The diabetic bone: A cellular and molecular perspective

International Journal of Lower Extremity Wounds

Volumn 10, Issue 1, 2011, Pages 16-32

  Blakytny, Robert ^a   Spraul, Maximilian ^b   Jude, Edward B ^c  

^a UNIVERSITY OF ULM   (Germany)

^b Mathias Infirmary and Jakobi Hospital   (Germany)

^c TAMESIDE GENERAL HOSPITAL   (United Kingdom)

Author keywords

bone; Charcot foot; diabetes; fracture; glycation; insulin

Indexed keywords

ADVANCED GLYCATION END PRODUCT; ALKALINE PHOSPHATASE; AMYLIN; BASIC FIBROBLAST GROWTH FACTOR; CALCIUM; COLLAGEN; COLLAGENASE 3; COPPER; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLUCOSE; GLUCOSE TRANSPORTER 4; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INSULIN; INTERLEUKIN 1; INTERLEUKIN 6; MAGNESIUM; MATRIX PROTEIN; NITRIC OXIDE; OSTEOCALCIN; PARATHYROID HORMONE; PROTEOGLYCAN; RECOMBINANT TRANSFORMING GROWTH FACTOR BETA1; SOMATOMEDIN BINDING PROTEIN 1; SOMATOMEDIN BINDING PROTEIN 3; SOMATOMEDIN C; STRONTIUM; TUMOR NECROSIS FACTOR ALPHA; UNINDEXED DRUG; VASCULOTROPIN; VITAMIN D;

APOPTOSIS; BODY MASS; BONE CELL; BONE DENSITY; BONE DISEASE; BONE MINERAL; BONE MINERALIZATION; CARTILAGE CELL; CELL ACTIVITY; CELL DIFFERENTIATION; CELL PROLIFERATION; DIABETIC BONE; FRACTURE; FRACTURE HEALING; FRACTURE NONUNION; GLUCOSE BLOOD LEVEL; GLUCOSE METABOLISM; GLUCOSE TRANSPORT; GLYCATION; HUMAN; INSULIN BLOOD LEVEL; INSULIN DEPENDENT DIABETES MELLITUS; MESENCHYMAL STEM CELL; MINERALIZATION; NEUROPATHIC JOINT DISEASE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; OSTEOBLAST; OSTEOCLAST; OSTEOLYSIS; OSTEOPENIA; OSTEOPOROSIS; OXIDATION; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; REVIEW; RISK; THROMBOCYTE RICH PLASMA; BONE; CYTOLOGY; DIABETES MELLITUS; PATHOLOGY;

BLOOD GLUCOSE; BONE AND BONES; DIABETES COMPLICATIONS; DIABETES MELLITUS, TYPE 1; DIABETES MELLITUS, TYPE 2; FRACTURES, BONE; GLYCOSYLATION END PRODUCTS, ADVANCED; HUMANS; INSULIN-LIKE GROWTH FACTOR I; OSTEOPOROSIS; OXIDATIVE STRESS;

EID: 79953300952     PISSN: 15347346     EISSN: 15526941     Source Type: Journal    
DOI: 10.1177/1534734611400256     Document Type: Review

References (242)

1. Gale EA The rise of childhood type 1 diabetes in the 20th century. Diabetes. 2002 ; 51: 3353-3361. (Pubitemid 35403436)
2. Wild S., Roglic G., Green A., Sicree R., King H. Global prevalence of diabetes: estimates for the year 2000 and projections for 2030. Diabetes Care. 2004 ; 27: 1047-1053. (Pubitemid 38579764)
3. Marcovecchio M., Mohn A., Chiarelli F. Type 2 diabetes mellitus in children and adolescents. J Endocrinol Invest. 2005 ; 28: 853-863. (Pubitemid 43162846)
4. Loder RT The influence of diabetes mellitus on the healing of closed fractures. Clin Orthop Relat Res. 1988 ; 232 ; 210-216.
5. Beam HA, Parsons JR, Lin SS The effects of blood glucose control upon fracture healing in the BB Wistar rat with diabetes mellitus. J Orthop Res. 2002 ; 20 ; 1210-1216. (Pubitemid 35363979)
6. Gandhi A., Doumas C., O'Connor JP, Parsons JR, Lin SS The effects of local platelet rich plasma delivery on diabetic fracture healing. Bone. 2006 ; 38: 540-546.
7. Kayal RA, Alblowi J., McKenzie E., et al. Diabetes causes the accelerated loss of cartilage during fracture repair which is reversed by insulin treatment. Bone. 2009 ; 44: 357-363.
8. Blotter RH, Connolly E., Wasan A., Chapman MW Acute complications in the operative treatment of isolated ankle fractures in patients with diabetes mellitus. Foot Ankle Int. 1999 ; 20: 687-694.
9. Ganesh SP, Pietrobon R., Cecilio WA, Pan D., Lightdale N., Nunley JA The impact of diabetes on patient outcomes after ankle fracture. J Bone Joint Surg Am. 2005 ; 87: 1712-1718. (Pubitemid 41061188)
10. Hartemann-Heurtier A., Van GH, Grimaldi A. The Charcot foot. Lancet. 2002 ; 360: 1776-1779. (Pubitemid 35476845)
11. Tan AL, Greenstein A., Jarrett SJ, McGonagle D. Acute neuropathic joint disease: a medical emergency ? Diabetes Care. 2005 ; 28: 2962-2964. (Pubitemid 43942932)
12. Verhaeghe J., Suiker AM, Einhorn TA, et al. Brittle bones in spontaneously diabetic female rats cannot be predicted by bone mineral measurements: studies in diabetic and ovariectomized rats. J Bone Miner Res. 1994 ; 9: 1657-1667. (Pubitemid 24300118)
13. Reddy GK, Stehno-Bittel L., Hamade S., Enwemeka CS The biomechanical integrity of bone in experimental diabetes. Diabetes Res Clin Pract. 2001 ; 54: 1-8. (Pubitemid 32782639)
14. Galluzzi F., Stagi S., Salti R., et al. Osteoprotegerin serum levels in children with type 1 diabetes: a potential modulating role in bone status. Eur J Endocrinol. 2005 ; 153: 879-885. (Pubitemid 43020239)
15. Botolin S., McCabe LR Bone loss and increased bone adiposity in spontaneous and pharmacologically induced diabetic mice. Endocrinology. 2007 ; 148: 198-205. (Pubitemid 46021451)
16. Khazai NB, Beck GR Jr, Umpierrez GE Diabetes and fractures: an overshadowed association. Curr Opin Endocrinol Diabetes Obes. 2009 ; 16: 435-445.
17. 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: 487-495. (Pubitemid 43343280)
18. 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: 495-505. (Pubitemid 47283633)
19. Liu Z., Aronson J., Wahl EC, et al. A novel rat model for the study of deficits in bone formation in type-2 diabetes. Acta Orthop. 2007 ; 78: 46-55. (Pubitemid 46570257)
20. 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: 372-379.
21. Baldock PA, Allison S., McDonald MM, et al. Hypothalamic regulation of cortical bone mass: opposing activity of Y2 receptor and leptin pathways. J Bone Miner Res. 2006 ; 21: 1600-1607. (Pubitemid 44484605)
22. Reinwald S., Peterson RG, Allen MR, Burr DB Skeletal changes associated with the onset of type 2 diabetes in the ZDF and ZDSD rodent models. Am J Physiol Endocrinol Metab. 2009 ; 296: E765 - E774.
23. Manolagas SC Birth and death of bone cells: basic regulatory mechanisms and implications for the pathogenesis and treatment of osteoporosis. Endocr Rev. 2000 ; 21: 115-137. (Pubitemid 32275592)
24. Noble BS, Reeve J. Osteocyte function, osteocyte death and bone fracture resistance. Mol Cell Endocrinol. 2000 ; 159: 7-13. (Pubitemid 30067635)
25. Rochefort GY, Pallu S., Benhamou CL Osteocyte: the unrecognized side of bone tissue. 2010 ; 21: 1457-1469.
26. Mohan S., Baylink DJ Bone growth factors. Clin Orthop Relat Res. 1991 ; 263: 30-48.
27. Karsdal MA, Martin TJ, Bollerslev J., Christiansen C., Henriksen K. Are nonresorbing osteoclasts sources of bone anabolic activity ? J Bone Miner Res. 2007 ; 22: 487-494. (Pubitemid 47457424)
28. Gerstenfeld LC, Cullinane DM, Barnes GL, Graves DT, Einhorn TA Fracture healing as a post-natal developmental process: molecular, spatial, and temporal aspects of its regulation. J Cell Biochem. 2003 ; 88: 873-884. (Pubitemid 36337032)
29. Tsiridis E., Upadhyay N., Giannoudis P. Molecular aspects of fracture healing: which are the important molecules ? Injury. 2007 ; 38 (suppl 1). S11 - S25.
30. Mathiassen B., Nielsen S., Johansen JS, et al. Long-term bone loss in insulin-dependent diabetic patients with microvascular complications. J Diabet Complications. 1990 ; 4: 145-149.
31. 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: 147-153. (Pubitemid 27395402)
32. Herrero S., Calvo OM, Garcia-Moreno C., et al. Low bone density with normal bone turnover in ovariectomized and streptozotocin-induced diabetic rats. Calcif Tissue Int. 1998 ; 62: 260-265. (Pubitemid 28127940)
33. Lopez-Ibarra PJ, Pastor MM, Escobar-Jimenez F., et al. Bone mineral density at time of clinical diagnosis of adult-onset type 1 diabetes mellitus. Endocr Pract. 2001 ; 7: 346-351. (Pubitemid 32904291)
34. 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 ; 33: 108-114. (Pubitemid 36952692)
35. Dixit PK, Stern AM Effect of insulin on the incorporation of citrate and calcium into the bones of alloxan-diabetic rats. Calcif Tissue Int. 1979 ; 27: 227-232. (Pubitemid 10220011)
36. Weiss RE, Gorn AH, Nimni ME Abnormalities in the biosynthesis of cartilage and bone proteoglycans in experimental diabetes. Diabetes. 1981 ; 30: 670-677. (Pubitemid 11017733)
37. 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: 3622-3631. (Pubitemid 41058134)
38. Spanheimer RG, Umpierrez GE, Stumpf V. Decreased collagen production in diabetic rats. Diabetes. 1988 ; 37: 371-376. (Pubitemid 18096371)
39. Zhang X., Fei Y., Zhang M., et al. Reversal of osteoporotic changes of mineral composition in femurs of diabetic rats by insulin. Biol Trace Elem Res. 2008 ; 121: 233-242.
40. Hie M., Yamazaki M., Tsukamoto I. Curcumin suppresses increased bone resorption by inhibiting osteoclastogenesis in rats with streptozotocin-induced diabetes. Eur J Pharmacol. 2009 ; 621: 1-9.
41. 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: 231-240. (Pubitemid 11136127)
42. Einhorn TA, Boskey AL, Gundberg CM, Vigorita VJ, Devlin VJ, Beyer MM The mineral and properties of bone in chronic experimental diabetes. J Orthop Res. 1988 ; 6: 317-323.
43. Bouillon R., Bex M., Van Herck E., et al. Influence of age, sex, and insulin on osteoblast function: osteoblast dysfunction in diabetes mellitus. J Clin Endocrinol Metab. 1995 ; 80: 1194-1202.
44. Axelsson I., Lorentzon R., Pita JC Biosynthesis of rat growth plate proteoglycans in diabetes and malnutrition. Calcif Tissue Int. 1983 ; 35: 237-342.
45. 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: 129-144.
46. 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: 855-861. (Pubitemid 24261618)
47. 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 ; 11: 931-937. (Pubitemid 26200043)
48. Oikawa A., Siragusa M., Quaini F., et al. Diabetes mellitus induces bone marrow microangiopathy. Arterioscler Thromb Vasc Biol. ; 30: 498-508.
49. 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: 485-492.
50. Hamada Y., Fujii H., Kitazawa R., Yodoi J., Kitazawa S., Fukagawa M. Thioredoxin-1 overexpression in transgenic mice attenuates streptozotocin- induced diabetic osteopenia: a novel role of oxidative stress and therapeutic implications. Bone. 2009 ; 44: 936-941.
51. Sasaki T., Kaneko H., Ramamurthy NS, Golub LM Tetracycline administration restores osteoblast structure and function during experimental diabetes. Anat Rec. 1991 ; 231: 25-34.
52. Weiss RE, Reddi AH Influence of experimental diabetes and insulin on matrix-induced cartilage and bone differentiation. Am J Physiol. 1980 ; 238: E200 - E207.
53. Maor G., Karnieli E. The insulin-sensitive glucose transporter (GLUT4) is involved in early bone growth in control and diabetic mice, but is regulated through the insulin-like growth factor I receptor. Endocrinology. 1999 ; 140: 1841-1851. (Pubitemid 29149257)
54. Nixon AJ, Lillich JT, Burton-Wurster N., Lust G., Mohammed HO Differentiated cellular function in fetal chondrocytes cultured with insulin-like growth factor-I and transforming growth factor-beta. J Orthop Res. 1998 ; 16: 531-541. (Pubitemid 28512431)
55. Pittenger MF, Mackay AM, Beck SC, et al. Multilineage potential of adult human mesenchymal stem cells. Science. 1999 ; 284: 143-147. (Pubitemid 29282067)
56. Stolzing A., Sellers D., Llewelyn O., Scutt A. Diabetes induced changes in rat mesenchymal stem cells. Cells Tissues Organs. 2010 ; 191: 453-465.
57. 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: 121-124. (Pubitemid 29350648)
58. Verhaeghe J., Suiker AM, Nyomba BL, et al. Bone mineral homeostasis in spontaneously diabetic BB rats. II. Impaired bone turnover and decreased osteocalcin synthesis. Endocrinology. 1989 ; 124: 573-582. (Pubitemid 19057040)
59. 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: 427-436. (Pubitemid 20222175)
60. 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: 249-256. (Pubitemid 30458818)
61. Horcajada-Molteni MN, Chanteranne B., Lebecque P., et al. Amylin and bone metabolism in streptozotocin-induced diabetic rats. J Bone Miner Res. 2001 ; 16: 958-965. (Pubitemid 32332307)
62. 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 ; 13: 371-382. (Pubitemid 28146219)
63. Lecka-Czernik B., Gubrij I., Moerman EJ, et al. Inhibition of Osf2/Cbfa1 expression and terminal osteoblast differentiation by PPARgamma2. J Cell Biochem. 1999 ; 74: 357-371. (Pubitemid 29344887)
64. Ostenson CG, Fiere V., Ahmed M., et al. Decreased cortical bone thickness in spontaneously non-insulin-dependent diabetic GK rats. J Diabetes Complications. 1997 ; 11: 319-322.
65. Ahmad T., Ohlsson C., Saaf M., Ostenson CG, Kreicbergs A. Skeletal changes in type-2 diabetic Goto-Kakizaki rats. J Endocrinology. 2003 ; 178: 111-116. (Pubitemid 36927015)
66. 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: 427-444. (Pubitemid 46354916)
67. Tamasi JA, Arey BJ, Bertolini DR, Feyen JH Characterization of bone structure in leptin receptor-deficient Zucker (fa/ fa) rats. J Bone Miner Res. 2003 ; 18: 1605-1611. (Pubitemid 37022918)
68. Isaia GC, Ardissone P., Di Stefano M., et al. Bone metabolism in type 2 diabetes mellitus. Acta Diabetol. 1999 ; 36: 35-38.
69. Suzuki K., Kurose T., Takizawa M., et al. 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: 117-125. (Pubitemid 40602618)
70. Vestergaard P. Bone metabolism in type 2 diabetes and role of thiazolidinediones. Curr Opin Endocrinol Diabetes Obes. 2009 ; 16: 125-131.
71. Hamann C., Gottsch C., Mettelsiefen J., et al. Bone regeneration in rats with type 2 diabetes mellitus. Osteologie. 2010 ; 19 (suppl 1). S27 - S28.
72. Follak N., Kloting I., Merk H. Influence of diabetic metabolic state on fracture healing in spontaneously diabetic rats. Diabetes Metab Res Rev. 2005 ; 21: 288-296. (Pubitemid 40716162)
73. Tyndall WA, Beam HA, Zarro C., O'Connor JP, Lin SS Decreased platelet derived growth factor expression during fracture healing in diabetic animals. Clin Orthop Relat Res. 2003 ; 408 ; 319-330. (Pubitemid 36307525)
74. Ogasawara A., Nakajima A., Nakajima F., Goto K., Yamazaki M. Molecular basis for affected cartilage formation and bone union in fracture healing of the streptozotocin-induced diabetic rat. Bone. 2008 ; 43: 832-839.
75. Macey LR, Kana SM, Jingushi S., Terek RM, Borretos J., Bolander ME Defects of early fracture-healing in experimental diabetes. J Bone Joint Surg Am. 1989 ; 71: 722-733. (Pubitemid 19179662)
76. Topping RE, Bolander ME, Balian G. Type X collagen in fracture callus and the effects of experimental diabetes. Clin Orthop Relat Res. 1994 ; 308 ; 220-228. (Pubitemid 24349332)
77. Kayal RA, Siqueira M., Alblowi J., et al. TNF-alpha mediates diabetes enhanced chondrocyte apoptosis during fracture healing and stimulates chondrocyte apoptosis through FOXO-1. J Bone Miner Res. 2010 ; 25: 1604-1615.
78. Knauper V., Lopez-Otin C., Smith B., Knight G., Murphy G. Biochemical characterization of human collagenase-3. J Biol Chem. 1996 ; 271: 1544-1550. (Pubitemid 26028643)
79. Kayal RA, Tsatsas D., Bauer MA, et al. 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: 560-568. (Pubitemid 47457433)
80. Kasahara T., Imai S., Kojima H., et al. Malfunction of bone marrow-derived osteoclasts and the delay of bone fracture healing in diabetic mice. Bone. 2010 ; 47: 617-625.
81. Kawaguchi H., Kurokawa T., Hanada K., et al. Stimulation of fracture repair by recombinant human basic fibroblast growth factor in normal and streptozotocin-diabetic rats. Endocrinology. 1994 ; 135: 774-781. (Pubitemid 24241262)
82. Al-Zube L., Breitbart EA, O'Connor JP, et al. Recombinant human platelet-derived growth factor BB (rhPDGF-BB) and beta-tricalcium phosphate/collagen matrix enhance fracture healing in a diabetic rat model. J Orthop Res. 2009 ; 27: 1074-1081.
83. Armstrong DG, Todd WF, Lavery LA, Harkless LB, Bushman TR The natural history of acute Charcot's arthropathy in a diabetic foot specialty clinic. Diabet Med. 1997 ; 14: 357-363. (Pubitemid 27248015)
84. Jeffcoate W., Lima J., Nobrega L. The Charcot foot. Diabet Med. 2000 ; 17: 253-258. (Pubitemid 30266118)
85. Edelson GW, Jensen JL, Kaczynski R. Identifying acute Charcot arthropathy through urinary cross-linked N-telopeptides. Diabetes. 1996 ; 45 (suppl 2). 108A.
86. Gough A., Abraha H., Li F., et al. Measurement of markers of osteoclast and osteoblast activity in patients with acute and chronic diabetic Charcot neuroarthropathy. Diabet Med. 1997 ; 14: 527-531. (Pubitemid 27298811)
87. Baumhauer JF, O'Keefe RJ, Schon LC, Pinzur MS Cytokine-induced osteoclastic bone resorption in charcot arthropathy: an immunohistochemical study. Foot Ankle Int. 2006 ; 27: 797-800. (Pubitemid 44497847)
88. Christensen TM, Bulow J., Simonsen L., Holstein PE, Svendsen OL Bone mineral density in diabetes mellitus patients with and without a Charcot foot. Clin Physiol Funct Imaging. 2010 ; 30: 130-134.
89. Jeffcoate W. The causes of the Charcot syndrome. Clin Podiatr Med Surg. 2008 ; 25: 29-42. (Pubitemid 350299818)
90. La Fontaine J., Harkless LB, Sylvia VL, Carnes D., Heim-Hall J., Jude E. Levels of endothelial nitric oxide synthase and calcitonin gene-related peptide in the Charcot foot: a pilot study. J Foot Ankle Surg. 2008 ; 47: 424-429.
91. Lowik CW, Nibbering PH, van de Ruit M., Papapoulos SE Inducible production of nitric oxide in osteoblast-like cells and in fetal mouse bone explants is associated with suppression of osteoclastic bone resorption. J Clin Invest. 1994 ; 93: 1465-1472. (Pubitemid 24116382)
92. Kasten TP, Collin-Osdoby P., Patel N., et al. Potentiation of osteoclast bone-resorption activity by inhibition of nitric oxide synthase. Proc Natl Acad Sci U S A. 1994 ; 91: 3569-3573. (Pubitemid 24139471)
93. van't Hof RJ, Ralston SH Cytokine-induced nitric oxide inhibits bone resorption by inducing apoptosis of osteoclast progenitors and suppressing osteoclast activity. J Bone Miner Res. 1997 ; 12: 1797-1804. (Pubitemid 27500191)
94. Molines L., Darmon P., Raccah D. Charcot's foot: newest findings on its pathophysiology, diagnosis and treatment. Diabetes Metab. 2010 ; 36: 251-255.
95. Dickinson PJ, Carrington AL, Frost GS, Boulton AJ Neurovascular disease, antioxidants and glycation in diabetes. Diabetes Metab Res Rev. 2002 ; 18: 260-272.
96. Ahmed N. Advanced glycation endproducts-role in pathology of diabetic complications. Diabetes Res Clin Pract. 2005 ; 67: 3-21. (Pubitemid 40037725)
97. Terada M., Inaba M., Yano Y., et al. Growth-inhibitory effect of a high glucose concentration on osteoblast-like cells. Bone. 1998 ; 22: 17-23. (Pubitemid 28033648)
98. Balint E., Szabo P., Marshall CF, Sprague SM Glucose-induced inhibition of in vitro bone mineralization. Bone. 2001 ; 28: 21-28. (Pubitemid 32114089)
99. Botolin S., McCabe LR Chronic hyperglycemia modulates osteoblast gene expression through osmotic and non-osmotic pathways. J Cell Biochem. 2006 ; 99: 411-424. (Pubitemid 44435559)
100. Vanella L., Kim DH, Asprinio D., et al. HO-1 expression increases mesenchymal stem cell-derived osteoblasts but decreases adipocyte lineage. Bone. 2010 ; 46: 236-243.
101. Chen ZX, Chang M., Peng YL, et al. Osteogenic growth peptide C-terminal pentapeptide [OGP(10-14)] acts on rat bone marrow mesenchymal stem cells to promote differentiation to osteoblasts and to inhibit differentiation to adipocytes. Regul Pep. 2007 ; 142: 16-23. (Pubitemid 46755903)
102. Kim JH, Kim YY, Kim SJ High glucose inhibits gene expression of tyrosyl-tRNA synthetase in osteoblast cells. Methods Find Exp Clin Pharmacol. 2009 ; 31: 639-644.
103. Inaba M., Terada M., Koyama H., et al. Influence of high glucose on 1,25-dihydroxyvitamin D3-induced effect on human osteoblast-like MG-63 cells. J Bone Miner Res. 1995 ; 10: 1050-1056.
104. Yoshida O., Inaba M., Terada M., et al. Impaired response of human osteosarcoma (MG-63) cells to human parathyroid hormone induced by sustained exposure to high glucose. Miner Electrolyte Metab. 1995 ; 21: 201-204.
105. Li M., Kim DH, Tsenovoy PL, et al. Treatment of obese diabetic mice with a heme oxygenase inducer reduces visceral and subcutaneous adiposity, increases adiponectin levels, and improves insulin sensitivity and glucose tolerance. Diabetes. 2008 ; 57: 1526-1535.
106. Guan CC, Yan M., Jiang XQ, et al. Sonic hedgehog alleviates the inhibitory effects of high glucose on the osteoblastic differentiation of bone marrow stromal cells. Bone. 2009 ; 45: 1146-1152.
107. Wittrant Y., Gorin Y., Woodruff K., et al. High D(+)glucose concentration inhibits RANKL-induced osteoclastogenesis. Bone. 2008 ; 42: 1122-1130.
108. Kim JM, Jeong D., Kang HK, Jung SY, Kang SS, Min BM Osteoclast precursors display dynamic metabolic shifts toward accelerated glucose metabolism at an early stage of RANKL-stimulated osteoclast differentiation. Cell Physiol Biochem. 2007 ; 20: 935-946.
109. Lien YH, Stern R., Fu JC, Siegel RC Inhibition of collagen fibril formation in vitro and subsequent cross-linking by glucose. Science. 1984 ; 225: 1489-1491. (Pubitemid 14033136)
110. 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 ; 21: 195-214.
111. Vashishth D., Gibson GJ, Khoury JI, Schaffler MB, Kimura J., Fyhrie DP Influence of nonenzymatic glycation on biomechanical properties of cortical bone. Bone. 2001 ; 28: 195-201. (Pubitemid 32140975)
112. Hernandez CJ, Tang SY, Baumbach BM, et al. Trabecular microfracture and the influence of pyridinium and nonenzymatic glycation-mediated collagen cross-links. Bone. 2005 ; 37: 825-832. (Pubitemid 41773493)
113. Garnero P., Borel O., Gineyts E., et al. Extracellular post-translational modifications of collagen are major determinants of biomechanical properties of fetal bovine cortical bone. Bone. 2006 ; 38: 300-309. (Pubitemid 43255423)
114. Tang SY, Vashishth D. Non-enzymatic glycation alters micro-damage formation in human cancellous bone. Bone. 2010 ; 46: 148-154.
115. Paul RG, Bailey AJ The effect of advanced glycation end-product formation upon cell-matrix interactions. Int J Biochem Cell Biol. 1999 ; 31: 653-660. (Pubitemid 29248874)
116. McCarthy AD, Etcheverry SB, Bruzzone L., Lettieri G., Barrio DA, Cortizo AM Non-enzymatic glycosylation of a type I collagen matrix: effects on osteoblastic development and oxidative stress. BMC Cell Biol. 2001 ; 2: 16.
117. 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 Diabetol. 2001 ; 38: 113-122. (Pubitemid 34042074)
118. Yamamoto T., Ozono K., Miyauchi A., et al. Role of advanced glycation end products in adynamic bone disease in patients with diabetic nephropathy. Am J Kidney Dis. 2001 ; 38 (4suppl1): S161 - S164.
119. Sanguineti R., Storace D., Monacelli F., Federici A., Odetti P. Pentosidine effects on human osteoblasts in vitro. Ann N Y Acad Sci. 2008 ; 1126: 166-172. (Pubitemid 351589306)
120. Alikhani M., Alikhani Z., Boyd C., et al. Advanced glycation end products stimulate osteoblast apoptosis via the MAP kinase and cytosolic apoptotic pathways. Bone. 2007 ; 40: 345-353. (Pubitemid 46054556)
121. Gangoiti MV, Cortizo AM, Arnol V., Felice JI, McCarthy AD Opposing effects of bisphosphonates and advanced glycation end-products on osteoblastic cells. Eur J Pharmacol. 2008 ; 600: 140-147.
122. Wang X., Shen X., Li X., Agrawal CM Age-related changes in the collagen network and toughness of bone. Bone. 2002 ; 31: 1-7. (Pubitemid 34754417)
123. Franke S., Siggelkow H., Wolf G., Hein G. Advanced glycation endproducts influence the mRNA expression of RAGE, RANKL and various osteoblastic genes in human osteoblasts. Arch Physiol Biochem. 2007 ; 113: 154-161. (Pubitemid 47547388)
124. Takagi M., Kasayama S., Yamamoto T., et al. Advanced glycation endproducts stimulate interleukin-6 production by human bone-derived cells. J Bone Miner Res. 1997 ; 12: 439-446. (Pubitemid 27120481)
125. Schurman L., McCarthy AD, Sedlinsky C., et al. Metformin reverts deleterious effects of advanced glycation end-products (AGEs) on osteoblastic cells. Exp Clin Endocrinol Diabetes. 2008 ; 116: 333-340. (Pubitemid 351947863)
126. DeGroot J., Verzijl N., Jacobs KM, et al. Accumulation of advanced glycation endproducts reduces chondrocyte-mediated extracellular matrix turnover in human articular cartilage. Osteoarthritis Cartilage. 2001 ; 9: 720-726.
127. Kume S., Kato S., Yamagishi S., et al. Advanced glycation end-products attenuate human mesenchymal stem cells and prevent cognate differentiation into adipose tissue, cartilage, and bone. J Bone Miner Res. 2005 ; 20: 1647-1658. (Pubitemid 41243553)
128. Miyata T., Notoya K., Yoshida K., et al. 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 ; 8: 260-270. (Pubitemid 127455881)
129. Valcourt U., Merle B., Gineyts E., Viguet-Carrin S., Delmas PD, Garnero P. Non-enzymatic glycation of bone collagen modifies osteoclastic activity and differentiation. J Biol Chem. 2007 ; 282: 5691-5703. (Pubitemid 47093757)
130. Basu S., Michaelsson K., Olofsson H., Johansson S., Melhus H. Association between oxidative stress and bone mineral density. Biochem Biophys Res Commun. 2001 ; 288: 275-279. (Pubitemid 32999758)
131. 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: 1408-1414. (Pubitemid 46550975)
132. Bai XC, Lu D., Bai J., et al. Oxidative stress inhibits osteoblastic differentiation of bone cells by ERK and NF-kappaB. Biochem Biophys Res Commun. 2004 ; 314: 197-207.
133. Fatokun AA, Stone TW, Smith RA Hydrogen peroxide-induced oxidative stress in MC3T3-E1 cells: the effects of glutamate and protection by purines. Bone. 2006 ; 39: 542-551. (Pubitemid 44149273)
134. Arai M., Shibata Y., Pugdee K., Abiko Y., Ogata Y. Effects of reactive oxygen species (ROS) on antioxidant system and osteoblastic differentiation in MC3T3-E1 cells. IUBMB Life. 2007 ; 59: 27-33.
135. Lee DH, Lim BS, Lee YK, Yang HC Effects of hydrogen peroxide (H2O2) on alkaline phosphatase activity and matrix mineralization of odontoblast and osteoblast cell lines. Cell Biol Toxicol. 2006 ; 22: 39-46. (Pubitemid 43207808)
136. Bax BE, Alam AS, Banerji B., et al. Stimulation of osteoclastic bone resorption by hydrogen peroxide. Biochem Biophys Res Commun. 1992 ; 183: 1153-1158.
137. Suda N., Morita I., Kuroda T., Murota S. Participation of oxidative stress in the process of osteoclast differentiation. Biochim Biophys Acta. 1993 ; 1157: 318-323. (Pubitemid 23207815)
138. Fraser JH, Helfrich MH, Wallace HM, Ralston SH Hydrogen peroxide, but not superoxide, stimulates bone resorption in mouse calvariae. Bone. 1996 ; 19: 223-226. (Pubitemid 26302605)
139. Cornish J., Callon KE, Reid IR Insulin increases histomorphometric indices of bone formation In vivo. Calcif Tissue Int. 1996 ; 59: 492-495. (Pubitemid 26397171)
140. Ogata N., Chikazu D., Kubota N., et al. Insulin receptor substrate-1 in osteoblast is indispensable for maintaining bone turnover. J Clin Invest. 2000 ; 105: 935-943. (Pubitemid 30203066)
141. Shimoaka T., Kamekura S., Chikuda H., et al. Impairment of bone healing by insulin receptor substrate-1 deficiency. J Biol Chem. 2004 ; 279: 15314-15322. (Pubitemid 38618929)
142. Huang S., Kaw M., Harris MT, et al. Decreased osteoclastogenesis and high bone mass in mice with impaired insulin clearance due to liver-specific inactivation to CEACAM1. Bone. 2010 ; 46: 1138-1145.
143. Gandhi A., Beam HA, O'Connor JP, Parsons JR, Lin SS The effects of local insulin delivery on diabetic fracture healing. Bone. 2005 ; 37: 482-490. (Pubitemid 41317321)
144. Hough S., Russell JE, Teitelbaum SL, Avioli LV Calcium homeostasis in chronic streptozotocin-induced diabetes mellitus in the rat. Am J Physiol. 1982 ; 242: E451 - E456.
145. Ikeda K., Matsumoto T., Morita K., et al. The role of insulin in the stimulation of renal 1,25-dihydroxyvitamin D synthesis by parathyroid hormone in rats. Endocrinology. 1987 ; 121: 1721-1726. (Pubitemid 18012776)
146. Bereket A., Lang CH, Blethen SL, Ng LC, Wilson TA Insulin treatment normalizes reduced free insulin-like growth factor-I concentrations in diabetic children. Clin Endocrinol. 1996 ; 45: 321-326. (Pubitemid 26313219)
147. Rosen DM, Luben RA Multiple hormonal mechanisms for the control of collagen synthesis in an osteoblast-like cell line, MMB-1. Endocrinology. 1983 ; 112: 992-999.
148. Hickman J., McElduff A. Insulin sensitizes a cultured rat osteogenic sarcoma cell line to hormones which activate adenylate cyclase. Calcif Tissue Int. 1990 ; 46: 401-405. (Pubitemid 20176239)
149. Felsenfeld AJ, Iida-Klein A., Hahn TJ Interrelationship between parathyroid hormone and insulin: effects on DNA synthesis in UMR-106-01 cells. J Bone Miner Res. 1992 ; 7: 1319-1325. (Pubitemid 23000973)
150. Conover CA, Lee PD, Riggs BL, Powell DR Insulin-like growth factor-binding protein-1 expression in cultured human bone cells: regulation by insulin and glucocorticoid. Endocrinology. 1996 ; 137: 3295-3301. (Pubitemid 26250178)
151. 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 ; 218: 789-793. (Pubitemid 26050741)
152. Hill PA, Tumber A., Meikle MC Multiple extracellular signals promote osteoblast survival and apoptosis. Endocrinology. 1997 ; 138: 3849-3858. (Pubitemid 27351939)
153. Bohme K., Conscience-Egli M., Tschan T., Winterhalter KH, Bruckner P. Induction of proliferation or hypertrophy of chondrocytes in serum-free culture: the role of insulin-like growth factor-I, insulin, or thyroxine. J Cell Biol. 1992 ; 116: 1035-1042.
154. Shukunami C., Ishizeki K., Atsumi T., Ohta Y., Suzuki F., Hiraki Y. Cellular hypertrophy and calcification of embryonal carcinoma-derived chondrogenic cell line ATDC5 in vitro. J Bone Miner Res. 1997 ; 12: 1174-1188. (Pubitemid 27334963)
155. Phornphutkul C., Wu KY, Gruppuso PA The role of insulin in chondrogenesis. Mol Cell Endocrinol. 2006 ; 249: 107-115.
156. Iwata K., Asawa Y., Fujihara Y., et al. The effects of rapid-or intermediate-acting insulin on the proliferation and differentiation of cultured chondrocytes. Curr Aging Sci. 2010 ; 3: 26-33.
157. Thomas DM, Udagawa N., Hards DK, et al. Insulin receptor expression in primary and cultured osteoclast-like cells. Bone. 1998 ; 23: 181-186. (Pubitemid 28434661)
158. Makimattila S., Fineman MS, Yki-Jarvinen H. Deficiency of total and nonglycosylated amylin in plasma characterizes subjects with impaired glucose tolerance and type 2 diabetes. J Clin Endocrinol Metab. 2000 ; 85: 2822-2827. (Pubitemid 32269159)
159. Bronsky J., Prusa R., Nevoral J. The role of amylin and related peptides in osteoporosis. Clin Chim Acta. 2006 ; 373: 9-16. (Pubitemid 44376461)
160. Bronsky J., Prusa R. Amylin fasting plasma levels are decreased in patients with osteoporosis. Osteoporos Int. 2004 ; 15: 243-247. (Pubitemid 38391541)
161. Weng HB, Gu Q., Liu M., Cheng NN, Li D., Gao X. Increased secretion and expression of amylin in spontaneously diabetic Goto-Kakizaki rats treated with rhGLP-1 (7-36). Acta Pharmacol Sin. 2008 ; 29: 573-579. (Pubitemid 351601444)
162. Cornish J., Callon KE, Cooper GJ, Reid IR Amylin stimulates osteoblast proliferation and increases mineralized bone volume in adult mice. Biochem Biophys Res Commun. 1995 ; 207: 133-139.
163. Cornish J., Callon KE, Lin CQ, et al. Dissociation of the effects of amylin on osteoblast proliferation and bone resorption. Am J Physiol. 1998 ; 274 (5pt1); E827 - E833.
164. Dacquin R., Davey RA, Laplace C., et al. Amylin inhibits bone resorption while the calcitonin receptor controls bone formation in vivo. J Cell Biol. 2004 ; 164: 509-514. (Pubitemid 38233312)
165. Villa I., Rubinacci A., Ravasi F., Ferrara AF, Guidobono F. Effects of amylin on human osteoblast-like cells. Peptides. 1997 ; 18: 537-540. (Pubitemid 27273748)
166. Cornish J., Callon KE, Lin CQ, et al. Comparison of the effects of calcitonin gene-related peptide and amylin on osteoblasts. J Bone Miner Res. 1999 ; 14: 1302-1309. (Pubitemid 29368292)
167. Cornish J., Callon KE, Bava U., Kamona SA, Cooper GJ, Reid IR Effects of calcitonin, amylin, and calcitonin gene-related peptide on osteoclast development. Bone. 2001 ; 29: 162-168. (Pubitemid 32737190)
168. Alam AS, Moonga BS, Bevis PJ, Huang CL, Zaidi M. Amylin inhibits bone resorption by a direct effect on the motility of rat osteoclasts. Exp Physiol. 1993 ; 78: 183-196. (Pubitemid 23135264)
169. Dobnig H., Piswanger-Solkner JC, Roth M., et al. Type 2 diabetes mellitus in nursing home patients: effects on bone turnover, bone mass, and fracture risk. J Clin Endocrinol Metab. 2006 ; 91: 3355-3363. (Pubitemid 44402104)
170. Karaguzel G., Akcurin S., Ozdem S., Boz A., Bircan I. Bone mineral density and alterations of bone metabolism in children and adolescents with type 1 diabetes mellitus. J Pediatr Endocrinol Metab. 2006 ; 19: 805-814. (Pubitemid 44083537)
171. Murakami R., Murakami S., Tsushima R., et al. Glycaemic control and serum intact parathyroid hormone levels in diabetic patients on haemodialysis therapy. Nephrol Dial Transplant. 2008 ; 23: 315-320. (Pubitemid 351767408)
172. Jilka RL Molecular and cellular mechanisms of the anabolic effect of intermittent PTH. Bone. 2007 ; 40: 1434-1446. (Pubitemid 46756429)
173. Nakazawa T., Nakajima A., Shiomi K., Moriya H., Einhorn TA, Yamazaki M. Effects of low-dose, intermittent treatment with recombinant human parathyroid hormone (1-34) on chondrogenesis in a model of experimental fracture healing. Bone. 2005 ; 37: 711-719. (Pubitemid 41476394)
174. Malluche HH, Koszewski N., Monier-Faugere MC, Williams JP, Mawad H. Influence of the parathyroid glands on bone metabolism. Eur J Clin Invest. 2006 ; 36 (suppl 2). 23-33. (Pubitemid 44050607)
175. 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: 825-836. (Pubitemid 34462792)
176. Wang YH, Liu Y., Buhl K., Rowe DW Comparison of the action of transient and continuous PTH on primary osteoblast cultures expressing differentiation stage-specific GFP. J Bone Miner Res. 2005 ; 20: 5-14. (Pubitemid 41716213)
177. 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 ; 263: 18574-18577. (Pubitemid 19005138)
178. 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 ; 6: 2153-2159. (Pubitemid 23021565)
179. Schmid C., Schlapfer I., Peter M., et al. Growth hormone and parathyroid hormone stimulate IGFBP-3 in rat osteoblasts. Am J Physiol. 1994 ; 267 (2pt1): E226 - E233.
180. Porte D., Tuckermann J., Becker M., et al. Both AP-1 and Cbfa1-like factors are required for the induction of interstitial collagenase by parathyroid hormone. Oncogene. 1999 ; 18: 667-678. (Pubitemid 29080324)
181. Jilka RL, Weinstein RS, Bellido T., Roberson P., Parfitt AM, Manolagas SC Increased bone formation by prevention of osteoblast apoptosis with parathyroid hormone. J Clin Invest. 1999 ; 104: 439-446. (Pubitemid 29534328)
182. Bellido T., Ali AA, Plotkin LI, et al. Proteasomal degradation of Runx2 shortens parathyroid hormone-induced anti-apoptotic signaling in osteoblasts. A putative explanation for why intermittent administration is needed for bone anabolism. J Biol Chem. 2003 ; 278: 50259-50272. (Pubitemid 37548867)
183. Zerega B., Cermelli S., Bianco P., Cancedda R., Cancedda FD Parathyroid hormone [PTH(1-34)] and parathyroid hormone-related protein [PTHrP(1-34)] promote reversion of hypertrophic chondrocytes to a prehypertrophic proliferating phenotype and prevent terminal differentiation of osteoblast-like cells. J Bone Miner Res. 1999 ; 14: 1281-1289. (Pubitemid 29368290)
184. Zhen X., Wei L., Wu Q., Zhang Y., Chen Q. Mitogen-activated protein kinase p38 mediates regulation of chondrocyte differentiation by parathyroid hormone. J Biol Chem. 2001 ; 276: 4879-4885.
185. Hiraki Y., Yutani Y., Takigawa M., Kato Y., Suzuki F. Differential effects of parathyroid hormone and somatomedin-like growth factors on the sizes of proteoglycan monomers and their synthesis in rabbit costal chondrocytes in culture. Biochim Biophys Acta. 1985 ; 845: 445-453. (Pubitemid 15016033)
186. Koike T., Iwamoto M., Shimazu A., Nakashima K., Suzuki F., Kato Y. Potent mitogenic effects of parathyroid hormone (PTH) on embryonic chick and rabbit chondrocytes. Differential effects of age on growth, proteoglycan, and cyclic AMP responses of chondrocytes to PTH. J Clin Invest. 1990 ; 85: 626-631. (Pubitemid 20087461)
187. Klaus G., von Eichel B., May T., et al. Synergistic effects of parathyroid hormone and 1,25-dihydroxyvitamin D3 on proliferation and vitamin D receptor expression of rat growth cartilage cells. Endocrinology. 1994 ; 135: 1307-1315. (Pubitemid 24307503)
188. Chen HL, Demiralp B., Schneider A., et al. Parathyroid hormone and parathyroid hormone-related protein exert both pro- and anti-apoptotic effects in mesenchymal cells. J Biol Chem. 2002 ; 277: 19374-19381. (Pubitemid 34967444)
189. McSheehy PM, Chambers TJ Osteoblastic cells mediate osteoclastic responsiveness to parathyroid hormone. Endocrinology. 1986 ; 118: 824-828. (Pubitemid 16162808)
190. Akatsu T., Takahashi N., Udagawa N., et al. Parathyroid hormone (PTH)-related protein is a potent stimulator of osteoclast-like multinucleated cell formation to the same extent as PTH in mouse marrow cultures. Endocrinology. 1989 ; 125: 20-27. (Pubitemid 19182636)
191. Dai JC, He P., Chen X., Greenfield EM TNFalpha and PTH utilize distinct mechanisms to induce IL-6 and RANKL expression with markedly different kinetics. Bone. 2006 ; 38: 509-520.
192. Rosato MT, Schneider SH, Shapses SA Bone turnover and insulin-like growth factor I levels increase after improved glycemic control in noninsulin-dependent diabetes mellitus. Calcif Tissue Int. 1998 ; 63: 107-111. (Pubitemid 28347682)
193. 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: 295-303. (Pubitemid 30426548)
194. Moyer-Mileur LJ, Slater H., Jordan KC, Murray MA IGF-1 and IGF-binding proteins and bone mass, geometry, and strength: relation to metabolic control in adolescent girls with type 1 diabetes. J Bone Miner Res. 2008 ; 23: 1884-1891.
195. Dunger DB, Acerini CL IGF-1 and diabetes in adolescence. Diabetes Metab. 1998 ; 24: 101-107.
196. Higgins TF, Johnson BD Effect of exogenous IGF-1 on chondrocyte apoptosis in a rabbit intraarticular osteotomy model. J Orthop Res. 2010 ; 28: 125-130.
197. Reed BY, Zerwekh JE, Sakhaee K., Breslau NA, Gottschalk F., Pak CY Serum IGF 1 is low and correlated with osteoblastic surface in idiopathic osteoporosis. J Bone Miner Res. 1995 ; 10: 1218-1224.
198. Kurland ES, Rosen CJ, Cosman F., et al. Insulin-like growth factor-I in men with idiopathic osteoporosis. J Clin Endocrinol Metab. 1997 ; 82: 2799-2805. (Pubitemid 27385627)
199. Bouxsein ML, Rosen CJ, Turner CH, et al. Generation of a new congenic mouse strain to test the relationships among serum insulin-like growth factor I, bone mineral density, and skeletal morphology in vivo. J Bone Miner Res. 2002 ; 17: 570-579. (Pubitemid 34246632)
200. Zhang M., Xuan S., Bouxsein ML, et al. Osteoblast-specific knockout of the insulin-like growth factor (IGF) receptor gene reveals an essential role of IGF signaling in bone matrix mineralization. J Biol Chem. 2002 ; 277: 44005-44012. (Pubitemid 36157826)
201. Jiang J., Lichtler AC, Gronowicz GA, et al. Transgenic mice with osteoblast-targeted insulin-like growth factor-I show increased bone remodeling. Bone. 2006 ; 39: 494-504. (Pubitemid 44149270)
202. Hock JM, Centrella M., Canalis E. Insulin-like growth factor I has independent effects on bone matrix formation and cell replication. Endocrinology. 1988 ; 122: 254-260. (Pubitemid 18027610)
203. McCarthy TL, Centrella M., Canalis E. Regulatory effects of insulin-like growth factors I and II on bone collagen synthesis in rat calvarial cultures. Endocrinology. 1989 ; 124: 301-309. (Pubitemid 19033660)
204. Canalis E. Growth factor control of bone mass. J Cell Biochem. 2009 ; 108: 769-777.
205. Canalis E., Rydziel S., Delany AM, Varghese S., Jeffrey JJ Insulin-like growth factors inhibit interstitial collagenase synthesis in bone cell cultures. Endocrinology. 1995 ; 136: 1348-1354.
206. Rydziel S., Delany AM, Canalis E. Insulin-like growth factor I inhibits the transcription of collagenase 3 in osteoblast cultures. J Cell Biochem. 1997 ; 67: 176-183. (Pubitemid 27431162)
207. Oh CD, Chun JS Signaling mechanisms leading to the regulation of differentiation and apoptosis of articular chondrocytes by insulin-like growth factor-1. J Biol Chem. 2003 ; 278: 36563-36571.
208. Hill PA, Reynolds JJ, Meikle MC Osteoblasts mediate insulin-like growth factor-I and -II stimulation of osteoclast formation and function. Endocrinology. 1995 ; 136: 124-131.
209. Fiorelli G., Formigli L., Zecchi Orlandini S., et al. Characterization and function of the receptor for IGF-1 in human preosteoclastic cells. Bone. 1996 ; 18: 269-276. (Pubitemid 26118124)
210. Hou P., Sato T., Hofstetter W., Foged NT Identification and characterization of the insulin-like growth factor I receptor in mature rabbit osteoclasts. J Bone Miner Res. 1997 ; 12: 534-540. (Pubitemid 27155212)
211. Jehle PM, Jehle DR, Mohan S., Bohm BO Serum levels of insulin-like growth factor system components and relationship to bone metabolism in Type 1 and Type 2 diabetes mellitus patients. J Endocrinol. 1998 ; 159: 297-306. (Pubitemid 28520183)
212. Ahmad T., Ugarph-Morawski A., Lewitt MS, Li J., Saaf M., Brismar K. Diabetic osteopathy and the IGF system in the Goto-Kakizaki rat. Growth Horm IGF Res. 2008 ; 18: 404-411. (Pubitemid 351944035)
213. Mohan S., Nakao Y., Honda Y., et al. Studies on the mechanisms by which insulin-like growth factor (IGF) binding protein-4 (IGFBP-4) and IGFBP-5 modulate IGF actions in bone cells. J Biol Chem. 1995 ; 270: 20424-20431.
214. Kiepe D., Andress DL, Mohan S., et al. Intact IGF-binding protein-4 and -5 and their respective fragments isolated from chronic renal failure serum differentially modulate IGF-1 actions in cultured growth plate chondrocytes. J Am Soc Nephrol. 2001 ; 12: 2400-2410. (Pubitemid 33021117)
215. Kiepe D., Ulinski T., Powell DR, Durham SK, Mehls O., Tonshoff B. Differential effects of insulin-like growth factor binding proteins-1, -2, -3, and -6 on cultured growth plate chondrocytes. Kidney Int. 2002 ; 62: 1591-1600. (Pubitemid 35286266)
216. Kanatani M., Sugimoto T., Nishiyama K., Chihara K. Stimulatory effect of insulin-like growth factor binding protein-5 on mouse osteoclast formation and osteoclastic bone-resorbing activity. J Bone Miner Res. 2000 ; 15: 902-910. (Pubitemid 30233414)
217. Miyakoshi N., Richman C., Kasukawa Y., Linkhart TA, Baylink DJ, Mohan S. Evidence that IGF-binding protein-5 functions as a growth factor. J Clin Invest. 2001 ; 107: 73-81. (Pubitemid 32047416)
218. Ben Lagha N., Seurin D., Le Bouc Y., et al. Insulin-like growth factor binding protein (IGFBP-1) involvement in intrauterine growth retardation: study on IGFBP-1 overexpressing transgenic mice. Endocrinology. 2006 ; 147: 4730-4737. (Pubitemid 44402181)
219. Conover CA Insulin-like growth factor-binding proteins and bone metabolism. Am J Physiol. 2008 ; 294: E10 - E14.
220. Bouillon R. Diabetic bone disease. Low turnover osteoporosis related to decreased IGF-1 production. Verh K Acad Geneeskd Belg. 1992 ; 54: 365-391.
221. Ward DT, Yau SK, Mee AP, et al. Functional, molecular, and biochemical characterization of streptozotocin-induced diabetes. J Am Soc Nephrol. 2001 ; 12: 779-790. (Pubitemid 32246706)
222. St-Arnaud R. The direct role of vitamin D on bone homeostasis. Arch Biochem Biophys. 2008 ; 473: 225-230.
223. Lian JB, Coutts M., Canalis E. Studies of hormonal regulation of osteocalcin synthesis in cultured fetal rat calvariae. J Biol Chem. 1985 ; 260: 8706-8710. (Pubitemid 16239667)
224. Oldberg A., Jirskog- Hed B., Axelsson S., Heinegard D. Regulation of bone sialoprotein mRNA by steroid hormones. J Cell Biol. 1989 ; 109 (6pt1). 3183-3186. (Pubitemid 20011941)
225. Zhang R., Ducy P., Karsenty G. 1,25-Dihydroxyvitamin D3 inhibits osteocalcin expression in mouse through an indirect mechanism. J Biol Chem. 1997 ; 272: 110-116. (Pubitemid 27021132)
226. McSheehy PM, Chambers TJ 1,25-Dihydroxyvitamin D3 stimulates rat osteoblastic cells to release a soluble factor that increases osteoclastic bone resorption. J Clin Invest. 1987 ; 80: 425-429.
227. Vincent C., Kogawa M., Findlay DM, Atkins GJ The generation of osteoclasts from RAW 264.7 precursors in defined, serum-free conditions. J Bone Miner Metab. 2009 ; 27: 114-119.
228. Linkhart TA, Keffer MJ Differential regulation of insulin-like growth factor-I (IGF-1) and IGF-II release from cultured neonatal mouse calvaria by parathyroid hormone, transforming growth factor-beta, and 1,25-dihydroxyvitamin D3. Endocrinology. 1991 ; 128: 1511-1518.
229. Davis RE, Calder JS, Curnow DH Serum pyridoxal and folate concentrations in diabetics. Pathology. 1976 ; 8: 151-156.
230. Wilson RG, Davis RE Serum pyridoxal concentrations in children with diabetes mellitus. Pathology. 1977 ; 9: 95-98. (Pubitemid 8124276)
231. Okada M., Shibuya M., Yamamoto E., Murakami Y. Effect of diabetes on vitamin B6 requirement in experimental animals. Diabetes Obes Metab. 1999 ; 1: 221-225.
232. 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. Osteoporos Int. 2006 ; 17: 1514-1523. (Pubitemid 44387486)
233. Bird TA, Levene CI Lysyl oxidase: evidence that pyridoxal phosphate is a cofactor. Biochem Biophys Res Commun. 1982 ; 108: 1172-1180.
234. Fujii K., Kajiwara T., Kurosu H. Effect of vitamin B6 deficiency on the crosslink formation of collagen. FEBS Lett. 1979 ; 97: 193-195. (Pubitemid 9108542)
235. Booth AA, Khalifah RG, Todd P., Hudson BG In vitro kinetic studies of formation of antigenic advanced glycation end products (AGEs). Novel inhibition of post-Amadori glycation pathways. J Biol Chem. 1997 ; 272: 5430-5437. (Pubitemid 27102361)
236. Anwar MM, Meki AR Oxidative stress in streptozotocin-induced diabetic rats: effects of garlic oil and melatonin. Comp Biochem Physiol A Mol Integr Physiol. 2003 ; 135: 539-547. (Pubitemid 37289114)
237. Astaneie F., Afshari M., Mojtahedi A., et al. Total antioxidant capacity and levels of epidermal growth factor and nitric oxide in blood and saliva of insulin-dependent diabetic patients. Arch Med Res. 2005 ; 36: 376-381. (Pubitemid 40798392)
238. Chien WY, Yang KD, Eng HL, et al. Increased plasma concentration of nitric oxide in type 2 diabetes but not in nondiabetic individuals with insulin resistance. Diabetes Metab. 2005 ; 31: 63-68. (Pubitemid 40327594)
239. Hukkanen M., Hughes FJ, Buttery LD, et al. Cytokine-stimulated expression of inducible nitric oxide synthase by mouse, rat, and human osteoblast-like cells and its functional role in osteoblast metabolic activity. Endocrinology. 1995 ; 136: 5445-5453.
240. Damoulis PD, Hauschka PV Nitric oxide acts in conjunction with proinflammatory cytokines to promote cell death in osteoblasts. J Bone Miner Res. 1997 ; 12: 412-422. (Pubitemid 27120478)
241. Kim SJ, Kim HG, Oh CD, et al. p38 kinase-dependent and- independent Inhibition of protein kinase C zeta and -alpha regulates nitric oxide-induced apoptosis and dedifferentiation of articular chondrocytes. J Biol Chem. 2002 ; 277: 30375-30381.
242. MacIntyre I., Zaidi M., Alam AS, et al. Osteoclastic inhibition: an action of nitric oxide not mediated by cyclic GMP. Proc Natl Acad Sci U S A. 1991 ; 88: 2936-2940. (Pubitemid 21916535)