Journal of Korean Neurosurgical Society

  • 제42권6호
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  • Pages.462-469
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  • 2007
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  • 2005-3711(pISSN)
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  • 1598-7876(eISSN)
대한신경외과학회 (The Korean Neurosurgical Society)
권호 표지

The VR1-Positive Primary Afferent-Mediated Expression of pERK in the Lumbosacral Neurons in Response to Mechanical and Chemical Stimulation of the Urinary Bladder in Rats

  • Yoo, Chan-Jong (Department of Neurosurgery Gachon University, Gil Medical Center) ;
  • Hwang, Se-Jin (Department of Anatomy and Cell Biology, College of Medicine Hanyang University)
  • 발행 : 2007.12.28
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초록

Objective : This study characterized the neurons in the lumbosacral cord that express phospho ERK (pERK) after distension or irritation of the bladder, and their relation to the vanilloid receptor 1 (VR1) positive primary afferents. Methods : Mechanical distension and chemical irritation of the bladder were induced by intravesical injection of the saline and mustard oil, respectively. Spinal neurons expressing pERK and the primary afferent fibers were characterized using multiple immunofluorescence for neurokinin 1 (NK1), neuronal nitric oxide synthetase (nNOS) and VR1. Results : Neurons in lamina I, medial dorsal horn (MDH), dorsal gray commissure (DGC) and sacral parasympathetic nucleus (SPN) were immunoreactive for pERK after either mechanical or chemical stimulation. The majority of pERK positive cells were positive for NK1 in lamina I and SPN, but not in the DGC. Most of pERK positive cells are not stained for nNOS except in a small population of the cells in the SPN and DGC. Contacts between perikarya and dendrites of pERK-positive cells and terminals of primary afferents expressing VR1 were identified in lamina I. lateral collateral path (LCP) and SPN. Conclusion : In this study, the lumbosacral neurons activated by mechanical and chemical stimulation of the urinary bladder were identified with expression of the pERK, and also provided the evidence that VR1-positive primary afferents may mediate the activation of these neurons.

키워드

참고문헌

  1. Almeida A, Lima D : Activation by cutaneous or visceral noxious stimulation of spinal neurons projecting to the medullary dorsal reticular nucleus in the rat : a c-fos study. Eur J Neurosci 9 : 686-695, 1997 https://doi.org/10.1111/j.1460-9568.1997.tb01417.x
  2. Birder LA, Roppolo JR, Erickson VL, de Groat WC : Increased c-fos expression in spinal lumbosacral projection neurons and preganglionic neurons after irritation of the lower urinary tract in the rat. Brain Res 834 : 55-65, 1999 https://doi.org/10.1016/S0006-8993(99)01546-2
  3. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D : The capsaicin receptor : a heat-activated ion channel in the pain pathway. Nature 389 : 816-824, 1997 https://doi.org/10.1038/39807
  4. Cervero F : Visceral nociception : peripheral and central aspects of visceral nociceptive systems. Philos Trans R Soc Lond B Biol Sci 308 : 325-337, 1985 https://doi.org/10.1098/rstb.1985.0033
  5. Cervero F, Laird JM : Visceral pain. Lancet 353 : 2145-2148, 1999 https://doi.org/10.1016/S0140-6736(99)01306-9
  6. Chowdhary S, Townend JN : Role of nitric oxide in the regulation of cardiovascular autonomic control. Clin Sci (Lond) 97 : 5-17, 1999 https://doi.org/10.1042/cs0970005
  7. Craig AD : Distribution of brainstem projections from spinal lamina I neurons in the cat and the monkey. J Comp Neurol 361 : 225- 248, 1995 https://doi.org/10.1002/cne.903610204
  8. Ding YQ, Qin BZ, Li JS, Mizuno N : Induction of c-fos-like protein in the spinoparabrachial tract-neurons locating within the sacral parasympathetic nucleus in the rat. Brain Res 659 : 283-286, 1994 https://doi.org/10.1016/0006-8993(94)90894-X
  9. Fields RD, Eshete F, Stevens B, Itoh K : Action potential-dependent regulation of gene expression : temporal specificity in Ca2+, cAMPresponsive element binding proteins, and mitogen-activated protein kinase signaling. J Neurosci 17 : 7252-7266, 1997 https://doi.org/10.1523/JNEUROSCI.17-19-07252.1997
  10. Furst S : Transmitters involved in antinociception in the spinal cord. Brain Res Bull 48 : 129-141, 1999 https://doi.org/10.1016/S0361-9230(98)00159-2
  11. Galan A, Cervero F, Laird JM : Extracellular signaling-regulated kinase-1 and -2 (ERK 1/2) mediate referred hyperalgesia in a murine model of visceral pain. Brain Res Mol Brain Res 116 : 126-134, 2003 https://doi.org/10.1016/S0169-328X(03)00284-5
  12. Gioia M, Moscheni C, Galbiati S, Gagliano N : Immunocytochemical localization of extracellular signal-regulated kinases 1 and 2 phosphorylated neurons in the brainstem of rat following visceral noxious stimulation. Neurosci Lett 349 : 167-170, 2003 https://doi.org/10.1016/S0304-3940(03)00821-8
  13. Guo A, Vulchanova L, Wang J, Li X, Elde R : Immunocytochemical localization of the vanilloid receptor 1 (VR1) : relationship to neuropeptides, the P2X3 purinoceptor and IB4 binding sites. Eur J Neurosci 11 : 946-958, 1999 https://doi.org/10.1046/j.1460-9568.1999.00503.x
  14. Habler HJ, Janig W, Koltzenburg M : Activation of unmyelinated afferent fibres by mechanical stimuli and inflammation of the urinary bladder in the cat. J Physiol 425 : 545-562, 1990 https://doi.org/10.1113/jphysiol.1990.sp018117
  15. Hamilton MO, Papka RE, O'Donoghue DL, Vaidya AM, Williams SJ, Poff CR, et al : Spinal projection neurons to the laterodorsal pontine tegmental nucleus : relationship to preganglionic neurons and nitric oxide synthase. J Comp Neurol 353 : 1-8, 1995 https://doi.org/10.1002/cne.903530102
  16. Helliwell RJ, McLatchie LM, Clarke M, Winter J, Bevan S, McIntyre P : Capsaicin sensitivity is associated with the expression of the vanilloid (capsaicin) receptor (VR1) mRNA in adult rat sensory ganglia. Neurosci Lett 250 : 177-180, 1998 https://doi.org/10.1016/S0304-3940(98)00475-3
  17. Honda CN : Visceral and somatic afferent convergence onto neurons near the central canal in the sacral spinal cord of the cat. J Neurophysiol 53 : 1059-1078, 1985 https://doi.org/10.1152/jn.1985.53.4.1059
  18. Hwang SJ, Burette A, Valtschanoff JG : VR1-positive primary afferents contact NK1-positive spinoparabrachial neurons. J Comp Neurol 460 : 255-265, 2003 https://doi.org/10.1002/cne.10647
  19. Hwang SJ, Valtschanoff JG : Vanilloid receptor VR1-positive afferents are distributed differently at different levels of the rat lumbar spinal cord. Neurosci Lett 349 : 41-44, 2003 https://doi.org/10.1016/S0304-3940(03)00750-X
  20. Janig W, Morrison JF : Functional properties of spinal visceral afferents supplying abdominal and pelvic organs, with special emphasis on visceral nociception. Prog Brain Res 67 : 87-114, 1986 https://doi.org/10.1016/S0079-6123(08)62758-2
  21. Ji RR, Baba H, Brenner GJ, Woolf CJ : Nociceptive-specific activation of ERK in spinal neurons contributes to pain hypersensitivity. Nat Neurosci 2 : 1114-1119, 1999 https://doi.org/10.1038/16040
  22. Jin SX, Zhuang ZY, Woolf CJ, Ji RR : p38 mitogen-activated protein kinase is activated after a spinal nerve ligation in spinal cord microglia and dorsal root ganglion neurons and contributes to the generation of neuropathic pain. J Neurosci 23 : 4017-4022, 2003 https://doi.org/10.1523/JNEUROSCI.23-10-04017.2003
  23. Kuo DC, Yang GC, Yamasaki DS, Krauthamer GM : A wide field electron microscopic analysis of the fiber constituents of the major splanchnic nerve in cat. J Comp Neurol 210 : 49-58, 1982 https://doi.org/10.1002/cne.902100106
  24. Marshall GE, Shehab SA, Spike RC, Todd AJ : Neurokinin-1 receptors on lumbar spinothalamic neurons in the rat. Neuroscience 72 : 255- 263, 1996 https://doi.org/10.1016/0306-4522(95)00558-7
  25. Martin KC, Michael D, Rose JC, Barad M, Casadio A, Zhu H, et al : MAP kinase translocates into the nucleus of the presynaptic cell and is required for long-term facilitation in Aplysia. Neuron 18 : 899- 912, 1997 https://doi.org/10.1016/S0896-6273(00)80330-X
  26. Matsushita M : Ascending propriospinal afferents to area X (substantia grisea centralis) of the spinal cord in the rat. Exp Brain Res 119 : 356- 366, 1998 https://doi.org/10.1007/s002210050351
  27. Miura A, Kawatani M, De Groat WC : Excitatory synaptic currents in lumbosacral parasympathetic preganglionic neurons evoked by stimulation of the dorsal commissure. J Neurophysiol 89 : 382- 389, 2003 https://doi.org/10.1152/jn.00180.2002
  28. Reuss MH, Reuss S : Nitric oxide synthase neurons in the rodent spinal cord : distribution, relation to Substance P fibers, and effects of dorsal rhizotomy. J Chem Neuroanat 21 : 181-196, 2001 https://doi.org/10.1016/S0891-0618(01)00091-6
  29. Rosen LB, Ginty DD, Weber MJ, Greenberg ME : Membrane depolarization and calcium influx stimulate MEK and MAP kinase via activation of Ras. Neuron 12 : 1207-1221, 1994 https://doi.org/10.1016/0896-6273(94)90438-3
  30. Seger R, Krebs EG : The MAPK signaling cascade. Faseb J 9 : 726- 735, 1995 https://doi.org/10.1096/fasebj.9.9.7601337
  31. Spike RC, Puskar Z, Andrew D, Todd AJ : A quantitative and morphological study of projection neurons in lamina I of the rat lumbar spinal cord. Eur J Neurosci 18 : 2433-2448, 2003 https://doi.org/10.1046/j.1460-9568.2003.02981.x
  32. Springell DA, Costin NS, Pilowsky PM, Goodchild AK : Hypotension and short-term anaesthesia induce ERK1/2 phosphorylation in autonomic nuclei of the brainstem. Eur J Neurosci 22 : 2257- 2270, 2005 https://doi.org/10.1111/j.1460-9568.2005.04413.x
  33. Sweatt JD : The neuronal MAP kinase cascade : a biochemical signal integration system subserving synaptic plasticity and memory. J Neurochem 76 : 1-10, 2001 https://doi.org/10.1046/j.1471-4159.2001.00054.x
  34. Todd AJ : Anatomy of primary afferents and projection neurones in the rat spinal dorsal horn with particular emphasis on substance P and the neurokinin 1 receptor. Exp Physiol 87 : 245-249, 2002 https://doi.org/10.1113/eph8702351
  35. Tominaga M, Caterina MJ, Malmberg AB, Rosen TA, Gilbert H, Skinner K, et al : The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 21 : 531-543, 1998 https://doi.org/10.1016/S0896-6273(00)80564-4
  36. Valtschanoff JG, Weinberg RJ, Rustioni A : NADPH diaphorase in the spinal cord of rats. J Comp Neurol 321 : 209-222, 1992 https://doi.org/10.1002/cne.903210204
  37. Vizzard MA : Increased expression of neuronal nitric oxide synthase in bladder afferent and spinal neurons following spinal cord injury. Dev Neurosci 19 : 232-246, 1997 https://doi.org/10.1159/000111212
  38. Vizzard MA : Increased expression of spinal cord Fos protein induced by bladder stimulation after spinal cord injury. Am J Physiol Regul Integr Comp Physiol 279 : R295-305, 2000 https://doi.org/10.1152/ajpregu.2000.279.1.R295
  39. Wall PD, Kerr BJ, Ramer MS : Primary afferent input to and receptive field properties of cells in rat lumbar area X. J Comp Neurol 449 : 298-306, 2002 https://doi.org/10.1002/cne.10294
  40. Widmann C, Gibson S, Jarpe MB, Johnson GL : Mitogen-activated protein kinase : conservation of a three-kinase module from yeast to human. Physiol Rev 79 : 143-180, 1999 https://doi.org/10.1152/physrev.1999.79.1.143
  41. Xu Z, Wang BR, Ding YQ, Kuang F, Wang X, Duan XL, et al : Extracellular signal-regulated kinases1/2 in neurons of the dorsal motor nucleus of the vagus nerve and nucleus of the solitary tract are activated by noxious visceral stimulus in mice. Neurosci Lett 334 : 103-106, 2002 https://doi.org/10.1016/S0304-3940(02)01113-8
  42. Youm JY, Kim Y : Study on the nNOS expression in the rat spinal cord of the spinal nerve ligation model with neuropathic pain and the dorsal rhizotomy. J Korean Neuorsurg Soc 29 : 877-885, 2000
  43. Zhang X, Verge V, Wiesenfeld-Hallin Z, Ju G, Bredt D, Synder SH, et al : Nitric oxide synthase-like immunoreactivity in lumbar dorsal root ganglia and spinal cord of rat and monkey and effect of peripheral axotomy. J Comp Neurol 335 : 563-575, 1993 https://doi.org/10.1002/cne.903350408