Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-22T20:45:42.691Z Has data issue: false hasContentIssue false
  • English
  • Français

Cellular and biochemical characterization of two closely related triosephosphate isomerases from Trichomonas vaginalis

Published online by Cambridge University Press:  29 August 2012

ELISA E. FIGUEROA-ANGULO ,
PRISCILA ESTRELLA-HERNÁNDEZ ,
HOLJES SALGADO-LUGO ,
ADRIÁN OCHOA-LEYVA ,
ARMANDO GÓMEZ PUYOU ,
SILVIA S. CAMPOS ,
GABRIELA MONTERO-MORAN ,
JAIME ORTEGA-LÓPEZ ,
GLORIA SAAB-RINCÓN  and
ROSSANA ARROYO
...Show all authors
ELISA E. FIGUEROA-ANGULO
Affiliation:
Departamento de Infectómica y Patogénesis Molecular, Centro de Investigación y de Estudios Avanzados del IPN, Col. San Pedro Zacatenco, Av. IPN, 2508, C.P. 07360, México, D.F.
PRISCILA ESTRELLA-HERNÁNDEZ
Affiliation:
Laboratorio Nacional de Genómica para la Biodiversidad, Centro de Investigación y de Estudios Avanzados del IPN, Km. 9·6 Libramiento Norte Carr. Irapuato-León 36821, Irapuato, Guanajuato, México
HOLJES SALGADO-LUGO
Affiliation:
Laboratorio Nacional de Genómica para la Biodiversidad, Centro de Investigación y de Estudios Avanzados del IPN, Km. 9·6 Libramiento Norte Carr. Irapuato-León 36821, Irapuato, Guanajuato, México
ADRIÁN OCHOA-LEYVA
Affiliation:
Instituto Nacional de Medicina Genómica (INMEGEN), Secretaría de Salud, México City, Distrito Federal, C.P. 01900, México
ARMANDO GÓMEZ PUYOU
Affiliation:
Departamento de Bioquímica y Biología Estructural, Instituto de Fisiología Celular, Universidad Nacional Autónoma de México, Mexico City, México
SILVIA S. CAMPOS
Affiliation:
Laboratorio Nacional de Genómica para la Biodiversidad, Centro de Investigación y de Estudios Avanzados del IPN, Km. 9·6 Libramiento Norte Carr. Irapuato-León 36821, Irapuato, Guanajuato, México
GABRIELA MONTERO-MORAN
Affiliation:
Laboratorio Nacional de Genómica para la Biodiversidad, Centro de Investigación y de Estudios Avanzados del IPN, Km. 9·6 Libramiento Norte Carr. Irapuato-León 36821, Irapuato, Guanajuato, México
JAIME ORTEGA-LÓPEZ
Affiliation:
Departamento de Biotecnología y Bioingeniería, Centro de Investigación y de Estudios Avanzados del IPN, Col. San Pedro Zacatenco, Av. IPN, 2508, C.P. 07360, México, D.F.
GLORIA SAAB-RINCÓN
Affiliation:
Departamento de Ingeniería Celular y Biocatálisis, Instituto de Biotecnología, Universidad Nacional Autónoma de México, Avenida Universidad 2001, Cuernavaca, C.P. 62210, México
ROSSANA ARROYO
Affiliation:
Departamento de Infectómica y Patogénesis Molecular, Centro de Investigación y de Estudios Avanzados del IPN, Col. San Pedro Zacatenco, Av. IPN, 2508, C.P. 07360, México, D.F.
CLAUDIA G. BENÍTEZ-CARDOZA
Affiliation:
Laboratorio de Investigación Bioquímica, Programa Institucional en Biomedicina Molecular ENMyH-Instituto Politécnico Nacional, Guillermo Massieu Helguera No. 239, La Escalera Ticomán, 07320, D.F, México
LUIS G. BRIEBA*
Affiliation:
Laboratorio Nacional de Genómica para la Biodiversidad, Centro de Investigación y de Estudios Avanzados del IPN, Km. 9·6 Libramiento Norte Carr. Irapuato-León 36821, Irapuato, Guanajuato, México
*
*Corresponding author: Laboratorio Nacional de Genómica para la Biodiversidad, Centro de Investigación y de Estudios Avanzados del IPN, Km. 9·6 Libramiento Norte Carr. Irapuato-León 36821, Irapuato, Guanajuato, México. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

The glycolytic enzyme triosephosphate isomerase catalyses the isomerization between glyceraldehyde 3-phosphate and dihydroxyacetone phosphate. Here we report that Trichomonas vaginalis contains 2 fully functional tpi genes. Both genes are located in separated chromosomal context with different promoter regulatory elements and encode ORFs of 254 amino acids; the only differences between them are the character of 4 amino acids located in α-helices 1, 2 and 8. Semi-quantitative RT-PCR assays showed that tpi2 transcript is approximately 3·3-fold more abundant than tpi1. Using an anti-TvTIM2 polyclonal antibody it was demonstrated that TIM proteins have a cytoplasmic localization and both enzymes are able to complement an Escherichia coli strain carrying a deletion of its endogenous tpi gene. Both TIM proteins assemble as dimers and their secondary structure assessment is essentially identical to TIM from Saccharomyces cerevisiae. The kinetic catalytic constants of the recombinant enzymes using glyceraldehyde-3-phosphate as substrate are similar to the catalytic constants of TIMs from other organisms including parasitic protozoa. As T. vaginalis depends on glycolysis for ATP production, we speculate 2 possible reasons to maintain a duplicated tpi copy on its genome: an increase in gene dosage or an early event of neofunctionalization of TIM as a moonlighting protein.

Keywords

duplicated geneevolutioncentral metabolismamitocondriate protozoastructure-function
Type
Research Article
Information
Parasitology , Volume 139 , Issue 13 , November 2012 , pp. 1729 - 1738
Copyright
Copyright © Cambridge University Press 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Alderete, J. F., O'Brien, J. L., Arroyo, R., Engbring, J. A., Musatovova, O., Lopez, O., Lauriano, C. and Nguyen, J. (1995). Cloning and molecular characterization of two genes encoding adhesion proteins involved in Trichomonas vaginalis cytoadherence. Molecular Microbiology 17, 69–83.CrossRefGoogle ScholarPubMed
Alvarez-Sanchez, M. E., Solano-Gonzalez, E., Yanez-Gomez, C. and Arroyo, R. (2007). Negative iron regulation of the CP65 cysteine proteinase cytotoxicity in Trichomonas vaginalis. Microbes and Infection 9, 1597–1605.CrossRefGoogle ScholarPubMed
Aurrecoechea, C., Brestelli, J., Brunk, B. P., Carlton, J. M., Dommer, J., Fischer, S., Gajria, B., Gao, X., Gingle, A., Grant, G., Harb, O. S., Heiges, M., Innamorato, F., Iodice, J., Kissinger, J. C., Kraemer, E., Li, W., Miller, J. A., Morrison, H. G., Nayak, V., Pennington, C., Pinney, D. F., Roos, D. S., Ross, C., Stoeckert, C. J. Jr., Sullivan, S., Treatman, C. and Wang, H. (2009). GiardiaDB and TrichDB: integrated genomic resources for the eukaryotic protist pathogens Giardia lamblia and Trichomonas vaginalis. Nucleic Acids Research 37(Database issue), D526–530.CrossRefGoogle ScholarPubMed
Bell, G. S., Russell, R. J., Kohlhoff, M., Hensel, R., Danson, M. J., Hough, D. W. and Taylor, G. L. (1998). Preliminary crystallographic studies of triosephosphate isomerase (TIM) from the hyperthermophilic Archaeon Pyrococcus woesei. Acta Crystallographica Section D: Biological Crystallography 54, 1419–1421.CrossRefGoogle ScholarPubMed
Blacklow, S. C., Raines, R. T., Lim, W. A., Zamore, P. D. and Knowles, J. R. (1988). Triosephosphate isomerase catalysis is diffusion controlled. Appendix: Analysis of triose phosphate equilibria in aqueous solution by 31P NMR. Biochemistry 27, 1158–1167.CrossRefGoogle Scholar
Carlton, J. M., Hirt, R. P., Silva, J. C., Delcher, A. L., Schatz, M., Zhao, Q., Wortman, J. R., Bidwell, S. L., Alsmark, U. C., Besteiro, S., Sicheritz-Ponten, T., Noel, C. J., Dacks, J. B., Foster, P. G., Simillion, C., Van de Peer, Y., Miranda-Saavedra, D., Barton, G. J., Westrop, G. D., Muller, S., Dessi, D., Fiori, P. L., Ren, Q., Paulsen, I., Zhang, H., Bastida-Corcuera, F. D., Simoes-Barbosa, A., Brown, M. T., Hayes, R. D., Mukherjee, M., Okumura, C. Y., Schneider, R., Smith, A. J., Vanacova, S., Villalvazo, M., Haas, B. J., Pertea, M., Feldblyum, T. V., Utterback, T. R., Shu, C. L., Osoegawa, K., de Jong, P. J., Hrdy, I., Horvathova, L., Zubacova, Z., Dolezal, P., Malik, S. B., Logsdon, J. M. Jr., Henze, K., Gupta, A., Wang, C. C., Dunne, R. L., Upcroft, J. A., Upcroft, P., White, O., Salzberg, S. L., Tang, P., Chiu, C. H., Lee, Y. S., Embley, T. M., Coombs, G. H., Mottram, J. C., Tachezy, J., Fraser-Liggett, C. M. and Johnson, P. J. (2007). Draft genome sequence of the sexually transmitted pathogen Trichomonas vaginalis. Science 315, 207–212.CrossRefGoogle ScholarPubMed
Conant, G. and Wolfe, K. (2007). Increased glycolytic flux as an outcome of whole-genome duplication in yeast. Molecular Systems Biology 3, 129.CrossRefGoogle ScholarPubMed
Conant, G. C. and Wolfe, K. H. (2008). Turning a hobby into a job: how duplicated genes find new functions. Nat Reviews Genetics 9, 938–950.CrossRefGoogle ScholarPubMed
Cui, J., Das, S., Smith, T. F. and Samuelson, J. (2010). Trichomonas transmembrane cyclases result from massive gene duplication and concomitant development of pseudogenes. PLoS Neglected Tropical Diseases 4, e782.CrossRefGoogle ScholarPubMed
Cui, J., Smith, T. F. and Samuelson, J. (2007). Gene expansion in Trichomonas vaginalis: a case study on transmembrane cyclases. Genome Inform 18, 35–43.Google ScholarPubMed
DeLuna, A., Springer, M., Kirschner, M. W. and Kishony, R. (2010). Need-based up-regulation of protein levels in response to deletion of their duplicate genes. PLoS Biol, 8(3), e1000347.CrossRefGoogle ScholarPubMed
Diamond, L. (1957). The establishment of various trichomonads of animals and man in axenic culture. Journal of Parasitology 43, 488–490.CrossRefGoogle Scholar
Enriquez-Flores, S., Rodriguez-Romero, A., Hernandez-Alcantara, G., Oria-Hernandez, J., Gutierrez-Castrellon, P., Perez-Hernandez, G., de la Mora-de la, Mora I., Castillo-Villanueva, A., Garcia-Torres, I., Mendez, S. T., Gomez-Manzo, S., Torres-Arroyo, A., Lopez-Velazquez, G. and Reyes-Vivas, H. (2011). Determining the molecular mechanism of inactivation by chemical modification of triosephosphate isomerase from the human parasite Giardia lamblia: a study for antiparasitic drug design. Proteins 79, 2711–2724.CrossRefGoogle ScholarPubMed
Espinosa, N., Hernandez, R., Lopez-Griego, L. and Lopez-Villasenor, I. (2002). Separable putative polyadenylation and cleavage motifs in Trichomonas vaginalis mRNAs. Gene 289, 81–86.CrossRefGoogle ScholarPubMed
Feierabend, J., Kurzok, H. G. and Schmidt, M. (1990). Genetics and evolution of chloroplast isozymes of triosephosphate isomerase. Progress in Clinical Biological Research 344, 665–682.Google ScholarPubMed
Felsenstein, J. (1993). PHYLIP (Phylogeny Inference Package) version 3.5c. Distributed by the author. Department of Genetics, Univestiy of Washington, Seattle, USA.Google Scholar
Gao, X. G., Garza-Ramos, G., Saavedra-Lira, E., Cabrera, N., De Gomez-Puyou, M. T., Perez-Montfort, R. and Gomez-Puyou, A. (1998). Reactivation of triosephosphate isomerase from three trypanosomatids and human: effect of suramin. Biochemical Journal 332, 91–96.CrossRefGoogle ScholarPubMed
Henze, K., Horner, D. S., Suguri, S., Moore, D. V., Sanchez, L. B., Muller, M. and Embley, T. M. (2001). Unique phylogenetic relationships of glucokinase and glucosephosphate isomerase of the amitochondriate eukaryotes Giardia intestinalis, Spironucleus barkhanus and Trichomonas vaginalis. Gene 281, 123–131.CrossRefGoogle ScholarPubMed
Huang, M. M., Arnheim, N. and Goodman, M. F. (1992). Extension of base mispairs by Taq DNA polymerase: implications for single nucleotide discrimination in PCR. Nucleic Acids Research 20, 4567–4573.CrossRefGoogle ScholarPubMed
Kanehisa, M., Goto, S., Sato, Y., Furumichi, M. and Tanabe, M. (2008). KEGG for integration and interpretation of large-scale molecular data sets. Nucleic Acids Research 40 (Database issue), D109–114.CrossRefGoogle Scholar
Knobeloch, D., Schmidt, A., Scheerer, P., Krauss, N., Wessner, H., Scholz, C., Kuttner, G., von Rintelen, T., Wessel, A. and Hohne, W. (2010). A coleopteran triosephosphate isomerase: X-ray structure and phylogenetic impact of insect sequences. Insect Molecular Biology 19, 35–48.CrossRefGoogle ScholarPubMed
Kohlhoff, M., Dahm, A. and Hensel, R. (1996). Tetrameric triosephosphate isomerase from hyperthermophilic Archaea. FEBS Letters 383, 245–250.CrossRefGoogle ScholarPubMed
Lama, A., Kucknoor, A., Mundodi, V. and Alderete, J. F. (2009). Glyceraldehyde-3-phosphate dehydrogenase is a surface-associated, fibronectin-binding protein of Trichomonas vaginalis. Infection and Immunity 77, 2703–2711.CrossRefGoogle ScholarPubMed
Leon-Sicairos, C. R., Leon-Felix, J. and Arroyo, R. (2004). tvcp12: a novel Trichomonas vaginalis cathepsin L-like cysteine proteinase-encoding gene. Microbiology, 150(Pt 5), 1131–1138.CrossRefGoogle ScholarPubMed
Liston, D. R. and Johnson, P. J. (1999). Analysis of a ubiquitous promoter element in a primitive eukaryote: early evolution of the initiator element. Molecular and Cellular Biology 19, 2380–2388.CrossRefGoogle Scholar
Merritt, T. J. and Quattro, J. M. (2001). Evidence for a period of directional selection following gene duplication in a neurally expressed locus of triosephosphate isomerase. Genetics 159, 689–697.CrossRefGoogle Scholar
Mertens, E. and Muller, M. (1990). Glucokinase and fructokinase of Trichomonas vaginalis and Tritrichomonas foetus. Journal of Protozoology 37, 384–388.CrossRefGoogle ScholarPubMed
Mertens, E., Van Schaftingen, E. and Muller, M. (1992). Pyruvate kinase from Trichomonas vaginalis, an allosteric enzyme stimulated by ribose 5-phosphate and glycerate 3-phosphate. Molecular and Biochemical Parasitology 54, 13–20.CrossRefGoogle ScholarPubMed
Meza-Cervantez, P., González-Robles, A., Cárdenas-Guerra, R., Ortega-López, J., Saavedra, E., Pineda, E. and Arroyo, R. (2011). Pyruvate : ferredoxin oxidoreductase (PFO) is a surface-associated cell-binding protein in Trichomonas vaginalis and is involved in trichomonal adherence to host cells. Microbiology 157, 3469–3482.CrossRefGoogle ScholarPubMed
Mundodi, V., Kucknoor, A. S. and Alderete, J. F. (2008). Immunogenic and plasminogen-binding surface-associated alpha-enolase of Trichomonas vaginalis. Infection and Immunity 76, 523–531.CrossRefGoogle ScholarPubMed
Olivares-Illana, V., Perez-Montfort, R., Lopez-Calahorra, F., Costas, M., Rodriguez-Romero, A., Tuena de Gomez-Puyou, M. and Gomez Puyou, A. (2006). Structural differences in triosephosphate isomerase from different species and discovery of a multitrypanosomatid inhibitor. Biochemistry 45, 2556–2560.CrossRefGoogle ScholarPubMed
Olivares-Illana, V., Rodriguez-Romero, A., Becker, I., Berzunza, M., Garcia, J., Perez-Montfort, R., Cabrera, N., Lopez-Calahorra, F., de Gomez-Puyou, M. T. and Gomez-Puyou, A. (2007). Perturbation of the dimer interface of triosephosphate isomerase and its effect on Trypanosoma cruzi. PLoS Neglected Tropical Diseases 1, e1.CrossRefGoogle ScholarPubMed
Poysti, N. J. and Oresnik, I. J. (2007). Characterization of Sinorhizobium meliloti triose phosphate isomerase genes. Journal of Bacteriology 189, 3445–3451.CrossRefGoogle ScholarPubMed
Reyes-Vivas, H., Diaz, A., Peon, J., Mendoza-Hernandez, G., Hernandez-Alcantara, G., De la Mora-De la, Mora I., Enriquez-Flores, S., Dominguez-Ramirez, L. and Lopez-Velazquez, G. (2007). Disulfide bridges in the mesophilic triosephosphate isomerase from Giardia lamblia are related to oligomerization and activity. Journal of Molecular Biology 365, 752–763.CrossRefGoogle ScholarPubMed
Reyes-Vivas, H., Hernandez-Alcantara, G., Lopez-Velazquez, G., Cabrera, N., Perez-Montfort, R., de Gomez-Puyou, M. T. and Gomez-Puyou, A. (2001). Factors that control the reactivity of the interface cysteine of triosephosphate isomerase from Trypanosoma brucei and Trypanosoma cruzi. Biochemistry 40, 3134–3140.CrossRefGoogle ScholarPubMed
Rodriguez-Romero, A., Hernandez-Santoyo, A., del Pozo Yauner, L., Kornhauser, A. and Fernandez-Velasco, D. A. (2002). Structure and inactivation of triosephosphate isomerase from Entamoeba histolytica. Journal of Molecular Biology 322, 669–675.CrossRefGoogle ScholarPubMed
Rozacky, E. E., Sawyer, T. H., Barton, R. A. and Gracy, R. W. (1971). Studies on human triosephosphate isomerase. I. Isolation and properties of the enzyme from erythrocytes. Archives of Biochemistry and Biophysics 146, 312–320.CrossRefGoogle ScholarPubMed
Saab-Rincon, G., Juarez, V. R., Osuna, J., Sanchez, F. and Soberon, X. (2001). Different strategies to recover the activity of monomeric triosephosphate isomerase by directed evolution. Protein Engineering 14, 149–155.CrossRefGoogle ScholarPubMed
Sanchez, L., Horner, D., Moore, D., Henze, K., Embley, T. and Muller, M. (2002). Fructose-1,6-bisphosphate aldolases in amitochondriate protists constitute a single protein subfamily with eubacterial relationships. Gene 295, 51–59.CrossRefGoogle ScholarPubMed
Singh, S., Singh, G., Singh, A. K., Gautam, G., Farmer, R., Lodhi, S. S. and Wadhwa, G. (2009). Prediction and analysis of paralogous proteins in Trichomonas vaginalis genome. Bioinformation 6, 31–34.CrossRefGoogle Scholar
Slamovits, C. H. and Keeling, P. J. (2006). Pyruvate-phosphate dikinase of oxymonads and parabasalia and the evolution of pyrophosphate-dependent glycolysis in anaerobic eukaryotes. Eukaryotic Cell 5, 148–154.CrossRefGoogle ScholarPubMed
Thompson, J. D., Higgins, D. G. and Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.CrossRefGoogle ScholarPubMed
Velanker, S. S., Ray, S. S., Gokhale, R. S., Suma, S., Balaram, H., Balaram, P. and Murthy, M. R. (1997). Triosephosphate isomerase from Plasmodium falciparum: the crystal structure provides insights into antimalarial drug design. Structure 5, 751–761.CrossRefGoogle ScholarPubMed
World Health Organization (2007). Global Prevalence and Incidencee of Selected Curable Sexually Transmitted Infections. World Health Organization, Geneva, Switzerland.Google Scholar
Wixon, J. and Kell, D. (2000). The Kyoto encyclopedia of genes and genomes–KEGG. Yeast 17, 48–55.Google ScholarPubMed
Zheng, P., Sun, J., van den Heuvel, J. and Zeng, A. P. (2006). Discovery and investigation of a new, second triose phosphate isomerase in Klebsiella pneumoniae. Journal of Biotechnology, 125(4), 462–473.CrossRefGoogle ScholarPubMed
Supplementary material: File

Brieba Supplementary Material

Appendix

Download Brieba Supplementary Material(File)
File 16.1 MB