Intranasal administration of progesterone increases dopaminergic activity in amygdala and neostriatum of male rats

Neuroscience

Volumn 157, Issue 1, 2008, Pages 196-203

  de Souza Silva, M A ^a   Topic, B ^a   Huston, J P ^a   Mattern, C ^b  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b M et P Pharma AG   (Switzerland)

Author keywords

basolateral amygdala; dopamine; dorsal striatum; intranasal; microdialysis; progesterone

Indexed keywords

DOPAMINE; PROGESTERONE; URETHAN;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DRUG EFFECT; DRUG MECHANISM; ELECTROCHEMICAL DETECTION; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; MALE; MICRODIALYSIS; NEOSTRIATUM; NONHUMAN; PRIORITY JOURNAL; RAT;

3,4-DIHYDROXYPHENYLACETIC ACID; ADMINISTRATION, INTRANASAL; AMYGDALA; ANIMALS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DOPAMINE; HOMOVANILLIC ACID; IMMUNOHISTOCHEMISTRY; INJECTIONS, SUBCUTANEOUS; MALE; MICRODIALYSIS; NEOSTRIATUM; PROGESTERONE; PROGESTINS; RATS; RATS, WISTAR;

EID: 54549088687     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2008.09.003     Document Type: Article

References (63)

1. Agis-Balboa R.C., Pinna G., Zhubi A., Maloku E., Veldic M., Costa E., and Guidotti A. Characterization of brain neurons that express enzymes mediating neurosteroid biosynthesis. Proc Natl Acad Sci U S A 103 (2006) 14602-14607
2. Anand Kumar T.C., David G.F., Sankaranarayanan A., Puri V., and Sundram K.R. Pharmacokinetics of progesterone after its administration to ovariectomized rhesus monkeys by injection, infusion, or nasal spraying. Proc Natl Acad Sci U S A 79 (1982) 4185-4189
3. Barron A.M., Fuller S.J., Verdile G., and Martins R.N. Reproductive hormones modulate oxidative stress in Alzheimer's disease. Antioxid Redox Signal 8 (2006) 2047-2059
4. Baulieu E.E., Robel P., and Schumacher M. Neurosteroids: beginning of the story. Int Rev Neurobiol 46 (2001) 1-32
5. Belelli D., and Lambert J.J. Neurosteroids: endogenous regulators of the GABA(A) receptor. Nat Rev Neurosci 6 (2005) 565-575
6. Birzniece V., Backstrom T., Johansson I.M., Lindblad C., Lundgren P., Lofgren M., Olsson T., Ragagnin G., Taube M., Turkmen S., Wahlstrom G., Wang M.D., Wihlback A.C., and Zhu D. Neuroactive steroid effects on cognitive functions with a focus on the serotonin and GABA systems. Brain Res Rev 51 (2006) 212-239
7. Boix F., Sandor P., Nogueira P.J., Huston J.P., and Schwarting R.K. Relationship between dopamine release in nucleus accumbens and place preference induced by substance P injected into the nucleus basalis magnocellularis region. Neuroscience 64 (1995) 1045-1055
8. Buddenberg T.E., Topic B., de Souza Silva M.A., Huston J.P., and Mattern C. Behavioral actions of intranasal application of dopamine: effects on forced swimming, elevated plus-maze and open field parameters. Neuropsychobiology 57 (2008) 70-79
9. Chen X.Q., Fawcett J.R., Rahman Y.E., Ala T.A., and Frey II W.H. Delivery of nerve growth factor to the brain via the olfactory pathway. J Alzheimers Dis 1 (1998) 35-44
10. Chow H.H., Anavy N., and Villalobos A. Direct nose-brain transport of benzoylecgonine following intranasal administration in rats. J Pharm Sci 90 (2001) 1729-1735
11. Chow H.S., Chen Z., and Matsuura G.T. Direct transport of cocaine from the nasal cavity to the brain following intranasal cocaine administration in rats. J Pharm Sci 88 (1999) 754-758
12. Cicinelli E., Cignarelli M., Resta L., Scorcia P., Petruzzi D., and Santoro G. Effects of the repetitive administration of progesterone by nasal spray in postmenopausal women. Fertil Steril 60 (1993) 1020-1024
13. Cicinelli E., Nahoul K., Sabatelli S., Petruzzi D., Lapenna M., Scorcia P., and Schonauer L.M. Administration of unmodified progesterone by nasal spray in fertile women. Gynecol Endocrinol 9 (1995) 289-293
14. Costantino H.R., Illum L., Brandt G., Johnson P.H., and Quay S.C. Intranasal delivery: physicochemical and therapeutic aspects. Int J Pharm 337 (2007) 1-24
15. David G.F., Puri C.P., and Anand Kumar T.C. Bioavailability of progesterone enhanced by intranasal spraying. Experientia 37 (1981) 533-534
16. Dazzi L., Serra M., Seu E., Cherchi G., Pisu M.G., Purdy R.H., and Biggio G. Progesterone enhances ethanol-induced modulation of mesocortical dopamine neurons: antagonism by finasteride. J Neurochem 83 (2002) 1103-1109
17. de Souza Silva M.A., Mattern C., Hacker R., Nogueira P.J., Huston J.P., and Schwarting R.K. Intranasal administration of the dopaminergic agonists L-DOPA, amphetamine, and cocaine increases dopamine activity in the neostriatum: a microdialysis study in the rat. J Neurochem 68 (1997) 233-239
18. de Souza Silva M.A., Mattern C., Hacker R., Tomaz C., Huston J.P., and Schwarting R.K. Increased neostriatal dopamine activity after intraperitoneal or intranasal administration of L-DOPA: on the role of benserazide pretreatment. Synapse 27 (1997) 294-302
19. de Souza Silva M.A., Müller C., and Huston J.P. Microdialysis in the brain of anesthetized vs. freely moving animals. In: Westerink B.H.C., and Cremers T.F.I.H. (Eds). Handbook of microdialysis: methods, applications and clinical aspects (2007), Elsevier, Amsterdam 71-92
20. de Souza Silva M.A., Topic B., Huston J.P., and Mattern C. Intranasal dopamine application increases dopaminergic activity in the neostriatum and nucleus accumbens and enhances motor activity in the open field. Synapse 62 (2008) 176-184
21. de Souza Silva M.A., Mattern C., Topic B., Buddenberg T.E., and Huston J.P. Dopaminergic and Serotonergic activity in neostriatum and nucleus accumbens enhanced by intranasal administration of testosterone. Eur Neuropsychopharmacol (2008) in press
22. de Ziegler D., and Fanchin R. Progesterone and progestins: applications in gynecology. Steroids 65 (2000) 671-679
23. Di Paolo T., Levesque D., and Daigle M. A physiological dose of progesterone affects rat striatum biogenic amine metabolism. Eur J Pharmacol 125 (1986) 11-16
24. Dreher J.C., Schmidt P.J., Kohn P., Furman D., Rubinow D., and Berman K.F. Menstrual cycle phase modulates reward-related neural function in women. Proc Natl Acad Sci U S A 104 (2007) 2465-2470
25. El Etr M., Vukusic S., Gignoux L., Durand-Dubief F., Achiti I., Baulieu E.E., and Confavreux C. Steroid hormones in multiple sclerosis. J Neurol Sci 233 (2005) 49-54
26. Engin E., and Treit D. The anxiolytic-like effects of allopregnanolone vary as a function of intracerebral microinfusion site: the amygdala, medial prefrontal cortex, or hippocampus. Behav Pharmacol 18 (2007) 461-470
27. Funada M., and Hara C. Differential effects of psychological stress on activation of the 5-hydroxytryptamine- and dopamine-containing neurons in the brain of freely moving rats. Brain Res 901 (2001) 247-251
28. Genazzani A.R., Bernardi F., Pluchino N., Begliuomini S., Lenzi E., Casarosa E., and Luisi M. Endocrinology of menopausal transition and its brain implications. CNS Spectr 10 (2005) 449-457
29. Goletiani N.V., Keith D.R., and Gorsky S.J. Progesterone: review of safety for clinical studies. Exp Clin Psychopharmacol 15 (2007) 427-444
30. Graff C.L., and Pollack G.M. Nasal drug administration: potential for targeted central nervous system delivery. J Pharm Sci 94 (2005) 1187-1195
31. Hori K., Tanaka J., and Nomura M. Effects of discrimination learning on the rat amygdala dopamine release: a microdialysis study. Brain Res 621 (1993) 296-300
32. Illum L. Is nose-to-brain transport of drugs in man a reality?. J Pharm Pharmacol 56 (2004) 3-17
33. Illum L. Nanoparticulate systems for nasal delivery of drugs: a real improvement over simple systems?. J Pharm Sci 96 (2007) 473-483
34. Inglis F.M., and Moghaddam B. Dopaminergic innervation of the amygdala is highly responsive to stress. J Neurochem 72 (1999) 1088-1094
35. Laconi M.R., Reggiani P.C., Penissi A., Yunes R., and Cabrera R.J. Allopregnanolone modulates striatal dopaminergic activity of rats under different gonadal hormones conditions. Neurol Res 29 (2007) 622-627
36. Liu X.F., Fawcett J.R., Thorne R.G., DeFor T.A., and Frey W.H. Intranasal administration of insulin-like growth factor-I bypasses the blood-brain barrier and protects against focal cerebral ischemic damage. J Neurol Sci 187 (2001) 91-97
37. Lu W., Jiang W., Chen J., Yin M., Wang Z., and Jiang X. Modulation of brain delivery and copulation by intranasal apomorphine hydrochloride. Int J Pharm 349 (2008) 196-205
38. Mani S.K. Signaling mechanisms in progesterone-neurotransmitter interactions. Neuroscience 138 (2006) 773-781
39. Mattsson L.A., Christiansen C., Colau J.C., Palacios S., Kenemans P., Bergeron C., Chevallier O., Von Holst T., and Gangar K. Clinical equivalence of intranasal and oral 17beta-estradiol for postmenopausal symptoms. Am J Obstet Gynecol 182 (2000) 545-552
40. McEwen B.S. Non-genomic and genomic effects of steroids on neural activity. Trends Pharmacol Sci 12 (1991) 141-147
41. Minn A., Leclerc S., Heydel J.M., Minn A.L., Denizcot C., Cattarelli M., Netter P., and Gradinaru D. Drug transport into the mammalian brain: the nasal pathway and its specific metabolic barrier. J Drug Target 10 (2002) 285-296
42. Mitsushima D., Yamada K., Takase K., Funabashi T., and Kimura F. Sex differences in the basolateral amygdala: the extracellular levels of serotonin and dopamine, and their responses to restraint stress in rats. Eur J Neurosci 24 (2006) 3245-3254
43. Nonaka N., Farr S.A., Kageyama H., Shioda S., and Banks W.A. Delivery of galanin-like peptide to the brain: targeting with intranasal delivery and cyclodextrins. J Pharmacol Exp Ther 325 (2008) 513-519
44. Paxinos G., and Watson C. The rat brain in stereotactic coordinates (1986), Academic Press, San Diego, CA
45. Petitclerc M., Bedard P.J., and Di Paolo T. Progesterone releases dopamine in male and female rat striatum: a behavioral and microdialysis study. Prog Neuropsychopharmacol Biol Psychiatry 19 (1995) 491-497
46. Robel P., and Baulieu E.E. Neurosteroids biosynthesis and function. Trends Endocrinol Metab 5 (1994) 1-8
47. Scharfman H.E., and MacLusky N.J. The influence of gonadal hormones on neuronal excitability, seizures, and epilepsy in the female. Epilepsia 47 (2006) 1423-1440
48. Schumacher M., Akwa Y., Guennoun R., Robert F., Labombarda F., Desarnaud F., Robel P., De Nicola A.F., and Baulieu E.E. Steroid synthesis and metabolism in the nervous system: trophic and protective effects. J Neurocytol 29 (2000) 307-326
49. Schumacher M., Guennoun R., Ghoumari A., Massaad C., Robert F., El Etr M., Akwa Y., Rajkowski K., and Baulieu E.E. Novel perspectives for progesterone in hormone replacement therapy, with special reference to the nervous system. Endocr Rev 28 (2007) 387-439
50. Schumacher M., Guennoun R., Robert F., Carelli C., Gago N., Ghoumari A., Gonzalez Deniselle M.C., Gonzalez S.L., Ibanez C., Labombarda F., Coirini H., Baulieu E.E., and De Nicola A.F. Local synthesis and dual actions of progesterone in the nervous system: neuroprotection and myelination. Growth Horm IGF Res 14 Suppl A (2004) S18-S33
51. Schumacher M., Guennoun R., Stein D.G., and De Nicola A.F. Progesterone: therapeutic opportunities for neuroprotection and myelin repair. Pharmacol Ther 116 (2007) 77-106
52. Smolders I., De Klippel N., Sarre S., Ebinger G., and Michotte Y. Tonic GABA-ergic modulation of striatal dopamine release studied by in vivo microdialysis in the freely moving rat. Eur J Pharmacol 284 (1995) 83-91
53. Stein D.G. Brain damage, sex hormones and recovery: a new role for progesterone and estrogen?. Trends Neurosci 24 (2001) 386-391
54. Stein D.G. The case for progesterone. Ann N Y Acad Sci 1052 (2005) 152-169
55. Stein D.G. Progesterone exerts neuroprotective effects after brain injury. Brain Res Rev 57 (2008) 386-397
56. Tavares M.C., Topic B., Abreu C., Waga I., Gomes U., Tomaz C., and Mattern C. Effects of intra-nasally administered testosterone on sexual proceptive behavior in female capuchin monkeys (Cebus apella). Behav Brain Res 179 (2007) 33-42
57. Thorne R.G., Pronk G.J., Padmanabhan V., and Frey W.H. Delivery of insulin-like growth factor-I to the rat brain and spinal cord along olfactory and trigeminal pathways following intranasal administration. Neuroscience 127 (2004) 481-496
58. Topic B., Tavares M.C., Tomaz C., and Mattern C. Prolonged effects of intra-nasally administered testosterone on proceptive behavior in female capuchin monkeys (Cebus apella). Behav Brain Res 179 (2007) 60-68
59. Vallee M., Mayo W., Koob G.F., and Le Moal M. Neurosteroids in learning and memory processes. Int Rev Neurobiol 46 (2001) 273-320
60. van den Berg M.P., Verhoef J.C., Romeijn S.G., and Merkus F.W. Uptake of estradiol or progesterone into the CSF following intranasal and intravenous delivery in rats. Eur J Pharm Biopharm 58 (2004) 131-135
61. van Wingen G.A., van Broekhoven F., Verkes R.J., Petersson K.M., Backstrom T., Buitelaar J.K., and Fernandez G. Progesterone selectively increases amygdala reactivity in women. Mol Psychiatry 13 (2008) 325-333
62. Wang X., He H., Leng W., and Tang X. Evaluation of brain-targeting for the nasal delivery of estradiol by the microdialysis method. Int J Pharm 317 (2006) 40-46
63. Yokoyama M., Suzuki E., Sato T., Maruta S., Watanabe S., and Miyaoka H. Amygdalic levels of dopamine and serotonin rise upon exposure to conditioned fear stress without elevation of glutamate. Neurosci Lett 379 (2005) 37-41