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The Journal of Neuroscience, August 18, 2004, 24(33):7344-7352; doi:10.1523/JNEUROSCI.1676-04.2004

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Cellular/Molecular
µ-Opioid Receptor Trafficking on Inhibitory Synapses in the Rat Brainstem

Kirsteen N. Browning,¹ Alexander E. Kalyuzhny,³ and R. Alberto Travagli^1,2

Departments of ¹Internal Medicine-Gastroenterology and ²Physiology, University of Michigan Medical Center, Ann Arbor, Michigan 48109, and ³Department of Neuroscience, University of Minnesota, Minneapolis, Minnesota 55455

Whole-cell recordings were made from identified gastric-projecting rat dorsal motor nucleus of the vagus (DMV) neurons. The amplitude of evoked IPSCs (eIPSCs) was unaffected by perfusion with met-enkephalin (ME) or by µ-, -, or -opioid receptor selective agonists, namely D-Ala²-N-Me-Phe⁴-Glycol⁵-enkephalin (DAMGO), cyclic [D-Pen²-D-Pen⁵]-enkephalin, or trans-3,4-dichloro-N-methyl-N-[2-(1-pyrolytinil)-cyclohexyl]-benzeneacetamide methane sulfonate (U50,488), respectively. Brief incubation with the adenylate cyclase activator forskolin or the nonhydrolysable cAMP analog 8-bromo-cAMP, thyrotropin releasing hormone, or cholecystokinin revealed the ability of ME and DAMGO to inhibit IPSC amplitude; this inhibition was prevented by pretreatment with the µ-opioid receptor (MOR1) selective antagonist D-Phe-Cys-Tyr-D-Trp-Orn-Thr-Pen-Thr-NH₂. Conversely, incubation with the adenylate cyclase inhibitor dideoxyadenosine, with the protein kinase A (PKA) inhibitor N-[2-(p-Bromocinnamyl-amino)ethyl]-5-isoquinolinesulfonamide dihydrochloride (H89), or with the Golgi-disturbing agent brefeldin A, blocked the ability of forskolin to facilitate the inhibitory actions of ME. Immunocytochemical experiments revealed that under control conditions, MOR1 immunoreactivity (MOR1-IR) was colocalized with glutamic acid decarboxylase (GAD)-IR in profiles apposing DMV neurons only after stimulation of the cAMP-PKA pathway. Pretreatment with H89 or brefeldin A or incubation at 4°C prevented the forskolin-mediated insertion of MOR1 on GAD-IR-positive profiles.

These results suggest that the cAMP-PKA pathway regulates trafficking of µ-opioid receptors into the cell surface of GABAergic nerve terminals. By consequence, the inhibitory actions of opioid peptides in the dorsal vagal complex may depend on the state of activation of brainstem vagal circuits.

Key words: autonomic; brainstem; gastrointestinal; opioid; vagus

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Received May 3, 2004; revised July 6, 2004; accepted July 8, 2004.

This article has been cited by other articles:

				G. M. Holmes, K. N. Browning, M. Tong, E. Qualls-Creekmore, and R. A. Travagli Vagally mediated effects of glucagon-like peptide 1: in vitro and in vivo gastric actions J. Physiol., October 1, 2009; 587(19): 4749 - 4759. [Abstract] [Full Text] [PDF]

				J. Nasse, D. Terman, S. Venugopal, G. Hermann, R. Rogers, and J. B. Travers Local circuit input to the medullary reticular formation from the rostral nucleus of the solitary tract Am J Physiol Regulatory Integrative Comp Physiol, November 1, 2008; 295(5): R1391 - R1408. [Abstract] [Full Text] [PDF]

				S. L. Poole, J. Deuchars, D. I. Lewis, and S. A. Deuchars Subdivision-Specific Responses of Neurons in the Nucleus of the Tractus Solitarius to Activation of Mu-Opioid Receptors in the Rat J Neurophysiol, November 1, 2007; 98(5): 3060 - 3071. [Abstract] [Full Text] [PDF]

				N. R. Glatzer, A. V. Derbenev, B. W. Banfield, and B. N. Smith Endomorphin-1 Modulates Intrinsic Inhibition in the Dorsal Vagal Complex J Neurophysiol, September 1, 2007; 98(3): 1591 - 1599. [Abstract] [Full Text] [PDF]

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				A. V. Derbenev, M. J. Monroe, N. R. Glatzer, and B. N. Smith Vanilloid-mediated heterosynaptic facilitation of inhibitory synaptic input to neurons of the rat dorsal motor nucleus of the vagus. J. Neurosci., September 20, 2006; 26(38): 9666 - 9672. [Abstract] [Full Text] [PDF]

				J. Ma, Y. Zhang, A. E. Kalyuzhny, and Z. Z. Pan Emergence of Functional {delta}-Opioid Receptors Induced by Long-Term Treatment with Morphine Mol. Pharmacol., April 1, 2006; 69(4): 1137 - 1145. [Abstract] [Full Text] [PDF]

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