Polyamines are required for virulence in Salmonella enterica serovar Typhimurium

PLoS ONE

Volumn 7, Issue 4, 2012, Pages

  Jelsbak, Lotte ^a   Thomsen, Line Elnif ^a   Wallrodt, Inke ^a   Jensen, Peter Ruhdal ^b   Olsen, John Elmerdahl ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

POLYAMINE; PUTRESCINE; SPERMIDINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL GENE; BACTERIAL SURVIVAL; BACTERIAL VIRULENCE; BACTERIUM CULTURE; CAENORHABDITIS ELEGANS; CELL INVASION; CONTROLLED STUDY; DISEASE MODEL; FEMALE; GENE EXPRESSION; GENE LOCUS; HILA GENE; INVF GENE; MOUSE; NONHUMAN; PATHOGENICITY ISLAND; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM; SIGNAL TRANSDUCTION; SIPB GENE; SOPB GENE; SPEB GENE; TYPHOID FEVER; WILD TYPE; ANIMAL; ANIMAL SALMONELLOSIS; BIOASSAY; BIOSYNTHESIS; CELL PROLIFERATION; EPITHELIUM CELL; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; INTRACELLULAR SPACE; METABOLISM; MICROBIAL VIABILITY; MICROBIOLOGY; MUTATION; PATHOGENICITY; VIRULENCE;

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

ANIMALS; BIOLOGICAL ASSAY; BIOSYNTHETIC PATHWAYS; CAENORHABDITIS ELEGANS; CELL PROLIFERATION; EPITHELIAL CELLS; FEMALE; GENE EXPRESSION REGULATION, BACTERIAL; GENES, BACTERIAL; HUMANS; INTRACELLULAR SPACE; MICE; MICROBIAL VIABILITY; MUTATION; POLYAMINES; SALMONELLA INFECTIONS, ANIMAL; SALMONELLA TYPHIMURIUM; VIRULENCE;

EID: 84860454320     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0036149     Document Type: Article

References (68)

1. Galan JE, Curtiss R III, (1989) Cloning and molecular characterization of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells. Proc Natl Acad Sci U S A 86: 6383-6387.
2. Groisman EA, Ochman H, (1993) Cognate gene clusters govern invasion of host epithelial cells by Salmonella typhimurium and Shigella flexneri. EMBO J 12: 3779-3787.
3. Hensel M, Shea JE, Gleeson C, Jones MD, Dalton E, et al. (1995) Simultaneous identification of bacterial virulence genes by negative selection. Science 269: 400-403.
4. Shea JE, Hensel M, Gleeson C, Holden DW, (1996) Identification of a virulence locus encoding a second type III secretion system in Salmonella typhimurium. Proc Natl Acad Sci U S A 93: 2593-2597.
5. Kaniga K, Trollinger D, Galan JE, (1995) Identification of two targets of the type III protein secretion system encoded by the inv and spa loci of Salmonella typhimurium that have homology to the Shigella IpaD and IpaA proteins. J Bacteriol 177: 7078-7085.
6. Kaniga K, Tucker S, Trollinger D, Galan JE, (1995) Homologs of the Shigella IpaB and IpaC invasins are required for Salmonella typhimurium entry into cultured epithelial cells. J Bacteriol 177: 3965-3971.
7. Knodler LA, Vallance BA, Celli J, Winfree S, Hansen B, et al. (2010) Dissemination of invasive Salmonella via bacterial-induced extrusion of mucosal epithelia. Proc Natl Acad Sci U S A.
8. Vazquez-Torres A, Jones-Carson J, Baumler AJ, Falkow S, Valdivia R, et al. (1999) Extraintestinal dissemination of Salmonella by CD18-expressing phagocytes. Nature 401 804-808. 10.1038/44593 [doi].
9. Hopkins SA, Niedergang F, Corthesy-Theulaz IE, Kraehenbuhl JP, (2000) A recombinant Salmonella typhimurium vaccine strain is taken up and survives within murine Peyer's patch dendritic cells. Cell Microbiol 2 59-68. cmi35 [pii].
10. Mastroeni P, Grant AJ, (2011) Spread of Salmonella enterica in the body during systemic infection: unravelling host and pathogen determinants. Expert Rev Mol Med 13 e12. S1462399411001840 [pii];10.1017/S1462399411001840 [doi].
11. Beuzon CR, Meresse S, Unsworth KE, Ruiz-Albert J, Garvis S, et al. (2000) Salmonella maintains the integrity of its intracellular vacuole through the action of SifA. EMBO J 19: 3235-3249.
12. Deiwick J, Salcedo SP, Boucrot E, Gilliland SM, Henry T, et al. (2006) The translocated Salmonella effector proteins SseF and SseG interact and are required to establish an intracellular replication niche. Infect Immun 74: 6965-6972.
13. Hensel M, Shea JE, Waterman SR, Mundy R, Nikolaus T, et al. (1998) Genes encoding putative effector proteins of the type III secretion system of Salmonella pathogenicity island 2 are required for bacterial virulence and proliferation in macrophages. Mol Microbiol 30: 163-174.
14. Ibarra JA, Steele-Mortimer O, (2009) Salmonella - the ultimate insider. Salmonella virulence factors that modulate intracellular survival. Cell Microbiol 11: 1579-1586.
15. Steele-Mortimer O, Brumell JH, Knodler LA, Meresse S, Lopez A, et al. (2002) The invasion-associated type III secretion system of Salmonella enterica serovar Typhimurium is necessary for intracellular proliferation and vacuole biogenesis in epithelial cells. Cell Microbiol 4: 43-54.
16. Guy RL, Gonias LA, Stein MA, (2000) Aggregation of host endosomes by Salmonella requires SPI2 translocation of SseFG and involves SpvR and the fms-aroE intragenic region. Mol Microbiol 37: 1417-1435.
17. Cirillo DM, Valdivia RH, Monack DM, Falkow S, (1998) Macrophage-dependent induction of the Salmonella pathogenicity island 2 type III secretion system and its role in intracellular survival. Mol Microbiol 30: 175-188.
18. Ochman H, Groisman EA, (1996) Distribution of pathogenicity islands in Salmonella spp. Infect Immun 64: 5410-5412.
19. Ochman H, Soncini FC, Solomon F, Groisman EA, (1996) Identification of a pathogenicity island required for Salmonella survival in host cells. Proc Natl Acad Sci U S A 93: 7800-7804.
20. Ellermeier JR, Slauch JM, (2007) Adaptation to the host environment: regulation of the SPI1 type III secretion system in Salmonella enterica serovar Typhimurium. Curr Opin Microbiol 10: 24-29.
21. Fass E, Groisman EA, (2009) Control of Salmonella pathogenicity island-2 gene expression. Curr Opin Microbiol 12: 199-204.
22. Lober S, Jackel D, Kaiser N, Hensel M, (2006) Regulation of Salmonella pathogenicity island 2 genes by independent environmental signals. Int J Med Microbiol 296: 435-447.
23. Deiwick J, Nikolaus T, Erdogan S, Hensel M, (1999) Environmental regulation of Salmonella pathogenicity island 2 gene expression. Mol Microbiol 31: 1759-1773.
24. Bajaj V, Lucas RL, Hwang C, Lee CA, (1996) Co-ordinate regulation of Salmonella typhimurium invasion genes by environmental and regulatory factors is mediated by control of hilA expression. Mol Microbiol 22: 703-714.
25. Pizarro-Cerda J, Tedin K, (2004) The bacterial signal molecule, ppGpp, regulates Salmonella virulence gene expression. Mol Microbiol 52: 1827-1844.
26. Thompson A, Rolfe MD, Lucchini S, Schwerk P, Hinton JC, et al. (2006) The bacterial signal molecule, ppGpp, mediates the environmental regulation of both the invasion and intracellular virulence gene programs of Salmonella. J Biol Chem 281: 30112-30121.
27. Chattopadhyay MK, Tabor CW, Tabor H, (2003) Polyamines protect Escherichia coli cells from the toxic effect of oxygen. Proc Natl Acad Sci U S A 100: 2261-2265.
28. Sturgill G, Rather PN, (2004) Evidence that putrescine acts as an extracellular signal required for swarming in Proteus mirabilis. Mol Microbiol 51: 437-446.
29. Wortham BW, Oliveira MA, Fetherston JD, Perry RD, (2010) Polyamines are required for the expression of key Hms proteins important for Yersinia pestis biofilm formation. Environ Microbiol 12: 2034-2047.
30. Gutnick D, Calvo JM, Klopotowski T, Ames BN, (1969) Compounds which serve as the sole source of carbon or nitrogen for Salmonella typhimurium LT-2. J Bacteriol 100: 215-219.
31. Barbagallo M, Di Martino ML, Marcocci L, Pietrangeli P, De CE, et al. (2011) A New Piece of the Shigella Pathogenicity Puzzle: Spermidine Accumulationby Silencing of the speG Gene. PLoS ONE 6 e27226. 10.1371/journal.pone.0027226 [doi];PONE-D-11-12167 [pii].
32. Durand JM, Bjork GR, (2003) Putrescine or a combination of methionine and arginine restores virulence gene expression in a tRNA modification-deficient mutant of Shigella flexneri: a possible role in adaptation of virulence. Mol Microbiol 47 519-527. 3314 [pii].
33. Russo BC, Horzempa J, O'Dee DM, Schmitt DM, Brown MJ, et al. (2011) A Francisella tularensis locus required for spermine responsiveness is necessary for virulence. Infect Immun. IAI.00135-11 [pii];10.1128/IAI.00135-11 [doi].
34. Carlson PE Jr, Horzempa J, O'Dee DM, Robinson CM, Neophytou P, et al. (2009) Global transcriptional response to spermine, a component of the intramacrophage environment, reveals regulation of Francisella gene expression through insertion sequence elements. J Bacteriol 191: 6855-6864.
35. Nasrallah GK, Riveroll AL, Chong A, Murray LE, Lewis PJ, et al. (2011) Legionella pneumophilaRequires Polyamines for Optimal Intracellular Growth. J Bacteriol 193 4346-4360. JB.01506-10 [pii];10.1128/JB.01506-10 [doi].
36. 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.
37. Hautefort I, Thompson A, Eriksson-Ygberg S, Parker ML, Lucchini S, et al. (2008) During infection of epithelial cells Salmonella enterica serovar Typhimurium undergoes a time-dependent transcriptional adaptation that results in simultaneous expression of three type 3 secretion systems. Cell Microbiol 10: 958-984.
38. Igarashi K, Kashiwagi K, (2009) Modulation of cellular function by polyamines. Int J Biochem Cell Biol.
39. Stein MA, Leung KY, Zwick M, Garcia-Del PF, Finlay BB, (1996) Identification of a Salmonella virulence gene required for formation of filamentous structures containing lysosomal membrane glycoproteins within epithelial cells. Mol Microbiol 20: 151-164.
40. Viala JP, Meresse S, Pocachard B, Guilhon AA, Aussel L, et al. (2011) Sensing and adaptation to low pH mediated by inducible amino acid decarboxylases in Salmonella. PLoS ONE 6 e22397. 10.1371/journal.pone.0022397 [doi];PONE-D-11-05545 [pii].
41. Ibarra JA, Knodler LA, Sturdevant DE, Virtaneva K, Carmody AB, et al. (2010) Induction of Salmonella pathogenicity island 1 under different growth conditions can affect Salmonella-host cell interactions in vitro. Microbiology 156: 1120-1133.
42. Hensel M, Shea JE, Raupach B, Monack D, Falkow S, et al. (1997) Functional analysis of ssaJ and the ssaK/U operon, 13 genes encoding components of the type III secretion apparatus of Salmonella Pathogenicity Island 2. Mol Microbiol 24: 155-167.
43. Rytkonen A, Poh J, Garmendia J, Boyle C, Thompson A, et al. (2007) SseL, a Salmonella deubiquitinase required for macrophage killing and virulence. Proc Natl Acad Sci U S A 104: 3502-3507.
44. Guiney DG, Fierer J, (2011) The Role of the spv Genes in Salmonella Pathogenesis. Front Microbiol 2 129. 10.3389/fmicb.2011.00129 [doi].
45. Labrousse A, Chauvet S, Couillault C, Kurz CL, Ewbank JJ, (2000) Caenorhabditis elegans is a model host for Salmonella typhimurium. Curr Biol 10 1543-1545. S0960-9822(00)00833-2 [pii].
46. Aballay A, Yorgey P, Ausubel FM, (2000) Salmonella typhimurium proliferates and establishes a persistent infection in the intestine of Caenorhabditis elegans. Curr Biol 10 1539-1542. S0960-9822(00)00830-7 [pii].
47. Tenor JL, McCormick BA, Ausubel FM, Aballay A, (2004) Caenorhabditis elegans-based screen identifies Salmonella virulence factors required for conserved host-pathogen interactions. Curr Biol 14: 1018-1024.
48. Shea JE, Beuzon CR, Gleeson C, Mundy R, Holden DW, (1999) Influence of the Salmonella typhimurium pathogenicity island 2 type III secretion system on bacterial growth in the mouse. Infect Immun 67: 213-219.
49. Watson KG, Holden DW, (2010) Dynamics of growth and dissemination of Salmonella in vivo. Cell Microbiol 12 1389-1397. CMI1511 [pii];10.1111/j.1462-5822.2010.01511.x [doi].
50. Brown NF, Vallance BA, Coombes BK, Valdez Y, Coburn BA, et al. (2005) Salmonella pathogenicity island 2 is expressed prior to penetrating the intestine. PLoS Pathog 1: e32.
51. Osborne SE, Coombes BK, (2011) Transcriptional priming of Salmonella Pathogenicity Island-2 precedes cellular invasion. PLoS ONE 6 e21648. 10.1371/journal.pone.0021648 [doi];PONE-D-11-06956 [pii].
52. Zhou L, Wang J, Zhang LH, (2007) Modulation of bacterial Type III secretion system by a spermidine transporter dependent signaling pathway. PLoS ONE 2 e1291. 10.1371/journal.pone.0001291 [doi].
53. Igarashi K, Kashiwagi K, (2000) Polyamines: mysterious modulators of cellular functions. Biochem Biophys Res Commun 271: 559-564.
54. Higashi K, Kashiwagi K, Taniguchi S, Terui Y, Yamamoto K, et al. (2006) Enhancement of +1 frameshift by polyamines during translation of polypeptide release factor 2 in Escherichia coli. J Biol Chem 281: 9527-9537.
55. Terui Y, Higashi K, Tabei Y, Tomitori H, Yamamoto K, et al. (2009) Enhancement of the synthesis of RpoE and StpA by polyamines at the level of translation in escherichia coli under heat shock conditions. J Bacteriol 191: 5348-5357.
56. Terui Y, Higashi K, Taniguchi S, Shigemasa A, Nishimura K, et al. (2007) Enhancement of the synthesis of RpoN, Cra, and H-NS by polyamines at the level of translation in Escherichia coli cultured with glucose and glutamate. J Bacteriol 189: 2359-2368.
57. McGinnis MW, Parker ZM, Walter NE, Rutkovsky AC, Cartaya-Marin C, et al. (2009) Spermidine regulates Vibrio cholerae biofilm formation via transport and signaling pathways. FEMS Microbiol Lett 299 166-174. FML1744 [pii];10.1111/j.1574-6968.2009.01744.x [doi].
58. Wallis TS, Paulin SM, Plested JS, Watson PR, Jones PW, (1995) The Salmonella dublin virulence plasmid mediates systemic but not enteric phases of salmonellosis in cattle. Infect Immun 63: 2755-2761.
59. Enomoto M, Stocker BA, (1974) Transduction by phage P1kc in Salmonella typhimurium. Virology 60: 503-514.
60. Datsenko KA, Wanner BL, (2000) One step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97: 6640-6645.
61. Chang AC, Cohen SN, (1978) Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J Bacteriol 134: 1141-1156.
62. Thomsen LE, Slutz SS, Tan MW, Ingmer H, (2006) Caenorhabditis elegans is a model host for Listeria monocytogenes. Appl Environ Microbiol 72: 1700-1701.
63. Schnabel H, Schnabel R, (1990) An Organ-Specific Differentiation Gene, pha-1, from Caenorhabditis elegans. Science 250 686-688. 250/4981/686 [pii];10.1126/science.250.4981.686 [doi].
64. Jelsbak L, Ingmer H, Valihrach L, Cohn MT, Christiansen MH, et al. (2010) The chaperone ClpX stimulates expression of Staphylococcus aureus protein A by Rot dependent and independent pathways. PLoS ONE 5: e12752.
65. Jelsbak L, Hemmingsen L, Donat S, Ohlsen K, Boye K, et al. (2010) Growth phase-dependent regulation of the global virulence regulator Rot in clinical isolates of Staphylococcus aureus. Int J Med Microbiol 300: 229-236.
66. Pfaffl MW, (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.
67. Shah P, Swiatlo E, (2008) A multifaceted role for polyamines in bacterial pathogens. Mol Microbiol 68 4-16. MMI6126 [pii];10.1111/j.1365-2958.2008.06126.x [doi].
68. Watson PR, Paulin SM, Bland AP, Jones PW, Wallis TS, (1995) Characterization of intestinal invasion by Salmonella typhimurium and Salmonella dublin and effect of a mutation in the invH gene. Infect Immun 63: 2743-2754.