The Phop/PhoQ system and Its role in serratia marcescens pathogenesis

Journal of Bacteriology

Volumn 194, Issue 11, 2012, Pages 2949-2961

  Barchiesi, Julieta ^a   Castelli, María Eugenia ^a   Di Venanzio, Gisela ^a   Colombo, María Isabel ^b   Véscovi, Eleonora García ^a  

^a UNIVERSIDAD NACIONAL DE ROSARIO   (Argentina)

^b Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; MAGNESIUM; PHOP PROTEIN; PHOQ PROTEIN; POLYMYXIN B; UNCLASSIFIED DRUG;

ACIDITY; ANIMAL CELL; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM MUTANT; CELL SURVIVAL; CONTROLLED STUDY; DNA BINDING MOTIF; ENVIRONMENTAL FACTOR; EPITHELIUM CELL; HOMEOSTASIS; NONHUMAN; ORTHOLOGY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SERRATIA MARCESCENS;

ACIDS; AMINO ACID SEQUENCE; ANIMALS; BACTERIAL PROTEINS; BASE SEQUENCE; CELL LINE; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; LYSOSOMES; MAGNESIUM; MICROBIAL VIABILITY; MOLECULAR SEQUENCE DATA; SEQUENCE ALIGNMENT; SERRATIA INFECTIONS; SERRATIA MARCESCENS; VIRULENCE;

BACTERIA (MICROORGANISMS); SERRATIA; SERRATIA MARCESCENS;

EID: 84863992178     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.06820-11     Document Type: Article

References (75)

1. Alexeyev MF. 1999. The pKNOCK series of broad-host-range mobilizable suicide vectors for gene knockout and targeted DNA insertion into the chromosome of gram-negative bacteria. Biotechniques 26:824-826, 828.
2. Anderson GG, Yahr TL, Lovewell RR, O'Toole GA. 2010. The Pseudomonas aeruginosa magnesium transporter MgtE inhibits transcription of the type III secretion system. Infect. Immun. 78:1239-1249.
3. Bailey TL, Elkan C. 1995. The value of prior knowledge in discovering motifs with MEME. Proc. Int. Conf. Intell. Syst. Mol. Biol. 3:21-29.
4. Bailey TL, Gribskov M. 1998. Methods and statistics for combining motif match scores. J. Comput. Biol. 5:211-221.
5. Bearson BL, Wilson L, Foster JW. 1998. A low pH-inducible, PhoPQdependent acid tolerance response protects Salmonella typhimurium against inorganic acid stress. J. Bacteriol. 180:2409-2417.
6. Bozue J, et al. 2011. The role of the phoPQ operon in the pathogenesis of the fully virulent CO92 strain of Yersinia pestis and the IP32953 strain of Yersinia pseudotuberculosis. Microb. Pathog. 50:314-321.
7. Bruce-Staskal PJ, Weidow CL, Gibson JJ, Bouton AH. 2002. Cas, Fak and Pyk2 function in diverse signaling cascades to promote Yersinia uptake. J. Cell Sci. 115:2689 -2700.
8. Cano DA, et al. 2001. Salmonella enterica serovar Typhimurium response involved in attenuation of pathogen intracellular proliferation. Infect. Immun. 69:64636474.
9. Castelli ME, et al. 2008. Enterobacterial common antigen integrity is a checkpoint for flagellar biogenesis in Serratia marcescens. J. Bacteriol. 190: 213-220.
10. 2+ regulation of the sensor protein PhoQ in Salmonella. J. Biol. Chem. 275:22948 -22954.
11. Cromie MJ, Shi Y, Latifi T, Groisman EA. 2006. An RNA sensor for intracellular Mg(2+). Cell 125:71-84.
12. Dann CE, et al. 2007. Structure and mechanism of a metal-sensing regulatory RNA. Cell 130:878-892.
13. de Lorenzo V, Herrero M, Jakubzik U, Timmis KN. 1990. Mini-Tn5 transposon derivatives for insertion mutagenesis, promoter probing, and chromosomal insertion of cloned DNA in gram-negative eubacteria. J. Bacteriol. 172:6568-6572.
14. Derzelle S, et al. 2004. The PhoP-PhoQ two-component regulatory system of Photorhabdus luminescens is essential for virulence in insects. J. Bacteriol. 186:1270-1279.
15. Drecktrah D, Knodler LA, Howe D, Steele-Mortimer O. 2007. Salmonella trafficking is defined by continuous dynamic interactions with the endolysosomal system. Traffic 8:212-225.
16. Fedrigo GV, Campoy EM, Di Venanzio G, Colombo MI, Garcia Vescovi E. 2011. Serratia marcescens is able to survive and proliferate in autophagic-like vacuoles inside non-phagocytic cells. PLoS One 6:24054.
17. Ferrer NL, Gomez AB, Neyrolles O, Gicquel B, Martin C. 2010. Interactions of attenuated Mycobacterium tuberculosis phoP mutant with human macrophages. PLoS One 5:12978.
18. Flego D, et al. 2000. A two-component regulatory system, pehR-pehS, controls endopolygalacturonase production and virulence in the plant pathogen Erwinia carotovora subsp. carotovora. Mol. Plant Microbe Interact. 13:447-455.
19. Flyg C, Kenne K, Boman HG. 1980. Insect pathogenic properties of Serratia marcescens: phage-resistant mutants with a decreased resistance to Cecropia immunity and a decreased virulence to Drosophila. J. Gen. Microbiol. 120:173-181.
20. Garcia-del Portillo F, Nunez-Hernandez C, Eisman B, Ramos-Vivas J. 2008. Growth control in the Salmonella-containing vacuole. Curr. Opin. Microbiol. 11:46-52.
21. Garcia Vescovi E, Sciara MI, Castelli ME. 2010. Two component systems in the spatial program of bacteria. Curr. Opin. Microbiol. 13:210-218.
22. Garcia Vescovi E, Soncini FC, Groisman EA. 1996. Mg2+ as an extracellular signal: environmental regulation of Salmonella virulence. Cell 84: 165-174.
23. Gardner PP, et al. 2011. Rfam: Wikipedia, clans and the decimal release. Nucleic Acids Res. 39:D141-D145.
24. Garvis SG, Beuzon CR, Holden DW. 2001. A role for the PhoP/Q regulon in inhibition of fusion between lysosomes and Salmonella-containing vacuoles in macrophages. Cell Microbiol. 3:731-744.
25. Gillespie JJ, et al. 2011. PATRIC: the comprehensive bacterial bioinformatics resource with a focus on human pathogenic species. Infect. Immun. 79:4286-4298.
26. Gooderham WJ, et al. 2009. The sensor kinase PhoQ mediates virulence in Pseudomonas aeruginosa. Microbiology 155:699-711.
27. 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.
28. Gupta S, Sinha A, Sarkar D. 2006. Transcriptional autoregulation by Mycobacterium tuberculosis PhoP involves recognition of novel direct repeat sequences in the regulatory region of the promoter. FEBS Lett. 580: 5328-5338.
29. Gutierrez MG, Munafo DB, Beron W, Colombo MI. 2004. Rab7 is required for the normal progression of the autophagic pathway in mammalian cells. J. Cell Sci. 117:2687-2697.
30. Harari O, Park SY, Huang H, Groisman EA, Zwir I. 2010. Defining the plasticity of transcription factor binding sites by deconstructing DNA consensus sequences: the PhoP-binding sites among gamma/ enterobacteria. PLoS Comput. Biol. 6:1000862.
31. Heesemann J, Laufs R. 1985. Double immunofluorescence microscopic technique for accurate differentiation of extracellularly and intracellularly located bacteria in cell culture. J. Clin. Microbiol. 22:168-175.
32. Hejazi A, Aucken HM, Falkiner FR. 2000. Epidemiology and susceptibility of Serratia marcescens in a large general hospital over an 8-year period. J. Hosp. Infect. 45:42-46.
33. Hejazi A, Falkiner FR. 1997. Serratia marcescens. J. Med. Microbiol. 46:903-912.
34. Hertle R, Schwarz H. 2004. Serratia marcescens internalization and replication in human bladder epithelial cells. BMC Infect. Dis. 4:16.
35. Holden DW. 2002. Trafficking of the Salmonella vacuole in macrophages. Traffic 3:161-169.
36. Jager S, et al. 2004. Role for Rab7 in maturation of late autophagic vacuoles. J. Cell Sci. 117:4837-4848.
37. Jamet A, et al. 2009. A two-component system is required for colonization of host cells by meningococcus. Microbiology 155:2288-2295.
38. Johnson CR, et al. 2001. Generation and characterization of a PhoP homologue mutant of Neisseria meningitidis. Mol. Microbiol. 39:1345-1355.
39. 2+-responsive promoters. J. Bacteriol. 181:5516-5520.
40. Kornfeld S. 1986. Trafficking of lysosomal enzymes in normal and disease states. J. Clin. Invest. 77:1- 6.
41. Kovach ME, et al. 1995. Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166:175-176.
42. Kramer A, Schwebke I, Kampf G. 2006. How long do nosocomial pathogens persist on inanimate surfaces? A systematic review. BMC Infect. Dis. 6:130.
43. Laupland KB, et al. 2008. Population-based laboratory surveillance for Serratia species isolates in a large Canadian health region. Eur. J. Clin. Microbiol. Infect. Dis. 27:89-95.
44. Lee JS, et al. 2008. Mutation in the transcriptional regulator PhoP contributes to avirulence of Mycobacterium tuberculosis H37Ra strain. Cell Host Microbe 3:97-103.
45. 2+-responsive PhoP-PhoQ regulon in Salmonella enterica. J. Bacteriol. 185:6287-6294.
46. Llama-Palacios A, Lopez-Solanilla E, Poza-Carrion C, Garcia-Olmedo F, Rodriguez-Palenzuela P. 2003. The Erwinia chrysanthemi phoP-phoQ operon plays an important role in growth at low pH, virulence and bacterial survival in plant tissue. Mol. Microbiol. 49:347-357.
47. Ludwig T, et al. 1994. Differential sorting of lysosomal enzymes in mannose 6-phosphate receptor-deficient fibroblasts. EMBO J. 13:3430-3437.
48. Mahlen SD. 2011. Serratia infections: from military experiments to current practice. Clin. Microbiol. Rev. 24:755-791.
49. 2+ transport protein is involved in Aeromonas hydrophila adherence. FEMS Microbiol. Lett. 198:18-195.
50. Miller JH. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
51. Monsieurs P, et al. 2005. Comparison of the PhoPQ regulon in Escherichia coli and Salmonella typhimurium. J. Mol. Evol. 60:462-474.
52. 2+ channels. Physiology (Bethesda) 23:275-285.
53. Moss JE, Fisher PE, Vick B, Groisman EA, Zychlinsky A. 2000. The regulatory protein PhoP controls susceptibility to the host inflammatory response in Shigella flexneri. Cell Microbiol. 2:443-452.
54. Munier-Lehmann H, Mauxion F, Bauer U, Lobel P, Hoflack B. 1996. Re-expression of the mannose 6-phosphate receptors in receptordeficient fibroblasts. Complementary function of the two mannose 6-phosphate receptors in lysosomal enzyme targeting. J. Biol. Chem. 271: 15166-15174.
55. Nakka S, Qi M, Zhao Y. 2010. The Erwinia amylovora PhoPQ system is involved in resistance to antimicrobial peptide and suppresses gene expression of two novel type III secretion systems. Microbiol. Res. 165:665-673.
56. Nehme NT, et al. 2007. A model of bacterial intestinal infections in Drosophila melanogaster. PLoS Pathog. 3:173.
57. Nelson DL, Kennedy EP. 1971. Magnesium transport in Escherichia coli. Inhibition by cobaltous ion. J. Biol. Chem. 246:3042-3049.
58. Noda T, Yoshimori T. 2010. Between canonical and antibacterial autophagy: Rab7 is required for GAS-containing autophagosome-like vacuole formation. Autophagy 6:419-420.
59. Oh YK, Swanson JA. 1996. Different fates of phagocytosed particles after delivery into macrophage lysosomes. J. Cell Biol. 132:585-593.
60. Oyston PC, et al. 2000. The response regulator PhoP is important for survival under conditions of macrophage-induced stress and virulence in Yersinia pestis. Infect. Immun. 68:3419-3425.
61. Perez E, et al. 2001. An essential role for phoP in Mycobacterium tuberculosis virulence. Mol. Microbiol. 41:179-187.
62. Perez JC, et al. 2009. Evolution of a bacterial regulon controlling virulence and Mg(2+) homeostasis. PLoS Genet. 5:1000428.
63. Prost LR, et al. 2007. Activation of the bacterial sensor kinase PhoQ by acidic pH. Mol. Cell 26:165-174.
64. Romano PS, Gutierrez MG, Beron W, Rabinovitch M, Colombo MI. 2007. The autophagic pathway is actively modulated by phase II Coxiella burnetii to efficiently replicate in the host cell. Cell Microbiol. 9:891-909.
65. Sieira R, Comerci DJ, Pietrasanta LI, Ugalde RA. 2004. Integration host factor is involved in transcriptional regulation of the Brucella abortus virB operon. Mol. Microbiol. 54:808-822.
66. Smith RL, Maguire ME. 1998. Microbial magnesium transport: unusual transporters searching for identity. Mol. Microbiol. 28:217-226.
67. Soncini FC, García Véscovi E, Solomon F, Groisman EA. 1996. Molecular basis of the magnesium deprivation response in Salmonella typhimurium: identification of PhoP-regulated genes. J. Bacteriol. 178:5092-5099.
68. Soncini FC, Vescovi EG, Groisman EA. 1995. Transcriptional autoregulation of the Salmonella typhimurium phoPQ operon. J. Bacteriol. 177: 4364-4371.
69. Spinelli SV, Pontel LB, Garcia VE, Soncini FC. 2008. Regulation of magnesium homeostasis in Salmonella: Mg(2+) targets the mgtA transcript for degradation by RNase E. FEMS Microbiol. Lett. 280:226-234.
70. Thompson JA, Liu M, Helaine S, Holden DW. 2011. Contribution of the PhoP/Q regulon to survival and replication of Salmonella enterica serovar Typhimurium in macrophages. Microbiology 157:2084-2093.
71. Tierrez A, Garcia-del Portillo F. 2005. New concepts in Salmonella virulence: the importance of reducing the intracellular growth rate in the host. Cell Microbiol. 7:901-909.
72. 2+ transporter from Providencia stuartii and the distribution of mgtE in gram-negative and gram-positive bacteria. J. Bacteriol. 177:5350-5354.
73. Tzeng YL, et al. 2006. Autoregulation of the MisR/MisS two-component signal transduction system in Neisseria meningitidis. J. Bacteriol. 188: 5055-5065.
74. 2+-responsive PhoP regulator in Yersinia pestis. FEMS Microbiol. Lett. 250:85-95.
75. Zwir I, et al. 2005. Dissecting the PhoP regulatory network of Escherichia coli and Salmonella enterica. Proc. Natl. Acad. Sci. U. S. A. 102:2862-2867.