Characteristics of diabetic osteopenia in KK-Ay diabetic mice

Biological and Pharmaceutical Bulletin

Volumn 35, Issue 3, 2012, Pages 438-443

  Takagi, Satoshi ^a,b   Miura, Toshihiro ^a   Yamashita, Takenori ^a   Ando, Naoki ^b   Nakao, Haruka ^a   Ishihara, Eriko ^a   Ishida, Torao ^a  

^a SUZUKA UNIVERSITY OF MEDICAL SCIENCE   (Japan)

^b Takagi Project   (Japan)

Author keywords

Bone mineral density; Femur; KK Ay mice; Osteopenia; Type 2 diabetes

Indexed keywords

GLUCOSE; OSTEOCALCIN;

ADULT ANIMAL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE DENSITY; CONTROLLED STUDY; DUAL ENERGY X RAY ABSORPTIOMETRY; FEMUR; GLUCOSE BLOOD LEVEL; MALE; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OSTEOPENIA; PROTEIN BLOOD LEVEL;

ANIMALS; BLOOD GLUCOSE; BONE DENSITY; BONE DISEASES, METABOLIC; DIABETES MELLITUS, TYPE 2; DISEASE MODELS, ANIMAL; FEMUR; MALE; MICE;

EID: 84857815681     PISSN: 09186158     EISSN: 13475215     Source Type: Journal    
DOI: 10.1248/bpb.35.438     Document Type: Article

References (53)

1. Ohkubo Y, Kishikawa H, Araki E, Miyata T, Isami S, Motoyoshi S, Kojima Y, Furuyoshi N, Shichiri M. Intensive insulin therapy prevents the progression of diabetic microvascular complications in Japanese patients with non-insulin-dependent diabetes mellitus: a randomized prospective 6-year study. Diabetes Res. Clin. Pract., 28, 103-117 (1995).
2. The Diabetes Control and Complications Trial Research Group. The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. N. Engl. J. Med., 329, 977-986 (1993).
3. UK Prospective Diabetes Study (UKPDS) Group. Intensive bloodglucose control with sulphonylureas or insulin compared with conventional treatment and risk of complications in patients with type 2 diabetes (UKPDS 33). Lancet, 352, 837-853 (1998).
4. Chen HF, Ho CA, Li CY. Increased risks of hip fracture in diabetic patients of Taiwan: a population-based study. Diabetes Care, 31, 75-80 (2008).
5. Hui SL, Epstein S, Johnston CC Jr. A prospective study of bone mass in patients with type I diabetes. J. Clin. Endocrinol. Metab., 60, 74-80 (1985).
6. 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., 166, 495-505 (2007).
7. Nicodemus KK, Folsom AR, Iowa Women's Health Study. Type 1 and type 2 diabetes and incident hip fractures in postmenopausal women. Diabetes Care, 24, 1192-1197 (2001).
8. Schwartz AV, Sellmeyer DE, Ensrud KE, Cauley JA, Tabor HK, Schreiner PJ, Jamal SA, Black DM, Cummings SR, Study of Osteoporotic Features Research Group. Older women with diabetes have an increased risk of fracture: a prospective study. J. Clin. Endocrinol. Metab., 86, 32-38 (2001).
9. 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, 48, 1292-1299 (2005).
10. Vestergaard P. Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2 diabetes - a meta-analysis. Osteoporos. Int., 18, 427-444 (2007).
11. Yamamoto M, Yamaguchi T, Yamauchi M, Kaji H, Sugimoto T. Bone mineral density is not sensitive enough to assess the risk of vertebral fractures in type 2 diabetic women. Calcif. Tissue Int., 80, 353-358 (2007).
12. Miazgowski T, Czekalski S. A 2-year follow-up study on bone mineral density and markers of bone turnover in patients with longstanding insulin-dependent diabetes mellitus. Osteoporos. Int., 8, 399-403 (1998).
13. Muñoz-Torres M, Jódar E, Escobar-Jiménez F, López-Ibarra PJ, Luna JD. Bone mineral density measured by dual X-ray absorptiometry in Spanish patients with insulin-dependent diabetes mellitus. Calcif. Tissue Int., 58, 316-319 (1996).
14. 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, 29, 306-311 (2006).
15. Tuominen JT, Impivaara O, Puukka P, Rönnemaa T. Bone mineral density in patients with type 1 and type 2 diabetes. Diabetes Care, 22, 1196-1200 (1999).
16. 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, 40, 1408-1414 (2007).
17. 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 life. J. Bone Miner. Res., 24, 1618-1627 (2009).
18. Verhaeghe J, Visser WJ, Einhorn TA, Bouillon R. Osteoporosis and diabetes: lessons from the diabetic BB rat. Horm. Res., 34, 245-248 (1990).
19. 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, 39, 477-482 (1990).
20. Petit MA, Paudel ML, Taylor BC, Hughes JM, Strotmeyer ES, Schwartz AV, Cauley JA, Zmuda JM, Hoffman AR, Ensrud KE, Osteoporotic Fractures in Men (MrOs) Study Group. Bone mass and strength in older men with type 2 diabetes: the Osteoporotic Fractures in Men Study. J. Bone Miner. Res., 25, 285-291 (2010).
21. Schwartz AV, Sellmeyer DE. Women, type 2 diabetes, and fracture risk. Curr. Diab. Rep., 4, 364-369 (2004).
22. Strotmeyer ES, Cauley JA, Schwartz AV, Nevitt MC, Resnick HE, Zmuda JM, Bauer DC, Tylavsky FA, de Rekeneire N, Harris TB, Newman AB, Health ABC, Health ABC Study. 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., 19, 1084-1091 (2004).
23. van Daele PL, Stolk RP, Burger H, Algra D, Grobbee DE, Hofman A, Birkenhäger JC, Pols HA. Bone density in non-insulin-dependent diabetes mellitus. The Rotterdam Study. Ann. Intern. Med., 122, 409-414 (1995).
24. 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., 24, 702-709 (2009).
25. Buysschaert M, Cauwe F, Jamart J, Brichant C, De Coster P, Magnan A, Donckier J. Proximal femur density in types 1 and 2 diabetic patients. Diabete Metab., 18, 32-37 (1992).
26. 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., 23, 43-54 (1994).
27. Isaia G, Bodrato L, Carlevatto V, Mussetta M, Salamano G, Molinatti GM. Osteoporosis in type II diabetes. Acta Diabetol. Lat., 24, 305-310 (1987).
28. Ishida H, Seino Y, Matsukura S, Ikeda M, Yawata M, Yamashita G, Ishizuka S, Imura H. Diabetic osteopenia and circulating levels of vitamin D metabolites in type 2 (noninsulin-dependent) diabetes. Metabolism, 34, 797-801 (1985).
29. Levin ME, Boisseau VC, Avioli LV. Effects of diabetes mellitus on bone mass in juvenile and adult-onset diabetes. N. Engl. J. Med., 294, 241-245 (1976).
30. Seino Y, Ishida H, Imura H, Akazawa Y, Aochi O, Hamada S, Horiuchi N, Hoshi M, Ikeda M, Igarashi T, Izumi K, Kanatsuna T, Kido H, Matsukura S, Matsuoka A, Miyamura K, Morita T, Mozai T, Nanbu S, Nannjo K, Nonaka K, Ohsawa A, Ohtsuka A, Sako Y, Seino Y, Seki J, Shichiri M, Shigeta Y, Shima K, Yamamoto M, Yawata M. Diabetic osteopenia in central Japan. Diabete Metab., 11, 216-219 (1985).
31. Amir G, Rosenmann E, Sherman Y, Greenfeld Z, Ne'eman Z, Cohen AM. Osteoporosis in the Cohen diabetic rat: correlation between histomorphometric changes in bone and microangiopathy. Lab. Invest., 82, 1399-1405 (2002).
32. Fujii H, Hamada Y, Fukagawa M. Bone formation in spontaneously diabetic Torii-newly established model of non-obese type 2 diabetes rats. Bone, 42, 372-379 (2008).
33. 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, 44, 648-655 (2009).
34. Lorentzon R, Alehagen U, Boquist L. Osteopenia in mice with genetic diabetes. Diabetes Res. Clin. Pract., 2, 157-163 (1986).
35. Akin O, Göl K, Aktürk M, Erkaya S. Evaluation of bone turnover in postmenopausal patients with type 2 diabetes mellitus using biochemical markers and bone mineral density measurements. Gynecol. Endocrinol., 17, 19-29 (2003).
36. Ishida H, Seino Y, Taminato T, Usami M, Takeshita N, Seino Y, 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, 37, 702-706 (1988).
37. 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., 68, 117-125 (2005).
38. 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.), 128, 69-73 (1993).
39. Verhaeghe J, Suiker AM, Nyomba BL, Visser WJ, Einhorn TA, Dequeker J, Bouillon R. Bone mineral homeostasis in spontaneously diabetic BB rats. II. Impaired bone turnover and decreased osteocalcin synthesis. Endocrinology, 124, 573-582 (1989).
40. Marks V, Lloyd K. Preservation of blood glucose analysis by glucose oxidase. Clin. Chim. Acta, 8, 326 (1963).
41. Bridges MJ, Moochhala SH, Barbour J, Kelly CA. Influence of diabetes on peripheral bone mineral density in men: a controlled study. Acta Diabetol., 42, 82-86 (2005).
42. Wakasugi M, Wakao R, Tawata M, Gan N, Koizumi K, Onaya T. Bone mineral density measured by dual energy X-ray absorptiometry in patients with non-insulin-dependent diabetes mellitus. Bone, 14, 29-33 (1993).
43. Nakamura M. A diabetic strain of the mouse. Proc. Jpn. Acad., 38, 348-352 (1962).
44. Nishimura M. Breeding of mice strains for diabetes mellitus. Exp. Anim., 18, 147-157 (1969).
45. 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., 82, 2915-2920 (1997).
46. Terada M, Inaba M, Yano Y, Hasuma T, Nishizawa Y, Morii H, Otani S. Growth-inhibitory effect of a high glucose concentration on osteoblast-like cells. Bone, 22, 17-23 (1998).
47. Einhorn TA, Boskey AL, Gundberg CM, Vigorita VJ, Devlin VJ, Beyer MM. The mineral and mechanical properties of bone in chronic experimental diabetes. J. Orthop. Res., 6, 317-323 (1988).
48. Kayath MJ, Tavares EF, Dib SA, Vieira JG. Prospective bone mineral density evaluation in patients with insulin-dependent diabetes mellitus. J. Diabetes Complications, 12, 133-139 (1998).
49. Sayinalp S, Gedik O, Koray Z. Increasing serum osteocalcin after glycemic control in diabetic men. Calcif. Tissue Int., 57, 422-425 (1995).
50. Ishida H, Seino Y, Takeshita N, Kurose T, Tsuji K, Okamoto Y, Someya Y, Hara K, Akiyama Y, Imura H, Nozawa M. Effect of pancreas transplantation on decreased levels of circulating bone gamma-carboxyglutamic acid-containing protein and osteopenia in rats with streptozotocin-induced diabetes. Acta Endocrinol. (Copenh.), 127, 81-85 (1992).
51. Tsujio M, Mizorogi T, Kitamura I, Maeda Y, Nishijima K, Kuwahara S, Ohno T, Niida S, Nagaya M, Saito R, Tanaka S. Bone mineral analysis through dual energy X-ray absorptiometry in laboratory animals. J. Vet. Med. Sci., 71, 1493-1497 (2009).
52. Dickson GR, Luczak M, Włodarski KH. The limitation of DEXA analysis for bone mass determination in mice. Folia Biol. (Krakow), 52, 125-129 (2004).
53. 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., 17, 1514-1523 (2006).