Factor H-related protein 5 interacts with pentraxin 3 and the extracellular matrix and modulates complement activation

Journal of Immunology

Volumn 194, Issue 10, 2015, Pages 4963-4973

  Csincsi, Ádám I ^a   Kopp, Anne ^b   Zöldi, Miklós ^a   Bánlaki, Zsófia ^a   Uzonyi, Barbara ^a   Hebecker, Mario ^a   Caesar, Joseph J E ^c   Pickering, Matthew C ^d   Daigo, Kenji ^e   Hamakubo, Takao ^e   Lea, Susan M ^c   De Jorge, Elena Goicoechea ^d   Józsi, Mihály ^a,b  

^a EÖTVÖS LORÁND UNIVERSITY   (Hungary)

^b HANS KNÖLL INSTITUTE   (Germany)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d IMPERIAL COLLEGE LONDON   (United Kingdom)

^e UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALTERNATIVE COMPLEMENT PATHWAY C3 C5 CONVERTASE; COMPLEMENT COMPONENT C1Q; COMPLEMENT FACTOR; FACTOR H RELATED PROTEIN 5; PENTRAXIN 3; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; C REACTIVE PROTEIN; COMPLEMENT; FHR5 PROTEIN, HUMAN; LIGAND; PROTEIN BINDING; SERUM AMYLOID P;

ARTICLE; BINDING AFFINITY; BINDING COMPETITION; BINDING SITE; COMPLEMENT ACTIVATION; CONTROLLED STUDY; EXTRACELLULAR MATRIX; GLOMERULOPATHY; HUMAN; HUMAN CELL; IMMUNOMODULATION; IMMUNOPATHOGENESIS; IN VITRO STUDY; LIGAND BINDING; PLASMA; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; METABOLISM; PHYSIOLOGY;

C-REACTIVE PROTEIN; COMPLEMENT ACTIVATION; COMPLEMENT SYSTEM PROTEINS; EXTRACELLULAR MATRIX; HUMANS; LIGANDS; PROTEIN BINDING; RECOMBINANT PROTEINS; SERUM AMYLOID P-COMPONENT;

EID: 84929095857     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1403121     Document Type: Article

References (54)

1. McRae, J. L., P. J. Cowan, D. A. Power, K. I. Mitchelhill, B. E. Kemp, B. P. Morgan, and B. F. Murphy. 2001. Human factor H-related protein 5 (FHR-5). A new complement-associated protein. J. Biol. Chem. 276: 6747-6754.
2. Józsi, M., and P. F. Zipfel. 2008. Factor H family proteins and human diseases. Trends Immunol. 29: 380-387.
3. Skerka, C., Q. Chen, V. Fremeaux-Bacchi, and L. T. Roumenina. 2013. Complement factor H related proteins (CFHRs). Mol. Immunol. 56: 170-180.
4. McRae, J. L., T. G. Duthy, K. M. Griggs, R. J. Ormsby, P. J. Cowan, B. A. Cromer, W. J. McKinstry, M. W. Parker, B. F. Murphy, and D. L. Gordon. 2005. Human factor H-related protein 5 has cofactor activity, inhibits C3 convertase activity, binds heparin and C-reactive protein, and associates with lipoprotein. J. Immunol. 174: 6250-6256.
5. Murphy, B. F., and A. J. d'Apice. 1988. Identification of the components of glomerular immune deposits using monoclonal antibodies. Pathology 20: 130-136.
6. Murphy, B., T. Georgiou, D. Machet, P. Hill, and J. McRae. 2002. Factor H-related protein-5: a novel component of human glomerular immune deposits. Am. J. Kidney Dis. 39: 24-27.
7. Abrera-Abeleda, M. A., C. Nishimura, J. L. Smith, S. Sethi, J. L. McRae, B. F. Murphy, G. Silvestri, C. Skerka, M. Józsi, P. F. Zipfel, et al. 2006. Variations in the complement regulatory genes factor H (CFH) and factor H related 5 (CFHR5) are associated with membranoproliferative glomerulonephritis type II (dense deposit disease). J. Med. Genet. 43: 582-589.
8. Monteferrante, G., S. Brioschi, J. Caprioli, G. Pianetti, P. Bettinaglio, E. Bresin, G. Remuzzi, and M. Noris. 2007. Genetic analysis of the complement factor H related 5 gene in haemolytic uraemic syndrome. Mol. Immunol. 44: 1704-1708.
9. Westra, D., K. A. Vernon, E. B. Volokhina, M. C. Pickering, N. C. van de Kar, and L. P. van den Heuvel. 2012. Atypical hemolytic uremic syndrome and genetic aberrations in the complement factor H-related 5 gene. J. Hum. Genet. 57: 459-464.
10. Gale, D. P., E. G. de Jorge, H. T. Cook, R. Martinez-Barricarte, A. Hadjisavvas, A. G. McLean, C. D. Pusey, A. Pierides, K. Kyriacou, Y. Athanasiou, et al. 2010. Identification of a mutation in complement factor H-related protein 5 in patients of Cypriot origin with glomerulonephritis. Lancet 376: 794-801.
11. Goicoechea de Jorge, E., J. J. Caesar, T. H. Malik, M. Patel, M. Colledge, S. Johnson, S. Hakobyan, B. P. Morgan, C. L. Harris, M. C. Pickering, and S. M. Lea. 2013. Dimerization of complement factor H-related proteins modulates complement activation in vivo. Proc. Natl. Acad. Sci. USA 110: 4685-4690.
12. Tortajada, A., H. Yébenes, C. Abarrategui-Garrido, J. Anter, J. M. García-Fernández, R. Martínez-Barricarte, M. Alba-Domínguez, T. H. Malik, R. Bedoya, R. Cabrera Pérez, et al. 2013. C3 glomerulopathy-associated CFHR1 mutation alters FHR oligomerization and complement regulation. J. Clin. Invest. 123: 2434-2446.
13. Chen, Q., M. Wiesener, H. U. Eberhardt, A. Hartmann, B. Uzonyi, M. Kirschfink, K. Amann, M. Buettner, T. Goodship, C. Hugo, et al. 2014. Complement factor H-related hybrid protein deregulates complement in dense deposit disease. J. Clin. Invest. 124: 145-155.
14. Bottazzi, B., A. Doni, C. Garlanda, and A. Mantovani. 2010. An integrated view of humoral innate immunity: pentraxins as a paradigm. Annu. Rev. Immunol. 28: 157-183.
15. Jarva, H., T. S. Jokiranta, J. Hellwage, P. F. Zipfel, and S. Meri. 1999. Regulation of complement activation by C-reactive protein: targeting the complement inhibitory activity of factor H by an interaction with short consensus repeat domains 7 and 8-11. J. Immunol. 163: 3957-3962.
16. Mihlan, M., M. Hebecker, H. M. Dahse, S. Hälbich, M. Huber-Lang, R. Dahse, P. F. Zipfel, and M. Józsi. 2009. Human complement factor H-related protein 4 binds and recruits native pentameric C-reactive protein to necrotic cells. Mol. Immunol. 46: 335-344.
17. Hakobyan, S., C. L. Harris, C. W. van den Berg, M. C. Fernandez-Alonso, E. G. de Jorge, S. R. de Cordoba, G. Rivas, P. Mangione, M. B. Pepys, and B. P. Morgan. 2008. Complement factor H binds to denatured rather than to native pentameric C-reactive protein. J. Biol. Chem. 283: 30451-30460.
18. Okemefuna, A. I., R. Nan, A. Miller, J. Gor, and S. J. Perkins. 2010. Complement factor H binds at two independent sites to C-reactive protein in acute phase concentrations. J. Biol. Chem. 285: 1053-1065.
19. Hammond, D. J., Jr., S. K. Singh, J. A. Thompson, B. W. Beeler, A. E. Rusiñol, M. K. Pangburn, L. A. Potempa, and A. Agrawal. 2010. Identification of acidic pH-dependent ligands of pentameric C-reactive protein. J. Biol. Chem. 285: 36235-36244.
20. Singh, S. K., A. Thirumalai, D. J. Hammond, Jr., M. K. Pangburn, V. K. Mishra, D. A. Johnson, A. E. Rusiñol, and A. Agrawal. 2012. Exposing a hidden functional site of C-reactive protein by site-directed mutagenesis. J. Biol. Chem. 287: 3550-3558.
21. Deban, L., S. Jaillon, C. Garlanda, B. Bottazzi, and A. Mantovani. 2011. Pentraxins in innate immunity: lessons from PTX3. Cell Tissue Res. 343: 237-249.
22. Woo, J. M., M. Y. Kwon, D. Y. Shin, Y. H. Kang, N. Hwang, and S. W. Chung. 2013. Human retinal pigment epithelial cells express the long pentraxin PTX3. Mol. Vis. 19: 303-310.
23. Daigo, K., A. Mantovani, and B. Bottazzi. 2014. The yin-yang of long pentraxin PTX3 in inflammation and immunity. Immunol. Lett. 161: 38-43.
24. Inforzato, A., C. Baldock, T. A. Jowitt, D. F. Holmes, R. Lindstedt, M. Marcellini, V. Rivieccio, D. C. Briggs, K. E. Kadler, A. Verdoliva, et al. 2010. The angiogenic inhibitor long pentraxin PTX3 forms an asymmetric octamer with two binding sites for FGF2. J. Biol. Chem. 285: 17681-17692.
25. Braunschweig, A., and M. Józsi. 2011. Human pentraxin 3 binds to the complement regulator c4b-binding protein. PLoS ONE 6: e23991.
26. Deban, L., H. Jarva, M. J. Lehtinen, B. Bottazzi, A. Bastone, A. Doni, T. S. Jokiranta, A. Mantovani, and S. Meri. 2008. Binding of the long pentraxin PTX3 to factor H: interacting domains and function in the regulation of complement activation. J. Immunol. 181: 8433-8440.
27. Kopp, A., S. Strobel, A. Tortajada, S. Rodríguez de Córdoba, P. Sánchez-Corral, Z. Prohászka, M. López-Trascasa, and M. Józsi. 2012. Atypical hemolytic uremic syndrome-associated variants and autoantibodies impair binding of factor H and factor H-related protein 1 to pentraxin 3. J. Immunol. 189: 1858-1867.
28. Agrawal, A., P. P. Singh, B. Bottazzi, C. Garlanda, and A. Mantovani. 2009. Pattern recognition by pentraxins. Adv. Exp. Med. Biol. 653: 98-116.
29. Daigo, K., N. Yamaguchi, T. Kawamura, K. Matsubara, S. Jiang, R. Ohashi, Y. Sudou, T. Kodama, M. Naito, K. Inoue, and T. Hamakubo. 2012. The proteomic profile of circulating pentraxin 3 (PTX3) complex in sepsis demonstrates the interaction with azurocidin 1 and other components of neutrophil extracellular traps. Mol. Cell. Proteomics 11: M111.015073. doi:10.1074/mcp.M111.015073.
30. Kühn, S., and P. F. Zipfel. 1995. The baculovirus expression vector pBSV-8His directs secretion of histidine-tagged proteins. Gene 162: 225-229.
31. Castiblanco-Valencia, M. M., T. R. Fraga, L. B. Silva, D. Monaris, P. A. Abreu, S. Strobel, M. Józsi, L. Isaac, and A. S. Barbosa. 2012. Leptospiral immunoglobulinlike proteins interact with human complement regulators factor H, FHL-1, FHR-1, and C4BP. J. Infect. Dis. 205: 995-1004.
32. Hebecker, M., A. I. Okemefuna, S. J. Perkins, M. Mihlan, M. Huber-Lang, and M. Józsi. 2010. Molecular basis of C-reactive protein binding and modulation of complement activation by factor H-related protein 4. Mol. Immunol. 47: 1347-1355.
33. Mihlan, M., S. Stippa, M. Józsi, and P. F. Zipfel. 2009. Monomeric CRP contributes to complement control in fluid phase and on cellular surfaces and increases phagocytosis by recruiting factor H. Cell Death Differ. 16: 1630-1640.
34. Hebecker, M., and M. Józsi. 2012. Factor H-related protein 4 activates complement by serving as a platform for the assembly of alternative pathway C3 convertase via its interaction with C3b protein. J. Biol. Chem. 287: 19528-19536.
35. Nauta, A. J., B. Bottazzi, A. Mantovani, G. Salvatori, U. Kishore, W. J. Schwaeble, A. R. Gingras, S. Tzima, F. Vivanco, J. Egido, et al. 2003. Biochemical and functional characterization of the interaction between pentraxin 3 and C1q. Eur. J. Immunol. 33: 465-473.
36. Timmann, C., M. Leippe, and R. D. Horstmann. 1991. Two major serum components antigenically related to complement factor H are different glycosylation forms of a single protein with no factor H-like complement regulatory functions. J. Immunol. 146: 1265-1270.
37. Hellwage, J., T. S. Jokiranta, V. Koistinen, O. Vaarala, S. Meri, and P. F. Zipfel. 1999. Functional properties of complement factor H-related proteins FHR-3 and FHR-4: binding to the C3d region of C3b and differential regulation by heparin. FEBS Lett. 462: 345-352.
38. Fritsche, L. G., N. Lauer, A. Hartmann, S. Stippa, C. N. Keilhauer, M. Oppermann, M. K. Pandey, J. Köhl, P. F. Zipfel, B. H. Weber, and C. Skerka. 2010. An imbalance of human complement regulatory proteins CFHR1, CFHR3 and factor H influences risk for age-related macular degeneration (AMD). Hum. Mol. Genet. 19: 4694-4704.
39. Eberhardt, H. U., D. Buhlmann, P. Hortschansky, Q. Chen, S. Böhm, M. J. Kemper, R. Wallich, A. Hartmann, T. Hallström, P. F. Zipfel, and C. Skerka. 2013. Human factor H-related protein 2 (CFHR2) regulates complement activation. PLoS ONE 8: e78617.
40. Heinen, S., A. Hartmann, N. Lauer, U. Wiehl, H. M. Dahse, S. Schirmer, K. Gropp, T. Enghardt, R. Wallich, S. Hälbich, et al. 2009. Factor H-related protein 1 (CFHR-1) inhibits complement C5 convertase activity and terminal complex formation. Blood 114: 2439-2447.
41. Strobel, S., C. Abarrategui-Garrido, E. Fariza-Requejo, H. Seeberger, P. Sánchez-Corral, and M. Józsi. 2011. Factor H-related protein 1 neutralizes anti-factor H autoantibodies in autoimmune hemolytic uremic syndrome. Kidney Int. 80: 397-404.
42. Hammerschmidt, C., T. Hallström, C. Skerka, R. Wallich, B. Stevenson, P. F. Zipfel, and P. Kraiczy. 2012. Contribution of the infection-associated complement regulator-acquiring surface protein 4 (ErpC) to complement resistance of Borrelia burgdorferi. Clin. Dev. Immunol. 2012: 349657.
43. Siegel, C., T. Hallström, C. Skerka, H. Eberhardt, B. Uzonyi, T. Beckhaus, M. Karas, R. Wallich, B. Stevenson, P. F. Zipfel, and P. Kraiczy. 2010. Complement factor H-related proteins CFHR2 and CFHR5 represent novel ligands for the infection-associated CRASP proteins of Borrelia burgdorferi. PLoS ONE 5: e13519.
44. Närkiö-Mäkelä, M., J. Hellwage, O. Tahkokallio, and S. Meri. 2001. Complement-regulator factor H and related proteins in otitis media with effusion. Clin. Immunol. 100: 118-126.
45. Haupt, K., P. Kraiczy, R. Wallich, V. Brade, C. Skerka, and P. F. Zipfel. 2007. Binding of human factor H-related protein 1 to serum-resistant Borrelia burgdorferi is mediated by borrelial complement regulator-acquiring surface proteins. J. Infect. Dis. 196: 124-133.
46. Reuter, M., C. C. Caswell, S. Lukomski, and P. F. Zipfel. 2010. Binding of the human complement regulators CFHR1 and factor H by streptococcal collagen-like protein 1 (Scl1) via their conserved C termini allows control of the complement cascade at multiple levels. J. Biol. Chem. 285: 38473-38485.
47. Józsi, M., and S. Meri. 2014. Factor H-related proteins. Methods Mol. Biol. 1100: 225-236.
48. Vernon, K. A., D. P. Gale, E. G. de Jorge, A. G. McLean, J. Galliford, A. Pierides, P. H. Maxwell, D. Taube, M. C. Pickering, and H. T. Cook. 2011. Recurrence of complement factor H-related protein 5 nephropathy in a renal transplant. Am. J. Transplant. 11: 152-155.
49. Byron, A., M. J. Randles, J. D. Humphries, A. Mironov, H. Hamidi, S. Harris, P. W. Mathieson, M. A. Saleem, S. C. Satchell, R. Zent, et al. 2014. Glomerular cell cross-talk influences composition and assembly of extracellular matrix. J. Am. Soc. Nephrol. 25: 953-966.
50. Lennon, R., A. Byron, J. D. Humphries, M. J. Randles, A. Carisey, S. Murphy, D. Knight, P. E. Brenchley, R. Zent, and M. J. Humphries. 2014. Global analysis reveals the complexity of the human glomerular extracellular matrix. J. Am. Soc. Nephrol. 25: 939-951.
51. Suliman, M. E., M. I. Yilmaz, J. J. Carrero, A. R. Qureshi, M. Saglam, O. M. Ipcioglu, M. Yenicesu, M. Tong, O. Heimbürger, P. Barany, et al. 2008. Novel links between the long pentraxin 3, endothelial dysfunction, and albuminuria in early and advanced chronic kidney disease. Clin. J. Am. Soc. Nephrol. 3: 976-985.
52. Tong, M., J. J. Carrero, A. R. Qureshi, B. Anderstam, O. Heimbürger, P. Bárány, J. Axelsson, A. Alvestrand, P. Stenvinkel, B. Lindholm, and M. E. Suliman. 2007. Plasma pentraxin 3 in patients with chronic kidney disease: associations with renal function, protein-energy wasting, cardiovascular disease, and mortality. Clin. J. Am. Soc. Nephrol. 2: 889-897.
53. Chen, J., M. M. Matzuk, X. J. Zhou, and C. Y. Lu. 2012. Endothelial pentraxin 3 contributes to murine ischemic acute kidney injury. Kidney Int. 82: 1195-1207.
54. Lech, M., C. Römmele, R. Gröbmayr, H. Eka Susanti, O. P. Kulkarni, S. Wang, H. J. Gröne, B. Uhl, C. Reichel, F. Krombach, et al. 2013. Endogenous and exogenous pentraxin-3 limits postischemic acute and chronic kidney injury. Kidney Int. 83: 647-661.