Cytokines profile in knee cartilage of rats during monoiodoacetate-induced osteoarthritis and administration of probiotic

Korotkyi, O. H.; Vovk, A. A.; Halenova, T. I.; Vovk, T. B.; Dvorshchenko, K. O.; Falalyeyeva, T. M.; Ostapchenko, L. I.

doi:10.7124/bc.000A1E

Biopolym. Cell. 2020; 36(1):23-35.

http://dx.doi.org/10.7124/bc.000A1E

Molecular Biomedicine

Cytokines profile in knee cartilage of rats during monoiodoacetate-induced osteoarthritis and administration of probiotic

1Korotkyi O. H., 1Vovk A. A., 1Halenova T. I., 1Vovk T. B., 1Dvorshchenko K. O., 1Falalyeyeva T. M., 1Ostapchenko L. I.

Educational and Scientific Center "Institute of Biology and Medicine",
Taras Shevchenko National University of Kyiv
64/13, Volodymyrska Str., Kyiv, Ukraine, 01601

Abstract

Aim. To identify the effect of probiotic (PB) on cytokines profile in knee cartilage of rats with experimental osteoarthritis (OA). Methods. The animals of 1st (Control) and 3rd (PB) groups got 50 µL of saline to both hind knees. The animals of 2nd (MIA-OA) and 4th groups (MIA-OA-PB) got single injection of 1 mg monoiodoacetate (MIA) dissolved in 50 µL of saline to knee, after which MIA-OA developed for 28 days. PB feeding [was] provided daily for 14 days during the MIA-OA progress. The levels of cytokines (IL-1β, TNF-α, IL-6, IL-8, IFN-γ, IL-4, IL-10, TGF-β, IGF-1) were measured in cartilage homogenates by [the] enzyme-linked immunosorbent assay (Biotrak ELISA System, GE Healthcare, USA). Results. MIA-OA caused [an] increase in the levels of IL-1β, TNF-α, IL-6, IL-8, IFN-γ, IL-10, TGF-β, decreased the level of IGF-1 and did not change the level of IL-4, compared to Control. PB during MIA-OA increased the level of IGF-1, decreased the levels of IL-1β, TNF-α, IL-6, IL-8, IFN-γ, TGF-β, compared to MIA-OA, but did not reach the Control values (unlike IL-4 and IL-10 that equaled to Control). Conclusions. MIA-OA caused significant changes in the levels of studied cytokines in knee cartilage. An application of PB has positive local anti-inflammatory effect in cartilage tissue of rats with MIA-OA.

Keywords: osteoarthritis, cytokines, growth factors, probiotic, cartilage

Full text: (PDF, in English)

References

[1] Glyn-Jones S, Palmer AJR, Agricola R, Price AJ, Vincent TL, Weinans H, Carr AJ. Osteoarthritis. Lancet. 2015; 386(9991):376-87.

[2] Woolf AD, Pfleger B. Burden of major musculoske-letal conditions. Bulletin of the World Health Organization. 2003; 81:646-56.

[3] Zhang W, Doherty MA, Peat G, Bierma-Zeinstra MA, Arden NK, Bresnihan B, Herrero-Beaumont G, Kirschner S, Leeb BF, Lohmander LS, Mazieres B, Pavelka K, Punzi L, So AK, Tuncer T, Watt I, Bijlsma JW. EULAR evidence-based recommendations for the diagnosis of knee osteoarthritis. Ann rheum dis. 2010; 69(3):483-9.

[4] Berenbaum F. Osteoarthritis as an inflammatory disease (osteoarthritis is not osteoarthrosis!). Osteoarthritis cartilage. 2013; 21(1):16-21.

[5] Yang CY, Chanalaris A, Troeberg L. ADAMTS and ADAM metalloproteinases in osteoarthritis-looking beyond the 'usual suspects'. Osteoarthritis Cartilage. 2017; 25(7):1000-9.

[6] Greene MA, Loeser RF. Aging-related inflammation in osteoarthritis. Osteoarthritis Cartilage. 2015; 23(11):1966-71.

[7] Pandey KR, Naik SR, Vakil BV. Probiotics, prebiotics and synbiotics-a review. J Food Sci Technol. 2015; 52(12):7577-87.

[8] Jevsevar DS, Shores PB, Mullen K, Schulte DM, Brown GA, Cummins DS. Mixed treatment comparisons for nonsurgical treatment of knee osteoarthritis: a network meta-analysis. J Am Acad Orthop Surg Glob Res Rev. 2018; 26(9):325-36.

[9] Bannuru RR., Osani MC, Vaysbrot EE, Arden NK, Bennell K, Bierma-Zeinstra SMA, Kraus VB, Lohmander LS, Abbott JH, Bhandari M, Dlanco FJ, Espinosa R, Haugen IK, Lin J, Mandl LA, Moilanen E, Nakamura N, Snyd-er-Mackler L, McAlindon TE. OARSI guidelines for the non-surgical management of knee, hip, and polyarticular osteoarthritis. Osteoarthritis Cartilage. 2019; S1063458419311161.

[10] Wongrakpanich S, Wongrakpanich A, Melhado K, Rangaswami J. A comprehensive review of non-steroidal anti-inflammatory drug use in the elderly. Aging Dis. 2018; 9(1):143.

[11] Rogers MA, Aronoff DM. The influence of non-steroidal anti-inflammatory drugs on the gut microbiome. Clinical Microbiolo Infect. 2016; 22(2):178.e1-178.e9.

[12] Savcheniuk O, Kobyliak N, Kondro M, Virchenko O, Falalyeyeva T, Beregova T. Short-term periodic consumption of multiprobiotic from childhood improves insulin sensitivity, prevents development of non-alcoholic fatty liver disease and adiposity in adult rats with glutamate-induced obesity. BMC Complementary Altern Med. 2014; 14(1):247.

[13] Kobyliak N, Abenavoli L, Falalyeyeva T, Beregova T. Efficacy of Probiotics and Smectite in Rats with Non-Alcoholic Fatty Liver Disease. Ann Hepatol. 2018; 17(1):153-161.

[14] Kobyliak N, Falalyeyeva T, Beregova T, Spivak M. Probiotics for experimental obesity prevention: focus on strain dependence and viability of composition. Endokrynol Pol. 2017; 68(6):659-667.

[15] Kobyliak N, Falalyeyeva T, Boyko N, Tsyryuk O, Beregova T, Ostapchenko L. Probiotics and nutraceuticals as a new frontier in obesity prevention and management. Diabetes Res Clin Pract. 2018; 141: 190-199.

[16] Kobyliak N, Virchenko O, Falalyeyeva T, Kondro M, Beregova T, Bodnar P, Shcherbakov O, Bubnov R, Caprnda M, Delev D, Sabo N, Kruzliak P, Rodrigo Opatrilova R, Spivak M. Cerium dioxide nanoparticles possess anti-inflammatory properties in the conditions of the obesity-associated NAFLD in rats. Biomed Pharmacother. 2017; 90: 608-614.

[17] Lee WJ, Hase K. Gut microbiota-generated metabolites in animal health and disease. Nat Chem Biol. 2014; 10(6):416.

[18] Li Y, Luo W, Deng Z, Lei G. Diet-intestinal microbiota axis in osteoarthritis: a possible role. Mediat Inflamm. 2016; 2016:3495173.

[19] Korotkyi O, Vovk A, Kuryk O, Dvorshchenko K, Falalyeyeva T, Ostapchenko L. Co-administration of live pro-biotics with chondroprotector in management of experimental knee osteoarthritis. Georgian Med News. 2018; 279:191-6.

[20] Dranitsina AS, Dvorshchenko KO, Korotkyi OH, Vovk AA, Falalyeyeva TM, Grebinyk DM, Ostapchenko LI. Expression of Nos2 and Acan Genes in Rat Knee Articular Cartilage in Osteoarthritis. Cytol Genet. 2019; 53(6):481-488.

[21] Korotkyi O, Dvorshchenko K, Vovk A, Dranitsina A, Tymoshenko M, Kot L, Ostapchenko L. Effect of probiotic composition on oxidative/antioxidant balance in blood of rats under experimental osteoarthritis. Ukr. Biochem. J. 2019; 91(6):49-58.

[22] Korotkyi O, Vovk A, Galenova T, Vovk T, Dvorschenko K, Luzza F, Abtnavoli L, Kobyiliak N, Falalyeyeva T, Ostapchenko L. Effect of probiotic on serum cytokines and matrix metalloproteinases profiles during monoi-odoacetate-induced osteoarthritis in rats. Minerva Biotecnol. 2019; 31(2):68-73.

[23] Dobrelia NV, Boitsova LV, Danova IV. Legal basis for conducting ethical expertise in preclinical studies of med-ical products using laboratory animals. Sixth National Congress on Bioethics. 2016; 47.

[24] National Research Council. Guide for the care and use of laboratory animals. Washington: "National Academies Press". 2010; 246p.

[25] Guzman RE, Evans MG, Bove S, Morenko B, Kilgore K. Monoiodoacetate-induced histologic changes in sub-chondral bone and articular cartilage of rat femorotibial joints: an animal model of osteoarthritis. Toxicol Pathol. 2003; 31(6): 619-24.

[26] Takahashi I, Matsuzaki T, Kuroki H, Hoso M. Induction of osteoarthritis by injecting monosodium iodoacetate into the patellofemoral joint of an experimental rat model. PloS One. 2018; 13(4):e0196625.

[27] Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976; 72(1-2):248-54.

[28] Kruger NJ. The Bradford method for protein quantitation. In: The protein protocols handbook. Totowa, NJ: "Humana Press", 2009; pp. 17-24.

[29] Horai R, Nakajima A, Habiro K, Kotani M, Nakae S, Matsuki T, Nambu A, Saiho S, Yayato K, Katsuko S, Oka-hara A, Tanioka H, Ikuse T, Ishii N, Schwartzberg PL, Abe R, Iwakura Y. TNF-α is crucial for the development of autoimmune arthritis in IL-1 receptor antagonist-deficient mice. J Clin Investig. 2004; 114(11): 1603-11.

[30] Turner MD, Nedjai B, Hurst T, Pennington DJ. Cytokines and chemokines: at the crossroads of cell signaling and inflammatory disease. Biochim Biophys Acta Mol Cell Res. 2014; 1843(11):2563-82.

[31] Wojdasiewicz P, Poniatowski ŁA, Szukiewicz D. The role of inflammatory and anti-inflammatory cytokines in the pathogenesis of osteoarthritis. Mediators Inflamm. 2014; 2014.

[32] So JS, Lee CG, Kwon HK, Yi HJ., Chae CS, Park JA, Hwang KC, Im, SH. Lactobacillus casei potentiates induc-tion of oral tolerance in experimental arthritis. Mol Immunol. 2008; 46(1):172-80.

[33] Bradley JR. TNF-mediated inflammatory disease. Rev Med Microbiol. 2008; 214(2):149-60.

[34] Yan S, Miao L, Lu Y, Wang L. MicroRNA-506 upregulation contributes to sirtuin 1 inhibition of osteoclastogenesis in bone marrow stromal cells induced by TNF-α treatment. Cell Biochem Funct. 2019; 2019.

[35] Daghestani HN, Kraus VB. Inflammatory biomarkers in osteoarthritis. Osteoarthritis Cartilage. 2015; 23(11):1890-6.

[36] So JS, Song MK, Kwon HK, Lee CG, Chae CS, Sahoo A, Jach A, Lee SH, Park ZY, Im SH. Lactobacillus casei enhances type II collagen/glucosamine-mediated suppression of inflammatory responses in experimental os-teoarthritis. Life Sci. 2011; 88(7-8):358-66.

[37] Goldring MB. The role of cytokines as inflammatory mediators in osteoarthritis: lessons from animal models. Connect Tissue Res. 1999; 40(1):1-11.

[38] Westacott CI, Sharif M. Cytokines in osteoarthritis: mediators or markers of joint destruction? Semin Arthritis Rheum. 1996; 25(4):254-72.

[39] Abdollahi-Roodsaz S, Abramson SB, Scher JU. The metabolic role of the gut microbiota in health and rheumatic disease: mechanisms and interventions. Nat Rev Rheumatol. 2016; 12(8):446.

[40] Cleophas MC, Crişan TO, Lemmers H, Toenhake-Dijkstra H, Fossati G, Jansen TL, Dinarello CA, Netea MG, Joosten LAB. Suppression of monosodium urate crystal-induced cytokine production by butyrate is mediated by the inhibition of class I histone deacetylases. Ann Rheum Dis. 2016; 75(3):593-600.

[41] Dinarello CA. Immunological and inflammatory functions of the interleukin-1 family. Ann Rev Immunol. 2009; 27:519-50.

[42] Seif F, Khoshmirsafa M, Aazami H, Mohsenzadegan M, Sedighi G, Bahar M. The role of JAK-STAT signaling pathway and its regulators in the fate of T helper cells. Cell Commun Signal. 2017; 15(1):23.

[43] Goldring MB, Otero M, Plumb DA, Dragomir C, Favero M, El Hachem K, Hashimoto K, Roach HI, Olivotto E, Borzi RM, Marcu KB. Roles of inflammatory and anabolic cytokines in cartilage metabolism: signals and multiple effectors converge upon MMP-13 regulation in osteoarthritis. Eur Cell Mater. 2011; 21:202.

[44] Sanderson NSR, Puntel M, Kroeger KM, Bondale NS, Swerdlow M, Iranmanesh N, Yagita H, Ibrahim A, Castro MG, Lowenstein PR. Cytotoxic immunological synapses do not restrict the action of interferon-γ to antigenic tar-get cells. Proc Natl Acad Sci. 2012; 109(20):7835-40.

[45] Kompanets IV, Korotkiy OG, Karpovets TP, Pilipenko SV, Nikolska VV, Ostapchenko LI, Yankovs-ky DS. Inter-feron titer and the 2',5'-oligoadenylate-synthetase activity in rat thymus lymphocytes in conditions of Omepra-zol-caused hypergastrinemia. Biopolym. Cell. 2013; 29(1):64-69.

[46] Kompanets I, Korotkiy A, Karpovets T, Ostapchenko L, Pilipenko S, Yankovskiy D. The interferon production and 2′,5′-oligoadenylate-synthetase activity in rat spleen lymphocytes at hypoacidity evoked by omeprazole injection and at administration of multiprobiotic «SYMBITER®». Curr. Issues Pharm. Med. Sci. 2013; 26(4):398-400.

[47] Seder RA, Gazzinelli R, Sher A, Paul WE. Interleukin 12 acts directly on CD4+ T cells to enhance priming for interferon gamma production and diminishes interleukin 4 inhibition of such priming. Proc Natl Acad Sci. 1993; 90(21):10188-92.

[48] O'Neill LA, Kishton RJ, Rathmell J. A guide to immunometabolism for immunologists. Nat Rev Immunol. 2016; 16(9):553.

[49] Mobasheri A, Bay-Jensen AC, Van-Spil WE, Larkin J, Levesque MC. Osteoarthritis Year in Review 2016: bio-markers (biochemical markers). Osteoarthritis Cartilage. 2017; 25(2):199-208.

[50] Vulpen LF, Popov-Celeketic J, Meegeren ME, Coeleveld K, Laar JM, Hack CE, Schutgens REG, Mastbergen SC, Lafeber, F. P. A fusion protein of interleukin-4 and interleukin-10 protects against blood-induced cartilage dam-age in vitro and in vivo. J Thromb Haemost. 2017; 15(9):1788-98.

[51] Steen-Louws C, Popov-Celeketic J, Mastbergen SC, Coeleveld K, Hack CE, Eijkelkamp N, Trifonidou M, Spruijt S, Roon JAG, Lafeber FPJG. IL4-10 fusion protein has chondroprotective, anti-inflammatory and potentially analgesic effects in the treatment of osteoarthritis. Osteoarthritis Cartilage. 2018; 26(8):1127-35.

[52] Roon JA, Lafeber FP, Bijlsma JW. Synergistic activity of interleukin-4 and interleukin-10 in suppression of in-flammation and joint destruction in rheumatoid arthritis [review]. Arthritis Rheum. 2001; 44:3-12.

[53] Davidson EB, Kraan PM, Berg WB. TGF-β and osteoarthritis. Osteoarthritis Cartilage. 2007; 15(6):597-604.

[54] Shen J, Li S, Chen D. TGF-β signaling and the development of osteoarthritis. Bone Res. 2014; 2:14002.

[55] Davidson ENB, Vitters EL, Berg WB, Kraan PM. TGF β-induced cartilage repair is maintained but fibrosis is blocked in the presence of Smad7. Arthritis Res Ther. 2006; 8(3):R65.

[56] Kraan PM, Davidson EB, Blom A, Berg WB. TGF-beta signaling in chondrocyte terminal differentiation and osteoarthritis: modulation and integration of signaling pathways through receptor Smads. Osteoarthritis Carti-lage. 2009; 17(12):1539-45.

[57] Korotkyi O, Vovk A, Dranitsina A, Dvorshenko K, Fagoonee S, Falalyeyeva T, Ostapchenko L. The influence of probiotic diet and chondroitin sulfate administration on Ptgs2, Tgfb1 and Col2a1 expression in rat knee cartilage during monoiodoacetate-induced osteoarthritis. Minerva Med. 2019; 110(5): 419-24.

[58] Korotkyi O, Vovk A, Blokhina O, Dvorshchenko K, Falalyeyeva T, Abenavoli L, Ostapchenko L. Effect of chon-droitin Sulfate on blood serum cytokine profile during carrageenan-induced edema and monoiodoacetate-induced osteoarthritis in rats. Rev Recent Clin Trials. 2019; 14(1): 50-55.

[59] Kraan PM. Differential role of transforming growth factor-beta in an osteoarthritic or a healthy joint. J Bone Metab. 2018; 25(2):65-72.

[60] Lu S, Lam J, Trachtenberg JE, Lee EJ, Seyednejad H, Beucken JJ, Tabata Y, Kasper FK, Scott DW, Wong ME, Jansen JA, Mikos AG: Technical report: correlation between the repair of cartilage and subchondral bone in an osteochondral defect using bilayered, biodegradable hydrogel composites. Tissue Eng Part C Methods. 2015; 21:1216-25.

[61] Wei FY, Lee JK, Wei L, Qu F, Zhang JZ. Correlation of insulin-like growth factor 1 and osteoarthritic cartilage degradation: a spontaneous osteoarthritis in guinea-pig. Eur Rev Med Pharmacol Sci. 2017; 21(20): 4493-50.

[62] Chubinskaya S, Hakimiyan A, Pacione C, Yanke A, Rappoport L, Aigner T, Rueger DC, Loeser RF. Synergistic effect of IGF-1 and OP-1 on matrix formation by normal and OA chondrocytes cultured in alginate beads. Os-teoarthritis Cartilage. 2007; 15(4): 421-30.

[63] Steves CJ, Bird S, Williams FM, Spector TD. The microbiome and musculoskeletal conditions of aging: a review of evidence for impact and potential therapeutics. JBMR Plus. 2016; 31(2):261-9.

[64] Sarah HY, Jernigan JA, McDonald LC. Prevalence of probiotic use among inpatients: a descriptive study of 145 US hospitals. Am J Infect Control. 2016; 44(5):548-53.

[65] Lee SH, Kwon JY, Jhun J, Jung K, Park SH, Yang CW, Cho Y, Kim SJ, Cho ML. Lactobacillus acidophilus ameli-orates pain and cartilage degradation in experimental osteoarthritis. Immunol Lett. 2018; 203:6-14.

[66] Lei M, Guo C, Wang D, Zhang C, Hua L. The effect of probiotic Lactobacillus casei Shirota on knee osteoarthri-tis: a randomised double-blind, placebo-controlled clinical trial. Benef Microbes. 2017; 8(5):697-703.

[67] Henrotin Y, Patrier S, Pralus A, Roche M, Nivoliez A. Protective actions of oral administration of Bifidobacterium longum CBi0703 in spontaneous osteoarthritis in Dunkin Hartley guinea pig model. Cartilage. 2019; 2019:1947603519841674.

[68] Kwon JY, Lee SH, Jhun J, Choi J, Jung K, Cho KH, Kim SJ, Yang CW, Park SH, Cho ML. The combination of probiotic complex, rosavin, and zinc improves pain and cartilage destruction in an osteoarthritis rat model. J Med Food. 2018; 21(4):364-71.