Evaluation of the effect of oxidative stress on articular cartilage in spontaneously osteoarthritic STR/OrtCrlj mice by measuring the biomarkers for oxidative stress and type II collagen degradation/synthesis

Watari,Taiji; Naito,Kiyohito; Sakamoto,Koji; Kurosawa,Hisashi; Nagaoka,Isao; Kaneko,Kazuo

doi:10.3892/etm.2011.196

Evaluation of the effect of oxidative stress on articular cartilage in spontaneously osteoarthritic STR/OrtCrlj mice by measuring the biomarkers for oxidative stress and type II collagen degradation/synthesis

Authors:
- Taiji Watari
- Kiyohito Naito
- Koji Sakamoto
- Hisashi Kurosawa
- Isao Nagaoka
- Kazuo Kaneko
View Affiliations

Affiliations: Department of Orthopaedic Surgery, Juntendo University Shizuoka Hospital, Shizuoka 410-2295, Japan, Koyo Chemical Co., Ltd., Tokyo 112-0072, Japan, Department of Orthopaedic Surgery, Juntendo University, Graduate School of Medicine, Tokyo 113-8421, Japan, Department of Host Defense and Biochemical Research, Juntendo University, Graduate School of Medicine, Tokyo 113-8421, Japan
Published online on: January 19, 2011 https://doi.org/10.3892/etm.2011.196
Pages: 245-250

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

To investigate the involvement of oxidative stress in the pathogenesis of osteoarthritis (OA), we evaluated the relationship between oxidative stress and articular cartilage degradation by measuring the serum levels of malondialdehyde (MDA, an oxidative stress marker), CTX-II (a type II collagen degradation marker) and CPII (a type II collagen synthesis marker) in obese and hyperlipidemic STR/Ort (STR) and control CBA mice. Seven-week-old osteoarthritic STR male mice (n=10) and control CBA male mice (n=10) were fed standard laboratory food ad libitum. At 35 weeks of age, the mice were sacrificed, and the serum levels of MDA, CTX-II and CPII were determined. Furthermore, histopathological changes were evaluated in the knee joints. Most of the STR mice spontaneously developed OA (18 of the 20 knees). By contrast, the CBA mice developed OA in only 4 of the 20 knees. Importantly, the serum levels of MDA, CTX-II and CPII were elevated to a greater extent in the STR mice compared to levels in the CBA mice. Notably, the level of MDA was correlated with that of CTX-II, but not of CPII. Moreover, the MDA levels were significantly correlated with the serum lipid (total cholesterol and triglyceride) levels as well as body weight. Together these observations suggest that oxidative stress is likely involved in the degradation of type II collagen in articular cartilage, thereby possibly contributing to the development of OA in obese and hyperlipidemic STR mice.

View Figures

View References

1.	Shah R, Raska K Jr and Tiku ML: The presence of molecular markers of in vivo lipid peroxidation in osteoarthritic cartilage. Arthritis Rheum. 52:2799–2807. 2005. View Article : Google Scholar : PubMed/NCBI
2.	Hamerman D: The biology of osteoarthritis. N Engl J Med. 320:1322–1330. 1989. View Article : Google Scholar : PubMed/NCBI
3.	Henrotin YE, Bruckner P and Pujol JP: The role of reactive oxygen species in homeostasis and degradation of cartilage. Osteoarthritis Cartilage. 11:747–755. 2003. View Article : Google Scholar : PubMed/NCBI
4.	Khan IM, Gilbert SJ, Caterson B, Sandell LJ and Archer CW: Oxidative stress induces expression of osteoarthritis markers procollagen IIA and 3B3(-) in adult bovine articular cartilage. Osteoarthritis Cartilage. 16:698–707. 2008. View Article : Google Scholar : PubMed/NCBI
5.	Finkel T and Holbrook NJ: Oxidants, oxidative stress and the biology of ageing. Nature. 408:239–247. 2000. View Article : Google Scholar : PubMed/NCBI
6.	Harman D: Aging: a theory based on free radical and radiation chemistry. J Gerontol. 11:298–300. 1956. View Article : Google Scholar : PubMed/NCBI
7.	Gey KF: On the antioxidant hypothesis with regard to arteriosclerosis. Bibl Nutr Dieta. 37:53–91. 1986.PubMed/NCBI
8.	Valvason C, Musacchio E, Pozzuoli A, Ramonda R, Aldegheri R and Punzi L: Influence of glucosamine sulphate on oxidative stress in human osteoarthritic chondrocytes: effects on HO-1, p22 (Phox) and iNOS expression. Rheumatology. 47:31–35. 2008. View Article : Google Scholar : PubMed/NCBI
9.	Melchiorri C, Meliconi R, Frizziero L, Silvestri T, Pulsatelli L, Mazzetti I, Borzi RM, Uguccioni M and Facchini A: Enhanced and coordinated in vivo expression of inflammatory cytokines and nitric oxide synthase by chondrocytes from patients with osteoarthritis. Arthritis Rheum. 41:2165–2174. 1998. View Article : Google Scholar : PubMed/NCBI
10.	Mathy-Hartert M, Hogge L, Sanchez C, Deby-Dupont G, Crielaard JM and Henrotin Y: Interleukin-1beta and interleukin-6 disturb the antioxidant enzyme system in bovine chondrocytes: a possible explanation for oxidative stress generation. Osteoarthritis Cartilage. 16:756–763. 2008. View Article : Google Scholar
11.	Henrotin Y, Kurz B and Aigner T: Oxygen and reactive oxygen species in cartilage degradation: friends or foes? Osteoarthritis Cartilage. 13:643–654. 2005. View Article : Google Scholar : PubMed/NCBI
12.	Uchida K, Urabe K, Naruse K, Ogawa Z, Mabuchi K and Itoman M: Hyperlipidemia and hyperinsulinemia in the spontaneous osteoarthritis mouse model, STR/Ort. Exp Anim. 58:181–187. 2009. View Article : Google Scholar : PubMed/NCBI
13.	Walton M: Degenerative joint disease in the mouse knee joint; histological observations. J Pathol. 123:109–122. 1977. View Article : Google Scholar : PubMed/NCBI
14.	Schunke M, Tillmann B, Bruck M and Muller-Ruckholtz W: Morphologic characteristics of developing osteoarthritic lesions in the knee cartilage of STR/IN mice. Arthritis Rheum. 31:898–905. 1988. View Article : Google Scholar : PubMed/NCBI
15.	Rousseau JC and Delmas PD: Biological markers in osteoarthritis. Nat Clin Pract Rheumatol. 3:346–356. 2007. View Article : Google Scholar
16.	Yagi K: Simple assay for the level of total lipid peroxides in serum or plasma. Methods Mol Biol. 108:101–106. 1998.PubMed/NCBI
17.	Armstrong D and Browne R: The analysis of free radicals, lipid peroxides, antioxidant enzymes and compounds to oxidative stress as applied to the clinical chemistry laboratory. Adv Exp Med Biol. 366:43–58. 1994. View Article : Google Scholar : PubMed/NCBI
18.	Witztum JL and Steinberg D: Role of oxidized low density lipoprotein in atherogenesis. J Clin Invest. 88:1785–1792. 1991. View Article : Google Scholar : PubMed/NCBI
19.	Kinoshita M, Oikawa S, Hayasaka K, Sekikawa A, Nagashima T, Toyota T and Miyazawa T: Age-related increases in plasma phosphatidylcholine hydroperoxide concentrations in control subjects and patients with hyperlipidemia. Clin Chem. 46:822–828. 2000.
20.	Carlo MD Jr and Loeser RF: Increased oxidative stress with aging reduces chondrocyte survival: correlation with intracellular glutathione levels. Arthritis Rheum. 48:3419–3430. 2003. View Article : Google Scholar
21.	Bates EJ, Harper GS, Lowther DA and Preston BN: Effect of oxygen-derived reactive species on cartilage proteoglycanhyaluronate aggregates. Biochem Int. 8:629–637. 1984.PubMed/NCBI
22.	Tiku ML, Gupta S and Deshmukh DR: Aggrecan degradation in chondrocytes is mediated by reactive oxygen species and protected by antioxidants. Free Radic Res. 30:395–405. 1999. View Article : Google Scholar : PubMed/NCBI
23.	Tiku ML, Allison GT, Naik K and Karry SK: Malondialdehyde oxidation of cartilage collagen by chondrocyte. Osteoarthritis Cartilage. 11:159–166. 2003. View Article : Google Scholar : PubMed/NCBI
24.	Garnero P, Rousseau JC and Delmas PD: Molecular basis and clinical use of biochemical markers of bone, cartilage, and synovium in joint disease. Arthritis Rheum. 43:953–968. 2000. View Article : Google Scholar : PubMed/NCBI
25.	Garnero P, Piperno M, Gineyts E, Christgau S, Delmas PD and Vignon E: Cross sectional evaluation of biochemical markers of bone, cartilage, and synovial tissue metabolism in patients with knee osteoarthritis: relations with disease activity and joint damage. Ann Rheum Dis. 60:619–626. 2001. View Article : Google Scholar
26.	Garnero P, Ayral X, Rousseau JC, Christgau S, Sandell LJ, Daugados M and Delmas PD: Uncoupling of type II collagen synthesis and degradation predicts progression of joint damage in patients with knee osteoarthritis. Arthritis Rheum. 46:2613–2624. 2002. View Article : Google Scholar : PubMed/NCBI
27.	Garnero P, Conrozier T, Christgau S, Mathieu P, Delmas PD and Vignon E: Urinary type II collagen C-telopeptide levels are increased in patients with rapidly destructive hip osteoarthritis. Ann Rheum Dis. 62:939–943. 2003. View Article : Google Scholar : PubMed/NCBI
28.	Reijman M, Hazes JM, Bierma-Zeinstra SM, Koes BW, Christgau S, Christiansen C, Uitterlinden AG and Pols HA: A new marker for osteoarthritis: cross-sectional and longitudinal approach. Arthritis Rheum. 50:2471–2478. 2004. View Article : Google Scholar : PubMed/NCBI
29.	Jordan KM, Syddall HE, Garnero P, Gineyts E, Dennison EM, Sayer AA, Delmas PD, Cooper C and Arden NK: Urinary CTX-II and glucosyl-galactosyl-pyridinoline are associated with the presense and severity of radiographic knee osteoarthritis in men. Ann Rheum Dis. 65:871–877. 2006. View Article : Google Scholar : PubMed/NCBI
30.	Meulenbelt I, Kloppenburg M, Kroon HM, et al: Urinary CTX-II levels are associated with radiographic subtypes of osteoarthritis in hip, knee, hand, and facet joints in subjects with familial osteoarthritis at multiple sites: the GARP study. Ann Rheum Dis. 65:360–365. 2006. View Article : Google Scholar : PubMed/NCBI
31.	Zhai G, Cicuttini F, Ding C, Scott F, Garnero P and Jones G: Correlates of knee pain in younger subjects. Clin Rheumatol. 26:75–80. 2007. View Article : Google Scholar : PubMed/NCBI
32.	Poole AR, Ionescu M, Fitzcharles MA and Billinghurst RC: The assessment of cartilage degradation in vivo: development of an immunoassay for the measurement in body fluids of type II collagen cleaved by collagenases. J Immunol Methods. 294:145–153. 2004. View Article : Google Scholar : PubMed/NCBI
33.	Nelson F, Dahlberg L, Laverty S, Reiner A, Pidoux I, Ionescu M, Fraser GL, Brooks E, Tanzer M, Rosenberg LC, Dieppe P and Poole AR: Evidence for altered synthesis of type II collagen in patients with osteoarthritis. J Clin Invest. 102:2115–2125. 1998. View Article : Google Scholar : PubMed/NCBI
34.	Keaney JF Jr, Larson MG, Vasan RS, Wilson PW, Lipinska I, Corey D, Massaro JM, Sutherland P, Vita JA and Benjamin EJ: Obesity and systemic oxidative stress: clinical correlates of oxidative stress in the Framingham Study. Arterioscler Thromb Vasc Biol. 23:434–439. 2003. View Article : Google Scholar : PubMed/NCBI
35.	Fujita K, Nishizawa H, Funahashi T, Shimomura I and Shimabukuro M: Systemic oxidative stress is associated with visceral fat accumulation and the metabolic syndrome. Circ J. 70:1437–1442. 2006. View Article : Google Scholar : PubMed/NCBI
36.	Siwik DA, Pagano PJ and Colucci WS: Oxidative stress regulates collagen synthesis and matrix metalloproteinase activity in cardiac fibroblasts. Am J Physiol Cell Physiol. 280:C53–C60. 2001.PubMed/NCBI