Skip to main content
Top
Published in: Malaria Journal 1/2008

Open Access 01-12-2008 | Research

Cytokine-associated neutrophil extracellular traps and antinuclear antibodies in Plasmodium falciparum infected children under six years of age

Authors: Virginia S Baker, Godwin E Imade, Norman B Molta, Pallavi Tawde, Sunday D Pam, Michael O Obadofin, Soloman A Sagay, Daniel Z Egah, Daniel Iya, Bangmboye B Afolabi, Murray Baker, Karen Ford, Robert Ford, Kenneth H Roux, Thomas CS Keller III

Published in: Malaria Journal | Issue 1/2008

Login to get access

Abstract

Background

In Plasmodium falciparum-infected children, the relationships between blood cell histopathology, blood plasma components, development of immunocompetence and disease severity remain poorly understood. Blood from Nigerian children with uncomplicated malaria was analysed to gain insight into these relationships. This investigation presents evidence for circulating neutrophil extracellular traps (NETs) and antinuclear IgG antibodies (ANA). The presence of NETs and ANA to double-stranded DNA along with the cytokine profiles found suggests autoimmune mechanisms that could produce pathogenesis in children, but immunoprotection in adults.

Methods

Peripheral blood smear slides and blood samples obtained from 21 Nigerian children under six years of age, presenting with uncomplicated malaria before and seven days after initiation of sulphadoxine-pyrimethamine (SP) treatment were analysed. The slides were stained with Giemsa and with DAPI. Levels of the pro-inflammatory cytokines IFN-γ, IL-2, TNF, CRP, and IL-6, select anti-inflammatory cytokines TGF-β and IL-10, and ANA were determined by immunoassay.

Results

The children exhibited circulating NETs with adherent parasites and erythrocytes, elevated ANA levels, a Th2 dominated cytokine profile, and left-shifted leukocyte differential counts. Nonspecific ANA levels were significant in 86% of the children pretreatment and in 100% of the children seven days after SP treatment, but in only 33% of age-matched control samples collected during the season of low parasite transmission. Levels of ANA specific for dsDNA were significant in 81% of the children both pre-treatment and post treatment.

Conclusion

The results of this investigation suggest that NET formation and ANA to dsDNA may induce pathology in falciparum-infected children, but activate a protective mechanism against falciparum malaria in adults. The significance of in vivo circulating chromatin in NETs and dsDNA ANA as a causative factor in the hyporesponsiveness of CpG oligonucleotide-based malaria vaccines is discussed.
Appendix
Available only for authorised users
Literature
1.
go back to reference Good MF, Xu H, Wykes M, Engwerda CR: Development and regulation of cell-mediated immune responses to the blood stages of malaria: implications for vaccine research. Annu Rev Immunol. 2005, 23: 69-99. 10.1146/annurev.immunol.23.021704.115638.CrossRefPubMed Good MF, Xu H, Wykes M, Engwerda CR: Development and regulation of cell-mediated immune responses to the blood stages of malaria: implications for vaccine research. Annu Rev Immunol. 2005, 23: 69-99. 10.1146/annurev.immunol.23.021704.115638.CrossRefPubMed
2.
go back to reference Malaguarnera L, Musumeci S: The immune response to Plasmodium falciparum malaria. Lancet Infect Dis. 2002, 2: 472-478. 10.1016/S1473-3099(02)00344-4.CrossRefPubMed Malaguarnera L, Musumeci S: The immune response to Plasmodium falciparum malaria. Lancet Infect Dis. 2002, 2: 472-478. 10.1016/S1473-3099(02)00344-4.CrossRefPubMed
3.
go back to reference Stevenson MM, Riley EM: Innate immunity to malaria. Nat Rev Immunol. 2004, 4: 169-180. 10.1038/nri1311.CrossRefPubMed Stevenson MM, Riley EM: Innate immunity to malaria. Nat Rev Immunol. 2004, 4: 169-180. 10.1038/nri1311.CrossRefPubMed
4.
go back to reference Millington OR, Di Lorenzo C, Phillips RS, Garside P, Brewer JM: Suppression of adaptive immunity to heterologous antigens during Plasmodium infection through hemozoin-induced failure of dendritic cell function. J Biol. 2006, 5: 5-10.1186/jbiol34.PubMedCentralCrossRefPubMed Millington OR, Di Lorenzo C, Phillips RS, Garside P, Brewer JM: Suppression of adaptive immunity to heterologous antigens during Plasmodium infection through hemozoin-induced failure of dendritic cell function. J Biol. 2006, 5: 5-10.1186/jbiol34.PubMedCentralCrossRefPubMed
5.
go back to reference Nussenblatt V, Mukasa G, Metzger A, Ndeezi G, Garrett E, Semba RD: Anemia and interleukin-10, tumor necrosis factor alpha, and erythropoietin levels among children with acute, uncomplicated Plasmodium falciparum malaria. Clin Diagn Lab Immunol. 2001, 8: 1164-1170. 10.1128/CDLI.8.6.1164-1170.2001.PubMedCentralPubMed Nussenblatt V, Mukasa G, Metzger A, Ndeezi G, Garrett E, Semba RD: Anemia and interleukin-10, tumor necrosis factor alpha, and erythropoietin levels among children with acute, uncomplicated Plasmodium falciparum malaria. Clin Diagn Lab Immunol. 2001, 8: 1164-1170. 10.1128/CDLI.8.6.1164-1170.2001.PubMedCentralPubMed
6.
go back to reference Griffiths MJ, Shafi MJ, Popper SJ, Hemingway CA, Kortok MM, Wathen A, Rockett KA, Mott R, Levin M, Newton CR, Marsh K, Relman DA, Kwiatkowski DP: Genomewide analysis of the host response to malaria in Kenyan children. J Infect Dis. 2005, 191: 1599-1611. 10.1086/429297.CrossRef Griffiths MJ, Shafi MJ, Popper SJ, Hemingway CA, Kortok MM, Wathen A, Rockett KA, Mott R, Levin M, Newton CR, Marsh K, Relman DA, Kwiatkowski DP: Genomewide analysis of the host response to malaria in Kenyan children. J Infect Dis. 2005, 191: 1599-1611. 10.1086/429297.CrossRef
7.
go back to reference Nzila A, Ward SA, Marsh K, Sims PF, Hyde JE: Comparative folate metabolism in humans and malaria parasites (part II): activities as yet untargeted or specific to Plasmodium. Trends Parasitol. 2005, 21: 334-339. 10.1016/j.pt.2005.05.008.PubMedCentralCrossRefPubMed Nzila A, Ward SA, Marsh K, Sims PF, Hyde JE: Comparative folate metabolism in humans and malaria parasites (part II): activities as yet untargeted or specific to Plasmodium. Trends Parasitol. 2005, 21: 334-339. 10.1016/j.pt.2005.05.008.PubMedCentralCrossRefPubMed
8.
go back to reference Nzila A, Ward SA, Marsh K, Sims PF, Hyde JE: Comparative folate metabolism in humans and malaria parasites (part I): pointers for malaria treatment from cancer chemotherapy. Trends Parasitol. 2005, 21: 292-298. 10.1016/j.pt.2005.04.002.PubMedCentralCrossRefPubMed Nzila A, Ward SA, Marsh K, Sims PF, Hyde JE: Comparative folate metabolism in humans and malaria parasites (part I): pointers for malaria treatment from cancer chemotherapy. Trends Parasitol. 2005, 21: 292-298. 10.1016/j.pt.2005.04.002.PubMedCentralCrossRefPubMed
9.
go back to reference Chillemi R, Zappacosta B, Simpore J, Persichilli S, Musumeci M, Musumeci S: Hyperhomocysteinemia in acute Plasmodium falciparum malaria: an effect of host-parasite interaction. Clin Chim Acta. 2004, 348: 113-120. 10.1016/j.cccn.2004.05.007.CrossRefPubMed Chillemi R, Zappacosta B, Simpore J, Persichilli S, Musumeci M, Musumeci S: Hyperhomocysteinemia in acute Plasmodium falciparum malaria: an effect of host-parasite interaction. Clin Chim Acta. 2004, 348: 113-120. 10.1016/j.cccn.2004.05.007.CrossRefPubMed
10.
go back to reference Gregson A, Plowe CV: Mechanisms of resistance of malaria parasites to antifolates. Pharmacol Rev. 2005, 57: 117-145. 10.1124/pr.57.1.4.CrossRefPubMed Gregson A, Plowe CV: Mechanisms of resistance of malaria parasites to antifolates. Pharmacol Rev. 2005, 57: 117-145. 10.1124/pr.57.1.4.CrossRefPubMed
11.
go back to reference Many A, Schreiber L, Rosner S, Lessing JB, Eldor A, Kupferminc MJ: Pathologic features of the placenta in women with severe pregnancy complications and thrombophilia. Obstet Gynecol. 2001, 98: 1041-1044. 10.1016/S0029-7844(01)01621-0.CrossRefPubMed Many A, Schreiber L, Rosner S, Lessing JB, Eldor A, Kupferminc MJ: Pathologic features of the placenta in women with severe pregnancy complications and thrombophilia. Obstet Gynecol. 2001, 98: 1041-1044. 10.1016/S0029-7844(01)01621-0.CrossRefPubMed
12.
go back to reference Bulgan Kilicdag E, Ay G, Celik A, Ustundag B, Ozercan I, Simsek M: Oxidant-antioxidant system changes relative to placental-umbilical pathology in patients with preeclampsia. Hypertens Pregnancy. 2005, 24: 147-157. 10.1081/PRG-200059863.CrossRefPubMed Bulgan Kilicdag E, Ay G, Celik A, Ustundag B, Ozercan I, Simsek M: Oxidant-antioxidant system changes relative to placental-umbilical pathology in patients with preeclampsia. Hypertens Pregnancy. 2005, 24: 147-157. 10.1081/PRG-200059863.CrossRefPubMed
13.
go back to reference Moore JM, Chaisavaneeyakorn S, Perkins DJ, Othoro C, Otieno J, Nahlen BL, Shi YP, Udhayakumar V: Hemozoin differentially regulates proinflammatory cytokine production in human immunodeficiency virus-seropositive and -seronegative women with placental malaria. Infect Immun. 2004, 72: 7022-7029. 10.1128/IAI.72.12.7022-7029.2004.PubMedCentralCrossRef Moore JM, Chaisavaneeyakorn S, Perkins DJ, Othoro C, Otieno J, Nahlen BL, Shi YP, Udhayakumar V: Hemozoin differentially regulates proinflammatory cytokine production in human immunodeficiency virus-seropositive and -seronegative women with placental malaria. Infect Immun. 2004, 72: 7022-7029. 10.1128/IAI.72.12.7022-7029.2004.PubMedCentralCrossRef
14.
go back to reference Llurba E, Gratacos E, Martin-Gallan P, Cabero L, Dominguez C: A comprehensive study of oxidative stress and antioxidant status in preeclampsia and normal pregnancy. Free Radic Biol Med. 2004, 37: 557-570. 10.1016/j.freeradbiomed.2004.04.035.CrossRefPubMed Llurba E, Gratacos E, Martin-Gallan P, Cabero L, Dominguez C: A comprehensive study of oxidative stress and antioxidant status in preeclampsia and normal pregnancy. Free Radic Biol Med. 2004, 37: 557-570. 10.1016/j.freeradbiomed.2004.04.035.CrossRefPubMed
15.
go back to reference Muller S: Redox and antioxidant systems of the malaria parasite Plasmodium falciparum. Mol Microbiol. 2004, 53: 1291-1305. 10.1111/j.1365-2958.2004.04257.x.CrossRefPubMed Muller S: Redox and antioxidant systems of the malaria parasite Plasmodium falciparum. Mol Microbiol. 2004, 53: 1291-1305. 10.1111/j.1365-2958.2004.04257.x.CrossRefPubMed
16.
go back to reference Pabon A, Carmona J, Burgos LC, Blair S: Oxidative stress in patients with non-complicated malaria. Clin Biochem. 2003, 36: 71-78. 10.1016/S0009-9120(02)00423-X.CrossRefPubMed Pabon A, Carmona J, Burgos LC, Blair S: Oxidative stress in patients with non-complicated malaria. Clin Biochem. 2003, 36: 71-78. 10.1016/S0009-9120(02)00423-X.CrossRefPubMed
17.
go back to reference Taylor PR, Carugati A, Fadok VA, Cook HT, Andrews M, Carroll MC, Savill JS, Henson PM, Botto M, Walport MJ: A hierarchical role for classical pathway complement proteins in the clearance of apoptotic cells in vivo. J Exp Med. 2000, 192: 359-366. 10.1084/jem.192.3.359.PubMedCentralCrossRefPubMed Taylor PR, Carugati A, Fadok VA, Cook HT, Andrews M, Carroll MC, Savill JS, Henson PM, Botto M, Walport MJ: A hierarchical role for classical pathway complement proteins in the clearance of apoptotic cells in vivo. J Exp Med. 2000, 192: 359-366. 10.1084/jem.192.3.359.PubMedCentralCrossRefPubMed
18.
go back to reference Stoute JA, Odindo AO, Owuor BO, Mibei EK, Opollo MO, Waitumbi JN: Loss of red blood cell-complement regulatory proteins and increased levels of circulating immune complexes are associated with severe malarial anemia. J Infect Dis. 2003, 187: 522-525. 10.1086/367712.CrossRefPubMed Stoute JA, Odindo AO, Owuor BO, Mibei EK, Opollo MO, Waitumbi JN: Loss of red blood cell-complement regulatory proteins and increased levels of circulating immune complexes are associated with severe malarial anemia. J Infect Dis. 2003, 187: 522-525. 10.1086/367712.CrossRefPubMed
19.
go back to reference Ciurana CL, Zwart B, van Mierlo G, Hack CE: Complement activation by necrotic cells in normal plasma environment compares to that by late apoptotic cells and involves predominantly IgM. Eur J Immunol. 2004, 34: 2609-2619. 10.1002/eji.200425045.CrossRefPubMed Ciurana CL, Zwart B, van Mierlo G, Hack CE: Complement activation by necrotic cells in normal plasma environment compares to that by late apoptotic cells and involves predominantly IgM. Eur J Immunol. 2004, 34: 2609-2619. 10.1002/eji.200425045.CrossRefPubMed
20.
go back to reference Dernellis J, Panaretou M: Effects of C-reactive protein and the third and fourth components of complement (C3 and C4) on incidence of atrial fibrillation. Am J Cardiol. 2006, 97: 245-248. 10.1016/j.amjcard.2005.08.027.CrossRefPubMed Dernellis J, Panaretou M: Effects of C-reactive protein and the third and fourth components of complement (C3 and C4) on incidence of atrial fibrillation. Am J Cardiol. 2006, 97: 245-248. 10.1016/j.amjcard.2005.08.027.CrossRefPubMed
21.
go back to reference Kravitz MS, Pitashny M, Shoenfeld Y: Protective Molecules-C-Reactive Protein (CRP), Serum Amyloid P (SAP), Pentraxin3 (PTX3), Mannose-Binding Lectin (MBL), and Apolipoprotein A1 (Apo A1), and Their Autoantibodies: Prevalence and Clinical Significance in Autoimmunity. J Clin Immunol. 2005, 25: 582-591. 10.1007/s10875-005-7828-2.CrossRefPubMed Kravitz MS, Pitashny M, Shoenfeld Y: Protective Molecules-C-Reactive Protein (CRP), Serum Amyloid P (SAP), Pentraxin3 (PTX3), Mannose-Binding Lectin (MBL), and Apolipoprotein A1 (Apo A1), and Their Autoantibodies: Prevalence and Clinical Significance in Autoimmunity. J Clin Immunol. 2005, 25: 582-591. 10.1007/s10875-005-7828-2.CrossRefPubMed
22.
go back to reference Roumenina LT, Kantardjiev AA, Atanasov BP, Waters P, Gadjeva M, Reid KB, Mantovani A, Kishore U, Kojouharova MS: Role of Ca2+ in the electrostatic stability and the functional activity of the globular domain of human C1q. Biochemistry. 2005, 44: 14097-14109. 10.1021/bi051186n.CrossRefPubMed Roumenina LT, Kantardjiev AA, Atanasov BP, Waters P, Gadjeva M, Reid KB, Mantovani A, Kishore U, Kojouharova MS: Role of Ca2+ in the electrostatic stability and the functional activity of the globular domain of human C1q. Biochemistry. 2005, 44: 14097-14109. 10.1021/bi051186n.CrossRefPubMed
23.
go back to reference Li SH, Szmitko PE, Weisel RD, Wang CH, Fedak PW, Li RK, Mickle DA, Verma S: C-reactive protein upregulates complement-inhibitory factors in endothelial cells. Circulation. 2004, 109: 833-836. 10.1161/01.CIR.0000117087.27524.0E.CrossRefPubMed Li SH, Szmitko PE, Weisel RD, Wang CH, Fedak PW, Li RK, Mickle DA, Verma S: C-reactive protein upregulates complement-inhibitory factors in endothelial cells. Circulation. 2004, 109: 833-836. 10.1161/01.CIR.0000117087.27524.0E.CrossRefPubMed
24.
go back to reference Daniel-Ribeiro CT: Is there a role for autoimmunity in immune protection against malaria?. Mem Inst Oswaldo Cruz. 2000, 95: 199-207.CrossRefPubMed Daniel-Ribeiro CT: Is there a role for autoimmunity in immune protection against malaria?. Mem Inst Oswaldo Cruz. 2000, 95: 199-207.CrossRefPubMed
25.
go back to reference Chaiyaroj SC, Rutta AS, Muenthaisong K, Watkins P, Na Ubol M, Looareesuwan S: Reduced levels of transforming growth factor-beta1, interleukin-12 and increased migration inhibitory factor are associated with severe malaria. Acta Trop. 2004, 89: 319-327. 10.1016/j.actatropica.2003.10.010.CrossRefPubMed Chaiyaroj SC, Rutta AS, Muenthaisong K, Watkins P, Na Ubol M, Looareesuwan S: Reduced levels of transforming growth factor-beta1, interleukin-12 and increased migration inhibitory factor are associated with severe malaria. Acta Trop. 2004, 89: 319-327. 10.1016/j.actatropica.2003.10.010.CrossRefPubMed
26.
go back to reference Coltel N, Combes V, Hunt NH, Grau GE: Cerebral malaria -- a neurovascular pathology with many riddles still to be solved. Curr Neurovasc Res. 2004, 1: 91-110. 10.2174/1567202043480116.CrossRefPubMed Coltel N, Combes V, Hunt NH, Grau GE: Cerebral malaria -- a neurovascular pathology with many riddles still to be solved. Curr Neurovasc Res. 2004, 1: 91-110. 10.2174/1567202043480116.CrossRefPubMed
27.
go back to reference Dalton DK, Haynes L, Chu CQ, Swain SL, Wittmer S: Interferon gamma eliminates responding CD4 T cells during mycobacterial infection by inducing apoptosis of activated CD4 T cells. J Exp Med. 2000, 192: 117-122. 10.1084/jem.192.1.117.PubMedCentralCrossRef Dalton DK, Haynes L, Chu CQ, Swain SL, Wittmer S: Interferon gamma eliminates responding CD4 T cells during mycobacterial infection by inducing apoptosis of activated CD4 T cells. J Exp Med. 2000, 192: 117-122. 10.1084/jem.192.1.117.PubMedCentralCrossRef
28.
go back to reference Griffiths MJ, Ndungu F, Baird KL, Muller DP, Marsh K, Newton CR: Oxidative stress and erythrocyte damage in Kenyan children with severe Plasmodium falciparum malaria. Br J Haematol. 2001, 113: 486-491. 10.1046/j.1365-2141.2001.02758.x.CrossRefPubMed Griffiths MJ, Ndungu F, Baird KL, Muller DP, Marsh K, Newton CR: Oxidative stress and erythrocyte damage in Kenyan children with severe Plasmodium falciparum malaria. Br J Haematol. 2001, 113: 486-491. 10.1046/j.1365-2141.2001.02758.x.CrossRefPubMed
29.
go back to reference Jennings VM, Actor JK, Lal AA, Hunter RL: Cytokine profile suggesting that murine cerebral malaria is an encephalitis. Infect Immun. 1997, 65: 4883-4887.PubMedCentralPubMed Jennings VM, Actor JK, Lal AA, Hunter RL: Cytokine profile suggesting that murine cerebral malaria is an encephalitis. Infect Immun. 1997, 65: 4883-4887.PubMedCentralPubMed
30.
go back to reference Kern P, Hemmer CJ, Van Damme J, Gruss HJ, Dietrich M: Elevated tumor necrosis factor alpha and interleukin-6 serum levels as markers for complicated Plasmodium falciparum malaria. Am J Med. 1989, 87: 139-143.CrossRefPubMed Kern P, Hemmer CJ, Van Damme J, Gruss HJ, Dietrich M: Elevated tumor necrosis factor alpha and interleukin-6 serum levels as markers for complicated Plasmodium falciparum malaria. Am J Med. 1989, 87: 139-143.CrossRefPubMed
31.
go back to reference Kurtzhals JA, Adabayeri V, Goka BQ, Akanmori BD, Oliver-Commey JO, Nkrumah FK, Behr C, Hviid L: Low plasma concentrations of interleukin 10 in severe malarial anaemia compared with cerebral and uncomplicated malaria. Lancet. 1998, 351: 1768-1772. 10.1016/S0140-6736(97)09439-7.CrossRefPubMed Kurtzhals JA, Adabayeri V, Goka BQ, Akanmori BD, Oliver-Commey JO, Nkrumah FK, Behr C, Hviid L: Low plasma concentrations of interleukin 10 in severe malarial anaemia compared with cerebral and uncomplicated malaria. Lancet. 1998, 351: 1768-1772. 10.1016/S0140-6736(97)09439-7.CrossRefPubMed
32.
go back to reference May J, Lell B, Luty AJ, Meyer CG, Kremsner PG: Plasma interleukin-10:Tumor necrosis factor (TNF)-alpha ratio is associated with TNF promoter variants and predicts malarial complications. J Infect Dis. 2000, 182: 1570-1573. 10.1086/315857.CrossRef May J, Lell B, Luty AJ, Meyer CG, Kremsner PG: Plasma interleukin-10:Tumor necrosis factor (TNF)-alpha ratio is associated with TNF promoter variants and predicts malarial complications. J Infect Dis. 2000, 182: 1570-1573. 10.1086/315857.CrossRef
33.
go back to reference Malaguarnera L, Imbesi RM, Pignatelli S, Simpore J, Malaguarnera M, Musumeci S: Increased levels of interleukin-12 in Plasmodium falciparum malaria: correlation with the severity of disease. Parasite Immunol. 2002, 24: 387-389. 10.1046/j.1365-3024.2002.00478.x.CrossRefPubMed Malaguarnera L, Imbesi RM, Pignatelli S, Simpore J, Malaguarnera M, Musumeci S: Increased levels of interleukin-12 in Plasmodium falciparum malaria: correlation with the severity of disease. Parasite Immunol. 2002, 24: 387-389. 10.1046/j.1365-3024.2002.00478.x.CrossRefPubMed
34.
go back to reference Means RT, Krantz SB: Progress in understanding the pathogenesis of the anemia of chronic disease. Blood. 1992, 80: 1639-1647.PubMed Means RT, Krantz SB: Progress in understanding the pathogenesis of the anemia of chronic disease. Blood. 1992, 80: 1639-1647.PubMed
35.
go back to reference Wassmer SC, de Souza JB, Frere C, Candal FJ, Juhan-Vague I, Grau GE: TGF-beta1 released from activated platelets can induce TNF-stimulated human brain endothelium apoptosis: a new mechanism for microvascular lesion during cerebral malaria. J Immunol. 2006, 176: 1180-1184.CrossRefPubMed Wassmer SC, de Souza JB, Frere C, Candal FJ, Juhan-Vague I, Grau GE: TGF-beta1 released from activated platelets can induce TNF-stimulated human brain endothelium apoptosis: a new mechanism for microvascular lesion during cerebral malaria. J Immunol. 2006, 176: 1180-1184.CrossRefPubMed
36.
go back to reference Rae C, McQuillan JA, Parekh SB, Bubb WA, Weiser S, Balcar VJ, Hansen AM, Ball HJ, Hunt NH: Brain gene expression, metabolism, and bioenergetics: interrelationships in murine models of cerebral and noncerebral malaria. Faseb J. 2004, 18: 499-510. 10.1096/fj.03-0543com.CrossRefPubMed Rae C, McQuillan JA, Parekh SB, Bubb WA, Weiser S, Balcar VJ, Hansen AM, Ball HJ, Hunt NH: Brain gene expression, metabolism, and bioenergetics: interrelationships in murine models of cerebral and noncerebral malaria. Faseb J. 2004, 18: 499-510. 10.1096/fj.03-0543com.CrossRefPubMed
37.
go back to reference Gupta AK, Hasler P, Holzgreve W, Gebhardt S, Hahn S: Induction of neutrophil extracellular DNA lattices by placental microparticles and IL-8 and their presence in preeclampsia. Hum Immunol. 2005, 66: 1146-1154. 10.1016/j.humimm.2005.11.003.CrossRefPubMed Gupta AK, Hasler P, Holzgreve W, Gebhardt S, Hahn S: Induction of neutrophil extracellular DNA lattices by placental microparticles and IL-8 and their presence in preeclampsia. Hum Immunol. 2005, 66: 1146-1154. 10.1016/j.humimm.2005.11.003.CrossRefPubMed
38.
go back to reference Urban CF, Reichard U, Brinkmann V, Zychlinsky A: Neutrophil extracellular traps capture and kill Candida albicans yeast and hyphal forms. Cell Microbiol. 2006, 8: 668-676. 10.1111/j.1462-5822.2005.00659.x.CrossRefPubMed Urban CF, Reichard U, Brinkmann V, Zychlinsky A: Neutrophil extracellular traps capture and kill Candida albicans yeast and hyphal forms. Cell Microbiol. 2006, 8: 668-676. 10.1111/j.1462-5822.2005.00659.x.CrossRefPubMed
39.
go back to reference Festjens N, Vanden Berghe T, Vandenabeele P: Necrosis, a well-orchestrated form of cell demise: signalling cascades, important mediators and concomitant immune response. Biochim Biophys Acta. 2006, 1757: 1371-1387. 10.1016/j.bbabio.2006.06.014.CrossRefPubMed Festjens N, Vanden Berghe T, Vandenabeele P: Necrosis, a well-orchestrated form of cell demise: signalling cascades, important mediators and concomitant immune response. Biochim Biophys Acta. 2006, 1757: 1371-1387. 10.1016/j.bbabio.2006.06.014.CrossRefPubMed
40.
go back to reference Fuchs TA, Abed U, Goosmann C, Hurwitz R, Schulze I, Wahn V, Weinrauch Y, Brinkmann V, Zychlinsky A: Novel cell death program leads to neutrophil extracellular traps. J Cell Biol. 2007, 176: 231-241. 10.1083/jcb.200606027.PubMedCentralCrossRef Fuchs TA, Abed U, Goosmann C, Hurwitz R, Schulze I, Wahn V, Weinrauch Y, Brinkmann V, Zychlinsky A: Novel cell death program leads to neutrophil extracellular traps. J Cell Biol. 2007, 176: 231-241. 10.1083/jcb.200606027.PubMedCentralCrossRef
41.
go back to reference Golstein P, Kroemer G: Cell death by necrosis: towards a molecular definition. Trends Biochem Sci. 2007, 32: 37-43. 10.1016/j.tibs.2006.11.001.CrossRefPubMed Golstein P, Kroemer G: Cell death by necrosis: towards a molecular definition. Trends Biochem Sci. 2007, 32: 37-43. 10.1016/j.tibs.2006.11.001.CrossRefPubMed
42.
go back to reference Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, Weinrauch Y, Zychlinsky A: Neutrophil extracellular traps kill bacteria. Science. 2004, 303: 1532-1535. 10.1126/science.1092385.CrossRefPubMed Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, Weiss DS, Weinrauch Y, Zychlinsky A: Neutrophil extracellular traps kill bacteria. Science. 2004, 303: 1532-1535. 10.1126/science.1092385.CrossRefPubMed
43.
go back to reference Gurunathan S, Wu CY, Freidag BL, Seder RA: DNA vaccines: a key for inducing long-term cellular immunity. Curr Opin Immunol. 2000, 12: 442-447. 10.1016/S0952-7915(00)00118-7.CrossRefPubMed Gurunathan S, Wu CY, Freidag BL, Seder RA: DNA vaccines: a key for inducing long-term cellular immunity. Curr Opin Immunol. 2000, 12: 442-447. 10.1016/S0952-7915(00)00118-7.CrossRefPubMed
44.
go back to reference Bevaart L, Van Ojik HH, Sun AW, Sulahian TH, Leusen JH, Weiner GJ, Van De Winkel JG, Van Vugt MJ: CpG oligodeoxynucleotides enhance FcgammaRI-mediated cross presentation by dendritic cells. Int Immunol. 2004, 16: 1091-1098. 10.1093/intimm/dxh110.CrossRefPubMed Bevaart L, Van Ojik HH, Sun AW, Sulahian TH, Leusen JH, Weiner GJ, Van De Winkel JG, Van Vugt MJ: CpG oligodeoxynucleotides enhance FcgammaRI-mediated cross presentation by dendritic cells. Int Immunol. 2004, 16: 1091-1098. 10.1093/intimm/dxh110.CrossRefPubMed
45.
go back to reference Katung PY: Socio-economic factors responsible for poor utilisation of the primary health care services in a rural community in Nigeria. Niger J Med. 2001, 10: 28-29.PubMed Katung PY: Socio-economic factors responsible for poor utilisation of the primary health care services in a rural community in Nigeria. Niger J Med. 2001, 10: 28-29.PubMed
46.
go back to reference Molta NB, Watila IM, Ogucho S: Responses of Plasmodium falciparum infections to antimalarial drugs in north eastern Nigeria --Part 1: 1988-1995. Journal of Pharmacy and Bioresources. 2004, 1: 51-60. Molta NB, Watila IM, Ogucho S: Responses of Plasmodium falciparum infections to antimalarial drugs in north eastern Nigeria --Part 1: 1988-1995. Journal of Pharmacy and Bioresources. 2004, 1: 51-60.
47.
go back to reference Schellenberg D, Menendez C, Kahigwa E, Font F, Galindo C, Acosta C, Schellenberg JA, Aponte JJ, Kimario J, Urassa H, Mshinda H, Tanner M, Alonso P: African children with malaria in an area of intense Plasmodium falciparum transmission: features on admission to the hospital and risk factors for death. Am J Trop Med Hyg. 1999, 61: 431-438.PubMed Schellenberg D, Menendez C, Kahigwa E, Font F, Galindo C, Acosta C, Schellenberg JA, Aponte JJ, Kimario J, Urassa H, Mshinda H, Tanner M, Alonso P: African children with malaria in an area of intense Plasmodium falciparum transmission: features on admission to the hospital and risk factors for death. Am J Trop Med Hyg. 1999, 61: 431-438.PubMed
48.
go back to reference WHO/AFRO: Manual of Infection Prevention and Control Policies and Guidelines. 2001, Harare, Zimbabwe, World Health Organization Regional Office for Africa WHO/AFRO: Manual of Infection Prevention and Control Policies and Guidelines. 2001, Harare, Zimbabwe, World Health Organization Regional Office for Africa
49.
go back to reference Kobayashi Y, Ozawa M, Maruo N, Kondo M: [Megakaryocyte ploidy in patients with myelodysplastic syndrome--by microcytofluorometry with DAPI staining after removal of Wright-Giemsa staining]. Rinsho Ketsueki. 1989, 30: 1915-1922.PubMed Kobayashi Y, Ozawa M, Maruo N, Kondo M: [Megakaryocyte ploidy in patients with myelodysplastic syndrome--by microcytofluorometry with DAPI staining after removal of Wright-Giemsa staining]. Rinsho Ketsueki. 1989, 30: 1915-1922.PubMed
50.
go back to reference O'Conner BH: A color atlas and instruction manual of peripheral cell morphology. 1984, Philadelphia, Lippincott Williams & Wilkins O'Conner BH: A color atlas and instruction manual of peripheral cell morphology. 1984, Philadelphia, Lippincott Williams & Wilkins
51.
go back to reference Harmening DM: Clinical Hematology. 2002, Philadelphia, F.A. Davis Company, 4th Harmening DM: Clinical Hematology. 2002, Philadelphia, F.A. Davis Company, 4th
53.
go back to reference Urban CF, Lourido S, Zychlinsky A: How do microbes evade neutrophil killing?. Cell Microbiol. 2006, 8: 1687-1696. 10.1111/j.1462-5822.2006.00792.x.CrossRefPubMed Urban CF, Lourido S, Zychlinsky A: How do microbes evade neutrophil killing?. Cell Microbiol. 2006, 8: 1687-1696. 10.1111/j.1462-5822.2006.00792.x.CrossRefPubMed
54.
go back to reference Buchanan JT, Simpson AJ, Aziz RK, Liu GY, Kristian SA, Kotb M, Feramisco J, Nizet V: DNase expression allows the pathogen group A Streptococcus to escape killing in neutrophil extracellular traps. Curr Biol. 2006, 16: 396-400. 10.1016/j.cub.2005.12.039.CrossRefPubMed Buchanan JT, Simpson AJ, Aziz RK, Liu GY, Kristian SA, Kotb M, Feramisco J, Nizet V: DNase expression allows the pathogen group A Streptococcus to escape killing in neutrophil extracellular traps. Curr Biol. 2006, 16: 396-400. 10.1016/j.cub.2005.12.039.CrossRefPubMed
55.
go back to reference Rothfield NF, Stollar BD: The relation of immunoglobulin class, pattern of anti-nuclear antibody, and complement-fixing antibodies to DNA in sera from patients with systemic lupus erythematosus. J Clin Invest. 1967, 46: 1785-1794.PubMedCentralCrossRefPubMed Rothfield NF, Stollar BD: The relation of immunoglobulin class, pattern of anti-nuclear antibody, and complement-fixing antibodies to DNA in sera from patients with systemic lupus erythematosus. J Clin Invest. 1967, 46: 1785-1794.PubMedCentralCrossRefPubMed
56.
go back to reference Hahn BH: Antibodies to DNA. N Engl J Med. 1998, 338: 1359-1368. 10.1056/NEJM199805073381906.CrossRef Hahn BH: Antibodies to DNA. N Engl J Med. 1998, 338: 1359-1368. 10.1056/NEJM199805073381906.CrossRef
57.
go back to reference Rothfield NF: Clinical significance of antinuclear antibodies. J Med Assoc Ga. 1967, 56: 491-494.PubMed Rothfield NF: Clinical significance of antinuclear antibodies. J Med Assoc Ga. 1967, 56: 491-494.PubMed
58.
go back to reference Cairo MS: Prevention and treatment of hyperuricemia in hematological malignancies. Clin Lymphoma. 2002, 3 Suppl 1: S26-31.CrossRef Cairo MS: Prevention and treatment of hyperuricemia in hematological malignancies. Clin Lymphoma. 2002, 3 Suppl 1: S26-31.CrossRef
59.
go back to reference Arese M, Strasly M, Ruva C, Costamagna C, Ghigo D, MacAllister R, Verzetti G, Tetta C, Bosia A, Bussolino F: Regulation of nitric oxide synthesis in uraemia. Nephrol Dial Transplant. 1995, 10: 1386-1397.PubMed Arese M, Strasly M, Ruva C, Costamagna C, Ghigo D, MacAllister R, Verzetti G, Tetta C, Bosia A, Bussolino F: Regulation of nitric oxide synthesis in uraemia. Nephrol Dial Transplant. 1995, 10: 1386-1397.PubMed
60.
61.
go back to reference Phillips RE, Pasvol G: Anaemia of Plasmodium falciparum malaria. Baillieres Clin Haematol. 1992, 5: 315-330.CrossRefPubMed Phillips RE, Pasvol G: Anaemia of Plasmodium falciparum malaria. Baillieres Clin Haematol. 1992, 5: 315-330.CrossRefPubMed
62.
go back to reference Toure-Balde A, Sarthou JL, Aribot G, Michel P, Trape JF, Rogier C, Roussilhon C: Plasmodium falciparum induces apoptosis in human mononuclear cells. Infect Immun. 1996, 64: 744-750.PubMedCentralPubMed Toure-Balde A, Sarthou JL, Aribot G, Michel P, Trape JF, Rogier C, Roussilhon C: Plasmodium falciparum induces apoptosis in human mononuclear cells. Infect Immun. 1996, 64: 744-750.PubMedCentralPubMed
63.
go back to reference Mortensen RF, Zhong W: Regulation of phagocytic leukocyte activities by C-reactive protein. J Leukoc Biol. 2000, 67: 495-500.PubMed Mortensen RF, Zhong W: Regulation of phagocytic leukocyte activities by C-reactive protein. J Leukoc Biol. 2000, 67: 495-500.PubMed
64.
65.
go back to reference Zhouhong C, Flanders KC, Bertolette D, LA L, JU W, WT P, JJ L, FW R, AB R: Levels of phosphor-Smad2/3 are sensors of the interplay between effects of TGF-B and retinoic acid on monocytic and granulocytic differentiation of HL-60 cells. Blood. 2003, 101: 498-507. 10.1182/blood-2002-05-1549.CrossRef Zhouhong C, Flanders KC, Bertolette D, LA L, JU W, WT P, JJ L, FW R, AB R: Levels of phosphor-Smad2/3 are sensors of the interplay between effects of TGF-B and retinoic acid on monocytic and granulocytic differentiation of HL-60 cells. Blood. 2003, 101: 498-507. 10.1182/blood-2002-05-1549.CrossRef
66.
go back to reference Torzewski M, Rist C, Mortensen RF, Zwaka TP, Bienek M, Waltenberger J, Koenig W, Schmitz G, Hombach V, Torzewski J: C-reactive protein in the arterial intima: role of C-reactive protein receptor-dependent monocyte recruitment in atherogenesis. Arterioscler Thromb Vasc Biol. 2000, 20: 2094-2099.CrossRefPubMed Torzewski M, Rist C, Mortensen RF, Zwaka TP, Bienek M, Waltenberger J, Koenig W, Schmitz G, Hombach V, Torzewski J: C-reactive protein in the arterial intima: role of C-reactive protein receptor-dependent monocyte recruitment in atherogenesis. Arterioscler Thromb Vasc Biol. 2000, 20: 2094-2099.CrossRefPubMed
67.
go back to reference Gurunathan S, Klinman DM, Seder RA: DNA vaccines: immunology, application, and optimization*. Annu Rev Immunol. 2000, 18: 927-974. 10.1146/annurev.immunol.18.1.927.CrossRefPubMed Gurunathan S, Klinman DM, Seder RA: DNA vaccines: immunology, application, and optimization*. Annu Rev Immunol. 2000, 18: 927-974. 10.1146/annurev.immunol.18.1.927.CrossRefPubMed
68.
go back to reference Takeda K, Akira S: Toll-like receptors in innate immunity. Int Immunol. 2005, 17: 1-14. 10.1093/intimm/dxh186.CrossRef Takeda K, Akira S: Toll-like receptors in innate immunity. Int Immunol. 2005, 17: 1-14. 10.1093/intimm/dxh186.CrossRef
Metadata
Title
Cytokine-associated neutrophil extracellular traps and antinuclear antibodies in Plasmodium falciparum infected children under six years of age
Authors
Virginia S Baker
Godwin E Imade
Norman B Molta
Pallavi Tawde
Sunday D Pam
Michael O Obadofin
Soloman A Sagay
Daniel Z Egah
Daniel Iya
Bangmboye B Afolabi
Murray Baker
Karen Ford
Robert Ford
Kenneth H Roux
Thomas CS Keller III
Publication date
01-12-2008
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2008
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-7-41

Other articles of this Issue 1/2008

Malaria Journal 1/2008 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.