A mu–delta opioid receptor brain atlas reveals neuronal co-occurrence in subcortical networks

Arttamangkul S, Quillinan N, Low MJ, von Zastrow M, Pintar J, Williams JT (2008) Differential activation and trafficking of micro-opioid receptors in brain slices. Mol Pharmacol 74(4):972–979 Aston-Jones G, Smith RJ, Moorman DE, Richardson KA (2009) Role of lateral hypothalamic orexin neurons in reward processing and addiction. Neuropharmacology 56(Suppl 1):112–121 Basbaum AI, Bautista DM, Scherrer G, Julius D (2009) Cellular and molecular mechanisms of pain. Cell 139(2):267–284 Befort K, Filliol D, Decaillot FM, Gaveriaux-Ruff C, Hoehe MR, Kieffer BL (2001) A single nucleotide polymorphic mutation in the human mu-opioid receptor severely impairs receptor signaling. J Biol Chem 276(5):3130–3137 Befort K, Filliol D, Ghate A, Darcq E, Matifas A, Muller J et al (2008) Mu-opioid receptor activation induces transcriptional plasticity in the central extended amygdala. Eur J Neurosci 27(11):2973–2984 Bellintani-Guardia B, Schweizer M, Herbert H (1996) Analysis of projections from the cochlear nucleus to the lateral paragigantocellular reticular nucleus in the rat. Cell Tissue Res 283(3):493–505 Berger AC, Whistler JL (2011) Morphine-induced mu opioid receptor trafficking enhances reward yet prevents compulsive drug use. EMBO Mol Med 3:385–397 Berrendero F, Castane A, Ledent C, Parmentier M, Maldonado R, Valverde O (2003) Increase of morphine withdrawal in mice lacking A2a receptors and no changes in CB1/A2a double knockout mice. Eur J Neurosci 17(2):315–324 Borgland SL, Connor M, Osborne PB, Furness JB, Christie MJ (2003) Opioid agonists have different efficacy profiles for G protein activation, rapid desensitization, and endocytosis of mu-opioid receptors. J Biol Chem 278(21):18776–18784 Cahill CM, McClellan KA, Morinville A, Hoffert C, Hubatsch D, O’Donnell D, Beaudet A (2001) Immunohistochemical distribution of delta opioid receptors in the rat central nervous system: evidence for somatodendritic labeling and antigen-specific cellular compartmentalization. J Comp Neurol 440(1):65–84 Cahill CM, Holdridge SV, Morinville A (2007) Trafficking of delta-opioid receptors and other G-protein-coupled receptors: implications for pain and analgesia. Trends Pharmacol Sci 28(1):23–31 Contet C, Filliol D, Matifas A, Kieffer BL (2008) Morphine-induced analgesic tolerance, locomotor sensitization and physical dependence do not require modification of mu opioid receptor, cdk5 and adenylate cyclase activity. Neuropharmacology 54(3):475–486 De Luca LA Jr, Vendramini RC, Pereira DT, Colombari DA, David RB, de Paula PM, Menani JV (2007) Water deprivation and the double- depletion hypothesis: common neural mechanisms underlie thirst and salt appetite. Braz J Med Biol Res 40(5):707–712 Dong HW, Swanson LW (2003) Projections from the rhomboid nucleus of the bed nuclei of the stria terminalis: implications for cerebral hemisphere regulation of ingestive behaviors. J Comp Neurol 463(4):434–472 Duncan K, Ketz N, Inati SJ, Davachi L (2012) Evidence for area CA1 as a match/mismatch detector: a high-resolution fMRI study of the human hippocampus. Hippocampus 22(3):389–398 Erbs E, Faget L, Scherrer G, Kessler P, Hentsch D, Vonesch JL, Matifas A, Kieffer BL, Massotte D (2012) Distribution of delta opioid receptor-expressing neurons in the mouse hippocampus. Neuroscience 221:203–213 Faget L, Erbs E, Le Merrer J, Scherrer G, Matifas A, Benturquia N, Noble F, Decossas M, Koch M, Kessler P, Vonesch JL, Schwab Y, Kieffer BL, Massotte D (2012) In vivo visualization of delta opioid receptors upon physiological activation uncovers a distinct internalization profile. J Neurosci 32(21):7301–7310 Feng Y, He X, Yang Y, Chao D, Lazarus LH, Xia Y (2012) Current research on opioid receptor function. Curr Drug Targets 13(2):230–246 Filizola M, Devi LA (2013) Grand opening of structure-guided design for novel opioids. Trends Pharmacol Sci 34(1):6–12 George SR, Zastawny RL, Briones-Urbina R, Cheng R, Nguyen T, Heiber M, Kouvelas A, Chan AS, O’Dowd BF (1994) Distinct distributions of mu, delta and kappa opioid receptor mRNA in rat brain. Biochem Biophys Res Commun 205(2):1438–1444 George SR, Fan T, Xie Z, Tse R, Tam V, Varghese G, O’Dowd BF (2000) Oligomerization of mu- and delta-opioid receptors. Generation of novel functional properties. J Biol Chem 275(34):26128–26135 Gomes I, Gupta A, Filipovska J, Szeto HH, Pintar JE, Devi LA (2004) A role for heterodimerization of mu and delta opiate receptors in enhancing morphine analgesia. Proc Natl Acad Sci USA 101(14):5135–5139 Gomes I, Fujita W, Gupta A, Saldanha AS, Negri A, Pinello CE, Roberts E, Filizola M, Hodder P, Devi LA (2013) Identification of a mu-delta opioid receptor heteromer-biased agonist with antinociceptive activity. Proc Natl Acad Sci USA 110(29):12072–12077 Goody RJ, Oakley SM, Filliol D, Kieffer BL, Kitchen I (2002) Quantitative autoradiographic mapping of opioid receptors in the brain of delta-opioid receptor gene knockout mice. Brain Res 945(1):9–19 Goto M, Swanson LW (2004) Axonal projections from the parasubthalamic nucleus. J Comp Neurol 469(4):581–607 Gray AC, Coupar IM, White PJ (2006) Comparison of opioid receptor distributions in the rat central nervous system. Life Sci 79(7):674–685 Gupta A, Mulder J, Gomes I, Rozenfeld R, Bushlin I, Ong E, Lim M, Maillet E, Junek M, Cahill CM, Harkany T, Devi LA (2010) ncreased abundance of opioid receptor heteromers after chronic morphine administration. Sci Signal 3(131):ra54 Haberstock-Debic H, Kim KA, Yu YJ, von Zastrow M (2005) Morphine promotes rapid, arrestin-dependent endocytosis of mu-opioid receptors in striatal neurons. J Neurosci 25(34):7847–7857 Hamson DK, Watson NV (2004) Regional brainstem expression of Fos associated with sexual behavior in male rats. Brain Res 1006(2):233–240 Harris GC, Aston-Jones G (2006) Arousal and reward: a dichotomy in orexin function. Trends Neurosci 29(10):571–577 Hayes DJ, Northoff G (2011) Identifying a network of brain regions involved in aversion-related processing: a cross-species translational investigation. Front Integr Neurosci 5:49 Hayes DJ, Northoff G (2012) Common brain activations for painful and non-painful aversive stimuli. BMC Neurosci 13:60 Jordan BA, Devi LA (1999) G-protein-coupled receptor heterodimerization modulates receptor function. Nature 399:697–700 King BM, Cook JT, Rossiter KN, Rollins BL (2003) Obesity-inducing amygdala lesions: examination of anterograde degeneration and retrograde transport. Am J Physiol Regul Integr Comp Physiol 284(4):R965–R982 Kitchen I, Slowe SJ, Matthes HW, Kieffer B (1997) Quantitative autoradiographic mapping of mu-, delta- and kappa-opioid receptors in knockout mice lacking the mu-opioid receptor gene. Brain Res 778(1):73–88 Kivell BM, Day DJ, McDonald FJ, Miller JH (2004) Mu and delta opioid receptor immunoreactivity and mu receptor regulation in brainstem cells cultured from late fetal and early postnatal rats. Brain Res Dev Brain Res 149(1):9–19 Komisaruk BR, Whipple B (2005) Functional MRI of the brain during orgasm in women. Annu Rev Sex Res 16:62–86 Le Merrer J, Becker JA, Befort K, Kieffer BL (2009) Reward processing by the opioid system in the brain. Physiol Rev 89(4):1379–1412 Lesscher HM, Bailey A, Burbach JP, Van Ree JM, Kitchen I, Gerrits MA (2003) Receptor-selective changes in mu-, delta- and kappa-opioid receptors after chronic naltrexone treatment in mice. Eur J Neurosci 17(5):1006–1012 Lutz PE, Kieffer BL (2012) Opioid receptors: distinct roles in mood disorders. Trends Neurosci 36:195–206 Mansour A, Khachaturian H, Lewis ME, Akil H, Watson SJ (1987) Autoradiographic differentiation of mu, delta, and kappa opioid receptors in the rat forebrain and midbrain. J Neurosci 7(8):2445–2464 Mansour A, Fox CA, Akil H, Watson SJ (1995) Opioid-receptor mRNA expression in the rat CNS: anatomical and functional implications. Trends Neurosci 18:22–29 Mascaro MB, Prosdocimi FC, Bittencourt JC, Elias CF (2009) Forebrain projections to brainstem nuclei involved in the control of mandibular movements in rats. Eur J Oral Sci 117(6):676–684 Massotte D (2006) Characterization of monoclonal antibodies directed against the N-terminus of human mu and delta opioid receptors. Bulletin de la Société Royale des Sciences de Liège 75:1–19 Pedersen NP, Vaughan CW, Christie MJ (2011) Opioid receptor modulation of GABAergic and serotonergic spinally projecting neurons of the rostral ventromedial medulla in mice. J Neurophysiol 106(2):731–740 Poole DP, Pelayo JC, Scherrer G, Evans CJ, Kieffer BL, Bunnett NW (2011) Localization and regulation of fluorescently labeled delta opioid receptor, expressed in enteric neurons of mice. Gastroenterology 141(3):982–991 e981–e988 Pradhan AA, Clarke PB (2005) Comparison between delta-opioid receptor functional response and autoradiographic labeling in rat brain and spinal cord. J Comp Neurol 481(4):416–426 Pradhan AA, Becker JA, Scherrer G, Tryoen-Toth P, Filliol D, Matifas A, Massotte D, Gaveriaux-Ruff C, Kieffer BL (2009) In vivo delta opioid receptor internalization controls behavioral effects of agonists. PLoS One 4(5):e5425 Pradhan AA, Befort K, Nozaki C, Gaveriaux-Ruff C, Kieffer BL (2011) The delta opioid receptor: an evolving target for the treatment of brain disorders. Trends Pharmacol Sci 32(10):581–590 Rau KK, Caudle RM, Cooper BY, Johnson RD (2005) Diverse immunocytochemical expression of opioid receptors in electrophysiologically defined cells of rat dorsal root ganglia. J Chem Neuroanat 29(4):255–264 Reis LC (2007) Role of the serotoninergic system in the sodium appetite control. An Acad Bras Cienc 79(2):261–283 Rodriguez-Munoz M, de la Torre-Madrid E, Sanchez-Blazquez P, Garzon J (2007) Morphine induces endocytosis of neuronal mu-opioid receptors through the sustained transfer of Galpha subunits to RGSZ2 proteins. Mol Pain 3:19 Rozenfeld R, Devi LA (2011) Exploring a role for heteromerization in GPCR signalling specificity. Biochem J 433(1):11–18 Scherrer G, Tryoen-Toth P, Filliol D, Matifas A, Laustriat D, Cao YQ, Basbaum AI, Dierich A, Vonesh JL, Gaveriaux-Ruff C, Kieffer BL (2006) Knockin mice expressing fluorescent delta-opioid receptors uncover G protein-coupled receptor dynamics in vivo. Proc Natl Acad Sci USA 103(25):9691–9696 Scherrer G, Imamachi N, Cao YQ, Contet C, Mennicken F, O’Donnell D, Kieffer BL, Basbaum AI (2009) Dissociation of the opioid receptor mechanisms that control mechanical and heat pain. Cell 137(6):1148–1159 Shin JW, Geerling JC, Stein MK, Miller RL, Loewy AD (2011) FoxP2 brainstem neurons project to sodium appetite regulatory sites. J Chem Neuroanat 42(1):1–23 Slowe SJ, Simonin F, Kieffer B, Kitchen I (1999) Quantitative autoradiography of mu-, delta- and kappa1 opioid receptors in kappa-opioid receptor knockout mice. Brain Res 818(2):335–345 Stevens CW (2009) The evolution of vertebrate opioid receptors. Front Biosci 14:1247–1269 Sturnieks DL, St George R, Lord SR (2008) Balance disorders in the elderly. Neurophysiol Clin 38(6):467–478 Tempel A, Zukin RS (1987) Neuroanatomical patterns of the mu, delta, and kappa opioid receptors of rat brain as determined by quantitative in vitro autoradiography. Proc Natl Acad Sci USA 84(12):4308–4312 Trafton JA, Abbadie C, Marek K, Basbaum AI (2000) Postsynaptic signaling via the [mu]-opioid receptor: responses of dorsal horn neurons to exogenous opioids and noxious stimulation. J Neurosci 20(23):8578–8584 van Rijn RM, Whistler JL (2009) The delta(1) opioid receptor is a heterodimer that opposes the actions of the delta(2) receptor on alcohol intake. Biol Psychiatry 66(8):777–784 Wang HB, Zhao B, Zhong YQ, Li KC, Li ZY, Wang Q, Lu YJ, Zhang ZN, He SQ, Zheng HC, Wu SX, Hokfelt TG, Bao L, Zhang X (2010) Coexpression of delta- and mu-opioid receptors in nociceptive sensory neurons. Proc Natl Acad Sci USA 107(29):13117–13122 Williams JT, Christie MJ, Manzoni O (2001) Cellular and synaptic adaptations mediating opioid dependence. Physiol Rev 81(1):299–343 Wilson DA, Sullivan RM (2011) Cortical processing of odor objects. Neuron 72(4):506–519