Pre- and post-synaptic switches of GABA actions associated with Cl- homeostatic changes are induced in the spinal nucleus of the trigeminal nerve in a rat model of trigeminal neuropathic pain

Neuroscience

Volumn 228, Issue , 2013, Pages 334-348

  Wei, B ^a   Kumada, T ^a   Furukawa, T ^a   Inoue, K ^a   Watanabe, M ^b   Sato, K ^a   Fukuda, A ^a  

^a HAMAMATSU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b HOKKAIDO UNIVERSITY   (Japan)

Author keywords

Allodynia; KCC2; NKCC1; Primary afferent depolarization; Trigeminal ganglion; Trigeminal neuralgia

Indexed keywords

1,1' DIOCTADECYL 3,3,3',3' TETRAMETHYLINDOCARBOCYANINE; 4 AMINOBUTYRIC ACID; INWARDLY RECTIFYING POTASSIUM CHANNEL; MESSENGER RNA; SODIUM POTASSIUM CHLORIDE COTRANSPORTER;

ALLODYNIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; DOWN REGULATION; EXCITATORY POSTSYNAPTIC POTENTIAL; GABAERGIC TRANSMISSION; HOMEOSTASIS; IMAGE ANALYSIS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; NEUROPATHIC PAIN; NOCICEPTION; NONHUMAN; OLIVARY NUCLEUS; PAIN THRESHOLD; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC INHIBITION; PRESYNAPTIC POTENTIAL; PRIMARY AFFERENT DEPOLARIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; RECEPTIVE FIELD; SIGNAL TRANSDUCTION; TRIGEMINAL NERVE; TRIGEMINAL NERVE INJURY; TRIGEMINAL NUCLEUS; TRIGEMINUS GANGLION; UPREGULATION;

ANIMALS; CHLORIDES; DISEASE MODELS, ANIMAL; GAMMA-AMINOBUTYRIC ACID; HEK293 CELLS; HOMEOSTASIS; HUMANS; MALE; NEURALGIA; ORGAN CULTURE TECHNIQUES; PAIN THRESHOLD; PRESYNAPTIC TERMINALS; RATS; RATS, WISTAR; SYNAPTIC POTENTIALS; TRIGEMINAL NUCLEUS, SPINAL;

EID: 84870211298     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2012.10.043     Document Type: Article

References (49)

1. Alvarez-Leefmans F.J., Leon-Olea M., Mendoza-Sotelo J., Alvarez F.J., Anton B., Garduno R. Immunolocalization of the Na(+)-K(+)-2Cl(-) cotransporter in peripheral nervous tissue of vertebrates. Neuroscience 2001, 104:569-582.
2. Banks G.T., Haas M.A., Line S., Shepherd H.L., Alqatari M., Stewart S., Rishal I., Philpott A., Kalmar B., Kuta A., Groves M., Parkinson N., Acevedo-Arozena A., Brandner S., Bannerman D., Greensmith L., Hafezparast M., Koltzenburg M., Deacon R., Fainzilber M., Fisher E.M. Behavioral and other phenotypes in a cytoplasmic Dynein light intermediate chain 1 mutant mouse. J Neurosci 2011, 31:5483-5494.
3. Ben-Ari Y. Excitatory actions of GABA during development: the nature of the nurture. Nat Rev Neurosci 2002, 3:728-739.
4. Bennett G.J., Xie Y.K. A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 1988, 33:87-107.
5. Blaesse P., Airaksinen M.S., Rivera C., Kaila K. Cation-chloride cotransporters and neuronal function. Neuron 2009, 61:820-838.
6. Cervero F., Laird J.M. Mechanisms of allodynia: interactions between sensitive mechanoreceptors and nociceptors. Neuroreport 1996, 7:526-528.
7. Cervero F., Laird J.M., Garcia-Nicas E. Secondary hyperalgesia and presynaptic inhibition: an update. Eur J Pain 2003, 7:345-351.
8. Costigan M., Scholz J., Woolf C.J. Neuropathic pain: a maladaptive response of the nervous system to damage. Annu Rev Neurosci 2009, 32:1-32.
9. Coull J.A., Boudreau D., Bachand K., Prescott S.A., Nault F., Sik A., De Koninck P., De Koninck Y. Trans-synaptic shift in anion gradient in spinal lamina I neurons as a mechanism of neuropathic pain. Nature 2003, 424:938-942.
10. De Koninck Y. Altered chloride homeostasis in neurological disorders: a new target. Curr Opin Pharmacol 2007, 7:93-99.
11. Delpire E. Cation-chloride cotransporters in neuronal communication. News Physiol Sci 2000, 15:309-312.
12. B receptors on A delta and C primary afferents. Br J Pharmacol 1984, 81:327-333.
13. Enoki R., Namiki M., Kudo Y., Miyakawa H. Optical monitoring of synaptic summation along the dendrites of CA1 pyramidal neurons. Neuroscience 2002, 113:1003-1014.
14. Funk K., Woitecki A., Franjic-Wurtz C., Gensch T., Mohrlen F., Frings S. Modulation of chloride homeostasis by inflammatory mediators in dorsal root ganglion neurons. Mol Pain 2008, 4:32.
15. Galan A., Cervero F. Painful stimuli induce in vivo phosphorylation and membrane mobilization of mouse spinal cord NKCC1 co-transporter. Neuroscience 2005, 133:245-252.
16. Garcia-Nicas E., Laird J.M., Cervero F. GABAA-Receptor blockade reverses the injury-induced sensitization of nociceptor-specific (NS) neurons in the spinal dorsal horn of the rat. J Neurophysiol 2006, 96:661-670.
17. Goldstein M.E., House S.B., Gainer H. NF-L and peripherin immunoreactivities define distinct classes of rat sensory ganglion cells. J Neurosci Res 1991, 30:92-104.
18. Gregg J.M. Studies of traumatic neuralgias in the maxillofacial region: surgical pathology and neural mechanisms. J Oral Maxillofac Surg 1990, 48:228-237. discussion 238-239.
19. Hayasaki H., Sohma Y., Kanbara K., Maemura K., Kubota T., Watanabe M. A local GABAergic system within rat trigeminal ganglion cells. Eur J Neurosci 2006, 23:745-757.
20. Idänpään-Heikkilä J.J., Guilbaud G. Pharmacological studies on a rat model of trigeminal neuropathic pain: baclofen, but not carbamazepine, morphine or tricyclic antidepressants, attenuates the allodynia-like behavior. Pain 1999, 79:281-290.
21. Imamura Y., Kawamoto H., Nakanishi O. Characterization of heat-hyperalgesia in an experimental trigeminal neuropathy in rats. Exp Brain Res 1997, 116:97-103.
22. - cotransporter, KCC2, with brain-type creatine kinase. FEBS Lett 2004, 564:131-135.
23. Kahle K.T., Staley K.J., Nahed B.V., Gamba G., Hebert S.C., Lifton R.P., Mount D.B. Roles of the cation-chloride cotransporters in neurological disease. Nat Clin Pract Neurol 2008, 4:490-503.
24. Kanaka C., Ohno K., Okabe A., Kuriyama K., Itoh T., Fukuda A., Sato K. The differential expression patterns of messenger RNAs encoding K-Cl cotransporters (KCC1,2) and Na-K-2Cl cotransporter (NKCC1) in the rat nervous system. Neuroscience 2001, 104:933-946.
25. Kitagawa J., Takeda M., Suzuki I., Kadoi J., Tsuboi Y., Honda K., Matsumoto S., Nakagawa H., Tanabe A., Iwata K. Mechanisms involved in modulation of trigeminal primary afferent activity in rats with peripheral mononeuropathy. Eur J Neurosci 2006, 24:1976-1986.
26. Laird J.M., Garcia-Nicas E., Delpire E.J., Cervero F. Presynaptic inhibition and spinal pain processing in mice: a possible role of the NKCC1 cation-chloride co-transporter in hyperalgesia. Neurosci Lett 2004, 361:200-203.
27. - co-transporter1 in mouse trigeminal subnucleus caudalis following pulpal inflammation. Brain Res Bull 2010, 81:561-564.
28. 1 receptor in nociceptor sensitization and inflammatory pain. PLoS One 2011, 6:e17268.
29. Melzack R., Wall P.D. Pain mechanisms: a new theory. Science 1965, 150:971-979.
30. Miletic G., Miletic V. Loose ligation of the sciatic nerve is associated with TrkB receptor-dependent decreases in KCC2 protein levels in the ipsilateral spinal dorsal horn. Pain 2008, 137:532-539.
31. Payne J.A., Rivera C., Voipio J., Kaila K. Cation-chloride co-transporters in neuronal communication, development and trauma. Trends Neurosci 2003, 26:199-206.
32. Pitcher M.H., Cervero F. Role of the NKCC1 co-transporter in sensitization of spinal nociceptive neurons. Pain 2010, 151:756-762.
33. Price G.D., Trussell L.O. Estimate of the chloride concentration in a central glutamatergic terminal: a gramicidin perforated-patch study on the calyx of Held. J Neurosci 2006, 26:11432-11436.
34. Price T.J., Cervero F., de Koninck Y. Role of cation-chloride-cotransporters (CCC) in pain and hyperalgesia. Curr Top Med Chem 2005, 5:547-555.
35. Price T.J., Hargreaves K.M., Cervero F. Protein expression and mRNA cellular distribution of the NKCC1 cotransporter in the dorsal root and trigeminal ganglia of the rat. Brain Res 2006, 1112:146-158.
36. Price T.J., Cervero F., Gold M.S., Hammond D.L., Prescott S.A. Chloride regulation in the pain pathway. Brain Res Rev 2009, 60:149-170.
37. - co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 1999, 397:251-255.
38. Robinson P.P., Boissonade F.M., Loescher A.R., Smith K.G., Yates J.M., Elcock C., Bird E.V., Davies S.L., Smith P.L., Vora A.R. Peripheral mechanisms for the initiation of pain following trigeminal nerve injury. J Orofac Pain 2004, 18:287-292.
39. Rudomin P., Schmidt R.F. Presynaptic inhibition in the vertebrate spinal cord revisited. Exp Brain Res 1999, 129:1-37.
40. Sessle B.J. Acute and chronic craniofacial pain: brainstem mechanisms of nociceptive transmission and neuroplasticity, and their clinical correlates. Crit Rev Oral Biol Med 2000, 11:57-91.
41. 2+ oscillations with KCC2 mRNA downregulation in injured facial motoneurons. J Neurophysiol 2003, 89:1353-1362.
42. - cotransporter mRNAs (KCC1, KCC2, and NKCC1) in rat trigeminal nervous system. Brain Res Mol Brain Res 2005, 133:12-18.
43. Vos B.P., Strassman A.M., Maciewicz R.J. Behavioral evidence of trigeminal neuropathic pain following chronic constriction injury to the rat's infraorbital nerve. J Neurosci 1994, 14:2708-2723.
44. Wachowiak M., Cohen L.B. Presynaptic afferent inhibition of lobster olfactory receptor cells: reduced action-potential propagation into axon terminals. J Neurophysiol 1998, 80:1011-1015.
45. Willis W.D. Dorsal root potentials and dorsal root reflexes: a double-edged sword. Exp Brain Res 1999, 124:395-421.
46. Willis W.D. John Eccles' studies of spinal cord presynaptic inhibition. Prog Neurobiol 2006, 78:189-214.
47. Woolf C.J., Salter M.W. Neuronal plasticity: increasing the gain in pain. Science 2000, 288:1765-1769.
48. - co-transporter 2 in mouse medullary dorsal horn contributes to the formalin-induced inflammatory orofacial pain. Neurosci Lett 2009, 457:36-40.
49. - uptake promoting depolarizing GABA actions in immature rat neocortical neurones is mediated by NKCC1. J Physiol 2004, 557:829-841.