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Evolutionary Acquisition of Multifunctionality by Glycolytic Enzymes

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Abstract

Solving the issue of the origin of life on Earth is impossible without understanding how the chemical, functional and regulatory principles underlying cellular metabolism arose, how cells acquired the properties that determine their evolution, and how biological systems function and develop. This review addresses functional versatility of glycolytic enzymes whose expression is considerably increased in some types of cells, for example, stem or malignant tumor cells. Almost all glycolytic enzymes share non-catalytic functions needed to maintain a high rate of cell proliferation, their active migration, and the formation of a stem-like phenotype. Glycolytic enzymes emerged very early in evolution. Since the genomes of ancient life forms contained a limited number of genes to encode all the multitude of required functions, glycolytic enzymes or the products of the reactions they catalyzed could be exploited as ancient regulators of inter- and intracellular communications. Subsequently, the multifunctionality of the main metabolic enzymes began to be used by tumor cells to ensure their survival and growth. In this review, we discuss some of the non-catalytic functions of glycolytic enzymes, as well as the possible evolutionary significance of acquiring such a multifunctionality.

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REFERENCES

  1. Ralser M (2018) An appeal to magic? The discovery of a non-enzymatic metabolism and its role in the origins of life. Biochem J 475(16): 2577–2592. https://doi.org/10.1042/BCJ20160866

    Article  CAS  PubMed  Google Scholar 

  2. Bräsen C, Esser D, Rauch B, Siebers B (2014) Carbohydrate metabolism in archaea: Current insights into unusual enzymes and pathways and their regulation. Microbiol Mol Biol Rev 78(1): 89–175. https://doi.org/10.1128/MMBR.00041-13

    Article  PubMed  PubMed Central  Google Scholar 

  3. Chen H, Lin F, Xing K, He X (2015) The reverse evolution from multicellularity to unicellularity during carcinogenesis. Nat Commun 6: 6367. https://doi.org/10.1038/ncomms7367

    Article  CAS  PubMed  Google Scholar 

  4. Corbet C, Pinto A, Martherus R, Santiago de Jesus JP, Polet F, Feron O (2016) Acidosis Drives the Reprogramming of Fatty Acid Metabolism in Cancer Cells through Changes in Mitochondrial and Histone Acetylation. Cell Metab 24 (2): 311–323. https://doi.org/10.1016/j.cmet.2016.07.003

    Article  CAS  PubMed  Google Scholar 

  5. Toyokuni S, Yanatori I, Kong Y, Zheng H, Motooka Y, Jiang L (2020) Ferroptosis at the crossroads of infection, aging and cancer. Cancer Sci 111(8): 2665–2671. https://doi.org/10.1111/cas.14496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Huang CK, Sun Y, Lv L, Ping Y (2022) ENO1 and Cancer. Mol Ther Oncolytics 24: 288–298. https://doi.org/ 10.1016/j.omto.2021.12.026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Cerella C, Dicato M, Diederich M (2014) Modulatory roles of glycolytic enzymes in cell death. Biochem Pharmacol 92: 22–30. https://doi.org/10.1016/j.bcp.2014.07.005

    Article  CAS  PubMed  Google Scholar 

  8. Munemoto M, Mukaisho K ichi, Miyashita T, Oyama K, Haba Y, Okamoto K, Kinoshita J, Ninomiya I, Fushida S, Taniura N, Sugihara H, Fujimura T (2019) Roles of the hexosamine biosynthetic pathway and pentose phosphate pathway in bile acid-induced cancer development. Cancer Sci 110: 2408–2420. https://doi.org/10.1111/cas.14105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Kim JW, Dang CV (2005) Multifaceted roles of glycolytic enzymes. Trends Biochem Sci 30 (3): 142–150. https://doi.org/10.1016/j.tibs.2005.01.005

    Article  CAS  PubMed  Google Scholar 

  10. Jang SR, Xuan Z, Lagoy RC, Jawerth LM, Gonzalez IJ, Singh M, Prashad S, Kim HS, Patel A, Albrecht DR, Hyman AA, Colón-Ramos DA (2021) Phosphofructokinase relocalizes into subcellular compartments with liquid-like properties in vivo. Biophys J 120 (7): 1170–1186. https://doi.org/10.1016/j.bpj.2020.08.002

    Article  CAS  PubMed  Google Scholar 

  11. Mu X, Shi W, Xu Y, Xu C, Zhao T, Geng B, Yang J, Pan J, Hu S, Zhang C, Zhang J, Wang C, Shen J, Che Y, Liu Z, Lv Y, Wen H, You Q (2018) Tumor-derived lactate induces M2 macrophage polarization via the activation of the ERK/STAT3 signaling pathway in breast cancer. Cell Cycle 17 (4): 428–438. https://doi.org/10.1080/15384101.2018.1444305

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Shatova O, Khomutov E, Zynkovich I, Skorobogatova Z, Bogaturova O (2009) Does lactate have an impact on enzyme activity? Europ J Cancer Sup 7: 1046. https://doi.org/10.1016/s1359-6349(09)70339-8

    Article  Google Scholar 

  13. Yang H, Zhong JT, Zhou SH, Han HM (2019) Review roles of GLUT-1 and HK-II expression in the biological behavior of head and neck cancer. Oncotarget 10 (32): 3066–30833. https://doi.org/10.18632/oncotarget.24684

    Article  PubMed  PubMed Central  Google Scholar 

  14. Sancho P, Barneda D, Heeschen C (2016) Hallmarks of cancer stem cell metabolism. Br J Cancer 114 (12): 1305–1312. https://doi.org/10.1038/bjc.2016.152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Kopeckova M, Pavkova I, Stulik J (2020) Diverse Localization and Protein Binding Abilities of Glyceraldehyde-3-Phosphate Dehydrogenase in Pathogenic Bacteria: The Key to its Multifunctionality? Front Cell Infect Microbiol 10: 89. https://doi.org/10.3389/fcimb.2020.00089

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Franco-Serrano L, Sánchez-Redondo D, Nájar-García A, Hernández S, Amela I, Perez-Pons JA, Piñol J, Mozo-Villarias A, Cedano J, Querol E (2021) Pathogen moonlighting proteins: From ancestral key metabolic enzymes to virulence factors. Microorganisms 9 (6): 1300. https://doi.org/10.3390/microorganisms9061300

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Yanagawa T, Funasaka T, Tsutsumi S, Watanabe H, Raz A (2004) Novel roles of the autocrine motility factor/phosphoglucose isomerase in tumor malignancy. Endocr Relat Cancer 11 (4): 749–759. https://doi.org/10.1677/erc.1.00811

    Article  CAS  PubMed  Google Scholar 

  18. Yanagawa T, Watanabe H, Takeuchi T, Fujimoto S, Kurihara H, Takagishi K (2004) Overexpression of autocrine motility factor in metastatic tumor cells: Possible association with augmented expression of KIF3A and GDI-β. Laboratory Investigation 84 (4): 513–522. https://doi.org/10.1038/labinvest.3700057

    Article  CAS  PubMed  Google Scholar 

  19. Bustamante E, Pedersen PL (1977) High aerobic glycolysis of rat hepatoma cells in culture: Role of mitochondrial hexokinase. Proc Natl Acad Sci USA 74 (9): 3735–3739. https://doi.org/10.1073/pnas.74.9.3735

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Wang W, Liu Z, Zhao L, Sun J, He Q, Yan W, Lu Z, Wang A (2017) Hexokinase 2 enhances the metastatic potential of tongue squamous cell carcinoma via the SOD2-H2O2 pathway. Oncotarget 8 (2): 3344–3354. https://doi.org/10.18632/oncotarget.13763

    Article  PubMed  Google Scholar 

  21. Weh E, Lutrzykowska Z, Smith A, Hager H, Pawar M, Wubben TJ, Besirli CG (2020) Hexokinase 2 is dispensable for photoreceptor development but is required for survival during aging and outer retinal stress. Cell Death Dis 11 (6): 422. https://doi.org/10.1038/s41419-020-2638-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Majewski N, Nogueira V, Bhaskar P, Coy PE, Skeen JE, Gottlob K, Chandel NS, Thompson CB, Robey RB, Hay N (2004) Hexokinase-mitochondria interaction mediated by Akt is required to inhibit apoptosis in the presence or absence of Bax and Bak. Mol Cell 16 (5): 819–830. https://doi.org/10.1016/j.molcel.2004.11.014

    Article  CAS  PubMed  Google Scholar 

  23. Rajala A, Gupta VK, Anderson RE, Rajala RVS (2013) Light activation of the insulin receptor regulates mitochondrial hexokinase. A possible mechanism of retinal neuroprotection. Mitochondrion 13 (6): 566–576. https://doi.org/10.1016/j.mito.2013.08.005

    Article  CAS  PubMed  Google Scholar 

  24. Masumura S, Hashimoto M, Hashimoto Y, SatŌ T, Kihara I, Watanabe Y (1982) Glycolytic activity of rat aorta after exercise. Eur J Appl Physiol Occup Physiol 48 (2): 157–161. https://doi.org/10.1007/BF00422977

    Article  CAS  PubMed  Google Scholar 

  25. Osthus RC, Shim H, Kim S, Li Q, Reddy R, Mukherjee M, Xu Y, Wonsey D, Lee LA, Dang CV (2000) Deregulation of glucose transporter 1 and glycolytic gene expression by c-Myc. J Biol Chem 275 (29):21797–21800. https://doi.org/10.1074/jbc.C000023200

    Article  CAS  PubMed  Google Scholar 

  26. Sato J, Yanagawa T, Dobashi Y, Yamaji T, Takagishi K, Watanabe H (2008) Prognostic significance of 18F-FDG uptake in primary osteosarcoma after but not before chemotherapy: A possible association with autocrine motility factor/phosphoglucose isomerase expression. Clin Exp Metastasis 25 (4): 427–435. https://doi.org/10.1007/s10585-008-9147-5

    Article  PubMed  Google Scholar 

  27. Chiao JW, Xu W, Yang YM, Kancherla R, Seiter K, Ahmed T, Mittelman A (1999) Regulation of growth and apoptosis of breast cancer cells by a 54 kDa lymphokine. Int J Oncol 15 (4): 835–838. https://doi.org/10.3892/ijo.15.4.835

    Article  CAS  PubMed  Google Scholar 

  28. Zong M, Lu T, Fan S, Zhang H, Gong R, Sun L, Fu Z, Fan L (2015) Glucose-6-phosphate isomerase promotes the proliferation and inhibits the apoptosis in fibroblast-like synoviocytes in rheumatoid arthritis. Arthritis Res Ther 17 (1): 100. https://doi.org/10.1186/s13075-015-0619-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Shimizu K, Tani M, Watanabe H, Nagamachi Y, Niinaka Y, Shiroishi T, Ohwada S, Raz A, Yokota J (1999) The autocrine motility factor receptor gene encodes a novel type of seven transmembrane protein. FEBS Lett 456 (2): 295–300. https://doi.org/10.1016/S0014-5793(99)00966-7

    Article  CAS  PubMed  Google Scholar 

  30. Funasaka T, Haga A, Raz A, Nagase H (2001) Tumor autocrine motility factor is an angiogenic factor that stimulates endothelial cell motility. Biochem Biophys Res Commun 285 (1): 118–128. https://doi.org/10.1006/bbrc.2001.5135

    Article  CAS  PubMed  Google Scholar 

  31. Kaynak K, Kara M, Oz B, Akgoz B, Sar M, Raz A (2005) Autocrine motility factor receptor expression implies an unfavourable prognosis in resected stage I pulmonary adenocarcinomas. Acta Chir Belg 105 (4): 378–382. https://doi.org/10.1080/00015458.2005.11679740

    Article  CAS  PubMed  Google Scholar 

  32. Mazzio E, Soliman KFA (2003) The role of glycolysis and gluconeogenesis in the cytoprotection of neuroblastoma cells against 1-methyl 4-phenylpyridinium ion toxicity. Neurotoxicology 24 (1): 137–147. https://doi.org/10.1016/S0161-813X(02)00110-9

    Article  CAS  PubMed  Google Scholar 

  33. Mazzio EA, Soliman KFA (2003) Cytoprotection of pyruvic acid and reduced β-nicotinamide adenine dinucleotide against hydrogen peroxide toxicity in neuroblastoma cells. Neurochem Res 28 (5): 733–741. https://doi.org/10.1023/A:1022813817743

    Article  CAS  PubMed  Google Scholar 

  34. Forbes RA, Verma A (2002) Hypoxia-inducible factor 1 activation by aerobic glycolysis implicates the Warburg effect in carcinogenesis. J Biol Chem277 (26): 23111–23115. https://doi.org/10.1074/jbc.M202487200

    Article  CAS  PubMed  Google Scholar 

  35. Enzo E, Santinon G, Pocaterra A, Aragona M, Bresolin S, Forcato M, Grifoni D, Pession A, Zanconato F, Guzzo G, Bicciato S, Dupont S (2015) Aerobic glycolysis tunes YAP / TAZ transcriptional activity. EMBO J 34 (10): 1349–1370. https://doi.org/10.15252/embj.201490379.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Zecchin A, Stapor PC, Goveia J, Carmeliet P (2015) Metabolic pathway compartmentalization: An underappreciated opportunity? Curr Opin Biotechnol 34: 73–81. https://doi.org/10.1016/j.copbio.2014.11.022

    Article  CAS  PubMed  Google Scholar 

  37. Pirovich DB, Da’dara AA, Skelly PJ (2021) Multifunctional Fructose 1,6-Bisphosphate Aldolase as a Therapeutic Target. Front Mol Biosci 8: 719678. https://doi.org/10.3389/fmolb.2021.719678

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Cieśla M, Mierzejewska J, Adamczyk M, Farrants AKÖ, Boguta M (2014) Fructose bisphosphate aldolase is involved in the control of RNA polymerase III-directed transcription. Biochim Biophys Acta Mol Cell Res 1843 (6): 11103–11110. https://doi.org/10.1016/j.bbamcr.2014.02.007

    Article  CAS  Google Scholar 

  39. Rangarajan ES, Park H, Fortin E, Sygusch J, Izard T (2010) Mechanism of aldolase control of sorting nexin 9 function in endocytosis. J Biol Chem 285 (16):11983–11990. https://doi.org/10.1074/jbc.M109.092049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Li M, Zhang CS, Zong Y, Feng JW, Ma T, Hu M, Lin Z, Li X, Xie C, Wu Y, Jiang D, Li Y, Zhang C, Tian X, Wang W, Yang Y, Chen J, Cui J, Wu YQ, Chen X, Liu QF, Wu J, Lin SY, Ye Z, Liu Y, Piao HL, Yu L, Zhou Z, Xie XS, Hardie DG, Lin SC (2019) Transient Receptor Potential V Channels Are Essential for Glucose Sensing by Aldolase and AMPK. Cell Metab 30 (3): 508–524. e12. https://doi.org/10.1016/j.cmet.2019.05.018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Ma D, Chen X, Zhang PY, Zhang H, Wei LJ, Hu S, Tang JZ, Zhou MT, Xie C, Ou R, Xu Y, Tang KF (2018) Upregulation of the ALDOA/DNA-PK/p53 pathway by dietary restriction suppresses tumor growth. Oncogene 37 (8): 1041–1048. https://doi.org/10.1038/onc.2017.398

    Article  CAS  PubMed  Google Scholar 

  42. Caspi M, Perry G, Skalka N, Meisel S, Firsow A, Amit M, Rosin-Arbesfeld R (2014) Aldolase positively regulates of the canonical Wnt signaling pathway. Mol Cancer 13: 164. https://doi.org/10.1186/1476-4598-13-164

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Li J, Wang F, Gao H, Huang S, Cai F, Sun J (2019) ALDOLASE A regulates invasion of bladder cancer cells via E-cadherin-EGFR signaling. J Cell Biochem 120 (8): 13694–13705. https://doi.org/10.1002/jcb.28642

    Article  CAS  PubMed  Google Scholar 

  44. Giegé P, Heazlewood JL, Roessner-Tunali U, Harvey Millar A, Fernie AR, Leaver CJ, Sweetlove LJ (2003) Enzymes of glycolysis are functionally associated with the mitochondrion in arabidopsis cells. Plant Cell 15 (9): 2140–2151. https://doi.org/10.1105/tpc.012500

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Wang X, Sirover MA, Anderson LE (1999) Pea chloroplast glyceraldehyde-3-phosphate dehydrogenase has uracil glycosylase activity. Arch Biochem Biophys 367 (2): 348–353. https://doi.org/10.1006/abbi.1999.1261

    Article  CAS  PubMed  Google Scholar 

  46. Mazzola JL, Sirover MA (2002) Alteration of nuclear glyceraldehyde-3-phosphate dehydrogenase structure in Huntington’s disease fibroblasts. Mol Brain Res 100: 95–101. https://doi.org/10.1016/S0169-328X(02)00160-2

    Article  CAS  PubMed  Google Scholar 

  47. Sirover MA (2005) New nuclear functions of the glycolytic protein, glyceraldehyde-3-phosphate dehydrogenase, in mammalian cells. J Cell Biochem 95: 45–52. https://doi.org/10.1002/jcb.20399

    Article  CAS  PubMed  Google Scholar 

  48. Sirover MA (1999) New insights into an old protein: The functional diversity of mammalian glyceraldehyde-3-phosphate dehydrogenase. Biochim Biophysi Acta - Protein Struct Mol Enzymol 1432 (2): 159–184. https://doi.org/10.1016/s0167-4838(99)00119-3

    Article  CAS  Google Scholar 

  49. Svedružić ŽM, Spivey HO (2006) Interaction between mammalian glyceraldehyde-3-phosphate dehydrogenase and L-lactate dehydrogenase from heart and muscle. Proteins: Structure, Function and Genetics 63 (3): 501–511. https://doi.org/10.1002/prot.20862

    Article  CAS  Google Scholar 

  50. Ohba S, Johannessen TCA, Chatla K, Yang X, Pieper RO, Mukherjee J (2020) Phosphoglycerate Mutase 1 Activates DNA Damage Repair via Regulation of WIP1 Activity. Cell Rep 31(2): 107518. https://doi.org/10.1016/j.celrep.2020.03.082

    Article  CAS  PubMed  Google Scholar 

  51. Subramanian A, Miller DM (2000) Structural analysis of α-enolase: Mapping the functional domains involved in down-regulation of the c-myc protooncogene. J Biol Chem 275 (8): 5958–5965. https://doi.org/10.1074/jbc.275.8.5958

    Article  CAS  PubMed  Google Scholar 

  52. Perconti G, Maranto C, Romancino DP, Rubino P, Feo S, Bongiovanni A, Giallongo A (2017) Pro-invasive stimuli and the interacting protein Hsp70 favour the route of alpha-enolase to the cell surface. Sci Rep 7 (1): 3841. https://doi.org/10.1038/s41598-017-04185-8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Hoshino A, Hirst JA, Fujii H (2007) Regulation of cell proliferation by interleukin-3-induced nuclear translocation of pyruvate kinase. J Biol Chem 282 (24): 11706–11711. https://doi.org/10.1074/jbc.M700094200

    Article  CAS  Google Scholar 

  54. Newsholme EA, Board M (1991) Application of metabolic-control logic to fuel utilization and its significance in tumor cells. Adv Enzyme Regul 31: 225–246. https://doi.org/10.1016/0065-2571(91)90015-E

    Article  CAS  PubMed  Google Scholar 

  55. Harris RA, Fenton AW (2019) A critical review of the role of M 2 PYK in the Warburg effect. Biochim Biophys Acta Rev Cancer 1871 (2): 225–239. https://doi.org/10.1016/j.bbcan.2019.01.004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Lee J, Kim HK, Han YM, Kim J (2008) Pyruvate kinase isozyme type M2 (PKM2) interacts and cooperates with Oct-4 in regulating transcription. Int J Biochem Cell Biol 40 (5): 1043–1054. https://doi.org/10.1016/j.biocel.2007.11.009

    Article  CAS  PubMed  Google Scholar 

  57. Urbańska K, Orzechowski A (2019) Unappreciated role of LDHA and LDHB to control apoptosis and autophagy in tumor cells. Int J Mol Sci 20 (9): 2085. https://doi.org/10.3390/ijms20092085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Brooks GA (2018) The Science and Translation of Lactate Shuttle Theory. Cell Metab 27 (4): 757–785. https://doi.org/10.1016/j.cmet.2018.03.008

    Article  CAS  PubMed  Google Scholar 

  59. Zhang Y, Zhang X, Wang X, Gan L, Yu G, Chen Y, Liu K, Li P, Pan J, Wang J, Qin S (2012) Inhibition of LDH-A by lentivirus-mediated small interfering RNA suppresses intestinal-type gastric cancer tumorigenicity through the downregulation of Oct4. Cancer Lett 321(1): 45–54. https://doi.org/10.1016/j.canlet.2012.03.013

    Article  CAS  PubMed  Google Scholar 

  60. Rong Y, Wu W, Ni X, Kuang T, Jin D, Wang D, Lou W (2013) Lactate dehydrogenase A is overexpressed in pancreatic cancer and promotes the growth of pancreatic cancer cells. Tumor Biol 34 (3): 1523–1530. https://doi.org/10.1007/s13277-013-0679-1

    Article  CAS  Google Scholar 

  61. Wang ZY, Loo TY, Shen JG, Wang N, Wang DM, Yang DP, Mo SL, Guan XY, Chen JP (2012) LDH-A silencing suppresses breast cancer tumorigenicity through induction of oxidative stress mediated mitochondrial pathway apoptosis. Breast Cancer Res Treat 131 (3): 791–800. https://doi.org/10.1007/s10549-011-1466-6

    Article  CAS  PubMed  Google Scholar 

  62. Lewis BC, Prescott JE, Campbell SE, Shim H, Orlowski RZ, Dang CV (2000) Tumor induction by the c-Myc target genes rcl and lactate dehydrogenase A. Cancer Res 60 (21): 6178–6183.

    CAS  PubMed  Google Scholar 

  63. Jiang F, Ma S, Xue Y, Hou J, Zhang Y (2016) LDH-A promotes malignant progression via activation of epithelial-to-mesenchymal transition and conferring stemness in muscle-invasive bladder cancer. Biochem Biophys Res Commun 469 (4): 985–992. https://doi.org/10.1016/j.bbrc.2015.12.078

    Article  CAS  PubMed  Google Scholar 

  64. Lin H, Muramatsu R, Maedera N, Tsunematsu H, Hamaguchi M, Koyama Y, Kuroda M, Ono K, Sawada M, Yamashita T (2018) Extracellular Lactate Dehydrogenase A Release From Damaged Neurons Drives Central Nervous System Angiogenesis. EBioMedicine 27: 71–85. https://doi.org/10.1016/j.ebiom.2017.10.033

    Article  PubMed  Google Scholar 

  65. Graziano F, Ruzzo A, Giacomini E, Ricciardi T, Aprile G, Loupakis F, Lorenzini P, Ongaro E, Zoratto F, Catalano V, Sarti D, Rulli E, Cremolini C, de Nictolis M, de Maglio G, Falcone A, Fiorentini G, Magnani M (2017) Glycolysis gene expression analysis and selective metabolic advantage in the clinical progression of colorectal cancer. Pharmacogenomics J 17 (3): 258–264. https://doi.org/10.1038/tpj.2016.13

    Article  CAS  PubMed  Google Scholar 

  66. Shegay PV, Zabolotneva AA, Shatova OP, Shestopalov AV, Kaprin AD (2022) Evolutionary View on Lactate-Dependent Mechanisms of Maintaining Cancer Cell Stemness and Reprimitivization. Cancers (Basel) 14: 4552. https://doi.org/10.3390/cancers14194552

  67. Shi Q, Le X, Wang B, Abbruzzese JL, Xiong Q, He Y, Xie K (2001) Regulation of vascular endothelial growth factor expression by acidosis in human cancer cells. Oncogene 20 (28): 3751–3756. https://doi.org/10.1038/sj.onc.1204500

    Article  CAS  PubMed  Google Scholar 

  68. Liu Y, Guo JZ, Liu Y, Wang K, Ding W, Wang H, Liu X, Zhou S, Lu XC, Yang H bin, Xu C, Gao W, Zhou L, Wang YP, Hu W, Wei Y, Huang C, Lei QY (2018) Nuclear lactate dehydrogenase A senses ROS to produce α-hydroxybutyrate for HPV-induced cervical tumor growth. Nat Commun 9 (1): 4429. https://doi.org/10.1038/s41467-018-06841-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Hemmadi V, Biswas M (2021) An overview of moonlighting proteins in Staphylococcus aureus infection. Arch Microbiol 203 (2): 481–498. https://doi.org/10.1007/s00203-020-02071-y

    Article  CAS  PubMed  Google Scholar 

  70. Henderson B (2014) An overview of protein moonlighting in bacterial infection. Biochem Soc Trans 42 (6): 1720–1727. https://doi.org/10.1042/BST20140236

    Article  CAS  PubMed  Google Scholar 

  71. Gómez-Arreaza A, Acosta H, Quiñones W, Concepción JL, Michels PAM, Avilán L (2014) Extracellular functions of glycolytic enzymes of parasites: Unpredicted use of ancient proteins. Mol Biochem Parasitol 193 (2): 75–81.

    Article  PubMed  Google Scholar 

  72. Gancedo C, Flores C-L (2008) Moonlighting Proteins in Yeasts. Microbiol Molecular Biol Rev 72 (1): 197–210. https://doi.org/10.1128/mmbr.00036-07

    Article  CAS  Google Scholar 

  73. Chang YC, Yang YC, Tien CP, Yang CJ, Hsiao M (2018) Roles of Aldolase Family Genes in Human Cancers and Diseases. Trends Endocrinol Metabol 29(8): 549–559. https://doi.org/10.1016/j.tem.2018.05.003

    Article  CAS  Google Scholar 

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This review article was written within the state budget funding.

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Authors and Affiliations

  1. Pirogov Russian National Research Medical University, Moscow, Russia

    O. P. Shatova, A. A. Zabolotneva & A. V. Shestopalov

  2. National Medical Research Center for Radiologoly of the Ministry of Healthcare of the Russian Federation, Moscow, Russia

    P. V. Shegay & A. D. Kaprin

  3. Dmitry Rogachev National Medical Research Center for Pediatric Hematology, Oncology and Immunology of the Ministry of Health of the Russian Federation, Moscow, Russia

    A. V. Shestopalov

  4. RUDN University, Moscow, Russia

    O. P. Shatova & A. D. Kaprin

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  1. O. P. Shatova
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  2. P. V. Shegay
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  3. A. A. Zabolotneva
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  4. A. V. Shestopalov
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Contributions

O.P.Sh.—writing of article sections; P.V.Sh.—conceptualization, writing of article sections; A.A.Z.—writing of article sections, graphical representation; A.V.Sh.—scientific consulting, text correction; A.D.K.—conceptualization, scientific consulting, final text correction.

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Correspondence to O. P. Shatova.

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Translated by A. Polyanovsky

Russian Text © The Author(s), 2023, published in Rossiiskii Fiziologicheskii Zhurnal imeni I.M. Sechenova, 2023, Vol. 109, No. 1, pp. 3–17https://doi.org/10.31857/S0869813923010119.

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Shatova, O.P., Shegay, P.V., Zabolotneva, A.A. et al. Evolutionary Acquisition of Multifunctionality by Glycolytic Enzymes. J Evol Biochem Phys 59, 107–118 (2023). https://doi.org/10.1134/S002209302301009X

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