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Review

S100-alarmins: potential therapeutic targets for arthritis

, &
Pages 738-750 | Received 01 Feb 2017, Accepted 10 May 2017, Published online: 25 May 2017

References

  • Foell D, Wittkowski H, Roth J. Mechanisms of disease: a ‘DAMP’ view of inflammatory arthritis. Nat Clin Pract Rheumatol. 2007;3:382–390.
  • Smolen JS, Breedveld FC, Burmester GR, et al. Treating rheumatoid arthritis to target: 2014 update of the recommendations of an international task force. Ann Rheum Dis. 2016;75:3–15.
  • Crofford LJ. Use of NSAIDs in treating patients with arthritis. Arthritis Res Ther. 2013;15;suppl.3:2.
  • Quan LD, Thiele GM, Tian J, et al. The development of novel therapies for rheumatoid arthritis. Expert Opin Ther Pat. 2008;18:723–738.
  • Curtis JR, Singh JA. Use of biologics in rheumatoid arthritis: current and emerging paradigms of care. Clin Ther. 2011;33:679–707.
  • Smolen JS, Landewe R, Breedveld FC, et al. EULAR recommendations for the management of rheumatoid arthritis with synthetic and biological disease-modifying antirheumatic drugs: 2013 update. Ann Rheum Dis. 2014;73:492–509.
  • Yamaoka K. Janus kinase inhibitors for rheumatoid arthritis. Curr Opin Chem Biol. 2016;32:29–33.
  • Shammas RM, Ranganath VK, Paulus HE. Remission in rheumatoid arthritis. Curr Rheumatol Rep. 2010;12:355–362.
  • Singh JA, Cameron C, Noorbaloochi S, et al. Risk of serious infection in biological treatment of patients with rheumatoid arthritis: a systematic review and meta-analysis. Lancet. 2015;386:258–265.
  • Medzhitov R, Ca J Jr. Decoding the patterns of self and nonself by the innate immune system. Science. 2002;296:298–300.
  • Ehrchen JM, Sunderkotter C, Foell D, et al. The endogenous toll-like receptor 4 agonist S100A8/S100A9 (calprotectin) as innate amplifier of infection, autoimmunity, and cancer. J Leukoc Biol. 2009;86:557–566.
  • Bianchi ME. DAMPs, PAMPs and alarmins: all we need to know about danger. J Leukoc Biol. 2007;81:1–5.
  • Bertheloot D, Latz E. HMGB1, IL-1alpha, IL-33 and S100 proteins: dual-function alarmins. Cell Mol Immunol. 2016;14:43–64.
  • Van Eden W, Spiering R, Broere F, et al. A case of mistaken identity: HSPs are no DAMPs but DAMPERs. Cell Stress Chaperones. 2012;17:281–292.
  • Varga G, Gattorno M, Foell D, et al. Redox distress and genetic defects conspire in systemic autoinflammatory diseases. Nat Rev Rheumatol. 2015;11:670–680.
  • Killeen ME, Ferris L, Kupetsky EA, et al. Signaling through purinergic receptors for ATP induces human cutaneous innate and adaptive Th17 responses: implications in the pathogenesis of psoriasis. J Immunol. 2013;190:4324–4336.
  • Leadbetter EA, Rifkin IR, Hohlbaum AM, et al. Chromatin-IgG complexes activate B cells by dual engagement of IgM and toll-like receptors. Nature. 2002;416:603–607.
  • Przybysz M, Borysewicz K, Katnik-Prastowska I. Fibronectin molecular status determination useful to differentiate between rheumatoid arthritis and systemic lupus erythematosus patients. Rheumatol Int. 2013;33:37–43.
  • Andersson U, Harris HE. The role of HMGB1 in the pathogenesis of rheumatic disease. Biochim Biophys Acta. 2010;1799:141–148.
  • Jia H, Halilou AI, Hu L, et al. Heat shock protein 10 (Hsp10) in immune-related diseases: one coin, two sides. Int J Biochem Mol Biol. 2011;2:47–57.
  • Srivastava P. Roles of heat-shock proteins in innate and adaptive immunity. Nat Rev Immunol. 2002;2:185–194.
  • Tukaj S, Kotlarz A, Jozwik A, et al. Hsp40 proteins modulate humoral and cellular immune response in rheumatoid arthritis patients. Cell Stress Chaperones. 2010;15:555–566.
  • Vercoulen Y, Van Teijlingen NH, De Kleer IM, et al. Heat shock protein 60 reactive T cells in juvenile idiopathic arthritis: what is new? Arthritis Res Ther. 2009;11:231.
  • Liang J, Jiang D, Noble PW. Hyaluronan as a therapeutic target in human diseases. Adv Drug Deliv Rev. 2016;97:186–203.
  • Zhang Q, Raoof M, Chen Y, et al. Circulating mitochondrial DAMPs cause inflammatory responses to injury. Nature. 2010;464:104–107.
  • Martin NT, Martin MU. Interleukin 33 is a guardian of barriers and a local alarmin. Nat Immunol. 2016;17:122–131.
  • Liew FY. IL-33: a janus cytokine. Ann Rheum Dis. 2012;71:i101–4.
  • Fassl SK, Austermann J, Papantonopoulou O, et al. Transcriptome assessment reveals a dominant role for TLR4 in the activation of human monocytes by the alarmin MRP8. J Immunol. 2015;194:575–583.
  • Pruenster M, Vogl T, Roth J, et al. S100A8/A9: from basic science to clinical application. Pharmacol Ther. 2016;167:120–131.
  • Foell D, Wittkowski H, Vogl T, et al. S100 proteins expressed in phagocytes: a novel group of damage-associated molecular pattern molecules. J Leukoc Biol. 2007;81:28–37.
  • Busso N, So A. Mechanisms of inflammation in gout. Arthritis Res Ther. 2010;12:206.
  • So A, Busso N. The concept of the inflammasome and its rheumatologic implications. Joint Bone Spine. 2014;81:398–402.
  • Tsan MF, Gao B. Cytokine function of heat shock proteins. Am J Physiol Cell Physiol. 2004;286:C739–44.
  • Oppenheim JJ, Yang D. Alarmins: chemotactic activators of immune responses. Curr Opin Immunol. 2005;17:359–365.
  • Nefla M, Holzinger D, Berenbaum F, et al. The danger from within: alarmins in arthritis. Nat Rev Rheumatol. 2016;12:669–683.
  • Lavric M, Miranda-Garcia MA, Holzinger D, et al. Alarmins firing arthritis: helpful diagnostic tools and promising therapeutic targets. Joint Bone Spine. 2016;84:101–110.
  • Moore BW. A soluble protein characteristic of the nervous system. Biochem Biophys Res Commun. 1965;19:739–744.
  • Santamaria-Kisiel L, Rintala-Dempsey AC, Shaw GS. Calcium-dependent and -independent interactions of the S100 protein family. Biochem J. 2006;396:201–214.
  • Donato R, Cannon BR, Sorci G, et al. Functions of S100 proteins. Curr Mol Med. 2013;13:24–57.
  • Gross SR, Sin CG, Barraclough R, et al. Joining S100 proteins and migration: for better or for worse, in sickness and in health. Cell Mol Life Sci. 2014;71:1551–1579.
  • Chan JK, Roth J, Oppenheim JJ, et al. Alarmins: awaiting a clinical response. J Clin Invest. 2012;122:2711–2719.
  • Marenholz I, Heizmann CW, Fritz G. S100 proteins in mouse and man: from evolution to function and pathology (including an update of the nomenclature). Biochem Biophys Res Commun. 2004;322:1111–1122.
  • Roth J, Vogl T, Sorg C, et al. Phagocyte-specific S100 proteins: a novel group of proinflammatory molecules. Trends Immunol. 2003;24:155–158.
  • Leukert N, Sorg C, Roth J. Molecular basis of the complex formation between the two calcium-binding proteins S100A8 (MRP8) and S100A9 (MRP14). Biol Chem. 2005;386:429–434.
  • Vogl T, Gharibyan AL, Morozova-Roche LA. Pro-inflammatory S100A8 and S100A9 proteins: self-assembly into multifunctional native and amyloid complexes. Int J Mol Sci. 2012;13:2893–2917.
  • Rammes A, Roth J, Goebeler M, et al. Myeloid-related protein (MRP) 8 and MRP14, calcium-binding proteins of the S100 family, are secreted by activated monocytes via a novel, tubulin-dependent pathway. J Biol Chem. 1997;272:9496–9502.
  • Pruenster M, Kurz AR, Chung KJ, et al. Extracellular MRP8/14 is a regulator of beta2 integrin-dependent neutrophil slow rolling and adhesion. Nat Commun. 2015;6:6915.
  • Tardif MR, Chapeton-Montes JA, Posvandzic A, et al. Secretion of S100A8, S100A9, and S100A12 by neutrophils involves reactive oxygen species and potassium efflux. J Immunol Res. 2015;2015:Article ID 296149.
  • Vogl T, Tenbrock K, Ludwig S, et al. Mrp8 and Mrp14 are endogenous activators of toll-like receptor 4, promoting lethal, endotoxin-induced shock. Nat Med. 2007;13:1042–1049.
  • Ehlermann P, Eggers K, Bierhaus A, et al. Increased proinflammatory endothelial response to S100A8/A9 after preactivation through advanced glycation end products. Cardiovasc Diabetol. 2006;5:6.
  • Turovskaya O, Foell D, Sinha P, et al. RAGE, carboxylated glycans and S100A8/A9 play essential roles in colitis-associated carcinogenesis. Carcinogenesis. 2008;29:2035–2043.
  • Alexaki VI, May AE, Fujii C, et al. S100A9 induces monocyte/macrophage migration via EMMPRIN. Thromb Haemost. 2016;117:636–639.
  • Hibino T, Sakaguchi M, Miyamoto S, et al. S100A9 is a novel ligand of EMMPRIN that promotes melanoma metastasis. Cancer Res. 2013;73:172–183.
  • Viemann D, Strey A, Janning A, et al. Myeloid-related proteins 8 and 14 induce a specific inflammatory response in human microvascular endothelial cells. Blood. 2005;105:2955–2962.
  • Wang L, Luo H, Chen X, et al. Functional characterization of S100A8 and S100A9 in altering monolayer permeability of human umbilical endothelial cells. Plos One. 2014;9:e90472.
  • Ryckman C, Vandal K, Rouleau P, et al. Proinflammatory activities of S100: proteins S100A8, S100A9, and S100A8/A9 induce neutrophil chemotaxis and adhesion. J Immunol. 2003;170:3233–3242.
  • Atallah M, Krispin A, Trahtemberg U, et al. Constitutive neutrophil apoptosis: regulation by cell concentration via S100 A8/9 and the MEK-ERK pathway. Plos One. 2012;7:e29333.
  • Bouma G, Lam-Tse WK, Wierenga-Wolf AF, et al. Increased serum levels of MRP-8/14 in type 1 diabetes induce an increased expression of CD11b and an enhanced adhesion of circulating monocytes to fibronectin. Diabetes. 2004;53:1979–1986.
  • Loser K, Vogl T, Voskort M, et al. The toll-like receptor 4 ligands Mrp8 and Mrp14 are crucial in the development of autoreactive CD8+ T cells. Nat Med. 2010;16:713–717.
  • Austermann J, Friesenhagen J, Fassl SK, et al. Alarmins MRP8 and MRP14 induce stress tolerance in phagocytes under sterile inflammatory conditions. Cell Rep. 2014;9:2112–2123.
  • Aneja R, Odoms K, Dunsmore K, et al. Extracellular heat shock protein-70 induces endotoxin tolerance in THP-1 cells. J Immunol. 2006;177:7184–7192.
  • Aneja RK, Tsung A, Sjodin H, et al. Preconditioning with high mobility group box 1 (HMGB1) induces lipopolysaccharide (LPS) tolerance. J Leukoc Biol. 2008;84:1326–1334.
  • Petersen B, Wolf M, Austermann J, et al. The alarmin Mrp8/14 as regulator of the adaptive immune response during allergic contact dermatitis. Embo J. 2013;32:100–111.
  • Gabrilovich DI, Nagaraj S. Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol. 2009;9:162–174.
  • Cheng P, Corzo CA, Luetteke N, et al. Inhibition of dendritic cell differentiation and accumulation of myeloid-derived suppressor cells in cancer is regulated by S100A9 protein. J Exp Med. 2008;205:2235–2249.
  • Foell D, Wittkowski H, Roth J. Monitoring disease activity by stool analyses: from occult blood to molecular markers of intestinal inflammation and damage. Gut. 2009;58:859–868.
  • Soyfoo MS, Roth J, Vogl T, et al. Phagocyte-specific S100A8/A9 protein levels during disease exacerbations and infections in systemic lupus erythematosus. J Rheumatol. 2009;36:2190–2194.
  • Horvath I, Jia X, Johansson P, et al. Pro-inflammatory S100A9 protein as a robust biomarker differentiating early stages of cognitive impairment in Alzheimer’s disease. ACS Chem Neurosci. 2016;20(7):34–39.
  • Markowitz J, Carson WE III. Review of S100A9 biology and its role in cancer. Biochim Biophys Acta. 2013;1835:100–109.
  • Pedersen SJ, Sorensen IJ, Lambert RG, et al. Radiographic progression is associated with resolution of systemic inflammation in patients with axial spondylarthritis treated with tumor necrosis factor alpha inhibitors: a study of radiographic progression, inflammation on magnetic resonance imaging, and circulating biomarkers of inflammation, angiogenesis, and cartilage and bone turnover. Arthritis Rheum. 2011;63:3789–3800.
  • Myklebust G, Gran JT. A prospective study of 287 patients with polymyalgia rheumatica and temporal arteritis: clinical and laboratory manifestations at onset of disease and at the time of diagnosis. Br J Rheumatol. 1996;35:1161–1168.
  • Choi IY, Gerlag DM, Herenius MJ, et al. MRP8/14 serum levels as a strong predictor of response to biological treatments in patients with rheumatoid arthritis. Ann Rheum Dis. 2015;74:499–505.
  • Foell D, Wulffraat N, Wedderburn LR, et al. Methotrexate withdrawal at 6 vs 12 months in juvenile idiopathic arthritis in remission: a randomized clinical trial. JAMA. 2010;303:1266–1273.
  • Odink K, Cerletti N, Bruggen J, et al. Two calcium-binding proteins in infiltrate macrophages of rheumatoid arthritis. Nature. 1987;330:80–82.
  • Youssef P, Roth J, Frosch M, et al. Expression of myeloid related proteins (MRP) 8 and 14 and the MRP8/14 heterodimer in rheumatoid arthritis synovial membrane. J Rheumatol. 1999;26:2523–2528.
  • Berntzen HB, Olmez U, Fagerhol MK, et al. The leukocyte protein L1 in plasma and synovial fluid from patients with rheumatoid arthritis and osteoarthritis. Scand J Rheumatol. 1991;20:74–82.
  • Sunahori K, Yamamura M, Yamana J, et al. The S100A8/A9 heterodimer amplifies proinflammatory cytokine production by macrophages via activation of nuclear factor kappa B and p38 mitogen-activated protein kinase in rheumatoid arthritis. Arthritis Res Ther. 2006;8:R69.
  • Van Lent PL, Grevers L, Blom AB, et al. Myeloid-related proteins S100A8/S100A9 regulate joint inflammation and cartilage destruction during antigen-induced arthritis. Ann Rheum Dis. 2008;67:1750–1758.
  • Kane D, Roth J, Frosch M, et al. Increased perivascular synovial membrane expression of myeloid-related proteins in psoriatic arthritis. Arthritis Rheum. 2003;48:1676–1685.
  • Grevers LC, De Vries TJ, Vogl T, et al. S100A8 enhances osteoclastic bone resorption in vitro through activation of toll-like receptor 4: implications for bone destruction in murine antigen-induced arthritis. Arthritis Rheum. 2011;63:1365–1375.
  • Hurnakova J, Zavada J, Hanova P, et al. Serum calprotectin (S100A8/9): an independent predictor of ultrasound synovitis in patients with rheumatoid arthritis. Arthritis Res Ther. 2015;17:252.
  • Hammer HB, Odegard S, Syversen SW, et al. Calprotectin (a major S100 leucocyte protein) predicts 10-year radiographic progression in patients with rheumatoid arthritis. Ann Rheum Dis. 2010;69:150–154.
  • Hammer HB, Odegard S, Fagerhol MK, et al. Calprotectin (a major leucocyte protein) is strongly and independently correlated with joint inflammation and damage in rheumatoid arthritis. Ann Rheum Dis. 2007;66:1093–1097.
  • Moncrieffe H, Ursu S, Holzinger D, et al. A subgroup of juvenile idiopathic arthritis patients who respond well to methotrexate are identified by the serum biomarker MRP8/14 protein. Rheumatology (Oxford). 2013;52:1467–1476.
  • Holzinger D, Frosch M, Kastrup A, et al. The toll-like receptor 4 agonist MRP8/14 protein complex is a sensitive indicator for disease activity and predicts relapses in systemic-onset juvenile idiopathic arthritis. Ann Rheum Dis. 2012;71:974–980.
  • Anink J, Van Suijlekom-Smit LW, Otten MH, et al. MRP8/14 serum levels as a predictor of response to starting and stopping anti-TNF treatment in juvenile idiopathic arthritis. Arthritis Res Ther. 2015;17:200.
  • Obry A, Lequerre T, Hardouin J, et al. Identification of S100A9 as biomarker of responsiveness to the methotrexate/etanercept combination in rheumatoid arthritis using a proteomic approach. Plos One. 2014;9:e115800.
  • Vogl T, Eisenblatter M, Voller T, et al. Alarmin S100A8/S100A9 as a biomarker for molecular imaging of local inflammatory activity. Nat Commun. 2014;5:4593.
  • Bjork P, Bjork A, Vogl T, et al. Identification of human S100A9 as a novel target for treatment of autoimmune disease via binding to quinoline-3-carboxamides. Plos Biol. 2009;7:e97.
  • Faust A, Voller T, Busch F, et al. Development and evaluation of a non-peptidic ligand for the molecular imaging of inflammatory processes using S100A9 (MRP14) as a novel target. Chem Commun (Camb). 2015;51:15637–15640.
  • Mansfield E, Chae JJ, Komarow HD, et al. The familial Mediterranean fever protein, pyrin, associates with microtubules and colocalizes with actin filaments. Blood. 2001;98:851–859.
  • Kallinich T, Haffner D, Niehues T, et al. Colchicine use in children and adolescents with familial Mediterranean fever: literature review and consensus statement. Pediatrics. 2007;119:e474–83.
  • Wei S, Chen X, Zhou J, et al. Microenvironment induced myelodysplastic syndrome (MDS) in S100A9 transgenic mice caused by myeloid-derived suppressor cells (MDSC). Blood. 2015;118:788. American Society of Hematology.
  • Raquil MA, Anceriz N, Rouleau P, et al. Blockade of antimicrobial proteins S100A8 and S100A9 inhibits phagocyte migration to the alveoli in streptococcal pneumonia. J Immunol. 2008;180:3366–3374.
  • Vandal K, Rouleau P, Boivin A, et al. Blockade of S100A8 and S100A9 suppresses neutrophil migration in response to lipopolysaccharide. J Immunol. 2003;171:2602–2609.
  • Cesaro A, Anceriz N, Plante A, et al. An inflammation loop orchestrated by S100A9 and calprotectin is critical for development of arthritis. Plos One. 2012;7:e45478.
  • Wang Y, Fang C, Gao H, et al. Platelet-derived S100 family member myeloid-related protein-14 regulates thrombosis. J Clin Invest. 2014;124:2160–2171.
  • Durante A, Bronzato S. The increased cardiovascular risk in patients affected by autoimmune diseases: review of the various manifestations. J Clin Med Res. 2015;7:379–384.
  • Qin H, Lerman B, Sakamaki I, et al. Generation of a new therapeutic peptide that depletes myeloid-derived suppressor cells in tumor-bearing mice. Nat Med. 2014;20:676–681.
  • Monnet E, Shang L, Lapeyre G, et al. AB0451 NI-0101, a monoclonal antibody targeting toll like receptor 4 (TLR4) being developed for rheumatoid arthritis (RA) treatment with a potential for personalized medicine. Ann Rheum Dis. 2015;74:1046.
  • Hatterer E, Shang L, Simonet P, et al. A specific anti-citrullinated protein antibody profile identifies a group of rheumatoid arthritis patients with a toll-like receptor 4-mediated disease. Arthritis Res Ther. 2016 Oct 6;18:224.
  • Van Den Bosch MH, Blom AB, Schelbergen RF, et al. Alarmin S100A9 induces proinflammatory and catabolic effects predominantly in the M1 macrophages of human osteoarthritic synovium. J Rheumatol. 2016;43:1874–1884.
  • Thone J, Linker RA. Laquinimod in the treatment of multiple sclerosis: a review of the data so far. Drug Des Devel Ther. 2016;10:1111–1118.
  • D’Haens G, Sandborn WJ, Colombel JF, et al. A phase II study of laquinimod in Crohn’s disease. Gut. 2015;64:1227–1235.
  • Kapanadze T, Gamrekelashvili J, Ma C, et al. Regulation of accumulation and function of myeloid derived suppressor cells in different murine models of hepatocellular carcinoma. J Hepatol. 2013;59:1007–1013.
  • Kilmartin B, Reen DJ. HSP60 induces self-tolerance to repeated HSP60 stimulation and cross-tolerance to other pro-inflammatory stimuli. Eur J Immunol. 2004;34:2041–2051.

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