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Novel techniques in the development of osteoporosis drug therapy: the osteoclast ruffled-border vacuolar H+-ATPase as an emerging target

, PhD & , PhD

Bibliography

  • Seeman E. Modeling and remodeling. In: Bilezikian JP, Raisz LG, Martin TJ, editors, Principles of bone biology. 3rd edition. Academic Press, Waltham, Massachusetts; 2008. p. 3-28
  • Kini U, Nandeesh BN. Physiology of bone formation, remodeling, and metabolism. In: Fogelman I, Gnanasegaran G, Van der Wall H, editors, Radionuclide and hybrid bone imaging. Springer-Verlag, Heidelberg; 2013. p. 29-57
  • Sims NA, Gooi JH. Bone remodeling: multiple cellular interactions required for coupling of bone formation and resorption. Semin Cell Dev Biol 2008;19(5):444-51
  • Crockett JC, Rogers MJ, Coxon FP, et al. Bone remodeling at a glance. J Cell Sci 2011;124(7):991-8
  • Shapiro F. Bone development and its relation to fracture repair. The role of mesenchymal osteoblasts and surface osteoblasts. Eur Cell Mater 2008;15:53-76
  • Schindeler A, McDonald MM, Bokko P, et al. Bone remodeling during fracture repair: the cellular picture. Semin Cell Dev Biol 2008;19(5):459-66
  • Feng X, McDonald JM. Disorders of bone remodeling. Annu Rev Pathol 2011;6:121-45
  • Aggarwal S. Skeletal dysplasias with increased bone density: evolution of molecular pathogenesis in the last century. Gene 2013;528(1):41-5
  • Becker DJ, Kilgore ML, Morrissey MA. The societal burden of osteoporosis. Curr Rheumatol Rep 2010;12(3):186-91
  • Deal C. Bone loss in rheumatoid arthritis: systemic, periarticular and focal. Curr Rheumatol Rep 2012;14(3):231-7
  • Chochran DL. Inflammation and bone loss in periodontal disease. J Periodontol 2008;79(Suppl 8):1569-76
  • Beck RT, Illingworth KD, Saleh KJ. Review of periprosthetic osteolysis in total joint arthroplasty: an emphasis on host factors and future directions. J Orthop Res 2012;30(4):541-6
  • Guise TA, Mohammad KS, Clines G, et al. Basic mechanisms responsible for osteolytic and osteoblastic bone metastases. Clin Cancer Res 2006;12(Suppl 20):6213s-6s
  • Naot D. Paget's disease of bone: an update. Curr Opin Endocrinol Diabetes Obes 2011;18(6):352-8
  • Rachner TD, Khosla S, Hofbauer LC. Osteoporosis: now and the future. Lancet 2011;377(9773):1276-87
  • Huang C, Ogawa R. Mechanotransduction in bone repair and regeneration. FASEB J 2010;24(10):3625-32
  • Raggatt LJ, Partridge NC. Cellular and molecular mechanisms of bone remodeling. J Biol Chem 2010;285(33):25103-8
  • Zaidi M. Skeletal remodeling in health and disease. Nat Med 2007;13(7):791-801
  • Xiong J, O'Brien CA. Osteocyte RANKL: new insights into control of bone remodeling. J Bone Miner Res 2012;27(3):499-505
  • Väänänen HK, Laitala-Leinonen T. Osteoclast lineage and function. Arch Biochem Biophys 2008;473(2):132-8
  • Schmidt S, Nakchbandi I, Ruppert R, et al. Kindlin-3-mediated signaling from multiple integrin classes is required for osteoclast-mediated bone resorption. J Cell Biol 2011;192(5):883-97
  • Gallagher CJ, Sai AJ. Molecular biology of bone remodeling: implications for new therapeutic targets for osteoporosis. Maturitas 2010;65(4):301-7
  • Long CL, Humphrey MB. Osteoimmunology: the expanding role of immunoreceptors in osteoclast and bone remodeling. BoneKey Rep 2012; 1(59)
  • Teitelbaum SL, Zou W. The osteoclast cytoskeleton: how does it work? IBMS BoneKEy 2011;8(2):74-83
  • Coxon FP, Taylor A. Vesicular trafficking in osteoclasts. Semin Cell Dev Biol 2008;19(5):424-33
  • Chen S-H, Bubb MR, Yarmola EG, et al. Vacuolar H+-ATPase binding to microfilaments: regulation in response to phosphatidylinositol 3-kinase activity and detailed characterization of the actin-binding site in subunit B. J Biol Chem 2004;279(9):7988-98
  • Lee BS, Gluck SL, Holliday LS. Interaction between vacuolar H+-ATPase and microfilaments during osteoclast activation. J Biol Chem 1999;274(41):29164-71
  • Marie PJ, Kassem M. Osteoblasts in osteoporosis: past, emerging, and future anabolic targets. Eur J Endocrinol 2011;165(1):1-10
  • Kawai M, Mödder UI, Khosla S, et al. Emerging therapeutic opportunities for skeletal restoration. Nat Rev Drug Discov 2011;10(2):141-56
  • Reid IR. Anti-resorptive therapy for osteoporosis. Semin Cell Dev Biol 2008;19(5):473-8
  • van Beek ER, Cohen LH, Leroy IM, et al. Differentiating the mechanisms of antiresorptive action of nitrogen containing bisphosphonates. Bone 2003;33(5):805-11
  • Baron R, Ferrari S, Russel RGG. Denosumab and bisphosphonates: different mechanisms of action and effects. Bone 2011;48(4):677-92
  • Lacey DL, Boyle WJ, Simonet WS, et al. Bench to bedside: elucidation of the OPG–RANK–RANKL pathway and the development of denosumab. Nat Rev Drug Discov 2012;11(5):401-19
  • Dougall WC, Glaccum M, Charrier K, et al. RANK is essential for osteoclast and lymph node development. Genes Dev 1999;13(18):2412-24
  • Cianferotti L, D'Asta F, Brandi ML. A review on strontium ranelate long-term antifracture efficacy in the treatment of postmenopausal osteoporosis. Ther Adv Musculoskelet Dis 2013;5(3):127-39
  • PRAC recommends suspending use of Potelos/Osseor (strontium ranelate). European Medicines Agency's Pharmacovigilance Risk Assessment Committee (EMA/PRAC). 2014. Available from: http://www.ema.europa.eu/docs/en_GB/document_library/Referrals_document/Protelos_and_Osseor/Recommendation_provided_by_Pharmacovigilance_Risk_Assessment_Committee/WC500159374.pdf [Last accessed 24 February 2014]
  • Duong LT. Therapeutic inhibition of cathepsin K—reducing bone resorption while maintaining bone formation. BoneKey Rep 2012;1:67
  • Padhi D, Jang G, Stouch B, et al. Single-dose placebo-controlled, randomized study of AMG 785, a sclerostin monoclonal antibody. J Bone Miner Res 2011;26(1):19-26
  • Deal C. Potential new targets for osteoporosis. Nat Clin Pract Rheumatol 2009;5(1):20-7
  • Prockop DJ. New targets for osteoporosis. N Engl J Med 2012;367(24):2353-4
  • Lim V, Clarke BL. New therapeutics for osteoporosis: beyond denosumab. Maturitas 2012;73(3):269-72
  • Lewiecki EM. New targets for intervention in the treatment of postmenopausal osteoporosis. Nat Rev Rheumatol 2011;7(11):631-8
  • Fisher JE, Scott K, Wei N, et al. Pharmacodynamic responses to combined treatment regimens with the calcium sensing receptor antagonist JTT-305/MK-5442 and alendronate in osteopenic ovariectomized rats. Bone 2012;50(6):1322-42
  • Inose H, Zhou B, Yadav VK, et al. Efficacy of serotonin inhibition in mouse models of bone loss. J Bone Miner Res 2011;26(9):2002-11
  • Havens AM, Shiozawa Y, Jung Y, et al. Human very small embryonic-like cells generate skeletal structures, in vivo. Stem Cells Dev 2013;15(4):622-30
  • Abbott A. Doubt cast over tiny stem cells. Nature 2013;499(7459):390
  • Mikami Y, Matsumoto T, Kano K, et al. Current status of drug therapies for osteoporosis and the search for stem cells adapted for bone regenerative medicine. Anat Sci Int 2013;89(1):1-10
  • Jain N, Weinstein RS. Giant osteoclasts after long-term bisphosphonate terapy: diagnostic challenges. Nat Rev Rheumatol 2009;5(6):341-6
  • Reid IR, Miller PD, Brown JP, et al. Effects of denosumab on bone histomorphometry: the FREEDOM and STAND studies. J Bone Miner Res 2010;25(10):2256-65
  • Lotinun S, Kiviranta R, Matsubara T, et al. Osteoclast-specific cathepsin K deletion stimulates S1P-dependent bone formation. J Clin Invest 2014;123(2):666-81
  • Duong LT. Inhibition of cathepsin K: blocking osteoclast bone resorption and more. IBMS BoneKEy 2013;10:396
  • Muench SP, Trinick J, Harrison MA. Structural divergence of the rotary ATPases. Q Rev Biophys 2011;44(3):311-56
  • Toei M, Saum R, Forgac M. Regulation and isoform function of the V-ATPases. Biochemistry 2010;49(23):4715-23
  • Saroussi S, Nelson N. Vacuolar H+-ATPases—an enzyme for all seasons. Pfluegers Arch 2009;457(3):581-7
  • Manolson MF, Wu B, Proteau D, et al. STV1 gene encodes functional homologue of 95-kDa yeast vacuolar H+-ATPase subunit Vph1p. J Biol Chem 1994;269(19):14064-74
  • Kawasaki-Nishi S, Bowers K, Nishi T, et al. The amino-terminal domain of the vacuolar proton-translocating ATPase a subunit controls targeting and in vivo dissociation, and the carboxyl-terminal domain affects coupling of proton transport and ATP hydrolysis. J Biol Chem 2001;276(50):47411-20
  • Finnigan GC, Hanson-Smith V, Houser BD, et al. The reconstructed ancestral subunit a functions as both V-ATPase isoforms Vph1p and Stv1p in Saccharomyces cerevisiae. Mol Biol Cell 2011;22(17):3176-91
  • Zhang Z, Zheng Y, Mazon H, et al. Structure of the yeast vacuolar ATPase. J Biol Chem 2008;283(51):35983-95
  • Kartner N, Yao Y, Li K, et al. Inhibition of osteoclast bone resorption by disrupting vacuolar H+-ATPase a3–B2 subunit interaction. J Biol Chem 2010;285(48):37476-90
  • Utku N, Heinemann T, Tullius SG, et al. Prevention of acute allograft rejection by antibody targeting of TIRC7, a novel T cell membrane protein. Immunity 1998;9(4):509-18
  • Kartner N, Yao Y, Bhargava A, et al. Topology, glycosylation and conformational changes in the membrane domain of the vacuolar H+-ATPase a subunit. J Cell Biochem 2013;114(7):1474-87
  • Toei M, Toei S, Forgac M. Definition of membrane topology and identification of residues important for transport in subunit a of the vacuolar ATPase. J Biol Chem 2011;286(40):35176-86
  • Findlay JBC, Harrison MA. A protein chemical approach to channel structure and function: The proton channel of the vacuolar H+-ATPase. Novartis Found Symp 2002;245:207-22
  • Wang Y, Inoue T, Forgac M. TM2 but not TM4 of subunit c" interacts with TM7 of subunit a of the yeast V-ATPase as defined by disulfide-mediated cross-linking. J Biol Chem 2004;279(43):44628-38
  • Bhargava A, Voronov I, Wang Y, et al. Osteopetrosis mutation R444L causes ER retention and misprocessing of vacuolar H+-ATPase a3 subunit. J Biol Chem 2012;287(32):26829-39
  • Srinivasan S, Vyas NK, Baker ML, et al. Crystal structure of the cytoplasmic N-terminal domain of subunit I, a homolog of subunit a, of V-ATPase. J Mol Biol 2011;412(1):14-21
  • Marshansky V, Futai M. The V-type H+-ATPase in vesicular trafficking: Targeting, regulation and function. Curr Opin Cell Biol 2008;20(4):415-26
  • Kane PM. The where, when, and how of organelle acidification by the yeast vacuolar H+-ATPase. Microbiol Mol Biol Rev 2006;70(1):177-91
  • Saroussi S, Nelson N. The little we know on the structure and machinery of V-ATPase. J Exp Biol 2009;212(11):1604-10
  • Nordström T, Rotstein OD, Romanek R, et al. Regulation of cytoplasmic pH in osteoclasts: contribution of proton pumps and a proton-selective conductance. J Biol Chem 1995;270(5):2203-12
  • Wagner CA, Devuyst O, Bourgeois S, et al. Regulated acid–base transport in the collecting duct. Pfluegers Arch 2009;458(1):137-56
  • Vaes G. On the mechanisms of bone resorption: the action of parathyroid hormone on the excretion and synthesis of lysosomal enzymes and on the extracellular release of acid by bone cells. J Cell Biol 1968;39(3):676-97
  • Baron R, Neff L, Louvard D, et al. Cell-mediated extracellular acidification and bone resorption: evidence for a low pH in resorbing lacunae and localization of a 100-kD lysosomal membrane protein at the osteoclast ruffled border. J Cell Biol 1985;101(6):2210-22
  • Manolson MF, Yu H, Chen W, et al. The a3 isoform of the 100-kDa V-ATPase subunit is highly but differentially expressed in large (≥ 10 nuclei) and small (≤ 5 nuclei) osteoclasts. J Biol Chem 2003;278(49):49271-8
  • Toyomura T, Murata Y, Yamamoto A, et al. From lysosomes to the plasma membrane: Localization of vacuolar-type H+-ATPase with the a3 isoform during osteoclast differentiation. J Biol Chem 2003;278(24):22023-30
  • Blair HC, Teitelbaum SL, Ghiselli R, et al. Osteoclastic bone resorption by a polarized vacuolar proton pump. Science 1989;245(4920):855-7
  • Li Y-P, Chen W, Liang Y, et al. Atp6i-deficient mice exhibit severe osteopetrosis due to loss of osteoclast-mediated extracellular acidification. Nat Genet 1999;23(4):447-51
  • Lee S-H, Rho J, Jeong D, et al. v-ATPase V0 subunit d2-deficient mice exhibit impaired osteoclast fusion and increased bone formation. Nat Med 2006;12(12):1403-9
  • Lee BS, Holliday LS, Ojikutu B, et al. Osteoclasts express the B2 isoform of vacuolar H+-ATPase intracellularly and on their plasma membranes. Am J Physiol Cell Physiol 1996;270(1):C382-C88
  • Feng S, Deng L, Chen W, et al. Atp6v1c1 is an essential component of the osteoclast proton pump and in F-actin ring formation in osteoclasts. Biochem J 2009;417(1):195-203
  • Toyomura T, Oka T, Yamaguchi C, et al. Three subunit a isoforms of mouse vacuolar H+-ATPase: Preferential expression of the a3 isoform during osteoclast differentiation. J Biol Chem 2000;275(12):8760-5
  • Zuo J, Jiang J, Chen S-H, et al. Actin binding activity of subunit B of vacuolar H+ATPase is involved in its targeting to ruffled membranes of osteoclasts. J Bone Miner Res 2006;21(5):714-21
  • Nakamura I, Takahashi N, Sasaki T, et al. Wortmannin, a specific inhibitor of phosphatidylinositol-3 kinase, blocks osteoclastic bone resorption. FEBS Lett 1995;361(1):79-84
  • Kane PM. Targeting reversible disassembly as a mechanism of controlling V-ATPase activity. Curr Protein Peptide Sci 2012;13(2):117-23
  • Hosokawa H, Dip PV, Merkulova M, et al. The N termini of a-subunit isoforms are involved in signaling between vacuolar H+-ATPase (V-ATPase) and cytohesin-2. J Biol Chem 2013;288(8):5896-913
  • Jansen EJR, Martens G. Novel insights into V-ATPase functioning: distinct roles for its accessory subunits ATP6AP1/Ac45 and ATP6AP2/(pro) renin receptor. Curr Protein Pept Sci 2012;13(2):124-33
  • Henriksen K, Flores C, Thomsen JS, et al. Dissociation of bone resorption and bone formation in adult mice with a non-functional V-ATPase in osteoclasts leads to increased bone strength. PLoS One 2011;6(11):e27482
  • Frattini A, Orchard PJ, Sobacchi C, et al. Defects in TCIRG1 subunit of the vacuolar proton pump are responsible for a subset of human autosomal recessive osteopetrosis. Nat Genet 2000;25(3):343-6
  • Karsdal MA, Martin TJ, Bollerslev J, et al. Are nonresorbing osteoclasts sources of bone anabolic activity? J Bone Miner Res 2007;22(4):487-94
  • Thudium CS, Jensen VK, Karsdal MA, et al. Disruption of the V-ATPase functionality as a way to uncouple bone formation and resorption – a novel target for treatment of osteoporosis. Curr Protein Pept Sci 2012;13(2):141-51
  • Holliday LS, Huynh N, Zuo J, et al. Mechanisms controlling vacuolar H+-adenosine triphosphatase activity: targets for the development of new therapeutic agents for the mangement of osteoporosis. Res Rep Biochem 2013;3:37-53
  • Huss M, Wieczorek H. Inhibitors of V-ATPases: old and new players. J Exp Biol 2009;212(3):341-6
  • Toro EJ, Zuo J, Ostrov DA, et al. Enoxacin directly inhibits osteoclastogenesis without inducing apoptosis. J Biol Chem 2012;287(21):17894-904
  • Osteresch C, Bender T, Grond S, et al. The binding site of the V-ATPase inhibitor apicularen is in the vicinity of those for bafilomycin and archazolid. J Biol Chem 2012;287(38):31866-76
  • Crasto GJ, Kartner N, Yao Y, et al. Luteolin inhibition of V-ATPase a3–d2 interaction decreases osteoclast resorptive activity. J Cell Biochem 2013;114(4):929-41
  • Ostrov DA, Magis AT, Wronski TJ, et al. Identification of Enoxacin as an inhibitor of osteoclast formation and bone resorption by structure-based virtual screening. J Med Chem 2009;52(16):5144-51
  • Jiang H, Chen W, Zhu G, et al. RNAi-mediated silencing of Atp6i and Atp6i haploinsufficiency prevents both bone loss and inflammation in a mouse model of periodontal disease. PLoS One 2013;8(4):e58599
  • Lemieux JM, Wu G, Morgan JA, et al. DMSO regulates osteoclast development in vitro. In Vitro Cell Dev Biol Anim 2011;47(3):260-7
  • Lin X, Han X, Kawai T, et al. Antibody to receptor activator of NF-κB ligand ameliorates T cell-mediated periodontal bone resorption. Infect Immun 2011;79(2):911-17
  • Kawai T, Matsuyama T, Hosokawa Y, et al. B and T lymphocytes are the primary source of RANKL in the bone resorptive lesion of periodontal disease. Am J Pathol 2006;169(3):987-98
  • Heinemann T, Bulwin G-C, Randall J, et al. Genomic organization of the gene coding for TIRC7, a novel membrane protein essential for T cell activation. Genomics 1999;57(3):398-406
  • Burge R, Dawson-Hughes B, Solomon DH, et al. Incidence and economic burden of osteoporosis-related fractures in the United States, 2005–2025. J Bone Miner Res 2007;22(3):465-75
  • Hernlund E, Svedbom A, Ivergård M, et al. Osteoporosis in the European Union: medical management, epidemiology and economic burden. Arch Osteoporos 2013;8(1–2):136
  • Martin JT, Gooi JH, Sims NA. Molecular mechanisms in coupling of bone formation to resorption. Crit Rev Eukaryot Gene Expr 2009;19(1):73-88
  • Pierroz DD, Bonnet N, Baldock PA, et al. Are osteoclasts needed for the bone anabolic response to parathyroid hormone? J Biol Chem 2010;285:28164-73
  • Black DM, Greenspan SL, Ensrud KE, et al. The effects of parathyroid hormone and alendronate alone or in combination in postmenopausal osteoporosis. N Engl J Med 2003;349(13):1207-15
  • Ettinger B, San Martin J, Crans G, et al. Differential effects of teriparatide on BMD after treatment with raloxifene or alendronate. J Bone Miner Res 2004;19(5):745-51
  • Finkelstein JS, Hayes A, Hunzelman JL, et al. The effects of parathyroid hormone, alendronate, or both in men with osteoporosis. N Engl J Med 2003;349(13):1216-26
  • Hodsman AB, Bauer DC, Dempster DW, et al. Parathyroid hormone and teriparatide for the treatment of osteoporosis: a review of the evidence and suggested guidelines for its use. Endocr Rev 2005;26(5):688-703
  • Müller KH, Kainov DE, El Bakkouri K, et al. The proton translocation domain of cellular vacuolar ATPase provides a target for the treatment of influenza A virus infections. Br J Pharmacol 2011;164(2):344-57
  • Miranda KC, Karet FE, Brown D. An extended nomenclature for mammalian V-ATPase subunit genes and splice variants. PLoS One 2010;5(3):e9531

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