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Toxic proteins released from mitochondria in cell death

Abstract

A plethora of apoptotic stimuli converge on the mitochondria and affect their membrane integrity. As a consequence, multiple death-promoting factors residing in the mitochondrial intermembrane space are liberated in the cytosol. Pro- and antiapoptotic Bcl-2 family proteins control the release of these mitochondrial proteins by inducing or preventing permeabilization of the outer mitochondrial membrane. Once released into the cytosol, these mitochondrial proteins activate both caspase-dependent and -independent cell death pathways. Cytochrome c was the first protein shown to be released from the mitochondria into the cytosol, where it induces apoptosome formation. Other released mitochondrial proteins include apoptosis-inducing factor (AIF) and endonuclease G, both of which contribute to apoptotic nuclear DNA damage in a caspase-independent way. Other examples are Smac/DIABLO (second mitochondria-derived activator of caspase/direct IAP-binding protein with low PI) and the serine protease HtrA2/OMI (high-temperature requirement protein A2), which both promote caspase activation and instigate caspase-independent cytotoxicity. The precise mode of action and importance of cytochrome c in apoptosis in mammalian cells has become clear through biochemical, structural and genetic studies. More recently identified factors, for example HtrA2/OMI and Smac/DIABLO, are still being studied intensively in order to delineate their functions in apoptosis. A better understanding of these functions may help to develop new strategies to treat cancer.

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References

  • Abdullaev Z, Bodrova ME, Chernyak BV, Dolgikh DA, Kluck RM, Pereverzev MO, Arseniev AS, Efremov RG, Kirpichnikov MP, Mokhova EN, Newmeyer DD, Roder H and Skulachev VP . (2002). Biochem J., 362, 749–754.

  • Acehan D, Jiang X, Morgan DG, Heuser JE, Wang X and Akey CW . (2002). Mol. Cell, 9, 423–432.

  • Adrain C, Slee EA, Harte MT and Martin SJ . (1999). J. Biol. Chem., 274, 20855–20860.

  • Arnoult D, Gaume B, Karbowski M, Sharpe JC, Cecconi F and Youle RJ . (2003). EMBO J., 22, 4385–4399.

  • Arnoult D, Tatischeff I, Estaquier J, Girard M, Sureau F, Tissier JP, Grodet A, Dellinger M, Traincard F, Kahn A, Ameisen JC and Petit PX . (2001). Mol. Cell. Biol., 12, 3016–3030.

  • Arnt CR, Chiorean MV, Heldebrant MP, Gores GJ and Kaufmann SH . (2002). J. Biol. Chem., 277, 44236–44243.

  • Ashwell G and Hickman J . (1952). Proc. Soc. Exp. Biol. Med., 80, 407–413.

  • Bernardi P and Azzone GF . (1981). J. Biol. Chem., 256, 7187–7192.

  • Boatright KM, Renatus M, Scott FL, Sperandio S, Shin H, Pedersen IM, Ricci JE, Edris WA, Sutherlin DP, Green DR and Salvesen GS . (2003). Mol. Cell, 11, 529–541.

  • Bratton SB, Walker G, Srinivasula SM, Sun XM, Butterworth M, Alnemri ES and Cohen GM . (2001). EMBO J., 20, 998–1009.

  • Cain K, Bratton SB, Langlais C, Walker G, Brown DG, Sun XM and Cohen GM . (2000). J. Biol. Chem., 275, 6067–6070.

  • Cecconi F, Alvarez-Bolado G, Meyer BI, Roth KA and Gruss P . (1998). Cell, 94, 727–737.

  • Chai J, Shiozaki E, Srinivasula SM, Wu Q, Datta P, Alnemri ES, Shi Y and Dataa P . (2001). Cell, 104, 769–780.

  • Chautan M, Chazal G, Cecconi F, Gruss P and Golstein P . (1999). Curr. Biol., 9, 967–970.

  • Chen M, He H, Zhan S, Krajewski S, Reed JC and Gottlieb RA . (2001). J. Biol. Chem., 276, 30724–30728.

  • Clark CG and Roger AJ . (1995). Proc. Natl. Acad. Sci. USA, 92, 6518–6521.

  • Clausen T, Southan C and Ehrmann M . (2002). Mol. Cell, 10, 443–455.

  • Cory S and Adams JM . (2002). Nat. Rev. Cancer, 2, 647–656.

  • Denecker G, Vercammen D, Declercq W and Vandenabeele P . (2001a). Cell. Mol. Life Sci., 58, 356–370.

  • Denecker G, Vercammen D, Steemans M, Vanden Berghe T, Brouckaert G, van Loo G, Zhivotovsky B, Fiers W, Grooten J, Declercq W and Vandenabeele P . (2001b). Cell Death Differ., 8, 829–840.

  • Deshmukh M, Kuida K and Johnson Jr EM . (2000). J. Cell Biol., 150, 131–143.

  • Deveraux QL, Leo E, Stennicke HR, Welsh K, Salvesen GS and Reed JC . (1999). EMBO J., 18, 5242–5251.

  • Dorstyn L, Read S, Cakouros D, Huh JR, Hay BA and Kumar S . (2002). J. Cell Biol., 156, 1089–1098.

  • Du C, Fang M, Li Y, Li L and Wang X . (2000). Cell, 102, 33–42.

  • Dumont C, Durrbach A, Bidere N, Rouleau M, Kroemer G, Bernard G, Hirsch F, Charpentier B, Susin SA and Senik A . (2000). Blood, 96, 1030–1038.

  • Esposti MD, Erler JT, Hickman JA and Dive C . (2001). Mol. Cell. Biol., 21, 7268–7276.

  • Faccio L, Fusco C, Chen A, Martinotti S, Bonventre JV and Zervos AS . (2000). J. Biol. Chem., 275, 2581–2588.

  • Fiers W, Beyaert R, Declercq W and Vandenabeele P . (1999). Oncogene, 18, 7719–7730.

  • Forman HJ and Azzi A . (1997). FASEB J., 11, 374–375.

  • Frade JM and Michaelidis TM . (1997). BioEssays, 19, 827–832.

  • Frank J, Wagenknecht T, McEwen BF, Marko M, Hsieh CE and Mannella CA . (2002). J. Struct. Biol., 138, 85–91.

  • Fu J, Jin Y and Arend LJ . (2003). J. Biol. Chem., 30, 30.

  • Fulda S, Wick W, Weller M and Debatin KM . (2002). Nat. Med., 8, 808–815.

  • Glatz JF, Luiken JJ, van Bilsen M and van der Vusse GJ . (2002). Mol. Cell. Biochem., 239, 3–7.

  • Gray CW, Ward RV, Karran E, Turconi S, Rowles A, Viglienghi D, Southan C, Barton A, Fantom KG, West A, Savopoulos J, Hassan NJ, Clinkenbeard H, Hanning C, Amegadzie B, Davis JB, Dingwall C, Livi GP and Creasy CL . (2000). Eur. J. Biochem., 267, 5699–5710.

  • Gurbuxani S, Schmitt E, Cande C, Parcellier A, Hammann A, Daugas E, Kouranti I, Spahr C, Pance A, Kroemer G and Garrido C . (2003). Oncogene, 22, 6669–6678.

  • Hackstein JH, Akhmanova A, Boxma B, Harhangi HR and Voncken FG . (1999). Trends Microbiol., 7, 441–447.

  • Hakem R, Hakem A, Duncan GS, Henderson JT, Woo M, Soengas MS, Elia A, de la Pompa JL, Kagi D, Khoo W, Potter J, Yoshida R, Kaufman SA, Lowe SW, Penninger JM and Mak TW . (1998). Cell, 94, 339–352.

  • Harris BZ and Lim WA . (2001). J. Cell Sci., 114, 3219–3231.

  • Hegde R, Srinivasula SM, Zhang Z, Wassell R, Mukattash R, Cilenti L, DuBois G, Lazebnik Y, Zervos AS, Fernandes-Alnemri T and Alnemri ES . (2002). J. Biol. Chem., 277, 432–438.

  • Honarpour N, Du C, Richardson JA, Hammer RE, Wang X and Herz J . (2000). Dev. Biol., 218, 248–258.

  • Hu Y, Ding L, Spencer DM and Nunez G . (1998). J. Biol. Chem., 273, 33489–33494.

  • Hu S and Yang X . (2003). J. Biol. Chem., 278, 10055–10060.

  • Huang Y, Park YC, Rich RL, Segal D, Myszka DG and Wu H . (2001). Cell, 104, 781–790.

  • Huang Y, Rich RL, Myszka DG and Wu H . (2003). J. Biol. Chem., 25, 25.

  • Hung AY and Sheng M . (2002). J. Biol. Chem., 277, 5699–5702.

  • Jia L, Patwari Y, Kelsey SM, Srinivasula SM, Agrawal SG, Alnemri ES and Newland AC . (2003). Oncogene, 22, 1589–1599.

  • Jiang X and Wang X . (2000). J. Biol. Chem., 275, 31199–31203.

  • Jones JM, Datta P, Srinivasula SM, Ji W, Gupta S, Zhang Z, Davies E, Hajnoczky G, Saunders TL, Van Keuren ML, Fernandes-Alnemri T, Meisler MH and Alnemri ES . (2003). Nature, 425, 721–727.

  • Joza N, Susin SA, Daugas E, Stanford WL, Cho SK, Li CY, Sasaki T, Elia AJ, Cheng HY, Ravagnan L, Ferri KF, Zamzami N, Wakeham A, Hakem R, Yoshida H, Kong YY, Mak TW, Zuniga-Pflucker JC, Kroemer G and Penninger JM . (2001). Nature, 410, 549–554.

  • Kanuka H, Sawamoto K, Inohara N, Matsuno K, Okano H and Miura M . (1999). Mol. Cell, 4, 757–769.

  • Kawane K, Fukuyama H, Yoshida H, Nagase H, Ohsawa Y, Uchiyama Y, Okada K, Iida T and Nagata S . (2003). Nat. Immunol., 4, 138–144.

  • Klein JA, Longo-Guess CM, Rossmann MP, Seburn KL, Hurd RE, Frankel WN, Bronson RT and Ackerman SL . (2002). Nature, 419, 367–374.

  • Kluck RM, Bossy-Wetzel E, Green DR and Newmeyer DD . (1997). Science, 275, 1132–1136.

  • Kluck RM, Ellerby LM, Ellerby HM, Naiem S, Yaffe MP, Margoliash E, Bredesen D, Mauk AG, Sherman F and Newmeyer DD . (2000). J. Biol. Chem., 275, 16127–16133.

  • Kohler C, Gahm A, Noma T, Nakazawa A, Orrenius S and Zhivotovsky B . (1999). FEBS Lett., 447, 10–12.

  • Koonin EV and Aravind L . (2002). Cell Death Differ., 9, 394–404.

  • Kovacsovics M, Martinon F, Micheau O, Bodmer JL, Hofmann K and Tschopp J . (2002). Curr. Biol., 12, 838–843.

  • Kroemer G and Reed JC . (2000). Nat. Med., 6, 513–519.

  • Krojer T, Garrido-Franco M, Huber R, Ehrmann M and Clausen T . (2002). Nature, 416, 455–459.

  • Kuida K, Haydar TF, Kuan CY, Gu Y, Taya C, Karasuyama H, Su MS, Rakic P and Flavell RA . (1998). Cell, 94, 325–337.

  • Kuwana T, Mackey MR, Perkins G, Ellisman MH, Latterich M, Schneiter R, Green DR and Newmeyer DD . (2002). Cell, 111, 331–342.

  • Lang BF, Gray MW and Burger G . (1999). Annu. Rev. Genet., 33, 351–397.

  • Li K, Li Y, Shelton JM, Richardson JA, Spencer E, Chen ZJ, Wang X and Williams RS . (2000). Cell, 101, 389–399.

  • Li LY, Luo X and Wang X . (2001). Nature, 412, 95–99.

  • Li W, Srinivasula SM, Chai J, Li P, Wu JW, Zhang Z, Alnemri ES and Shi Y . (2002). Nat. Struct. Biol., 9, 436–441.

  • Li F, Srinivasan A, Wang Y, Armstrong RC, Tomaselli KJ and Fritz LC . (1997). J. Biol. Chem., 272, 30299–30305.

  • Lipinska B, Zylicz M and Georgopoulos C . (1990). J Bacteriol., 172, 1791–1797.

  • Liu X, Kim CN, Yang J, Jemmerson R and Wang X . (1996). Cell, 86, 147–157.

  • Liu Z, Sun C, Olejniczak ET, Meadows RP, Betz SF, Oost T, Herrmann J, Wu JC and Fesik SW . (2000). Nature, 408, 1004–1008.

  • Liu X, Zou H, Slaughter C and Wang X . (1997). Cell, 89, 175–184.

  • MacFarlane M, Merrison W, Bratton SB and Cohen GM . (2002). J. Biol. Chem., 277, 36611–36616.

  • Mancini M, Nicholson DW, Roy S, Thornberry NA, Peterson EP, Casciola-Rosen LA and Rosen A . (1998). J. Cell Biol., 140, 1485–1495.

  • Marsden VS, O'Connor L, O'Reilly LA, Silke J, Metcalf D, Ekert PG, Huang DC, Cecconi F, Kuida K, Tomaselli KJ, Roy S, Nicholson DW, Vaux DL, Bouillet P, Adams JM and Strasser A . (2002). Nature, 419, 634–637.

  • Martins LM, Iaccarino I, Tenev T, Gschmeissner S, Totty NF, Lemoine NR, Savopoulos J, Gray CW, Creasy CL, Dingwall C and Downward J . (2002). J. Biol. Chem., 277, 439–444.

  • Martins LM, Turk BE, Cowling V, Borg A, Jarrell ET, Cantley LC and Downward J . (2003). J. Biol. Chem., 278, 49417–49427.

  • Marzo I, Brenner C, Zamzami N, Jurgensmeier JM, Susin SA, Vieira HL, Prevost MC, Xie Z, Matsuyama S, Reed JC and Kroemer G . (1998). Science, 281, 2027–2031.

  • McIlroy D, Tanaka M, Sakahira H, Fukuyama H, Suzuki M, Yamamura K, Ohsawa Y, Uchiyama Y and Nagata S . (2000). Genes Dev., 14, 549–558.

  • Melloni E, Averna M, Salamino F, Sparatore B, Minafra R and Pontremoli S . (2000). J. Biol. Chem., 275, 82–86.

  • Miramar MD, Costantini P, Ravagnan L, Saraiva LM, Haouzi D, Brothers G, Penninger JM, Peleato ML, Kroemer G and Susin SA . (2001). J. Biol. Chem., 276, 16391–16398.

  • Mitchell SA, Brown EC, Coldwell MJ, Jackson RJ and Willis AE . (2001). Mol. Cell. Biol., 21, 3364–3374.

  • Mootha VK, Wei MC, Buttle KF, Scorrano L, Panoutsakopoulou V, Mannella CA and Korsmeyer SJ . (2001). EMBO J., 20, 661–671.

  • Ohiro Y, Garkavtsev I, Kobayashi S, Sreekumar KR, Nantz R, Higashikubo BT, Duffy SL, Higashikubo R, Usheva A, Gius D, Kley N and Horikoshi N . (2002). FEBS Lett., 524, 163–171.

  • Okada H, Suh WK, Jin J, Woo M, Du C, Elia A, Duncan GS, Wakeham A, Itie A, Lowe SW, Wang X and Mak TW . (2002). Mol. Cell. Biol., 22, 3509–3517.

  • Parrish J, Li L, Klotz K, Ledwich D, Wang X and Xue D . (2001). Nature, 412, 90–94.

  • Parrish JZ, Yang C, Shen B and Xue D . (2003). EMBO J., 22, 3451–3460.

  • Puthalakath H and Strasser A . (2002). Cell. Death. Differ., 9, 505–512.

  • Qin ZH, Wang Y, Kikly KK, Sapp E, Kegel KB, Aronin N and DiFiglia M . (2001). J. Biol. Chem., 276, 8079–8086.

  • Ravagnan L, Gurbuxani S, Susin SA, Maisse C, Daugas E, Zamzami N, Mak T, Jaattela M, Penninger JM, Garrido C and Kroemer G . (2001). Nat. Cell Biol., 3, 839–843.

  • Renatus M, Stennicke HR, Scott FL, Liddington RC and Salvesen GS . (2001). Proc. Natl. Acad. Sci. USA, 98, 14250–14255.

  • Ricci JE, Gottlieb RA and Green DR . (2003). J. Cell Biol., 160, 65–75.

  • Riedl SJ, Renatus M, Schwarzenbacher R, Zhou Q, Sun C, Fesik SW, Liddington RC and Salvesen GS . (2001). Cell, 104, 791–800.

  • Roberts DL, Merrison W, MacFarlane M and Cohen GM . (2001). J. Cell Biol., 153, 221–228.

  • Rodriguez A, Oliver H, Zou H, Chen P, Wang X and Abrams JM . (1999). Nat. Cell Biol., 1, 272–279.

  • Sahara S, Aoto M, Eguchi Y, Imamoto N, Yoneda Y and Tsujimoto Y . (1999). Nature, 401, 168–173.

  • Sakahira H, Enari M and Nagata S . (1998). Nature, 391, 96–99.

  • Salvesen GS and Duckett CS . (2002). Nat. Rev. Mol. Cell. Biol., 3, 401–410.

  • Samali A, Zhivotovsky B, Jones DP and Orrenius S . (1998). FEBS Lett., 431, 167–169.

  • Scorrano L, Ashiya M, Buttle K, Weiler S, Oakes SA, Mannella CA and Korsmeyer SJ . (2002). Dev. Cell, 2, 55–67.

  • Shiozaki EN, Chai J, Rigotti DJ, Riedl SJ, Li P, Srinivasula SM, Alnemri ES, Fairman R and Shi Y . (2003). Mol. Cell, 11, 519–527.

  • Skorko-Glonek J, Zurawa D, Kuczwara E, Wozniak M, Wypych Z and Lipinska B . (1999). Mol Gen Genet, 262, 342–350.

  • Spiess C, Beil A and Ehrmann M . (1999). Cell, 97, 339–347.

  • Srinivasula SM, Ahmad M, Fernandes-Alnemri T and Alnemri ES . (1998). Mol. Cell, 1, 949–957.

  • Srinivasula SM, Gupta S, Datta P, Zhang Z, Hegde R, Cheong N, Fernandes-Alnemri T and Alnemri ES . (2003). J. Biol. Chem., 278, 31469–31472.

  • Srinivasula SM, Hegde R, Saleh A, Datta P, Shiozaki E, Chai J, Lee RA, Robbins PD, Fernandes-Alnemri T, Shi Y and Alnemri ES . (2001). Nature, 410, 112–116.

  • Stennicke HR, Deveraux QL, Humke EW, Reed JC, Dixit VM and Salvesen GS . (1999). J. Biol. Chem., 274, 8359–8362.

  • Susin SA, Lorenzo HK, Zamzami N, Marzo I, Brenner C, Larochette N, Prevost MC, Alzari PM and Kroemer G . (1999a). J. Exp. Med., 189, 381–394.

  • Susin SA, Lorenzo HK, Zamzami N, Marzo I, Snow BE, Brothers GM, Mangion J, Jacotot E, Costantini P, Loeffler M, Larochette N, Goodlett DR, Aebersold R, Siderovski DP, Penninger JM and Kroemer G . (1999b). Nature, 397, 441–446.

  • Suzuki Y, Imai Y, Nakayama H, Takahashi K, Takio K and Takahashi R . (2001a). Mol. Cell, 8, 613–621.

  • Suzuki Y, Nakabayashi Y and Takahashi R . (2001b). Proc. Natl. Acad. Sci. USA, 98, 8662–8667.

  • Tyler DD . (1992). The Mitochondrion in Health and Disease. VCH Publishers: London, pp. 1–557.

    Google Scholar 

  • van Loo G, Demol H, van Gurp M, Hoorelbeke B, Schotte P, Beyaert R, Zhivotovsky B, Gevaert K, Declercq W, Vandekerckhove J and Vandenabeele P . (2002). Cell Death Differ., 9, 301–308.

  • van Loo G, Saelens X, Matthijssens F, Schotte P, Beyaert R, Declercq W and Vandenabeele P . (2002a). Cell Death Differ., 9, 1207–1211.

  • van Loo G, Schotte P, van Gurp M, Demol H, Hoorelbeke B, Gevaert K, Rodriguez I, Ruiz-Carrillo A, Vandekerckhove J, Declercq W, Beyaert R and Vandenabeele P . (2001). Cell Death Differ., 8, 1136–1142.

  • van Loo G, van Gurp M, Depuydt B, Srinivasula SM, Rodriguez I, Alnemri ES, Gevaert K, Vandekerckhove J, Declercq W and Vandenabeele P . (2002b). Cell Death Differ., 9, 20–26.

  • Verhagen AM, Ekert PG, Pakusch M, Silke J, Connolly LM, Reid GE, Moritz RL, Simpson RJ and Vaux DL . (2000). Cell, 102, 43–53.

  • Verhagen AM, Silke J, Ekert PG, Pakusch M, Kaufmann H, Connolly LM, Day CL, Tikoo A, Burke R, Wrobel C, Moritz RL, Simpson RJ and Vaux DL . (2002). J. Biol. Chem., 277, 445–454.

  • Wang X, Yang C, Chai J, Shi Y and Xue D . (2002). Science, 298, 1587–1592.

  • Waterhouse NJ, Goldstein JC, von Ahsen O, Schuler M, Newmeyer DD and Green DR . (2001). J. Cell Biol., 153, 319–328.

  • Widlak P, Li LY, Wang X and Garrard WT . (2001). J. Biol. Chem., 276, 48404–48409.

  • Wu G, Chai J, Suber TL, Wu JW, Du C, Wang X and Shi Y . (2000). Nature, 408, 1008–1012.

  • Wu M, Xu LG, Li X, Zhai Z and Shu HB . (2002). J. Biol. Chem., 277, 25617–25623.

  • Xue L, Fletcher GC and Tolkovsky AM . (1999). Mol. Cell Neurosci., 14, 180–198.

  • Yang QH, Church-Hajduk R, Ren J, Newton ML and Du C . (2003). Genes Dev., 17, 1487–1496.

  • Yang Y, Fang S, Jensen JP, Weissman AM and Ashwell JD . (2000). Science, 288, 874–877.

  • Yang J, Liu X, Bhalla K, Kim CN, Ibrado AM, Cai J, Peng TI, Jones DP and Wang X . (1997). Science, 275, 1129–1132.

  • Ye H, Cande C, Stephanou NC, Jiang S, Gurbuxani S, Larochette N, Daugas E, Garrido C, Kroemer G and Wu H . (2002). Nat. Struct. Biol., 9, 680–684.

  • Yu SW, Wang H, Poitras MF, Coombs C, Bowers WJ, Federoff HJ, Poirier GG, Dawson TM and Dawson VL . (2002). Science, 297, 259–263.

  • Zamzami N, Susin SA, Marchetti P, Hirsch T, Gomez-Monterrey I, Castedo M and Kroemer G . (1996). J. Exp. Med., 183, 1533–1544.

  • Zhang J, Liu X, Scherer DC, van Kaer L, Wang X and Xu M . (1998). Proc. Natl. Acad. Sci. USA, 95, 12480–12485.

  • Zhivotovsky B, Orrenius S, Brustugun OT and Doskeland SO . (1998). Nature, 391, 449–450.

  • Zhivotovsky B, Samali A, Gahm A and Orrenius S . (1999). Cell Death Differ., 6, 644–651.

  • Zou H, Henzel WJ, Liu X, Lutschg A and Wang X . (1997). Cell, 90, 405–413.

  • Zou H, Yang R, Hao J, Wang J, Sun C, Fesik SW, Wu JC, Tomaselli KJ and Armstrong RC . (2003). J. Biol. Chem., 278, 8091–8098.

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Acknowledgements

We thank Amin Bredan for editorial help. This work was supported by the Interuniversitaire Attractiepolen (IUAP-V), the Fonds voor Wetenschappelijk Onderzoek-Vlaanderen (Grants 31.5189.00 and 3G.0006.01) and the EC-RTD (Grant QLRT-CT-1999-00739), the Ghent University cofinancing EU project (011C0300) and GOA project (12050502). X Saelens is supported by the ‘Biotech Fonds’ and GOA project (12050502), L Vande Walle and N Festjens by a grant from the IWT, M van Gurp by a grant from the ‘Centrum voor Gezwelziekten’, G van Loo was paid by the IUAP-V.

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Saelens, X., Festjens, N., Walle, L. et al. Toxic proteins released from mitochondria in cell death. Oncogene 23, 2861–2874 (2004). https://doi.org/10.1038/sj.onc.1207523

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