Abstract
A direct role for IgA either for elimination of malaria parasite or for improvement in tissue pathology has not been investigated in case of Malaria infection while IgG, IgE and IgM were all implicated in the adverse pathology. In this communication, we delineate further that Malaria specific IgA appears to be significant among individuals who had multiple episodes of infection. Interestingly, the IgA elicited by immunization of the homologous peptides derived from Plasmodium berghei ANKA have also resulted in protection of host from adverse lung pathology, while the parasite load is unaffected. The PfrVI immunized mice and mice infected with repeated cycles of ‘infection and recovery’, simulating an endemic like situation, have resulted in development of B cell population that secretes the IgA specific to this region VI. Summarily, our results suggest that the IgA specific to the malarial antigen can confer significant advantage to hosts in protecting the overall tissue pathology.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Barry A, Hansen D (2016) Naturally acquired immunity to malaria. Parasitology 143:125–128. https://doi.org/10.1017/S0031182015001778
Ahmed Ismail H, Tijani MK, Langer C, Reiling L, White MT, Beeson JG, Wahlgren M, Nwuba R, Persson KEM (2014) Subclass responses and their half-lives for antibodies against EBA175 and PfRh2 in naturally acquired immunity against Plasmodium falciparum malaria. Malar J 13:425. https://doi.org/10.1186/1475-2875-13-425
Villasis E, Lopez-Perez M, Torres K, Gamboa D, Neyra V, Bendezu J, Tricoche N, Lobo C, Vinetz JM, Lustigman S (2012) Anti-Plasmodium falciparum invasion ligand antibodies in a low malaria transmission region, Loreto, Peru. Malar J 11:361. https://doi.org/10.1186/1475-2875-11-361
Richards JS, Stanisic DI, Fowkes FJI, Tavul L, Dabod E, Thompson JK, Kumar S, Chitnis CE, Narum DL, Michon P, Siba PM, Cowman AF, Mueller I, Beeson JG (2010) Association between naturally acquired antibodies to erythrocyte-binding antigens of Plasmodium falciparum and protection from malaria and high-density parasitemia. Clin Infect Dis 51:e50–e60. https://doi.org/10.1086/656413
Monteiro RC (2014) Immunoglobulin A as an anti-inflammatory agent. Clin Exp Immunol 178:108–110. https://doi.org/10.1111/cei.12531
Motegi Y, Kita H, Kato M, Morikawa A (2000) Role of secretory IgA, secretory component, and eosinophils in mucosal inflammation. Int Arch Allergy Immunol 122:25–27. https://doi.org/10.1159/000053627
Nikolova EB, Tomana M, Russell MW (1994) All forms of human IgA antibodies bound to antigen interfere with complement (C3) fixation induced by IgG or by antigen alone. Scand J Immunol 39:275–280. https://doi.org/10.1111/j.1365-3083.1994.tb03371.x
Chen E, Paing MM, Salinas N, Sim BK, Tolia NH (2013) Structural and functional basis for inhibition of erythrocyte invasion by antibodies that target Plasmodium falciparum EBA-175. PLoS Pathog 9:e1003390. https://doi.org/10.1371/journal.ppat.1003390
Sakura T, Yahata K, Kaneko O (2013) The upstream sequence segment of the C-terminal cysteine-rich domain is required for microneme trafficking of Plasmodium falciparum erythrocyte binding antigen 175. Parasitol Int 62:157–164. https://doi.org/10.1016/j.parint.2012.12.002
Kumar A, Deore S, Kumar S, Bankar T, Lotke A, Parab P, Krishnasastry M (2015) Kix domain specific immunoglobulin A can protect from adverse lung and cerebral pathology induced by Plasmodium berghei ANKA. Biochem Biophys Res Commun 464:943–948. https://doi.org/10.1016/j.bbrc.2015.07.075
Bao LQ, Huy NT, Kikuchi M, Yanagi T, Senba M, Shuaibu MN, Honma K, Yui K, Hirayama K (2013) CD19(+) B cells confer protection against experimental cerebral malaria in semi-immune rodent model. PLoS ONE 8:e64836. https://doi.org/10.1371/journal.pone.0064836
Frey A, Di Canzio J, Zurakowski D (1998) A statistically defined endpoint titer determination method for immunoassays. J Immunol Methods 221:35–41
Ndungu FM, Bull PC, Ross A, Lowe BS, Kabiru E, Marsh K (2002) Naturally acquired immunoglobulin (Ig)G subclass antibodies to crude asexual Plasmodium falciparum lysates: evidence for association with protection for IgG1 and disease for IgG2. Parasite Immunol 24:77–82
Biswas S, Saxena QB, Roy A, Kabilan L (1995) Naturally occurring plasmodium-specific IgA antibody in humans from a malaria endemic area. J Biosci 20:453–460. https://doi.org/10.1007/BF02703849
Healer J, Thompson JK, Riglar DT, Wilson DW, Chiu YHC, Miura K, Chen L, Hodder AN, Long CA, Hansen DS, Baum J, Cowman AF (2013) Vaccination with conserved regions of erythrocyte-binding antigens induces neutralizing antibodies against multiple strains of Plasmodium falciparum. PLoS ONE 8:e72504. https://doi.org/10.1371/journal.pone.0072504
Pleass RJ, Holder AA (2005) Opinion: antibody-based therapies for malaria. Nat Rev Microbiol 3:893–899. https://doi.org/10.1038/nrmicro1267
Guevara Patiño JA, Holder AA, McBride JS, Blackman MJ (1997) Antibodies that inhibit malaria merozoite surface protein-1 processing and erythrocyte invasion are blocked by naturally acquired human antibodies. J Exp Med 186:1689–1699
Aitken EH, Negri EM, Barboza R, Lima MR, Álvarez JM, Marinho CR, Caldini EG, Epiphanio S (2014) Ultrastructure of the lung in a murine model of malaria-associated acute lung injury/acute respiratory distress syndrome. Malar J 13:230. https://doi.org/10.1186/1475-2875-13-230
Prakash D, Fesel C, Jain R, Cazenave P-A, Mishra GC, Pied S (2006) Clusters of cytokines determine malaria severity in Plasmodium falciparum-infected patients from endemic areas of Central India. J Infect Dis 194:198–207. https://doi.org/10.1086/504720
Omer FM, Kurtzhals JAL, Riley EM (2000) Maintaining the immunological balance in parasitic infections: a role for TGF-β? Parasitol Today 16:18–23. https://doi.org/10.1016/S0169-4758(99)01562-8
Seo G, Jang Y, Kim H-A, Lee M-R, Park M-H, Park S, Lee J, Choe J, Kim P (2013) Retinoic acid, acting as a highly specific IgA isotype switch factor, cooperates with TGF-β1 to enhance the overall IgA response. J Leukoc Biol 94:325–335. https://doi.org/10.1189/jlb.0313128
Stavnezer J, Kang J (2009) The surprising discovery that TGF beta specifically induces the IgA class switch. J Immunol 182:5–7. https://doi.org/10.4049/jimmunol.182.1.5
Duraisingh MT, Maier AG, Triglia T, Cowman AF (2003) Erythrocyte-binding antigen 175 mediates invasion in Plasmodium falciparum utilizing sialic acid-dependent and -independent pathways. Proc Natl Acad Sci USA 100:4796–4801. https://doi.org/10.1073/pnas.0730883100
Kassim OO, Ako-Anai KA, Torimiro SE, Hollowell GP, Okoye VC, Martin SK (2000) Inhibitory factors in breastmilk, maternal and infant sera against in vitro growth of Plasmodium falciparum malaria parasite. J Trop Pediatr 46:92–96
Acknowledgements
The authors thank Dr. Shekhar Mande for institutional assistance, Dr. Prakash Deshpande for providing us the endemic human sera samples. Financial assistance for the work is provided by Department of Biotechnology, Government of India (Grant No. BT/PR5492/MED/14/641/2004) through an intramural research of National Center for Cell Science, Pune, India. SD is an SRF of UGC India., AK SK and EM are recipients of SRF from CSIR, India.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Deore, S., Kumar, A., Kumar, S. et al. Erythrocyte binding ligand region VI specific IgA confers tissue protection in malaria infection. Mol Biol Rep 46, 3801–3808 (2019). https://doi.org/10.1007/s11033-019-04822-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11033-019-04822-7