Chronic administration of Glucagon-like peptide-1 receptor agonists improves trabecular bone mass and architecture in ovariectomised mice

Bone

Volumn 81, Issue , 2015, Pages 459-467

  Pereira, M ^a   Jeyabalan, J ^a   Jorgensen C S ^a   Hopkinson, M ^a   Al Jazzar, A ^a   Roux, J P ^b   Chavassieux, P ^b   Orriss, I R ^a   Cleasby, M E ^a   Chenu, C ^a  

^a ROYAL VETERINARY COLLEGE   (United Kingdom)

^b UNIVERSITÉ DE LYON   (France)

Author keywords

Bone architecture; Diabetes; Glucagon like peptide 1

Indexed keywords

ALIZARIN; CALCEIN; CALCITONIN; EXENDIN 4; GLUCAGON LIKE PEPTIDE 1 RECEPTOR AGONIST; LIRAGLUTIDE; MESSENGER RNA; PLACEBO; SCLEROSTIN; GLP1R PROTEIN, MOUSE; GLUCAGON LIKE PEPTIDE 1 RECEPTOR; GLYCOPROTEIN; PEPTIDE; SOST PROTEIN, MOUSE; VENOM;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE CELL; BONE MASS; BONE MINERALIZATION; BONE STRUCTURE; CELL CULTURE; CELL SURFACE; CONTROLLED STUDY; CORTICAL BONE; DISEASE ASSOCIATION; DRUG EFFECT; FEMALE; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MICRO-COMPUTED TOMOGRAPHY; MORPHOMETRICS; MOUSE; MOUSE MODEL; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OSSIFICATION; OSTEOBLAST; OSTEOCLAST; OSTEOLYSIS; OSTEOPOROSIS; OVARIECTOMY; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR UPREGULATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA GENE; TIBIA; TOXICOKINETICS; TRABECULAR BONE; UPREGULATION; AGONISTS; ANIMAL; BLOOD; BONE; BONE DEVELOPMENT; C57BL MOUSE; CYTOLOGY; DIABETES MELLITUS, TYPE 2; DIAGNOSTIC IMAGING; DISEASE MODEL; DRUG EFFECTS; METABOLISM; OSTEOCYTE;

ANIMALS; BONE AND BONES; BONE RESORPTION; CALCITONIN; DIABETES MELLITUS, TYPE 2; DISEASE MODELS, ANIMAL; FEMALE; GLUCAGON-LIKE PEPTIDE-1 RECEPTOR; GLYCOPROTEINS; IMMUNOHISTOCHEMISTRY; LIRAGLUTIDE; MICE; MICE, INBRED C57BL; OSTEOBLASTS; OSTEOCLASTS; OSTEOCYTES; OSTEOGENESIS; OSTEOPOROSIS; OVARIECTOMY; PEPTIDES; RNA, MESSENGER; TIBIA; VENOMS; X-RAY MICROTOMOGRAPHY;

EID: 84940750812     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2015.08.006     Document Type: Article

References (50)

1. Yamamoto M., Yamaguchi T., Yamauchi M., Kaji H., Sugimoto T. Diabetic patients have an increased risk of vertebral fractures independent of BMD or diabetic complications. J. Bone Miner. Res. 2009, 24(4):702-709.
2. Janghorbani M., Van Dam R.M., Willett W.C., Hu F.B. Systematic review of type 1 and type 2 diabetes mellitus and risk of fracture. Am. J. Epidemiol. 2007, 166(5):495-505.
3. Dede A.D., Tournis S., Dontas I., Trovas G. Type 2 diabetes mellitus and fracture risk. Metab. Clin. Exp. 2014, 63(12):1480-1490.
4. Garcia-Martin A., Rozas-Moreno P., Reyes-Garcia R., Morales-Santana S., Garcia-Fontana B., Garcia-Salcedo J.A., Munoz-Torres M. Circulating levels of sclerostin are increased in patients with type 2 diabetes mellitus. J. Clin. Endocrinol. Metab. 2012, 97(1):234-241.
5. Balint E., Szabo P., Marshall C.F., Sprague S.M. Glucose-induced inhibition of in vitro bone mineralization. Bone 2001, 28(1):21-28.
6. La Fontaine J., Shibuya N., Sampson H.W., Valderrama P. Trabecular quality and cellular characteristics of normal, diabetic, and charcot bone. J. Foot Ankle Surg. 2011, 50(6):648-653.
7. Lecka-Czernik B. Bone loss in diabetes: use of antidiabetic thiazolidinediones and secondary osteoporosis. Curr. Osteoporos. Rep. 2010, 8(4):178-184.
8. Mai Q.G., Zhang Z.M., Xu S., Lu M., Zhou R.P., Zhao L., Jia C.H., Wen Z.H., Jin D.D., Bai X.C. Metformin stimulates osteoprotegerin and reduces RANKL expression in osteoblasts and ovariectomized rats. J. Cell. Biochem. 2011, 112(10):2902-2909.
9. Vestergaard P., Rejnmark L., Mosekilde L. Relative fracture risk in patients with diabetes mellitus, and the impact of insulin and oral antidiabetic medication on relative fracture risk. Diabetologia 2005, 48(7):1292-1299.
10. Jeyabalan J., Viollet B., Smitham P., Ellis S.A., Zaman G., Bardin C., Goodship A., Roux J.P., Pierre M., Chenu C. The anti-diabetic drug metformin does not affect bone mass in vivo or fracture healing. Osteoporos. Int. 2013, 24(10):2659-2670.
11. Creutzfeldt W. The entero-insular axis in type 2 diabetes-incretins as therapeutic agents. Exp. Clin. Endocrinol. Diab. 2001, 109(Suppl. 2):S288-S303.
12. Mudaliar S., Henry R.R. The incretin hormones: from scientific discovery to practical therapeutics. Diabetologia 2012, 55(7):1865-1868.
13. DeFronzo R.A., Ratner R.E., Han J., Kim D.D., Fineman M.S., Baron A.D. Effects of exenatide (exendin-4) on glycemic control and weight over 30weeks in metformin-treated patients with type 2 diabetes. Diabetes Care 2005, 28(5):1092-1100.
14. Ryan G.J., Foster K.T., Jobe L.J. Review of the therapeutic uses of liraglutide. Clin. Ther. 2011, 33(7):793-811.
15. Fineman M.S., Bicsak T.A., Shen L.Z., Taylor K., Gaines E., Varns A., Kim D., Baron A.D. Effect on glycemic control of exenatide (synthetic exendin-4) additive to existing metformin and/or sulfonylurea treatment in patients with type 2 diabetes. Diabetes Care 2003, 26(8):2370-2377.
16. Baggio L.L., Drucker D.J. Glucagon-like peptide-1 receptors in the brain: controlling food intake and body weight. J. Clin. Invest. 2014, 124(10):4223-4226.
17. Bjarnason N.H., Henriksen E.E., Alexandersen P., Christgau S., Henriksen D.B., Christiansen C. Mechanism of circadian variation in bone resorption. Bone 2002, 30(1):307-313.
18. Clowes J.A., Hannon R.A., Yap T.S., Hoyle N.R., Blumsohn A., Eastell R. Effect of feeding on bone turnover markers and its impact on biological variability of measurements. Bone 2002, 30(6):886-890.
19. Lamari Y., Boissard C., Moukhtar M.S., Jullienne A., Rosselin G., Garel J.M. Expression of glucagon-like peptide 1 receptor in a murine C cell line: regulation of calcitonin gene by glucagon-like peptide 1. FEBS Lett. 1996, 393(2-3):248-252.
20. Yamada C., Yamada Y., Tsukiyama K., Yamada K., Udagawa N., Takahashi N., Tanaka K., Drucker D.J., Seino Y., Inagaki N. The murine glucagon-like peptide-1 receptor is essential for control of bone resorption. Endocrinology 2008, 149(2):574-579.
21. Mabilleau G., Mieczkowska A., Irwin N., Flatt P.R., Chappard D. Optimal bone mechanical and material properties require a functional glucagon-like peptide-1 receptor. J. Endocrinol. 2013, 219(1):59-68.
22. Mieczkowska A., Mansur S., Bouvard B., Flatt P.R., Thorens B., Irwin N., Chappard D., Mabilleau G. Double incretin receptor knock-out (DIRKO) mice present with alterations of trabecular and cortical micromorphology and bone strength. Osteoporos. Int. 2015, 26(1):209-218.
23. Nuche-Berenguer B., Lozano D., Gutierrez-Rojas I., Moreno P., Marinoso M.L., Esbrit P., Villanueva-Penacarrillo M.L. GLP-1 and exendin-4 can reverse hyperlipidic-related osteopenia. J. Endocrinol. 2011, 209(2):203-210.
24. Nuche-Berenguer B., Moreno P., Esbrit P., Dapia S., Caeiro J.R., Cancelas J., Haro-Mora J.J., Villanueva-Penacarrillo M.L. Effect of GLP-1 treatment on bone turnover in normal, type 2 diabetic, and insulin-resistant states. Calcif. Tissue Int. 2009, 84(6):453-461.
25. Nuche-Berenguer B., Moreno P., Portal-Nunez S., Dapia S., Esbrit P., Villanueva-Penacarrillo M.L. Exendin-4 exerts osteogenic actions in insulin-resistant and type 2 diabetic states. Regul. Pept. 2010, 159(1-3):61-66.
26. Kim J.Y., Lee S.K., Jo K.J., Song D.Y., Lim D.M., Park K.Y., Bonewald L.F., Kim B.J. Exendin-4 increases bone mineral density in type 2 diabetic OLETF rats potentially through the down-regulation of SOST/sclerostin in osteocytes. Life Sci. 2013, 92(10):533-540.
27. Sun H.X., Lu N., Luo X., Zhao L., Liu J.M. Liraglutide, the glucagon-like peptide-1 receptor agonist, has anabolic bone effects in diabetic Goto-Kakizaki rats. J. Diabetes 2015, 7(4):584-588.
28. Ma X., Meng J., Jia M., Bi L., Zhou Y., Wang Y., Hu J., He G., Luo X. Exendin-4, a glucagon-like peptide-1 receptor agonist, prevents osteopenia by promoting bone formation and suppressing bone resorption in aged ovariectomized rats. J. Bone Miner. Res. 2013, 28(7):1641-1652.
29. Nuche-Berenguer B., Portal-Nunez S., Moreno P., Gonzalez N., Acitores A., Lopez-Herradon A., Esbrit P., Valverde I., Villanueva-Penacarrillo M.L. Presence of a functional receptor for GLP-1 in osteoblastic cells, independent of the cAMP-linked GLP-1 receptor. J. Cell. Physiol. 2010, 225(2):585-592.
30. Aoyama E., Watari I., Podyma-Inoue K.A., Yanagishita M., Ono T. Expression of glucagon-like peptide-1 receptor and glucose-dependent insulinotropic polypeptide receptor is regulated by the glucose concentration in mouse osteoblastic MC3T3-E1 cells. Int. J. Mol. Med. 2014, 34(2):475-482.
31. Pacheco-Pantoja E.L., Ranganath L.R., Gallagher J.A., Wilson P.J., Fraser W.D. Receptors and effects of gut hormones in three osteoblastic cell lines. BMC Physiol. 2011, 11:12.
32. Sanz C., Vazquez P., Blazquez C., Barrio P.A., Alvarez Mdel M., Blazquez E. Signaling and biological effects of glucagon-like peptide 1 on the differentiation of mesenchymal stem cells from human bone marrow. Am. J. Physiol. Endocrinol. Metab. 2010, 298(3):E634-E643.
33. Jeon Y.K., Bae M.J., Kim J.I., Kim J.H., Choi S.J., Kwon S.K., An J.H., Kim S.S., Kim B.H., Kim Y.K., Kim I.J. Expression of glucagon-like peptide 1 receptor during osteogenic differentiation of adipose-derived stem cells. Endocrinol. Metab. 2014, 29(4):567-573.
34. Jeyabalan J., Shah M., Viollet B., Roux J.P., Chavassieux P., Korbonits M., Chenu C. Mice lacking AMP-activated protein kinase alpha1 catalytic subunit have increased bone remodelling and modified skeletal responses to hormonal challenges induced by ovariectomy and intermittent PTH treatment. J. Endocrinol. 2012, 214(3):349-358.
35. Shah M., Kola B., Bataveljic A., Arnett T.R., Viollet B., Saxon L., Korbonits M., Chenu C. AMP-activated protein kinase (AMPK) activation regulates in vitro bone formation and bone mass. Bone 2010, 47(2):309-319.
36. Chappard D., Palle S., Alexandre C., Vico L., Riffat G. Bone embedding in pure methyl methacrylate at low temperature preserves enzyme activities. Acta Histochem. 1987, 81(2):183-190.
37. Dempster D.W., Compston J.E., Drezner M.K., Glorieux F.H., Kanis J.A., Malluche H., Meunier P.J., Ott S.M., Recker R.R., Parfitt A.M. Standardized nomenclature, symbols, and units for bone histomorphometry: a 2012 update of the report of the ASBMR Histomorphometry Nomenclature Committee. J. Bone Miner. Res. 2013, 28(1):2-17.
38. Woo S.M., Rosser J., Dusevich V., Kalajzic I., Bonewald L.F. Cell line IDG-SW3 replicates osteoblast-to-late-osteocyte differentiation in vitro and accelerates bone formation in vivo. J. Bone Miner. Res. 2011, 26(11):2634-2646.
39. Orriss I.R., Taylor S.E., Arnett T.R. Rat osteoblast cultures. Methods Mol. Biol. 2012, 816:31-41.
40. Taylor S.E., Shah M., Orriss I.R. Generation of rodent and human osteoblasts. BoneKEy Rep. 2014, 3:585.
41. Orriss I.R., Arnett T.R. Rodent osteoclast cultures. Methods Mol. Biol. 2012, 816:103-117.
42. Silva M.J., Gibson L.J. Modeling the mechanical behavior of vertebral trabecular bone: effects of age-related changes in microstructure. Bone 1997, 21(2):191-199.
43. Buse J.B., Nauck M., Forst T., Sheu W.H., Shenouda S.K., Heilmann C.R., Hoogwerf B.J., Gao A., Boardman M.K., Fineman M., Porter L., Schernthaner G. Exenatide once weekly versus liraglutide once daily in patients with type 2 diabetes (DURATION-6): a randomised, open-label study. Lancet 2013, 381(9861):117-124.
44. Drucker DJ, Buse JB, Taylor K, Kendall DM, Trautmann M, Zhuang D, Porter L, Group D-S Exenatide once weekly versus twice daily for the treatment of type 2 diabetes: a randomised, open-label, non-inferiority study. Lancet 2008, 372(9645):1240-1250.
45. Henriksen D.B., Alexandersen P., Hartmann B., Adrian C.L., Byrjalsen I., Bone H.G., Holst J.J., Christiansen C. Disassociation of bone resorption and formation by GLP-2: a 14-day study in healthy postmenopausal women. Bone 2007, 40(3):723-729.
46. Steiniche T., Eriksen E.F., Kudsk H., Mosekilde L., Melsen F. Reconstruction of the formative site in trabecular bone by a new, quick, and easy method. Bone 1992, 13(2):147-152.
47. Madsen L.W., Knauf J.A., Gotfredsen C., Pilling A., Sjogren I., Andersen S., Andersen L., de Boer A.S., Manova K., Barlas A., Vundavalli S., Nyborg N.C., Knudsen L.B., Moelck A.M., Fagin J.A. GLP-1 receptor agonists and the thyroid: C-cell effects in mice are mediated via the GLP-1 receptor and not associated with RET activation. Endocrinology 2012, 153(3):1538-1547.
48. Bjerre Knudsen L., Madsen L.W., Andersen S., Almholt K., de Boer A.S., Drucker D.J., Gotfredsen C., Egerod F.L., Hegelund A.C., Jacobsen H., Jacobsen S.D., Moses A.C., Molck A.M., Nielsen H.S., Nowak J., Solberg H., Thi T.D., Zdravkovic M., Moerch U. Glucagon-like Peptide-1 receptor agonists activate rodent thyroid C-cells causing calcitonin release and C-cell proliferation. Endocrinology 2010, 151(4):1473-1486.
49. Kauther M.D., Bachmann H.S., Neuerburg L., Broecker-Preuss M., Hilken G., Grabellus F., Koehler G., von Knoch M., Wedemeyer C. Calcitonin substitution in calcitonin deficiency reduces particle-induced osteolysis. BMC Musculoskelet. Disord. 2011, 12:186.
50. Li X., Ominsky M.S., Niu Q.T., Sun N., Daugherty B., D'Agostin D., Kurahara C., Gao Y., Cao J., Gong J., Asuncion F., Barrero M., Warmington K., Dwyer D., Stolina M., Morony S., Sarosi I., Kostenuik P.J., Lacey D.L., Simonet W.S., Ke H.Z., Paszty C. Targeted deletion of the sclerostin gene in mice results in increased bone formation and bone strength. J. Bone Miner. Res. 2008, 23(6):860-869.