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2014 | 1 | 1 |
Article title

ER stress protection in cancer cells: the
multifaceted role of the heat shock protein TRAP1

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EN
Abstracts
EN
TRAP1 is an HSP90 chaperone, upregulated in
human cancers and involved in organelles’ homeostasis
and tumor cell metabolism. Indeed, TRAP1 is a key
regulator of adaptive responses used by highly proliferative
tumors to face the metabolic stress induced by increased
demand of protein synthesis and hostile environments.
Besides well-characterized roles in prevention of
mitochondrial permeability transition pore opening and
in regulating mitochondrial respiration, TRAP1 is involved
in novel regulatory mechanisms: i) the attenuation
of global protein synthesis, ii) the co-translational
regulation of protein synthesis and ubiquitination of
specific client proteins, and iii) the protection from
Endoplasmic Reticulum stress. This provides a crucial role
to TRAP1 in maintaining cellular homeostasis through
protein quality control, by avoiding the accumulation of
damaged or misfolded proteins and, likely, facilitating
the synthesis of selective cancer-related proteins. Herein,
we summarize how these regulatory mechanisms are
part of an integrated network, which enables cancer cells
to modulate their metabolism and to face, at the same
time, oxidative and metabolic stress, oxygen and nutrient
deprivation, increased demand of energy production and
macromolecule biosynthesis. The possibility to undertake
a new strategy to disrupt such networks of integrated
control in cancer cells holds great promise for treatment
of human malignancies.
Publisher
Year
Volume
1
Issue
1
Physical description
Dates
published
1 - 1 - 2014
received
16 - 9 - 2014
online
17 - 12 - 2014
accepted
3 - 11 - 2014
References
  • ---
  • [1] Amoroso M.R., Matassa D.S., Sisinni L., Lettini G., Landriscina M., Esposito F., TRAP1 revisited: novel localizations and functions of a ‘next-generation’ biomarker (review), Int J Oncol., 2014, 45(3), 969-977.
  • [2] Altieri D.C., Stein G.S., Lian J.B., Languino L.R.,TRAP-1, the mitochondrial Hsp90, Biochim Biophys Acta., 2012, 1823(3),767-773.
  • [3] Yoshida S., Tsutsumi S., Muhlebach G., Sourbier C., Lee M.J., Lee S., et al., Molecular chaperone TRAP1 regulates a metabolic switch between mitochondrial respiration and aerobic glycolysis, Proc Natl Acad Sci U S A., 2013, 110(17), 1604-1612.[Crossref]
  • [4] Amoroso M.R., Matassa D.S., Laudiero G., Egorova A.V., Polishchuk R.S., Maddalena F., et al., TRAP1 and the proteasome regulatory particle TBP7/Rpt3 interact in the endoplasmic reticulum and control cellular ubiquitination of specific mitochondrial proteins, Cell Death Differ., 2012, 19(4), 592-604.
  • [5] Chen W.T., Lee A.S., 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.
  • [6] Kirkin V., Dikic I., Ubiquitin networks in cancer, Curr Opin Genet Dev., 2011, 21, 21-28.[Crossref]
  • [7] Maddalena F., Sisinni L., Lettini G., Condelli V., Matassa D.S., Piscazzi A., et al., Resistance to paclitxel in breast carcinoma cells requires a quality control of mitochondrial antiapoptotic proteins by TRAP1, Mol Oncol., 2013, 7(5), 895-906.
  • [8] Liao P.C., Tan S.K., Lieu C.H., Jung H.K., Involvement of endoplasmic reticulum in paclitaxel-induced apoptosis, J Cell Biochem., 2008, 104, 1509-1523.[Crossref]
  • [9] Wang J., Yin Y., Hua H., Li M., Luo T., X, L., et al., Blockade of GRP78 sensitizes breast cancer cells to microtubules-interfering agents that induce the unfolded protein response. J Cell Mol Med., 2009, 13, 3888-3897.[Crossref]
  • [10] Mhaidat N.M., Alali F.Q., Matalqah S.M., Matalka I.I., Jaradat S.A., Al-Sawalha N.A., et al., Inhibition of MEK sensitizes paclitaxel-induced apoptosis of human colorectal cancer cells by downregulation of GRP78, Anticancer Drug., 2009, 20, 601-606.[Crossref]
  • [11] Sisinni L., Maddalena F., Lettini G., Condelli V., Matassa D.S., Esposito F., et al., TRAP1 role in endoplasmic reticulum stress protection favors resistance to anthracyclins in breast carcinoma cells, Int J Oncol., 2014, 44(2), 573-582.
  • [12] Ron D., Translational control in the endoplasmic reticulum stress response, J Clin Invest., 2002, 110(10), 1383-1388.[Crossref]
  • [13] Matassa D.S., Amoroso M.R., Agliarulo I., Maddalena F., Sisinni L., Paladino S., et al., Translational control in the stress adaptive response of cancer cells: a novel role for the heat shock protein TRAP1, Cell Death Dis., 2013, 4, 851-860.
  • [14] Ye J., Kumanova M., Hart L.S., Sloane K., Zhang H., De Panis D.N. et al. The GCN2-ATF4 pathway is critical for tumour cell survival and proliferation in response to nutrient deprivation, EMBO J., 2010, 29, 2082–2096.[Crossref]
  • [15] Lewerenz J., Maher P., Basal levels of eIF2alpha phosphorylation determine cellular antioxidant status by regulating ATF4 and xCT expression, J Biol Chem., 2009, 284, 1106–1115.
  • [16] Meyers M.B., Pickel V.M., Sheu S.S., Sharma V.K., Scotto K.W., Fishman G.I., Association of Sorcin with the cardiac ryanodine receptor, J Biol Chem., 1995, 270, 26411-26418.
  • [17] Farrell E.F., Antaramian A., Rueda A., Gómez A.M., Valdivia H.H., Sorcin inhibits calcium release and modulates excitation-contraction coupling in the heart, J Biol Chem, 2003, 278, 34660-34666.
  • [18] Meyers M.B., Fischer A., Sun Y.J., Lopes C.M., Rohacs T., Nakamura T.Y., et al., Sorcin regulates excitation-contraction coupling in the heart, J Biol Chem., 2003, 278, 28865-28871.
  • [19] Landriscina M., Laudiero G., Maddalena F., Amoroso M.R., 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.[Crossref]
  • [20] Maddalena F., Laudiero G., Piscazzi A., Secondo A., Scorziello A., Lombardi V., et al., Sorcin induces a drug-resistant phenotype in human colorectal cancer by modulating Ca(2+) homeostasis, Cancer Res., 2011, 71(24), 7659-7669.[Crossref]
  • [21] Mattson M.P., Neuronal life-and-death signaling, apoptosis, and neurodegenerative disorders, Antioxid Redox Signal., 2006, 8, 1997-2006.
  • [22] Siegelin M.D., Dohi T., Raskett C.M., Orlowski G.M., Powers C.M., Gilbert C.A., et al., Exploiting the mitochondrial unfolded protein response for cancer therapy in mice and human cells, J Clin Invest., 2011, 121, 1349-1360.[Crossref]
  • [23] 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.[Crossref]
  • [24] Bi M., Naczki C., Koritzinsky M., Fels D., Blais J., Hu N., et al., ER stress-regulated translation increases tolerance to extreme hypoxia and promotes tumor growth, EMBO J., 2005, 24, 3470–3481.[Crossref][PubMed]
  • [25] Matassa D.S., Agliarulo I., Amoroso M.R., Maddalena F., Sepe L., Ferrari M.C., et al. TRAP1-dependent regulation of p70S6K is involved in the attenuation of protein synthesis and cell migration: Relevance in human colorectal tumors, Mol Oncol., (in press) DOI: 10.1016/j.molonc.2014.06.003.[Crossref]
  • [26] Hart L.S., Cunningham J.T., Datta T., Dey S., Tameire F., Lehman S.L., et al., ER stress–mediated autophagy promotes Myc-dependent transformation and tumor growth, JCI, 2012, 122(12), 4621-4634.[Crossref]
  • [27] Han J., Back S.H., Hur J., Lin Y.H., Gildersleeve R., Shan J., et al., ER-stress-induced transcriptional regulation increases protein synthesis leading to cell death, Nat Cell Biol., 2013, 15(5), 481-490.[Crossref]
  • [28] Frydman J., Folding of newly translated proteins in vivo: the role of molecular chaperones, Annu. Rev. Biochem., 2001, 70, 603–647.[Crossref]
  • [29] Pechmann S., Willmund F., Frydman J., The ribosome as a hub for protein quality control, Mol. Cell., 2013, 49, 411–421.[Crossref]
  • [30] Albanèse V., Yam A.Y., Baughman J., Parnot C., Frydman J., Systems analyses reveal two chaperone networks with distinct functions in eukaryotic cells, Cell 2006, 124, 75–88.[Crossref]
  • [31] Duttler S., Pechmann S., Frydman J., Principles of cotranslational ubiquitination and quality control at the ribosome, Mol. Cell, 2013, 50, 379–393.[Crossref]
  • [32] Wang F,, Durfee L.A., Huibregtse J.M., () A cotranslational ubiquitination pathway for quality control of misfolded proteins, Mol. Cell, 2013, 50, 368–378.[Crossref]
  • [33] Medicherla B. and Goldberg A.L., Heat shock and oxygen radicals stimulate ubiquitin-dependent degradation mainly of newly synthesized proteins, J. Cell Biol., 2008, 182, 663–673
  • [34] Sonenberg N. and Hinnebusch A.G., Regulation of translation initiation in eukaryotes: mechanisms and biological targets, Cell, 2009, 136, 731–745
  • [35] Holcik M. and Sonenberg N. Translational control in stress and apoptosis, Nat. Rev. Mol. Cell Biol. 2005, 6, 318–327.[Crossref]
  • [36] Liu B., Han Y., Qian S.B. Cotranslational response to proteotoxic stress by elongation pausing of ribosomes. Mol. Cell, 2013, 49, 453–463[Crossref]
  • [37] Shalgi R., Hurt J.A., Krykbaeva I., Taipale M., Lindquist S., Burge C.B., Widespread regulation of translation by elongation pausing in heat shock, Mol. Cell, 2013, 49, 439–452[Crossref]
  • [38] Visweswaraiah J., Lageix S., Castilho B.A., Izotova L., Kinzy T.G., Hinnebusch A.G., et al., Evidence that eukaryotic translation elongation factor 1A (eEF1A) binds the Gcn2 protein C terminus and inhibits Gcn2 activity. J. Biol. Chem., 2011, 286 (42), 36568-36579.
  • [39] Ma X.M. and Blenis J., Molecular mechanisms of mTOR-mediated translational control, Nat. Rev. Mol. Cell Biol., 2009, 10, 307–318.[Crossref]
  • [40] Jackson R.J., Hellen C.U., Pestova T.V., The mechanism of eukaryotic translation initiation and principles of its regulation. Nat. Rev. Mol. Cell Biol., 2010, 11, 113–127.[Crossref]
  • [41] Choo A.Y., Yoon S.O., Kim S.G., Roux P.P., Blenis J., Rapamycin differentially inhibits S6Ks and 4EBP1 to mediate cell-type-specific repression of mRNA translation, Proc. Natl. Acad. Sci. U.S.A., 2008, 105, 17414–17419.[Crossref]
  • [42] Mokrejs M., Masek T., Vopálensky V., Hlubucek P., Delbos P., Pospísek M., IRESite--a tool for the examination of viral and cellular internal ribosome entry sites, Nucleic Acids Res., 2010, 38, 131-136.[Crossref]
  • [43] Holcík M., Targeting translation for treatment of cancer--a novel role for IRES?, Curr Cancer Drug Targets., 2004, 4(3), 299-311.
  • [44] Leprivier G., Remke M., Rotblat B., Dubuc A., Mateo A.R., Kool M., et al., The eEF2 kinase confers resistance to nutrient deprivation by blocking translation elongation, Cell, 2013, 153(5), 1064-1079.
  • [45] Zaher H.S. and Green R., Fidelity at the molecular level: lessons from protein synthesis, Cell, 2009, 136, 746–762.
  • [46] Meriin A.B., Mense M., Colbert J.D., Liang F., Bihler H., Zaarur N., et al., A novel approach to recovery of function of mutant proteins by slowing down translation, J. Biol. Chem., 2012, 287, 34264–34272.
  • [47] Meriin A.B., Zaarur N., Sherman M.Y., Association of translation factor eEF1A with defective ribosomal products generates a signal for aggresome formation, J. Cell Sci., 2012, 125, 2665–2674.[Crossref]
  • [48] Chuang S.M., Chen L., Lambertson D., Anand M., Kinzy T.G., Madura K., Proteasome-mediated degradation of cotranslationally damaged proteins involves translation elongation factor 1A, Mol Cell Biol., 2005, 25(1), 403-413.[Crossref]
  • [49] Sha Z., Brill L.M., Cabrera R., Kleifeld O., Scheliga J.S., Glickman M.H., et al., The eIF3 interactome reveals the translasome, a supercomplex linking protein synthesis and degradation machineries, Mol. Cell, 2009, 36(1), 141-52.
  • [50] Sciacovelli M., Guzzo G., Morello V., Frezza C., Zheng L., Nannini N., et al., The mitochondrial chaperone TRAP1 promotes neoplastic growth by inhibiting succinate dehydrogenase, Cell Metab., 2013, 17(6), 988-999.[Crossref]
  • [51] Matassa D.S., Amoroso M.R., Maddalena F., Landriscina M., Esposito F. New insights into TRAP1 pathway, Am J Cancer Res., 2012, 2(2), 235-248.
  • [52] Harel-Sharvit L., Eldad N., Haimovich G., Barkai O., Duek L., Choder M., RNA Polymerase II Subunits Link Transcription and mRNA Decay to Translation, Cell, 2010, 143(4), 552-563.[Crossref]
  • [53] Russo A., Cirulli C., Amoresano A., Pucci P., Pietropaolo C., Russo G., cis-acting sequences and trans-acting factors in the localization of mRNA for mitochondrial ribosomal proteins, Biochim Biophys Acta., 2008, 1779(12), 820-829
  • [54] Hotamisligil G.S., Endoplasmic reticulum stress and the inflammatory basis of metabolic disease, Cell, 2010, 140, 900–917.
  • [55] Neckers L., Workman P., Hsp90 molecular chaperone inhibitors: are we there yet?, Clin Cancer Res., 2012, 18(1), 64-76.
  • [56] 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(4), 342-350.[Crossref]
  • [57] 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(2), 257-270.
  • [58] Pridgeon JW, Olzmann JA, Chin LS, Li L: PINK1 protects against oxidative stress by phosphorylating mitochondrial chaperone TRAP1. PLoS Biol, 2007, 5(7), e172.
  • [59] Costantino, E., Maddalena, F., Calise, S., Piscazzi, A., Tirino, V., Fersini, A., Ambrosi, A., Neri, V., Esposito, F., Landriscina, M: TRAP1, a novel mitochondrial chaperone responsible for multi-drug resistance and protection from apoptotis in human colorectal carcinoma cells. Cancer Lett, 2009, 279(1), 39-46.
  • [60] Ghosh JC, Siegelin MD, Dohi T, Altieri DC: Heat shock protein 60 regulation of the mitochondrial permeability transition pore in tumor cells. Cancer Res, 2010, 70(22), 8988-8993.
  • [61] Rasola A, Sciacovelli M, Chiara F, Pantic B, Brusilow WS, Bernardi P. Activation of mitochondrial ERK protects cancer cells from death through inhibition of the permeability transition. Proc Natl Acad Sci U S A., 2010,107(2), 726-731.[Crossref]
  • [62] Guzzo G, Sciacovelli M, Bernardi P, Rasola A. Inhibition of succinate dehydrogenase by the mitochondrial chaperone TRAP1 has anti-oxidant and anti-apoptotic effects on tumor cells. Oncotarget, in press.
  • [63] Condelli V, Piscazzi A, Sisinni L, Matassa DS, Maddalena F, Lettini G, Simeon V, Palladino G, Amoroso MR, Trino S, Esposito F, Landriscina M. TRAP1 is involved in BRAF regulation and downstream attenuation of ERK phosphorylation and cell cycle progression: a novel target for BRAF-mutated colorectal tumors. Cancer Res., in press.
  • [64] Chae YC, Angelin A, Lisanti S, Kossenkov AV, Speicher KD, Wang H, Powers JF, Tischler AS, Pacak K, Fliedner S, Michalek RD, Karoly ED, Wallace DC, Languino LR, Speicher DW, Altieri DC.Landscape of the mitochondrial Hsp90 metabolome in tumours. Nat Commun., 2013, 4, 2139.
  • [65] Lisanti S, Tavecchio M, Chae YC, Liu Q, Brice AK, Thakur ML, Languino LR, Altieri DC. Deletion of the mitochondrial chaperone TRAP-1 uncovers global reprogramming of metabolic networks. Cell Rep., 2014, 8(3), 671-677.[Crossref]
  • [66] Chen CF, Chen Y, Dai K, Chen PL, Riley DJ, Lee WH. A new member of the hsp90 family of molecular chaperones interacts with the retinoblastoma protein during mitosis and after heat shock. Mol Cell Biol, 1996, 16, 4691-4699.
  • [67] Caino MC, Chae YC, Vaira V, Ferrero S, Nosotti M, Martin NM, Weeraratna A, O’Connell M, Jernigan D, Fatatis A, Languino LR, Bosari S, Altieri DC. Metabolic stress regulates cytoskeletal dynamics and metastasis of cancer cells. J Clin Invest., 2013, 123(7), 2907-2920.[Crossref]
  • [68] Lavery LA, Partridge JR, Ramelot TA, Elnatan D, Kennedy MA, Agard DA. Structural asymmetry in the closed state of mitochondrial Hsp90 (TRAP1) supports a two-step ATP hydrolysis mechanism. Mol Cell., 2014, 53(2), 330-343.
  • [69] Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell, 2011, 144(5), 646-674.[Crossref]
  • [70] Arkin MR, Wells JA. Small-molecule inhibitors of protein–protein interactions: progressing towards the dream. Nat. Rev. Drug Discov., 2004, 3, 301–317.[Crossref]
Document Type
Publication order reference
YADDA identifier
bwmeta1.element.-psjd-doi-10_2478_ersc-2014-0003
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