A new method for isolation of purified genomic DNA from haemosporidian parasites inhabiting nucleated red blood cells

Experimental Parasitology

Volumn 133, Issue 3, 2013, Pages 275-280

  Palinauskas, Vaidas ^a   KriŽanauskiene, Asta ^a   Iezhova, Tatjana A ^a   Bolshakov, Casimir V ^b   Jönsson, Jane ^c   Bensch, Staffan ^c   Valkiunas, Gediminas ^a  

^a VILNIUS UNIVERSITY   (Lithuania)

^b Zoological Institute   (Russian Federation)

^c LUND UNIVERSITY   (Sweden)

Author keywords

Avian malaria; DNA purification; Haemoproteus tartakovskyi; Haemosporidians; HSISKIN1; Next generation sequencing; Template

Indexed keywords

GENOMIC DNA;

ARTICLE; BIRD; CELL NUCLEUS; CENTRIFUGATION; CONTROLLED STUDY; DNA ISOLATION; DNA PURIFICATION; ERYTHROCYTE; EXFLAGELLATE; FLAGELLATE; GAMETOCYTE; HAEMOPROTEUS TARTAKOVSKYI; HAEMOSPORIDA; HOST CELL; IN VITRO STUDY; MICROGAMETE; NONHUMAN; NUCLEATED ERYTHROCYTE; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL;

ANIMALS; BIRD DISEASES; CELL NUCLEUS; DNA, PROTOZOAN; ELECTROPHORESIS, AGAR GEL; ERYTHROCYTES; GENOME, PROTOZOAN; HAEMOSPORIDA; PASSERIFORMES; POLYMERASE CHAIN REACTION; PROTOZOAN INFECTIONS, ANIMAL; SEQUENCE ANALYSIS, DNA;

AVES; HAEMOPROTEUS; HAEMOSPORIDA; MAMMALIA; PLASMODIUM (APICOMPLEXA); REPTILIA; SQUAMATA; VERTEBRATA;

EID: 84872423541     PISSN: 00144894     EISSN: 10902449     Source Type: Journal    
DOI: 10.1016/j.exppara.2012.12.003     Document Type: Article

References (46)

1. Arabidopsis Genome Initiative T. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 2000, 408:796-815.
2. Arai M., Billker O., Morris H.R., Panico M., Delcroix M., Dixon D., Ley S.V., Sinden R.E. Both mosquito-derived xanthurenic acid and a host blood-derived factor regulate gametogenesis of Plasmodium in the midgut of the mosquito. Mol. Biochem. Parasitol. 2001, 116:17-24.
3. Austin C.C., Perkins S.L. Parasites in a biodiversity hotspot: a survey of hematozoa and a molecular phylogenetic analysis of Plasmodium in New Guinea skinks. J. Parasitol. 2006, 92:770-777.
4. Ball G.H. In vitro culture of the mosquito phase of avian malaria. J. Parasitol. 1964, 50:3-10.
5. Ball G.H., Chao J. Infectivity to canaries of sporozoites of Plasmodium relictum developing in vitro. J. Parasitol. 1961, 47:787-790.
6. Beadell J.S., Ishtiaq F., Covas R., Melo M., Warren B.H., Atkinson C.T., Bensch S., Graves G.R., Jhala Y.V., Peirce M.a., Rahmani A.R., Fonseca D.M., Fleischer R.C. Global phylogeographic limits of Hawaii's avian malaria. Proc. R. Soc. Lond. B: Biol. Sci. 2006, 273:2935-2944.
7. Bensch S., Stjernman M., Hasselquist D., Ostman O., Hansson B., Westerdahl H., Pinheiro R.T. Host specificity in avian blood parasites: a study of Plasmodium and Haemoproteus mitochondrial DNA amplified from birds. Proc. R. Soc. Lond. B: Biol. Sci. 2000, 267:1583-1589.
8. Bensch S., Pérez-Tris J., Waldenström J., Hellgren O. Linkage between nuclear and mitochondrial DNA sequences in avian malaria parasites: multiple cases of cryptic speciation?. Evolution 2004, 58:1617-1621.
9. Bensch S., Hellgren O., Pérez-Tris J. MalAvi: a public database of malaria parasites and related haemosporidians in avian hosts based on mitochondrial cytochrome b lineages. Mol. Ecol. Resour. 2009, 9:1353-1358.
10. Carlton J.M., Angiuoli S.V., Suh B.B., Kooij T.W., Pertea M., Silva J.C., Ermolaeva M.D., Allen J.E., Selengut J.D., Koo H.L., Peterson J.D., Pop M., Kosack D.S., Shumway M.F., Bidwell S.L., Shallom S.J., van Aken S.E., Riedmuller S.B., Feldblyum T.V., Cho J.K., Quackenbush J., Sedegah M., Shoaibi A., Cummings L.M., Florens L., Yates J.R., Raine J.D., Sinden R.E., Harris M.A., Cunningham D.A., Preiser P.R., Bergman L.W., Vaidya A.B., van Lin L.H., Janse C.J., Waters A.P., Smith H.O., White O.R., Salzberg S.L., Venter J.C., Fraser C.M., Hoffman S.L., Gardner M.J., Carucci D.J. Genome sequence and comparative analysis of the model rodent malaria parasite Plasmodium yoelii yoelii. Nature 2002, 419:512-519.
11. Carlton J., Silva J., Hall N. The genome of model malaria parasites, and comparative genomics. Curr. Issues Mol. Biol. 2005, 7:23-37.
12. Coatney, G.R., Cooper, W.C., Eddy, N.B., Greenbeeg, J., 1953. Survey of Antimalarial Agents. Chemotherapy of Plasmodium gallinaceum Infections; Toxicity; Correlation of Structure and Action, 9th ed. Public Health Monograph, Washington.
13. Davey D.G. Chemotherapy of malaria. Brit. Med. Bull. 1951, 8.
14. DeBarry J.D., Kissinger J.C. Jumbled genomes: missing Apicomplexan synteny. Mol. Biol. Evol. 2011, 28:2855-2871.
15. Gardner M.J., Hall N., Fung E., White O., Berriman M., Hyman R.W., Carlton J.M., Pain A., Nelson K.E., Bowman S., Paulsen I.T., James K., Eisen J.A., Rutherford K., Salzberg S.L., Craig A., Kyes S., Chan M.-S., Nene V., Shallom S.J., Suh B., Peterson J., Angiuoli S., Pertea M., Allen J., Selengut J., Haft D., Mather M.W., Vaidya A.B., Martin D.M.A., Fairlamb A.H., Fraunholz M.J., Roos D.S., Ralph S.A., McFadden G.I., Cummings L.M., Subramanian G.M., Mungall C., Venter J.C., Carucci D.J., Hoffman S.L., Newbold C., Davis R.W., Fraser C.M., Barrell B. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 2002, 419:498-511.
16. Garnham P.C.C. Malaria Parasites and Other Haemosporidia 1966, Blackwell Scientific Publications Ltd., Oxford.
17. Godfrey R.D., Fedynich A.M., Pence D.B. Quantification of hematozoa in blood smears. J. Wildl. Dis. 1987, 23:558-565.
18. Graczyk T.K., Cranfield M.R., Shiff C.J. Extraction of Haemoproteus columbae (Haemosporina: Haemoproteidae) antigen from rock dove pigeons (Columba livia) and its use in an antibody ELISA. J. Parasitol. 1994, 80:713-718.
19. Hall, A., 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program of Windows 95/98/NT. in: Nucleic Acids Symp. Ser., pp. 95-98.
20. Hellgren O., Waldenström J., Bensch S. A new PCR assay for simultaneous studies of Leucocytozoon, Plasmodium, and Haemoproteus from avian blood. J. Parasitol. 2004, 90:797-802.
21. Janssen C.S., Barrett M.P., Lawson D., Quail M.A., Harris D., Bowman S., Phillips R.S., Turner C.M.R. Gene discovery in Plasmodium chabaudi by genome survey sequencing. Mol. Biochem. Parasitol. 2001, 113:251-260.
22. Knowles S.C.L., Palinauskas V., Sheldon B.C. Chronic malaria infections increase family inequalities and reduce parental fitness: experimental evidence from a wild bird population. J. Evol. Biol. 2010, 23:557-569.
23. Lander E.S., Linton L.M., Birren B., Nusbaum C., Zody M.C., et al. Initial sequencing and analysis of the human genome. Nature 2001, 409:860-921.
24. Levin I.I., Outlaw D.C., Vargas F.H., Parker P.G. Plasmodium blood parasite found in endangered Galapagos penguins (Spheniscus mendiculus). Biol. Conserv. 2009, 142:3191-3195.
25. Margulies M., Egholm M., Altman W.E., Attiya S., Bader J.S., et al. Genome sequencing in microfabricated high-density picolitre reactors. Nature 2005, 437:376-380.
26. Martinsen E.S., Perkins S.L., Schall J.J. A three-genome phylogeny of malaria parasites (Plasmodium and closely related genera): evolution of life-history traits and host switches. Mol. Phylogenet. Evol. 2008, 47:261-273.
27. Marzal A., Ricklefs R.E., Valkiūnas G., Albayrak T., Arriero E., Bonneaud C., Czirják G.A., Ewen J., Hellgren O., Hořáková D., Iezhova T.A., Jensen H., KriŽanauskiene A., Lima M.R., de Lope F., Magnussen E., Martin L.B., Møller A.P., Palinauskas V., Pap P.L., Pérez-Tris J., Sehgal R.N.M., Soler M., Szöllosi E., Westerdahl H., Zetindjiev P., Bensch S. Diversity, loss, and gain of malaria parasites in a globally invasive bird. PLoS ONE 2011, 6:e21905.
28. McGhee R.B., Singh S.D., Weathersby A.B. Plasmodium gallinaceum: vaccination in chickens. Exp. Parasitol. 1977, 43:231-238.
29. Outlaw D.C., Ricklefs R.E. Comparative gene evolution in haemosporidian (Apicomplexa) parasites of birds and mammals. Mol. Biol. Evol. 2010, 27:537-542.
30. Pain A., Böhme U., Berry A.E., Mungall K., Finn R.D., et al. The genome of the simian and human malaria parasite Plasmodium knowlesi. Nature 2008, 455:799-803.
31. Palinauskas V., Valkiūnas G., Bolshakov C.V., Bensch S. Plasmodium relictum (lineage P-SGS1): effects on experimentally infected passerine birds. Exp. Parasitol. 2008, 120:372-380.
32. Palinauskas V., Dolnik O.V., Valkiūnas G., Bensch S. Laser microdissection microscopy and single cell PCR of avian hemosporidians. J. Parasitol. 2010, 96:420-424.
33. Perkins S.L. Species concepts and malaria parasites: detecting a cryptic species of Plasmodium. Proc. R. Soc. Lond. B: Biol. Sci. 2000, 267:2345-2350.
34. Perkins S.L. Molecular systematics of the three mitochondrial protein-coding genes of malaria parasites: corroborative and new evidence for the origins of human malaria. Mitochondr. DNA 2008, 19:471-478.
35. Pick C., Ebersberger I., Spielmann T., Bruchhaus I., Burmester T. Phylogenomic analyses of malaria parasites and evolution of their exported proteins. BMC Evol. Biol. 2011, 11:167.
36. Ricklefs R.E., Outlaw D.C. A molecular clock for malaria parasites. Science 2010, 329:226-229.
37. Ricklefs R.E., Fallon S.M., Bermingham E. Evolutionary relationships, cospeciation, and host switching in avian malaria parasites. Syst. Biol. 2004, 53:111-119.
38. Sinden R.E. Gametogenesis and sexual development. Malaria: Parasite Biology, Pathogenesis, and Protection 1998, 25-48. American Society for Microbiology Press, Washington, DC. I.W. Sherman (Ed.).
39. Trager W. Studies on the extracellular cultivation of an intracellular parasite (avian malaria). I. Development of the organisms in erythrocyte extracts, and the favoring effect of adenosinetriphosphate. J. Exp. Med. 1950, 92:349-366.
40. Valkiūnas G. Avian Malaria Parasites and Other Haemosporidia 2005, CRC Press, America.
41. Valkiūnas G., Iezhova T.A., KriŽanauskiene A., Palinauskas V., Bensch S. In vitro hybridization of Haemoproteus spp.: an experimental approach for direct investigation of reproductive isolation of parasites. J. Parasitol. 2008, 94:1385-1394.
42. Valkiūnas G., Iezhova T., KriŽanauskiene A.A., Palinauskas V., Sehgal R.N.M., Bensch S. A comparative analysis of microscopy and PCR-based detection methods for blood parasites. J. Parasitol. 2008, 94:1395-1401.
43. Valkiūnas G., Palinauskas V., Asta KriŽanauskiene A., Bernotiene R., Rita Kazlauskiene R., Iezhova T.A. Further observations on in vitro hybridization of hemosporidian parasites: patterns of ookinete development in Haemoproteus spp. J. Parasitol. 2012, 10.1645/GE-3226.1.
44. Waltari E., Edwards S.V. Evolutionary dynamics of intron size, genome size, and physiological correlates in archosaurs. Am. Nat. 2002, 160:539-552.
45. Warren W.C., Clayton D.F., Ellegren H., Arnold A.P., Hillier L.W., et al. The genome of a songbird. Nature 2010, 464:757-762.
46. Zehtindjiev P., KriŽanauskiene A., Bensch S., Palinauskas V., Asghar M., Dimitrov D., Scebba S., Valkiūnas G. A new morphologically distinct avian malaria parasite that fails detection by established polymerase chain reaction-based protocols for amplification of the cytochrome B gene. J. Parasitol. 2012, 98:657-665.