The chemical biology of apoptosis: Exploring protein-protein interactions and the life and death of cells with small molecules

Chemistry and Biology

Volumn 9, Issue 10, 2002, Pages 1059-1072

  Huang, Ziwei ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CASPASE; LIGAND; PROTEIN BCL 2;

AMINO ACID SEQUENCE; ANIMAL; APOPTOSIS; BINDING SITE; BIOLOGICAL MODEL; CELL SURVIVAL; CHEMICAL STRUCTURE; DRUG ANTAGONISM; GENETICS; HUMAN; METABOLISM; MITOCHONDRION; MOLECULAR GENETICS; PHYSIOLOGY; PROTEIN BINDING; PROTEIN TERTIARY STRUCTURE; REVIEW; SEQUENCE ALIGNMENT;

AMINO ACID SEQUENCE; ANIMALS; APOPTOSIS; BINDING SITES; CASPASES; CELL SURVIVAL; HUMANS; LIGANDS; MITOCHONDRIA; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PROTO-ONCOGENE PROTEINS C-BCL-2; SEQUENCE ALIGNMENT;

ANIMALIA;

EID: 0036773678     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1074-5521(02)00247-8     Document Type: Review

References (110)

1. Wyllie A.H., Kerr J.F., Currie A.R. Cell death. the significance of apoptosis Int. Rev. Cytol. 68:1980;251-306.
2. Thompson C.B. Apoptosis in the pathogenesis and treatment of disease. Science. 267:1995;1456-1462.
3. Alnemri E.S., Livingston D.J., Nicholson D.W., Salvesen G., Thornberry N.A., Wong W.W., Yuan J. Human ICE/CED-3 protease nomenclature. Cell. 87:1996;171.
4. Thornberry N., Lazebnik Y. Caspases. enemies within Science. 281:1998;1312-1316.
5. Green D.R., Reed J.C. Mitochondria and apoptosis. Science. 281:1998;1309-1312.
6. Ashkenazi A., Dixit V.M. Death receptors. signaling and modulation Science. 281:1998;1305-1308.
7. Peczuh M.W., Hamilton A.D. Peptide and protein recognition by designed molecules. Chem. Rev. 100:2000;2479-2494.
8. Cochran A.G. Protein-protein interfaces. mimics and inhibitors Curr. Opin. Chem. Biol. 5:2001;654-659.
9. Adams J., Cory S. The Bcl-2 protein family. arbiters of cell survival Science. 281:1998;1322-1326.
10. Chao D., Korsmeyer S. Bcl-2 family. regulators of cell death Annu. Rev. Immunol. 16:1998;395-419.
11. Vaux D.L., Korsmeyer S.J. Cell death in development. Cell. 96:1999;245-254.
12. Adams J.M., Cory S. Life-or-death decisions by the Bcl-2 protein family. Trends Biochem. Sci. 25:2001;61-66.
13. Hengartner M.O. The biochemistry of apoptosis. Nature. 407:2000;770-776.
14. Zimmermann K.C., Bonzon C., Green D.R. The machinery of programmed cell death. Pharmacol. Ther. 92:2001;57-70.
15. Budihardjo I., Oliver H., Lutter M., Luo X., Wang X. Biochemical pathways of caspase activation during apoptosis. Annu. Rev. Cell Dev. Biol. 15:1999;269-290.
16. Wyllie A.H. Apoptosis and carcinogenesis. Eur. J. Cell Biol. 73:1997;189-197.
17. Reed J.C., Miyashita T., Takayama S., Wang H.G., Sato T., Krajewski S., Aime-Sempe C., Bodrug S., Kitada S., Hanada M. BCL-2 family proteins. regulators of cell death involved in the pathogenesis of cancer and resistance to therapy J. Cell. Biochem. 60:1996;23-32.
18. Mattson M.P. Apoptosis in neurodegenerative disorders. Nat. Rev. Mol. Cell Biol. 1:2000;120-129.
19. Andreeff M., Goodrich D.W., Pardee A.B. Chapter 2. Cell Proliferation, Differentiation and Apoptosis:2000;B.C. Decker, Inc, Hamilton, Ontario, Canada.
20. Fesik S.W. Insights into programmed cell death through structural biology. Cell. 103:2000;273-282.
21. Shi Y. A structural view of mitochondria-mediated apoptosis. Nat. Struct. Biol. 8:2001;394-401.
22. Petros A.M., Medek A., Nettesheim D.G., Kim D.H., Yoon H.S., Swift K., Matayoshi E.D., Oltersdorf T., Fesik S.W. Solution structure of the antiapoptotic protein bcl-2. Proc. Natl. Acad. Sci. USA. 98:2001;3012-3017.
23. L, an inhibitor of programmed cell death. Nature. 381:1996;335-341.
24. L. Implications for the function of the Bcl-2 protein family. J. Biol. Chem. 272:1997;27886-27892.
25. Suzuki M., Youle R.J., Tjandra N. Structure of Bax. coregulation of dimer formation and intracellular localization Cell. 103:2000;645-654.
26. McDonnell J.M., Fushman D., Milliman C.L., Korsmeyer S.J., Cowburn D. Solution structure of the proapoptotic molecule BID. a structural basis for apoptotic agonists and antagonists Cell. 96:1999;625-634.
27. Chou J.J., Li H., Salvesen G.S., Yuan J., Wagner G. Solution structure of BID, an intracellular amplifier of apoptotic signaling. Cell. 96:1999;615-624.
28. L and Bcl-2, displaces Bax and promotes cell death. Cell. 80:1995;285-291.
29. Oltvai Z.N., Milliman C.L., Korsmeyer S.J. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell. 74:1993;609-619.
30. L-Bak peptide complex. recognition between regulators of apoptosis Science. 275:1997;983-986.
31. Desagher S., Osen-Sand A., Nichols A., Eskes R., Montessuit S., Lauper S., Maundrell K., Antonsson B., Martinou J.C. Bid-induced conformational change of Bax is responsible for mitochondrial cytochrome c release during apoptosis. J. Cell Biol. 144:1999;891-901.
32. L. Cell. 87:1996;619-628.
33. Slee E.A., Keogh S.A., Martin S.J. Cleavage of BID during cytotoxic drug and UV radiation-induced apoptosis occurs downstream of the point of Bcl-2 action and is catalysed by caspase-3. a potential feedback loop for amplification of apoptosis-associated mitochondrial cytochrome c release Cell Death Differ. 95:2000;556-565.
34. Li H., Zhu H., Xu C.J., Yuan J. Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell. 94:1998;491-501.
35. Luo X., Budihardjo I., Zou H., Slaughter C., Wang X. Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell. 94:1998;481-490.
36. Kelekar A., Thompson C.B. Bcl-2-family proteins. the role of the BH3 domain in apoptosis Trends Cell Biol. 8:1998;324-330.
37. Yin X.M., Oltvai Z.N., Korsmeyer S.J. BH1 and BH2 domains of Bcl-2 are required for inhibition of apoptosis and heterodimerization with Bax. Nature. 369:1994;321-323.
38. Chittenden T., Flemington C., Houghton A.B., Ebb R.G., Gallo G.J., Elangovan B., Chinnadurai G., Lutz R.J. A conserved domain in Bak, distinct from BH1 and BH2, mediates cell death and protein binding functions. EMBO J. 14:1995;5589-5596.
39. Boyd J.M., Gallo G.J., Elangovan B., Houghton A.B., Malstrom S., Avery B.J., Ebb R.G., Subramanian T., Chittenden T., Lutz R.J.et al. Bik, a novel death-inducing protein shares a distinct sequence motif with Bcl-2 family proteins and interacts with viral and cellular survival-promoting proteins. Oncogene. 11:1995;1921-1928.
40. Zha H., Aime-Sempe C., Sato T., Reed J.C. Proapoptotic protein Bax heterodimerizes with Bcl-2 and homodimerizes with Bax via a novel domain (BH3) distinct from BH1 and BH2. J. Biol. Chem. 271:1996;7440-7444.
41. L. Mol. Cell. Biol. 17:1997;7040-7046.
42. L/Bad peptide complex formation from structure, mutagenesis, and biophysical studies. Protein Sci. 9:2000;2528-2534.
43. L proteins. J. Biol. Chem. 272:1997;30866-30872.
44. Diaz J.L., Oltersdorf T., Horne W., McConnell M., Wilson G., Weeks S., Garcia T., Fritz L.C. A common binding site mediates heterodimerization and homodimerization of Bcl-2 family members. J. Biol. Chem. 272:1997;11350-11355.
45. Cosulich S., Worrall V., Hedge P., Green S., Clarke P. Regulation of apoptosis by BH3 domains in a cell-free system. Curr. Biol. 7:1997;913-920.
46. Jurgensmeier J.M., Xie Z., Deveraux Q., Ellerby L., Bredesen D., Reed J.C. Bax directly induces release of cytochrome c from isolated mitochondria. Proc. Natl. Acad. Sci. USA. 95:1998;4997-5002.
47. Narita M., Shimizu S., Ito T., Chittenden T., Lutz R.J., Matsuda H., Tsujimoto Y. Bax interacts with the permeability transition pore to induce permeability transition and cytochrome c release in isolated mitochondria. Proc. Natl. Acad. Sci. USA. 95:1998;14681-14686.
48. Morgan, B.A., Finnegan, N.M., Prevost, G., and Cotter, T.G. (2000). 91st Annual Meeting of the American Association for Cancer Research. 42, 4693.
49. Theodore L., Derossi D., Chassaing G., Llirbat B., Kubes M., Jordan P., Chneiweiss H., Godement P., Prochiantz A. Intraneuronal delivery of protein kinase C pseudosubstrate leads to growth cone collapse. J. Neurosci. 15:1995;7158-7167.
50. Ball K.L., Lain S., Fahraeus R., Smythe C., Lane D.P. Cell-cycle arrest and inhibition of Cdk4 activity by small peptides based on the carboxy-terminal domain of p21WAF1. Curr. Biol. 7:1997;71-80.
51. Bonfanti M., Taverna S., Salmona M., D'Incalci M., Broggini M. p21WAF1-derived peptides linked to an internalization peptide inhibit human cancer cell growth. Cancer Res. 57:1997;1442-1446.
52. Selivanova G., Iotsova V., Okan I., Fritsche M., Strom M., Groner B., Grafstrom R.C., Wiman K.G. Restoration of the growth suppression function of mutant p53 by a synthetic peptide derived from the p53 C-terminal domain. Nat. Med. 3:1997;632-638.
53. Williams E.J., Dunican D.J., Green P.J., Howell F.V., Derossi D., Walsh F.S., Doherty P. Selective inhibition of growth factor-stimulated mitogenesis by a cell-permeable Grb2-binding peptide. J. Biol. Chem. 272:1997;22349-22354.
54. Hall H., Williams E.J., Moore S.E., Walsh F.S., Prochiantz A., Doherty P. Inhibition of FGF-stimulated phosphatidylinositol hydrolysis and neurite outgrowth by a cell-membrane permeable phosphopeptide. Curr. Biol. 6:1996;580-587.
55. L function and induce apoptosis through cytochrome c-independent activation of caspases. J. Biol. Chem. 274:1999;13298-13304.
56. Ioannides C.G., Freedman R.S., Liskamp R.M., Ward N.E., O'Brian C.A. Inhibition of IL-2 receptor induction and IL-2 production in the human leukemic cell line Jurkat by a novel peptide inhibitor of protein kinase C. Cell. Immunol. 131:1990;242-252.
57. Kole H.K., Garant M.J., Kole S., Bernier M. A peptide-based protein-tyrosine phosphatase inhibitor specifically enhances insulin receptor function in intact cells. J. Biol. Chem. 271:1996;14302-14307.
58. Wang J.L., Zhang Z.J., Choksi S., Shan S., Lu Z., Croce C.M., Alnemri E.S., Korngold R., Huang Z. Cell Permeable Bcl-2 Binding Peptides. A Chemical Approach to Apotosis Induction in Tumor Cells Cancer Res. 60:2000;1498-1502.
59. Shimizu S., Konishi A., Kodama T., Tsujimoto Y. BH4 domain of antiapoptotic Bcl-2 family members closes voltage-dependent anion channel and inhibits apoptotic mitochondrial changes and cell death. Proc. Natl. Acad. Sci. USA. 97:2000;3100-3105.
60. Green M., Loewenstein P.M. Autonomous functional domains of chemically synthesized human immunodeficiency virus tat trans-activator protein. Cell. 55:1988;1179-1188.
61. Derossi D., Calvet S., Trembleau A., Brunissen A., Chassaing G., Prochiantz A. Cell internalization of the third helix of the Antennapedia homeodomain is receptor-independent. J. Biol. Chem. 271:1996;18188-18193.
62. Schwarze S.R., Ho A., Vocero-Akbani A., Dowdy S.F. In vivo protein transduction. delivery of a biologically active protein into the mouse Science. 285:1999;1569-1572.
63. Tzung S.P., Kim K.M., Basanez G., Giedt C.D., Simon J., Zimmerberg J., Zhang K.Y., Hockenbery D.M. Antimycin A mimics a cell-death-inducing Bcl-2 homology domain 3. Nat. Cell Biol. 3:2001;183-191.
64. Lugovskoy A.A., Degterev A.I., Fahmy A.F., Zhou P., Gross J.D., Yuan J., Wagner G. A novel approach for characterizing protein ligand complexes. molecular basis for specificity of small-molecule Bcl-2 inhibitors J. Am. Chem. Soc. 124:2002;1234-1240.
65. L. Nat. Cell Biol. 3:2001;173-182.
66. Wang J., Liu D., Zhang Z., Shan S., Han X., Srinivasula S.M., Croce C.M., Alnemri E.S., Huang Z. Structure-based discovery of a novel organic compound that binds Bcl-2 protein and induces apoptosis of tumor cells. Proc. Natl. Acad. Sci. USA. 97:2000;7124-7129.
67. Enyedy I.J., Ling Y., Nacro K., Tomita Y., Wu X., Cao Y., Guo R., Li B., Zhu X., Huang Y.et al. Discovery of small-molecule inhibitors of Bcl-2 through structure-based computer screening. J. Med. Chem. 44:2001;4313-4324.
68. L antagonist based on a-helix mimicry. J. Am. Chem. Soc., in press.
69. Huang Z. Structural chemistry and therapeutic intervention of protein-protein interaction in immune response, HIV entry and apoptosis. Pharmacol. Ther. 86:2000;201-215.
70. Yu N., Aramini J.M., Germann M.W., Huang Z. Reactions of salicylaldehydes with alkyl cyanoacetates on the surface of solid catalysts. syntheses of 4H-chromene derivatives Tetrahedron Lett. 41:2000;6993-6996.
71. Dunshee B.R., Leben C., Keitt G.W., Strong F.M. The isolation and properties of antimycin A. J. Am. Chem. Soc. 71:1949;2436-2437.
72. Tokutake N., Miyoshi H., Satoh T., Hatano T., Iwamura H. Structural factors of antimycin A molecule required for inhibitory action. Biochim. Biophys. Acta. 1185:1994;271-278.
73. Miyoshi H., Tokutake N., Imaeda Y., Akagi T., Iwamura H. A model of antimycin A binding based on structure-activity studies of synthetic antimycin A analogues. Biochim. Biophys. Acta. 1229:1995;149-154.
74. Orner B.P., Ernst J.T., Hamilton A.D. Towards proteomimetics. terphenyl derivatives as structural and functional mimics of extended regions of an a-helix J. Am. Chem. Soc. 123:2001;5382-5383.
75. Ernst J.T., Kutzki O., Debnath A.K., Jiang S., Lu H., Hamilton A.D. Design of a protein surface antagonist based on a-helix mimicry. inhibition of gp41 assembly and viral fusion Angew. Chem. Int. Ed. 41:2002;278-281.
76. Reed J.C. Bcl-2 and the regulation of programmed cell death. J. Cell Biol. 124:1994;1-6.
77. Huang Z. The Bcl-2 family of proteins as targets for anticancer drug design. Oncogene. 19:2000;6627-6631.
78. Liu D., Huang Z. Synthetic peptides and non-peptidic molecules as probes of structure and function of Bcl-2 family proteins and modulators of apoptosis. Apoptosis. 6:2001;453-462.
79. Yamaguchi H., Paranawithana S.R., Lee M.W., Huang Z.W., Bhalla K.N., Wang H.G. Epothione B analogue (BMS-247550)-mediated cytotoxicity through induction of Bax conformational change in human breast cancer cells. Cancer Res. 62:2002;466-471.
80. Milella M., Kornblau S.M., Estrov Z., Konopleva M., Tari A., Schober W.D., Carter B., Harris D., Leysath C.L., Berestein G.L.et al. Simultaneous disruption of the Bcl-2 and MEK/MAPK pathways sinergistically induces apoptosis in acute myelogenous leukemia. Blood. 62:2002;466-471.
81. Veis D., Sorenson C., Shutter J., Korsmeyer S. Bcl-2-deficient mice demonstrate fulminant lymphoid apoptosis, polycystic kidneys, and hypopigmented hair. Cell. 75:1993;229-240.
82. Evan G., Littlewood T. A matter of life and cell death. Science. 281:1998;1317-1322.
83. Webb A., Cunningham D., Cotter F., Clarke P., di Stefano F., Ross P., Corbo M., Dziewanowska Z. Bcl-2 antisense therapy in patients with non-Hodgkin lymphoma. Lancet. 349:1997;1137-1141.
84. L expression efficiently induces apoptosis in tumor cells. Clin. Cancer Res. 6:2000;2547-2555.
85. L bispecific antisense oligonucleotide. Clin. Cancer Res. 7:2001;1446-1451.
86. Gozani O., Boyce M., Yoo L., Karuman P., Yuan J. Life and death in paradise. Nat. Cell Biol. 4:2002;E159-E162.
87. Thornberry N.A., Rano T.A., Peterson E.P., Rasper D.M., Timkey T., Garcia-Calvo M., Houtzager V.M., Nordstrom P.A., Roy S., Vaillancourt J.P.et al. A combinatorial approach defines specificities of members of the caspase family and granzyme B. Functional relationships established for key mediators of apoptosis. J. Biol. Chem. 272:1997;17907-17911.
88. Deveraux Q.L., Reed J.C. IAP family proteins-suppressors of apoptosis. Genes Dev. 13:1999;239-252.
89. Hay B.A. Understanding IAP function and regulation. a view from Drosophila Cell Death Differ. 7:2000;1045-1056.
90. Altieri D.C. The molecular basis and potential role of survivin in cancer diagnosis and therapy. Trends Mol. Med. 7:2001;542-547.
91. Sun C., Cai M., Gunasekera A.H., Meadows R.P., Wang H., Chen J., Zhang H., Wu W., Xu N., Ng S.C.et al. NMR structure and mutagenesis of the inhibitor-of-apoptosis protein XIAP. Nature. 401:1999;818-822.
92. Sun C., Cai M., Meadows R.P., Xu N., Gunasekera A.H., Herrmann J., Wu J.C., Fesik S.W. NMR structure and mutagenesis of the third Bir domain of the inhibitor of apoptosis protein XIAP. J. Biol. Chem. 275:2000;33777-33781.
93. Chantalat L., Skoufias D.A., Kleman J.P., Jung B., Dideberg O., Margolis R.L. Crystal structure of human survivin reveals a bow tie-shaped dimer with two unusual alpha-helical extensions. Mol. Cell. 6:2000;183-189.
94. Muchmore S.W., Chen J., Jakob C., Zakula D., Matayoshi E.D., Wu W., Zhang H., Li F., Ng S.C., Altieri D.C. Crystal structure and mutagenic analysis of the inhibitor-of-apoptosis protein survivin. Mol. Cell. 6:2000;173-182.
95. Verdecia M.A., Huang H., Dutil E., Kaiser D.A., Hunter T., Noel J.P. Structure of the human anti-apoptotic protein survivin reveals a dimeric arrangement. Nat. Struct. Biol. 7:2000;602-608.
96. 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.
97. Huang Y., Park Y.C., Rich R.L., Segal D., Myszka D.G., Wu H. Structural basis of caspase inhibition by XIAP. differential roles of the linker versus the BIR domain Cell. 104:2001;781-790.
98. Riedl S.J., Renatus M., Schwarzenbacher R., Zhou Q., Sun C., Fesik S.W., Liddington R.C., Salvesen G.S. Structural basis for the inhibition of caspase-3 by XIAP. Cell. 104:2001;791-800.
99. 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.
100. Liu Z., Sun C., Olejniczak E.T., Meadows R.P., Betz S.F., Oost T., Herrmann J., Wu J.C., Fesik S.W. Structural basis for binding of Smac/DIABLO to the XIAP BIR3 domain. Nature. 408:2000;1004-1008.
101. Fesik S.W., Shi Y. Controlling the caspase. Science. 294:2001;1477-1478.
102. Srinivasula S.M., Hegde R., Saleh A., Datta P., Shiozaki E., Chai J., Lee R.A., Robbins P.D., Fernandes-Alnemri T., Shi Y.et al. A conserved XIAP-interaction motif in caspase-9 and Smac/DIABLO regulates caspase activity and apoptosis. Nature. 410:2001;112-116.
103. 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.
104. Olie R.A., Simoes-Wust A.P., Baumann B., Leech S.H., Fabbro D., Stahel R.A., Zangemeister-Wittke U. A novel antisense oligonucleotide targeting survivin expression induces apoptosis and sensitizes lung cancer cells to chemotherapy. Cancer Res. 60:2001;2805-2809.
105. Shi Y. A conserved tetrapeptide motif. potentiating apoptosis through IAP-binding Cell Death Differ. 9:2002;93-95.
106. Chai J., Du C., Wu J.W., Kyin S., Wang X., Shi Y. Structural and biochemical basis of apoptotic activation by Smac/DIABLO. Nature. 406:2000;855-862.
107. Srinivasula S.M., Datta P., Fan X.J., Fernandes-Alnemri T., Huang Z., Alnemri E.S. Molecular determinants of the caspase-promoting activity of Smac/DIABLO and its role in the death receptor pathway. J. Biol. Chem. 275:2000;36152-36157.
108. Kipp R.A., Case M.A., Wist A.D., Cresson C.M., Carrell M., Griner E., Wiita A., Albiniak P.A., Chai J., Shi Y.et al. Molecular targeting of inhibitor of apoptosis proteins based on small molecule mimics of natural binding partners. Biochemistry. 41:2002;7344-7349.
109. Guo F., Nimmanapalli R., Paranawithana S., Wittman S., Griffin D., Bali P., O'Bryan E., Fumero C., Wang H.G., Bhalla K. Ectopic overexpression of second mitochondria-derived activator of caspases (Smac/DIABLO) or cotreatment with N-terminus of Smac/DIABLO peptide potentiates epothilone B derivative-(BMS 247550) and Apo-2L/TRAIL-induced apoptosis. Blood. 99:2002;3419-3426.
110. Fulda S., Wick W., Weller M., Debatin K.M. Smac agonists sensitize for Apo2L/TRAIL- or anticancer drug-induced apoptosis and induce regression of malignant glioma in vivo. Nat. Med. 8:2002;808-815.