Author:
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Jaffe RI, Lowell GH, Gordon DM, 1990. Differences in susceptibility among mouse strains to infection with Plasmodium berghei (ANKA clone) sporozoites and its relationship to protection by gamma-irradiated sporozoites. Am J Trop Med Hyg 42: 309–313.
-
2.
Chattopadhyay R, Conteh S, Li M, James ER, Epstein JE, Hoffman SL, 2009. The effects of radiation on the safety and protective efficacy of an attenuated Plasmodium yoelii sporozoite malaria vaccine. Vaccine 27: 3675–3680.
-
3.
Chatterjee S, Perignon JL, Van Marck E, Druilhe P, 2006. How reliable are models for malaria vaccine development? Lessons from irradiated sporozoite immunizations. J Postgrad Med 52: 321–324.
-
4.
Bray RS, 1976. Vaccination against Plasmodium falciparum: a negative result. Trans R Soc Trop Med Hyg 70: 258.
-
5.
Edelman R, Hoffman SL, Davis JR, Beier M, Sztein MB, Losonsky G, Herrington DA, Eddy HA, Hollingdale MR, Gordon DM, Clyde DF, 1993. Long-term persistence of sterile immunity in a volunteer immunized with X-irradiated Plasmodium falciparum sporozoites. J Infect Dis 168: 1066–1070.
-
6.
Herrington D, Davis J, Nardin E, Beier M, Cortese J, Eddy H, Losonsky G, Hollingdale M, Sztein M, Levine M, Nussenzweig M, Clyde RS, Edelman DR, 1991. Successful immunization of humans with irradiated malaria sporozoites: humoral and cellular responses of the protected individuals. Am J Trop Med Hyg 45: 539–547.
-
7.
Chatterjee S, Ngonseu E, Van Overmeir C, Correwyn A, Druilhe P, Wery M, 2001. Rodent malaria in the natural host–irradiated sporozoites of Plasmodium berghei induce liver-stage specific immune responses in the natural host Grammomys surdaster and protect immunized Grammomys against P. berghei sporozoite challenge. Afr J Med Med Sci 30 (Suppl): 25–33.
-
8.
Lecompte E, Granjon L, Peterhans JK, Denys C, 2002. Cytochrome b-based phylogeny of the Praomys group (Rodentia, Murinae): a new African radiation? C R Biol 325: 827–840.
-
9.
LUM Center. Plasmodium berghei: Life Histories and Stabilates (Deep-Frozen Samples) of Isolates, Lines, and Clones Maintained at the University of Edinburgh. Available at: https://www.lumc.nl/sub/1040/att/811071156182556/811130228382556/908051142222557.pdf. Accessed November 8, 2016.
-
10.
Killick-Kendrick R, 1974. Parasitic protozoa of the blood of rodents: a revision of Plasmodium berghei. Parasitology 69: 225–237.
-
11.
Schwan TG, Anderson JM, Lopez JE, Fischer RJ, Raffel SJ, McCoy BN, Safronetz D, Sogoba N, Maiga O, Traore SF, 2012. Endemic foci of the tick-borne relapsing fever spirochete Borrelia crocidurae in Mali, west Africa, and the potential for human infection. PLoS Negl Trop Dis 6: e1924.
-
12.
Dieterlen F, 2013. Genus Grammomys thicket rats. Happold DCD, ed. Mammals of Africa, Vol. III. London, United Kingdom: Bloomsbury Publishing, 404–405.
-
13.
Happold DCD, 2013. Grammomys dolichurus woodland thicket rat (Common Grammomys). Happold DCD, ed. Mammals of Africa, Vol. III. London, United Kingdom: Bloomsbury Publishing, 410–411.
-
14.
Matuschewski K, Hafalla JC, Borrmann S, Friesen J, 2011. Arrested Plasmodium liver stages as experimental anti-malaria vaccines. Hum Vaccin 7 (Suppl): 16–21.
-
15.
Siu E, Ploss A, 2015. Modeling malaria in humanized mice: opportunities and challenges. Ann N Y Acad Sci 1342: 29–36.
-
16.
Waters H, 2011. Better animal models needed for malaria vaccine development, experts say. Available at: http://blogs.nature.com/spoonful/2011/10/better_animal_models_needed_fo_1.htm. Accessed.
-
17.
Perkins SL, 2008. Molecular systematics of the three mitochondrial protein-coding genes of malaria parasites: corroborative and new evidence for the origins of human malaria. Mitochondrial DNA 19: 471–478.
-
18.
De Niz M, Ullrich AK, Heiber A, Blancke Soares A, Pick C, Lyck R, Keller D, Kaiser G, Prado M, Flemming S, Del Portillo H, Janse CJ, Heussler V, Spielmann T, 2016. The machinery underlying malaria parasite virulence is conserved between rodent and human malaria parasites. Nat Commun 7: 11659.
-
19.
Larremore DB, Sundararaman SA, Liu W, Proto WR, Clauset A, Loy DE, Speede S, Plenderleith LJ, Sharp PM, Hahn BH, Rayner JC, Buckee CO, 2015. Ape parasite origins of human malaria virulence genes. Nat Commun 6: 8368.
-
20.
Perkins SL, Sarkar IN, Carter R, 2007. The phylogeny of rodent malaria parasites: simultaneous analysis across three genomes. Infect Genet Evol 7: 74–83.
-
21.
Perkins SL, Schall JJ, 2002. A molecular phylogeny of malarial parasites recovered from cytochrome b gene sequences. J Parasitol 88: 972–978.
-
22.
Yoeli M, Alger N, Most H, 1963. Tree rat, Thamnomys surdaster surdaster, in laboratory research. Science 142: 1585–1586.
-
23.
Yoeli M, Most H, 1964. A study of Plasmodium berghei in Thamnomys surdaster, and in other experimental hosts. Am J Trop Med Hyg 13: 659–663.
-
24.
Yoeli M, 1974. Slow maturing primary exo-erythrocytic schizonts of Plasmodium berghei in an experimentally infected tree-rat (Thamnomys surdaster). Trans R Soc Trop Med Hyg 68: 302–305.
-
25.
Buscher P, Bin Shamamba SK, Ngoyi DM, Pyana P, Baelmans R, Magnus E, Van Overmeir C, 2005. Susceptibility of Grammomys surdaster thicket rats to Trypanosoma brucei gambiense infection. Trop Med Int Health 10: 850–855.
-
26.
Musser GG, Carlteon MD, 2005. Superfamily Muroidea. Wilson D, Reeder D, eds. Mammal Species of the World: A Taxonomic and Geographic Reference, 3rd edition. Baltimore, MD: Johns Hopkins University Press, 894–1531.
-
27.
Hoffman SL, Goh LM, Luke TC, Schneider I, Le TP, Doolan DL, Sacci J, de la Vega P, Dowler M, Paul C, Gordon DM, Stoute JA, Church LW, Sedegah M, Heppner DG, Ballou WR, Richie TL, 2002. Protection of humans against malaria by immunization with radiation-attenuated Plasmodium falciparum sporozoites. J Infect Dis 185: 1155–1164.
-
28.
Seder RA, Chang LJ, Enama ME, Zephir KL, Sarwar UN, Gordon IJ, Holman LA, James ER, Billingsley PF, Gunasekera A, Richman A, Chakravarty S, Manoj A, Velmurugan S, Li M, Ruben AJ, Li T, Eappen AG, Stafford RE, Plummer SH, Hendel CS, Novik L, Costner PJ, Mendoza FH, Saunders JG, Nason MC, Richardson JH, Murphy J, Davidson SA, Richie TL, Sedegah M, Sutamihardja A, Fahle GA, Lyke KE, Laurens MB, Roederer M, Tewari K, Epstein JE, Sim BK, Ledgerwood JE, Graham BS, Hoffman SL, the VRC 312 Study Team, 2013. Protection against malaria by intravenous immunization with a nonreplicating sporozoite vaccine. Science 341: 1359–1365.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 71 | 71 | 16 |
| Full Text Views | 365 | 151 | 1 |
| PDF Downloads | 114 | 38 | 0 |
Grammomys surdaster, the Natural Host for Plasmodium berghei Parasites, as a Model to Study Whole-Organism Vaccines Against Malaria
Solomon Conteh
Solomon Conteh
Laboratory of Malaria Immunology and Vaccinology (LMIV), National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Rockville, Maryland.
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Charles Anderson
Charles Anderson
Laboratory of Malaria Immunology and Vaccinology (LMIV), National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Rockville, Maryland.
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Lynn Lambert
Lynn Lambert
Laboratory of Malaria Immunology and Vaccinology (LMIV), National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Rockville, Maryland.
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Sachy Orr-Gonzalez
Sachy Orr-Gonzalez
Laboratory of Malaria Immunology and Vaccinology (LMIV), National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Rockville, Maryland.
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Jessica Herrod
Jessica Herrod
Laboratory of Malaria Immunology and Vaccinology (LMIV), National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Rockville, Maryland.
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Yvette L. Robbins
Yvette L. Robbins
Laboratory of Malaria Immunology and Vaccinology (LMIV), National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Rockville, Maryland.
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Dariyen Carter
Dariyen Carter
Laboratory of Malaria Immunology and Vaccinology (LMIV), National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Rockville, Maryland.
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Stomy Bin Shamamba Karhemere
Stomy Bin Shamamba Karhemere
Department of Parasitology, Institut National de Recherche Biomédicale (INRB), Kinshasa, Democratic Republic of Congo.
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Pati Pyana
Pati Pyana
Department of Parasitology, Institut National de Recherche Biomédicale (INRB), Kinshasa, Democratic Republic of Congo.
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Philippe Büscher
Philippe Büscher
Department of Biomedical Sciences, Unit of Parasite Diagnostics, Institute of Tropical Medicine, Antwerp, Belgium.
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Patrick E. Duffy
Patrick E. Duffy
Laboratory of Malaria Immunology and Vaccinology (LMIV), National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Rockville, Maryland.
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Inbred mice are commonly used to test candidate malaria vaccines, but have been unreliable for predicting efficacy in humans. To establish a more rigorous animal model, we acquired African woodland thicket rats of the genus Grammomys, the natural hosts for Plasmodium berghei. Thicket rats were acquired and identified as Grammomys surdaster by skull and teeth measurements and mitochondrial DNA genotyping. Herein, we demonstrate that thicket rats are highly susceptible to infection by P. berghei, and moderately susceptible to Plasmodium yoelii and Plasmodium chabaudi: 1–2 infected mosquito bites or 25–100 sporozoites administered by intravenous injection consistently resulted in patent parasitemia with P. berghei, and resulted in patent parasitemia with P. yoelii and P. chabaudi strains for at least 50% of animals. We then assessed efficacy of whole-organism vaccines to induce sterile immunity, and compared the thicket rat model to conventional mouse models. Using P. berghei ANKA radiation-attenuated sporozoites, and P. berghei ANKA and P. yoelii chemoprophylaxis vaccination approaches, we found that standard doses of vaccine sufficient to protect laboratory mice for a long duration against malaria challenge, are insufficient to protect thicket rats, which require higher doses of vaccine to achieve even short-term sterile immunity. Thicket rats may offer a more stringent and pertinent model for evaluating whole-organism vaccines.
Author Notes
Financial support: This research was supported and funded by the Intramural Research Program of the National Institute for Allergy and Infectious Disease of the National Institutes of Health.
Authors' addresses: Solomon Conteh, Charles Anderson, Lynn Lambert, Sachy Orr-Gonzalez, Jessica Herrod, Yvette L. Robbins, Dariyen Carter, and Patrick E. Duffy, Laboratory of Malaria Immunology and Vaccinology (LMIV), National Institute of Allergy and Infectious Diseases (NIAID), National Institutes of Health (NIH), Rockville, MD, E-mails: solomon.conteh@nih.gov, charles.anderson@nih.gov, lelambert@niaid.nih.gov, satos@niaid.nih.gov, herrodja@gmail.com, yvette.robbins@nih.gov, carterd4@niaid.nih.gov, and patrick.duffy@nih.gov. Stomy Bin Shamamba Karhemere and Pati Pyana, Department of Parasitology, Institut National de Recherche Biomédicale (INRB), Kinshasa, Democratic Republic of Congo, E-mails: stomy_karhem@yahoo.fr and ppyana@yahoo.fr. Philippe Büscher, Department of Biomedical Sciences, Prince Leopold Institute of Tropical Medicine, Antwerp, Belgium, E-mail: pbuscher@itg.be.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Jaffe RI, Lowell GH, Gordon DM, 1990. Differences in susceptibility among mouse strains to infection with Plasmodium berghei (ANKA clone) sporozoites and its relationship to protection by gamma-irradiated sporozoites. Am J Trop Med Hyg 42: 309–313.
-
2.
Chattopadhyay R, Conteh S, Li M, James ER, Epstein JE, Hoffman SL, 2009. The effects of radiation on the safety and protective efficacy of an attenuated Plasmodium yoelii sporozoite malaria vaccine. Vaccine 27: 3675–3680.
-
3.
Chatterjee S, Perignon JL, Van Marck E, Druilhe P, 2006. How reliable are models for malaria vaccine development? Lessons from irradiated sporozoite immunizations. J Postgrad Med 52: 321–324.
-
4.
Bray RS, 1976. Vaccination against Plasmodium falciparum: a negative result. Trans R Soc Trop Med Hyg 70: 258.
-
5.
Edelman R, Hoffman SL, Davis JR, Beier M, Sztein MB, Losonsky G, Herrington DA, Eddy HA, Hollingdale MR, Gordon DM, Clyde DF, 1993. Long-term persistence of sterile immunity in a volunteer immunized with X-irradiated Plasmodium falciparum sporozoites. J Infect Dis 168: 1066–1070.
-
6.
Herrington D, Davis J, Nardin E, Beier M, Cortese J, Eddy H, Losonsky G, Hollingdale M, Sztein M, Levine M, Nussenzweig M, Clyde RS, Edelman DR, 1991. Successful immunization of humans with irradiated malaria sporozoites: humoral and cellular responses of the protected individuals. Am J Trop Med Hyg 45: 539–547.
-
7.
Chatterjee S, Ngonseu E, Van Overmeir C, Correwyn A, Druilhe P, Wery M, 2001. Rodent malaria in the natural host–irradiated sporozoites of Plasmodium berghei induce liver-stage specific immune responses in the natural host Grammomys surdaster and protect immunized Grammomys against P. berghei sporozoite challenge. Afr J Med Med Sci 30 (Suppl): 25–33.
-
8.
Lecompte E, Granjon L, Peterhans JK, Denys C, 2002. Cytochrome b-based phylogeny of the Praomys group (Rodentia, Murinae): a new African radiation? C R Biol 325: 827–840.
-
9.
LUM Center. Plasmodium berghei: Life Histories and Stabilates (Deep-Frozen Samples) of Isolates, Lines, and Clones Maintained at the University of Edinburgh. Available at: https://www.lumc.nl/sub/1040/att/811071156182556/811130228382556/908051142222557.pdf. Accessed November 8, 2016.
-
10.
Killick-Kendrick R, 1974. Parasitic protozoa of the blood of rodents: a revision of Plasmodium berghei. Parasitology 69: 225–237.
-
11.
Schwan TG, Anderson JM, Lopez JE, Fischer RJ, Raffel SJ, McCoy BN, Safronetz D, Sogoba N, Maiga O, Traore SF, 2012. Endemic foci of the tick-borne relapsing fever spirochete Borrelia crocidurae in Mali, west Africa, and the potential for human infection. PLoS Negl Trop Dis 6: e1924.
-
12.
Dieterlen F, 2013. Genus Grammomys thicket rats. Happold DCD, ed. Mammals of Africa, Vol. III. London, United Kingdom: Bloomsbury Publishing, 404–405.
-
13.
Happold DCD, 2013. Grammomys dolichurus woodland thicket rat (Common Grammomys). Happold DCD, ed. Mammals of Africa, Vol. III. London, United Kingdom: Bloomsbury Publishing, 410–411.
-
14.
Matuschewski K, Hafalla JC, Borrmann S, Friesen J, 2011. Arrested Plasmodium liver stages as experimental anti-malaria vaccines. Hum Vaccin 7 (Suppl): 16–21.
-
15.
Siu E, Ploss A, 2015. Modeling malaria in humanized mice: opportunities and challenges. Ann N Y Acad Sci 1342: 29–36.
-
16.
Waters H, 2011. Better animal models needed for malaria vaccine development, experts say. Available at: http://blogs.nature.com/spoonful/2011/10/better_animal_models_needed_fo_1.htm. Accessed.
-
17.
Perkins SL, 2008. Molecular systematics of the three mitochondrial protein-coding genes of malaria parasites: corroborative and new evidence for the origins of human malaria. Mitochondrial DNA 19: 471–478.
-
18.
De Niz M, Ullrich AK, Heiber A, Blancke Soares A, Pick C, Lyck R, Keller D, Kaiser G, Prado M, Flemming S, Del Portillo H, Janse CJ, Heussler V, Spielmann T, 2016. The machinery underlying malaria parasite virulence is conserved between rodent and human malaria parasites. Nat Commun 7: 11659.
-
19.
Larremore DB, Sundararaman SA, Liu W, Proto WR, Clauset A, Loy DE, Speede S, Plenderleith LJ, Sharp PM, Hahn BH, Rayner JC, Buckee CO, 2015. Ape parasite origins of human malaria virulence genes. Nat Commun 6: 8368.
-
20.
Perkins SL, Sarkar IN, Carter R, 2007. The phylogeny of rodent malaria parasites: simultaneous analysis across three genomes. Infect Genet Evol 7: 74–83.
-
21.
Perkins SL, Schall JJ, 2002. A molecular phylogeny of malarial parasites recovered from cytochrome b gene sequences. J Parasitol 88: 972–978.
-
22.
Yoeli M, Alger N, Most H, 1963. Tree rat, Thamnomys surdaster surdaster, in laboratory research. Science 142: 1585–1586.
-
23.
Yoeli M, Most H, 1964. A study of Plasmodium berghei in Thamnomys surdaster, and in other experimental hosts. Am J Trop Med Hyg 13: 659–663.
-
24.
Yoeli M, 1974. Slow maturing primary exo-erythrocytic schizonts of Plasmodium berghei in an experimentally infected tree-rat (Thamnomys surdaster). Trans R Soc Trop Med Hyg 68: 302–305.
-
25.
Buscher P, Bin Shamamba SK, Ngoyi DM, Pyana P, Baelmans R, Magnus E, Van Overmeir C, 2005. Susceptibility of Grammomys surdaster thicket rats to Trypanosoma brucei gambiense infection. Trop Med Int Health 10: 850–855.
-
26.
Musser GG, Carlteon MD, 2005. Superfamily Muroidea. Wilson D, Reeder D, eds. Mammal Species of the World: A Taxonomic and Geographic Reference, 3rd edition. Baltimore, MD: Johns Hopkins University Press, 894–1531.
-
27.
Hoffman SL, Goh LM, Luke TC, Schneider I, Le TP, Doolan DL, Sacci J, de la Vega P, Dowler M, Paul C, Gordon DM, Stoute JA, Church LW, Sedegah M, Heppner DG, Ballou WR, Richie TL, 2002. Protection of humans against malaria by immunization with radiation-attenuated Plasmodium falciparum sporozoites. J Infect Dis 185: 1155–1164.
-
28.
Seder RA, Chang LJ, Enama ME, Zephir KL, Sarwar UN, Gordon IJ, Holman LA, James ER, Billingsley PF, Gunasekera A, Richman A, Chakravarty S, Manoj A, Velmurugan S, Li M, Ruben AJ, Li T, Eappen AG, Stafford RE, Plummer SH, Hendel CS, Novik L, Costner PJ, Mendoza FH, Saunders JG, Nason MC, Richardson JH, Murphy J, Davidson SA, Richie TL, Sedegah M, Sutamihardja A, Fahle GA, Lyke KE, Laurens MB, Roederer M, Tewari K, Epstein JE, Sim BK, Ledgerwood JE, Graham BS, Hoffman SL, the VRC 312 Study Team, 2013. Protection against malaria by intravenous immunization with a nonreplicating sporozoite vaccine. Science 341: 1359–1365.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 71 | 71 | 16 |
| Full Text Views | 365 | 151 | 1 |
| PDF Downloads | 114 | 38 | 0 |