Osteoarthritis and Cartilage
Volume 17, Issue 7 , Pages 906-916 , July 2009

Hyaluronan promotes the chondrocyte response to BMP-7

  • R.A. Andhare

      Affiliations

    • Department of Biochemistry, Rush Medical College, Rush University Medical Center, Chicago, IL, USA
    • Department of Oral Biology, University of Illinois, Chicago, IL, USA
    • ,
  • N. Takahashi

      Affiliations

    • Department of Anatomy and Cell Biology, Brody School of Medicine, East Carolina University, Greenville, NC, USA
    • ,
  • W. Knudson

      Affiliations

    • Department of Anatomy and Cell Biology, Brody School of Medicine, East Carolina University, Greenville, NC, USA
    • ,
  • C.B. Knudson

      Affiliations

    • Department of Biochemistry, Rush Medical College, Rush University Medical Center, Chicago, IL, USA
    • Department of Anatomy and Cell Biology, Brody School of Medicine, East Carolina University, Greenville, NC, USA
    • Corresponding Author InformationAddress correspondence and reprint requests to: C. B. Knudson, Department of Anatomy and Cell Biology, Brody School of Medicine, East Carolina University, 600 Moye Blvd, Greenville, NC, 27834, USA. Tel: 1-252-744-2851; Fax: 1-252-744-2850.

Received 22 February 2008 ,Accepted 17 December 2008.

References 

  1. Hardingham TE, Fosang AJ. Proteoglycans: many forms and many functions. FASEB J. 1992;6:861–870
  2. Knudson W, Knudson C. An update on hyaluronan and CD44 in cartilage. Curr Opin Orthop. 2004;15:369–375
  3. Knudson CB, Knudson W. Hyaluronan-binding proteins in development, tissue homeostasis and disease. FASEB J. 1993;7:1233–1241
  4. Nishida Y, Knudson CB, Nietfeld JJ, Margulis A, Knudson W. Antisense inhibition of hyaluronan synthase-2 in human articular chondrocytes inhibits proteoglycan retention and matrix assembly. J Biol Chem. 1999;274:21893–21899
  5. Toole BP. Hyaluronan: from extracellular glue to pericellular cue. Nat Rev Cancer. 2004;4:528–539
  6. Turley EA, Noble PW, Bourguignon LY. Signaling properties of hyaluronan receptors. J Biol Chem. 2002;277:4589–4592
  7. Reddi AH. Cartilage morphogenetic proteins: role in joint development, homoeostasis, and regeneration. Ann Rheum Dis. 2003;62(Suppl. 2):ii73–ii78
  8. Chubinskaya S, Kuettner KE. Regulation of osteogenic proteins by chondrocytes. Int J Biochem Cell Biol. 2003;35:1323–1340
  9. Nishida Y, Knudson CB, Kuettner KE, Knudson W. Osteogenic protein-1 promotes the synthesis and retention of extracellular matrix within bovine articular cartilage and chondrocyte cultures. Osteoarthritis Cartilage. 2000;8:127–136
  10. Nishida Y, Knudson CB, Eger W, Kuettner KE, Knudson W. Osteogenic protein-1 stimulates cell-associated matrix assembly by normal human articular chondrocytes. Arthritis Rheum. 2000;43:206–214
  11. Flechtenmacher J, Huch K, Thonar EJMA, Mollenhauer J, Davies SR, Schmid TM, et al. Recombinant human osteogenic protein 1 is a potent stimulator of the synthesis of cartilage proteoglycans and collagens by human articular chondrocytes. Arthritis Rheum. 1996;39:478–488
  12. Greenwald J, Groppe J, Gray P, Wiater E, Kwiatkowski W, Vale W, et al. The BMP7/ActRII extracellular domain complex provides new insights into the cooperative nature of receptor assembly. Mol Cell. 2003;11:605–617
  13. Miyazono K, Maeda S, Imamura T. BMP receptor signaling: transcriptional targets, regulation of signals, and signaling cross-talk. Cytokine Growth Factor Rev. 2005;16:251–263
  14. Macias-Silva M, Hoodless PA, Tang SJ, Buchwald M, Wrana JL. Specific activation of Smad1 signaling pathways by the BMP7 type I receptor, ALK2. J Biol Chem. 1998;273:25628–25636
  15. Ebisawa T, Tada K, Kitajima I, Tojo K, Sampath TK, Kawabata M, et al. Characterization of bone morphogenetic protein-6 signaling pathways in osteoblast differentiation. J Cell Sci. 1999;112:3519–3527
  16. Gazzerro E, Canalis E. Bone morphogenetic proteins and their antagonists. Rev Endocr Metab Disord. 2006;7:51–65
  17. Itoh S, ten Dijke P. Negative regulation of TGF-beta receptor/Smad signal transduction. Curr Opin Cell Biol. 2007;19:176–184
  18. Peterson RS, Andhare RA, Rousche KT, Knudson W, Wang W, Grossfield JB, et al. CD44 modulates Smad1 activation in the BMP-7 signaling pathway. J Cell Biol. 2004;166:1081–1091
  19. Knudson CB, Nofal GA, Pamintuan L, Aguiar DJ. The chondrocyte pericellular matrix: a model for hyaluronan-mediated cell-matrix interactions. Biochem Soc Trans. 1999;27:142–147
  20. Chow G, Knudson CB, Homandberg G, Knudson W. Increased expression of CD44 in bovine articular chondrocytes by catabolic cellular mediators. J Biol Chem. 1995;270:27734–27741
  21. Maltzman JS, Carman JA, Monroe JG. Role of EGR1 in regulation of stimulus-dependent CD44 transcription in B lymphocytes. Mol Cell Biol. 1996;16:2283–2294
  22. Fitzgerald KA, O'Neill LA. Characterization of CD44 induction by IL-1: a critical role for Egr-1. J Immunol. 1999;162:4920–4927
  23. Simpson MA, Wilson CM, Furcht LT, Spicer AP, Oegema TR, McCarthy JB. Manipulation of hyaluronan synthase expression in prostate adenocarcinoma cells alters pericellular matrix retention and adhesion to bone marrow endothelial cells. J Biol Chem. 2002;277:10050–10057
  24. Ohno S, Im HJ, Knudson CB, Knudson W. Hyaluronan oligosaccharide-induced activation of transcription factors in bovine articular chondrocytes. Arthritis Rheum. 2005;52:800–809
  25. Iacob S, Knudson CB. Hyaluronan fragments activate nitric oxide synthase and the production of nitric oxide by articular chondrocytes. Int J Biochem Cell Biol. 2006;38:123–133
  26. 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;281:17952–17960
  27. Kothapalli D, Flowers J, Xu T, Pure E, Assoian RK. Differential activation of ERK and Rac mediates the proliferative and anti-proliferative effects of hyaluronan and CD44. J Biol Chem. 2008;
  28. Pardali K, Kowanetz M, Heldin CH, Moustakas A. Smad pathway-specific transcriptional regulation of the cell cycle inhibitor p21(WAF1/Cip1). J Cell Physiol. 2005;204:260–272
  29. Thorne RF, Legg JW, Isacke CM. The role of the CD44 transmembrane and cytoplasmic domains in co-ordinating adhesive and signalling events. J Cell Sci. 2004;117:373–380
  30. Mori T, Kitano K, Terawaki SI, Maesaki R, Fukami Y, Hakoshima T. Structural basis for CD44 recognition by ERM proteins. J Biol Chem. 2008;283:29602–29612
  31. Runyan CE, Schnaper HW, Poncelet AC. The role of internalization in transforming growth factor beta1-induced Smad2 association with Smad anchor for receptor activation (SARA) and Smad2-dependent signaling in human mesangial cells. J Biol Chem. 2005;280:8300–8308
  32. Chen YG, Wang Z, Ma J, Zhang L, Lu Z. Endofin, a FYVE domain protein, interacts with Smad4 and facilitates transforming growth factor-beta signaling. J Biol Chem. 2007;282:9688–9695
  33. Shi W, Chang C, Nie S, Xie S, Wan M, Cao X. Endofin acts as a Smad anchor for receptor activation in BMP signaling. J Cell Sci. 2007;120:1216–1224
  34. Ye L, Lewis-Russell JM, Kynaston H, Jiang WG. Endogenous bone morphogenetic protein-7 controls the motility of prostate cancer cells through regulation of bone morphogenetic protein antagonists. J Urol. 2007;178:1086–1091
  35. Lin J, Patel SR, Wang M, Dressler GR. The cysteine-rich domain protein KCP is a suppressor of transforming growth factor beta/activin signaling in renal epithelia. Mol Cell Biol. 2006;26:4577–4585
  36. Takada T, Katagiri T, Ifuku M, Morimura N, Kobayashi M, Hasegawa K, et al. Sulfated polysaccharides enhance the biological activities of bone morphogenetic proteins. J Biol Chem. 2003;278:43229–43235
  37. Irie A, Habuchi H, Kimata K, Sanai Y. Heparan sulfate is required for bone morphogenetic protein-7 signaling. Biochem Biophys Res Commun. 2003;308:858–865
  38. Paine-Saunders S, Viviano BL, Economides AN, Saunders S. Heparan sulfate proteoglycans retain Noggin at the cell surface: a potential mechanism for shaping bone morphogenetic protein gradients. J Biol Chem. 2002;277:2089–2096
  39. Niikura T, Reddi AH. Differential regulation of lubricin/superficial zone protein by transforming growth factor beta/bone morphogenetic protein superfamily members in articular chondrocytes and synoviocytes. Arthritis Rheum. 2007;56:2312–2321
  40. Shintani N, Hunziker EB. Chondrogenic differentiation of bovine synovium: bone morphogenetic proteins 2 and 7 and transforming growth factor beta1 induce the formation of different types of cartilaginous tissue. Arthritis Rheum. 2007;56:1869–1879
  41. Li T-F, Darowish M, Zuscik MJ, Chen D, Schwarz EM, Rosier RN, et al. Smad3-deficient chondrocytes have enhanced BMP signaling and accelerated differentiation. J Bone Miner Res. 2006;21:4–16
  42. Homandberg G, Meyers R, Xie DL. Fibronectin fragments cause chondrolysis of bovine articular cartilage slices in culture. J Biol Chem. 1992;267:3597–3604
  43. Knudson W, Casey B, Nishida Y, Eger W, Kuettner KE, Knudson CB. Hyaluronan oligosaccharides perturb cartilage matrix homeostasis and induce chondrogenic chondrolysis. Arthritis Rheum. 2000;43:1165–1174
  44. Nagano O, Saya H. Mechanism and biological significance of CD44 cleavage. Cancer Sci. 2004;95:930–935

PII: S1063-4584(08)00380-4

doi: 10.1016/j.joca.2008.12.007

Osteoarthritis and Cartilage
Volume 17, Issue 7 , Pages 906-916 , July 2009

Article Tools

* Image Usage & Resolution