Proinflammatory S100A12 can activate human monocytes via toll-like receptor 4

American Journal of Respiratory and Critical Care Medicine

Volumn 187, Issue 12, 2013, Pages 1324-1334

  Foell, Dirk ^a,b   Wittkowski, Helmut ^a   Kessel, Christoph ^a   Lüken, Aloys ^b   Weinhage, Toni ^a   Varga, Georg ^a   Vogl, Thomas ^b   Wirth, Timo ^a   Viemann, Dorothee ^c   Björk, Per ^d   Van Zoelen, Marieke A D ^e   Gohar, Faekah ^a   Srikrishna, Geetha ^f   Kraft, Matthias ^g   Roth, Johannes ^b  

^a UNIVERSITY HOSPITAL MÜNSTER   (Germany)

^b UNIVERSITY OF MÜNSTER   (Germany)

^c HANNOVER MEDICAL SCHOOL   (Germany)

^d Active Biotech Research AB   (Sweden)

^e UNIVERSITY OF AMSTERDAM   (Netherlands)

^f BURNHAM INSTITUTE   (United States)

^g UNIVERSITY OF GREIFSWALD   (Germany)

Author keywords

Granulocytes; Inflammation; Innate immunity; Pattern recognition receptors; Receptor for advanced glycation end products

Indexed keywords

ADVANCED GLYCATION END PRODUCT RECEPTOR; CALCIUM BINDING PROTEIN; INTERLEUKIN 15 RECEPTOR ALPHA; INTERLEUKIN 18; INTERLEUKIN 7; MONOCYTE CHEMOTACTIC PROTEIN 1; PROTEIN S100A12; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL ACTIVATION; CELL STRESS; CYTOKINE RELEASE; ENDOTOXEMIA; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; INNATE IMMUNITY; MONOCYTE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; SEPSIS; SIGNAL TRANSDUCTION; UPREGULATION;

ADULT; AGED; CELLS, CULTURED; FEMALE; HUMANS; INFLAMMATION; MALE; MIDDLE AGED; MONOCYTES; S100 PROTEINS; SEPSIS; TOLL-LIKE RECEPTOR 4; YOUNG ADULT;

EID: 84879567790     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.201209-1602OC     Document Type: Article

References (54)

1. Bianchi ME. DAMPs, PAMPs and alarmins: all we need to know about danger. J Leukoc Biol 2007;81: 1-5.
2. Oppenheim JJ, Yang D. Alarmins: chemotactic activators of immune responses. Curr Opin Immunol 2005;17: 359-365.
3. Stern D, Yan SD, Yan SF, Schmidt AM. Receptor for advanced glycation endproducts: a multiligand receptor magnifying cell stress in diverse pathologic settings. Adv Drug Deliv Rev 2002;54: 1615-1625.
4. Lotze MT, Tracey KJ. High-mobility group box 1 protein (HMGB1): nuclear weapon in the immune arsenal. Nat Rev Immunol 2005;5: 331-342.
5. Hofmann MA, Drury S, Fu C, Qu W, Taguchi A, Lu Y, Avila C, Kambham N, Bierhaus A, Nawroth P, et al. RAGE mediates a novel proinflammatory axis: a central cell surface receptor for S100/calgranulin polypeptides. Cell 1999;97: 889-901.
6. Foell D, Wittkowski H, Roth J. Mechanisms of disease: a 'DAMP' view of inflammatory arthritis. Nat Clin Pract Rheumatol 2007;3: 382-390.
7. Loser K, Vogl T, Voskort M, Lueken A, Kupas V, Nacken W, Klenner L, Kuhn A, Foell D, Sorokin L, et al. The Toll-like receptor 4 ligands Mrp8 and Mrp14 are crucial in the development of autoreactive CD81 T cells. Nat Med 2010;16: 713-717.
8. Vogl T, Tenbrock K, Ludwig S, Leukert N, Ehrhardt C, van Zoelen MA, Nacken W, Foell D, van der Poll T, Sorg C, et al. Mrp8 and Mrp14 are endogenous activators of Toll-like receptor 4, promoting lethal, endotoxin-induced shock. Nat Med 2007;13: 1042-1049.
9. Heizmann CW, Fritz G, Schafer BW. S100 proteins: structure, functions and pathology. Front Biosci 2002;7: d1356-d1368.
10. Vogl T, Propper C, Hartmann M, Strey A, Strupat K, van den Bos C, Sorg C, Roth J. S100A12 is expressed exclusively by granulocytes and acts independently from MRP8 and MRP14. J Biol Chem 1999;274: 25291-25296.
11. Wittkowski H, Sturrock A, van Zoelen MA, Viemann D, van der Poll T, Hoidal JR, Roth J, Foell D. Neutrophil-derived S100A12 in acute lung injury and respiratory distress syndrome. Crit Care Med 2007;35: 1369-1375.
12. Foell D, Kane D, Bresnihan B, Vogl T, Nacken W, Sorg C, Fitzgerald O, Roth J. Expression of the pro-inflammatory protein S100A12 (EN-RAGE) in rheumatoid and psoriatic arthritis. Rheumatology (Oxford) 2003;42: 1383-1389.
13. Foell D, Seeliger S, Vogl T, Koch HG, Maschek H, Harms E, Sorg C, Roth J. Expression of S100A12 (EN-RAGE) in cystic fibrosis. Thorax 2003;58: 613-617.
14. Foell D, Kucharzik T, Kraft M, Vogl T, Sorg C, Domschke W, Roth J. Neutrophil derived human S100A12 (EN-RAGE) is strongly expressed during chronic active inflammatory bowel disease. Gut 2003;52: 847-853.
15. Foell D, Wittkowski H, Ren Z, Turton J, Pang G, Daebritz J, Ehrchen J, Heidemann J, Borody T, Roth J, et al. Phagocyte-specific S100 proteins are released from affected mucosa and promote immune responses during inflammatory bowel disease. J Pathol 2008;216: 183-192.
16. Schmidt AM, Yan SD, Yan SF, Stern DM. The multiligand receptor RAGE as a progression factor amplifying immune and inflammatory responses. J Clin Invest 2001;108: 949-955.
17. Goova MT, Li J, Kislinger T, Qu W, Lu Y, Bucciarelli LG, Nowygrod S, Wolf BM, Caliste X, Yan SF, et al. Blockade of receptor for advanced glycation end-products restores effective wound healing in diabetic mice. Am J Pathol 2001;159: 513-525.
18. Fuellen G, Foell D, Nacken W, Sorg C, Kerkhoff C. Absence of S100A12 in mouse: implications for RAGE-S100A12 interaction. Trends Immunol 2003;24: 622-624.
19. Ravasi T, Hsu K, Goyette J, Schroder K, Yang Z, Rahimi F, Miranda LP, Alewood PF, Hume DA, Geczy C. Probing the S100 protein family through genomic and functional analysis. Genomics 2004;84: 10-22.
20. Yang Z, Yan WX, Cai H, Tedla N, Armishaw C, Di Girolamo N, Wang HW, Hampartzoumian T, Simpson JL, Gibson PG, et al. S100A12 provokes mast cell activation: a potential amplification pathway in asthma and innate immunity. J Allergy Clin Immunol 2007;119: 106-114.
21. Gordon S, Taylor PR. Monocyte and macrophage heterogeneity. Nat Rev Immunol 2005;5: 953-964.
22. Foell D, Wittkowski H, Viemann D, Heidemann J, Lebiez P, Kucharzik T, Roth J. The role of the pro-inflammatory mediator S100A12 in IBD [abstract]. Gastroenterology 2006;130: A28.
23. Foell D, Wittkowski H, Viemann D, Ehrchen J, Vogl T, Roth J. The mediator S100A12 is critically involved in early inflammatory events of rheumatoid diseases [abstract]. Arthritis Rheum 2005;52: S477.
24. Foell D, Wittkowski H, Viemann D, Weigle B, Vogl T, Roth J. Neutrophil-derived S100A12 (EN-RAGE): Molecular basis of its expression, secretion, receptor-binding, and pro-inflammatory effects [abstract]. Ann Rheum Dis 2006;65: 455.
25. Foell D, Wittkowski H, Lueken A, Daebritz J, Viemann D, Heidemann J, Vogl T, Roth J. The Mediator S100a12 is critically involved in early inflammatory events of inflammatory bowel disease [abstract]. Gastroenterology 2009;136: 254.
26. Zwadlo G, Brocker EB, von Bassewitz DB, Feige U, Sorg C. A monoclonal antibody to a differentiation antigen present on mature human macrophages and absent from monocytes. J Immunol 1985;134: 1487-1492.
27. Raucci A, Cugusi S, Antonelli A, Barabino SM, Monti L, Bierhaus A, Reiss K, Saftig P, Bianchi ME. A soluble form of the receptor for advanced glycation endproducts (RAGE) is produced by proteolytic cleavage of the membrane-bound form by the sheddase a disintegrin and metalloprotease 10 (ADAM10). FASEB J 2008;22: 3716-3727.
28. Srikrishna G, Nayak J,Weigle B, Temme A, Foell D, Hazelwood L, Olsson A, Volkmann N, Hanein D, Freeze HH. Carboxylated N-glycans on RAGE promote S100A12 binding and signaling. J Cell Biochem 2010; 110: 645-659.
29. Viemann D, Goebeler M, Schmid S, Klimmek K, Sorg C, Ludwig S, Roth J. Transcriptional profiling of IKK2/NF-kappa B- and p38 MAP kinase-dependent gene expression in TNF-alpha-stimulated primary human endothelial cells. Blood 2004;103: 3365-3373.
30. Quackenbush J. Microarray data normalization and transformation. Nat Genet 2002;32: 496-501.
31. Vogl T, Ludwig S, Goebeler M, Strey A, Thorey IS, Reichelt R, Foell D, Gerke V, Manitz MP, Nacken W, et al. MRP8 and MRP14 control microtubule reorganization during transendothelial migration of phagocytes. Blood 2004;104: 4260-4268.
32. Kikkawa T, Sato N, Kojika M, Takahashi G, Aoki K, Hoshikawa K, Akitomi S, Shozushima T, Suzuki K, Wakabayashi G, et al. Significance of measuring S100A12 and sRAGE in the serum of sepsis patients with postoperative acute lung injury. Dig Surg 2010;27: 307-312.
33. Wittkowski H, Frosch M, Wulffraat N, Goldbach-Mansky R, Kallinich T, Kuemmerle-Deschner J, Fruhwald MC, Dassmann S, Pham TH, Roth J, et al. S100A12 is a novel molecular marker differentiating systemic-onset juvenile idiopathic arthritis from other causes of fever of unknown origin. Arthritis Rheum 2008;58: 3924-3931.
34. Donato R. S100: a multigenic family of calcium-modulated proteins of the EF-hand type with intracellular and extracellular functional roles. Int J Biochem Cell Biol 2001;33: 637-668.
35. Foell D, Ichida F, Vogl T, Yu X, Chen R, Miyawaki T, Sorg C, Roth J. S100A12 (EN-RAGE) in monitoring Kawasaki disease. Lancet 2003; 361: 1270-1272.
36. Foell D, Roth J. Proinflammatory S100 proteins in arthritis and autoimmune disease. Arthritis Rheum 2004;50: 3762-3771.
37. Donato R. RAGE: a single receptor for several ligands and different cellular responses: the case of certain S100 proteins. Curr Mol Med 2007;7: 711-724.
38. Hudson BI, Kalea AZ, Del Mar Arriero M, Harja E, Boulanger E, D'Agati V, Schmidt AM. Interaction of the RAGE cytoplasmic domain with diaphanous-1 is required for ligand-stimulated cellular migration through activation of Rac1 and Cdc42. J Biol Chem 2008; 283: 34457-34468.
39. Zhang H, Tasaka S, Shiraishi Y, Fukunaga K, Yamada W, Seki H, Ogawa Y, Miyamoto K, Nakano Y, Hasegawa N, et al. Role of soluble receptor for advanced glycation end products on endotoxin-induced lung injury. Am J Respir Crit Care Med 2008; 178: 356-362.
40. Liliensiek B, Weigand MA, Bierhaus A, Nicklas W, Kasper M, Hofer S, Plachky J, Grone HJ, Kurschus FC, Schmidt AM, et al. Receptor for advanced glycation end products (RAGE) regulates sepsis but not the adaptive immune response. J Clin Invest 2004;113: 1641-1650.
41. Goyette J, Yan WX, Yamen E, Chung YM, Lim SY, Hsu K, Rahimi F, Di Girolamo N, Song C, Jessup W, et al. Pleiotropic roles of S100A12 in coronary atherosclerotic plaque formation and rupture. J Immunol 2009;183: 593-603.
42. Miranda LP, Tao T, Jones A, Chernushevich I, Standing KG, Geczy CL, Alewood PF. Total chemical synthesis and chemotactic activity of human S100A12 (EN-RAGE). FEBS Lett 2001;488: 85-90.
43. Yang Z, Tao T, Raftery MJ, Youssef P, Di Girolamo N, Geczy CL. Proinflammatory properties of the human S100 protein S100A12. J Leukoc Biol 2001;69: 986-994.
44. Mikkelsen SE, Novitskaya V, Kriajevska M, Berezin V, Bock E, Norrild B, Lukanidin E. S100A12 protein is a strong inducer of neurite outgrowth from primary hippocampal neurons. J Neurochem 2001; 79: 767-776.
45. Foell D, Hernandez-Rodriguez J, Sanchez M, Vogl T, Cid MC, Roth J. Early recruitment of phagocytes contributes to the vascular inflammation of giant cell arteritis. J Pathol 2004;204: 311-316.
46. Foell D, Wittkowski H, Hammerschmidt I, Wulffraat N, Schmeling H, Frosch M, Horneff G, Kuis W, Sorg C, Roth J. Monitoring neutrophil activation in juvenile rheumatoid arthritis by S100A12 serum concentrations. Arthritis Rheum 2004;50: 1286-1295.
47. Moroz OV, Burkitt W, Wittkowski H, He W, Ianoul A, Novitskaya V, Xie J, Polyakova O, Lednev IK, Shekhtman A, et al. Both Ca21 and Zn21 are essential for S100A12 protein oligomerization and function. BMC Biochem 2009;10: 11.
48. Zeng S, Zhang QY, Huang J, Vedantham S, Rosario R, Ananthakrishnan R, Yan SF, Ramasamy R, DeMatteo RP, Emond JC, et al. Opposing roles of RAGE and Myd88 signaling in extensive liver resection. FASEB J 2012;26: 882-893.
49. Cieri N, Camisa B, Cocchiarella F, Forcato M, Oliveira G, Provasi E, Bondanza A, Bordignon C, Peccatori J, Ciceri F, et al. IL-7 and IL-15 instruct the generation of human memory stem T cells from naive precursors. Blood 2013;121: 573-584.
50. McCaughtry TM, Etzensperger R, Alag A, Tai X, Kurtulus S, Park JH, Grinberg A, Love P, Feigenbaum L, Erman B, et al. Conditional deletion of cytokine receptor chains reveals that IL-7 and IL-15 specify CD8 cytotoxic lineage fate in the thymus. J ExpMed 2012;209: 2263-2276.
51. Mortier E, Bernard J, Plet A, Jacques Y. Natural, proteolytic release of a soluble form of human IL-15 receptor alpha-chain that behaves as a specific, high affinity IL-15 antagonist. J Immunol 2004;173: 1681-1688.
52. Neely GG, Epelman S, Ma LL, Colarusso P, Howlett CJ, Amankwah EK, McIntyre AC, Robbins SM, Mody CH. Monocyte surface-bound IL-15 can function as an activating receptor and participate in reverse signaling. J Immunol 2004;172: 4225-4234.
53. Regamey N, Obregon C, Ferrari-Lacraz S, van Leer C, Chanson M, Nicod LP, Geiser T. Airway epithelial IL-15 transforms monocytes into dendritic cells. Am J Respir Cell Mol Biol 2007;37: 75-84.
54. Yoshioka A, Okamoto R, Oshima S, Akiyama J, Tsuchiya K, Nakamura T, Kanai T, Watanabe M. Flagellin stimulation suppresses IL-7 secretion of intestinal epithelial cells. Cytokine 2008;44: 57-64.