Modeling of the role of a Bax-activation switch in the mitochondrial apoptosis decision

Biophysical Journal

Volumn 92, Issue 12, 2007, Pages 4304-4315

  Chen, Chun ^a   Cui, Jun ^a   Lu, Haizhu ^a   Wang, Rui ^a   Zhang, Shuai ^a   Shen, Pingping ^a  

^a NANJING UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN BAX; PROTEIN BCL 2;

APOPTOSIS; ARTICLE; CYTOSOL; MITOCHONDRION; POLYMERIZATION; PROTEIN FAMILY; PROTEIN STABILITY; STOCHASTIC MODEL;

EID: 34250350056     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1529/biophysj.106.099606     Document Type: Article

References (54)

1. Milo, R., S. Shen-Orr, S. Itzkovitz, N. Kashtan, D. Chklovskii, and U. Alon. 2002. Network motifs: simple building blocks of complex networks. Science. 298:824-827.
2. Swat, M., A. Kel, and H. Herzel. 2004. Bifurcation analysis of the regulatory modules of the mammalian G1/S transition. Bioinformatics. 20:1506-1511.
3. Tyson, J. J., K. Chen, and B. Novak. 2001. Network dynamics and cell physiology. Nat. Rev. Mol. Cell Biol. 2:908-916.
4. Gombert, A. K., and J. Niesen. 2000. Mathematical modeling of metabolism. Curr. Opin. Biotechnol. 11:180-186.
5. Varner, J., and D. Ramkrishna. 1999. Mathematical models of metabolic pathways. Curr. Opin. Biotechnol. 10:146-150.
6. Fussenegger, M., J. E. Bailey, and J. Varner. 2000. A mathematical model of caspase function in apoptosis. Nat. Biotechnol. 18:768-774.
7. Castiglione, F., and S. Succi. 2005. Simulating the G-protein cAMP pathway with a two-compartment reactive lattice gas. Theor. Biosci. 123:413-429.
8. Wishart, D. S., R. Yang, D. Arndt, P. Tang, and J. Cruz. 2005. Dynamic cellular automata: an alternative approach to cellular simulation. In Silico Biol. 5:1-23.
9. Wurthner, J. U., A. K. Mukhopadhyay, and C. Peimann. 2000. A cellular automaton model of cellular signal transduction. Comput. Biol. Med. 30:1-21.
10. Shimizu, T. S., S. V. Aksenov, and D. Bray. 2003. A spatially extended stochastic model of the bacterial chemotaxis signaling pathway. J. Mol. Biol. 329:291-309.
11. Goldstein, J. C., R. M. Kluck, and D. R. Green. 2000. A single cell analysis of apoptosis: ordering the apoptotic phenotype. Ann. N. Y. Acad. Sci. 926:132-141.
12. Nair, V. D., T. Yuen, C. W. Olanow, and S. C. Sealfon. 2004. Early single cell bifurcation of pro- and antiapoptotic states during oxidative stress. J. Biol. Chem. 279:27494-27501.
13. Valentijn, A. J., A. D. Metcalfe, J. Kott, C. H. Streuli, and A. P. Gilmore. 2003. Spatial and temporal changes in Bax subcellular localization during anoikis. J. Cell Biol. 162:599-612.
14. Bentele, M., I. Lavrik, M. Ulrich, S. Stosser, D. W. Heermann, H. Kalthoff, P. H. Krammer, and R. Eils. 2004. Mathematical modeling reveals threshold mechanism in CD95-induced apoptosis. J. Cell Biol. 166:839-851.
15. Eissing, T., H. Conzelmann, E. D. Gilles, F. Allgower, E. Bullinger, and P. Scheurich. 2004. Bistability analyses of a caspase activation model for receptor-induced apoptosis. J. Biol. Chem. 279:36892-36897.
16. Bagci, E. Z., Y. Vodovotz, T. R. Billiar, G. B. Ermentrout, and I. Bahar. 2005. Bistability in apoptosis: roles of Bax, Bcl-2 and mitochondrial permeability transition pores. Biophys. J. 90:1546-1559.
17. Green, D. R., and G. Kroemer. 2005. Pharmacological manipulation of cell death: clinical applications in sight? J. Clin. Invest. 115:2610-2617.
18. Rao, C. V., D. M. Wolf, and A. P. Arkin. 2002. Control, exploitation and tolerance of intracellular noise. Nature. 420:231-237.
19. Tian, T., and K. Burrage. 2006. Stochastic models for regulatory networks of the genetic toggle switch. Proc. Natl. Acad. Sci. USA. 103:8372-8377.
20. Siehs, C., R. Oberbauer, G. Mayer, A. Lukas, and B. Mayer. 2002. Discrete simulation of regulatory homo- and heterodimerization in the apoptosis effector phase. Bioinformatics. 18:67-76.
21. Saikumar, P., Z. Dong, V. Mikhailov, M. Denton, J. M. Weiberg, and M. A. Venkatachalam. 1999. Apoptosis: definition, mechanisms, and relevance to disease. Am. J. Med. 107:489-506.
22. Loo, G., X. Saelens, M. Gurp, M. MacFarlane, S. Martin, and P. Vandenabeele. 2002. The role of mitochondrial factors in apoptosis: a Russian roulette with more than one bullet. Cell Death Differ. 9:1031-1042.
23. Letai, A. 2005. Pharmacological manipulation of Bcl-2 family members to control cell death. J. Clin. Invest. 115:2648-2655.
24. Schinzel, A., T. Kaufmann, and C. Borner. 2003. Bcl-2 family members: intracellular targeting, membrane-insertion, and changes in subcellular localization. Biochim. Biophys. Acta. 1644:95-105.
25. Bouchier-Hayes, L., L. Lartigue, and D. D. Newmeyer. 2005. Mitochondria: pharmacological manipulation of cell death. J. Clin. Invest. 115:2640-2647.
26. Tsujimoto, Y. 2003. Cell death regulation by the bcl-2 protein family in the mitochondria. J. Cell. Physiol. 195:158-167.
27. Cartron, P. F., T. Gallenne, G. Bougras, F. Gautier, F. Manero, P. Vusio, K. Meflah, F. M. Vallette, and P. Juin. 2004. The first alpha 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.
28. Marani, M., T. Tenev, D. Hancock, J. Downward, and N. R. Lemoine. 2002. Identification of novel isoforms of the BH3 domain protein Bim which directly activate Bax to trigger apoptosis. Mol. Cell. Biol. 22:3577-3589.
29. Esposti, M. D., and C. Dive. 2003. Mitochondrial membrane permeabilization by Bax/Bak. Biochem. Biophys. Res. 304:455-461.
30. Ruffolo, S. C., and G. C. Shore. 2003. Bcl-2 selectively interacts with the Bid-induced open conformer of BAK, inhibiting BAK autooligomerization. J. Biol. Chem. 278:25039-25045.
31. Yi, X., X. Yin, and Z. Dong. 2003. Inhibition of Bid-induced apoptosis by Bcl-2, tBid insertion, Bax translocation, and Bax/Bak oligomerization suppressed. J. Biol. Chem. 278:16992-16999.
32. Letai, A., M. C. Bassik, L. D. Walensky, S. Weiler, and J. Korsmeyer. 2002. Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell. 2:183-192.
33. Gilmore, A. P., A. D. Metcalfe, L. H. Romer, and C. H. Streuli. 2000. Integrin-mediated survival signals regulate the apoptotic function of Bax through its conformation and subcellular localization. J. Cell Biol. 149:431-445.
34. Dejean, L. M., S. Martinez-Caballero, S. Manon, and K. W. Kinnally. 2006. Regulation of the mitochondrial apoptosis-induced channel, MAC, by Bcl-2 family proteins. Biochim. Biophys. Acta. 1762:191-201.
35. Saito, M., S. J. Korsmeyer, and P. H. Schlesinger. 2000. Baxdependent transport of cytochrome c reconstituted in pure liposomes. Nat. Cell Biol. 2:553-555.
36. Nechushtan, A., C. L. Smith, I. Lamensdorf, S. Yoon, and R. J. Youle. 2001. Bax and Bak coalesce into novel mitochondria-associated clusters during apoptosis. J. Cell Biol. 153:1265-1276.
37. Verrier, F., B. Mignotte, G. Jan, and C. Brenner. 2003. Study of PTPC composition during apoptosis for identification of viral protein target. Ann. N. Y. Acad. Sci. 1010:126-142.
38. Zamzami, N., and G. Kroemer. 2001. The mitochondrion in apoptosis: how Pandora's box opens. Nat. Rev. Mol. Cell Biol. 2:67-71.
39. Alber, M. S., M. A. Kiskowski, J. A. Glazier, and Y. Jiang. 2003. On cellular automaton approaches to modeling biological cells. In Mathematical Systems Theory in Biology, Communication, and Finance. J. Rosenthal, and D. S. Gilliam, editors. Springer-Verlag, New York.
40. Minton, A. P. 2001. The influence of macromolecular crowding and macromolecular confinement on biochemical reactions in physiological media. J. Biol. Chem. 276:10577-10580.
41. Chen, C., J. Cui, S. Zhang, and P. Shen. 2006. Cellular automaton simulation of the Bcl-2 family proteins regulated mitochondrial outer membrane permeabilization. In The Study of Intelligent Computing Theory and Methodology in Bioinformatics. D. Huang et al., editors. USTC Publishers/China, Hefei. 194-200.
42. Kuwana, T., M. R. Mackey, G. Perkins, M. H. Ellisman, M. Latterich, R. Schneiter, D. R. Green, and D. D. Newmeyer. 2002. Bid, Bax and lipids cooperate to form supramolecular openings in the outer mitochondrial membrane. Cell. 111:331-342.
43. Hua, F., M. G. Cornejo, M. H. Cardone, C. L. Stokes, and D. A. Lauffenburger. 2005. Effects of Bcl-2 levels on Fas signaling induce Capase-3 activation: molecular genetic tests of computational model predictions. J. Immunol. 175:985-995.
44. Bhattacharyya, A., D. Mandal, L. Lahiry, G. Sa, and T. Das. 2004. Black tea protects immunocytes from tumor-induced apoptosis by changing Bcl-2/Bax ratio. Cancer Lett. 209:147-154.
45. Tirado, O. M., S. Mateo-Lozano, and V. Notario. 2005. Rapamycin induces apoptosis of JN-DSRCT-1 cells by increasing the Bax:Bcl-Xl ratio through concurrent mechanisms dependent and independent of its mTOR inhibitory activity. Oncogene. 24:3348-3357.
46. Childs, A. C., S. L. Phaneuf, A. J. Dirks, T. Philips, and C. Leeuwenburgh. 2002. Doxorubicin treatment in vivo causes cytochrome c release and cardiomyocyte apoptosis, as well as increased mitochondrial efficiency, superoxide dismutase activity, and Bcl-2:Bax ratio. Cancer Res. 62:4595-4598.
47. Chang, L. K., and E. M. Johnson. 2002. Cyclosporin A inhibits caspase-independent death of NGF-deprived sympathetic neurons: a potential role for mitochondrial permeability transition. J. Cell Biol. 157:771-781.
48. Shimizu, S., Y. Matsuoka, Y. Shinohara, Y. Yoneda, and Y. Tsujimoto. 2001. Essential role of voltage-dependent anion channel in various forms of apoptosis in mammalian cells. J. Cell Biol. 152:237-250.
49. Adachi, M., H. Higuchi, S. Miura, T. Azuma, S. Inokuchi, H. Saito, S. Kato, and H. Ishii. 2004. Bax interacts with the voltage-dependent anion channel and mediates ethanol-induced apoptosis in rat hepatocytes. Am. J. Physiol. Gastrointest. Liver Physiol. 287:695-705.
50. Terada, S., T. Kumagai, N. Yamamoto, A. Ogawa, J. Ishimura, T. Fujita, E. Suzuki, and M. Miki. 2003. Generation of a novel apoptosis-resistant hepatoma cell line. J. Biosci. Bioeng. 95:146-151.
51. Tan, C., P. J. Dlugosz, J. Peng, Z. Zhang, S. M. Lapolla, S. M. Plafker, D. W. Andrews, and J. Lin. 2006. Auto-activation of the apoptosis protein Bax increases mitochondrial membrane permeability and is inhibited by Bcl-2. J. Biol. Chem. 281:14764-14775.
52. Ferrell, J. M., and W. Xiong. 2001. Bistability in cell signaling: how to make continuous processes discontinuous, and reversible processes irreversible. Chaos. 11:227-238.
53. Hasty, J., J. Pradines, M. Dolnik, and J. J. Collins. 2000. Noise-based switches and amplifiers for gene expressions. Proc. Natl. Acad. Sci. USA. 97:2075-2080.
54. Chopard, B., and M. Droz. 1998. Cellular Automata Modeling of Physical Systems. Cambridge University Press, Cambridge, UK.