The FUN of identifying gene function in bacterial pathogens; insights from Salmonella functional genomics

Current Opinion in Microbiology

Volumn 16, Issue 5, 2013, Pages 643-651

  Hammarlöf, Disa L ^a   Canals, Rocío ^a   Hinton, Jay CD ^a  

^a UNIVERSITY OF LIVERPOOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; PEPTIDOGLYCAN; VIRULENCE FACTOR;

ANTIBIOTIC RESISTANCE; BACTERIAL CELL WALL; BACTERIAL GENE; BACTERIAL GENETICS; BACTERIAL MEMBRANE; BACTERIAL METABOLISM; BACTERIAL VIRULENCE; BORRELIA BURGDORFERI; DETOXIFICATION; EPITHELIUM CELL; ESCHERICHIA COLI; FUN GENE; FUNCTIONAL GENOMICS; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE IDENTIFICATION; GENE MUTATION; HOST PATHOGEN INTERACTION; MUTAGENESIS; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PATHOGENICITY ISLAND; REGULATOR GENE; REVIEW; SALMONELLA; SALMONELLA ENTERITIDIS; SALMONELLA TYPHI; SALMONELLA TYPHIMURIUM; SALMONELLOSIS; STREPTOCOCCUS PNEUMONIAE; TRANSCRIPTOMICS; TRANSPOSON;

BACTERIA (MICROORGANISMS); MAMMALIA; SALMONELLA;

DNA MUTATIONAL ANALYSIS; GENE EXPRESSION PROFILING; GENES, BACTERIAL; GENOMICS; MICROBIOLOGICAL TECHNIQUES; SALMONELLA;

EID: 84887621185     PISSN: 13695274     EISSN: 18790364     Source Type: Journal    
DOI: 10.1016/j.mib.2013.07.009     Document Type: Review

References (95)

1. Feasey N.A., Dougan G., Kingsley R.A., Heyderman R.S., Gordon M.A. Invasive non-typhoidal Salmonella disease: an emerging and neglected tropical disease in Africa. Lancet 2012, 379:2489-2499.
2. van der Heijden J., Finlay B.B. Type III effector-mediated processes in Salmonella infection. Fut Microbiol 2012, 7:685-703.
3. Hébrard M., Kröger C., Sivasankaran S.K., Händler K., Hinton J.C. The challenge of relating gene expression to the virulence of Salmonella enterica serovar Typhimurium. Curr Opin Biotechnol 2011, 22:200-210.
4. Eriksson S., Lucchini S., Thompson A., Rhen M., Hinton J.C. Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol Microbiol 2003, 47:103-118.
5. Hinton J.C. The Escherichia coli genome sequence: the end of an era or the start of the FUN?. Mol Microbiol 1997, 26:417-422.
6. Hautefort I., Thompson A., Eriksson-Ygberg S., Parker M.L., Lucchini S., Danino V., Bongaerts R.J., Ahmad N., Rhen M., Hinton J.C. 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 2008, 10:958-984.
7. Wright J.A., Totemeyer S.S., Hautefort I., Appia-Ayme C., Alston M., Danino V., Paterson G.K., Mastroeni P., Menager N., Rolfe M., et al. Multiple redundant stress resistance mechanisms are induced in Salmonella enterica serovar Typhimurium in response to alteration of the intracellular environment via TLR4 signalling. Microbiology 2009, 155:2919-2929.
8. Nunez-Hernandez C., Tierrez A., Ortega A.D., Pucciarelli M.G., Godoy M., Eisman B., Casadesus J., Garcia-del Portillo F. Genome expression analysis of nonproliferating intracellular Salmonella enterica serovar Typhimurium unravels an acid pH-dependent PhoP-PhoQ response essential for dormancy. Infect Immun 2013, 81:154-165.
9. Moreira C.G., Herrera C.M., Needham B.D., Parker C.T., Libby S.J., Fang F.C., Trent M.S., Sperandio V. Virulence and stress-related periplasmic protein (VisP) in bacterial/host associations. Proc Natl Acad Sci U S A 2013, 110:1470-1475.
10. Kawano M., Manabe T., Kawasaki K. Salmonella enterica serovar Typhimurium lipopolysaccharide deacylation enhances its intracellular growth within macrophages. FEBS Lett 2010, 584:207-212.
11. Kawasaki K., Teramoto M., Tatsui R., Amamoto S. Lipid A 3'-O-deacylation by Salmonella outer membrane enzyme LpxR modulates the ability of lipid A to stimulate Toll-like receptor 4. Biochem Biophys Res Commun 2012, 428:343-347.
12. Chaudhuri R.R., Morgan E., Peters S.E., Pleasance S.J., Hudson D.L., Davies H.M., Wang J., van Diemen P.M., Buckley A.M., Bowen A.J., et al. Comprehensive assignment of roles for Salmonella Typhimurium genes in intestinal colonization of food-producing animals. PLoS Genet 2013, 9:e1003456.
13. Boneca I.G. The role of peptidoglycan in pathogenesis. Curr Opin Microbiol 2005, 8:46-53.
14. Haneda T., Ishii Y., Danbara H., Okada N. Genome-wide identification of novel genomic islands that contribute to Salmonella virulence in mouse systemic infection. FEMS Microbiol Lett 2009, 297:241-249.
15. Shi L., Adkins J.N., Coleman J.R., Schepmoes A.A., Dohnkova A., Mottaz H.M., Norbeck A.D., Purvine S.O., Manes N.P., Smallwood H.S., et al. 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 2006, 281:29131-29140.
16. Yu X.J., McGourty K., Liu M., Unsworth K.E., Holden D.W. pH sensing by intracellular Salmonella induces effector translocation. Science 2010, 328:1040-1043.
17. Seputiene V., Suziedelis K., Normark S., Melefors O., Suziedeliene E. Transcriptional analysis of the acid-inducible asr gene in enterobacteria. Res Microbiol 2004, 155:535-542.
18. Allam U.S., Krishna M.G., Sen M., Thomas R., Lahiri A., Gnanadhas D.P., Chakravortty D. Acidic pH induced STM1485 gene is essential for intracellular replication of Salmonella. Virulence 2012, 3:122-135.
19. Gilberthorpe N.J., Lee M.E., Stevanin T.M., Read R.C., Poole R.K. NsrR: a key regulator circumventing Salmonella enterica serovar Typhimurium oxidative and nitrosative stress in vitro and in IFN-gamma-stimulated J774.2 macrophages. Microbiology 2007, 153:1756-1771.
20. Karlinsey J.E., Bang I.S., Becker L.A., Frawley E.R., Porwollik S., Robbins H.F., Thomas V.C., Urbano R., McClelland M., Fang F.C. The NsrR regulon in nitrosative stress resistance of Salmonella enterica serovar Typhimurium. Mol Microbiol 2012, 85:1179-1193.
21. Eriksson S., Björkman J., Borg S., Syk A., Pettersson S., Andersson D.I., Rhen M. Salmonella Typhimurium mutants that downregulate phagocyte nitric oxide production. Cell Microbiol 2000, 2:239-250.
22. Prior K., Hautefort I., Hinton J.C., Richardson D.J., Rowley G. All stressed out, Salmonella pathogenesis and reactive nitrogen species. Adv Microb Physiol 2009, 56:1-28.
23. Wu H., Jones R.M., Neish A.S. The Salmonella effector AvrA mediates bacterial intracellular survival during infection in vivo. Cell Microbiol 2012, 14:28-39.
24. Ellermeier C.D., Ellermeier J.R., Slauch J.M. HilD, HilC and RtsA constitute a feed forward loop that controls expression of the SPI1 type three secretion system regulator hilA in Salmonella enterica serovar Typhimurium. Mol Microbiol 2005, 57:691-705.
25. Ismail T.M., Hart C.A., McLennan A.G. Regulation of dinucleoside polyphosphate pools by the YgdP and ApaH hydrolases is essential for the ability of Salmonella enterica serovar Typhimurium to invade cultured mammalian cells. J Biol Chem 2003, 278:32602-32607.
26. Kim J.S., Eom J.S., Jang J.I., Kim H.G., Seo D.W., Bang I.S., Bang S.H., Lee I.S., Park Y.K. Role of Salmonella pathogenicity Island 1 protein IacP in Salmonella enterica serovar Typhimurium pathogenesis. Infect Immun 2011, 79:1440-1450.
27. Eom J.S., Kim J.S., Jang J.I., Kim H.G., Bang I.S., Park Y.K. Effect of iacP mutation on flagellar phase variation in Salmonella enterica serovar Typhimurium strain UK-1. J Bacteriol 2012, 194:4332-4341.
28. Figueira R., Watson K.G., Holden D.W., Helaine S. Identification of Salmonella pathogenicity island-2 type III secretion system effectors involved in intramacrophage replication of S. enterica serovar Typhimurium: implications for rational vaccine design. MBio 2013, 4.
29. Odendall C., Rolhion N., Förster A., Poh J., Lamont D.J., Liu M., Freemont P.S., Catling A.D., Holden D.W. The Salmonella kinase SteC targets the MAP kinase MEK to regulate the host actin cytoskeleton. Cell Host Microbe 2012, 12:657-668.
30. Poh J., Odendall C., Spanos A., Boyle C., Liu M., Freemont P., Holden D.W. SteC is a Salmonella kinase required for SPI-2-dependent F-actin remodelling. Cell Microbiol 2008, 10:20-30.
31. Baisón-Olmo F., Cardenal-Muñoz E., Ramos-Morales F. PipB2 is a substrate of the Salmonella pathogenicity island 1-encoded type III secretion system. Biochem Biophys Res Commun 2012, 423:240-246.
32. Rytkönen A., Poh J., Garmendia J., Boyle C., Thompson A., Liu M., Freemont P., Hinton J.C., Holden D.W. SseL, a Salmonella deubiquitinase required for macrophage killing and virulence. Proc Natl Acad Sci U S A 2007, 104:3502-3507.
33. Mesquita F.S., Thomas M., Sachse M., Santos A.J., Figueira R., Holden D.W. The Salmonella deubiquitinase SseL inhibits selective autophagy of cytosolic aggregates. PLoS Pathog 2012, 8:e1002743.
34. Eisenreich W., Dandekar T., Heesemann J., Goebel W. Carbon metabolism of intracellular bacterial pathogens and possible links to virulence. Nat Rev Microbiol 2010, 8:401-412.
35. Bowden S.D., Rowley G., Hinton J.C., Thompson A. Glucose and glycolysis are required for the successful infection of macrophages and mice by Salmonella enterica serovar Typhimurium. Infect Immun 2009, 77:3117-3126.
36. Steeb B., Claudi B., Burton N.A., Tienz P., Schmidt A., Farhan H., Mazé A., Bumann D. Parallel exploitation of diverse host nutrients enhances Salmonella virulence. PLoS Pathog 2013, 9:e1003301.
37. DebRoy S., Dao J., Soderberg M., Rossier O., Cianciotto N.P. Legionella pneumophila type II secretome reveals unique exoproteins and a chitinase that promotes bacterial persistence in the lung. Proc Natl Acad Sci U S A 2006, 103:19146-19151.
38. Toledo-Arana A., Dussurget O., Nikitas G., Sesto N., Guet-Revillet H., Balestrino D., Loh E., Gripenland J., Tiensuu T., Vaitkevicius K., et al. The Listeria transcriptional landscape from saprophytism to virulence. Nature 2009, 459:950-956.
39. Barquist L., Boinett C.J., Cain A.K. Approaches to querying bacterial genomes with transposon-insertion sequencing. RNA Biol 2013, 10.
40. Tamayo R., Choudhury B., Septer A., Merighi M., Carlson R., Gunn J.S. Identification of cptA, a PmrA-regulated locus required for phosphoethanolamine modification of the Salmonella enterica serovar Typhimurium lipopolysaccharide core. J Bacteriol 2005, 187:3391-3399.
41. Reynolds C.M., Ribeiro A.A., McGrath S.C., Cotter R.J., Raetz C.R., Trent M.S. An outer membrane enzyme encoded by Salmonella Typhimurium lpxR that removes the 3'-acyloxyacyl moiety of lipid A. J Biol Chem 2006, 281:21974-21987.
42. Lee H., Hsu F.F., Turk J., Groisman E.A. The PmrA-regulated pmrC gene mediates phosphoethanolamine modification of lipid A and polymyxin resistance in Salmonella enterica. J Bacteriol 2004, 186:4124-4133.
43. Shi Y., Latifi T., Cromie M.J., Groisman E.A. Transcriptional control of the antimicrobial peptide resistance ugtL gene by the Salmonella PhoP and SlyA regulatory proteins. J Biol Chem 2004, 279:38618-38625.
44. Shi Y., Cromie M.J., Hsu F.F., Turk J., Groisman E.A. PhoP-regulated Salmonella resistance to the antimicrobial peptides magainin 2 and polymyxin B. Mol Microbiol 2004, 53:229-241.
45. Navarre W.W., Halsey T.A., Walthers D., Frye J., McClelland M., Potter J.L., Kenney L.J., Gunn J.S., Fang F.C., Libby S.J. Co-regulation of Salmonella enterica genes required for virulence and resistance to antimicrobial peptides by SlyA and PhoP/PhoQ. Mol Microbiol 2005, 56:492-508.
46. Wang Q., Mariconda S., Suzuki A., McClelland M., Harshey R.M. Uncovering a large set of genes that affect surface motility in Salmonella enterica serovar Typhimurium. J Bacteriol 2006, 188:7981-7984.
47. Frye J., Karlinsey J.E., Felise H.R., Marzolf B., Dowidar N., McClelland M., Hughes K.T. Identification of new flagellar genes of Salmonella enterica serovar Typhimurium. J Bacteriol 2006, 188:2233-2243.
48. Collier-Hyams L.S., Zeng H., Sun J., Tomlinson A.D., Bao Z.Q., Chen H., Madara J.L., Orth K., Neish A.S. Cutting edge: Salmonella AvrA effector inhibits the key proinflammatory, anti-apoptotic NF-kappa B pathway. J Immunol 2002, 169:2846-2850.
49. Du F., Galán J.E. Selective inhibition of type III secretion activated signaling by the Salmonella effector AvrA. PLoS Pathog 2009, 5:e1000595.
50. Lahiri A., Das P., Chakravortty D. The LysR-type transcriptional regulator Hrg counteracts phagocyte oxidative burst and imparts survival advantage to Salmonella enterica serovar Typhimurium. Microbiology 2008, 154:2837-2846.
51. Nishino K., Latifi T., Groisman E.A. Virulence and drug resistance roles of multidrug efflux systems of Salmonella enterica serovar Typhimurium. Mol Microbiol 2006, 59:126-141.
52. Eswarappa S.M., Panguluri K.K., Hensel M., Chakravortty D. The yejABEF operon of Salmonella confers resistance to antimicrobial peptides and contributes to its virulence. Microbiology 2008, 154:666-678.
53. White A.P., Weljie A.M., Apel D., Zhang P., Shaykhutdinov R., Vogel H.J., Surette M.G. A global metabolic shift is linked to Salmonella multicellular development. PLoS ONE 2010, 5:e11814.
54. Navarre W.W., Zou S.B., Roy H., Xie J.L., Savchenko A., Singer A., Edvokimova E., Prost L.R., Kumar R., Ibba M., et al. PoxA, yjeK, and elongation factor P coordinately modulate virulence and drug resistance in Salmonella enterica. Mol Cell 2010, 39:209-221.
55. Ellermeier C.D., Slauch J.M. RtsA and RtsB coordinately regulate expression of the invasion and flagellar genes in Salmonella enterica serovar Typhimurium. J Bacteriol 2003, 185:5096-5108.
56. Chaudhuri R.R., Peters S.E., Pleasance S.J., Northen H., Willers C., Paterson G.K., Cone D.B., Allen A.G., Owen P.J., Shalom G., et al. Comprehensive identification of Salmonella enterica serovar Typhimurium genes required for infection of BALB/c mice. PLoS Pathog 2009, 5:e1000529.
57. Ahmad I., Lamprokostopoulou A., Le Guyon S., Streck E., Barthel M., Peters V., Hardt W.D., Römling U. Complex c-di-GMP signaling networks mediate transition between virulence properties and biofilm formation in Salmonella enterica serovar Typhimurium. PLoS ONE 2011, 6:e28351.
58. Knodler L.A., Vallance B.A., Hensel M., Jäckel D., Finlay B.B., Steele-Mortimer O. Salmonella type III effectors PipB and PipB2 are targeted to detergent-resistant microdomains on internal host cell membranes. Mol Microbiol 2003, 49:685-704.
59. Henry T., Couillault C., Rockenfeller P., Boucrot E., Dumont A., Schroeder N., Hermant A., Knodler L.A., Lecine P., Steele-Mortimer O., et al. The Salmonella effector protein PipB2 is a linker for kinesin-1. Proc Natl Acad Sci U S A 2006, 103:13497-13502.
60. Lawley T.D., Chan K., Thompson L.J., Kim C.C., Govoni G.R., Monack D.M. Genome-wide screen for Salmonella genes required for long-term systemic infection of the mouse. PLoS Pathog 2006, 2:e11.
61. Morgan E., Campbell J.D., Rowe S.C., Bispham J., Stevens M.P., Bowen A.J., Barrow P.A., Maskell D.J., Wallis T.S. Identification of host-specific colonization factors of Salmonella enterica serovar Typhimurium. Mol Microbiol 2004, 54:994-1010.
62. Gerlach R.G., Jäckel D., Stecher B., Wagner C., Lupas A., Hardt W.D., Hensel M. Salmonella pathogenicity Island 4 encodes a giant non-fimbrial adhesin and the cognate type 1 secretion system. Cell Microbiol 2007, 9:1834-1850.
63. Brumell J.H., Kujat-Choy S., Brown N.F., Vallance B.A., Knodler L.A., Finlay B.B. SopD2 is a novel type III secreted effector of Salmonella Typhimurium that targets late endocytic compartments upon delivery into host cells. Traffic 2003, 4:36-48.
64. Cooper C.A., Zhang K., Andres S.N., Fang Y., Kaniuk N.A., Hannemann M., Brumell J.H., Foster L.J., Junop M.S., Coombes B.K. Structural and biochemical characterization of SrcA, a multi-cargo type III secretion chaperone in Salmonella required for pathogenic association with a host. PLoS Pathog 2010, 6:e1000751.
65. Kujat Choy S.L., Boyle E.C., Gal-Mor O., Goode D.L., Valdez Y., Vallance B.A., Finlay B.B. SseK1 and SseK2 are novel translocated proteins of Salmonella enterica serovar Typhimurium. Infect Immun 2004, 72:5115-5125.
66. Coombes B.K., Lowden M.J., Bishop J.L., Wickham M.E., Brown N.F., Duong N., Osborne S., Gal-Mor O., Finlay B.B. SseL is a Salmonella-specific translocated effector integrated into the SsrB-controlled Salmonella pathogenicity island 2 type III secretion system. Infect Immun 2007, 75:574-580.
67. Geddes K., Worley M., Niemann G., Heffron F. Identification of new secreted effectors in Salmonella enterica serovar Typhimurium. Infect Immun 2005, 73:6260-6271.
68. Tomljenovic-Berube A.M., Henriksbo B., Porwollik S., Cooper C.A., Tuinema B.R., McClelland M., Coombes B.K. Mapping and regulation of genes within SPI-12 that contribute to in vivo fitness of Salmonella Typhimurium. Infect Immun 2013, 81:2394-2404.
69. Arrach N., Cheng P., Zhao M., Santiviago C.A., Hoffman R.M., McClelland M. High-throughput screening for Salmonella avirulent mutants that retain targeting of solid tumors. Cancer Res 2010, 70:2165-2170.
70. Shah D.H., Lee M.J., Park J.H., Lee J.H., Eo S.K., Kwon J.T., Chae J.S. Identification of Salmonella gallinarum virulence genes in a chicken infection model using PCR-based signature-tagged mutagenesis. Microbiology 2005, 151:3957-3968.
71. Santiviago C.A., Reynolds M.M., Porwollik S., Choi S.H., Long F., Andrews-Polymenis H.L., McClelland M. Analysis of pools of targeted Salmonella deletion mutants identifies novel genes affecting fitness during competitive infection in mice. PLoS Pathog 2009, 5:e1000477.
72. Larsen T., Petersen B.O., Storgaard B.G., Duus J., Palcic M.M., Leisner J.J. Characterization of a novel Salmonella Typhimurium chitinase which hydrolyzes chitin, chitooligosaccharides and an N-acetyllactosamine conjugate. Glycobiology 2011, 21:426-436.
73. Harvey P.C., Watson M., Hulme S., Jones M.A., Lovell M., Berchieri A., Young J., Bumstead N., Barrow P. Salmonella enterica serovar Typhimurium colonizing the lumen of the chicken intestine grows slowly and upregulates a unique set of virulence and metabolism genes. Infect Immun 2011, 79:4105-4121.
74. Osborne S.E., Tuinema B.R., Mok M.C., Lau P.S., Bui N.K., Tomljenovic-Berube A.M., Vollmer W., Zhang K., Junop M., Coombes B.K. Characterization of DalS, an ATP-binding cassette transporter for d-alanine, and its role in pathogenesis in Salmonella enterica. J Biol Chem 2012, 287:15242-15250.
75. Becker D., Selbach M., Rollenhagen C., Ballmaier M., Meyer T.F., Mann M., Bumann D. Robust Salmonella metabolism limits possibilities for new antimicrobials. Nature 2006, 440:303-307.
76. Campoy S., Jara M., Busquets N., Pérez De Rozas A.M., Badiola I., Barbé J. Role of the high-affinity zinc uptake znuABC system in Salmonella enterica serovar Typhimurium virulence. Infect Immun 2002, 70:4721-4725.
77. Troy E.B., Lin T., Gao L., Lazinski D.W., Camilli A., Norris S.J., Hu L. Understanding barriers to Borrelia burgdorferi dissemination during infection using massively parallel sequencing. Infect Immun 2013, 81:2347-2357.
78. Narasimhan S., Caimano M.J., Liang F.T., Santiago F., Laskowski M., Philipp M.T., Pachner A.R., Radolf J.D., Fikrig E., Camaino M.J. Borrelia burgdorferi transcriptome in the central nervous system of non-human primates. Proc Natl Acad Sci U S A 2003, 100:15953-15958.
79. Eckert S.E., Dziva F., Chaudhuri R.R., Langridge G.C., Turner D.J., Pickard D.J., Maskell D.J., Thomson N.R., Stevens M.P. Retrospective application of transposon-directed insertion site sequencing to a library of signature-tagged mini-Tn5Km2 mutants of Escherichia coli O157:H7 screened in cattle. J Bacteriol 2011, 193:1771-1776.
80. Poirier K., Faucher S.P., Béland M., Brousseau R., Gannon V., Martin C., Harel J., Daigle F. Escherichia coli O157:H7 survives within human macrophages: global gene expression profile and involvement of the Shiga toxins. Infect Immun 2008, 76:4814-4822.
81. Sassetti C.M., Rubin E.J. Genetic requirements for mycobacterial survival during infection. Proc Natl Acad Sci U S A 2003, 100:12989-12994.
82. Rengarajan J., Bloom B.R., Rubin E.J. Genome-wide requirements for Mycobacterium tuberculosis adaptation and survival in macrophages. Proc Natl Acad Sci U S A 2005, 102:8327-8332.
83. Griffin J.E., Gawronski J.D., Dejesus M.A., Ioerger T.R., Akerley B.J., Sassetti C.M. High-resolution phenotypic profiling defines genes essential for mycobacterial growth and cholesterol catabolism. PLoS Pathog 2011, 7:e1002251.
84. Zhang Y.J., Ioerger T.R., Huttenhower C., Long J.E., Sassetti C.M., Sacchettini J.C., Rubin E.J. Global assessment of genomic regions required for growth in Mycobacterium tuberculosis. PLoS Pathog 2012, 8:e1002946.
85. Tailleux L., Waddell S.J., Pelizzola M., Mortellaro A., Withers M., Tanne A., Castagnoli P.R., Gicquel B., Stoker N.G., Butcher P.D., et al. Probing host pathogen cross-talk by transcriptional profiling of both Mycobacterium tuberculosis and infected human dendritic cells and macrophages. PLoS ONE 2008, 3:e1403.
86. Rohde K.H., Abramovitch R.B., Russell D.G. Mycobacterium tuberculosis invasion of macrophages: linking bacterial gene expression to environmental cues. Cell Host Microbe 2007, 2:352-364.
87. Rachman H., Strong M., Ulrichs T., Grode L., Schuchhardt J., Mollenkopf H., Kosmiadi G.A., Eisenberg D., Kaufmann S.H. Unique transcriptome signature of Mycobacterium tuberculosis in pulmonary tuberculosis. Infect Immun 2006, 74:1233-1242.
88. Silva C.A., Blondel C.J., Quezada C.P., Porwollik S., Andrews-Polymenis H.L., Toro C.S., Zaldívar M., Contreras I., McClelland M., Santiviago C.A. Infection of mice by Salmonella enterica serovar Enteritidis involves additional genes that are absent in the genome of serovar Typhimurium. Infect Immun 2012, 80:839-849.
89. Ge S., Danino V., He Q., Hinton J.C., Granfors K. Microarray analysis of response of Salmonella during infection of HLA-B27-transfected human macrophage-like U937 cells. BMC Genomics 2010, 11:456.
90. Dhawi A.A., Elazomi A., Jones M.A., Lovell M.A., Li H., Emes R.D., Barrow P.A. Adaptation to the chicken intestine in Salmonella Enteritidis PT4 studied by transcriptional analysis. Vet Microbiol 2011, 153:198-204.
91. Sabbagh S.C., Lepage C., McClelland M., Daigle F. Selection of Salmonella enterica serovar Typhi genes involved during interaction with human macrophages by screening of a transposon mutant library. PLoS ONE 2012, 7:e36643.
92. Faucher S.P., Porwollik S., Dozois C.M., McClelland M., Daigle F. Transcriptome of Salmonella enterica serovar Typhi within macrophages revealed through the selective capture of transcribed sequences. Proc Natl Acad Sci U S A 2006, 103:1906-1911.
93. Chan K., Kim C.C., Falkow S. Microarray-based detection of Salmonella enterica serovar Typhimurium transposon mutants that cannot survive in macrophages and mice. Infect Immun 2005, 73:5438-5449.
94. van Opijnen T., Camilli A. A fine scale phenotype-genotype virulence map of a bacterial pathogen. Genome Res 2012, 22:2541-2551.
95. Orihuela C.J., Radin J.N., Sublett J.E., Gao G., Kaushal D., Tuomanen E.I. Microarray analysis of pneumococcal gene expression during invasive disease. Infect Immun 2004, 72:5582-5596.