Lymphocyte-specific protein tyrosine kinase (Lck) interacts with CR6-interacting factor 1 (CRIF1) in mitochondria to repress oxidative phosphorylation

BMC Cancer

Volumn 15, Issue 1, 2015, Pages

  Vahedi, Shahrooz ^a   Chueh, Fu Yu ^a   Chandran, Bala ^a   Yu, Chao Lan ^a,b  

^a ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

^b CHANG GUNG UNIVERSITY COLLEGE OF MEDICINE   (Taiwan)

Author keywords

Cancer metabolism; CRIF1; Electron transport chain; Lck; Leukemia; Mitochondria; Mitoribosome; Oxidative phosphorylation; Proximity ligation assay; Tid1

Indexed keywords

CR6 INTERACTING FACTOR 1; LYMPHOCYTE SPECIFIC PROTEIN TYROSINE KINASE; PROTEIN TID1; PROTEIN TYROSINE KINASE; REACTIVE OXYGEN METABOLITE; SHORT HAIRPIN RNA; SUPEROXIDE; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; DNAJA3 PROTEIN, HUMAN; GADD45GIP1 PROTEIN, HUMAN; HEAT SHOCK PROTEIN 40; NUCLEAR PROTEIN; PROTEIN KINASE LCK;

ANIMAL CELL; ARTICLE; CANCER CELL LINE; CELL FRACTIONATION; CELL STRUCTURE; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DOWN REGULATION; ELECTRON TRANSPORT; ENZYME ACTIVITY; ENZYME LOCALIZATION; ENZYME PHOSPHORYLATION; ENZYME REPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; JCAM CELL LINE; JURKAT CELL LINE; LEUKEMOGENESIS; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; MITOCHONDRION; MITORIBOSOME; MOUSE; NONHUMAN; NUCLEAR REPROGRAMMING; OXIDATIVE PHOSPHORYLATION; OXYGEN CONSUMPTION; PRECIPITATION; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; PROTEOMICS; RIBOSOME; T CELL LEUKEMIA; T LYMPHOCYTE; TRANSLATION REGULATION; TRANSMISSION ELECTRON MICROSCOPY; COMPARATIVE STUDY; METABOLISM; PHYSIOLOGY; PROCEDURES; TUMOR CELL LINE;

CELL CYCLE PROTEINS; CELL LINE, TUMOR; HSP40 HEAT-SHOCK PROTEINS; HUMANS; JURKAT CELLS; LEUKEMIA, T-CELL; LYMPHOCYTE SPECIFIC PROTEIN TYROSINE KINASE P56(LCK); MEMBRANE POTENTIAL, MITOCHONDRIAL; MITOCHONDRIA; NUCLEAR PROTEINS; OXIDATIVE PHOSPHORYLATION; PROTEOMICS;

EID: 84937779724     PISSN: None     EISSN: 14712407     Source Type: Journal    
DOI: 10.1186/s12885-015-1520-6     Document Type: Article

References (54)

1. Scatena R. Mitochondria and cancer: a growing role in apoptosis, cancer cell metabolism and dedifferentiation. Adv Exp Med Biol. 2012;942:287-308.
2. Seyfried TN, Shelton LM. Cancer as a metabolic disease. Nutr Metab (Lond). 2010;7:7.
3. Chatterjee A, Mambo E, Sidransky D. Mitochondrial DNA mutations in human cancer. Oncogene. 2006;25(34):4663-74.
4. Carew JS, Huang P. Mitochondrial defects in cancer. Mol Cancer. 2002;1:9.
5. Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: The metabolic requirements of cell proliferation. Science. 2009;324:1029-33.
6. Zu XL, Guppy M. Cancer metabolism: facts, fantasy, and fiction. Biochem Biophys Res Commun. 2004;313:459-65.
7. Moreno-Sáncheza R, Rodríguez-Enríquez S, Marín-Hernándeza A, Saavedra E. Energy metabolism in tumor cells. FEBS J. 2007;274:1393-418.
8. Moreno-Sáncheza R, Marín-Hernándeza A, Saavedra E, Pardob JP, Ralphc SJ, Rodríguez-Enríquez S. Who controls the ATP supply in cancer cells? Biochemistry lessons to understand cancer energy metabolism. Int J Biochem Cell Biol. 2014;50:10-23.
9. Wallace DC. Mitochondria and cancer. Nat Rev Cancer. 2012;12:685-98.
10. Ryan MT, Hoogenraad NJ. Mitochondrial-Nuclear Communications. Annu Rev Biochem. 2007;76:701-22.
11. Smits P, Smeitink J, van den Heuvel L. Mitochondrial translation and beyond: processes implicated in combined oxidative phosphorylation deficiencies. J Biomed Biotechnol. 2010;2010:737385.
12. Kim SJ, Kwon MC, Ryu MJ, Chung HK, Tadi S, Kim YK, et al. CRIF1 is essential for the synthesis and insertion of oxidative phosphorylation polypeptides in the mammalian mitochondrial membrane. Cell Metab. 2012;16(2):274-83.
13. van Gisbergen MW, Voets AM, Starmans MHW, de Cood IFM, Yadak R, Hoffmann RF, et al. How do changes in the mtDNA and mitochondrial dysfunction influence cancer and cancer therapy? Challenges, opportunities and models. Mutation ResRev Mutation Res. 2015;764:16-30.
14. Nargund AM, Fiorese CJ, Pellegrino MW, Deng P, Haynes CM. Mitochondrial and nuclear accumulation of the transcription factor ATFS-1 promotes OXPHOS recovery during the UPRmt. Mol Cell. 2015;58:123-33.
15. Taanman J-W. The mitochondrial genome: structure, transcription, translation and replication. Biochim Biophys Acta. 1999;1410:103-23.
16. Pagliarini DJ, Dixon JE. Mitochondrial modulation: reversible phosphorylation takes center stage? Trend Biochem Sci. 2006;31(1):26-34.
17. Krause DS, Van Etten RA. Tyrosine kinases as targets for cancer therapy. N Engl J Med. 2005;353(2):172-87.
18. Demory ML, Boerner JL, Davidson R, Faust W, Miyake T, Lee I, et al. Epidermal growth factor receptor translocation to the mitochondria: regulation and effect. J Biol Chem. 2009;284(52):36592-604.
19. Hitosugi T, Fan J, Chung TW, Lythgoe K, Wang X, Xie J, et al. Tyrosine phosphorylation of mitochondrial pyruvate dehydrogenase kinase 1 is important for cancer metabolism. Mol Cell. 2011;44(6):864-77.
20. Ding Y, Liu Z, Desai S, Zhao Y, Liu H, Pannell LK, et al. Receptor tyrosine kinase ErbB2 translocates into mitochondria and regulates cellular metabolism. Nat Commun. 2012;3:1271.
21. Tibaldi E, Brunati AM, Massimino ML, Stringaro A, Colone M, Agostinelli E, et al. Src-Tyrosine kinases are major agents in mitochondrial tyrosine phosphorylation. J Cell Biochem. 2008;104(3):840-9.
22. Arachiche A, Augereau O, Decossas M, Pertuiset C, Gontier E, Letellier T, et al. Localization of PTP-1B, SHP-2, and Src exclusively in rat brain mitochondria and functional consequences. J Biol Chem. 2008;283(36):24406-11.
23. Ogura M, Yamaki J, Homma MK, Homma Y. Mitochondrial c-Src regulates cell survival through phosphorylation of respiratory chain components. Biochem J. 2012;447(2):281-9.
24. Hebert-Chatelain E. Src kinases are important regulators of mitochondrial functions. Int J Biochem Cell Biol. 2013;45:90-8.
25. Van Laethem F, Tikhonova AN, Pobezinsky LA, Tai X, Kimura MY, Le Saout C, et al. Lck availability during thymic selection determines the recognition specificity of the T cell repertoire. Cell. 2013;154(6):1326-41.
26. Palacios EH, Weiss A. Function of the Src-family kinases, Lck and Fyn, in T-cell development and activation. Oncogene. 2004;23(48):7990-8000.
27. Yasuda K, Kosugi A, Hayashi F, Saitoh S, Nagafuku M, Mori Y, et al. Serine 6 of Lck tyrosine kinase: a critical site for Lck myristoylation, membrane localization, and function in T lymphocytes. J Immunol. 2000;165(6):3226-31.
28. Chueh F-Y, Yu C-L. Engagement of T-cell antigen receptor and CD4/CD8 co-receptors induces prolonged STAT activation through autocrine/paracrine stimulation in human primary T cells. Biochem Biophys Res Commun. 2012;426(2):242-6.
29. Burnett RC, David JC, Harden AM, Le Beau MM, Rowley JD, Diaz MO. The LCK gene is involved in the t(1;7)(p34;q34) in the T-cell acute lymphoblastic leukemia derived cell line, HSB-2. Gene Chromosome Cancer. 1991;3(6):461-7.
30. Majolini MB, Boncristiano M, Baldari CT. Dysregulation of the protein tyrosine kinase LCK in lymphoproliferative disorders and in other neoplasias. Leuk Lymphoma. 1999;35(3-4):245-54.
31. Kim RK, Yoon CH, Hyun KH, Lee H, An S, Park MJ, et al. Role of lymphocyte-specific protein tyrosine kinase (LCK) in the expansion of glioma-initiating cells by fractionated radiation. Biochem Biophys Res Commun. 2010;402(4):631-6.
32. Elsberger B, Fullerton R, Zino S, Jordan F, Mitchell TJ, Brunton VG, et al. Breast cancer patients' clinical outcome measures are associated with Src kinase family member expression. Br J Cancer. 2010;103(6):899-909.
33. Veillette A, Foss FM, Sausville EA, Bolen JB, Rosen N. Expression of the lck tyrosine kinase gene in human colon carcinoma and other non-lymphoid human tumor cell lines. Oncogene Res. 1987;1(4):357-74.
34. Robinson D, He F, Pretlow T, Kung HJ. A tyrosine kinase profile of prostate carcinoma. Proc Natl Acad Sci U S A. 1996;93(12):5958-62.
35. Chakraborty G, Rangaswami H, Jain S, Kundu GC. Hypoxia regulates cross-talk between Syk and Lck leading to breast cancer progression and angiogenesis. J Biol Chem. 2006;281(16):11322-31.
36. Yu C-L, Jove R, Burakoff SJ. Constitutive activation of the Janus kinase-STAT pathway in T lymphoma overexpressing the Lck protein tyrosine kinase. J Immunol. 1997;159(11):5206-10.
37. Shi M, Cooper JC, Yu C-L. A constitutively active Lck kinase promotes cell proliferation and resistance to apoptosis through signal transducer and activator of transcription 5b activation. Mol Cancer Res. 2006;4(1):39-45.
38. Venkitachalam S, Chueh F-Y, Yu C-L. Nuclear localization of lymphocyte-specific protein tyrosine kinase (Lck) and its role in regulating LIM domain only 2 (Lmo2) gene. Biochem Biophys Res Commun. 2012;417(3):1058-62.
39. Chueh F-Y, Leong K-F, Yu C-L. Mitochondrial translocation of signal transducer and activator of transcription 5 (STAT5) in leukemic T cells and cytokine-stimulated cells. Biochem Biophys Res Commun. 2010;402(4):778-83.
40. Chueh F-Y, Leong K-F, Cronk RJ, Venkitachalam S, Pabich S, Yu C-L. Nuclear localization of pyruvate dehydrogenase complex-E2 (PDC-E2), a mitochondrial enzyme, and its role in signal transducer and activator of transcription 5 (STAT5)-dependent gene transcription. Cell Signal. 2011;23(7):1170-8.
41. Sgobbo P, Pacelli C, Grattagliano I, Villani G, Cocco T. Carvedilol inhibits mitochondrial complex I and induces resistance to H2O2-mediated oxidative insult in H9C2 myocardial cells. Biochim Biophys Acta. 2007;1767:222-32.
42. Chueh F-Y, Cronk RJ, Alsuwaidan AN, Mallers TM, Jaiswal MK, Beaman KD, et al. Mouse LSTRA leukemia as a model of human natural killer T cell and highly aggressive lymphoid malignancies. Leuk Lymphoma. 2014;55(3):706-8.
43. Abraham RT, Weiss A. Jurkat T cells and development of the T-cell receptor signalling paradigm. Nat Rev Immunol. 2004;4:301-8.
44. Perry SW, Norman JP, Barbieri J, Brown EB, Gelbard HA. Mitochondrial membrane potential probes and the proton gradient: a practical usage guide. Biotechniques. 2011;50(2):98-115.
45. Brand MD, Nicholls DG. Assessing mitochondrial dysfunction in cells. Biochem J. 2011;435:297-312.
46. Turrens JF. Mitochondrial formation of reactive oxygen species. J Physiol. 2003;552(Pt 2):335-44.
47. Ran Q, Hao P, Xiao Y, Xiang L, Ye X, Deng X, et al. CRIF1 interacting with CDK2 regulates bone marrow microenvironment-induced G0/G1 arrest of leukemia cells. PLoS One. 2014;9(2):e85328.
48. Kang HJ, Hong YB, Kim HJ, Bae I. CR6-interacting factor 1 (CRIF1) regulates NF-E2-related factor 2 (NRF2) protein stability by proteasome-mediated degradation. J Biol Chem. 2010;285(28):21258-68.
49. Park KC, Song KH, Chung HK, Kim H, Kim DW, Song JH, et al. CR6-interacting factor 1 interacts with orphan nuclear receptor Nur77 and inhibits its transactivation. Mol Endocrinol. 2005;19(1):12-24.
50. Shin J, Lee SH, Kwon MC, Yang DK, Seo HR, Kim J, et al. Cardiomyocyte specific deletion of Crif1 causes mitochondrial cardiomyopathy in mice. PLoS One. 2013;8(1):e53577.
51. Ryu MJ, Kim SJ, Kim YK, Choi MJ, Tadi S, Lee MH, et al. Crif1 deficiency reduces adipose OXPHOS capacity and triggers inflammation and insulin resistance in mice. PLoS Genet. 2013;9(3):e1003356.
52. Feng J, Lucchinetti E, Enkavi G, Wang Y, Gehrig P, Roschitzki B, et al. Tyrosine phosphorylation by Src within the cavity of the adenine nucleotide translocase 1 regulates ADP/ATP exchange in mitochondria. Am J Physiol Cell Physiol. 2010;298(3):C740-8.
53. Yogev O, Pines O. Dual targeting of mitochondrial proteins: Mechanism, regulation and function. Biochim Biophys Acta. 2011;1808:1012-20.
54. Mandujano-Tinoco EA, Gallardo-Perez JC, Marín-Hernándeza A, Moreno-Sáncheza R, Rodríguez-Enríquez S. Anti-mitochondrial therapy in human breast cancer multi-cellular spheroids. Biochim Biophys Acta. 2013;1833(3):541-51.