Activation of 5-HT2A receptors upregulates the function of the neuronal K-Cl cotransporter KCC2

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 1, 2013, Pages 348-353

  Bos, Rémi ^a   Sadlaoud, Karina ^a   Boulenguez, Pascale ^a   Buttigieg, Dorothée ^a   Liabeuf, Sylvie ^a   Brocard, Cécile ^a   Haase, Georg ^a   Bras, Hélène ^a   Vinay, Laurent ^a  

^a AIX MARSEILLE UNIVERSITÉ   (France)

Author keywords

[No Author keywords available]

Indexed keywords

KCC2 PROTEIN; SEROTONIN 2A RECEPTOR; SODIUM CHLORIDE COTRANSPORTER; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; ELECTROPHYSIOLOGY; ENZYME ACTIVATION; HYPERPOLARIZATION; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RECEPTOR UPREGULATION; SPASTICITY; SPINAL CORD INJURY;

ANIMALS; BICYCLO COMPOUNDS; BLOTTING, WESTERN; CHLORIDES; GENE EXPRESSION REGULATION; H-REFLEX; IMMUNOHISTOCHEMISTRY; INHIBITORY POSTSYNAPTIC POTENTIALS; METHYLAMINES; MOTOR NEURONS; MUSCLE SPASTICITY; RATS; RECEPTOR, SEROTONIN, 5-HT2A; SEROTONIN; SEROTONIN 5-HT2 RECEPTOR AGONISTS; SPINAL CORD INJURIES; SYMPORTERS;

RATTUS;

EID: 84871982368     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1213680110     Document Type: Article

References (53)

1. Blaesse P, Airaksinen MS, Rivera C, Kaila K (2009) Cation-chloride cotransporters and neuronal function. Neuron 61(6):820-838.
2. Payne JA, Stevenson TJ, Donaldson LF (1996) Cation-chloride co-transporters in neuronal communication, development and trauma. J Biol Chem 271(27):16245-16252.
3. Payne JA, Rivera C, Voipio J, Kaila K (2003) Molecular characterization of a putative K-Cl cotransporter in rat brain. A neuronal-specific isoform. Trends Neurosci 26(4):199-206.
4. Kahle KT, et al. (2008) Roles of the cation-chloride cotransporters in neurological disease. Nat Clin Pract Neurol 4(9):490-503.
5. Jean-Xavier C, Mentis GZ, O'Donovan MJ, Cattaert D, Vinay L (2007) Dual personality of GABA/glycine-mediated depolarizations in immature spinal cord. Proc Natl Acad Sci USA 104(27):11477-11482.
6. Doyon N, et al. (2011) Efficacy of synaptic inhibition depends on multiple, dynamically interacting mechanisms implicated in chloride homeostasis. PLOS Comput Biol 7(9):e1002149.
7. Prescott SA, Sejnowski TJ, De Koninck Y (2006) Reduction of anion reversal potential subverts the inhibitory control of firing rate in spinal lamina I neurons: Towards a biophysical basis for neuropathic pain. Mol Pain 2:32.
8. Biering-Sørensen F, Nielsen JB, Klinge K (2006) Spasticity-assessment: A review. Spinal Cord 44(12):708-722.
9. Boulenguez P, Vinay L (2009) Strategies to restore motor functions after spinal cord injury. Curr Opin Neurobiol 19(6):587-600.
10. Boulenguez P, et al. (2010) Down-regulation of the potassium-chloride cotransporter KCC2 contributes to spasticity after spinal cord injury. Nat Med 16(3):302-307.
11. Cramer SW, et al. (2008) The role of cation-dependent chloride transporters in neuropathic pain following spinal cord injury. Mol Pain 4:36.
12. Lu Y, Zheng J, Xiong L, Zimmermann M, Yang J (2008) Spinal cord injury-induced attenuation of GABAergic inhibition in spinal dorsal horn circuits is associated with downregulation of the chloride transporter KCC2 in rat. J Physiol 586(Pt 23):5701-5715.
13. Lee HH, et al. (2007) Direct protein kinase C-dependent phosphorylation regulates the cell surface stability and activity of the potassium chloride cotransporter KCC2. J Biol Chem 282(41):29777-29784.
14. Pearlstein E, Ben Mabrouk F, Pflieger JF, Vinay L (2005) Serotonin refines the locomotor-related alternations in the in vitro neonatal rat spinal cord. Eur J Neurosci 21(5):1338-1346.
15. Norreel JC, et al. (2003) Reversible disorganization of the locomotor pattern after neonatal spinal cord transection in the rat. J Neurosci 23(5):1924-1932.
16. Jordan LM, Sławińska U (2011) Chapter 12 - modulation of rhythmic movement: Control of coordination. Prog Brain Res 188:181-195.
17. Grillner S (2003) The motor infrastructure: From ion channels to neuronal networks. Nat Rev Neurosci 4(7):573-586.
18. Kiehn O (2006) Locomotor circuits in the mammalian spinal cord. Annu Rev Neurosci 29:279-306.
19. Jean-Xavier C, Pflieger JF, Liabeuf S, Vinay L (2006) Inhibitory postsynaptic potentials in lumbar motoneurons remain depolarizing after neonatal spinal cord transection in the rat. J Neurophysiol 96(5):2274-2281.
20. Sadlaoud K, et al. (2010) Differential plasticity of the GABAergic and glycinergic synaptic transmission to rat lumbar motoneurons after spinal cord injury. J Neurosci 30(9):3358-3369.
21. McLean TH, et al. (2006) 1-Aminomethylbenzocycloalkanes: Conformationally restricted hallucinogenic phenethylamine analogues as functionally selective 5-HT2A receptor agonists. J Med Chem 49(19):5794-5803.
22. Fox MA, French HT, LaPorte JL, Blackler AR, Murphy DL (2010) The serotonin 5-HT(2A) receptor agonist TCB-2: A behavioral and neurophysiological analysis. Psychopharmacology (Berl) 212(1):13-23.
23. Delpire E, et al. (2009) Small-molecule screen identifies inhibitors of the neuronal K-Cl cotransporter KCC2. Proc Natl Acad Sci USA 106(13):5383-5388.
24. Martiny-Baron G, et al. (1993) Selective inhibition of protein kinase C isozymes by the indolocarbazole Gö 6976. J Biol Chem 268(13):9194-9197.
25. Fulton BP, Walton K (1986) Electrophysiological properties of neonatal rat moto-neurones studied in vitro. J Physiol 370:651-678.
26. Lev-Tov A, Pinco M (1992) In vitro studies of prolonged synaptic depression in the neonatal rat spinal cord. J Physiol 447:149-169.
27. Wallis DI, Wu J (1992) FAST and SLOW ipsilateral and contralateral spinal reflexes in the neonate rat are modulated by 5-HT. Gen Pharmacol 23(6):1035-1044.
28. Jiang Z, Carlin KP, Brownstone RM (1999) An in vitro functionally mature mouse spinal cord preparation for the study of spinal motor networks. Brain Res 816(2):493-499.
29. Thompson FJ, Reier PJ, Lucas CC, Parmer R (1992) Altered patterns of reflex excitability subsequent to contusion injury of the rat spinal cord. J Neurophysiol 68(5):1473-1486.
30. Grey MJ, et al. (2008) Post-activation depression of soleus stretch reflexes in healthy and spastic humans. Exp Brain Res 185(2):189-197.
31. Brustein E, Drapeau P (2005) Serotoninergic modulation of chloride homeostasis during maturation of the locomotor network in zebrafish. J Neurosci 25(46):10607-10616.
32. Mayer SE, Sanders-Bush E (1994) 5-Hydroxytryptamine type 2A and 2C receptors linked to Na+/K+/Cl- cotransport. Mol Pharmacol 45(5):991-996.
33. Broadbelt KG, Paterson DS, Rivera KD, Trachtenberg FL, Kinney HC (2010) Neuroanatomic relationships between the GABAergic and serotonergic systems in the developing human medulla. Auton Neurosci 154(1-2):30-41.
34. Fiumelli H, Cancedda L, Poo MM (2005) Modulation of GABAergic transmission by activity via postsynaptic Ca2+-dependent regulation of KCC2 function. Neuron 48(5):773-786.
35. Woodin MA, Ganguly K, Poo MM (2003) Coincident pre- and postsynaptic activity modifies GABAergic synapses by postsynaptic changes in Cl- transporter activity. Neuron 39(5):807-820.
36. Fiumelli H, Woodin MA (2007) Role of activity-dependent regulation of neuronal chloride homeostasis in development. Curr Opin Neurobiol 17(1):81-86.
37. Lee HH, Deeb TZ, Walker JA, Davies PA, Moss SJ (2011) NMDA receptor activity downregulates KCC2 resulting in depolarizing GABAA receptor-mediated currents. Nat Neurosci 14(6):736-743.
38. Aloyo VJ, Berg KA, Spampinato U, Clarke WP, Harvey JA (2009) Current status of inverse agonism at serotonin2A (5-HT2A) and 5-HT2C receptors. Pharmacol Ther 121(2):160-173.
39. Berg KA, Clarke WP, Sailstad C, Saltzman A, Maayani S (1994) Signal transduction differences between 5-hydroxytryptamine type 2A and type 2C receptor systems. Mol Pharmacol 46(3):477-484.
40. Berg KA, Stout BD, Maayani S, Clarke WP (2001) Differences in rapid desensitization of 5-hydroxytryptamine2A and 5-hydroxytryptamine2C receptor-mediated phospholipase C activation. J Pharmacol Exp Ther 299(2):593-602.
41. Halberstadt AL, et al. (2009) 5-HT(2A) and 5-HT(2C) receptors exert opposing effects on locomotor activity in mice. Neuropsychopharmacology 34(8):1958-1967.
42. Machacek DW, Garraway SM, Shay BL, Hochman S (2001) Serotonin 5-HT(2) receptor activation induces a long-lasting amplification of spinal reflex actions in the rat. J Physiol 537(Pt 1):201-207.
43. Murray KC, et al. (2010) Recovery of motoneuron and locomotor function after spinal cord injury depends on constitutive activity in 5-HT2C receptors. NatMed 16(6):694-700.
44. Murray KC, Stephens MJ, Ballou EW, Heckman CJ, Bennett DJ (2011) Motoneuron excitability and muscle spasms are regulated by 5-HT2B and 5-HT2C receptor activity. J Neurophysiol 105(2):731-748.
45. Pearlstein E, Bras H, Deneris ES, Vinay L (2011) Contribution of 5-HT to locomotion - the paradox of Pet-1(-/-) mice. Eur J Neurosci 33(10):1812-1822.
46. Doly S, et al. (2004) 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 472(4):496-511.
47. Kong XY, Wienecke J, Hultborn H, Zhang M (2010) Robust upregulation of serotonin 2A receptors after chronic spinal transection of rats: An immunohistochemical study. Brain Res 1320:60-68.
48. Kong XY, Wienecke J, Chen M, Hultborn H, Zhang M (2011) The time course of serotonin 2A receptor expression after spinal transection of rats: An immunohistochemical study. Neuroscience 177:114-126.
49. Bennett DJ, Sanelli L, Cooke CL, Harvey PJ, Gorassini MA (2004) Spastic long-lasting reflexes in the awake rat after sacral spinal cord injury. J Neurophysiol 91(5):2247-2258.
50. Gorassini MA, Knash ME, Harvey PJ, Bennett DJ, Yang JF (2004) Role of motoneurons in the generation of muscle spasms after spinal cord injury. Brain 127(Pt 10):2247-2258.
51. González-Maeso J, Sealfon SC (2009) Psychedelics and schizophrenia. Trends Neurosci 32(4):225-232.
52. Millan MJ (2002) Descending control of pain. Prog Neurobiol 66(6):355-474.
53. Blaesse P, et al. (2006) Oligomerization of KCC2 correlates with development of inhibitory neurotransmission. J Neurosci 26(41):10407-10419.