Characteristics of dorsal root ganglia neurons sensitive to Substance P
详细信息    查看全文
  • 作者:Eder Ricardo Moraes (1)
    Christopher Kushmerick (1)
    Ligia Araujo Naves (1)

    1. Departamento de Fisiologia e Biof铆sica ICB
    ; Universidade Federal de Minas Gerais ; Belo Horizonte ; MG ; 31270-901 ; Brasil
  • 关键词:Dorsal root ganglia ; Substance P ; Acid sensing ion channels ; P2X channels ; TRPV1 channel
  • 刊名:Molecular Pain
  • 出版年:2014
  • 出版时间:December 2014
  • 年:2014
  • 卷:10
  • 期:1
  • 全文大小:586 KB
  • 参考文献:1. Belmonte, C, Viana, F (2008) Molecular and cellular limits to somatosensory specificity. Mol Pain 4: pp. 14 CrossRef
    2. Tandrup, T (2004) Unbiased estimates of number and size of rat dorsal root ganglion cells in studies of structure and cell survival. J Neurocytol 33: pp. 173-192 CrossRef
    3. Harper, AA, Lawson, SN (1985) Conduction velocity is related to morphological cell type in rat dorsal root ganglion neurones. J Physiol 359: pp. 31-46 CrossRef
    4. Petruska, JC, Napaporn, J, Johnson, RD, Gu, JG, Cooper, BY (2000) Subclassified acutely dissociated cells of rat DRG: histochemistry and patterns of capsaicin-, proton-, and ATP-activated currents. J Neurophysiol 84: pp. 2365-2379
    5. Taddese, A, Nah, SY, McCleskey, EW (1995) Selective opioid inhibition of small nociceptive neurons. Science 270: pp. 1366-1369 CrossRef
    6. Ribeiro-da-Silva, A, H枚kfelt, T (2000) Neuroanatomical localisation of Substance P in the CNS and sensory neurons. Neuropeptides 34: pp. 256-271 CrossRef
    7. Harrison, S, Geppetti, P (2001) Substance P. Int J Biochem Cell Biol 33: pp. 555-576 CrossRef
    8. Nichols, ML, Allen, BJ, Rogers, SD, Ghilardi, JR, Honore, P, Luger, NM, Finke, MP, Li, J, Lappi, DA, Simone, DA, Mantyh, PW (1999) Transmission of chronic nociception by spinal neurons expressing the substance P receptor. Science 286: pp. 1558-1561 CrossRef
    9. Suzuki, R, Morcuende, S, Webber, M, Hunt, SP, Dickenson, AH (2002) Superficial NK1-expressing neurons control spinal excitability through activation of descending pathways. Nat Neurosci 5: pp. 1319-1326 CrossRef
    10. Li, HS, Zhao, ZQ (1998) Small sensory neurons in the rat dorsal root ganglia express functional NK-1 tachykinin receptor. Eur J Neurosci 10: pp. 1292-1299 CrossRef
    11. Abdulla, FA, Stebbing, MJ, Smith, PA (2001) Effects of substance P on excitability and ionic currents of normal and axotomized rat dorsal root ganglion neurons. Eur J Neurosci 13: pp. 545-552 CrossRef
    12. Sculptoreanu, A, de Groat, WC (2003) Protein kinase C is involved in neurokinin receptor modulation of N- and L-type Ca2+ channels in DRG neurons of the adult rat. J Neurophysiol 90: pp. 21-31 CrossRef
    13. Sculptoreanu, A, de Groat, WC (2007) Neurokinins enhance excitability in capsaicin-responsive DRG neurons. Exp Neurol 205: pp. 92-100 CrossRef
    14. Sculptoreanu, A, Artim, DE, de Groat, WC (2009) Neurokinins inhibit low threshold inactivating K鈥?鈥塩urrents in capsaicin responsive DRG neurons. Exp Neurol 219: pp. 562-573 CrossRef
    15. Park, CK, Bae, JH, Kim, HY, Jo, HJ, Kim, YH, Jung, SJ, Kim, JS, Oh, SB (2010) Substance P sensitizes P2X3 in nociceptive trigeminal neurons. J Dent Res 89: pp. 1154-1159 CrossRef
    16. Zhang, H, Cang, CL, Kawasaki, Y, Liang, LL, Zhang, YQ, Ji, RR, Zhao, ZQ (2007) Neurokinin-1 receptor enhances TRPV1 activity in primary sensory neurons via PKCepsilon: a novel pathway for heat hyperalgesia. J Neurosci 27: pp. 12067-12077 CrossRef
    17. Cang, CL, Zhang, H, Zhang, YQ, Zhao, ZQ (2009) PKCepsilon-dependent potentiation of TTX-resistant Nav1.8 current by neurokinin-1 receptor activation in rat dorsal root ganglion neurons. Mol Pain 5: pp. 33 CrossRef
    18. Lin, CC, Chen, WN, Chen, CJ, Lin, YW, Zimmer, A, Chen, CC (2012) An antinociceptive role for substance P in acid-induced chronic muscle pain. Proc Natl Acad Sci U S A 109: pp. E76-E83 CrossRef
    19. Djouhri, L, Lawson, SN (2001) Differences in the size of the somatic action potential overshoot between nociceptive and non-nociceptive dorsal root ganglion neurones in the guinea-pig. Neuroscience 108: pp. 479-491 CrossRef
    20. Fang, X, McMullan, S, Lawson, SN, Djouhri, L (2005) Electrophysiological differences between nociceptive and non-nociceptive dorsal root ganglion neurones in the rat in vivo. J Physiol 565: pp. 927-943 CrossRef
    21. Perl, ER (2011) Pain mechanisms: a commentary on concepts and issues. Prog Neurobiol 94: pp. 20-38 CrossRef
    22. Burgard, EC, Niforatos, W, van Biesen, T, Lynch, KJ, Touma, E, Metzger, RE, Kowaluk, EA, Jarvis, MF (1999) P2X receptor-mediated ionic currents in dorsal root ganglion neurons. J Neurophysiol 82: pp. 1590-1598
    23. Burnstock, G, Wood, JN (1996) Purinergic receptors: their role in nociception and primary afferent neurotransmission. Curr Opin Neurobiol 6: pp. 526-532 CrossRef
    24. Nakagawa, H (2006) Hiura, A: Capsaicin, transient receptor potential (TRP) protein subfamilies and the particular relationship between capsaicin receptors and small primary sensory neurons. Anat Sci Int 81: pp. 135-155 CrossRef
    25. Poirot, O, Berta, T, Decosterd, I, Kellenberger, S (2006) Distinct ASIC currents are expressed in rat putative nociceptors and are modulated by nerve injury. J Physiol 576: pp. 215-234 CrossRef
    26. Djouhri, L, Lawson, SN (2004) Abeta-fiber nociceptive primary afferent neurons: a review of incidence and properties in relation to other afferent A-fiber neurons in mammals. Brain Res Rev 46: pp. 131-145 CrossRef
    27. Yagi, J, Wenk, HN, Naves, LA, McCleskey, EW (2006) Sustained currents through ASIC3 ion channels at the modest pH changes that occur during myocardial ischemia. Circ Res 99: pp. 501-509 CrossRef
    28. Dussor, G, Zylka, MJ, Anderson, DJ, McCleskey, EW (2008) Cutaneous sensory neurons expressing the Mrgprd receptor sense extracellular ATP and are putative nociceptors. J Neurophysiol 99: pp. 1581-1589 CrossRef
    29. Guo, A, Vulchanova, L, Wang, J, Li, X, Elde, R (1999) Immunocytochemical localization of the vanilloid receptor 1 (VR1): relationship to neuropeptides, the P2X3 purinoceptor and IB4 binding sites. Eur J Neurosci 11: pp. 946-958 CrossRef
    30. Michael, GJ, Priestley, JV (1999) Differential expression of the mRNA for the vanilloid receptor subtype 1 in cells of the adult rat dorsal root and nodose ganglia and its downregulation by axotomy. J Neurosci 19: pp. 1844-1854
    31. Petersen, M, LaMotte, RH (1991) Relationships between capsaicin sensitivity of mammalian sensory neurons, cell size and type of voltage gated Ca-currents. Brain Res 561: pp. 20-26 CrossRef
    32. Pearce, RJ, Duchen, MR (1994) Differential expression of membrane currents in dissociated mouse primary sensory neurons. Neuroscience 63: pp. 1041-1056 CrossRef
    33. Olson, TH, Riedl, MS, Vulchanova, L, Ortiz-Gonzalez, XR, Elde, R (1998) An acid sensing ion channel (ASIC) localizes to small primary afferent neurons in rats. Neuroreport 9: pp. 1109-1113 CrossRef
    34. Alvarez de la Rosa, D, Zhang, P, Shao, D, White, F, Canessa, CM (2002) Functional implications of the localization and activity of acid-sensitive channels in rat peripheral nervous system. Proc Natl Acad Sci U S A 99: pp. 2326-2331 CrossRef
    35. Lin, YW, Min, MY, Lin, CC, Chen, WN, Wu, WL, Yu, HM, Chen, CC (2008) Identification and characterization of a subset of mouse sensory neurons that express acid-sensing ion channel 3. Neuroscience 151: pp. 544-557 CrossRef
    36. Boer, PA, Ueno, M, Sant鈥檃na, JS, Saad, MJ, Gontijo, JA (2005) Expression and localization of NK(1)R, substance P and CGRP are altered in dorsal root ganglia neurons of spontaneously hypertensive rats (SHR). Mol Brain Res 138: pp. 35-44 CrossRef
    37. Jafri, MS, Weinreich, D (1998) Substance P regulates Ih via a NK-1 receptor in vagal sensory neurons of the ferret. J Neurophysiol 79: pp. 769-777
    38. Jafri, MS, Weinreich, D (1996) Substance P hyperpolarizes vagal sensory neurones of the ferret. J Physiol Lond 494: pp. 907
    39. Akopian, AN, Souslova, V, England, S, Okuse, K, Ogata, N, Ure, J, Smith, A, Kerr, BJ, McMahon, SB, Boyce, S, Hill, R, Stanfa, LC, Dickenson, AH, Wood, JN (1999) The tetrodotoxin-resistant sodium channel SNS has a specialized function in pain pathways. Nat Neurosci 2: pp. 541-548 CrossRef
    40. Bell, TJ, Thaler, C, Castiglioni, AJ, Helton, TD, Lipscombe, D (2004) Cell-specific alternative splicing increases calcium channel current density in the pain pathway. Neuron 41: pp. 127-138 CrossRef
    41. Wang, R, Lewin, GR (2011) The Cav3.2 T-type calcium channel regulates temporal coding in mouse mechanoreceptors. J Physiol 589: pp. 2229-2243 CrossRef
    42. Teichert, RW, Memon, T, Aman, JW, Olivera, BM (2014) Using constellation pharmacology to define comprehensively a somatosensory neuronal subclass. Proc Natl Acad Sci U S A 111: pp. 2319-2324 CrossRef
    43. Vulchanova, L, Riedl, MS, Shuster, SJ, Stone, LS, Hargreaves, KM, Buell, G, Surprenant, A, North, RA, Elde, R (1998) P2X3 is expressed by DRG neurons that terminate in inner lamina II. Eur J Neurosci 10: pp. 3470-3478 CrossRef
    44. Deval, E, No毛l, J, Gasull, X, Delaunay, A, Alloui, A, Friend, V, Eschalier, A, Lazdunski, M, Lingueglia, E (2011) Acid-Sensing Ion Channels in Postoperative Pain. J Neurosci 31: pp. 6059-6066 CrossRef
    45. Chen, CC, Wong, CW (2013) Neurosensory mechanotransduction through acid-sensing ion channels. J Cell Mol Med 17: pp. 337-349 CrossRef
    46. Wemmie, JA, Taugher, RJ, Kreple, CJ (2013) Acid-sensing ion channels in pain and disease. Nat Rev Neurosci 14: pp. 461-471 CrossRef
    47. Jankowski, MP, Rau, KK, Ekmann, KM, Anderson, CE, Koerber, HR (2013) Comprehensive phenotyping of group III and IV muscle afferents in mouse. J Neurophysiol 109: pp. 2374-2381 CrossRef
    48. Price, MP, McIlwrath, SL, Xie, J, Cheng, C, Qiao, J, Tarr, DE, Sluka, KA, Brennan, TJ, Lewin, GR, Welsh, MJ (2001) The DRASIC cation channel contributes to the detection of cutaneous touch and acid stimuli in mice. Neuron 32: pp. 1071-1083 CrossRef
    49. Page, AJ, Brierley, SM, Martin, CM, Price, MP, Symonds, E, Butler, R, Wemmie, JA, Blackshaw, LA (2005) Different contributions of ASIC channels 1a, 2, and 3 in gastrointestinal mechanosensory function. Gut 54: pp. 1408-1415 CrossRef
    50. Ditting, T, Tiegs, G, Rodionova, K, Reeh, PW, Neuhuber, W, Freisinger, W, Veelken, R (2009) Do distinct populations of dorsal root ganglion neurons account for the sensory peptidergic innervation of the kidney?. Am J Physiol Renal Physiol 297: pp. F1427-F1434 CrossRef
    51. Molliver, DC, Immke, DC, Fierro, L, Par茅, M, Rice, FL, McCleskey, EW (2005) ASIC3, an acid-sensing ion channel, is expressed in metaboreceptive sensory neurons. Mol Pain 1: pp. 35 CrossRef
    52. Lawson, SN, Crepps, B, Perl, ER (2002) Calcitonin gene-related peptide immunoreactivity and afferent receptive properties of dorsal root ganglion neurones in guinea-pigs. J Physiol 540: pp. 989-1002 CrossRef
    53. Light, AR, Hughen, RW, Zhang, J, Rainier, J, Liu, Z, Lee, J (2008) Dorsal root ganglion neurons innervating skeletal muscle respond to physiological combinations of protons, ATP, and lactate mediated by ASIC, P2X, and TRPV1. J Neurophysiol 100: pp. 1184-1201 CrossRef
    54. Fromy, B, Lingueglia, E, Sigaudo-Roussel, D, Saumet, JL, Lazdunski, M (2012) ASIC3 is a neuronal mechanosensor for pressure-induced vasodilation that protects against pressure ulcers. Nat Med 18: pp. 1205-1207 CrossRef
    55. Eckert, SP, Taddese, A, McCleskey, EW (1997) Isolation and culture of rat sensory neurons having distinct sensory modalities. J Neurosci Methods 77: pp. 183-190 CrossRef
    56. Hamill, OP, Marty, A, Neher, E, Sakmann, B, Sigworth, FJ (1981) Improved patch-clamp techniques for high-resolution current recording from cells and cell-free membrane patches. Pflugers Arch 391: pp. 85-100 CrossRef
    57. Jarvis, MF, Khakh, BS (2009) ATP-gated P2X cation-channels. Neuropharmacology 56: pp. 208-215 CrossRef
    58. Caterina, MJ, Schumacher, MA, Tominaga, M, Rosen, TA, Levine, JD, Julius, D (1997) The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389: pp. 816-824 CrossRef
    59. Burnham, KP, Anderson, DR (2002) Model Selection and Multimodel Inference. A Practical Information-Theoretic Approach. Springer-Verlag, New York
  • 刊物主题:Pain Medicine; Molecular Medicine;
  • 出版者:BioMed Central
  • ISSN:1744-8069
文摘
Background Substance P modulates ion channels and the excitability of sensory neurons in pain pathways. Within the heterogeneous population of Dorsal Root Ganglia (DRG) primary sensory neurons, the properties of cells that are sensitive to Substance P are poorly characterized. To define this population better, dissociated rat DRG neurons were tested for their responsiveness to capsaicin, ATP and acid. Responses to ATP were classified according to the kinetics of current activation and desensitization. The same cells were then tested for modulation of action potential firing by Substance P. Results Acid and capsaicin currents were more frequently encountered in the largest diameter neurons. P2X3-like ATP currents were concentrated in small diameter neurons. Substance P modulated the excitability in 20 of 72 cells tested (28%). Of the Substance P sensitive cells, 10 exhibited an increase in excitability and 10 exhibited a decrease in excitability. There was no significant correlation between sensitivity to capsaicin and to Substance P. Excitatory effects of Substance P were strongly associated with cells that had large diameters, fired APs with large overshoots and slowly decaying after hyperpolarizations, and expressed acid currents at pH 7. No neurons that were excited by Substance P presented P2X3-like currents. In contrast, neurons that exhibited inhibitory effects of Substance P fired action potentials with rapidly decaying after hyperpolarizations. Conclusion We conclude that excitatory effects of Substance P are restricted to a specific neuronal subpopulation with limited expression of putative nociceptive markers.
NGLC 2004-2010.National Geological Library of China All Rights Reserved.
Add:29 Xueyuan Rd,Haidian District,Beijing,PRC. Mail Add: 8324 mailbox 100083
For exchange or info please contact us via email.