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Trans-sialidase genes expressed in mammalian forms of Trypanosoma cruzi evolved from ancestor genes expressed in insect forms of the parasite

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Abstract

The trans-sialidase of Trypanosoma cruzi mammalian forms transfers sialic acids from host's cell-surface glycoconjugates to acceptor molecules on parasite cell surface. To investigate the mechanism by which the mammalian stages of Trypanosoma cruzi have acquired their trans-sialidase, we compared the nucleotide and predicted amino acid sequences of trans-sialidase genes expressed in different developmental stages and strains of Trypanosoma cruzi with the sialidase gene of Trypanosoma rangeli and the sialidase genes of the prokaryotic genera Clostridium, Salmonella, and Actinomyces. The trans-sialidase gene products of Trypanosoma cruzi have a significant degree of structural and biochemical similarity to the sialidases found in bacteria and viruses, which would hint that horizontal gene transfer occurred in Trypanosome cruzi trans-sialidase evolutionary history. The comparison of inferred gene trees with species trees suggests that the genes encoding the T. cruzi trans-sialidase of mammalian forms might be derived from genes expressed in the insect forms of the genus Trypanosome. The branching order of trees inferred from T. cruzi trans-sialidase sequences, the sialidase from Trypanosoma rangeli, and bacterial sialidases parallels the expected branching order of the species and suggests that the divergence times of these sequences are remarkably long. Therefore, a “vertical” inheritance from a hypothetical eukaryotic trans-sialidase gene expressed in insect forms of trypanosomes is more likely to have occurred than the horizontal gene transfer from bacteria, and thus explains the presence of this enzyme in the mammalian infective forms of Trypanosoma cruzi.

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References

  • Briones MRS, Nelson K, Beverley SM, Affonso MHT, Camargo EP, Floeter-Winter LM (1992) Leishmania tarentolae taxonomic relatedness inferred from phylogenetic analysis of the small subunit ribosomal RNA gene. Mol Biochem Parasitol 53:121–128

    Google Scholar 

  • Buschiazzo A, Cremona ML, Campetella O, Frasch ACC, Sanchez DO (1993) Sequence of a Trypanosoma rangeli gene closely related to Trypanosoma cruzi trans-sialidase. Mol Biochem Parasitol 62:115–116

    Google Scholar 

  • Campetella O, Sanchez D, Cazzulo JJ, Frasch ACC (1992) A superfamily of Trypanosoma cruzi surface antigens. Parasitol Today 8: 378–381

    Google Scholar 

  • Cazzulo JJ, Frasch ACC (1992) SAPA/trans-sialidase and cruzipain: two antigens from Trypanosoma cruzi contain immunodominant but enzymatically inactive domains. FASEB J 6:3259–3264

    Google Scholar 

  • Chaves LB, Briones MRS, Schenkman S (1993) Trans-sialidase from Trypanosoma cruzi epimastigotes is expressed at the stationary phase and is different from the enzyme expressed in trypomastigotes. Mol Biochem Parasitol 61:97–106

    Google Scholar 

  • Cote GL, Tao BY (1990) Oligosaccharide synthesis by enzymatic transglycosylation. Glycoconj J 7:145–162

    Google Scholar 

  • Crennel SJ, Garman EF, Laver GW, Vimr E, Taylor GL (1993) First crystal structure of a bacterial sialidase (Salmonella thyphimurium LT2) shows same fold as influenza virus neuraminidase. Proc Natl Acad Sci USA 90:9842–9856

    Google Scholar 

  • Cross GAM, Takle GB (1993) The surface trans-sialidase family of Trypanosoma cruzi. Annu Rev Microbiol 47:385–411

    Google Scholar 

  • Engstler M, Reuter G, Schauer R (1992a) Identification of a trans-sialidase activity in procyclic Trypanosoma brucei. Hoppe Seylers Z Physiol Chem 373:843 (Abstr)

    Google Scholar 

  • Engstler M, Reuter G, Schauer R (1992b) Purification and characterization of a novel sialidase found in procyclic culture forms of Trypanosoma brucei. Mol Biochem Parasitol 54:21–30

    Google Scholar 

  • Engstler M, Schauer R (1993) Sialidases from african Trypanosomes. Parasitol Today 9:222–225

    Google Scholar 

  • Felsenstein J (1978) Cases in which parsimony or compatibility methods will be positively misleading. Syst Zool 27:401–410

    Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Google Scholar 

  • Felsenstein J (1988) Phylogenies from molecular sequences: inference and reliability. Ann Rev Genet 22:521–565

    Google Scholar 

  • Felsenstein J (1993) PHYLIP. Phylogeny inference package, version 3.5. Distributed by the author, Dept. of Genetics, Univ Washington, USA

    Google Scholar 

  • Fernandes AP, Nelson K, Beverley SM (1993) Evolution of nuclear ribosomal RNAs in kinetoplastid protozoa: new perspectives on the age and origins of parasitism. Proc Natl Acad Sci USA 90:11608–11612

    Google Scholar 

  • Fitch WM (1977) On the problem of discovering the most parsimonious tree. Am Nat 111:223–257

    Google Scholar 

  • Fitch WM, Margoliash E (1967) Construction of phylogenetic trees. Science 155:279–284

    CAS  PubMed  Google Scholar 

  • Hall BF, Joiner KA (1993) Developmentally-regulated virulence factors of Trypanosoma cruzi and their relationship to evasion of host defences. J Protozool 40:207–213

    Google Scholar 

  • Hernandez R, Rios P, Valdes AM, Pinero D (1990) Primary structure of Trypanosoma cruzi small-subunit ribosomal RNA coding region: comparison with other trypanosomatids. Mol Biochem Parasitol 41:207–212

    Google Scholar 

  • Hoyer LL, Hamilton AC, Steenbergen SM, Vimr ER (1992) Cloning, sequencing and expression of the Salmonella typhimurium LT2 sialidase gene, nanH, provides evidence for interspecies gene transfer. Mol Microbiol 6:873–884

    Google Scholar 

  • Irwin DM, Kocher TD, Wilson AC (1991) Evolution of cytochrome b gene of mammals. J Mol Evol 32:128–144

    CAS  PubMed  Google Scholar 

  • Kahn S, Colbert TG, Wallace JC, Hoagland NA, Eisen H (1991) The major 85-kDa surface antigen of the mammalian-stage forms of Trypanosoma cruzi is a family of sialidases. Proc Natl Acad Sci USA 88:4481–4485

    Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16;111–120

    CAS  PubMed  Google Scholar 

  • Lainson R, Shaw JJ (1987) Evolution, classification and geographical distribution. In: Peters W, Killick-Kendrick R (eds) The Leishmanias in biology and medicine. Academic Press, New York, pp 1–20

    Google Scholar 

  • Lerner PI (1990) Actinomyces and Arachnia species. In: Mandell GL, Douglas R, Bennett J (eds) Principles and practice of infectious diseases. Churchill Livingstone, New York, pp 1932–1933

    Google Scholar 

  • Li W-H, Graur D (1991) Fundamentals of molecular evolution. Sinauer Associates, Sunderland, MA

    Google Scholar 

  • Maddison WP, Maddison DR (1992) MacClade: analysis of phylogeny and character evolution, version 3.0. Sinauer Associates, Sunderland, MA

    Google Scholar 

  • Medina-Acosta E, Paul S, Tomlinson S, Pontes de Carvalho L (1994) Mol Biochem Parasitol (in press)

  • Michels PA, Marchand M, Kohl L, Allert S, Wierenga RK, Opperdoes FR (1991) The cytosolic and glycosomal isoenzymes of glyceraldehyde-3-phosphate dehydrogenase in Trypanosoma brucei have a distant evolutionary relationship. Eur J Biochem 198:421–428

    Article  Google Scholar 

  • Pereira MEA, Mejia JS, Ortega-Barria E, Matzilevich D, Prioli RP (1991) The Trypanosoma cruzi neuraminidase contains sequences similar to bacterial neuraminidases, YWTD repeats of the low density lipoprotein receptor, and type III modules of fibronectin. J Exp Med 174:179–191

    Google Scholar 

  • Pollevick GD, Affranchino JL, Frasch ACC, Sanchez DO (1991) The complete sequence of a shed acute-phase antigen of Trypanosoma cruzi. Mol Biochem Parasitol 47:247–250

    Google Scholar 

  • Pollock JJ, Sharon N (1970) Studies on the acceptor specificity of the lysozyme-catalyzed transglycosylation reaction. Biochemistry 9: 3913–3925

    Google Scholar 

  • Pontes de Carvalho L, Tomlinson S, Vandekerckhove F, Bienen EJ, Clarkson AB, Jiang MS, Hart GW, Nussenzweig V (1993a) Characterization of a novel trans-sialidase of Trypanosoma brucei procyclic trypomastigotes and identification of procyclin as the main sialic acid acceptor. J Exp Med 177:465–474

    Google Scholar 

  • Pontes de Carvalho LC, Tomlinson S, Nussenzweig V (1993b) Trypanosoma rangeli sialidase lacks trans-sialidase activity. Mol Biochem Parasitol 62:19–26

    Google Scholar 

  • Previato JO, Andrade AF, Pessolani MC, Mendonça-Previato L (1985) Incorporation of sialic acid into Trypanosoma cruzi macromolecules. A proposal for a new metabolic route. Mol Biochem Parasitol 16:85–96

    Google Scholar 

  • Roggentin P, Rothe B, Lothspeich F, Schauer R (1988) Cloning and sequencing of a Clostridium perfringens sialidase gene. FEBS Lett 238:31–34

    Google Scholar 

  • Roggentin P, Schauer R, Hoyer LL, Vimr ER (1993) The sialidase superfamily and its spread by horizontal gene transfer. Mol Microbiol 9:915–921

    Google Scholar 

  • Rothe B, Roggentin P, Frank R, Bloecker H, Schauer R (1989) Cloning, sequencing and expression of a sialidase gene from Clostridium sordellii G12. J Gen Microbiol 135:3087–3096

    Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    CAS  PubMed  Google Scholar 

  • Schauer R, Reuter G, Muhlpfordt H, Andrade AF, Pereira ME (1983) The occurrence of N-acetyl- and N-glycoloylneuraminic acid in Trypanosoma cruzi. Hoppe Seylers Z Physiol Chem 364:1053–1057

    Google Scholar 

  • Schenkman S, Man-Shiow J, Hart GW, Nussenzweig V (1991) A novel cell surface trans-sialidase of Trypanosoma cruzi generates a stage-specific epitope required for invasion of mammalian cells. Cell 65:1117–1125

    Google Scholar 

  • Schenkman S, de Carvalho LP, Nussenzweig V (1992) Trypanosoma cruzi trans-sialidase and neuraminidase activities can be mediated by the same enzymes. J Exp Med 175:567–575

    Google Scholar 

  • Schenkman S, Eichinger D (1993) Trypanosoma cruzi trans-sialidase and cell invasion. Parasitol Today 9:218–222

    Google Scholar 

  • Swofford DL (1991) Phylogenetic analysis using parsimony, PAUP, version 3.0. Illinois Natural History Survey, Champaign, IL

    Google Scholar 

  • Swofford DL, Olsen G (1990) Phylogeny reconstruction. In: Hillis DM, Moritz C (eds) Molecular systematics. Sinauer Associates, Sunderland, MA, pp 411–501

    Google Scholar 

  • Takle GB, Cross GAM (1991) An 85-kilo-dalton surface antigen gene family of Trypanosoma cruzi encodes polypeptides homologous to bacterial neuraminidases. Mol Biochem Parasitol 48:185–198

    Google Scholar 

  • Uemura H, Schenkman S, Nussenzweig V, Eichinger D (1992) Only some members of a gene family in Trypanosoma cruzi encode proteins which express both trans-sialidase and neuraminidase. EMBO J 11:3837–3844

    Google Scholar 

  • Yeung MK (1993) Complete nucleotide sequence of the Actinomyces viscousus T14V sialidase gene: presence of a conserved repeating sequence among strains of Actinomyces spp. Infect Immunol 61: 109–116

    Google Scholar 

  • Zingales B, Camiol C, de Lederkremer RM, Colli W (1987) Direct sialic acid transfer from a protein donor to glycolipids of trypomastigote forms of Trypanosoma cruzi. Mol Biochem Parasitol 26:135–144

    Google Scholar 

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Authors and Affiliations

  1. Departamento de Microbiologia, Imunologia e Parasitologia, Escola Paulista de Medicina, R. Botucatu 862, 8° andar, 04023-062, São Paulo, S.P. Brasil

    Marcelo R. S. Briones, Claudia M. Egima & Sergio Schenkman

  2. Michael Heidelberger Division of Immunology, New York University, 10016, New York, NY, USA

    Daniel Eichinger

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  1. Marcelo R. S. Briones
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  2. Claudia M. Egima
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  3. Daniel Eichinger
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  4. Sergio Schenkman
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Correspondence to: M.R.S. Briones

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Briones, M.R.S., Egima, C.M., Eichinger, D. et al. Trans-sialidase genes expressed in mammalian forms of Trypanosoma cruzi evolved from ancestor genes expressed in insect forms of the parasite. J Mol Evol 41, 120–131 (1995). https://doi.org/10.1007/BF00170663

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