Evidence that estrogen hastens epiphyseal fusion and cessation of longitudinal bone growth by irreversibly depleting the number of resting zone progenitor cells in female rabbits

Endocrinology

Volumn 155, Issue 8, 2014, Pages 2892-2899

  Nilsson, Ola ^a,b   Weise, Martina ^a   Landman, Ellie B M ^a,b   Meyers, Jodi L ^a   Barnes, Kevin M ^a   Baron, Jeffrey ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

AGING; ANIMALS; BONE DEVELOPMENT; CELL PROLIFERATION; CELL SIZE; CHONDROCYTES; ESTRADIOL; ESTROGENS; FEMALE; GROWTH PLATE; RABBITS; TIBIA;

EID: 84905046569     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2013-2175     Document Type: Article

References (34)

1. Abad V, Meyers JL, Weise M, et al. The role of the resting zone in growth plate chondrogenesis. Endocrinology. 2002; 143(5):1851-1857.
2. Hunziker EB. Mechanism of longitudinal bone growth and its regulation by growth plate chondrocytes. Microsc Res Tech. 1994; 28(6):505-519.
3. Kronenberg HM. Developmental regulation of the growth plate. Nature. 2003; 423(6937):332-336.
4. Walker KV, Kember NF. Cell kinetics of growth cartilage in the rat tibia. I. Measurements in young male rats. Cell Tissue Kinet. 1972; 5(5):401-408.
5. Baron J, Klein KO, Yanovski JA, et al. Induction of growth plate cartilage ossification by basic fibroblast growth factor. Endocrinology. 1994; 135(6):2790-2793.
6. Gerber HP, Vu TH, Ryan AM, Kowalski J, Werb Z., Ferrara N. VEGF couples hypertrophic cartilage remodeling, ossification and angiogenesis during endochondral bone formation. Nat Med. 1999; 5(6):623-628.
7. Marino R, Hegde A, Barnes KM, et al. Catch-up growth after hypothyroidism is caused by delayed growth plate senescence. Endocrinology. 2008; 149(4):1820-1828.
8. Nilsson O, Baron J. Fundamental limits on longitudinal bone growth: growth plate senescence and epiphyseal fusion. Trends Endocrinol Metab. 2004; 15(8):370-374.
9. Walker KV, Kember NF. Cell kinetics of growth cartilage in the rat tibia. II. Measurements during ageing. Cell Tissue Kinet. 1972; 5(5): 409-419.
10. Forcinito P, Andrade AC, Finkielstain GP, Baron J, Nilsson O., Lui JC. Growth-inhibiting conditions slow growth plate senescence. J Endocrinol. 2011; 208(1):59-67.
11. Gafni RI, Weise M, Robrecht DT, et al. Catch-up growth is associated with delayed senescence of the growth plate in rabbits. Pediatr Res. 2001; 50(5):618-623.
12. Hunziker EB, Schenk RK. Physiological mechanisms adopted by chondrocytes in regulating longitudinal bone growth in rats. J Physiol. 1989; 414:55-71.
13. Schrier L, Ferns SP, Barnes KM et al. Depletion of resting zone chondrocytes during growth plate senescence. J Endocrinol. 2006; 189(1):27-36.
14. Carel JC, Lahlou N, Roger M, Chaussain JL. Precocious puberty and statural growth. Hum Reprod Update. 2004; 10(2):135-147.
15. Uriarte MM, Baron J, Garcia HB, Barnes K.M., Loriaux DL, Cutler GB Jr. The effect of pubertal delay on adult height in men with isolated hypogonadotropic hypogonadism. J Clin Endocrinol Metab. 1992; 74(2):436-440.
16. Morishima A, Grumbach MM, Simpson ER, Fisher C, Qin K. Aromatase deficiency in male and female siblings caused by a novel mutation and the physiological role of estrogens. J Clin Endocrinol Metab. 1995; 80(12):3689-3698.
17. Quaynor SD, Stradtman EW, Jr, Kim HG, et al. Delayed puberty and estrogen resistance in a woman with estrogen receptor α variant. N Engl J Med. 2013; 369(2):164-171.
18. Smith EP, Boyd J, Frank GR, et al. Estrogen resistance caused by a mutation in the estrogen-receptor gene in a man. N Engl J Med. 1994; 331(16):1056-1061.
19. Börjesson AE, Windahl SH, Karimian E, et al. The role of estrogen receptor-α and its activation function-1 for growth plate closure in female mice. Am J Physiol Endocrinol Metab. 2012; 302(11): E1381-E1389.
20. Weise M, De-Levi S, Barnes KM, Gafni R.I., Abad V., Baron J. Effects of estrogen on growth plate senescence and epiphyseal fusion. Proc Natl Acad Sci USA. 2001; 98(12):6871-6876.
21. Koziel L, Wuelling M, Schneider S, Vortkamp A. Gli3 acts as a repressor downstream of Ihh in regulating two distinct steps of chondrocyte differentiation. Development. 2005; 132(23):5249-5260.
22. Heinrichs C, Yanovski JA, Roth A.H., et al. Dexamethasone increases growth hormone receptor messenger ribonucleic acid levels in liver and growth plate. Endocrinology. 1994; 135(3):1113-1118.
23. Weise M, Flor A, Barnes KM, Cutler G.B., Jr, Baron J. Determinants of growth during gonadotropin-releasing hormone analog therapy for precocious puberty. J Clin Endocrinol Metab. 2004; 89(1):103-107.
24. Chau M, Forcinito P, Andrade AC, et al. Organization of the Indian hedgehog-parathyroid hormone-related protein system in the postnatal growth plate. J Mol Endocrinol. 2011; 47(1):99-107.
25. Chung UI, Schipani E, McMahon AP, Kronenberg HM. Indian hedgehog couples chondrogenesis to osteogenesis in endochondral bone development. J Clin Invest. 2001; 107(3):295-304.
26. Lanske B, Karaplis AC, Lee K, et al. PTH/PTHrP receptor in early development and Indian hedgehog-regulated bone growth. Science. 1996; 273(5275):663-666.
27. Vortkamp A, Lee K, Lanske B, Segre G.V., Kronenberg HM, Tabin CJ. Regulation of rate of cartilage differentiation by Indian hedgehog and PTH-related protein. Science. 1996; 273(5275):613-622.
28. Lui JC, Andrade AC, Forcinito P, et al. Spatial and temporal regulation of gene expression in the mammalian growth plate. Bone. 2010; 46(5):1380-1390.
29. Nilsson O, Parker EA, Hegde A, Chau M, Barnes K.M., Baron J. Gradients in bone morphogenetic protein-related gene expression across the growth plate. J Endocrinol. 2007; 193(1):75-84.
30. Dao DY, Jonason JH, Zhang Y, et al. Cartilage-specific β-catenin signaling regulates chondrocyte maturation, generation of ossification centers, and perichondrial bone formation during skeletal development. J Bone Miner Res. 2012; 27(8):1680-1694.
31. De Luca F, Barnes KM, Uyeda JA, et al. Regulation of growth plate chondrogenesis by bone morphogenetic protein-2. Endocrinology. 2001; 142(1):430-436.
32. Shu B, Zhang M, Xie R, et al. BMP2, but not BMP4, is crucial for chondrocyte proliferation and maturation during endochondral bone development. J Cell Sci. 2011; 124(Pt 20):3428-3440.
33. Yoon BS, Ovchinnikov DA, Yoshii I, Mishina Y, Behringer R.R., Lyons KM. Bmpr1a and Bmpr1b have overlapping functions and are essential for chondrogenesis in vivo. Proc Natl Acad Sci USA. 2005; 102(14):5062-5067.
34. Hirai T, Chagin AS, Kobayashi T, Mackem S, Kronenberg HM. Parathyroid hormone/parathyroid hormone-related protein receptor signaling is required for maintenance of the growth plate in postnatal life. Proc Natl Acad Sci USA. 2011; 108(1):191-196.