Implants of estradiol conjugated to bovine serum albumin in the male rat medial preoptic area promote copulatory behavior

Neuroendocrinology

Volumn 86, Issue 4, 2007, Pages 249-259

  Huddleston, Gloria G ^a   Paisley, Jacquelyn C ^a   Graham, Sean ^a   Grober, Matthew S ^a   Clancy, Andrew N ^a  

^a GEORGIA STATE UNIVERSITY   (United States)

Author keywords

Dihydrotestosterone; Estrogen receptor; Immunocytochemistry; Sexual behavior

Indexed keywords

ANDROSTANOLONE; ESTRADIOL; SERUM ALBUMIN;

ANALYTIC METHOD; ANIMAL EXPERIMENT; ARTICLE; CASTRATION; CELL MEMBRANE; CELL SURFACE; CONTROLLED STUDY; COPULATION; FEMALE; IMMUNOCYTOCHEMISTRY; MALE; MATING; NONHUMAN; PREOPTIC AREA; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION;

ANIMALS; CATTLE; COPULATION; DRUG IMPLANTS; ESTRADIOL; ESTROGENS, CONJUGATED (USP); FEMALE; MALE; PREOPTIC AREA; RATS; RATS, SPRAGUE-DAWLEY; SERUM ALBUMIN, BOVINE;

EID: 36248934661     PISSN: 00283835     EISSN: None     Source Type: Journal    
DOI: 10.1159/000107695     Document Type: Article

References (74)

1. Massa R, Stupnicka E, Kniewald Z, Martini L: The transformation of testosterone to dihydrotestosterone by the brain and anterior pituitary. J Steroid Biochem 1972;3:385-399.
2. Naftolin F, Ryan KJ, Davies IJ, Reddy V, Flores F, Petro Z, Kuhn M, White RJ, Takaoka Y, Wolin L: The formation of estrogens by central neuroendocrine tissues. Recent Prog Horm Res 1975;31:295-319.
3. Vagell ME, McGiniss MY: The role of aromatization in the restoration of male rat reproductive behavior. J Neuroendocrinol 1997;9:415-421.
4. Davidson JH: Activation of the male rat's sexual behavior by intracerebral implantation of androgen. Endocrinology 1966;79:783-794.
5. Cottingham SL, Pfaff D: Interconnectedness of steroid hormone-binding neurons: existence and implications. Curr Top Neuroendocrinol 1986;7:223-249.
6. Pfaff DW: Drive: Neurobiological and Molecular Mechanisms of Sexual Motivation, ed 1. Cambridge, MIT, 1999.
7. Simerly RB, Swanson LW: The organization of neural inputs to the medial preoptic nucleus of the rat. J Comp Neural 1986;246:312-342.
8. Simerly RB, Swanson LW: Projections of the medial preoptic nucleus: a Phaseolus vulgaris leucoagglutinin anterograde tract-tracing study in the rat. J Comp Neurol 1988;270:209-242.
9. Larsson K, Heimer L: Mating behavior of male rats after lesions in the preoptic area. Nature 1964;202:413-414.
10. Christensen LW, Nance DM, Gorski RA: Effects of hypothalamic and preoptic lesions on reproductive behavior in male rats. Brain Res Bull 1977;2:137-141.
11. Liu YC, Salamone JD, Sachs BD: Lesions in medial preoptic area and bed nucleus of stria terminalis: differential effects on copulatory behavior and noncontact erection in male rats. J Neurosci 1997;13:5245-5253.
12. Hanson S, Kohler C, Goldstein M, Steinbusch HVM: Effects of ibotenic acid-induced neuronal degeneration in the medial preoptic area and the lateral hypothalamic area on sexual behavior in the male rat. Brain Res 1982;239:213-232.
13. Brackett NL, Edwards DA: Medial preoptic connections with the midbrain tegementum are essential for male sexual behavior. Physiol Behav 1984;32:79-84.
14. Maillard-Gutekunst CA, Edwards DA: Preoptic and subthalamic connections with the caudal brainstem are important for copulation in the male rat. Behav Neurosci 1994;108:758-766.
15. Pfaff DW, Pfaffmann C: Olfactory and hormonal influences on the basal forebrain of the male rat. Brain Res 1969;15:137-156.
16. Yamada Y: Effects of testosterone on unit activity in rat hypothalamus and septum. Brain Res 1979;172:165-168.
17. Bueno J, Pfaff DW: Single unit recording in hypothalamus and preoptic area of estrogentreated and untreated ovariectomized female rats. Brain Res 1976;101:67-78.
18. Kelly MJ, Moss RL, Dudley CA: Differential sensitivity of preoptic-septal neurons to microelectrophoresed estrogen during the estrus cycle. Brain Res 1976;114:152-157.
19. McGinnis MY, William GW, Lumia AR: Inhibition of male sexual behavior by androgen receptor blockade in preoptic area or hypothalamus, but not amygdala or septum. Physiol Behav 1996;60:783-789.
20. Davis PG, Barfield RJ: Activation of masculine sexual behavior by intracranial estradiol benzoate implants in male rats. Neuroendocrinology 1979;28:217-227.
21. Gréco B, Edwards DA, Michael RP, Clancy AN: Androgen receptors and estrogen receptors are colocalized in male rat hypothalamic and limbic neurons that express fos immunoreactivity induced by mating. Neuroendocrinology 1998;67:18-28.
22. Sagar SM, Sharp FR, Curran T: Expression of c-fos protein in brain: metabolic mapping at the cellular level. Science 1988;240:1328-1331.
23. Bonsall RW, Clancy AN, Michael RP: Effects of the nonsteroidal inhibitor, fadrozole, on sexual behavior in male rats. Horm Behav 1992;20:240-254.
24. Clancy AN, Zumpe D, Michael RP: Intracerebral infusion of an aromatase inhibitor, sexual behavior and brain estrogen receptorlike immunoreactivity in intact male rats. Neuroendocrinology 1995;61:98-111.
25. Clancy AN, Zumpe D, Michael RP: Estrogen in the medial preoptic area of male rats facilitates copulatory behavior. Horm Behav 2000;38:86-93.
26. Jensen EV, Suzuki T, Kawashima T, Stumpf WE, Jungblut PW, DeSombre ER: A two-step mechanism for the interaction of estradiol with rat uterus. Proc Natl Acad Sci USA 1968;59:632-638.
27. White R, Lees JA, Needham M, Ham J, Parker M: Structural organization and expression of the mouse estrogen receptor. Mol Endocrinol 1987;1:735-744.
28. King WJ, Greene GL: Monoclonal antibodies localize oestrogen receptor in the nuclei of target cells. Nature 1984;307:745-747.
29. McGinnis MY, Kahn DF: Inhibition of male sexual behavior by intracranial implants of the protein synthesis inhibitor anisomycin into the medial preoptic area of the rat. Horm Behav 1997;31:15-23.
30. Charlier TD, Ball GF, Balthazart J: Inhibition of steroid coactivator-1 blocks estrogen and androgen activation on male sexual behavior and associated brain plasticity. J Neurosci 2005;25:906-913.
31. Pietras R, Szego CM: Specific binding sites for oestrogen at the outer surfaces of isolated endometrial cells. Nature 1977;265:69-72.
32. Minami T, Oomura Y, Nabekura J, Fukuda A: 17β-Estradiol depolarization of hypothalamic neurons is mediated by cyclic AMP. Brain Res 1990;519:301-307.
33. Thomas P, Pang Y, Filardo EJ, Dong J: Identity of an estrogen membrane receptor coupled to a G protein in human breast cancer cells. Endocrinology 2005;146:624-632.
34. Revankar CM, Cimino DF, Sklar LA, Arterburn JB, Prossnitz ER: A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science 2005;307:1625-1630.
35. Zhou Y, Watters J, Dorsa DM: Estrogen rapidly induces the phosphorylation of the cAMP response element binding protein in rat brain. Endocrinology 1996;137:2163-2166.
36. Watters JJ, Campbell JS, Cunningham MJ, Krebs EG, Dorsa DM: Rapid membrane effects of steroids in neuroblastoma cells: effects of estrogen on mitogen activated protein kinase signaling cascade and c-fos immediate early gene transcription. Endocrinology 1997;138:4030-4033.
37. + current in hippocampal pyramidal neurons. J Neurosci 2003;23:6338-6344.
38. Chaban VV, Lakhter AJ, Micevych P: A membrane estrogen receptor mediates intracellular calcium release in astrocytes. Endocrinology 2004;145:3788-3795.
39. Lagrange AH, Rønnekleiv OK, Kelly MJ: Modulation of G protein-coupled receptors by an estrogen receptor that activates protein kinase A. Mol Pharmacol 1997;4:605-612.
40. Pappas TC, Bahiru G, Watson C: Membrane estrogen receptor identified by multiple antibody labeling and impeded-ligand binding. FASEB J 1995;9:404-410.
41. Lugg JA, Rajfer J, González-Cadavid NF: Dihydrotestosterone is the active androgen in the maintenance of nitric oxide-mediated penile erection in the rat. Endocrinology 1995;136:1495-1501.
42. Ando S, Aquila S, Beraldi E, Canonaco M, Panno ML, Valenti A, Dessi-Fulgheri F: Physiological changes in androgen plasma levels with elapsing of time from castration in adult male rats. Horm Metab Res 1988:20:96-99.
43. Parte P, Juneja HS: Temporal changes in the serum levels of gonadotrophins and testosterone in male rats bearing subcutaneous implants of 5 alpha-dihydrotestosterone. Int J Androl 1992;15:355-364.
44. Swanson LW: Brain maps: Structure of the Rat Brain, ed 2, revised. Amsterdam, Elsevier, 1998.
45. Brackett NL, Iuvone PM, Edwards DA: Midbrain lesions, dopamine and male sexual behavior. Behav Brain Res 1986;20:231-240.
46. Kirk RE: Experimental Design: Procedures for the Behavioral Sciences. Belmont, Wadsworth, 1968.
47. Simoncini T, Nafezi-Moghadam A, Brazil DP, Klaus L, Chin WW, Liao JK: Interaction of oestrogen receptor with the regulatory subunit of phosphatidylinositol-3-OH-kinase. Nature 2000;407:538-541.
48. Kousteni S, Chen JR, Bellido T, Han L, Ali AA, O'Brien CA, Plotkin L, Fu Q, Mancino AT, Wen Y, Vertino AM, Powers CC, Stewart SA, Ebert R, Parfitt AM, Weinstein RS, Jilka RL, Manolagas SC: Reversal of bone loss in mice by nongenotropic signaling of sex steroids. Science 2002;298:843-846.
49. Cross E, Roselli CE: 17β-Estradiol rapidly facilitates chemoinvestigation and mounting in castrate male rats. Am J Physiol 1999;276:1346-1350.
50. Frye CA, Mermelstein PG, DeBold JF: Evidence for a non-genomic action of progestins on sexual receptivity in hamster ventral tegmental areas but not hypothalamus. Brain Res 1992;578:87-93.
51. Paisley JC, Huddleston GG, Denman HN, Carruth LL, Grober MS, Petrulis A, Clancy AN: Inhibition of estrogen receptor synthesis in the medial preoptic area, but not the medial amygdala, reduces male rat mating behavior. Horm Behav 2005;48:94.
52. Price RH, Lorenzon N, Handa RJ: Differential expression of estrogen receptor beta splice variants in rat brain: identification and characterization of a novel variant missing exon 4. Brain Res Mol Brain Res 2000;80:260-268.
53. Wersinger JR, Sannen K, Villalba C, Lubahn DB, Rissman EF, De Vries GJ: Masculine sexual behavior is disrupted in male and female mice lacking a functional estrogen receptor alpha gene. Horm Behav 1997;32:176-183.
54. Khan MM, Hadman M, Wakade C, De Sevilla LM, Dhandapani KM, Mahesh VB, Vadlamudi RK, Brann DW: Cloning, expression, and localization of MNAR/PELP1 in rodent brain: colocalization in estrogen receptor-α- but not in gonadotropin-releasing hormone-positive neurons. Endocrinology 2005;146:5215-5227.
55. Huddleston GG, Paisley JC, Clancy AN: Effects of estrogen in the male rat medial amygdala: infusion of an aromatase inhibitor lowers mating and bovine serum albumin conjugated-estradiol implants do not promote mating. Neuroendocrinology 2006;83:106-116.
56. Carrer HF, Cambiasso MJ, Gorosito S: Effects of estrogen on neuronal growth and differentiation. J Steroid Biochem Mol Biol 2005;93:319-323.
57. Lin BC, Scanlan TS: Few things in life are 'free': cellular uptake of steroid hormones by an active transport mechanism. Mol Interv 2005;5:338-340.
58. Harrington WR, Kim SH, Funk CC, Madak-Erdogan Z, Schiff R, Katzenellenbogen JA, Katzenellenbogen BS: Estrogen dendrimer conjugates that preferentially activate extranuclear, nongenomic versus genomic pathways of estrogen action. Mol Endocrinol 2006;20:491-502.
59. Huddleston GG, Michael RP, Zumpe D, Clancy AN: Estradiol in the male rat amygdala facilitates mounting but not ejaculation. Physiol Behav 2003;79:239-246.
60. Greene GL, Sobel NB, King WJ, Jensen EV: Immunochemical studies of estrogen receptors. J Steroid Biochem 1984;20:51-56.
61. Axelson JF, van Leeuwen FW: Differential localization of estrogen receptors in various vasopressin synthesizing nuclei of the rat brain. J Neuroendocrinol 1990;2:209-216.
62. Clancy AN, Michael RP: Effects of testosterone and aromatase inhibition on estrogen receptor-like immunoreactivity in male rat brain. Neuroendocrinology 1994;59:552-560.
63. Kuiper GG, Enmark F, Pelto-Huikko M, Nilsson S, Gustafsson JA: Cloning of a novel receptor expressed in the rat prostate and ovary. Proc Natl Acad Sci USA 1996;93:5925-5930.
64. Yang SH, Liu R, Perez EJ, Wen Y, Stevens SM Jr, Valencia T, Brun-Zinkernagal AM, Porkai L, Will Y, Dykens J, Koulen P, Simpkins JW: Mitochondrial localization of estrogen receptor β. Proc Natl Acad Sci USA 2004;101:4130-4135.
65. Chambliss KL, Yuhanna IS, Anderson RGW, Mendelsohn ME, Shaul PW: ERβ has nongenomic action at caveolae. Mol Endocrinol 2002;16:938-946.
66. Kelly MJ, Qiu H, Rønnekleiv OK: Estrogen modulation of G-protein-coupled receptor activation of potassium channels to the central nervous system. Ann NY Acad Sci 2003;1007:6-16.
67. Watson CS, Lange CA: Steadying the boat: integrating mechanisms of membrane and nuclear-steroid-receptor signaling. EMBO Rep 2005;6:116-119.
68. Wade CB, Robinson S, Shapiro A, Dorsa DM: Estrogen alpha (ER)α and ERβ exhibit unique pharmacologic properties when coupled to activation of the mitogen-activated protein kinase pathway. Endocrinology 2001;142:2336-2342.
69. Marin R, Ramirez CM, Gonźalez M, Alonso R, Diaz M: Alternative estrogen receptors homologous to classical receptor α in murine neural tissues. Neurosci Lett 2005;395:7-11.
70. Clarke CH, Norfleet AM, Clarke MSF, Watson CS, Cunningham KA, Thomas ML: Perimembrane localization of the estrogen receptor α protein in neuronal processes of cultured hippocampal neurons. Neuroendocrinology 2000;71:34-42.
71. Evinger AJ III, Levin ER: Requirements for estrogen receptor α membrane localization and function. Steroids 2005;70:361-363.
72. Song RXD, Zhang Z, Santen RJ: Estrogen rapid action via protein complex formation involving ERα and Src. Trends Endocrinol Metab 2005;16:347-353.
73. Lu Q, Pallas DC, Surks HK, Baur WE, Mendelsohn ME, Karas RH: Striatin assembles a membrane signaling complex necessary for rapid, nongenomic activation of endothelial NO synthase by estrogen receptor alpha. Proc Natl Acad Sci USA 2004;101:17126-17131.
74. Nethrapelli IS, Tinnikou AA, Krishnan V, Lei DC, Torran-Allerand CD: Estrogen activates mitogen-activated protein kinase in native, nontransfected CHO-K1, COS-7, RAT2 fibroblast cell lines. Endocrinology 2005;146:56-63.