Crystal structure of the DegS stress sensor: How a PDZ domain recognizes misfolded protein and activates a protease

Cell

Volumn 117, Issue 4, 2004, Pages 483-494

  Wilken, Corinna ^a   Kitzing, Karina ^a   Kurzbauer, Robert ^a   Ehrmann, Michael ^b   Clausen, Tim ^a  

^a RESEARCH INSTITUTE OF MOLECULAR PATHOLOGY   (Austria)

^b CARDIFF UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DEGS PROTEASE; HEAT SHOCK PROTEIN; PDZ PROTEIN; PEPTIDE DERIVATIVE; PROTEINASE; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CATALYST; COMPLEX FORMATION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ESCHERICHIA COLI; HYBRID; MOLECULAR BIOLOGY; MOLECULAR MECHANICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; NEGIBACTERIA;

EID: 2342659637     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(04)00454-4     Document Type: Article

References (50)

1. Ades S.E., Connolly L.E., Alba B.M., Gross C.A. The Escherichia coli sigma(E)-dependent extracytoplasmic stress response is controlled by the regulated proteolysis of an anti-sigma factor. Genes Dev. 13:1999;2449-2461
2. Ades S.E., Grigorova I.L., Gross C.A. Regulation of the alternative sigma factor sigma(E) during initiation, adaptation, and shutoff of the extracytoplasmic heat shock response in Escherichia coli. J. Bacteriol. 185:2003;2512-2519
3. Alba B.M., Leeds J.A., Onufryk C., Lu C.Z., Gross C.A. DegS and YaeL participate sequentially in the cleavage of RseA to activate the sigma(E)-dependent extracytoplasmic stress response. Genes Dev. 16:2002;2156-2168
4. Alba B.M., Zhong H.J., Pelayo J.C., Gross C.A. degS (hhoB) is an essential Escherichia coli gene whose indispensable function is to provide sigma (E) activity. Mol. Microbiol. 40:2001;1323-1333
5. Baldi A., De Luca A., Morini M., Battista T., Felsani A., Baldi F., Catricala C., Amantea A., Noonan D.M., Albini A., et al. The HtrA1 serine protease is down-regulated during human melanoma progression and represses growth of metastatic melanoma cells. Oncogene. 21:2002;6684-6688
6. Bode W., Huber R. Induction of the bovine trypsinogen-trypsin transition by peptides sequentially similar to the N-terminus of trypsin. FEBS Lett. 68:1976;231-236
7. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., Jiang J.S., Kuszewski J., Nilges M., Pannu N.S., et al. Crystallography & NMR system. A new software suite for macromolecular structure determination Acta Crystallogr. D Biol. Crystallogr. 54:1998;905-921
8. Cabral J.H.M., Petosa C., Sutcliffe M.J., Raza S., Byron O., Poy F., Marfatia S.M., Chishti A.H., Liddington R.C. Crystal structure of a PDZ domain. Nature. 382:1996;649-652
9. Campbell E.A., Tupy J.L., Gruber T.M., Wang S., Sharp M.M., Gross C.A., Darst S.A. Crystal structure of Escherichia coli sigmaE with the cytoplasmic domain of its anti-sigma RseA. Mol. Cell. 11:2003;1067-1078
10. Clausen T., Southan C., Ehrmann M. The HtrA family of proteases. implications for protein composition and cell fate Mol. Cell. 10:2002;443-455
11. CCP4 High-throughput (Collaborative Computational Project in Macromolecular Crystallography) structure determination. Proceedings of the 2002 CCP4 study weekend. Acta Crystallogr. D Biol. Crystallogr. 58:2002;1897-1970.. January, 2002. York, United Kingdom
12. De Las Penas A., Connolly L., Gross C.A. The sigmaE-mediated response to extracytoplasmic stress in Escherichia coli is transduced by RseA and RseB, two negative regulators of sigmaE. Mol. Microbiol. 24:1997;373-385
13. Doyle D.A., Lee A., Lewis J., Kim E., Sheng M., MacKinnon R. Crystal structures of a complexed and peptide-free membrane protein-binding domain. Molecular basis of peptide recognition by PDZ Cell. 85:1996;1067-1076
14. Friedrich R., Panizzi P., Fuentes-Prior P., Richter K., Verhamme I., Anderson P.J., Kawabata S., Huber R., Bode W., Bock P.E. Staphylocoagulase is a prototype for the mechanism of cofactor-induced zymogen activation. Nature. 425:2003;535-539
15. Harris B.Z., Lim W.A. Mechanism and role of PDZ domains in signaling complex assembly. J. Cell Sci. 114:2001;3219-3231
16. Harrison S.C. Peptide-surface association. The case of PDZ and PTB domains Cell. 86:1996;341-343
17. Hegde R., Srinivasula S.M., Zhang Z., Wassell R., Mukattash R., Cilenti L., DuBois G., Lazebnik Y., Zervos A.S., Fernandes-Alnemri T., Alnemri E.S. Identification of Omi/HtrA2 as a mitochondrial apoptotic serine protease that disrupts inhibitor of apoptosis protein-caspase interaction. J. Biol. Chem. 277:2002;432-438
18. Hengge R., Bukau B. Proteolysis in prokaryotes. protein quality control and regulatory principles Mol. Microbiol. 49:2003;1451-1462
19. Huber R., Bode W. Structural basis of the activation and action of trypsin. J. Mol. Biol. 11:1978;114-122
20. Jones T.A., Zou J.Y., Cowan S.W., Kjeldgaard M. Improved methods For building protein models in electron-density maps and the location of errors in these models. Acta Crystallogr. A. 47:1991;110-119
21. Jones C.H., Dexter P., Evans A.K., Liu C., Hultgren S.J., Hruby D.E. Escherichia coli DegP protease cleaves between paired hydrophobic residues in a natural substrate. the PapA pilin J. Bacteriol. 184:2002;5762-5771
22. Jones J.M., Datta P., Srinivasula S.M., Ji W., Gupta S., Zhang Z., Davies E., Hajnoczky G., Saunders T.L., Van Keuren M.L., et al. Loss of Omi mitochondrial protease activity causes the neuromuscular disorder of mnd2 mutant mice. Nature. 425:2003;721-727
23. Kanehara K., Ito K., Akiyama Y. YaeL (EcfE) activates the sigma(E) pathway of stress response through a site-2 cleavage of anti-sigma(E), RseA. Genes Dev. 16:2002;2147-2155
24. Kim D.Y., Kim D.R., Ha S.C., Lokanath N.K., Lee C.J., Hwang H.Y., Kim K.K. Crystal structure of the protease domain of a heat-shock protein HtrA from Thermotoga maritima. J. Biol. Chem. 278:2003;6543-6551
25. Kraulis P.J. Molscript - a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24:1991;946-950
26. Krojer T., Garrido-Franco M., Huber R., Ehrmann M., Clausen T. Crystal structure of DegP (HtrA) reveals a new protease-chaperone machine. Nature. 416:2002;455-459
27. Li W., Srinivasula S.M., Chai J., Li P., Wu J.W., Zhang Z., Alnemri E.S., Shi Y. Structural insights into the pro-apoptotic function of mitochondrial serine protease HtrA2/Omi. Nat. Struct. Biol. 9:2002;436-441
28. Liao D.I., Qian J., Chisholm D.A., Jordan D.B., Diner B.A. Crystal structures of the photosystem II D1 C-terminal processing protease. Nat. Struct. Biol. 7:2000;749-753
29. Liberek K., Galitski T.P., Zylicz M., Georgopoulos C. The DnaK chaperone modulates the heat shock response of Escherichia coli by binding to the sigma 32 transcription factor. Proc. Natl. Acad. Sci. USA. 89:1992;3516-3520
30. Ma Y., Hendershot L.M. The unfolding tale of the unfolded protein response. Cell. 107:2001;827-830
31. Martins L.M., Iaccarino I., Tenev T., Gschmeissner S., Totty N.F., Lemoine N.R., Savopoulos J., Gray C.W., Creasy C.L., Dingwall C., Downward J. The serine protease Omi/HtrA2 regulates apoptosis by binding XIAP through a reaper-like motif. J. Biol. Chem. 277:2002;439-444
32. Martins L.M., Turk B.E., Cowling V., Borg A., Jarrell E.T., Cantley L.C., Downward J. Binding specificity and regulation of the serine protease and PDZ domains of HtrA2/Omi. J. Biol. Chem. 278:2003;49417-49427
33. Mecsas J., Rouviere P.E., Erickson J.W., Donohue T.J., Gross C.A. The activity of sigma E, an Escherichia coli heat-inducible sigma-factor, is modulated by expression of outer membrane proteins. Genes Dev. 7:1993;2618-2628
34. Merritt, E.A., and Bacon, D.J. (1997). Raster3D: Photorealistic molecular graphics. In Macromolecular Crystallography, Pt B, pp. 505-524.
35. Missiakas D., Mayer M.P., Lemaire M., Georgopoulos C., Raina S. Modulation of the Escherichia coli sigmaE (RpoE) heat-shock transcription-factor activity by the RseA, RseB and RseC proteins. Mol. Microbiol. 24:1997;355-371
36. Nie G.Y., Li Y., Minoura H., Batten L., Ooi G.T., Findlay J.K., Salamonsen L.A. A novel serine protease of the mammalian HtrA family is up-regulated in mouse uterus coinciding with placentation. Mol. Hum. Reprod. 9:2003;279-290
37. Otwinowski, Z., and Minor, W. (1997). Processing of X-ray diffraction data collected in oscillation mode. In Macromolecular Crystallography, Pt a, pp. 307-326.
38. Pallen M.J., Wren B.W. The HtrA family of serine proteases. Mol. Microbiol. 26:1997;209-221
39. Perona J.J., Craik C.S. Structural basis of substrate-specificity in the serine proteases. Protein Sci. 4:1995;337-360
40. Raivio T.L., Silhavy T.J. Periplasmic stress and ECF sigma factors. Annu. Rev. Microbiol. 55:2001;591-624
41. Rouviere P.E., De Las Penas A., Mecsas J., Lu C.Z., Rudd K.E., Gross C.A. rpoE, the gene encoding the second heat-shock sigma factor, sigma E, in Escherichia coli. EMBO J. 14:1995;1032-1042
42. Shridhar V., Sen A., Chien J., Staub J., Avula R., Kovats S., Lee J., Lillie J., Smith D.I. Identification of underexpressed genes in early- and late-stage primary ovarian tumors by suppression subtraction hybridization. Cancer Res. 62:2002;262-270
43. Songyang Z., Fanning A.S., Fu C., Xu J., Marfatia S.M., Chishti A.H., Crompton A., Chan A.C., Anderson J.M., Cantley L.C. Recognition of unique carboxyl-terminal motifs by distinct PDZ domains. Science. 275:1997;73-77
44. Srinivasula S.M., Gupta S., Datta P., Zhang Z., Hegde R., Cheong N., Fernandes-Alnemri T., Alnemri E.S. Inhibitor of apoptosis proteins are substrates for the mitochondrial serine protease Omi/HtrA2. J. Biol. Chem. 278:2003;31469-31472
45. Straus D., Walter W., Gross C.A. DnaK, DnaJ, and GrpE heat shock proteins negatively regulate heat shock gene expression by controlling the synthesis and stability of sigma 32. Genes Dev. 4:1990;2202-2209
46. Walsh N.P., Alba B.M., Bose B., Gross C.A., Sauer R.T. OMP peptide signals initiate the envelope-stress response by activating DegS protease via relief of inhibition mediated by its PDZ domain. Cell. 113:2003;61-71
47. Wickner S., Maurizi M.R., Gottesman S. Posttranslational quality control. Folding, refolding, and degrading proteins Science. 286:1999;1888-1893
48. Yamaguchi H., Bhalla K., Wang H.G. Bax plays a pivotal role in thapsigargin-induced apoptosis of human colon cancer HCT116 cells by controlling Smac/Diablo and Omi/HtrA2 release from mitochondria. Cancer Res. 63:2003;1483-1489
49. Yang Q.H., Church-Hajduk R., Ren J., Newton M.L., Du C. Omi/HtrA2 catalytic cleavage of inhibitor of apoptosis (IAP) irreversibly inactivates IAPs and facilitates caspase activity in apoptosis. Genes Dev. 17:2003;1487-1496
50. Young J.C., Hartl F.U. A stress sensor for the bacterial periplasm. Cell. 113:2003;1-2