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Review

Targeting Subchondral Bone Mesenchymal Stem Cell Activities for Intrinsic Joint Repair in Osteoarthritis

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Article: FSO228 | Received 27 Apr 2017, Accepted 02 Jun 2017, Published online: 06 Sep 2017

References

  • Golightly YM, Allen KD, Jordan JM. Defining the burden of osteoarthritis in population-based surveys. Arthritis Care Res. (Hoboken) 68(5), 571–573 (2016).
  • Loeser RF. Aging processes and the development of osteoarthritis. Curr. Opin. Rheumatol. 25(1), 108–113 (2013).
  • Sharma AR, Jagga S, Lee SS, Nam JS. Interplay between cartilage and subchondral bone contributing to pathogenesis of osteoarthritis. Int. J. Mol. Sci. 14(10), 19805–19830 (2013).
  • Smith MD. The normal synovium. Open Rheumatol. J. 5, 100–106 (2011).
  • Li G, Yin J, Gao J et al. Subchondral bone in osteoarthritis: insight into risk factors and microstructural changes. Arthritis Res. Ther. 15(6), 223 (2013).
  • Mcgonagle D, Tan AL, Carey J, Benjamin M. The anatomical basis for a novel classification of osteoarthritis and allied disorders. J. Anat. 216(3), 279–291 (2010).
  • Goldring MB, Goldring SR. Articular cartilage and subchondral bone in the pathogenesis of osteoarthritis. Ann. NY Acad. Sci. 1192, 230–237 (2010).
  • Bettica P, Cline G, Hart DJ, Meyer J, Spector TD. Evidence for increased bone resorption in patients with progressive knee osteoarthritis: longitudinal results from the Chingford study. Arthritis Rheum. 46(12), 3178–3184 (2002).
  • Burr DB, Gallant MA. Bone remodelling in osteoarthritis. Nat. Rev. Rheumatol. 8(11), 665–673 (2012).
  • Bowes MA, Mclure SW, Wolstenholme CB et al. Osteoarthritic bone marrow lesions almost exclusively colocate with denuded cartilage: a 3D study using data from the Osteoarthritis initiative. Ann. Rheum. Dis. 75(10), 1852–1857 (2016).
  • Wong SH, Chiu KY, Yan CH. Review article: osteophytes. J. Orthop. Surg. (Hong Kong) 24(3), 403–410 (2016).
  • Rucci N. Molecular biology of bone remodelling. Clin. Cases Miner. Bone Metab. 5(1), 49–56 (2008).
  • Nakahama K. Cellular communications in bone homeostasis and repair. Cell Mol. Life Sci. 67(23), 4001–4009 (2010).
  • Charles JF, Aliprantis AO. Osteoclasts: more than ‘bone eaters’. Trends Mol. Med. 20(8), 449–459 (2014).
  • Crane JL, Cao X. Bone marrow mesenchymal stem cells and TGF-beta signaling in bone remodeling. J. Clin. Invest. 124(2), 466–472 (2014).
  • Xian L, Wu X, Pang L et al. Matrix IGF-1 maintains bone mass by activation of mTOR in mesenchymal stem cells. Nat. Med. 18(7), 1095–1101 (2012).
  • Crane JL, Cao X. Function of matrix IGF-1 in coupling bone resorption and formation. J. Mol. Med. (Berl.) 92(2), 107–115 (2014).
  • Bianco P, Robey PG. Skeletal stem cells. Development 142(6), 1023–1027 (2015).
  • Greenbaum A, Hsu YM, Day RB et al. CXCL12 in early mesenchymal progenitors is required for haematopoietic stem-cell maintenance. Nature 495(7440), 227–230 (2013).
  • Oshita K, Yamaoka K, Udagawa N et al. Human mesenchymal stem cells inhibit osteoclastogenesis through osteoprotegerin production. Arthritis Rheum. 63(6), 1658–1667 (2011).
  • Ziegler P, Boettcher S, Takizawa H, Manz MG, Brummendorf TH. LPS-stimulated human bone marrow stroma cells support myeloid cell development and progenitor cell maintenance. Ann. Hematol. 95(2), 173–178 (2016).
  • Sakaguchi Y, Sekiya I, Yagishita K, Ichinose S, Shinomiya K, Muneta T. Suspended cells from trabecular bone by collagenase digestion become virtually identical to mesenchymal stem cells obtained from marrow aspirates. Blood 104(9), 2728–2735 (2004).
  • Jones E, English A, Churchman SM et al. Large-scale extraction and characterization of CD271+ multipotential stromal cells from trabecular bone in health and osteoarthritis: implications for bone regeneration strategies based on uncultured or minimally cultured multipotential stromal cells. Arthritis Rheum. 62, 1944–1954 (2010).
  • Cox G, Boxall SA, Giannoudis PV et al. High abundance of CD271(+) multipotential stromal cells (MSCs) in intramedullary cavities of long bones. Bone 50(2), 510–517 (2012).
  • Campbell TM, Churchman SM, Gomez A et al. Mesenchymal stem cell alterations in bone marrow lesions in hip osteoarthritis. Arthritis Rheumatol. (Hoboken, NJ) 68(7), 1648–1659 (2016).
  • Dominici M, Le Blanc K, Mueller I et al. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8(4), 315–317 (2006).
  • Churchman SM, Ponchel F, Boxall SA et al. Transcriptional profile of native CD271+ multipotential stromal cells: evidence for multiple fates, with prominent osteogenic and Wnt pathway signaling activity. Arthritis Rheum. 64(8), 2632–2643 (2012).
  • Qian H, Le Blanc K, Sigvardsson M. Primary mesenchymal stem and progenitor cells from bone marrow lack expression of CD44 protein. J. Biol. Chem. 287(31), 25795–25807 (2012).
  • Morikawa S, Mabuchi Y, Kubota Y et al. Prospective identification, isolation, and systemic transplantation of multipotent mesenchymal stem cells in murine bone marrow. J. Exp. Med. 206(11), 2483–2496 (2009).
  • Boxall SA, Jones E. Markers for characterization of bone marrow multipotential stromal cells. Stem Cells Int. 2012, 975871 (2012).
  • Tormin A, Li O, Brune JC et al. CD146 expression on primary nonhematopoietic bone marrow stem cells is correlated with in situ localization. Blood 117, 5067–5077 (2011).
  • Sacchetti B, Funari A, Michienzi S et al. Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell 131, 324–336 (2007).
  • Li H, Ghazanfari R, Zacharaki D, Lim HC, Scheding S. Isolation and characterization of primary bone marrow mesenchymal stromal cells. Ann. NY Acad. Sci. 1370(1), 109–118 (2016).
  • Houlihan DD, Mabuchi Y, Morikawa S et al. Isolation of mouse mesenchymal stem cells on the basis of expression of Sca-1 and PDGFR-alpha. Nat. Protoc. 7(12), 2103–2111 (2012).
  • Mendez-Ferrer S, Michurina TV, Ferraro F et al. Mesenchymal and haematopoietic stem cells form a unique bone marrow niche. Nature 466(7308), 829–834 (2010).
  • Pinho S, Lacombe J, Hanoun M et al. PDGFRalpha and CD51 mark human nestin+ sphere-forming mesenchymal stem cells capable of hematopoietic progenitor cell expansion. J. Exp. Med. 210(7), 1351–1367 (2013).
  • Roberts S, Genever P, Mccaskie A, De Bari C. Prospects of stem cell therapy in osteoarthritis. Regen. Med. 6(3), 351–366 (2011).
  • Barry F, Murphy M. Mesenchymal stem cells in joint disease and repair. Nat Rev Rheumatol. 9(10), 584–594 (2013).
  • Murphy JM, Dixon K, Beck S, Fabian D, Feldman A, Barry F. Reduced chondrogenic and adipogenic activity of mesenchymal stem cells from patients with advanced osteoarthritis. Arthritis Rheum. 46(3), 704–713 (2002).
  • Zhen G, Wen C, Jia X et al. Inhibition of TGF-β signaling in mesenchymal stem cells of subchondral bone attenuates osteoarthritis. Nat. Med. 19, 704–712 (2013).
  • Tang Y, Wu X, Lei W et al. TGF-beta1-induced migration of bone mesenchymal stem cells couples bone resorption with formation. Nat. Med. 15(7), 757–765 (2009).
  • Goldring MB. Chondrogenesis, chondrocyte differentiation, and articular cartilage metabolism in health and osteoarthritis. Ther. Adv. Musculoskelet. Dis. 4(4), 269–285 (2012).
  • Sanchez C, Deberg MA, Bellahcene A et al. Phenotypic characterization of osteoblasts from the sclerotic zones of osteoarthritic subchondral bone. Arthritis Rheum. 58(2), 442–455 (2008).
  • Tat SK, Pelletier JP, Velasco CR, Padrines M, Martel-Pelletier J. New perspective in osteoarthritis: the OPG and RANKL system as a potential therapeutic target? Keio J. Med. 58(1), 29–40 (2009).
  • Kwan Tat S, Pelletier JP, Lajeunesse D, Fahmi H, Lavigne M, Martel-Pelletier J. The differential expression of osteoprotegerin (OPG) and receptor activator of nuclear factor kappaB ligand (RANKL) in human osteoarthritic subchondral bone osteoblasts is an indicator of the metabolic state of these disease cells. Clin. Exp. Rheumatol. 26(2), 295–304 (2008).
  • Massicotte F, Lajeunesse D, Benderdour M et al. Can altered production of interleukin-1beta, interleukin-6, transforming growth factor-beta and prostaglandin E(2) by isolated human subchondral osteoblasts identify two subgroups of osteoarthritic patients. Osteoarthritis Cartilage 10(6), 491–500 (2002).
  • Couchourel D, Aubry I, Delalandre A et al. Altered mineralization of human osteoarthritic osteoblasts is attributable to abnormal Type I collagen production. Arthritis Rheum. 60(5), 1438–1450 (2009).
  • Kumarasinghe DD, Sullivan T, Kuliwaba JS, Fazzalari NL, Atkins GJ. Evidence for the dysregulated expression of TWIST1, TGFbeta1 and SMAD3 in differentiating osteoblasts from primary hip osteoarthritis patients. Osteoarthritis Cartilage 20(11), 1357–1366 (2012).
  • Prideaux M, Findlay DM, Atkins GJ. Osteocytes: the master cells in bone remodelling. Curr. Opin. Pharmacol. 28, 24–30 (2016).
  • Xiong J, Onal M, Jilka RL, Weinstein RS, Manolagas SC, O’brien CA. Matrix-embedded cells control osteoclast formation. Nat. Med. 17(10), 1235–1241 (2011).
  • Komori T. Functions of the osteocyte network in the regulation of bone mass. Cell Tissue Res. 352(2), 191–198 (2013).
  • Kennedy OD, Herman BC, Laudier DM, Majeska RJ, Sun HB, Schaffler MB. Activation of resorption in fatigue-loaded bone involves both apoptosis and active pro-osteoclastogenic signaling by distinct osteocyte populations. Bone 50(5), 1115–1122 (2012).
  • Teti A, Zallone A. Do osteocytes contribute to bone mineral homeostasis? Osteocytic osteolysis revisited. Bone 44(1), 11–16 (2009).
  • Wysolmerski JJ. Osteocytic osteolysis: time for a second look? Bonekey Rep. 1, 229 (2012).
  • Fowler TW, Acevedo C, Mazur CM et al. Glucocorticoid suppression of osteocyte perilacunar remodeling is associated with subchondral bone degeneration in osteonecrosis. Sci. Rep. 7, 44618 (2017).
  • Manolagas SC, Parfitt AM. What old means to bone. Trends Endocrinol. Metab. 21(6), 369–374 (2010).
  • Tanamas SK, Wluka AE, Pelletier JP et al. Bone marrow lesions in people with knee osteoarthritis predict progression of disease and joint replacement: a longitudinal study. Rheumatology (Oxford) 49(12), 2413–2419 (2010).
  • Zhu S, Chen K, Lan Y, Zhang N, Jiang R, Hu J. Alendronate protects against articular cartilage erosion by inhibiting subchondral bone loss in ovariectomized rats. Bone 53(2), 340–349 (2013).
  • Davis AJ, Smith TO, Hing CB, Sofat N. Are bisphosphonates effective in the treatment of osteoarthritis pain? A meta-analysis and systematic review. PLoS ONE 8(9), e72714 (2013).
  • Karsdal MA, Bay-Jensen AC, Lories RJ et al. The coupling of bone and cartilage turnover in osteoarthritis: opportunities for bone antiresorptives and anabolics as potential treatments? Ann. Rheum. Dis. 73(2), 336–348 (2014).
  • Laslett LL, Dore DA, Quinn SJ et al. Zoledronic acid reduces knee pain and bone marrow lesions over 1 year: a randomised controlled trial. Ann. Rheum. Dis. 71(8), 1322–1328 (2012).
  • Misra J, Mohanty ST, Madan S et al. Zoledronate attenuates accumulation of DNA damage in mesenchymal stem cells and protects their function. Stem Cells 34(3), 756–767 (2016).
  • Han W, Fan S, Bai X, Ding C. Strontium ranelate, a promising disease modifying osteoarthritis drug. Expert Opin. Investig. Drugs 26(3), 375–380 (2017).
  • Reginster JY, Badurski J, Bellamy N et al. Efficacy and safety of strontium ranelate in the treatment of knee osteoarthritis: results of a double-blind, randomised placebo-controlled trial. Ann. Rheum. Dis. 72(2), 179–186 (2013).
  • Pelletier JP, Roubille C, Raynauld JP et al. Disease-modifying effect of strontium ranelate in a subset of patients from the Phase III knee osteoarthritis study SEKOIA using quantitative MRI: reduction in bone marrow lesions protects against cartilage loss. Ann. Rheum. Dis. 74(2), 422–429 (2015).
  • Boonen S, Rosenberg E, Claessens F, Vanderschueren D, Papapoulos S. Inhibition of cathepsin K for treatment of osteoporosis. Curr. Osteoporos. Rep. 10(1), 73–79 (2012).
  • Mcdougall JJ, Schuelert N, Bowyer J. Cathepsin K inhibition reduces CTXII levels and joint pain in the guinea pig model of spontaneous osteoarthritis. Osteoarthritis Cartilage 18(10), 1355–1357 (2010).
  • Hayami T, Zhuo Y, Wesolowski GA, Pickarski M, Duong LT. Inhibition of cathepsin K reduces cartilage degeneration in the anterior cruciate ligament transection rabbit and murine models of osteoarthritis. Bone 50(6), 1250–1259 (2012).
  • Duong Le T, Leung AT, Langdahl B. Cathepsin K inhibition: a new mechanism for the treatment of osteoporosis. Calcif. Tissue Int. 98(4), 381–397 (2016).
  • Blaney Davidson EN, Vitters EL, Van Der Kraan PM, Van Den Berg WB. Expression of transforming growth factor-beta (TGFbeta) and the TGFbeta signalling molecule SMAD-2P in spontaneous and instability-induced osteoarthritis: role in cartilage degradation, chondrogenesis and osteophyte formation. Ann. Rheum. Dis. 65(11), 1414–1421 (2006).
  • Shen J, Li S, Chen D. TGF-beta signaling and the development of osteoarthritis. Bone Res. 2, 14002 (2014).
  • Xie L, Tintani F, Wang X et al. Systemic neutralization of TGF-beta attenuates osteoarthritis. Ann. NY Acad. Sci. 1376(1), 53–64 (2016).
  • Goldring SR, Goldring MB. Changes in the osteochondral unit during osteoarthritis: structure, function and cartilage-bone crosstalk. Nat. Rev. Rheumatol. 12(11), 632–644 (2016).
  • Wu M, Chen G, Li YP. TGF-beta and BMP signaling in osteoblast, skeletal development, and bone formation, homeostasis and disease. Bone Res. 4, 16009 (2016).
  • Macnabb C, Patton D, Hayes JS. Sclerostin antibody therapy for the treatment of osteoporosis: clinical prospects and challenges. J. Osteoporos. 2016, 6217286 (2016).
  • Roudier M, Li X, Niu QT et al. Sclerostin is expressed in articular cartilage but loss or inhibition does not affect cartilage remodeling during aging or following mechanical injury. Arthritis Rheum. 65(3), 721–731 (2013).
  • Bouaziz W, Funck-Brentano T, Lin H et al. Loss of sclerostin promotes osteoarthritis in mice via beta-catenin-dependent and -independent Wnt pathways. Arthritis Res. Ther. 17, 24 (2015).
  • Wehmeyer C, Frank S, Beckmann D et al. Sclerostin inhibition promotes TNF-dependent inflammatory joint destruction. Sci. Transl. Med. 8(330), 330ra335 (2016).
  • Koelling S, Kruegel J, Irmer M et al. Migratory chondrogenic progenitor cells from repair tissue during the later stages of human osteoarthritis. Cell Stem Cell 4(4), 324–335 (2009).
  • Harris Q, Seto J, O’brien K et al. Monocyte chemotactic protein-1 inhibits chondrogenesis of synovial mesenchymal progenitor cells: an in vitro study. Stem Cells 31(10), 2253–2265 (2013).
  • Min BH, Choi WH, Lee YS et al. Effect of different bone marrow stimulation techniques (BSTs) on MSCs mobilization. J. Orthop. Res. 31(11), 1814–1819 (2013).
  • Kanbe K, Takagishi K, Chen Q. Stimulation of matrix metalloprotease 3 release from human chondrocytes by the interaction of stromal cell-derived factor 1 and CXC chemokine receptor 4. Arthritis Rheum. 46(1), 130–137 (2002).
  • Dong Y, Liu H, Zhang X et al. Inhibition of SDF-1alpha/CXCR4 signalling in subchondral bone attenuates post-traumatic osteoarthritis. Int. J. Mol. Sci. 17(6), 943 (2016).
  • Smith BD, Grande DA. The current state of scaffolds for musculoskeletal regenerative applications. Nat. Rev. Rheumatol. 11(4), 213–222 (2015).
  • Dhillon RS, Schwarz EM, Maloney MD. Platelet-rich plasma therapy - future or trend? Arthritis Res. Ther. 14(4), 219 (2012).
  • Moraes VY, Lenza M, Tamaoki MJ, Faloppa F, Belloti JC. Platelet-rich therapies for musculoskeletal soft tissue injuries. Cochrane Database Syst. Rev. (4), CD010071 (2014).
  • Sanchez M, Anitua E, Delgado D et al. A new strategy to tackle severe knee osteoarthritis: combination of intra-articular and intraosseous injections of platelet rich plasma. Expert Opin. Biol. Ther. 16(5), 627–643 (2016).
  • Philippart P, Meuleman N, Stamatopoulos B et al. In vivo production of mesenchymal stromal cells after injection of autologous platelet-rich plasma activated by recombinant human soluble tissue factor in the bone marrow of healthy volunteers. Tissue Eng. Part A 20(1–2), 160–170 (2014).
  • Tan HB, Giannoudis PV, Boxall SA, Mcgonagle D, Jones E. The systemic influence of platelet-derived growth factors on bone marrow mesenchymal stem cells in fracture patients. BMC Med. 13, 6 (2015).
  • Cassano JM, Kennedy JG, Ross KA, Fraser EJ, Goodale MB, Fortier LA. Bone marrow concentrate and platelet-rich plasma differ in cell distribution and interleukin 1 receptor antagonist protein concentration. Knee Surg. Sports Traumatol. Arthrosc. doi:10.1007/s00167-016-3981-9 (2016) ( Epub ahead of print).
  • Banerjee S, Issa K, Pivec R, Kapadia BH, Khanuja HS, Mont MA. Osteonecrosis of the hip: treatment options and outcomes. Orthop. Clin. North. Am. 44(4), 463–476 (2013).
  • Cohen SB, Sharkey PF. Subchondroplasty for treating bone marrow lesions. J. Knee Surg. 29(7), 555–563 (2016).
  • Felson DT, Parkes MJ, Marjanovic EJ et al. Bone marrow lesions in knee osteoarthritis change in 6–12 weeks. Osteoarthritis Cartilage 20(12), 1514–1518 (2012).
  • Muinos-Lopez E, Delgado D, Sanchez P et al. Modulation of synovial fluid-derived mesenchymal stem cells by intra-articular and intraosseous platelet rich plasma administration. Stem Cells Int. 2016, 1247950 (2016).