Towards the control of intracellular protein turnover: Mitochondrial Lon protease inhibitors versus proteasome inhibitors

Biochimie

Volumn 90, Issue 2, 2008, Pages 260-269

  Bayot, Aurélien ^a   Basse, Nicolas ^b   Lee, Irene ^c   Gareil, Monique ^a   Pirotte, Bernard ^d   Bulteau, Anne Laure ^a   Friguet, Bertrand ^a   Reboud Ravaux, Michèle ^b  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b CNRS   (France)

^c CASE WESTERN RESERVE UNIVERSITY   (United States)

^d UNIVERSITY OF LIÈGE   (Belgium)

Author keywords

Coumarinic derivatives; Lon protease inhibitors; Proteasome inhibitors

Indexed keywords

PROTEASOME INHIBITOR; PROTEINASE INHIBITOR;

ARTICLE; CATALYSIS; ENZYME STRUCTURE; EUKARYOTE; HUMAN; MITOCHONDRIAL MEMBRANE; NONHUMAN; PROTEIN METABOLISM;

CATALYSIS; HUMANS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; PROTEASE INHIBITORS; PROTEASE LA; PROTEASOME ENDOPEPTIDASE COMPLEX;

EUKARYOTA;

EID: 38749126464     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2007.10.010     Document Type: Article

References (76)

1. Bulteau A.L., Szweda L.I., and Friguet B. Mitochondrial protein oxidation and degradation in response to oxidative stress and aging. Exp. Gerontol. 41 (2006) 653-657
2. Bartoli M., and Richard I. Calpains in muscle wasting. Int. J. Biochem. Cell Biol. 37 (2005) 2115-2133
3. Béchet D., Tassa A., Taillandier D., Combaret L., and Attaix D. Lysosomal proteolysis in skeletal muscle. Int. J. Biochem. Cell Biol. 37 (2005) 2098-2114
4. Meijer A.J., and Codogno P. Signalling and autophagy regulation in health, aging and disease. Mol. Aspects Med. 27 (2006) 411-425
5. Dahlmann B. Proteasomes. Essays Biochem. 41 (2005) 31-48
6. Bader N., and Grune T. Protein oxidation and proteolysis. Biol. Chem. 387 (2006) 1351-1355
7. Leidhold C., and Voos W. Chaperones and proteases: guardians of protein integrity in eukaryotic organelles. Ann. N.Y. Acad. Sci. 1113 (2007) 72-86
8. Escobar-Henriques M., and Langer T. Mitochondrial shaping cuts. Biochim. Biophys. Acta 1763 (2006) 422-429
9. Bota D.A., Ngo J.K., and Davies K.J. Downregulation of the human Lon protease impairs mitochondrial structure and function and causes cell death. Free Radic. Biol. Med. 38 (2005) 665-677
10. Lu B., Yadav S., Shah P.G., Liu T., Tian B., Pukszta S., Villaluna N., Kutejova E., Newlon C.S., Santos J.H., and Suzuki C.K. Roles for the human ATP-dependent Lon protease in mitochondrial DNA maintenance. J. Biol. Chem. 282 (2007) 17363-17374
11. Bota D.A., and Davies K.J. Lon protease preferentially degrades oxidized mitochondrial aconitase by an ATP-stimulated mechanism. Nat. Cell Biol. 4 (2002) 674-680
12. Bulteau A.L., Ikeda-Saito M., and Szweda L.I. Redox-dependent modulation of aconitase activity in intact mitochondria. Biochemistry 42 (2003) 14846-14855
13. Suzuki C.K., Rep M., van Dijl J.M., Suda K., Grivell L.A., and Schatz G. ATP-dependent proteases that also chaperone protein biogenesis. Trends Biochem. Sci. 22 (1997) 118-123
14. Liu T., Lu B., Lee I., Ondrovicova G., Kutejova E., and Suzuki C.K. DNA and RNA binding by the mitochondrial lon protease is regulated by nucleotide and protein substrate. J. Biol. Chem. 279 (2004) 13902-13910
15. Borissenko L., and Groll M. 20S proteasome and its inhibitors: crystallographic knowledge for drug development. Chem. Rev. 107 (2007) 687-717
16. Watanabe N., and Yamada S. Activation of 20S proteasomes from spinach leaves by fatty acids. Plant Cell Physiol. 37 (1996) 147-151
17. Dahlmann B., Rutschmann M., Kuehn L., and Reinauer H. Activation of the multicatalytic proteinase from rat skeletal muscle by fatty acids or sodium dodecyl sulphate. Biochem. J. 228 (1985) 171-177
18. Ciechanover A. Intracellular protein degradation: from a vague idea, through the lysosome and the ubiquitin-proteasome system, and onto human diseases and drug targeting (Nobel lecture). Angew Chem. Int. Ed. Engl. 44 (2005) 5944-5967
19. Brannigan J.A., Dodson G., Duggleby H.J., Moody P.C., Smith J.L., Tomchick D.R., and Murzin A.G. A protein catalytic framework with an N-terminal nucleophile is capable of self-activation. Nature 378 (1995) 416-419
20. Groll M., Ditzel L., Lowe J., Stock D., Bochtler M., Bartunik H.D., and Huber R. Structure of 20S proteasome from yeast at 2.4 A resolution. Nature 386 (1997) 463-471
21. Unno M., Mizushima T., Morimoto Y., Tomisugi Y., Tanaka K., Yasuoka N., and Tsukihara T. The structure of the mammalian 20S proteasome at 2.75 A resolution. Structure 10 (2002) 609-618
22. Ditzel L., Huber R., Mann K., Heinemeyer W., Wolf D.H., and Groll M. Conformational constraints for protein self-cleavage in the proteasome. J. Mol. Biol. 279 (1998) 1187-1191
23. Groll M., Heinemeyer W., Jager S., Ullrich T., Bochtler M., Wolf D.H., and Huber R. The catalytic sites of 20S proteasomes and their role in subunit maturation: a mutational and crystallographic study. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 10976-10983
24. Groll M., Nazif T., Huber R., and Bogyo M. Probing structural determinants distal to the site of hydrolysis that control substrate specificity of the 20S proteasome. Chem. Biol. 9 (2002) 655-662
25. Groll M., Huber R., and Potts B.C. Crystal structures of Salinosporamide A (NPI-0052) and B (NPI-0047) in complex with the 20S proteasome reveal important consequences of beta-lactone ring opening and a mechanism for irreversible binding. J. Am. Chem. Soc. 128 (2006) 5136-5141
26. Wang N., Gottesman S., Willingham M.C., Gottesman M.M., and Maurizi M.R. A human mitochondrial ATP-dependent protease that is highly homologous to bacterial Lon protease. Proc. Natl. Acad. Sci. U.S.A. 90 (1993) 11247-11251
27. Botos I., Melnikov E.E., Cherry S., Tropea J.E., Khalatova A.G., Rasulova F., Dauter Z., Maurizi M.R., Rotanova T.V., Wlodawer A., and Gustchina A. The catalytic domain of Escherichia coli Lon protease has a unique fold and a Ser-Lys dyad in the active site. J. Biol. Chem. 279 (2004) 8140-8148
28. Stahlberg H., Kutejova E., Suda K., Wolpensinger B., Lustig A., Schatz G., Engel A., and Suzuki C.K. Mitochondrial Lon of Saccharomyces cerevisiae is a ring-shaped protease with seven flexible subunits. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 6787-6790
29. Botos I., Melnikov E.E., Cherry S., Khalatova A.G., Rasulova F.S., Tropea J.E., Maurizi M.R., Rotanova T.V., Gustchina A., and Wlodawer A. Crystal structure of the AAA+ alpha domain of E. coli Lon protease at 1.9A resolution. J. Struct. Biol. 146 (2004) 113-122
30. Amerik A., Antonov V.K., Ostroumova N.I., Rotanova T.V., and Chistiakova L.G. Cloning, structure and expression of the full-size lon gene in Escherichia coli coding for ATP-dependent La-proteinase. Bioorg. Khim. 16 (1990) 869-880 (in Russian)
31. Mogk A., Dougan D., Weibezahn J., Schlieker C., Turgay K., and Bukau B. Broad yet high substrate specificity: the challenge of AAA+ proteins. J. Struct. Biol. 146 (2004) 90-98
32. Rotanova T.V., Melnikov E.E., Khalatova A.G., Makhovskaya O.V., Botos I., Wlodawer A., and Gustchina A. Classification of ATP-dependent proteases Lon and comparison of the active sites of their proteolytic domains. Eur. J. Biochem. 271 (2004) 4865-4871
33. Li M., Rasulova F., Melnikov E.E., Rotanova T.V., Gustchina A., Maurizi M.R., and Wlodawer A. Crystal structure of the N-terminal domain of E. coli Lon protease. Protein Sci. 14 (2005) 2895-2900
34. Lupas A.N., and Martin J. AAA proteins. Curr. Opin. Struct. Biol. 12 (2002) 746-753
35. Thomas-Wohlever J., and Lee I. Kinetic characterization of the peptidase activity of Escherichia coli Lon reveals the mechanistic similarities in ATP-dependent hydrolysis of peptide and protein substrates. Biochemistry 41 (2002) 9418-9425
36. Amerik A., Antonov V.K., Gorbalenya A.E., Kotova S.A., Rotanova T.V., and Shimbarevich E.V. Site-directed mutagenesis of La protease. A catalytically active serine residue. FEBS Lett. 287 (1991) 211-214
37. Starkova N.N., Koroleva E.P., Rumsh L.D., Ginodman L.M., and Rotanova T.V. Mutations in the proteolytic domain of Escherichia coli protease Lon impair the ATPase activity of the enzyme. FEBS Lett. 422 (1998) 218-220
38. Besche H., and Zwickl P. The Thermoplasma acidophilum Lon protease has a Ser-Lys dyad active site. Eur. J. Biochem. 271 (2004) 4361-4365
39. Botos I., Melnikov E.E., Cherry S., Kozlov S., Makhovskaya O.V., Tropea J.E., Gustchina A., Rotanova T.V., and Wlodawer A. Atomic-resolution crystal structure of the proteolytic domain of Archaeoglobus fulgidus lon reveals the conformational variability in the active sites of lon proteases. J. Mol. Biol. 351 (2005) 144-157
40. Ondrovicova G., Liu T., Singh K., Tian B., Li H., Gakh O., Perecko D., Janata J., Granot Z., Orly J., Kutejova E., and Suzuki C.K. Cleavage site selection within a folded substrate by the ATP-dependent lon protease. J. Biol. Chem. 280 (2005) 25103-25110
41. Rasulova F.S., Dergousova N.I., Starkova N.N., Melnikov E.E., Rumsh L.D., Ginodman L.M., and Rotanova T.V. The isolated proteolytic domain of Escherichia coli ATP-dependent protease Lon exhibits the peptidase activity. FEBS Lett. 432 (1998) 179-181
42. von Janowsky B., Knapp K., Major T., Krayl M., Guiard B., and Voos W. Structural properties of substrate proteins determine their proteolysis by the mitochondrial AAA+ protease Pim1. Biol. Chem. 386 (2005) 1307-1317
43. Braun H.A., Umbreen S., Groll M., Kuckelkorn U., Mlynarczuk I., Wigand M.E., Drung I., Kloetzel P.M., and Schmidt B. Tripeptide mimetics inhibit the 20 S proteasome by covalent bonding to the active threonines. J. Biol. Chem. 280 (2005) 28394-28401
44. Adams J., Behnke M., Chen S., Cruickshank A.A., Dick L.R., Grenier L., Klunder J.M., Ma Y.T., Plamondon L., and Stein R.L. Potent and selective inhibitors of the proteasome: dipeptidyl boronic acids. Bioorg. Med. Chem. Lett. 8 (1998) 333-338
45. Adams J., and Kauffman M. Development of the proteasome inhibitor Velcade (Bortezomib). Cancer Invest. 22 (2004) 304-311
46. Bogyo M., McMaster J.S., Gaczynska M., Tortorella D., Goldberg A.L., and Ploegh H. Covalent modification of the active site threonine of proteasomal beta subunits and the Escherichia coli homolog HslV by a new class of inhibitors. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 6629-6634
47. Ovaa H., van Swieten P.F., Kessler B.M., Leeuwenburgh M.A., Fiebiger E., van den Nieuwendijk A.M., Galardy P.J., van der Marel G.A., Ploegh H.L., and Overkleeft H.S. Chemistry in living cells: detection of active proteasomes by a two-step labeling strategy. Angew Chem. Int. Ed. Engl. 42 (2003) 3626-3629
48. Kisselev A.F., and Goldberg A.L. Proteasome inhibitors: from research tools to drug candidates. Chem. Biol. 8 (2001) 739-758
49. Papapostolou D., and Reboud-Ravaux M. Proteasome and proteolysis. J. Soc. Biol. 198 (2004) 263-278
50. Elofsson M., Splittgerber U., Myung J., Mohan R., and Crews C.M. Towards subunit-specific proteasome inhibitors: synthesis and evaluation of peptide alpha',beta'-epoxyketones. Chem. Biol. 6 (1999) 811-822
51. Fenteany G., Standaert R.F., Lane W.S., Choi S., Corey E.J., and Schreiber S.L. Inhibition of proteasome activities and subunit-specific amino-terminal threonine modification by lactacystin. Science 268 (1995) 726-731
52. Chauhan D., Catley L., Li G., Podar K., Hideshima T., Velankar M., Mitsiades C., Mitsiades N., Yasui H., Letai A., Ovaa H., Berkers C., Nicholson B., Chao T.H., Neuteboom S.T., Richardson P., Palladino M.A., and Anderson K.C. A novel orally active proteasome inhibitor induces apoptosis in multiple myeloma cells with mechanisms distinct from Bortezomib. Cancer Cell 8 (2005) 407-419
53. Asai A., Tsujita T., Sharma S.V., Yamashita Y., Akinaga S., Funakoshi M., Kobayashi H., and Mizukami T. A new structural class of proteasome inhibitors identified by microbial screening using yeast-based assay. Biochem. Pharmacol. 67 (2004) 227-234
54. Schmidtke G., Holzhutter H.G., Bogyo M., Kairies N., Groll M., de Giuli R., Emch S., and Groettrup M. How an inhibitor of the HIV-I protease modulates proteasome activity. J. Biol. Chem. 274 (1999) 35734-35740
55. Furet P., Imbach P., Noorani M., Koeppler J., Laumen K., Lang M., Guagnano V., Fuerst P., Roesel J., Zimmermann J., and Garcia-Echeverria C. Entry into a new class of potent proteasome inhibitors having high antiproliferative activity by structure-based design. J. Med. Chem. 47 (2004) 4810-4813
56. Kohno J., Koguchi Y., Nishio M., Nakao K., Kuroda M., Shimizu R., Ohnuki T., and Komatsubara S. Structures of TMC-95A-D: novel proteasome inhibitors from Apiospora montagnei Sacc. TC 1093. J. Org. Chem. 65 (2000) 990-995
57. Koguchi Y., Kohno J., Nishio M., Takahashi K., Okuda T., Ohnuki T., and Komatsubara S. TMC-95A, B, C, and D, novel proteasome inhibitors produced by Apiospora montagnei Sacc. TC 1093. Taxonomy, production, isolation, and biological activities. J. Antibiot. (Tokyo) 53 (2000) 105-109
58. Groll M., Koguchi Y., Huber R., and Kohno J. Crystal structure of the 20 S proteasome:TMC-95A complex: a non-covalent proteasome inhibitor. J. Mol. Biol. 311 (2001) 543-548
59. Kaiser M., Groll M., Siciliano C., Assfalg-Machleidt I., Weyher E., Kohno J., Milbradt G., Renner C., Huber R., and Moroder L. Binding mode of TMC-95A analogues to eukaryotic 20S proteasome. Chembiochem 5 (2004) 1256-1266
60. Kaiser M., Milbradt A.G., Siciliano C., Assfalg-Machleidt I., Machleidt W., Groll M., Renner C., and Moroder L. TMC-95A analogues with endocyclic biphenyl ether group as proteasome inhibitors. Chem. Biodivers 1 (2004) 161-173
61. Basse N., Piguel S., Papapostolou D., Ferrier-Berthelot A., Richy N., Pagano M., Sarthou P., Sobczak-Thepot J., Reboud-Ravaux M., and Vidal J. Linear TMC-95-based proteasome inhibitors. J. Med. Chem. 50 (2007) 2842-2850
62. Kroll M., Arenzana-Seisdedos F., Bachelerie F., Thomas D., Friguet B., and Conconi M. The secondary fungal metabolite gliotoxin targets proteolytic activities of the proteasome. Chem. Biol. 6 (1999) 689-698
63. Basse N., Papapostolou D., Pagano M., Reboud-Ravaux M., Bernard E., Felten A.S., and Vanderesse R. Development of lipopeptides for inhibiting 20S proteasomes. Bioorg. Med. Chem. Lett. 16 (2006) 3277-3281
64. Loidl G., Groll M., Musiol H.J., Huber R., and Moroder L. Bivalency as a principle for proteasome inhibition. Proc. Natl. Acad. Sci. U.S.A. 96 (1999) 5418-5422
65. Xu B., Monsarrat B., Gairin J.E., and Girbal-Neuhauser E. Effect of ajoene, a natural antitumor small molecule, on human 20S proteasome activity in vitro and in human leukemic HL60 cells. Fundam. Clin. Pharmacol. 18 (2004) 171-180
66. Marastoni M., Baldisserotto A., Canella A., Gavioli R., Risi C.D., Pollini G.P., and Tomatis R. Arecoline tripeptide inhibitors of proteasome. J. Med. Chem. 47 (2004) 1587-1590
67. Wan S.B., Landis-Piwowar K.R., Kuhn D.J., Chen D., Dou Q.P., and Chan T.H. Structure-activity study of epi-gallocatechin gallate (EGCG) analogs as proteasome inhibitors. Bioorg. Med. Chem. 13 (2005) 2177-2185
68. Granot Z., Geiss-Friedlander R., Melamed-Book N., Eimerl S., Timberg R., Weiss A., Hales K.H., Hales D.B., Stocco D.M., and Orly J. Proteolysis of normal and mutated steroidogenic acute regulatory proteins in the mitochondria: the fate of unwanted proteins. Mol. Endocrinol. 17 (2003) 2461-2476
69. Frase H., Hudak J., and Lee I. Identification of the proteasome inhibitor MG262 as a potent ATP-dependent inhibitor of the Salmonella enterica serovar Typhimurium Lon protease. Biochemistry 45 (2006) 8264-8274
70. Pekol T., Daniels J.S., Labutti J., Parsons I., Nix D., Baronas E., Hsieh F., Gan L.S., and Miwa G. Human metabolism of the proteasome inhibitor bortezomib: identification of circulating metabolites. Drug Metab. Dispos. 33 (2005) 771-777
71. Pochet L., Doucet C., Schynts M., Thierry N., Boggetto N., Pirotte B., Jiang K.Y., Masereel B., de Tullio P., Delarge J., and Reboud-Ravaux M. Esters and amides of 6-(chloromethyl)-2-oxo-2H-1-benzopyran-3-carboxylic acid as inhibitors of alpha-chymotrypsin: significance of the "aromatic" nature of the novel ester-type coumarin for strong inhibitory activity. J. Med. Chem. 39 (1996) 2579-2585
72. Doucet C., Pochet L., Thierry N., Pirotte B., Delarge J., and Reboud-Ravaux M. 6-Substituted 2-oxo-2H-1-benzopyran-3-carboxylic acid as a core structure for specific inhibitors of human leukocyte elastase. J. Med. Chem. 42 (1999) 4161-4171
73. 14C]-3,4-dichloroisocoumarin with subunits of pituitary and spleen multicatalytic proteinase complexes (proteasomes). Biochemistry 36 (1997) 13946-13953
74. Frase H., and Lee I. Peptidyl boronates inhibit Salmonella enterica serovar Typhimurium Lon protease by a competitive ATP-dependent mechanism. Biochemistry 46 (2007) 6647-6657
75. Cardozo C., Vinitsky A., Hidalgo M.C., Michaud C., and Orlowski M. A 3,4-dichloroisocoumarin-resistant component of the multicatalytic proteinase complex. Biochemistry 31 (1992) 7373-7380
76. Dumond J., Boggetto N., Schramm H.J., Schramm W., Takahashi M., and Reboud-Ravaux M. Thyroxine-derivatives of lipopeptides: bifunctional dimerization inhibitors of human immunodeficiency virus-1 protease. Biochem. Pharmacol. 65 (2003) 1097-1102