XProteolysis inside the membrane is a rate-governed reaction not driven by Substrate Affinity

Cell

Volumn 155, Issue 6, 2013, Pages

  Dickey, Seth W ^a   Baker, Rosanna P ^a   Cho, Sangwoo ^a   Urban, Siniša ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEUTERIUM OXIDE; FLUORESCEIN ISOTHIOCYANATE; MEMBRANE PROTEIN; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; PROTEINASE; PROTEOLIPOSOME; RHOMBOID PROTEASE; TATA BINDING PROTEIN; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; ESCHERICHIA COLI PROTEIN; GLPG PROTEIN, E COLI; LIPOSOME;

AQUIFEX AEOLICUS; ARTICLE; BACTERIAL CELL; BINDING AFFINITY; CATALYSIS; CELL DIVISION; CIRCULAR DICHROISM; DISSOCIATION; DRUG DESIGN; ENZYME ACTIVITY; ENZYME SUBSTRATE; ESCHERICHIA COLI; GEL FILTRATION; HYDROLYSIS; INDUCIBLE MEMBRANE RECONSTITUTION SYSTEM; KINETICS; MASS SPECTROMETRY; MEMBRANE RECONSTITUTION; MICELLE; MICHAELIS MENTEN KINETICS; PH; PRECIPITATION; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROVIDENCIA STUARTII; QUANTITATIVE ANALYSIS; STEADY STATE; ULTRACENTRIFUGATION; AMINO ACID SEQUENCE; BACTERIUM; CELL MEMBRANE; CHEMICAL STRUCTURE; CHEMISTRY; CYTOLOGY; ENZYMOLOGY; METABOLISM; MOLECULAR GENETICS; SEQUENCE ALIGNMENT; BACTERIA;

AMINO ACID SEQUENCE; BACTERIA; CELL MEMBRANE; DNA-BINDING PROTEINS; ENDOPEPTIDASES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; KINETICS; LIPOSOMES; MEMBRANE PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEOLYSIS; SEQUENCE ALIGNMENT;

EID: 84890087383     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2013.10.053     Document Type: Article

References (56)

1. C. Adrain, and M. Freeman New lives for old: evolution of pseudoenzyme function illustrated by iRhoms Nat. Rev. Mol. Cell Biol. 13 2012 489 498
2. R.P. Baker, and S. Urban Architectural and thermodynamic principles underlying intramembrane protease function Nat. Chem. Biol. 8 2012 759 768
3. R.P. Baker, K. Young, L. Feng, Y. Shi, and S. Urban Enzymatic analysis of a rhomboid intramembrane protease implicates transmembrane helix 5 as the lateral substrate gate Proc. Natl. Acad. Sci. USA 104 2007 8257 8262
4. T. Casci, and M. Freeman Control of EGF receptor signalling: lessons from fruitflies Cancer Metastasis Rev. 18 1999 181 201
5. L. Chávez-Gutiérrez, L. Bammens, I. Benilova, A. Vandersteen, M. Benurwar, M. Borgers, S. Lismont, L. Zhou, S. Van Cleynenbreugel, and H. Esselmann The mechanism of γ-Secretase dysfunction in familial Alzheimer disease EMBO J. 31 2012 2261 2274
6. G. Deckert, P.V. Warren, T. Gaasterland, W.G. Young, A.L. Lenox, D.E. Graham, R. Overbeek, M.A. Snead, M. Keller, and M. Aujay The complete genome of the hyperthermophilic bacterium Aquifex aeolicus Nature 392 1998 353 358
7. B. De Strooper, and W. Annaert Novel research horizons for presenilins and γ-secretases in cell biology and disease Annu. Rev. Cell Dev. Biol. 26 2010 235 260
8. A. Doucet, G.S. Butler, D. Rodríguez, A. Prudova, and C.M. Overall Metadegradomics: toward in vivo quantitative degradomics of proteolytic post-translational modifications of the cancer proteome Mol. Cell. Proteomics 7 2008 1925 1951
9. M. Drag, and G.S. Salvesen Emerging principles in protease-based drug discovery Nat. Rev. Drug Discov. 9 2010 690 701
10. J.P. Elrod, J.L. Hogg, D.M. Quinn, K.S. Venkatasubban, and R.L. Schowen Protonic reorganization and substrate structure in catalysis by serine proteases J. Am. Chem. Soc. 102 1980 3917 3922
11. A. Fersht Structure and Mechanism in Protein Science: A Guide to Enzyme Catalysis and Protein Folding 1999 W.H. Freeman and Company New York
12. L. Fleig, N. Bergbold, P. Sahasrabudhe, B. Geiger, L. Kaltak, and M.K. Lemberg Ubiquitin-dependent intramembrane rhomboid protease promotes ERAD of membrane proteins Mol. Cell 47 2012 558 569
13. R. Fluhrer, H. Steiner, and C. Haass Intramembrane proteolysis by signal peptide peptidases: a comparative discussion of GXGD-type aspartyl proteases J. Biol. Chem. 284 2009 13975 13979
14. J.I. Friedman, and J.T. Stivers Detection of damaged DNA bases by DNA glycosylase enzymes Biochemistry 49 2010 4957 4967
15. M. Gallio, G. Sturgill, P. Rather, and P. Kylsten A conserved mechanism for extracellular signaling in eukaryotes and prokaryotes Proc. Natl. Acad. Sci. USA 99 2002 12208 12213
16. J.P. Hummel, and W.J. Dreyer Measurement of protein-binding phenomena by gel filtration Biochim. Biophys. Acta 63 1962 530 532
17. J.A. Huntington Thrombin plasticity Biochim. Biophys. Acta 1824 2012 246 252
18. N.A. Kuznetsov, V.V. Koval, G.A. Nevinsky, K.T. Douglas, D.O. Zharkov, and O.S. Fedorova Kinetic conformational analysis of human 8-oxoguanine-DNA glycosylase J. Biol. Chem. 282 2007 1029 1038
19. C. Lazareno-Saez, E. Arutyunova, N. Coquelle, and M.J. Lemieux Domain swapping in the cytoplasmic domain of the Escherichia coli rhomboid protease J. Mol. Biol. 425 2013 1127 1142
20. M.K. Lemberg, and M. Freeman Functional and evolutionary implications of enhanced genomic analysis of rhomboid intramembrane proteases Genome Res. 17 2007 1634 1646
21. X. Li, B. Wang, L. Feng, H. Kang, Y. Qi, J. Wang, and Y. Shi Cleavage of RseA by RseP requires a carboxyl-terminal hydrophobic amino acid following DegS cleavage Proc. Natl. Acad. Sci. USA 106 2009 14837 14842
22. X. Li, S. Dang, C. Yan, X. Gong, J. Wang, and Y. Shi Structure of a presenilin family intramembrane aspartate protease Nature 493 2013 56 61
23. C. López-Otín, and J.S. Bond Proteases: multifunctional enzymes in life and disease J. Biol. Chem. 283 2008 30433 30437
24. H. Makinoshima, and M.S. Glickman Site-2 proteases in prokaryotes: regulated intramembrane proteolysis expands to microbial pathogenesis Microbes Infect. 8 2006 1882 1888
25. S.M. Moin, and S. Urban Membrane immersion allows rhomboid proteases to achieve specificity by reading transmembrane segment dynamics Elife 1 2012 e00173
26. P. Osenkowski, W. Ye, R. Wang, M.S. Wolfe, and D.J. Selkoe Direct and potent regulation of gamma-secretase by its lipid microenvironment J. Biol. Chem. 283 2008 22529 22540
27. J.J. Perona, and C.S. Craik Evolutionary divergence of substrate specificity within the chymotrypsin-like serine protease fold J. Biol. Chem. 272 1997 29987 29990
28. P.N. Rather, X. Ding, R.R. Baca-DeLancey, and S. Siddiqui Providencia stuartii genes activated by cell-to-cell signaling and identification of a gene required for production or activity of an extracellular factor J. Bacteriol. 181 1999 7185 7191
29. C.A. Schnaitman Examination of the protein composition of the cell envelope of Escherichia coli by polyacrylamide gel electrophoresis J. Bacteriol. 104 1970 882 889
30. C.A. Schnaitman Protein composition of the cell wall and cytoplasmic membrane of Escherichia coli J. Bacteriol. 104 1970 890 901
31. S. Shah, S.F. Lee, K. Tabuchi, Y.H. Hao, C. Yu, Q. LaPlant, H. Ball, C.E. Dann 3rd, T. Südhof, and G. Yu Nicastrin functions as a gamma-secretase-substrate receptor Cell 122 2005 435 447
32. H.R. Stennicke, M. Renatus, M. Meldal, and G.S. Salvesen Internally quenched fluorescent peptide substrates disclose the subsite preferences of human caspases 1, 3, 6, 7 and 8 Biochem. J. 350 2000 563 568
33. L.G. Stevenson, K. Strisovsky, K.M. Clemmer, S. Bhatt, M. Freeman, and P.N. Rather Rhomboid protease AarA mediates quorum-sensing in Providencia stuartii by activating TatA of the twin-arginine translocase Proc. Natl. Acad. Sci. USA 104 2007 1003 1008
34. K. Strisovsky, H.J. Sharpe, and M. Freeman Sequence-specific intramembrane proteolysis: identification of a recognition motif in rhomboid substrates Mol. Cell 36 2009 1048 1059
35. J.C. Timmer, W. Zhu, C. Pop, T. Regan, S.J. Snipas, A.M. Eroshkin, S.J. Riedl, and G.S. Salvesen Structural and kinetic determinants of protease substrates Nat. Struct. Mol. Biol. 16 2009 1101 1108
36. S. Urban Making the cut: central roles of intramembrane proteolysis in pathogenic microorganisms Nat. Rev. Microbiol. 7 2009 411 423
37. S. Urban Taking the plunge: integrating structural, enzymatic and computational insights into a unified model for membrane-immersed rhomboid proteolysis Biochem. J. 425 2010 501 512
38. S. Urban, and M.S. Wolfe Reconstitution of intramembrane proteolysis in vitro reveals that pure rhomboid is sufficient for catalysis and specificity Proc. Natl. Acad. Sci. USA 102 2005 1883 1888
39. S. Urban, and R.P. Baker In vivo analysis reveals substrate-gating mutants of a rhomboid intramembrane protease display increased activity in living cells Biol. Chem. 389 2008 1107 1115
40. S. Urban, and S.W. Dickey The rhomboid protease family: a decade of progress on function and mechanism Genome Biol. 12 2011 231
41. K.R. Vinothkumar, K. Strisovsky, A. Andreeva, Y. Christova, S. Verhelst, and M. Freeman The structural basis for catalysis and substrate specificity of a rhomboid protease EMBO J. 29 2010 3797 3809
42. P.J. Wilderman, A.I. Vasil, W.E. Martin, R.C. Murphy, and M.L. Vasil Pseudomonas aeruginosa synthesizes phosphatidylcholine by use of the phosphatidylcholine synthase pathway J. Bacteriol. 184 2002 4792 4799
43. M.S. Wolfe Intramembrane proteolysis Chem. Rev. 109 2009 1599 1612
44. M. Wysocka, A. Lesner, A. Legowska, A. Jaśkiewicz, H. Miecznikowska, and K. Rolka Designing of substrates and inhibitors of bovine alpha-chymotrypsin with synthetic phenylalanine analogues in position P(1) Protein Pept. Lett. 15 2008 260 264
45. Y. Xue, and Y. Ha Catalytic mechanism of rhomboid protease GlpG probed by 3,4-dichloroisocoumarin and diisopropyl fluorophosphonate J. Biol. Chem. 287 2012 3099 3107
46. Y. Xue, S. Chowdhury, X. Liu, Y. Akiyama, J. Ellman, and Y. Ha Conformational change in rhomboid protease GlpG induced by inhibitor binding to its S' subsites Biochemistry 51 2012 3723 3731
47. D. Zhang, and I.M. Kovach Deuterium solvent isotope effect and proton-inventory studies of factor Xa-catalyzed reactions Biochemistry 45 2006 14175 14182
48. Y. Zhou, S.M. Moin, S. Urban, and Y. Zhang An internal water-retention site in the rhomboid intramembrane protease GlpG ensures catalytic efficiency Structure 20 2012 1255 1263
49. A.T. Brünger, P.D. Adams, G.M. Clore, W.L. DeLano, P. Gros, R.W. Grosse-Kunstleve, J.S. Jiang, J. Kuszewski, M. Nilges, and N.S. Pannu Crystallography & NMR system: a new software suite for macromolecular structure determination Acta Crystallogr. D Biol. Crystallogr. 54 1998 905 921
50. Collaborative Computational Project, Number 4 The CCP4 suite: programs for protein crystallography Acta Crystallogr. D Biol. Crystallogr. 50 1994 760 763
51. K.A. Datsenko, and B.L. Wanner One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products Proc. Natl. Acad. Sci. USA 97 2000 6640 6645
52. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. D Biol. Crystallogr. 60 2004 2126 2132
53. G.N. Murshudov, P. Skubák, A.A. Lebedev, N.S. Pannu, R.A. Steiner, R.A. Nicholls, M.D. Winn, F. Long, and A.A. Vagin REFMAC5 for the refinement of macromolecular crystal structures Acta Crystallogr. D Biol. Crystallogr. 67 2011 355 367
54. Z. Otwinowski, and W. Minor Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol. 276 1997 307 326
55. O.A. Pierrat, K. Strisovsky, Y. Christova, J. Large, K. Ansell, N. Bouloc, E. Smiljanic, and M. Freeman Monocyclic β-lactams are selective, mechanism-based inhibitors of rhomboid intramembrane proteases ACS Chem. Biol. 6 2011 325 335
56. Z. Wu, N. Yan, L. Feng, A. Oberstein, H. Yan, R.P. Baker, L. Gu, P.D. Jeffrey, S. Urban, and Y. Shi Structural analysis of a rhomboid family intramembrane protease reveals a gating mechanism for substrate entry Nat. Struct. Mol. Biol. 13 2006 1084 1091