SL1 RNA gene recovery from Enterobius vermicularis ancient DNA in pre-Columbian human coprolites

International Journal for Parasitology

Volumn 36, Issue 13, 2006, Pages 1419-1425

  Iñiguez, Alena Mayo ^a   Reinhard, Karl ^b   Carvalho Gonçalves, Marcelo Luiz ^a   Ferreira, Luiz Fernando ^a   Araújo, Adauto ^a   Paulo Vicente, Ana Carolina ^a  

^a INSTITUTO OSWALDO CRUZ   (Brazil)

^b UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

5S rRNA spacer; Ancient DNA; Coprolites; Enterobius vermicularis; Paleoparasitology; Polymerase chain reaction; Splicing leader RNA gene

Indexed keywords

ANTIGEN; ANTIGEN SM; DNA; RNA; RNA 5S; UNCLASSIFIED DRUG;

COPROLITE; EVOLUTIONARY THEORY; GENE EXPRESSION; GENETIC ANALYSIS; HUNTER-GATHERER; MOLECULAR ANALYSIS; NEMATODE; POLYMORPHISM; RNA; SOCIOECONOMIC CONDITIONS;

ANTIGEN BINDING; ARCHEOLOGY; ARTICLE; BINDING SITE; CHILE; CONTROLLED STUDY; ENTEROBIUS VERMICULARIS; GENETIC ANALYSIS; GENETIC POLYMORPHISM; MICROSCOPY; MOLECULAR EVOLUTION; NONHUMAN; NORTH AMERICA; NUCLEOTIDE SEQUENCE; PARASITOLOGY; RNA GENE; RNA SEQUENCE; RNA STRUCTURE; SEQUENCE ANALYSIS; SOUTH AMERICA;

ANIMALS; BASE SEQUENCE; DNA, HELMINTH; ENTEROBIASIS; ENTEROBIUS; HISTORY, ANCIENT; HUMANS; MOLECULAR SEQUENCE DATA; PALEOPATHOLOGY; POLYMERASE CHAIN REACTION; RNA, HELMINTH; RNA, SPLICED LEADER; SEQUENCE ANALYSIS, DNA;

ANTOFAGASTA; CHILE; NORTH AMERICA; SAN PEDRO DE ATACAMA; SOUTH AMERICA; TULAN;

ENTEROBIUS VERMICULARIS; VERMES;

EID: 33749358015     PISSN: 00207519     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpara.2006.07.005     Document Type: Article

References (66)

1. Araujo A., Ferreira L.F., Confalonieri U.E., Nunez L., Ribeiro, and Filho B.M. The finding of Enterobius vermicularis eggs in pre-Columbian human coprolites. Mem. Inst. Oswaldo Cruz 80 (1985) 141-143
2. Araujo A., and Ferreira L.F. Paleoparasitology and antiquity of human host-parasite relationships. Mem. Inst. Oswaldo Cruz 95 (2000) 89-93
3. Aufderheide A.C., Salo W., Madden M., Streitz J., Buikstra J., Guhl F., Arriaza B., Renier C., Wittmers Jr. L.E., Fornaciari G., and Allison M. A 9000-year record of Chagas' disease. Proc. Natl. Acad. Sci. USA 101 (2004) 2034-2039
4. Blaxter M., and Liu L. Nematode spliced leaders: ubiquity, evolution and utility. Int. J. Parasitol. 26 (1996) 1025-1036
5. Bouchet F., Guidon N., Katharina D., Harter S., Ferreira L.F., Chaves S.M., Reinhard K., and Araujo A. Parasite remains in archaeological sites. Mem. Inst. Oswaldo Cruz 98 (2003) 47-52
6. Brown T.A., and Brown K.A. Ancient DNA using molecular biology to explore the past. BioEssays 16 (1994) 719-726
7. Callen E.O., and Cameron T.W.M. A prehistoric diet as revealed in coprolites. New Scientist 8 (1960) 35-40
8. Crubézy E., Ludes B., Poveda J.-D., Clayton J., Crouau-Roy B., and Montagnon D. Identification of Mycobacterium DNA in an Egyptian Pott's disease of 5400 years old. C. R. Acad. Sci. III 321 (1998) 941-951
9. Dassanayake R.S., Chandrasekharan N.V., and Karunanayake E.H. Trans-spliced leader RNA, 5S-rRNA genes and novel variant orphan spliced-leader of the lymphatic filarial nematode Wuchereria bancrofti, and a sensitive polymerase chain reaction based detection assay. Gene 269 (2001) 185-193
10. Denker J.A., Maroney P.A., Yu Y.T., Kanost R.A., and Nilsen T.W. Multiple requirements for nematode spliced leader RNP function in trans-splicing. RNA 2 (1996) 746-755
11. Donoghue H.D., Holton J., and Spigelman M. PCR primers that can detect low levels of Mycobacterium leprae DNA. J. Med. Microbiol. 50 (2001) 177-182
12. Drancourt M., and Raoult D. Palaeomicrobiology: current issues and perspectives. Nat. Rev. Microbiol. 3 (2005) 23-35
13. Drancourt M., Roux V., Dang L.V., Tran-Hung L., Castex D., Chenal-Francisque V., Ogata H., Fournier P.E., Crubézy E., and Raoult D. Genotyping, Orientalis-like Yersinia pestis, and plague pandemics. Emerg. Infect. Dis. 10 (2004) 1585-1592
14. Evans D., Zorio D., MacMorris M., Winter C.E., Lea K., and Blumenthal T. Operons and SL2 trans-splicing exist in nematodes outside the genus Caenorhabditis. Proc. Natl. Acad. Sci. USA 94 (1997) 9751-9756
15. Evans D., and Blumenthal T. Trans-splicing of polycistronic Caenorhabditis elegans pre-mRNAs: analysis of the SL2 RNA. Mol. Cell. Biol. 20 (2000) 6659-6667
16. Favia G., Bazzocchi C., Cancrini G., Genchi C., and Bandi C. Unusual organization of the 5S ribosomal spacer in Dirofilaria repens: absence of a canonical spliced leader 1 sequence. Parasitol. Res. 86 (2000) 497-499
17. Ferguson K.C., and Rothman J.H. Alterations in the conserved SL1 trans-spliced leader of Caenorhabditis elegans demonstrate flexibility in length and sequence requirements in vivo. Mol. Cell. Biol. 19 (1999) 1892-1900
18. Ferreira L.F., Araujo A., Confalonieri U., and Chame M. Enterobius vermicualris infection in pre-Columbian population from San Pedro de Atacama, Chile. Mem. Inst. Oswaldo Cruz 84 (1989) 197-199
19. Ferreira L.F., Reinhard K.J., Araújo A., and Coura L.C. Paleoparasitology of oxyuriasis. Ann. Acad. Nac. Med. 157 (1997) 20-24
20. Ferreira L.F., Britto C., Cardoso M.A., Fernandes O., Reinhard K., and Araújo A. Paleoparasitology of Chagas disease revealed by infected tissues from Chilean mummies. Acta Trop. 75 (2000) 79-84
21. Fry G.F., and Hall H.J. Parasitological examination of prehistoric human coprolites from Utah. Proc. Utah Acad. Sci. Art Lett. 46 (1969) 127-154
22. Golenberg E.M., Bickel A., and Weihs P. Effect of highly fragmented DNA on PCR. Nucleic Acids Res. 24 (1996) 5026-5033
23. Gonçalves M.L.C., Araujo A., and Ferreira L.F. Human intestinal parasites in the past: new findings and a review. Mem. Inst. Oswaldo Cruz 98 (2003) 103-118
24. Guhl F., Jaramillo C., Vallejo G.A., Yockteng R., Cardenas-Arroyo F., Fornaciari G., Arriaza B., and Aufderheide A.C. Isolation of Trypanosoma cruzi DNA in 4000-year-old mummified human tissue from northern Chile. Am. J. Phys. Anthropol. 108 (1999) 401-407
25. Haas C.J., Zink A., Palfi G., Szeimies U., and Nerlich A.G. Detection of leprosy in ancient human skeletal remains by molecular identification of Mycobacterium leprae. Am. J. Clin. Pathol. 114 (2000) 428-436
26. Handt O., Krings M., Ward R.H., and Pääbo S. The retrieval of ancient human DNA sequences. Am. J. Hum. Genet. 59 (1996) 368-376
27. Herrmann B. Parasitologisch-epidemiologische auswertungen mittelalterlicher kloaken. Z Archaol. Mittelalters 13 (1985) 131-161
28. Herrmann B., and Hummel S. Ancient DNA: Recovery and Analysis of Genetic Material from Paleontological, Archaeological, Museum, Medical, and Forensic Specimens (1994), Springer-Verlag, New York
29. Higuchi R., Bowman B., Freiberger M., Ryder O.A., and Wilson A.C. DNA sequences from the quagga, an extinct member of the horse family. Nature 312 (1984) 282-284
30. Hofreiter M., Serre D., Poinar H.N., Kuch M., and Pääbo S. Ancient DNA. Nat. Rev. Genet. 2 (2001) 353-359
31. Hofreiter M., Jaenicke V., Serre D., Haeseler A.V.A., and Pääbo S. DNA sequences from multiple amplifications reveal artifacts induced by cytosine deamination in ancient DNA. Nucleic Acids Res. 29 (2001) 4793-4799
32. Horne P.D.J. First evidence of enterobiasis in ancient Egypt. Parasitology 88 (2002) 1019-1021
33. Hugot J.P., Reinhard K.J., Gardner S.L., and Morand S. Human enterobiases in evolution: origin, specificity e transmission. Parasite 6 (1999) 201-208
34. Iniguez A.M., Vicente A.C.P., Araújo A., Ferreira L.F., and Reinhard K.J. Enterobius vermicularis: specific detection by amplification of an internal region of 5S ribosomal RNA intergenic spacer and trans-splicing leader RNA analysis. Exp. Parasitol. 102 (2002) 218-222
35. Iniguez A.M., Araujo A., Ferreira L.F., and Vicente A.C.P. Analysis of ancient DNA from coprolites: a perspective with random amplified polymorphic DNA-polymerase chain reaction approach. Mem. Inst. Oswaldo Cruz 98 (2003) 63-65
36. Iniguez A.M., Reinhard K.J., Araujo A., Ferreira L.F., and Vicente A.C.P. Enterobius vermicularis: ancient DNA from North and South American Human Coprolites. Mem. Inst. Oswaldo Cruz 98 (2003) 67-69
37. Kolman C.J., Centurion-Lara A., Lukehart S.A., Owsley D.W., and Tuross N. Identification of Treponema pallidum subspecies pallidum in a 200-year-old skeletal specimen. J. Infect. Dis. 180 (1999) 2060-2063
38. Liu L.X., Blaxter M.L., and Shi A. The 5S ribosomal RNA intergenic region of parasitic nematodes: variation in size and presence of SL1 RNA. Mol. Biochem. Parasitol. 83 (1996) 235-239
39. Liu L.X., Chi J., Upton M.P., and Ash L.R. Eosinophilic colitis associated with larvae of the pinworm Enterobius vermicularis. Lancet 346 (1995) 410-412
40. Loreille O., Roumat E., Verneau O., Bouchet F., and Hanni C. Ancient DNA from Ascaris: extraction amplification and sequences from eggs collected in coprolites. Int. J. Parasitol. 31 (2001) 1101-1116
41. Luciani F., Fornacieri G., Rikards O., Labargas C.M., and Rollo F. Molecular characterization of a pre-Columbian mummy and in situ coprolite. Am. J. Phys. Anthropol. 129 (2006) 620-629
42. Lukes J., Horak A., and Scholz T. Helminth genome projects: all or nothing. Trends Parasitol. 21 (2005) 265-266
43. Lutz A. O Schistosomum mansoni e a schistosomatose segundo observações feitas no Brasil. Mem. Inst. Oswaldo Cruz 11 (1919) 121-155
44. Marota I., and Rollo F. Molecular paleontology. Cell. Mol. Life Sci. 59 (2002) 97-111
45. Montiel R., Garci{dotless}́a C., Cañadas M.P., Isidro A., Guijo J.M., and Malgosa A. DNA sequences of Mycobacterium leprae recovered from ancient bones. FEMS Microbiol. Lett. 226 (2003) 413-414
46. Nilsen T.W. Evolutionary origin of SL-addition trans-splicing: still an enigma. Trends Genet. 17 (2001) 678-680
47. Pääbo S. Amplifying ancient DNA. In: Innis M.A., Gelfand D.H., Sninsky J.J., and White T.J. (Eds). PCR Protocols: A Guide to Methods and Applications (1990), Academic Press, California 159-166
48. Pääbo S., Poinar H., Serre D., Jaenicke-Després V., Hebler J., Rohland N., Kuch M., Krause J., Vigilant L., and Hofreiter M. Genetic analyses from ancient DNA. Annu. Rev. Genet. 38 (2004) 645-679
49. Patruco R., Tello R., and Bonavia D. Parasitological studies of coprolites of pre-hispanic Peruvian populations. Curr. Antropol. 24 (1983) 393-394
50. Poinar H.N., Hofreiter M., Spaulding W.G., Martin P.S., Stankiewicz B.A., Bland H., Evershed R.P., Possnert G., and Pääbo S. Molecular micoproscopy: dung and diet of the extinct ground sloth Nothrotheriops shastensis. Science 281 (1998) 402-406
51. Raoult D., Aboudharam G., Larrouy E.C.G., Ludes B., and Drancourt M. Molecular identification by "suicide PCR" of Yersinia pestis as the agent of medieval black death. Proc. Natl. Acad. Sci. USA 97 (2000) 12800-12803
52. Reinhard K.J. Archaeoparasitology in North America. Am. J. Phys. Anthropol. 82 (1990) 145-162
53. Rothschild M.B., Martin L.D., Lev G., Bercovier H., Bar-Gal G.K., Greenblat C., Donoghue H., Spigelman M., and Brittain D. Mycobacterium tuberculosis complex DNA from an extinct bison dated 17,000 years before the present. Clin. Infect. Dis. 33 (2001) 305-311
54. Sallares R., and Gomzi S. Biomolecular archaeology of malaria. Anc. Biomol. 3 (2001) 195-213
55. Stratford R., and Shields R. A trans-spliced leader RNA sequence in plant parasitic nematodes. Mol. Biochem. Parasitol. 67 (1994) 147-155
56. Stucki U., Braun R., and Roditi I. Eimeria tenella: characterization of a 5S ribosomal RNA repeat unit and its use a species-specific probe. Exp. Parasitol. 76 (1993) 68-75
57. Sturm N.R., Yu M.C., and Campbell D.A. Transcription termination and 3′-end processing of the spliced leader RNA in kinetoplastids. Mol. Cell. Biol. 19 (1999) 1595-1604
58. van der Giessen J.W.B., Fonville M., Briels I., and Pozio E. Phylogenetic analysis of encapsulated and non-encapsulated Trichinella species by studying the 5S rDNA tandemly repeated intergenic region. Vet. Parasitol. 132 (2005) 51-55
59. Vandenberghe A.E., Meedel T.H., and Hastings K.E.M. mRNA 5′-lader trans-splicing in the chordates. Genes Dev. 15 (2001) 294-303
60. Veronico P., De Luca F., and De Giorgi C. Molecular dissection of the rDNA array and of the 5S rDNA gene in Meloidogyne artiellia: phylogenetic and diagnostic implications. Mol. Cell. Probes 18 (2004) 177-183
61. Xie H., Bain O., and Williams A.S. Molecular phylogenetic studies on filarial parasites based on 5S ribosomal spacer sequences. Parasite 1 (1994) 114-151
62. Xie H., and Hirsh D. In vivo function of mutated spliced leader RNAs in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 95 (1998) 4235-4240
63. Xu Y., Liu L., and Michaeli S. Functional analyses of positions across the 5′ splice site of the trypanosomatid spliced leader RNA: implications for base-pair interaction with U5 and U6 snRNAs. J. Biol. Chem. 275 (2000) 27883-27892
64. Zimmerman M.R., and Morilla R.E. Enterobiasis in pre-Columbian America. Paleopathol. News 42 (1983) 8
65. Zink A.R., Sola C., Reischl U., Grabner W., Rastogi N., Wolf H., and Nerlich A.G. Characterization of Mycobacterium tuberculosis complex DNAs from Egyptian mummies by spoligotyping. J. Clin. Microbiol. 41 (2003) 359-367
66. Zuker M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31 (2003) 3406-3415