Novel functions for insulin in bone

Bone

Volumn 50, Issue 2, 2012, Pages 452-456

  Fulzele, Keertik ^a   Clemens, Thomas L ^b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Glucose homeostasis; Insulin receptor; Knockout mice; Osteoblasts; Osteocalcin

Indexed keywords

INSULIN; OSTEOCALCIN; RECEPTOR TYROSINE KINASE LIKE ORPHAN RECEPTOR; SOMATOMEDIN;

BIOAVAILABILITY; BONE CELL; BONE CHARACTERISTICS AND FUNCTIONS; CELL PROLIFERATION; CELL SURVIVAL; DIABETES MELLITUS; ENERGY EXPENDITURE; FOOD INTAKE; GROWTH; HOMEOSTASIS; HORMONE ACTION; HUMAN; METABOLIC DISORDER; METABOLIC REGULATION; NONHUMAN; OSTEOBLAST; OSTEOPOROSIS; REPRODUCTION; REVIEW; SMELLING;

ANIMALS; BONE AND BONES; HUMANS; INSULIN; OSTEOBLASTS; OSTEOCALCIN; RECEPTOR, INSULIN; SIGNAL TRANSDUCTION;

EID: 84855864159     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2011.06.018     Document Type: Review

References (56)

1. Kulkarni R.N., Bruning J.C., Winnay J.N., Postic C., Magnuson M.A., Kahn C.R. Tissue-specific knockout of the insulin receptor in pancreatic beta cells creates an insulin secretory defect similar to that in type 2 diabetes. Cell 1999, 96:329-339.
2. Michael M.D., Kulkarni R.N., Postic C., Previs S.F., Shulman G.I., Magnuson M.A., et al. Loss of insulin signaling in hepatocytes leads to severe insulin resistance and progressive hepatic dysfunction. Mol Cell 2000, 6:87-97.
3. Bluher M., Michael M.D., Peroni O.D., Ueki K., Carter N., Kahn B.B., et al. Adipose tissue selective insulin receptor knockout protects against obesity and obesity-related glucose intolerance. Dev Cell 2002, 3:25-38.
4. Fukumoto S., Martin T.J. Bone as an endocrine organ. Trends Endocrinol Metab 2009, 20:230-236.
5. Lee N.K., Karsenty G. Reciprocal regulation of bone and energy metabolism. Trends Endocrinol Metab 2008, 19:161-166.
6. Nef S., Parada L.F. Hormones in male sexual development. Genes Dev 2000, 14:3075-3086.
7. Tissenbaum H.A., Ruvkun G. An insulin-like signaling pathway affects both longevity and reproduction in Caenorhabditis elegans. Genetics 1998, 148:703-717.
8. Kim J.J., Accili D. Signalling through IGF-I and insulin receptors: where is the specificity?. Growth Horm IGF Res 2002, 12:84-90.
9. Ebina Y., Ellis L., Jarnagin K., Edery M., Graf L., Clauser E., et al. The human insulin receptor cDNA: the structural basis for hormone-activated transmembrane signalling. Cell 1985, 40:747-758.
10. Ullrich A., Bell J.R., Chen E.Y., Herrera R., Petruzzelli L.M., Dull T.J., et al. Human insulin receptor and its relationship to the tyrosine kinase family of oncogenes. Nature 1985, 313:756-761.
11. Ullrich A., Gray A., Tam A.W., Yang-Feng T., Tsubokawa M., Collins C., et al. Insulin-like growth factor I receptor primary structure: comparison with insulin receptor suggests structural determinants that define functional specificity. EMBO J 1986, 5:2503-2512.
12. Morgan D.O., Edman J.C., Standring D.N., Fried V.A., Smith M.C., Roth R.A., et al. Insulin-like growth factor II receptor as a multifunctional binding protein. Nature 1987, 329:301-307.
13. Hubbard S.R. Crystal structure of the activated insulin receptor tyrosine kinase in complex with peptide substrate and ATP analog. EMBO J 1997, 16:5572-5581.
14. Hubbard S.R., Wei L., Ellis L., Hendrickson W.A. Crystal structure of the tyrosine kinase domain of the human insulin receptor. Nature 1994, 372:746-754.
15. Schlessinger J. Cell signaling by receptor tyrosine kinases. Cell 2000, 103:211-225.
16. Taniguchi C.M., Emanuelli B., Kahn C.R. Critical nodes in signalling pathways: insights into insulin action. Nature Reviews. Mol Cell Biol 2006, 7:85-96.
17. Cooke D.W., Plotnick L. Type 1 diabetes mellitus in pediatrics. Pediatr Rev 2008, 29:374-384. [quiz 385].
18. Pun K.K., Lau P., Ho P.W. The characterization, regulation, and function of insulin receptors on osteoblast-like clonal osteosarcoma cell line. J Bone Miner Res 1989, 4:853-862.
19. Kream B.E., Smith M.D., Canalis E., Raisz L.G. Characterization of the effect of insulin on collagen synthesis in fetal rat bone. Endocrinology 1985, 116:296-302.
20. Hahn T.J., Westbrook S.L., Sullivan T.L., Goodman W.G., Halstead L.R. Glucose transport in osteoblast-enriched bone explants: characterization and insulin regulation. J Bone Miner Res 1988, 3:359-365.
21. Ituarte E.A., Halstead L.R., Iida-Klein A., Ituarte H.G., Hahn T.J. Glucose transport system in UMR-106-01 osteoblastic osteosarcoma cells: regulation by insulin. Calcif Tissue Int 1989, 45:27-33.
22. Kemink S.A., Hermus A.R., Swinkels L.M., Lutterman J.A., Smals A.G. Osteopenia in insulin-dependent diabetes mellitus; prevalence and aspects of pathophysiology. J Endocrinol Invest 2000, 23:295-303.
23. Thrailkill K.M. Insulin-like growth factor-I in diabetes mellitus: its physiology, metabolic effects, and potential clinical utility. Diabetes Technol Ther 2000, 2:69-80.
24. Janghorbani M., Feskanich D., Willett W.C., Hu F. Prospective study of diabetes and risk of hip fracture: the nurses' health study. Diabetes Care 2006, 29:1573-1578.
25. Nicodemus K.K., Folsom A.R. Type 1 and type 2 diabetes and incident hip fractures in postmenopausal women. Diabetes Care 2001, 24:1192-1197.
26. Loder R.T. The influence of diabetes mellitus on the healing of closed fractures. Clin Orthop Relat Res 1988, 210-216.
27. Gandhi A., Beam H.A., O'Connor J.P., Parsons J.R., Lin S.S. The effects of local insulin delivery on diabetic fracture healing. Bone 2005, 37:482-490.
28. Herrero S., Calvo O.M., Garcia-Moreno C., Martin E., San Roman J.I., Martin M., et al. Low bone density with normal bone turnover in ovariectomized and streptozotocin-induced diabetic rats. Calcif Tissue Int 1998, 62:260-265.
29. Verhaeghe J., van Herck E., Visser W.J., Suiker A.M., Thomasset M., Einhorn T.A., et al. Bone and mineral metabolism in BB rats with long-term diabetes. Decreased bone turnover and osteoporosis. Diabetes 1990, 39:477-482.
30. Goodman W.G., Hori M.T. Diminished bone formation in experimental diabetes. Relationship to osteoid maturation and mineralization. Diabetes 1984, 33:825-831.
31. Shires R., Teitelbaum S.L., Bergfeld M.A., Fallon M.D., Slatopolsky E., Avioli L.V. The effect of streptozotocin-induced chronic diabetes mellitus on bone and mineral homeostasis in the rat. J Lab Clin Med 1981, 97:231-240.
32. Verhaeghe J., Suiker A.M., Visser W.J., Van Herck E., Van Bree R., Bouillon R. The effects of systemic insulin, insulin-like growth factor-I and growth hormone on bone growth and turnover in spontaneously diabetic BB rats. J Endocrinol 1992, 134:485-492.
33. Zhang M., Xuan S., Bouxsein M.L., von Stechow D., Akeno N., Faugere M.C., 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 2002, 277:44005-44012.
34. Fulzele K., DiGirolamo D.J., Liu Z., Xu J., Messina J.L., Clemens T.L. Disruption of the insulin-like growth factor type 1 receptor in osteoblasts enhances insulin signaling and action. J Biol Chem 2007, 282:25649-25658.
35. Fulzele K., Riddle R.C., DiGirolamo D.J., Cao X., Wan C., Chen D., et al. Insulin receptor signaling in osteoblasts regulates postnatal bone acquisition and body composition. Cell 2010, 142:309-319.
36. Ferron M., Wei J., Yoshizawa T., Del Fattore A., DePinho R.A., Teti A., et al. Insulin signaling in osteoblasts integrates bone remodeling and energy metabolism. Cell 2010, 142:296-308.
37. Irwin R., Lin H.V., Motyl K.J., McCabe L.R. Normal bone density obtained in the absence of insulin receptor expression in bone. Endocrinology 2006, 147:5760-5767.
38. Okamoto H., Nakae J., Kitamura T., Park B.C., Dragatsis I., Accili D. Transgenic rescue of insulin receptor-deficient mice. J Clin Invest 2004, 114:214-223.
39. Ducy P., Amling M., Takeda S., Priemel M., Schilling A.F., Beil F.T., et al. Leptin inhibits bone formation through a hypothalamic relay: a central control of bone mass. Cell 2000, 100:197-207.
40. Lee N.K., Sowa H., Hinoi E., Ferron M., Ahn J.D., Confavreux C., et al. Endocrine regulation of energy metabolism by the skeleton. Cell 2007, 130:456-469.
41. Ducy P., Desbois C., Boyce B., Pinero G., Story B., Dunstan C., et al. Increased bone formation in osteocalcin-deficient mice. Nature 1996, 382:448-452.
42. Hauschka P.V., Lian J.B., Cole D.E., Gundberg C.M. Osteocalcin and matrix Gla protein: vitamin K-dependent proteins in bone. Physiol Rev 1989, 69:990-1047.
43. Delmas P.D., Wilson D.M., Mann K.G., Riggs B.L. Effect of renal function on plasma levels of bone Gla-protein. J Clin Endocrinol Metab 1983, 57:1028-1030.
44. Egawa K., Maegawa H., Shimizu S., Morino K., Nishio Y., Bryer-Ash M., et al. Protein-tyrosine phosphatase-1B negatively regulates insulin signaling in l6 myocytes and Fao hepatoma cells. J Biol Chem 2001, 276:10207-10211.
45. Engelke J.A., Hale J.E., Suttie J.W., Price P.A. Vitamin K-dependent carboxylase: utilization of decarboxylated bone Gla protein and matrix Gla protein as substrates. Biochim Biophys Acta 1991, 1078:31-34.
46. Ferron M., Hinoi E., Karsenty G., Ducy P. Osteocalcin differentially regulates beta cell and adipocyte gene expression and affects the development of metabolic diseases in wild-type mice. Proc Natl Acad Sci USA 2008, 105:5266-5270.
47. Wellendorph P., Brauner-Osborne H. Molecular cloning, expression, and sequence analysis of GPRC6A, a novel family CG-protein-coupled receptor. Gene 2004, 335:37-46.
48. Pi M., Faber P., Ekema G., Jackson P.D., Ting A., Wang N., et al. Identification of a novel extracellular cation-sensing G-protein-coupled receptor. J Biol Chem 2005, 280:40201-40209.
49. Pi M., Chen L., Huang M.Z., Zhu W., Ringhofer B., Luo J., et al. GPRC6A null mice exhibit osteopenia, feminization and metabolic syndrome. PLoS One 2008, 3:e3858.
50. Oury F., Sumara G., Sumara O., Ferron M., Chang H., Smith C.E., et al. Endocrine regulation of male fertility by the skeleton. Cell 2011, 144:796-809.
51. Wellendorph P., Hansen K.B., Balsgaard A., Greenwood J.R., Egebjerg J., Brauner-Osborne H. Deorphanization of GPRC6A: a promiscuous L-alpha-amino acid receptor with preference for basic amino acids. Mol Pharmacol 2005, 67:589-597.
52. Kindblom J.M., Ohlsson C., Ljunggren O., Karlsson M.K., Tivesten A., Smith U., et al. Plasma osteocalcin is inversely related to fat mass and plasma glucose in elderly Swedish men. J Bone Miner Res 2009, 24:785-791.
53. Yeap B.B., Chubb S.A., Flicker L., McCaul K.A., Ebeling P.R., Beilby J.P., et al. Reduced serum total osteocalcin is associated with metabolic syndrome in older men via waist circumference, hyperglycemia, and triglyceride levels. Eur J Endocrinol 2010, 163:265-272.
54. Hwang Y.C., Jeong I.K., Ahn K.J., Chung H.Y. The uncarboxylated form of osteocalcin is associated with improved glucose tolerance and enhanced beta-cell function in middle-aged male subjects. Diabetes Metab Res Rev 2009, 25:768-772.
55. Reinehr T., Roth C.L. A new link between skeleton, obesity and insulin resistance: relationships between osteocalcin, leptin and insulin resistance in obese children before and after weight loss. Int J Obes 2010, 34:852-858.
56. Basu R., Peterson J., Rizza R., Khosla S. Effects of physiological variations in circulating insulin levels on bone turnover in humans. J Clin Endocrinol Metab 2011, [Epub 16 Feb]. 10.1210/jc.2010-2877.