Leptin treatment prevents type I diabetic marrow adiposity but not bone loss in mice

Journal of Cellular Physiology

Volumn 218, Issue 2, 2009, Pages 376-384

  Motyl, Katherine J ^a   McCabe, Laura R ^a,b  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b 2201 Biomedical Physical Science Bldg ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LEPTIN; RNA; INSULIN;

ADIPOCYTE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; INSULIN DEPENDENT DIABETES MELLITUS; MALE; MOUSE; NONHUMAN; OBESITY; OSSIFICATION; OSTEOLYSIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; TRABECULAR BONE; ANIMAL; BAGG ALBINO MOUSE; BLOOD; BODY WEIGHT; BONE MARROW; DRUG EFFECT; FEEDING BEHAVIOR; GLUCOSE BLOOD LEVEL; HYPERPHAGIA; METABOLISM; PATHOLOGY;

MUS; RODENTIA;

ADIPOSITY; ANIMALS; BLOOD GLUCOSE; BODY WEIGHT; BONE MARROW; BONE RESORPTION; DIABETES MELLITUS, TYPE 1; FEEDING BEHAVIOR; HYPERPHAGIA; INSULIN; LEPTIN; MICE; MICE, INBRED BALB C;

EID: 58149263759     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcp.21608     Document Type: Article

References (61)

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. Akirav EM, Chan O, Inouye K, Riddell MC, Matthews SG, Vranic M. 2004. Partial leptin restoration increases hypothalamic-pituitary-adrenal activity while diminishing weight loss and hyperphagia in streptozotocin diabetic rats. Metabolism 53:1558-1564.
3. 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.
4. Barzilai N, Wang J, Massilon D, Vuguin P, Hawkins M, Rossetti L. 1997. Leptin selectively decreases visceral adiposity and enhances insulin action. J Clin Invest 100:3105-3110.
5. 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.
6. Botolin S, McCabe LR. 2006. Inhibition of PPARgamma prevents type I diabetic bone marrow adiposity but not bone loss. J Cell Physiol 209:967-976.
7. Botolin S, McCabe LR. 2007. Bone loss and increased bone adiposity in spontaneous and pharmacologically induced diabetic mice. Endocrinology 148:198-205.
8. Bouillon R, Bex M, Van Herck E, Laureys J, Dooms L, Lesaffre E, Ravussin E. 1995. Influence of age, sex, and insulin on osteoblast function: Osteoblast dysfunction in diabetes mellitus. J Clin Endocrinol Metab 80:1194-1202.
9. Burguera B, Hofbauer LC, Thomas T, Gori F, Evans GL, Khosla S, Riggs BL, Turner RT. 2001. Leptin reduces ovariectomy-induced bone loss in rats. Endocrinology 142:3546-3553.
10. Chan JL, Mantzoros CS. 2005. Role of leptin in energy-deprivation states: Normal human physiology and clinical implications for hypothalamic amenorrhoea and anorexia nervosa. Lancet 366:74-85.
11. Considine RV, Sinha MK, Heiman ML, Kriauciunas A, Stephens TW, Nyce MR, Ohannesian JP, Marco CC, McKee LJ, Bauer TL, Caro JF. 1996. Serum immunoreactive-leptin concentrations in normal-weight and obese humans. N Engl J Med 334:292-295.
12. Cornish J, Callon KE, Bava U, Lin C, Naot D, Hill BL, Grey AB, Broom N, Myers DE, Nicholson GC, Reid IR. 2002. Leptin directly regulates bone cell function in vitro and reduces bone fragility in vivo. J Endocrinol 175:405-415.
13. Ducy P, Amling M, Takeda S, Priemel M, Schilling AF, Beil FT, Shen J, Vinson C, Rueger JM, Karsenty G. 2000. Leptin inhibits bone formation through a hypothalamic relay: A central control of bone mass. Cell 100:197-207.
14. Duque G. 2008. Bone and fat connection in aging bone. Curr Opin Rheumatol 20:429-434.
15. Fowlkes JL, Bunn RC, Liu L, Wahl EC, Coleman HN, Cockrell GE, Perrien DS, Lumpkin CK, Jr., Thrailkill KM. 2008. Runt-related transcription factor 2 (RUNX2) and RUNX2-related osteogenic genes are down-regulated throughout osteogenesis in type 1 diabetes mellitus. Endocrinology 149:1697-1704.
16. Gad HI. 2007. The potential osteogenic effects of systemic leptin and insulin administration in streptozotocin-induced diabetic female rats. Saudi Med J 28:1185-1190.
17. Gimble JM, Zvonic S, Floyd ZE, Kassem M, Nuttall ME. 2006. Playing with bone and fat. J Cell Biochem 98:251-266.
18. Goodman WG, Hori MT. 1984. Diminished bone formation in experimental diabetes. Relationship to osteoid maturation and mineralization. Diabetes 33:825-831.
19. Goulding A, Taylor RW. 1998. Plasma leptin values in relation to bone mass and density and to dynamic biochemical markers of bone resorption and formation in postmenopausal women. Calcif Tissue Int 63:456-458.
20. Gulen S, Dincer S. 2007. Effects of leptin on oxidative stress in healthy and Streptozotocin-induced diabetic rats. Mol Cell Biochem 302:59-65.
21. Hamrick MW. 2004. Leptin, bone mass, and the thrifty phenotype. J Bone Miner Res 19:1607-1611.
22. Hamrick MW, Della Fera MA, Choi YH, Hartzell D, Pennington C, Baile CA. 2007. Injections of leptin into rat ventromedial hypothalamus increase adipocyte apoptosis in peripheral fat and in bone marrow. Cell Tissue Res 327:133-141.
23. Hamrick MW, Della-Fera MA, Choi YH, Pennington C, Hartzell D, Baile CA. 2005. Leptin treatment induces loss of bone marrow adipocytes and increases bone formation in leptin-deficient ob/ob mice. J Bone Miner Res 20:994-1001.
24. Hamrick MW, Pennington C, Newton D, Xie D, Isales C. 2004. Leptin deficiency produces contrasting phenotypes in bones of the limb and spine. Bone 34:376-383.
25. Hanaki K, Becker DJ, Arslanian SA. 1999. Leptin before and after insulin therapy in children with new-onset type 1 diabetes. J Clin Endocrinol Metab 84:1524-1526.
26. Hidaka S, Yoshimatsu H, Kondou S, Tsuruta Y, Oka K, Noguchi H, Okamoto K, Sakino H, Teshima Y, Okeda T, Sakata T. 2002. Chronic central leptin infusion restores hyperglycemia independent of food intake and insulin level in streptozotocin-induced diabetic rats. FASEB J 16:509-518.
27. Irwin R, Lin HV, Motyl KJ, McCabe LR. 2006. Normal bone density obtained in the absence of insulin receptor expression in bone. Endocrinology 147:5760-5767.
28. Iwaniec UT, Boghossian S, Lapke PD, Turner RT, Kalra SP. 2007. Central leptin gene therapy corrects skeletal abnormalities in leptin-deficient ob/ob mice. Peptides 28:1012-1019.
29. Janghorbani M, Van Dam RM, Willett WC, Hu FB. 2007. Systematic review of type 1 and type 2 diabetes mellitus and risk of fracture. Am J Epidemiol 166:495-505.
30. Jilka RL, Weinstein RS, Takahashi K, Parfitt AM, Manolagas SC. 1996. Linkage of decreased bone mass with impaired osteoblastogenesis in a murine model of accelerated senescence. J Clin Invest 97:1732-1740.
31. Kajkenova O, Lecka-Czernik B, Gubrij I, Hauser SP, Takahashi K, Parfitt AM, Jilka RL, Manolagas SC, Lipschitz DA. 1997. Increased adipogenesis and myelopoiesis in the bone marrow of SAMP6, a murine model of defective osteoblastogenesis and low turnover osteopenia. J Bone Miner Res 12:1772-1779.
32. Karaguzel G, Ozdem S, Boz A, Bircan I, Akcurin S. 2006. Leptin levels and body composition in children and adolescents with type 1 diabetes. Clin Biochem 39:788-793.
33. Karsenty G. 2001. Leptin controls bone formation through a hypothalamic relay. Recent Prog Horm Res 56:401-415.
34. 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.
35. Kiess W, Anil M, Blum WF, Englaro P, Juul A, Attanasio A, Dotsch J, Rascher W. 1998. Serum leptin levels in children and adolescents with insulin-dependent diabetes mellitus in relation to metabolic control and body mass index. Eur J Endocrinol 138:501-509.
36. Kim GS, Hong JS, Kim SW, Koh JM, An CS, Choi JY, Cheng SL. 2003. Leptin induces apoptosis via ERK/cPLA2/cytochrome c pathway in human bone marrow stromal cells. J Biol Chem 278:21920-21929.
37. 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.
38. 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.
39. Lorentzon R, Alehagen U, Boquist L. 1986. Osteopenia in mice with genetic diabetes. Diabetes Res Clin Pract 2:157-163.
40. Martin A, David V, Malaval L, Lafage-Proust MH, Vico L, Thomas T. 2007. Opposite effects of leptin on bone metabolism: A dose-dependent balance related to energy intake and insulin-like growth factor-I pathway. Endocrinology 148:3419-3425.
41. Martin A, de Vittoris R, David V, Moraes R, Begeot M, Lafage-Proust MH, Alexandre C, Vico L, Thomas T. 2005. Leptin modulates both resorption and formation while preventing disuse-induced bone loss in tail-suspended female rats. Endocrinology 146:3652-3659.
42. Martin LM, McCabe LR. 2007. Type I diabetic bone phenotype is location but not gender dependent. Histochem Cell Biol 128:125-133.
43. Mathey J, Horcajada-Molteni MN, Chanteranne B, Picherit C, Puel C, Lebecque P, Cubizoles C, Davicco MJ, Coxam V, Barlet JP. 2002. Bone mass in obese diabetic Zucker rats: Influence of treadmill running. Calcif Tissue Int 70:305-311.
44. McCabe LR. 2007. Understanding the pathology and mechanisms of type I diabetic bone loss. J Cell Biochem 102:1343-1357.
45. Miyanaga F, Ogawa Y, Ebihara K, Hidaka S, Tanaka T, Hayashi S, Masuzaki H, Nakao K. 2003. Leptin as an adjunct of insulin therapy in insulin-deficient diabetes. Diabetologia 46:1329-1337.
46. Moerman EJ, Teng K, Lipschitz DA, Lecka-Czernik B. 2004. Aging activates adipogenic and suppresses osteogenic programs in mesenchymal marrow stroma/stem cells: The role of PPAR-gamma2 transcription factor and TGF-beta/BMP signaling pathways. Aging Cell 3:379-389.
47. 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.
48. Ontiveros C, McCabe LR. 2003. Simulated microgravity suppresses osteoblast phenotype, Runx2 levels and AP-1 transactivation. J Cell Biochem 88:427-437.
49. Page KA, Hartzell DL, Li C, Westby AL, Della-Fera MA, Azain MJ, Pringle TD, Baile CA. 2004. beta-Adrenergic receptor agonists increase apoptosis of adipose tissue in mice. Domest Anim Endocrinol 26:23-31.
50. Reseland JE, Syversen U, Bakke I, Qvigstad G, Eide LG, Hjertner O, Gordeladze JO, Drevon CA. 2001. Leptin is expressed in and secreted from primary cultures of human osteoblasts and promotes bone mineralization. J Bone Miner Res 16:1426-1433.
51. Rosen CJ, Bouxsein ML. 2006. Mechanisms of disease: Is osteoporosis the obesity of bone? Nat Clin Pract Rheumatol 2:35-43.
52. Sindelar DK, Havel PJ, Seeley RJ, Wilkinson CW, Woods SC, Schwartz MW. 1999. Low plasma leptin levels contribute to diabetic hyperphagia in rats. Diabetes 48:1275-1280.
53. Sivitz WI, Walsh SA, Morgan DA, Thomas MJ, Haynes WG. 1997. Effects of leptin on insulin sensitivity in normal rats. Endocrinology 138:3395-3401.
54. Steppan CM, Crawford DT, Chidsey-Frink KL, Ke H, Swick AG. 2000. Leptin is a potent stimulator of bone growth in ob/ob mice. Regul Pept 92:73-78.
55. Takeda S, Elefteriou F, Levasseur R, Liu X, Zhao L, Parker KL, Armstrong D, Ducy P, Karsenty G. 2002. Leptin regulates bone formation via the sympathetic nervous system. Cell 111:305-317.
56. Thomas T, Gori F, Khosla S, Jensen MD, Burguera B, Riggs BL. 1999. Leptin acts on human marrow stromal cells to enhance differentiation to osteoblasts and to inhibit differentiation to adipocytes. Endocrinology 140:1630-1638.
57. Vengellur A, LaPres JJ. 2004. The role of hypoxia inducible factor 1alpha in cobalt chloride induced cell death in mouse embryonic fibroblasts. Toxicol Sci 82:638-646.
58. 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.
59. Vestergaard P. 2007. Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2 diabetes - A meta-analysis. Osteoporos Int 18:427-444.
60. Wang JL, Chinookoswong N, Scully S, Qi M, Shi ZQ. 1999. Differential effects of leptin in regulation of tissue glucose utilization in vivo. Endocrinology 140:2117-2124.
61. Wiren KM, Zhang XW, Toombs AR, Kasparcova V, Gentile MA, Harada S, Jepsen KJ. 2004. Targeted overexpression of androgen receptor in osteoblasts: Unexpected complex bone phenotype in growing animals. Endocrinology 145:3507-3522.