Zinc-mediated allosteric inhibition of caspase-6

Journal of Biological Chemistry

Volumn 287, Issue 43, 2012, Pages 36000-36011

  Velázquez Delgado, Elih M ^a   Hardy, Jeanne A ^a  

^a UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE; ALLOSTERIC INHIBITION; ANOMALOUS DIFFRACTION; APOPTOTIC; CASPASES; CYSTEINE PROTEASE; ENZYMATIC ACTIVITIES; HELICAL CONFORMATION; INDUCTIVELY COUPLED PLASMA-OPTICAL EMISSION SPECTROSCOPY; NEURODEGENERATIVE; NEURODEGENERATIVE DISORDERS; WATER MOLECULE; ZINC BINDING;

AMINO ACIDS; CELL DEATH; EMISSION SPECTROSCOPY; ENZYME ACTIVITY; INDUCTIVELY COUPLED PLASMA;

ZINC;

CASPASE 6; CASPASE 9; GLUTAMINE; HISTIDINE; LYSINE; MONOMER; ZINC;

ALLOSTERISM; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME BINDING; ENZYME CONFORMATION; ENZYME INHIBITION; MASS SPECTROMETRY; METAL BINDING; PRIORITY JOURNAL; STRUCTURE ACTIVITY RELATION;

ALLOSTERIC REGULATION; BINDING SITES; CASPASE 6; HUMANS; PEPTIDE MAPPING; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; ZINC;

EID: 84867805315     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.397752     Document Type: Article

References (71)

1. Fernandes-Alnemri, T., Litwack, G., and Alnemri, E. S. (1995) Mch2, a new member of the apoptotic Ced-3/Ice cysteine protease gene family. Cancer Res. 55, 2737-2742
2. Suzuki, A., Kusakai, G., Kishimoto, A., Shimojo, Y., Miyamoto, S., Ogura, T., Ochiai, A., and Esumi, H. (2004) Regulation of caspase-6 and FLIP by the AMPK family member ARK5. Oncogene 23, 7067-7075 (Pubitemid 39319168)
3. Ruchaud, S., Korfali, N., Villa, P., Kottke, T. J., Dingwall, C., Kaufmann, S. H., and Earnshaw, W. C. (2002) Caspase-6 gene disruption reveals a requirement for lamin A cleavage in apoptotic chromatin condensation. EMBO J. 21, 1967-1977 (Pubitemid 34437194)
4. Takahashi, A., Alnemri, E. S., Lazebnik, Y. A., Fernandes-Alnemri, T., Litwack, G., Moir, R. D., Goldman, R. D., Poirier, G. G., Kaufmann, S. H., and Earnshaw, W. C. (1996) Cleavage of lamin A by Mch2α but not CPP32. Multiple interleukin 1β-converting enzyme-related proteases with distinct substrate recognition properties are active in apoptosis. Proc. Natl. Acad. Sci. U.S.A. 93, 8395-8400
5. 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., Chapman, K. T., and Nicholson, D. W. (1997) 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, 17907-17911 (Pubitemid 27306365)
6. Albrecht, S., Bourdeau, M., Bennett, D., Mufson, E. J., Bhattacharjee, M., and LeBlanc, A. C. (2007) Activation of caspase-6 in aging and mild cognitive impairment. Am. J. Pathol. 170, 1200-1209 (Pubitemid 47339328)
7. Guo, H., Albrecht, S., Bourdeau, M., Petzke, T., Bergeron, C., and LeBlanc, A. (2004) Active caspase-6 and caspase-6-cleaved Tau in neuropil threads, neuritic plaques, and neurofibrillary tangles of Alzheimer disease. Am. J. Pathol. 165, 523-531 (Pubitemid 38971382)
8. Graham, R. K., Deng, Y., Carroll, J., Vaid, K., Cowan, C., Pouladi, M. A., Metzler, M., Bissada, N., Wang, L., Faull, R. L., Gray, M., Yang, X. W., Raymond, L. A., and Hayden, M. R. (2010) Cleavage at the 586-amino acid caspase-6 site in mutant huntingtin influences caspase-6 activation in vivo. J. Neurosci. 30, 15019-15029
9. Singh, A. B., Kaushal, V., Megyesi, J. K., Shah, S. V., and Kaushal, G. P. (2002) Cloning and expression of rat caspase-6 and its localization in renal ischemia/reperfusion injury. Kidney Int. 62, 106-115 (Pubitemid 34754053)
10. Sivananthan, S. N., Lee, A. W., Goodyer, C. G., and LeBlanc, A. C. (2010) Familial amyloid precursor protein mutants cause caspase-6-dependent but amyloid β-peptide-independent neuronal degeneration in primary human neuron cultures. Cell Death Dis. 1, e100
11. Galvan, V., Gorostiza, O. F., Banwait, S., Ataie, M., Logvinova, A. V., Sitaraman, S., Carlson, E., Sagi, S. A., Chevallier, N., and Jin, K. (2006) Reversal of Alzheimer-like pathology and behavior in human APP transgenic mice by mutation of Asp-664. Proc. Natl. Acad. Sci. U.S.A. 103, 7130-7135
12. Hermel, E., Gafni, J., Propp, S. S., Leavitt, B. R., Wellington, C. L., Young, J. E., Hackam, A. S., Logvinova, A. V., Peel, A. L., Chen, S. F., Hook, V., Singaraja, R., Krajewski, S., Goldsmith, P. C., Ellerby, H. M., Hayden, M. R., Bredesen, D. E., and Ellerby, L. M. (2004) Specific caspase interactions and amplification are involved in selective neuronal vulnerability in Huntington disease. Cell Death Differ. 11, 424-438 (Pubitemid 38489420)
13. Nikolaev, A., McLaughlin, T., O'Leary, D. D., and Tessier-Lavigne, M. (2009) APP binds DR6 to trigger axon pruning and neuron death via distinct caspases. Nature 457, 981-989
14. Sultana, R., Banks, W. A., and Butterfield, D. A. (2010) Decreased levels of PSD95 and two associated proteins and increased levels of BCl2 and caspase 3 in hippocampus from subjects with amnestic mild cognitive impairment. Insights into their potential roles for loss of synapses and memory, accumulation of Aβ, and neurodegeneration in a prodromal stage of Alzheimer disease. J. Neurosci. Res. 88, 469-477
15. Fuentes-Prior, P., and Salvesen, G. S. (2004) The protein structures that shape caspase activity, specificity, activation, and inhibition. Biochem. J. 384, 201-232 (Pubitemid 39656233)
16. Vaidya, S., Velázquez-Delgado, E. M., Abbruzzese, G., and Hardy, J. A. (2011) Substrate-induced conformational changes occur in all cleaved forms of caspase-6. J. Mol. Biol. 406, 75-91
17. Vaidya, S., and Hardy, J. A. (2011) Caspase-6 latent state stability relies on helical propensity. Biochemistry 50, 3282-3287
18. Baumgartner, R., Meder, G., Briand, C., Decock, A., D'arcy, A., Hassiepen, U., Morse, R., and Renatus, M. (2009) The crystal structure of caspase-6, a selective effector of axonal degeneration. Biochem. J. 423, 429-439
19. Wang, X. J., Cao, Q., Liu, X., Wang, K. T., Mi, W., Zhang, Y., Li, L. F., LeBlanc, A. C., and Su, X. D. (2010) Crystal structures of human caspase 6 reveal a new mechanism for intramolecular cleavage self-activation. EMBO Rep. 11, 841-847
20. Walsh, J. G., Cullen, S. P., Sheridan, C., Lüthi, A., Gerner, C., and Martin, S. J. (2008) Executioner caspase-3 and caspase-7 are functionally distinct proteases. Proc. Natl. Acad. Sci. U.S.A. 105, 12815-12819
21. Slee, E. A., Adrain, C., and Martin, S. J. (2001) Executioner caspase-3, -6, and -7 perform distinct, nonredundant roles during the demolition phase of apoptosis. J. Biol. Chem. 276, 7320-7326
22. Deveraux, Q. L., Takahashi, R., Salvesen, G. S., and Reed, J. C. (1997) X-linked IAP is a direct inhibitor of cell-death proteases. Nature 388, 300-304 (Pubitemid 27317977)
23. Velázquez-Delgado, E. M., and Hardy, J. A. (2012) Phosphorylation regulates assembly of the caspase-6 substrate-binding groove. Structure 20, 742-751
24. Jiménez Del Río, M., and Vélez-Pardo, C. (2004) Transition metal-induced apoptosis in lymphocytes via hydroxyl radical generation, mitochondria dysfunction, and caspase-3 activation. An in vitro model for neurodegeneration. Arch. Med. Res. 35, 185-193
25. Rudolf, E., and Cervinka, M. (2010) Zinc pyrithione induces cellular stress signaling and apoptosis in Hep-2 cervical tumor cells. The role of mitochondria and lysosomes. Biometals 23, 339-354
26. Rogers, J. M., Taubeneck, M. W., Daston, G. P., Sulik, K. K., Zucker, R. M., Elstein, K. H., Jankowski, M. A., and Keen, C. L. (1995) Zinc deficiency causes apoptosis but not cell cycle alterations in organogenesis-stage rat embryos. Effect of varying duration of deficiency. Teratology 52, 149-159
27. Chimienti, F., Seve, M., Richard, S., Mathieu, J., and Favier, A. (2001) Role of cellular zinc in programmed cell death. Temporal relationship between zinc depletion, activation of caspases, and cleavage of Sp family transcription factors. Biochem. Pharmacol. 62, 51-62 (Pubitemid 32488977)
28. Schrantz, N., Auffredou, M. T., Bourgeade, M. F., Besnault, L., Leca, G., and Vazquez, A. (2001) Zinc-mediated regulation of caspases activity. Dose-dependent inhibition or activation of caspase-3 in the human Burkitt lymphoma B cells (Ramos). Cell Death Differ. 8, 152-161 (Pubitemid 32201363)
29. Stennicke, H. R., and Salvesen, G. S. (1997) Biochemical characteristics of caspases-3, -6, -7, and -8. J. Biol. Chem. 272, 25719-25723 (Pubitemid 27438890)
30. Truong-Tran, A. Q., Grosser, D., Ruffin, R. E., Murgia, C., and Zalewski, P. D. (2003) Apoptosis in the normal and inflamed airway epithelium. Role of zinc in epithelial protection and procaspase-3 regulation. Biochem. Pharmacol. 66, 1459-1468 (Pubitemid 38373334)
31. Truong-Tran, A. Q., Ruffin, R. E., Foster, P. S., Koskinen, A. M., Coyle, P., Philcox, J. C., Rofe, A. M., and Zalewski, P. D. (2002) Altered zinc homeostasis and caspase-3 activity in murine allergic airway inflammation. Am. J. Respir. Cell Mol. Biol. 27, 286-296 (Pubitemid 34979286)
32. Kondoh, M., Tasaki, E., Takiguchi, M., Higashimoto, M., Watanabe, Y., and Sato, M. (2005) Activation of caspase-3 in HL-60 cells treated with pyrithione and zinc. Biol. Pharm. Bull. 28, 757-759 (Pubitemid 40879954)
33. Peterson, Q. P., Goode, D. R., West, D. C., Ramsey, K. N., Lee, J. J., and Hergenrother, P. J. (2009) PAC-1 activates procaspase-3 in vitro through relief of zinc-mediated inhibition. J. Mol. Biol. 388, 144-158
34. Lucas, P. W., Schmit, J. M., Peterson, Q. P., West, D. C., Hsu, D. C., Novotny, C. J., Dirikolu, L., Churchwell, M. I., Doerge, D. R., Garrett, L. D., Hergenrother, P. J., and Fan, T. M. (2011) Pharmacokinetics and derivation of an anticancer dosing regimen for PAC-1, a preferential small molecule activator of procaspase-3, in healthy dogs. Invest. New Drugs 29, 901-911
35. Peterson, Q. P., Hsu, D. C., Goode, D. R., Novotny, C. J., Totten, R. K., and Hergenrother, P. J. (2009) Procaspase-3 activation as an anti-cancer strategy. Structure-activity relationship of procaspase-activating compound 1 (PAC-1) and its cellular co-localization with caspase-3. J. Med. Chem. 52, 5721-5731
36. Huber, K. L., and Hardy, J. A. (2012) Mechanism of zinc-mediated inhibition of caspase-9. Protein Sci. 21, 1056-1065
37. Li, Y., Hawkins, B. E., DeWitt, D. S., Prough, D. S., and Maret, W. (2010) The relationship between transient zinc ion fluctuations and redox signaling in the pathways of secondary cellular injury. Relevance to traumatic brain injury. Brain Res. 1330, 131-141
38. Lovell, M. A., Robertson, J. D., Teesdale, W. J., Campbell, J. L., and Markesbery, W. R. (1998) Copper, iron, and zinc in Alzheimer disease senile plaques. J. Neurol. Sci. 158, 47-52 (Pubitemid 28277534)
39. Popescu, B. F., and Nichol, H. (2011) Mapping brain metals to evaluate therapies for neurodegenerative disease. CNS Neurosci. Ther. 17, 256-268
40. Religa, D., Strozyk, D., Cherny, R. A., Volitakis, I., Haroutunian, V., Winblad, B., Naslund, J., and Bush, A. I. (2006) Elevated cortical zinc in Alzheimer disease. Neurology 67, 69-75 (Pubitemid 44305464)
41. Pettit, F. K., Bare, E., Tsai, A., and Bowie, J. U. (2007) HotPatch. A statistical approach to finding biologically relevant features on protein surfaces. J. Mol. Biol. 369, 863-879 (Pubitemid 46709917)
42. de Calignon, A., Fox, L. M., Pitstick, R., Carlson, G. A., Bacskai, B. J., Spires-Jones, T. L., and Hyman, B. T. (2010) Caspase activation precedes and leads to tangles. Nature 464, 1201-1204
43. LeBlanc, A., Liu, H., Goodyer, C., Bergeron, C., and Hammond, J. (1999) Caspase-6 role in apoptosis of human neurons, amyloidogenesis, and Alzheimer disease. J. Biol. Chem. 274, 23426-23436
44. Rissman, R. A., Poon, W. W., Blurton-Jones, M., Oddo, S., Torp, R., Vitek, M. P., LaFerla, F. M., Rohn, T. T., and Cotman, C. W. (2004) Caspase-cleavage of Tau is an early event in Alzheimer disease tangle pathology. J. Clin. Invest. 114, 121-130 (Pubitemid 39071651)
45. Witkowski, W. A., and Hardy, J. A. (2009) L2 loop is critical for caspase-7 active site formation. Protein Sci. 18, 1459-1468
46. Collaborative Computational Project, Number 4 (1994) The CCP4 suite programs for protein crystallography. Acta Crystallogr.DBiol. Crystallogr. 50, 760-763
47. McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., and Read, R. J. (2007) Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (Pubitemid 47080256)
48. Emsley, P., and Cowtan, K. (2004) Coot. Model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (Pubitemid 41742764)
49. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 (Pubitemid 27235885)
50. Laskowski, R. A., MacArthur, M. W., Moss, D. S., and Thornton, J. M. (1993) PROCHECK. A program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26, 283-291
51. Chen, V. B., Arendall, W. B., 3rd, Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010) MolProbity. All-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66, 12-21
52. Perry, D. K., Smyth, M. J., Stennicke, H. R., Salvesen, G. S., Duriez, P., Poirier, G. G., and Hannun, Y. A. (1997) Zinc is a potent inhibitor of the apoptotic protease, caspase-3. A novel target for zinc in the inhibition of apoptosis. J. Biol. Chem. 272, 18530-18533 (Pubitemid 27318188)
53. Klaiman, G., Champagne, N., and LeBlanc, A. C. (2009) Self-activation of caspase-6 in vitro and in vivo. Caspase-6 activation does not induce cell death in HEK293T cells. Biochim. Biophys. Acta 1793, 592-601
54. Boucher, D., Blais, V., and Denault, J. B. (2012) Caspase-7 uses an exosite to promote poly(ADP ribose) polymerase 1 proteolysis. Proc. Natl. Acad. Sci. U.S.A. 109, 5669-5674
55. Shu, N. (2010) Protein Structure Prediction: Zinc-binding Sites, One-dimensional Structure, and Remote Homology, pp. 47-52, Stockholm University, Elsevier Science Publishers B.V., Amsterdam
56. Sousa, S. F., Lopes, A. B., Fernandes, P. A., and Ramos, M. J. (2009) The zinc proteome. A tale of stability and functionality. Dalton Trans., 7946-7956
57. Vallee, B. L., and Auld, D. S. (1993) Zinc. Biological functions and coordination motifs. Acc. Chem. Res. 26, 543-551
58. Vallee, B. L., and Auld, D. S. (1993) New perspective on zinc biochemistry. Cocatalytic sites in multi-zinc enzymes. Biochemistry 32, 6493-6500 (Pubitemid 23217117)
59. Alberts, I. L., Nadassy, K., and Wodak, S. J. (1998) Analysis of zinc-binding sites in protein crystal structures. Protein Sci. 7, 1700-1716 (Pubitemid 29133175)
60. Maret, W. (2005) Zinc coordination environments in proteins determine zinc functions. J. Trace Elem. Med. Biol. 19, 7-12
61. Maret, W. (2012) New perspectives of zinc coordination environments in proteins. J. Inorg. Biochem. 111, 110-116
62. Sukumar, N., Choi, M., and Davidson, V. L. (2011) Replacement of the axial copper ligand methionine with lysine in amicyanin converts it to a zinc-binding protein that no longer binds copper. J. Inorg. Biochem. 105, 1638-1644
63. Hardy, J. A., Lam, J., Nguyen, J. T., O'Brien, T., and Wells, J. A. (2004) Discovery of an allosteric site in the caspases. Proc. Natl. Acad. Sci. U.S.A. 101, 12461-12466 (Pubitemid 39122046)
64. Hardy, J. A., and Wells, J. A. (2009) Dissecting an allosteric switch in caspase-7 using chemical and mutational probes. J. Biol. Chem. 284, 26063-26069
65. Datta, D., Scheer, J. M., Romanowski, M. J., and Wells, J. A. (2008) An allosteric circuit in caspase-1. J. Mol. Biol. 381, 1157-1167
66. Scheer, J. M., Romanowski, M. J., and Wells, J. A. (2006) A common allosteric site and mechanism in caspases. Proc. Natl. Acad. Sci. U.S.A. 103, 7595-7600
67. Lee, A. W., Champagne, N., Wang, X., Su, X. D., Goodyer, C., and Leblanc, A. C. (2010) Alternatively spliced caspase-6B isoform inhibits the activation of caspase-6A. J. Biol. Chem. 285, 31974-31984
68. Roberge, M., Santell, L., Dennis, M. S., Eigenbrot, C., Dwyer, M. A., and Lazarus, R. A. (2001) A novel exosite on coagulation factor VIIa and its molecular interactions with a new class of peptide inhibitors. Biochemistry 40, 9522-9531 (Pubitemid 32757890)
69. Yoo, N. J., Kim, M. S., Park, S. W., Seo, S. I., Song, S. Y., Lee, J. Y., and Lee, S. H. (2010) Expression analysis of caspase-6, caspase-9, and BNIP3 in prostate cancer. Tumori 96, 138-142
70. Stanger, K., Steffek, M., Zhou, L., Pozniak, C. D., Quan, C., Franke, Y., Tom, J., Tam, C., Elliott, J. M., Lewcock, J. W., Zhang, Y., Murray, J., and Hannoush, R. N. (2012) Allosteric peptides bind a caspase zymogen and mediate caspase tetramerization. Nat. Chem. Biol. 8, 655-660
71. Müller, I., Lamers, M. B., Ritchie, A. J., Park, H., Dominguez, C., Munoz- Sanjuan, I., Maillard, M., and Kiselyov, A. (2011) A new apo-caspase-6 crystal form reveals the active conformation of the apoenzyme. J. Mol. Biol. 410, 307-315