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The Journal of Neuroscience, August 20, 2008, 28(34):8489-8501; doi:10.1523/JNEUROSCI.2552-08.2008

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Neurobiology of Disease
Differential Implication of Proinflammatory Cytokine Interleukin-6 in the Development of Cephalic versus Extracephalic Neuropathic Pain in Rats

Alban Latrémolière,^1,2 Annie Mauborgne,^1,3 Justine Masson,^1,2 Sylvie Bourgoin,^1,2 Valérie Kayser,^1,2 Michel Hamon,^1,2 and Michel Pohl^1,3

¹Université Pierre et Marie Curie–Paris 6, Faculté de Médecine Pierre et Marie Curie, Site Pitié-Salpêtrière, Institut Fédératif de Recherche 70 des Neurosciences, Unité Mixte de Recherche S677, F-75013 Paris, France, and ²Inserm, Unité 677 and ³Unité 713, F-75013 Paris, France

Correspondence should be addressed to Dr. Alban Latrémolière, Unité Mixte de Recherche 677, Inserm/Université Pierre et Marie Curie, Faculté de Médecine Pierre et Marie Curie, Site Pitié-Salpêtrière, 75634 Paris Cedex 13, France. Email: allodynie{at}hotmail.com

Responses resulting from injury to the trigeminal nerve exhibit differences compared with those caused by lesion of other peripheral nerves. With the aim of elucidating the physiopathological mechanisms underlying cephalic versus extracephalic neuropathic pain, we determined the time course expression of proinflammatory cytokines interleukin-6 (IL-6) and IL-1β, neuronal injury (ATF3), macrophage/microglial (OX-42), and satellite cells/astrocyte (GFAP) markers in central and ganglion tissues in rats that underwent unilateral chronic constriction injury (CCI) to either infraorbital nerve (IoN) (cephalic area) or sciatic nerve (SN) (extracephalic area). Whereas CCI induced microglial activation in both models, we observed a concomitant upregulation of IL-6 and ATF3 in the ipsilateral dorsal horn of the lumbar cord in SN-CCI rats but not in the ipsilateral spinal nucleus of the trigeminal nerve (Sp5c) in IoN-CCI rats. Preemptive treatment with minocycline (daily administration of 20 mg/kg, i.p., for 2 weeks) partially prevented pain behavior and microglial activation in SN-CCI rats but was ineffective in IoN-CCI rats. We show that IL-6 can upregulate OX-42 and ATF3 expression in cultured microglia and neurons from spinal cord, respectively, as well as in the dorsal horn after acute intrathecal administration of the cytokine. We propose that IL-6 could be one of the promoters of the signaling cascade leading to abnormal pain behavior in SN-CCI but not IoN-CCI rats. Our data further support the idea that different pathophysiological mechanisms contribute to the development of cephalic versus extracephalic neuropathic pain.

Key words: neuropathic pain; trigeminal; microglia; minocycline; IL-6; ATF3

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Received June 4, 2008; revised July 2, 2008; accepted July 6, 2008.

Correspondence should be addressed to Dr. Alban Latrémolière, Unité Mixte de Recherche 677, Inserm/Université Pierre et Marie Curie, Faculté de Médecine Pierre et Marie Curie, Site Pitié-Salpêtrière, 75634 Paris Cedex 13, France. Email: allodynie{at}hotmail.com

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