Plasmodium falciparum serine repeat antigen 5 (SE36) as a malaria vaccine candidate

Vaccine

Volumn 29, Issue 35, 2011, Pages 5837-5845

  Palacpac, Nirianne Marie Q ^a,b   Arisue, Nobuko ^a   Tougan, Takahiro ^a   Ishii, Ken J ^c,d   Horii, Toshihiro ^a  

^a OSAKA UNIVERSITY   (Japan)

^b Osaka University   (Japan)

^c OSAKA UNIVERSITY   (Japan)

^d NATIONAL INSTITUTE OF BIOMEDICAL INNOVATION   (Japan)

Author keywords

Malaria; Plasmodium falciparum; Serine repeat antigen; Vaccine candidate

Indexed keywords

ALUMINUM HYDROXIDE; DNA VACCINE; IMMUNOGLOBULIN G; IMMUNOLOGICAL ADJUVANT; MALARIA VACCINE; MEROZOITE SURFACE PROTEIN 1; PARASITE ANTIGEN; PLACEBO; RECOMBINANT PROTEIN; RTS S AS02; SE 47 ANTIGEN; SE36 PROTEIN; SERINE REPEAT ANTIGEN 5; SERINE REPEAT ANTIGEN 7; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANTIBODY RESPONSE; ANTIBODY TITER; ANTIGENIC VARIATION; ASEXUAL REPRODUCTION; CLINICAL TRIAL; DNA IMMUNIZATION; DRUG TARGETING; ENDEMIC DISEASE; ENZYME LINKED IMMUNOSORBENT ASSAY; EPIDEMIOLOGICAL DATA; GENE DELIVERY SYSTEM; GENE EXPRESSION; GENE SEQUENCE; GENE TARGETING; GENETIC POLYMORPHISM; GENETIC VARIABILITY; HUMAN; IMMUNE RESPONSE; IMMUNOGENICITY; INJECTION SITE ERYTHEMA; INJECTION SITE INDURATION; INNATE IMMUNITY; LIFE CYCLE; MALARIA FALCIPARUM; MULTIGENE FAMILY; NONHUMAN; PARASITE IMMUNITY; PARASITE TRANSMISSION; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROCESSING; PROTEIN TARGETING; REVIEW; SEROCONVERSION; VACCINE PRODUCTION;

ADOLESCENT; ADULT; ANIMALS; ANTIBODIES, PROTOZOAN; ANTIGENS, PROTOZOAN; CHILD; CHILD, PRESCHOOL; CLINICAL TRIALS, PHASE I AS TOPIC; HUMANS; INFANT; MALARIA VACCINES; MALARIA, FALCIPARUM; PLASMODIUM FALCIPARUM; TREATMENT OUTCOME; YOUNG ADULT;

EID: 79960724541     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2011.06.052     Document Type: Review

References (84)

1. WHO World malaria report 2010 2010, WHO Global Malaria Programme. http://whqlibdoc.who.int/publications/2010/9789241564106_eng.pdf.
2. WHO Secretariat Malaria prevention and control: sustaining the gains and reducing transmission. WHO Executive Board 128th Session 25 November 2010, http://apps.who.int/gb/ebwha/pdf_files/EB128/B128_14-en.pdf.
3. Dhingra N., Jha P., Sharma V.P., Cohen A.A., Jotkar R.M., Rodriguez P.S., et al. Adult and child malaria mortality in India: a nationally representative mortality survey. Lancet 2010, 376(9754):1768-1774.
4. Cabral A.C., Fé N.F., Suárez-Mutis M.C., Bóia M.N., Carvalho-Costa F.A. Increasing incidence of malaria in the Negro River basin Brazilian Amazon. Trans R Soc Trop Med Hyg 2010, 104(8):556-562.
5. Nahum A., Erhart A., Mayé A., Ahounou D., van Overmeir C., Menten J., et al. Malaria incidence and prevalence among children living in a peri-urban area on the Coast of Benin, West Africa: a Longitudinal Study. Am J Trop Med Hyg 2010, 83(3):465-473.
6. Krungkrai J., Imprasittichai W., Otjungreed S., Pongsabut S., Krungkrai S.R. Artemisinin resistance or tolerance in human malaria patients. Asian Pac J Trop Med 2010, 3(9):748-753.
7. Prugnolle F., Durand P., Neel C., Ollomo B., Ayala F.J., Arnathau C., et al. African great apes are natural hosts of multiple related malaria species, including Plasmodium falciparum. Proc Natl Acad Sci U S A 2010, 107(4):1458-1463.
8. Liu W., Li Y., Learn G.H., Rudicell R.S., Robertson J.D., Keele B.F., et al. Origin of the human malaria parasite Plasmodium falciparum in gorillas. Nature 2010, 467(7314):420-425.
9. Putaporntip C., Hongsrimuang T., Seethamchai S., Kobasa T., Limkittikul K., Cui L., et al. Differential prevalence of Plasmodium infections and cryptic Plasmodium knowlesi malaria in humans in Thailand. J Infect Dis 2009, 199(8):1143-1150.
10. Crompton P.D., Pierce S.K., Miller L.H. Advances and challenges in malaria vaccine development. J Clin Invest 2010, 120(12):4168-4178.
11. Kappe S.H., Vaughan A.M., Boddey J.A., Cowman A.F. That was then but this is now; malaria research in the time of an eradication agenda. Science 2010, 328(5980):862-866.
12. The malERA Consultative Group on Vaccines A research agenda for malaria eradication: vaccines. PLoS Med 2011, 8(1):e1000398. PMID: 21311586.
13. Gardner M.J., Hall N., Fung E., White O., Berriman M., Hyman R.W., et al. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 2002, 419(6906):498-511.
14. Aurrecoechea C., Brestelli J., Brunk B.P., Dommer J., Fischer S., Gajria B., et al. PlasmoDB: a functional genomic database for malaria parasites. Nucleic Acids Res 2009, 37(Database issue):D539-D543.
15. Bojang K.A., Milligan P.J.M., Pinder M., Vigneron L., Alloueche A., Kester K.E., et al. Efficacy of RTS,S/AS02 malaria vaccine against Plasmodium falciparum infection in semi-immune adult men in The Gambia: a randomised trial. Lancet 2001, 358(9297):1927-1934.
16. Alonso P.L., Sacarlal J., Aponte J.J., Leach A., Macete E., Milman J., et al. Efficacy of the RTS,S/AS02A vaccine against Plasmodium falciparum infection and disease in young African children: randomised controlled trial. Lancet 2004, 364(9443):1411-1420.
17. Aponte J.J., Aide P., Renom M., Mandomando I., Bassat Q., Sacarlal J., et al. Safety of the RTS,S/AS02D candidate malaria vaccine in infants living in a highly endemic area of Mozambique: a double blind randomised controlled phase I/IIb trial. Lancet 2007, 370(9598):1543-1551.
18. Abdulla S., Oberholzer R., Juma O., Kubhoja S., Machera F., Membi C., et al. Safety and immunogenicity of RTS S/AS02D malaria vaccine in infants. New Engl J Med 2008, 359(24):2533-2544.
19. Aide P., Aponte J.J., Renom M., Nhampossa T., Sacarlal J., Mandomando I., et al. Safety, immunogenicity and duration of protection of the RTS,S/AS02D malaria vaccine: one year follow-up of a randomized controlled phase I/IIb trial. PLoS One 2010, 5(11):e13838. 10.1371/journal.pone.0013838.
20. Bejon P., Lusingu J., Olotu A., Leach A., Lievens M., Vekemans J., et al. Efficacy of RTS S/AS01E vaccine against malaria in children 5 to 17 months of age. New Engl J Med 2008, 359(24):2521-2532.
21. Perrin L.H., Merkli B., Loche M., Chizzolini C., Smart J., Richle R. Antimalarial immunity in Saimiri monkeys Immunization with surface components of asexual blood stages. J Exp Med 1984, 160(2):441-451.
22. Chulay J.D., Lyon J.A., Haynes J.D., Meierovics A.I., Atkinson A.T., Aikawa M. Monoclonal antibody characterization of Plasmodium falciparum antigens in immune complexes formed when schizonts rupture in the presence of immune serum. J Immunol 1987, 139(8):2768-2774.
23. Delplace P., Fortier B., Tronchin G., Dubremetz J.F., Vernes A. Localization, biosynthesis, processing and isolation of a major 126kDa antigen of the parasitophorous vacuole of Plasmodium falciparum. Mol Biochem Parasitol 1987, 23(3):193-201.
24. Knapp B., Hundt E., Nau U., Küpper H.A. Molecular cloning, genomic structure and localization of a blood stage antigen of Plasmodium falciparum characterized by a serine stretch. Mol Biochem Parasitol 1989, 32(1):73-83.
25. Delplace P., Bhatia A., Cagnard M., Camus D., Colombet G., Debrabant A., et al. Protein p126: a parasitophorous vacuole antigen associated with the release of Plasmodium falciparum merozoites. Biol Cell 1988, 64(2):215-221.
26. Horii T., Bzik D.J., Inselburg J. Characterization of antigen-expressing Plasmodium falciparum cDNA clones that are reactive with parasite inhibitory antibodies. Mol Biochem Parasitol 1988, 30(1):9-18.
27. Bzik D.J., Li W.B., Horii T., Inselburg J. Amino acid sequence of the serine-repeat antigen (SERA) of Plasmodium falciparum determined from cloned cDNA. Mol Biochem Parasitol 1988, 30(3):279-288.
28. Bourgon R., Delorenzi M., Sargeant T., Hodder A.N., Crabb B.S., Speed T.P. The serine repeat antigen (SERA) gene family phylogeny in Plasmodium: the impact of GC content and reconciliation of gene and species trees. Mol Biol Evol 2004, 21(11):2161-2171.
29. Kooij T.W.A., Carlton J.M., Bidwell S.L., Hall N., Ramesar J., Janse C.J., et al. A Plasmodium whole-genome synteny map: indels and synteny breakpoints as foci for species-specific genes. PLoS Pathog 2005, 1(4):e44. 10.1371/journal.ppat.0010044.
30. Arisue N., Hirai M., Arai M., Matsuoka H., Horii T. Phylogeny and evolution of the SERA multigene family in the genus Plasmodium. J Mol Evol 2007, 65(1):82-91.
31. Arisue N., Kawai S., Hirai M., Palacpac N.M.Q., Jia M., Kaneko A., et al. Clues to evolution of the SERA multigene family in 18 Plasmodium species. PLoS One 2011, 6(3):e17775. 10.1371/journal.pone.0017775.
32. Higgins D.G., McConnell D.J., Sharp P.M. Malarial proteinase?. Nature 1989, 340(6235):604.
33. Aly A.S.I., Matuschewski K. A malarial cysteine protease is necessary for Plasmodium sporozoite egress from oocysts. J Exp Med 2005, 202(2):225-230.
34. Miller S.K., Good R.T., Drew D.R., Delorenzi M., Sanders P.R., Hodder A.N., et al. A subset of Plasmodium falciparum SERA genes are expressed and appear to play an important role in the erythrocytic cycle. J Biol Chem 2002, 277(49):47524-47532.
35. Schmidt-Christensen A., Sturm A., Horstmann S., Heussler V.T. Expression and processing of Plasmodium berghei SERA3 during liver stages. Cell Microbiol 2008, 10(8):1723-1734.
36. Putrianti E.D., Schmidt-Christensen A., Arnold I., Heussler V.T., Matuschewski K., Silvie O. The Plasmodium serine-type SERA proteases display distinct expression patterns and non-essential in vivo roles during life cycle progression of the malaria parasite. Cell Microbiol 2010, 12(6):725-739.
37. Aoki S., Li J., Itagaki S., Okech B.A., Egwang T.G., Matsuoka H., et al. Serine repeat antigen (SERA5) is predominantly expressed among the SERA multigene family of Plasmodium falciparum, and the acquired antibody titers correlate with serum inhibition of the parasite growth. J Biol Chem 2002, 277(49):47533-47540.
38. Palacpac N.M.Q., Leung B.W.Y., Arisue N., Tanabe K., Sattabongkot J., Tsuboi T., et al. Plasmodium vivax serine repeat antigen (SERA) multigene family exhibits similar expression patterns in independent infections. Mol Biochem Parasitol 2006, 150(2):353-358.
39. Fox B.A., Bzik D.J. Analysis of stage-specific transcripts of the Plasmodium falciparum serine repeat antigen (SERA) gene and transcription from the SERA locus. Mol Biochem Parasitol 1994, 68(1):133-144.
40. Lasonder E., Ishihama Y., Andersen J.S., Vermunt A.M., Pain A., Sauerwein R.W., et al. Analysis of the Plasmodium falciparum proteome by high-accuracy mass spectrometry. Nature 2002, 419(6906):537-542.
41. McCoubrie J.E., Miller S.K., Sargeant T., Good R.T., Hodder A.N., Speed T.P., et al. Evidence for a common role for the serine-type Plasmodium falciparum serine repeat antigen proteases: implications for vaccine and drug design. Infect Immun 2007, 75(12):5565-5574.
42. Yeoh S., O'Donnell R.A., Koussis K., Dluzewski A.R., Ansell K.H., Osborne S.A., et al. Subcellular discharge of a serine protease mediates release of invasive malaria parasites from host erythrocytes. Cell 2007, 131(6):1072-1083.
43. Hodder A.N., Drew D.R., Epa V.C., Delorenzi M., Bourgon R., Miller S.K., et al. Enzymic, phylogenetic, and structural characterization of the unusual papain-like protease domain of Plasmodium falciparum SERA5. J Biol Chem 2003, 278(48):48169-48177.
44. Hodder A.N., Malby R.L., Clarke O.B., Fairlie W.D., Colman P.M., Crabb B.S., et al. Structural insights into the protease-like antigen Plasmodium falciparum SERA5 and its noncanonical active-site serine. J Mol Biol 2009, 392(1):154-165.
45. Perkins M.E., Ziefer A. Preferential binding of Plasmodium falciparum SERA and rhoptry proteins to erythrocyte membrane inner leaflet phospholipids. Infect Immun 1994, 62(4):1207-1212.
46. Sato D., Li J., Mitamura T., Horii T. Plasmodium falciparum serine-repeat antigen (SERA) forms a homodimer through disulfide bond. Parasitol Int 2005, 54(4):261-265.
47. Blackman M.J. Malarial proteases and host cell egress: an 'emerging' cascade. Cell Microbiol 2008, 10(10):1925-1934.
48. Debrabant A., Maes P., Delplace P., Dubremetz J.F., Tartar A., Camus D. Intramolecular mapping of Plasmodium falciparum p126 proteolytic fragments by N-terminal amino acid sequencing. Mol Biochem Parasitol 1992, 53(1-2):89-96.
49. Li J., Mitamura T., Fox B.A., Bzik D.J., Horii T. Differential localization of processed fragments of Plasmodium falciparum serine repeat antigen and further processing of its N-terminal 47kDa fragment. Parasitol Int 2002, 51(4):343-352.
50. Okitsu S.L., Boato F., Mueller M.S., Li D.B., Vogel D., Westerfeld N., et al. Antibodies elicited by a virosomally formulated Plasmodium falciparum serine repeat antigen-5 derived peptide detect the processed 47kDa fragment both in sporozoites and merozoites. Peptides 2007, 28(10):2051-2060.
51. Li J., Matsuoka H., Mitamura T., Horii T. Characterization of proteases involved in the processing of Plasmodium falciparum serine repeat antigen (SERA). Mol Biochem Parasitol 2002, 120(2):177-186.
52. Arastu-Kapur S., Ponder E.L., Fonović U.P., Yeoh S., Yuan F., Fonović M., et al. Identification of proteases that regulate erythrocyte rupture by the malaria parasite Plasmodium falciparum. Nat Chem Biol 2008, 4(3):203-213.
53. Fairlie W.D., Spurck T.P., McCoubrie J.E., Gilson P.R., Miller S.K., McFadden G.I., et al. Inhibition of malaria parasite development by a cyclic peptide that targets the vital parasite protein SERA5. Infect Immun 2008, 76(9):4332-4344.
54. Barr P.J., Inselburg J., Green K.M., Kansopon J., Hahm B.K., Gibson H.L., et al. Immunogenicity of recombinant Plasmodium falciparum SERA proteins in rodents. Mol Biochem Parasitol 1991, 45(1):159-170.
55. Sugiyama T., Suzue K., Okamoto M., Inselburg J., Tai K., Horii T. Production of recombinant SERA proteins of Plasmodium falciparum in Escherichia coli by using synthetic genes. Vaccine 1996, 14(11):1069-1076.
56. Inselburg J., Bzik D.J., Li W.B., Green K.M., Kansopon J., Hahm B.K., et al. Protective immunity induced in Aotus monkeys by recombinant SERA proteins of Plasmodium falciparum. Infect Immun 1991, 59(4):1247-1250.
57. Inselburg J., Bathurst I.C., Kansopon J., Barchfeld G.L., Barr P.J., Rossan R.N. Protective immunity induced in Aotus monkeys by a recombinant SERA protein of Plasmodium falciparum: adjuvant effects on induction of protective immunity. Infect Immun 1993, 61(5):2041-2047.
58. Inselburg J., Bathurst I.C., Kansopon J., Barr P.J., Rossan R. Protective immunity induced in Aotus monkeys by a recombinant SERA protein of Plasmodium falciparum: further studies using SERA 1 and MF75.2 adjuvant. Infect Immun 1993, 61(5):2048-2052.
59. Suzue K., Ito M., Matsumoto Y., Tanioka Y., Horii T. Protective immunity induced in squirrel monkeys with recombinant serine repeat antigen (SERA) of Plasmodium falciparum. Parasitol Int 1997, 46(1):17-25.
60. Chauhan V.S., Yazdani S.S., Gaur D. Malaria vaccine development based on merozoite surface proteins of Plasmodium falciparum. Hum Vaccine 2010, 6(9):757-762.
61. Fox B.A., Xing-Li P., Suzue K., Horii T., Bzik D.J. Plasmodium falciparum: an epitope within a highly conserved region of the 47-kDa amino-terminal domain of the serine repeat antigen is a target of parasite-inhibitory antibodies. Exp Parasitol 1997, 85(2):121-134.
62. Morimatsu K., Morikawa T., Tanabe K., Bzik D.J., Horii T. Sequence diversity in the amino-terminal 47kDa fragment of the Plasmodium falciparum serine repeat antigen. Mol Biochem Parasitol 1997, 86(2):249-254.
63. Liu Q., Ferreira M.U., Ndawi B.T., Ohmae H., Adagu I.S., Morikawa T., et al. Sequence diversity of serine repeat antigen gene exon II of Plasmodium falciparum in worldwide collected wild isolates. Southeast Asian J Trop Med Public Health 2000, 31(4):808-817.
64. Safitri I., Jalloh A., Tantular I.S., Pusarawati S., Win T.T., Liu Q., et al. Sequence diversity in the amino-terminal region of the malaria-vaccine candidate serine repeat antigen in natural Plasmodium falciparum populations. Parasitol Int 2003, 52(2):117-131.
65. Pratt-Riccio L.R., Sallenave-Sales S., de Oliveira-Ferreira J., da Silva B.T., Guimaraes M.L., Santos F., et al. Evaluation of the genetic polymorphism of Plasmodium falciparum P126 protein (SERA or SERP) and its influence on naturally acquired specific antibody responses in malaria-infected individuals living in the Brazilian Amazon. Malar J 2008, 7(144):7-144. 10.1186/1475-2875-7-144.
66. Horii T., Shirai H., Jie L., Ishii K.J., Palacpac N.Q., Tougan T., et al. Evidences of protection against blood-stage infection of Plasmodium falciparum by the novel protein vaccine SE36. Parasitol Int 2010, 59(3):380-386.
67. Banic D.M., Goldberg A.C., Pratt-Riccio L.R., De Oliveira-Ferreira J., Santos F., Gras-Masse H. Human leukocyte antigen class II control of the immune response to p126-derived amino terminal peptide from Plasmodium falciparum. Am J Trop Med Hyg 2002, 66(5):509-515.
68. Banic D.M., de Oliveira-Ferreira J., Pratt-Riccio L.R., Conseil V., Goncalves D., Fialho R.R., et al. Immune response and lack of immune response to Plasmodium falciparum P126 antigen and its amino-terminal repeat in malaria-infected humans. Am J Trop Med Hyg 1998, 58(6):768-774.
69. Okech B.A., Nalunkuma A., Okello D., Pang X.L., Suzue K., Li J., et al. Natural human immunoglobulin G subclass responses to Plasmodium falciparum serine repeat antigen in Uganda. Am J Trop Med Hyg 2001, 65(6):912-917.
70. Okech B., Mujuzi G., Ogwal A., Shirai H., Horii T., Egwang T.G. High titers of IgG antibodies against Plasmodium falciparum serine repeat antigen 5 (SERA5) are associated with protection against severe malaria in Ugandan children. Am J Trop Med Hyg 2006, 74(2):191-197.
71. Banyal H.S., Inselburg J. Isolation and characterization of parasite-inhibitory Plasmodium falciparum monoclonal antibodies. Am J Trop Med Hyg 1985, 34(6):1055-1064.
72. Banic D.M., Bossus M., Delplace P., Tartar A., Gras-Masse H., Conseil V., et al. Immunogenicity and antigenicity of the N-term repeat amino acid sequence of the Plasmodium falciparum P126 antigen. Mem Inst Oswaldo Cruz 1992, 87(3):159-162.
73. Fox B.A., Horii T., Bzik D.J. Plasmodium falciparum: fine-mapping of an epitope of the serine repeat antigen that is a target of parasite-inhibitory antibodies. Exp Parasitol 2002, 101(1):69-72.
74. Bathurst I.C., Gibson H.L., Kansopon J., Hahm B.K., Green K.M., Chang S.P., et al. An experimental vaccine cocktail for Plasmodium falciparum malaria. Vaccine 1993, 11(4):449-456.
75. Pang X.L., Horii T. Complement-mediated killing of Plasmodium falciparum erythrocytic schizont with antibodies to the recombinant serine repeat antigen (SERA). Vaccine 1998, 16(13):1299-1305.
76. Sakai T., Horii T., Hisaeda H., Zhang M., Ishii K., Nakano Y., et al. DNA immunization with Plasmodium falciparum serine repeat antigen: regulation of humoral immune response by coinoculation of cytokine expression plasmid. Parasitol Int 1999, 48(1):27-33.
77. Belperron A.A., Feltquate D., Fox B.A., Horii T., Bzik D.J. Immune responses induced by gene gun or intramuscular injection of DNA vaccines that express immunogenic regions of the serine repeat antigen from Plasmodium falciparum. Infect Immun 1999, 67(10):5163-5169.
78. Pang X.L., Mitamura T., Horii T. Antibodies reactive with the N-terminal domain of Plasmodium falciparum serine repeat antigen inhibit cell proliferation by agglutinating merozoites and schizonts. Infect Immun 1999, 67(4):1821-1827.
79. Soe S., Singh S., Camus D., Horii T., Druilhe P. Plasmodium falciparum serine repeat protein, a new target of monocyte-dependent antibody-mediated parasite killing. Infect Immun 2002, 70(12):7182-7184.
80. Taylor R.R., Smith D.B., Robinson V.J., McBride J.S., Riley E.M. Human antibody response to Plasmodium falciparum merozoite surface protein 2 is serogroup specific and predominantly of the immunoglobulin G3 subclass. Infect Immun 1995, 63(11):4382-4388.
81. Rzepczyk C.M., Hale K., Woodroffe N., Bobogare A., Csurhes P., Ishii A., et al. Humoral immune responses of Solomon Islanders to the merozoite surface antigen 2 of Plasmodium falciparum show pronounced skewing towards antibodies of the immunoglobulin G3 subclass. Infect Immun 1997, 65(3):1098-1100.
82. Bouharoun-Tayoun H., Druilhe P. Plasmodium falciparum malaria: evidence for an isotype imbalance which may be responsible for delayed acquisition of protective immunity. Infect Immun 1992, 60(4):1473-1481.
83. Coler R.N., Carter D., Friede M., Reed S.G. Adjuvants for malaria vaccines. Parasite Immunol 2009, 31(9):520-528.
84. Stoute J.A., Slaoui M., Heppner G., Momin P., Kester K.E., Desmons P., et al. A preliminary evaluation of a recombinant circumsporozoite protein vaccine against Plasmodium falciparum malaria. N Engl J Med 1997, 336(2):86-91.