Revealing mechanisms underlying variation in malaria virulence: Effective propagation and host control of uninfected red blood cell supply

Journal of the Royal Society Interface

Volumn 9, Issue 76, 2012, Pages 2804-2813

  Metcalf, C J E ^a   Long, G H ^b   Mideo, N ^c   Forester, J D ^d   Bjornstad O N ^c   Graham, A L ^e  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b ADDENBROOKE S HOSPITAL   (United Kingdom)

^c PENNSYLVANIA STATE UNIVERSITY   (United States)

^d UNIVERSITY OF MINNESOTA   (United States)

^e PRINCETON UNIVERSITY   (United States)

Author keywords

Evolution; Health; Malaria

Indexed keywords

BLOOD; CELLS; CLONING; DISEASES; HEALTH;

EVOLUTION; MALARIA; MALARIA PARASITE; RED BLOOD CELL; SELF-DEFENCE; TRANSMISSION RATES;

MALARIA CONTROL;

ARTICLE; CELL KILLING; CONTROLLED STUDY; CORRELATION ANALYSIS; EFFECTOR CELL; ERYTHROCYTE; MALARIA; MORTALITY; NONHUMAN; PARASITE VIRULENCE; SPLEEN;

EID: 84867441813     PISSN: 17425689     EISSN: 17425662     Source Type: Journal    
DOI: 10.1098/rsif.2012.0340     Document Type: Article

References (52)

1. Holmes, E. C. & Burch, S. S. 2000 The causes and consequences of genetic variation in dengue virus. Trends Microbiol. 8, 74-77. (doi:10.1016/S0966-842X(99)01669-8)
2. Paul, R. E. L., Ariey, F. & Robert, V. 2003 The evolutionary ecology of Plasmodium. Ecol. Lett. 6, 866-880. (doi:10.1046/j.1461-0248.2003.00509.x)
3. Reece, S. E., Ramiro, R. S. & Nussey, D. H. 2009 Plastic parasites: sophisticated strategies for survival and reproduction? Evol. Appl. 2, 11-23. (doi:10.1111/j.1752-4571.2008.00060.x)
4. Manning, S. D. et al. 2011 Variation in virulence among clades of Escherichia coli O157:H7 associated with disease outbreaks. Proc. Natl Acad. Sci. USA 105, 4868-4873. (doi:10.1073/pnas.0710834105)
5. Mackinnon, M. J., Gaffney, D. J. & Read, A. F. 2002 Virulence in malaria parasites: host genotype by parasite genotype interactions. Infect. Genet. Evol. 1, 287-297. (doi:10.1016/S1567-1348(02)00039-4)
6. Diep, B. A., Carleton, H., Chang, A. R., Sensabaugh, F. G. F. & Perdreau-Remington, F. 2006 Roles of 34 virulence genes in the evolution of hospital- and community-associated strains of methicillin-resistant Staphylococcus aureus. J. Infect. Dis. 193, 1495-1503. (doi:10.1086/503777)
7. Gandon, S., Mackinnon, M. J., Nee, S. & Read, A. F. 2001 Imperfect vaccines and the evolution of pathogen virulence. Nature 414, 751-756. (doi:10.1038/414751a)
8. Frank, S. A. 1996 Models of parasite virulence. Q. Rev. Biol. 71, 37-78. (doi:10.1086/419267)
9. Mackinnon, M. J. & Read, A. F. 2004 Virulence in malaria: an evolutionary viewpoint. Phil. Trans. R. Soc. Lond. B 359, 965-986. (doi:10.1098/rstb.2003.1414)
10. Alizon, S., Hurford, A., Mideo, N. & Van Baalen, M. 2009 Virulence evolution and the trade-off hypothesis: history, current state of affairs and the future. J. Evol. Biol. 22, 245-259. (doi:10.1111/j.1420-9101.2008.01658.x)
11. Anderson, R. M. & May, R. M. 1982 Coevolution of hosts and parasites. Parasitology 85, 411-426. (doi:10.1017/S0031182000055360)
12. Mideo, N., Nelson, W. A., Reece, S. E., Bell, A. S., Read, A. F. & Day, T. 2011 Bridging scales in the evolution of infectious disease life histories: application. Evolution 65, 3298-3310. (doi:10.1111/j.1558-5646.2011. 01382.x)
13. Fenner, F., Day, M. F. & Woodroofe, G. M. 1956 The epidemiological consequences of the mechanical transmission of myxomatosis by mosquitoes. J. Hyg. 54, 284-303. (doi:10.1017/S0022172400044521)
14. Fraser, C., Hollingsworth, T. D., Chapman, R., de Wolf, F. & Hanage, W. P. 2007 Variation in HIV-1 set-point viral load: epidemiological analysis and an evolutionary hypothesis. Proc. Natl Acad. Sci. USA 104, 17 441-17 446. (doi:10.1073/pnas.0710909105)
15. de Roode, J. C., Yates, A. J. & Altizer, S. 2008 Virulence- transmission trade-offs and population divergence in virulence in a naturally occurring butterfly parasite. Proc. Natl Acad. Sci. USA 105, 7489-7494. (doi:10.1073/pnas.0710909105)
16. Mideo, N., Day, T. & Read, A. 2008 Modelling malaria pathogenesis. Cell. Microbiol. 10, 1947-1955. (doi:10.1111/j.1462-5822.2008.01208.x)
17. Mideo, N. 2009 Parasite adaptations to within-host competition. Trends Parasitol. 25, 261-268. (doi:10.1016/j.pt.2009.03.001)
18. McQueen, P. G. & McKenzie, F. E. 2006 Competition for red blood cells can enhance Plasmodium vivax parasitemia in mixed-species malaria infections. Am. J. Trop. Med. Hyg. 75, 112-125. (Pubitemid 351627579)
19. Lipsitch, M. & Moxon, R. E. 1997 Virulence and transmissibility of pathogens: what is the relationship? Trends Microbiol. 5, 31-37. (doi:10.1016/S0966-842X(97)81772-6)
20. Graham, A. L., Allen, J. E. & Read, A. F. 2005 Evolutionary causes and consequences of immunopathology. Annu. Rev. Ecol. Syst. 36, 373-397. (doi:10.1146/annurev.ecolsys.36.102003.152622)
21. Graham, A. L., Hayward, A. D., Watt, K. A., Pilkington, J. G., Pemberton, J. M. & Nussey, D. H. 2010 Fitness correlates of heritable variation in antibody responsiveness in a wild mammal. Science 330, 662-665. (doi:10.1126/science.1194878)
22. Long, G. H. & Boots, M. 2011 How can immunopathology shape the evolution of parasite virulence. Trends Parasitol. 27, 300-305. (doi:10.1016/j.pt.2011.03.012)
23. Long, G. H. & Graham, A. L. 2011 Consequences of immunopathology for pathogen virulence evolution and public health: malaria as a case study. Evol. Appl. 4, 278-291. (doi:10.1111/j.1752-4571.2010.00178.x)
24. Clark, I. A., Alleva, L., Mills, M. A. C. & Cowden, W. B. 2004 Pathogenesis of malaria and clinically similar conditions. Clin. Microbiol. Rev. 17, 509-539. (doi:10.1128/CMR.17.3.509-539.2004)
25. Langhorne, J., Quin, J. S. & Sanni, L. A. 2002 Mouse models of blood-stage malaria infections: immune responses and cytokines involved in protection and pathology. Chem. Immunol. 80, 204-228. (doi:10.1159/000058845)
26. Price, R. N., Simpson, J., Nosten, F., Luxemburger, C., Hkirjaroen, L., ter Kuile, F. O., Chongsuphajaisiddhi, T. & White, N. J. 2001 Factors contributing to anemia following uncomplicated falciparum malaria. Am. J. Trop. Med. Hyg. 65, 614-622. (Pubitemid 33134602)
27. Buffet, P. A., Safeukui, I., Deplaine, G., Brousse, V., Prendki, V., Thellier, M., Turner, G. D. & Mercereau-Puijalon, O. 2011 The pathogenesis of Plasmodium falciparum malaria in humans: insights from splenic physiology. Blood 117, 381-392. (doi:10.1182/blood-2010-04-202911)
28. Cromer, D., Stark, J. & Davenport, M. 2009 Low red cell production may protect against severe anemia during a malaria infection: insights from modeling. J. Theor. Biol. 257, 533-542. (doi:10.1016/j.jtbi.2008.12.019)
29. Metcalf, C. J. E., Graham, A. L., Huijben, S., Barclay, V. C., Long, G. H., Grenfell, B. T., Read, A. F. & Bjornstad, O. N. 2011 Partitioning regulatory mechanisms of within-host malaria dynamics using the effective propagation number. Science 333, 984-988. (doi:10.1126/science.1204588)
30. Nowak, M. A. & May, R. M. 2000 Virus dynamics: mathematical principles of immunology and virology. Oxford, UK: Oxford University Press.
31. Huijben, S., Nelson, W. A., Wargo, A. R., Sim, D. G., Drew, D. R. & Read, A. F. 2010 Chemotherapy, within-host ecology and the fitness of drug resistant malaria parasites. Evolution 64, 2952-2968.
32. Mackinnon, M. J. & Read, A. F. 1999 Genetic relationships between parasite virulence and transmission in the rodent malaria Plasmodium chabaudi. Evolution 53, 689-703. (doi:10.2307/2640710)
33. Long, G. H., Chan, B. H. K., Allen, J. E., Read, A. F. & Graham, A. L. 2006 Parasite genetic diversity does not influence TNF-mediated effects on the virulence of primary rodent malaria infections. Parasitology 133, 673-684. (doi:10.1017/S003118200600117X)
34. Long, G. H., Chan, B. H. K., Allen, J. E., Read, A. F. & Graham, A. L. 2008 Experimental manipulation of immune-mediated disease and its fitness costs for rodent malaria parasites. BMC Evol. Biol. 8, 128. (doi:10.1186/1471- 2148-8-128)
35. Antia, R., Yates, A. & de Roode, J. C. 2008 The dynamics of acute malaria infections. I. Effect of the parasites red blood cell preference. Proc. R. Soc. B 275, 1449-1458. (doi:10.1098/rspb.2008.0198)
36. Mideo, N., Barclay, V. C., Chan, B. H. K., Savill, N. J., Read, A. F. & Day, T. 2008 Understanding and predicting strain-specific patterns of pathogenesis in the rodent malaria Plasmodium chabaudi. Am. Nat. 172, E214-E238. (doi:10.1086/591684)
37. Haydon, D. T., Matthews, L., Timms, R. & Colegrave, N. 2003 Top-down or bottom-up regulation of intra-host blood-stage malaria: do malaria parasites most resemble the dynamics of prey or predator? Proc. R. Soc. Lond. B 270, 289-298. (doi:10.1098/rspb.2002.2203)
38. Kochin, B. F., Yates, A. J., de Roode, J. C. & Antia, R. 2010 On the control of acute rodent malaria infections by innate immunity. PLoS ONE 5, e10444. (doi:10.1371/journal.pone.0010444)
39. Miller, M. R., Raberg, L., Read, A. F. & Savill, N. J. 2010 Quantitative analysis of immune response and erythropoesis during rodent malarial infection. PLoS Comp. Biol. 6, e1000946. (doi:10.1371/journal.pcbi. 1000946)
40. Mideo, N., Savill, N. J., Chadwick, W., Schnieder, P., Read, A. F., Day, T. & Reece, S. E. 2011 Causes of variation in malaria infection dynamics: insights from theory and data. Am. Nat. 178, E174-E188. (doi:10.1086/662670)
41. Read, A. F. & Taylor, L. H. 1997 Why so few transmission stages? Reproductive restraint by malaria parasites. Parasitol. Today 13, 135-140. (doi:10.1016/S0169-4758(97)89810-9)
42. Van Putten, L. M. 1958 The life span of red cells in the rate and the mouse as determined by labeling with Dfp32 in vivo. Blood 13, 789-794.
43. Bannerman, R. M. 1983 Hematology. In The mouse in biomedical research volume III: normative biology, immunology, and husbandry (eds H. Foster, L. J. D. Small & J. G. Fox), pp. 293-313. New York, NY: Academic Press.
44. Jakeman, G. N., Saul, A., Hogarth, W. L. & Collins, W. E. 1999 Anaemia of acute malaria infections in non-immune patients primarily results from destruction of uninfected erythrocytes. Parasitology 119, 127-133. (doi:10.1017/S0031182099004564)
45. Yoeli, M., Hargreaves, B., Carter, R. & Walliker, D. 1975 Sudden increase in virulence in a strain of Plasmodium berghei yoelii. Annu. Trop. Med. Parasitol. 69, 183-178.
46. Beale, G. H., Walliker, D. & Carter, R. 1978 Genetics. In Rodent malaria (eds R. Killick-Kendrick & W. Peters), pp. 213-245. London, UK: Academic Press.
47. Franklin, B. S. et al. 2009 Malaria primes the innate immune response due to interferon-γ induced enhancement of toll-like receptor expression and function. Proc. Natl Acad. Sci. USA 106, 5789-5794. (doi:10.1073/pnas. 0809742106)
48. Wu, X., Gowda, N. J., Kumar, S. & Gowda, D. C. 2010 Protein-DNA complex is the exclusive malaria parasite component that activates dendritic cells and triggers innate immune responses. J. Immunol. 184, 4338-4348. (doi:10.4049/jimmunol.0903824)
49. Su, Z. & Stevenson, M. M. 2000 Central role of endogenous gamma interferon in protective immunity against blood-stage Plasmodium chabaudi AS infection. Infect. Immunol. 68, 4399-4406. (doi:10.1128/IAI.68.8.4399-4406.2000)
50. Su, Z., Fortin, A., Gros, P. & Stevenson, M. M. 2002 Opsonin-independent phagocytosis: an effector mechanism against acute blood-stage Plasmodium chabaudi AS infection. J. Infect. Dis. 186, 1321-1329. (doi:10.1086/344576)
51. Chang, K.-H., Tam, M. & Stevenson, M. M. 2004 Modulation of the course and outcome of blood-stage malaria by erythropoietin-induced reticulocytosis. J. Infect. Dis. 189, 735-743. (doi:10.1086/381458)
52. Lazzaro, B. P. & Little, T. J. 2009 Immunity in a variable world. Phil. Trans. R. Soc. B 364, 15-25. (doi:10.1098/rstb.2008.0141)