Distribution and localization of 5-HT 1A receptors in the rat lumbar spinal cord after transection and deafferentation

Journal of Neurotrauma

Volumn 26, Issue 4, 2009, Pages 575-584

  Otoshi, Chad K ^a   Walwyn, Wendy M ^a   Tillakaratne, Niranjala J K ^a   Zhong, Hui ^a   Roy, Roland R ^a   Edgerton, V Reggie ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

5 HT1A receptor; Afferent input; serotonin; spinal cord isolation; spinal cord transection

Indexed keywords

SEROTONIN 1A RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; CONTROLLED STUDY; DEAFFERENTATION; DENDRITE; FEMALE; LUMBAR SPINAL CORD; NONHUMAN; RAT; SENSORY STIMULATION; TOPOGRAPHY; UPREGULATION;

ANIMALS; ANTIBODIES; ANTIBODY SPECIFICITY; AXONS; CELL COUNT; DENDRITES; DENERVATION; DISEASE MODELS, ANIMAL; FEMALE; IMMUNOHISTOCHEMISTRY; LUMBAR VERTEBRAE; NEURONAL PLASTICITY; POSTERIOR HORN CELLS; PROTEIN STRUCTURE, TERTIARY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, SEROTONIN, 5-HT1A; RHIZOTOMY; SENSATION; SEROTONIN; SPINAL CORD INJURIES; SPINE; UP-REGULATION;

EID: 64849104329     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2008.0640     Document Type: Article

References (71)

1. Alaimo, M., Smith, J.L., Roy, R.R., and Edgerton, V.R. (1984). EMG activity of slow and fast ankle extensors following spinal cord transection. J. Appl. Physiol. 56, 1608-1613.
2. Anden, N.E., Haeggendal, J., Magnusson, T., and Rosengren, E. (1964). The time course of the disappearance of noradrenaline and 5-hydroxytryptamine in the spinal cord after transection. Acta Physiol. Scand. 62, 115-118.
3. Andrade, R., Malenka, R.C., and Nicoll, R.A. (1986). A G protein couples serotonin and GABAB receptors to the same channels in hippocampus. Science 234, 1261-1265.
4. Anthony, T.E., and Azmitia, E.C. (1997). Molecular characterization of antipeptide antibodies against the 5-HT1A receptor: evidence for state-dependent antibody binding. Brain Res. Mol. Brain Res. 50, 277-284.
5. Antri, M., Barthe, J.Y., Mouffle, C., and Orsal, D. (2005). Long-lasting recovery of locomotor function in chronic spinal rat following chronic combined pharmacological stimulation of serotonergic receptors with 8-OH-DPAT and quipazine. Neurosci. Lett. 384, 162-167.
6. Azmitia, E.C., Gannon, P.J., Kheck, N.M., and Whitaker-Azmitia, P.M. (1996). Cellular localization of the 5-HT1A receptor in primate brain neurons and glial cells. Neuropsychopharma-cology 14, 35-46.
7. Azmitia, E.C., Yu, I., Akbari, H.M., Kheck, N., Whitaker-Azmitia, P.M., and Marshak, D.R. (1992). Antipeptide antibodies against the 5-HT1A receptor. J. Chem. Neuroanat. 5, 289-298.
8. Barbeau, H., and Rossignol, S. (1990). The effects of serotonergic drugs on the locomotor pattern and on cutaneous reflexes of the adult chronic spinal cat. Brain Res. 514, 55-67.
9. Bowker, R.M., Westlund, K.N., and Coulter, J.D. (1981). Origins of serotonergic projections to the spinal cord in rat: an immunocy-tochemical- retrograde transport study. Brain Res. 226, 187-199.
10. Cai, L.L., Fong, A.J., Otoshi, C.K., Liang, Y., Burdick, J.W., Roy, R.R., and Edgerton, V.R. (2006). Implications of assist-as-needed robotic step training after a complete spinal cord injury on intrinsic strategies of motor learning. J. Neurosci. 26, 10564-10568.
11. Chalmers, G.R., Roy, R.R., and Edgerton, V.R. (1992). Adaptability of the oxidative capacity of motoneurons. Brain Res. 570, 1-10.
12. Claustre, Y., Benavides, J., and Scatton, B. (1988). 5-HT1A receptor agonists inhibit carbachol-induced stimulation of phospho-inositide turnover in the rat hippocampus. Eur. J. Pharmacol. 149, 149-153.
13. Courtine, G., Song, B., Roy, R.R., Zhong, H., Herrmann, J.M., Ao, Y., Edgerton, V.R., and Sofroniew, M.V. (2008). Recovery of supraspinal control of stepping mediated by indirect pro-priospinal relay connections after severe spinal cord injury. Nature Med. 14, 69-74.
14. Daval, G., Verge, D., Basbaum, A.I., Bourgoin, S., and Hamon, M. (1987). Autoradiographic evidence of serotonin 1 binding sites on primary afferent fibers in the dorsal horn of the rat spinal cord. Neurosci. Lett. 83, 71-76.
15. Dutton, R.C., Carsten, M.I., Antognini, J.F., and Carsten, E. (2006). Long ascending propriospinal projections from lum-bosacral to upper cervical spinal cord in the rat. Brain Res. 1119, 76-85.
16. Edgerton, V.R., Courtine, G., Gerasimenko, Y.P., Lavrov, I., Ichiyama, R.M., Fong, A.J., Cai, L.L., Otoshi, C.K., Tillakar-atne, N.J., Burdick, J.W., and Roy, R.R. (2008). Training loco-motor networks. Brain Res. Rev. 57, 241-254.
17. Edgerton, V.R., Kim, S.J., Ichiyama, R.M., Gerasimenko, Y.P., and Roy, R.R. (2006). Rehabilitative therapies after spinal cord injury. J. Neurotrauma 23, 560-570.
18. El Mestikawy, S., Riad, M., Laporte, A.M., Verge, D., Daval, G., Gozlan, H., and Hamon, M. (1990). Production of specific anti-rat 5-HT1A receptor antibodies in rabbits injected with a synthetic peptide. Neurosci. Lett. 118, 189-192.
19. Fong, A.J., Cai, L.L., Otoshi, C.K., Reinkensmeyer, D.J., Burdick, J.W., Roy, R.R., and Edgerton, V.R. (2005). Spinal cord-transected mice learn to step in response to quipazine treatment and robotic training. J. Neurosci. 25, 11738-11747.
20. Friedman, B., Kleinfeld, D., Ip, N.Y., Verge, V.M., Moulton, R., Boland, P., Zlotchenko, E., Lindsay, R.M., and Liu, L. (1995). BDNF and NT-4/5 exert neurotrophic influences on injured adult spinal motor neurons. J. Neurosci. 15, 1044-1056.
21. Garnovskaya, M.N., Gettys, T.W., van Biesen, T., Prpic, V., Chuprun, J.K., and Raymond, J.R. (1997). 5-HT1A receptor activates Na+/H+ exchange in CHO-K1 cells through Gial-pha2 and Gialpha3. J. Biol. Chem. 272, 7770-7776.
22. Garnovskaya, M.N., Mukhin, Y., and Raymond, J.R. (1998). Rapid activation of sodium-proton exchange and extracellular signal-regulated protein kinase in fibroblasts by G-protein-coupled 5-HT1A receptor involves distinct signaling cascades. Biochem. J. 330, 489-495.
23. Garnovskaya, M.N., van Biesen, T., Hawe, B., Casanas Ramos, S., Lefkowitz, R.J., and Raymond, J.R. (1996). Ras-dependent activation of fibroblast mitogen-activated protein kinase by 5-HT1A receptor via a G protein beta gamma-subunit-initiated pathway. Biochemistry 35, 13716-13722.
24. Giroux, N., Rossignol, S., and Reader, T.A. (1999). Autoradio-graphic study of alpha1- and alpha2-noradrenergic and serotonin1A receptors in the spinal cord of normal and chronically transected cats. J. Comp. Neurol. 406, 402-414.
25. Gomez-Pinilla, F., Ying, Z., Roy, R.R., Hodgson, J.A., and Edgerton, V.R. (2004). Afferent input modulates neurotrophins and syn-aptic plasticity in the spinal cord. J. Neurophysiol. 92, 3423-3432.
26. Grossman, E.J., Roy, R.R., Talmadge, R.J., Zhong, H., and Edgerton, V.R. (1998). Effects of inactivity on myosin heavy chain composition and size of rat soleus fibers. Muscle Nerve 21, 375-389.
27. Grunnet, M., Jespersen, T., and Perrier, J.F. (2004). 5-HT1A receptors modulate small-conductance Ca2+-activated K+ channels. J. Neurosci. Res. 78, 845-854.
28. Hains, B.C., Willis, W.D., and Hulsebosch, C.E. (2003). Serotonin receptors 5-HT1A and 5-HT3 reduce hyperexcitability of dorsal horn neurons after chronic spinal cord hemisection injury in rat. Exp. Brain Res. 149, 174-186.
29. Hochman, S., Garraway, S.M., Machacek, D.W., and Shay, B.L. (2001). 5-HT receptors and the neuromodulatory control of spinal cord function, in: Motor Neurobiology of the Spinal Cord. T.C. Cope (ed), CRC Press: Boca Raton, FL, pps. 47-87.
30. Kao, T., Shumsky, J.S., Jacob-Vadakot, S., Himes, B.T., Murray, M., and Moxon, K.A. (2006). Role of the 5-HT2C receptor in improving weight-supported stepping in adult rats spinalized as neonates. Brain Res. 1112, 159-168.
31. Kemp, B.E., and Pearson, R.B. (1990). Protein kinase recognition sequence motifs. Trends Biochem. Sci. 15, 342-346.
32. Kheck, N.M., Gannon, P.J., and Azmitia, E.C. (1995). 5-HT1A receptor localization on the axon hillock of cervical spinal motoneurons in primates. J. Comp. Neurol. 355, 211-220.
33. Kia, H.K., Miquel, M.C., Brisorgueil, M.J., Daval, G., Riad, M., El Mestikawy, S., Hamon, M., and Verge, D. (1996). Immuno-cytochemical localization of serotonin1A receptors in the rat central nervous system. J. Comp. Neurol. 365, 289-305.
34. Kiehn, O. (2006). Locomotor circuits in the mammalian spinal cord. Annu. Rev. Neurosci. 29, 279-306.
35. Kim, D., Adipudi, V., Shibayama, M., Giszter, S., Tessler, A., Murray, M., and Simansky, K.J. (1999). Direct agonists for serotonin receptors enhance locomotor function in rats that received neural transplants after neonatal spinal transection. J. Neurosci. 19, 6213-6224.
36. Kossel, A., Lowel, S., and Bolz, J. (1995). Relationships between dendritic fields and functional architecture in striate cortex of normal and visually deprived cats. J. Neurosci. 15, 3913-3926.
37. Kubasak, M.D., Hedlund, E., Roy, R.R., Carpenter, E.M., Edge-rton, V.R., and Phelps, P.E. (2005). L1 CAM expression is increased surrounding the lesion site in rats with complete spinal cord transection as neonates. Exp. Neurol. 194, 363-375.
38. Kubasak, M.D., Jindrich, D.L., Zhong, H., Takeoka, A., McFar-land, K.C., Minoz-Quiles, C., Roy, R.R., Edgerton, V.R., Ramon-Cueto, A., and Phelps, P.E. (2008). OEG implantation and step training enhance hindlimb-stepping ability in adult spinal transected rats. Brain 131, 264-276.
39. Laporte, A.M., Fattaccini, C.M., Lombard, M.C., Chauveau, J., and Hamon, M. (1995). Effects of dorsal rhizotomy and selective lesion of serotonergic and noradrenergic systems on 5-HT1A, 5-HT1B, and 5-HT3 receptors in the rat spinal cord. J. Neural. Transm. Gen. Sect. 100, 207-223.
40. Makman, M.H., Dvorkin, B., and Crain, S.M. (1988). Modulation of adenylate cyclase activity of mouse spinal cord-ganglion explants by opioids, serotonin and pertussis toxin. Brain Res. 445, 303-313.
41. Malmberg, A., and Strange, P.G. (2000). Site-directed mutations in the third intracellular loop of the serotonin 5-HT(1A) receptor alter G protein coupling from G(i) to G(s) in a ligand-dependent manner. J. Neurochem. 75, 1283-1293.
42. Mannouryla Cour, C.,ElMestikawy, S., Hanoun, N., Hamon, M., and Lanfumey, L. (2006). Regional differences in the coupling of 5-hydroxytryptamine-1A receptors to G proteins in the rat brain. Mol. Pharmacol. 70, 1013-1021.
43. Marlier, L., Poulat, P., Rajaofetra, N., and Privat, A. (1991b). Modification of serotonergic immunoreactive pattern in the dorsal horn of the rat spinal cord following dorsal root rhi-zotomy. Neurosci. Lett. 128, 9-12.
44. Marlier, L., Poulat, P., Rajaofetra, N., and Privat, A. (1991c). Modifications of serotonin-, substance P- and calcitonin gene-related peptide-like immunoreactivities in the dorsal horn of the spinal cord of arthritic rats: a quantitative immunocyto-chemical study. Exp. Brain Res. 85, 482-490.
45. Marlier, L., Rajaofetra, N., Poulat, P., and Privat, A. (1990). Modification of serotonergic innervation of the rat spinal cord dorsal horn after neonatal capsaicin treatment. J. Neurosci. Res. 25, 112-118.
46. Marlier, L., Teilhac, J.R., Cerruti, C., and Privat, A. (1991a). Autoradiographic mapping of 5-HT1, 5-HT1A, 5-HT1B and 5-HT2 receptors in the rat spinal cord. Brain Res. 550, 15-23.
47. Marty, S., Berzaghi Mda, P., and Berninger, B. (1997). Neuro-trophins and activity-dependent plasticity of cortical inter-neurons. Trends Neurosci. 20, 198-202.
48. Nenonene, E.K., Radja, F., Carli, M., Grondin, L., and Reader, T.A. (1994). Heterogeneity of cortical and hippocampal 5-HT1A receptors: a reappraisal of homogenate binding with 8-[3H] hydroxydipropylaminotetralin. J. Neurochem. 62, 1822-1834.
49. Newton, B.W., and Hamill, R.W. (1988). The morphology and distribution of rat serotonergic intraspinal neurons: an im-munohistochemical study. Brain Res. Bull. 20, 349-360.
50. Okada, F., Tokumitsu, Y., and Nomura, Y. (1989). Pertussis toxin attenuates 5-hydroxytryptamine1A receptor-mediated inhibition of forskolin-stimulated adenylate cyclase activity in rat hippocampal membranes. J. Neurochem. 52, 1566-1569.
51. Oleskevich, S., Leck, K.J., Matthaei, K., and Hendry, I.A. (2005). Enhanced serotonin response in the hippocampus of Galphaz protein knock-out mice. Neuroreport 16, 921-925.
52. Otoshi, C.K., Fong, A.J., Cai, L.L., Zhong, H., Roy, R.R., Tilla-karatne, N.J.K., and Edgerton, V.R. (2004). Changes in 5-HT1A receptor distribution following spinal cord transection are dependent upon spinal 5-HT content and peripheral sensory input in adult rats. In: Society for Neuroscience 34th Annual Meeting; Oct. 23-27; San Diego, CA; 418.11.
53. Perrier, J.F., Alaburda, A., and Hounsgaard, J. (2003). 5-HT1A receptors increase excitability of spinal motoneurons by inhibiting a TASK-1-like K+ current in the adult turtle. J. Phy-siol. 548, 485-492.
54. Raymond, J.R., Fargin, A., Middleton, J.P., Graff, J.M., Haupt, D.M., Caron, M.G., Lefkowitz, R.J., and Dennis, V.W. (1989). The human 5-HT1A receptor expressed in HeLa cells stimulates sodium-dependent phosphate uptake via protein kinase C. J. Biol. Chem. 264, 21943-21950.
55. Riad, M., Garcia, S., Watkins, K.C., Jodoin, N., Doucet, E., Lan-glois, X., el Mestikawy, S., Hamon, M., and Descarries, L. (2000). Somatodendritic localization of 5-HT1A and preter-minal axonal localization of 5-HT1B serotonin receptors in adult rat brain. J. Comp. Neurol. 417, 181-194.
56. Roy, R.R., Hodgson, J.A., Lauretz, S.D., Pierotti, D.J., Gayek, R.J., and Edgerton, V.R. (1992). Chronic spinal cord-injured cats: surgical procedures and management. Lab. Anim. Sci. 42, 335-343.
57. Roy, R.R., Kim, J.A., Grossman, E.J., Bekmezian, A., Talmadge, R.J., Zhong, H., and Edgerton, V.R. (2000). Persistence of myosin heavy chain-based fiber types in innervated but silenced rat fast muscle. Muscle Nerve 23, 735-747.
58. Roy, R.R., Matsumoto, A., Zhong, H., Ishihara, A., and Edge-rton, V.R. (2007a). Rat α- and γ-motoneuron soma size and succinate dehydrogenase activity are independent of neuro-muscular activity level. Muscle Nerve 36, 234-241.
59. Roy, R.R., Zhong, H., Khalili, N., Kim, S.J., Higuchi, N., Monti, R.J., Grossman, E., Hodgson, J.A., and Edgerton, V.R. (2007b). Is spinal cord isolation a good model of muscle disuse? Muscle Nerve 35, 312-321.
60. Sauer, H., Wong, V., and Bjorklund, A. (1995). Brain-derived neurotrophic factor and neurotrophin-4/5 modify neurotrans-mitter-related gene expression in the 6-hydroxydopamine-lesioned rat striatum. Neuroscience 65, 927-933.
61. Schmidt, B.J., and Jordan, L.M. (2000). The role of serotonin in reflex modulation and locomotor rhythm production in the mammalian spinal cord. Brain Res. Bull. 53, 689-710.
62. Talmadge, R.J., Garcia, N.D., Roy, R.R., and Edgerton, V.R. (2004). Myosin heavy chain isoform mRNA and protein levels after long-term paralysis. Biochem. Biophys. Res. Commun. 325, 296-301.
63. Talmadge, R.J., Roy, R.R., Caiozzo, V.J., and Edgerton, V.R. (2002). Mechanical properties of rat soleus after long-term spinal cord transection. J. Appl. Physiol. 93, 1487-1497.
64. Thor, K.B., Nickolaus, S., and Helke, C.J. (1993). Auto-radiographic localization of 5-hydroxytryptamine1A, 5-hydroxytryptamine1B and 5-hydroxytryptamine1C/2 binding sites in the rat spinal cord. Neuroscience 55, 235-252.
65. Turner, J.H., Gelasco, A.K., and Raymond, J.R. (2004). Calmo-dulin interacts with the third intracellular loop of the serotonin 5-hydroxytryptamine1A receptor at two distinct sites: putative role in receptor phosphorylation by protein kinase C. J. Biol. Chem. 279, 17027-17037.
66. Weber, E.D., and Stelzner, D.J. (1977). Behavioral effects of spinal cord transection in the developing rat. Brain Res. 125, 241-255.
67. Wu, X., Kushwaha, N., Albert, P.R., and Penington, N.J. (2002). A critical protein kinase C phosphorylation site on the 5-HT(1A) receptor controlling coupling to N-type calcium channels. J. Physiol. 538, 41-51.
68. Yakovenko, S., Kowalczewski, J., and Prochazka, A. (2007). In-traspinal stimulation caudal to spinal cord transections in rats. Testing the propriospinal hypothesis. J. Neurophysiol. 97, 2570-2574.
69. Zgombick, J.M., Beck, S.G., Mahle, C.D., Craddock-Royal, B., and Maayani, S. (1989). Pertussis toxin-sensitive guanine nucleotide-binding protein(S) couple adenosine A1 and 5-hydroxytryptamine1A receptors to the same effector systems in rat hippocampus: biochemical and electrophysiological studies. Mol. Pharmacol. 35, 484-494.
70. Zhang, Y., Gray, T.S., D'Souza, D.N., Carrasco, G.A., Darnjanoska, K.J., Dudas, B., Garcia, F., Zainelli, G.M., Sullivan Hanley, N.R., Battaglia, G., Muma, N.A., and Van de Kar, L.D. (2004). De-sensitization of 5-HT1A receptors by 5-HT2A receptors in neu-roendocrine neurons in vivo. J. Pharmacol. Exp. Ther. 310, 59-66.
71. Zhou, F.C., Patel, T.D., Swartz, D., Xu, Y., and Kelley, M.R. (1999). Production and characterization of an anti-serotonin 1A receptor antibody which detects functional 5-HT1A binding sites. Brain Res. Mol. Brain Res. 69, 186-201.