Main Pro-Apoptotic Member of Bcl-2 Family Proteins – Bax
DOI:
https://doi.org/10.2478/v10107-009-0004-3Keywords:
apoptosis, Bcl-2 family, Bax, apoptosis mitochondrial pathwayAbstract
Programmed cell death (apoptosis) plays a vital role in the regulation of cellular homeostasis. Because of apoptosis fundamental importance, this process is highly regulated. One important set of factors involved in apoptosis regulation is the Bcl-2 family proteins. Bcl-2 family members form a complex regulatory network that controls cell survival and death in response to different physiological and pathological signals. This family includes both pro- and anti-apoptotic members, and Bax protein (Mol wt 21 kDa) is a major pro-apoptotic factor with multifunctional activity. This review summarizes new data about the main representative of Bcl-2 family – Bax, its structure and mechanism(s) by which this protein modulates apoptosis.
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Apte, S.S., Mattei, M.G., Olsen, B.R. 1995. Mapping of the human bax gene to chromosome 19q13.3-13.4 and isolation of a novel alternatively spliced transcript Bax delta. Genomics 26: 592–594.
Google Scholar
Bargou, R.C., Bommert, K., Weinmann, P., Daniel, P.T., Wagener, C., Mapara, M.Y., Dörken, B. 1995. Expression of the bcl-2 gene family in normal and malignant breast tissue: low bax-alpha expression in tumor cells correlates with resistance towards apoptosis. Eur. J. Immunol. 25: 770–775.
Google Scholar
Bednarek, J., Kiliańska, Z.M. 2005. Białka przestrzeni międzybłonowej mitochondriów uczestniczące w procesie apoptozy. Post. Biochem. 51: 447–458.
Google Scholar
Borner C. 2003. The Bcl-2 protein family: sensors and checkpoints for life-or-death decisions. Mol. Immunol. 39: 615–647.
Google Scholar
Breckenridge, D.G., Germain, M., Mathai, J.P., Nguyen, M., Shore, G.C. 2003. Regulation of apoptosis by endoplasmic reticulum pathway. Oncogene 22: 8608–8618.
Google Scholar
Brustovetsky, T., Li, T., Yang, Y., Zhang, J.T., Antonsson, B., Brustovetsky, N. 2010. Bax insertion, oligomerization, and outer membrane permeabilization in brain mitochondria: Role of permeability transition and SH-redox regulation. Biochim. Biphys. Acta 1797: 1795–1806.
Google Scholar
Cao, X., Deng, X., May, W.S. 2003. Cleavage of Bax to p18 Bax accelerates stress-induced apoptosis, and a cathepsin-like protease may rapidly degrade p18 Bax. Blood. 102: 2605–2614.
Google Scholar
Cartron, P.F., Gallenne, T., Bugras, G., Gautier., Manero, F., Vuso, P., Meflah, K., Vallette, F.M., Juin, P. 2004. The first α-helix of Bax plays a necessary role in its ligand-induced activation by the BH3-only proteins Bid and Puma. Mol. Cell. 16: 807–818.
Google Scholar
Cartron, P.F., Oliver, L., Martin, S., Moreau, C., Lecabellec, M.T., Jezequel, P., Meflah, K., Vallette, F.M. 2002. The expression of a new variant of the pro-apoptotic molecule Bax, Bax psi, is correlated with an increased survival of glioblastoma multiforme patients. Hum. Mol. Genet. 11: 675–687.
Google Scholar
Castle, V.P., Heidelberger, K.P., Bromberg, J., Ou, X., Dole, M., Nuñez, G. 1993. Expression of the apoptosis-suppressing protein Bcl-2 in neuroblastoma is associated with unfavorable histology and N-myc amplification. Am. J. Pathol. 143: 1543–1550.
Google Scholar
Chipuk, J.E., Bouchier-Hayes, L., Green, D.R. 2006. Mitochondrial outer membrane permeabilization during apoptosis: the innocent bystander scenario. Cell. Death Differ. 13: 1396–1402.
Google Scholar
Chipuk, J.E., Green, D. 2004. Cytoplasmic p53: bax and forward. Cell Cycle. 3: 429–431.
Google Scholar
Chipuk, J.E., Green, D. 2008. How do Bcl-2 proteins induce mitochondria outer membrane permeabilization? Trends Cell. Biol. 18: 157–164.
Google Scholar
Christenson, E., Merlin, S., Saito, M., Schlesinger, P. 2008. Cholesterol effects on Bax pore activation. J. Mol. Biol. 381: 1168–1183.
Google Scholar
Codogno, P., Meijer, A.J. 2006. Atg: more than autophagy factor. Nat. Cell. Biol. 8: 1045–1047.
Google Scholar
Cornblau, S.M., Thall, P.F., Estrov, Z., Walterscheid, M., Patel, S., Theriault, A., Keating, M.J., Kantarjian, H., Estey, E., Andreeff, M. 1999. The prognostic impact of Bcl2 protein expression in acute myelogenous leukemia varies with cytogenetics. Clin. Cancer. Res. 5: 1758–1766.
Google Scholar
Cory, S., Huang, D.C., Adams, J.M. 2003. The Bcl-2 family: roles in cell survival and oncogenesis. Oncogene 22: 8590–8607.
Google Scholar
Cuddeback, S.M., Yamaguchi, H., Komatsu, K., Miyashita, T., Yamada, M., Wu, C., Singh, S., Wang, H.G. 2001. Molecular cloning and characterization of Bif-1. A novel Src homology 3 domain-containing protein that associates with Bax. J. Biol. Chem. 276: 20559–20565.
Google Scholar
Day, C.L., Smits, C., Fan, F.C., Lee, E.F., Fairlie, W.D., Hinds, M.G. 2008. Structure of the BH3 domains from the p53-inducible BH3-only proteins Noxa and Puma in complex with Mcl-1. J. Mol. Biol. 380: 958–971.
Google Scholar
Desagher, S., Osen-Sand, A., Nichols, A., Eskes, R., Montessiut, S., Lauper, S., Maundrell, K., Antonsson, B., Martinou, J.C. 1999. Bid-induced conformational change of Bax is responsible for mitochondrial cytochrome c release during apoptosis. J. Cell Biol. 144: 891–901.
Google Scholar
Droin, N.M., Green, D.R. 2004. Role of Bcl-2 family members in immunity and disease. Biochim. Biophys. Acta. 1644: 179–188.
Google Scholar
Ewings, K.E., Hadfield-Moorhouse, K., Wiggins, C.M., Wickenden, J.A., Balmanno, K., Gilley, R., Degenhardt, K., White, E., Cook, S.J. 2007. ERK1/2-dependent phosphorylation of BimEL promotes its rapid dissociation from Mcl-1 and Bcl-XL. EMBO J. 26: 2856–2867.
Google Scholar
Falke, D., Fisher, M., Ye, D., Juliano, R.L. 2003. Design of artificial transcription factors to selectively regulate the pro-apoptotic bax gene. Nucleic Acids Res. 31(3): e10.
Google Scholar
Ferreira, C.G., Epping, M., Kruyt, F.A.E., Giaccone, G. 2002. Apoptosis: target of cancer therapy. Clin. Cancer Res. 8: 2024–2034.
Google Scholar
Frey, V., Viaud, J., Subra, G., Cauquil, N., Guichou, J.F., Casara, P., Grassy, G., Chavanieu, A. 2008. Structure-activity relationships of Bak derived peptides: Affinity and specificity modulations by amino acid replacement. Eur. J. Med. Chem. 43: 966–972.
Google Scholar
Gao, G., Dou, Q.P. 2000. N-terminal cleavage of Bax by calpain generates a potent proapoptotic 18 kDa fragment that promotes bcl-2-independent cytochrome c release and apoptotic cell death. J. Cell. Biochem. 80: 53–72.
Google Scholar
George, N.M., Targy, N., Evans, J.J., Zhang, L., Luo, X. 2010. Bax contains two functional mitochondrial targeting sequences and translocates to mitochondria in a conformational change- and homo-oligomerization-driven process. J. Biol. Chem. 285: 1384–1392.
Google Scholar
Gotoh, T., Terada, K., Oyadomari, S., Mori, M. 2004. Hsp70-DnaJ chaperone pair prevents nitric oxide- and CHOP-induced apoptosis by inhibiting translocation of Bax to mitochondria. Cell. Death. Differ. 11: 390–402.
Google Scholar
Greijer, A.E., van der Wall, E. 2004. The role of hypoxia inducible factor 1 (HIF-1) in hypoxia induced apoptosis. J. Clin. Pathol. 57: 1009–1014.
Google Scholar
Griffiths, G. J., Corfe, B.M., Savory, P., Leech, S., Esposti, M.D., Hickman, J.A., Dive, C. 2001. Cellular damage signals promote sequential changes at the N-terminus and BH-1 domain of the pro-apoptotic protein Bak. Oncogene 20: 7668–7676.
Google Scholar
Guo, B., Godzik, A., Reed, J.C. 2001. Bcl-G, a novel pro-apoptotic member of the Bcl-2 family. J. Biol. Chem. 276: 2780–2785.
Google Scholar
Gurudutta, G.U., Verma, Y.K., Singh, V.K., Gupta, P., Raj, H.G., Sharma, R.K., Chandra, R. 2005. Structural conservation of residues in BH1 and BH2 domains of Bcl-2 family proteins. FEBS Lett. 579: 3503–3507.
Google Scholar
Hanson, C.J., Bootman, M.D., Distelhorst, C.W., Maraldi, T., Roderick, H.L. 2008. The cellular concentration of Bcl-2 determinates its pro- or anti-apoptotic effect. Cell. Calcium 44: 243–258.
Google Scholar
Hayashi, T., Faustman, D.L. 2003. Role of defective apoptosis in type 1 diabetes and other autoimmune diseases. Rec. Prog. Horm. Res. 58: 131–153.
Google Scholar
Hengartner, M.O. 2000. The biochemistry of apoptosis. Nature 407: 770–776.
Google Scholar
Hetz, C., Glimcher, L. 2008. The daily job of night killers: alternative roles of the Bcl-2 family in organelle physiology. Trends. Cell. Biol. 18: 38–44.
Google Scholar
Hossini, A.M., Eberle, J. 2008. Apoptosis induction by Bcl-2 proteins independent of the BH3 domain. Biochem. Pharmacol. 76: 1612–1619.
Google Scholar
Hückelhoven, R. 2004. Bax inhibitor-1, an ancient cell death suppressor in animals and plants with prokaryotic relatives. Apoptosis 9: 299–307.
Google Scholar
Jansen, B., Schlagbauer-Wadl, H., Brown, B.D., Bryan, B.D., van Elsas, A., Müller, M., Wolff, K., Eichler, H.G., Pehamberger, H. 1998. Bcl-2 antisense therapy chemosensitizes human melanoma in SCID mice. Nat. Med. 4: 232–234.
Google Scholar
Jin, K.L., Graham S.H., Mao, X.O., He, X., Nagayama, T., Simon, R.P., Greenberg, D.A. 2001. Bax kappa, a novel Bax splice variant from ischemic rat brain lacking an ART domain, promotes neuronal cell death. J. Neurochem. 77: 1508–1519.
Google Scholar
Karst, A.M., Li, G. 2007. BH3-only proteins in tumorigenesis and malignant melanoma. Cell. Mol. Life Sci. 64: 318–330.
Google Scholar
Kataoka, T., Holler, N., Micheau, O., Martinon, F., Tinel, A., Hofmann, K., Tschopp, J. 2001. Bcl-rambo, a novel Bcl-2 homologue that induces apoptosis via its unique C-terminal extension. J. Biol. Chem. 276: 19548–19554.
Google Scholar
Ke, N., Godzik, A., Reed, J.C. 2001. Bcl-B, a novel Bcl-2 family member that differentially binds and regulates Bax and Bak. J. Biol. Chem. 276: 12481–12484.
Google Scholar
Khor, L.Y., Moughan, J., Al-Saleem, T., Hammond, E.H., Venkatesan, V., Rosenthal, S.A., Ritter, Ma., Sandler, H.M., Hanks, G.E., Shipley, W.U., Pollack, A. 2007. Bcl-2 and Bax expression predict prostate cancer outcome in men treated with androgen deprivation and radiotherapy on radiation therapy oncology group protocol 92-02. Clin. Cancer Res. 13: 3585–3590.
Google Scholar
Kiliańska, Z.M. 2002. Apoptoza organizmów zwierzęcych. In: L. Kłyszejko-Stefanowicz (ed.) Cytobiochemia. Biochemia niektórych struktur komórkowych. Wydawnictwo Naukowe PWN, Warszawa, pp. 772–814.
Google Scholar
Kobayashi, T., Sawa, H., Morikawa, J., Zhang, W., Shiku, H. 2000. Bax induction activates apoptotic cascade via mitochondrial cytochrome c release and Bax overexpression enhances apoptosis induced by chemotherapeutic agents in DLD-1 colon cancer cells. Jpn. J. Cancer Res. 91: 1264–1268.
Google Scholar
Kobylinska, A., Bednarek, J., Blonski, J.Z., Hanausek, M., Walaszek, Z., Robak, T., Kilianska, Z.M., 2006. In vitro sensitivity of B-cell chronic lymphocytic leukemia to cladribine and its combinations with mafosfamide and/or mitoxantrone. Oncol. Rep. 16: 1389–1395.
Google Scholar
Kolluri, S.K., Zhu, X., Zhou, X., Lin, B., Chen, Y., Sun, K., Tian, X., Town, J., Cao, X., Lin, F., Zhai, D., Kitada, S., Luciano, F., Donnell, E., Cao, Y., He, F., Lin, J., Reed, J.C., Satterthwait, A.C., Zhang, X.K. 2008. A short Nur77- derived peptide converts Bcl-2 from a protector to a killer. Cancer Cell. 14: 285–298.
Google Scholar
Konopleva, M., Tari, A.M., Estrov, Z., Harris, D., Xie, Z., Zhao, S., López-Berestein, G., Andreeff, M. 2000. Liposomal Bcl-2 antisense oligonucleotides enhance proliferation, sensitize acute myeloid leukemia to cytosine-arabinoside, and induce apoptosis independent of other antiapoptotic proteins. Blood 95: 3929–3938.
Google Scholar
Krajewski, S., Krajewska, M., Ellerby, L.M., Welsh, K., Xie, Z., Deveraux, Q.L., Salvesen, G.S., Bredesen, D.E., Rosenthal, R.E., Fiskum, G., Reed, J.C. 1999. Release of caspase-9 from mitochondria during neuronal apoptosis and cerebral ischemia. Proc. Natl. Acad. Sci. U.S.A. 96: 5752–5757.
Google Scholar
Kumarswamy, R., Chandna, S. 2009. Putative partners in Bax mediated cytochrome-c release: ANT, CypD, VDAC or none of them? Mitochondrion 9: 1–8.
Google Scholar
Leber, B., Lin, J., Andrews, D.W. 2007. Embedded together: the life and death consequences of interaction of the Bcl-2 family with membranes. Apoptosis. 12: 897–911.
Google Scholar
Lee, R.M., Chen, J., Matthews, C.P., Mcdougall, J.K., Neiman, P.E. 2001. Characterization of NR13-related human cel death regulator, Boo/Diva, in normal and cancer tissues. Biochim. Biophys. Acta 1520: 187–194.
Google Scholar
Li, X., Marani, M., Yu, J., Nan, B., Roth, J.A., Kagawa, S., Fang, B., Denner, L., Marcelli, M. 2001. Adenovirus-mediated Bax overexpression for the induction of therapeutic apoptosis in prostate cancer. Cancer Res. 61: 186–191.
Google Scholar
Lin, B., Kolluri, S.K., Lin, F., Liu, W., Han, Y.H., Cao, X., Dawson, M.I., Reed, J.C., Zhang, X.K. 2004. Conversion of Bcl-2 from protector to killer by interaction with nuclear orphan receptor Nur77/TR3. Cell 116: 527–540.
Google Scholar
Lowe, S.W., Cepero, E., Evan, G. 2004. Intrinsic tumour suppression. Nature 432: 307–315.
Google Scholar
Luciano, F., Krajewska, M., Ortiz-Rubio, P., Krajewski, S., Zhai, D., Faustin, B., Bruey, J.M., Bailly-Maitre, B., Lichtenstein, A., Kolluri, S.K., Satterthwait, A.C., Zhang, X.K., Reed, J.C. 2007. Nur77 converts phenotype of Bcl-B, an antiapoptotic protein expressed in plasma cells and myeloma. Blood. 109: 3849–3855.
Google Scholar
Lucken-Ardjomande, S., Martinou, J.C. 2005. Regulation of Bcl-2 proteins and of the permeability of the outer mitochondrial membrane, Regulation of Bcl-2 proteins and of the permeability of the outer mitochondrial membrane. C. R. Biol. 328: 616–631.
Google Scholar
Luo, X., Budihardjo, J., Zou, H., Slaughter, C., Wang, X. 1998. Bid, an Bcl-2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 94: 481–490.
Google Scholar
Majewski, N., Nogueira, V., Bhaskar, P., Coy, P.E., Skeen, J.E., Gottlob, K., Chandel, N.S., Thompson, C.B., Robey, R.B., Hay. N. 2004. Hexokinase-mitochondria interaction mediated by Akt is required to inhibit apoptosis in the presence or absence of Bax and Bak. Mol. Cell. 16: 819–830.
Google Scholar
Meir, O., Dvash, E., Werman, A., Rubinstein, M. 2010. C/EBP-beta regulates endoplasmic reticulum stress-triggered cel death in mouse human models. PLOS One 5: e9516.
Google Scholar
Ming, L., Wang, P., Bank, A., Zhang, L. 2006. PUMA dissociates Bax and Bcl-XL to induce apoptosis in colon cancer cells. J. Biol. Chem. 281: 16034–16042.
Google Scholar
Moldoveanu, T., Liu, Q., Tocilj, A., Watson, M., Shore, G., Gehring, K. 2006. The X-ray structure of Bak homodimer reveals an inhibitory zinc binding site. Mol. Cell. 24: 677–688.
Google Scholar
Ndozangue-Touriguine, O., Hamelin, J., Bréard, J. 2008. Cytoskeleton and apoptosis. Biochem. Pharmacol. 76: 11–18.
Google Scholar
Oltvai, Z., Korsmeyer, S. 1993. Bcl-2 heterodimrizes in vivo with conserved homolog, Bax, that accelerates programmed cell death. Cell 74: 609–619.
Google Scholar
Ouyang, H., Furukawa, T., Abe, T., Kato, Y., Horii, A. 1998. The BAX gene, the promoter of apoptosis, is mutated in genetically unstable cancers of the colorectum, stomach, and endometrium. Clin. Cancer. Res. 4: 1071–1074.
Google Scholar
Pepper, C., Hoy, T., Bentley, D.P. 1997. Bcl-2/Bax ratios in chronic lymphocytic leukemia and their correlation with in vitro apoptosis and clinical resistance. Br. J. Cancer 76: 935–958.
Google Scholar
Perez, G.I., Knudson, C.M., Leykin, L., Korsmeyer, S.J., Tilly, J.L. 1997. Apoptosis-associated signaling pathways are required for chemotherapy-mediated female germ cell destruction. Nat. Med. 3: 1228–1332.
Google Scholar
Petros, A.M., Olejniczak, E.T., Fesik, S.W. 2004. Structural biology of the Bcl-2 family of proteins. Biochim. Biophys. Acta 1644: 83–94.
Google Scholar
Pirocanac, E.C., Nassirpour, R., Yang, M., Wang, J., Nardin, S.R., Gu, J., Fang, B., Moossa, A.R., Hoffman, R.M., Bouvet, M. 2002. Bax-induction gene therapy of pancreatic cancer. J. Surg. Res. 106: 346–351.
Google Scholar
Rampino, N., Yamamoto, H., Ionov, Y., Li., Y., Sawai., H., Reed, J.C., Perucho, M. 1997. Somatic frameshift mutations in the BAX gene in colon cancers of the microsatellite mutator phenotype. Science 275: 967–969.
Google Scholar
Reed, J.C. 1999. Dysregulation of apoptosis in cancer. J. Clin. Oncol. 17: 2941–2953.
Google Scholar
Reed, J.C. 2008. Bcl-2 family proteins and hematologic malignancies: history and future prospects. Blood. 111: 3322–3330.
Google Scholar
Rodolfo C., Piacentini M. 2002. Does cytoskeleton `Akt' in apoptosis? Cell. Death Differ. 9: 477–478.
Google Scholar
Rogalińska, M., Błoński, J.Z., Komina, O., Góralski, P., Żołnierczyk, J.D., Piekarski, H., Robak, T., Kiliańska, Z.M., Wesierska-Gadek, J. 2010. R-roscovitine (Seliciclib) affects CLL cells more strongly than combinations of fludarabine or cladribine with cyclophosphamide: Inhibition of CDK7 sensitizes leukemic cells to caspase-dependent apoptosis. J. Cell. Biochem. 76: 11–18.
Google Scholar
Savaraj, N., You, M., Wu, C., Wangpaichitr, M., Kuo, M.T., Feun, L.G. 2010. Arginine deprivation, autophagy, apoptosis (AAA) for the treatment of melanoma. Curr. Mol. Med. 10: 405–412.
Google Scholar
Schinzel, A., Kaufmann, T., Borner, C. 2004a. Bcl-2 family members: integrators of survival and death signals in physiology and pathology [corrected]. Biochim. Biophys. Acta. 1644: 95–105.
Google Scholar
Schinzel, A., Kaufmann ,T., Schuler, M., Martinalbo, J., Grubb, D., Borner, C. 2004b. Conformational control of Bax localization and apoptotic activity by Pro168. J. Cell. Biol. 164: 1021–1032.
Google Scholar
Schlesinger, P.H., Saito, M. 2006. The Bax pore in liposomes. Biophysics. Cell. Death Differ.13: 1403–1408.
Google Scholar
Schröder, M. 2008. Endoplasmic reticulum stress responses. Cell. Mol. Life Sci. 65: 862–894.
Google Scholar
Seo, E., Kim, S., Jho, E.H. 2009. Induction of cancer cell-specific death via MMP2 promoter-dependent Bax expression. B. M. B. Rep. 42: 217–222.
Google Scholar
Shan, Y.X., Liu, T.J., Su, H.F., Samsamshariat, A., Mestril, R., Wang, P.H. 2003. Hsp10 and Hsp60 modulate Bcl-2 family and mitochondria apoptosis signaling induced by doxorubicin in cardiac muscle cells. J. Mol. Cell. Cardiol. 35: 1135–1143.
Google Scholar
Sharpe, J.C., Arnoult, D., Youle, R.J. 2004. Control of mitochondrial permeability by Bcl-2 family members. Biochem. Biophys. Acta 1644: 107–113.
Google Scholar
Skommer, J., Wlodkowic, D., Deptala, A. 2007. Larger than life: mitochondria and the Bcl-2 family. Leuk. Res. 31: 277–286.
Google Scholar
Suzuki, M., Youle, R.J., Tjandra, N. 2000. Structure of Bax: coregulation of dimer formation and intracellular localization. Cell 103: 645–654.
Google Scholar
Takahashi, Y., Karbowski, M., Yamaguchi, H., Kazi, A., Wu, J., Sebti, S.M., Youle, R.J., Wang, H.G. 2005. Loss of Bif-1 suppresses Bax/Bak conformational change and mitochondria apoptosis. Mol. Cell. Biol. 25: 9369–9382.
Google Scholar
Terrones, O., Antonsson, B., Yamaguchi, H., Wang, H.G., Liu, J., Lee, R.M., Herrmann, A., Basañez, G. 2004. Lipidic pore formation by the concerted action of proapoptotic Bax and tBid. J. Biol. Chem. 279: 30081–30091.
Google Scholar
Wagener, C., Bargou, C., Daniel, P.T., Bommert, K., Mapara, M.Y., Royer, H.D., Dörken, B. 1996. Induction of the death-promoting gene bax-α sensitizes cultured breast-cancer cells to drug-induced apoptosis. Int. J. Cancer 67: 138–141.
Google Scholar
Warr, M.R., Shore, G.C. 2008. Small-molecule Bcl-2 antagonists as targeted therapy in oncology. Curr. Oncol. 15: 256–261.
Google Scholar
Wei, M.C., Lindsten, T., Mootha V.K, Weiler, S., Gross, A., Ashiya, M., Thompson, C.B., Korsmeyer, S.J., 2000. tBid, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev. 14: 2060–2071.
Google Scholar
Wyllie, A.H. 2010. “Where, o death, is thy sting?” A brief review of apoptosis biology. Mol. Neurobiol. 42: 4–10.
Google Scholar
Xu, Q., Reed, J.C., 1998, Bax inhibitor-1, a mammalian apoptosis suppressor identified by functional screening in yeast. Mol. Cell. 1: 337–346.
Google Scholar
Yan, N., Shi, Y. 2003. Histone H1.2 as a trigger for apoptosis. Nat. Struct. Biol. 10: 983–985.
Google Scholar
Yedavalli, V.S., Shih, H.M., Chiang, Y.P., Lu, C.Y., Chang, L.Y., Chen, M.Y., Chuang, C.Y., Dayton, A.I., Jeang, K.T., Huang, L.M. 2005. Human immunodeficiency virus type 1 Vpr interacts with antiapoptotic mitochondrial protein HAX1, J. Virol. 79: 13735–13746.
Google Scholar
Yousefi, S., Perozzo R., Schmid, I., Ziemiecki, A., Schaffner, T., Scapozza, L., Brunner, T., Simon, H.U. 2006. Calpain-mediated cleavage of Atg5 switches autophagy to apoptosis. Nat. Cell. Biol. 8: 1124–1132.
Google Scholar
Zamzami, N., Hamel, E., Maisse, C., Brenner, C., Muñoz-Pinedo, C., Balzacq, A.S., Costantini, P., Vieira, H., Loeffler, M., Molle, G., Kroemer, G. 2000. Bid acts on the permeability transition pore complex to induce apoptosis. Oncogene 19: 6342–6350.
Google Scholar
Zhai, D., Luciano, F., Zhu, X., Guo, B., Satterthwait, A.C., Reed, J.C. 2005. Humanin binds and nullifies Bid activity by blocking its activation of Bax and Bak. J. Biol. Chem. 280: 15815–15824.
Google Scholar
Żołnierczyk, J.D., Błoński, J.Z., Robak, T., Kiliańska, Z.M., Wesierska-Gadek, J. 2009. Roscovitine triggers apoptosis in B-cell chronic lymphocytic leukemia cells with similar efficiency as combinations of conventional purine analogs with cyclophosphamide. Ann. N.Y. Acad. Sci. 1171: 124–131.
Google Scholar
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