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ISSN 2522-9028 (Print)
ISSN 2522-9036 (Online)
DOI: https://doi.org/10.15407/fz

Fiziologichnyi Zhurnal

is a scientific journal issued by the

Bogomoletz Institute of Physiology
National Academy of Sciences of Ukraine

Editor-in-chief: V.F. Sagach

The journal was founded in 1955 as
1955 – 1977 "Fiziolohichnyi zhurnal" (ISSN 0015 – 3311)
1978 – 1993 "Fiziologicheskii zhurnal" (ISSN 0201 – 8489)
1994 – 2016 "Fiziolohichnyi zhurnal" (ISSN 0201 – 8489)
2017 – "Fiziolohichnyi zhurnal" (ISSN 2522-9028)

Fiziol. Zh. 2004; 50(6): 62-75


Effect of muscle pain on c-fos expression and nadph-diaphorase activityin the spinal cord

A.V. Maznychenko

    A.A. Bogomoletz Institute of Physiology, National Academy ofSciences of Ukraine, Kiev.


Abstract

Capsaicin (Sigma, 5 mg/1 ml) was unilaterally injected into dorsal neck muscles (mm. trapezius, splenius) of the cat (n = 6) anesthetized with ?-chloralose. The laminar distribution of Fos- immunoreactive (Fos-ir) and NADPH-d-reactive neurons was studied in the sections of the cervical and lumbar seg- ments. In comparison to sham operated animals (n = 2), 2 h after capsaicin injection the significant c-fos expression was found throughout the cervical cord (C1 – C8) ipsilaterally and lumbar cord bilaterally (L1 – L7), while the predominant mean number of Fos-ir neurons was detected in the C1 – C4 and L3 – L6 segments. In cervical spinal cord, c-fos expression was three times more than in lumbar spinal cord. Dorsal neck nox- ious stimulation produced widespread c-fos expression in the large and small labeled cells within lamina I, at the neck of the dorsal horn (lamina V) and also in the medial part of the inter- mediate zone (lamina VII) where cells of origin of the long crossed and uncrossed descending propriospinal pathways to the lumbar cord were known to be localized. The main accu- mulations of NADPH-d-reactive cells were registered within the marginal zone (laminae I and II) and medial part of the intermediate zone (lamina VII). Fos-ir neurons were co-dis- tributed with NADPH-d-reactive cells within the marginal zone, and the neck of the dorsal horn, however, double-stain- ing spinal neurons were not registered. These results strongly suggest that the revealed c-fos expression in cervical and lumbar segments depends on the activity of vanilloid receptors of the cervical muscles and confirmed the anatomical coupling of both regions through long propriospinal pathways which may be underlying in the cervico-lumbar nociceptive processing. An influence of the spino-cerebro-spinal loop on modulation c-fos expression in these regions is not excluded also.

References

  1. Agnati L.F., Zoli M., Stromberg I., Fuxe K. Intercellu- lar communication in the brain: wiring versus volume transmission // Neuroscience – 1995. – 69. – P. 711–726.
  2. Arima T., Svensson P., Arendt-Nielsen L. Capsaicin- induced muscle hyperalgesia in the exercised and non- exercised human masseter muscle // J. Orofac. Pain – 2000. – 14. – P. 213–223.
  3. Arnold W.P., Mittal C.K., Katsuki S., Murad F. Nitric oxide activates guanylyl cyclase and increases gua- nosine 3':5'-cyclic monophosphate levels in various tissue preparation // Proc. Nat. Acad. Sci. USA. – 1977. – 74. – P. 3203–3207.
  4. Basbaum A.I., Fields H.L. Endogenous pain control mechanisms: review and hypothesis // Ann. Neurol. – 1978. – 4. – P. 451–462.
  5. Bernardi P.S., Valtschanoff J.G., Weinberg R.J. et al. Synaptic interactions between primary afferent termi- nals and GABA and nitric oxide-synthesizing neurons in superficial laminae of the rat spinal cord // J. Neuro- sci. – 1995. – 15, №2. – P. 1363–1371.
  6. Bredt D.S., Snyder S.H. Nitric oxide mediates glutamate- linked enhancement of cGMP levels in the cerebellum // Proc. Nat. Acad. Sci. USA. – 1989. – 86. – P. 9030–9033.
  7. Brown A.G. Organization of the Spinal Cord. The Anatomy and Physiology of Identified Neurons. – New York: Springer, 1981. – 238 p.
  8. Callsen-Cencic P., Hoheisel U., Kaske A. et al. The controversy about spinal neuronal nitric oxide syn- thase: under which conditions is it up- or downre- gulated? // Cell and Tissue Res. – 1999. – 295. – P. 183–194.
  9. 9. Caterina M.J., Rosen T.A., Tominaga M. et al. A capsaicin-receptor homologue with a high threshold for noxious heat // Nature. – 1999. – 398. – P. 436–441.
  10. 10. Caterina M.J., Schumacher M.A., Tominaga M. et al. The capsaicin receptor: a heat-activated ion channel in the pain pathway // Ibid. – 1997. – 389. – P. 816–824.
  11. Ellaway P.H., Murthy K.S. Reflex effects from high threshold neck muscle afferents on hind limb extensor gamma motoneurones in the cat // Exp. Brain Res. – 1984. – 54, №2. – 212–216.
  12. Forstermann U., Gath I., Schwarz P. et al. Isoforms of nitric oxide sythase. Properties, cellular distribution and expressional control // Biochem. Pharmacol. – 1995. – 50. – P. 1321–1332.
  13. Garthwaite J., Boulton C.L. Nitric oxide signaling in the central nervous system //Ann. Rev. Physiol. – 1995. – 57. – P. 683–707.
  14. Govsa F., Kayalioрlu G., Erdem B. et al. Laminar dis- tribution of the sources of ascending spino-supraspi- nal pathways involved in nociceptive transmission and pain modulation // Tr. J. Med. Sci. – 1998. – 28. – P. 41–46.
  15. Harris J.A. Using c-fos as a Neural Marker of Pain // Brain. Res. Bull. – 1998. – 45, №1 – P. 1–8.
  16. Herdegen T., Rudiger S., Mayer B. et al. Expression of nitric oxide synthase and colocalization with Jun, Fos and Krox transcription factors in spinal cord neurons following noxious stimulation of the rat hindpaw // Brain Res. Mol. Brain Res. – 1994. – 22. – P. 245–258.
  17. Holzer P. Local effector functions of capsaicin-sensi- tive sensory nerve ending: involvement of tachykinins, calcitonin gene-related peptide and other neuropeptides // Neuroscience. – 1988. – 24. – P. 739–768.
  18. Holscher C. Nitric oxide, the enigmatic neuronal messenger: its role in synaptic plasticity // Trends Neurosci. – 1997. – 20. – P. 298–303.
  19. 19. Hsu S.-M., Raine L., Fanger H. Use of avidin-biotin- peroxidase complex (ABC) in immunoperoxidase tech- niques: a comparison between ABC and unlabelled an- tibody (PAP) procedures // J. Histochem. and Cytochem. – 1981. – 29. – P. 577–580.
  20. 20. Hunt S.P., Pini A., Evan G. Induction of c-fos-like pro- tein in spinal cord neurons following sensory stimula- tion // Nature. – 1987. – 328. – P. 632–634.
  21. Irving R.E. The tonic protective reflexes: a proposed nomenclature and classifications system // J. Manipu- lative Physiol. Ther. – 1980. – 3. – P. 244–252.
  22. Johansson H., Windhorst U., Djupsjobacka M., Passa- tore M. Chronic work-related myalgia: neuromuscular mechanisms behind work-related chronic muscle pain syndromes. – Gavle: Gavle University Press, 2003. – 310 p.
  23. Kayalioglu G., Hariri N.I., Govsa F., Erdеm B., Pеker G., Maiskii V.A. Laminar distribution of the cells of origin of the spinocerеbral pathways involved in noci- ceptive transmission and pain modulation in the rat // Neurophysiology/Neirofiziologiya. – 1996. – 28. – P. 111–122.
  24. Marshall G.E., Shehab S.A.S., Spike R.C., Todd A.J. Neurokinin-1 receptors on lumbar spinothalamic neurons in the rat // Neuroscience. – 1996. – 72. – P. 255–263.
  25. Mayer B. Biochemistry and molecular pharmacology of nitric oxide synthase. – In: Vincent SR (ed). Nitric oxide in the nervous system. – New York: Acad. Press, 1995. – P. 21–42.
  26. Menetrey D., de Pommery J., Roudier F. Propriospi- nal fibers reaching the lumbar enlargement in the rat // Neurosci. Lett. – 1985. – 58. – P. 257–261.
  27. Menetrey D., Gannon A., Levine J.D., Basbaum A.I.Expression of c-fos protein in interneurons and pro- jection neurons of the rat spinal cord in response to noxious somatic, articular, and visceral stimulation // J. Comp. Neurol. – 1989. – 285. – P. 177–195.
  28. Mense S. Nociception from skeletal muscle in relation to clinical muscle pain // Pain. – 1993. – 54. – P. 241–289.
  29. 29. Millan M.J. Descending control of pain // Prog. Neurobiol. – 2002. – 66. – P. 355–474.
  30. 30. Mitsikostas D.D., Sanchez del Rio M. Receptor sys- tems mediating c-fos expression within trigeminal nucleus caudalis in animal models of migraine // Brain Res. Rev. – 2001. – 35. – P. 20–35.
  31. Nakamura A., Shiomi H. Recent advances in neurophar- macology of cutaneous nociceptors // Jpan. J. Pharma- col. – 1999. – 79. – P. 427–431.
  32. Oka T., Hori T. Brain cytokines and pain. – In: Watkins LR, Maier SF, eds. Cytokines and pain. – Basel: Birkhauser Verlag, 1999. – Р. 183–204.
  33. Pettorossi V.E., Della Torre G., Bortolami R., Brunetti O. The role of capsaicin-sensitive muscle afferents in fatigue-induced modulation of the monosynaptic reflex in the rat // J. Physiol. (Lond.) – 1999. – 515. – P. 599–607.
  34. Peunova N., Enikolopov G. Amplification of calcium- induced gene transcription by nitric oxide in neuronal cells // Nature. – 1993. – 364. – P. 450–453.
  35. Pilyavskii A.I., Maisky V.A. et al. c-fos expression and NADPH-diaphorase reactivity in spinal neurons after fatiguing stimulation of hindlimb muscles in the rat // Brain. Res. – 2001. – 923. – P. 91–102.
  36. Puskar Z., Polgar E., Todd A.J. A population of large lamina I projection neurons with selective inhibitory input in rat spinal cord // Neuroscience. – 2001. – 102, №1. – P. 167–176.
  37. Rexed B. A cytoarchitectonic atlas of the spinal cord in the cat // J. Comp. Neurol. – 1954. – 100, №2. – P. 297–379.
  38. Spike R.C., Todd A.J., Johnston H.M. Coexistence of NADPH-diaphorase with GABA, glycine, and acetyl- choline in rat spinal cord // Ibid. – 1993. – 335, №3. – P. 320–333.
  39. 39. Sugiura Y., Lee C.L., Perl E.R. Central projections of identified, unmyelinated (C) afferent fibers innervating mammalian skin // Science. – 1987 – 234. – Р. 358– 361.
  40. 40. Todd A. J. Cells in laminae III and IV of rat spinal dorsal horn receive monosynaptic primary afferent input in lamina II // J. Comp. Neurol. – 1989. – 289. – Р. 676–686.
  41. Todd A.J., Spike R.С., Brodbelt A.R. et al. Some in- hibitory neurons in the spinal cord develop c-fos- immunoreactivity after noxious stimulation // Neuroscience –1994. – 63, № 3, – Р. 805–816.
  42. Vizzard M.A., Erdman S.L., Roppolo J.R. et al. Dif- ferential localization of neuronal nitric oxide synthase immunoreactivity and NADPH-diaphorase activity in the cat spinal cord // Cell Tissue Res. – 1994. – 278, №2. – P. 299–309.
  43. Watkins L.R., Milligan E.D, Maier S.F. Spinal cord glia: new players in pain // Pain. – 2001. – 93. – P. 201–205.
  44. Willis W. D., Coggeshall R. E. Sensory Mechanisms of the Spinal Cord. – New York: Plenum, 1991. – 230 p.
  45. Witting N., Svensson P., Gottrup H. et al. Intramuscu- lar and intradermal injection of capsaicin: a comparison of local and referred pain // Pain. – 2000. – 84. – P. 407–412.
  46. Wu J., Fang L., Lin Q., Willis W.D. Nitric oxide syn- thase in spinal cord central sensitization following in- tradermal injection of capsaicin // Ibid. – 2001. – 94. – P. 47–58.
  47. Yezierski R.P., Culberson J.L., Brown P.B. Cells of origin of propriospinal connections to cat lumbosacral gray as determined with horseradish peroxidase // Exp. Neurol. – 1980. – 69, №3. – P. 493–512.

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