Evolutionary Acquisition of Multifunctionality by Glycolytic Enzymes

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Solving the question of the origin of life on Earth is impossible without understanding how the chemical, functional, and regulatory principles that determine cellular metabolism arose, how cells acquired the properties that determine their evolution, and how biological systems function and develop. This review is devoted to the consideration of the versatility of the functions of glycolytic enzymes, the expression of which is significantly increased in some types of cells, for example, cells with stem properties or malignant tumor cells. Almost all glycolysis enzymes have been found to have non-catalytic functions that are necessary to maintain a high rate of cell proliferation, their a-ctive migration, and the formation of a stem-like phenotype. Glycolytic enzymes arose very early during the evolution. Since the genomes of ancient life forms had a limited number of genes to encode the entire set of necessary functions, glycolytic enzymes or the products of the reactions they catalyzed could be used as ancient regulators of intercellular and intracellular communication. 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 noncatalytic functions of glycolytic enzymes, as well as the possible evolutionary significance of acquiring such multifunctionality.

作者简介

O. Shatova

Pirogov Russian National Research Medical University,; RUDN University

编辑信件的主要联系方式.
Email: shatova.op@gmail.com
Russia, Moscow; Russia, Moscow

P. Shegay

Institution National Medical Research Radiology Center of the Ministry of Healthcare
of the Russian Federation

Email: shatova.op@gmail.com
Russia, Moscow

A. Zabolotneva

Pirogov Russian National Research Medical University,

Email: shatova.op@gmail.com
Russia, Moscow

A. Shestopalov

Pirogov Russian National Research Medical University,; Dmitry Rogachev National Medical Research Center of Pediatric Hematology,
Oncology and Immunology, Ministry of Health of the Russian Federation

Email: shatova.op@gmail.com
Russia, Moscow; Russia, Moscow

A. Kaprin

Institution National Medical Research Radiology Center of the Ministry of Healthcare
of the Russian Federation; RUDN University

Email: shatova.op@gmail.com
Russia, Moscow; Russia, Moscow

参考

  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
  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
  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
  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
  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
  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
  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
  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
  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
  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
  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
  12. Shatova O, Khomutov E, Zynkovich I, Skorobogatova Z, Bogaturova O (2009) Does lactate have an impact on enzyme activity? Eur J Cancer Sup 7: 1046. https://doi.org/10.1016/s1359-6349(09)70339-8
  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
  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
  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
  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
  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
  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. Lab Invest 84(4): 513–522. https://doi.org/10.1038/labinvest.3700057
  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
  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
  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
  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
  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
  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
  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
  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
  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
  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
  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
  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
  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
  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
  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
  34. Forbes RA, Verma A (2002) Hypoxia-inducible factor 1 activation by aerobic glycolysis implicates the Warburg effect in carcinogenesis. J Biol Chem 277(26): 23111–23115. https://doi.org/10.1074/jbc.M202487200
  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
  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
  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
  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
  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
  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
  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
  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
  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
  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
  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
  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
  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
  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
  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
  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
  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
  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
  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
  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
  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
  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
  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
  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
  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
  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
  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
  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.
  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
  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. EBioMed 27: 71–85. https://doi.org/10.1016/j.ebiom.2017.10.033
  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
  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
  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
  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
  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
  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.
  72. Gancedo C, Flores C-L (2008) Moonlighting Proteins in Yeasts. Microbiol Mol Biol Rev 72(1): 197–210. https://doi.org/10.1128/mmbr.00036-07
  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

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