Mitochondrial intermembrane proteins in cell death

Biochemical and Biophysical Research Communications

Volumn 304, Issue 3, 2003, Pages 487-497

  Van Gurp, Maria ^a   Festjens, Nele ^a   Van Loo, Geert ^a,b   Saelens, Xavier ^a   Vandenabeele, Peter ^a  

^a GHENT UNIVERSITY   (Belgium)

^b EUROPEAN MOLECULAR BIOLOGY LABORATORY EMBL   (Italy)

Author keywords

Acyl CoA binding protein; AIF; Apoptosis; Caspase; Cytochrome c; Endonuclease G; Mitochondria; Omi HtrA2; Smac DIABLO

Indexed keywords

ACYL COENZYME A BINDING PROTEIN; ADENINE NUCLEOTIDE TRANSLOCASE; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ADENYLATE KINASE; ADENYLATE KINASE 2; APOPTOSIS INDUCING FACTOR; BINDING PROTEIN; CARDIOLIPIN; CASEIN KINASE I; CASEIN KINASE II; CYTOCHROME C; ENDONUCLEASE; ENDONUCLEASE G; MEMBRANE PROTEIN; MITOCHONDRIAL PROTEIN; POLYPYRIMIDINE TRACT BINDING PROTEIN; PROTEIN BAD; PROTEIN BAK; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BCL XL; PROTEIN BID; PROTEIN KINASE B; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; SECOND MITOCHONDRIAL ACTIVATOR OF CASPASE; SERINE PROTEINASE OMI; UNCLASSIFIED DRUG; VOLTAGE GATED CHANNEL FORMING PROTEIN;

AMINO ACID SEQUENCE; APOPTOSIS; ARTICLE; CELL DEATH; DNA DEGRADATION; EVOLUTION; HUMAN; MEMBRANE PERMEABILITY; MITOCHONDRIAL MEMBRANE; MOLECULAR MECHANICS; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SECRETION; SEQUENCE HOMOLOGY;

EID: 0037427444     PISSN: 0006291X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-291X(03)00621-1     Document Type: Article

References (93)

1. Ameisen J.C. On the origin, evolution, and nature of programmed cell death: a timeline of four billion years. Cell Death Differ. 9:2002;367-393.
2. Clarke P.G. Apoptosis: from morphological types of cell death to interacting pathways. Trends Pharmacol. Sci. 23:2002;308-309.
3. Li P., Nijhawan D., Budihardjo I., Srinivasula S.M., Ahmad M., Alnemri E.S., Wang X. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell. 91:1997;479-489.
4. Loud A.V. A quantitative stereological description of the ultrastructure of normal rat liver parenchymal cells. J. Cell Biol. 37:1968;27-46.
5. Crompton M. The mitochondrial permeability transition pore and its role in cell death. Biochem. J. 341:1999;233-249.
6. Martinou J.C., Green D.R. Breaking the mitochondrial barrier. Nat. Rev. Mol. Cell. Biol. 2:2001;63-67.
7. Zamzami N., Kroemer G. The mitochondrion in apoptosis: how Pandora's box opens. Nat. Rev. Mol. Cell. Biol. 2:2001;67-71.
8. Schendel S.L., Azimov R., Pawlowski K., Godzik A., Kagan B.L., Reed J.C. Ion channel activity of the BH3 only Bcl-2 family member, BID. J. Biol. Chem. 274:1999;21932-21936.
9. Fesik S.W. Insights into programmed cell death through structural biology. Cell. 103:2000;273-282.
10. Eskes R., Desagher S., Antonsson B., Martinou J.C. Bid induces the oligomerization and insertion of Bax into the outer mitochondrial membrane. Mol. Cell. Biol. 20:2000;929-935.
11. Suzuki M., Youle R.J., Tjandra N. Structure of Bax: coregulation of dimer formation and intracellular localization. Cell. 103:2000;645-654.
12. Wei M.C., Zong W.X., Cheng E.H., Lindsten T., Panoutsakopoulou V., Ross A.J., Roth K.A., MacGregor G.R., Thompson C.B., Korsmeyer S.J. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science. 292:2001;727-730.
13. Puthalakath H., Huang D.C., O'Reilly L.A., King S.M., Strasser A. The proapoptotic activity of the Bcl-2 family member Bim is regulated by interaction with the dynein motor complex. Mol. Cell. 3:1999;287-296.
14. Soane L., Cho H.J., Niculescu F., Rus H., Shin M.L. C5b-9 terminal complement complex protects oligodendrocytes from death by regulating Bad through phosphatidylinositol 3-kinase/Akt pathway. J. Immunol. 167:2001;2305-2311.
15. Esposti M.D. The roles of Bid. Apoptosis. 7:2002;433-440.
16. Wang K., Yin X.M., Chao D.T., Milliman C.L., Korsmeyer S.J. BID: a novel BH3 domain-only death agonist. Genes Dev. 10:1996;2859-2869.
17. Grinberg M., Sarig R., Zaltsman Y., Frumkin D., Grammatikakis N., Reuveny E., Gross A. tBID Homooligomerizes in the mitochondrial membrane to induce apoptosis. J. Biol. Chem. 277:2002;12237-12245.
18. Barry M., Heibein J.A., Pinkoski M.J., Lee S.F., Moyer R.W., Green D.R., Bleackley R.C. Granzyme B short-circuits the need for caspase 8 activity during granule-mediated cytotoxic T-lymphocyte killing by directly cleaving Bid. Mol. Cell. Biol. 20:2000;3781-3794.
19. Stoka V., Turk B., Schendel S.L., Kim T.H., Cirman T., Snipas S.J., Ellerby L.M., Bredesen D., Freeze H., Abrahamson M., Bromme D., Krajewski S., Reed J.C., Yin X.M., Turk V., Salvesen G.S. Lysosomal protease pathways to apoptosis. Cleavage of bid, not pro- caspases, is the most likely route. J. Biol. Chem. 276:2001;3149-3157.
20. Chen M., He H., Zhan S., Krajewski S., Reed J.C., Gottlieb R.A. Bid is cleaved by calpain to an active fragment in vitro and during myocardial ischemia/reperfusion. J. Biol. Chem. 276:2001;30724-30728.
21. Kuwana T., Mackey M.R., Perkins G., Ellisman M.H., Latterich M., Schneiter R., Green D.R., Newmeyer D.D. Bid, Bax, and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane. Cell. 111:2002;331-342.
22. Gross A., Yin X.M., Wang K., Wei M.C., Jockel J., Milliman C., Erdjument-Bromage H., Tempst P., Korsmeyer S.J. Caspase cleaved BID targets mitochondria and is required for cytochrome c release, while BCL-XL prevents this release but not tumor necrosis factor-R1/Fas death. J. Biol. Chem. 274:1999;1156-1163.
23. Desagher S., Osen-Sand A., Montessuit S., Magnenat E., Vilbois F., Hochmann A., Journot L., Antonsson B., Martinou J.C. Phosphorylation of bid by casein kinases I and II regulates its cleavage by caspase 8. Mol. Cell. 8:2001;601-611.
24. Ito T., Deng X., Carr B., May W.S. Bcl-2 phosphorylation required for anti-apoptosis function. J. Biol. Chem. 272:1997;11671-11673.
25. Oda E., Ohki R., Murasawa H., Nemoto J., Shibue T., Yamashita T., Tokino T., Taniguchi T., Tanaka N. Noxa, a BH3-only member of the Bcl-2 family and candidate mediator of p53-induced apoptosis. Science. 288:2000;1053-1058.
26. Fei P., Bernhard E.J., El-Deiry W.S. Tissue-specific induction of p53 targets in vivo. Cancer Res. 62:2002;7316-7327.
27. Van Loo G., Demol H., van Gurp M., Hoorelbeke B., Schotte P., Beyaert R., Zhivotovsky B., Gevaert K., Declercq W., Vandekerckhove J., Vandenabeele P. A matrix-assisted laser desorption ionization post-source decay (MALDI- PSD) analysis of proteins released from isolated liver mitochondria treated with recombinant truncated Bid. Cell Death Differ. 9:2002;301-308.
28. Patterson S.D., Spahr C.S., Daugas E., Susin S.A., Irinopoulou T., Koehler C., Kroemer G. Mass spectrometric identification of proteins released from mitochondria undergoing permeability transition. Cell Death Differ. 7:2000;137-144.
29. Spahr C.S., Susin S.A., Bures E.J., Robinson J.H., Davis M.T., McGinley M.D., Kroemer G., Patterson S.D. Simplification of complex peptide mixtures for proteomic analysis: reversible biotinylation of cysteinyl peptides. Electrophoresis. 21:2000;1635-1650.
30. Winkler H.H., Lehninger A.L. The atractyloside-sensitive nucleotide binding site in a membrane preparation from rat liver mitochondria. J. Biol. Chem. 243:1968;3000-3008.
31. Keilin D. Cytochrome and intracellular oxidase. Proc. R. Soc. Lond. B. 106:1930;418-444.
32. Zhivotovsky B., Hanson K.P., Orrenius S. Back to the future: the role of cytochrome c in cell death. Cell Death Differ. 5:1998;459-460.
33. Kluck R.M., Ellerby L.M., Ellerby H.M., Naiem S., Yaffe M.P., Margoliash E., Bredesen D., Mauk A.G., Sherman F., Newmeyer D.D. Determinants of cytochrome c pro-apoptotic activity. The role of lysine 72 trimethylation. J. Biol. Chem. 275:2000;16127-16133.
34. Yang X., Chang H.Y., Baltimore D. Essential role of CED-4 oligomerization in CED-3 activation and apoptosis. Science. 281:1998;1355-1357.
35. Acehan D., Jiang X., Morgan D.G., Heuser J.E., Wang X., Akey C.W. Three-dimensional structure of the apoptosome: implications for assembly, procaspase-9 binding, and activation. Mol. Cell. 9:2002;423-432.
36. Li K., Li Y., Shelton J.M., Richardson J.A., Spencer E., Chen Z.J., Wang X., Williams R.S. Cytochrome c deficiency causes embryonic lethality and attenuates stress-induced apoptosis. Cell. 101:2000;389-399.
37. Adams J.M., Cory S. Apoptosomes: engines for caspase activation. Curr. Opin. Cell Biol. 14:2002;715-720.
38. Joza N., Susin S.A., Daugas E., Stanford W.L., Cho S.K., Li C.Y., Sasaki T., Elia A.J., Cheng H.Y., Ravagnan L., Ferri K.F., Zamzami N., Wakeham A., Hakem R., Yoshida H., Kong Y.Y., Mak T.W., Zuniga-Pflucker J.C., Kroemer G., Penninger J.M. Essential role of the mitochondrial apoptosis-inducing factor in programmed cell death. Nature. 410:2001;549-554.
39. Marsden V.S., O'Connor L., O'Reilly L.A., Silke J., Metcalf D., Ekert P.G., Huang D.C., Cecconi F., Kuida K., Tomaselli K.J., Roy S., Nicholson D.W., Vaux D.L., Bouillet P., Adams J.M., Strasser A. Apoptosis initiated by Bcl-2-regulated caspase activation independently of the cytochrome c/Apaf-1/caspase-9 apoptosome. Nature. 419:2002;634-637.
40. Ogilvy S., Metcalf D., Print C.G., Bath M.L., Harris A.W., Adams J.M. Constitutive Bcl-2 expression throughout the hematopoietic compartment affects multiple lineages and enhances progenitor cell survival. Proc. Natl. Acad. Sci. USA. 96:1999;14943-14948.
41. Abdullaev Z., Bodrova M.E., Chernyak B.V., Dolgikh D.A., Kluck R.M., Pereverzev M.O., Arseniev A.S., Efremov R.G., Kirpichnikov M.P., Mokhova E.N., Newmeyer D.D., Roder H., Skulachev V.P. A cytochrome c mutant with high electron transfer and antioxidant activities but devoid of apoptogenic effect. Biochem. J. 362:2002;749-754.
42. Rodriguez A., Oliver H., Zou H., Chen P., Wang X., Abrams J.M. Dark is a Drosophila homologue of Apaf-1/CED-4 and functions in an evolutionarily conserved death pathway. Nat. Cell Biol. 1:1999;272-279.
43. Dorstyn L., Read S., Cakouros D., Huh J.R., Hay B.A., Kumar S. The role of cytochrome c in caspase activation in Drosophila melanogaster cells. J. Cell Biol. 156:2002;1089-1098.
44. Varkey J., Chen P., Jemmerson R., Abrams J.M. Altered cytochrome c display precedes apoptotic cell death in Drosophila. J. Cell Biol. 144:1999;701-710.
45. Cande C., Cecconi F., Dessen P., Kroemer G. Apoptosis-inducing factor (AIF): key to the conserved caspase-independent pathways of cell death? J. Cell Sci. 115:2002;4727-4734.
46. Yu S.W., Wang H., Poitras M.F., Coombs C., Bowers W.J., Federoff H.J., Poirier G.G., Dawson T.M., Dawson V.L. Mediation of poly(ADP-ribose) polymerase-1-dependent cell death by apoptosis-inducing factor. Science. 297:2002;259-263.
47. Susin S.A., Daugas E., Ravagnan L., Samejima K., Zamzami N., Loeffler M., Costantini P., Ferri K.F., Irinopoulou T., Prevost M.C., Brothers G., Mak T.W., Penninger J., Earnshaw W.C., Kroemer G. Two distinct pathways leading to nuclear apoptosis. J. Exp. Med. 192:2000;571-580.
48. Ravagnan L., Gurbuxani S., Susin S.A., Maisse C., Daugas E., Zamzami N., Mak T., Jaattela M., Penninger J.M., Garrido C., Kroemer G. Heat-shock protein 70 antagonizes apoptosis-inducing factor. Nat. Cell Biol. 3:2001;839-843.
49. Klein J.A., Longo-Guess C.M., Rossmann M.P., Seburn K.L., Hurd R.E., Frankel W.N., Bronson R.T., Ackerman S.L. The harlequin mouse mutation downregulates apoptosis-inducing factor. Nature. 419:2002;367-374.
50. Mate M.J., Ortiz-Lombardia M., Boitel B., Haouz A., Tello D., Susin S.A., Penninger J., Kroemer G., Alzari P.M. The crystal structure of the mouse apoptosis-inducing factor AIF. Nat. Struct. Biol. 9:2002;442-446.
51. Miramar M.D., Costantini P., Ravagnan L., Saraiva L.M., Haouzi D., Brothers G., Penninger J.M., Peleato M.L., Kroemer G., Susin S.A. NADH oxidase activity of mitochondrial apoptosis-inducing factor. J. Biol Chem. 276:2001;16391-16398.
52. Wang X., Yang C., Chai J., Shi Y., Xue D. Mechanisms of AIF-mediated apoptotic DNA degradation in Caenorhabditis elegans. Science. 298:2002;1587-1592.
53. van Loo G., Saelens X., Matthijssens F., Schotte P., Beyaert R., Declercq W., Vandenabeele P. Caspases are not localized in mitochondria during life or death. Cell Death Differ. 9:2002;1207-1211.
54. Wu M., Xu L.G., Li X., Zhai Z., Shu H.B. AMID, an apoptosis-inducing factor-homologous mitochondrion-associated protein, induces caspase-independent apoptosis. J. Biol. Chem. 277:2002;25617-25623.
55. Ohsato T., Ishihara N., Muta T., Umeda S., Ikeda S., Mihara K., Hamasaki N., Kang D. Mammalian mitochondrial endonuclease G. Digestion of R-loops and localization in intermembrane space. Eur. J. Biochem. 269:2002;5765-5770.
56. Li L.Y., Luo X., Wang X. Endonuclease G is an apoptotic DNase when released from mitochondria. Nature. 412:2001;95-99.
57. 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., Vandenabeele P. Endonuclease G: a mitochondrial protein released in apoptosis and involved in caspase-independent DNA degradation. Cell Death Differ. 8:2001;1136-1142.
58. Widlak P., Li L.Y., Wang X., Garrard W.T. Action of recombinant human apoptotic endonuclease G on naked DNA and chromatin substrates: cooperation with exonuclease and DNase I. J. Biol. Chem. 276:2001;48404-48409.
59. Sakahira H., Enari M., Nagata S. Cleavage of CAD inhibitor in CAD activation and DNA degradation during apoptosis. Nature. 391:1998;96-99.
60. McIlroy D., Tanaka M., Sakahira H., Fukuyama H., Suzuki M., Yamamura K., Ohsawa Y., Uchiyama Y., Nagata S. An auxiliary mode of apoptotic DNA fragmentation provided by phagocytes. Genes Dev. 14:2000;549-558.
61. Samejima K., Tone S., Earnshaw W.C. CAD/DFF40 nuclease is dispensable for high molecular weight DNA cleavage and stage I chromatin condensation in apoptosis. J. Biol. Chem. 276:2001;45427-45432.
62. Susin S.A., Lorenzo H.K., Zamzami N., Marzo I., Snow B.E., Brothers G.M., Mangion J., Jacotot E., Costantini P., Loeffler M., Larochette N., Goodlett D.R., Aebersold R., Siderovski D.P., Penninger J.M., Kroemer G. Molecular characterization of mitochondrial apoptosis-inducing factor. Nature. 397:1999;441-446.
63. Parrish J., Li L., Klotz K., Ledwich D., Wang X., Xue D. Mitochondrial endonuclease G is important for apoptosis in C. elegans. Nature. 412:2001;90-94.
64. Denecker G., Vercammen D., Declercq W., Vandenabeele P. Apoptotic and necrotic cell death induced by death domain receptors. Cell. Mol. Life Sci. 58:2001;356-370.
65. Deveraux Q.L., Roy N., Stennicke H.R., Van Arsdale T., Zhou Q., Srinivasula S.M., Alnemri E.S., Salvesen G.S., Reed J.C. IAPs block apoptotic events induced by caspase-8 and cytochrome c by direct inhibition of distinct caspases. EMBO J. 17:1998;2215-2223.
66. Verhagen A.M., Ekert P.G., Pakusch M., Silke J., Connolly L.M., Reid G.E., Moritz R.L., Simpson R.J., Vaux D.L. Identification of DIABLO, a mammalian protein that promotes apoptosis by binding to and antagonizing IAP proteins. Cell. 102:2000;43-53.
67. Du C., Fang M., Li Y., Li L., Wang X. Smac, a mitochondrial protein that promotes cytochrome c-dependent caspase activation by eliminating IAP inhibition. Cell. 102:2000;33-42.
68. Wu G., Chai J., Suber T.L., Wu J.W., Du C., Wang X., Shi Y. Structural basis of IAP recognition by Smac/DIABLO. Nature. 408:2000;1008-1012.
69. Srinivasula S.M., Hegde R., Saleh A., Datta P., Shiozaki E., Chai J., Lee R.A., Robbins P.D., Fernandes-Alnemri T., Shi Y., Alnemri E.S. A conserved XIAP-interaction motif in caspase-9 and Smac/DIABLO regulates caspase activity and apoptosis. Nature. 410:2001;112-116.
70. Chai J., Shiozaki E., Srinivasula S.M., Wu Q., Datta P., Alnemri E.S., Shi Y., Dataa P. Structural basis of caspase-7 inhibition by XIAP. Cell. 104:2001;769-780.
71. Roberts D.L., Merrison W., MacFarlane M., Cohen G.M. The inhibitor of apoptosis protein-binding domain of Smac is not essential for its proapoptotic activity. J. Cell Biol. 153:2001;221-228.
72. Meier P., Silke J., Leevers S.J., Evan G.I. The Drosophila caspase DRONC is regulated by DIAP1. EMBO J. 19:2000;598-611.
73. Goyal L., McCall K., Agapite J., Hartwieg E., Steller H. Induction of apoptosis by Drosophila reaper, hid and grim through inhibition of IAP function. EMBO J. 19:2000;589-597.
74. Wing J.P., Karres J.S., Ogdahl J.L., Zhou L., Schwartz L.M., Nambu J.R. Drosophila sickle is a novel grim-reaper cell death activator. Curr. Biol. 12:2002;131-135.
75. Wang S.L., Hawkins C.J., Yoo S.J., Muller H.A., Hay B.A. The Drosophila caspase inhibitor DIAP1 is essential for cell survival and is negatively regulated by HID. Cell. 98:1999;453-463.
76. Wu J.W., Cocina A.E., Chai J., Hay B.A., Shi Y. Structural analysis of a functional DIAP1 fragment bound to grim and hid peptides. Mol. Cell. 8:2001;95-104.
77. Christich A., Kauppila S., Chen P., Sogame N., Ho S.I., Abrams J.M. The damage-responsive Drosophila gene sickle encodes a novel IAP binding protein similar to but distinct from reaper, grim, hid. Curr. Biol. 12:2002;137-140.
78. Gray C.W., Ward R.V., Karran E., Turconi S., Rowles A., Viglienghi D., Southan C., Barton A., Fantom K.G., West A., Savopoulos J., Hassan N.J., Clinkenbeard H., Hanning C., Amegadzie B., Davis J.B., Dingwall C., Livi G.P., Creasy C.L. Characterization of human HtrA2, a novel serine protease involved in the mammalian cellular stress response. Eur. J. Biochem. 267:2000;5699-5710.
79. Faccio L., Fusco C., Chen A., Martinotti S., Bonventre J.V., Zervos A.S. Characterization of a novel human serine protease that has extensive homology to bacterial heat shock endoprotease HtrA and is regulated by kidney ischemia. J. Biol. Chem. 275:2000;2581-2588.
80. Spiess C., Beil A., Ehrmann M. A temperature-dependent switch from chaperone to protease in a widely conserved heat shock protein. Cell. 97:1999;339-347.
81. Suzuki Y., Imai Y., Nakayama H., Takahashi K., Takio K., Takahashi R. A serine protease, HtrA2, is released from the mitochondria and interacts with XIAP, inducing cell death. Mol. Cell. 8:2001;613-621.
82. Verhagen A.M., Silke J., Ekert P.G., Pakusch M., Kaufmann H., Connolly L.M., Day C.L., Tikoo A., Burke R., Wrobel C., Moritz R.L., Simpson R.J., Vaux D.L. HtrA2 promotes cell death through its serine protease activity and its ability to antagonize inhibitor of apoptosis proteins. J. Biol. Chem. 277:2002;445-454.
83. Costantini P., Jacotot E., Decaudin D., Kroemer G. Mitochondrion as a novel target of anticancer chemotherapy. J. Natl. Cancer Inst. 92:2000;1042-1053.
84. Savopoulos J.W., Carter P.S., Turconi S., Pettman G.R., Karran E.H., Gray C.W., Ward R.V., Jenkins O., Creasy C.L. Expression, purification, functional analysis of the human serine protease HtrA2. Protein Expr. Purif. 19:2000;227-234.
85. van Loo G., van Gurp M., Depuydt B., Srinivasula S.M., Rodriguez I., Alnemri E.S., Gevaert K., Vandekerckhove J., Declercq W., Vandenabeele P. The serine protease Omi/HtrA2 is released from mitochondria during apoptosis. Omi interacts with caspase-inhibitor XIAP and induces enhanced caspase activity. Cell Death Differ. 9:2002;20-26.
86. Hegde R., Srinivasula S.M., Zhang Z., Wassell R., Mukattash R., Cilenti L., DuBois G., Lazebnik Y., Zervos A.S., Fernandes-Alnemri T., Alnemri E.S. Identification of Omi/HtrA2 as a mitochondrial apoptotic serine protease that disrupts inhibitor of apoptosis protein-caspase interaction. J. Biol. Chem. 277:2002;432-438.
87. Li W., Srinivasula S.M., Chai J., Li P., Wu J.W., Zhang Z., Alnemri E.S., Shi Y. Structural insights into the pro-apoptotic function of mitochondrial serine protease HtrA2/Omi. Nat. Struct. Biol. 9:2002;436-441.
88. Melloni E., Averna M., Salamino F., Sparatore B., Minafra R., Pontremoli S. Acyl-CoA-binding protein is a potent m-calpain activator. J. Biol. Chem. 275:2000;82-86.
89. Wang K.K. Calpain and caspase: can you tell the difference? Trends Neurosci. 23:2000;20-26.
90. Gosert R., Chang K.H., Rijnbrand R., Yi M., Sangar D.V., Lemon S.M. Transient expression of cellular polypyrimidine-tract binding protein stimulates cap-independent translation directed by both picornaviral and flaviviral internal ribosome entry sites In vivo. Mol. Cell. Biol. 20:2000;1583-1595.
91. Kamath R.V., Leary D.J., Huang S. Nucleocytoplasmic shuttling of polypyrimidine tract-binding protein is uncoupled from RNA export. Mol. Biol. Cell. 12:2001;3808-3820.
92. Mitchell S.A., Brown E.C., Coldwell M.J., Jackson R.J., Willis A.E. Protein factor requirements of the Apaf-1 internal ribosome entry segment: roles of polypyrimidine tract binding protein and upstream of N-ras. Mol. Cell. Biol. 21:2001;3364-3374.
93. Denecker G., Vercammen D., Steemans M., Vanden Berghe T., Brouckaert G., Van Loo G., Zhivotovsky B., Fiers W., Grooten J., Declercq W., Vandenabeele P. Death receptor-induced apoptotic and necrotic cell death: differential role of caspases and mitochondria. Cell Death Differ. 8:2001;829-840.