Knee loading reduces MMP13 activity in the mouse cartilage

详细信息    查看全文

• 作者：Kazunori Hamamura (1)
  Ping Zhang (1) (2)
  Liming Zhao (1)
  Joon W Shim (1)
  Andy Chen (1)
  Todd R Dodge (1)
  Qiaoqiao Wan (1)
  Han Shih (1)
  Sungsoo Na (1)
  Chien-Chi Lin (1)
  Hui Bin Sun (3)
  Hiroki Yokota (1) (4)
  
• 关键词：Knee loading ; Cartilage ; Chondrocyte ; Osteoarthritis ; MMP13 ; Rac1
• 刊名：BMC Musculoskeletal Disorders
• 出版年：2013
• 出版时间：December 2013
• 年：2013
• 卷：14
• 期：1
• 全文大小：1,046 KB
• 参考文献：1. Zhang P, Sun Q, Turner CH, Yokota H: Knee loading accelerates bone healing in mice. / J Bone Miner Res 2007, 22:1979-987. CrossRef
  2. Shim JW, Hamamura K, Chen A, Wan Q, Na S, Yokota H: Rac1 mediates load-driven attenuation of mRNA expression of nerve growth factor beta in cartilage and chondrocytes. / J Musculoskeletal Neuro Interac 2013, 13:334-41.
  3. Responte DJ, Lee JK, Hu JC, Athanasiou KA: Biomechanics-driven chondrogenesis: from embryo to adult. / FASEB J 2012, 26:3614-624. CrossRef
  4. Leong DJ, Hardin JA, Cobelli NJ, Sun HB: Mechanotransduction and cartilage integrity. / Ann N Y Acad Sci 2011, 1240:32-7. CrossRef
  5. Fink B, Egl M, Singer J, Fuerst M, Bubenheim M, Neuen-Jacob E: Morphologic changes in the vastus medialis muscle in patients with osteoarthritis of the knee. / Arthritis Rheum 2007, 56:3626-633. CrossRef
  6. Zhang P, Su M, Tanaka SM, Yokota H: Knee loading stimulates cortical bone formation in murine femurs. / BMC Musculoskelet Disord 2006, 7:73. CrossRef
  7. Zhang P, Tanaka SM, Sun Q, Turner CH, Yokota H: Frequency-dependent enhancement of bone formation in murine tibiae and femora with knee loading. / J Bone Miner Metab 2007, 25:383-91. CrossRef
  8. Zhang P, Yokota H: Knee loading stimulates healing of mouse bone wounds in a femur neck. / Bone 2011, 49:867-72. CrossRef
  9. Zhang P, Turner CH, Yokota H: Joint loading-driven bone formation and signaling pathways predicted from genome-wide expression profiles. / Bone 2009, 44:989-98. CrossRef
  10. Zhang P, Su M, Liu Y, Hsu A, Yokota H: Knee loading dynamically alters intramedullary pressure in mouse femora. / Bone 2007, 40:538-43. CrossRef
  11. Zhang P, Yokota H: Effects of surgical holes in mouse tibiae on bone formation induced by knee loading. / Bone 2007, 40:1320-328. CrossRef
  12. Warden SJ: Breaking the rules for bone adaptation to mechanical loading. / J Appl Physiol 2006, 100:1441-442. CrossRef
  13. Hamamura K, Goldring MB, Yokota H: Involvement of p38 MAPK in regulation of MMP13 mRNA in chondrocytes in response to surviving stress to endoplasmic reticulum. / Arch Oral Biol 2009, 54:279-86. CrossRef
  14. Mengshol JA, Vincenti MP, Coon CI, Barchowsky A, Brinckerhoff CE: Inrerleukin-1 induction of collagenase 3 (matrix metalloproteinase 13) gene expression in chondrocytes requires p38, c-Jun N-terminal kinase, and nuclear factor kappaB: differential regulation of collagenase 1 and collagenase3. / Arthritis Rheum 2000, 43:801-11. CrossRef
  15. Tzima E: Role of small GTPases in endothelial cytoskeletal dynamics and the shear stress response. / Circ Res 2006, 98:176-85. CrossRef
  16. Wang G, Beier F: Rac1/Cdc42 and RhoA GTPases antagonistically regulate chondrocyte proliferation, hypertrophy, and apoptosis. / J Bone Miner Res 2005, 20:1022-031. CrossRef
  17. Kamekura S, Hoshi K, Shimoaka T, Chung U, Chikuda H, Chikuda H, Yamada T, Uchida M, Ogata N, Seichi A, Nakamura K, Kawaguchi H: Osteoarthritis development in novel experimental mouse models induced by knee joint instability. / Osteoarthritis Cartilage 2005, 13:632-41. CrossRef
  18. Chambers MG, Cox L, Chong L, Suri N, Cover P, Bayliss MT, Mason RM: Matrix metalloproteinases and aggrecanases cleave aggrecan in different zones of normal cartilage but colocalize in the development of osteoarthritis lesions in STR/ort mice. / Arthritis Rheum 2001, 44:1455-465. CrossRef
  19. Yokota H, Goldring MB, Sun HB: CITED2-mediated regulation of MMP-1 and MMP-13 in human chondrocytes under flow shear. / J Biol Chem 2003, 278:47275-7280. CrossRef
  20. Hamamura K, Lin CC, Yokota H: Salubrinal reduces expression and activity of MMP13 in chondrocytes. / Osteoarthritis Cartilage 2013, 21:764-72. CrossRef
  21. Ohno S, Im HJ, Knudson CB, Knudson W: Hyaluronan oligosaccharides induce matrix metalloproteinase 13 via transcriptional activation of NFkappaB and p38 MAP kinase in articular chondrocytes. / J Biol Chem 2006, 281:17952-7960. CrossRef
  22. Li Q, Ho CS, Marinescu V, Bhatti H, Bokoch GM, Ernst SA, Holz RW, Stuenkel EL: Facilitation of Ca(2+)-dependent exocytosis by Rac1-GTPase in bovine chromaffin cells. / J Physiol 2003, 550:431-45. CrossRef
  23. Liu L, Zong C, Li B, Shen D, Tang Z, Chen J, Zheng Q, Tong X, Gao C, Wang J: The interaction between β1 integrins and ERK1/2 in osteogenic differentiation of human mesenchymal stem cells under fluid shear stress modelled by a perfusion system. / J Tissue Eng Regen Med 2012. doi:10.1002/term.1498
  24. Tanaka SM, Sun HB, Roeder RK, Burr DB, Turner CH, Yokota H: Osteoblast responses one hour after load-induced fluid flow in a three-dimensional porous matrix. / Calcif Tissue Int 2005, 76:261-71. CrossRef
  25. Hamamura K, Swarnkar G, Tanjung N, Cho E, Li J, Na S, Yokota H: RhoA-mediated signaling in mechanotransduction of osteoblasts. / Connect Tissue Res 2012, 53:398-06. CrossRef
  26. Woods A, Pala D, Kennedy L, McLean S, Rockel JS, Wang G, Leask A, Beier F: Rac1 signaling regulates CTGF/CCN2 gene expression via TGFbeta/Smad signaling in chondrocytes. / Osteoarthritis Cartilage 2009, 17:406-13. CrossRef
  27. Wang G, Yan Q, Woods A, Aubrey LA, Feng Q, Beier F: Inducible nitric oxide synthase-nitric oxide signaling mediates the mitogenic activity of Rac1 during endochondral bone growth. / J Cell Sci 2011, 124:3405-413. CrossRef
  28. Long DL, Willey JS, Loeser RF: Rac1 is required for matrix metalloproteinase 13 production by chondrocytes in response to fibronectin fragments. / Arthritis Rheum 2013, 65:1561-568. CrossRef
  29. Akhtar N, Rasheed Z, Ramamurthy S, Anbazhagan AN, Voss FR, Haqqi TM: MicroRNA-27b regulates the expression of matrix metalloproteinase 13 in human osteoarthritis chondrocytes. / Arthritis Rheum 2010, 62:1361-371. CrossRef
  30. Zhang Y, Gong LH, Zhang HQ, Du Q, You JF, Tian XX, Fang WG: Extracellular ATP enhances in vitro invasion of prostate cancer cells by activating Rho GTPase and upregulating MMPs expression. / Cancer Lett 2010, 293:189-97. CrossRef
  31. Nakagawa K, Teramura T, Takehara T, Onodera Y, Hamanishi C, Akagi M, Fukuda K: Cyclic compression-induced p38 activation and subsequent MMP13 expression requires Rho/ROCK activity in bovine cartilage explants. / Inflamm Res 2012, 61:1093-100. CrossRef
  32. Leung R, Wang Y, Cuddy K, Sun C, Magalhaes J, Grynpas M, Glogauer M: Filamin A regulates monocyte migration through Rho small GTPases during osteoclastogenesis. / J Bone Miner Res 2010, 25:1077-091.
  33. Nam J, Perera P, Liu J, Wu LC, Rath B, Butterfield TA, Agarwal S: Transcriptome-wide gene regulation by gentle treadmill walking during the progression of monoiodoacetate-induced arthritis. / Arthritis Rheum 2011, 63:1613-625. CrossRef
  34. Nam J, Aguda BD, Rath B, Agarwal S: Biomechanical thresholds regulate inflammation through the NF-kappaB pathway: experiments and modeling. / PLoS One 2009, 4:e5262. CrossRef
  35. The pre-publication history for this paper can be accessed here:http://www.biomedcentral.com/1471-2474/14/312/prepub
  
• 作者单位：Kazunori Hamamura (1)
  Ping Zhang (1) (2)
  Liming Zhao (1)
  Joon W Shim (1)
  Andy Chen (1)
  Todd R Dodge (1)
  Qiaoqiao Wan (1)
  Han Shih (1)
  Sungsoo Na (1)
  Chien-Chi Lin (1)
  Hui Bin Sun (3)
  Hiroki Yokota (1) (4)
  
  1. Department of Biomedical Engineering, Indiana University Purdue University Indianapolis, SL220C, 723 West Michigan Street, Indianapolis, IN 46202, USA
  2. School of Basic Medical Sciences, Tianjin Medical University, Tanjin, 300070, People’s Republic of China
  3. Department of Orthopaedic Surgery, Albert Einstein College of Medicine, Bronx, NY 10461, USA
  4. Department of Anatomy and Cell Biology, Indiana University School of Medicine, Indianapolis, IN 46202, USA
  
• ISSN：1471-2474

文摘

Background Moderate loads with knee loading enhance bone formation, but its effects on the maintenance of the knee are not well understood. In this study, we examined the effects of knee loading on the activity of matrix metalloproteinase13 (MMP13) and evaluated the role of p38 MAPK and Rac1 GTPase in the regulation of MMP13. Methods Knee loading (0.5-?N for 5?min) was applied to the right knee of surgically-induced osteoarthritis (OA) mice as well as normal (non-OA) mice, and MMP13 activity in the femoral cartilage was examined. The sham-loaded knee was used as a non-loading control. We also employed primary non-OA and OA human chondrocytes as well as C28/I2 chondrocyte cells, and examined MMP13 activity and molecular signaling in response to shear at 2-0?dyn/cm2. Results Daily knee loading at 1?N for 2?weeks suppressed cartilage destruction in the knee of OA mice. Induction of OA elevated MMP13 activity and knee loading at 1?N suppressed this elevation. MMP13 activity was also increased in primary OA chondrocytes, and this increase was attenuated by applying shear at 10?dyn/cm2. Load-driven reduction in MMP13 was associated with a decrease in the phosphorylation level of p38 MAPK (p-p38) and NFκB (p-NFκB). Molecular imaging using a fluorescence resonance energy transfer (FRET) technique showed that Rac1 activity was reduced by shear at 10?dyn/cm2 and elevated by it at 20?dyn/cm2. Silencing Rac1 GTPase significantly reduced MMP13 expression and p-p38 but not p-NFκB. Transfection of a constitutively active Rac1 GTPase mutant increased MMP13 activity, while a dominant negative mutant decreased it. Conclusions Knee loading reduces MMP13 activity at least in part through Rac1-mediated p38 MAPK signaling. This study suggests the possibility of knee loading as a therapy not only for strengthening bone but also preventing tissue degradation of the femoral cartilage.