Dopamine agonist-induced penile erection and yawning: A comparative study in outbred Roman high- and low-avoidance rats

Pharmacology Biochemistry and Behavior

Volumn 109, Issue , 2013, Pages 59-66

  Sanna, Fabrizio ^a   Corda, Maria Giuseppa ^a   Melis, Maria Rosaria ^a   Piludu, Maria Antonietta ^a   Löber, Stefan ^c   Hübner, Harald ^c   Gmeiner, Peter ^c   Argiolas, Antonio ^a,b   Giorgi, Osvaldo ^a  

^a UNIVERSITY OF CAGLIARI   (Italy)

^b CNR   (Italy)

^c UNIVERSITY OF ERLANGEN NUREMBERG   (Germany)

Author keywords

Dopamine agonists; Dopamine antagonists; Penile erection; Roman rats; Yawning

Indexed keywords

3 [[4 (4 CHLOROPHENYL) 1 PIPERAZINYL]METHYL] 1H PYRROLO[2,3 B]PYRIDINE; 3 [[4 (4 CHLOROPHENYL) 4 HYDROXYPIPERIDIN 1YL]METHYL 1H INDOLE]; [2 [4 (4 CHLOROPHENYL)PIPERAZIN 1 YL]METHYL]PYRAZOLO[1,5 A]PYRIDINE; APOMORPHINE; DOPAMINE 2 RECEPTOR; DOPAMINE 3 RECEPTOR; DOPAMINE 4 RECEPTOR; DOPAMINE RECEPTOR BLOCKING AGENT; FAUC 213; L 741626; N [4 (2 CYANOPHENYL) 1 PIPERAZINYLMETHYL] 3 METHYLBENZAMIDE; N [4 [2 (6 CYANO 1,2,3,4 TETRAHYDRO 2 ISOQUINOLINYL)ETHYL]CYCLOHEXYL] 4 QUINOLINECARBOXAMIDE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; COMPARATIVE STUDY; DOSE RESPONSE; DRUG EFFECT; DRUG RECEPTOR BINDING; DRUG RESPONSE; MALE; NONHUMAN; PENIS ERECTION; PRIORITY JOURNAL; RAT; YAWNING;

ANIMALS; AVOIDANCE LEARNING; BENZAMIDES; DOPAMINE AGONISTS; PENILE ERECTION; PIPERAZINES; PYRAZOLES; PYRIDINES; PYRROLES; RATS; RATS, SPRAGUE-DAWLEY; SPECIES SPECIFICITY; YAWNING;

RATTUS;

EID: 84878236867     PISSN: 00913057     EISSN: 18735177     Source Type: Journal    
DOI: 10.1016/j.pbb.2013.05.002     Document Type: Article

References (62)

1. A. Argiolas, and M.R. Melis Neuromodulation of penile erection: an overview of the role of neurotransmitters and neuropeptides Prog Neurobiol 47 1995 235 255 (Pubitemid 26022923)
2. A. Argiolas, and M.R. Melis The neuropharmacology of yawning Eur J Pharmacol 343 1998 1 16 (Pubitemid 28161046)
3. A. Argiolas, and M.R. Melis Central control of penile erection: role of the paraventricular nucleus of the hypothalamus Prog Neurobiol 76 2005 1 21 (Pubitemid 41033401)
4. T.A. Baskerville, and A.J. Douglas Interactions between dopamine and oxytocin in the control of sexual behaviour Prog Brain Res 170 2008 277 290 (Pubitemid 352010235)
5. T.A. Baskerville, J. Allard, C. Wayman, and A.J. Douglas Dopamine-oxytocin interactions in penile erection Eur J Neurosci 30 2009 2151 2164
6. G. Bignami Selection for high rates and low rates of avoidance conditioning in the rat Anim Behav 13 1965 221 227
7. J.D. Brioni, R.B. Moreland, M. Cowart, G.C. Hsieh, A.O. Stewart, and P. Hedlund Activation of dopamine D4 receptors by ABT-724 induces penile erection in rats Proc Natl Acad Sci U S A 101 2004 6758 6763 (Pubitemid 38586047)
8. R.M. Buijs, M. Geffard, C.W. Pool, and E.M. Hoorneman The dopaminergic innervation of the supraoptic and paraventricular nucleus. A light and electron microscopical study Brain Res 323 1984 65 72 (Pubitemid 15216770)
9. J. Carrasco, C. Marquez, R. Nadal, A. Tobeña, A. Fernandez-Teuel, and A. Armario Characterization of central and peripheral components of the hypothalamus-pituitary-adrenal axis in the inbred Roman rat strains Psychoneuroendocrinology 33 2008 437 445
10. G.T. Collins, A.H. Newman, P. Grundt, K.C. Rice, S.M. Husbands, and C. Chauvignac Yawning and hypothermia in rats: effects of dopamine D3 and D2 agonists and antagonists Psychopharmacology 193 2007 159 170 (Pubitemid 47025018)
11. G.T. Collins, A. Truccone, F. Haji-Abdi, A.H. Newman, P. Grundt, and K.C. Rice Proerectile effects of dopamine D2-like agonists are mediated by the D3 receptor in rats and mice J Pharmacol Exp Ther 329 2009 210 217
12. A. Dahlström, and K. Fuxe Evidence for the existence of monoamine containing neurons in the central nervous system. I: demonstration of monoamines in the cell bodies of brain stem neurons Acta Physiol Scand 62 1964 1 55
13. R. Depoortère, L. Bardin, M. Rodrigues, E. Abrial, M. Allaga, and A. Newman-Tancredi Penile erection and yawning induced by dopamine D2-like receptor agonists in rats: influence of strain and contribution of dopamine D2, but not D3 and D4 receptors Behav Pharmacol 20 2009 303 311
14. P. Driscoll, and K. Bättig Behavioral, emotional and neurochemical profiles of rats selected for extreme differences in active, two-way avoidance performance I. Lieblich, Genetics of the brain 1982 Elsevier Amsterdam 95 123
15. P. Driscoll, I. Lieblich, and E. Cohen Amphetamine-induced stereotypic responses in Roman high- and Roman low-avoidance rats Pharmacol Biochem Behav 24 1986 1329 1332 (Pubitemid 16067418)
16. P. Driscoll, R.M. Escorihuela, A. Fernández-Teruel, O. Giorgi, H. Schwegler, and T. Steimer Genetic selection and differential stress responses: the Roman lines/strains of rats Ann N Y Acad Sci 851 1998 501 510
17. M.J. Durcan, D.W. Fulker, and I.C. Camphell Differences in the stereotypy response but not the hypomotility response to apomorphine in the Roman high and low avoiding strains of rats Psychopharmacology 82 1984 215 220 (Pubitemid 14184545)
18. C. Enguehard-Gueiffier, H. Hübner, A. El Hakmaoui, H. Allouchi, P. Gmeiner, and A. Argiolas 2-[(4-Phenylpiperazin-1-yl)methyl]imidazo(di)azines as selective D4-ligands. Induction of penile erection by 2-[4-(2-methoxyphenyl) piperazin-1-ylmethyl]imidazo[1,2-a]pyridine (PIP3EA), a potent and selective D4 partial agonist J Med Chem 49 2006 3938 3947 (Pubitemid 43967891)
19. R.M. Escorihuela, A. Tobenã, P. Driscoll, and A. Fernández-Teruel Effects of training, early handling, and perinatal flumazenil on shuttle box acquisition in Roman low-avoidance rats: toward overcoming a genetic deficit Neurosci Biobehav Rev 19 1995 353 367
20. R.M. Escorihuela, A. Fernández-Teruel, A. Tobeña, W. Langhans, K. Bättig, and P. Driscoll Labyrinth exploration, emotional reactivity, and conditioned fear in young Roman/Verh inbred rats Behav Genet 27 1997 573 578 (Pubitemid 28098965)
21. R.M. Escorihuela, A. Fernández-Teruel, L. Gil, R. Aguilar, A. Tobeña, and P. Driscoll Inbred Roman high- and low-avoidance rats: differences in anxiety, novelty-seeking, and shuttlebox behaviors Physiol Behav 67 1999 19 26 (Pubitemid 29329488)
22. L. Fattore, G. Piras, M.G. Corda, and O. Giorgi The Roman high- and low-avoidance rat lines differ in the acquisition, maintenance, extinction, and reinstatement of intravenous cocaine self-administration Neuropsychopharmacology 34 2009 1091 1101
23. A. Fernández-Teruel, R.M. Escorihuela, B. Castellano, B. González, and A. Tobeña Neonatal handling and environmental enrichment effects on emotionality, novelty/reward seeking, and age-related cognitive and hippocampal impairments: focus on the Roman rat lines Behav Genet 27 1997 513 526 (Pubitemid 28098959)
24. A. Fernández-Teruel, P. Driscoll, L. Gil, R. Aguilar, A. Tobeña, and R.M. Escorihuela Enduring effects of environmental enrichment on novelty seeking, saccharin and ethanol intake in two rat lines (RHA/Verh and RLA/Verh) differing in incentive-seeking behavior Pharmacol Biochem Behav 73 2002 225 231 (Pubitemid 34667034)
25. L. Giménez-Llort, T. Cañete, M. Guitart-Masip, A. Fernández-Teruel, and A. Tobeña Differential apomorphine-induced locomotion, stereotypy and yawning patterns in Roman high- and low avoidance rats: revealing two singular dopaminergic phenotypes Physiol Behav 86 2005 458 466
26. O. Giorgi, M. Orlandi, R.M. Escorihuela, P. Driscoll, D. Lecca, and M.G. Corda GABAergic and dopaminergic transmission in the brain of Roman high-avoidance and Roman low-avoidance rats Brain Res 638 1994 133 138 (Pubitemid 24063297)
27. O. Giorgi, D. Lecca, G. Piras, P. Driscoll, and M.G. Corda Dissociation between mesocortical dopamine release and fear-related behaviours in two psychogenetically selected lines of rats that differ in coping strategies to aversive conditions Eur J Neurosci 17 2003 2716 2726 (Pubitemid 36819296)
28. O. Giorgi, D. Lecca, G. Piras, and M.G. Corda Differential activation of dopamine release in the nucleus accumbens core and shell after acute or repeated amphetamine injections: a comparative study in the Roman high- and low-avoidance rat lines Neuroscience 135 2005 987 998 (Pubitemid 41407760)
29. O. Giorgi, G. Piras, and M.G. Corda The psychogenetically selected Roman high- and low-avoidance rat lines: a model to study the individual vulnerability to drug addiction Neurosci Biobehav Rev 31 2007 148 163 (Pubitemid 44880079)
30. S.A. Glase, H.C. Akunne, L.M. Georgic, T.G. Heffner, R.G. MacKenzie, and P.J. Manley Substituted [(4-phenylpiperazinyl)-methyl]benzamides: selective dopamine D4 agonists J Med Chem 40 1997 1771 1772 (Pubitemid 27251265)
31. M. Guitart-Masip, B. Johansson, A. Fernández-Teruel, T. Cañete, A. Tobeña, and L. Terenius Divergent anatomical pattern of D1 and D3 binding and DARPP-32 mRNA expression in the Roman rat strains. Implications for drug addiction Neuroscience 142 2006 1231 1243
32. M. Guitart-Masip, B. Johansson, A. Fernández-Teruel, A. Tobeña, and L. Giménez-Llort Divergent effect of the selective D3 receptor agonist PD-128,907 on locomotor activity in Roman high- and low-avoidance rats: relationship to NGFI-A gene expression in the Calleja islands Psychopharmacology 196 2008 39 49
33. G.C. Hsieh, P.R. Hollingsworth, B. Martino, R. Chang, M.A. Terranova, and A.B. O'Neill Central mechanisms regulating penile erection in conscious rats: the dopaminergic systems related to the proerectile effect of apomorphine J Pharmacol Exp Ther 308 2004 330 338 (Pubitemid 38090735)
34. J.J. Kulagowski, H.B. Broughton, N.R. Curtis, I.M. Mawer, M.P. Ridgill, and R. Baker 3-[[4-(4-Chlorophenyl)piperazin-1-yl]-methyl]-1H-pyrrolo[2,3-b] pyridine: an antagonist with high affinity and selectivity for the human dopamine D4 receptor J Med Chem 39 1996 1941 1942 (Pubitemid 26163243)
35. N.M. Lauzon, and S.R. Laviolette Dopamine D4-receptor modulation of cortical neuronal network activity and emotional processing: implications for neuropsychiatric disorders Behav Brain Res 208 2010 12 22
36. D. Lecca, G. Piras, P. Driscoll, O. Giorgi, and M.G. Corda A differential activation of dopamine output in the shell and core of the nucleus accumbens is associated with the motor responses to addictive drugs: a brain dialysis study in Roman high- and low-avoidance rats Neuropharmacology 46 2004 688 699 (Pubitemid 38292973)
37. O. Lindvall, A. Björklund, and G. Skagerberg Selective histochemical demonstration of dopamine terminal systems in rat di- and telencephalon: new evidence for dopaminergic innervation of hypothalamic neurosecretory nuclei Brain Res 306 1984 19 30 (Pubitemid 14090441)
38. S. Löber, H. Hubner, W. Utz, and P. Gmeiner Rationally based efficacy tuning of selective dopamine D4 receptor ligands leading to the complete antagonist 2-[4-(4-Chlorophenyl)piperazin-1-ylmethyl]pyrazolo[1,5-a] pyridine (FAUC 213) J Med Chem 44 2001 2691 2694 (Pubitemid 32879710)
39. S. Löber, N. Tschammer, H. Hübner, M.R. Melis, A. Argiolas, and P. Gmeiner The azulene framework as a novel arene bioisostere: design of potent dopamine D4 receptor ligands inducing penile erection ChemMedChem 4 2009 325 328
40. S. Löber, H. Hübner, A. Buschauer, F. Sanna, A. Argiolas, and M.R. Melis Novel azulene derivatives for the treatment of erectile dysfunction Bioorg Med Chem Lett 22 2012 7151 7154
41. R. López-Aumatell, E. Vicens-Costa, M. Guitart-Masip, E. Martínez-Membrives, W. Valdar, and M. Johannesson Unlearned anxiety predicts learned fear: a comparison among heterogeneous rats and the Roman rat strains Behav Brain Res 202 2009 92 101
42. M.R. Melis, and A. Argiolas Dopamine and sexual behavior Neurosci Biobehav Rev 19 1995 19 38
43. M.R. Melis, and A. Argiolas Yawning: role of hypothalamic paraventricular nitric oxide Acta Pharmacol Sin 20 1999 778 788 (Pubitemid 29459742)
44. M.R. Melis, and A. Argiolas Central oxytocinergic neurotransmission: a drug target for the therapy of psychogenic erectile dysfunction Curr Drug Targets 4 2003 55 66 (Pubitemid 36131641)
45. M.R. Melis, and A. Argiolas Central control of penile erection: a re-visitation of the role of oxytocin and its interaction with dopamine and glutamic acid in male rats Neurosci Biobehav Rev 35 2011 939 955
46. M.R. Melis, A. Argiolas, and G.L. Gessa Apomorphine-induced penile erection and yawning: site of action in brain Brain Res 415 1987 98 104 (Pubitemid 17097379)
47. M.R. Melis, S. Succu, M.S. Mascia, and A. Argiolas PD-168077, a selective dopamine D4 receptor agonist, induces penile erection when injected into the paraventricular nucleus of male rats Neurosci Lett 379 2005 59 62 (Pubitemid 40462399)
48. M.R. Melis, S. Succu, F. Sanna, T. Melis, M.S. Mascia, and C. Enguehard-Gueiffier PIP3EA and PD-168077, two selective dopamine D4 receptor agonists, induce penile erection in male rats: site and mechanism of action in the brain Eur J Neurosci 24 2006 2021 2030 (Pubitemid 44583486)
49. C. Missale, S.R. Nash, S.W. Robinson, M. Jaber, and M.G. Caron Dopamine receptors: from structure to function Physiol Rev 78 1998 189 225 (Pubitemid 28070979)
50. M. Moreno, D. Diana Cardona, M.J. Gómez, F. Sánchez-Santed, A. Tobeña, and A. Fernández-Teruel Impulsivity characterization in the Roman high- and low-avoidance rat strains: behavioral and neurochemical differences Neuropsychopharmacology 35 2010 1198 1208
51. S. Patel, S. Freedman, K.L. Chapman, F. Emms, A.E. Fletcher, and M. Knowles Biological profile of L 745,870, a selective antagonist with high affinity for the dopamine D4 receptor J Pharmacol Exp Ther 283 1997 636 647 (Pubitemid 27514621)
52. G. Piras, O. Giorgi, and M.G. Corda Effects of antidepressants on the performance in the forced swim test of two psychogenetically selected lines of rats that differ in coping strategies to aversive conditions Psychopharmacology 211 2010 403 414
53. C. Reavill, S.G. Taylor, M.D. Wood, T. Ashmeade, N.E. Austin, and K.Y. Avenell Pharmacological actions of a novel, high-affinity, and selective human dopamine D3 receptor antagonist, SB-277011A J Pharmacol Exp Ther 294 2000 1154 1165 (Pubitemid 30666872)
54. F. Sanna, S. Succu, H. Hübner, P. Gmeiner, A. Argiolas, and M.R. Melis Dopamine D2-like receptor agonists induce penile erection in male rats: differential role of D2, D3 and D4 receptors in the paraventricular nucleus of the hypothalamus Behav Brain Res 2011 [255-169-76]
55. F. Sanna, A. Argiolas, and M.R. Melis Oxytocin-induced yawning: sites of action in the brain and interaction with mesolimbic/mesocortical and incertohypothalamic dopaminergic neurons in male rats Horm Behav 62 2012 505 514
56. F. Sanna, S. Succu, M.R. Melis, and A. Argiolas Dopamine agonist-induced penile erection and yawning: differential role of D2 like receptors and correlation with nitric oxide production in the paraventricular nucleus of male rats Behav Brain Res 230 2012 355 364
57. P. Seeman, and H.H.M. Van Tol Dopamine receptor pharmacology Trends Pharmacol Sci 15 1994 264 270 (Pubitemid 24210734)
58. N. Shioda, Y. Takeuchi, and K. Fukunaga Advanced research on dopamine signaling to develop drugs for the treatment of mental disorders: proteins interacting with the third cytoplasmic loop of dopamine D2 and D3 receptors J Pharmacol Sci 114 2010 25 31
59. P. Sokoloff, and J.C. Schwartz Novel dopamine receptors half a decade later Trends Pharmacol Sci 16 1995 270 275
60. T. Steimer, and P. Driscoll Divergent stress responses and coping styles in psychogenetically selected Roman high-(RHA) and low-(RLA) avoidance rats: behavioural, neuroendocrine and developmental aspects Stress 6 2003 87 100 (Pubitemid 36681959)
61. G. Stemp, T. Ashmeade, C.L. Branch, M.S. Hadley, A.J. Hunter, and C.N. Johnson Design and synthesis of trans-N-[4-[2-(6-cyano-1,2,3,4- tetrahydroisoquinolin-2-yl)ethyl] cyclo hexyl]-4-quinolinecarboxamide (SB-277011): a potent and selective dopamine D3 receptor antagonist with high oral bioavailability and CNS penetration in the rat J Med Chem 43 2000 1878 1885 (Pubitemid 30305020)
62. S. Succu, F. Sanna, T. Melis, A. Boi, A. Argiolas, and M.R. Melis Stimulation of dopamine receptors in the paraventricular nucleus of the hypothalamus of male rats induces penile erection and increases extra-cellular dopamine in the nucleus accumbens: involvement of central oxytocin Neuropharmacology 52 2007 1034 1043 (Pubitemid 46227490)