Leishmania mexicana: Molecular cloning and characterization of enolase

Experimental Parasitology

Volumn 116, Issue 3, 2007, Pages 241-251

  Quiñones, Wilfredo ^a   Peña, Priscila ^a   Domingo Sananes, Maria ^a   Cáceres, Ana ^a   Michels, Paul A M ^b   Avilan, Luisana ^a   Concepción, Juan Luis ^a  

^a FACULTAD DE CIENCIAS   (Venezuela)

^b DE DUVE INSTITUTE   (Belgium)

Author keywords

2 phosphoglycerate; 2PGA; Enolase; inorganic pyrophosphate; Kinetics; Leishmania mexicana; Membrane localization; PEP; PEP carboxykinase; PEPCK; phosphoenolpyruvate; PPDK; PPi; pyruvate phosphate dikinase

Indexed keywords

ENOLASE;

ARTICLE; CELL MEMBRANE PERMEABILITY; CENTRIFUGATION; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME KINETICS; ENZYME LOCALIZATION; ENZYME PURIFICATION; GENE OVEREXPRESSION; IMMUNOFLUORESCENCE TEST; LEISHMANIA MEXICANA; MICROSOME MEMBRANE; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMASTIGOTE; TRYPANOSOMA BRUCEI; WESTERN BLOTTING;

AMINO ACID SEQUENCE; ANIMALS; ANTIBODIES, PROTOZOAN; BASE SEQUENCE; BLOTTING, WESTERN; CELL MEMBRANE PERMEABILITY; CLONING, MOLECULAR; DIGITONIN; ELECTROPHORESIS, POLYACRYLAMIDE GEL; FLUORESCENT ANTIBODY TECHNIQUE; INDICATORS AND REAGENTS; KINETICS; LEISHMANIA MEXICANA; MICE; MOLECULAR SEQUENCE DATA; PHOSPHOPYRUVATE HYDRATASE; RABBITS; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT;

ESCHERICHIA COLI; LEISHMANIA MEXICANA; TRYPANOSOMA BRUCEI; TRYPANOSOMATIDAE;

EID: 34248212625     PISSN: 00144894     EISSN: 10902449     Source Type: Journal    
DOI: 10.1016/j.exppara.2007.01.008     Document Type: Article

References (46)

1. Acosta H., Dubourdieu M., Quiñones W., Caceres A., Bringaud F., and Concepcion J.L. Pyruvate phosphate dikinase and pyrophosphate metabolism in the glycosome of Trypanosoma cruzi epimastigotes. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 138 (2004) 347-356
2. Albert M.A., Haanstra J.R., Hannaert V., Van Roy J., Opperdoes F.R., Bakker B.M., and Michels P.A.M. Experimental and in silico analyses of glycolytic flux control in bloodstream form Trypanosoma brucei. Journal of Biological Chemistry 280 (2005) 28306-28315
3. Avilan L., Calcagno M., Figuera M., Lemus L., Puig J., and Rodriguez A.M. Interaction of Leishmania mexicana promastigotes with the plasminogen-plasmin system. Molecular and Biochemical Parasitology 110 (2000) 183-193
4. Bergmeyer H.U. Methods of Enzymatic Analysis (1983), Academic Press, New York
5. Berriman M., Ghedin E., Hertz-Fowler C., Blandin G., Renauld H., Bartholomeu D., Lennard N., Caler E., Hamlin N., Haas B., Bohme U., Hannick L., Aslett M., Shallom J., Marcello L., Hou L., Wickstead B., Alsmark U., Arrowsmith C., Atkin R., Barron A., Bringaud F., Brooks K., Carrington M., Cherevach I., Chillingworth T., Churcher C., Clark L., Corton C., Cronin A., Davies R., Doggett J., Djikeng A., Feldblyum T., Field M., Fraser A., Goodhead I., Hance Z., Harper D., Harris B., Hauser H., Hostetler J., Ivens A., Jagels K., Johnson D., Johnson J., Jones K., Kerhornou A., Koo H., Larke N., Landfear S., Larkin C., Leech V., Line A., Lord A., MacLeod A., Mooney P., Moule S., Martin D., Morgan G., Mungall K., Norbertczak H., Ormond D., Pai G., Peacock C., Peterson J., Quail M., Rabbinowitsch E., Rajandream M., Reitter C., Salzberg S., Sanders M., Schobel S., Sharp S., Simmonds M., Simpson A., Tallon L., Turner C., Tait A., Tivey A., Van Aken S., Walker D., Wanless D., Wang S., White B., White O., Whitehead S., Woodward J., Wortman J., Adams M., Embley T., Gull K., Ullu E., Barry J., Fairlamb A., Opperdoes F., Barrell B., Donelson J., Hall N., Fraser C., et al. The genome of the African trypanosome Trypanosoma brucei. Science 309 (2005) 416-422
6. Besteiro S., Biran M., Biteau N., Coustou V., Baltz T., Canioni P., and Bringaud F. Succinate secreted by Trypanosoma brucei is produced by a novel and unique glycosomal enzyme, NADH-dependent fumarate reductase. Journal of Biological Chemistry 277 (2002) 38001-38012
7. Bringaud F., Baltz D., and Baltz T. Functional and molecular characterization of a glycosomal PPi-dependent enzyme in trypanosomatids: pyruvate, phosphate dikinase. Proceedings of the National Academy of Sciences of the United States of America 95 (1998) 7963-7968
8. Bringaud F., Riviere L., and Coustou V. Energy metabolism of trypanosomatids: adaptation to available carbon sources. Molecular and Biochemical Parasitology 149 (2006) 1-9
9. Caceres A.J., Portillo R., Acosta H., Rosales D., Quiñones W., Avilan L., Salazar L., Dubourdieu M., Michels P.A.M., and Concepción J.L. Molecular and biochemical characterization of hexokinase from Trypanosoma cruzi. Molecular and Biochemical Parasitology 126 (2003) 251-262
10. Carneiro C.R., Postol E., Nomizo R., Reis L.F., and Brentani R.R. Identification of enolase as a laminin-binding protein on the surface of Staphylococcus aureus. Microbes and Infection 6 (2004) 604-608
11. Concepcion J.L., Chataing B., and Dubourdieu M. Purification and properties of phosphoglucose isomerases of Trypanosoma cruzi. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology 122 (1999) 211-222
12. Croft S.L., and Coombs G.H. Leishmaniasis-current chemotherapy and recent advances in the search for novel drugs. Trends in Parasitology 19 (2003) 502-508
13. da Silva Giotto M.T., Hannaert V., Vertommen D., de A.S. Navarro M.V., Rider M.H., Michels P.A., Garratt R.C., and Rigden D.J. The crystal structure of Trypanosoma brucei enolase: visualisation of the inhibitory metal binding site III and potential as target for selective, irreversible inhibition. Journal of Molecular Biology 331 (2003) 653-665
14. Denny P.W., Gokool S., Russsell D.G., Field M.C., and Smith D.F. Acylation-dependent protein export in Leishmania. Journal of Biological Chemistry 275 (2000) 11017-11025
15. Edwards S.R., Braley R., and Chaffin W.L. Enolase is present in the cell wall of Saccharomyces cerevisiae. FEMS Microbiology Letter 177 (1999) 211-216
16. Entian K.D., Meurer B., and Mecke D. Purification of three distinct enolase isoenzymes from yeast. Analytical Biochemistry 132 (1983) 225-228
17. Fratelli M., Demol H., Puype M., Casagrande S., Eberini I., Salmona M., Bonetto V., Mengozzi M., Duffieux F., Miclet E., Bachi A., Vandekerckhove J., Gianazza E., and Ghezzi P. Identification by redox proteomics of glutathionylated proteins in oxidatively stressed human T lymphocytes. Proceedings of the National Academy of Sciences of the United States of America 99 (2002) 3505-3510
18. Gierow P., and Jergil B. Spectrometric method for glucose-6-phosphatase. Methods in Enzymology 89 (1982) 44-47
19. Hannaert V., Albert M.A., Rigden D.J., da Silva Giotto M.T., Thiemann O., Garratt R.C., Van Roy J., Opperdoes F.R., and Michels P.A.M. Kinetic characterization, structure modelling studies and crystallization of Trypanosoma brucei enolase. European Journal of Biochemistry 270 (2003) 3205-3213
20. Hannaert, V., Bringaud, F., Opperdoes, F.R., Michels, P.A.M., 2003b. Evolution of energy metabolism and its compartmentation in Kinetoplastida. Kinetoplastid Biology and Disease 2, 11. http://www.kinetoplastids.com/content/2/1/11.
21. Hannaert V., Blaauw M., Kohl L., Allert S., Opperdoes F.R., and Michels P.A. Molecular analysis of the cytosolic and glycosomal glyceraldehyde-3-phosphate dehydrogenase in Leishmania mexicana. Molecular and Biochemical Parasitology 55 (1992) 115-126
22. Hudock M.P., Sanz-Rodriguez C.E., Song Y., Chan J.M., Zhang Y., Odeh S., Kosztowski T., Leon-Rossell A., Concepcion J.L., Yardley V., Croft S.L., Urbina J.A., and Oldfield E. Inhibition of Trypanosoma cruzi hexokinase by bisphosphonates. Journal of Medical Chemistry 49 (2006) 215-223
23. Ishii T., and Uchida K. Induction of reversible cysteine-targeted protein oxidation by an endogenous electrophile 15-deoxy-delta12,14-prostaglandin J2. Chemical Research in Toxicology 17 (2004) 1313-1322
24. Jolodar A., Fischer P., Bergmann S., Buttner D.W., Hammerschmidt S., and Brattig N.W. Molecular cloning of an alpha-enolase from the human filarial parasite Onchocerca volvulus that binds human plasminogen. Biochimica et Biophysica Acta 1627 (2003) 111-120
25. Keller A., Rouzeau J.D., Farhadian F., Wisnewsky C., Marotte F., Lamande N., Samuel J.L., Schwartz K., Lazar M., and Lucas M. Differential expression of alpha- and beta-enolase genes during rat heart development and hypertrophy. American Journal of Physiology 269 (1995) 1843-1851
26. Kohler P., and Bachmann R. Mechanisms of respiration and phosphorylation in Ascaris muscle mitochondria. Molecular and Biochemical Parasitology 1 (1980) 75-90
27. Krishnamurthy G., Vikram R., Singh S.B., Patel N., Agarwal S., Mukhopadhyay G., Basu S.K., and Mukhopadhyay A. Hemoglobin receptor in Leishmania is a hexokinase located in the flagellar pocket. Journal of Biological Chemistry 280 (2005) 5884-5891
28. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680-685
29. Lopez-Villar E., Monteoliva L., Larsen M.R., Sachon E., Shabaz M., Pardo M., Pla J., Gil C., Roepstorff P., and Nombela C. Genetic and proteomic evidences support the localization of yeast enolase in the cell surface. Proteomics 6 (2006) S107-S118
30. Maldonado J., Calcagno M., Puig J., Maizo Z., and Avilan L. A study of cutaneous lesions caused by Leishmania mexicana in plasminogen-deficient mice. Experimental and Molecular Pathology 80 (2006) 289-294
31. McConville M.J., Mullin K.A., Ilgoutz S.C., and Teasdale R.D. Secretory pathway of trypanosomatid parasites. Microbiology and Molecular Biology Reviews 66 (2002) 122-154
32. Mertens E. ATP versus pyrophosphate: glycolysis revisited in parasitic protists. Parasitology Today 9 (1993) 122-126
33. Michels P.A.M., Hannaert V., and Bringaud F. Metabolic aspects of glycosomes in trypanosomatidae-new data and views. Parasitology Today 16 (2000) 482-489
34. Michels P.A.M., Marchand M., Kohl L., Allert S., Wierenga R.K., and Opperdoes F.R. The cytosolic and glycosomal isoenzymes of glyceraldehyde-3-phosphate dehydrogenase in Trypanosoma brucei have a distant evolutionary relationship. European Journal of Biochemistry 198 (1991) 421-428
35. Miernyk J.A., and Dennis D.T. Enolase isozymes from Ricinus communis: partial purification and characterization of the isozymes. Archives of Biochemistry and Biophysics 233 (1984) 643-651
36. 31P NMR spectroscopy of Trypanosoma brucei, Trypanosoma cruzi, and Leishmania major. Evidence for high levels of condensed inorganic phosphates. Journal of Biological Chemistry 275 (2000) 28356-28362
37. Opperdoes F.R., and Michels P.A. Enzymes of carbohydrate metabolism as potential drug targets. International Journal for Parasitology 31 (2001) 482-490
38. Pancholi V. Multifunctional alpha-enolase: its role in diseases. Cellular and Molecular Life Sciences 58 (2001) 902-920
39. Pérez H., Labrador F., and Torrealba J.W. Variations in the response of five strains of mice to Leishmania mexicana. International Journal for Parasitology 9 (1979) 27-32
40. Ramajo-Hernandez A., Perez-Sanchez R., Ramajo-Martin V., and Oleaga A. Schistosoma bovis: plasminogen binding in adults and the identification of plasminogen-binding proteins from the worm tegument. Experimental Parasitology 115 (2007) 83-91
41. Sambrook J., Fritsch E.F., and Maniatis T. Molecular Cloning: A Laboratory Manual. second ed. (1989), Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York
42. Sarkar M., Hamilton C.J., and Fairlamb A.H. Properties of phosphoenolpyruvate mutase, the first enzyme in the aminoethylphosphonate biosynthetic pathway in Trypanosoma cruzi. Journal of Biological Chemistry 278 (2003) 22703-22708
43. Shimizu A., Suzuki F., and Kato K. Characterization of alpha alpha, beta beta, gamma gamma and alpha gamma human enolase isozymes, and preparation of hybrid enolases (alpha gamma, beta gamma and alpha beta) from homodimeric forms. Biochimica et Biophysica Acta 748 (1983) 278-284
44. Spring T.G., and Wold F. The purification and characterization of Escherichia coli enolase. Journal of Biological Chemistry 246 (1971) 6797-6802
45. Suzuki F., Umeda Y., and Kato K. Rat brain enolase isozymes. Purification of three forms of enolase. Journal of Biochemistry (Tokyo) 87 (1980) 1587-1594
46. Thompson J.D., Higgins D.G., and Gibson T.J. 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 (1994) 4673-4680