Chapter 3 : Metabolic Adaptations of Intracellullar Bacterial Pathogens and their Mammalian Host Cells during Infection (“Pathometabolism”)

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Metabolic Adaptations of Intracellullar Bacterial Pathogens and their Mammalian Host Cells during Infection (“Pathometabolism”), Page 1 of 2

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Metabolic adaptation reactions are common when prokaryotes interact with eukaryotic cells, especially when the bacteria are internalized by these host cells. Such adaptations lead to significant changes in the metabolism of both partners. While the final outcome may be sometimes beneficial (e.g., in case of insect endosymbiosis) or (mainly) neutral for the interacting partners (e.g., microbiota and their hosts) ( ), it is usually detrimental in infections of mammalian cells by intracellular bacterial pathogens. In this encounter, a host cell-defense program is initiated, including antimicrobial metabolic reactions aimed to damage the invading pathogen and/or to withdraw essential nutrients, while the intracellular pathogen tries to deprive nutrients from the host cell and to counteract the antimicrobial reactions, resulting in damaging of the host cell. Our knowledge of the metabolic adaptation processes occurring during this liaison and the link between these metabolic changes and the pathogenicity is still rather fragmentary. For these complex metabolic interactions, we coin the term “pathometabolism”. Studies of pathometabolism are not only central for a deeper understanding of bacterial infections caused by intracellular bacterial pathogens, but may also provide promising bacterial and host cell targets for the development of novel antimicrobial therapeutic measures.

Citation: Eisenreich W, Heesemann J, Rudel T, Goebel W. 2015. Metabolic Adaptations of Intracellullar Bacterial Pathogens and their Mammalian Host Cells during Infection (“Pathometabolism”), p 27-58. In Conway T, Cohen P (ed), Metabolism and Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MBP-0002-2014
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Figure 1

Metabolic potential of intracellular bacterial pathogens replicating in the cytosol of host cells. (a) , (b) , and (c) . Solid arrows indicate reversible (double-headed arrows) and essentially irreversible (single-headed arrows) reactions of glycolysis and gluconeogenesis (GL/GN), red arrows), pentose phosphate pathway (PPP, blue arrows), Entner-Doudoroff pathway (ED, orange arrows), the tricarboxylic acid cycle (TCA). The irreversible reactions involved in GN are marked by dotted-framed boxes: fbp for phosphofructo-1,6-bisphosphatase, pps for PEP synthase, and pckA for PEP carboxykinase. Broken black arrows depict anaplerotic reactions: GS for glyoxylate shunt, pycA for pyruvate carboxylase, ppc for PEP carboxylase; pckA for PEP carboxykinase, and maeA (sfcA) for malate enzyme. Yellow boxes and arrows mark major carbon and energy substrates and black-framed boxes mark the biosynthesis of amino acids, vitamins, nucleotides, cell envelope components, and fatty acids/lipids as well as the major sites of ATP production. The major sites for the generation of NADH/H, NADPH/H and FADH are also shown.

Citation: Eisenreich W, Heesemann J, Rudel T, Goebel W. 2015. Metabolic Adaptations of Intracellullar Bacterial Pathogens and their Mammalian Host Cells during Infection (“Pathometabolism”), p 27-58. In Conway T, Cohen P (ed), Metabolism and Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MBP-0002-2014
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Figure 2

Metabolic potential of intracellular bacterial pathogens replicating in specialized vacuoles of the host cells. (a) , (b) L, and (c) . See legend of Fig 1 for further explanations and abbreviations.

Citation: Eisenreich W, Heesemann J, Rudel T, Goebel W. 2015. Metabolic Adaptations of Intracellullar Bacterial Pathogens and their Mammalian Host Cells during Infection (“Pathometabolism”), p 27-58. In Conway T, Cohen P (ed), Metabolism and Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MBP-0002-2014
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Figure 3

Carbon metabolism and its regulation in mammalian cells. (a) Major carbon sources and their transporters are indicated by yellow boxes and arrows. Main catabolic and anabolic pathways, including glycolysis (GL, red solid arrows) with lactose formation (red broken arrows), pentose-phosphate pathway (PPP, blue arrows) in the cyctosol, TCA cycle in the mitochondria and associated cytosolic reactions (black arrows), and glutaminolysis (purple arrows); catabolic breakdown of amino acids and fatty acids are indicated by dotted arrows. The reactions indicated by the green arrows are two anaplerotic reactions (catalysed by PCK and PYC). The starting points for the biosynthesis of the “non-essential” amino acids, nucleotides and fatty acids/lipids are schematically indicated by broken arrows. (b) Regulation of glucose uptake, glycolysis and pentose-phosphate pathway and (c) of the TCA cycle, glutaminolysis, aerobic respiration, and lactate production by general transcription factors, tumor suppressors, and oncogenes. Activation of the target enzymes (yellow boxes) are shown by green pointed arrows and inhibition by the red symbol. Explanations and abbreviations: Fru-2,6P: fructose 2,6-bisphosphate, the formation of which is catalysed by the fructokinase 2 (PFK2); Fru-2,6P activates fructokinase 1(PFK1); ACL: cytosolic ATP-dependent citrate lyase; ICD-2: cytosolic NADP-dependent isocitrate dehydrogenase; ME: cytosolic malate dehydrogenase (malic enzyme); GLS: glutaminase; HIF-1: hypoxia-inducible factor1; p53: tumor suppressor protein 53 encoded by the gene TP53; TIGAR: TP53-inducible glycolysis and apoptosis regulator; PTEN: phosphatase and tensin homolog; mTORC1: mammalian target of rapamycin complex 1; PI3K/Akt: phosphoinositide-dependent kinase-1/protein kinase B. For further details regarding the complex regulation circuit, see ( ) and further references cited there.

Citation: Eisenreich W, Heesemann J, Rudel T, Goebel W. 2015. Metabolic Adaptations of Intracellullar Bacterial Pathogens and their Mammalian Host Cells during Infection (“Pathometabolism”), p 27-58. In Conway T, Cohen P (ed), Metabolism and Bacterial Pathogenesis. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.MBP-0002-2014
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1. Lupp C,, Robertson ML,, Wickham ME,, Sekirov I,, Champion OL,, Gaynor EC,, Finlay BB . 2007. Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae. Cell Host Microbe 2 : 119 129.[PubMed] [CrossRef]
2. Stecher B,, Robbiani R,, Walker AW,, Westendorf AM,, Barthel M,, Kremer M,, Chaffron S,, Macpherson AJ,, Buer J,, Parkhill J,, Dougan G,, von Mering C,, Hardt WD . 2007. Salmonella enterica serovar typhimurium exploits inflammation to compete with the intestinal microbiota. PLoS Biol 5 : 2177 2189.[PubMed] [CrossRef]
3. Chaston J,, Goodrich-Blair H . 2010. Common trends in mutualism revealed by model associations between invertebrates and bacteria. FEMS Microbiol Rev 34 : 41 58.[PubMed] [CrossRef]
4. Omsland A,, Cockrell DC,, Howe D,, Fischer ER,, Virtaneva K,, Sturdevant DE,, Porcella SF,, Heinzen RA . 2009. Host cell-free growth of the Q fever bacterium Coxiella burnetii . Proc Natl Acad Sci U S A 106 : 4430 4434.[PubMed] [CrossRef]
5. Omsland A,, Sager J,, Nair V,, Sturdevant DE,, Hackstadt T . 2012. Developmental stage-specific metabolic and transcriptional activity of Chlamydia trachomatis in an axenic medium. Proc Natl Acad Sci U S A 109 : 19781 19785.[PubMed] [CrossRef]
6. Méresse S,, Steele-Mortimer O,, Moreno E,, Desjardins M,, Finlay B,, Gorvel JP . 1999. Controlling the maturation of pathogen-containing vacuoles: a matter of life and death. Nat Cell Biol 1 : E183 E188.[PubMed]
7. Hackstadt T . 1998. The diverse habitats of obligate intracellular parasites. Curr Opin Microbiol 1 : 82 87.[PubMed] [CrossRef]
8. Beatty WL . 2008. Late endocytic multivesicular bodies intersect the chlamydial inclusion in the absence of CD63. Infect Immun 76 : 2872 2881.[PubMed] [CrossRef]
9. Kerr MC,, Teasdale RD . 2009. Defining macropinocytosis. Traffic 10 : 364 371.[PubMed] [CrossRef]
10. Ma B,, Xiang Y,, An L . 2011. Structural bases of physiological functions and roles of the vacuolar H(+)-ATPase. Cell Signal 23 : 1244 1256.[PubMed] [CrossRef]
11. Lim JP,, Gleeson PA . 2011. Macropinocytosis: an endocytic pathway for internalising large gulps. Immunol Cell Biol 89 : 836 843.[PubMed] [CrossRef]
12. Ouellette SP,, Dorsey FC,, Moshiach S,, Cleveland JL,, Carabeo RA . 2011. Chlamydia species-dependent differences in the growth requirement for lysosomes. PLoS One 6 : e16783. doi:10.1371/journal.pone.0016783 [PubMed] [CrossRef]
13. Liu Z,, Zhang YW,, Chang YS,, Fang FD . 2006. The role of cytoskeleton in glucose regulation. Biochemistry (Mosc) 71 : 476 480.[PubMed] [CrossRef]
14. Beuzon CR,, Salcedo SP,, Holden DW . 2002. Growth and killing of a Salmonella enterica serovar Typhimurium sifA mutant strain in the cytosol of different host cell lines. Microbiology 148 : 2705 2715.[PubMed]
15. van der Wel N,, Hava D,, Houben D,, Fluitsma D,, van Zon M,, Pierson J,, Brenner M,, Peters PJ . 2007. M. tuberculosis and M. leprae translocate from the phagolysosome to the cytosol in myeloid cells. Cell 129 : 1287 1298.[PubMed] [CrossRef]
16. Knodler LA,, Vallance BA,, Celli J,, Winfree S,, Hansen B,, Montero M,, Steele-Mortimer O . 2010. Dissemination of invasive Salmonella via bacterial-induced extrusion of mucosal epithelia. Proc Natl Acad Sci U S A 107 : 17733 17738.[PubMed] [CrossRef]
17. Malik-Kale P,, Winfree S,, Steele-Mortimer O . 2012. The bimodal lifestyle of intracellular Salmonella in epithelial cells: replication in the cytosol obscures defects in vacuolar replication. PLoS One 7 : e38732. doi:10.1371/journal.pone.0038732 [CrossRef]
18. Grant AJ,, Morgan FJ,, McKinley TJ,, Foster GL,, Maskell DJ,, Mastroeni P . 2012. Attenuated Salmonella Typhimurium lacking the pathogenicity island-2 type 3 secretion system grow to high bacterial numbers inside phagocytes in mice. PLoS Pathog 8 : e1003070. doi:10.1371/journal.ppat.1003070 [CrossRef]
19. Birmingham CL,, Canadien V,, Kaniuk NA,, Steinberg BE,, Higgins DE,, Brumell JH . 2008. Listeriolysin O allows Listeria monocytogenes replication in macrophage vacuoles. Nature 451 : 350 354.[PubMed] [CrossRef]
20. Schmidt H,, Hensel M . 2004. Pathogenicity islands in bacterial pathogenesis. Clin Microbiol Rev 17 : 14 56.[PubMed] [CrossRef]
21. Rohmer L,, Hocquet D,, Miller SI . 2011. Are pathogenic bacteria just looking for food? Metabolism and microbial pathogenesis. Trends Microbiol 19 : 341 348.[PubMed] [CrossRef]
22. Lopez CA,, Winter SE,, Rivera-Chavez F,, Xavier MN,, Poon V,, Nuccio SP,, Tsolis RM,, Baumler AJ . 2012. Phage-mediated acquisition of a type III secreted effector protein boosts growth of salmonella by nitrate respiration. MBio 3 : e00143-12. doi:10.1128/mBio.00143-12 [CrossRef]
23. Maurelli AT,, Fernández RE,, Bloch CA,, Rode CK,, Fasano A . 1998. “Black holes” and bacterial pathogenicity: a large genomic deletion that enhances the virulence of Shigella spp. and enteroinvasive Escherichia coli . Proc Natl Acad Sci U S A 95 : 3943 3948.[PubMed] [CrossRef]
24. Ochman H,, Moran NA . 2001. Genes lost and genes found: evolution of bacterial pathogenesis and symbiosis. Science 292 : 1096 1099.[PubMed] [CrossRef]
25. Rocco CJ,, Escalante-Semerena JC . 2010. In Salmonella enterica, 2-methylcitrate blocks gluconeogenesis. J Bacteriol 192 : 771 778.[PubMed] [CrossRef]
26. Bliven KA,, Maurelli AT . 2012. Antivirulence genes: insights into pathogen evolution through gene loss. Infect Immun 80 : 4061 4070.[PubMed] [CrossRef]
27. Eisenreich W,, Dandekar T,, Heesemann J,, Goebel W . 2010. Carbon metabolism of intracellular bacterial pathogens and possible links to virulence. Nat Rev Microbiol 8 : 401 412.[PubMed] [CrossRef]
28. Fuchs TM,, Eisenreich W,, Heesemann J,, Goebel W . 2012. Metabolic adaptation of human pathogenic and related nonpathogenic bacteria to extra- and intracellular habitats. FEMS Microbiol Rev 36 : 435 462.[PubMed] [CrossRef]
29. Aké FM,, Joyet P,, Deutscher J,, Milohanic E . 2011. Mutational analysis of glucose transport regulation and glucose-mediated virulence gene repression in Listeria monocytogenes . Mol Microbiol 81 : 274 293.[PubMed] [CrossRef]
30. Eisenreich W,, Heesemann J,, Rudel T,, Goebel W . 2013. Metabolic host responses to infection by intracellular bacterial pathogens. Front Cell Infect Microbiol 3 : 24. [PubMed] [CrossRef]
31. Creasey EA,, Isberg RR . 2012. The protein SdhA maintains the integrity of the Legionella-containing vacuole. Proc Natl Acad Sci U S A 109 : 3481 3486.[PubMed] [CrossRef]
32. Aachoui Y,, Leaf IA,, Hagar JA,, Fontana MF,, Campos CG,, Zak DE,, Tan MH,, Cotter PA,, Vance RE,, Aderem A,, Miao EA . 2013. Caspase-11 protects against bacteria that escape the vacuole. Science 339 : 975 978.[PubMed] [CrossRef]
33. Pearce EL,, Pearce EJ . 2013. Metabolic pathways in immune cell activation and quiescence. Immunity 38 : 633 643.[PubMed] [CrossRef]
34. Goetz M,, Bubert A,, Wang G,, Chico-Calero I,, Vazquez-Boland JA,, Beck M,, Slaghuis J,, Szalay AA,, Goebel W . 2001. Microinjection and growth of bacteria in the cytosol of mammalian host cells. Proc Natl Acad Sci U S A 98 : 12221 12226.[PubMed] [CrossRef]
35. Meibom KL,, Charbit A . 2010. Francisella tularensis metabolism and its relation to virulence. Front Microbiol 1 : 140. [PubMed] [CrossRef]
36. Schauer K,, Geginat G,, Liang C,, Goebel W,, Dandekar T,, Fuchs TM . 2010. Deciphering the intracellular metabolism of Listeria monocytogenes by mutant screening and modelling. BMC Genomics 11 : 573. [PubMed] [CrossRef]
37. Fuchs TM,, Eisenreich W,, Kern T,, Dandekar T . 2012. Toward a systemic understanding of Listeria monocytogenes metabolism during infection. Front Microbiol 3 : 23. [PubMed] [CrossRef]
38. Abu Kwaik Y,, Bumann D . 2013. Microbial quest for food in vivo: ‘nutritional virulence’ as an emerging paradigm. Cell Microbiol 15 : 882 890.[PubMed] [CrossRef]
39. Gordon S,, Taylor PR . 2005. Monocyte and macrophage heterogeneity. Nat Rev Immunol 5 : 953 964.[PubMed] [CrossRef]
40. Martinez FO,, Sica A,, Mantovani A,, Locati M . 2008. Macrophage activation and polarization. Front Biosci 13 : 453 461.[PubMed] [CrossRef]
41. Odegaard JI,, Chawla A . 2011. Alternative macrophage activation and metabolism. Annu Rev Pathol 6 : 275 297.[PubMed] [CrossRef]
42. Appelberg R . 2006. Macrophage nutriprive antimicrobial mechanisms. J Leukoc Biol 79 : 1117 1128.[PubMed] [CrossRef]
43. Cellier MF,, Courville P,, Campion C . 2007. Nramp1 phagocyte intracellular metal withdrawal defense. Microbes Infect 9 : 1662 1670.[PubMed] [CrossRef]
44. Taylor MW,, Feng GS . 1991. Relationship between interferon-gamma, indoleamine 2,3-dioxygenase, and tryptophan catabolism. FASEB J 5 : 2516 2522.[PubMed]
45. Gouin E,, Welch MD,, Cossart P . 2005. Actin-based motility of intracellular pathogens. Curr Opin Microbiol 8 : 35 45.[PubMed] [CrossRef]
46. Chen J,, de Felipe KS,, Clarke M,, Lu H,, Anderson OR,, Segal G,, Shuman HA . 2004. Legionella effectors that promote nonlytic release from protozoa. Science 303 : 1358 1361.[PubMed] [CrossRef]
47. Hagedorn M,, Rohde KH,, Russell DG,, Soldati T . 2009. Infection by tubercular mycobacteria is spread by nonlytic ejection from their amoeba hosts. Science 323 : 1729 1733.[PubMed] [CrossRef]
48. Vander Heiden MG,, Cantley LC,, Thompson CB . 2009. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 324 : 1029 1033.[PubMed] [CrossRef]
49. Smolková K,, Ježek P . 2012. The role of mitochondrial NADPH-dependent isocitrate dehydrogenase in cancer cells. Int J Cell Biol 2012 : 273947. [PubMed] [CrossRef]
50. Dang L,, Jin S,, Su SM . 2010. IDH mutations in glioma and acute myeloid leukemia. Trends Mol Med 16 : 387 397.[PubMed] [CrossRef]
51. Chen JQ,, Russo J . 2012. Dysregulation of glucose transport, glycolysis, TCA cycle and glutaminolysis by oncogenes and tumor suppressors in cancer cells. Biochim Biophys Acta 1826 : 370 384.[CrossRef]
52. Cardaci S,, Ciriolo MR . 2012. TCA cycle defects and cancer: when metabolism tunes redox state. Int J Cell Biol 2012 : 161837. [PubMed] [CrossRef]
53. Jones RG,, Thompson CB . 2009. Tumor suppressors and cell metabolism: a recipe for cancer growth. Genes Dev 23 : 537 548.[PubMed] [CrossRef]
54. Puzio-Kuter AM . 2011. The role of p53 in metabolic regulation. Genes Cancer 2 : 385 391.[PubMed] [CrossRef]
55. Parsot C . 2005. Shigella spp. and enteroinvasive Escherichia coli pathogenicity factors. FEMS Microbiol Lett 252 : 11 18.[PubMed] [CrossRef]
56. Bernardini ML,, Mounier J,, d’Hauteville H,, Coquis-Rondon M,, Sansonetti PJ . 1989. Identification of icsA, a plasmid locus of Shigella flexneri that governs bacterial intra- and intercellular spread through interaction with F-actin. Proc Natl Acad Sci U S A 86 : 3867 3871.[PubMed] [CrossRef]
57. Parsot C . 2009. Shigella type III secretion effectors: how, where, when, for what purposes? Curr Opin Microbiol 12 : 110 116.[PubMed] [CrossRef]
58. Barabote RD,, Saier MH Jr . 2005. Comparative genomic analyses of the bacterial phosphotransferase system. Microbiol Mol Biol Rev 69 : 608 634.[PubMed] [CrossRef]
59. Island MD,, Wei BY,, Kadner RJ . 1992. Structure and function of the uhp genes for the sugar phosphate transport system in Escherichia coli and Salmonella typhimurium . J Bacteriol 174 : 2754 2762.[PubMed]
60. Verhamme DT,, Arents JC,, Postma PW,, Crielaard W,, Hellingwerf KJ . 2001. Glucose-6-phosphate-dependent phosphoryl flow through the Uhp two-component regulatory system. Microbiology 147 : 3345 3352.[PubMed]
61. Runyen-Janecky LJ,, Payne SM . 2002. Identification of chromosomal Shigella flexneri genes induced by the eukaryotic intracellular environment. Infect Immun 70 : 4379 4388.[PubMed] [CrossRef]
62. Lucchini S,, Liu H,, Jin Q,, Hinton JC,, Yu J . 2005. Transcriptional adaptation of Shigella flexneri during infection of macrophages and epithelial cells: insights into the strategies of a cytosolic bacterial pathogen. Infect Immun 73 : 88 102.[PubMed] [CrossRef]
63. Hamilton S,, Bongaerts RJ,, Mulholland F,, Cochrane B,, Porter J,, Lucchini S,, Lappin-Scott HM,, Hinton JC . 2009. The transcriptional programme of Salmonella enterica serovar Typhimurium reveals a key role for tryptophan metabolism in biofilms. BMC Genomics 10 : 599. [PubMed] [CrossRef]
64. Cersini A,, Salvia AM,, Bernardini ML . 1998. Intracellular multiplication and virulence of Shigella flexneri auxotrophic mutants. Infect Immun 66 : 549 557.[PubMed]
65. Götz A,, Eylert E,, Eisenreich W,, Goebel W . 2010. Carbon metabolism of enterobacterial human pathogens growing in epithelial colorectal adenocarcinoma (Caco-2) cells. PLoS One 5 : e10586. doi:10.1371/journal.pone.0010586 [PubMed]
66. Gore AL,, Payne SM . 2010. CsrA and Cra influence Shigella flexneri pathogenesis. Infect Immun 78 : 4674 4682.[PubMed] [CrossRef]
67. Romeo T . 1998. Global regulation by the small RNA-binding protein CsrA and the non-coding RNA molecule CsrB. Mol Microbiol 29 : 1321 1330.[PubMed] [CrossRef]
68. Saier MH Jr,, Ramseier TM . 1996. The catabolite repressor/activator (Cra) protein of enteric bacteria. J Bacteriol 178 : 3411 3417.[PubMed]
69. Noriega FR,, Losonsky G,, Wang JY,, Formal SB,, Levine MM . 1996. Further characterization of delta aroA delta virG Shigella flexneri 2a strain CVD 1203 as a mucosal Shigella vaccine and as a live-vector vaccine for delivering antigens of enterotoxigenic Escherichia coli . Infect Immun 64 : 23 27.[PubMed]
70. Cersini A,, Martino MC,, Martini I,, Rossi G,, Bernardini ML . 2003. Analysis of virulence and inflammatory potential of Shigella flexneri purine biosynthesis mutants. Infect Immun 71 : 7002 7013.[PubMed] [CrossRef]
71. Bergounioux J,, Elisee R,, Prunier AL,, Donnadieu F,, Sperandio B,, Sansonetti P,, Arbibe L . 2012. Calpain activation by the Shigella flexneri effector VirA regulates key steps in the formation and life of the bacterium’s epithelial niche. Cell Host Microbe 11 : 240 252.[PubMed] [CrossRef]
72. Pieper R,, Zhang Q,, Parmar PP,, Huang ST,, Clark DJ,, Alami H,, Donohue-Rolfe A,, Fleischmann RD,, Peterson SN,, Tzipori S . 2009. The Shigella dysenteriae serotype 1 proteome, profiled in the host intestinal environment, reveals major metabolic modifications and increased expression of invasive proteins. Proteomics 9 : 5029 5045.[PubMed] [CrossRef]
73. Velge P,, Roche SM . 2010. Variability of Listeria monocytogenes virulence: a result of the evolution between saprophytism and virulence? Future Microbiol 5 : 1799 1821.[PubMed] [CrossRef]
74. Mostowy S,, Cossart P . 2012. Virulence factors that modulate the cell biology of Listeria infection and the host response. Adv Immunol 113 : 19 32.[PubMed] [CrossRef]
75. Camejo A,, Carvalho F,, Reis O,, Leitão E,, Sousa S,, Cabanes D . 2011. The arsenal of virulence factors deployed by Listeria monocytogenes to promote its cell infection cycle. Virulence 2 : 379 394.[PubMed] [CrossRef]
76. Stoll R,, Goebel W . 2010. The major PEP-phosphotransferase systems (PTSs) for glucose, mannose and cellobiose of Listeria monocytogenes, and their significance for extra- and intracellular growth. Microbiology 156 : 1069 1083.[PubMed] [CrossRef]
77. Chico-Calero I,, Suárez M,, González-Zorn B,, Scortti M,, Slaghuis J,, Goebel W,, Vazquez-Boland JA . 2002. Hpt, a bacterial homolog of the microsomal glucose-6-phosphate translocase, mediates rapid intracellular proliferation in Listeria . Proc Natl Acad Sci U S A 99 : 431 436.[PubMed] [CrossRef]
78. Eisenreich W,, Slaghuis J,, Laupitz R,, Bussemer J,, Stritzker J,, Schwarz C,, Schwarz R,, Dandekar T,, Goebel W,, Bacher A . 2006. 13C isotopologue perturbation studies of Listeria monocytogenes carbon metabolism and its modulation by the virulence regulator PrfA. Proc Natl Acad Sci U S A 103 : 2040 2045.[PubMed] [CrossRef]
79. Schär J,, Stoll R,, Schauer K,, Loeffler DI,, Eylert E,, Joseph B,, Eisenreich W,, Fuchs TM,, Goebel W . 2010. Pyruvate carboxylase plays a crucial role in carbon metabolism of extra- and intracellularly replicating Listeria monocytogenes . J Bacteriol 192 : 1774 1784.[PubMed] [CrossRef]
80. Premaratne RJ,, Lin WJ,, Johnson EA . 1991. Development of an improved chemically defined minimal medium for Listeria monocytogenes . Appl Environ Microbiol 57 : 3046 3048.[PubMed]
81. Tsai HN,, Hodgson DA . 2003. Development of a synthetic minimal medium for Listeria monocytogenes . Appl Environ Microbiol 69 : 6943 6945.[CrossRef]
82. Stoll R,, Mertins S,, Joseph B,, Müller-Altrock S,, Goebel W . 2008. Modulation of PrfA activity in Listeria monocytogenes upon growth in different culture media. Microbiology 154 : 3856 3876.[PubMed] [CrossRef]
83. Schneebeli R,, Egli T . 2013. A defined, glucose-limited mineral medium for the cultivation of Listeria spp. Appl Environ Microbiol 79 : 2503 2511.[PubMed] [CrossRef]
84. Glaser P,, Frangeul L,, Buchrieser C,, Rusniok C,, Amend A,, Baquero F,, Berche P,, Bloecker H,, Brandt P,, Chakraborty T,, Charbit A,, Chetouani F,, Couvé E,, de Daruvar A,, Dehoux P,, Domann E,, Domínguez-Bernal G,, Duchaud E,, Durant L,, Dussurget O,, Entian KD,, Fsihi H,, García-del Portillo F,, Garrido P,, Gautier L,, Goebel W,, Gómez-López N,, Hain T,, Hauf J,, Jackson D,, Jones LM,, Kaerst U,, Kreft J,, Kuhn M,, Kunst F,, Kurapkat G,, Madueno E,, Maitournam A,, Vicente JM,, Ng E,, Nedjari H,, Nordsiek G,, Novella S,, de Pablos B,, Pérez-Diaz JC,, Purcell R,, Remmel B,, Rose M,, Schlueter T,, Simoes N,, Tierrez A,, Vázquez-Boland JA,, Voss H,, Wehland J,, Cossart P . 2001. Comparative genomics of Listeria species. Science 294 : 849 852.[PubMed]
85. Joseph B,, Przybilla K,, Stühler C,, Schauer K,, Slaghuis J,, Fuchs TM,, Goebel W . 2006. Identification of Listeria monocytogenes genes contributing to intracellular replication by expression profiling and mutant screening. J Bacteriol 188 : 556 568.[PubMed] [CrossRef]
86. Lobel L,, Sigal N,, Borovok I,, Ruppin E,, Herskovits AA . 2012. Integrative genomic analysis identifies isoleucine and CodY as regulators of Listeria monocytogenes virulence. PLoS Genet 8 : e1002887. doi:10.1371/journal.pgen.1002887 [CrossRef]
87. Chakraborty T,, Leimeister-Wächter M,, Domann E,, Hartl M,, Goebel W,, Nichterlein T,, Notermans S . 1992. Coordinate regulation of virulence genes in Listeria monocytogenes requires the product of the prfA gene. J Bacteriol 174 : 568 574.[PubMed]
88. Joseph B,, Mertins S,, Stoll R,, Schär J,, Umesha KR,, Luo Q,, Müller-Altrock S,, Goebel W . 2008. Glycerol metabolism and PrfA activity in Listeria monocytogenes . J Bacteriol 190 : 5412 5430.[PubMed] [CrossRef]
89. de las Heras A,, Cain RJ,, Bielecka MK,, Vázquez-Boland JA . 2011. Regulation of Listeria virulence: PrfA master and commander. Curr Opin Microbiol 14 : 118 127.[PubMed] [CrossRef]
90. Shivers RP,, Sonenshein AL . 2004. Activation of the Bacillus subtilis global regulator CodY by direct interaction with branched-chain amino acids. Mol Microbiol 53 : 599 611.[PubMed] [CrossRef]
91. Chatterjee SS,, Hossain H,, Otten S,, Kuenne C,, Kuchmina K,, Machata S,, Domann E,, Chakraborty T,, Hain T . 2006. Intracellular gene expression profile of Listeriamonocytogenes . Infect Immun 74 : 1323 1338.[PubMed] [CrossRef]
92. Donaldson JR,, Nanduri B,, Pittman JR,, Givaruangsawat S,, Burgess SC,, Lawrence ML . 2011. Proteomic expression profiles of virulent and avirulent strains of Listeria monocytogenes isolated from macrophages. J Proteomics 74 : 1906 1917.[PubMed] [CrossRef]
93. Eylert E,, Schär J,, Mertins S,, Stoll R,, Bacher A,, Goebel W,, Eisenreich W . 2008. Carbon metabolism of Listeria monocytogenes growing inside macrophages. Mol Microbiol 69 : 1008 1017.[PubMed] [CrossRef]
94. Gillmaier N,, Götz A,, Schulz A,, Eisenreich W,, Goebel W . 2012. Metabolic responses of primary and transformed cells to intracellular Listeria monocytogenes . PLoS One 7 : e52378. doi:10.1371/journal.pone.0052378 [PubMed]
95. Toledo-Arana A,, Dussurget O,, Nikitas G,, Sesto N,, Guet-Revillet H,, Balestrino D,, Loh E,, Gripenland J,, Tiensuu T,, Vaitkevicius K,, Barthelemy M,, Vergassola M,, Nahori MA,, Soubigou G,, Régnault B,, Coppée JY,, Lecuit M,, Johansson J,, Cossart P . 2009. The Listeria transcriptional landscape from saprophytism to virulence. Nature 459 : 950 956.[PubMed] [CrossRef]
96. Camejo A,, Buchrieser C,, Couvé E,, Carvalho F,, Reis O,, Ferreira P,, Sousa S,, Cossart P,, Cabanes D . 2009. In vivo transcriptional profiling of Listeria monocytogenes and mutagenesis identify new virulence factors involved in infection. PLoS Pathog 5 : e1000449. doi:10.1371/journal.ppat.1000449
97. Port GC,, Freitag NE . 2007. Identification of novel Listeria monocytogenes secreted virulence factors following mutational activation of the central virulence regulator, PrfA. Infect Immun 75 : 5886 5897.[PubMed] [CrossRef]
98. Cohen P,, Bouaboula M,, Bellis M,, Baron V,, Jbilo O,, Poinot-Chazel C,, Galiègue S,, Hadibi EH,, Casellas P . 2000. Monitoring cellular responses to Listeria monocytogenes with oligonucleotide arrays. J Biol Chem 275 : 11181 11190.[PubMed] [CrossRef]
99. Lecuit M,, Sonnenburg JL,, Cossart P,, Gordon JI . 2007. Functional genomic studies of the intestinal response to a foodborne enteropathogen in a humanized gnotobiotic mouse model. J Biol Chem 282 : 15065 15072.[PubMed] [CrossRef]
100. Valbuena G,, Walker DH . 2009. Infection of the endothelium by members of the order Rickettsiales. Thromb Haemost 102 : 1071 1079.[PubMed] [CrossRef]
101. Cowan G . 2000. Rickettsial diseases: the typhus group of fevers–a review. Postgrad Med J 76 : 269 272.[PubMed] [CrossRef]
102. Walker DH,, Ismail N . 2008. Emerging and re-emerging rickettsioses: endothelial cell infection and early disease events. Nat Rev Microbiol 6 : 375 386.[PubMed] [CrossRef]
103. Andersson SG,, Zomorodipour A,, Andersson JO,, Sicheritz-Pontén T,, Alsmark UC,, Podowski RM,, Näslund AK,, Eriksson AS,, Winkler HH,, Kurland CG . 1998. The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature 396 : 133 140.[PubMed] [CrossRef]
104. Winkler HH . 1995. Rickettsia prowazekii, ribosomes and slow growth. Trends Microbiol 3 : 196 198.[PubMed] [CrossRef]
105. Winkler HH,, Daugherty RM . 1986. Acquisition of glucose by Rickettsia prowazekii through the nucleotide intermediate uridine 5′-diphosphoglucose. J Bacteriol 167 : 805 808.[PubMed]
106. Zomorodipour A,, Andersson SG . 1999. Obligate intracellular parasites: Rickettsia prowazekii and Chlamydia trachomatis . FEBS Lett 452 : 11 15.[PubMed] [CrossRef]
107. Fuxelius HH,, Darby A,, Min CK,, Cho NH,, Andersson SG . 2007. The genomic and metabolic diversity of Rickettsia . Res Microbiol 158 : 745 753.[PubMed] [CrossRef]
108. Frohlich KM,, Audia JP . 2013. Dual mechanisms of metabolite acquisition by the obligate intracytosolic pathogen Rickettsia prowazekii reveal novel aspects of triose phosphate transport. J Bacteriol 195 : 3752 3760.[PubMed] [CrossRef]
109. Smith DK,, Winkler HH . 1977. Characterization of a lysine-specific active transport system in Rickettsia prowazeki . J Bacteriol 129 : 1349 1355.[PubMed]
110. Atkinson WH,, Winkler HH . 1989. Permeability of Rickettsia prowazekii to NAD. J Bacteriol 171 : 761 766.[PubMed]
111. Tucker AM,, Winkler HH,, Driskell LO,, Wood DO . 2003. S-adenosylmethionine transport in Rickettsia prowazekii . J Bacteriol 185 : 3031 3035.[PubMed] [CrossRef]
112. Frohlich KM,, Roberts RA,, Housley NA,, Audia JP . 2010. Rickettsia prowazekii uses an sn-glycerol-3-phosphate dehydrogenase and a novel dihydroxyacetone phosphate transport system to supply triose phosphate for phospholipid biosynthesis. J Bacteriol 192 : 4281 4288.[PubMed] [CrossRef]
113. Sahni SK,, Rydkina E . 2009. Host-cell interactions with pathogenic Rickettsia species. Future Microbiol 4 : 323 339.[PubMed] [CrossRef]
114. Clifton DR,, Goss RA,, Sahni SK,, van Antwerp D,, Baggs RB,, Marder VJ,, Silverman DJ,, Sporn LA . 1998. NF-kappa B-dependent inhibition of apoptosis is essential for host cellsurvival during Rickettsia rickettsii infection. Proc Natl Acad Sci U S A 95 : 4646 4651.[PubMed] [CrossRef]
115. Malik-Kale P,, Jolly CE,, Lathrop S,, Winfree S,, Luterbach C,, Steele-Mortimer O . 2011. Salmonella - at home in the host cell. Front Microbiol 2 : 125. [PubMed] [CrossRef]
116. Swart AL,, Hensel M . 2012. Interactions of Salmonella enterica with dendritic cells. Virulence 3 : 660 667.[PubMed] [CrossRef]
117. de Jong HK,, Parry CM,, van der Poll T,, Wiersinga WJ . 2012. Host-pathogen interaction in invasive Salmonellosis. PLoS Pathog 8 : e1002933. doi:10.1371/journal.ppat.1002933 [PubMed] [CrossRef]
118. van der Heijden J,, Finlay BB . 2012. Type III effector-mediated processes in Salmonella infection. Future Microbiol 7 : 685 703.[PubMed] [CrossRef]
119. Fàbrega A,, Vila J . 2013. Salmonella enterica serovar Typhimurium skills to succeed in the host: virulence and regulation. Clin Microbiol Rev 26 : 308 341.[PubMed] [CrossRef]
120. McClelland M,, Sanderson KE,, Spieth J,, Clifton SW,, Latreille P,, Courtney L,, Porwollik S,, Ali J,, Dante M,, Du F,, Hou S,, Layman D,, Leonard S,, Nguyen C,, Scott K,, Holmes A,, Grewal N,, Mulvaney E,, Ryan E,, Sun H,, Florea L,, Miller W,, Stoneking T,, Nhan M,, Waterston R,, Wilson RK . 2001. Complete genome sequence of Salmonella enterica serovar Typhimurium LT2. Nature 413 : 852 856.[PubMed] [CrossRef]
121. Haraga A,, Ohlson MB,, Miller SI . 2008. Salmonellae interplay with host cells. Nat Rev Microbiol 6 : 53 66.[PubMed] [CrossRef]
122. Bumann D . 2009. System-level analysis of Salmonella metabolism during infection. Curr Opin Microbiol 12 : 559 567.[PubMed] [CrossRef]
123. Bowden SD,, Rowley G,, Hinton JC,, Thompson A . 2009. Glucose and glycolysis are required for the successful infection of macrophages and mice by Salmonella enterica serovar typhimurium. Infect Immun 77 : 3117 3126.[PubMed] [CrossRef]
124. Tchawa Yimga M,, Leatham MP,, Allen JH,, Laux DC,, Conway T,, Cohen PS . 2006. Role of gluconeogenesis and the tricarboxylic acid cycle in the virulence of Salmonella enterica serovar Typhimurium in BALB/c mice. Infect Immun 74 : 1130 1140.[PubMed] [CrossRef]
125. Moest TP,, Méresse S . 2013. Salmonella T3SSs: successful mission of the secret(ion) agents. Curr Opin Microbiol 16 : 38 44.[PubMed] [CrossRef]
126. Knodler LA,, Finlay BB,, Steele-Mortimer O . 2005. The Salmonella effector protein SopB protects epithelial cells from apoptosis by sustained activation of Akt. J Biol Chem 280 : 9058 9064.[PubMed] [CrossRef]
127. Yin C,, Qie S,, Sang N . 2012. Carbon source metabolism and its regulation in cancer cells. Crit Rev Eukaryot Gene Expr 22 : 17 35.[PubMed] [CrossRef]
128. Kuijl C,, Savage ND,, Marsman M,, Tuin AW,, Janssen L,, Egan DA,, Ketema M,, van den Nieuwendijk R,, van den Eeden SJ,, Geluk A,, Poot A,, van der Marel G,, Beijersbergen RL,, Overkleeft H,, Ottenhoff TH,, Neefjes J . 2007. Intracellular bacterial growth is controlled by a kinase network around PKB/AKT1. Nature 450 : 725 730.[PubMed] [CrossRef]
129. Hardt WD,, Gálan JE . 1997. A secreted Salmonella protein with homology to an avirulence determinant of plant pathogenic bacteria. Proc Natl Acad Sci U S A 94 : 9887 9892.[PubMed] [CrossRef]
130. Liu X,, Lu R,, Xia Y,, Wu S,, Sun J . 2010. Eukaryotic signaling pathways targeted by Salmonella effector protein AvrA in intestinal infection in vivo . BMC Microbiol 10 : 326. [PubMed] [CrossRef]
131. Wu S,, Ye Z,, Liu X,, Zhao Y,, Xia Y,, Steiner A,, Petrof EO,, Claud EC,, Sun J . 2010. Salmonella typhimurium infection increases p53 acetylation in intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol 298 : G784 G794.[PubMed] [CrossRef]
132. Thiennimitr P,, Winter SE,, Winter MG,, Xavier MN,, Tolstikov V,, Huseby DL,, Sterzenbach T,, Tsolis RM,, Roth JR,, Bäumler AJ . 2011. Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota. Proc Natl Acad Sci U S A 108 : 17480 17485.[PubMed] [CrossRef]
133. Bertin Y,, Girardeau JP,, Chaucheyras-Durand F,, Lyan B,, Pujos-Guillot E,, Harel J,, Martin C . 2011. Enterohaemorrhagic Escherichia coli gains a competitive advantage by using ethanolamine as a nitrogen source in the bovine intestinal content. Environ Microbiol 13 : 365 377.[PubMed] [CrossRef]
134. Shi L,, Chowdhury SM,, Smallwood HS,, Yoon H,, Mottaz-Brewer HM,, Norbeck AD,, McDermott JE,, Clauss TR,, Heffron F,, Smith RD,, Adkins JN . 2009. Proteomic investigation of the time course responses of RAW 264.7 macrophages to infection with Salmonella enterica . Infect Immun 77 : 3227 3233.[PubMed] [CrossRef]
135. Uchiya K,, Nikai T . 2004. Salmonella enterica serovar Typhimurium infection induces cyclooxygenase 2 expression in macrophages: involvement of Salmonella pathogenicity island 2. Infect Immun 72 : 6860 6869.[PubMed] [CrossRef]
136. Fraser DW,, Tsai TR,, Orenstein W,, Parkin WE,, Beecham HJ,, Sharrar RG,, Harris J,, Mallison GF,, Martin SM,, McDade JE,, Shepard CC,, Brachman PS . 1977. Legionnaires’ disease: description of an epidemic of pneumonia. N Engl J Med 297 : 1189 1197.[PubMed] [CrossRef]
137. Xu L,, Luo ZQ . 2013. Cell biology of infection by Legionella pneumophila . Microbes Infect 15 : 157 167.[PubMed] [CrossRef]
138. Tilney LG,, Harb OS,, Connelly PS,, Robinson CG,, Roy CR . 2001. How the parasitic bacterium Legionella pneumophila modifies its phagosome and transforms it into rough ER: implications for conversion of plasma membrane to the ER membrane. J Cell Sci 114 : 4637 4650.[PubMed]
139. Heidtman M,, Chen EJ,, Moy MY,, Isberg RR . 2009. Large-scale identification of Legionella pneumophila Dot/Icm substrates that modulate host cell vesicle trafficking pathways. Cell Microbiol 11 : 230 248.[PubMed] [CrossRef]
140. Zhu W,, Banga S,, Tan Y,, Zheng C,, Stephenson R,, Gately J,, Luo ZQ . 2011. Comprehensive identification of protein substrates of the Dot/Icm type IV transporter of Legionella pneumophila . PLoS One 6 : e17638. doi:10.1371/journal.pone.0017638 [PubMed] [CrossRef]
141. Faucher SP,, Mueller CA,, Shuman HA . 2011. Legionella pneumophila transcriptome during intracellular multiplication in human macrophages. Front Microbiol 2 : 60. [PubMed] [CrossRef]
142. Isberg RR,, O’Connor TJ,, Heidtman M . 2009. The Legionella pneumophila replication vacuole: making a cosy niche inside host cells. Nat Rev Microbiol 7 : 13 24.[PubMed] [CrossRef]
143. Xu L,, Shen X,, Bryan A,, Banga S,, Swanson MS,, Luo ZQ . 2010. Inhibition of host vacuolar H +-ATPase activity by a Legionella pneumophila effector. PLoS Pathog 6 : e1000822. doi:10.1371/journal.ppat.1000822 [PubMed] [CrossRef]
144. Chien M,, Morozova I,, Shi S,, Sheng H,, Chen J,, Gomez SM,, Asamani G,, Hill K,, Nuara J,, Feder M,, Rineer J,, Greenberg JJ,, Steshenko V,, Park SH,, Zhao B,, Teplitskaya E,, Edwards JR,, Pampou S,, Georghiou A,, Chou IC,, Iannuccilli W,, Ulz ME,, Kim DH,, Geringer-Sameth A,, Goldsberry C,, Morozov P,, Fischer SG,, Segal G,, Qu X,, Rzhetsky A,, Zhang P,, Cayanis E,, De Jong PJ,, Ju J,, Kalachikov S,, Shuman HA,, Russo JJ . 2004. The genomic sequence of the accidental pathogen Legionella pneumophila . Science 305 : 1966 1968.[PubMed] [CrossRef]
145. Warren WJ,, Miller RD . 1979. Growth of Legionnaires disease bacterium ( Legionella pneumophila) in chemically defined medium. J Clin Microbiol 10 : 50 55.[PubMed]
146. Eylert E,, Herrmann V,, Jules M,, Gillmaier N,, Lautner M,, Buchrieser C,, Eisenreich W,, Heuner K . 2010. Isotopologue profiling of Legionella pneumophila: role of serine and glucose as carbon substrates. J Biol Chem 285 : 22232 22243.[PubMed] [CrossRef]
147. Brüggemann H,, Cazalet C,, Buchrieser C . 2006. Adaptation of Legionella pneumophila to the host environment: role of protein secretion, effectors and eukaryotic-like proteins. Curr Opin Microbiol 9 : 86 94.[PubMed] [CrossRef]
148. Heuner K,, Eisenreich W . 2013. The intracellular metabolism of legionella by isotopologue profiling. Methods Mol Biol 954 : 163 181.[PubMed] [CrossRef]
149. Schwöppe C,, Winkler HH,, Neuhaus HE . 2002. Properties of the glucose-6-phosphate transporter from Chlamydia pneumoniae (HPTcp) and the glucose-6-phosphate sensor from Escherichia coli (UhpC). J Bacteriol 184 : 2108 2115.[PubMed] [CrossRef]
150. George JR,, Pine L,, Reeves MW,, Harrell WK . 1980. Amino acid requirements of Legionella pneumophila . J Clin Microbiol 11 : 286 291.[PubMed]
151. Tesh MJ,, Morse SA,, Miller RD . 1983. Intermediary metabolism in Legionella pneumophila: utilization of amino acids and other compounds as energy sources. J Bacteriol 154 : 1104 1109.[PubMed]
152. Sauer JD,, Bachman MA,, Swanson MS . 2005. The phagosomal transporter A couples threonine acquisition to differentiation and replication of Legionella pneumophila in macrophages. Proc Natl Acad Sci U S A 102 : 9924 9929.[PubMed] [CrossRef]
153. Brüggemann H,, Hagman A,, Jules M,, Sismeiro O,, Dillies MA,, Gouyette C,, Kunst F,, Steinert M,, Heuner K,, Coppée JY,, Buchrieser C . 2006. Virulence strategies for infecting phagocytes deduced from the in vivo transcriptional program of Legionella pneumophila . Cell Microbiol 8 : 1228 1240.[PubMed] [CrossRef]
154. Aurass P,, Pless B,, Rydzewski K,, Holland G,, Bannert N,, Flieger A . 2009. bdhA-patD operon as a virulence determinant, revealed by a novel large-scale approach for identification of Legionella pneumophila mutants defective for amoeba infection. Appl Environ Microbiol 75 : 4506 4515.[PubMed] [CrossRef]
155. Herrmann V,, Eidner A,, Rydzewski K,, Bládel I,, Jules M,, Buchrieser C,, Eisenreich W,, Heuner K . 2011. GamA is a eukaryotic-like glucoamylase responsible for glycogen- and starch-degrading activity of Legionella pneumophila . Int J Med Microbiol 301 : 133 139.[PubMed] [CrossRef]
156. Wieland H,, Ullrich S,, Lang F,, Neumeister B . 2005. Intracellular multiplication of Legionella pneumophila depends on host cell amino acid transporter SLC1A5. Mol Microbiol 55 : 1528 1537.[PubMed] [CrossRef]
157. Otto GP,, Wu MY,, Clarke M,, Lu H,, Anderson OR,, Hilbi H,, Shuman HA,, Kessin RH . 2004. Macroautophagy is dispensable for intracellular replication of Legionella pneumophila in Dictyostelium discoideum . Mol Microbiol 51 : 63 72.[PubMed] [CrossRef]
158. Amer AO,, Swanson MS . 2005. Autophagy is an immediate macrophage response to Legionella pneumophila . Cell Microbiol 7 : 765 778.[PubMed] [CrossRef]
159. Tung SM,, Unal C,, Ley A,, Peña C,, Tunggal B,, Noegel AA,, Krut O,, Steinert M,, Eichinger L . 2010. Loss of Dictyostelium ATG9 results in a pleiotropic phenotype affecting growth, development, phagocytosis and clearance and replication of Legionella pneumophila . Cell Microbiol 12 : 765 780.[PubMed] [CrossRef]
160. Price CT,, Al-Quadan T,, Santic M,, Rosenshine I,, Abu Kwaik Y . 2011. Host proteasomal degradation generates amino acids essential for intracellular bacterial growth. Science 334 : 1553 1557.[PubMed] [CrossRef]
161. Hubber A,, Kubori T,, Nagai H . 2013. Modulation of the ubiquitination machinery by Legionella . Curr Top Microbiol Immunol 376 : 227 247.[PubMed] [CrossRef]
162. Losick VP,, Isberg RR . 2006. NF-kappaB translocation prevents host cell death after low-dose challenge by Legionella pneumophila . J Exp Med 203 : 2177 2189.[PubMed] [CrossRef]
163. Losick VP,, Haenssler E,, Moy MY,, Isberg RR . 2010. LnaB: a Legionella pneumophila activator of NF-kappaB. Cell Microbiol 12 : 1083 1097.[PubMed] [CrossRef]
164. Rathore MG,, Saumet A,, Rossi JF,, de Bettignies C,, Tempé D,, Lecellier CH,, Villalba M . 2012. The NF-kappaB member p65 controls glutamine metabolism through miR-23a. Int J Biochem Cell Biol 44 : 1448 1456.[PubMed] [CrossRef]
165. Li Z,, Dugan AS,, Bloomfield G,, Skelton J,, Ivens A,, Losick V,, Isberg RR . 2009. The amoebal MAP kinase response to Legionella pneumophila is regulated by DupA. Cell Host Microbe 6 : 253 267.[PubMed] [CrossRef]
166. Hervet E,, Charpentier X,, Vianney A,, Lazzaroni JC,, Gilbert C,, Atlan D,, Doublet P . 2011. Protein kinase LegK2 is a type IV secretion system effector involved in endoplasmic reticulum recruitment and intracellular replication of Legionella pneumophila . Infect Immun 79 : 1936 1950.[PubMed] [CrossRef]
167. Wright HR,, Turner A,, Taylor HR . 2008. Trachoma. Lancet 371 : 1945 1954.[PubMed] [CrossRef]
168. Blasi F,, Tarsia P,, Aliberti S . 2009. Chlamydophila pneumoniae . Clin Microbiol Infect 15 : 29 35.[PubMed] [CrossRef]
169. Betts HJ,, Wolf K,, Fields KA . 2009. Effector protein modulation of host cells: examples in the Chlamydia spp. arsenal. Curr Opin Microbiol 12 : 81 87.[PubMed] [CrossRef]
170. Campbell LA,, Kuo CC . 2004. Chlamydia pneumoniae--an infectious risk factor for atherosclerosis? Nat Rev Microbiol 2 : 23 32.[PubMed] [CrossRef]
171. Haider S,, Wagner M,, Schmid MC,, Sixt BS,, Christian JG,, Hacker G,, Pichler P,, Mechtler K,, Müller A,, Baranyi C,, Toenshoff ER,, Montanaro J,, Horn M . 2010. Raman microspectroscopy reveals long-term extracellular activity of Chlamydiae. Mol Microbiol 77 : 687 700.[PubMed] [CrossRef]
172. Sixt BS,, Siegl A,, Müller C,, Watzka M,, Wultsch A,, Tziotis D,, Montanaro J,, Richter A,, Schmitt-Kopplin P,, Horn M . 2013. Metabolic features of Protochlamydia amoebophila elementary bodies--a link between activity and infectivity in Chlamydiae. PLoS Pathog 9 : e1003553. [PubMed] [CrossRef]
173. van Ooij C,, Kalman L,, van Ijzendoorn,, Nishijima M,, Hanada K,, Mostov K,, Engel JN . 2000. Host cell-derived sphingolipids are required for the intracellular growth of Chlamydia trachomatis . Cell Microbiol 2 : 627 637.[PubMed] [CrossRef]
174. Robertson DK,, Gu L,, Rowe RK,, Beatty WL . 2009. Inclusion biogenesis and reactivation of persistent Chlamydia trachomatis requires host cell sphingolipid biosynthesis. PLoS Pathog 5 : e1000664. doi:10.1371/journal.ppat.1000664 [PubMed] [CrossRef]
175. Wyrick PB . 2000. Intracellular survival by Chlamydia . Cell Microbiol 2 : 275 282.[PubMed] [CrossRef]
176. Schoborg RV . 2011. Chlamydia persistence – a tool to dissect chlamydia--host interactions. Microbes Infect 13 : 649 662.[PubMed] [CrossRef]
177. Stephens RS,, Kalman S,, Lammel C,, Fan J,, Marathe R,, Aravind L,, Mitchell W,, Olinger L,, Tatusov RL,, Zhao Q,, Koonin EV,, Davis RW . 1998. Genome sequence of an obligate intracellular pathogen of humans: Chlamydia trachomatis . Science 282 : 754 759.[PubMed] [CrossRef]
178. Kalman S,, Mitchell W,, Marathe R,, Lammel C,, Fan J,, Hyman RW,, Olinger L,, Grimwood J,, Davis RW,, Stephens RS . 1999. Comparative genomes of Chlamydia pneumoniae and C. trachomatis . Nat Genet 21 : 385 389.[PubMed] [CrossRef]
179. Hatch TP,, Al-Hossainy E,, Silverman JA . 1982. Adenine nucleotide and lysine transport in Chlamydia psittaci . J Bacteriol 150 : 662 670.[PubMed]
180. Wyllie S,, Ashley RH,, Longbottom D,, Herring AJ . 1998. The major outer membrane protein of Chlamydia psittaci functions as a porin-like ion channel. Infect Immun 66 : 5202 5207.[PubMed]
181. Trentmann O,, Horn M,, van Scheltinga AC,, Neuhaus HE,, Haferkamp I . 2007. Enlightening energy parasitism by analysis of an ATP/ADP transporter from chlamydiae. PLoS Biol 5 : e231. doi:10.1371/journal.pbio.0050231 [PubMed] [CrossRef]
182. Gérard HC,, Freise J,, Wang Z,, Roberts G,, Rudy D,, Krauss-Opatz B,, Köhler L,, Zeidler H,, Schumacher HR,, Whittum-Hudson JA,, Hudson AP . 2002. Chlamydia trachomatis genes whose products are related to energy metabolism are expressed differentially in active vs. persistent infection. Microbes Infect 4 : 13 22.[PubMed] [CrossRef]
183. Skipp P,, Robinson J,, O’Connor CD,, Clarke IN . 2005. Shotgun proteomic analysis of Chlamydia trachomatis . Proteomics 5 : 1558 1573.[PubMed] [CrossRef]
184. Iliffe-Lee ER,, McClarty G . 2000. Regulation of carbon metabolism in Chlamydia trachomatis . Mol Microbiol 38 : 20 30.[PubMed] [CrossRef]
185. Lu C,, Lei L,, Peng B,, Tang L,, Ding H,, Gong S,, Li Z,, Wu Y,, Zhong G . 2013. Chlamydia trachomatis GlgA is secreted into host cell cytoplasm. PLoS One 8 : e68764. doi:10.1371/journal.pone.0068764 [PubMed] [CrossRef]
186. Meurice G,, Deborde C,, Jacob D,, Falentin H,, Boyaval P,, Dimova D . 2004. In silico exploration of the fructose-6-phosphate phosphorylation step in glycolysis: genomic evidence of the coexistence of an atypical ATP-dependent along with a PPi-dependent phosphofructokinase in Propionibacterium freudenreichii subsp. shermanii. In Silico Biol 4 : 517 528.[PubMed]
187. Siebers B,, Klenk HP,, Hensel R . 1998. PPi-dependent phosphofructokinase from Thermoproteus tenax, an archaeal descendant of an ancient line in phosphofructokinase evolution. J Bacteriol 180 : 2137 2143.[PubMed]
188. Tjaden J,, Winkler HH,, Schwoppe C,, Van Der Laan M,, Mohlmann T,, Neuhaus HE . 1999. Two nucleotide transport proteins in Chlamydia trachomatis, one for net nucleoside triphosphate uptake and the other for transport of energy. J Bacteriol 181 : 1196 1202.[PubMed]
189. Zhong G,, Fan P,, Ji H,, Dong F,, Huang Y . 2001. Identification of a chlamydial protease-like activity factor responsible for the degradation of host transcription factors. J Exp Med 193 : 935 942.[PubMed] [CrossRef]
190. Wu X,, Lei L,, Gong S,, Chen D,, Flores R,, Zhong G . 2011. The chlamydial periplasmic stress response serine protease cHtrA is secreted into host cell cytosol. BMC Microbiol 11 : 87. [PubMed] [CrossRef]
191. Chen AL,, Johnson KA,, Lee JK,, Sütterlin C,, Tan M . 2012. CPAF: a Chlamydial protease in search of an authentic substrate. PLoS Pathog 8 : e1002842. doi:10.1371/journal.ppat.1002842 [PubMed] [CrossRef]
192. Fox A,, Rogers JC,, Gilbart J,, Morgan S,, Davis CH,, Knight S,, Wyrick PB . 1990. Muramic acid is not detectable in Chlamydia psittaci or Chlamydia trachomatis by gas chromatography-mass spectrometry. Infect Immun 58 : 835 837.[PubMed]
193. Wood H,, Fehlner-Gardner C,, Berry J,,