Immunological characterization of a VIR protein family member (VIR-14) in Plasmodium vivax-infected subjects from different epidemiological regions in Africa and South America.

Plasmodium vivax is a major challenge for malaria control due to its wide geographic distribution, high frequency of submicroscopic infections, and ability to induce relapses due to the latent forms present in the liver (hypnozoites). Deepening our knowledge of parasite biology and its molecular components is key to develop new tools for malaria control and elimination. This study aims to investigate and characterize a P. vivax protein (PvVir14) for its role in parasite biology and its interactions with the immune system. We collected sera or plasma from P.vivax-infected subjects in Brazil (n = 121) and Cambodia (n = 55), and from P. falciparum-infected subjects in Mali (n = 28), to assess antibody recognition of PvVir14. Circulating antibodies against PvVir14 appeared in 61% and 34.5% of subjects from Brazil and Cambodia, respectively, versus none (0%) of the P. falciparum-infected subjects from Mali who have no exposure to P. vivax. IgG1 and IgG3 most frequently contributed to anti-PvVir14 responses. PvVir14 antibody levels correlated with those against other well-characterized sporozoite/liver (PvCSP) and blood stage (PvDBP-RII) antigens, which were recognized by 7.6% and 42% of Brazilians, respectively. Concerning the cellular immune profiling of Brazilian subjects, PvVir14 seroreactive individuals displayed significantly higher levels of circulating atypical (CD21- CD27-) B cells, raising the possibility that atypical B cells may be contribute to the PvVir14 antibody response. When analyzed at a single-cell level, the B cell receptor gene hIGHV3-23 was only seen in subjects with active P.vivax infection where it comprised 20% of V gene usage. Among T cells, CD4+ and CD8+ levels differed (lower and higher, respectively) between subjects with versus without antibodies to PvVir14, while NKT cell levels were higher in those without antibodies. Specific B cell subsets, anti-PvVir14 circulating antibodies, and NKT cell levels declined after treatment of P. vivax. This study provides the immunological characterization of PvVir14, a unique P. vivax protein, and possible association with acute host's immune responses, providing new information of specific host-parasite interaction. Trial registration: TrialClinicalTrials.gov Identifier: NCT00663546 & ClinicalTrials.gov NCT02334462.

[1]  R. Fujiwara,et al.  Proteomic Analysis of Urine from Patients with Plasmodium vivax Malaria Unravels a Unique Plasmodium vivax Protein That Is Absent from Plasmodium falciparum , 2022, Tropical medicine and infectious disease.

[2]  Abhinav Sinha,et al.  Plasmodium vivax Duffy Binding Protein-Based Vaccine: a Distant Dream , 2022, Frontiers in Cellular and Infection Microbiology.

[3]  R. Price,et al.  High-dimensional mass cytometry identifies T cell and B cell signatures predicting reduced risk of Plasmodium vivax malaria , 2021, JCI insight.

[4]  A. Madi,et al.  Shared transcriptional profiles of atypical B cells suggest common drivers of expansion and function in malaria, HIV, and autoimmunity , 2021, Science Advances.

[5]  N. Tolia,et al.  A human monoclonal antibody blocks malaria transmission and defines a highly conserved neutralizing epitope on gametes , 2021, Nature Communications.

[6]  Peter D. Crompton,et al.  Plasmodium falciparum–specific IgM B cells dominate in children, expand with malaria, and produce functional IgM , 2021, The Journal of experimental medicine.

[7]  T. Housen,et al.  Malaria in Cambodia: A Retrospective Analysis of a Changing Epidemiology 2006–2019 , 2021, International journal of environmental research and public health.

[8]  Andrea A. Berry,et al.  Atypical B cells are part of an alternative lineage of B cells that participates in responses to vaccination and infection in humans , 2021, Cell reports.

[9]  J. Adams,et al.  Progress towards the development of a P. vivax vaccine , 2021, Expert review of vaccines.

[10]  A. Knudsen,et al.  Acquisition and decay of IgM and IgG responses to merozoite antigens after Plasmodium falciparum malaria in Ghanaian children , 2020, PloS one.

[11]  C. Abeijon,et al.  Urine-Based Antigen (Protein) Detection Test for the Diagnosis of Visceral Leishmaniasis , 2020, Microorganisms.

[12]  E. Bunnik,et al.  Potential functions of atypical memory B cells in Plasmodium-exposed individuals , 2020, International journal for parasitology.

[13]  P. Duffy,et al.  Malaria vaccines since 2000: progress, priorities, products , 2020, npj Vaccines.

[14]  K. Battle,et al.  Plasmodium vivax in the Era of the Shrinking P. falciparum Map , 2020, Trends in parasitology.

[15]  Peter D. Crompton,et al.  PD-1 Expression on NK Cells in Malaria-Exposed Individuals Is Associated with Diminished Natural Cytotoxicity and Enhanced Antibody-Dependent Cellular Cytotoxicity , 2020, Infection and Immunity.

[16]  R. Sauerwein,et al.  Activatory Receptor NKp30 Predicts NK Cell Activation During Controlled Human Malaria Infection , 2019, Front. Immunol..

[17]  Danny W. Wilson,et al.  Induction and kinetics of complement-fixing antibodies against Plasmodium vivax MSP3α and relationship with IgG subclasses and IgM. , 2019, The Journal of infectious diseases.

[18]  N. Tolia,et al.  Naturally Acquired Antibody Response to Malaria Transmission Blocking Vaccine Candidate Pvs230 Domain 1 , 2019, Front. Immunol..

[19]  I. Soares,et al.  Apical membrane protein 1‐specific antibody profile and temporal changes in peripheral blood B‐cell populations in Plasmodium vivax malaria , 2019, Parasite immunology.

[20]  J. McCarthy,et al.  IgM in human immunity to Plasmodium falciparum malaria , 2019, Science Advances.

[21]  S. P. Kurup,et al.  T cell-mediated immunity to malaria , 2019, Nature Reviews Immunology.

[22]  P. Christe,et al.  Sex-biased parasitism in vector-borne disease: Vector preference? , 2019, PloS one.

[23]  C. Sundling,et al.  B cell profiling in malaria reveals expansion and remodelling of CD11c+ B cell subsets. , 2019, JCI insight.

[24]  N. Tolia,et al.  Structural basis for neutralization of Plasmodium vivax by naturally acquired human antibodies that target , 2019 .

[25]  Virander S. Chauhan,et al.  Differential Patterns of IgG Subclass Responses to Plasmodium falciparum Antigens in Relation to Malaria Protection and RTS,S Vaccination , 2019, Front. Immunol..

[26]  A. Dondorp,et al.  Malaria: What's New in the Management of Malaria? , 2019, Infectious disease clinics of North America.

[27]  Danny W. Wilson,et al.  Targets of complement-fixing antibodies in protective immunity against malaria in children , 2019, Nature Communications.

[28]  I. Soares,et al.  To B or Not to B: Understanding B Cell Responses in the Development of Malaria Infection , 2018, Front. Immunol..

[29]  B. M. Sanchez,et al.  Blood-stage Plasmodium vivax antibody dynamics in a low transmission setting: A nine year follow-up study in the Amazon region , 2018, PloS one.

[30]  N. Gogtay,et al.  Vivax infection alters peripheral B‐cell profile and induces persistent serum IgM , 2018, Parasite immunology.

[31]  M. White,et al.  Age, exposure and immunity , 2018, eLife.

[32]  Chao Yang,et al.  Natural Killer Cells: Development, Maturation, and Clinical Utilization , 2018, Front. Immunol..

[33]  E. Ashley,et al.  Malaria , 2018, The Lancet.

[34]  A. Haque,et al.  Recent Insights into CD4+ Th Cell Differentiation in Malaria , 2018, The Journal of Immunology.

[35]  D. Gowda,et al.  Epidemiology, drug resistance, and pathophysiology of Plasmodium vivax malaria , 2018, Journal of vector borne diseases.

[36]  P. Siba,et al.  Naturally acquired antibody responses to more than 300 Plasmodium vivax proteins in three geographic regions , 2017, PLoS neglected tropical diseases.

[37]  C. Menéndez,et al.  Chronic Exposure to Malaria Is Associated with Inhibitory and Activation Markers on Atypical Memory B Cells and Marginal Zone-Like B Cells , 2017, Front. Immunol..

[38]  W. Monteiro,et al.  Malaria in Brazil, Colombia, Peru and Venezuela: current challenges in malaria control and elimination , 2017, Malaria Journal.

[39]  M. Rhee,et al.  Diversity of vir Genes in Plasmodium vivax from Endemic Regions in the Republic of Korea: an Initial Evaluation , 2017, The Korean journal of parasitology.

[40]  E. Riley,et al.  NK Cells: Uncertain Allies against Malaria , 2017, Front. Immunol..

[41]  D. Díaz-Arévalo,et al.  What Is Known about the Immune Response Induced by Plasmodium vivax Malaria Vaccine Candidates? , 2017, Front. Immunol..

[42]  J. Rayner,et al.  Plasmodium vivax vaccine research - we've only just begun. , 2017, International journal for parasitology.

[43]  David L. Smith,et al.  Global Epidemiology of Plasmodium vivax , 2016, The American journal of tropical medicine and hygiene.

[44]  J. McCarthy,et al.  The Impact of Established Immunoregulatory Networks on Vaccine Efficacy and the Development of Immunity to Malaria , 2016, The Journal of Immunology.

[45]  C. Menéndez,et al.  Plasmodium vivax VIR Proteins Are Targets of Naturally-Acquired Antibody and T Cell Immune Responses to Malaria in Pregnant Women , 2016, PLoS neglected tropical diseases.

[46]  Hao Chen,et al.  Cytofkit: A Bioconductor Package for an Integrated Mass Cytometry Data Analysis Pipeline , 2016, PLoS Comput. Biol..

[47]  Peter D. Crompton,et al.  Somatically Hypermutated Plasmodium-Specific IgM+ Memory B Cells Are Rapid, Plastic, Early Responders upon Malaria Rechallenge , 2016, Immunity.

[48]  X. Ambroggio,et al.  Structural and Immunological Characterization of Recombinant 6-Cysteine Domains of the Plasmodium falciparum Sexual Stage Protein Pfs230* , 2016, The Journal of Biological Chemistry.

[49]  D. Horn,et al.  Epigenetic Regulation of Virulence Gene Expression in Parasitic Protozoa , 2016, Cell host & microbe.

[50]  Peter D. Crompton,et al.  Malaria-associated atypical memory B cells exhibit markedly reduced B cell receptor signaling and effector function , 2015, eLife.

[51]  D. Bartholomeu,et al.  Phenotypic profiling of CD8+ T cells during Plasmodium vivax blood-stage infection , 2015, BMC Infectious Diseases.

[52]  D. Bartholomeu,et al.  CD4+ T cells apoptosis in Plasmodium vivax infection is mediated by activation of both intrinsic and extrinsic pathways , 2015, Malaria Journal.

[53]  N. White,et al.  Severe vivax malaria: a systematic review and meta-analysis of clinical studies since 1900 , 2014, Malaria Journal.

[54]  C. Menéndez,et al.  Pregnancy and Malaria Exposure Are Associated with Changes in the B Cell Pool and in Plasma Eotaxin Levels , 2014, The Journal of Immunology.

[55]  N. Tolia,et al.  Red Blood Cell Invasion by Plasmodium vivax: Structural Basis for DBP Engagement of DARC , 2014, PLoS pathogens.

[56]  V. A. Stewart,et al.  Immune mechanisms in malaria: new insights in vaccine development , 2013, Nature Medicine.

[57]  J. Langhorne,et al.  T cell control of malaria pathogenesis. , 2012, Current opinion in immunology.

[58]  J. Waitumbi,et al.  B-cell activity in children with malaria , 2012, Malaria Journal.

[59]  H. D. del Portillo,et al.  On the cytoadhesion of Plasmodium vivax-infected erythrocytes. , 2010, The Journal of infectious diseases.

[60]  S. Hoffman,et al.  Acquired Antibody Responses against Plasmodium vivax Infection Vary with Host Genotype for Duffy Antigen Receptor for Chemokines (DARC) , 2010, PloS one.

[61]  B. Andrade,et al.  Severe Plasmodium vivax malaria exhibits marked inflammatory imbalance , 2010, Malaria Journal.

[62]  A. Jin,et al.  Structure of the Plasmodium falciparum Circumsporozoite Protein, a Leading Malaria Vaccine Candidate* , 2009, The Journal of Biological Chemistry.

[63]  Hagai Ginsburg,et al.  The transcriptome of Plasmodium vivax reveals divergence and diversity of transcriptional regulation in malaria parasites , 2008, Proceedings of the National Academy of Sciences.

[64]  Jonathan Crabtree,et al.  Comparative genomics of the neglected human malaria parasite Plasmodium vivax , 2008, Nature.

[65]  Charles C. Kim,et al.  Experimental Malaria Infection Triggers Early Expansion of Natural Killer Cells , 2008, Infection and Immunity.

[66]  D. Conway,et al.  Duration of Naturally Acquired Antibody Responses to Blood-Stage Plasmodium falciparum Is Age Dependent and Antigen Specific , 2008, Infection and Immunity.

[67]  G. Teng,et al.  Immunoglobulin somatic hypermutation. , 2007, Annual review of genetics.

[68]  H. D. del Portillo,et al.  Evaluation of the acquired immune responses to Plasmodium vivax VIR variant antigens in individuals living in malaria-endemic areas of Brazil , 2006, Malaria Journal.

[69]  E. Riley,et al.  Heterogeneous Human NK Cell Responses to Plasmodium falciparum-Infected Erythrocytes1 , 2005, The Journal of Immunology.

[70]  M. Theisen,et al.  Association between Protection against Clinical Malaria and Antibodies to Merozoite Surface Antigens in an Area of Hyperendemicity in Myanmar: Complementarity between Responses to Merozoite Surface Protein 3 and the 220-Kilodalton Glutamate-Rich Protein , 2004, Infection and Immunity.

[71]  M. Takiguchi,et al.  Differentiation of Human CD8+ T Cells from a Memory to Memory/Effector Phenotype1 , 2002, The Journal of Immunology.

[72]  T. Schumacher,et al.  CD27 is required for generation and long-term maintenance of T cell immunity , 2000, Nature Immunology.

[73]  Saul Tzipori,et al.  Biology of , 2021, Evolutionary Biology of Carabus Ground Beetles.