Loss of SIRT3 provides growth advantage for B cell malignancies

Journal of Biological Chemistry

Volumn 291, Issue 7, 2016, Pages 3268-3279

  Yu, Wei ^a   Denu, Ryan A ^a   Krautkramer, Kimberly A ^a   Grindle, Kreg M ^a   Yang, David T ^a   Asimakopoulos, Fotis ^a,b   Hematti, Peiman ^a,b   Denu, John M ^a,b,c  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^b UNIVERSITY OF WISCONSIN   (United States)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLATION; CELL CULTURE; CHEMICAL ACTIVATION; CYTOLOGY; DISEASES; ENZYMES; OXYGEN; PROTEINS; TUMORS;

CHRONIC LYMPHOCYTIC LEUKEMIAS; ENZYMATIC ACTIVITIES; HYPOXIA-INDUCIBLE FACTOR 1; ISOCITRATE DEHYDROGENASE; MITOCHONDRIAL MATRIX; MITOCHONDRIAL PROTEIN; REACTIVE OXYGEN SPECIES; SUPEROXIDE DISMUTASE 2;

CELLS;

HYPOXIA INDUCIBLE FACTOR 1ALPHA; ISOCITRATE DEHYDROGENASE 2; MANGANESE SUPEROXIDE DISMUTASE; MESSENGER RNA; SIRTUIN 3; ISOCITRATE DEHYDROGENASE; ISOCITRATE DEHYDROGENASE 2, HUMAN; REACTIVE OXYGEN METABOLITE; RECOMBINANT PROTEIN; SIRT3 PROTEIN, HUMAN; SUPEROXIDE DISMUTASE; TUMOR PROTEIN;

ACETYLATION; AEROBIC METABOLISM; ARTICLE; B LYMPHOCYTE; BURKITT LYMPHOMA; CANCER CELL; CANCER PROGNOSIS; CANCER SURVIVAL; CELL GROWTH; CELL PROLIFERATION; CHRONIC LYMPHATIC LEUKEMIA; CONTROLLED STUDY; DEACETYLATION; DOWN REGULATION; ENZYME ACTIVITY; FOLLICULAR LYMPHOMA; GENE MUTATION; GROWTH INHIBITION; HUMAN; HUMAN CELL; LACTATE DEHYDROGENASE BLOOD LEVEL; LEUKOCYTE COUNT; MANTLE CELL LYMPHOMA; MITOCHONDRIAL MEMBRANE POTENTIAL; MULTIPLE MYELOMA; OVERALL SURVIVAL; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN EXPRESSION; SURVIVAL RATE; AGED; AGONISTS; ANTAGONISTS AND INHIBITORS; CANCER STAGING; CHEMISTRY; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PATHOLOGY; PROTEIN PROCESSING; RNA INTERFERENCE; SURVIVAL ANALYSIS; TUMOR CELL CULTURE; TUMOR CELL LINE;

ACETYLATION; AGED; BURKITT LYMPHOMA; CELL LINE, TUMOR; CELL PROLIFERATION; ENZYME ACTIVATION; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; ISOCITRATE DEHYDROGENASE; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; LYMPHOMA, FOLLICULAR; LYMPHOMA, MANTLE-CELL; NEOPLASM PROTEINS; NEOPLASM STAGING; PROTEIN PROCESSING, POST-TRANSLATIONAL; REACTIVE OXYGEN SPECIES; RECOMBINANT PROTEINS; RNA INTERFERENCE; SIRTUIN 3; SUPEROXIDE DISMUTASE; SURVIVAL ANALYSIS; TUMOR CELLS, CULTURED;

EID: 84964680484     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.702076     Document Type: Article

References (49)

1. Harris, N. L., and Jaffe, E. S., Diebold, J., Flandrin, G., Muller-Hermelink, H. K., Vardiman, J., Lister, T.A., and Bloomfield, C.D. (1999) The World Health Organization classification of neoplastic diseases of the hematopoietic and lymphoid tissues: Report of the Clinical Advisory Committee meeting, Airlie House, Virginia, November, 1997. Ann. Oncol. 10, 1419-1432
2. Zwiebel, J. A., and Cheson, B. D. (1998) Chronic lymphocytic leukemia: staging and prognostic factors. Semin. Oncol. 25, 42-59
3. Keating, M. J., Chiorazzi, N, Messmer, B., Damle, R. N., Allen, S. L., Rai, K. R., Ferrarini, M., and Kipps, T. J. (2003) Biology and treatment of chronic lymphocytic leukemia. Hematology Am. Soc. Hematol. Educ. Program 153-175
4. Chiorazzi, N, and Rai, K. R., and Ferrarini, M. (2005) Chronic lymphocytic leukemia. N. Engl. J. Med. 352, 804-815
5. Imai, S., and Armstrong, C. M., Kaeberlein, M., and Guarente, L. (2000) Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature 403, 795-800
6. Michishita, E., and Park, J. Y., Burneskis, J. M., Barrett, J. C., and Horikawa, I. (2005) Evolutionarily conserved and nonconserved cellular localizations and functions of human SIRT proteins. Mol. Biol. Cell 16, 4623-4635
7. +-dependent deacetylases. Trends Biochem. Sci. 28, 41-48
8. Feldman, J. L., Dittenhafer-Reed, K. E., and Denu, J. M. (2012) Sirtuin catalysis and regulation. J. Biol. Chem. 287, 42419-42427
9. Guarente, L., and Picard, F. (2005) Calorie restriction: the SIR2 connection. Cell 120, 473-482
10. + levels dictate cell survival. Cell 130, 1095-1107
11. Hebert, A. S., Dittenhafer-Reed, K. E., Yu, W., Bailey, D. J., Selen, E. S., Boersma, M. D., Carson, J. J., Tonelli, M., Balloon, A. J., Higbee, A. J., Westphall, M. S., Pagliarini, D. J., Prolla, T. A., Assadi-Porter, F., Roy, S., Denu, J. M., and Coon, J. J. (2013) Calorie restriction and SIRT3 trigger global reprogramming of the mitochondrial protein acetylome. Mol. Cell 49, 186-199
12. Someya, S., Yu, W., Hallows, W. C., Xu, J., Vann, J. M., Leeuwenburgh, C., Tanokura, M., Denu, J. M., and Prolla, T. A. (2010) Sirt3 mediates reduction of oxidative damage and prevention of age-related hearing loss under caloric restriction. Cell 143, 802-812
13. Schlicker, C, Gertz, M., Papatheodorou, P., Kachholz, B., and Becker, C. F., and Steegborn, C. (2008) Substrates and regulation mechanisms for the human mitochondrial sirtuins Sirt3 and Sirt5. J. Mol. Biol. 382, 790-801
14. Yu, W., Dittenhafer-Reed, K. E., and Denu, J. M. (2012) SIRT3 protein deacetylates isocitrate dehydrogenase 2 (IDH2) and regulates mitochondrial redox status. J. Biol. Chem. 287, 14078-14086
15. +-dependent isocitrate dehydrogenase. J. Biol. Chem. 276, 16168-16176
16. Tao, R., Coleman, M. C., Pennington, J. D., Ozden, O., Park, S. H, Jiang, H, Kim, H. S., Flynn, C. R., Hill, S., Hayes McDonald, W., Olivier, A. K., Spitz, D. R., and Gius, D. (2010) Sirt3-mediated deacetylation of evolutionarily conserved lysine 122 regulates MnSOD activity in response to stress. Mol. Cell 40, 893-904
17. Chen, Y., Zhang, J., Lin, Y., Lei, Q., and Guan, K. L., Zhao, S., and Xiong, Y. (2011) Tumour suppressor SIRT3 deacetylates and activates manganese superoxide dismutase to scavenge ROS. EMBO Rep. 12, 534-541
18. Qiu, X., Brown, K., Hirschey, M. D., Verdin, E., and Chen, D. (2010) Calorie restriction reduces oxidative stress by SIRT3-mediated SOD2 activation. Cell Metab. 12, 662-667
19. Liou, G. Y., and Storz, P. (2010) Reactive oxygen species in cancer. Free Radic. Res. 44, 479-496
20. 2 sensing. J. Biol. Chem. 275, 25130-25138
21. Finley, L. W., Carracedo, A., Lee, J., Souza, A., Egia, A., Zhang, J., Teruya-Feldstein, J., Moreira, P. I., and Cardoso, S. M., Clish, C. B., Pandolfi, P. P., and Haigis, M. C. (2011) SIRT3 opposes reprogramming of cancer cell metabolism through HIF1a destabilization. Cancer Cell 19, 416-428
22. Warburg, O. (1956) On the origin of cancer cells. Science 123, 309-314
23. Kim, H. S., Patel, K., Muldoon-Jacobs, K., Bisht, K. S., Aykin-Burns, N., Pennington, J. D., van der Meer, R., Nguyen, P., Savage, J., Owens, K. M., Vassilopoulos, A., Ozden, O., Park, S. H., Singh, K. K., Abdulkadir, S. A., Spitz, D. R., Deng, C. X., and Gius, D. (2010) SIRT3 is a mitochondria-localized tumor suppressor required for maintenance of mitochondrial integrity and metabolism during stress. Cancer Cell 17, 41-52
24. Bell, E. L., and Emerling, B. M., Ricoult, S. J., and Guarente, L. (2011) SirT3 suppresses hypoxia inducible factor 1a and tumor growth by inhibiting mitochondrial ROS production. Oncogene 30, 2986-2996
25. Alhazzazi, T. Y., Kamarajan, P., Joo, N, and Huang, J. Y., Verdin, E., D'Silva, N. J., and Kapila, Y. L. (2011) Sirtuin-3 (SIRT3), a novel potential therapeutic target for oral cancer. Cancer 117, 1670-1678
26. + metabolites and modulates cellular redox. J. Biol. Chem. 284, 11256-11266
27. Kim, J., and Denu, R. A., Dollar, B.A., Escalante, L. E., Kuether, J. P., and Callander, N. S., Asimakopoulos, F., and Hematti, P. (2012) Macrophages and mesenchymal stromal cells support survival and proliferation of multiple myeloma cells. Br. J. Haematol. 158, 336-346
28. Oberley, M. J., and Rajguru, S. A., Zhang, C, Kim, K., and Shaw, G. R., Grindle, K. M., Kahl, B. S., Kanugh, C, Laffin, J., and Yang, D. T. (2013) Immunohistochemical evaluation of MYC expression in mantle cell lymphoma. Histopathology 63, 499-508
29. Semenza, G. L. (2003) Targeting HIF-1 for cancer therapy. Nat. Rev. Cancer 3, 721-732
30. Hoster, E., Dreyling, M., Klapper, W., Gisselbrecht, C, van Hoof, A., Kluin-Nelemans, H. C., Pfreundschuh, M., Reiser, M., Metzner, B., Einsele, H., Peter, N., Jung, W., Wörmann, B., Ludwig, W. D., Dührsen, U., Eimermacher, H., Wandt, H., Hasford, J., Hiddemann, W., Unterhalt, M., German Low Grade Lymphoma Study Group (GLSG), and European Mantle Cell Lymphoma Network (2008) A new prognostic index (MIPI) for patients with advanced-stage mantle cell lymphoma. Blood 111, 558-565
31. Li, N, Ragheb, K., Lawler, G., Sturgis, J., Rajwa, B., Melendez, J. A., and Robinson, J. P. (2003) Mitochondrial complex I inhibitor rotenone induces apoptosis through enhancing mitochondrial reactive oxygen species production. J. Biol. Chem. 278, 8516-8525
32. Carew, J. S., Zhou, Y., Albitar, M., Carew, J. D., and Keating, M. J., and Huang, P. (2003) Mitochondrial DNA mutations in primary leukemia cells after chemotherapy: clinical significance and therapeutic implications. Leukemia 17, 1437-1447
33. Lilienthal, N, Prinz, C, Peer-Zada, A. A., Doering, M., Ba, L. A., Hallek, M., Jacob, C., and Herling, M. (2011) Targeting the disturbed redox equilibrium in chronic lymphocytic leukemia by novel reactive oxygen species-catalytic 'sensor/effector' compounds. Leuk. Lymphoma 52, 1407-1411
34. Perry, S. W., and Norman, J. P., Barbieri, J., Brown, E. B., and Gelbard, H. A. (2011) Mitochondrial membrane potential probes and the proton gradient: a practical usage guide. BioTechniques 50, 98-115
35. Giannoni, E., Buricchi, F., Raugei, G., Ramponi, G., and Chiarugi, P. (2005) Intracellular reactive oxygen species activate Src tyrosine kinase during cell adhesion and anchorage-dependent cell growth. Mol. Cell Biol. 25, 6391-6403
36. Lee, S. R., and Yang, K. S., Kwon, J., Lee, C., Jeong, W., and Rhee, S. G. (2002) Reversible inactivation of the tumor suppressor PTEN by H2O2. J. Biol. Chem. 277, 20336-20342
37. Tretter, L., and Adam-Vizi, V. (2005) α-Ketoglutarate dehydrogenase: a target and generator of oxidative stress. Philos. Trans. R. Soc. Lond. B Biol. Sci. 360, 2335-2345
38. Alhazzazi, T. Y., Kamarajan, P., Verdin, E., and Kapila, Y. L. (2011) SIRT3 and cancer: tumor promoter or suppressor? Biochim. Biophys. Acta 1816, 80-88
39. Yan, S. M., Han, X., Han, P. J., and Chen, H. M., Huang, L. Y., and Li, Y. (2014) SIRT3 is a novel prognostic biomarker for esophageal squamous cell carcinoma. Med. Oncol. 31, 103
40. Ashraf, N, Zino, S., Macintyre, A., Kingsmore, D., and Payne, A. P., George, W. D., and Shiels, P. G. (2006) Altered sirtuin expression is associated with node-positive breast cancer. Br. J. Cancer 95, 1056-1061
41. Wang, J. X., Yi, Y., Li, Y. W., and Cai, X. Y., He, H. W., Ni, X. C., Zhou, J., and Cheng, Y. F., Jin, J. J., Fan, J., and Qiu, S. J. (2014) Down-regulation of sirtuin 3 is associated with poor prognosis in hepatocellular carcinoma after resection. BMC Cancer 14, 297
42. Zhang, Y. Y., and Zhou, L. M. (2012) Sirt3 inhibits hepatocellular carcinoma cell growth through reducing Mdm2-mediated p53 degradation. Biochem. Biophys. Res. Commun. 423, 26-31
43. Liu, C., Huang, Z., Jiang, H., and Shi, F. (2014) The sirtuin 3 expression profile is associated with pathological and clinical outcomes in colon cancer patients. Biomed. Res. Int. 2014, 871263
44. Van Damme, M., Crompot, E., Meuleman, N., Mineur, P., Bron, D., Lagneaux, L., and Stamatopoulos, B. (2012) HDAC isoenzyme expression is deregulated in chronic lymphocytic leukemia B-cells and has a complex prognostic significance. Epigenetics 7, 1403-1412
45. Wang, J. C., and Kafeel, M. I., Avezbakiyev, B., Chen, C., Sun, Y., Rathnasabapathy, C., Kalavar, M., He, Z., Burton, J., and Lichter, S. (2011) Histone deacetylase in chronic lymphocytic leukemia. Oncology 81, 325-329
46. Sasca, D., Hähnel, P. S., Szybinski, J., Khawaja, K., Kriege, O., Pante, S. V., Bullinger, L., Strand, S., Strand, D., Theobald, M., and Kindler, T. (2014) SIRT1 prevents genotoxic stress-induced p53 activation in acute myeloid leukemia. Blood 124, 121-133
47. Miyamoto, S., Ochiai, A., Boku, N., Ohtsu, A., Tahara, M., Yoshida, S., Okabe, H., Takechi, T., and Fukushima, M. (2001) Discrepancies between the gene expression, protein expression, and enzymatic activity of thymidylate synthase and dihydropyrimidine dehydrogenase in human gastrointestinal cancers and adjacent normal mucosa. Int. J. Oncol. 18, 705-713
48. Schedel, J., Distler, O., Woenckhaus, M., Gay, R. E., Simmen, B., and Michel, B. A., Müller-Ladner, U., and Gay, S. (2004) Discrepancy between mRNA and protein expression of tumour suppressor maspin in synovial tissue may contribute to synovial hyperplasia in rheumatoid arthritis. Ann. Rheum Dis. 63, 1205-1211
49. Kim, J. W., Tchernyshyov, I., Semenza, G. L., and Dang, C. V. (2006) HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab. 3, 177-185