#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Within-host Competition Does Not Select for Virulence in Malaria Parasites; Studies with


Malaria infections are very often composed of multiple strains of malaria parasites. It is thought that these strains may compete for resources such as space and nutrients within the host. Here we show that such “within-host competition” has repercussions for the virulence of the malaria infection, so that infections composed of multiple strains are more virulent in terms of disease severity, than single strain infections containing the constituent parasites. Following from this, it has been proposed that as such competition would favour those parasites with faster growth rates, then these parasites would be selected in nature when within-host competition is common. We show, however, that this is not necessarily the case, as parasites with faster growth rates in the mammalian host were no more successful at transmitting to mosquitoes than parasites with slower growth rates. These results show that a reassessment of our current understanding of the role of within-host competition in the selection of virulence in malaria parasites is required.


Vyšlo v časopise: Within-host Competition Does Not Select for Virulence in Malaria Parasites; Studies with. PLoS Pathog 11(2): e32767. doi:10.1371/journal.ppat.1004628
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004628

Souhrn

Malaria infections are very often composed of multiple strains of malaria parasites. It is thought that these strains may compete for resources such as space and nutrients within the host. Here we show that such “within-host competition” has repercussions for the virulence of the malaria infection, so that infections composed of multiple strains are more virulent in terms of disease severity, than single strain infections containing the constituent parasites. Following from this, it has been proposed that as such competition would favour those parasites with faster growth rates, then these parasites would be selected in nature when within-host competition is common. We show, however, that this is not necessarily the case, as parasites with faster growth rates in the mammalian host were no more successful at transmitting to mosquitoes than parasites with slower growth rates. These results show that a reassessment of our current understanding of the role of within-host competition in the selection of virulence in malaria parasites is required.


Zdroje

1. Beier MS, Schwartz IK, Beier JC, Perkins P V, Onyango F, et al. (1988) Identification of malaria species by ELISA in sporozoite and oocyst infected Anopheles from western Kenya. Am J Trop Med Hyg 39: 323–327. 3056055

2. Snounou G, Pinheiro L, Gonçalves A, Fonseca L, Dias F, et al. (n.d.) The importance of sensitive detection of malaria parasites in the human and insect hosts in epidemiological studies, as shown by the analysis of field samples from Guinea Bissau. Trans R Soc Trop Med Hyg 87: 649–653. doi: 10.1016/0035-9203(93)90274-T

3. Arez AP, Palsson K, Pinto J, Franco AS, Dinis J, et al. (1997) Transmission of mixed malaria species and strains by mosquitoes, as detected by PCR, in a study area in Guinea-Bissau. Parassitologia 39: 65–70. 9419850

4. Richie TL (1988) Interactions between malaria parasites infecting the same vertebrate host. Parasitology 96 (Pt 3): 607–639. doi: 10.1017/S0031182000080227 3043327

5. Collins WE, Jeffery GM (1999) A retrospective examination of sporozoite- and trophozoite-induced infections with Plasmodium falciparum in patients previously infected with heterologous species of Plasmodium: effect on development of parasitologic and clinical immunity. Am J Trop Med Hyg 61: 36–43. doi: 10.4269/tropmed.1999.61-020 10432043

6. Snounou G, Bourne T, Jarra W, Viriyakosol S, Brown KN (1992) Identification and quantification of rodent malaria strains and species using gene probes. Parasitology 105 (Pt 1: 21–27. doi: 10.1017/S0031182000073649 1359498

7. De Roode JC, Pansini R, Cheesman SJ, Helinski MEH, Huijben S, et al. (2005) Virulence and competitive ability in genetically diverse malaria infections. Proc Natl Acad Sci U S A 102: 7624–7628. doi: 10.1073/pnas.0500078102 15894623

8. Griffiths EC, Pedersen AB, Fenton A, Petchey OL (2011) The nature and consequences of coinfection in humans. J Infect 63: 200–206. doi: 10.1016/j.jinf.2011.06.005 21704071

9. Black J, Hommel M, Snounou G, Pinder M (1994) Mixed Infections with Plasmodium falciparum and P malariae and fever In malaria. Lancet 343: 1095. doi: 10.1016/S0140-6736(94)90203-8 7909108

10. Bruce MC, Macheso A, Kelly-Hope LA, Nkhoma S, McConnachie A, et al. (2008) Effect of transmission setting and mixed species infections on clinical measures of malaria in Malawi. PLoS One 3: e2775. doi: 10.1371/journal.pone.0002775 18648666

11. Alifrangis M, Lemnge MM, Moon R, Theisen M, Bygbjerg I, et al. (1999) IgG reactivities against recombinant Rhoptry-Associated Protein-1 (rRAP-1) are associated with mixed Plasmodium infections and protection against disease in Tanzanian children. Parasitology 119 (Pt 4: 337–342. doi: 10.1017/S0031182099004825 10581610

12. Luxemburger C, Ricci F, Nosten F, Raimond D, Bathet S, et al. (1997) The epidemiology of severe malaria in an area of low transmission in Thailand. Trans R Soc Trop Med Hyg 91: 256–262. doi: 10.1016/S0035-9203(97)90066-3 9231189

13. Maitland K, Williams TN, Bennett S, Newbold CI, Peto TEA, et al. (1996) The interaction between Plasmodium falciparum and P. vivax in children on Espiritu Santo island, Vanuatu. Trans R Soc Trop Med Hyg 90: 614–620. doi: 10.1016/S0035-9203(96)90406-X 9015495

14. Price RN, Nosten F, Luxemburger C, van Vugt M, Phaipun L, et al. (1997) Artesunate/mefloquine treatment of multi-drug resistant falciparum malaria. Trans R Soc Trop Med Hyg 91: 574–577. doi: 10.1016/S0035-9203(97)90032-8 9463672

15. Babiker HA, Charlwood JD, Smith T, Walliker D (1995) Gene flow and cross-mating in Plasmodium falciparum in households in a Tanzanian village. Parasitology 111 (Pt 4: 433–442. doi: 10.1017/S0031182000065938 11023407

16. Babiker HA, Ranford-Cartwright LC, Currie D, Charlwood JD, Billingsley P, et al. (1994) Random mating in a natural population of the malaria parasite Plasmodium falciparum. Parasitology 109 (Pt 4: 413–421. doi: 10.1017/S0031182000080665 7800409

17. Huber W, Haji H, Charlwood JD, Certa U, Walliker D, et al. (1998) Genetic characterization of the malaria parasite Plasmodium falciparum in the transmission from the host to the vector. Parasitology 116 (Pt 2: 95–101. doi: 10.1017/S0031182097002138 9509019

18. Paul RE, Packer MJ, Walmsley M, Lagog M, Ranford-Cartwright LC, et al. (1995) Mating patterns in malaria parasite populations of Papua New Guinea. Science 269: 1709–1711. doi: 10.1126/science.7569897 7569897

19. Taylor LH, Walliker D, Read AF (1997) Mixed-genotype infections of malaria parasites: within-host dynamics and transmission success of competing clones. Proc Biol Sci 264: 927–935. doi: 10.1098/rspb.1997.0128 9225482

20. Taylor LH, Walliker D, Read AF (1997) Mixed-genotype infections of the rodent malaria Plasmodium chabaudi are more infectious to mosquitoes than single-genotype infections. Parasitology 115 (Pt 2: 121–132. doi: 10.1017/S0031182097001145 10190168

21. Culleton R, Carter R (2012) Genetic Mapping of Virulence in Rodent Malarias. In: Sibley L, Howlett B, Heitman J, editors. Evolution of Virulence in Eukaryotic Microbes. Wiley-Blackwell. pp. 269–284.

22. Bell AS, de Roode JC, Sim D, Read AF (2006) Within-host competition in genetically diverse malaria infections: parasite virulence and competitive success. Evolution 60: 1358–1371. doi: 10.1554/05-611.1 16929653

23. Ferguson HM, Mackinnon MJ, Chan BH, Read AF (2003) Mosquito mortality and the evolution of malaria virulence. Evolution 57: 2792–2804. doi: 10.1111/j.0014-3820.2003.tb01521.x 14761058

24. Hacker CS, Kilama WL (1974) The relationship between plasmodium gallinaceum density and the fecundity of Aedes aegypti. J Invertebr Pathol 23: 101–105. doi: 10.1016/0022-2011(74)90079-2 4819576

25. Hogg JC, Hurd H (1995) Plasmodium yoelii nigeriensis: the effect of high and low intensity of infection upon the egg production and bloodmeal size of Anopheles stephensi during three gonotrophic cycles. Parasitology 111 (Pt 5: 555–562. doi: 10.1017/S0031182000077027 8559587

26. Hogg JC, Hurd H (1995) Malaria-induced reduction of fecundity during the first gonotrophic cycle of Anopheles stephensi mosquitoes. Med Vet Entomol 9: 176–180. doi: 10.1111/j.1365-2915.1995.tb00175.x 7787226

27. Hogg JC, Hurd H (1997) The effects of natural Plasmodium falciparum infection on the fecundity and mortality of Anopheles gambiae s. l. in north east Tanzania. Parasitology 114 (Pt 4: 325–331. doi: 10.1017/S0031182096008542 9107019

28. Hurd H, Carter V, Nacer A (2005) Interactions between malaria and mosquitoes: the role of apoptosis in parasite establishment and vector response to infection. Curr Top Microbiol Immunol 289: 185–217. 15791957

29. Hurd H, Grant KM, Arambage SC (2006) Apoptosis-like death as a feature of malaria infection in mosquitoes. Parasitology 132 Suppl: S33–S47. doi: 10.1017/S0031182006000849 17018164

30. Gamage-Mendis AC, Rajakaruna J, Weerasinghe S, Mendis C, Carter R, et al. (n.d.) Infectivity of Plasmodium vivax and P. falciparum to Anopheles tessellatus; relationship between oocyst and sporozoite development. Trans R Soc Trop Med Hyg 87: 3–6. doi: 10.1016/0035-9203(93)90396-8

31. Vezilier J, Nicot A, Gandon S, Rivero A (2012) Plasmodium infection decreases fecundity and increases survival of mosquitoes. Proc R Soc B Biol Sci 279: 4033–4041. doi: 10.1098/rspb.2012.1394

32. Maier WA, Becker-Feldman H, Seitz HM (1987) Pathology of malaria-infected mosquitoes. Parasitol Today 3: 216–218. doi: 10.1016/0169-4758(87)90063-9 15462959

33. Vernick KD, Oduol F, Lazzaro BP, Glazebrook J, Xu J, et al. (2005) Molecular genetics of mosquito resistance to malaria parasites. Curr Top Microbiol Immunol 295: 383–415. 16265899

34. Ferguson HM, Read AF (2002) Why is the effect of malaria parasites on mosquito survival still unresolved? Trends Parasitol 18: 256–261. doi: 10.1016/S1471-4922(02)02281-X 12036738

35. Pollitt LC, Reece SE, Mideo N, Nussey DH, Colegrave N (2012) The problem of auto-correlation in parasitology. PLoS Pathog 8: e1002590. doi: 10.1371/journal.ppat.1002590 22511865

36. R Development Core Team (2014) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. R Found Stat Comput Vienna, Austria.

37. Imwong M, Nakeesathit S, Day NPJ, White NJ (2011) A review of mixed malaria species infections in anopheline mosquitoes. Malar J 10: 253. doi: 10.1186/1475-2875-10-253 21880138

38. Genton B, D’Acremont V, Rare L, Baea K, Reeder JC, et al. (2008) Plasmodium vivax and mixed infections are associated with severe malaria in children: a prospective cohort study from Papua New Guinea. PLoS Med 5: e127. doi: 10.1371/journal.pmed.0050127 18563961

39. Bruce MC, Galinski MR, Barnwell JW, Donnelly CA, Walmsley M, et al. (2000) Genetic diversity and dynamics of plasmodium falciparum and P. vivax populations in multiply infected children with asymptomatic malaria infections in Papua New Guinea. Parasitology 121 (Pt 3: 257–272. doi: 10.1017/S0031182099006356 11085246

40. Read AF (2001) The Ecology of Genetically Diverse Infections. Science (80-) 292: 1099–1102. doi: 10.1126/science.1059410

41. Zimmerman PA, Mehlotra RK, Kasehagen LJ, Kazura JW (2004) Why do we need to know more about mixed Plasmodium species infections in humans? Trends Parasitol 20: 440–447. doi: 10.1016/j.pt.2004.07.004 15324735

42. Hastings IM, Nsanzabana C, Smith TA (2010) A comparison of methods to detect and quantify the markers of antimalarial drug resistance. Am J Trop Med Hyg 83: 489–495. doi: 10.4269/ajtmh.2010.10-0072 20810808

43. Regev-Rudzki N, Wilson DW, Carvalho TG, Sisquella X, Coleman BM, et al. (2013) Cell-cell communication between malaria-infected red blood cells via exosome-like vesicles. Cell 153: 1120–1133. doi: 10.1016/j.cell.2013.04.029 23683579

44. Pollitt LC, Mideo N, Drew DR, Schneider P, Colegrave N, et al. (2011) Competition and the evolution of reproductive restraint in malaria parasites. Am Nat 177: 358–367. doi: 10.1086/658175 21460544

45. Reece SE, Drew DR, Gardner A (2008) Sex ratio adjustment and kin discrimination in malaria parasites. Nature 453: 609–614. doi: 10.1038/nature06954 18509435

46. Kiwuwa MS, Ribacke U, Moll K, Byarugaba J, Lundblom K, et al. (2013) Genetic diversity of Plasmodium falciparum infections in mild and severe malaria of children from Kampala, Uganda. Parasitol Res 112: 1691–1700. doi: 10.1007/s00436-013-3325-3 23408340

47. Ranjit MR, Das A, Das BP, Das BN, Dash BP, et al. (2005) Distribution of Plasmodium falciparum genotypes in clinically mild and severe malaria cases in Orissa, India. Trans R Soc Trop Med Hyg 99: 389–395. doi: 10.1016/j.trstmh.2004.09.010 15780346

48. Rout R, Mohapatra BN, Kar SK, Ranjit M (2009) Genetic complexity and transmissibility of Plasmodium falciparum parasites causing severe malaria in central-east coast India. Trop Biomed 26: 165–172. 19901903

49. Conway DJ, Greenwood BM, McBride JS (1991) The epidemiology of multiple-clone Plasmodium falciparum infections in Gambian patients. Parasitology 103 Pt 1: 1–6. doi: 10.1017/S0031182000059217 1682870

50. Durand R, Ariey F, Cojean S, Fontanet A, Ranaivo L, et al. (2008) Analysis of circulating populations of Plasmodium falciparum in mild and severe malaria in two different epidemiological patterns in Madagascar. Trop Med Int Health 13: 1392–1399. doi: 10.1111/j.1365-3156.2008.02156.x 18803610

51. Kun JF, Schmidt-Ott RJ, Lehman LG, Lell B, Luckner D, et al. (n.d.) Merozoite surface antigen 1 and 2 genotypes and rosetting of Plasmodium falciparum in severe and mild malaria in Lambaréné, Gabon. Trans R Soc Trop Med Hyg 92: 110–114. doi: 10.1016/S0035-9203(98)90979-8

52. Nielsen MA, Staalsoe T, Kurtzhals JAL, Goka BQ, Dodoo D, et al. (2002) Plasmodium falciparum variant surface antigen expression varies between isolates causing severe and nonsevere malaria and is modified by acquired immunity. J Immunol 168: 3444–3450. doi: 10.4049/jimmunol.168.7.3444 11907103

53. Mayengue PI, Kalmbach Y, Issifou S, Kremsner PG, Ntoumi F (2007) No variation in the prevalence of point mutations in the Pfcrt and Pfmdr1 genes in isolates from Gabonese patients with uncomplicated or severe Plasmodium falciparum malaria. Parasitol Res 100: 487–493. doi: 10.1007/s00436-006-0287-8 17096149

54. A-Elbasit IE, ElGhazali G, A-Elgadir TME, Hamad AA, Babiker HA, et al. (2007) Allelic polymorphism of MSP2 gene in severe P. falciparum malaria in an area of low and seasonal transmission. Parasitol Res 102: 29–34. doi: 10.1007/s00436-007-0716-3 17768641

55. Amodu OK, Oyedeji SI, Ntoumi F, Orimadegun AE, Gbadegesin RA, et al. (2008) Complexity of the msp2 locus and the severity of childhood malaria, in south-western Nigeria. Ann Trop Med Parasitol 102: 95–102. doi: 10.1179/136485908X252340 18318931

56. Robert F, Ntoumi F, Angel G, Candito D, Rogier C, et al. (n.d.) Extensive genetic diversity of Plasmodium falciparum isolates collected from patients with severe malaria in Dakar, Senegal. Trans R Soc Trop Med Hyg 90: 704–711. doi: 10.1016/S0035-9203(96)90446-0

57. Schneider P, Bell AS, Sim DG, O’Donnell AJ, Blanford S, et al. (2012) Virulence, drug sensitivity and transmission success in the rodent malaria, Plasmodium chabaudi. Proc Biol Sci 279: 4677–4685. doi: 10.1098/rspb.2012.1792 23015626

58. De Roode JC, Helinski MEH, Anwar MA, Read AF (2005) Dynamics of multiple infection and within-host competition in genetically diverse malaria infections. Am Nat 166: 531–542. doi: 10.1086/491659 16224719

59. De Roode JC, Culleton R, Cheesman SJ, Carter R, Read AF (2004) Host heterogeneity is a determinant of competitive exclusion or coexistence in genetically diverse malaria infections. Proc Biol Sci 271: 1073–1080. doi: 10.1098/rspb.2004.2695 15293862

60. Wargo AR, de Roode JC, Huijben S, Drew DR, Read AF (2007) Transmission stage investment of malaria parasites in response to in-host competition. Proc Biol Sci 274: 2629–2638. doi: 10.1098/rspb.2007.0873 17711832

61. Baker DA (2010) Malaria gametocytogenesis. Mol Biochem Parasitol 172: 57–65. doi: 10.1016/j.molbiopara.2010.03.019 20381542

62. Culleton RL, Abkallo HM (2014) Malaria parasite genetics: doing something useful. Parasitol Int. doi: 10.1016/j.parint.2014.07.006

63. Yoeli M, Hargreaves B, Carter R, Walliker D (1975) Sudden increase in virulence in a strain of Plasmodium berghei yoelii. Ann Trop Med Parasitol 69: 173–178. 1098585

64. Pattaradilokrat S, Cheesman SJ, Carter R (2008) Congenicity and genetic polymorphism in cloned lines derived from a single isolate of a rodent malaria parasite. Mol Biochem Parasitol 157: 244–247. doi: 10.1016/j.molbiopara.2007.10.011 18068827

65. Inoue M, Tang J, Miyakoda M, Kaneko O, Yui K, et al. (2012) The species specificity of immunity generated by live whole organism immunisation with erythrocytic and pre-erythrocytic stages of rodent malaria parasites and implications for vaccine development. Int J Parasitol 42: 859–870. doi: 10.1016/j.ijpara.2012.07.001 22846785

66. Cheesman SJ, de Roode JC, Read AF, Carter R (2003) Real-time quantitative PCR for analysis of genetically mixed infections of malaria parasites: technique validation and applications. Mol Biochem Parasitol 131: 83–91. doi: 10.1016/S0166-6851(03)00195-6 14511807

67. Mackinnon M, Read A (1999) Genetic relationships between parasite virulence and transmission in rodent malaria Plasmodium chabaudi. Evolution (N Y) 53: 689–703.

68. Carlton JM., Vinkenoog R, Waters AP, Walliker D (1998) Gene synteny in species of Plasmodium. Mol Biochem Parasitol 93: 285–294. doi: 10.1016/S0166-6851(98)00043-7 9662712

69. Abkallo HM, Liu W, Hokama S, Ferreira PE, Nakazawa S, et al. (2014) DNA from pre-erythrocytic stage malaria parasites is detectable by PCR in the faeces and blood of hosts. Int J Parasitol. doi: 10.1016/j.ijpara.2014.03.002 24704779

Štítky
Hygiena a epidemiológia Infekčné lekárstvo Laboratórium

Článok vyšiel v časopise

PLOS Pathogens


2015 Číslo 2
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#