Information
References
Contents
Download
[1]O Warburg: On respiratory impairment in cancer cells. Science 124(3215), 269-270 (1956)
[2]O Warburg: On the origin of cancer cells. Science 123(3191), 309-314 (1956)
[3]O Warburg, S Minami: Versuche an Uberlebendem Carcinomgewebe. Klin Wochenschr 2(17), 776-777 (1923)
[4]E Racker: Bioenergetics and the problem of tumor growth. Am Sci 60(1), 56-63 (1972)
[5]A J Levine, A M Puzio-Kuter: The control of the metabolic switch in cancers by oncogenes and tumor suppressor genes. Science 330(6009), 1340-1344 (2010)
[6]C Munoz-Pinedo, N El Mjiyad, J E Ricci: Cancer metabolism: current perspectives and future directions. Cell Death Dis 3, e248 (2012)
[7]C V Dang, G L Semenza: Oncogenic alterations of metabolism. Trends Biochem Sci 24(2), 68-72 (1999)
[8]R C Osthus, H Shim, S Kim, Q Li, R Reddy, M Mukherjee, Y Xu, D Wonsey, L A Lee, C V Dang: Deregulation of glucose transporter 1 and glycolytic gene expression by c-Myc. J Biol Chem 275(29), 21797-21800 (2000)
[9]T Soga: Cancer metabolism: key players in metabolic reprogramming. Cancer Sci 104(3), 275-281 (2013)
[10]D Burk: A colloquial consideration of the Pasteur and neo-Pasteur effects. Cold Spring Harb Symp Quant Biol 7, 420-459 (1939)
[11]P Gao, I Tchernyshyov, T C Chang, Y S Lee, K Kita, T Ochi, K I Zeller, A M De Marzo, J E Van Eyk, J T Mendell, C V Dang: c-Myc suppression of miR-23a/b enhances mitochondrial glutaminase expression and glutamine metabolism. Nature 458(7239), 762-765 (2009)
[12]W H Koppenol, P L Bounds, C V Dang: Otto Warburg’s contributions to current concepts of cancer metabolism. Nat Rev Cancer 11(5), 325-337 (2011)
[13]D Senyilmaz, A A Teleman: Chicken or the egg: Warburg effect and mitochondrial dysfunction. F1000Prime Rep 7, 41 (2015)
[14]D G Hardie, F A Ross, S A Hawley: AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat Rev Mol Cell Biol 13(4), 251-262 (2012)
[15]H Yan, D W Parsons, G Jin, R McLendon, B A Rasheed, W Yuan, I Kos, I Batinic-Haberle, S Jones, G J Riggins, H Friedman, A Friedman, D Reardon, J Herndon, K W Kinzler, V E Velculescu, B Vogelstein, D D Bigner: IDH1 and IDH2 mutations in gliomas. N Engl J Med 360(8), 765-773 (2009)
[16]G Yang, F Cui, N Hou, X Cheng, J Zhang, Y Wang, N Jiang, X Gao, X Yang: Transgenic mice that express Cre recombinase in hypertrophic chondrocytes. Genesis 42(1), 33-36 (2005)
[17]V C de Boer, S M Houten: A mitochondrial expatriate: nuclear pyruvate dehydrogenase. Cell 158(1), 9-10 (2014)
[18]S A Comerford, Z Huang, X Du, Y Wang, L Cai, A K Witkiewicz, H Walters, M N Tantawy, A Fu, H C Manning, J D Horton, R E Hammer, S L McKnight, B P Tu: Acetate dependence of tumors. Cell 159(7), 1591-1602 (2014)
[19]G Sutendra, A Kinnaird, P Dromparis, R Paulin, T H Stenson, A Haromy, K Hashimoto, N Zhang, E Flaim, E D Michelakis: A nuclear pyruvate dehydrogenase complex is important for the generation of acetyl-CoA and histone acetylation. Cell 158(1), 84-97 (2014)
[20]T Mikawa, L L ME, A Takaori-Kondo, N Inagaki, M Yokode, H Kondoh: Dysregulated glycolysis as an oncogenic event. Cell Mol Life Sci 72(10), 1881-1892 (2015)
[21]T Hitosugi, S Kang, M G Vander Heiden, T W Chung, S Elf, K Lythgoe, S Dong, S Lonial, X Wang, G Z Chen, J Xie, T L Gu, R D Polakiewicz, J L Roesel, T J Boggon, F R Khuri, D G Gilliland, L C Cantley, J Kaufman, J Chen: Tyrosine phosphorylation inhibits PKM2 to promote the Warburg effect and tumor growth. Sci Signal 2(97), ra73 (2009)
[22]H Ji, J H Lee, Y Wang, Y Pang, T Zhang, Y Xia, L Zhong, J Lyu, Z Lu: EGFR phosphorylates FAM129B to promote Ras activation. Proc Natl Acad Sci U S A 113(3), 644-649 (2016)
[23]H R Christofk, M G Vander Heiden, M H Harris, A Ramanathan, R E Gerszten, R Wei, M D Fleming, S L Schreiber, L C Cantley: The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature 452(7184), 230-233 (2008)
[24]M Cortes-Cros, C Hemmerlin, S Ferretti, J Zhang, J S Gounarides, H Yin, A Muller, A Haberkorn, P Chene, W R Sellers, F Hofmann: M2 isoform of pyruvate kinase is dispensable for tumor maintenance and growth. Proc Natl Acad Sci U S A 110(2), 489-494 (2013)
[25]B C Lewis, J E Prescott, S E Campbell, H Shim, R Z Orlowski, C V Dang: Tumor induction by the c-Myc target genes rcl and lactate dehydrogenase A. Cancer Res 60(21), 6178-6183 (2000)
[26]H Shim, C Dolde, B C Lewis, C S Wu, G Dang, R A Jungmann, R Dalla-Favera, C V Dang: c-Myc transactivation of LDH-A: implications for tumor metabolism and growth. Proc Natl Acad Sci U S A 94(13), 6658-6663 (1997)
[27]J D Firth, B L Ebert, P J Ratcliffe: Hypoxic regulation of lactate dehydrogenase A. Interaction between hypoxia-inducible factor 1 and cAMP response elements. J Biol Chem 270(36), 21021-21027 (1995)
[28]C Benassayag, L Montero, N Colombie, P Gallant, D Cribbs, D Morello: Human c-Myc isoforms differentially regulate cell growth and apoptosis in Drosophila melanogaster. Mol Cell Biol 25(22), 9897-9909 (2005)
[29]L Aram, T Braun, C Braverman, Y Kaplan, L Ravid, S Levin-Zaidman, E Arama: A Krebs Cycle Component Limits Caspase Activation Rate through Mitochondrial Surface Restriction of CRL Activation. Dev Cell 37(1), 15-33 (2016)
[30]X Ding, Q B Jiang, R Li, S Chen, S Zhang: NOK/STYK1 has a strong tendency towards forming aggregates and colocalises with epidermal growth factor receptor in endosomes. Biochem Biophys Res Commun, 421(3) 468-473 (2012)
[31]L Shi, B P Tu: Acetyl-CoA and the regulation of metabolism: mechanisms and consequences. Curr Opin Cell Biol 33, 125-131 (2015)
[32]L Cai, B M Sutter, B Li, B P Tu: Acetyl-CoA induces cell growth and proliferation by promoting the acetylation of histones at growth genes. Mol Cell 42(4) 426-437 (2011)
Article Metrics
Download
- Contents
Information
Download
Contents
Frontiers in Bioscience-Landmark (FBL) is published by IMR Press from Volume 26 Issue 5 (2021). Previous articles were published by another publisher on a subscription basis, and they are hosted by IMR Press on imrpress.com as a courtesy and upon agreement with Frontiers in Bioscience.
NOK mediates glycolysis and nuclear PDC associated histone acetylation
1 Department of Microbiology, Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences and School of Basic Medicine, Peking Union Medical College, Beijing 100005, China
2 State Key Laboratory of Proteomics, Genetic Laboratory of Development and Diseases, Institute of Biotechnology, Beijing 100071, China
3 National Key Laboratory of Medical Molecular Biology and Department of Immunology, Institute of Basic Medical Sciences, Chinese Academy of Medical Sciences, Beijing 100005, China
4 Department of Radiation Oncology, Weill Medical College of Cornell University, New York, New York 10065, USA
Abstract
NOK is a potent oncogene that can transform normal cells to cancer cells. We hypothesized that NOK might impact cancer cell metabolism and histone acetylation. We show that NOK localizes in the mitochondria, and while it minimally impacts tricarboxylic acid (TCA) cycle, it markedly inhibits the process of electron transport and oxidative phosphorylation processes and dramatically enhances aerobic glycolysis in cancer cells. NOK promotes the mitochondrial-nuclear translocation of pyruvate dehydrogenase complex (PDC), and enhances histone acetylation in the nucleus. Together, these findings show that NOK mediates glycolysis and nuclear PDC associated histone acetylation.
Keywords
- RPTK
- NOK
- Warburg Effect
- Aerobic Glycolysis
- Mitochondria-Nucleus Translocation
- Mitochondria
- acetyl-CoA
- Acetylation
- Histone
- Pyruvate Dehydrogenase Complex
- Tricarboxylic Acid Cycle
References
- [1] O Warburg: On respiratory impairment in cancer cells. Science 124(3215), 269-270 (1956)
- [2] O Warburg: On the origin of cancer cells. Science 123(3191), 309-314 (1956)
- [3] O Warburg, S Minami: Versuche an Uberlebendem Carcinomgewebe. Klin Wochenschr 2(17), 776-777 (1923)
- [4] E Racker: Bioenergetics and the problem of tumor growth. Am Sci 60(1), 56-63 (1972)
- [5] A J Levine, A M Puzio-Kuter: The control of the metabolic switch in cancers by oncogenes and tumor suppressor genes. Science 330(6009), 1340-1344 (2010)
- [6] C Munoz-Pinedo, N El Mjiyad, J E Ricci: Cancer metabolism: current perspectives and future directions. Cell Death Dis 3, e248 (2012)
- [7] C V Dang, G L Semenza: Oncogenic alterations of metabolism. Trends Biochem Sci 24(2), 68-72 (1999)
- [8] R C Osthus, H Shim, S Kim, Q Li, R Reddy, M Mukherjee, Y Xu, D Wonsey, L A Lee, C V Dang: Deregulation of glucose transporter 1 and glycolytic gene expression by c-Myc. J Biol Chem 275(29), 21797-21800 (2000)
- [9] T Soga: Cancer metabolism: key players in metabolic reprogramming. Cancer Sci 104(3), 275-281 (2013)
- [10] D Burk: A colloquial consideration of the Pasteur and neo-Pasteur effects. Cold Spring Harb Symp Quant Biol 7, 420-459 (1939)
- [11] P Gao, I Tchernyshyov, T C Chang, Y S Lee, K Kita, T Ochi, K I Zeller, A M De Marzo, J E Van Eyk, J T Mendell, C V Dang: c-Myc suppression of miR-23a/b enhances mitochondrial glutaminase expression and glutamine metabolism. Nature 458(7239), 762-765 (2009)
- [12] W H Koppenol, P L Bounds, C V Dang: Otto Warburg’s contributions to current concepts of cancer metabolism. Nat Rev Cancer 11(5), 325-337 (2011)
- [13] D Senyilmaz, A A Teleman: Chicken or the egg: Warburg effect and mitochondrial dysfunction. F1000Prime Rep 7, 41 (2015)
- [14] D G Hardie, F A Ross, S A Hawley: AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat Rev Mol Cell Biol 13(4), 251-262 (2012)
- [15] H Yan, D W Parsons, G Jin, R McLendon, B A Rasheed, W Yuan, I Kos, I Batinic-Haberle, S Jones, G J Riggins, H Friedman, A Friedman, D Reardon, J Herndon, K W Kinzler, V E Velculescu, B Vogelstein, D D Bigner: IDH1 and IDH2 mutations in gliomas. N Engl J Med 360(8), 765-773 (2009)
- [16] G Yang, F Cui, N Hou, X Cheng, J Zhang, Y Wang, N Jiang, X Gao, X Yang: Transgenic mice that express Cre recombinase in hypertrophic chondrocytes. Genesis 42(1), 33-36 (2005)
- [17] V C de Boer, S M Houten: A mitochondrial expatriate: nuclear pyruvate dehydrogenase. Cell 158(1), 9-10 (2014)
- [18] S A Comerford, Z Huang, X Du, Y Wang, L Cai, A K Witkiewicz, H Walters, M N Tantawy, A Fu, H C Manning, J D Horton, R E Hammer, S L McKnight, B P Tu: Acetate dependence of tumors. Cell 159(7), 1591-1602 (2014)
- [19] G Sutendra, A Kinnaird, P Dromparis, R Paulin, T H Stenson, A Haromy, K Hashimoto, N Zhang, E Flaim, E D Michelakis: A nuclear pyruvate dehydrogenase complex is important for the generation of acetyl-CoA and histone acetylation. Cell 158(1), 84-97 (2014)
- [20] T Mikawa, L L ME, A Takaori-Kondo, N Inagaki, M Yokode, H Kondoh: Dysregulated glycolysis as an oncogenic event. Cell Mol Life Sci 72(10), 1881-1892 (2015)
- [21] T Hitosugi, S Kang, M G Vander Heiden, T W Chung, S Elf, K Lythgoe, S Dong, S Lonial, X Wang, G Z Chen, J Xie, T L Gu, R D Polakiewicz, J L Roesel, T J Boggon, F R Khuri, D G Gilliland, L C Cantley, J Kaufman, J Chen: Tyrosine phosphorylation inhibits PKM2 to promote the Warburg effect and tumor growth. Sci Signal 2(97), ra73 (2009)
- [22] H Ji, J H Lee, Y Wang, Y Pang, T Zhang, Y Xia, L Zhong, J Lyu, Z Lu: EGFR phosphorylates FAM129B to promote Ras activation. Proc Natl Acad Sci U S A 113(3), 644-649 (2016)
- [23] H R Christofk, M G Vander Heiden, M H Harris, A Ramanathan, R E Gerszten, R Wei, M D Fleming, S L Schreiber, L C Cantley: The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature 452(7184), 230-233 (2008)
- [24] M Cortes-Cros, C Hemmerlin, S Ferretti, J Zhang, J S Gounarides, H Yin, A Muller, A Haberkorn, P Chene, W R Sellers, F Hofmann: M2 isoform of pyruvate kinase is dispensable for tumor maintenance and growth. Proc Natl Acad Sci U S A 110(2), 489-494 (2013)
- [25] B C Lewis, J E Prescott, S E Campbell, H Shim, R Z Orlowski, C V Dang: Tumor induction by the c-Myc target genes rcl and lactate dehydrogenase A. Cancer Res 60(21), 6178-6183 (2000)
- [26] H Shim, C Dolde, B C Lewis, C S Wu, G Dang, R A Jungmann, R Dalla-Favera, C V Dang: c-Myc transactivation of LDH-A: implications for tumor metabolism and growth. Proc Natl Acad Sci U S A 94(13), 6658-6663 (1997)
- [27] J D Firth, B L Ebert, P J Ratcliffe: Hypoxic regulation of lactate dehydrogenase A. Interaction between hypoxia-inducible factor 1 and cAMP response elements. J Biol Chem 270(36), 21021-21027 (1995)
- [28] C Benassayag, L Montero, N Colombie, P Gallant, D Cribbs, D Morello: Human c-Myc isoforms differentially regulate cell growth and apoptosis in Drosophila melanogaster. Mol Cell Biol 25(22), 9897-9909 (2005)
- [29] L Aram, T Braun, C Braverman, Y Kaplan, L Ravid, S Levin-Zaidman, E Arama: A Krebs Cycle Component Limits Caspase Activation Rate through Mitochondrial Surface Restriction of CRL Activation. Dev Cell 37(1), 15-33 (2016)
- [30] X Ding, Q B Jiang, R Li, S Chen, S Zhang: NOK/STYK1 has a strong tendency towards forming aggregates and colocalises with epidermal growth factor receptor in endosomes. Biochem Biophys Res Commun, 421(3) 468-473 (2012)
- [31] L Shi, B P Tu: Acetyl-CoA and the regulation of metabolism: mechanisms and consequences. Curr Opin Cell Biol 33, 125-131 (2015)
- [32] L Cai, B M Sutter, B Li, B P Tu: Acetyl-CoA induces cell growth and proliferation by promoting the acetylation of histones at growth genes. Mol Cell 42(4) 426-437 (2011)