Peptide-assisted degradation of the Salmonella MgtC virulence factor

EMBO Journal

Volumn 27, Issue 3, 2008, Pages 546-557

  Alix, Eric ^a,b   Blanc Potard, Anne Béatrice ^a,b  

^a INSERM   (France)

^b UNIV MONTPELLIER   (France)

Author keywords

FtsH; MgtC; Regulatory peptide; Salmonella enterica serovar Typhimurium

Indexed keywords

MEMBRANE PROTEIN; MGTC PROTEIN; MGTR PROTEIN; PEPTIDE; PROTEINASE; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; GENE OVEREXPRESSION; HYDROPHOBICITY; MOUSE; NEGATIVE FEEDBACK; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SALMONELLA; TWO HYBRID SYSTEM;

ADENOSINE TRIPHOSPHATASES; AMINO ACID SEQUENCE; ANIMALS; BACTERIAL PROTEINS; BASE SEQUENCE; CATION TRANSPORT PROTEINS; CELL LINE; DOWN-REGULATION; GENE EXPRESSION REGULATION, BACTERIAL; MACROPHAGES; MICE; MOLECULAR SEQUENCE DATA; PEPTIDES; REGULATORY SEQUENCES, NUCLEIC ACID; SALMONELLA TYPHIMURIUM; VIRULENCE; VIRULENCE FACTORS;

BACTERIA (MICROORGANISMS); SALMONELLA; SALMONELLA ENTERICA; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM;

EID: 38949185102     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/sj.emboj.7601983     Document Type: Article

References (48)

1. Adkins JN, Mottaz HM, Norbeck AD, Gustin JK, Rue J, Clauss TR, Purvine SO, Rodland KD, Heffron F, Smith RD (2006) Analysis of the Salmonella typhimurium proteome through environmental response toward infectious conditions. Mol Cell Proteomic 5: 1450-1461
2. Aldridge P, Karlinsey J, Hughes KT (2003) The type III secretion chaperone FlgN regulates flagellar assembly via a negative feedback loop containing its chaperone substrates FlgK and FlgL. Mol Microbiol 49: 1333-1345
3. Alix E, Blanc-Potard AB (2007) MgtC: a key player in intramacrophage survival. Trends Microbiol 15: 252-256
4. Baker TA, Sauer RT (2006) ATP-dependent proteases of bacteria: recognition logic and operating principles. Trends Biochem Sci 31: 647-653
5. Begg KJ, Tomoyasu T, Donachie WD, Khattar M, Niki H, Yamanaka K, Hiraga S, Ogura T (1992) Escherichia coli mutant Y16 is a double mutant carrying thermosensitive ftsH and ftsI mutations. J Bacteriol 174: 2416-2417
6. Blanc-Potard AB, Groisman EA (1997) The Salmonella selC locus contains a pathogenicity island mediating intramacrophage survival. EMBO J 16: 5376-5385
7. Blanc-Potard AB, Lafay B (2003) MgtC as a horizontally acquired virulence factor of intracellular bacterial pathogens: evidence from molecular phylogeny and comparative genomics. J Mol Evol 57: 479-486
8. Bolivar F, Rodriguez RL, Greene PJ, Betlach MC, Heyneker HL, Boyer HW (1977) Construction and characterization of new cloning vehicles. II. A multipurpose cloning system. Gene 2: 95-113
9. Buchmeier N, Blanc-Potard A, Ehrt S, Piddington D, Riley L, Groisman EA (2000) A parallel intraphagosomal survival strategy shared by Mycobacterium tuberculosis and Salmonella enterica. Mol Microbiol 35: 1375-1382
10. Cutting S, Anderson M, Lysenko E, Page A, Tomoyasu T, Tatematsu K, Tatsuta T, Kroos L, Ogura T (1997) SpoVM, a small protein essential to development in Bacillus subtilis, interacts with the ATP-dependent protease FtsH. J Bacteriol 179: 5534-5542
11. Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97: 6640-6645
12. Datta AB, Roy S, Parrack P (2005) Role of C-terminal residues in oligomerization and stability of lambda CII: implications for lysis-lysogeny decision of the phage. J Mol Biol 345: 315-324
13. Dougan DA, Mogk A, Zeth K, Turgay K, Bukau B (2002) AAA+ proteins and substrate recognition, it all depends on their partner in crime. FEBS Lett 529: 6-10
14. Eriksson S, Lucchini S, Thompson A, Rhen M, Hinton JC (2003) Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol Microbiol 47: 103-118
15. Frees D, Qazi SN, Hill PJ, Ingmer H (2003) Alternative roles of ClpX and ClpP in Staphylococcus aureus stress tolerance and virulence. Mol Microbiol 48: 1565-1578
16. 2+ as an extracellular signal: environmental regulation of Salmonella virulence. Cell 84: 165-174
17. Gottesman S (2003) Proteolysis in bacterial regulatory circuits. Annu Rev Cell Dev Biol 19: 565-587
18. Grabenstein JP, Fukuto HS, Palmer LE, Bliska JB (2006) Characterization of phagosome trafficking and identification of PhoP-regulated genes important for survival of Yersinia pestis in macrophages. Infect Immun 74: 3727-3741
19. 2+ transporter. Cold Spring Harb Symp Quant Biol 71: 251-258
20. +-ATPase. J Bacteriol 188: 5586-5594
21. Hanahan D (1983) Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166: 557-580
22. Hoskins JR, Wickner S (2006) Two peptide sequences can function cooperatively to facilitate binding and unfolding by ClpA and degradation by ClpAP. Proc Natl Acad Sci USA 103: 909-914
23. Ito K, Akiyama Y (2005) Cellular functions, mechanism of action, and regulation of FtsH protease. Annu Rev Microbiol 59: 211-231
24. Karimova G, Dautin N, Ladant D (2005) Interaction network among Escherichia coli membrane proteins involved in cell division as revealed by bacterial two-hybrid analysis. J Bacteriol 187: 2233-2243
25. Karimova G, Pidoux J, Ullmann A, Ladant D (1998) A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proc Natl Acad Sci USA 95: 5752-5756
26. Kovach ME, Phillips RW, Elzer PH, Roop RM, Peterson KM (1994) pBBR1MCS: a broad-host-range cloning vector. Biotechniques 16: 800-802
27. Kwon HY, Ogunniyi AD, Choi MH, Pyo SN, Rhee DK, Paton JC (2004) The ClpP protease of Streptococcus pneumoniae modulates virulence gene expression and protects against fatal pneumococcal challenge. Infect Immun 72: 5646-5653
28. 2+ environment. Infect Immun 73: 3160-3163
29. Lawley TD, Chan K, Thompson LJ, Kim CC, Govoni GR, Monack DM (2006) Genome-wide screen for Salmonella genes required for long-term systemic infection of the mouse. PLoS Pathog 2: e11
30. Maloney KE, Valvano MA (2006) The mgtC gene of Burkholderia cenocepacia is required for growth under magnesium limitation conditions and intracellular survival in macrophages. Infect Immun 74: 5477-5486
31. Maloy SR (1990) Experimental Techniques in Bacterial Genetics. Boston, MA: Jones and Bartlett Publishers
32. Manes NP, Gustin JK, Rue J, Mottaz HM, Purvine SO, Norbeck AD, Monroe ME, Zimmer JS, Metz TO, Adkins JN, Smith RD, Heffron F (2007) Targeted protein degradation by Salmonella under phagosome-mimicking culture conditions investigated using comparative peptidomics. Mol Cell Proteomics 6: 717-727
33. Miller JH (1972) Experiments in Molecular Genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory
34. Moncrief MB, Maguire ME (1998) Magnesium and the role of MgtC in growth of Salmonella typhimurium. Infect Immun 66: 3802-3809
35. Ogura T, Inoue K, Tatsuta T, Suzaki T, Karata K, Young K, Su LH, Fierke CA, Jackman JE, Raetz CR, Coleman J, Tomoyasu T, Matsuzawa H (1999) Balanced biosynthesis of major membrane components through regulated degradation of the committed enzyme of lipid A biosynthesis by the AAA protease FtsH (HflB) in Escherichia coli. Mol Microbiol 31: 833-844
36. Okuno T, Yamanaka K, Ogura T (2006) An AAA protease FtsH can initiate proteolysis from internal sites of a model substrate, apo-flavodoxin. Genes Cells 11: 261-268
37. Prajapati RS, Ogura T, Cutting SM (2000) Structural and functional studies on an FtsH inhibitor from Bacillus subtilis. Biochim Biophys Acta 1475: 353-359
38. Rang C, Alix E, Felix C, Heitz A, Tasse L, Blanc-Potard AB (2007) Dual role of the MgtC virulence factor in host and non-host environments. Mol Microbiol 63: 605-622
39. Schneider D, Finger C, Prodohl A, Volkmer T (2007) From interactions of single transmembrane helices to folding of alpha-helical membrane proteins: analyzing transmembrane helix-helix interactions in bacteria. Curr Protein Pept Sci 8: 45-61
40. Shi L, Adkins JN, Coleman JR, Schepmoes AA, Dohnkova A, Mottaz HM, Norbeck AD, Purvine SO, Manes NP, Smallwood HS, Wang H, Forbes J, Gros P, Uzzau S, Rodland KD, Heffron F, Smith RD, Squier TC (2006) Proteomic analysis of Salmonella enterica serovar Typhimurium isolated from RAW 264.7 macrophages: identification of a novel protein that contributes to the replication of serovar Typhimurium inside macrophages. J Biol Chem 281: 29131-29140
41. Smith RL, Kaczmarek MT, Kucharski LM, Maguire ME (1998) Magnesium transport in Salmonella typhimurium: regulation of mgtA and mgtCB during invasion of epithelial and macrophage cells. Microbiology 144: 1835-1843
42. 2+ transport locus of Salmonella typhimurium encodes a P-type ATPase. J Biol Chem 266: 815-823
43. Takaya A, Kubota Y, Isogai E, Yamamoto T (2005) Degradation of the HilC and HilD regulator proteins by ATP-dependent Lon protease leads to downregulation of Salmonella pathogenicity island 1 gene expression. Mol Microbiol 55: 839-852
44. Takaya A, Suzuki M, Matsui H, Tomoyasu T, Sashinami H, Nakane A, Yamamoto T (2003) Lon, a stress-induced ATP-dependent protease, is critically important for systemic Salmonella enterica serovar typhimurium infection of mice. Infect Immun 71: 690-696
45. Uzzau S, Figueroa-Bossi N, Rubino S, Bossi L (2001) Epitope tagging of chromosomal genes in Salmonella. Proc Natl Acad Sci USA 98: 15264-15269
46. Walters RF, DeGrado WF (2006) Helix-packing motifs in membrane proteins. Proc Natl Acad Sci USA 103: 13658-13663
47. Yamamoto T, Sashinami H, Takaya A, Tomoyasu T, Matsui H, Kikuchi Y, Hanawa T, Kamiya S, Nakane A (2001) Disruption of the genes for ClpXP protease in Salmonella enterica serovar Typhimurium results in persistent infection in mice, and development of persistence requires endogenous gamma interferon and tumor necrosis factor alpha. Infect Immun 69: 3164-3174
48. Zwir I, Shin D, Kato A, Nishino K, Latifi T, Solomon F, Hare JM, Huang H, Groisman EA (2005) Dissecting the PhoP regulatory network of Escherichia coli and Salmonella enterica. Proc Natl Acad Sci USA 102: 2862-2867