The role of heparan sulfate as determining pathogenic factor in complement factor H-associated diseases

Molecular Immunology

Volumn 63, Issue 2, 2015, Pages 203-208

  Loeven, Markus A ^a   Rops, Angelique Lwmm ^a   Berden, Jo Hm ^a   Daha, Mohamed R ^b   Rabelink, Ton J ^b   van der Vlag, Johan ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Age related macular degeneration; Complement factor H; Complement mediated nephropathies; Endothelial microenvironment; Glycocalyx; Heparan sulfate

Indexed keywords

COMPLEMENT FACTOR H; HEPARAN SULFATE;

AGE RELATED MACULAR DEGENERATION; BINDING AFFINITY; BINDING SITE; COMPLEMENT ACTIVATION; COMPLEMENT DISORDER; CONFORMATIONAL TRANSITION; DENSE DEPOSIT DISEASE; DNA POLYMORPHISM; EYE INJURY; GENETIC RISK; GENETIC VARIABILITY; GLOMERULUS BASEMENT MEMBRANE; GLYCOCALYX; HEMOLYTIC UREMIC SYNDROME; HOST CELL; HUMAN; INFLAMMATION; KIDNEY INJURY; KIDNEY PARENCHYMA; OLIGOMERIZATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; RISK FACTOR; ANTIBODY SPECIFICITY; CHEMISTRY; IMMUNOLOGY; KIDNEY DISEASE; METABOLISM;

COMPLEMENT FACTOR H; HEPARITIN SULFATE; HUMANS; KIDNEY DISEASES; ORGAN SPECIFICITY;

EID: 84912036123     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2014.08.005     Document Type: Review

References (63)

1. Abrera-Abeleda M.A., Nishimura C., Smith J.L., Sethi S., McRae J.L., Murphy B.F., Silvestri G., Skerka C., Jozsi M., Zipfel P.F., Hageman G.S., Smith R.J. 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. 2006, 43:582-589.
2. Barbour T.D., Pickering M.C., Cook H.T. Recent insights into C3 glomerulopathy. Nephrol. Dial. Transplant. 2013, 28:1685-1693.
3. Boels M.G., Lee D.H., van den Berg B.M., Dane M.J., van der Vlag J., Rabelink T.J. The endothelial glycocalyx as a potential modifier of the hemolytic uremic syndrome. Eur. J. Intern. Med. 2013, 24:503-509.
4. Bouts A., Monnens L., Davin J.C., Struijk G., Spanjaard L. Insufficient protection by Neisseria meningitidis vaccination alone during eculizumab therapy. Pediatr. Nephrol. 2011, 26:1919-1920.
5. Clark S.J., Bishop P.N., Day A.J. Complement factor H and age-related macular degeneration: the role of glycosaminoglycan recognition in disease pathology. Biochem. Soc. Trans. 2010, 38:1342-1348.
6. Clark S.J., Higman V.A., Mulloy B., Perkins S.J., Lea S.M., Sim R.B., Day A.J. His-384 allotypic variant of factor H associated with age-related macular degeneration has different heparin binding properties from the non-disease-associated form. J. Biol. Chem. 2006, 281:24713-24720.
7. Clark S.J., Ridge L.A., Herbert A.P., Hakobyan S., Mulloy B., Lennon R., Wurzner R., Morgan B.P., Uhrin D., Bishop P.N., Day A.J. Tissue-specific host recognition by complement factor H is mediated by differential activities of its glycosaminoglycan-binding regions. J. Immunol. 2013, 190:2049-2057.
8. de Cordoba S.R., de Jorge E.G. Translational mini-review series on complement factor H: genetics and disease associations of human complement factor H. Clin. Exp. Immunol. 2008, 151:1-13.
9. Do D.V. Implications of the comparisons of age-related macular degeneration treatments trials on clinical practice: what have we learned?. Ophthalmology 2013, 120:S8-S10.
10. Donoso L.A., Vrabec T., Kuivaniemi H. The role of complement factor H in age-related macular degeneration: a review. Surv. Ophthalmol. 2010, 55:227-246.
11. Esko J.D., Selleck S.B. Order out of chaos: assembly of ligand binding sites in heparan sulfate. Annu. Rev. Biochem. 2002, 71:435-471.
12. Fernando A.N., Furtado P.B., Clark S.J., Gilbert H.E., Day A.J., Sim R.B., Perkins S.J. Associative and structural properties of the region of complement factor H encompassing the Tyr402His disease-related polymorphism and its interactions with heparin. J. Mol. Biol. 2007, 368:564-581.
13. Feyzi E., Saldeen T., Larsson E., Lindahl U., Salmivirta M. Age-dependent modulation of heparan sulfate structure and function. J. Biol. Chem. 1998, 273:13395-13398.
14. Guimond S.E., Puvirajesinghe T.M., Skidmore M.A., Kalus I., Dierks T., Yates E.A., Turnbull J.E. Rapid purification and high sensitivity analysis of heparan sulfate from cells and tissues: toward glycomics profiling. J. Biol. Chem. 2009, 284:25714-25722.
15. Hageman G.S., Anderson D.H., Johnson L.V., Hancox L.S., Taiber A.J., Hardisty L.I., Hageman J.L., Stockman H.A., Borchardt J.D., Gehrs K.M., Smith R.J., Silvestri G., Russell S.R., Klaver C.C., Barbazetto I., Chang S., Yannuzzi L.A., Barile G.R., Merriam J.C., Smith R.T., Olsh A.K., Bergeron J., Zernant J., Merriam J.E., Gold B., Dean M., Allikmets R. A common haplotype in the complement regulatory gene factor H (HF1/CFH) predisposes individuals to age-related macular degeneration. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:7227-7232.
16. Harrison R.A., Lachmann P.J. The physiological breakdown of the third component of human complement. Mol. Immunol. 1980, 17:9-20.
17. Hellwage J., Jokiranta T.S., Koistinen V., Vaarala O., Meri S., Zipfel P.F. 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. 1999, 462:345-352.
18. Hughes A.E., Orr N., Esfandiary H., Diaz-Torres M., Goodship T., Chakravarthy U. A common CFH haplotype, with deletion of CFHR1 and CFHR3, is associated with lower risk of age-related macular degeneration. Nat. Genet. 2006, 38:1173-1177.
19. Jozsi M., Zipfel P.F. Factor H family proteins and human diseases. Trends Immunol. 2008, 29:380-387.
20. Kaiser P.K. Emerging therapies for neovascular age-related macular degeneration: drugs in the pipeline. Ophthalmology 2013, 120:S11-S15.
21. Keenan T.D., Pickford C.E., Holley R.J., Clark S.J., Lin W., Dowsey A.W., Merry C.L., Day A.J., Bishop P.N. Age-dependent changes in heparan sulfate in human Bruch's membrane: implications for age-related macular degeneration. Invest. Ophthalmol. Vis. Sci. 2014, 55:5370-5379.
22. Kelly U., Yu L., Kumar P., Ding J.D., Jiang H., Hageman G.S., Arshavsky V.Y., Frank M.M., Hauser M.A., Rickman C.B. Heparan sulfate, including that in Bruch's membrane, inhibits the complement alternative pathway: implications for age-related macular degeneration. J. Immunol. 2010, 185:5486-5494.
23. Khan S., Fung K.W., Rodriguez E., Patel R., Gor J., Mulloy B., Perkins S.J. The solution structure of heparan sulfate differs from that of heparin: implications for function. J. Biol. Chem. 2013, 288:27737-27751.
24. Khan S., Nan R., Gor J., Mulloy B., Perkins S.J. Bivalent and co-operative binding of complement factor H to heparan sulfate and heparin. Biochem. J. 2012, 444:417-428.
25. Kim H., Xu G.L., Borczuk A.C., Busch S., Filmus J., Capurro M., Brody J.S., Lange J., D'Armiento J.M., Rothman P.B., Powell C.A. The heparan sulfate proteoglycan GPC3 is a potential lung tumor suppressor. Am. J. Respir. Cell Mol. Biol. 2003, 29:694-701.
26. Langford-Smith A., Keenan T.D., Clark S.J., Bishop P.N., Day A.J. The role of complement in age-related macular degeneration: heparan sulphate, a zip code for complement factor H?. J. Innate. Immun. 2013.
27. Law S.K., Levine R.P. Interaction between the third complement protein and cell surface macromolecules. Proc. Natl. Acad. Sci. U.S.A. 1977, 74:2701-2705.
28. Lehtinen M.J., Rops A.L., Isenman D.E., van der Vlag J., Jokiranta T.S. Mutations of factor H impair regulation of surface-bound C3b by three mechanisms in atypical hemolytic uremic syndrome. J. Biol. Chem. 2009, 284:15650-15658.
29. Lemjabbar-Alaoui H., van Zante A., Singer M.S., Xue Q., Wang Y.Q., Tsay D., He B., Jablons D.M., Rosen S.D. Sulf-2, a heparan sulfate endosulfatase, promotes human lung carcinogenesis. Oncogene 2010, 29:635-646.
30. Lindahl U., Kjellen L. Pathophysiology of heparan sulphate: many diseases, few drugs. J. Intern. Med. 2013, 273:555-571.
31. Makou E., Herbert A.P., Barlow P.N. Functional anatomy of complement factor H. Biochemistry 2013, 52:3949-3962.
32. McRae J.L., Duthy T.G., Griggs K.M., Ormsby R.J., Cowan P.J., Cromer B.A., McKinstry W.J., Parker M.W., Murphy B.F., Gordon D.L. 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. 2005, 174:6250-6256.
33. Meri S., Pangburn M.K. Discrimination between activators and nonactivators of the alternative pathway of complement: regulation via a sialic acid/polyanion binding site on factor H. Proc. Natl. Acad. Sci. U.S.A. 1990, 87:3982-3986.
34. Morgan H.P., Schmidt C.Q., Guariento M., Blaum B.S., Gillespie D., Herbert A.P., Kavanagh D., Mertens H.D., Svergun D.I., Johansson C.M., Uhrin D., Barlow P.N., Hannan J.P. Structural basis for engagement by complement factor H of C3b on a self surface. Nat. Struct. Mol. Biol. 2011, 18:463-470.
35. Mullins R.F., Aptsiauri N., Hageman G.S. Structure and composition of drusen associated with glomerulonephritis: implications for the role of complement activation in drusen biogenesis. Eye (Lond) 2001, 15:390-395.
36. Murata K., Horiuchi Y. Age-dependent distribution of acidic glycosaminoglycans in human kidney tissue. Nephron 1978, 20:111-118.
37. Nan R., Farabella I., Schumacher F.F., Miller A., Gor J., Martin A.C., Jones D.T., Lengyel I., Perkins S.J. Zinc binding to the Tyr402 and His402 allotypes of complement factor H: possible implications for age-related macular degeneration. J. Mol. Biol. 2011, 408:714-735.
38. O'Flynn J., Flierman R., van der Pol P., Rops A., Satchell S.C., Mathieson P.W., van Kooten C., van der Vlag J., Berden J.H., Daha M.R. Nucleosomes and C1q bound to glomerular endothelial cells serve as targets for autoantibodies and determine complement activation. Mol. Immunol. 2011, 49:75-83.
39. Okemefuna A.I., Nan R., Gor J., Perkins S.J. Electrostatic interactions contribute to the folded-back conformation of wild type human factor H. J. Mol. Biol. 2009, 391:98-118.
40. Olson S.T., Bjork I., Sheffer R., Craig P.A., Shore J.D., Choay J. Role of the antithrombin-binding pentasaccharide in heparin acceleration of antithrombin-proteinase reactions. Resolution of the antithrombin conformational change contribution to heparin rate enhancement. J. Biol. Chem. 1992, 267:12528-12538.
41. Ori A., Wilkinson M.C., Fernig D.G. The heparanome and regulation of cell function: structures, functions and challenges. Front. Biosci. 2008, 13:4309-4338.
42. Pangburn M.K. Host recognition and target differentiation by factor H, a regulator of the alternative pathway of complement. Immunopharmacology 2000, 49:149-157.
43. Pangburn M.K., Schreiber R.D., Muller-Eberhard H.J. Formation of the initial C3 convertase of the alternative complement pathway. Acquisition of C3b-like activities by spontaneous hydrolysis of the putative thioester in native C3. J. Exp. Med. 1981, 154:856-867.
44. Pellegrini L. Role of heparan sulfate in fibroblast growth factor signalling: a structural view. Curr. Opin. Struct. Biol. 2001, 11:629-634.
45. Perkins S.J., Nan R., Li K., Khan S., Miller A. Complement factor H-ligand interactions: self-association, multivalency and dissociation constants. Immunobiology 2012, 217:281-297.
46. Pries A.R., Secomb T.W., Gaehtgens P. The endothelial surface layer. Pflugers Arch. 2000, 440:653-666.
47. Rayes J., Roumenina L.T., Dimitrov J.D., Repesse Y., Ing M., Christophe O., Jokiranta T.S., Halbwachs-Mecarelli L., Borel-Derlon A., Kaveri S.V., Fremeaux-Bacchi V., Lacroix-Desmazes S. The interaction between factor H and VWF increases factor H cofactor activity and regulates VWF prothrombotic status. Blood 2014, 123:121-125.
48. Rops A.L., van der Vlag J., Lensen J.F., Wijnhoven T.J., van den Heuvel L.P., van Kuppevelt T.H., Berden J.H. Heparan sulfate proteoglycans in glomerular inflammation. Kidney Int. 2004, 65:768-785.
49. Sadler J.E. Biochemistry and genetics of von Willebrand factor. Annu. Rev. Biochem. 1998, 67:395-424.
50. Sarrazin S., Lamanna W.C., Esko J.D. Heparan sulfate proteoglycans. Cold Spring Harb. Perspect. Biol. 2011, 3.
51. Saunders R.E., Goodship T.H., Zipfel P.F., Perkins S.J. An interactive web database of factor H-associated hemolytic uremic syndrome mutations: insights into the structural consequences of disease-associated mutations. Hum. Mutat. 2006, 27:21-30.
52. Schmidt C.Q., Herbert A.P., Hocking H.G., Uhrin D., Barlow P.N. Translational mini-review series on complement factor H: structural and functional correlations for factor H. Clin. Exp. Immunol. 2008, 151:14-24.
53. Schmidt C.Q., Herbert A.P., Kavanagh D., Gandy C., Fenton C.J., Blaum B.S., Lyon M., Uhrin D., Barlow P.N. A new map of glycosaminoglycan and C3b binding sites on factor H. J. Immunol. 2008, 181:2610-2619.
54. Seddon J.M., Reynolds R., Maller J., Fagerness J.A., Daly M.J., Rosner B. Prediction model for prevalence and incidence of advanced age-related macular degeneration based on genetic, demographic, and environmental variables. Invest. Ophthalmol. Vis. Sci. 2009, 50:2044-2053.
55. Silva A.S., Teixeira A.G., Bavia L., Lin F., Velletri R., Belfort R., Isaac L. Plasma levels of complement proteins from the alternative pathway in patients with age-related macular degeneration are independent of Complement Factor H Tyr(4)(0)(2)His polymorphism. Mol. Vis. 2012, 18:2288-2299.
56. Toida T., Yoshida H., Toyoda H., Koshiishi I., Imanari T., Hileman R.E., Fromm J.R., Linhardt R.J. Structural differences and the presence of unsubstituted amino groups in heparan sulphates from different tissues and species. Biochem. J. 1997, 322(Pt 2):499-506.
57. Turnbull J., Powell A., Guimond S. Heparan sulfate: decoding a dynamic multifunctional cell regulator. Trends Cell Biol. 2001, 11:75-82.
58. Weiler J.M., Daha M.R., Austen K.F., Fearon D.T. Control of the amplification convertase of complement by the plasma protein beta1H. Proc. Natl. Acad. Sci. U. S. A. 1976, 73:3268-3272.
59. Weismann D., Hartvigsen K., Lauer N., Bennett K.L., Scholl H.P., Charbel Issa P., Cano M., Brandstatter H., Tsimikas S., Skerka C., Superti-Furga G., Handa J.T., Zipfel P.F., Witztum J.L., Binder C.J. Complement factor H binds malondialdehyde epitopes and protects from oxidative stress. Nature 2011, 478:76-81.
60. Westra D., Wetzels J.F., Volokhina E.B., van den Heuvel L.P., van de Kar N.C. A new era in the diagnosis and treatment of atypical haemolytic uraemic syndrome. Neth. J. Med. 2012, 70:121-129.
61. Zipfel P.F., Edey M., Heinen S., Jozsi M., Richter H., Misselwitz J., Hoppe B., Routledge D., Strain L., Hughes A.E., Goodship J.A., Licht C., Goodship T.H., Skerka C. Deletion of complement factor H-related genes CFHR1 and CFHR3 is associated with atypical hemolytic uremic syndrome. PLoS Genet. 2007, 3:e41.
62. Zipfel P.F., Skerka C. FHL-1/reconectin: a human complement and immune regulator with cell-adhesive function. Immunol. Today 1999, 20:135-140.
63. Zipfel P.F., Skerka C. Complement regulators and inhibitory proteins. Nat. Rev. Immunol. 2009, 9:729-740.