Acetylation control of metabolic enzymes in cancer: An updated version

Acta Biochimica et Biophysica Sinica

Volumn 46, Issue 3, 2014, Pages 204-213

  Huang, Wei ^a,b   Wang, Zhen ^a,c   Lei, Qun Ying ^a  

^a FUDAN UNIVERSITY   (China)

^b UNIVERSITY OF NOTRE DAME   (United States)

^c FUDAN UNIVERSITY   (China)

Author keywords

acetylation; cancer metabolism

Indexed keywords

ENZYME; GLUCOSE; LACTATE DEHYDROGENASE; PYRUVATE KINASE;

ACETYLATION; BIOLOGICAL MODEL; CANCER METABOLISM; GLYCOLYSIS; HUMAN; METABOLISM; NEOPLASM; REVIEW;

ACETYLATION; CANCER METABOLISM;

ACETYLATION; ENZYMES; GLUCOSE; GLYCOLYSIS; HUMANS; L-LACTATE DEHYDROGENASE; MODELS, BIOLOGICAL; NEOPLASMS; PYRUVATE KINASE;

EID: 84897693802     PISSN: 16729145     EISSN: 17457270     Source Type: Journal    
DOI: 10.1093/abbs/gmt154     Document Type: Review

References (74)

1. Warburg O. On respiratory impairment in cancer cells. Science 1956, 124: 269-270.
2. Warburg O. On the origin of cancer cells. Science 1956, 123: 309-314.
3. Lin R, Zhou X, Huang W, Zhao D, Lv L, Xiong Y and Guan KL, et al. Acetylation control of cancer cell metabolism. Curr Pharm Des 2013, PMID: 23859620.
4. Vander Heiden MG, Cantley LC and Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 2009, 324: 1029-1033.
5. Wang Q, Zhang Y, Yang C, Xiong H, Lin Y, Yao J and Li H, et al. Acetylation of metabolic enzymes coordinates carbon source utilization and metabolic flux. Science 2010, 327: 1004-1007.
6. Xiong Y and Guan KL. Mechanistic insights into the regulation of metabolic enzymes by acetylation. J Cell Biol 2012, 198: 155-164.
7. Zhao S, Xu W, Jiang W, Yu W, Lin Y, Zhang T and Yao J, et al. Regulation of cellular metabolism by protein lysine acetylation. Science 2010, 327: 1000-1004.
8. Guan KL and Xiong Y. Regulation of intermediary metabolism by protein acetylation. Trends Biochem Sci 2011, 36: 108-116.
9. Xu W, Li Y, Liu C and Zhao S. Protein lysine acetylation guards metabolic homeostasis to fight against cancer. Oncogene 2013, 163: 1-7.
10. Gao X, Wang H, Yang JJ, Liu X and Liu ZR. Pyruvate kinase M2 regulates gene transcription by acting as a protein kinase. Mol Cell 2012, 45: 598-609.
11. Yang W, Xia Y, Hawke D, Li X, Liang J, Xing D and Aldape K, et al. PKM2 phosphorylates histone H3 and promotes gene transcription and tumorigenesis. Cell 2012, 150: 685-696.
12. Yang W, Xia Y, Ji H, Zheng Y, Liang J, Huang W and Gao X, et al. Nuclear PKM2 regulates beta-catenin transactivation upon EGFR activation. Nature 2011, 480: 118-122.
13. Gatenby RA and Gillies RJ. Why do cancers have high aerobic glycolysis? Nat Rev Cancer 2004, 4: 891-899.
14. Kim JW and Dang CV. Cancer's molecular sweet tooth and the Warburg effect. Cancer Res 2006, 66: 8927-8930.
15. Hanahan D and Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011, 144: 646-674.
16. McKeehan WL. Glycolysis, glutaminolysis and cell proliferation. Cell Biol Int Rep 1982, 6: 635-650.
17. Kanno H, Fujii H, Hirono A and Miwa S. cDNA cloning of human R-Type pyruvate kinase and identification of a single amino acid substitution (Thr384- -Met) affecting enzymatic stability in a pyruvate kinase variant (PK Tokyo) associated with hereditary hemolytic anemia. Proc Natl Acad Sci USA 1991, 88: 8218-8221.
18. Tani K, Fujii H, Tsutsumi H, Sukegawa J, Toyoshima K, Yoshida MC and Noguchi T, et al. Human liver type pyruvate kinase: cDNA cloning and chromosomal assignment. Biochem Biophys Res Commun 1987, 143: 431-438.
19. Brinck U, Eigenbrodt E, Oehmke M, Mazurek S and Fischer G. L- and M2-pyruvate kinase expression in renal cell carcinomas and their metastases. Virchows Arch 1994, 424: 177-185.
20. Corcoran E, Phelan JJ and Fottrell PF. Purification and properties of pyruvate kinase from human lung. Biochim Biophys Acta 1976, 446: 96-104.
21. Eigenbrodt E, Reinacher M, Scheefers-Borchel U, Scheefers H and Friis R. Double role for pyruvate kinase type M2 in the expansion of phosphometabolite pools found in tumor cells. Crit Rev Oncog 1992, 3: 91-115.
22. Mazurek S, Boschek CB, Hugo F and Eigenbrodt E. Pyruvate kinase type M2 and its role in tumor growth and spreading. Semin Cancer Biol 2005, 15: 300-308.
23. Reinacher M and Eigenbrodt E. Immunohistological demonstration of the same type of pyruvate kinase isoenzyme (M2-Pk) in tumors of chicken and rat. Virchows Arch B Cell Pathol Incl Mol Pathol 1981, 37: 79-88.
24. Tolle SW, Dyson RD, Newburgh RW and Cardenas JM. Pyruvate kinase isozymes in neurons, glia, neuroblastoma, and glioblastoma. J Neurochem 1976, 27: 1355-1360.
25. Christofk HR, Vander Heiden MG, Harris MH, Ramanathan A, Gerszten RE, Wei R and Fleming MD, et al. The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature 2008, 452: 230-233.
26. David CJ, Chen M, Assanah M, Canoll P and Manley JL. HnRNP proteins controlled by c-Myc deregulate pyruvate kinase mRNA splicing in cancer. Nature 2009, 463: 364-368.
27. Bluemlein K, Gruning NM, Feichtinger RG, Lehrach H, Kofler B and Ralser M. No evidence for a shift in pyruvate kinase PKM1 to PKM2 expression during tumorigenesis. Oncotarget 2011, 2: 393-400.
28. Yang W, Xia Y, Cao Y, Zheng Y, Bu W, Zhang L and You MJ, et al. EGFR-induced and PKC1 monoubiquitylation-dependent NF-kB activation upregulates PKM2 expression and promotes tumorigenesis. Mol Cell 2012, 48: 771-784.
29. Christofk HR, Vander Heiden MG, Wu N, Asara JM and Cantley LC. Pyruvate kinase M2 is a phosphotyrosine-binding protein. Nature 2008, 452: 181-186.
30. Lv L, Li D, Zhao D, Lin R, Chu Y, Zhang H and Zha Z, et al. Acetylation targets the M2 isoform of pyruvate kinase for degradation through chaperone-mediated autophagy and promotes tumor growth. Mol Cell 2011, 42: 719-730.
31. Goldman RD, Kaplan NO and Hall TC. Lactic dehydrogenase in human neoplastic tissues. Cancer Res 1964, 24: 389-399.
32. Koukourakis MI, Giatromanolaki A, Sivridis E, Bougioukas G, Didilis V, Gatter KC and Harris AL. Lactate dehydrogenase-5 (LDH-5) overexpression in non-small-cell lung cancer tissues is linked to tumour hypoxia, angiogenic factor production and poor prognosis. Br J Cancer 2003, 89: 877-885.
33. Koukourakis MI, Giatromanolaki A, Sivridis E, Gatter KC and Harris AL. Lactate dehydrogenase 5 expression in operable colorectal cancer: strong association with survival and activated vascular endothelial growth factor pathway-A report of the Tumour Angiogenesis Research Group. J Clin Oncol 2006, 24: 4301-4308.
34. Koukourakis MI, Kontomanolis E, Giatromanolaki A, Sivridis E and Liberis V. Serum and tissue LDH levels in patients with breast/gynaecological cancer and benign diseases. Gynecol Obstet Invest 2009, 67: 162-168.
35. Kim JW, Zeller KI, Wang Y, Jegga AG, Aronow BJ, O'Donnell KA and Dang CV. Evaluation of myc E-box phylogenetic footprints in glycolytic genes by chromatin immunoprecipitation assays. Mol Cell Biol 2004, 24: 5923-5936.
36. Semenza GL, Roth PH, Fang HM and Wang GL. Transcriptional regulation of genes encoding glycolytic enzymes by hypoxia-inducible factor 1. J Biol Chem 1994, 269: 23757-23763.
37. Le A, Cooper CR, Gouw AM, Dinavahi R, Maitra A, Deck LM and Royer RE, et al. Inhibition of lactate dehydrogenase A induces oxidative stress and inhibits tumor progression. Proc Natl Acad Sci USA 2010, 107: 2037-2042.
38. Zhao D, Zou SW, Liu Y, Zhou X, Mo Y, Wang P and Xu YH, et al. Lysine-5 acetylation negatively regulates lactate dehydrogenase A and is decreased in pancreatic cancer. Cancer Cell 2013, 23: 464-476.
39. Kim HS, Patel K, Muldoon-Jacobs K, Bisht KS, Aykin-Burns N, Pennington JD and van der Meer R, et al. SIRT3 is a mitochondrialocalized tumor suppressor required for maintenance of mitochondrial integrity and metabolism during stress. Cancer Cell 2010, 17: 41-52.
40. Bauer DE, Hatzivassiliou G, Zhao F, Andreadis C and Thompson CB. ATP citrate lyase is an important component of cell growth and transformation. Oncogene 2005, 24: 6314-6322.
41. Berwick DC, Hers I, Heesom KJ, Moule SK and Tavare JM. The identification of ATP-citrate lyase as a protein kinase B (Akt) substrate in primary adipocytes. J Biol Chem 2002, 277: 33895-33900.
42. Migita T, Narita T, Nomura K, Miyagi E, Inazuka F, Matsuura M and Ushijima M, et al. ATP citrate lyase: Activation and therapeutic implications in non-small cell lung cancer. Cancer Res 2008, 68: 8547-8554.
43. Potapova IA, El-Maghrabi MR, Doronin SV and Benjamin WB. Phosphorylation of recombinant human ATP:citrate lyase by cAMPdependent protein kinase abolishes homotropic allosteric regulation of the enzyme by citrate and increases the enzyme activity. Allosteric activation of ATP:citrate lyase by phosphorylated sugars. Biochemistry 2000, 39: 1169-1179.
44. Lin R, Tao R, Gao X, Li T, Zhou X, Guan KL and Xiong Y, et al. Acetylation stabilizes ATP-citrate lyase to promote lipid biosynthesis and tumor growth. Mol Cell 2013, 51: 506-518.
45. Hatzivassiliou G, Zhao F, Bauer DE, Andreadis C, Shaw AN, Dhanak D and Hingorani SR, et al. ATP citrate lyase inhibition can suppress tumor cell growth. Cancer Cell 2005, 8: 311-321.
46. Dickinson BC and Chang CJ. Chemistry and biology of reactive oxygen species in signaling or stress responses. Nat Chem Biol 2011, 7: 504-511.
47. Gupta SC, Hevia D, Patchva S, Park B, Koh Wand Aggarwal BB. Upsides and downsides of reactive oxygen species for cancer: the roles of reactive oxygen species in tumorigenesis, prevention, and therapy. Antioxid Redox Signal 2012, 16: 1295-1322.
48. Irani K, Xia Y, Zweier JL, Sollott SJ, Der CJ, Fearon ER and Sundaresan M, et al. Mitogenic signaling mediated by oxidants in Ras-Transformed fibroblasts. Science 1997, 275: 1649-1652.
49. Waris G and Ahsan H. Reactive oxygen species: role in the development of cancer and various chronic conditions. J Carcinog 2006, 5: 14.
50. Miao L and St. Clair DK. Regulation of superoxide dismutase genes: implications in disease. Free Radic Biol Med 2009, 47: 344-356.
51. Chen Y, Zhang J, Lin Y, Lei Q, Guan KL, Zhao S and Xiong Y. Tumour suppressor SIRT3 deacetylates and activates manganese superoxide dismutase to scavenge ROS. EMBO Rep 2011, 12: 534-541.
52. Qiu X, Brown K, Hirschey MD, Verdin E and Chen D. Calorie restriction reduces oxidative stress by SIRT3-mediated SOD2 activation. Cell Metab 2010, 12: 662-667.
53. Tao R, Coleman MC, Pennington JD, Ozden O, Park SH, Jiang H and Kim HS, et al. Sirt3-mediated deacetylation of evolutionarily conserved lysine 122 regulates MnSOD activity in response to stress. Mol Cell 2010, 40: 893-904.
54. Someya S, Yu W, Hallows WC, Xu J, Vann JM, Leeuwenburgh C and Tanokura M, et al. Sirt3 mediates reduction of oxidative damage and prevention of age-related hearing loss under caloric restriction. Cell 2010, 143: 802-812.
55. Bhardwaj A and Wilkinson MF. A metabolic enzyme doing double duty as a transcription factor. Bioessays 2005, 27: 467-471.
56. Jeffery CJ. Moonlighting proteins: old proteins learning new tricks. Trends Genet 2003, 19: 415-417.
57. Luo W, Hu H, Chang R, Zhong J, Knabel M, O'Meally R and Cole RN, et al. Pyruvate kinase M2 is a PHD3-stimulated coactivator for hypoxia-inducible factor 1. Cell 2011, 145: 732-744.
58. Yang W, Zheng Y, Xia Y, Ji H, Chen X, Guo F and Lyssiotis CA, et al. ERK1/2-dependent phosphorylation and nuclear translocation of PKM2 promotes the Warburg effect. Nat Cell Biol 2012, 14: 1295-1304.
59. Lv L, Xu YP, Zhao D, Li FL, Wang W, Sasaki N and Jiang Y, et al. Mitogenic and oncogenic stimulation of K433 acetylation promotes PKM2 protein kinase activity and nuclear localization. Mol Cell 2013, 52: 1-13.
60. Zhang T, Wang S, Lin Y, Xu W, Ye D, Xiong Y and Zhao S, et al. Acetylation negatively regulates glycogen phosphorylase by recruiting protein phosphatase 1. Cell Metab 2012, 15: 75-87.
61. Ronai Z. Glycolytic enzymes as DNA binding proteins. Int J Biochem 1993, 25: 1073-1076.
62. Sirover MA. New insights into an old protein: the functional diversity of mammalian glyceraldehyde-3-phosphate dehydrogenase. Biochim Biophys Acta 1999, 1432: 159-184.
63. Bonafe N, Gilmore-Hebert M, Folk NL, Azodi M, Zhou Y and Chambers SK. Glyceraldehyde-3-phosphate dehydrogenase binds to the AU-Rich 30 untranslated region of colony-stimulating factor-1 (CSF-1) messenger RNA in human ovarian cancer cells: possible role in CSF-1 posttranscriptional regulation and tumor phenotype. Cancer Res 2005, 65: 3762-3771.
64. Krynetski EY, Krynetskaia NF, Bianchi ME and Evans WE. A nuclear protein complex containing high mobility group proteins B1 and B2, heat shock cognate protein 70, ERp60, and glyceraldehyde-3-phosphate dehydrogenase is involved in the cytotoxic response to DNA modified by incorporation of anticancer nucleoside analogues. Cancer Res 2003, 63: 100-106.
65. Demarse NA, Ponnusamy S, Spicer EK, Apohan E, Baatz JE, Ogretmen B and Davies C. Direct binding of glyceraldehyde 3-phosphate dehydrogenase to telomeric DNA protects telomeres against chemotherapy-induced rapid degradation. J Mol Biol 2009, 394: 789-803.
66. Sundararaj KP, Wood RE, Ponnusamy S, Salas AM, Szulc Z, Bielawska A and Obeid LM, et al. Rapid shortening of telomere length in response to ceramide involves the inhibition of telomere binding activity of nuclear glyceraldehyde-3-phosphate dehydrogenase. J Biol Chem 2004, 279: 6152-6162.
67. Shashidharan P, Chalmers-Redman RM, Carlile GW, Rodic V, Gurvich N, Yuen T and Tatton WG, et al. Nuclear translocation of GAPDH-GFP fusion protein during apoptosis. Neuroreport 1999, 10: 1149-1153.
68. Hara MR, Agrawal N, Kim SF, Cascio MB, Fujimuro M, Ozeki Y and Takahashi M, et al. S-nitrosylated GAPDH initiates apoptotic cell death by nuclear translocation following Siah1 binding. Nat Cell Biol 2005, 7: 665-674.
69. Huang Q, Lan F, Zheng Z, Xie F, Han J, Dong L and Xie Y, et al. Akt2 kinase suppresses glyceraldehyde-3-phosphate dehydrogenase (GAPDH)- mediated apoptosis in ovarian cancer cells via phosphorylating GAPDH at threonine 237 and decreasing its nuclear translocation. J Biol Chem 2011, 286: 42211-42220.
70. Ventura M, Mateo F, Serratosa J, Salaet I, Carujo S, Bachs O and Pujol MJ. Nuclear translocation of glyceraldehyde-3-phosphate dehydrogenase is regulated by acetylation. Int J Biochem Cell Biol 2010, 42: 1672-1680.
71. Sen N, Hara MR, Kornberg MD, Cascio MB, Bae BI, Shahani N and Thomas B, et al. Nitric oxide-induced nuclear GAPDH activates p300/CBP and mediates apoptosis. Nat Cell Biol 2008, 10: 866-873.
72. Joo HY, Woo SR, Shen YN, Yun MY, Shin HJ, Park ER and Kim SH, et al. SIRT1 interacts with and protects glyceraldehyde-3-phosphate dehydrogenase (GAPDH) from nuclear translocation: implications for cell survival after irradiation. Biochem Biophys Res Commun 2012, 424: 681-686.
73. Harada N, Yasunaga R, Higashimura Y, Yamaji R, Fujimoto K, Moss J and Inui H, et al. Glyceraldehyde-3-phosphate dehydrogenase enhances transcriptional activity of androgen receptor in prostate cancer cells. J Biol Chem 2007, 282: 22651-22661.
74. Heinlein CA and Chang C. Androgen receptor in prostate cancer. Endocr Rev 2004, 25: 276-308.