Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-10T09:43:07.623Z Has data issue: false hasContentIssue false
  • English
  • Français

The role of Plasmodium knowlesi in the history of malaria research

Published online by Cambridge University Press:  10 November 2016

G. A. BUTCHER  and
G. H. MITCHELL
G. A. BUTCHER
Affiliation:
Retired. Formerly, Faculty of Life Sciences, Imperial College, London, UK
G. H. MITCHELL*
Affiliation:
School of Biological Sciences, University of Essex, Wivenhoe Park, Colchester, Essex CO3 4SQ, UK
*
*Corresponding author: School of Biological Sciences, University of Essex, Wivenhoe Park, Colchester, Essex CO3 4SQ, UK. E-mail: gmitch@essex.ac.uk
Get access Rights & Permissions [Opens in a new window]

Summary

In recent years, a malaria infection of humans in South East Asia, originally diagnosed as a known human-infecting species, Plasmodium malariae, has been identified as a simian parasite, Plasmodium knowlesi. This species had been subject to considerable investigation in monkeys since the 1930s. With the development of continuous culture of the erythrocytic stages of the human malarial parasite, Plasmodium falciparum in 1976, the emphasis in research shifted away from knowlesi. However, its importance as a human pathogen has provoked a renewed interest in P. knowlesi, not least because it too can be maintained in continuous culture and thus provides an experimental model. In fact, this parasite species has a long history in malaria research, and the purpose of this chapter is to outline approximately the first 50 years of this history.

Keywords

malariaplasmodiumknowlesihistorymonkeymacaqueimmunitypathologyculture
Type
Special Issue Review
Information
Parasitology , Volume 145 , Special Issue 1: Plasmodium knowlesi , January 2018 , pp. 6 - 17
Check for updates
Copyright
Copyright © Cambridge University Press 2016 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Aberle, S. D. (1945). Primate Malaria. US National Research Council, Division of Medical Science, Washington, DC.Google Scholar
Ahmed, A. M., Pinheiro, M. M., Divis, P. C., Siner, A., Zainudin, R., Wong, I. T., Lu, C. W., Singh-Khaira, S. K., Millar, S. B., Lynch, S., Willmann, M., Singh, B., Krishna, S. and Cox-Singh, J. (2014). Disease progression in Plasmodium knowlesi malaria is linked to variation in invasion gene family members. PLoS Neglected Tropical Diseases 14, e3086.CrossRefGoogle Scholar
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, 72–82.CrossRefGoogle ScholarPubMed
Anfinsen, C. B., Geiman, Q. M., McKee, R. W., Ormsbee, R. A. and Ball, E. G. (1946). Studies on malarial parasites. VIII. nutrition of Plasmodium knowlesi. Factors affecting the growth of Plasmodium knowlesi in vitro . Journal of Experimental Medicine 84, 607–621.Google Scholar
Assefa, S., Lim, C., Preston, M. D., Duffy, C. W., Nair, M. B., Adroub, S. A., Kadir, K. A., Goldberg, J. M., Neafsey, D. E., Divis, P., Clark, T. G., Duraisingh, M. T., Conway, D. J., Pain, A. and Singh, B. (2015). Population genomic structure and adaptation in the zoonotic malaria parasite Plasmodium knowlesi . Proceedings of the National Academy of Sciences of the United States of America 112, 13027–13032.CrossRefGoogle ScholarPubMed
Ball, E. G., McKee, R. W., Anfinsen, C. B., Cruz, W. O. and Geiman, Q. M. (1948). Studies on malarial parasites. IX. Chemical and metabolic changes during growth and multiplication in vivo and in vitro . Journal of Biological Chemistry 175, 547–571.CrossRefGoogle Scholar
Bannister, L. H., Butcher, G. A., Dennis, E. D. and Mitchell, G. H. (1975). Structure and invasive behaviour of Plasmodium knowlesi merozoites in vitro . Parasitology 71, 483–491.Google Scholar
Bannister, L. H., Mitchell, G. H., Butcher, G. A. and Dennis, E. D. (1986). Lamellar membranes associated with rhoptries in erythrocytic merozoites of Plasmodium knowlesi: a clue to the mechanism of invasion. Parasitology 92, 291–303.CrossRefGoogle Scholar
Banyal, H. S., Misra, G. C., Gupta, C. M. and Dutta, G. P. (1981). Involvement of malarial proteases in the interaction between the parasite and host erythrocyte in Plasmodium knowlesi infections. Journal of Parasitology 67, 623–626.Google Scholar
Barnwell, J. W., Howard, R. K. and Miller, L. H. (1983). Influence of the spleen on the expression of surface antigens on parasitized red cells. In Malaria and the Red Cell (ed. Evered, D. and Whelan, J.), pp. 117–136. CIBA Foundation Symposium 94. Pitman, London.Google Scholar
Bass, C. C. and Johns, F. M. (1912). The cultivation of malarial plasmodia (Plasmodium vivax and Plasmodium falciparum) in vitro . Journal of Experimental Medicine 16, 567–579.Google Scholar
Bertagna, P., Cohen, S., Geiman, Q. M., Haworth, J., Konigk, E., Richards, W. H. G. and Trigg, P. I. (1972). Cultivation techniques for the erythrocytic stages of malaria parasites. Bulletin of the World Health Organisation 47, 357–373.Google Scholar
Brown, I. N. and Brown, K. N. (1965). Immunity to malaria: antigenic variation in chronic infections of P. knowlesi . Nature 208, 1286–1288.Google Scholar
Brown, K. N., Brown, I. N. and Hills, L. A. (1970 a). Immunity to malaria: I protection against Plasmodium knowlesi shown by monkeys sensitised by drug-suppressed infections or by dead parasites in Freund's adjuvant. Experimental Parasitology 28, 304–317.CrossRefGoogle ScholarPubMed
Brown, K. N., Brown, I. N., Phillips, R. S., Trigg, P. L., Hills, L. A., Wolstencroft, R. A. and Dumonde, D. C. (1970 b). Immunity to malaria: studies with Plasmodium knowlesi . Transactions of the Royal Society of Tropical Medicine and Hygiene 64, 3–5.Google ScholarPubMed
Butcher, G. A. (1970). Experimental studies on immunity to Plasmodium knowlesi . Ph.D. thesis. University of London, London.Google Scholar
Butcher, G. A. (1979). Factors affecting the in vitro culture of Plasmodium falciparum and Plasmodium knowlesi . Bulletin of the World Health Organisation 57 (Suppl. 1) 17–26.Google Scholar
Butcher, G. A. (1982). The behaviour of different strains of Plasmodium falciparum in suspension and static culture. Transactions of the Royal Society of Tropical Medicine and Hygiene 76, 407–409.Google Scholar
Butcher, G. A. (1992). Immunity to simian malaria in the natural hosts–problems for investigation. Southeast Asian Journal of Tropical Medicine and Public Health 23, 177–183.Google Scholar
Butcher, G. A. (1996). Models for malaria: nature knows best. Parasitology Today 12, 378–382.Google Scholar
Butcher, G. A. and Cohen, S. (1970). Schizogony of Plasmodium knowlesi in the presence of normal and immune sera. Transactions of the Royal Society of Tropical Medicine and Hygiene 64, 470 (Film).CrossRefGoogle ScholarPubMed
Butcher, G. A. and Cohen, S. (1971). Short term culture of Plasmodium knowlesi . Parasitology 62, 309–320.CrossRefGoogle ScholarPubMed
Butcher, G. A. and Cohen, S. (1972). Antigenic variation and protective immunity in Plasmodium knowlesi malaria. Immunology 23, 503–521.Google Scholar
Butcher, G. A., Cohen, S. and Garnham, P. C. C. (1970). Passive immunity in Plasmodium knowlesi malaria. Transactions of the Royal Society of Tropical Medicine and Hygiene 64, 850–856.Google Scholar
Butcher, G. A., Mitchell, G. H. and Cohen, S. (1973). Mechanisms of host specificity in malarial infection. Nature 244, 40–42.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, 77–86.Google Scholar
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 (Macaca mulatta). Transactions of the Royal Society of Tropical Medicine and Hygiene 104, 75–77.Google Scholar
Cheong, W. H., Warren, M. W., Omar, A. H. and Mahadevan, S. (1965). Anopheles balabacensis balabacensis identified as vector of simian malaria in Malaysia. Science 150, 1314.CrossRefGoogle ScholarPubMed
Chin, W., Contacos, P. G., Coatney, G. R. and Kimball, H. R. (1965). A naturally acquired quotidian type malaria in man transferable to monkeys. Science 149, 865.Google Scholar
Chin, W., Contacos, P. G., Collins, W. E., Jeter, M. H. and Alpert, E. (1968). Experimental mosquito transmission of Plasmodium knowlesi to man and monkey. American Journal of Tropical Medicine and Hygiene 17, 355–358.CrossRefGoogle Scholar
Ciuca, M., Ballif, L., Chelaresco, M., Lavrineko, M. and Zotta, E. (1937). Contributions a l'etude de l'action pathogene de Pl knowlesi pour l'homme (Considerations sur l'immunite naturalle et l'immunite acquise contre cette espece de parasite). Bulletin de la Societe de Pathologie Exotique 30, 305–315.Google Scholar
Ciuca, M., Chelarescu, M., Sofletea, A., Constantinescu, P.,Teriteanu, E.,Cortez, P., Balanovschi, G. and Ilies, M. (1955). Contribution experimentale a l’ etude de l'immunite dans le paludisme Editions Acad. Rep. Pop. Roumaine pp108 (not seen; cited in Coatneyi et al. 1971).Google Scholar
Clark, H. C. and Tomlinson, W. J. (1949). Pathological anatomy of malaria. In Malariology, Vol. 2 (ed. Boyd, M. F.), pp. 874–903. W B Saunders, Philadelphia.Google Scholar
Clark, I. A. (2009). Along a TNF-paved road from dead parasites in red cells to cerebral malaria and beyond. Parasitology 136, 1457–1468.CrossRefGoogle ScholarPubMed
Coatney, G. R., Collins, W., Warren, M. and Contacos, P. G. (1971). The Primate Malarias. US Department of Health, Education and Welfare, Bethesda, MD, USA.Google Scholar
Cohen, S. and Butcher, G. A. (1969). Comments on immunisation. Military Medicine (Special Issue) 134, 1191–1197.Google Scholar
Cohen, S., Mcgregor, I. A. and Carrington, S. C. (1961). Gamma globulin and acquired immunity to human malaria. Nature 192, 733–737.Google Scholar
Cohen, S., Butcher, G. A. and Crandall, R. B. (1969). Action of malarial antibody in vitro . Nature 223, 368–371.Google Scholar
Cohen, S., Butcher, G. A. and Mitchell, G. H. (1974). Mechanisms of immunity to malaria. Bulletin of the World Health Organisation 50, 251–257.Google Scholar
Coggeshall, L. T. (1943). Immunity to malaria. Medicine 22, 87–102.CrossRefGoogle Scholar
Coggeshall, L. T. and Eaton, M. (1938). Complement fixation reaction in monkey malaria. Journal of Experimental Medicine 68, 29.Google Scholar
Coggeshall, L. T. and Kumm, H. W. (1937). Demonstration of passive immunity in experimental monkey malaria. Journal of Experimental Medicine 66, 177–190.CrossRefGoogle ScholarPubMed
Collins, W. E. (2012). Plasmodium knowlesi: a malaria parasite of monkeys and humans. Annual Review of Entomology 57, 107–121.Google Scholar
Collins, W. E., Contacos, P. G., Skinner, J. C., Chin, W. and Guinn, E. (1967). Fluorescent-antibody studies on simian malaria I Development of antibodies to Plasmodium knowlesi . American Journal of Tropical Medicine and Hygiene 16, 1–6.Google Scholar
Cox-Singh, J. and Singh, B. (2008). Knowlesi malaria: newly emergent and of public health importance. Trends in Parasitology 24, 406–410.Google Scholar
Cox-Singh, J., Davis, T. M. E., Lee, K.-S., Shamsul, S. S., Matusop, A., Rahman, H. A., Conway, D. J. and Singh, B. (2008). Plasmodium knowlesi in humans is widely distributed and potentially life-threatening. Clinical Infectious Diseases 46, 165–171.Google Scholar
Cruz, W. O. and De Mello, R. P. (1947). Infeccao do macaco sul americano ‘sagui’ (Callithrix jacchus) como Plasmodium knowlesi . Memorias do Instituto Oswaldo Cruz 45, 119–121.CrossRefGoogle Scholar
Daniel, T. M. (2010). Merrill Wallace Chase and cellular immunology (Founders of our knowledge). International Journal of Tuberculosis and Lung Disease 14, 397–398.Google Scholar
David, P. H., Hudson, D. E., Hadley, T. J., Klotz, F. W. and Miller, L. H. (1985). Immunization of monkeys with a 140 kilodalton merozoite surface protein of Plasmodium knowlesi malaria: appearance of alternate forms of this protein. Journal of Immunology 134, 4146–4152.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, 297–309.Google ScholarPubMed
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 kilodalton merozoite antigen. Parasite Immunology 10, 535–552.CrossRefGoogle 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, 475–481.Google Scholar
De Zeeuw, R. A., Wjsbeek, J., Rock, R. C. and McCormick, G. J. (1972). Composition of phospholipids in Plasmodium knowlesi membranes and in host rhesus erythrocyte membranes. Proceedings of the Helminthological in Society of Washington 39 (Special Issue), 412–418.Google Scholar
Dunn, M. J. (1969). Alterations of red blood cell metabolism in simian-malaria: evidence for abnormalities of non-parasitised cells. Military Medicine (Special Issue) 134, 1100–1105.Google Scholar
Dvorak, J. A., Miller, L. H., Whitehouse, W. C. and Shiroishi, T. (1975). Invasion of erythrocytes by malaria merozoites. Science 187, 748–750.Google Scholar
Edeson, J. F. B. and Davey, D. G. (1953). Isolation of a virulent strain of Plasmodium knowlesi Sinton and Mulligan 1932. Transactions of the Royal Society of Tropical Medicine and Hygiene 47, 259–260.Google Scholar
Ellis, J., Ozaki, L. S., Gwadz, R. W., Cochrane, A. H., Nussenzweig, V., Nussenzweig, R. S. and Godson, G. N. (1983). Cloning and expression in E. coli of the malarial sporozoite surface antigen gene from Plasmodium knowlesi . Nature 302, 536–538.Google Scholar
Franchini, G. (1927). Su di un plasmodio pigmentato di una scimmmia. Arch Ital Sci Med Colon Parassit 8, 187–190 (not seen; cited in Garnham 1966).Google Scholar
Freund, J., Thomson, K. J., Sommer, H. E., Walter, A. W. and Pisani, T. M. (1948). Immunisation of monkeys against malaria by means of killed parasites with adjuvants. American Journal of Tropical Medicine 28, 1–22.Google Scholar
Garnham, P. C. C. (1966). Malaria Parasites and Other Haemosporidia. Blackwell Scientific Publications, Oxford.Google Scholar
Geiman, Q. M., Anfinsen, C. B., McKee, R. W., Ormsbee, R. A. and Ball, E. G. (1946). Studies on malarial parasites : vii. Methods and techniques for cultivation. Journal of Experimental Medicine 84, 583–606. Google Scholar
Geiman, Q. M., Siddiqui, W. A. and Schnell, J. V. (1966). In vitro studies on erythrocytic stages of plasmodia. Medium improvement and results with seven species of malarial parasites. Military Medicine (Supplement) 131, 1015–1025.Google Scholar
Gwadz, R. W. and Green, I. (1978). Malaria immunization in rhesus monkeys. A vaccine effective against both the sexual and asexual stages of Plasmodium knowlesi . Journal of Experimental Medicine 148, 1311–1323.Google Scholar
Gwadz, R. W., Cochrane, A. H., Nussenzweig, V. and Nussenzweig, R. S. (1979). Preliminary studies on vaccination of rhesus monkeys with irradiated sporozoites of Plasmodium knowlesi and characterization of surface antigens of these parasites. Bulletin of the World Health Organisation 57 (Suppl. 1), 165–173.Google Scholar
Hadley, T., Aikawa, M. and Miller, L. H. (1983). Plasmodium knowlesi: studies on invasion of rhesus erythrocytes by merozoites in the presence of protease inhibitors. Experimental Parasitology 55, 306–311.Google Scholar
Haynes, J. D., Diggs, C. L., Hines, F. A. and Desjardins, R. E. (1976). Culture of human malaria parasites Plasmodium falciparum . Nature 263, 767–769.Google Scholar
Horuk, R., Chitnis, C. E., Darbonne, W. C., Colby, T. J., Rybicki, A., Hadley, T. J. and Miller, L. H. (1993). A receptor for the malarial parasite Plasmodium vivax: the erythrocyte chemokine receptor. Science. 261, 1182–1184.CrossRefGoogle ScholarPubMed
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, 4129–4133.Google Scholar
Hsieh, H. C. (1960). Malaria parasites of the Taiwan monkey. Formosan Science 14, 477–487 (not seen; cited in Coatneyi et al. 1971).Google Scholar
Jiram, A. I., Vythilingam, I., NoorAzian, Y. M., Yusof, Y. M., Azahari, A. H. and Fong, M. Y. (2012). Entomologic investigation of Plasmodium knowlesi vectors in Kuala Lipis, Pahang, Malaysia. Malaria Journal 11, 213.Google Scholar
Jolly, A. M. D., Lavergne, X. and Tanguy, Y. (1937). Etude experimentale du Plasmodium knowlesi chez le singe et chez l'homme. Annales de l'Institut Pasteur 58, 297–325 (not seen; cited in Coatney et al 1971).Google Scholar
Knisely, M. H., Stratman-Thomas, W. K. and Eliot, T. S. (1941). Observation on circulating blood in the small vessels of internal organs in living Macacus rhesus infected with malarial parasites. Anatomical Record 79, 90.Google Scholar
Knowles, P. and Das Gupta, B. M. (1932). A study of monkey malaria and its experimental transmission to man. Indian Medical Gazette LXVII, 301–320.Google Scholar
Korir, C. C. and Galinski, M. R. (2006). Proteomic studies of Plasmodium knowlesi SICA variant antigens demonstrate their relationship with P. falciparum EMP1. Infection Genetics and Evolution 6, 75–79.Google Scholar
Lambrecht, F. L., Dunn, F. L. and Eyles, D. E. (1961). Isolation of Plasmodium knowlesi from Philippine macaques. Nature 191, 1117–1118.Google Scholar
Langhorne, J., Butcher, G. A., Mitchell, G. H. and Cohen, S. (1979). Preliminary investigations on the role of the spleen in immunity to Plasmodium knowlesi malaria. In Role of the Spleen in the Immunology of Parasitic Diseases. Tropical Disease Research Series 1, pp. 205–225. UNDP/WORLD BANK/WHO, Schwabe, Basel.Google Scholar
Maegraith, B. G., Devakul, K. and Lighthead, C. S. (1959). The terminal stages of Plasmodium knowlesi infection in Macaca mulatta . Annals of Tropical Medicine and Parasitology 53, 369–379.Google Scholar
Mason, S. J., Miller, L. H., Shiroishi, T., Dvorak, J. A. and McGinniss, M. H. (1977). The Duffy blood group determinants: their role in the susceptibility of human and animal erythrocytes to Plasmodium knowlesi malaria. British Journal of Haematology 36, 327–335.Google Scholar
McKee, R. W. and Geiman, Q. M. (1946). Studies on malarial parasites V. Effects of ascorbic acid on malaria (Plasmodium knowlesi) in monkeys. Proceedings of the Society for Experimental Biology and Medicine 63, 313–315.Google Scholar
Mclaren, D. J., Bannister, L. H., Trigg, P. I. and Butcher, G. A. (1977). A freeze-fracture study on the parasite-erythrocyte interrelationship in Plasmodium knowlesi infections. Bulletin of the World health Organisation 55, 199–203.Google Scholar
Menon, T. B. (1939). The visceral lesions in simian malaria with special reference to the splenic reaction. Transactions of the Royal Society of Tropical Medicine and Hygiene 32, 481–495.CrossRefGoogle Scholar
Miller, L. H. (1977). Hypothesis on the mechanism of erythrocyte invasion by malaria merozoites. Bulletin of the World Health Organisation 55, 157–62Google Scholar
Miller, L. H., Dvorak, J. A., Shiroishi, T. and Durocher, J. R. (1973). Influence of erythrocyte membrane components on malaria merozoite invasion. Journal of Experimental Medicine 138, 1597–1601.Google Scholar
Miller, L. H., Mason, S. J., Dvorak, J. A., McGinniss, M. H. and Rothman, I. K. (1975). Erythrocyte receptors for (Plasmodium knowlesi) malaria: duffy blood group determinants. Science 189, 561–563.Google Scholar
Miller, L. H., Powers, K. G. and Shiroishi, T. (1977). Plasmodium knowlesi: functional immunity and antimerozoite antibodies in rhesus monkeys after repeated infection. Experimental Parasitology 41, 105–111.Google Scholar
Miller, L. H., Aikawa, M., Johnson, J. G. and Shiroishi, T. (1979). Interaction between cytochalasin B-treated malarial parasites and erythrocytes. Attachment and junction formation. Journal of Experimental Medicine 149, 172–184.Google Scholar
Miller, L. H., Hudson, D., Rener, J., Taylor, D., Hadley, T. J. and Zilberstein, D. (1983). A monoclonal antibody to rhesus erythrocyte band 3 inhibits invasion by malaria (Plasmodium knowlesi) merozoites. Journal of Clinical Investigation 134, 4146–4152.Google Scholar
Miller, L. H., David, P. H., Hudson, D. E., Hadley, T. J., Richards, R. L. and Aikawa, M. (1984). Monoclonal antibodies to a 140,000-m.w. protein on Plasmodium knowlesi merozoites inhibit their invasion of rhesus erythrocytes. Journal of Immunology 132, 438–442.Google Scholar
Millet, P., Fisk, T. L., Collins, W. E., Broderson, J. R. and Nguyen-Dinh, P. (1988). Cultivation of exoerythrocytic stages of Plasmodium cynomolgi, P. knowlesi, P. coatneyi and P. inui in Macaca mulatta hepatocytes. American Journal of Tropical Medicine and Hygiene 39, 529–534.Google Scholar
Mitchell, G. H. (1975). Experimental studies on acquired malarial immunity. Ph.D. thesis. University of London, London.Google Scholar
Mitchell, G. H. (1977). A review of merozoite vaccination against Plasmodium knowlesi malaria. Transactions of the Royal Society of Tropical Medicine and Hygiene 71, 281–282.Google Scholar
Mitchell, G. H., Butcher, G. A. and Cohen, S. (1973). Isolation of blood-stage merozoites from Plasmodium knowlesi malaria. International Journal of Parasitology 3, 443–445.Google Scholar
Mitchell, G. H., Butcher, G. A., Voller, A. and Cohen, S. (1976). The effect of human immune IgG on the in vitro development of Plasmodium falciparum . Parasitology 72, 149–162.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, 276–279.Google Scholar
Mitchell, G. H., Richards, W. H. G., Voller, A., Dietrich, F. M. and Dukor, P. (1979). Nor-MDP, saponin, corynebacteria, and pertussis organisms as immunological adjuvants in experimental malaria vaccination of macaques. Bulletin of the world Health Organisation 57 (Suppl. 1), 189–197.Google Scholar
Mitchell, G. H., Butcher, G. A., Cohen, S. (1975). Merozoite vaccination against Plasmodium knowlesi malaria. Immunology 29, 397–407.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 Scince of the United States of America 110, 531–536.Google Scholar
Mulligan, H. W. and Sinton, J. A. (1933). Superinfection with various strains of monkey malaria. Record of the Malaria Survey, India 3, 529–568.Google Scholar
Mulligan, H. W., Sommerville, T. and Swaminath, C. S. (1940). Cellular and humoral agencies in defence against malaria. Journal of the Malaria Institute of India 3, 563–579.Google Scholar
Mun, Y. F., Ahmed, M. A., Wong, S. S., Yee, L. L. and Sitam, F. (2015). Genetic diversity and natural selection of the Plasmodium knowlesi circumsporozoite protein nonrepeat regions. PLoS ONE 10, e0137734.Google Scholar
Napier, L. E. and Campbell, H. G. M. (1932). Observations on a plasmodium infection which causes haemoglobinuria in certain species of monkey. Indian Medical Gazette 67, 151–160.Google Scholar
Nillni, E. A., Schmidt-Ullrich, R., Mikkelsen, R. B. and Wallach, D. F. (1985). Extracellular development of Plasmodium knowlesi erythrocytic stages in an artificial intracellular medium. Molecular and Biochemical Parasitology 17, 219–237.Google Scholar
Pain, A., Böhme, 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. et al. (2008). The genome of the simian and human malaria parasite Plasmodium knowlesi . Nature 455, 799–803.Google Scholar
Phillips, R. S. (1970). Plasmodium berghei: passive transfer of immunity by antisera and cells. Experimental Parasitology 27, 479–495.CrossRefGoogle ScholarPubMed
Phillips, R. S., Wolstencroft, R. A., Brown, I. N., Brown, I. N. and Dumonde, D. C. (1970). Immunity to malaria III Posssible occurrence of a cell-mediated immunity to Plasmodium knowlesi in chronically infected and Freund's Adjuvant-sensitised monkeys. Experimental Parasitology 28, 339–355.CrossRefGoogle Scholar
Pinheiro, M. M., Ahmed, M. A., Millar, S. B., Sanderson, T., Otto, T. D., Lu, W. C., Krishna, S., Rayner, J. C. and Cox-Singh, J. (2015). Plasmodium knowlesi genome sequences from clinical isolates reveal extensive genomic dimorphism. PLoS ONE 10, e0121303.Google Scholar
Porter, R. (1997). The Greatest Benefit to Mankind. Fontana Press, London, pp. 445–448.Google Scholar
Russell, P. F. (1955). Man's Mastery of Malaria. OUP, London, p. 1.Google Scholar
Schenkel, R. H., Simpson, G. L. and Silverman, P. H. (1973). Vaccination of rhesus monkeys (Macaca mulatta) against Plasmodium knowlesi by the use of non-viable antigen. Bulletin of the World Health Organisation 48, 597–604.Google Scholar
Sharma, S., Svec, P., Mitchell, G. H. and Godson, G. N. (1985). Diversity of circumsporozoite antigen genes from two strains of the malarial parasite Plasmodium knowlesi . Science 229, 779–782.Google Scholar
Siddiqui, W. A. and Schnell, J. V. (1972). In vitro and in vivo studies with Plasmodium falciparum and Plasmodium knowlesi . Proceedings of the Helminthological in Society of Washington 39 (Special- Issue), 204–210.Google Scholar
Siddiqui, W. A., Schnell, J. V. and Geiman, Q. M. (1969). Nutritional requirements for in vitro cultivation of a simian malarial parasite, Plasmodium knowlesi . Military Medicine 134 (Special Issue), 929–938.Google Scholar
Sinton, J. A. and Mulligan, H. W. (1932). A critical review of the literature relating to the identification of the malarial parasites recorded from monkeys of the families Cercopithecidae and Colobidae. Records of the Malaria Survey of India 3, 357–380.Google Scholar
Stocker, R., Hunt, N. H., Weidermann, M. J. and Clark, I. A. (1986). Protection of vitamin E from oxidation by increased by ascorbic acid content within Plasmodium vinckei-infected erythrocytes. Biochemica Biophysica Acta 876, 294–299.Google Scholar
Taliaferro, W. H. (1949). Immunity to the malarial infections. In Malariology (ed. Boyd, M. F.), pp. 935–965. Saunders, Philadelphia.Google Scholar
Taliaferro, W. H. and Taliaferro, L. G. (1944). The effect of immunity on the asexual reproduction of Plasmodium brasilianum . Journal of Infectious Diseases 75, 1–32.Google Scholar
Tan, C. H., Vythilingam, I., Matusop, A., Chan, S. T. and Singh, B. (2008). Bionomics of Anopheles latens in Kapit, Sarawak, Malaysian Borneo in relation to the transmission of zoonotic simian malaria parasite Plasmodium knowlesi . Malaria Journal 7, 52.Google Scholar
Targett, G. A. T. and Fulton, J. D. (1965). Immunisation of rhesus monkeys against Plasmodium knowlesi . Experimental Parasitology 17, 180–193.Google Scholar
Trager, W. and Jensen, J. B. (1976). Human malaria parasites in continuous culture. Science 193, 673–675.CrossRefGoogle ScholarPubMed
Trigg, P. I. (1969). The use of proprietary tissue-culture media for the cultivation in vitro of the erythrocytic stages of Plasmodium knowlesi . Parasitology 59, 925–935.Google Scholar
Trigg, P. I. (1985). Recent advances in malaria parasite cultivation and their application to studies on host-parasite relationships: a review. Bulletin of the World Health Organisation 63, 387–398.Google Scholar
Trigg, P. I. and Shakespeare, P. G. (1976). The effect of incubation in vitro on the susceptibility of monkey erythrocytes to invasion by Plasmodium knowlesi . Parasitology 73, 149–160.Google Scholar
van Rooyen, C. E. and Pile, G. R. (1935). Observations on infection by Plasmodium knowlesi (ape malaria) in the treatment of general paralysis of the insane. British Medical Journal 2, 662–666.CrossRefGoogle ScholarPubMed
Voller, A. and Rossan, R. N. (1969 a). Immunological studies with simian malarias. II Heterologous immunity in the “cynomolgi” group. Transactions of the Royal Society of Tropical Medicine and Hygiene 63, 57–63.Google Scholar
Voller, A. and Rossan, R. N. (1969 b). Immunological studies on simian malaria.III Immunity to challenge and antigenic variation in P. knowlesi . Transactions of the Royal Society of Tropical Medicine and Hygiene 63, 507–523.Google Scholar
Wharton, R. H. and Eyles, D. E. (1961). Anopheles hackeri, a vector of Plasmodium knowlesi in Malaya. Science 134, 279–280.Google Scholar
Wheatley, B. P. (1980). Malaria as a possible selective factor in the speciation of macaques. Journal of Mammology 61, 304–307.Google Scholar
Wickham, J. M., Dennis, E. D. and Mitchell, G. H. (1980). Long term cultivation of a simian malaria parasite (Plasmodium knowlesi) in a semi-automated apparatus. Transactions of the Royal Society of Tropical Medicine and Hygiene 74, 789–792.Google Scholar
Wong, M. L., Chua, T. H., Leong, C. S., Khaw, L. T., Fornace, K., Wan-Sulaiman, W. Y., William, T., Drakeley, C., Ferguson, H. M. and Vythilingam, I. (2015). Seasonal and spatial dynamics of the primary vector of Plasmodium knowlesi within a major transmission focus in Sabah, Malaysia. PLoS Neglected Tropical Diseases 9, e0004135.Google Scholar
World Health Organisation (1975). Developments in Malaria Immunology. Technical Report Series, No 579, WHO, Geneva.Google Scholar