Maillard reaction and aging: can bacteria shed light on the link?

References

• Medawar PB. An unsolved problem of biology. 1st ed. London: Lewis; 1952.
   Google Scholar
• Williams GC. Pleiotropy, natural selection and the evolution of senescence. Evolution. 1957;11:398–411.
   Web of Science ®Google Scholar
• Kirkwood TB. Evolution of ageing. Nature. 1977;270:301–304.
   PubMed Web of Science ®Google Scholar
• Darwin CR. On the origin of species by means of natural selection, or the preservation of favoured races in the struggle for life. 1st ed. London: John Murray; 1859.
   Google Scholar
• Gallant J, Palmer L. Error propagation in viable cells. Mech Ageing Dev. 1979;10:27–38.
   PubMed Web of Science ®Google Scholar
• Barton A. Some aspects of cell division in Saccharomyces cerevisiae. J Gen Microbiol. 1950;4:84–86.
   PubMedGoogle Scholar
• Mortimer RK, Johnston JR. Life span of individual yeast cells. Nature. 1959;183:1751–1752.
   PubMed Web of Science ®Google Scholar
• Nyström T, Liu B. The mystery of aging and rejuvenation - a budding topic. Curr Opin Microbiol. 2014;18:61–67.
   PubMed Web of Science ®Google Scholar
• Higuchi-Sanabria R, Pernice WM, Vevea JD. Role of asymmetric cell division in lifespan control in Saccharomyces cerevisiae. FEMS Yeast Res. 2014;14:1133–1146.
   PubMed Web of Science ®Google Scholar
• Hill SM, Hao X, Grönvall J, et al. Asymmetric inheritance of aggregated proteins and age reset in yeast are regulated by Vac17-dependent vacuolar functions. Cell Rep. 2016;16:826–838.
   PubMed Web of Science ®Google Scholar
• Szilard L. On the nature of the aging process. Proc Natl Acad Sci USA. 1959;45:30–45.
   PubMed Web of Science ®Google Scholar
• Alexander P. The role of DNA lesions in the processes leading to aging in mice. Symp Soc Exp Biol. 1967;21:29–50.
   PubMedGoogle Scholar
• Harman D. Aging: a theory based on free radical and radiation chemistry. J Gerontol. 1956;11:298–300.
   PubMedGoogle Scholar
• Cerami A. Aging of proteins and nucleic acids: what is the role of glucose?. Trends Biochem Sci. 1986;11:311–314.
   Web of Science ®Google Scholar
• Monnier VM. Toward a Maillard reaction theory of aging. Prog Clin Biol Res. 1989;304:1–22.
   PubMedGoogle Scholar
• Mironova R, Niwa T, Hayashi H, et al. Evidence for non-enzymatic glycosylation in Escherichia coli. Mol Microbiol. 2001;39:1061–1068.
   PubMed Web of Science ®Google Scholar
• Stewart EJ, Madden R, Paul G, et al. Aging and death in an organism that reproduces by morphologically symmetric division. PLoS Biol. 2005;3:e45.
   PubMed Web of Science ®Google Scholar
• Wang P, Robert L, Pelletier J, et al. Robust growth of Escherichia coli. Curr Biol. 2010;20:1099–1103.
   PubMed Web of Science ®Google Scholar
• Maillard LC. Action des acides amines sur les sucres: formation des melanoidines par voie methodique [Action of amino acids on sugars: method for melanoidines formation]. C R Acad Sci. 1912;154:66–68.
   Google Scholar
• Hodge JE. The Amadori rearrangement. Adv Carbohydr Chem. 1955;10:169–205.
   PubMed Web of Science ®Google Scholar
• Nakayama T, Hayase F, Kato H. Formation of Nε-(2-formyl-5-hydroxy-methyl-pyrrol-1-yl)-L-norleucine in the Maillard reaction between D-glucose and L-lysine. Agric Biol Chem. 1980;44:1201–1202.
   Web of Science ®Google Scholar
• Pongor S, Ulrich PC, Bencsath FA, et al. A. Aging of proteins: isolation and identification of a fluorescent chromophore from the reaction of polypeptides with glucose. Proc Natl Acad Sci USA. 1984;81:2684–2688.
   PubMed Web of Science ®Google Scholar
• Ahmed MU, Thorpe SR, Baynes JW. Identification of N epsilon-carboxymethyllysine as a degradation product of fructoselysine in glycated protein. J Biol Chem. 1986;261:4889–4894.
   PubMed Web of Science ®Google Scholar
• Sell DR, Monnier VM. Structure elucidation of a senescence cross-link from human extracellular matrix. Implication of pentoses in the aging process. J Biol Chem. 1989;264:21597–21602.
   PubMed Web of Science ®Google Scholar
• Ahmed N, Thornalley PJ. Quantitative screening of protein biomarkers of early glycation, advanced glycation, oxidation and nitrosation in cellular and extracellular proteins by tandem mass spectrometry multiple reaction monitoring. Biochem Soc Trans. 2003;31:1417–1422.
   PubMed Web of Science ®Google Scholar
• Thornalley PJ, Battah S, Ahmed N, et al. Quantitative screening of advanced glycation endproducts in cellular and extracellular proteins by tandem mass spectrometry. Biochem J. 2003;375:581–592.
   PubMed Web of Science ®Google Scholar
• Thorpe SR, Baynes JW. Maillard reaction products in tissue proteins: new products and new perspectives. Amino Acids. 2003;25:275–281.
   PubMed Web of Science ®Google Scholar
• Lapolla A, Molin L, Traldi P. Protein glycation in diabetes as determined by mass spectrometry. Int J Endocrinol. 2013;2013:412103.
   PubMed Web of Science ®Google Scholar
• Thornalley PJ, Waris S, Fleming T, et al. Imidazopurinones are markers of physiological genomic damage linked to DNA instability and glyoxalase 1-associated tumour multidrug resistance. Nucleic Acids Res. 2010;38:5432–5442.
   PubMed Web of Science ®Google Scholar
• Rabbani N, Thornalley PJ. Dicarbonyl proteome and genome damage in metabolic and vascular disease. Biochem Soc Trans. 2014;42:425–432.
   PubMed Web of Science ®Google Scholar
• Rahbar S. An abnormal hemoglobin in red cells of diabetics. Clin Chim Acta. 1968;22:296–298.
   PubMed Web of Science ®Google Scholar
• Brownlee M. Advanced protein glycosylation in diabetes and aging. Annu Rev Med. 1995;46:223–234.
   PubMed Web of Science ®Google Scholar
• Thorpe SR, Baynes JW. Role of the Maillard reaction in diabetes mellitus and diseases of aging. Drugs Aging. 1996;9:69–77.
   PubMed Web of Science ®Google Scholar
• Ulrich P, Cerami A. Protein glycation, diabetes, and aging. Recent Prog Horm Res. 2001;56:1–21.
   PubMedGoogle Scholar
• Nass N, Bartling B, Navarrete Santos A, et al. Advanced glycation end products, diabetes and ageing. Z Gerontol Geriatr. 2007;40:349–356.
   PubMed Web of Science ®Google Scholar
• Hellwig M, Henle T. Baking, ageing, diabetes: a short history of the Maillard reaction. Angew Chem Int Ed Engl. 2014;53:10316–10329.
   PubMed Web of Science ®Google Scholar
• Sadowska-Bartosz I, Bartosz G. Effect of glycation inhibitors on aging and age-related diseases. Mech Ageing Dev. 2016;160:1–18.
   PubMed Web of Science ®Google Scholar
• Semba RD, Nicklett EJ, Ferrucci L. Does accumulation of advanced glycation end products contribute to the aging phenotype?. J Gerontol A Biol Sci Med Sci. 2010;65:963–975.
   PubMed Web of Science ®Google Scholar
• Bjorksten J. A common molecular basis for the aging syndrome. J Am Geriatr Soc. 1958;8:740–748.
   PubMed Web of Science ®Google Scholar
• Bjorksten J, Tenhu H. The crosslinking theory of aging-added evidence. Exp Gerontol. 1990;25:91–95.
   PubMed Web of Science ®Google Scholar
• Cárdenas-León M, Díaz-Díaz E, Argüelles-Medina R, et al. Glycation and protein crosslinking in the diabetes and ageing pathogenesis. Rev Invest Clin. 2009;61:505–520.
   PubMedGoogle Scholar
• Monnier VM, Mustata GT, Biemel KL, et al. Cross-linking of the extracellular matrix by the Maillard reaction in aging and diabetes: an update on ‘puzzle nearing resolution’. Ann N Y Acad Sci. 2005;1043:533–544.
   PubMed Web of Science ®Google Scholar
• Beisswenger PJ, Howell S, Mackenzie T, et al. Two fluorescent wavelengths, 440(ex)/520(em) nm and 370(ex)/440(em) nm, reflect advanced glycation and oxidation end products in human skin without diabetes. Diabetes Technol Ther. 2012;14:285–292.
   PubMed Web of Science ®Google Scholar
• Couppé C, Hansen P, Kongsgaard M, et al. Mechanical properties and collagen cross-linking of the patellar tendon in old and young men. J Appl Physiol. 2009;107:880–886.
   PubMed Web of Science ®Google Scholar
• Snedeker JG, Gautieri A. The role of collagen crosslinks in ageing and diabetes - the good, the bad, and the ugly. Muscles Ligaments Tendons J. 2014;4:303–308.
   PubMedGoogle Scholar
• Verzijl N, DeGroot J, Thorpe SR, et al. Effect of collagen turnover on the accumulation of advanced glycation end products. J Biol Chem. 2000;275:39027–39031.
   PubMed Web of Science ®Google Scholar
• Verzijl N, DeGroot J, Ben ZC, et al. Crosslinking by advanced glycation end products increases the stiffness of the collagen network in human articular cartilage: a possible mechanism through which age is a risk factor for osteoarthritis. Arthritis Rheum. 2002;46:114–123.
   PubMed Web of Science ®Google Scholar
• Saito M, Marumo K, Fujii K, et al. Single-column high-performance liquid chromatographic-fluorescence detection of immature, mature, and senescent cross-links of collagen. Anal Biochem. 1997;253:26–32.
   PubMed Web of Science ®Google Scholar
• Saito M. Age-related changes in biochemical characteristics of collagen from human weight-bearing and non-weight bearing bone. Tokyo Jikeikai Med J. 1999;114:327–337.
   Google Scholar
• Wang X, Shen X, Li X, et al. Age-related changes in the collagen network and toughness of bone. Bone. 2002;31:1–7. Erratum in: Bone. 2003;32(1):107.
   PubMed Web of Science ®Google Scholar
• Saito M, Fujii K, Mori Y, et al. Role of collagen enzymatic and glycation induced cross-links as a determinant of bone quality in spontaneously diabetic WBN/Kob rats. Osteoporos Int. 2006;17:1514–1523.
   PubMed Web of Science ®Google Scholar
• Sady C, Khosrof S, Nagaraj R. Advanced Maillard reaction and crosslinking of corneal collagen in diabetes. Biochem Biophys Res Commun. 1995;214:793–797.
   PubMed Web of Science ®Google Scholar
• Aronson D. Cross-linking of glycated collagen in the pathogenesis of arterial and myocardial stiffening of aging and diabetes. J Hypertens. 2003;21:3–12.
   PubMed Web of Science ®Google Scholar
• Sims TJ, Rasmussen LM, Oxlund H, et al. The role of glycation cross-links in diabetic vascular stiffening. Diabetologia. 1996;39:946–951.
   PubMed Web of Science ®Google Scholar
• Salahuddin P, Rabbani G, Khan RH. The role of advanced glycation end products in various types of neurodegenerative disease: a therapeutic approach. Cell Mol Biol Lett. 2014;19:407–437.
   PubMed Web of Science ®Google Scholar
• Muronetz VI, Melnikova AK, Seferbekova ZN, et al. Glycolysis, and neurodegenerative diseases: is there any connection?. Biochemistry (Moscow). 2017;82:874–886.
   PubMed Web of Science ®Google Scholar
• Thomas B, Beal MF. Molecular insights into Parkinson's disease. F1000 Med Rep. 2011;3:7.
   PubMedGoogle Scholar
• WIKIMEDIA COMMONS [Internet]: Marvin 101 - Own work, CC BY-SA3.0. Available from: https://commons.wikimedia.org/w/index.php?curid=7533521
   Google Scholar
• WIKIMEDIA COMMONS [Internet]: Nephron - Own work, CC BY-SA 3.0. Available from: https://commons.wikimedia.org/w/index.php?curid=12274694
   Google Scholar
• Plotegher N, Bubacco L. Lysines, Achilles' heel in alpha-synuclein conversion to a deadly neuronal endotoxin. Ageing Res Rev. 2016;26:62–71.
   PubMed Web of Science ®Google Scholar
• Haines DD, Trushin MV, Rose S, et al. Parkinson's disease: Alpha synuclein, heme oxygenase and biotherapeutic countermeasures. Curr Pharm Des. 2018;24:2317–2321.
   PubMed Web of Science ®Google Scholar
• Dalfó E, Portero-Otín M, Ayala V, et al. Evidence of oxidative stress in the neocortex in incidental Lewy body disease. J Neuropathol Exp Neurol. 2005;64:816–830.
   PubMed Web of Science ®Google Scholar
• Kurz A, Rabbani N, Walter M, et al. Alpha-synuclein deficiency leads to increased glyoxalase I expression and glycation stress. Cell Mol Life Sci. 2011;68:721–733.
   PubMed Web of Science ®Google Scholar
• Münch G, Lüth HJ, Wong A, et al. Crosslinking of alpha-synuclein by advanced glycation endproducts - an early pathophysiological step in Lewy body formation?. J Chem Neuroanat. 2000;20:253–257.
   PubMed Web of Science ®Google Scholar
• Choi YG, Lim S. N(ɛ)-(carboxymethyl)lysine linkage to α-synuclein and involvement of advanced glycation end products in α-synuclein deposits in an MPTP-intoxicated mouse model. Biochimie. 2010;92:1379–1386.
   PubMed Web of Science ®Google Scholar
• Lee D, Park CW, Paik SR, et al. The modification of alpha-synuclein by dicarbonyl compounds inhibits its fibril-forming process. Biochim Biophys Acta. 2009;1794:421–430.
   PubMed Web of Science ®Google Scholar
• Kö Nig A, Vicente Miranda H, Outeiro TF. Alpha-synuclein glycation and the action of anti-diabetic agents in Parkinson's disease. J Parkinsons Dis. 2018;8:33–43.
   PubMedGoogle Scholar
• Wong A, Lüth HJ, Deuther-Conrad W, et al. Advanced glycation endproducts co-localize with inducible nitric oxide synthase in Alzheimer's disease. Brain Res. 2001;920:32–40.
   PubMed Web of Science ®Google Scholar
• Reddy VP, Obrenovich ME, Atwood CS, et al. Involvement of Maillard reactions in Alzheimer disease. Neurotox Res. 2002;4:191–209.
   PubMed Web of Science ®Google Scholar
• Chen K, Maley J, Yu PH. Potential inplications of endogenous aldehydes in beta-amyloid misfolding, oligomerization and fibrillogenesis. J Neurochem. 2006;99:1413–1424.
   PubMed Web of Science ®Google Scholar
• Münch G, Westcott B, Menini T, et al. Advanced glycation endproducts and their pathogenic roles in neurological disorders. Amino Acids. 2012;42:1221–1236.
   PubMed Web of Science ®Google Scholar
• Münch G, Mayer S, Michaelis J, et al. Influence of advanced glycation end-products and AGE-inhibitors on nucleation-dependent polymerization of beta-amyloid peptide. Biochim Biophys Acta. 1997;1360:17–29.
   PubMed Web of Science ®Google Scholar
• Freitas AA, de Magalhães JP. A review and appraisal of the DNA damage theory of ageing. Mutat Res. 2011;728:12–22.
   PubMed Web of Science ®Google Scholar
• Liu B, Wang J, Chan KM, et al. Genomic instability in laminopathy-based premature aging. Nat Med. 2005;11:780–785.
   PubMed Web of Science ®Google Scholar
• Mostoslavsky R, Chua KF, Lombard DB, et al. Genomic instability and aging-like phenotype in the absence of mammalian SIRT6. Cell. 2006;124:315–329.
   PubMed Web of Science ®Google Scholar
• Holcomb VB, Vogel H, Hasty P. Deletion of Ku80 causes early aging independent of chronic inflammation and Rag-1-induced DSBs. Mech Ageing Dev. 2007;128:601–608.
   PubMed Web of Science ®Google Scholar
• Hoeijmakers JH. DNA damage, aging, and cancer. N Engl J Med. 2009;361:1475–1485. Erratum in: N Engl J Med. 2009;361(19):1914.
   PubMed Web of Science ®Google Scholar
• Iyama T, Wilson DM. 3rd. Elements that regulate the DNA damage response of proteins defective in Cockayne syndrome. J Mol Biol. 2016;428:62–78.
   PubMed Web of Science ®Google Scholar
• Kanfi Y, Naiman S, Amir G, et al. The sirtuin SIRT6 regulates lifespan in male mice. Nature. 2012;483:218–221.
   PubMed Web of Science ®Google Scholar
• De Luca G, Ventura I, Sanghez V, et al. Prolonged lifespan with enhanced exploratory behavior in mice overexpressing the oxidized nucleoside triphosphatase hMTH1. Aging Cell. 2013;12:695–705.
   PubMed Web of Science ®Google Scholar
• Cho M, Suh Y. Genome maintenance and human longevity. Curr Opin Genet Dev. 2014;26:105–115.
   PubMed Web of Science ®Google Scholar
• Dominick G, Bowman J, Li X, et al. mTOR regulates the expression of DNA damage response enzymes in long-lived Snell dwarf, GHRKO, and PAPPA-KO mice. Aging Cell. 2017;16:52–60.
   PubMed Web of Science ®Google Scholar
• White MC, Holman DM, Boehm JE, et al. Age and cancer risk: a potentially modifiable relationship. Am J Prev Med. 2014;46:S7–S15.
   PubMed Web of Science ®Google Scholar
• Smetana K, Jr, Lacina L, Szabo P, et al. Ageing as an important risk factor for cancer. Anticancer Res. 2016;36:5009–5017.
   PubMed Web of Science ®Google Scholar
• Aunan JR, Cho WC, Søreide K. The biology of aging and cancer: a brief overview of shared and divergent molecular hallmarks. Aging Dis. 2017;8:628–642.
   PubMed Web of Science ®Google Scholar
• Acharya PV. The isolation and partial characterization of age-correlated oligo-deoxyribo-ribonucleotides with covalently linked aspartyl-glutamyl polypeptides. Johns Hopkins Med J Suppl. 1972;(1:):254–260.
   Google Scholar
• Ermolaeva MA, Schumacher B. Systemic DNA damage responses: organismal adaptations to genome instability. Trends Genet. 2014;30:95–102.
   PubMed Web of Science ®Google Scholar
• Ribezzo F, Shiloh Y, Schumacher B. Systemic DNA damage responses in aging and diseases. Semin Cancer Biol. 2016;37-38:26–35.
   PubMed Web of Science ®Google Scholar
• Ames BN, Gold LS. Endogenous mutagens and the causes of aging and cancer. Mutat Res. 1991;250:3–16.
   PubMed Web of Science ®Google Scholar
• Ames BN, Shigenaga MK, Hagen TM. Oxidants, antioxidants, and the degenerative diseases of aging. Proc Natl Acad Sci USA. 1993;90:7915–7922.
   PubMed Web of Science ®Google Scholar
• Bucala R, Model P, Cerami A. Modification of DNA by reducing sugars: a possible mechanism for nucleic acid aging and age-related dysfunction in gene expression. Proc Natl Acad Sci USA. 1984;81:105–109.
   PubMed Web of Science ®Google Scholar
• Baynes JW. The Maillard hypothesis on aging: time to focus on DNA. Ann N Y Acad Sci. 2002;959:360–367.
   PubMed Web of Science ®Google Scholar
• Mironova R, Niwa T, Handzhiyski Y, et al. Evidence for non-enzymatic glycosylation of Escherichia coli chromosomal DNA. Mol Microbiol. 2005;55:1801–1811.
   PubMed Web of Science ®Google Scholar
• Rabbani N, Shaheen F, Anwar A, et al. Assay of methylglyoxal-derived protein and nucleotide AGEs. Biochem Soc Trans. 2014;42:511–517.
   PubMed Web of Science ®Google Scholar
• Waris S, Winklhofer-Roob BM, Roob JM, et al. Increased DNA dicarbonyl glycation and oxidation markers in patients with type 2 diabetes and link to diabetic nephropathy. J Diabetes Res. 2015;2015:1.
   Web of Science ®Google Scholar
• Stone MP, Cho YJ, Huang H, et al. Interstrand DNA cross-links induced by alpha,beta-unsaturated aldehydes derived from lipid peroxidation and environmental sources. Acc Chem Res. 2008;41:793–804.
   PubMed Web of Science ®Google Scholar
• Niedernhofer LJ, Daniels JS, Rouzer CA, et al. Malondialdehyde, a product of lipid peroxidation, is mutagenic in human cells. J Biol Chem. 2003;278:31426–31433.
   PubMed Web of Science ®Google Scholar
• Dooley PA, Zhang M, Korbel GA, et al. NMR determination of the conformation of a trimethylene interstrand cross-link in an oligodeoxynucleotide duplex containing a 5'-d(GpC) motif. J Am Chem Soc. 2003;125:62–72.
   PubMed Web of Science ®Google Scholar
• Edfeldt NB, Harwood EA, Sigurdsson ST, et al. Solution structure of a nitrous acid induced DNA interstrand cross-link. Nucleic Acids Res. 2004;32:2785–2794.
   PubMed Web of Science ®Google Scholar
• Burleigh IG, Dawes EA. Studies on the endogenous metabolism and senescence of starved Sarcina lutea. Biochem J. 1967;102:236–250.
   PubMed Web of Science ®Google Scholar
• Nyström T. Starvation, cessation of growth and bacterial aging. Curr Opin Microbiol. 1999;2:214–219.
   PubMed Web of Science ®Google Scholar
• Nyström T. Not quite dead enough: on bacterial life, culturability, senescence, and death. Arch Microbiol. 2001;176:159–164.
   PubMed Web of Science ®Google Scholar
• Miller MB, Bassler BL. Quorum sensing in bacteria. Annu Rev Microbiol. 2001;55:165–199.
   PubMed Web of Science ®Google Scholar
• Finkel SE. Long-term survival during stationary phase: evolution and the GASP phenotype. Nat Rev Microbiol. 2006;4:113–120.
   PubMed Web of Science ®Google Scholar
• Ericsson M, Hanstorp D, Hagberg P, et al. Sorting out bacterial viability with optical tweezers. J Bacteriol. 2000;182:5551–5555.
   PubMed Web of Science ®Google Scholar
• Zambrano MM, Kolter R. GASPing for life in stationary phase. Cell. 1996;86:181–184.
   PubMed Web of Science ®Google Scholar
• Vulic M, Kolter R. Evolutionary cheating in Escherichia coli stationary phase cultures. Genetics. 2001;158:519–526.
   PubMed Web of Science ®Google Scholar
• Gagliardi A, Lamboglia E, Bianchi L, et al. Proteomics analysis of a long-term survival strain of Escherichia coli K-12 exhibiting a growth advantage in stationary-phase (GASP) phenotype. Proteomics. 2016;16:963–972.
   PubMed Web of Science ®Google Scholar
• Arunasri K, Adil M, Khan PA, et al. Global gene expression analysis of long-term stationary phase effects in E. coli K12 MG1655. PLoS One. 2014;9:e96701.
   PubMed Web of Science ®Google Scholar
• Zinser ER, Kolter R. Escherichia coli evolution during stationary phase. Res Microbiol. 2004;155:328–336.
   PubMed Web of Science ®Google Scholar
• Zinser ER, Kolter R. Mutations enhancing amino acid catabolism confer a growth advantage in stationary phase. J Bacteriol. 1999;181:5800–5807.
   PubMed Web of Science ®Google Scholar
• Zinser ER, Kolter R. Prolonged stationary-phase incubation selects for lrp mutations in Escherichia coli K-12. J Bacteriol. 2000;182:4361–4365.
   PubMed Web of Science ®Google Scholar
• Zinser ER, Schneider D, Blot M, et al. Bacterial evolution through the selective loss of beneficial Genes. Trade-offs in expression involving two loci. Genetics. 2003;164:1271–1277.
   PubMed Web of Science ®Google Scholar
• Nyström T. Conditional senescence in bacteria: death of the immortals. Mol Microbiol. 2003;48:17–23.
   PubMed Web of Science ®Google Scholar
• Dimitrova R, Mironova R, Ivanov I. Glycation of proteins in Escherichia coli: Interference of strain diversity and growth conditions with glycation. C R Bulg Acad Sci. 2004;57:71–75.
   Google Scholar
• Dimitrova R, Mironova R, Ivanov I. Glycation of proteins in Escherichia coli: Effect of nutrient broth ingredients on glycation. Biotechnol Biotechnol Equip. 2004;18:99–103.
   Google Scholar
• Mironova R, Handzhiyski Y, T N, et al. Maillard reaction and spontaneous mutagenesis in Escherichia coli. In: Knutsen DW, Bruns SS, editors. Bacterial DNA, DNA polymerase and DNA helicases. New York (NY): Nova Science Publishers; 2008. p. 51–89.
   Google Scholar
• Pepper ED, Farrell MJ, Nord G, et al. Antiglycation effects of carnosine and other compounds on the long-term survival of Escherichia coli. Appl Environ Microbiol. 2010;76:7925–7930.
   PubMed Web of Science ®Google Scholar
• Kram KE, Finkel SE. Rich medium composition affects Escherichia coli survival, glycation, and mutation frequency during long-term batch culture. Appl Environ Microbiol. 2015;81:4442–4450.
   PubMed Web of Science ®Google Scholar
• Kram KE, Finkel SE. Culture volume and vessel affect long-term survival, mutation frequency, and oxidative stress of Escherichia coli. Appl Environ Microbiol. 2014;80:1732–1738.
   PubMed Web of Science ®Google Scholar
• Handzhiyski Y, Mironova R, Ivanov I. Effect of acetyl salicyilic acid on glycation and mutability of Escherichia coli chromosomal DNA. Biotechnol Biotechnol Equip. 2009;23:1079–1083.
   Web of Science ®Google Scholar
• Colman RJ, Beasley TM, Kemnitz JW, et al. Caloric restriction reduces age-related and all-cause mortality in rhesus monkeys. Nat Commun. 2014;5:3557.
   PubMed Web of Science ®Google Scholar
• Nyström T. Aging in bacteria. Curr Opin Microbiol. 2002;5:596–601.
   PubMed Web of Science ®Google Scholar
• Lindner AB, Madden R, Demarez A, et al. Asymmetric segregation of protein aggregates is associated with cellular aging and rejuvenation. Proc Natl Acad Sci USA. 2008;105:3076–3081.
   PubMed Web of Science ®Google Scholar
• Winkler J, Seybert A, König L, et al. Quantitative and spatio-temporal features of protein aggregation in Escherichia coli and consequences on protein quality control and cellular ageing. EMBO J. 2010;29:910–923.
   PubMed Web of Science ®Google Scholar
• den Blaauwen T, de Pedro MA, Nguyen-Distèche M, et al. Morphogenesis of rod-shaped sacculi. FEMS Microbiol Rev. 2008;32:321–344.
   PubMed Web of Science ®Google Scholar
• Mogk A, Deuerling E, Vorderwülbecke S, et al. Small heat shock proteins, ClpB and the DnaK system form a functional triade in reversing protein aggregation. Mol Microbiol. 2003;50:585–595.
   PubMed Web of Science ®Google Scholar
• Tsekovska RG, Boyanova МS, Mironova RS, et al. Effect of arginine on glycation and stability of recombinant human interferon-gamma. Biotechnol Biotechnol Equip. 2009;23:1063–1067.
   Web of Science ®Google Scholar
• Tsekovska RG, Boyanova MS, Mironova RS, et al. Impact of glycation inhibitors on the biologic activity of recombinant human interferon-gamma. Biotechnol Biotechnol Equip. 2012;26:170–174. Sе:
   Web of Science ®Google Scholar
• Mironova R, Niwa T, Dimitrova R, et al. Glycation and post-translational processing of human interferon-gamma expressed in Escherichia coli. J Biol Chem. 2003;278:51068–51074.
   PubMed Web of Science ®Google Scholar
• Boyanova M, Mironova R, Niwa T, et al. Post-translational processing of human interferon-gamma and approaches for its prevention. In: Georgiev VS, Western KA, McGovan, JJ, editors. Infectious disease. Totowa (NJ): Humana Press; 2008. p. 365–373.
   Google Scholar
• Tsanev R, Ivanov I. Immune interferon. 1st ed. New York (NY): CRC Press; 2002.
   Google Scholar
• Ahmed IH, Krachmarova E, Nacheva G, et al. Nucleic acids in inclusion bodies obtained from E. coli cells expressing human interferon-gamma. Poster session presented at: The 8th Poster Session of the University of Chemical Technology and Metallurgy; May 18; Sofia, Bulgaria, 2011.
   Google Scholar
• Krachmarova E, Nacheva G, Ivanov I. Inclusion bodies obtained from E. coli cells expressing human interferon-gamma contain nucleic acids. In: Abstract book of the Anniversary Molecular Biology Conference ‘50 Year Roumen Tsanev Institute of Molecular Biology’, Sofia, Bulgaria; 2011 Oct 6–7, p. 90.
   Google Scholar
• Popov M, Petrov S, Nacheva G, et al. Effects of a recombinant gene expression on ColE1-like plasmid segregation in Escherichia coli. BMC Biotechnol. 2011;11:18.
   PubMed Web of Science ®Google Scholar
• Pepper ED. Mechanisms of long-term survival in Escherichia coli (dissertation). Los Angeles (CA): University of Southern California; 2007.
   Google Scholar
• Kosmachevskaya OV, Shumaev KB, Topunov AF. Carbonyl stress in bacteria: Causes and consequences. Biochemistry Mosc. 2015;80:1655–1671.
   PubMed Web of Science ®Google Scholar
• Ahmed MU, Brinkmann Frye E, Degenhardt TP, et al. N-epsilon-(carboxyethyl)lysine, a product of the chemical modification of proteins by methylglyoxal, increases with age in human lens proteins. Biochem J. 1997;324: 565–570.
   PubMed Web of Science ®Google Scholar
• Hopper DJ, Cooper RA. The purification and properties of Escherichia coli methylglyoxal synthase. Biochem J. 1972;128:321–329.
   PubMed Web of Science ®Google Scholar
• Tötemeyer S, Booth NA, Nichols WW, et al. From famine to feast: the role of methylglyoxal production in Escherichia coli. Mol Microbiol. 1998;27:553–562.
   PubMed Web of Science ®Google Scholar
• Freedberg WB, Kistler WS, Lin EC. Lethal synthesis of methylglyoxal by Escherichia coli during unregulated glycerol metabolism. J Bacteriol. 1971;108:137–144.
   PubMed Web of Science ®Google Scholar
• Rekarte UD, Zwaig N, Istúriz T. Accumulation of methylglyoxal in a mutant of Escherichia coli constitutive for gluconate catabolism. J Bacteriol. 1973;115:727–731.
   PubMed Web of Science ®Google Scholar
• Ackerman RS, Cozzarelli NR, Epstein W. Accumulation of toxic concentrations of methylglyoxal by wild-type Escherichia coli K-12. J Bacteriol. 1974;119:357–362.
   PubMed Web of Science ®Google Scholar
• Kadner RJ, Murphy GP, Stephens CM. Two mechanisms for growth inhibition by elevated transport of sugar phosphates in Escherichia coli. J Gen Microbiol. 1992;138:2007–2014.
   PubMedGoogle Scholar
• MacLean MJ, Ness LS, Ferguson GP, et al. 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. 1998;27:563–571.
   PubMed Web of Science ®Google Scholar
• Ferguson GP. Protective mechanisms against toxic electrophiles in Escherichia coli. Trends Microbiol. 1999;7:242–247.
   PubMed Web of Science ®Google Scholar
• Misra K, Banerjee AB, Ray S, et al. Glyoxalase III from Escherichia coli: a single novel enzyme for the conversion of methylglyoxal into D-lactate without reduced glutathione. Biochem J. 1995;305: 999–1003.
   PubMed Web of Science ®Google Scholar
• Subedi KP, Choi D, Kim I, et al. Hsp31 of Escherichia coli K-12 is glyoxalase III. Mol Microbiol. 2011;81:926–936.
   PubMed Web of Science ®Google Scholar
• Misra K, Banerjee AB, Ray S, et al. Reduction of methylglyoxal in Escherichia coli K12 by an aldehyde reductase and alcohol dehydrogenase. Mol Cell Biochem. 1996;156:117–124.
   PubMed Web of Science ®Google Scholar
• Saikusa T, Rhee H, Watanabe K, et al. Metabolism of 2-oxoaldehydes in bacteria: purification and characterization of methylglyoxal reductase from Escherichia coli. Agric Biol Chem. 1987;51:1893–1899.
   Web of Science ®Google Scholar
• Ko J, Kim I, Yoo S, et al. Conversion of methylglyoxal to acetol by Escherichia coli aldo-keto reductases. J Bacteriol. 2005;187:5782–5789.
   PubMed Web of Science ®Google Scholar
• Abdallah J, Mihoub M, Gautier V, et al. The DJ-1 superfamily members YhbO and YajL from Escherichia coli repair proteins from glycation by methylglyoxal and glyoxal. Biochem Biophys Res Commun. 2016;470:282–286.
   PubMed Web of Science ®Google Scholar
• Lee C, Lee J, Lee JY, et al. Characterization of the Escherichia coli YajL, YhbO and ElbB glyoxalases. FEMS Microbiol Lett. 2016;363:fnv239.
   PubMed Web of Science ®Google Scholar
• Delpierre G, Collard F, Fortpied J, et al. Fructosamine 3-kinase is involved in an intracellular deglycation pathway in human erythrocytes. Biochem J. 2002;365:801–808.
   PubMed Web of Science ®Google Scholar
• Delpierre G, Rider MH, Collard F, et al. Identification, cloning, and heterologous expression of a mammalian fructosamine-3-kinase. Diabetes. 2000;49:1627–1634.
   PubMed Web of Science ®Google Scholar
• Gemayel R, Fortpied J, Rzem R, et al. Many fructosamine 3-kinase homologues in bacteria are ribulosamine/erythrulosamine 3-kinases potentially involved in protein deglycation. FEBS J. 2007;274:4360–4374.
   PubMed Web of Science ®Google Scholar
• Wiame E, Delpierre G, Collard F, et al. Identification of a pathway for the utilization of the Amadori product fructoselysine in Escherichia coli. J Biol Chem. 2002;277:42523–42529.
   PubMed Web of Science ®Google Scholar
• Katz C, Cohen-Or I, Gophna U, et al. The ubiquitous conserved glycopeptidase Gcp prevents accumulation of toxic glycated proteins. MBio. 2010; 1:e00195-10.
   Google Scholar
• Cohen-Or I, Katz C, Ron EZ. AGEs secreted by bacteria are involved in the inflammatory response. PLoS One. 2011;6:e17974.
   PubMed Web of Science ®Google Scholar
• Cohen-Or I, Katz C, Ron EZ. Metabolism of AGEs-bacterial AGEs are degraded by metallo-proteases. PLoS One. 2013;8:e74970.
   PubMed Web of Science ®Google Scholar
• Yuan B, Cao H, Jiang Y, et al. Efficient and accurate bypass of N2-(1-carboxyethyl)-2'-deoxyguanosine by DinB DNA polymerase in vitro and in vivo. Proc Natl Acad Sci USA. 2008;105:8679–8684.
   PubMed Web of Science ®Google Scholar
• Frischmann M, Bidmon C, Angerer J, et al. Identification of DNA adducts of methylglyoxal. Chem Res Toxicol. 2005;18:1586–1592.
   PubMed Web of Science ®Google Scholar
• Schneider M, Thoss G, Hübner-Parajsz C, et al. Determination of glycated nucleobases in human urine by a new monoclonal antibody specific for N2-carboxyethyl-2'-deoxyguanosine. Chem Res Toxicol. 2004;17:1385–1390.
   PubMed Web of Science ®Google Scholar
• Li H, Nakamura S, Miyazaki S, et al. N2-carboxyethyl-2'-deoxyguanosine, a DNA glycation marker, in kidneys and aortas of diabetic and uremic patients. Kidney Int. 2006;69:388–392.
   PubMed Web of Science ®Google Scholar
• Fuchs RP, Fujii S, Wagner J. Properties and functions of Escherichia coli: Pol IV and Pol V. Adv Protein Chem. 2004;69:229–264.
   PubMedGoogle Scholar
• McKenzie GJ, Harris RS, Lee PL, et al. The SOS response regulates adaptive mutation. Proc Natl Acad Sci USA. 2000;97:6646–6651.
   PubMed Web of Science ®Google Scholar
• Tamae D, Lim P, Wuenschell GE, et al. Mutagenesis and repair induced by the DNA advanced glycation end product N2-1-(carboxyethyl)-2'-deoxyguanosine in human cells. Biochemistry. 2011;50:2321–2329.
   PubMed Web of Science ®Google Scholar
• Jarosz DF, Beuning PJ, Cohen SE, et al. Y-family DNA polymerases in Escherichia coli. Trends Microbiol. 2007;15:70–77.
   PubMed Web of Science ®Google Scholar
• Boteva E, Handzhiyski Y, Kotseva M, et al. Phosphoglucose isomerase deficiency in Escherichia coli K-12 is associated with increased spontaneous mutation rate. AiM. 2018;08:390–405.
   Google Scholar
• Gao H, Chen Y, Leary JA. Kinetic measurements of phosphoglucose isomerase and phosphomannose isomerase by direct analysis of phosphorylated aldose–ketose isomers using tandem mass spectrometry. Int J Mass Spectrom. 2005;240:291–299.
   Web of Science ®Google Scholar
• Ishii N, Suga Y, Hagiya A, et al. Dynamic simulation of an in vitro multi-enzyme system. FEBS Lett. 2007;581:413–420.
   PubMed Web of Science ®Google Scholar
• Kao HW, Lee SC. Phosphoglucose isomerases of hagfish, zebrafish, gray mullet, toad, and snake, with reference to the evolution of the genes in vertebrates. Mol Biol Evol. 2002;19:367–374.
   PubMed Web of Science ®Google Scholar
• Hansen T, Schönheit P. Escherichia coli phosphoglucose isomerase can be substituted by members of the PGI family, the PGI/PMI family, and the cPGI family. FEMS Microbiol Lett. 2005;250:49–53.
   PubMed Web of Science ®Google Scholar
• Richarme G, Mihoub M, Dairou J, et al. Parkinsonism-associated protein DJ-1/Park7 is a major protein deglycase that repairs methylglyoxal- and glyoxal-glycated cysteine, arginine, and lysine residues. J Biol Chem. 2015;290:1885–1897.
   PubMed Web of Science ®Google Scholar
• Richarme G, Liu C, Mihoub M, et al. Guanine glycation repair by DJ-1/Park7 and its bacterial homologs. Science. 2017;357:208–211.
   PubMed Web of Science ®Google Scholar
• Lo TW, Westwood ME, McLellan AC, et al. Binding and modification of proteins by methylglyoxal under physiological conditions. A kinetic and mechanistic study with N alpha-acetylarginine, N alpha-acetylcysteine, and N alpha-acetyllysine, and bovine serum albumin. J Biol Chem. 1994;269:32299–32305.
   PubMed Web of Science ®Google Scholar
• Rabbani N, Thornalley PJ. Dicarbonyl stress in cell and tissue dysfunction contributing to ageing and disease. Biochem Biophys Res Commun. 2015;458:221–226.
   PubMed Web of Science ®Google Scholar