Strain-specific immunity may drive adaptive polymorphism in the merozoite surface protein 1 of the rodent malaria parasite Plasmodium chabaudi

Infection, Genetics and Evolution

Volumn 9, Issue 2, 2009, Pages 248-255

  Cheesman, Sandra ^a   Tanabe, Kazuyuki ^b   Sawai, Hiromi ^b   O'Mahony, Elaine ^a   Carter, Richard ^a  

^a Ashworth Laboratories   (United Kingdom)

^b OSAKA UNIVERSITY   (Japan)

Author keywords

Malaria; Merozoite surface protein 1; Plasmodium; Strain specific protective immunity

Indexed keywords

MEROZOITE SURFACE PROTEIN 1;

3' UNTRANSLATED REGION; ADAPTIVE IMMUNITY; ALLELE; AMINO ACID SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; GENE SEQUENCE; GENETIC DIFFERENCE; GENETIC POLYMORPHISM; GENETIC STRAIN; GENETIC VARIABILITY; MALARIA; MEROZOITE; NONHUMAN; NUCLEOTIDE SEQUENCE; PLASMODIUM CHABAUDI; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; RAT; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; STRAIN DIFFERENCE;

ANIMALS; GENES, MITOCHONDRIAL; GENES, PROTOZOAN; MALARIA; MEROZOITE SURFACE PROTEIN 1; MICE; PHYLOGENY; PLASMODIUM CHABAUDI; POLYMORPHISM, GENETIC; RATS; SELECTION (GENETICS); SEQUENCE HOMOLOGY, AMINO ACID;

MUS; PLASMODIUM CHABAUDI; PLASMODIUM CHABAUDI CHABAUDI; PLASMODIUM FALCIPARUM; RODENTIA;

EID: 59749084371     PISSN: 15671348     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.meegid.2008.12.002     Document Type: Article

References (47)

1. Beale G.H., Carter R., and Walliker D. Genetics. In: Killick-Kendrick R., and Peters W. (Eds). Rodent Malaria (1978), Academic Press, London 213-245
2. Benjamin P.A., Ling I.T., Clottey G., Valero L.M., Ogun S.A., Fleck S.L., Walliker D., Morgan W.D., Birdsall B., Feeney J., and Holder A.A. Antigenic and sequence diversity at the C-terminus of the merozoite surface protein-1 from rodent malaria isolates, and the binding of protective monoclonal antibodies. Mol. Biochem. Parasitol. 104 (1999) 147-156
3. Blackman M.J., Heidrich H.G., Donachie S., McBride J.S., and Holder A.A. A single fragment of a malaria merozoite surface protein remains on the parasite during red cell invasion and is the target of invasion-inhibiting antibodies. J. Exp. Med. 172 (1990) 379-382
4. Carter R., and Walliker D. New observations on the malaria parasites of rodents of the Central African Republic-Plasmodium vinckei petteri subsp. nov. and Plasmodium chabaudi. Landau, 1965. Ann. Trop. Med. Parasitol. 69 (1975) 187-196
5. Carter R., and Walliker D. Malaria parasites of rodents of the Congo (Brazzaville): Plasmodium chabaudi adami subsp. nov. and Plasmodium vinckei lentum Landau, Michel, Adam and Boulard, 1970. Ann. Parasitol. Hum. Comp. 51 (1976) 637-646
6. Carter R., Hunt P., and Cheesman S. Linkage Group Selection-a fast approach to the genetic analysis of malaria parasites. Int. J. Parasitol. 37 (2007) 285-293
7. Cavanagh D.R., Elhassan I.M., Roper C., Robinson V.J., Giha H., Holder A.A., Hviid L., Theander T.G., Arnot D.E., and McBride J.S. A longitudinal study of type-specific antibody responses to Plasmodium falciparum merozoite surface protein 1 in an area of unstable malaria in Sudan. J. Immunol. 161 (1998) 347-359
8. Cavanagh D.R., and McBride J.S. Antigenicity of recombinant proteins derived from Plasmodium falciparum merozoite surface protein 1. Mol. Biol. Parasitol. 85 (1997) 197-211
9. Cheesman S., Raza A., and Carter R. Mixed strain infections and strain-specific protective immunity in the rodent malaria parasite Plasmodium chabaudi chabaudi in mice. Infect. Immun. 74 (2006) 2996-3001
10. Conway D.J., Cavanagh D.R., Tanabe K., Roper C., Mikes Z.S., Sakihama N., Bojang K.A., Oduola A.M., Kremsner P.G., Arnot D.E., Greenwood B.M., and McBride J.S. A principal target of human immunity to malaria identified by molecular population genetic and immunological analyses. Nat. Med. 6 (2000) 689-692
11. Culleton R., Martinelli A., Hunt P., and Carter R. Linkage group selection: rapid gene discovery in malaria parasites. Genome Res. 15 (2005) 92-97
12. Deleersnijder W., Hendrix D., Bendahman N., Hanegreefs J., Brijs L., Hamers-Casterman C., and Hamers R. Molecular cloning and sequence analysis of the gene encoding the major merozoite surface antigen of Plasmodium chabaudi chabaudi IP-PC1. Mol. Biochem. Parasitol. 43 (1990) 231-244
13. Egan A.F., Chappel J.A., Burghaus P.A., Morris J.S., McBride J.S., Holder A.A., Kaslow D.C., and Riley E.M. Serum antibodies from malaria-exposed people recognize conserved epitopes formed by the two epidermal growth factor motifs of MSP1 (19), the carboxy-terminal fragment of the major merozoite surface protein of Plasmodium falciparum. Infect. Immun. 63 (1995) 456-466
14. Egan A.F., Morris J., Barnish G., Allen S., Greenwood B., Kaslow D.C., Holder A.A., and Riley E.M. Clinical immunity to Plasmodium falciparum malaria is associated with serum antibodies to the 19 kDa C terminal fragment of the merozoite surface antigen, PfMSP-1. J. Infect. Dis. 173 (1996) 765-769
15. Eisen D., Billman-Jacobe H., Marshall V.F., Fryauff D., and Coppel R.L. Temporal variation of the merozoite surface protein-2 gene of Plasmodium falciparum. Infect. Immun. 66 (1998) 239-246
16. Eisen D.P., Saul A., Fryauff D.J., Reeder J.C., and Coppel R.L. Alterations in Plasmodium falciparum genotypes during sequential infections suggest the presence of strain specific immunity. Am. J. Trop. Med. Hyg. 67 (2002) 8-16
17. Holder A.A., and Freeman R.R. Biosynthesis and processing of a Plasmodium falciparum schizont antigen recognised by immune serum and a monoclonal antibody. J. Exp. Med. 156 (1982) 1528-1538
18. Hughes A.L. Positive selection and interallelic recombination at the merozoite surface antigen-1 (MSA-1) locus of Plasmodium falciparum. Mol. Biol. Evol. 9 (1992) 381-393
19. Jarra W., and Brown K.N. Protective immunity to malaria: studies with cloned lines of rodent malaria in CBA/Ca mice. IV. The specificity of mechanisms resulting in crisis and resolution of the primary acute phase parasitaemia of Plasmodium chabaudi chabaudi and P. yoelii yoelii. Parasite Immunol. 11 (1989) 1-13
20. Jennings G., Toebe C.S., van Belkum A., and Wiser M.F. The complete sequence of Plasmodium berghei merozoite surface protein-1 and its inter- and intra-species variability. Mol. Biol. Parasitol. 93 (1998) 43-55
21. 19) can play a protective role against blood-stage Plasmodium falciparum infection in a malaria endemic area of Africa. J. Immunol. 173 (2004) 666-672
22. Jones T.R., Obaldia III N., Gramzinski R.A., and Hoffman S.L. Repeated infection of Aotus monkeys with Plasmodium falciparum induces protection against subsequent challenge with homologous and heterologous strains of parasite. Am. J. Trop. Med. Hyg. 62 (2000) 675-680
23. Killick-Kendrick R., and Peters W. Rodent Malaria (1978), Academic Press Inc. Ltd, London
24. Kumar S., Tamura K., and Nei M. MEGA3: integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform. 5 (2004) 150-163
25. Li W.-H. Molecular Evolution (1997), Sinauer Associates, Sunderland, MA
26. Martinelli A., Cheesman S., Hunt P., Culleton R., Raza A., Mackinnon M., and Carter R. A genetic approach to the de novo identification of targets of strain-specific immunity in malaria parasites. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 814-819
27. McDonald J.H., and Kreitman M. Adaptive protein evolution at the Adh locus in Drosophila. Nature 351 (1991) 114-116
28. McKean P.G., O'Dea K., and Brown K.N. A single amino acid determines the specificity of a monoclonal antibody which inhibits Plasmodium chabaudi AS in vivo. Mol. Biol. Parasitol. 62 (1993) 211-221
29. McKean P.G., O'Dea K., Brown, and Neil K. Nucleotide sequence analysis and epitope mapping of the merozoite surface protein 1 from Plasmodium chabaudi chabaudi AS. Mol. Biol. Parasitol. 62 (1993) 199-210
30. Nei M. Molecular Population Genetics and Evolution (1975), North-Holland, Amsterdam
31. O'Dea K.P., McKean P., Harris A., and Brown K.N. Processing of the Plasmodium chabaudi chabaudi AS merozoite surface protein 1 in vivo and in vitro. Mol. Biol. Parasitol. 72 (1995) 111-119
32. O'Donnell R.A., Saul A., Cowman A.F., and Crabb B. Functional conservation of the malaria vaccine antigen MSP-119 across distantly related Plasmodium species. Nat. Med. 6 (2000) 91-95
33. Okech B.A., Corran P.H., Todd J., Joynson-Hicks A., Uthaipibull C., Egwang T.G., Holder A.A., and Riley E.M. Fine specificity of serum antibodies to Plasmodium falciparum merozoite surface protein, PfMSP-1(19), predicts protection from malaria infection and high-density parasitemia. Infect. Immun. 72 (2004) 557-567
34. Pacheco M.A., Poe A.C., Collins W.E., Lal A.A., Tanabe K., Kariuki S.K., Udhayakumar V., and Escalante A.A. A comparative study of the genetic diversity of the 42 kDa fragment of the merozoite surface protein 1 in Plasmodium falciparum and P. vivax. Infect. Genet. Evol. 7 (2007) 180-187
35. Pattaradilokrat S., Cheesman S.J., and Carter R. Linkage group selection: towards identifying genes controlling strain-specific protective immunity in malaria. PLoS ONE 2 9 (2007) e857
36. Perkins S.L., Sarkar I.N., and Carter R. The phylogeny of rodent malaria genomes: simultaneous analysis across three genomes. Infect. Genet. Evol. 7 (2007) 74-83
37. Polley S.D., Weedall G.D., Thomas A.W., Golightly L.M., and Conway D.J. Orthologous gene sequences of merozoite surface protein 1 (MSP1) from Plasmodium reichenowi and P. gallinaceum confirm an ancient divergence of P. falciparum alleles. Mol. Biol. Parasitol. 142 (2005) 25-31
38. Renia L., Ling I.T., Marussig M., Miltgen F., Holder A.A., and Mazier D. Immunization with a recombinant C-terminal fragment of Plasmodium yoelii merozoite surface protein 1 protects mice against homologous but not heterologous P. yoelii sporozoite challenge. Infect. Immun. 65 (1997) 4419-4423
39. Riley E.M., Allen S.J., Wheeler J.G., Blackman M.J., Bennett S., Takacs B., Schönfeld H.J., Holder A.A., and Greenwood B.M. Naturally acquired cellular and humoral immune responses to the major merozoite surface antigen (PfMSP1) of Plasmodium falciparum are associated with reduced malaria morbidity. Parasite Immunol. 14 (1992) 321-337
40. Rozas J., Sanchez-DelBarrio J.C., Messeguer X., and Rozas R. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19 (2003) 2496-2497
41. Sakiham a.N., Mitamura T., Kaneko A., Horii T., and Tanabe K. Long PCR amplification of Plasmodium falciparum DNA extracted from filter paper blots. Exp. Parasitol. 97 (2001) 50-54
42. Shi Y.P., Sayed U., Qari S.H., Roberts J.M., Udhayakumar V., Oloo A.J., Hawley W.A., Kaslow D.C., Nahlen B.L., and Lal A.A. Natural immune response to the C-terminal 19-kilodalton domain of Plasmodium falciparum merozoite surface protein 1. Infect. Immun. 64 (1996) 2716-2723
43. Swofford, D.L. 1998. PAUP*. Phylogentic analysese using parsimony (* and other methods). Version 4. Sinauer Associates, Sunderland, Massachusetts. (2002. PAUP.(version 4.0b10), Sinauer Associates, Sunderland, Massachusetts).
44. Takala S.L., Coulibaly D., Thera M.A., Dicko A., Smith D.L., Guindo A.B., Kone A.K., Traore K., Ouattara A., Djimde A.A., Sehdev P.S., Lyke K.E., Diallo D.A., Doumbo O.K., and Plowe C.V. Dynamics of polymorphism in a malaria vaccine antigen at a vaccine-testing site in Mali. PloS Med. 4 (2007) e93 0523-0534
45. Tanabe K., Mackay M., Gowman M., and Scaife J.G. Allelic dimorphism in a surface antigen gene of the malaria parasite Plasmodium falciparum. J. Mol. Biol. 195 (1987) 273-287
46. Tanabe K., Sakihama N., Walliker D., Babiker H., Abdel-Muhsin A.A., Bakote'e B., Ohmae H., Arisue N., Horii T., Rooth I., Färnert A., Björkman A., and Ranford-Cartwright L. Allelic dimorphism-associated restriction of recombination in Plasmodium falciparum msp1. Gene 397 (2007) 153-160
47. Thera M.A., Doumbo O.K., Coulibaly D., Diallo D.A., Sagara I., Dicko A., Diemert D.J., Heppner Jr. D.G., Stewart V.A., Angov E., Soisson L., Leach A., Tucker K., Lyke K.E., Plowe C.V., and Mali FMP1 Working Group. Safety and allele-specific immunogenicity of a malaria vaccine in Malian adults: results of a phase I randomized trial. PLoS Clin. Trials 1 7 (2006) e34