Recombinant Mycobacterium bovis bacillus Calmette-Guerin secreting merozoite surface protein 1 (MSP1) induces protection against rodent malaria parasite infection depending on MSP1-stimulated interferon γ and parasite- specific antibodies

Journal of Experimental Medicine

Volumn 188, Issue 5, 1998, Pages 845-854

  Matsumoto, Sohkichi ^a   Yukitake, Hideharu ^a   Kanbara, Hiroji ^a   Yamada, Takeshi ^a  

^a NAGASAKI UNIVERSITY   (Japan)

Author keywords

Cytokine; Malaria vaccine; Protection; Recombinant bacillus Calmette Guerin; Secretion system

Indexed keywords

BCG SECRETING MSP1; GAMMA INTERFERON; IMMUNOGLOBULIN G2A; MALARIA VACCINE; MEMBRANE PROTEIN; MEROZOITE SURFACE PROTEIN 1; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ANTIBODY SPECIFICITY; ARTICLE; CONTROLLED STUDY; IMMUNE RESPONSE; MALARIA; MEROZOITE; MOUSE; MYCOBACTERIUM BOVIS; NONHUMAN; PARASITE CONTROL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN SECRETION;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIBODIES, PROTOZOAN; ANTIBODY SPECIFICITY; BCG VACCINE; FEMALE; IMMUNE SERA; INTERFERON TYPE II; INTERLEUKIN-4; MALARIA; MALARIA VACCINES; MEROZOITE SURFACE PROTEIN 1; MICE; MICE, INBRED A; MICE, INBRED C3H; MYCOBACTERIUM BOVIS; MYCOBACTERIUM KANSASII; NITROUS OXIDE; PEPTIDE FRAGMENTS; PLASMODIUM YOELII; PROTEIN CONFORMATION; PROTEIN PRECURSORS; PROTOZOAN PROTEINS; RATS; RECOMBINANT FUSION PROTEINS; VACCINES, SYNTHETIC;

EID: 0032494134     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.188.5.845     Document Type: Article

References (65)

1. Nussenzweig, R.S., and C.A. Long. 1994. Malaria vaccines: multiple targets. Science. 265:1381-1383.
2. Snapper, S.B., R.E. Melton, S. Mustafa, T. Kieser, and W.J. Jacobs. 1990. Isolation and characterization of efficient plasmid transformation mutants of Mycobacterium smegmatis. Mol. Microbiol. 4:1911-1919.
3. Matsuo, K., R. Yamaguchi, A. Yamazaki, H. Tasaka, K. Terasaka, M. Totsuka, K. Kobayashi, H. Yukitake, and T. Yamada. 1990. Establishment of a foreign antigen secretion system in mycobacteria. Infect. Immun. 58:4049-4054.
4. Aldovini, A., and R.A. Young. 1991. Humoral and cell-mediated immune responses to live recombinant BCG-HIV vaccines. Nature. 351:479-482.
5. Stover, C.K., V.F. de la Cruz, T.R. Fuerst, J.E. Burlein, L.A. Benson, L.T. Bennett, G.P. Bansal, J.F. Young, M.H. Lee, G.F. Hatfull, et al. 1991. New use of BCG for recombinant vaccines. Nature. 351:456-460.
6. Winter, N., M. Lagranderie, J. Rauzier, J. Timm, C. Leclerc, B. Guy, M.P. Kieny, M. Gheorghiu, and B. Gicquel. 1991. Expression of heterologous genes in Mycobacterium bovis BCG: induction of a cellular response against HIV-1 Nef protein. Gene. 109:47-54.
7. Fuerst, T.R., C.K. Stover, and V.F. de la Cruz. 1991. Development of BCG as a live recombinant vector system: potential use as an HIV vaccine. Biotcehnol. Ther. 2:159-178.
8. Yasutomi, Y., S. Koenig, S.S. Haun, C.K. Stover, R.K. Jackson, P. Conard, A.J. Conley, E.A. Emini, T.R. Fuerst, and N.L. Letvin. 1993. Immunization with recombinant BCG-SIV elicits SIV-specific cytotoxic T lymphocytes in rhesus monkeys. J. Immunol. 150:3101-3107.
9. Lagranderie, M., A. Murray, B. Gicquel, C. Leclerc, and M. Gheorghiu. 1993. Oral immunization with recombinant BCG induces cellular and humoral immune responses against the foreign antigen. Vaccine. 11:1283-1290.
10. Haeseleer, F., J.F. Pollet, M. Haumont, A. Bollen, and P. Jacobs. 1993. Stable integration and expression of the Plasmodium falciparum circumsporozoite protein coding sequence in mycobacteria. Mol. Biochem. Parasitol. 57:117-126.
11. Connell, N.D., A.E. Medina, W.R. McMaster, B.R. Bloom, and D.G. Russell. 1993. Effective immunization against cutaneous leishmaniasis with recombinant bacille Calmette-Guérin expressing the Leishmania surface proteinase gp63. Proc. Natl. Acad. Sci. USA. 90:11473-11477.
12. O'Donnell, M.A., A. Aldovini, R.B. Duda, H. Yang, A. Szilvasi, R.A. Young, and W.C. DeWolf. 1994. Recombinant Mycobacterium bovis BCG secreting functional interleukin-2 enhances gamma interferon production by splenocytes. Infect. Immun. 62:2508-2514.
13. Stover, C.K., G.P. Bansal, M.S. Hanson, J.E. Burlein, S.R. Palaszynski, J.F. Young, S. Koenig, D.B. Young, A. Sadziene, and A.G. Barbour. 1993. Protective immunity elicited by recombinant bacille Calmette-Guérin (BCG) expressing outer surface protein A (OspA) lipoprotein: a candidate Lyme disease vaccine. J. Exp. Med. 178:197-209.
14. Langermann, S., S. Palaszynski, A. Sadziene, C.K. Stover, and S. Koenig. 1994. Systemic and mucosal immunity induced by BCG vector expressing outer-surface protein A of Borrelia burgdorferi. Nature. 372:552-555.
15. Langermann, S., S.R. Palaszynski, J.E. Burlein, S. Koenig, M.S. Hanson, D.E. Briles, and C.K. Stover. 1994. Protective humoral response against pneumococcal infection in mice elicited by recombinant bacille Calmette-Guérin vaccines expressing pneumococcal surface protein A. J. Exp. Med. 180: 2277-2286.
16. Clark, I.A., A.C. Allison, and F.E. Cox. 1976. Protection of mice against Babesia and Plasmodium with BCG. Nature. 259: 309-311.
17. Murphy, J.R. 1981. Host defenses in murine malaria: non-specific resistance to Plasmodium bergliei generated in response to Mycobacterium bovis infection or Corynebacterium parvum stimulation. Infect. Immun. 33:199-211.
18. Lussow, A.R., G.G. Del, L. Renia, D. Mazier, J.P. Verhave, A.S. Verdini, A. Pessi, J.A. Louis, and P.H. Lambert. 1990. Use of a tuberculin purified protein derivative-Asn-Ala-Asn-Pro conjugate in bacillus Calmette-Guerin primed mice overcomes H-2 restriction of the antibody response and avoids the need tor adjuvants. Proc. Natl. Acad. Sci. USA. 87: 2960-2964.
19. Matsumoto, S., T. Yanagi, N. Ohara, N. Wada, H. Kanbara, and T. Yamada. 1996. Stable expression and secretion of the B-cell epitope of rodent malaria from Mycobacterium bovis BCG and induction of long-lasting humoral response in mouse. Vaccine. 14:54-60.
20. Holder, A.A., and R.R. Freeman. 1982. Biosynthesis and processing of a Plasmodium falciparum schizont antigen recognized by immune serum and a monoclonal antibody. J. Exp. Med. 156:1528-1538.
21. del Portillo, H.A., J. Gysin, D.M. Mattei, E. Khouri, P.V. Udagama, K.N. Mendis, and P.H. David. 1988. Plasmodium vivax: cloning and expression of a major blood-stage surface antigen. Exp. Parasitol. 67:346-353.
22. Epstein, N., L.H. Miller, D.C. Kaushel, I.J. Udeinya, J. Rener, R.J. Howard, R. Asofsky, M. Aikawa, and R.L. Hess. 1981. Monoclonal antibodies against a specific surface determinant on malarial (Plasmodium knowlesi) merozoites block erythrocyte invasion. J. Immunol. 127:212-217.
23. Holder, A.A., R.R. Freeman, and C.I. Newbold. 1983. Serological cross-reaction between high molecular weight proteins synthesized in blood schizonts of Plasmodium yoelii, Plasmodium chabaudi and Plasmodium falciparum. Mol. Biochem. Parasitol. 9:191-196.
24. Holder, A.A., and R.R. Freeman. 1981. Immunization against blood-stage rodent malaria using purified parasite antigens. Nature. 294:361-364.
25. Boyle, D.B., C.I. Newbold, C.C. Smith, and K.N. Brown. 1982. Monoclonal antibodies that protect in vivo against Plasmodium chabaudi recognize a 250,000-dalton parasite polypeptide. Infect. Immun. 38:94-102.
26. Newbold, C.I., D.B. Boyle, C.C. Smith, and K.N. Brown. 1982. Identification of a schizont- and species-specific surface glycoprotein on erythrocytes infected with rodent malarias. Mol. Biochem. Parasitol. 5:45-54.
27. Hall, R., J.E. Hyde, M. Goman, D.L. Simmons, I.A. Hope, M. Mackay, J. Scaife, B. Merkli, R. Richle, and J. Stocker. 1984. Major surface antigen gene of a human malaria parasite cloned and expressed in bacteria. Nature. 311:379-382.
28. Perrin, L.H., B. Merkli, M. Loche, C. Chizzolini, J. Smart, and R. Richle. 1984. Antimalarial immunity in Saimiri monkeys. Immunization with surface components of asexual blood stages. J. Exp. Med. 160:441-451.
29. Cheung, A., J. Leban, A.R. Shaw, B. Merkli, J. Stocker, C. Chizzolini, C. Sander, and L.H. Perrin. 1986. Immunization with synthetic peptides of a Plasmodium falciparum surface antigen induces antimerozoite antibodies. Proc. Natl. Acad. Sci. USA. 83:8328-8332.
30. Siddiqui, W.A., L.Q. Tam, K.J. Kramer, G.S. Hui, S.E. Case, K.M. Yamaga, S.P. Chang, E.B. Chan, and S.C. Kan. 1987. Merozoite surface coat precursor protein completely protects Aotus monkeys against Plasmodium falciparum malaria. Proc. Natl. Acad. Sci. USA. 84:3014-3018.
31. Holder, A.A., R.R. Freeman, and S.C. Nicholls. 1988. Immunization against Plasmodium falciparum with recombinant polypeptides produced in Escherichia coli. Parasite Immunol. (Oxf.). 10:607-617.
32. Herrera, S., M.A. Herrera, B.L. Perlaza, Y. Burki, P. Caspers, H. Dobeli, D. Rotmann, and U. Certa. 1990. Immunization of Aotus monkeys with Plasmodium falciparum blood-stage recombinant proteins. Proc. Natl. Acad. Sci. USA. 87:4017-4021.
33. Etlinger, H.M., P. Caspers, H. Matile, H.J. Schoenfeld, D. Stueber, and B. Takacs. 1991. Ability of recombinant or native proteins to protect monkeys against heterologous challenge with Plasmodium falciparum. Infect. Immun. 59:3498-3503.
34. Herrera, M.A., F. Rosero, S. Herrera, P. Caspers, D. Rotmann, F. Sinigaglia, and U. Certa. 1992. Protection against malaria in Aotus monkeys immunized with a recombinant blood-stage antigen fused to a universal T-cell epitope: correlation of serum gamma interferon levels with protection. Infect. Immun. 60:154-158.
35. Blackman, M.J., H.G. Heidrich, S. Donachie, J.S. McBride, and A.A. Holder. 1990. A single fragment of a malaria merozoite surface protein remains on the parasite during red cell invasion and is the target of invasion-inhibiting antibodies. J. Exp. Med. 172:379-382.
36. Blackman, M.J., I.T. Ling, S.C. Nicholls, and A.A. Holder. 1991. Proteolytic processing of the Plasmodium falciparum merozoite surface protein-1 produces a membrane-bound fragment containing two epidermal growth factor-like domains. Mol. Biochem. Parasitol. 49:29-33.
37. Blackman, M.J., and A.A. Holder. 1992. Secondary processing of the Plasmodium falciparum merozoite surface protein-1 (MSP1) by a calcium-dependent membrane-bound serine protease: shedding of MSP133 as a noncovalently associated complex with other fragments of the MSP1. Mol. Biochem. Parasitol. 50:307-315.
38. Miller, L.H., T. Roberts, M. Shahabuddin, and T.F. McCutchan. 1993. Analysis of sequence diversity in the Plasmodium falciparum merozoite surface protein-1 (MSP-1). mol. Biochem. Parasitol. 59:1-14.
39. Blackman, M.J., J.A. Chappel, S. Shai, and A.A. Holder. 1993. A conserved parasite serine protease processes the Plasmodium falciparum merozoite surface protein-1. Mol. Biochem. Parasitol. 62:103-114.
40. Pirson, P.J., and M.E. Perkins. 1985. Characterization with monoclonal antibodies of a surface antigen of Plasmodium falciparum merozoites. J. Immunol. 134:1946-1951.
41. Chang, S.P., H.L. Gibson, N.C. Lee, P.J. Barr, and G.S. Hui. 1992. A carboxyl-terminal fragment of Plasmodium falciparum gp195 expressed by a recombinant baculovirus induces antibodies that completely inhibit parasite growth. J. Immunol. 149:548-555.
42. Blackman, M.J., F.T. Scott, S. Shai, and A.A. Holder. 1994. Antibodies inhibit the protease-mediated processing of a malaria merozoite surface protein. J. Exp. Med. 180:389-393.
43. Majarian, W.R., T.M. Daly, W.P. Weidanz, and C.A. Long. 1984. Passive immunization against murine malaria with an IgG3 monoclonal antibody. J. Immunol. 132:3131-3137.
44. Burns, J.J., T.M. Daly, A.B. Vaidya, and C.A. Long. 1988. The 3′ portion of the gene for a Plasmodium yoelii merozoite surface antigen encodes the epitope recognized by a protective monoclonal antibody. Prof. Natl. Acad. Sci. USA. 85: 602-606.
45. Burns, J.J., W.R. Majarian, J.F. Young, T.M. Daly, and C.A. Long. 1989. A protective monoclonal antibody recognizes an epitope in the carboxyl-terminal cysteine-rich domain in the precursor of the major merozoite surface antigen of the rodent malarial parasite, Plasmodium yoelii. J. Immunol. 143: 2670-2676.
46. Daly, T.M., and C.A. Long. 1993. A recombinant 15-kilodalton carboxyl-terminal fragment of Plasmodium yoelii yoelii 17XL merozoite surface protein I induces a protective immune response in mice. Infect. Immun. 61:2462-2467.
47. Matsumoto, S., M. Tamaki, H. Yukitake, T. Matsuo, M. Naito, H. Teraoka, and T. Yamada. 1996. A stable Escherichia coli-mycobacteria shuttle vector 'pSO246' in Mycobacterium bovis BCG. FEMS Microbiol Lett. 135:237-243.
48. Lewis, A.P. 1989. Cloning and analysis of the gene encoding the 230-kilodalton merozoite surface antigen of Plasmodium yoelii. Mol. Biochem. Parasitol. 36:271-282.
49. Matsuo, K., R. Yamaguchi, A. Yamazaki, H. Tasaka, K. Terasaka, and T. Yamada. 1990. Cloning and expression of the gene for the cross-reactive alpha antigen of Mycobacterium kansasii. Infect. Immun. 58:550-556.
50. Daly, T.M., and C.A. Long. 1995. Humoral response to a carboxyl-terminal region of the merozoite surface protein-1 plays a predominant role in controlling blood-stage infection in rodent malaria. J. Immunol. 155:236-243.
51. Hirunpetcharat, C., J.H. Tian, D.C. Kaslow, N. van Rooijen, S. Kumar, J.A. Berzofsky, L.H. Miller, and M.F. Good. 1997. Complete protective immunity induced in mice by immunization with the 19-kilodalton carboxyl-terminal fragment of the merozoite surface protein-1 (MSP1[19]) of Plasmodium yoelii expressed in Saccharomyces cerevisiae: correlation of protection with antigen-specific antibody titer, but not with effector CD4+ T cells. J. Immunol. 159:3400-3411.
52. Freeman, R.R., and A.A. Holder. 1983. Characteristics of the protective response of BALB/c mice immunized with a purified Plasmodium yoelii schizont antigen. Clin. Exp. Immunol. 54:609-616.
53. Kumar, S., A. Yadava, D.B. Keister, J.H. Tian, M. Ohl, G.K. Perdue, L.H. Miller, and D.C. Kaslow. 1995. Immunogenicity and in vivo efficacy of recombinant Plasmodium falciparum merozoite surface protein-1 in Aotus monkeys. Mol. Med. 1: 325-332.
54. Burghaus, P.A., B.T. Wellde, T. Hall, R.L. Richards, A.F. Egan, E.M. Riley, W.R. Ballou, and A.A. Holder. 1996. Immunization of Aotus nancymai with recombinant C terminus of Plasmodium falciparum merozoite surface protein 1 in liposomes and alum adjuvant does not induce protection against a challenge infection. Infect. Immun. 64:3614-3619.
55. Mosmann, T.R., and R.L. Coffman. 1987. Two types of mouse helper T-cell clone: implications tor immune regulation. Imniunol. Today. 8:223-227.
56. Stuehr, D.J., and C.F. Nathan. 1989. Nitric oxide. A macrophage product responsible for cytostasis and respiratory inhibition in tumor target cells. J. Exp. Med. 169:1543-1555.
57. Taylor, R.A., R.S. Phillips, A. Severn, S. Moncada, and F.Y. Liew. 1993. The role of TH1 and TH2 cells in a rodent malaria infection. Science. 260:1931-1934.
58. Jacobs, P., D. Radzioch, and M.M. Stevenson. 1995. Nitric oxide expression in the spleen, but not in the liver, correlates with resistance to blood-stage malaria in mice. J. Immunol. 155:5306-5313.
59. Jacobs, P., D. Radzioch, and M.M. Stevenson. 1996. A Th1-associated increase in tumor necrosis factor alpha expression in the spleen correlates with resistance to blood-stage malaria in mice. Infect. Immun. 64:535-541.
60. Ding, A. H., C.F. Nathan, and D.J. Stuehr. 1988. Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages. Comparison of activating cytokines and evidence for independent production. J. Immunol. 141:2407-2412.
61. Bouharoun, T.H., P. Attanath, A. Sabchareon, T. Chong-suphajaisiddhi, and P. Druilhe. 1990. Antibodies that protect humans against Plasmodium falciparum blood stages do not on their own inhibit parasite growth and invasion in vitro, but act in cooperation with monocytes. J. Exp. Med. 172:1633-1641.
62. Bouharoun, T.H., and P. Druilhe. 1992. Plasmodium falciparum malaria: evidence for an isotype imbalance which may be responsible for delayed acquisition of protective immunity. Infect. Immun. 60:1473-1481.
63. Soares, I.S., G. Levitus, J.M. Souza, P.H. Del, and M.M. Rodrigues. 1997. Acquired immune responses to the N- and C-terminal regions of Plasmodium vivax merozoite surface protein 1 in individuals exposed to malaria. Infect. Immun. 65: 1606-1614.
64. Rzepczyk, C.M., K. Hale, N. Woodroffe, A. Bobogare, P. Csurhes, A. Ishii, and A. Ferrante. 1997. Humoral immune responses of Solomon Islanders to the merozoite surface antigen 2 of Plasmodiun falciparum show pronounced skewing towards antibodies of the immunoglobulin G3 subclass. Infect. Immun. 65:1098-1100.
65. von der Weid, T., N. Honarvar, and J. Langhorne. 1996. Gene-targeted mice lacking B cells are unable to eliminate a blood stage malaria infection. J. Immunol. 156:2510-2516.