The time course of serotonin 2C receptor expression after spinal transection of rats: An immunohistochemical study

Neuroscience

Volumn 236, Issue , 2013, Pages 31-46

  Ren, L Q ^a,b   Wienecke, J ^a   Chen, M ^a,b   Moller M ^a   Hultborn, H ^a   Zhang, M ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b CHENGDE MEDICAL COLLEGE   (China)

Author keywords

Immunohistochemistry; Serotonin; Serotonin receptor; Spasticity; Spinal cord injury

Indexed keywords

SEROTONIN 2A RECEPTOR; SEROTONIN 2C RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENDRITE; GRAY MATTER; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MOTONEURON; NERVE EXCITABILITY; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; RAT; SPASTICITY; SPINAL CORD; SPINAL CORD DORSAL HORN; SPINAL CORD INJURY; SPINAL CORD TRANSSECTION; UPREGULATION; WESTERN BLOTTING;

ANIMALS; ANTERIOR HORN CELLS; BLOTTING, WESTERN; DISEASE MODELS, ANIMAL; IMMUNOHISTOCHEMISTRY; INTERNEURONS; MALE; MUSCLE SPASTICITY; RATS; RATS, WISTAR; RECEPTOR, SEROTONIN, 5-HT2C; SPINAL CORD INJURIES; TIME; UP-REGULATION;

EID: 84874357232     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.12.063     Document Type: Article

References (81)

1. Abramowski D., Rigo M., Duc D., Hoyer D., Staufenbiel M. Localization of the 5-hydroxytryptamine2C receptor protein in human and rat brain using specific antisera. Neuropharmacology 1995, 34:1635-1645.
2. Antri M., Barthe J.Y., Mouffle C., Orsal D. Long-lasting recovery of locomotor function in chronic spinal rat following chronic combined pharmacological stimulation of serotonergic receptors with 8-OHDPAT and quipazine. Neurosci Lett 2005, 384:162-167.
3. Antri M., Mouffle C., Orsal D., Barthe J.Y. 5-HT1A receptors are involved in short- and long-term processes responsible for 5-HT-induced locomotor function recovery in chronic spinal rat. Eur J Neurosci 2003, 18:1963-1972.
4. Antri M., Orsal D., Barthe J.Y. Locomotor recovery in the chronic spinal rat: effects of long-term treatment with a 5-HT2 agonist. Eur J Neurosci 2002, 16:467-476.
5. Bancila M., Vergé D., Rampin O., Backstrom J.R., Sanders-Bush E., McKenna K.E., Marson L., Calas A., Giuliano F. 5-Hydroxytryptamine 2C receptors on spinal neurons controlling penile erection in the rat. Neuroscience 1999, 92:1523-1537.
6. Barbeau H., Rossignol S. The effects of serotonergic drugs on the locomotor pattern and on cutaneous reflexes of the adult chronic spinal cat. Brain Res 1990, 514:55-67.
7. Basura G.J., Zhou S.Y., Walker P.D., Goshgarian H.G. Distribution of serotonin 2A and 2C receptor mRNA expression in the cervical ventral horn and phrenic motoneurons following spinal cord hemisection. Exp Neurol 2001, 169:255-263.
8. Bennett D.J., Gorassini M., Fouad K., Sanelli L., Han Y., Cheng J. Spasticity in rats with sacral spinal cord injury. J Neurotrauma 1999, 16:69-84.
9. Bennett D.J., Li Y., Harvey P.J., Gorassini M. Evidence for plateau potentials in tail motoneurons of awake chronic spinal rats with spasticity. J Neurophysiol 2001, 86:1972-1982.
10. Bennett D.J., Li Y., Siu M. Plateau potentials in sacrocaudal motoneurons of chronic spinal rats, recorded in vitro. J Neurophysiol 2001, 86:1955-1971.
11. Bennett D.J., Sanelli L., Cooke C.L., Harvey P.J., Gorassini M.A. Spastic long-lasting reflexes in the awake rat after sacral spinal cord injury. J Neurophysiol 2004, 91:2247-2258.
12. Bhattacharyya S., Raote I., Bhattacharya A., Miledi R., Panicker M.M. Activation, internalization, and recycling of the serotonin 2A receptor by dopamine. Proc Natl Acad Sci U S A 2006, 103:15248-15253.
13. Burns C.M., Chu H., Rueter S.M., Hutchinson L.K., Canton H., Sanders-Bush E., Emeson R.B. Regulation of serotonin-2C receptor G-protein coupling by RNA editing. Nature 1997, 387:303-308.
14. Chen Y., Peng L., Zhang X., Stolzenburg J.U., Hertz L. Further evidence that fluoxetine interacts with a 5-HT2C receptor in glial cells. Brain Res Bull 1995, 38:153-159.
15. Ciechanover A. Intracellular protein degradation: from a vague idea, through the lysosome and the ubiquitin-proteasome system, and onto human diseases and drug targeting (Nobel lecture). Angew Chem Int Ed Engl 2005, 44:5944-5967.
16. Clemett D.A., Punhani T., Duxon M.S., Blackburn T.P., Fone K.C. Immunohistochemical localisation of the 5-HT2C receptor protein in the rat CNS. Neuropharmacology 2000, 39:123-132.
17. Deribe Y.L., Pawson T., Dikic I. Post-translational modifications in signal integration. Nat Struct Mol Biol 2010, 17:666-672.
18. Dietz V. Spastic movement disorder. Spinal Cord 2000, 8:389-393.
19. Doly S., Madeira A., Fischer J., Brisorgueil M.J., Daval G., Bernard R., Verge D., Conrath M. The 5-HT2A receptor is widely distributed in the rat spinal cord and mainly localized at the plasma membrane of postsynaptic neurons. J Comp Neurol 2004, 472:496-511.
20. Eken T., Hultborn H., Kiehn O. Possible functions of transmitter-controlled plateau potentials in alpha motoneurones. Prog Brain Res 1989, 80:257-267.
21. Ferry R.C., Molinoff P.B. Regulation of 5-HT2A receptor mRNA in P11 cells. Behav Brain Res 1996, 73:187-191.
22. Fonseca M.I., Ni Y.G., Dunning D.D., Miledi R. Distribution of serotonin 2A, 2C and 3 receptor mRNA in spinal cord and medulla oblongata. Brain Res Mol Brain Res 2001, 89:11-19.
23. Fritschy J.M. Is my antibody-staining specific? How to deal with pitfalls of immunohistochemistry. Eur J Neurosci 2008, 28:2365-2370.
24. Fuller D.D., Baker-Herman T.L., Golder F.J., Doperalski N.J., Watters J.J., Mitchell G.S. Cervical spinal cord injury upregulates ventral spinal 5-HT2A receptors. J Neurotrauma 2005, 22:203-213.
25. Gajendiran M. In vivo evidence for serotonin 5-HT2C receptor-mediated long-lasting excitability of lumbar spinal reflex and its functional interaction with 5-HT1A receptor in the mammalian spinal cord. Brain Res Bull 2008, 75:674-680.
26. Giroux N., Rossignol S., Reader T.A. Autoradiographic study of alpha1- and alpha2-noradrenergic and serotonin1A receptors in the spinal cord of normal and chronically transected cats. J Comp Neurol 1999, 406:402-414.
27. Griffin T.J., Gygi S.P., Ideker T., Rist B., Eng J., Hood L., Aebersold R Complementary profiling of gene expression at the transcriptome and proteome levels in Saccharomyces cerevisiae. Mol Cell Proteomics 2002, 1:323-333.
28. Gygi S.P., Rochon Y., Franza B.R., Aebersold R. Correlation between protein and mRNA abundance in yeast. Mol Cell Biol 1999, 19:1720-1730.
29. Halberstadt A.L., Van Der Heijden I., Ruderman M.A., Risbrough V.B., Gingrich J.A., Geyer M.A., Powell S.B. 5-HT(2A) and 5-HT(2C) receptors exert opposing effects on locomotor activity in mice. Neuropsychopharmacology 2009, 34:1958-1967.
30. Harvey P.J., Li X., Li Y., Bennett D.J. 5-HT2 receptor activation facilitates a persistent sodium current and repetitive firing in spinal motoneurons of rats with and without chronic spinal cord injury. J Neurophysiol 2006, 96:1158-1170.
31. Harvey P.J., Li X., Li Y., Bennett D.J. Endogenous monoamine receptor activation is essential for enabling persistent sodium currents and repetitive firing in rat spinal motoneurons. J Neurophysiol 2006, 96:1171-1186.
32. Hayashi Y., Jacob-Vadakot S., Dugan E.A., McBride S., Olexa R., Simansky K., Murray M., Shumsky J.S. 5-HT precursor loading, but not 5-HT receptor agonists, increases motor function after spinal cord contusion in adult rats. Exp Neurol 2010, 221:68-78.
33. Helton L.A., Thor K.B., Baez M. 5-Hydroxytryptamine2a, 5-hydroxytryptamine2B, and 5-hydroxytryptamine2C receptor mRNA expression in the spinal cord of rat, cat, monkey and human. Neuroreport 1994, 5:2617-2620.
34. Herrick-Davis K., Grinde E., Niswender C.M. Serotonin 5-HT2C receptor RNA editing alters receptor basal activity: implications for serotonergic signal transduction. J Neurochem 1999, 73:1711-1717.
35. Hertz L. Autonomic control of neuronal-astrocytic interactions, regulating metabolic activities, and ion fluxes in the CNS. Brain Res Bull 1992, 29:303-313.
36. Holmes G.M. 5-Hydroxytryptamine2C receptors on pudendal motoneurons innervating the external anal sphincter. Brain Res 2005, 1057:65-71.
37. Jackson D.A., White S.R. Receptor subtypes mediating facilitation by serotonin of excitability of spinal motoneurons. Neuropharmacology 1990, 29:787-797.
38. Jankowska E. Spinal interneuronal systems: identification, multifunctional character and reconfigurations in mammals. J Physiol 2001, 533(Pt1):31-40.
39. Jordan LM, Fabczak H, Kisielnicka E, Leszczynska A, Majczynski H, Nagy JI, Slawinska U (2010) Segmental distribution of 5-HT2A and 5-HT2C receptor up-regulation one month after complete spinal cord injury. Soc Neurosci Abstr 259.20.
40. Kao T., Shumsky J.S., Jacob-Vadakot S., Himes B.T., Murray M., Moxon K.A. Role of the 5-HT2C receptor in improving weight-supported stepping in adult rats spinalized as neonates. Brain Res 2006, 1112:159-168.
41. Kim D., Murray M., Simansky K.J. The serotonergic 5-HT(2C) agonist m-chlorophenylpiperazine increases weight-supported locomotion without development of tolerance in rats with spinal transections. Exp Neurol 2001, 169:496-500.
42. Kong X.-Y., Wienecke J., Hultborn H., Zhang M. Robust upregulation of serotonin 2A receptors after chronic spinal transection of rats: an immunohistochemical study. Brain Res 2010, 1320:60-68.
43. Kong XY, Wienecke J, Chen M, Hultborn H, Zhang M (2010b) Concomitant but differential upregulation of serotonin 2A and 2C receptors after sacral spinal transection of rats. In: Soc Neurosci Abstr 82.9.
44. Kong X.Y., Wienecke J., Chen M., Hultborn H., Zhang M. The time course of serotonin 2A receptor expression after spinal transection of rats: an immunohistochemical study. Neuroscience 2011, 177:114-126.
45. Lance J.W. Symposium synopsis. Spasticity: Disordered Motor Control. Symposia Specialists Miami 1980, 485-500. Year Book Medical Publishers, Chicago.
46. Landry E.S., Guertin P.A. Differential effects of 5-HT1 and 5-HT2 receptor agonists on hindlimb movements in paraplegic mice. Prog Neuropsychopharmacol Biol Psychiatry 2004, 28:1053-1060.
47. Lauder J.M., Wilkie M.B., Wu C., Singh S. Expression of 5-HT(2A), 5-HT(2B) and 5-HT(2C) receptors in the mouse embryo. Int J Dev Neurosci 2000, 18:653-662.
48. Lee J.K., Johnson C.S., Wrathall J.R. Up-regulation of 5-HT2 receptors is involved in the increased H-reflex amplitude after contusive spinal cord injury. Exp Neurol 2007, 203:502-511.
49. Li Y., Gorassini M.A., Bennett D.J. Role of persistent sodium and calcium currents in motoneuron firing and spasticity in chronic spinal rats. J Neurophysiol 2004, 91:767-783.
50. Li Y, Sanelli L, Li L, Vavrek R, Geddes F, Stephens M, Murray K, Winship I, Fouad K, Bennett DJ (2012) Monoamine synthesis in interneurons and vessels is upregulated after spinal cord injury. In: Soc Neurosci Abstr 182.02.
51. Li X., Murray K., Harvey P.J., Ballou E.W., Bennett D.J. Serotonin facilitates a persistent calcium current in motoneurons of rats with and without chronic spinal cord injury. J Neurophysiol 2007, 97:1236-1246.
52. MacFarlane P.M., Vinit S., Mitchell G.S. Serotonin 2A and 2B receptor-induced phrenic motor facilitation: differential requirement for spinal NADPH oxidase activity. Neuroscience 2011, 178:45-55.
53. Machacek D.W., Garraway S.M., Shay B.L., Hochman S. Serotonin 5-HT(2) receptor activation induces a long-lasting amplification of spinal reflex actions in the rat. J Physiol 2001, 537:201-207.
54. Majczyński H., Maleszak K., Cabaj A., Sławińska U. Serotonin-related enhancement of recovery of hind limb motor functions in spinal rats after grafting of embryonic raphe nuclei. J Neurotrauma 2005, 22:590-604.
55. Marlier L., Teilhac J.R., Cerruti C., Privat A. Autoradiographic mapping of 5-HT1, 5-HT1A, 5-HT1B and 5-HT2 receptors in the rat spinal cord. Brain Res 1991, 550:15-23.
56. Moore C.A., Milano S.K., Benovic J.L. Regulation of receptor trafficking by GRKs and arrestins. Annu Rev Physiol 2007, 69:451-482.
57. Murray K.C., Nakae A., Stephens M.J., Rank M., D'Amico J., Harvey P.J., Li X., Harris R.L., Ballou E.W., Anelli R., Heckman C.J., Mashimo T., Vavrek R., Sanelli L., Gorassini M.A., Bennett D.J., Fouad K. Recovery of motoneuron and locomotor function after spinal cord injury depends on constitutive activity in 5-HT2C receptors. Nat Med 2010, 16:694-700.
58. Murray K.C., Stephens M.J., Ballou E.W., Heckman C.J., Bennett D.J. Motoneuron excitability and muscle spasms are regulated by 5-HT2B and 5-HT2C receptor activity. J Neurophysiol 2011, 105:731-748.
59. Navarrett S., Collier L., Cardozo C., Dracheva S. Alterations of serotonin 2C and 2A receptors in response to T10 spinal cord transection in rats. Neurosci Lett 2012, 506:74-78.
60. Newton B.W., Hamill R.W. The morphology and distribution of rat serotoninergic intraspinal neurons: an immunohistochemical study. Brain Res Bull 1988, 20:349-360.
61. Nichols D.E., Nichols C.D. Serotonin receptors. Chem Rev 2008, 108:1614-1641.
62. Niebauer R.T., Wedekind A., Robinson A.S. Decreases in yeast expression yields of the human adenosine A2a receptor are a result of translational or post-translational events. Protein Expr Purif 2004, 37:134-143.
63. Nielsen J.B., Crone C., Hultborn H. The spinal pathophysiology of spasticity-from a basic science point of view. Acta Physiol (Oxf) 2007, 189:171-180.
64. Otoshi C.K., Walwyn W.M., Tillakaratne N.J., Zhong H., Roy R.R., Edgerton V.R. Distribution and localization of 5-HT(1A) receptors in the rat lumbar spinal cord after transection and deafferentation. J Neurotrauma 2009, 26:575-584.
65. Perrier J.F., Cotel F. Serotonin differentially modulates the intrinsic properties of spinal motoneurons from the adult turtle. J Physiol 2008, 586:1233-1238.
66. Perrier J.F., Hounsgaard J. 5-HT2 receptors promote plateau potentials in turtle spinal motoneurons by facilitating an L-type calcium current. J Neurophysiol 2003, 89:954-959.
67. Pierce P.A., Xie G.X., Levine J.D., Peroutka S.J. 5-Hydroxytryptamine receptor subtype messenger RNAs in rat peripheral sensory and sympathetic ganglia: a polymerase chain reaction study. Neuroscience 1996, 70. 553-539.
68. Pompeiano M., Palacios J.M., Mengod G. Distribution of the serotonin 5-HT2 receptor family mRNAs: comparison between 5-HT2A and 5-HT2C receptors. Brain Res Mol Brain Res 1994, 23:163-178.
69. Ren LQ, Wienecke J, Kong XY, Chen M, Møller M, Hultborn H, Zhang M (2011) The time course of serotonin 2C receptor upregulation in spinal motoneurons after sacral spinal transection is coincident with the development of tail spasticity in rats. In: Soc Neurosci Abstr 706.11.
70. Ren LQ, Wienecke J, Chen M, Guo S, Ma Q, Zheng XY, Li HY, Zhao SM, Kong XY, Hultborn H, Zhang M (2012) Aromatic l-amino acid decarboxylase cells in spinal cord could potentially provide serotonin but not dopamine after complete spinal cord transaction. In: Soc Neurosci Abstr 182.10.
71. Ritter S.L., Hall R.A. Fine-tuning of GPCR activity by receptor-interacting proteins. Nat Rev Mol Cell Biol 2009, 10:819-830.
72. Schmidt B.J., Jordan L.M. The role of serotonin in reflex modulation and locomotor rhythm production in the mammalian spinal cord. Brain Res Bull 2000, 53:689-710.
73. Shay B.L., Sawchuk M., Machacek D.W., Hochman S. Serotonin 5-HT2 receptors induce a long-lasting facilitation of spinal reflexes independent of ionotropic receptor activity. J Neurophysiol 2005, 94:2867-2877.
74. Sharma A., Punhani T., Fone K.C. Distribution of the 5-hydroxytryptamine2C receptor protein in adult rat brain and spinal cord determined using a receptor-directed antibody: effect of 5,7-dihydroxytryptamine. Synapse 1997, 27:45-56.
75. Skropeta D. The effect of individual N-glycans on enzyme activity. Bioorg Med Chem 2009, 17:2645-2653.
76. Thor K.B., Nickolaus S., Helke C.J. Autoradiographic localization of 5-hydroxytryptamine1A, 5-hydroxytryptamine1B and 5-hydroxytryptamine1C/2 binding sites in the rat spinal cord. Neuroscience 1993, 55:235-352.
77. Ung R.V., Landry E.S., Rouleau P., Lapointe N.P., Rouillard C., Guertin P.A. Role of spinal 5-HT2 receptor subtypes in quipazine-induced hindlimb movements after a low-thoracic spinal cord transection. Eur J Neurosci 2008, 28:2231-2242.
78. Vogt N., Gibaud A., Almeida A., Ourliac-Garnier I., Debatisse M., Malfoy B. Relationships linking amplification level to gene over-expression in gliomas. PLoS One 2010, 5:e14249.
79. Werry T.D., Loiacono R., Sexton P.M., Christopoulos A. RNA editing of the serotonin 5HT2C receptor and its effects on cell signalling, pharmacology and brain function. Pharmacol Ther 2008, 119:7-23.
80. Wienecke J., Westerdahl A.C., Hultborn H., Kiehn O., Ryge J. Global gene expression analysis of rodent motor neurons following spinal cord injury associates molecular mechanisms with development of postinjury spasticity. J Neurophysiol 2010, 103:761-778.
81. Zhou S.Y., Basura G.J., Goshgarian H.G. Serotonin (2) receptors mediate respiratory recovery after cervical spinal cord hemisection in adult rats. J Appl Physiol 2001, 91:2665-2673.