47
Views
16
CrossRef citations to date
0
Altmetric
Review

Skeletal actions of insulin-like growth factors

&
Pages 47-56 | Published online: 10 Jan 2014

References

  • Juul A. Serum levels of insulin-like growth factor I and its binding proteins in health and disease. Growth Horm. IGF Res. 13, 113–170 (2003).
  • Efstratiadis A. Genetics of mouse growth. Int. J. Dev. Biol. 42, 955–976 (1998).
  • Clemens TL, Chernausek SD. Genetic strategies for elucidating insulin-like growth factor action in bone. Growth Horm. IGF Res. 14, 195–199 (2004).
  • Davey RA, MacLean HE, McManus JF, Findlay DM, Zajac JD. Genetically modified animal models as tools for studying bone and mineral metabolism. J. Bone. Miner. Res. 19, 882–892 (2004).
  • Collett-Solberg PF, Cohen P. Genetics, chemistry, and function of the IGF/IGFBP system. Endocrine 12, 121–136 (2000).
  • Soon L, Flechner L, Gutkind JS et al. Insulin-like growth factor I synergizes with interleukin-4 for hematopoietic cell proliferation independent of insulin receptor substrate expression. Mol. Cell Biol. 19, 3816–3828 (1999).
  • Grey A, Chen Q, Xu X, Callon K, Cornish J. Parallel phosphatidylinositol-3 kinase and p42/44 mitogen-activated protein kinase signaling pathways subserve the mitogenic and antiapoptotic actions of insulin-like growth factor I in osteoblastic cells. Endocrinology144,4886–4893 (2003).
  • Hall K, Hilding A, Thoren M. Determinants of circulating insulin-like growth factor-I. J. Endocrinol. Invest. 22, 48–57 (1999).
  • Clayton PE, Hall CM. Insulin-like growth factor I levels in healthy children. Horm. Res. 62, 2–7 (2004).
  • Boisclair YR, Rhoads RP, Ueki I, Wang, J, Ooi GT. The acid-labile subunit (ALS) of the 150 kDa IGF-binding protein complex: an important but forgotten component of the circulating IGF system. J. Endocrinol. 170, 63–70 (2001).
  • Holly JM, Perks CM, Stewart CE. Overview of insulin-like growth factor physiology. Growth Horm. IGF Res. 10 (Suppl A), S8–S9 (2000).
  • Le Roith D, Bondy C, Yakar S, Liu JL, Butler A. The somatomedin hypothesis: 2001. Endocr. Rev. 22, 53–74 (2001).
  • Woods KA, Camacho-Hubner C, Savage MO, Clark AJ. Intrauterine growth retardation and postnatal growth failure associated with deletion of the insulin-like growth factor I gene. N. Engl. J. Med. 335, 1363–1367 (1996).
  • van der Eerden BC, Karperien M, Wit JM. Systemic and local regulation of the growth plate. Endocr. Rev. 24, 782–801 (2003).
  • Guler HP, Zapf J, Scheiwiller E, Froesch ER. Recombinant human insulin-like growth factor I stimulates growth and has distinct effects on organ size in hypophysectomized rats. Pro. Natl. Acad. Sci. USA 85, 4889–4893 (1988).
  • Liu JP, Baker J, Perkins AS, Robertson EJ, Efstratiadis A. 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 (1993).
  • Wang J, Zhou J, Bondy CA. Igf1 promotes longitudinal bone growth by insulin-like actions augmenting chondrocyte hypertrophy. FASEB J. 13, 1985–1990 (1999).
  • DeChiara TM, Efstratiadis A, Robertson EJ. A growth-deficiency phenotype in heterozygous mice carrying an insulin-like growth factor II gene disrupted by targeting. Nature 345, 78–80 (1990).
  • Hoshi K, Ogata N, Shimoaka T, Terauchi Y et al. Deficiency of insulin receptor substrate-1 impairs skeletal growth through early closure of epiphyseal cartilage. J. Bone. Miner. Res. 19, 214–223 (2004).
  • Salmon WD Jr, Daughaday WH. A hormonally controlled serum factor which stimulates sulfate incorporation by cartilage in vitro. J. Lab. Clin. Med. 49, 825–836 (1957).
  • Isaksson OGP, Lindhal A, Nilsson A, Isgaard J. Mechanism of the stimulatory effect of growth hormone on longitudinal bone growth. Endocr. Rev. 8, 426–438 (1987).
  • Ohlsson C, Nilsson A, Isaksson O, Lindhal A. Growth hormone induces multiplication of the slowly cycling germinal cells of the rat tibial growth plate. Proc. Natl. Acad. Sci. USA 89, 9826–9830 (1992).
  • Barnard R, Haynes KM, Werther GA,Waters MJ. The ontogeny of growth hormone receptors in the rabbit tibia. Endocrinology 122, 2562–2569 (1988).
  • Werther GA, Haynes K, Edmonson S et al. Identification of growth hormone receptors on human growth plate chondrocytes. Acta. Paediatr. Suppl. 82 (Suppl. 391), 50–53 (1993).
  • Bentham J, Ohlsson C, Lindhal A, Isaksson O, Nilsson A. A double-staining technique for detection of growth hormone and insulin-like growth factor-I binding to rat tibial epiphyseal chondrocytes. J. Endocrinol. 137, 361–367 (1993).
  • Lupu F, Terwilliger JD, Lee K, Segre GV, Efstratiadis A. Roles of growth hormone and insulin-like growth factor 1 in mouse postnatal growth. Dev. Biol. 229, 141–162 (2001).
  • Yakar S, Liu JL, Stannard B et al. Normal growth and development in the absence of hepatic insulin-like growth factor-I. Proc. Natl. Acad. Sci. USA 96, 7324–7329 (1999).
  • Yakar S, Rosen CJ, Beamer WG, Ackert-Bicknell CL et al. Circulating levels of IGF-1 directly regulate bone growth and density. J. Clin. Invest. 110, 771–781 (2002).
  • Yakar S, Pennisi P, Wu Y, Zhao H, LeRoith D. Clinical relevance of systemic and local IGF-I. Endocr. Dev. 9, 11–16 (2005).
  • Ueki I, Ooi GT, Tremblay ML, Hurst KR, Bach LA, Boisclair YR. Inactivation of the acid labile subunit gene in mice results in mild retardation of postnatal growth despite profound disruptions in the circulating insulin-like growth factor system. Proc. Natl. Acad. Sci. USA 97, 6868–6873 (2000).
  • Martel-Pelletier J, Di Battista JA, Lajeunesse D, Pelletier JP. IGF/IGFBP axis in cartilage and bone in osteoarthritis pathogenesis. Inflamm. Res. 47, 90–100 (1998).
  • Shen FH, Visger JM, Balian G, Hurwitz SR, Diduch DR. Systemically administered mesenchymal stromal cells transduced with insulin-like growth factor-I localize to a fracture site and potentiate healing. J. Orthop. Trauma 16, 651–659 (2002).
  • Prockop DJ, Gregory CA, Spees JL. One strategy for cell and gene therapy: harnessing the power of adult stem cells to repair tissues. Proc. Natl. Acad. Sci. USA 100 (Suppl. 1), 11917–11923 (2003).
  • Spagnoli A, Longobardi L, O’Rear L. Cartilage disorders: potential therapeutic use of mesenchymal stem cells. Endocr. Dev. 9, 17–30 (2005).
  • Canalis E. The fate of circulating osteoblasts. N. Engl. J. Med. 352, 2014–2016 (2005).
  • Conover CA. In vitro studies of insulin-like growth factor I and bone. Growth Horm. IGF Res. 10 (Suppl. B), S107–S110 (2000).
  • Goldspink G, Harridge DR. Growth factors and muscle ageing. Exp. Gerontol. 39, 1433–1438 (2004).
  • Cheema U, Brown R, Mudera V, Yang SY, McGrouther G, Goldspink G. Mechanical signals and IGF-I gene splicing in vitro in relation to development of skeletal muscle. J. Cell Physiol. 202, 67–75 (2004).
  • West CA, Arnett TR, Farrow SM. Expression of insulin-like growth factor I (IGF-I) mRNA variants in rat bone. Bone 19, 41–46 (1996).
  • Lin WW, Oberbauer AM. Spatiotemporal expression of alternatively spliced IGF-I mRNA in the rat costochondral growth plate. J. Endocrinol. 160, 461–467 (1999).
  • Bikle DD, Sakata T, Leary C, Elalieh H et al. Insulin-like growth factor I is required for the anabolic actions of parathyroid hormone on mouse bone. J. Bone. Miner. Res. 17, 1570–1578 (2002).
  • Canalis E, Centrella M, Burch W, McCarthy TL. Insulin-like growth factor I mediates selective anabolic effects of parathyroid hormone in bone cultures. J. Clin. Invest. 83, 60–65 (1989).
  • Sims NA, Clement-Lacroix P, Da Ponte F et al. Bone homeostasis in growth hormone receptor-null mice is restored by IGF-I but independent of Stat5. J. Clin. Invest. 106, 1095–1103 (2000).
  • Canalis E, Giustina A. Glucocorticoid-induced osteoporosis: summary of a workshop. J. Clin. Endocrinol. Metab. 86, 5681–5685 (2001).
  • Delany AM, Durant D, Canalis E. Glucocorticoid suppression of IGF I transcription in osteoblasts. Mol. Endocrinol. 15, 1781–1789 (2001).
  • Canalis E, Economides AN, Gazzerro E. Bone morphogenetic proteins, their antagonists, and the skeleton. Endocr. Rev. 24, 218–235 (2003).
  • Gangji V, Rydziel S, Gabbitas B, Canalis E. Insulin-like growth factor II promoter expression in cultured rodent osteoblasts and adult rat bone. Endocrinology 139, 2287–2292 (1998).
  • Kveiborg M, Flyvbjerg A, Eriksen EF, Kassem M. Treatment with 1,25-dihydroxyvitamin D3 reduces impairment of human osteoblast functions during cellular aging in culture. J. Endocrinol. 169, 549–561 (2001).
  • Hock JM, Centrella M, Canalis E. Insulin-like growth factor I has independent effects on bone matrix formation and cell replication. Endocrinology 122, 254–260 (1988).
  • Canalis E, Rydziel S, Delany AM, Varghese S, Jeffrey JJ. Insulin-like growth factors inhibit interstitial collagenase synthesis in bone cell cultures. Endocrinology 136, 1348–1354 (1995).
  • Walsh S, Jefferiss CM, Stewart K, Beresford JN. IGF-I does not affect the proliferation or early osteogenic differentiation of human marrow stromal cells. Bone 33, 80–89 (2003).
  • Kalajzic I, Staal A, Yang WP et al. Expression profile of osteoblast lineage at defined stages of differentiation. J. Biol. Chem. 280, 24618–24626 (2005).
  • Mochizuki H, Hakeda Y, Wakatsuki N et al. Insulin-like growth factor-I supports formation and activation of osteoclasts. Endocrinology 131, 1075–1080 (1992).
  • Rubin J, Ackert-Bicknell CL, Zhu L et al. IGF-I regulates osteoprotegerin (OPG) and receptor activator of nuclear factor-κB ligand in vitro and OPG in vivo. J. Clin. Endocrinol. Metab. 87, 4273–4279 (2002).
  • Zhang M, Xuan S, Bouxsein ML et al. 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).
  • Zhao G, Monier-Faugere MC, Langub MC et al. 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 (2000).
  • Bikle D, Majumdar S, Laib A et al. The skeletal structure of insulin-like growth factor I-deficient mice. J. Bone. Miner. Res. 16, 2320–2329 (2001).
  • Beamer WH, Eicher EM. Stimulation of growth in the little mouse. J. Endocrinol. 71, 37–45 (1976).
  • Maheshwari HG, Bouillon R, Nijs J, Oganov VS, Bakulin AV, Baumann, G. The impact of congenital, severe, untreated growth hormone (GH) deficiency on bone size and density in young adults: insights from genetic GH-releasing hormone receptor deficiency. J. Clin. Endocrinol. Metab. 88, 2614–2618 (2003).
  • Klein RF. Genetic regulation of bone mineral density in mice. J. Musculoskelet. Neuronal Interact. 2, 232–236 (2002).
  • Beamer WG, Shultz KL, Donahue LR et al. Quantitative trait loci for femoral and lumbar vertebral bone mineral density in C57BL/6J and C3h/HeJ inbred strains of mice. J. Bone. Miner. Res. 16, 1195–1206 (2001).
  • Bouxsein ML, Rosen CJ, Turner C et al. 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 (2002).
  • Rosen CJ, Ackert-Bicknell CL, Adamo ML et al. Congenic mice with low serum IGF-I have increased body fat, reduced bone mineral density, and an altered osteoblast differentiation program. Bone 35, 1046–1058 (2004).
  • Rosen CJ, Ackert-Bicknell C, Beamer WG et al. Allelic differences in a quantitative trait locus affecting insulin-like growth factor-I impact skeletal acquisition and body composition. Pediatr. Nephrol. 20, 255–260 (2005).
  • Govoni KE, Baylink DJ, Mohan S. The multi-functional role of insulin-like growth factor binding proteins in bone. Pediatr. Nephrol. 20, 261–268 (2005).
  • Murphy LJ. The role of the insulin-like growth factors and their binding proteins in glucose homeostasis. Exp. Diab. Res. 4, 213–224 (2003).
  • Fisher MC, Meyer C, Garber G, Dealy CN. Role of IGFBP2, IGF-I and IGF-II in regulating long bone growth. Bone (2005) (In Press).
  • Eckstein F, Pavicic T, Nedbal S et al. Insulin-like growth factor-binding 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. 206, 139–148 (2002).
  • Amin S, Riggs BL, Atkinson EJ, Oberg AL, Melton LJ III, Khosla S. A potentially deleterious role of IGFBP-2 on bone density in aging men and women. J. Bone Miner. Res. 19, 1075–1083 (2004).
  • O’Rear L, Longobardi L, Torello M et al. Signaling cross-talk between IGF-binding protein-3 and transforming growth factor-β in mesenchymal chondroprogenitor cell growth. J. Mol. Endocrinol. 34, 723–737 (2005).
  • Longobardi L, Torello M, Buckway C et al. A novel insulin-like growth factor (IGF)-independent role for IGF binding protein-3 in mesenchymal chondroprogenitor cell apoptosis. Endocrinology 144, 1695–1702 (2003).
  • Silha JV, Mishra S, Rosen CJ et al. Perturbations in bone formation and resorption in insulin-like growth factor binding protein-3 transgenic mice. J. Bone. Miner. Res. 18, 1834–1841 (2003).
  • Kiepe D, Ciarmatori S, Hoeflich A, Wolf E, Tonshoff B. Differential expression of IGF system components in proliferating vs. differentiating growth plate chondrocytes: the functional role of IGFBP-5. Endocrinology 146, 3096–3104 (2005).
  • Miyakoshi N, Qin X, Kasukawa Y et al. 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 (2001).
  • Richman C, Baylink DJ, Lang K, Dony C, Mohan S. Recombinant human insulin-like growth factor-binding protein-5 stimulates bone formation parameters in vitro and in vivo. Endocrinology 140, 4699–4705 (1999).
  • Devlin RD, 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 143, 3955–3962 (2002).
  • Zhang M, Faugere MC, Malluche H, Rosen CJ, Chernausek SD, Clemens TL. Paracrine overexpression of IGFBP-4 in osteoblasts of transgenic mice decreases bone turnover and causes global growth retardation. J. Bone. Miner. Res. 18, 836–843 (2003).
  • Boonen S, Aerssens J, Dequeker J et al. Age-associated decline in human femoral neck cortical and trabecular content of insulin-like growth factor I: potential implications for age-related (type II) osteoporotic fracture occurrence. Calcif. Tissue Int. 61, 173–178 (1997).
  • Langlois JA, Rosen CJ, Visser M et al. Association between insulin-like growth factor I and bone mineral density in older women and men: the Framingham Heart Study. J. Clin. Endocrinol. Metab. 83, 4257–4262 (1998).
  • Sugimoto T, Nishiyama K, Kuribayashi F, Chihara K. Serum levels of insulin-like growth factor (IGF) I, IGF-binding protein (IGFBP)-2, and IGFBP-3 in osteoporotic patients with and without spinal fractures. J. Bone. Miner. Res. 12, 1272–1279 (1997).
  • Rivadeneira F, Houwing-Duistermaat JJ, Vaessen N et al. Association between an insulin-like growth factor I gene promoter polymorphism and bone mineral density in the elderly: the Rotterdam Study. J. Clin. Endocrinol. Metab. 88, 3878–3884 (2003).
  • Ghiron LJ, Thompson JL, Holloway L et al. Effects of recombinant insulin-like growth factor-I and growth hormone on bone turnover in elderly women. J. Bone. Miner. Res. 10, 1844–1852 (1995).
  • Monson JP. Long-term experience with GH replacement therapy: efficacy and safety. Eur. Endocrinol. 148, S9–S14 (2003).
  • Rosenfeld RG. The IGF system: new developments relevant to pediatric practice. Endocr. Dev. 9, 1–10 (2005).
  • Rosen CJ, Bilezikian JP. Clinical review 123: anabolic therapy for osteoporosis. J. Clin. Endocrinol. Metab. 86, 957–964 (2001).
  • Grinspoon S, Baum H, Lee K, Anderson E, Herzog D, Klibanski A. Effects of short-term recombinant human insulin-like growth factor I administration on bone turnover in osteopenic women with anorexia nervosa. J. Clin. Endocrinol. Metab. 81, 3864–3870 (1996).
  • Grinspoon S, Thomas L, Miller K, Herzog D, Klibanski A. Effects of recombinant human IGF-I and oral contraceptive administration on bone density in anorexia nervosa. J. Clin. Endocrinol. Metab. 87, 2883–2891 (2002).
  • Clark RG. Recombinant human insulin-like growth factor I (IGF-I): risks and benefits of normalizing blood IGF-I concentrations. Horm. Res.62 (Suppl 1), 93–100 (2004).
  • Ranke MB. Insulin-like growth factor-I treatment of growth disorders, diabetes mellitus and insulin resistance. Trends Endocrinol. Metab. 16, 190–197 (2005).
  • Hodsman AB, Bauer DC, Dempster DW et al. Parathyroid hormone and teriparatide for the treatment of osteoporosis: a review of the evidence and suggested guidelines for its use. Endocr. Rev. 26, 688–703 (2005).
  • Rosen CJ. The cellular and clinical parameters of anabolic therapy for osteoporosis. Crit. Rev. Eukaryot. Gene. Expr. 13, 25–38 (2003).
  • Ishizuyza T, Yokose S, Hori M et al. Parathyroid hormone exerts disparate effects on osteoblast differentiation depending on exposure time in rat osteoblastic cells. J. Clin. Invest. 99, 2961–2970 (1997).
  • Locklin RM, Khosla S, Turner RT, Riggs BL. Mediators of the biphasic responses of bone to intermittent and continuously administered parathyroid hormone. J. Cell Biochem. 89, 180–190 (2003).
  • 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).
  • Ogata N, Chikazu D, Kubota N et al. Insulin receptor substrate-1 in osteoblast is indispensable for maintaining bone turnover. J. Clin. Invest. 105, 935–943 (2000).
  • Yamaguchi M, Ogata N, Shinoda Y et al. Insulin receptor substrate-1 is required for bone anabolic function of parathyroid hormone in mice. Endocrinology 146, 2620–2628 (2005).
  • Rosen CJ. Insulin-like growth factor I and bone mineral density: experience from animal models and human observational studies. Best Pract. Res. Clin. Endocrinol. Metab. 18(3), 423–435 (2004).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.