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Biochemistry (Moscow)

, Volume 80, Issue 13, pp 1655–1671 | Cite as

Carbonyl Stress in Bacteria: Causes and Consequences

  • O. V. Kosmachevskaya
  • K. B. Shumaev
  • A. F. TopunovEmail author
Review

Abstract

Pathways of synthesis of the α-reactive carbonyl compound methylglyoxal (MG) in prokaryotes are described in this review. Accumulation of MG leads to development of carbonyl stress. Some pathways of MG formation are similar for both pro- and eukaryotes, but there are reactions specific for prokaryotes, e.g. the methylglyoxal synthase reaction. This reaction and the glyoxalase system constitute an alternative pathway of glucose catabolism–the MG shunt not associated with the synthesis of ATP. In violation of the regulation of metabolism, the cell uses MG shunt as well as other glycolysis shunting pathways and futile cycles enabling stabilization of its energetic status. MG was first examined as a biologically active metabolic factor participating in the formation of phenotypic polymorphism and hyperpersistent potential of bacterial populations. The study of carbonyl stress is interesting for evolutionary biology and can be useful for constructing highly effective producer strains.

Key words

carbonyl stress bacteria methylglyoxal metabolite overproduction 

Abbreviations

AGEs

advanced glycation end products

DHAP

dihydroxyacetone phosphate

FBA

flux balance analysis

GAPD

glyceraldehyde-3-phosphate dehydrogenase

GloI/GloII and GloIII

glyoxalases I/II and III

G3P

glyceraldehyde-3-phosphate

GSH

reduced glutathione

MG

methylglyoxal

MGS

methylglyoxal synthase

Pi

inorganic phosphate

RCS

reactive carbonyl species

ROS

reactive oxygen species.

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References

  1. 1.
    Baynes, J. W. (1991) Role of oxidative stress in development of complications in diabetes, Diabetes, 40, 405–412.PubMedCrossRefGoogle Scholar
  2. 2.
    Rabbani, N., and Thornalley, P. J. (2012) Glycation research in amino acids: a place to call home, Amino Acids, 42, 1087–1096.PubMedCrossRefGoogle Scholar
  3. 3.
    Maillard, L. C. (1912) Action des acids amine sur les sucres: formation des melanoidines per voie methodique, C. R. Acad. Sci., 154, 66–68.Google Scholar
  4. 4.
    Hodge, J. E., and Rist, C. E. (1952) N-Glycosyl derivatives of secondary amines, J. Amer. Chem. Soc., 74, 1494–1497.CrossRefGoogle Scholar
  5. 5.
    Rahbar, S. (1968) An abnormal hemoglobin in red cells of diabetics, Clin. Chim. Acta, 22, 296–298.PubMedCrossRefGoogle Scholar
  6. 6.
    Thornalley, P. (2005) Dicarbonyl intermediates in the Maillard reaction, Ann. N. Y. Acad. Sci., 1043, 111–117.PubMedCrossRefGoogle Scholar
  7. 7.
    Mironova, R., Niwa, T., Hayashi, H., Dimitrova, R., and Ivanov, I. (2001) Evidence for nonenzymatic glycosylation in Escherichia coli, Mol. Microbiol., 39, 1061–1068.PubMedCrossRefGoogle Scholar
  8. 8.
    Pepper, E. (2007) Mechanisms of Long-Term Survival in Escherichia coli: PhD thesis (Molecular Biology), University of Southern California, USA, p. 138.Google Scholar
  9. 9.
    Cooper, R. A., and Anderson, A. (1970) The formation and catabolism of methylglyoxal during glycolysis in Escherichia coli, FEBS Lett., 11, 273–276.PubMedCrossRefGoogle Scholar
  10. 10.
    Yim, H. S., Kang, S. O., Hah, Y. C., Chock, P. B., and Yim, M. B. (1995) Free radicals generated during the gly-cation reaction of amino acids by methylglyoxal. A model study of protein-cross-linked free radicals, J. Biol. Chem., 270, 28228–28233.PubMedCrossRefGoogle Scholar
  11. 11.
    Nohara, Y., Usui, T., Kinoshita, T., and Watanabe, M. (2002) Generation of superoxide anions during the reaction of guanidine compounds with methylglyoxal, Chem. Pharm. Bull. (Tokyo), 50, 179–184.CrossRefGoogle Scholar
  12. 12.
    Desai, K. M., and Wu, L. (2008) Free radical generation by methylglyoxal in tissues, Drug Metab. Drug Interact., 23, 151–173.CrossRefGoogle Scholar
  13. 13.
    Kalapos, M. P. (2008) The tandem of free radicals and methylglyoxal, Chem. Biol. Interact., 171, 251–271.PubMedCrossRefGoogle Scholar
  14. 14.
    Shumaev, K. B., Gubkina, S. A., Kumskova, E. M., Shepel’kova, G. S., Ruuge, E. K., and Lankin, V. Z. (2009) Mechanism for the superoxide radical formation upon L-lysine interaction with dicarbonyl compounds, Biochemistry (Moscow), 74, 461–466.CrossRefGoogle Scholar
  15. 15.
    Fravel, H. N., and McBrien, B. C. (1980) The effect of methylglyoxal on cell division and the synthesis of protein and DNA in synchronous and asynchronous cultures of Escherichia coli B/r, J. Gen. Microbiol., 117, 127–134.Google Scholar
  16. 16.
    Ferguson, G. P., and Booth, I. R. (1998) Importance of glutathione for growth and survival of Escherichia coli cells: detoxification of methylglyoxal and maintenance of intra-cellular K+, J. Bacteriol., 180, 4314–4318.PubMedPubMedCentralGoogle Scholar
  17. 17.
    MacLean, M. J., Ness, L. S., Ferguson, G. P., and Booth, I. R. (1998) The role of glyoxalase I in the detoxification of methylglyoxal and in the activation of the KefB K+ efflux system in Escherichia coli, Mol. Microbiol., 27, 563–571.PubMedCrossRefGoogle Scholar
  18. 18.
    Kizil, G., Wilks, K., Wells, D., and Ala’Aldeen, D. A. (2000) Detection and characterization of the genes encod-ing glyoxalase I and II from Neisseria meningitides, J. Med. Microbiol., 49, 669–673.PubMedCrossRefGoogle Scholar
  19. 19.
    Sukdeo, N., and Honek, J. F. (2008) Microbial glyoxalase enzymes: metalloenzymes controlling cellular levels of methylglyoxal, Drug Metab. Drug Interact., 23, 29–50.CrossRefGoogle Scholar
  20. 20.
    Kline, E. S., and Mahler, H. R. (1965) The lactic dehydro-genases of E. coli, Ann. N. Y. Acad. Sci., 119, 905–919.PubMedCrossRefGoogle Scholar
  21. 21.
    Gaballa, A., Newton, G. L., Antelmann, H., Parsonage, D., Upton, H., Rawat, M., Claiborne, A., Fahey, R. C., and Helmann, J. D. (2010) Biosynthesis and functions of bacillithiol, a major low-molecular-weight thiol in bacilli, Proc. Natl. Acad. Sci. USA, 107, 6482–6486.PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Chandrangsu, P., Dusi, R., Hamilton, C. J., and Helmann, J. D. (2014) Methylglyoxal resistance in Bacillus subtilis: contributions of bacillithiol-dependent and independent pathways, Mol. Microbiol., 91, 706–715.PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Newton, G. L., Buchmeier, N., and Fahey, R. C. (2008) Biosynthesis and functions of mycothiol, the unique pro-tective thiol of Actinobacteria, Microbiol. Mol. Biol. Rev., 72, 471–494.PubMedPubMedCentralCrossRefGoogle Scholar
  24. 24.
    Oren, A., and Gurevich, P. (1995) Occurrence of the methylglyoxal bypass in halophilic Archaea, FEMS Microbiol. Lett., 125, 83–87.CrossRefGoogle Scholar
  25. 25.
    Newton, G. L., Fahey, R. C., and Rawat, M. (2012) Detoxification of toxins by bacillithiol in Staphylococcus aureus, Microbiology, 158, 1117–1126.PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Korithoski, B., Levesque, C. M., and Cvitkovitch, D. G. (2007) Involvement of the detoxifying enzyme lactoylglu-tathione lyase in Streptococcus mutans aciduricity, J. Bacteriol., 189, 7586–7592.PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Chakraborty, S., Gogoi, M., and Chakravortty, D. (2015) Lactoylglutathione lyase, a critical enzyme in methylglyox-al detoxification, contributes to survival of Salmonella in the nutrient rich environment, Virulence, 6, 50–65.PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Marmstal, E., and Mannervik, B. (1979) Purification, characterization and kinetic studies of glyoxalase-I from rat liver, Biochim. Biophys. Acta, 566, 362–370.PubMedCrossRefGoogle Scholar
  29. 29.
    Shih, M. J., Edinger, J. W., and Creighton, D. J. (1997) Diffusion-dependent kinetic properties of glyoxalase I and estimates of the steady-state concentrations of glyoxalase-pathway intermediates in glycolyzing erythrocytes, Eur. J. Biochem., 244, 852–857.PubMedCrossRefGoogle Scholar
  30. 30.
    Misra, K., Banerjee, A. B., Ray, S., and Ray, M. (1995) Glyoxalase-III from Escherichia coli–a single novel enzyme for the conversion of methylglyoxal into D-lactate without reduced glutathione, Biochem. J., 305, 999–1003.PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Subedi, K. P., Choi, D., Kim, I., Min, B., and Park, C. (2011) Hsp31 of Escherichia coli K-12 is glyoxalase III, Mol. Microbiol., 81, 926–936.PubMedCrossRefGoogle Scholar
  32. 32.
    Benov, L., Sequeira, F., and Beema, A. F. (2004) Role of rpoS in the regulation of glyoxalase III in Escherichia coli, Acta Biochim. Pol., 51, 857–860.PubMedGoogle Scholar
  33. 33.
    Szwergold, B. S. (2013) Maillard reactions in hyperther-mophilic Archaea: implications for better understanding of non-enzymatic glycation in biology, Rejuvenation Res., 16, 259–272.PubMedCrossRefGoogle Scholar
  34. 34.
    Totemeyer, S., Booth, N. A., Nichols, W. W., Dunbar, B., and Booth, I. R. (1998) From famine to feast: the role of methylglyoxal production in Escherichia coli, Mol. Microbiol., 27, 553–562.PubMedCrossRefGoogle Scholar
  35. 35.
    Cooper, R. A. (1984) Metabolism of methylglyoxal in microorganisms, Annu. Rev. Microbiol., 38, 49–68.PubMedCrossRefGoogle Scholar
  36. 37.
    Hopper, D. J., and Cooper, R. A. (1971) The regulation of Escherichia coli methylglyoxal synthase: a new control of glycolysis, FEBS Lett., 13, 213–216.PubMedCrossRefGoogle Scholar
  37. 38.
    Freedberg, W. B., Kistler, W. S., and Lin, E. C. (1971) Lethal synthesis of methylglyoxal by Escherichia coli during unregulated glycerol metabolism, J. Bacteriol., 108, 137–144.PubMedPubMedCentralGoogle Scholar
  38. 39.
    Booth, I. R., Ferguson, G. P., Miller, S., Li, C., Gunasekera, B., and Kinghorn, S. (2003) Bacterial pro-duction of methylglyoxal: a survival strategy or death by misadventure? Biochem. Soc. Trans., 31, 1406–1408.PubMedCrossRefGoogle Scholar
  39. 40.
    Ferguson, G. P., Chacko, A. D., Lee, C., and Booth, I. R. (1996) The activity of the high-affinity K+ uptake system Kdp sensitizes cells of Escherichia coli to methylglyoxal, J. Bacteriol., 178, 3957–3961.PubMedPubMedCentralGoogle Scholar
  40. 41.
    Ferguson, G. P. (1999) Protective mechanisms against toxic electrophiles in Escherichia coli, Trends Microbiol., 7, 242–247.PubMedCrossRefGoogle Scholar
  41. 42.
    Russell, J. B. (2007) The energy spilling reactions of bacte-ria and other organisms, J. Mol. Microbiol. Biotechnol., 13, 1–11.PubMedCrossRefGoogle Scholar
  42. 43.
    Igamberdiev, A. U. (1995) Logic in Organization of Living Systems [in Russian], Voronezh University Press, Voronezh.Google Scholar
  43. 44.
    Qian, H., and Beard, D. A. (2006) Metabolic futile cycles and their functions: a systems analysis of energy and con-trol, Syst. Biol. (Stevenage), 153, 192–200.CrossRefGoogle Scholar
  44. 45.
    D’Ari, R., and Casadesus, J. (1998) Underground metabo-lism, Bioessays, 20, 181–186.PubMedCrossRefGoogle Scholar
  45. 46.
    Notebaarta, R. A., Szappano, B., Kintses, B., Pal, F., Gyorkei, A., Bogos, B., Lazar, V., Spohn, R., Csorgo, B., Wagner, A., Ruppin, E., Pal, C., and Papp, B. (2014) Network-level architecture and the evolutionary potential of underground metabolism, Proc. Natl. Acad. Sci. USA, 111, 11762–11767.CrossRefGoogle Scholar
  46. 47.
    Ozyamak, E., Black, S. S., Walker, C. A., Maclean, M. J., Bartlett, W., Miller, S., and Booth, I. R. (2010) The critical role of S-lactoylglutathione formation during methylglyox-al detoxification in Escherichia coli, Mol. Microbiol., 78, 1577–1590.PubMedPubMedCentralCrossRefGoogle Scholar
  47. 48.
    Mitsumoto, A., Kim, K. R., Oshima, G., Kunimoto, M., Okawa, K., Iwamatsu, A., and Nakagawa, Y. (1999) Glyoxalase I is a novel nitric-oxide-responsive protein, Biochem. J., 344, 837–844.PubMedPubMedCentralCrossRefGoogle Scholar
  48. 49.
    Mitsumoto, A., Kim, K. R., Oshima, G., Kunimoto, M., Okawa, K., Iwamatsu, A., and Nakagawa, Y. (2000) Nitric oxide inactivates glyoxalase I in cooperation with glu-tathione, J. Biochem., 128, 647–654.PubMedCrossRefGoogle Scholar
  49. 50.
    Sahoo, R., Sengupta, R., and Ghosh, S. (2003) Nitrosative stress on yeast: inhibition of glyoxalase-I and glyceralde-hyde-3-phosphate dehydrogenase in the presence of GSNO, Biochem. Biophys. Res. Commun., 302, 665–670.PubMedCrossRefGoogle Scholar
  50. 51.
    Birkenmeier, G., Stegemann, C., Hoffmann, R., Gunther, R., Huse, K., and Birkemeyer, C. (2010) Posttranslational modification of human glyoxalase 1 indicates redox-dependent regulation, PLoS One, 5, e10399.PubMedPubMedCentralCrossRefGoogle Scholar
  51. 52.
    De Hemptinne, V., Rondas, D., Toepoel, M., and Vancompernolle, K. (2009) Phosphorylation on Thr106 and NO-modification of glyoxalase I suppress the TNF-induced transcriptional activity of NF-κB, Mol. Cell Biochem., 325, 169–178.PubMedCrossRefGoogle Scholar
  52. 53.
    Zhu, M. M., Skraly, F. A., and Cameron, D. C. (2001) Accumulation of methylglyoxal in anaerobically grown Escherichia coli and its detoxification by expression of the Pseudomonas putida glyoxalase I gene, Metab. Eng., 3, 218–225.PubMedCrossRefGoogle Scholar
  53. 54.
    Trujillo, C., Blumenthal, A., Marrero, J., Rhee, K. Y., Schnappinger, D., and Ehrt, S. (2014) Triosephosphate iso-merase is dispensable in vitro yet essential for Mycobacterium tuberculosis to establish infection, MBio, 5, e00085.PubMedPubMedCentralCrossRefGoogle Scholar
  54. 55.
    Hipkiss, A. R. (2011) Energy metabolism and ageing regu-lation: metabolically driven deamidation of triosephos-phate isomerase may contribute to proteostatic dysfunc-tion, Ageing Res. Rev., 10, 498–502.PubMedCrossRefGoogle Scholar
  55. 56.
    Beisswenger, P. J., Howell, S. K., Smith, K., and Szwergold, B. S. (2003) Glyceraldehyde-3-phosphate dehydrogenase activity as an independent modifier of methylglyoxal levels in diabetes, Biochim. Biophys. Acta, 1637, 98–106.PubMedCrossRefGoogle Scholar
  56. 57.
    Kadner, R. J., Murphy, G. P., and Stephens, C. M. (1992) Two mechanisms for growth inhibition by elevated trans-port of sugar phosphates in Escherichia coli, J. Gen. Microbiol., 138, 2007–2014.PubMedCrossRefGoogle Scholar
  57. 58.
    Bond, D. R., and Russell, J. B. (1996) A role for fructose 1,6-diphosphate in the ATPase-mediated energy-spilling reaction of Streptococcus bovis, Appl. Environ. Microbiol., 62, 2095–2099.PubMedPubMedCentralGoogle Scholar
  58. 59.
    Kim, I., Kim, E., Yoo, S., Shin, D., Min, B., Song, J., and Park, C. (2004) Ribose utilization with an excess of mutarotase causes cell death due to accumulation of methylglyoxal, J. Bacteriol., 186, 7229–7235.PubMedPubMedCentralCrossRefGoogle Scholar
  59. 60.
    Bond, D. R., and Russell, J. B. (1998) Relationship between intracellular phosphate, proton motive force, and rate of nongrowth energy dissipation (energy spilling) in Streptococcus bovis JB1, Appl. Environ. Microbiol., 64, 976–981.PubMedPubMedCentralGoogle Scholar
  60. 61.
    Cook, G. M., and Russell, J. B. (1994) Energy-spilling reactions of Streptococcus bovis and resistance of its mem-brane to proton conductance, Appl. Environ. Microbiol., 60, 1942–1948.PubMedPubMedCentralGoogle Scholar
  61. 62.
    Weber, J., Kayser, A., and Rinas, U. (2005) Metabolic flux analysis of Escherichia coli in glucose-limited continuous culture. II. Dynamic response to famine and feast, activa-tion of the methylglyoxal pathway and oscillatory behavior, Microbiology, 151, 707–716.PubMedCrossRefGoogle Scholar
  62. 63.
    Russell, J. B. (1993) Glucose toxicity in Prevotella rumini-cola: methylglyoxal accumulation and its effect on mem-brane physiology, Appl. Environ. Microbiol., 59, 2844–2850.PubMedPubMedCentralGoogle Scholar
  63. 64.
    Kosmachevskaya, O. V., and Topunov, A. F. (2009) Existence of glycated leghemoglobin–hemoglobin of legume plants, IMARS Highlights, 4, 10–13.Google Scholar
  64. 65.
    Kosmachevskaya, O. V., and Topunov, A. F. (2010) Formation of glycated recombinant leghemoglobin in Escherichia coli cells, Appl. Biochem. Microbiol., 46, 297–302.CrossRefGoogle Scholar
  65. 66.
    Mironova, R., Niwa, T., Dimitrova, R., Boyanov, M., and Ivanov, I. (2003) Glycation and posttranslational process-ing of human interferon gamma expressed in Escherichia coli, J. Biol. Chem., 278, 51068–51074.PubMedCrossRefGoogle Scholar
  66. 67.
    Mironova, R., Niwa, T., Handzhiyski, Y., Sredovska, A., and Ivanov, I. (2005) Glycation and post-translational pro-cessing of human interferon-gamma expressed in Escherichia coli, J. Biol. Chem., 278, 51068–51074.CrossRefGoogle Scholar
  67. 68.
    Maiden, M. F. J., Pham, C., and Kashket, S. (2004) Glucose toxicity effect and accumulation of methylglyoxal by the periodontal pathogen Bacteroides forsythus, Anaerobe, 10, 27–32.PubMedCrossRefGoogle Scholar
  68. 69.
    Richard, J. P. (1993) Mechanism for the formation of methylglyoxal from triosephosphates, Biochem. Soc. Trans., 21, 549–553.PubMedCrossRefGoogle Scholar
  69. 70.
    Phillips, S. A., and Thornalley, P. J. (1993) The formation of methylglyoxal from triose phosphates. Investigation using a specific assay for methylglyoxal, Eur. J. Biochem., 212, 101–105.PubMedCrossRefGoogle Scholar
  70. 71.
    Ationu, A., and Humphries, A. (1998) The feasibility of replacement therapy for inherited disorder of glycolysis: triosephosphate isomerase deficiency, Int. J. Mol. Med., 2, 701–704.PubMedGoogle Scholar
  71. 72.
    Ahmed, N., Battah, S., Karachalias, N., Babaei-Jadidi, R., Horanyi, M., Baroti, K., Hollan, S., and Thornalley, P. J. (2003) Increased formation of methylglyoxal and protein glycation, oxidation and nitrosation in triosephosphate iso-merase deficiency, Biochim. Biophys. Acta, 1639, 121–132.PubMedCrossRefGoogle Scholar
  72. 73.
    Orosz, F., Olah, J., and Ovadi, J. (2009) Triosephosphate isomerase deficiency: new insights into an enigmatic dis-ease, Biochim. Biophys. Acta, 1792, 1168–1174.PubMedCrossRefGoogle Scholar
  73. 74.
    Selvamani, V. R. S., Telaar, M., Friehs, K., and Flaschel, E. (2014) Antibiotic-free segregational plasmid stabilization in Escherichia coli owing to the knockout of triosephos-phate isomerase (tpiA), Microb. Cell Fact., 13, 58.CrossRefGoogle Scholar
  74. 75.
    Solem, C., Koebmann, B., and Jensen, P. R. (2008) Control analysis of the role of triosephosphate isomerase in glucose metabolism in Lactococcus lactis, IET Syst. Biol., 2, 64–72.PubMedCrossRefGoogle Scholar
  75. 76.
    Souza, J. M., and Radi, R. (1998) Glyceraldehyde-3-phos-phate dehydrogenase inactivation by peroxynitrite, Arch. Biochem. Biophys., 360, 187–194.PubMedCrossRefGoogle Scholar
  76. 77.
    Mohr, S., Stamler, J. S., and Brune, B. (1994) Mechanism of covalent modification of glyceraldehyde-3-phosphate dehy-drogenase at its active site thiol by nitric oxide, peroxynitrite and related nitrosating agents, FEBS Lett., 348, 223–227.PubMedCrossRefGoogle Scholar
  77. 78.
    Padgett, C. M., and Whorton, A. R. (1995) S-Nitrosoglutathione reversibly inhibits GAPDH by S-nitro-sylation, Am. J. Physiol., 269, 739–749.Google Scholar
  78. 79.
    Galli, F., Rovidati, S., Ghibelli, L., and Canestrari, F. (1998) S-Nitrosylation of glyceraldehyde-3-phosphate dehydrogenase decreases the enzyme affinity to the ery-throcyte membrane, Nitric Oxide, 2, 17–27.PubMedCrossRefGoogle Scholar
  79. 80.
    Mohr, S., Hallak, H., De Boitte, A., Lapetina, E. G., and Brune, B. (1999) Nitric oxide-induced S-glutathionylation and inactivation of glyceraldehyde-3-phosphate dehydro-genase, J. Biol. Chem., 274, 9427–9430.PubMedCrossRefGoogle Scholar
  80. 81.
    Ishii, T., Sunami, O., Nakajima, H., Nishio, H., Takeuchi, T., and Hata, F. (1999) Critical role of sulfenic acid forma-tion of thiols in the inactivation of glyceraldehyde-3-phos-phate dehydrogenase by nitric oxide, Biochem. Pharmacol., 58, 133–143.PubMedCrossRefGoogle Scholar
  81. 82.
    Leoncini, G., Maresca, M., and Bonsignore, A. (1980) The effect of methylglyoxal on the glycolytic enzymes, FEBS Lett., 117, 17–18.PubMedCrossRefGoogle Scholar
  82. 83.
    Morgan, P. E., Dean, R. T., and Davies, M. J. (2002) Inactivation of cellular enzymes by carbonyls and protein-bound glycation glycoxidation products, Arch. Biochem. Biophys., 403, 259–269.PubMedCrossRefGoogle Scholar
  83. 84.
    Diaz-Ruiz, R., Rigoulet, M., and Devin, A. (2011) The Warburg and Crabtree effects: on the origin of cancer cell energy metabolism and of yeast glucose repression, Biochim. Biophys. Acta, 1807, 568–576.PubMedCrossRefGoogle Scholar
  84. 85.
    Magasanik, B. (1961) Catabolite repression, Cold Spring Harb. Symp. Quant. Biol., 26, 249–256.PubMedCrossRefGoogle Scholar
  85. 86.
    Pastan, I., and Perlman, R. (1970) Cyclic adenosine monophosphate in bacteria, Science, 169, 339–344.PubMedCrossRefGoogle Scholar
  86. 87.
    Ackerman, R. S., Cozzarelli, N. R., and Epstein, W. (1974) Accumulation of toxic concentrations of methylglyoxal by wild-type Escherichia coli K-12, J. Bacteriol., 119, 357–362.PubMedPubMedCentralGoogle Scholar
  87. 88.
    Bachi, B., and Kornberg, H. L. (1975) Utilization of glu-conate by Escherichia coli. A role of adenosine 3′:5′-cyclic monophosphate in the induction of gluconate catabolism, Biochem. J., 150, 123–128.PubMedPubMedCentralCrossRefGoogle Scholar
  88. 89.
    Peekhaus, N., and Conway, T. (1998) What’s for dinner? Entner–Doudoroff metabolism in Escherichia coli, J. Bacteriol., 180, 3495–3502.PubMedPubMedCentralGoogle Scholar
  89. 90.
    Puskas, R., Fredd, N., Gazdar, C., and Peterkofsky, A. (1983) Methylglyoxal-mediated growth inhibition in an Escherichia coli cAMP receptor protein mutant, Arch. Biochem. Biophys., 223, 503–513.PubMedCrossRefGoogle Scholar
  90. 91.
    Burke, R. M., and Tempest, D. W. (1990) Growth of Bacillus stearothermophilus on glycerol in chemostat cul-ture: expression of an unusual phenotype, J. Gen. Microbiol., 136, 1381–1385.PubMedCrossRefGoogle Scholar
  91. 92.
    Russell, J. B., and Cook, G. M. (1995) Energetics of bac-terial growth: balance of anabolic and catabolic reactions, Microbiol. Rev., 59, 48–62.PubMedPubMedCentralGoogle Scholar
  92. 93.
    Xu, D., Liu, X., Guo, C., and Zhao, J. (2006) Methylglyoxal detoxification by an aldo-keto reductase in the cyanobacterium Synechococcus sp. PCC 7002, Microbiology, 152, 2013–2021.PubMedCrossRefGoogle Scholar
  93. 94.
    Koobs, D. H. (1972) Phosphate mediation of the Crabtree and Pasteur effects, Science, 178, 127–133.PubMedCrossRefGoogle Scholar
  94. 95.
    Iddar, A., Valverde, F., Assobhei, O., Serrano, A., and Soukri, A. (2005) Widespread occurrence of non-phos-phorylating glyceraldehyde-3-phosphate dehydrogenase among Gram-positive bacteria, Int. Microbiol., 8, 251–258.PubMedGoogle Scholar
  95. 96.
    Ito, F., Miyake, M., Fushinobu, S., Nakamura, S., Shimizu, K., and Wakagi, T. (2014) Engineering the allosteric properties of archaeal non-phosphorylating glyc-eraldehyde-3-phosphate dehydrogenases, Biochim. Biophys. Acta, 1844, 759–766.PubMedCrossRefGoogle Scholar
  96. 97.
    Dan’shina, P. V., Schmalhausen, E. V., Arutiunov, D. Y., Pleten’, A. P., and Muronetz, V. I. (2003) Acceleration of glycolysis in the presence of the non-phosphorylating and the oxidized phosphorylating glyceraldehyde-3-phosphate dehydrogenases, Biochemistry (Moscow), 68, 593–600.CrossRefGoogle Scholar
  97. 98.
    Danshina, P. V., Schmalhausen, E. V., Avetisyan, A. V., and Muronetz, V. I. (2001) Mildly oxidized glyceralde-hyde-3-phosphate dehydrogenase as a possible regulator of glycolysis, IUBMB Life, 51, 309–314.PubMedCrossRefGoogle Scholar
  98. 99.
    Crabtree, H. G. (1929) Observations on the carbohydrate metabolism of tumors, Biochem. J., 23, 536–545.PubMedPubMedCentralCrossRefGoogle Scholar
  99. 100.
    Vemuri, G. N., Altman, E., Sangurdekar, D. P., Khodursky, A. B., and Eiteman, M. A. (2006) Overflow metabolism in Escherichia coli during steady-state growth: transcriptional regulation and effect of the redox ratio, Appl. Environ. Microbiol., 72, 3653–3661.PubMedPubMedCentralCrossRefGoogle Scholar
  100. 101.
    Paczia, N., Nilgen, A., Lehmann, T., Gatgens, J., Wiechert, W., and Noack, S. (2012) Extensive exometabolome analysis reveals extended overflow metab-olism in various microorganisms, Microb. Cell Fact., 122, 1–14.Google Scholar
  101. 102.
    Molenaar, D., Van Berlo, R., De Ridder, D., and Teusink, B. (2009) Shifts in growth strategies reflect tradeoffs in cel-lular economics, Mol. Syst. Biol., 5, 323.PubMedPubMedCentralCrossRefGoogle Scholar
  102. 103.
    Evtodienko, Y. V., and Teplova, V. V. (1996) Biological sig-nificance and mechanisms of Crabtree effect in rapidly proliferating cells. Role of Ca2+ ions, Biochemistry (Moscow), 61, 1423–1431.Google Scholar
  103. 104.
    Lele, U. N., and Watve, M. G. (2014) Bacterial growth rate and growth yield: is there a relationship? Proc. Ind. Natl. Sci. Acad., 80, 537–546.CrossRefGoogle Scholar
  104. 105.
    Travisano, M., and Velicer, G. J. (2004) Strategies of microbial cheater control, Trends Microbiol., 12, 72–78.PubMedCrossRefGoogle Scholar
  105. 106.
    Kreft, J. U., and Bonhoeffer, S. (2005) The evolution of groups of cooperating bacteria and the growth rate versus yield trade-off, Microbiology, 151, 637–641.PubMedCrossRefGoogle Scholar
  106. 107.
    Pfeiffer, T., and Morley, A. (2014) An evolutionary per-spective on the Crabtree effect, Front. Mol. Biosci., 21, 1–6.Google Scholar
  107. 108.
    Shimizu, K. (2014) Regulation systems of bacteria such as Escherichia coli in response to nutrient limitation and environmental stresses, Metabolites, 4, 1–35.PubMedCentralCrossRefGoogle Scholar
  108. 109.
    Sharma, P., Hellingwerf, K. J., De Mattos, M. J. T., and Bekker, M. (2012) Uncoupling of substrate-level phospho-rylation in Escherichia coli during glucose-limited growth, Appl. Environ. Microbiol., 78, 6908–6913.PubMedPubMedCentralCrossRefGoogle Scholar
  109. 110.
    Lowry, O. H., Carter, J., Ward, J. B., and Glaser, L. (1971) The effect of carbon and nitrogen sources on the level of metabolic intermediates in Escherichia coli, J. Biol. Chem., 246, 6511–6521.PubMedGoogle Scholar
  110. 111.
    Schaefer, U., Boos, W., Takors, R., and Weuster-Botz, D. (1999) Automated sampling device for monitoring intra-cellular metabolite dynamics, Anal. Biochem., 270, 88–96.PubMedCrossRefGoogle Scholar
  111. 112.
    Chassagnole, C., Noisommit-Rizzi, N., Schmid, J. W., Mauch, K., and Reuss, M. (2002) Dynamic modeling of the central carbon metabolism of Escherichia coli, Biotechnol. Bioeng., 79, 53–73.PubMedCrossRefGoogle Scholar
  112. 113.
    Russell, J. B. (1992) Glucose toxicity and inability of Bacteroides ruminicola to regulate glucose transport and utilization, Appl. Environ. Microbiol., 58, 2040–2045.PubMedPubMedCentralGoogle Scholar
  113. 114.
    Emmerling, M., Dauner, M., Ponti, A., Fiaux, J., Hochuli, M., Szyperski, T., Wuthrich, K., Bailey J. E., and Sauer, U. (2002) Metabolic flux responses to pyruvate kinase knock-out in Escherichia coli, J. Bacteriol., 184, 152–164.PubMedPubMedCentralCrossRefGoogle Scholar
  114. 115.
    Sanden, A. M., Prytz, I., Tubulekas, I., Forberg, C., Le, H., Hektor, A., Neubauer, P., Pragai, Z., Harwood, C., Ward, A., Picon, A., De Mattos, T. J., Postma, P., Farewell, A., Nystrom, T., Reeh, S., Pedersen, S., and Larsson, G. (2003) Limiting factors in Escherichia coli fed-batch production of recombinant proteins, Biotechnol. Bioeng., 81, 158–166.PubMedCrossRefGoogle Scholar
  115. 116.
    Sikorski, M. M., Topunov, A. F., Strozycki, P., Vorgias, C. E., Wilson, K. S., and Legocki, A. B. (1995) Cloning and expression of plant leghemoglobin cDNA of Lupinus luteus in Escherichia coli and purification of the recombinant protein, Plant Sci., 108, 109–117.CrossRefGoogle Scholar
  116. 117.
    Wang, H., Wang, F., Wang, W., Yao, X., Wei, D., Cheng, H., and Deng, Z. (2014) Improving the expression of recombinant proteins in E. coli BL21 (DE3) under acetate stress: an alkaline pH shift approach, PLoS One, 9, e112777.Google Scholar
  117. 118.
    Kosmachevskaya, O. V., Shumaev, K. B., Nasybullina, E. I., Gubkina, S. A., and Topunov, A. F. (2013) Interaction of S-nitrosoglutathione with methemoglobin under condi-tions of modeling carbonyl stress, Hemoglobin, 37, 205–218.PubMedCrossRefGoogle Scholar
  118. 119.
    Kosmachevskaya, O. V., Shumaev, K. B., Nasybullina, E. I., and Topunov, A. F. (2014) Formation of nitri-and nitrosylhemoglobin in systems modeling the Maillard reaction, Clin. Chem. Lab. Med., 52, 161–168.PubMedCrossRefGoogle Scholar
  119. 120.
    Maiden, M. F. J., Pham, C., and Kashket, S. (2004) Glucose toxicity effect and accumulation of methylglyoxal by the periodontal pathogen Bacteroides forsythus, Anaerobe, 10, 27–32.PubMedCrossRefGoogle Scholar
  120. 121.
    Bechara, E. J., Dutra, F., Cardoso, V. E., Sartori, A., Olympio, K. P., Penatti, C. A., Adhikari, A., and Assuncao, N. A. (2007) The dual face of endogenous α-aminoketones: pro-oxidizing metabolic weapons, Comp. Biochem. Physiol. C. Toxicol. Pharmacol., 146, 88–110.PubMedCrossRefGoogle Scholar
  121. 122.
    Mathys, K. C., Ponnampalam, S. N., Padival, S., and Nagaraj, R. H. (2002) Semicarbazide-sensitive amine oxi-dase in aortic smooth muscle cells mediates synthesis of a methylglyoxal-AGE: implications for vascular complica-tions in diabetes, Biochem. Biophys. Res. Commun., 297, 863–869.PubMedCrossRefGoogle Scholar
  122. 123.
    O’Sullivan, J., Unzeta, M., Healy, J., O’Sullivan, M. I., Davey, G., and Tipton, K. F. (2004) Semicarbazide-sensi-tive amine oxidases: enzymes with quite a lot to do, Neurotoxicology, 25, 303–315.PubMedCrossRefGoogle Scholar
  123. 124.
    Sartori, A., Mano, C. M., Mantovani, M. C., Dyszy, F. H., Massari, J., Tokikawa, R., Nascimento, O. R., Nantes, I. L., and Bechara, E. J. (2013) Ferricytochrome c directly oxidizes aminoacetone to methylglyoxal, a catabolite accumulated in carbonyl stress, PLoS One, 8, e57790.Google Scholar
  124. 125.
    Dutra, F., Knudsen, F. S., Curi, D., and Bechara, E. J. H. (2001) Aerobic oxidation of aminoacetone, a threonine catabolite: iron catalysis and coupled iron release from fer-ritin, Chem. Res. Toxicol., 14, 1323–1329.PubMedCrossRefGoogle Scholar
  125. 126.
    Turner, J. M. (1966) Microbial metabolism of amino ketones. Aminoacetone formation from 1-aminopropan-2-ol by a dehydrogenase in Escherichia coli, Biochem. J., 99, 427–433.PubMedCentralCrossRefGoogle Scholar
  126. 127.
    Boylan, S. A., and Dekker, E. E. (1981) L-threonine dehy-drogenase of Escherichia coli K-12, J. Biol. Chem., 256, 1809–1815.PubMedGoogle Scholar
  127. 128.
    Elliott, W. H. (1960) Aminoacetone formation by Staphylococcus aureus, Biochem. J., 74, 478–485.PubMedPubMedCentralCrossRefGoogle Scholar
  128. 129.
    Green, M. L., and Elliott, W. H. (1964) The enzymic for-mation of aminoacetone from threonine and its further metabolism, Biochem. J., 92, 537–549.PubMedPubMedCentralCrossRefGoogle Scholar
  129. 130.
    Neuberger, A., and Tait, G. H. (1962) Production of aminoacetone by Rhodopseudomonas spheroids, Biochem. J., 84, 317–328.PubMedPubMedCentralCrossRefGoogle Scholar
  130. 131.
    Faulkner, A., and Turner, J. M. (1974) Microbial metabo-lism of amino alcohols. Aminoacetone metabolism via 1-aminopropan-2-ol in Pseudomonas sp. N.C.I.B. 8858, Biochem. J., 138, 263–276.PubMedPubMedCentralCrossRefGoogle Scholar
  131. 132.
    Green, M. L., and Lewis, J. B. (1968) The oxidation of aminoacetone by a species of Arthrobacter, Biochem. J., 106, 267–270.PubMedPubMedCentralCrossRefGoogle Scholar
  132. 133.
    Rahhar, D. A., Turner, J. M., and Willetts, A. I. (1967) The role of aminoacetone in L-threonine metabolism by Bacillus subtilis, Biochem. J., 103, 73–73.CrossRefGoogle Scholar
  133. 134.
    Willets, A. J., and Turner, J. M. (1970). Threonine metab-olism in a strain of Bacillus subtilis: enzymic oxidation of the intermediate DL-lactaldehyde, Biochim. Biophys. Acta, 222, 234–236.CrossRefGoogle Scholar
  134. 135.
    Machielsen, R., and Van der Oost, J. (2006) Production and characterization of a thermostable L-threonine dehy-drogenase from the hyperthermophilic archaeon Pyrococcus furiosus, FEBS J., 273, 2722–2729.PubMedCrossRefGoogle Scholar
  135. 136.
    Bell, S. C., and Turner, J. M. (1976) Bacterial catabolism of threonine. Threonine degradation initiated by L-threo-nine NAD+ oxidoreductase, Biochem. J., 156, 449–458.PubMedPubMedCentralCrossRefGoogle Scholar
  136. 137.
    Newman, E. B., Kapoor, V., and Potter, R. (1976) Role of L-threonine dehydrogenase in the catabolism of threonine and synthesis of glycine by Escherichia coli, J. Bacteriol., 126, 1245–1249.PubMedPubMedCentralGoogle Scholar
  137. 138.
    Potter, R., Kapoor, V., and Newman, E. B. (1977) Role of threonine dehydrogenase in Escherichia coli threonine degradation, J. Bacteriol., 132, 385–391.PubMedPubMedCentralGoogle Scholar
  138. 139.
    Tressel, T., Thompson, R., Zieske, L. R., Menendez, M. I., and Davis, L. (1986) Interaction between L-threonine dehydrogenase and aminoacetone synthetase and mecha-nism of aminoacetone production, J. Biol. Chem., 261, 16428–16437.PubMedGoogle Scholar
  139. 140.
    Higgins, I. J., and Turner J. M. (1969) Enzymes of methyl-glyoxal metabolism in a pseudomonad, which rapidly metabolizes aminoacetone, Biochim. Biophys. Acta, 184, 464–467.PubMedCrossRefGoogle Scholar
  140. 141.
    Takors, R., Bathe, B., Rieping, M., Hans, S., Kelle, R., and Huthmacher, K. (2007) Systems biology for industrial strains and fermentation processes–example: amino acids, J. Biotechnol., 129, 181–190.PubMedCrossRefGoogle Scholar
  141. 142.
    Lee, K. H., Park, J. H., Kim, T. Y., Kim, H. U., and Lee, S. Y. (2007) Systems metabolic engineering of Escherichia coli for L-threonine production, Mol. Syst. Biol., 3, 149.Google Scholar
  142. 143.
    Nishikawa, T., Edelstein, D., Du, X. L., Yamagishi, S., Matsumura, T., Kaneda, Y., Yorek, M. A., Beebe, D., Oates, P. J., Hammes, H. P., Giardino, I., and Brownlee, M. (2000) Normalizing mitochondrial superoxide produc-tion blocks three pathways of hyperglycemic damage, Nature, 404, 787–790.PubMedCrossRefGoogle Scholar
  143. 144.
    Xie, L., Eiteman, M. A., and Altman, E. (2003) Production of 5-aminolevulinic acid by an Escherichia coli aminolevulinate dehydratase mutant that overproduces Rhodobacter sphaeroides aminolevulinate synthase, Biotechnol. Lett., 25, 1751–1755.PubMedCrossRefGoogle Scholar
  144. 145.
    Hiraku, Y., and Kawanishi, S. (1999) Involvement of oxidative DNA damage and apoptosis in antitumor actions of amino sugars, Free Radic. Res., 31, 389–403.PubMedCrossRefGoogle Scholar
  145. 146.
    Hiraku, Y., Sugimoto, J., Yamaguchi, T., and Kawanishi, S. (1999) Oxidative DNA damage induced by aminoace-tone, an amino acid metabolite, Arch. Biochem. Biophys., 365, 62–70.PubMedCrossRefGoogle Scholar
  146. 147.
    Szent-Gyorgyi, A., Egyiid, L. G., and McLaughlin, J. A. (1967) Ketoaldehydes and cell division, Science, 155, 539–541.PubMedCrossRefGoogle Scholar
  147. 148.
    Egyud, L. G. (1967) Studies on cell division: the effect of aldehydes, ketones, and α-ketoaldehydes on the prolifera-tion of Escherichia coli, Curr. Mol. Biol., 1, 14–20.Google Scholar
  148. 149.
    Egyud, L. G., and Szent-Gyorgyi, A. (1966) On the regu-lation of cell division, Proc. Natl. Acad. Sci. USA, 56, 203–207.PubMedPubMedCentralCrossRefGoogle Scholar
  149. 150.
    Campbell, A. K., Naseem, R., Holland, I. B., Matthews, S. B., and Wann, K. T. (2007) Methylglyoxal and other carbohydrate metabolites induce lanthanum-sensitive Ca2+-transients and inhibit growth in E. coli, Arch. Biochem. Biophys., 468, 107–113.PubMedCrossRefGoogle Scholar
  150. 151.
    Rosas-Lemus, M., Uribe-Alvarez, C., Chiquete-Felix, N., and Uribe-Carvajal, S. (2014) In Saccharomyces cerevisiae fructose-1,6-bisphosphate contributes to the Crabtree effect through closure of the mitochondrial unspecific channel, Arch. Biochem. Biophys., 555/556, 66–70.CrossRefGoogle Scholar
  151. 152.
    Naseem, R., Davies, S. R., Jones, H., Wann, K., Holland, I. B., and Campbell, A. K. (2007) Cytosolic Ca2+ regulates protein expression in E. coli through release from inclusion bodies, Biochem. Biophys. Res. Commun., 360, 33–39.PubMedCrossRefGoogle Scholar
  152. 153.
    Dhar, N., and McKinney, J. D. (2007) Microbial pheno-typic heterogeneity and antibiotic tolerance, Curr. Opin. Microbiol., 10, 30–38.PubMedCrossRefGoogle Scholar
  153. 154.
    Girgis, H. S., Harrisa, K., and Tavazoiea, S. (2012) Large mutational target size for rapid emergence of bacterial per-sistence, Proc. Natl. Acad. Sci. USA, 109, 12740–12745.PubMedPubMedCentralCrossRefGoogle Scholar
  154. 155.
    Rachman, H., Kim, N., Ulrichs, T., Baumann, S., Pradl, L., Eddine, A. N., Bild, M., Rother, M., Kuban, R.-J., Lee, J. S., Hurwitz, R., Brinkmann, V., Kosmiadi, G. A., and Kaufmann, S. H. E. (2006) Critical role of methylgly-oxal and AGE in mycobacteria-induced macrophage apoptosis and activation, PLoS One, 1, e29.PubMedPubMedCentralCrossRefGoogle Scholar
  155. 156.
    Rachman, H., Strong, M., Ulrichs, T., Grode, L., Schuchhardt, J., Mollenkopf, H., Kosmiadi, G. A., Eisenberg, D., and Kaufmann, S. H. E. (2006) Unique transcriptome signature of Mycobacterium tuberculosis in pulmonary tuberculosis, Infect. Immun., 74, 1233–1242.PubMedPubMedCentralCrossRefGoogle Scholar
  156. 157.
    Gray, M. J., Wholey, W. Y., Parker, B. W., Kim, M., and Jakob, U. (2013) NemR is a bleach-sensing transcription factor, J. Biol. Chem., 288, 13789–13798.PubMedPubMedCentralCrossRefGoogle Scholar
  157. 158.
    Lee, C., Shin, J., and Park, C. (2013) Novel regulatory sys-tem nemRA–gloA for electrophile reduction in Escherichia coli K-12, Mol. Microbiol., 88, 395–412.PubMedCrossRefGoogle Scholar
  158. 159.
    Ozyamak, E., De Almeida, C., De Moura, A. P. S., Miller, S., and Booth, I. R. (2013) Integrated stress response of Escherichia coli to methylglyoxal: transcriptional readthrough from the nemRA operon enhances protection through increased expression of glyoxalase I, Mol. Microbiol., 88, 936–950.PubMedPubMedCentralCrossRefGoogle Scholar
  159. 160.
    Bakker, E. P., and Mangerich, W. E. (1982) N-ethyl-maleimide induces K+-H+ antiport activity in Escherichia coli K-12, FEBS Lett., 140, 177–180.PubMedCrossRefGoogle Scholar
  160. 161.
    Elmore, M. J., Lamb, A. J., Ritchie, G. Y., Douglas, R. M., Munro, A., Gajewska, A., and Booth, I. R. (1990) Activation of potassium efflux from Escherichia coli by glu-tathione metabolites, Mol. Microbiol., 4, 405–412.PubMedCrossRefGoogle Scholar
  161. 162.
    Ferguson, G. P., Munro, A. W., Douglas, R. M., McLaggan, D., and Booth, I. R. (1993) Activation of potassium channels during metabolite detoxification in Escherichia coli, Mol. Microbiol., 9, 1297–1303.PubMedCrossRefGoogle Scholar
  162. 163.
    Miller, S., Ness, L. S., Wood, C. M., Fox, B. C., and Booth, I. R. (2000) Identification of an ancillary protein, YabF, required for activity of the KefC glutathione-gated potassium efflux system in Escherichia coli, J. Bacteriol., 182, 6536–6540.PubMedPubMedCentralCrossRefGoogle Scholar
  163. 164.
    Roosild, T. P., Castronovo, S., Miller. S., Li, C., Rasmussen, T., Bartlett, W., Gunasekera, B., Choe, S., and Booth, I. R. (2009) KTN (RCK) domains regulate K+ channels and transporters by controlling the dimer-hinge conformation, Structure, 17, 893–903.PubMedPubMedCentralCrossRefGoogle Scholar
  164. 165.
    Ozyamak, E., Black, S. S., MacLean, M. J., Bartlett, W., Miller, S., and Booth, I. R. (2011) The critical role of S-lactoylglutathione formation during methylglyoxal detoxi-fication in Escherichia coli, Mol. Microbiol., 78, 1577–1590.CrossRefGoogle Scholar
  165. 166.
    Rekarte, U. D., Zwaig, N., and Isturiz, T. (1973) Accumulation of methylglyoxal in a mutant of Escherichia coli constitutive for gluconate catabolism, J. Bacteriol., 115, 727–731.PubMedPubMedCentralGoogle Scholar
  166. 167.
    Baskaran, S., Rajan, D. P., and Balasubramanian, K. A. (1989) Formation of methylglyoxal by bacteria isolated from human faces, J. Med. Microbiol., 28, 211–215.PubMedCrossRefGoogle Scholar
  167. 168.
    Kashket, S., Maiden, M. F., Haffajee, A. D., and Kashket, E. R. (2003) Accumulation of methylglyoxal in the gingi-val crevicular fluid of chronic periodontitis patients, J. Clin. Periodontol., 30, 364–367.PubMedCrossRefGoogle Scholar
  168. 169.
    Chakraborty, S., Karmakar, K., and Chakravortty, D. (2014) Cells producing their own nemesis: understanding methylglyoxal metabolism, IUBMB Life, 66, 667–678.PubMedCrossRefGoogle Scholar
  169. 170.
    Campbell, A. K., Matthews, S. B., Vassel, N., Cox, C. D., Naseem, R., Chaichi, J., Holland, I. B., Greene, J., and Wann, K. T. (2010) Bacterial metabolic “toxins”: a new mechanism for lactose and food intolerance, and irritable bowel syndrome, Toxicology, 278, 268–276.PubMedCrossRefGoogle Scholar
  170. 171.
    Wendisch, V. F., Lindner, S. N., and Meiswinkel, T. M. (2011) Use of glycerol in biotechnological applications, Biodiesel–Quality, Emissions and By-products (Montero, G., and Stoytcheva, M., eds.) InTech, Rijeka.Google Scholar
  171. 172.
    Clomburg, J. M., and Gonzalez, R. (2011) Metabolic engineering of Escherichia coli for the production of 1,2-propanediol from glycerol, Biotechnol. Bioeng., 108, 867–879.PubMedCrossRefGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2015

Authors and Affiliations

  • O. V. Kosmachevskaya
    • 1
  • K. B. Shumaev
    • 1
  • A. F. Topunov
    • 1
    Email author
  1. 1.Bach Institute of BiochemistryResearch Center of Biotechnology of the Russian Academy of SciencesMoscowRussia

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