Distinct quaternary structures of the AAA+ Lon protease control substrate degradation

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 22, 2013, Pages

  Vieux, Ellen F ^a   Wohlever, Matthew L ^a   Chen, James Z ^a   Sauer, Robert T ^a   Baker, Tania A ^a,b  

^a Department of Biology ^*  (United States)

^b MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

ATP dependent protease; EM structure; IbpB; Regulated proteolysis; Substrate gating

Indexed keywords

DODECAMER; ENDOPEPTIDASE LA; ENZYME; POLYMER; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BACTERIAL STRAIN; CONTROLLED STUDY; CRYSTAL STRUCTURE; ELECTRON MICROSCOPY; ENZYME ACTIVITY; ENZYME SUBSTRATE; ESCHERICHIA COLI; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN QUATERNARY STRUCTURE;

ATP-DEPENDENT PROTEASE; EM STRUCTURE; IBPB; REGULATED PROTEOLYSIS; SUBSTRATE GATING;

BLOTTING, WESTERN; CHROMATOGRAPHY, GEL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; LASERS; MICROSCOPY, ELECTRON; MODELS, MOLECULAR; MULTIENZYME COMPLEXES; MUTATION, MISSENSE; PROTEASE LA; PROTEIN CONFORMATION; PROTEOLYSIS; SCATTERING, RADIATION; ULTRACENTRIFUGATION;

ESCHERICHIA COLI;

EID: 84878450345     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1307066110     Document Type: Article

References (51)

1. Fredriksson A, Ballesteros M, Dukan S, Nyström T (2005) Defense against protein carbonylation by DnaK/DnaJ and proteases of the heat shock regulon. J Bacteriol 187(12):4207-4213.
2. Kowit JD, Goldberg AL (1977) Intermediate steps in the degradation of a specific abnormal protein in Escherichia coli. J Biol Chem 252(23):8350-8357.
3. Shineberg B, Zipser D (1973) The ion gene and degradation of beta-galactosidase nonsense fragments. J Bacteriol 116(3):1469-1471.
4. Gottesman S, Halpern E, Trisler P (1981) Role of sulA and sulB in filamentation by lon mutants of Escherichia coli K-12. J Bacteriol 148(1):265-273.
5. Mizusawa S, Gottesman S (1983) Protein degradation in Escherichia coli: The lon gene controls the stability of sulA protein. Proc Natl Acad Sci USA 80(2):358-362.
6. Bissonnette SA, Rivera-Rivera I, Sauer RT, Baker TA (2010) The IbpA and IbpB small heatshock proteins are substrates of theAAA+ Lon protease. Mol Microbiol 75(6):1539-1549.
7. Goff SA, Casson LP, Goldberg AL (1984) Heat shock regulatory gene htpR influences rates of protein degradation and expression of the lon gene in Escherichia coli. Proc Natl Acad Sci USA 81(21):6647-6651.
8. Phillips TA, VanBogelen RA, Neidhardt FC (1984) lon gene product of Escherichia coli is a heat-shock protein. J Bacteriol 159(1):283-287.
9. Goff SA, Goldberg AL (1985) Production of abnormal proteins in E. coli stimulates transcription of lon and other heat shock genes. Cell 41(2):587-595.
10. Van Melderen L, Aertsen A (2009) Regulation and quality control by Lon-dependent proteolysis. Res Microbiol 160(9):645-651.
11. Bender T, Lewrenz I, Franken S, Baitzel C, Voos W (2011) Mitochondrial enzymes are protected from stress-induced aggregation by mitochondrial chaperones and the Pim1/LON protease. Mol Biol Cell 22(5):541-554.
12. Venkatesh S, Lee J, Singh K, Lee I, Suzuki CK (2012) Multitasking in the mitochondrion by the ATP-dependent Lon protease. Biochim Biophys Acta 1823(1):56-66.
13. Ngo JK, Davies KJ (2009) Mitochondrial Lon protease is a human stress protein. Free Radic Biol Med 46(8):1042-1048.
14. Ngo JK, Pomatto LC, Bota DA, Koop AL, Davies KJ (2011) Impairment of lon-induced protection against the accumulation of oxidized proteins in senescent wi-38 fibroblasts. J Gerontol A Biol Sci Med Sci 66(11):1178-1185.
15. Bernstein SH, et al. (2012) The mitochondrial ATP-dependent Lon protease: A novel target in lymphoma death mediated by the synthetic triterpenoid CDDO and its derivatives. Blood 119(14):3321-3329.
16. Rosen R, et al. (2002) Protein aggregation in Escherichia coli: Role of proteases. FEMS Microbiol Lett 207(1):9-12.
17. Goldberg AL, Moerschell RP, Chung CH, Maurizi MR (1994) ATP-dependent protease La (lon) from Escherichia coli. Methods Enzymol 244:350-375.
18. Botos I, et al. (2004) 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(9):8140-8148.
19. Park SC, et al. (2006) Oligomeric structure of the ATP-dependent protease La (Lon) of Escherichia coli. Mol Cells 21(1):129-134.
20. Sauer RT, Baker TA (2011) AAA+ proteases: ATP-fueled machines of protein destruction. Annu Rev Biochem 80:587-612.
21. Sauer RT, et al. (2004) Sculpting the proteome with AAA(+) proteases and disassembly machines. Cell 119(1):9-18.
22. Joshi SA, Hersch GL, Baker TA, Sauer RT (2004) Communication between ClpX and ClpP during substrate processing and degradation. Nat Struct Mol Biol 11(5):404-411.
23. Roudiak SG, Seth A, Knipfer N, Shrader TE (1998) The lon protease from Mycobacterium smegmatis: Molecular cloning, sequence analysis, functional expression, and enzymatic characterization. Biochemistry 37(1):377-386.
24. Starkova NN, Koroleva EP, Rumsh LD, Ginodman LM, Rotanova TV (1998) Mutations in the proteolytic domain of Escherichia coli protease Lon impair the ATPase activity of the enzyme. FEBS Lett 422(2):218-220.
25. van Dijl JM, et al. (1998) The ATPase and protease domains of yeast mitochondrial Lon: Roles in proteolysis and respiration-dependent growth. Proc Natl Acad Sci USA 95(18):10584-10589.
26. Waxman L, Goldberg AL (1986) Selectivity of intracellular proteolysis: Protein substrates activate the ATP-dependent protease (La). Science 232(4749):500-503.
27. Gur E, Sauer RT (2009) Degrons in protein substrates program the speed and operating efficiency of the AAA+ Lon proteolytic machine. Proc Natl Acad Sci USA 106(44):18503-18508.
28. Van Melderen L, Gottesman S (1999) Substrate sequestration by a proteolytically inactive Lon mutant. Proc Natl Acad Sci USA 96(11):6064-6071.
29. Duman RE, Löwe J (2010) Crystal structures of Bacillus subtilis Lon protease. J Mol Biol 401(4):653-670.
30. Jiao W, Qian M, Li P, Zhao L, Chang Z (2005) The essential role of the flexible termini in the temperature-responsiveness of the oligomeric state and chaperone-like activity for the polydisperse small heat shock protein IbpB from Escherichia coli. J Mol Biol 347(4):871-884.
31. Shearstone JR, Baneyx F (1999) Biochemical characterization of the small heat shock protein IbpB from Escherichia coli. J Biol Chem 274(15):9937-9945.
32. Farrell HM, Jr., et al. (2002) Molten globule structures in milk proteins: Implications for potential new structure-function relationships. J Dairy Sci 85(3):459-471.
33. Lucey JA, Srinivasan M, Singh H, Munro PA (2000) Characterization of commercial and experimental sodium caseinates by multiangle laser light scattering and size-exclusion chromatography. J Agric Food Chem 48(5):1610-1616.
34. Gur E, Sauer RT (2008) Recognition of misfolded proteins by Lon, a AAA(+) protease. Genes Dev 22(16):2267-2277.
35. Kenniston JA, Baker TA, Fernandez JM, Sauer RT (2003) Linkage between ATP consumption and mechanical unfolding during the protein processing reactions of an AAA+ degradation machine. Cell 114(4):511-520.
36. Cha SS, et al. (2010) Crystal structure of Lon protease: Molecular architecture of gated entry to a sequestered degradation chamber. EMBO J 29(20):3520-3530.
37. Roudiak SG, Shrader TE (1998) Functional role of the N-terminal region of the Lon protease from Mycobacterium smegmatis. Biochemistry 37(32):11255-11263.
38. Melnikov EE, et al. (2008) Limited proteolysis of E. coli ATP-dependent protease Lon-A unified view of the subunit architecture and characterization of isolated enzyme fragments. Acta Biochim Pol 55(2):281-296.
39. Chir JL, Liao JH, Lin YC, Wu SH (2009) The N-terminal sequence after residue 247 plays an important role in structure and function of Lon protease from Brevibacillus thermoruber WR-249. Biochem Biophys Res Commun 382(4):762-765.
40. Ishii Y, Amano F (2001) Regulation of SulA cleavage by Lon protease by the C-terminal amino acid of SulA, histidine. Biochem J 358(Pt 2):473-480.
41. Shah IM, Wolf RE, Jr. (2006) Sequence requirements for Lon-dependent degradation of the Escherichia coli transcription activator SoxS: Identification of the SoxS residues critical to proteolysis and specific inhibition of in vitro degradation by a peptide comprised of the N-terminal 21 amino acid residues. J Mol Biol 357(3):718-731.
42. GonzalezM, Frank EG, Levine AS, Woodgate R (1998) Lon-mediated proteolysis of the Escherichia coli UmuD mutagenesis protein: In vitro degradation and identification of residues required for proteolysis. Genes Dev 12(24):3889-3899.
43. Mogk A, Deuerling E, Vorderwülbecke S, Vierling E, Bukau B (2003) Small heat shock proteins, ClpB and the DnaK system form a functional triade in reversing protein aggregation. Mol Microbiol 50(2):585-595.
44. Mogk A, et al. (2003) Refolding of substrates bound to small Hsps relies on a disaggregation reaction mediated most efficiently by ClpB/DnaK. J Biol Chem 278(33): 31033-31042.
45. Rudyak SG, Brenowitz M, Shrader TE (2001) Mg2+-linked oligomerization modulates the catalytic activity of the Lon (La) protease from Mycobacterium smegmatis. Biochemistry 40(31):9317-9323.
46. Brown PH, Schuck P (2006) Macromolecular size-and-shape distributions by sedimentation velocity analytical ultracentrifugation. Biophys J 90(12):4651-4661.
47. Ali Azam T, Iwata A, Nishimura A, Ueda S, Ishihama A (1999) Growth phasedependent variation in protein composition of the Escherichia coli nucleoid. J Bacteriol 181(20):6361-6370.
48. Henderson R, et al. (2011) Tilt-pair analysis of images from a range of different specimens in single-particle electron cryomicroscopy. J Mol Biol 413(5):1028-1046.
49. Nørby JG (1988) Coupled assay of Na+,K+-ATPase activity. Methods Enzymol 156: 116-119.
50. Lindsley JE (2001) Use of a real-time, coupled assay to measure the ATPase activity of DNA topoisomerase II. Methods Mol Biol 95:57-64.
51. Gottesman S, Roche E, Zhou Y, Sauer RT (1998) The ClpXP and ClpAP proteases degrade proteins with carboxy-terminal peptide tails added by the SsrA-tagging system. Genes Dev 12(9):1338-1347.