The Effect of Spinal Cord Injury on P2 Signaling in the Cholinergic Synapse

Capa

Citar

Texto integral

Acesso aberto Acesso aberto
Acesso é fechado Acesso está concedido
Acesso é fechado Somente assinantes

Resumo

It is known that in spinal motor neurons, after damage to the upper level of the spinal cord, neuronal degradation occurs, accompanied by axon degeneration. In the present study, the functional integrity of neuromuscular transmission was assessed by the method of stimulation mechanomiography. We demonstrated a decrease in the modulating activity of ATP in the cholinergic synapse due to spinal cord injury (a model of spinal cord contusion injury) in comparison with hypodynamia (a model of anti-orthostatic hanging of the hind limbs). The demonstrated abnormal modulation of the neuromuscular junction by purines provides evidence of axon degeneration and suggests that trans-synaptic degeneration of motor neurons may occur below the level of spinal cord injury in patients with similar injuries.

Sobre autores

A. Khairullin

Kazan State Medical University; Kazan Federal University

Autor responsável pela correspondência
Email: khajrulli@yandex.ru
Russia, Kazan; Russia, 420008, Kazan

D. Efimova

Kazan State Medical University

Email: khajrulli@yandex.ru
Russia, Kazan

A. Eremeev

Kazan Federal University

Email: khajrulli@yandex.ru
Russia, 420008, Kazan

D. Sabirova

Kazan Federal University

Email: khajrulli@yandex.ru
Russia, 420008, Kazan

S. Grishin

Kazan State Medical University

Email: khajrulli@yandex.ru
Russia, Kazan

A. Ziganshin

Kazan State Medical University

Email: khajrulli@yandex.ru
Russia, Kazan

Bibliografia

  1. Pollin MM, McHanwell S, Slater CR (1991) The effect of age on motor neurone death following axotomy in the mouse. Development 112(1): 83–89. https://doi.org/10.1242/dev.112.1.83
  2. Rishal I, Fainzilber M (2014) Axon-soma communication in neuronal injury. Nat Rev Neurosci 15(1): 32–42. https://doi.org/10.1038/nrn3609
  3. Jackson AB, Dijkers M, Devivo MJ, Poczatek RB (2004) A demographic profile of new traumatic spinal cord injuries: change and stability over 30 years. Arch Phys Med Rehabil 85(11): 1740–1748. https://doi.org/10.1016/j.apmr.2004.04.035
  4. Burns AS, Jawaid S, Zhong H, Yoshihara H, Bhagat S, Murray M, Roy RR, Tessler A, Son YJ (2007) Paralysis elicited by spinal cord injury evokes selective disassembly of neuromuscular synapses with and without terminal sprouting in ankle flexors of the adult rat. J Comp Neurol 500(1): 116–133. https://doi.org/10.1002/cne.21143
  5. Burns AS, Lemay MA, Tessler A (2005) Abnormal spontaneous potentials in distal muscles in animal models of spinal cord injury. Muscle Nerve 31(1): 46 –51. https://doi.org/10.1002/mus.20229
  6. Kaelan C, Jacobsen PF, Kakulas BA (1988) An investigation of possible transynaptic neuronal degeneration in human spinal cord injury. J Neurol Sci 86(2–3): 231–237. https://doi.org/10.1016/0022-510x(88)90101-3
  7. Bjugn R, Nyengaard JR, Rosland JH (1997) Spinal cord transection – no loss of distal ventral horn neurons. Modern stereological techniques reveal no transneuronal changes in the ventral horns of the mouse lumbar spinal cord after thoracic cord transection. Exp Neurol 148(1): 179 –186.
  8. Kirshblum S, Lim S, Garstang S, Millis S (2001) Electrodiagnostic changes of the lower limbs in subjects with chronic complete cervical spinal cord injury. Arch Phys Med Rehabil 82(5): 604–607. https://doi.org/10.1053/apmr.2001.22348
  9. Burns AS, Boyce VS, Tessler A, Lemay MA (2007) Fibrillation potentials following spinal cord injury: Improvement with neurotrophins and exercise. Muscle Nerve 35(5): 607–613. https://doi.org/10.1002/mus.20738
  10. Carter JG, Sokoll MD, Gergis SD (1981) Effect of spinal cord transection on neuromuscular function in the rat. Anesthesiology 55(5): 542–546. https://doi.org/10.1097/00000542-198111000-00011
  11. Dahlstrom A, Heiwall PO, Booj S, Dahllof AG (1978) The influence of supraspinal impulse activity on the intra-axonal transport of acetylcholine, choline acetyltransferase and acetylcholinesterase in rat motor neurons. Acta Physiol Scand 103(3): 308–319. https://doi.org/10.1111/j.1748-1716.1978.tb06218.x
  12. Akaaboune M, Culican SM, Turney SG, Lichtman JW (1999) Rapid and reversible effects of activity on acetylcholine receptor density at the neuromuscular junction in vivo. Science 286(5439): 503–507. https://doi.org/10.1126/science.286.5439.503
  13. Bruneau E, Sutter D, Hume RI, Akaaboune M (2005) Identification of nicotinic acetylcholine receptor recycling and its role in maintaining receptor density at the neuromuscular junction in vivo. J Neurosci 25(43): 9949–9959. https://doi.org/10.1523/JNEUROSCI.3169-05.2005
  14. Xiong GX, Zhang JW, Hong Y, Guan Y, Guan H (2008) Motor unit number estimation of the tibialis anterior muscle in spinal cord injury. Spinal Cord 46(10): 696–702. https://doi.org/10.1038/sc.2008.7
  15. Cotrina, ML, Lin JH, Alves-Rodrigues A, Liu S, Li J, Azmi-Ghadimi H, Kang J, Naus CC, Nedergaard M (1988) Connexins regulate calcium signaling by controlling ATP release. Proc Natl Acad Sci U S A 95(26): 15735–15740. https://doi.org/10.1073/pnas.95.26.15735
  16. Guthrie PB, Knappenberger J, Segal M, Bennett MV, Charles AC, Kater SB (1999) ATP released from astrocytes mediates glial calcium waves. J Neurosci 19(2): 520–528. https://doi.org/10.1523/JNEUROSCI.19-02-00520.1999
  17. Arcuino G, Lin JHC, Takano T, Liu C, Jiang L, Gao Q, Kang J, Nedergaard M (2002) Intercellular calcium signaling mediated by point-source burst release of ATP. Proc Natl Acad Sci U S A 99(15): 9840–9845. https://doi.org/10.1073/pnas.152588599
  18. Fields RD, Stevens-Graham B (2002) New insights into neuron-glia communication. Science 298(5593): 556–562. https://doi.org/10.1126/science.298.5593.556
  19. Haydon PG (2001) Glia: listening and talking to the synapse. Nat Rev Neurosci 2(3): 185–193. https://doi.org/10.1038/35058528
  20. Nedergaard M, Ransom B, Goldman S (2003) New roles for astrocytes: Redefining the functional architecture of the brain. Trends Neurosci 26(10): 523–530. https://doi.org/10.1016/j.tins.2003.08.008
  21. Fam SR, Gallagher CJ, Salter MW (2000) P2Y(1) purinoceptor-mediated Ca2+ signaling and Ca2+ wave propagation in dorsal spinal cord astrocytes. J Neurosci 20(8): 2800–2808. https://doi.org/10.1523/JNEUROSCI.20-08-02800.2000
  22. Khakh BS, North RA (2006) P2X receptors as cell-surface ATP sensors in health and disease. Nature 442(7102): 527–532. https://doi.org/10.1038/nature04886
  23. Gourine AV, Dale N, Llaudet E, Poputnikov DM, Spyer KM, Gourine VN (2007) Release of ATP in the central nervous system during systemic inflammation: Real-time measurement in the hypothalamus of conscious rabbits. J Physiol 585(Pt 1): 305–316. https://doi.org/10.1113/jphysiol.2007.143933
  24. Wang X, Arcuino G, Takano T, Lin J, Peng WG, Wan P, Li P, Xu Q, Liu QS, Goldman SA, Nedergaard M (2004) P2X7 receptor inhibition improves recovery after spinal cord injury. Nature Med 10(8): 821–827. https://doi.org/10.1038/nm1082
  25. North A (2002) Molecular physiology of P2X receptors. Physiol Rev 82(4): 1013–1067. https://doi.org/10.1152/physrev.00015.2002
  26. Solle M, Labasi J, Perregaux DG, Stam E, Petrushova N, Koller BH, Griffiths RJ, Gabel CA (2001) Altered cytokine production in mice lacking P2X7 receptors. J Biol Chem 276(1): 125–132. https://doi.org/10.1074/jbc.M006781200
  27. Kahlenberg J, Dubyak GW (2004) Mechanisms of caspase-1 activation by P2X7 receptor-mediated K+ release. Am J Physiol 286(5): 1100–1108. https://doi.org/10.1152/ajpcell.00494.2003
  28. Samad TA, Moore KA, Sapirstein A, Billet S, Allchorne A, Poole S, Bonventre JV, Woolf CJ (2001) Interleukin-1beta-mediated induction of Cox-2 in the CNS contributes to inflammatory pain hypersensitivity. Nature 410(6827): 471– 475. https://doi.org/10.1038/35068566
  29. Suzuki T, Hide I, Ido K, Kohsaka S, Inoue K, Nakata Y (2004) Production and release of neuroprotective tumor necrosis factor by P2X7 receptor-activated microglia. J Neurosci 24(1): 1–7. https://doi.org/10.1523/JNEUROSCI.13-12-05153.1993
  30. Allen AR (1911) Surgery of experimental lesion of spinal cord equivalent to crush injury of fracture dislocation of spinal column: a preliminary report. JAMA 57: 878–880.
  31. Ильин ЕА, Новиков ВЕ (1980) Стенд для моделирования физиологических эффектов невесомости в лабораторных экспериментах с крысами. Косм биол авиакосм мед 14(3): 79–80. [Ilyin EA, Novikov VE (1980) Stand for modeling the physiological effects of weightlessness in laboratory experiments with rats. Cosm biol aerocosm med 14(3): 79–80. (In Russ)].
  32. Morey-Holton ER, Globus RK (2002) Hindlimb unloading rodent model: technical aspects. J Appl Physiol 92(4): 1367–1377. https://doi.org/10.1152/japplphysiol.00969.2001
  33. Morey-Holton ER, Globus RK (1988) Hindlimb unloading of growing rats: a model for predicting skeletal changes during space flight. Bone 22(5 Suppl): 83–88. https://doi.org/10.1016/s8756-3282(98)00019-2
  34. Khairullin AE, Efimova DV, Markosyan VA, Grishin SN, Teplov AY, Ziganshin AU (2021) The effect of acute unilateral denervation injury on purinergic signaling in the cholinergic synapse. Biophysics 66(3): 483–486. https://doi.org/10.1134/S0006350921030064
  35. Profyris C, Cheema SS, Zang DW, Azari MF, Boyle K, Petratos S (2004) Degenerative and regenerative mechanisms governing spinal cord injury. Neurobiol Disease 15(3): 415–436. https://doi.org/10.1016/j.nbd.2003.11.015
  36. Beattie MS, Farooqui AA, Bresnahan JC (2000) Review of current evidence for apoptosis after spinal cord injury. J Neurotrauma 17(10): 915 – 925. https://doi.org/10.1089/neu.2000.17.915
  37. Peng W, Cotrina ML, Han X, Yu H, Bekar L, Blum L, Takano T, Tian GF, Goldman SA, Nedergaard M (2009) Systemic administration of an antagonist of the ATP-sensitive receptor P2X7 improves recovery after spinal cord injury. Proc Natl Acad Sci U S A 106(30): 12489–12493. https://doi.org/10.1073/pnas.0902531106
  38. Grafe P, Schaffer V, Rucker F (2006) Kinetics of ATP release following compression injury of a peripheral nerve trunk. Purinerg Signal 2: 527– 536.
  39. Cook SP, McCleskey EW (2002) Cell damage excites nociceptors through release of cytosolic ATP. Pain 95(1–2): 41–47.
  40. Neary JT, Kang Y, Willoughby KA, Ellis EF (2003) Activation of extracellular signal-regulated kinase by stretch-induced injury in astrocytes involves extracellular ATP and P2 purinergic receptors. J Neurosci 23(6): 2348–2356. https://doi.org/10.1523/JNEUROSCI.23-06-02348.2003
  41. Du S, Rubin A, Klepper S, Barrett C, Kim YC, Rhim HW, Lee EB, Park CW, Markelonis GJ, Oh TH (1999) Calcium influx and activation of calpain I mediate acute reactive gliosis in injured spinal cord. Exp Neurol 157(1): 96–105. https://doi.org/10.1006/exnr.1999.7041
  42. Stokes BT, Fox P, Hollinden G (1983) Extracellular calcium activity in the injured spinal cord. Exp Neurol 80(3): 561–572.
  43. Nilsson P, Hillered L, Olsson Y, Sheardown MJ, Hansen AJ (1993) Regional changes in interstitial K+ and Ca2+ levels following cortical compression contusion trauma in rats. J Cereb Blood Flow Metab 13(2): 183–192. https://doi.org/10.1038/jcbfm.1993.22
  44. Stout C, Charles A (2003) Modulation of intercellular calcium signaling in astrocytes by extracellular calcium and magnesium. Glia 43(3): 265–273. https://doi.org/10.1002/glia.10257
  45. Bianchi BR, Lynch KJ, Touma E, Niforatos W, Burgard EC, Alexander KM, Park HS, Yu H, Metzger R, Kowaluk E, Jarvis MF, Biesen T (1999) Pharmacological characterization of recombinant human and rat P2X receptor subtypes. Eur J Pharmacol 376(1–2): 127–138. https://doi.org/10.1002/glia.10257
  46. Di Virgilio, Chiozzi FP, Falzoni S, Ferrari D, Sanz JM, Venketaraman V, Baricordi OR (1998) Cytolytic P2X purinoceptors. Cell Death Differ 5(3): 191–199.
  47. Deuchars SA, Atkinson L, Brooke RE, Musa H, Milligan CJ, Batten TF, Buckley NJ, Parson SH, Deuchars J (2001) Neuronal P2X7 receptors are targeted to presynaptic terminals in the central and peripheral nervous systems. J Neurosci 21(18): 7143–7152. https://doi.org/10.1523/JNEUROSCI.21-18-07143.2001
  48. Gerasimenko YP, Avelev VD, Nikitin OA, Lavrov IA (2003) Initiation of locomotor activity in spinal cats by epidural stimulation of the spinal cord. Neurosci Behav Physiol 33(3): 247–254. https://doi.org/10.1023/a:1022199214515
  49. Lavrov I, Dy CJ, Fong AJ, Gerasimenko Y, Courtine G, Zhong H, Roy RR, Edgerton VR (2008) Epidural stimulation induced modulation of spinal locomotor networks in adult spinal rats. J Neurosci 28(23): 6022–6029. https://doi.org/10.1523/JNEUROSCI.0080-08.2008
  50. Irnich D, Burgstahler R, Bostock H, Grafe P (2001) ATP affects both axons and Schwann cells of unmyelinated C fibers. Pain 92: 343–350. https://doi.org/10.1016/S0304-3959(01)00277-9
  51. Lucas DR, Newhouse JP (1957) The Toxic Effect of Sodium L-Glutamate on the Inner Layers of the Retina. AMA Archiv Ophthalmol 58(2): 193–201. https://doi.org/10.1001/archopht.1957.00940010205006

Arquivos suplementares

Arquivos suplementares
Ação
1. JATS XML
Baixar
2.

Baixar (429KB)
Metadados
3.

Baixar (138KB)
Metadados
4.

Baixar (144KB)
Metadados
5.

Baixar (160KB)
Metadados

Declaração de direitos autorais © А.Е. Хайруллин, Д.В. Ефимова, А.А. Еремеев, Д.Э. Сабирова, С.Н. Гришин, А.У. Зиганшин, 2023

Este site utiliza cookies

Ao continuar usando nosso site, você concorda com o procedimento de cookies que mantêm o site funcionando normalmente.

Informação sobre cookies