Clues to evolution of the SERA multigene family in 18 Plasmodium species

PLoS ONE

Volumn 6, Issue 3, 2011, Pages

  Arisue, Nobuko ^a   Kawai, Satoru ^b   Hirai, Makoto ^c   Palacpac, Nirianne M Q ^a   Jia, Mozhi ^a,g   Kaneko, Akira ^d,e,f   Tanabe, Kazuyuki ^a   Horii, Toshihiro ^a  

^a OSAKA UNIVERSITY   (Japan)

^b DOKKYO MEDICAL UNIVERSITY   (Japan)

^c GUNMA UNIVERSITY   (Japan)

^d OSAKA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^e KAROLINSKA INSTITUTE   (Sweden)

^f NAGASAKI UNIVERSITY   (Japan)

^g PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; EXON; GENE CLUSTER; GENE DUPLICATION; GENE EXPRESSION; GENE IDENTIFICATION; GENE NUMBER; GENE STRUCTURE; HOST RANGE; INTRON; MOLECULAR EVOLUTION; MULTIGENE FAMILY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PLASMODIUM; PLASMODIUM BERGHEI; PLASMODIUM CHABAUDI; PLASMODIUM COATNEYI; PLASMODIUM CYNOMOLGI; PLASMODIUM FALCIPARUM; PLASMODIUM FIELDI; PLASMODIUM FRAGILE; PLASMODIUM GONDERI; PLASMODIUM HYLOBATI; PLASMODIUM INUI; PLASMODIUM KNOWLESI; PLASMODIUM MALARIAE; PLASMODIUM OVALE; PLASMODIUM REICHENOWI; PLASMODIUM SIMIOVALE; PLASMODIUM VIVAX; PLASMODIUM YOELII; SEQUENCE ALIGNMENT; SERINE REPEAT ANTIGEN MULTIGENE FAMILY; ANIMAL; GENE; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; GENETICS; HAPLORHINI; HUMAN; MOLECULAR GENETICS; PARASITE; PARASITOLOGY; RODENT; SPECIES DIFFERENCE; STATISTICAL MODEL;

MAMMALIA; PLASMODIUM MALARIAE; PLASMODIUM OVALE; PRIMATES; RODENTIA;

PARASITE ANTIGEN; SERINE REPEAT ANTIGEN, PLASMODIUM;

ANIMALS; ANTIGENS, PROTOZOAN; BASE SEQUENCE; EVOLUTION, MOLECULAR; GENE DUPLICATION; GENES, PROTOZOAN; GENETIC VARIATION; HAPLORHINI; HUMANS; LIKELIHOOD FUNCTIONS; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PARASITES; PHYLOGENY; PLASMODIUM; RODENTIA; SPECIES SPECIFICITY; TRANSCRIPTION, GENETIC;

EID: 79952651273     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0017775     Document Type: Article

References (48)

1. Janssen CS, Phillips RS, Turner CM, Barrett MP, (2004) Plasmodium interspersed repeats: the major multigene superfamily of malaria parasites. Nucleic Acids Res 32: 5712-5720.
2. Nei M, Rooney AP, (2005) Concerted and birth-and death evolution of multigene families. Annu Rev Genet 39: 121-152.
3. Gardner MJ, Hall N, Fung E, White O, Berriman M, et al. (2002) Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419: 498-511.
4. Horii T, Shirai H, Jie L, Ishii KJ, Palacpac NQ, et al. (2010) Evidences of protection against blood-stage infection of Plasmodium falciparum by the novel protein vaccine SE36. Parasitol Int 593: 380-386.
5. Okech BA, Nalunkuma A, Okello D, Pang XL, Suzue K, et al. (2001) Natural human immunoglobulin G subclass responses to Plasmodium falciparum serine repeat antigen in Uganda. Am J Trop Med Hyg 65: 912-917.
6. Okech B, Mujuzi G, Ogwal A, Shirai H, Horii T, et al. (2006) 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 74: 191-197.
7. Aoki S, Li J, Itagaki S, Okech BA, Egwang TG, et al. (2002) 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 277: 47533-47540.
8. Inselburg J, Bathurst IC, Kansopon J, Barchfeld GL, Barr PJ, et al. (1993) Protective immunity induced in Aotus monkeys by a recombinant SERA protein of Plasmodium falciparum: adjuvant effects on induction of protective immunity. Infect Immun 61: 2041-2047.
9. Inselburg J, Bathurst IC, Kansopon J, Barr PJ, Rossan R, (1993) 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 61: 2048-2052.
10. Sugiyama T, Suzue K, Okamoto M, Inselburg J, Tai K, et al. (1996) Production of recombinant SERA proteins of Plasmodium falciparum in Escherichia coli by using synthetic genes Vaccine 14: 1069-1076.
11. Delplace P, Fortier B, Tronchin G, Dubremetz JF, Vernes A, (1987) Localization, biosynthesis, processing and isolation of a major 126 kDa antigen of the parasitophorous vacuole of Plasmodium falciparum. Mol Biochem Parasitol 23: 193-201.
12. Debrabant A, Maes P, Delplace P, Dubremetz JF, Tartar A, et al. (1992) Intramolecular mapping of Plasmodium falciparum P126 proteolytic fragments by N-terminal amino acid sequencing. Mol Biochem Parasitol 53: 89-95.
13. Li J, Matsuoka H, Mitamura T, Horii T, (2002) Characterization of proteases involved in the processing of Plasmodium falciparum serine repeat antigen (SERA) Mol Biochem Parasitol 120: 177-186.
14. Li J, Mitamura T, Fox BA, Bzik DJ, Horii T, (2002) Differential localization of processed fragments of Plasmodium falciparum serine repeat antigen and further processing of its N-terminal 47 kDa fragment. Parasitol Int 51: 343-352.
15. Yeoh S, O'Donnell RA, Koussis K, Dluzewski AR, Ansell KH, et al. (2007) Subcellular discharge of a serine protease mediates release of invasive malaria parasites from host erythrocytes. Cell 131: 1072-1083.
16. Arastu-Kapur S, Ponder EL, Fonovic UP, Yeoh S, Yuan F, et al. (2008) Identificartion of proteases that regulate erythrocyte rupture by the malaria parasite Plasmodium falciparum. Nat Chem Biol 4: 203-210.
17. Arisue N, Hirai M, Arai M, Matsuoka H, Horii T, (2007) Phylogeny and evolution of the SERA multigene family in the genus Plasmodium. J Mol Evol 65: 82-91.
18. Escalante AA, Cornejo OE, Freeland DE, Poe AC, Durrego E, et al. (2005) A monkey's tale: the origin of Plasmodium vivax as a human malaria parasite. Proc Natl Acad Sci USA 102: 1980-1985.
19. Hayakawa T, Culleton R, Otani H, Horii T, Tanabe K, (2008) Big bang in the evolution of extant malaria parasites. Mol Biol Evol 25: 2233-2239.
20. Ricklefs RE, Outlaw DC, (2010) A molecular clock for malaria parasites. Science 329: 226-229.
21. Bzik DJ, Li WB, Horii T, Inselburg J, (1988) Amino acid sequence of the serine-repeat antigen (SERA) of Plasmodium falciparum determined from cloned cDNA. Mol Biochem Parasitol 30: 279-288.
22. Hodder AN, Drew DR, Epa VC, Delorenzi M, Bourgon R, et al. (2003) Enzymic, phylogenetic, and structural characterization of the unusual papain-like protease domain of Plasmodium falciparum SERA5. J Biol Chem 278: 48169-48177.
23. Hodder AN, Malby RL, Clarke OB, Fairlie WD, Colman PM, et al. (2009) Structural insights into the protease-like antigen Plasmodium falciparum SERA5 and its noncanonical active-site serine. J Mol Biol 392: 154-65.
24. Garzón-Ospina D, Cadavid LF, Patarroyo MA, (2010) Differential expansion of the merozoite surface protein (msp)-7 gene family in Plasmodium species under a birth-and-death model of evolution. Mol Phylogenet Evol 55: 399-408.
25. Ziegler T, Abegg C, Meijaard E, Perwitasari-Farajallah D, Walter L, et al. (2007) Molecular phylogeny and evolutionary history of Southeast Asian macaques forming the M. silenus group. Mol Phylogenet Evol 42: 807-816.
26. Coatney GR, Collins WE, Warren M, Contacos PG, (1971) The Primate Malarias. Washington DC US Government Printing Office.
27. Mu J, Joy DA, Duan J, Huang Y, Carlton J, et al. (2005) Host switch leads to emergence of Plasmodium vivax malaria in humans. Mol Biol Evol 22: 1686-1693.
28. Fooden J, (1994) Malaria in Macaques. Int J Primatol 15: 573-596.
29. Hayakawa T, Arisue N, Udono T, Hirai H, Sattabongkot J, et al. (2009) Identification of Plasmodium malariae, a human malaria parasite, in imported chimpanzees. PLoS One 4: e7412.
30. Duval L, Nerrienet E, Rousset D, Sadeuh Mba SA, Houze S, et al. (2009) Chimpanzee malaria parasites related to Plasmodium ovale in Africa. PLoS One 4: e5520.
31. Ollomo B, Durand P, Prugnolle F, Douzery E, Arnathau C, et al. (2009) A new malaria agent in African hominids. PLoS Pathog 5: e1000446.
32. Krief S, Escalante AA, Pacheco MA, Mugisha L, André C, et al. (2010) On the diversity of malaria parasites in African apes and the origin of Plasmodium falciparum from Bonobos. PLos Pathog 6: e1000765.
33. Prugnolle F, Durand P, Neel C, Ollomo B, Ayala FJ, et al. (2010) African great apes are natural hosts of multiple related malaria species, including Plasmodium falciparum. Proc Natl Acad Sci USA 107: 1458-1463.
34. Duval L, Fourment M, Nerrienet E, Rousset D, Sadeuh SA, et al. (2010) African apes as reservoirs of Plasmodium falciparum and the origin and diversification of the Laverania subgenus. Proc Natl Acad Sci USA 107: 10561-10566.
35. Liu W, Li Y, Learn GH, Rudicell RS, Robertson JD, et al. (2010) Origin of the human malaria parasite Plasmodium falciparum in gorillas. Nature 467: 420-425.
36. Aly ASI, Matuschewski K, (2005) A malarial cysteine protease is necessary for Plasmodium sporozoite egress from oocysts. J Exp Med 202: 225-230.
37. Palacpac NM, Leung BW, Arisue N, Tanabe K, Sattabongkot J, et al. (2006) Plasmodium vivax serine repeat antigen (SERA) multigene family exhibits similar expression patterns in independent infections. Mol Biochem Parasitol 150: 353-358.
38. Miller SK, Good RT, Drew DR, Delorenzi M, Sanders PR, et al. (2002) A subset of Plasmodium falciparum SERA genes are expressed and appear to play an important role in the erythrocytic cycle. J Biol Chem 277: 47524-47532.
39. Putrianti ED, Schmidt-Christensen A, Arnold I, Heussler VT, Matuschewski K, et al. (2010) 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 12: 725-739.
40. McCoubrie JE, Miller SK, Sargeant T, Good RT, Hodder AN, et al. (2007) Evidence for a common role for the serine-type Plasmodium falciparum serine repeat antigen proteases: Implications for vaccine and drug design. Infect Immun 75: 5565-5574.
41. Pain A, Bohme U, Berry AE, Mungall K, Finn RD, et al. (2008) The genome of the simian and human malaria parasite Plasmodium knowlesi. Nature 455: 799-803.
42. Chen X, Wu R, (1997) Direct amplification of unknown genes and fragments by Uneven polymerase chain reaction. Gene 185: 195-199.
43. Thompson JD, Higgins DG, Gibson TJ, (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22: 4673-4680.
44. Tamura K, Dudley J, Nei M, Kumar S, (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24: 1596-1599.
45. Felsenstein J, (1996) Inferring phylogenies from protein sequences by parsimony, distance, and likelihood methods. Methods Enzymol 266: 418-427.
46. Jones DT, Taylor WR, Thornton JM, (1992) The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8: 275-282.
47. Yang Z, (1997) PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci 13: 555-556.
48. Yang Z, (2007) PAML 4: a program package for phylogenetic analysis by maximum likelihood. Mol Biol Evol 24: 1586-1591.