Complement activation by ceramide transporter proteins

Journal of Immunology

Volumn 192, Issue 3, 2014, Pages 1154-1161

  Bode, Gerard H ^a   Losen, Mario ^a   Buurman, Wim A ^a   Veerhuis, Robert ^b   Molenaar, Peter C ^a   Steinbusch, Harry W M ^a   De Baets, Marc H ^a   Daha, Mohamed R ^c   Martinez Martinez, Pilar ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CARRIER PROTEIN; CERAMIDE TRANSPORTER PROTEIN; CERAMIDE TRANSPORTER PROTEIN LONGER SPLICING ISOFORM; COLLAGEN TYPE 4; COMPLEMENT COMPONENT C1Q; COMPLEMENT COMPONENT C3; COMPLEMENT COMPONENT C4; COMPLEMENT MEMBRANE ATTACK COMPLEX; SERUM AMYLOID P; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL SURFACE; CELLULAR DISTRIBUTION; COMPLEMENT ACTIVATION; COMPLEMENT CLASSICAL PATHWAY; CONTROLLED STUDY; HUMAN; INNATE IMMUNITY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN IMMOBILIZATION; PROTEIN LOCALIZATION;

ANTIBODIES, MONOCLONAL; APOPTOSIS; BINDING SITES; COMPLEMENT C1Q; COMPLEMENT PATHWAY, ALTERNATIVE; COMPLEMENT PATHWAY, CLASSICAL; HUMANS; IMMUNITY, INNATE; JURKAT CELLS; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; PROTEIN-SERINE-THREONINE KINASES; RECOMBINANT FUSION PROTEINS; SERUM AMYLOID P-COMPONENT;

EID: 84893367415     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1301673     Document Type: Article

References (57)

1. Medzhitov, R. 2007. Recognition of microorganisms and activation of the immune response. Nature 449: 819-826.
2. Matzinger, P. 2002. The danger model: a renewed sense of self. Science 296: 301-305.
3. Ghebrehiwet, B., K. K. Hosszu, A. Valentino, and E. I. Peerschke. 2012. The C1q family of proteins: insights into the emerging non-traditional functions. Front. Immunol. April 5: 3.
4. Litvack, M. L., and N. Palaniyar. 2010. Review: Soluble innate immune patternrecognition proteins for clearing dying cells and cellular components: implications on exacerbating or resolving inflammation. Innate Immun. 16: 191-200.
5. Poon, I. K., M. D. Hulett, and C. R. Parish. 2010. Molecular mechanisms of late apoptotic/necrotic cell clearance. Cell Death Differ. 17: 381-397.
6. Trouw, L. A., A. M. Blom, and P. Gasque. 2008. Role of complement and complement regulators in the removal of apoptotic cells. Mol. Immunol. 45: 1199-1207.
7. Daha, M. R. 2010. Role of complement in innate immunity and infections. Crit. Rev. Immunol. 30: 47-52.
8. Lambris, J. D., D. Ricklin, and B. V. Geisbrecht. 2008. Complement evasion by human pathogens. Nat. Rev. Microbiol. 6: 132-142.
9. Chen, M., M. R. Daha, and C. G. Kallenberg. 2010. The complement system in systemic autoimmune disease. J. Autoimmun. 34: J276-J286.
10. Walport, M. J. 2001. Complement. First of two parts. N. Engl. J. Med. 344: 1058-1066.
11. Walport, M. J. 2001. Complement. Second of two parts. N. Engl. J. Med. 344: 1140-1144.
12. 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.
13. Gadjeva, M. G., M. M. Rouseva, A. S. Zlatarova, K. B. Reid, U. Kishore, and M. S. Kojouharova. 2008. Interaction of human C1q with IgG and IgM: revisited. Biochemistry 47: 13093-13102.
14. Agrawal, A., A. K. Shrive, T. J. Greenhough, and J. E. Volanakis. 2001. Topology and structure of the C1q-binding site on C-reactive protein. J. Immunol. 166: 3998-4004.
15. Nauta, A. J., L. A. Trouw, M. R. Daha, O. Tijsma, R. Nieuwland, W. J. Schwaeble, A. R. Gingras, A. Mantovani, E. C. Hack, and A. Roos. 2002. Direct binding of C1q to apoptotic cells and cell blebs induces complement activation. Eur. J. Immunol. 32: 1726-1736.
16. Martin, M., J. Leffler, and A. M. Blom. 2012. Annexin A2 and A5 serve as new ligands for C1q on apoptotic cells. J. Biol. Chem. 287: 33733-33744.
17. Sjoberg, A. P., L. A. Trouw, and A. M. Blom. 2009. Complement activation and inhibition: a delicate balance. Trends Immunol. 30: 83-90.
18. Mencarelli, C., G. H. Bode, M. Losen, M. Kulharia, P. C. Molenaar, R. Veerhuis, H. W. Steinbusch, M. H. De Baets, G. A. Nicolaes, and P. Martinez-Martinez. 2012. Goodpasture antigen-binding protein/ceramide transporter binds to human serum amyloid P-component and is present in brain amyloid plaques. J. Biol. Chem. 287: 14897-14911.
19. Mencarelli, C., M. Losen, C. Hammels, J. De Vry, M. K. Hesselink, H. W. Steinbusch, M. H. De Baets, and P. Martínez-Martínez. 2010. The ceramide transporter and the Goodpasture antigen binding protein: one protein -one function J. Neurochem. 113: 1369-1386.
20. Raya, A., F. Revert-Ros, P. Martinez-Martinez, S. Navarro, E. Rosello, B. Vieites, F. Granero, J. Forteza, and J. Saus. 2000. Goodpasture antigenbinding protein, the kinase that phosphorylates the goodpasture antigen, is an alternatively spliced variant implicated in autoimmune pathogenesis. J. Biol. Chem. 275: 40392-40399.
21. Hanada, K., K. Kumagai, S. Yasuda, Y. Miura, M. Kawano, M. Fukasawa, and M. Nishijima. 2003. Molecular machinery for non-vesicular trafficking of ceramide. Nature 426: 803-809.
22. Revert, F., I. Ventura, P. Martínez-Martínez, F. Granero-Moltó, F. Revert-Ros, J. Macías, and J. Saus. 2008. Goodpasture antigen-binding protein is a soluble exportable protein that interacts with type IV collagen. Identification of novel membrane-bound isoforms. J. Biol. Chem. 283: 30246-30255.
23. Raya, A., F. Revert, S. Navarro, and J. Saus. 1999. Characterization of a novel type of serine/threonine kinase that specifically phosphorylates the human goodpasture antigen. J. Biol. Chem. 274: 12642-12649.
24. Granero, F., F. Revert, F. Revert-Ros, S. Lainez, P. Martínez- Martínez, and J. Saus. 2005. A human-specific TNF-responsive promoter for Goodpasture antigen-binding protein. FEBS J. 272: 5291-5305.
25. Revert, F., R. Merino, C. Monteagudo, J. Macias, A. Peydró, J. Alcácer, P. Muniesa, R. Marquina, M. Blanco, M. Iglesias, et al. 2007. Increased Goodpasture antigen-binding protein expression induces type IV collagen disorganization and deposit of immunoglobulin A in glomerular basement membrane. Am. J. Pathol. 171: 1419-1430.
26. Xu, W., S. P. Berger, L. A. Trouw, H. C. de Boer, N. Schlagwein, C. Mutsaers, M. R. Daha, and C. van Kooten. 2008. Properdin binds to late apoptotic and necrotic cells independently of C3b and regulates alternative pathway complement activation. J. Immunol. 180: 7613-7621.
27. Groeneveld, T. W., T. H. Ramwadhdoebé, L. A. Trouw, D. L. van den Ham, V. van der Borden, J. W. Drijfhout, P. S. Hiemstra, M. R. Daha, and A. Roos. 2007. Human neutrophil peptide-1 inhibits both the classical and the lectin pathway of complement activation. Mol. Immunol. 44: 3608-3614.
28. Groeneveld, T. W., M. Oroszlán, R. T. Owens, M. C. Faber-Krol, A. C. Bakker, G. J. Arlaud, D. J. McQuillan, U. Kishore, M. R. Daha, and A. Roos. 2005. Interactions of the extracellular matrix proteoglycans decorin and biglycan with C1q and collectins. J. Immunol. 175: 4715-4723.
29. Roos, A., M. Essers, D. van Gijlswijk-Janssen, N. V. Bovin, and M. R. Daha. 2001. Both IgG and IgM anti-pig antibodies induce complement activation and cytotoxicity. Xenotransplantation 8: 3-14.
30. Roos, A., L. H. Bouwman, J. Munoz, T. Zuiverloon, M. C. Faber-Krol, F. C. Fallaux-van den Houten, N. Klar-Mohamad, C. E. Hack, M. G. Tilanus, and M. R. Daha. 2003. Functional characterization of the lectin pathway of complement in human serum. Mol. Immunol. 39: 655-668.
31. Hoekzema, R., M. Martens, M. C. Brouwer, and C. E. Hack. 1988. The distortive mechanism for the activation of complement component C1 supported by studies with a monoclonal antibody against the "arms" of C1q. Mol. Immunol. 25: 485-494.
32. Sievers, F., A. Wilm, D. Dineen, T. J. Gibson, K. Karplus, W. Li, R. Lopez, H. McWilliam, M. Remmert, J. Soding, et al. 2011. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol. 7: 539.
33. Kishore, U., R. Ghai, T. J. Greenhough, A. K. Shrive, D. M. Bonifati, M. G. Gadjeva, P. Waters, M. S. Kojouharova, T. Chakraborty, and A. Agrawal. 2004. Structural and functional anatomy of the globular domain of complement protein C1q. Immunol. Lett. 95: 113-128.
34. Pettus, B. J., C. E. Chalfant, and Y. A. Hannun. 2002. Ceramide in apoptosis: an overview and current perspectives. Biochim. Biophys. Acta 1585: 114-125.
35. Arboleda, G., L. C. Morales, B. Benítez, and H. Arboleda. 2009. Regulation of ceramide-induced neuronal death: cell metabolism meets neurodegeneration. Brain Res. Brain Res. Rev. 59: 333-346.
36. Babiychuk, E. B., A. P. Atanassoff, K. Monastyrskaya, C. Brandenberger, D. Studer, C. Allemann, and A. Draeger. 2011. The targeting of plasmalemmal ceramide to mitochondria during apoptosis. PLoS ONE 6: e23706.
37. Grassme, H., A. Jekle, A. Riehle, H. Schwarz, J. Berger, K. Sandhoff, R. Kolesnick, and E. Gulbins. 2001. CD95 signaling via ceramide-rich membrane rafts. J. Biol. Chem. 276: 20589-20596.
38. Wajant, H. 2002. The Fas signaling pathway: more than a paradigm. Science 296: 1635-1636.
39. Perry, D. K., J. Carton, A. K. Shah, F. Meredith, D. J. Uhlinger, and Y. A. Hannun. 2000. Serine palmitoyltransferase regulates de novo ceramide generation during etoposide-induced apoptosis. J. Biol. Chem. 275: 9078-9084.
40. Gullstrand, B., U. Martensson, G. Sturfelt, A. A. Bengtsson, and L. Truedsson. 2009. Complement classical pathway components are all important in clearance of apoptotic and secondary necrotic cells. Clin. Exp. Immunol. 156: 303-311.
41. Nauta, A. J., G. Castellano, W. Xu, A. M. Woltman, M. C. Borrias, M. R. Daha, C. van Kooten, and A. Roos. 2004. Opsonization with C1q and mannose-binding lectin targets apoptotic cells to dendritic cells. J. Immunol. 173: 3044-3050.
42. Roos, A., W. Xu, G. Castellano, A. J. Nauta, P. Garred, M. R. Daha, and C. van Kooten. 2004. Mini-review: A pivotal role for innate immunity in the clearance of apoptotic cells. Eur. J. Immunol. 34: 921-929.
43. Gaboriaud, C., J. Juanhuix, A. Gruez, M. Lacroix, C. Darnault, D. Pignol, D. Verger, J. C. Fontecilla-Camps, and G. J. Arlaud. 2003. The crystal structure of the globular head of complement protein C1q provides a basis for its versatile recognition properties. J. Biol. Chem. 278: 46974-46982.
44. Khoshnoodi, J., V. Pedchenko, and B. G. Hudson. 2008. Mammalian collagen IV. Microsc. Res. Tech. 71: 357-370.
45. Duncan, A. R., and G. Winter. 1988. The binding site for C1q on IgG. Nature 332: 738-740.
46. Kovacs, H., I. D. Campbell, P. Strong, S. Johnson, F. J. Ward, K. B. Reid, and P. Eggleton. 1998. Evidence that C1q binds specifically to CH2-like immunoglobulin gamma motifs present in the autoantigen calreticulin and interferes with complement activation. Biochemistry 37: 17865-17874.
47. Agrawal, A., and J. E. Volanakis. 1994. Probing the C1q-binding site on human C-reactive protein by site-directed mutagenesis. J. Immunol. 152: 5404-5410.
48. Nonaka, M., and A. Kimura. 2006. Genomic view of the evolution of the complement system. Immunogenetics 58: 701-713.
49. Pickering, M., and H. T. Cook. 2011. Complement and glomerular disease: new insights. Curr. Opin. Nephrol. Hypertens. 20: 271-277.
50. Sethu, S., and A. J. Melendez. 2011. New developments on the TNFa-mediated signalling pathways. Biosci. Rep. 31: 63-76.
51. Veerhuis, R., H. M. Nielsen, and A. J. Tenner. 2011. Complement in the brain. Mol. Immunol. 48: 1592-1603.
52. Veerhuis, R., M. J. Van Breemen, J. M. Hoozemans, M. Morbin, J. Ouladhadj, F. Tagliavini, and P. Eikelenboom. 2003. Amyloid beta plaque-Associated proteins C1q and SAP enhance the Abeta1-42 peptide-induced cytokine secretion by adult human microglia in vitro. Acta Neuropathol. 105: 135-144.
53. Gershov, D., S. Kim, N. Brot, and K. B. Elkon. 2000. C-Reactive protein binds to apoptotic cells, protects the cells from assembly of the terminal complement components, and sustains an antiinflammatory innate immune response: implications for systemic autoimmunity. J. Exp. Med. 192: 1353-1364.
54. Berman, S., H. Gewurz, and C. Mold. 1986. Binding of C-reactive protein to nucleated cells leads to complement activation without cytolysis. J. Immunol. 136: 1354-1359.
55. Cribbs, D. H., N. C. Berchtold, V. Perreau, P. D. Coleman, J. Rogers, A. J. Tenner, and C. W. Cotman. 2012. Extensive innate immune gene activation accompanies brain aging, increasing vulnerability to cognitive decline and neurodegeneration: a microarray study. J. Neuroinflammation 9: 179.
56. Fishelson, Z., N. Donin, S. Zell, S. Schultz, and M. Kirschfink. 2003. Obstacles to cancer immunotherapy: expression of membrane complement regulatory proteins (mCRPs) in tumors. Mol. Immunol. 40: 109-123.
57. Heering, J., N. Weis, M. Holeiter, F. Neugart, A. Staebler, T. N. Fehm, A. Bischoff, J. Schiller, S. Duss, S. Schmid, et al. 2012. Loss of the ceramide transfer protein augments EGF receptor signaling in breast cancer. Cancer Res. 72: 2855-2866.