The impact of immunization on competition within Plasmodium infections

Evolution

Volumn 62, Issue 9, 2008, Pages 2359-2371

  Grech, Katrina ^a   Chan, Brian H K ^a,c   Anders, Robin F ^b   Read, Andrew F ^a,c  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b LA TROBE UNIVERSITY   (Australia)

^c PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Malaria; Multiple infection; Plasmodium chabaudi; Virulence; Within host competition

Indexed keywords

ANTIGEN; RECOMBINANT PROTEIN;

COMPETITION (ECOLOGY); EVOLUTIONARY THEORY; HOMINID; HOST SELECTION; HOST-PATHOGEN INTERACTION; IMMUNIZATION; MALARIA; NATURAL SELECTION; POPULATION DENSITY; PROTOZOAN; PUBLIC HEALTH; RODENT; VACCINATION; VIRULENCE;

ANIMAL; ARTICLE; C57BL MOUSE; FEMALE; GENETIC SELECTION; HOST PARASITE INTERACTION; IMMUNIZATION; IMMUNOLOGY; MALARIA; MOUSE; PARASITOLOGY; PATHOGENICITY; PHYSIOLOGY; PLASMODIUM; RAT; VIRULENCE;

ANIMALS; ANTIGENS; FEMALE; HOST-PARASITE INTERACTIONS; IMMUNIZATION; MALARIA; MICE; MICE, INBRED C57BL; PLASMODIUM; RATS; RECOMBINANT PROTEINS; SELECTION (GENETICS); VIRULENCE;

MUS; PLASMODIUM CHABAUDI;

EID: 51249095422     PISSN: 00143820     EISSN: 15585646     Source Type: Journal    
DOI: 10.1111/j.1558-5646.2008.00438.x     Document Type: Article

References (71)

1. Adler, F. R., and J. Mosquera Losanda. 2002. Super- and coinfection: filling the range. Pp. 138 149 in U. Dieckmann, J. A. J. Metz, M. A. Sabelis and K. Sigmund, eds. Adaptive dynamics of infectious diseases: in pursuit of virulence management. Cambridge Univ. Press, Cambridge, U.K.
2. Anders, R. F., P. E. Crewther, S. Edwards, M. Margetts, M. Matthew, B. Pollock, and D. Pye. 1998. Immunisation with recombinant AMA-1 protects mice against infection with Plasmodium chabaudi. Vaccine 16 : 240 247.
3. Arnot, D. 1998. Clone multiplicity of Plasmodium falciparum infections in individuals exposed to variable levels of disease transmission. Trans. R. Soc. Trop. Med. Hyg. 92 : 580 585.
4. Babiker, H. A., A. M. Creasey, B. Fenton, R. A. L. Bayoumi, D. E. Arnot, and D. Walliker. 1991. Genetic diversity of Plasmodium falciparum in a village in Eastern Sudan. Diversity of enzymes, 2d-Page proteins and antigens. Trans. R. Soc. Trop. Med. Hyg. 85 : 572 577.
5. Babiker, H. A., L. C. Ranford-Cartwright, and D. Walliker. 1999. The epidemiology of multiple Plasmodium falciparum infections. Genetic structure and dynamics of Plasmodium falciparum infections in the Kilombero region of Tanzania. Trans. R. Soc. Trop. Med. Hyg. 93 : S11 S14.
6. Barclay, V. C., L. Raberg, B. H. K. Chan, S. Brown, D. Gray, and A. F. Read. 2008. CD4+ cells do not mediate within-host competition between genetically diverse parasites. Proc. R. Soc. Lond. B 275 : 1171 1179.
7. Beale, G. H., R. Carter, and D. Walliker. 1978. Genetics in rodent malaria. Pp. 213 246 in K. Kendrick and W. R. Peters, eds. Rodent Malaria. Academic Press, London.
8. Bell, A. S., J. de Roode, D. Sim, and A. F. Read. 2006. Within-host competition in genetically diverse malaria infections: parasite virulence and competition. Evolution 60 : 1358 1371.
9. Bonhoeffer, S., and M. A. Nowak. 1994. Intra-host and inter-host selection: viral evolution of immune function impairment. Proc. Natl. Acad. Sci. USA 91 : 8062 8066.
10. Bruce, M. C., C. A. Donnelly, M. P. Alpers, M. R. Galinski, J. W. Barnwell, D. Walliker, and K. P. Day. 2000. Cross-species interactions between malaria parasites in humans. Science 287 : 845 848.
11. Buckling, A., and A. F. Read. 2001. The effect of partial host immunity on the transmission of malaria parasites. Proc. R. Soc. Lond. B 268 : 2325 2330.
12. Cheesman, S., A. Raza, and R. Carter. 2006. Mixed strain infections and strain-specific protective immunity in the rodent malaria parasite Plasmodium chabaudi chabaudi in mice. Infect. Immun. 74 : 2996 3001.
13. Cheesman, S. J., J. C. de Roode, A. F. Read, and R. Carter. 2003. Real-time quantitative PCR for analysis of genetically mixed infections of malaria parasites: technique validation and applications. Mol. Biochem. Parasitol. 131 : 83 91.
14. Conway, D. J., B. M. Greenwood, and J. S. McBride. 1991. The epidemiology of multiple-clone Plasmodium falciparum infections in Gambian patients. Parasitology 103 : 1 6.
15. Daubersies, P., S. SallenaveSales, S. Magne, J. F. Trape, H. Contamin, T. Fandeur, C. Rogier, O. MercereauPuijalon, and P. Druilhe. 1996. Rapid turnover of Plasmodium falciparum populations in asymptomatic individuals living in a high transmission area. Am. J. Trop. Med. Hyg. 54 : 18 26.
16. de Roode, J. C., A. F. Read, B. H. K. Chan, and M. J. Mackinnon. 2003. Rodent malaria parasites suffer from the presence of conspecific clones in three-clone Plasmodium chabaudi infections. Parasitology 127 : 411 418.
17. de Roode, J. C., R. Culleton, A. S. Bell, and A. F. Read. 2004a. Competitive release of drug resistance following drug treatment of mixed Plasmodium chabaudi infections. Malaria J. 3 : 33.
18. de Roode, J. C., R. Culleton, S. J. Cheesman, R. Carter, and A. F. Read. 2004b. Host heterogeneity is a determinant of competitive exclusion or coexistence in genetically diverse malaria infections. Proc. R. Soc. Lond. B 271 : 1073 1080.
19. de Roode, J. C., M. E. H. Helinski, M. A. Anwar, and A. F. Read. 2005a. Dynamics of multiple infection and within-host competition in genetically diverse malaria infections. Am. Nat. 166 : 531 542.
20. de Roode, J. C., R. Pansini, S. J. Cheesman, M. E. H. Helinski, S. Huijben, A. R. Wargo, A. S. Bell, B. H. K. Chan, D. Walliker, and A. F. Read. 2005b. Virulence and competitive ability in genetically diverse malaria infections. Proc. Natl. Acad. Sci. USA 102 : 7624 7628.
21. Ewald, P. W. 1983. Host-parasite relations, vectors, and the evolution of disease severity. Annu. Rev. Ecol. Syst. 14 : 465 485.
22. Frank, S. A. 1996. Models of parasite virulence. Q. Rev. Biol. 71 : 37 78.
23. Frank, S. A. 1998. Foundations of social evolution. Princeton Univ. Press, Princeton, NJ.
24. Galvani, A. P. 2003. Epidemiology meets evolutionary ecology. Trends Ecol. Evol. 18 : 132 139.
25. Gamain, B., J. D. Smith, N. K. Viebig, J. Gysin, and A. Scherf. 2007. Pregnancy-associated malaria: parasite binding, natural immunity and vaccine development. Int. J. Parasitol. 37 : 273 283.
26. Gandon, S., V. A. A. Jansen, and M. van Baalen. 2001a. Host life history and the evolution of parasite virulence. Evolution 55 : 1056 1062.
27. Gandon, S., M. J. Mackinnon, S. Nee, and A. F. Read. 2001b. Imperfect vaccines and the evolution of pathogen virulence. Nature 414 : 751 756.
28. Good, M. F., H. J. Xu, M. Wykes, and C. R. Engwerda. 2005. Development and regulation of cell-mediated immuneresponses to the blood stages of malaria: implications for vaccine research. Annu. Rev. Immunol. 23 : 69 99.
29. Grech, K. 2006. The ecology and evolution of malaria: laboratory studies of Plasmodium chabaudi and its rodent and insect hosts. Ph.D. thesis. The Open Univ., Edinburgh.
30. Hart, A. R., and M. W. Cloyd. 1990. Interference patterns of human immunodeficiency virus Hiv-1 and virus-Hiv-2. Virology 177 : 1 10.
31. Hastings, I. M. 2003. Malaria control and the evolution of drug resistance: an intriguing link. Trends Parasitol. 19 : 70 73.
32. Hastings, I. M. 2006. Complex dynamics and stability of resistance to antimalarial drugs. Parasitology 132 : 615 624.
33. Hastings, I. M., and U. D'Alessandro. 2000. Modelling a predictable disaster: the rise and spread of drug- resistant malaria. Parasitol. Today 16 : 340 347.
34. Hellriegel, B. 1992. Modeling the immune response to malaria with ecological concepts. Short-term behavior against long-term equilibrium. Proc. R. Soc. Lond. B 250 : 249 256.
35. Jafari, S., J. Le Bras, O. Bouchaud, and R. Durand. 2004. Plasmodium falciparum clonal population dynamics during malaria treatment. J. Infect. Dis. 189 : 195 203.
36. Jarra, W., and K. N. Brown. 1985. Protective immunity to malaria. Studies with cloned lines of Plasmodium chabaudi and P. berghei in CBA/Ca mice. The effectiveness and inter-species and intra-species specificity of immunity induced by infection. Parasite Immunol. 7 : 595 606.
37. Jarra, W., and K. N. Brown. 1989. Protective immunity to malaria. Studies with cloned lines of rodent malaria in CBA/Ca mice. The specificity of mechanisms resulting in crisis and resolution of the primary acute phase parasitemia of Plasmodium chabaudi chabaudi and Plasmodium yoelii yoelii. Parasite Immunol. 11 : 1 13.
38. Levin, S., and D. Pimentel. 1981. Selection of intermediate rates of increase in parasite-host systems. Am. Nat. 117 : 308 315.
39. Li, C., E. Seixas, and J. Langhorne. 2001. Rodent malarias: the mouse as a model for understanding immune responses and pathology induced by the erythrocytic stages of the parasite. Medical Microbiol. Immunol. 189 : 115 126.
40. Mackinnon, M. J., and A. F. Read. 2003. The effects of host immunity on virulence-transmissibility relationships in the rodent malaria parasite Plasmodium chabaudi. Parasitology 126 : 103 112.
41. Mackinnon, M. J., and A. F. Read. 2004. Immunity promotes virulence evolution in a malaria model. Plos Biol. 2 : 1286 1292.
42. Mahanty, S., A. Saul, and L. H. Miller. 2003. Progress in the development of recombinant and synthetic blood-stage malaria vaccines. J. Exp. Biol. 206 : 3781 3788.
43. Martinelli, A., S. Cheesman, P. Hunt, R. Culleton, A. Raza, M. Mackinnon, and R. Carter. 2005. A genetic approach to the de novo identification of targets of strain-specific immunity in malaria parasites. Proc. Natl. Acad. Sci. USA 102 : 814 819.
44. Matuschewski, K. 2006. Vaccine development against malaria. Curr. Opin. Immunol. 18 : 449 457.
45. Mercereau-Puijalon, O. 1996. Revisiting host/parasite interactions: molecular analysis of parasites collected during longitudinal and cross-sectional surveys in humans. Parasite Immunol. 18 : 173 180.
46. Mosquera, J., and F. R. Adler. 1998. Evolution of virulence: a unified framework for coinfection and superinfection. J. Theor. Biol. 195 : 293 313.
47. Mota, M. M., K. N. Brown, A. A. Holder, and W. Jarra. 1998. Acute Plasmodium chabaudi chabaudi malaria infection induces antibodies which bind to the surfaces of parasitized erythrocytes and promote their phagocytosis by macrophages in vitro. Infect. Immun. 66 : 4080 4086.
48. Nowak, M. A., and R. M. May. 1994. Superinfection and the evolution of parasite virulence. Proc. R. Soc. Lond. B 255 : 81 89.
49. Phillips, R. S., L. R. Brannan, P. Balmer, and P. Neuville. 1997. Antigenic variation during malaria infection - the contribution from the murine parasite Plasmodium chabaudi. Parasite Immunol. 19 : 427 434.
50. Porco, T. C., J. O. Lloyd-Smith, K. L. Gross, and A. P. Galvani. 2005. The effect of treatment on pathogen virulence. J. Theor. Biol. 233 : 91 102.
51. Raberg, L., J. deRoode, A. S. Bell, S. Panagiota, D. Gray, and A. F. Read. 2006. The role of immune-mediated apparent competition in genetically diverse malaria infections. Am. Nat. 168 : 41 53.
52. Read, A. F., and L. H. Taylor. 2001. The ecology of genetically diverse infections. Science. 292 : 1099 1102.
53. Read, A. F., M. J. Mackinnon, M. Anwar, and L. H. Taylor. 2002. Kin selection models as evolutionary explanations of malaria. Pp. 165 178 in U. Dieckmann, J. A. J. Metz, M. A. Sabelis, and K. Sigmund, eds. Adaptive dynamics of infectious diseases: in pursuit of virulence management. Cambridge Univ. Press, Cambridge, U.K.
54. Riley, M. A., and J. E. Wertz. 2002. Bacteriocins: evolution, ecology, and application. Annu. Rev. Microbiol. 56 : 117 137.
55. SAS Institute. 1999. SAS OnlineDoc. Version 8. SAS Institute, Cary, NC.
56. Smith, T., I. Felger, M. Tanner, and H. P. Beck. 1999. The epidemiology of multiple Plasmodium falciparum infections. Premunition in Plasmodium falciparum infection: insights from the epidemiology of multiple infections. Trans. R. Soc. Trop. Med. Hyg. 93 : S59 S64.
57. Snounou, G., W. Jarra, S. Viriyakosol, J. C. Wood, and K. N. Brown. 1989. Use of a DNA probe to analyze the dynamics of infection with rodent malaria parasites confirms that parasite clearance during crisis is predominantly strain-specific and species-specific. Mol. Biochem. Parasitol. 37 : 37 46.
58. Snounou, G., T. Bourne, W. Jarra, S. Viriyakosol, J. C. Wood, and K. N. Brown. 1992. Assessment of parasite population dynamics in mixed infections of rodent plasmodia. Parasitology 105 : 363 374.
59. Talisuna, A. O., A. Erhart, S. Samarasinghe, C. Van Overmeir, N. Speybroeck, and U. D'Alessandro. 2006. Malaria transmission intensity and the rate of spread of chloroquine resistant Plasmodium falciparum: why have theoretical models generated conflicting results? Infect. Genet. Evol. 6 : 241 248.
60. Tanner, M., H. P. Beck, I. Felger, and T. Smith. 1999. The epidemiology of multiple Plasmodium falciparum infections. Trans. R. Soc. Trop. Med. Hyg. 93 : S1 S2.
61. Taylor, L. H., and A. F. Read. 1997. Why so few transmission stages? Reproductive restraint by malaria parasites. Parasitol. Today 13 : 135 140.
62. Taylor, L. H., and A. F. Read. 1998. Determinants of transmission success of individual clones from mixed-clone infections of the rodent malaria Plasmodium chabaudi. Intl. J. Parasitol. 28 : 719 725.
63. Taylor, L. H., D. Walliker, and A. F. Read. 1997. Mixed-genotype infections of malaria parasites: within-host dynamics and transmission success of competing clones. Proc. R. Soc. Lond. B 264 : 927 935.
64. Taylor-Robinson, A. W. 1995. Regulation of immunity to malaria - valuable lessons learned from murine models. Parasitol. Today 11 : 334 342.
65. Timms, R., N. Colegrave, B. H. K. Chan, and A. F. Read. 2001. The effect of parasite dose on disease severity in the rodent malaria Plasmodium chabaudi. Parasitology 123 : 1 11.
66. van Baalen, M., and M. W. Sabelis. 1995. The dynamics of multiple infection and the evolution of virulence. Am. Nat. 146 : 881 910.
67. Walliker, D., R. Carter, and A. Sanderson. 1975. Genetic studies on Plasmodium chabaudi. Recombination between enzyme markers. Parasitology 70 : 19 24.
68. Wargo, A. R., S. Huijben, J. C. de Roode, J. Shepherd, and A. F. Read. 2007a. Competitive release and facilitation of drug-resistant parasites after therapeutic chemotherapy in a rodent malaria model. Proc. Natl. Acad. Sci. USA 104 : 19914 19919.
69. Wargo, A. R., J. C. de Roode, S. Huijben, D. R. Drew, and A. F. Read. 2007b. Transmission stage investment of malaria parasites in response to in-host competition. Proc. R. Soc. Lond. B 274 : 2759 2768.
70. West, S. A., A. S. Griffin, A. Gardner, and S. P. Diggle. 2006. Social evolution theory for microorganisms. Nat. Rev. Microbiol. 4 : 597 607.
71. Yap, G. S., and M. M. Stevenson. 1994. Blood-transfusion alters the course and outcome of Plasmodium chabaudi AS infection in mice. Infect. Immun. 62 : 3761 3765.