Prepubertal OVX increases IGF-I expression and bone accretion in C57BL/6J mice

American Journal of Physiology - Endocrinology and Metabolism

Volumn 295, Issue 5, 2008, Pages

  Govoni, Kristen E ^a,c   Wergedal, Jon E ^a,b   Chadwick, Robert B ^a,b   Srivastava, Apurva K ^a,b   Mohan, Subburaman ^a,b  

^a Jerry L Pettis Memorial VA Medical Center   (United States)

^b LOMA LINDA UNIVERSITY   (United States)

^c UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

Bone mineral density; Bone size; Estrogen; Osteoporosis; Puberty

Indexed keywords

ESTROGEN; SOMATOMEDIN C;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; BONE MINERAL; CONTROLLED STUDY; FEMALE; IMPLANT; MORPHOMETRICS; MOUSE; NONHUMAN; OSSIFICATION; OSTEOLYSIS; OVARIECTOMY; POSTOPERATIVE PERIOD; PREPUBERTY; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ADIPOSE TISSUE; ANIMALS; BODY WEIGHT; BONE AND BONES; BONE DENSITY; BONE DEVELOPMENT; COLLAGEN TYPE I; ESTROGENS; FEMALE; FEMUR; GENE EXPRESSION; INSULIN-LIKE GROWTH FACTOR BINDING PROTEIN 5; INSULIN-LIKE GROWTH FACTOR I; LIVER; MICE; MICE, INBRED C57BL; MODELS, BIOLOGICAL; ORGAN SIZE; OSTEOGENESIS; OVARIECTOMY; PEPTIDE FRAGMENTS; PEPTIDES; PROCOLLAGEN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEXUAL MATURATION; UTERUS;

EID: 57049132080     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.90507.2008     Document Type: Article

References (59)

1. Bain SD, Bailey MC, Celino DL, Lantry MM, Edwards MW. High-dose estrogen inhibits bone resorption and stimulates bone formation in the ovariectomized mouse. J Bone Miner Res 8: 435-442, 1993.
2. Delhanty PJ, Scott CD, Babu S, Baxter RC. Acid-labile subunit regulation during the early stages of liver regeneration: implications for glucoregulation. Am J Physiol Endocrinol Metab 280: E287-E295, 2001.
3. Dorak MT. Real-time PCR [Online]. http://dorakmt.tripod.com/ genetics/ realtime.html [2005].
4. Edwards MW, Bain SD, Bailey MC, Lantry MM, Howard GA. 17βestradiol stimulation of endosteal bone formation in the ovariectomized mouse: an animal model for the evaluation of bone-targeted estrogens. Bone 13: 29-34, 1992.
5. Evans G, Bryant HU, Magee D, Sato M, Turner RT. The effects of raloxifene on tibia histomorphometry in ovariectomized rats. Endocrinology 134: 2283-2288, 1994.
6. Garn MS. The Earlier Gain and Later Loss of Cortical Bone. Springfield, IL: Bannerstone House, 1970.
7. Garnett SP, Hogler W, Blades B, Baur LA, Peat J, Lee J, Cowell CT. Relation between hormones and body composition, including bone, in prepubertal children. Am J Clin Nutr 80: 966-972, 2004.
8. Govoni KE, Amaar YG, Kramer A, Winter E, Baylink DJ, Mohan S. Regulation of insulin-like growth factor binding protein-5, four and a half lim-2, and a disintegrin and metalloprotease-9 expression in osteoblasts. Growth Horm IGF Res, 2005.
9. Govoni KE, Lee SK, Chung YS, Behringer RR, Wergedal JE, Baylink DJ, Mohan S. Disruption of insulin-like growth factor-I expression in type IIαI collagen-expressing cells reduces bone length and width in mice. Physiol Genomics 30: 354-362, 2007.
10. Govoni KE, Wergedal JE, Florin L, Angel P, Baylink DJ, Mohan S. Conditional deletion of insulin-like growth factor-I in collagen type 1α2-expressing cells results in postnatal lethality and a dramatic reduction in bone accretion. Endocrinology 148: 5706-5715, 2007.
11. Jilka RL. Cytokines, bone remodeling, and estrogen deficiency: a 1998 update. Bone 23: 75-81, 1998.
12. Jilka RL, Takahashi K, Munshi M, Williams DC, Roberson PK, Manolagas SC. Loss of estrogen upregulates osteoblastogenesis in the murine bone marrow. Evidence for autonomy from factors released during bone resorption. J Clin Invest 101: 1942-1950, 1998.
13. Juul A. The effects of oestrogens on linear bone growth. Hum Reprod Update 7: 303-313, 2001.
14. Kasukawa Y, Baylink DJ, Guo R, Mohan S. Evidence that sensitivity to growth hormone (GH) is growth period and tissue type dependent: studies in GH-deficient lit/lit mice. Endocrinology 144: 3950-3957, 2003.
15. Kidder LS, Schmidt IU, Evans GL, Turner RT. Effects of growth hormone and low dose estrogen on bone growth and turnover in long bones of hypophysectomized rats. Calcif Tissue Int 61: 327-335, 1997.
16. Kim BT, Mosekilde L, Duan Y, Zhang XZ, Tornvig L, Thomsen JS, Seeman E. The structural and hormonal basis of sex differences in peak appendicular bone strength in rats. J Bone Miner Res 18: 150-155, 2003.
17. Leong GM, Moverare S, Brce J, Doyle N, Sjogren K, Dahlman-Wright K, Gustafsson JA, Ho KK, Ohlsson C, Leung KC. Estrogen up-regulates hepatic expression of suppressors of cytokine signaling-2 and -3 in vivo and in vitro. Endocrinology 145: 5525-5531, 2004.
18. Leung KC, Johannsson G, Leong GM, Ho KK. Estrogen regulation of growth hormone action. Endocr Rev 25: 693-721, 2004.
19. Libanati C, Baylink DJ, Lois-Wenzel E, Srinvasan N, Mohan S. Studies on the potential mediators of skeletal changes occurring during puberty in girls. J Clin Endocrinol Metab 84: 2807-2814, 1999.
20. Lindberg MK, Erlandsson M, Alatalo SL, Windahl S, Andersson G, Halleen JM, Carlsten H, Gustafsson JA, Ohlsson C. Estrogen receptor-α, but not estrogen receptor-β, is involved in the regulation of the OPG/RANKL (osteoprotegerin/receptor activator of NF-κB ligand) ratio and serum interleukin-6 in male mice. J Endocrinol 171: 425-433, 2001.
21. Lindberg MK, Weihua Z, Andersson N, Moverare S, Gao H, Vidal O, Erlandsson M, Windahl S, Andersson G, Lubahn DB, Carlsten H, Dahlman-Wright K, Gustafsson JA, Ohlsson C. Estrogen receptor specificity for the effects of estrogen in ovariectomized mice. J Endocrinol 174: 167-178, 2002.
22. Liu JL, Yakar S, LeRoith D. Mice deficient in liver production of insulin-like growth factor I display sexual dimorphism in growth hormone-stimulated postnatal growth. Endocrinology 141: 4436-4441, 2000.
23. Miyakoshi N, Kasukawa Y, Linkhart TA, Baylink DJ, Mohan S. Evidence that anabolic effects of PTH on bone require IGF-I in growing mice. Endocrinology 142: 4349-4356, 2001.
24. Modder UI, Riggs BL, Spelsberg TC, Fraser DG, Atkinson EJ, Arnold R, Khosla S. Dose-response of estrogen on bone versus the uterus in ovariectomized mice. Eur J Endocrinol 151: 503-510, 2004.
25. Mohan S, Baylink DJ. Development of a simple valid method for the complete removal of insulin-like growth factor (IGF)-binding proteins from IGFs in human serum and other biological fluids: comparison with acid-ethanol treatment and C18 Sep-Pak separation. J Clin Endocrinol Metab 80: 637-647, 1995.
26. Mohan S, Baylink DJ. Impaired skeletal growth in mice with haploinsufficiency of IGF-I: genetic evidence that differences in IGF-I expression could contribute to peak bone mineral density differences. J Endocrinol 185: 415-420, 2005.
27. Mohan S, Libanati C, Dony C, Lang K, Srinivasan N, Baylink DJ. Development, validation, and application of a radioimmunoassay for insulin-like growth factor binding protein-5 in human serum and other biological fluids. J Clin Endocrinol Metab 80: 2638-2645, 1995.
28. Mohan S, Richman C, Guo R, Amaar Y, Donahue LR, Wergedal J, Baylink DJ. Insulin-like growth factor regulates peak bone mineral density in mice by both growth hormone-dependent and -independent mechanisms. Endocrinology 144: 929-936, 2003.
29. Ooi GT, Cohen FJ, Tseng LY, Rechler MM, Boisclair YR. Growth hormone stimulates transcription of the gene encoding the acid-labile subunit (ALS) of the circulating insulin-like growth factor-binding protein complex and ALS promoter activity in rat liver. Mol Endocrinol 11: 997-1007, 1997.
30. Peng ZQ, Vaananen HK, Tuukkanen J. Ovariectomy-induced bone loss can be affected by different intensities of treadmill running exercise in rats. Calcif Tissue Int 60: 441-448, 1997.
31. Powell DR, Durham SK, Brewer ED, Frane JW, Watkins SL, Hogg RJ, Mohan S. Effects of chronic renal failure and growth hormone on serum levels of insulin-like growth factor-binding protein-4 (IGFBP-4) and IGFBP-5 in children: a report of the Southwest Pediatric Nephrology Study Group. J Clin Endocrinol Metab 84: 596-601, 1999.
32. Richman C, Kutilek S, Miyakoshi N, Srivastava AK, Beamer WG, Donahue LR, Rosen CJ, Wergedal JE, Baylink DJ, Mohan S. Postnatal and pubertal skeletal changes contribute predominantly to the differences in peak bone density between C3H/HeJ and C57BL/6J mice. J Bone Miner Res 16: 386-397, 2001.
33. Rickard DJ, Iwaniec UT, Evans G, Hefferan TE, Hunter JC, Waters KM, Lydon JP, O'Malley BW, Khosla S, Spelsberg TC, Turner RT. Bone growth and turnover in progesterone receptor knockout mice. Endocrinology 149: 2383-2390, 2008.
34. Rosen CJ, Donahue LR. Insulin-like growth factors and bone: the osteoporosis connection revisited. Proc Soc Exp Biol Med 219: 1-7, 1998.
35. Ross JL, Cassorla FG, Skerda MC, Valk IM, Loriaux DL, Cutler GB Jr. A preliminary study of the effect of estrogen dose on growth in Turner's syndrome. N Engl J Med 309: 1104-1106, 1983.
36. Salih DA, Mohan S, Kasukawa Y, Tripathi G, Lovett FA, Anderson NF, Carter EJ, Wergedal JE, Baylink DJ, Pell JM. Insulin-like growth factor-binding protein-5 induces a gender-related decrease in bone mineral density in transgenic mice. Endocrinology 146: 931-940, 2005.
37. Schoenau E. Bone mass increase in puberty: what makes it happen? Horm Res 65, Suppl 2: 2-10, 2006.
38. Sjogren K, Sheng M, Moverare S, Liu JL, Wallenius K, Tornell J, Isaksson O, Jansson JO, Mohan S, Ohlsson C. Effects of liver-derived insulin-like growth factor I on bone metabolism in mice. J Bone Miner Res 17: 1977-1987, 2002.
39. Spelsberg TC, Subramaniam M, Riggs BL, Khosla S. The actions and interactions of sex steroids and growth factors/cytokines on the skeleton. Mol Endocrinol 13: 819-828, 1999.
40. Srivastava AK, Bhattacharyya S, Castillo G, Wergedal J, Mohan S, Baylink DJ. Development and application of a serum C-telopeptide and osteocalcin assay to measure bone turnover in an ovariectomized rat model. Calcif Tissue Int 66: 435-442, 2000.
41. Thoren M, Hilding A, Brismar T, Magnusson P, Degerblad M, Larsson L, Saaf M, Baylink DJ, Mohan S. Serum levels of insulin-like growth factor binding proteins (IGFBP)-4 and -5 correlate with bone mineral density in growth hormone (GH)-deficient adults and increase with GH replacement therapy. J Bone Miner Res 13: 891-899, 1998.
42. Turner RT, Evans GL, Cavolina JM, Halloran B, Morey-Holton E. Programmed administration of parathyroid hormone increases bone formation and reduces bone loss in hindlimb-unloaded ovariectomized rats. Endocrinology 139: 4086-4091, 1998.
43. Turner RT, Evans GL, Sluka JP, Adrian MD, Bryant HU, Turner CH, Sato M. Differential responses of estrogen target tissues in rats including bone to clomiphene, enclomiphene, and zuclomiphene. Endocrinology 139: 3712-3720, 1998.
44. Turner RT, Evans GL, Wakley GK. Reduced chondroclast differentiation results in increased cancellous bone volume in estrogen-treated growing rats. Endocrinology 134: 461-466, 1994.
45. Turner RT, Hannon KS, Demers LM, Buchanan J, Bell NH. Differential effects of gonadal function on bone histomorphometry in male and female rats. J Bone Miner Res 4: 557-563, 1989.
46. Turner RT, Kidder LS, Zhang M, Harris SA, Westerlind KC, Maran A, Wronski TJ. Estrogen has rapid tissue-specific effects on rat bone. J Appl Physiol 86: 1950-1958, 1999.
47. van der Eerden BC, Karperien M, Wit JM. Systemic and local regulation of the growth plate. Endocr Rev 24: 782-801, 2003.
48. van der Meulen MCH, Carter DR. Mechanical determinants of peak bone mass. In: The Aging Skeleton, edited by Rosen CJ, Glowacki J, and Bilezikian JP. San Deigo, CA: Academic, 1999, p. 105-114.
49. Vanderschueren D, Venken K, Ophoff J, Bouillon R, Boonen S. Clinical Review: sex steroids and the periosteum-reconsidering the roles of androgens and estrogens in periosteal expansion. J Clin Endocrinol Metab 91: 378-382, 2006.
50. Veldhuis JD. Neuroendocrine control of pulsatile growth hormone release in the human: relationship with gender. Growth Horm IGF Res 8, Suppl B: 49-59, 1998.
51. Veldhuis JD, Bowers CY. Sex-steroid modulation of growth hormone (GH) secretory control: three-peptide ensemble regulation under dual feedback restraint by GH and IGF-I. Endocrine 22: 25-40, 2003.
52. Venken K, De Gendt K, Boonen S, Ophoff J, Bouillon R, Swinnen JV, Verhoeven G, Vanderschueren D. Relative impact of androgen and estrogen receptor activation in the effects of androgens on trabecular and cortical bone in growing male mice: a study in the androgen receptor knockout mouse model. J Bone Miner Res 21: 576-585, 2006.
53. Venken K, Schuit F, Van Lommel L, Tsukamoto K, Kopchick JJ, Coschigano K, Ohlsson C, Moverare S, Boonen S, Bouillon R, Vanderschueren D. Growth without growth hormone receptor: estradiol is a major growth hormone-independent regulator of hepatic IGF-I synthesis. J Bone Miner Res 20: 2138-2149, 2005.
54. Westerlind KC, Gibson KJ, Evans GL, Turner RT. The catechol estrogen, 4-hydroxyestrone, has tissue-specific estrogen actions. J Endocrinol 167: 281-287, 2000.
55. Yakar S, Pennisi P, Wu Y, Zhao H, LeRoith D. Clinical relevance of systemic and local IGF-I. Endocr Dev 9: 11-16, 2005.
56. Yakar S, Rosen CJ, Beamer WG, Ackert-Bicknell CL, Wu Y, Liu JL, Ooi GT, Setser J, Frystyk J, Boisclair YR, LeRoith D. Circulating levels of IGF-1 directly regulate bone growth and density. J Clin Invest 110: 771-781, 2002.
57. Yilmaz D, Ersoy B, Bilgin E, Gumuser G, Onur E, Pinar ED. 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, 2005.
58. Zhang M, Xuan S, Bouxsein ML, von Stechow D, Akeno N, Faugere MC, Malluche H, Zhao G, Rosen CJ, Efstratiadis A, Clemens TL. Osteoblast-specific knockout of the insulin-like growth factor (IGF) receptor gene reveals an essential role of IGF signaling in bone matrix mineralization. J Biol Chem 277: 44005-44012, 2002.
59. Zhang XZ, Kalu DN, Erbas B, Hopper JL, Seeman E. The effects of gonadectomy on bone size, mass, and volumetric density in growing rats are gender-, site-, and growth hormone-specific. J Bone Miner Res 14: 802-809, 1999.