Role of streptococcus intermedius DnaK chaperone system in stress tolerance and pathogenicity

Cell Stress and Chaperones

Volumn 17, Issue 1, 2012, Pages 41-55

  Tomoyasu, Toshifumi ^a   Tabata, Atsushi ^a   Imaki, Hidenori ^a   Tsuruno, Keigo ^b   Miyazaki, Aya ^b   Sonomoto, Kenji ^b   Whiley, Robert Alan ^c   Nagamune, Hideaki ^a  

^a UNIVERSITY OF TOKUSHIMA   (Japan)

^b KYUSHU UNIVERSITY   (Japan)

^c QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

DnaK chaperone system; Escherichia coli; Intermedilysin; Streptococcus intermedius; Thermosensitivity

Indexed keywords

BACTERIAL PROTEIN; CHAPERONIN; INTERMEDILYSIN; PROTEIN DNAK; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; BACTERIOCIN; CHAPERONE; DNAK PROTEIN, E COLI; ESCHERICHIA COLI PROTEIN; HEAT SHOCK PROTEIN 70; INTERMEDILYSIN PROTEIN, STREPTOCOCCUS INTERMEDIUS;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM MUTANT; CELL STRAIN HEPG2; CONTROLLED STUDY; CYTOTOXICITY; ESCHERICHIA COLI; HEAT SENSITIVITY; HEMOLYSIS; HUMAN; HUMAN CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENICITY; PLASMID; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; REGULATORY MECHANISM; STREPTOCOCCUS INTERMEDIUS; STRESS; AMINO ACID SEQUENCE; GENE INACTIVATION; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; PHYSIOLOGICAL STRESS; SEQUENCE ALIGNMENT;

ESCHERICHIA COLI; STREPTOCOCCUS INTERMEDIUS;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BACTERIOCINS; CHAPERONIN 60; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE KNOCKOUT TECHNIQUES; HEP G2 CELLS; HSP70 HEAT-SHOCK PROTEINS; HUMANS; MOLECULAR CHAPERONES; MOLECULAR SEQUENCE DATA; MUTATION; SEQUENCE ALIGNMENT; STREPTOCOCCUS INTERMEDIUS; STRESS, PHYSIOLOGICAL;

EID: 84858976879     PISSN: 13558145     EISSN: 14661268     Source Type: Journal    
DOI: 10.1007/s12192-011-0284-4     Document Type: Article

References (54)

1. Abranches J, Nascimento MM, Zeng L, Browngardt CM, Wen ZT, Rivera MF, Burne RA (2008) Ccp A regulates central metabolism and virulence gene expression in Streptococcus mutans. J Bacteriol 190:2340-2349. doi:10.1128/JB.01237-07 (Pubitemid 351466329)
2. Arsène F, Tomoyasu T, Bukau B (2000) The heat shock response of Escherichia coli. Int J Food Microbiol 55:3-9 (Pubitemid 30160797)
3. Ben-Zvi AP, Goloubinoff P (2001) Review: mechanisms ofdisaggre-gation and refolding of stable protein aggregates by molecular chaperones. J Struct Biol 135:84-93. doi:10.1006/jsbi.2001.4352
4. Borenfreund E, Puerner JA (1985) Toxicity determined in vitro by morphological alterations and neutral red absorption. Toxicol Lett 24:119-124 (Pubitemid 15103513)
5. Bukau B, Walker GC (1989a) Cellular defects caused by deletion of the Escherichia coli dna K gene indicate roles for heat shock protein in normal metabolism. J Bacteriol 171:2337-2346
6. Bukau B, Walker GC (1989b) Δdna K52 mutants of Escherichia coli have defects in chromosome segregation and plasmid maintenance at normal growth temperatures. J Bacteriol 171:6030-6038 (Pubitemid 19266926)
7. Bukau B, Walker GC (1990) Mutations altering heat shock specific subunit of RNA polymerase suppress major cellular defects of E. coli mutants lacking the Dna K chaperone. EMBO J 9:4027-4036
8. Claridge JE, Attorri S, Musher DM, Hebert J, Dunbar S (2001) Streptococcus intermedius, Streptococcus constellatus, and Strep-tococcus anginosus ("Streptococcus milleri group") are of different clinical importance and are not equally associated with abscess. Clin Infect Dis 15:1511-1515. doi:10.1086/320163 (Pubitemid 32424290)
9. Dougan DA, Mogk A, Bukau B (2002) Protein folding and degradation in bacteria: to degrade or not to degrade? That is the question. Cell Mol Life Sci 59:1607-1616. doi:10.1007/PL00012487 (Pubitemid 35346963)
10. Gamer J, Bujard H, Bukau B (1992) Physical interaction between heat shock proteins Dna K, Dna J, and Grp E and the bacterial heat shock transcription factor σ . Cell 69:833-842. doi:10.1016/ 0092-8674(92)90294-M
11. Genevaux P, Georgopoulos C, Kelley WL (2007) The Hsp70 chaperone machines of Escherichia coli: a paradigm for the repartition of chaperone functions. Mol Microbiol 66:840-857. doi:10.1111/j.1365-2958.2007.05961.x (Pubitemid 350050417)
12. Hanawa T, Fukuda M, Kawakami H, Hirano H, Kamiya S, Yamamoto T (1999) The Listeria monocytogenes Dna K chaperone is required for stress tolerance and efficient phagocytosis with macrophages. Cell Stress Chaperones 4:118-128 (Pubitemid 29438122)
13. Henderson B, Allan E, Coates AR (2006) Stress wars: the direct role ofhost and bacterial molecular chaperones in bacterial infection. Infect Immun 74:3693-3706. doi:10.1128/IAI.01882-05 (Pubitemid 43993301)
14. Jackson MW, Silva-Herzog E, Plano GV (2004) The ATP-dependent Clp XP and Lon proteases regulate expression of the Yersinia pestis type III secretion system via regulated proteolysis of Ymo A, a small histone-like protein. Mol Microbiol 54:1364-1378. doi:10.1111/j.1365-2958.2004.04353.x (Pubitemid 39578278)
15. Jacobs JA, Pietersen HG, Stobberingh EE, Soeters PB (1995) Streptococcus anginosus, Streptococcus constellatus and Strepto-coccus intermedius. Clinical relevance, hemolytic and serologic characteristics. Am J Clin Pathol 104:547-553
16. Jensen PR, Hammer K (1998) The sequence of spacers between the consensus sequences modulates the strength of prokaryotic promoters. Appl Environ Microbiol 64:82-87 (Pubitemid 28040295)
17. Jerng JS, Hsueh PR, Teng LJ, Lee LN, Yang PC, Luh KT (1997) Empyema thoracis and lung abscess caused by viridans streptococci. Am J Respir Crit Care Med 156:1508-1514 (Pubitemid 27505517)
18. Kietzman CC, Caparon MG (2010) Ccp A and Lac D.1 affect temporal regulation of Streptococcus pyogenes virulence genes. Infect Immun 78:241-252. doi:10.1128/IAI.00746-09
19. ++ in Streptococcus pneumoniae. Arch Pharm Res 31:462-467. doi:10.1007/s12272-001-1179-4
20. Koch B, Kilstrup M, Vogensen FK, Hammer K (1998) Induced levels of heat shock proteins in a dna K mutant of Lactococcus lactis. J Bacteriol 180:3873-3881 (Pubitemid 28361583)
21. Köhler S, Ekaza E, Paquet JY, Walravens K, Teyssier J, Godfroid J, Liautard JP (2002) Induction of dna K through its native heat shock promoter is necessary for intramacrophagic replication of Brucella suis. Infect Immun 70:1631-1634 (Pubitemid 34163447)
22. Kusukawa N, Yura T, Ueguchi C, Akiyama Y, Ito K (1989) Effects of mutations in heat-shock genes gro ES and gro EL on protein export in Escherichia coli. EMBO J 8:3517-3521 (Pubitemid 19273582)
23. Laemmli UK (1970) Cleavage ofstructural proteins during the assembly oftheheadofbacteriophage T4. Nature 227:680-685. doi:10.1038/ 227680a0
24. Lanzer M, Bujard H (1988) Promoters determine largely the efficiency of repressor action. Proc Natl Acad Sci USA 85:6632-6636
25. Lemos JA, Chen YY, Burne RA (2001) Genetic and physiologic analysis of the gro E operon and role of the Hrc A repressor in stress gene regulation and acid tolerance in Streptococcus mutans. J Bacteriol 183:6074-6084. doi:10.1128/JB.183.20.6074-6084.2001 (Pubitemid 32917427)
26. Lemos JA, Luzardo Y, Burne RA (2007) Physiologic effects offorced down-regulation ofdna Kandgro EL expression in Streptococcus mutans. JBacteriol 189:1582-1588. doi:10.1128/JB.01655-06 (Pubitemid 46446119)
27. Lutz R, Bujard H (1997) Independent and tight regulation of transcriptional units in Escherichia coli via the Lac R/O, the Tet R/O and Ara C/I1-I2 regulatory elements. Nucleic Acids Res 25:1203-1210 (Pubitemid 27303212)
28. Mayer MP, Rüdiger S, Bukau B (2000) Molecular basis for interactions of the Dna K chaperone with substrates. Biol Chem 381:877-885
29. 32-dependent class of heat shock genes in Bradyrhizobium japonicum. Mol Gen Genet 254:195-206
30. Mogk A, Homuth G, Scholz C, Kim L, Schmid FX, Schumann W (1997) The Gro E chaperonin machine is a major modulator of the CIRCE heat shock regulon of Bacillus subtilis. EMBO J 16:4579-4590. doi:10.1093/emboj/16.15.4579 (Pubitemid 27326595)
31. Mogk A, Bukau B, Lutz R, Schumann W (1999) Construction and analysis of hybrid Escherichia coli-Bacillus subtilis dna K genes. J Bacteriol 181:1971-1974 (Pubitemid 29138639)
32. Nagamune H, Ohnishi C, Katsuura A, Fushitani K, Whiley RA, Tsuji A, Matsuda Y (1996) Intermedilysin, a novel cytotoxin specific for human cells secreted by Streptococcus intermedius UNS46 isolated from ahuman liver abscess. Infect Immun 64:3093-3100 (Pubitemid 26256151)
33. Nagamune H, Whiley RA, Goto T, Inai Y Maeda T, Hardie JM, Kourai H (2000) Distribution of the intermedilysin gene among the anginosus group streptococci and correlation between intermedilysin production and deep-seated infection with Strep-tococcus intermedius. J Clin Microbiol 38:220-226
34. Rodriguez F, Arsène-Ploetze F, Rist W, Rüdiger S, Schneider-Mergener J, Mayer MP, Bukau B (2008) Molecular basis for regulation of the heat shock transcription factor σ by the Dna K and Dna J chaperones. Mol Cell 32:347-358. doi:10.1016/j. molcel.2008.09.016
35. Schulz A, Tzschaschel B, Schumann W (1995) Isolation and analysis of mutants of the dna K operon of Bacillus subtilis. Mol Microbiol 15:421-429
36. Shelburne SA, Davenport MT, Keith DB, Musser JM (2008a) The role of complex carbohydrate catabolism in the pathogenesis of invasive streptococci. Trends Microbiol 16:318-325. doi:10.1016/j.tim.2008.04.002
37. Shelburne SA, Keith D, Horstmann N, Sumby P, Davenport MT, Graviss EA, Brennan RG, Musser JM (2008b) A direct link between carbohydrate utilization and virulence in the major human pathogen group A Streptococcus. Proc Natl Acad Sci USA 105:1698-1703. doi:10.1073/pnas.0711767105 (Pubitemid 351346577)
38. Singh VK, Utaida S, Jackson LS, Jayaswal RK, Wilkinson BJ, Chamberlain NR (2007) Role for dna K locus in tolerance of multiple stresses in Staphylococcus aureus. Microbiology 153:3162-3173. doi:10.1099/mic.0.2007/009506-0 (Pubitemid 47517076)
39. Sugimoto S, Higashi C, Saruwatari K, Nakayama J, Sonomoto K (2007) A gram-negative characteristic segment in Escherichia coli Dna K is essential for the ATP-dependent cooperative function with the co-chaperones Dna J and Grp E. FEBS Lett 581:2993-2999. doi:10.1016/j.febslet.2007.05.055 (Pubitemid 46908808)
40. Sugimoto S, Saruwatari K, Higashi C, Tsuruno K, Matsumoto S, Nakayama J, Sonomoto K (2008) In vivo and in vitro complemen-tation study comparing the function of Dna K chaperone systems from halophilic lactic acid bacterium Tetragenococcus halophilus and Escherichia coli. Biosci Biotechnol Biochem 72:811-822. doi:10.1271/bbb.70691 (Pubitemid 351463671)
41. Sukeno A, Nagamune H, Whiley RA, Jafar SI, Aduse-Opoku J, Ohkura K, Maeda T, Hirota K, Miyake Y, Kourai H (2005) Intermedilysin is essential forthe invasion of hepatoma Hep G2 cells by Streptococcus intermedius. Microbiol Immunol 49:681-694 (Pubitemid 41289355)
42. Sussman MD, Setlow P (1987) Nucleotide sequence of Bacillus megaterium gene homologous to the dna K gene of Escherichia coli. Nucleic Acids Res 15:3923
43. Takaya A, Tomoyasu T, Tokumitsu A, Morioka M, Yamamoto T (2002) The ATP-dependent lon protease of Salmonella enterica serovar Typhimurium regulates invasion and expression of genes carried on Salmonella pathogenicity island 1. J Bacteriol 184:224-32. doi:10.1128/JB.184.1.224-232.2002 (Pubitemid 34003303)
44. Takaya A, Tomoyasu T, Matsui H, Yamamoto T (2004) The Dna K/ Dna J chaperone machinery of Salmonella enterica serovar Typhimurium is essential for invasion of epithelial cells and survival within macrophages, leading to systemic infection. Infect Immun 72:1364-73. doi:10.1128/IAI.72.3.1364-1373.2004 (Pubitemid 38263757)
45. Tilly K, Hauser R, Campbell J, Ostheimer GJ (1993) Isolation of dna J, dna K, and grp E homologues from Borrelia burgdorferi and complementation of Escherichia coli mutants. Mol Microbiol 7:359-369 (Pubitemid 23051201)
46. Tomoyasu T, Mogk A, Langen H, Goloubinoff P, Bukau B (2001) Genetic dissection of the roles ofchaperones and proteases in protein folding and degradation in the Escherichia coli cytosol. Mol Microbiol 40:397-413. doi:10.1046/j.1365-2958.2001.02383.x (Pubitemid 32391634)
47. Tomoyasu T, Takaya A, Handa Y, Karata K, Yamamoto T (2005) Clp XP controls the expression of LEE genes in enterohaemorrhagic Escherichia coli. FEMS Microbiol Lett 253:59-66. doi:10.1016/j. femsle.2005.09.020 (Pubitemid 41605395)
48. Tomoyasu T, Tabata A, Hiroshima R, Imaki H, Masuda S, Whiley RA, Aduse-Opoku J, Kikuchi K, Hiramatsu K, Nagamune H (2010a) Role of catabolite control protein A in the regulation of intermedilysin production by Streptococcus intermedius. Infect Immun 78:4012-4021. doi:10.1128/IAI.00113-10
49. Tomoyasu T, Tabata A, Nagamune H (2010b) Investigation of the chaperone function of the small heat shock protein-Ags A. BMC Biochem 24:11-27. doi:10.1186/1471-2091-11-27
50. Whiley RA, Fraser H, Hardie JM, Beighton D (1990) Phenotypic differentiation of Streptococcus intermedius, Streptococcus constel-latus, and Streptococcus anginosus strains within the "Streptococcus milleri group". J Clin Microbiol 28:1497-1501 (Pubitemid 20212873)
51. Whiley RA, Beighton D, Winstanley TG, Fraser HY, Hardie JM (1992) Streptococcus intermedius, Streptococcus constellatus, and Streptococcus anginosus (the Streptococcus milleri group): association with different body sites and clinical infections. J Clin Microbiol 30:243-244
52. Woodbury R, Haldenwang WG (2003) Hrc A is a negative regulator of the dna K and gro ESL operons of Streptococcus pyogenes. Biochem Biophys Res Commun 302:722-727. doi:10.1016/ S0006-291X(03)00254-7 (Pubitemid 36294033)
53. Yamamoto T, Sashinami H, Takaya A, Tomoyasu T, Matsui H, Kikuchi Y, Hanawa T, Kamiya S, Nakane A (2001) Disruption of the genes for Clp XP protease in Salmonella enterica serovar Typhimurium results in persistent infection in mice, and development of persistence requires endogenous gamma inter-feron and tumor necrosis factor alpha. Infect Immun 69:3164-3174. doi:10.1128/IAI.69.5. 3164-31742001 (Pubitemid 32332213)
54. Yura T, Nakahigashi K(1999) Regulation of the heat-shock response. Curr Opin Microbiol 2:153-158. doi:10.1016/S1369-5274(99)80027-7 (Pubitemid 29176938)