A Network Approach to Analyzing Highly Recombinant Malaria Parasite Genes

PLoS Computational Biology

Volumn 9, Issue 10, 2013, Pages

  Larremore, Daniel B ^a   Clauset, Aaron ^b,c,d   Buckee, Caroline O ^a  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b University of Colorado   (United States)

^c UNIVERSITY OF COLORADO   (United States)

^d SANTA FE INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEX NETWORKS; DISEASES; POPULATION STATISTICS; PROTEINS; STOCHASTIC MODELS; STOCHASTIC SYSTEMS; VALUE ENGINEERING;

ANTIGEN PROTEINS; GENES ENCODE; HIGH RATE; HUMAN MALARIA PARASITE; MALARIA PARASITE; NETWORK COMMUNITIES; PLASMODIUM FALCIPARUM; RATE OF RECOMBINATION; RED BLOOD CELL; VARIABLE REGIONS;

GENES;

DUFFY BINDING LIKE ALPHA PROTEIN; PROTOZOAL PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; DBLALPHA GENE; GENE; GENE FUNCTION; GENE IDENTIFICATION; GENE MAPPING; GENE REGULATORY NETWORK; GENE SEQUENCE; GENETIC VARIABILITY; GENOME ANALYSIS; MOLECULAR EVOLUTION; MOSAICISM; NONHUMAN; PFEMP1 GENE; PHENOTYPIC VARIATION; PLASMODIUM FALCIPARUM; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTOZOAL GENETICS; RECOMBINANT GENE; STOCHASTIC MODEL;

PLASMODIUM FALCIPARUM;

AMINO ACID SEQUENCE; COMPUTATIONAL BIOLOGY; COMPUTER SIMULATION; GENETIC VARIATION; HUMANS; MALARIA, FALCIPARUM; MOLECULAR SEQUENCE DATA; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; STOCHASTIC PROCESSES;

EID: 84887267765     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1003268     Document Type: Article

References (50)

1. World Malaria Report (2012) World Malaria Report. World Health Organization pp. 1-33.
2. Bull PC, Lowe BS, Kortok M, Molyneux CS, Newbold CI, et al. (1998) Parasite antigens on the infected red cell surface are targets for naturally acquired immunity to malaria. Nature medicine 4: 358-360.
3. Bull PC, Marsh K, (2002) The role of antibodies to Plasmodium falciparum-infected-erythrocyte surface antigens in naturally acquired immunity to malaria. Trends in Microbiology 10: 55-58.
4. Dodoo D, Staalsoe T, Giha H, Kurtzhals JA, Akanmori BD, et al. (2001) Antibodies to variant antigens on the surfaces of infected erythrocytes are associated with protection from malaria in Ghanaian children. Infection and Immunity 69: 3713-3718 doi:-10.1128/IAI.69.6.3713-3718.2001.
5. Giha HA, Staalsoe T, Dodoo D, Roper C, Satti GM, et al. (2000) Antibodies to variable Plasmodium falciparum-infected erythrocyte surface antigens are associated with protection from novel malaria infections. Immunology letters 71: 117-126.
6. Newbold CI, Pinches R, Roberts DJ, Marsh K, (1992) Plasmodium falciparum: The human agglutinating antibody response to the infected red cell surface is predominantly variant specific. Experimental parasitology 75: 281-292.
7. Chan J-A, Howell KB, Reiling L, Ataide R, Mackintosh CL, et al. (2012) Targets of antibodies against Plasmodium falciparum-infected erythrocytes in malaria immunity. J Clin Invest 122: 3227-3238 doi:10.1172/JCI62182DS1.
8. Bull PC, Lowe BS, Kortok M, Marsh K, (1999) Antibody recognition of Plasmodium falciparum erythrocyte surface antigens in Kenya: evidence for rare and prevalent variants. Infection and Immunity 67: 733-739.
9. Kyes S, Horrocks P, Newbold C, (2001) Antigenic variation at the infected red cell surface in malaria. Annual Reviews in Microbiology 55: 673-707.
10. Bull PC, Berriman M, Kyes S, Quail MA, Hall N, et al. (2005) Plasmodium falciparum Variant Surface Antigen Expression Patterns during Malaria. PLoS Pathog 1: e26 doi:10.1371/journal.ppat.0010026.st003.
11. Frank M, Kirkman L, Costantini D, Sanyal S, Lavazec C, et al. (2008) Frequent recombination events generate diversity within the multi-copy variant antigen gene families of Plasmodium falciparum. International Journal for Parasitology 38: 1099-1109 doi:10.1016/j.ijpara.2008.01.010.
12. Atkinson HJ, Morris JH, Ferrin TE, Babbitt PC, (2009) Using Sequence Similarity Networks for Visualization of Relationships Across Diverse Protein Superfamilies. PLoS ONE 4: e4345 doi:10.1371/journal.pone.0004345.t002.
13. Bull PC, Buckee CO, Kyes S, Kortok MM, Thathy V, et al. (2008) Plasmodium falciparumantigenic variation. Mapping mosaic vargene sequences onto a network of shared, highly polymorphic sequence blocks. Molecular Microbiology 68: 1519-1534 doi:10.1111/j.1365-2958.2008.06248.x.
14. Freitas-Junior LH, Bottius E, Pirrit LA, Deitsch KW, Scheidig C, et al. (2000) Frequent ectopic recombination of virulence factor genes in telomeric chromosome clusters of P. falciparum. Nature 407: 1018-1022 doi:10.1038/35039531.
15. Barry AE, Leliwa-Sytek A, Tavul L, Imrie H, Migot-Nabias F, et al. (2007) Population Genomics of the Immune Evasion (var) Genes of Plasmodium falciparum. PLoS Pathog 3: e34 doi:10.1371/journal.ppat.0030034.st002.
16. Gupta S, Snow RW, Donnelly CA, Marsh K, Newbold C, (1999) Immunity to non-cerebral severe malaria is acquired after one or two infections. Nature medicine 5: 340-343.
17. Bockhorst J, Lu F, Janes JH, Keebler J, Gamain B, et al. (2007) Structural polymorphism and diversifying selection on the pregnancy malaria vaccine candidate VAR2CSA. Molecular and Biochemical Parasitology 155: 103-112 doi:10.1016/j.molbiopara.2007.06.007.
18. Rask TS, Hansen DA, Theander TG, Gorm Pedersen A, Lavstsen T, (2010) Plasmodium falciparum Erythrocyte Membrane Protein 1 Diversity in Seven Genomes - Divide and Conquer. PLoS Comput Biol 6: e1000933 Available: http://dx.plos.org/10.1371/journal.pcbi.1000933.
19. Kraemer SM, Smith JD, (2006) A family affair: var genes, PfEMP1 binding, and malaria disease. Current Opinion in Microbiology 9: 374-380 doi:10.1016/j.mib.2006.06.006.
20. Trimnell AR, Kraemer SM, Mukherjee S, Phippard DJ, Janes JH, et al. (2006) Global genetic diversity and evolution of var genes associated with placental and severe childhood malaria{star, open}. Molecular and Biochemical Parasitology 148: 169-180 doi:10.1016/j.molbiopara.2006.03.012.
21. Awadalla P, (2003) The evolutionary genomics of pathogen recombination. Nat Rev Genet 4: 50-60 doi:10.1038/nrg964.
22. Apeltsin L, Morris JH, Babbitt PC, Ferrin TE, (2011) Improving the quality of protein similarity network clustering algorithms using the network edge weight distribution. Bioinformatics 27: 326-333.
23. Bockhorst J, Jojic N (2007) Discovering Patterns in Biological Sequences by Optimal Segmentation. In: Proceedings of the 23rd International Conference on Uncertainty in Artificial Intelligence; July 19-22, 2007; Vancouver, Canada. Available: http://uai.sis.pitt.edu/displayArticleDetails.jsp?mmnu=2&smnu=2&article_id=1669&author_id=1517.
24. Newman M (2010) Networks: an introduction. New York: Oxford University Press.
25. Alvarez-Ponce D, Lopez P, Bapteste E, McInerney JO, (2013) Gene similarity networks provide tools for understanding eukaryote origins and evolution. Proceedings of the National Academy of Sciences 110 (17) (): E1594-E1603.
26. Kosakovsky Pond SL, (2006) Automated Phylogenetic Detection of Recombination Using a Genetic Algorithm. Molecular Biology and Evolution 23: 1891-1901 doi:10.1093/molbev/msl051.
27. Huson DH, Scornavacca C, (2011) A Survey of Combinatorial Methods for Phylogenetic Networks. Genome Biology and Evolution 3: 23-35 doi:10.1093/gbe/evq077.
28. Song YS, Hein J, (2005) Constructing minimal ancestral recombination graphs. Journal of Computational Biology 12: 147-169.
29. Halary S, Leigh JW, Cheaib B, Lopez P, Bapteste E, (2010) Network analyses structure genetic diversity in independent genetic worlds. Proceedings of the National Academy of Sciences 107: 127-132 doi:10.1073/pnas.0908978107.
30. Fondi M, Fani R, (2010) The horizontal flow of the plasmid resistome: clues from inter-generic similarity networks. Environmental Microbiology 12: 3228-3242 doi:10.1111/j.1462-2920.2010.02295.x.
31. Dagan T, Artzy-Randrup Y, Martin W, (2008) Modular networks and cumulative impact of lateral transfer in prokaryote genome evolution. Proceedings of the National Academy of Sciences 105: 10039-10044.
32. Bapteste E, Lopez P, Bouchard F, Baquero F, McInerney JO, et al. (2012) Evolutionary analyses of non-genealogical bonds produced by introgressive descent. Proceedings of the National Academy of Sciences 109: 18266-18272 doi:10.1073/pnas.1206541109/-/DCSupplemental/pnas.201206541SI.pdf.
33. Smith JD, Subramanian G, Gamain B, Baruch DI, Miller LH, (2000) Classification of adhesive domains in the Plasmodium falciparum erythrocyte membrane protein 1 family. Molecular and Biochemical Parasitology 110: 293-310.
34. Su X-Z, Heatwole VM, Wertheimer SP, Guinet F, Herrfeldt JA, et al. (1995) The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of plasmodium falciparum-infected erythrocytes. Cell 82: 89-100.
35. Gardner MJ, Hall N, Fung E, White O, Berriman M, et al. (2002) Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419: 498-511.
36. Kraemer SM, Kyes SA, Aggarwal G, Springer AL, Nelson SO, et al. (2007) Patterns of gene recombination shape var gene repertoires in Plasmodium falciparum: comparisons of geographically diverse isolates. BMC Genomics 8: 45.
37. Edgar RC, (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research 32: 1792-1797 doi:10.1093/nar/gkh340.
38. Castresana J, (2000) Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17: 540-52.
39. Karrer B, Newman M, (2011) Stochastic blockmodels and community structure in networks. Phys Rev E 83: 016107 doi:10.1103/PhysRevE.83.016107.
40. Meilǎ M (2005) Comparing clusterings: an axiomatic view: Proceeding ICML '05 Proceedings of the 22nd international conference on Machine learning: 577-584.
41. Lavstsen T, Salanti A, Jensen ATR, Arnot DE, Theander TG, (2003) Sub-grouping of Plasmodium falciparum 3D7 var genes based on sequence analysis of coding and non-coding regions. Malar J 2: 27.
42. Buckee CO, Recker M, (2012) Evolution of the Multi-Domain Structures of Virulence Genes in the Human Malaria Parasite, Plasmodium falciparum. PLoS Comput Biol 8: e1002451 doi:10.1371/journal.pcbi.1002451.g006.
43. Kraemer SM, Smith JD, (2003) Evidence for the importance of genetic structuring to the structural and functional specialization of the Plasmodium falciparum var gene family. Molecular Microbiology 50: 1527-1538 doi:10.1046/j.1365-2958.2003.03814.x.
44. Bopp SER, Manary MJ, Bright AT, Johnston GL, Dharia NV, et al. (2013) Mitotic Evolution of Plasmodium falciparum Shows a Stable Core Genome but Recombination in Antigen Families. PLoS Genet 9: e1003293 doi:10.1371/journal.pgen.1003293.s008.
45. Newman M, (2002) Assortative Mixing in Networks. Phys Rev Lett 89: 208701 doi:10.1103/PhysRevLett.89.208701.
46. Warimwe GM, Keane TM, Fegan G, Musyoki JN, Newton CRJC, et al. (2009) Plasmodium falciparum var gene expression is modified by host immunity. Proceedings of the National Academy of Sciences 106: 21801-21806 Available: http://www.pnas.org/content/106/51/21801.full.pdfhtml.
47. Bull PC, Kyes S, Buckee CO, Montgomery J, Kortok MM, et al. (2007) An approach to classifying sequence tags sampled from Plasmodium falciparum var genes. Molecular and Biochemical Parasitology 154: 98-102 doi:10.1016/j.molbiopara.2007.03.011.
48. Warimwe GM, Fegan G, Musyoki JN, Newton CRJC, Opiyo M, et al. (2012) Prognostic Indicators of Life-Threatening Malaria Are Associated with Distinct Parasite Variant Antigen Profiles. Science Translational Medicine 4: 129ra45-129ra45 Available: http://www.translationalmedicine.org/content/4/129/129ra45.short.
49. ORGEL LE, (1963) The maintenance of the accuracy of protein synthesis and its relevance to ageing. Proceedings of the National Academy of Sciences 49: 517-521.
50. Mucha PJ, Richardson T, Macon K, Porter MA, Onnela JP, (2010) Community Structure in Time-Dependent, Multiscale, and Multiplex Networks. Science 328: 876-878 doi:10.1126/science.1184819.