Mechanisms of beneficial effects of high molecular weight hyaluronan on cultured cartilage tissue

Current Rheumatology Reviews

Volumn 2, Issue 1, 2006, Pages 23-30

  Homandberg, Gene A ^a  

^a UNIVERSITY OF NORTH DAKOTA SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

Author keywords

Anabolic; Cartilage; Catabolic; Damage; Hyaluronan; Hyaluronic acid; Repair

Indexed keywords

CYTOKINE; HYALURONIC ACID; NITRIC OXIDE;

ANTIOXIDANT ACTIVITY; CARTILAGE CELL; CARTILAGE DEGENERATION; CARTILAGE MATRIX; CHONDROPROTECTION; CULTURE MEDIUM; DISEASE MODEL; DRUG EFFICACY; DRUG INDICATION; DRUG MECHANISM; HUMAN; IN VITRO STUDY; MOLECULAR WEIGHT; OSTEOARTHRITIS; PRIORITY JOURNAL; REVIEW; TISSUE CULTURE; TISSUE METABOLISM; TISSUE STRUCTURE;

EID: 33745876227     PISSN: 15733971     EISSN: None     Source Type: Journal    
DOI: 10.2174/157339706775696973     Document Type: Review

References (82)

1. Kim NH, Han CD, Lee HM, Yang IH. Effect of sodium hyaluronate on prevention of OA. Yonsei Med J 1991; 32: 139-46.
2. Creamer P, Dieppe PA. Novel drug treatment strategies for OA. J Rheumatol 1993; 20: 1461-4.
3. Iwata S. Pharmacological and clinical aspects of intraarticular injection of hyaluronate. Clin Orthop Rel Res 1993; 289: 285-91.
4. Pelletier JP, Martel-Pelletier J. The pathophysiology of OA and the implication of the use of hyaluronan and hylan as therapeutic agents in viscosupplementation. J Rheumatol Suppl 1993;3 9: 19-24.
5. Leslie M. Hyaluronic acid treatment for OA of the knee. Nurse Pract 1999; 24: 41-8.
6. Simon LS. Viscosupplementation therapy with intra-articular hyaluronic acid. Fact or fantasy? Rheum Dis Clin North Am 1999; 25: 345-57.
7. Niethard FU. Pathogenesis of OA--approaches to specific therapy. Am J Orthop, 1999; 28: 8-10.
8. Uebelhart D, Williams JM. Effects of hyaluronic acid on cartilage degradation. Curr Opin Rheumatol 1999; 11: 427-35.
9. Dougados M. Sodium hyaluronate therapy in OA: arguments for a potential beneficial structural effect. Semin Arthritis Rheum 2000; 30: 19-25.
10. Moskowitz RW. Hyaluronic acid supplementation. Curr Rheumatol Rep 2000; 2: 466-71.
11. Ghosh P, Guidolin D. Potential mechanism of action of intra-articular hyaluronan therapy in OA: are the effects molecular weight dependent? Semin Arthritis Rheum 2002; 32: 10-37.
12. Moreland LW. Intra-articular hyaluronan [hyaluronic acid] and hylans for the treatment of OA: mechanisms of action. Arthritis Res Ther 2003; 5: 54-67.
13. Brandt KD, Smith GN Jr, Simon LS. Intraarticular injection of hyaluronan as treatment for knee OA: what is the evidence? Arthritis Rheum. 2000; 43: 1192-203.
14. Takahashi K, Hashimoto S, Kubo T, Hirasawa Y, Lotz M, Amiel D. Effect of hyaluronan on chondrocyte apoptosis and nitric oxide production in experimentally induced osteoarthritis. J Rheumatol 2000; 27: 1713-20.
15. Williams JM, Rayan V, Sumner DR, Thonar EJ. The use of intra-articular Na-hyaluronate as a potential chondroprotective device in experimentally induced acute articular cartilage injury and repair in rabbits. J Orthop Res 2003; 21: 305-11.
16. Williams JM, Zhang J, Kang H, Ummadi V, Homandberg GA. The effects of hyaluronic acid on fibronectin fragment mediated cartilage chondrolysis in skeletally mature rabbits. Osteoarthr Cartil 2003; 11: 44-9.
17. Takahashi K, Hashimoto S, Kubo T, Hirasawa Y, Lotz M, Amiel D. Hyaluronan suppressed nitric oxide production in the meniscus and synovium of rabbit osteoarthritis model. J Orthop Res 2001; 19: 500-3.
18. Kobayashi K, Amiel M, Harwood FL, et al. The long-term effects of hyaluronan during development of osteoarthritis following partial meniscectomy in a rabbit model. Osteoarthr Cartil 2000; 8: 359-65.
19. Kato Y, Mukudai Y, Okimura A, Shimazu A, Nakamura S. Effects of hyaluronic acid on the release of cartilage matrix proteoglycan and fibronectin from the cell matrix layer of chondrocyte cultures: interactions between hyaluronic acid and chondroitin sulfate glycosaminoglycan. J Rheumatol Suppl 1995; 43: 158-9.
20. Homandberg GA, Hui F, Wen C. Kuettner KE, Williams JM. Hyaluronic acid suppresses fibronectin fragment mediated cartilage chondrolysis in vitro. Osteoarthr Cartil 1997; 5: 309-19.
21. Kikuchi T, Yamada H, Fujikawa K. Effects of high molecular weight hyaluronan on the distribution and movement of proteoglycan around chondrocytes cultured in alginate beads. Osteoarthr Cartil 2001; 9: 351-6.
22. Cortivo R, Brun P, Cardarelli L, O'Regan M, Radice M, Abatangeto G. Antioxidant effects of hyaluronan and its alpha-methyl-prednisolone derivative in chondrocyte and cartilage cultures. Semin Arthritis Rheum 1996; 26: 492-501.
23. Brun P, Panfilo S, Daga Gordini D, Cortivo R, Abatangelo G. The effect of byaluronan on CD44-mediated survival of normal and hydroxyl radical-damaged chondrocytes. Osteoarthr Cartil 2003; 11: 208-16.
24. Fukuda K, Takayama M, Ueno M, et al. Hyaluronic acid inhibits interleukin-1-induced superoxide anion in bovine chondrocytes. Inflamm Res 1997; 46: 114-7.
25. Fukuda K, Oh M, Asada S, et al. Sodium hyaluronate inhibits interleukin-1-evoked reactive oxygen species of bovine articular chondrocytes. Osteoarthr Cartil 2001; 9: 390-2.
26. Fukuda K, Dan H, Takayama M, Kumano F, Saitoh M, Tanaka S. Hyaluronic acid increases proteoglycan synthesis in bovine articular cartilage in the presence of interleukin-1. J Pharmacol Exp Ther 1996; 277: 1672-5.
27. Morris EA, Wilcon S, Treadwell BV. Inhibition of interleukin 1 mediated proteoglycan degradation in bovine articular cartilage explants by addition of sodium hyaluronate. Am J Vet Res 1992; 53: 1977-82.
28. Larsen NE, Lombard KM, Parent EG, Balazs EA. Effect of hylan on cartilage and chondrocyte cultures. J Orthop Res 1992; 10: 23-32.
29. Shimazu A, Jikko A, Iwamoto M, et al. Effects of hyaluronic acid on the release of proteoglycans from the cell matrix in rabbit chondrocyte cultures in the presence and absence of cytokines. Arthritis Rheum 1993; 36: 247-53.
30. Akatsuka M, Yamamoto Y, Tobetto K, Yasui T, Ando T. In vitro effects of hyaluronan on prostaglandin E2 induction by interleukin-1 in rabbit articular chondrocytes. Agents Actions 1993; 38: 122-5.
31. Goto H, Onodera T, Hirano H, Shimamura T. Hyaluronic acid suppresses the reduction of alpha2[VI] collagen gene expression caused by interleukin-1beta in cultured rabbit articular chondrocytes. Tohoku J Exp Med 1999; 187: 1-13.
32. Kim G, Okumura M, Ishiguro T, Kadosawa T, Fujinaga T. Preventive effect of hyaluronic acid on the suppression of attachment and migration abilities of bovine chondrocytes by IL-1alpha in vitro. J Vet Med Sci 2003; 65: 427-30.
33. Homandberg GA, Ummadi V, Kang, H. High molecular weight hyaluronan promotes repair of IL-1β damaged cartilage explants from both young and old bovines. Osteoarthr Cartil 2003; 11: 177-86.
34. Tung JT, Venta PJ, Caron JP. Inducible nitric oxide expression in equine articular chondrocytes: effects of antiinflammatory compounds. Osteoarthr Cartil 2002; 10: 5-12.
35. Kobayashi K, Matsuzaka S, Yoshida Y, Miyauchi S, Wada Y, Moriya H. The effects of intraarticularly injected sodium hyaluronate on levels of intact aggrecan and nitric oxide in the joint fluid of patients with knee osteoarthritis. Osteoarthr Cartil 2004; 12: 536-42.
36. Homandberg GA, Hui F, Wen C. Association of proteoglycan degradation with catabolic cytokine and stromelysin release from cartilage cultured with fibronectin fragments. Arch Biochem Biophys 1996; 334: 325-31.
37. Homandberg GA, Hui F, Wen C, et al. Fibronectin fragment induced cartilage chondrolysis is associated with release of catabolic cytokines. Biochem J 1997; 321: 751-7.
38. Kawasaki K, Ochi M, Uchio Y, Adachi N, Matsusaki M. Hyaluronic acid enhances proliferation and chondroitin sulfate synthesis in cultured chondrocytes embedded in collagen gels. J Cell Physiol 1999; 179: 142-8.
39. Han F, Ishiguro N, Ito T, Sakai T, Iwata H. Effects of sodium hyaluronate on experimental osteoarthritis in rabbit knee joints. Nagoya J Med Sci 1999; 62: 115-26.
40. Frean SP, Abraham LA, Lees P. In vitro stimulation of equine articular cartilage proteoglycan synthesis by hyaluronan and carprofen. Res Vet Sci 1999; 67: 183-90.
41. Wiebkin OW, Muir H. The inhibition of sulphate incorporation in isolated adult chondrocytes by hyaluronic acid. FEBs Lett 1973; 37: 42-6.
42. Brown RA, Taylor AM, McDowell JM. Inhibition of sulphate incorporation by chondrocytes in intact cartilage by hyaluronate from foetal cartilage. Connect Tissue Res 1990; 24: 157-68.
43. Ng CK, Handley CJ, Preston BN, Robinson HC, Bolis S, Parker G. Effect of exogenous hyaluronan and hyaluronan oligosaccharides on hyaluronan and aggrecan synthesis and catabolism in adult articular cartilage explants. Arch Biochem Biophys 1995; 316: 596-606.
44. Solursh M, Vaerewyck SA, Reiter RS. Depression by hyaluronic acid of glycosaminoglycan synthesis by cultured chick embryo chondrocytes. Dev Biol 1974; 41: 233-44.
45. Handley CJ, Lowther DA. Inhibition of proteoglycan biosynthesis by hyaluronic acid in chondrocytes in cell culture. Biochim Biophys Acta 1976; 444: 69-74.
46. Homandberg GA, Meyers R, Xie DL. Fibronectin fragments cause chondrolysis of bovine articular cartilage slices in culture. J Biol Chem 1992; 267: 3597-604.
47. Xie DL, Hui F, Meyers R, Homandberg GA. Cartilage chondrolysis by fibronectin fragments is associated with release of several proteinases: stromelysin plays a major role in chondrolysis. Arch Biochem Biophys 1994; 311: 205-12.
48. Homandberg GA, Hui F, Manigalis C, Shrikhande A. Cartilage chondrolysis caused by fibronectin fragments causes cleavage of aggrecan at the same sites as in OA. Osteoarthr Cartil 1997; 5: 450-3.
49. Homandberg GA. Potential regulation of cartilage metabolism in OA by fibronectin fragments. In: Malemud CJ, Frontiers in Bioscience 1999; 4: d713-30 [http://www.bioscience.org/cuffent/special/osteoart.htm].
50. Homandberg GA, Meyers R, Williams J. Intraarticular injection of fibronectin fragments causes severe depletion of cartilage proteoglycans in vivo. J Rheumatol 1993; 20: 1378-82.
51. Williams JM, Plaza V, Hui F, Wen C, Kuettner KE, Homandberg GA. Hyaluronic acid suppresses fibronectin fragment mediated cartilage chondrolysis: II. In vivo. Osteoarthr Cartil 1997; 5: 235-40.
52. Williams JM, Zhang J, Kang H, Ummadi V, Homandberg GA. The effects of hyaluronic acid on fibronectin fragment mediated cartilage chondrolysis in skeletally mature rabbits. Osteoarthr Cartil 2003; 11: 44-9.
53. Kang Y, Williams J, Koepp H, Kuettner KE, Homandberg GA. Hyaluronan suppresses fibronectin fragment mediated damage to human cartilage explant cultures by enhancing proteoglycan synthesis. J Orthop Res 2000; 17: 858-69.
54. Pichika R, Homandberg, GA. Fibronectin fragments elevate nitric oxide (NO) and inducible NO synthetase (iNOS) levels in bovine cartilage and INOS inhibitors block fibronectin fragment mediated damage and promote repair. Inflamm Res 2004; 53: 405-412.
55. Luyten FJP, Hascall VC, Nissley SP, Morales TI, Reddi AH. Insulin-like growth factors maintain steady-state metabolism of proteoglycans in bovine articular cartilage explants. Arch Biochem Biophys 1988; 267: 416-25.
56. Homandberg GA, Ummadi VJ, Kang H. The role of insulin-like growth factor-1 in hyaluronan mediated repair of cultured cartilage explants. Inflamm Res 2004; 53: 396-404.
57. Homandberg GA, Ummadi VJ, Kang H. Hyaluronan enhances cartilage repair through low grade tissue remodeling involving cytokines and matrix metalloproteinases. Inflamm Res 2004; 53: 534-43.
58. Nam JT, Busby WH, Clemmons DR. Human fibroblasts secrete a serine protease that cleaves insulin-like growth factor binding protein-5. Endocrinology 1994; 135: 1385-91.
59. Fowlkes J, Freemark M. Evidence for a novel insulin-like growth factor [IGF]-dependent protease regulating IGF-binding protein-4 in dermal fibroblasts. Endocrinology 1992; 131: 2071-6.
60. Fowlkes JL, Enghild JJ, Suzuki K, Nagase H. Matrix metalloproteinases degrade insulin-like growth factor-binding protein-3 in dermal fibroblast culture. J Biol Chem 1994; 269: 25742-6.
61. Fowlkes JL, Suzuki K, Nagase H, Thrailkill KM. Proteolysis of insulin-like growth factor binding protem-3 during rat pregnancy: a role for matrix metalloproteinases. Endocrinology 1994; 135: 2810-3.
62. De Ceuninck F, Caliez A, Dassencourt L; Anract P, Rendard P. Pharmacologic disruption of insulin-like growth factor 1 binding to IGF-binding proteins restores anabolic responses in human osteoarthritic cartilage. Arthritis Res Ther 2004; 97: 593-7.
63. Bhakta NR, Garcia AM, Frank EH, Grodzinsky AJ, Morales TI. The Insulin-like growth factors [IGFs] I and II bind to articular cartilage via the IGF-binding proteins. J Biol Chem 2000; 275: 5860-6.
64. Zhang Y, Thant AA, Hiraiwa Y, et al. A role for focal adhesion kinase in a hyaluronana-dependent MMP-2 secretion in a human small-cell lung carcinoma cell line, QG90. Biochem Biophys Res Commun 2002; 290: 1123-7.
65. Sakuma M, Miyachi S, Sakamoto T. The effect of sodium hyaluronate on the expression of gelatinases in rabbit corneal epithelial wound healing. Jpn J Ophthalmol 2000; 44: 475-81.
66. McKee CM, Lowenstein CJ, Horton MR, et al. Hyaluronan fragments induce nitric-oxide synthase in murine macrophages through a nuclear factor kappaB-dependent mechanism. J Biol Chem 1997; 272: 8013-18.
67. Maleski MP, Knudson CB. Matrix Accumulation and retention in embryonic cartilage and in vitro chondrogenesis. Connective Tissue Res 1996; 34: 75-86.
68. Knudson W, Casey B, Nishida Y, Eger W, Kuettner KE, Knudson CB. Hyaluronan oligosaccharides perturb cartilage matrix homeostasis and induce cartilage chondrolysis. Arthritis Rheum 2000; 43: 1165-74.
69. Kobayashi H, Suzuki M, Kanayama N, Nishida T, Takigawa M, Terao T. CD44 stimulation by fragmented hyaluronic acid induces upregulation of urokinase-type plasminogen activator and its receptor and subsequently facilitates invasion of human chondrosarcoma cells. Int J Cancer 2002; 102: 379-89.
70. Ohno-Nakahara M, Honda K, Tanimoto K, et al. Induction of CD44 and MMP expression by hyaluronidase treatment of articular chondrocytes. J Biochem (Tokyo) 2004; 135: 567-75.
71. Fieber C, Baumann P, Vallon R, et al. Hyaluronan-oligosac-charide-induced transcription of metalloproteinases. J Cell Science 2004; 117: 359-67.
72. Komatsu, S, Iwata H, Nabeshima T, et al. Studies on the kinetics, metabolism and re-utilisation after intra-articular administration of hyaluronan to rabbits. Arzneimittelforschung 1999; 49: 427-33.
73. Julovi SM, Yasuda T, Shimizu M, Hiramitsu T, Nakamura T. Inhibition of interleukin-1beta-stimulated production of matrix metalloproteinases by hyaluronan via CD44 in human articular cartilage. Arthritis Rheum 2004; 50: 516-25.
74. Homandberg GA, Hui F. High concentrations of fibronectin fragments cause short term catabolic effects in cartilage tissue while lower concentrations cause continuous anabolic effects. Arch Biochem Biophys 1994; 311: 213-8.
75. Homandberg GA, Wen C. Exposure of cartilage to a fibronectin fragment amplifies catabolic processes while also enhancing anabolic processes to limit damage. J Orthop Res 1998; 16: 237-46.
76. Matsumoto T, Tsukazaki T, Enomoto H, Iwasaki K, Yamashita S. Effects of interleukin-1 beta on insulin-like growth factor-I autocrine/paracrine axis in cultured rat articular chondrocytes. Ann Rheum Dis 1994; 53: 128-33.
77. Fukui N, Zhu Y, Maloney WJ, Clohisy J, Sandell LJ. Stimulation of BMP-2 expression by pro-inflammatory cytokines IL-1 and TNF-a1pha in normal and osteoarthritic chondrocytes. J Bone Joint Surg Am 2003; 85: 59-66.
78. Sunic D, McNeil JD, Rayner TE, Andress DL, Belford DA. Regulation of insulin-like growth factor-binding protein-5 by insulin-like growth factor I and interleukin-1 alpha in ovine articular chondrocytes. Endocrinology 1998; 139: 2356-62.
79. Lisignoli G, Grassi F, Piacentini A, et al. Hyaluronan does not affect cytokine and chemokine expression in OA chondrocytes and synoviocytes. Osteoarthr Cartil 2001; 9: 161-8.
80. Hui W, Rowan AD, Cawston T. Insulin-like growth factor 1 blocks collagen release and down regulates matrix metalloproteinase-1, -3, -8, and -13 mRNA expression in bovine nasal cartilage stimulated with oncostatin M in combination with interleukin lalpha. Ann Rheum Dis 2001; 60: 254-61.
81. Hui W, Rowan AD, Cawston T. Modulation of the expression of matrix metalloproteinase and tissue inhibitors of metalloproteinases by TGF-beta1 and IGF-I in primary human articular and bovine nasal chondrocytes stimulated with TNF-alpha Cytokine 2001; 16: 31-5.
82. Purple CR, Untermann TG, Pichika R, Homandberg GA. Fibronectin Fragments Upregulate Insulin-like Growth Factor Binding Proteins in Chondrocytes. Osteoarthr Cartil 2002; 10: 734-46.