Inhibitors of rhomboid proteases

Biochimie

Volumn 122, Issue , 2016, Pages 38-47

  Wolf, Eliane V ^a   Verhelst, Steven H L ^b,c  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b LEIBNIZ INSTITUT FÜR ANALYTISCHE WISSENSCHAFTEN ISAS E V   (Germany)

^c UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Activity based probes; Inhibitors; Intramembrane proteases; Rhomboids

Indexed keywords

ELECTROPHILE; HISTIDINE; PROTEINASE; PROTEINASE INHIBITOR; REAGENT; SERINE; PEPTIDE HYDROLASE; PROTEIN BINDING;

ARTICLE; COVALENT BOND; ENZYME ACTIVE SITE; ENZYME SUBSTRATE COMPLEX; ESCHERICHIA COLI; HIGH THROUGHPUT SCREENING; MOLECULAR RECOGNITION; PROTEIN FAMILY; BIOCATALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; DRUG DEVELOPMENT; DRUG EFFECTS; METABOLISM; MOLECULAR MODEL; PROCEDURES; PROTEIN TERTIARY STRUCTURE; STRUCTURE ACTIVITY RELATION;

BIOCATALYSIS; CATALYTIC DOMAIN; DRUG DISCOVERY; MODELS, MOLECULAR; MOLECULAR STRUCTURE; PEPTIDE HYDROLASES; PROTEASE INHIBITORS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84957840802     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2015.07.007     Document Type: Review

References (73)

1. R.B. Rawson, N.G. Zelenski, D. Nijhawan, J. Ye, J. Sakai, M.T. Hasan, T.Y. Chang, M.S. Brown, and J.L. Goldstein Complementation cloning of S2P, a gene encoding a putative metalloprotease required for intramembrane cleavage of SREBPs Mol. Cell 1 1997 47 57
2. M.S. Wolfe, and R. Kopan Intramembrane proteotysis: theme and variations Science 305 2004 1119 1123
3. M.S. Wolfe Intramembrane proteolysis Chem. Rev. 109 2009 1599 1612
4. M.K. Lemberg Intramembrane proteolysis in regulated protein trafficking Traffic 12 2011 1109 1118
5. K. Strisovsky Structural and mechanistic principles of intramembrane proteolysis-lessons from rhomboids FEBS J. 280 2013 1579 1603
6. D. Langosch, C. Scharnagl, H. Steiner, and M.K. Lemberg Understanding intramembrane proteolysis: from protein dynamics to reaction kinetics Trends Biochem. Sci. 40 2015 318 327
7. A. Weihofen, K. Binns, M.K. Lemberg, K. Ashman, and B. Martoglio Identification of signal peptide peptidase, a presenilin-type aspartic protease Science 296 2002 2215 2218
8. M.S. Wolfe, W. Xia, C.L. Moore, D.D. Leatherwood, B. Ostaszewski, T. Rahmati, I.O. Donkor, and D.J. Selkoe Peptidomimetic probes and molecular modeling suggest that Alzheimer's gamma-secretase is an intramembrane-cleaving aspartyl protease Biochemistry 38 1999 4720 4727
9. M.S. Wolfe, W. Xia, B.L. Ostaszewski, T.S. Diehl, W.T. Kimberly, and D.J. Selkoe Two transmembrane aspartates in presenilin-1 required for presenilin endoproteolysis and gamma-secretase activity Nature 398 1999 513 517
10. I. Manolaridis, K. Kulkarni, R.B. Dodd, S. Ogasawara, Z. Zhang, G. Bineva, N. O'Reilly, S.J. Hanrahan, A.J. Thompson, N. Cronin, S. Iwata, and D. Barford Mechanism of farnesylated CAAX protein processing by the intramembrane protease Rce1 Nature 504 2013 301 305
11. S. Urban, J.R. Lee, and M. Freeman Drosophila Rhomboid-1 defines a family of putative intramembrane serine proteases Cell 107 2001 173 182
12. J.R. Lee, S. Urban, C.F. Garvey, and M. Freeman Regulated intracellular ligand transport and proteolysis control EGF signal activation in Drosophila Cell 107 2001 161 171
13. E.V. Koonin, K.S. Makarova, I.B. Rogozin, L. Davidovic, M.C. Letellier, and L. Pellegrini The rhomboids: a nearly ubiquitous family of intramembrane serine proteases that probably evolved by multiple ancient horizontal gene transfers Genome Biol. 4 2003 R19
14. M.K. Lemberg, and M. Freeman Functional and evolutionary implications of enhanced genomic analysis of rhomboid intramembrane proteases Genome Res. 17 2007 1634 1646
15. 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. U. S. A. 104 2007 1003 1008
16. T.J. Dowse, J.C. Pascall, K.D. Brown, and D. Soldati Apicomplexan rhomboids have a potential role in microneme protein cleavage during host cell invasion Int. J. Parasitol. 35 2005 747 756
17. S.A. Howell, F. Hackett, A.M. Jongco, C. Withers-Martinez, K. Kim, V.B. Carruthers, and M.J. Blackman Distinct mechanisms govern proteolytic shedding of a key invasion protein in apicomplexan pathogens Mol. Microbiol. 57 2005 1342 1356
18. F. Brossier, T.J. Jewett, L.D. Sibley, and S. Urban A spatially localized rhomboid protease cleaves cell surface adhesins essential for invasion by Toxoplasma Proc. Natl. Acad. Sci. U. S. A. 102 2005 4146 4151
19. R.P. Baker, R. Wijetilaka, and S. Urban Two Plasmodium rhomboid proteases preferentially cleave different adhesins implicated in all invasive stages of malaria PLoS Pathog. 2 2006 e113
20. G.A. McQuibban, S. Saurya, and M. Freeman Mitochondrial membrane remodelling regulated by a conserved rhomboid protease Nature 423 2003 537 541
21. M. Herlan, F. Vogel, C. Bornhovd, W. Neupert, and A.S. Reichert Processing of Mgm1 by the rhomboid-type protease Pcp1 is required for maintenance of mitochondrial morphology and of mitochondrial DNA J. Biol. Chem. 278 2003 27781 27788
22. H. Sesaki, S.M. Southard, A.E. Hobbs, and R.E. Jensen Cells lacking Pcp1p/Ugo2p, a rhomboid-like protease required for Mgm1p processing, lose mtDNA and mitochondrial structure in a Dnm1p-dependent manner, but remain competent for mitochondrial fusion Biochem. Biophys. Res. Commun. 308 2003 276 283
23. S. Cipolat, T. Rudka, D. Hartmann, V. Costa, L. Serneels, K. Craessaerts, K. Metzger, C. Frezza, W. Annaert, L. D'Adamio, C. Derks, T. Dejaegere, L. Pellegrini, R. D'Hooge, L. Scorrano, and B. De Strooper Mitochondrial rhomboid PARL regulates cytochrome c release during apoptosis via OPA1-dependent cristae remodeling Cell 126 2006 163 175
24. E. Deas, H. Plun-Favreau, S. Gandhi, H. Desmond, S. Kjaer, S.H. Loh, A.E. Renton, R.J. Harvey, A.J. Whitworth, L.M. Martins, A.Y. Abramov, and N.W. Wood PINK1 cleavage at position A103 by the mitochondrial protease PARL Hum. Mol. Genet. 20 2011 867 879
25. C. Meissner, H. Lorenz, A. Weihofen, D.J. Selkoe, and M.K. Lemberg The mitochondrial intramembrane protease PARL cleaves human Pink1 to regulate Pink1 trafficking J. Neurochem. 117 2011 856 867
26. S. Maegawa, K. Ito, and Y. Akiyama Proteolytic action of GlpG, a rhomboid protease in the Escherichia coli cytoplasmic membrane Biochemistry 44 2005 13543 13552
27. 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
28. 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. U. S. A. 102 2005 1883 1888
29. S.M. Moin, and S. Urban Membrane immersion allows rhomboid proteases to achieve specificity by reading transmembrane segment dynamics eLife 1 2012 e00173
30. E. Arutyunova, P. Panwar, P.M. Skiba, N. Gale, M.W. Mak, and M.J. Lemieux Allosteric regulation of rhomboid intramembrane proteolysis EMBO J. 33 2014 1869 1881
31. Y. Xue, and Y. Ha Large lateral movement of transmembrane helix S5 is not required for substrate access to the active site of rhomboid intramembrane protease J. Biol. Chem. 288 2013 16645 16654
32. M.K. Lemberg, J. Menendez, A. Misik, M. Garcia, C.M. Koth, and M. Freeman Mechanism of intramembrane proteolysis investigated with purified rhomboid proteases EMBO J. 24 2005 464 472
33. 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
34. S. Zoll, S. Stanchev, J. Began, J. Skerle, M. Lepsik, L. Peclinovska, P. Majer, and K. Strisovsky Substrate binding and specificity of rhomboid intramembrane protease revealed by substrate-peptide complex structures EMBO J. 33 2014 2408 2421
35. E.V. Wolf, A. Zeissler, O. Vosyka, E. Zeiler, S. Sieber, and S.H. Verhelst A new class of rhomboid protease inhibitors discovered by activity-based fluorescence polarization PLoS One 8 2013 e72307
36. J.M. Antos, G.L. Chew, C.P. Guimaraes, N.C. Yoder, G.M. Grotenbreg, M.W. Popp, and H.L. Ploegh Site-specific N- and C-terminal labeling of a single polypeptide using sortases of different specificity J. Am. Chem. Soc. 131 2009 10800 10801
37. O. Vosyka, K.R. Vinothkumar, E.V. Wolf, A.J. Brouwer, R.M. Liskamp, and S.H.L. Verhelst Activity-based probes for rhomboid proteases discovered in a mass spectrometry-based assay Proc. Natl. Acad. Sci. U. S. A. 110 2013 2472 2477
38. S.S. Twining Fluorescein isothiocyanate-labeled casein assay for proteolytic enzymes Anal. Biochem. 143 1984 30 34
39. L.J. Jones, R.H. Upson, R.P. Haugland, N. Panchuk-Voloshina, M. Zhou, and R.P. Haugland Quenched BODIPY dye-labeled casein substrates for the assay of protease activity by direct fluorescence measurement Anal. Biochem. 251 1997 144 152
40. Y. Wang, Y. Zhang, and Y. Ha Crystal structure of a rhomboid family intramembrane protease Nature 444 2006 179 180
41. 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
42. 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
43. O.A. Pierrat, K. Strisovsky, Y. Christova, J. Large, K. Ansell, N. Bouloc, E. Smiljanic, and M. Freeman Monocyclic beta-lactams are selective, mechanism-based inhibitors of rhomboid intramembrane proteases ACS Chem. Biol. 6 2011 325 335
44. S.W. Dickey, R.P. Baker, S. Cho, and S. Urban Proteolysis inside the membrane is a rate-governed reaction not driven by substrate affinity Cell 155 2013 1270 1281
45. A.R. Sherratt, D.R. Blais, H. Ghasriani, J.P. Pezacki, and N.K. Goto Activity-based protein profiling of the Escherichia coli GlpG rhomboid protein delineates the catalytic core Biochemistry 51 2012 7794 7803
46. E.V. Wolf, M. Seybold, R. Hadravova, K. Strisovsky, and S.H.L. Verhelst Activity-based protein profiling of rhomboid proteases in liposomes ChemBioChem 2015 10.1002/cbic.201500213 (in press)
47. D.V. Jeyaraju, H.M. McBride, R.B. Hill, and L. Pellegrini Structural and mechanistic basis of Parl activity and regulation Cell Death Differ. 18 2011 1531 1539
48. S. Sekine, Y. Kanamaru, M. Koike, A. Nishihara, M. Okada, H. Kinoshita, M. Kamiyama, J. Maruyama, Y. Uchiyama, N. Ishihara, K. Takeda, and H. Ichijo Rhomboid protease PARL mediates the mitochondrial membrane potential loss-induced cleavage of PGAM5 J. Biol. Chem. 287 2012 34635 34645
49. T.L. Cheng, Y.T. Wu, H.Y. Lin, F.C. Hsu, S.K. Liu, B.I. Chang, W.S. Chen, C.H. Lai, G.Y. Shi, and H.L. Wu Functions of rhomboid family protease RHBDL2 and thrombomodulin in wound healing J. Invest Dermatol. 131 2011 2486 2494
50. J.W. Harper, K. Hemmi, and J.C. Powers Reaction of serine proteases with substituted isocoumarins - discovery of 3,4-dichloroisocoumarin, a new general mechanism based serine protease inhibitor Biochemistry 24 1985 1831 1841
51. 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
52. J. Vijayalakshmi, E.F. Meyer, C.M. Kam, and J.C. Powers Structural study of porcine pancreatic elastase complexed with 7-Amino-3-(2-Bromoethoxy)-4-Chloroisocoumarin as a nonreactivatable doubly covalent enzyme-inhibitor complex Biochemistry 30 1991 2175 2183
53. K.R. Vinothkumar, O.A. Pierrat, J.M. Large, and M. Freeman Structure of rhomboid protease in complex with beta-lactam inhibitors defines the S2′ cavity Structure 21 2013 1051 1058
54. J.C. Powers, J.L. Asgian, O.D. Ekici, and K.E. James Irreversible inhibitors of serine, cysteine, and threonine proteases Chem. Rev. 102 2002 4639 4750
55. U. Haedke, E.V. Kuttler, O. Vosyka, Y. Yang, and S.H.L. Verhelst Tuning probe selectivity for chemical proteomics applications Curr. Opin. Chem. Biol. 17 2013 102 109
56. S. Serim, U. Haedke, and S.H.L. Verhelst Activity-based probes for the study of proteases: recent advances and developments ChemMedChem 7 2012 1146 1159
57. L.E. Sanman, and M. Bogyo Activity-based profiling of proteases Annu. Rev. Biochem. 83 2014 249 273
58. Y.S. Liu, M.P. Patricelli, and B.F. Cravatt Activity-based protein profiling: the serine hydrolases Proc. Natl. Acad. Sci. U. S. A. 96 1999 14694 14699
59. D. Kidd, Y.S. Liu, and B.F. Cravatt Profiling serine hydrolase activities in complex proteomes Biochemistry 40 2001 4005 4015
60. D.A. Bachovchin, S.J. Brown, H. Rosen, and B.F. Cravatt Identification of selective inhibitors of uncharacterized enzymes by high-throughput screening with fluorescent activity-based probes Nat. Biotechnol. 27 2009 387 394
61. 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
62. A. Ben-Shem, D. Fass, and E. Bibi Structural basis for intramembrane proteolysis by rhomboid serine proteases Proc. Natl. Acad. Sci. U. S. A. 104 2007 462 466
63. M.J. Lemieux, S.J. Fischer, M.M. Cherney, K.S. Bateman, and M.N. James The crystal structure of the rhomboid peptidase from Haemophilus influenzae provides insight into intramembrane proteolysis Proc. Natl. Acad. Sci. U. S. A. 104 2007 750 754
64. 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. U. S. A. 104 2007 8257 8262
65. 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
66. R.P. Baker, and S. Urban Cytosolic extensions directly regulate a rhomboid protease by modulating substrate gating Nature 523 2015 101 105
67. 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
68. T. Bottcher, and S.A. Sieber beta-lactones as privileged structures for the active-site labeling of versatile bacterial enzyme classes Angew. Chem. Int. Ed. 47 2008 4600 4603
69. P. Kasperkiewicz, M. Poreba, S.J. Snipas, H. Parker, C.C. Winterbourn, G.S. Salvesen, and M. Drag Design of ultrasensitive probes for human neutrophil elastase through hybrid combinatorial substrate library profiling Proc. Natl. Acad. Sci. U. S. A. 111 2014 2518 2523
70. T. Reddy, and J.K. Rainey Multifaceted substrate capture scheme of a rhomboid protease J. Phys. Chem. B 116 2012 8942 8954
71. 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
72. J. Singh, R.C. Petter, T.A. Baillie, and A. Whitty The resurgence of covalent drugs Nat. Rev. Drug Discov. 10 2011 307 317
73. R.A. Bauer Covalent inhibitors in drug discovery: from accidental discoveries to avoided liabilities and designed therapies Drug Discov. Today 2015 10.1016/j.drugdis.2015.05.005 (in press)