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. 1988 Nov;8(11):4745–4755. doi: 10.1128/mcb.8.11.4745

Tandemly repeated exons encode 81-base repeats in multiple, developmentally regulated Schistosoma mansoni transcripts.

R E Davis 1, A H Davis 1, S M Carroll 1, A Rajkovic 1, F M Rottman 1
PMCID: PMC365566  PMID: 3211127

Abstract

The adult Schistosoma mansoni cDNA clone 10-3 encodes an antigen that is recognized by sera from infected humans. We characterized multiple developmentally regulated transcripts homologous to the 10-3 cDNA and portions of the complex genomic loci encoding those transcripts. Transcripts of approximately 950, 870, and 780 nucleotides were expressed in adults, whereas only the 780-nucleotide transcript was observed in the larval stage. These transcripts were highly similar, containing variable numbers of identical direct tandem repeats of 81 bases. Although the sequence of the repeating elements and sequences 3' to them were identical in all the transcripts, sequences 5' of the repeating elements exhibited variations, including a 27-base insertion, alternative start sites for transcription, and alternate 5' exon usage. These transcripts appeared to be derived in part by the developmentally controlled alternative splicing of small exons and the use of alternative transcription initiation sites from the one or two complex loci of at least 40 kilobase pairs. Each 81-base repeat in the transcripts was encoded by three dispersed 27-base-pair exons. These 27-base-pair exons were contained within highly conserved, reiterated 3-kilobase-pair genomic tandem arrays.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Basch P. F., Humbert R. Cultivation of Schistosoma mansoni in vitro. III. implantation of cultured worms into mouse mesenteric veins. J Parasitol. 1981 Apr;67(2):191–195. [PubMed] [Google Scholar]
  2. Bianco A. E., Favaloro J. M., Burkot T. R., Culvenor J. G., Crewther P. E., Brown G. V., Anders R. F., Coppel R. L., Kemp D. J. A repetitive antigen of Plasmodium falciparum that is homologous to heat shock protein 70 of Drosophila melanogaster. Proc Natl Acad Sci U S A. 1986 Nov;83(22):8713–8717. doi: 10.1073/pnas.83.22.8713. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bobek L., Rekosh D. M., van Keulen H., LoVerde P. T. Characterization of a female-specific cDNA derived from a developmentally regulated mRNA in the human blood fluke Schistosoma mansoni. Proc Natl Acad Sci U S A. 1986 Aug;83(15):5544–5548. doi: 10.1073/pnas.83.15.5544. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bressan G. M., Argos P., Stanley K. K. Repeating structure of chick tropoelastin revealed by complementary DNA cloning. Biochemistry. 1987 Mar 24;26(6):1497–1503. doi: 10.1021/bi00380a001. [DOI] [PubMed] [Google Scholar]
  5. Cavener D. R. Comparison of the consensus sequence flanking translational start sites in Drosophila and vertebrates. Nucleic Acids Res. 1987 Feb 25;15(4):1353–1361. doi: 10.1093/nar/15.4.1353. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Chang L. Y., Slightom J. L. Isolation and nucleotide sequence analysis of the beta-type globin pseudogene from human, gorilla and chimpanzee. J Mol Biol. 1984 Dec 25;180(4):767–784. doi: 10.1016/0022-2836(84)90256-0. [DOI] [PubMed] [Google Scholar]
  7. Church G. M., Gilbert W. Genomic sequencing. Proc Natl Acad Sci U S A. 1984 Apr;81(7):1991–1995. doi: 10.1073/pnas.81.7.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Cowman A. F., Saint R. B., Coppel R. L., Brown G. V., Anders R. F., Kemp D. J. Conserved sequences flank variable tandem repeats in two S-antigen genes of Plasmodium falciparum. Cell. 1985 Apr;40(4):775–783. doi: 10.1016/0092-8674(85)90337-x. [DOI] [PubMed] [Google Scholar]
  9. Davis A. H., Blanton R., Rottman F., Maurer R., Mahmoud A. Isolation of cDNA clones for differentially expressed genes of the human parasite Schistosoma mansoni. Proc Natl Acad Sci U S A. 1986 Aug;83(15):5534–5538. doi: 10.1073/pnas.83.15.5534. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Duvall R. H., DeWitt W. B. An improved perfusion technique for recovering adult schistosomes from laboratory animals. Am J Trop Med Hyg. 1967 Jul;16(4):483–486. doi: 10.4269/ajtmh.1967.16.483. [DOI] [PubMed] [Google Scholar]
  11. Eckert R. L., Green H. Structure and evolution of the human involucrin gene. Cell. 1986 Aug 15;46(4):583–589. doi: 10.1016/0092-8674(86)90884-6. [DOI] [PubMed] [Google Scholar]
  12. Feinberg A. P., Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. doi: 10.1016/0003-2697(83)90418-9. [DOI] [PubMed] [Google Scholar]
  13. Garfinkel M. D., Pruitt R. E., Meyerowitz E. M. DNA sequences, gene regulation and modular protein evolution in the Drosophila 68C glue gene cluster. J Mol Biol. 1983 Aug 25;168(4):765–789. doi: 10.1016/s0022-2836(83)80074-6. [DOI] [PubMed] [Google Scholar]
  14. Guerin-Marchand C., Druilhe P., Galey B., Londono A., Patarapotikul J., Beaudoin R. L., Dubeaux C., Tartar A., Mercereau-Puijalon O., Langsley G. A liver-stage-specific antigen of Plasmodium falciparum characterized by gene cloning. Nature. 1987 Sep 10;329(6135):164–167. doi: 10.1038/329164a0. [DOI] [PubMed] [Google Scholar]
  15. Hattori M., Sakaki Y. Dideoxy sequencing method using denatured plasmid templates. Anal Biochem. 1986 Feb 1;152(2):232–238. doi: 10.1016/0003-2697(86)90403-3. [DOI] [PubMed] [Google Scholar]
  16. Johnson K. S., Taylor D. W., Cordingley J. S. Possible eggshell protein gene from Schistosoma mansoni. Mol Biochem Parasitol. 1987 Jan 2;22(1):89–100. doi: 10.1016/0166-6851(87)90072-7. [DOI] [PubMed] [Google Scholar]
  17. Kidd S., Kelley M. R., Young M. W. Sequence of the notch locus of Drosophila melanogaster: relationship of the encoded protein to mammalian clotting and growth factors. Mol Cell Biol. 1986 Sep;6(9):3094–3108. doi: 10.1128/mcb.6.9.3094. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Klickstein L. B., Wong W. W., Smith J. A., Weis J. H., Wilson J. G., Fearon D. T. Human C3b/C4b receptor (CR1). Demonstration of long homologous repeating domains that are composed of the short consensus repeats characteristics of C3/C4 binding proteins. J Exp Med. 1987 Apr 1;165(4):1095–1112. doi: 10.1084/jem.165.4.1095. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kochan J., Perkins M., Ravetch J. V. A tandemly repeated sequence determines the binding domain for an erythrocyte receptor binding protein of P. falciparum. Cell. 1986 Mar 14;44(5):689–696. doi: 10.1016/0092-8674(86)90834-2. [DOI] [PubMed] [Google Scholar]
  20. Kozak M. Compilation and analysis of sequences upstream from the translational start site in eukaryotic mRNAs. Nucleic Acids Res. 1984 Jan 25;12(2):857–872. doi: 10.1093/nar/12.2.857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lanar D. E., Pearce E. J., James S. L., Sher A. Identification of paramyosin as schistosome antigen recognized by intradermally vaccinated mice. Science. 1986 Oct 31;234(4776):593–596. doi: 10.1126/science.3094144. [DOI] [PubMed] [Google Scholar]
  22. Lazdins J. K., Stein M. J., David J. R., Sher A. Schistosoma mansoni: rapid isolation and purification of schistosomula of different developmental stages by centrifugation on discontinuous density gradients of Percoll. Exp Parasitol. 1982 Feb;53(1):39–44. doi: 10.1016/0014-4894(82)90090-x. [DOI] [PubMed] [Google Scholar]
  23. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  24. Meinkoth J., Wahl G. Hybridization of nucleic acids immobilized on solid supports. Anal Biochem. 1984 May 1;138(2):267–284. doi: 10.1016/0003-2697(84)90808-x. [DOI] [PubMed] [Google Scholar]
  25. Moore J. T., Hagstrom J., McCormick D. J., Harvey S., Madden B., Holicky E., Stanford D. R., Wieben E. D. The major clotting protein from guinea pig seminal vesicle contains eight repeats of a 24-amino acid domain. Proc Natl Acad Sci U S A. 1987 Oct;84(19):6712–6714. doi: 10.1073/pnas.84.19.6712. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Mowatt M. R., Clayton C. E. Developmental regulation of a novel repetitive protein of Trypanosoma brucei. Mol Cell Biol. 1987 Aug;7(8):2838–2844. doi: 10.1128/mcb.7.8.2838. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Muskavitch M. A., Hogness D. S. An expandable gene that encodes a Drosophila glue protein is not expressed in variants lacking remote upstream sequences. Cell. 1982 Jul;29(3):1041–1051. doi: 10.1016/0092-8674(82)90467-6. [DOI] [PubMed] [Google Scholar]
  28. Narayan P., Ayers D. F., Rottman F. M., Maroney P. A., Nilsen T. W. Unequal distribution of N6-methyladenosine in influenza virus mRNAs. Mol Cell Biol. 1987 Apr;7(4):1572–1575. doi: 10.1128/mcb.7.4.1572. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Newport G. R., Harrison R. A., McKerrow J., Tarr P., Kallestad J., Agabian N. Molecular cloning of Schistosoma mansoni myosin. Mol Biochem Parasitol. 1987 Nov;26(1-2):29–38. doi: 10.1016/0166-6851(87)90127-7. [DOI] [PubMed] [Google Scholar]
  30. Ozaki L. S., Svec P., Nussenzweig R. S., Nussenzweig V., Godson G. N. Structure of the plasmodium knowlesi gene coding for the circumsporozoite protein. Cell. 1983 Oct;34(3):815–822. doi: 10.1016/0092-8674(83)90538-x. [DOI] [PubMed] [Google Scholar]
  31. Padgett R. A., Grabowski P. J., Konarska M. M., Seiler S., Sharp P. A. Splicing of messenger RNA precursors. Annu Rev Biochem. 1986;55:1119–1150. doi: 10.1146/annurev.bi.55.070186.005351. [DOI] [PubMed] [Google Scholar]
  32. Peterson D. S., Wrightsman R. A., Manning J. E. Cloning of a major surface-antigen gene of Trypanosoma cruzi and identification of a nonapeptide repeat. Nature. 1986 Aug 7;322(6079):566–568. doi: 10.1038/322566a0. [DOI] [PubMed] [Google Scholar]
  33. Rackwitz H. R., Zehetner G., Frischauf A. M., Lehrach H. Rapid restriction mapping of DNA cloned in lambda phage vectors. Gene. 1984 Oct;30(1-3):195–200. doi: 10.1016/0378-1119(84)90120-3. [DOI] [PubMed] [Google Scholar]
  34. Rigby P. W., Dieckmann M., Rhodes C., Berg P. Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol. 1977 Jun 15;113(1):237–251. doi: 10.1016/0022-2836(77)90052-3. [DOI] [PubMed] [Google Scholar]
  35. Roditi I., Carrington M., Turner M. Expression of a polypeptide containing a dipeptide repeat is confined to the insect stage of Trypanosoma brucei. Nature. 1987 Jan 15;325(6101):272–274. doi: 10.1038/325272a0. [DOI] [PubMed] [Google Scholar]
  36. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Sharp P. M., Li W. H. Ubiquitin genes as a paradigm of concerted evolution of tandem repeats. J Mol Evol. 1987;25(1):58–64. doi: 10.1007/BF02100041. [DOI] [PubMed] [Google Scholar]
  38. Simpson A. J., Sher A., McCutchan T. F. The genome of Schistosoma mansoni: isolation of DNA, its size, bases and repetitive sequences. Mol Biochem Parasitol. 1982 Aug;6(2):125–137. doi: 10.1016/0166-6851(82)90070-6. [DOI] [PubMed] [Google Scholar]
  39. Slightom J. L., Theisen T. W., Koop B. F., Goodman M. Orangutan fetal globin genes. Nucleotide sequence reveal multiple gene conversions during hominid phylogeny. J Biol Chem. 1987 Jun 5;262(16):7472–7483. [PubMed] [Google Scholar]
  40. Stahl H. D., Crewther P. E., Anders R. F., Brown G. V., Coppel R. L., Bianco A. E., Mitchell G. F., Kemp D. J. Interspersed blocks of repetitive and charged amino acids in a dominant immunogen of Plasmodium falciparum. Proc Natl Acad Sci U S A. 1985 Jan;82(2):543–547. doi: 10.1073/pnas.82.2.543. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Vournakis J. N., Efstratiadis A., Kafatos F. C. Electrophoretic patterns of deadenylylated chorion and globin mRNAs. Proc Natl Acad Sci U S A. 1975 Aug;72(8):2959–2963. doi: 10.1073/pnas.72.8.2959. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Yamada Y., Avvedimento V. E., Mudryj M., Ohkubo H., Vogeli G., Irani M., Pastan I., de Crombrugghe B. The collagen gene: evidence for its evolutinary assembly by amplification of a DNA segment containing an exon of 54 bp. Cell. 1980 Dec;22(3):887–892. doi: 10.1016/0092-8674(80)90565-6. [DOI] [PubMed] [Google Scholar]
  43. Yamamoto T., Davis C. G., Brown M. S., Schneider W. J., Casey M. L., Goldstein J. L., Russell D. W. The human LDL receptor: a cysteine-rich protein with multiple Alu sequences in its mRNA. Cell. 1984 Nov;39(1):27–38. doi: 10.1016/0092-8674(84)90188-0. [DOI] [PubMed] [Google Scholar]
  44. Yang C. Y., Chen S. H., Gianturco S. H., Bradley W. A., Sparrow J. T., Tanimura M., Li W. H., Sparrow D. A., DeLoof H., Rosseneu M. Sequence, structure, receptor-binding domains and internal repeats of human apolipoprotein B-100. Nature. 1986 Oct 23;323(6090):738–742. doi: 10.1038/323738a0. [DOI] [PubMed] [Google Scholar]
  45. Yanofsky C. Prokaryotic mechanisms in eukaryotes? Nature. 1983 Apr 28;302(5911):751–752. doi: 10.1038/302751a0. [DOI] [PubMed] [Google Scholar]

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