Adaptation of Plasmodium falciparum to humans involved the loss of an ape-specific erythrocyte invasion ligand.
Animals
CRISPR-Cas Systems
/ genetics
Cell Engineering
Erythrocytes
/ metabolism
Evolution, Molecular
Frameshift Mutation
Gene Editing
HEK293 Cells
Host Specificity
/ genetics
Humans
Loss of Function Mutation
Malaria, Falciparum
/ parasitology
Pan troglodytes
/ parasitology
Plasmodium falciparum
/ genetics
Protozoan Proteins
/ genetics
Sialic Acids
/ metabolism
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
04 10 2019
04 10 2019
Historique:
received:
15
02
2019
accepted:
02
09
2019
entrez:
6
10
2019
pubmed:
6
10
2019
medline:
15
2
2020
Statut:
epublish
Résumé
Plasmodium species are frequently host-specific, but little is currently known about the molecular factors restricting host switching. This is particularly relevant for P. falciparum, the only known human-infective species of the Laverania sub-genus, all other members of which infect African apes. Here we show that all tested P. falciparum isolates contain an inactivating mutation in an erythrocyte invasion associated gene, PfEBA165, the homologues of which are intact in all ape-infective Laverania species. Recombinant EBA165 proteins only bind ape, not human, erythrocytes, and this specificity is due to differences in erythrocyte surface sialic acids. Correction of PfEBA165 inactivating mutations by genome editing yields viable parasites, but is associated with down regulation of both PfEBA165 and an adjacent invasion ligand, which suggests that PfEBA165 expression is incompatible with parasite growth in human erythrocytes. Pseudogenization of PfEBA165 may represent a key step in the emergence and evolution of P. falciparum.
Identifiants
pubmed: 31586047
doi: 10.1038/s41467-019-12294-3
pii: 10.1038/s41467-019-12294-3
pmc: PMC6778099
doi:
Substances chimiques
Protozoan Proteins
0
Sialic Acids
0
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
4512Subventions
Organisme : NIAID NIH HHS
ID : R37 AI050529
Pays : United States
Organisme : NIAID NIH HHS
ID : T32 AI007532
Pays : United States
Organisme : Wellcome Trust
ID : 206194/Z/17/Z
Pays : United Kingdom
Organisme : NIAID NIH HHS
ID : P30 AI045008
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI120810
Pays : United States
Organisme : NIAID NIH HHS
ID : R01 AI091595
Pays : United States
Organisme : Wellcome Trust
Pays : United Kingdom
Commentaires et corrections
Type : ErratumIn
Références
Liu, W. et al. Origin of the human malaria parasite Plasmodium falciparum in gorillas. Nature 467, 420–425 (2010).
doi: 10.1038/nature09442
Liu, W. et al. Multigenomic delineation of Plasmodium species of the Laverania subgenus infecting wild-living Chimpanzees and Gorillas. Genome Biol. Evol. 8, 1929–1939 (2016).
doi: 10.1093/gbe/evw128
Liu, W. et al. Wild bonobos host geographically restricted malaria parasites including a putative new Laverania species. Nat. Commun. 8, 1635 (2017).
doi: 10.1038/s41467-017-01798-5
Otto, T. D. et al. Genomes of all known members of a Plasmodium subgenus reveal paths to virulent human malaria. Nat. Microbiol. 3, 687–697 (2018).
doi: 10.1038/s41564-018-0162-2
Sundararaman, S. A. et al. Plasmodium falciparum-like parasites infecting wild apes in southern Cameroon do not represent a recurrent source of human malaria. Proc. Natl Acad. Sci. USA 110, 7020–7025 (2013).
doi: 10.1073/pnas.1305201110
Loy, D. E. et al. Investigating zoonotic infection barriers to ape Plasmodium parasites using faecal DNA analysis. Int. J. Parasitol. 48, 531–542 (2018).
doi: 10.1016/j.ijpara.2017.12.002
Delicat-Loembet, L. et al. No evidence for ape Plasmodium infections in humans in Gabon. PloS ONE 10, e0126933 (2015).
doi: 10.1371/journal.pone.0126933
Rayner, J. C., Liu, W., Peeters, M., Sharp, P. M. & Hahn, B. H. A plethora of Plasmodium species in wild apes: a source of human infection? Trends Parasitol. 27, 222–229 (2011).
doi: 10.1016/j.pt.2011.01.006
Ngoubangoye, B. et al. The host specificity of ape malaria parasites can be broken in confined environments. Int. J. Parasitol. 46, 737–744 (2016).
doi: 10.1016/j.ijpara.2016.06.004
Singh, B. et al. A large focus of naturally acquired Plasmodium knowlesi infections in human beings. Lancet 363, 1017–1024 (2004).
doi: 10.1016/S0140-6736(04)15836-4
Otto, T. D. et al. Genome sequencing of chimpanzee malaria parasites reveals possible pathways of adaptation to human hosts. Nat. Commun. 5, 4754 (2014).
doi: 10.1038/ncomms5754
Sundararaman, S. A. et al. Genomes of cryptic chimpanzee Plasmodium species reveal key evolutionary events leading to human malaria. Nat. Commun. 7, 11078 (2016).
doi: 10.1038/ncomms11078
Plenderleith, L. J. et al. Adaptive Evolution of RH5 in Ape Plasmodium species of the Laverania Subgenus. mBio 9, pii: e02237–17 (2018).
Wanaguru, M., Liu, W., Hahn, B. H., Rayner, J. C., Wright, G. J. RH5-Basigin interaction plays a major role in the host tropism of Plasmodium falciparum. Proc. Natl Acad. Sci. USA 110, 20735–20740 (2013).
doi: 10.1073/pnas.1320771110
Cowman, A. F., Tonkin, C. J., Tham, W. H. & Duraisingh, M. T. The Molecular basis of erythrocyte invasion by malaria parasites. Cell Host Microbe 22, 232–245 (2017).
doi: 10.1016/j.chom.2017.07.003
Sim, B. K., Chitnis, C. E., Wasniowska, K., Hadley, T. J. & Miller, L. H. Receptor and ligand domains for invasion of erythrocytes by Plasmodium falciparum. Science 264, 1941–1944 (1994).
doi: 10.1126/science.8009226
Maier, A. G. et al. Plasmodium falciparum erythrocyte invasion through glycophorin C and selection for Gerbich negativity in human populations. Nat. Med. 9, 87–92 (2003).
doi: 10.1038/nm807
Lobo, C. A., Rodriguez, M., Reid, M. & Lustigman, S. Glycophorin C is the receptor for the Plasmodium falciparum erythrocyte binding ligand PfEBP-2 (baebl). Blood 101, 4628–4631 (2003).
doi: 10.1182/blood-2002-10-3076
Mayer, D. C. et al. Glycophorin B is the erythrocyte receptor of Plasmodium falciparum erythrocyte-binding ligand, EBL-1. Proc. Natl Acad. Sci. USA 106, 5348–5352 (2009).
doi: 10.1073/pnas.0900878106
Triglia, T., Thompson, J. K. & Cowman, A. F. An EBA175 homologue which is transcribed but not translated in erythrocytic stages of Plasmodium falciparum. Mol. Biochemical Parasitol. 116, 55–63 (2001).
doi: 10.1016/S0166-6851(01)00303-6
Rayner, J. C., Huber, C. S. & Barnwell, J. W. Conservation and divergence in erythrocyte invasion ligands: Plasmodium reichenowi EBL genes. Mol. biochemical Parasitol. 138, 243–247 (2004).
doi: 10.1016/j.molbiopara.2004.08.008
Wanaguru, M., Crosnier, C., Johnson, S., Rayner, J. C. & Wright, G. J. Biochemical Analysis of the Plasmodium falciparum Erythrocyte-binding Antigen-175 (EBA175)-Glycophorin-A Interaction: Implications for Vaccine Design. J. Biol. Chem. 288, 32106–32117 (2013).
doi: 10.1074/jbc.M113.484840
Chou, H. H. et al. A mutation in human CMP-sialic acid hydroxylase occurred after the Homo-Pan divergence. Proc. Natl Acad. Sci. USA 95, 11751–11756 (1998).
doi: 10.1073/pnas.95.20.11751
Muchmore, E. A., Diaz, S. & Varki, A. A structural difference between the cell surfaces of humans and the great apes. Am. J. Phys. Anthropol. 107, 187–198 (1998).
doi: 10.1002/(SICI)1096-8644(199810)107:2<187::AID-AJPA5>3.0.CO;2-S
Orlandi, P. A., Klotz, F. W. & Haynes, J. D. A malaria invasion receptor, the 175-kilodalton erythrocyte binding antigen of Plasmodium falciparum recognizes the terminal Neu5Ac(alpha 2-3)Gal- sequences of glycophorin A. J. Cell Biol. 116, 901–909 (1992).
doi: 10.1083/jcb.116.4.901
Dankwa, S. et al. Ancient human sialic acid variant restricts an emerging zoonotic malaria parasite. Nat. Commun. 7, 11187 (2016).
doi: 10.1038/ncomms11187
Reed, M. B. et al. Targeted disruption of an erythrocyte binding antigen in Plasmodium falciparum is associated with a switch toward a sialic acid-independent pathway of invasion. Proc. Natl Acad. Sci. USA 97, 7509–7514 (2000).
doi: 10.1073/pnas.97.13.7509
Duraisingh, M. T., Maier, A. G., Triglia, T. & Cowman, A. F. Erythrocyte-binding antigen 175 mediates invasion in Plasmodium falciparum utilizing sialic acid-dependent and -independent pathways. Proc. Natl Acad. Sci. USA 100, 4796–4801 (2003).
doi: 10.1073/pnas.0730883100
Duraisingh, M. T. et al. Phenotypic variation of Plasmodium falciparum merozoite proteins directs receptor targeting for invasion of human erythrocytes. EMBO J. 22, 1047–1057 (2003).
doi: 10.1093/emboj/cdg096
Poole, J. Red cell antigens on band 3 and glycophorin A. Blood Rev. 14, 31–43 (2000).
doi: 10.1054/blre.1999.0124
Dolan, S. A., Miller, L. H. & Wellems, T. E. Evidence for a switching mechanism in the invasion of erythrocytes by Plasmodium falciparum. J. Clin. Investig. 86, 618–624 (1990).
doi: 10.1172/JCI114753
Crowley, V. M., Rovira-Graells, N., Ribas de Pouplana, L. & Cortes, A. Heterochromatin formation in bistable chromatin domains controls the epigenetic repression of clonally variant Plasmodium falciparum genes linked to erythrocyte invasion. Mol. Microbiol. 80, 391–406 (2011).
doi: 10.1111/j.1365-2958.2011.07574.x
Stubbs, J. et al. Molecular mechanism for switching of P. falciparum invasion pathways into human erythrocytes. Science 309, 1384–1387 (2005).
doi: 10.1126/science.1115257
Lemieux, J. E. et al. Statistical estimation of cell-cycle progression and lineage commitment in Plasmodium falciparum reveals a homogeneous pattern of transcription in ex vivo culture. Proc. Natl Acad. Sci. USA 106, 7559–7564 (2009).
doi: 10.1073/pnas.0811829106
Tarr, S. J. et al. Schizont transcriptome variation among clinical isolates and laboratory-adapted clones of the malaria parasite Plasmodium falciparum. BMC genomics 19, 894 (2018).
doi: 10.1186/s12864-018-5257-x
Spadafora, C. et al. Complement receptor 1 is a sialic acid-independent erythrocyte receptor of Plasmodium falciparum. PLoS Pathog. 6, e1000968 (2010).
doi: 10.1371/journal.ppat.1000968
Tham, W. H. et al. Complement receptor 1 is the host erythrocyte receptor for Plasmodium falciparum PfRh4 invasion ligand. Proc. Natl Acad. Sci. USA 107, 17327–17332 (2010).
doi: 10.1073/pnas.1008151107
Tham, W. H., Healer, J. & Cowman, A. F. Erythrocyte and reticulocyte binding-like proteins of Plasmodium falciparum. Trends Parasitol. 28, 23–30 (2012).
doi: 10.1016/j.pt.2011.10.002
Baum, J., Maier, A. G., Good, R. T., Simpson, K. M. & Cowman, A. F. Invasion by P. falciparum merozoites suggests a hierarchy of molecular interactions. PLoS Pathog. 1, e37 (2005).
doi: 10.1371/journal.ppat.0010037
Moon, R. W. et al. Normocyte-binding protein required for human erythrocyte invasion by the zoonotic malaria parasite Plasmodium knowlesi. Proc. Natl Acad. Sci. USA 113, 7231–7236 (2016).
doi: 10.1073/pnas.1522469113
Reddy, K. S. et al. Bacterially expressed full-length recombinant Plasmodium falciparum RH5 protein binds erythrocytes and elicits potent strain-transcending parasite-neutralizing antibodies. Infect. Immun. 82, 152–164 (2014).
doi: 10.1128/IAI.00970-13
Volz, J. C. et al. Essential role of the PfRh5/PfRipr/CyRPA complex during Plasmodium falciparum Invasion of erythrocytes. Cell Host Microbe 20, 60–71 (2016).
doi: 10.1016/j.chom.2016.06.004
Galaway, F. et al. P113 is a merozoite surface protein that binds the N terminus of Plasmodium falciparum RH5. Nat. Commun. 8, 14333 (2017).
doi: 10.1038/ncomms14333
Crosnier, C. et al. A library of functional recombinant cell surface and secreted Plasmodium falciparum merozoite proteins. Mol. Cell. Proteom. 12, 3976–86 (2013).
doi: 10.1074/mcp.O113.028357
Petersen, T. N., Brunak, S., von Heijne, G. & Nielsen, H. SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat. Methods 8, 785–786 (2011).
doi: 10.1038/nmeth.1701
Sonnhammer, E. L., von Heijne, G. & Krogh, A. A hidden Markov model for predicting transmembrane helices in protein sequences. Proc. Int. Conf. Intell. Syst. Mol. Biol. 6, 175–182 (1998).
pubmed: 9783223
Bushell, K. M., Sollner, C., Schuster-Boeckler, B., Bateman, A. & Wright, G. J. Large-scale screening for novel low-affinity extracellular protein interactions. Genome Res. 18, 622–630 (2008).
doi: 10.1101/gr.7187808
Giarratana, M. C. et al. Proof of principle for transfusion of in vitro-generated red blood cells. Blood 118, 5071–5079 (2011).
doi: 10.1182/blood-2011-06-362038
Trager, W. & Jensen, J. B. Human malaria parasites in continuous culture. Science 193, 673–675 (1976).
doi: 10.1126/science.781840
Lim M. Y., et al. UDP-galactose and acetyl-CoA transporters as Plasmodium multidrug resistance genes. Nat. Microbiol. 1, 16166 (2016).
Heng L. Aligning sequence reads, clone sequences and assembly with BWA-MEM. https://arxiv.org/abs/1303.3997 [arxiv.org] (2013).
Garrison E., Gabor, M. Haplotype-based variant detection from short-read sequencing. https://arxiv.org/abs/1207.3907 [arxiv.org] (2012).
Cingolani, P. et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly. (Austin) 6, 80–92 (2012).
doi: 10.4161/fly.19695
Theron, M., Hesketh, R. L., Subramanian, S. & Rayner, J. C. An adaptable two-color flow cytometric assay to quantitate the invasion of erythrocytes by Plasmodium falciparum parasites. Cytom. A 77, 1067–1074 (2010).
doi: 10.1002/cyto.a.20972
Spence, P. J. et al. Vector transmission regulates immune control of Plasmodium virulence. Nature 498, 228–231 (2013).
doi: 10.1038/nature12231
Kozarewa, I. et al. Amplification-free Illumina sequencing-library preparation facilitates improved mapping and assembly of (G+C)-biased genomes. Nat. Methods 6, 291–295 (2009).
doi: 10.1038/nmeth.1311
Anders, S. & Huber, W. Differential expression analysis for sequence count data. Genome Biol. 11, R106 (2010).
doi: 10.1186/gb-2010-11-10-r106
Rovira-Graells, N. et al. Transcriptional variation in the malaria parasite Plasmodium falciparum. Genome Res. 22, 925–938 (2012).
doi: 10.1101/gr.129692.111