Osteoarthritis and Cartilage
Volume 19, Issue 9 , Pages 1150-1157 , September 2011

Regulation of osteoarthritis by omega-3 (n-3) polyunsaturated fatty acids in a naturally occurring model of disease

  • L. Knott

      Affiliations

    • Matrix Biology, Div. VPII, University of Bristol, Veterinary School, Langford, Bristol BS40 5DU, UK
    • ,
  • N.C. Avery

      Affiliations

    • Matrix Biology, Div. VPII, University of Bristol, Veterinary School, Langford, Bristol BS40 5DU, UK
    • ,
  • A.P. Hollander

      Affiliations

    • Stem Cell Biology, Cellular and Molecular Medicine, University of Bristol, Bristol BS8 1TD, UK
    • ,
  • J.F. Tarlton

      Affiliations

    • Matrix Biology, Div. VPII, University of Bristol, Veterinary School, Langford, Bristol BS40 5DU, UK
    • Corresponding Author InformationAddress correspondence and reprint requests to: J.F. Tarlton, Matrix Biology, Div. VPII, University of Bristol, Veterinary School, Langford, Bristol BS40 5DU, UK. Tel: 44-117-9289266; Fax: 44-117-9289505.

Received 25 October 2010 ,Accepted 9 June 2011.

References 

  1. Woolf AD, Pfleger B. Burden of major musculoskeletal conditions. Bull World Health Organ. 2003;81:646–656
  2. Plumb MS, Aspden RM. High levels of fat and (n-6) fatty acids in cancellous bone in osteoarthritis. Lipids Health Dis. 2004;3:12
  3. Wang Y, Wluka AE, Hodge AM, English DR, Giles GG, O’Sullivan R, et al. Effect of fatty acids on bone marrow lesions and knee cartilage in healthy, middle-aged subjects without clinical knee osteoarthritis. Osteoarthritis Cartilage. 2008;16:579–583
  4. Simopoulos AP. Evolutionary aspects of diet, the omega-6/omega-3 ratio and genetic variation: nutritional implications for chronic diseases. Biomed Pharmacother. 2006;60:502–507
  5. Heinecke LF, Grzanna MW, Au AY, Mochal CA, Rashmir-Raven A, Frondoza CG. Inhibition of cyclooxygenase-2 expression and prostaglandin E2 production in chondrocytes by avocado soybean unsaponifiables and epigallocatechin gallate. Osteoarthritis Cartilage. 2010;18:220–227
  6. Li X, Ellman M, Muddasani P, Wang JH, Cs-Szabo G, van Wijnen AJ, et al. Prostaglandin E2 and its cognate EP receptors control human adult articular cartilage homeostasis and are linked to the pathophysiology of osteoarthritis. Arthritis Rheum. 2009;60:513–523
  7. Attur M, Al-Mussawir HE, Patel J, Kitay A, Dave M, Palmer G, et al. Prostaglandin E2 exerts catabolic effects in osteoarthritis cartilage: evidence for signaling via the EP4 receptor. J Immunol. 2008;181:5082–5088
  8. Gruenwald J, Petzold E, Busch R, Petzold HP, Graubaum HJ. Effect of glucosamine sulfate with or without omega-3 fatty acids in patients with osteoarthritis. Adv Ther. 2009;26:858–871
  9. Roush JK, Cross AR, Renberg WC, Dodd CE, Sixby KA, Fritsch DA, et al. Evaluation of the effects of dietary supplementation with fish oil omega-3 fatty acids on weight bearing in dogs with osteoarthritis. J Am Vet Med Assoc. 2010;236:67–73
  10. Fritsch DA, Allen TA, Dodd CE, Jewell DE, Sixby KA, Leventhal PS, et al. A multicenter study of the effect of dietary supplementation with fish oil omega-3 fatty acids on carprofen dosage in dogs with osteoarthritis. J Am Vet Med Assoc. 2010;236:535–539
  11. Hurst S, Zainal Z, Caterson B, Hughes CE, Harwood JL. Dietary fatty acids and arthritis. Prostaglandins Leukot Essent Fatty Acids. 2010;82:315–318
  12. Zainal Z, Longman AJ, Hurst S, Duggan K, Caterson B, Hughes CE, et al. Relative efficacies of omega-3 polyunsaturated fatty acids in reducing expression of key proteins in a model system for studying osteoarthritis. Osteoarthritis Cartilage. 2009;17:896–905
  13. Hogstrom M, Nordstrom P, Nordstrom A. n-3 fatty acids are positively associated with peak bone mineral density and bone accrual in healthy men: the NO2 study. Am J Clin Nutr. 2007;85:803–807
  14. Watkins BA, Li Y, Seifert MF. Dietary ratio of n-6/n-3 PUFAs and docosahexaenoic acid: actions on bone mineral and serum biomarkers in ovariectomized rats. J Nutr Biochem. 2006;17:282–289
  15. Muraoka T, Hagino H, Okano T, Enokida M, Teshima R. Role of subchondral bone in osteoarthritis development: a comparative study of two strains of guinea pigs with and without spontaneously occurring osteoarthritis. Arthritis Rheum. 2007;56:3366–3374
  16. Young BD, Samii VF, Mattoon JS, Weisbrode SE, Bertone AL. Subchondral bone density and cartilage degeneration patterns in osteoarthritic metacarpal condyles of horses. Am J Vet Res. 2007;68:841–849
  17. Quasnichka HL, Anderson-MacKenzie JM, Bailey AJ. Subchondral bone and ligament changes precede cartilage degradation in guinea pig osteoarthritis. Biorheology. 2006;43:389–397
  18. Bruyere O, Dardenne C, Lejeune E, Zegels B, Pahaut A, Richy F, et al. Subchondral tibial bone mineral density predicts future joint space narrowing at the medial femoro-tibial compartment in patients with knee osteoarthritis. Bone. 2003;32:541–545
  19. Dequeker J, Mokassa L, Aerssens J, Boonen S. Bone density and local growth factors in generalized osteoarthritis. Microsc Res Tech. 1997;37:358–371
  20. Bendele AM, Hulman JF. Spontaneous cartilage degeneration in guinea pigs. Arthritis Rheum. 1988;31:561–565
  21. Jimenez PA, Glasson SS, Trubetskoy OV, Haimes HB. Spontaneous osteoarthritis in Dunkin Hartley guinea pigs: histologic, radiologic, and biochemical changes. Lab Anim Sci. 1997;47:598–601
  22. McDougall JJ, Andruski B, Schuelert N, Hallgrimsson B, Matyas JR. Unravelling the relationship between age, nociception and joint destruction in naturally occurring osteoarthritis of Dunkin Hartley guinea pigs. Pain. 2009;141:222–232
  23. Anderson-MacKenzie JM, Quasnichka HL, Starr RL, Lewis EJ, Billingham ME, Bailey AJ. Fundamental subchondral bone changes in spontaneous knee osteoarthritis. Int J Biochem Cell Biol. 2005;37:224–236
  24. Huebner JL, Hanes MA, Beekman B, TeKoppele JM, Kraus VB. A comparative analysis of bone and cartilage metabolism in two strains of guinea-pig with varying degrees of naturally occurring osteoarthritis. Osteoarthritis Cartilage. 2002;10:758–767
  25. Pritzker KP, Gay S, Jimenez SA, Ostergaard K, Pelletier JP, Revell PA, et al. Osteoarthritis cartilage histopathology: grading and staging. Osteoarthritis Cartilage. 2006;14:13–29
  26. Hollander AP, Heathfield TF, Webber C, Iwata Y, Bourne R, Rorabeck C, et al. Increased damage to type II collagen in osteoarthritic articular cartilage detected by a new immunoassay. J Clin Invest. 1994;93:1722–1732
  27. Handley CJ, Buttle DJ. Assay of proteoglycan degradation. Methods Enzymol. 1995;248:47–58
  28. Tarlton JF, Vickery CJ, Leaper DJ, Bailey AJ. Postsurgical wound progression monitored by temporal changes in the expression of matrix metalloproteinase-9. Br J Dermatol. 1997;137:506–516
  29. Knott L, Tarlton JF, Bailey AJ. Chemistry of collagen cross-linking: biochemical changes in collagen during the partial mineralization of turkey leg tendon. Biochem J. 1997;322(Pt 2):535–542
  30. Bannister DW, Burns AB. Adaptation of the Bergman and Loxley technique for hydroxyproline determination to the autoanalyzer and its use in determining plasma hydroxyproline in the domestic fowl. Analyst. 1970;95:596–600
  31. Avery NC, Sims TJ, Bailey AJ. Quantitative determination of collagen cross-links. Methods Mol Biol. 2009;522:103–121
  32. Tietz NW, Burtis CA, Duncan P, Ervin K, Petitclerc CJ, Rinker AD, et al. A reference method for measurement of alkaline phosphatase activity in human serum. Clin Chem. 1983;29:751–761
  33. Daly JA, Ertingshausen G. Direct method for determining inorganic phosphate in serum with the “CentrifiChem”. Clin Chem. 1972;18:263–265
  34. Janssen JW, Helbing AR. Arsenazo III: an improvement of the routine calcium determination in serum. Eur J Clin Chem Clin Biochem. 1991;29:197–201
  35. Tidswell HK, Innes JF, Avery NC, Clegg PD, Barr AR, Vaughan-Thomas A, et al. High-intensity exercise induces structural, compositional and metabolic changes in cuboidal bones – findings from an equine athlete model. Bone. 2008;43:724–733
  36. Pokharna HK, Monnier V, Boja B, Moskowitz RW. Lysyl oxidase and Maillard reaction-mediated crosslinks in aging and osteoarthritic rabbit cartilage. J Orthop Res. 1995;13:13–21
  37. Bank RA, Verzijl N, Lafeber FP, Tekoppele JM. Putative role of lysyl hydroxylation and pyridinoline cross-linking during adolescence in the occurrence of osteoarthritis at old age. Osteoarthritis Cartilage. 2002;10:127–134
  38. Clegg PD, Carter SD. Matrix metalloproteinase-2 and -9 are activated in joint diseases. Equine Vet J. 1999;31:324–330
  39. Masuhara K, Nakai T, Yamaguchi K, Yamasaki S, Sasaguri Y. Significant increases in serum and plasma concentrations of matrix metalloproteinases 3 and 9 in patients with rapidly destructive osteoarthritis of the hip. Arthritis Rheum. 2002;46:2625–2631
  40. Kanyama M, Kuboki T, Kojima S, Fujisawa T, Hattori T, Takigawa M, et al. Matrix metalloproteinases and tissue inhibitors of metalloproteinases in synovial fluids of patients with temporomandibular joint osteoarthritis. J Orofac Pain. 2000;14:20–30
  41. Hulejova H, Baresova V, Klezl Z, Polanska M, Adam M, Senolt L. Increased level of cytokines and matrix metalloproteinases in osteoarthritic subchondral bone. Cytokine. 2007;38:151–156
  42. Couchourel D, Aubry I, Delalandre A, Lavigne M, Martel-Pelletier J, Pelletier JP, et al. Altered mineralization of human osteoarthritic osteoblasts is attributable to abnormal type I collagen production. Arthritis Rheum. 2009;60:1438–1450
  43. Sanchez C, Deberg MA, Bellahcene A, Castronovo V, Msika P, Delcour JP, et al. Phenotypic characterization of osteoblasts from the sclerotic zones of osteoarthritic subchondral bone. Arthritis Rheum. 2008;58:442–455
  44. Dieppe P, Cushnaghan J, Young P, Kirwan J. Prediction of the progression of joint space narrowing in osteoarthritis of the knee by bone scintigraphy. Ann Rheum Dis. 1993;52:557–563
  45. Mansell JP, Tarlton JF, Bailey AJ. Biochemical evidence for altered subchondral bone collagen metabolism in osteoarthritis of the hip. Br J Rheumatol. 1997;36:16–19
  46. Mansell JP, Tarlton JF, Bailey AJ. Expression of gelatinases within the trabecular bone compartment of ovariectomized and parathyroidectomized adult female rats. Bone. 1997;20:533–538
  47. Logar DB, Komadina R, Prezelj J, Ostanek B, Trost Z, Marc J. Expression of bone resorption genes in osteoarthritis and in osteoporosis. J Bone Miner Metab. 2007;25:219–225
  48. Teti A, Migliaccio S, Taranta A, Bernardini S, De Rossi G, Luciani M, et al. Mechanisms of osteoclast dysfunction in human osteopetrosis: abnormal osteoclastogenesis and lack of osteoclast-specific adhesion structures. J Bone Miner Res. 1999;14:2107–2117
  49. Hilal G, Martel-Pelletier J, Pelletier JP, Ranger P, Lajeunesse D. Osteoblast-like cells from human subchondral osteoarthritic bone demonstrate an altered phenotype in vitro: possible role in subchondral bone sclerosis. Arthritis Rheum. 1998;41:891–899
  50. Kouri JB, Aguilera JM, Reyes J, Lozoya KA, Gonzalez S. Apoptotic chondrocytes from osteoarthrotic human articular cartilage and abnormal calcification of subchondral bone. J Rheumatol. 2000;27:1005–1019
  51. Sato M, Wada M, Miyoshi N, Imamura Y, Noriki S, Uchida K, et al. Hydroxyapatite maturity in the calcified cartilage and underlying subchondral bone of guinea pigs with spontaneous osteoarthritis: analysis by Fourier transform infrared microspectroscopy. Acta Histochemica Et Cytochemica. 2004;37:101–107
  52. Chichocki T, Gonsior B, Hofert M, Jarczyk L, Raith B, Rokita E, et al. Measurements of mineralization process in the femur growth plate and rib cartilage of the mouse using pixe in combination with a proton microprobe. Histochemistry. 1988;89:99–104
  53. Ali SY, Rees JA, Scotchford CA. Microcrystal deposition in cartilage and in osteoarthritis. Bone Miner. 1992;17:115–118
  54. Ali SY, Wisby A, Evans L, Craig-Gray J. The sequence of calcium and phosphorus accumulation by matrix vesicles. Calcif Tissue Res. 1977;(22 Suppl):490–493
  55. Rosenbaum CC, O’Mathuna DP, Chavez M, Shields K. Antioxidants and antiinflammatory dietary supplements for osteoarthritis and rheumatoid arthritis. Altern Ther Health Med. 2010;16:32–40
  56. Sun D, Krishnan A, Zaman K, Lawrence R, Bhattacharya A, Fernandes G. Dietary n-3 fatty acids decrease osteoclastogenesis and loss of bone mass in ovariectomized mice. J Bone Miner Res. 2003;18:1206–1216
  57. Watkins BA, Li Y, Lippman HE, Feng S. Modulatory effect of omega-3 polyunsaturated fatty acids on osteoblast function and bone metabolism. Prostaglandins Leukot Essent Fatty Acids. 2003;68:387–398
  58. Watkins BA, Li Y, Lippman HE, Seifert MF. Omega-3 polyunsaturated fatty acids and skeletal health. Exp Biol Med (Maywood). 2001;226:485–497
  59. Bailey AJ, Mansell JP, Sims TJ, Banse X. Biochemical and mechanical properties of subchondral bone in osteoarthritis. Biorheology. 2004;41:349–358
  60. Massicotte F, Lajeunesse D, Benderdour M, Pelletier JP, Hilal G, Duval N, 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. 2002;10:491–500

PII: S1063-4584(11)00164-6

doi: 10.1016/j.joca.2011.06.005

Osteoarthritis and Cartilage
Volume 19, Issue 9 , Pages 1150-1157 , September 2011

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