Effects of systemic and local administration of recombinant human IGF-I (rhIGF-I) on de novo bone formation in an aged mouse model

Journal of Bone and Mineral Research

Volumn 21, Issue 9, 2006, Pages 1359-1366

  Fowlkes, John L ^a,b   Thrailkill, Kathryn M ^a   Liu, Lichu ^b   Wahl, Elizabeth C ^b   Bunn, Robert C ^a   Cockrell, Gael E ^a   Perrien, Daniel S ^a,c   Aronson, James ^c   Lumpkin Jr , Charles K ^a  

^a UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^b ARKANSAS CHILDREN S HOSPITAL   (United States)

^c UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

Author keywords

Aging; Anabolic agents; Distraction osteogenesis; Limb lengthening; Osteoporosis

Indexed keywords

ANABOLIC AGENT; OSTEOCALCIN; RECOMBINANT SOMATOMEDIN C; SOMATOMEDIN C;

AGING; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE REGENERATION; COMPUTER ASSISTED TOMOGRAPHY; CONTROLLED STUDY; DISTRACTION OSTEOGENESIS; DRUG EFFECT; ENZYME IMMUNOASSAY; ENZYME LINKED IMMUNOSORBENT ASSAY; HISTOPATHOLOGY; MALE; MOUSE; NONHUMAN; OSMOTIC MINIPUMP; OSSIFICATION; OSTEOBLAST; OSTEOBLASTOGENESIS; OSTEOPOROSIS; OSTEOTOMY; RADIOGRAPHY;

AGING; ANIMALS; ELECTRON PROBE MICROANALYSIS; HUMANS; INJECTIONS, INTRALESIONAL; INSULIN-LIKE GROWTH FACTOR I; MALE; MICE; MICE, INBRED C57BL; MODELS, ANIMAL; MODELS, BIOLOGICAL; OSTEOGENESIS; OSTEOTOMY; RECOMBINANT PROTEINS; TIBIA;

EID: 33748051393     PISSN: 08840431     EISSN: None     Source Type: Journal    
DOI: 10.1359/jbmr.060618     Document Type: Article

References (58)

1. Margolis RN, Canalis E, Partridge NC 1996 Invited review of a workshop: Anabolic hormones in bone: Basic research and therapeutic potential. J Clin Endocrinol Metab 81:872-877.
2. Mohan S, Baylink DJ 1996 Insulin-like growth factor system components and the coupling of bone formation to resorption. Horm Res 45(Suppl 1):59-62.
3. Ohlsson C, Bengtsson BA, Isaksson OG, Andreassen TT, Slootweg MC 1998 Growth hormone and bone. Endocr Rev 19:55-79.
4. Baker J, Liu JP, Robertson EJ, Efstratiadis A 1993 Role of insulin-like growth factors in embryonic and postnatal growth. Cell 75:73-82.
5. Liu JP, Baker J, Perkins AS, Robertson EJ, Efstratiadis A 1993 Mice carrying null mutations of the genes encoding insulin-like growth factor I (Igf-1) and type 1 IGF receptor (Igf1r). Cell 75:59-72.
6. Bikle D, Majumdar S, Laib A, Powell-Braxton L, Rosen C, Beamer W, Nauman E, Leary C, Halloran B 2001 The skeletal structure of insulin-like growth factor I-deficient mice. J Bone Miner Res 16:2320-2329.
7. Miyakoshi N, Qin X, Kasukawa Y, Richman C, Srivastava AK, Baylink DJ, Mohan S 2001 Systemic administration of insulin-like growth factor (IGF)-binding protein-4 (IGFBP-4) increases bone formation parameters in mice by increasing IGF bioavailability via an IGFBP-4 protease-dependent mechanism. Endocrinology 142:2641-2648.
8. Sjogren K, Sheng M, Moverare S, Liu JL, Wallenius K, Tornell J, Isaksson O, Jansson JO, Mohan S, Ohlsson C 2002 Effects of liver-derived insulin-like growth factor I on bone metabolism in mice. J Bone Miner Res 17:1977-1987.
9. Wong GL, Kotliar D, Schlaeger D, Brandes SJ 1990 IGF-I production by mouse osteoblasts. J Bone Miner Res 5:133-140.
10. Thrailkill KM, Siddhanti SR, Fowlkes JL, Quarles LD 1995 Differentiation of MC3T3-E1 osteoblasts is associated with temporal changes in the expression of IGF-I and IGFBPs. Bone 17:307-313.
11. Slootweg MC, van Buul-Offers SC, Hoogerbrugge CM, Herrmann-Erlee MP, van den Eijnden-van Raaij AJ, Duursma SA, van Zoelen EJ 1990 Characterization of growth factor activity produced by fetal mouse osteoblasts. J Endocrinol 124:301-309.
12. Mohan S, Baylink DJ 1991 Bone growth factors. Clin Orthop 263:30-48.
13. Canalis E, Centrella M, Burch W, McCarthy TL 1989 Insulin-like growth factor I mediates selective anabolic effects of parathyroid hormone in bone cultures. J Clin Invest 83:60-65.
14. Swolin D, Brantsing C, Matejka G, Ohlsson C 1996 Cortisol decreases IGF-I mRNA levels in human osteoblast-like cells. J Endocrinol 149:397-403.
15. Slootweg MC, Hoogerbrugge CM, de Poorter TL, Duursma SA, van Buul-Offers SC 1990 The presence of classical insulin-like growth factor (IGF) type-I and -II receptors on mouse osteoblasts: Autocrine/paracrine growth effect of IGFs? J Endocrinol 125:271-277.
16. Okazaki R, Conover CA, Harris SA, Spelsberg TC, Riggs BL 1995 Normal human osteoblast-like cells consistently express genes for insulin-like growth factors I and II but transformed human osteoblast cell lines do not. J Bone Miner Res 10:788-795.
17. Kanzaki S, Baxter RC, Knutsen R, Baylink DJ, Mohan S 1995 Evidence that human bone cells in culture secrete insulin-like growth factor (IGF)-II and IGF binding protein-3 but not acid-labile subunit both under basal and regulated conditions. J Bone Miner Res 10:854-858.
18. Schmid C, Schlapfer I, Gosteli-Peter MA, Froesch ER, Zapf J 1995 Expression, effects, and fate of IGFBP-5 are different in normal and malignant osteoblastic cells. Prog Growth Factor Res 6:167-173.
19. Bautista CM, Baylink DJ, Mohan S 1991 Isolation of a novel insulin-like growth factor (IGF) binding protein from human bone: A potential candidate for fixing IGF-II in human bone. Biochem Biophys Res Commun 176:756-763.
20. Mohan S, Baylink DJ 1997 Serum insulin-like growth factor binding protein (IGFBP)-4 and IGFBP-5 levels in aging and age-associated diseases. Endocrine 7:87-91.
21. Aronson J, Liu L, Liu Z, Gao GG, Perrien DS, Brown EC, Skinner RA, Thomas J, Morris K, Suva L, Badger TM, Lumpkin CK Jr 2002 Decreased endosteal intramembranous bone formation accompanies aging in a mouse model of distraction osteogenesis. J Regenerative Med 3:7-16.
22. Aronson J, Shen XC, Gao GG, Miller F, Quattlebaum T, Skinner RA, Badger TM, Lumpkin CK Jr 1997 Sustained proliferation accompanies distraction osteogenesis in the rat. J Orthop Res 15:563-569.
23. Perrien DS, Brown EC, Aronson J, Skinner RA, Montague DC, Badger TM, Lumpkin CK Jr 2002 Immunohistochemical study of osteopontin expression during distraction osteogenesis in the rat. J Histochem Cytochem 50:567-574.
24. Thrailkill KM, Liu L, Wahl EC, Bunn RC, Perrien DS, Cockrell GE, Skinner RA, Hogue WR, Carver AA, Fowlkes JL, Aronson J, Lumpkin CK 2005 Bone Formation Is Impaired in a Model of Type 1 Diabetes. Diabetes 54:2875-2881.
25. Aronson J 2004 Modulation of distraction osteogenesis in the aged rat by fibroblast growth factor. Clin Orthop Relat Res 425:264-283.
26. Yakar S, Rosen CJ, Beamer WG, Ackert-Bicknell CL, Wu Y, Liu JL, Ooi GT, Setser J, Frystyk J, Boisclair YR, LeRoith D 2002 Circulating levels of IGF-1 directly regulate bone growth and density. J Clin Invest 110:771-781.
27. Bouxsein ML, Rosen CJ, Turner CH, Ackert CL, Shultz KL, Donahue LR, Churchill G, Adamo ML, Powell DR, Turner RT, Muller R, Beamer WG 2002 Generation of a new congenic mouse strain to test the relationships among serum insulin-like growth factor I, bone mineral density, and skeletal morphology in vivo. J Bone Miner Res 17:570-579.
28. Zhang M, Xuan S, Bouxsein ML, von Stechow D, Akeno N, Faugere MC, Malluche H, Zhao G, Rosen CJ, Efstratiadis A, Clemens TL 2002 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.
29. Zhao G, Monier-Faugere MC, Langub MC, Geng Z, Nakayama T, Pike JW, Chernausek SD, Rosen CJ, Donahue LR, Malluche HH, Fagin JA, Clemens TL 2000 Targeted overexpression of insulin-like growth factor I to osteoblasts of transgenic mice: Increased trabecular bone volume without increased osteoblast proliferation. Endocrinology 141:2674-2682.
30. Jiang J, Lichtler AC, Gronowicz GA, Adams DJ, Clark SH, Rosen CJ, Kream BE 2006 Transgenic mice with osteoblast-targeted insulin-like growth factor-I show increased bone remodeling. Bone (in press).
31. Schmidmaier G, Wildemann B, Bail H, Lucke M, Fuchs T, Stemberger A, Flyvbjerg A, Haas NP, Raschke M 2001 Local application of growth factors (insulin-like growth factor-1 and transforming growth factor-beta1) from a biodegradable poly(D,L-lactide) coating of osteosynthetic implants accelerates fracture healing in rats. Bone 28:341-350.
32. Wakisaka A, Tanaka H, Barnes J, Liang CT 1998 Effect of locally infused IGF-I on femoral gene expression and bone turnover activity in old rats. J Bone Miner Res 13:13-19.
33. Meinel L, Zoidis E, Zapf J, Hassa P, Hottiger MO, Auer JA, Schneider R, Gander B, Luginbuehl V, Bettschart-Wolfisberger R, Illi OE, Merkle HP, von Rechenberg B 2003 Localized insulin-like growth factor I delivery to enhance new bone formation. Bone 33:660-672.
34. Bach LA, Rechler MM 1995 Insulin-like growth factor binding proteins. Diabetes Rev 3:38-61.
35. Jones JI, Clemmons DR 1995 Insulin-like growth factors and their binding proteins: Biological actions. Endocr Rev 16:3-34.
36. Oh Y, Nagalla SR, Yamanaka Y, Kim HS, Wilson E, Rosenfeld RG 1996 Synthesis and characterization of insulin-like growth factor-binding protein (IGFBP)-7. Recombinant human mac25 protein specifically binds IGF-I and -II. J Biol Chem 271:30322-30325.
37. Rechler MM 1993 Insulin-like growth factor binding proteins. Vitamin Horm 47:1-114.
38. Rechler MM 1995 Non-receptor-binding proteins for insulin-like growth factors and other cytokines: Modulators of peptide action. In: Weintraub BD (ed.) Molecular Endocrinology: Basic Concepts and Clinical Correlations. Raven Press, New York, NY, USA, pp. 155-180.
39. Mohan S, Bautista CM, Wergedal J, Baylink DJ 1989 Isolation of an inhibitory insulin-like growth factor (IGF) binding protein from bone cell-conditioned medium: A potential local regulator of IGF action. Proc Natl Acad Sci USA 86:8338-8342.
40. Andress DL, Birnbaum RS 1992 Human osteoblast-derived insulin-like growth factor (IGF) binding protein-5 stimulates osteoblast mitogenesis and potentiates IGF action. J Biol Chem 267:22467-22472.
41. Andress DL, Loop SM, Zapf J, Kiefer MC 1993 Carboxy-truncated insulin-like growth factor binding protein-5 stimulates mitogenesis in osteoblast-like cells. Biochem Biophys Res Commun 195:25-30.
42. Campbell PG, Novak JF, Yanosick TB, McMaster JH 1992 Involvement of the plasmin system in dissociation of the insulin-like growth factor-binding protein complex. Endocrinology 130:1401-1412.
43. Conover CA, Kiefer MC 1993 Regulation and biological effect of endogenous insulin-like growth factor binding protein-5 in human osteoblastic cells. J Clin Endocrinol Metab 76:1153-1159.
44. Hakeda Y, Kawaguchi H, Hurley M, Pilbeam CC, Abreu C, Linkhart TA, Mohan S, Kumegawa M, Raisz LG 1996 Intact insulin-like growth factor binding protein-5 (IGFBP-5) associates with bone matrix and the soluble fragments of IGFBP-5 accumulated in culture medium of neonatal mouse calvariae by parathyroid hormone and prostaglandin E2-treatment. J Cell Physiol 166:370-379.
45. Mohan S, Nakao Y, Honda Y, Landale E, Leser U, Dony C, Lang K, Baylink DJ 1995 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 270:20424-20431.
46. Nam TJ, Busby WH Jr, Rees C, Clemmons DR 2000 Thrombospondin and osteopontin bind to insulin-like growth factor (IGF)-binding protein-5 leading to an alteration in IGF-I-stimulated cell growth. Endocrinology 141:1100-1106.
47. Jones JI, Gockerman A, Busby WH Jr, Camacho-Hubner C, Clemmons DR 1993 Extracellular matrix contains insulin-like growth factor binding protein-5: Potentiation of the effects of IGF-I. J Cell Biol 121:679-687.
48. Fowlkes JL, Enghild JJ, Suzuki K, Nagase H 1994 Matrix metalloproteinases degrade insulin-like growth factor-binding protein-3 in dermal fibroblast cultures. J Biol Chem 269:25742-25746.
49. Fowlkes JL, Serra DM, Bunn RC, Thrailkill KM, Enghild JJ, Nagase H 2004 Regulation of insulin-like growth factor (IGF)-I action by matrix metalloproteinase-3 involves selective disruption of IGF-I/IGF-binding protein-3 complexes. Endocrinology 145:620-626.
50. Fowlkes JL, Suzuki K, Nagase H, Thrailkill KM 1994 Proteolysis of insulin-like growth factor binding protein-3 during rat pregnancy: A role for matrix metalloproteinases. Endocrinology 135:2810-2813.
51. Thrailkill KM, Quarles LD, Nagase H, Suzuki K, Serra DM, Fowlkes JL 1995 Characterization of insulin-like growth factor-binding protein 5-degrading proteases produced throughout murine osteoblast differentiation. Endocrinology 136:3527-3533.
52. Carvalho RS, Einhorn TA, Lehmann W, Edgar C, Al-Yamani A, Apazidis A, Pacicca D, Clemens TL, Gerstenfeld LC 2004 The role of angiogenesis in a murine tibial model of distraction osteogenesis. Bone 34:849-861.
53. Grinspoon S, Thomas L, Miller K, Herzog D, Klibanski A 2002 Effects of recombinant human IGF-I and oral contraceptive administration on bone density in anorexia nervosa. J Clin Endocrinol Metab 87:2883-2891.
54. Kasukawa Y, Stabnov L, Miyakoshi N, Baylink DJ, Mohan S 2002 Insulin-like growth factor I effect on the number of osteoblast progenitors is impaired in ovariectomized mice. J Bone Miner Res 17:1579-1587.
55. Boonen S, Rosen C, Bouillon R, Sommer A, McKay M, Rosen D, Adams S, Broos P, Lenaerts J, Raus J, Vanderschueren D, Geusens P 2002 Musculoskeletal effects of the recombinant human IGF-I/IGF binding protein-3 complex in osteoporotic patients with proximal femoral fracture: A double-blind, placebo-controlled pilot study. J Clin Endocrinol Metab 87:1593-1599.
56. Kemp SF, Thrailkill KM 2005 SomatoKine: Is there a use in treating growth disorders? Curr Opin Investig Drugs 6:373-377.
57. Thrailkill KM 2000 Insulin-like growth factor-I in diabetes mellitus: Its physiology, metabolic effects, and potential clinical utility. Diabetes Technol Ther 2:69-80.
58. Kaaks R 2004 Nutrition, insulin, IGF-1 metabolism and cancer risk: A summary of epidemiological evidence. Novartis Found Symp 262:247-268.