An insulin-sensitizing thiazolidinedione, which minimally activates PPARγ, does not cause bone loss

Journal of Bone and Mineral Research

Volumn 30, Issue 3, 2015, Pages 508-515

  Fukunaga, Tomohiro ^a   Zou, Wei ^a   Rohatgi, Nidhi ^a   Colca, Jerry R ^b   Teitelbaum, Steven L ^a  

^a WASHINGTON UNIVERSITY   (United States)

^b Metabolic Solutions Development Company   (United States)

Author keywords

Bone histomorphometry; Bone CT; Osteoclasts; Thiazolidinedione; Type II diabetes mellitus

Indexed keywords

2,4 THIAZOLIDINEDIONE DERIVATIVE; CD36 ANTIGEN; CELL NUCLEUS RECEPTOR; MSDC 0602; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; ROSIGLITAZONE; UNCLASSIFIED DRUG; 2,4-THIAZOLIDINEDIONE; INSULIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE MASS; CELL COUNT; CONTROLLED STUDY; DRUG MECHANISM; GENE; GENE EXPRESSION; GENE TARGETING; HOMEOSTASIS; IN VITRO STUDY; IN VIVO STUDY; INSULIN SENSITIVITY; MALE; MOUSE; NONHUMAN; OSTEOCLAST; OSTEOCLASTOGENESIS; OSTEOLYSIS; PROTEIN EXPRESSION; AGONISTS; ANIMAL; C57BL MOUSE; CHEMICALLY INDUCED; CYTOLOGY; DRUG EFFECTS; METABOLISM; OSTEOPOROSIS; PATHOLOGY;

ANIMALS; INSULIN; MALE; MICE; MICE, INBRED C57BL; OSTEOCLASTS; OSTEOPOROSIS; PPAR GAMMA; THIAZOLIDINEDIONES;

EID: 84922883000     PISSN: 08840431     EISSN: 15234681     Source Type: Journal    
DOI: 10.1002/jbmr.2364     Document Type: Article

References (44)

1. DeFronzo RA, Abdul-Ghani MA. Preservation of beta-cell function: The key to diabetes prevention. J Clin Endocrinol Metab. 2011;96(8): 2354-66.
2. Lehmann JM, Moore LB, Smith-Oliver TA, Wilkison WO, Willson TM, Kliewer SA. An antidiabetic thiazolidinedione is a high affinity ligand for peroxisome proliferator-activated receptor gamma (PPAR gamma). J Biol Chem. 1995;270(22): 12953-6.
3. Ahmadian M, Suh JM, Hah N, et al. PPAR gamma signaling and metabolism: The good, the bad and the future. Nat Med. 2013; 19(5): 557-66.
4. Evans RM, Barish GD, Wang YX. PPARs and the complex journey to obesity. Nat Med. 2004;10(4): 355-61.
5. Cariou B, Charbonnel B, Staels B. Thiazolidinediones and PPARgamma agonists: Time for a reassessment. Trends Endocrinol Metab. 2012;23(5): 205-15.
6. Teitelbaum SL. Osteoclasts: What do they do and how do they do it? Am J Pathol. 2007;170(2): 427-35.
7. PittengerMF, MackayAM, Beck SC, et al.Multilineage potential of adult human mesenchymal stem cells. Science. 1999;284(5411): 143-7.
8. Novack DV, Teitelbaum SL. The osteoclast: Friend or foe? Annu Rev Pathol. 2008;3: 457-84.
9. Collot-Teixeira S, Martin J, McDermott-Roe C, Poston R, McGregor JL. CD36 and macrophages in atherosclerosis. Cardiovasc Res. 2007;75(3): 468-77.
10. Silverstein RL, Febbraio M. CD36, a scavenger receptor involved in immunity, metabolism, angiogenesis, and behavior. Sci Signal. 2009;2(72): Re3.
11. Chawla A, Barak Y, Nagy L, Liao D, Tontonoz P, Evans RM. PPARgamma dependent and independent effects on macrophage-gene expression in lipid metabolism and inflammation. Nat Med. 2001;7(1): 48-52.
12. Helming L, Winter J, Gordon S. The scavenger receptor CD36 plays a role in cytokine-induced macrophage fusion. J Cell Sci. 2009;122(Pt 4): 453-9.
13. Tontonoz P, Nagy L, Alvarez JG, Thomazy VA, Evans RM. PPARgamma promotes monocyte/macrophage differentiation and uptake of oxidized LDL. Cell. 1998;93(2): 241-52.
14. Ballesteros I, Cuartero MI, Pradillo JM, et al. Rosiglitazone-induced CD36 up-regulation resolves inflammation by PPARgamma and 5-LO-dependent pathways. J Leukoc Biol. 2014;95(4): 587-98.
15. Akune T, Ohba S, Kamekura S, et al. PPARgamma insufficiency enhances osteogenesis through osteoblast formation from bone marrow progenitors. J Clin Invest. 2004;113(6): 846-55.
16. Barak Y, Nelson MC, Ong ES, et al. PPAR gamma is required for placental, cardiac, and adipose tissue development. Mol Cell. 1999;4(4): 585-95.
17. Wan Y. PPARgamma in bone homeostasis. Trends Endocrinol Metab. 2010;21(12): 722-8.
18. Wan Y, Chong LW, Evans RM. PPAR-gamma regulates osteoclastogenesis in mice. Nat Med. 2007;13(12): 1496-503.
19. Ali AA, Weinstein RS, Stewart SA, Parfitt AM, Manolagas SC, Jilka RL. Rosiglitazone causes bone loss in mice by suppressing osteoblast differentiation and bone formation. Endocrinology. 2005;146(3): 1226-35.
20. Lazarenko OP, Rzonca SO, HogueWR, Swain FL, Suva LJ, Lecka-Czernik B. Rosiglitazone induces decreases in bonemass and strength that are reminiscent of aged bone. Endocrinology. 2007;148(6): 2669-80.
21. Li M, Pan LC, Simmons HA, et al. Surface-specific effects of a PPARgamma agonist, darglitazone, on bone in mice. Bone. 2006; 39(4): 796-806.
22. Soroceanu MA, Miao D, Bai XY, Su H, Goltzman D, Karaplis AC. Rosiglitazone impacts negatively on bone by promoting osteoblast/osteocyte apoptosis. J Endocrinol. 2004;183(1): 203-16.
23. Sottile V, Seuwen K, Kneissel M. Enhanced marrow adipogenesis and bone resorption in estrogen-deprived rats treated with the PPARgamma agonist BRL49653 (rosiglitazone). Calcif Tissue Int. 2004;75(4): 329-37.
24. Rzonca SO, Suva LJ, Gaddy D, Montague DC, Lecka-Czernik B. Bone is a target for the antidiabetic compound rosiglitazone. Endocrinology. 2004;145(1): 401-6.
25. Chen Z, Vigueira PA, Chambers KT, et al. Insulin resistance and metabolic derangements in obese mice are ameliorated by a novel peroxisome proliferator-activated receptor gamma-sparing thiazolidinedione. J Biol Chem. 2012;287(28): 23537-48.
26. Faccio R, Zou W, Colaianni G, Teitelbaum SL, Ross FP. High dose MCSF partially rescues the Dap12-/-osteoclast phenotype. J Cell Biochem. 2003;90(5): 871-83.
27. Craft CS, Zou W, Watkins M, et al. Microfibril-associated glycoprotein-1, an extracellular matrix regulator of bone remodeling. J Biol Chem. 2010;285(31): 23858-67.
28. Ishii KA, Fumoto T, Iwai K, et al. Coordination of PGC-1beta and iron uptake in mitochondrial biogenesis and osteoclast activation. Nat Med. 2009;15(3): 259-66.
29. Wei W, Wang X, Yang M, et al. PGC1beta mediates PPARgamma activation of osteoclastogenesis and rosiglitazone-induced bone loss. Cell Metab. 2010;11(6): 503-16.
30. Tontonoz P, Spiegelman BM. Fat and beyond: The diverse biology of PPARgamma. Annu Rev Biochem. 2008;77: 289-312.
31. Duan SZ, Ivashchenko CY, Whitesall SE, et al. Hypotension, lipodystrophy, and insulin resistance in generalized PPARgamma-deficient mice rescued from embryonic lethality. J Clin Invest. 2007;117(3): 812-22.
32. Kletzien RF, Foellmi LA, Harris PK, Wyse BM, Clarke SD. Adipocyte fatty acid-binding protein: Regulation of gene expression in vivo and in vitro by an insulin-sensitizing agent. Mol Pharmacol. 1992; 42(4): 558-62.
33. Nolan JJ, Ludvik B, Beerdsen P, Joyce M, Olefsky J. Improvement in glucose tolerance and insulin resistance in obese subjects treated with troglitazone. N Engl J Med. 1994;331(18): 1188-93.
34. Day C. Thiazolidinediones: A new class of antidiabetic drugs. Diabet Med. 1999;16(3): 179-92.
35. Hauner H. The mode of action of thiazolidinediones. Diabetes Metab Res Rev. 2002;18(Suppl 2): S10-5.
36. Choi JH, Banks AS, Kamenecka TM, et al. Antidiabetic actions of a nonagonist PPARgamma ligand blocking Cdk5-mediated phosphorylation. Nature. 2011;477(7365): 477-81.
37. Choi JH, Banks AS, Estall JL, et al. Anti-diabetic drugs inhibit obesitylinked phosphorylation of PPARgamma by Cdk5. Nature. 2010; 466(7305): 451-6.
38. Feinstein DL, Spagnolo A, Akar C, et al. Receptor-independent actions of PPAR thiazolidinedione agonists: Is mitochondrial function the key? Biochem Pharmacol. 2005;70(2): 177-88.
39. Bricker DK, Taylor EB, Schell JC, et al. A mitochondrial pyruvate carrier required for pyruvate uptake in yeast, Drosophila, and humans. Science. 2012;337(6090): 96-100.
40. Divakaruni AS, Wiley SE, Rogers GW, et al. Thiazolidinediones are acute, specific inhibitors of the mitochondrial pyruvate carrier. Proc Natl Acad Sci USA. 2013;110(14): 5422-7.
41. Ackert-Bicknell CL, Shockley KR, Horton LG, Lecka-Czernik B, Churchill GA, Rosen CJ. Strain-specific effects of rosiglitazone on bone mass, body composition, and serum insulin-like growth factor-I. Endocrinology. 2009;150(3): 1330-40.
42. Lee B, Shao J. Adiponectin and energy homeostasis. Rev Endocr Metab Disord. 2014;15(2): 149-56.
43. Saltiel AR. You are what you secrete. Nat Med. 2001;7(8): 887-8.
44. Bruedigam C, Eijken M, Koedam M, et al. A new concept underlying stem cell lineage skewing that explains the detrimental effects of thiazolidinediones on bone. Stem Cells. 2010;28(5): 916-27.