Inhibition of PPARγ prevents type I diabetic bone marrow adiposity but not bone loss

Journal of Cellular Physiology

Volumn 209, Issue 3, 2006, Pages 967-976

  Botolin, Sergiu ^a   McCabe, Laura R ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2,2 BIS(4 GLYCIDYLOXYPHENYL)PROPANE; 4,4' ISOPROPYLIDENEDIPHENOL; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; UNCLASSIFIED DRUG; 2,2-BIS(4-GLYCIDYLOXYPHENYL)PROPANE; BIOLOGICAL MARKER; EPOXIDE;

ADIPOCYTE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE DENSITY; BONE MARROW; CELL DIFFERENTIATION; CONTROLLED STUDY; FATTY ACID BLOOD LEVEL; GENE EXPRESSION; HYPERGLYCEMIA; HYPERLIPIDEMIA; INSULIN DEPENDENT DIABETES MELLITUS; MALE; NONHUMAN; OBESITY; OSTEOBLAST; OSTEOLYSIS; PRIORITY JOURNAL; TRIACYLGLYCEROL BLOOD LEVEL; WEIGHT REDUCTION; ANIMAL; BAGG ALBINO MOUSE; CELL CULTURE; CYTOLOGY; DRUG ANTAGONISM; DRUG EFFECT; EXPERIMENTAL DIABETES MELLITUS; GENETICS; METABOLISM; MOUSE; NONOBESE DIABETIC MOUSE; OSTEOPOROSIS; PHYSIOLOGY; RADIOGRAPHY; TIBIA;

ADIPOCYTES; ANIMALS; BIOLOGICAL MARKERS; BONE MARROW; CELL DIFFERENTIATION; CELLS, CULTURED; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; EPOXY COMPOUNDS; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED NOD; OSTEOBLASTS; OSTEOPOROSIS; PPAR GAMMA; TIBIA;

EID: 33750506697     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcp.20804     Document Type: Article

References (59)

1. Ahdjoudj S, Lasmoles F, Holy X, Zerath E, Marie PJ. 2002. Transforming growth factor beta2 inhibits adipocyte differentiation induced by skeletal unloading in rat bone marrow stroma. J Bone Miner Res 17:668-677.
2. Ahdjoudj S, Fromigue O, Marie PJ. 2004. Plasticity and regulation of human bone marrow stromal osteoprogenitor cells: Potential implication in the treatment of age-related bone loss. Histol Histopathol 19:151-157.
3. Akune T, Ohba S, Kamekura S, Yamaguchi M, Chung UI, Kubota N, Terauchi Y, Harada Y, Azuma Y, Nakamura K, Kadowaki T, Kawaguchi H. 2004. PPARgamma insufficiency enhances osteogenesis through osteoblast formation from bone marrow progenitors. J Clin Invest 113:846-855.
4. Ali AA, Weinstein RS, Stewart SA, Parfitt AM, Manolagas SC, Jilka RL. 2005. Rosiglitazone causes bone loss in mice by suppressing osteoblast differentiation and bone formation. Endocrinology 146:1226-1235.
5. Auwerx J, Dequeker J, Bouillon R, Geusens P, Nijs J. 1988. Mineral metabolism and bone mass at peripheral and axial skeleton in diabetes mellitus. Diabetes 37:8-12.
6. Botolin S, Faugere MC, Malluche H, Orth M, Meyer R, McCabe LR. 2005. Increased bone adiposity and peroxisomal proliferator-activated receptor-gamma2 expression in type I diabetic mice. Endocrinology 146:3622-3631.
7. Bouillon R. 1991. Diabetic bone disease [editorial]. Calcif Tissue Int 49:155-160.
8. Buysschaert M, Cauwe F, Jamart J, Brichant C, De Coster P, Magnan A, Donckier J. 1992. Proximal femur density in type 1 and 2 diabetic patients. Diabete Metab 18:32-37.
9. Chomczynski P, Sacchi N. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156-159.
10. Christeff N, Homo-Delarche F, Thobie N, Durant S, Dardenne M, Nunez EA. 1994. Free fatty acid profiles in the non-obese diabetic (NOD) mouse: Basal serum levels and effects of endocrine manipulation. Prostaglandins Leukot Essent Fatty Acids 51:125-131.
11. Cock TA, Back J, Elefteriou F, Karsenty G, Kastner P, Chan S, Auwerx J. 2004. Enhanced bone formation in lipodystrophic PPARgamma(hyp/hyp) mice relocates haematopoiesis to the spleen. EMBO Rep 5:1007-1012.
12. Cullen P, von Eckardstein A, Souris S, Schulte H, Assmann G. 1999. Dyslipidaemia and cardiovascular risk in diabetes. Diabetes Obes Metab 1:189-198.
13. Cuzzocrea S, Pisano B, Dugo L, Ianaro A, Maffia P, Patel NS, Di Paola R, Ialenti A, Genovese T, Chatterjee PK, Di Rosa M, Caputi AP, Thiemermann C. 2004. Rosiglitazone, a ligand of the peroxisome proliferator-activated receptor-gamma, reduces acute inflammation. Eur J Pharmacol 483:79-93.
14. Diascro DD Jr, Vogel RL, Johnson TE, Witherup KM, Pitzenberger SM, Rutledge SJ, Prescott DJ, Rodan GA, Schmidt A. 1998. High fatty acid content in rabbit serum is responsible for the differentiation of osteoblasts into adipocyte-like cells. J Bone Miner Res 13:96-106.
15. Duque G. 2003. Will reducing adopogenesis in bone increase bone mass? PPARgamma2 as a key target in the treatment of age-related bone loss. Drug News Perspect 16:341-346.
16. Ferre P. 2004. The biology of peroxisome proliferator-activated receptors: Relationship with lipid metabolism and insulin sensitivity. Diabetes 53 (Suppl 1):S43-S50.
17. Folk JW, Starr AJ, Early JS. 1999. Early wound complications of operative treatment of calcaneus fractures: Analysis of 190 fractures. J Orthop Trauma 13:369-372.
18. Forsen L, Meyer HE, Midthjell K, Edna TH. 1999. Diabetes mellitus and the incidence of hip fracture: Results from the Nord-Trondelag Health Survey. Diabetologia 42:920-925.
19. Gunczler P, Lanes R, Paz-Martinez V, Martins R, Esaa S, Colmenares V, Weisinger JR. 1998. Decreased lumbar spine bone mass and low bone turnover in children and adolescents with insulin dependent diabetes mellitus followed longitudinally. J Pediatr Endocrinol Metab 11:413-419.
20. Hadjadj S, Duly-Bouhanick B, Bekherraz A, BrIdoux F, Gallois Y, Mauco G, Ebran J, Marre M. 2004. Serum triglycerides are a predictive factor for the development and the progression of renal and retinal complications in patients with type 1 diabetes. Diabetes Metab 30:43-51.
21. Hampson G, Evans C, Petitt RJ, Evans WD, Woodhead SJ, Peters JR, Ralston SH. 1998. Bone mineral density, collagen type 1 alpha 1 genotypes and bone turnover in premenopausal women with diabetes mellitus. Diabetologia 41:1314-1320.
22. Herskind AM, Christensen K, Norgaard-Andersen K, Andersen JF. 1992. Diabetes mellitus and healing of closed fractures. Diabete Metab 18:63-64.
23. Hui SL, Epstein S, Johnston CC Jr. 1985. A prospective study of bone mass in patients with type I diabetes. J Clin Endocrinol Metab 60:74-80.
24. Jackson SM, Demer LL. 2000. Peroxisome proliferator-activated receptor activators modulate the osteoblastic maturation of MC3T3-E1 preosteoblasts. FEBS Lett 471:119-124.
25. Kast-Woelbern HR, Dana SL, Cesario RM, Sun L, de Grandpre LY, Brooks ME, Osburn DL, Reifel-Miller A, Klausing K, Leibowitz MD. 2004. Rosiglitazone induction of Insig-1 in white adipose tissue reveals a novel interplay of peroxisome proliferator-activated receptor gamma and sterol regulatory element-binding protein in the regulation of adipogenesis. J Biol Chem 279:23908-23915.
26. Kemink SA, Hermus AR, Swinkels LM, Lutterman JA, Smals AG. 2000. Osteopenia in insulin-dependent diabetes mellitus; prevalence and aspects of pathophysiology. J Endocrinol Invest 23:295-303.
27. Knouff C, Auwerx J. 2004. Peroxisome proliferator-activated receptor-gamma calls for activation in moderation: Lessons from genetics and pharmacology. Endocr Rev 25:899-918.
28. Krakauer JC, McKenna MJ, Buderer NF, Rao DS, Whitehouse FW, Parfitt AM. 1995. Bone loss and bone turnover in diabetes. Diabetes 44:775-782.
29. Lazarenko OP, Rzonca SO, Suva LJ, Lecka-Czernik B. 2006. Netoglitazone is a PPAR-gamma ligand with selective effects on bone and fat. Bone 38:74-84.
30. Lecka-Czernik B, Moerman EJ, Grant DF, Lehmann JM, Manolagas SC, Jilka RL. 2002. Divergent effects of selective peroxisome proliferator-activated receptor-gamma 2 ligands on adipocyte versus osteoblast differentiation. Endocrinology 143:2376-2384.
31. Levin ME, Boisseau VC, Avioli LV. 1976. Effects of diabetes mellitus on bone mass in juvenile and adult-onset diabetes. N Engl J Med 294:241-245.
32. Lewis ML, Hughes-Fulford M. 2000. Regulation of heat shock protein message in Jurkat cells cultured under serum-starved and gravity-altered conditions. J Cell Biochem 77:127-134.
33. Li J, Takaishi K, Cook W, McCorkle SK, Unger RH. 2003. Insig-1 "brakes" lipogenesis in adipocytes and inhibits differentiation of preadipocytes. Proc Natl Acad Sci USA 100:9476-9481.
34. McBeath R, Pirone DM, Nelson CM, Bhadriraju K, Chen CS. 2004. Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev Cell 6:483-495.
35. McCabe LR, Kockx M, Lian J, Stein J, Stein G. 1995. Selective expression of fos- and jun-related genes during osteoblast proliferation and differentiation. Exp Cell Res 218:255-262.
36. McNair P, Christiansen C, Christensen MS, Madsbad S, Faber OK, Binder C, Transbol I. 1981. Development of bone mineral loss in insulin-treated diabetes: A 1 1/2 years follow-up study in sixty patients. Eur J Clin Invest 11:55-59.
37. Munoz-Torres M, Jodar E, Escobar-Jimenez F, Lopez-Ibarra PJ, Luna JD. 1996. Bone mineral density measured by dual X-ray absorptiometry in Spanish patients with insulin-dependent diabetes mellitus. Calcif Tissue Int 58:316-319.
38. Nuttall ME, Gimble JM. 2004. Controlling the balance between osteoblastogen-esis and adipogenesis and the consequent therapeutic implications. Curr Opin Pharmacol 4:290-294.
39. Nuttall ME, Patton AJ, Olivera DL, Nadeau DP, Gowen M. 1998. Human trabecular bone cells are able to express both osteoblastic and adipocytic phenotype: Implications for osteopenic disorders. J Bone Miner Res 13:371-382.
40. Ontiveros C, McCabe LR. 2003. Simulated microgravity suppresses osteoblast phenotype. runx2 levels and AP-1 transactivation. J Cell Biochem 88:427-437.
41. Ontiveros C, Irwin R, Wiseman RW, McCabe LR. 2004. Hypoxia suppresses runx2 independent of modeled microgravity. J Cell Physiol 200:169-176.
42. Parhami F, Jackson SM, Tintut Y, Le V, Balucan JP, Territo M, Demer LL. 1999. Atherogenic diet and minimally oxidized low density lipoprotein inhibit osteogenic and promote adipogenic differentiation of marrow stromal cells. J Bone Miner Res 14:2067-2078.
43. Pechhold K, Patterson NB, Blum C, Fleischacker CL, Boehm BO, Harlan DM. 2001. Low dose streptozotocin-induced diabetes in rat insulin promoter-mCD80-transgenic mice is T cell autoantigen-specific and CD28 dependent. J Immunol 166:2531-2539.
44. Picard F, Auwerx J. 2002. PPAR(gamma) and glucose homeostasis. Annu Rev Nutr 22:167-197.
45. Piepkorn B, Kann P, Forst T, Andreas J, Pfutzner A, Beyer J. 1997. Bone mineral density and bone metabolism in diabetes mellitus. Horm Metab Res 29:584-591.
46. Pighin D, Karabatas L, Pastorale C, Dascal E, Carbone C, Chicco A, Lombardo YB, Basabe JC. 2005. Role of lipids in the early developmental stages of experimental immune diabetes induced by multiple low-dose streptozotocin. J Appl Physiol 98:1064-1069.
47. Prentki M, Joly E, El-Assaad W, Roduit R. 2002. Malonyl-CoA signaling, lipid partitioning, and glucolipotoxicity: Role in beta-cell adaptation and failure in the etiology of diabetes. Diabetes 51 (Suppl 3):S405-S413.
48. Rzonca SO, Suva LJ, Gaddy D, Montague DC, Lecka-Czernik B. 2004. Bone is a target for the antidiabetic compound rosiglitazone. Endocrinology 145:401-406.
49. Schwartz AV, Sellmeyer DE, Ensrud KE, Cauley JA, Tabor HK, Schreiner PJ, Jamal SA, Black DM, Cummings SR. 2001. Older women with diabetes have an increased risk of fracture: A prospective study. J Clin Endocrinol Metab 86:32-38.
50. Szkudelski T. 2001. The mechanism of alloxan and streptozotocin action in B cells of the rat pancreas. Physiol Res 50:537-546.
51. Tornvig L, Mosekilde LI, Justesen J, Falk E, Kassem M. 2001. Troglitazone treatment increases bone marrow adipose tissue volume but does not affect trabecular bone volume in mice. Calcif Tissue Int 69:46-50.
52. Trogan E, Choudhury RP, Dansky HM, Hong JX, Breslow JL, Fisher EA. 2002. Laser capture microdissection analysis of gene expression in macrophages from atherosclerotic lesions of apolipoprotein E-deficient mice. Proc Natl Acad Sci USA 99:2234-2239.
53. Tuominen JT, Impivaara O, Puukka P, Ronnemaa T. 1999. Bone mineral density in patients with type 1 and type 2 diabetes. Diabetes Care 22:1196-1200.
54. Verma S, Rajaratnam JH, Denton J, Hoyland JA, Byers RJ. 2002. Adipocytic proportion of bone marrow is inversely related to bone formation in osteoporosis. J Clin Pathol 55:693-698.
55. White CB, Turner NS, Lee GC, Haidukewych GJ. 2003. Open ankle fractures in patients with diabetes mellitus. Clin Orthop 414:37-44.
56. Wiske PS, Wentworth SM, Norton JA Jr, Epstein S, Johnston CC Jr. 1982. Evaluation of bone mass and growth in young diabetics. Metabolism 31:848-854.
57. Wright HM, Clish CB, Mikami T, Hauser S, Yanagi K, Hiramatsu R, Serhan CN, Spiegelman BM. 2000. A synthetic antagonist for the peroxisome proliferator-activated receptor gamma inhibits adipocyte differentiation. J Biol Chem 275:1873-1877.
58. Yoshimatsu M, Shibata Y, Kitaura H, Chang X, Moriishi T, Hashimoto F, Yoshida N, Yamaguchi A. 2006. Experimental model of tooth movement by orthodontic force in mice and its application to tumor necrosis factor receptor-deficient mice. J Bone Miner Metab 24:20-27.
59. Zhang W, Lu D, Kawazu S, Komeda K, Takeuchi T. 2002. Adenoviral insulin gene therapy prolongs survival of IDDM model BB rats by improving hyperlipidemia. Horm Metab Res 34:577-582.