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Malaria Journal
Published in: Malaria Journal 1/2016

Open Access 01-12-2016 | Methodology

An ultrasensitive NanoLuc-based luminescence system for monitoring Plasmodium berghei throughout its life cycle

Authors: Mariana De Niz, Rebecca R. Stanway, Rahel Wacker, Derya Keller, Volker T. Heussler

Published in: Malaria Journal | Issue 1/2016

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Abstract

Background

Bioluminescence imaging is widely used for cell-based assays and animal imaging studies, both in biomedical research and drug development. Its main advantages include its high-throughput applicability, affordability, high sensitivity, operational simplicity, and quantitative outputs. In malaria research, bioluminescence has been used for drug discovery in vivo and in vitro, exploring host-pathogen interactions, and studying multiple aspects of Plasmodium biology. While the number of fluorescent proteins available for imaging has undergone a great expansion over the last two decades, enabling simultaneous visualization of multiple molecular and cellular events, expansion of available luciferases has lagged behind. The most widely used bioluminescent probe in malaria research is the Photinus pyralis firefly luciferase, followed by the more recently introduced Click-beetle and Renilla luciferases. Ultra-sensitive imaging of Plasmodium at low parasite densities has not been previously achieved. With the purpose of overcoming these challenges, a Plasmodium berghei line expressing the novel ultra-bright luciferase enzyme NanoLuc, called PbNLuc has been generated, and is presented in this work.

Results

NanoLuc shows at least 150 times brighter signal than firefly luciferase in vitro, allowing single parasite detection in mosquito, liver, and sexual and asexual blood stages. As a proof-of-concept, the PbNLuc parasites were used to image parasite development in the mosquito, liver and blood stages of infection, and to specifically explore parasite liver stage egress, and pre-patency period in vivo.

Conclusions

PbNLuc is a suitable parasite line for sensitive imaging of the entire Plasmodium life cycle. Its sensitivity makes it a promising line to be used as a reference for drug candidate testing, as well as the characterization of mutant parasites to explore the function of parasite proteins, host-parasite interactions, and the better understanding of Plasmodium biology. Since the substrate requirements of NanoLuc are different from those of firefly luciferase, dual bioluminescence imaging for the simultaneous characterization of two lines, or two separate biological processes, is possible, as demonstrated in this work.
Literature
1.
WHO. World Malaria Report. Geneva: World Health Organization; 2015.
2.
Waheed AA, Ghanchi NK, Rehman KA, Raza A, Mahmood SF, Beg MA. Vivax malaria and chloroquine resistance: a neglected disease as an emerging threat. Malar J. 2015;14:146.PubMedPubMedCentralCrossRef
3.
Tanner M, Greenwood B, Whitty CJ, Ansah EK, Price RN, Dondorp AM, et al. Malaria eradication and elimination: views on how to translate a vision into reality. BMC Med. 2015;13:167.PubMedPubMedCentralCrossRef
4.
Craig AG, Grau GE, Janse C, Kazura JW, Milner D, Barnwell JW, et al. The role of animal models for research on severe malaria. PLoS Pathog. 2012;8:e1002401.PubMedPubMedCentralCrossRef
5.
Goodman AL, Forbes EK, Williams AR, Douglas AD, de Cassan SC, Bauza K, et al. The utility of Plasmodium berghei as a rodent model for anti-merozoite malaria vaccine assessment. Sci Rep. 2013;3:1706.PubMedPubMedCentralCrossRef
6.
Wykes MN, Good MF. What have we learnt from mouse models for the study of malaria? Eur J Immunol. 2009;39:2004–7.PubMedCrossRef
7.
Siciliano G, Alano P. Enlightening the malaria parasite life cycle: bioluminescent Plasmodium in fundamental and applied research. Front Microbiol. 2015;6:391.PubMedPubMedCentralCrossRef
8.
Annoura T, Chevalley S, Janse CJ, Franke-Fayard B, Khan SM. Quantitative analysis of Plasmodium berghei liver stages by bioluminescence imaging. Methods Mol Biol. 2013;923:429–43.PubMedCrossRef
9.
Manzoni G, Briquet S, Risco-Castillo V, Gaultier C, Topcu S, Ivanescu ML, et al. A rapid and robust selection procedure for generating drug-selectable marker-free recombinant malaria parasites. Sci Rep. 2014;4:4760.PubMedPubMedCentralCrossRef
10.
Miller JL, Murray S, Vaughan AM, Harupa A, Sack B, Baldwin M, et al. Quantitative bioluminescent imaging of pre-erythrocytic malaria parasite infection using luciferase-expressing Plasmodium yoelii. PLoS ONE. 2013;8:e60820.PubMedPubMedCentralCrossRef
11.
Mwakingwe A, Ting LM, Hochman S, Chen J, Sinnis P, Kim K. Noninvasive real-time monitoring of liver-stage development of bioluminescent Plasmodium parasites. J Infect Dis. 2009;200:1470–8.PubMedCrossRef
12.
Ploemen IH, Chakravarty S, van Gemert GJ, Annoura T, Khan SM, Janse CJ, et al. Plasmodium liver load following parenteral sporozoite administration in rodents. Vaccine. 2013;31:3410–6.PubMedCrossRef
13.
Ploemen IH, Prudencio M, Douradinha BG, Ramesar J, Fonager J, van Gemert GJ, et al. Visualisation and quantitative analysis of the rodent malaria liver stage by real time imaging. PLoS ONE. 2009;4:e7881.PubMedPubMedCentralCrossRef
14.
Vaughan AM, Mikolajczak SA, Camargo N, Lakshmanan V, Kennedy M, Lindner SE, et al. A transgenic Plasmodium falciparum NF54 strain that expresses GFP-luciferase throughout the parasite life cycle. Mol Biochem Parasitol. 2012;186:143–7.PubMedCrossRef
15.
Zuzarte-Luis V, Sales-Dias J, Mota MM. Simple, sensitive and quantitative bioluminescence assay for determination of malaria pre-patent period. Malar J. 2014;13:15.PubMedPubMedCentralCrossRef
16.
Fonager J, Pasini EM, Braks JA, Klop O, Ramesar J, Remarque EJ, et al. Reduced CD36-dependent tissue sequestration of Plasmodium-infected erythrocytes is detrimental to malaria parasite growth in vivo. J Exp Med. 2012;209:93–107.PubMedPubMedCentralCrossRef
17.
Franke-Fayard B, Janse CJ, Cunha-Rodrigues M, Ramesar J, Buscher P, Que I, et al. Murine malaria parasite sequestration: CD36 is the major receptor, but cerebral pathology is unlinked to sequestration. Proc Natl Acad Sci USA. 2005;102:11468–73.PubMedPubMedCentralCrossRef
18.
Pasini EM, Braks JA, Fonager J, Klop O, Aime E, Spaccapelo R, et al. Proteomic and genetic analyses demonstrate that Plasmodium berghei blood stages export a large and diverse repertoire of proteins. Mol Cell Proteomics. 2013;12:426–48.PubMedPubMedCentralCrossRef
19.
Franke-Fayard B, Waters AP, Janse CJ. Real-time in vivo imaging of transgenic bioluminescent blood stages of rodent malaria parasites in mice. Nat Protoc. 2006;1:476–85.PubMedCrossRef
20.
Adjalley SH, Johnston GL, Li T, Eastman RT, Ekland EH, Eappen AG, et al. Quantitative assessment of Plasmodium falciparum sexual development reveals potent transmission-blocking activity by methylene blue. Proc Natl Acad Sci USA. 2011;108:E1214–23.PubMedPubMedCentralCrossRef
21.
Bischoff E, Guillotte M, Mercereau-Puijalon O, Bonnefoy S. A member of the Plasmodium falciparum Pf60 multigene family codes for a nuclear protein expressed by readthrough of an internal stop codon. Mol Microbiol. 2000;35:1005–16.PubMedCrossRef
22.
Calderwood MS, Gannoun-Zaki L, Wellems TE, Deitsch KW. Plasmodium falciparum var genes are regulated by two regions with separate promoters, one upstream of the coding region and a second within the intron. J Biol Chem. 2003;278:34125–32.PubMedCrossRef
23.
de Koning-Ward TF, Speranca MA, Waters AP, Janse CJ. Analysis of stage specificity of promoters in Plasmodium berghei using luciferase as a reporter. Mol Biochem Parasitol. 1999;100:141–6.PubMedCrossRef
24.
De Niz M, Helm S, Horstmann S, Annoura T, Del Portillo HA, Khan SM, Heussler VT. In vivo and in vitro characterization of a Plasmodium liver stage-specific promoter. PLoS ONE. 2015;10:e0123473.PubMedPubMedCentralCrossRef
25.
Deitsch KW, del Pinal A, Wellems TE. Intra-cluster recombination and var transcription switches in the antigenic variation of Plasmodium falciparum. Mol Biochem Parasitol. 1999;101:107–16.PubMedCrossRef
26.
27.
Frank M, Deitsch K. Activation, silencing and mutually exclusive expression within the var gene family of Plasmodium falciparum. Int J Parasitol. 2006;36:975–85.PubMedCrossRef
28.
Helm S, Lehmann C, Nagel A, Stanway RR, Horstmann S, Llinas M, et al. Identification and characterization of a liver stage-specific promoter region of the malaria parasite Plasmodium. PLoS ONE. 2010;5:e13653.PubMedPubMedCentralCrossRef
29.
Lopez-Estrano C, Gopalakrishnan AM, Semblat JP, Fergus MR, Mazier D, Haldar K. An enhancer-like region regulates hrp3 promoter stage-specific gene expression in the human malaria parasite Plasmodium falciparum. Biochim Biophys Acta. 2007;1769:506–13.PubMedPubMedCentralCrossRef
30.
Mair GR, Braks JA, Garver LS, Wiegant JC, Hall N, Dirks RW, et al. Regulation of sexual development of Plasmodium by translational repression. Science. 2006;313:667–9.PubMedPubMedCentralCrossRef
31.
Oguariri RM, Dunn JM, Golightly LM. 3′ gene regulatory elements required for expression of the Plasmodium falciparum developmental protein, Pfs25. Mol Biochem Parasitol. 2006;146:163–72.PubMedCrossRef
32.
Patakottu BR, Singh PK, Malhotra P, Chauhan VS, Patankar S. In vivo analysis of translation initiation sites in Plasmodium falciparum. Mol Biol Rep. 2012;39:2225–32.PubMedCrossRef
33.
Zhang X, Tolzmann CA, Melcher M, Haas BJ, Gardner MJ, Smith JD, et al. Branch point identification and sequence requirements for intron splicing in Plasmodium falciparum. Eukaryot Cell. 2011;10:1422–8.PubMedPubMedCentralCrossRef
34.
Bergmann-Leitner E, Li Q, Caridha D, O’Neil MT, Ockenhouse CF, Hickman M, et al. Protective immune mechanisms against pre-erythrocytic forms of Plasmodium berghei depend on the target antigen. Trials Vaccinol. 2014;3:6–10.CrossRef
35.
Derbyshire ER, Prudencio M, Mota MM, Clardy J. Liver-stage malaria parasites vulnerable to diverse chemical scaffolds. Proc Natl Acad Sci USA. 2012;109:8511–6.PubMedPubMedCentralCrossRef
36.
Lacrue AN, Saenz FE, Cross RM, Udenze KO, Monastyrskyi A, Stein S, et al. 4(1H)-Quinolones with liver stage activity against Plasmodium berghei. Antimicrob Agents Chemother. 2013;57:417–24.PubMedPubMedCentralCrossRef
37.
Marcsisin SR, Sousa JC, Reichard GA, Caridha D, Zeng Q, Roncal N, et al. Tafenoquine and NPC-1161B require CYP 2D metabolism for anti-malarial activity: implications for the 8-aminoquinoline class of anti-malarial compounds. Malar J. 2014;13:2.PubMedPubMedCentralCrossRef
38.
Meister S, Plouffe DM, Kuhen KL, Bonamy GM, Wu T, Barnes SW, et al. Imaging of Plasmodium liver stages to drive next-generation antimalarial drug discovery. Science. 2011;334:1372–7.PubMedPubMedCentralCrossRef
39.
Prado M, Eickel N, De Niz M, Heitmann A, Agop-Nersesian C, Wacker R, et al. Long-term live imaging reveals cytosolic immune responses of host hepatocytes against Plasmodium infection and parasite escape mechanisms. Autophagy. 2015;11:1561–79.PubMedPubMedCentralCrossRef
40.
Ramalhete C, da Cruz FP, Lopes D, Mulhovo S, Rosario VE, Prudencio M, et al. Triterpenoids as inhibitors of erythrocytic and liver stages of Plasmodium infections. Bioorg Med Chem. 2011;19:7474–81.PubMedCrossRef
41.
Cui L, Miao J, Wang J, Li Q, Cui L. Plasmodium falciparum: development of a transgenic line for screening antimalarials using firefly luciferase as the reporter. Exp Parasitol. 2008;120:80–7.PubMedPubMedCentralCrossRef
42.
Franke-Fayard B, Djokovic D, Dooren MW, Ramesar J, Waters AP, Falade MO, et al. Simple and sensitive antimalarial drug screening in vitro and in vivo using transgenic luciferase expressing Plasmodium berghei parasites. Int J Parasitol. 2008;38:1651–62.PubMedCrossRef
43.
Lin JW, Sajid M, Ramesar J, Khan SM, Janse CJ, Franke-Fayard B. Screening inhibitors of P. berghei blood stages using bioluminescent reporter parasites. Methods Mol Biol. 2013;923:507–22.PubMedCrossRef
44.
Lucumi E, Darling C, Jo H, Napper AD, Chandramohanadas R, Fisher N, et al. Discovery of potent small-molecule inhibitors of multidrug-resistant Plasmodium falciparum using a novel miniaturized high-throughput luciferase-based assay. Antimicrob Agents Chemother. 2010;54:3597–604.PubMedPubMedCentralCrossRef
45.
Myrick A, Munasinghe A, Patankar S, Wirth DF. Mapping of the Plasmodium falciparum multidrug resistance gene 5′-upstream region, and evidence of induction of transcript levels by antimalarial drugs in chloroquine sensitive parasites. Mol Microbiol. 2003;49:671–83.PubMedCrossRef
46.
Waller KL, Muhle RA, Ursos LM, Horrocks P, Verdier-Pinard D, Sidhu AB, et al. Chloroquine resistance modulated in vitro by expression levels of the Plasmodium falciparum chloroquine resistance transporter. J Biol Chem. 2003;278:33593–601.PubMedCrossRef
47.
Cevenini L, Camarda G, Michelini E, Siciliano G, Calabretta MM, Bona R, et al. Multicolor bioluminescence boosts malaria research: quantitative dual-color assay and single-cell imaging in Plasmodium falciparum parasites. Anal Chem. 2014;86:8814–21.PubMedPubMedCentralCrossRef
48.
Lucantoni L, Duffy S, Adjalley SH, Fidock DA, Avery VM. Identification of MMV malaria box inhibitors of Plasmodium falciparum early-stage gametocytes using a luciferase-based high-throughput assay. Antimicrob Agents Chemother. 2013;57:6050–62.PubMedPubMedCentralCrossRef
49.
Lucantoni L, Fidock DA, Avery VM. Luciferase-based, high-throughput assay for screening and profiling transmission-blocking compounds against Plasmodium falciparum gametocytes. Antimicrob Agents Chemother. 2016;60:2097–107.PubMedCrossRef
50.
Stone WJ, Churcher TS, Graumans W, van Gemert GJ, Vos MW, Lanke KH, et al. A scalable assessment of Plasmodium falciparum transmission in the standard membrane-feeding assay, using transgenic parasites expressing green fluorescent protein-luciferase. J Infect Dis. 2014;210:1456–63.PubMedCrossRef
51.
Annoura T, Ploemen IH, van Schaijk BC, Sajid M, Vos MW, van Gemert GJ, et al. Assessing the adequacy of attenuation of genetically modified malaria parasite vaccine candidates. Vaccine. 2012;30:2662–70.PubMedCrossRef
52.
Spaccapelo R, Janse CJ, Caterbi S, Franke-Fayard B, Bonilla JA, Syphard LM, et al. Plasmepsin 4-deficient Plasmodium berghei are virulence attenuated and induce protective immunity against experimental malaria. Am J Pathol. 2010;176:205–17.PubMedPubMedCentralCrossRef
53.
Claser C, Malleret B, Gun SY, Wong AY, Chang ZW, Teo P, et al. CD8+ T cells and IFN-gamma mediate the time-dependent accumulation of infected red blood cells in deep organs during experimental cerebral malaria. PLoS ONE. 2011;6:e18720.PubMedPubMedCentralCrossRef
54.
Ploemen I, Behet M, Nganou-Makamdop K, van Gemert GJ, Bijker E, Hermsen C, et al. Evaluation of immunity against malaria using luciferase-expressing Plasmodium berghei parasites. Malar J. 2011;10:350.PubMedPubMedCentralCrossRef
55.
Sack BK, Miller JL, Vaughan AM, Douglass A, Kaushansky A, Mikolajczak S, et al. Model for in vivo assessment of humoral protection against malaria sporozoite challenge by passive transfer of monoclonal antibodies and immune serum. Infect Immun. 2014;82:808–17.PubMedPubMedCentralCrossRef
56.
Matsuoka H, Tomita H, Hattori R, Arai M, Hirai M. Visualization of malaria parasites in the skin using the luciferase transgenic parasite. Plasmodium berghei. Trop Med Health. 2015;43:53–61.PubMedPubMedCentralCrossRef
57.
de Wet JR, Wood KV, DeLuca M, Helinski DR, Subramani S. Firefly luciferase gene: structure and expression in mammalian cells. Mol Cell Biol. 1987;7:725–37.PubMedPubMedCentralCrossRef
58.
de Wet JR, Wood KV, Helinski DR, DeLuca M. Cloning of firefly luciferase cDNA and the expression of active luciferase in Escherichia coli. Proc Natl Acad Sci USA. 1985;82:7870–3.PubMedPubMedCentralCrossRef
59.
Karkhanis YD, Cormier MJ. Isolation and properties of Renilla reniformis luciferase, a low molecular weight energy conversion enzyme. Biochemistry. 1971;10:317–26.PubMedCrossRef
60.
Lorenz WW, McCann RO, Longiaru M, Cormier MJ. Isolation and expression of a cDNA encoding Renilla reniformis luciferase. Proc Natl Acad Sci USA. 1991;88:4438–42.PubMedPubMedCentralCrossRef
61.
Wood KV, Lam YA, McElroy WD, Seliger HH. Bioluminescent click beetles revisited. J Biolumin Chemilumin. 1989;4:31–9.PubMedCrossRef
62.
Wood KV, Lam YA, Seliger HH, McElroy WD. Complementary DNA coding click beetle luciferases can elicit bioluminescence of different colors. Science. 1989;244:700–2.PubMedCrossRef
63.
64.
65.
66.
67.
68.
69.
70.
Hall MP, Unch J, Binkowski BF, Valley MP, Butler BL, Wood MG, et al. Engineered luciferase reporter from a deep sea shrimp utilizing a novel imidazopyrazinone substrate. ACS Chem Biol. 2012;7:1848–57.PubMedPubMedCentralCrossRef
71.
Chen S, Bagdasarian M, Walker ED. Elizabethkingia anophelis: molecular manipulation and interactions with mosquito hosts. Appl Environ Microbiol. 2015;81:2233–43.PubMedPubMedCentralCrossRef
72.
Germain-Genevois C, Garandeau O, Couillaud F. Detection of brain tumors and systemic metastases using NanoLuc and Fluc for dual reporter imaging. Mol Imaging Biol. 2016;18:62–9.PubMedCrossRef
73.
Karlsson EA, Meliopoulos VA, Savage C, Livingston B, Mehle A, Schultz-Cherry S. Visualizing real-time influenza virus infection, transmission and protection in ferrets. Nat Commun. 2015;6:6378.PubMedPubMedCentralCrossRef
74.
Schaub FX, Reza MS, Flaveny CA, Li W, Musicant AM, Hoxha S, et al. Fluorophore-NanoLuc BRET Reporters enable sensitive in vivo optical imaging and flow cytometry for monitoring tumorigenesis. Cancer Res. 2015;75:5023–33.PubMedCrossRef
75.
Seay K, Khajoueinejad N, Zheng JH, Kiser P, Ochsenbauer C, Kappes JC, et al. The vaginal acquisition and dissemination of HIV-1 infection in a novel transgenic mouse model is facilitated by coinfection with Herpes Simplex Virus 2 and is inhibited by microbicide treatment. J Virol. 2015;89:9559–70.PubMedPubMedCentralCrossRef
76.
Stacer AC, Nyati S, Moudgil P, Iyengar R, Luker KE, Rehemtulla A, et al. NanoLuc reporter for dual luciferase imaging in living animals. Mol Imaging. 2013;12:1–13.PubMedPubMedCentral
77.
Sun C, Gardner CL, Watson AM, Ryman KD, Klimstra WB. Stable, high-level expression of reporter proteins from improved alphavirus expression vectors to track replication and dissemination during encephalitic and arthritogenic disease. J Virol. 2014;88:2035–46.PubMedPubMedCentralCrossRef
78.
Tran V, Moser LA, Poole DS, Mehle A. Highly sensitive real-time in vivo imaging of an influenza reporter virus reveals dynamics of replication and spread. J Virol. 2013;87:13321–9.PubMedPubMedCentralCrossRef
79.
Chen S, Kaufman MG, Korir ML, Walker ED. Ingestibility, digestibility, and engineered biological control potential of Flavobacterium hibernum, isolated from larval mosquito habitats. Appl Environ Microbiol. 2014;80:1150–8.PubMedPubMedCentralCrossRef
80.
Chen Y, Wang L, Cheng X, Ge X, Wang P. An ultrasensitive system for measuring the USPs and OTULIN activity using Nanoluc as a reporter. Biochem Biophys Res Commun. 2014;455:178–83.PubMedCrossRef
81.
He SX, Song G, Shi JP, Guo YQ, Guo ZY. Nanoluciferase as a novel quantitative protein fusion tag: application for overexpression and bioluminescent receptor-binding assays of human leukemia inhibitory factor. Biochimie. 2014;106:140–8.PubMedCrossRef
82.
Heise K, Oppermann H, Meixensberger J, Gebhardt R, Gaunitz F. Dual luciferase assay for secreted luciferases based on Gaussia and NanoLuc. Assay Drug Dev Technol. 2013;11:244–52.PubMedCrossRef
83.
Hikiji T, Norisada J, Hirata Y, Okuda K, Nagasawa H, Ishigaki S, et al. A highly sensitive assay of IRE1 activity using the small luciferase NanoLuc: evaluation of ALS-related genetic and pathological factors. Biochem Biophys Res Commun. 2015;463:881–7.PubMedCrossRef
84.
Ho PI, Yue K, Pandey P, Breault L, Harbinski F, McBride AJ, et al. Reporter enzyme inhibitor study to aid assembly of orthogonal reporter gene assays. ACS Chem Biol. 2013;8:1009–17.PubMedCrossRef
85.
Liu Y, Shao XX, Zhang L, Song G, Liu YL, Xu ZG, et al. Novel bioluminescent receptor-binding assays for peptide hormones: using ghrelin as a model. Amino Acids. 2015;47:2237–43.PubMedCrossRef
86.
Machleidt T, Woodroofe CC, Schwinn MK, Mendez J, Robers MB, Zimmerman K, et al. NanoBRET–a novel BRET platform for the analysis of protein-protein interactions. ACS Chem Biol. 2015;10:1797–804.PubMedCrossRef
87.
Morath V, Truong DJ, Albrecht F, Polte I, Ciccone RA, Funke LF, et al. Design and characterization of a modular membrane protein anchor to functionalize the moss Physcomitrella patens with extracellular catalytic and/or binding activities. ACS Synth Biol. 2014;3:990–4.PubMedCrossRef
88.
Norisada J, Hirata Y, Amaya F, Kiuchi K, Oh-hashi K. A sensitive assay for the biosynthesis and secretion of MANF using NanoLuc activity. Biochem Biophys Res Commun. 2014;449:483–9.PubMedCrossRef
89.
Robers MB, Binkowski BF, Cong M, Zimprich C, Corona C, McDougall M, et al. A luminescent assay for real-time measurements of receptor endocytosis in living cells. Anal Biochem. 2015;489:1–8.PubMedCrossRef
90.
Shigeto H, Ikeda T, Kuroda A, Funabashi H. A BRET-based homogeneous insulin assay using interacting domains in the primary binding site of the insulin receptor. Anal Chem. 2015;87:2764–70.PubMedCrossRef
91.
Song G, Jiang Q, Xu T, Liu YL, Xu ZG, Guo ZY. A convenient luminescence assay of ferroportin internalization to study its interaction with hepcidin. FEBS J. 2013;280:1773–81.PubMedCrossRef
92.
Song G, Wu QP, Xu T, Liu YL, Xu ZG, Zhang SF, et al. Quick preparation of nanoluciferase-based tracers for novel bioluminescent receptor-binding assays of protein hormones: using erythropoietin as a model. J Photochem Photobiol B. 2015;153:311–6.PubMedCrossRef
93.
Stoddart LA, Johnstone EK, Wheal AJ, Goulding J, Robers MB, Machleidt T, et al. Application of BRET to monitor ligand binding to GPCRs. Nat Methods. 2015;12:661–3.PubMedPubMedCentralCrossRef
94.
Tuckow AP, Temeyer KB. Discovery, adaptation and transcriptional activity of two tick promoters: construction of a dual luciferase reporter system for optimization of RNA interference in Rhipicephalus (Boophilus) microplus cell lines. Insect Mol Biol. 2015;24:454–66.PubMedCrossRef
95.
Zhang L, Song G, Xu T, Wu QP, Shao XX, Liu YL, et al. A novel ultrasensitive bioluminescent receptor-binding assay of INSL3 through chemical conjugation with nanoluciferase. Biochimie. 2013;95:2454–9.PubMedCrossRef
96.
Zhao J, Nelson TJ, Vu Q, Truong T, Stains CI. Self-assembling NanoLuc luciferase fragments as probes for protein aggregation in living cells. ACS Chem Biol. 2015;11:132–8.PubMedCrossRef
97.
Azevedo MF, Nie CQ, Elsworth B, Charnaud SC, Sanders PR, Crabb BS, et al. Plasmodium falciparum transfected with ultra bright NanoLuc luciferase offers high sensitivity detection for the screening of growth and cellular trafficking inhibitors. PLoS ONE. 2014;9:e112571.PubMedPubMedCentralCrossRef
98.
Burda PC, Roelli MA, Schaffner M, Khan SM, Janse CJ, Heussler VT. A Plasmodium phospholipase is involved in disruption of the liver stage parasitophorous vacuole membrane. PLoS Pathog. 2015;11:e1004760.PubMedPubMedCentralCrossRef
99.
Janse CJ, Ramesar J, Waters AP. High-efficiency transfection and drug selection of genetically transformed blood stages of the rodent malaria parasite Plasmodium berghei. Nat Protoc. 2006;1:346–56.PubMedCrossRef
100.
Stanway RR, Graewe S, Rennenberg A, Helm S, Heussler VT. Highly efficient subcloning of rodent malaria parasites by injection of single merosomes or detached cells. Nat Protoc. 2009;4:1433–9.PubMedCrossRef
101.
Sturm A, Amino R, van de Sand C, Regen T, Retzlaff S, Rennenberg A, et al. Manipulation of host hepatocytes by the malaria parasite for delivery into liver sinusoids. Science. 2006;313:1287–90.PubMedCrossRef
102.
Molina-Cruz A, Lehmann T, Knockel J. Could culicine mosquitoes transmit human malaria? Trends Parasitol. 2013;29:530–7.PubMedCrossRef
103.
Delves MJ, Sinden RE. A semi-automated method for counting fluorescent malaria oocysts increases the throughput of transmission blocking studies. Malar J. 2010;9:35.PubMedPubMedCentralCrossRef
104.
Graewe S, Stanway RR, Rennenberg A, Heussler VT. Chronicle of a death foretold: plasmodium liver stage parasites decide on the fate of the host cell. FEMS Microbiol Rev. 2012;36:111–30.PubMedCrossRef
105.
Vos MW, Stone WJ, Koolen KM, van Gemert GJ, van Schaijk B, Leroy D, et al. A semi-automated luminescence based standard membrane feeding assay identifies novel small molecules that inhibit transmission of malaria parasites by mosquitoes. Sci Rep. 2015;5:18704.PubMedPubMedCentralCrossRef
106.
Golenda CF, Burge R, Schneider I. Plasmodium falciparum and P. berghei: detection of sporozoites and the circumsporozoite proteins in the saliva of Anopheles stephensi mosquitoes. Parasitol Res. 1992;78:563–9.PubMedCrossRef
107.
Medica DL, Sinnis P. Quantitative dynamics of Plasmodium yoelii sporozoite transmission by infected anopheline mosquitoes. Infect Immun. 2005;73:4363–9.PubMedPubMedCentralCrossRef
108.
Engelmann S, Sinnis P, Matuschewski K. Transgenic Plasmodium berghei sporozoites expressing beta-galactosidase for quantification of sporozoite transmission. Mol Biochem Parasitol. 2006;146:30–7.PubMedPubMedCentralCrossRef
109.
Menard R, Tavares J, Cockburn I, Markus M, Zavala F, Amino R. Looking under the skin: the first steps in malarial infection and immunity. Nat Rev Microbiol. 2013;11:701–12.PubMedCrossRef
110.
Baer K, Klotz C, Kappe SH, Schnieder T, Frevert U. Release of hepatic Plasmodium yoelii merozoites into the pulmonary microvasculature. PLoS Pathog. 2007;3:e171.PubMedPubMedCentralCrossRef
111.
Dacres H, Dumancic MM, Horne I, Trowell SC. Direct comparison of bioluminescence-based resonance energy transfer methods for monitoring of proteolytic cleavage. Anal Biochem. 2009;385:194–202.PubMedCrossRef
112.
Dacres H, Michie M, Anderson A, Trowell SC. Advantages of substituting bioluminescence for fluorescence in a resonance energy transfer-based periplasmic binding protein biosensor. Biosens Bioelectron. 2013;41:459–64.PubMedCrossRef
113.
Dacres H, Michie M, Wang J, Pfleger KD, Trowell SC. Effect of enhanced Renilla luciferase and fluorescent protein variants on the Forster distance of Bioluminescence resonance energy transfer (BRET). Biochem Biophys Res Commun. 2012;425:625–9.PubMedCrossRef
114.
Dacres H, Wang J, Leitch V, Horne I, Anderson AR, Trowell SC. Greatly enhanced detection of a volatile ligand at femtomolar levels using bioluminescence resonance energy transfer (BRET). Biosens Bioelectron. 2011;29:119–24.PubMedCrossRef
115.
Pfleger KD, Dromey JR, Dalrymple MB, Lim EM, Thomas WG, Eidne KA. Extended bioluminescence resonance energy transfer (eBRET) for monitoring prolonged protein-protein interactions in live cells. Cell Signal. 2006;18:1664–70.PubMedCrossRef
116.
Pfleger KD, Eidne KA. Illuminating insights into protein-protein interactions using bioluminescence resonance energy transfer (BRET). Nat Methods. 2006;3:165–74.PubMedCrossRef
117.
Pfleger KD, Seeber RM, Eidne KA. Bioluminescence resonance energy transfer (BRET) for the real-time detection of protein-protein interactions. Nat Protoc. 2006;1:337–45.PubMedCrossRef
118.
119.
Caysa H, Jacob R, Muther N, Branchini B, Messerle M, Soling A. A redshifted codon-optimized firefly luciferase is a sensitive reporter for bioluminescence imaging. Photochem Photobiol Sci. 2009;8:52–6.PubMedCrossRef
Metadata
Title
An ultrasensitive NanoLuc-based luminescence system for monitoring Plasmodium berghei throughout its life cycle
Authors
Mariana De Niz
Rebecca R. Stanway
Rahel Wacker
Derya Keller
Volker T. Heussler
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Malaria Journal / Issue 1/2016
Electronic ISSN: 1475-2875
DOI
https://doi.org/10.1186/s12936-016-1291-9

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