Transplant-mediated enhancement of spinal cord GABAergic inhibition reverses paclitaxel-induced mechanical and heat hypersensitivity

Pain

Volumn 156, Issue 6, 2015, Pages 1084-1091

  Bráz, João M ^a   Wang, Xidao ^a   Guan, Zhonghui ^a   Rubenstein, John L ^a   Basbaum, Allan I ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

GABA; Mouse; Neuropathic pain; Paclitaxel; Spinal cord; Transplantation

Indexed keywords

4 AMINOBUTYRIC ACID; ACTIVATING TRANSCRIPTION FACTOR 3; BETA ACTIN; BIOLOGICAL MARKER; GLUTAMATE DECARBOXYLASE 65; GLUTAMATE DECARBOXYLASE 67; IBA 1 PROTEIN; MESSENGER RNA; PACLITAXEL; PEPTIDES AND PROTEINS; UNCLASSIFIED DRUG; VESICULAR INHIBITORY AMINO ACID TRANSPORTER; ANTINEOPLASTIC AGENT; ATF3 PROTEIN, MOUSE; GLUTAMATE DECARBOXYLASE; GLUTAMATE DECARBOXYLASE 1; GLUTAMATE DECARBOXYLASE 2; VIAAT PROTEIN, MOUSE;

4 AMINOBUTYRIC ACID RELEASE; ADULT; ALLODYNIA; ANALGESIA; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINOCICEPTION; ARTICLE; CANCER CHEMOTHERAPY; CONTROLLED STUDY; GABAERGIC SYSTEM; HEAT HYPERALGESIA; HEAT PAIN THRESHOLD; HYPERALGESIA; INTERNEURON; MALE; MECHANICAL HYPERALGESIA; MEDIAN EMINENCE; MOUSE; NEURAL STEM CELL TRANSPLANTATION; NEUROPATHIC PAIN; NONHUMAN; PRIORITY JOURNAL; SPINAL CORD; UPREGULATION; ANIMAL; C57BL MOUSE; CELL COUNT; CELL TRANSPLANTATION; CHEMICALLY INDUCED; DISEASE MODEL; GENETICS; METABOLISM; PAIN MEASUREMENT; PAIN THRESHOLD; PROCEDURES; TRANSGENIC MOUSE;

ACTIVATING TRANSCRIPTION FACTOR 3; ANIMALS; ANTINEOPLASTIC AGENTS, PHYTOGENIC; CELL COUNT; CELL TRANSPLANTATION; DISEASE MODELS, ANIMAL; GAMMA-AMINOBUTYRIC ACID; GLUTAMATE DECARBOXYLASE; HYPERALGESIA; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PACLITAXEL; PAIN MEASUREMENT; PAIN THRESHOLD; SPINAL CORD; VESICULAR INHIBITORY AMINO ACID TRANSPORT PROTEINS;

EID: 84931288626     PISSN: 03043959     EISSN: 18726623     Source Type: Journal    
DOI: 10.1097/j.pain.0000000000000152     Document Type: Article

References (50)

1. Authier N, Gillet JP, Fialip J, Eschalier A, Coudore F. Description of a short-term Taxol-induced nociceptive neuropathy in rats. Brain Res 2000;887:239-49.
2. Baraban SC, Southwell DG, Estrada RC, Jones DL, Sebe JY, Alfaro-Cervello C, Garcia-Verdugo JM, Rubenstein JL, Alvarez-Buylla A. Reduction of seizures by transplantation of cortical GABAergic interneuron precursors into Kv1.1 mutant mice. Proc Natl Acad Sci U S A 2009;106:15472-7.
3. Bardoni R, Takazawa T, Tong CK, Choudhury P, Scherrer G, Macdermott AB. Pre-and postsynaptic inhibitory control in the spinal cord dorsal horn. Ann N Y Acad Sci 2013;1279:90-6.
4. Braz J, Solorzano C, Wang X, Basbaum AI. Transmitting pain and itch messages: a contemporary view of the spinal cord circuits that generate gate control. Neuron 2014;82:522-36.
5. Braz JM, Basbaum AI. Differential ATF3 expression in dorsal root ganglion neurons reveals the profile of primary afferents engaged by diverse noxious chemical stimuli. PAIN 2010;150:290-301.
6. Braz JM, Juarez-Salinas D, Ross SE, Basbaum AI. Transplant restoration of spinal cord inhibitory controls ameliorates neuropathic itch. JClin Invest 2014;124:3612-6.
7. Braz JM, Sharif-Naeini R, Vogt D, Kriegstein A, Alvarez-Buylla A, Rubenstein JL, Basbaum AI. Forebrain GABAergic neuron precursors integrate into adult spinal cord and reduce injury-induced neuropathic pain. Neuron 2012;74:663-75.
8. Cao YQ, Mantyh PW, Carlson EJ, Gillespie AM, Epstein CJ, Basbaum AI. Primary afferent tachykinins are required to experience moderate to intense pain. Nature 1998;392:390-4.
9. Castro-Lopes JM, Tavares I, Coimbra A. GABA decreases in the spinal cord dorsal horn after peripheral neurectomy. Brain Res 1993;620: 287-91.
10. Cata JP,Weng HR, Chen JH, Dougherty PM. Altered discharges of spinal wide dynamic range neurons and down-regulation of glutamate transporter expression in rats with paclitaxel-induced hyperalgesia. Neuroscience 2006;138:329-38.
11. Cavanaugh DJ, Lee H, Lo L, Shields SD, Zylka MJ, Basbaum AI, Anderson DJ. Distinct subsets of unmyelinated primary sensory fibers mediate behavioral responses to noxious thermal and mechanical stimuli. Proc Natl Acad Sci U S A 2009;106:9075-80.
12. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL. Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 1994; 53:55-63.
13. Chen SR, Zhu L, Chen H, Wen L, Laumet G, Pan HL. Increased spinal cord Na1-K1-2Cl-cotransporter-1 (NKCC1) activity contributes to impairment of synaptic inhibition in paclitaxel-induced neuropathic pain. J Biol Chem 2014;289:31111-20.
14. Chen Y, Yang C, Wang ZJ. Proteinase-activated receptor 2 sensitizes transient receptor potential vanilloid 1, transient receptor potential vanilloid 4, and transient receptor potential ankyrin 1 in paclitaxelinduced neuropathic pain. Neuroscience 2011;193:440-51.
15. Dirig DM, Yaksh TL. Intrathecal baclofen and muscimol, but not midazolam, are antinociceptive using the rat-formalin model. J Pharmacol Exp Ther 1995;275:219-27.
16. Eaton MJ, Plunkett JA, Karmally S, Martinez MA, Montanez K. 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 1998;16: 57-72.
17. Flatters SJ, Bennett GJ. Studies of peripheral sensory nerves in paclitaxel-induced painful peripheral neuropathy: evidence for mitochondrial dysfunction. PAIN 2006;122:245-57.
18. Fukuoka T, Tokunaga A, Kondo E, Miki K, Tachibana T, Noguchi K. Change in mRNAs for neuropeptides and the GABA(A) receptor in dorsal root ganglion neurons in a rat experimental neuropathic painmodel. PAIN 1998;78:13-26.
19. Hammond DL, Drower EJ. Effects of intrathecally administered THIP, baclofen and muscimol on nociceptive threshold. Eur J Pharmacol 1984; 103:121-5.
20. Hwang JH, Yaksh TL. The effect of spinal GABA receptor agonists on tactile allodynia in a surgically-induced neuropathic pain model in the rat. PAIN 1997;70:15-22.
21. Ibuki T, Hama AT, Wang XT, Pappas GD, Sagen J. Loss of GABAimmunoreactivity in the spinal dorsal horn of rats with peripheral nerve injury and promotion of recovery by adrenal medullary grafts. Neuroscience 1997;76:845-58.
22. Jergova S, Hentall ID, Gajavelli S, Varghese MS, Sagen J. Intraspinal transplantation of GABAergic neural progenitors attenuates neuropathic pain in rats: a pharmacologic and neurophysiological evaluation. Exp Neurol 2012;234:39-49.
23. Jimenez-Andrade JM, Peters CM, Mejia NA, Ghilardi JR, Kuskowski MA, Mantyh PW. Sensory neurons and their supporting cells located in the trigeminal, thoracic and lumbar ganglia differentially express markers of injury following intravenous administration of paclitaxel in the rat. Neurosci Lett 2006;405:62-7.
24. Kardon AP, Polgar E, Hachisuka J, Snyder LM, Cameron D, Savage S, Cai X, Karnup S, Fan CR, Hemenway GM, Bernard CS, Schwartz ES, Nagase H, Schwarzer C, Watanabe M, Furuta T, Kaneko T, Koerber HR, Todd AJ, Ross SE. Dynorphin acts as a neuromodulator to inhibit itch in the dorsal horn of the spinal cord. Neuron 2014;82:573-86.
25. Knabl J,Witschi R, Hosl K, Reinold H, Zeilhofer UB, Ahmadi S, Brockhaus J, Sergejeva M, Hess A, Brune K, Fritschy JM, Rudolph U, Mohler H, Zeilhofer HU. Reversal of pathological pain through specific spinal GABAA receptor subtypes. Nature 2008;451:330-4.
26. Kohno T, Moore KA, Baba H, Woolf CJ. Peripheral nerve injury alters excitatory synaptic transmission in lamina II of the rat dorsal horn. J Physiol 2003;548:131-8.
27. Kumru H, Kofler M, Flores MC, Portell E, Robles V, Leon N, Vidal J. Effect of intrathecal baclofen on evoked pain perception: an evoked potentials and quantitative thermal testing study. Eur J Pain 2013;17:1039-47.
28. Liu CC, Lu N, Cui Y, Yang T, Zhao ZQ, Xin WJ, Liu XG. Prevention of paclitaxel-induced allodynia by minocycline: effect on loss of peripheral nerve fibers and infiltration of macrophages in rats. Mol Pain 2010;6:76.
29. Madisen L, Zwingman TA, Sunkin SM, Oh SW, Zariwala HA, Gu H, Ng LL, Plamiter RD, Hawrylycz MJ, Jones AR, Lein ES, Zeng H. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat Neurosci 2010;13:133-40.
30. Munro G, Ahring PK, Mirza NR. Developing analgesics by enhancing spinal inhibition after injury: GABAA receptor subtypes as novel targets. Trends Pharmacol Sci 2009;30:453-9.
31. Narita M, Yoshida T, Nakajima M, Narita M, Miyatake M, Takagi T, Yajima Y, Suzuki T. Direct evidence for spinal cord microglia in the development of a neuropathic pain-like state in mice. J Neurochem 2006;97:1337-48.
32. Peters CM, Jimenez-Andrade JM, Kuskowski MA, Ghilardi JR, Mantyh PW. An evolving cellular pathology occurs in dorsal root ganglia, peripheral nerve and spinal cord following intravenous administration of paclitaxel in the rat. Brain Res 2007;1168:46-59.
33. Pevida M, Lastra A, Hidalgo A, Baamonde A, Menendez L. Spinal CCL2 and microglial activation are involved in paclitaxel-evoked cold hyperalgesia. Brain Res Bull 2013;95:21-7.
34. Polgar E, Gray S, Riddell JS, Todd AJ. Lack of evidence for significant neuronal loss in laminae I-III of the spinal dorsal horn of the rat in the chronic constriction injury model. PAIN 2004;111:144-50.
35. Polomano RC, Mannes AJ, Clark US, Bennett GJ. A painful peripheral neuropathy in the rat produced by the chemotherapeutic drug, paclitaxel. PAIN 2001;94:293-304.
36. Potter GB, Petryniak MA, Shevchenko E, McKinsey GL, Ekker M, Rubenstein JL. Generation of Cre-transgenic mice using Dlx1/Dlx2 enhancers and their characterization in GABAergic interneurons. Mol Cell Neurosci 2009;40:167-86.
37. Ross SE, Mardinly AR, McCord AE, Zurawski J, Cohen S, Jung C, Hu L, Mok SI, Shah A, Savner EM, Tolias C, Corfas R, Chen S, Inquimbert P, Xu Y, McInnes RR, Rice FL, Corfas G, Ma Q, Woolf CJ, Greenberg ME. Loss of inhibitory interneurons in the dorsal spinal cord and elevated itch in Bhlhb5 mutant mice. Neuron 2010;65:886-98.
38. Scholz J, Broom DC, Youn DH, Mills CD, Kohno T, Suter MR, Moore KA, Decosterd I, Coggeshall RE, Woolf CJ. 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 2005; 25:7317-23.
39. Shields SD, Eckert WA III, Basbaum AI. Spared nerve injury model of neuropathic pain in the mouse: a behavioral and anatomic analysis. J Pain 2003;4:465-70.
40. Smith SB, Crager SE, Mogil JS. Paclitaxel-induced neuropathic hypersensitivity in mice: responses in 10 inbred mouse strains. Life Sci 2004;74:2593-604.
41. Sugimoto T, Bennett GJ, Kajander KC. Transsynaptic degeneration in the superficial dorsal horn after sciatic nerve injury: effects of a chronic constriction injury, transection, and strychnine. PAIN 1990;42: 205-13.
42. Sweitzer SM, Schubert P, DeLeo JA. Propentofylline, a glial modulating agent, exhibits antiallodynic properties in a rat model of neuropathic pain. J Pharmacol Exp Ther 2001;297:1210-7.
43. Tamamaki N, Yanagawa Y, Tomioka R, Miyazaki J, Obata K, Kaneko T. Green fluorescent protein expression and colocalization with calretinin, parvalbumin, and somatostatin in the GAD67-GFP knock-in mouse. J Comp Neurol 2003;467:60-79.
44. Tong Q, Ye CP, Jones JE, Elmquist JK, Lowell BB. Synaptic release of GABA by AgRP neurons is required for normal regulation of energy balance. Nat Neurosci 2008;11:998-1000.
45. Tsuda M, Shigemoto-Mogami Y, Koizumi S, Mizokoshi A, Kohsaka S, Salter MW, Inoue K. P2X4 receptors induced in spinal microglia gate tactile allodynia after nerve injury. Nature 2003;424:778-83.
46. Tsujino H, Kondo E, Fukuoka T, Dai Y, Tokunaga A, Miki K, Yonenobu K, Ochi T, Noguchi K. Activating transcription factor 3 (ATF3) induction by axotomy in sensory and motoneurons: a novel neuronal marker of nerve injury. Mol Cell Neurosci 2000;15:170-82.
47. Watkins LR, Milligan ED, Maier SF. Spinal cord glia: new players in pain. PAIN 2001;93:201-5.
48. Zeilhofer HU, Wildner H, Yevenes GE. Fast synaptic inhibition in spinal sensory processing and pain control. Physiol Rev 2012;92:193-235.
49. Zhang J, Cavanaugh DJ, Nemenov MI, Basbaum AI. The modalityspecific contribution of peptidergic and non-peptidergic nociceptors is manifest at the level of dorsal horn nociresponsive neurons. J Physiol 2013;591:1097-110.
50. Zuniga RE, Schlicht CR, Abram SE. Intrathecal baclofen is analgesic in patients with chronic pain. Anesthesiology 2000;92:876-80.