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The Long Pentraxin PTX3 Is of Major Importance Among Acute Phase Proteins in Chickens

. 2019 ; 10 () : 124. [epub] 20190201

Language English Country Switzerland Media electronic-ecollection

Document type Journal Article, Research Support, Non-U.S. Gov't, Research Support, U.S. Gov't, Non-P.H.S.

Grant support
BB/M028208/1 Biotechnology and Biological Sciences Research Council - United Kingdom
BB/M028305/1 Biotechnology and Biological Sciences Research Council - United Kingdom
BBS/E/D/20320000 Biotechnology and Biological Sciences Research Council - United Kingdom

The expression level of acute phase proteins (APPs) mirrors the health status of an individual. In human medicine, C-reactive protein (CRP), and other members of the pentraxin family are of significant relevance for assessing disease severity and prognosis. In chickens, however, which represent the most common livestock species around the world, no such marker has yet gained general acceptance. The aim of this study was therefore, to characterize chicken pentraxin 3 (chPTX3) and to evaluate its applicability as a general marker for inflammatory conditions. The mammalian and chicken PTX3 proteins were predicted to be similar in sequence, domain organization and polymeric structure. Nevertheless, some characteristics like certain sequence sections, which have varied during the evolution of mammals, and species-specific glycosylation patterns, suggest distinct biological functions. ChPTX3 is constitutively expressed in various tissues but, interestingly, could not be found in splenic tissue samples without stimulation. However, upon treatment with lipopolysaccharide (LPS), PTX3 expression in chicken spleens increased to 95-fold within hours. A search for PTX3 reads in various publicly available RNA-seq data sets of chicken spleen and bursa of Fabricius also showed that PTX3 expression increases within days after experimental infection with viral and bacterial pathogens. An experimental infection with avian pathogenic E.coli and qPCR analysis of spleen samples further established a challenge dose-dependent significant up-regulation of chPTX3 in subclinically infected birds of up to over 150-fold as compared to untreated controls. Our results indicate the potential of chPTX3 as an APP marker to monitor inflammatory conditions in poultry flocks.

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Herrero M, Havlik P, Valin H, Notenbaert A, Rufino MC, Thornton PK, et al. . Biomass use, production, feed efficiencies, and greenhouse gas emissions from global livestock systems. Proc Natl Acad Sci USA. (2013) 110:20888–93. 10.1073/pnas.1308149110 PubMed DOI PMC

Jaillon S, Bonavita E, Gentile S, Rubino M, Laface I, Garlanda C, et al. . The long pentraxin PTX3 as a key component of humoral innate immunity and a candidate diagnostic for inflammatory diseases. Int Arch Allergy Immunol. (2014) 165:165–78. 10.1159/000368778 PubMed DOI

Dowton SB, Colten HR. Acute phase reactants in inflammation and infection. Semin Hematol. (1988) 25:84–90. PubMed

Gabay C, Kushner I. Acute-phase proteins and other systemic responses to inflammation. N Engl J Med. (1999) 340:448–54. 10.1056/NEJM199902113400607 PubMed DOI

O'Reilly EL, Eckersall PD. Acute phase proteins: a review of their function, behaviour and measurement in chickens. Worlds Poult Sci J. (2014) 70:27–44. 10.1017/S0043933914000038 DOI

Ma R, Xu H, Wu J, Sharma A, Bai S, Dun B, et al. . Identification of serum proteins and multivariate models for diagnosis and therapeutic monitoring of lung cancer. Oncotarget (2017) 8:18901–13. 10.18632/oncotarget.14782 PubMed DOI PMC

Liu S, Qu X, Liu F, Wang C. Pentraxin 3 as a prognostic biomarker in patients with systemic inflammation or infection. Mediators Inflamm. (2014) 2014:421429 10.1155/2014/421429 PubMed DOI PMC

Arellano-Orden E, Calero-Acuna C, Cordero JA, Abad-Arranz M, Sanchez-Lopez V, Marquez-Martin E, et al. . Specific networks of plasma acute phase reactants are associated with the severity of chronic obstructive pulmonary disease: a case-control study. Int J Med Sci. (2017) 14:67–74. 10.7150/ijms.16907 PubMed DOI PMC

Javard R, Grimes C, Bau-Gaudreault L, Dunn M. Acute-phase proteins and iron status in cats with chronic kidney disease. J Vet Intern Med. (2017) 31:457–64. 10.1111/jvim.14661 PubMed DOI PMC

Guardino CM, Dunkel Schetter C, Hobel CJ, Gaines Lanzi R, Schafer P, Thorp JM, et al. . Chronic stress and C-reactive protein in mothers during the first postpartum year. Psychosom Med. (2016) 79:450–60. 10.1097/PSY.0000000000000424 PubMed DOI PMC

Tillett WS, Francis T. Serological reactions in pneumonia with a non-protein somatic fraction of pneumococcus. J Exp Med. (1930) 52:561–71. 10.1084/jem.52.4.561 PubMed DOI PMC

Pepys MB, Hirschfield GM. C-reactive protein: a critical update. J Clin Invest. (2003) 111:1805–12. 10.1172/JCI200318921 PubMed DOI PMC

Sylte MJ, Suarez DL. Vaccination and acute phase mediator production in chickens challenged with low pathogenic avian influenza virus; novel markers for vaccine efficacy? Vaccine (2012) 30:3097–105. 10.1016/j.vaccine.2012.02.055 PubMed DOI

Zulkifli I, Najafi P, Nurfarahin AJ, Soleimani AF, Kumari S, Aryani AA, et al. . Acute phase proteins, interleukin 6, and heat shock protein 70 in broiler chickens administered with corticosterone. Poult Sci. (2014) 93:3112–8. 10.3382/ps.2014-04099 PubMed DOI

Koppenol A, Everaert N, Buyse J, Delezie E. Challenge with lipopolysaccharides or Freund's adjuvant? What is the best option to trigger acute phase protein production in broilers? Res Vet Sci. (2015) 99:96–8. 10.1016/j.rvsc.2015.01.013 PubMed DOI

Eid C, Hemadi M, Ha-Duong NT, El Hage Chahine JM. Iron uptake and transfer from ceruloplasmin to transferrin. Biochim Biophys Acta (2014) 1840:1771–81. 10.1016/j.bbagen.2014.01.011 PubMed DOI

Kumar S, Sharma D, Kumar R, Kumar R. Electrostatic effects control the stability and iron release kinetics of ovotransferrin. J Biol Inorg Chem. (2014) 19:1009–24. 10.1007/s00775-014-1145-2 PubMed DOI

Urien S, Bree F, Testa B, Tillement JP. pH-dependency of basic ligand binding to alpha 1-acid glycoprotein (orosomucoid). Biochem J. (1991) 280 (Pt 1):277–80. PubMed PMC

Dalgaard TS, Skovgaard K, Norup LR, Pleidrup J, Permin A, Schou TW, et al. . Immune gene expression in the spleen of chickens experimentally infected with Ascaridia galli. Vet Immunol Immunopathol. (2015) 164:79–86. 10.1016/j.vetimm.2015.01.003 PubMed DOI

Kjaerup RM, Dalgaard TS, Norup LR, Hamzic E, Sorensen P, Juul-Madsen HR. Characterization of cellular and humoral immune responses after IBV infection in chicken lines differing in MBL serum concentration. Viral Immunol. (2014) 27:529–42. 10.1089/vim.2014.0088 PubMed DOI PMC

Norup LR, Dalgaard TS, Friggens NC, Sorensen P, Juul-Madsen HR. Influence of chicken serum mannose-binding lectin levels on the immune response towards Escherichia coli. Poult Sci. (2009) 88:543–53. 10.3382/ps.2008-00431 PubMed DOI

Millet S, Bennett J, Lee KA, Hau M, Klasing KC. Quantifying and comparing constitutive immunity across avian species. Dev Comp Immunol. (2007) 31:188–201. 10.1016/j.dci.2006.05.013 PubMed DOI

Laursen SB, Nielsen OL. Mannan-binding lectin (MBL) in chickens: molecular and functional aspects. Dev Comp Immunol. (2000) 24:85–101. 10.1016/S0145-305X(99)00066-X PubMed DOI

de Seny D, Cobraiville G, Charlier E, Neuville S, Esser N, Malaise D, et al. . Acute-phase serum amyloid a in osteoarthritis: regulatory mechanism and proinflammatory properties. PLoS ONE (2013) 8:e66769. 10.1371/journal.pone.0066769 PubMed DOI PMC

Landman WJ, Sletten K, Koch CA, Tooten PC, Gruys E. Chicken joint amyloid protein is of the AA-type. I Characterization of the amyloid protein. Scand J Immunol. (1996) 43:210–8. 10.1046/j.1365-3083.1996.d01-31.x PubMed DOI

Upragarin N, Landman WJ, Gaastra W, Gruys E. Extrahepatic production of acute phase serum amyloid A. Histol Histopathol. (2005) 20:1295–307. 10.14670/HH-20.1295 PubMed DOI

Nazifi S, Dadras H, Hoseinian SA, Ansari-Lari M, Masoudian M. Measuring acute phase proteins (haptoglobin, ceruloplasmin, serum amyloid A, and fibrinogen) in healthy and infectious bursal disease virus-infected chicks. Comp Clin Pathol. (2010) 19:283–6. 10.1007/s00580-009-0858-z DOI

Nazifi S, Tabandeh MR, Hosseinian SA, Ansari-Lari M, Safari H. Evaluation of sialic acid and acute-phase proteins (haptoglobin and serum amyloids A) in healthy and avian infection bronchitis virus-infected chicks. Comp Clin Pathol. (2011) 20:69–73. 10.1007/s00580-009-0939-z PubMed DOI PMC

Muhammad IF, Borne Y, Hedblad B, Nilsson PM, Persson M, Engstrom G. Acute-phase proteins and incidence of diabetes: a population-based cohort study. Acta Diabetol. (2016) 53:981–9. 10.1007/s00592-016-0903-8 PubMed DOI PMC

Muhammad IF, Borne Y, Ostling G, Kennback C, Gottsater M, Persson M, et al. . Acute phase proteins as prospective risk markers for arterial stiffness: the malmo diet and cancer cohort. PLoS ONE (2017) 12:e0181718. 10.1371/journal.pone.0181718 PubMed DOI PMC

Rajamanickam A, Munisankar S, Bhootra Y, Dolla C, Nutman TB, Babu S. Microbial translocation associated with an acute-phase response and elevations in MMP-1, HO-1, and proinflammatory cytokines in Strongyloides stercoralis infection. Infect Immun. (2017) 85:e00772–16. 10.1128/IAI.00772-16 PubMed DOI PMC

Daigo K, Mantovani A, Bottazzi B. The yin-yang of long pentraxin PTX3 in inflammation and immunity. Immunol Lett. (2014) 161:38–43. 10.1016/j.imlet.2014.04.012 PubMed DOI PMC

Inforzato A, Rivieccio V, Morreale AP, Bastone A, Salustri A, Scarchilli L, et al. . Structural characterization of PTX3 disulfide bond network and its multimeric status in cumulus matrix organization. J Biol Chem. (2008) 283:10147–61. 10.1074/jbc.M708535200 PubMed DOI

Jaillon S, Moalli F, Ragnarsdottir B, Bonavita E, Puthia M, Riva F, et al. . The humoral pattern recognition molecule PTX3 is a key component of innate immunity against urinary tract infection. Immunity (2014) 40:621–32. 10.1016/j.immuni.2014.02.015 PubMed DOI

Reading PC, Bozza S, Gilbertson B, Tate M, Moretti S, Job ER, et al. . Antiviral activity of the long chain pentraxin PTX3 against influenza viruses. J Immunol. (2008) 180:3391–8. 10.4049/jimmunol.180.5.3391 PubMed DOI

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) 420:182–6. 10.1038/nature01195 PubMed DOI

Huang XL, Zhang L, Duan Y, Wang YJ, Wang J. Association of pentraxin 3 with autoimmune diseases: a systematic review and meta-analysis. Arch Med Res. (2016) 47:223–31. 10.1016/j.arcmed.2016.05.006 PubMed DOI

Röell S, Häertle S, Lütteke T, Kaspers B, Häertle S. Tissue and time specific expression pattern of interferon regulated genes in the chicken. BMC Genomics (2017) 18:264 10.1186/s12864-017-3641-6 PubMed DOI PMC

Burnette WN. “Western blotting”: electrophoretic transfer of proteins from sodium dodecyl sulfate–polyacrylamide gels to unmodified nitrocellulose and radiographic detection with antibody and radioiodinated protein A. Anal Biochem. (1981) 112:195–203. 10.1016/0003-2697(81)90281-5 PubMed DOI

Johnson TJ, Kariyawasam S, Wannemuehler Y, Mangiamele P, Johnson SJ, Doetkott C, et al. . The genome sequence of avian pathogenic Escherichia coli strain O1:K1:H7 shares strong similarities with human extraintestinal pathogenic E. coli genomes. J Bacteriol. (2007) 189:3228–36. 10.1128/JB.01726-06 PubMed DOI PMC

Gatzmann F, Metzler D, Krebs S, Blum H, Sing A, Takano A, et al. . NGS population genetics analyses reveal divergent evolution of a Lyme Borreliosis agent in Europe and Asia. Ticks Tick Borne Dis. (2015) 6:344–51. 10.1016/j.ttbdis.2015.02.008 PubMed DOI

Borowska D, Rothwell L, Bailey RA, Watson K, Kaiser P. Identification of stable reference genes for quantitative PCR in cells derived from chicken lymphoid organs. Vet Immunol Immunopathol. (2016) 170:20–4. 10.1016/j.vetimm.2016.01.001 PubMed DOI

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. J Biol Chem. (1997) 272:32817–23. 10.1074/jbc.272.52.32817 PubMed DOI

Van Goor A, Ashwell CM, Persia ME, Rothschild MF, Schmidt CJ, Lamont SJ. Unique genetic responses revealed in RNA-seq of the spleen of chickens stimulated with lipopolysaccharide and short-term heat. PLoS ONE (2017) 12:e0171414 10.1371/journal.pone.0171414 PubMed DOI PMC

Bumstead N, Huggins MB, Cook JK. Genetic differences in susceptibility to a mixture of avian infectious bronchitis virus and Escherichia coli. Br Poult Sci. (1989) 30:39–48. 10.1080/00071668908417123 PubMed DOI

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) 45:11540–51. 10.1021/bi0607453 PubMed DOI

Doni A, Garlanda C, Mantovani A. PTX3 orchestrates tissue repair. Oncotarget (2015) 6:30435–6. 10.18632/oncotarget.5453 PubMed DOI PMC

Inforzato A, Baldock C, Jowitt TA, Holmes DF, Lindstedt R, Marcellini M, et al. . The angiogenic inhibitor long pentraxin PTX3 forms an asymmetric octamer with two binding sites for FGF2. J Biol Chem. (2010) 285:17681–92. 10.1074/jbc.M109.085639 PubMed DOI PMC

Inforzato A, Reading PC, Barbati E, Bottazzi B, Garlanda C, Mantovani A. The “sweet” side of a long pentraxin: how glycosylation affects PTX3 functions in innate immunity and inflammation. Front Immunol. (2012) 3:407. 10.3389/fimmu.2012.00407 PubMed DOI PMC

Deban L, Russo RC, Sironi M, Moalli F, Scanziani M, Zambelli V, et al. . Regulation of leukocyte recruitment by the long pentraxin PTX3. Nat Immunol. (2010) 11:328–34. 10.1038/ni.1854 PubMed DOI

Wilks S, de Graaf M, Smith DJ, Burke DF. A review of influenza haemagglutinin receptor binding as it relates to pandemic properties. Vaccine (2012) 30:4369–76. 10.1016/j.vaccine.2012.02.076 PubMed DOI PMC

Neu U, Bauer J, Stehle T. Viruses and sialic acids: rules of engagement. Curr Opin Struct Biol. (2011) 21:610–8. 10.1016/j.sbi.2011.08.009 PubMed DOI PMC

Urbaniak K, Markowska-Daniel I, Kowalczyk A, Kwit K, Pomorska-Mol M, Fracek B, et al. . Reassortment process after co-infection of pigs with avian H1N1 and swine H3N2 influenza viruses. BMC Vet Res. (2017) 13:215. 10.1186/s12917-017-1137-x PubMed DOI PMC

Jain S, Gautam V, Naseem S. Acute-phase proteins: as diagnostic tool. J Pharm Bioallied Sci. (2011) 3:118–27. 10.4103/0975-7406.76489 PubMed DOI PMC

Chapwanya A, Meade KG, Doherty ML, Callanan JJ, O'Farrelly C. Endometrial epithelial cells are potent producers of tracheal antimicrobial peptide and serum amyloid A3 gene expression in response to E. coli stimulation. Vet Immunol Immunopathol. (2013) 151:157–62. 10.1016/j.vetimm.2012.09.042 PubMed DOI

Inforzato A, Jaillon S, Moalli F, Barbati E, Bonavita E, Bottazzi B, et al. . The long pentraxin PTX3 at the crossroads between innate immunity and tissue remodelling. Tissue Antigens (2011) 77:271–82. 10.1111/j.1399-0039.2011.01645.x PubMed DOI

Nauta AJ, de Haij S, Bottazzi B, Mantovani A, Borrias MC, Aten J, et al. . Human renal epithelial cells produce the long pentraxin PTX3. Kidney Int. (2005) 67:543–53. 10.1111/j.1523-1755.2005.67111.x PubMed DOI

Hanel KH, Cornelissen C, Luscher B, Baron JM. Cytokines and the skin barrier. Int J Mol Sci. (2013) 14:6720–45. 10.3390/ijms14046720 PubMed DOI PMC

Martovetsky G, Tee JB, Nigam SK. Hepatocyte nuclear factors 4alpha and 1alpha regulate kidney developmental expression of drug-metabolizing enzymes and drug transporters. Mol Pharmacol. (2013) 84:808–23. 10.1124/mol.113.088229 PubMed DOI PMC

Rubino M, Kunderfranco P, Basso G, Greco CM, Pasqualini F, Serio S, et al. . Epigenetic regulation of the extrinsic oncosuppressor PTX3 gene in inflammation and cancer. Oncoimmunology (2017) 6:e1333215. 10.1080/2162402X.2017.1333215 PubMed DOI PMC

Sun H, Liu P, Nolan LK, Lamont SJ. Novel pathways revealed in bursa of fabricius transcriptome in response to extraintestinal pathogenic Escherichia coli (ExPEC) infection. PLoS ONE (2015) 10:e0142570. 10.1371/journal.pone.0142570 PubMed DOI PMC

Nissinen L, Kahari VM. Matrix metalloproteinases in inflammation. Biochim Biophys Acta (2014) 1840:2571–80. 10.1016/j.bbagen.2014.03.007 PubMed DOI

Steelant B, Farre R, Wawrzyniak P, Belmans J, Dekimpe E, Vanheel H, et al. . Impaired barrier function in patients with house dust mite-induced allergic rhinitis is accompanied by decreased occludin and zonula occludens-1 expression. J Allergy Clin Immunol. (2016) 137:1043–53.e5. 10.1016/j.jaci.2015.10.050 PubMed DOI

Marques AT, Lecchi C, Grilli G, Giudice C, Nodari SR, Vinco LJ, et al. . The effect of transport stress on turkey (Meleagris gallopavo) liver acute phase proteins gene expression. Res Vet Sci. (2016) 104:92–5. 10.1016/j.rvsc.2015.11.014 PubMed DOI

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