Killing the hypnozoite – drug discovery approaches to prevent relapse in Plasmodium vivax

References

• Molyneux ME. History of discoveries, malaria. Encycl Malar. 2014;1–10.
   Google Scholar
• Grassi B, Feletti R. Sui parassiti della malaria. Rif Med. 1890;6:62–4.
   Google Scholar
• Thayer W. Lectures on the malarial fevers. New York: Appleton; 1897.
   Google Scholar
• Rodrigues T, Prudêncio M, Moreira R, Mota MM, Lopes F. Targeting the liver stage of malaria parasites: a yet unmet goal. J Med Chem [Internet]. 2011;55(3):995–1012, [cited 2012 Jul 18]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22122518.
   PubMed Web of Science ®Google Scholar
• Douglas NM, Simpson JA, Phyo AP, Siswantoro H, Hasugian AR, Kenangalem E, et al. Gametocyte dynamics and the role of drugs in reducing the transmission potential of Plasmodium vivax. J Infect Dis [Internet]. 2013;208(5):801–812, [cited 2013 Aug 26]. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid = 3733516&tool = pmcentrez&rendertype = abstract.
   PubMed Web of Science ®Google Scholar
• Markus MB. Malaria: origin of the term “Hypnozoite”. J Hist Biol [Internet]. 2010;., [cited 2011 Nov 16]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/20665090.
   Google Scholar
• Mueller Y, Zimmerman PA, Reeder JC. Plasmodium malariae and Plasmodium ovale – the “bashful” malaria parasites. Trends Parasitol. 2007;23(6):278–83.
   PubMed Web of Science ®Google Scholar
• Collins WE, Jeffery GM. Plasmodium ovale: parasite and disease. Clin Microbiol Rev. 2005;18(3):570.
   PubMed Web of Science ®Google Scholar
• Baird JK. Malaria caused by Plasmodium vivax: recurrent, difficult to treat, disabling, and threatening to life – averting the infectious bite preempts these hazards. Pathog Glob Health [Internet]. 2013;107:475–479, Available from: http://www.scopus.com/inward/record.url?eid = 2-s2.0-84892713548&partnerID = 40&md5 = 0b41d85f92844b820c1ed375d88dc214.
   PubMedGoogle Scholar
• Douglas NM, Anstey NM, Buffet PA, Poespoprodjo JR, Yeo TW, White NJ, et al. The anaemia of Plasmodium vivax malaria. Malar J [Internet]. 2012;11(1):135. [cited 2012 May 8]. Available from: http://www.malariajournal.com/content/11/1/135.
   PubMedGoogle Scholar
• Anstey NM, Douglas NM, Poespoprodjo JR, Price RN. Plasmodium vivax: clinical spectrum, risk factors and pathogenesis [Internet]. Adv Parasitol. Elsevier; 2012. Available from: http://dx.doi.org/10.1016/B978-0-12-397900-1.00003-7.
   Web of Science ®Google Scholar
• Price RN, Tjitra E, Guerra CA, Yeung S, White NJ, Anstey NM. Vivax malaria: neglected and not benign. Am J Trop Med Hyg [Internet]. 2007;77(6 Suppl):79–87.
   PubMed Web of Science ®Google Scholar
• Battle KE, Gething PW, Elyazar IRF, Moyes CL, Sinka ME, Howes RE, et al. The global public health significance of Plasmodium vivax [Internet]. Adv Parasitol. Elsevier; 2012. [cited 2013 Feb 22]. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid = 3548406&tool = pmcentrez&rendertype = abstract.
   Web of Science ®Google Scholar
• Baird JK. Evidence and implications of mortality associated with acute Plasmodium vivax malaria. Clin Microbiol Rev [Internet]. 2013;26(1):36–57, [cited 2013 May 22]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/23297258.
   PubMed Web of Science ®Google Scholar
• Mendis K, Sina BJ, Marchesini P, Carter R. The neglected burden of Plasmodium vivax malaria. Am J Trop Med Hyg. 2001;64(1–2 Suppl):97–106.
   PubMed Web of Science ®Google Scholar
• Ménard D, Barnadas C, Bouchier C, Henry-Halldin C, Gray LR, Ratsimbasoa A, et al. Plasmodium vivax clinical malaria is commonly observed in Duffy-negative Malagasy people. Proc Natl Acad Sci U S A. 2010;107(13):5967–71.
   PubMed Web of Science ®Google Scholar
• Price RN, von Seidlein L, Valecha N, Nosten F, Baird JK, White NJ. Global extent of chloroquine-resistant Plasmodium vivax: a systematic review and meta-analysis. Lancet Infect Dis [Internet]. 2014;3099(14):1–10, Price et al. Open Access article distributed under the terms of CC-BY; [cited 2014 Sep 9]. Available from: http://linkinghub.elsevier.com/retrieve/pii/S1473309914708552.
   Google Scholar
• Ebringer A, Heathcote G, Baker J, Waller M, Shanks GD, Edstein MD. Evaluation of the safety and tolerability of a short higher-dose primaquine regimen for presumptive anti-relapse therapy in healthy subjects. Trans R Soc Trop Med Hyg. 2011;105:568–73.
   PubMed Web of Science ®Google Scholar
• World Health Organization. Guidelines for the treatment of malaria [Internet]. 2nd edn: WHO; 2010; p. 197. Available from: http://whqlibdoc.who.int/publications/2010/9789241547925_eng.pdf?ua = 1.
   Google Scholar
• John GK, Douglas NM, von Seidlein L, Nosten F, Baird KJ, White NJ, et al. Primaquine radical cure of Plasmodium vivax: a critical review of the literature. Malar J [Internet]. 2012;11(1):280. [cited 2012 Aug 20]. Available from: http://www.malariajournal.com/content/11/1/280.
   PubMedGoogle Scholar
• Brueckner RP, Lasseter KC, Lin ET, Schuster BG. First-time-in-humans safety and pharmacokinetics of WR 238605, a new antimalarial. Am J Trop Med Hyg [Internet]. 1998;58(5):645–9.
   PubMed Web of Science ®Google Scholar
• Fryauff DJ, Baird JK, Basri H, Sumawinata I, Purnomo, Richie TL, et al. Randomised placebo-controlled trial of primaquine for prophylaxis of falciparum and vivax malaria. Lancet. 1995;346:1190–3.
   PubMed Web of Science ®Google Scholar
• Baird JK, Fryauff DJ, Basri H, Bangs MJ, Subianto B, Wiady I, et al. Primaquine for prophylaxis against malaria among nonimmune transmigrants in Irian Jaya, Indonesia. Am J Trop Med Hyg. 1995;52:479–84.
   PubMed Web of Science ®Google Scholar
• Weiss WR, Oloo AJ, Johnson A, Koech D, Hoffman SL. Daily primaquine is effective for prophylaxis against falciparum malaria in Kenya: comparison with mefloquine, doxycycline, and chloroquine plus proguanil. J Infect Dis. 1995;171(6):1569–75.
   PubMed Web of Science ®Google Scholar
• Clayman CB, Arnold J, Hockwald RS, Yount EH, Edgecomb JH, Alving AS. Toxicity of primaquine in caucasians. J Am Med Assoc. 1952;149(17):1563–8.
   PubMed Web of Science ®Google Scholar
• Shanks GD, Kain KC, Keystone JS. Malaria chemoprophylaxis in the age of drug resistance. II. Drugs that may be available in the future. Clin Infect Dis. 2001;33:381–5.
   PubMed Web of Science ®Google Scholar
• Ganesan S, Tekwani BL, Sahu R, Tripathi LM, Walker LA. Cytochrome P(450)-dependent toxic effects of primaquine on human erythrocytes. Toxicol Appl Pharmacol [Internet]. Elsevier B.V.; 2009 [cited 2011 Jun 21];241(1):14–22. Available from: http://www.ncbi.nlm.nih.gov/pubmed/19616568.
   Google Scholar
• Salvidio E, Pannacciulli I, Tizianello A, Ajmar F. Nature of hemolytic crises and the fate of G6PD deficient, drug-damaged erythrocytes in Sardinians. N Engl J Med. 1967;276:1339–44.
   PubMed Web of Science ®Google Scholar
• Fletcher KA, Barton PF, Kelly JA. Studies on the mechanisms of oxidation in the erythrocyte by metabolites of primaquine. Biochem Pharmacol. 1988;37:2683–90.
   PubMed Web of Science ®Google Scholar
• Ashley EA, Recht J, White NJ. Primaquine: the risks and the benefits. Malar J. 2014;13:418–24.
   PubMed Web of Science ®Google Scholar
• Recht J, Ashley E, White N. Safety of 8-aminoquinoline antimalarial medicines. 2014.
   Google Scholar
• Bennett JW, Pybus BS, Yadava A, Tosh D, Sousa JC, McCarthy WF, et al. Primaquine failure and cytochrome P-450 2D6 in Plasmodium vivax malaria. N Engl J Med [Internet]. 2013;369:1381–2.
   PubMed Web of Science ®Google Scholar
• Pybus BS, Marcsisin SR, Jin X, Deye G, Sousa JC, Li Q, et al. The metabolism of primaquine to its active metabolite is dependent on CYP 2D6. Malar J [Internet]. 2013;12(1):212. [cited 2013 Aug 31]. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid = 3689079&tool = pmcentrez&rendertype = abstract.
   PubMedGoogle Scholar
• Fasinu PS, Tekwani BL, Nanayakkara ND, Avula B, Herath HB, Wang Y-H, et al. Enantioselective metabolism of primaquine by human CYP2D6. Malar J [Internet]. 2014;13(1):507. [cited 2015 Jan 5]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/25518709.
   PubMedGoogle Scholar
• Vale N, Moreira R, Gomes P. Primaquine revisited six decades after its discovery. Eur J Med Chem [Internet]. 2009;44(3):937–953, Elsevier Masson SAS; [cited 2011 Jul 28]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/18930565.
   Web of Science ®Google Scholar
• Saunders D, Vanachayangkul P, Imerbsin R, Khemawoot P, Siripokasupkul R, Tekwani BL, et al. Pharmacokinetics and pharmacodynamics of (+)-primaquine and ( − )-primaquine enantiomers in rhesus macaques (Macaca mulatta). Antimicrob Agents Chemother. 2014;58(12):7283–91.
   PubMed Web of Science ®Google Scholar
• Crockett M, Kain KC. Tafenoquine: a promising new antimalarial agent. Expert Opin Investig Drugs. 2007;16:705–15.
   PubMed Web of Science ®Google Scholar
• Llanos-Cuentas A, Lacerda MV, Rueangweerayut R, Krudsood S, Gupta SK, Kochar SK, et al. Tafenoquine plus chloroquine for the treatment and relapse prevention of Plasmodium vivax malaria (DETECTIVE): a multicentre, double-blind, randomised, phase 2b dose-selection study. Lancet [Internet]. Elsevier Ltd; 2013 [cited 2013 Dec 19]; 6736(9922):1049–1058, Available from: http://www.ncbi.nlm.nih.gov/pubmed/24360369.
   Google Scholar
• Burrows JN, van Huijsduijnen RH, Möhrle JJ, Oeuvray C, Wells TNC, Hooft van Huijsduijnen R, et al. Designing the next generation of medicines for malaria control and eradication. Malar J [Internet]. 2013;12(187):187. [cited 2013 Jun 10]. Available from: http://www.malariajournal.com/content/12/1/187.
   PubMedGoogle Scholar
• Clyde DF. Clinical problems associated with the use of primaquine as a tissue schizontocidal and gametocytocidal drug. Bull World Health Organ. 1981;59:391–5.
   PubMed Web of Science ®Google Scholar
• Delves M, Plouffe D, Scheurer C, Meister S, Wittlin S, Winzeler EA, et al. The activities of current antimalarial drugs on the life cycle stages of Plasmodium: a comparative study with human and rodent parasites. PLoS Med [Internet]. 2012;9(2), [cited 2012 Mar 16]. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid = 3283556&tool = pmcentrez&rendertype = abstract.
   PubMed Web of Science ®Google Scholar
• Zeeman A-M, van Amsterdam SM, McNamara CW, Voorberg-van der Wel A, Klooster EJ, van den Berg A, et al. KAI407, a potent non-8-aminoquinoline compound that kills Plasmodium cynomolgi early dormant liver stage parasites in vitro. Antimicrob Agents Chemother [Internet]. 2014;58(3):1586–1595, [cited 2014 Jul 14]. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid = 3957848&tool = pmcentrez&rendertype = abstract.
   PubMed Web of Science ®Google Scholar
• Pybus BS, Marcsisin SR, Jin X, Deye G, Sousa JC, Li Q, et al. The metabolism of primaquine to its active metabolite is dependent on CYP 2D6. Malar J [Internet]. 2013;12(1):212.
   PubMedGoogle Scholar
• 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 [Internet]. 2014;13(1):2. [cited 2014 Jan 6]. Available from: http://www.malariajournal.com/content/13/1/2.
   PubMedGoogle Scholar
• Li Q, O'Neil M, Xie L, Caridha D, Zeng Q, Zhang J, et al. Assessment of the prophylactic activity and pharmacokinetic profile of oral tafenoquine compared to primaquine for inhibition of liver stage malaria infections. Malar J [Internet]. 2014;13(1):141. [cited 2014 May 16]. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid = 3989846&tool = pmcentrez&rendertype = abstract.
   PubMedGoogle Scholar
• Wells TNC, Burrows JN, Baird JK. Targeting the hypnozoite reservoir of Plasmodium vivax: the hidden obstacle to malaria elimination. Trends Parasitol [Internet]. 2010;26(3):145–151, Elsevier Ltd; [cited 2012 Apr 22]. Available from: http://dx.doi.org/10.1016/j.pt.2009.12.005.
   PubMed Web of Science ®Google Scholar
• Puri SK, Dutta GP. Plasmodium cynomolgi: gametocytocidal activity of the anti-malarial compound CDRI 80/53 (elubaquine) in rhesus monkeys. Exp Parasitol [Internet]. 2005;111(1):8–13, [cited 2011 Dec 22]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/16005457.
   PubMed Web of Science ®Google Scholar
• Gogtay NJ, Kamtekar KD, Dalvi SS, Mehta SS, Chogle AR, Aigal U, et al. A randomized, parallel study of the safety and efficacy of 45 mg primaquine versus 75 mg bulaquine as gametocytocidal agents in adults with blood schizonticide-responsive uncomplicated falciparum malaria [ISCRTN50134587]. BMC Infect Dis [Internet]. 2006;6:16. [cited 2011 Oct 19]. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid = 1389708&tool = pmcentrez&rendertype = abstract.
   PubMed Web of Science ®Google Scholar
• Tekwani BL, Walker LA. 8-Aminoquinolines: future role as antiprotozoal drugs. Curr Opin Infect Dis [Internet]. 2006;19(6):623–31.
   PubMed Web of Science ®Google Scholar
• Succinate Q, Nanayakkara NPD, Ager AL, Bartlett MS, Yardley V, Croft SL, et al. Antiparasitic activities and toxicities of individual enantiomers of the 8-aminoquinoline 8-[(4-amino-1-methylbutyl)amino]-6-methoxy-4-methyl-5-[3,4-dichlorophenoxy]quinoline succinate. Antimicrob Agents Chemother [Internet]. 2008;52(6):2130–2137, [cited 2011 Aug 4]. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid = 2415774&tool = pmcentrez&rendertype = abstract.
   PubMed Web of Science ®Google Scholar
• Meister S, Plouffe DM, Kuhen KL, Bonamy GMC, Wu T, Barnes SW, et al. Imaging of Plasmodium liver stages to drive next-generation antimalarial drug discovery. Science. 2011;334:1372–7.
   PubMed Web of Science ®Google Scholar
• Ploemen IHJ, Prudêncio M, Douradinha BG, Ramesar J, Fonager J, van Gemert G-J, et al. Visualisation and quantitative analysis of the rodent malaria liver stage by real time imaging. PLoS One [Internet]. 2009;4(11):e7881. [cited 2011 Aug 2]. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid = 2775639&tool = pmcentrez&rendertype = abstract.
   Google Scholar
• Dow GS, Gettayacamin M, Hansukjariya P, Imerbsin R, Komcharoen S, Sattabongkot J, et al. Radical curative efficacy of tafenoquine combination regimens in Plasmodium cynomolgi-infected Rhesus monkeys (Macaca mulatta). Malar J. 2011;10(1):212.
   PubMedGoogle Scholar
• Schmidt LH. Relationships between chemical structures of 8-aminoquinolines and their capacities for radical cure of infections with Plasmodium cynomolgi in rhesus monkeys. Antimicrob Agents Chemother [Internet]. 1983;24(5):615–52.
   PubMed Web of Science ®Google Scholar
• Puri SK, Dutta GP. Quinoline esters as potential antimalarial drugs: Plasmodium cynomolgi infections in monkeys. Trans R Soc Trop Med Hyg. 1990;84(6):759–60.
   PubMed Web of Science ®Google Scholar
• Schmidt LH, Rossan RN, Fradkin R, Sullivan R, Schulemann W, Kratz L. Antimalarial activities and subacute toxicity of RC-12, a 4-amino-substituted pyrocatechol. Antimicrob Agents Chemother. 1985;28(5):612–25.
   PubMed Web of Science ®Google Scholar
• Clyde DF, McCarthy VC, Miller RM. Inactivity of rc-12 as a causal prophylactic and relapse inhibitor of Plasmodium vivax in man. Trans R Soc Trop Med Hyg. 1974;68(2):167–8.
   Web of Science ®Google Scholar
• Liu X, Wang X, Li Q, Kozar MP, Melendez V, O'Neil MT, et al. Synthesis and antimalarial activity of 2-guanidino-4-oxoimidazoline derivatives. J Med Chem [Internet]. 2011;54(13):4523–35.
   PubMed Web of Science ®Google Scholar
• Voorberg-van der Wel A, Zeeman AM, van Amsterdam SM, van den Berg A, Klooster EJ, Iwanaga S, et al. Transgenic fluorescent Plasmodium cynomolgi liver stages enable live imaging and purification of Malaria hypnozoite-forms. PLoS One [Internet]. 2013;8(1):e54888. [cited 2013 May 22]. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid = 3554669&tool = pmcentrez&rendertype = abstract.
   Google Scholar
• McNamara CW, Lee MCS, Lim CS, Lim SH, Roland J, Nagle A, et al. Targeting Plasmodium PI(4)K to eliminate malaria. Nature [Internet]. 2013;:4. Nature Publishing Group; [cited 2013 Nov 28]. Available from: http://www.nature.com/doifinder/10.1038/nature12782.
   Google Scholar
• Myint HY, Berman J, Walker L, Pybus B, Melendez V, Baird JK, et al. Review: improving the therapeutic index of 8-aminoquinolines by the use of drug combinations: review of the literature and proposal for future investigations. Am J Trop Med Hyg. 2011;85(6):1010–4.
   PubMed Web of Science ®Google Scholar
• Hill DR, Baird JK, Parise ME, Lewis LS, Ryan ET, Magill AJ. Primaquine: report from CDC expert meeting on malaria chemoprophylaxis I. Am J Trop Med Hyg [Internet]. 2006;75(3):402–15.
   PubMed Web of Science ®Google Scholar
• Leroy D, Campo B, Ding X, Jeremy BN, Cherbuin S. Defining the biology component of the drug discovery strategy for malaria eradication. Trends Parasitol [Internet]. 2014 [cited 2014 Aug 19]; 2014;1–13, Available from: http://www.ncbi.nlm.nih.gov/pubmed/25131411.
   Google Scholar
• Dembele L, Gego A, Zeeman A-M, Franetich J-F, Silvie O, Rametti A, et al. Towards an in vitro model of Plasmodium hypnozoites suitable for drug discovery. PLoS One [Internet]. 2011;6(3):e18162. [cited 2011 Jun 21]. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid = 3069045&tool = pmcentrez&rendertype = abstract.
   Google Scholar
• Dembélé L, Franetich J-F, Lorthiois A, Gego A, Zeeman A-M, Kocken CHM, et al. Persistence and activation of malaria hypnozoites in long-term primary hepatocyte cultures. Nat Med [Internet]. 2014;20(3):307–312, [cited 2014 Feb 12]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/24509527.
   PubMed Web of Science ®Google Scholar
• Deye GA, Gettayacamin M, Hansukjariya P, Im-Erbsin R, Sattabongkot J, Rothstein Y, et al. Use of a Rhesus Plasmodium cynomolgi Model to Screen for Anti-Hypnozoite Activity of Pharmaceutical Substances. Am J Trop Med Hyg [Internet]. 2012;86(6):931–935, [cited 2012 Jun 12]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22665596.
   PubMed Web of Science ®Google Scholar
• Sutanto I, Tjahjono B, Basri H, Taylor WR, Putri FA, Meilia RA, et al. Randomized, open-label trial of primaquine against vivax malaria relapse in Indonesia. Antimicrob Agents Chemother [Internet]. 2013;57(3):1128–1135, [cited 2013 Jun 3]. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid = 3591862&tool = pmcentrez&rendertype = abstract.
   PubMed Web of Science ®Google Scholar
• Rochford R, Ohrt C, Baresel PC, Campo B, Sampath A, Magill AJ, et al. Humanized mouse model of glucose 6-phosphate dehydrogenase deficiency for in vivo assessment of hemolytic toxicity. Proc Natl Acad Sci U S A [Internet]. 2013;110(43):17486–91.
   PubMed Web of Science ®Google Scholar
• Burrows JN, Chibale K, Wells TNC. The state of the art in anti-malarial drug discovery and development. Curr Top Med Chem [Internet]. 2011;11(10):1226–54.
   PubMed Web of Science ®Google Scholar
• Wells TNC, Alonso PL, Gutteridge WE. New medicines to improve control and contribute to the eradication of malaria. Nat Rev Drug Discov [Internet]. 2009;8(11):879–891, Nature Publishing Group; [cited 2011 Jun 21]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/19834482.
   PubMed Web of Science ®Google Scholar
• Hulden L, Hulden L. Activation of the hypnozoite: a part of Plasmodium vivax life cycle and survival. Malar J [Internet]. 2011;10(1):90. BioMed Central Ltd; [cited 2011 Sep 10]. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid = 3086824&tool = pmcentrez&rendertype = abstract.
   PubMedGoogle Scholar
• Hall N. Genomic insights into the other malaria. Nat Genet [Internet]. 2012;44(9):962–963, Nature Publishing Group; [cited 2013 Aug 8]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22932497.
   PubMed Web of Science ®Google Scholar
• Mazier D, Landau I, Druilhe P, Miltgen F, Guguen-Guillouzo C, Baccam D, et al. Cultivation of the liver forms of Plasmodium vivax in human hepatocytes. Nature [Internet]. 1984;307(5949):367–9.
   Google Scholar
• Hollingdale MR, Collins WE, Campbell CC. In vitro culture of exoerythrocytic parasites of the North Korean strain of Plasmodium vivax in hepatoma cells. Am J Trop Med Hyg [Internet]. 1986;35(2):275–6.
   PubMed Web of Science ®Google Scholar
• Sattabongkot J, Yimamnuaychoke N, Leelaudomlipi S, Rasameesoraj M, Jenwithisuk R, Coleman RE, et al. Establishment of a human hepatocyte line that supports in vitro development of the exo-erythrocytic stages of the malaria parasites Plasmodium falciparum and P. vivax. Am J Trop Med Hyg [Internet]. 2006;74(5):708–15.
   PubMed Web of Science ®Google Scholar
• March S, Ng S, Velmurugan S, Galstian A, Shan J, Logan DJ, et al. A microscale human liver platform that supports the hepatic stages of Plasmodium falciparum and vivax. Cell Host Microbe [Internet]. 2013;14(1):104–115, Elsevier Inc.; [cited 2013 Jul 30]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/23870318.
   PubMed Web of Science ®Google Scholar
• Maher SP, Crouse RB, Conway AJ, Bannister EC, Adams JH, Kyle DE, et al. Microphysical space of a liver sinusoid device enables simplified long-term maintenance of chimeric mouse-expanded human hepatocytes. Biomed Microdevices. 2014;16(5):727–36.
   PubMed Web of Science ®Google Scholar
• Trager W, Jensen JB. Human malaria parasites in continuous culture. Science [Internet]. 1976;193(4254):673–5.
   Google Scholar
• Noulin F, Borlon C, Van Den Abbeele J, D'Alessandro U, Erhart A. 1912–2012: a century of research on Plasmodium vivax in vitro culture. Trends Parasitol [Internet]. 2013;:1–9, [cited 2013 May 22]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/23623759.
   Google Scholar
• Larrouy G, Magnaval JF, Moro F. Obtaining intraerythrocytic forms of Plasmodium vivax by in vitro culture. C R Seances Acad Sci III. 1981;292(16):929–30.
   PubMedGoogle Scholar
• Banerjee T, Sharma SK, Kapoor N, Dwivedi V, Surolia N, Surolia A. Benzothiophene carboxamide derivatives as inhibitors of Plasmodium falciparum enoyl-ACP reductase. IUBMB Life [Internet]. 2011;63(12):1101–1110, [cited 2014 May 21]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22006792.
   PubMed Web of Science ®Google Scholar
• Kumar AA, Lim C, Moreno Y, Mace CR, Syed A, Tyne D, et al. Enrichment of reticulocytes from whole blood using aqueous multiphase systems of polymers. Am J Hematol. 2015;90(1):31–6.
   PubMed Web of Science ®Google Scholar
• Udomsangpetch R, Kaneko O, Chotivanich K, Sattabongkot J. Cultivation of Plasmodium vivax. Trends Parasitol [Internet]. 2008;24(2):85–88, [cited 2011 Jun 27]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/18180202.
   PubMed Web of Science ®Google Scholar
• Golenda CF, Li J, Rosenberg R. Continuous in vitro propagation of the malaria parasite Plasmodium vivax. Proc Natl Acad Sci U S A. 1997;94(June):6786–91.
   PubMedGoogle Scholar
• Udomsangpetch R, Somsri S, Panichakul T, Chotivanich K, Sirichaisinthop J, Yang Z, et al. Short-term in vitro culture of field isolates of Plasmodium vivax using umbilical cord blood. Parasitol Int. 2007;56(1):65–9.
   PubMed Web of Science ®Google Scholar
• Panichakul T, Sattabongkot J, Chotivanich K, Sirichaisinthop J, Cui L, Udomsangpetch R. Production of erythropoietic cells in vitro for continuous culture of Plasmodium vivax. Int J Parasitol. 2007;37(14):1551–7.
   PubMed Web of Science ®Google Scholar
• Noulin F, Borlon C, van den Eede P, Boel L, Verfaillie CM, D'Alessandro U, et al. Cryopreserved reticulocytes derived from hematopoietic stem cells can be invaded by cryopreserved Plasmodium vivax isolates. PLoS One. 2012;7(7):1–8.
   Google Scholar
• Van J, Noulin F, Manesia JK, Rosanas-Urgell A, Erhart A, Abbeele D, et al. Hematopoietic stem/progenitor cell sources to generate reticulocytes for Plasmodium vivax culture. PLoS One. 2014;9(11):e112496.
   Google Scholar
• Furuya T, Sá JM, Chitnis CE, Wellems TE, Stedman TT. Reticulocytes from cryopreserved erythroblasts support Plasmodium vivax infection in vitro. Parasitol Int. 2014;63(2):278–84.
   PubMed Web of Science ®Google Scholar
• Zuo Z, Polski J, Kasyan A, Medeiros J. Acute erythroid leukemia. Arch Pathol Lab Med. 2010;139(9):1261–70.
   Google Scholar
• Shah S, Huang X, Cheng L. Concise review: stem cell-based approaches to red blood cell production for transfusion. Stem Cells Transl Med [Internet]. 2014;3:346–55.
   PubMed Web of Science ®Google Scholar
• Ploss A. Mouse models for human infectious diseases. J Immunol Methods. 2014;410:1–2.
   PubMed Web of Science ®Google Scholar
• Kaushansky A, Mikolajczak SA, Vignali M, Kappe SHI. Of men in mice: the success and promise of humanized mouse models for human malaria parasite infections. Cell Microbiol. 2014;16(March):602–11.
   PubMedGoogle Scholar
• Rongvaux A, Takizawa H, Strowig T, Willinger T, Eynon EE, Flavell RA, et al. Human hemato-lymphoid system mice: current use and future potential for medicine. Annu Rev Immunol [Internet]. 2013;31:635–74.
   PubMed Web of Science ®Google Scholar
• Rongvaux A, Willinger T, Martinek J, Strowig T, Gearty SV, Teichmann LL, et al. Development and function of human innate immune cells in a humanized mouse model. Nat Biotechnol [Internet]. 2014;32:364–72.
   PubMed Web of Science ®Google Scholar
• Vaughan AM, Mikolajczak SA, Wilson EM, Grompe M, Kaushansky A, Camargo N, et al. Complete Plasmodium falciparum liver stage development in liver-chimeric mice. J Clin Invest. 2012;122(10):1–11.
   Google Scholar
• Azuma H, Paulk N, Ranade A, Dorrell C, Al-Dhalimy M, Ellis E, et al. Robust expansion of human hepatocytes in Fah-/-/Rag2-/-/Il2rg-/- mice. Nat Biotechnol. 2007;25(8):903–10.
   PubMed Web of Science ®Google Scholar
• Bissig K-D, Le TT, Woods N-B, Verma IM. Repopulation of adult and neonatal mice with human hepatocytes: a chimeric animal model. Proc Natl Acad Sci U S A. 2007;104(51):20507–11.
   PubMed Web of Science ®Google Scholar
• Galinski MR, Meyer EVS, Barnwell JW. Plasmodium vivax: modern strategies to study a persistent parasite's life cycle [Internet]. Adv Parasitol. 2013;., Elsevier; [cited 2013 Feb 25]. Available from: http://www.ncbi.nlm.nih.gov/pubmed/23384620.
   Web of Science ®Google Scholar
• Moreno M, Tong C, Guzmán M, Chuquiyauri R, Llanos-Cuentas A, Rodriguez H, et al. Infection of laboratory-colonized Anopheles darlingi mosquitoes by Plasmodium vivax. Am J Trop Med Hyg. 2014;90(4):612–6.
   PubMed Web of Science ®Google Scholar
• Ghosh SK, Tiwari S, Raghavendra K, Sathyanarayan TS, Dash AP. Observations on sporozoite detection in naturally infected sibling species of the Anopheles culicifacies complex and variant of Anopheles stephensi in India. J Biosci. 2008;33(3):333–6.
   PubMed Web of Science ®Google Scholar
• Goo Y-K, Seo E-J, Choi Y-K, Shin H-I, Sattabongkot J, Ji S-Y, et al. First characterization of Plasmodium vivax liver stage antigen (PvLSA) using synthetic peptides. Parasit Vectors [Internet]. 2014;7(1):64. Parasites & Vectors; [cited 2014 Nov 27]. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid = 3925417&tool = pmcentrez&rendertype = abstract.
   PubMedGoogle Scholar
• Mathias DK, Jardim JG, Parish LA, Armistead JS, Trinh HV, Kumpitak C, et al. Differential roles of an Anopheline midgut GPI-anchored protein in mediating Plasmodium falciparum and Plasmodium vivax ookinete invasion. InfectGenet Evol. 2014;28:635–47.
   PubMed Web of Science ®Google Scholar
• Zhu G, Xia H, Zhou H, Li J, Lu F, Liu Y, et al. Susceptibility of Anopheles sinensis to Plasmodium vivax in malarial outbreak areas of central China. Parasit Vectors [Internet]. 2013;6(1):1. Parasites & Vectors. Available from: Parasites & Vectors.
   PubMedGoogle Scholar
• Kennedy M, Fishbaugher ME, Vaughan AM, Patrapuvich R, Boonhok R, Yimamnuaychok N, et al. A rapid and scalable density gradient purification method for Plasmodium sporozoites. Malar J [Internet]. 2012;11(1):421. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid = 3543293&tool = pmcentrez&rendertype = abstract.
   PubMedGoogle Scholar
• Epstein JE, Tewari K, Lyke KE, Sim BKL, Billingsley PF, Laurens MB, et al. Live attenuated malaria vaccine designed to protect through hepatic CD8+T cell immunity. Science. 2011;334(6055):475–80.
   PubMed Web of Science ®Google Scholar
• Hoffman SL, Billingsley PF, James E, Richman A, Loyevsky M, Li T, et al. Development of a metabolically active, non-replicating sporozoite vaccine to prevent Plasmodium falciparum malaria. Hum Vaccin. 2010;6:97–106.
   PubMed Web of Science ®Google Scholar
• Gosden RG. Memoir of fertility preservation. Adv Exp Med Biol. 2013;761:85–94.
   PubMed Web of Science ®Google Scholar
• Gosden R. Cryopreservation: a cold look at technology for fertility preservation. Fertil Steril. 2011;96(2):264–8.
   PubMed Web of Science ®Google Scholar
• Holoch P, Wald M. Current options for preservation of fertility in the male. Fertil Steril. 2011;96(2):286–90.
   PubMed Web of Science ®Google Scholar
• Clark NA, Swain JE. Oocyte cryopreservation: searching for novel improvement strategies. J Assist Reprod Genet. 2013;30:865–75.
   PubMed Web of Science ®Google Scholar
• Hollingdale MR, Collins WE, Campbell CC, Schwartz AL. In vitro culture of two populations (dividing and nondividing) of exoerythrocytic parasites of Plasmodium vivax. Am J Trop Med Hyg. 1985;34(2):216–22.
   PubMed Web of Science ®Google Scholar
• Chattopadhyay R, Velmurugan S, Chakiath C, Donkor LA, Milhous W, Barnwell JW, et al. Establishment of an in vitro assay for assessing the effects of drugs on the liver stages of Plasmodium vivax malaria. PLoS One. 2010;5(12):1–8.
   Google Scholar
• Kafsack BFC, Llinás M. Eating at the table of another: metabolomics of host/parasite interactions. Cell Host Microbe. 2010;7(2):90–9.
   PubMed Web of Science ®Google Scholar
• Lakshmanan V, Rhee K, Daily J. Metabolomics and malaria biology. Mol Biochem Parasitol. 2011;175(2):104–11.
   PubMed Web of Science ®Google Scholar
• Fraunholz MJ. Systems biology in malaria research. Trends Parasitol. 2005;21(9):393–5.
   PubMed Web of Science ®Google Scholar