Skip to main content
Top
Published in: Malaria Journal 1/2013

Open Access 01-12-2013 | Research

High levels of IgG3 anti ICB2-5 in Plasmodium vivax-infected individuals who did not develop symptoms

Authors: Fernanda G Versiani, Maria EM Almeida, Gisely C Melo, Francivaldo OL Versiani, Patrícia P Orlandi, Luís André M Mariúba, Leidiane A Soares, Luciana P Souza, Antonio A da Silva Balieiro, Wuelton M Monteiro, Fabio TM Costa, Hernando A del Portillo, Marcus VG Lacerda, Paulo A Nogueira

Published in: Malaria Journal | Issue 1/2013

Login to get access

Abstract

Background

Plasmodium vivax has the potential to infect 2.85 billion individuals worldwide. Nevertheless, the limited number of studies investigating the immune status of individuals living in malaria-endemic areas, as well as the lack of reports investigating serological markers associated with clinical protection, has hampered development of vaccines for P. vivax. It was previously demonstrated that naturally total IgG against the N-terminus of P. vivax merozoite surface protein 1 (Pv-MSP1) was associated with reduced risk of malarial infection.

Methods

Immune response against Pv-MSP1 (N-terminus) of 313 residents of the Rio Pardo rural settlement (Amazonas State, Brazil) was evaluated in a cross-sectional and longitudinal follow up over two months (on site) wherein gold standard diagnosis by thick blood smear and rRNA gene-based nested real-time PCR were used to discriminate symptomless Plasmodium vivax-infected individuals who did not develop clinical symptoms during a 2-months from those uninfected ones or who have had acute malaria. The acquisition of antibodies against Pv-MSP1 was also evaluated as survival analysis by prospective study over a year collecting information of new malaria infections in surveillance database.

Results

The majority of P. vivax-infected individuals (52-67%) showed immune recognition of the N-terminus of Pv-MSP1. Interesting data on infected individuals who have not developed symptoms, total IgG levels against the N-terminus Pv-MSP1 were age-dependent and the IgG3 levels were significantly higher than levels of subjects had acute malaria or those uninfected ones. The total IgG anti ICB2-5 was detected to be an important factor of protection against new malaria vivax attacks in survival analysis in a prospective survey (p = 0.029).

Conclusions

The study findings illustrate the importance of IgG3 associated to 2-months of symptomless in P. vivax infected individuals and open perspectives for the rationale of malaria vaccine designs capable to sustain high levels of IgG3 against polymorphic malaria antigens.
Appendix
Available only for authorised users
Literature
1.
go back to reference Mueller I, Galinski MR, Baird JK, Carlton JM, Kochar DK, Alonso PL, del Portillo HA: Key gaps in the knowledge of Plasmodium vivax, a neglected human malaria parasite. Lancet Infect Dis. 2009, 9: 555-566. 10.1016/S1473-3099(09)70177-X.CrossRefPubMed Mueller I, Galinski MR, Baird JK, Carlton JM, Kochar DK, Alonso PL, del Portillo HA: Key gaps in the knowledge of Plasmodium vivax, a neglected human malaria parasite. Lancet Infect Dis. 2009, 9: 555-566. 10.1016/S1473-3099(09)70177-X.CrossRefPubMed
2.
go back to reference Galinski MR, Barnwell JW: Plasmodium vivax: who cares?. Malar J. 2008, 1 (7): S9-CrossRef Galinski MR, Barnwell JW: Plasmodium vivax: who cares?. Malar J. 2008, 1 (7): S9-CrossRef
3.
go back to reference Oliveira-Ferreira J, Lacerda MV, Brasil P, Ladislau JL, Tauil PL, Daniel-Ribeiro CT: Malaria in Brazil: an overview. Malar J. 2010, 9: 115-10.1186/1475-2875-9-115.PubMedCentralCrossRefPubMed Oliveira-Ferreira J, Lacerda MV, Brasil P, Ladislau JL, Tauil PL, Daniel-Ribeiro CT: Malaria in Brazil: an overview. Malar J. 2010, 9: 115-10.1186/1475-2875-9-115.PubMedCentralCrossRefPubMed
4.
go back to reference Lacerda MV, Mourao MP, Alexandre MA, Siqueira AM, Magalhaes BM, Martinez-Espinosa FE, Filho FS, Brasil P, Ventura AM, Tada MS, Couto VS, Silva AR, Silva RS, Alecrim MG: Understanding the clinical spectrum of complicated Plasmodium vivax malaria: a systematic review on the contributions of the Brazilian literature. Malar J. 2012, 11: 12-10.1186/1475-2875-11-12.PubMedCentralCrossRefPubMed Lacerda MV, Mourao MP, Alexandre MA, Siqueira AM, Magalhaes BM, Martinez-Espinosa FE, Filho FS, Brasil P, Ventura AM, Tada MS, Couto VS, Silva AR, Silva RS, Alecrim MG: Understanding the clinical spectrum of complicated Plasmodium vivax malaria: a systematic review on the contributions of the Brazilian literature. Malar J. 2012, 11: 12-10.1186/1475-2875-11-12.PubMedCentralCrossRefPubMed
5.
go back to reference Costa FT, Lopes SC, Albrecht L, Ataide R, Siqueira AM, Souza RM, Russell B, Renia L, Marinho CR, Lacerda MV: On the pathogenesis of Plasmodium vivax malaria: perspectives from the Brazilian field. Int J Parasitol. 2012, 42: 1099-1105. 10.1016/j.ijpara.2012.08.007.CrossRefPubMed Costa FT, Lopes SC, Albrecht L, Ataide R, Siqueira AM, Souza RM, Russell B, Renia L, Marinho CR, Lacerda MV: On the pathogenesis of Plasmodium vivax malaria: perspectives from the Brazilian field. Int J Parasitol. 2012, 42: 1099-1105. 10.1016/j.ijpara.2012.08.007.CrossRefPubMed
6.
go back to reference Carvalho BO, Lopes SC, Nogueira PA, Orlandi PP, Bargieri DY, Blanco YC, Mamoni R, Leite JA, Rodrigues MM, Soares IS, Oliveira TR, Wunderlich G, Lacerda MV, del Portillo HA, Araújo MO, Russell B, Suwanarusk R, Snounou G, Rénia L, Costa FT: On the cytoadhesion of Plasmodium vivax-infected erythrocytes. J Infect Dis. 2010, 202: 638-647. 10.1086/654815.CrossRefPubMed Carvalho BO, Lopes SC, Nogueira PA, Orlandi PP, Bargieri DY, Blanco YC, Mamoni R, Leite JA, Rodrigues MM, Soares IS, Oliveira TR, Wunderlich G, Lacerda MV, del Portillo HA, Araújo MO, Russell B, Suwanarusk R, Snounou G, Rénia L, Costa FT: On the cytoadhesion of Plasmodium vivax-infected erythrocytes. J Infect Dis. 2010, 202: 638-647. 10.1086/654815.CrossRefPubMed
7.
go back to reference Lu F, Wang B, Cao J, Sattabongkot J, Zhou H, Zhu G, Kim K, Gao Q, Han ET: Prevalence of drug resistance-associated gene mutations in Plasmodium vivax in Central China. Korean J Parasitol. 2012, 50: 379-384. 10.3347/kjp.2012.50.4.379.PubMedCentralCrossRefPubMed Lu F, Wang B, Cao J, Sattabongkot J, Zhou H, Zhu G, Kim K, Gao Q, Han ET: Prevalence of drug resistance-associated gene mutations in Plasmodium vivax in Central China. Korean J Parasitol. 2012, 50: 379-384. 10.3347/kjp.2012.50.4.379.PubMedCentralCrossRefPubMed
8.
go back to reference Garg S, Saxena V, Lumb V, Pakalapati D, Boopathi PA, Subudhi AK, Chowdhury S, Kochar SK, Kochar DK, Sharma YD, Das A: Novel mutations in the antifolate drug resistance marker genes among Plasmodium vivax isolates exhibiting severe manifestations. Exp Parasitol. 2012, 132: 410-416. 10.1016/j.exppara.2012.09.018.CrossRefPubMed Garg S, Saxena V, Lumb V, Pakalapati D, Boopathi PA, Subudhi AK, Chowdhury S, Kochar SK, Kochar DK, Sharma YD, Das A: Novel mutations in the antifolate drug resistance marker genes among Plasmodium vivax isolates exhibiting severe manifestations. Exp Parasitol. 2012, 132: 410-416. 10.1016/j.exppara.2012.09.018.CrossRefPubMed
9.
go back to reference Vargas-Rodriguez Rdel C, da Silva BM, Menezes MJ, Orjuela-Sanchez P, Ferreira MU: Single-nucleotide polymorphism and copy number variation of the multidrug resistance-1 locus of Plasmodium vivax: local and global patterns. Am J Trop Med Hyg. 2012, 87: 813-821. 10.4269/ajtmh.2012.12-0094.CrossRefPubMed Vargas-Rodriguez Rdel C, da Silva BM, Menezes MJ, Orjuela-Sanchez P, Ferreira MU: Single-nucleotide polymorphism and copy number variation of the multidrug resistance-1 locus of Plasmodium vivax: local and global patterns. Am J Trop Med Hyg. 2012, 87: 813-821. 10.4269/ajtmh.2012.12-0094.CrossRefPubMed
10.
go back to reference Kerlin DH, Boyce K, Marfurt J, Simpson JA, Kenangalem E, Cheng Q, Price RN, Gatton ML: An analytical method for assessing stage-specific drug activity in Plasmodium vivax malaria: implications for ex vivo drug susceptibility testing. PLoS Negl Trop Dis. 2012, 6: e1772-10.1371/journal.pntd.0001772.PubMedCentralCrossRefPubMed Kerlin DH, Boyce K, Marfurt J, Simpson JA, Kenangalem E, Cheng Q, Price RN, Gatton ML: An analytical method for assessing stage-specific drug activity in Plasmodium vivax malaria: implications for ex vivo drug susceptibility testing. PLoS Negl Trop Dis. 2012, 6: e1772-10.1371/journal.pntd.0001772.PubMedCentralCrossRefPubMed
11.
go back to reference Marfurt J, Chalfein F, Prayoga P, Wabiser F, Wirjanata G, Sebayang B, Piera KA, Wittlin S, Haynes RK, Mohrle JJ, Anstey NM, Kenangalem E, Price RN: Comparative ex vivo activity of novel endoperoxides in multidrug-resistant Plasmodium falciparum and P. vivax. Antimicrob Agents Chemother. 2012, 56: 5258-5263. 10.1128/AAC.00283-12.PubMedCentralCrossRefPubMed Marfurt J, Chalfein F, Prayoga P, Wabiser F, Wirjanata G, Sebayang B, Piera KA, Wittlin S, Haynes RK, Mohrle JJ, Anstey NM, Kenangalem E, Price RN: Comparative ex vivo activity of novel endoperoxides in multidrug-resistant Plasmodium falciparum and P. vivax. Antimicrob Agents Chemother. 2012, 56: 5258-5263. 10.1128/AAC.00283-12.PubMedCentralCrossRefPubMed
12.
go back to reference Aguiar AC, Santos Rde M, Figueiredo FJ, Cortopassi WA, Pimentel AS, Franca TC, Meneghetti MR, Krettli AU: Antimalarial activity and mechanisms of action of two novel 4-aminoquinolines against chloroquine-resistant parasites. PLoS One. 2012, 7: e37259-10.1371/journal.pone.0037259.PubMedCentralCrossRefPubMed Aguiar AC, Santos Rde M, Figueiredo FJ, Cortopassi WA, Pimentel AS, Franca TC, Meneghetti MR, Krettli AU: Antimalarial activity and mechanisms of action of two novel 4-aminoquinolines against chloroquine-resistant parasites. PLoS One. 2012, 7: e37259-10.1371/journal.pone.0037259.PubMedCentralCrossRefPubMed
13.
14.
go back to reference Gama BE, Lacerda MV, Daniel-Ribeiro CT, Ferreira-da-Cruz Mde F: Chemoresistance of Plasmodium falciparum and Plasmodium vivax parasites in Brazil: consequences on disease morbidity and control. Mem Inst Oswaldo Cruz. 2011, 106 (1): 159-166.CrossRefPubMed Gama BE, Lacerda MV, Daniel-Ribeiro CT, Ferreira-da-Cruz Mde F: Chemoresistance of Plasmodium falciparum and Plasmodium vivax parasites in Brazil: consequences on disease morbidity and control. Mem Inst Oswaldo Cruz. 2011, 106 (1): 159-166.CrossRefPubMed
15.
go back to reference Alexandre MA, Ferreira CO, Siqueira AM, Magalhaes BL, Mourao MP, Lacerda MV, Alecrim M: Severe Plasmodium vivax malaria, Brazilian Amazon. Emerg Infect Dis. 2010, 16: 1611-1614. 10.3201/eid1610.100685.PubMedCentralCrossRefPubMed Alexandre MA, Ferreira CO, Siqueira AM, Magalhaes BL, Mourao MP, Lacerda MV, Alecrim M: Severe Plasmodium vivax malaria, Brazilian Amazon. Emerg Infect Dis. 2010, 16: 1611-1614. 10.3201/eid1610.100685.PubMedCentralCrossRefPubMed
16.
go back to reference Price RN, Douglas NM, Anstey NM: New developments in Plasmodium vivax malaria: severe disease and the rise of chloroquine resistance. Curr Opin Infect Dis. 2009, 22: 430-435. 10.1097/QCO.0b013e32832f14c1.CrossRefPubMed Price RN, Douglas NM, Anstey NM: New developments in Plasmodium vivax malaria: severe disease and the rise of chloroquine resistance. Curr Opin Infect Dis. 2009, 22: 430-435. 10.1097/QCO.0b013e32832f14c1.CrossRefPubMed
17.
go back to reference Holder AA, Blackman MJ, Burghaus PA, Chappel JA, Ling IT, McCallum-Deighton N, Shai S: A malaria merozoite surface protein (MSP1)-structure, processing and function. Mem Inst Oswaldo Cruz. 1992, 87 (Suppl 3): 37-42.CrossRefPubMed Holder AA, Blackman MJ, Burghaus PA, Chappel JA, Ling IT, McCallum-Deighton N, Shai S: A malaria merozoite surface protein (MSP1)-structure, processing and function. Mem Inst Oswaldo Cruz. 1992, 87 (Suppl 3): 37-42.CrossRefPubMed
18.
go back to reference Kadekoppala M, Holder AA: Merozoite surface proteins of the malaria parasite: the MSP1 complex and the MSP7 family. Int J Parasitol. 2010, 40: 1155-1161. 10.1016/j.ijpara.2010.04.008.CrossRefPubMed Kadekoppala M, Holder AA: Merozoite surface proteins of the malaria parasite: the MSP1 complex and the MSP7 family. Int J Parasitol. 2010, 40: 1155-1161. 10.1016/j.ijpara.2010.04.008.CrossRefPubMed
19.
go back to reference Putaporntip C, Jongwutiwes S, Sakihama N, Ferreira MU, Kho WG, Kaneko A, Kanbara H, Hattori T, Tanabe K: Mosaic organization and heterogeneity in frequency of allelic recombination of the Plasmodium vivax merozoite surface protein-1 locus. Proc Natl Acad Sci USA. 2002, 99: 16348-16353. 10.1073/pnas.252348999.PubMedCentralCrossRefPubMed Putaporntip C, Jongwutiwes S, Sakihama N, Ferreira MU, Kho WG, Kaneko A, Kanbara H, Hattori T, Tanabe K: Mosaic organization and heterogeneity in frequency of allelic recombination of the Plasmodium vivax merozoite surface protein-1 locus. Proc Natl Acad Sci USA. 2002, 99: 16348-16353. 10.1073/pnas.252348999.PubMedCentralCrossRefPubMed
20.
go back to reference del Portillo HA, Longacre S, Khouri E, David PH: Primary structure of the merozoite surface antigen 1 of Plasmodium vivax reveals sequences conserved between different Plasmodium species. Proc Natl Acad Sci USA. 1991, 88: 4030-4034. 10.1073/pnas.88.9.4030.PubMedCentralCrossRefPubMed del Portillo HA, Longacre S, Khouri E, David PH: Primary structure of the merozoite surface antigen 1 of Plasmodium vivax reveals sequences conserved between different Plasmodium species. Proc Natl Acad Sci USA. 1991, 88: 4030-4034. 10.1073/pnas.88.9.4030.PubMedCentralCrossRefPubMed
21.
go back to reference Ellis RD, Wu Y, Martin LB, Shaffer D, Miura K, Aebig J, Orcutt A, Rausch K, Zhu D, Mogensen A, Fay MP, Narum DL, Long C, Miller L, Durbin AP: Phase 1 study in malaria naive adults of BSAM2/Alhydrogel(R) + CPG 7909, a blood stage vaccine against P. falciparum malaria. PLoS One. 2012, 7: e46094-10.1371/journal.pone.0046094.PubMedCentralCrossRefPubMed Ellis RD, Wu Y, Martin LB, Shaffer D, Miura K, Aebig J, Orcutt A, Rausch K, Zhu D, Mogensen A, Fay MP, Narum DL, Long C, Miller L, Durbin AP: Phase 1 study in malaria naive adults of BSAM2/Alhydrogel(R) + CPG 7909, a blood stage vaccine against P. falciparum malaria. PLoS One. 2012, 7: e46094-10.1371/journal.pone.0046094.PubMedCentralCrossRefPubMed
22.
go back to reference Bergmann-Leitner ES, Duncan EH, Mease RM, Angov E: Impact of pre-existing MSP1(42)-allele specific immunity on potency of an erythrocytic Plasmodium falciparum vaccine. Malar J. 2012, 11: 315-10.1186/1475-2875-11-315.PubMedCentralCrossRefPubMed Bergmann-Leitner ES, Duncan EH, Mease RM, Angov E: Impact of pre-existing MSP1(42)-allele specific immunity on potency of an erythrocytic Plasmodium falciparum vaccine. Malar J. 2012, 11: 315-10.1186/1475-2875-11-315.PubMedCentralCrossRefPubMed
23.
go back to reference Moss DK, Remarque EJ, Faber BW, Cavanagh DR, Arnot DE, Thomas AW, Holder AA: Plasmodium falciparum 19-kilodalton merozoite surface protein 1 (MSP1)-specific antibodies that interfere with parasite growth in vitro can inhibit MSP1 processing, merozoite invasion, and intracellular parasite development. Infect Immun. 2012, 80: 1280-1287. 10.1128/IAI.05887-11.PubMedCentralCrossRefPubMed Moss DK, Remarque EJ, Faber BW, Cavanagh DR, Arnot DE, Thomas AW, Holder AA: Plasmodium falciparum 19-kilodalton merozoite surface protein 1 (MSP1)-specific antibodies that interfere with parasite growth in vitro can inhibit MSP1 processing, merozoite invasion, and intracellular parasite development. Infect Immun. 2012, 80: 1280-1287. 10.1128/IAI.05887-11.PubMedCentralCrossRefPubMed
24.
go back to reference Cowan GJ, Creasey AM, Dhanasarnsombut K, Thomas AW, Remarque EJ, Cavanagh DR: A malaria vaccine based on the polymorphic block 2 region of MSP-1 that elicits a broad serotype-spanning immune response. PLoS One. 2011, 6: e26616-10.1371/journal.pone.0026616.PubMedCentralCrossRefPubMed Cowan GJ, Creasey AM, Dhanasarnsombut K, Thomas AW, Remarque EJ, Cavanagh DR: A malaria vaccine based on the polymorphic block 2 region of MSP-1 that elicits a broad serotype-spanning immune response. PLoS One. 2011, 6: e26616-10.1371/journal.pone.0026616.PubMedCentralCrossRefPubMed
25.
go back to reference Sheehy SH, Duncan CJ, Elias SC, Collins KA, Ewer KJ, Spencer AJ, Williams AR, Halstead FD, Moretz SE, Miura K, Epp C, Dicks MD, Poulton ID, Lawrie AM, Berrie E, Moyle S, Long CA, Colloca S, Cortese R, Gilbert SC, Nicosia A, Hill AV, Draper SJ: Phase Ia clinical evaluation of the Plasmodium falciparum blood-stage antigen MSP1 in ChAd63 and MVA vaccine vectors. Mol Ther. 2011, 19: 2269-2276. 10.1038/mt.2011.176.PubMedCentralCrossRefPubMed Sheehy SH, Duncan CJ, Elias SC, Collins KA, Ewer KJ, Spencer AJ, Williams AR, Halstead FD, Moretz SE, Miura K, Epp C, Dicks MD, Poulton ID, Lawrie AM, Berrie E, Moyle S, Long CA, Colloca S, Cortese R, Gilbert SC, Nicosia A, Hill AV, Draper SJ: Phase Ia clinical evaluation of the Plasmodium falciparum blood-stage antigen MSP1 in ChAd63 and MVA vaccine vectors. Mol Ther. 2011, 19: 2269-2276. 10.1038/mt.2011.176.PubMedCentralCrossRefPubMed
26.
go back to reference Tetteh KK, Conway DJ: A polyvalent hybrid protein elicits antibodies against the diverse allelic types of block 2 in Plasmodium falciparum merozoite surface protein 1. Vaccine. 2011, 29: 7811-7817. 10.1016/j.vaccine.2011.07.106.PubMedCentralCrossRefPubMed Tetteh KK, Conway DJ: A polyvalent hybrid protein elicits antibodies against the diverse allelic types of block 2 in Plasmodium falciparum merozoite surface protein 1. Vaccine. 2011, 29: 7811-7817. 10.1016/j.vaccine.2011.07.106.PubMedCentralCrossRefPubMed
27.
go back to reference Soares IS, Levitus G, Souza JM, Del Portillo HA, Rodrigues MM: Acquired immune responses to the N- and C-terminal regions of Plasmodium vivax merozoite surface protein 1 in individuals exposed to malaria. Infect Immun. 1997, 65: 1606-1614.PubMedCentralPubMed Soares IS, Levitus G, Souza JM, Del Portillo HA, Rodrigues MM: Acquired immune responses to the N- and C-terminal regions of Plasmodium vivax merozoite surface protein 1 in individuals exposed to malaria. Infect Immun. 1997, 65: 1606-1614.PubMedCentralPubMed
28.
go back to reference Soares IS, da Cunha MG, Silva MN, Souza JM, Del Portillo HA, Rodrigues MM: Longevity of naturally acquired antibody responses to the N- and C-terminal regions of Plasmodium vivax merozoite surface protein 1. Am J Trop Med Hyg. 1999, 60: 357-363.PubMed Soares IS, da Cunha MG, Silva MN, Souza JM, Del Portillo HA, Rodrigues MM: Longevity of naturally acquired antibody responses to the N- and C-terminal regions of Plasmodium vivax merozoite surface protein 1. Am J Trop Med Hyg. 1999, 60: 357-363.PubMed
29.
go back to reference Levitus G, Mertens F, Speranca MA, Camargo LM, Ferreira MU, del Portillo HA: Characterization of naturally acquired human IgG responses against the N-terminal region of the merozoite surface protein 1 of Plasmodium vivax. Am J Trop Med Hyg. 1994, 51: 68-76.PubMed Levitus G, Mertens F, Speranca MA, Camargo LM, Ferreira MU, del Portillo HA: Characterization of naturally acquired human IgG responses against the N-terminal region of the merozoite surface protein 1 of Plasmodium vivax. Am J Trop Med Hyg. 1994, 51: 68-76.PubMed
30.
go back to reference Nogueira PA, Alves FP, Fernandez-Becerra C, Pein O, Santos NR, da Silva LH P, Camargo EP, del Portillo HA: A reduced risk of infection with Plasmodium vivax and clinical protection against malaria are associated with antibodies against the N terminus but not the C terminus of merozoite surface protein 1. Infect Immun. 2006, 74: 2726-2733. 10.1128/IAI.74.5.2726-2733.2006.PubMedCentralCrossRefPubMed Nogueira PA, Alves FP, Fernandez-Becerra C, Pein O, Santos NR, da Silva LH P, Camargo EP, del Portillo HA: A reduced risk of infection with Plasmodium vivax and clinical protection against malaria are associated with antibodies against the N terminus but not the C terminus of merozoite surface protein 1. Infect Immun. 2006, 74: 2726-2733. 10.1128/IAI.74.5.2726-2733.2006.PubMedCentralCrossRefPubMed
31.
go back to reference Fernandez-Becerra C, Sanz S, Brucet M, Stanisic DI, Alves FP, Camargo EP, Alonso PL, Mueller I, del Portillo HA: Naturally-acquired humoral immune responses against the N- and C-termini of the Plasmodium vivax MSP1 protein in endemic regions of Brazil and Papua New Guinea using a multiplex assay. Malar J. 2010, 9: 29-10.1186/1475-2875-9-29.PubMedCentralCrossRefPubMed Fernandez-Becerra C, Sanz S, Brucet M, Stanisic DI, Alves FP, Camargo EP, Alonso PL, Mueller I, del Portillo HA: Naturally-acquired humoral immune responses against the N- and C-termini of the Plasmodium vivax MSP1 protein in endemic regions of Brazil and Papua New Guinea using a multiplex assay. Malar J. 2010, 9: 29-10.1186/1475-2875-9-29.PubMedCentralCrossRefPubMed
32.
go back to reference Storti-Melo LM, Souza-Neiras WC, Cassiano GC, Taveira LC, Cordeiro AJ, Couto VS, Povoa MM, Cunha MG, Echeverry DM, Rossit AR, Arévalo-Herrera M, Herrera S, Machado RL: Evaluation of the naturally acquired antibody immune response to the Pv200L N-terminal fragment of Plasmodium vivax merozoite surface protein-1 in four areas of the Amazon Region of Brazil. Am J Trop Med Hyg. 2011, 84 (Suppl 2): 58-63.PubMedCentralCrossRefPubMed Storti-Melo LM, Souza-Neiras WC, Cassiano GC, Taveira LC, Cordeiro AJ, Couto VS, Povoa MM, Cunha MG, Echeverry DM, Rossit AR, Arévalo-Herrera M, Herrera S, Machado RL: Evaluation of the naturally acquired antibody immune response to the Pv200L N-terminal fragment of Plasmodium vivax merozoite surface protein-1 in four areas of the Amazon Region of Brazil. Am J Trop Med Hyg. 2011, 84 (Suppl 2): 58-63.PubMedCentralCrossRefPubMed
33.
go back to reference del Portillo HA, Levitus G, Camargo LM, Ferreira MU, Mertens F: Human IgG responses against the N-terminal region of the Merozoite Surface Protein 1 of Plasmodium vivax. Mem Inst Oswaldo Cruz. 1992, 87 (Suppl 3): 77-84.CrossRefPubMed del Portillo HA, Levitus G, Camargo LM, Ferreira MU, Mertens F: Human IgG responses against the N-terminal region of the Merozoite Surface Protein 1 of Plasmodium vivax. Mem Inst Oswaldo Cruz. 1992, 87 (Suppl 3): 77-84.CrossRefPubMed
34.
go back to reference Mertens F, Levitus G, Camargo LM, Ferreira MU, Dutra AP, Del Portillo HA: Longitudinal study of naturally acquired humoral immune responses against the merozoite surface protein 1 of Plasmodium vivax in patients from Rondonia, Brazil. Am J Trop Med Hyg. 1993, 49: 383-392.PubMed Mertens F, Levitus G, Camargo LM, Ferreira MU, Dutra AP, Del Portillo HA: Longitudinal study of naturally acquired humoral immune responses against the merozoite surface protein 1 of Plasmodium vivax in patients from Rondonia, Brazil. Am J Trop Med Hyg. 1993, 49: 383-392.PubMed
35.
go back to reference Bastos MS, da Silva-Nunes M, Malafronte RS, Hoffmann EH, Wunderlich G, Moraes SL, Ferreira MU: Antigenic polymorphism and naturally acquired antibodies to Plasmodium vivax merozoite surface protein 1 in rural Amazonians. Clin Vaccine Immunol. 2007, 14: 1249-1259. 10.1128/CVI.00243-07.PubMedCentralCrossRefPubMed Bastos MS, da Silva-Nunes M, Malafronte RS, Hoffmann EH, Wunderlich G, Moraes SL, Ferreira MU: Antigenic polymorphism and naturally acquired antibodies to Plasmodium vivax merozoite surface protein 1 in rural Amazonians. Clin Vaccine Immunol. 2007, 14: 1249-1259. 10.1128/CVI.00243-07.PubMedCentralCrossRefPubMed
36.
go back to reference Browder J, Pedlowski M, Walker R, Wynee R, Summers P, Abad A, Becerra-Cordoba N, Mil-Homens J: Revisiting theories of frontier expansion in the Brazilian Amazon: a survey of the colonist farming population in Rondonia’s post-frontier, 1992-2002. World Development. 2008, 36: 1469-1492. 10.1016/j.worlddev.2007.08.008.CrossRef Browder J, Pedlowski M, Walker R, Wynee R, Summers P, Abad A, Becerra-Cordoba N, Mil-Homens J: Revisiting theories of frontier expansion in the Brazilian Amazon: a survey of the colonist farming population in Rondonia’s post-frontier, 1992-2002. World Development. 2008, 36: 1469-1492. 10.1016/j.worlddev.2007.08.008.CrossRef
38.
go back to reference Perandin F, Manca N, Calderaro A, Piccolo G, Galati L, Ricci L, Medici MC, Arcangeletti MC, Snounou G, Dettori G, Chezzi C: Development of a real-time PCR assay for detection of Plasmodium falciparum, Plasmodium vivax, and Plasmodium ovale for routine clinical diagnosis. J Clin Microbiol. 2004, 42: 1214-1219. 10.1128/JCM.42.3.1214-1219.2004.PubMedCentralCrossRefPubMed Perandin F, Manca N, Calderaro A, Piccolo G, Galati L, Ricci L, Medici MC, Arcangeletti MC, Snounou G, Dettori G, Chezzi C: Development of a real-time PCR assay for detection of Plasmodium falciparum, Plasmodium vivax, and Plasmodium ovale for routine clinical diagnosis. J Clin Microbiol. 2004, 42: 1214-1219. 10.1128/JCM.42.3.1214-1219.2004.PubMedCentralCrossRefPubMed
39.
go back to reference Rougemont M, Van Saanen M, Sahli R, Hinrikson HP, Bille J, Jaton K: Detection of four Plasmodium species in blood from humans by 18S rRNA gene subunit-based and species-specific real-time PCR assays. J Clin Microbiol. 2004, 42: 5636-5643. 10.1128/JCM.42.12.5636-5643.2004.PubMedCentralCrossRefPubMed Rougemont M, Van Saanen M, Sahli R, Hinrikson HP, Bille J, Jaton K: Detection of four Plasmodium species in blood from humans by 18S rRNA gene subunit-based and species-specific real-time PCR assays. J Clin Microbiol. 2004, 42: 5636-5643. 10.1128/JCM.42.12.5636-5643.2004.PubMedCentralCrossRefPubMed
40.
go back to reference Galamo CD, Jafarshad A, Blanc C, Druilhe P: Anti-MSP1 block 2 antibodies are effective at parasite killing in an allele-specific manner by monocyte-mediated antibody-dependent cellular inhibition. J Infect Dis. 2009, 199: 1151-1154. 10.1086/597426.CrossRefPubMed Galamo CD, Jafarshad A, Blanc C, Druilhe P: Anti-MSP1 block 2 antibodies are effective at parasite killing in an allele-specific manner by monocyte-mediated antibody-dependent cellular inhibition. J Infect Dis. 2009, 199: 1151-1154. 10.1086/597426.CrossRefPubMed
41.
go back to reference Sarthou JL, Angel G, Aribot G, Rogier C, Dieye A, Toure Balde A, Diatta B, Seignot P, Roussilhon C: Prognostic value of anti-Plasmodium falciparum-specific immunoglobulin G3, cytokines, and their soluble receptors in West African patients with severe malaria. Infect Immun. 1997, 65: 3271-3276.PubMedCentralPubMed Sarthou JL, Angel G, Aribot G, Rogier C, Dieye A, Toure Balde A, Diatta B, Seignot P, Roussilhon C: Prognostic value of anti-Plasmodium falciparum-specific immunoglobulin G3, cytokines, and their soluble receptors in West African patients with severe malaria. Infect Immun. 1997, 65: 3271-3276.PubMedCentralPubMed
42.
go back to reference Miura K, Zhou H, Diouf A, Moretz SE, Fay MP, Miller LH, Martin LB, Pierce MA, Ellis RD, Mullen GE, Long CA: Anti-apical-membrane-antigen-1 antibody is more effective than anti-42-kilodalton-merozoite-surface-protein-1 antibody in inhibiting Plasmodium falciparum growth, as determined by the in vitro growth inhibition assay. Clin Vaccine Immunol. 2009, 16: 963-968. 10.1128/CVI.00042-09.PubMedCentralCrossRefPubMed Miura K, Zhou H, Diouf A, Moretz SE, Fay MP, Miller LH, Martin LB, Pierce MA, Ellis RD, Mullen GE, Long CA: Anti-apical-membrane-antigen-1 antibody is more effective than anti-42-kilodalton-merozoite-surface-protein-1 antibody in inhibiting Plasmodium falciparum growth, as determined by the in vitro growth inhibition assay. Clin Vaccine Immunol. 2009, 16: 963-968. 10.1128/CVI.00042-09.PubMedCentralCrossRefPubMed
43.
go back to reference Jouin H, Rogier C, Trape JF, Mercereau-Puijalon O: Fixed, epitope-specific, cytophilic antibody response to the polymorphic block 2 domain of the Plasmodium falciparum merozoite surface antigen MSP-1 in humans living in a malaria-endemic area. Eur J Immunol. 2001, 31: 539-550. 10.1002/1521-4141(200102)31:2<539::AID-IMMU539>3.0.CO;2-1.CrossRefPubMed Jouin H, Rogier C, Trape JF, Mercereau-Puijalon O: Fixed, epitope-specific, cytophilic antibody response to the polymorphic block 2 domain of the Plasmodium falciparum merozoite surface antigen MSP-1 in humans living in a malaria-endemic area. Eur J Immunol. 2001, 31: 539-550. 10.1002/1521-4141(200102)31:2<539::AID-IMMU539>3.0.CO;2-1.CrossRefPubMed
44.
go back to reference Lazarou M, Guevara Patino JA, Jennings RM, McIntosh RS, Shi J, Howell S, Cullen E, Jones T, Adame-Gallegos JR, Chappel JA, McBride JS, Blackman MJ, Holder AA, Pleass RJ: Inhibition of erythrocyte invasion and Plasmodium falciparum merozoite surface protein 1 processing by human immunoglobulin G1 (IgG1) and IgG3 antibodies. Infect Immun. 2009, 77: 5659-5667. 10.1128/IAI.00167-09.PubMedCentralCrossRefPubMed Lazarou M, Guevara Patino JA, Jennings RM, McIntosh RS, Shi J, Howell S, Cullen E, Jones T, Adame-Gallegos JR, Chappel JA, McBride JS, Blackman MJ, Holder AA, Pleass RJ: Inhibition of erythrocyte invasion and Plasmodium falciparum merozoite surface protein 1 processing by human immunoglobulin G1 (IgG1) and IgG3 antibodies. Infect Immun. 2009, 77: 5659-5667. 10.1128/IAI.00167-09.PubMedCentralCrossRefPubMed
45.
go back to reference Cavanagh DR, Dodoo D, Hviid L, Kurtzhals JA, Theander TG, Akanmori BD, Polley S, Conway DJ, Koram K, McBride JS: Antibodies to the N-terminal block 2 of Plasmodium falciparum merozoite surface protein 1 are associated with protection against clinical malaria. Infect Immun. 2004, 72: 6492-6502. 10.1128/IAI.72.11.6492-6502.2004.PubMedCentralCrossRefPubMed Cavanagh DR, Dodoo D, Hviid L, Kurtzhals JA, Theander TG, Akanmori BD, Polley S, Conway DJ, Koram K, McBride JS: Antibodies to the N-terminal block 2 of Plasmodium falciparum merozoite surface protein 1 are associated with protection against clinical malaria. Infect Immun. 2004, 72: 6492-6502. 10.1128/IAI.72.11.6492-6502.2004.PubMedCentralCrossRefPubMed
46.
go back to reference Roussilhon C, Oeuvray C, Muller-Graf C, Tall A, Rogier C, Trape JF, Theisen M, Balde A, Perignon JL, Druilhe P: Long-term clinical protection from falciparum malaria is strongly associated with IgG3 antibodies to merozoite surface protein 3. PLoS Med. 2007, 4: e320-10.1371/journal.pmed.0040320.PubMedCentralCrossRefPubMed Roussilhon C, Oeuvray C, Muller-Graf C, Tall A, Rogier C, Trape JF, Theisen M, Balde A, Perignon JL, Druilhe P: Long-term clinical protection from falciparum malaria is strongly associated with IgG3 antibodies to merozoite surface protein 3. PLoS Med. 2007, 4: e320-10.1371/journal.pmed.0040320.PubMedCentralCrossRefPubMed
47.
go back to reference Jafarshad A, Dziegiel MH, Lundquist R, Nielsen LK, Singh S, Druilhe PL: A novel antibody-dependent cellular cytotoxicity mechanism involved in defense against malaria requires costimulation of monocytes FcgammaRII and FcgammaRIII. J Immunol. 2007, 178: 3099-3106.CrossRefPubMed Jafarshad A, Dziegiel MH, Lundquist R, Nielsen LK, Singh S, Druilhe PL: A novel antibody-dependent cellular cytotoxicity mechanism involved in defense against malaria requires costimulation of monocytes FcgammaRII and FcgammaRIII. J Immunol. 2007, 178: 3099-3106.CrossRefPubMed
48.
go back to reference Druilhe P, Perignon JL: Mechanisms of defense against P. falciparum asexual blood stages in humans. Immunol Lett. 1994, 41: 115-120. 10.1016/0165-2478(94)90118-X.CrossRefPubMed Druilhe P, Perignon JL: Mechanisms of defense against P. falciparum asexual blood stages in humans. Immunol Lett. 1994, 41: 115-120. 10.1016/0165-2478(94)90118-X.CrossRefPubMed
49.
go back to reference Druilhe P, Perignon JL: A hypothesis about the chronicity of malaria infection. Parasitol Today. 1997, 13: 353-357. 10.1016/S0169-4758(97)01095-8.CrossRefPubMed Druilhe P, Perignon JL: A hypothesis about the chronicity of malaria infection. Parasitol Today. 1997, 13: 353-357. 10.1016/S0169-4758(97)01095-8.CrossRefPubMed
50.
go back to reference Woodberry T, Minigo G, Piera KA, Hanley JC, de Silva HD, Salwati E, Kenangalem E, Tjitra E, Coppel RL, Price RN, Anstey NM, Plebanski M: Antibodies to Plasmodium falciparum and Plasmodium vivax merozoite surface protein 5 in Indonesia: species-specific and cross-reactive responses. J Infect Dis. 2008, 198: 134-142. 10.1086/588711.CrossRefPubMed Woodberry T, Minigo G, Piera KA, Hanley JC, de Silva HD, Salwati E, Kenangalem E, Tjitra E, Coppel RL, Price RN, Anstey NM, Plebanski M: Antibodies to Plasmodium falciparum and Plasmodium vivax merozoite surface protein 5 in Indonesia: species-specific and cross-reactive responses. J Infect Dis. 2008, 198: 134-142. 10.1086/588711.CrossRefPubMed
51.
go back to reference McCallum FJ, Persson KE, Mugyenyi CK, Fowkes FJ, Simpson JA, Richards JS, Williams TN, Marsh K, Beeson JG: Acquisition of growth-inhibitory antibodies against blood-stage Plasmodium falciparum. PLoS One. 2008, 3: e3571-10.1371/journal.pone.0003571.PubMedCentralCrossRefPubMed McCallum FJ, Persson KE, Mugyenyi CK, Fowkes FJ, Simpson JA, Richards JS, Williams TN, Marsh K, Beeson JG: Acquisition of growth-inhibitory antibodies against blood-stage Plasmodium falciparum. PLoS One. 2008, 3: e3571-10.1371/journal.pone.0003571.PubMedCentralCrossRefPubMed
52.
go back to reference Stubbs J, Olugbile S, Saidou B, Simpore J, Corradin G, Lanzavecchia A: Strain-transcending Fc-dependent killing of Plasmodium falciparum by merozoite surface protein 2 allele-specific human antibodies. Infect Immun. 2011, 79: 1143-1152. 10.1128/IAI.01034-10.PubMedCentralCrossRefPubMed Stubbs J, Olugbile S, Saidou B, Simpore J, Corradin G, Lanzavecchia A: Strain-transcending Fc-dependent killing of Plasmodium falciparum by merozoite surface protein 2 allele-specific human antibodies. Infect Immun. 2011, 79: 1143-1152. 10.1128/IAI.01034-10.PubMedCentralCrossRefPubMed
53.
go back to reference Bouharoun-Tayoun H, Oeuvray C, Lunel F, Druilhe P: Mechanisms underlying the monocyte-mediated antibody-dependent killing of Plasmodium falciparum asexual blood stages. J Exp Med. 1995, 182: 409-418. 10.1084/jem.182.2.409.CrossRefPubMed Bouharoun-Tayoun H, Oeuvray C, Lunel F, Druilhe P: Mechanisms underlying the monocyte-mediated antibody-dependent killing of Plasmodium falciparum asexual blood stages. J Exp Med. 1995, 182: 409-418. 10.1084/jem.182.2.409.CrossRefPubMed
54.
go back to reference Akpogheneta OJ, Duah NO, Tetteh KK, Dunyo S, Lanar DE, Pinder M, Conway DJ: Duration of naturally acquired antibody responses to blood-stage Plasmodium falciparum is age dependent and antigen specific. Infect Immun. 2008, 76: 1748-1755. 10.1128/IAI.01333-07.PubMedCentralCrossRefPubMed Akpogheneta OJ, Duah NO, Tetteh KK, Dunyo S, Lanar DE, Pinder M, Conway DJ: Duration of naturally acquired antibody responses to blood-stage Plasmodium falciparum is age dependent and antigen specific. Infect Immun. 2008, 76: 1748-1755. 10.1128/IAI.01333-07.PubMedCentralCrossRefPubMed
55.
go back to reference Scopel KK, da Silva-Nunes M, Malafronte RS, Braga EM, Ferreira MU: Variant-specific antibodies to merozoite surface protein 2 and clinical expression of Plasmodium falciparum malaria in rural Amazonians. Am J Trop Med Hyg. 2007, 76: 1084-1091.PubMed Scopel KK, da Silva-Nunes M, Malafronte RS, Braga EM, Ferreira MU: Variant-specific antibodies to merozoite surface protein 2 and clinical expression of Plasmodium falciparum malaria in rural Amazonians. Am J Trop Med Hyg. 2007, 76: 1084-1091.PubMed
56.
go back to reference Cavanagh DR, Dobano C, Elhassan IM, Marsh K, Elhassan A, Hviid L, Khalil EA, Theander TG, Arnot DE, McBride JS: Differential patterns of human immunoglobulin G subclass responses to distinct regions of a single protein, the merozoite surface protein 1 of Plasmodium falciparum. Infect Immun. 2001, 69: 1207-1211. 10.1128/IAI.69.2.1207-1211.2001.PubMedCentralCrossRefPubMed Cavanagh DR, Dobano C, Elhassan IM, Marsh K, Elhassan A, Hviid L, Khalil EA, Theander TG, Arnot DE, McBride JS: Differential patterns of human immunoglobulin G subclass responses to distinct regions of a single protein, the merozoite surface protein 1 of Plasmodium falciparum. Infect Immun. 2001, 69: 1207-1211. 10.1128/IAI.69.2.1207-1211.2001.PubMedCentralCrossRefPubMed
57.
go back to reference Bueno LL, Lobo FP, Morais CG, Mourao LC, de Avila RA, Soares IS, Fontes CJ, Lacerda MV, Chavez Olortegui C, Bartholomeu DC, Fujiwara RT, Braga EM: Identification of a highly antigenic linear B cell epitope within Plasmodium vivax apical membrane antigen 1 (AMA-1). PLoS One. 2011, 6: e21289-10.1371/journal.pone.0021289.PubMedCentralCrossRefPubMed Bueno LL, Lobo FP, Morais CG, Mourao LC, de Avila RA, Soares IS, Fontes CJ, Lacerda MV, Chavez Olortegui C, Bartholomeu DC, Fujiwara RT, Braga EM: Identification of a highly antigenic linear B cell epitope within Plasmodium vivax apical membrane antigen 1 (AMA-1). PLoS One. 2011, 6: e21289-10.1371/journal.pone.0021289.PubMedCentralCrossRefPubMed
58.
go back to reference Okenu DM, Riley EM, Bickle QD, Agomo PU, Barbosa A, Daugherty JR, Lanar DE, Conway DJ: Analysis of human antibodies to erythrocyte binding antigen 175 of Plasmodium falciparum. Infect Immun. 2000, 68: 5559-5566. 10.1128/IAI.68.10.5559-5566.2000.PubMedCentralCrossRefPubMed Okenu DM, Riley EM, Bickle QD, Agomo PU, Barbosa A, Daugherty JR, Lanar DE, Conway DJ: Analysis of human antibodies to erythrocyte binding antigen 175 of Plasmodium falciparum. Infect Immun. 2000, 68: 5559-5566. 10.1128/IAI.68.10.5559-5566.2000.PubMedCentralCrossRefPubMed
Metadata
Title
High levels of IgG3 anti ICB2-5 in Plasmodium vivax-infected individuals who did not develop symptoms
Authors
Fernanda G Versiani
Maria EM Almeida
Gisely C Melo
Francivaldo OL Versiani
Patrícia P Orlandi
Luís André M Mariúba
Leidiane A Soares
Luciana P Souza
Antonio A da Silva Balieiro
Wuelton M Monteiro
Fabio TM Costa
Hernando A del Portillo
Marcus VG Lacerda
Paulo A Nogueira
Publication date
01-12-2013
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2013
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/1475-2875-12-294

Other articles of this Issue 1/2013

Malaria Journal 1/2013 Go to the issue
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 discuss last year's major advances in heart failure and cardiomyopathies.