Disease progression in Plasmodium knowlesi malaria is linked to variation in invasion gene family members
Emerging pathogens undermine initiatives to control the global health impact of infectious diseases. Zoonotic malaria is no exception. Plasmodium knowlesi, a malaria parasite of Southeast Asian macaques, has entered the human population. P. knowlesi, like Plasmodium falciparum, can reach high parasi...
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| Published in | PLoS neglected tropical diseases Vol. 8; no. 8; p. e3086 |
|---|---|
| Main Authors | , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
01.08.2014
Public Library of Science (PLoS) |
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| Abstract | Emerging pathogens undermine initiatives to control the global health impact of infectious diseases. Zoonotic malaria is no exception. Plasmodium knowlesi, a malaria parasite of Southeast Asian macaques, has entered the human population. P. knowlesi, like Plasmodium falciparum, can reach high parasitaemia in human infections, and the World Health Organization guidelines for severe malaria list hyperparasitaemia among the measures of severe malaria in both infections. Not all patients with P. knowlesi infections develop hyperparasitaemia, and it is important to determine why. Between isolate variability in erythrocyte invasion, efficiency seems key. Here we investigate the idea that particular alleles of two P. knowlesi erythrocyte invasion genes, P. knowlesi normocyte binding protein Pknbpxa and Pknbpxb, influence parasitaemia and human disease progression. Pknbpxa and Pknbpxb reference DNA sequences were generated from five geographically and temporally distinct P. knowlesi patient isolates. Polymorphic regions of each gene (approximately 800 bp) were identified by haplotyping 147 patient isolates at each locus. Parasitaemia in the study cohort was associated with markers of disease severity including liver and renal dysfunction, haemoglobin, platelets and lactate, (r = ≥ 0.34, p = <0.0001 for all). Seventy-five and 51 Pknbpxa and Pknbpxb haplotypes were resolved in 138 (94%) and 134 (92%) patient isolates respectively. The haplotypes formed twelve Pknbpxa and two Pknbpxb allelic groups. Patients infected with parasites with particular Pknbpxa and Pknbpxb alleles within the groups had significantly higher parasitaemia and other markers of disease severity. Our study strongly suggests that P. knowlesi invasion gene variants contribute to parasite virulence. We focused on two invasion genes, and we anticipate that additional virulent loci will be identified in pathogen genome-wide studies. The multiple sustained entries of this diverse pathogen into the human population must give cause for concern to malaria elimination strategists in the Southeast Asian region. |
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| AbstractList | Emerging pathogens undermine initiatives to control the global health impact of infectious diseases. Zoonotic malaria is no exception. Plasmodium knowlesi, a malaria parasite of Southeast Asian macaques, has entered the human population. P. knowlesi, like Plasmodium falciparum, can reach high parasitaemia in human infections, and the World Health Organization guidelines for severe malaria list hyperparasitaemia among the measures of severe malaria in both infections. Not all patients with P. knowlesi infections develop hyperparasitaemia, and it is important to determine why. Between isolate variability in erythrocyte invasion, efficiency seems key. Here we investigate the idea that particular alleles of two P. knowlesi erythrocyte invasion genes, P. knowlesi normocyte binding protein Pknbpxa and Pknbpxb, influence parasitaemia and human disease progression. Pknbpxa and Pknbpxb reference DNA sequences were generated from five geographically and temporally distinct P. knowlesi patient isolates. Polymorphic regions of each gene (approximately 800 bp) were identified by haplotyping 147 patient isolates at each locus. Parasitaemia in the study cohort was associated with markers of disease severity including liver and renal dysfunction, haemoglobin, platelets and lactate, (r= greater than or equal to 0.34,p=<0.0001 for all). Seventy-five and 51 Pknbpxa and Pknbpxb haplotypes were resolved in 138 (94%) and 134 (92%) patient isolates respectively. The haplotypes formed twelve Pknbpxa and two Pknbpxb allelic groups. Patients infected with parasites with particular Pknbpxa and Pknbpxb alleles within the groups had significantly higher parasitaemia and other markers of disease severity. Our study strongly suggests that P. knowlesi invasion gene variants contribute to parasite virulence. We focused on two invasion genes, and we anticipate that additional virulent loci will be identified in pathogen genome-wide studies. The multiple sustained entries of this diverse pathogen into the human population must give cause for concern to malaria elimination strategists in the Southeast Asian region. Plasmodium knowlesi, a parasite of Southeast Asian macaques, has entered the human population. Approximately 10% of P. knowlesi infections are severe, 1-2% are fatal, in Sarawak, Malaysian Borneo. Increase in parasitaemia is associated with disease severity, but little is known about parasite virulence in this newly described human pathogen. Here we present the results of a study on P. knowlesi parasites collected from 147 patients. We use the isolates to produce DNA sequences from a polymorphic (genetically variable) region of two P. knowlesi genes, Pknbpxa and Pknbpxb, that are involved in parasite entry into host red blood cells. We addressed the question that some parasite genotypes may have an invasion advantage leading to severe disease in human infections. We analysed the DNA sequences with matched clinical and laboratory data from the patient cohort (n=147). We found that specific DNA sequences (Pknbpxa and Pknbpxb alleles) clustered with high parasitaemia and markers of disease severity. Here, for the first time, we provide evidence that variant alleles of the Plasmodium Reticulocyte Binding-Like Protein invasion gene family can influence disease progression in patients with malaria. The biological characteristics of the variants will be studied to aid our understanding of malaria pathophysiology and to inform intervention strategies. Emerging pathogens undermine initiatives to control the global health impact of infectious diseases. Zoonotic malaria is no exception. Plasmodium knowlesi, a malaria parasite of Southeast Asian macaques, has entered the human population. P. knowlesi, like Plasmodium falciparum, can reach high parasitaemia in human infections, and the World Health Organization guidelines for severe malaria list hyperparasitaemia among the measures of severe malaria in both infections. Not all patients with P. knowlesi infections develop hyperparasitaemia, and it is important to determine why. Between isolate variability in erythrocyte invasion, efficiency seems key. Here we investigate the idea that particular alleles of two P. knowlesi erythrocyte invasion genes, P. knowlesi normocyte binding protein Pknbpxa and Pknbpxb, influence parasitaemia and human disease progression. Pknbpxa and Pknbpxb reference DNA sequences were generated from five geographically and temporally distinct P. knowlesi patient isolates. Polymorphic regions of each gene (approximately 800 bp) were identified by haplotyping 147 patient isolates at each locus. Parasitaemia in the study cohort was associated with markers of disease severity including liver and renal dysfunction, haemoglobin, platelets and lactate, (r = ≥ 0.34, p = <0.0001 for all). Seventy-five and 51 Pknbpxa and Pknbpxb haplotypes were resolved in 138 (94%) and 134 (92%) patient isolates respectively. The haplotypes formed twelve Pknbpxa and two Pknbpxb allelic groups. Patients infected with parasites with particular Pknbpxa and Pknbpxb alleles within the groups had significantly higher parasitaemia and other markers of disease severity. Our study strongly suggests that P. knowlesi invasion gene variants contribute to parasite virulence. We focused on two invasion genes, and we anticipate that additional virulent loci will be identified in pathogen genome-wide studies. The multiple sustained entries of this diverse pathogen into the human population must give cause for concern to malaria elimination strategists in the Southeast Asian region. Emerging pathogens undermine initiatives to control the global health impact of infectious diseases. Zoonotic malaria is no exception. Plasmodium knowlesi, a malaria parasite of Southeast Asian macaques, has entered the human population. P. knowlesi, like Plasmodium falciparum, can reach high parasitaemia in human infections, and the World Health Organization guidelines for severe malaria list hyperparasitaemia among the measures of severe malaria in both infections. Not all patients with P. knowlesi infections develop hyperparasitaemia, and it is important to determine why. Between isolate variability in erythrocyte invasion, efficiency seems key. Here we investigate the idea that particular alleles of two P. knowlesi erythrocyte invasion genes, P. knowlesi normocyte binding protein Pknbpxa and Pknbpxb, influence parasitaemia and human disease progression. Pknbpxa and Pknbpxb reference DNA sequences were generated from five geographically and temporally distinct P. knowlesi patient isolates. Polymorphic regions of each gene (approximately 800 bp) were identified by haplotyping 147 patient isolates at each locus. Parasitaemia in the study cohort was associated with markers of disease severity including liver and renal dysfunction, haemoglobin, platelets and lactate, (r = [greater than or equal to] 0.34, p =,0.0001 for all). Seventy-five and 51 Pknbpxa and Pknbpxb haplotypes were resolved in 138 (94%) and 134 (92%) patient isolates respectively. The haplotypes formed twelve Pknbpxa and two Pknbpxb allelic groups. Patients infected with parasites with particular Pknbpxa and Pknbpxb alleles within the groups had significantly higher parasitaemia and other markers of disease severity. Our study strongly suggests that P. knowlesi invasion gene variants contribute to parasite virulence. We focused on two invasion genes, and we anticipate that additional virulent loci will be identified in pathogen genome-wide studies. The multiple sustained entries of this diverse pathogen into the human population must give cause for concern to malaria elimination strategists in the Southeast Asian region. Emerging pathogens undermine initiatives to control the global health impact of infectious diseases. Zoonotic malaria is no exception. Plasmodium knowlesi , a malaria parasite of Southeast Asian macaques, has entered the human population. P. knowlesi , like Plasmodium falciparum , can reach high parasitaemia in human infections, and the World Health Organization guidelines for severe malaria list hyperparasitaemia among the measures of severe malaria in both infections. Not all patients with P. knowlesi infections develop hyperparasitaemia, and it is important to determine why. Between isolate variability in erythrocyte invasion, efficiency seems key. Here we investigate the idea that particular alleles of two P. knowlesi erythrocyte invasion genes, P. knowlesi normocyte binding protein Pknbpxa and Pknbpxb , influence parasitaemia and human disease progression. Pknbpxa and Pknbpxb reference DNA sequences were generated from five geographically and temporally distinct P. knowlesi patient isolates. Polymorphic regions of each gene (approximately 800 bp) were identified by haplotyping 147 patient isolates at each locus. Parasitaemia in the study cohort was associated with markers of disease severity including liver and renal dysfunction, haemoglobin, platelets and lactate, (r = ≥0.34 , p = <0.0001 for all). Seventy-five and 51 Pknbpxa and Pknbpxb haplotypes were resolved in 138 (94%) and 134 (92%) patient isolates respectively. The haplotypes formed twelve Pknbpxa and two Pknbpxb allelic groups. Patients infected with parasites with particular Pknbpxa and Pknbpxb alleles within the groups had significantly higher parasitaemia and other markers of disease severity. Our study strongly suggests that P. knowlesi invasion gene variants contribute to parasite virulence. We focused on two invasion genes, and we anticipate that additional virulent loci will be identified in pathogen genome-wide studies. The multiple sustained entries of this diverse pathogen into the human population must give cause for concern to malaria elimination strategists in the Southeast Asian region. Plasmodium knowlesi , a parasite of Southeast Asian macaques, has entered the human population. Approximately 10% of P. knowlesi infections are severe, 1–2% are fatal, in Sarawak, Malaysian Borneo. Increase in parasitaemia is associated with disease severity, but little is known about parasite virulence in this newly described human pathogen. Here we present the results of a study on P. knowlesi parasites collected from 147 patients. We use the isolates to produce DNA sequences from a polymorphic (genetically variable) region of two P. knowlesi genes, Pknbpxa and Pknbpxb , that are involved in parasite entry into host red blood cells. We addressed the question that some parasite genotypes may have an invasion advantage leading to severe disease in human infections. We analysed the DNA sequences with matched clinical and laboratory data from the patient cohort (n = 147). We found that specific DNA sequences ( Pknbpxa and Pknbpxb alleles) clustered with high parasitaemia and markers of disease severity. Here, for the first time, we provide evidence that variant alleles of the Plasmodium Reticulocyte Binding-Like Protein invasion gene family can influence disease progression in patients with malaria. The biological characteristics of the variants will be studied to aid our understanding of malaria pathophysiology and to inform intervention strategies. Emerging pathogens undermine initiatives to control the global health impact of infectious diseases. Zoonotic malaria is no exception. Plasmodium knowlesi, a malaria parasite of Southeast Asian macaques, has entered the human population. P. knowlesi, like Plasmodium falciparum, can reach high parasitaemia in human infections, and the World Health Organization guidelines for severe malaria list hyperparasitaemia among the measures of severe malaria in both infections. Not all patients with P. knowlesi infections develop hyperparasitaemia, and it is important to determine why. Between isolate variability in erythrocyte invasion, efficiency seems key. Here we investigate the idea that particular alleles of two P. knowlesi erythrocyte invasion genes, P. knowlesi normocyte binding protein Pknbpxa and Pknbpxb, influence parasitaemia and human disease progression. Pknbpxa and Pknbpxb reference DNA sequences were generated from five geographically and temporally distinct P. knowlesi patient isolates. Polymorphic regions of each gene (approximately 800 bp) were identified by haplotyping 147 patient isolates at each locus. Parasitaemia in the study cohort was associated with markers of disease severity including liver and renal dysfunction, haemoglobin, platelets and lactate, (r = ≥0.34, p = <0.0001 for all). Seventy-five and 51 Pknbpxa and Pknbpxb haplotypes were resolved in 138 (94%) and 134 (92%) patient isolates respectively. The haplotypes formed twelve Pknbpxa and two Pknbpxb allelic groups. Patients infected with parasites with particular Pknbpxa and Pknbpxb alleles within the groups had significantly higher parasitaemia and other markers of disease severity. Our study strongly suggests that P. knowlesi invasion gene variants contribute to parasite virulence. We focused on two invasion genes, and we anticipate that additional virulent loci will be identified in pathogen genome-wide studies. The multiple sustained entries of this diverse pathogen into the human population must give cause for concern to malaria elimination strategists in the Southeast Asian region. |
| Audience | Academic |
| Author | Divis, Paul C Zainudin, Ramlah Lynch, Sean Wong, Ing Tien Siner, Angela Cox-Singh, Janet Singh, Balbir Krishna, Sanjeev Willmann, Matthias Pinheiro, Miguel M Singh-Khaira, Sarina K Millar, Scott B Lu, Chan Woon Ahmed, Atique M |
| AuthorAffiliation | 3 Faculty of Resource Science and Technology, University Malaysia Sarawak, Kuching, Sarawak, Malaysia 2 School of Medicine, University of St Andrews, St Andrews, United Kingdom Institute of Tropical Medicine (NEKKEN), Japan 6 Division of Clinical Sciences, St. George's, University of London, London, United Kingdom 7 Clinical Blood Sciences, St. George's, University of London, London, United Kingdom 5 Sarikei Hospital, Sarikei, Sarawak, Malaysia 1 Malaria Research Centre, University Malaysia Sarawak, Kuching, Sarawak, Malaysia 4 Sibu Hospital, Sibu, Sarawak, Malaysia 8 Institute of Medical Microbiology and Hygiene, University of Tübingen, Tübingen, Germany |
| AuthorAffiliation_xml | – name: Institute of Tropical Medicine (NEKKEN), Japan – name: 2 School of Medicine, University of St Andrews, St Andrews, United Kingdom – name: 6 Division of Clinical Sciences, St. George's, University of London, London, United Kingdom – name: 5 Sarikei Hospital, Sarikei, Sarawak, Malaysia – name: 3 Faculty of Resource Science and Technology, University Malaysia Sarawak, Kuching, Sarawak, Malaysia – name: 7 Clinical Blood Sciences, St. George's, University of London, London, United Kingdom – name: 4 Sibu Hospital, Sibu, Sarawak, Malaysia – name: 8 Institute of Medical Microbiology and Hygiene, University of Tübingen, Tübingen, Germany – name: 1 Malaria Research Centre, University Malaysia Sarawak, Kuching, Sarawak, Malaysia |
| Author_xml | – sequence: 1 givenname: Atique M surname: Ahmed fullname: Ahmed, Atique M organization: Malaria Research Centre, University Malaysia Sarawak, Kuching, Sarawak, Malaysia – sequence: 2 givenname: Miguel M surname: Pinheiro fullname: Pinheiro, Miguel M organization: School of Medicine, University of St Andrews, St Andrews, United Kingdom – sequence: 3 givenname: Paul C surname: Divis fullname: Divis, Paul C organization: Malaria Research Centre, University Malaysia Sarawak, Kuching, Sarawak, Malaysia – sequence: 4 givenname: Angela surname: Siner fullname: Siner, Angela organization: Malaria Research Centre, University Malaysia Sarawak, Kuching, Sarawak, Malaysia – sequence: 5 givenname: Ramlah surname: Zainudin fullname: Zainudin, Ramlah organization: Malaria Research Centre, University Malaysia Sarawak, Kuching, Sarawak, Malaysia; Faculty of Resource Science and Technology, University Malaysia Sarawak, Kuching, Sarawak, Malaysia – sequence: 6 givenname: Ing Tien surname: Wong fullname: Wong, Ing Tien organization: Sibu Hospital, Sibu, Sarawak, Malaysia – sequence: 7 givenname: Chan Woon surname: Lu fullname: Lu, Chan Woon organization: Sarikei Hospital, Sarikei, Sarawak, Malaysia – sequence: 8 givenname: Sarina K surname: Singh-Khaira fullname: Singh-Khaira, Sarina K organization: Division of Clinical Sciences, St. George's, University of London, London, United Kingdom – sequence: 9 givenname: Scott B surname: Millar fullname: Millar, Scott B organization: School of Medicine, University of St Andrews, St Andrews, United Kingdom – sequence: 10 givenname: Sean surname: Lynch fullname: Lynch, Sean organization: Clinical Blood Sciences, St. George's, University of London, London, United Kingdom – sequence: 11 givenname: Matthias surname: Willmann fullname: Willmann, Matthias organization: Institute of Medical Microbiology and Hygiene, University of Tübingen, Tübingen, Germany – sequence: 12 givenname: Balbir surname: Singh fullname: Singh, Balbir organization: Malaria Research Centre, University Malaysia Sarawak, Kuching, Sarawak, Malaysia – sequence: 13 givenname: Sanjeev surname: Krishna fullname: Krishna, Sanjeev organization: Malaria Research Centre, University Malaysia Sarawak, Kuching, Sarawak, Malaysia; Division of Clinical Sciences, St. George's, University of London, London, United Kingdom – sequence: 14 givenname: Janet surname: Cox-Singh fullname: Cox-Singh, Janet organization: Malaria Research Centre, University Malaysia Sarawak, Kuching, Sarawak, Malaysia; School of Medicine, University of St Andrews, St Andrews, United Kingdom; Division of Clinical Sciences, St. George's, University of London, London, United Kingdom |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25121807$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | COPYRIGHT 2014 Public Library of Science 2014 Ahmed et al 2014 Ahmed et al 2014 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Malaria Is Linked to Variation in Invasion Gene Family Members. PLoS Negl Trop Dis 8(8): e3086. doi:10.1371/journal.pntd.0003086 |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Conceived and designed the experiments: JCS SK. Performed the experiments: AMA PCD SL MW. Analyzed the data: JCS AMA MMP RZ. Contributed reagents/materials/analysis tools: MMP SBM. Wrote the paper: JCS AMA. Patient recruitment: ITW CWL. Field work: AMA JCS BS AS. Data extraction and entry: SKSK. The authors have declared that no competing interests exist. |
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| Title | Disease progression in Plasmodium knowlesi malaria is linked to variation in invasion gene family members |
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