PTX3 as a paradigm for the interaction of pentraxins with the Complement system

Seminars in Immunology

Volumn 25, Issue 1, 2013, Pages 79-85

  Inforzato, Antonio ^a   Doni, Andrea ^a   Barajon, Isabella ^a,b   Leone, Roberto ^a   Garlanda, Cecilia ^a   Bottazzi, Barbara ^a   Mantovani, Alberto ^a,b  

^a HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

Author keywords

Complement; Pentraxins; PTX3

Indexed keywords

C REACTIVE PROTEIN; COMPLEMENT COMPONENT C1Q; COMPLEMENT FACTOR H; FICOLIN; LECTIN; PENTRAXIN 3; SERUM AMYLOID P;

AUTOIMMUNITY; BLOOD; COMPLEMENT SYSTEM; GLYCOSYLATION; HOST RESISTANCE; HUMAN; MACROPHAGE; MASS SPECTROMETRY; NEUTROPHIL; NONHUMAN; PATTERN RECOGNITION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; TISSUES; X RAY CRYSTALLOGRAPHY; X RAY DIFFRACTION;

COMPLEMENT; PENTRAXINS; PTX3;

ACUTE-PHASE REACTION; ANIMALS; C-REACTIVE PROTEIN; COMPLEMENT ACTIVATION; COMPLEMENT SYSTEM PROTEINS; HOST-PATHOGEN INTERACTIONS; IMMUNITY, INNATE; IMMUNOMODULATION; PROTEIN BINDING; RECEPTORS, PATTERN RECOGNITION; SERUM AMYLOID P-COMPONENT;

EID: 84879887039     PISSN: 10445323     EISSN: 10963618     Source Type: Journal    
DOI: 10.1016/j.smim.2013.05.002     Document Type: Review

References (79)

1. Ricklin D., Hajishengallis G., Yang K., Lambris J.D. Complement: a key system for immune surveillance and homeostasis. Nature Immunology 2010, 11:785-797.
2. Bottazzi B., Doni A., Garlanda C., Mantovani A. An integrated view of humoral innate immunity: pentraxins as a paradigm. Annual Review of Immunology 2010, 28:157-183.
3. Holmskov U., Thiel S., Jensenius J.C. Collectins and ficolins: humoral lectins of the innate immune defense. Annual Review of Immunology 2003, 21:547-578.
4. Endo Y., Matsushita M., Fujita T. The role of ficolins in the lectin pathway of innate immunity. International Journal of Biochemistry and Cell Biology 2011, 43:705-712.
5. Fujita T. Evolution of the lectin-complement pathway and its role in innate immunity. Nature Reviews Immunology 2002, 2:346-353.
6. Garlanda C., Bottazzi B., Bastone A., Mantovani A. Pentraxins at the crossroads between innate immunity, inflammation, matrix deposition, and female fertility. Annual Review of Immunology 2005, 23:337-366.
7. Emsley J., White H.E., O'Hara B.P., Oliva G., Srinivasan N., Tickle I.J., et al. Structure of pentameric human serum amyloid P component. Nature 1994, 367:338-345.
8. Goodman A.R., Cardozo T., Abagyan R., Altmeyer A., Wisniewski H.G., Vilcek J. Long pentraxins: an emerging group of proteins with diverse functions. Cytokine and Growth Factor Reviews 1996, 7:191-202.
9. Martinez de la Torre Y., Fabbri M., Jaillon S., Bastone A., Nebuloni M., Vecchi A., et al. Evolution of the pentraxin family: the new entry PTX4. Journal of Immunology 2010, 184:5055-5064.
10. Poon I.K., Hulett M.D., Parish C.R. Molecular mechanisms of late apoptotic/necrotic cell clearance. Cell Death and Differentiation 2010, 17:381-397.
11. Pepys M.B., Hirschfield G.M. C-reactive protein: a critical update. Journal of Clinical Investigation 2003, 111:1805-1812.
12. Casas J.P., Shah T., Hingorani A.D., Danesh J., Pepys M.B. C-reactive protein and coronary heart disease: a critical review. Journal of Internal Medicine 2008, 264:295-314.
13. Bijl M., Bootsma H., Van Der Geld Y., Limburg P.C., Kallenberg C.G., Van Rijswijk M.H., et al. Serum amyloid P component levels are not decreased in patients with systemic lupus erythematosus and do not rise during an acute phase reaction. Annals of the Rheumatic Diseases 2004, 63:831-835.
14. Shrive A.K., Cheetham G.M., Holden D., Myles D.A., Turnell W.G., Volanakis J.E., et al. Three dimensional structure of human C-reactive protein. Natural Structural Biology 1996, 3:346-354.
15. Ashton A.W., Boehm M.K., Gallimore J.R., Pepys M.B., Perkins S.J. Pentameric and decameric structures in solution of serum amyloid P component by X-ray and neutron scattering and molecular modelling analyses. Journal of Molecular Biology 1997, 272:408-422.
16. Thompson D., Pepys M.B., Wood S.P. The physiological structure of human C-reactive protein and its complex with phosphocholine. Structure 1999, 7:169-177.
17. Mikolajek H., Kolstoe S.E., Pye V.E., Mangione P., Pepys M.B., Wood S.P. Structural basis of ligand specificity in the human pentraxins, C-reactive protein and serum amyloid P component. Journal of Molecular Recognition 2011, 24:371-377.
18. Lu J., Marnell L.L., Marjon K.D., Mold C., Du Clos T.W., Sun P.D. Structural recognition and functional activation of Fc gamma R by innate pentraxins. Nature 2008, 456:989-992.
19. Marnell L.L., Mold C., Volzer M.A., Burlingame R.W., Du Clos T.W. C-reactive protein binds to Fc gamma RI in transfected COS cells. Journal of Immunology 1995, 155:2185-2193.
20. Bharadwaj D., Mold C., Markham E., Du Clos T.W. Serum amyloid P component binds to Fc gamma receptors and opsonizes particles for phagocytosis. Journal of Immunology 2001, 166:6735-6741.
21. Lu J., Marjon K.D., Mold C., Du Clos T.W., Sun P.D. Pentraxins and Fc receptors. Immunological Reviews 2012, 250:230-238.
22. Nauta A.J., Daha M.R., van Kooten C., Roos A. Recognition and clearance of apoptotic cells: a role for complement and pentraxins. Trends in Immunology 2003, 24:148-154.
23. Agrawal A., Shrive A.K., Greenhough T.J., Volanakis J.E. Topology and structure of the C1q-binding site on C-reactive protein. Journal of Immunology 2001, 166:3998-4004.
24. Roumenina L.T., Ruseva M.M., Zlatarova A., Ghai R., Kolev M., Olova N., et al. Interaction of C1q with IgG1, C-reactive protein and pentraxin 3: mutational studies using recombinant globular head modules of human C1q A, B, and C chains. Biochemistry 2006, 45:4093-4104.
25. Ng P.M., Le Saux A., Lee C.M., Tan N.S., Lu J., Thiel S., et al. C-reactive protein collaborates with plasma lectins to boost immune response against bacteria. EMBO Journal 2007, 26:3431-3440.
26. Gershov D., Kim S., Brot N., Elkon K.B. 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. Journal of Experimental Medicine 2000, 192:1353-1364.
27. Jarva H., Jokiranta T.S., Hellwage J., Zipfel P.F., Meri S. 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. Journal of Immunology 1999, 163:3957-3962.
28. Okemefuna A.I., Nan R., Miller A., Gor J., Perkins S.J. Complement factor H binds at two independent sites to C-reactive protein in acute phase concentrations. Journal of Biological Chemistry 2010, 285:1053-1065.
29. Sjoberg A.P., Trouw L.A., McGrath F.D., Hack C.E., Blom A.M. Regulation of complement activation by C-reactive protein: targeting of the inhibitory activity of C4b-binding protein. Journal of Immunology 2006, 176:7612-7620.
30. Garcia de Frutos P., Hardig Y., Dahlback B. Serum amyloid P component binding to C4b-binding protein. Journal of Biological Chemistry 1995, 270:26950-26955.
31. Gorsuch W.B., Chrysanthou E., Schwaeble W.J., Stahl G.L. The complement system in ischemia-reperfusion injuries. Immunobiology 2012, 217:1026-1033.
32. Gill R., Kemp J.A., Sabin C., Pepys M.B. Human C-reactive protein increases cerebral infarct size after middle cerebral artery occlusion in adult rats. Journal of Cerebral Blood Flow and Metabolism 2004, 24:1214-1218.
33. Schoos M.M., Munthe-Fog L., Skjoedt M.O., Ripa R.S., Lonborg J., Kastrup J., et al. Association between lectin complement pathway initiators, C-reactive protein and left ventricular remodeling in myocardial infarction-A magnetic resonance study. Molecular Immunology 2013, 54:408-414.
34. Kopp A., Hebecker M., Svobodová E., Józsi M. Factor H: a complement regulator in health and disease, and a mediator of cellular interactions. Biomolecules 2012, 2:46-75.
35. Breviario F., d'Aniello E.M., Golay J., Peri G., Bottazzi B., Bairoch A., et al. Interleukin-1-inducible genes in endothelial cells cloning of a new gene related to C-reactive protein and serum amyloid P component. Journal of Biological Chemistry 1992, 267:22190-22197.
36. Altmeyer A., Klampfer L., Goodman A.R., Vilcek J. Promoter structure and transcriptional activation of the murine TSG-14 gene encoding a tumor necrosis factor/interleukin-1-inducible pentraxin protein. Journal of Biological Chemistry 1995, 270:25584-25590.
37. Basile A., Sica A., d'Aniello E., Breviario F., Garrido G., Castellano M., et al. Characterization of the promoter for the human long pentraxin PTX3. Role of NF-kappaB in tumor necrosis factor-alpha and interleukin-1beta regulation. Journal of Biological Chemistry 1997, 272:8172-8178.
38. Bottazzi B., Vouret-Craviari V., Bastone A., De Gioia L., Matteucci C., Peri G., et al. Multimer formation and ligand recognition by the long pentraxin PTX3. Similarities and differences with the short pentraxins C-reactive protein and serum amyloid P component. Journal of Biological Chemisty 1997, 272:32817-32823.
39. Presta M., Camozzi M., Salvatori G., Rusnati M. Role of the soluble pattern recognition receptor PTX3 in vascular biology. Journal of Cellular and Molecular Medicine 2007, 11:723-738.
40. Inforzato A., Baldock C., Jowitt T.A., Holmes D.F., Lindstedt R., Marcellini M., et al. The angiogenic inhibitor long pentraxin PTX3 forms an asymmetric octamer with two binding sites for FGF2. Journal of Biological Chemistry 2010, 285:11768-17692.
41. Introna M., Alles V.V., Castellano M., Picardi G., De Gioia L., Bottazzi B., et al. Cloning of mouse PTX3, a new member of the pentraxin gene family expressed at extrahepatic sites. Blood 1996, 87:1862-1872.
42. Inforzato A., Peri G., Doni A., Garlanda C., Mantovani A., Bastone A., et al. Structure and function of the long pentraxin PTX3 glycosidic moiety: fine-tuning of the interaction with C1q and complement activation. Biochemistry 2006, 45:11540-11551.
43. Inforzato A., Rivieccio V., Morreale A.P., Bastone A., Salustri A., Scarchilli L., et al. Structural characterization of PTX3 disulfide bond network and its multimeric status in cumulus matrix organization. Journal of Biological Chemistry 2008, 283:10147-10161.
44. Deban L., Jarva H., Lehtinen M.J., Bottazzi B., Bastone A., Doni A., et al. Binding of the long pentraxin PTX3 to Factor H: interacting domains and function in the regulation of complement activation. Journal of Immunology 2008, 181:8433-8440.
45. Gout E., Moriscot C., Doni A., Dumestre-Perard C., Lacroix M., Perard J., et al. M-ficolin interacts with the long pentraxin PTX3: a novel case of cross-talk between soluble pattern-recognition molecules. Journal of Immunology 2011, 186:5815-5822.
46. Reading P.C., Bozza S., Gilbertson B., Tate M., Moretti S., Job E.R., et al. Antiviral activity of the long chain pentraxin ptx3 against influenza viruses. Journal of Immunology 2008, 180:3391-3398.
47. Deban L., Castro Russo R., Sironi M., Moalli F., Scanziani M., Zambelli V., et al. Regulation of leukocyte recruitment by the long pentraxin PTX3. Nature Immunology 2010, 11:328-334.
48. Bottazzi B., Garlanda C., Cotena A., Moalli F., Jaillon S., Deban L., et al. The long pentraxin PTX3 as a prototypic humoral pattern recognition receptor: interplay with cellular innate immunity. Immunological Reviews 2009, 227:9-18.
49. Norata G.D., Marchesi P., Pirillo A., Uboldi P., Chiesa G., Maina V., et al. Long pentraxin 3, a key component of innate immunity, is modulated by high-density lipoproteins in endothelial cells. Arteriosclerosis, Thrombosis, and Vascular Biology 2008, 28:925-931.
50. Sironi M., Conti A., Bernasconi S., Fra A.M., Pasqualini F., Nebuloni M., et al. Generation and characterization of a mouse lymphatic endothelial cell line. Cell and Tissue Research 2006, 325:91-100.
51. Jaillon S., Peri G., Delneste Y., Fremaux I., Doni A., Moalli F., et al. The humoral pattern recognition receptor PTX3 is stored in neutrophil granules and localizes in extracellular traps. Journal of Experimental Medicine 2007, 204:793-804.
52. Maina V., Cotena A., Doni A., Nebuloni M., Pasqualini F., Milner C.M., et al. Coregulation in human leukocytes of the long pentraxin PTX3 and TSG-6. Journal of Leukocyte Biology 2009, 86:123-132.
53. Doni A., Michela M., Bottazzi B., Peri G., Valentino S., Polentarutti N., et al. Regulation of PTX3, a key component of humoral innate immunity in human dendritic cells: stimulation by IL-10 and inhibition by IFN-gamma. Journal of Leukocyte Biology 2006, 79:797-802.
54. Doni A., Mantovani G., Porta C., Tuckermann J., Reichardt H.M., Kleiman A., et al. Cell-specific regulation of PTX3 by glucocorticoid hormones in hematopoietic and non-hematopoietic cells. Journal of Biological Chemistry 2008, 283:29983-29992.
55. Salio M., Chimenti S., De Angelis N., Molla F., Maina V., Nebuloni M., et al. Cardioprotective function of the long pentraxin PTX3 in acute myocardial infarction. Circulation 2008, 117:1055-1064.
56. Han B., Mura M., Andrade C.F., Okutani D., Lodyga M., dos Santos C.C., et al. TNFalpha-induced long pentraxin PTX3 expression in human lung epithelial cells via JNK. Journal of Immunology 2005, 175:8303-8311.
57. Ma Y.J., Doni A., Hummelshoj T., Honore C., Bastone A., Mantovani A., et al. Synergy between ficolin-2 and PTX3 boost innate immune recognition and complement deposition. Journal of Biological Chemistry 2009, [Epub ahead of print].
58. Ma Y.J., Doni A., Skjoedt M.O., Honore C., Arendrup M., Mantovani A., et al. Synergy between ficolin-2 and PTX3 boost innate immune recognition and complement deposition. Journal of Biological Chemistry 2009, 284:28263-28275.
59. Braunschweig A., Jozsi M. Human pentraxin 3 binds to the complement regulator c4b-binding protein. PLoS ONE 2011, 6:e23991.
60. Garlanda C., Hirsch E., Bozza S., Salustri A., De Acetis M., Nota R., et al. Non-redundant role of the long pentraxin PTX3 in anti-fungal innate immune response. Nature 2002, 420:182-186.
61. Diniz S.N., Nomizo R., Cisalpino P.S., Teixeira M.M., Brown G.D., Mantovani A., et al. PTX3 function as an opsonin for the dectin-1-dependent internalization of zymosan by macrophages. Journal of Leukocyte Biology 2004, 75:649-656.
62. Jeannin P., Bottazzi B., Sironi M., Doni A., Rusnati M., Presta M., et al. Complexity and complementarity of outer membrane protein A recognition by cellular and humoral innate immunity receptors. Immunity 2005, 22:551-560.
63. Moalli F., Paroni M., Veliz Rodriguez T., Riva F., Polentarutti N., Bottazzi B., et al. The therapeutic potential of the humoral pattern recognition molecule PTX3 in chronic lung infection caused by pseudomonas aeruginosa. Journal of Immunology 2011, 186:5425-5434.
64. Bozza S., Bistoni F., Gaziano R., Pitzurra L., Zelante T., Bonifazi P., et al. Pentraxin 3 protects from MCMV infection and reactivation through TLR sensing pathways leading to IRF3 activation. Blood 2006, 108:3387-3396.
65. Cotena A., Maina V., Sironi M., Bottazzi B., Jeannin P., Vecchi A., et al. Complement dependent amplification of the innate response to a cognate microbial ligand by the long pentraxin PTX3. Journal of Immunology 2007, 179:6311-6317.
66. Moalli F., Doni A., Deban L., Zelante T., Zagarella S., Bottazzi B., et al. Role of complement and Fc gamma receptors in the protective activity of the long pentraxin PTX3 against Aspergillus fumigatus. Blood 2010, 116:5170-5180.
67. Peri G., Introna M., Corradi D., Iacuitti G., Signorini S., Avanzini F., et al. PTX3, a prototypical long pentraxin, is an early indicator of acute myocardial infarction in humans. Circulation 2000, 102:636-641.
68. Lech M., Rommele C., Grobmayr R., Eka Susanti H., Kulkarni O.P., Wang S., et al. Endogenous and exogenous pentraxin-3 limits postischemic acute and chronic kidney injury. Kidney International 2013, 83:647-661.
69. Han B., Haitsma J.J., Zhang Y., Bai X., Rubacha M., Keshavjee S., et al. Long pentraxin PTX3 deficiency worsens LPS-induced acute lung injury. Intensive Care Medicine 2011, 37:334-342.
70. Jeannin P., Jaillon S., Delneste Y. Pattern recognition receptors in the immune response against dying cells. Current Opinion in Immunology 2008, 20:530-537.
71. Rovere P., Peri G., Fazzini F., Bottazzi B., Doni A., Bondanza A., et al. The long pentraxin PTX3 binds to apoptotic cells and regulates their clearance by antigen-presenting dendritic cells. Blood 2000, 96:4300-4306.
72. Baruah P., Dumitriu I.E., Peri G., Russo V., Mantovani A., Manfredi A.A., et al. The tissue pentraxin PTX3 limits C1q-mediated complement activation and phagocytosis of apoptotic cells by dendritic cells. Journal of Leukocyte Biology 2006, 80:87-95.
73. van Rossum A.P., Fazzini F., Limburg P.C., Manfredi A.A., Rovere-Querini P., Mantovani A., et al. The prototypic tissue pentraxin PTX3, in contrast to the short pentraxin serum amyloid P, inhibits phagocytosis of late apoptotic neutrophils by macrophages. Arthritis and Rheumatism 2004, 50:2667-2674.
74. Jaillon S., Jeannin P., Hamon Y., Fremaux I., Doni A., Bottazzi B., et al. Endogenous PTX3 translocates at the membrane of late apoptotic human neutrophils and is involved in their engulfment by macrophages. Cell Death and Differentiation 2009, 16:465-474.
75. Lech M., Rommele C., Kulkarni O.P., Susanti H.E., Migliorini A., Garlanda C., et al. Lack of the long pentraxin PTX3 promotes autoimmune lung disease but not glomerulonephritis in murine systemic lupus erythematosus. PLoS ONE 2011, 6:e20118.
76. Trouw L.A., Bengtsson A.A., Gelderman K.A., Dahlback B., Sturfelt G., Blom A.M. C4b-binding protein and factor H compensate for the loss of membrane-bound complement inhibitors to protect apoptotic cells against excessive complement attack. Journal of Biological Chemistry 2007, 282:28540-28548.
77. Lo Giudice P., Campo S., De Santis R., Salvatori G Effect of PTX3 and voriconazole combination in a rat model of invasive pulmonary aspergillosis. Antimicrobial Agents and Chemotherapy 2012, 56:6400-6402.
78. Lo Giudice P., Campo S., Verdoliva A., Rivieccio V., Borsini F., De Santis R., et al. Efficacy of PTX3 in a rat model of invasive aspergillosis. Antimicrobial Agents and Chemotherapy 2010, 54:4513-4515.
79. Bally I., Ancelet S., Moriscot C., Gonnet F., Mantovani A., Daniel R., et al. Expression of recombinant human complement C1q allows identification of the C1r/C1s-binding sites. Proceedings of the National Academy of Sciences of the United States of America 2013, 110:8650-8655.