Expansion of host cellular niche can drive adaptation of a zoonotic malaria parasite to humans

Nature Communications

Volumn 4, Issue , 2013, Pages

  Lim, Caeul ^a   Hansen, Elsa ^a   Desimone, Tiffany M ^a   Moreno, Yovany ^a   Junker, Klara ^a   Bei, Amy ^a   Brugnara, Carlo ^a   Buckee, Caroline O ^a,b   Duraisingh, Manoj T ^a  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION; BLOOD; EVOLUTIONARY BIOLOGY; HOMINID; HOST RANGE; MALARIA; NICHE BREADTH; NUMERICAL MODEL; PARASITE INFESTATION; PRIMATE; PROTOZOAN; RANGE EXPANSION;

ADAPTATION; ARTICLE; CELL INVASION; CELL PROLIFERATION; CONTROLLED STUDY; ERYTHROCYTE; HOST CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; PATHOGENESIS; PLASMODIUM KNOWLESI;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; ERYTHROCYTES; HUMANS; MACACA MULATTA; PLASMODIUM KNOWLESI; ZOONOSES;

SOUTHEAST ASIA;

PLASMODIUM FALCIPARUM; PLASMODIUM KNOWLESI; PRIMATES;

EID: 84875787172     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms2612     Document Type: Article

References (50)

1. Cox Singh, J. & Singh, B. Knowlesi malaria: newly emergent and of public health importance? Trends Parasitol. 24, 406-410 (2008).
2. Lee, K.-S. et al. Plasmodium knowlesi: reservoir hosts and tracking the emergence in humans and macaques. PLoS Pathog. 7, e1002015 (2011).
3. Chin, W., Contacos, P. G., Coatney, G. R. & Kimball, H. R. A naturally acquired quotidian-type malaria in man transferable to monkeys. Science 149, 865-865 (1965).
4. Cox Singh, J. Zoonotic malaria. Curr. Opin. Infect. Dis. 25, 530-536 (2012).
5. Daneshvar, C. et al. Clinical and laboratory features of human Plasmodium knowlesi infection. Clin. Infect. Dis. 49, 852-860 (2009).
6. Cox Singh, J. et al. Anti-inflammatory cytokines predominate in acute human Plasmodium knowlesi infections. PLoS ONE 6, e20541 (2011).
7. Barber, B. E. et al. A prospective comparative study of knowlesi, falciparum and vivax malaria in Sabah, Malaysia: high proportion with severe disease from Plasmodium knowlesi and P. vivax but no mortality with early referral and artesunate therapy. Clin. Infect. Dis. 56, 383-397 (2013).
8. Bosman, G. J. C. G. M., Werre, J. M., Willekens, F. L. A. & Novotný, V. M. J. Erythrocyte ageing in vivoand in vitro: structural aspects and implications for transfusion. Transfus. Med. 18, 335-347 (2008).
9. Kitchen, S. F. The infection of reticulocytes by Plasmodium vivax. Am. J. Trop. Med. 18, 347-353 (1938).
10. Collins, W. E. & Jeffery, G. M. Plasmodium ovale: parasite and disease. Clin. Microbiol. Rev. 18, 570-581 (2005). (Pubitemid 40995117)
11. Kitchen, S. The infection of mature and immature erythrocytes by Plasmodium falciparum and Plasmodium malariae. Am. J. Trop. Med. Hyg. 1, 47-62 (1939).
12. Pasvol, G., Weatherall, D. J. & Wilson, R. J. The increased susceptibility of young red cells to invasion by the malarial parasite Plasmodium falciparum. Br. J. Haematol. 45, 285-295 (1980). (Pubitemid 10120179)
13. Chotivanich, K. et al. Parasite multiplication potential and the severity of Falciparum malaria. J. Infect. Dis. 181, 1206-1209 (2000). (Pubitemid 30194518)
14. Collins, W. E. & Barnwell, J. W. Plasmodium knowlesi: finally being recognized. J. Infect. Dis. 199, 1107-1108 (2009).
15. Hegner, R. Relative frequency of ring-stage plasmodia in reticulocytes and mature erythrocytes in man and monkey. Am. J. Epidemiol. 27, 690-718 (1938).
16. Miller, L. H. & Chien, S. Density distribution of red cells infected by Plasmodium knowlesi and Plasmodium coatneyi. Exp. Parasitol. 29, 451-456 (1971).
17. Singh, B. et al. A large focus of naturally acquired Plasmodium knowlesi infections in human beings. Lancet 363, 1017-1024 (2004). (Pubitemid 38410774)
18. Cox-Singh, J. et al. Plasmodium knowlesi malaria in humans is widely distributed and potentially life threatening. Clin. Infect. Dis. 46, 165-171 (2008). (Pubitemid 351269152)
19. Antia, R., Regoes, R. R., Koella, J. C. & Bergstrom, C. T. The role of evolution in the emergence of infectious diseases. Nature 426, 658-661 (2003). (Pubitemid 38009372)
20. Kocken, C. H. M. et al. Plasmodium knowlesi provides a rapid in vitro and in vivo transfection system that enables double-crossover gene knockout studies. Infect. Immun. 70, 655-660 (2002). (Pubitemid 34083824)
21. Salvo, G., Caprari, P., Samoggia, P., Mariani, G. & Salvati, A. M. Human erythrocyte separation according to age on a discontinuous 'Percoll' density gradient. Clinica Chimica Acta 122, 293-300 (1982). (Pubitemid 12088780)
22. Omodeo-Salè, F. et al. Accelerated senescence of human erythrocytes cultured with Plasmodium falciparum. Blood 102, 705-711 (2003). (Pubitemid 36841995)
23. Trager, W. & Jensen, J. B. Human malaria parasites in continuous culture. Science 193, 673-675 (1976).
24. McQueen, P. G. & McKenzie, F. E. Age-structured red blood cell susceptibility and the dynamics of malaria infections. Proc. Natl Acad. Sci. USA 101, 9161-9166 (2004). (Pubitemid 38781628)
25. McQueen, P. G. & McKenzie, F. E. Host control of malaria infections: constraints on immune and erythropoeitic response kinetics. PLoS Comput. Biol. 4, e1000149 (2008).
26. Mideo, N. et al. Understanding and predicting strain-specific patterns of pathogenesis in the rodent malaria Plasmodium chabaudi. Am. Nat. 172, E214-E238 (2008).
27. Antia, R., Yates, A. & de Roode, J. C. The dynamics of acute malaria infections. I. Effect of the parasite's red blood cell preference. Proc. R. Soc. B: Biol. Sci. 275, 1449-1458 (2008). (Pubitemid 351653013)
28. Cromer, D., Stark, J. & Davenport, M. P. Low red cell production may protect against severe anemia during a malaria infection-insights from modeling. J. Theor. Biol. 257, 533-542 (2009).
29. Cromer, D., Evans, K. J., Schofield, L. & Davenport, M. P. Preferential invasion of reticulocytes during late-stage Plasmodium berghei infection accounts for reduced circulating reticulocyte levels. Int. J. Parasitol. 36, 1389-1397 (2006). (Pubitemid 44485653)
30. Kantele, A. & Jokiranta, T. S. Review of cases with the emerging fifth human malaria parasite, Plasmodium knowlesi. Clin. Infect. Dis. 52, 1356-1362 (2011).
31. Ward, G. E. G., Fujioka, H. H., Aikawa, M. M. & Miller, L. H. L. Staurosporine inhibits invasion of erythrocytes by malarial merozoites. Exp. Parasitol. 79, 480-487 (1994).
32. Ward, G. E., Miller, L. H. & Dvorak, J. A. The origin of parasitophorous vacuole membrane lipids in malaria-infected erythrocytes. J. Cell. Sci. 106(Part 1): 237-248 (1993). (Pubitemid 23286796)
33. Kocken, C. H. M., Zeeman, A.-M., Voorberg-van der Wel, A. & Thomas, A. W. Transgenic Plasmodium knowlesi: relieving a bottleneck in malaria research? Trends Parasitol. 25, 370-374 (2009).
34. Dhangadamajhi, G., Kar, S. K. & Ranjit, M. The survival strategies of malaria parasite in the red blood cell and host cell polymorphisms. Malaria Res. Treat. 2010, 1-9 (2010).
35. Pasvol, G., Weatherall, D. J. & Wilson, R. J. Cellular mechanism for the protective effect of haemoglobin S against P. falciparum malaria. Nature 274, 701-703 (1978). (Pubitemid 8405068)
36. Aidoo, M. M. et al. Protective effects of the sickle cell gene against malaria morbidity and mortality. Lancet 359, 2-2 (2002).
37. Miller, L. H. L., Mason, S. J. S., Dvorak, J. A. J., McGinniss, M. H. M. & Rothman, I. K. I. Erythrocyte receptors for (Plasmodium knowlesi) malaria: Duffy blood group determinants. Science 189, 561-563 (1975).
38. Miller, L. H., Mason, S. J., Clyde, D. F. & McGinniss, M. H. The resistance factor to Plasmodium vivax in blacks. The Duffy-blood-group genotype, FyFy. N. Engl. J. Med. 295, 302-304 (1976).
39. Liu, W. et al. Origin of the human malaria parasite Plasmodium falciparum in gorillas. Nature 467, 420-425 (2010).
40. Iyer, J. K., Amaladoss, A., Ganesan, S. & Preiser, P. R. Variable expression of the 235kDa rhoptry protein of Plasmodium yoelii mediate host cell adaptation and immune evasion. Mol. Microbiol. 65, 333-346 (2007). (Pubitemid 47052717)
41. Jiang, N. et al. Co-infections with Plasmodium knowlesi and other malaria parasites, Myanmar. Emerg. Infect. Dis. 16, 1476-1478 (2010).
42. Marchand, R. Co-infections of Plasmodium knowlesi, P. falciparum, and P. vivax among humans and Anopheles dirus mosquitoes, Southern Vietnam. Emerg. Infect. Dis. 17, 1232-1239 (2011).
43. McQueen, P. G. P. & McKenzie, F. E. F. Competition for red blood cells can enhance Plasmodium vivax parasitemia in mixed-species malaria infections. Am. J. Trop. Med. Hyg. 75, 112-125 (2006).
44. Vythilingam, I. et al. Natural transmission of Plasmodium knowlesi to humans by Anopheles latens in Sarawak, Malaysia. Trans. R Soc. Trop. Med. Hyg. 100, 1087-1088 (2006). (Pubitemid 44309212)
45. Yakob, L., Bonsall, M. B. & Yan, G. Modelling knowlesi malaria transmission in humans: vector preference and host competence. Malar. J. 9, 329 (2010).
46. Vythilingam, I. Plasmodium knowlesi in humans: a review on the role of its vectors in Malaysia. Trop. Biomed. 27, 1-12 (2010).
47. Ciuca, M. & Rom̂ne, A. R. P. Contribution expérimentale à l'étude de l'immunité dans le paludisme (résumé) (1955).
48. Golenda, C. F., Li, J. & Rosenberg, R. Continuous in vitro propagation of the malaria parasite Plasmodium vivax. Proc. Natl Acad. Sci. USA 94, 6786-6791 (1997). (Pubitemid 27281942)
49. Russell, B. et al. A reliable ex vivo invasion assay of human reticulocytes by Plasmodium vivax. Blood 118, e74-e81 (2011).
50. Gravenor, M. B., McLean, A. R. & Kwiatkowski, D. The regulation of malaria parasitaemia: parameter estimates for a population model. Parasitology 110(Part 2): 115-122 (1995).