Receptor tyrosine kinase ErbB2 translocates into mitochondria and regulates cellular metabolism

Nature Communications

Volumn 3, Issue , 2012, Pages

  Ding, Yan ^a,e   Liu, Zixing ^a   Desai, Shruti ^a   Zhao, Yuhua ^a   Liu, Hao ^a   Pannell, Lewis K ^a   Yi, Hong ^b   Wright, Elizabeth R ^b   Owen, Laurie B ^a   Dean Colomb, Windy ^a   Fodstad, Oystein ^c   Lu, Jianrong ^d   Ledoux, Susan P ^a   Wilson, Glenn L ^a   Tan, Ming ^a  

^a UNIVERSITY OF SOUTH ALABAMA   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c OSLO UNIVERSITY HOSPITAL   (Norway)

^d UNIVERSITY OF FLORIDA   (United States)

^e CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; EPIDERMAL GROWTH FACTOR RECEPTOR 2; HEAT SHOCK PROTEIN 70; TRASTUZUMAB;

ANTIBODY; BIOTECHNOLOGY; CANCER; DISEASE RESISTANCE; ELECTRON; ENZYME ACTIVITY; MEMBRANE; MITOCHONDRION; OXYGEN; PLASMA; RESPIRATION; SAMPLING; TRANSPORT PROCESS;

ARTICLE; CANCER CELL; CANCER RESISTANCE; CELL HYPOXIA; CELL LEVEL; CELL METABOLISM; CONTROLLED STUDY; GLYCOLYSIS; HUMAN; HUMAN CELL; MITOCHONDRIAL ENERGY TRANSFER; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; MITOCHONDRIAL TARGETING SIGNAL; MITOCHONDRION; OXYGEN CONSUMPTION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION;

ANTIBODIES, MONOCLONAL, HUMANIZED; ANTINEOPLASTIC AGENTS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL RESPIRATION; DRUG RESISTANCE, NEOPLASM; ELECTRON TRANSPORT; FEMALE; GLYCOLYSIS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; MITOCHONDRIA; OXIDATIVE PHOSPHORYLATION; PROTEIN TRANSPORT; RECEPTOR, ERBB-2;

EID: 84871905514     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms2236     Document Type: Article

References (39)

1. Warburg, O. On respiratory impairment in cancer cells. Science 124, 269-270 (1956).
2. Kim, J. W. & Dang, C. V. Cancer's molecular sweet tooth and the Warburg effect. Cancer Res. 66, 8927-8930 (2006).
3. Chen, Z., Lu, W. Q., Garcia-Prieto, C. & Huang, P. The Warburg effect and its cancer therapeutic implications. J. Bioenerg. Biomembr. 39, 267-274 (2007).
4. Gatenby, R. A. & Gillies, R. J. Glycolysis in cancer: a potential target for therapy. Int. J. Biochem. Cell Biol. 39, 1358-1366 (2007).
5. DeBerardinis, R. J., Lum, J. J., Hatzivassiliou, G. & Thompson, C. B. The biology of cancer: metabolic reprogramming fuels cell growth and proliferation. Cell Metab. 7, 11-20 (2008).
6. Gillies, R. J., Robey, I. & Gatenby, R. A. Causes and consequences of increased glucose metabolism of cancers. J. Nucl. Med. 49(Suppl 2): 24S-42S (2008).
7. Hsu, P. P. & Sabatini, D. M. Cancer cell metabolism: Warburg and beyond. Cell 134, 703-707 (2008).
8. Kroemer, G. & Pouyssegur, J. Tumor cell metabolism: cancer's Achilles' heel. Cancer Cell 13, 472-482 (2008).
9. Vander Heiden, M. G., Cantley, L. C. & Thompson, C. B. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324, 1029-1033 (2009).
10. Galluzzi, L., Larochette, N., Zamzami, N. & Kroemer, G. Mitochondria as therapeutic targets for cancer chemotherapy. Oncogene 25, 4812-4830 (2006).
11. Vaughn, A. E. & Deshmukh, M. Glucose metabolism inhibits apoptosis in neurons and cancer cells by redox inactivation of cytochrome c. Nat. Cell Biol. 10, 1477-1483 (2008).
12. Zhou, M. et al. Warburg effect in chemosensitivity: targeting lactate dehydrogenase-A re-sensitizes Taxol-resistant cancer cells to Taxol. Mol. Cancer 9, 9-33 (2010).
13. Zhao, Y. et al. Overcoming trastuzumab resistance in breast cancer by targeting dysregulated glucose metabolism. Cancer Res. 1, 4585-4597 (2011).
14. Slamon, D. J. et al. Studies of the HER-2/neu proto-oncogene in human breast and ovarian cancer. Science 244, 707-712 (1989).
15. Guy, C. T. et al. Expression of the neu protooncogene in the mammary epithelium of transgenic mice induces metastatic disease. Proc. Natl Acad. Sci. USA 89, 10578-10582 (1992).
16. Tan, M., Yao, J. & Yu, D. Overexpression of the c-erbB-2 gene enhanced intrinsic metastasis potential in human breast cancer cells without increasing their transformation abilities. Cancer Res. 57, 1199-1205 (1997).
17. Tan, M. et al. ErbB2 promotes Src synthesis and stability: novel mechanisms of Src activation that confer breast cancer metastasis. Cancer Res. 65, 1858-1867 (2005).
18. Tan, M. et al. Selective inhibition of ErbB2-overexpressing breast cancer in vivo by a novel TAT-based ErbB2-targeting signal transducers and activators of transcription 3-blocking peptide. Cancer Res. 66, 3764-3772 (2006a).
19. Tan, M. et al. Upregulation and activation of PKC alpha by ErbB2 through Src promotes breast cancer cell invasion that can be blocked by combined treatment with PKC alpha and Src inhibitors. Oncogene 25, 3286-3295 (2006b).
20. Yarden, Y. & Sliwkowski, M. X. Untangling the ErbB signalling network. Nat. Rev. Mol. Cell Biol. 2, 127-137 (2001).
21. Zhou, X. et al. Activation of the Akt/mammalian target of rapamycin/4E-BP1 pathway by ErbB2 overexpression predicts tumor progression in breast cancers. Clin. Cancer Res. 10, 6779-6788 (2004).
22. Zhang, H. et al. ErbB receptors: from oncogenes to targeted cancer therapies. J. Clin. Invest. 117, 2051-2058 (2007).
23. Zhao, Y. H. et al. Upregulation of lactate dehydrogenase A by ErbB2 through heat shock factor 1 promotes breast cancer cell glycolysis and growth. Oncogene 28, 3689-3701 (2009).
24. Wang, S. C. & Hung, M. C. Nuclear translocation of the epidermal growth factor receptor family membrane tyrosine kinase receptors. Clin. Cancer Res. 15, 6484-6489 (2009).
25. Sun, Y. et al. Induction or suppression of expression of cytochrome c oxidase subunit II by heregulin beta 1 in human mammary epithelial cells is dependent on the levels of ErbB2 expression. J. Cell Physiol. 192, 225-233 (2002).
26. Grazette, L. P. et al. Inhibition of ErbB2 causes mitochondrial dysfunction in cardiomyocytes: implications for herceptin-induced cardiomyopathy. J. Am. Coll Cardiol. 44, 2231-2238 (2004).
27. Lasfer, M. et al. Protein kinase PKC delta and c-Abl are required for mitochondrial apoptosis induction by genotoxic stress in the absence of p53, p73 and Fas receptor. FEBS Lett. 580, 2547-2552 (2006).
28. Tibaldi, E. et al. Src-Tyrosine kinases are major agents in mitochondrial tyrosine phosphorylation. J. Cell Biochem. 104, 840-849 (2008).
29. Baines, C. P. et al. Mitochondrial PKCepsilon and MAPK form signaling modules in the murine heart: enhanced mitochondrial PKCepsilon-MAPK interactions and differential MAPK activation in PKCepsilon-induced cardioprotection. Circ. Res. 90, 390-397 (2002).
30. Arachiche, A. et al. Localization of PTP-1B, SHP-2, and Src exclusively in rat brain mitochondria and functional consequences. J. Biol. Chem. 283, 24406-24411 (2008).
31. Miedlich, S. U., Zalutskaya, A., Zhu, E. D. & Demay, M. B. Phosphate-induced apoptosis of hypertrophic chondrocytes is associated with a decrease in mitochondrial membrane potential and is dependent upon ERK1/2 phosphorylation. J. Biol. Chem. 24, 18270-18275 (2010).
32. Neupert, W. & Herrmann, J. M. Translocation of proteins into mitochondria. Annu. Rev. Biochem. 76, 723-749 (2007).
33. Chacinska, A. et al. Importing mitochondrial proteins: machineries and mechanism. Cell 138, 628-644 (2009).
34. Fantin, V. R., St-Pierre, J. & Leder, P. Attenuation of LDH-A expression uncovers a link between glycolysis, mitochondrial physiology, and tumor maintenance. Cancer Cell 9, 425-434 (2006).
35. Austin, C. D. et al. Endocytosis and sorting of ErbB2 and the site of action of cancer therapeutics trastuzumab and geldanamycin. Mol. Biol. Cell 15, 5268-5282 (2004).
36. Tan, M. et al. Phosphorylation on tyrosine-15 of p34 (Cdc2) by ErbB2 inhibits p34(Cdc2) activation and is involved in resistance to taxol-induced apoptosis. Mol. Cell 9, 993-1004 (2002).
37. Miyazaki, T. et al. Regulation of cytochrome c oxidase activity by c-Src in osteoclasts. J. Cell Biol. 160, 709-718 (2003).
38. Lemmon, M. A. & Schlessinger, J. Cell signaling by receptor tyrosine kinases. Cell 141, 1117-1134 (2010).
39. Weihua, Z. et al. Survival of cancer cells is maintained by EGFR independent of its kinase activity. Cancer Cell 13, 385-393 (2008).