CD163 binding to haptoglobin-hemoglobin complexes involves a dual-point electrostatic receptor-ligand pairing

Journal of Biological Chemistry

Volumn 288, Issue 26, 2013, Pages 18834-18841

  Nielsen, Marianne Jensby ^a   Andersen, Christian Brix Folsted ^a   Moestrup, Søren Kragh ^a,b  

^a AARHUS UNIVERSITY   (Denmark)

^b AARHUS UNIVERSITY HOSPITAL   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ACIDIC AMINO ACIDS; CONSENSUS MOTIF; HIGH AFFINITY BINDING; HUMAN PLASMAS; LIGAND-BINDING SITES; RECEPTOR LIGANDS; SCAVENGER RECEPTOR; SITE DIRECTED MUTAGENESIS;

AMINO ACIDS; CALCIUM; HEMOGLOBIN; LIGANDS;

ELECTROSTATICS;

CD163 ANTIGEN; HAPTOGLOBIN; HEMOGLOBIN;

ANTIBODY AFFINITY; ANTIGEN BINDING; ARTICLE; BINDING AFFINITY; BINDING SITE; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENDOCYTOSIS; GENE MUTATION; HUMAN; HUMAN CELL; LIGAND BINDING; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RECEPTOR BINDING; SEQUENCE ALIGNMENT; SITE DIRECTED MUTAGENESIS; STATIC ELECTRICITY;

CALCIUM-BINDING PROTEINS; HEMOGLOBIN; LIGAND-BINDING PROTEIN; RECEPTOR ENDOCYTOSIS; SCAVENGER RECEPTOR;

AMINO ACID SEQUENCE; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION, MYELOMONOCYTIC; BINDING SITES; CALCIUM; HAPTOGLOBINS; HEK293 CELLS; HEMOGLOBINS; HEMOLYSIS; HUMANS; IONS; LIGANDS; METALS; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; PROTEIN BINDING; RECEPTORS, CELL SURFACE; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; STATIC ELECTRICITY; SURFACE PLASMON RESONANCE;

EID: 84879345382     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.471060     Document Type: Article

References (33)

1. Kristiansen, M., Graversen, J. H., Jacobsen, C., Sonne, O., Hoffman, H. J., Law, S. K., and Moestrup, S. K. (2001) Identification of the haemoglobin scavenger receptor. Nature 409, 198-201 (Pubitemid 32144285)
2. Hwang, P. K., and Greer, J. (1980) Interaction between hemoglobin subunits in the hemoglobin-haptoglobin complex. J. Biol. Chem. 255, 3038-3041 (Pubitemid 10089257)
3. Andersen, C. B., Torvund-Jensen, M., Nielsen, M. J., de Oliveira, C. L., Hersleth, H. P., Andersen, N. H., Pedersen, J. S., Andersen, G. R., and Moestrup, S. K. (2012) Structure of the haptoglobin-haemoglobin complex. Nature 489, 456-459
4. Buehler, P. W., Abraham, B., Vallelian, F., Linnemayr, C., Pereira, C. P., Cipollo, J. F., Jia, Y., Mikolajczyk, M., Boretti, F. S., Schoedon, G., Alayash, A. I., and Schaer, D. J. (2009) Haptoglobin preserves the CD163 hemoglobin scavenger pathway by shielding hemoglobin from peroxidative modification. Blood 113, 2578-2586
5. Lim, S. K., Kim, H., Lim, S. K., bin Ali, A., Lim, Y. K., Wang, Y., Chong, S. M., Costantini, F., and Baumman, H. (1998) Increased susceptibility in Hp knockout mice during acute hemolysis. Blood 92, 1870-1877 (Pubitemid 28446675)
6. Sadrzadeh, S. M., Graf, E., Panter, S. S., Hallaway, P. E., and Eaton, J. W. (1984) Hemoglobin: a biologic Fenton reagent. J. Biol. Chem. 259, 14354-14356
7. Etzerodt, A., and Moestrup, S. K. (2013) CD163 and inflammation: biological, diagnostic, and therapeutic aspects. Antioxid. Redox Signal. 18, 2352-2363
8. Nielsen, M. J., and Moestrup, S. K. (2009) Receptor targeting of hemoglobin mediated by the haptoglobins: roles beyond heme scavenging. Blood 114, 764-771
9. Nielsen, M. J., Moller, H. J., and Moestrup, S. K. (2010) Hemoglobin and heme scavenger receptors. Antioxid. Redox Signal. 12, 261-273
10. Martínez, V. G., Moestrup, S. K., Holmskov, U., Mollenhauer, J., and Lozano, F. (2011) The conserved scavenger receptor cysteine-rich superfamily in therapy and diagnosis. Pharmacol. Rev. 63, 967-1000
11. Law, S. K., Micklem, K. J., Shaw, J. M., Zhang, X. P., Dong, Y., Willis, A. C., and Mason, D. Y. (1993) A new macrophage differentiation antigen which is a member of the scavenger receptor superfamily. Eur. J. Immunol. 23, 2320-2325 (Pubitemid 23265900)
12. Greer, J. (1980) Model for haptoglobin heavy-chain based upon structural homology. Proc. Natl. Acad. Sci. U.S.A. 77, 3393-3397
13. Kurosky, A., Barnett, D. R., Rasco, M. A., Lee, T. H., and Bowman, B. H. (1974) Evidence of homology between β-chain of human haptoglobin and chymotrypsin family of serine proteases. Biochem. Genet. 11, 279-293
14. Kurosky, A., Barnett, D. R., Lee, T. H., Touchstone, B., Hay, R. E., Arnott, M. S., Bowman, B. H., and Fitch, W. M. (1980) Covalent structure of human haptoglobin: a serine protease homolog. Proc. Natl. Acad. Sci. U.S.A. 77, 3388-3392 (Pubitemid 10012242)
15. Bensi, G., Raugei, G., Klefenz, H., and Cortese, R. (1985) Structure and expression of the human haptoglobin locus. EMBO J. 4, 119-126
16. Maeda, N., Yang, F., Barnett, D. R., Bowman, B. H., and Smithies, O. (1984) Duplication within the haptoglobin Hp2 gene. Nature 309, 131-135 (Pubitemid 14142780)
17. Maeda, N. (1985) Nucleotide sequence of the haptoglobin and haptoglobin-related gene pair: the haptoglobin-related gene contains a retroviruslike element. J. Biol. Chem. 260, 6698-6709
18. Nielsen, M. J., Petersen, S. V., Jacobsen, C., Oxvig, C., Rees, D., Møller, H. J., and Moestrup, S. K. (2006) Haptoglobin-related protein is a high-affinity hemoglobin-binding plasma protein. Blood 108, 2846-2849
19. Madsen, M., Møller, H. J., Nielsen, M. J., Jacobsen, C., Graversen, J. H., van den Berg, T., and Moestrup, S. K. (2004) Molecular characterization of the haptoglobin-hemoglobin receptor CD163: ligand binding properties of the scavenger receptor cysteine-rich domain region. J. Biol. Chem. 279, 51561-51567
20. Nielsen, M. J., Petersen, S. V., Jacobsen, C., Thirup, S., Enghild, J. J., Graversen, J. H., and Moestrup, S. K. (2007) A unique loop extension in the serine protease domain of haptoglobin is essential for CD163 recognition of the haptoglobin-hemoglobin complex. J. Biol. Chem. 282, 1072-1079 (Pubitemid 47076555)
21. Schaer, D. J., Schaer, C. A., Buehler, P. W., Boykins, R. A., Schoedon, G., Alayash, A. I., and Schaffner, A. (2006) CD163 is the macrophage scavenger receptor for native and chemically modified hemoglobins in the absence of haptoglobin. Blood 107, 373-380 (Pubitemid 43053566)
22. Etzerodt, A., Kjolby, M., Nielsen, M. J., Maniecki, M., Svendsen, P., and Moestrup, S. K. (2013) Plasma clearance of hemoglobin and haptoglobin in mice and effect of CD163 gene targeting disruption. Antioxid. Redox Signal. 18, 2254-2263
23. Ojala, J. R., Pikkarainen, T., Tuuttila, A., Sandalova, T., and Tryggvason, K. (2007) Crystal structure of the cysteine-rich domain of scavenger receptor MARCO reveals the presence of a basic and an acidic cluster that both contribute to ligand recognition. J. Biol. Chem. 282, 16654-16666 (Pubitemid 47100358)
24. Andersen, C. B., Madsen, M., Storm, T., Moestrup, S. K., and Andersen, G. R. (2010) Structural basis for receptor recognition of vitamin B12-intrinsic factor complexes. Nature 464, 445-448
25. Gerasimenko, J. V., Tepikin, A. V., Petersen, O. H., and Gerasimenko, O. V. (1998) Calcium uptake via endocytosis with rapid release from acidifying endosomes. Curr. Biol. 8, 1335-1338 (Pubitemid 29006710)
26. Fisher, C., Beglova, N., and Blacklow, S. C. (2006) Structure of an LDLR-RAP complex reveals a general mode for ligand recognition by lipoprotein receptors. Mol. Cell 22, 277-283
27. Møller, H. J., Nielsen, M. J., Maniecki, M. B., Madsen, M., and Moestrup, S. K. (2010) Soluble macrophage-derived CD163: a homogeneous ectodomain protein with a dissociable haptoglobin-hemoglobin binding. Immunobiology 215, 406-412
28. Nielsen, M. J., Nielsen, L. B., and Moestrup, S. K. (2006) High-density lipoprotein and innate immunity. Fut. Lipidol. 1, 729-734
29. Gronlund, J., Vitved, L., Lausen, M., Skjodt, K., and Holmskov, U. (2000) Cloning of a novel scavenger receptor cysteine-rich type I transmembrane molecule (M160) expressed by human macrophages. J. Immunol. 165, 6406-6415
30. Van Gorp, H., Delputte, P. L., and Nauwynck, H. J. (2010) Scavenger receptor CD163, a Jack-of-all-trades and potential target for cell-directed therapy. Mol. Immunol. 47, 1650-1660
31. Fabriek, B. O., Polfliet, M. M., Vloet, R. P., van der Schors, R. C., Ligtenberg, A. J., Weaver, L. K., Geest, C., Matsuno, K., Moestrup, S. K., Dijkstra, C. D., and van den Berg, T. K. (2007) The macrophage CD163 surface glycoprotein is an erythroblast adhesion receptor. Blood 109, 5223-5229 (Pubitemid 46890540)
32. Fabriek, B. O., van Bruggen, R., Deng, D. M., Ligtenberg, A. J., Nazmi, K., Schornagel, K., Vloet, R. P., Dijkstra, C. D., and van den Berg, T. K. (2009) The macrophage scavenger receptor CD163 functions as an innate immune sensor for bacteria. Blood 113, 887-892
33. Moeller, J. B., Nielsen, M. J., Reichhardt, M. P., Schlosser, A., Sorensen, G. L., Nielsen, O., Tornøe, I., Grønlund, J., Nielsen, M. E., Jørgensen, J. S., Jensen, O. N., Mollenhauer, J., Moestrup, S. K., and Holmskov, U. (2012) CD163-L1 is an endocytic macrophage protein strongly regulated by mediators in the inflammatory response. J. Immunol. 188, 2399-2409