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Grape Seed Proanthocyanidin Extract Ameliorates Monosodium Iodoacetate-Induced Osteoarthritis

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Grape Seed Proanthocyanidin Extract Ameliorates Monosodium Iodoacetate-Induced Osteoarthritis EXPERIMENTAL and MOLECULAR MEDICINE, Vol. 43, No. 10, 561-570, October 2011 Grape seed proanthocyanidin extract ameliorates monosodium iodoacetate-induced osteoarthritis Yun Ju Woo1*, Young Bin Joo4*, monosodium iodoacetate (MIA)-induced arthritis of Young Ok Jung2, Ji Hyeon Ju1, Mi La Cho1,5, the knee joint of rat, which is an animal model of human Hye Jwa Oh1, Joo Youn Jhun1, OA. GSPE (100 mg/kg or 300 mg/kg) or saline was given Mi Kyung Park1, Jin Sil Park1, orally three times per week for 4 weeks after the MIA injection. Pain was measured using the paw with- Chang Min Kang1, Mi Sook Sung3, drawal latency (PWL), the paw withdrawal threshold Sung Hwan Park1, Ho Youn Kim1 4,5 (PWT) and the hind limb weight bearing ability. Joint and Jun Ki Min damage was assessed using histological and micro- scopic analysis and microcomputerized tomography. 1 The Rheumatism Research Center Matrix metalloproteinase-13 (MMP13) and nitro- Catholic Research Institute of Medical Science tyrosine were detected using immunohistochemistry. The Catholic University of Korea Administration of GSPE to the MIA-treated rats sig- Seoul 137-701, Korea 2 nificantly increased the PWL and PWT and this resulted Division of Rheumatology in recovery of hind paw weight distribution (P ＜ 0.05). Department of Internal Medicine GSPE reduced the loss of chondrocytes and proteo- Kangnam Sacred Heart Hospital glycan, the production of MMP13, nitrotyrosine and Hallym University IL-1β and the formation of osteophytes, and it reduced Seoul 137-701, Korea the number of subchondral bone fractures in the 3Department of Radiology 4 MIA-treated rats. These results indicate that GSPE is Department of Internal Medicine antinociceptive and it is protective against joint dam- Bucheon St. Mary's Hospital age in the MIA-treated rat model of OA. GSPE could Bucheon 420-818, Korea 5Corresponding authors: Tel, 82-2-2258-7467; open up novel avenues for the treatment of OA. Fax, 82-2-599-4287; E-mail, [email protected] (M.L.C.) Keywords: antioxidants; grape seed proanthocyani- Tel, 82-32-340-7016; Fax, 82-32-340-2669; dins; inflammation; interleukin-1β; osteoarthritis E-mail, [email protected] (J.K.M.) *These authors contributed equally to this work. http://dx.doi.org/10.3858/emm.2011.43.10.062 Introduction Accepted 25 July 2011 Osteoarthritis (OA) is a degenerative disorder of Available Online 28 July 2011 the joints that causes significant pain and func- Abbreviations: GSPE, grape seed proanthocyanidin extract; tional disability. OA involves not only the articular MIA, monosodium iodoacetate; MMP, matrix metalloproteinase; cartilage, but also the subchondral bone, liga- - O2 , superoxide anion; OA, osteoarthritis; OH, hydroxyl radicals; ments, synovial membrane and periarticular mus- ONOO-, peroxynitrite; PWL, paw withdrawal latency; PWT, cle (Chen et al., 2010; Henrotin and Kurz, 2007; paw withdrawal threshold; ROS, reactive oxygen species; Krasnokutsky et al., 2008). The cause of OA is un- TRP, transient receptor potential; VIP, vasoactive intestinal known, but several studies have suggested that peptide this joint degeneration results from the combination of mechanical stress and biochemical factors, and mainly reactive oxygen species (ROS) and matrix metalloproteinases (MMPs) (Henrotin and Kurz, Abstract 2007). - ROS such as the superoxide anion (O2 ), hydro- Osteoarthritis (OA) is an age-related joint disease that gen peroxide (H2O2) and hydroxyl radicals (OH) act is characterized by degeneration of articular cartilage as a physiological defense system against micro- and chronic pain. Oxidative stress is considered one bial infection and they are involved in maintaining of the pathophysiological factors in the progression of normal cellular functions and intracellular signal OA. We investigated the effects of grape seed proan- transduction (Filippin et al., 2008). However, as thocyanidin extract (GSPE), which is an antioxidant, on ROS are capable of damaging lipids, proteins, 562 Exp. Mol. Med. Vol. 43(10), 561-570, 2011 DNA and the extracellular matrix, excess ROS are Results removed by antioxidants (Dröge, 2002). Ultimately, oxidative stress refers to a cellular Effects of GSPE on the pain in the MIA-induced OA state in which the production of ROS is elevated model and/or the levels of antioxidants are reduced. The mechanical paw withdrawal thresholds to von There is much evidence indicating that oxidative Frey stimuli were measured for 4 weeks after MIA stress is involved in the pathogenesis of OA. injection using a dynamic plantar esthesiometer. Increased ROS promote cartilage degradation by Four days after the injection of MIA, the paw with- inhibiting cartilage matrix synthesis and inducing drawal latency (PWL) and paw withdrawal thresh- chondrocyte apoptosis and cartilage matrix break- down (Henrotin et al., 2005). The serum total anti- oxidant capacity, the thiol level and the catalase activity of OA patients are low (Altindag et al., 2007). The cartilage from patients with OA contains less extracellular antioxidants such as superoxide dismutase than does normal cartilage (Regan et al., 2005). The levels of nitrated type II collagen peptides in the sera of patients with OA are ele- vated, which is indicative of the formation of perox- ynitrite (ONOO-), which is a marker of oxidative stress (Deberg et al., 2005). Intra-articular injection of monosodium iodoace- tate (MIA) induces disorganization of the articular cartilage by inhibiting the activity of glycer- aldehyde-3- phosphate dehydrogenase in chon- drocytes, and this results in disruption of glycolysis and eventual cell death. These chondrocytes have similar histopathology to that of human OA and the MIA induced OA animal model closely mimics both the pain and structural changes associated with the disease (Janusz et al., 2001; Bove et al., 2003). Grape seed extract contains lipids, proteins, car- bohydrates and polyphenols. Proanthocyanidins are potent natural antioxidants, and they are the most abundant phenolic compounds in grape seeds and they are high molecular weight poly- mers comprised of dimers or trimers of (+)-cat- echin and (-)-epicatechin (Fine, 2000). It has been suggested that grape seed proanthocyanidin ex- tract (GSPE) is an effective therapy for oxida- tion-related diseases in animal models of tumors, atherosclerosis, gastric ulcers, cataracts, diabetic retinopathy and rheumatoid arthritis (Ray et al., 2001; Sato et al., 2001; Pataki et al., 2002; Durukan et al., 2006; Cho et al., 2009; Prasain et al., 2009). However, its effects on the chronic pain Figure 1. Effects of GSPE on the pain in MIA-induced OA. An ex- and structural damage relevant to the pain in OA perimental model of OA in rats was induced by intraarticular injection of have not been investigated. We examined whether monosodium iodoacetate (MIA) into the knee joint. Oral treatment with GSPE (100 mg/kg or 300 mg/kg given three times per week) or with ve- GSPE relieves pain and if it prevents the structural hicle was initiated on MIA injection (day 0). (A) The paw withdrawal la- changes known to cause pain in a rat model of OA tency and (B) paw withdrawal threshold were measured by a dynamic produced by MIA injection. plantar aesthesiometer and this was compared with that of the MIA-treat- ed group. △: nonarthritis group, ▲: MIA-treated group, ◇: MIA-treated rats treated with 300 mg/kg GSPE. *P ＜ 0.05, **P ＜ 0.01 compared with the MIA injection group. (C) Weight bearing was measured by an in- capacitance tester and this was compared with that of the MIA-treated group at 4 weeks after the injection of MIA. *P ＜ 0.05 compared with the MIA injection group. The experiment was repeated 3 times with sim- ilar results. GSPE ameliorate osteoarthritis 563 0.01). Seven days after the injection of MIA, the PWL and PWT in the GSPE-treated groups had re- covered to a greater extent than that in the MIA-treated group (P ＜ 0.05) and this trend was maintained for 4 weeks (Figures 1A and 1B). Hind limb weight bearing is a measure of pain and this was measured using an incapacitance tester. Four weeks after the MIA injection, the hind limb weight bearing of the ipsilateral limb was sig- nificantly lower in the MIA-treated group than that in the nonarthritis group. The 300 mg/kg GSPE treated group exhibited significant recovery of hind limb weight bearing (P ＜ 0.05, Figure 1C). OA is characterized not only by progressive car- tilage destruction, but also by alterations in bone such as osteoclast recruitment to subchondral bone and osteophyte formation. Osteophytes are also called bone spurs, and they are smooth out- growths of bone that build up on the edges of joints Figure 2. Osteoclastic activity and osteophyte formation for 4 weeks af- due to OA. Therefore, we analyzed the osteoclastic ter MIA injection. Bone and osteophyte formation was evaluated in the activity and osteophyte formation. At 4 weeks after hematoxylin and eosin-stained, paraffin-embedded knee joint sections MIA injection along with GSPE treatment, histo- and micro-CT analysis of the MIA injected rats treated with GSPE or ve- logical analysis revealed osteoclasts on the sub- hicle, respectively. (A) Osteoclast generation was assessed using hema- toxylin and eosin. The bar graphs represent the mean values ± SD of chondral bone fragmented trabeculae of the the cells that stained positive (original magnification × 200). **P ＜ 0.01 MIA-treated group (arrow), but GPSE decreased compared with the MIA injection group. (B) Osteophyte analysis using osteoclast generation (Figure 2A). We used mi- Micro-CT. cro-CT to examine the direct effect of GSPE on the MIA-induced osteophyte formation. Osteophytes were detected in the MIA-treated group, but not in old (PWT) were lower in the MIA-treated group the GSPE-treated groups (Figure 2B). In our rat than in the nonarthritis group, which had received a model of OA, the histological and micro-CT analy- saline injection instead of MIA.
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