Polyphosphate, cyclic AMP, guanosine tetraphosphate, and c-di-GMP reduce in vitro Lon activity

Bioengineered

Volumn 5, Issue 4, 2014, Pages 264-268

  Osbourne, Devon O ^a   Soo, Valerie Wc ^a   Konieczny, Igor ^c   Wood, Thomas K ^a,b  

^a The Pennsylvania State University   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF GDA SK   (Poland)

Author keywords

c di GMP; cAMP; Lon protease; Polyphosphate; ppGpp

Indexed keywords

ALPHA CASEIN; ANTITOXIN; CYCLIC AMP; CYCLIC DI GMP; CYCLIC GMP DERIVATIVE; ENDOPEPTIDASE LA; GUANOSINE 3' DIPHOSPHATE 5' DIPHOSPHATE; POLYPHOSPHATE; RIBOSOME PROTEIN; UNCLASSIFIED DRUG; GUANOSINE PHOSPHATE;

ARTICLE; BINDING AFFINITY; BINDING SITE; CHEMICAL STRUCTURE; CONTROLLED STUDY; DNA BINDING MOTIF; ENZYME ACTIVITY; ENZYME DEGRADATION; ENZYME INHIBITION; ENZYME REGULATION; ESCHERICHIA COLI; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IN VITRO STUDY; NONHUMAN; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PURIFICATION; SIGNAL TRANSDUCTION; BINDING ASSAY; ENZYME PURIFICATION; PROTEIN BINDING;

EID: 84903975405     PISSN: 19491018     EISSN: 19491026     Source Type: Journal    
DOI: 10.4161/bioe.29261     Document Type: Article

References (43)

1. Goldberg AL, Moerschell RP, Chung CH, Maurizi MR. ATP-dependent protease La (Lon) from Escherichia coli. Methods Enzymol 1994; 244:350-75; PMID:7845219; http://dx.doi.org/10.1016/0076-6879(94)44027-1
2. Swamy KH, Goldberg AL. E. coli contains eight soluble proteolytic activities, one being ATP dependent. Nature 1981; 292:652-4; PMID:7019728; http://dx.doi.org/10.1038/292652a0
3. Neuwald AF, Aravind L, Spouge JL, Koonin EV. AAA+: A class of chaperone-like ATPases associated with the assembly, operation, and disassembly of protein complexes. Genome Res 1999; 9:27-43; PMID:9927482
4. Rotanova TV, Melnikov EE, Khalatova AG, Makhovskaya OV, Botos I, Wlodawer A, Gustchina A. Classification of ATP-dependent proteases Lon and comparison of the active sites of their proteolytic domains. Eur J Biochem 2004; 271:4865-71; PMID:15606774; http://dx.doi.org/10.1111/j.1432-1033.2004.04452.x
5. Botos I, Melnikov EE, Cherry S, Tropea JE, Khalatova AG, Rasulova F, Dauter Z, Maurizi MR, Rotanova TV, Wlodawer A, et al. The catalytic domain of Escherichia coli Lon protease has a unique fold and a Ser-Lys dyad in the active site. J Biol Chem 2004; 279:8140-8; PMID:14665623; http://dx.doi.org/10.1074/jbc.M312243200
6. Tsilibaris V, Maenhaut-Michel G, Van Melderen L. Biological roles of the Lon ATP-dependent protease. Res Microbiol 2006; 157:701-13; PMID:16854568; http://dx.doi.org/10.1016/j.resmic.2006.05.004
7. Suzuki CK, Rep M, van Dijl JM, Suda K, Grivell LA, Schatz G. ATP-dependent proteases that also chaperone protein biogenesis. Trends Biochem Sci 1997; 22:118-23; PMID:9149530; http://dx.doi.org/10.1016/S0968-0004(97)01020-7
8. Bonnefoy E, Almeida A, Rouviere-Yaniv J. Londependent regulation of the DNA binding protein HU in Escherichia coli. Proc Natl Acad Sci U S A 1989; 86:7691-5; PMID:2682620; http://dx.doi.org/10.1073/pnas.86.20.7691
9. Ishii Y, Amano F. Regulation of SulA cleavage by Lon protease by the C-terminal amino acid of SulA, histidine. Biochem J 2001; 358:473-80; PMID:11513747; http://dx.doi.org/10.1042/0264-6021:3580473
10. Torres-Cabassa AS, Gottesman S. Capsule synthesis in Escherichia coli K-12 is regulated by proteolysis. J Bacteriol 1987; 169:981-9; PMID:3029041
11. Gerdes K, Maisonneuve E. Bacterial persistence and toxin-antitoxin loci. Annu Rev Microbiol 2012; 66:103-23; PMID:22994490; http://dx.doi.org/10.1146/annurev-micro-092611-150159
12. Bretz J, Losada L, Lisboa K, Hutcheson SW. Lon protease functions as a negative regulator of type III protein secretion in Pseudomonas syringae. Mol Microbiol 2002; 45:397-409; PMID:12123452; http://dx.doi.org/10.1046/j.1365-2958.2002.03008.x
13. Rosen R, Biran D, Gur E, Becher D, Hecker M, Ron EZ. Protein aggregation in Escherichia coli: role of proteases. FEMS Microbiol Lett 2002; 207:9-12; PMID:11886743; http://dx.doi.org/10.1111/j.1574-6968.2002.tb11020.x
14. Goff SA, Goldberg AL. An increased content of protease La, the lon gene product, increases protein degradation and blocks growth in Escherichia coli. J Biol Chem 1987; 262:4508-15; PMID:3549709
15. Gur E, Sauer RT. Recognition of misfolded proteins by Lon, a AAA+ protease. Genes Dev 2008; 22:2267-77; PMID:18708584; http://dx.doi.org/10.1101/gad.1670908
16. Chung CH, Goldberg AL. The product of the lon (capR) gene in Escherichia coli is the ATP-dependent protease, protease La. Proc Natl Acad Sci U S A 1981; 78:4931-5; PMID:6458037; http://dx.doi.org/10.1073/pnas.78.8.4931
17. Rotanova TV, Botos I, Melnikov EE, Rasulova F, Gustchina A, Maurizi MR, Wlodawer A. Slicing a protease: structural features of the ATP-dependent Lon proteases gleaned from investigations of isolated domains. Protein Sci 2006; 15:1815-28; PMID:16877706; http://dx.doi.org/10.1110/ps.052069306
18. Skorupski K, Tomaschewski J, Rüger W, Simon LD. A bacteriophage T4 gene which functions to inhibit Escherichia coli Lon protease. J Bacteriol 1988; 170:3016-24; PMID:2838455
19. Sugiyama N, Minami N, Ishii Y, Amano F. Inhibition of Lon protease by bacterial lipopolisaccharide (LPS) though inhibition of ATPase. Adv. Biosci. Biotechnol 2013; 4:590-8; http://dx.doi.org/10.4236/abb.2013.44077
20. Frase H, Hudak J, Lee I. Identification of the proteasome inhibitor MG262 as a potent ATP-dependent inhibitor of the Salmonella enterica serovar Typhimurium Lon protease. Biochemistry 2006; 45:8264-74; PMID:16819825; http://dx.doi.org/10.1021/bi060542e
21. Kuroda A. A polyphosphate-lon protease complex in the adaptation of Escherichia coli to amino acid starvation. Biosci Biotechnol Biochem 2006; 70:325-31; PMID:16495646; http://dx.doi.org/10.1271/bbb.70.325
22. Kuroda A, Nomura K, Ohtomo R, Kato J, Ikeda T, Takiguchi N, Ohtake H, Kornberg A. Role of inorganic polyphosphate in promoting ribosomal protein degradation by the Lon protease in E. coli. Science 2001; 293:705-8; PMID:11474114; http://dx.doi.org/10.1126/science.1061315
23. Nomura K, Kato J, Takiguchi N, Ohtake H, Kuroda A. Effects of inorganic polyphosphate on the proteolytic and DNA-binding activities of Lon in Escherichia coli. J Biol Chem 2004; 279:34406-10; PMID:15187082; http://dx.doi.org/10.1074/jbc.M404725200
24. Chung CH, Goldberg AL. DNA stimulates ATP-dependent proteolysis and protein-dependent ATPase activity of protease La from Escherichia coli. Proc Natl Acad Sci U S A 1982; 79:795-9; PMID:6461007; http://dx.doi.org/10.1073/pnas.79.3.795
25. Charette MF, Henderson GW, Doane LL, Markovitz A. DNA-stimulated ATPase activity on the lon (CapR) protein. J Bacteriol 1984; 158:195-201; PMID:6325386
26. Römling U, Galperin MY, Gomelsky M. Cyclic diGMP: the first 25 years of a universal bacterial second messenger. Microbiol Mol Biol Rev 2013; 77:1-52; PMID:23471616; http://dx.doi.org/10.1128/MMBR.00043-12
27. Ma Q, Yang Z, Pu M, Peti W, Wood TK. Engineering a novel c-di-GMP-binding protein for biofilm dispersal. Environ Microbiol 2011; 13:631-42; PMID:21059164; http://dx.doi.org/10.1111/j.1462-2920.2010.02368.x
28. Benach J, Swaminathan SS, Tamayo R, Handelman SK, Folta-Stogniew E, Ramos JE, Forouhar F, Neely H, Seetharaman J, Camilli A, et al. The structural basis of cyclic diguanylate signal transduction by PilZ domains. EMBO J 2007; 26:5153-66; PMID:18034161; http://dx.doi.org/10.1038/sj.emboj.7601918
29. Li T-N, Chin K-H, Fung K-M, Yang M-T, Wang A-H, Chou S-H. A novel tetrameric PilZ domain structure from xanthomonads. PLoS One 2011; 6:e22036; PMID:21760949; http://dx.doi.org/10.1371/journal.pone.0022036
30. Christen B, Christen M, Paul R, Schmid F, Folcher M, Jenoe P, Meuwly M, Jenal U. Allosteric control of cyclic di-GMP signaling. J Biol Chem 2006; 281:32015-24; PMID:16923812; http://dx.doi.org/10.1074/jbc.M603589200
31. Whitney JC, Colvin KM, Marmont LS, Robinson H, Parsek MR, Howell PL. Structure of the cytoplasmic region of PelD, a degenerate diguanylate cyclase receptor that regulates exopolysaccharide production in Pseudomonas aeruginosa. J Biol Chem 2012; 287:23582-93; PMID:22605337; http://dx.doi.org/10.1074/jbc.M112.375378
32. Breidenstein EBM, Janot L, Strehmel J, Fernandez L, Taylor PK, Kukavica-Ibrulj I, Gellatly SL, Levesque RC, Overhage J, Hancock REW. The Lon protease is essential for full virulence in Pseudomonas aeruginosa. PLoS One 2012; 7:e49123; PMID:23145092; http://dx.doi.org/10.1371/journal.pone.0049123
33. Düvel J, Bertinetti D, Möller S, Schwede F, Morr M, Wissing J, Radamm L, Zimmermann B, Genieser H-G, Jänsch L, et al. A chemical proteomics approach to identify c-di-GMP binding proteins in Pseudomonas aeruginosa. J Microbiol Methods 2012; 88:229-36; PMID:22178430; http://dx.doi.org/10.1016/j.mimet.2011.11.015
34. Kubik S, Wegrzyn K, Pierechod M, Konieczny I. Opposing effects of DNA on proteolysis of a replication initiator. Nucleic Acids Res 2012; 40:1148-59; PMID:21976729; http://dx.doi.org/10.1093/nar/gkr813
35. Ueda A, Wood TK. Connecting quorum sensing, c-di-GMP, pel polysaccharide, and biofilm formation in Pseudomonas aeruginosa through tyrosine phosphatase TpbA (PA3885). PLoS Pathog 2009; 5:e1000483; PMID:19543378; http://dx.doi.org/10.1371/journal.ppat.1000483
36. Kuroda A, Ohtake H. Molecular analysis of polyphosphate accumulation in bacteria. Biochemistry (Mosc) 2000; 65:304-8; PMID:10739472
37. Kuroda A, Kornberg A. Polyphosphate kinase as a nucleoside diphosphate kinase in Escherichia coli and Pseudomonas aeruginosa. Proc Natl Acad Sci U S A 1997; 94:439-42; PMID:9012801; http://dx.doi.org/10.1073/pnas.94.2.439
38. Rodionov DG, Ishiguro EE. Direct correlation between overproduction of guanosine 3′,5′-bispyrophosphate (ppGpp) and penicillin tolerance in Escherichia coli. J Bacteriol 1995; 177:4224-9; PMID:7635809
39. Gomelsky M. cAMP, c-di-GMP, c-di-AMP and now cGMP: bacteria use them all! Mol Microbiol 2011; 79:562-5; PMID:21255104; http://dx.doi.org/10.1111/j.1365-2958.2010.07514.x
40. Cotta MA, Wheeler MB, Whitehead TR. Cyclic AMP in ruminal and other anaerobic bacteria. FEMS Microbiol Lett 1994; 124:355-9; PMID:7851742; http://dx.doi.org/10.1111/j.1574-6968.1994.tb07308.x
41. Simm R, Morr M, Remminghorst U, Andersson M, Römling U. Quantitative determination of cyclic diguanosine monophosphate concentrations in nucleotide extracts of bacteria by matrix-assisted laser desorption/ionization-time-of-flight mass spectrometry. Anal Biochem 2009; 386:53-8; PMID:19135022; http://dx.doi.org/10.1016/j.ab.2008.12.013
42. Barraud N, Schleheck D, Klebensberger J, Webb JS, Hassett DJ, Rice SA, Kjelleberg S. Nitric oxide signaling in Pseudomonas aeruginosa biofilms mediates phosphodiesterase activity, decreased cyclic di-GMP levels, and enhanced dispersal. J Bacteriol 2009; 191:7333-42; PMID:19801410; http://dx.doi.org/10.1128/JB.00975-09
43. Minami N, Yasuda T, Ishii Y, Fujimori K, Amano F. Regulatory role of cardiolipin in the activity of an ATP-dependent protease, Lon, from Escherichia coli. J Biochem 2011; 149:519-27; PMID:21436141; http://dx.doi.org/10.1093/jb/mvr036