Visceral adipose tissue‑derived serine protease inhibitor inhibits interleukin‑1β‑induced catabolic and inflammatory responses in murine chondrocytes

Bao,Jia‑Peng; Jiang,Li‑Feng; Li,Jing; Chen,Wei‑Ping; Hu,Peng‑Fei; Wu,Li‑Dong

doi:10.3892/mmr.2014.2478

Visceral adipose tissue‑derived serine protease inhibitor inhibits interleukin‑1β‑induced catabolic and inflammatory responses in murine chondrocytes

Authors:
- Jia‑Peng Bao
- Li‑Feng Jiang
- Jing Li
- Wei‑Ping Chen
- Peng‑Fei Hu
- Li‑Dong Wu
View Affiliations

Affiliations: Department of Orthopedics Surgery, The Second Hospital of Medical College, Zhejiang University, Hangzhou, Zhejiang 310009, P.R. China
Published online on: August 11, 2014 https://doi.org/10.3892/mmr.2014.2478
Pages: 2191-2197

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

Visceral adipose tissue‑derived serine protease inhibitor (vaspin) is a newly identified member of the adipocytokine family, whose precise role in chondrocyte metabolism remains to be elucidated. The aim of the present study was to investigate the effect of vaspin on chondrocytes. The cell viability and the cytotoxicity of vaspin in chondrocytes were examined. Furthermore, the gene expression of matrix metalloproteinases‑2 and -9, a disintegrin and metalloproteinase with thrombospondin motifs 4 and 5 and cathepsin D was also examined, as well as the protein production of cyclooxygenase‑2, prostaglandin E2 and inducible nitrous oxide synthase following treatment with different concentrations of vaspin in the absence or presence of interleukin‑1‑beta (IL‑1β). In addition, the protein levels of the inhibitor of nuclear factor‑κB (IκB‑α) and the phosphorylation of nuclear factor kappa B (NF‑κB) were investigated. Vaspin was not able to stimulate the proliferation of chondrocytes and demonstrated no significant cytotoxic effect at concentrations of 10‑500 ng/ml following coincubation for 24 and 48 h. However, vaspin inhibited IL‑1β‑induced production of catabolic factors and inflammatory mediators in chondrocytes, and also suppressed the phosphorylation of NF‑κB and the degradation of IκB‑α. The data from the present study suggested that vaspin has a protective effect in chondrocyte metabolism and is an important factor in the pathophysiology of osteoarthritis.

View Figures

View References

1	Krasnokutsky S, Samuels J and Abramson SB: Osteoarthritis in 2007. Bull NYU Hosp Jt Dis. 65:222–228. 2007.
2	Kapoor M, Martel-Pelletier J, Lajeunesse D, Pelletier JP and Fahmi H: Role of proinflammatory cytokines in the pathophysiology of osteoarthritis. Nat Rev Rheumatol. 71:33–42. 2011. View Article : Google Scholar
3	Goldring MB and Goldring SR: Osteoarthritis. J Cell Physiol. 213:626–634. 2007. View Article : Google Scholar : PubMed/NCBI
4	Yusuf E: Metabolic factors in osteoarthritis: obese people do not walk on their hands. Arthritis Res Ther. 14:1232012. View Article : Google Scholar : PubMed/NCBI
5	Cicuttini FM, Baker JR and Spector TD: The association of obesity with osteoarthritis of the hand and knee in women: a twin study. J Rheumatol. 23:1221–1226. 1996.PubMed/NCBI
6	Yusuf E: Metabolic factors in osteoarthritis: obese people do not walk on their hands. Arthritis Res Ther. 14:1232012. View Article : Google Scholar : PubMed/NCBI
7	Bay-Jensen AC, Slagboom E, Chen-An P, et al: Role of hormones in cartilage and joint metabolism: understanding an unhealthy metabolic phenotype in osteoarthritis. Menopause. 20:578–586. 2013.PubMed/NCBI
8	Hida K, Wada J, Eguchi J, et al: Visceral adipose tissue-derived serine protease inhibitor: a unique insulin-sensitizing adipocytokine in obesity. Proc Natl Acad Sci USA. 102:10610–10615. 2005. View Article : Google Scholar
9	Fain JN, Buehrer B, Bahouth SW, Tichansky DS and Madan AK: Comparison of messenger RNA distribution for 60 proteins in fat cells vs the nonfat cells of human omental adipose tissue. Metabolism. 57:1005–1015. 2008. View Article : Google Scholar : PubMed/NCBI
10	Klöting N, Berndt J, Kralisch S, et al: Vaspin gene expression in human adipose tissue: association with obesity and type 2 diabetes. Biochem Biophys Res Commun. 339:430–436. 2006.
11	Meyer-Hoffert U: Reddish, scaly, and itchy: how proteases and their inhibitors contribute to inflammatory skin diseases. Arch Immunol Ther Exp (Warsz). 57:345–354. 2009. View Article : Google Scholar : PubMed/NCBI
12	Klöting N, Kovacs P, Kern M, et al: Central vaspin administration acutely reduces food intake and has sustained blood glucose-lowering effects. Diabetologia. 54:1819–1823. 2011.
13	Körner A, Neef M, Friebe D, et al: Vaspin is related to gender, puberty and deteriorating insulin sensitivity in children. Int J Obes (Lond). 35:578–586. 2011.PubMed/NCBI
14	Youn BS, Klöting N, Kratzsch J, et al: Serum vaspin concentrations in human obesity and type 2 diabetes. Diabetes. 57:372–377. 2008. View Article : Google Scholar : PubMed/NCBI
15	Ozgen M, Koca SS, Dagli N, Balin M, Ustundag B and Isik A: Serum adiponectin and vaspin levels in rheumatoid arthritis. Arch Med Res. 41:457–463. 2010. View Article : Google Scholar : PubMed/NCBI
16	Klaasen R, Herenius MM, Wijbrandts CA, et al: Treatment-specific changes in circulating adipocytokines: a comparison between tumour necrosis factor blockade and glucocorticoid treatment for rheumatoid arthritis. Ann Rheum Dis. 71:1510–1516. 2012. View Article : Google Scholar
17	Senolt L, Polanská M, Filková M, et al: Vaspin and omentin: new adipokines differentially regulated at the site of inflammation in rheumatoid arthritis. Ann Rheum Dis. 69:1410–1411. 2010. View Article : Google Scholar : PubMed/NCBI
18	Kamio N, Kawato T, Tanabe N, et al: Vaspin attenuates RANKL-induced osteoclast formation in RAW264.7 cells. Connect Tissue Res. 54:147–152. 2013. View Article : Google Scholar
19	Choi SH, Hong ES and Lim S: Clinical implications of adipocytokines and newly emerging metabolic factors with relation to insulin resistance and cardiovascular health. Front Endocrinol (Lausanne). 4:972013.PubMed/NCBI
20	Wada J: Vaspin: a novel serpin with insulin-sensitizing effects. Expert Opin Investig Drugs. 17:327–333. 2008. View Article : Google Scholar : PubMed/NCBI
21	Kadoglou NP, Gkontopoulos A, Kapelouzou A, et al: Serum levels of vaspin and visfatin in patients with coronary artery disease-Kozani study. Clin Chim Acta. 412:48–52. 2011. View Article : Google Scholar : PubMed/NCBI
22	Phalitakul S, Okada M, Hara Y and Yamawaki H: Vaspin prevents methylglyoxal-induced apoptosis in human vascular endothelial cells by inhibiting reactive oxygen species generation. Acta Physiol (Oxf). 209:212–219. 2013.
23	Phalitakul S, Okada M, Hara Y and Yamawaki H: Vaspin prevents TNF-α-induced intracellular adhesion molecule-1 via inhibiting reactive oxygen species-dependent NF-κB and PKCθ activation in cultured rat vascular smooth muscle cells. Pharmacol Res. 64:493–500. 2011.PubMed/NCBI
24	Kukla M, Mazur W, Bułdak RJ and Zwirska-Korczala K: Potential role of leptin, adiponectin and three novel adipokines - visfatin, chemerin and vaspin - in chronic hepatitis. Mol Med. 17:1397–1410. 2011. View Article : Google Scholar
25	Fu BD, Yamawaki H, Okada M and Hara Y: Vaspin can not inhibit TNF-α-induced inflammation of human umbilical vein endothelial cells. J Vet Med Sci. 71:1201–1207. 2009.
26	Bao JP, Chen WP, Feng J, Hu PF, Shi ZL and Wu LD: Leptin plays a catabolic role on articular cartilage. Mol Biol Rep. 37:3265–3272. 2010. View Article : Google Scholar : PubMed/NCBI
27	Hu PF, Chen WP, Tang JL, Bao JP and Wu LD: Apelin plays a catabolic role on articular cartilage: in vivo and in vitro studies. Int J Mol Med. 26:357–363. 2010.PubMed/NCBI
28	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
29	Chen TH, Chen L, Hsieh MS, Chang CP, Chou DT and Tsai SH: Evidence for a protective role for adiponectin in osteoarthritis. Biochim Biophys Acta. 1762:711–718. 2006. View Article : Google Scholar : PubMed/NCBI
30	Hsieh YS, Yang SF, Chu SC, et al: Expression changes of gelatinases in human osteoarthritic knees and arthroscopic debridement. Arthroscopy. 20:482–488. 2004. View Article : Google Scholar : PubMed/NCBI
31	Birkedal-Hansen H, Moore WG, Bodden MK, et al: Matrix metalloproteinases: a review. Crit Rev Oral Biol Med. 4:197–250. 1993.PubMed/NCBI
32	Kozaci LD, Buttle DJ and Hollander AP: Degradation of type II collagen, but not proteoglycan, correlates with matrix metalloproteinase activity in cartilage explant cultures. Arthritis Rheum. 40:164–174. 1997. View Article : Google Scholar
33	Fushimi K, Troeberg L, Nakamura H, Lim NH and Nagase H: Functional differences of the catalytic and non-catalytic domains in human ADAMTS-4 and ADAMTS-5 in aggrecanolytic activity. J Biol Chem. 283:6706–6716. 2008. View Article : Google Scholar : PubMed/NCBI
34	Handley CJ, Mok MT, Ilic MZ, Adcocks C, Buttle DJ and Robinson HC: Cathepsin D cleaves aggrecan at unique sites within the interglobular domain and chondroitin sulfate attachment regions that are also cleaved when cartilage is maintained at acid pH. Matrix Biol. 20:543–553. 2001. View Article : Google Scholar
35	Chabane N, Zayed N, Afif H, et al: Histone deacetylase inhibitors suppress interleukin-1β-induced nitric oxide and prostaglandin E2 production in human chondrocytes. Osteoarthritis Cartilage. 16:1267–1274. 2008.
36	Salvemini D, Misko TP, Masferrer JL, Seibert K, Currie MG and Needleman P: Nitric oxide activates cyclooxygenase enzymes. Proc Natl Acad Sci USA. 90:7240–7244. 1993. View Article : Google Scholar : PubMed/NCBI
37	Sasaki K, Hattori T, Fujisawa T, Takahashi K, Inoue H and Takigawa M: Nitric xide mediates interleukin-1-induced gene expression of matrix metalloproteinases and basic fibroblast growth factor in cultured rabbit articular chondrocytes. J Biochem. 123:431–439. 1998. View Article : Google Scholar
38	Amin AR, Attur M, Patel RN, et al: Superinduction of cyclooxygenase-2 activity in human osteoarthritis-affected cartilage. Influence of nitric oxide. J Clin Invest. 99:1231–1237. 1997. View Article : Google Scholar : PubMed/NCBI
39	Wang P, Zhu F and Konstantopoulos K: Prostaglandin E2 induces interleukin-6 expression in human chondrocytes via cAMP/protein kinase A- and phosphatidylinositol 3-kinase-dependent NF-κB activation. Am J Physiol Cell Physio. 298:C1445–C1456. 2010.PubMed/NCBI
40	Vincenti MP and Brinckerhoff CE: Transcriptional regulation of collagenase (MMP-1, MMP-13) genes in arthritis: integration of complex signaling pathways for the recruitment of gene-specific transcription factors. Arthritis Res. 4:157–164. 2002. View Article : Google Scholar
41	Tian B and Brasier AR: Identification of a nuclear factor κB-dependent gene network. Recent Prog Horm Res. 58:95–130. 2003.
42	Hayden MS and Ghosh S: Signaling to NF-κB. Genes Dev. 18:2195–2224. 2004.
43	Li H, Peng W, Zhuang J, et al: Vaspin attenuates high glucose-induced vascular smooth muscle cells proliferation and chemokinesis by inhibiting the MAPK, PI3K/Akt, and NF-κB signaling pathways. Atherosclerosis. 228:61–68. 2013.PubMed/NCBI