Bone inflammation and altered gene expression with type Idiabetes early onset

Journal of Cellular Physiology

Volumn 218, Issue 3, 2009, Pages 575-583

  Motyl, Katherine J ^a,b   Botolin, Sergiu ^a   Irwin, Regina ^a,b   Appledorn, Daniel M ^c   Kadakia, Tejas ^c   Amalfitano, Andrea ^c   Schwartz, Richard C ^c   McCabe, Laura R ^a,b  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b Michigan State University   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; GLUCOSE; MESSENGER RNA; OSTEOCALCIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA 2; STREPTOZOCIN; TRANSCRIPTION FACTOR RUNX2; BIOLOGICAL MARKER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY FAT; BONE INFLAMMATION; BONE METABOLISM; CONTROLLED STUDY; FEMALE; GENE; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; INSULIN DEPENDENT DIABETES MELLITUS; MOUSE; MUSCLE MASS; MUSCULOSKELETAL SYSTEM INFLAMMATION; NONHUMAN; OSSIFICATION; OSTEOLYSIS; PRIORITY JOURNAL; TRAP5 GENE; ANIMAL; BAGG ALBINO MOUSE; BLOOD; EXPERIMENTAL DIABETES MELLITUS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; OSTEITIS; OSTEOCLAST; PHENOTYPE; TIME;

MUS;

ANIMALS; BIOLOGICAL MARKERS; BONE RESORPTION; CYTOKINES; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; FEMALE; GENE EXPRESSION REGULATION; MICE; MICE, INBRED BALB C; OSTEITIS; OSTEOCLASTS; PHENOTYPE; RNA, MESSENGER; TIME FACTORS;

EID: 58149388693     PISSN: 00219541     EISSN: None     Source Type: Journal    
DOI: 10.1002/jcp.21626     Document Type: Article

References (103)

1. Auwerx J, Dequeker J, Bouillon R, Geusens P, Nijs J. 1988. Mineral metabolism and bone mass at peripheral and axial skeleton in diabetes mellitus. Diabetes 37:8-12.
2. Baker PJ, Dixon M, Evans RT, Dufour L, Johnson E, Roopenian DC. 1999. CD4(+) T cells and the proinflammatory cytokines gamma interferon and interleukin-6 contribute to alveolar bone loss in mice. Infect Immun 67:2804-2809.
3. Bonfanti R, Mora S, Prinster C, Bognetti E, Meschi F, Puzzovio M, Proverbio MC, Chiumello G. 1997. Bone modeling indexes at onset and during the first year of follow-up in insulin-dependent diabetic children. Calcif Tissue Int 60:397-400.
4. Botolin S, McCabe LR. 2006. Inhibition of PPARgamma prevents type I diabetic bone marrow adiposity but not bone loss. J Cell Physiol 209:967-976.
5. Botolin S, McCabe LR. 2007. Bone loss and increased bone adiposity in spontaneous and pharmacologically induced diabetic mice. Endocrinology 148:198-205.
6. Botolin S, Faugere MC, Malluche H, Orth M, Meyer R, McCabe LR. 2005. Increased bone adiposity and peroxisomal proliferator-activated receptor-gamma2 expression in type I diabetic mice. Endocrinology 146:3622-3631.
7. Bouillon R. 1991. Diabetic bone disease [editorial]. Calcif Tissue Int 49:155-160.
8. Cakatay U, Telci A, Kayali R, Akcay T, Sivas A, Aral F. 1998. Changes in bone turnover on deoxypyridinoline levels in diabetic patients. Diabetes Res Clin Pract 40:75-79.
9. Cenci S, Toraldo G, Weitzmann MN, Roggia C, Gao Y, Qian WP, Sierra O, Pacifici R. 2003. Estrogen deficiency induces bone loss by increasing T cell proliferation and lifespan through IFN-gamma-induced class II transactivator. Proc Natl Acad Sci USA 100:10405-10410.
10. Chen RM, Chen TL, Chiu WT, Chang CC. 2005. Molecular mechanism of nitric oxide-induced osteoblast apoptosis. J Orthop Res 23:462-468.
11. Chomczynski P, Sacchi N. 1987. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156-159.
12. Cloos C, Wahl P, Hasslacher C, Traber L, Kistner M, Jurkuhn K, Schmidt-Gayk H. 1998. Urinary glycosylated, free and total pyridinoline and free and total deoxypyridinoline in diabetes mellitus. Clin Endocrinol (Oxf) 48:317-323.
13. Compston JE, Vedi S, Croucher PI, Garrahan NJ, O'Sullivan MM. 1994. Bone turnover in non-steroid treated rheumatoid arthritis. Ann Rheum Dis 53:163-166.
14. Cvetkovic I, Al-Abed Y, Miljkovic D, Maksimovic-Ivanic D, Roth J, Bacher M, Lan HY, Nicoletti F, Stosic-Grujicic S. 2005. Critical role of macrophage migration inhibitory factor activity in experimental autoimmune diabetes. Endocrinology 146:2942-2951.
15. Ding KH, Wang ZZ, Hamrick MW, Deng ZB, Zhou L, Kang B, Yan SL, She JX, Stern DM, Isales CM, Mi QS. 2006. Disordered osteoclast formation in RAGE-deficient mouse establishes an essential role for RAGE in diabetes related bone loss. Biochem Biophys Res Commun 340:1091-1097.
16. Drachenberg CB, Klassen DK, Weir MR, Wiland A, Fink JC, Bartlett ST, Cangro CB, Blahut S, Papadimitriou JC. 1999. Islet cell damage associated with tacrolimus and cyclosporine: Morphological features in pancreas allograft biopsies and clinical correlation. Transplantation 68:396-402.
17. El-Mahmoudy A, Shimizu Y, Shiina T, Matsuyama H, Nikami H, Takewaki T. 2005. Macrophage-derived cytokine and nitric oxide profiles in type I and type II diabetes mellitus: Effect of thymoquinone. Acta Diabetol 42:23-30.
18. Forsen L, Meyer HE, Midthjell K, Edna TH. 1999. Diabetes mellitus and the incidence of hip fracture: Results from the Nord-Trondelag Health Survey. Diabetologia 42:920-925.
19. Fox SW, Chambers TJ. 2000. Interferon-gamma directly inhibits TRANCE-induced osteoclastogenesis. Biochem Biophys Res Commun 276:868-872.
20. Gao Y, Grassi F, Ryan MR, Terauchi M, Page K, Yang X, Weitzmann MN, Pacifici R. 2007. IFN-gamma stimulates osteoclast formation and bone loss in vivo via antigen-driven T cell activation. J Clin Invest 117:122-132.
21. Gilbert L, He X, Farmer P, Rubin J, Drissi H, van Wijnen AJ, Lian JB, Stein GS, Nanes MS. 2002. Expression of the osteoblast differentiation factor RUNX2 (Cbfa1/AML3/Pebp2alpha A) is inhibited by tumor necrosis factor-alpha. J Biol Chem 277:2695-2701.
22. Goodman WG, Hori MT. 1984. Diminished bone formation in experimental diabetes. Relationship to osteoid maturation and mineralization. Diabetes 33:825-831.
23. Gowen M, Mundy GR. 1986. Actions of recombinant interleukin 1, interleukin 2, and interferon-gamma on bone resorption in vitro. J Immunol 136:2478-2482.
24. Graves DT, Kayal RA. 2008. Diabetic complications and dysregulated innate immunity. Front Biosci 13:1227-1239.
25. Gunczler P, Lanes R, Paz-Martinez V, Martins R, Esaa S, Colmenares V, Weisinger JR. 1998. Decreased lumbar spine bone mass and low bone turnover in children and adolescents with insulin dependent diabetes mellitus followed longitudinally. J Pediatr Endocrinol Metab 11:413-419.
26. Halleen JM, Alatalo SL, Suominen H, Cheng S, Janckila AJ, Vaananen HK. 2000. Tartrate-resistant acid phosphatase 5b: A novel serum marker of bone resorption. J Bone Miner Res 15:1337-1345.
27. Halleen JM, Ylipahkala H, Alatalo SL, Janckila AJ, Heikkinen JE, Suominen H, Cheng S, Vaananen HK. 2002. Serum tartrate-resistant acid phosphatase 5b, but not 5a, correlates with other markers of bone turnover and bone mineral density. Calcif Tissue Int 71:20-25.
28. Hayward MD, Jones BK, Saparov A, Hain HS, Trillat AC, Bunzel MM, Corona A, Li-Wang B, Strenkowski B, Giordano C, Shen H, Arcamone E, Weidlick J, Vilensky M, Tugusheva M, Felkner RH, Campbell W, Rao Y, Grass DS, Buiakova O. 2007. An extensive phenotypic characterization of the hTNFalpha transgenic mice. BMC Physiol 7:13.
29. He H, Liu R, Desta T, Leone C, Gerstenfeld LC, Graves DT. 2004. Diabetes causes decreased osteoclastogenesis, reduced bone formation, and enhanced apoptosis of osteoblastic cells in bacteria stimulated bone loss. Endocrinology 145:447-452.
30. Herrero S, Calvo OM, Garcia-Moreno C, Martin E, San Roman JI, Martin M, Garcia-Talavera JR, Calvo JJ, del Pino-Montes J. 1998. Low bone density with normal bone turnover in ovariectomized and streptozotocin-induced diabetic rats. Calcif Tissue Int 62:260-265.
31. Hie M, Shimono M, Fujii K, Tsukamoto I. 2007. Increased cathepsin K and tartrate-resistant acid phosphatase expression in bone of streptozotocin-induced diabetic rats. Bone 41:1045-1050.
32. Horcajada-Molteni MN, Chanteranne B, Lebecque P, Davicco MJ, Coxam V, Young A, Barlet JP. 2001. Amylin and bone metabolism in streptozotocin-induced diabetic rats. J Bone Miner Res 16:958-965.
33. Hough S, Avioli LV, Bergfeld MA, Fallon MD, Slatopolsky E, Teitelbaum SL. 1981. Correction of abnormal bone and mineral metabolism in chronic streptozotocin-induced diabetes mellitus in the rat by insulin therapy. Endocrinology 108:2228-2234.
34. Hui SL, Epstein S, Johnston CC, Jr. 1985. A prospective study of bone mass in patients with type I diabetes. J Clin Endocrinol Metab 60:74-80.
35. Ikejima S, Sasaki S, Sashinami H, Mori F, Ogawa Y, Nakamura T, Abe Y, Wakabayashi K, Suda T, Nakane A. 2005. Impairment of host resistance to Listeria monocytogenes infection in liver of db/db and ob/ob mice. Diabetes 54:182-189.
36. Inzerillo AM, Epstein S. 2004. Osteoporosis and diabetes mellitus. Rev Endocr Metab Disord 5:261-268.
37. Kasama T, Isozaki T, Odai T, Matsunawa M, Wakabayashi K, Takeuchi HT, Matsukura S, Adachi M, Tezuka M, Kobayashi K. 2007. Expression of angiopoietin-1 in osteoblasts and its inhibition by tumor necrosis factor-alpha and interferon-gamma. Transl Res 149:265-273.
38. Kast-Woelbern HR, Dana SL, Cesario RM, Sun L, de Grandpre LY, Brooks ME, Osburn DL, Reifel-Miller A, Klausing K, Leibowitz MD. 2004. Rosiglitazone induction of Insig-1 in white adipose tissue reveals a novel interplay of peroxisome proliferator-activated receptor gamma and sterol regulatory element-binding protein in the regulation of adipogenesis. J Biol Chem 279:23908-23915.
39. Kemink SA, Hermus AR, Swinkels LM, Lutterman JA, Smals AG. 2000. Osteopenia in insulin-dependent diabetes mellitus; prevalence and aspects of pathophysiology. J Endocrinol Invest 23:295-303.
40. Key LL, Jr., Rodriguiz RM, Willi SM, Wright NM, Hatcher HC, Eyre DR, Cure JK, Griffin PP, Ries WL. 1995. Long-term treatment of osteopetrosis with recombinant human interferon gamma. N Engl J Med 332:1594-1599.
41. Krakauer JC, McKenna MJ, Buderer NF, Rao DS, Whitehouse FW, Parfitt AM. 1995. Bone loss and bone turnover in diabetes. Diabetes 44:775-782.
42. Lacroix-Lamande S, Mancassola R, Naciri M, Laurent F. 2002. Role of gamma interferon in chemokine expression in the ileum of mice and in a murine intestinal epithelial cell line after Cryptosporidium parvum infection. Infect Immun 70:2090-2099.
43. Lee LF, Xu B, Michie SA, Beilhack GF, Warganich T, Turley S, McDevitt HO. 2005. The role of TNF-alpha in the pathogenesis of type 1 diabetes in the nonobese diabetic mouse: Analysis of dendritic cell maturation. Proc Natl Acad Sci USA 102:15995-16000.
44. Leidig-Bruckner G, Ziegler R. 2001. Diabetes mellitus a risk for osteoporosis? Exp Clin Endocrinol Diabetes 109:S493-514.
45. Lewis ML, Hughes-Fulford M. 2000. Regulation of heat shock protein message in Jurkat cells cultured under serum-starved and gravity-altered conditions. J Cell Biochem 77:127-134.
46. Li YP, Stashenko P. 1992. Proinflammatory cytokines tumor necrosis factor-alpha and IL-6, but not IL-1, down-regulate the osteocalcin gene promoter. J Immunol 148:788-794.
47. Li J, Takaishi K, Cook W, McCorkle SK, Unger RH. 2003. Insig-1 "brakes" lipogenesis in adipocytes and inhibits differentiation of preadipocytes. Proc Natl Acad Sci USA 100:9476-9481.
48. Lindberg MK, Moverare S, Eriksson AL, Skrtic S, Gao H, Dahlman-Wright K, Gustafsson JA, Ohlsson C. 2002. Identification of estrogen-regulated genes of potential importance for the regulation of trabecular bone mineral density. J Bone Miner Res 17:2183-2195.
49. Liu R, Bal HS, Desta T, Behl Y, Graves DT. 2006. Tumor necrosis factor-alpha mediates diabetes-enhanced apoptosis of matrix-producing cells and impairs diabetic healing. Am J Pathol 168:757-764.
50. Locatto ME, Abranzon H, Caferra D, Fernandez MC, Alloatti R, Puche RC. 1993. Growth and development of bone mass in untreated alloxan diabetic rats. Effects of collagen glycosylation and parathyroid activity on bone turnover. Bone Miner 23:129-144.
51. Maksimovic-Ivanic D, Trajkovic V, Miljkovic DJ, Mostarica Stojkovic M, Stosic-Grujicic S. 2002. Down-regulation of multiple low dose streptozotocin-induced diabetes by mycophenolate mofetil. Clin Exp Immunol 129:214-223.
52. Mann GN, Jacobs TW, Buchinsky FJ, Armstrong EC, Li M, Ke HZ, Ma YF, Jee WS, Epstein S. 1994. Interferon-gamma causes loss of bone volume in vivo and fails to ameliorate cyclosporin A-induced osteopenia. Endocrinology 135:1077-1083.
53. Manoury-Schwartz B, Chiocchia G, Bessis N, Abehsira-Amar O, Batteux F, Muller S, Huang S, Boissier MC, Fournier C. 1997. High susceptibility to collagen-induced arthritis in mice lacking IFN-gamma receptors. J Immunol 158:5501-5506.
54. McCabe LR. 2007. Understanding the pathology and mechanisms of type I diabetic bone loss. J Cell Biochem 102:1343-1357.
55. McCabe LR, Kockx M, Lian J, Stein J, Stein G. 1995. Selective expression of fos- and jun-related genes during osteoblast proliferation and differentiation. Exp Cell Res 218:255-262.
56. Miao J, Brismar K, Nyren O, Ugarph-Morawski A, Ye W. 2005. Elevated hip fracture risk in type 1 diabetic patients: A population-based cohort study in Sweden. Diabetes Care 28:2850-2855.
57. Mishima N, Sahara N, Shirakawa M, Ozawa H. 2002. Effect of streptozotocin-induced diabetes mellitus on alveolar bone deposition in the rat. Arch Oral Biol 47:843-849.
58. Mogi M, Kinpara K, Kondo A, Togari A. 1999. Involvement of nitric oxide and biopterin in proinflammatory cytokine-induced apoptotic cell death in mouse osteoblastic cell line MC3T3-E1. Biochem Pharmacol 58:649-654.
59. Mogi M, Kondo A, Kinpara K, Togari A. 2000. Anti-apoptotic action of nerve growth factor in mouse osteoblastic cell line. Life Sci 67:1197-1206.
60. Mohanty SK, Shivakumar P, Sabla G, Bezerra JA. 2006. Loss of interleukin-12 modifies the pro-inflammatory response but does not prevent duct obstruction in experimental biliary atresia. BMC Gastroenterol 6:14.
61. Moriyama H, Ukai T, Hara Y. 2002. Interferon-gamma production changes in parallel with bacterial lipopolysaccharide induced bone resorption in mice: An immunohistometrical study. Calcif Tissue Int 71:53-58.
62. Nanes MS. 2003. Tumor necrosis factor-alpha: Molecular and cellular mechanisms in skeletal pathology. Gene 321:1-15.
63. Ontiveros C, McCabe LR. 2003. Simulated microgravity suppresses osteoblast phenotype, Runx2 levels and AP-1 transactivation. J Cell Biochem 88:427-437.
64. Ontiveros C, Irwin R, Wiseman RW, McCabe LR. 2004. Hypoxia suppresses runx2 independent of modeled microgravity. J Cell Physiol 200:169-176.
65. Ozeki N, Mogi M, Nakamura H, Togari A. 2002. Differential expression of the Fas-Fas ligand system on cytokine-induced apoptotic cell death in mouse osteoblastic cells. Arch Oral Biol 47:511-517.
66. Pechhold K, Patterson NB, Blum C, Fleischacker CL, Boehm BO, Harlan DM. 2001. Low dose streptozotocin-induced diabetes in rat insulin promoter-mCD80-transgenic mice is T cell autoantigen-specific and CD28 dependent. J Immunol 166:2531-2539.
67. Pighin D, Karabatas L, Pastorale C, Dascal E, Carbone C, Chicco A, Lombardo YB, Basabe JC. 2005. Role of lipids in the early developmental stages of experimental immune diabetes induced by multiple low-dose streptozotocin. J Appl Physiol 98:1064-1069.
68. Rabinovitch A, Suarez-Pinzon WL. 1998. Cytokines and their roles in pancreatic islet beta-cell destruction and insulin-dependent diabetes mellitus. Biochem Pharmacol 55:1139-1149.
69. Rachmiel M, Bloch O, Bistritzer T, Weintrob N, Ofan R, Koren-Morag N, Rapoport MJ. 2006. TH1/TH2 cytokine balance in patients with both type 1 diabetes mellitus and asthma. Cytokine 34:170-176.
70. Rodriguiz RM, Key LL, Jr., Ries WL. 1993. Combination macrophage-colony stimulating factor and interferon-gamma administration ameliorates the osteopetrotic condition in microphthalmic (mi/mi) mice. Pediatr Res 33:384-389.
71. Schwab AM, Granholm S, Persson E, Wilkes B, Lerner UH, Conaway HH. 2005. Stimulation of resorption in cultured mouse calvarial bones by thiazolidinediones. Endocrinology 146:4349-4361.
72. Schwartz AV, Sellmeyer DE, Ensrud KE, Cauley JA, Tabor HK, Schreiner PJ, Jamal SA, Black DM, Cummings SR. 2001. Older women with diabetes have an increased risk of fracture: A prospective study. J Clin Endocrinol Metab 86:32-38.
73. Smith DD, Gowen M, Mundy GR. 1987. Effects of interferon-gamma and other cytokines on collagen synthesis in fetal rat bone cultures. Endocrinology 120:2494-2499.
74. Solomon SS, Heckemeyer CM, Barker JA, Duckworth WC. 1985. Hormonal control of lipolysis in perifused adipocytes from diabetic rats. Endocrinology 117:1350-1354.
75. Szkudelski T. 2001. The mechanism of alloxan and streptozotocin action in B cells of the rat pancreas. Physiol Res 50:537-546.
76. Takayanagi H. 2005. Mechanistic insight into osteoclast differentiation in osteoimmunology. J Mol Med 83:170-179.
77. Takayanagi H, Ogasawara K, Hida S, Chiba T, Murata S, Sato K, Takaoka A, Yokochi T, Oda H, Tanaka K, Nakamura K, Taniguchi T. 2000. T-cell-mediated regulation of osteoclastogenesis by signalling cross-talk between RANKL and IFN-gamma. Nature 408:600-605.
78. Takayanagi H, Sato K, Takaoka A, Taniguchi T. 2005. Interplay between interferon and other cytokine systems in bone metabolism. Immunol Rev 208:181-193.
79. Takeshita N, Ishida H, Yamamoto T, Koh G, Kurose T, Tsuji K, Okamoto Y, Ikeda H, Seino Y. 1993. 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.
80. 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. 2005. Bone formation is impaired in a model of type 1 diabetes. Diabetes 54:2875-2881.
81. Togari A, Arai M, Mogi M, Kondo A, Nagatsu T. 1998. Coexpression of GTP cyclohydrolase I and inducible nitric oxide synthase mRNAs in mouse osteoblastic cells activated by proinflammatory cytokines. FEBS Lett 428:212-216.
82. Trogan E, Choudhury RP, Dansky HM, Rong JX, Breslow JL, Fisher EA. 2002. Laser capture microdissection analysis of gene expression in macrophages from atherosclerotic lesions of apolipoprotein E-deficient mice. Proc Natl Acad Sci USA 99:2234-2239.
83. Tuominen JT, Impivaara O, Puukka P, Ronnemaa T. 1999. Bone mineral density in patients with type 1 and type 2 diabetes. Diabetes Care 22:1196-1200.
84. Valcourt U, Merle B, Gineyts E, Viguet-Carrin S, Delmas PD, Garnero P. 2007. Non-enzymatic glycation of bone collagen modifies osteoclastic activity and differentiation. J Biol Chem 282:5691-5703.
85. Valerio G, del Puente A, Esposito-del Puente A, Buono P, Mozzillo E, Franzese A. 2002. The lumbar bone mineral density is affected by long-term poor metabolic control in adolescents with type 1 diabetes mellitus. Horm Res 58:266-272.
86. Vengellur A, LaPres JJ. 2004. The role of hypoxia inducible factor 1alpha in cobalt chloride induced cell death in mouse embryonic fibroblasts. Toxicol Sci 82:638-646.
87. Verhaeghe J, Suiker AM, Nyomba BL, Visser WJ, Einhorn TA, Dequeker J, Bouillon R. 1989. Bone mineral homeostasis in spontaneously diabetic BB rats. II. Impaired bone turnover and decreased osteocalcin synthesis. Endocrinology 124:573-582.
88. Verhaeghe J, van Herck E, Visser WJ, Suiker AM, Thomasset M, Einhorn TA, Faierman E, Bouillon R. 1990. Bone and mineral metabolism in BB rats with long-term diabetes. Decreased bone turnover and osteoporosis. Diabetes 39:477-482.
89. Verhaeghe J, Oloumi G, van Herck E, van Bree R, Dequeker J, Einhorn TA, Bouillon R. 1997. Effects of long-term diabetes and/or high-dose 17 beta-estradiol on bone formation, bone mineral density, and strength in ovariectomized rats. Bone 20:421-428.
90. Verhaeghe J, Thomsen JS, van Bree R, van Herck E, Bouillon R, Mosekilde L. 2000. Effects of exercise and disuse on bone remodeling, bone mass, and biomechanical competence in spontaneously diabetic female rats. Bone 27:249-256.
91. Wang Z, Gleichmann H. 1998. GLUT2 in pancreatic islets: Crucial target molecule in diabetes induced with multiple low doses of streptozotocin in mice. Diabetes 47:50-56.
92. Waud CE, Marks SC, Jr., Lew R, Baran DT. 1994. Bone mineral density in the femur and lumbar vertebrae decreases after twelve weeks of diabetes in spontaneously diabetic-prone BB/Worcester rats. Calcif Tissue Int 54:237-240.
93. Weghofer M, Karlic H, Haslberger A. 2001. Quantitative analysis of immune-mediated stimulation of tumor necrosis factor-alpha in macrophages measured at the level of mRNA and protein synthesis. Ann Hematol 80:733-736.
94. Weih DS, Yilmaz ZB, Weih F. 2001. Essential role of RelB in germinal center and marginal zone formation and proper expression of homing chemokines. J Immunol 167:1909-1919.
95. Wen Y, Gu J, Li SL, Reddy MA, Natarajan R, Nadler JL. 2006. Elevated glucose and diabetes promote interleukin-12 cytokine gene expression in mouse macrophages. Endocrinology 147:2518-2525.
96. West E, Simon OR, Morrison EY. 1996. Streptozotocin alters pancreatic beta-cell responsiveness to glucose within six hours of injection into rats. West Indian Med J 45:60-62.
97. Wiren KM, Zhang XW, Toombs AR, Kasparcova V, Gentile MA, Harada S, Jepsen KJ. 2004. Targeted overexpression of androgen receptor in osteoblasts: Unexpected complex bone phenotype in growing animals. Endocrinology 145:3507-3522.
98. Wittrant Y, Gorin Y, Woodruff K, Horn D, Abboud HE, Mohan S, Abboud-Werner SL. 2008. High d(+)glucose concentration inhibits RANKL-induced osteoclastogenesis. Bone 42:1122-1130.
99. Yang XD, Tisch R, Singer SM, Cao ZA, Liblau RS, Schreiber RD, McDevitt HO. 1994. Effect of tumor necrosis factor alpha on insulin-dependent diabetes mellitus in NOD mice. I. The early development of autoimmunity and the diabetogenic process. J Exp Med 180:995-1004.
100. Yoon JW, Reddi AH. 1984. Decreased bone formation and mineralization in virus-induced diabetes mellitus. Am J Physiol 246:C177-C179.
101. Young N, Mikhalkevich N, Yan Y, Chen D, Zheng WP. 2005. Differential regulation of osteoblast activity by Th cell subsets mediated by parathyroid hormone and IFN-gamma. J Immunol 175:8287-8295.
102. Zhao S, Zhang YK, Harris S, Ahuja SS, Bonewald LF. 2002. MLO-Y4 osteocyte-like cells support osteoclast formation and activation. J Bone Miner Res 17:2068-2079.
103. Zhou FH, Foster BK, Zhou XF, Cowin AJ, Xian CJ. 2006. TNF-alpha mediates p38 MAP kinase activation and negatively regulates bone formation at the injured growth plate in rats. J Bone Miner Res 21:1075-1088.