Peripherally Acting μ-Opioid Receptor Agonists Attenuate Ongoing Pain-associated Behavior and Spontaneous Neuronal Activity after Nerve Injury in Rats

Author:

Tiwari Vinod1,Anderson Michael1,Yang Fei1,Tiwari Vineeta1,Zheng Qin1,He Shao-Qiu1,Zhang Tong1,Shu Bin1,Chen Xueming1,Grenald Shaness A.1,Stephens Kimberly E.1,Chen Zhiyong1,Dong Xinzhong1,Raja Srinivasa N.1,Guan Yun1

Affiliation:

1. From the Department of Anesthesiology and Critical Care Medicine (Vinod T., M.A., F.Y., Vineeta T., S.-Q.H., T.Z., B.S., S.A.G., Z.C., S.N.R., Y.G.), the Solomon H. Snyder Department of Neuroscience, Center for Sensory Biology (M.A., Q.Z., X.D.), Department of Pharmacology and Molecular Sciences and the Center for Epigenetics (K.E.S.), and the Howard Hughes Medical Institute (X.D.), Johns Hopkins

Abstract

Abstract Background Ongoing neuropathic pain is difficult to treat. The authors examined whether dermorphin [D-Arg2, Lys4] (1–4) amide, a peripherally acting µ-opioid receptor agonist, attenuates ongoing pain-associated manifestations after nerve injury in rats and mice. Methods Using conditioned place preference assay, the authors tested whether animals show a preference to the environment associated with drug treatment. Wide-dynamic range and dorsal root ganglion neuronal activities were measured by electrophysiology recording and calcium imaging. Results Nerve-injured animals stayed longer in dermorphin [D-Arg2, Lys4] (1–4) amide–paired chamber after conditioning than during preconditioning (rats: 402.4 ± 61.3 vs. 322.1 ± 45.0 s, 10 mg/kg, n = 9, P = 0.009; mice: 437.8 ± 59.4 vs. 351.3 ± 95.9 s, 2 mg/kg, n = 8, P = 0.047). Topical ganglionic application of dermorphin [D-Arg2, Lys4] (1–4) amide (5 μM, 1 μl, n = 5) reduced the numbers of small-diameter dorsal root ganglion neurons that showed spontaneous activity (1.1 ± 0.4 vs. 1.5 ± 0.3, P = 0.044) and that were activated by test stimulation (15.5 ± 5.5 vs. 28.2 ± 8.2, P = 0.009) after injury. In neuropathic rats, dermorphin [D-Arg2, Lys4] (1–4) amide (10 mg/kg, n = 8) decreased spontaneous firing rates in wide-dynamic range neurons to 53.2 ± 46.6% of predrug level, and methylnaltrexone (5 mg/kg, n = 9) blocked dermorphin [D-Arg2, Lys4] (1–4) amide–induced place preference and inhibition of wide-dynamic range neurons. Dermorphin [D-Arg2, Lys4] (1–4) amide increased paw withdrawal threshold (17.5 ± 2.2 g) from baseline (3.5 ± 0.7 g, 10 mg/kg, n = 8, P = 0.002) in nerve-injured rats, but the effect diminished after repeated administrations. Conclusions Peripherally acting μ-opioids may attenuate ongoing pain-related behavior and its neurophysiologic correlates. Yet, repeated administrations cause antiallodynic tolerance.

Publisher

Ovid Technologies (Wolters Kluwer Health)

Subject

Anesthesiology and Pain Medicine

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