Dopamine D1 receptors have subcellular distributions conducive to interactions with prodynorphin in the rat nucleus accumbens shell

Synapse

Volumn 60, Issue 1, 2006, Pages 1-19

  Hara, Yuko ^a   Yakovleva, Tatiana ^b   Bakalkin, Georgy ^b   Pickel, Virginia M ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Dense core vesicle; Immunocytochemistry; Neuropeptide; Ultrastructure

Indexed keywords

COMPLEMENTARY DNA; DOPAMINE; DOPAMINE 1 RECEPTOR; NEUROPEPTIDE; PRODYNORPHIN; TYROSINE 3 MONOOXYGENASE;

ANIMAL TISSUE; ARTICLE; CELL ULTRASTRUCTURE; CELLULAR DISTRIBUTION; DENDRITE; DENDRITIC SPINE; DOPAMINE RELEASE; DOPAMINERGIC SYSTEM; ELECTRON MICROSCOPY; HELA CELL; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; RAT; WESTERN BLOTTING;

ANIMALS; AXONS; BLOTTING, WESTERN; DENDRITES; DYNORPHINS; ENKEPHALINS; IMMUNOHISTOCHEMISTRY; MALE; MICROSCOPY, ELECTRON, TRANSMISSION; NUCLEUS ACCUMBENS; PROTEIN PRECURSORS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, DOPAMINE D1; TRANSFECTION;

EID: 33646684949     PISSN: 08874476     EISSN: 10982396     Source Type: Journal    
DOI: 10.1002/syn.20273     Document Type: Article

References (72)

1. Bakalkin G, Ponomariev D, Sarkisyan RA, Terenius L. 1991. Sequence similarity between opioid peptide precursors and DNA-binding proteins. FEBS Lett 282:175-177.
2. Bals-Kubik R, Ableitner A, Herz A, Shippenberg TS. 1993. Neuroanatomical sites mediating the motivational effects of opioids as mapped by the conditioned place preference paradigm in rats. J Pharmacol Exp Ther 264:489-495.
3. Bottger A, Spruce BA. 1995. Proenkephalin is a nuclear protein responsive to growth arrest and differentiation signals. J Cell Biol 130:1251-1262
4. Chang HT, Kitai ST. 1985. Projection neurons of the nucleus accumbens: an intracellular labeling study. Brain Res 347:112-116.
5. Charara A, Grace AA. 2003. Dopamine receptor subtypes selectively modulate excitatory afferents from the hippocampus and amygdala to rat nucleus accumbens neurons. Neuropsychopharmacology 28:1412-1421.
6. Collins SL, D'Addario C, Izenwasser S. 2001. Effects of kappa-opioid receptor agonists on long-term cocaine use and dopamine neurotransmission. Eur J Pharmacol 426:25-34.
7. Colonnier M. 1968. Synaptic patterns on different cell types in the different laminae of the cat visual cortex. An electron microscope study. Brain Res 9:268-287.
8. Curran EJ, Watson SJ, Jr. 1995. Dopamine receptor mRNA expression patterns by opioid peptide cells in the nucleus accumbens of the rat: a double in situ hybridization study. J Comp Neurol 361: 57-76.
9. Day R, Lazure C, Basak A, Boudreault A, Limperis P, Dong W, Lindberg I. 1998. Prodynorphin processing by proprotein convertase 2. Cleavage at single basic residues and enhanced processing in the presence of carboxypeptidase activity. J Biol Chem 273: 829-836.
10. Delle Donne KT, Sesack SR, Pickel VM. 1997. Ultrastructural immunocytochemical localization of the dopamine D2 receptor within GABAergic neurons of the rat striatum. Brain Res 746: 239-255.
11. Deutch AY, Cameron DS. 1992. Pharmacological characterization of dopamine systems in the nucleus accumbens core and shell. Neuroscience 46:49-56.
12. Difiglia M, Pasik T, Pasik P. 1980. Ultrastructure of Golgi-impregnated and gold-toned spiny and aspiny neurons in the monkey neostriatum. J Neurocytol 9:471-492.
13. Drake CT, Terman GW, Simmons ML, Milner TA, Kunkel DD, Schwartzkroin PA, Chavkin C. 1994. Dynorphin opioids present in dentate granule cells may function as retrograde inhibitory neurotransmitters. J Neurosci 14:3736-3750.
14. Dupuy A, Lindberg I, Zhou Y, Akil H, Lazure C, Chretien M, Seidah NG, Day R. 1994. Processing of prodynorphin by the prohormone convertage PC1 results in high molecular weight intermediate forms. Cleavage at a single arginine residue. FEBS Lett 337:60-65.
15. Fagergren P, Smith HR, Daunais JB, Nader MA, Porrino LJ, Hurd YL. 2003. Temporal upregulation of prodynorphin mRNA in the primate striatum after cocaine self-administration. Eur J Neurosci 17:2212-2218.
16. Fallon JH, Leslie FM. 1986. Distribution of dynorphin and enkephalin peptides in the rat brain. J Comp Neurol 249:293-336.
17. Funada M, Suzuki T, Narita M, Misawa M, Nagase H. 1993. Blockade of morphine reward through the activation of kappa-opioid receptors in mice. Neuropharmacology 32:1315-1323.
18. Furuta T, Zhou L, Kaneko T. 2002. Preprodynorphin-, preproenkephalin-, preprotachykinin A- and preprotachykinin B-immunoreactive neurons in the accumbens nucleus and olfactory tubercle: double-immunofluorescence analysis. Neuroscience 114:611-627.
19. Gainer H, Same Y, Brownstein MJ. 1977. Biosynthesis and axonal transport of rat neurohypophysial proteins and peptides. J Cell Biol 73:366-381.
20. Gracy KN, Pickel VM. 1996. Ultrastructural immunocytochemical localization of the N-methyl-D-aspartate receptor and tyrosine hydroxylase in the shell of the rat nucleus accumbens. Brain Res 739:169-181.
21. Gray EG. 1959. Axo-somatic and axo-dendritic synapses of the cerebral cortex: an electron microscope study. J Anat 93:420-433.
22. Groenewegen HJ, Wright CI, Beijer AV, Voorn P. 1999. Convergence and segregation of ventral striatal inputs and outputs. Ann NY Acad Sci 877:49-63.
23. Hanson GR, Singh N, Merchant K, Johnson M, Gibb JW. 1995. The role of NMDA receptor systems in neuropeptide responses to stimulants of abuse. Drug Alcohol Depend 37:107-110.
24. Hara Y, Pickel VM. 2005. Overlapping intracellular and differential synaptic distributions of dopamine D1 and glutamate NMDA receptors in rat nucleus accumbens. J Comp Neurol 492:442-455.
25. Heidbreder C, Feldon J. 1998. Amphetamine-induced neurochemical and locomotor responses are expressed differentially across the anteroposterior axis of the core and shell subterritories of the nucleus accumbens. Synapse 29:310-322.
26. Heidbreder CA, Goldberg SR, Shippenberg TS. 1993. The kappa-opioid receptor agonist U-69593 attenuates cocaine-induced behavioral sensitization in the rat. Brain Res 616:335-338.
27. Heidbreder CA, Schenk S, Partridge B, Shippenberg TS. 1998. Increased responsiveness of mesolimbic and mesostriatal dopamine neurons to cocaine following repeated administration of a selective kappa-opioid receptor agonist. Synapse 30:255-262.
28. Heijna MH, Padt M, Hogenboom F, Portoghese PS, Mulder AH, Schoffelmeer AN. 1990. Opioid receptor-mediated inhibition of dopamine and acetylcholine release from slices of rat nucleus accumbens, olfactory tubercle and frontal cortex. Eur J Pharmacol 181:267-278.
29. Heimer L, Zahm DS, Churchill L, Kalivas PW, Wohltmann C. 1991. Specificity in the projection patterns of accumbal core and shell in the rat. Neuroscience 41:89-125.
30. Hokfelt T, Broberger C, Xu ZQ, Sergeyev V, Ubink R, Diez M. 2000. Neuropeptides-an overview. Neuropharmacology 39:1337-1356.
31. Höllt V. 1983. Multiple endogenous opioid peptides. Trends Neurosci 6:24-26.
32. Ikemoto S. 2002. Ventral striatal anatomy of locomotor activity induced by cocaine, D-amphetamine, dopamine and D1/D2 agonists. Neuroscience 113:939-955.
33. Ito R, Dalley JW, Howes SR, Robbins TW, Everitt BJ. 2000. Dissociation in conditioned dopamine release in the nucleus accumbens core and shell in response to cocaine cues and during cocaine-seeking behavior in rats. J Neurosci 20:7489-7495.
34. Johnson LR, Aylward RL, Hussain Z, Totterdell S. 1994. Input from the amygdala to the rat nucleus accumbens: its relationship with tyrosine hydroxylase immunoreactivity and identified neurons. Neuroscience 61:851-865.
35. Lee T, Kaneko T, Taki K, Mizuno N. 1997. Preprodynorphin-, pre-proenkephalin-, and preprotachykinin-expressing neurons in the rat neostriatum: an analysis by immunocytochemistry and retrograde tracing. J Comp Neurol 386:229-244.
36. Levey AI, Hersch SM, Rye DB, Sunahara RK, Niznik HB, Kitt CA, Price DL, Maggio R, Brann MR, Ciliax BJ. 1993. Localization of D1 and D2 dopamine receptors in brain with subtype-specific antibodies. Proc Natl Acad Sci USA 90:8861-8865.
37. Mains RE, Cullen EI, May V, Eipper BA. 1987. The role of secretory granules in peptide biosynthesis. Ann NY Acad Sci 493:278-291.
38. Mao L, Conquet F, Wang JQ. 2001. Augmented motor activity and reduced striatal Preprodynorphin mRNA induction in response to acute amphetamine administration in metabotropic glutamate receptor 1 knockout mice. Neuroscience 106:303-312.
39. Mao L, Conquet F, Wang JQ. 2002. Impaired preprodynorphin, but not preproenkephalin, mRNA induction in the striatum of mGluR1 mutant mice in response to acute administration of the full dopamine D(1) agonist SKF-82958. Synapse 44:86-93.
40. Meredith GE. 1999. The synaptic framework for chemical signaling in nucleus accumbens. Ann NY Acad Sci 877:140-156.
41. Merg F, Filliol D, Usynin I, Bazov I, Bark N, Hurd YL, Yakovleva T, Kieffer BL, Bakalkin G. 2006. Big dynorphin as a putative endogenous ligand for the kappa-opioid receptor. J Neurochem 97:292-301.
42. Nikoshkov A, Hurd YL, Yakovleva T, Bazov I, Marinova Z, Cebers G, Pasikova N, Gharibyan A, Terenius L, Bakalkin G. 2005. Prodynorphin transcripts and proteins differentially expressed and regulated in the adult human brain. FASEB J 19:1543-1545.
43. Nirenberg MJ, Chan J, Pohorille A, Vaughan RA, Uhl GR, Kuhar MJ, Pickel VM. 1997. The dopamine transporter: comparative ultrastructure of dopaminergic axons in limbic and motor compartments of the nucleus accumbens. J Neurosci 17:6899-6907.
44. O'Donnell P, Grace AA. 1993. Dopaminergic modulation of dye coupling between neurons in the core and shell regions of the nucleus accumbens. J Neurosci 13:3456-3471.
45. Parsons LH, Justice JB, Jr. 1992. Extracellular concentration and in vivo recovery of dopamine in the nucleus accumbens using microdialysis. J Neurochem 58:212-218.
46. Paxinos G, Watson C. 1986. The Rat Brain in Stereotaxic Coordinates. Orlando: Academic Press.
47. Peters A, Palay SL, Webster HD. 1991. The Fine Structure of the Nervous System. New York: Oxford University Press.
48. Pickel VM, Chan J, Kash TL, Rodriguez JJ, MacKie K. 2004. Compartment-specific localization of cannabinoid 1 (CBl) and mu-opioid receptors in rat nucleus accumbens. Neuroscience 127:101-112.
49. Pickel VM, Nirenberg MJ, Milner TA. 1996. Ultrastructural view of central catecholaminergic transmission: immunocytochemical localization of synthesizing enzymes, transporters and receptors. J Neurocytol 25:843-856.
50. Reynolds ES. 1963. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208-212.
51. Rodd-Henricks ZA, McKinzie DL, Li TK, Murphy JM, McBride WJ. 2002. Cocaine is self-administered into the shell but not the core of the nucleus accumbens of Wistar rats. J Pharmacol Exp Ther 303:1216-1226.
52. Sante AB, Nobre MJ, Brandao ML. 2000. Place aversion induced by blockade of mu or activation of kappa opioid receptors in the dorsal periaqueductal gray matter. Behav Pharmacol 11:583-589.
53. Schenk S, Partridge B, Shippenberg TS. 1999. U69593, a kappa-opioid agonist, decreases cocaine self-administration and decreases cocaine-produced drug-seeking. Psychopharmacology (Berl) 144:339-346.
54. Schlussman SD, Zhang Y, Yuferov V, LaForge KS, Ho A, Kreek MJ. 2003. Acute "binge" cocaine administration elevates dynorphin mRNA in the caudate putamen of C57BL/6J but not 129/J mice. Brain Res 974:249-253.
55. Sesack SR, Pickel VM. 1992. Prefrontal cortical efferents in the rat synapse on unlabeled neuronal targets of catecholamine terminals in the nucleus accumbens septi and on dopamine neurons in the ventral tegmental area. J Comp Neurol 320:145-160.
56. Shippenberg TS, LeFevour A, Heidbreder C. 1996. Kappa-Opioid receptor agonists prevent sensitization to the conditioned rewarding effects of cocaine. J Pharmacol Exp Ther 276:545-554.
57. Sotelo C, Gotow T, Wassef M. 1986. Localization of glutamic-acid- decarboxylase-immunoreactive axon terminals in the inferior olive of the rat, with special emphasis on anatomical relations between GABAergic synapses and dendrodendritic gap junctions. J Comp Neurol 252:32-50.
58. Sotelo C, Korn H. 1978. Morphological correlates of electrical and other interactions through low-resistance pathways between neurons of the vertebrate central nervous system. Int Rev Cytol 55:67-107.
59. Svingos AL, Chavkin C, Colago EE, Pickel VM. 2001. Major coexpression of kappa-opioid receptors and the dopamine transporter in nucleus accumbens axonal profiles. Synapse 42:185-192.
60. Svingos AL, Colago EE, Pickel VM. 1999. Cellular sites for dynorphin activation of kappa-opioid receptors in the rat nucleus accumbens shell. J Neurosci 19:1804-1813.
61. Swanson LW. 1982. The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Res Bull 9:321-353.
62. Thompson AC, Zapata A, Justice JB, Jr., Vaughan RA, Sharpe LG, Shippenberg TS. 2000. Kappa-opioid receptor activation modifies dopamine uptake in the nucleus accumbens and opposes the effects of cocaine. J Neurosci 20:9333-9340.
63. Thureson-Klein AK, Klein RL. 1990. Exocytosis from neuronal large dense-cored vesicles. Int Rev Cytol 121:67-126.
64. Totterdell S, Smith AD. 1989. Convergence of hippocampal and dopaminergic input onto identified neurons in the nucleus accumbens of the rat. J Chem Neuroanat 2:285-298.
65. Van Bockstaele EJ, Sesack SR, Pickel VM. 1994. Dynorphin-immunoreactive terminals in the rat nucleus accumbens: cellular sites for modulation of target neurons and interactions with catecholamine afferents. J Comp Neurol 341:1-15.
66. Voorn P, Jorritsma-Byham B, Van Dijk C, Buijs RM. 1986. The dopaminergic innervation of the ventral striatum in the rat: a light- and electron-microscopical study with antibodies against dopamine. J Comp Neurol 251:84-99.
67. West AR, Floresco SB, Charara A, Rosenkranz JA, Grace AA. 2003. Electrophysiological interactions between striatal glutamatergic and dopaminergic systems. Ann NY Acad Sci 1003:53-74.
68. Winsky-Sommerer R, Benjannet S, Rovere C, Barbero P, Seidah NG, Epelbaum J, Dournaud P. 2000. Regional and cellular localization of the neuroendocrine prohormone convertases PC1 and PC2 in the rat central nervous system. J Comp Neurol 424:439-460.
69. Yung KK, Bolam JP, Smith AD, Hersch SM, Ciliax BJ, Levey AI. 1995. Immunocytochemical localization of D1 and D2 dopamine receptors in the basal ganglia of the rat: light and electron microscopy. Neuroscience 65:709-730.
70. Zahm DS, Brog JS. 1992. On the significance of subterritories in the "accumbens" part of the rat ventral striatum. Neuroscience 50:751-767.
71. Zhou Y, Spangler R, Schlussman SD, Yuferov VP, Sora I, Ho A, Uhl GR, Kreek MJ. 2002. Effects of acute "binge" cocaine on pre-prodynorphin, preproenkephalin, proopiomelanocortin, and corticotropin-releasing hormone receptor mRNA levels in the striatum and hypothalamic-pituitary-adrenal axis of mu-opioid receptor knockout mice. Synapse 45:220-229.
72. Zupanc GK. 1996. Peptidergic transmission: from morphological correlates to functional implications. Micron 27:35-91.