Na+,K+,2Cl- cotransport and intracellular chloride regulation in rat primary sensory neurons: Thermodynamic and kinetic aspects

Journal of Neurophysiology

Volumn 100, Issue 1, 2008, Pages 169-184

  Rocha González, Héctor I ^a   Mao, Shihong ^a   Alvarez Leefmans, Francisco J ^a  

^a WRIGHT STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; BUMETANIDE; CALCEIN; CHLORIDE; N (ETHOXYCARBONYLMETHYL) 6 METHOXYQUINOLINIUM BROMIDE; POTASSIUM; SODIUM; UNCLASSIFIED DRUG; FLUORESCEIN DERIVATIVE; FLUORESCENT DYE; LOOP DIURETIC AGENT; N (ETHOXYCARBONYLMETHYL) 6 METHOXYQUINOLINIUM; N-(ETHOXYCARBONYLMETHYL)-6-METHOXYQUINOLINIUM; QUINOLINE DERIVATIVE; SODIUM POTASSIUM CHLORIDE COTRANSPORTER;

4 AMINOBUTYRIC ACID RELEASE; ANIMAL CELL; ARTICLE; CELL VOLUME; CHLORIDE TRANSPORT; CONTROLLED STUDY; ELECTROCHEMICAL ANALYSIS; FLUORESCENCE MICROSCOPY; INTERNEURON; NEGATIVE FEEDBACK; NEWBORN; NONHUMAN; POTASSIUM TRANSPORT; PRESYNAPTIC INHIBITION; PRIMARY AFFERENT DEPOLARIZATION; PRIORITY JOURNAL; RAT; SENSORY NERVE CELL; SODIUM TRANSPORT; SPINAL GANGLION; STEADY STATE; THERMODYNAMICS; ANIMAL; CYTOLOGY; DOSE RESPONSE; DRUG EFFECT; EXTRACELLULAR FLUID; METABOLISM; PHYSIOLOGY;

ANIMALS; ANIMALS, NEWBORN; BUMETANIDE; CHLORIDES; DOSE-RESPONSE RELATIONSHIP, DRUG; EXTRACELLULAR FLUID; FLUORESCEINS; FLUORESCENT DYES; GANGLIA, SPINAL; NEURONS, AFFERENT; QUINOLINIUM COMPOUNDS; RATS; SODIUM; SODIUM POTASSIUM CHLORIDE SYMPORTER INHIBITORS; SODIUM-POTASSIUM-CHLORIDE SYMPORTERS; THERMODYNAMICS;

EID: 51049108643     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.01007.2007     Document Type: Article

References (92)

1. - regulation and synaptic inhibition in vertebrate and invertebrate neurons. In: Chloride Channels and Carriers in Nerve, Muscle, and Glial Cells, edited by Alvarez-Leefmans FJ, Russell JM. New York: Plenum, 1990, p. 109-158.
2. Alvarez-Leefmans FJ. Intracellular chloride regulation. In: Cell Physiology Sourcebook: A Molecular Approach, edited by Sperelakis N. San Diego, CA: Academic, 2001, p. 301-318.
3. Alvarez-Leefmans FJ, Altamirano J, Crowe WE. Use of ion-selective microelectrodes and fluorescent probes to measure cell volume. Methods Neurosci 27: 361-391, 1995.
4. Alvarez-Leefmans FJ, Gamiño SM, Giraldez F, Nogueron I. Intracellular chloride regulation in amphibian dorsal root ganglion neurones studied with ion-selective microelectrodes. J Physiol 406: 225-246, 1988.
5. Alvarez-Leefmans FJ, Herrera-Pérez JJ, Márquez MS, Blanco VM. Simultaneous measurement of water volume and pH in single cells using BCECF and fluorescence imaging microscopy. Biophys J 90: 608-618, 2006.
6. Alvarez-Leefmans FJ, Nani A, Márquez MS. Chloride transport, osmotic balance, and presynaptic inhibition. In: Presynaptic Inhibition and Neural Control, edited by Rudomin P, Romo R, Mendell LM. New York: Oxford, 1998, p. 50-79.
7. A receptor-mediated excitation of nociceptive afferents in the rat isolated spinal cord-tail preparation. Neuropharmacology 33: 109-114, 1994.
8. Ballanyi K, Grafe P. An intracellular analysis of gamma-aminobutyric-acidassociated ion movements in rat sympathetic neurones. J Physiol 365: 41-58, 1985.
9. Ben-Ari Y, Gaiarsa JL, Tyzio R, Khazipov R. GABA: a pioneer transmitter that excites immature neurons and generates primitive oscillations. Physiol Rev 87: 1215-1284, 2007.
10. Bevensee MO, Apkon M, Boron WF. Intracellular pH regulation in cultured astrocytes from rat hippocampus. II. Electrogenic Na/HCO3 cotransport. J Gen Physiol 110: 467-483, 1997.
11. Bhisitkul RB, Villa JE, Kocsis JD. Axonal GABA receptors are selectively present on normal and regenerated sensory fibers in rat peripheral nerve. Exp Brain Res 66: 659-663, 1987.
12. Boettger T, Rust MB, Maier H, Seidenbecher T, Schweizer M, Keating DJ, Faulhaber J, Ehmke H, Pfeffer C, Scheel O, Lemcke B, Horst J, Leuwer R, Pape HC, Volkl H, Hubner CA, Jentsch TJ. Loss of K-Cl co-transporter KCC3 causes deafness, neurodegeneration and reduced seizure threshold. Embo J 22: 5422-5434, 2003.
13. i dependent. Am J Physiol Cell Physiol 258: C749-753, 1990.
14. Burkey TH, Hingtgen CM, Vasko MR. Isolation and culture of sensory neurons from the dorsal-root ganglia of embryonic or adult rats. In: Pain Research: Methods and Protocols, edited by Luo DZ. Totowa, NJ: Humana, 2004, p. 189-202.
15. Cala PM, Maldonado HM. pH regulatory Na/H exchange by Amphiuma red blood cells. J Gen Physiol 103: 1035-1053, 1994.
16. Carlton SM, Zhou S, Coggeshall RE. Peripheral GABA(A) receptors: evidence for peripheral primary afferent depolarization. Neuroscience 93: 713-122, 1999.
17. Chub N, Mentis GZ, O'Donovan MJ. Chloride-sensitive MEQ fluorescence in chick embryo motoneurons following manipulations of chloride and during spontaneous network activity. J Neurophysiol 95: 323-330, 2006.
18. Coull JA, Boudreau D, Bachand K, Prescott SA, 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 424: 938-942, 2003.
19. Crowe WE, Altamirano J, Huerto L, Alvarez-Leefmans FJ. Volume changes in single N1E-115 neuroblastoma cells measured with a fluorescent probe. Neuroscience 69: 283-296, 1995.
20. Curtis DR, Lodge D. The depolarization of feline ventral horn group Ia spinal afferent terminations by GABA. Exp Brain Res 46: 215-233, 1982.
21. Davidoff RA, Hackman JC. GABA: presynaptic actions. In: Neurotransmitter Actions in the Vertebrate Nervous System, edited by Rogawski MA, Barker JL. New York: Plenum, 1985, p. 3-32.
22. De Groat WC, Lalley PM, Saum WR. Depolarization of dorsal root ganglia in the cat by GABA and related amino acids: antagonism by picrotoxin and bicuculline. Brain Res 44: 273-277, 1972.
23. Delpire E, Gagnon KB. SPAK and OSR1, key kinases involved in the regulation of chloride transport. Acta Physiol 187: 103-113, 2006.
24. Desarmenien M, Santangelo F, Loeffler JP, Feltz P. Comparative study of GABA-mediated depolarizations of lumbar A delta and C primary afferent neurons of the rat. Exp Brain Res 54: 521-528, 1984.
25. Deschenes M, Feltz P. GABA-induced rise of extracellular potassium in rat dorsal root ganglia: an electrophysiological study in vivo. Brain Res 118: 494-499, 1976.
26. Deschenes M, Feltz P, Lamour Y. A model for an estimate in vivo of the ionic basis of presynaptic inhibition: an intracellular analysis of the GABA-induced depolarization in rat dorsal root ganglia. Brain Res 118: 486-493, 1976.
27. Fang X, McMullan S, Lawson SN, Djouhri L. Electrophysiological differences between nociceptive and non-nociceptive dorsal root ganglion neurons in the rat in vivo. J Physiol 565: 927-943, 2005.
28. Fiori J, Ballardini R, Hrelia P, Andrisano V, Tarozzi A, Cavrini V. Investigation of the photochemical properties and in vitro phototoxic potential of bumetanide. Photochem Photobiol Sci 2: 1011-1017, 2003.
29. French AS, Panek I, Torkkeli PH. Shunting versus inactivation: simulation of GABAergic inhibition in spider mechanoreceptors suggests that either is sufficient. Neurosci Res 55: 189-196, 2006.
30. - channels-homing in on an elusive channel species. Prog Neurobiol 60: 247-289, 2000.
31. Galan A, Cervero F. Painful stimuli induce in vivo phosphorylation and membrane mobilization of mouse spinal cord NKCC1 co-transporter. Neuroscience 133: 245-252, 2005.
32. Gallagher JP, Higashi H, Nishi S. Characterization and ionic basis of GABA-induced depolarizations recorded in vitro from cat primary afferent neurones. J Physiol 275: 263-282, 1978.
33. Gamba G. Molecular physiology and pathophysiology of electroneutral cation-chloride cotransporters. Physiol Rev 85: 423-493, 2005.
34. Geck P, Heinz E. The Na-K-2Cl cotransport system. J Membr Biol 91: 97-105, 1986.
35. - in Ehrlich cells. Biochim Biophys Acta 600: 432-447, 1980.
36. Hannaert P, Alvarez-Guerra M, Pirot D, Nazaret C, Garay RP. Rat NKCC2/NKCC1 cotransporter selectivity for loop diuretic drugs. Naunyn Schmiedebergs Arch Pharmacol 365: 193-199, 2002.
37. Hartzell C, Putzier I, Arreola J. Calcium-activated chloride channels. Annu Rev Physiol 67: 719-758, 2005.
38. Hoffmann EK. The pump and leak steady-state concept with a variety of regulated leak pathways. J Membr Biol 184: 321-330, 2001.
39. Hoffmann EK, Schettino T, Marshall WS. The role of volume-sensitive ion transport systems in regulation of epithelial transport. Comp Biochem Physiol A Mol Integr Physiol 148: 29-43, 2007.
40. Hong S, Morrow TJ, Paulson PE, Isom LL, Wiley JW. Early painful diabetic neuropathy is associated with differential changes in tetrodotoxin-sensitive and -resistant sodium channels in dorsal root ganglion neurons in the rat. J Biol Chem 279: 29341-29350, 2004.
41. --dependent mechanism. Am J Physiol Cell Physiol 281: C1948-1953, 2001.
42. Jones RW. Principles of Biological Regulation: An Introduction to Feedback Systems. New York: Academic, 1973.
43. - flux by altering the phosphorylation state of the Na-K-Cl and K-Cl cotransporters. Physiology 21: 326-335, 2006.
44. Kakazu Y, Akaike N, Komiyama S, Nabekura J. Regulation of intracellular chloride by cotransporters in developing lateral superior olive neurons. J Neurosci 19: 2843-2851, 1999.
45. 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 104: 933-946, 2001.
46. Kaneko H, Nakamura T, Lindemann B. Noninvasive measurement of chloride concentration in rat olfactory receptor cells with use of a fluorescent dye. Am J Physiol Cell Physiol 280: C1387-1393, 2001.
47. Kaneko H, Putzier I, Frings S, Gensch T. Determination of intracellular chloride concentration in dorsal root ganglion neurons by fluorescence lifetime imaging. In: Calcium-Acivated Chloride Channels, edited by Fuller CM. Boston: Elsevier/Academic, 2002, p. 167-189.
48. -] in cultured aortic smooth muscle cells. Am J Physiol 267: H2114-2123, 1994.
49. Krapf R, Berry CA, Verkman AS. Estimation of intracellular chloride activity in isolated perfused rabbit proximal convoluted tubules using a fluorescent indicator. Biophys J 53: 955-962, 1988.
50. A receptors expressed by nociceptors and other postnatal sensory neurons in rat. J Physiol 549: 131-142, 2003.
51. 2+-evoked fluid secretion by murine nasal submucosal gland serous acinar cells. J Physiol 582: 1099-1124, 2007.
52. Levy RA. The role of GABA in primary afferent depolarization. Prog Neurobiol 9: 211-267, 1977.
53. Lytle C, McManus T. Coordinate modulation of Na-K-2Cl cotransport and K-Cl cotransport by cell volume and chloride. Am J Physiol Cell Physiol 283: C1422-1431, 2002.
54. Ma C, LaMotte RH. Enhanced excitability of dissociated primary sensory neurons after chronic compression of the dorsal root ganglion in the rat. Pain 113: 106-112, 2005.
55. - exchanger activity in human fibroblasts. Am J Physiol Cell Physiol 275: C515-526, 1998.
56. Martinez-Zaguilan R, Gillies RJ, Sanchez-Armass S. Regulation of pH in rat brain synaptosomes. II. Role of Cl. J Neurophysiol 71: 2249-2257, 1994.
57. Momose-Sato Y, Sato K, Hirota A, Kamino K. GABA-Induced intrinsic light-scattering changes associated with voltage-sensitive dye signals in embryonic brain stem slices: coupling of depolarization and cell shrinkage. J Neurophysiol 79: 2208-2217, 1998.
58. Nakamura T, Kaneko H, Nishida N. Direct measurement of the chloride concentration in newt olfactory receptors with the fluorescent probe. Neurosci Lett 237: 5-8, 1997.
59. Nishi S, Minota S, Karczmar AG. Primary afferent neurones: the ionic mechanism of GABA-mediated depolarization. Neuropharmacology 13: 215-219, 1974.
60. Owens DF, Kriegstein AR. Developmental neurotransmitters? Neuron 36: 989-991, 2002a.
61. Owens DF, Kriegstein AR. Is there more to GABA than synaptic inhibition? Nat Rev Neurosci 3: 715-727, 2002b.
62. - transport. Am J Physiol Renal Physiol 290: F1094-1102, 2006.
63. Payne JA, Rivera C, Voipio J, Kaila K. Cation-chloride co-transporters in neuronal communication, development and trauma. Trends Neurosci 26: 199-206, 2003.
64. Petruska JC, Napaporn J, Johnson RD, Gu JG, Cooper BY. Subclassified acutely dissociated cells of rat DRG: histochemistry and patterns of capsaicin-, proton-, and ATP-activated currents. J Neurophysiol 84: 2365-2379, 2000.
65. Pieraut S, Laurent-Matha V, Sar C, Hubert T, Mechaly I, Hilaire C, Mersel M, Delpire E, Valmier J, Scamps F. NKCC1 phosphorylation stimulates neurite growth of injured adult sensory neurons. J Neurosci 27: 6751-6759, 2007.
66. Plotkin MD, Snyder EY, Hebert SC, Delpire E. Expression of the Na-K-2Cl cotransporter is developmentally regulated in postnatal rat brains: a possible mechanism underlying GABA's excitatory role in immature brain. J Neurobiol 33: 781-795, 1997.
67. Reed DJ, Withrow CD, Woodbury DM. Electrolyte and acid-base parameters of rat cerebrospinal fluid. Exp Brain Res 3: 212-219, 1967.
68. - cotransporter KCC2 and carbonic anhydrase CAVII. J Physiol 562: 27-36, 2005.
69. - co-transporter KCC2 renders GABA hyperpolarizing during neuronal maturation. Nature 397: 251-255, 1999.
70. - in rat primary afferent neurons. Soc Neurosci Abstr 246.1/09, 2006.
71. Rudomin P, Schmidt RF. Presynaptic inhibition in the vertebrate spinal cord revisited. Exp Brain Res 129: 1-37, 1999.
72. Russell JM. Sodium-potassium-chloride cotransport. Physiol Rev 80: 211-276, 2000.
73. -. J Neurophysiol 89: 159 -167, 2003.
74. Schrock H, Kuschinsky W. Cerebrospinal fluid ionic regulation, cerebral blood flow, and glucose use during chronic metabolic alkalosis. Am J Physiol Heart Circ Physiol 257: H1220-1227, 1989.
75. Song XJ, Wang ZB, Gan Q, Walters ET. cAMP and cGMP contribute to sensory neuron hyperexcitability and hyperalgesia in rats with dorsal root ganglia compression. J Neurophysiol 95: 479-492, 2006.
76. A receptor function following gene transfer of the CLC-2 chloride channel. Neuron 17: 543-551, 1996.
77. Stein V, Hermans-Borgmeyer I, Jentsch TJ, Hubner CA. Expression of the KCl cotransporter KCC2 parallels neuronal maturation and the emergence of low intracellular chloride. J Comp Neurol 468: 57-64, 2004.
78. Strange K, Denton J, Nehrke K. Ste20-type kinases: evolutionarily conserved regulators of ion transport and cell volume. Physiology 21: 61-68, 2006.
79. A receptor-mediated currents in dorsal root ganglion neurons isolated from Na-K-2Cl cotransporter null mice. J Neurosci 20: 7531-7538, 2000.
80. - cotransporter mRNAs (KCC1, KCC2, and NKCC1) in rat trigeminal nervous system. Brain Res Mol Brain Res 133: 12-18, 2005.
81. - cotransporter in the development of capsaicin-induced neurogenic inflammation. J Neurophysiol 95: 3553-3561, 2006.
82. 2+ exchange in rat dorsal root ganglion neurons. J Neurophysiol 77: 484-490, 1997.
83. Verkman AS, Sellers MC, Chao AC, Leung T, Ketcham R. Synthesis and characterization of improved chloride-sensitive fluorescent indicators for biological applications. Anal Biochem 178: 355-361, 1989.
84. Villiere V, McLachlan EM. Electrophysiological properties of neurons in intact rat dorsal root ganglia classified by conduction velocity and action potential duration. J Neurophysiol 76: 1924-1941, 1996.
85. Wang H, Yan Y, Kintner DB, Lytle C, Sun D. GABA-mediated trophic effect on oligodendrocytes requires Na-K-2Cl cotransport activity. J Neurophysiol 90: 1257-1265, 2003.
86. Willis WD. John Eccles' studies of spinal cord presynaptic inhibition. Prog Neurobiol 78: 189-214, 2006.
87. Willis WD. Dorsal root potentials and dorsal root reflexes: a double-edged sword. Exp Brain Res 124: 395-421, 1999.
88. Yamada J, Okabe A, Toyoda H, Kilb W, Luhmann HJ, Fukuda A. Cl- uptake promoting depolarizing GABA actions in immature rat neocortical neurones is mediated by NKCC1. J Physiol 557: 829-841, 2004.
89. Yu K, Kocsis JD. Schwann cell engraftment into injured peripheral nerve prevents changes in action potential properties. J Neurophysiol 94: 1519-1527, 2005.
90. Zhang JM, Song XJ, LaMotte RH. Enhanced excitability of sensory neurons in rats with cutaneous hyperalgesia produced by chronic compression of the dorsal root ganglion. J Neurophysiol 82: 3359-3366, 1999.
91. Zheng JH, Walters ET, Song XJ. Dissociation of dorsal root ganglion neurons induces hyperexcitability that is maintained by increased responsiveness to cAMP and cGMP. J Neurophysiol 97: 15-25, 2007.
92. Zhu L, Lovinger D, Delpire E. Cortical neurons lacking KCC2 expression show impaired regulation of intracellular chloride. J Neurophysiol 93: 1557-1568, 2005.