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Cytoskeleton and Proteoglycan Synthesis in Chondrocytes Under Hydrostatic Pressure

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Book cover Advances in Osteoarthritis

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Summary

Articular cartilage is normally subject to various magnitudes of pressures which control the content of matrix proteoglycans (PGs). Short-term cyclic hydrostatic pressurization (5MPa, 1.5 h) stimulated PG synthesis in chondrocytes embedded in their natural environment in explants, but inhibited it when maintained in monolayer cultures. In long-term cyclic pressurization (5MPa, 20h), the inhibiting response of the cell cultures was reversed to stimulation. Continuous 30MPa pressure reduced total PG synthesis and the steady-state mRNA level of aggrecan, while continuous 5MPa pressure had no effect. Increased size of aggrecans, secreted under continuous 30MPa pressure, was observed. Continuous 30MPa hydrostatic pressure led to a reversible disorganization of microtubules, and the Golgi apparatus was packed into a perinuclear clump of vesicles. After depolymerization of the microtubules, pressurization did not influence the appearance of the Golgi apparatus or PG secretion. High hydrostatic pressure inhibited the organization of microfilaments and induced heat-shock protein 70 expression both at the mRNA and protein level. The results demonstrate that hydrostatic pressure controls the synthesis and structure of PGs in cultured chondrocytes. The simultaneous cytoskeletal changes may participate in the regulation of PG synthesis and secretion. The results further suggest that microtubules are important for PG metabolism. Hydrostatic pressure may control PG synthesis both at transcriptional and translational/posttranslational levels of biosynthesis.

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References

  1. Tammi M, Paukkonen K, Kiviranta I, et al (1987) Joint loading-induced alterations in articular cartilage. In: Helminen HJ, Kiviranta I, Tammi, M, et al (eds) Joint loading—Biology and health of articular structures. Wright & Sons, Bristol, pp 64–88

    Google Scholar 

  2. Helminen HJ, Kiviranta I, Säämänen A-M, et al (1992) Effect of motion and load on articular cartilage in animal models. In: Kuettner K, Schleyerbach R, Peyron JG, Hascall VC (eds) Articular cartilage and osteoarthritis. Raven Press, New York, pp 501–510

    Google Scholar 

  3. Sandberg M, Vuorio E (1987) Localization of types I, II and III collagen mRNAs in developing human skeletal tissues by in situ hybridization. J Cell Biol 104:1077–1084

    Article  PubMed  CAS  Google Scholar 

  4. Goetinck PF, Kiss I, Deâk F, et al (1990) Macromolecular organization of the extracellular matrix of cartilage. Ann NY Acad Sci 599:29–38

    Article  PubMed  CAS  Google Scholar 

  5. Mundlos S, Meyer R, Yamada Y, et al (1991) Distribution of cartilage proteoglycan (aggrecan) core protein and link protein gene expression during human skeletal development. Matrix 11:339–346

    PubMed  CAS  Google Scholar 

  6. Glumoff V, Savontaus M, Vehanen J, et al (1994) Analysis of aggrecan and tenascin gene expression in mouse skeletal tissues by Northern and in situ hybridization using specific cDNA probes. Biochim Biophys Acta 1219:613–622

    PubMed  Google Scholar 

  7. Bianco P, Fisher LW, Young MF, et al (1990) Expression and localization of the two small proteoglycans biglycan and decorin in developing human skeletal and non-skeletal tissues. J Histochem Cytochem 38:1549–1563

    Article  PubMed  CAS  Google Scholar 

  8. Weigel PH, Hascall VC, Tammi M (1997) Hyaluronan synthases. J Biol Chem 272:13997–14000

    Article  PubMed  CAS  Google Scholar 

  9. Hascall VC, Handley CJ, McQuillan DJ, et al (1983) The effect of serum on biosynthesis of proteoglycans by bovine articular cartilage in culture. Arch Biochem Biophys 224:206–223

    Article  PubMed  CAS  Google Scholar 

  10. Morales TI, Hascall VC (1988) Correlated metabolism of proteoglycans and hyaluronic acid in bovine cartilage organ cultures. J Biol Chem 268:3632–3638

    Google Scholar 

  11. Ng CK, Handley CJ, Preston BN, et al (1992) The extracellular processing and catabolism of hyaluronan in cultured adult articular cartilage expiants. Arch Biochem Biophys 298:70–79

    Article  PubMed  CAS  Google Scholar 

  12. Haapala J, Lammi MJ, Inkinen RI, et al (1996) Coordinated regulation of hyaluronan and aggrecan content in the articular cartilage of immobilized and exercised dogs. J Rheumatol 23:1586–1593

    PubMed  CAS  Google Scholar 

  13. Mow VC, Ratcliffe A, Poole AR (1992) Cartilage and diarthrodial joints as paradigms for hierarchical materials and structures. Biomaterials 13:67–97

    Article  PubMed  CAS  Google Scholar 

  14. Rizkalla G, Reiner A, Bogoch E, et al (1992) Studies of the articular cartilage proteoglycan aggrecan in health and osteoarthritis. Evidence for molecular heterogeneity and extensive molecular changes in disease. J Clin Invest 90:2268–2277

    Article  PubMed  CAS  Google Scholar 

  15. Väätäinen U, Häkkinen T, Kiviranta I, et al (1995) Proteoglycan depletion and size reduction in lesions of early grade chondromalacia of the patella. Ann Rheum Dis 54:831–835

    Article  PubMed  Google Scholar 

  16. Sandy JD, Adams ME, Billingham MEJ, et al (1984) In vivo and in vitro stimulation of chondrocyte biosynthetic activity in early experimental osteoarthritis. Arthritis Rheum 27:388–397

    Article  PubMed  CAS  Google Scholar 

  17. Poole AR, Rizkalla G, Ionescu M, et al (1993) Osteoarthritis in the human knee: a dynamic process of cartilage matrix degradation, synthesis and reorganization. In: van den Berg WB, van der Kraan PM, van Lent PLEM (eds) Joint destruction in arthritis and osteoarthritis. Birkhäuser Verlag, Basel, pp 3–13

    Google Scholar 

  18. Palmoski MJ, Brandt KD (1984) Effects of static and cyclic compressive loading on articular cartilage plugs in vitro. Arthritis Rheum 27:675–681

    Article  PubMed  CAS  Google Scholar 

  19. Klämfeldt A (1985) Continuous mechanical pressure and joint tissue. Effect of synovial membrane products and indomethacin in vitro. Scand J Rheum 14:431–437

    Article  PubMed  Google Scholar 

  20. Schneiderman R, Keret D, Maroudas A (1986) Effects of mechanical and osmotic pressure on the rate of glycosaminoglycan synthesis in the human adult femoral head cartilage: an in vitro study. J Orthop Res 4:393–408

    Article  PubMed  CAS  Google Scholar 

  21. Gray ML, Pizzanelli AM, Grodzinsky AJ, et al (1988) Mechanical and physico-chemical determinants of the chondrocyte biosynthetic response. J Orthop Res 6:777–792

    Article  PubMed  CAS  Google Scholar 

  22. Sah RL, Kim Y-J, Doong J-Y, et al (1989) Biosynthetic response of cartilage expiants to dynamic compression. J Orthop Res 7:619–636

    Article  PubMed  CAS  Google Scholar 

  23. Guilak F, Meyer BC, Ratcliffe A, et al (1991) The effect of static loading on proteoglycan biosynthesis and turnover in articular cartilage expiants. Trans Orthop Res Soc 16:50

    Google Scholar 

  24. Larsson T, Aspden RM, Heinegârd D (1991) Effects of mechanical load on cartilage matrix biosynthesis in vitro. Matrix 11:388–394

    PubMed  CAS  Google Scholar 

  25. Sah RL, Doong J-Y, Grodzinsky AJ, et al (1991) Effects of compression on the loss of newly synthesized proteoglycans and proteins from cartilage expiants. Arch Biochem Biophys 286:20–29

    Article  PubMed  CAS  Google Scholar 

  26. Korver THV, van de Stadt RJ, Kiljan E, et al (1992) Effects of loading on the synthesis of proteoglycans in different layers of anatomically intact articular cartilage in vitro. J Rheum 19:905–912

    PubMed  CAS  Google Scholar 

  27. Parkkinen JJ, Lammi MJ, Helminen HJ, et al (1992) Local stimulation of proteoglycan synthesis in articular cartilage expiants by dynamic compression in vitro. J Orthop Res 10:610–620

    Article  PubMed  CAS  Google Scholar 

  28. Lee RC, Rich JB, Kelley KM, et al (1982) A comparison of in vitro cellular responses to mechanical and electrical stimulation. Am Surg 48:567–574

    PubMed  CAS  Google Scholar 

  29. de Witt MT, Handley CJ, Oakes BW, et al (1984) In vitro response of chondrocytes to mechanical loading. The effect of short term mechanical tension. Connect Tissue Res 12:97–109

    Article  PubMed  Google Scholar 

  30. Uchida A, Yamashita K, Hashimoto K, et al (1988) The effect of mechanical stress on cultured growth cartilage cells. Connect Tissue Res 17:305–311

    Article  PubMed  CAS  Google Scholar 

  31. Parkkinen JJ, Lammi MJ, Tammi MI, et al (1994) Proteoglycan synthesis and cytoskeleton in hydrostatically loaded chondrocytes. In: Mow VC, Guilak F, Tran-Son-Tay R, Hochsmuth RM (eds) Cell mechanics and cellular engineering. Springer-Verlag, New York, pp 420–444

    Chapter  Google Scholar 

  32. Imamura K, Ozawa H, Hiraide T, et al (1990) Continuously applied compressive pressure induces bone resorption by a mechanism involving prostaglandin E2 synthesis. J Cell Physiol 144:222–228

    Article  PubMed  CAS  Google Scholar 

  33. Ozawa H, Imamura K, Abe E, et al (1990) Effect of a continuously applied compressive pressure on mouse osteoblast-like cells (MC3T3-E1) in vitro. J Cell Physiol 142:177–185

    Article  PubMed  CAS  Google Scholar 

  34. Quinn RS, Rodan GA (1981) Enhancement of ornithine decarboxylase and Na+, K+ ATPase in osteoblastoma cells by intermittent compression. Biochem Biophys Res Commun 100:1696–1702

    Google Scholar 

  35. Goldinger JM, Kang BS, Choo YE, et al (1980) Effect of hydrostatic pressure on ion transport and metabolism in human erythrocytes. J Appl Physiol 49:224–231

    PubMed  CAS  Google Scholar 

  36. Heremans K (1982) High pressure effects on proteins and other biomolecules. Annu Rev Biophys Bioeng 11:1–21

    Article  PubMed  CAS  Google Scholar 

  37. Varga S, Mullner N, Pikula S, et al (1986) Pressure effects on sarcoplasmic reticulum. J Biol Chem 261:13943–13956

    PubMed  CAS  Google Scholar 

  38. Zimmerman AM, Tahir S, Zimmerman S (1987) Macromolecular synthesis under hydrostatic pressure. In: Jannasch HW, Marquis RE, Zimmerman AM (eds) Current perspectives in high pressure biology. Academic Press, London, pp 49–63

    Google Scholar 

  39. Heinemann SH, Conti F, Stuhmer W, et al (1989) Effects of hydrostatic pressure on membrane processes. J Gen Physiol 90:765–778

    Article  Google Scholar 

  40. Kavecansky J, Dannenberg AJ, Zakim D (1992) Effects of high pressure on the catalytic and regulatory properties of UDP-glucuronosyltransferase in intact microsomes. Biochemistry 31:162–168

    Article  PubMed  CAS  Google Scholar 

  41. Acevedo AD, Bowser SS, Gerritsen ME, et al (1993) Morphological and proliferative responses of endothelial cells to hydrostatic pressure: role of fibroblast growth factor. J Cell Physiol 157:603–614

    Article  PubMed  CAS  Google Scholar 

  42. Haskin C, Cameron I (1993) Physiological levels of hydrostatic pressure alter morphology and organization of cytoskeletal and adhesion proteins in MG-63 osteosarcoma cells. Biochem Cell Biol 71:27–35

    Article  PubMed  CAS  Google Scholar 

  43. Crenshaw HC, Allen JA, Skeen V, et al (1996) Hydrostatic pressure has different effects on the assembly of tubulin, actin, myosin II, vinculin, talin, vimentin and cytokeratin in mammalian cells. Exp Cell Res 227:285–297

    Article  PubMed  CAS  Google Scholar 

  44. Parkkinen JJ, Ikonen J, Lammi MJ, et al (1993) Effects of cyclic hydrostatic pressure on proteoglycan synthesis in cultured chondrocytes and articular cartilage expiants. Arch Biochem Biophys 300:458–465

    Article  PubMed  CAS  Google Scholar 

  45. Lammi MJ, Inkinen R, Parkkinen JJ, et al (1994) Expression of reduced amounts of structurally altered aggrecan in articular cartilage chondrocytes subjected to high hydrostatic pressure. Biochem J 304:723–730

    PubMed  CAS  Google Scholar 

  46. Takahashi K, Kubo T, Kobayashi K, et al (1997) Hydrostatic pressure influences mRNA expression of transforming growth factor-1 and heat shock protein 70 in chondrocyte-like cell line. J Orthop Res 15:150–158

    Article  PubMed  CAS  Google Scholar 

  47. Parkkinen JJ, Lammi MJ, Inkinen R, et al (1995) Influence of short-term hydrostatic pressure on stress fiber organization in cultured chondrocytes. J Orthop Res 13:495–502

    Article  PubMed  CAS  Google Scholar 

  48. Parkkinen JJ, Lammi MJ, Pelttari A, et al (1993) Altered Golgi apparatus in hydrostatically loaded articular cartilage chondrocytes. Ann Rheum Dis 52:192–198

    Article  PubMed  CAS  Google Scholar 

  49. Frank EH, Grodzinsky AJ (1987) Cartilage electromechanics. I. Electrokinetic transduction and effects of electrolyte pH and ionic strength. J Biomech 20:615–627

    Article  PubMed  CAS  Google Scholar 

  50. O’Connor P, Orford R, Gardner DL (1988) Differential response to compressive loads of zones of canine hyaline articular cartilage: micromechanical, light and electron microscopic studies. Ann Rheum Dis 47:414–420

    Article  PubMed  Google Scholar 

  51. Jannasch HW, Marquis RE, Zimmerman AM (1987) Current perspectives in high pressure biology. Academic Press, London

    Google Scholar 

  52. Urban JPG, Hall AC, Gehl KA (1993) Regulation of matrix synthesis rates by the ionic environment of articular chondrocytes. J Cell Physiol 154:262–270

    Article  PubMed  CAS  Google Scholar 

  53. Smith RL, Rusk SF, Ellison BE, et al (1996) In vitro stimulation of articular chondrocyte mRNA and extracellular matrix synthesis by hydrostatic pressure. J Orthop Res 14:50–60

    Google Scholar 

  54. Lohmander LS, Shinomura T, Hascall VC, et al (1989) Xylosyl transfer to the core protein precursor of the rat chondrosarcoma proteoglycan. J Biol Chem 264:18775–18780

    PubMed  CAS  Google Scholar 

  55. Parkkinen JJ, Lammi MJ, Pelttari A, et al (1993) Hydrostatic pressure modulates the organization of the cytoskeleton and Golgi apparatus in cultured chondrocytes. Trans Orthop Res Soc 18:617

    Google Scholar 

  56. Curtis AJ, Devenish RJ, Handley CJ (1992) Modulation of aggrecan and link-protein synthesis in articular cartilage. Biochem J 288:721–726

    PubMed  CAS  Google Scholar 

  57. Bagchi T, Larson DE, Sells BH (1987) Cytoskeletal association of muscle-specific mRNAs in differentiating L6 rat myoblasts. Exp Cell Res 168:160–172

    Article  PubMed  CAS  Google Scholar 

  58. Symington AL, Zimmerman S, Stein J, et al (1991) Hydrostatic pressure influences histone mRNA. J Cell Sci 98:123–129

    PubMed  CAS  Google Scholar 

  59. Takano KJ, Takano T, Yamanouchi Y, et al (1997) Pressure-induced apoptosis in human lymphoblasts. Exp Cell Res 235:155–160

    Article  PubMed  CAS  Google Scholar 

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Author information

Authors and Affiliations

  1. Department of Pathology, University of Kuopio, P.O. Box 1627, FIN-70211, Kuopio, Finland

    Jyrki J. Parkkinen

  2. Department of Anatomy, University of Kuopio, P.O. Box 1627, FIN-70211, Kuopio, Finland

    Mikko J. Lammi, Matti O. Jortikka, Ritva I. Inkinen, Kai Kaarniranta, Heikki J. Helminen & Markku I. Tammi

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Editors and Affiliations

  1. Kinki University School of Medicine, 377-2 Ohno-Higashi, Osaka-Sayama, 589-8511, Osaka, Japan

    Seisuke Tanaka M.D. (Dean) (Dean)

  2. Department of Orthopedic Surgery, Kinki University School of Medicine, 377-2 Ohno-Higashi, Osaka-Sayama, 589-8511, Osaka, Japan

    Chiaki Hamanishi M.D. (Professor) (Professor)

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© 1999 Springer-Verlag Tokyo

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Parkkinen, J.J. et al. (1999). Cytoskeleton and Proteoglycan Synthesis in Chondrocytes Under Hydrostatic Pressure. In: Tanaka, S., Hamanishi, C. (eds) Advances in Osteoarthritis. Springer, Tokyo. https://doi.org/10.1007/978-4-431-68497-8_2

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  • DOI: https://doi.org/10.1007/978-4-431-68497-8_2

  • Publisher Name: Springer, Tokyo

  • Print ISBN: 978-4-431-68499-2

  • Online ISBN: 978-4-431-68497-8

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