Sildenafil counteracts the inhibitory effect of social subordination on competitive aggression and sexual motivation in male mice

Behavioural Brain Research

Volumn 216, Issue 1, 2011, Pages 193-199

  Dadomo, Harold ^a   Volpi, Riccardo ^a   Ferrari, Massimiliano ^a   Vignali, Alessandro ^a   Bartolomucci, Alessandro ^a   Palanza, Paola ^a   Parmigiani, Stefano ^a  

^a UNIVERSITY OF PARMA   (Italy)

Author keywords

Body weight; Competitive aggression; Sexual behaviour; Sildenafil; Social subordination; Stress; Tadalafil; Vardenafil

Indexed keywords

SILDENAFIL; SODIUM CHLORIDE;

AGGRESSION; ANIMAL EXPERIMENT; ARTICLE; CENTRAL NERVOUS SYSTEM; COMPETITIVE BEHAVIOR; CONTROLLED STUDY; FEMALE; LATENT PERIOD; MALE; MENTAL STRESS; MOTIVATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SEX DIFFERENCE; SEXUAL BEHAVIOR; SIBLING; SOCIAL BEHAVIOR; SOCIAL DOMINANCE; SOCIAL INTERACTION; WEIGHT GAIN;

AGGRESSION; ANALYSIS OF VARIANCE; ANIMALS; DOMINANCE-SUBORDINATION; MALE; MICE; MOTIVATION; PIPERAZINES; PURINES; SEXUAL BEHAVIOR, ANIMAL; SULFONES;

EID: 78149408403     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2010.07.036     Document Type: Article

References (70)

1. Jackson G., Gillies H., Osterloh I. Past, present, and future: a 7-year update of Viagra (sildenafil citrate). Int J Clin Pract 2005, 59:680-691.
2. Demas G., Eliasson M., Dawson T., Dawson V., Kriegsfeld L., Nelson R., et al. Inhibition of neuronal nitric oxide synthase increases aggressive behavior in mice. Mol Med 1997, 3:610-616.
3. Philips B.G., Kato M., Pesek C.A., Winnicki M., Narkiewicz K., Davison D., et al. Sympathetic activation by sildenafil. Circulation 2000, 19:3068-3073.
4. Loughney K., Hill T., Florio V., Uher L., Rosman G., Wolda S., et al. Isolation and characterization of cDNAs encoding PDE5A, a human cGMP-binding, cGMP-specific 3',5'-cyclic nucleotide phosphodiesterase. Gene 1998, 216:139-147.
5. Beavo J. Cyclic nucleotide phosphodiesterases: functional implications of multiple isoforms. Physiol Rev 1995, 75:725-748.
6. Vobig M. Retinal side-effects of sildenafil. Lancet 1999, 353:1442.
7. Sanna F., Succu S., Boi A., Melis M., Argiolas A. Phosphodiesterase type 5 inhibitors facilitate noncontact erections in male rats: site of action in the brain and mechanism of action. J Sex Med 2009, 10:2680-2689.
8. Zhang R., Wang Y., Zhang L., Zhang Z., Tsang W., Lu M., et al. Sildenafil (Viagra) induces neurogenesis and promotes functional recovery after stroke in rats. Stroke 2002, 33:2675-2680.
9. Zhang R., Zhang Z., Zhang L., Wang Y., Zhang C., Chopp M. Delayed treatment with sildenafil enhances neurogenesis and improves functional recovery in aged rats after focal cerebral ischemia. J Neurosci Res 2006, 83:1213-1219.
10. Singh N., Parle M. Sildenafil improves acquisition and retention of memory in mice. Indian J Physiol Pharmacol 2003, 47:318-324.
11. Schultheiss D., Müller S., Nager W., Stief C., Schlote N., Jonas U., et al. Central effects of sildenafil (Viagra) on auditory selective attention and verbal recognition memory in humans: a study with event-related brain potentials. World J Urol 2001, 19:46-50.
12. Ferrari F., Ottani A., Giuliani D. Influence of sildenafil on central dopamine-mediated behaviour in male rats. Life Sci 2002, 70:1501-1508.
13. Hotchkiss A., Pyter L., Gatien M., Wen J., Milman H., Nelson R. Aggressive behavior increases after termination of chronic sildenafil treatment in mice. Physiol Behav 2005, 83:683-688.
14. Harkin A., Bruce K., Craft B., Paul I. Nitric oxide synthase inhibitors have antidepressant-like properties in mice. 1. Acute treatments are active in the forced swim test. Eur J Pharmacol 1999, 372:207-213.
15. Parmigiani S., Ferrari P., Palanza P. An evolutionary approach to behavioral pharmacology: using drugs to understand proximate and ultimate mechanisms of different forms of aggression in mice. Neurosci Biobehav Rev 1998, 23:143-153.
16. Parmigiani S., Palanza P., Rogers J., Ferrari P. Selection, evolution of behavior and animal models in behavioral neuroscience. Neurosci Biobehav Rev 1999, 23:957-969.
17. Reimer J., Petras M. Breeding structure of the house mouse, Mus musculus, in a population cage. J Mammal 1967, 48:88-99.
18. Berry R.J. Population dynamics of the house mouse. Biology of the house mouse 1981, vol. 47:395-425. Symp Zool Soc, London.
19. Hurst J.L. Behavioral variation in wild house mice Mus domesticus Rutty: a quantitative assessment of female social organization. Anim Behav 1987, 35:1846-1857.
20. Kudryavtseva N., Amstislavskaya T., Kucheryavy S. Effects of repeated aggressive encounters on approach to a female and plasma testosterone in male mice. Horm Behav 2004, 45:103-107.
21. Soma K., Scotti M., Newman A., Charlier T., Demas G. Novel mechanisms for neuroendocrine regulation of aggression. Front Neuroendocrinol 2008, 29:476-489.
22. Gleason E., Fuxjager M., Oyegbile T., Marler C. Testosterone release and social context: when it occurs and why. Front Neuroendocrinol 2009, 30:460-469.
23. Shimozuru M., Kikusui T., Takeuchi Y., Mori Y. Social-defeat stress suppresses scent-marking and social-approach behaviors in male Mongolian gerbils (Meriones unguiculatus). Physiol Behav 2006, 88:620-627.
24. D'Amato F. Effects of male social status on reproductive success and on behavior in mice (Mus musculus). J Comp Psychol 1988, 102:146-151.
25. D'Amato F., Pavone F. Role of anxiety in subordinate male mice sexual behavior. Pharmacol Biochem Behav 1992, 43:181-185.
26. D'Amato F., Rizzi R., Moles A. A model of social stress in dominant mice: effects on socio-sexual behaviour. Physiol Behav 2001, 73:421-426.
27. Shimozuru M., Kikusui T., Takeuchi Y., Mori Y. Scent-marking and sexual activity may reflect social hierarchy among group-living male Mongolian gerbils (Meriones unguiculatus). Physiol Behav 2006, 89:644-649.
28. Bartolomucci A., Palanza P., Sacerdote P., Ceresini G., Chirieleison A., Panerai A., et al. Individual housing induces altered immuno-endocrine responses to psychological stress in male mice. Psychoneuroendocrinology 2003, 28:540-558.
29. Bartolomucci A., Pederzani T., Sacerdote P., Panerai A., Parmigiani S., Palanza P. Behavioral and physiological characterization of male mice under chronic psychosocial stress. Psychoneuroendocrinology 2004, 29:899-910.
30. Behn D., Potter M. Sildenafil-mediated reduction in retinal function in heterozygous mice lacking the gamma-subunit of phosphodiesterase. Invest Ophthalmol Vis Sci 2001, 42:523-527.
31. Brain P. The use of animals in aggression research. Aggress Behav 1981, 7:383-387.
32. Bartolomucci A., Palanza P., Gaspani L., Limiroli E., Panerai A., Ceresini G., et al. Social status in mice: behavioral, endocrine and immune changes are context dependent. Physiol Behav 2001, 73:401-410.
33. Bartolomucci A., Palanza P., Parmigiani S., Pederzani T., Merlot E., Neveu P., et al. Chronic psychosocial stress down-regulates central cytokines mRNA. Brain Res Bull 2003, 62:173-178.
34. Parmigiani S., Palanza P., Brain P.F. Ethoexperimental analysis of different forms of intraspecific aggression in the house mouse (Mus musculus). NATO ASI series 1989, 418-431. Kluwer Science Publisher, Dodrecht, The Netherlands. R. Blanchard, P.F. Brain, D.C. Blanchard, S. Parmigiani (Eds.).
35. Palanza P., Gioiosa L., Parmigiani S. Social stress in mice: gender differences and effects of estrous cycle and social dominance. Physiol Behav 2001, 73:411-420.
36. Van Oortmerssen G. Biological significance, genetics and evolutionary origin of variability in behaviour within and between inbred strains of mice (Mus musculus). A behaviour genetic study. Behaviour 1971, 38:1-92.
37. Wilcox R.R. New statistical procedures for the social sciences: modern solutions to the basic problems 1987, Erlbaum, Hillsdale, NJ.
38. Everitt B. Sexual motivation: a neural and behavioural analysis of the mechanisms underlying appetitive and copulatory responses of male rats. Neurosci Biobehav Rev 1990, 14:217-232.
39. Agmo A., Pfaff D. Research on the neurobiology of sexual behavior at the turn of the millennium. Behav Brain Res 1999, 105:1-4.
40. Agmo A. Sexual motivation-an inquiry into events determining the occurrence of sexual behavior. Behav Brain Res 1999, 105:129-150.
41. Chan J., Olivier B., de Jong T., Snoeren E., Kooijman E., van Hasselt F., et al. Translational research into sexual disorders: pharmacology and genomics. Eur J Pharmacol 2008, 585:426-435.
42. Bouayed J., Desor F., Soulimani R. Subacute oral exposure to benzo[alpha]pyrene (B[alpha]P) increases aggressiveness and affects consummatory aspects of sexual behaviour in male mice. J Hazard Mater 2009, 169:581-585.
43. Bartolomucci A., Palanza P., Sacerdote P., Panerai A., Sgoifo A., Dantzer R., et al. Social factors and individual vulnerability to chronic stress exposure. Neurosci Biobehav Rev 2005, 29:67-81.
44. Bartolomucci A., Cabassi A., Govoni P., Ceresini G., Cero C., Berra D., et al. Metabolic consequences and vulnerability to diet-induced obesity in male mice under chronic social stress. PLoS One 2009, 4:e4331.
45. Bartolomucci A. Resource loss and stress-related disease: is there a link?. Med Sci Monit 2005, 11:147-154.
46. Canteros G., Rettori V., Genaro A., Suburo A., Gimeno M., McCann S. Nitric oxide synthase content of hypothalamic explants: increase by norepinephrine and inactivated by NO and cGMP. Proc Natl Acad Sci USA 1996, 93:4246-4250.
47. Nelson R., Trainor B., Chiavegatto S., Demas G. Pleiotropic contributions of nitric oxide to aggressive behavior. Neurosci Biobehav Rev 2006, 30:346-355.
48. Nelson R.J. Effects of nitric oxide on the HPA axis and aggression. Novartis Found Symp 2005, 268:147-160. [discussion 160-6, 167-70].
49. Angel C., Deluca D., Murphree O. Probenecid-induced accumulation of cyclic nucleotides, 5-hydroxyindoleacetic acid, and homovanillic acid in cisternal spinal fluid of genetically nervous dogs. Biol Psychiatry 1976, 11:743-753.
50. Brown G., Goodwin F., Ballenger J., Goyer P. Cerebrospinal fluid amine metabolites and cyclic nucleotides in human aggression. Psychopharmacol Bull 1981, 17:63-65.
51. Kantak K., Hegstrand L., Eichelman B. Influence of cyclic nucleotides on defensive, offensive and predatory aggression in rodents. Prog Clin Biol Res 1984, 169:305-317.
52. Nelson R., Chiavegatto S. Molecular basis of aggression. Trends Neurosci 2001, 24:713-719.
53. Chiavegatto S., Dawson V., Mamounas L., Koliatsos V., Dawson T., Nelson R. Brain serotonin dysfunction accounts for aggression in male mice lacking neuronal nitric oxide synthase. Proc Natl Acad Sci USA 2001, 98:1277-1281.
54. Saraiva K., Silva A., Wanderley M., De Araújo A., De Souza J., Peixoto C. Chronic treatment with sildenafil stimulates Leydig cell and testosterone secretion. Int J Exp Pathol 2009, 90:454-462.
55. Giammanco M., Tabacchi G., Giammanco S., Di Majo D., La Guardia M. Testosterone and aggressiveness. Med Sci Monit 2005, 11:RA136-145.
56. Pfaff D., Choleris E., Ogawa S. Genes for sex hormone receptors controlling mouse aggression. Novartis Found Symp, 268 2005, 78-89. [discussion 89-95, 96-9].
57. Archer J. Testosterone and human aggression: an evaluation of the challenge hypothesis. Neurosci Biobehav Rev 2006, 30:319-345.
58. D'Aquila P., Brain P., Willner P. Effects of chronic mild stress on performance in behavioural tests relevant to anxiety and depression. Physiol Behav 1994, 56:861-867.
59. Grønli J., Murison R., Fiske E., Bjorvatn B., Sørensen E., Portas C., et al. Effects of chronic mild stress on sexual behavior, locomotor activity and consumption of sucrose and saccharine solutions. Physiol Behav 2005, 84:571-577.
60. Yoshimura H., Kimura N. Ethopharmacology of copulatory disorder induced by chronic social conflict in male mice. Neurosci Biobehav Rev 1991, 15(4):497-500.
61. Sugiura K., Yoshimura H., Yokoyama M. An animal model of copulatory disorder induced by social stress in male mice: effects of apomorphine and l-dopa. Psychopharmacology (Berl) 1997, 133:249-255.
62. Melis M., Succu S., Argiolas A. Dopamine agonists increase nitric oxide production in the paraventricular nucleus of the hypothalamus: correlation with penile erection and yawning. Eur J Neurosci 1996, 8:2056-2063.
63. Du J., Hull E. Effects of testosterone on neuronal nitric oxide synthase and tyrosine hydroxylase. Brain Res 1999, 836:90-98.
64. Ottani A., Giuliani D., Ferrari F. Modulatory activity of sildenafil on copulatory behaviour of both intact and castrated male rats. Pharmacol Biochem Behav 2002, 72:717-722.
65. Giuliani D., Ottani A., Ferrari F. Influence of sildenafil on copulatory behaviour in sluggish or normal ejaculator male rats: a central dopamine mediated effect?. Neuropharmacology 2002, 42:562-567.
66. Hull E., Lorrain D., Du J., Matuszewich L., Lumley L., Putnam S., et al. Hormone-neurotransmitter interactions in the control of sexual behavior. Behav Brain Res 1999, 105:105-116.
67. D'yakonova V., Krushinskii A. Effects of an NO synthase inhibitor on aggressive and sexual behavior in male crickets. Neurosci Behav Physiol 2006, 36:565-571.
68. Iwasaki M., Nishino H., Delago A., Aonuma H. Effects of NO/cGMP signaling on behavioral changes in subordinate male crickets, Gryllus bimaculatus. Zoolog Sci 2007, 24:860-868.
69. Bartolomucci A., Leopardi R. Stress and depression: preclinical research and clinical implications. PLoS One 2009, 4:e4265.
70. Ayala J., Bracy D., Julien B., Rottman J., Fueger P., Wasserman D. Chronic treatment with sildenafil improves energy balance and insulin action in high fat-fed conscious mice. Diabetes 2007, 56:1025-1033.