Skip to main content
Top
Published in: BMC Infectious Diseases 1/2017

Open Access 01-12-2017 | Research article

Comparison of apoptosis in human primary pulmonary endothelial cells and a brain microvascular endothelial cell line co-cultured with Plasmodium falciparum field isolates

Authors: Jean Claude Biteghe Bi Essone, Nadine N’Dilimabaka, Julien Ondzaga, Jean Bernard Lekana-Douki, Dieudonné Nkoghe Mba, Philippe Deloron, Dominique Mazier, Frédrérick Gay, Fousseyni S. Touré Ndouo

Published in: BMC Infectious Diseases | Issue 1/2017

Login to get access

Abstract

Background

Plasmodium falciparum infection can progress unpredictably to severe forms including respiratory distress and cerebral malaria. The mechanisms underlying the variable natural course of malaria remain elusive.

Methods

The cerebral microvascular endothelial cells-D3 and lung endothelial cells both from human were cultured separately and challenged with P. falciparum field isolates taken directly from malaria patients or 3D7 strain (in vitro maintained culture). The capacity of these P. falciparum isolates to induce endothelial cell apoptosis via cytoadherence or not was then assessed.

Results

Overall, 27 P. falciparum isolates were collected from patients with uncomplicated malaria (n = 25) or severe malaria (n = 2). About half the isolates (n = 17) were able to bind brain endothelial cells (12 isolates, 44%) or lung endothelial cells (17 isolates, 63%) or both (12 isolates, 44%). Sixteen (59%) of the 27 isolates were apoptogenic for brain and/or lung endothelial cells. The apoptosis stimulus could be cytoadherence, direct cell-cell contact without cytoadherence, or diffusible soluble factors. While some of the apoptogenic isolates used two stimuli (direct contact with or without cytoadherence, plus soluble factors) to induce apoptosis, others used only one. Among the 16 apoptogenic isolates, eight specifically targeted brain endothelial cells, one lung endothelial cells, and seven both.

Conclusion

These results indicate that the brain microvascular cell line was more susceptible to apoptosis triggered by P. falciparum than the primary pulmonary endothelial cells and may have relevance to host-parasite interaction.
Literature
4.
5.
6.
go back to reference Pino P, Vouldoukis I, Kolb JP, Mahmoudi N, Desportes-Livage I, Bricaire F, et al. Plasmodium falciparum--infected erythrocyte adhesion induces caspase activation and apoptosis in human endothelial cells. J Infect Dis. 2003;187(8):1283–90. doi:10.1086/373992.CrossRefPubMed Pino P, Vouldoukis I, Kolb JP, Mahmoudi N, Desportes-Livage I, Bricaire F, et al. Plasmodium falciparum--infected erythrocyte adhesion induces caspase activation and apoptosis in human endothelial cells. J Infect Dis. 2003;187(8):1283–90. doi:10.​1086/​373992.CrossRefPubMed
7.
go back to reference Mazier D, Nitcheu J, Idrissa-Boubou M. Cerebral malaria and immunogenetics. Parasite Immunol. 2000;22(12):613–23.CrossRefPubMed Mazier D, Nitcheu J, Idrissa-Boubou M. Cerebral malaria and immunogenetics. Parasite Immunol. 2000;22(12):613–23.CrossRefPubMed
8.
go back to reference Taoufiq Z, Gay F, Balvanyos J, Ciceron L, Tefit M, Lechat P, et al. Rho kinase inhibition in severe malaria: thwarting parasite-induced collateral damage to endothelia. J Infect Dis. 2008;197(7):1062–73. doi:10.1086/528988.CrossRefPubMed Taoufiq Z, Gay F, Balvanyos J, Ciceron L, Tefit M, Lechat P, et al. Rho kinase inhibition in severe malaria: thwarting parasite-induced collateral damage to endothelia. J Infect Dis. 2008;197(7):1062–73. doi:10.​1086/​528988.CrossRefPubMed
9.
go back to reference Toure FS, Ouwe-Missi-Oukem-Boyer O, Bisvigou U, Moussa O, Rogier C, Pino P, et al. Apoptosis: a potential triggering mechanism of neurological manifestation in Plasmodium falciparum malaria. Parasite Immunol. 2008;30(1):47–51. doi:10.1111/j.1365-3024.2007.00986.x.PubMed Toure FS, Ouwe-Missi-Oukem-Boyer O, Bisvigou U, Moussa O, Rogier C, Pino P, et al. Apoptosis: a potential triggering mechanism of neurological manifestation in Plasmodium falciparum malaria. Parasite Immunol. 2008;30(1):47–51. doi:10.​1111/​j.​1365-3024.​2007.​00986.​x.PubMed
11.
go back to reference Zougbede S, Miller F, Ravassard P, Rebollo A, Ciceron L, Couraud PO, et al. Metabolic acidosis induced by Plasmodium falciparum intraerythrocytic stages alters blood-brain barrier integrity. J Cereb Blood Flow Metab. 2011;31(2):514–26. doi:10.1038/jcbfm.2010.121.CrossRefPubMed Zougbede S, Miller F, Ravassard P, Rebollo A, Ciceron L, Couraud PO, et al. Metabolic acidosis induced by Plasmodium falciparum intraerythrocytic stages alters blood-brain barrier integrity. J Cereb Blood Flow Metab. 2011;31(2):514–26. doi:10.​1038/​jcbfm.​2010.​121.CrossRefPubMed
14.
go back to reference Siau A, Toure FS, Ouwe-Missi-Oukem-Boyer O, Ciceron L, Mahmoudi N, Vaquero C, et al. Whole-transcriptome analysis of Plasmodium falciparum field isolates: identification of new pathogenicity factors. J Infect Dis. 2007;196(11):1603–12. doi:10.1086/522012.CrossRefPubMed Siau A, Toure FS, Ouwe-Missi-Oukem-Boyer O, Ciceron L, Mahmoudi N, Vaquero C, et al. Whole-transcriptome analysis of Plasmodium falciparum field isolates: identification of new pathogenicity factors. J Infect Dis. 2007;196(11):1603–12. doi:10.​1086/​522012.CrossRefPubMed
17.
go back to reference Muanza K, Gay F, Behr C, Scherf A. Primary culture of human lung microvessel endothelial cells: a useful in vitro model for studying Plasmodium falciparum-infected erythrocyte cytoadherence. Res Immunol. 1996;147(3):149–63. Muanza K, Gay F, Behr C, Scherf A. Primary culture of human lung microvessel endothelial cells: a useful in vitro model for studying Plasmodium falciparum-infected erythrocyte cytoadherence. Res Immunol. 1996;147(3):149–63.
18.
go back to reference Weksler BB, Subileau EA, Perriere N, Charneau P, Holloway K, Leveque M, et al. Blood-brain barrier-specific properties of a human adult brain endothelial cell line. FASEB J. 2005;19(13):1872–4. doi:10.1096/fj.04-3458fje.PubMed Weksler BB, Subileau EA, Perriere N, Charneau P, Holloway K, Leveque M, et al. Blood-brain barrier-specific properties of a human adult brain endothelial cell line. FASEB J. 2005;19(13):1872–4. doi:10.​1096/​fj.​04-3458fje.PubMed
19.
go back to reference Pino P, Taoufiq Z, Nitcheu J, Vouldoukis I, Mazier D. Blood-brain barrier breakdown during cerebral malaria: suicide or murder? Thromb Haemost. 2005;94(2):336–40. doi:10.1267/THRO05020336.PubMed Pino P, Taoufiq Z, Nitcheu J, Vouldoukis I, Mazier D. Blood-brain barrier breakdown during cerebral malaria: suicide or murder? Thromb Haemost. 2005;94(2):336–40. doi:10.​1267/​THRO05020336.PubMed
21.
go back to reference N'Dilimabaka N, Taoufiq Z, Zougbede S, Bonnefoy S, Lorthiois A, Couraud PO et al. P. falciparum isolate-specific distinct patterns of induced apoptosis in pulmonary and brain endothelial cells. PLoS One. 2014;9(3):e90692. doi:10.1371/journal.pone.0090692 N'Dilimabaka N, Taoufiq Z, Zougbede S, Bonnefoy S, Lorthiois A, Couraud PO et al. P. falciparum isolate-specific distinct patterns of induced apoptosis in pulmonary and brain endothelial cells. PLoS One. 2014;9(3):e90692. doi:10.​1371/​journal.​pone.​0090692
22.
go back to reference WHO. Severe falciparum malaria. World Health Organization, communicable diseases cluster. Trans R Soc Trop Med Hyg 2000;94(1):S1–90. WHO. Severe falciparum malaria. World Health Organization, communicable diseases cluster. Trans R Soc Trop Med Hyg 2000;94(1):S1–90.
23.
go back to reference Trager W, Jensen JB. Human malaria parasites in continuous culture. Science. 1976;193(4254):673–5.CrossRefPubMed Trager W, Jensen JB. Human malaria parasites in continuous culture. Science. 1976;193(4254):673–5.CrossRefPubMed
24.
go back to reference Goodyer ID, Johnson J, Eisenthal R, Hayes DJ. Purification of mature-stage Plasmodium falciparum by gelatine flotation. Ann Trop Med Parasitol. 1994;88(2):209–11.CrossRefPubMed Goodyer ID, Johnson J, Eisenthal R, Hayes DJ. Purification of mature-stage Plasmodium falciparum by gelatine flotation. Ann Trop Med Parasitol. 1994;88(2):209–11.CrossRefPubMed
25.
go back to reference Gay F, Robert C, Pouvelle B, Peyrol S, Scherf A, Gysin J. Isolation and characterization of brain microvascular endothelial cells from Saimiri monkeys. An in vitro model for sequestration of Plasmodium falciparum-infected erythrocytes. J Immunol Methods. 1995;184(1):15–28. Gay F, Robert C, Pouvelle B, Peyrol S, Scherf A, Gysin J. Isolation and characterization of brain microvascular endothelial cells from Saimiri monkeys. An in vitro model for sequestration of Plasmodium falciparum-infected erythrocytes. J Immunol Methods. 1995;184(1):15–28.
26.
go back to reference Toure FS, Ouwe-Missi-Oukem-Boyer O, Mezui-Me-Ndong J, Ndong-Atome GR, Bisvigou U, Mazier D, et al. Cytoadherence and genotype of Plasmodium falciparum strains from symptomatic children in Franceville, southeastern Gabon. Clin Med Res. 2007;5(2):106–13. doi:10.3121/cmr.2007.696.CrossRefPubMedPubMedCentral Toure FS, Ouwe-Missi-Oukem-Boyer O, Mezui-Me-Ndong J, Ndong-Atome GR, Bisvigou U, Mazier D, et al. Cytoadherence and genotype of Plasmodium falciparum strains from symptomatic children in Franceville, southeastern Gabon. Clin Med Res. 2007;5(2):106–13. doi:10.​3121/​cmr.​2007.​696.CrossRefPubMedPubMedCentral
27.
go back to reference Anders RF, Brown GV, Edwards A. Characterization of an S antigen synthesized by several isolates of Plasmodium falciparum. Proc Natl Acad Sci U S A. 1983;80(21):6652–6.CrossRefPubMedPubMedCentral Anders RF, Brown GV, Edwards A. Characterization of an S antigen synthesized by several isolates of Plasmodium falciparum. Proc Natl Acad Sci U S A. 1983;80(21):6652–6.CrossRefPubMedPubMedCentral
30.
go back to reference Meredith J Jr, Mu Z, Saido T, Du X. Cleavage of the cytoplasmic domain of the integrin beta3 subunit during endothelial cell apoptosis. J Biol Chem. 1998;273(31):19525–31.CrossRefPubMed Meredith J Jr, Mu Z, Saido T, Du X. Cleavage of the cytoplasmic domain of the integrin beta3 subunit during endothelial cell apoptosis. J Biol Chem. 1998;273(31):19525–31.CrossRefPubMed
31.
go back to reference Jimenez B, Volpert OV, Crawford SE, Febbraio M, Silverstein RL, Bouck N. Signals leading to apoptosis-dependent inhibition of neovascularization by thrombospondin-1. Nat Med. 2000;6(1):41–8. doi:10.1038/71517.CrossRefPubMed Jimenez B, Volpert OV, Crawford SE, Febbraio M, Silverstein RL, Bouck N. Signals leading to apoptosis-dependent inhibition of neovascularization by thrombospondin-1. Nat Med. 2000;6(1):41–8. doi:10.​1038/​71517.CrossRefPubMed
32.
go back to reference Ringwald P, Peyron F, Lepers JP, Rabarison P, Rakotomalala C, Razanamparany M, et al. Parasite virulence factors during falciparum malaria: rosetting, cytoadherence, and modulation of cytoadherence by cytokines. Infect Immun. 1993;61(12):5198–204.PubMedPubMedCentral Ringwald P, Peyron F, Lepers JP, Rabarison P, Rakotomalala C, Razanamparany M, et al. Parasite virulence factors during falciparum malaria: rosetting, cytoadherence, and modulation of cytoadherence by cytokines. Infect Immun. 1993;61(12):5198–204.PubMedPubMedCentral
33.
go back to reference Ockenhouse CF, Klotz FW, Tandon NN, Jamieson GA. Sequestrin, a CD36 recognition protein on Plasmodium falciparum malaria-infected erythrocytes identified by anti-idiotype antibodies. Proc Natl Acad Sci U S A. 1991;88(8):3175–9.CrossRefPubMedPubMedCentral Ockenhouse CF, Klotz FW, Tandon NN, Jamieson GA. Sequestrin, a CD36 recognition protein on Plasmodium falciparum malaria-infected erythrocytes identified by anti-idiotype antibodies. Proc Natl Acad Sci U S A. 1991;88(8):3175–9.CrossRefPubMedPubMedCentral
34.
go back to reference Chaiyaroj SC, Angkasekwinai P, Buranakiti A, Looareesuwan S, Rogerson SJ, Brown GV. Cytoadherence characteristics of Plasmodium falciparum isolates from Thailand: evidence for chondroitin sulfate a as a cytoadherence receptor. Am J Trop Med Hyg. 1996;55(1):76–80.CrossRefPubMed Chaiyaroj SC, Angkasekwinai P, Buranakiti A, Looareesuwan S, Rogerson SJ, Brown GV. Cytoadherence characteristics of Plasmodium falciparum isolates from Thailand: evidence for chondroitin sulfate a as a cytoadherence receptor. Am J Trop Med Hyg. 1996;55(1):76–80.CrossRefPubMed
Metadata
Title
Comparison of apoptosis in human primary pulmonary endothelial cells and a brain microvascular endothelial cell line co-cultured with Plasmodium falciparum field isolates
Authors
Jean Claude Biteghe Bi Essone
Nadine N’Dilimabaka
Julien Ondzaga
Jean Bernard Lekana-Douki
Dieudonné Nkoghe Mba
Philippe Deloron
Dominique Mazier
Frédrérick Gay
Fousseyni S. Touré Ndouo
Publication date
01-12-2017
Publisher
BioMed Central
Published in
BMC Infectious Diseases / Issue 1/2017
Electronic ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-017-2552-0

Other articles of this Issue 1/2017

BMC Infectious Diseases 1/2017 Go to the issue