High mobility group box-1 protein induces the migration and activation of human dendritic cells and acts as an alarmin

Journal of Leukocyte Biology

Volumn 81, Issue 1, 2007, Pages 59-66

  Yang, De ^a,b   Chen, Qian ^a   Yang, Huan ^c   Tracey, Kevin J ^c   Bustin, Michael ^d   Oppenheim, Joost J ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b SAIC FREDERICK INC   (United States)

^c National Institutes of Health ^*  (United States)

^d NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Chemotaxis; HMGB1; Maturation; RAGE

Indexed keywords

B7 ANTIGEN; CD83 ANTIGEN; CD86 ANTIGEN; CHEMOATTRACTANT; CYTOKINE; HIGH MOBILITY GROUP B1 PROTEIN; HLA A ANTIGEN; HLA B ANTIGEN; HLA C ANTIGEN; INHIBITORY GUANINE NUCLEOTIDE BINDING PROTEIN; INTERLEUKIN 12P70; INTERLEUKIN 6; INTERLEUKIN 8; PERTUSSIS TOXIN; PROTEIN ANTIBODY; RANTES; SECONDARY LYMPHOID TISSUE CHEMOKINE; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CELL ACTIVATION; CELL FUNCTION; CELL MATURATION; CELL MIGRATION; CONTROLLED STUDY; DENDRITIC CELL; GLYCATION; HUMAN; HUMAN CELL; LYMPHOCYTE PROLIFERATION; MONOCYTE; PHENOTYPE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN QUALITY; UPREGULATION; WESTERN BLOTTING;

ANTIGENS, NEOPLASM; CELL DIFFERENTIATION; CELLS, CULTURED; CHEMOTACTIC FACTORS; CHEMOTAXIS; DENDRITIC CELLS; DOSE-RESPONSE RELATIONSHIP, DRUG; GTP-BINDING PROTEIN ALPHA SUBUNITS, GI-GO; HMGB1 PROTEIN; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASES; MONOCYTES; PERTUSSIS TOXIN;

EID: 33845885124     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0306180     Document Type: Article

References (43)

1. Goodwin, G. H., Johns, E. W. (1973) Isolation and characterization of two calf-thymus chromatin non-histone proteins with high contents of acidic and basic amino acids. Eur. J. Biochem. 40, 215-219.
2. Bustin, M., Lehn, D. A., Landsman, D. (1990) Structural features of the HMG chromosomal proteins and their genes. Biochim. Biophys. Acta 1049, 231-243.
3. Andersson, U., Erlandsson-Harris, H., Yang, H., Tracey, K. J. (2002) HMGB1 as a DNA-binding cytokine. J. Leukoc. Biol. 72, 1084-1091.
4. Einck, L., Bustin, M. (1985) The intracellular distribution and function of the high mobility group chromosomal proteins. Exp. Cell Res. 156, 295-310.
5. Thomas, J. O., Travers, A. A. (2001) HMG1 and 2, and related "architectural" DNA-binding proteins. Trends Biochem. Sci. 26, 167-174.
6. Bustin, M. (1999) Regulation of DNA-dependent activities by the functional motifs of the high-mobility-group chromosomal proteins. Mol. Cell. Biol. 19, 5237-5246.
7. Calogero, S., Grassi, F., Aguzzi, A., Voigtlander, T., Ferrier, P., Ferrari, S., Bianchi, M. E. (1999) The lack of chromosomal protein Hmg1 does not disrupt cell growth but causes lethal hypoglycaemia in newborn mice. Nat. Genet. 22, 276-280.
8. Wang, H., Bloom, O., Zhang, M., Vishnubhakat, J. M., Ombrellino, M., Che, J., Frazier, A., Yang, H., Ivanova, S., Borovikova, L., et al. (1999) HMG-1 as a late mediator of endotoxin lethality in mice. Science 285, 248-251.
9. Scaffidi, P., Misteli, T., Bianchi, M. E. (2002) Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature 418, 191-195.
10. Rovere-Querini, P., Capobianco, A., Scaffidi, P., Valentinis, B., Catalanotti, F., Giazzon, M., Dumitriu, I. E., Muller, S., Iannacone, M., Traversari, C., Bianchi, M. E., Manfredi, A. A. (2004) HMGB1 is an endogenous immune adjuvant released by necrotic cells. EMBO Rep. 5, 825-830.
11. Chen, G., Li, J., Ochani, M., Rendon-Mitchell, B., Qiang, X., Susarla, S., Ulloa, L., Yang, H., Fan, S., Goyert, S. M., Wang, P., Tracey, K. J., Sama, A. E., Wang, H. (2004) Bacterial endotoxin stimulates macrophages to release HMGB1 partly through CD14- and TNF-dependent mechanisms. J. Leukoc. Biol. 76, 994-1001.
12. Rendon-Mitchell, B., Ochani, M., Li, J., Han, J., Wang, H., Yang, H., Susarla, S., Czura, C., Mitchell, R. A., Chen, G., Sama, A. E., Tracey, K. J. (2003) IFN-γ induces high mobility group box 1 protein release partly through a TNF-dependent mechanism. J. Immunol. 170, 3890-3897.
13. Wang, H., Liao, H., Ochani, M., Justiniani, M., Lin, X., Yang, L., Al-Abed, Y., Metz, C., Miller, E. J., Tracey, K. J., Ulloa, L. (2004) Cholinergic agonists inhibit HMGB1 release and improve survival in experimental sepsis. Nat. Med. 10, 1216-1221.
14. Dumitriu, I. E., Baruah, P., Valentinis, B., Voll, R. E., Herrmann, M., Nawroth, P. P., Arnold, B., Bianchi, M. E., Manfredi, A. A., Rovere-Querini, P. (2005) Release of high mobility group box 1 by dendritic cells controls T cell activation via the receptor for advanced glycation end products. J. Immunol. 174, 7506-7515.
15. Semino, C., Angelini, G., Poggi, A., Rubartelli, A. (2005) NK/iDC interaction results in IL-18 secretion by DCs at the synaptic cleft followed by NK cell activation and release of the DC maturation factor HMGB1. Blood 106, 609-616.
16. Bonaldi, T., Talamo, F., Scaffidi, P., Ferrera, D., Porto, A., Bachi, A., Rubartelli, A., Agresti, A., Bianchi, M. E. (2003) Monocytic cells hyperacetylate chromatin protein HMGB1 to redirect it towards secretion. EMBO J. 22, 5551-5560.
17. Hori, O., Brett, J., Slattery, T., Cao, R., Zhang, J., Chen, J. X., Nagashima, M., Lundh, E. R., Vijay, S., Nitecki, D., et al. (1995) The receptor for advanced glycation end products (RAGE) is a cellular binding site for amphoterin. Mediation of neurite outgrowth and co-expression of rage and amphoterin in the developing nervous system. J. Biol. Chem. 270, 25752-25761.
18. Huttunen, H. J., Fages, C., Rauvala, H. (1999) Receptor for advanced glycation end products (RAGE)-mediated neurite outgrowth and activation of NF-κB require the cytoplasmic domain of the receptor but different downstream signaling pathways. J. Biol. Chem. 274, 19919-19924.
19. Rouhiainen, A., Kuja-Panula, J., Wilkman, E., Pakkanen, J., Stenfors, J., Tuominen, R. K., Lepantalo, M., Carpen, O., Parkkinen, J., Rauvala, H. (2004) Regulation of monocyte migration by amphoterin (HMGB1). Blood 104, 1174-1182.
20. Degryse, B., Bonaldi, T., Scaffidi, P., Muller, S., Resnati, M., Sanvito, F., Arrigoni, G., Bianchi, M. E. (2001) The high mobility group (HMG) boxes of the nuclear protein HMG1 induce chemotaxis and cytoskeleton reorganization in rat smooth muscle cells. J. Cell Biol. 152, 1197-1206.
21. Palumbo, R., Sampaolesi, M., De Marchis, F., Tonlorenzi, R., Colombetti, S., Mondino, A., Cossu, G., Bianchi, M. E. (2004) Extracellular HMGB1, a signal of tissue damage, induces mesoangioblast migration and proliferation. J. Cell Biol. 164, 441-449.
22. Dumitriu, I. E., Baruah, P., Bianchi, M. E., Manfredi, A. A., Rovere-Querini, P. (2005) Requirement of HMGB1 and RAGE for the maturation of human plasmacytoid dendritic cells. Eur. J. Immunol. 35, 2184-2190.
23. Messmer, D., Yang, H., Telusma, G., Knoll, F., Li, J., Messmer, B., Tracey, K. J., Chiorazzi, N. (2004) High mobility group box protein 1: an endogenous signal for dendritic cell maturation and Th1 polarization. J. Immunol. 173, 307-313.
24. Yenugu, S., Hamil, K. G., Birse, C. E., Ruben, S. M., French, F. S., Hall, S. H. (2003) Antibacterial properties of the sperm-binding proteins and peptides of human epididymis 2 (HE2) family; salt sensitivity, structural dependence and their interaction with outer and cytoplasmic membranes of Escherichia coli. Biochem. J. 372, 473-483.
25. Yang, D., Biragyn, A., Hoover, D. M., Lubkowski, J., Oppenheim, J. J. (2004) Multiple roles of antimicrobial defensins, cathelicidins, and eosinophil-derived neurotoxin in host defense. Annu. Rev. Immunol. 22, 181-215.
26. Yang, D., Chen, Q., Rosenberg, H. F., Rybak, S. M., Newton, D. L., Wang, Z. Y., Fu, Q., Tchernev, V. T., Wang, M., Schweitzer, B., Kingsmore, S. F., Patel, D. D., Oppenheim, J. J., Howard, O. M. (2004) Human ribonuclease A superfamily members, eosinophil-derived neurotoxin and pancreatic ribonuclease, induce dendritic cell maturation and activation. J. Immunol. 173, 6134-6142.
27. Yang, D., Oppenheim, J. J. (2004) Antimicrobial proteins act as "alarmins" in joint immune defense. Arthritis Rheum. 50, 3401-3403.
28. Oppenheim, J. J., Yang, D. (2005) Alarmins: chemotactic activators of immune responses. Curr. Opin. Immunol. 17, 359-365.
29. Li, J., Wang, H., Mason, J. M., Levine, J., Yu, M., Ulloa, L., Czura, C. J., Tracey, K. J., Yang, H. (2004) Recombinant HMGB1 with cytokine-stimulating activity. J. Immunol. Methods 289, 211-223.
30. Adachi, Y., Mizuno, S., Yoshida, M. (1990) Efficient large-scale purification of non-histone chromosomal proteins HMG1 and HMG2 by using Polybuffer-exchanger PBE94. J. Chromatogr. 530, 39-46.
31. De Yang, Chen, Q., Schmidt, A. P., Anderson, G. M., Wang, J. M., Wooters, J., Oppenheim, J. J., Chertov, O. (2000) LL-37, the neutrophil granule- and epithelial cell-derived cathelicidin, utilizes formyl peptide receptor-like 1 (FPRL1) as a receptor to chemoattract human peripheral blood neutrophils, monocytes, and T cells. J. Exp. Med. 192, 1069-1074.
32. Yang, D., Chen, Q., Chertov, O., Oppenheim, J. J. (2000) Human neutrophil defensins selectively chemoattract naïve T and immature dendritic cells. J. Leukoc. Biol. 68, 9-14.
33. Kurosaka, K., Chen, Q., Yarovinsky, F., Oppenheim, J. J., Yang, D. (2005) Mouse cathelin-related antimicrobial peptide chemoattracts leukocytes using formyl peptide receptor-like 1/mouse formyl peptide receptor-like 2 as the receptor and acts as an immune adjuvant. J. Immunol. 174, 6257-6265.
34. Yang, D., Howard, O. M. Z., Chen, Q., Oppenheim, J. J. (1999) Cutting edge: immature dendritic cells generated from monocytes in the presence of TGF-β1 express functional C-C chemokine receptor 6. J. Immunol. 163, 1737-1741.
35. Murphy, P. M. (1996) Chemokine receptors: structure, function and role in microbial pathogenesis. Cytokine Growth Factor Rev. 7, 47-64.
36. Kaslow, H. R., Burns, D. L. (1992) Pertussis toxin and target eukaryotic cells: binding, entry, and activation. FASEB J. 6, 2684-2690.
37. Banchereau, J., Steinman, R. M. (1998) Dendritic cells and the control of immunity. Nature 392, 245-251.
38. Park, J. S., Svetkauskaite, D., He, Q., Kim, J. Y., Strassheim, D., Ishizaka, A., Abraham, E. (2004) Involvement of Toll-like receptors 2 and 4 in cellular activation by high mobility group box 1 protein. J. Biol. Chem. 279, 7370-7377.
39. Kokkola, R., Andersson, A., Mullins, G., Ostberg, T., Treutiger, C. J., Arnold, B., Nawroth, P., Andersson, U., Harris, R. A., Harris, H. E. (2005) RAGE is the major receptor for the proinflammatory activity of HMGB1 in rodent macrophages. Scand. J. Immunol. 61, 1-9.
40. Park, J. S., Arcaroli, J., Yum, H. K., Yang, H., Wang, H., Yang, K. Y., Choe, K. H., Strassheim, D., Pitts, T. M., Tracey, K. J., Abraham, E. (2003) Activation of gene expression in human neutrophils by high mobility group box 1 protein. Am. J. Physiol. Cell Physiol. 284, C870-C879.
41. Liliensiek, B., Weigand, M. A., Bierhaus, A., Nicklas, W., Kasper, M., Hofer, S., Plachky, J., Grone, H. J., Kurschus, F. C., Schmidt, A. M., Yan, S. D., Martin, E., Schleicher, E., Stern, D. M., Hammerling, G. G., Nawroth, P. P., Arnold, B. (2004) Receptor for advanced glycation end products (RAGE) regulates sepsis but not the adaptive immune response. J. Clin. Invest. 113, 1641-1650.
42. Yang, H., Ochani, M., Li, J., Qiang, X., Tanovic, M., Harris, H. E., Susarla, S. M., Ulloa, L., Wang, H., DiRaimo, R., Czura, C. J., Roth, J., Warren, H. S., Fink, M. P., Fenton, M. J., Andersson, U., Tracey, K. J. (2004) Reversing established sepsis with antagonists of endogenous high-mobility group box 1. Proc. Natl. Acad. Sci. USA 101, 296-301.
43. Park, J. S., Gamboni-Robertson, F., He, Q., Svetkauskaite, D., Kim, J. Y., Strassheim, D., Sohn, J. W., Yamada, S., Maruyama, I., Banerjee, A., Ishizaka, A., Abraham, E. (2006) High mobility group box 1 protein interacts with multiple Toll-like receptors. Am. J. Physiol. Cell Physiol. 290, C917-C924.