The C-terminal acidic tail is responsible for the inhibitory effects of HMGB1 on efferocytosis

Journal of Leukocyte Biology

Volumn 88, Issue 5, 2010, Pages 973-979

  Banerjee, Sami ^a   Friggeri, Arnaud ^a,b,c   Liu, Gang ^a   Abraham, Edward ^a  

^a University of Alabama at Birmingham   (United States)

^b AMIENS UNIVERSITY HOSPITAL   (France)

^c INSERM   (France)

Author keywords

Apoptosis; Inflammation; Macrophages; Neutrophils; Phagocytosis

Indexed keywords

ADVANCED GLYCATION END PRODUCT RECEPTOR; HIGH MOBILITY GROUP B1 PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; RAC1 PROTEIN; VITRONECTIN RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CARBOXY TERMINAL ACIDIC TAIL; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME ACTIVATION; GENE DELETION; IN VITRO STUDY; IN VIVO STUDY; LUNG ALVEOLUS MACROPHAGE; MACROPHAGE; MALE; MOLECULAR INTERACTION; MOUSE; NEUTROPHIL; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN STRUCTURE; RECEPTOR BINDING;

ANIMALS; APOPTOSIS; HMGB1 PROTEIN; HUMANS; INTEGRIN ALPHAVBETA3; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MITOGEN-ACTIVATED PROTEIN KINASES; NEUTROPHILS; PEPTIDE FRAGMENTS; PHAGOCYTOSIS; PLASMIDS;

MURINAE; MUS;

EID: 78649627022     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0510262     Document Type: Article

References (47)

1. Bianchi, M. E., Agresti, A. (2005) HMG proteins: dynamic players in gene regulation and differentiation. Curr. Opin. Genet. Dev. 15, 496-506.
2. Dumitriu, I. E., Baruah, P., Manfredi, A. A., Bianchi, M. E., Rovere-Querini, P. (2005) HMGB1: guiding immunity from within. Trends Immunol. 26, 381-387.
3. Muller, S., Scaffidi, P., Degryse, B., Bonaldi, T., Ronfani, L., Agresti, A., Beltrame, M., Bianchi, M. E. (2001) New EMBO members' review: the double life of HMGB1 chromatin protein: architectural factor and extracellular signal. EMBO J. 20, 4337-4340.
4. Angus, D. C., Yang, L., Kong, L., Kellum, J. A., Delude, R. L., Tracey, K. J., Weissfeld, L. (2007) Circulating high-mobility group box 1 (HMGB1) concentrations are elevated in both uncomplicated pneumonia and pneumonia with severe sepsis. Crit. Care Med. 35, 1061-1067. (Pubitemid 46598956)
5. Abraham, E., Arcaroli, J., Carmody, A., Wang, H., Tracey, K. J. (2000) HMG-1 as a mediator of acute lung inflammation. J. Immunol. 165, 2950-2954.
6. Wang, H., Bloom, O., Zhang, M., Vishnubhakat, J. M., Ombrellino, M., Che, J., Frazier, A., Yang, H., Ivanova, S., Borovikova, L., Manogue, K. R., Faist, E., Abraham, E., Andersson, J., Andersson, U., Molina, P. E., Abumrad, N. N., Sama, A., Tracey, K. J. (1999) HMG-1 as a late mediator of endotoxin lethality in mice. Science 285, 248-251.
7. 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.
8. Bianchi, M. E. (2009) HMGB1 loves company. J. Leukoc. Biol. 86, 573-576.
9. Hreggvidsdottir, H. S., Ostberg, T., Wahamaa, H., Schierbeck, H., Aveberger, A-C., Klevenvall, L., Palmblad, K., Ottosson, L., Andersson, U., Harris, H. E. (2009) The alarmin HMGB1 acts in synergy with endogenous and exogenous danger signals to promote inflammation. J. Leukoc. Biol. 86, 655-662.
10. Sha, Y., Zmijewski, J., Xu, Z., Abraham, E. (2008) HMGB1 develops enhanced proinflammatory activity by binding to cytokines. J. Immunol. 180, 2531-2537.
11. Rouhiainen, A., Tumova, S., Valmu, L., Kalkkinen, N., Rauvala, H. (2007) Pivotal advance: analysis of proinflammatory activity of highly purified eukaryotic recombinant HMGB1 (amphoterin). J. Leukoc. Biol. 81, 49-58.
12. Tian, J., Avalos, A. M., Mao, S. Y., Chen, B., Senthil, K., Wu, H., Parroche, P., Drabic, S., Golenbock, D., Sirois, C., Hua, J., An, L. L., Audoly, L., La Rosa, G., Bierhaus, A., Naworth, P., Marshak-Rothstein, A., Crow, M. K., Fitzgerald, K. A., Latz, E., Kiener, P. A., Coyle, A. J. (2007) Toll-like receptor 9-dependent activation by DNA-containing immune complexes is mediated by HMGB1 and RAGE. Nat. Immunol. 8, 487-496.
13. Penzo, M., Molteni, R., Suda, T., Samaniego, S., Raucci, A., Habiel, D. M., Miller, F., Jiang, H-P., Li, J., Pardi, R., Palumbo, R., Olivotto, E., Kew, R. R., Bianchi, M. E., Marcu, K. B. (2010) Inhibitor of NK-{κ}B kinases {α} and {β} are both essential for high mobility group box 1-mediated chemotaxis. J. Immunol. 184, 4497-4509.
14. Liu, G., Wang, J., Park, Y. J., Tsuruta, Y., Lorne, E. F., Zhao, X., Abraham, E. (2008) High mobility group protein-1 inhibits phagocytosis of apoptotic neutrophils through binding to phosphatidylserine. J. Immunol. 181, 4240-4246.
15. Nagata, S., Hanayama, R., Kawane, K. (2010) Autoimmunity and the clearance of dead cells. Cell 140, 619-630.
16. Erwig, L-P., Henson, P. M. (2007) Immunological consequences of apoptotic cell phagocytosis. Am. J. Pathol. 171, 2-8.
17. 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.
18. Erlandsson Harris, H., Andersson, U. (2004) Mini-review: the nuclear protein HMGB1 as a proinflammatory mediator. Eur. J. Immunol. 34, 1503-1512.
19. Qin, Y-H., Dai, S-M., Tang, G-S., Zhang, J., Ren, D., Wang, Z-W., Shen, Q. (2009) HMGB1 enhances the proinflammatory activity of lipopolysaccharide by promoting the phosphorylation of MAPK p38 through receptor for advanced glycation end products. J. Immunol. 183, 6244-6250.
20. 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. (Pubitemid 38294612)
21. Wang, H., Ward, M. F., Sama, A. E. (2009) Novel HMGB1-inhibiting therapeutic agents for experimental sepsis. Shock 32, 348-357.
22. Knapp, S., Muller, S., Digilio, G., Bonaldi, T., Bianchi, M. E., Musco, G. (2004) The long acidic tail of high mobility group box 1 (HMGB1) protein forms an extended and flexible structure that interacts with specific residues within and between the HMG boxes. Biochemistry 43, 11992-11997.
23. Guazzi, S., Strangio, A., Franzi, A. T., Bianchi, M. E. (2003) HMGB1, an architectural chromatin protein and extracellular signaling factor, has a spatially and temporally restricted expression pattern in mouse brain. Gene Expr. Patterns 3, 29-33.
24. Schwenger, V., Morath, C., Salava, A., Amann, K., Seregin, Y., Deppisch, R., Ritz, E., Bierhaus, A., Nawroth, P. P., Zeier, M. (2006) Damage to the peritoneal membrane by glucose degradation products is mediated by the receptor for advanced glycation end-products. J. Am. Soc. Nephrol. 17, 199-207.
25. 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.
26. Yum, H. K., Arcaroli, J., Kupfner, J., Shenkar, R., Penninger, J. M., Sasaki, T., Yang, K. Y., Park, J. S., Abraham, E. (2001) Involvement of phosphoinositide 3-kinases in neutrophil activation and the development of acute lung injury. J. Immunol. 167, 6601-6608.
27. Gong, W., Li, Y., Chao, F., Huang, G., He, F. (2009) Amino acid residues 201-205 in C-terminal acidic tail region plays a crucial role in antibacterial activity of HMGB1. J. Biomed. Sci. 16, 83.
28. Watson, M., Stott, K., Thomas, J. O. (2007) Mapping intramolecular interactions between domains in HMGB1 using a tail-truncation approach. J. Mol. Biol. 374, 1286-1297.
29. Mitkova, E., Ugrinova, I., Pashev, I. G., Pasheva, E. A. (2005) The inhibitory effect of HMGB-1 protein on the repair of cisplatin-damaged DNA is accomplished through the acidic domain. Biochemistry 44, 5893-5898. (Pubitemid 40525126)
30. Wu, Y., Tibrewal, N., Birge, R. B. (2006) Phosphatidylserine recognition by phagocytes: a view to a kill. Trends Cell Biol. 16, 189-197.
31. Henson, P. M., Tuder, R. M. (2008) Apoptosis in the lung: induction, clearance and detection. Am. J. Physiol. Lung Cell. Mol. Physiol. 294, L601-L611.
32. Ravichandran, K. S., Lorenz, U. (2007) Engulfment of apoptotic cells: signals for a good meal. Nat. Rev. Immunol. 7, 964-974.
33. Kinchen, J. M., Ravichandran, K. S. (2007) Journey to the grave: signaling events regulating removal of apoptotic cells. J. Cell Sci. 120, 2143-2149.
34. Huttunen, H. J., Fages, C., Kuja-Panula, J., Ridley, A. J., Rauvala, H. (2002) Receptor for advanced glycation end products-binding COOH-terminal motif of amphoterin inhibits invasive migration and metastasis. Cancer Res. 62, 4805-4811.
35. Gong, W., Zheng, Y., Chao, F., Li, Y., Xu, Z., Huang, G., Gao, X., Li, S., He, F. (2010) The anti-inflammatory activity of HMGB1 A box is enhanced when fused with C-terminal acidic tail. J. Biomed. Biotechnol. 2010, 915234.
36. Watson, M., Stott, K., Thomas, J. O. (2007) Mapping intramolecular interactions between domains in HMGB1 using a tail-truncation approach. J. Mol. Biol. 374, 1286-1297.
37. Bergeron, S., Madathiparambil, T., Swanson, P. C. (2005) Both high mobility group (HMG)-boxes and the acidic tail of HMGB1 regulate recombination-activating gene (RAG)-mediated recombination signal synapsis and cleavage in vitro. J. Biol. Chem. 280, 31314-31324.
38. Li, J., Kokkola, R., Tabibzadeh, S., Yang, R., Ochani, M., Qiang, X., Harris, H. E., Czura, C. J., Wang, H., Ulloa, L., Warren, H. S., Moldawer, L. L., Fink, M. P., Andersson, U., Tracey, K. J., Yang, H. (2003) Structural basis for the proinflammatory cytokine activity of high mobility group box 1. Mol. Med. 9, 37-45.
39. Kawase, T., Sato, K., Ueda, T., Yoshida, M. (2008) Distinct domains in HMGB1 are involved in specific intramolecular and nucleosomal interactions. Biochemistry 47, 13991-13996.
40. Wang, Q., Zeng, M., Wang, W., Tang, J. (2007) The HMGB1 acidic tail regulates HMGB1 DNA binding specificity by a unique mechanism. Biochem. Biophys. Res. Commun. 360, 14-19.
41. Pasheva, E., Sarov, M., Bidjekov, K., Ugrinova, I., Sarg, B., Lindner, H., Pashev, I. G. (2004) In vitro acetylation of HMGB-1 and -2 proteins by CBP: the role of the acidic tail. Biochemistry 43, 2935-2940.
42. Agresti, A., Lupo, R., Bianchi, M. E., Muller, S. (2003) HMGB1 interacts differentially with members of the Rel family of transcription factors. Biochem. Biophys. Res. Commun. 302, 421-426. (Pubitemid 36397940)
43. Dumitriu, I. E., Bianchi, M. E., Bacci, M., Manfredi, A. A., Rovere-Querini, P. (2007) The secretion of HMGB1 is required for the migration of maturing dendritic cells. J. Leukoc. Biol. 81, 84-91.
44. 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.
45. Suda, K., Kitagawa, Y., Ozawa, S., Saikawa, Y., Ueda, M., Ebina, M., Yamada, S., Hashimoto, S., Fukata, S., Abraham, E., Maruyama, I., Kitajima, M., Ishizaka, A. (2006) Anti-high-mobility group box chromosomal protein 1 antibodies improve survival of rats with sepsis. World J. Surg. 30, 1755-1762.
46. Kim, J. Y., Park, J. S., Strassheim, D., Douglas, I., Diaz Del Valle, F., Asehnoune, K., Mitra, S., Kwak, S. H., Yamada, S., Maruyama, I., Ishizaka, A., Abraham, E. (2005) HMGB1 contributes to the development of acute lung injury after hemorrhage. Am. J. Physiol. Lung Cell. Mol. Physiol. 288, L958-L965.
47. Rowe, S. M., Jackson, P. L., Liu, G., Hardison, M., Livraghi, A., Solomon, G. M., McQuaid, D. B., Noerager, B. D., Gaggar, A., Clancy, J. P., O'Neal, W., Sorscher, E. J., Abraham, E., Blalock, J. E. (2008) Potential role of high-mobility group box 1 in cystic fibrosis airway disease. Am. J. Respir. Crit. Care Med. 178, 822-831.