Adaptive radiation within the vaccine target tetraspanin-23 across nine Schistosoma species from Africa

International Journal for Parasitology

Volumn 43, Issue 1, 2013, Pages 95-103

  Sealey, Katie L ^a,b   Kirk, Ruth S ^a   Walker, Anthony J ^a   Rollinson, David ^b   Lawton, Scott P ^a  

^a KINGSTON UNIVERSITY   (United Kingdom)

^b DEPARTMENT OF LIFE SCIENCES   (United Kingdom)

Author keywords

Antigenicity; Polymorphism; Positive selection; Schistosoma; Tetraspanin 23

Indexed keywords

DNA; TETRASPANIN; TETRASPANIN 23; UNCLASSIFIED DRUG;

ADAPTIVE RADIATION; ANTIGEN; DNA; DRUG DEVELOPMENT; FLATWORM; PHYLOGENETICS; POLYMORPHISM; VACCINE;

ADAPTIVE RADIATION; AFRICA; ANTIGENICITY; ARTICLE; DNA SEQUENCE; EVOLUTION; GENETIC POLYMORPHISM; GENETIC SELECTION; GENETIC VARIABILITY; HOST PARASITE INTERACTION; HOST RANGE; IMMUNE SYSTEM; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PROTEIN STRUCTURE; SCHISTOSOMA; SCHISTOSOMA BOVIS; SCHISTOSOMA CURASSONI; SCHISTOSOMA GUINEENSIS; SCHISTOSOMA HEMATOBIUM; SCHISTOSOMA INTERCALATUM; SCHISTOSOMA MANSONI; SCHISTOSOMA MARGREBOWIEI; SCHISTOSOMA MATTHEEI; SCHISTOSOMA RODHAINI; SPECIES DIFFERENCE;

AFRICA; ANIMALS; CLUSTER ANALYSIS; EVOLUTION, MOLECULAR; HELMINTH PROTEINS; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYMORPHISM, GENETIC; SCHISTOSOMA; SELECTION, GENETIC; SEQUENCE ANALYSIS, DNA; TETRASPANINS;

AFRICA;

SCHISTOSOMA; SCHISTOSOMA BOVIS; SCHISTOSOMA CURASSONI; SCHISTOSOMA GUINEENSIS; SCHISTOSOMA HAEMATOBIUM; SCHISTOSOMA INTERCALATUM; SCHISTOSOMA MANSONI; SCHISTOSOMA MARGREBOWIEI; SCHISTOSOMA MATTHEEI; SCHISTOSOMA RODHAINI;

EID: 84872394464     PISSN: 00207519     EISSN: 18790135     Source Type: Journal    
DOI: 10.1016/j.ijpara.2012.11.007     Document Type: Article

References (44)

1. Berriman M., Haas B.J., LoVerde P.T., Wilson R.A., Dillon G.P., Cerqueira G.C., Mashiyama S.T., Al-Lazikani B., Andrade L.F., Ashton P.D., Aslett M.A., Bartholomeu D.C., Blandin G., Caffrey C.R., Coghlan A., Coulson R., Day T.A., Delcher A., DeMarco R., Djikeng A., Eyre T., Gamble J.A., Ghedin E., Gu Y., Hertz-Fowler C., Hirai H., Hirai Y., Houston R., Ivens A., Johnston D.A., Lacerda D., Macedo C.D., McVeigh P., Ning Z., Oliveira G., Overington J.P., Parkhill J., Pertea M., Pierce R.J., Protasio A.V., Quail M.A., Rajandream M.A., Rogers J., Sajid M., Salzberg S.L., Stanke M., Tivey A.R., White O., Williams D.L., Wortman J., Wu W., Zamanian M., Zerlotini A., Fraser-Liggett C.M., Barrell B.G., El-Sayed N. The genome of the blood fluke Schistosoma mansoni. Nature 2009, 460:352-358.
2. Bhoora R., Quan M., Matjila P.T., Zweygarth E., Guthrie A.J., Collins N.E. Sequence heterogenity in the equi merozoite antigen gene (ema-1) of Theileria equi and the development of an ema-1-specific TaqMan MGB™ assay for the detection of T. equi. Vet. Parasitol. 2010, 172:33-45.
3. Cai P., Bu L.Y., Wang J.A., Wang Z.S., Zhong X.A., Wang H. Molecular characterization of Schistosoma japonicum tegument protein tetraspanin-2: sequence variation and possible implications for immune evasion. Biochem. Biophys. Res. Comm. 2008, 372:197-202.
4. Chow C., Gauci C.G., Vural G., Jenkins D.J., Heath D.D., Rosenzvit M.C., Harandi M.F., Lightowlers M.W. Echinococcus granulosus: variability of the host protective EG95 vaccine antigen in G6 and G7 geneotypic variants. Exp. Parasitol. 2008, 119:499-505.
5. Cupit P.M., Steinauer M.L., Tonnessen B.W., Agola L.E., Kinuthia J.M., Mwangi I.N., Mutuka M.W., Mkoji G.M., Loker E.S., Cunningham C. Polymorphism associated within Schistosoma mansoni tetraspanin-2 gene. Int. J. Parasitol. 2011, 41:1249-1252.
6. Da'Dara A.A., Li Y.S., Xiong T., Zhou J., Williams G.M., McManus D.P., Feng Z., Yu X.L., Gray D.J., Harn D.A. DNA-based vaccine protect against zoonotic schistosomiasis in water buffalo. Vaccine 2008, 26:3617-3625.
7. Dunne D.W., Cooke A. A worm's eye view of the immune system: consequences for evolution of human autoimmune disease. Nat. Rev. Immunol. 2005, 5:420-426.
8. Emery A.E., Allan F.E., Rabone M.E., Rollinson D. Schistosomiasis collection at NHM (SCAN). Parasites Vectors 2012, 5:185.
9. Fallon P.G., Doenhoff M.J. Drug-resistance schistosomiasis: resistance to praziquantel and oxamniquine induced in Schistosoma mansoni in mice is drug specific. Am. J. Trop. Med. Hyg. 1994, 51:83-88.
10. Fenwick A., Webster J.P. Schistosomiasis: challenges for control, treatment and drug resistance. Curr. Opin. Infect. Dis. 2006, 19:577-582.
11. Goni N., Fajoardo A., Moratorio G., Colina R., Cristina J. Modeling gene sequences over time in 2009 H1N1 Influenza A virus populations. Virol. J. 2009, 6:215.
12. Hall T.A. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids. Symp. Ser. 1999, 41:95-98.
13. Harn D.A., Mitsuyama M., Huguenel E.D., David J.R. Schistosoma mansoni: detection by monoclonal antibody of a 22,000-dalton surface membrane antigen which may be blocked by host molecules on lung stage parasites. J. Immunol. 1985, 135:2115-2120.
14. Inal J., Bickle Q. Sequence and immunogenicity of the 23-kDa transmembrane antigen of Schistosoma haematobium. Mol. Biochem. Parasitol. 1995, 74:217-221.
15. Ismail M., Botros S., Metwally A., William S., Farghally A., Tao L.F., Day T.A., Bennett J.L. Resistance to praziquantel: direct evidence from Schistosoma mansoni isolated from Egyptian villagers. Am. J. Trop. Med. Hyg. 1999, 60:932-935.
16. Jiang N., Cai P., Yin J., Hao L., Lu H., Wang X., Wang H., Chen Q. Characterization of antibody responses to the Sj23 antigen of Schistosoma japonicum after infection and immunisation. Acta Trop. 2010, 116:9-14.
17. Kiss I., Gyarmati P., Zohari S., Ramsey K.W., Metreveli G., Weiss E., Brytting M., Stivers M., Lindstrom S., Lundkvist A., Nemirov K., Thoren P., Berg M., Czifra G., Belak S. Molecular characterization of highly pathogenic H5N1 avian influenza viruses isolated in Sweden in 2006. Virol. J. 2008, 5:113.
18. Kolaskar A.S., Tongaonkar P.C. A semi-empirical method for prediction of antigenic determinants on protein antigens. FEBS Lett. 1990, 276:172-174.
19. Kolvalenko O.V., Metcalf D.G., DeGrado W.F., Hemler M.E. Structural organisation and interactions of transmembrane domains in tetraspanin proteins. BMC Struct. Biol. 2005, 5:11.
20. Kong Y., Chung J., Yun D., Kim L., Kang S., Ito A., Ma L., Cho S. Variation of antigenic proteins of eggs and developmental stages of Paragonimus westermani. Korean J. Parasitol. 1997, 35:197-202.
21. Lawton S.P., Hirai H., Ironside J.E., Johnston D.A., Rollinson D. Genomes and geography: genomic insights into the evolution and phylogeography of the genus Schistosoma. Parasites Vectors 2011, 4:131.
22. Lewis-Rodgers N., McClellan D.A., Crandall K.A. The evolution of foot-and-mouth disease virus: impacts of recombination and selection. Infect. Genet. Evol. 2008, 8:786-798.
23. Librado P., Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009, 25:1451-2452.
24. Liu F., Zhou Y., Wang Z.Q., Lu G., Zheng H., Brindley P.J., McManus D.P., Blair D., Zhang Q.H., Zhong Y., Wang S., Han Z.G., Chen Z. The Schistosoma japonicum genome reveals features of host-parasite interplay. Nature 2009, 460:345-351.
25. Maass D.R., Harrison G.B., Grant W.N., Hein W.R., Shoemaker C.B. Intraspecific epitopic variation in carbohydrate antigen exposed on the surface of Trichostrongylous colubriformis infective L3 larvae. PLoS Pathog. 2009, 5:e1000597.
26. McManus D.P. Prospects for development of a transmission blocking vaccine against Schistosoma japonicum. Parasite Immunol. 2005, 27:297-308.
27. McManus D.P., Loukas A. Current status of vaccines for schistosomiasis. Clin. Micro. 2008, 21:225-242.
28. Melman S.D., Steinauer M.L., Cunningham C., Kubatko L.S., Mwangi I.N., Wynn N.B., Mutuku M.W., Karanja D.M., Colley D.G., Black C.L., Secor W.E., Mkoji G.M., Loker E.S. Reduced susceptibility to praziquantel among naturally occurring Kenyan isolates of Schistosoma mansoni. PLoS Neg. Trop. Dis. 2009, 3:e504.
29. Nei M. Molecular Evolutionary Genetics 1987, Columbia Univ. Press, New York.
30. Orjuela-Sanchez P., Da Silva-Nunes M., Da Silva N.S., Scopel K.K.G., Goncalves R.M., Malafronte R.S., Ferreira M.U. Population dynamics of genetically diverse Plasmodium falciparum lineages: community-based prospective study in rural Amazonia. Parasitology 2009, 136:1097-1105.
31. Rodgers E., Grunau C., Pierce R.J., Hirai H., Gourbal B., Galinier R., Emans R., Cesari I.M., Mitta G. Controlled chaos of polymorphic mucins in a metazoan parasite (Schistosoma mansoni) interacting with its invertebrate host (Biomphalaria glabrata). PLoS Neg. Trop. Dis. 2008, 2:e330.
32. Rollinson D., Southgate V.R. The genus Schistosoma: a taxonomic appraisal. The Biology of Schistosomes: From Genes to Latrines 1987, 1-49. Academic Press, London. D. Rollinson, A.J.G. Simpson (Eds.).
33. Sawai H., Otani H., Arisue N., Palacpac N., de Oliveira Martins L., Pathirana S., Handunnetti S., Kawai S., Kishino H., Horii T., Tanabe K. Lineage-specific positive selection at the merozoite surface protein 1 (msp1) locus of Plasmodium vivax and related simian malaria parasites. BMC Evol. Biol. 2010, 10:52.
34. Sepulveda J., Tremblay J.M., DeGnore J.P., Skelly P.J., Shoemaker C.B. Schistosoma mansoni host exposed surface antigens characterised by sera and recombinant antibodies from schistosomiasis - resistant rats. Int. J. Parasitol. 2010, 40:1407-1417.
35. Steinmann P., Keiser J., Bos R., Tanner M., Utzinger J. Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infect. Dis. 2006, 6:411-425.
36. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: Molecular Evolutionary Genetics Analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011, 28:2731-2739.
37. Thiele E.A., Sorensen R.E., Gazzinelli A., Minchella D.J. Genetic diversity and population structuring of Schistosoma mansoni in a Brazilian village. Int. J. Parasitol. 2008, 38:389-399.
38. Walker A.J. Insights into the functional biology of schistosomes. Parasites Vectors 2011, 4:203.
39. Webster B.L., Southgate V.R., Littlewood T.J. A revision of the interrelationships of Schistosoma including the recently described Schistosoma guineensis. Int. J. Parasitol. 2006, 36:947-955.
40. Wilson R.A., Coulson P.S. Schistosome vaccines: a critical appraisal. Mem. Inst. Oswaldo Cruz. 2006, 101:13-20.
41. Wu C., Cai P., Chang Q., Hao L., Peng S., Sun X., Lu H., Yin J., Jiang N., Chen Q. Mapping the binding between tetraspanin molecule (Sjc23) of Schistosoma japonicum and human non-immune IgG. PLoS One 2011, 6:e19112.
42. Yuan C., Fu Y., Li J., Yue Y., Cai L., Xiao W., Chen J., Yang L. Schistosoma japonicum: efficient and rapid purification of the tetraspanin extracellular loop 2, a potential protective antigen against schistosomiasis in mammalian. Exp. Parasitol. 2010, 126:456-461.
43. Zhao J., Yan X., Chai X., Martella V., Luo G., Zhang H., Gao H., Liu Y., Bai X., Zhang L., Chen T., Xu L., Zhao C., Wang F., Shao X., Wu W., Cheng S. Phylogenetic analysis of the haemagglutinin gene of canine distemper virus strains detected from breeding foxes, raccoon dogs and minks in China. Vet. Microbiol. 2010, 140:34-42.
44. Zhang M., Li J., Duke M., Jones M.K., Kuang L., Zhang J., Blair D., Li Y., McManus D.P. Inconsistent protective efficacy and marked polymorphism limits the value of Schistosoma japonicum Tetraspanin-2 as a vaccine target. PLoS Neg. Trop. Dis. 2011, 5:5.