Immunization of mice with live-attenuated late liver stage-arresting plasmodium yoelii parasites generates protective antibody responses to preerythrocytic stages of malaria

Infection and Immunity

Volumn 82, Issue 12, 2014, Pages 5143-5153

  Keitany, Gladys J ^a   Sack, Brandon ^a   Smithers, Hannah ^a,d   Chen, Lin ^a,b   Jang, Ihn K ^a   Sebastian, Leslie ^a   Gupta, Megha ^a   Sather, D Noah ^a   Vignali, Marissa ^a   Vaughan, Ashley M ^a   Kappe, Stefan H I ^a,c   Wang, Ruobing ^a,c  

^a SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

^b THIRD MILITARY MEDICAL UNIVERSITY   (China)

^c UNIVERSITY OF WASHINGTON   (United States)

^d SEATTLE CHILDREN S RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2; IMMUNOGLOBULIN G2B; IMMUNOGLOBULIN G2C; LIVE VACCINE; MALARIA VACCINE; PARASITE ANTIBODY; SPOROZOITE VACCINE; UNCLASSIFIED DRUG; IMMUNOGLOBULIN G; PROTOZOON ANTIBODY;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ARTICLE; CONTROLLED STUDY; FEMALE; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL; MALARIA CONTROL; MOSQUITO BITE; MOUSE; NONHUMAN; PARASITE IMMUNITY; PARASITE LOAD; PLASMODIUM YOELII INFECTION; SPOROZOITE; TREATMENT OUTCOME; VACCINATION; ANIMAL; BAGG ALBINO MOUSE; BLOOD; C57BL MOUSE; IMMUNIZATION; IMMUNOLOGY; MALARIA; PLASMODIUM YOELII; PROCEDURES;

ANIMAL EXPERIMENTATION; ANIMALS; ANTIBODIES, PROTOZOAN; FEMALE; IMMUNIZATION; IMMUNOGLOBULIN G; MALARIA; MALARIA VACCINES; MICE, INBRED BALB C; MICE, INBRED C57BL; PLASMODIUM YOELII; VACCINES, ATTENUATED;

EID: 84911420998     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.02320-14     Document Type: Article

References (55)

1. Murray CJ, Rosenfeld LC, Lim SS, Andrews KG, Foreman KJ, Haring D, Fullman N, Naghavi M, Lozano R, Lopez AD. 2012. Global malaria mortality between 1980 and 2010: a systematic analysis. Lancet 379:413-431. http://dx.doi.org/10.1016/S0140-6736(12)60034-8.
2. Epstein JE, Tewari K, Lyke KE, Sim BK, Billingsley PF, Laurens MB, Gunasekera A, Chakravarty S, James ER, Sedegah M, Richman A, Velmurugan S, Reyes S, Li M, Tucker K, Ahumada A, Ruben AJ, Li T, Stafford R, Eappen AG, Tamminga C, Bennett JW, Ockenhouse CF, Murphy JR, Komisar J, Thomas N, Loyevsky M, Birkett A, Plowe CV, Loucq C, Edelman R, Richie TL, Seder RA, Hoffman SL. 2011. Live attenuated malaria vaccine designed to protect through hepatic CD8(+)T cell immunity. Science 334:475-480. http://dx.doi.org/10.1126/science.1211548.
3. Doolan DL, Martinez-Alier N. 2006. Immune response to preerythrocytic stages of malaria parasites. Curr. Mol. Med. 6:169-185. http://dx.doi.org/10.2174/156652406776055249.
4. Cockburn IA, Amino R, Kelemen RK, Kuo SC, Tse SW, Radtke A, Mac-Daniel L, Ganusov VV, Zavala F, Menard R. 2013. In vivo imaging of CD8+ T cell-mediated elimination of malaria liver stages. Proc. Natl. Acad. Sci. U. S. A. 110:9090-9095. http://dx.doi.org/10.1073/pnas.1303858110.
5. Cockburn IA, Tse SW, Zavala F. 2014. CD8+ T cells eliminate liver stage Plasmodium parasites without detectable bystander effect. Infect. Immun. 82:1460-1464. http://dx.doi.org/10.1128/IAI.01500-13.
6. Schmidt NW, Butler NS, Badovinac VP, Harty JT. 2010. Extreme CD8 T cell requirements for anti-malarial liver-stage immunity following immunization with radiation attenuated sporozoites. PLoS Pathog. 6:e1000998. http://dx.doi.org/10.1371/journal.ppat.1000998.
7. Schofield L, Villaquiran J, Ferreira A, Schellekens H, Nussenzweig R, Nussenzweig V. 1987. Gamma interferon, CD8+ T cells and antibodies required for immunity to malaria sporozoites. Nature 330:664-666. http://dx.doi.org/10.1038/330664a0.
8. Weiss WR, Sedegah M, Beaudoin RL, Miller LH, Good MF. 1988. CD8+T cells (cytotoxic/suppressors) are required for protection in mice immunized with malaria sporozoites. Proc. Natl. Acad. Sci. U. S. A. 85: 573-576. http://dx.doi.org/10.1073/pnas.85.2.573.
9. Rodrigues M, Nussenzweig RS, Zavala F. 1993. The relative contribution of antibodies, CD4+ and CD8+T cells to sporozoite-induced protection against malaria. Immunology 80:1-5.
10. Jobe O, Lumsden J, Mueller AK, Williams J, Silva-Rivera H, Kappe SH, Schwenk RJ, Matuschewski K, Krzych U. 2007. Genetically attenuated Plasmodium berghei liver stages induce sterile protracted protection that is mediated by major histocompatibility complex class I-dependent interferongamma-producing CD8+ T cells. J. Infect. Dis. 196:599-607. http://dx.doi.org/10.1086/519743.
11. Teirlinck AC, McCall MB, Roestenberg M, Scholzen A, Woestenenk R, de Mast Q, van der Ven AJ, Hermsen CC, Luty AJ, Sauerwein RW. 2011. Longevity and composition of cellular immune responses following experimental Plasmodium falciparum malaria infection in humans. PLoS Pathog. 7:e1002389. http://dx.doi.org/10.1371/journal.ppat.1002389.
12. 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, VRC312 Study Team. 2013. Protection against malaria by intravenous immunization with a nonreplicating sporozoite vaccine. Science 341:1359-1365. http://dx.doi.org/10.1126/science.1241800.
13. Roestenberg M, McCall M, Hopman J, Wiersma J, Luty AJ, van Gemert GJ, van de Vegte-Bolmer M, van Schaijk B, Teelen K, Arens T, Spaarman L, de Mast Q, Roeffen W, Snounou G, Renia L, van der Ven A, Hermsen CC, Sauerwein R. 2009. Protection against a malaria challenge by sporozoite inoculation. N. Engl. J. Med. 361:468-477. http://dx.doi.org/10.1056/NEJMoa0805832.
14. Behet MC, Foquet L, van Gemert GJ, Bijker EM, Meuleman P, Leroux-Roels G, Hermsen CC, Scholzen A, Sauerwein RW. 2014. Sporozoite immunization of human volunteers under chemoprophylaxis induces functional antibodies against pre-erythrocytic stages of Plasmodium falciparum. Malar. J. 13:136. http://dx.doi.org/10.1186/1475-2875-13-136.
15. Alonso PL, Sacarlal J, Aponte JJ, Leach A, Macete E, Milman J, Mandomando I, Spiessens B, Guinovart C, Espasa M, Bassat Q, Aide P, Ofori-Anyinam O, Navia MM, Corachan S, Ceuppens M, Dubois MC, Demoitie MA, Dubovsky F, Menendez C, Tornieporth N, Ballou WR, Thompson R, Cohen J. 2004. Efficacy of the RTS,S/AS02A vaccine against Plasmodium falciparum infection and disease in young African children: randomised controlled trial. Lancet 364:1411-1420. http://dx.doi.org/10.1016/S0140-6736(04)17223-1.
16. White MT, Bejon P, Olotu A, Griffin JT, Riley EM, Kester KE, Ockenhouse CF, Ghani AC. 2013. The relationship between RTS,S vaccineinduced antibodies, CD4(+) T cell responses and protection against Plasmodium falciparum infection. PLoS One 8:e61395. http://dx.doi.org/10.1371/journal.pone.0061395.
17. Stewart MJ, Nawrot RJ, Schulman S, Vanderberg JP. 1986. Plasmodium berghei sporozoite invasion is blocked in vitro by sporozoite-immobilizing antibodies. Infect. Immun. 51:859-864.
18. Vanderberg JP, Frevert U. 2004. Intravital microscopy demonstrating antibody-mediated immobilisation of Plasmodium berghei sporozoites injected into skin by mosquitoes. Int. J. Parasitol. 34:991-996. http://dx.doi.org/10.1016/j.ijpara.2004.05.005.
19. Kebaier C, Voza T, Vanderberg J. 2009. Kinetics of mosquito-injected Plasmodium sporozoites in mice: fewer sporozoites are injected into sporozoite-immunized mice. PLoS Pathog. 5:e1000399. http://dx.doi.org/10.1371/journal.ppat.1000399.
20. Hollingdale MR, Zavala F, Nussenzweig RS, Nussenzweig V. 1982. Antibodies to the protective antigen of Plasmodium berghei sporozoites prevent entry into cultured cells. J. Immunol. 128:1929-1930.
21. Luo S, Liu D, Ye B, Shu H, Fu R. 1995. Effect of monoclonal antibodies on the entry and development of Plasmodium vivax sporozoite in cultured cells. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi 13:284-289.
22. Sack BK, Miller JL, Vaughan AM, Douglass A, Kaushansky A, Mikolajczak S, Coppi A, Gonzalez-Aseguinolaza G, Tsuji M, Zavala F, Sinnis P, Kappe SH. 2014. Model for in vivo assessment of humoral protection against malaria sporozoite challenge by passive transfer of monoclonal antibodies and immune serum. Infect. Immun. 82:808-817. http://dx.doi.org/10.1128/IAI.01249-13.
23. Yoshida N, Nussenzweig RS, Potocnjak P, Nussenzweig V, Aikawa M. 1980. Hybridoma produces protective antibodies directed against the sporozoite stage of malaria parasite. Science 207:71-73. http://dx.doi.org/10.1126/science.6985745.
24. Danforth HD, Aikawa M, Cochrane AH, Nussenzweig RS. 1980. Sporozoites of mammalian malaria: attachment to, interiorization and fate within macrophages. J. Protozool. 27:193-202. http://dx.doi.org/10.1111/j.1550-7408.1980.tb04680.x.
25. Schwenk R, Asher LV, Chalom I, Lanar D, Sun P, White K, Keil D, Kester KE, Stoute J, Heppner DG, Krzych U. 2003. Opsonization by antigen-specific antibodies as a mechanism of protective immunity induced by Plasmodium falciparum circumsporozoite protein-based vaccine. Parasite Immunol. 25:17-25. http://dx.doi.org/10.1046/j.1365-3024.2003.00495.x.
26. Chen DH, Tigelaar RE, Weinbaum FI. 1977. Immunity to sporozoiteinduced malaria infection in mice. I. The effect of immunization of T and B cell-deficient mice. J. Immunol. 118:1322-1327.
27. Egan JE, Weber JL, Ballou WR, Hollingdale MR, Majarian WR, Gordon DM, Maloy WL, Hoffman SL, Wirtz RA, Schneider I, Woollett GR, Young JF, Hockmeyer WT. 1987. Efficacy of murine malaria sporozoite vaccines: implications for human vaccine development. Science 236:453-456. http://dx.doi.org/10.1126/science.3551073.
28. + T cells. J. Infect. Dis. 196:608-616. http://dx.doi.org/10.1086/519742.
29. Foquet L, Hermsen CC, van Gemert GJ, Van Braeckel E, Weening KE, Sauerwein R, Meuleman P, Leroux-Roels G. 2013. Vaccine-induced monoclonal antibodies targeting circumsporozoite protein prevent Plasmodium falciparum infection. J. Clin. Invest. 124:140-144. http://dx.doi.org/10.1172/JCI70349.
30. Doolan DL, Hoffman SL. 2000. The complexity of protective immunity against liver-stage malaria. J. Immunol. 165:1453-1462. http://dx.doi.org/10.4049/jimmunol.165.3.1453.
31. Schulte S, Sukhova GK, Libby P. 2008. Genetically programmed biases in Th1 and Th2 immune responses modulate atherogenesis. Am. J. Pathol. 172:1500-1508. http://dx.doi.org/10.2353/ajpath.2008.070776.
32. Locksley RM, Heinzel FP, Sadick MD, Holaday BJ, Gardner KD, Jr. 1987. Murine cutaneous leishmaniasis: susceptibility correlates with differential expansion of helper T-cell subsets. Ann. Inst. Pasteur Immunol. 138:744-749. http://dx.doi.org/10.1016/S0769-2625(87)80030-2.
33. Vaughan AM, O'Neill MT, Tarun AS, Camargo N, Phuong TM, Aly AS, Cowman AF, Kappe SH. 2009. Type II fatty acid synthesis is essential only for malaria parasite late liver stage development. Cell. Microbiol. 11:506-520. http://dx.doi.org/10.1111/j.1462-5822.2008.01270.x.
34. Miller JL, Murray S, Vaughan AM, Harupa A, Sack B, Baldwin M, Crispe IN, Kappe SH. 2013. Quantitative bioluminescent imaging of pre-erythrocytic malaria parasite infection using luciferase-expressing Plasmodium yoelii. PLoS One 8:e60820. http://dx.doi.org/10.1371/journal.pone.0060820.
35. Trimnell A, Takagi A, Gupta M, Richie TL, Kappe SH, Wang R. 2009. Genetically attenuated parasite vaccines induce contact-dependentCD8+ T cell killing of Plasmodium yoelii liver stage-infected hepatocytes. J. Immunol. 183:5870-5878. http://dx.doi.org/10.4049/jimmunol.0900302.
36. Sellhorn G, Caldwell Z, Mineart C, Stamatatos L. 2009. Improving the expression of recombinant soluble HIV Envelope glycoproteins using pseudo-stable transient transfection. Vaccine 28:430-436. http://dx.doi.org/10.1016/j.vaccine.2009.10.028.
37. Carbonetti S, Oliver BG, Glenn J, Stamatatos L, Sather DN. 2014. Soluble HIV-1 envelope immunogens derived from an elite neutralizer elicit cross-reactive V1V2 antibodies and low potency neutralizing antibodies. PLoS One 9:e86905. http://dx.doi.org/10.1371/journal.pone.0086905.
38. Kennedy M, Fishbaugher ME, Vaughan AM, Patrapuvich R, Boonhok R, Yimamnuaychok N, Rezakhani N, Metzger P, Ponpuak M, Sattabongkot J, Kappe SH, Hume JC, Lindner SE. 2012. A rapid and scalable density gradient purification method for Plasmodium sporozoites. Malar. J. 11:421. http://dx.doi.org/10.1186/1475-2875-11-421.
39. Butler NS, Schmidt NW, Vaughan AM, Aly AS, Kappe SH, Harty JT. 2011. Superior antimalarial immunity after vaccination with late liver stage-arresting genetically attenuated parasites. Cell Host Microbe 9:451-462. http://dx.doi.org/10.1016/j.chom.2011.05.008.
40. Zavala F, Hollingdale MR, Schwartz AL, Nussenzweig RS, Nussenzweig V. 1985. Immunoradiometric assay to measure the in vitro penetration of sporozoites of malaria parasites into hepatoma cells. J. Immunol. 134: 1202-1205.
41. Nganou-Makamdop K, Sauerwein RW. 2013. Liver or blood-stage arrest during malaria sporozoite immunization: the later the better? Trends Parasitol. 29:304-310. http://dx.doi.org/10.1016/j.pt.2013.03.008.
42. Cooney LA, Gupta M, Thomas S, Mikolajczak S, Choi KY, Gibson C, Jang IK, Danziger S, Aitchison J, Gardner MJ, Kappe SH, Wang R. 2013. Short-lived effector CD8 T cells induced by genetically attenuated malaria parasite vaccination express CD11c. Infect. Immun. 81:4171-4181. http://dx.doi.org/10.1128/IAI.00871-13.
43. Silvie O, Greco C, Franetich JF, Dubart-Kupperschmitt A, Hannoun L, van Gemert GJ, Sauerwein RW, Levy S, Boucheix C, Rubinstein E, Mazier D. 2006. Expression of human CD81 differently affects host cell susceptibility to malaria sporozoites depending on the Plasmodium species. Cell. Microbiol. 8:1134-1146. http://dx.doi.org/10.1111/j.1462-5822.2006.00697.x.
44. Silvie O, Rubinstein E, Franetich JF, Prenant M, Belnoue E, Renia L, Hannoun L, Eling W, Levy S, Boucheix C, Mazier D. 2003. Hepatocyte CD81 is required for Plasmodium falciparum and Plasmodium yoelii sporozoite infectivity. Nat. Med. 9:93-96. http://dx.doi.org/10.1038/nm808.
45. Mwakingwe A, Ting LM, Hochman S, Chen J, Sinnis P, Kim K. 2009. Noninvasive real-time monitoring of liver-stage development of bioluminescent Plasmodium parasites. J. Infect. Dis. 200:1470-1478. http://dx.doi.org/10.1086/606115.
46. Ploemen IH, Prudencio M, Douradinha BG, Ramesar J, Fonager J, van Gemert GJ, Luty AJ, Hermsen CC, Sauerwein RW, Baptista FG, Mota MM, Waters AP, Que I, Lowik CW, Khan SM, Janse CJ, Franke-Fayard BM. 2009. Visualisation and quantitative analysis of the rodent malaria liver stage by real time imaging. PLoS One 4:e7881. http://dx.doi.org/10.1371/journal.pone.0007881.
47. Martin RM, Brady JL, Lew AM. 1998. The need for IgG2c specific antiserum when isotyping antibodies from C57BL/6 and NOD mice. J. Immunol. Methods 212:187-192. http://dx.doi.org/10.1016/S0022-1759 (98)00015-5.
48. Clyde DF, Most H, McCarthy VC, Vanderberg JP. 1973. Immunization of man against sporozite-induced falciparum malaria. Am. J. Med. Sci. 266:169-177. http://dx.doi.org/10.1097/00000441-197309000-00002.
49. Leatherbarrow RJ, Dwek RA. 1984. Binding of complement subcomponent C1q to mouse IgG1, IgG2a and IgG2b: a novel C1q binding assay. Mol. Immunol. 21:321-327. http://dx.doi.org/10.1016/0161-5890(84) 90103-2.
50. Kipps TJ, Parham P, Punt J, Herzenberg LA. 1985. Importance of immunoglobulin isotype in human antibody-dependent, cell-mediated cytotoxicity directed by murine monoclonal antibodies. J. Exp. Med. 161: 1-17. http://dx.doi.org/10.1084/jem.161.1.1.
51. Oi VT, Vuong TM, Hardy R, Reidler J, Dangle J, Herzenberg LA, Stryer L. 1984. Correlation between segmental flexibility and effector function of antibodies. Nature 307:136-140. http://dx.doi.org/10.1038/307136a0.
52. Doolan DL, Mu Y, Unal B, Sundaresh S, Hirst S, Valdez C, Randall A, Molina D, Liang X, Freilich DA, Oloo JA, Blair PL, Aguiar JC, Baldi P, Davies DH, Felgner PL. 2008. Profiling humoral immune responses to P. falciparum infection with protein microarrays. Proteomics 8:4680-4694. http://dx.doi.org/10.1002/pmic.200800194.
53. Felgner PL, Roestenberg M, Liang L, Hung C, Jain A, Pablo J, Nakajima-Sasaki R, Molina D, Teelen K, Hermsen CC, Sauerwein R. 2013. Pre-erythrocytic antibody profiles induced by controlled human malaria infections in healthy volunteers under chloroquine prophylaxis. Sci. Rep. 3:3549. http://dx.doi.org/10.1038/srep03549.
54. Trieu A, Kayala MA, Burk C, Molina DM, Freilich DA, Richie TL, Baldi P, Felgner PL, Doolan DL. 2011. Sterile protective immunity to malaria is associated with a panel of novel P. falciparum antigens. Mol. Cell. Proteomics 10:M111.007948. http://dx.doi.org/10.1074/mcp.M111.007948.
55. Ewer KJ, O'Hara GA, Duncan CJ, Collins KA, Sheehy SH, Reyes-Sandoval A, Goodman AL, Edwards NJ, Elias SC, Halstead FD, Longley RJ, Rowland R, Poulton ID, Draper SJ, Blagborough AM, Berrie E, Moyle S, Williams N, Siani L, Folgori A, Colloca S, Sinden RE, Lawrie AM, Cortese R, Gilbert SC, Nicosia A, Hill AV. 2013. Protective CD8+ T-cell immunity to human malaria induced by chimpanzee adenovirus-MVA immunisation. Nat. Commun. 4:2836. http://dx.doi.org/10.1038/ncomms3836.