Intraspinal transplantation of GABAergic neural progenitors attenuates neuropathic pain in rats: A pharmacologic and neurophysiological evaluation

Experimental Neurology

Volumn 234, Issue 1, 2012, Pages 39-49

  Jergova, Stanislava ^a,b   Hentall, Ian D ^a   Gajavelli, Shyam ^a   Varghese, Mathew S ^a   Sagen, Jacqueline ^a  

^a UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^b INSTITUTE OF CHEMISTRY   (Slovakia)

Author keywords

GABA receptors; GABAergic progenitors; Neuropathic pain; Post discharges; Wind up

Indexed keywords

1 (4,4 DIPHENYL 3 BUTENYL)NIPECOTIC ACID; 3 AMINOPROPYL(DIETHOXYMETHYL)PHOSPHINIC ACID; 4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR; BICUCULLINE;

ALLODYNIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTINOCICEPTION; ARTICLE; CELL DIFFERENTIATION; CELL TRANSPLANTATION; CONTROLLED STUDY; ELECTROPHYSIOLOGY; FEMALE; GABAERGIC NEURAL PROGENITOR CELL; GABAERGIC TRANSMISSION; HYPERALGESIA; INTRASPINAL TRANSPLANTATION; MALE; NERVE CELL STIMULATION; NEURAL STEM CELL; NEUROPATHIC PAIN; NEUROPHYSIOLOGY; NONHUMAN; PRIORITY JOURNAL; RAT; SCIATIC NERVE; SPINAL CORD DORSAL HORN; SPINAL CORD INJURY; TREATMENT RESPONSE;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; DISEASE MODELS, ANIMAL; EMBRYO, MAMMALIAN; EMBRYONIC STEM CELLS; FEMALE; GABA AGENTS; GAMMA-AMINOBUTYRIC ACID; HYPERALGESIA; INJECTIONS, SPINAL; LAMINECTOMY; MALE; NERVE FIBERS; NEURONS; PAIN MEASUREMENT; PAIN THRESHOLD; PHYSICAL STIMULATION; PREGNANCY; RATS; RATS, SPRAGUE-DAWLEY; REACTION TIME; SCIATICA; SPINAL CORD; TEMPERATURE; TIME FACTORS;

EID: 84857501147     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2011.12.005     Document Type: Article

References (64)

1. 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.
2. Castro-Lopes J.M., Tavares I., Coimbra A. GABA decreases in the spinal cord dorsal horn after peripheral neurectomy. Brain Res. 1993, 620:287-291.
3. Cejas P.J., Martinez M., Karmally S., McKillop M., McKillop J., Plunkett J.A., Oudega M., Eaton M.J. Lumbar transplant of neurons genetically modified to secrete brain-derived neurotrophic factor attenuates allodynia and hyperalgesia after sciatic nerve constriction. Pain 2000, 86:195-210.
4. Chapman V., Suzuki R., Dickenson A.H. Electrophysiological characterization of spinal neuronal response properties in anaesthetized rats after ligation of spinal nerves L5-L6. J. Physiol. 1998, 507(Pt. 3):881-894.
5. Drew G.M., Siddall P.J., Duggan A.W. Mechanical allodynia following contusion injury of the rat spinal cord is associated with loss of GABAergic inhibition in the dorsal horn. Pain 2004, 109:379-388.
6. Eaton M.J., Wolfe S.Q. Clinical feasibility for cell therapy using human neuronal cell line to treat neuropathic behavioral hypersensitivity following spinal cord injury in rats. J. Rehabil. Res. Dev. 2009, 46:145-165.
7. Eaton M.J., Plunkett J.A., Karmally S., Martinez M.A., 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.
8. Eaton M.J., Martinez M.A., Karmally S. A single intrathecal injection of GABA permanently reverses neuropathic pain after nerve injury. Brain Res. 1999, 835:334.
9. Eaton M.J., Plunkett J.A., Martinez M.A., Lopez T., Karmally S., Cejas P., Whittemore S.R. Transplants of neuronal cells bioengineered to synthesize GABA alleviate chronic neuropathic pain. Cell Transplant. 1999, 8:87-101.
10. Eaton M.J., Wolfe S.Q., Martinez M., Hernandez M., Furst C., Huang J., Frydel B.R., Gomez-Marin O. Subarachnoid transplant of a human neuronal cell line attenuates chronic allodynia and hyperalgesia after excitotoxic spinal cord injury in the rat. J. Pain 2007, 8:33-50.
11. Eide P.K., Jorum E., Stenehjem A.E. Somatosensory findings in patients with spinal cord injury and central dysaesthesia pain. J. Neurol. Neurosurg. Psychiatry 1996, 60:411-415.
12. Felsby S., Nielsen J., Arendt-Nielsen L., Jensen T.S. NMDA receptor blockade in chronic neuropathic pain: a comparison of ketamine and magnesium chloride. Pain 1996, 64:283-291.
13. Furmanski O., Gajavelli S., Lee J.W., Collado M.E., Jergova S., Sagen J. Combined extrinsic and intrinsic manipulations exert complementary neuronal enrichment in embryonic rat neural precursor cultures: an in vitro and in vivo analysis. J. Comp. Neurol. 2009, 515:56-71.
14. Gwak Y.S., Tan H.Y., Nam T.S., Paik K.S., Hulsebosch C.E., Leem J.W. Activation of spinal GABA receptors attenuates chronic central neuropathic pain after spinal cord injury. J. Neurotrauma 2006, 23:1111-1124.
15. Hama A., Sagen J. Antinociceptive effects of the marine snail peptides conantokin-G and conotoxin MVIIA alone and in combination in rat models of pain. Neuropharmacology 2009, 56:556-563.
16. Hao J.X., Xu X.J., Wiesenfeld-Hallin Z. Intrathecal gamma-aminobutyric acidB (GABAB) receptor antagonist CGP 35348 induces hypersensitivity to mechanical stimuli in the rat. Neurosci. Lett. 1994, 182:299-302.
17. Hargreaves K., Dubner R., Brown F., Flores C., Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 1988, 32:77-88.
18. Hendricks W.A., Pak E.S., Owensby J.P., Menta K.J., Glazova M., Moretto J., Hollis S., Brewer K.L., Murashov A.K. Predifferentiated embryonic stem cells prevent chronic pain behaviors and restore sensory function following spinal cord injury in mice. Mol. Med. 2006, 12:34-46.
19. Hokfelt T., Zhang X., Xu X., Wiesenfeld-Hallin Z. Central consequences of peripheral nerve damage. Texbook Of Pain 2005, 947-961. Elsevier. S. McMahon, M. Koltzenburg (Eds.).
20. Hollrigel G.S., Toth K., Soltesz I. Neuroprotection by propofol in acute mechanical injury: role of GABAergic inhibition. J. Neurophysiol. 1996, 76:2412-2422.
21. Hwang J.H., Yaksh T.L. 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.
22. Ibuki T., Hama A.T., Wang X.T., Pappas G.D., Sagen J. Loss of GABA-immunoreactivity in the spinal dorsal horn of rats with peripheral nerve injury and promotion of recovery by adrenal medullary grafts. Neuroscience 1997, 76:845-858.
23. Jergova S., Furmanski O., Collado M., Varghese M., Gajavelli S., Manoah L., Hentall I., Sagen J. Behavioral and neurophysiological effects of GABAergic neuronal precursor cell transplantation in a rat model of chronic neuropathic pain. Soc. Neurosci. Abstr. 2009, 39. 458.454.
24. Jergova S., Varghese M., Gajavelli S., Hentall I., Sagen J. Pharmacologic and neurophysiological evaluation of antinociceptive effects of GABAergic neural progenitor cell transplants in the spinal cord following peripheral nerve injury. Soc. Neurosci. Abstr. 2010, 40. 681.616.
25. Jolkkonen J., Halonen T., Jolkkonen E., Nissinen J., Pitkanen A. Seizure-induced damage to the hippocampus is prevented by modulation of the GABAergic system. Neuroreport 1996, 7:2031-2035.
26. Kim D.S., Jung S.J., Nam T.S., Jeon Y.H., Lee D.R., Lee J.S., Leem J.W., Kim D.W. Transplantation of GABAergic neurons from ESCs attenuates tactile hypersensitivity following spinal cord injury. Stem Cells 2010, 28:2099-2108.
27. Laird J.M., Bennett G.J. An electrophysiological study of dorsal horn neurons in the spinal cord of rats with an experimental peripheral neuropathy. J. Neurophysiol. 1993, 69:2072-2085.
28. Lee J.W., Furmanski O., Castellanos D.A., Daniels L.A., Hama A.T., Sagen J. Prolonged nociceptive responses to hind paw formalin injection in rats with a spinal cord injury. Neurosci. Lett. 2008, 439:212-215.
29. Loomis C.W., Khandwala H., Osmond G., Hefferan M.P. Coadministration of intrathecal strychnine and bicuculline effects synergistic allodynia in the rat: an isobolographic analysis. J. Pharmacol. Exp. Ther. 2001, 296:756-761.
30. Lyden P.D., Lonzo L. Combination therapy protects ischemic brain in rats - a glutamate antagonist plus a gamma-aminobutyric-acid agonist. Stroke 1994, 25:189-195.
31. Malan T.P., Mata H.P., Porreca F. Spinal GABA(A) and GABA(B) receptor pharmacology in a rat model of neuropathic pain. Anesthesiology 2002, 96:1161-1167.
32. McDonald J.W., Liu X.Z., Qu Y., Liu S., Mickey S.K., Turetsky D., Gottlieb D.I., Choi D.W. Transplanted embryonic stem cells survive, differentiate and promote recovery in injured rat spinal cord. Nat. Med. 1999, 5:1410-1412.
33. Mitsui T., Kakizaki H., Tanaka H., Shibata T., Matsuoka I., Koyanagi T. Immortalized neural stem cells transplanted into the injured spinal cord promote recovery of voiding function in the rat. J. Urol. 2003, 170:1421-1425.
34. Moore K.A., Kohno T., Karchewski L.A., Scholz J., Baba H., Woolf C.J. Partial peripheral nerve injury promotes a selective loss of GABAergic inhibition in the superficial dorsal horn of the spinal cord. J. Neurosci. 2002, 22:6724-6731.
35. Mukhida K., Mendez I., McLeod M., Kobayashi N., Haughn C., Milne B., Baghbaderani B., Sen A., Behie L.A., Hong M. Spinal GABAergic transplants attenuate mechanical allodynia in a rat model of neuropathic pain. Stem Cells 2007, 25:2874-2885.
36. Palecek J., Dougherty P.M., Kim S.H., Paleckova V., Lekan H., Chung J.M., Carlton S.M., Willis W.D. Responses of spinothalamic tract neurons to mechanical and thermal stimuli in an experimental model of peripheral neuropathy in primates. J. Neurophysiol. 1992, 68:1951-1966.
37. Park W.B., Kim S.Y., Lee S.H., Kim H.W., Park J.S., Hyun J.K. The effect of mesenchymal stem cell transplantation on the recovery of bladder and hindlimb function after spinal cord contusion in rats. BMC Neurosci. 2010, 11:119.
38. Polgar E., Todd A.J. Tactile allodynia can occur in the spared nerve injury model in the rat without selective loss of GABA or GABA(A) receptors from synapses in laminae I-II of the ipsilateral spinal dorsal horn. Neuroscience 2008, 156:193-202.
39. Polgar E., Hughes D.I., Riddell J.S., Maxwell D.J., Puskar Z., Todd A.J. 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 2003, 104:229-239.
40. Polgar E., Gray S., Riddell J.S., Todd A.J. 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, 111:144-150.
41. Price D.D., Long S., Huitt C. Sensory testing of pathophysiological mechanisms of pain in patients with reflex sympathetic dystrophy. Pain 1992, 49:163-173.
42. Randall L.O., Selitto J.J. A method for measurement of analgesic activity on inflamed tissue. Arch. Int. Pharmacodyn. Ther. 1957, 111:409-419.
43. Reeve A.J., Dickenson A.H., Kerr N.C. Spinal effects of bicuculline: modulation of an allodynia-like state by an A1-receptor agonist, morphine, and an NMDA-receptor antagonist. J. Neurophysiol. 1998, 79:1494-1507.
44. Rexed B. The cytoarchitectonic organization of the spinal cord in the cat. J. Comp. Neurol. 1952, 96:414-495.
45. Robert W.T., Swati M., Jo-Anne L.A., Brianne F., Dalton L.W., Jane T.C.H., Andrea F.T., Christine S. A systematic review of pharmacologic treatments of pain after spinal cord injury. Arch. Phys. Med. Rehabil. 2010, 91:816-831.
46. Schoffnegger D., Heinke B., Sommer C., Sandkuhler J. Physiological properties of spinal lamina II GABAergic neurons in mice following peripheral nerve injury. J. Physiol. 2006, 577:869-878.
47. Schouenborg J. Functional and topographical properties of field potentials evoked in rat dorsal horn by cutaneous C-fibre stimulation. J. Physiol. 1984, 356:169-192.
48. Schuler V., Luscher C., Blanchet C., Klix N., Sansig G., Klebs K., Schmutz M., Heid J., Gentry C., Urban L., Fox A., Spooren W., Jaton A.L., Vigouret J., Pozza M., Kelly P.H., Mosbacher J., Froestl W., Kaslin E., Korn R., Bischoff S., Kaupmann K., van der Putten H., Bettler B. Epilepsy, hyperalgesia, impaired memory, and loss of pre- and postsynaptic GABA(B) responses in mice lacking GABA(B(1)). Neuron 2001, 31:47-58.
49. Sivilotti L., Nistri A. GABA receptor mechanisms in the central nervous system. Prog. Neurobiol. 1991, 36:35-92.
50. Sivilotti L., Woolf C.J. The contribution of GABAA and glycine receptors to central sensitization: disinhibition and touch-evoked allodynia in the spinal cord. J. Neurophysiol. 1994, 72:169-179.
51. Slonimski M., Abram S.E., Zuniga R.E. Intrathecal baclofen in pain management. Reg. Anesth. Pain Med. 2004, 29:269-276.
52. Sokal D.M., Chapman V. Spinal GABA(B)-receptor antagonism increases nociceptive transmission in vivo. Neuroreport 2001, 12:3247-3250.
53. Sokal D.M., Chapman V. Inhibitory effects of spinal baclofen on spinal dorsal horn neurones in inflamed and neuropathic rats in vivo. Brain Res. 2003, 987:67-75.
54. Stubley L.A., Martinez M.A., Karmally S., Lopez T., Cejas P., Eaton M.J. Only early intervention with gamma-aminobutyric acid cell therapy is able to reverse neuropathic pain after partial nerve injury. J. Neurotrauma 2001, 18:471-477.
55. Su H., Zhang W., Guo J., Guo A., Yuan Q., Wu W. Neural progenitor cells enhance the survival and axonal regeneration of injured motoneurons after transplantation into the avulsed ventral horn of adult rats. J. Neurotrauma 2009, 26:67-80.
56. Ugarte S.D., Homanics G.E., Firestone L.L., Hammond D.L. Sensory thresholds and the antinociceptive effects of GABA receptor agonists in mice lacking the beta3 subunit of the GABA(A) receptor. Neuroscience 2000, 95:795-806.
57. Vaysse L., Sol J.C., Lazorthes Y., Courtade-Saidi M., Eaton M.J., Jozan S. GABAergic pathway in a rat model of chronic neuropathic pain: modulation after intrathecal transplantation of a human neuronal cell line. Neurosci. Res. 2011, 69:111-120.
58. Vikman K.S., Siddall P.J., Duggan A.W. Increased responsiveness of rat dorsal horn neurons in vivo following prolonged intrathecal exposure to interferon-gamma. Neuroscience 2005, 135:969-977.
59. Vikman K.S., Duggan A.W., Siddall P.J. Interferon-gamma induced disruption of GABAergic inhibition in the spinal dorsal horn in vivo. Pain 2007, 133:18-28.
60. Wolfe S.Q., Garg M., Cumberbatch N.M., Furst C., Martinez M., Hernandez M., Reimers R., Berrocal Y., Gomez-Marin O., Eaton M.J. Optimizing the transplant dose of a human neuronal cell line graft to treat SCI pain in the rat. Neurosci. Lett. 2007, 414:121-125.
61. Xu X.J., Zhang X., Hokfelt T., Wiesenfeld-Hallin Z. Plasticity in spinal nociception after peripheral nerve section: reduced effectiveness of the NMDA receptor antagonist MK-801 in blocking wind-up and central sensitization of the flexor reflex. Brain Res. 1995, 670:342-346.
62. Yakhnitsa V., Linderoth B., Meyerson B.A. Spinal cord stimulation attenuates dorsal horn neuronal hyperexcitability in a rat model of mononeuropathy. Pain 1999, 79:223-233.
63. Yaksh T.L., Rudy T.A. Chronic catheterization of the spinal subarachnoid space. Physiol. Behav. 1976, 17:1031-1036.
64. Zhao Z.M., Li H.J., Liu H.Y., Lu S.H., Yang R.C., Zhang Q.J., Han Z.C. Intraspinal transplantation of CD34+ human umbilical cord blood cells after spinal cord hemisection injury improves functional recovery in adult rats. Cell Transplant. 2004, 13:113-122.