Therapeutic strategies for rheumatoid arthritis: towards biotechnological therapies

Authors

  • Ángel Fernando Cisneros Caballero
  • María José Felgueres Planells
  • Elisa Vela Jarquín
  • Diana Gómez Martín

Keywords:

Rheumatoid arthritis, inflammatory process, therapeutic targets, biotechnological therapies

Abstract

Rheumatoid arthritis (RA) is a multigenic autoimmune disease characterized by the chronic

inflammation of the joints due to the hyperplasia of the synovium. This process creates a

conglomerate of immune cells capable of secreting proinflammatory cytokines that contribute

to the surrounding bone and cartilage destruction. Patients who suffer from this disease develop

symptoms such as constant pain, functional disability, fatigue, and depression. Specifically, RA

affects the synovial joints (also called diarthrodial joints), which connect bones with a large

range of movement. Since it is one of the main causes of incapacitation for carrying out daily

tasks, RA represents, as a consequence, a severe public health problem. It has a worldwide

prevalence between 0.3 and 1% and affects mainly the productive age group. Up to this day,

there is still no cure for RA, and current treatments are partially effective in slowing down the disease’s progression and alleviating the symptoms. This review article summarizes the RA’s physiopathology, particularly focusing on pro-inflammatory cytokines responsible for the disease’s onset and prognosis, as they have been used as a common therapeutic target in RA. Furthermore, this review also describes the latest biotechnological therapeutic approaches, focusing on both the research and development of genetic and biological therapies, being antibodies the most important, in order to go further beyond the palliative care and straight into more efficient anti-RA treatment.

References

Barrera-Cruz A, Beltrán Castillo D, Blanco-Favela D, Flores-Aguilar D, Jara-Quezada D, Neri-Gómez, D et al. Diagnóstico y tratamiento de artritis reumatoide del adulto. Sistema Nacional de Salud. México: Gobierno Federal; 2010.

Traister R, Hirsch R. Gene therapy for arthritis. Mod Rheumatol. 2008; 18 (1): 2-14.

WHO. Chronic rheumatic conditions. World Health Organization; 2015. [Recuperado el 20 de noviembre de 2015]. Disponible en: http: //www.who.int/chp/topics/ rheumatic/en/

Secretaría de Salud. Diagnóstico y tratamiento de artritis reumatoide del adulto. CENETEC, Gobierno Federal; 2010. [Recuperado el 25 de febrero de 2017]. Disponible en: http://www.cenetec.salud.gob.mx/descargas/gpc/ CatalogoMaestro/195_ARTRITIS_REUMATOIDE/ Artritis_reumatoidE_EVR_CENETEC.pdf

Vandever L. Rheumatoid arthritis by the numbers: facts, statistics, and you. Healthline; 2014. [Recuperado el 20 de noviembre de 2015]. Disponible en: http: // www.healthline.com/health/rheumatoid-arthritis/facts- statistics-infographic

Cardiel MH, Díaz-Borjón A, Vázquez del Mercado Espinosa M, Gámez-Nava JI, Barile-Fabris LA, Pacheco-Tena C et al. Actualización de la Guía mexicana para el tratamiento farmacológico de la artritis reumatoide del Colegio Mexicano de Reumatología. Reumatol Clin. 2013; 10 (4): 227-240.

Smolen J, Steiner G. Therapeutic strategies for rheumatoid

arthritis. Nat Rev Drug Discov. 2003; 2 (6): 473-488.

Belmonte-Serrano MA. ¿Es la puntuación DAS28 el

métodomásadecuadoparaestimarlaactividaddelaartritis

reumatoide? Consideraciones clinimétricas y escenarios de

simulación. Reumatol Clin. 2008; 4 (5): 183-190.

American College of Rheumatology, Clinical Disease Activity Index (CDAI). (s. f.). American College of Rheumatology [Recuperado el 19 de septiembre de 2016]. Disponible en: http://www.rheumatology.org/Learning- Center/Glossary/ArticleType/ArticleView/ArticleID/423

McInnes IB, Schett G. Cytokines in the pathogenesis of rheumatoid arthritis. Nat Rev Immunol. 2007; 7 (6): 429-442.

Ranganath VK, Khanna D, Paulus HE. ACR remission criteria and response criteria. Clin Exp Rheumatol. 2006; 24 (6 Suppl. 43): S14-S21.

Choy E. Understanding the dynamics: pathways involved in the pathogenesis of rheumatoid arthritis. Rheumatology (Oxford). 2012; 51 Suppl 5: v3-v11.

Smolen JS, Aletaha D, Koeller M, Weisman MH, Emery P. New therapies for treatment of rheumatoid arthritis. Lancet. 2007; 370 (9602): 1861-1874.

López-Lasanta M, Julià A, Maymó J, Fernández- Gutiérrez B, Ureña-Garnica I, Blanco FJ et al. Variation at interleukin-6 receptor gene is associated to joint damage in rheumatoid arthritis. Arthritis Res Ther. 2015; 17: 242.

Suzuki A, Kochi Y, Okada Y, Yamamoto K. Insight from genome-wide association studies in rheumatoid arthritis and multiple sclerosis. FEBS Lett. 2011; 585 (23): 3627-3632.

Nakajima A. Application of cellular gene therapy for rheumatoid arthritis. Mod Rheumatol. 2006; 16 (5): 269-275.

Sánchez-Ramón S, López-Longo FJ, Carreño L. Interleucinas en la fisiopatología de la artritis reumatoide: más allá de las citocinas proinflamatorias. Reumatol Clin. 2011; 6 (S3): S20-S24.

Al-Saeed A. Gastrointestinal and cardiovascular risk of nonsteroidal anti-inflammatory drugs. Oman Med J. 2011; 26 (6): 385-391.

Wienecke T, Gøtzsche PC. Paracetamol versus nonsteroidal anti-inflammatory drugs for rheumatoid arthritis. Cochrane Database Syst Rev. 2004; (1): CD003789.

Guzmán R, Restrepo J. Artritis reumatoide temprana. Rev Colomb Reumatol. 2002; 9 (3): 171-175.

Wilkie WS, Schwieterman P. Strategies for the management of rheumatoid arthritis. Orthopedics. 2012; 35 (2): 125-130.

Tian H, Cronstein BN. Understanding the mechanisms of action of methotrexate: implications for the treatment of rheumatoid arthritis. Bull NYU Hosp Jt Dis. 2007; 65 (3): 168-173.

Hernandez-Baldizon S. ¿Cómo hacer buen uso del metotrexato en artritis reumatoide? Reumatol Clin. 2012; 8 (1): 42-45.

Provenzano G. Chronic pulmonary toxicity of methotrexate and rheumatoid arthritis. Rheumatology (Oxford). 2003; 42 (6): 802-803; author reply 803-804.

Roubille C, Haraoui B. Interstitial lung diseases induced or exacerbated by DMARDs and biologic agents in rheumatoid arthritis: a systematic literature review.

Semin Arthritis Rheum. 2014; 43 (5): 613-626.

Dawson JK, Graham DR, Desmond J, Fewins HE, Lynch MP. Investigation of the chronic pulmonary effects of low-dose oral methotrexate in patients with rheumatoid arthritis: a prospective study incorporating HRCT scanning and pulmonary function tests. Rheumatology (Oxford). 2002; 41 (3): 262-267.

Buchbinder R, Barber M, Heuzenroeder L, Wluka AE, Giles G, Hall S et al. Incidence of melanoma and other

malignancies among rheumatoid arthritis patients treated with methotrexate. Arthritis Rheum. 2008; 59 (6): 794-799.

Osuga T, Ikura Y, Kadota C, Hirano S, Iwai Y, Hayakumo T. Significance of liver biopsy for the evaluation of methotrexate-induced liver damage in patients with rheumatoid arthritis. Int J Clin Exp Pathol. 2015; 8 (2): 1961-1966.

McCurry J. Japan deaths spark concerns over arthritis drug. Lancet. 2004; 363 (9407): 461.

Sakai F, Noma S, Kurihara Y, Yamada H, Azuma A, Kudoh S et al. Leflunomide-related lung injury in patients with rheumatoid arthritis: imaging features. Mod Rheumatol. 2005; 15 (3): 173-179.

Suissa S, Hudson M, Ernst P. Leflunomide use and the risk of interstitial lung disease in rheumatoid arthritis. Arthritis Rheum. 2006; 54 (5): 1435-1439.

Levine SJ. Mechanisms of soluble cytokine receptor generation. J Immunol. 2004; 173 (9): 5343-5348.

HuS,LiangS,GuoH,ZhangD,LiH,WangXet al. Comparison of the inhibition mechanisms of adalimumab and infliximab in treating tumor necrosis factor α-associated diseases from a molecular view. J Biol Chem. 2013; 288 (38): 27059-27067.

Llord de la Mata J, González-Crespo R, Maese-Manzano J. Tratamiento de la artritis reumatoide con anakinra: revisión sistemática. Reumatol Clin. 2007; 3 (4): 153-158.

Van Vollenhoven RF. Treatment of rheumatoid arthritis: state of the art 2009. Nat Rev Rheumatol. 2009; 5 (10): 531-541.

Yilmaz-Elis S, Aartsma-Rus A, Vroon A, van Deutekom J, de Kimpe S, ‘t Hoen PA et al. Antisense oligonucleotide mediated exon skipping as a potential strategy for the treatment of a variety of inflammatory diseases such as rheumatoid arthritis. Ann Rheum Dis. 2012; 71 Suppl 2: i75-i77.

Jefferis R, Lefranc MP. Human immunoglobulin allotypes: possible implications for immunogenicity. MAbs. 2009; 1 (4): 332-338.

Fischer JA, Hueber AJ, Wilson S, Galm M, Baum W, Kitson C et al. Combined inhibition of tumor necrosis factor α and interleukin-17 as a therapeutic opportunity in rheumatoid arthritis: development and characterization of a novel bispecific antibody. Arthritis Rheumatol. 2015; 67 (1): 51-62.

Robbins PD, Evans CH, Chernajovsky Y. Gene therapy for arthritis. Gene Ther. 2003; 10 (10): 902-911.

Evans CH, Robbins PD, Ghivizzani SC, Wasko MC, Tomaino MM, Kang R et al. Gene transfer to human

joints: progress toward a gene therapy of arthritis. Proc

Natl Acad Sci U S A. 2005; 102 (24): 8698-8703.

Apparailly F, Jorgensen C. siRNA-based therapeutic approaches for rheumatic diseases. Nat Rev Rheumatol.

; 9 (1): 56-62.

Lee SJ, Lee A, Hwang SR, Park JS, Jang J, Huh MS

et al. TNF-α gene silencing using polymerized siRNA/ thiolated glycol chitosan nanoparticles for rheumatoid arthritis. Mol Ther. 2014; 22 (2): 397-408.

Nehoff H, Parayath NN, Domanovitch L, Taurin S, Greish K. Nanomedicine for drug targeting: strategies beyond the enhanced permeability and retention effect. Int J Nanomedicine. 2014; 9: 2539-2555.

Aartsma-Rus A, van Ommen GJ. Antisense-mediated exon skipping: a versatile tool with therapeutic and research applications. RNA. 2007; 13 (10): 1609-1624.

Jing W, Zhang X, Sun W, Hou X, Yao Z, Zhu Y. CRISPR/ CAS9-mediated genome editing of miRNA-155 inhibits proinflammatory cytokine production by RAW264.7 cells. Biomed Res Int. 2015; 2015: 326042.

Li YT, Chen SY, Wang CR, Liu MF, Lin CC, Jou IM et al. Brief report: amelioration of collagen-induced arthritis in mice by lentivirus-mediated silencing of microRNA-223. Arthritis Rheum. 2012; 64 (10): 3240-3245.

Xue Y, Yang Y, Su Z, Barnie PA, Zheng D, Zhang Y et al. Local delivery of T-bet shRNA reduces inflammation in collagen II-induced arthritis via downregulation of IFN-γ and IL-17. Mol Med Rep. 2014; 9 (3): 899-903.

Liu S, Kiyoi T, Takemasa E, Maeyama K. Systemic lentivirus-mediated delivery of short hairpin RNA targeting calcium release-activated calcium channel 3 as gene therapy for collagen-induced arthritis. J Immunol. 2015; 194 (1): 76-83.

Weizmann Institute of Science. PLAU Gene (Protein Coding) Plasminogen Activator, Urokinase. GeneCards; 2015 [Recuperado el 26 de noviembre de 2015]. Disponible en: http://www.genecards.org/cgi-bin/ carddisp.pl?gene=PLAU

Jin T, Tarkowski A, Carmeliet P, Bokarewa M. Urokinase, a constitutive component of the inflamed synovial fluid, induces arthritis. Arthritis Res Ther. 2003; 5 (1): R9-R17.

Serratì S, Margheri F, Chillà A, Neumann E, Müller- Ladner U, Benucci M et al. Reduction of in vitro invasion and in vivo cartilage degradation in a SCID mouse model by loss of function of the fibrinolytic system of rheumatoid arthritis synovial fibroblasts. Arthritis Rheum. 2011; 63 (9): 2584-2594.

Smith HW, Marshall CJ. Regulation of cell signalling by uPAR. Nat Rev Mol Cell Biol. 2010; 11 (1): 23-36.

Pap T, Müller-Ladner U, Gay RE, Gay S. Fibroblast

biology. Role of synovial fibroblasts in the pathogenesis

of rheumatoid arthritis. Arthritis Res. 2000; 2 (5): 361-367. 54. Naranjos-Ramírez N, Torres-Cantú D, Castillo- Rodríguez V, Galindo-Rodríguez G, Chávez-Montes A, Castro-Ríos R et al. Preparación de nanopartículas poliméricas con aplicación farmacéutica usando técnicas basadas en emulsificación. Revista Mexicana

de Física. 2011; 57 (2): 41-43.

Reilly JF, Mizukoshi E, Maher PA. Ligand dependent and independent internalization and nuclear translocation of fibroblast growth factor (FGF) receptor 1. DNA Cell Biol. 2004; 23 (9): 538-548.

Dolati S, Sadreddini S, Rostamzadeh D, Ahmadi M, Jadidi-Niaragh F, Yousefi M. Utilization of nanoparticle technology in rheumatoid arthritis treatment. Biomed

Pharmacother. 2016; 80: 30-41.

Kim MJ, Park JS, Lee SJ, Jang J, Park JS, Back SH et al. Notch1 targeting siRNA delivery nanoparticles for rheumatoid arthritis therapy. J Control Release. 2015; 216: 140-148.

Son S, Song S, Lee SJ, Min S, Kim SA, Yhee JY et al. Self-crosslinked human serum albumin nanocarriers for systemic delivery of polymerized siRNA to tumors. Biomaterials. 2013; 34 (37): 9475-9485.

Peng SF, Tseng MT, Ho YC, Wei MC, Liao ZX, Sung HW. Mechanisms of cellular uptake and intracellular trafficking with chitosan/DNA/poly(γ-glutamic acid) complexes as a gene delivery vector. Biomaterials. 2011; 32 (1): 239-248.

Arend WP, Guthridge CJ. Biological role of interleukin 1 receptor antagonist isoforms. Ann Rheum Dis. 2000; 59 Suppl. 1: i60-i64.

Gabay C, Arend WP. Treatment of rheumatoid arthritis with IL-1 inhibitors. Springer Semin Immunopathol. 1998; 20 (1-2): 229-246.

Kanangat S, Postlethwaite AE, Higgins GC, Hasty KA. Novel functions of intracellular IL-1ra in human dermal fibroblasts: implications in the pathogenesis of fibrosis. J Invest Dermatol. 2006; 126 (4): 756-765.

Sims JE, Smith DE. The IL-1 family: regulators of immunity. Nat Rev Immunol. 2010; 10 (2): 89-102.

Taylor SL, Renshaw BR, Garka KE, Smith DE, Sims JE. Genomic organization of the interleukin-1 locus. Genomics. 2002; 79 (5): 726-733.

Srirangan S, Choy EH. The role of interleukin 6 in the pathophysiology of rheumatoid arthritis. Ther Adv Musculoskelet Dis. 2010; 2 (5): 247-256.

Flores-García Y, Talamás-Rohana P. Interleucina 17, funciones biológicas y su receptor. Rev Educ Bioquímica. 2012; 31 (1): 3-9.

Iwakura Y, Ishigame H, Saijo S, Nakae S. Functional specialization of interleukin-17 family members. Immunity. 2011; 34 (2): 149-162.

McInnes IB, Liew FY, Gracie JA. Interleukin-18: a therapeutic target in rheumatoid arthritis? Arthritis Res Ther. 2005; 7 (1): 38-41.

Nolan KF, Greaves DR, Waldmann H. The human interleukin 18 gene IL18 maps to 11q22.2-q22.3, closely linked to the DRD2 gene locus and distinct from mapped IDDM loci. Genomics. 1998; 51 (1): 161-163.

Faragó B, Magyari L, Sáfrány E, Csöngei V, Járomi L, Horvatovich K et al. Functional variants of interleukin-23 receptor gene confer risk for rheumatoid arthritis but not for systemic sclerosis. Ann Rheum Dis. 2008; 67 (2): 248-250.

Orozco G, Rueda B, Robledo G, García A, Martín J.

Investigation of the IL23R gene in a Spanish rheumatoid

arthritis cohort. Hum Immunol. 2007; 68 (8): 681-684.

Park JH, Kim YJ, Park BL, Bae JS, Shin HD, Bae SC. Lack of association between interleukin 23 receptor gene polymorphisms and rheumatoid arthritis

susceptibility. Rheumatol Int. 2009; 29 (7): 781-786.

Rong C, Hu W, Wu FR, Cao XJ, Chen FH. Interleukin-23 as a potential therapeutic target for rheumatoid arthritis.

Mol Cell Biochem. 2012; 361 (1-2): 243-248.

Eken A, Singh A, Oukka M. Interleukin 23. In: Encyclopedia of inflammatory diseases. Basel, Suiza: Springer Basel; 2015. pp. 1-10.

Gong F, Pan YH, Huang X, Chen J, Xiao JH, Zhu HY. Interleukin-27 as a potential therapeutic target for rheumatoid arthritis: has the time come? Clin Rheumatol. 2013; 32 (10): 1425-1428.

Pickens SR, Chamberlain ND, Volin MV, Mandelin AM 2nd, Agrawal H, Matsui M et al. Local expression of interleukin-27 ameliorates collagen-induced arthritis. Arthritis Rheum. 2011; 63 (8): 2289-2298.

Bosmann M, Ward PA. Modulation of inflammation by interleukin-27. J Leukoc Biol. 2013; 94 (6): 1159-1165. 78. Heinhuis B, Koenders MI, van de Loo FA, Netea MG, van den Berg WB, Joosten LA. Inflammation-dependent secretion and splicing of IL-32{gamma} in rheumatoid arthritis. Proc

Natl Acad Sci U S A. 2011; 108 (12): 4962-4967.

Kang JW, Park YS, Lee DH, Kim MS, Bak Y, Ham SY et al. Interaction network mapping among IL-32 isoforms.

Biochimie. 2014; 101: 248-251.

Khawar B, Abbasi MH, Sheikh N. A panoramic spectrum

of complex interplay between the immune system and IL-32 during pathogenesis of various systemic infections and inflammation. Eur J Med Res. 2015; 20: 7.

Kim S. Interleukin-32 in inflammatory autoimmune diseases. Immune Netw. 2014; 14 (3): 123-127.

Ning X, Jian Z, Wang W. Low serum levels of interleukin 35 in patients with rheumatoid arthritis. Tohoku J Exp Med. 2015; 237 (2): 77-82.

Šenolt L, Šumová B, Jandová R, Hulejová H, Mann H, Pavelka K et al. Interleukin 35 synovial fluid levels are associated with disease activity of rheumatoid arthritis. PLoS One. 2015; 10 (7): e0132674.

Posadas-Sánchez R, Pérez-Hernández N, Ángeles- Martínez J, López-Bautista F, Villarreal-Molina T, Rodríguez-Pérez J et al. Interleukin 35 polymorphisms are associated with decreased risk of premature coronary artery disease, metabolic parameters, and IL-35 levels: the genetics of atherosclerotic disease (GEA) study. Mediators of Inflammation. 2017; 2017: ID 6012795.

Atzeni F, Sarzi-Puttini P, Botsios C, Carletto A, Cipriani P, Favalli EG et al. Long-term anti-TNF therapy and the risk of serious infections in a cohort of patients with rheumatoid arthritis: comparison of adalimumab, etanercept and infliximab in the GISEA registry. Autoimmun Rev. 2012; 12 (2): 225-229.

Bradley JR. TNF-mediated inflammatory disease. J Pathol. 2008; 214 (2): 149-160.

Marenco de la Fuente J, Solís-Díaz R. Antagonistas del

TNF. Nuevos datos de eficacia. Reumatol Clin. 2009;

Supl 1: 71-76.

Nie H, Zheng Y, Li R, Guo TB, He D, Fang L et al. Phosphorylation of FOXP3 controls regulatory T cell function and is inhibited by TNFα in rheumatoid arthritis. Nat Med. 2013; 19 (3): 322-328.

Rego-Pérez I, Fernández-Moreno M, Blanco FJ. Gene polymorphisms and pharmacogenetics in rheumatoid arthritis. Curr Genomics. 2008; 9 (6): 381-393.

Park JS, Kwok SK, Lim MA, Oh HJ, Kim EK, Jhun JY et al. TWEAK promotes osteoclastogenesis in rheumatoid arthritis. Am J Pathol. 2013; 183 (3): 857-867.

Bhattacharjee M, Raju R, Radhakrishnan A, Nanjappa V, Muthusamy B, Singh K et al. A bioinformatics resource for TWEAK-Fn14 signaling pathway. J Signal Transduct. 2012; 2012: 376470.

Dillon SR, Gross JA, Ansell SM, Novak AJ. An APRIL to remember: novel TNF ligands as therapeutic targets. Nat Rev Drug Discov. 2006; 5 (3): 235-246.

Moore PA, Belvedere O, Orr A, Pieri K, LaFleur DW, Feng P et al. BLyS: member of the tumor necrosis factor family and B lymphocyte stimulator. Science. 1999; 285 (5425): 260-263.

Gorth DJ, Mauck RL, Chiaro JA, Mohanraj B, Hebela NM, Dodge GR et al. IL-1ra delivered from poly(lactic- co-glycolic acid) microspheres attenuates IL-1β- mediated degradation of nucleus pulposus in vitro. Arthritis Res Ther. 2012; 14 (4): R179.

Cohen SB, Moreland LW, Cush JJ, Greenwald MW, Block S, Shergy WJ et al. A multicentre, double blind, randomised, placebo controlled trial of anakinra (Kineret), a recombinant interleukin 1 receptor antagonist, in patients with rheumatoid arthritis treated with background methotrexate. Ann Rheum Dis. 2004; 63 (9): 1062-1068.

Maini RN, Taylor PC, Szechinski J, Pavelka K, Bröll J, Balint G et al. Double-blind randomized controlled clinical trial of the interleukin-6 receptor antagonist, tocilizumab, in European patients with rheumatoid arthritis who had an incomplete response to methotrexate. Arthritis Rheum. 2006; 54 (9): 2817-2829.

Mease P, Strand V, Shalamberidze L, Dimic A, Raskina T, Xu LA et al. A phase II, double-blind, randomised, placebo- controlled study of BMS945429 (ALD518) in patients with rheumatoid arthritis with an inadequate response to methotrexate. Ann Rheum Dis. 2012; 71 (7): 1183-1189.

Kellner H. Targeting interleukin-17 in patients with active rheumatoid arthritis: rationale and clinical potential. Ther Adv Musculoskelet Dis. 2013; 5 (3): 141-152.

Genovese MC, Durez P, Richards HB, Supronik J, Dokoupilova E, Mazurov V et al. Efficacy and safety of secukinumab in patients with rheumatoid arthritis: a phase II, dose-finding, double-blind, randomised, placebo controlled study. Ann Rheum Dis. 2013; 72 (6): 863-869.

Genovese MC, Greenwald M, Cho CS, Berman A, Jin L, Cameron GS et al. A phase 2 study of multiple subcutaneous doses of LY2439821, an anti-IL-17

monoclonal antibody, in patients with rheumatoid arthritis

in two populations: nave to biologic therapy inadequate

responders to tumor necrosis factor alpha inhibitors.

Arthritis Rheumatism. 2011; 63 (Supl. 10): 2591.

Pavelka K, Chon Y, Newmark R, Erondu N, Lin S. A randomized, double-blind, placebo-controlled, multiple- dose study to evaluate the safety, tolerability, and efficacy of brodalumab (AMG 827) in subjects with rheumatoid arthritis and an inadequate response to methotrexate.

Arthritis & Rheumatology. 2012; 64 (Supl. 10): 831.

Plater-Zyberk C, Joosten LA, Helsen MM, Sattonnet- Roche P, Siegfried C, Alouani S et al. Therapeutic effect of neutralizing endogenous IL-18 activity in the collagen-induced model of arthritis. J Clin Invest. 2001; 108 (12): 1825-1832.

Qian X, Ning H, Zhang J, Hoft DF, Stumpo DJ, Blackshear PJ et al. Posttranscriptional regulation of IL-23 expression by IFN-gamma through tristetraprolin. J Immunol. 2011; 186 (11): 6454-6464.

Al-Salleeh F, Petro TM. Promoter analysis reveals critical roles for SMAD-3 and ATF-2 in expression of IL-23 p19 in macrophages. J Immunol. 2008; 181 (7): 4523-4533.

Niedbala W, Cai B, Wei X, Patakas A, Leung BP, McInnes IB et al. Interleukin 27 attenuates collagen-induced arthritis. Ann Rheum Dis. 2008; 67 (10): 1474-1479.

Heinhuis B, Koenders MI, van Riel PL, van de Loo FA, Dinarello CA, Netea MG et al. Tumour necrosis factor alpha-driven IL-32 expression in rheumatoid arthritis synovial tissue amplifies an inflammatory cascade. Ann Rheum Dis. 2011; 70 (4): 660-667.

Thiolat A, Denys A, Petit M, Biton J, Lemeiter D, Herve R et al. Interleukin-35 gene therapy exacerbates experimental rheumatoid arthritis in mice. Cytokine. 2014; 69 (1): 87-93.

Kochetkova I, Golden S, Holderness K, Callis G, Pascual DW. IL-35 stimulation of CD39+ regulatory T cells confers protection against collagen II-induced arthritis via the production of IL-10. J Immunol. 2010; 184 (12): 7144-7153.

Wisniacki N, Amaravadi L, Galluppi GR, Zheng TS, Zhang R, Kong J et al. Safety, tolerability, pharmacokinetics, and pharmacodynamics of anti-TWEAK monoclonal antibody in patients with rheumatoid arthritis. Clin Ther. 2013; 35 (8): 1137-1149.

Tak PP, Thurlings RM, Rossier C, Nestorov I, Dimic A, Mircetic V et al. Atacicept in patients with rheumatoid arthritis: results of a multicenter, phase Ib, double-blind, placebo-controlled, dose-escalating, single- and repeated- dose study. Arthritis Rheum. 2008; 58 (1): 61-72.

Qandil AM. Prodrugs of nonsteroidal anti-inflammatory drugs (NSAIDs), more than meets the eye: a critical review. Int J Mol Sci. 2012; 13 (12): 17244-17274.

Crofford LJ. Use of NSAIDs in treating patients with arthritis. Arthritis Res Ther. 2013; 15 Supl. 3: S2.

Wishart DS, Knox C, Guo AC, Shrivastava S, Hassanali

M, Stothard P et al. DrugBank: a comprehensive resource for in silico drug discovery and exploration. Nucleic Acids Res. 2006; 34 (Database issue): D668-D672.

Pawade R, Bhaterao P, Kunkulol R, Kute N. Disease-

modifying anti-rheumatic drugs (DMARDs) used for

rheumatoid arthritis —a review. Indian Journal of Basic and Applied Medical Research. 2015; 4 (3): 272-288.

Equipo de Redacción de IQB [23 de diciembre de 2010]. Aurotioglucosa. Instituto Químico Biológico [Recuperado el 26 de noviembre de 2015]. Disponible en: http://www. iqb.es/cbasicas/farma/farma04/a074.htm

Arthritis. Nature Biotechnology. 2000; 18: IT12-IT14.

Published

2024-08-19

How to Cite

1.
Cisneros Caballero Ángel F, Felgueres Planells MJ, Vela Jarquín E, Gómez Martín D. Therapeutic strategies for rheumatoid arthritis: towards biotechnological therapies. InDiscap [Internet]. 2024 Aug. 19 [cited 2024 Sep. 19];6(2):69-87. Available from: https://dsm.inr.gob.mx/indiscap/index.php/INDISCAP/article/view/333

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Evidence synthesis and meta-research

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