Polynucleotide phosphorylase negatively controls spv virulence gene expression in Salmonella enterica

Infection and Immunity

Volumn 74, Issue 2, 2006, Pages 1243-1254

  Ygberg, Sofia Eriksson ^a   Clements, Mark O ^b   Rytkönen, Anne ^c   Thompson, Arthur ^d   Holden, David W ^c   Hinton, Jay C D ^d   Rhen, Mikael ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c IMPERIAL COLLEGE LONDON   (United Kingdom)

^d INSTITUTE OF FOOD RESEARCH   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; POLYRIBONUCLEOTIDE NUCLEOTIDYLTRANSFERASE; TRANSCRIPTOME; VIRULENCE FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL GROWTH; BACTERIAL VIRULENCE; BACTERIUM CULTURE; BACTERIUM MUTANT; CULTURE MEDIUM; ENZYME ACTIVITY; ENZYME DEFICIENCY; FEMALE; GENE CONTROL; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENE INDUCTION; MACROPHAGE; MOUSE; NONHUMAN; PNP GENE; PRIORITY JOURNAL; PROTEIN FUNCTION; SALMONELLA ENTERICA; SALMONELLOSIS; UPREGULATION;

ANIMALS; BACTERIAL PROTEINS; CELL LINE; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; MACROPHAGES; MICE; MICE, INBRED BALB C; MUTATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PLASMIDS; POLYRIBONUCLEOTIDE NUCLEOTIDYLTRANSFERASE; PROTEOME; SALMONELLA TYPHIMURIUM; TRANSCRIPTION FACTORS; VIRULENCE; VIRULENCE FACTORS;

EID: 31844446927     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.74.2.1243-1254.2006     Document Type: Article

References (87)

1. Abe, A., and K. Kawahara. 1995. Transcriptional regulation and promoter sequence of the spvR gene of virulence plasmid pKDSC50 in Salmonella choleraesuis serovar Choleraesuis. FEMS Microbiol. Lett. 129:225-230.
2. Bernstein, J. A., P. H. Lin, S. N. Cohen, and S. Lin-Chao. 2004. Global analysis of Escherichia coli RNA degradosome function using DNA microarrays. Proc. Natl. Acad. Sci. USA 101:2758-2763.
3. Beuzon, C. R., S. Meresse, K. E. Unsworth, J. Ruiz-Albert, S. Garvis, S. R. Waterman, T. A. Ryder, E. Boucrot, and D. W. Holden. 2000. Salmonella maintains the integrity of its intracellular vacuole through the action of SifA. EMBO J. 19:3235-3249.
4. Björkman, J., M. Rhen, and D. I. Andersson. 1996. Salmonella typhimurium cob mutants are not hypervirulent. FEMS Microbiol. Lett. 139:121-126.
5. Caldwell, A. L., and P. A. Gulig. 1991. The Salmonella typhimurium virulence plasmid encodes a positive regulator of a plasmid-encoded virulence gene. J. Bacteriol. 173:7176-7185.
6. Carniel, E. 2002. Plasmids and pathogenicity islands in Yersinia. Curr. Top. Microbiol. Immunol. 264:89-108.
7. Carpousis, A. J. 2002. The Escherichia coli RNA degradosome: structure, function and relationship in other ribonucleolytic multienzyme complexes. Biochem. Soc. Trans. 30:150-155.
8. Carter, P. B., and F. M. Collins. 1974. The route of enteric infection in normal mice. J. Exp. Med. 139:1189-1203.
9. Chen, L. M., K. Kaniga, and J. E. Galán. 1996. Salmonella spp. are cytotoxic for cultured macrophages. Mol. Microbiol. 21:1101-1115.
10. Clements, M., S. Eriksson, D. Tezcan-Merdol, J. C. Hinton, and M. Rhen. 2001. Virulence gene regulation in Salmonella enterica. Ann. Med. 33:178-185.
11. Clements, M. O., S. Eriksson, A. Thompson, S. Lucchini, J. C. Hinton, S. Normark, and M. Rhen. 2002. Polynucleotide phosphorylase is a global regulator of virulence and persistency in Salmonella enterica. Proc. Natl. Acad. Sci. USA 99:8784-8789.
12. Collazo, C. M., and J. E. Galán. 1997. The invasion-associated type III protein secretion system in Salmonella-a review. Gene 192:51-59.
13. Coynault, C., V. Robbe-Saule, M. Y. Popoff, and F. Norel. 1992. Growth phase and SpvR regulation of Salmonella typhimurium spvABC virulence genes. Microb. Pathog. 13:133-145.
14. Decktrach, D., L. A. Knodler, K. Galbraith, and O. Steele-Mortimer. 2005. The Salmonella SPI1 effector SopB stimulates nitric oxide production long after invasion. Cell. Microbiol. 7:105-113.
15. El-Gedaily, A., G. Paesold, C.-Y. Chen, G. D. Guiney, and M. Krause. 1997. Plasmid virulence gene expression induced by short chain fatty acids in Salmonella dublin: identification of rpoS-dependent and rpoS-independent mechanisms. J. Bacteriol. 179:1409-1412.
16. Eriksson, S., M. Clements, and M. Rhen. 2001. Salmonella as a tenant in phagocytic cells. Res. Adv. Microbiol. 2:87-102.
17. Eriksson, S., S. Lucchini, A. Thompson, M. Rhen, and J. C. Hinton. 2003. Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol. Microbiol. 47:103-118.
18. Eriksson, S., B. J. Chambers, and M. Rhen. 2003. Nitric oxide production by murine dendritic cells is cytotoxic for intracellular Salmonella typhimurium. Scand. J. Immunol. 58:493-502.
19. Fahlen, T. F., N. Mathur, and B. D. Jones. 2000. Identification and characterization of mutants with increased expression of hilA, the invasion gene transcriptional activator of Salmonella typhimurium. FEMS Immunol. Med. Microbiol. 28:25-35.
20. Fang, F. C., M. Krause, C. Roudier, J. Fierer, and D. G. Guiney. 1991. Growth regulation of a Salmonella plasmid gene essential for virulence. J. Bacteriol. 173:6783-6789.
21. Fang, F. C., S. J. Libby, N. A. Buchmeier, P. C. Loewen, J. Switala, J. Harwood, and D. G. Guiney. 1992. The alternative σ-factor KatF (RpoS) regulates Salmonella virulence. Proc. Natl. Acad. Sci. USA 89:11978-11982.
22. Favaro, R., and G. Deho. 2003. Polynucleotide phosphorylase-deficient mutants of Pseudomonas putida. J. Bacteriol. 185:5279-5286.
23. Fields, P. I., E. A. Groisman, and F. Heffron. 1989. A Salmonella locus that controls resistance to microbicidal proteins from phagocytic cells. Science 243:1059-1062.
24. Fierer, J., L. Eckmann, F. Fang, C. Pfeifer, B. B. Finlay, and D. G. Guiney. 1993. Expression of the Salmonella virulence plasmid gene spvB in cultured macrophages and non-phagocytic cells. Infect. Immun. 61:5231-5236.
25. Figueroa-Bossi, N., and L. Bossi. 1999. Inducible prophages contribute to Salmonella virulence in mice. Mol. Microbiol. 33:167-176.
26. Galán, J. E., and D. Zhou. 2000. Striking a balance: modulation of the actin cytoskeleton by Salmonella. Proc. Natl. Acad. Sci. USA 97:8754-8761.
27. Garvis, S. G., C. R. Beuzon, and D. W. Holden. 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.
28. Gerschenson, L. E., and R. J. Rotello. 1992. Apoptosis: a different type of cell death. FASEB J. 6:2450-2455.
29. Goverde, R. L., J. H. Huisin't Veld, J. G. Kusters, and F. R. Mooi. 1998. The psychrotrophic bacterium Yersinia enterocolitica requires expression of pnp, the gene for polynucleotide phosphorylase, for growth at low temperature (5°C). Mol. Microbiol. 28:555-569.
30. Groisman, E. A. 2001. The pleiotropic two-component regulatory system PhoP-PhoQ. J. Bacteriol. 183:1835-1842.
31. Groisman, E. A., and H. Ochman. 1997. How Salmonella became a pathogen. Trends Microbiol. 5:343-349.
32. Gulig, P. A., H. Danbara, D. G. Guiney, A. J. Lax, F. Norel, and M. Rhen. 1993. Molecular analysis of spv virulence genes of the Salmonella virulence plasmid. Mol. Microbiol. 7:825-830.
33. Gulig, P. A., and T. J. Doyle. 1993. The Salmonella typhimurium virulence plasmid increases the growth rate of Salmonellae in mice. Infect. Immun. 61:504-511.
34. Hansen-Wester, I., and M. Hensel. 2001. Salmonella pathogenicity islands encoding type III secretion systems. Microbes Infect. 3:549-559.
35. Heiskanen, P., S. Taira, and M. Rhen. 1994. Role of rpoS in the regulation of spv virulence genes of Salmonella typhimurium. FEMS Microbiol. Lett. 123:125-130.
36. Hinton, J. C., I. Hautefort, S. Eriksson, A. Thompson, and M. Rhen. 2004. Benefits and pitfalls of using microarrays to monitor bacterial gene expression during infection. Curr. Opin. Microbiol. 7:277-282.
37. Hobbie, S., L. M. Chen, R. J. Davis, and J. E. Galán. 1997. Involvement of mitogen-activated protein kinase pathways in the nuclear responses and cytokine production induced by Salmonella typhimurium in cultured intestinal epithelial cells. J. Immunol. 159:5550-5559.
38. Hurme, R., K. D. Berndt, S. J. Normark, and M. Rhen. 1997. A proteinaceous gene regulatory thermometer in Salmonella. Cell 90:55-64.
39. Kim, C. C., and S. Falkow. 2004. Delineation of upstream signaling events in the Salmonella pathogenicity island 2 transcriptional activation pathway. J. Bacteriol. 186:4694-4704.
40. Knodler, L. A., J. Celli, W. D. Hardt, B. A. Vallance, C. Yip, and B. B. Finlay. 2002. Salmonella effectors within a single pathogenicity island are differentially expressed and translocated by separate type III secretion systems. Mol. Microbiol. 43:1089-1103.
41. Kowarz, L., C. Coynault, V. Robbe-Saule, and F. Norel. 1994. The Salmonella typhimurium kalF (rpoS) gene: cloning, nucleotide sequence, and regulation of spvR and spvABCD virulence plasmid genes. J. Bacteriol. 176:6852-6860.
42. Kox, L. F., M. M. Wosten, and E. A. Groisman. 2000. A small protein that mediates the activation of a two-component system by another two-component system. EMBO J. 19:1861-1872.
43. Krause, M., C. Roudier, J. Fierer, J. Hardwood, and D. G. Guiney. 1991. Molecular analysis of the virulence locus of the Salmonella dublin plasmid pSDL2. Mol. Microbiol. 5:307-316.
44. Kudla, J., R. Hayes, and W. Gruissem. 1996. Polyadenylation accelerates degradation of chloroplast mRNA. EMBO J. 15:7137-7146.
45. Kurita, A., H. Gotoh, M. Eguchi, N. Okada, S. Matsumura, H. Mastui, H. Danbara, and Y. Kikuchi. 2003. Intracellular expression of the Salmonella virulence plasmid virulence protein SpvB causes apoptotic cell death in eukaryotic cells. Microb. Pathog. 35:43-48.
46. Lesnick, M. L., N. E. Reiner, J. U. Fierer, and D. G. Guiney. 2001. The Salmonella spvB virulence gene encodes an enzyme that ADP-ribosylates actin and destabilizes the cytoskeleton of eukaryotic cells. Mol. Microbiol. 39:1464-1470.
47. Leszczyniecka, M., R. DeSalle, D. C. Kang, and P. B. Fisher. 2004. The origin of polynucleotide phosphorylase domains. Mol. Phylogenet. Evol. 31:123-130.
48. Leszczyniecka, M., D. C. Kang, D. Sarkar, Z. Z. Su, M. Holmes, K. Valerie, and P. B. Fisher. 2002. Identification and cloning of human polynucleotide phosphorylase, hPNPase old-35, in the context of terminal differentiation and cellular senescence. Proc. Natl. Acad. Sci. USA 99:16636-16641.
49. Libby, S. J., M. Lesnick, P. Hasegawa, E. Weidenhammer, and D. G. Guiney. 2000. The Salmonella virulence plasmid spv genes are required for cytopathology in human monocyte-derived macrophages. Cell. Microbiol. 2:49-58.
50. Lundberg, U., U. Vinatzer, D. Berdnik, A. von Gabain, and M. Baccarini. 1999. Growth phase-regulated induction of Salmonella-induced macrophage apoptosis correlates with transient expression of SPI-1 genes. J. Bacteriol. 181:3433-3437.
51. Mangan, D. F., and S. M. Wahl. 1991. Differential regulation of human monocyte programmed cell death (apoptosis) by chemotactic factors and proinflammatory cytokines. J. Immunol. 147:3408-3412.
52. Marshall, D. G., B. J. Sheehan, and C. J. Dorman. 1999. A role for the leucine-responsive regulator protein and integration host factor in the regulation of the Salmonella plasmid virulence (spv) locus in Salmonella typhimurium. Mol. Microbiol. 34:134-145.
53. Mastroeni, P., and M. Sheppard. 2004. Salmonella infections in the mouse model: host resistance factors and in vivo dynamics of bacterial spread and distribution in the tissues. Microb. Infect. 6:398-405.
54. Matsui, H., A. Abe, S. Suzuki, M. Kijima, Y. Tamura, M. Nakamura, K. Kawahara, and H. Danbara. 1993. Molecular mechanism of the regulation of expression of plasmid-encoded mouse bacteremia (mba) genes in Salmonella serovar cholearesuis. Mol. Gen. Genet. 236:219-226.
55. McClelland, M., K. E. Sanderson, J. Spieth, S. W. Clifton, P. Latreille, L. Courtney, S. Porwollik, J. Ali, M. Dante, F. Du, S. Hou, D. Layman, S. Leonard, C. Nguyen, K. Scott, A. Holmes, N. Grewal, E. Mulvaney, E. Ryan, H. Sun, L. Florea, W. Miller, T. Stoneking, M. Nhan, R. Waterston, and R. K. Wilson. 2001. Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413:852-856.
56. Meresse, S., K. E. Unsworth, A. Habermann, G. Griffiths, F. Fang, M. J. Martinez-Lorenzo, et al 2001. Remodelling of the actin cytoskeleton is essential for replication of intravacuolar Salmonella. Cell. Microbiol. 3:567-577.
57. Miao, E. A., M. Brittnacher, A. Haraga, R. L. Jeng, M. D. Welch, and S. I. Miller. 2003. Salmonella effectors translocated across the vacuolar membrane interact with the actin cytoskeleton. Mol. Microbiol. 48:401-415.
58. Miki, T., N. Okada, and H. Danbara. 2004. Two periplasmic disulfide oxidoreductases, DsbA and SrgA, target outer membrane protein SpiA, a component of the Salmonella pathogenicity island type III secretion system. J. Biol. Chem. 279:34631-34642.
59. Miller, J. H. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Press, Cold Spring Harbor, N.Y.
60. Miller, S. I., and J. J. Mekalanos. 1990. Constitutive expression of the phoP regulon attenuates Salmonella virulence and survival within macrophages. J. Bacteriol. 172:2485-2490.
61. +/+ mice and can be reactivated by IFN-γ neutralization. J. Exp. Med. 199:231-241.
62. Monack, D. M., C. S. Detweiler, and S. Falkow. 2001. Salmonella pathogenicity island 2-dependent macrophage death is mediated in part by the host cysteine protease caspase-1. Cell. Microbiol. 3:825-837.
63. Monack, D. M., W. W. Navarre, and S. Falkow. 2001. Salmonella-induced macrophage death: the role of caspase-1 in death and inflammation. Microb. Infect. 3:1201-1212.
64. Monsieurs, P., S. de Keersmaecker, W. W. Navarre, M. W. Bader, F. De Smet, M. McLelland, F. C. Fang, B. De Moor, J. Vanderleyden, and K. Marchal. 2005. Comparison of the PhoPQ regulon in Escherichia coli and Salmonella typhimurium. J. Mol. Evol. 60:462-479.
65. O'Byrne, C. P., and C. J. Dorman. 1994. Transcription of the Salmonella typhimurium spv virulence locus is regulated negatively by the nucleoid-associated protein H-NS. FEMS Microbiol. Lett. 121:99-106.
66. O'Byrne, C. P., and C. J. Dorman. 1994. The spv virulence operon of Salmonella typhimurium LT-2 is negatively regulated by the cyclic AMP (cAMP)-cAMP receptor protein system. J. Bacteriol. 176:905-912.
67. Otto, H., D. Tezcan, R. Girish, F. Haag, M. Rhen, and F. Koch-Nolte. 2000. The spvB gene product of the Salmonella enterica virulence plasmid is a mono(ADP-ribosyl)transferase. Mol. Microbiol. 37:1106-1115.
68. Pullinger, G. D., G. D. Baird, G. M. Williamson, and A. J. Lax. 1989. Nucleotide sequence of a plasmid gene involved in the virulence of Salmonella. Nucleic Acids Res. 17:7983.
69. Py, B., C. F. Higgins, H. M. Krisch, and A. J. Caprousis. 1996. A DEAD-box RNA helicase in the Escherichia coli RNA degradosome. Nature 381:169-172.
70. Raupach, B., N. Kurth, K. Pfeffer, and S. H. E. Kaufmann. 2003. Salmonella typhimurium strains carrying independent mutations display similar virulence phenotypes yet are controlled by distinct host defense mechanisms. J. Immunol. 170:6133-6140.
71. Rhen, M., and C. J. Dorman. 2005. Hierarchial gene regulators adapt Salmonella enterica to its host milieus. Int. J. Med. Microbiol. 294:487-502.
72. Rhen, M., P. Riikonen, and S. Taira. 1993. Transcriptional regulation of Salmonella enterica virulence plasmid genes in cultured macrophages. Mol. Microbiol. 10:45-56.
73. Rhen, M., M. Virtanen, and P. H. Mäkelä. 1989. Localization by insertion mutagenesis of a virulence-associated region on the Salmonella typhimurium 96 kilobase pair plasmid. Microb. Pathog. 6:153-158.
74. Rosenzweig, J. A., G. Weltman, G. V. Plane, and K. Schesser. 2005. Modulation of Yersinia type three secretion system by the S1 domain of polynucleotide phosphorylase. J. Biol. Chem. 280:156-163.
75. Sarkar, D., M. Leszczyniecka, D. C. Kang, I. V. Lebedeva, K. Valerie, K., Dhar, S. Pandita, and P. B. Fisher. 2003. Down-regulation of Myc as a potential target for growth arrest induced by human polynucleotide phosphorylase (hPNPaseold-35) in human melanoma cells. J. Biol. Chem. 278:24542-24551.
76. Schmieger, H. 1972. Phage P22 mutants with increased or decreased transduction abilities. Mol. Gen. Genet. 119:75-78.
77. Shea, J. E., M. Hensel, C. Gleeson, and D. W. Holden. 1996. Identification of a virulence locus encoding a second type III secretion system in Salmonella typhimurium. Proc. Natl. Acad. Sci. USA 93:2593-2597.
78. Shea, J. E., C. R. Beuzon, C. Gleeson, R. Mundy, and D. W. Holden. 1999. Influence of the Salmonella typhimurium pathogenicity island 2 type III secretion system on bacterial growth in the mouse. Infect. Immun. 67:213-219.
79. Symmons, M. F., G. H. Jones, and B. F. Luisi. 2000. A duplicated fold is the structural basis for polynucleotide phosphorylase catalytic activity, processivity, and regulation. Structure Fold. Des. 8:1215-1226.
80. Taira, S., P. Heiskanen, R. Hurme, H. Heikkilä, P. Riikonen, and M. Rhen. 1995. Evidence for functional polymorphism of the spvR gene regulating virulence gene expression in Salmonella. Mol. Gen. Genet. 246:437-444.
81. Taira, S., P. Riikonen, H. Saarilahti, S. Sukupolvi, and M. Rhen. 1992. The mkaC virulence gene of the Salmonella serovar Typhimurium 96 kb plasmid encodes a transcriptional activator. Mol. Gen. Genet. 228:381-384.
82. Tedin, K., and U. Blasi. 1996. The RNA chain elongation rate of the lambda late mRNA is unaffected by high levels of ppGpp in the absence of amino acid starvation. J. Biol. Chem. 271:17675-17686.
83. Tezcan-Merdol, D., T. Nyman, U. Lindberg, F. Haag, F. Koch-Nolte, and M. Rhen. 2001. Actin is ADP-ribosylated by the Salmonella enterica virulence-associated protein SpvB. Mol. Microbiol. 39:606-619.
84. Wilson, J. A., T. J. Doyle, and P. A. Gulig. 1997. Exponential-phase expression of spvA of the Salmonella typhimurium virulence plasmid: induction in intracellular salts medium and intracellularly in mice and cultured mammalian cells. Microbiology 143:3827-3839.
85. Wilson, J. A., and P. A. Gulig. 1998. Regulation of the spvR gene of the Salmonella typhimurium virulence plasmid during exponential-phase growth in intracellular salts medium and a t stationary phase in L broth. Microbiology 144:1823-1833.
86. Yamanaka, K., and M. Inouye. 2001. Selective mRNA degradation by polynucleotide phosphorylase in cold shock adaptation in Escherichia coli. J. Bacteriol. 183:2808-2816.
87. Yehudai-Resheff, S., M. Hirsh, and G. Schuster. 2001. Polynucleotide phosphorylase functions as both an exonuclease and a poly(A) polymerase in spinach chloroplasts. Mol. Cell. Biol. 21:5408-5416.