Serotonin receptor and KCC2 gene expression in lumbar flexor and extensor motoneurons posttransection with and without passive cycling

Journal of Neurophysiology

Volumn 113, Issue 5, 2015, Pages 1369-1376

  Chopek, Jeremy W ^a   Sheppard, Patricia C ^a   Gardiner, Kalan ^a   Gardiner, Phillip F ^a,b  

^a UNIVERSITY OF MANITOBA   (Canada)

^b UNIVERSITY OF MANITOBA   (Canada)

Author keywords

Exercise; Gene expression; Lumbar flexor and extensor motoneurons; Serotonin receptors and KCC2; Spinal transection

Indexed keywords

GLUTAMATE RECEPTOR 1; MESSENGER RNA; METABOTROPIC RECEPTOR 1; POTASSIUM CHLORIDE COTRANSPORTER 2; SEROTONIN RECEPTOR; COTRANSPORTER; METABOTROPIC GLUTAMATE RECEPTOR TYPE 1; METABOTROPIC RECEPTOR; POTASSIUM-CHLORIDE SYMPORTERS;

ADULT; ANIMAL EXPERIMENT; ARTICLE; EXTENSOR MUSCLE; FEMALE; FLEXOR MUSCLE; GENE EXPRESSION; LASER CAPTURE MICRODISSECTION; LUMBAR SPINE; MOTONEURON; MUSCLE MASS; NONHUMAN; PRIORITY JOURNAL; RAT; RECEPTOR DOWN REGULATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPINAL CORD TRANSSECTION; ANIMAL; EXERCISE; GENETICS; HINDLIMB; INNERVATION; METABOLISM; PHYSIOLOGY; SKELETAL MUSCLE; SPRAGUE DAWLEY RAT;

ANIMALS; FEMALE; HINDLIMB; MOTOR NEURONS; MUSCLE, SKELETAL; PHYSICAL EXERTION; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, METABOTROPIC GLUTAMATE; RECEPTORS, SEROTONIN; SYMPORTERS;

EID: 84923924612     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00550.2014     Document Type: Article

References (54)

1. Alvarez FJ, Dewey DE, Carr PA, Cope TC, Fyffe RE. Downregulation of metabotropic glutamate receptor 1a in motoneurons after axotomy. Neuroreport 8: 1711–1716, 1997
2. Bennett DJ, Gorassini M, Fouad K, Sanelli L, Han Y, Cheng J. Spasticity in rats with sacral spinal cord injury. J Neurotrauma 16: 69–84, 1999
3. Bos R, Sadlaoud K, Boulenguez P, Buttigieg D, Liabeuf S, Brocard C, Haase G, Bras H, Vinay L. Activation of 5-HT2A receptors upregulates the function of the neuronal K-Cl cotransporter KCC2. Proc Natl Acad Sci USA 110: 348–353, 2013
4. Boulenguez P, Liabeuf S, Bos R, Bras H, Jean-Xavier C, Brocard C, Stil A, Darbon P, Cattaert D, Delpire E, Marsala M, Vinay L. Downregulation of the potassium-chloride cotransporter KCC2 contributes to spasticity after spinal cord injury. Nat Med 16: 302–307, 2010
5. Chopek JW, Macdonell CW, Gardiner K, Gardiner P. Daily passive cycling attenuates the hyperexcitability and restores the responsiveness of the extensor monosynaptic reflex to quipazine in the chronic spinal transected rat. J Neurotrauma 31: 1083–1087, 2014
6. Cote MP, Gandhi S, Zambrotta M, Houle JD. Exercise modulates chloride homeostasis after spinal cord injury. J Neurosci 34: 8976–8987, 2014
7. Cotel F, Exley R, Cragg SJ, Perrier JF. Serotonin spillover onto the axon initial segment of motoneurons induces central fatigue by inhibiting action potential initiation. Proc Natl Acad Sci USA 110: 4774–4779, 2013
8. D’Amico JM, Condliffe EG, Martins KJ, Bennett DJ, Gorassini MA. Recovery of neuronal and network excitability after spinal cord injury and implications for spasticity. Front Integr Neurosci 8: 36, 2014.
9. Delgado-Lezama R, Hounsgaard J. Adapting motoneurons for motor behavior. Prog Brain Res 123: 57–63, 1999
10. Delgado-Lezama R, Perrier JF, Hounsgaard J. Local facilitation of plateau potentials in dendrites of turtle motoneurones by synaptic activation of metabotropic receptors. J Physiol 515: 203–207, 1999
11. Doly S, Fischer J, Brisorgueil MJ, Verge D, Conrath M. Pre and postsynaptic localization of the 5-HT7 receptor in rat dorsal spinal cord: immunocytochemical evidence. J Comp Neurol 490: 256–269, 2005
12. Dupont-Versteegden EE, Houle JD, Dennis RA, Zhang J, Knox M, Wagoner G, Peterson CA. Exercise-induced gene expression in soleus muscle is dependent on time after spinal cord injury in rats. Muscle Nerve 29: 73–81, 2004
13. Ferraiuolo L, De Bono JP, Heath PR, Holden H, Kasher P, Channon KM, Kirby J, Shaw PJ. Transcriptional response of the neuromuscular system to exercise training and potential implications for ALS. J Neurochem 109: 1714–1724, 2009
14. Fong AJ, Roy RR, Ichiyama RM, Lavrov I, Courtine G, Gerasimenko Y, Tai YC, Burdick J, Edgerton VR. Recovery of control of posture and locomotion after a spinal cord injury: solutions staring us in the face. Prog Brain Res 175: 393–418, 2009
15. Ghiani CA, Ying Z, de Vellis J, Gomez-Pinilla F. Exercise decreases myelin-associated glycoprotein expression in the spinal cord and positively modulates neuronal growth. Glia 55: 966–975, 2007
16. Giroux N, Rossignol S, Reader TA. Autoradiographic 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, 1999
17. Gomez-Pinilla F, Ying Z, Opazo P, Roy RR, Edgerton VR. Differential regulation by exercise of BDNF and NT-3 in rat spinal cord and skeletal muscle. Eur J Neurosci 13: 1078–1084, 2001
18. Gomez-Pinilla F, Ying Z, Roy RR, Molteni R, Edgerton VR. Voluntary exercise induces a BDNF-mediated mechanism that promotes neuroplasticity. J Neurophysiol 88: 2187–2195, 2002
19. Hoffman MS, Mitchell GS. Spinal 5-HT7 receptor activation induces longlasting phrenic motor facilitation. J Physiol 589: 1397–1407, 2001
20. Houle JD, Morris K, Skinner RD, Garcia-Rill E, Peterson CA. Effects of fetal spinal cord tissue transplants and cycling exercise on the soleus muscle in spinalized rats. Muscle Nerve 22: 846–856, 1999
21. Inoue T, Itoh S, Wakisaka S, Ogawa S, Saito M, Morimoto T. Involvement of 5-HT7 receptors in serotonergic effects on spike afterpotentials in presumed jaw-closing motoneurons of rats. Brain Res 954: 202–211, 2002
22. Jordan LM, Fabsczak HK, Leszczynska A, Majczynski H, Nagy JI, Slawinska U. Segmental distribution of 5-HT2A and 5-HT2C receptor up-regulation one month after complete spinal cord injury. Neuroscience Meeting Planner 259–20, 2010
23. Keeler BE, Liu G, Siegfried RN, Zhukareva V, Murray M, Houle JD. Acute and prolonged hindlimb exercise elicits different gene expression in motoneurons than sensory neurons after spinal cord injury. Brain Res 1438, 8–21, 2012
24. Kong XY, 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 177: 114–126, 2011
25. Kong XY, Wienecke J, Hultborn H, Zhang M. Robust upregulation of serotonin 2A receptors after chronic spinal transection of rats: an immunohistochemical study. Brain Res 1320: 60–68, 2010
26. Li Y, Bennett DJ. Persistent sodium and calcium currents cause plateau potentials in motoneurons of chronic spinal rats. J Neurophysiol 90: 857–869, 2003.
27. Liu J, Jordan LM. Stimulation of the parapyramidal region of the neonatal rat brain stem produces locomotor-like activity involving spinal 5-HT7 and 5-HT2A receptors. J Neurophysiol 94: 1392–1404, 2005
28. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2[-delta delta C(T)] method. Methods 25: 402–408, 2001
29. Macias M, Dwornik A, Ziemlinska E, Fehr S, Schachner M, Czarkowska-Bauch J, Skup M. Locomotor exercise alters expression of pro-brainderived neurotrophic factor, brain-derived neurotrophic factor and its receptor TrkB in the spinal cord of adult rats. Eur J Neurosci 25: 2425–2444, 2007
30. Macias M, Fehr S, Dwornik A, Sulejczak D, Wiater M, Czarkowska-Bauch J, Skup M, Schachner M. Exercise increases mRNA levels for adhesion molecules N-CAM and L1 correlating with BDNF response. Neuroreport 13: 2527–2530, 2002
31. Murphy RJ, Dupont-Versteegden EE, Peterson CA, Houle JD. Two experimental strategies to restore muscle mass in adult rats following spinal cord injury. Neurorehab Neural Repair 13: 125–134, 1999
32. Murray KC, Nakae A, Stephens MJ, Rank M, D’Amico J, Harvey PJ, Li X, Harris RL, Ballou EW, Anelli R, Heckman CJ, Mashimo T, Vavrek R, Sanelli L, Gorassini MA, Bennett DJ, Fouad K. Recovery of motoneuron and locomotor function after spinal cord injury depends on constitutive activity in 5-HT(2C) receptors. Nat Med 16: 694–700, 2010
33. Murray KC, Stephens MJ, Ballou EW, Heckman CJ, Bennett DJ. Motoneuron excitability and muscle spasms are regulated by 5-HT2B and 5-HT2C receptor activity. J Neurophysiol 105: 731–748, 2011
34. 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 506: 74–78, 2012
35. Nistri A, Ostroumov K, Sharifullina E, Taccola G. Tuning and playing a motor rhythm: how metabotropic glutamate receptors orchestrate generation of motor patterns in the mammalian central nervous system. J Physiol 572: 323–334, 2006
36. Noga BR, Johnson DM, Riesgo MI, Pinzon A. Locomotor-activated neurons of the cat. I. Serotonergic innervation and co-localization of 5-HT7, 5-HT2A, and 5-HT1A receptors in the thoraco-lumbar spinal cord. J Neurophysiol 102: 1560–1576, 2009
37. Ollivier-Lanvin K, Keeler BE, Siegfried R, Houle JD, Lemay MA. Proprioceptive neuropathy affects normalization of the H-reflex by exercise after spinal cord injury. Exp Neurol 221: 198–205, 2010
38. Otoshi CK, Walwyn WM, Tillakaratne NJ, Zhong H, Roy RR, Edgerton VR. Distribution and localization of 5-HT(1A) receptors in the rat lumbar spinal cord after transection and deafferentation. J Neurotrauma 26: 575–584, 2009.
39. Payne JA, Rivera C, Voipio J, Kaila K. Cation-chloride co-transporters in neuronal communication, development and trauma. Trends Neurosci 26: 199–206, 2003
40. Perreau VM, Adlard PA, Anderson AJ, Cotman CW. Exercise-induced gene expression changes in the rat spinal cord. Gene Expr 12: 107–121, 2005
41. Peterson CA, Murphy RJ, Dupont-Versteegden EE, Houle JD. Cycling exercise and fetal spinal cord transplantation act synergistically on atrophied muscle following chronic spinal cord injury in rats. Neurorehabil Neural Repair 14: 85–91, 2000
42. Ren LQ, Wienecke J, Chen M, Moller M, Hultborn H, Zhang M. The time course of serotonin 2C receptor expression after spinal transection of rats: an immunohistochemical study. Neuroscience 236: 31–46, 2013
43. Roy RR Jr, Acosta L. Fiber type and fiber size changes in selected thigh muscles six months after low thoracic spinal cord transection in adult cats: exercise effects. Exp Neurol 92: 675–685, 1986
44. Ryge J, Winther O, Wienecke J, Sandelin A, Westerdahl AC, Hultborn H, Kiehn O. Transcriptional regulation of gene expression clusters in motor neurons following spinal cord injury. BMC Genomics 11: 365, 2010.
45. Schmidt BJ Jordan LM. The role of serotonin in reflex modulation and locomotor rhythm production in the mammalian spinal cord. Brain Res Bull 53: 689–710, 2000
46. Skinner RD, Houle JD, Reese NB, Berry CL, GarciaRill E. Effects of exercise and fetal spinal cord implants on the H-reflex in chronically spinalized adult rats. Brain Res 729: 127–131, 1996
47. Skup M, Gajewska-Wozniak O, Grygielewicz P, Mankovskaya T, Czarkowska-Bauch J. Different effects of spinalization and locomotor training of spinal animals on cholinergic innervation of the soleus and tibialis anterior motoneurons. Eur J Neurosci 36: 2679–2688, 2012
48. Slawinska U, Majczynski H, Dai Y, Jordan LM. The upright posture improves plantar stepping and alters responses to serotonergic drugs in spinal rats. J Physiol 590: 1721–1736, 2012
49. Ung RV, Landry ES, Rouleau P, Lapointe NP, Rouillard C, Guertin PA. Role of spinal 5-HT receptor subtypes in quipazine-induced hindlimb movements after a low-thoracic spinal cord transection. Eur J Neurosci 28: 2231–2242, 2008
50. Valerio A, Paterlini M, Boifava M, Memo M, Spano P. Metabotropic glutamate receptor mRNA expression in rat spinal cord. Neuroreport 8: 2695–2699, 1997
51. West SP, Roy RR, Edgerton VR. Fiber type and fiber size of cat ankle, knee, and hip extensors and flexors following low thoracic spinal cord transection at an early age. Exp Neurol 91: 174–182, 1986
52. Wienecke J, Westerdahl AC, 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 103: 761–778, 2010
53. Ying Z, Roy RR, Edgerton VR, Gomez-Pinilla F. Voluntary exercise increases neurotrophin-3 and its receptor TrkC in the spinal cord. Brain Res 987: 93–99, 2003
54. Ziemlinska E, Kugler S, Schachner M, Wewior I, Czarkowska-Bauch J, Skup M. Overexpression of BDNF increases excitability of the lumbar spinal network and leads to robust early locomotor recovery in completely spinalized rats. PLoS One 9: e88833, 2014.