Gender- and region-specific variations of estrogen receptor α and β expression in the growth plate of spine and limb during development and adulthood

Histochemistry and Cell Biology

Volumn 137, Issue 1, 2012, Pages 79-95

  Li, Xin Feng ^a,b   Wang, Shan Jin ^a   Jiang, Lei Sheng ^a   Dai, Li Yang ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

Estrogen; Estrogen receptor; Growth plate; Limb; Longitudinal growth; Spine

Indexed keywords

ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; MESSENGER RNA;

ADULTHOOD; ANIMAL EXPERIMENT; ARTICLE; CARTILAGE CELL; FEMALE; GENDER AND SEX; GROWTH PLATE; IMMUNOREACTIVITY; MALE; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PUBERTY; RAT; SEX DIFFERENCE; SPINE; TIBIA;

AGING; ANIMALS; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; EXTREMITIES; FEMALE; GENE EXPRESSION PROFILING; GROWTH PLATE; IMMUNOHISTOCHEMISTRY; MALE; RATS; RATS, WISTAR; REAL-TIME POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEX CHARACTERISTICS; SPINE;

RATTUS;

EID: 84857630276     PISSN: 09486143     EISSN: 1432119X     Source Type: Journal    
DOI: 10.1007/s00418-011-0877-0     Document Type: Article

References (63)

1. Bass S, Delmas PD, Pearce G, Hendrich E, Tabensky A, Seeman E (1999) The differing tempo of growth in bone size, mass, and density in girls is region-specific. J Clin Invest 104:795-804 (Pubitemid 29536365)
2. Ben-Hur H, Mor G, Blickstein I, Likhman I, Kohen F, Dgani R, Insler V, Yaffe P, Ornoy A (1993) Localization of estrogen receptors in long bones and vertebrae of human fetuses. Calcif Tissue Int 53:91-96 (Pubitemid 23215382)
3. 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 (Pubitemid 28385657)
4. Bord S, Horner A, Beavan S, Compston J (2001) Estrogen receptors alpha and beta are differentially expressed in developing human bone. J Clin Endocrinol Metab 86:2309-2314 (Pubitemid 32472956)
5. Bradney M, Karlsson MK, Duan Y, Stuckey S, Bass S, Seeman E (2000) Heterogeneity in the growth of the axial and appendicular skeleton in boys: implications for the pathogenesis of bone fragility in men. J Bone Miner Res 15:1871-1878
6. 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
7. Braidman IP, Hainey L, Batra G, Selby PB, Saunders PT, Hoyland JA (2001) Localization of estrogen receptor protein expression in adult human bone. J Bone Miner Res 16:214-220 (Pubitemid 32105402)
8. Buie HR, Moore CP, Boyd SK (2008) Postpubertal architectural developmental patterns differ between the L3 vertebra and proximal tibia in three inbred strains of mice. J Bone Miner Res 23:2048-2059
9. Byers S, Moore AJ, Byard RW, Fazzalari NL (2000) Quantitative histomorphometric analysis of the human growth plate from birth to adolescence. Bone 27:495-501
10. Camper L, Holmvall K,Wängnerud C, Aszódi A, Lundgren-Akerlund E (2001) Distribution of the collagen-binding integrin alpha10beta1 during mouse development. Cell Tissue Res 306:107-116 (Pubitemid 32905603)
11. 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 337:91-95 (Pubitemid 27284394)
12. Chagin AS, Sävendahl L (2009) Genes of importance in the hormonal regulation of growth plate cartilage. Horm Res 71(Suppl 2):41-47
13. Chagin AS, Lindberg MK, Andersson N, Moverare S, Gustafsson JA, Sävendahl L, Ohlsson C (2004) Estrogen receptor-b inhibits skeletal growth and has the capacity to mediate growth plate fusion in female mice. J Bone Miner Res 19:72-77 (Pubitemid 41295140)
14. Couse JF, Korach KS (1999) Estrogen receptor null mice: what have we learned and where will they lead us? Endocr Rev 20:358-417 (Pubitemid 30654784)
15. Egerbacher M, Helmreich M, Rossmanith W, Haeusler G (2002) Estrogen receptor-a and estrogen receptor-b are present in the human growth plate in childhood and adolescence, in identical distribution. Horm Res 58:99-103 (Pubitemid 35007586)
16. Fukunaga T, Yamashiro T, Oya S, Takeshita N, Takigawa M, Takano-Yamamoto T (2003) Connective tissue growth factor mRNA expression pattern in cartilages is associated with their type I collagen expression. Bone 33:911-918 (Pubitemid 37543567)
17. Gevers EF, van der Eerden BC, Karperien M, Raap AK, Robinson IC, Wit JM (2002) Localization and regulation of the growth hormone receptor and growth hormone-binding protein in the rat growth plate. J Bone Miner Res 17:1408-1419 (Pubitemid 34803825)
18. Giustina A, Mazziotti G, Canalis E (2008) Growth hormone, insulinlike growth factors, and the skeleton. Endocr Rev 29:535-559
19. Glatt V, Canalis E, Stadmeyer L, Bouxsein ML (2007) Age-related changes in trabecular architecture differ in female and male C57BL/6J mice. J Bone Miner Res 22:1197-1207 (Pubitemid 351339702)
20. Grumbach MM (2000) Estrogen, bone, growth and sex: a sea change in conventional wisdom. J Pediatr Endocrinol Metab 13(Suppl 6):1439-1455 (Pubitemid 32063201)
21. Hosoya A, Hoshi K, Sahara N, Ninomiya T, Akahane S, Kawamoto T, Ozawa H (2005) Effects of fixation and decalcification on the immunohistochemical localization of bone matrix proteins in fresh-frozen bone sections. Histochem Cell Biol 123:639-646 (Pubitemid 41126083)
22. Hughes PC, Tanner JM (1970) The assessment of skeletal maturity in the growing rat. J Anat 106:371-402
23. Kaludjerovic J, Ward WE (2008) Diethylstilbesterol has genderspecific effects on weight gain and bone development in mice. J Toxicol Environ Health A 71:1032-1042 (Pubitemid 352000681)
24. Kennedy J, Baris C, Hoyland JA, Selby PL, Freemont AJ, Braidman IP (1999) Immunofluorescent localization of estrogen receptor-a in growth plates of rabbits, but not in rats, at sexual maturity. Bone 24:9-16 (Pubitemid 28546700)
25. Khosla S, Riggs BL, Atkinson EJ, Oberg AL, McDaniel LJ, Holets M, Peterson JM, Melton LJ III (2006) Effects of sex and age on bone microstructure at the ultradistal radius: a population-based noninvasive in vivo assessment. J Bone Miner Res 21:124-131 (Pubitemid 43023234)
26. Kronenberg HM (2003) Developmental regulation of the growth plate. Nature 423:332-336 (Pubitemid 40852707)
27. Kusec V, Virdi AS, Prince R, Triffitt JT (1998) Localization of estrogen receptor- in human and rabbit skeletal tissues. J Clin Endocrinol Metab 83:2421-2428 (Pubitemid 28503041)
28. Laue L, Kenigsberg D, Pescovitz OH, Hench KD, Barnes KM, Loriaux DL, Cutler GB Jr (1989) Treatment of familial male precocious puberty with spironolactone and testolactone. N Engl J Med 320:496-502 (Pubitemid 19062525)
29. Lebovitz HE, Eisenbarth GS (1975) Hormonal regulation of cartilage growth and metabolism. Vitam Horm 33:575-648
30. Lee PA, Witchel SF (1997) The influence of estrogen on growth. Curr Opin Pediatr 9:431-436 (Pubitemid 27404270)
31. Li H, Jiang LS, Dai LY (2010) High glucose potentiates collagen synthesis and bone morphogenetic protein-2-induced early osteoblast gene expression in rat spinal ligament cells. Endocrinology 151:63-74
32. Li XF, Yan J, Jiang LS, Dai LY (2011) Age-related variations of leptin receptor expression in the growth plate of spine and limb: genderand region-specific changes. Histochem Cell Biol 135:487-497
33. Lindberg MK, Alatalo SL, Halleen JM, Mohan S, Gustafsson JA, Ohlsson C (2001) Estrogen receptor specificity in the regulation of the skeleton in female mice. J Endocrinol 171:229-236 (Pubitemid 33061699)
34. Maffei L, Murata Y, Rochira V, Tubert G, Aranda C, Vazquez M, Clyne CD, Davis S, Simpson ER, Carani C (2004) Dysmetabolic syndrome in a man with a novel mutation of the aromatase gene: effects of testosterone, alendronate, and estradiol treatment. J Clin Endocrinol Metab 89:61-70 (Pubitemid 38183860)
35. Matthews JB (1982) Influence of decalcification on immunohistochemical staining of formalin-fixed paraffin-embedded tissue. J Clin Pathol 35:1392-1394 (Pubitemid 13168198)
36. Mitani H, Takahashi I, Onodera K, Bae JW, Sato T, Takahashi N, Sasano Y, Igarashi K, Mitani H (2006) Comparison of agedependent expression of aggrecan and ADAMTSs in mandibular condylar cartilage, tibial growth plate, and articular cartilage in rats. Histochem Cell Biol 126:371-380
37. 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 80:3689-3698
38. Mundlos S, Zabel B (1994) Developmental expression of human cartilage matrix protein. Dev Dyn 199:241-252 (Pubitemid 24101006)
39. Neves JD, Omar NF, Narvaes EA, Gomes JR, Novaes PD (2011) Influence of different decalcifying agents on EGF and EGFR immunostaining. Acta Histochem 113:484-488
40. Nilsson LO, Boman A, Sävendahl L, Grigelioniene G, Ohlsson C, Ritzén EM, Wroblewski J (1999) Demonstration of estrogen receptor-b immunoreactivity in human growth plate cartilage. J Clin Endocrinol Metab 84:370-373 (Pubitemid 29036729)
41. Nilsson O, Abad V, Chrysis D, Ritzén EM, Sävendahl L, Baron J (2002) Estrogen receptor-a and -b are expressed throughout postnatal development in the rat and rabbit growth plate. J Endocrinol 173:407-414 (Pubitemid 34704712)
42. Nilsson O, Chrysis D, Pajulo O, Boman A, Holst M, Rubinstein J, Martin Ritzén E, Sävendahl L (2003) Localization of estrogen receptors-a and -b and androgen receptor in the human growth plate at different pubertal stages. J Endocrinol 177:319-326 (Pubitemid 36656405)
43. Nilsson O, Marino R, De Luca F, Phillip M, Baron J (2005) Endocrine regulation of the growth plate. Horm Res 64:157-165 (Pubitemid 41642759)
44. Ornoy A, Giron S, Aner R, Goldstein M, Boyan BD et al (1994) Gender dependent effects of testosterone and 17 b-estradiol on bone growth and modelling in young mice. Bone Miner 24:43-58
45. Parikka V, Peng Z, Hentunen T, Risteli J, Elo T, Väänänen HK, Härkönen P (2005) Estrogen responsiveness of bone formation in vitro and altered bone phenotype in aged estrogen receptor-a deficient male and female mice. Eur J Endocrinol 152:301-314 (Pubitemid 40309579)
46. Sampson HW, Dearman AC, Akintola AD, Zimmer WE, Parrish AR (2007) Immunohistochemical localization of cadherin and catenin adhesion molecules in the murine growth plate. J Histochem Cytochem 55:845-852 (Pubitemid 47068275)
47. Seeman E (2001) Unresolved issues in osteoporosis in men. Rev Endocr Metab Disord 2:45-64 (Pubitemid 33643892)
48. Sims NA, Dupont S, Krust A, Clement-Lacroix P, Minet D, Resche- Rigon M, Gaillard-Kelly M, Baron R (2002) Deletion of estrogen receptors reveals a regulatory role for estrogen receptors- b in bone remodeling in females but not in males. Bone 30:18-25 (Pubitemid 34044296)
49. 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 331:1056-1061 (Pubitemid 24317698)
50. Tozum TF, Oppenlander ME, Koh-Paige AJ, Robins DM, McCauley LK (2004) Effects of sex steroid receptor specificity in the regulation of skeletal metabolism. Calcif Tissue Int 75:60-70 (Pubitemid 38989220)
51. Tsunenari T, Tsutsumi M, Ohno K, Yamamoto Y, Kawakatsu M, Shimogaki K, Negishi H, Sugimoto T, Fukase M, Fujita T (1993) Age- and gender-related changes in body composition in Japanese subjects. J Bone Miner Res 8:397-402 (Pubitemid 23105835)
52. van der Eerden BC, Karperien M, Gevers EF, Löwik CW, Wit JM (2000) Expression of Indian hedgehog, parathyroid hormonerelated 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 (Pubitemid 30350067)
53. van der Eerden BCJ, Karperien M, Wit JM (2001) The estrogen receptor in the growth plate: implications for pubertal growth. J Pediatr Endocrinol Metab 14:1527-1533 (Pubitemid 33730769)
54. van der Eerden BCJ, Gevers EF, Lowik CW, Karperien M, Wit JM (2002) Expression of estrogen receptor and in the epiphyseal plate of the rat. Bone 30:478-485 (Pubitemid 34204122)
55. Vidal O, Lindberg M, Sävendahl L, Lubahn DB, Ritzen EM, Gustafsson JA, Ohlsson C (1999) Disproportional body growth in female estrogen receptor-a-inactivated mice. Biochem Biophys Res Commun 265:569-571
56. Vidal O, Lindberg MK, Hollberg K, Baylink DJ, Andersson G, Lubahn DB, Mohan S, Gustafsson JA, Ohlsson C (2000) Estrogen receptor specificity in the regulation of skeletal growth and maturation in male mice. Proc Natl Acad Sci USA 97:5474-5479 (Pubitemid 30313743)
57. Windahl SH, Vidal O, Andersson G, Gustafsson JA, Ohlsson C (1999) Increased cortical bone mineral content but unchanged trabecular bone mineral density in female ERb (-/-) mice. J Clin Invest 104:895-901 (Pubitemid 29536339)
58. Windahl SH, Hollberg K, Vidal O, Gustafsson JA, Ohlsson C, Andersson G (2001) Female estrogen receptor b-/- mice are partially protected against age-related trabecular bone loss. J Bone Miner Res 16:1388-1398 (Pubitemid 32677073)
59. Yilmaz D, Ersoy B, Bilgin E, Gümüşer G, Onur E, Pinar ED (2005) Bone mineral density in girls and boys at different pubertal stages: relation with gonadal steroids, bone formation markers, and growth parameters. J Bone Miner Metab 23:476-482 (Pubitemid 41571115)
60. Yuen KW, Kwok TC, Qin L, Leung JC, Chan DC, Kwok AW, Woo J, Leung PC (2010) Characteristics of age-related changes in bone compared between male and female reference Chinese populations in Hong Kong: a pQCT study. J Bone Miner Metab 28:672-681
61. Zachmann M, Prader A, Sobel EH, Crigler JF Jr, Ritzén EM, Atarés M, Ferrandez A (1986) Pubertal growth in patients with androgen insensitivity: indirect evidence for the importance of estrogens in pubertal growth of girls. J Pediatr 108:694-697 (Pubitemid 16064111)
62. Zhang XZ, Kalu DN, Erbas B, Hopper JL, Seeman E (1999) The effects of gonadectomy on bone size, mass, and volumetric density in growing rats are gender-, site-, and growth hormonespecific. J Bone Miner Res 14:802-809 (Pubitemid 29210607)
63. Zhao CQ, Liu D, Li H, Jiang LS, Dai LY (2008) Expression of leptin and its functional receptor on disc cells: contribution to cell proliferation. Spine 33:E858-E864