Insulin like growth factor-I: A critical mediator of the skeletal response to parathyroid hormone

Current Molecular Pharmacology

Volumn 5, Issue 2, 2012, Pages 135-142

  Bikle, Daniel D ^a   Wang, Yongmei ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Insulin like growth factor; Osteoblasts; Osteoclasts; Osteoprogenitors; Parathyroid hormone

Indexed keywords

ALKALINE PHOSPHATASE; ANABOLIC AGENT; ANGIOPOIETIN 1; BISPHOSPHONIC ACID DERIVATIVE; COLLAGEN TYPE 1; EPHRIN B2; EPHRIN RECEPTOR B4; MESSENGER RNA; OSTEOCALCIN; OSTEOCLAST DIFFERENTIATION FACTOR; OSTEOPROTEGERIN; PARATHYROID HORMONE; SOMATOMEDIN C; TRANSCRIPTION FACTOR RUNX2; WNT PROTEIN;

APOPTOSIS; BONE MINERALIZATION; CARTILAGE CELL; CATABOLISM; CELL DIFFERENTIATION; CELL PROLIFERATION; DRUG EXPOSURE; GENE DELETION; HEMATOPOIETIC STEM CELL; HORMONE RECEPTOR INTERACTION; HORMONE RELEASE; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; OSSIFICATION; OSTEOBLAST; OSTEOCLAST; OSTEOCLASTOGENESIS; OSTEOLYSIS; OSTEOPENIA; OSTEOPOROSIS; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVIEW; TRANSGENIC MOUSE; WNT SIGNALING PATHWAY;

EID: 84861733148     PISSN: 18744672     EISSN: 18744702     Source Type: Journal    
DOI: 10.2174/1874-470211205020135     Document Type: Review

References (87)

1. Neer, R.M.; Arnaud, C.D.; Zanchetta, J.R.; Prince, R.; Gaich, G.A.; Reginster, J.Y.; Hodsman, A.B.; Eriksen, E.F.; Ish-Shalom, S.; Genant, H.K.; Wang, O.; Mitlak, B.H. Effect of parathyroid hormone (1-34) on fractures and bone mineral density in postmenopausal women with osteoporosis. N. Engl. J. Med., 2001, 344, 1434-1441.
2. Black, D.M.; Greenspan, S.L.; Ensrud, K.E.; Palermo, L.; McGowan, J.A.; Lang, T.F.; Garnero, P.; Bouxsein, M.L.; Bilezikian, J.P.; Rosen, C.J. The effects of parathyroid hormone and alendronate alone or in combination in postmenopausal osteoporosis. N. Engl. J. Med., 2003, 349, 1207-1215.
3. Finkelstein, J.S.; Hayes, A.; Hunzelman, J.L.; Wyland, J.J.; Lee, H.; Neer, R.M. The effects of parathyroid hormone, alendronate, or both in men with osteoporosis. N. Engl. J. Med., 2003, 349, 1216-1226.
4. Ma, Y.L.; Cain, R.L.; Halladay, D.L.; Yang, X.; Zeng, Q.; Miles, R.R.; Chandrasekhar, S.; Martin, T.J.; Onyia, J.E. Catabolic effects of continuous human PTH (1--38) in vivo is associated with sustained stimulation of RANKL and inhibition of osteoprotegerin and gene-associated bone formation. Endocrinology, 2001, 142, 4047-4054.
5. Frolik, C.A.; Black, E.C.; Cain, R.L.; Satterwhite, J.H.; Brown-Augsburger, P.L.; Sato, M.; Hock, J.M. Anabolic and catabolic bone effects of human parathyroid hormone (1-34) are predicted by duration of hormone exposure. Bone, 2003, 33, 372-379.
6. Huang, J.C.; Sakata, T.; Pfleger, L.L.; Bencsik, M.; Halloran, B.P.; Bikle, D.D.; Nissenson, R.A. PTH differentially regulates expression of RANKL and OPG. J. Bone Miner. Res., 2004, 19:235-244
7. Wang, Y.; Nishida, S.; Boudignon, B.M.; Burghardt, A.; Elalieh, H.Z.; Hamilton, M.M.; Majumdar, S.; Halloran, B.P.; Clemens, T.L.; Bikle, D.D. IGF-I receptor is required for the anabolic actions of parathyroid hormone on bone. J. Bone Miner. Res., 2007, 22, 1329-1337.
8. Nishida, S.; Yamaguchi, A.; Tanizawa, T.; Endo, N.; Mashiba, T.; Uchiyama, Y.; Suda, T.; Yoshiki, S.; Takahashi, H.E. Increased bone formation by intermittent parathyroid hormone administration is due to the stimulation of proliferation and differentiation of osteoprogenitor cells in bone marrow. Bone, 1994, 15, 717-723.
9. Wang, Y.H.; Liu, Y.; Buhl, K.; Rowe, D.W. Comparison of the action of transient and continuous PTH on primary osteoblast cultures expressing differentiation stage-specific GFP. J. Bone Miner. Res., 2005, 20, 5-14.
10. Koh, A.J.; Demiralp, B.; Neiva, K.G.; Hooten, J.; Nohutcu, R.M.; Shim, H.; Datta, N.S.; Taichman, R.S.; McCauley, L.K. Cells of the osteoclast lineage as mediators of the anabolic actions of parathyroid hormone in bone. Endocrinology, 2005, 146, 4584-4596.
11. Zhao, C.; Irie, N.; Takada, Y.; Shimoda, K.; Miyamoto, T.; Nishiwaki, T.; Suda, T.; Matsuo, K. Bidirectional ephrinB2-EphB4 signaling controls bone homeostasis. Cell Metab.; 2006, 4, 111-121.
12. Wang, Y.; Elalieh, H.; Chang, W.; Clemens, T.L.; Bikle, D. Ablation of IGF-I signaling drisrupts the communication between osteoblasts and osteoblasts. J. Bone Min. Res., 2007, 22, S241.
13. Kostenuik, P.J.; Harris, J.; Halloran, B.P.; Turner, R.T.; Morey-Holton, E.R.; Bikle, D.D. Skeletal unloading causes resistance of osteoprogenitor cells to parathyroid hormone and to insulin-like growth factor-I. J. Bone Miner. Res., 1999, 14, 21-31.
14. Wang, Y.; Nishida, S.; Elalieh, H.Z.; Long, R.K.; Halloran, B.P.; Bikle, D.D. Role of IGF-I signaling in regulating osteoclastogenesis. J. Bone Miner. Res., 2006, 21, 1350-1358.
15. Bikle, D.; Majumdar, S.; Laib, A.; Powell-Braxton, L.; Rosen, C.; Beamer, W.; Nauman, E.; Leary, C.; Halloran, B. The skeletal structure of insulin-like growth factor I-deficient mice. J. Bone Miner. Res., 2001, 16, 2320-2329.
16. Zhang, M.; Xuan, S.; Bouxsein, M.L.; von Stechow, D.; Akeno, N.; Faugere, M.C.; Malluche, H.; Zhao, G.; Rosen, C.J.; Efstratiadis, A.; Clemens, T.L. 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., 2002, 277, 44005-44012.
17. Wang, Y.; Long, R.; Elalieh, H.; Bikle, D. Ablation of IGF-I Signaling in Osteoprogenitors Decreases Bone Formation and Blunts the Skeletal Response to PTH. J. Bone Min. Res., 2008, 23, S55.
18. th Endocrine Society Annual Meeting, 2008, 112.
19. Chen, Q.; Kaji, H.; Iu, M.F.; Nomura, R.; Sowa, H.; Yamauchi, M.; Tsukamoto, T.; Sugimoto, T.; Chihara, K. Effects of an excess and a deficiency of endogenous parathyroid hormone on volumetric bone mineral density and bone geometry determined by peripheral quantitative computed tomography in female subjects. J. Clin. Endocrinol. Metab., 2003, 88, 4655-4658.
20. Miao, D.; He, B.; Lanske, B.; Bai, X.Y.; Tong, X.K.; Hendy, G.N.; Goltzman, D.; Karaplis, A.C. Skeletal abnormalities in Pth-null mice are influenced by dietary calcium. Endocrinology, 2004, 145, 2046-2053.
21. Dempster, D.W.; Cosman, F.; Kurlandm E.S.; Zhou, H.; Nieves, J.; Woelfert, L.; Shane, E.; Plavetic, K.; Muller, R.; Bilezikian, J.; Lindsay, R. Effects of daily treatment with parathyroid hormone on bone microarchitecture and turnover in patients with osteoporosis: a paired biopsy study. J. Bone Miner. Res., 2001, 16, 1846-1853.
22. Misof, B.M.; Roschger, P.; Cosman, F.; Kurland, E.S.; Tesch, W.; Messmer, P.; Dempster, D.W.; Nieves, J.; Shane, E.; Fratzl, P.; Klaushofer, K.; Bilezikian, J.; Lindsay, R. Effects of intermittent parathyroid hormone administration on bone mineralization density in iliac crest biopsies from patients with osteoporosis: a paired study before and after treatment. J. Clin. Endocrinol. Metab., 2003, 88, 1150-1156.
23. Bikle, D.D.; Sakata, T.; Leary, C.; Elalieh, H.; Ginzinger, D.; Rosen, C.J.; Beamer, W.; Majumdar, S.; Halloran, B.P. Insulin-like growth factor I is required for the anabolic actions of parathyroid hormone on mouse bone. J. Bone Miner. Res., 2002, 17, 1570-1578.
24. Wang, Y.; Sakata, T.; Elalieh, H.Z.; Munson, S.J.; Burghardt, A.; Majumdar, S.; Halloran, B.P.; Bikle, D.D. Gender differences in the response of CD-1 mouse bone to parathyroid hormone: potential role of IGF-I. J. Endocrinol., 2006, 189, 279-287.
25. Dempster, D.W.; Cosman, F.; Parisien, M.; Shen, V.; Lindsay, R. Anabolic actions of parathyroid hormone on bone. Endocr. Rev., 1993, 14, 690-709.
26. Halloran, B.P.; Bikle, D.D.; Harris, J.; Tanner, S.; Curren, T.; Morey-Holton, E. Regional responsiveness of the tibia to intermittent administration of parathyroid hormone as affected by skeletal unloading. J. Bone Miner. Res., 1997, 12, 1068-1074.
27. Iida-Klein, A, Zhou, H.; Lu, S.S.; Levine, L.R.; Ducayen-Knowles, M.; Dempster, D.W.; Nieves, J.; Lindsay, R. Anabolic action of parathyroid hormone is skeletal site specific at the tissue and cellular levels in mice. J. Bone Miner. Res., 17, 808-816.
28. Miao, D.; He, B.; Karaplis, A.C.; Goltzman, D. Parathyroid hormone is essential for normal fetal bone formation. J. Clin. Invest., 2002, 109, 1173-1182.
29. Goltzman, D. Studies on the mechanisms of the skeletal anabolic action of endogenous and exogenous parathyroid hormone. Arch. Biochem. Biophys., 2008, 473, 218-224.
30. Wang, Y.; Clemens, T.L.; Bikle, D.D.; Chang, W. Chondrocytespecific knockout of the IGF-IR impedes chondrocyte growth, survival, and differentiation. J. Bone Min. Res., 2006, 21, S50.
31. Rouleau, M.F.; Mitchell, J.; Goltzman, D. In vivo distribution of parathyroid hormone receptors in bone: evidence that a predominant osseous target cell is not the mature osteoblast. Endocrinology, 1988, 123, 187-191.
32. Lee, K.; Deeds, J.D.; Chiba, S.; Un-No, M.; Bond, A.T.; Segre, G.V. Parathyroid hormone induces sequential c-fos expression in bone cells in vivo: in situ localization of its receptor and c-fos messenger ribonucleic acids. Endocrinology, 1994, 134, 441-450.
33. Irie, K.; Ozawa, H. Immunohistochemical localization of parathyroid hormone/parathyroid hormone-related peptide receptor in rat tibiae. J. Bone Miner. Metab., 1996, 14, 10-14.
34. Dempster, D.W.; Hughes-Begos, C.E.; Plavetic-Chee, K.; Brandao-Burch, A.; Cosman, F.; Nieves, J.; Neubort, S.; Lu, S.S.; Iida-Klein, A.; Arnett, T.; Lindsay, R. Normal human osteoclasts formed from peripheral blood monocytes express PTH type 1 receptors and are stimulated by PTH in the absence of osteoblasts. J. Cell Biochem., 2005, 95, 139-148.
35. Merciris, D.; Marty, C.; Collet, C.; de Vernejoul, M.C.; Geoffroy, V. Overexpression of the transcriptional factor Runx2 in osteoblasts abolishes the anabolic effect of parathyroid hormone in vivo. Am. J. Pathol., 2007, 170, 1676-1685.
36. Jilka, R.L. 2007 Molecular and cellular mechanisms of the anabolic effect of intermittent PTH. Bone, 40, 1434-1446.
37. Onyia, J.E.; Bidwell, J.; Herring, J.; Hulman, J.; Hock, J.M. In vivo, human parathyroid hormone fragment (hPTH 1-34) transiently stimulates immediate early response gene expression, but not proliferation, in trabecular bone cells of young rats. Bone, 1995, 17, 479-484.
38. Swarthout, J.T.; D'Alonzo, R.C.; Selvamurugan, N.; Partridge, N.C. Parathyroid hormone-dependent signaling pathways regulating genes in bone cells. Gene, 2002, 282, 1-17.
39. Clohisy, J.C.; Scott, D.K.; Brakenhoff, K.D.; Quinn, C.O.; Partridge, N.C. Parathyroid hormone induces c-fos and c-jun messenger RNA in rat osteoblastic cells. Mol. Endocrinol., 1992, 6, 1834-1842.
40. Onishi, T.; Zhang, W.; Cao, X.; Hruska, K. The mitogenic effect of parathyroid hormone is associated with E2F-dependent activation of cyclin-dependent kinase 1 (cdc2) in osteoblast precursors. J. Bone Miner. Res., 1997, 12, 1596-1605.
41. Wang, Y.H.; Liu, Y.; Rowe, D.W. Effects of transient PTH on early proliferation, apoptosis, and subsequent differentiation of osteoblast in primary osteoblast cultures. Am. J. Physiol. Endocrinol. Metab., 292, 594-603.
42. Samadfam, R.; Xia, Q.; Goltzman, D. Co-treatment of PTH with osteoprotegerin or alendronate increases its anabolic effect on the skeleton of oophorectomized mice. J. Bone Miner. Res., 2007, 22, 55-63.
43. Allan, E.H.; Hausler, K.D.; Wei, T.; Gooi, J.H.; Quinn, J.M.; Crimeen-Irwin, B.; Pompolo, S.; Sims, N.A.; Gillespie, M.T.; Onyia, J.E.; Martin, T.J. EphrinB2 Regulation by Parathyroid Hormone (PTH) and PTHrP Revealed by Molecular Profiling in Differentiating Osteoblasts. J. Bone Miner. Res., 2008, 23, 1170-1181.
44. Lee, S.K.; Lorenzo, J.A. Parathyroid hormone stimulates TRANCE and inhibits osteoprotegerin messenger ribonucleic acid expression in murine bone marrow cultures: correlation with osteoclast-like cell formation. Endocrinology, 1999, 140, 3552-3561.
45. Centrella, M.; Christakos, S.; McCarthy, T.L. Skeletal hormones and the C/EBP and Runx transcription factors: interactions that integrate and redefine gene expression. Gene, 2004, 342, 13-24.
46. Yang, D.; Singh, R.; Divieti, P.; Guo, J.; Bouxsein, M.L.; Bringhurst, F.R. Contributions of parathyroid hormone (PTH)/PTH-related peptide receptor signaling pathways to the anabolic effect of PTH on bone. Bone, 2007, 40, 1453-1461.
47. Kulkarni, N.H.; Halladay, D.L.; Miles, R.R.; Gilbert, L.M.; Frolik, C.A.; Galvin R.J.; Martin, T.J.; Gillespie, M.T.; Onyia, J.E. Effects of parathyroid hormone on Wnt signaling pathway in bone. J. Cell Biochem., 2005, 95, 1178-1190.
48. Suzuki, A.; Ozono, K.; Kubota, T.; Kondou, H.; Tachikawa, K.; Michigami, T. PTH/cAMP/PKA signaling facilitates canonical Wnt signaling via inactivation of glycogen synthase kinase-3beta in osteoblastic Saos-2 cells. J. Cell Biochem., 104, 304-317.
49. Keller, H.; Kneissel, M. SOST is a target gene for PTH in bone. Bone, 2005, 37, 148-158.
50. Sawakami, K.; Robling, A.G.; Ai, M.; Pitner, N.D.; Liu, D.; Warden, S.J.; Li, J.; Maye, P.; Rowe, D.W.; Duncan, R.L.; Warman, M.L.; Turner, C.H. The Wnt co-receptor LRP5 is essential for skeletal mechanotransduction but not for the anabolic bone response to parathyroid hormone treatmet. J. Biol. Chem., 2006, 281, 23698-23711.
51. Iwaniec, U.T.; Wronski, T.J.; Liu, J.; Rivera, M.F.; Arzaga, R.R.; Hansen, G.; Brommage, R. PTH stimulates bone formation in mice deficient in Lrp5. J. Bone Miner. Res., 2007, 22, 394-402.
52. Canalis, E.; Centrella, M.; Burch, W.; McCarthy, T.L. Insulin-like growth factor I mediates selective anabolic effects of parathyroid hormone in bone cultures. J. Clin. Invest., 1989, 83, 60-65.
53. Pfeilschifter, J.; Laukhuf, F.; Muller-Beckmann, B.; Blum, W.F.; Pfister, T.; Ziegler, R. Parathyroid hormone increases the concentration of insulin-like growth factor-I and transforming growth factor beta 1 in rat bone. J. Clin. Invest., 1995., 96, 767-774.
54. Watson, P.; Lazowski, D.; Han, V.; Fraher, L.; Steer, B.; Hodsman, A. Parathyroid hormone restores bone mass and enhances osteoblast insulin-like growth factor I gene expression in ovariectomized rats. Bone, 1995, 16, 357-365.
55. Linkhart, T.A.; Mohan, S. Parathyroid hormone stimulates release of insulin-like growth factor-I (IGF-I) and IGF-II from neonatal mouse calvaria in organ culture. Endocrinology, 1989, 125, 1484-1491.
56. Lazowski, D.A.; Fraher, L.J.; Hodsman, A.; Steer, B.; Modrowski, D.; Han, V.K. Regional variation of insulin-like growth factor-I gene expression in mature rat bone and cartilage. Bone, 1994, 15, 563-576.
57. Locklin, R.M.; Khosla, S.; Turner, R.T.; Riggs, B.L. Mediators of the biphasic responses of bone to intermittent and continuously administered parathyroid hormone. J. Cell Biochem., 2003, 89, 180-190.
58. Hock, J.M.; Canalis, E.; Centrella, M. Transforming growth factorbeta stimulates bone matrix apposition and bone cell replication in cultured fetal rat calvariae. Endocrinology, 1990, 126, 421-426.
59. White, H.D.; Ahmad, A.M.; Durham, B.H.; Patwala, A.; Whittingham, P.; Fraser, W.D.; Vora, J.P. Growth hormone replacement is important for the restoration of parathyroid hormone sensitivity and improvement in bone metabolism in older adult growth hormone-deficient patients. J. Clin. Endocrinol. Metab., 2005, 90, 3371-3380.
60. Le Roith, D.; Bondy, C.; Yakar, S.; Liu, J.L.; Butler, A. The somatomedin hypothesis: 2001. Endocr Rev., 2001, 22, 53-74.
61. LeRoith, D.; Werner, H.; Beitner-Johnson, D.; Roberts, C.T. Jr. Molecular and cellular aspects of the insulin-like growth factor I receptor. Endocr. Rev., 1995, 16, 143-163.
62. Yakar, S.; Liu, J.L.; Stannard, B.; Butler, A.; Accili, D.; Sauer, B.; LeRoith, D. Normal growth and development in the absence of hepatic insulin-like growth factor I. Proc. Natl. Acad. Sci. USA, 1999, 96, 7324-7329.
63. Yakar, S.; Rosen, C.J.; Beamer, W.G.; Ackert-Bicknell, C.L.; Wu, Y.; Liu, J.L.; Ooi, G.T.; Setser, J.; Frystyk, J.; Boisclair, Y.R.; LeRoith, D. Circulating levels of IGF-1 directly regulate bone growth and density. J. Clin. Invest., 2002, 110, 771-781.
64. Zhao, G.; Monier-Faugere, M.C.; Langub, M.C.; Geng, Z.; Nakayama, T.; Pike, J.W.; Chernausek, S.D.; Rosen, C.J.; Donahue, L.R.; Malluche, H.H.; Fagin, J.A.; Clemens, T.L. Targeted overexpression of insulin-like growth factor I to osteoblasts of transgenic mice: increased trabecular bone volume without increased osteoblast proliferation. Endocrinology, 2000, 141, 2674-2682.
65. Clemens, T.L.; Chernausek, S.D. Genetic strategies for elucidating insulin-like growth factor action in bone. Growth Horm. IGF Res., 2004, 14, 195-199.
66. Hoeflich, A.; Gotz, W.; Lichanska, A.M.; Bielohuby, M.; Tonshoff, B.; Kiepe, D. Effects of insulin-like growth factor binding proteins in bone--a matter of cell and site. Arch. Physiol. Biochem., 2007, 113,142-153.
67. Eckstein, F.; Pavicic, T.; Nedbal, S.; Schmidt, C.; Wehr, U.; Rambeck, W.; Wolf, E.; Hoeflich, A. Insulin-like growth factorbinding protein-2 (IGFBP-2) overexpression negatively regulates bone size and mass, but not density, in the absence and presence of growth hormone/IGF-I excess in transgenic mice. Anat. Embryol., 2002, 206, 139-148.
68. Palermo, C.; Manduca, P.; Gazzerro, E.; Foppiani, L.; Segat, D.; Barreca, A. Potentiating role of IGFBP-2 on IGF-II-stimulated alkaline phosphatase activity in differentiating osteoblasts. Am. J. Physiol. Endocrinol. Metab., 2004, 286, E648-657.
69. Khosla, S.; Hassounm A.A.; Baker, B.K.; Liu, F.; Zein, N.N.; Whyte, M.P.; Reasner, C.A.; Nippoldt, T.B.; Tiegs, R.D.; Hintz, R.L.; Conover, C.A. Insulin-like growth factor system abnormalities in hepatitis C-associated osteosclerosis. Potential insights into increasing bone mass in adults. J. Clin. Invest., 1998, 101, 2165-2173.
70. Silha, J.V.; Mishra, S.; Rosen, C.J.; Beamer, W.G.; Turner, R.T.; Powell, D.R.; Murphy, L.J. Perturbations in bone formation and resorption in insulin-like growth factor binding protein-3 transgenic mice. J. Bone Miner. Res., 2003, 18, 1834-1841.
71. Bagi, C.M.; DeLeon, E.; Brommage, R.; Rosen, D.; Sommer, A. Treatment of ovariectomized rats with the complex of rhIGFI/IGFBP-3 increases cortical and cancellous bone mass and improves structure in the femoral neck. Calcif. Tissue Int., 57, 40-46.
72. Zhang, M.; Faugere, M.C.; Malluche, H.; Rosen, C.J.; Chernausek, S.D.; Clemens, T.L. Paracrine overexpression of IGFBP-4 in osteoblasts of transgenic mice decreases bone turnover and causes global growth retardation. J. Bone Miner. Res., 2003, 18, 836-843.
73. Qin, X.; Wergedal, J.E.; Rehage, M.; Tran, K.; Newton, J.; Lam, P.; Baylink, D.J.; Mohan, S. Pregnancy-associated plasma protein-A increases osteoblast proliferation in vitro and bone formation in vivo. Endocrinology, 2006, 147, 5653-5661.
74. Devlin, R.D.; Du, Z.; Buccilli, V.; Jorgetti, V.; Canalis, E. Transgenic mice overexpressing insulin-like growth factor binding protein-5 display transiently decreased osteoblastic function and osteopenia. Endocrinology, 2002, 143, 3955-3962.
75. Salih, D.A.; Mohan, S.; Kasukawa, Y.; Tripathi, G.; Lovett, F.A.; Anderson, N.F.; Carter, E.J.; Wergedal, J.E.; Baylink, D.J.; Pell, J.M. Insulin-like growth factor-binding protein-5 induces a genderrelated decrease in bone mineral density in transgenic mice. Endocrinology, 2005, 146, 931-940.
76. Andress, D.L. IGF-binding protein-5 stimulates osteoblast activity and bone accretion in ovariectomized mice. Am. J. Physiol. Endocrinol. Metab., 2001, 281, 283-288.
77. Mohan, S.; Nakao, Y.; Honda, Y.; Landale, E.; Leser, U.; Dony, C.; Lang, K.; Baylink, D.J. Studies on the mechanisms by which insulin-like growth factor (IGF) binding protein-4 (IGFBP-4) and IGFBP-5 modulate IGF actions in bone cells. J. Biol. Chem., 1995, 270, 20424-20431.
78. Erclik, M.S.; Mitchell, J. Activation of the insulin-like growth factor binding protein-5 promoter by parathyroid hormone in osteosarcoma cells requires activation of an activated protein-2 element. J. Mol. Endocrinol., 2005, 34, 713-722.
79. Liu, J.P.; Baker. J.; Perkins, A.S.; Robertson, E.J.; Efstratiadis, A. Mice carrying null mutations of the genes encoding insulin-like growth factor I (Igf-1) and type 1 IGF receptor (Igf1r). Cell, 1993, 75, 59-72.
80. Baker. J.; Liu, J.P.; Robertson, E.J.; Efstratiadis, A. Role of insulinlike growth factors in embryonic and postnatal growth. Cell, 1993, 75, 73-82.
81. Camacho-Hubner, C.; Woods, K.A.; Clark, A.J.; Savage, M.O. Insulin-like growth factor (IGF)-I gene deletion. Rev. Endocr. Metab. Disord., 2002, 3, 357-361.
82. Hou, P.; Sato, T.; Hofstetter, W.; Foged, N.T. Identification and characterization of the insulin-like growth factor I receptor in mature rabbit osteoclasts. J. Bone Miner. Res., 12, 534-540.
83. Fiorelli, G.; Formigli, L.; Zecchi Orlandini, S.; Gori, F.; Falchetti, A.; Morelli, A.; Tanini, A.; Benvenuti, S.; Brandi, M.L. Characterization and function of the receptor for IGF-I in human preosteoclastic cells. Bone, 1996, 18, 269-276.
84. Hayden, J.M.; Mohan. S.; Baylink, D.J. The insulin-like growth factor system and the coupling of formation to resorption. Bone, 1995, 17, 93S-98S.
85. Hill, P.A.; Reynolds, J.J.; Meikle, M.C. Osteoblasts mediate insulin-like growth factor-I and-II stimulation of osteoclast formation and function. Endocrinology, 1995, 136,124-131.
86. Rubin, J.; Ackert-Bicknell, C.L.; Zhu, L.; Fan, X.; Murphy, T.C.; Nanes, M.S.; Marcus, R.; Holloway, L.; Beamer, W.G.; Rosen, C.J. IGF-I regulates osteoprotegerin (OPG) and receptor activator of nuclear factor-kappaB ligand in vitro and OPG in vivo. J. Clin. Endocrinol. Metab., 2002, 87, 4273-4279.
87. Govoni, K.E.; Wergedal, J.E.; Florin, L.; Angel, P.; Baylink, D.J.; Mohan, S. Conditional deletion of insulin-like growth factor-I in collagen type 1alpha2-expressing cells results in postnatal lethality and a dramatic reduction in bone accretion. Endocrinology, 2007, 148, 5706-5715.