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Plasmodium knowlesi: a relevant, versatile experimental malaria model

Published online by Cambridge University Press:  12 December 2016

ERICA M. PASINI
Affiliation:
Department of Parasitology, Biomedical Primate Research Centre, PO Box 3306, 2280 GH Rijswijk, The Netherlands
ANNE-MARIE ZEEMAN
Affiliation:
Department of Parasitology, Biomedical Primate Research Centre, PO Box 3306, 2280 GH Rijswijk, The Netherlands
ANNEMARIE VOORBERG-VAN DER WEL
Affiliation:
Department of Parasitology, Biomedical Primate Research Centre, PO Box 3306, 2280 GH Rijswijk, The Netherlands
CLEMENS H. M. KOCKEN*
Affiliation:
Department of Parasitology, Biomedical Primate Research Centre, PO Box 3306, 2280 GH Rijswijk, The Netherlands
*
*Corresponding author: Department of Parasitology, Biomedical Primate Research Centre, PO Box 3306, 2280 GH Rijswijk, The Netherlands. E-mail: [email protected]

Summary

The primate malaria Plasmodium knowlesi has a long-standing history as an experimental malaria model. Studies using this model parasite in combination with its various natural and experimental non-human primate hosts have led to important advances in vaccine development and in our understanding of malaria invasion, immunology and parasite–host interactions. The adaptation to long-term in vitro continuous blood stage culture in rhesus monkey, Macaca fascicularis and human red blood cells, as well as the development of various transfection methodologies has resulted in a highly versatile experimental malaria model, further increasing the potential of what was already a very powerful model. The growing evidence that P. knowlesi is an important human zoonosis in South-East Asia has added relevance to former and future studies of this parasite species.

Type
Special Issue Review
Copyright
Copyright © Cambridge University Press 2016 

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References

REFERENCES

Aikawa, M., Miller, L. H., Johnson, J. and Rabbege, J. (1978). Erythrocyte entry by malarial parasites. A moving junction between erythrocyte and parasite. Journal of Cell Biology 77, 7282.Google Scholar
al-Khedery, B., Barnwell, J. W. and Galinski, M. R. (1999). Antigenic variation in malaria: a 3′ genomic alteration associated with the expression of a P. knowlesi variant antigen. Molecular Cell 3, 131141.Google Scholar
Amir, A., Russell, B., Liew, J. W., Moon, R. W., Fong, M. Y., Vythilingam, I., Subramaniam, V., Snounou, G. and Lau, Y. L. (2016). Invasion characteristics of a Plasmodium knowlesi line newly isolated from a human. Scientific Reports 6, 24623.Google Scholar
Andrade, B. B. and Barral-Netto, M. (2011). Biomarkers for susceptibility to infection and disease severity in human malaria. Memorias do Instituto Oswaldo Cruz 106 (Suppl. 1), 7078.Google Scholar
Ball, E. G., Anfinsen, C. B., Geiman, Q. M., McKee, R. W. and Ormsbee, R. A. (1945). In vitro growth and multiplication of the Malaria parasite, Plasmodium Knowlesi . Science 101, 542544.Google Scholar
Bannister, L. H., Butcher, G. A. and Mitchell, G. H. (1977). Recent advances in understanding the invasion of erythrocytes by merozoites of Plasmodium knowlesi . Bulletin of the World Health Organization 55, 163169.Google Scholar
Barasa, M., Ng'ang'a, Z. W., Sowayi, G. A., Okoth, J. M., Barasa, M. B., Namulanda, F. B., Kagasi, E. A., Gicheru, M. M. and Ozwara, S. H. (2012). Cytokine expression in malaria-infected non-human primate placentas. Open Veterinary Journal 2, 5864.Google Scholar
Barnwell, J. W. (1999). Malaria. A new escape and evasion tactic. Nature 398, 562563.Google Scholar
Barnwell, J. W., Howard, R. J. and Miller, L. H. (1982). Altered expression of Plasmodium knowlesi variant antigen on the erythrocyte membrane in splenectomized rhesus monkeys. Journal of Immunology 128, 224226.CrossRefGoogle ScholarPubMed
Barnwell, J. W., Howard, R. J., Coon, H. G. and Miller, L. H. (1983). Splenic requirement for antigenic variation and expression of the variant antigen on the erythrocyte membrane in cloned Plasmodium knowlesi malaria. Infection and Immunity 40, 985994.CrossRefGoogle ScholarPubMed
Beignon, A. S., Le Grand, R. and Chapon, C. (2014). In vivo imaging in NHP models of malaria: challenges, progress and outlooks. Parasitology International 63, 206215.Google Scholar
Brown, K. N. and Brown, I. N. (1965). Immunity to malaria: antigenic variation in chronic infections of Plasmodium knowlesi . Nature 208, 12861288.CrossRefGoogle ScholarPubMed
Butcher, G. A. (1996). Models for malaria: Nature knows best. Parasitol Today 12, 378382.Google Scholar
Butcher, G. A., Mitchell, G. H. and Cohen, S. (1978). Antibody mediated mechanisms of immunity to malaria induced by vaccination with Plasmodium knowlesi merozoites. Immunology 34, 7786.Google ScholarPubMed
Butcher, G. A., Mitchell, G. H. and Cohen, S. (2010). Plasmodium knowlesi infections in a small number of non-immune natural hosts (Macaca fascicularis) and in rhesus monkeys (M. mulatta). Transactions of the Royal Society of Tropical Medicine and Hygiene 104, 7577.Google Scholar
Chen, L., Li, G., Lu, Y. and Luo, Z. (2001). Histopathological changes of Macaca mulatta infected with Plasmodium knowlesi . Chinese Medical Journal (English) 114, 10731077.Google Scholar
Chin, W., Contacos, P. G., Coatney, G. R. and Kimball, H. R. (1965). A naturally acquitted quotidian-type malaria in man transferable to monkeys. Science 149, 865.Google Scholar
Clark, I. A. and Alleva, L. M. (2009). Is human malarial coma caused, or merely deepened, by sequestration? Trends in Parasitology 25, 314318.Google Scholar
Coatney, G. R., Collins, W. E., Warren, M. and Contacos, P. G. (1971). The Primate Malarias. U.S. Government printing office, Washington, DC.Google Scholar
Coggeshall, L. T. and Kumm, H. W. (1937). Demonstration of passive immunity in experimental monkey malaria. Journal of Experimental Medicine 66, 177190.Google Scholar
Cohen, S., Mc, G. I. and Carrington, S. (1961). Gamma-globulin and acquired immunity to human malaria. Nature 192, 733737.Google Scholar
Collins, W. E. (2012). Plasmodium knowlesi: a malaria parasite of monkeys and humans. Annual Review of Entomology 57, 107121.Google Scholar
Collins, W. E., Contacos, P. G. and Chin, W. (1978). Infection of the squirrel monkey Saimiri sciureus, with Plasmodium knowlesi . Transactions of the Royal Society of Tropical Medicine and Hygiene 72, 662663.Google Scholar
Collins, W. E., Contacos, P. G. and Guinn, E. G. (1967). Studies on the transmission of simian malarias. II. Transmission of the H strain of Plasmodium knowlesi by Anopheles balabacensis balabacensis. J Parasitol 53, 841844.CrossRefGoogle Scholar
Collins, W. E., Contacos, P. G., Skinner, J. C., Stanfill, P. S. and Richardson, B. B. (1981). Susceptibility of Peruvian Aotus monkeys to infection with different species of Plasmodium. American Journal of Tropical Medicine and Hygiene 30, 2630.Google Scholar
Collins, W. E., Skinner, J. C., Broderson, J. R., Filipski, V. K., Morris, C. M., Stanfill, P. S. and Warren, M. (1992). Susceptibility of Macaca fascicularis monkeys from Mauritius to different species of Plasmodium. J Parasitol, 78, 505511.Google Scholar
Corredor, V., Meyer, E. V., Lapp, S., Corredor-Medina, C., Huber, C. S., Evans, A. G., Barnwell, J. W. and Galinski, M. R. (2004). A SICAvar switching event in Plasmodium knowlesi is associated with the DNA rearrangement of conserved 3′ non-coding sequences. Molecular & Biochemical Parasitology 138, 3749.CrossRefGoogle ScholarPubMed
Cox-Singh, J., Davis, T. M., Lee, K. S., Shamsul, S. S., Matusop, A., Ratnam, S., Rahman, H. A., Conway, D. J. and Singh, B. (2008). Plasmodium knowlesi malaria in humans is widely distributed and potentially life threatening. Clinical Infectious Diseases 46, 165171.Google Scholar
Cox-Singh, J., Hiu, J., Lucas, S. B., Divis, P. C., Zulkarnaen, M., Chandran, P., Wong, K. T., Adem, P., Zaki, S. R., Singh, B. and Krishna, S. (2010). Severe malaria - a case of fatal Plasmodium knowlesi infection with post-mortem findings: a case report. Malaria Journal 9, 10.Google Scholar
Craig, A. G., Grau, G. E., Janse, C., Kazura, J. W., Milner, D., Barnwell, J. W., Turner, G., Langhorne, J. and participants of the Hinxton Retreat meeting on Animal Models for Research on Severe, M. (2012). The role of animal models for research on severe malaria. PLoS Pathogens 8, e1002401.Google Scholar
Cunnington, A. J., Riley, E. M. and Walther, M. (2013). Stuck in a rut? Reconsidering the role of parasite sequestration in severe malaria syndromes. Trends in Parasitology 29, 585592.Google Scholar
Daneshvar, C., Davis, T. M., Cox-Singh, J., Rafa'ee, M. Z., Zakaria, S. K., Divis, P. C. and Singh, B. (2009). Clinical and laboratory features of human Plasmodium knowlesi infection. Clinical Infectious Diseases 49, 852860.Google Scholar
Dankwa, S., Lim, C., Bei, A. K., Jiang, R. H., Abshire, J. R., Patel, S. D., Goldberg, J. M., Moreno, Y., Kono, M., Niles, J. C. and Duraisingh, M. T. (2016). Ancient human sialic acid variant restricts an emerging zoonotic malaria parasite. Nature Communications 7, 11187.Google Scholar
de Koning-Ward, T. F., Gilson, P. R. and Crabb, B. S. (2015). Advances in molecular genetic systems in malaria. Nature Reviews. Microbiology 13, 373387.Google Scholar
Deans, J. A., Alderson, T., Thomas, A. W., Mitchell, G. H., Lennox, E. S. and Cohen, S. (1982). Rat monoclonal antibodies which inhibit the in vitro multiplication of Plasmodium knowlesi . Clinical and Experimental Immunology 49, 297309.Google Scholar
Deans, J. A., Knight, A. M., Jean, W. C., Waters, A. P., Cohen, S. and Mitchell, G. H. (1988). Vaccination trials in rhesus monkeys with a minor, invariant, Plasmodium knowlesi 66 kD merozoite antigen. Parasite Immunology 10, 535552.Google Scholar
Dennis, E. D., Mitchell, G. H., Butcher, G. A. and Cohen, S. (1975). In vitro isolation of Plasmodium knowlesi merozoites using polycarbonate sieves. Parasitology 71, 475481.CrossRefGoogle ScholarPubMed
Doudna, J. A. and Charpentier, E. (2014). Genome editing. The new frontier of genome engineering with CRISPR-Cas9. Science 346, 1258096.Google Scholar
Doxiadis, G. G., Otting, N., de Groot, N. G., de Groot, N., Rouweler, A. J., Noort, R., Verschoor, E. J., Bontjer, I. and Bontrop, R. E. (2003). Evolutionary stability of MHC class II haplotypes in diverse rhesus macaque populations. Immunogenetics 55, 540551.CrossRefGoogle ScholarPubMed
Duraisingh, M. T., Triglia, T. and Cowman, A. F. (2002). Negative selection of Plasmodium falciparum reveals targeted gene deletion by double crossover recombination. International Journal for Parasitology 32, 8189.Google Scholar
Dutta, G. P. (1982). Non lethal chronic infection in Bonnet monkeys (macaca radiate). Indian J Med Res, 134140.Google Scholar
Epstein, J. E., Charoenvit, Y., Kester, K. E., Wang, R., Newcomer, R., Fitzpatrick, S., Richie, T. L., Tornieporth, N., Heppner, D. G., Ockenhouse, C., Majam, V., Holland, C., Abot, E., Ganeshan, H., Berzins, M., Jones, T., Freydberg, C. N., Ng, J., Norman, J., Carucci, D. J., Cohen, J. and Hoffman, S. L. (2004). Safety, tolerability, and antibody responses in humans after sequential immunization with a PfCSP DNA vaccine followed by the recombinant protein vaccine RTS,S/AS02A. Vaccine 22, 15921603.Google Scholar
Epstein, J. E., Tewari, K., Lyke, K. E., Sim, B. K., Billingsley, P. F., Laurens, M. B., Gunasekera, A., Chakravarty, S., James, E. R., Sedegah, M., Richman, A., Velmurugan, S., Reyes, S., Li, M., Tucker, K., Ahumada, A., Ruben, A. J., Li, T., Stafford, R., Eappen, A. G., Tamminga, C., Bennett, J. W., Ockenhouse, C. F., Murphy, J. R., Komisar, J., Thomas, N., Loyevsky, M., Birkett, A., Plowe, C. V., Loucq, C., Edelman, R., Richie, T. L., Seder, R. A. and Hoffman, S. L. (2011). Live attenuated malaria vaccine designed to protect through hepatic CD8(+) T cell immunity. Science 334, 475480.Google Scholar
Faber, B. W., Younis, S., Remarque, E. J., Rodriguez Garcia, R., Riasat, V., Walraven, V., van der Werff, N., van der Eijk, M., Cavanagh, D. R., Holder, A. A., Thomas, A. W. and Kocken, C. H. (2013). Diversity covering AMA1-MSP119 fusion proteins as malaria vaccines. Infection and Immunity 81, 14791490.Google Scholar
Fatih, F. A., Siner, A., Ahmed, A., Woon, L. C., Craig, A. G., Singh, B., Krishna, S. and Cox-Singh, J. (2012). Cytoadherence and virulence - the case of Plasmodium knowlesi malaria. Malaria Journal 11, 33.CrossRefGoogle ScholarPubMed
Fatih, F. A., Staines, H. M., Siner, A., Ahmed, M. A., Woon, L. C., Pasini, E. M., Kocken, C. H., Singh, B., Cox-Singh, J. and Krishna, S. (2013). Susceptibility of human Plasmodium knowlesi infections to anti-malarials. Malaria Journal 12, 425.Google Scholar
Fisk, T. L., Millet, P., Collins, W. E. and Nguyen-Dinh, P. (1989). In vitro activity of antimalarial compounds on the exoerythrocytic stages of Plasmodium cynomolgi and P. knowlesi . Am J Trop Med Hyg 40, 235239.Google Scholar
Flynn, S., Satkoski, J., Lerche, N., Kanthaswamy, S. and Smith, D. G. (2009). Genetic variation at the TNF-alpha promoter and malaria susceptibility in rhesus (Macaca mulatta) and long-tailed (Macaca fascicularis) macaques. Infection Genetics and Evolution 9, 769777.Google Scholar
Frech, C. and Chen, N. (2011). Genome comparison of human and non-human malaria parasites reveals species subset-specific genes potentially linked to human disease. PLoS Computational Biology 7, e1002320.Google Scholar
Galinski, M. R. and Corredor, V. (2004). Variant antigen expression in malaria infections: posttranscriptional gene silencing, virulence and severe pathology. Molecular & Biochemical Parasitology 134, 1725.Google Scholar
Ghorbal, M., Gorman, M., Macpherson, C. R., Martins, R. M., Scherf, A. and Lopez-Rubio, J. J. (2014). Genome editing in the human malaria parasite Plasmodium falciparum using the CRISPR-Cas9 system. Nature Biotechnology 32, 819821.Google Scholar
Goonewardene, R., Daily, J., Kaslow, D., Sullivan, T. J., Duffy, P., Carter, R., Mendis, K. and Wirth, D. (1993). Transfection of the malaria parasite and expression of firefly luciferase. Proceedings of the National Academy of Sciences of the United States of America 90, 52345236.Google Scholar
Grau, G. E. and Craig, A. G. (2012). Cerebral malaria pathogenesis: revisiting parasite and host contributions. Future Microbiology 7, 291302.CrossRefGoogle ScholarPubMed
Hamid, M. M., Remarque, E. J., El Hassan, I. M., Hussain, A. A., Narum, D. L., Thomas, A. W., Kocken, C. H., Weiss, W. R. and Faber, B. W. (2011). Malaria infection by sporozoite challenge induces high functional antibody titres against blood stage antigens after a DNA prime, poxvirus boost vaccination strategy in Rhesus macaques. Malaria Journal 10, 29.Google Scholar
Helms, G., Dasanna, A. K., Schwarz, U. S. and Lanzer, M. (2016). Modeling cytoadhesion of Plasmodium falciparum-infected erythrocytes and leukocytes-common principles and distinctive features. FEBS Letters 590, 19551971.Google Scholar
Hoffman, S. L., Billingsley, P. F., James, E., Richman, A., Loyevsky, M., Li, T., Chakravarty, S., Gunasekera, A., Chattopadhyay, R., Li, M., Stafford, R., Ahumada, A., Epstein, J. E., Sedegah, M., Reyes, S., Richie, T. L., Lyke, K. E., Edelman, R., Laurens, M. B., Plowe, C. V. and Sim, B. K. (2010). Development of a metabolically active, non-replicating sporozoite vaccine to prevent Plasmodium falciparum malaria. Human Vaccines 6, 97106.Google Scholar
Howard, R. J. and Barnwell, J. W. (1985). Immunochemical analysis of surface membrane antigens on erythrocytes infected with non-cloned SICA[+] or cloned SICA[-] Plasmodium knowlesi . Parasitology 91(Pt 2), 245261.Google Scholar
Howard, R. J., Barnwell, J. W. and Kao, V. (1983). Antigenic variation of Plasmodium knowlesi malaria: identification of the variant antigen on infected erythrocytes. Proceedings of the National Academy of Sciences of the United States of America 80, 41294133.Google Scholar
Ibiwoye, M. O., Howard, C. V., Sibbons, P., Hasan, M. and van Velzen, D. (1993). Cerebral malaria in the rhesus monkey (Macaca mulatta): observations on host pathology. Journal of Comparative Pathology 108, 303310.Google Scholar
Ibiwoye, M. O., Sibbons, P. D., Hasan, M., Howard, C. V., Desalu, A. B., Singhal, K. C. and van Velzen, D. (1995). Lipofuscin pigment in cerebellar Purkinje neurones and choroid plexus epithelial cells of macaque monkeys with Plasmodium knowlesi cerebral malaria: an electron microscopical observation. Zentralbl Veterinarmed B 42, 140146.Google Scholar
Ishizuka, A. S., Lyke, K. E., DeZure, A., Berry, A. A., Richie, T. L., Mendoza, F. H., Enama, M. E., Gordon, I. J., Chang, L. J., Sarwar, U. N., Zephir, K. L., Holman, L. A., James, E. R., Billingsley, P. F., Gunasekera, A., Chakravarty, S., Manoj, A., Li, M., Ruben, A. J., Li, T., Eappen, A. G., Stafford, R. E., K, C. N., Murshedkar, T., DeCederfelt, H., Plummer, S. H., Hendel, C. S., Novik, L., Costner, P. J., Saunders, J. G., Laurens, M. B., Plowe, C. V., Flynn, B., Whalen, W. R., Todd, J. P., Noor, J., Rao, S., Sierra-Davidson, K., Lynn, G. M., Epstein, J. E., Kemp, M. A., Fahle, G. A., Mikolajczak, S. A., Fishbaugher, M., Sack, B. K., Kappe, S. H., Davidson, S. A., Garver, L. S., Bjorkstrom, N. K., Nason, M. C., Graham, B. S., Roederer, M., Sim, B. K., Hoffman, S. L., Ledgerwood, J. E. and Seder, R. A. (2016). Protection against malaria at 1 year and immune correlates following PfSPZ vaccination. Natural Medicines 22, 614623.Google Scholar
Janse, C. J., Franke-Fayard, B., Mair, G. R., Ramesar, J., Thiel, C., Engelmann, S., Matuschewski, K., Gemert, G. J., Sauerwein, R. W. and Waters, A. P. (2006). High efficiency transfection of Plasmodium berghei facilitates novel selection procedures. Molecular & Biochemical Parasitology 145, 6070.Google Scholar
Jerusalem, C., Polder, T., Wijers-Rouw, M., Heinen, U., Eling, W., Osunkoya, B. O. and Trinh, P. (1983). Comparative clinical and experimental study on the pathogenesis of cerebral malaria. Contributions to Microbiology and Immunology 7, 130138.Google Scholar
Jiang, G., Shi, M., Conteh, S., Richie, N., Banania, G., Geneshan, H., Valencia, A., Singh, P., Aguiar, J., Limbach, K., Kamrud, K. I., Rayner, J., Smith, J., Bruder, J. T., King, C. R., Tsuboi, T., Takeo, S., Endo, Y., Doolan, D. L., Richie, T. L. and Weiss, W. R. (2009). Sterile protection against Plasmodium knowlesi in rhesus monkeys from a malaria vaccine: comparison of heterologous prime boost strategies. PLoS ONE 4, e6559.Google Scholar
Jinek, M., Chylinski, K., Fonfara, I., Hauer, M., Doudna, J. A. and Charpentier, E. (2012). A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337, 816821.Google Scholar
Kim, H., Higgins, S., Liles, W. C. and Kain, K. C. (2011). Endothelial activation and dysregulation in malaria: a potential target for novel therapeutics. Current Opinion in Hematology 18, 177185.Google Scholar
Knowles, R. (1935). Monkey malaria. British Medical Journal 1020.Google Scholar
Kocken, C. H., Ozwara, H., van der Wel, A., Beetsma, A. L., Mwenda, J. M. and Thomas, A. W. (2002). Plasmodium knowlesi provides a rapid in vitro and in vivo transfection system that enables double-crossover gene knockout studies. Infection and Immunity 70, 655660.Google Scholar
Kocken, C. H., Zeeman, A. M., Voorberg-van der Wel, A. and Thomas, A. W. (2009). Transgenic Plasmodium knowlesi: relieving a bottleneck in malaria research? Trends in Parasitology 25, 370374.Google Scholar
Langermans, J. A., Andersen, P., van Soolingen, D., Vervenne, R. A., Frost, P. A., van der Laan, T., van Pinxteren, L. A., van den Hombergh, J., Kroon, S., Peekel, I., Florquin, S. and Thomas, A. W. (2001). Divergent effect of bacillus Calmette-Guerin (BCG) vaccination on Mycobacterium tuberculosis infection in highly related macaque species: implications for primate models in tuberculosis vaccine research. Proceedings of the National Academy of Sciences of the United States of America 98, 1149711502.Google Scholar
Langhorne, J. and Cohen, S. (1979). Plasmodium knowlesi in the marmoset (Callithrix jacchus). Parasitology 78, 6776.Google Scholar
Langhorne, J., Butcher, G. A., Mitchell, G. H. and Cohen, S. (1977). Preliminary investigations on the role of the spleen in immunology to Plasmodium knowlesi malaria In The role of the spleen in the immunology of parasitic diseases (ed. Torrigiani, G.), pp. 205. Schwabe, Basel.Google Scholar
Langhorne, J., Buffet, P., Galinski, M., Good, M., Harty, J., Leroy, D., Mota, M. M., Pasini, E., Renia, L., Riley, E., Stins, M. and Duffy, P. (2011). The relevance of non-human primate and rodent malaria models for humans. Malaria Journal 10, 23.Google Scholar
Lapp, S. A., Mok, S., Zhu, L., Wu, H., Preiser, P. R., Bozdech, Z. and Galinski, M. R. (2015). Plasmodium knowlesi gene expression differs in ex vivo compared to in vitro blood-stage cultures. Malaria Journal 14, 110.Google Scholar
Lim, C., Hansen, E., DeSimone, T. M., Moreno, Y., Junker, K., Bei, A., Brugnara, C., Buckee, C. O. and Duraisingh, M. T. (2013). Expansion of host cellular niche can drive adaptation of a zoonotic malaria parasite to humans. Nature Communications 4, 1638.Google Scholar
Mahdi, A. A. and Ahmad, S. (1991). Pathogenesis of cerebral malaria. Indian Journal of Experimental Biology 29, 267271.Google Scholar
Mahdi Abdel Hamid, M., Remarque, E. J., van Duivenvoorde, L. M., van der Werff, N., Walraven, V., Faber, B. W., Kocken, C. H. and Thomas, A. W. (2011). Vaccination with Plasmodium knowlesi AMA1 formulated in the novel adjuvant co-vaccine HT protects against blood-stage challenge in Rhesus Macaques. PLoS ONE 6, e20547.Google Scholar
Menard, R., Sultan, A. A., Cortes, C., Altszuler, R., van Dijk, M. R., Janse, C. J., Waters, A. P., Nussenzweig, R. S. and Nussenzweig, V. (1997). Circumsporozoite protein is required for development of malaria sporozoites in mosquitoes. Nature 385, 336340.Google Scholar
Messaoudi, I., Estep, R., Robinson, B. and Wong, S. W. (2011). Nonhuman primate models of human immunology. Antioxidants & Redox Signaling 14, 261273.Google Scholar
Miller, L. H., Usami, S. and Chien, S. (1971). Alteration in the rheologic properties of Plasmodium knowlesi-infected red cells. A possible mechanism for capillary obstruction. The Journal of Clinical Investigation 50, 14511455.Google Scholar
Millet, P., Collins, W. E., Aikawa, M., Cochrane, A. H. and Nguyen-Dinh, P. (1990). Use of non-human primate hepatocytes for in vitro study of the pre-erythrocytic stages of malaria parasites. Bulletin of the World Health Organization 68 (Suppl.), 6065.Google ScholarPubMed
Mitchell, G. H., Butcher, G. A. and Cohen, S. (1975). Merozoite vaccination against Plasmodium knowlesi malaria. Immunology 29, 397407.Google Scholar
Mitchell, G. H., Butcher, G. A., Langhorne, J. and Cohen, S. (1977). A freeze-dried merozoite vaccine effective against Plasmodium knowlesi malaria. Clinical and Experimental Immunology 28, 276279.Google Scholar
Moon, R. W., Hall, J., Rangkuti, F., Ho, Y. S., Almond, N., Mitchell, G. H., Pain, A., Holder, A. A. and Blackman, M. J. (2013). Adaptation of the genetically tractable malaria pathogen Plasmodium knowlesi to continuous culture in human erythrocytes. Proceedings of the National Academy of Sciences of the United States of America 110, 531536.CrossRefGoogle ScholarPubMed
Moon, R. W., Sharaf, H., Hastings, C. H., Ho, Y. S., Nair, M. B., Rchiad, Z., Knuepfer, E., Ramaprasad, A., Mohring, F., Amir, A., Yusuf, N. A., Hall, J., Almond, N., Lau, Y. L., Pain, A., Blackman, M. J. and Holder, A. A. (2016). Normocyte-binding protein required for human erythrocyte invasion by the zoonotic malaria parasite Plasmodium knowlesi . Proceedings of the National Academy of Sciences of the United States of America 113, 72317236.Google Scholar
Moyes, C. L., Shearer, F. M., Huang, Z., Wiebe, A., Gibson, H. S., Nijman, V., Mohd-Azlan, J., Brodie, J. F., Malaivijitnond, S., Linkie, M., Samejima, H., O'Brien, T. G., Trainor, C. R., Hamada, Y., Giordano, A. J., Kinnaird, M. F., Elyazar, I. R., Sinka, M. E., Vythilingam, I., Bangs, M. J., Pigott, D. M., Weiss, D. J., Golding, N. and Hay, S. I. (2016). Predicting the geographical distributions of the macaque hosts and mosquito vectors of Plasmodium knowlesi malaria in forested and non-forested areas. Parasites & Vectors 9, 242.Google Scholar
Murphy, J. R., Weiss, W. R., Fryauff, D., Dowler, M., Savransky, T., Stoyanov, C., Muratova, O., Lambert, L., Orr-Gonzalez, S., Zeleski, K. L., Hinderer, J., Fay, M. P., Joshi, G., Gwadz, R. W., Richie, T. L., Villasante, E. F., Richardson, J. H., Duffy, P. E. and Chen, J. (2014). Using infective mosquitoes to challenge monkeys with Plasmodium knowlesi in malaria vaccine studies. Malaria Journal 13, 215.Google Scholar
Nyakundi, R. K., Nyamongo, O., Maamun, J., Akinyi, M., Mulei, I., Farah, I. O., Blankenship, D., Grimberg, B., Hau, J., Malhotra, I., Ozwara, H., King, C. L. and Kariuki, T. M. (2016). Protective effect of Chronic Schistosomiasis in Baboons coinfected with Schistosoma mansoni and Plasmodium knowlesi . Infection and Immunity 84, 13201330.Google Scholar
Onditi, F. I., Nyamongo, O. W., Omwandho, C. O., Maina, N. W., Maloba, F., Farah, I. O., King, C. L., Moore, J. M. and Ozwara, H. S. (2015). Parasite accumulation in placenta of non-immune baboons during Plasmodium knowlesi infection. Malaria Journal 14, 118.Google Scholar
Ozwara, H., Langermans, J. A., Kocken, C. H., van der Wel, A., van der Meide, P. H., Vervenne, R. A., Mwenda, J. M. and Thomas, A. W. (2003 a). Transfected Plasmodium knowlesi produces bioactive host gamma interferon: a new perspective for modulating immune responses to malaria parasites. Infection and Immunity 71, 43754381.Google Scholar
Ozwara, H., Langermans, J. A., Maamun, J., Farah, I. O., Yole, D. S., Mwenda, J. M., Weiler, H. and Thomas, A. W. (2003 b). Experimental infection of the olive baboon (Paplio anubis) with Plasmodium knowlesi: severe disease accompanied by cerebral involvement. American Journal of Tropical Medicine and Hygiene 69, 188194.Google Scholar
Ozwara, H., van der Wel, A., Kocken, C. H. and Thomas, A. W. (2003 c). Heterologous promoter activity in stable and transient Plasmodium knowlesi transgenes. Molecular & Biochemical Parasitology 130, 6164.Google Scholar
Pain, A., Bohme, U., Berry, A. E., Mungall, K., Finn, R. D., Jackson, A. P., Mourier, T., Mistry, J., Pasini, E. M., Aslett, M. A., Balasubrammaniam, S., Borgwardt, K., Brooks, K., Carret, C., Carver, T. J., Cherevach, I., Chillingworth, T., Clark, T. G., Galinski, M. R., Hall, N., Harper, D., Harris, D., Hauser, H., Ivens, A., Janssen, C. S., Keane, T., Larke, N., Lapp, S., Marti, M., Moule, S., Meyer, I. M., Ormond, D., Peters, N., Sanders, M., Sanders, S., Sargeant, T. J., Simmonds, M., Smith, F., Squares, R., Thurston, S., Tivey, A. R., Walker, D., White, B., Zuiderwijk, E., Churcher, C., Quail, M. A., Cowman, A. F., Turner, C. M., Rajandream, M. A., Kocken, C. H., Thomas, A. W., Newbold, C. I., Barrell, B. G. and Berriman, M. (2008). The genome of the simian and human malaria parasite Plasmodium knowlesi . Nature 455, 799803.Google Scholar
Pasini, E. M., Kirkegaard, M., Mortensen, P., Mann, M. and Thomas, A. W. (2010). Deep-coverage rhesus red blood cell proteome: a first comparison with the human and mouse red blood cell. Blood Transfusion 8 (Suppl. 3), s126s139.Google Scholar
Peterson, M. G., Marshall, V. M., Smythe, J. A., Crewther, P. E., Lew, A., Silva, A., Anders, R. F. and Kemp, D. J. (1989). Integral membrane protein located in the apical complex of Plasmodium falciparum . Molecular and Cellular Biology 9, 31513154.Google Scholar
Price, R. N., Tjitra, E., Guerra, C. A., Yeung, S., White, N. J. and Anstey, N. M. (2007). Vivax malaria: neglected and not benign. American Journal of Tropical Medicine and Hygiene 77, 7987.Google Scholar
Rajahram, G. S., Barber, B. E., William, T., Grigg, M. J., Menon, J., Yeo, T. W. and Anstey, N. M. (2016). Falling Plasmodium knowlesi malaria death rate among adults despite rising Incidence, Sabah, Malaysia, 2010–2014. Emerging Infectious Diseases 22, 4148.Google Scholar
Remarque, E. J., Faber, B. W., Kocken, C. H. and Thomas, A. W. (2008). Apical membrane antigen 1: a malaria vaccine candidate in review. Trends in Parasitology 24, 7484.Google Scholar
Richards, W. H., Mitchell, G. H. Butcher, G. A. and Cohen, S. (1977). Merozoite vaccination of rhesus monkeys against Plasmodium knowlesi malaria; immunity to sporozoite (mosquito-transmitted) challenge. Parasitology 191198.Google Scholar
Richie, T. L., Billingsley, P. F., Sim, B. K., James, E. R., Chakravarty, S., Epstein, J. E., Lyke, K. E., Mordmuller, B., Alonso, P., Duffy, P. E., Doumbo, O. K., Sauerwein, R. W., Tanner, M., Abdulla, S., Kremsner, P. G., Seder, R. A. and Hoffman, S. L. (2015). Progress with Plasmodium falciparum sporozoite (PfSPZ)-based malaria vaccines. Vaccine 33, 74527461.Google Scholar
Roestenberg, M., Teirlinck, A. C., McCall, M. B., Teelen, K., Makamdop, K. N., Wiersma, J., Arens, T., Beckers, P., van Gemert, G., van de Vegte-Bolmer, M., van der Ven, A. J., Luty, A. J., Hermsen, C. C. and Sauerwein, R. W. (2011). Long-term protection against malaria after experimental sporozoite inoculation: an open-label follow-up study. Lancet 377, 17701776.Google Scholar
Rogers, W. O., Baird, J. K., Kumar, A., Tine, J. A., Weiss, W., Aguiar, J. C., Gowda, K., Gwadz, R., Kumar, S., Gold, M. and Hoffman, S. L. (2001). Multistage multiantigen heterologous prime boost vaccine for Plasmodium knowlesi malaria provides partial protection in rhesus macaques. Infection and Immunity 69, 55655572.Google Scholar
Rogers, W. O., Weiss, W. R., Kumar, A., Aguiar, J. C., Tine, J. A., Gwadz, R., Harre, J. G., Gowda, K., Rathore, D., Kumar, S. and Hoffman, S. L. (2002). Protection of rhesus macaques against lethal Plasmodium knowlesi malaria by a heterologous DNA priming and poxvirus boosting immunization regimen. Infection and Immunity 70, 43294335.Google Scholar
Salinas, J. L., Kissinger, J. C., Jones, D. P. and Galinski, M. R. (2014). Metabolomics in the fight against malaria. Memorias do Instituto Oswaldo Cruz 109, 589597.Google Scholar
Schmidt, L. H., Fradkin, R., Harrison, J. and Rossan, R. N. (1977). Differences in the virulence of Plasmodium knowlesi for Macaca irus (fascicularis) of Philippine and Malayan origins. American Journal of Tropical Medicine and Hygiene 26, 612622.Google Scholar
Sedegah, M., Hedstrom, R., Hobart, P. and Hoffman, S. L. (1994). Protection against malaria by immunization with plasmid DNA encoding circumsporozoite protein. Proceedings of the National Academy of Sciences of the United States of America 91, 98669870.Google Scholar
Sedegah, M., Jones, T. R., Kaur, M., Hedstrom, R., Hobart, P., Tine, J. A. and Hoffman, S. L. (1998). Boosting with recombinant vaccinia increases immunogenicity and protective efficacy of malaria DNA vaccine. Proceedings of the National Academy of Sciences of the United States of America 95, 76487653.Google Scholar
Sedegah, M., Weiss, W., Sacci, J. B. Jr., Charoenvit, Y., Hedstrom, R., Gowda, K., Majam, V. F., Tine, J., Kumar, S., Hobart, P. and Hoffman, S. L. (2000). Improving protective immunity induced by DNA-based immunization: priming with antigen and GM-CSF-encoding plasmid DNA and boosting with antigen-expressing recombinant poxvirus. Journal of Immunology 164, 59055912.Google Scholar
Siddiqui, W. A., Schnell, J. V. and Richmond-Crum, S. M. (1974). Susceptibility of a new world monkey (Aotus trivirgatus) to an old world simian malarial parasite (Plasmodium knowlesi). Trans R Soc Trop Med Hyg 68, 387391.Google Scholar
Shastri, S., Zeeman, A. M., Berry, L., Verburgh, R. J., Braun-Breton, C., Thomas, A. W., Gannoun-Zaki, L., Kocken, C. H. and Vial, H. J. (2010). Plasmodium CDP-DAG synthase: an atypical gene with an essential N-terminal extension. International Journal for Parasitology 40, 12571268.Google Scholar
Silva, J. C., Egan, A., Arze, C., Spouge, J. L. and Harris, D. G. (2015). A new method for estimating species age supports the coexistence of malaria parasites and their mammalian hosts. Molecular Biology and Evolution 32, 13541364.Google Scholar
Singh, B. and Daneshvar, C. (2013). Human infections and detection of Plasmodium knowlesi . Clinical Microbiology Reviews 26, 165184.Google Scholar
Singh, A. P., Ozwara, H., Kocken, C. H., Puri, S. K., Thomas, A. W. and Chitnis, C. E. (2005). Targeted deletion of Plasmodium knowlesi Duffy binding protein confirms its role in junction formation during invasion. Molecular Microbiology 55, 19251934.Google Scholar
Sinton, J. A. and Mulligan, H. W. (1932). A critical review of the lieterature relating to the identification of the malaria parasites recorded from monkeys of the families Cercopithecidae and Colobidae. Records of the Malaria Survey of India III, 357443.Google Scholar
Siregar, J. E., Faust, C. L., Murdiyarso, L. S., Rosmanah, L., Saepuloh, U., Dobson, A. P. and Iskandriati, D. (2015). Non-invasive surveillance for Plasmodium in reservoir macaque species. Malaria Journal 14, 404.Google Scholar
Tarr, S. J., Moon, R. W., Hardege, I. and Osborne, A. R. (2014). A conserved domain targets exported PHISTb family proteins to the periphery of Plasmodium infected erythrocytes. Molecular & Biochemical Parasitology 196, 2940.Google Scholar
van der Wel, A. M., Tomas, A. M., Kocken, C. H., Malhotra, P., Janse, C. J., Waters, A. P. and Thomas, A. W. (1997). Transfection of the primate malaria parasite Plasmodium knowlesi using entirely heterologous constructs. Journal of Experimental Medicine 185, 14991503.Google Scholar
van Dijk, M. R., Waters, A. P. and Janse, C. J. (1995). Stable transfection of malaria parasite blood stages. Science 268, 13581362.Google Scholar
Vythilingam, I., Tan, C. H., Asmad, M., Chan, S. T., Lee, K. S. and Singh, B. (2006). Natural transmission of Plasmodium knowlesi to humans by Anopheles latens in Sarawak, Malaysia. Transactions of the Royal Society of Tropical Medicine and Hygiene 100, 10871088.Google Scholar
Wagner, J. C., Platt, R. J., Goldfless, S. J., Zhang, F. and Niles, J. C. (2014). Efficient CRISPR-Cas9-mediated genome editing in Plasmodium falciparum . Nature Methods 11, 915918.Google Scholar
Wang, R., Epstein, J., Baraceros, F. M., Gorak, E. J., Charoenvit, Y., Carucci, D. J., Hedstrom, R. C., Rahardjo, N., Gay, T., Hobart, P., Stout, R., Jones, T. R., Richie, T. L., Parker, S. E., Doolan, D. L., Norman, J. and Hoffman, S. L. (2001). Induction of CD4(+) T cell-dependent CD8(+) type 1 responses in humans by a malaria DNA vaccine. Proceedings of the National Academy of Sciences of the United States of America 98, 1081710822.Google Scholar
Weiss, W. R. and Jiang, C. G. (2012). Protective CD8+ T lymphocytes in primates immunized with malaria sporozoites. PLoS ONE 7, e31247.Google Scholar
Wel, A., Kocken, C. H., Pronk, T. C., Franke-Fayard, B. and Thomas, A. W. (2004). New selectable markers and single crossover integration for the highly versatile Plasmodium knowlesi transfection system. Molecular & Biochemical Parasitology 134, 97104.Google Scholar
White, N. J., Turner, G. D., Medana, I. M., Dondorp, A. M. and Day, N. P. (2010). The murine cerebral malaria phenomenon. Trends in Parasitology 26, 1115.Google Scholar
White, N. J., Turner, G. D., Day, N. P. and Dondorp, A. M. (2013). Lethal malaria: Marchiafava and Bignami were right. Journal of Infectious Diseases 208, 192198.Google Scholar
World Health Organisation (2015). World Malaria Report. World Health Organisation, Geneva, Switserland.Google Scholar
Wu, Y., Sifri, C. D., Lei, H. H., Su, X. Z. and Wellems, T. E. (1995). Transfection of Plasmodium falcipaprum within human red blood cells. Proceedings of the National Academy of Sciences of the United States of America 92, 973977.Google Scholar
Yusof, R., Lau, Y. L., Mahmud, R., Fong, M. Y., Jelip, J., Ngian, H. U., Mustakim, S., Hussin, H. M., Marzuki, N. and Mohd Ali, M. (2014). High proportion of knowlesi malaria in recent malaria cases in Malaysia. Malaria Journal 13, 168.Google Scholar
Yusuf, N. A., Green, J. L., Wall, R. J., Knuepfer, E., Moon, R. W., Schulte-Huxel, C., Stanway, R. R., Martin, S. R., Howell, S. A., Douse, C. H., Cota, E., Tate, E. W., Tewari, R. and Holder, A. A. (2015). The Plasmodium class XIV Myosin, MyoB, has a distinct subcellular location in invasive and motile stages of the malaria parasite and an unusual light chain. Journal of Biological Chemistry 290, 1214712164.Google Scholar
Zeeman, A. M., van Amsterdam, S. M., McNamara, C. W., Voorberg-van der Wel, A., Klooster, E. J., van den Berg, A., Remarque, E. J., Plouffe, D. M., van Gemert, G. J., Luty, A., Sauerwein, R., Gagaring, K., Borboa, R., Chen, Z., Kuhen, K., Glynne, R. J., Chatterjee, A. K., Nagle, A., Roland, J., Winzeler, E. A., Leroy, D., Campo, B., Diagana, T. T., Yeung, B. K., Thomas, A. W. and Kocken, C. H. (2014). KAI407, a potent Non-8-Aminoquinoline compound that kills Plasmodium cynomolgi early dormant liver stage parasites in vitro. Antimicrobial Agents and Chemotherapy 58, 15861595.Google Scholar
Zhang, C., Xiao, B., Jiang, Y., Zhao, Y., Li, Z., Gao, H., Ling, Y., Wei, J., Li, S., Lu, M., Su, X. Z., Cui, H. and Yuan, J. (2014). Efficient editing of malaria parasite genome using the CRISPR/Cas9 system. MBio 5, e0141401414.Google Scholar
Zimin, A. V., Cornish, A. S., Maudhoo, M. D., Gibbs, R. M., Zhang, X., Pandey, S., Meehan, D. T., Wipfler, K., Bosinger, S. E., Johnson, Z. P., Tharp, G. K., Marcais, G., Roberts, M., Ferguson, B., Fox, H. S., Treangen, T., Salzberg, S. L., Yorke, J. A. and Norgren, R. B. Jr. (2014). A new rhesus macaque assembly and annotation for next-generation sequencing analyses. Biology Direct 9, 20.Google Scholar