Time-of-day of infection: impact on liver stage malaria parasites in untreated and drug-treated hosts | Parasites & Vectors

  • Haus EL, Smolensky MH. Shift work and cancer risk: potential mechanistic roles of circadian disruption, light at night, and sleep deprivation. Sleep Med Rev. 2013;17:273–84.

    PubMed 

    Google Scholar 

  • Scheiermann C, Gibbs J, Ince L, Loudon A. Clocking in to immunity. Nat Rev Immunol. 2018;18:423–37.

    CAS 
    PubMed 

    Google Scholar 

  • Gibbs J, Ince L, Matthews L, Mei J, Bell T, Yang N, et al. An epithelial circadian clock controls pulmonary inflammation and glucocorticoid action. Nat Med. 2014;20:919–26.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Curtis AM, Bellet MM, Sassone-Corsi P, O’Neill LA. Circadian clock proteins and immunity. Immunity. 2014;40:178–86.

    CAS 
    PubMed 

    Google Scholar 

  • Borrmann H, McKeating JA, Zhuang X. The circadian clock and viral infections. J Biol Rhythms. 2021;36:9–22.

    CAS 
    PubMed 

    Google Scholar 

  • Westwood ML, O’Donnell AJ, Bekker Cd, Lively CM, Zuk M, Reece SE. The evolutionary ecology of circadian rhythms in infection. Nat Ecol Evol. 2019;3:552–60.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Kiessling S, Dubeau-Laramée G, Ohm H, Labrecque N, Olivier M, Cermakian N. The circadian clock in immune cells controls the magnitude of Leishmania parasite infection. Sci Rep. 2017;7:10892.

    PubMed 
    PubMed Central 

    Google Scholar 

  • O’Donnell AJ, Schneider P, McWatters HG, Reece SE. Fitness costs of disrupting circadian rhythms in malaria parasites. Proc Biol Sci. 2011;278:2429–36.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Prior KF, van der Veen DR, O’Donnell AJ, Cumnock K, Schneider D, Pain A, et al. Timing of host feeding drives rhythms in parasite replication. PLoS Pathog. 2018;14:e1006900.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Hirako IC, Assis PA, Hojo-Souza NS, Reed G, Nakaya H, Golenbock DT, et al. Daily rhythms of TNFα expression and food intake regulate synchrony of Plasmodium stages with the host circadian cycle. Cell Host Microbe. 2018;23:796–808.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Bellet MM, Deriu E, Liu JZ, Grimaldi B, Blaschitz C, Zeller M, et al. Circadian clock regulates the host response to Salmonella. Proc Natl Acad Sci USA. 2013;110:9897–902.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Lundy SR, Ahmad T, Simoneaux T, Benyeogor I, Robinson Y, George Z, et al. Effect of time of day of infection on Chlamydia infectivity and pathogenesis. Sci Rep. 2019;9:11405.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Gagnidze K, Hajdarovic KH, Moskalenko M, Karatsoreos IN, McEwen BS, Bulloch K. Nuclear receptor REV-ERBα mediates circadian sensitivity to mortality in murine vesicular stomatitis virus-induced encephalitis. Proc Natl Acad Sci USA. 2016;113:5730–5.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Lee JE, Edery I. Circadian regulation in the ability of Drosophila to combat pathogenic infections. Curr Biol. 2008;18:195–9.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Edgar RS, Stangherlin A, Nagy AD, Nicoll MP, Efstathiou S, O’Neill JS, et al. Cell autonomous regulation of herpes and influenza virus infection by the circadian clock. Proc Natl Acad Sci USA. 2016;113:10085–90.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Matsuzawa T, Nakamura Y, Ogawa Y, Ishimaru K, Goshima F, Shimada S, et al. Differential day-night outcome to HSV-2 cutaneous infection. J Invest Dermatol. 2018;138:233–6.

    PubMed 

    Google Scholar 

  • Rees H, Rzechorzek NM, Dodd AN, Hodge JJL, Stevenson TJ, Mv S, et al. BioClocksUK: driving robust cycles of discovery to impact. Philos Trans R Soc B Biol Sci. 2025;380:20230345.

    Google Scholar 

  • Sougoufara S, Diedhiou SM, Doucoure S, Diagne N, Sembene PM, Harry M, et al. Biting by Anopheles funestus in broad daylight after use of long-lasting insecticidal nets: a new challenge to malaria elimination. Malar J. 2014;13:125.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Moiroux N, Gomez MB, Pennetier C, Elanga E, Djenontin A, Chandre F, et al. Changes in Anopheles funestus biting behavior following universal coverage of long-lasting insecticidal nets in Benin. J Infect Dis. 2012;206:1622–9.

    CAS 
    PubMed 

    Google Scholar 

  • Sangbakembi-Ngounou C, Costantini C, Longo-Pendy NM, Ngoagouni C, Akone-Ella O, Rahola N, et al. Diurnal biting of malaria mosquitoes in the Central African Republic indicates residual transmission may be “out of control.” Proc Natl Acad Sci USA. 2022;119:e2104282119.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Sherrard-Smith E, Skarp JE, Beale AD, Fornadel C, Norris LC, Moore SJ, et al. Mosquito feeding behavior and how it influences residual malaria transmission across Africa. Proc Natl Acad Sci USA. 2019;116:15086–95.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Hawking F, Worms MJ, Gammage K. 24- and 48-hour cycles of malaria parasites in the blood; their purpose, production and control. Trans R Soc Trop Med Hyg. 1968;62:731–65.

    CAS 
    PubMed 

    Google Scholar 

  • Schneider P, Rund SSC, Smith NL, Prior KF, O’Donnell AJ, Reece SE. Adaptive periodicity in the infectivity of malaria gametocytes to mosquitoes. Proc Biol Sci. 2018;285:20181876.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Habtewold T, Tapanelli S, Masters EKG, Windbichler N, Christophides GK. The circadian clock modulates Anopheles gambiae infection with Plasmodium falciparum. PLoS ONE. 2022;17:e0278484.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Pigeault R, Caudron Q, Nicot A, Rivero A, Gandon S. Timing malaria transmission with mosquito fluctuations. Evol Lett. 2018;2:378–89.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Bento I, Parrington B, Pascual R, Goldberg AS, Wang E, Liu H, et al. Parasite and vector circadian clocks mediate efficient malaria transmission. Nat Microbiol. 2025;10:882–96.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Ezema CA, Okagu IU, Ezeorba TPC. Escaping the enemy’s bullets: an update on how malaria parasites evade host immune response. Parasitol Res. 2023;122:1715–31.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Zhang R, Lahens NF, Ballance HI, Hughes ME, Hogenesch JB. A circadian gene expression atlas in mammals: implications for biology and medicine. Proc Natl Acad Sci USA. 2014;111:16219–24.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Stokkan KA, Yamazaki S, Tei H, Sakaki Y, Menaker M. Entrainment of the circadian clock in the liver by feeding. Science. 2001;291:490–3.

    CAS 
    PubMed 

    Google Scholar 

  • O’Donnell AJ, Prior KF, Reece SE. Host circadian clocks do not set the schedule for the within-host replication of malaria parasites. Proc Biol Sci. 2020;287:20200347.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Owolabi ATY, Reece SE, Schneider P. Daily rhythms of both host and parasite affect antimalarial drug efficacy. Evol Med Public Health. 2021;9:208–19.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Platon L, Leroy D, Fidock DA, Ménard D. Drug-induced stress mediates Plasmodium falciparum ring-stage growth arrest and reduces in vitro parasite susceptibility to artemisinin. Microbiol Spectr. 2024;12:e0350023.

    PubMed 

    Google Scholar 

  • Teuscher F, Gatton ML, Chen N, Peters J, Kyle DE, Cheng Q. Artemisinin-induced dormancy in Plasmodium falciparum: duration, recovery rates, and implications in treatment failure. J Infect Dis. 2010;202:1362–8.

    PubMed 

    Google Scholar 

  • Tucker MS, Mutka T, Sparks K, Patel J, Kyle DE. Phenotypic and genotypic analysis of in vitro selected artemisinin-resistant progeny of Plasmodium falciparum. Antimicrob Agents Chemother. 2012;56:302–14.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Nakazawa S, Maoka T, Uemura H, Ito Y, Kanbara H. Malaria parasites giving rise to recrudescence in vitro. Antimicrob Agents Chemother. 2002;46:958–65.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Roques M, Bindschedler A, Beyeler R, Heussler VT. Same, same but different: exploring Plasmodium cell division during liver stage development. PLOS Pathog. 2023;19:e1011210.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Vvd V, Riede SJ, Gorter JA, Eijer WG, Sellix MT, Menaker M, et al. Cold and hunger induce diurnality in a nocturnal mammal. Proc Natl Acad Sci USA. 2014;111:15256–60.

    Google Scholar 

  • Coleman MD, Mihaly GW, Edwards G, Ward SA, Howells RE, Breckenridge AM. Pyrimethamine pharmacokinetics and its tissue localization in mice: effect of dose size. J Pharm Pharmacol. 1985;37:170–4.

    CAS 
    PubMed 

    Google Scholar 

  • O’Donnell AJ, Reece SE. Ecology of asynchronous asexual replication: the intraerythrocytic development cycle of Plasmodium berghei is resistant to host rhythms. Malar J. 2021;20:105.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Carvalho Cabral P, Weinerman J, Olivier M, Cermakian N. Time of day and circadian disruption influence host response and parasite growth in a mouse model of cerebral malaria. iScience. 2024;27:109684.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Spence PJ, Jarra W, Lévy P, Nahrendorf W, Langhorne J. Mosquito transmission of the rodent malaria parasite Plasmodium chabaudi. Malar J. 2012;11:e407.

    Google Scholar 

  • Foley DH, Harrison G, Murphy JR, Dowler M, Rueda LM, Wilkerson RC. Mosquito bisection as a variable in estimates of PCR-derived malaria sporozoite rates. Malar J. 2012;11:145.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Pichugin A, Krzych U. Detection of Plasmodium berghei and Plasmodium yoelii liver-stage parasite burden by quantitative real-time PCR. New York: Humana Press; 2015.

    Google Scholar 

  • Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleid Acids Res. 2001;29:e45.

    CAS 

    Google Scholar 

  • Chen H, Rangasamy M, Tan SY, Wang H, Siegfried BD. Evaluation of five methods for total DNA extraction from western corn rootworm beetles. PLoS ONE. 2010;5:e11963.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Bell AS, Blanford S, Jenkins N, Thomas MB, Read AF. Real-time quantitative PCR for analysis of candidate fungal biopesticides against malaria: technique validation and first applications. J Invertebr Pathol. 2009;100:160–8.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Churcher TS, Sinden RE, Edwards NJ, Poulton ID, Rampling TW, Brock PM, et al. Probability of transmission of malaria from mosquito to human is regulated by mosquito parasite density in naïve and vaccinated hosts. PLoS Pathog. 2017;13:e1006108.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Andolina C, Graumans W, Guelbeogo M, van Gemert GJ, Ramjith J, Harouna S, et al. Quantification of sporozoite expelling by Anopheles mosquitoes infected with laboratory and naturally circulating P falciparum gametocytes. Elife. 2024;12:90989.

    Google Scholar 

  • R Core Team. R: A Language and Environment for Statistical Computing. 4.3.0 ed: R Foundation for Statistical Computing, Vienna, Austria.; 2023.

  • Anderson DR, Burnham KP. Avoiding pitfalls when using information-theoretic methods. J Wildl Manag. 2002;66:912–8.

    Google Scholar 

  • Prior KF, Middleton B, Owolabi ATY, Westwood ML, Holland J, O’Donnell AJ, et al. Synchrony between daily rhythms of malaria parasites and hosts is driven by an essential amino acid. Wellcome Open Res. 2021;6:186.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Sengupta S, Tang SY, Devine JC, Anderson ST, Nayak S, Zhang SL, et al. Circadian control of lung inflammation in influenza infection. Nat Comm. 2019;10:4107.

    Google Scholar 

  • March S, Nerurkar N, Jain A, Andrus L, Kim D, Whittaker CA, et al. Autonomous circadian rhythms in the human hepatocyte regulate hepatic drug metabolism and inflammatory responses. Sci Adv. 2024;10:9281.

    Google Scholar 

  • Gomes PS, Bhardwaj J, Rivera-Correa J, Freire-De-Lima CG, Morrot A. Immune escape strategies of malaria parasites. Front Microbiol. 2016;7:1617.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Lahree A, Mello-Vieira J, Mota MM. The nutrient games – Plasmodium metabolism during hepatic development. Trends Parasitol. 2023;39:445–60.

    CAS 
    PubMed 

    Google Scholar 

  • Chora ÂF, Mota MM, Prudêncio M. The reciprocal influence of the liver and blood stages of the malaria parasite’s life cycle. Int J Parasitol. 2022;52:711–5.

    PubMed 

    Google Scholar 

  • Rund SSC, Hou TY, Ward SM, Collins FH, Duffield GE. Genome-wide profiling of diel and circadian gene expression in the malaria vector Anopheles gambiae. Proc Natl Acad Sci USA. 2011;108:E421–30.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Schleicher TR, Yang J, Freudzon M, Rembisz A, Craft S, Hamilton M, et al. A mosquito salivary gland protein partially inhibits Plasmodium sporozoite cell traversal and transmission. Nat Comm. 2018;9:2908.

    Google Scholar 

  • Arora G, Chuang YM, Sinnis P, Dimopoulos G, Fikrig E. Malaria: influence of Anopheles mosquito saliva on Plasmodium infection. Trends Immunol. 2023;44:256–65.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • O’Donnell AJ, Rund SSC, Reece SE. Time-of-day of blood-feeding: effects on mosquito life history and malaria transmission. Parasit Vectors. 2019;12:301.

    PubMed 
    PubMed Central 

    Google Scholar 

  • Bogale HN, Pascini TV, Kanatani S, Sá JM, Wellems TE, Sinnis P, et al. Transcriptional heterogeneity and tightly regulated changes in gene expression during Plasmodium berghei sporozoite development. Proc Natl Acad Sci USA. 2021;118:e2023438118.

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Continue Reading