The dimorphic yeast Yarrowia lipolytica possesses an atypical phosphofructokinase: Characterization of the enzyme and its encoding gene

Microbiology

Volumn 151, Issue 5, 2005, Pages 1465-1474

  Flores, Carmen Lisset ^a   Martínez Costa, Oscar H ^a   Sánchez, Valentina ^a   Gancedo, Carlos ^a   Aragón, Juan J ^a  

^a UNIVERSIDAD AUTÓNOMA DE MADRID   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

6 PHOSPHOFRUCTOKINASE; ADENOSINE DIPHOSPHATE; ADENOSINE PHOSPHATE; ADENOSINE TRIPHOSPHATE MAGNESIUM; FRUCTOSE 2,6 BISPHOSPHATE; FRUCTOSE 6 PHOSPHATE; GLUCOSE; PHOSPHOENOLPYRUVATE;

ARTICLE; CARBON SOURCE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ANALYSIS; ENZYME INHIBITION; ENZYME KINETICS; ENZYME PURIFICATION; ENZYME SUBUNIT; FUNGUS ISOLATION; GENE DISRUPTION; GENETIC CODE; GLUCOSE METABOLISM; GLYCOLYSIS; INTRACELLULAR SPACE; INTRON; MOLECULAR WEIGHT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; SACCHAROMYCES CEREVISIAE; YARROWIA LIPOLYTICA; YEAST;

AMINO ACID SEQUENCE; CULTURE MEDIA; GENE EXPRESSION REGULATION, FUNGAL; GLUCOSE; KINETICS; MOLECULAR SEQUENCE DATA; PHOSPHOFRUCTOKINASES; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; YARROWIA;

SACCHAROMYCES CEREVISIAE; YARROWIA LIPOLYTICA;

EID: 19044397060     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.27856-0     Document Type: Article

References (59)

1. Ammerer, G. (1983). Expression of genes in yeast using the ADCI promoter. Methods Enzymol 101, 192-201.
2. Aragón, J. J., Sánchez, V. & Boto, L. (1986). Fructose 2,6-bisphosphate in Dictyostelium discoideum. Independence of cyclic AMP production and inhibition of fructose-1,6-bisphosphatase. Eur J Biochem 161, 757-761.
3. Arts, E., Kubicek, C. P. & Rohr, M. (1987). Regulation of phosphofructokinase from Aspergillus niger: effect of fructose 2,6-bisphosphate on the action of citrate, ammonium ions and AMP. J Gen Microbiol 133, 1195-1199.
4. Bañuelos, M., Gancedo, C. & Gancedo, J. M. (1977). Activation by phosphate of yeast phosphofructokinase. J Biol Chem 252, 6394-6398.
5. Bär, J., Schellenberger, W. & Kopperschläger, G. (1997). Purification and characterization of phosphofructokinase from the yeast Kluyveromyces lactis. Yeast 13, 1309-1317.
6. Barth, G. & Gaillardin, C. (1996). Yarrowia lipolytica. In Non-Conventional Yeasts in Biotechnology. A Handbook, pp. 313-388. Edited by K. Wolf. New York, NY: Springer.
7. Barth, G. & Scheuber, T. (1993). Cloning of the isocitrate lyase gene (ICL1) from Yarrowia lipolytica and characterization of the deduced protein. Mol Gen Genet 24, 422-430.
8. Becker, D. M., Fikes, J. D. & Guarente, L. (1991). A cDNA encoding a human CCAAT-binding protein cloned by functional complementation in yeast. Proc Natl Acad Sci U S A 8, 1968-1972.
9. Belinchón, M. M., Flores, C. L. & Gancedo, J. M. (2004). Sampling Saccharomyces cerevisiae cells by rapid filtration improves the yield of mRNAs. FEMS Yeast Res 4, 751-756.
10. Bergmeyer, H. U., Bergmeyer, J. & Graßl, M. (1987). Methods of Enzymatic Analysis, 3rd edn, vols VI and VII. Weinheim: VCH.
11. Blangy, D., Buc, H. & Monod, J. (1968). Kinetics of the allosteric interactions of phosphofructokinase from Escherichia coli. J Mol Biol 31, 13-35.
12. Bradford, M. M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72, 248-254.
13. Breitenbach-Schmitt, I., Schmitt, H. D., Heinisch, J. & Zimmermann, F. K. (1984). Genetic and physiological evidence for the existence of a second glycolytic pathway in yeasts parallel to the phosphofructokinase-aldolase reaction sequences. Mol Gen Genet 195, 536-540.
14. Carlson, M. (1999). Glucose repression in yeast. Curr Opin Microbiol 2, 202-207.
15. Ciriacy, M. & Breitenbach, I. (1979). Physiological effects of seven different blocks in glycolysis in Saccharomyces cerevisiae. J Bacteriol 139, 152-160.
16. Davies, S. E. C. & Brindle, K. M. (1992). Effects of overexpression of phosphofructokinase on glycolysis in the yeast Saccharomyces cerevisiae. Biochemistry 31, 4729-4735.
17. Djafarzadeh, R., Kerscher, S., Zwicker, K., Radermacher, M., Lindahl, M., Schagger, H. & Brandt, U. (2000). Biophysical and structural characterization of proton-translocating NADH-dehydrogenase (complex I) from the strictly aerobic yeast Yarrowia lipolytica. Biochim Biophys Acta 1459, 230-238.
18. Domínguez, A., Fermiñán, E. & Gaillardin, C. (2000). Yarrowia lipolytica: an organism amenable to genetic manipulation as a model for analysing dimorphism in fungi. In Contributions to Microbiology, vol. 5, pp. 151-162. Edited by J. F. Ernst & A. Schmidt. Basel, Switzerland: Karger.
19. Dujon, B., Sherman, D., Durrens, P. & 63 other authors (2004). Genome evolution in yeasts. Nature 430, 35-44.
20. Flores, C.-L. & Gancedo, C. (2005). Yarrowia lipolytica mutants devoid of pyruvate carboxylase activity show an unusual growth phenotype. Eukaryot Cell 4, 356-364.
21. Flores, C.-L., Rodriguez, C., Petit, T. & Gancedo, C. (2000). Carbohydrate and energy-yielding metabolism in non-conventional yeasts. FEMS Microbiol Rev 24, 507-529.
22. Gaillardin, C. & Ribet, A. M. (1987). LEU2-directed expression of β-galactosidase activity and phleomycin resistance in Yarrowia lipolytica. Curr Genet 11, 369-375.
23. Gamo, F. J., Portillo, F. & Gancedo, C. (1993). Characterization of mutations that overcome the toxic effect of glucose on phosphoglucose isomerase less strains of Saccharomyces cerevisiae. FEMS Microbiol Lett 106, 233-238.
24. Gancedo, J. M. (1998). Yeast carbon catabolite repression. Microbiol Mol Biol Rev 62, 334-361.
25. González-Mateos, F., Gómez, M.-E., García-Salguero, L., Sánchez, V. & Aragón, J. J. (1993). Inhibition of glycolysis by amino acids in ascites tumor cells. Specificity and mechanism. J Biol Chem 268, 7809-7817.
26. Habison, A., Kubicek, C. P. & Rohr, M. (1983). Partial purification and regulatory properties of phosphofructokinase from Aspergillus niger. Biochem J 209, 669-676.
27. Heinisch, J., Ritzel, R. G., von Borstel, R. C., Aguilera, A., Rodicio, R. & Zimmermann, F. K. (1989). The phosphofructokinase genes of yeast evolved from two duplication events. Gene 78, 309-321.
28. Heinisch, J., Kirchrath, L., Liesen, T., Vogelsang, K. & Hollenberg, C. P. (1993). Molecular genetics of phosphofructokinase in the yeast Kluyveromyces lactis. Mol Microbiol 8, 559-570.
29. Higgins, D., Thompson, J., Gibson, T., Thompson, J. D., Higgins, D. G. & 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 Res 22, 4673-4680.
30. Hirai, M., Tanaka, A. & Fukui, S. (1975). Difference in pyruvate kinase regulation among three groups of yeasts. Biochim Biophys Acta 391, 282-291.
31. Hoffman, C. S. & Winston, F. (1987). A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of E. coil Gene 57, 266-272.
32. Hofmann, E. & Kopperschläger, G. (1982). Phosphofructokinase from yeast. Methods Enzymol 90, 49-60.
33. Hofmeyr, J. H. & Cornish-Bowden, A. (1991). Quantitative assessment of regulation in metabolic systems. Eur J Biochem 200, 223-236.
34. Ito, H., Fukuda, Y., Murata, K. & Kimura, A. (1983). Transformation of intact yeast cells treated with alcali cations. J Bacteriol 153, 163-168.
35. Jacoby, J., Hollenberg, C. P. & Heinisch, J. J. (1993). Transaldolase mutants in the yeast Kluyveromyces lactis provide evidence that glucose can be metabolized through the pentose phosphate pathway. Mol Microbiol 10, 867-876.
36. Kemp, R. G. & Foe, L. G. (1983). Allosteric regulatory properties of muscle phosphofructokinase. Mol Cell Biochem 57, 147-154.
37. Kirchberger, J., Bär, J., Schellenberger, W., Dihazi, H. & Kopperschläger, G. (2002). 6-phosphofructokinase from Pichia pastoris: purification, kinetic and molecular characterization of the enzyme. Yeast 19, 933-947.
38. Kopperschläger, G., Bär, J., Nissler, K. & Hofmann, E. (1977). Physicochemical parameters and subunit composition of yeast phosphofructokinase. Eur J Biochem 81, 317-325.
39. Kurtzman, C. P. & Blanz, P. A. (1998). Ribosomal RNA/DNA sequence comparisons for assessing phylogenetic relationships. In The Yeasts. A Taxonomic Study, 4th edn, pp. 69-74. Edited by C. P. Kurtzman & J. W. Fell. Amsterdam: Elsevier.
40. Lorberg, A., Kirchrath, L., Ernst, J. F. & Heinisch, J. J. (1999). Genetic and biochemical characterization of phosphofructokinase from the opportunistic pathogenic yeast Candida albicans. Eur J Biochem 260, 217-226.
41. Martínez-Costa, O. H., Estévez, A. M., Sánchez, V. & Aragón, J. J. (1994). Purification and properties of phosphofructokinase from Dictyostelium discoideum. Eur J Biochem 226, 1007-1017.
42. Martínez-Costa, O. H., Hermida, C., Sánchez-Martínez, C., Santamaría, B. & Aragón, J. J. (2004). Identification of C-terminal motifs responsible for transmission of ATP inhibition of mammalian phosphofructokinase, and their contribution to other allosteric effects. Biochem J 377, 77-84.
43. Monod, J., Wyman, J. & Changeux, J.-P. (1965). On the nature allosteric transitions: a plausible model. J Mol Biol 12, 88-118.
44. Nomenclature Committee of the International Union of Biochemistry (1985). Nomenclature for incompletely specified bases in nucleic acid sequences. Recommendations 1984. Eur J Biochem 150, 1-5.
45. Ogushi, S., Lawson, J. W. R., Dobson, G. P., Veech, R. L. & Oyeda, K. (1990). A new transient activator of phosphofructokinase during initiation of rapid glycolysis in brain. J Biol Chem 265, 10943-10949.
46. Orosz, F., Santamaría, B., Ovádi, J. & Aragón, J. J. (1999). Phosphofructokinase from Dictyostelium discoideum is a potent inhibitor of tubulin polymerization. Biochemistry 38, 1857-1865.
47. Petit, T. & Gancedo, C. (1999). Molecular cloning and characterization of the gene HXK1 encoding the hexokinase from Yarrowia lipolytica. Yeast 15, 1573-1581.
48. Poorman, R. A., Randolph, A., Kemp, R. G. & Heinrikson, R. L. (1984). Evolution of phosphofructokinase: gene duplication and creation of new effector sites. Nature 309, 467-469.
49. Reuter, R., Naumann, M., Bär, J., Haferburg, D. & Kopperschläger, G. (2000). Purification, molecular and kinetic characterization of phosphofructokinase-1 from the yeast Schizosaccharomyces pombe: evidence for an unusual subunit composition. Yeast 16, 1273-1285.
50. Sambrook, J., Fritsch, E. F. & Maniatis, T. (1989). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
51. Schröter, A. & Kopperschläger, G. (1996). 6-phosphofructo-1-kinase from the lipid-accumulating, non-fermentative, red yeast Rhodotorula glutinis. FEMS Microbiol Lett 142, 247-252.
52. Shirakihara, Y. & Evans, P. R. (1988). Crystal structure of the complex of phosphofructokinase from Escherichia coli with its reaction products. J Mol Biol 204, 973-994.
53. Sikorski, R. S. & Hieter, P. (1989). A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122, 19-27.
54. Sols, A. (1981). Multimodulation of enzyme activity. Curr Top Cell Regul 19, 77-101.
55. Souciet, J., Aigle, M., Artiguenave, F. & 21 other authors (2000). Genomic exploration of the hemiascomycetous yeasts: 1. A set of yeast species for molecular evolution studies. FEBS Lett 487, 3-12.
56. Tornheim, K. (1988). Fructose 2,6-bisphosphate and glycolytic oscillations in skeletal muscle extracts. J Biol Chem 263, 2619-2624.
57. Uyeda, K. (1979). Phosphofructokinase. Adv Enzymol Relat Areas Mol Biol 48, 193-244.
58. Van Schaftingen, E. (1987). Fructose 2,6-bisphosphate. Adv Enzymol Relat Areas Mol Biol 59, 315-395.
59. Yuan, W., Tuttle, D. L., Shi, Y. J., Ralph, G. S. & Dunn, W. A., Jr (1997). Glucose-induced microautophagy in Pichia pastoris requires the alpha-subunit of phosphofructokinase. J Cell Sci 110, 1935-1945.