Casp8p41 generated by HIV protease kills CD4 T cells through direct Bak activation

Journal of Cell Biology

Volumn 206, Issue 7, 2014, Pages 867-876

  Sainski, Amy M ^a,b   Dai, Haiming ^a   Natesampillai, Sekar ^b   Pang, Yuan Ping ^a   Bren, Gary D ^b   Cummins, Nathan W ^b   Correia, Cristina ^a   Meng, X Wei ^a   Tarara, James E ^d   Ramirez Alvarado, Marina ^d   Katzmann, David J ^d   Ochsenbauer, Christina ^c   Kappes, John C ^c   Kaufmann, Scott H ^a   Badley, Andrew D ^b,e  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b University of Alabama at Birmingham   (United States)

^c University of Alabama at Birmingham   (United States)

^d MAYO GRADUATE SCHOOL   (United States)

^e MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BH3 PROTEIN; CASP8P41 PROTEIN; CASPASE; HUMAN IMMUNODEFICIENCY VIRUS PROTEINASE; PROCASPASE 8; PROTEIN BAK; UNCLASSIFIED DRUG; BAK1 PROTEIN, HUMAN; CASP8 PROTEIN, HUMAN; CASPASE 8; PROTEIN BINDING;

ANIMAL CELL; ARTICLE; CD4+ T LYMPHOCYTE; CELL DEATH; CELL KILLING; CONTROLLED STUDY; EMBRYO; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; MEMBRANE PERMEABILITY; MOUSE; MUTATION; NONHUMAN; OLIGOMERIZATION; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; AMINO ACID SEQUENCE; APOPTOSIS; CHEMISTRY; ENZYMOLOGY; HEK293 CELL LINE; HUMAN IMMUNODEFICIENCY VIRUS 1; JURKAT CELL LINE; METABOLISM; MISSENSE MUTATION; MOLECULAR GENETICS; PHYSIOLOGY; PROTEIN DEGRADATION; PROTEIN MULTIMERIZATION; VIROLOGY;

HUMAN IMMUNODEFICIENCY VIRUS;

AMINO ACID SEQUENCE; APOPTOSIS; BCL-2 HOMOLOGOUS ANTAGONIST-KILLER PROTEIN; CASPASE 8; CD4-POSITIVE T-LYMPHOCYTES; HEK293 CELLS; HIV PROTEASE; HIV-1; HUMANS; JURKAT CELLS; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN MULTIMERIZATION; PROTEOLYSIS;

EID: 84907758778     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201405051     Document Type: Article

References (38)

1. Algeciras-Schimnich, A., A.S. Belzacq-Casagrande, G.D. Bren, Z. Nie, J.A. Taylor, S.A. Rizza, C. Brenner, and A.D. Badley. 2007. Analysis of HIV protease killing through caspase 8 reveals a novel interaction between caspase 8 and mitochondria. Open Virol. J. 1:39-46.
2. Baum, E.Z., G.A. Bebernitz, and Y. Gluzman. 1990. Isolation of mutants of human immunodeficiency virus protease based on the toxicity of the enzyme in Escherichia coli. Proc. Natl. Acad. Sci. USA. 87:5573-5577. http://dx.doi.org/10.1073/pnas.87.14.5573
3. Berendsen, H.J.C., J.P.M. Postma, W.F. van Gunsteren, A. Di Nola, and J.R. Haak. 1984. Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81:3684-3690. http://dx.doi.org/10.1063/1.448118
4. Blanco, R., L. Carrasco, and I. Ventoso. 2003. Cell killing by HIV-1 protease. J. Biol. Chem. 278:1086-1093. http://dx.doi.org/10.1074/jbc.M205636200
5. Case, D.A., T.E. Cheatham III, T. Darden, H. Gohlke, R. Luo, K.M. Merz Jr., A. Onufriev, C. Simmerling, B. Wang, and R.J. Woods. 2005. The Amber biomolecular simulation programs. J. Comput. Chem. 26:1668-1688. http://dx.doi.org/10.1002/jcc.20290
6. Cheng, E.H., M.C. Wei, S. Weiler, R.A. Flavell, T.W. Mak, T. Lindsten, and S.J. Korsmeyer. 2001. BCL-2, BCL-X(L) sequester BH3 domainonly molecules preventing BAX- and BAK-mediated mitochondrial apoptosis. Mol. Cell. 8:705-711. http://dx.doi.org/10.1016/S1097-2765 (01)00320-3
7. Cooper, A., M. García, C. Petrovas, T. Yamamoto, R.A. Koup, and G.J. Nabel. 2013. HIV-1 causes CD4 cell death through DNA-dependent protein kinase during viral integration. Nature. 498:376-379. http://dx.doi.org/ 10.1038/nature12274
8. Czabotar, P.E., D. Westphal, G. Dewson, S. Ma, C. Hockings, W.D. Fairlie, E.F. Lee, S. Yao, A.Y. Robin, B.J. Smith, et al. 2013. Bax crystal structures reveal how BH3 domains activate Bax and nucleate its oligomerization to induce apoptosis. Cell. 152:519-531. http://dx.doi.org/10.1016/j.cell.2012.12.031
9. Dai, H., A. Smith, X.W. Meng, P.A. Schneider, Y.-P. Pang, and S.H. Kaufmann. 2011. Transient binding of an activator BH3 domain to the Bak BH3-binding groove initiates Bak oligomerization. J. Cell Biol. 194:39-48. http://dx.doi.org/10.1083/jcb.201102027
10. Darden, T., D. York, and L. Pedersen. 1993. Particle mesh Ewald: an N log(N) method for Ewald sums in large systems. J. Chem. Phys. 98:10089- 10092. http://dx.doi.org/10.1063/1.464397
11. Doitsh, G., M. Cavrois, K.G. Lassen, O. Zepeda, Z. Yang, M.L. Santiago, A.M. Hebbeler, and W.C. Greene. 2010. Abortive HIV infection mediates CD4 T cell depletion and inflammation in human lymphoid tissue. Cell. 143:789-801. http://dx.doi.org/10.1016/j.cell.2010.11.001
12. Earnshaw, W.C., L.M. Martins, and S.H. Kaufmann. 1999. Mammalian caspases: structure, activation, substrates, and functions during apoptosis. Annu. Rev. Biochem. 68:383-424. http://dx.doi.org/10.1146/annurev.biochem.68.1.383
13. Fulda, S., and D. Vucic. 2012. Targeting IAP proteins for therapeutic intervention in cancer. Nat. Rev. Drug Discov. 11:109-124. http://dx.doi.org/10.1038/nrd3627
14. Galluzzi, L., C. Brenner, E. Morselli, Z. Touat, and G. Kroemer. 2008. Viral control of mitochondrial apoptosis. PLoS Pathog. 4:e1000018. http://dx.doi.org/10.1371/journal.ppat.1000018
15. Gavathiotis, E., D.E. Reyna, M.L. Davis, G.H. Bird, and L.D. Walensky. 2010. BH3-triggered structural reorganization drives the activation of proapoptotic BAX. Mol. Cell. 40:481-492. http://dx.doi.org/10.1016/j.molcel.2010.10.019
16. Hornak, V., R. Abel, A. Okur, B. Strockbine, A. Roitberg, and C. Simmerling. 2006. Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins. 65:712-725. http://dx.doi.org/10.1002/prot.21123
17. Jorgensen, W.L., J. Chandreskhar, J.D. Madura, R.W. Impey, and M.L. Klein. 1983. Comparison of simple potential functions for simulating liquid water. J. Chem. Phys. 79:926-935. http://dx.doi.org/10.1063/1.445869
18. Kaplan, A.H., M. Manchester, and R. Swanstrom. 1994. The activity of the protease of human immunodeficiency virus type 1 is initiated at the membrane of infected cells before the release of viral proteins and is required for release to occur with maximum efficiency. J. Virol. 68:6782-6786.
19. Kim, H., H.C. Tu, D. Ren, O. Takeuchi, J.R. Jeffers, G.P. Zambetti, J.J. Hsieh, and E.H. Cheng. 2009. Stepwise activation of BAX and BAK by tBID, BIM, and PUMA initiates mitochondrial apoptosis. Mol. Cell. 36:487- 499. http://dx.doi.org/10.1016/j.molcel.2009.09.030
20. Kuwana, T., L. Bouchier-Hayes, J.E. Chipuk, C. Bonzon, B.A. Sullivan, D.R. Green, and D.D. Newmeyer. 2005. BH3 domains of BH3-only proteins differentially regulate Bax-mediated mitochondrial membrane permeabilization both directly and indirectly. Mol. Cell. 17:525-535. http:// dx.doi.org/10.1016/j.molcel.2005.02.003
21. Letai, A., M.C. Bassik, L.D. Walensky, M.D. Sorcinelli, S. Weiler, and S.J. Korsmeyer. 2002. Distinct BH3 domains either sensitize or activate mitochondrial apoptosis, serving as prototype cancer therapeutics. Cancer Cell. 2:183-192. http://dx.doi.org/10.1016/S1535-6108(02)00127-7
22. Llambi, F., T. Moldoveanu, S.W. Tait, L. Bouchier-Hayes, J. Temirov, L.L. McCormick, C.P. Dillon, and D.R. Green. 2011. A unified model of mammalian BCL-2 protein family interactions at the mitochondria. Mol. Cell. 44:517-531. http://dx.doi.org/10.1016/j.molcel.2011.10.001
23. Miller, L.K. 1999. An exegesis of IAPs: salvation and surprises from BIR motifs. Trends Cell Biol. 9:323-328. http://dx.doi.org/10.1016/S0962-8924(99)01609-8
24. Moldoveanu, T., C.R. Grace, F. Llambi, A. Nourse, P. Fitzgerald, K. Gehring, R.W. Kriwacki, and D.R. Green. 2013. BID-induced structural changes in BAK promote apoptosis. Nat. Struct. Mol. Biol. 20:589-597. http:// dx.doi.org/10.1038/nsmb.2563
25. Natesampillai, S., Z. Nie, N.W. Cummins, D. Jochmans, G.D. Bren, J.B. Angel, and A.D. Badley. 2010. Patients with discordant responses to antiretroviral therapy have impaired killing of HIV-infected T cells. PLoS Pathog. 6:e1001213. http://dx.doi.org/10.1371/journal.ppat.1001213
26. Nie, Z., B.N. Phenix, J.J. Lum, A. Alam, D.H. Lynch, B. Beckett, P.H. Krammer, R.P. Sekaly, and A.D. Badley. 2002. HIV-1 protease processes procaspase 8 to cause mitochondrial release of cytochrome c, caspase cleavage, and nuclear fragmentation. Cell Death Differ. 9:1172-1184. http://dx.doi.org/10.1038/sj.cdd.4401094
27. Nie, Z., G.D. Bren, S.A. Rizza, and A.D. Badley. 2008. HIV protease cleavage of procaspase 8 is necessary or death of HIV-infected cells. Open Virol. J. 2:1-7. http://dx.doi.org/10.2174/1874357900802010001
28. Pang, Y.-P., H. Dai, A. Smith, X.W. Meng, P.A. Schneider, and S.H. Kaufmann. 2012. Bak conformational changes induced by ligand binding: Insight into BH3 domain binding and Bak homo-oligomerization. Sci. Rep. 2:257. http://dx.doi.org/10.1038/srep00257
29. Pearlman, D.A., D.A. Case, J.W. Caldwell, W.S. Ross, T.E. Cheatham III, S. Debolt, D. Ferguson, G. Seibel, and P.A. Kollman. 1995. AMBER, a package of computer programs for applying molecular mechanics, normal mode analysis, molecular dynamics and free energy calculations to simulate the structural and energetic properties of molecules. Comput. Phys. Commun. 91:1-41. http://dx.doi.org/10.1016/ 0010-4655(95)00041-D
30. Sainski, A.M., S. Natesampillai, N.W. Cummins, G.D. Bren, J. Taylor, D.T. Saenz, E.M. Poeschla, and A.D. Badley. 2011. The HIV-1-specific protein Casp8p41 induces death of infected cells through Bax/Bak. J. Virol. 85:7965-7975. http://dx.doi.org/10.1128/JVI.02515-10
31. Strasser, A., S. Cory, and J.M. Adams. 2011. Deciphering the rules of programmed cell death to improve therapy of cancer and other diseases. EMBO J. 30:3667-3683. http://dx.doi.org/10.1038/emboj.2011.307
32. Taylor, R.C., S.P. Cullen, and S.J. Martin. 2008. Apoptosis: controlled demolition at the cellular level. Nat. Rev. Mol. Cell Biol. 9:231-241. http://dx.doi.org/10.1038/nrm2312
33. Ventoso, I., R. Blanco, C. Perales, and L. Carrasco. 2001. HIV-1 protease cleaves eukaryotic initiation factor 4G and inhibits cap-dependent translation. Proc. Natl. Acad. Sci. USA. 98:12966-12971. http://dx.doi.org/10.1073/ pnas.231343498
34. Walensky, L.D., K. Pitter, J. Morash, K.J. Oh, S. Barbuto, J. Fisher, E. Smith, G. L. Verdine, and S.J. Korsmeyer. 2006. A stapled BID BH3 helix directly binds and activates BAX. Mol. Cell. 24:199-210. http://dx.doi.org/10.1016/j.molcel.2006.08.020
35. Wei, M.C., W.X. Zong, E.H. Cheng, T. Lindsten, V. Panoutsakopoulou, A.J. Ross, K.A. Roth, G.R. MacGregor, C.B. Thompson, and S.J. Korsmeyer. 2001. Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science. 292:727-730. http://dx.doi.org/10.1126/science.1059108
36. Wickstrom, L., A. Okur, and C. Simmerling. 2009. Evaluating the performance of the ff99SB force field based on NMR scalar coupling data. Biophys. J. 97:853-856. http://dx.doi.org/10.1016/j.bpj.2009.04.063
37. Wu, S., and Y. Zhang. 2008. MUSTER: Improving protein sequence profileprofile alignments by using multiple sources of structure information. Proteins. 72:547-556. http://dx.doi.org/10.1002/prot.21945
38. Yu, J.W., P.D. Jeffrey, and Y. Shi. 2009. Mechanism of procaspase-8 activation by c-FLIPL. Proc. Natl. Acad. Sci. USA. 106:8169-8174. http://dx.doi.org/10.1073/pnas.0812453106