Acetylation Targets the M2 Isoform of Pyruvate Kinase for Degradation through Chaperone-Mediated Autophagy and Promotes Tumor Growth

Molecular Cell

Volumn 42, Issue 6, 2011, Pages 719-730

  Lv, Lei ^a,b   Li, Dong ^c   Zhao, Di ^a,b   Lin, Ruiting ^a,b   Chu, Yajing ^d   Zhang, Heng ^a,b   Zha, Zhengyu ^a   Liu, Ying ^a   Li, Zi ^e   Xu, Yanping ^a,b   Wang, Gang ^d   Huang, Yiran ^c   Xiong, Yue ^a,b,f   Guan, Kun Liang ^a,g   Lei, Qun Ying ^a  

^a FUDAN UNIVERSITY   (China)

^b FUDAN UNIVERSITY   (China)

^c SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^d INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^e Shanghai Jiao Tong University Affiliated Sixth People s Hospital   (China)

^f UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHAPERONE; GLYCOLYTIC ENZYME; HEAT SHOCK COGNATE PROTEIN 70; MUTANT PROTEIN; PYRUVATE KINASE;

ACETYLATION; ANAEROBIC GLYCOLYSIS; ANIMAL CELL; ARTICLE; AUTOPHAGY; CELL PROLIFERATION; CONTROLLED STUDY; ENZYME ACTIVITY; GENETIC ASSOCIATION; HUMAN; LYSOSOME; MOUSE; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; TUMOR CELL; TUMOR GROWTH;

ACETYLATION; ANIMALS; AUTOPHAGY; CELL PROLIFERATION; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME ACTIVATION; GLUCOSE; HUMANS; ISOENZYMES; LYSINE; LYSOSOMES; MALE; MICE; MICE, NUDE; MOLECULAR CHAPERONES; MUTATION; P300-CBP TRANSCRIPTION FACTORS; PROSTATIC NEOPLASMS; PYRUVATE KINASE; STRUCTURE-ACTIVITY RELATIONSHIP; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 79959371914     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2011.04.025     Document Type: Article

References (44)

1. Altenberg B., Greulich K.O. Genes of glycolysis are ubiquitously overexpressed in 24 cancer classes. Genomics 2004, 84:1014-1020.
2. Avalos J.L., Bever K.M., Wolberger C. Mechanism of sirtuin inhibition by nicotinamide: altering the NAD(+) cosubstrate specificity of a Sir2 enzyme. Mol. Cell 2005, 17:855-868.
3. Bensaad K., Tsuruta A., Selak M.A., Vidal M.N., Nakano K., Bartrons R., Gottlieb E., Vousden K.H. TIGAR, a p53-inducible regulator of glycolysis and apoptosis. Cell 2006, 126:107-120.
4. Chen C.C., Carson J.J., Feser J., Tamburini B., Zabaronick S., Linger J., Tyler J.K. Acetylated lysine 56 on histone H3 drives chromatin assembly after repair and signals for the completion of repair. Cell 2008, 134:231-243.
5. Choudhary C., Kumar C., Gnad F., Nielsen M.L., Rehman M., Walther T.C., Olsen J.V., Mann M. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 2009, 325:834-840.
6. Christofk H.R., Vander Heiden M.G., Harris M.H., Ramanathan A., Gerszten R.E., Wei R., Fleming M.D., Schreiber S.L., Cantley L.C. The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature 2008, 452:230-233.
7. Christofk H.R., Vander Heiden M.G., Wu N., Asara J.M., Cantley L.C. Pyruvate kinase M2 is a phosphotyrosine-binding protein. Nature 2008, 452:181-186.
8. Ciechanover A. Intracellular protein degradation: from a vague idea thru the lysosome and the ubiquitin-proteasome system and onto human diseases and drug targeting. Cell Death Differ. 2005, 12:1178-1190.
9. Cuervo A.M. Chaperone-mediated autophagy: selectivity pays off. Trends Endocrinol. Metab. 2009, 21:142-150.
10. Cuervo A.M., Knecht E., Terlecky S.R., Dice J.F. Activation of a selective pathway of lysosomal proteolysis in rat liver by prolonged starvation. Am. J. Physiol. 1995, 269:C1200-C1208.
11. Cuervo A.M., Stefanis L., Fredenburg R., Lansbury P.T., Sulzer D. Impaired degradation of mutant alpha-synuclein by chaperone-mediated autophagy. Science 2004, 305:1292-1295.
12. Dang C.V., Semenza G.L. Oncogenic alterations of metabolism. Trends Biochem. Sci. 1999, 24:68-72.
13. David C.J., Chen M., Assanah M., Canoll P., Manley J.L. HnRNP proteins controlled by c-Myc deregulate pyruvate kinase mRNA splicing in cancer. Nature 2009, 463:364-368.
14. Dice J.F. Peptide sequences that target cytosolic proteins for lysosomal proteolysis. Trends Biochem. Sci. 1990, 15:305-309.
15. Dice J.F., Terlecky S.R., Chiang H.L., Olson T.S., Isenman L.D., Short-Russell S.R., Freundlieb S., Terlecky L.J. A selective pathway for degradation of cytosolic proteins by lysosomes. Semin. Cell Biol. 1990, 1:449-455.
16. Dombrauckas J.D., Santarsiero B.D., Mesecar A.D. Structural basis for tumor pyruvate kinase M2 allosteric regulation and catalysis. Biochemistry 2005, 44:9417-9429.
17. Ekwall K., Olsson T., Turner B.M., Cranston G., Allshire R.C. Transient inhibition of histone deacetylation alters the structural and functional imprint at fission yeast centromeres. Cell 1997, 91:1021-1032.
18. Funes J.M., Quintero M., Henderson S., Martinez D., Qureshi U., Westwood C., Clements M.O., Bourboulia D., Pedley R.B., Moncada S., Boshoff C. Transformation of human mesenchymal stem cells increases their dependency on oxidative phosphorylation for energy production. Proc. Natl. Acad. Sci. USA 2007, 104:6223-6228.
19. Furumai R., Komatsu Y., Nishino N., Khochbin S., Yoshida M., Horinouchi S. Potent histone deacetylase inhibitors built from trichostatin A and cyclic tetrapeptide antibiotics including trapoxin. Proc. Natl. Acad. Sci. USA 2001, 98:87-92.
20. Gordan J.D., Bertout J.A., Hu C.J., Diehl J.A., Simon M.C. HIF-2alpha promotes hypoxic cell proliferation by enhancing c-myc transcriptional activity. Cancer Cell 2007, 11:335-347.
21. Gordan J.D., Thompson C.B., Simon M.C. HIF and c-Myc: sibling rivals for control of cancer cell metabolism and proliferation. Cancer Cell 2007, 12:108-113.
22. Hitosugi T., Kang S., Vander Heiden M.G., Chung T.W., Elf S., Lythgoe K., Dong S., Lonial S., Wang X., Chen G.Z., et al. Tyrosine phosphorylation inhibits PKM2 to promote the Warburg effect and tumor growth. Sci. Signal. 2009, 2:ra73. 10.1126/scisignal.2000431.
23. Jeong H., Then F., Melia T.J., Mazzulli J.R., Cui L., Savas J.N., Voisine C., Paganetti P., Tanese N., Hart A.C., et al. Acetylation targets mutant huntingtin to autophagosomes for degradation. Cell 2009, 137:60-72.
24. Jurica M.S., Mesecar A., Heath P.J., Shi W., Nowak T., Stoddard B.L. The allosteric regulation of pyruvate kinase by fructose-1,6-bisphosphate. Structure 1998, 6:195-210.
25. Kim S.C., Sprung R., Chen Y., Xu Y., Ball H., Pei J., Cheng T., Kho Y., Xiao H., Xiao L., et al. Substrate and functional diversity of lysine acetylation revealed by a proteomics survey. Mol. Cell 2006, 23:607-618.
26. Lei Q., Jiao J., Xin L., Chang C.J., Wang S., Gao J., Gleave M.E., Witte O.N., Liu X., Wu H. NKX3.1 stabilizes p53, inhibits AKT activation, and blocks prostate cancer initiation caused by PTEN loss. Cancer Cell 2006, 9:367-378.
27. Levine B., Kroemer G. Autophagy in the pathogenesis of disease. Cell 2007, 132:27-42.
28. Liang Y., Buettger C., Berner D.K., Matschinsky F.M. Chronic effect of fatty acids on insulin release is not through the alteration of glucose metabolism in a pancreatic beta-cell line (beta HC9). Diabetologia 1997, 40:1018-1027.
29. Liebermeister W. Predicting physiological concentrations of metabolites from their molecular structure. J. Comput. Biol. 2005, 12:1307-1315.
30. Majeski A.E., Dice J.F. Mechanisms of chaperone-mediated autophagy. Int. J. Biochem. Cell Biol. 2004, 36:2435-2444.
31. Majumder P.K., Febbo P.G., Bikoff R., Berger R., Xue Q., McMahon L.M., Manola J., Brugarolas J., McDonnell T.J., Golub T.R., et al. mTOR inhibition reverses Akt-dependent prostate intraepithelial neoplasia through regulation of apoptotic and HIF-1-dependent pathways. Nat. Med. 2004, 10:594-601.
32. Manning B.D., Cantley L.C. AKT/PKB signaling: navigating downstream. Cell 2007, 129:1261-1274.
33. Massey A., Kiffin R., Cuervo A.M. Pathophysiology of chaperone-mediated autophagy. Int. J. Biochem. Cell Biol. 2004, 36:2420-2434.
34. Matoba S., Kang J.G., Patino W.D., Wragg A., Boehm M., Gavrilova O., Hurley P.J., Bunz F., Hwang P.M. p53 regulates mitochondrial respiration. Science 2006, 312:1650-1653.
35. Mazurek S., Boschek C.B., Hugo F., Eigenbrodt E. Pyruvate kinase type M2 and its role in tumor growth and spreading. Semin. Cancer Biol. 2005, 15:300-308.
36. Mizushima N., Levine B., Cuervo A.M., Klionsky D.J. Autophagy fights disease through cellular self-digestion. Nature 2008, 451:1069-1075.
37. Ramanathan A., Wang C., Schreiber S.L. Perturbational profiling of a cell-line model of tumorigenesis by using metabolic measurements. Proc. Natl. Acad. Sci. USA 2005, 102:5992-5997.
38. Soutoglou E., Katrakili N., Talianidis I. Acetylation regulates transcription factor activity at multiple levels. Mol. Cell 2000, 5:745-751.
39. Wang X., Hayes J.J. Acetylation mimics within individual core histone tail domains indicate distinct roles in regulating the stability of higher-order chromatin structure. Mol. Cell. Biol. 2008, 28:227-236.
40. Warburg O. On the origin of cancer cells. Science 1956, 123:309-314.
41. Wing S., Chiang H.L., Goldberg A.L., Dice J.F. Proteins containing peptide sequences related to KFERQ are selectively depleted in liver and heart, but notskeletal muscle, of fasted rats. Biochem. J. 1991, 275:165-169.
42. Yang Q., She H., Gearing M., Colla E., Lee M., Shacka J.J., Mao Z. Regulation of neuronal survival factor MEF2D by chaperone-mediated autophagy. Science 2009, 323:124-127.
43. Zhang W., Bone J.R., Edmondson D.G., Turner B.M., Roth S.Y. Essential and redundant functions of histone acetylation revealed by mutation of target lysines and loss of the Gcn5p acetyltransferase. EMBO J. 1998, 17:3155-3167.
44. Zhao S., Xu W., Jiang W., Yu W., Lin Y., Zhang T., Yao J., Zhou L., Zeng Y., Li H., et al. Regulation of cellular metabolism by protein lysine acetylation. Science 2010, 327:1000-1004.