Fitness costs of disrupting circadian rhythms in malaria parasites

Proceedings of the Royal Society B: Biological Sciences

Volumn 278, Issue 1717, 2011, Pages 2429-2436

  O'Donnell, Aidan J ^a   Schneider, Petra ^b   McWatters, Harriet G ^c   Reece, Sarah E ^a,b  

^a Institute of Immunology and Infection Research   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

Biological rhythms; Cell cycle; Periodicity; Plasmodium chabaudi; Plasticity; Synchronicity

Indexed keywords

CIRCADIAN RHYTHM; CYTOLOGY; DISEASE TRANSMISSION; FITNESS; HOST-PARASITE INTERACTION; LIFE HISTORY TRAIT; MALARIA; PATHOGEN; PERIODICITY; PROTOZOAN; RODENT; SURVIVAL; SYNCHRONY;

ANIMAL; ARTICLE; CIRCADIAN RHYTHM; DISEASE TRANSMISSION; EVOLUTION; HOST PARASITE INTERACTION; LIGHT; MALARIA; MALE; MOUSE; PARASITOLOGY; PHOTOPERIODICITY; PHYSIOLOGY; PLASMODIUM CHABAUDI; RADIATION EXPOSURE; REPRODUCTION; REPRODUCTIVE FITNESS; RODENT DISEASE;

ANIMALS; BIOLOGICAL EVOLUTION; CIRCADIAN CLOCKS; CIRCADIAN RHYTHM; GENETIC FITNESS; HOST-PARASITE INTERACTIONS; LIGHT; MALARIA; MALE; MICE; PHOTOPERIOD; PLASMODIUM CHABAUDI; REPRODUCTION; RODENT DISEASES;

PLASMODIUM CHABAUDI; RODENTIA;

EID: 79960127451     PISSN: 09628452     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rspb.2010.2457     Document Type: Article

References (67)

1. Dunlap, J. C., Loros, J. J. & Decoursey, P. J. 2004 Chronobiology: biological time keeping. Sunderland, UK: SinauerAssociates
2. Pittendrigh, C. S. 1960 Circadian rhythms and the circadianorganization of living systems. In Cold Spring Harborsymposium on quantitative biology, pp. 159-184. ColdSpring Harbor, NY: Cold Spring Harbor LaboratoryPress.
3. Ouyang, Y., Andersson, C. R., Kondo, T., Golden, S. S. & Johnson, C. H. 1998 Resonating circadian clocks enhancefitness in cyanobacteria. Proc. Natl Acad. Sci. USA 95,8660-8664. (doi:10.1073/pnas.95.15.8660)
4. Dodd, A. N., Salathia, N., Hall, A., Kevei, E., Toth, R., Nagy, F., Hibberd, J. M., Millar, A. J. & Webb, A. A. R.2005 Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309, 630-633. (doi:10.1126/science.1115581)
5. Saunders, D. S. 1972 Circadian control of larval growth rate in Sarcophaga argyrostoma. Proc. Natl Acad. Sci.USA 69, 2738-2740. (doi:10.1073/pnas.69.9.2738)
6. Yerushalmi, S. & Green, R. M. 2009 Evidence for the adaptive significance of circadian rhythms. Ecol. Lett. 12, 970-981. (doi:10.1111/j.1461-0248.2009.01343.x)
7. Allada, R. & Chung, B. Y. 2010 Circadian organization of behavior and physiology in Drosophila. Annu. Rev. Physiol.72, 605-624. (doi:10.1146/annurev-physiol-021909-135815)
8. Brunner, M. & Kaldi, K. 2008 Interlocked feedback loops of the circadian clock of Neurospora crassa. Mol.Microbiol. 68, 255-262. (doi:10.1111/j.1365-2958.2008.06148.x)
9. Dibner, C., Schibler, U. & Albrecht, U. 2010 Themammalian circadian timing system: organization and coordination of central and peripheral clocks. Annu. Rev. Physiol. 72, 517-549. (doi:10.1146/annurev-physiol-021909-135821)
10. Stelling, J., Gilles, E. D. & Doyle, F. J. 2004 Robustness properties of circadian clock architectures. Proc. NatlAcad. Sci. USA 101, 13210-13215. (doi:10.1073/pnas.0401463101)
11. Troein, C., Locke, J. C. W., Turner, M. S. & Millar, A. J.2009 Weather and seasons together demand complex biological clocks. Curr. Biol. 19, 1961-1964. (doi:10.1016/j.cub.2009.09.024)
12. DeCoursey, P. J., Walker, J. K. & Smith, S. A. 2000 Acir cadian pacemaker in free-living chipmunks: essential for survival? J. Comp. Physiol. A 186, 169-180. (doi:10.1007/s003590050017)
13. Hawking, F. 1970 The clock of the malaria parasite. Sci. Am. 222, 123-131. (doi:10.1038/scientificamerican0670-123)
14. Reece, S. E., Ramiro, R. S. & Nussey, D. H. 2009 Plasticparasites: sophisticated strategies for survival and reproduction? Evol. Appl. 2, 11-23. (doi:10.1111/j.1752-4571.2008.00060.x)
15. Babiker, H. A., Schneider, P. & Reece, S. E. 2008 Gametocytes: insights gained during a decade of molecular monitoring. Trends Parasitol. 24, 525-530. (doi:10.1016/j.pt.2008.08.001)
16. Cheesman, S. J., de Roode, J. C., Read, A. F. & 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)
17. Wargo, A. R., Randle, N., Chan, B. H. K., Thompson, J., Read, A. F. & Babiker, H. A. 2006 Plasmodium chabaudi: reverse transcription PCR for the detection and quantification of transmission stage malaria parasites. Exp. Parasitol. 112, 13-20. (doi:10.1016/j.exppara.2005.08.013)
18. Foster, K. R. 2005 Biomedicine-Hamiltonian medicine: why the social lives of pathogens matter. Science 308,1269-1270. (doi:10.1126/science.1108158)
19. 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)
20. Stearns, S. C. & Koella, J. C. 2008 Evolution in health anddisease. Oxford, UK: Oxford University Press.
21. Gautret, P., Deharo, E., Tahar, R., Chabaud, A. G. & Landau, I. 1995 The adjustment of the schizogonic cycle of Plasmodium chabaudi chabaudi in the blood tothe circadian rhythm of the host. Parasite (Paris, France) 2, 69-74.
22. Taliaferro, L. G. 1928 Return to normal of the asexual cycle in bird malaria after retardation by low temperaturesin vitro. J. Prev. Med. 2, 525-541.
23. Taliaferro, W. H. & Taliaferro, L. G. 1934 Alteration in the time of sporulation of Plasmodium brasilianum inmonkeys by reversal of light and dark. Am. J. Epidemiol.20, 50-59.
24. Trager, W. & Jensen, J. B. 1976 Human malaria parasitesin continuous culture. Science 193, 673-675. (doi:10.1126/science.781840)
25. Hotta, C. T., Gazarini, M. L., Beraldo, F. H., Varotti, F. P., Lopes, C., Markus, R. P., Pozzan, T. & Garcia, C. R. S. 2000 Calcium-dependent modulation by melatoninof the circadian rhythm in malarial parasites. Nat.Cell Biol. 2, 466-468. (doi:10.1038/35017112)
26. Killick-Kendrick, R. & Peters, W. 1978 Rodent malaria.New York, NY: Academic Press.
27. Vitaterna, M. H. et al. 1994 Mutagenesis and mapping ofa mouse gene clock, essential for circadian behavior. Science 264, 719-725. (doi:10.1126/science.8171325)
28. Mackinnon, M. J. & Read, A. F. 1999 Genetic relationshipsbetween parasite virulence and transmission in therodent malaria Plasmodium chabaudi. Evolution 53,689-703. (doi:10.2307/2640710)
29. Wargo, A. R., de Roode, J. C., Huijben, S., Drew, D. R. & Read, A. F. 2007 Transmission stage investment of malariaparasites in response to in-host competition. Proc. R. Soc.B 274, 2629-2638. (doi:10.1098/rspb.2007.0873)
30. Garnham, P. C. C. 1966 Malaria parasites and otherhaemosporidia. Oxford, UK: Blackwell Scientific.
31. Mota, M. M., Jarra, W., Hirst, E., Patnaik, P. K. & Holder, A. A. 2000 Plasmodium chabaudi-infectederythrocytes adhere to CD36 and bind to microvascular endothelial cells in an organ-specific way. Infect. Immun.68, 4135-4144. (doi:10.1128/IAI.68.7.4135-4144.2000)
32. Crawley, M. J. 2007 The R book. Chichester, UK: JohnWiley & Sons Ltd.
33. Bell, A. S., de Roode, J. C., Sim, D. & Read, A. F. 2006 Within-host competition in genetically diverse malariainfections: parasite virulence and competitive success.Evolution 60, 1358-1371.
34. Mackinnon, M. J. & Read, A. F. 2004 Immunity promotesvirulence evolution in a malaria model.PLoS Biol. 2, 1286-1292.(doi:10.1371/journal.pbio.0020230)
35. Reece, S. E., Ali, E., Schneider, P. & Babiker, H. A. 2010 Stress, drugs and the evolution of reproductive restraintin malaria parasites. Proc. R. Soc. B 277, 3123-3129.(doi:10.1098/rspb.2010.0564)
36. Schneider, P., Chan, B. H. K., Reece, S. E. & Read, A. F.2008 Does the drug sensitivity of malaria parasites dependon their virulence? Malar. J 7, 257.(doi:10.1186/1475-2875-7-257)
37. Pollitt, L. C., Mideo, N., Drew, D. R., Colegrave, N. & Reece, S. E. In press. Coping with competition: strategiesfor sex and survival. Am. Nat.
38. de Roode, J. C., Helinski, M. E., Anwar, M. A. & Read, A. F. 2005 Dynamics of multiple infection and withinhostcompetition in genetically diverse malaria infections.Am. Nat. 166, 531-542.(doi:10.1086/491659)
39. de Roode, J. C., Read, A., Chan, B. & Mackinnon, M. J.2003 Rodent malaria parasites suffer from the presenceof conspecific clones in three-clone Plasmodium chabaudiinfections. Parasitology 127, 411-418.(doi:10.1017/S0031182003004001)
40. Drakeley, C., Sutherland, C., Bousema, J. T., Sauerwein, R. W. & Targett, G. A. T. 2006 The epidemiology ofPlasmodium falciparum gametocytes: weapons of massdispersion. Trends Parasitol. 22, 424-430.(doi:10.1016/j.pt.2006.07.001)
41. Mackinnon, M. J. & Read, A. F. 2004 Virulence inmalaria: an evolutionary viewpoint. Phil. Trans. R. Soc.Lond. B 359, 965-986.(doi:10.1098/rstb.2003.1414)
42. Schneider, P., Bousema, J., Gouagna, L. C., Otieno, S., Van De Vegte-Bolmer, M., Omar, S. A. & Sauerwein, R. W. 2007 Submicroscopic Plasmodium falciparumgametocyte densities frequently result in mosquitoinfection. Am. J. Trop. Med. Hyg. 76, 470-474.
43. Keller, M., Mazuch, J., Abraham, U., Eom, G. D., Herzog, E. D., Volk, H. D., Kramer, A. & Maier, B.2009 A circadian clock in macrophages controls inflammatoryimmune responses. Proc. Natl Acad. Sci. USA 106, 21 407-21 412.(doi:10.1073/pnas.0906361106)
44. Peng, Z. C., Kristensson, K. & Bentivoglio, M. 1994 Dysregulation of photic induction of Fos-related proteinin the biological clock during experimental trypanosomiasis.Neurosci. Lett. 182, 104-106. (doi:10.1016/0304-3940(94)90217-8)
45. Sanchez, Y., Rosado, J. D., Vega, L., Elizondo, G., Estrada-Muniz, E., Saavedra, R., Juarez, I. & Rodriguez-Sosa, M. 2010 The unexpected role for thearyl hydrocarbon receptor on susceptibility to experimentaltoxoplasmosis. J. Biomed. Biotechnol. 2010, 505694.(doi:10.1155/2010/505694)
46. Cornford, E. M., Freeman, B. J. & MacInnis, A. J. 1976 Physiological relationships and circadian periodicities inrodent trypanosomes. Trans. R. Soc. Trop. Med. Hyg.70, 238-243.(doi:10.1016/0035-9203(76)90047-X)
47. Fantinou, A. A., Alexandri, M. P. & Tsitsipis, J. A. 1998 Adult emergence rhythm of the egg-parasitoid Telenomusbusseolae. Biocontrol 43, 141-151.(doi:10.1023/A:1009984318289)
48. Toledo, R., Muñoz-Antoli, C. & Esteban, J. G. 1999 Productionand chronobiology of emergence of the cercariaeof Euparyphium albuferensls (Trematoda: Echinostomatidae).J. Parasitol. 85, 263-267.(doi:10.2307/3285630)
49. Leete, T. H. & Rubin, H. 1996 Malaria and the cell cycle.Trends Parasitol. 12, 442-444.
50. Teuscher, F., Gatton, M. L., Chen, N., Peters, J., Kyle D. E. & Cheng, Q. 2010 Artemisinin-induced dormancyin Plasmodium falciparum: duration, recovery rates, andimplications in treatment failure. J. Infect. Dis. 202,1362-1368. (doi:10.1086/656476)
51. Veiga, M. I., Ferreira, P. E., Schmidt, B. A., Ribacke, U.,Bjorkman, A., Tichopad, A. & Gil, J. P. 2010 Antimalarialexposure delays Plasmodium falciparum intra-erythrocyticcycle and drives drug transporter genes expression. PLoSONE 5.(doi:10.1371/journal.pone.0012408)
52. Witkowski, B., Lelievre, J., Barragan, M. J., Laurent, V., Su, X. Z., Berry, A. & Benoit-Vical, F. 2010 Increased toleranceto artemisinin in Plasmodium falciparum is mediatedby a quiescence mechanism. Antimicrob. Agents Chemother.54, 1872-1877 (doi:10.1128/AAC.01636-09)
53. Rouzine, I. M. & McKenzie, F. E. 2003 Link betweenimmune response and parasite synchronization inmalaria. Proc. Natl Acad. Sci. USA 100, 3473-3478. (doi:10.1073/pnas.262796299)
54. Gravenor, M. B. & Kwiatkowski, D. 1998 An analysis ofthe temperature effects of fever on the intra-host populationdynamics of Plasmodium falciparum. Parasitology117, 97-105. (doi:10.1017/S0031182098002893)
55. Kwiatkowski, D. 1989 Febrile temperatures can synchronizethe growth of Plasmodium falciparum in vitro. J. Exp.Med. 169, 357-361. (doi:10.1084/jem.169.1.357)
56. Garnham, P. C. C. &Powers, K. G. 1974 Periodicity ofinfectivity of plasmodial gametocytes: the Hawkingphenomenon. Int. J. Parasitol. 4, 103-106. (doi:10.1016/0020-7519(74)90014-9)
57. Hawking, F., Worms, M. J. & Gammage, K. 1968 24-and 48-hour cycles of malaria parasites in blood-theirpurpose production and control. Trans. R. Soc. Trop.Med. Hyg. 62, 731-760. (doi:10.1016/0035-9203(68)90001-1)
58. Bray, R. S., McCrae, A. W. R. & Smalley, M. E. 1976 Lack of a circadian rhythm in the ability of the gametocytesof Plasmodium falciparum to infect Anophelesgambiae. Int. J. Parasitol. 6, 399-401. (doi:10.1016/0020-7519(76)90025-4)
59. Githeko, A. K., Brandling-Bennett, A. D., Beier, M.,Mbogo, C. M., Atieli, F. K., Owaga, M. L., Juma, F. &Collins, F. H. 2008 Confirmation that Plasmodium falciparumhas aperiodic infectivity to Anopheles gambiae.Med. Vet. Entomol. 7, 373-376. (doi:10.1111/j.1365-2915.1993.tb00708.x)
60. Magesa, S. M.,Mdira, Y.K., Akida, J. A.,Bygbjerg, I.C. & Jakobsen, P. H. 2000 Observations on the periodicity ofPlasmodium falciparum gametocytes in natural humaninfections. Acta Trop. 76, 239-246. (doi:10.1016/S0001-706X(00)00110-8)
61. Smalley, M. E. & Sinden, R. E. 2009 Plasmodiumfalciparum gametocytes: their longevity and infectivity.Parasitology 74, 1-8. (doi:10.1017/S0031182000047478)
62. Clark, R. H. & Korst, D. R. 1969 Circadian periodicity ofbone marrow mitotic activity and reticulocyte counts inrats and mice. Science 166, 236-237. (doi:10.1126/science.166.3902.236)
63. Savill, N. J., Chadwick, W. & Reece, S. E. 2009 Quantitativeanalysis of mechanisms that govern red blood cellage structure and dynamics during anaemia. PLoSComput. Biol. 5, e1000416. (doi:10.1371/journal.pcbi.1000416)
64. Naotunne, T. D., Karunaweera, N. D., Delgiudice, G.,Kularatne, M. U., Grau, G. E., Carter, R. & Mendis, K. N. 1991 Cytokines kill malaria parasites during infectioncrisis-extracellular complementary factors areessential. J. Exp. Med. 173, 523-529. (doi:10.1084/jem.173.3.523)
65. Rosbash, M. 2009 The implications of multiple circadianclock origins. PLoS Biol. 7, 421-425. (doi:10.1371/journal.pbio.1000062)
66. Rand, D. A., Shulgin, B. V., Salazar, D. &Millar, A. J. 2004 Design principles underlying circadian clocks. J. R. Soc.Interface 1, 119-130. (doi:10.1098/rsif.2004.0014)
67. Merrow, M. & Roenneberg, T. 2007 Circadian entrainmentof Neurospora crassa. Clocks Rhythms 72, 279-285.