Skip to main content
SpringerLink
Log in

Isocitrate lyase isozymes and their role in organisms with different levels of organization

  • Published:
Biology Bulletin Reviews Aims and scope Submit manuscript

Abstract

The current state of the problem regarding the prevalence of isocitrate lyase isoenzymes is discussed. Isocitrate lyase is an essential enzyme of the glyoxylate cycle, which is widespread in nature and functions in different physiological periods of life in many organisms. To date, there has been no consensus regarding the induction of this isozyme in animals and bird tissues, despite numerous studies into the functioning of isocitrate lyase isozymes in cells of bacteria, protists, fungi, plants, and nematodes. The kinetic and physical-chemical parameters of plant and animal isocitrate lyases and the molecular-biological aspects of their operation, as well as mechanisms for the expression regulation of these enzymes, are considered. The physiological role of isocitrate lyase isoenzymes in organisms of different taxonomic groups is discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Atomi, H., Veda, M., Hikida, M., et al., Peroximal isocitrate lyase of the n-alkane-assimilating yeast: gene analysis and characterization, J. Biochem., 1990, vol. 107, no. 2.

    Google Scholar 

  • Beeching, J.R., Nucleic acid (cDNA) and amino acid sequences of isocitrate lyase from castor bean, Plant Mol. Biol., 1987, vol. 8, no. 6, pp. 471–475.

    Article  CAS  PubMed  Google Scholar 

  • Bentrup, K.H.Z., Characterization of activity and expression of isocitrate lyase in Mycobacterium avium and Mycobacterium tuberculosis, J. Bacteriol., 1999, vol. 181, no. 23, pp. 7161–7167.

    CAS  Google Scholar 

  • Bowyer, P., Mueller, E., and Lucas, J., Use of an isocitrate lyase promoter-GFP fusion to monitor carbon metabolism of the plant pathogen Tapesia yallundae during infection of wheat, Mol. Plant Pathol., 2000, vol. 1, no. 1, pp. 253–262.

    CAS  PubMed  Google Scholar 

  • Brock, M., Generation and phenotypic characterization of Aspergillus nidulans methylisocitrate lyase deletion mutants: methylisocitrate inhibits growth and conidiation, Appl. Environ. Microbiol., 2005, vol. 71, pp. 5465–5475.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Brock, M., Darley, D., and Textor, S., 2-Methylisocitrate lyases from the bacterium Escherichia coli and the filamentous fungus Aspergillus nidulans: characterization and comparison of both enzymes, J. Biochem., 2001, vol. 268, pp. 3577–3586.

    CAS  Google Scholar 

  • Chan, Ch.T.Kh., Eprintsev, A.T., and Maslova, E.V., Separation of isoenzymes of isocitrate lyase from maize inflorescences using ion-exchange chromatography, Sorbtsionnye Khromatogr. Protsessy, 2008, vol. 8, no. 2, pp. 297–303.

    Google Scholar 

  • Comai, L., Coordinate expression of transcriptionally regulated isocitrate lyase and malate synthase genes in Brassica napus L., Plant Cell, 1989, vol. 1, no. 3, pp. 293–300.

    CAS  PubMed Central  PubMed  Google Scholar 

  • Davis, W.L. and Goodman, D.B., Evidence for the glyoxylate cycle in human liver, Source Anat. Rec., 1992, vol. 234, no. 4, pp. 461–468.

    Article  CAS  Google Scholar 

  • Davis, W.L., Goodman, D.B., and Crawford, L.A., Hibernation activates glyoxylate cycle and gluconeogenesis in black bear brown adipose tissue, Biochim. Biophys. Acta, 1990, vol. 1051, no. 3, pp. 276–278.

    Article  CAS  PubMed  Google Scholar 

  • Davis, W.L., Matthews, J.L., and Goodman, D.B., Glyoxylate cycle in the rat liver: effect of vitamin D3-treatment, FASEB J., 1989, vol. 3, pp. 1651–1655.

    CAS  PubMed  Google Scholar 

  • De los Reyes, B.G., Myers, S.J., and McGrath, J.M., Differential induction of glyoxylate cycle enzymes by stress as a marker 5, Theor. Appl. Genet., 2003, vol. 107, pp. 54–61.

    PubMed  Google Scholar 

  • Delkin, G. and Vodkin, L., Specific elements of the glyoxylate pathway play a significant role in the functional transition of the soybean cotyledon during seedling development, BMC Genomics, 2007, vol. 8, no. 468, pp. 1–2.

    Google Scholar 

  • Diaz-Perez, A.L., Roman-Doval, C., Diaz-Perez, C., et al., Identification of the aceA gene encoding isocitrate lyase required for the growth of Pseudomonas aeruginosa on acetate, acyclic terpenes, and leucine, FEMS Microbiol. Lett., 2007, vol. 269, no. 2, pp. 309–316.

    Article  CAS  PubMed  Google Scholar 

  • Eastmond, P.J., Germain, V, and Lange, P.R., Postgerminative growth and lipid catabolism in oilseeds lacking the glyoxylate cycle, Proc. Natl. Acad. Sci. USA, 2000, vol. 97, no. 10, pp. 5669–5674.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Ebel, F., Schwienbacher, M., and Beyer, J., Analysis of the regulation, expression, and localization of the isocitrate lyase from Aspergillus fumigatus, a potential target for antifungal drug development, Fungal Genet. Biol., 2006, vol. 43, pp. 476–489.

    Article  CAS  PubMed  Google Scholar 

  • Eprintsev, A.T., Popov, V.N., and Shevchenko, M.Yu., Glioksilatnyi tsikl: universal’nyi mekhanizm adaptatsii? (Is Glyoxylate Cycle Universal Adaptation Mechanism?), Moscow: Akademkniga, 2007.

    Google Scholar 

  • Eprintsev, A.T., Shevchenko, M.Yu., and Popov, V.N., Purification and properties of isocitrate lyase from pupas of the butterfly Papilio machaon L., Biochemistry (Moscow), 2004, vol. 69, no. 4, pp. 376–380.

    Article  CAS  Google Scholar 

  • Eprintsev, A.T., Shevchenko, M.Yu., and Popov, V.N., Ekspressiya i regulyatsiya fermentov glioksilatnogo tsikla (Expression and Enzymatic Regulation of Glyoxylate Cycle), Voronezh: Tsentr.-Chernozem. Knizh. Izd., 2005.

    Google Scholar 

  • Eprintsev, A.T., Shevchenko, M.Yu., and Popov, V.N., Distribution of glyoxylate cycle in organisms of different taxonomic groups, Usp. Sovrem. Biol., 2008, vol. 128, no. 3, pp. 271–280.

    CAS  Google Scholar 

  • Ernesto, J.M., Tuberculosis isocitrate lyase 1 and 2 are jointly required for in vivo growth and virulence, Nat. Med., 2005, vol. 11, pp. 638–644.

    Article  Google Scholar 

  • Fernandez, E. and Moreno, F., The icl1 gene from Saccharomyces cerevisiae, Biochemistry, 1992, vol. 204, no. 1, pp. 983–990.

    CAS  Google Scholar 

  • Frevert, J., Koller, W., and Kindi, H., Occurrence and biosynthesis of glyoxysomal enzymes in ripening cucumber seeds, Physiol. Chem., 1980, vol. 361, no. 10, pp. 1557–1565.

    CAS  Google Scholar 

  • Godavari, H.R., Isocitrate lyase in green leaves, Plant Physiol., 1973, vol. 51, no. 6, pp. 863–867.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gould, T.A., van de Langemheen, H., Munoz-Elias, E.J., et al., Dual role of isocitrate lyase 1 in the glyoxylate and methylcitrate cycles in Mycobacterium tuberculosis, Mol. Microbiol., 2006, vol. 61, no. 4, pp. 940–947.

    Article  CAS  PubMed  Google Scholar 

  • Guo, Y. Cai, Z., Gan, S., et al., Transcriptome of Arabidopsis leaf senescence, Plant Cell Environ., 2004, vol. 27, pp. 521–549.

    Article  CAS  Google Scholar 

  • Holmes, R.P., The absence of glyoxylate cycle enzymes in rodent and embryonic chick liver, Biochim. Biophys. Acta, 1993, vol. 1158, pp. 47–51.

    Article  CAS  PubMed  Google Scholar 

  • Igamberdiev, A.U., Mikroel’tsa v metabolisme rstenii (A Role of Microbodies in the Plant Metabolism), Voronezh: Voronezh. Gos. Univ., 1990.

    Google Scholar 

  • Jones, C.T., Is there a glyoxylate cycle in the liver of the fetal guinea pig, Biochem., Biophys. Res. Commun., 1980, vol. 95, pp. 849–856.

    Article  CAS  Google Scholar 

  • Jones, J.D., Burnett, P., and Zollman, P., The glyoxylate cycle: does it function in the dormant or active bear? Comp. Biochem. Physiol. B, 1999, vol. 124, pp. 177–179.

    Article  CAS  PubMed  Google Scholar 

  • Joosten, H.-J., Identification of fungal oxaloacetate hydrolase within the isocitrate lyase/PEP mutase enzyme superfamily using a sequence marker-based method, Proteins: Struct., Funct., Bioinf., 2007, vol. 70, no. 1, pp. 157–166.

    Article  Google Scholar 

  • Kamel, M.Y. and Fahmy, A.S., Biochemical studies of tick embryogenesis. Purification and partial characterization of isocitrate lyase from eggs of the tick Hyalomma dromedarii, Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol., 1982, vol. 72, pp. 107–115.

    CAS  Google Scholar 

  • Kazuo, N., Amano, Y., and Nakadate, M., Purification and properties of isocitrate lyase from Candida brassicae E-l7, J. Ferment. Bioeng., 1989, vol. 67, no. 3, pp. 153–157.

    Article  Google Scholar 

  • Kornberg, H.L. and Krebs, H.A., Synthesis of cell constituents from C2-units by a modified tricarboxylic acid cycle, Nature, 1957, vol. 179, pp. 988–991.

    Article  CAS  PubMed  Google Scholar 

  • Li, J., Xi, L.Y., Liu, H.F., et al., Differential expression of isocitrate lyase in P. marneffei phagocytized by nonstimulated and stimulated marine macrophages, J. South. Med. Univ., 2007, vol. 27, no. 5, pp. 631–634.

    CAS  Google Scholar 

  • Liu, F., Thatcher, J.D., and Barral, J.M., Bifunctional glyoxylate cycle protein of Caenorhabditis elegans: a developmentally regulated protein of intestine and muscle, Dev. Biol., 1995, vol. 169, pp. 399–414.

    Article  CAS  PubMed  Google Scholar 

  • Liu, F., Thatcher, J.D., and Epstein, H.F., Induction of glyoxylate cycle expression in Caenorhabditis elegans: a fasting response throughout larval development, Biochemistry, 1997, vol. 36, pp. 255–260.

    Article  CAS  PubMed  Google Scholar 

  • Lucas, J.R., Gregory, S., and Turner, G., Analysis of the regulation of the Aspergillus nidulans acuD gene, encoding isocitrate lyase, by construction of a hybrid promoter, Mol. Gen. Genet., 1994, vol. 243, no. 6, pp. 6546–6559.

    Article  Google Scholar 

  • Luttik, A.H., Kötter, P., Salomons, F.A., et al., The Saccharomyces cerevisiae ich gene encodes a mitochondrial 2-methylisocitrate lyase involved in propionyl-Co-A metabolism, J. Bacteriol., 2000, vol. 182, no. 5, pp. 7007–7013.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Malhotra, O.P. and Srivaslava, P.K., Isolation and characterization of isocitrate lyase of castor endosperm, Arch. Biochem. Biophys., 1982, vol. 214, no. 1, pp. 164–171.

    Article  CAS  PubMed  Google Scholar 

  • Masaaki, U., Ueda, M., and Matsuki, T., Properties of isocitrate lyase from n-alkane-utilizable yeast, Candida tropicalis, Agric. Biol. Chem., 1986, vol. 50, no. 1, pp. 127–134.

    Article  Google Scholar 

  • Masayoshi, M., Isolation, hyperexpression, and sequencing of the aceA gene encoding isocitrate lyase in Escherichia coli, J. Bacteriol., 1988, vol. 170, no. 10, pp. 4528–4536.

    Google Scholar 

  • McFadden, B.A., Rao, G.R., Cohen, A.L., and Roche, T.E., Isocitrate lyase from Pseudomonas indigofera, V. Subunits and terminal residues and the relation to catalytic activity, Biochemistry, 1968, vol. 7, no. 10, pp. 3574–3582.

    Article  CAS  PubMed  Google Scholar 

  • Ono, K., Kondo, M., and Osafune, T., Presence of glyoxylate cycle enzymes in the mitochondria of Euglena gracilis, J. Eukaryotic Microbiol., 2003, vol. 50, no. 2, pp. 92–96.

    Article  CAS  Google Scholar 

  • Osumi, M., Kazama, H., and Sato, S., Microbody-associated DNA in Candida tropicalis, FEBS Lett., 1978, vol. 90, no. 2, pp. 309–312.

    Article  CAS  PubMed  Google Scholar 

  • Phue, J.N. and Shiloach, J., Transcription levels of key metabolic genes are the cause for different glucose utilization pathways in E. coli B (BL21) and E. coli K (JM109), J. Biotechnol., 2004, vol. 109, no. 2, pp. 21–30.

    Article  CAS  PubMed  Google Scholar 

  • Pinzauti, G., Giachetti, E., and Vanni, P., Isocitrate lyase of conifers Pinus pinea, Int. J. Biochem., 1982, vol. 14, no. 4, pp. 2672–2675.

    Google Scholar 

  • Popov, V.N., Igamberdiev, A.U., and Schnarrenberger, C., Induction of glyoxylate cycle enzymes in rat liver upon food starvation, FEBS Lett., 1996, vol. 390, pp. 258–260.

    Article  CAS  PubMed  Google Scholar 

  • Popov, V.N., Volvenkin, S.V., and Eprintsev, A.T., Glyoxylate cycle enzymes are present in liver peroxisomes of alloxan-treated rats, FEBS Lett., 1998, vol. 440, pp. 55–58.

    Article  CAS  PubMed  Google Scholar 

  • Popov, V.N., Volvenkin, S.V., Eprintsev, A.T., and Igamberdiev, A.U., The induction of glyoxylate cycle enzymes in tissues of starving rats, Biol. Bull., 2000, vol. 27, no. 6, pp. 565–570.

    Article  CAS  Google Scholar 

  • Sharma, V. and Sharma, G., Structure of isocitrate lyase, a persistent factor of Mycobacterium tuberculosis, Nat. Struct. Biol., 2000, vol. 7, pp. 663–668.

    Article  CAS  PubMed  Google Scholar 

  • Siddiqui, A.A., Stanley, C.S., and Berk, S.L., Cloning and expression of isocitrate lyase from human round Strongyloides stercoralis, Parasite, 2000, vol. 7, pp. 233–236.

    CAS  PubMed  Google Scholar 

  • Sokolovskii, M.Yu. and Belozerskaya, T.A., The effect of stress factors on differential gene expression in ontogenesis of Neurospora crassa, Usp. Biol. Khim., 2000, vol. 40, pp. 85–152.

    Google Scholar 

  • Surendranathan, K.K. and Nair, P.M., Properties of an Mg2+-independent isocatrate lyase from gamma irradiated preclimacteric banana Musa cavendishii, Proc. Indian Acad. Sci., B, 1978, vol. 87, no. 4, pp. 119–126.

    Google Scholar 

  • Vanni, P. and Vincenzini, M.T., The presence of isocitrate lyase and malate synthase activity in germinating Ginkgo biloba seeds, Experimentia, 1972, vol. 28, no. 4, pp. 405–406.

    Article  CAS  Google Scholar 

  • Vinccenzini, M.T., Vanni, P., and Giachetti, E., Steadystate kinetic analysis of isocitrate lyase from Lupinus seeds: considerations of isocitrate on a possible catalytic mechanism of isocitrate lyase from plants, J. Biochem., 1986, vol. 99, no. 2, pp. 375–383.

    Google Scholar 

  • Volvenkin, S.V., Popov, V.N., and Eprintsev, A.T., Subcellular localization and properties of glyoxylate cycle enzymes in the liver of rats with alloxin diabetes, Biochemistry (Moscow), 1999, vol. 64, no. 9, pp. 994–999.

    CAS  Google Scholar 

  • Zemlyanukhin, A.A., Zemlyanukhin, L.A., Eprintsev, A.T., and Igamberdiev, A.U., Glioksilatnyi tsikl rastenii (Glyoxylate Cycle in the Plant), Voronezh: Voronezh. Gos. Univ., 1986.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Voronezh State University, pl. Universitetskaya 1, Voronezh, 394006, Russia

    A. T. Eprintsev, A. V. Salnikov, A. M. Haba & M. V. Zaichikova

Authors
  1. A. T. Eprintsev
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. V. Salnikov
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. M. Haba
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. M. V. Zaichikova
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to A. T. Eprintsev.

Additional information

Original Russian Text © A.T. Eprintsev, A.V. Salnikov, A.M. Haba, M.V. Zaichikova, 2013, published in Uspekhi Sovremennoi Biologii, 2013, Vol. 133, No. 6, pp. 550–563.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Eprintsev, A.T., Salnikov, A.V., Haba, A.M. et al. Isocitrate lyase isozymes and their role in organisms with different levels of organization. Biol Bull Rev 4, 323–334 (2014). https://doi.org/10.1134/S2079086414040021

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S2079086414040021

Keywords

Search

Navigation