Biomolecules & Therapeutics

The Korean Society of Applied Pharmacology (한국응용약물학회)
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A Pattern Recognition Receptor, SIGN-R1, Mediates ROS Generation against Polysaccharide Dextran, Resulting in Increase of Peroxiredoxin-1 and Its Interaction to SIGN-R1

  • Choi, Heong-Jwa (Department of Biomedical Science & Technology, Institute of Biomedical Science & Technology, Konkuk University) ;
  • Choi, Woo-Sung (Department of Biomedical Science & Technology, Institute of Biomedical Science & Technology, Konkuk University) ;
  • Park, Jin-Yeon (Department of Biomedical Science & Technology, Institute of Biomedical Science & Technology, Konkuk University) ;
  • Kang, Kyeong-Hyeon (Department of Biomedical Science & Technology, Institute of Biomedical Science & Technology, Konkuk University) ;
  • Prabagar, Miglena G. (Department of Biomedical Science & Technology, Institute of Biomedical Science & Technology, Konkuk University) ;
  • Shin, Chan-Young (Department of Pharmacology, School of Medicine, Konkuk University) ;
  • Kang, Young-Sun (Department of Biomedical Science & Technology, Institute of Biomedical Science & Technology, Konkuk University)
  • Received : 2010.06.01
  • Accepted : 2010.07.02
  • Published : 2010.07.31
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Abstract

Streptococcus pneumoniae is the major pathogen that frequently causes serious infections in children, the elderly and immunocompromised patients. S. pneumoniae is known to produce reactive oxygen species (ROS) and S. pneumoniae-produced ROS is considered to play a role in pneumococci pathogenesis. SIGN-R1 is the principal receptor of capsular polysaccharides (CPSs) of S. pneumoniae. However, there is a considerable lack of knowledge about the protective role of SIGN-R1 against S. pneumoniae-produced ROS in SIGN-$R1^+$ macrophages. While investigating the protective role of SIGN-R1 against ROS, we found that SIGN-R1 intimately bound to peroxiredoxin-1 (Prx-1), one of small antioxidant proteins in vitro and in vivo. This interaction was increased with ROS generation which was produced by stimulating SIGN-R1 with dextran, a polysaccharide ligand of SIGN-R1. Also, SIGN-R1 crosslinking with 22D1 anti-SIGN-R1 antibody increased Prx-1 in vitro or in vivo. These results suggested that SIGN-R1 stimulation with CPSs of S. pneumoniae increase the expression level of Prx-1 through ROS and its subsequent interaction to SIGN-R1, providing an important antioxidant role for the host protection against S. pneumoniae.

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References

  1. Brown, G. D. and Gordon, S. (2001). Immune recognition. A new receptor for beta-glucans. Nature 413, 36-37.
  2. Bryk, R., Griffin, P. and Nathan, C. (2000). Peroxynitrite reductase activity of bacterial peroxiredoxins. Nature 407, 211-215. https://doi.org/10.1038/35025109
  3. Chae, H. Z., Kim, I. H., Kim, K. and Rhee, S. G. (1993). Cloning, sequencing, and mutation of thiol-specific antioxidant gene of Saccharomyces cerevisiae. J. Biol. Chem. 268, 16815-16821.
  4. Chandel, N. S., Schumacker, P. T. and Arch, R. H. (2001).Reactive oxygen species are downstream products of TRAF-mediatedsignal transduction. J. Biol. Chem. 276, 42728-42736. https://doi.org/10.1074/jbc.M103074200
  5. Conway, J. P. and Kinter, M. (2006). Dual role of peroxiredoxin I in macrophage-derived foam cells. J. Biol. Chem. 281, 27991-28001. https://doi.org/10.1074/jbc.M605026200
  6. Farnell, M. B., Crippen, T. L., He, H., Swaggerty, C. L. andKogut, M. H. (2003). Oxidative burst mediated by toll like receptors (TLR) and CD14 on avian heterophils stimulated with bacterial toll agonists. Dev. Comp. Immunol. 27,423-429. https://doi.org/10.1016/S0145-305X(02)00115-5
  7. Feinberg, H., Mitchell, D. A., Drickamer, K. and Weis, W. I.(2001). Structural basis for selective recognition of oligosaccharides by DC-SIGN and DC-SIGNR. Science 294, 2163-2166. https://doi.org/10.1126/science.1066371
  8. Finch, R. (2001). Community-acquired pneumonia: the evolving challenge. Clin. Microbiol. Infect. 7(Suppl 3), 30-38. https://doi.org/10.1046/j.1469-0691.2001.00052.x
  9. Fu, H., Karlsson, J., Bylund, J., Movitz, C., Karlsson, A. andDahlgren, C. (2006). Ligand recognition and activation of formyl peptide receptors in neutrophils. J. Leukoc. Biol. 79, 247- 256. https://doi.org/10.1189/jlb.0905498
  10. Fujii, J. and Ikeda, Y. (2002). Advances in our understanding of peroxiredoxin, a multifunctional, mammalian redox protein.Redox. Rep. 7, 123-130. https://doi.org/10.1179/135100002125000352
  11. Gantner, B. N., Simmons, R. M. and Underhill, D. M. (2005).Dectin-1 mediates macrophage recognition of Candida albicans yeast but not filaments. EMBO J. 24, 1277-1286. https://doi.org/10.1038/sj.emboj.7600594
  12. Geijtenbeek, T. B., Groot, P. C., Nolte, M. A., van Vliet, S. J.,Gangaram-Panday, S. T., van Duijnhoven, G. C., Kraal, G.,van Oosterhout, A. J. and van Kooyk, Y. (2002). Marginal zone macrophages express a murine homologue of DC-SIGN that captures blood-borne antigens in vivo. Blood 100, 2908-2916. https://doi.org/10.1182/blood-2002-04-1044
  13. Guzik, T. J. and Harrison, D. G. (2006). Vascular NADPH oxidases as drug targets for novel antioxidant strategies. Drug Discov. Today 11, 524-533. https://doi.org/10.1016/j.drudis.2006.04.003
  14. Hellstrand, K., Asea, A., Dahlgren, C. and Hermodsson, S. (1994).Histaminergic regulation of NK cells. Role of monocytederived reactive oxygen metabolites. J. Immunol. 153, 4940-4947.
  15. Hofmann, B., Hecht, H. J. and Flohe, L. (2002). Peroxiredoxins.Biol. Chem. 383, 347-364. https://doi.org/10.1515/BC.2002.040
  16. Hultqvist, M. and Holmdahl, R. (2005). Ncf1 (p47phox) polymorphism determines oxidative burst and the severity of arthritis in rats and mice. Cell. Immunol. 233, 97-101. https://doi.org/10.1016/j.cellimm.2005.04.008
  17. Jackson, S. H., Devadas, S., Kwon, J., Pinto, L. A. and Williams,M.S. (2004). T cells express a phagocyte-type NADPH oxidase that is activated after T cell receptor stimulation. Nat. Immunol. 5, 818-827. https://doi.org/10.1038/ni1096
  18. Jung, K. C., Park, W. S., Kim, H. J., Choi, E. Y., Kook, M. C.,Lee, H. W. and Bae, Y. (2004). TCR-independent and caspaseindependent apoptosis of murine thymocytes by CD24 cross-linking. J. Immunol. 172, 795-802. https://doi.org/10.4049/jimmunol.172.2.795
  19. Kang, S. W., Chae, H. Z., Seo, M. S., Kim, K., Baines, I. C. andRhee, S. G. (1998). Mammalian peroxiredoxin isoforms can reduce hydrogen peroxide generated in response to growth factors and tumor necrosis factor-alpha. J. Biol. Chem. 273,6297-6302. https://doi.org/10.1074/jbc.273.11.6297
  20. Kang, Y. S., Do, Y., Lee, H. K., Park, S. H., Cheong, C., Lynch,R. M., Loeffler, J. M., Steinman, R. M. and Park, C. G.(2006). A dominant complement fixation pathway for pneumococcal polysaccharides initiated by SIGN-R1 interacting with C1q. Cell 125, 47-58. https://doi.org/10.1016/j.cell.2006.01.046
  21. Kang, Y. S., Kim, J. Y., Bruening, S. A., Pack, M., Charalambous,A., Pritsker, A., Moran, T. M., Loeffler, J. M., Steinman,R. M. and Park, C. G. (2004). The C-type lectin SIGN-R1 mediates uptake of the capsular polysaccharide of Streptococcus pneumoniae in the marginal zone of mouse spleen.Proc. Natl. Acad. Sci. U S A 101, 215-220. https://doi.org/10.1073/pnas.0307124101
  22. Kang, Y. S., Yamazaki, S., Iyoda, T., Pack, M., Bruening, S. A.,Kim, J. Y., Takahara, K., Inaba, K., Steinman, R. M. and Park,C. G. (2003). SIGN-R1, a novel C-type lectin expressed by marginal zone macrophages in spleen, mediates uptake of the polysaccharide dextran. Int. Immunol. 15, 177-186. https://doi.org/10.1093/intimm/dxg019
  23. Kim, H., Lee, T. H., Park, E. S., Suh, J. M., Park, S. J., Chung,H. K., Kwon, O. Y., Kim, Y. K., Ro, H. K. and Shong, M. (2000).Role of peroxiredoxins in regulating intracellular hydrogen peroxide and hydrogen peroxide-induced apoptosis in thyroid cells. J. Biol. Chem. 275, 18266-18270. https://doi.org/10.1074/jbc.275.24.18266
  24. Klein, M., Koedel, U. and Pfister, H. W. (2006). Oxidative stress in pneumococcal meningitis: a future target for adjunctive therapy? Prog. Neurobiol. 80, 269-280. https://doi.org/10.1016/j.pneurobio.2006.11.008
  25. Koppel, E. A., Ludwig, I. S., Appelmelk, B. J., van Kooyk, Y. andGeijtenbeek, T. B. (2005a). Carbohydrate specificities of the murine DC-SIGN homologue mSIGNR1. Immunobiology210, 195-201. https://doi.org/10.1016/j.imbio.2005.05.012
  26. Koppel, E. A., Wieland, C. W., van den Berg, V. C., Litjens, M.,Florquin, S., van Kooyk, Y., van der Poll, T. and Geijtenbeek,T. B. (2005b). Specific ICAM-3 grabbing nonintegrin-related 1 (SIGNR1) expressed by marginal zone macrophages is essential for defense against pulmonary Streptococcus pneumoniae infection. Eur. J. Immunol. 35, 2962-2969. https://doi.org/10.1002/eji.200526216
  27. Lanoue, A., Clatworthy, M. R., Smith, P., Green, S., Townsend,M. J., Jolin, H. E., Smith, K. G., Fallon, P. G. and McKenzie,A. N. (2004). SIGN-R1 contributes to protection against lethal pneumococcal infection in mice. J. Exp. Med. 200, 1383-1393. https://doi.org/10.1084/jem.20040795
  28. Martner, A., Dahlgren, C., Paton, J. C. and Wold, A. E. (2008).Pneumolysin released during Streptococcus pneumoniae autolysis is a potent activator of intracellular oxygen radical production in neutrophils. Infection. Immun. 76, 4079-4087. https://doi.org/10.1128/IAI.01747-07
  29. Mitsumoto, A., Takanezawa, Y., Okawa, K., Iwamatsu, A. andNakagawa, Y. (2001). Variants of peroxiredoxins expression in response to hydroperoxide stress. Free Radic. Biol. Med.30, 625-635. https://doi.org/10.1016/S0891-5849(00)00503-7
  30. Moens, L., Jeurissen, A., Wuyts, G., Fallon, P. G., Louis, B.,Ceuppens, J. L. and Bossuyt, X. (2007). Specific intracellular adhesion molecule-grabbing nonintegrin R1 is not involved in the murine antibody response to pneumococcal polysaccharides. Infection. Immun. 75, 5748-5752. https://doi.org/10.1128/IAI.00574-07
  31. Mollnes, T. E., Brekke, O. L., Fung, M., Fure, H., Christiansen,D., Bergseth, G., Videm, V., Lappegard, K. T., Kohl, J. andLambris, J. D. (2002). Essential role of the C5a receptor in E coli-induced oxidative burst and phagocytosis revealed by a novel lepirudin-based human whole blood model of inflammation. Blood 100, 1869-1877.
  32. Musher, D. M. (1992). Infections caused by Streptococcus pneumoniae:clinical spectrum, pathogenesis, immunity, and treatment. Clin. Infect. Dis. 14, 801-807. https://doi.org/10.1093/clinids/14.4.801
  33. Neumann, C. A., Krause, D. S., Carman, C. V., Das, S., Dubey,D. P., Abraham, J. L., Bronson, R. T., Fujiwara, Y., Orkin, S.H. and Van Etten, R. A. (2003). Essential role for the peroxiredoxin Prdx1 in erythrocyte antioxidant defence and tumour suppression. Nature 424, 561-565. https://doi.org/10.1038/nature01819
  34. Olofsson, P., Holmberg, J., Pettersson, U. and Holmdahl, R.(2003). Identification and isolation of dominant susceptibility loci for pristane-induced arthritis. J. Immunol. 171, 407-416. https://doi.org/10.4049/jimmunol.171.1.407
  35. Phillips, R., Svensson, M., Aziz, N., Maroof, A., Brown, N.,Beattie, L., Signoret, N. and Kaye, P. M. (2010). Innate killing of Leishmania donovani by macrophages of the splenic marginal zone requires IRF-7. PLoS Pathog. 6, e1000813. https://doi.org/10.1371/journal.ppat.1000813
  36. Rhee, S. G., Chae, H. Z. and Kim, K. (2005). Peroxiredoxins: a historical overview and speculative preview of novel mechanisms and emerging concepts in cell signaling. Free Radic. Biol. Med. 38, 1543-1552. https://doi.org/10.1016/j.freeradbiomed.2005.02.026
  37. Rhee, S. G., Kang, S. W., Chang, T. S., Jeong, W. and Kim, K. (2001). Peroxiredoxin, a novel family of peroxidases. IUBMB Life 52, 35-41. https://doi.org/10.1080/15216540252774748
  38. Saunders, S. P., Barlow, J. L., Walsh, C. M., Bellsoi, A., Smith,P., McKenzie, A. N. and Fallon, P. G. (2010). C-type lectin SIGN-R1 has a role in experimental colitis and responsiveness to lipopolysaccharide. J. Immunol. 184, 2627-2637. https://doi.org/10.4049/jimmunol.0901970
  39. Schreibelt, G., van Horssen, J., Haseloff, R. F., Reijerkerk, A.,van der Pol, S. M., Nieuwenhuizen, O., Krause, E., Blasig, I.E., Dijkstra, C. D., Ronken, E. and De Vries, H. E. (2008).Protective effects of peroxiredoxin-1 at the injured bloodbrain barrier. Free Radic. Biol. Med. 45, 256-264. https://doi.org/10.1016/j.freeradbiomed.2008.03.024
  40. Segal, A. W. (2005). How neutrophils kill microbes. Ann. Rev. Immunol. 23, 197-223. https://doi.org/10.1146/annurev.immunol.23.021704.115653
  41. Steele, C., Marrero, L., Swain, S., Harmsen, A. G., Zheng, M.,Brown, G. D., Gordon, S., Shellito, J. E. and Kolls, J. K.(2003). Alveolar macrophage-mediated killing of Pneumocystis carinii f. sp. muris involves molecular recognition by the Dectin-1 beta-glucan receptor. J. Exp. Med. 198, 1677-1688. https://doi.org/10.1084/jem.20030932
  42. Waddell, T. K., Fialkow, L., Chan, C. K., Kishimoto, T. K. andDowney, G. P. (1994). Potentiation of the oxidative burst of human neutrophils. A signaling role for L-selectin. J. Biol. Chem. 269, 18485-18491.
  43. Wen, S. T. and Van Etten, R. A. (1997). The PAG gene product, a stress-induced protein with antioxidant properties, is an Abl SH3-binding protein and a physiological inhibitor of c-Abl tyrosine kinase activity. Genes Dev. 11, 2456- 2467. https://doi.org/10.1101/gad.11.19.2456

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