Peripheral G protein-coupled inwardly rectifying potassium channels are involved in δopioid receptor-mediated anti-hyperalgesia in rat masseter muscle

European Journal of Pain (United Kingdom)

Volumn 18, Issue 1, 2014, Pages 29-38

  Chung, M K ^a   Cho, Y S ^b   Bae, Y C ^b   Lee, J ^a   Zhang, X ^a,c   Ro, J Y ^a  

^a UNIVERSITY OF MARYLAND DENTAL SCHOOL   (United States)

^b Kyungpook National University   (South Korea)

^c CHINA MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; CAPSAICIN; DELTA OPIATE RECEPTOR; DELTA OPIATE RECEPTOR AGONIST; ENKEPHALIN[2,5 DEXTRO PENICILLAMINE]; EPITOPE; G PROTEIN COUPLED INWARDLY RECTIFYING POTASSIUM CHANNEL; PROTEIN FOS; RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINOCICEPTION; ARTICLE; BEHAVIOR; BRAIN STEM; CONTROLLED STUDY; HYPERALGESIA; MALE; MASSETER MUSCLE; MYOSITIS; NOCICEPTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANALGESICS, OPIOID; ANIMALS; BEHAVIOR, ANIMAL; BLOTTING, WESTERN; BRAIN STEM; CAPSAICIN; ENKEPHALIN, D-PENICILLAMINE (2,5)-; G PROTEIN-COUPLED INWARDLY-RECTIFYING POTASSIUM CHANNELS; GENES, FOS; HYPERALGESIA; IMMUNOHISTOCHEMISTRY; MALE; MASSETER MUSCLE; PHYSICAL STIMULATION; RATS; RATS, SPRAGUE-DAWLEY; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, OPIOID, DELTA; RNA, MESSENGER; SENSORY SYSTEM AGENTS; TRIGEMINAL GANGLION;

EID: 84893327152     PISSN: 10903801     EISSN: 15322149     Source Type: Journal    
DOI: 10.1002/j.1532-2149.2013.00343.x     Document Type: Article

References (54)

1. Akins, P.T., McCleskey, E.W. (1993). Characterization of potassium currents in adult rat sensory neurons and modulation by opioids and cyclic AMP. Neuroscience 56, 759-769.
2. Alvarez, P., Chen, X., Bogen, O., Green, P.G., Levine, J.D. (2012a). IB4(+) nociceptors mediate persistent muscle pain induced by GDNF. J Neuro-physiol 108, 2545-2553.
3. Alvarez, P., Gear, R.W., Green, P.G., Levine, J.D. (2012b). IB4-saporin attenuates acute and eliminates chronic muscle pain in the rat. Exp Neurol 233, 859-865.
4. Ambalavanar, R., Morris, R. (1992). The distribution of binding by iso-lectin I-B4 from Griffonia simplicifolia in the trigeminal ganglion and brainstem trigeminal nuclei in the rat. Neuroscience 47, 421-429.
5. Auh, Q.S., Ro, J.Y. (2012). Effects of peripheral kappa opioid receptor activation on inflammatory mechanical hyperalgesia in male and female rats. Neurosci Lett 524, 111-115.
6. Blednov, Y.A., Stoffel, M., Alva, H., Harris, R.A. (2003). A pervasive mechanism for analgesia: Activation of GIRK2 channels. Proc Natl Acad Sci U S A 100, 277-282.
7. Cavanaugh, D.J., Lee, H., Lo, L., Shields, S.D., Zylka, M.J., Basbaum, A.I., Anderson, D.J. (2009). Distinct subsets of unmyelinated primary sensory fibers mediate behavioral responses to noxious thermal and mechanical stimuli. Proc Natl Acad Sci U S A 106, 9075-9080.
8. Dionne, R.A., Lepinski, A.M., Gordon, S.M., Jaber, L., Brahim, J.S., Hargreaves, K.M. (2001). Analgesic effects of peripherally administered opioids in clinical models of acute and chronic inflammation. Clin Pharmacol Ther 70, 66-73.
9. Duckett, J.W., Cangiano, T., Cubina, M., Howe, C., Cohen, D. (1997). Intravesical morphine analgesia after bladder surgery. J Urol 157, 1407-1409.
10. Eisenach, J.C., Carpenter, R., Curry, R. (2003). Analgesia from a peripherally active kappa-opioid receptor agonist in patients with chronic pancreatitis. Pain 101, 89-95.
11. Gao, X.F., Zhang, H.L., You, Z.D., Lu, C.L., He, C. (2007). G proteincoupled inwardly rectifying potassium channels in dorsal root ganglion neurons. Acta Pharmacol Sin 28, 185-190.
12. Garlicki, J., Dorazil-Dudzik, M., Wordliczek, J., Przewlocka, B. (2006). Effect of intraarticular tramadol administration in the rat model of knee joint inflammation. Pharmacol Rep 58, 672-679.
13. Guan, Y., Johanek, L.M., Hartke, T.V., Shim, B., Tao, Y.X., Ringkamp, M., Meyer, R.A., Raja, S.N. (2008). Peripherally acting mu-opioid receptor agonist attenuates neuropathic pain in rats after L5 spinal nerve injury. Pain 138, 318-329.
14. Hendrich, J., Alvarez, P., Chen, X., Levine, J.D. (2012). GDNF induces mechanical hyperalgesia in muscle by reducing I(BK) in isolectin B4-positive nociceptors. Neuroscience 219, 204-213.
15. Hwang, S.J., Oh, J.M., Valtschanoff, J.G. (2005). The majority of bladder sensory afferents to the rat lumbosacral spinal cord are both IB4-and CGRP-positive. Brain Res 1062, 86-91.
16. Ikeda, K., Kobayashi, T., Kumanishi, T., Yano, R., Sora, I., Niki, H. (2002). Molecular mechanisms of analgesia induced by opioids and ethanol: Is the GIRK channel one of the keys? Neurosci Res 44, 121-131.
17. Jelacic, T.M., Kennedy, M.E., Wickman, K., Clapham, D.E. (2000). Functional and biochemical evidence for G-protein-gated inwardly rectifying K+ (GIRK) channels composed of GIRK2 and GIRK3. J Biol Chem 275, 36211-36216.
18. Kanjhan, R. (1995). Opioids and pain. Clin Exp Pharmacol Physiol 22, 397-403.
19. Kashiba, H., Uchida, Y., Senba, E. (2001). Difference in binding by isolec-tin B4 to trkA and c-ret mRNA-expressing neurons in rat sensory ganglia. Brain Res Mol Brain Res 95, 18-26.
20. Kawano, T., Zhao, P., Nakajima, S., Nakajima, Y. (2004). Single-cell RT-PCR analysis of GIRK channels expressed in rat locus coeruleus and nucleus basalis neurons. Neurosci Lett 18(358), 63-67.
21. Keskinbora, K., Aydinli, I. (2009). Perineural morphine in patients with chronic ischemic lower extremity pain: Efficacy and long-term results. J Anesth 23, 11-18.
22. Khodorova, A., Navarro, B., Jouaville, L.S., Murphy, J.E., Rice, F.L., Mazurkiewicz, J.E., Long-Woodward, D., Stoffel, M., Strichartz, G.R., Yukhananov, R., Davar, G. (2003). Endothelin-B receptor activation triggers an endogenous analgesic cascade at sites of peripheral injury. Nat Med 9, 1055-1061.
23. Kim, Y.S., Paik, S.K., Cho, Y.S., Shin, H.S., Bae, J.Y., Moritani, M., Yoshida, A., Ahn, D.K., Valtschanoff, J., Hwang, S.J., Moon, C., Bae, Y.C. (2008). Expression of P2X3 receptor in the trigeminal sensory nuclei of the rat. J Comp Neurol 506, 627-639.
24. Kim, Y.S., Son, J.Y., Kim, T.H., Paik, S.K., Dai, Y., Noguchi, K., Ahn, D.K., Bae, Y.C. (2010). Expression of transient receptor potential ankyrin 1 (TRPA1) in the rat trigeminal sensory afferents and spinal dorsal horn. J Comp Neurol 518, 687-698.
25. Lee, J., Saloman, J.L., Weiland, G., Auh, Q.S., Chung, M.K., Ro, J.Y. (2012). Functional interactions between NMDA receptors and TRPV1 in trigeminal sensory neurons mediate mechanical hyperalgesia in the rat masseter muscle. Pain 153, 1514-1524.
26. Likar, R., Koppert, W., Blatnig, H., Chiari, F., Sittl, R., Stein, C., Schafer, M. (2001). Efficacy of peripheral morphine analgesia in inflamed, non-inflamed and perineural tissue of dental surgery patients. J Pain Symptom Manage 21, 330-337.
27. Lima, F.O., Souza, G.R., Verri, W.A., Jr, Parada, C.A., Ferreira, S.H., Cunha, F.Q., Cunha, T.M. (2010). Direct blockade of inflammatory hypernociception by peripheral A1 adenosine receptors: Involvement of the NO/cGMP/PKG/KATP signaling pathway. Pain 151, 506-515.
28. Luscher, C., Slesinger, P.A. (2010). Emerging roles for G protein-gated inwardly rectifying potassium (GIRK) channels in health and disease. Nat Rev Neurosci 11, 301-315.
29. Marker, C.L., Lujan, R., Colon, J., Wickman, K. (2006). Distinct populations of spinal cord lamina II interneurons expressing G-protein-gated potassium channels. J Neurosci 26, 12251-12259.
30. Marker, C.L., Lujan, R., Loh, H.H., Wickman, K. (2005). Spinal G-protein-gated potassium channels contribute in a dose-dependent manner to the analgesic effect of mu-and delta-but not kappa-opioids. J Neurosci 25, 3551-3559.
31. Marker, C.L., Stoffel, M., Wickman, K. (2004). Spinal G-protein-gated K+ channels formed by GIRK1 and GIRK2 subunits modulate thermal nociception and contribute to morphine analgesia. J Neurosci 24, 2806-2812.
32. Mitrovic, I., Margeta-Mitrovic, M., Bader, S., Stoffel, M., Jan, L.Y., Basbaum, A.I. (2003). Contribution of GIRK2-mediated postsynaptic signaling to opiate and alpha 2-adrenergic analgesia and analgesic sex differences. Proc Natl Acad Sci U S A 100, 271-276.
33. Niu, K., Saloman, J.L., Zhang, Y., Ro, J.Y. (2011). Sex differences in the contribution of ATP-sensitive K+ channels in trigeminal ganglia under an acute muscle pain condition. Neuroscience 180, 344-352.
34. Nunez, S., Lee, J.S., Zhang, Y., Bai, G., Ro, J.Y. (2007). Role of peripheral mu-opioid receptors in inflammatory orofacial muscle pain. Neuroscience 146, 1346-1354.
35. Obara, I., Parkitna, J.R., Korostynski, M., Makuch, W., Kaminska, D., Przewlocka, B., Przewlocki, R. (2009). Local peripheral opioid effects and expression of opioid genes in the spinal cord and dorsal root ganglia in neuropathic and inflammatory pain. Pain 141, 283-291.
36. Ocaña, M., Cendan, C.M., Cobos, E.J., Entrena, J.M., Baeyens, J.M. (2004). Potassium channels and pain: Present realities and future opportunities. Eur J Pharmacol 500, 203-219.
37. Ortiz, M.I., Castro-Olguin, J., Pena-Samaniego, N., Castaneda-Hernandez, G. (2005). Probable activation of the opioid receptor-nitric oxide-cyclic GMP-K+ channels pathway by codeine. Pharmacol Biochem Behav 82, 695-703.
38. Pacheco, D.F., Duarte, I.D. (2005). Delta-opioid receptor agonist SNC80 induces peripheral antinociception via activation of ATP-sensitive K+ channels. Eur J Pharmacol 512, 23-28.
39. Paxinos, G., Watson, C. (2007). The Rat Brain in Stereotaxic Coordinates, 3rd edn (Waltham, MA: Academic Press).
40. Price, T.J., Flores, C.M. (2007). Critical evaluation of the colocalization between calcitonin gene-related peptide, substance P, transient receptor potential vanilloid subfamily type 1 immunoreactivities, and isolectin B4 binding in primary afferent neurons of the rat and mouse. J Pain 8, 263-272.
41. Ro, J.Y., Lee, J.S., Zhang, Y. (2009). Activation of TRPV1 and TRPA1 leads to muscle nociception and mechanical hyperalgesia. Pain 144, 270-277.
42. Rodrigues, A.R., Duarte, I.D. (2000). The peripheral antinociceptive effect induced by morphine is associated with ATP-sensitive K(+) channels. Br J Pharmacol 129, 110-114.
43. Romero, T.R., Duarte, I.D. (2009). Involvement of ATP-sensitive K(+) channels in the peripheral antinociceptive effect induced by the alpha(2)-adrenoceptor agonist xylazine. J Pharmacol Sci 111, 323-327.
44. Rorarius, M., Suominen, P., Baer, G., Pajunen, P., Tuimala, R., Laippala, P. (1999). Peripherally administered sufentanil inhibits pain perception after postpartum tubal ligation. Pain 79, 83-88.
45. Ruscheweyh, R., Forsthuber, L., Schoffnegger, D., Sandkühler, J. (2007). Modification of classical neurochemical markers in identified primary afferent neurons with Abeta-, Adelta-, and C-fibers after chronic constriction injury in mice. J Comp Neurol 502, 325-336.
46. Sachs, D., Cunha, F.Q., Ferreira, S.H. (2004). Peripheral analgesic blockade of hypernociception: Activation of arginine/NO/cGMP/protein kinase G/ATP-sensitive K+ channel pathway. Proc Natl Acad Sci U S A 101, 3680-3685.
47. Sadja, R., Alagem, N., Reuveny, E. (2003). Gating of GIRK channels: Details of an intricate, membrane-delimited signaling complex. Neuron 39, 9-12.
48. Saloman, J.L., Niu, K.Y., Ro, J.Y. (2011). Activation of peripheral delta-opioid receptors leads to anti-hyperalgesic responses in the masseter muscle of male and female rats. Neuroscience 190, 379-385.
49. Scherrer, G., Imamachi, N., Cao, Y.Q., Contet, C., Mennicken, F., O'Donnell, D., Kieffer, B.L., Basbaum, A.I. (2009). Dissociation of the opioid receptor mechanisms that control mechanical and heat pain. Cell 137, 1148-1159.
50. Stein, C., Schafer, M., Machelska, H. (2003). Attacking pain at its source: New perspectives on opioids. Nat Med 9, 1003-1008.
51. Wang, H.B., Zhao, B., Zhong, Y.Q., Li, K.C., Li, Z.Y., Wang, Q., Lu, Y.J., Zhang, Z.N., He, S.Q., Zheng, H.C., Wu, S.X., Hokfelt, T.G., Bao, L., Zhang, X. (2010). Coexpression of delta-and mu-opioid receptors in nociceptive sensory neurons. Proc Natl Acad Sci U S A 107, 13117-13122.
52. Yang, D., Zhang, X., Hughes, B.A. (2008). Expression of inwardly rectifying potassium channel subunits in native human retinal pigment epithelium. Exp Eye Res 87, 176-183.
53. Zhang, X., Bao, L. (2012). Interaction and regulatory functions of mu-and delta-opioid receptors in nociceptive afferent neurons. Neurosci Bull 28, 121-130.
54. Zoga, V., Kawano, T., Liang, M.Y., Bienengraeber, M., Weihrauch, D., McCallum, B., Gemes, G., Hogan, Q., Sarantopoulos, C. (2010). KATP channel subunits in rat dorsal root ganglia: Alterations by painful axotomy. Mol Pain 6, 6.