: Yafarova G.G., Andrianov V.V., Pashkevich S.G., Stukach Ju.P., Dosina M.O., Bogodvid T.Kh., Kulchitsky V.A., Gainutdinov Kh.L. Brain damage led to decrease of nitric oxide content in the hippocampus of rats: Investigation by EPR spectroscopy. Uchenye Zapiski Kazanskogo Universiteta. Seriya Estestvennye Nauki, 2018, vol. 160, no. 4, pp. 654–662.

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