Cell and Tissue Research

, Volume 343, Issue 1, pp 237–249 | Cite as

Pentraxins in innate immunity: lessons from PTX3

  • Livija Deban
  • Sebastien Jaillon
  • Cecilia Garlanda
  • Barbara Bottazzi
  • Alberto Mantovani
Review

Abstract

The innate immune system constitutes the first line of defence against microorganisms and plays a primordial role in the activation and regulation of adaptive immunity. The innate immune system is composed of a cellular arm and a humoral arm. Components of the humoral arm include members of the complement cascade and soluble pattern recognition molecules (PRMs). These fluid-phase PRMs represent the functional ancestors of antibodies and play a crucial role in the discrimination between self, non-self and modified-self. Moreover, evidence has been presented that these soluble PRMs participate in the regulation of inflammatory responses and interact with the cellular arm of the innate immune system. Pentraxins consist of a set of multimeric soluble proteins and represent the prototypic components of humoral innate immunity. Based on the primary structure of the protomer, pentraxins are divided into two groups: short pentraxins and long pentraxins. The short pentraxins C-reactive protein and serum amyloid P-component are produced by the liver and represent the main acute phase proteins in human and mouse, respectively. The long pentraxin PTX3 is produced by innate immunity cells (e.g. PMN, macrophages, dendritic cells), interacts with several ligands and plays an essential role in innate immunity, tuning inflammation and matrix deposition. PTX3 provides a paradigm for the mode of action of humoral innate immunity.

Keywords

Innate immunity Inflammation Pattern recognition Pentraxins PTX3 

References

  1. Abderrahim-Ferkoune A, Bezy O, Chiellini C, Maffei M, Grimaldi P, Bonino F, Moustaid-Moussa N, Pasqualini F, Mantovani A, Ailhaud G, Amri EZ (2003) Characterization of the long pentraxin PTX3 as a TNFalpha-induced secreted protein of adipose cells. J Lipid Res 44:994–1000PubMedGoogle Scholar
  2. Abernethy TJ, Avery OT (1941) The occurrence during acute infections of a protein not normally present in the blood. I. Distribution of the reactive protein in patients' sera and the effect of calcium on the flocculation reaction with C polysaccharide of pneumococcus. J Exp Med 73:173–182PubMedGoogle Scholar
  3. Akira S, Uematsu S, Takeuchi O (2006) Pathogen recognition and innate immunity. Cell 124:783–801PubMedGoogle Scholar
  4. Alles VV, Bottazzi B, Peri G, Golay J, Introna M, Mantovani A (1994) Inducible expression of PTX3, a new member of the pentraxin family, in human mononuclear phagocytes. Blood 84:3483–3493PubMedGoogle Scholar
  5. Altmeyer A, Klampfer L, Goodman AR, Vilcek J (1995) Promoter structure and transcriptional activation of the murine TSG-14 gene encoding a tumor necrosis factor/interleukin-1-inducible pentraxin protein. J Biol Chem 270:25584–25590PubMedGoogle Scholar
  6. Armstrong PB, Swarnakar S, Srimal S, Misquith S, Hahn EA, Aimes RT, Quigley JP (1996) A cytolytic function for a sialic acid-binding lectin that is a member of the pentraxin family of proteins. J Biol Chem 271:14717–14721PubMedGoogle Scholar
  7. Assi F, Fruscio R, Bonardi C, Ghidini A, Allavena P, Mantovani A, Locatelli A (2007) Pentraxin 3 in plasma and vaginal fluid in women with preterm delivery. Br J Obstet Gynaecol 114:143–147Google Scholar
  8. Augusto JF, Onno C, Blanchard S, Dubuquoi S, Mantovani A, Chevailler A, Jeannin P, Subra JF (2009) Detection of anti-PTX3 autoantibodies in systemic lupus erythematosus. Rheumatology (Oxford) 48:442–444Google Scholar
  9. Azzurri A, Sow OY, Amedei A, Bah B, Diallo S, Peri G, Benagiano M, D'Elios MM, Mantovani A, Del Prete G (2005) IFN-gamma-inducible protein 10 and pentraxin 3 plasma levels are tools for monitoring inflammation and disease activity in Mycobacterium tuberculosis infection. Microbes Infect 7:1–8PubMedGoogle Scholar
  10. Baruah P, Dumitriu IE, Peri G, Russo V, Mantovani A, Manfredi AA, Rovere-Querini P (2006a) The tissue pentraxin PTX3 limits C1q-mediated complement activation and phagocytosis of apoptotic cells by dendritic cells. J Leukoc Biol 80:87–95PubMedGoogle Scholar
  11. Baruah P, Propato A, Dumitriu IE, Rovere-Querini P, Russo V, Fontana R, Accapezzato D, Peri G, Mantovani A, Barnaba V, Manfredi AA (2006b) The pattern recognition receptor PTX3 is recruited at the synapse between dying and dendritic cells, and edits the cross-presentation of self, viral, and tumor antigens. Blood 107:151–158PubMedGoogle Scholar
  12. Basile A, Sica A, d'Aniello E, Breviario F, Garrido G, Castellano M, Mantovani A, Introna M (1997) Characterization of the promoter for the human long pentraxin PTX3. Role of NF-kappaB in tumor necrosis factor-alpha and interleukin-1beta regulation. J Biol Chem 272:8172–8178PubMedGoogle Scholar
  13. Bharadwaj D, Stein MP, Volzer M, Mold C, Du Clos TW (1999) The major receptor for C-reactive protein on leukocytes is Fcgamma receptor II. J Exp Med 190:585–590PubMedGoogle Scholar
  14. Bickerstaff MC, Botto M, Hutchinson WL, Herbert J, Tennent GA, Bybee A, Mitchell DA, Cook HT, Butler PJ, Walport MJ, Pepys MB (1999) Serum amyloid P component controls chromatin degradation and prevents antinuclear autoimmunity. Nat Med 5:694–697PubMedGoogle Scholar
  15. Bottazzi B, Vouret-Craviari V, Bastone A, De Gioia L, Matteucci C, Peri G, Spreafico F, Pausa M, D'Ettorre C, Gianazza E, Tagliabue A, Salmona M, Tedesco F, Introna M, Mantovani A (1997) 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. J Biol Chem 272:32817–32823PubMedGoogle Scholar
  16. Bottazzi B, Garlanda C, Cotena A, Moalli F, Jaillon S, Deban L, Mantovani A (2009) The long pentraxin PTX3 as a prototypic humoral pattern recognition receptor: interplay with cellular innate immunity. Immunol Rev 227:9–18PubMedGoogle Scholar
  17. Bottazzi B, Doni A, Garlanda C, Mantovani A (2010) An integrated view of humoral innate immunity: pentraxins as a paradigm. Annu Rev Immunol 28:157–183PubMedGoogle Scholar
  18. Botto M, Hawkins PN, Bickerstaff MC, Herbert J, Bygrave AE, McBride A, Hutchinson WL, Tennent GA, Walport MJ, Pepys MB (1997) Amyloid deposition is delayed in mice with targeted deletion of the serum amyloid P component gene. Nat Med 3:855–859PubMedGoogle Scholar
  19. Bozza S, Bistoni F, Gaziano R, Pitzurra L, Zelante T, Bonifazi P, Perruccio K, Bellocchio S, Neri M, Iorio AM, Salvatori G, De Santis R, Calvitti M, Doni A, Garlanda C, Mantovani A, Romani L (2006) Pentraxin 3 protects from MCMV infection and reactivation through TLR sensing pathways leading to IRF3 activation. Blood 108:3387–3396PubMedGoogle Scholar
  20. Breviario F, d'Aniello EM, Golay J, Peri G, Bottazzi B, Bairoch A, Saccone S, Marzella R, Predazzi V, Rocchi M, Della Valle G, Dejana E, Mantovani A, Introna M (1992) Interleukin-1-inducible genes in endothelial cells. Cloning of a new gene related to C-reactive protein and serum amyloid P component. J Biol Chem 267:22190–22197PubMedGoogle Scholar
  21. Brugger-Andersen T, Ponitz V, Kontny F, Staines H, Grundt H, Sagara M, Nilsen DW (2009) The long pentraxin 3 (PTX3): a novel prognostic inflammatory marker for mortality in acute chest pain. Thromb Haemost 102:555–563PubMedGoogle Scholar
  22. Cetin I, Cozzi V, Pasqualini F, Nebuloni M, Garlanda C, Vago L, Pardi G, Mantovani A (2006) Elevated maternal levels of the long pentraxin 3 (PTX3) in preeclampsia and intrauterine growth restriction. Am J Obstet Gynecol 194:1347–1353PubMedGoogle Scholar
  23. Cotena A, Maina V, Sironi M, Bottazzi B, Jeannin P, Vecchi A, Corvaia N, Daha MR, Mantovani A, Garlanda C (2007) Complement dependent amplification of the innate response to a cognate microbial ligand by the long pentraxin PTX3. J Immunol 179:6311–6317PubMedGoogle Scholar
  24. D'Angelo C, De Luca A, Zelante T, Bonifazi P, Moretti S, Giovannini G, Iannitti RG, Zagarella S, Bozza S, Campo S, Salvatori G, Romani L (2009) Exogenous pentraxin 3 restores antifungal resistance and restrains inflammation in murine chronic granulomatous disease. J Immunol 183:4609–4618PubMedGoogle Scholar
  25. Deban L, Jarva H, Lehtinen MJ, Bottazzi B, Bastone A, Doni A, Jokiranta TS, Mantovani A, Meri S (2008) Binding of the long pentraxin PTX3 to Factor H: interacting domains and function in the regulation of complement activation. J Immunol 181:8433–8440PubMedGoogle Scholar
  26. Deban L, Bottazzi B, Garlanda C, Torre YM de la, Mantovani A (2009) Pentraxins: multifunctional proteins at the interface of innate immunity and inflammation. Biofactors 35:138–145PubMedGoogle Scholar
  27. Deban L, Russo RC, Sironi M, Moalli F, Scanziani M, Zambelli V, Cuccovillo I, Bastone A, Gobbi M, Valentino S, Doni A, Garlanda C, Danese S, Salvatori G, Sassano M, Evangelista V, Rossi B, Zenaro E, Constantin G, Laudanna C, Bottazzi B, Mantovani A (2010) Regulation of leukocyte recruitment by the long pentraxin PTX3. Nat Immunol 11:328–334PubMedGoogle Scholar
  28. Dias AA, Goodman AR, Dos Santos JL, Gomes RN, Altmeyer A, Bozza PT, Horta MF, Vilcek J, Reis LF (2001) TSG-14 transgenic mice have improved survival to endotoxemia and to CLP-induced sepsis. J Leukoc Biol 69:928–936PubMedGoogle Scholar
  29. Diniz SN, Nomizo R, Cisalpino PS, Teixeira MM, Brown GD, Mantovani A, Gordon S, Reis LF, Dias AA (2004) PTX3 function as an opsonin for the dectin-1-dependent internalization of zymosan by macrophages. J Leukoc Biol 75:649–656PubMedGoogle Scholar
  30. Doni A, Peri G, Chieppa M, Allavena P, Pasqualini F, Vago L, Romani L, Garlanda C, Mantovani A (2003) Production of the soluble pattern recognition receptor PTX3 by myeloid, but not plasmacytoid, dendritic cells. Eur J Immunol 33:2886–2893PubMedGoogle Scholar
  31. Doni A, Michela M, Bottazzi B, Peri G, Valentino S, Polentarutti N, Garlanda C, Mantovani A (2006) Regulation of PTX3, a key component of humoral innate immunity in human dendritic cells: stimulation by IL-10 and inhibition by IFN-gamma. J Leukoc Biol 79:797–802PubMedGoogle Scholar
  32. Doni A, Mantovani G, Porta C, Tuckermann J, Reichardt HM, Kleiman A, Sironi M, Rubino L, Pasqualini F, Nebuloni M, Signorini S, Peri G, Sica A, Beck-Peccoz P, Bottazzi B, Mantovani A (2008) Cell-specific regulation of ptx3 by glucocorticoid hormones in hematopoietic and nonhematopoietic cells. J Biol Chem 283:29983–29992PubMedGoogle Scholar
  33. Elliott P, Chambers JC, Zhang W, Clarke R, Hopewell JC, Peden JF, Erdmann J, Braund P, Engert JC, Bennett D, Coin L, Ashby D, Tzoulaki I, Brown IJ, Mt-Isa S, McCarthy MI, Peltonen L, Freimer NB, Farrall M, Ruokonen A, Hamsten A, Lim N, Froguel P, Waterworth DM, Vollenweider P, Waeber G, Jarvelin MR, Mooser V, Scott J, Hall AS, Schunkert H, Anand SS, Collins R, Samani NJ, Watkins H, Kooner JS (2009) Genetic loci associated with C-reactive protein levels and risk of coronary heart disease. JAMA 302:37–48PubMedGoogle Scholar
  34. Emsley J, White HE, O'Hara BP, Oliva G, Srinivasan N, Tickle IJ, Blundell TL, Pepys MB, Wood SP (1994) Structure of pentameric human serum amyloid P component. Nature 367:338–345PubMedGoogle Scholar
  35. Endo Y, Matsushita M, Fujita T (2007) Role of ficolin in innate immunity and its molecular basis. Immunobiology 212:371–379PubMedGoogle Scholar
  36. Fazzini F, Peri G, Doni A, Dell'Antonio G, Dal Cin E, Bozzolo E, D'Auria F, Praderio L, Ciboddo G, Sabbadini MG, Manfredi AA, Mantovani A, Querini PR (2001) PTX3 in small-vessel vasculitides: an independent indicator of disease activity produced at sites of inflammation. Arthritis Rheum 44:2841–2850PubMedGoogle Scholar
  37. Garlanda C, Hirsch E, Bozza S, Salustri A, De Acetis M, Nota R, Maccagno A, Riva F, Bottazzi B, Peri G, Doni A, Vago L, Botto M, De Santis R, Carminati P, Siracusa G, Altruda F, Vecchi A, Romani L, Mantovani A (2002) Non-redundant role of the long pentraxin PTX3 in anti-fungal innate immune response. Nature 420:182–186PubMedGoogle Scholar
  38. Garlanda C, Bottazzi B, Bastone A, Mantovani A (2005) Pentraxins at the crossroads between innate immunity, inflammation, matrix deposition, and female fertility. Annu Rev Immunol 23:337–366PubMedGoogle Scholar
  39. Gaziano R, Bozza S, Bellocchio S, Perruccio K, Montagnoli C, Pitzurra L, Salvatori G, De Santis R, Carminati P, Mantovani A, Romani L (2004) Anti-Aspergillus fumigatus efficacy of pentraxin 3 alone and in combination with antifungals. Antimicrob Agents Chemother 48:4414–4421PubMedGoogle Scholar
  40. Gershov D, Kim S, Brot N, Elkon KB (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 192:1353–1364PubMedGoogle Scholar
  41. Gillmore JD, Hutchinson WL, Herbert J, Bybee A, Mitchell DA, Hasserjian RP, Yamamura K, Suzuki M, Sabin CA, Pepys MB (2004) Autoimmunity and glomerulonephritis in mice with targeted deletion of the serum amyloid P component gene: SAP deficiency or strain combination? Immunology 112:255–264PubMedGoogle Scholar
  42. Goodman AR, Levy DE, Reis LF, Vilcek J (2000) Differential regulation of TSG-14 expression in murine fibroblasts and peritoneal macrophages. J Leukoc Biol 67:387–395PubMedGoogle Scholar
  43. Haas CJ de, Leeuwen EM van, Bommel T van, Verhoef J, Kessel KP van, Strijp JA van (2000) Serum amyloid P component bound to gram-negative bacteria prevents lipopolysaccharide-mediated classical pathway complement activation. Infect Immun 68:1753–1759PubMedGoogle Scholar
  44. Han B, Mura M, Andrade CF, Okutani D, Lodyga M, Santos CC dos, Keshavjee S, Matthay M, Liu M (2005) TNFalpha-induced long pentraxin PTX3 expression in human lung epithelial cells via JNK. J Immunol 175:8303–8311PubMedGoogle Scholar
  45. Holmskov U, Thiel S, Jensenius JC (2003) Collectins and ficolins: humoral lectins of the innate immune defense. Annu Rev Immunol 21:547–578PubMedGoogle Scholar
  46. Inforzato A, Peri G, Doni A, Garlanda C, Mantovani A, Bastone A, Carpentieri A, Amoresano A, Pucci P, Roos A, Daha MR, Vincenti S, Gallo G, Carminati P, De Santis R, Salvatori G (2006) Structure and function of the long pentraxin PTX3 glycosidic moiety: fine-tuning of the interaction with C1q and complement activation. Biochemistry 45:11540–11551PubMedGoogle Scholar
  47. Inforzato A, Rivieccio V, Morreale AP, Bastone A, Salustri A, Scarchilli L, Verdoliva A, Vincenti S, Gallo G, Chiapparino C, Pacello L, Nucera E, Serlupi-Crescenzi O, Day AJ, Bottazzi B, Mantovani A, De Santis R, Salvatori G (2008) Structural characterization of PTX3 disulfide bond network and its multimeric status in cumulus matrix organization. J Biol Chem 283:10147–10161PubMedGoogle Scholar
  48. Inforzato A, Baldock C, Jowitt TA, Holmes DF, Lindstedt R, Marcellini M, Rivieccio V, Briggs DC, Kadler KE, Verdoliva A, Bottazzi B, Mantovani A, Salvatori G, Day AJ (2010) The angiogenic inhibitor long pentraxin PTX3 forms an asymmetric octamer with two binding sites for FGF2. J Biol Chem 285:17681–17692PubMedGoogle Scholar
  49. Inoue K, Sugiyama A, Reid PC, Ito Y, Miyauchi K, Mukai S, Sagara M, Miyamoto K, Satoh H, Kohno I, Kurata T, Ota H, Mantovani A, Hamakubo T, Daida H, Kodama T (2007) Establishment of a high sensitivity plasma assay for human pentraxin3 as a marker for unstable angina pectoris. Arterioscler Thromb Vasc Biol 27:161–167PubMedGoogle Scholar
  50. Introna M, Alles VV, Castellano M, Picardi G, De Gioia L, Bottazzai B, Peri G, Breviario F, Salmona M, De Gregorio L, Dragani TA, Srinivasan N, Blundell TL, Hamilton TA, Mantovani A (1996) Cloning of mouse ptx3, a new member of the pentraxin gene family expressed at extrahepatic sites. Blood 87:1862–1872PubMedGoogle Scholar
  51. Iwasaki A, Medzhitov R (2010) Regulation of adaptive immunity by the innate immune system. Science 327:291–295PubMedGoogle Scholar
  52. Jaillon S, Peri G, Delneste Y, Fremaux I, Doni A, Moalli F, Garlanda C, Romani L, Gascan H, Bellocchio S, Bozza S, Cassatella MA, Jeannin P, Mantovani A (2007) The humoral pattern recognition receptor PTX3 is stored in neutrophil granules and localizes in extracellular traps. J Exp Med 204:793–804PubMedGoogle Scholar
  53. Jaillon S, Jeannin P, Hamon Y, Fremaux I, Doni A, Bottazzi B, Blanchard S, Subra JF, Chevailler A, Mantovani A, Delneste Y (2009) Endogenous PTX3 translocates at the membrane of late apoptotic human neutrophils and is involved in their engulfment by macrophages. Cell Death Differ 16:465–474PubMedGoogle Scholar
  54. Jarva H, Jokiranta TS, Hellwage J, Zipfel PF, Meri S (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 163:3957–3962PubMedGoogle Scholar
  55. Jeannin P, Bottazzi B, Sironi M, Doni A, Rusnati M, Presta M, Maina V, Magistrelli G, Haeuw JF, Hoeffel G, Thieblemont N, Corvaia N, Garlanda C, Delneste Y, Mantovani A (2005) Complexity and complementarity of outer membrane protein A recognition by cellular and humoral innate immunity receptors. Immunity 22:551–560PubMedGoogle Scholar
  56. Jeannin P, Jaillon S, Delneste Y (2008) Pattern recognition receptors in the immune response against dying cells. Curr Opin Immunol 20:530–537PubMedGoogle Scholar
  57. Jenny NS, Arnold AM, Kuller LH, Tracy RP, Psaty BM (2009) Associations of pentraxin 3 with cardiovascular disease and all-cause death: the Cardiovascular Health Study. Arterioscler Thromb Vasc Biol 29:594–599PubMedGoogle Scholar
  58. Kaneko Y, Nimmerjahn F, Ravetch JV (2006) Anti-inflammatory activity of immunoglobulin G resulting from Fc sialylation. Science 313:670–673PubMedGoogle Scholar
  59. Latini R, Maggioni AP, Peri G, Gonzini L, Lucci D, Mocarelli P, Vago L, Pasqualini F, Signorini S, Soldateschi D, Tarli L, Schweiger C, Fresco C, Cecere R, Tognoni G, Mantovani A (2004) Prognostic significance of the long pentraxin PTX3 in acute myocardial infarction. Circulation 110:2349–2354PubMedGoogle Scholar
  60. Lee GW, Lee TH, Vilcek J (1993) TSG-14, a tumor necrosis factor- and IL-1-inducible protein, is a novel member of the pentaxin family of acute phase proteins. J Immunol 150:1804–1812PubMedGoogle Scholar
  61. Lu J, Marnell LL, Marjon KD, Mold C, Du Clos TW, Sun PD (2008) Structural recognition and functional activation of FcgammaR by innate pentraxins. Nature 456:989–992PubMedGoogle Scholar
  62. Luchetti MM, Piccinini G, Mantovani A, Peri G, Matteucci C, Pomponio G, Fratini M, Fraticelli P, Sambo P, Di Loreto C, Doni A, Introna M, Gabrielli A (2000) Expression and production of the long pentraxin PTX3 in rheumatoid arthritis (RA). Clin Exp Immunol 119:196–202PubMedGoogle Scholar
  63. Ma YJ, Doni A, Hummelshoj T, Honore C, Bastone A, Mantovani A, Thielens NM, Garred P (2009) Synergy between ficolin-2 and pentraxin 3 boosts innate immune recognition and complement deposition. J Biol Chem 284:28263–28275PubMedGoogle Scholar
  64. Mairuhu AT, Peri G, Setiati TE, Hack CE, Koraka P, Soemantri A, Osterhaus AD, Brandjes DP, Meer JW van der, Mantovani A, Gorp EC van (2005) Elevated plasma levels of the long pentraxin, pentraxin 3, in severe dengue virus infections. J Med Virol 76:547–552PubMedGoogle Scholar
  65. Mantovani A, Garlanda C, Doni A, Bottazzi B (2008) Pentraxins in innate immunity: from C-reactive protein to the long pentraxin PTX3. J Clin Immunol 28:1–13PubMedGoogle Scholar
  66. Martinez de la Torre Y, Fabbri M, Jaillon S, Bastone A, Nebuloni M, Vecchi A, Mantovani A, Garlanda C (2010) Evolution of the pentraxin family: the new entry PTX4. J Immunol 184:5055–5064PubMedGoogle Scholar
  67. Matsui S, Ishii J, Kitagawa F, Kuno A, Hattori K, Ishikawa M, Okumura M, Kan S, Nakano T, Naruse H, Tanaka I, Nomura M, Hishida H, Ozaki Y (2010) Pentraxin 3 in unstable angina and non-ST-segment elevation myocardial infarction. Atherosclerosis 210:220–225PubMedGoogle Scholar
  68. Mauri T, Bellani G, Patroniti N, Coppadoro A, Peri G, Cuccovillo I, Cugno M, Iapichino G, Gattinoni L, Pesenti A, Mantovani A (2010) Persisting high levels of plasma pentraxin 3 over the first days after severe sepsis and septic shock onset are associated with mortality. Intensive Care Med 36:621–629PubMedGoogle Scholar
  69. Mihlan M, Stippa S, Jozsi M, Zipfel PF (2009) Monomeric CRP contributes to complement control in fluid phase and on cellular surfaces and increases phagocytosis by recruiting Factor H. Cell Death Differ 16:1630–1640PubMedGoogle Scholar
  70. Miyaki A, Maeda S, Yoshizawa M, Misono M, Sasai H, Shimojo N, Tanaka K, Ajisaka R (2010) Is pentraxin 3 involved in obesity-induced decrease in arterial distensibility? J Atheroscler Thromb 17:278–284PubMedGoogle Scholar
  71. Mold C, Gewurz H (1981) Inhibitory effect of C-reactive protein on alternative C pathway activation by liposomes and Streptococcus pneumoniae. J Immunol 127:2089–2092PubMedGoogle Scholar
  72. Mold C, Gresham HD, Du Clos TW (2001) Serum amyloid P component and C-reactive protein mediate phagocytosis through murine Fc gamma Rs. J Immunol 166:1200–1205PubMedGoogle Scholar
  73. Murphy JE, Tedbury PR, Homer-Vanniasinkam S, Walker JH, Ponnambalam S (2005) Biochemistry and cell biology of mammalian scavenger receptors. Atherosclerosis 182:1–15PubMedGoogle Scholar
  74. Nauta AJ, Bottazzi B, Mantovani A, Salvatori G, Kishore U, Schwaeble WJ, Gingras AR, Tzima S, Vivanco F, Egido J, Tijsma O, Hack EC, Daha MR, Roos A (2003a) Biochemical and functional characterization of the interaction between pentraxin 3 and C1q. Eur J Immunol 33:465–473PubMedGoogle Scholar
  75. Nauta AJ, Daha MR, Kooten C van, Roos A (2003b) Recognition and clearance of apoptotic cells: a role for complement and pentraxins. Trends Immunol 24:148–154PubMedGoogle Scholar
  76. Nauta AJ, Haij S de, Bottazzi B, Mantovani A, Borrias MC, Aten J, Rastaldi MP, Daha MR, Kooten C van, Roos A (2005) Human renal epithelial cells produce the long pentraxin PTX3. Kidney Int 67:543–553PubMedGoogle Scholar
  77. Ng PM, Le Saux A, Lee CM, Tan NS, Lu J, Thiel S, Ho B, Ding JL (2007) C-reactive protein collaborates with plasma lectins to boost immune response against bacteria. EMBO J 26:3431–3440PubMedGoogle Scholar
  78. Norata GD, Marchesi P, Pulakazhi Venu VK, Pasqualini F, Anselmo A, Moalli F, Pizzitola I, Garlanda C, Mantovani A, Catapano AL (2009) Deficiency of the long pentraxin PTX3 promotes vascular inflammation and atherosclerosis. Circulation 120:699–708PubMedGoogle Scholar
  79. Noursadeghi M, Bickerstaff MC, Gallimore JR, Herbert J, Cohen J, Pepys MB (2000) Role of serum amyloid P component in bacterial infection: protection of the host or protection of the pathogen. Proc Natl Acad Sci USA 97:14584–14589PubMedGoogle Scholar
  80. Ogawa T, Kawano Y, Imamura T, Kawakita K, Sagara M, Matsuo T, Kakitsubata Y, Ishikawa T, Kitamura K, Hatakeyama K, Asada Y, Kodama T (2010) Reciprocal contribution of pentraxin 3 and C-reactive protein to obesity and metabolic syndrome. Obesity (Silver Spring) (in press)Google Scholar
  81. Okemefuna AI, Nan R, Miller A, Gor J, Perkins SJ (2010) Complement Factor H binds at two independent sites to C-reactive protein in acute phase concentrations. J Biol Chem 285:1053–1065PubMedGoogle Scholar
  82. Pepys MB, Hirschfield GM (2003) C-reactive protein: a critical update. J Clin Invest 111:1805–1812PubMedGoogle Scholar
  83. Peri G, Introna M, Corradi D, Iacuitti G, Signorini S, Avanzini F, Pizzetti F, Maggioni AP, Moccetti T, Metra M, Cas LD, Ghezzi P, Sipe JD, Re G, Olivetti G, Mantovani A, Latini R (2000) PTX3, a prototypical long pentraxin, is an early indicator of acute myocardial infarction in humans. Circulation 102:636–641PubMedGoogle Scholar
  84. Polentarutti N, Picardi G, Basile A, Cenzuales S, Rivolta A, Matteucci C, Peri G, Mantovani A, Introna M (1998) Interferon-gamma inhibits expression of the long pentraxin PTX3 in human monocytes. Eur J Immunol 28:496–501PubMedGoogle Scholar
  85. Poon IK, Hulett MD, Parish CR (2010) Molecular mechanisms of late apoptotic/necrotic cell clearance. Cell Death Differ 17:381–397PubMedGoogle Scholar
  86. Ravizza T, Moneta D, Bottazzi B, Peri G, Garlanda C, Hirsch E, Richards GJ, Mantovani A, Vezzani A (2001) Dynamic induction of the long pentraxin PTX3 in the CNS after limbic seizures: evidence for a protective role in seizure-induced neurodegeneration. Neuroscience 105:43–53PubMedGoogle Scholar
  87. Reading PC, Bozza S, Gilbertson B, Tate M, Moretti S, Job ER, Crouch EC, Brooks AG, Brown LE, Bottazzi B, Romani L, Mantovani A (2008) Antiviral activity of the long chain pentraxin PTX3 against influenza viruses. J Immunol 180:3391–3398PubMedGoogle Scholar
  88. Robey FA, Liu TY (1981) Limulin: a C-reactive protein from Limulus polyphemus. J Biol Chem 256:969–975PubMedGoogle Scholar
  89. Rossum AP van, Fazzini F, Limburg PC, Manfredi AA, Rovere-Querini P, Mantovani A, Kallenberg CG (2004) The prototypic tissue pentraxin PTX3, in contrast to the short pentraxin serum amyloid P, inhibits phagocytosis of late apoptotic neutrophils by macrophages. Arthritis Rheum 50:2667–2674PubMedGoogle Scholar
  90. Roumenina LT, Ruseva MM, Zlatarova A, Ghai R, Kolev M, Olova N, Gadjeva M, Agrawal A, Bottazzi B, Mantovani A, Reid KB, Kishore U, Kojouharova MS (2006) 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 45:4093–4104PubMedGoogle Scholar
  91. Rovere-Querini P, Antonacci S, Dell'Antonio G, Angeli A, Almirante G, Cin ED, Valsecchi L, Lanzani C, Sabbadini MG, Doglioni C, Manfredi AA, Castiglioni MT (2006) Plasma and tissue expression of the long pentraxin 3 during normal pregnancy and preeclampsia. Obstet Gynecol 108:148–155PubMedGoogle Scholar
  92. Rubio N, Sharp PM, Rits M, Zahedi K, Whitehead AS (1993) Structure, expression, and evolution of guinea pig serum amyloid P component and C-reactive protein. J Biochem 113:277–284PubMedGoogle Scholar
  93. Saeland E, Royen A van, Hendriksen K, Vile-Weekhout H, Rijkers GT, Sanders LA, Winkel JG van de (2001) Human C-reactive protein does not bind to FcgammaRIIa on phagocytic cells. J Clin Invest 107:641–643PubMedGoogle Scholar
  94. Salio M, Chimenti S, De Angelis N, Molla F, Maina V, Nebuloni M, Pasqualini F, Latini R, Garlanda C, Mantovani A (2008) Cardioprotective function of the long pentraxin PTX3 in acute myocardial infarction. Circulation 117:1055–1064PubMedGoogle Scholar
  95. Santos CC dos, Han B, Andrade CF, Bai X, Uhlig S, Hubmayr R, Tsang M, Lodyga M, Keshavjee S, Slutsky AS, Liu M (2004) DNA microarray analysis of gene expression in alveolar epithelial cells in response to TNFalpha, LPS, and cyclic stretch. Physiol Genomics 19:331–342PubMedGoogle Scholar
  96. Schwalbe RA, Dahlback B, Coe JE, Nelsestuen GL (1992) Pentraxin family of proteins interact specifically with phosphorylcholine and/or phosphorylethanolamine. Biochemistry 31:4907–4915PubMedGoogle Scholar
  97. Seery LT, Schoenberg DR, Barbaux S, Sharp PM, Whitehead AS (1993) Identification of a novel member of the pentraxin family in Xenopus laevis. Proc Biol Sci 253:263–270PubMedGoogle Scholar
  98. Shrive AK, Metcalfe AM, Cartwright JR, Greenhough TJ (1999) C-reactive protein and SAP-like pentraxin are both present in Limulus polyphemus haemolymph: crystal structure of Limulus SAP. J Mol Biol 290:997–1008PubMedGoogle Scholar
  99. Souza DG, Amaral FA, Fagundes CT, Coelho FM, Arantes RM, Sousa LP, Matzuk MM, Garlanda C, Mantovani A, Dias AA, Teixeira MM (2009) The long pentraxin PTX3 is crucial for tissue inflammation after intestinal ischemia and reperfusion in mice. Am J Pathol. 174:1309-1318PubMedGoogle Scholar
  100. Sprong T, Peri G, Neeleman C, Mantovani A, Signorini S, Meer JW van der, Deuren M van (2009) Pentraxin 3 and C-reactive protein in severe meningococcal disease. Shock 31:28–32PubMedGoogle Scholar
  101. Suankratay C, Mold C, Zhang Y, Potempa LA, Lint TF, Gewurz H (1998) Complement regulation in innate immunity and the acute-phase response: inhibition of mannan-binding lectin-initiated complement cytolysis by C-reactive protein (CRP). Clin Exp Immunol 113:353–359PubMedGoogle Scholar
  102. Szalai AJ (2002) The antimicrobial activity of C-reactive protein. Microbes Infect 4:201–205PubMedGoogle Scholar
  103. Szalai AJ, VanCott JL, McGhee JR, Volanakis JE, Benjamin WH Jr (2000) Human C-reactive protein is protective against fatal Salmonella enterica serovar typhimurium infection in transgenic mice. Infect Immun 68:5652–5656PubMedGoogle Scholar
  104. Tanio M, Wakamatsu K, Kohno T (2009) Binding site of C-reactive protein on M-ficolin. Mol Immunol 47:215–221PubMedGoogle Scholar
  105. Tennent GA, Lovat LB, Pepys MB (1995) Serum amyloid P component prevents proteolysis of the amyloid fibrils of Alzheimer disease and systemic amyloidosis. Proc Natl Acad Sci USA 92:4299–4303PubMedGoogle Scholar
  106. Tillett WS, Francis TJ (1930) Serological reactions in pneumonia with a non protein somatic fraction of pneumococcus. J Exp Med 52:561–585PubMedGoogle Scholar
  107. Trouw LA, Bengtsson AA, Gelderman KA, Dahlback B, Sturfelt G, Blom AM (2007) C4b-binding protein and Factor H compensate for the loss of membrane-bound complement inhibitors to protect apoptotic cells against excessive complement attack. J Biol Chem 282:28540–28548PubMedGoogle Scholar
  108. Verma S, Szmitko PE, Ridker PM (2005) C-reactive protein comes of age. Nat Clin Pract 2:29–36Google Scholar
  109. Yano Y, Matsuda S, Hatakeyama K, Sato Y, Imamura T, Shimada K, Kodama T, Kario K, Asada Y (2010) Plasma pentraxin 3, but not high-sensitivity C-reactive protein, is a useful inflammatory biomarker for predicting cognitive impairment in elderly hypertensive patients. J Gerontol 65:547–552Google Scholar
  110. Yuste J, Botto M, Bottoms SE, Brown JS (2007) Serum amyloid P aids complement-mediated immunity to Streptococcus pneumoniae. PLoS Pathog 3:1208–1219PubMedGoogle Scholar
  111. Zacho J, Tybjaerg-Hansen A, Jensen JS, Grande P, Sillesen H, Nordestgaard BG (2008) Genetically elevated C-reactive protein and ischemic vascular disease. N Engl J Med 359:1897–1908PubMedGoogle Scholar
  112. Zanetti M, Bosutti A, Ferreira C, Vinci P, Biolo G, Fonda M, Valente M, Cattin L, Guarnieri G, Barazzoni R (2009) Circulating pentraxin 3 levels are higher in metabolic syndrome with subclinical atherosclerosis: evidence for association with atherogenic lipid profile. Clin Exp Med 9:243–248PubMedGoogle Scholar
  113. Zhang J, Koh J, Lu J, Thiel S, Leong BS, Sethi S, He CY, Ho B, Ding JL (2009) Local inflammation induces complement crosstalk which amplifies the antimicrobial response. PLoS Pathog 5:e1000282PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Livija Deban
    • 1
  • Sebastien Jaillon
    • 1
  • Cecilia Garlanda
    • 1
  • Barbara Bottazzi
    • 1
  • Alberto Mantovani
    • 1
    • 2
  1. 1.Istituto Clinico Humanitas IRCCSRozzanoItaly
  2. 2.Department of Translational MedicineUniversity of MilanRozzanoItaly

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