Veterinary Research Communications

, Volume 31, Issue 5, pp 591–601 | Cite as

Plasma Concentrations of a Type II Collagen-derived Peptide and Its Nitrated Form in Growing Ardenner Sound Horses and in Horses Suffering from Juvenile Digital Degenerative Osteoarthropathy

  • J.-Ph. Lejeune
  • D. Serteyn
  • M. Gangl
  • N. Schneider
  • G. Deby-Dupont
  • M. Deberg
  • Y. Henrotin
Article

Abstract

Several breeds of draft horses suffer from degenerative digital osteoarthropathy, resulting in a reduced active lifespan. A group of 30 Ardenner horses was followed, in standardized conditions, from 15 to 28 months of age to detect the early manifestations of the disease. The severity of the disease was assessed according to a personal grading system including clinical and radiographic items. Coll 2-1, a peptide of the helical region of type II collagen, and its nitrated form (Coll 2-1 NO2) were assayed in blood plasma collected at 452 ± 18 days, 504 ± 20 days, 558 ± 18 days, 613 ± 19 days, 675 ± 19 days, 752 ± 21 days and 852 ± 19 days of age. At the end of the follow-up period, 53.3% of Ardenner horses were affected by a degenerative digital osteoarthropathy. A significant effect (p < 0.05) of time, sex and pathology was observed for Coll 2-1 NO2. Variations of Coll 2-1 were not significant except for the time effect. The elevation of Coll 2-1 NO2 in the pathological group could indicate an inflammatory process during the growth of the affected horses, as nitration of tyrosine is mediated through reactive oxygen/nitrogen species and/or myeloperoxidase activity. Coll 2-1 NO2 appears to be an interesting early marker of cartilage degradation and oxidation in degenerative osteoarthropathy.

Keywords

Ardenner horses type II collagen degenerative digital osteoarthropathy 

Abbreviations

AAEP

American Association of Equine Practitioners

BSA

bovine serum albumin

Coll 2-1 NO2

nitrate Coll 2-1

COMP

cartilage oligomeric matrix protein

CPII

carboxypeptide type II

ECM

extracellular matrix

EDTA

ethylenediaminetetraacetic acid

KS

keratan sulphate

LSM

least-squares mean

MMP

matrix metalloproteinase

MPO

myeloperoxidase

OA

osteoarthritis

PBS

phosphate-buffered saline

ROS

reactive oxygen species

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. AAEP; American Association of Equine Practitioners, 1999. Guide to Veterinary Services for Horse Shows, 7th edn, (AAEP, Lexington, Ky)Google Scholar
  2. Arai, K., Misumi, K., Carter, S.D., Shinbara S., Fujiki, M. and Sakamoto, H., 2005. Analysis of cartilage oligomeric matrix protein (COMP) degradation and synthesis in equine joint disease. Equine Veterinary Journal, 37, 31–36PubMedGoogle Scholar
  3. Baldus, S., Eiserich, J.P., Brennan, M.-L., Jackson, R.M., Alexander, C.B. and Freeman, B.A., 2002. Spatial mapping of pulmonary and vascular nitrotyrosine reveals the pivotal role of myeloperoxidase as a catalyst for tyrosine nitration in inflammatory diseases. Free Radical Biology and Medicine, 33, 1010–1019PubMedCrossRefGoogle Scholar
  4. Beckman, J.S., Chen, J., Ischiropoulos, H. and Crow, J.P., 1994. Oxidative chemistry of peroxynitrite. Methods in Enzymology, 233, 229–240PubMedCrossRefGoogle Scholar
  5. Billinghurst, R.C., Brama, P.A.J., Van Weeren, P.R., Knowlton, M.S. and McIlwraith, C.W., 2004. Evaluation of serum concentrations of biomarkers of skeletal metabolism and results of radiography as indicators of severity of osteochondrosis in foals. American Journal of Veterinary Research, 65, 143–150PubMedCrossRefGoogle Scholar
  6. Brama, P.A., TeKoppele, J.M., Beekman, B., Van Weeren, P.R. and Barneveld, A., 1998. Matrix metalloproteinase activity in equine synovial fluid: influence of age, osteoarthritis, and osteochondrosis. Annals of the Rheumatic Diseases, 57, 697–699PubMedCrossRefGoogle Scholar
  7. Brama, P.A., TeKoppele, J.M., Beekman, B., Van El, B., Barneveld, A. and Van Weeren, P.R., 2000. Influence of development and joint pathology on stromelysin enzyme activity in equine synovial fluid. Annals of the Rheumatic Diseases, 59, 155–157PubMedCrossRefGoogle Scholar
  8. Brennan, M.-L., Wu, W., Fu, X., Shen, Z., Song, W., Frost, H., Vadseth, C., Narine, L., Lenkiewicz, E., Borchers, M.T., Lusis, A.J. and Hazen, S.L., 2002. A tale of two controversies. Defining both the role of peroxidases in nitrotyrosine formation in vivo using eosinophil peroxidase and myeloperoxidase-deficient mice, and the nature of peroxidase-generated reactive nitrogen species. Journal of Biological Chemistry, 277, 17415–17427PubMedCrossRefGoogle Scholar
  9. Burner, U., Furtmuller, P.G., Kettle, A.J., Koppenol, W.H. and Obinger, C., 2000. Mechanisms of reaction of myeloperoxydase with nitrite. Journal of Biological Chemistry, 275, 20957–20601CrossRefGoogle Scholar
  10. Caron, J.P., 2003. Osteoarthritis. In: M.W. Ross and S.J. Dyson (eds), Diagnosis and Management of Lameness in the Horse, (Saunders, St Louis), 572–591Google Scholar
  11. Caudron, I., 1997. Approche orthopédique des affections ostéo-articulaires dégénératives de l'extrémité digitale du cheval. Prévention et traitement, (PhD thesis, Université de Liège, Sart-Tilman)Google Scholar
  12. Chiang, K., Parthasarathy, S. and Santanam, N., 2004. Estrogen, neutrophils and oxidation. Life Sciences, 75, 2425–2438PubMedCrossRefGoogle Scholar
  13. Cho, M.M., Ziats, N.P., Pal, D., Utian, W.H. and Gorodeski, G.L., 1999. Estrogen modulates paracellular permeability of human endothelial cells by eNOS and iNOS-related mechanisms. American Journal of Physiology–Cell Physiology, 276, 337–349Google Scholar
  14. Deberg, M., Labasse, A., Christgau, S., Cloos, P., Bang Henriksen, D., Chapelle, J.P., Zegels, B., Reginster, J.Y. and Henrotin, Y., 2005. New serum biochemical markers (Coll 2-1 and Coll 2-1 NO2) for studying oxidative-related type II collagen network degradation in patients with osteoarthritis and rheumatoid arthritis. Osteoarthritis and Cartilage, 13, 258–265PubMedCrossRefGoogle Scholar
  15. Dimock, A.N., Siciliano, P.D. and McIlwraith, C.W., 2000. Evidence supporting an increased presence of reactive oxygen species in the diseased equine joint. Equine Veterinary Journal, 32, 439–443PubMedGoogle Scholar
  16. Dyson, S.J., 2003. The distal phalanx and distal interphalangeal joint. In: M.W. Ross, and S.J. Dyson (eds), Diagnosis and Management of Lameness in the Horse, (Saunders, St Louis), 310–325Google Scholar
  17. Frisbie, D.D., Ray, C.S., Ionescu, M., Poole, A.R., Chapman, P.L. and McIlwraith C.W., 1999. Measurement of synovial fluid and serum concentrations of the 846 epitope of chondroitin sulfate and of carboxy propeptides of type II procollagen for diagnosis of osteochondral fragmentation in horses. American Journal of Veterinary Research, 60, 306–309PubMedGoogle Scholar
  18. Gaut, J.P., Byun, J., Tran, H.D., Lauber, W.M., Carroll, J.A., Hotchkiss, R.S., Belaaouaj, A. and Heinecke, J.W., 2002. Myeloperoxidase produces nitrating oxidants in vivo. Journal of Clinical Investigation, 109, 1311–1319PubMedCrossRefGoogle Scholar
  19. Golden, B.L., Brinks, J.S. and Bourdon R.M., 1991. A performance programmed method for computing inbreeding coefficients from large data sets for use in mixed-model analyses. Journal of Animal Science, 69, 3564–3573PubMedGoogle Scholar
  20. Henrotin, Y.E., Deby-Dupont, G.P., Deby, C., De Bruyn, M., Lamy, M. and Franchimont, P., 1993. Production of active oxygen species by isolated human chondrocytes. British Journal of Rheumatology, 32, 562–567PubMedCrossRefGoogle Scholar
  21. Henrotin, Y.E., Zheng, S.X., Deby-Dupont, G.P., Labasse, A., Crielaard, J. and Reginster, J.Y., 1998. Nitric oxide downregulates interleukin 1β (IL-1β) stimulated IL-6, IL-8 and prostaglandin E2 production by human chondrocytes. Journal of Rheumatology, 25, 1595–1601PubMedGoogle Scholar
  22. Henrotin, Y.E., Bruckner, P. and Pujol, J.P.L., 2003. The role of active oxygen species in homeostasis and degradation of cartilage. Osteoarthritis and Cartilage, 11, 747–755PubMedCrossRefGoogle Scholar
  23. Henrotin, Y.E., Deberg, M., Dubuc, J.E., Quettier, E., Christgau, S. and Reginster, J.Y., 2004. Type II collagen peptides for measuring cartilage degradation. Biorheology, 41, 543–547PubMedGoogle Scholar
  24. Jouglin, M., Robert C., Valette, J.P., Gavard, F., Quintin-Colonna, F. and Denoix, J.M., 2000. Metalloproteinases and tumor necrosis factor-alpha activities in synovial fluids of horses: correlation with articular cartilage alterations. Veterinary Research, 31, 507–515PubMedCrossRefGoogle Scholar
  25. Kaur, H. and Halliwel, B., 1994. Evidence for nitric oxide-mediated oxidative damage in chronic inflammation. Nitrotyrosine in serum and synovial fluid from rheumatoid patients. FEBS Letters, 350, 9–12PubMedCrossRefGoogle Scholar
  26. Kettle, A.J., van Dalen, C.J. and Winterbourn, C.C., 1997. Peroxynitrite and myeloperoxidase leave the same footprint in protein nitration. Redox Report, 3, 257–258PubMedGoogle Scholar
  27. Kubala, L., 2004a. Myeloperoxidase-dependent modulation of the oxylipin metabolome. 11th Annual Meeting of the Society for Free Radical Biology and Medicine Google Scholar
  28. Kubala, L., 2004b. Glycosaminoglycan-dependent sequestration of myeloperoxidase. 11th Annual Meeting of the Society for Free Radical Biology and Medicine Google Scholar
  29. Kuwabara, K., Jyoyama, H., Fleisch, J.H. and Hori, Y., 2002. Inhibition of antigen-induced arthritis in guinea-pigs by a selective LTB4 receptor antagonist LY293111Na. Inflammation Research, 51, 541–550PubMedCrossRefGoogle Scholar
  30. Lejeune, J.P., Schneider, N., Duvivier, D.H., Michaux, C., Caudron, I. and Serteyn, D., 2002. Arthropathie interphalangienne dégénérative juvénile chez le cheval ardennais: protocole d&évaluation radiographique (Partie II). Annales de Médecine Vétérinaire, 146, 173–179Google Scholar
  31. Liang, M., Ekblad, E., Lydrup, M.L. and Nilsson, B.O., 2003. Combined lack of estrogen receptors alpha and beta affects vascular iNOS protein expression. Cell and Tissue Research, 313, 63–70PubMedCrossRefGoogle Scholar
  32. McIlwraith, C.W., 2005. Use of synovial fluid and serum biomarkers in equine bone and joint disease: a review. Equine Veterinary Journal, 37, 473–482PubMedGoogle Scholar
  33. May, S.A., 1996. Radiology refresher article. Radiological aspects of degenerative joint disease. Equine Veterinary Education, 8, 114–120CrossRefGoogle Scholar
  34. Mershon, J.L., Baker, R.S. and Clarck, K.E., 2002. Estrogen increases iNOS expression in the ovine coronary artery. American Journal of Physiology—Heart and Circulatory Physiology, 283, 1169–1180Google Scholar
  35. Robert, C., Denoix, J.M. and Houliez, D., 1995. Evolution des images radiologiques des articulations des membres de chevaux entre 3 et 6 ans: résultats préliminaires sur 46 sujets. Pratique Vétérinaire Equine, 27, 143–152Google Scholar
  36. Rosenquist, C., Fledelius, C., Christgau, S., Pedersen, B.J., Bonde, M., Qvist, P. and Christiansen, C., 1998. Serum CrossLaps one step ELISA. First application of monoclonal antibodies for measurement in serum of bone-related degradation products from C-terminal telopeptides of type I collagen. Clinical Chemistry, 44, 2281–2289PubMedGoogle Scholar
  37. Ruggles, A.J., 2003. The proximal and middle phalanges and proximal interphalangeal joint. In: M.W. Ross and S.J. Dyson (eds), Diagnosis and Management of Lameness in the Horse, (Saunders, St Louis), 342–348Google Scholar
  38. Stadler, J., Stefanovic-Racic M., Billiar, T.R., Curran, R.D., McIntyre L.A., Georgescu, H.I., Simmons, R.L. and Evans, C.H., 1991. Articular chondrocytes synthesize nitric oxide in response to cytokines and lipopolysaccharide. Journal of Immunology, 147, 3915–3920Google Scholar
  39. Stichtenoth, D.O. and Frölich, J.C., 1998. Nitric oxide and inflammatory joint diseases. British Journal of Rheumatology, 37, 246–257PubMedCrossRefGoogle Scholar
  40. Todhunter, R.J., Fubini, S.L., Freeman, K.P. and Lust, G., 1997. Concentrations of keratan sulfate in plasma and synovial fluid from clinically normal horses and horses with joint disease. Journal of the American Veterinary Medical Association, 210, 369–374PubMedGoogle Scholar
  41. Van der Vliet, A., O'Neill, C.A., Halliwell, B., Cross, C.E. and Kaur, H., 1994. Aromatic hydroxylation and nitration of phenylalanine and tyrosine by peroxynitrite. Evidence for hydroxyl radical production from peroxynitrite. FEBS Letters, 339, 89–92PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science + Business Media, Inc. 2007

Authors and Affiliations

  • J.-Ph. Lejeune
    • 1
  • D. Serteyn
    • 1
    • 2
    • 3
  • M. Gangl
    • 2
  • N. Schneider
    • 1
  • G. Deby-Dupont
    • 3
  • M. Deberg
    • 4
  • Y. Henrotin
    • 3
    • 4
  1. 1.Centre Européen du ChevalMont-le-Soie
  2. 2.Department of Clinical Sciences, Large Animal Surgery, Faculty of Veterinary MedicineUniversity of LiègeLiège
  3. 3.Center for Oxygen Research and DevelopmentUniversity of LiègeLiège
  4. 4.Bone and Cartilage Research UnitUniversity of Liège, Institute of PathologyLiègeBelgium

Personalised recommendations