TRAP1 and the proteasome regulatory particle TBP7/Rpt3 interact in the endoplasmic reticulum and control cellular ubiquitination of specific mitochondrial proteins

Cell Death and Differentiation

Volumn 19, Issue 4, 2012, Pages 592-602

  Amoroso, M R ^a   Matassa, D S ^a   Laudiero, G ^a   Egorova, A V ^b   Polishchuk, R S ^b   Maddalena, F ^c   Piscazzi, A ^d   Paladino, S ^a,e   Sarnataro, D ^a,e   Garbi, C ^a   Landriscina, M ^d   Esposito, F ^a  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b TELETHON INSTITUTE OF GENETICS AND MEDICINE TIGEM   (Italy)

^c REFERRAL CANCER CENTER OF BASILICATA   (Italy)

^d UNIVERSITY OF FOGGIA   (Italy)

^e CEINGE BIOTECNOLOGIE AVANZATE   (Italy)

Author keywords

apoptosis; mitochondria ER crosstalk; protein quality control; TBP7; TRAP1; ubiquitination

Indexed keywords

MESSENGER RNA; MITOCHONDRIAL PROTEIN; PROTEASOME; PROTEIN TBP7; SHORT HAIRPIN RNA; THAPSIGARGIN; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED PROTEIN 1; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL DEATH; CHEMICAL ANALYSIS; CONFOCAL MICROSCOPY; CORRELATION ANALYSIS; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; FLUORESCENCE RESONANCE ENERGY TRANSFER; HUMAN; HUMAN CELL; MASS SPECTROMETRY; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; QUALITY CONTROL; UBIQUITINATION; UPREGULATION;

CELL LINE, TUMOR; COLORECTAL NEOPLASMS; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; GENE SILENCING; HSP90 HEAT-SHOCK PROTEINS; HUMANS; MITOCHONDRIAL PROTEINS; NEOPLASM PROTEINS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN FOLDING; UBIQUITINATION;

EID: 84858156763     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2011.128     Document Type: Article

References (37)

1. Song HY, Dunbar JD, Zhang YX, Guo D, Donner DB. Identification of a protein with homology to HSP90 that binds the type 1 tumor necrosis factor receptor. J Biol Chem 1995; 270: 3574-3581.
2. Felts SJ, Owen BA, Nguyen P, Trepel J, Donner DB, Toft DO. The HSP90-related protein TRAP1 is a mitochondrial protein with distinct functional properties. J Biol Chem 2000; 275: 3305-3312. (Pubitemid 30083032)
3. Montesano Gesualdi N, Chirico G, Catanese MT, Pirozzi G, Esposito F. AROS-29 is involved in adaptive response to oxidative stress. Free Radic Res 2006; 40: 467-476.
4. Montesano Gesualdi N, Chirico G, Pirozzi G, Costantino E, Landriscina M, Esposito F. Tumor necrosis factor-associated protein 1 (TRAP-1) protects cells from oxidative stress and apoptosis. Stress 2007; 10: 342-350. (Pubitemid 350125789)
5. Costantino E, Maddalena F, Calise S, Piscazzi A, Tirino V, Fersini A et al. TRAP1, a novel mitochondrial chaperone responsible for multi-drug resistance and protection from apoptosis in human colorectal carcinoma cells. Cancer Lett 2009; 279: 39-46.
6. Kang BH, Plescia J, Dohi T, Rosa J, Doxsey SJ, Altieri DC. Regulation of tumor cell mitochondrial homeostasis by an organelle-specific HSP90 chaperone network. Cell 2007; 131: 257-270. (Pubitemid 47576138)
7. Leav I, Plescia J, Goel HL, Li J, Jiang Z, Cohen RJ et al. Cytoprotective mitochondrial chaperone TRAP-1 as a novel molecular target in localized and metastatic prostate cancer. Am J Pathol 2010; 176: 393-401.
8. Kang BH, Siegelin MD, Plescia J, Raskett CM, Garlick DS, Dohi T et al. Preclinical characterization of mitochondria-targeted small molecule HSP90 inhibitors, gamitrinibs, in advanced prostate cancer. Clin Cancer Res 2010; 16: 4779-4788.
9. Kang BH, Tavecchio M, Goel HL, Hsieh CC, Garlick DS, Raskett CM et al. Targeted inhibition of mitochondrial HSP90 suppresses localised and metastatic prostate cancer growth in a genetic mouse model of disease. Br J Cancer 2011; 104: 629-634.
10. Siegelin MD, Dohi T, Raskett CM, Orlowski GM, Powers CM, Gilbert CA et al. Exploiting the mitochondrial unfolded protein response for cancer therapy in mice and human cells. J Clin Invest 2011; 121: 1349-1360.
11. Takemoto K, Miyata S, Takamura H, Katayama T, Tohyama M. Mitochondrial TRAP1 regulates the unfolded protein response in the endoplasmic reticulum. Neurochem Int 2011; 58: 880-887.
12. Landriscina M, Laudiero G, Maddalena F, Amoroso MR, Piscazzi A, Cozzolino F et al. Mitochondrial chaperone TRAP1 and the calcium binding protein Sorcin interact and protect cells against apoptosis induced by antiblastic agents. Cancer Res 2010; 70: 6577-6586.
13. Marx FP, Soehn AS, Berg D, Melle C, Schiesling C, Lang M et al. The proteasomal subunit S6 ATPase is a novel synphilin-1 interacting protein-implications for Parkinson's disease. FASEB J 2007; 21: 1759-1767. (Pubitemid 46855622)
14. Kaneko T, Hamazaki J, Iemura S, Sasaki K, Furuyama K, Natsume T et al. Assembly pathway of the mammalian proteasome base subcomplex is mediated by multiple specific chaperones. Cell 2009; 137: 914-925.
15. Landriscina M, Amoroso MR, Piscazzi A, Esposito F. Heat shock proteins, cell survival and drug resistance: the mitochondrial chaperone TRAP1, a potential novel target for ovarian cancer therapy. Gynecol Oncol 2010; 117: 177-182.
16. Landriscina M, Maddalena F, Laudiero G, Esposito F. Adaptation to oxidative stress, chemoresistance, and cell survival. Antioxid Redox Signal 2009; 11: 2701-2716.
17. Truax AD, Koues OI, Mentel MK, Greer SF. The 19S ATPase S6a (S60/TBP1) regulates the transcription initiation of class II transactivator. J Mol Biol 2010; 395: 254-269.
18. Tsai YC, Weissman AM. The unfolded protein response, degradation from endoplasmic reticulum and cancer. Genes Cancer 2010; 1: 764-778.
19. Ohana B, Moore PA, Ruben SM, Southgate CD, Green MR, Rosen CA. The type 1 human immunodeficiency virus Tat binding protein is a transcriptional activator belonging to an additional family of evolutionarily conserved genes. Proc Natl Acad Sci USA 1993; 90: 138-142. (Pubitemid 23010265)
20. Kenworthy AK, Edidin M. Imaging fluorescence resonance energy transfer as probe of membrane organization and molecular associations of GPI-anchored proteins. Methods Mol Biol 1999; 116: 37-49.
21. Enyedi B, Várnai P, Geiszt M. Redox state of the endoplasmic reticulum is controlled by Ero1L-alpha and intraluminal calcium. Antioxid Redox Signal 2010; 13: 721-729.
22. Masuda Y, Shima G, Aiuchi T, Horie M, Hori K, Nakajo S et al. Involvement of tumor necrosis factor receptor-associated protein 1 (TRAP1) in apoptosis induced by betahydroxyisovalerylshikonin. J Biol Chem 2004; 279: 42503-42515. (Pubitemid 39372134)
23. Morales AP, Carvalho AC, Monteforte PT, Hirata H, Han SW, Hsu YT et al. Endoplasmic reticulum calcium release engages Bax translocation in cortical astrocytes. Neurochem Res 2011; 36: 829-838.
24. Chen WT, Lee AS. Measurement and modification of the expression level of the chaperone protein and signaling regulator GRP78/BiP in mammalian cells. Methods Enzymol 2011; 490: 217-233.
25. Hayashi T, Su TP. Sigma-1 receptor chaperones at the ER-mitochondrion interface regulate Ca(2+) signaling and cell survival. Cell 2007; 131: 596-610. (Pubitemid 350017760)
26. Azzu V, Brand MD. Degradation of an intramitochondrial protein by the cytosolic proteasome. J Cell Sci 2010; 123 (Part 4): 578-585.
27. Baker BM, Haynes CM. Mitochondrial protein quality control during biogenesis and aging. Trends Biochem Sci 2011; 36: 254-261.
28. Livnat-Levanon N, Glickman MH. Ubiquitin-proteasome system and mitochondria-reciprocity. Biochim Biophys Acta 2011; 1809: 80-87.
29. Germain D. Ubiquitin-dependent and-independent mitochondrial protein quality controls: implications in ageing and neurodegenerative diseases. Mol Microbiol 2008; 70: 1334-1341.
30. Kozieł R, Greussing R, Maier AB, Declercq L, Jansen-Dürr P. Functional interplay between mitochondrial and proteasome activity in skin aging. J Invest Dermatol 2011; 131: 594-603.
31. Neznanov N, Komarov AP, Neznanova L, Stanhope-Baker P, Gudkov A. Proteotoxic stress targeted therapy (PSTT): induction of protein misfolding enhances the antitumor effect of the proteasome inhibitor bortezomib. Oncotarget 2011; 2: 209-221.
32. Ludwig H, Beksac M, BladéJ, Cavenagh J, Cavo M, Delforge M et al. Multiple myeloma treatment strategies with novel agents in 2011: a European perspective. Oncologist 2011; 16: 388-403.
33. Hassink GC, Zhao B, Sompallae R, Altum M, Gastaldello S, Zinin NV et al. The ER-resident ubiquitin-specific protease19 participates in the UPR and rescues ERAD substrates. EMBO Rep 2009; 10: 755-761.
34. Fujiki Y, Hubbard AL, Fowler S, Lazarow PB. Isolation of intracellular membranes by means of sodium carbonate treatment: application to endoplasmic reticulum. J Cell Biol 1982; 93: 97-102. (Pubitemid 12117045)
35. George TC, Basiji DA, Hall BE, Lynch DH, Ortyn WE, Perry DJ et al. Distinguishing modes of cell death using the ImageStream multispectral imaging flow cytometer. Cytometry A 2004; 59: 237-245. (Pubitemid 38736299)
36. Polishchuk EV, Di Pentima A, Luini A, Polishchuk RS. Mechanism of constitutive export from the Golgi: bulk flow via the formation, protrusion, and en bloc cleavage of large trans-Golgi network tubular domains. Mol Biol Cell 2003; 14: 4470-4485. (Pubitemid 37444649)
37. Lieberman AP, Harmison G, Strand AD, Olson JM, Fischbeck KH. Altered transcriptional regulation in cells expressing the expanded polyglutamine androgen receptor. Hum Mol Genet 2002; 11: 1967-1976. (Pubitemid 34924907)