Parasitic infection as a potential therapeutic tool against rheumatoid arthritis (Review)
- Authors:
- Shadike Apaer
- Tuerhongjiang Tuxun
- Hai‑Zhang Ma
- Heng Zhang
- Amina Aierken
- Abudusalamu Aini
- Yu‑Peng Li
- Ren‑Yong Lin
- Hao Wen
-
Affiliations: State Key Laboratory of Xinjiang Major Diseases Research and Xinjiang Key Laboratory of Echinococcosis, First Affiliated Hospital of Xinjiang Medical University, Urumqi, Xinjiang 830054, P.R. China, Department of Ultrasonography, First Affiliated Hospital of Xinjiang Medical University, Urumqi, Xinjiang 830054, P.R. China - Published online on: September 5, 2016 https://doi.org/10.3892/etm.2016.3660
- Pages: 2359-2366
This article is mentioned in:
Abstract
|
Davidson A and Diamond B: Autoimmune diseases. N Engl J Med. 345:340–350. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Hollan I, Meroni PL, Ahearn JM, Tervaert JW Cohen, Curran S, Goodyear CS, Hestad KA, Kahaleh B, Riggio M, Shields K and Wasko MC: Cardiovascular disease in autoimmune rheumatic diseases. Autoimmun Rev. 12:1004–115. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Cooper GS, Bynum ML and Somers EC: Recent insights in the epidemiology of autoimmune diseases: Improved prevalence estimates and understanding of clustering of diseases. J Autoimmun. 33:197–207. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Hayter SM and Cook MC: Updated assessment of the prevalence, spectrum and case definition of autoimmune disease. Autoimmun Rev. 11:754–765. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Wahren-Herlenius M and Dörner T: Immunopathogenic mechanisms of systemic autoimmune disease. Lancet. 382:819–831. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Somers EC, Thomas SL, Smeeth L and Hall AJ: Autoimmune diseases co-occurring within individuals and within families: A systematic review. Epidemiology. 17:202–217. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Fina-Aviles F, Medina-Peralta M, Mendez-Boo L, Hermosilla E, Elorza JM, Garcia-Gil M, Ramos R, Bolibar B, Javaid MK, Edwards CJ, et al: The descriptive epidemiology of rheumatoid arthritis in Catalonia: A retrospective study using routinely collected data. Clin Rheumatol. 35:751–757. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Cotsapas C, Voight BF, Rossin E, Lage K, Neale BM, Wallace C, Abecasis GR, Barrett JC, Behrens T, Cho J, et al: Pervasive sharing of genetic effects in autoimmune disease. PLoS Genet. 7:e10022542011. View Article : Google Scholar : PubMed/NCBI | |
|
Maruotti N, d'Onofrio F and Cantatore FP: Metabolic syndrome and chronic arthritis: Effects of anti-TNF-α therapy. Clin Exp Med. 27:433–438. 2015. View Article : Google Scholar | |
|
Bilecik NA, Tuna S, Samanci N, Balci N and Akbaş H: Prevalence of metabolic syndrome in women with rheumatoid arthritis and effective factors. Int J Clin Exp Med. 7:2258–2256. 2014.PubMed/NCBI | |
|
Zhang J, Fu L, Shi J, Chen X, Li Y, Ma B and Zhang Y: The risk of metabolic syndrome in patients with rheumatoid arthritis: A meta-analysis of observational studies. PLoS One. 8:e781512013. View Article : Google Scholar : PubMed/NCBI | |
|
Johnston MJ, MacDonald JA and McKay DM: Parasitic helminths: A pharmacopeia of anti-inflammatory molecules. Parasitology. 136:125–147. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Richard-Miceli C and Criswell LA: Emerging patterns of genetic overlap across autoimmune disorders. Genome Med. 4:62012. View Article : Google Scholar : PubMed/NCBI | |
|
Im CH, Kim NR, Kang JW, Kim JH, Kang JY, Bae GB, Nam EJ and Kang YM: Inflammatory burden interacts with conventional cardiovascular risk factors for carotid plaque formation in rheumatoid arthritis. Rheumatology (Oxford). 9:808–815. 2015. View Article : Google Scholar | |
|
Rubbert-Roth A: Assessing the safety of biologic agents in patients with rheumatoid arthritis. Rheumatology (Oxford). 51 Suppl 5:v38–v47. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Greenwood BM, Voller A and Herrick EM: Suppression of adjuvant arthritis by infection with a strain of the rodent malaria parasite Plasmodium berghei. Ann Rheum Dis. 29:321–333. 1970. View Article : Google Scholar : PubMed/NCBI | |
|
Pearson DJ and Taylor G: The influence of the nematode Syphacia oblevata on adjuvant arthritis in the rat. Immunology. 29:391–396. 1975.PubMed/NCBI | |
|
Rocha FA, Leite AK, Pompeu MM, Cunha TM, Verri WA Jr, Soares FM, Castro RR and Cunha FQ: Protective effect of an extract from Ascaris suum in experimental arthritis models. Infect Immun. 76:2736–2745. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Osada Y, Shimizu S, Kumagai T, Yamada S and Kanazawa T: Schistosoma mansoni infection reduces severity of collagen-induced arthritis via down-regulation of pro-inflammatory mediators. Int J Parasitol. 39:457–464. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Zaccone P, Fehervari Z, Phillips JM, Dunne DW and Cooke A: Parasitic worms and inflammatory diseases. Parasite Immunol. 28:515–523. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Greenwood BM, Herrick EM and Voller A: Can parasitic infection suppress autoimmune disease? Proc R Soc Med. 63:19–20. 1970.PubMed/NCBI | |
|
Espinoza-Jiménez A, Rivera-Montoya I, Cárdenas-Arreola R, Morán Land and Terrazas LI: Taenia crassiceps infection attenuates multiple low-dose streptozotocin-induced diabetes. J Biomed Biotechnol. 2010:8505412010. View Article : Google Scholar : PubMed/NCBI | |
|
Taylor G and Walker J: CharlesHarrison, Blackley 1820-1900. Clin Allergy. 3:103–108. 1973. View Article : Google Scholar : PubMed/NCBI | |
|
Strachan DP: Hay fever, hygiene, and household size. BMJ. 299:1259–1260. 1989. View Article : Google Scholar : PubMed/NCBI | |
|
Rook GA: 99th Dahlem conference on infection, inflammation and chronic inflammatory disorders: Darwinian medicine and the ‘hygiene’ or ‘old friends’ hypothesis. Clin Exp Immunol. 160:70–79. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Reyes JL, Espinoza-Jiménez AF, González MI, Verdin L and Terrazas LI: Taenia crassiceps infection abrogates experimental autoimmune encephalomyelitis. Cell Immunol. 267:77–87. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
La Flamme AC, Ruddenklau K and Bäckström BT: Schistosomiasis decreases central nervous system inflammation and alters the progression of experimental autoimmune encephalomyelitis. Infect Immun. 71:4996–5004. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Somers EC, Thomas SL, Smeeth L and Hall AJ: Autoimmune diseases co-occurring within individuals and within families: A systematic review. Epidemiology. 17:202–227. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
McKay DM: The beneficial helminth parasite? Parasitology. 132:1–12. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Graepel R, Leung G, Wang A, Villemaire M, Jirik FR, Sharkey KA, McDougall JJ and McKay DM: Murine autoimmune arthritis is exaggerated by infection with the rat tapeworm, Hymenolepis diminuta. Int J Parasitol. 43:593–601. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Hunter MM, Wang A and McKay DM: Helminth infection enhances disease in a murine TH2 model of colitis. Gastroenterology. 132:1320–1330. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Chen CC, Louie S, McCormick B, Walker WA and Shi HN: Concurrent infection with an intestinal helminth parasite impairs host resistance to enteric Citrobacter rodentium and enhances Citrobacter-induced colitis in mice. Infect Immun. 73:5468–5481. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Shi M, Wang A, Prescott D, Waterhouse CC, Zhang S, McDougall JJ, Sharkey KA and McKay DM: Infection with an intestinal helminth parasite reduces Freund's complete adjuvant-induced monoarthritis in mice. Arthritis Rheum. 63:434–444. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Balic A, Harcus Y, Holland MJ and Maizels RM: Selective maturation of dendritic cells by Nippostrongylus brasiliensis-secreted proteins drives Th2 immune responses. Eur J Immunol. 34:3047–3059. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Smits HH, Everts B, Hartgers FC and Yazdanbakhsh M: Chronic helminth infections protect against allergic diseases by active regulatory processes. Curr Allergy Asthma Rep. 10:3–12. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Harn DA, McDonald J, Atochina O and Da'dara AA: Modulation of host immune responses by helminth glycans. Immunol Rev. 230:247–257. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Daniłowicz-Luebert E, O'Regan NL, Steinfelder S and Hartmann S: Modulation of specific and allergy-related immune responses by helminths. J Biomed Biotechnol. 2011:8215782011. View Article : Google Scholar : PubMed/NCBI | |
|
Bouchery T, Kyle R, Ronchese F and Le Gros G: The differentiation of CD4 (+) T-helper cell subsets in the context of helminth parasite infection. Front Immunol. 5:4872014. View Article : Google Scholar : PubMed/NCBI | |
|
Vignali DA, Crocker P, Bickle QD, Cobbold S, Waldmann H and Taylor MG: A role for CD4+ but not CD8+ T cells in immunity to Schistosoma mansoni induced by 20 krad-irradiated and Ro 11-3128-terminated infections. Immunology. 67:466–472. 1989.PubMed/NCBI | |
|
Katona IM, Urban JF Jr and Finkelman FD: The role of L3T4+ and Lyt-2+ T cells in the IgE response and immunity to Nippostrongylus brasiliensis. J Immunol. 140:3206–3211. 1988.PubMed/NCBI | |
|
Urban JF Jr, Noben-Trauth N, Donaldson DD, Madden KB, Morris SC, Collins M and Finkelman FD: IL-13, IL-4Ralpha and Stat6 are required for the expulsion of the gastrointestinal nematode parasite Nippostrongylus brasiliensis. Immunity. 8:255–264. 1998. View Article : Google Scholar : PubMed/NCBI | |
|
Allen JE and Maizels RM: Diversity and dialogue in immunity to helminths. Nat Rev Immunol. 11:375–358. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Zhu J, Min B, Hu-Li J, Watson CJ, Grinberg A, Wang Q, Killeen N, Urban JF Jr, Guo L and Paul WE: Conditional deletion of Gata3 shows its essential function in T (H)1-T (H)2 responses. Nat Immunol. 5:1157–1165. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang Y, Chen L, Gao W, Hou X, Gu Y, Gui L, Huang D, Liu M, Ren C, Wang S and Shen J: IL-17 neutralization significantly ameliorates hepatic granulomatous inflammation and liver damage in Schistosoma japonicum infected mice. Eur J Immunol. 42:1523–1535. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Rutitzky LI, da Rosa JR Lopes and Stadecker MJ: Severe CD4 T cell-mediated immunopathology in murine schistosomiasis is dependent on IL-12p40 and correlates with high levels of IL-17. J Immunol. 175:3920–3926. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Baumgart M, Tompkins F, Leng J and Hesse M: Naturally occurring CD4+Foxp3+ regulatory T cells are an essential, IL-10-independent part of the immunoregulatory network in Schistosoma mansoni egg-induced inflammation. J Immunol. 176:5374–5387. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Taylor MD, LeGoff L, Harris A, Malone E, Allen JE and Maizels RM: Removal of regulatory T cell activity reverses hyporesponsiveness and leads to filarial parasite clearance in vivo. J Immunol. 174:4924–4933. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Taylor JJ, Mohrs M and Pearce EJ: Regulatory T cell responses develop in parallel to Th responses and control the magnitude and phenotype of the Th effector population. J Immunol. 176:5839–5847. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Faulkner H, Humphreys N, Renauld JC, Van Snick J and Grencis R: Interleukin-9 is involved in host protective immunity to intestinal nematode infection. Eur J Immunol. 27:2536–2540. 1997. View Article : Google Scholar : PubMed/NCBI | |
|
Harris ED Jr: Rheumatoid arthritis. Pathophysiology and implications for therapy. N Engl J Med. 322:1277–2289. 1990. View Article : Google Scholar : PubMed/NCBI | |
|
Schulze-Koops H and Kalden JR: The balance of Th1/Th2 cytokines in rheumatoid arthritis. Best Pract Res Clin Rheumatol. 15:677–691. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Choy EH and Panayi GS: Cytokine pathways and joint inflammation in rheumatoid arthritis. N Engl J Med. 344:907–916. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Kong YY, Feige U, Sarosi I, Bolon B, Tafuri A, Morony S, Capparelli C, Li J, Elliott R, McCabe S, et al: Activated T cells regulate bone loss and joint destruction in adjuvant arthritis through osteoprotegerin ligand. Nature. 402:304–309. 1999. View Article : Google Scholar : PubMed/NCBI | |
|
Mitamura M, Nakano N, Yonekawa T, Shan L, Kaise T, Kobayashi T, Yamashita K, Kikkawa H and Kinoshita M: T cells are involved in the development of arthritis induced by anti-type II collagen antibody. Int Immunopharmacol. 7:1360–1368. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Billingham ME: Models of arthritis and the search for anti-arthritic drugs. Pharmacol Ther. 21:389–428. 1983. View Article : Google Scholar : PubMed/NCBI | |
|
Cho YG, Cho ML, Min SY and Kim HY: Type II collagen autoimmunity in a mouse model of human rheumatoid arthritis. Autoimmun Rev. 7:65–70. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Balkwill FR and Burke F: The cytokine network. Immunol Today. 10:299–304. 1989. View Article : Google Scholar : PubMed/NCBI | |
|
Shingu M and Nagai Y, Isayama T, Naono T, Nobunaga M and Nagai Y: The effects of cytokines on metalloproteinase inhibitors (TIMP) and collagenase production by human chondrocytes and TIMP production by synovial cells and endothelial cells. Clin Exp Immunol. 94:145–149. 1993. View Article : Google Scholar : PubMed/NCBI | |
|
Vermeire K, Heremans H, Vandeputte M, Huang S, Billiau A and Matthys P: Accelerated collagen-induced arthritis in IFN-gamma receptor-deficient mice. J Immunol. 158:5507–5513. 1997.PubMed/NCBI | |
|
Kelchtermans H, Billiau A and Matthys P: How interferon-gamma keeps autoimmune diseases in check. Trends Immunol. 29:479–486. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Guedez YB, Whittington KB, Clayton JL, Joosten LA, van de Loo FA, van den Berg WB and Rosloniec EF: Genetic ablation of interferon-gamma up-regulates interleukin-1beta expression and enables the elicitation of collagen-induced arthritis in a nonsusceptible mouse strain. Arthritis Rheum. 44:2413–2424. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Manoury-Schwartz B, Chiocchia G, Bessis N, Abehsira-Amar O, Batteux F, Muller S, Huang S, Boissier MC and Fournier C: High susceptibility to collagen-induced arthritis in mice lacking IFN-gamma receptors. J Immunol. 158:5501–5506. 1997.PubMed/NCBI | |
|
Remmers EF, Plenge RM, Lee AT, Graham RR, Hom G, Behrens TW, de Bakker PI, Le JM, Lee HS, Batliwalla F, et al: STAT4 and the risk of rheumatoid arthritis and systemic lupus erythematosus. N Engl J Med. 357:977–986. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Trinchieri G: Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat Rev Immunol. 3:133–146. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Boissier MC: Cell and cytokine imbalances in rheumatoid synovitis. Joint Bone Spine. 78:230–234. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Chen R, Tao Y, Qiu K, Huang W, Huang C and Li J: Association of circulating Treg cells with disease activity in patients with rheumatoid arthritis. Nan Fang Yi Ke Da Xue Xue Bao. 32:886–889. 2012.(In Chinese). PubMed/NCBI | |
|
Groux H, O'Garra A, Bigler M, Rouleau M, Antonenko S, de Vries JE and Roncarolo MG: A CD4+ T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature. 389:737–742. 1997. View Article : Google Scholar : PubMed/NCBI | |
|
O'Garra A and Vieira P: Regulatory T cells and mechanisms of immune system control. Nat Med. 10:801–805. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Schopf LR, Hoffmann KF, Cheever AW, Urban JF Jr and Wynn TA: IL-10 is critical for host resistance and survival during gastrointestinal helminth infection. J Immunol. 168:2383–2392. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Harrington LE, Hatton RD, Mangan PR, Turner H, Murphy TL, Murphy KM and Weaver CT: Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol. 6:1123–1132. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Langrish CL, Chen Y, Blumenschein WM, Mattson J, Basham B, Sedgwick JD, McClanahan T, Kastelein RA and Cua DJ: IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J Exp Med. 201:233–240. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Hirota K, Hashimoto M, Yoshitomi H, Tanaka S, Nomura T, Yamaguchi T, Iwakura Y, Sakaguchi N and Sakaguchi S: T cell self-reactivity forms a cytokine milieu for spontaneous development of IL-17+ Th cells that cause autoimmune arthritis. J Exp Med. 204:41–47. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Nakae S, Nambu A, Sudo K and Iwakura Y: Suppression of immune induction of collagen-induced arthritis in IL-17-deficient mice. J Immunol. 171:6173–6177. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Lubberts E, van den Bersselaar L, Oppers-Walgreen B, Schwarzenberger P, Coenen-de Roo CJ, Kolls JK, Joosten LA and van den Berg WB: IL-17 promotes bone erosion in murine collagen-induced arthritis through loss of the receptor activator of NF-kappaB ligand/osteoprotegerin balance. J Immunol. 170:2655–2662. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
van den Berg WB and Miossec P: IL-17 as a future therapeutic target for rheumatoid arthritis. Nat Rev Rheumatol. 5:549–553. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Hirota K, Yoshitomi H, Hashimoto M, Maeda S, Teradaira S, Sugimoto N, Yamaguchi T, Nomura T, Ito H, Nakamura T, et al: Preferential recruitment of CCR6-expressing Th17 cells to inflamed joints via CCL20 in rheumatoid arthritis and its animal model. J Exp Med. 204:2803–2812. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Cua DJ, Sherlock J, Chen Y, Murphy CA, Joyce B, Seymour B, Lucian L, To W, Kwan S, Churakova T, et al: Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature. 421:744–748. 2003. View Article : Google Scholar : PubMed/NCBI | |
|
Tallima H, Salah M, Guirguis FR and E Ridi R: Transforming growth factor-beta and Th17 responses in resistance to primary murine Schistosomiasis mansoni. Cytokine. 48:239–245. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Chen Z and O'Shea JJ: Regulation of IL-17 production in human lymphocytes. Cytokine. 41:71–78. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Azizi G, Jadidi-Niaragh F and Mirshafiey A: Th17 cells in immunopathogenesis and treatment of rheumatoid arthritis. Int J Rheum Dis. 16:243–253. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Roeleveld DM and Koenders MI: The role of the Th17 cytokines IL-17 and IL-22 in Rheumatoid Arthritis pathogenesis and developments in cytokine immunotherapy. Cytokine. 74:101–107. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Song X, Shen J, Wen H, Zhong Z, Luo Q, Chu D, Qi Y, Xu Y and Wei W: Impact of Schistosoma japonicum infection on collagen-induced arthritis in DBA/1 mice: A murine model of human rheumatoid arthritis. PLoS One. 6:e234532011. View Article : Google Scholar : PubMed/NCBI | |
|
Mattsson L, Larsson P, Erlandsson-Harris H, Klareskog L and Harris RA: Parasite-mediated down-regulation of collagen-induced arthritis (CIA) in DA rats. Clin Exp Immunol. 122:477–483. 2000. View Article : Google Scholar : PubMed/NCBI | |
|
Brennan FM, Chantry D, Turner M, Foxwell B, Maini R and Feldmann M: Detection of transforming growth factor-beta in rheumatoid arthritis synovial tissue: Lack of effect on spontaneous cytokine production in joint cell cultures. Clin Exp Immunol. 81:278–285. 1990. View Article : Google Scholar : PubMed/NCBI | |
|
Pohlers D, Beyer A, Koczan D, Wilhelm T, Thiesen HJ and Kinne RW: Constitutive upregulation of the transforming growth factor-beta pathway in rheumatoid arthritis synovial fibroblasts. Arthritis Res Ther. 9:R592007. View Article : Google Scholar : PubMed/NCBI | |
|
Gonzalo-Gil E, do G, Santiago B, Dotor J, Pablos JL and Galindo M: Transforming growth factor (TGF)-β signalling is increased in rheumatoid synovium but TGF-β blockade does not modify experimental arthritis. Clin Exp Immunol. 174:245–255. 2013.PubMed/NCBI | |
|
McGovern JL, Nguyen DX, Notley CA, Mauri C, Isenberg DA and Ehrenstein MR: Th17 cells are restrained by Treg cells via the inhibition of interleukin-6 in patients with rheumatoid arthritis responding to anti-tumor necrosis factor antibody therapy. Arthritis Rheum. 64:3129–3138. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Oh SJ and DH Chung DH: Invariant NKT cells producing IL-4 or IL-10, but not IFN-gamma, inhibit the Th1 response in experimental autoimmune encephalomyelitis, whereas none of these cells inhibits the Th17 response. J Immunol. 186:6815–6821. 2011. View Article : Google Scholar : PubMed/NCBI | |
|
Song GG, Bae SC, Kim JH and Lee YH: Interleukin-4, interleukin-4 receptor, and interleukin-18 polymorphisms and rheumatoid arthritis: A meta-analysis. Immunol Invest. 42:455–469. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Finnegan A, Grusby MJ, Kaplan CD, O'Neill SK, Eibel H, Koreny T, Czipri M, Mikecz K and Zhang J: IL-4 and IL-12 regulate proteoglycan-induced arthritis through Stat-dependent mechanisms. J Immunol. 169:3345–3352. 2002. View Article : Google Scholar : PubMed/NCBI | |
|
Cao Y, Brombacher F, Tunyogi-Csapo M, Glant TT and Finnegan A: Interleukin-4 regulates proteoglycan-induced arthritis by specifically suppressing the innate immune response. Arthritis Rheum. 56:861–870. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Kageyama Y, Koide Y, Yoshida A, Uchijima M, Arai T, Miyamoto S, Ozeki T, Hiyoshi M, Kushida K and Inoue T: Reduced susceptibility to collagen-induced arthritis in mice deficient in IFN-gamma receptor. J Immunol. 161:1542–1548. 1998.PubMed/NCBI | |
|
De Klerck B, Carpentier I, Lories RJ, Habraken Y, Piette J, Carmeliet G, Beyaert R, Billiau A and Matthys P: Enhanced osteoclast development in collagen-induced arthritis in interferon-gamma receptor knock-out mice as related to increased splenic CD11b+ myelopoiesis. Arthritis Res Ther. 6:R220–R231. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Joosten LA, Lubberts E, Helsen MM, Saxne T, Coenen-de Roo CJ, Heinegård D and van den Berg WB: Protection against cartilage and bone destruction by systemic interleukin-4 treatment in established murine type II collagen-induced arthritis. Arthritis Res. 1:81–91. 1999. View Article : Google Scholar : PubMed/NCBI | |
|
Heo YJ, Joo YB, Oh HJ, Park MK, Heo YM, Cho ML, Kwok SK, Ju JH, Park KS, Cho SG, et al: IL-10 suppresses Th17 cells and promotes regulatory T cells in the CD4+ T cell population of rheumatoid arthritis patients. Immunol Lett. 127:150–156. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Gu Y, Yang J, Ouyang X, Liu W, Li H, Yang J, Bromberg J, Chen SH, Mayer L, Unkeless JC and Xiong H: Interleukin 10 suppresses Th17 cytokines secreted by macrophages and T cells. Eur J Immunol. 38:1807–1813. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Wang J, Lin R, Zhang W, Li L, Gottstein B, Blagosklonov O, Lü G, Zhang C, Lu X, Vuitton DA and Wen H: Transcriptional profiles of cytokine/chemokine factors of immune cell-homing to the parasitic lesions: A comprehensive one-year course study in the liver of E. PLoS One. 9:e916382014. View Article : Google Scholar : PubMed/NCBI | |
|
Anthony RM, Rutitzky LI, Urban JF Jr, Stadecker MJ and Gause WC: Protective immune mechanisms in helminth infection. Nat Rev Immunol. 7:975–987. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Layland LE, Mages J, Loddenkemper C, Hoerauf A, Wagner H, Lang R and da Costa CU: Pronounced phenotype in activated regulatory T cells during a chronic helminth infection. J Immunol. 184:713–724. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Tuxun T, Wang JH, Lin RY, Shan JY, Tai QW, Li T, Zhang JH, Zhao JM and Wen H: Th17/Treg imbalance in patients with liver cystic echinococcosis. Parasite Immunol. 34:520–527. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Lee DM and Weinblatt ME: Rheumatoid arthritis. Lancet. 358:903–911. 2001. View Article : Google Scholar : PubMed/NCBI | |
|
Carranza F, Falcón CR, Nuñez N, Knubel C, Correa SG, Bianco I, Maccioni M, Fretes R, Triquell MF, Motrán CC and Cervi L: Helminth antigens enable CpG-activated dendritic cells to inhibit the symptoms of collagen-induced arthritis through Foxp3+ regulatory T cells. PLoS One. 7:e403562012. View Article : Google Scholar : PubMed/NCBI | |
|
van Amelsfort JM, van Roon JA, Noordegraaf M, Jacobs KM, Bijlsma JW, Lafeber FP and Taams LS: Proinflammatory mediator-induced reversal of CD4+, CD25+ regulatory T cell-mediated suppression in rheumatoid arthritis. Arthritis Rheum. 56:732–742. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Morgan ME, Flierman R, van Duivenvoorde LM, Witteveen HJ, van Ewijk W, van Laar JM, de Vries RR and Toes RE: Effective treatment of collagen-induced arthritis by adoptive transfer of CD25+ regulatory T cells. Arthritis Rheum. 52:2212–2221. 2005. View Article : Google Scholar : PubMed/NCBI | |
|
Esensten JH, Wofsy D and Bluestone JA: Regulatory T cells as therapeutic targets in rheumatoid arthritis. Nat Rev Rheumatol. 5:560–565. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Yang J, Zhao J, Yang Y, Zhang L, Yang X, Zhu X, Ji M, Sun N and Su C: Schistosoma japonicum egg antigens stimulate CD4 CD25 T cells and modulate airway inflammation in a murine model of asthma. Immunology. 120:8–18. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Mo HM, Liu WQ, Lei JH, Cheng YL, Wang CZ and Li YL: Schistosoma japonicum eggs modulate the activity of CD4+ CD25+ Tregs and prevent development of colitis in mice. Exp Parasitol. 116:385–389. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Jankovic D, Kullberg MC, Caspar P and Sher A: Parasite-induced Th2 polarization is associated with down-regulated dendritic cell responsiveness to Th1 stimuli and a transient delay in T lymphocyte cycling. J Immunol. 173:2419–2427. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Cervi L, MacDonald AS, Kane C, Dzierszinski F and Pearce EJ: Cutting edge: Dendritic cells copulsed with microbial and helminth antigens undergo modified maturation, segregate the antigens to distinct intracellular compartments and concurrently induce microbe-specific Th1 and helminth-specific Th2 responses. J Immunol. 172:2016–1020. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Zhang L, Fu J, Sheng K, Li Y, Song S, Li P, Song S, Wang Q, Chen J, Yu J and Wei W: Bone marrow CD11b (+)F4/80 (+) dendritic cells ameliorate collagen-induced arthritis through modulating the balance between Treg and Th17. Int Immunopharmacol. 25:96–105. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Saei A and Hadjati J: Tolerogenic dendritic cells: Key regulators of peripheral tolerance in health and disease. Int Arch Allergy Immunol. 161:293–303. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Stoop JN, Harry RA, von Delwig A, Isaacs JD, Robinson JH and Hilkens CM: Therapeutic effect of tolerogenic dendritic cells in established collagen-induced arthritis is associated with a reduction in Th17 responses. Arthritis Rheum. 62:3656–3665. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Torres-Aguilar H, Aguilar-Ruiz SR, González-Pérez G, Munguía R, Bajaña S, Meraz-Ríos MA and Sánchez-Torres C: Tolerogenic dendritic cells generated with different immunosuppressive cytokines induce antigen-specific anergy and regulatory properties in memory CD4+ T cells. J Immunol. 184:1765–1775. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Falcón C, Carranza F, Martínez FF, Knubel CP, Masih DT, Motrán CC and Cervi L: Excretory-secretory products (ESP) from Fasciola hepatica induce tolerogenic properties in myeloid dendritic cells. Vet Immunol Immunopathol. 137:36–46. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Falcón CR, Carranza FA, Aoki P, Motrán CC and Cervi L: Adoptive transfer of dendritic cells pulsed with Fasciola hepatica antigens and lipopolysaccharides confers protection against fasciolosis in mice. J Infect Dis. 205:506–514. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Harnett W and Harnett MM: Helminth-derived immunomodulators: Can understanding the worm produce the pill? Nat Rev Immunol. 10:278–284. 2010. View Article : Google Scholar : PubMed/NCBI |
