Understanding the skeletal pathology of type 1 and 2 diabetes mellitus

Critical Reviews in Eukaryotic Gene Expression

Volumn 21, Issue 2, 2011, Pages 187-206

  McCabe, Laura R ^a   Zhang, Jing ^a   Raehtz, Sandi ^a  

^a MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPOCYTOKINE; ADVANCED GLYCATION END PRODUCT; AMINO TERMINAL TELOPEPTIDE; CALCIUM; CARBOXY TERMINAL TELOPEPTIDE; COLLAGEN TYPE 1; COLLAGENASE 3; DEOXYPYRIDINOLINE; FIBROBLAST GROWTH FACTOR 2; INSULIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; INTERSTITIAL COLLAGENASE; OSTEOCALCIN; OSTEOPROTEGERIN; PARATHYROID HORMONE; PROSTAGLANDIN E2; SOMATOMEDIN BINDING PROTEIN 3; SOMATOMEDIN C; TUMOR NECROSIS FACTOR ALPHA; VITAMIN D;

BONE DENSITY; BONE DISEASE; BONE MATRIX; DIABETIC PATIENT; FEMUR NECK FRACTURE; FRACTURE; GLYCATION; HUMAN; HYPERGLYCEMIA; INFLAMMATION; INSULIN DEPENDENT DIABETES MELLITUS; INSULIN SENSITIVITY; LIFESPAN; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OSTEOBLAST; OSTEOCLAST; OSTEOLYSIS; OSTEOPENIA; OSTEOPOROSIS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; RADIUS FRACTURE; REVIEW; SPINE FRACTURE; WELLBEING;

EID: 80755136754     PISSN: 10454403     EISSN: None     Source Type: Journal    
DOI: 10.1615/CritRevEukarGeneExpr.v21.i2.70     Document Type: Review

References (243)

1. Parfitt AM. The coupling of bone formation to bone resorption: a critical analysis of the concept and of its relevance to the pathogenesis of osteoporosis. Metab Bone Dis Relat Res. 1982;4(1):1-6.
2. Mundy GR. Local factors in bone remodeling. Recent Prog Horm Res. 1989;45:507-27.
3. Hayward M, Fiedler-Nagy C. Mechanisms of bone loss: rheumatoid arthritis, periodontal disease and osteoporosis. Agents Actions. 1987;22(3-4):251-4.
4. Morrison L, Bogan I. Bone development in diabetic children: a roentgen study. Am J Med Sci. 1927;174:313-18.
5. Bouillon R, Bex M, Van Herck E, Laureys J, Dooms L, Lesaffre E, Ravussin E. Influence of age, sex, and insulin on osteoblast function: osteoblast dysfunction in diabetes mellitus. J Clin Endocrinol Metab. 1995;80(4):1194-202.
6. Kemink SA, Hermus AR, Swinkels LM, Lutterman JA, Smals AG. Osteopenia in insulin-dependent diabetes mellitus; prevalence and aspects of pathophysiology. J Endocrinol Invest. 2000;23(5):295-303.
7. Auwerx J, Dequeker J, Bouillon R, Geusens P, Nijs J. Mineral metabolism and bone mass at peripheral and axial skeleton in diabetes mellitus. Diabetes. 1988;37(1):8-12.
8. Krakauer JC, McKenna MJ, Buderer NF, Rao DS, Whitehouse FW, Parfitt AM. Bone loss and bone turnover in diabetes. Diabetes. 1995;44(7):775-82.
9. Levin ME, Boisseau VC, Avioli LV. Effects of diabetes mellitus on bone mass in juvenile and adult-onset diabetes. N Engl J Med. 1976;294(5):241-5.
10. Tuominen JT, Impivaara O, Puukka P, Ronnemaa T. Bone mineral density in patients with type 1 and type 2 diabetes. Diabetes Care. 1999;22(7):1196-200.
11. Munoz-Torres M, Jodar E, Escobar-Jimenez F, Lopez-Ibarra PJ, Luna JD. Bone mineral density measured by dual X-ray absorptiometry in Spanish patients with insulin-dependent diabetes mellitus. Calcif Tissue Int. 1996;58(5):316-9.
12. Buysschaert M, Cauwe F, Jamart J, Brichant C, De Coster P, Magnan A, Donckier J. Proximal femur density in type 1 and 2 diabetic patients. Diabete Metab. 1992;18(1):32-7.
13. Alexopoulou O, Jamart J, Devogelaer JP, Brichard S, de Nayer P, Buysschaert M. Bone density and markers of bone remodeling in type 1 male diabetic patients. Diabetes Metab. 2006;32(5 Pt 1):453-8.
14. Forsen L, Meyer HE, Midthjell K, Edna TH. Diabetes mellitus and the incidence of hip fracture: results from the Nord-Trondelag Health Survey. Diabetologia. 1999;42(8):920-5.
15. Bouillon R. Diabetic bone disease [editorial]. Calcif Tissue Int. 1991;49(3):155-60.
16. Bouillon R. Diabetic bone disease. Low turnover osteoporosis related to decreased IGF-I production. Verh K Acad Geneeskd Belg. 1992;54(4):365-91.
17. Hofbauer LC, Brueck CC, Singh SK, Dobnig H. Osteoporosis in patients with diabetes mellitus. J Bone Miner Res. 2007;22(9):1317-28.
18. Khazai NB, Beck GR Jr., Umpierrez GE. Diabetes and fractures: an overshadowed association. Curr Opin Endocrinol Diabetes Obes. 2009;16(6):435-45.
19. Inzerillo AM, Epstein S. Osteoporosis and diabetes mellitus. Rev Endocr Metab Disord. 2004;5(3):261-8.
20. Strotmeyer ES, Cauley JA, Orchard TJ, Steenkiste AR, Dorman JS. Middle-aged premenopausal women with type 1 diabetes have lower bone mineral density and calcaneal quantitative ultrasound than nondiabetic women. Diabetes Care. 2006;29(2):306-11.
21. Hadjidakis DJ, Raptis AE, Sfakianakis M, Mylonakis A, Raptis SA. Bone mineral density of both genders in Type 1 diabetes according to bone composition. J Diabetes Complications. 2006;20(5):302-7.
22. Christensen JO, Svendsen OL. Bone mineral in pre-and postmenopausal women with insulin-dependent and non-insulin-dependent diabetes mellitus. Osteoporos Int. 1999;10(4):307-11.
23. Ingberg CM, Palmer M, Aman J, Arvidsson B, Schvarcz E, Berne C. Body composition and bone mineral density in long-standing type 1 diabetes. J Intern Med. 2004;255(3):392-8.
24. Saha MT, Sievanen H, Salo MK, Tulokas S, Saha HH. Bone mass and structure in adolescents with type 1 diabetes compared to healthy peers. Osteoporos Int. 2009;20(8):1401-6.
25. Lunt H, Florkowski CM, Cundy T, Kendall D, Brown LJ, Elliot JR, Wells JE, Turner JG. A population-based study of bone mineral density in women with longstanding type 1 (insulin dependent) diabetes. Diabetes Res Clin Pract. 1998;40(1):31-8.
26. Nicodemus KK, Folsom AR. Type 1 and type 2 diabetes and incident hip fractures in postmenopausal women. Diabetes Care. 2001;24(7):1192-7.
27. Nevitt MC, Ettinger B, Black DM, Stone K, Jamal SA, Ensrud K, Segal M, Genant HK, Cummings SR. The association of radiographically detected vertebral fractures with back pain and function: a prospective study. Ann Intern Med. 1998;128(10):793-800.
28. Hamilton EJ, Rakic V, Davis WA, Chubb SA, Kamber N, Prince RL, Davis TM. Prevalence and predictors of osteopenia and osteoporosis in adults with Type 1 diabetes. Diabet Med. 2009;26(1):45-52.
29. Meyer HE, Tverdal A, Falch JA. Risk factors for hip fracture in middle-aged Norwegian women and men. Am J Epidemiol. 1993;137(11):1203-11.
30. Miao J, Brismar K, Nyren O, Ugarph-Morawski A, Ye W. Elevated hip fracture risk in type 1 diabetic patients: a population-based cohort study in Sweden. Diabetes Care. 2005;28(12):2850-5.
31. Schwartz AV, Sellmeyer DE, Ensrud KE, Cauley JA, Tabor HK, Schreiner PJ, Jamal SA, Black DM, Cummings SR. Older women with diabetes have an increased risk of fracture: a prospective study. J Clin Endocrinol Metab. 2001;86(1):32-8.
32. Janghorbani M, Van Dam RM, Willett WC, Hu FB. Systematic review of type 1 and type 2 diabetes mellitus and risk of fracture. Am J Epidemiol. 2007;166(5):495-505.
33. Bechtold S, Dirlenbach I, Raile K, Noelle V, Bonfig W, Schwarz HP. Early manifestation of type 1 diabetes in children is a risk factor for changed bone geometry: data using peripheral quantitative computed tomography. Pediatrics. 2006;118(3):e627-34.
34. Gunczler P, Lanes R, Paz-Martinez V, Martins R, Esaa S, Colmenares V, Weisinger JR. Decreased lumbar spine bone mass and low bone turnover in children and adolescents with insulin dependent diabetes mellitus followed longitudinally. J Pediatr Endocrinol Metab. 1998;11(3):413-19.
35. Wiske PS, Wentworth SM, Norton JA Jr, Epstein S, Johnston CC Jr. Evaluation of bone mass and growth in young diabetics. Metabolism. 1982;31(8):848-54.
36. Vestergaard P, Rejnmark L, Mosekilde L. Diabetes and its complications and their relationship with risk of fractures in type 1 and 2 diabetes. Calcif Tissue Int. 2009;84(1):45-55.
37. McCabe LR. Understanding the pathology and mechanisms of type I diabetic bone loss. J Cell Biochem. 2007;102(6):1343-57.
38. Botolin S, McCabe LR. Bone loss and increased bone adiposity in spontaneous and pharmacologically induced diabetic mice. Endocrinology. 2007;148(1):198-205.
39. Bain S, Ramamurthy NS, Impeduglia T, Scolman S, Golub LM, Rubin C. Tetracycline prevents cancellous bone loss and maintains near-normal rates of bone formation in streptozotocin diabetic rats. Bone. 1997;21(2):147-53.
40. Botolin S, Faugere MC, Malluche H, Orth M, Meyer R, McCabe LR. Increased bone adiposity and peroxisomal proliferator-activated receptor-gamma2 expression in type I diabetic mice. Endocrinology. 2005;146(8):3622-31.
41. Epstein S, Takizawa M, Stein B, Katz IA, Joffe II, Romero DF, Liang XG, Li M, Ke HZ, Jee WS, Jacobs W, Berlin J. Effect of cyclosporin A on bone mineral metabolism in experimental diabetes mellitus in the rat. J Bone Miner Res. 1994;9(4):557-66.
42. Glajchen N, Epstein S, Ismail F, Thomas S, Fallon M, Chakrabarti S. Bone mineral metabolism in experimental diabetes mellitus: osteocalcin as a measure of bone remodeling. Endocrinology. 1988;123(1):290-5.
43. Verhaeghe J, Suiker AM, Visser WJ, 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(3):485-92.
44. Shires R, Teitelbaum SL, Bergfeld MA, Fallon MD, Slatopolsky E, Avioli LV. The effect of streptozotocin-induced chronic diabetes mellitus on bone and mineral homeostasis in the rat. J Lab Clin Med. 1981;97(2):231-40.
45. Motyl K, McCabe LR. Streptozotocin, type I diabetes severity and bone. Biol Proced Online. 2009;11(1):296-315.
46. Martin LM, McCabe LR. Type I diabetic bone phenotype is location but not gender dependent. Histochem Cell Biol. 2007;128(2):125-33.
47. Herrero S, Calvo OM, Garcia-Moreno C, Martin E, San Roman JI, Martin M, Garcia-Talavera JR, Calvo JJ, del Pino-Montes J. Low bone density with normal bone turnover in ovariectomized and streptozotocin-induced diabetic rats. Calcif Tissue Int. 1998;62(3):260-5.
48. Hanley DA, Brown JP, Tenenhouse A, Olszynski WP, Ioannidis G, Berger C, Prior JC, Pickard L, Murray TM, Anastassiades T, Kirkland S, Joyce C, Joseph L, Papaioannou A, Jackson SA, Poliquin S, Adachi JD. Associations among disease conditions, bone mineral density, and prevalent vertebral deformities in men and women 50 years of age and older: cross-sectional results from the Canadian Multicentre Osteoporosis Study. J Bone Miner Res. 2003;18(4):784-90.
49. Strotmeyer ES, Cauley JA, Schwartz AV, Nevitt MC, Resnick HE, Zmuda JM, Bauer DC, Tylavsky FA, de Rekeneire N, Harris TB, Newman AB. Diabetes is associated independently of body composition with BMD and bone volume in older white and black men and women: the Health, Aging, and Body Composition Study. J Bone Miner Res. 2004;19(7):1084-91.
50. Bonds DE, Larson JC, Schwartz AV, Strotmeyer ES, Robbins J, Rodriguez BL, Johnson KC, Margolis KL. Risk of fracture in women with type 2 diabetes: the Women's Health Initiative Observational Study. J Clin Endocrinol Metab. 2006;91(9):3404-10.
51. Burghardt AJ, Issever AS, Schwartz AV, Davis KA, Masharani U, Majumdar S, Link TM. High-resolution peripheral quantitative computed tomographic imaging of cortical and trabecular bone microarchitecture in patients with type 2 diabetes mellitus. J Clin Endocrinol Metab. 2010 Nov;95(11):5045-55.
52. Cummings SR, Nevitt MC, Browner WS, Stone K, Fox KM, Ensrud KE, Cauley J, Black D, Vogt TM. Risk factors for hip fracture in white women. Study of Osteoporotic Fractures Research Group. N Engl J Med. 1995;332(12):767-73.
53. Petit MA, Paudel ML, Taylor BC, Hughes JM, Strotmeyer ES, Schwartz AV, Cauley JA, Zmuda JM, Hoffman AR, Ensrud KE. Bone mass and strength in older men with type 2 diabetes: the Osteoporotic Fractures in Men Study. J Bone Miner Res. 2010 Feb;25(2):285-91.
54. Gregorio F, Cristallini S, Santeusanio F, Filipponi P, Fumelli P. Osteopenia associated with non-insulin-dependent diabetes mellitus: what are the causes? Diabetes Res Clin Pract. 1994;23(1):43-54.
55. Schwartz AV. Diabetes mellitus: does it affect bone? Calcif Tissue Int. 2003;73(6):515-9.
56. Rakel A, Sheehy O, Rahme E, LeLorier J. Osteoporosis among patients with type 1 and type 2 diabetes. Diabetes Metab. 2008;34(3):193-205.
57. Vestergaard P. Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2 diabetes- a meta-analysis. Osteoporos Int. 2007;18(4):427-44.
58. Lipscombe LL, Jamal SA, Booth GL, Hawker GA. The risk of hip fractures in older individuals with diabetes: a population-based study. Diabetes Care. 2007;30(4):835-41.
59. Strotmeyer ES, Cauley JA, Schwartz AV, Nevitt MC, Resnick HE, Bauer DC, Tylavsky FA, de Rekeneire N, Harris TB, Newman AB. Nontraumatic fracture risk with diabetes mellitus and impaired fasting glucose in older white and black adults: the health, aging, and body composition study. Arch Intern Med. 2005;165(14):1612-7.
60. Janghorbani M, Feskanich D, Willett WC, Hu F. Prospective study of diabetes and risk of hip fracture: the Nurses' Health Study. Diabetes Care. 2006;29(7):1573-8.
61. Taylor BC, Schreiner PJ, Stone KL, Fink HA, Cummings SR, Nevitt MC, Bowman PJ, Ensrud KE. Long-term prediction of incident hip fracture risk in elderly white women: study of osteoporotic fractures. J Am Geriatr Soc. 2004;52(9):1479-86.
62. Ottenbacher KJ, Ostir GV, Peek MK, Goodwin JS, Markides KS. Diabetes mellitus as a risk factor for hip fracture in mexican american older adults. J Gerontol A Biol Sci Med Sci. 2002;57(10):M648-53.
63. Heath H 3rd, Melton LJ 3rd, Chu CP. Diabetes mellitus and risk of skeletal fracture. N Engl J Med. 1980;303(10):567-70.
64. Korpelainen R, Korpelainen J, Heikkinen J, Väänänen K, Keinänen-Kiukaanniemi S. Lifestyle factors are associated with osteoporosis in lean women but not in normal and overweight women: a population-based cohort study of 1222 women. Osteoporos Int. 2003;14(1):34-43.
65. Dobnig H, Piswanger-Sölkner JC, Roth M, Obermayer-Pietsch B, Tiran A, Strele A, Maier E, Maritschnegg P, Sieberer C, Fahrleitner-Pammer A. Type 2 diabetes mellitus in nursing home patients: effects on bone turnover, bone mass, and fracture risk. J Clin Endocrinol Metab. 2006;91(9):3355-63.
66. Kelsey JL, Browner WS, Seeley DG, Nevitt MC, Cummings SR. Risk factors for fractures of the distal forearm and proximal humerus. The Study of Osteoporotic Fractures Research Group. Am J Epidemiol. 1992;135(5):477-89.
67. 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):1292-9.
68. Mazziotti G, Gola M, Bianchi A, Porcelli T, Giampietro A, Cimino V, Doga M, Gazzaruso C, De Marinis L, Giustina A. Influence of diabetes mellitus on vertebral fractures in men with acromegaly. Endocrine. 2011 Aug;40(1):102-8.
69. 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):702-9.
70. Botushanov NP, Orbetzova MM. Bone mineral density and fracture risk in patients with type 1 and type 2 diabetes mellitus. Folia Med (Plovdiv). 2009;51(4):12-7.
71. Yamaguchi T, Yamamoto M, Kanazawa I, Yamauchi M, Yano S, Tanaka N, Nitta E, Fukuma A, Uno S, Sho-No T, Sugimoto T. Quantitative ultrasound and vertebral fractures in patients with type 2 diabetes. J Bone Miner Metab. 2011 Sep;29(5):626-32.
72. Shu A, Yin MT, Stein E, Cremers S, Dworakowski E, Ives R, Rubin MR. Bone structure and turnover in type 2 diabetes mellitus. Osteoporos Int. 2011 Mar 19. [Epub ahead of print]
73. Lumachi F, Camozzi V, Tombolan V, Luisetto G. Bone mineral density, osteocalcin, and bone-specific alkaline phosphatase in patients with insulin-dependent diabetes mellitus. Ann N Y Acad Sci. 2009;1173 Suppl 1:E64-7.
74. Cakatay U, Telci A, Kayali R, Akcay T, Sivas A, Aral F. Changes in bone turnover on deoxypyridinoline levels in diabetic patients. Diabetes Res Clin Pract. 1998;40(2):75-9.
75. Verhaeghe J, Oloumi G, van Herck E, van Bree R, Dequeker J, Einhorn TA, Bouillon R. Effects of long-term diabetes and/or high-dose 17 beta-estradiol on bone formation, bone mineral density, and strength in ovariectomized rats. Bone. 1997;20(5):421-8.
76. Ishida H, Seino Y, Taminato T, Usami M, Takeshita N, Tsutsumi C, Moriuchi S, Akiyama Y, Hara K. Circulating levels and bone contents of bone gamma-carboxyglutamic acid-containing protein are decreased in streptozocin-induced diabetes. Possible marker for diabetic osteopenia. Diabetes. 1988;37(6):702-6.
77. Motyl KJ, Botolin S, Irwin R, Appledorn DM, Kadakia T, Amalfitano A, Schwartz RC, McCabe LR. Bone inflammation and altered gene expression with type I diabetes early onset. J Cell Physiol. 2009;218(3):575-83.
78. Motyl KJ, McCabe LR. Leptin treatment prevents type I diabetic marrow adiposity but not bone loss in mice. J Cell Physiol. 2009;218(2):376-84.
79. Verhaeghe J, van Herck E, Visser WJ, Suiker AM, Thomasset M, Einhorn TA, Faierman E, Bouillon R. Bone and mineral metabolism in BB rats with long-term diabetes. Decreased bone turnover and osteoporosis. Diabetes. 1990;39(4):477-82.
80. Gopalakrishnan V, Vignesh RC, Arunakaran J, Aruldhas MM, Srinivasan N. Effects of glucose and its modulation by insulin and estradiol on BMSC differentiation into osteoblastic lineages. Biochem Cell Biol. 2006;84(1):93-101.
81. Botolin S, McCabe LR. Inhibition of PPARgamma prevents type I diabetic bone marrow adiposity but not bone loss. J Cell Physiol. 2006;209(3):967-76.
82. McCabe L. Switching fat from the periphery to bone-why in type I diabetes? Expert Rev Endocrinol Metab. 2009;4(3):203-7.
83. Coe LM, Irwin R, Lippner D, McCabe LR. The bone marrow microenvironment contributes to type I diabetes induced osteoblast death. J Cell Physiol. 2011 Feb;226(2):477-83.
84. Al-Mashat HA, Kandru S, Liu R, Behl Y, Desta T, Graves DT. Diabetes enhances mRNA levels of proapoptotic genes and caspase activity, which contribute to impaired healing. Diabetes. 2006;55(2):487-95.
85. Graves DT, Liu R, Oates TW. Diabetes-enhanced inflammation and apoptosis: impact on periodontal pathosis. Periodontol 2000. 2007;45:128-37.
86. Bonfanti R, Mora S, Prinster C, Bognetti E, Meschi F, Puzzovio M, Proverbio MC, Chiumello G. Bone modeling indexes at onset and during the first year of follow-Up in insulin-dependent diabetic children. Calcif Tissue Int. 1997;60 (5):397-400.
87. Bjorgaas M, Haug E, Johnsen HJ. The urinary excretion of deoxypyridinium cross-links is higher in diabetic than in nondiabetic adolescents. Calcif Tissue Int. 1999;65(2):121-4.
88. Cloos C, Wahl P, Hasslacher C, Traber L, Kistner M, Jurkuhn K, Schmidt-Gayk H. Urinary glycosylated, free and total pyridinoline and free and total deoxypyridinoline in diabetes mellitus. Clin Endocrinol (Oxf). 1998;48(3):317-23.
89. Mishima N, Sahara N, Shirakawa M, Ozawa H. Effect of streptozotocin-induced diabetes mellitus on alveolar bone deposition in the rat. Arch Oral Biol. 2002;47(12):843-9.
90. Locatto ME, Abranzon H, Caferra D, Fernandez MC, Alloatti R, Puche RC. Growth and development of bone mass in untreated alloxan diabetic rats. Effects of collagen glycosylation and parathyroid activity on bone turnover. Bone Miner. 1993;23(2):129-44.
91. Verhaeghe J, Thomsen JS, van Bree R, van Herck E, Bouillon R, Mosekilde L. Effects of exercise and disuse on bone remodeling, bone mass, and biomechanical competence in spontaneously diabetic female rats. Bone. 2000;27(2):249-56.
92. Horcajada-Molteni MN, Chanteranne B, Lebecque P, Davicco MJ, Coxam V, Young A, Barlet JP. Amylin and bone metabolism in streptozotocin-induced diabetic rats. J Bone Miner Res. 2001;16(5):958-65.
93. Kayal RA, Tsatsas D, Bauer MA, Allen B, Al-Sebaei MO, Kakar S, Leone CW, Morgan EF, Gerstenfeld LC, Einhorn TA, Graves DT. Diminished bone formation during diabetic fracture healing is related to the premature resorption of cartilage associated with increased osteoclast activity. J Bone Miner Res. 2007;22(4):560-8.
94. Kaneko H, Sasaki T, Ramamurthy NS, Golub LM. Tetracycline administration normalizes the structure and acid phosphatase activity of osteoclasts in streptozotocin-induced diabetic rats. Anat Rec. 1990;227(4):427-36.
95. Takeshita N, Ishida H, Yamamoto T, Koh G, Kurose T, Tsuji K, Okamoto Y, Ikeda H, Seino Y. Circulating levels and bone contents of bone gamma-carboxyglutamic acid-containing protein in rat models of non-insulin-dependent diabetes mellitus. Acta Endocrinol (Copenh). 1993;128(1):69-73.
96. Ahmad T, Ohlsson C, Saaf M, Ostenson CG, Kreicbergs A. Skeletal changes in type-2 diabetic Goto-Kakizaki rats. J Endocrinol. 2003;178(1):111-6.
97. Ostenson CG, Fiere V, Ahmed M, Lindstrom P, Brismar K, Brismar T, Kreicbergs A. Decreased cortical bone thickness in spontaneously non-insulin-dependent diabetic GK rats. J Diabetes Complications. 1997;11(6):319-22.
98. Ahmad T, Ugarph-Morawski A, Li J, Bileviciute-Ljungar I, Finn A, Ostenson CG, Kreicbergs A. Bone and joint neuropathy in rats with type-2 diabetes. Regul Pept. 2004;119(1-2):61-7.
99. Fujii H, Hamada Y, Fukagawa M. Bone formation in spontaneously diabetic Torii-newly established model of non-obese type 2 diabetes rats. Bone. 2008;42(2):372-9.
100. Hamada Y, Kitazawa S, Kitazawa R, Fujii H, Kasuga M, Fukagawa M. Histomorphometric analysis of diabetic osteopenia in streptozotocin-induced diabetic mice: a possible role of oxidative stress. Bone. 2007;40(5):1408-14.
101. Bai XC, Lu D, Bai J, Zheng H, Ke ZY, Li XM, Luo SQ. Oxidative stress inhibits osteoblastic differentiation of bone cells by ERK and NF-kappaB. Biochem Biophys Res Commun. 2004;314(1):197-207.
102. Mody N, Parhami F, Sarafian TA, Demer LL. Oxidative stress modulates osteoblastic differentiation of vascular and bone cells. Free Radic Biol Med. 2001;31(4):509-19.
103. Kawashima Y, Fritton JC, Yakar S, Epstein S, Schaffler MB, Jepsen KJ, LeRoith D. Type 2 diabetic mice demonstrate slender long bones with increased fragility secondary to increased osteoclastogenesis. Bone. 2009;44(4):648-55.
104. He H, Liu R, Desta T, Leone C, Gerstenfeld LC, Graves DT. Diabetes causes decreased osteoclastogenesis, reduced bone formation, and enhanced apoptosis of osteoblastic cells in bacteria stimulated bone loss. Endocrinology. 2004;145(1):447-52.
105. Liu R, Bal HS, Desta T, Krothapalli N, Alyassi M, Luan Q, Graves DT. Diabetes enhances periodontal bone loss through enhanced resorption and diminished bone formation. J Dent Res. 2006;85(6):510-4.
106. Anderson DM, Maraskovsky E, Billingsley WL, Dougall WC, Tometsko ME, Roux ER, Teepe MC, DuBose RF, Cosman D, Galibert L. A homologue of the TNF receptor and its ligand enhance T-cell growth and dendritic-cell function. Nature. 1997;390(6656):175-9.
107. Lacey DL, Timms E, Tan HL, Kelley MJ, Dunstan CR, Burgess T, Elliott R, Colombero A, Elliott G, Scully S, Hsu H, Sullivan J, Hawkins N, Davy E, Capparelli C, Eli A, Qian YX, Kaufman S, Sarosi I, Shalhoub V, Senaldi G, Guo J, Delaney J, Boyle WJ. Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell. 1998;93(2):165-76.
108. Bonde M, Fledelius C, Qvist P, Christiansen C. Coated-tube radioimmunoassay for C-telopeptides of type I collagen to assess bone resorption. Clin Chem. 1996;42(10):1639-44.
109. Uebelhart D, Schlemmer A, Johansen JS, Gineyts E, Christiansen C, Delmas PD. Effect of menopause and hormone replacement therapy on the urinary excretion of pyridinium cross-links. J Clin Endocrinol Metab. 1991;72(2):367-73.
110. Hanson DA, Weis MA, Bollen AM, Maslan SL, Singer FR, Eyre DR. A specific immunoassay for monitoring human bone resorption: quantitation of type I collagen cross-linked N-telopeptides in urine. J Bone Miner Res. 1992;7(11):1251-8.
111. Suzuki K, Kurose T, Takizawa M, Maruyama M, Ushikawa K, Kikuyama M, Sugimoto C, Seino Y, Nagamatsu S, Ishida H. Osteoclastic function is accelerated in male patients with type 2 diabetes mellitus: the preventive role of osteoclastogenesis inhibitory factor/osteoprotegerin (OCIF/OPG) on the decrease of bone mineral density. Diabetes Res Clin Pract. 2005;68(2):117-25.
112. Tornvig L, Mosekilde LI, Justesen J, Falk E, Kassem M. Troglitazone treatment increases bone marrow adipose tissue volume but does not affect trabecular bone volume in mice. Calcif Tissue Int. 2001;69(1):46-50.
113. Lazarenko OP, Rzonca SO, Suva LJ, Lecka-Czernik B. Netoglitazone is a PPAR-gamma ligand with selective effects on bone and fat. Bone. 2006;38(1):74-84.
114. Lecka-Czernik B, Moerman EJ, Grant DF, Lehmann JM, Manolagas SC, Jilka RL. Divergent effects of selective peroxisome proliferator-activated receptor-gamma 2 ligands on adipocyte versus osteoblast differentiation. Endocrinology. 2002;143(6):2376-84.
115. Meunier P, Aaron J, Edouard C, Vignon G. Osteoporosis and the replacement of cell populations of the marrow by adipose tissue. A quantitative study of 84 iliac bone biopsies. Clin Orthop. 1971;80:147-54.
116. Jilka RL, Weinstein RS, Takahashi K, Parfitt AM, Manolagas SC. Linkage of decreased bone mass with impaired osteoblastogenesis in a murine model of accelerated senescence. J Clin Invest. 1996;97(7):1732-40.
117. Kajkenova O, Lecka-Czernik B, Gubrij I, Hauser SP, Takahashi K, Parfitt AM, Jilka RL, Manolagas SC, Lipschitz DA. Increased adipogenesis and myelopoiesis in the bone marrow of SAMP6, a murine model of defective osteoblastogenesis and low turnover osteopenia. J Bone Miner Res. 1997;12(11):1772-9.
118. Verma S, Rajaratnam JH, Denton J, Hoyland JA, Byers RJ. Adipocytic proportion of bone marrow is inversely related to bone formation in osteoporosis. J Clin Pathol. 2002;55(9):693-8.
119. Gimble JM, Zvonic S, Floyd ZE, Kassem M, Nuttall ME. Playing with bone and fat. J Cell Biochem. 2006;98(2):251-66.
120. Di Iorgi N, Rosol M, Mittelman SD, Gilsanz V. Reciprocal relation between marrow adiposity and the amount of bone in the axial and appendicular skeleton of young adults. J Clin Endocrinol Metab. 2008;93(6):2281-6.
121. Akune T, Ohba S, Kamekura S, Yamaguchi M, Chung UI, Kubota N, Terauchi Y, Harada Y, Azuma Y, Nakamura K, Kadowaki T, Kawaguchi H. PPARgamma insufficiency enhances osteogenesis through osteoblast formation from bone marrow progenitors. J Clin Invest. 2004;113(6):846-55.
122. Cock TA, Back J, Elefteriou F, Karsenty G, Kastner P, Chan S, Auwerx J. Enhanced bone formation in lipodystrophic PPARgamma(hyp/hyp) mice relocates haematopoiesis to the spleen. EMBO Rep. 2004;5(10):1007-12.
123. Kawai M, Sousa KM, MacDougald OA, Rosen CJ. The many facets of PPARgamma: novel insights for the skeleton. Am J Physiol Endocrinol Metab. 2010 Jul;299(1):E3-9.
124. Barbagallo I, Vanella A, Peterson SJ, Kim DH, Tibullo D, Giallongo C, Vanella L, Parrinello N, Palumbo GA, Di Raimondo F, Abraham NG, Asprinio D. Overexpression of heme oxygenase-1 increases human osteoblast stem cell differentiation. J Bone Miner Metab. 2010 May;28(3):276-88.
125. Ferré P. The biology of peroxisome proliferator-activated receptors: relationship with lipid metabolism and insulin sensitivity. Diabetes. 2004;53 Suppl 1:S43-50.
126. 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.
127. Krings A, Rahman S, Huang S, Lu Y, Czernik PJ, Lecka-Czernik B. Bone marrow fat has brown adipose tissue characteristics, which are attenuated with aging and diabetes. Bone. 2011 Jun 24. [Epub ahead of print]
128. Hamrick MW, Della-Fera MA, Choi YH, Pennington C, Hartzell D, Baile CA. Leptin treatment induces loss of bone marrow adipocytes and increases bone formation in leptin-deficient ob/ob mice. J Bone Miner Res. 2005;20(6):994-1001.
129. Rosen CJ, Klibanski A. Bone, fat, and body composition: evolving concepts in the pathogenesis of osteoporosis. Am J Med. 2009;122(5):409-14.
130. Rosen CJ, Bouxsein ML. Mechanisms of disease: is osteoporosis the obesity of bone? Nat Clin Pract Rheumatol. 2006;2(1):35-43.
131. Reseland JE, Syversen U, Bakke I, Qvigstad G, Eide LG, Hjertner O, Gordeladze JO, Drevon CA. Leptin is expressed in and secreted from primary cultures of human osteoblasts and promotes bone mineralization. J Bone Miner Res. 2001;16(8):1426-33.
132. Cornish J, Callon KE, Bava U, Lin C, Naot D, Hill BL, Grey AB, Broom N, Myers DE, Nicholson GC, Reid IR. Leptin directly regulates bone cell function in vitro and reduces bone fragility in vivo. J Endocrinol. 2002;175(2):405-15.
133. Hamrick MW. Leptin, bone mass, and the thrifty phenotype. J Bone Miner Res. 2004;19(10):1607-11.
134. Hamrick MW, Della Fera MA, Choi YH, Hartzell D, Pennington C, Baile CA. Injections of leptin into rat ventromedial hypothalamus increase adipocyte apoptosis in peripheral fat and in bone marrow. Cell Tissue Res. 2007;327(1):133-41.
135. Ducy P, Amling M, Takeda S, Priemel M, Schilling AF, Beil FT, Shen J, Vinson C, Rueger JM, Karsenty G. Leptin inhibits bone formation through a hypothalamic relay: a central control of bone mass. Cell. 2000;100(2):197-207.
136. Karsenty G. Leptin controls bone formation through a hypothalamic relay. Recent Prog Horm Res. 2001;56:401-15.
137. Hamrick MW, Pennington C, Newton D, Xie D, Isales C. Leptin deficiency produces contrasting phenotypes in bones of the limb and spine. Bone. 2004;34(3):376-83.
138. Steppan CM, Crawford DT, Chidsey-Frink KL, Ke H, Swick AG. Leptin is a potent stimulator of bone growth in ob/ob mice. Regul Pept. 2000;92(1-3):73-8.
139. Hanaki K, Becker DJ, Arslanian SA. Leptin before and after insulin therapy in children with new-onset type 1 diabetes. J Clin Endocrinol Metab. 1999;84(5):1524-6.
140. Karaguzel G, Ozdem S, Boz A, Bircan I, Akcurin S. Leptin levels and body composition in children and adolescents with type 1 diabetes. Clin Biochem. 2006;39(8):788-93.
141. Luna R, Garcia-Mayor RV, Lage M, Andrade MA, Barreiro J, Pombo M, Dieguez C, Casanueva FF. High serum leptin levels in children with type 1 diabetes mellitus: contribution of age, BMI, pubertal development and metabolic status. Clin Endocrinol. 1999;51(5):603-10.
142. Lo HC, Lin SC, Wang YM. The relationship among serum cytokines, chemokine, nitric oxide, and leptin in children with type 1 diabetes mellitus. Clin Biochem. 2004;37(8):666-72.
143. Martin LM, McCabe LR. Type I diabetic bone phenotype is location but not gender dependent. Histochem Cell Biol. 2007;128(2):125-33.
144. Considine RV, Sinha MK, Heiman ML, Kriauciunas A, Stephens TW, Nyce MR, Ohannesian JP, Marco CC, McKee LJ, Bauer TL. Serum immunoreactive-leptin concentrations in normal-weight and obese humans. N Engl J Med. 1996;334(5):292-5.
145. Goulding A, Taylor RW. 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. 1998;63(6):456-8.
146. Thomas T, Gori F, Khosla S, Jensen MD, Burguera B, Riggs BL. Leptin acts on human marrow stromal cells to enhance differentiation to osteoblasts and to inhibit differentiation to adipocytes. Endocrinology. 1999;140(4):1630-8.
147. Vasilkova O, Mokhort T, Sharshakova T, Hayashida N, Takamura N. Leptin is an independent determinant of bone mineral density in men with type 2 diabetes mellitus. Acta Diabetol. 2011 Feb 16. [Epub ahead of print]
148. Bilgic S, Aktas E, Salman F, Ersahin G, Erten G, Yilmaz MT, Deniz G. Intracytoplasmic cytokine levels and neutrophil functions in early clinical stage of type 1 diabetes. Diabetes Res Clin Pract. 2008;79(1):31-6.
149. Kayal RA, Siqueira M, Alblowi J, McLean J, Krothapalli N, Faibish D, Einhorn TA, Gerstenfeld LC, Graves DT. TNF-alpha mediates diabetes-enhanced chondrocyte apoptosis during fracture healing and stimulates chondrocyte apoptosis through FOXO1. J Bone Miner Res. 2010;25(7):1604-15.
150. Alblowi J, Kayal RA, Siqueira M, McKenzie E, Krothapalli N, McLean J, Conn J, Nikolajczyk B, Einhorn TA Gerstenfeld L, Graves DT. High levels of tumor necrosis factor-alpha contribute to accelerated loss of cartilage in diabetic fracture healing. Am J Pathol. 2009;175(4):1574-85.
151. Salvi GE, Yalda B, Collins JG, Jones BH, Smith FW, Arnold RR, Offenbacher S. Inflammatory mediator response as a potential risk marker for periodontal diseases in insulin-dependent diabetes mellitus patients. J Periodontol. 1997;68(2):127-35.
152. Lalla E, Lamster IB, Feit M, Huang L, Spessot A, Qu W, Kislinger T, Lu Y, Stern DM, Schmidt AM. Blockade of RAGE suppresses periodontitis-associated bone loss in diabetic mice. J Clin Invest. 2000;105(8):1117-24.
153. El-seweidy MM, El-Swefy SE, Ameen RS, Hashem RM. Effect of age receptor blocker and/or anti-inflammatory coadministration in relation to glycation, oxidative stress and cytokine production in stz diabetic rats. Pharmacol Res. 2002 May;45(5):391-8.
154. Neumann A, Schinzel R, Palm D, Riederer P, Munch G. High molecular weight hyaluronic acid inhibits advanced glycation endproduct-induced NF-kappaB activation and cytokine expression. FEBS Lett. 1999;453(3):283-7.
155. Goova MT, Li J, Kislinger T, Qu W, Lu Y, Bucciarelli LG, Nowygrod S, Wolf BM, Caliste X, Yan SF, Stern DM, Schmidt AM. Blockade of receptor for advanced glycation end-products restores effective wound healing in diabetic mice. Am J Pathol. 2001;159(2):513-25.
156. Kurtis B, Develioglu H, Taner IL, Balos K, Tekin IO. IL-6 levels in gingival crevicular fluid (GCF) from patients with non-insulin dependent diabetes mellitus (NIDDM), adult periodontitis and healthy subjects. J Oral Sci. 1999 Dec;41(4):163-7.
157. Salvi GE, Collins JG, Yalda B, Arnold RR, Lang NP, Offenbacher S. Monocytic TNF alpha secretion patterns in IDDM patients with periodontal diseases. J Clin Periodontol. 1997 Jan;24(1):8-16.
158. McCabe LR. Understanding the pathology and mechanisms of type I diabetic bone loss. J Cell Biochem. 2007 Dec 15;102(6):1343-57.
159. Thomas DM, Maher F, Rogers SD, Best JD. Expression and regulation by insulin of GLUT 3 in UMR 106-01, a clonal rat osteosarcoma cell line. Biochem Biophys Res Commun. 1996 Jan 26;218(3):789-93.
160. Zayzafoon M, Stell C, Irwin R, McCabe LR. Extracellular glucose influences osteoblast differentiation and c-Jun expression. J Cell Biochem. 2000 Aug 2;79(2):301-10.
161. Botolin S, McCabe LR. Chronic hyperglycemia modulates osteoblast gene expression through osmotic and non-osmotic pathways. J Cell Biochem. 2006 Oct 1;99(2):411-24.
162. Zayzafoon M, Botolin S, McCabe LR. P38 and activating transcription factor-2 involvement in osteoblast osmotic response to elevated extracellular glucose. J Biol Chem. 2002 Oct 4;277(40):37212-8.
163. Wolff SP, Dean RT. Monosaccharide autoxidation: a potential source of oxidative stress in diabetes? Model reactions with nucleotides and protein. Bioelectrochem Bioenergetics. 1987;18(1-3):283-93.
164. Hunt JV, Smith CC, Wolff SP. Autoxidative glycosylation and possible involvement of peroxides and free-radicals in LDL modification by glucose. Diabetes. 1990;39(11):1420-4.
165. Zayzafoon M, Botolin S, McCabe LR. p38 and activating transcription factor-2 involvement in osteoblast osmotic response to elevated extracellular glucose. J Biol Chem. 2002 Oct 4;277(40):37212-8.
166. Zayzafoon M, Stell C, Irwin R, McCabe LR. Extracellular glucose influences osteoblast differentiation and c-jun expression. J Cell Biochem. 2000 Aug 2;79(2):301-10.
167. Brownlee M, Vlassara H, Cerami A. Nonenzymatic glycosylation and the pathogenesis of diabetic complications. Ann Int Med. 1984;101(4):527-37.
168. Katayama Y, Akatsu T, Yamamoto M, Kugai N, Nagata N. Role of nonenzymatic glycosylation of type I collagen in diabetic osteopenia. J Bone Miner Res. 1996 Jul;11(7):931-7.
169. Locatto ME, Abranzon H, Caferra D, Fernandez MD, Alloatti R, Puche RC. Growth and development of bone mass in untreated alloxan-diabetic rats-effects of collagen glycosylation and parathyroid activity on bone turnover. Bone Miner. 1993 Nov;23(2):129-44.
170. McCarthy AD, Etcheverry SB, Bruzzone L, Cortizo AM. Effects of advanced glycation end-products on the proliferation and differentiation of osteoblast-like cells. Mol Cell Biochem. 1997 May;170(1-2):43-51.
171. McCarthy AD, Etcheverry SB, Cortizo AM. Effect of advanced glycation endproducts on the secretion of insulin-like growth factor-I and its binding proteins: role in osteoblast development. Acta Diabetologica. 2001;38(3):113-22.
172. Wautier JL, Guillausseau PJ. Advanced glycation end products, their receptors and diabetic angiopathy. Diabetes Metab. 2001 Nov;27(5 Pt 1):535-42.
173. Dyer DG, Dunn JA, Thorpe SR, Bailie KE, Lyons TJ, McCance DR, Baynes JW. Accumulation of maillard reaction-products in skin collagen in diabetes and aging. J Clin Invest. 1993 Jun;91(6):2463-9.
174. McCance DR, Dryer DG, Dunn JA, Bailie KE, Thorpe SR, Baynes JW, Lyons TJ. Maillard reaction products and their relation to complications in insulin-dependent diabetes mellitus. J Clin Invest. 1993 Jun;91(6):2470-8.
175. Stitt AW. Advanced glycation: an important pathological event in diabetic and age related ocular disease. Brit J Ophthalmol. 2001 Jun;85(6):746-53.
176. Saito M, Marumo K, Fujii K, Ishioka N. Single-column high-performance liquid chromatographic fluorescence detection of immature, mature, and senescent cross-links of collagen. Anal Biochem. 1997 Nov 1;253(1):26-32.
177. Yamamoto M, Yamaguchi T, Yamauchi M, Yano S, Sugimoto T. Serum pentosidine levels are positively associated with the presence of vertebral fractures in postmenopausal women with type 2 diabetes. J Clin Endocrinol Metab. 2008 Mar;93(3):1013-9.
178. Schwartz AV, Garnero P, Hillier TA, Sellmeyer DE, Strotmeyer ES, Feingold KR, Resnick HE, Tylavsky FA, Black DM, Cummings SR, Harris TB, Bauer, DC; Health, Aging, and Body Composition Study. Pentosidine and increased fracture risk in older adults with type 2 diabetes. J Clin Endocrinol Metab. 2009 Jul;94(7):2380-6.
179. Sell DR, Nagaraj RH, Grandhee SK, Odetti P, Lapolla A, Fogarty J, Monnier VM. Pentosidine-a molecular marker for the cumulative damage to proteins in diabetes, aging, and uremia. Diabetes-Metabol Revs. 1991 Dec;7(4):239-51.
180. Dunn JA, Patrick JS, Thorpe SR, Baynes JW. Oxidation of glycated proteins: age-dependent accumulation of N epsilon-(carboxymethyl)lysine in lens proteins. Biochemistry. 1989 Nov 28;28(24):9464-8.
181. Lyons TJ, Bailie KE, Dyer DG, Dunn JA, Baynes JW. Decrease in skin collagen glycation with improved glycemic control in patients with insulin-dependent diabetes-mellitus. J Clin Invest. 1991 Jun;87(6):1910-5.
182. Forbes JM, Cooper ME, Oldfield MD, Thomas MC. Role of advanced glycation end products in diabetic nephropathy. J Am Soc Nephrol. 2003 Aug;14(8 Suppl 3):S254-8.
183. Lalla E, Lamster IB, Drury S, Fu C, Schmidt AM. Hyperglycemia, glycoxidation and receptor for advanced glycation endproducts: potential mechanisms underlying diabetic complications, including diabetes-associated periodontitis. Periodontology 2000. 2000 Jun;23:50-62.
184. Saito M, Marumo K. Collagen cross-links as a determinant of bone quality: a possible explanation for bone fragility in aging, osteoporosis, and diabetes mellitus. Osteoporosis Int. 2010 Feb;21(2):195-214.
185. Vashishth D. The role of the collagen matrix in skeletal fragility. Curr Osteoporos Rep. 2007 Jun;5(2):62-6.
186. Hernandez CJ, Tang SY, Baumbach BM, Hwu PB, Sakkee AN, van der Ham F, DeGroot J, Bank RA, Keaveny TM. Trabecular microfracture and the influence of pyridinium and non-enzymatic glycation-mediated collagen cross-links. Bone. 2005 Dec;37(6):825-32.
187. Saito M, Fujii K, Mori Y, Marumo K. Role of collagen enzymatic and glycation induced cross-links as a determinant of bone quality in spontaneously diabetic WBN/ Kob rats. Osteoporosis Int. 2006 Oct;17(10):1514-23.
188. Viguet-Carrin S, Roux JP, Arlot ME, Merabet Z, Leeming DJ, Byrjalsen I, Delmas PD, Bouxsein ML. Contribution of the advanced glycation end product pentosidine and of maturation of type I collagen to compressive biomechanical properties of human lumbar vertebrae. Bone. 2006 Nov;39(5):1073-9.
189. Saito M, Mori S, Mashiba T, Komatsubara S, Marumo K. Collagen maturity, glycation induced-pentosidine, and mineralization are increased following 3-year treatment with incadronate in dogs. Osteoporosis Int. 2008 Sep;19(9):1343-54.
190. Vashishth D. Collagen glycation and its role in fracture properties of bone. J Musculoskelet Neuronal Interact. 2005 Oct-Dec;5(4):316.
191. Saito M, Marumo K. Collagen cross-links as a determinant of bone quality: a possible explanation for bone fragility in aging, osteoporosis, and diabetes mellitus. Osteoporos Int. 2010 Feb;21(2):195-214.
192. Silva MJ, Brodt MD, Lynch MA, McKenzie JA, Tanouye KM, Nyman JS, Wang X. Type 1 diabetes in young rats leads to progressive trabecular bone loss, cessation of cortical bone growth, and diminished whole bone strength and fatigue. J Bone Miner Res. 2009 Sep;24(9):1618-27.
193. Tomasek JJ, Meyers SW, Basinger JB, Green DT, Shew RL. Diabetic and age-related enhancement of collagen-linked fluorescence in cortical bones of rats. Life Sci. 1994;55(11):855-61.
194. Saito M, Fujii K, Soshi S, Tanaka T. Reductions in degree of mineralization and enzymatic collagen cross-links and increases in glycation-induced pentosidine in the femoral neck cortex in cases of femoral neck fracture. Osteoporos Int. 2006;17(7):986-95.
195. Saito M, Fujii K, Marumo K. Degree of mineralization-related collagen crosslinking in the femoral neck cancellous bone in cases of hip fracture and controls. Calcif Tissue Int. 2006 Sep;79(3):160-8.
196. Odetti P, Rossi S, Monacelli F, Poggi A, Cirnigliaro M, Federici M, Federici A. Advanced glycation end products and bone loss during aging. Ann N Y Acad Sci. 2005 Jun;1043:710-7.
197. Schwartz AV, Garnero P, Hillier TA, Sellmeyer DE, Strotmeyer ES, Feingold KR, Resnick HE, Tylavsky FA, Black DM, Cummings SR, Harris TB, Bauer DC. Pentosidine and increased fracture risk in older adults with type 2 diabetes. J Clin Endocrinol Metab. 2009 Jul;94(7):2380-6.
198. Yamamoto M, Yamaguchi T, Yamauchi M, Yano S, Sugimoto T. Serum pentosidine levels are positively associated with the presence of vertebral fractures in postmenopausal women with type 2 diabetes. J Clin Endocrinol Metab. 2008 Mar;93(3):1013-9.
199. Kislinger T, Fu C, Huber B, Qu W, Taguchi A, Du Yan S, Hofmann M, Yan SF, Pischetsrieder M, Stern D, Schmidt AM. N ε-(carboxymethyl)lysine adducts of proteins are ligands for receptor for advanced glycation end products that activate cell signaling pathways and modulate gene expression. J Biol Chem. 1999 Oct 29;274(44):31740-9.
200. Lalla E, Lamster IB, Schmidt AM. Enhanced interaction of advanced glycation end products with their cellular receptor RAGE: implications for the pathogenesis of accelerated periodontal disease in diabetes. Ann Periodontol. 1998 Jul;3(1):13-9.
201. Kume S, Kato S, Yamagishi SI, Inagaki Y, Ueda S, Arima N, Okawa T, Kojiro M, Nagata K. Advanced glycation end-products attenuate human mesenchymal stem cells and prevent cognate differentiation into adipose tissue, cartilage, and bone. J Bone Miner Res. 2005 Sep;20(9):1647-58.
202. Miyata T, Notoya K, Yoshida K, Horie K, Maeda K, Kurokawa K, Taketomi S. Advanced glycation end products enhance osteoclast-induced bone resorption in cultured mouse unfractionated bone cells and in rats implanted subcutaneously with devitalized bone particles. J Am Soc Nephrol. 1997 Feb;8(2):260-70.
203. Zhou Z, Immel D, Xi CX, Bierhaus A, Feng X, Mei L, Nawroth P, Stern DM, Xiong WC. Regulation of osteoclast function and bone mass by RAGE. J Exp Med. 2006 Apr 17;203(4):1067-80.
204. Yamamoto M, Yamaguchi T, Yamauchi M, Sugimoto T. Low serum level of the endogenous secretory receptor for advanced glycation end products (esRAGE) is a risk factor for prevalent vertebral fractures independent of bone mineral density in patients with type 2 diabetes. Diabetes Care. 2009 Dec;32(12):2263-8.
205. Brett J, Schmidt AM, Yan SD, Zou YS, Weidman E, Pinsky D, Nowygrod R, Neeper M, Przysiecki C, Shaw A, Migheli A, Stern D. Survey of the distribution of a newly characterized receptor for advanced glycation end-products in tissues. Am J Pathol. 1993 Dec;143(6):1699-712.
206. Owen WF Jr, Hou FF, Stuart RO, Kay J, Boyce J, Chertow GM, Schimidt AM. Beta 2-microglobulin modified with advanced glycation end products modulates collagen synthesis by human fibroblasts. Kidney Int. 1998 May;53(5):1365-73.
207. Hough S, Avioli LV, Bergfeld MA, Fallon MD, Slatopolsky E, Teitelbaum SL. Correction of abnormal bone and mineral metabolism in chronic streptozotocin-induced diabetes mellitus in the rat by insulin therapy. Endocrinology. 1981 Jun;108(6):2228-34.
208. McCracken M, Lemons JE, Rahemtulla F, Prince CW, Feldman D. Bone response to titanium alloy implants placed in diabetic rats. Int J Oral Maxillofac Implants. 2000 May-Jun;15(3):345-54.
209. Thrailkill KM, Liu L, Wahl EC, Bunn RC, Perrien DS, Cockrell GE, Skinner RA, Hogue WR, Carver AA, Fowlkes JL, Aronson J, Lumpkin CK Jr. Bone formation is impaired in a model of type 1 diabetes. Diabetes. 2005 Oct;54(10):2875-81.
210. Gandhi A, Beam HA, O'Connor JP, Parsons JR, Lin SS. The effects of local insulin delivery on diabetic fracture healing. Bone. 2005 Oct;37(4):482-90.
211. Motyl KJ, McCabe LR, Schwartz AV. Bone and glucose metabolism: a two-way street. Arch Biochem Biophys. 2010 Nov 1;503(1):2-10.
212. Lee NK, Sowa H, Hinoi E, Ferron M, Ahn JD, Confavreux C, Dacquin R, Mee PJ, McKee MD, Jung DY, Zhang Z, Kim JK, Mauvais-Jarvis F, Ducy P, Karsenty G. Endocrine regulation of energy metabolism by the skeleton. Cell. 2007 Aug 10;130(3):456-69.
213. 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 U S A. 2008 Apr 1;105(13):5266-70.
214. Ferron M, Wei J, Yoshizawa T, Del Fattore A, DePinho RA, Teti A, Ducy P, Karsenty G. Insulin signaling in osteoblasts integrates bone remodeling and energy metabolism. Cell. 2010 Jul 23;142(2):296-308.
215. Fulzele K, Riddle RC, DiGirolamo DJ, Cao X, Wan C, Chen D, Faugere MC, Aja S, Hussain MA, Bruning JC, Clemens TL. Insulin receptor signaling in osteoblasts regulates postnatal bone acquisition and body composition. Cell. 2010 Jul 23;142(2):309-19.
216. Irwin R, Lin HV, Motyl KJ, McCabe LR. Normal bone density obtained in the absence of insulin receptor expression in bone. Endocrinology. 2006 Dec;147(12):5760-7.
217. Hickman J, McElduff A. Insulin sensitizes a cultured rat osteogenic sarcoma cell line to hormones which activate adenylate cyclase. Calcif Tissue Int. 1990 Jun;46(6):401-5.
218. Hill PA, Tumber A, Meikle MC. Multiple extracellular signals promote osteoblast survival and apoptosis. Endocrinology. 1997 Sep;138(9):3849-58.
219. Fulzele K, Riddle RC, DiGirolamo DJ, Cao X, Wan C, Chen D, Faugere MC, Aja S, Hussain MA, Bruning JC, Clemens TL. Insulin receptor signaling in osteoblasts regulates postnatal bone acquisition and body composition. Cell. 2010 Jul 23;142(2):309-19.
220. Ogata N, Chikazu D, Kubota N, Terauchi Y, Tobe K, Azuma Y, Ohta T, Kadowaki T, Nakamura K, Kawaguchi H. Insulin receptor substrate-1 in osteoblast is indispensable for maintaining bone turnover. J Clin Invest. 2000 Apr;105(7):935-43.
221. Shimoaka T, Kamekura S, Chikuda H, Hoshi K, Chung UI, Akune T, Maruyama Z, Komori T, Matsumoto M, Ogawa W, Terauchi Y, Kadowaki T, Nakamura K, Kawaguchi H. Impairment of bone healing by insulin receptor substrate-1 deficiency. J Biol Chem. 2004 Apr 9;279(15):15314-22.
222. Singh DK, Winocour P, Summerhayes B, Viljoen A, Sivakumar G, Farrington K. Low serum osteoprotegerin levels in normoalbuminuric type 1 diabetes mellitus. Acta Diabetol. 2010 Dec;47(Suppl 1):105-10.
223. Al-Qadreh A, Voskaki I, Kassiou C, Athanasopoulou H, Sarafidou E, Bartsocas CS. Treatment of osteopenia in children with insulin-dependent diabetes mellitus: the effect of 1 alpha-hydroxyvitamin D3. Eur J Pediatr. 1996 Jan;155(1):15-17.
224. Goodman WG, Hori MT. Diminished bone formation in experimental diabetes. Relationship to osteoid maturation and mineralization. Diabetes. 1984 Sep;33(9):825-31.
225. Bierschenk L, Alexander J, Wasserfall C, Haller M, Schatz D, Atkinson M. Vitamin D levels in subjects with and without type 1 diabetes residing in a solar rich environment. Diabetes Care. 2009 Nov;32(11):1977-9.
226. Svoren BM, Volkening LK, Wood JR, Laffel LM. Significant vitamin D deficiency in youth with type 1 diabetes mellitus. J Pediatr. 2009 Jan;154(1):132-4.
227. Bener A, Alsaied A, Al-Ali M, Hassan AS, Basha B, Al-Kubaisi A, Abraham A, Mian M, Guiter G, Tewfik I. Impact of lifestyle and dietary habits on hypovitaminosis D in type 1 diabetes mellitus and healthy children from Qatar, a sun-rich country. Ann Nutr Metab. 2008;53(3-4):215-22.
228. Janner M, Ballinari P, Mullis PE, Fluck CE. High prevalence of vitamin D deficiency in children and adolescents with type 1 diabetes. Swiss Med Wkly. 2010 Sep 3;140:w13091.
229. Baumgartl HJ, Standl E, Schmidt-Gayk H, Kolb HJ, Janka HU, Ziegler AG. Changes of vitamin D3 serum concentrations at the onset of immune-mediated type 1 (insulin-dependent) diabetes mellitus. Diabetes Res. 1991 Mar;16(3):145-8.
230. Elder GJ, Mackun K. 25-Hydroxyvitamin D deficiency and diabetes predict reduced BMD in patients with chronic kidney disease. J Bone Miner Res. 2006 Nov;21(11):1778-84.
231. Tsuchida T, Sato K, Miyakoshi N, Abe T, Kudo T, Tamura Y, Kasukawa Y, Suzuki K. Histomorphometric evaluation of the recovering effect of human parathyroid hormone (1-34) on bone structure and turnover in streptozotocin-induced diabetic rats. Calcif Tissue Int. 2000 Mar;66(3):229-33.
232. Lozano D, de Castro LF, Dapia S, Andrade-Zapata I, Manzarbeitia F, Alvarez-Arroyo MV, Gomez-Barrena E, Esbrit P. Role of parathyroid hormone-related protein in the decreased osteoblast function in diabetes-related osteopenia. Endocrinology. 2009 May;150(5):2027-35.
233. Motyl KJ, McCauley LK, McCabe LR. Amelioration of type I diabetes-induced osteoporosis by parathyroid hormone is associated with improved osteoblast survival. J Cell Physiol. 2011 May 20. doi: 10.1002/jcp.22844. [Epub ahead of print]
234. Baynes KC, Boucher BJ, Feskens EJ, Kromhout D. Vitamin D, glucose tolerance and insulinaemia in elderly men. Diabetologia. 1997 Mar;40(3):344-7.
235. Okazaki R, Totsuka Y, Hamano K, Ajima M, Miura M, Hirota Y, Hata K, Fukumoto S, Matsumoto T. Metabolic improvement of poorly controlled noninsulin-dependent diabetes mellitus decreases bone turnover. J Clin Endocrinol Metab. 1997 Sep;82(9):2915-20.
236. Nuttall ME, Patton AJ, Olivera DL, Nadeau DP, Gowen M. Human trabecular bone cells are able to express both osteoblastic and adipocytic phenotype: implications for osteopenic disorders. J Bone Miner Res. 1998 Mar;13(3):371-82.
237. Gordeladze JO, Drevon CA, Syversen U, Reseland JE. Leptin stimulates human osteoblastic cell proliferation, de novo collagen synthesis, and mineralization: impact on differentiation markers, apoptosis, and osteoclastic signaling. J Cell Biochem. 2002;85(4):825-36.
238. Suzuki K, Miyakoshi N, Tsuchida T, Kasukawa Y, Sato K, Itoi E. Effects of combined treatment of insulin and human parathyroid hormone(1-34) on cancellous bone mass and structure in streptozotocin-induced diabetic rats. Bone. 2003 Jul;33(1):108-14.
239. Noda M, Yoon K, Rodan GA. Cyclic AMP-mediated stabilization of osteocalcin mRNA in rat osteoblast-like cells treated with parathyroid hormone. J Biol Chem. 1988 Dec 5;263(34):18574-7.
240. Scott DK, Brakenhoff KD, Clohisy JC, Quinn CO, Partridge NC. Parathyroid hormone induces transcription of collagenase in rat osteoblastic cells by a mechanism using cyclic adenosine 3',5'-monophosphate and requiring protein synthesis. Mol Endocrinol. 1992 Dec;6(12):2153-9.
241. Schmid C, Schlapfer I, Peter M, Boni-Schnetzler M, Schwander J, Zapf J, Froesch ER. Growth hormone and parathyroid hormone stimulate IGFBP-3 in rat osteoblasts. Am J Physiol. 1994 Aug;267(2 Pt 1):E226-33.
242. Porte D, Tuckermann J, Becker M, Baumann B, Teurich S, Higgins T, Owen MJ, Schorpp-Kistner M, Angel P. Both AP-1 and Cbfa1-like factors are required for the induction of interstitial collagenase by parathyroid hormone. Oncogene. 1999 Jan 21;18(3):667-78.
243. McSheehy PM, Chambers TJ. Osteoblastic cells mediate osteoclastic responsiveness to parathyroid hormone. Endocrinology. 1986 Feb;118(2):824-8.