Phosphorylated hamartin-Hsp70 complex regulates apoptosis via mitochondrial localization

Biochemical and Biophysical Research Communications

Volumn 391, Issue 1, 2010, Pages 1148-1153

  Inoue, Hirofumi ^a   Uyama, Takumi ^a   Suzuki, Tsukasa ^a   Kazami, Machiko ^a   Hino, Okio ^b   Kobayashi, Toshiyuki ^b   Kobayashi, Ken Ichi ^a   Tadokoro, Tadahiro ^a   Yamamoto, Yuji ^a  

^a TOKYO UNIVERSITY OF AGRICULTURE   (Japan)

^b JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

Apoptosis; Hamartin; Hsp70; Mitochondria; Phosphorylation

Indexed keywords

HAMARTIN; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 70; KNK 437; MUTANT PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELLULAR DISTRIBUTION; EMBRYO; MITOCHONDRION; MOUSE; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT; REGULATORY MECHANISM;

ANIMALS; APOPTOSIS; CELL LINE, TUMOR; CERCOPITHECUS AETHIOPS; COS CELLS; HSP70 HEAT-SHOCK PROTEINS; MICE; MITOCHONDRIA; MITOCHONDRIAL MEMBRANES; PHOSPHORYLATION; TUMOR SUPPRESSOR PROTEINS;

EID: 72949119106     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2009.12.054     Document Type: Article

References (38)

1. Rosner M., Freilinger A., and Hengstschläger M. Proteins interacting with the tuberous sclerosis gene products. Amino Acids 27 (2004) 119-128
2. Gomez M.R., Sampson J.R., and Wittemore V.H. Tuberous Sclerosis Complex. third ed. (1999), Oxford University Press, USA
3. Consortium E.C.T.S. Identification and characterization of the tuberous sclerosis gene on chromosome 16. Cell 75 (1993) 1305-1315
4. van Slegtenhorst M., Nellist M., Nagelkerken B., Cheadle J., Snell R., van den Ouweland A., Reuser A., Sampson J., Hell D., and van der Sluijs P. Interaction between hamartin and tuberin, the TSC1 and TSC2 gene products. Hum. Mol. Genet. 7 (1998) 1053-1057
5. Inoki K., Li Y., Xu T., and Guan K.L. Rheb GTPase is a direct target of TSC2 GAP activity and regulates mTOR signaling. Genes Dev. 17 (2003) 1829-1834
6. Dan H.C., Sun M., Yang L., Feldman R.I., Sui X.M., Ou C.C., Nellist M., Yeung R.S., Halley D.J., Nicosia S.V., Pledger W.J., and Cheng J.Q. Phosphatidylinositol 3-kinase/AKT pathway regulates tuberous sclerosis tumor suppressor complex by phosphorylation of tuberin. J. Biol. Chem. 277 (2002) 35364-35370
7. Inoki K., Li Y., Zhu T., Wu J., and Guan K. TSC2 is phosphorylated and inhibited by Akt and suppresses mTOR signaling. Nat. Cell. Biol. 4 (2002) 648-657
8. Goncharova E.A., Goncharov D.A., Eszterhas A., Hunter D.S., Glassberg M.K., Yeung R.S., Walker C.L., Noonan D., Kwiatkowski D.J., Chou M.M., Panettieri Jr. R.A., and Krymskaya V.P. Tuberin regulates p70 S6 kinase activation and ribosomal protein S6 phosphorylation. A role for the TSC2 tumor suppressor gene in pulmonary lymphangioleiomyomatosis (LAM). J. Biol. Chem. 277 (2002) 30958-30967
9. Inoki K., Zhu T., and Guan K.L. TSC2 mediates cellular energy response to control cell growth and survival. Cell 115 (2003) 577-590
10. Clements D., Mayer R.J., and Johnson S.R. Subcellular distribution of the TSC2 gene product tuberin in human airway smooth muscle cells is driven by multiple localization sequences and is cell-cycle dependent. Am. J. Physiol. Lung Cell Mol. Physiol. 292 (2006) 258-266
11. Gan B., Melkoumian Z.K., Wu X., Guan K.L., and Guan J.L. Identification of FIP200 interaction with the TSC1-TSC2 complex and its role in regulation of cell size control. J. Cell Biol. 170 (2005) 379-389
12. Suzuki T., Das S.K., Inoue H., Kazami M., Hino O., Kobayashi T., Yeung R.S., Kobayashi K., Tadokoro T., and Yamamoto Y. Tuberous sclerosis complex 2 loss-of-function mutation regulates reactive oxygen species production through Rac1 activation. Biochem. Biophys. Res. Commun. 368 (2008) 132-137
13. Xiao H., Shoarinejad F., Jin F., Golemis E.A., and Yeung R.S. The tuberous sclerosis 2 gene product, tuberin, functions as a Rab5 GTPase activating protein (GAP) in modulating endocytosis. J. Biol. Chem. 272 (1997) 6097-6100
14. Jones K.A., Jiang X., Yamamoto Y., and Yeung R.S. Tuberin is a component of lipid rafts and mediates caveolin-1 localization: role of TSC2 in post-Golgi transport. Exp. Cell Res. 295 (2004) 512-524
15. Rosner M., Freilinger A., Hanneder M., Fujita N., Lubec G., Tsuruo T., and Hengstschläger M. P27Kip1 localization depends on the tumor suppressor protein tuberin. Hum. Mol. Genet. 16 (2007) 1541-1556
16. Henry K.W., Yuan X., Koszewski N.J., Onda H., Kwiatkowski D.J., and Noonan D.J. Tuberous sclerosis gene 2 product modulates transcription mediated by steroid hormone receptor family members. J. Biol. Chem. 273 (1998) 20535-20539
17. Astrinidis A., Senapedis W., and Henske E.P. Hamartin, the tuberous sclerosis complex 1 gene product, interacts with polo-like kinase 1 in a phosphorylation-dependent manner. Hum. Mol. Genet. 15 (2006) 287-297
18. Nakashima A., Yoshino K., Miyamoto T., Eguchi S., Oshiro N., Kikkawa U., and Yonezawa K. Identification of TBC7 having TBC domain as a novel binding protein to TSC1-TSC2 complex. Biochem. Biophys. Res. Commun. 361 (2007) 218-223
19. Chong-Kopera H., Inoki K., Li Y., Zhu T., Garcia-Gonzalo F.R., Rosa J.L., and Guan K.L. TSC1 stabilizes TSC2 by inhibiting the interaction between TSC2 and the HERC1 ubiquitin ligase. J. Biol. Chem. 281 (2006) 8313-8316
20. Inoue H., Ndong M., Suzuki T., Kazami M., Uyama T., Kobayashi K., Tadokoro T., and Yamamoto Y. Hamartin-Hsp70 interaction is necessary for akt-dependent tuberin phosphorylation during heat shock. Biosci. Biothechnol. Biochem. 73 (2009) 2488-2493
21. Barnes J.A., Dix D.J., Collins B.W., Luft C., and Allen J.W. Expression of inducible Hsp70 enhances the proliferation of MCF-7 breast cancer cells and protects against the cytotoxic effects of hyperthermia. Cell Stress Chaperones 6 (2001) 316-325
22. Jäättelä M. Over-expression of Hsp70 confers tumorigenicity to mouse fibrosarcoma cells. Int. J. Cancer 60 (1995) 689-693
23. Kobayashi T., Minowa O., Sugitani Y., Takai S., Mitani H., Kobayashi E., Noda T., and Hino O. A germ-line Tsc1 mutation causes tumor development and embryonic lethality that are similar, but not identical to, those caused by Tsc2 mutation in mice. Proc. Natl. Acad. Sci. USA 98 (2001) 8762-8767
24. Aicher L.D., Campbell J.S., and Yeung R.S. Tuberin phosphorylation regulates its interaction with hamartin. Two proteins involved in tuberous sclerosis. J. Biol. Chem. 276 (2001) 21017-21021
25. Ozcan U., Ozcan L., Yilmaz E., Düvel K., Sahin M., Manning B.D., and Hotamisligil G.S. Loss of the tuberous sclerosis complex tumor suppressors triggers the unfolded protein response to regulate insulin signaling and apoptosis. Mol. Cell. 29 (2007) 541-551
26. Chandra D., Choy G., Deng X., Bhatia B., Daniel P., and Tang D. Association of active caspase 8 with the mitochondrial membrane during apoptosis: potential roles in cleaving BAP31 and caspase 3 and mediating mitochondrion-endoplasmic reticulum cross talk in etoposide-induced cell death. Mol. Cell. Biol. 24 (2004) 6592-6607
27. Lufei C., Ma J., Huang G., Zhang T., Diermayr V.N., Thing Ong C., and Cao X. GRIM-19, a death-regulatory gene product, suppresses Stat3 activity via functional interaction. EMBO J. 22 (2003) 1325-1335
28. Zhang J., Yang J., Roy S.K., Tininini S., Hu J., Bromberg J.F., Poli V., Stark G.R., and Kalvakolanu D.V. The cell death regulator GRIM-19 is an inhibitor of signal transducer and activator of transcription 3. Proc. Natl. Acad. Sci. USA 100 (2003) 9342-9347
29. Yokota S., Kitahara M., and Nagata K. Benzylidene lactam compound, KNK437, a novel inhibitor of acquisition of thermotolerance and heat shock protein induction in human colon carcinoma cells. Cancer Res. 60 (2000) 2942-2948
30. Nylandsted J., Rohde M., Brand K., Bastholm L., Elling F., and Jäättelä M. Selective depletion of heat shock protein 70 (Hsp70) activates a tumor-specific death program that is independent of caspases and bypasses Bcl-2. Proc. Natl. Acad. Sci. USA 97 (2000) 7871-7876
31. Yamamoto Y., Jones K.A., Mak B.C., Muehlenbachs A., and Yeung R.S. Multicompartmental distribution of the tuberous sclerosis gene products, hamartin and tuberin. Arch. Biochem. Biophys. 404 (2002) 210-217
32. Cai S.L., Tee A.R., Short J.D., Bergeron J.M., Kim J., Shen J., Guo R., Johnson C.L., Kiguchi K., and Walker C.L. Activity of TSC2 is inhibited by Akt-mediated phosphorylation and membrane partitioning. J. Cell. Biol. 172 (2006) 279-289
33. Young J.C., Hoogenraad N.J., and Hartl F.U. Molecular chaperones Hsp90 and Hsp70 deliver preproteins to the mitochondrial import receptor Tom70. Cell 112 (2003) 41-50
34. Green D.R., and Kroemer G. The pathophysiology of mitochondrial cell death. Science 305 (2004) 626-629
35. Yasui S., Tsuzaki K., Ninomiya H., Floricel F., Asano Y., Maki H., Takamura A., Nanba E., Higaki K., and Ohno K. The TSC1 gene product hamartin interacts with NADE. Mol. Cell. Neurosci. 35 (2007) 100-108
36. Chen C., Liu Y., Liu R., Ikenoue T., Guan K.L., Liu Y., and Zheng P. TSC-mTOR maintains quiescence and function of hematopoietic stem cells by repressing mitochondrial biogenesis and reactive oxygen species. J. Exp. Med. 205 (2008) 2397-2408
37. Schieke S.M., Phillips D., MoCoy J.P., Aponte A.M., Shen R.F., Balaban R.S., and Finkel T. The mammalian target of rapamycin (mTOR) pathway regulates mitochondrial oxygen consumption and oxidative capacity. J. Biol. Chem. 281 (2006) 27643-27652
38. Chen C., Liu Y., Liu Y., and Zheng P. The axis of mTOR-mitochondria-ROS and stemness of the hematopoietic stem cells. Cell Cycle 8 (2009) 1158-1160