Infectivity of Plasmodium berghei sporozoites delivered by intravenous inoculation versus mosquito bite: Implications for sporozoite vaccine trials

Infection and Immunity

Volumn 67, Issue 8, 1999, Pages 4285-4289

  Vaughan, Jefferson A ^a   Scheller, Libia F ^a   Wirtz, Robert A ^a,b   Azad, Abdu F ^a  

^a UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^b CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SPOROZOITE VACCINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; FEMALE; IMMUNIZATION; INFECTION PREVENTION; INOCULATION; INSECT BITE; INTRAVENOUS DRUG ADMINISTRATION; MALARIA; MOSQUITO; MOUSE; NONHUMAN; PLASMODIUM BERGHEI; PRIORITY JOURNAL; SPOROZOITE;

EID: 0032770010     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/iai.67.8.4285-4289.1999     Document Type: Article

References (56)

1. Anders, R. F., P. E. Crewther, S. Edwards, M. Margetts, M. L. Matthew, B. Pollock, and D. Pye. 1998. Immunisation with recombinant AMA-1 protects mice against infection with Plasmodium chabaudi. Vaccine 16:240-247.
2. Becker, S. I., R. Wang, R. C. Hedstrom, J. C. Aguiar, T. R. Jones, S. L. Hoffman, and M. J. Gardner. 1998. Protection of mice against Plasmodium yoelii sporozoite challenge with P. yoelii merozoite surface protein 1 DNA vaccines. Infect. Immun. 66:3457-3461.
3. Beier, J. C., J. R. Davis, J. A. Vaughan, B. H. Noden, and M. S. Beier. 1991. Quantitation of Plasmodium falciparum sporozoites transmitted by experimentally infected Anopheles gambiae and Anopheles stephensi. Am. J. Trop. Med. Hyg. 44:564-570.
4. Beier, J. C., M. S. Beier, J. A. Vaughan, C. B. Pumpuni, J. R. Davis, and B. H. Noden. 1992. Sporozoite transmission by Anopheles freeborni and Anopheles gambiae experimentally infected with Plasmodium falciparum. J. Am. Mosq. Control Assoc. 8:404-408.
5. Beier, M. S., J. R. Davis, C. B. Pumpuni, B. H. Noden, and J. C. Beier. 1992. Ingestion of Plasmdium falciparum sporozoites during transmission by anopheline mosquitoes. Am. J. Trop. Med. Hyg. 47:195-200.
6. Bosworth, A. B., I. Schneider, and J. E. Freier. 1975. Mass isolation of Anopheles stephensi salivary glands infected with malarial sporozoites. J. Parasitol. 61:769-772.
7. Chatterjee, S., G. Francois, P. Druilhe, G. Timperman, and M. Wery. 1996. Immunity to Plasmodium berghei exoerythrocytic forms derived from irradiated sporozoites. Parasitol. Res. 82:297-303.
8. Church, L. W., T. P. Le, J. P. Bryan, D. M. Gordon, R. Edelman, L. Fries, J. R. Davis, D. A. Herrington, D. F. Clyde, M. J. Shmuklarsky, J. Schneider, T. W. McGovern, J. D. Chulay, W. R. Ballou, and S. L. Hoffman. 1997. Clinical manifestations of Plasmodium falciparum malaria experimentally induced by mosquito challenge. J. Infect. Dis. 175:915-920.
9. Clyde, D. F., H. Most, V. C. McCarthy, and J. P. Vanderberg. 1973. Immunization of man against sporozoite-induced falciparum malaria. Am. J. Med. Sci. 266:169-177.
10. Doolan, D. L., M. Sedegah, R. C. Hedstrom, P. Hobart, Y. Charoenvit, and S. L. Hoffman. 1996. Circumventing genetic restriction of protection against malaria with multigene DNA immunization: CD8+ cell-, interferon gamma-, and nitric oxide-dependent immunity. J. Exp. Med. 183:1739-1746.
11. Edelman, R., S. L. Hoffman, J. R. Davis, M. Beier, M. B. Sztein, G. Losonsky, D. A. Herrington, H. A. Eddy, M. R. Hollingdale, D. M. Gordon, and D. F. Clyde. 1993. Long-term persistence of sterile immunity in a volunteer immunized with X-irradiated Plasmodium falciparum sporozoites. J. Infect. Dis. 168:1066-1070.
12. Edwards, J. F., S. Higgs, and B. J. Beatty. 1998. Mosquito feeding-induced enhancement of Cache Valley virus (Bunyaviridae) infection in mice. J. Med. Entomol. 35:261-265.
13. Egan, J. E., J. L. Weber, W. R. Ballou, M. R. Hollingdale, W. R. Majarian, D. M. Gordon, W. L. Maloy, S. L. Hoffman, R. A. Wirtz, I. Schneider, G. R. Woollett, J. F. Young, and W. T. Hockmeyer. 1987. Efficacy of murine malaria sporozoite vaccines: implications for human vaccine development. Science 236:453-456.
14. Fries, L. F., D. M. Gordon, I. Schneider, J. C. Beier, G. W. Long, M. Gross, J. U. Que, S. J. Cryz, and J. C. Sadoff. 1992. Safety, immunogenicity, and efficacy of a Plasmodium falciparum vaccine comprising a circumsporozoite protein repeat region peptide conjugated to Pseudomonas aeruginosa toxin A. Infect. Immun. 60:1834-1839.
15. Gordon, D. M., T. W. McGovern, U. Krzych, J. C. Cohen, I. Schneider, R. LaChance, D. G. Heppner, G. Yuan, M. R. Hollingdale, M. Slaoui, et al. 1995. Safety, immunogenicity, and efficacy of a recombinantly produced Plasmodium falciparum circumsporozoite protein-hepatitis B surface antigen subunit vaccine. J. Infect. Dis. 171:1576-1585.
16. Griffiths, R. B., and R. M. Gordon. 1952. An apparatus which enables the process of feeding by mosquitoes to be observed; together with an account of the ejection of saliva and its significance in malaria. Ann. Trop. Med. Parasitol. 46:311-319.
17. Heppner, D. G., D. M. Gordon, M. Gross, B. Wellde, W. Leitner, U. Krzych, I. Schneider, R. A. Wirtz, R. L. Richards, A. Trofa, T. Hall, J. C. Sadoff, P. Boerger, C. R. Alving, D. R. Sylvester, T. G. Porter, and W. R. Ballou. 1996. Safety, immunogenicity, and efficacy of Plasmodium falciparum repeatless circumsporozoite protein vaccine encapsulated in liposomes. J. Infect. Dis. 174:361-366.
18. Herrington, D. A., D. F. Clyde, J. R. Murphy, S. Baqar, M. M. Levine, V. do Rosario, and M. R. Hollingdale. 1988. A model for Plasmodium falciparum sporozoite challenge and very early therapy of parasitaemia for efficacy studies of sporozoite vaccines. Trop. Geogr. Med. 40:124-127.
19. Hoffman, S. L., M. Sedegah, and R. C. Hedstrom. 1994. Protection against malaria by immunization with a Plasmodium yoelii circumsporozoite protein nucleic acid vaccine. Vaccine 12:1529-1533.
20. Hoffman, S. L., R. Edelman, J. P. Bryan, I. Schneider, J. Davis, M. Sedegah, D. Gordon, P. Church, M. Gross, C. Silverman, et al. 1994. Safety, immunogenicity, and efficacy of a malaria sporozoite vaccine administered with monophosphoryl lipid A, cell wall skeleton of mycobacteria, and squalane as adjuvant. Am. J. Trop. Med. Hyg. 51:603-612.
21. Jaffe, R. I., G. H. Lowell, and D. M. Gordon. 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.
22. Jones, L. D., W. R. Kaufman, and P. A. Nuttall. 1992. Modification of the skin feeding site by tick saliva mediates virus transmission. Experientia 48: 779-782.
23. Khan, Z. M., and J. P. Vanderberg. 1991. Role of host cellular response in differential susceptibility of nonimmunized BALB/c mice to Plasmodium berghei and Plasmodium yoelii sporozoites. Infect. Immun. 59:2529-2534.
24. Klotz, F. W., L. F. Scheller, M. C. Seguin, N. Kumar, M. A. Marletta, S. J. Green, and A. F. Azad. 1995. Co-localization of inducible-nitric oxide synthase and Plasmodium berghei in hepatocytes from rats immunized with irradiated sporozoites. J. Immunol. 154:3391-3395.
25. Labuda, M., L. D. Jones, T. Williams, and P. A. Nuttall. 1993. Enhancement of tick-borne encephalitis virus transmission by tick salivary gland extracts. Med. Vet. Entomol. 7:193-196.
26. Marussig, M., L. Renia, A. Motard, F. Miltgen, P. Petour, V. Chauhan, G. Corradin, and D. Mazier. 1997. Linear and multiple antigen peptides containing defined T and B epitopes of the Plasmodium yoelii circumsporozoite protein: antibody-mediated protection and boosting by sporozoite infection. Int. Immunol. 9:1817-1824.
27. Maynes, B. 1933. The injection of mosquito sporozoites in malaria therapy. Public Health Rep. 48:909-916.
28. Ockenhouse, C. F., P. F. Sun, D. E. Lanar, B. T. Wellde, B. T. Hall, K. Kester, J. A. Stoute, A. Magill, U. Krzych, L. Farley, R. A. Wirtz, J. C. Sadoff, D. C. Kaslow, S. Kumar, L. W. Church, J. M. Crutcher, B. Wizel, S. Hoffman, A. Lalvani, A. V. Hill, J. A. Tine, K. P. Guito, C. de Taisne, R. Anders, W. R. Ballou, et al. 1998. Phase I/IIa safety, immunogenicity, and efficacy trial of NYVAC-Pf7, a pox-vectored, multiantigen, multistage vaccine candidate for Plasmodium falciparum malaria. J. Infect. Dis. 177:1664-1673.
29. Ozaki, L. S., R. W. Gwadz, and G. N. Godson. 1984. Simple centrifugation method for rapid separation of sporozoites from mosquitoes. J. Parasitol. 70:831-833.
30. Pacheco, N. D., C. P. A. Strome, F. Mitchell, M. P. Bawden, and R. L. Beaudoin. 1979. Rapid, large-scale isolation of Plasmodium berghei sporozoites from infected mosquitoes. J. Parasitol. 65:414-417.
31. Ponnudurai, T., A. H. Lensen, G. J. Van Glemert, M. G. Bolmer, and J. H. Meuwissen. 1991. Feeding behaviour and sporozoite ejection by infected Anopheles Stephensi. Trans. R. Soc. Trop. Med. Hyg. 85:175-180.
32. Pumpuni, C. B., C. Mendis, and J. C. Beier. 1997. Plasmodium yoelii sporozoite infectivity varies as a function of sporozoite loads in Anopheles stephensi mosquitoes. J. Parasitol. 83:652-655.
33. Renia, L., M. M. Rodrigues, and V. Nussenzweig. 1994. Intrasplenic immunization with infected hepatocytes: a mouse model for studying protective immunity against malaria pre-erythrocytic stage. Immunology 82:164-168.
34. Renia, L., I. T. Ling, M. Marussig, F. Miltgen, A. A. Holder, and D. Mazier. 1997. Immunization with a recombinant C-terminal fragment of Plasmodium yoelii merozoite surface protein 1 protects mice against homologous but not hcterologous P. yoelii sporozoite challenge. Infect. Immun. 65:4419-4423.
35. Ribeiro, J. M., and R. H. Nussenzveig. 1993. The salivary catechol oxidase/ peroxidase activities of the mosquito Anopheles albimanus. J. Exp. Biol. 179:273-287.
36. Ribeiro, J. M., R. H. Nussenzveig, and G. Tortorella. 1994. Salivary vasodilators of Aedes triseriatus and Anopheles gambiae (Diptera: Culicidae). J. Med. Entomol. 31:747-753.
37. Ribeiro, J. M. 1996. NAD(P)H-dependent production of oxygen reactive species by the salivary glands of the mosquito Anopheles albimanus. Insect Biochem. Mol. Biol. 26:715-720.
38. Rodrigues, E. G., F. Zavala, D. Eichinger, J. M. Wilson, and M. Tsuji. 1997. Single immunizing dose of recombinant adenovirus efficiently induces CD8+ T cell-mediated protective immunity against malaria. J. Immunol. 158:1268-1274.
39. Rosenberg, R., R. A. Wirtz, I. Schneider, and R. Burge. 1990. An estimation of the number of malaria sporozoites ejected by a feeding mosquito. Trans. R Soc. Trop. Med. Hyg. 84:209-212.
40. Scheller, L. F., H. A. Wirtz, and A. F. Azad. 1994. Susceptibility of different strains of mice to hepatic infection with Plasmodium berghei. Infect. Immun. 62:4844-4847.
41. Sedegah, M., T. R. Jones, M. Kaur, R. Hedstrom, P. Hobart, J. A. Tine, and S. L. Hoffman. 1998. Boosting with recombinant vaccinia increases immunogenicity and protective efficacy of malaria DNA vaccine. Proc. Natl. Acad. Sci. USA 95:7648-7653.
42. Seguin, M. C., W. R. Ballou, and C. A. Nacy. 1989. Interactions of Plasmodium berghei sporozoites and murine Kupffer cells in vitro. J. Immunol. 143:1716-1722.
43. Sidjanski, S., and J. P. Vanderberg. 1997. Delayed migration of Plasmodium sporozoites from the mosquito bite site to the blood. Am. J. Trop. Med. Hyg. 57:426-429.
44. Stark, K. R., and A. A. James. 1996. Salivary gland anticoagulants in culicine and anopheline mosquitoes (Diptera:Culicidae). J. Med. Entomol. 33:645- 650.
45. Stoute, J. A., M. Slaoui, D. G. Heppner, P. Momin, K. E. Kester, P. Desmons, B. T. Wellde, N. Garcon, U. Krzych, and M. Marchand. 1997. A preliminary evaluation of a recombinant circumsporozoite protein vaccine against Plasmodium falciparum malaria. N. Engl. J. Med. 336:86-91.
46. Sturchler, D., R. Berger, C. Rudin, M. Just, A. Saul, C. Rzepczyk, G. Brown, R. Anders, R. Coppel, G. Woodrow, et al. 1995. Safety, immunogenicity, and pilot efficacy of Plasmodium falciparum sporozoite and asexual blood-stage combination vaccine in Swiss adults. Am. J. Trop. Med. Hyg. 53:423-431.
47. Titus, R. G., and J. M. Ribeiro. 1988. Salivary gland lysates from the sand fly Lutzomyia longipalpis enhance Leishmania infectivity. Science 239:1306-1308.
48. Tonkin, I. M. 1947. The influence of the suspending fluid on the survival of sporozoites in vitro. Trans. R. Soc. Trop. Med. Hyg. 41:259-262.
49. Touray, M. G., A. Warburg, A. Laughinghouse, A. U. Krettli, and L. H. Miller. 1992. Developmentally regulated infectivity of malaria sporozoites for mosquito salivary glands and the vertebrate host. J. Exp. Med. 175:1607-1612.
50. Vanderberg, J. P. 1974. Studies on the motility of Plasmodium sporozoites. J. Protozool. 21:527-537.
51. Vanderberg, J. P., Z. M. Khan, and M. J. Stewart. 1993. Induction of hepatic inflammatory response by Plasmodium berghei sporozoites protects BALB/c mice against challenge with Plasmodium yoelii sporozoites. J. Parasitol. 79: 763-767.
52. Wang, R., Y. Charoenvit, G. Corradin, R. Porrozzi, R. L. Hunter, G. Glenn, C. R. Alving, P. Church, and S. L. Hoffman. 1995. Induction of protective polyclonal antibodies by immunization with a Plasmodium yoelii circumsporozoite protein multiple antigen peptide vaccine. J. Immunol. 154:2784-2793.
53. Wang, R., Y. Charoenvit, G. Corradin, P. De La Vega, E. D. Franke, and S. L. Hoffman. 1996. Protection against malaria by Plasmodium yoelii sporozoite surface protein 2 linear peptide induction of CD4+ T cell- and IFN-gamma-dependent elimination of infected hepatocytes. J. Immunol. 157:4061-4071.
54. Weber, J. L., J. E. Egan, J. L. Lyon, R. A. Wirtz, Y. Charoenvit, W. L. Maloy, and W. T. Hockmeyer. 1987. Plasmodium berghei: cloning of the circumsporozoite protein gene. Exp. Parasitol. 53:295-300.
55. White, K. L., H. L. Snyder, and U. Krzych. 1996. MHC class I-dependent presentation of exoerythrocytic antigens to CD8+ T lymphocytes is required for protective immunity against Plasmodium berghei. J. Immunol. 156:3374- 3381.
56. Yorke, W., and J. W. Macfie. 1924. The action of the salivary secretion of mosquitoes and of Glossina tachinoides or human blood. Ann. Trop. Med. Parasitol. 18:103-108.