Spinal nerve ligation decreases γ-aminobutyric acid B receptors on specific populations of immunohistochemically identified neurons in L5 dorsal root ganglion of the rat

Journal of Comparative Neurology

Volumn 520, Issue 8, 2012, Pages 1663-1677

  Engle, Mitchell P ^a,b   Merrill, Michelle A ^a   Marquez De Prado, Blanca ^a   Hammond, Donna L ^a  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

Mechanical allodynia; Neuropathic pain; Primary afferent neuron

Indexed keywords

4 AMINOBUTYRIC ACID B RECEPTOR; CALCITONIN GENE RELATED PEPTIDE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; ISOLECTIN B4; MESSENGER RNA; NEURON SPECIFIC NUCLEAR PROTEIN;

ALLODYNIA; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL LABELING; CONTROLLED STUDY; CYTOPLASM; DOWN REGULATION; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; NERVE LIGATION; NEUROFILAMENT; NEUROPATHIC PAIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; REAL TIME POLYMERASE CHAIN REACTION; SATELLITE CELL; SENSORY NERVE CELL; SPINAL GANGLION; SPINAL NERVE;

ANIMALS; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GANGLIA, SPINAL; IMMUNOHISTOCHEMISTRY; LIGATION; LUMBOSACRAL REGION; MALE; MICROSCOPY, CONFOCAL; NEURALGIA; NEURONS, AFFERENT; RATS; RATS, SPRAGUE-DAWLEY; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, GABA-B; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SPINAL NERVES;

EID: 84859299155     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.23005     Document Type: Article

References (83)

1. Ataka T, Kumamoto E, Shimoji K, Yoshimura M. 2000. Baclofen inhibits more effectively C-afferent than Adelta-afferent glutamatergic transmission in substantia gelatinosa neurons of adult rat spinal cord slices. Pain 86: 273-282.
2. B receptors. Pharmacol Ther 110: 533-543.
3. Boucher TJ, Okuse K, Bennett DL, Munson JB, Wood JN, McMahon SB. 2000. Potent analgesic effects of GDNF in neuropathic pain states. Science 290: 124-127.
4. 2+/calmodulin-dependent protein kinase II a-containing dorsal root ganglion neurons in the rat: colocalization with isolectin Griffonia simplicifolia, calcitonin gene-related peptide, or vanilloid receptor 1. J Comp Neurol 448: 102-110.
5. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL. 1994. Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 53: 55-63.
6. Choi Y, Yoon YW, Na HS, Kim SH, Chung JM. 1994. Behavioral signs of ongoing pain and cold allodynia in a rat model of neuropathic pain. Pain 59: 369-376.
7. Cocchia D, Michetti F. 1981. S-100 antigen in satellite cells of the adrenal medulla and the superior cervical ganglion of the rat. An immunochemical and immunocytochemical study. Cell Tissue Res 215: 103-112.
8. Coggeshall RE. 1992. A consideration of neural counting methods. Trends Neurosci 15: 9-13.
9. Coggeshall RE, Lekan HA. 1996. Methods for determining numbers of cells and synapses: a case for more uniform standards of review J Comp Neurol 364: 6-15.
10. B receptors: a new paradigm in G protein signaling. Mol Cell Neurosci 16: 296-312.
11. Degn J, Tandrup T, Jakobsen J. 1999. Effect of nerve crush on perikaryal number and volume of neurons in adult rat dorsal root ganglion. J Comp Neurol 412: 186-192.
12. Djouhri L, Koutsikou S, Fang X, McMullan S, Lawson SN. 2006. Spontaneous pain, both neuropathic and inflammatory, is related to frequency of spontaneous firing in intact C-fiber nociceptors. J Neurosci 26: 1281-1292.
13. B2 protein mRNA in the rat CNS. Mol Brain Res 71: 185-200.
14. Eaton MJ, Plunkett JA, Karmally S, Martinez MA, Montanez K. 1998. Changes in GAD- and GABA- immunoreactivity in the spinal dorsal horn after peripheral nerve injury and promotion of recovery by lumbar transplant of immortalized serotonergic precursors. J Chem Neuroanat 16: 57-72.
15. B receptors in spinal cord and dorsal root ganglia of the rat. Neuroscience 138: 1277-1287.
16. B2 during postnatal development in rodent brain. J Comp Neurol 477: 235-252.
17. A receptor in dorsal root ganglion neurons in a rat experimental neuropathic pain model. Pain 78: 13-26.
18. Fukuoka T, Kondo E, Dai Y, Hashimoto N, Noguchi K. 2001. Brain-derived neurotrophic factor increases in the uninjured dorsal root ganglion neurons in selective spinal nerve ligation model. J Neurosci 21: 4891-4900.
19. 3, increases in the spared L4 DRG in rats with L5 spinal nerve ligation. Pain 99: 111-120.
20. B receptors in peripheral nociceptors in vivo. Mol Pain 5: 68.
21. B(2)-deficient mice. J Neurosci 24: 6086-6097.
22. Go VLW, Yaksh TL. 1987. Release of substance P from the cat spinal cord. J Physiol (Lond) 391: 141-167.
23. Goldstein ME, Cooper HS, Bruce J, Carden MJ, Lee VM, Schlaepfer WW. 1987. Phosphorylation of neurofilament proteins and chromatolysis following transection of rat sciatic nerve. J Neurosci 7: 1586-1594.
24. Gonzalez-Martinez T, Perez-Pinera P, Diaz-Esnal B, Vega JA. 2003. S-100 proteins in the human peripheral nervous system. Microsc Res Tech 60: 633-638.
25. Hammond DL. 1997. Inhibitory neurotransmitters and nociception: role of GABA and glycine. In: Dickenson A, Besson JM, editors. The pharmacology of pain. Berlin: Springer. p 361-384.
26. Hammond DL, Ackerman L, Holdsworth R, Elzey B. 2004. Effects of spinal nerve ligation on immunohistochemically identified neurons in the L4 and L5 dorsal root ganglia of the rat. J Comp Neurol 475: 575-589.
27. B) receptor antagonist CGP 35348 induces hypersensitivity to mechanical stimuli in the rat. Neurosci Lett 182: 299-302.
28. Hogan Q, Sapunar D, Modric-Jednacak K, McCallum JB. 2004. Detection of neuropathic pain in a rat model of peripheral nerve injury. Anesthesiology 101: 476-487.
29. Hudson LJ, Bevan S, McNair K, Gentry C, Fox A, Kuhn R, Winter J. 2002. Metabotropic glutamate receptor 5 upregulation in A-fibers after spinal nerve injury: 2-methyl-6-(phenylethynyl)-pyridine (MPEP) reverses the induced thermal hyperalgesia. J Neurosci 22: 2660-2668.
30. Ibuki T, Hama AT, Wang X-T, Pappas GD, Sagen J. 1997. Loss of GABA-immunoreactivity in the spinal dorsal horn of rats with peripheral nerve injury and promotion of recovery by adrenal medullary grafts. Neuroscience 76: 845-858.
31. Iyadomi M, Iyadomi I, Kumamoto E, Tomokuni K, Yoshimura M. 2000. Presynaptic inhibition by baclofen of miniature EPSCs and IPSCs in substantia gelatinosa neurons of the adult rat spinal dorsal horn. Pain 85: 385-393.
32. Kangrga I, Jiang M, Randic M. 1991. Actions of (-) baclofen on rat dorsal horn neurons. Brain Res 562: 265-275.
33. Kim SH, Chung JM. 1992. An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 50: 355-363.
34. 4 into peripheral nerves. Neuroscience 54: 545-551.
35. Koltzenburg M, Wall PD, McMahon SB. 1999. Does the right side know what the left is doing? Trends Neurosci 22: 122-127.
36. Kosaras B, Jakubowski M, Kainz V, Burstein R. 2009. Sensory innervation of the calvarial bones of the mouse. J Comp Neurol 515: 331-348.
37. Lever I, Cunningham J, Grist J, Yip PK, Malcangio M. 2003. Release of BDNF and GABA in the dorsal horn of neuropathic rats. Eur J Neurosci 18: 1169-1174.
38. Liu CN, Wall PD, Ben-Dor E, Michaelis M, Amir R, Devor M. 2000a. Tactile allodynia in the absence of C-fiber activation: altered firing properties of DRG neurons following spinal nerve injury. Pain 85: 503-521.
39. Liu X, Eschenfelder S, Blenk KH, Janig W, Habler H. 2000b. Spontaneous activity of axotomized afferent neurons after L5 spinal nerve injury in rats. Pain 84: 309-318.
40. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25: 402-408.
41. Ma C, Shu Y, Zheng Z, Chen Y, Yao H, Greenquist KW, White FA, LaMotte RH. 2003. Similar electrophysiological changes in axotomized and neighboring intact dorsal root ganglion neurons. J Neurophysiol 89: 1588-1602.
42. A receptor activation, inhibits electrically evoked substance P-like immunoreactivity release from the rat spinal cord in vitro. J Pharmacol Exp Ther 266: 1490-1496.
43. Martin SC, Steiger JL, Gravielle MC, Lyons HR, Russek SJ, Farb DH. 2004. Differential expression of γ-aminobutyric acid type B receptor subunit mRNAs in the developing nervous system and receptor coupling to adenylyl cyclase in embryonic neurons. J Comp Neurol 473: 16-29.
44. B receptor gene expression in rat spinal cord. Neuropharmacology 38: 1767-1773.
45. Mullen RJ, Buck CR, Smith AM. 1992. NeuN, a neuronal specific nuclear protein in vertebrates. Development 116: 201-211.
46. Nagano M, Sakai A, Takahashi N, Umino M, Yoshioka K, Suzuki H. 2003. Decreased expression of glial cell line-derived neurotrophic factor signaling in rat models of neuropathic pain. Br J Pharmacol 140: 1252-1260.
47. B receptor coupling to G-proteins and ion channels. Adv Pharmacol 58: 123-147.
48. Perry MJ, Lawson SN, Robertson J. 1991. Neurofilament immunoreactivity in populations of rat primary afferent neurons: a quantitative study of phosphorylated and non-phosphorylated subunits. J Neurocytol 20: 746-758.
49. B receptors: physiological functions and mechanisms of diversity. Adv Pharmacol 58: 231-255.
50. B, and NK1 receptors of major pain control medullary areas in pathways targeting the rat spinal cord: implications for descending modulation of nociceptive transmission. J Comp Neurol 510: 175-187.
51. Polgar E, Hughes DI, Riddell JS, Maxwell DJ, Puskar Z, Todd AJ. 2003. Selective loss of spinal GABAergic or glycinergic neurons is not necessary for development of thermal hyperalgesia in the chronic constriction injury model of neuropathic pain. Pain 104: 229-239.
52. B R1a and R1b in the rat CNS and dorsal root ganglia. Anat Embryol (Berl) 201: 1-13.
53. Popken GJ, Farel PB. 1997. Sensory neuron number in neonatal and adult rats estimated by means of stereologic and profile-based methods. J Comp Neurol 386: 8-15.
54. B binding sites in mammalian spinal cord. Synapse 1: 530-538.
55. Rezajooi K, Pavlides M, Winterbottom J, Stallcup WB, Hamlyn PJ, Lieberman AR, Anderson PN. 2004. NG2 proteoglycan expression in the peripheral nervous system: upregulation following injury and comparison with CNS lesions. Mol Cell Neurosci 25: 572-584.
56. Robertson B, Perry MJ, Lawson SN. 1991. Populations of rat spinal primary afferent neurons with choleragenoid binding compared with those labelled by markers for neurofilament and carbohydrate groups: a quantitative immunocytochemical study. J Neurocytol 20: 387-395.
57. Sandkuhler J. 2009. Models and mechanisms of hyperalgesia and allodynia. Physiol Rev 89: 707-758.
58. Sapunar D, Ljubkovic M, Lirk P, McCallum JB, Hogan QH. 2005. Distinct membrane effects of spinal nerve ligation on injured and adjacent dorsal root ganglion neurons in rats. Anesthesiology 103: 360-376.
59. Schäfers M, Sorkin LS, Geis C, Shubayev VI. 2003. Spinal nerve ligation induces transient upregulation of tumor necrosis factor receptors 1 and 2 in injured and adjacent uninjured dorsal root ganglia in the rat. Neurosci Lett 347: 179-182.
60. Schionning JD, Larsen JO, Tandrup T, Braendgaard H. 1998. Selective degeneration of dorsal root ganglia and dorsal nerve roots in methyl mercury-intoxicated rats: a stereological study. Acta Neuropathol (Berl) 96: 191-201.
61. B receptors. Neuroscience 20: 385-393.
62. Schmalbruch H. 1987. The number of neurons in dorsal root ganglia L4-L6 of the rat. Anat Rec 219: 315-322.
63. Scholz J, Broom DC, Youn DH, Mills CD, Kohno T, Suter MR, Moore KA, Decosterd I, Coggeshall RE, Woolf CJ. 2005. Blocking caspase activity prevents transsynaptic neuronal apoptosis and the loss of inhibition in lamina II of the dorsal horn after peripheral nerve injury. J Neurosci 25: 7317-7323.
64. B(1). Neuron 31: 47-58.
65. Somers DL, Clemente FR. 2002. Dorsal horn synaptosomal content of aspartate, glutamate, glycine and GABA are differentially altered following chronic constriction injury to the rat sciatic nerve. Neurosci Lett 323: 171-174.
66. Stefansson K, Wollmann RL, Moore BW. 1982. Distribution of S-100 protein outside the central nervous system. Brain Res 234: 309-317.
67. Stiller CO, Cui JG, O'Connor WT, Brodin E, Meyerson BA, Linderoth B. 1996. Release of γ-aminobutyric acid in the dorsal horn and suppression of tactile allodynia by spinal cord stimulation in mononeuropathic rats. Neurosurgery 39: 367-374.
68. Streit WJ, Schulte BA, Balentine JD, Spicer SS. 1986. Evidence for glycoconjugate in nociceptive primary sensory neurons and its origin from the Golgi complex. Brain Res 377: 1-17.
69. Sukhotinsky I, Ben-Dor E, Raber P, Devor M. 2004. Key role of the dorsal root ganglion in neuropathic tactile hypersensibility. Eur J Pain 8: 135-143.
70. Tandrup T. 1993. A method for unbiased and efficient estimation of number and mean volume of specified neuron subtypes in rat dorsal root ganglion. J Comp Neurol 329: 269-276.
71. Todd AJ. 2010. Neuronal circuitry for pain processing in the dorsal horn. Nat Rev Neurosci 11: 823-836.
72. B receptor protein and mRNA distribution in rat spinal cord and dorsal root ganglia. Eur J Neurosci 12: 3201-3210.
73. Vestergaard S, Tandrup T, Jakobsen J. 1997. Effect of permanent axotomy on number and volume of dorsal root ganglion cell bodies. J Comp Neurol 388: 307-312.
74. Wang HF, Robertson B, Grant G. 1998. Anterograde transport of horseradish-peroxidase conjugated isolectin B4 from Griffonia simplicifolia I in spinal primary sensory neurons of the rat. Brain Res 811: 34-39.
75. B receptor function in spinal superficial dorsal horn neurons in rats with diabetic neuropathy. J Physiol (Lond) 579: 849-861.
76. B receptors in the spinal cord dorsal horn in diabetic neuropathy. Neurosci Lett 490: 112-115.
77. West MJ. 1999. Stereological methods for estimating the total number of neurons and synapses: issues of precision and bias. Trends Neurosci 22: 51-61.
78. Willcockson WS, Chung JM, Hori Y, Lee KH, Willis WD. 1984. Effects of iontophoretically released amino acids and amines on primate spinothalamic tract cells. J Neurosci 4: 732-740.
79. Wolf HK, Buslei R, Schmidt-Kastner R, Schmidt-Kastner PK, Pietsch T, Wiestler OD, Blumcke I. 1996. NeuN: a useful neuronal marker for diagnostic histopathology. J Histochem Cytochem 44: 1167-1171.
80. Yan H, Keast JR. 2008. Neurturin regulates postnatal differentiation of parasympathetic pelvic ganglion neurons, initial axonal projections, and maintenance of terminal fields in male urogenital organs. J Comp Neurol 507: 1169-1183.
81. B receptor in the spinal dorsal horn of adult rat. Brain Res Bull 55: 479-485.
82. B receptor-like immunoreactive terminals in the rat spinal dorsal horn. Brain Res Bull 58: 499-507.
83. Zhang XF, Zhu CZ, Thimmapaya R, Choi WS, Honore P, Scott VE, Kroeger PE, Sullivan JP, Faltynek CR, Gopalakrishnan M, Shieh CC. 2004. Differential action potentials and firing patterns in injured and uninjured small dorsal root ganglion neurons after nerve injury. Brain Res 1009: 147-158.