Reactive oxygen species and oxidative stress in osteoclastogenesis, skeletal aging and bone diseases

Springer Science and Business Media LLC - Tập 33 Số 4 - Trang 359-370 - 2015
Danielle Callaway1, Jean X. Jiang1
1Department of Biochemistry, University of Texas Health Science Center, San Antonio, USA

Tóm tắt

Từ khóa


Tài liệu tham khảo

Wauquier F, Leotoing L, Coxam V, Guicheux J, Wittrant Y (2009) Oxidative stress in bone remodelling and disease. Trends Mol Med 15:468–477

Vaananen HK, Zhao H, Mulari M, Halleen JM (2000) The cell biology of osteoclast function. J Cell Sci 113:377–381

Boyle W, Simonet W, Lacey DL (2003) Osteoclast differentiation and activation. Nature 423:337–342

Altindag O, Erel O, Soran N, Celik H, Selek S (2008) Total oxidative/anti-oxidative status and relation to bone mineral density in osteoporosis. Rheumatol Int 28:317–321

Almeida M, Han L, Martin-Millan M, Plotkin LI, Stewart SA, Roberson PK, Kousteni S, O’Brien CA, Bellido T, Parfitt AM, Weinstein RS, Jilka RL, Manolagas SC (2007) Skeletal involution by age-associated oxidative stress and its acceleration by loss of sex steroids. J Biol Chem 282:27285–27297

Muthusami S, Ramachandran H, Muthusamy B, Vasudevan G, Prabhu V, Subramaniam V, Jagadeesan A, Narasimhan S (2005) Ovariectomy induces oxidative stress and impairs bone antioxidant system in adult rats. Clin Chim Acta 360:81–86

Ozgocmen S, Kaya H, Fadillioglu E, Aydogan R, Yilmaz Z (2007) Role of antioxidant systems, lipid peroxidation, and nitric oxide in postmenopausal osteoporosis. Mol Cell Biochem 295:45–52

Bax BE, Alam ASMT, Banerji B, Bax CMR, Bevis PJR, Stevens CR, Moonga BS, Blake DR, Zaidi M (1992) Stimulation of osteoclastic bone-resorption by hydrogen-peroxide. Biochem Biophys Res Commun 183:1153–1158

Garrett IR, Boyce BF, Oreffo RO, Bonewald L, Poser J, Mundy GR (1990) Oxygen-derived free radicals stimulate osteoclastic bone resorption in rodent bone in vitro and in vivo. J Clin Invest 85:632–639

Yalin S, Bagis S, Polat G, Dogruer N, Aksit SC, Hatungil R, Erdogan C (2005) Is there a role of free oxygen radicals in primary male osteoporosis ? Clin Exp Rheumatol 23:689–692

Harman D (1956) Aging—a theory based on free-radical and radiation-chemistry. J Gerontol 11:298–300

Droge W (2002) Free radicals in the physiological control of cell function. Physiol Rev 82:47–95

Sareila O, Kelkka T, Pizzolla A, Hultqvist M, Holmdahl R (2011) NOX2 complex-derived ROS as immune regulators. Antioxid Redox Signal 15:2197–2208

Key LL, Ries WL, Taylor RG, Hays BD, Pitzer BL (1990) Oxygen derived free-radicals in osteoclasts—the specificity and location of the nitroblue tetrazolium Reaction. Bone 11:115–119

Key LL, Wolf WC, Gundberg CM, Ries WL (1994) Superoxide and bone-resorption. Bone 15:431–436

Steinbeck MJ, Appel WH, Verhoeven AJ, Karnovsky MJ (1994) Nadph-oxidase expression and in-situ production of superoxide by osteoclasts actively resorbing bone. J Cell Biol 126:765–772

Yang S, Ries WL, Key LL (1998) Nicotinamide adenine dinucleotide phosphate oxidase in the formation of superoxide in osteoclasts. Calcif Tissue Int 63:346–350

Darden AG, Ries WL, Wolf WC, Rodriguiz RM, Key LL (1996) Osteoclastic superoxide production and bone resorption: stimulation and inhibition by modulators of NADPH oxidase. J Bone Miner Res 11:671–675

Fraser JH, Helfrich MH, Wallace HM, Ralston SH (1996) Hydrogen peroxide, but not superoxide, stimulates bone resorption in mouse calvariae. Bone 19:223–226

Suda N, Morita I, Kuroda T, Murota SI (1993) Participation of oxidative stress in the process of osteoclast differentiation. Biochim Biophys Acta 1157:318–323

Kim H, Kim IY, Lee SY, Jeong D (2006) Bimodal actions of reactive oxygen species in the differentiation and bone-resorbing functions of osteoclasts. FEBS Lett 580:5661–5665

Hall TJ, Schaeublin M, Jeker H, Fuller K, Chambers TJ (1995) The role of reactive oxygen intermediates in osteoclastic bone-resorption. Biochem Biophys Res Commun 207:280–287

Wong BR, Josien R, Choi Y (1999) TRANCE is a TNF family member that regulates dendritic cell and osteoclast function. J Leukoc Biol 65:715–724

Ha H, Kwak HB, Lee SW, Jin HM, Kim HM, Kim HH, Lee ZH (2004) Reactive oxygen species mediate RANK signaling in osteoclasts. Exp Cell Res 301:119–127

Lee NK, Choi YG, Baik JY, Han SY, Jeong DW, Bae YS, Kim N, Lee SY (2005) A crucial role for reactive oxygen species in RANKL-induced osteoclast differentiation. Blood 106:852–859

Bartell S, Kim H, Ambrogini E, Han L, Iyer S, Serra Ucer S, Rabinovitch P, Jilka R, Weinstein R, Zhao H, O’Brien C, Manolagas S, Almeida M (2014) FoxO proteins restrain osteoclastogenesis and bone resorption by attenuating H2O2 accumulation. Nat Commun 5:3773

Lee NK, Choi HK, Kim DK, Lee SY (2006) Rac1 GTPase regulates osteoclast differentiation through TRANCE-induced NF-kappa B activation. Mol Cell Biochem 281:55–61

Wang YQ, Lebowitz D, Sun CX, Thang H, Grynpas MD, Glogauer M (2008) Identifying the relative contributions of Rac1 and Rac2 to osteoclastogenesis. J Bone Miner Res 23:260–270

Sasaki H, Yamamoto H, Tominaga K, Masuda K, Kawai T, Teshima-Kondo S, Rokutan K (2009) NADPH oxidase-derived reactive oxygen species are essential for differentiation of a mouse macrophage cell line (RAW264.7) into osteoclasts. J Med Invest 56:33–41

Sasaki H, Yamamoto H, Tominaga K, Masuda K, Kawai T, Teshima-Kondo S, Matsuno K, Yabe-Nishimura C, Rokutan K (2009) Receptor activator of nuclear factor-kappa B ligand-induced mouse osteoclast differentiation is associated with switching between NADPH oxidase homologues. Free Radic Biol Med 47:189–199

Yang S, Madyastha P, Bingel S, Ries W, Key L (2001) A new superoxide-generating oxidase in murine osteoclasts. J Biol Chem 276:5452–5458

Yang S, Zhang YZ, Ries W, Key L (2004) Expression of Nox4 in osteoclasts. J Cell Biochem 92:238–248

Martyn KD, Frederick LM, von Loehneysen K, Dinauer MC, Knaus UG (2006) Functional analysis of Nox4 reveals unique characteristics compared to other NADPH oxidases. Cell Signal 18:69–82

Takac I, Schroder K, Zhang LL, Lardy B, Anilkumar N, Lambeth JD, Shah AM, Morel F, Brandes RP (2011) The e-loop is involved in hydrogen peroxide formation by the nadph oxidase Nox4. J Biol Chem 286:13304–13313

Case AJ, Li SM, Basu U, Tian J, Zimmerman MC (2013) Mitochondrial-localized NADPH oxidase 4 is a source of superoxide in angiotensin II-stimulated neurons. Am J Physiol Heart Circ Physiol 305:H19–H28

Block K, Gorin Y, Abboud HE (2009) Subcellular localization of Nox4 and regulation in diabetes. Proc Natl Acad Sci USA 106:14385–14390

Goettsch C, Babelova A, Trummer O, Erben RG, Rauner M, Rammelt S, Weissmann N, Weinberger V, Benkhoff S, Kampschulte M, Obermayer-Pietsch B, Hofbauer LC, Brandes RR, Schroder K (2013) NADPH oxidase 4 limits bone mass by promoting osteoclastogenesis. J Clin Investig 123:4731–4738

Asagiri M, Sato K, Usami T, Ochi S, Nishina H, Yoshida H, Morita I, Wagner EF, Mak TW, Serfling E, Takayanagi H (2005) Autoamplification of NFATc1 expression determines its essential role in bone homeostasis. J Exp Med 202:1261–1269

Kim MS, Yang YM, Son A, Tian YS, Lee SI, Kang SW, Muallem S, Shin DM (2010) RANKL-mediated reactive oxygen species pathway that induces long lasting Ca2+ oscillations essential for osteoclastogenesis. J Biol Chem 285:6913–6921

Schreck R, Rieber P, Baeuerle PA (1991) Reactive oxygen intermediates as apparently widely used messengers in the activation of the NF-kappa-B transcription factor and HIV-1. EMBO J 10:2247–2258

Decuypere JP, Monaco G, Missiaen L, De Smedt H, Parys JB, Bultynck G (2011) IP(3) receptors, mitochondria, and Ca signaling: implications for aging. J Aging Res 2011:920178

Rizzuto R, Brini M, Murgia M, Pozzan T (1993) Microdomains with high Ca2+ close to IP3-sensitive channels that are sensed by neighboring mitochondria. Science 262:744–747

Figueira TR, Barros MH, Camargo AA, Castilho RF, Ferreira JCB, Kowaltowski AJ, Sluse FE, Souza-Pinto NC, Vercesi AE (2013) Mitochondria as a source of reactive oxygen and nitrogen species: from molecular mechanisms to human health. Antioxid Redox Signal 18:2029–2074

McCormack JG, Halestrap AP, Denton RM (1990) Role of calcium-ions in regulation of mammalian intramitochondrial metabolism. Physiol Rev 70:391–425

Srinivasan S, Koenigstein A, Joseph J, Sun L, Kalyanaraman B, Zaidi M, Avadhani NG (2010) Role of mitochondrial reactive oxygen species in osteoclast differentiation. Skelet Biol Med 1192:245–252

Zhou J, Ye S, Fujiwara T, Manolagas SC, Zhao H (2013) Steap4 plays a critical role in osteoclastogenesis in vitro by regulating cellular iron/reactive oxygen species (ROS) levels and cAMP response element-binding protein (CREB) activation. J Biol Chem 288:30064–30074

Ishii KA, Fumoto T, Iwai K, Takeshita S, Ito M, Shimohata N, Aburatani H, Taketani S, Lelliott CJ, Vidal-Puig A, Ikeda K (2009) Coordination of PGC-1beta and iron uptake in mitochondrial biogenesis and osteoclast activation. Nat Med 15:259–266

Kanzaki H, Shinohara F, Kajiya M, Kodama T (2013) The Keap1/Nrf2 protein axis plays a role in osteoclast differentiation by regulating intracellular reactive oxygen species signaling. J Biol Chem 288:23009–23020

Hyeon S, Lee H, Yang Y, Jeong W (2013) Nrf2 deficiency induces oxidative stress and promotes RANKL-induced osteoclast differentiation. Free Radic Biol Med 65:789–799

Brandi ML, Hukkanen M, Umeda T, Moradi-Bidhendi N, Bianchi S, Gross SS, Polak JM, MacIntyre I (1995) Bidirectional regulation of osteoclast function by nitric oxide synthase isoforms. Proc Natl Acad Sci USA 92:2954–2958

Mancini L, Moradi-Bidhendi N, Brandi ML, MacIntyre I (1998) Nitric oxide superoxide and peroxynitrite modulate osteoclast activity. Biochem Biophys Res Commun 243:785–790

Evans DM, Ralston SH (1996) Nitric oxide and bone. J Bone Miner Res 11:300–305

Lowik CW, Nibbering PH, van de Ruit M, Papapoulos SE (1994) 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 93:1465–1472

Ralston SH, Ho LP, Helfrich MH, Grabowski PS, Johnston PW, Benjamin N (1995) Nitric oxide: a cytokine-induced regulator of bone resorption. J Bone Miner Res 10:1040–1049

Nilforoushan D, Gramoun A, Glogauer M, Manolson MF (2009) Nitric oxide enhances osteoclastogenesis possibly by mediating cell fusion. Nitric Oxide 21:27–36

Baek KH, Oh KW, Lee WY, Lee SS, Kim MK, Kwon HS, Rhee EJ, Han JH, Song KH, Cha BY, Lee KW, Kang MI (2010) Association of oxidative stress with postmenopausal osteoporosis and the effects of hydrogen peroxide on osteoclast formation in human bone marrow cell cultures. Calcif Tissue Int 87:226–235

Lean JM, Jagger CJ, Kirstein B, Fuller K, Chambers TJ (2005) Hydrogen peroxide is essential for estrogen-deficiency bone loss and osteoclast formation. Endocrinology 146:728–735

Deyhim F, Stoecker BJ, Brusewitz GH, Devareddy L, Arjmandi BH (2005) Dried plum reverses bone loss in an osteopenic rat model of osteoporosis. Menopause 12:755–762

Franklin M, Bu SY, Lerner MR, Lancaster EA, Bellmer D, Marlow D, Lightfoot SA, Arjmandi BH, Brackett DJ, Lucas EA, Smith BJ (2006) Dried plum prevents bone loss in a male osteoporosis model via IGF-I and the RANK pathway. Bone 39:1331–1342

Bai XC, Lu D, Liu AL, Zhang ZM, Li XM, Zou ZP, Zeng WS, Cheng BL, Luo SQ (2005) Reactive oxygen species stimulates receptor activator of NF-kappa B ligand expression in osteoblast. J Biol Chem 280:17497–17506

Bu SY, Lerner M, Stoecker BJ, Boldrin E, Brackett DJ, Lucas EA, Smith BJ (2008) Dried plum polyphenols inhibit osteoclastogenesis by downregulating NFATc1 and inflammatory mediators. Calcif Tissue Int 82:475–488

Moon HJ, Kim SE, Yun YP, Hwang YS, Bang JB, Park JH, Kwon IK (2011) Simvastatin inhibits osteoclast differentiation by scavenging reactive oxygen species. Exp Mol Med 43:605–612

Kim HJ, Chang EJ, Kim HM, Lee SB, Kim HD, Su KG, Kim HH (2006) Antioxidant alpha-lipoic acid inhibits osteoclast differentiation by reducing nuclear factor-kappaB DNA binding and prevents in vivo bone resorption induced by receptor activator of nuclear factor-kappaB ligand and tumor necrosis factor-alpha. Free Radic Biol Med 40:1483–1493

Koh JM, Lee YS, Byun CH, Chang EJ, Kim H, Kim YH, Kim HH, Kim GS (2005) Alpha-lipoic acid suppresses osteoclastogenesis despite increasing the receptor activator of nuclear factor kappaB ligand/osteoprotegerin ratio in human bone marrow stromal cells. J Endocrinol 185:401–413

Polat B, Halici Z, Cadirci E, Albayrak A, Karakus E, Bayir Y, Bilen H, Sahin A, Yuksel TN (2013) The effect of alpha-lipoic acid in ovariectomy and inflammation-mediated osteoporosis on the skeletal status of rat bone. Eur J Pharmacol 718:469–474

Lever JH (2002) Paget’s disease of bone in Lancashire and arsenic pesticide in cotton mill wastewater: a speculative hypothesis. Bone 31:434–436

Szymczyk KH, Kerr BAE, Freeman TA, Adams CS, Steinbeck MJ (2006) Involvement of hydrogen peroxide in the differentiation and apoptosis of preosteoclastic cells exposed to arsenite. Biochem Pharmacol 72:761–769

Xiao XH, Liao EY, Zhou HD, Dai RC, Yuan LQ, Wu XP (2005) Ascorbic acid inhibits osteoclastogenesis of RAW264.7 cells induced by receptor activated nuclear factor kappaB ligand (RANKL) in vitro. J Endocrinol Invest 28:253–260

Le Nihouannen D, Barralet JE, Fong JE, Komarova SV (2010) Ascorbic acid accelerates osteoclast formation and death. Bone 46:1336–1343

Sanbe T, Tomofuji T, Ekuni D, Azuma T, Irie K, Tamaki N, Yamamoto T, Morita M (2009) Vitamin C intake inhibits serum lipid peroxidation and osteoclast differentiation on alveolar bone in rats fed on a high-cholesterol diet. Arch Oral Biol 54:235–240

Kim MH, Ryu SY, Bae MA, Choi JS, Min YK, Kim SH (2008) Baicalein inhibits osteoclast differentiation and induces mature osteoclast apoptosis. Food Chem Toxicol 46:3375–3382

Moon HJ, Ko WK, Han SW, Kim DS, Hwang YS, Park HK, Kwon IK (2012) Antioxidants, like coenzyme Q10, selenite, and curcumin, inhibited osteoclast differentiation by suppressing reactive oxygen species generation. Biochem Biophys Res Commun 418:247–253

Léotoing L, Wauquier F, Guicheux J, Miot-Noirault E, Wittrant Y, Coxam V (2013) The polyphenol fisetin protects bone by repressing NF-kappa B and MKP-1-dependent signaling pathways in osteoclasts. Plos One 8:e68388

Sakai E, Shimada-Sugawara M, Yamaguchi Y, Sakamoto H, Fumimoto R, Fukuma Y, Nishishita K, Okamoto K, Tsukuba T (2013) Fisetin inhibits osteoclastogenesis through prevention of RANKL-induced ROS production by Nrf2-mediated up-regulation of phase II antioxidant enzymes. J Pharmacol Sci 121:288–298

Guo JD, Li L, Shi YM, Wang HD, Hou SX (2013) Hydrogen water consumption prevents osteopenia in ovariectomized rats. Br J Pharmacol 168:1412–1420

Li DZ, Zhang QX, Dong XX, Li HD, Ma X (2013) Treatment with hydrogen molecules prevents RANKL-induced osteoclast differentiation associated with inhibition of ROS formation and inactivation of MAPK, AKT and NF-kappa B pathways in murine RAW264.7 cells. J Bone Miner Metab 32:494–504

Kondo H, Togari A (2011) Continuous treatment with a low-dose beta-agonist reduces bone mass by increasing bone resorption without suppressing bone formation. Calcif Tissue Int 88:23–32

Kondo H, Takeuchi S, Togari A (2013) beta-Adrenergic signaling stimulates osteoclastogenesis via reactive oxygen species. Am J Physiol Endocrinol Metab 304:E507–E515

Rao LG, Krishnadev N, Banasikowska K, Rao AV (2003) Lycopene I–effect on osteoclasts: lycopene inhibits basal and parathyroid hormone-stimulated osteoclast formation and mineral resorption mediated by reactive oxygen species in rat bone marrow cultures. J Med Food 6:69–78

Arshad A, Sengupta S, Sharma S, Ghosh R, Sawlani V, Singh MM (2004) In vitro anti-resorptive activity and prevention of ovariectomy-induced osteoporosis in female Sprague-Dawley rats by ormeloxifene, a selective estrogen receptor modulator. J Steroid Biochem Mol Biol 91:67–78

Kharkwal G, Chandra V, Fatima I, Dwivedi A (2012) Ormeloxifene inhibits osteoclast differentiation in parallel to downregulating RANKL-induced ROS generation and suppressing the activation of ERK and JNK in murine RAW264.7 cells. J Mol Endocrinol 48:261–270

Nomura M, Yoshimura Y, Kikuiri T, Hasegawa T, Taniguchi Y, Deyama Y, Koshiro K, Sano H, Suzuki K, Inoue N (2011) Platinum nanoparticles suppress osteoclastogenesis through scavenging of reactive oxygen species produced in RAW264.7 cells. J Pharmacol Sci 117:243–252

Oka Y, Iwai S, Amano H, Irie Y, Yatomi K, Ryu K, Yamada S, Inagaki K, Oguchi K (2012) Tea polyphenols inhibit rat osteoclast formation and differentiation. J Pharmacol Sci 118:55–64

He X, Andersson G, Lindgren U, Li Y (2010) Resveratrol prevents RANKL-induced osteoclast differentiation of murine osteoclast progenitor RAW 264.7 cells through inhibition of ROS production. Biochem Biophys Res Commun 401:356–362

Kyung TW, Lee JE, Shin HH, Choi HS (2008) Rutin inhibits osteoclast formation by decreasing reactive oxygen species and TNF-alpha by inhibiting activation of NF-kappa B. Exp Mol Med 40:52–58

Horcajada-Molteni MN, Crespy V, Coxam V, Davicco MJ, Remesy C, Barlet JP (2000) Rutin inhibits ovariectomy-induced osteopenia in rats. J Bone Miner Res 15:2251–2258

Kim MH, Ryu SY, Choi JS, Min YK, Kim SH (2009) Saurolactam inhibits osteoclast differentiation and stimulates apoptosis of mature osteoclasts. J Cell Physiol 221:618–628

Han KY, Yang D, Chang EJ, Lee Y, Huang H, Sung SH, Lee ZH, Kim YC, Kim HH (2007) Inhibition of osteoclast differentiation and bone resorption by sauchinone. Biochem Pharmacol 74:911–923

Ahn KS, Sethi G, Chaturvedi MM, Aggarwal BB (2008) Simvastatin, 3-hydroxy-3-methylglutaryl coenzyme a reductase inhibitor, suppresses osteoclastogenesis induced by receptor activator of nuclear factor-kappa B ligand through modulation of NF-kappa B pathway. Int J Cancer 123:1733–1740

Hie M, Tsukamoto I (2011) Administration of zinc inhibits osteoclastogenesis through the suppression of RANK expression in bone. Eur J Pharmacol 668:140–146