Proapoptotic activities of Protein Disulfide Isomerase (PDI) and PDIA3 protein, a role of the Bcl-2 protein Bak

Journal of Biological Chemistry

Volumn 290, Issue 14, 2015, Pages 8949-8963

  Zhao, Guoping ^a   Lu, Huayi ^b   Li, Chi ^a  

^a University of Louisville School of Medicine   (United States)

^b JILIN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DEATH; ENZYME ACTIVITY; MITOCHONDRIA; SIGNALING;

APOPTOTIC RESPONSE; APOPTOTIC SIGNALING; APOPTOTIC STIMULI; MISFOLDED PROTEINS; MOLECULAR MECHANISM; PRO-APOPTOTIC FUNCTION; PROAPOPTOTIC ACTIVITY; PROTEIN DISULFIDE ISOMERASES;

PROTEINS;

PROTEIN BAK; PROTEIN BAX; PROTEIN DISULFIDE ISOMERASE; BAK1 PROTEIN, MOUSE; PDIA3 PROTEIN, MOUSE;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; ENZYME INHIBITION; IN VITRO STUDY; MITOCHONDRIAL MEMBRANE; MOUSE; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PURIFICATION; SIGNAL TRANSDUCTION; UNFOLDED PROTEIN RESPONSE; ANIMAL; BIOCATALYSIS; FLUORESCENT ANTIBODY TECHNIQUE; METABOLISM; PHYSIOLOGY;

ANIMALS; APOPTOSIS; BCL-2 HOMOLOGOUS ANTAGONIST-KILLER PROTEIN; BIOCATALYSIS; FLUORESCENT ANTIBODY TECHNIQUE; MICE; PROTEIN DISULFIDE-ISOMERASES;

EID: 84926629894     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.619353     Document Type: Article

References (48)

1. Ellgaard, L., and Ruddock, L. W. (2005) The human protein disulphide isomerase family: substrate interactions and functional properties. EMBO Rep. 6, 28-32
2. Galligan, J. J., and Petersen, D. R. (2012) The human protein disulfide isomerase gene family. Hum. Genomics 6, 6
3. Freedman, R. B., Hirst, T. R., and Tuite, M. F. (1994) Protein disulphide isomerase: building bridges in protein folding. Trends Biochem. Sci. 19, 331-336
4. Coe, H., and Michalak, M. (2010) ERp57, a multifunctional endoplasmic reticulum resident oxidoreductase. Int. J. Biochem. Cell Biol. 42, 796-799
5. Turano, C., Coppari, S., Altieri, F., and Ferraro, A. (2002) Proteins of the PDI family: unpredicted non-ER locations and functions. J. Cell. Physiol. 193, 154-163
6. Mossuto, M. F. (2013) Disulfide bonding in neurodegenerative misfolding diseases. Int. J. Cell Biol. 2013, 318319
7. Hetz, C., Russelakis-Carneiro, M., Wälchli, S., Carboni, S., Vial-Knecht, E., Maundrell, K., Castilla, J., and Soto, C. (2005) The disulfide isomerase Grp58 is a protective factor against prion neurotoxicity. J. Neurosci. 25, 2793-2802
8. Uehara, T., Nakamura, T., Yao, D., Shi, Z. Q., Gu, Z., Ma, Y., Masliah, E., Nomura, Y., and Lipton, S. A. (2006) S-nitrosylated protein-disulphide isomerase links protein misfolding to neurodegeneration. Nature 441, 513-517
9. Wang, S. B., Shi, Q., Xu, Y., Xie, W. L., Zhang, J., Tian, C., Guo, Y., Wang, K., Zhang, B. Y., Chen, C., Gao, C., and Dong, X. P. (2012) Protein disulfide isomerase regulates endoplasmic reticulum stress and the apoptotic process during prion infection and PrP mutant-induced cytotoxicity. PloS ONE 7, e38221
10. Tanaka, S., Uehara, T., and Nomura, Y. (2000) Up-regulation of protein-disulfide isomerase in response to hypoxia/brain ischemia and its protective effect against apoptotic cell death. J. Biol. Chem. 275, 10388-10393
11. Muller, C., Bandemer, J., Vindis, C., Camaré, C., Mucher, E., Guéraud, F., Larroque-Cardoso, P., Bernis, C., Auge, N., Salvayre, R., and Negre-Salvayre, A. (2013) Protein disulfide isomerase modification and inhibition contribute to ER stress and apoptosis induced by oxidized low density lipoproteins. Antioxid. Redox Signal. 18, 731-742
12. Corazzari, M., Lovat, P. E., Armstrong, J. L., Fimia, G. M., Hill, D. S., Birch-Machin, M., Redfern, C. P., and Piacentini, M. (2007) Targeting homeostatic mechanisms of endoplasmic reticulum stress to increase susceptibility of cancer cells to fenretinide-induced apoptosis: the role of stress proteins ERdj5 and ERp57. Br. J. Cancer 96, 1062-1071
13. Lovat, P. E., Corazzari, M., Armstrong, J. L., Martin, S., Pagliarini, V., Hill, D., Brown, A. M., Piacentini, M., Birch-Machin, M. A., and Redfern, C. P. (2008) Increasing melanoma cell death using inhibitors of protein disulfide isomerases to abrogate survival responses to endoplasmic reticulum stress. Cancer Res. 68, 5363-5369
14. Ron, D., and Walter, P. (2007) Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 8, 519-529
15. Ryu, E. J., Harding, H. P., Angelastro, J. M., Vitolo, O. V., Ron, D., and Greene, L. A. (2002) Endoplasmic reticulum stress and the unfolded protein response in cellular models of Parkinson's disease. J. Neurosci. 22, 10690-10698
16. Harding, H. P., and Ron, D. (2002) Endoplasmic reticulum stress and the development of diabetes: a review. Diabetes 51, S455-S461
17. Ni, M., and Lee, A. S. (2007) ER chaperones in mammalian development and human diseases. FEBS Lett. 581, 3641-3651
18. Hoffstrom, B. G., Kaplan, A., Letso, R., Schmid, R. S., Turmel, G. J., Lo, D. C., and Stockwell, B. R. (2010) Inhibitors of protein disulfide isomerase suppress apoptosis induced by misfolded proteins. Nat. Chem. Biol. 6, 900-906
19. Helton, E. S., and Chen, X. (2007) p53 modulation of the DNA damage response. J. Cell. Biochem. 100, 883-896
20. Xu, D., Perez, R. E., Rezaiekhaligh, M. H., Bourdi, M., and Truog, W. E. (2009) Knockdown of ERp57 increases BiP/GRP78 induction and protects against hyperoxia and tunicamycin-induced apoptosis. Am. J. Physiol. Lung Cell. Mol. Physiol. 297, L44-L51
21. Anathy, V., Roberson, E., Cunniff, B., Nolin, J. D., Hoffman, S., Spiess, P., Guala, A. S., Lahue, K. G., Goldman, D., Flemer, S., van der Vliet, A., Heintz, N. H., Budd, R. C., Tew, K. D., and Janssen-Heininger, Y. M. (2012) Oxidative processing of latent Fas in the endoplasmic reticulum controls the strength of apoptosis. Mol. Cell. Biol. 32, 3464-3478
22. Roberson, E. C., Tully, J. E., Guala, A. S., Reiss, J. N., Godburn, K. E., Pociask, D. A., Alcorn, J. F., Riches, D. W., Dienz, O., Janssen-Heininger, Y. M., and Anathy, V. (2012) Influenza induces endoplasmic reticulum stress, caspase-12-dependent apoptosis, and c-Jun N-terminal kinase-mediated transforming growth factor-β release in lung epithelial cells. Am. J. Respir. Cell and Mol. Biol. 46, 573-581
23. Sliskovic, I., and Mutus, B. (2006) Reversible inhibition of caspase-3 activity by iron(III): potential role in physiological control of apoptosis. FEBS Lett. 580, 2233-2237
24. White, C., Li, C., Yang, J., Petrenko, N. B., Madesh, M., Thompson, C. B., and Foskett, J. K. (2005) The endoplasmic reticulum gateway to apoptosis by Bcl-XL modulation of the InsP3R. Nat. Cell Biol. 7, 1021-1028
25. Zhao, G., Zhu, Y., Eno, C. O., Liu, Y., Deleeuw, L., Burlison, J. A., Chaires, J. B., Trent, J. O., and Li, C. (2014) Activation of the proapoptotic bcl-2 protein bax by a small molecule induces tumor cell apoptosis. Mol. Cell. Biol. 34, 1198-1207
26. Wang, X., Olberding, K. E., White, C., and Li, C. (2011) Bcl-2 proteins regulate ER membrane permeability to luminal proteins during ER stress-induced apoptosis. Cell Death Differ. 18, 38-47
27. Eno, C. O., Zhao, G., Olberding, K. E., and Li, C. (2012) The Bcl-2 proteins Noxa and Bcl-xL co-ordinately regulate oxidative stress-induced apoptosis. Biochem. J. 444, 69-78
28. Dickerhof, N., Kleffmann, T., Jack, R., and McCormick, S. (2011) Bacitracin inhibits the reductive activity of protein disulfide isomerase by disulfide bond formation with free cysteines in the substrate-binding domain. FEBS J. 278, 2034-2043
29. Huber-Ruano, I., Pinilla-Macua, I., Torres, G., Casado, F. J., and Pastor-Anglada, M. (2010) Link between high-affinity adenosine concentrative nucleoside transporter-2 (CNT2) and energy metabolism in intestinal and liver parenchymal cells. J. Cell. Physiol. 225, 620-630
30. Cartron, P. F., Juin, P., Oliver, L., Martin, S., Meflah, K., and Vallette, F. M. (2003) Nonredundant role of Bax and Bak in Bid-mediated apoptosis. Mol. Cell. Biol. 23, 4701-4712
31. Kepp, O., Rajalingam, K., Kimmig, S., and Rudel, T. (2007) Bak and Bax are non-redundant during infection- and DNA damage-induced apoptosis. EMBO J. 26, 825-834
32. Chipuk, J. E., and Green, D. R. (2008) How do BCL-2 proteins induce mitochondrial outer membrane permeabilization? Trends Cell Biol. 18, 157-164
33. Renault, T. T., and Chipuk, J. E. (2014) Death upon a kiss: mitochondrial outer membrane composition and organelle communication govern sensitivity to BAK/BAX-dependent apoptosis. Chem. Biol. 21, 114-123
34. Kuwana, T., and Newmeyer, D. D. (2003) Bcl-2-family proteins and the role of mitochondria in apoptosis. Curr. Opin. Cell Biol. 15, 691-699
35. Wei, M. C., Lindsten, T., Mootha, V. K., Weiler, S., Gross, A., Ashiya, M., Thompson, C. B., and Korsmeyer, S. J. (2000) tBID, a membrane-targeted death ligand, oligomerizes BAK to release cytochrome c. Genes Dev. 14, 2060-2071
36. Wang, X. (2001) The expanding role of mitochondria in apoptosis. Genes Dev. 15, 2922-2933
37. Newmeyer, D. D., and Ferguson-Miller, S. (2003) Mitochondria: releasing power for life and unleashing the machineries of death. Cell 112, 481-490
38. Jiang, X., and Wang, X. (2004) Cytochrome c-mediated apoptosis. Annu. Rev. Biochem. 73, 87-106
39. Lindsten, T., Ross, A. J., King, A., Zong, W. X., Rathmell, J. C., Shiels, H. A., Ulrich, E., Waymire, K. G., Mahar, P., Frauwirth, K., Chen, Y., Wei, M., Eng, V. M., Adelman, D. M., Simon, M. C., Ma, A., Golden, J. A., Evan, G., Korsmeyer, S. J., MacGregor, G. R., and Thompson, C. B. (2000) The combined functions of proapoptotic Bcl-2 family members bak and bax are essential for normal development of multiple tissues. Mol. Cell 6, 1389-1399
40. 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., and Korsmeyer, S. J. (2001) Proapoptotic BAX and BAK: a requisite gateway to mitochondrial dysfunction and death. Science 292, 727-730
41. Shimazu, T., Degenhardt, K., Nur-E-Kamal, A., Zhang, J., Yoshida, T., Zhang, Y., Mathew, R., White, E., and Inouye, M. (2007) NBK/BIK antagonizes MCL-1 and BCL-XL and activates BAK-mediated apoptosis in response to protein synthesis inhibition. Genes Dev. 21, 929-941
42. Wang, C., and Youle, R. J. (2012) Predominant requirement of Bax for apoptosis in HCT116 cells is determined by Mcl-1's inhibitory effect on Bak. Oncogene 31, 3177-3189
43. Lindenboim, L., Kringel, S., Braun, T., Borner, C., and Stein, R. (2005) Bak but not Bax is essential for Bcl-x (s)-induced apoptosis. Cell Death Differ. 12, 713-723
44. Madesh, M., Zong, W. X., Hawkins, B. J., Ramasamy, S., Venkatachalam, T., Mukhopadhyay, P., Doonan, P. J., Irrinki, K. M., Rajesh, M., Pacher, P., and Thompson, C. B. (2009) Execution of superoxide-induced cell death by the proapoptotic Bcl-2-related proteins Bid and Bak. Mol. Cell. Biol. 29, 3099-3112
45. Llambi, F., Moldoveanu, T., Tait, S. W., Bouchier-Hayes, L., Temirov, J., McCormick, L. L., Dillon, C. P., and Green, D. R. (2011) Aunified model of mammalian BCL-2 protein family interactions at the mitochondria. Mol. Cell 44, 517-531
46. Gardai, S. J., McPhillips, K. A., Frasch, S. C., Janssen, W. J., Starefeldt, A., Murphy-Ullrich, J. E., Bratton, D. L., Oldenborg, P. A., Michalak, M., and Henson, P. M. (2005) Cell-surface calreticulin initiates clearance of viable or apoptotic cells through trans-activation of LRP on the phagocyte. Cell 123, 321-334
47. Burikhanov, R., Zhao, Y., Goswami, A., Qiu, S., Schwarze, S. R., and Rangnekar, V. M. (2009) The tumor suppressor Par-4 activates an extrinsic pathway for apoptosis. Cell 138, 377-388
48. Obeid, M., Panaretakis, T., Joza, N., Tufi, R., Tesniere, A., van Endert, P., Zitvogel, L., and Kroemer, G. (2007) Calreticulin exposure is required for the immunogenicity of γ-irradiation and UVC light-induced apoptosis. Cell Death Differ. 14, 1848-1850