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Published in: Malaria Journal 1/2016

Open Access 01-12-2016 | Research

Plasma levels of eight different mediators and their potential as biomarkers of various clinical malaria conditions in African children

Authors: Rachida Tahar, Catarina Albergaria, Neil Zeghidour, Vincent Foumane Ngane, Leonardo K. Basco, Christian Roussilhon

Published in: Malaria Journal | Issue 1/2016

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Abstract

Background

Plasmodium falciparum infection can lead to several clinical manifestations ranging from asymptomatic infections (AM) and uncomplicated malaria (UM) to potentially fatal severe malaria (SM), including cerebral malaria (CM). Factors implicated in the progression towards severe disease are not fully understood.

Methods

In the present study, an enzyme-linked immunosorbent assay (ELISA) method was used to investigate the plasma content of several biomarkers of the immune response, namely Neopterin, sCD163, suPAR, Pentraxin 3 (PTX3), sCD14, Fractalkine (CX3CL1), sTREM-1 and MIG (CXCL9), in patients with distinct clinical manifestations of malaria. The goal of this study was to determine the relative involvement of these inflammatory mediators in the pathogenesis of malaria and test their relevance as biomarkers of disease severity.

Results

ROC curve analysis show that children with AM were characterized by high levels of Fractalkine and sCD163 whereas children with UM were distinguishable by the presence of PTX3 in their plasma. Furthermore, principal component analysis indicated that the combination of Fractalkine, MIG, and Neopterin was the best predictor of AM condition, while suPAR, PTX3 and sTREM-1 combination was the best indicator of UM when compared to AM. The association of Neopterin, suPAR and Fractalkine was strongly predictive of SM or CM compared to UM.

Conclusions

The results indicate that the simultaneous evaluation of these bioactive molecules as quantifiable blood parameters may be helpful to get a better insight into the clinical syndromes in children with malaria.
Literature
1.
go back to reference WHO. World malaria report. Geneva: World Health Organization; 2014. WHO. World malaria report. Geneva: World Health Organization; 2014.
2.
go back to reference Murray CJ, Rosenfeld LC, Lim SS, Andrews KG, Foreman KJ, Haring D, et al. Global malaria mortality between 1980 and 2010: a systematic analysis. Lancet. 2012;379:413–31.CrossRefPubMed Murray CJ, Rosenfeld LC, Lim SS, Andrews KG, Foreman KJ, Haring D, et al. Global malaria mortality between 1980 and 2010: a systematic analysis. Lancet. 2012;379:413–31.CrossRefPubMed
3.
go back to reference Pongponratn E, Riganti M, Punpoowong B, Aikawa M. Microvascular sequestration of parasitized erythrocytes in human falciparum malaria: a pathological study. Am J Trop Med Hyg. 1991;44:168–75.PubMed Pongponratn E, Riganti M, Punpoowong B, Aikawa M. Microvascular sequestration of parasitized erythrocytes in human falciparum malaria: a pathological study. Am J Trop Med Hyg. 1991;44:168–75.PubMed
4.
go back to reference WHO. Global malaria programme. Geneva: World Health Organization; 2011. WHO. Global malaria programme. Geneva: World Health Organization; 2011.
5.
go back to reference Mackintosh CL, Beeson JG, Marsh K. Clinical features and pathogenesis of severe malaria. Trends Parasitol. 2004;20:597–603.CrossRefPubMed Mackintosh CL, Beeson JG, Marsh K. Clinical features and pathogenesis of severe malaria. Trends Parasitol. 2004;20:597–603.CrossRefPubMed
6.
go back to reference Ranjit MR, Das A, Das BP, Das BN, Dash BP, Chhotray GP. Distribution of Plasmodium falciparum genotypes in clinically mild and severe malaria cases in Orissa, India. Trans R Soc Trop Med Hyg. 2005;99:389–95.CrossRefPubMed Ranjit MR, Das A, Das BP, Das BN, Dash BP, Chhotray GP. Distribution of Plasmodium falciparum genotypes in clinically mild and severe malaria cases in Orissa, India. Trans R Soc Trop Med Hyg. 2005;99:389–95.CrossRefPubMed
7.
8.
go back to reference de Kossodo S, Grau GE. Profiles of cytokine production in relation with susceptibility to cerebral malaria. J Immunol. 1993;151:4811–20.PubMed de Kossodo S, Grau GE. Profiles of cytokine production in relation with susceptibility to cerebral malaria. J Immunol. 1993;151:4811–20.PubMed
9.
go back to reference Lyke KE, Burges R, Cissoko Y, Sangare L, Dao M, Diarra I, et al. Serum levels of the proinflammatory cytokines interleukin-1 beta (IL-1beta), IL-6, IL-8, IL-10, tumor necrosis factor alpha, and IL-12(p70) in Malian children with severe Plasmodium falciparum malaria and matched uncomplicated malaria or healthy controls. Infect Immun. 2004;72:5630–7.CrossRefPubMedPubMedCentral Lyke KE, Burges R, Cissoko Y, Sangare L, Dao M, Diarra I, et al. Serum levels of the proinflammatory cytokines interleukin-1 beta (IL-1beta), IL-6, IL-8, IL-10, tumor necrosis factor alpha, and IL-12(p70) in Malian children with severe Plasmodium falciparum malaria and matched uncomplicated malaria or healthy controls. Infect Immun. 2004;72:5630–7.CrossRefPubMedPubMedCentral
10.
go back to reference Kurtzhals JA, Adabayeri V, Goka BQ, Akanmori BD, Oliver-Commey JO, Nkrumah FK, et al. Low plasma concentrations of interleukin 10 in severe malarial anaemia compared with cerebral and uncomplicated malaria. Lancet. 1998;351:1768–72.CrossRefPubMed Kurtzhals JA, Adabayeri V, Goka BQ, Akanmori BD, Oliver-Commey JO, Nkrumah FK, et al. Low plasma concentrations of interleukin 10 in severe malarial anaemia compared with cerebral and uncomplicated malaria. Lancet. 1998;351:1768–72.CrossRefPubMed
11.
go back to reference Esamai F, Ernerudh J, Janols H, Welin S, Ekerfelt C, Mining S, et al. Cerebral malaria in children: serum and cerebrospinal fluid TNF-alpha and TGF-beta levels and their relationship to clinical outcome. J Trop Pediatr. 2003;49:216–23.CrossRefPubMed Esamai F, Ernerudh J, Janols H, Welin S, Ekerfelt C, Mining S, et al. Cerebral malaria in children: serum and cerebrospinal fluid TNF-alpha and TGF-beta levels and their relationship to clinical outcome. J Trop Pediatr. 2003;49:216–23.CrossRefPubMed
12.
go back to reference Turner GD, Morrison H, Jones M, Davis TM, Looareesuwan S, Buley ID, et al. An immunohistochemical study of the pathology of fatal malaria. Evidence for widespread endothelial activation and a potential role for intercellular adhesion molecule-1 in cerebral sequestration. Am J Pathol. 1994;145:1057–69.PubMedPubMedCentral Turner GD, Morrison H, Jones M, Davis TM, Looareesuwan S, Buley ID, et al. An immunohistochemical study of the pathology of fatal malaria. Evidence for widespread endothelial activation and a potential role for intercellular adhesion molecule-1 in cerebral sequestration. Am J Pathol. 1994;145:1057–69.PubMedPubMedCentral
13.
go back to reference Moxon CA, Wassmer SC, Milner DA Jr, Chisala NV, Taylor TE, Seydel KB, et al. Loss of endothelial protein C receptors links coagulation and inflammation to parasite sequestration in cerebral malaria in African children. Blood. 2013;122:842–51.CrossRefPubMedPubMedCentral Moxon CA, Wassmer SC, Milner DA Jr, Chisala NV, Taylor TE, Seydel KB, et al. Loss of endothelial protein C receptors links coagulation and inflammation to parasite sequestration in cerebral malaria in African children. Blood. 2013;122:842–51.CrossRefPubMedPubMedCentral
14.
go back to reference Awandare GA, Goka B, Boeuf P, Tetteh JK, Kurtzhals JA, Behr C, et al. Increased levels of inflammatory mediators in children with severe Plasmodium falciparum malaria with respiratory distress. J Infect Dis. 2006;194:1438–46.CrossRefPubMed Awandare GA, Goka B, Boeuf P, Tetteh JK, Kurtzhals JA, Behr C, et al. Increased levels of inflammatory mediators in children with severe Plasmodium falciparum malaria with respiratory distress. J Infect Dis. 2006;194:1438–46.CrossRefPubMed
15.
go back to reference Moxon CA, Chisala NV, Wassmer SC, Taylor TE, Seydel KB, Molyneux ME, et al. Persistent endothelial activation and inflammation after Plasmodium falciparum infection in Malawian children. J Infect Dis. 2014;209:610–5.CrossRefPubMed Moxon CA, Chisala NV, Wassmer SC, Taylor TE, Seydel KB, Molyneux ME, et al. Persistent endothelial activation and inflammation after Plasmodium falciparum infection in Malawian children. J Infect Dis. 2014;209:610–5.CrossRefPubMed
16.
go back to reference Moussiliou A, Alao MJ, Denoeud-Ndam L, Tahar R, Ezimegnon S, Sagbo G, et al. High plasma sEPCR levels are associated with increased mortality in children with cerebral malaria in Benin. J Infect Dis. 2015;211:1484–8.CrossRefPubMed Moussiliou A, Alao MJ, Denoeud-Ndam L, Tahar R, Ezimegnon S, Sagbo G, et al. High plasma sEPCR levels are associated with increased mortality in children with cerebral malaria in Benin. J Infect Dis. 2015;211:1484–8.CrossRefPubMed
17.
go back to reference Weiss G, Murr C, Zoller H, Haun M, Widner B, Ludescher C, et al. Modulation of neopterin formation and tryptophan degradation by Th1- and Th2-derived cytokines in human monocytic cells. Clin Exp Immunol. 1999;116:435–40.CrossRefPubMedPubMedCentral Weiss G, Murr C, Zoller H, Haun M, Widner B, Ludescher C, et al. Modulation of neopterin formation and tryptophan degradation by Th1- and Th2-derived cytokines in human monocytic cells. Clin Exp Immunol. 1999;116:435–40.CrossRefPubMedPubMedCentral
18.
go back to reference Facer CA. Malaria antigens stimulate neopterin secretion by PBMC and U937 cells. Microbiol Immunol. 1995;39:207–11.CrossRefPubMed Facer CA. Malaria antigens stimulate neopterin secretion by PBMC and U937 cells. Microbiol Immunol. 1995;39:207–11.CrossRefPubMed
19.
go back to reference Kusi KA, Gyan BA, Goka BQ, Dodoo D, Obeng-Adjei G, Troye-Blomberg M, et al. Levels of soluble CD163 and severity of malaria in children in Ghana. Clin Vaccine Immunol. 2008;15:1456–60.CrossRefPubMedPubMedCentral Kusi KA, Gyan BA, Goka BQ, Dodoo D, Obeng-Adjei G, Troye-Blomberg M, et al. Levels of soluble CD163 and severity of malaria in children in Ghana. Clin Vaccine Immunol. 2008;15:1456–60.CrossRefPubMedPubMedCentral
20.
go back to reference Kunes P, Holubcova Z, Kolackova M, Krejsek J. Pentraxin 3(PTX 3): an endogenous modulator of the inflammatory response. Mediators Inflamm. 2012;2012:920517.CrossRefPubMedPubMedCentral Kunes P, Holubcova Z, Kolackova M, Krejsek J. Pentraxin 3(PTX 3): an endogenous modulator of the inflammatory response. Mediators Inflamm. 2012;2012:920517.CrossRefPubMedPubMedCentral
21.
go back to reference Fauser S, Deininger MH, Kremsner PG, Magdolen V, Luther T, Meyermann R, et al. Lesion associated expression of urokinase-type plasminogen activator receptor (uPAR, CD87) in human cerebral malaria. J Neuroimmunol. 2000;111:234–40.CrossRefPubMed Fauser S, Deininger MH, Kremsner PG, Magdolen V, Luther T, Meyermann R, et al. Lesion associated expression of urokinase-type plasminogen activator receptor (uPAR, CD87) in human cerebral malaria. J Neuroimmunol. 2000;111:234–40.CrossRefPubMed
22.
go back to reference Hawkes M, Elphinstone RE, Conroy AL, Kain KC. Contrasting pediatric and adult cerebral malaria: the role of the endothelial barrier. Virulence. 2013;4:543–55.CrossRefPubMed Hawkes M, Elphinstone RE, Conroy AL, Kain KC. Contrasting pediatric and adult cerebral malaria: the role of the endothelial barrier. Virulence. 2013;4:543–55.CrossRefPubMed
23.
go back to reference Deban L, Bottazzi B, Garlanda C, de la Torre YM, Mantovani A. Pentraxins: multifunctional proteins at the interface of innate immunity and inflammation. BioFactors. 2009;35:138–45.CrossRefPubMed Deban L, Bottazzi B, Garlanda C, de la Torre YM, Mantovani A. Pentraxins: multifunctional proteins at the interface of innate immunity and inflammation. BioFactors. 2009;35:138–45.CrossRefPubMed
24.
go back to reference 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. Immunol Rev. 2009;227:9–18.CrossRefPubMed 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. Immunol Rev. 2009;227:9–18.CrossRefPubMed
25.
go back to reference Moalli F, Jaillon S, Inforzato A, Sironi M, Bottazzi B, Mantovani A, et al. Pathogen recognition by the long pentraxin PTX3. J Biomed Biotechnol. 2011;2011:830421.CrossRefPubMedPubMedCentral Moalli F, Jaillon S, Inforzato A, Sironi M, Bottazzi B, Mantovani A, et al. Pathogen recognition by the long pentraxin PTX3. J Biomed Biotechnol. 2011;2011:830421.CrossRefPubMedPubMedCentral
26.
go back to reference Bottazzi B, Doni A, Garlanda C, Mantovani A. An integrated view of humoral innate immunity: pentraxins as a paradigm. Annu Rev Immunol. 2010;28:157–83.CrossRefPubMed Bottazzi B, Doni A, Garlanda C, Mantovani A. An integrated view of humoral innate immunity: pentraxins as a paradigm. Annu Rev Immunol. 2010;28:157–83.CrossRefPubMed
27.
go back to reference Arias MA, Rey Nores JE, Vita N, Stelter F, Borysiewicz LK, Ferrara P, et al. Cutting edge: human B cell function is regulated by interaction with soluble CD14: opposite effects on IgG1 and IgE production. J Immunol. 2000;164:3480–6.CrossRefPubMed Arias MA, Rey Nores JE, Vita N, Stelter F, Borysiewicz LK, Ferrara P, et al. Cutting edge: human B cell function is regulated by interaction with soluble CD14: opposite effects on IgG1 and IgE production. J Immunol. 2000;164:3480–6.CrossRefPubMed
28.
go back to reference Filipp D, Alizadeh-Khiavi K, Richardson C, Palma A, Paredes N, Paredes N, et al. Soluble CD14 enriched in colostrum and milk induces B cell growth and differentiation. Proc Natl Acad Sci USA. 2001;98:603–8.CrossRefPubMedPubMedCentral Filipp D, Alizadeh-Khiavi K, Richardson C, Palma A, Paredes N, Paredes N, et al. Soluble CD14 enriched in colostrum and milk induces B cell growth and differentiation. Proc Natl Acad Sci USA. 2001;98:603–8.CrossRefPubMedPubMedCentral
29.
go back to reference Wenisch C, Wenisch H, Parschalk B, Vanijanonta S, Burgmann H, Staudinger T, et al. Elevated levels of soluble CD14 in serum of patients with acute Plasmodium falciparum malaria. Clin Exp Immunol. 1996;105:74–8.CrossRefPubMedPubMedCentral Wenisch C, Wenisch H, Parschalk B, Vanijanonta S, Burgmann H, Staudinger T, et al. Elevated levels of soluble CD14 in serum of patients with acute Plasmodium falciparum malaria. Clin Exp Immunol. 1996;105:74–8.CrossRefPubMedPubMedCentral
30.
go back to reference Ollivier V, Faure S, Tarantino N, Chollet-Martin S, Deterre P, Combadière C, et al. Fractalkine/CX3CL1 production by human aortic smooth muscle cells impairs monocyte procoagulant and inflammatory responses. Cytokine. 2003;21:303–11.CrossRefPubMed Ollivier V, Faure S, Tarantino N, Chollet-Martin S, Deterre P, Combadière C, et al. Fractalkine/CX3CL1 production by human aortic smooth muscle cells impairs monocyte procoagulant and inflammatory responses. Cytokine. 2003;21:303–11.CrossRefPubMed
31.
go back to reference Hatabu T, Kawazu S, Aikawa M, Kano S. Binding of Plasmodium falciparum-infected erythrocytes to the membrane-bound form of Fractalkine/CX3CL1. Proc Natl Acad Sci USA. 2003;100:15942–6.CrossRefPubMedPubMedCentral Hatabu T, Kawazu S, Aikawa M, Kano S. Binding of Plasmodium falciparum-infected erythrocytes to the membrane-bound form of Fractalkine/CX3CL1. Proc Natl Acad Sci USA. 2003;100:15942–6.CrossRefPubMedPubMedCentral
32.
go back to reference Gomez-Pina V, Soares-Schanoski A, Rodriguez-Rojas A, Del Fresno C, Garcia F, Vallejo-Cremades MT, et al. Metalloproteinases shed TREM-1 ectodomain from lipopolysaccharide-stimulated human monocytes. J Immunol. 2007;179:4065–73.CrossRefPubMed Gomez-Pina V, Soares-Schanoski A, Rodriguez-Rojas A, Del Fresno C, Garcia F, Vallejo-Cremades MT, et al. Metalloproteinases shed TREM-1 ectodomain from lipopolysaccharide-stimulated human monocytes. J Immunol. 2007;179:4065–73.CrossRefPubMed
33.
go back to reference Lemarie J, Barraud D, Gibot S. Host response biomarkers in sepsis: overview on sTREM-1 detection. Methods Mol Biol. 2015;1237:225–39.CrossRefPubMed Lemarie J, Barraud D, Gibot S. Host response biomarkers in sepsis: overview on sTREM-1 detection. Methods Mol Biol. 2015;1237:225–39.CrossRefPubMed
34.
go back to reference Loetscher M, Gerber B, Loetscher P, Jones SA, Piali L, Clark-Lewis I, et al. Chemokine receptor specific for IP10 and mig: structure, function, and expression in activated T-lymphocytes. J Exp Med. 1996;184:963–9.CrossRefPubMed Loetscher M, Gerber B, Loetscher P, Jones SA, Piali L, Clark-Lewis I, et al. Chemokine receptor specific for IP10 and mig: structure, function, and expression in activated T-lymphocytes. J Exp Med. 1996;184:963–9.CrossRefPubMed
35.
go back to reference Burian K, Endresz V, Deak J, Kormanyos Z, Pal A, Nelson D, et al. Transcriptome analysis indicates an enhanced activation of adaptive and innate immunity by chlamydia-infected murine epithelial cells treated with interferon γ. J Infect Dis. 2010;202:1405–14.CrossRefPubMedPubMedCentral Burian K, Endresz V, Deak J, Kormanyos Z, Pal A, Nelson D, et al. Transcriptome analysis indicates an enhanced activation of adaptive and innate immunity by chlamydia-infected murine epithelial cells treated with interferon γ. J Infect Dis. 2010;202:1405–14.CrossRefPubMedPubMedCentral
36.
go back to reference Petro M, Kish D, Guryanova OA, Ilyinskaya G, Kondratova A, Fairchild RL, et al. Cutaneous tumors cease CXCL9/Mig production as a result of IFN-γ-mediated immunoediting. J Immunol. 2013;190:832–41.CrossRefPubMed Petro M, Kish D, Guryanova OA, Ilyinskaya G, Kondratova A, Fairchild RL, et al. Cutaneous tumors cease CXCL9/Mig production as a result of IFN-γ-mediated immunoediting. J Immunol. 2013;190:832–41.CrossRefPubMed
37.
go back to reference WHO. Severe falciparum malaria. Trans R Soc Trop Med Hyg. 2000;94(suppl 1):1–90. WHO. Severe falciparum malaria. Trans R Soc Trop Med Hyg. 2000;94(suppl 1):1–90.
38.
go back to reference Zweig MH, Campbell G. Receiver-operating characteristic (ROC) plots: a fundamental evaluation tool in clinical medicine. Clin Chem. 1993;39:561–77.PubMed Zweig MH, Campbell G. Receiver-operating characteristic (ROC) plots: a fundamental evaluation tool in clinical medicine. Clin Chem. 1993;39:561–77.PubMed
40.
go back to reference Zweig MH. ROC plots display test accuracy, but are still limited by the study design. Clin Chem. 1993;39:1345–6.PubMed Zweig MH. ROC plots display test accuracy, but are still limited by the study design. Clin Chem. 1993;39:1345–6.PubMed
41.
go back to reference Ho W. Severe malaria. Trop Med Int Health. 2014;19(Suppl 1):7–131. Ho W. Severe malaria. Trop Med Int Health. 2014;19(Suppl 1):7–131.
42.
go back to reference Thomsen HH, Moller HJ, Trolle C, Groth KA, Skakkebaek A, Bojesen A, et al. The macrophage low-grade inflammation marker sCD163 is modulated by exogenous sex steroids. Endocr Connect. 2013;2:216–24.CrossRefPubMedPubMedCentral Thomsen HH, Moller HJ, Trolle C, Groth KA, Skakkebaek A, Bojesen A, et al. The macrophage low-grade inflammation marker sCD163 is modulated by exogenous sex steroids. Endocr Connect. 2013;2:216–24.CrossRefPubMedPubMedCentral
43.
go back to reference Garcia GE, Xia Y, Chen S, Wang Y, Ye RD, Harrison JK, et al. NF-kappaB-dependent fractalkine induction in rat aortic endothelial cells stimulated by IL-1beta, TNF-alpha, and LPS. J Leukoc Biol. 2000;67:577–84.PubMed Garcia GE, Xia Y, Chen S, Wang Y, Ye RD, Harrison JK, et al. NF-kappaB-dependent fractalkine induction in rat aortic endothelial cells stimulated by IL-1beta, TNF-alpha, and LPS. J Leukoc Biol. 2000;67:577–84.PubMed
44.
go back to reference Hao F, Zhang NN, Zhang DM, Bai HY, Piao H, Yuan B, et al. Chemokine fractalkine attenuates overactivation and apoptosis of BV-2 microglial cells induced by extracellular ATP. Neurochem Res. 2013;38:1002–12.CrossRefPubMed Hao F, Zhang NN, Zhang DM, Bai HY, Piao H, Yuan B, et al. Chemokine fractalkine attenuates overactivation and apoptosis of BV-2 microglial cells induced by extracellular ATP. Neurochem Res. 2013;38:1002–12.CrossRefPubMed
45.
go back to reference Johnston IN, Milligan ED, Wieseler-Frank J, Frank MG, Zapata V, Campisi J, et al. A role for proinflammatory cytokines and fractalkine in analgesia, tolerance, and subsequent pain facilitation induced by chronic intrathecal morphine. J Neurosci. 2004;24:7353–65.CrossRefPubMed Johnston IN, Milligan ED, Wieseler-Frank J, Frank MG, Zapata V, Campisi J, et al. A role for proinflammatory cytokines and fractalkine in analgesia, tolerance, and subsequent pain facilitation induced by chronic intrathecal morphine. J Neurosci. 2004;24:7353–65.CrossRefPubMed
46.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
47.
go back to reference Bouchon A, Dietrich J, Colonna M. Cutting edge: inflammatory responses can be triggered by TREM-1, a novel receptor expressed on neutrophils and monocytes. J Immunol. 2000;164:4991–5.CrossRefPubMed Bouchon A, Dietrich J, Colonna M. Cutting edge: inflammatory responses can be triggered by TREM-1, a novel receptor expressed on neutrophils and monocytes. J Immunol. 2000;164:4991–5.CrossRefPubMed
48.
go back to reference Gibot S, Kolopp-Sarda MN, Bene MC, Bollaert PE, Lozniewski A, Mory F, et al. A soluble form of the triggering receptor expressed on myeloid cells-1 modulates the inflammatory response in murine sepsis. J Exp Med. 2004;200:1419–26.CrossRefPubMedPubMedCentral Gibot S, Kolopp-Sarda MN, Bene MC, Bollaert PE, Lozniewski A, Mory F, et al. A soluble form of the triggering receptor expressed on myeloid cells-1 modulates the inflammatory response in murine sepsis. J Exp Med. 2004;200:1419–26.CrossRefPubMedPubMedCentral
49.
go back to reference Sgadari C, Farber JM, Angiolillo AL, Liao F, Teruya-Feldstein J, Burd PR, et al. Mig, the monokine induced by interferon-gamma, promotes tumor necrosis in vivo. Blood. 1997;89:2635–43.PubMed Sgadari C, Farber JM, Angiolillo AL, Liao F, Teruya-Feldstein J, Burd PR, et al. Mig, the monokine induced by interferon-gamma, promotes tumor necrosis in vivo. Blood. 1997;89:2635–43.PubMed
50.
go back to reference Jin T, Bokarewa M, Tarkowski A. Urokinase-type plasminogen activator, an endogenous antibiotic. J Infect Dis. 2005;192:429–37.CrossRefPubMed Jin T, Bokarewa M, Tarkowski A. Urokinase-type plasminogen activator, an endogenous antibiotic. J Infect Dis. 2005;192:429–37.CrossRefPubMed
51.
go back to reference Perch M, Kofoed P, Fischer TK, Co F, Rombo L, Rombo L, et al. Serum levels of soluble urokinase plasminogen activator receptor is associated with parasitemia in children with acute Plasmodium falciparum malaria infection. Parasite Immunol. 2004;26:207–11.CrossRefPubMed Perch M, Kofoed P, Fischer TK, Co F, Rombo L, Rombo L, et al. Serum levels of soluble urokinase plasminogen activator receptor is associated with parasitemia in children with acute Plasmodium falciparum malaria infection. Parasite Immunol. 2004;26:207–11.CrossRefPubMed
52.
go back to reference Cao D, Mizukami IF, Garni-Wagner BA, Kindzelskii AL, Todd RF 3rd, Boxer LA, et al. Human urokinase-type plasminogen activator primes neutrophils for superoxide anion release. Possible roles of complement receptor type 3 and calcium. J Immunol. 1995;154:1817–29.PubMed Cao D, Mizukami IF, Garni-Wagner BA, Kindzelskii AL, Todd RF 3rd, Boxer LA, et al. Human urokinase-type plasminogen activator primes neutrophils for superoxide anion release. Possible roles of complement receptor type 3 and calcium. J Immunol. 1995;154:1817–29.PubMed
53.
go back to reference Ostrowski SR, Shulman CE, Peshu N, Staalsoe T, Hoyer-Hansen G, Pedersen BK, et al. Elevated plasma urokinase receptor predicts low birth weight in maternal malaria. Parasite Immunol. 2007;29:37–46.CrossRefPubMed Ostrowski SR, Shulman CE, Peshu N, Staalsoe T, Hoyer-Hansen G, Pedersen BK, et al. Elevated plasma urokinase receptor predicts low birth weight in maternal malaria. Parasite Immunol. 2007;29:37–46.CrossRefPubMed
54.
go back to reference 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.CrossRefPubMed 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.CrossRefPubMed
55.
go back to reference D’Angelo C, De Luca A, Zelante T, Bonifazi P, Moretti S, Giovannini G, et al. Exogenous pentraxin 3 restores antifungal resistance and restrains inflammation in murine chronic granulomatous disease. J Immunol. 2009;183:4609–18.CrossRefPubMed D’Angelo C, De Luca A, Zelante T, Bonifazi P, Moretti S, Giovannini G, et al. Exogenous pentraxin 3 restores antifungal resistance and restrains inflammation in murine chronic granulomatous disease. J Immunol. 2009;183:4609–18.CrossRefPubMed
56.
go back to reference 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. J Exp Med. 2007;204:793–804.CrossRefPubMedPubMedCentral 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. J Exp Med. 2007;204:793–804.CrossRefPubMedPubMedCentral
57.
go back to reference Napoleone E, di Santo A, Peri G, Mantovani A, de Gaetano G, Donati MB, et al. The long pentraxin PTX3 up-regulates tissue factor in activated monocytes: another link between inflammation and clotting activation. J Leukoc Biol. 2004;76:203–9.CrossRefPubMed Napoleone E, di Santo A, Peri G, Mantovani A, de Gaetano G, Donati MB, et al. The long pentraxin PTX3 up-regulates tissue factor in activated monocytes: another link between inflammation and clotting activation. J Leukoc Biol. 2004;76:203–9.CrossRefPubMed
58.
go back to reference Fernandez-Real JM, Broch M, Richart C, Vendrell J, Lopez-Bermejo A, Ricart W. CD14 monocyte receptor, involved in the inflammatory cascade, and insulin sensitivity. J Clin Endocrinol Metab. 2003;88:1780–4.CrossRefPubMed Fernandez-Real JM, Broch M, Richart C, Vendrell J, Lopez-Bermejo A, Ricart W. CD14 monocyte receptor, involved in the inflammatory cascade, and insulin sensitivity. J Clin Endocrinol Metab. 2003;88:1780–4.CrossRefPubMed
59.
go back to reference Pan Z, Zhou L, Hetherington CJ, Zhang DE. Hepatocytes contribute to soluble CD14 production, and CD14 expression is differentially regulated in hepatocytes and monocytes. J Biol Chem. 2000;275:36430–5.CrossRefPubMed Pan Z, Zhou L, Hetherington CJ, Zhang DE. Hepatocytes contribute to soluble CD14 production, and CD14 expression is differentially regulated in hepatocytes and monocytes. J Biol Chem. 2000;275:36430–5.CrossRefPubMed
60.
go back to reference Sahay B, Patsey RL, Eggers CH, Salazar JC, Radolf JD, Sellati TJ. CD14 signaling restrains chronic inflammation through induction of p38-MAPK/SOCS-dependent tolerance. PLoS Pathog. 2009;5:e1000687.CrossRefPubMedPubMedCentral Sahay B, Patsey RL, Eggers CH, Salazar JC, Radolf JD, Sellati TJ. CD14 signaling restrains chronic inflammation through induction of p38-MAPK/SOCS-dependent tolerance. PLoS Pathog. 2009;5:e1000687.CrossRefPubMedPubMedCentral
61.
go back to reference Funderburg NT, Mayne E, Sieg SF, Asaad R, Jiang W, Luciano AA, et al. Increased tissue factor expression on circulating monocytes in chronic HIV infection: relationship to in vivo coagulation and immune activation. Blood. 2010;115:161–7.CrossRefPubMedPubMedCentral Funderburg NT, Mayne E, Sieg SF, Asaad R, Jiang W, Luciano AA, et al. Increased tissue factor expression on circulating monocytes in chronic HIV infection: relationship to in vivo coagulation and immune activation. Blood. 2010;115:161–7.CrossRefPubMedPubMedCentral
62.
go back to reference Pugin J, Heumann ID, Tomasz A, Kravchenko VV, Akamatsu Y, Nishijima M, et al. CD14 is a pattern recognition receptor. Immunity. 1994;1:509–16.CrossRefPubMed Pugin J, Heumann ID, Tomasz A, Kravchenko VV, Akamatsu Y, Nishijima M, et al. CD14 is a pattern recognition receptor. Immunity. 1994;1:509–16.CrossRefPubMed
63.
go back to reference Oxenkrug G, Tucker KL, Requintina P, Summergrad P. Neopterin, a marker of interferon-gamma-inducible inflammation, correlates with pyridoxal-5′-phosphate, waist circumference, HDL-cholesterol, insulin resistance and mortality risk in adult Boston community dwellers of Puerto Rican origin. Am J Neuroprot Neuroregen. 2011;3:48–52.CrossRefPubMedPubMedCentral Oxenkrug G, Tucker KL, Requintina P, Summergrad P. Neopterin, a marker of interferon-gamma-inducible inflammation, correlates with pyridoxal-5′-phosphate, waist circumference, HDL-cholesterol, insulin resistance and mortality risk in adult Boston community dwellers of Puerto Rican origin. Am J Neuroprot Neuroregen. 2011;3:48–52.CrossRefPubMedPubMedCentral
64.
go back to reference Biemba G, Gordeuk VR, Thuma PE, Mabeza GF, Weiss G. Prolonged macrophage activation and persistent anaemia in children with complicated malaria. Trop Med Int Health. 1998;3:60–5.CrossRefPubMed Biemba G, Gordeuk VR, Thuma PE, Mabeza GF, Weiss G. Prolonged macrophage activation and persistent anaemia in children with complicated malaria. Trop Med Int Health. 1998;3:60–5.CrossRefPubMed
65.
go back to reference Thuma PE, Weiss G, Herold M, Gordeuk VR. Serum neopterin, interleukin-4, and interleukin-6 concentrations in cerebral malaria patients and the effect of iron chelation therapy. Am J Trop Med Hyg. 1996;54:164–8.PubMed Thuma PE, Weiss G, Herold M, Gordeuk VR. Serum neopterin, interleukin-4, and interleukin-6 concentrations in cerebral malaria patients and the effect of iron chelation therapy. Am J Trop Med Hyg. 1996;54:164–8.PubMed
66.
go back to reference Gibot S, Kolopp-Sarda MN, Bene MC, Cravoisy A, Levy B, Faure GC, et al. Plasma level of a triggering receptor expressed on myeloid cells-1: its diagnostic accuracy in patients with suspected sepsis. Ann Intern Med. 2004;141:9–15.CrossRefPubMed Gibot S, Kolopp-Sarda MN, Bene MC, Cravoisy A, Levy B, Faure GC, et al. Plasma level of a triggering receptor expressed on myeloid cells-1: its diagnostic accuracy in patients with suspected sepsis. Ann Intern Med. 2004;141:9–15.CrossRefPubMed
67.
go back to reference Gibot S. Soluble triggering receptor expressed on myeloid cells and the diagnosis of pneumonia and severe sepsis. Semin Respir Crit Care Med. 2006;27:29–33.CrossRefPubMed Gibot S. Soluble triggering receptor expressed on myeloid cells and the diagnosis of pneumonia and severe sepsis. Semin Respir Crit Care Med. 2006;27:29–33.CrossRefPubMed
68.
go back to reference Spapen HD, Hachimi-Idrissi S, Corne L, Huyghens LP. Diagnostic markers of sepsis in the emergency department. Acta Clin Belg. 2006;1:138–42.CrossRef Spapen HD, Hachimi-Idrissi S, Corne L, Huyghens LP. Diagnostic markers of sepsis in the emergency department. Acta Clin Belg. 2006;1:138–42.CrossRef
69.
go back to reference Gibot S. The therapeutic potential of TREM-1 modulation in the treatment of sepsis and beyond. Curr Opin Investig Drugs. 2006;7:438–42.PubMed Gibot S. The therapeutic potential of TREM-1 modulation in the treatment of sepsis and beyond. Curr Opin Investig Drugs. 2006;7:438–42.PubMed
70.
go back to reference Ostrowski SR, Ullum H, Goka BQ, Hoyer-Hansen G, Obeng-Adjei G, Pedersen BK, et al. Plasma concentrations of soluble urokinase-type plasminogen activator receptor are increased in patients with malaria and are associated with a poor clinical or a fatal outcome. J Infect Dis. 2005;191:1331–41.CrossRefPubMed Ostrowski SR, Ullum H, Goka BQ, Hoyer-Hansen G, Obeng-Adjei G, Pedersen BK, et al. Plasma concentrations of soluble urokinase-type plasminogen activator receptor are increased in patients with malaria and are associated with a poor clinical or a fatal outcome. J Infect Dis. 2005;191:1331–41.CrossRefPubMed
71.
go back to reference Fevang B, Eugen-Olsen J, Yndestad A, Brosstad F, Beiske K, Aukrust P, et al. Enhanced levels of urokinase plasminogen activator and its soluble receptor in common variable immunodeficiency. Clin Immunol. 2009;131:438–46.CrossRefPubMed Fevang B, Eugen-Olsen J, Yndestad A, Brosstad F, Beiske K, Aukrust P, et al. Enhanced levels of urokinase plasminogen activator and its soluble receptor in common variable immunodeficiency. Clin Immunol. 2009;131:438–46.CrossRefPubMed
72.
go back to reference Clark IA, Alleva LM, Budd AC, Cowden WB. Understanding the role of inflammatory cytokines in malaria and related diseases. Travel Med Infect Dis. 2008;6:67–81.CrossRefPubMed Clark IA, Alleva LM, Budd AC, Cowden WB. Understanding the role of inflammatory cytokines in malaria and related diseases. Travel Med Infect Dis. 2008;6:67–81.CrossRefPubMed
73.
go back to reference Angulo I, Fresno M. Cytokines in the pathogenesis of and protection against malaria. Clin Diagn Lab Immunol. 2002;9:1145–52.PubMedPubMedCentral Angulo I, Fresno M. Cytokines in the pathogenesis of and protection against malaria. Clin Diagn Lab Immunol. 2002;9:1145–52.PubMedPubMedCentral
74.
go back to reference Erdman LK, Dhabangi A, Musoke C, Conroy AL, Hawkes M, Higgins S, et al. Combinations of host biomarkers predict mortality among Ugandan children with severe malaria: a retrospective case-control study. PLoS One. 2011;6:e17440.CrossRefPubMedPubMedCentral Erdman LK, Dhabangi A, Musoke C, Conroy AL, Hawkes M, Higgins S, et al. Combinations of host biomarkers predict mortality among Ugandan children with severe malaria: a retrospective case-control study. PLoS One. 2011;6:e17440.CrossRefPubMedPubMedCentral
Metadata
Title
Plasma levels of eight different mediators and their potential as biomarkers of various clinical malaria conditions in African children
Authors
Rachida Tahar
Catarina Albergaria
Neil Zeghidour
Vincent Foumane Ngane
Leonardo K. Basco
Christian Roussilhon
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2016
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-016-1378-3

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