Skip to main content
Top
Published in: Pediatric Nephrology 3/2005

01-03-2005 | Review

Genomic and non-genomic actions of sex steroids in the growth plate

Authors: Marcel Karperien, Bram C. J. van der Eerden, Jan Maarten Wit

Published in: Pediatric Nephrology | Issue 3/2005

Login to get access

Abstract

Sex steroids, and particularly estrogens, are important regulators of bone growth and bone mass accrual. For a long time, it was thought that these effects were mainly caused by their modulatory effects on the somatotrophic axis. Data gathered in the past years have challenged this view and it is now widely accepted that many of the effects of sex steroids on growth and bone mass accrual are caused by direct effects on target cells in the growth plate and bone. This review summarizes and discusses some of our latest findings on the expression of sex steroid receptors in the growth plate, the source of the ligands activating these receptors, and their putatitive mechanism of action predominantly focusing on observations in the rat.
Literature
1.
go back to reference Smith EP, Boyd J, Frank GR, Takahashi H, Cohen RM, Specker B, Williams TC, Lubahn DB, Korach KS (1994) Estrogen resistance caused by a mutation in the estrogen-receptor gene in a man. N Engl J Med 331:1056–1060CrossRefPubMed Smith EP, Boyd J, Frank GR, Takahashi H, Cohen RM, Specker B, Williams TC, Lubahn DB, Korach KS (1994) Estrogen resistance caused by a mutation in the estrogen-receptor gene in a man. N Engl J Med 331:1056–1060CrossRefPubMed
2.
go back to reference Morishima A, Grumbach MM, Simpson ER, Fisher C, Qin K (1995) Aromatase deficiency in male and female siblings caused by a novel mutation and the physiological role of estrogens. J Clin Endocrinol Metab 80:3689–3698CrossRefPubMed Morishima A, Grumbach MM, Simpson ER, Fisher C, Qin K (1995) Aromatase deficiency in male and female siblings caused by a novel mutation and the physiological role of estrogens. J Clin Endocrinol Metab 80:3689–3698CrossRefPubMed
3.
go back to reference Carani C, Qin K, Simoni M, Faustini-Fustini M, Serpente S, Boyd J, Korach KS, Simpson ER (1997) Effect of testosterone and estradiol in a man with aromatase deficiency. N Engl J Med 337:91–95CrossRefPubMed Carani C, Qin K, Simoni M, Faustini-Fustini M, Serpente S, Boyd J, Korach KS, Simpson ER (1997) Effect of testosterone and estradiol in a man with aromatase deficiency. N Engl J Med 337:91–95CrossRefPubMed
4.
go back to reference Grumbach MM (2001) Estrogen, bone, growth and sex: a sea change in conventional wisdom. J Pediatr Endocrinol Metab 13 [Suppl 6]:1439–1455 Grumbach MM (2001) Estrogen, bone, growth and sex: a sea change in conventional wisdom. J Pediatr Endocrinol Metab 13 [Suppl 6]:1439–1455
5.
go back to reference Juul A (2001) The effects of oestrogens on linear bone growth. Hum Reprod Update 7:303–313CrossRef Juul A (2001) The effects of oestrogens on linear bone growth. Hum Reprod Update 7:303–313CrossRef
6.
go back to reference Veldhuis JD (1998) Neuroendocrine control of pulsatile growth hormone release in the human: relationship with gender. Growth Horm IGF Res 8 [Suppl B]:49–59 Veldhuis JD (1998) Neuroendocrine control of pulsatile growth hormone release in the human: relationship with gender. Growth Horm IGF Res 8 [Suppl B]:49–59
7.
go back to reference Martha PM Jr, Gorman KM, Blizzard RM, Rogol AD, Veldhuis JD (1992) Endogenous growth hormone secretion and clearance rates in normal boys, as determined by deconvolution analysis: relationship to age, pubertal status, and body mass. J Clin Endocrinol Metab 74:336–344CrossRef Martha PM Jr, Gorman KM, Blizzard RM, Rogol AD, Veldhuis JD (1992) Endogenous growth hormone secretion and clearance rates in normal boys, as determined by deconvolution analysis: relationship to age, pubertal status, and body mass. J Clin Endocrinol Metab 74:336–344CrossRef
8.
go back to reference Metzger DL, Kerrigan JR (1993) Androgen receptor blockade with flutamide enhances growth hormone secretion in late pubertal males: evidence for independent actions of estrogen and androgen. J Clin Endocrinol Metab 76:1147–1152CrossRef Metzger DL, Kerrigan JR (1993) Androgen receptor blockade with flutamide enhances growth hormone secretion in late pubertal males: evidence for independent actions of estrogen and androgen. J Clin Endocrinol Metab 76:1147–1152CrossRef
9.
go back to reference Attie KM, Ramirez NR, Conte FA, Kaplan SL, Grumbach MM (1990) The pubertal growth spurt in eight patients with true precocious puberty and growth hormone deficiency: evidence for a direct role of sex steroids. J Clin Endocrinol Metab 71:975–983 Attie KM, Ramirez NR, Conte FA, Kaplan SL, Grumbach MM (1990) The pubertal growth spurt in eight patients with true precocious puberty and growth hormone deficiency: evidence for a direct role of sex steroids. J Clin Endocrinol Metab 71:975–983
10.
go back to reference Ren SG, Malozowski S, Sanchez P, Sweet DE, Loriaux DL, Cassorla F (1989) Direct administration of testosterone increases rat tibial epiphyseal growth plate width. Acta Endocrinol (Copenh) 121:401–405 Ren SG, Malozowski S, Sanchez P, Sweet DE, Loriaux DL, Cassorla F (1989) Direct administration of testosterone increases rat tibial epiphyseal growth plate width. Acta Endocrinol (Copenh) 121:401–405
11.
go back to reference Jansson JO, Eden S, Isaksson O (1983) Sites of action of testosterone and estradiol on longitudinal bone growth. Am J Physiol 244:E135–E140 Jansson JO, Eden S, Isaksson O (1983) Sites of action of testosterone and estradiol on longitudinal bone growth. Am J Physiol 244:E135–E140
12.
go back to reference Gevers EF, Wit JM, Robinson ICAF (1995) Effect of gonadectomy on growth and GH responsiveness in dwarf rats. J Endocrinol 145:69–79 Gevers EF, Wit JM, Robinson ICAF (1995) Effect of gonadectomy on growth and GH responsiveness in dwarf rats. J Endocrinol 145:69–79
13.
go back to reference Tanner JM (1962) Growth at adolescence. Blackwell, Oxford, pp 223–239 Tanner JM (1962) Growth at adolescence. Blackwell, Oxford, pp 223–239
14.
go back to reference Kusec V, Virdi AS, Prince R, Triffitt JT (1998) Localization of estrogen receptor-alpha in human and rabbit skeletal tissues. J Clin Endocrinol Metab 83:2421–2428CrossRef Kusec V, Virdi AS, Prince R, Triffitt JT (1998) Localization of estrogen receptor-alpha in human and rabbit skeletal tissues. J Clin Endocrinol Metab 83:2421–2428CrossRef
15.
go back to reference Kennedy J, Baris C, Hoyland JA, Selby PL, Freemont AJ, Braidman IP (1999) Immunofluorescent localization of estrogen receptor-alpha in growth plates of rabbits, but not in rats, at sexual maturity. Bone 24:9–16CrossRef Kennedy J, Baris C, Hoyland JA, Selby PL, Freemont AJ, Braidman IP (1999) Immunofluorescent localization of estrogen receptor-alpha in growth plates of rabbits, but not in rats, at sexual maturity. Bone 24:9–16CrossRef
16.
go back to reference Nilsson LO, Boman A, Savendahl L, Grigelioniene G, Ohlsson C, Ritzen EM, Wroblewski J (1999) Demonstration of estrogen receptor-beta immunoreactivity in human growth plate cartilage. J Clin Endocrinol Metab 84:370–373CrossRefPubMed Nilsson LO, Boman A, Savendahl L, Grigelioniene G, Ohlsson C, Ritzen EM, Wroblewski J (1999) Demonstration of estrogen receptor-beta immunoreactivity in human growth plate cartilage. J Clin Endocrinol Metab 84:370–373CrossRefPubMed
17.
go back to reference Abu EO, Horner A, Kusec V, Triffitt JT, Compston JE (1997) The localization of androgen receptors in human bone. J Clin Endocrinol Metab 82:3493–3497CrossRefPubMed Abu EO, Horner A, Kusec V, Triffitt JT, Compston JE (1997) The localization of androgen receptors in human bone. J Clin Endocrinol Metab 82:3493–3497CrossRefPubMed
18.
go back to reference Van der Eerden BCJ, Gevers EF, Karperien M, Löwik CWGM, Wit JM (2002) Expression of estrogen receptor α and β in the epiphyseal plate of the rat. Bone 30:478–485CrossRefPubMed Van der Eerden BCJ, Gevers EF, Karperien M, Löwik CWGM, Wit JM (2002) Expression of estrogen receptor α and β in the epiphyseal plate of the rat. Bone 30:478–485CrossRefPubMed
19.
go back to reference Van der Eerden BCJ, Til NP van, Brinkmann AO, Löwik CWGM, Wit JM, Karperien M (2002) Sex differences in the expression of the androgen receptor in the tibial growth plate and metaphyseal bone of the rat. Bone 30:491–496 Van der Eerden BCJ, Til NP van, Brinkmann AO, Löwik CWGM, Wit JM, Karperien M (2002) Sex differences in the expression of the androgen receptor in the tibial growth plate and metaphyseal bone of the rat. Bone 30:491–496
20.
go back to reference Chagin AS, Lindberg MK, Andersson N, Moverare S, Gustafsson JA, Savendahl L, Ohlsson C (2004) Estrogen receptor-beta inhibits skeletal growth and has the capacity to mediate growth plate fusion in female mice. J Bone Miner Res 19:72–77 Chagin AS, Lindberg MK, Andersson N, Moverare S, Gustafsson JA, Savendahl L, Ohlsson C (2004) Estrogen receptor-beta inhibits skeletal growth and has the capacity to mediate growth plate fusion in female mice. J Bone Miner Res 19:72–77
21.
go back to reference Dohler KD, Wuttke W (1976) Circadian fluctuations of serum hormone levels in prepubertal male and female rats. Acta Endocrinol (Copenh) 83:269–279 Dohler KD, Wuttke W (1976) Circadian fluctuations of serum hormone levels in prepubertal male and female rats. Acta Endocrinol (Copenh) 83:269–279
22.
go back to reference Saksena SK, Lau IF (1979) Variations in serum androgens, estrogens, progestins, gonadotropins and prolactin levels in male rats from prepubertal to advanced age. Exp Aging Res 5:179–194 Saksena SK, Lau IF (1979) Variations in serum androgens, estrogens, progestins, gonadotropins and prolactin levels in male rats from prepubertal to advanced age. Exp Aging Res 5:179–194
23.
go back to reference Labrie C, Belanger A, Labrie F (1988) Androgenic activity of dehydroepiandrosterone and androstenedione in the rat ventral prostate. Endocrinology 123:1412–1417 Labrie C, Belanger A, Labrie F (1988) Androgenic activity of dehydroepiandrosterone and androstenedione in the rat ventral prostate. Endocrinology 123:1412–1417
24.
go back to reference Labrie F, Luu-The V, Lin SX, Simard J, Labrie C, El Alfy M, Pelletier G, Belanger A (2000) Intracrinology: role of the family of 17 beta-hydroxysteroid dehydrogenases in human physiology and disease. J Mol Endocrinol 25:1–16 Labrie F, Luu-The V, Lin SX, Simard J, Labrie C, El Alfy M, Pelletier G, Belanger A (2000) Intracrinology: role of the family of 17 beta-hydroxysteroid dehydrogenases in human physiology and disease. J Mol Endocrinol 25:1–16
25.
go back to reference Pelletier G, Labrie C, Labrie F (2000) Localization of oestrogen receptor alpha, oestrogen receptor beta and androgen receptors in the rat reproductive organs. J Endocrinol 165:359–370PubMed Pelletier G, Labrie C, Labrie F (2000) Localization of oestrogen receptor alpha, oestrogen receptor beta and androgen receptors in the rat reproductive organs. J Endocrinol 165:359–370PubMed
26.
go back to reference Simpson E, Rubin G, Clyne C, Robertson K, O’Donnell L, Jones M, Davis S (2000) The role of local estrogen biosynthesis in males and females. Trends Endocrinol Metab 11:184–188CrossRef Simpson E, Rubin G, Clyne C, Robertson K, O’Donnell L, Jones M, Davis S (2000) The role of local estrogen biosynthesis in males and females. Trends Endocrinol Metab 11:184–188CrossRef
27.
go back to reference Sasano H, Uzuki M, Sawai T, Nagura H, Matsunaga G, Kashimoto O, Harada N (1997) Aromatase in human bone tissue. J Bone Miner Res 12:1416–1423PubMed Sasano H, Uzuki M, Sawai T, Nagura H, Matsunaga G, Kashimoto O, Harada N (1997) Aromatase in human bone tissue. J Bone Miner Res 12:1416–1423PubMed
28.
go back to reference Saito H, Yanaihara T (1998) Steroid formation in osteoblast-like cells. J Int Med Res 26:1–12 Saito H, Yanaihara T (1998) Steroid formation in osteoblast-like cells. J Int Med Res 26:1–12
29.
go back to reference Janssen JM, Bland R, Hewison M, Coughtrie MW, Sharp S, Arts J, Pols HA, Leeuwen JP van (1999) Estradiol formation by human osteoblasts via multiple pathways: relation with osteoblast function. J Cell Biochem 75:528–537 Janssen JM, Bland R, Hewison M, Coughtrie MW, Sharp S, Arts J, Pols HA, Leeuwen JP van (1999) Estradiol formation by human osteoblasts via multiple pathways: relation with osteoblast function. J Cell Biochem 75:528–537
30.
go back to reference Oz OK, Millsaps R, Welch R, Welch R, Birch J, Birch J, Zerwekh JE (2001) Expression of aromatase in the human growth plate. J Mol Endocrinol 27:249–253CrossRef Oz OK, Millsaps R, Welch R, Welch R, Birch J, Birch J, Zerwekh JE (2001) Expression of aromatase in the human growth plate. J Mol Endocrinol 27:249–253CrossRef
31.
go back to reference Kartsogiannis V, Udagawa N, Ng KW, Martin TJ, Moseley JM, Zhou H (1998) Localization of parathyroid hormone-related protein in osteoclasts by in situ hybridization and immunohistochemistry. Bone 22:189–194CrossRef Kartsogiannis V, Udagawa N, Ng KW, Martin TJ, Moseley JM, Zhou H (1998) Localization of parathyroid hormone-related protein in osteoclasts by in situ hybridization and immunohistochemistry. Bone 22:189–194CrossRef
32.
go back to reference Onoe Y, Miyaura C, Ohta H, Nozawa S, Suda T (1997) Expression of estrogen receptor beta in rat bone. Endocrinology 138:4509–4512CrossRefPubMed Onoe Y, Miyaura C, Ohta H, Nozawa S, Suda T (1997) Expression of estrogen receptor beta in rat bone. Endocrinology 138:4509–4512CrossRefPubMed
33.
go back to reference Wiren KM, Zhang X, Chang C, Keenan E, Orwoll ES (1997) Transcriptional up-regulation of the human androgen receptor by androgen in bone cells. Endocrinology 138:2291–2300CrossRef Wiren KM, Zhang X, Chang C, Keenan E, Orwoll ES (1997) Transcriptional up-regulation of the human androgen receptor by androgen in bone cells. Endocrinology 138:2291–2300CrossRef
34.
go back to reference Braidman IP, Davenport LK, Carter DH, Selby PL, Mawer EB, Freemont AJ (1995) Preliminary in situ identification of estrogen target cells in bone. J Bone Miner Res 10:74–80 Braidman IP, Davenport LK, Carter DH, Selby PL, Mawer EB, Freemont AJ (1995) Preliminary in situ identification of estrogen target cells in bone. J Bone Miner Res 10:74–80
35.
go back to reference Braidman IP, Hainey L, Batra G, Selby PB, Saunders PT, Hoyland JA (2001) Localization of estrogen receptor α protein expression in adult human bone. J Bone Miner Res 16:214–220 Braidman IP, Hainey L, Batra G, Selby PB, Saunders PT, Hoyland JA (2001) Localization of estrogen receptor α protein expression in adult human bone. J Bone Miner Res 16:214–220
36.
go back to reference Noble B, Routledge J, Stevens H, Hughes I, Jacobson W (1999) Androgen receptors in bone-forming tissue. Horm Res 51:31–36CrossRef Noble B, Routledge J, Stevens H, Hughes I, Jacobson W (1999) Androgen receptors in bone-forming tissue. Horm Res 51:31–36CrossRef
37.
go back to reference Sylvia VL, Gay I, Hardin R, Dean DD, Boyan BD, Schwartz Z (2002) Rat costochondral chondrocytes produce 17beta-estradiol and regulate its production by 1alpha,25(OH)(2)D(3). Bone 30:57–63CrossRef Sylvia VL, Gay I, Hardin R, Dean DD, Boyan BD, Schwartz Z (2002) Rat costochondral chondrocytes produce 17beta-estradiol and regulate its production by 1alpha,25(OH)(2)D(3). Bone 30:57–63CrossRef
38.
go back to reference Blanchard O, Tsagris L, Rappaport R, Duval-Beaupere G, Corvol M (1991) Age-dependent responsiveness of rabbit and human cartilage cells to sex steroids in vitro. J Steroid Biochem Mol Biol 40:711–716CrossRefPubMed Blanchard O, Tsagris L, Rappaport R, Duval-Beaupere G, Corvol M (1991) Age-dependent responsiveness of rabbit and human cartilage cells to sex steroids in vitro. J Steroid Biochem Mol Biol 40:711–716CrossRefPubMed
39.
go back to reference Van der Eerden BC, Van de Ven J, Löwik CWGM, Wit JM, Karperien M (2002) Sex steroid metabolism in the tibial growth plate of the rat. Endocrinology 143:4048–4055CrossRef Van der Eerden BC, Van de Ven J, Löwik CWGM, Wit JM, Karperien M (2002) Sex steroid metabolism in the tibial growth plate of the rat. Endocrinology 143:4048–4055CrossRef
40.
go back to reference Back DJ, Breckenridge AM, Crawford FE, Giles M, Orme ML, Rowe PH (1981) The pharmacokinetics of oestrone sulphate in the rat. J Steroid Biochem 14:1045–1047CrossRef Back DJ, Breckenridge AM, Crawford FE, Giles M, Orme ML, Rowe PH (1981) The pharmacokinetics of oestrone sulphate in the rat. J Steroid Biochem 14:1045–1047CrossRef
41.
go back to reference Tanaka T, Suguro N, Kubodera A (1985) Facile radioimmunoassay of estradiol 3-sulfate in plasma during pregnancy. Clin Chem 31:1846–1848 Tanaka T, Suguro N, Kubodera A (1985) Facile radioimmunoassay of estradiol 3-sulfate in plasma during pregnancy. Clin Chem 31:1846–1848
42.
go back to reference Bilezikian JP, Morishima A, Bell J, Grumbach MM (1998) Increased bone mass as a result of estrogen therapy in a man with aromatase deficiency. N Engl J Med. 339:599–603 Bilezikian JP, Morishima A, Bell J, Grumbach MM (1998) Increased bone mass as a result of estrogen therapy in a man with aromatase deficiency. N Engl J Med. 339:599–603
43.
go back to reference Turner RT, Evans GL, Wakley GK (1994) Reduced chondroclast differentiation results in increased cancellous bone volume in estrogen-treated growing rats. Endocrinology 134:461–466CrossRef Turner RT, Evans GL, Wakley GK (1994) Reduced chondroclast differentiation results in increased cancellous bone volume in estrogen-treated growing rats. Endocrinology 134:461–466CrossRef
44.
go back to reference Wakley GK, Evans GL, Turner RT (1997) Short-term effects of high dose estrogen on tibiae of growing male rats. Calcif Tissue Int 60:37–42CrossRef Wakley GK, Evans GL, Turner RT (1997) Short-term effects of high dose estrogen on tibiae of growing male rats. Calcif Tissue Int 60:37–42CrossRef
45.
go back to reference Tobias JH, Chow J, Colston KW, Chambers TJ (1991) High concentrations of 17 beta-estradiol stimulate trabecular bone formation in adult female rats. Endocrinology 128:408–412 Tobias JH, Chow J, Colston KW, Chambers TJ (1991) High concentrations of 17 beta-estradiol stimulate trabecular bone formation in adult female rats. Endocrinology 128:408–412
46.
go back to reference Eerden BC van der, Emons J, Ahmed S, Essen HW van, Löwik CWGM, Wit JM, Karperien M (2002) Evidence for genomic and nongenomic actions of estrogen in growth plate regulation in female and male rats at the onset of sexual maturation. J Endocrinol 175:277–288CrossRef Eerden BC van der, Emons J, Ahmed S, Essen HW van, Löwik CWGM, Wit JM, Karperien M (2002) Evidence for genomic and nongenomic actions of estrogen in growth plate regulation in female and male rats at the onset of sexual maturation. J Endocrinol 175:277–288CrossRef
47.
go back to reference Carel JC, Lahlou N, Roger M, Chaussain JL (1994) Precocious puberty and statural growth. Hum Reprod Update 10:135–147CrossRef Carel JC, Lahlou N, Roger M, Chaussain JL (1994) Precocious puberty and statural growth. Hum Reprod Update 10:135–147CrossRef
48.
go back to reference Gunther DF, Calikoglu AS, Underwood LE (1999) The effects of the estrogen receptor blocker, faslodex (ICI 182,780), on estrogen-accelerated bone maturation in mice. Pediatr Res 46:269–273 Gunther DF, Calikoglu AS, Underwood LE (1999) The effects of the estrogen receptor blocker, faslodex (ICI 182,780), on estrogen-accelerated bone maturation in mice. Pediatr Res 46:269–273
49.
go back to reference Manolagas SC, Weinstein RS, Bellido T, Bodenner DL, Jilka RL, Parfitt AM (1999) Activators of non-genomic estrogen-like signalling (ANGELS): a novel class of small molecules with bone anabolic properties. J Bone Miner Res 14:S180 Manolagas SC, Weinstein RS, Bellido T, Bodenner DL, Jilka RL, Parfitt AM (1999) Activators of non-genomic estrogen-like signalling (ANGELS): a novel class of small molecules with bone anabolic properties. J Bone Miner Res 14:S180
50.
go back to reference Kousteni S, Bellido T, Plotkin LI, O’Brien CA, Bodenner DL, Han L, Han K, DiGregorio GB, Katzenellenbogen JA, Katzenellenbogen BS, Roberson PK, Weinstein RS, Jilka RL, Manolagas SC (2001) Nongenotropic, sex-nonspecific signaling through the estrogen or androgen receptors: dissociation from transcriptional activity. Cell 104:719–730PubMed Kousteni S, Bellido T, Plotkin LI, O’Brien CA, Bodenner DL, Han L, Han K, DiGregorio GB, Katzenellenbogen JA, Katzenellenbogen BS, Roberson PK, Weinstein RS, Jilka RL, Manolagas SC (2001) Nongenotropic, sex-nonspecific signaling through the estrogen or androgen receptors: dissociation from transcriptional activity. Cell 104:719–730PubMed
51.
go back to reference Kousteni S, Han L, Chen JR, Almeida M, Plotkin LI, Bellido T, Manolagas SC (2003) Kinase-mediated regulation of common transcription factors accounts for the bone-protective effects of sex steroids. J Clin Invest 111:1651–1664CrossRefPubMed Kousteni S, Han L, Chen JR, Almeida M, Plotkin LI, Bellido T, Manolagas SC (2003) Kinase-mediated regulation of common transcription factors accounts for the bone-protective effects of sex steroids. J Clin Invest 111:1651–1664CrossRefPubMed
52.
go back to reference Manolagas SC (2000) Birth and death of bone cells: basic regulatory mechanisms and implications for the pathogenesis and treatment of osteoporosis. Endocr Rev 21:115–137CrossRefPubMed Manolagas SC (2000) Birth and death of bone cells: basic regulatory mechanisms and implications for the pathogenesis and treatment of osteoporosis. Endocr Rev 21:115–137CrossRefPubMed
53.
go back to reference Sylvia VL, Walton J, Lopez D, Dean DD, Boyan BD, Schwartz Z (2001) 17 beta-estradiol-BSA conjugates and 17 beta-estradiol regulate growth plate chondrocytes by common membrane associated mechanisms involving PKC dependent and independent signal transduction. J Cell Biochem 81:413–429CrossRefPubMed Sylvia VL, Walton J, Lopez D, Dean DD, Boyan BD, Schwartz Z (2001) 17 beta-estradiol-BSA conjugates and 17 beta-estradiol regulate growth plate chondrocytes by common membrane associated mechanisms involving PKC dependent and independent signal transduction. J Cell Biochem 81:413–429CrossRefPubMed
54.
go back to reference VanderKuur JA, Hafner MS, Christman JK, Brooks SC (1993) Effects of estradiol-17 beta analogues on activation of estrogen response element regulated chloramphenicol acetyltransferase expression. Biochemistry 32:7016–7021 VanderKuur JA, Hafner MS, Christman JK, Brooks SC (1993) Effects of estradiol-17 beta analogues on activation of estrogen response element regulated chloramphenicol acetyltransferase expression. Biochemistry 32:7016–7021
55.
go back to reference Vidal O, Kindblom LG, Ohlsson C (1999) Expression and localization of estrogen receptor-beta in murine and human bone. J Bone Miner Res 14:923–929 Vidal O, Kindblom LG, Ohlsson C (1999) Expression and localization of estrogen receptor-beta in murine and human bone. J Bone Miner Res 14:923–929
56.
go back to reference Eyre LJ, Bland R, Bujalska IJ, Sheppard MC, Stewart PM, Hewison M (1998) Characterization of aromatase and 17 beta-hydroxysteroid dehydrogenase expression in rat osteoblastic cells. J Bone Miner Res 13:996–1004 Eyre LJ, Bland R, Bujalska IJ, Sheppard MC, Stewart PM, Hewison M (1998) Characterization of aromatase and 17 beta-hydroxysteroid dehydrogenase expression in rat osteoblastic cells. J Bone Miner Res 13:996–1004
57.
go back to reference Eerden BC van der, Löwik CWGM, Wit JM, Karperien M (2004) Expression of estrogen receptors and enzymes involved in sex steroid metabolism in the rat tibia during sexual maturation. J Endocrinol 180:457–467CrossRef Eerden BC van der, Löwik CWGM, Wit JM, Karperien M (2004) Expression of estrogen receptors and enzymes involved in sex steroid metabolism in the rat tibia during sexual maturation. J Endocrinol 180:457–467CrossRef
58.
go back to reference Wronski TJ, Walsh CC, Ignaszewski LA (1986) Histologic evidence for osteopenia and increased bone turnover in ovariectomized rats. Bone 7:119–123CrossRef Wronski TJ, Walsh CC, Ignaszewski LA (1986) Histologic evidence for osteopenia and increased bone turnover in ovariectomized rats. Bone 7:119–123CrossRef
59.
go back to reference Bagi CM, Mecham M, Weiss J, Miller SC (1993) Comparative morphometric changes in rat cortical bone following ovariectomy and/or immobilization. Bone 14:877–883CrossRef Bagi CM, Mecham M, Weiss J, Miller SC (1993) Comparative morphometric changes in rat cortical bone following ovariectomy and/or immobilization. Bone 14:877–883CrossRef
60.
go back to reference Samuels A, Perry MJ, Tobias JH (1999) High-dose estrogen-induced osteogenesis in the mouse is partially suppressed by indomethacin. Bone 25:675–680CrossRefPubMed Samuels A, Perry MJ, Tobias JH (1999) High-dose estrogen-induced osteogenesis in the mouse is partially suppressed by indomethacin. Bone 25:675–680CrossRefPubMed
61.
go back to reference Chow JW, Lean JM, Abe T, Chambers TJ (1992) The anabolic effect of 17 beta-oestradiol on the trabecular bone of adult rats is suppressed by indomethacin. J Endocrinol 133:189–195 Chow JW, Lean JM, Abe T, Chambers TJ (1992) The anabolic effect of 17 beta-oestradiol on the trabecular bone of adult rats is suppressed by indomethacin. J Endocrinol 133:189–195
62.
go back to reference Corvol MT, Carrascosa A, Tsagris L, Blanchard O, Rappaport R (1987) Evidence for a direct in vitro action of sex steroids on rabbit cartilage cells during skeletal growth: influence of age and sex. Endocrinology 120:1422–1429PubMed Corvol MT, Carrascosa A, Tsagris L, Blanchard O, Rappaport R (1987) Evidence for a direct in vitro action of sex steroids on rabbit cartilage cells during skeletal growth: influence of age and sex. Endocrinology 120:1422–1429PubMed
63.
go back to reference Weise M, De-Levi S, Barnes KM, Gafni RI, Abad V, Baron J (2001) Effects of estrogen on growth plate senescence and epiphyseal fusion. Proc Natl Acad Sci USA 98:6871–6876CrossRef Weise M, De-Levi S, Barnes KM, Gafni RI, Abad V, Baron J (2001) Effects of estrogen on growth plate senescence and epiphyseal fusion. Proc Natl Acad Sci USA 98:6871–6876CrossRef
64.
go back to reference Reinecke M, Schmid AC, Heyberger-Meyer B, Hunziker EB, Zapf J (2000) Effect of growth hormone and insulin-like growth factor I (IGF-I) on the expression of IGF-I messenger ribonucleic acid and peptide in rat tibial growth plate and articular chondrocytes in vivo. Endocrinology 141:2847–2853CrossRef Reinecke M, Schmid AC, Heyberger-Meyer B, Hunziker EB, Zapf J (2000) Effect of growth hormone and insulin-like growth factor I (IGF-I) on the expression of IGF-I messenger ribonucleic acid and peptide in rat tibial growth plate and articular chondrocytes in vivo. Endocrinology 141:2847–2853CrossRef
65.
go back to reference Minina E, Kreschel C, Naski MC, Ornitz DM, Vortkamp A (2002) Interaction of FGF, Ihh/Pthlh, and BMP signaling integrates chondrocyte proliferation and hypertrophic differentiation. Dev Cell 3:439–449CrossRef Minina E, Kreschel C, Naski MC, Ornitz DM, Vortkamp A (2002) Interaction of FGF, Ihh/Pthlh, and BMP signaling integrates chondrocyte proliferation and hypertrophic differentiation. Dev Cell 3:439–449CrossRef
66.
go back to reference Eerden BC van der, Karperien M, Gevers EF, Lowik CW, Wit JM (2000) Expression of Indian hedgehog, parathyroid hormone-related protein, and their receptors in the postnatal growth plate of the rat: evidence for a locally acting growth restraining feedback loop after birth. J Bone Miner Res 15:1045–1055 Eerden BC van der, Karperien M, Gevers EF, Lowik CW, Wit JM (2000) Expression of Indian hedgehog, parathyroid hormone-related protein, and their receptors in the postnatal growth plate of the rat: evidence for a locally acting growth restraining feedback loop after birth. J Bone Miner Res 15:1045–1055
67.
go back to reference Dailey L, Laplantine E, Priore R, Basilico C (2003) A network of transcriptional and signaling events is activated by FGF to induce chondrocyte growth arrest and differentiation. J Cell Biol 161:1053–1066CrossRef Dailey L, Laplantine E, Priore R, Basilico C (2003) A network of transcriptional and signaling events is activated by FGF to induce chondrocyte growth arrest and differentiation. J Cell Biol 161:1053–1066CrossRef
68.
go back to reference Kronenberg HM (2003) Developmental regulation of the growth plate. Nature 423:332–336CrossRef Kronenberg HM (2003) Developmental regulation of the growth plate. Nature 423:332–336CrossRef
Metadata
Title
Genomic and non-genomic actions of sex steroids in the growth plate
Authors
Marcel Karperien
Bram C. J. van der Eerden
Jan Maarten Wit
Publication date
01-03-2005
Publisher
Springer-Verlag
Published in
Pediatric Nephrology / Issue 3/2005
Print ISSN: 0931-041X
Electronic ISSN: 1432-198X
DOI
https://doi.org/10.1007/s00467-004-1710-y

Other articles of this Issue 3/2005

Pediatric Nephrology 3/2005 Go to the issue