FoxOs, Wnts and oxidative stress-induced bone loss: New players in the periodontitis arena?

Journal of Periodontal Research

Volumn 46, Issue 4, 2011, Pages 397-406

  Galli, C ^a,b   Passeri, G ^a   Macaluso, G M ^b  

^a Department of Internal Medicine ^*  (Italy)

^b UNIVERSITY OF PARMA   (Italy)

Author keywords

FoxO; Oxidative stress; Periodontal disease; Wnt

Indexed keywords

BETA CATENIN; FORKHEAD TRANSCRIPTION FACTOR; PROTEIN KINASE B; REACTIVE OXYGEN METABOLITE; WNT PROTEIN;

ALVEOLAR BONE LOSS; CHRONIC PERIODONTITIS; HUMAN; LIPID PEROXIDATION; METABOLISM; OXIDATIVE STRESS; PHYSIOLOGY; SHORT SURVEY;

ALVEOLAR BONE LOSS; BETA CATENIN; CHRONIC PERIODONTITIS; FORKHEAD TRANSCRIPTION FACTORS; HUMANS; LIPID PEROXIDATION; OXIDATIVE STRESS; PROTO-ONCOGENE PROTEINS C-AKT; REACTIVE OXYGEN SPECIES; WNT PROTEINS;

EID: 79959622157     PISSN: 00223484     EISSN: 16000765     Source Type: Journal    
DOI: 10.1111/j.1600-0765.2011.01354.x     Document Type: Short Survey

References (154)

1. Liu R, Bal HS, Desta T et al. Diabetes enhances periodontal bone loss through enhanced resorption and diminished bone formation. J Dent Res 2006;85:510-514.
2. Nishimura F, Taniguchi A, Yamaguchi-Morimoto M et al. Periodontal infection and dyslipidemia in type 2 diabetics: association with increased HMG-CoA reductase expression. Horm Metab Res 2006;38:530-535.
3. Bullon P, Morillo JM, Ramirez-Tortosa MC, Quiles JL, Newman HN, Battino M. Metabolic syndrome and periodontitis: is oxidative stress a common link? J Dent Res 2009;88:503-518.
4. Chen L, Wei B, Li J et al. Association of periodontal parameters with metabolic level and systemic inflammatory markers in patients with type 2 diabetes. J Periodontol 2010;81:364-371.
5. Li P, He L, Sha YQ, Luan QX. Relationship of metabolic syndrome to chronic periodontitis. J Periodontol 2009;80:541-549.
6. D'Aiuto F, Sabbah W, Netuveli G et al. Association of the metabolic syndrome with severe periodontitis in a large U.S. population-based survey. J Clin Endocrinol Metab 2008;93:3989-3994.
7. Shimazaki Y, Saito T, Yonemoto K, Kiyohara Y, Iida M, Yamashita Y. Relationship of metabolic syndrome to periodontal disease in Japanese women: the Hisayama Study. J Dent Res 2007;86:271-275.
8. Nishimura F, Murayama Y. Periodontal inflammation and insulin resistance - lessons from obesity. J Dent Res 2001;80:1690-1694.
9. Mealey BL, Ocampo GL. Diabetes mellitus and periodontal disease. Periodontol 2000 2007;44:127-153.
10. Graves DT, Liu R, Oates TW. Diabetes-enhanced inflammation and apoptosis: impact on periodontal pathosis. Periodontol 2000 2007;45:128-137.
11. Huttner EA, Machado DC, de Oliveira RB, Antunes AG, Hebling E. Effects of human aging on periodontal tissues. Spec Care Dentist 2009;29:149-155.
12. Arai K, Tanaka S, Yamamoto-Sawamura T, Sone K, Miyaishi O, Sumi Y. Aging changes in the periodontal bone of F344/N rat. Arch Gerontol Geriatr 2005;40:225-229.
13. Streckfus CF, Parsell DE, Streckfus JE, Pennington W, Johnson RB. Relationship between oral alveolar bone loss and aging among African-American and Caucasian individuals. Gerontology 1999;45:110-114.
14. Ritchie CS. Mechanistic links between type 2 diabetes and periodontitis. J Dent 2009;37:S578-S579.
15. Chapple IL. Reactive oxygen species and antioxidants in inflammatory diseases. J Clin Periodontol 1997;24:287-296.
16. Chapple IL. Role of free radicals and antioxidants in the pathogenesis of the inflammatory periodontal diseases. Clin Mol Pathol 1996;49:M247-M255.
17. Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J. Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 2007;39:44-84.
18. Battino M, Bullon P, Wilson M, Newman H. Oxidative injury and inflammatory periodontal diseases: the challenge of anti-oxidants to free radicals and reactive oxygen species. Crit Rev Oral Biol Med 1999;10:458-476.
19. Halliwell B. Mechanisms involved in the generation of free radicals. Pathol Biol (Paris) 1996;44:6-13.
20. Sies H. Biochemistry of oxidative stress. Angew Chem Int Ed Engl 1986; 25: 1058-1071.
21. Halliwell B, Gutteridge JM. Free radicals and antioxidant protection: mechanisms and significance in toxicology and disease. Hum Toxicol 1988;7:7-13.
22. Halliwell B, Gutteridge JM. Role of free radicals and catalytic metal ions in human disease: an overview. Methods Enzymol 1990;186:1-85.
23. Janssen-Heininger YM, Mossman BT, Heintz NH et al. Redox-based regulation of signal transduction: principles, pitfalls, and promises. Free Radic Biol Med 2008;45:1-17.
24. Zhang DX, Gutterman DD. Mitochondrial reactive oxygen species-mediated signaling in endothelial cells. Am J Physiol Heart Circ Physiol 2007;292:H2023-H2031.
25. Sedelnikova OA, Redon CE, Dickey JS, Nakamura AJ, Georgakilas AG, Bonner WM. Role of oxidatively induced DNA lesions in human pathogenesis. Mutat Res 2010;704:152-159.
26. Cataldi A, Di Giulio C. "Oxygen supply" as modulator of aging processes: hypoxia and hyperoxia models for aging studies. Curr Aging Sci 2009;2:95-102.
27. Steinboeck F, Hubmann M, Bogusch A, Dorninger P, Lengheimer T, Heidenreich E. The relevance of oxidative stress and cytotoxic DNA lesions for spontaneous mutagenesis in non-replicating yeast cells. Mutat Res 2010;688:47-52.
28. Rossi P, Marzani B, Giardina S, Negro M, Marzatico F. Human skeletal muscle aging and the oxidative system: cellular events. Curr Aging Sci 2008;1:182-191.
29. Quarrie JK, Riabowol KT. Murine models of life span extension. Sci Aging Knowledge Environ 2004; 2004: re5.
30. Chapple IL, Brock GR, Milward MR, Ling N, Matthews JB. Compromised GCF total antioxidant capacity in periodontitis: cause or effect? J Clin Periodontol 2007;34:103-110.
31. Toker H, Ozdemir H, Eren K, Ozer H, Sahin G. N-acetylcysteine, a thiol antioxidant, decreases alveolar bone loss in experimental periodontitis in rats. J Periodontol 2009;80:672-678.
32. Matthews JB, Wright HJ, Roberts A, Ling-Mountford N, Cooper PR, Chapple IL. Neutrophil hyper-responsiveness in periodontitis. J Dent Res 2007;86:718-722.
33. Sheikhi M, Bouhafs RK, Hammarstrom KJ, Jarstrand C. Lipid peroxidation caused by oxygen radicals from Fusobacterium-stimulated neutrophils as a possible model for the emergence of periodontitis. Oral Dis 2001;7:41-46.
34. Sheikhi M, Gustafsson A, Jarstrand C. Cytokine, elastase and oxygen radical release by Fusobacterium nucleatum-activated leukocytes: a possible pathogenic factor in periodontitis. J Clin Periodontol 2000;27:758-762.
35. Keely S, Glover LE, MacManus CF et al. Selective induction of integrin beta1 by hypoxia-inducible factor: implications for wound healing. FASEB J 2009;23:1338-1346.
36. Rehman A, Nourooz-Zadeh J, Moller W, Tritschler H, Pereira P, Halliwell B. Increased oxidative damage to all DNA bases in patients with type II diabetes mellitus. FEBS Lett 1999;448:120-122.
37. Chapple IL, Brock G, Eftimiadi C, Matthews JB. Glutathione in gingival crevicular fluid and its relation to local antioxidant capacity in periodontal health and disease. Mol Pathol 2002;55:367-373.
38. Waddington RJ, Moseley R, Embery G. Reactive oxygen species: a potential role in the pathogenesis of periodontal diseases. Oral Dis 2000;6:138-151.
39. Chapple IL, Matthews JB. The role of reactive oxygen and antioxidant species in periodontal tissue destruction. Periodontol 2000 2007;43:160-232.
40. D'Aiuto F, Nibali L, Parkar M, Patel K, Suvan J, Donos N. Oxidative stress, systemic inflammation, and severe periodontitis. J Dent Res 2010;89:1241-1246.
41. Brock GR, Butterworth CJ, Matthews JB, Chapple IL. Local and systemic total antioxidant capacity in periodontitis and health. J Clin Periodontol 2004;31:515-521.
42. Tamaki N, Tomofuji T, Ekuni D, Yamanaka R, Morita M. Periodontal treatment decreases plasma oxidized LDL level and oxidative stress. Clin Oral Investig 2010. [Epub ahead of print].
43. Abou Sulaiman AE, Shehadeh RM. Assessment of total antioxidant capacity and the use of vitamin C in the treatment of non-smokers with chronic periodontitis. J Periodontol 2010;81:1547-1554.
44. Wei D, Zhang XL, Wang YZ, Yang CX, Chen G. Lipid peroxidation levels, total oxidant status and superoxide dismutase in serum, saliva and gingival crevicular fluid in chronic periodontitis patients before and after periodontal therapy. Aust Dent J 2010;55:70-78.
45. Grant MM, Brock GR, Matthews JB, Chapple IL. Crevicular fluid glutathione levels in periodontitis and the effect of non-surgical therapy. J Clin Periodontol 2010;37:17-23.
46. Linden GJ, McClean KM, Woodside JV et al. Antioxidants and periodontitis in 60-70-year-old men. J Clin Periodontol 2009;36:843-849.
47. Chapple IL, Milward MR, Dietrich T. The prevalence of inflammatory periodontitis is negatively associated with serum antioxidant concentrations. J Nutr 2007;137:657-664.
48. Patel SP, Pradeep AR, Chowdhry S. Crevicular fluid levels of plasma glutathione peroxidase (eGPx) in periodontal health and disease. Arch Oral Biol 2009;54:543-548.
49. Liskmann S, Vihalemm T, Salum O, Zilmer K, Fischer K, Zilmer M. Characterization of the antioxidant profile of human saliva in peri-implant health and disease. Clin Oral Implants Res 2007;18:27-33.
50. Manolagas SC. From estrogen-centric to aging and oxidative stress: a revised perspective of the pathogenesis of osteoporosis. Endocr Rev 2010;31:266-300.
51. Almeida M, Ambrogini E, Han L, Manolagas SC, Jilka RL. Increased lipid oxidation causes oxidative stress, increased peroxisome proliferator-activated receptor-gamma expression, and diminished pro-osteogenic Wnt signaling in the skeleton. J Biol Chem 2009;284:27438-27448.
52. Almeida M, Han L, Martin-Millan M, O'Brien CA, Manolagas SC. Oxidative stress antagonizes Wnt signaling in osteoblast precursors by diverting beta-catenin from T cell factor- to forkhead box O-mediated transcription. J Biol Chem 2007;282:27298-27305.
53. Manolagas SC, Almeida M. Gone with the Wnts: beta-catenin, T-cell factor, forkhead box O, and oxidative stress in age-dependent diseases of bone, lipid, and glucose metabolism. Mol Endocrinol 2007;21:2605-2614.
54. Jagger CJ, Lean JM, Davies JT, Chambers TJ. Tumor necrosis factor-alpha mediates osteopenia caused by depletion of antioxidants. Endocrinology 2005;146:113-118.
55. Lean JM, Davies JT, Fuller K et al. A crucial role for thiol antioxidants in estrogen-deficiency bone loss. J Clin Invest 2003;112:915-923.
56. Tomofuji T, Ekuni D, Irie K et al. Preventive effects of a cocoa-enriched diet on gingival oxidative stress in experimental periodontitis. J Periodontol 2009;80:1799-1808.
57. Halliwell B. Antioxidant defence mechanisms: from the beginning to the end (of the beginning). Free Radic Res 1999;31:261-272.
58. Barthel A, Schmoll D, Unterman TG. FoxO proteins in insulin action and metabolism. Trends Endocrinol Metab 2005;16:183-189.
59. Kaestner KH, Knochel W, Martinez DE. Unified nomenclature for the winged helix/forkhead transcription factors. Genes Dev 2000;14:142-146.
60. Greer EL, Brunet A. FOXO transcription factors at the interface between longevity and tumor suppression. Oncogene 2005;24:7410-7425.
61. Brunet A, Bonni A, Zigmond MJ et al. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 1999;96:857-868.
62. Huang H, Tindall DJ. Dynamic FoxO transcription factors. J Cell Sci 2007;120:2479-2487.
63. Biggs WH 3rd, Meisenhelder J, Hunter T, Cavenee WK, Arden KC. Protein kinase B/Akt-mediated phosphorylation promotes nuclear exclusion of the winged helix transcription factor FKHR1. Proc Natl Acad Sci USA 1999;96:7421-7426.
64. Furuyama T, Nakazawa T, Nakano I, Mori N. Identification of the differential distribution patterns of mRNAs and consensus binding sequences for mouse DAF-16 homologues. Biochem J 2000;349:629-634.
65. Gilley J, Coffer PJ, Ham J. FOXO transcription factors directly activate bim gene expression and promote apoptosis in sympathetic neurons. J Cell Biol 2003;162:613-622.
66. Dijkers PF, Medema RH, Lammers JW, Koenderman L, Coffer PJ. Expression of the pro-apoptotic Bcl-2 family member Bim is regulated by the forkhead transcription factor FKHR-L1. Curr Biol 2000;10:1201-1204.
67. Nakamura T, Sakamoto K. Forkhead transcription factor FOXO subfamily is essential for reactive oxygen species-induced apoptosis. Mol Cell Endocrinol 2008;281:47-55.
68. Kops GJ, Dansen TB, Polderman PE et al. Forkhead transcription factor FOXO3a protects quiescent cells from oxidative stress. Nature 2002;419:316-321.
69. Martinez-Gac L, Marques M, Garcia Z, Campanero MR, Carrera AC. Control of cyclin G2 mRNA expression by forkhead transcription factors: novel mechanism for cell cycle control by phosphoinositide 3-kinase and forkhead. Mol Cell Biol 2004;24:2181-2189.
70. Seoane J, Le HV, Shen L, Anderson SA, Massague J. Integration of Smad and forkhead pathways in the control of neuroepithelial and glioblastoma cell proliferation. Cell 2004;117:211-223.
71. Nakamura N, Ramaswamy S, Vazquez F, Signoretti S, Loda M, Sellers WR. Forkhead transcription factors are critical effectors of cell death and cell cycle arrest downstream of PTEN. Mol Cell Biol 2000;20:8969-8982.
72. Kops GJ, Medema RH, Glassford J et al. Control of cell cycle exit and entry by protein kinase B-regulated forkhead transcription factors. Mol Cell Biol 2002;22:2025-2036.
73. Ramaswamy S, Nakamura N, Sansal I, Bergeron L, Sellers WR. A novel mechanism of gene regulation and tumor suppression by the transcription factor FKHR. Cancer Cell 2002;2:81-91.
74. Schmidt M, Fernandez de Mattos S, van der Horst A et al. Cell cycle inhibition by FoxO forkhead transcription factors involves downregulation of cyclin D. Mol Cell Biol 2002;22:7842-7852.
75. Modur V, Nagarajan R, Evers BM, Milbrandt J. FOXO proteins regulate tumor necrosis factor-related apoptosis inducing ligand expression. Implications for PTEN mutation in prostate cancer. J Biol Chem 2002;277:47928-47937.
76. Nemoto S, Finkel T. Redox regulation of forkhead proteins through a p66shc-dependent signaling pathway. Science 2002;295:2450-2452.
77. Tran H, Brunet A, Grenier JM et al. DNA repair pathway stimulated by the forkhead transcription factor FOXO3a through the Gadd45 protein. Science 2002;296:530-534.
78. Tothova Z, Kollipara R, Huntly BJ et al. FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell 2007;128:325-339.
79. Vogt PK, Jiang H, Aoki M. Triple layer control: phosphorylation, acetylation and ubiquitination of FOXO proteins. Cell Cycle 2005;4:908-913.
80. Yang Y, Hou H, Haller EM, Nicosia SV, Bai W. Suppression of FOXO1 activity by FHL2 through SIRT1-mediated deacetylation. EMBO J 2005;24:1021-1032.
81. Brunet A, Sweeney LB, Sturgill JF et al. Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 2004;303:2011-2015.
82. Lam EW, Francis RE, Petkovic M. FOXO transcription factors: key regulators of cell fate. Biochem Soc Trans 2006;34:722-726.
83. Furuyama T, Kitayama K, Shimoda Y et al. Abnormal angiogenesis in Foxo1 (Fkhr)-deficient mice. J Biol Chem 2004;279:34741-34749.
84. Hosaka T, Biggs WH 3rd, Tieu D et al. Disruption of forkhead transcription factor (FOXO) family members in mice reveals their functional diversification. Proc Natl Acad Sci USA 2004;101:2975-2980.
85. Castrillon DH, Miao L, Kollipara R, Horner JW, DePinho RA. Suppression of ovarian follicle activation in mice by the transcription factor Foxo3a. Science 2003;301:215-218.
86. Lin L, Hron JD, Peng SL. Regulation of NF-kappaB, Th activation, and autoinflammation by the forkhead transcription factor Foxo3a. Immunity 2004;21:203-213.
87. Rached MT, Kode A, Xu L et al. FoxO1 is a positive regulator of bone formation by favoring protein synthesis and resistance to oxidative stress in osteoblasts. Cell Metab 2010;11:147-160.
88. Ambrogini E, Almeida M, Martin-Millan M et al. FoxO-mediated defense against oxidative stress in osteoblasts is indispensable for skeletal homeostasis in mice. Cell Metab 2010;11:136-146.
89. Kandel ES, Hay N. The regulation and activities of the multifunctional serine/threonine kinase Akt/PKB. Exp Cell Res 1999;253:210-229.
90. Lawlor MA, Alessi DR. PKB/Akt: a key mediator of cell proliferation, survival and insulin responses? J Cell Sci 2001;114:2903-2910.
91. Cantley LC. The phosphoinositide 3-kinase pathway. Science 2002;296:1655-1657.
92. Jiang BH, Liu LZ. PI3K/PTEN signaling in tumorigenesis and angiogenesis. Biochim Biophys Acta 2008;1784:150-158.
93. Nogueira V, Park Y, Chen CC et al. Akt determines replicative senescence and oxidative or oncogenic premature senescence and sensitizes cells to oxidative apoptosis. Cancer Cell 2008;14:458-470.
94. Korkaya H, Paulson A, Charafe-Jauffret E et al. Regulation of mammary stem/progenitor cells by PTEN/Akt/beta-catenin signaling. PLoS Biol 2009;7:e1000121.
95. Kandel ES, Skeen J, Majewski N et al. Activation of Akt/protein kinase B overcomes a G(2)/m cell cycle checkpoint induced by DNA damage. Mol Cell Biol 2002;22:7831-7841.
96. Nakae J, Biggs WH 3rd, Kitamura T et al. Regulation of insulin action and pancreatic beta-cell function by mutated alleles of the gene encoding forkhead transcription factor Foxo1. Nat Genet 2002;32:245-253.
97. Kushner JA, Simpson L, Wartschow LM et al. Phosphatase and tensin homolog regulation of islet growth and glucose homeostasis. J Biol Chem 2005;280:39388-39393.
98. Kaneto H, Kajimoto Y, Miyagawa J et al. Beneficial effects of antioxidants in diabetes: possible protection of pancreatic beta-cells against glucose toxicity. Diabetes 1999;48:2398-2406.
99. Tanaka Y, Gleason CE, Tran PO, Harmon JS, Robertson RP. Prevention of glucose toxicity in HIT-T15 cells and Zucker diabetic fatty rats by antioxidants. Proc Natl Acad Sci USA 1999;96:10857-10862.
100. Yang H, Roberts LJ, Shi MJ et al. Retardation of atherosclerosis by overexpression of catalase or both Cu/Zn-superoxide dismutase and catalase in mice lacking apolipoprotein E. Circ Res 2004;95:1075-1081.
101. Menini S, Amadio L, Oddi G et al. Deletion of p66Shc longevity gene protects against experimental diabetic glomerulopathy by preventing diabetes-induced oxidative stress. Diabetes 2006;55:1642-1650.
102. Kamei Y, Miura S, Suzuki M et al. Skeletal muscle FOXO1 (FKHR) transgenic mice have less skeletal muscle mass, down-regulated Type I (slow twitch/red muscle) fiber genes, and impaired glycemic control. J Biol Chem 2004;279:41114-41123.
103. Yang-Snyder J, Miller JR, Brown JD, Lai CJ, Moon RT. A frizzled homolog functions in a vertebrate Wnt signaling pathway. Curr Biol 1996;6:1302-1306.
104. Moon RT, Brown JD, Yang-Snyder JA, Miller JR. Structurally related receptors and antagonists compete for secreted Wnt ligands. Cell 1997;88:725-728.
105. van Amerongen R, Mikels A, Nusse R. Alternative wnt signaling is initiated by distinct receptors. Sci Signal 2008;1:re9.
106. Hartmann C. A Wnt canon orchestrating osteoblastogenesis. Trends Cell Biol 2006;16:151-158.
107. Mikels AJ, Nusse R. Purified Wnt5a protein activates or inhibits beta-catenin-TCF signaling depending on receptor context. PLoS Biol 2006;4:e115.
108. Gordon MD, Nusse R. Wnt signaling: multiple pathways, multiple receptors, and multiple transcription factors. J Biol Chem 2006;281:22429-22433.
109. Angers S, Moon RT. Proximal events in Wnt signal transduction. Nat Rev Mol Cell Biol 2009;10:468-477.
110. Clevers H. Wnt/beta-catenin signaling in development and disease. Cell 2006;127:469-480.
111. Verheyen EM, Gottardi CJ. Regulation of Wnt/beta-catenin signaling by protein kinases. Dev Dyn 2009;239:34-44.
112. Mosimann C, Hausmann G, Basler K. Beta-catenin hits chromatin: regulation of Wnt target gene activation. Nat Rev Mol Cell Biol 2009;10:276-286.
113. Tutter AV, Fryer CJ, Jones KA. Chromatin-specific regulation of LEF-1-beta-catenin transcription activation and inhibition in vitro. Genes Dev 2001;15:3342-3354.
114. Huelsken J, Vogel R, Brinkmann V, Erdmann B, Birchmeier C, Birchmeier W. Requirement for beta-catenin in anterior-posterior axis formation in mice. J Cell Biol 2000;148:567-578.
115. Martin BL, Kimelman D. Wnt signaling and the evolution of embryonic posterior development. Curr Biol 2009;19:R215-R219.
116. Nusse R. Wnt signaling and stem cell control. Cell Res 2008;18:523-527.
117. Rodda SJ, McMahon AP. Distinct roles for Hedgehog and canonical Wnt signaling in specification, differentiation and maintenance of osteoblast progenitors. Development 2006;133:3231-3244.
118. Krishnan V, Bryant HU, Macdougald OA. Regulation of bone mass by Wnt signaling. J Clin Invest 2006;116:1202-1209.
119. Balemans W, Ebeling M, Patel N et al. Increased bone density in sclerosteosis is due to the deficiency of a novel secreted protein (SOST). Hum Mol Genet 2001;10:537-543.
120. Brunkow ME, Gardner JC, Van Ness J et al. Bone dysplasia sclerosteosis results from loss of the SOST gene product, a novel cystine knot-containing protein. Am J Hum Genet 2001;68:577-589.
121. van Bezooijen RL, Bronckers AL, Gortzak RA et al. Sclerostin in mineralized matrices and van Buchem disease. J Dent Res 2009;88:569-574.
122. Wan M, Yang C, Li J et al. Parathyroid hormone signaling through low-density lipoprotein-related protein 6. Genes Dev 2008;22:2968-2979.
123. Glass DA 2nd, Bialek P, Ahn JD et al. Canonical Wnt signaling in differentiated osteoblasts controls osteoclast differentiation. Dev Cell 2005;8:751-764.
124. Allard D, Figg N, Bennett MR, Littlewood TD. Akt regulates the survival of vascular smooth muscle cells via inhibition of FoxO3a and GSK3. J Biol Chem 2008;283:19739-19747.
125. Rokutanda S, Fujita T, Kanatani N et al. Akt regulates skeletal development through GSK3, mTOR, and FoxOs. Dev Biol 2009;328:78-93.
126. Hoogeboom D, Burgering BM. Should I stay or should I go: beta-catenin decides under stress. Biochim Biophys Acta 2009;1796:63-74.
127. Hoogeboom D, Essers MA, Polderman PE, Voets E, Smits LM, Burgering BM. Interaction of FOXO with beta-catenin inhibits beta-catenin/T cell factor activity. J Biol Chem 2008;283:9224-9230.
128. Essers MA, Weijzen S, de Vries-Smits AM et al. FOXO transcription factor activation by oxidative stress mediated by the small GTPase Ral and JNK. EMBO J 2004;23:4802-4812.
129. Ishitani T, Ninomiya-Tsuji J, Nagai S et al. The TAK1-NLK-MAPK-related pathway antagonizes signalling between beta-catenin and transcription factor TCF. Nature 1999;399:798-802.
130. Lu H, Kraut D, Gerstenfeld LC, Graves DT. Diabetes interferes with the bone formation by affecting the expression of transcription factors that regulate osteoblast differentiation. Endocrinology 2003;144:346-352.
131. 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.
132. 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.
133. Kuhn H, Borchert A. Regulation of enzymatic lipid peroxidation: the interplay of peroxidizing and peroxide reducing enzymes. Free Radic Biol Med 2002;33:154-172.
134. Lee JY, Jung GY, Heo HJ et al. 4-Hydroxynonenal induces vascular smooth muscle cell apoptosis through mitochondrial generation of reactive oxygen species. Toxicol Lett 2006;166:212-221.
135. Klein RF, Allard J, Avnur Z et al. Regulation of bone mass in mice by the lipoxygenase gene Alox15. Science 2004;303:229-232.
136. Akune T, Ohba S, Kamekura S et al. PPARgamma insufficiency enhances osteogenesis through osteoblast formation from bone marrow progenitors. J Clin Invest 2004;113:846-855.
137. 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;143:2376-2384.
138. Soroceanu MA, Miao D, Bai XY, Su H, Goltzman D, Karaplis AC. Rosiglitazone impacts negatively on bone by promoting osteoblast/osteocyte apoptosis. J Endocrinol 2004;183:203-216.
139. Ali AA, Weinstein RS, Stewart SA, Parfitt AM, Manolagas SC, Jilka RL. Rosiglitazone causes bone loss in mice by suppressing osteoblast differentiation and bone formation. Endocrinology 2005;146:1226-1235.
140. Garrett IR, Boyce BF, Oreffo RO, Bonewald L, Poser J, Mundy GR. Oxygen-derived free radicals stimulate osteoclastic bone resorption in rodent bone in vitro and in vivo. J Clin Invest 1990;85:632-639.
141. Bai XC, Lu D, Liu AL et al. Reactive oxygen species stimulates receptor activator of NF-kappaB ligand expression in osteoblast. J Biol Chem 2005;280:17497-17506.
142. Lean JM, Jagger CJ, Kirstein B, Fuller K, Chambers TJ. Hydrogen peroxide is essential for estrogen-deficiency bone loss and osteoclast formation. Endocrinology 2005;146:728-735.
143. Lee NK, Choi YG, Baik JY et al. A crucial role for reactive oxygen species in RANKL-induced osteoclast differentiation. Blood 2005;106:852-859.
144. Kim MS, Yang YM, Son A et al. RANKL-mediated reactive oxygen species pathway that induces long lasting Ca2+ oscillations essential for osteoclastogenesis. J Biol Chem 2010;285:6913-6921.
145. Srinivasan S, Avadhani NG. Hypoxia-mediated mitochondrial stress in RAW264.7 cells induces osteoclast-like TRAP-positive cells. Ann N Y Acad Sci 2007;1117:51-61.
146. Koh JM, Lee YS, Kim YS et al. Homocysteine enhances bone resorption by stimulation of osteoclast formation and activity through increased intracellular ROS generation. J Bone Miner Res 2006;21:1003-1011.
147. Almeida M, Martin-Millan M, Ambrogini E et al. Estrogens attenuate oxidative stress and the differentiation and apoptosis of osteoblasts by dna binding-independent actions of the ER alpha. J Bone Miner Res 2010;25:769-781.
148. Almeida M, Han L, Ambrogini E, Bartell SM, Manolagas SC. Oxidative stress stimulates apoptosis and activates NF-kappaB in osteoblastic cells via a PKCbeta/p66shc signaling cascade: counter regulation by estrogens or androgens. Mol Endocrinol 2010;24:2030-2037.
149. Jilka RL, Almeida M, Ambrogini E et al. Decreased oxidative stress and greater bone anabolism in the aged, when compared to the young, murine skeleton with parathyroid hormone administration. Aging Cell 2010;9:851-867.
150. Maruyama T, Tomofuji T, Endo Y et al. Supplementation of green tea catechins in dentifrices suppresses gingival oxidative stress and periodontal inflammation. Arch Oral Biol 2011;56:48-53.
151. Govindaraj J, Emmadi P, Deepalakshmi, Rajaram V, Prakash G, Puvanakrishnan R. Protective effect of proanthocyanidins on endotoxin induced experimental periodontitis in rats. Indian J Exp Biol 2010;48:133-142.
152. Tomofuji T, Ekuni D, Sanbe T et al. Effects of vitamin C intake on gingival oxidative stress in rat periodontitis. Free Radic Biol Med 2009;46:163-168.
153. Khmelevskii IuV, Danilevskii NF, Borisenko AV, Poberezkina NV. [Effect of vitamins A, E and K on the indices of the glutathione antiperoxide system in gingival tissues in periodontosis]. Vopr Pitan 1985;4:54-56.
154. Hirasawa M, Takada K, Makimura M, Otake S. Improvement of periodontal status by green tea catechin using a local delivery system: a clinical pilot study. J Periodontal Res 2002;37:433-438.