Malarial parasite diversity in chimpanzees: The value of comparative approaches to ascertain the evolution of Plasmodium falciparum antigens

Malaria Journal

Volumn 12, Issue 1, 2013, Pages

  Pacheco, M Andreína ^a   Cranfield, Michael ^b   Cameron, Kenneth ^c   Escalante, Ananias A ^a,d  

^a ARIZONA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c Wildlife Health Program   (Congo)

^d ARIZONA STATE UNIVERSITY   (United States)

Author keywords

Antigen; Chimpanzee; Circumsporozoite protein; Co evolution; Dihydrofolate reductase thymidylate synthase; Malaria; Merozoite surface protein 2; Mitochondrion genome; Pan troglodytes; Parasite evolution; Plasmodium; Plasmodium falciparum; Plasmodium phylogeny; Var2CSA

Indexed keywords

CHLOROQUINE; CIRCUMSPOROZOITE PROTEIN; DIHYDROFOLATE REDUCTASE; MEROZOITE SURFACE PROTEIN 2; PARASITE ANTIGEN; PLASMODIUM FALCIPARUM ANTIGEN; THYMIDYLATE SYNTHASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHIMPANZEE; CLADISTICS; CONTROLLED STUDY; FEMALE; GENETIC POLYMORPHISM; GENETIC VARIABILITY; HUMAN; MALE; MEDICAL EXAMINATION; MICROBIAL DIVERSITY; MITOCHONDRIAL GENOME; MOLECULAR CLOCK; MONOPHYLY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PLASMODIUM FALCIPARUM; SPECIES DIVERSITY; TANDEM REPEAT;

ANIMALS; CLUSTER ANALYSIS; DNA, MITOCHONDRIAL; DNA, PROTOZOAN; EVOLUTION, MOLECULAR; FEMALE; GENETIC VARIATION; HUMANS; MALARIA; MALE; MOLECULAR SEQUENCE DATA; PAN TROGLODYTES; PHYLOGENY; PLASMODIUM; POLYMERASE CHAIN REACTION; PRIMATE DISEASES; SEQUENCE ANALYSIS, DNA;

EID: 84883881064     PISSN: None     EISSN: 14752875     Source Type: Journal    
DOI: 10.1186/1475-2875-12-328     Document Type: Article

References (80)

1. Worldwide incidence of malaria in 2009: estimates, time trends, and a critique of methods. Cibulskis RE, Aregawi M, Williams R, Otten M, Dye C, PLoS Med 2011 8 1001142
2. WHO, World malaria report 2011 Geneva: World Health Organization http://www.who.int/malaria/world-malaria-report-2011/ (accessed July 24, 2012)
3. Coatney RG, Collins WE, Warren M, Contacos PG, The primate malaria Washington DC: US Government Printing Office 1971
4. Phylogeny of the malarial genus Plasmodium derived from rRNA gene sequences. Escalante AA, Ayala FJ, Proc Natl Acad Sci USA 1994 91 11373 11377 (Pubitemid 24356346)
5. The evolution of primate malaria parasites based on the gene encoding cytochrome b from the linear mitochondrial genome. Escalante AA, Freeland DE, Collins WE, Lal AA, Proc Nat Acad Sci USA 1998 95 8124 8129 (Pubitemid 28326077)
6. A monkey's tale: the origin of Plasmodium vivax as a human malaria parasite. Escalante AA, Cornejo OE, Freeland DE, Poe AC, Durrego E, Collins WE, Lal AA, Proc Natl Acad Sci USA 2005 102 1980 1985 (Pubitemid 40261998)
7. The origin of malignant malaria. Rich SM, Leendertz FH, Xu G, LeBreton M, Djoko CF, Aminake MN, Takang EE, Diffo JL, Pike BL, Rosenthal BM, Formenty P, Boesch C, Ayala FJ, Wolfe ND, Proc Natl Acad Sci USA 2009 106 14902 14907
8. African apes as reservoirs of Plasmodium falciparum and the origin and diversification of the Laverania subgenus. Duval L, Fourment M, Nerrienet E, Rousset D, Sadeuh SA, Goodman SM, Andriaholinirina NV, Randrianarivelojosia M, Paul RE, Robert V, Ayala FJ, Ariey F, Proc Natl Acad Sci USA 2010 107 10561 10566
9. On the diversity of malaria parasites in African apes and the origin of Plasmodium falciparum from Bonobos. Krief S, Escalante AA, Pacheco MA, Mugisha L, André C, Halbwax M, Fischer A, Krief JM, Kasenene JM, Crandfield M, Cornejo OE, Chavatte JM, Lin C, Letourneur F, Grüner AC, McCutchan TF, Rénia L, Snounou G, PLoS Pathog 2010 6 1000765
10. Origin of the human malaria parasite Plasmodium falciparum in gorillas. Liu W, Li Y, Learn GH, Rudicell RS, Robertson JD, Keele BF, Ndjango JB, Sanz CM, Morgan DB, Locatelli S, Gonder MK, Kranzusch PJ, Walsh PD, Delaporte E, Mpoudi-Ngole E, Georgiev AV, Muller MN, Shaw GM, Peeters M, Sharp PM, Rayner JC, Hahn BH, Nature 2010 467 420 425
11. A fresh look at the origin of Plasmodium falciparum, the most malignant malaria agent. Prugnolle F, Durand P, Ollomo B, Duval L, Ariey F, Arnathau C, Gonzalez JP, Leroy E, Renaud F, PLoS Pathog 2011 7 1001283
12. Unresolved direction of host transfer of Plasmodium vivax v. P. simium and P. malariae v. P. brasilianum. Tazi L, Ayala FJ, Infect Genet Evol 2011 11 209 221
13. The origin of malarial parasites in orangutans. Pacheco MA, Reid MJ, Schillaci MA, Lowenberger CA, Galdikas BM, Jones-Engel L, Escalante AA, PLoS One 2012 7 34990
14. A large focus of naturally acquired Plasmodium knowlesi infections in human beings. Singh B, Kim Sung L, Matusop A, Radhakrishnan A, Shamsul SS, Cox-Singh J, Thomas A, Conway DJ, Lancet 2004 363 1017 1024 (Pubitemid 38410774)
15. Plasmodium knowlesi: reservoir hosts and tracking the emergence in humans and macaques. Lee KS, Divis PC, Zakaria SK, Matusop A, Julin RA, Conway DJ, Cox-Singh J, Singh B, PLoS Pathog 2011 7 1002015
16. Evolutionary origin of human and primate malarias: evidence from the circumsporozoite protein gene. Escalante AA, Barrio E, Ayala FJ, Mol Biol Evol 1995 12 616 626
17. Wild chimpanzees infected with 5 Plasmodium species. Kaiser M, Löwa A, Ulrich M, Ellerbrok H, Goffe AS, Blasse A, Zommers Z, Couacy-Hymann E, Babweteera F, Zuberbühler K, Metzger S, Geidel S, Boesch C, Gillespie TR, Leendertz FH, Emerg Infect Dis 2010 16 1956 1959
18. Plasmodium falciparum-like parasites infecting wild apes in southern Cameroon do not represent a recurrent source of human malaria. Sundararaman SA, Liu W, Keele BF, Learn GH, Bittinger K, Mouacha F, Ahuka-Mundeke S, Manske M, Sherrill-Mix S, Li Y, Malenke JA, Delaporte E, Laurent C, Mpoudi Ngole E, Kwiatkowski DP, Shaw GM, Rayner JC, Peeters M, Sharp PM, Bushman FD, Hahn BH, Proc Natl Acad Sci USA 2013 110 7020 7025
19. Genome variation and evolution of the malaria parasite Plasmodium falciparum. Jeffares DC, Pain A, Berry A, Cox AV, Stalker J, Ingle CE, Thomas A, Quail MA, Siebenthall K, Uhlemann AC, Kyes S, Krishna S, Newbold C, Dermitzakis ET, Berriman M, Nat Genet 2007 39 120 125 (Pubitemid 46026511)
20. Gene-specific signatures of elevated non-synonymous substitution rates correlate poorly across the Plasmodium genus. Weedall GD, Polley SD, Conway DJ, PLoS One 2008 3 2281
21. A new malaria agent in African hominids. Ollomo B, Durand P, Prugnolle F, Douzery E, Arnathau C, Nkoghe D, Leroy E, Renaud F, PLoS Pathog 2009 5 1000446
22. A plethora of Plasmodium species in wild apes: a source of human infection? Rayner JC, Liu W, Peeters M, Sharp PM, Hahn BH, Trends Parasitol 2011 27 222 229
23. Malaria: host range, diversity and speciation. Escalante AA, Ayala FJ, Evolution of virulence in eukaryotic microbes New Jersey: Wiley-Blackwell, Sibley LD, Howlett BJ, Heitman J, 2012 93 110
24. Genetic polymorphism and natural selection in the malaria parasite Plasmodium falciparum. Escalante AA, Lal AA, Ayala FJ, Genetics 1998 149 189 202
25. Timing the origin of human malarias: the lemur puzzle. Pacheco MA, Battistuzzi FU, Junge RE, Cornejo OE, Williams CV, Landau I, Rabetafika L, Snounou G, Jones-Engel L, Escalante AA, BMC Evol Biol 2011 11 299
26. A simple, fast and accurate algorithm to estimate large phylogenies by maximum likelihood. Guindon S, Gascuel O, Syst Biol 2003 52 696 704 (Pubitemid 37365050)
27. Bayesian phylogenetic inference under mixed models. Ronquist F, Huelsenbeck JP, MrBayes 3, Bioinformatics 2003 19 1572 1574 (Pubitemid 37038874)
28. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S, Mol Biol Evol 2011 28 2731 2739
29. Drummond AJ, Rambaut A, BEAST version 1.3 [computer program] 2003 Available at http://beast.bio.ed.ac.uk/Main-Page
30. Asynchronous colonization of Madagascar by the four endemic clades of primates, tenrecs, carnivores, and rodents as inferred from nuclear genes. Poux C, Madsen O, Marquard E, Vieites DR, De Jong WW, Vences M, Syst Biol 2005 54 719 730 (Pubitemid 43142291)
31. Mammalian biodiversity on Madagascar controlled by ocean currents. Ali JR, Huber M, Nature 2010 463 653 656
32. Fossil macaques, phyletic relationships and a scenario of deployment. Delson E, The macaques-studies in ecology, behavior and evolution New York: Van Nostrand Reinhold Co, Lindburg DG, 1980 10 29
33. Host switch leads to emergence of Plasmodium vivax malaria in humans. Mu J, Joy DA, Duan J, Huang Y, Carlton J, Walker J, Barnwell J, Beerli P, Charleston MA, Pybus OG, Su XZ, Mol Biol Evol 2005 22 1686 1693 (Pubitemid 41373579)
34. Big bang in the evolution of extant malaria parasites. Hayakawa T, Culleton R, Otani H, Horii T, Tanabe K, Mol Biol Evol 2008 25 2233 2239
35. Paleontological evidence to date the tree of life. Benton MJ, Donoghue PC, Mol Biol Evol 2007 24 26 53 (Pubitemid 46026279)
36. Application of a molecular marker for surveillance of chloroquine-resistant falciparum malaria. Djimde A, Doumbo OK, Steketee RW, Plowe CV, Lancet 2001 358 890 891 (Pubitemid 32900575)
37. An immunologically cryptic epitope of Plasmodium falciparum circumsporozoite protein facilitates liver cell recognition and induces protective antibodies that block liver cell invasion. Rathore D, Nagarkatti R, Jani D, Chattopadhyay R, de la Vega P, Kumar S, McCutchan TF, J Biol Chem 2005 280 20524 20529 (Pubitemid 40776753)
38. The Plasmodium circunsporozoite protein is proteolytically processed during cell invasion. Coppi A, Pinzon-Ortiz C, Hutter C, Sinnis P, J Exp Med 2005 201 27 33 (Pubitemid 40130080)
39. A CD4(+) T-cell immune response to a conserved epitope in the circumsporozoite protein correlates with protection from natural Plasmodium falciparum infection and disease. Reece WH, Pinder M, Gothard PK, Milligan P, Bojang K, Doherty T, Plebanski M, Akinwunmi P, Everaere S, Watkins KR, Voss G, Tornieporth N, Alloueche A, Greenwood BM, Kester KE, McAdam KP, Cohen J, Hill AV, Nat Med 2004 10 406 410 (Pubitemid 38508520)
40. Plasmodium falciparum: extensive polymorphism in merozoite surface antigen 2 alleles in an area with endemic malaria in Papua New Guinea. Felger I, Tavul L, Kabintik S, Marshall V, Genton B, Alpers M, Beck HP, Exp Parasitol 1994 79 106 116 (Pubitemid 24277222)
41. Antigenic characterization of an intrinsically unstructured protein, Plasmodium falciparum merozoite surface protein 2. Adda CG, MacRaild CA, Reiling L, Wycherley K, Boyle MJ, Kienzle V, Masendycz P, Foley M, Beeson JG, Norton RS, Anders RF, Infect Immun 2012 80 4177 4185
42. Plasmodium falciparum: worldwide sequence diversity and evolution of the malaria vaccine candidate merozoite surface protein-2 (MSP-2). Ferreira MU, Hartl DL, Exp Parasitol 2007 115 32 40
43. Positive selection and interallelic recombination at the merozoite surface antigen-1 (MSA-1) locus of Plasmodium falciparum. Hughes AL, Mol Biol Evol 1992 9 381 393
44. Population structure and recent evolution of Plasmodium falciparum. Rich SM, Ayala FJ, Proc Natl Acad Sci USA 2000 97 6994 7001 (Pubitemid 30431407)
45. A single member of the Plasmodium falciparum var multigene family determines cytoadhesion to the placental receptor chondroitin sulphate A. Viebig NK, Gamain B, Scheidig C, Lépolard C, Przyborski J, Lanzer M, Gysin J, Scherf A, EMBO Rep 2005 6 775 781 (Pubitemid 43108701)
46. Broad analysis reveals a consistent pattern of var gene transcription in Plasmodium falciparum repeatedly selected for a defined adhesion phenotype. Duffy MF, Byrne TJ, Elliott SR, Wilson DW, Rogerson SJ, Beeson JG, Noviyanti R, Brown GV, Mol Microbiol 2005 56 774 788 (Pubitemid 40562369)
47. Adherence of Plasmodium falciparum to chondroitin sulfate A in the human placenta. Fried M, Duffy PE, Science 1996 272 1502 15044
48. Structural polymorphism and diversifying selection on the pregnancy malaria vaccine candidate VAR2CSA. Bockhorst J, Lu F, Janes JH, Keebler J, Gamain B, Awadalla P, Su XZ, Samudrala R, Jojic N, Smith JD, Mol Biochem Parasitol 2007 155 103 112 (Pubitemid 47238448)
49. Plasmodium falciparum erythrocyte membrane protein 1 diversity in seven genomes-divide and conquer. Rask TS, Hansen DA, Theander TG, Gorm Pedersen A, Lavstsen T, PLoS Comput Biol 2010 6 1000933
50. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Nei M, Gojobori T, Mol Biol Evol 1986 3 418 426 (Pubitemid 16010523)
51. Nei M, Kumar S, Molecular evolution and phylogenetics New York: Oxford University press 2000
52. Garnham PCC, Malaria parasites and other haemosporidia Oxford: Blackwell Scientific Publications 1966
53. Molecular evolution and phylogenetics of rodent malaria parasites. Ramiro RS, Reece SE, Obbard DJ, BMC Evol Biol 2012 12 219
54. Relaxed phylogenetics and dating with confidence. Drummond AJ, Ho SY, Phillips MJ, Rambaut A, PLoS Biol 2006 4 88
55. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. Hasegawa M, Kishino H, Yano T, J Mol Evol 1985 22 160 174 (Pubitemid 16227864)
56. Molecular estimates of primate divergences and new hypotheses for primate dispersal and the origin of modern humans. Arnason U, Gullberg A, Burguete AS, Janke A, Hereditas 2000 133 217 228 (Pubitemid 32514514)
57. Early origin and recent expansion of Plasmodium falciparum. Joy DA, Feng X, Mu J, Furuya T, Chotivanich K, Krettli AU, Ho M, Wang A, White NJ, Suh E, Science 2003 300 318 321 (Pubitemid 36433721)
58. The primary structure of the circumsporozoite protein of Plasmodium atheruri, a malaria parasite of the African porcupine Atherurus africanus. Costa FT, Snounou G, Letourneur F, Lebrun N, Landau I, Rénia L, Mol Biochem Parasitol 2001 114 125 127 (Pubitemid 32453223)
59. Molecular mechanism of host specificity in Plasmodium falciparum infection: role of circumsporozoite protein. Rathore D, Hrstka SC, Sacci JB Jr, De la Vega P, Linhardt RJ, Kumar S, McCutchan TF, J Biol Chem 2003 278 40905 40910 (Pubitemid 37280910)
60. Evolutionary dynamics of the immunodominant repeats of the Plasmodium vivax malaria-vaccine candidate circumsporozoite protein (CSP). Patil A, Orjuela-Sánchez P, Da Silva-Nunes M, Ferreira MU, Infect Genet Evol 2010 10 298 303
61. The circumsporozoite gene of the Plasmodium cynomolgi complex. Galinski MR, Arnot DE, Cochrane AH, Barnwell JW, Nussenzweig RS, Enea V, Cell 1987 48 311 319
62. A study of genetic diversity in the gene encoding the circumsporozoite protein (CSP) of Plasmodium falciparum from different transmission areas-XVI: asembo bay cohort project. Escalante AA, Grebert HM, Isea R, Goldman IF, Basco L, Magris M, Biswas S, Kariuki S, Lal AA, Mol Biochem Parasitol 2002 125 83 90 (Pubitemid 35449248)
63. A binding site for highly sulfated heparan sulfate is identified in the N terminus of the circumsporozoite protein: significance for malarial sporozoite attachment to hepatocytes. Ancsin JB, Kisilevsky R, J Biol Chem 2004 279 21824 21832 (Pubitemid 38679371)
64. Unexpected fold in the circumsporozoite protein target of malaria vaccines. Doud MB, Koksal AC, Mi LZ, Song G, Lu C, Springer TA, Proc Natl Acad Sci USA 2012 109 7817 7822
65. SignalP 4.0: discriminating signal peptides from transmembrane regions. Petersen TN, Brunak S, Von Heijne G, Nielsen H, Nat Methods 2011 8 785 786
66. The malaria circumsporozoite protein has two functional domains, each with distinct roles as sporozoites journey from mosquito to mammalian host. Coppi A, Natarajan R, Pradel G, Bennett BL, James ER, Roggero MA, Corradin G, Persson C, Tewari R, Sinnis P, J Exp Med 2011 208 341 356
67. Comparison of circumsporozoite proteins from avian and mammalian malarias: biological and phylogenetic implications. McCutchan TF, Kissinger JC, Touray MG, Rogers MJ, Li J, Sullivan M, Braga EM, Krettli AU, Miller LH, Proc Natl Acad Sci USA 1996 93 11889 11894 (Pubitemid 26347219)
68. Genomics, population genetics and evolutionary history of Plasmodium vivax. Carlton JM, Das A, Escalante AA, Adv Parasitol 2013 81 203 222
69. Structural and antigenic polymorphism of the 35-to 48-kilodalton merozoite surface antigen (MSA-2) of the malaria parasite Plasmodium falciparum. Fenton B, Clark JT, Khan CM, Robinson JV, Walliker D, Ridley R, Scaife JG, McBride JS, Mol Cell Biol 1991 11 963 971 (Pubitemid 21895446)
70. Merozoite surface protein 2 of Plasmodium reichenowi is a unique mosaic of Plasmodium falciparum allelic forms and species-specific elements. Dubbeld MA, Kocken CH, Thomas AW, Mol Biochem Parasitol 1998 92 187 192
71. A cautionary note concerning Plasmodium in apes. Valkiunas G, Ashford RW, Bensch S, Killick-Kendrick R, Perkins S, Trends Parasitol 2011 27 231 232
72. Species concepts and species delimitation. De Queiroz K, Syst Biol 2007 56 879 886 (Pubitemid 350129638)
73. Studies on malaria in chimpanzees: VI laverania falciparum. Bray RS, Am J Trop Med Hyg 1958 7 20 24
74. Misclassification of Plasmodium infections by conventional microscopy and the impact of remedial training on the proficiency of laboratory technicians in species identification. Obare P, Ogutu B, Adams M, Odera JS, Lilley K, Dosoo D, Adhiambo C, Owusu-Agyei S, Binka F, Wanja E, Johnson J, Malar J 2013 12 113
75. A restriction enzyme-based assay to distinguish between avian hemosporidians. Beadell JS, Fleischer RC, J Parasitol 2005 91 683 685 (Pubitemid 40993462)
76. Identification of Plasmodium (Haemamoeba) lutzi (Lucena, 1939) from Turdus fuscater (great thrush) in Colombia. Mantilla Granados JS, Matta NE, Pacheco MA, Escalante A, Gonzalez AD, Moncada LI, J Parasitol 2013 99 662 668
77. Two nonrecombining sympatric forms of the human malaria parasite Plasmodium ovale occur globally. Sutherland CJ, Tanomsing N, Nolder D, Oguike M, Jennison C, Pukrittayakamee S, Dolecek C, Hien TT, Do Rosário VE, Arez AP, Pinto J, Michon P, Escalante AA, Nosten F, Burke M, Lee R, Blaze M, Otto TD, Barnwell JW, Pain A, Williams J, White NJ, Day NP, Snounou G, Lockhart PJ, Chiodini PL, Imwong M, Polley SD, J Infect Dis 2010 201 1544 1550
78. Evolution of human-chimpanzee differences in malaria susceptibility: relationship to human genetic loss of N-glycolylneuraminic acid. Martin MJ, Rayner JC, Gagneux P, Barnwell JW, Varki A, Proc Natl Acad Sci USA 2005 102 12819 12824 (Pubitemid 41279449)
79. Low-complexity regions in Plasmodium falciparum: missing links in the evolution of an extreme genome. Zilversmit MM, Volkman SK, DePristo MA, Wirth DF, Awadalla P, Hartl DL, Mol Biol Evol 2010 27 2198 2209
80. A recombinant blood-stage malaria vaccine reduces Plasmodium falciparum density and exerts selective pressure on parasite populations in a phase 1-2b trial in Papua New Guinea. Genton B, Betuela I, Felger I, Al-Yaman F, Anders RF, Saul A, Rare L, Baisor M, Lorry K, Brown GV, Pye D, Irving DO, Smith TA, Beck HP, Alpers MP, J Infect Dis 2002 185 820 827 (Pubitemid 34226210)