Balancing selection and high genetic diversity of Plasmodium vivax circumsporozoite central region in parasites from Brazilian Amazon and Rio de Janeiro Atlantic Forest

Circumsporozoite protein (CSP) is the primary pre-erythrocytic vaccine target in Plasmodium species. Knowledge about their genetic diversity can help predict vaccine efficacy and the spread of novel parasite variants. Thus, we investigated pvcsp gene polymorphisms in 219 isolates (136 from Brazilian...

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Veröffentlicht in:PloS one 2020-11, Vol.15 (11), p.e0241426
Hauptverfasser: Almeida-de-Oliveira, Natália Ketrin, Abreu-Fernandes, Rebecca de, Lima-Cury, Lidiane, Lavigne, Aline Rosa de, Pina-Costa, Anielle de, Perce-da-Silva, Daiana de Souza, Catanho, Marcos, Rossi, Atila Duque, Brasil, Patrícia, Daniel-Ribeiro, Cláudio Tadeu, Ferreira-da-Cruz, Maria de Fátima
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container_issue 11
container_start_page e0241426
container_title PloS one
container_volume 15
creator Almeida-de-Oliveira, Natália Ketrin
Abreu-Fernandes, Rebecca de
Lima-Cury, Lidiane
Lavigne, Aline Rosa de
Pina-Costa, Anielle de
Perce-da-Silva, Daiana de Souza
Catanho, Marcos
Rossi, Atila Duque
Brasil, Patrícia
Daniel-Ribeiro, Cláudio Tadeu
Ferreira-da-Cruz, Maria de Fátima
description Circumsporozoite protein (CSP) is the primary pre-erythrocytic vaccine target in Plasmodium species. Knowledge about their genetic diversity can help predict vaccine efficacy and the spread of novel parasite variants. Thus, we investigated pvcsp gene polymorphisms in 219 isolates (136 from Brazilian Amazon [BA], 71 from Rio de Janeiro Atlantic Forest [AF], and 12 from non-Brazilian countries [NB]). Forty-eight polymorphic sites were detected, 46 in the central repeat region (CR), and two in the C-terminal region. Also, the CR presents InDels and a variable number of repeats. All samples correspond to the VK210 variant, and 24 VK210 subtypes based on CR. Nucleotide diversity (π = 0.0135) generated a significant number of haplotypes (168) with low genetic differentiation between the Brazilian regions (Fst = 0.208). The haplotype network revealed similar distances among the BA and AF regions. The linkage disequilibrium indicates that recombination does not seem to be acting in diversity, reinforcing natural selection's role in accelerating adaptive evolution. The high diversity (low Fst) and polymorphism frequencies could be indicators of balancing selection. Although malaria in BA and AF have distinct vector species and different host immune pressures, consistent genetic signature was found in two regions. The immunodominant B-cell epitope mapped in the CR varies from seven to 19 repeats. The CR T-cell epitope is conserved only in 39 samples. Concerning to C-terminal region, the Th2R epitope presented nonsynonymous SNP only in 6% of Brazilian samples, and the Th3R epitope remained conserved in all studied regions. We conclude that, although the uneven distribution of alleles may jeopardize the deployment of vaccines directed to a specific variable locus, a unique vaccine formulation could protect populations in all Brazilian regions.
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Knowledge about their genetic diversity can help predict vaccine efficacy and the spread of novel parasite variants. Thus, we investigated pvcsp gene polymorphisms in 219 isolates (136 from Brazilian Amazon [BA], 71 from Rio de Janeiro Atlantic Forest [AF], and 12 from non-Brazilian countries [NB]). Forty-eight polymorphic sites were detected, 46 in the central repeat region (CR), and two in the C-terminal region. Also, the CR presents InDels and a variable number of repeats. All samples correspond to the VK210 variant, and 24 VK210 subtypes based on CR. Nucleotide diversity (π = 0.0135) generated a significant number of haplotypes (168) with low genetic differentiation between the Brazilian regions (Fst = 0.208). The haplotype network revealed similar distances among the BA and AF regions. The linkage disequilibrium indicates that recombination does not seem to be acting in diversity, reinforcing natural selection's role in accelerating adaptive evolution. The high diversity (low Fst) and polymorphism frequencies could be indicators of balancing selection. Although malaria in BA and AF have distinct vector species and different host immune pressures, consistent genetic signature was found in two regions. The immunodominant B-cell epitope mapped in the CR varies from seven to 19 repeats. The CR T-cell epitope is conserved only in 39 samples. Concerning to C-terminal region, the Th2R epitope presented nonsynonymous SNP only in 6% of Brazilian samples, and the Th3R epitope remained conserved in all studied regions. We conclude that, although the uneven distribution of alleles may jeopardize the deployment of vaccines directed to a specific variable locus, a unique vaccine formulation could protect populations in all Brazilian regions.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0241426</identifier><identifier>PMID: 33166298</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Amino Acid Sequence ; Amino Acid Substitution ; Animals ; Atlantic Ocean ; Balancing ; Biology and Life Sciences ; Brazil ; Circumsporozoite protein ; Codon - genetics ; Epitopes ; Epitopes, B-Lymphocyte - chemistry ; Epitopes, B-Lymphocyte - genetics ; Epitopes, T-Lymphocyte - chemistry ; Epitopes, T-Lymphocyte - genetics ; Evolution ; Gene polymorphism ; Genetic aspects ; Genetic diversity ; Genetic polymorphisms ; Genetic Variation ; Geography ; Haplotypes ; Haplotypes - genetics ; Health aspects ; INDEL Mutation - genetics ; Infections ; Laboratories ; Linkage disequilibrium ; Linkage Disequilibrium - genetics ; Lymphocytes B ; Lymphocytes T ; Malaria ; Medicine and Health Sciences ; Microbiological research ; Monkeys &amp; apes ; Mosquitoes ; Natural selection ; Nucleotides ; Nucleotides - genetics ; Parasites ; Parasites - genetics ; People and places ; Peptides - chemistry ; Phylogeny ; Plasmodium (Protozoa) ; Plasmodium vivax - genetics ; Plasmodium vivax - isolation &amp; purification ; Polymorphism ; Polymorphism, Genetic ; Protozoan Proteins - chemistry ; Protozoan Proteins - genetics ; Recombination ; Research and Analysis Methods ; Selection, Genetic ; Single-nucleotide polymorphism ; Vaccine efficacy ; Vaccines ; Vector-borne diseases ; Virulence (Microbiology) ; Zoonoses</subject><ispartof>PloS one, 2020-11, Vol.15 (11), p.e0241426</ispartof><rights>COPYRIGHT 2020 Public Library of Science</rights><rights>2020 Almeida-de-Oliveira et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. 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Knowledge about their genetic diversity can help predict vaccine efficacy and the spread of novel parasite variants. Thus, we investigated pvcsp gene polymorphisms in 219 isolates (136 from Brazilian Amazon [BA], 71 from Rio de Janeiro Atlantic Forest [AF], and 12 from non-Brazilian countries [NB]). Forty-eight polymorphic sites were detected, 46 in the central repeat region (CR), and two in the C-terminal region. Also, the CR presents InDels and a variable number of repeats. All samples correspond to the VK210 variant, and 24 VK210 subtypes based on CR. Nucleotide diversity (π = 0.0135) generated a significant number of haplotypes (168) with low genetic differentiation between the Brazilian regions (Fst = 0.208). The haplotype network revealed similar distances among the BA and AF regions. The linkage disequilibrium indicates that recombination does not seem to be acting in diversity, reinforcing natural selection's role in accelerating adaptive evolution. The high diversity (low Fst) and polymorphism frequencies could be indicators of balancing selection. Although malaria in BA and AF have distinct vector species and different host immune pressures, consistent genetic signature was found in two regions. The immunodominant B-cell epitope mapped in the CR varies from seven to 19 repeats. The CR T-cell epitope is conserved only in 39 samples. Concerning to C-terminal region, the Th2R epitope presented nonsynonymous SNP only in 6% of Brazilian samples, and the Th3R epitope remained conserved in all studied regions. We conclude that, although the uneven distribution of alleles may jeopardize the deployment of vaccines directed to a specific variable locus, a unique vaccine formulation could protect populations in all Brazilian regions.</description><subject>Amino Acid Sequence</subject><subject>Amino Acid Substitution</subject><subject>Animals</subject><subject>Atlantic Ocean</subject><subject>Balancing</subject><subject>Biology and Life Sciences</subject><subject>Brazil</subject><subject>Circumsporozoite protein</subject><subject>Codon - genetics</subject><subject>Epitopes</subject><subject>Epitopes, B-Lymphocyte - chemistry</subject><subject>Epitopes, B-Lymphocyte - genetics</subject><subject>Epitopes, T-Lymphocyte - chemistry</subject><subject>Epitopes, T-Lymphocyte - genetics</subject><subject>Evolution</subject><subject>Gene polymorphism</subject><subject>Genetic aspects</subject><subject>Genetic diversity</subject><subject>Genetic polymorphisms</subject><subject>Genetic Variation</subject><subject>Geography</subject><subject>Haplotypes</subject><subject>Haplotypes - genetics</subject><subject>Health aspects</subject><subject>INDEL Mutation - genetics</subject><subject>Infections</subject><subject>Laboratories</subject><subject>Linkage disequilibrium</subject><subject>Linkage Disequilibrium - genetics</subject><subject>Lymphocytes B</subject><subject>Lymphocytes T</subject><subject>Malaria</subject><subject>Medicine and Health Sciences</subject><subject>Microbiological research</subject><subject>Monkeys &amp; apes</subject><subject>Mosquitoes</subject><subject>Natural selection</subject><subject>Nucleotides</subject><subject>Nucleotides - genetics</subject><subject>Parasites</subject><subject>Parasites - genetics</subject><subject>People and places</subject><subject>Peptides - chemistry</subject><subject>Phylogeny</subject><subject>Plasmodium (Protozoa)</subject><subject>Plasmodium vivax - genetics</subject><subject>Plasmodium vivax - isolation &amp; purification</subject><subject>Polymorphism</subject><subject>Polymorphism, Genetic</subject><subject>Protozoan Proteins - chemistry</subject><subject>Protozoan Proteins - genetics</subject><subject>Recombination</subject><subject>Research and Analysis Methods</subject><subject>Selection, Genetic</subject><subject>Single-nucleotide polymorphism</subject><subject>Vaccine efficacy</subject><subject>Vaccines</subject><subject>Vector-borne diseases</subject><subject>Virulence (Microbiology)</subject><subject>Zoonoses</subject><issn>1932-6203</issn><issn>1932-6203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>BENPR</sourceid><sourceid>DOA</sourceid><recordid>eNqNk11rFDEUhgdRbK3-A9GAIHixa77m66awLVZXCpX6cRvOZJLZLDPJmswsbX-RP9OsOy07oCBzkUnyvO85vOQkyUuC54Tl5P3aDd5CO984q-aYcsJp9ig5JiWjs4xi9vjg_yh5FsIa45QVWfY0OWKMZBkti-Pk1xm0YKWxDQqqVbI3ziKwNVqZZoUaZVVvJKrNVvlg-lvkNPrSQuhcbYYObc0WbpA0Xg5d2Djv7pzpFZLK9h5a5FWzszMWbcBD1KuAtHcdOvNwZ1oDFi06uBsrXhuHaoU-g1XGO7ToY2O74hfOq9A_T55oaIN6Ma4nyfeLD9_OP80urz4uzxeXM5mVtJ_lGstcgWa4VITHTa0ZK4tCFwRjWXGFU6005VBxzGnFGS1pStMKNKQlpYSdJK_3vpvWBTGGHATlaVHyMgYaieWeqB2sxcabDvytcGDEnwPnGwE-Nt4qUZckL2SudcGA60JVGOdVJUnFcMxfptHrdKw2VJ2qx-AmptMba1aicVuRZ7HrnEWDN6OBdz-HmNM_Wh6pBmJXxmoXzWRnghSLjBMcY6BFpOZ_oeJXq87I-My0iecTwbuJIDK9uukbGEIQy6_X_89e_Ziybw_YlYK2XwXXDrvHGaYg34PSuxC80g_JESx2U3KfhthNiRinJMpeHab-ILofC_YbyXIQlA</recordid><startdate>20201109</startdate><enddate>20201109</enddate><creator>Almeida-de-Oliveira, Natália Ketrin</creator><creator>Abreu-Fernandes, Rebecca de</creator><creator>Lima-Cury, Lidiane</creator><creator>Lavigne, Aline Rosa de</creator><creator>Pina-Costa, Anielle de</creator><creator>Perce-da-Silva, Daiana de Souza</creator><creator>Catanho, Marcos</creator><creator>Rossi, Atila Duque</creator><creator>Brasil, Patrícia</creator><creator>Daniel-Ribeiro, Cláudio Tadeu</creator><creator>Ferreira-da-Cruz, Maria de Fátima</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>IOV</scope><scope>ISR</scope><scope>3V.</scope><scope>7QG</scope><scope>7QL</scope><scope>7QO</scope><scope>7RV</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TG</scope><scope>7TM</scope><scope>7U9</scope><scope>7X2</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8AO</scope><scope>8C1</scope><scope>8FD</scope><scope>8FE</scope><scope>8FG</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABJCF</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>ARAPS</scope><scope>ATCPS</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BGLVJ</scope><scope>BHPHI</scope><scope>C1K</scope><scope>CCPQU</scope><scope>D1I</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>H94</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB.</scope><scope>KB0</scope><scope>KL.</scope><scope>L6V</scope><scope>LK8</scope><scope>M0K</scope><scope>M0S</scope><scope>M1P</scope><scope>M7N</scope><scope>M7P</scope><scope>M7S</scope><scope>NAPCQ</scope><scope>P5Z</scope><scope>P62</scope><scope>P64</scope><scope>PATMY</scope><scope>PDBOC</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PTHSS</scope><scope>PYCSY</scope><scope>RC3</scope><scope>5PM</scope><scope>DOA</scope><orcidid>https://orcid.org/0000-0001-6235-8807</orcidid><orcidid>https://orcid.org/0000-0003-3522-3792</orcidid></search><sort><creationdate>20201109</creationdate><title>Balancing selection and high genetic diversity of Plasmodium vivax circumsporozoite central region in parasites from Brazilian Amazon and Rio de Janeiro Atlantic Forest</title><author>Almeida-de-Oliveira, Natália Ketrin ; Abreu-Fernandes, Rebecca de ; Lima-Cury, Lidiane ; Lavigne, Aline Rosa de ; Pina-Costa, Anielle de ; Perce-da-Silva, Daiana de Souza ; Catanho, Marcos ; Rossi, Atila Duque ; Brasil, Patrícia ; Daniel-Ribeiro, Cláudio Tadeu ; Ferreira-da-Cruz, Maria de Fátima</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c692t-7f0c7eaf309e14f0cdf33988f8100cb4e05fef24ab4042b43292525bafa592213</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>Amino Acid Sequence</topic><topic>Amino Acid Substitution</topic><topic>Animals</topic><topic>Atlantic Ocean</topic><topic>Balancing</topic><topic>Biology and Life Sciences</topic><topic>Brazil</topic><topic>Circumsporozoite protein</topic><topic>Codon - genetics</topic><topic>Epitopes</topic><topic>Epitopes, B-Lymphocyte - chemistry</topic><topic>Epitopes, B-Lymphocyte - genetics</topic><topic>Epitopes, T-Lymphocyte - chemistry</topic><topic>Epitopes, T-Lymphocyte - genetics</topic><topic>Evolution</topic><topic>Gene polymorphism</topic><topic>Genetic aspects</topic><topic>Genetic diversity</topic><topic>Genetic polymorphisms</topic><topic>Genetic Variation</topic><topic>Geography</topic><topic>Haplotypes</topic><topic>Haplotypes - genetics</topic><topic>Health aspects</topic><topic>INDEL Mutation - genetics</topic><topic>Infections</topic><topic>Laboratories</topic><topic>Linkage disequilibrium</topic><topic>Linkage Disequilibrium - genetics</topic><topic>Lymphocytes B</topic><topic>Lymphocytes T</topic><topic>Malaria</topic><topic>Medicine and Health Sciences</topic><topic>Microbiological research</topic><topic>Monkeys &amp; apes</topic><topic>Mosquitoes</topic><topic>Natural selection</topic><topic>Nucleotides</topic><topic>Nucleotides - genetics</topic><topic>Parasites</topic><topic>Parasites - genetics</topic><topic>People and places</topic><topic>Peptides - chemistry</topic><topic>Phylogeny</topic><topic>Plasmodium (Protozoa)</topic><topic>Plasmodium vivax - genetics</topic><topic>Plasmodium vivax - isolation &amp; purification</topic><topic>Polymorphism</topic><topic>Polymorphism, Genetic</topic><topic>Protozoan Proteins - chemistry</topic><topic>Protozoan Proteins - genetics</topic><topic>Recombination</topic><topic>Research and Analysis Methods</topic><topic>Selection, Genetic</topic><topic>Single-nucleotide polymorphism</topic><topic>Vaccine efficacy</topic><topic>Vaccines</topic><topic>Vector-borne diseases</topic><topic>Virulence (Microbiology)</topic><topic>Zoonoses</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Almeida-de-Oliveira, Natália Ketrin</creatorcontrib><creatorcontrib>Abreu-Fernandes, Rebecca de</creatorcontrib><creatorcontrib>Lima-Cury, Lidiane</creatorcontrib><creatorcontrib>Lavigne, Aline Rosa de</creatorcontrib><creatorcontrib>Pina-Costa, Anielle de</creatorcontrib><creatorcontrib>Perce-da-Silva, Daiana de Souza</creatorcontrib><creatorcontrib>Catanho, Marcos</creatorcontrib><creatorcontrib>Rossi, Atila Duque</creatorcontrib><creatorcontrib>Brasil, Patrícia</creatorcontrib><creatorcontrib>Daniel-Ribeiro, Cláudio Tadeu</creatorcontrib><creatorcontrib>Ferreira-da-Cruz, Maria de Fátima</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Nursing &amp; 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Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing &amp; Allied Health Database (Alumni Edition)</collection><collection>Meteorological &amp; Geoastrophysical Abstracts - Academic</collection><collection>ProQuest Engineering Collection</collection><collection>ProQuest Biological Science Collection</collection><collection>Agricultural Science Database</collection><collection>Health &amp; Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biological Science Database</collection><collection>Engineering Database</collection><collection>Nursing &amp; Allied Health Premium</collection><collection>Advanced Technologies &amp; Aerospace Database</collection><collection>ProQuest Advanced Technologies &amp; Aerospace Collection</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Environmental Science Database</collection><collection>Materials Science Collection</collection><collection>Publicly Available Content Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>Engineering Collection</collection><collection>Environmental Science Collection</collection><collection>Genetics Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PloS one</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Almeida-de-Oliveira, Natália Ketrin</au><au>Abreu-Fernandes, Rebecca de</au><au>Lima-Cury, Lidiane</au><au>Lavigne, Aline Rosa de</au><au>Pina-Costa, Anielle de</au><au>Perce-da-Silva, Daiana de Souza</au><au>Catanho, Marcos</au><au>Rossi, Atila Duque</au><au>Brasil, Patrícia</au><au>Daniel-Ribeiro, Cláudio Tadeu</au><au>Ferreira-da-Cruz, Maria de Fátima</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Balancing selection and high genetic diversity of Plasmodium vivax circumsporozoite central region in parasites from Brazilian Amazon and Rio de Janeiro Atlantic Forest</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2020-11-09</date><risdate>2020</risdate><volume>15</volume><issue>11</issue><spage>e0241426</spage><pages>e0241426-</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>Circumsporozoite protein (CSP) is the primary pre-erythrocytic vaccine target in Plasmodium species. Knowledge about their genetic diversity can help predict vaccine efficacy and the spread of novel parasite variants. Thus, we investigated pvcsp gene polymorphisms in 219 isolates (136 from Brazilian Amazon [BA], 71 from Rio de Janeiro Atlantic Forest [AF], and 12 from non-Brazilian countries [NB]). Forty-eight polymorphic sites were detected, 46 in the central repeat region (CR), and two in the C-terminal region. Also, the CR presents InDels and a variable number of repeats. All samples correspond to the VK210 variant, and 24 VK210 subtypes based on CR. Nucleotide diversity (π = 0.0135) generated a significant number of haplotypes (168) with low genetic differentiation between the Brazilian regions (Fst = 0.208). The haplotype network revealed similar distances among the BA and AF regions. The linkage disequilibrium indicates that recombination does not seem to be acting in diversity, reinforcing natural selection's role in accelerating adaptive evolution. The high diversity (low Fst) and polymorphism frequencies could be indicators of balancing selection. Although malaria in BA and AF have distinct vector species and different host immune pressures, consistent genetic signature was found in two regions. The immunodominant B-cell epitope mapped in the CR varies from seven to 19 repeats. The CR T-cell epitope is conserved only in 39 samples. Concerning to C-terminal region, the Th2R epitope presented nonsynonymous SNP only in 6% of Brazilian samples, and the Th3R epitope remained conserved in all studied regions. We conclude that, although the uneven distribution of alleles may jeopardize the deployment of vaccines directed to a specific variable locus, a unique vaccine formulation could protect populations in all Brazilian regions.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>33166298</pmid><doi>10.1371/journal.pone.0241426</doi><tpages>e0241426</tpages><orcidid>https://orcid.org/0000-0001-6235-8807</orcidid><orcidid>https://orcid.org/0000-0003-3522-3792</orcidid><oa>free_for_read</oa></addata></record>
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identifier ISSN: 1932-6203
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1932-6203
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source MEDLINE; DOAJ Directory of Open Access Journals; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; Free Full-Text Journals in Chemistry; Public Library of Science (PLoS)
subjects Amino Acid Sequence
Amino Acid Substitution
Animals
Atlantic Ocean
Balancing
Biology and Life Sciences
Brazil
Circumsporozoite protein
Codon - genetics
Epitopes
Epitopes, B-Lymphocyte - chemistry
Epitopes, B-Lymphocyte - genetics
Epitopes, T-Lymphocyte - chemistry
Epitopes, T-Lymphocyte - genetics
Evolution
Gene polymorphism
Genetic aspects
Genetic diversity
Genetic polymorphisms
Genetic Variation
Geography
Haplotypes
Haplotypes - genetics
Health aspects
INDEL Mutation - genetics
Infections
Laboratories
Linkage disequilibrium
Linkage Disequilibrium - genetics
Lymphocytes B
Lymphocytes T
Malaria
Medicine and Health Sciences
Microbiological research
Monkeys & apes
Mosquitoes
Natural selection
Nucleotides
Nucleotides - genetics
Parasites
Parasites - genetics
People and places
Peptides - chemistry
Phylogeny
Plasmodium (Protozoa)
Plasmodium vivax - genetics
Plasmodium vivax - isolation & purification
Polymorphism
Polymorphism, Genetic
Protozoan Proteins - chemistry
Protozoan Proteins - genetics
Recombination
Research and Analysis Methods
Selection, Genetic
Single-nucleotide polymorphism
Vaccine efficacy
Vaccines
Vector-borne diseases
Virulence (Microbiology)
Zoonoses
title Balancing selection and high genetic diversity of Plasmodium vivax circumsporozoite central region in parasites from Brazilian Amazon and Rio de Janeiro Atlantic Forest
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