The role of insulin-like growth factor-I and growth factor-associated signal transduction pathways in estradiol and progesterone facilitation of female reproductive behaviors

Frontiers in Neuroendocrinology

Volumn 27, Issue 4, 2006, Pages 363-375

  Etgen, Anne M ^a   González Flores, Oscar ^b   Todd, Brigitte J ^a  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b DEPARTAMENTO DE FÍSICA   (Mexico)

Author keywords

Estradiol; IGF I; Insulin like growth factor I; Lordosis; Luteinizing hormone release; MAPK; Mitogen activated protein kinase; Progesterone; Progestin receptor; Reproductive behavior

Indexed keywords

ALPHA 1B ADRENERGIC RECEPTOR; CYCLIC GMP; DELTA OPIATE RECEPTOR AGONIST; ESTRADIOL; GROWTH FACTOR; LUTEINIZING HORMONE; MITOGEN ACTIVATED PROTEIN KINASE; PHOSPHATIDYLINOSITOL 3 KINASE INHIBITOR; PROGESTERONE; PROGESTERONE RECEPTOR; PROTEASOME; SOMATOMEDIN C;

ANIMAL BEHAVIOR; BRAIN FUNCTION; BRAIN REGION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; ESTRUS CYCLE; HORMONE ACTION; HORMONE RELEASE; HYPOTHALAMUS; LORDOSIS; NEUROENDOCRINE SYSTEM; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; REPRODUCTION; REVIEW; SEXUAL BEHAVIOR; SIGNAL TRANSDUCTION;

ANIMALS; CYCLIC GMP; ESTRADIOL; FEMALE; INSULIN-LIKE GROWTH FACTOR I; MITOGEN-ACTIVATED PROTEIN KINASES; NEURITES; NEUROSECRETORY SYSTEMS; POSTURE; PROGESTERONE; RECEPTORS, ESTROGEN; RECEPTORS, OPIOID, DELTA; REPRODUCTION; SEXUAL BEHAVIOR; SIGNAL TRANSDUCTION;

EID: 33750959736     PISSN: 00913022     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.yfrne.2006.06.001     Document Type: Review

References (152)

1. Acosta-Martinez M., and Etgen A.M. The role of delta-opioid receptors in estrogen facilitation of lordosis behavior. Behav. Brain Res. 136 (2002) 93-102
2. Acosta-Martinez M., Gonzalez-Flores O., and Etgen A.M. The role of progestin receptors and the mitogen-activated protein kinase pathway in delta opioid receptor facilitation of female reproductive behaviors. Horm Behav. 49 (2006) 458-462
3. Apostolakis E.M., Garai J., Lohmann J.E., Clark J.H., and O'Malley B.W. Epidermal growth factor activates reproductive behavior independent of ovarian steroids in female rodents. Mol. Endocrinol. 14 (2000) 1086-1098
4. Apostolakis E.M., Ramamurphy M., Zhou D., Onate S., and O'Malley B.W. Acute disruption of select steroid receptor coactivators prevents reproductive behavior in rats and unmasks genetic adaptation in knockout mice. Mol. Endocrinol. 16 (2002) 1511-1523
5. Audet N., Paquin-Gobeil M., Landry-Paquet O., Schiller P.W., and Pineyro G. Internalization and src activity regulate the time course of ERK activation by delta opioid receptor ligands. J. Biol. Chem. 280 (2005) 7808-7816
6. Auger A.P., Perrot-Sinal T.S., Auger C.J., Ekas L.A., Tetel M.J., and McCarthy M.M. Expression of the nuclear receptor coactivator, cAMP response element-binding protein, is sexually dimorphic and modulates sexual differentiation of neonatal rat brain. Endocrinology 143 (2002) 3009-3016
7. Beyer C., Gonzalez-Flores O., Garcia-Juarez M., and Gonzalez-Mariscal G. Non-ligand activation of estrous behavior in rodents: cross-talk at the progesterone receptor. Scand. J. Psychol. 44 (2003) 221-229
8. Beyer C., Gonzalez-Flores O., and Gonzalez-Mariscal G. Ring A reduced progestins potently stimulate estrous behavior in rats: paradoxical effect through the progesterone receptor. Physiol. Behav. 58 (1995) 985-993
9. Beyer C., Gonzalez-Flores O., and Gonzalez-Mariscal G. Progesterone receptor participates in the stimulatory effect of LHRH, prostaglandin E2, and cyclic AMP on lordosis and proceptive behaviours in rats. J. Neuroendocrinol. 9 (1997) 609-614
10. Beyer C., and Gonzalez-Mariscal G. Elevation in hypothalamic cyclic AMP as a common factor in the facilitation of lordosis in rodents: a working hypothesis. Ann. NY. Acad. Sci. 474 (1986) 270-281
11. Beyer C., Gonzalez-Mariscal G., Eguibar J.R., and Gomora P. Lordosis facilitation in estrogen primed rats by intrabrain injection of pregnanes. Pharmacol. Biochem. Behav. 31 (1988) 919-926
12. Beyer C., and Karolczak M. Estrogenic stimulation of neurite growth in midbrain dopaminergic neurons depends on cAMP/protein kinase A signalling. J. Neurosci. Res. 59 (2000) 107-116
13. Bi R., Foy M.R., Vouimba R.M., Thompson R.F., and Baudry M. Cyclic changes in estradiol regulate synaptic plasticity through the MAP kinase pathway. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 13391-13395
14. Blaustein J.D. Alteration of sensitivity to progesterone facilitation of lordosis in guinea pigs by modulation of hypothalamic progestin receptors. Brain Res. 243 (1982) 287-300
15. Blaustein J.D. Progestin receptors: neuronal integrators of hormonal and environmental stimulation. Ann. NY. Acad. Sci. 1007 (2003) 238-250
16. Blaustein J.D., and Erskine M. Feminine sexual behavior: cellular integration of hormonal and afferent information in the rodent brain. In: Pfaff D.W., Arnold A.P., Etgen A.M., Fahrbach S.E., and Rubin R.T. (Eds). Hormones, Brain and Behavior vol. 1 (2002), Academic Press, San Diego, CA 139-214
17. Blaustein J.D., and Feder H.H. Cytoplasmic progestin receptors in female guinea pig brain and their relationship to refractoriness in expression of female sexual behavior. Brain Res. 177 (1979) 489-498
18. Blaustein J.D., and Feder H.H. Nuclear progestin receptors in guinea pig brain measured by an in vitro exchange assay after hormonal treatments that affect lordosis. Endocrinology 106 (1980) 1061-1069
19. Blaustein J.D., and Wade G.N. Sequential inhibition of sexual behavior by progesterone in female rats: comparison with a synthetic antiestrogen. J. Comp. Physiol. Psychol. 91 (1977) 752-760
20. Brown T.J., and Blaustein J.D. Inhibition of sexual behavior in female guinea pigs by a progestin receptor antagonist. Brain Res. 301 (1984) 343-349
21. Camacho-Arroyo I., Villamar-Cruz O., Gonzalez-Arenas A., and Guerra-Araiza C. Participation of the 26S proteasome in the regulation of progesterone receptor concentrations in the rat brain. Neuroendocrinology 76 (2002) 267-271
22. Cambiasso M.J., Colombo J.A., and Carrer H.F. Differential effect of oestradiol and astroglia-conditioned media on the growth of hypothalamic neurons from male and female rat brains. Eur. J. Neurosci. 12 (2000) 2291-2298
23. Cardona-Gomez G.P., Chowen J.A., and Garcia-Segura L.M. Estradiol and progesterone regulate the expression of insulin-like growth factor-I receptor and insulin-like growth factor binding protein-2 in the hypothalamus of adult female rats. J. Neurobiol. 43 (2000) 269-281
24. Cardona-Gomez G.P., Mendez P., DonCarlos L.L., Azcoitia I., and Garcia-Segura L.M. Interactions of estrogens and insulin-like growth factor-I in the brain: implications for neuroprotection. Brain Res. Brain Res. Rev. 37 (2001) 320-334
25. Cardona-Gomez G.P., Mendez P., DonCarlos L.L., Azcoitia I., and Garcia-Segura L.M. Interactions of estrogen and insulin-like growth factor-I in the brain: molecular mechanisms and functional implications. J. Steroid Biochem. Mol. Biol. 83 (2002) 211-217
26. Cardona-Gomez G.P., Mendez P., and Garcia-Segura L.M. Synergistic interaction of estradiol and insulin-like growth factor-I in the activation of PI3K/Akt signaling in the adult rat hypothalamus. Brain Res. Mol. Brain Res. 107 (2002) 80-88
27. Chauchereau A., Cohen-Solal K., Jolivet A., Bailly A., and Milgrom E. Phosphorylation sites in ligand-induced and ligand-independent activation of the progesterone receptor. Biochemistry 33 (1994) 13295-13303
28. Cheng Y.J., and Karavolas H.J. Conversion of progesterone to 5 alpha-pregnane-3, 20-dione and 3 alpha-hydroxy-5 alpha-pregnan-20-one by rat medial basal hypothalami and the effects of estradiol and stage of estrous cycle on the conversion. Endocrinology 93 (1973) 1157-1162
29. Chu H.P., and Etgen A.M. A potential role of cyclic GMP in the regulation of lordosis behavior of female rats. Horm. Behav. 32 (1997) 125-132
30. Chu H.P., Morales J.C., and Etgen A.M. Cyclic GMP may potentiate lordosis behaviour by progesterone receptor activation. J. Neuroendocrinol. 11 (1999) 107-113
31. Daftary S.S., and Gore A.C. Developmental changes in hypothalamic insulin-like growth factor-1: relationship to gonadotropin-releasing hormone neurons. Endocrinology 144 (2003) 2034-2045
32. Daftary S.S., and Gore A.C. The hypothalamic insulin-like growth factor-1 receptor and its relationship to gonadotropin-releasing hormone neurones during postnatal development. J. Neuroendocrinol. 16 (2004) 160-169
33. Daftary S.S., and Gore A.C. IGF-1 in the brain as a regulator of reproductive neuroendocrine function. Exp. Biol. Med. (Maywood) 230 (2005) 292-306
34. Etgen A.M. Estrogen regulation of neurotransmitter and growth factor signaling in the brain. In: Pfaff D.W., Arnold A.P., Etgen A.M., Fahrbach S.E., and Rubin R.T. (Eds). Hormones, Brain and Behavior Vol. 3 (2002), Academic Press, San Diego, CA 381-440
35. Etgen A.M. Ovarian steroid and growth factor regulation of female reproductive function involves modification of hypothalamic alpha 1-adrenoceptor signaling. Ann. NY. Acad. Sci. 1007 (2003) 153-161
36. Etgen A.M., and Acosta-Martinez M. Participation of growth factor signal transduction pathways in estradiol facilitation of female reproductive behavior. Endocrinology 144 (2003) 3828-3835
37. Etgen A.M., Ansonoff M.A., and Quesada A. Mechanisms of ovarian steroid regulation of norepinephrine receptor-mediated signal transduction in the hypothalamus: implications for female reproductive physiology. Horm. Behav. 40 (2001) 169-177
38. Etgen A.M., Ungar S., and Petitti N. Estradiol and progesterone modulation of norepinephrine neurotransmission: implications for the regulation of female reproductive behavior. J. Neuroendocrinology. 31 (1992) 799-807
39. Faivre E., Skildum A., Pierson-Mullany L., and Lange C.A. Integration of progesterone receptor mediated rapid signaling and nuclear actions in breast cancer cell models: role of mitogen-activated protein kinases and cell cycle regulators. Steroids 70 (2005) 418-426
40. Fan G.H., Zhao J., Wu Y.L., Lou L.G., Zhang Z., Jing Q., Ma L., and Pei G. N-Methyl-D-aspartate attenuates opioid receptor-mediated G protein activation and this process involves protein kinase C. Mol. Pharmacol. 53 (1998) 684-690
41. Feder H.H., and Marrone B.L. Progesterone: its role in the central nervous system as a facilitator and inhibitor of sexual behavior and gonadotropin release. Ann. NY. Acad. Sci. 286 (1977) 331-354
42. Fernandez-Galaz M.C., Morschl E., Chowen J.A., Torres-Aleman I., Naftolin F., and Garcia-Segura L.M. Role of astroglia and insulin-like growth factor-I in gonadal hormone-dependent synaptic plasticity. Brain Res. Bull. 44 (1997) 525-531
43. Fernandez-Galaz M.C., Naftolin F., and Garcia-Segura L.M. Phasic synaptic remodeling of the rat arcuate nucleus during the estrous cycle depends on insulin-like growth factor-I receptor activation. J. Neurosci. Res. 55 (1999) 286-292
44. Fernandez-Guasti A., Rodriguez-Manzo G., and Beyer C. Effect of guanine derivatives on lordosis behavior in estrogen primed rats. Physiol. Behav. 31 (1983) 589-592
45. Filardo E.J. Epidermal growth factor receptor (EGFR) transactivation by estrogen via the G-protein-coupled receptor, GPR30: a novel signaling pathway with potential significance for breast cancer. J. Steroid Biochem. Mol. Biol. 80 (2002) 231-238
46. Filardo E.J., Quinn J.A., Bland K.I., and Frackelton Jr. A.R. Estrogen-induced activation of Erk-1 and Erk-2 requires the G protein-coupled receptor homolog, GPR30, and occurs via trans-activation of the epidermal growth factor receptor through release of HB-EGF. Mol. Endocrinol. 14 (2000) 1649-1660
47. Filardo E.J., Quinn J.A., Frackelton Jr. A.R., and Bland K.I. Estrogen action via the G protein-coupled receptor, GPR30: stimulation of adenylyl cyclase and cAMP-mediated attenuation of the epidermal growth factor receptor-to-MAPK signaling axis. Mol. Endocrinol. 16 (2002) 70-84
48. Filardo E.J., and Thomas P. GPR30: a seven-transmembrane-spanning estrogen receptor that triggers EGF release. Trends Endocrinol. Metab. 16 (2005) 362-367
49. Frye C.A., Bayon L.E., Pursnani N.K., and Purdy R.H. The neurosteroids, progesterone and 3alpha, 5alpha-THP, enhance sexual motivation, receptivity, and proceptivity in female rats. Brain Res. 808 (1998) 72-83
50. Frystyk J., Delhanty P.J., Skjaerbaek C., and Baxter R.C. Changes in the circulating IGF system during short-term fasting and refeeding in rats. Am. J. Physiol. 277 (1999) E245-E252
51. Galand P., and Rooryck J. Mediation by epidermal growth factor of the estradiol-induced increase in cyclic guanosine 3′,5′-monophosphate content in the rat uterus. Endocrinology 137 (1996) 1932-1937
52. Garcia-Segura L.M., Baetens D., and Naftolin F. Synaptic remodelling in arcuate nucleus after injection of estradiol valerate in adult female rats. Brain Res. 366 (1986) 131-136
53. Garcia-Segura L.M., Chowen J.A., Duenas M., Torres-Aleman I., and Naftolin F. Gonadal steroids as promoters of neuro-glial plasticity. Psychoneuroendocrinology 19 (1994) 445-453
54. Glickman M.H., and Ciechanover A. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol. Rev. 82 (2002) 373-428
55. Goldstein S., Harp J.B., and Phillips L.S. Nutrition and somatomedin. XXII: Molecular regulation of insulin-like growth factor-I during fasting and refeeding in rats. J. Mol. Endocrinol. 6 (1991) 33-43
56. Gonzalez-Flores O., and Etgen A.M. The nitric oxide pathway participates in estrous behavior induced by progesterone and some of its ring A-reduced metabolites. Horm. Behav. 45 (2004) 50-57
57. Gonzalez-Flores O., Guerra-Araiza C., Cerbon M., Camacho-Arroyo I., and Etgen A.M. The 26S proteasome participates in the sequential inhibition of estrous behavior induced by progesterone in rats. Endocrinology 145 (2004) 2328-2336
58. Gonzalez-Flores O., Shu J., Camacho-Arroyo I., and Etgen A.M. Regulation of lordosis by cyclic 3′, 5′-guanosine monophosphate, progesterone, and its 5alpha-reduced metabolites involves mitogen-activated protein kinase. Endocrinology 145 (2004) 5560-5567
59. Gonzalez-Mariscal G., Melo A.I., and Beyer C. Progesterone, but not LHRH or prostaglandin E2, induces sequential inhibition of lordosis to various lordogenic agents. Neuroendocrinology 57 (1993) 940-945
60. Gorzalka B.B., and Whalen R.E. The effects of progestins, mineralocorticoids, glucocorticoids, and steroid solubility on the induction of sexual receptivity in rats. Horm. Behav. 8 (1977) 94-99
61. Herbison A.E. Noradrenergic regulation of cyclic GnRH secretion. Rev. Reprod. 2 (1997) 1-6
62. Herbison A.E., Simonian S.X., Thanky N.R., and Bicknell R.J. Oestrogen modulation of noradrenaline neurotransmission. Neuronal and Cognitive Effects of Oestrogens (2000), John Wiley & Sons Ltd, West Sussex, England 74-93
63. Hiney J.K., Srivastava V., Nyberg C.L., Ojeda S.R., and Dees W.L. Insulin-like growth factor I of peripheral origin acts centrally to accelerate the initiation of female puberty. Endocrinology 137 (1996) 3717-3728
64. Ho A.K., Hashimoto K., and Chik C.L. 3′,5′-cyclic guanosine monophosphate activates mitogen-activated protein kinase in rat pinealocytes. J. Neurochem. 73 (1999) 598-604
65. Hosny S., and Jennes L. Identification of alpha1B adrenergic receptor protein in gonadotropin releasing hormone neurones of the female rat. J. Neuroendocrinol. 10 (1998) 687-692
66. Jones J.E., and Wade G.N. Acute fasting decreases sexual receptivity and neural estrogen receptor-alpha in female rats. Physiol. Behav. 77 (2002) 19-25
67. Kakeya T., Takeuchi S., and Takahashi S. Epidermal growth factor, insulin, and estrogen stimulate development of prolactin-secreting cells in cultures of GH3 cells. Cell Tissue Res. 299 (2000) 237-243
68. Karkanias G.B., Ansonoff M.A., and Etgen A.M. Estradiol regulation of alpha 1b-adrenoceptor mRNA in female rat hypothalamus-preoptic area. J. Neuroendocrinol. 8 (1996) 449-455
69. Karoor V., and Malbon C.C. Insulin-like growth factor receptor-1 stimulates phosphorylation of the beta2-adrenergic receptor in vivo on sites distinct from those phosphorylated in response to insulin. J. Biol. Chem. 271 (1996) 29347-29352
70. Karoor V., Shih M., Tholanikunnel B., and Malbon C.C. Regulating expression and function of G-protein-linked receptors. Prog. Neurobiol. 48 (1996) 555-568
71. Katzenellenbogen J.A., O'Malley B.W., and Katzenellenbogen B.S. Tripartite steroid hormone receptor pharmacology: interaction with multiple effector sites as a basis for the cell- and promoter-specific action of these hormones. Mol. Endocrinol. 10 (1996) 119-131
72. Kazeto Y., Goto-Kazeto R., Thomas P., and Trant J.M. Molecular characterization of three forms of putative membrane-bound progestin receptors and their tissue-distribution in channel catfish, Ictalurus punctatus. J. Mol. Endocrinol 34 (2005) 781-791
73. Kinyamu H.K., Chen J., and Archer T.K. Linking the ubiquitin-proteasome pathway to chromatin remodeling/modification by nuclear receptors. J. Mol. Endocrinol. 34 (2005) 281-297
74. Komalavilas P., Shah P.K., Jo H., and Lincoln T.M. Activation of mitogen-activated protein kinase pathways by cyclic GMP and cyclic GMP-dependent protein kinase in contractile vascular smooth muscle cells. J. Biol. Chem. 274 (1999) 34301-34309
75. Kontula K., Janne O., Vihko R., de Jager E., de Visser J., and Zeelen F. Progesterone-binding proteins: in vitro binding and biological activity of different steroidal ligands. Acta. Endocrinol-Cop 78 (1975) 574-592
76. Kow L.M., and Pfaff D.W. The membrane actions of estrogens can potentiate their lordosis behavior-facilitating genomic actions. P. Natl. Acad. Sci. USA 101 (2004) 12354-12357
77. Kow L.M., Weesner G.D., and Pfaff D.W. Alpha 1-adrenergic agonists act on the ventromedial hypothalamus to cause neuronal excitation and lordosis facilitation: electrophysiological and behavioral evidence. Brain Res. 588 (1992) 237-245
78. Lange C.A., Shen T., and Horwitz K.B. Phosphorylation of human progesterone receptors at serine-294 by mitogen-activated protein kinase signals their degradation by the 26S proteasome. P. Natl. Acad. Sci. USA 97 (2000) 1032-1037
79. Law P.Y., Wong Y.H., and Loh H.H. Molecular mechanisms and regulation of opioid receptor signaling. Annu. Rev. Pharmacol. Toxicol. 40 (2000) 389-430
80. Lee P.D., Giudice L.C., Conover C.A., and Powell D.R. Insulin-like growth factor binding protein-1: recent findings and new directions. Proc. Soc. Exp. Biol. Med. 216 (1997) 319-357
81. LeRoith D., Werner H., Beitner-Johnson D., and Roberts C.T. Molecular and cellular aspects of the insulin-like growth factor I receptor. Endocr. Rev. 16 (1995) 143-163
82. Liang Y.Q., Akishita M., Kim S., Ako J., Hashimoto M., Iijima K., Ohike Y., Watanabe T., Sudoh N., Toba K., Yoshizumi M., and Ouchi Y. Estrogen receptor beta is involved in the anorectic action of estrogen. Int. J. Obes. Relat. Metab. Disord. 26 (2002) 1103-1109
83. Lingham R.B., Stancel G.M., and Loose-Mitchell D.S. Estrogen regulation of epidermal growth factor receptor messenger ribonucleic acid. Mol. Endocrinol. 2 (1988) 230-235
84. Luttrell L.M., Daaka Y., and Lefkowitz R.J. Regulation of tyrosine kinase cascades by G-protein-coupled receptors. Curr. Opin. Cell Biol. 11 (1999) 177-183
85. Ma Y.J., Hill D.F., Junier M.P., Costa M.E., Felder S.E., and Ojeda S.R. Expression of epidermal growth factor receptor changes in the hypothalamus during the onset of female puberty. Mol. Cell Neurosci. 5 (1994) 246-262
86. MacLusky N.J., and McEwen B.S. Oestrogen modulates progestin receptor concentrations in some rat brain regions but not in others. Nature 274 (1978) 276-278
87. Mani S. Signalling mechanisms in progesterone-neurotransmitter interactions. J. Mol. Endocrinol. 30 (2003) 127-137
88. Marrone B.L., Rodriguez-Sierra J.F., and Feder H.H. Lordosis: inhibiting effects of progesterone in the female rat. Horm. Behav. 8 (1977) 391-402
89. McEwen B.S., and Alves S.E. Estrogen actions in the central nervous system. Endocr. Rev. 20 (1999) 279-307
90. Mellon S.H., and Vaudry H. Biosynthesis of neurosteroids and regulation of their synthesis. Int. Rev. Neurobiol. 46 (2001) 33-78
91. Mendez P., Wandosell F., and Garcia-Segura L.M. Cross talk between estrogen receptors and insulin-like growth factor-I receptor in the brain: cellular and molecular mechanisms. Front. Neuroendocrinol. (2006)
92. Miyake A., Tasaka K., Otsuka S., Kohmura H., Wakimoto H., and Aono T. Epidermal growth factor stimulates secretion of rat pituitary luteinizing hormone in vitro. Acta. Endocrinol-Cop 108 (1985) 175-178
93. Moguilewsky M., and Raynaud J.P. Estrogen-sensitive progestin-binding sites in the female rat brain and pituitary. Brain Res. 164 (1979) 165-175
94. Moguilewsky M., and Raynaud J.P. The relevance of hypothalamic and hyphophyseal progestin receptor regulation in the induction and inhibition of sexual behavior in the female rat. Endocrinology 105 (1979) 516-522
95. Morin L.P. Theoretical review. Progesterone: inhibition of rodent sexual behavior. Physiol. Behav. 18 (1977) 701-715
96. Mukku V.R., and Stancel G.M. Regulation of epidermal growth factor receptor by estrogen. J. Biol. Chem. 260 (1985) 9820-9824
97. Murphy L.J., Seneviratne C., Moreira P., and Reid R.E. Enhanced expression of insulin-like growth factor-binding protein-I in the fasted rat: the effects of insulin and growth hormone administration. Endocrinology 128 (1991) 689-696
98. Nadler R.D. A biphasic influence of progesterone on sexual receptivity of spayed female rats. Physiol. Behav. 5 (1970) 95-97
99. Naftolin F., Mor G., Horvath T.L., Luquin S., Fajer A.B., Kohen F., and Garcia-Segura L.M. Synaptic remodeling in the arcuate nucleus during the estrous cycle is induced by estrogen and precedes the preovulatory gonadotropin surge. Endocrinology 137 (1996) 5576-5580
100. Nestler E.J., and Greengard P. Protein phosphorylation in the brain. Nature 305 (1983) 583-588
101. Nestler E.J., Walaas S.I., and Greengard P. Neuronal phosphoproteins: physiological and clinical implications. Science 225 (1984) 1357-1364
102. Niblock M.M., Brunso-Bechtold J.K., and Riddle D.R. Insulin-like growth factor I stimulates dendritic growth in primary somatosensory cortex. J. Neurosci. 20 (2000) 4165-4176
103. O'Dowd B.F., Nguyen T., Marchese A., Cheng R., Lynch K.R., Heng H.H., Kolakowski Jr. L.F., and George S.R. Discovery of three novel G-protein-coupled receptor genes. Genomics 47 (1998) 310-313
104. Ojeda S.R., Ma Y.J., Lee B.J., and Prevot V. Glia-to-neuron signaling and the neuroendocrine control of female puberty. Recent Prog. Horm. Res. 55 (2000) 197-223 discussion 223-224
105. Olmos G., Aguilera P., Tranque P., Naftolin F., and Garcia-Segura L.M. Estrogen-induced synaptic remodelling in adult rat brain is accompanied by the reorganization of neuronal membranes. Brain Res. 425 (1987) 57-64
106. Olmos G., Naftolin F., Perez J., Tranque P.A., and Garcia-Segura L.M. Synaptic remodeling in the rat arcuate nucleus during the estrous cycle. Neuroscience 32 (1989) 663-667
107. Owman C., Blay P., Nilsson C., and Lolait S.J. Cloning of human cDNA encoding a novel heptahelix receptor expressed in Burkitt's lymphoma and widely distributed in brain and peripheral tissues. Biochem. Biophys. Res. Commun. 228 (1996) 285-292
108. Parducz A., Szilagyi T., Hoyk S., Naftolin F., and Garcia-Segura L.M. Neuroplastic changes in the hypothalamic arcuate nucleus: the estradiol effect is accompanied by increased exoendocytotic activity of neuronal membranes. Cell Mol. Neurobiol. 16 (1996) 259-269
109. Petitti N., Karkanias G.B., and Etgen A.M. Estradiol selectively regulates alpha 1B-noradrenergic receptors in the hypothalamus and preoptic area. J. Neurosci. 12 (1992) 3869-3876
110. Pfaff D., Ogawa S., Kia K., Vasudevan N., Krebs C., Frohlich J., and Kow L.-M. Genetic mechanisms in neural and hormonal controls over female reproductive behaviors. In: Pfaff D.W., Arnold A.P., Etgen A.M., Fahrbach S.E., and Rubin R.T. (Eds). Hormones, Brain and Behavior Vol. 3 (2002), Academic Press, San Diego, CA 441-510
111. Pfaff D.W., Sakuma Y., Kow L.M., Lee A.W.L., and Easton A. Hormonal, neural, and genomic mechanisms for female reproductive behaviors. In: Neill J.D. (Ed). Knobil and Neill's Physiology of Reproduction Vol. 2 (2006), Academic Press, San Diego, CA 1825-1920
112. Pfaff D.W., Schwartz-Giblin S., McCarthy M.M., and Kow L.M. Cellular and molecular mechanisms of female reproductive behaviors. In: Knobil E., and Neill J.D. (Eds). The Physiology of Reproduction Vol. 2 (1994), Raven Press, New York 107-220
113. Pfaus J.G., Pendleton N., and Gorzalka B.B. Dual effect of morphiceptin on lordosis behavior: possible mediation by different opioid receptor subtypes. Pharmacol. Biochem. Behav. 24 (1986) 1461-1464
114. Pfaus J.G., and Pfaff D.W. Mu-, delta-, and kappa-opioid receptor agonists selectively modulate sexual behaviors in the female rat: differential dependence on progesterone. Horm. Behav. 26 (1992) 457-473
115. Pierson-Mullany L.K., Skildum A., Faivre E., and Lange C.A. Cross-talk between growth factor and progesterone receptor signaling pathways: implications for breast cancer cell growth. Breast Dis. 18 (2003) 21-31
116. Pietrzkowski Z., Wernicke D., Porcu P., Jameson B.A., and Baserga R. Inhibition of cellular proliferation by peptide analogues of insulin-like growth factor 1. Cancer Res. 52 (1992) 6447-6451
117. Piwien-Pilipuk G., Huo J.S., and Schwartz J. Growth hormone signal transduction. J. Pediatr. Endocrinol. Metab 15 (2002) 771-786
118. Poletti A., Coscarella A., Negri-Cesi P., Colciago A., Celotti F., and Martini L. 5 alpha-reductase isozymes in the central nervous system. Steroids 63 (1998) 246-251
119. Qiu M., Olsen A., Faivre E., Horwitz K.B., and Lange C.A. Mitogen-activated protein kinase regulates nuclear association of human progesterone receptors. Mol. Endocrinol. 17 (2003) 628-642
120. Quesada A., and Etgen A.M. Insulin-like growth factor-1 regulation of alpha(1)-adrenergic receptor signaling is estradiol dependent in the preoptic area and hypothalamus of female rats. Endocrinology 142 (2001) 599-607
121. Quesada A., and Etgen A.M. Functional interactions between estrogen and insulin-like growth factor-I in the regulation of alpha 1B-adrenoceptors and female reproductive function. J. Neurosci. 22 (2002) 2401-2408
122. Rao K.V., Peralta W.D., Greene G.L., and Fox C.F. Cellular progesterone receptor phosphorylation in response to ligands activating protein kinases. Biochem. Biophys. Res. Commun. 146 (1987) 1357-1365
123. Rupprecht R., Reul J.M., Trapp T., van Steensel B., Wetzel C., Damm K., Zieglgansberger W., and Holsboer F. Progesterone receptor-mediated effects of neuroactive steroids. Neuron 11 (1993) 523-530
124. Schwartz S.M., Blaustein J.D., and Wade G.N. Inhibition of estrous behavior by progesterone in rats: role of neural estrogen and progestin receptors. Endocrinology 105 (1979) 1078-1082
125. Shen T., Horwitz K.B., and Lange C.A. Transcriptional hyperactivity of human progesterone receptors is coupled to their ligand-dependent down-regulation by mitogen-activated protein kinase-dependent phosphorylation of serine 294. Mol. Cell Biol. 21 (2001) 6122-6131
126. Simoncini T., Hafezi-Moghadam A., Brazil D.P., Ley K., Chin W.W., and Liao J.K. Interaction of oestrogen receptor with the regulatory subunit of phosphatidylinositol-3-OH kinase. Nature 407 (2000) 538-541
127. Singh M. Ovarian hormones elicit phosphorylation of Akt and extracellular-signal regulated kinase in explants of the cerebral cortex. Endocrine 14 (2001) 407-415
128. Singh M., Setalo Jr. G., Guan X., Warren M., and Toran-Allerand C.D. Estrogen-induced activation of mitogen-activated protein kinase in cerebral cortical explants: convergence of estrogen and neurotrophin signaling pathways. J. Neurosci. 19 (1999) 1179-1188
129. Sjogren K., Liu J.L., Blad K., Skrtic S., Vidal O., Wallenius V., LeRoith D., Tornell J., Isaksson O.G., Jansson J.O., and Ohlsson C. Liver-derived insulin-like growth factor I (IGF-I) is the principal source of IGF-I in blood but is not required for postnatal body growth in mice. Proc. Natl. Acad Sci. U S A 96 (1999) 7088-7092
130. Skildum A., Faivre E., and Lange C.A. Progesterone receptors induce cell cycle progression via activation of mitogen-activated protein kinases. Mol. Endocrinol. 19 (2005) 327-339
131. Smith H.E., Smith R.G., Toft D.O., Neergaard J.R., Burrows E.P., and O'Malley B.W. Binding of steroids to progesterone receptor proteins in chick oviduct and human uterus. J. Biol. Chem. 249 (1974) 5924-5932
132. Soh J.W., Mao Y., Liu L., Thompson W.J., Pamukcu R., and Weinstein I.B. Protein kinase G activates the JNK1 pathway via phosphorylation of MEKK1. J. Biol. Chem. 276 (2001) 16406-16410
133. Soldani R., Cagnacci A., and Yen S.S. Insulin, insulin-like growth factor I (IGF-I) and IGF-II enhance basal and gonadotrophin-releasing hormone-stimulated luteinizing hormone release from rat anterior pituitary cells in vitro. Eur. J. Endocrinol. 131 (1994) 641-645
134. Stancel G.M., Gardner R.M., Kirkland J.L., Lin T.H., Lingham R.B., Loose-Mitchell D.S., Mukku V.R., Orengo C.A., and Verner G. Interactions between estrogen and EGF in uterine growth and function. Adv. Exp. Med. Biol. 230 (1987) 99-118
135. Thomas P., Zhu Y., and Pace M. Progestin membrane receptors involved in the meiotic maturation of teleost oocytes: a review with some new findings. Steroids 67 (2002) 511-517
136. Topalli I., and Etgen A.M. Insulin-like growth factor-I receptor and estrogen receptor crosstalk mediates hormone-induced neurite outgrowth in PC12 cells. Brain Res. 1030 (2004) 116-124
137. Toran-Allerand C.D. Novel sites and mechanisms of oestrogen action in the brain. Novartis Found Symp. 230 (2000) 56-69 discussion 69-73.
138. Toran-Allerand C.D., Ellis L., and Pfenninger K.H. Estrogen and insulin synergism in neurite growth enhancement in vitro: mediation of steroid effects by interactions with growth factors?. Brain Res. 469 (1988) 87-100
139. Toran-Allerand C.D., Singh M., and Setalo Jr. G. Novel mechanisms of estrogen action in the brain: new players in an old story. Front. Neuroendocrinol. 20 (1999) 97-121
140. Tsai M.J., and O'Malley B.W. Molecular mechanisms of action of steroid/thyroid receptor superfamily members. Annu. Rev. Biochem. 63 (1994) 451-486
141. Underwood L.E., Clemmons D.R., Maes M., D'Ercole A.J., and Ketelslegers J.M. Regulation of somatomedin-C/insulin-like growth factor I by nutrients. Horm. Res. 24 (1986) 166-176
142. Varshavsky A. Regulated protein degradation. Trends Biochem. Sci. 30 (2005) 283-286
143. Voigt P., Ma Y.J., Gonzalez D., Fahrenbach W.H., Wetsel W.C., Berg-von der Emde K., Hill D.F., Taylor K.G., Costa M.E., Seidah N.G., and Ojeda S.R. Neural and glial-mediated effects of growth factors acting via tyrosine kinase receptors on luteinizing hormone-releasing hormone neurons. Endocrinology 137 (1996) 2593-2605
144. Wade G.N., and Jones J.E. Neuroendocrinology of nutritional infertility. Am. J. Physiol. Regul. Integr. Comp. Physiol. 287 (2004) R1277-R1296
145. Watters J.J., Campbell J.S., Cunningham M.J., Krebs E.G., and Dorsa D.M. Rapid membrane effects of steroids in neuroblastoma cells: effects of estrogen on mitogen activated protein kinase signalling cascade and c-fos immediate early gene transcription. Endocrinology 138 (1997) 4030-4033
146. Weesner G.D., Krey L.C., and Pfaff D.W. Alpha 1 adrenergic regulation of estrogen-induced increases in luteinizing hormone-releasing hormone mRNA levels and release. Brain Res. Mol. Brain Res. 17 (1993) 77-82
147. Woolley C.S. Estrogen-mediated structural and functional synaptic plasticity in the female rat hippocampus. Horm. Behav. 34 (1998) 140-148
148. Zhang Y., Beck C.A., Poletti A., Clement J.P.t., Prendergast P., Yip T.T., Hutchens T.W., Edwards D.P., and Weigel N.L. Phosphorylation of human progesterone receptor by cyclin-dependent kinase 2 on 3 sites that are authentic basal phosphorylation sites in vivo. Mol. Endocrinol. 11 (1997) 823-832
149. Zhang Y., Beck C.A., Poletti A., Edwards D.P., and Weigel N.L. Identification of phosphorylation sites unique to the B form of human progesterone receptor. In vitro phosphorylation by casein kinase II. J. Biol. Chem. 269 (1994) 31034-31040
150. Zhu Y., Bond J., and Thomas P. Identification, classification, and partial characterization of genes in humans and other vertebrates homologous to a fish membrane progestin receptor. P. Natl. Acad. Sci. USA 100 (2003) 2237-2242
151. Zhu Y., Rice C.D., Pang Y., Pace M., and Thomas P. Cloning, expression, and characterization of a membrane progestin receptor and evidence it is an intermediary in meiotic maturation of fish oocytes. P. Natl. Acad. Sci. USA 100 (2003) 2231-2236
152. Zucker I., and Goy R.W. Sexual receptivity in the guinea pig: inhibitory and faciltatory actions of progesterone and related compounds. J. Comp. Physiol. Psychol. 64 (1967) 378-383