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The Journal of Neuroscience, September 29, 2004, 24(39):8494-8499; doi:10.1523/JNEUROSCI.2982-04.2004

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Neurobiology of Disease
Spinal Dorsal Horn Calcium Channel ₂-1 Subunit Upregulation Contributes to Peripheral Nerve Injury-Induced Tactile Allodynia

Chun-Ying Li,¹ Yan-Hua Song,³ Emiliano S. Higuera,³ and Z. David Luo^1,2

Departments of ¹Anesthesiology and ²Pharmacology, College of Medicine, University of California, Irvine, Irvine, California 92717, and ³Department of Anesthesiology, School of Medicine, University of California, San Diego, La Jolla, California 92093

Peripheral nerve injury induces upregulation of the calcium channel ₂-1 structural subunit in dorsal root ganglia (DRG) and dorsal spinal cord of spinal nerve-ligated rats with neuropathic pain, suggesting a role of the calcium channel ₂-1 subunit in central sensitization. To investigate whether spinal dorsal horn ₂-1 subunit upregulation derives from increased DRG ₂-1 subunit and plays a causal role in neuropathic pain development, we examined spinal dorsal horn₂-1 subunit expression with or without dorsal rhizotomy in spinal nerve-ligated rats and its correlation with tactile allodynia, a neuropathic pain state defined as reduced thresholds to non-noxious tactile stimulation. We also examined the effects of intrathecal ₂-1 antisense oligonucleotides on ₂-1 subunit expression and neuropathic allodynia in the nerve-ligated rats. Our data indicated that spinal nerve injury resulted in time-dependent₂-1 subunit upregulation in the spinal dorsal horn that correlated temporally with neuropathic allodynia development and maintenance. Dorsal rhizotomy diminished basal level expression and blocked injury-induced expression of the spinal dorsal horn₂-1 subunit and reversed injury-induced tactile allodynia. In addition, intrathecal ₂-1 antisense oligonucleotides blocked injury-induced dorsal horn ₂-1 subunit upregulation and diminished tactile allodynia. These findings indicate that ₂-1 subunit basal expression occurs presynaptically and postsynaptically in spinal dorsal horn. Nerve injury induces mainly presynaptic ₂-1 subunit expression that derives from increased ₂-1 subunit in injured DRG neurons. Thus, changes in presynaptic ₂-1 subunit expression contribute to injury-induced spinal neuroplasticity and central sensitization that underlies neuropathic pain development and maintenance.

Key words: central sensitization; spinal cord; allodynia; neuropathic pain; nerve injury; calcium channels

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Received July 21, 2004; revised August 17, 2004; accepted August 19, 2004.

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