Delayed pubertal development by hypothalamic suppression causes an increase in periosteal modeling but a reduction in bone strength in growing female rats

Bone

Volumn 42, Issue 6, 2008, Pages 1137-1143

  Yingling, Vanessa R ^a   Taylor, Garvin ^b  

^a TEMPLE UNIVERSITY   (United States)

^b CITY UNIVERSITY OF NEW YORK   (United States)

Author keywords

Biomechanics; Bone histomorphometry; Hormones; Modeling; Puberty

Indexed keywords

CALCEIN; ESTRADIOL; GONADORELIN ANTAGONIST; SOMATOMEDIN C;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE MINERAL; BONE STRENGTH; BONE STRESS; CONTROLLED STUDY; CORTICAL BONE; DELAYED PUBERTY; DOSE RESPONSE; ESTRADIOL BLOOD LEVEL; FEMALE; FEMUR; HYPOTHALAMUS; MORPHOMETRICS; NONHUMAN; OSSIFICATION; OVARY; PERIOSTEUM; RAT; TIBIA; UTERUS WEIGHT; VAGINA; YOUNG MODULUS;

ANIMALS; BONE AND BONES; DOSE-RESPONSE RELATIONSHIP, DRUG; ESTRADIOL; FEMALE; GONADOTROPIN-RELEASING HORMONE; HUMANS; HYPOTHALAMUS; INSULIN-LIKE GROWTH FACTOR I; OSTEOGENESIS; PERIOSTEUM; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; SEXUAL MATURATION; STRESS, MECHANICAL;

EID: 43149113000     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2008.02.005     Document Type: Article

References (56)

1. Golden N.H. Osteoporosis prevention: a pediatric challenge. Arch Pediatr Adolesc Med 154 (2000) 542-543
2. Ferrari S.L., Chevalley T., Bonjour J.P., and Rizzoli R. Childhood fractures are associated with decreased bone mass gain during puberty: an early marker of persistent bone fragility?. J Bone Miner Res 21 (2006) 501-507
3. Myburgh K.H., Hutchins J., Fataar A.B., Hough S.F., and Noakes T.D. Low bone density is an etiologic factor for stress fractures in athletes. Ann Intern Med 113 (1990) 754-759
4. Kadel N.J., Teitz C.C., and Kronmal R.A. Stress fractures in ballet dancers. Am J Sports Med 20 (1992) 445-449
5. Warren M.P., Brooks-Gunn J., Fox R.P., Lancelot C., Newman D., and Hamilton W.G. Lack of bone accretion and amenorrhea: evidence for a relative osteopenia in weight-bearing bones. J Clin Endocrinol Metab 72 (1991) 847-853
6. Feingold D., and Hame S.L. Female athlete triad and stress fractures. Orthop Clin North Am 37 (2006) 575-583
7. Nattiv A., Loucks A.B., Manore M.M., Sanborn C.F., Sundgot-Borgen J., and Warren M.P. The female athlete triad. Med Sci Sports Exerc 39 (2007) 1867-1882
8. Redman L.M., and Loucks A.B. Menstrual disorders in athletes. Sports Med 35 (2005) 747-755
9. Warren MP, Stiehl AL. Exercise and female adolescents: effects on the reproductive and skeletal systems. J Am Med Womens Assoc 1999;54:115,20, 138.
10. Bailey D.A. The Saskatchewan pediatric bone mineral accrual study: bone mineral acquisition during the growing years. Int J Sports Med 18 Suppl 3 (1997) S191-S194
11. Bailey D.A., Martin A.D., McKay H.A., Whiting S., and Mirwald R. Calcium accretion in girls and boys during puberty: a longitudinal analysis. J Bone Miner Res 15 (2000) 2245-2250
12. Warren M.P., Brooks-Gunn J., Fox R.P., Holderness C.C., Hyle E.P., and Hamilton W.G. Osteopenia in exercise-associated amenorrhea using ballet dancers as a model: a longitudinal study. J Clin Endocrinol Metab 87 (2002) 3162-3168
13. Carbon R., Sambrook P.N., Deakin V., et al. Bone density of elite female athletes with stress fractures. Med J Aust 153 (1990) 373-376
14. Gafni R.I., McCarthy E.F., Hatcher T., et al. Recovery from osteoporosis through skeletal growth: early bone mass acquisition has little effect on adult bone density. FASEB J 16 (2002) 736-738
15. Yingling V.R., and Khaneja A. Short-term delay of puberty causes a transient reduction in bone strength in growing female rats. Bone 38 (2006) 67-73
16. Gafni R.I., and Baron J. Catch-up growth: possible mechanisms. Pediatr Nephrol 14 (2000) 616-619
17. Warren M.P., Brooks-Gunn J., Fox R.P., et al. Persistent osteopenia in ballet dancers with amenorrhea and delayed menarche despite hormone therapy: a longitudinal study. Fertil Steril 80 (2003) 398-404
18. Price C., Herman B.C., Lufkin T., Goldman H.M., and Jepsen K.J. Genetic variation in bone growth patterns defines adult mouse bone fragility. J Bone Miner Res 20 (2005) 1983-1991
19. Turner R.T., Vandersteenhoven J.J., and Bell N.H. The effects of ovariectomy and 17 beta-estradiol on cortical bone histomorphometry in growing rats. J Bone Miner Res 2 (1987) 115-122
20. Valentino R., Savastano S., Tommaselli A.P., D'Amore G., Dorato M., and Lombardi G. The influence of intense ballet training on trabecular bone mass, hormone status, and gonadotropin structure in young women. J Clin Endocrinol Metab 86 (2001) 4674-4678
21. Anai T., Miyazaki F., Tomiyasu T., and Matsuo T. Risk of irregular menstrual cycles and low peak bone mass during early adulthood associated with age at menarche. Pediatr Int 43 (2001) 483-488
22. Dhuper S., Warren M.P., Brooks-Gunn J., and Fox R. Effects of hormonal status on bone density in adolescent girls. J Clin Endocrinol Metab 71 (1990) 1083-1088
23. Yingling V.R., Xiang Y., Raphan T., Schaffler M.B., Koser K., and Malique R. The effect of a short-term delay of puberty on trabecular bone mass and structure in female rats: a texture-based and histomorphometric analysis. Bone 40 (2007) 419-424
24. Roth C., Leonhardt S., Seidel C., Lakomek M., Wuttke W., and Jarry H. GnRH antagonist cetrorelix prevents sexual maturation of peripubertal male rats. Exp Clin Endocrinol Diabetes 108 (2000) 358-363
25. Roth C.L., Neu C., Jarry H., and Schoenau E. Different effects of agonistic vs. antagonistic gnrh-analogues (triptorelin vs. cetrorelix) on bone modeling and remodeling in peripubertal female rats. Exp Clin Endocrinol Diabetes 113 (2005) 451-456
26. Turner R.T., Maran A., Lotinun S., et al. Animal models for osteoporosis. Rev Endocr Metab Disord 2 (2001) 117-127
27. Parfitt A.M., Drezner M.K., Glorieux F.H., et al. Bone histomorphometry: standardization of nomenclature, symbols, and units. Report of the ASBMR histomorphometry nomenclature committee. J Bone Miner Res 2 (1987) 595-610
28. Turner C.H., and Burr D.B. Basic biomechanical measurements of bone: a tutorial. Bone 14 (1993) 595-608
29. Jepsen K.J., Akkus O.J., Majeska R.J., and Nadeau J.H. Hierarchical relationship between bone traits and mechanical properties in inbred mice. Mamm Genome 14 (2003) 97-104
30. Brodt M.D., Ellis C.B., and Silva M.J. Growing C57Bl/6 mice increase whole bone mechanical properties by increasing geometric and material properties. J Bone Miner Res 14 (1999) 2159-2166
31. Di Masso R.J., Font M.T., Capozza R.F., Detarsio G., Sosa F., and Ferretti J.L. Long-bone biomechanics in mice selected for body conformation. Bone 20 (1997) 539-545
32. Wiren K.M., Zhang X.W., Toombs A.R., et al. Targeted overexpression of androgen receptor in osteoblasts: unexpected complex bone phenotype in growing animals. Endocrinology 145 (2004) 3507-3522
33. Rakover Y., Lu P., Briody J.N., et al. Effects of delaying puberty on bone mineralization in female rats. Hum Reprod 15 (2000) 1457-1461
34. Xiang Y., Yingling V.R., Malique R., Li C.Y., Schaffler M.B., and Raphan T. Comparative assessment of bone mass and structure using texture-based and histomorphometric analyses. Bone 40 (2007) 544-552
35. van der Meulen M.C., Jepsen K.J., and Mikic B. Understanding bone strength: size isn't everything. Bone 29 (2001) 101-104
36. Jepsen K.J., Goldstein S.A., Kuhn J.L., Schaffler M.B., and Bonadio J. Type-I collagen mutation compromises the post-yield behavior of Mov13 long bone. J Orthop Res 14 (1996) 493-499
37. Manolagas S.C. Birth and death of bone cells: basic regulatory mechanisms and implications for the pathogenesis and treatment of osteoporosis. Endocr Rev 21 (2000) 115-137
38. Jilka R.L., Takahashi K., Munshi M., Williams D.C., Roberson P.K., and Manolagas S.C. Loss of estrogen upregulates osteoblastogenesis in the murine bone marrow. Evidence for autonomy from factors released during bone resorption. J Clin Invest 101 (1998) 1942-1950
39. Khosla S. Minireview: the OPG/RANKL/RANK system. Endocrinology 142 (2001) 5050-5055
40. Wronski T.J., Cintron M., Doherty A.L., and Dann L.M. Estrogen treatment prevents osteopenia and depresses bone turnover in ovariectomized rats. Endocrinology 123 (1988) 681-686
41. Riggs B.L., O'Fallon W.M., Muhs J., O'Connor M.K., Kumar R., and Melton III L.J. Long-term effects of calcium supplementation on serum parathyroid hormone level, bone turnover, and bone loss in elderly women. J Bone Miner Res 13 (1998) 168-174
42. Ahlborg H.G., Johnell O., Turner C.H., Rannevik G., and Karlsson M.K. Bone loss and bone size after menopause. N Engl J Med 349 (2003) 327-334
43. Szulc P., Seeman E., Duboeuf F., Sornay-Rendu E., and Delmas P.D. Bone fragility: failure of periosteal apposition to compensate for increased endocortical resorption in postmenopausal women. J Bone Miner Res 21 (2006) 1856-1863
44. Ihle R., and Loucks A.B. Dose-response relationships between energy availability and bone turnover in young exercising women. J Bone Miner Res 19 (2004) 1231-1240
45. Venken K., Moverare-Skrtic S., Kopchick J.J., et al. Impact of androgens, growth hormone, and igf-I on bone and muscle in male mice during puberty. J Bone Miner Res 22 (2007) 72-82
46. Handelsman D.J., Spaliviero J.A., Scott C.D., and Baxter R.C. Hormonal regulation of the peripubertal surge of insulin-like growth factor-I in the rat. Endocrinology 120 (1987) 491-496
47. Fisher J.S., Kohrt W.M., and Brown M. Food restriction suppresses muscle growth and augments osteopenia in ovariectomized rats. J Appl Physiol 88 (2000) 265-271
48. Ferrari B., Pezzuto A., Barusi L., and Coppola F. Gonadotropin-releasing hormone antagonists increase follicular fluid insulin-like growth factor-I and vascular endothelial growth factor during ovarian stimulation cycles. Gynecol Endocrinol 22 (2006) 289-296
49. Bateman T.A., Zimmerman R.J., Ayers R.A., Ferguson V.L., Chapes S.K., and Simske S.J. Histomorphometric, physical, and mechanical effects of spaceflight and insulin-like growth factor-I on rat long bones. Bone 23 (1998) 527-535
50. Wronski T.J., Schenck P.A., Cintron M., and Walsh C.C. Effect of body weight on osteopenia in ovariectomized rats. Calcif Tissue Int 40 (1987) 155-159
51. Meli R., Pacilio M., Raso G.M., et al. Estrogen and raloxifene modulate leptin and its receptor in hypothalamus and adipose tissue from ovariectomized rats. Endocrinology 145 (2004) 3115-3121
52. Yakar S., and Rosen C.J. From mouse to man: redefining the role of insulin-like growth factor-I in the acquisition of bone mass. Exp Biol Med (Maywood) 228 (2003) 245-252
53. Hayden J.M., Mohan S., and Baylink D.J. The insulin-like growth factor system and the coupling of formation to resorption. Bone 17 (1995) 93S-98S
54. Drinkwater B.L., Nilson K., Chesnut III C.H., Bremner W.J., Shainholtz S., and Southworth M.B. Bone mineral content of amenorrheic and eumenorrheic athletes. N Engl J Med 311 (1984) 277-281
55. Pettersson U., Stalnacke B., Ahlenius G., Henriksson-Larsen K., and Lorentzon R. Low bone mass density at multiple skeletal sites, including the appendicular skeleton in amenorrheic runners. Calcif Tissue Int 64 (1999) 117-125
56. Cumming D.C. Exercise-associated amenorrhea, low bone density, and estrogen replacement therapy. Arch Intern Med 156 (1996) 2193-2195