Interaction of insulin-like growth factor-I and estradiol signaling pathways on hypothalamic neuronal differentiation

Neuroscience

Volumn 74, Issue 2, 1996, Pages 531-539

  Duenas M ^a   Torres Aleman, I ^a   Naftolin, F ^b   Garcia Segura, L M ^a  

^a INSTITUTO CAJAL   (Spain)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

estrogen receptor; ICI 182,780; microtubule associated protein 2; neuronal survival; sex steroids; trophic factors

Indexed keywords

ANTISENSE OLIGONUCLEOTIDE; ESTRADIOL; ESTROGEN RECEPTOR; FULVESTRANT; MESSENGER RNA; MICROTUBULE ASSOCIATED PROTEIN 2; SOMATOMEDIN C;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; CONTROLLED STUDY; FEMALE; FETUS; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; MORPHOMETRICS; NERVE CELL CULTURE; NERVE CELL DIFFERENTIATION; NERVE CELL GROWTH; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION;

EID: 0030593428     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/0306-4522(96)00142-X     Document Type: Article

References (86)

1. Ang L. C., Bhaumick B., Juurlink B. H. J. Neurite promoting activity of insulin, insulin-like growth factor I and nerve growth factor on spinal motoneurons is astrocyte dependent. Devl Brain Res. 74:1993;83-88.
2. Arimatsu Y., Hatanada H. Estrogen treatment enhances survival of cultured fetal rat amygdala neurons in a defined medium. Devl Brain Res. 26:1986;151-159.
3. Aronica S. M., Katzenellenbogen B. S. Progesterone receptor regulation in uterine cells: stimulation by estrogen, cyclic adenosine 3′,5′-monophosphate, and insulin-like growth factor I and supression by antiestrogens and protein kinase inhibitors. Endocrinology. 128:1991;2045-2052.
4. Aronica S. M., Katzenellenbogen B. S. Stimulation of estrogen receptor-mediated transcription and alteration in the phosphorylation state of the rat uterine estrogen receptor by estrogen, cyclic adenosine monophosphate, and insulin-like growth factor-I. Molec. Endocr. 7:1993;743-752.
5. Beato M. Gene regulation by steroid hormones. Cell. 56:1989;335-344.
6. Black M. M., Baas P. W. The basis of polarity in neurons. Trends Neurosci. 12:1989;211-214.
7. Bondy C., Werner H., Roberts C. T., LeRoith D. Cellular pattern of type-I insulin-like growth factor receptor gene expression during maturation of the rat brain: comparison with insulin-like growth factors I and II. Neuroscience. 46:1992;909-923.
8. Caceres A., Kosik K. S. Inhibition of neurite polarity by tau antisense oligonucleotides in primary cerebellar neurons. Nature. 343:1990;461-462.
9. Castro-Alamancos M. A., Torres-Aleman I. Learning of the conditioned eye-blink response is impaired by an antisense insulin-like growth factor I oligonucleotide. Proc. natn. Acad. Sci. U.S.A. 91:1994;10203-10207.
10. Cho H., Aronica S. M., Katzenellenbogen B. S. Regulation of progesterone receptor gene expression in MCF-7 breast cancer cells: a comparison of the effects of cyclic adenosine 3′,5′-monophosphate, estradiol, insulin-like growth factor I, and serum factors. Endocrinology. 134:1994;658-664.
11. Chowen J. A., Torres-Aleman I., Garcia-Segura L. M. Trophic effects of estradiol on fetal rat hypothalamic neurons. Neuroendocrinology. 56:1992;895-901.
12. Constantino C. X., Keyes P. L., Kostyo J. L. Insulin-like growth factor-I stimulates steroidogenesis in rabbit luteal cells. Endocrinology. 128:1991;1702-1708.
13. DeVoogd T., Nottebohm F. Gonadal hormones induce dendritic growth in the adult avian brain. Science. 214:1981;202-204.
14. Díaz H., Lorenzo A., Carrer H. F., Cáceres A. Time lapse study of neurite growth in hypothalamic dissociated neurons in culture: sex differences and estrogen effects. J. Neurosci. Res. 33:1992;266-281.
15. Dickson R. B., McManaway M. E., Lippman M. E. Estrogen-induced factors of breast cancer cells partially replace estrogen to promote tumor growth. Science. 232:1986;1540-1543.
16. Dueñas M., Luquin S., Chowen J. A., Torres-Aleman I., Naftolin F., Garcia-Segura L. M. Gonadal hormone regulation of insulin-like growth factor-I-like immunoreactivity in hypothalamic astroglia of developing and adult rats. Neuroendocrinology. 59:1994;528-538.
17. Erickson G. F., Garzo V. G., Magoffin D. A. Insulin-like growth factor-I (IGF-I) regulates aromatase activity in human granulosa and granulosa luteal cells. J. clin. Endocr. Metab. 69:1989;716-724.
18. Evans R. M. The steroid and thyroid hormone receptor superfamily. Science. 240:1988;889-895.
19. Faivre-Bauman A., Rosenbau E., Puymirat J., Grousell D., Tixier-Vidal A. Differentiation of fetal mouse hypothalamic cells in serum-free medium. Devl Neurosci. 4:1981;118-119.
20. Ferreira A., Busciglio J., Caceres A. Microtubule formation and neurite growth in cerebellar macroneurons which develop in vitro: evidence for the involvement of the microtubule-associated proteins MAP-1a, HMW-MAP-2, and Tau. Devl Brain Res. 49:1989;215-228.
21. Ferreira A., Cáceres A. Estrogen-enhanced neurite growth: evidence for a selective induction of tau and stable microtubules. J. Neurosci. 11:1991;392-400.
22. Freiss G., Prebois C., Rochefort H., Vignon F. Anti-steroidal and anti-growth factor activities of anti-estrogens. J. Steroid Biochem. molec. Biol. 37:1990;777-781.
23. Gahary A., Chakrabarti S., Murphy L. J. Localization of the sites of synthesis and action of insulin-like growth factor-1 in the rat uterus. Molec. Endocr. 4:1990;191-195.
24. Gahr M., Konishi M. Developmental changes in estrogen sensitive neurons in the forebrain of the zebra finch. Proc. natn. Acad. Sci. U.S.A. 85:1988;7380-7383.
25. Garcia-Segura L. M., Pérez J., Pons S., Rejas M. T., Torres-Aleman I. Localization of insulin-like growth factor I (IGF-I)-like immunoreactivity in the developing and adult rat brain. Brain Res. 560:1991;167-174.
26. Garcia-Segura L. M., Chowen J. A., Párducz A., Naftolin F. Gonadal hormones as promoters of structural synaptic plasticity: cellular mechanisms. Prog. Neurobiol. 44:1994;279-307.
27. Garcia-Segura L. M., Cañas B., Parducz A., Rougon G., Theodosis D., Naftolin F., Torres-Aleman I. Estradiol promotion of changes in the morphology of astroglia growing in culture depends on the expression of polysialic acid on neural membranes. Glia. 13:1995;209-216.
28. Garcia-Segura L. M., Dueñas M., Busiguina S., Naftolin F., Chowen J. A. Gonadal hormone regulation of neuronal-glial interactions in the developing neuroendocrine hypothalamus. J. Steroid Biochem. molec. Biol. 53:1995;293-298.
29. NGFR and ChAT expression in the medial septum and diagonal band of Broca. Expl Neurol. 116:1992;23-39.
30. Gibbs R. B., Wu D., Hersh L. B., Pfaff D. W. Effects of estrogen replacement on the relative levels of choline acetyltransferase, trkA, and nerve growth factor messenger RNAs in the basal forebrain and hippocampal formation of adult rats. Expl Neurol. 129:1994;70-80.
31. Guillamón A., Segovia S., del Abril A. Early effects of gonadal steroids on the neuron number of the medial posterior region of the lateral division of the bed nucleus of the stria terminalis in the rat. Devl Brain Res. 44:1988;281-290.
32. Hasegawa N., Takeo T., Sakuma Y. Differential regulation of estrogen-dependent sexual development of rat brain by growth factors. Neurosci. Lett. 123:1991;183-186.
33. Hauser K. F., Toran-Allerand C. D. Androgen increases the number of cells in fetal mouse spinal cord cultures: implications for motoneuron survival. Brain Res. 485:1989;157-162.
34. Hernandez E. R., Resnick C. E., Svoboda M. E., Van Wyk J., Payne D. W., Adashi E. Y. Somatomedin-C/insulin-like growth factor I as an enhancer of androgen biosynthesis by cultured rat ovarian cells. Endocrinology. 122:1988;1603-1612.
35. Horton R., Pasupuletti V., Antonipillai I. Androgen induction of steroid 5α-reductase may be mediated via insulin-like growth factor-I. Endocrinology. 133:1993;447-451.
36. Huff K. K., Kaufman D., Gabbay K. H., Spencer E. M., Lippman M. E., Dickson R. B. Secretion of an insulin-like growth factor-I related protein by human breast cancer cells. Cancer Res. 46:1986;4613-4619.
37. Ignar-Trowbridge D. M., Teng C. T., Ross K. A., Parker M. G., Korach K. S., McLachlan J. A. Peptide growth factors elicit estrogen receptor-dependent transcriptional activation of an estrogen-responsive element. Molec. Endocr. 7:1993;992-998.
38. Kapur S., Tamada H., Dey S. K., Andrews G. K. Expression of insulin-like growth factor-I (IGF-I) and its receptor in the peri-implantation mouse uterus, and cell-specific regulation of IGF-I gene expression by estradiol and progesterone. Biol. Reprod. 46:1992;208-219.
39. Kato S., Endoh H., Masuhiro Y., Kitamoto T., Uchiyama S., Sasaki H., Masushige S., Gotoh Y., Nishida E., Kawashima H., Metzger D., Chambon P. Activation of the estrogen receptor through phosphorylation by mitogen-activated protein kinase. Science. 270:1995;1491-1494.
40. Katzenellenbogen B. S., Norman M. J. Multihormonal regulation of the progesterone receptor in MCF-7 human breast cancer cells: interrelationships among insulin/insulin-like growth factor-I, serum, and estrogen. Endocrinology. 126:1990;891-898.
41. Krywicki R. F., Figueroa J. A., Jackson J. G., Kozelsky T. W., Shimasaki S., Von Hoff D. D., Yee D. Regulation of insulin-like growth factor binding proteins in ovarian cancer cells by oestrogen. Eur. J. Cancer. 29A:1993;2015-2019.
42. Kurz E. M., Sengelaub D. R., Arnold A. P. Androgens regulate the dendritic length of mammalian motoneurons in adulthood. Science. 232:1986;395-398.
43. Lenoir D., Honegger P. Insulin-like growth factor I stimulates DNA synthesis in fetal rat brain cell cultures. Devl Brain Res. 7:1983;205-213.
44. Lin T., Haskel J., Vinson N., Terracio L. Direct stimulatory effects of insulin-like growth factor-I on Leydig cell steroidogenesis in primary culture. Biochem. biophys. Res. Commun. 137:1986;950-956.
45. Lorenzo A., Díaz H., Carrer H., Cáceres A. Amygdala neurons in vitro: neurite growth and effects of estradiol. J. Neurosci. Res. 33:1992;418-435.
46. Ma Y. J., Junier M. P., Costa M. E., Ojeda S. R. Transforming growth factor-α gene expression in the hypothalamus is developmentally regulated and linked to sexual maturation. Neuron. 9:1992;657-670.
47. Ma Z. Q., Santagati S., Patrone C., Pollio G., Vegeto E., Maggi A. Insulin-like growth factors activate estrogen receptor to control the growth and differentiation of the human neuroblastoma cell line SK-ER3. Molec. Endocr. 8:1994;910-918.
48. Matsumoto A. Synaptogenic action of sex steroids in developing and adult neuroendocrine brain. Psychoneuroendocrinology. 16:1991;25-40.
49. Matus A. Microtubule associated proteins and neuronal morphogenesis. J. Cell Sci. 15(Suppl):1991;61-67.
50. McCarthy M. M., Schlenker E. H., Pfaff D. W. Enduring consequences of neonatal treatment with antisense oligodeoxynucleotides to estrogen receptor messenger ribonucleic acid on sexual differentiation of rat brain. Endocrinology. 133:1993;433-439.
51. Meisel R. L., Luttrell W. R. Estradiol increases the dendritic length of ventromedial hypothalamic neurons in female Syrian hamsters. Brain Res. Bull. 25:1990;165-168.
52. 125I]insulin-like growth factor-I (IGF-I) binding and IGF-I gene expression by estrogen. Endocrinology. 132:1993;23-29.
53. Miranda R. C., Sohrabji F., Toran-Allerand C. D. Presumptive estrogen target neurons express mRNAs for the neurotrophins and neurotrophin receptors: a basis for potential developmental interactions of estrogen with the neurotrophins. Molec. cell. Neurosci. 4:1993;510-525.
54. Mitchison T., Krischner M. W. Cytoskeletal dynamics and nerve growth. Neuron. 1:1988;761-772.
55. Molnar P., Murphy L. J. Effects of oestrogen on rat uterine expression of insulin-like growth factor-binding proteins. J. Molec. Endocr. 13:1994;59-67.
56. Murphy L. J., Murphy L. C., Friesen H. G. Estrogen induces insulin-like growth factor-I expression in the rat uterus. Molec. Endocr. 1:1987;445-450.
57. Naftolin F. and MacLusky N. J. (1984) Aromatization hypothesis revisited. In Sexual Differentiation of the Brain: Basic and Clinical Aspects (eds Serio M., Motta M., Zanisi M. and Martini L.), pp. 79-82. Raven Press, New York.
58. Newton C. J., Buric R., Trapp T., Brockmeier S., Pagotto U., Stalla G. K. The unligand estrogen receptor (ER) transduces growth factor signals. J. Steroid Biochem. molec. Biol. 48:1994;481-486.
59. Nieto-Bona M. P., Busiguina S., Torres-Aleman I. Insulin-like growth factor I is an afferent trophic signal that modulates calbindin-28kD in adult Purkinje cells. J. Neurosci. Res. 42:1995;371-376.
60. Nordeen E. J., Nordeen K. W., Sengelaub D. R., Arnold A. P. Androgens prevent normally occurring cell death in a sexually dimorphic spinal nucleus. Science. 229:1985;671-673.
61. Owens P. C., Gill P. G., De Young N. J., Weger M. A., Knowels S. E., Moyse K. J. Estrogen and progesterone regulate secretion of insulin-like growth factor binding proteins by human breast cancer cells. Biochem. biophys. Res. Commun. 193:1993;467-473.
62. Parker M. G., Arbuckle N., Dauvois S., Danielian P., White R. Structure and function of the estrogen receptor. Ann. N. Y. Acad. Sci. 684:1993;119-126.
63. Pons S., Torres-Aleman I. Estradiol modulates insulin-like growth factor I receptors and binding proteins in neurons from the hypothalamus. J. Neuroendocr. 5:1993;267-271.
64. Pons S., Rejas M. T., Torres-Aleman I. Ontogeny of insulin-like growth factor I, its receptor, and its binding proteins in the rat hypothalamus. Devl Brain Res. 62:1991;169-175.
65. Sahlin L., Norstedt G., Eriksson H. Estrogen regulation of the estrogen receptor and insulin-like growth factor-I in the rat uterus: a potential coupling between effects of estrogen and IGF-I. Steroids. 59:1994;421-430.
66. Sengelaub D. R., Arnold A. P. Hormonal control of neuron number in sexually dimorphic spinal nuclei of the rat. I. Testosterone-regulated death in the dorsolateral nucleus. J. comp. Neurol. 280:1989;622-629.
67. Sengelaub D. R., Jordan C. L., Kurz E. M., Arnold A. P. Hormonal control of neuron number in sexually dimorphic spinal nuclei of the rat. II. Development of the spinal nucleus of the bulbocavernosus in androgen-insensitive (Tfm) rats. J. comp. Neurol. 280:1989;630-636.
68. Sengelaub D. R., Nordeen E. J., Nordeen K. W., Arnold A. P. Hormonal control of neuron number in sexually dimorphic spinal nuclei of the rat. III. Differential effects of androgen dihydrotestosterone. J. comp. Neurol. 280:1989;637-644.
69. Simmen R. C. M., Simmen F. A., Hofig A., Farmer S. J., Bazer F. W. Hormonal regulation of insulin-like growth factor gene expression in pig uterus. Endocrinology. 127:1990;2166-2174.
70. Sohrabji F., Greene L. A., Miranda R. C., Toran-Allerand D. Reciprocal regulation of estrogen and NGF receptors by their ligands in PC12 cells. J. Neurobiol. 25:1994;974-988.
71. Sohrabji F., Miranda C., Toran-Allerand C. D. Estrogen differentially regulates estrogen and nerve growth factor receptor mRNA in adult sensory neurons. J. Neurosci. 14:1994;459-471.
72. Thorsen T., Lahood H., Rasmussen M., Aakvaag A. Estradiol treatment increases the sensitivity of MCF-7 cells for the growth stimulatory effect of IGF-1. J. Steroid Biochem. molec. Biol. 41:1992;537-540.
73. Toran-Allerand C. D. Sex steroids and the development of the newborn mouse hypothalamus and preoptic area in vitro: implications for sexual differentiation. Brain Res. 106:1976;407-412.
74. Toran-Allerand C. D., Bentham W., Miranda R. C., Anderson J. P. Insulin influences astroglial morphology and glial fibrillary acidic protein (GFAP) expression in organotypic cultures. Brain Res. 558:1991;296-304.
75. Toran-Allerand C. D., Ellis L., Pfenninger K. H. Estrogen and insulin synergism in neurite growth enhancement in vitro: mediation of steroid effects by interactions with growth factors? Devl Brain Res. 41:1988;87-100.
76. Toran-Allerand C. D., Hashimoto K., Greenough W. T., Saltarelli N. Sex steroids and the development of the newborn mouse hypothalamus in vitro: III. Effects of estrogen on dendritic differentiation. Devl Brain Res. 7:1983;97-101.
77. Toran-Allerand C. D., Miranda R. C., Bentham W., Sohrabji F., Brown E. J., Hochberg R. B., MacLusky N. J. Estrogen receptors co-localize with low-affinity NGF receptors in cholinergic neurons of the basal forebrain. Proc. natn. Acad. Sci. U.S.A. 89:1992;4668-4672.
78. Torres-Aleman I., Naftolin F., Robbins R. J. Trophic effect of insulin-like growth factor-I on fetal rat hypothalamic cells in culture. Neuroscience. 35:1990;601-608.
79. Torres-Aleman I., Pons S., Santos-Benito F. F. Survival of Purkinje cells in cerebellar cultures is increased by insulin-like growth factor I. Eur. J. Neurosci. 4:1992;864-869.
80. Umayahara Y., Kawamori R., Watada H., Imano E., Iwama N., Morishima T., Yamasaki Y., Kajimoto Y., Kamada T. Estrogen regulation of the insulin-like growth factor I gene transcription involves an AP-1 enhancer. J. biol. Chem. 269:1994;16433-16442.
81. Van der Burg B., Ruttermann G. R., Blankenstein M. A., de Laat S. W., van Zoelen E. J. J. Mitogenic stimulation of human breast cancer cells in a growth factor defined medium: synergistic action of insulin and estrogen. J. Cell Physiol. 123:1988;101-108.
82. Wade G. N., Blaustein J. D., Gray J. M., Meredith J. M. ICI 182,780: a pure antiestrogen that affects behaviors and energy balance in rats without acting in the brain. Am. J. Physiol. 265:1993;R1392-R1398.
83. Wimalasena J., Meehan D., Dostal R., Foster J. S., Cameron M., Smith M. Growth factors interact with estradiol and gonadotrophins in the regulation of ovarian cancer cell growth and growth factor receptors. Oncol. Res. 5:1993;325-337.
84. Wosikowski K., Kung W., Hasmann M., Loser R., Eppenberger U. Inhibition of growth-factor-activated proliferation by anti-estrogens and effects on early gene expression of MCF-7 cells. Int. J. Cancer. 53:1993;290-297.
85. Wright L. L., Marchetti D., Perez-Polo J. R. Effects of gonadal steroids on nerve growth factor receptors in sympathetic and sensory ganglia of neonatal rats. Int. J. devl Neurosci. 6:1988;217-222.
86. Yallampalli C., Rajaraman S., Nagamani M. Insulin-like growth factor binding proteins in the rat uterus and their regulation by oestradiol and growth hormone. J. Reprod. Fert. 97:1993;501-505.