Multiplicity of S almonella entry mechanisms, a new paradigm for S almonella pathogenesis

Abstract

The S almonella enterica species includes about 2600 diverse serotypes, most of which cause a wide range of food‐ and water‐borne diseases ranging from self‐limiting gastroenteritis to typhoid fever in both humans and animals. Moreover, some serotypes are restricted to a few animal species, whereas other serotypes are able to infect plants as well as cold‐ and warm‐blooded animals. An essential feature of the pathogenicity of S almonella is its capacity to cross a number of barriers requiring invasion of a large variety of phagocytic and nonphagocytic cells. The aim of this review is to describe the different entry pathways used by S almonella serotypes to enter different nonphagocytic cell types. Until recently, it was accepted that S almonella invasion of eukaryotic cells required only the type III secretion system ( T3SS ) encoded by the S almonella pathogenicity island‐1. However, recent evidence shows that S almonella can cause infection in a T3SS ‐1‐independent manner. Currently, two outer membrane proteins Rck and PagN have been clearly identified as S almonella invasins. As Rck mediates a Z ipper‐like entry mechanism, S almonella is therefore the first bacterium shown to be able to induce both Z ipper and T rigger mechanisms to invade host cells. In addition to these known entry pathways, recent data have shown that unknown entry routes could be used according to the serotype, the host and the cell type considered, inducing either Z ipper‐like or T rigger‐like entry processes. The new paradigm presented here should change our classic view of S almonella pathogenicity. It could also modify our understanding of the mechanisms leading to the different S almonella ‐induced diseases and to S almonella‐ host specificity.

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90. 90.

    Parsons DA, Heffron F. sciS, an icmF homolog in Salmonella enterica serovar Typhimurium, limits intracellular replication and decreases virulence. Infect. Immun. 2005;73:4338-4345.

    Not in our library10.1128/iai.73.7.4338-4345.2005

91. 91.

    Pascopella L, Raupach B, Ghori N, Monack D, Falkow S, Small PL. Host restriction phenotypes of Salmonella Typhi and Salmonella Gallinarum. Infect. Immun. 1995;63:4329-4335.

    Not in our library10.1128/iai.63.11.4329-4335.1995

92. 92.

    Patel JC, Galan JE. Differential activation and function of Rho GTPases during Salmonella-host cell interactions. J. Cell Biol. 2006;175:453-463.

    Not in our library10.1083/jcb.200605144

93. 93.

    Patel JC, Hueffer K, Lam TT, Galan JE. Diversification of a Salmonella virulence protein function by ubiquitin-dependent differential localization. Cell. 2009;137:283-294.

    Not in our library10.1016/j.cell.2009.01.056

94. 94.

    Paulin SM, Watson PR, Benmore AR, Stevens MP, Jones PW, Villarreal-Ramos B, et al. Analysis of Salmonella enterica serotype-host specificity in calves: avirulence of S. enterica serotype Gallinarum correlates with bacterial dissemination from mesenteric lymph nodes and persistence in vivo. Infect. Immun. 2002;70:6788-6797.

    Not in our library10.1128/iai.70.12.6788-6797.2002

95. 95.

    Perrett CA, Jepson MA. Regulation of Salmonella-induced membrane ruffling by SipA differs in strains lacking other effectors. Cell Microbiol. 2009;11:475-487.

    Not in our library10.1111/j.1462-5822.2008.01268.x

96. 96.

    Pezzoli L, Elson R, Little C, Fisher I, Yip H, Peters T, et al. International outbreak of Salmonella Senftenberg in 2007. Euro. Surveill. 2007;12:E070614.3.

    Not in our library10.2807/esw.12.24.03218-en

97. 97.

    Pier GB, Grout M, Zaidi T, Meluleni G, Mueschenborn SS, Banting G, et al. Salmonella Typhi uses CFTR to enter intestinal epithelial cells. Nature. 1998;393:79-82.

    Not in our library10.1038/30006

98. 98.

    Popp D, Yamamoto A, Iwasa M, Nitanai Y, Maeda Y. Single molecule polymerization, annealing and bundling dynamics of SipA induced actin filaments. Cell Motil. Cytoskelet. 2008;65:165-177.

    Not in our library10.1002/cm.20252

99. 99.

    Pullinger GD, Paulin SM, Charleston B, Watson PR, Bowen AJ, Dziva F, et al. Systemic translocation of Salmonella enterica serovar Dublin in cattle occurs predominantly via efferent lymphatics in a cell-free niche and requires type III secretion system 1 (T3SS-1) but not T3SS-2. Infect. Immun. 2007;75:5191-5199.

    Not in our library10.1128/iai.00784-07

100. 100.

     Rabsch W, Andrews HL, Kingsley RA, Prager R, Tschape H, Adams LG, et al. Salmonella enterica serotype Typhimurium and its host-adapted variants. Infect. Immun. 2002;70:2249-2255.

     Not in our library10.1128/iai.70.5.2249-2255.2002

101. 101.

     Radtke AL, Wilson JW, Sarker S, Nickerson CA. Analysis of interactions of Salmonella type three secretion mutants with 3-D intestinal epithelial cells. PLoS ONE. 2010;5:e15750.

     Not in our library10.1371/journal.pone.0015750

102. 102.
     Epidemiology of Escherichia coli O157:H7 Outbreaks, United States, 1982–2002 · 2005

     No notice
103. 103.

     Rolhion N, Barnich N, Claret L, Darfeuille-Michaud A. Strong decrease in invasive ability and outer membrane vesicle release in Crohn's disease-associated adherent-invasive Escherichia coli strain LF82 with the yfgL gene deleted. J. Bacteriol. 2005;187:2286-2296.

     Not in our library10.1128/jb.187.7.2286-2296.2005

104. 104.

     Rosselin M, Virlogeux-Payant I, Roy C, Bottreau E, Sizaret PY, Mijouin L, et al. Rck of Salmonella enterica, subspecies enterica serovar Enteritidis, mediates Zipper-like internalization. Cell Res. 2010;20:647-664.

     Not in our library10.1038/cr.2010.45

105. 105.

     Rosselin M, Abed N, Virlogeux-Payant I, Bottreau E, Sizaret PY, Velge P, et al. Heterogeneity of type III secretion system (T3SS)-1-independent entry mechanisms used by Salmonella Enteritidis to invade different cell types. Microbiology. 2011;157:839-847.

     Not in our library10.1099/mic.0.044941-0

106. 106.

     Rosselin M, Abed N, Namdari F, Virlogeux Payant I, Velge P, Wiedemann A. The different strategies used by Salmonella to invade host cells. Salmonella/Book2. 2012.

     Not in our library

107. 107.

     Rudge SA, Anderson DM, Emr SD. Vacuole size control: regulation of PtdIns(3,5)P2 levels by the vacuole-associated Vac14-Fig 4 complex, a PtdIns(3,5)P2-specific phosphatase. Mol. Biol. Cell. 2004;15:24-36.

     Not in our library10.1091/mbc.e03-05-0297

108. 108.

     Rychlik I, Gregorova D, Hradecka H. Distribution and function of plasmids in Salmonella enterica. Vet. Microbiol. 2006;112:1-10.

     Not in our library10.1016/j.vetmic.2005.10.030

109. 109.

     Rychlik I, Karasova D, Sebkova A, Volf J, Sisak F, Havlickova H, et al. Virulence potential of five major pathogenicity islands (SPI-1 to SPI-5) of Salmonella enterica serovar Enteritidis for chickens. BMC Microbiol. 2009;9:268.

     Not in our library10.1186/1471-2180-9-268

110. 110.

     Salcedo SP, Noursadeghi M, Cohen J, Holden DW. Intracellular replication of Salmonella Typhimurium strains in specific subsets of splenic macrophages in vivo. Cell Microbiol. 2001;3:587-597.

     Not in our library10.1046/j.1462-5822.2001.00137.x

111. 111.

     Santos RL, Zhang S, Tsolis RM, Kingsley RA, Adams LG, Baumler AJ. Animal models of Salmonella infections: enteritis versus typhoid fever. Microbes Infect. 2001;3:1335-1344.

     Not in our library10.1016/s1286-4579(01)01495-2

112. 112.

     Santos RL, Raffatellu M, Bevins CL, Adams LG, Tukel C, Tsolis RM, et al. Life in the inflamed intestine, Salmonella style. Trends Microbiol. 2009;17:498-506.

     Not in our library10.1016/j.tim.2009.08.008

113. 113.

     Schikora A, Virlogeux-Payant I, Bueso E, Garcia AV, Nilau T, Charrier A, et al. Conservation of Salmonella infection mechanisms in plants and animals. PLoS ONE. 2011;6:e24112.

     Not in our library10.1371/journal.pone.0024112

114. 114.

     Schlieker C, Zentgraf H, Dersch P, Mogk A. ClpV, a unique Hsp100/Clp member of pathogenic proteobacteria. Biol. Chem. 2005;386:1115-1127.

     Not in our library10.1515/bc.2005.128

115. 115.
     Burkholderia Type VI Secretion Systems Have Distinct Roles in Eukaryotic and Bacterial Cell Interactions · 2010

     No notice
116. 116.

     Shames SR, Auweter SD, Finlay BB. Co-evolution and exploitation of host cell signaling pathways by bacterial pathogens. Int. J. Biochem. Cell Biol. 2009;41:380-389.

     Not in our library10.1016/j.biocel.2008.08.013

117. 117.

     Shirron N, Yaron S. Active suppression of early immune response in tobacco by the human pathogen Salmonella Typhimurium. PLoS ONE. 2011;6:e18855.

     Not in our library10.1371/journal.pone.0018855

118. 118.

     Shivaprasad HL. Fowl typhoid and pullorum disease. Rev. Sci. Tech. 2000;19:405-424.

     Not in our library10.20506/rst.19.2.1222

119. 119.

     Smith JN, Ahmer BM. Detection of other microbial species by Salmonella: expression of the SdiA regulon. J. Bacteriol. 2003;185:1357-1366.

     Not in our library10.1128/jb.185.4.1357-1366.2003

120. 120.

     Smith JN, Dyszel JL, Soares JA, Ellermeier CD, Altier C, Lawhon SD, et al. SdiA, an N-acylhomoserine lactone receptor, becomes active during the transit of Salmonella enterica through the gastrointestinal tract of turtles. PLoS ONE. 2008;3:e2826.

     Not in our library10.1371/journal.pone.0002826

121. 121.

     van Sorge NM, Zialcita PA, Browne SH, Quach D, Guiney DG, Doran KS. Penetration and activation of brain endothelium by Salmonella enterica serovar Typhimurium. J. Infect. Dis. 2011;203:401-405.

     Not in our library10.1093/infdis/jiq048

122. 122.

     Stecher B, Hapfelmeier S, Muller C, Kremer M, Stallmach T, Hardt WD. Flagella and chemotaxis are required for efficient induction of Salmonella enterica serovar Typhimurium colitis in streptomycin-pretreated mice. Infect. Immun. 2004;72:4138-4150.

     Not in our library10.1128/iai.72.7.4138-4150.2004

123. 123.

     Steele-Mortimer O, Brumell JH, Knodler LA, Meresse S, Lopez A, Finlay BB. 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. 2002;4:43-54.

     Not in our library10.1046/j.1462-5822.2002.00170.x

124. 124.

     Stevens MP, Humphrey TJ, Maskell DJ. Molecular insights into farm animal and zoonotic Salmonella infections. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2009;364:2709-2723.

     Not in our library10.1098/rstb.2009.0094

125. 125.

     Strauss EJ, Ghori N, Falkow S. An Edwardsiella tarda strain containing a mutation in a gene with homology to shlB and hpmB is defective for entry into epithelial cells in culture. Infect. Immun. 1997;65:3924-3932.

     Not in our library10.1128/iai.65.9.3924-3932.1997

126. 126.

     Takeuchi A. Electron microscope studies of experimental Salmonella infection. I. Penetration into the intestinal epithelium by Salmonella typhimurium. Am. J. Pathol. 1967;50:109-136.

     Not in our library

127. 127.

     Uzzau S, Brown DJ, Wallis T, Rubino S, Leori G, Bernard S, et al. Host adapted serotypes of Salmonella enterica. Epidemiol. Infect. 2000;125:229-255.

     Not in our library10.1017/s0950268899004379

128. 128.

     Vazquez-Torres A, Jones-Carson J, Baumler AJ, Falkow S, Valdivia R, Brown W, et al. Extraintestinal dissemination of Salmonella by CD18-expressing phagocytes. Nature. 1999;401:804-808.

     Not in our library10.1038/44593

129. 129.

     Velge P, Cloeckaert A, Barrow P. Emergence of Salmonella epidemics: the problems related to Salmonella enterica serotype Enteritidis and multiple antibiotic resistance in other major serotypes. Vet. Res. 2005;36:267-288.

     Not in our library10.1051/vetres:2005005

130. 130.

     Wagner C, Hensel M. Adhesive mechanisms of Salmonella enterica. Adv. Exp. Med. Biol. 2011;715:17-34.

     Not in our library10.1007/978-94-007-0940-9_2

131. 131.

     Zhou D, Mooseker MS, Galan JE. Role of the S. typhimurium actin-binding protein Sipa in bacterial internalization. Science. 1999;283:2092-2095.

     Not in our library10.1126/science.283.5410.2092

132. 132.

     Zhou D, Chen LM, Hernandez L, Shears SB, Galan JE. A Salmonella inositol polyphosphatase acts in conjunction with other bacterial effectors to promote host cell actin cytoskeleton rearrangements and bacterial internalization. Mol. Microbiol. 2001;39:248-260.

     Not in our library10.1046/j.1365-2958.2001.02230.x

133. 133.

     Zou W, Al-Khaldi SF, Branham WS, Han T, Fuscoe JC, Han J, et al. Microarray analysis of virulence gene profiles in Salmonella serovars from food/food animal environment. J. Infect. Dev. Ctries. 2011;5:94-105.

     Not in our library10.3855/jidc.1396

Cited by papers we hold 2

• SipD and IpaD induce a cross-protection against Shigella and Salmonella infections. · 2020
  Not checked
• Nanoscale Bacteria‐Enabled Autonomous Drug Delivery System (NanoBEADS) Enhances Intratumoral Transport of Nanomedicine · 2018
  No notice

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