Systems approach to investigating host-pathogen interactions in infections with the biothreat agent Francisella. Constraints-based model of Francisella tularensis

BMC Systems Biology

Volumn 4, Issue , 2010, Pages

  Raghunathan, Anu ^a,b   Shin, Sookil ^a   Daefler, Simon ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b NATIONAL CHEMICAL LABORATORY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

FRANCISELLA; FRANCISELLA TULARENSIS;

ANTIINFECTIVE AGENT; CARBON;

ARTICLE; BACTERIAL GENE; BIOLOGICAL MODEL; BIOLOGICAL WARFARE AGENT; DRUG EFFECT; FRANCISELLA TULARENSIS; GENE EXPRESSION PROFILING; GENETICS; HOST PATHOGEN INTERACTION; METABOLISM; METHODOLOGY; PATHOGENICITY; PHYSIOLOGY; SYSTEMS BIOLOGY; TULAREMIA;

ANTI-BACTERIAL AGENTS; BIOLOGICAL WARFARE AGENTS; CARBON; FRANCISELLA TULARENSIS; GENE EXPRESSION PROFILING; GENES, BACTERIAL; HOST-PATHOGEN INTERACTIONS; METABOLIC NETWORKS AND PATHWAYS; MODELS, BIOLOGICAL; SYSTEMS BIOLOGY; TULAREMIA;

EID: 77956416193     PISSN: None     EISSN: 17520509     Source Type: Journal    
DOI: 10.1186/1752-0509-4-118     Document Type: Article

References (51)

1. McLendon MK, Apicella MA, Allen LA. Francisella tularensis: taxonomy, genetics, and Immunopathogenesis of a potential agent of biowarfare. Annu Rev Microbiol 2006, 60:167-185. 10.1146/annurev.micro.60.080805.142126, 1945232, 16704343.
2. Dennis DT, Inglesby TV, Henderson DA, Bartlett JG, Ascher MS, Eitzen E, Fine AD, Friedlander AM, Hauer J, Layton M, Lillibridge SR, McDade JE, Osterholm MT, O'Toole T, Parker G, Perl TM, Russell PK, Tonat K. Tularemia as a biological weapon: medical and public health management. JAMA 2001, 285:2763-2773. 10.1001/jama.285.21.2763, 11386933.
3. Feist AM, Herrgard MJ, Thiele I, Reed JL, Palsson BO. Reconstruction of biochemical networks in microorganisms. Nat Rev Microbiol 2009, 7:129-143.
4. Feist AM, Henry CS, Reed JL, Krummenacker M, Joyce AR, Karp PD, Broadbelt LJ, Hatzimanikatis V, Palsson BO. A genome-scale metabolic reconstruction for Escherichia coli K-12 MG1655 that accounts for 1260 ORFs and thermodynamic information. Mol Syst Biol 2007, 3:121. 10.1038/msb4100155, 1911197, 17593909.
5. Raghunathan A, Reed J, Shin S, Palsson B, Daefler S. Constraint-based analysis of metabolic capacity of Salmonella typhimurium during host-pathogen interaction. BMC Syst Biol 2009, 3:38. 10.1186/1752-0509-3-38, 2678070, 19356237.
6. Raghunathan A, Price ND, Galperin MY, Makarova KS, Purvine S, Picone AF, Cherny T, Xie T, Reilly TJ, Munson RJ, Tyler RE, Akerley BJ, Smith AL, Palsson BO, Kolker E. In Silico Metabolic Model and Protein Expression of Haemophilus influenzae Strain Rd KW20 in Rich Medium. OMICS 2004, 8:25-41. 10.1089/153623104773547471, 15107235.
7. Forster J, Famili I, Fu P, Palsson BO, Nielsen J. Genome-scale reconstruction of the Saccharomyces cerevisiae metabolic network. Genome Res 2003, 13:244-253. 10.1101/gr.234503, 420374, 12566402.
8. Chavali AK, Whittemore JD, Eddy JA, Williams KT, Papin JA. Systems analysis of metabolism in the pathogenic trypanosomatid Leishmania major. Mol Syst Biol 2008, 4:177. 10.1038/msb.2008.15, 2290936, 18364711.
9. Price ND, Reed JL, Palsson BO. Genome-scale models of microbial cells: evaluating the consequences of constraints. Nat Rev Microbiol 2004, 2:886-897. 10.1038/nrmicro1023, 15494745.
10. Larsson P, Oyston PC, Chain P, Chu MC, Duffield M, Fuxelius HH, Garcia E, Halltorp G, Johansson D, Isherwood KE, Karp PD, Larsson E, Liu Y, Michell S, Prior J, Prior R, Malfatti S, Sjostedt A, Svensson K, Thompson N, Vergez L, Wagg JK, Wren BW, Lindler LE, Andersson SG, Forsman M, Titball RW. The complete genome sequence of Francisella tularensis, the causative agent of tularemia. Nat Genet 2005, 37:153-159. 10.1038/ng1499, 15640799.
11. Chamberlain RE. Evaluation of live tularemia vaccine prepared in a chemically defined medium. Applied Microbiol 1965, 13:232-235.
12. Traub A, Mager J, GROSSOWICZ N. Studies on the nutrition of Pasteurella tularensis. J Bacteriol 1955, 70:60-69. 357633, 13242527.
13. Karlsson J, Prior RG, Williams K, Lindler L, Brown KA, Chatwell N, Hjalmarsson K, Loman N, Mack KA, Pallen M, Popek M, Sandstrom G, Sjostedt A, Svensson T, Tamas I, Andersson SG, Wren BW, Oyston PC, Titball RW. Sequencing of the Francisella tularensis strain Schu 4 genome reveals the shikimate and purine metabolic pathways, targets for the construction of a rationally attenuated auxotrophic vaccine. Microb Comp Genomics 2000, 5:25-39. 10.1089/10906590050145249, 11011763.
14. Whittaker P, Day JB, Curtis SK, Fry FS. Evaluating the use of fatty acid profiles to identify Francisella tularensis. J AOAC Int 2007, 90:465-469.
15. Fleming DE, Foshay L. Studies on the physiology of virulence of Pasteurella tularensis. II. Serine deaminase and transaminase activity. J Bacteriol 1956, 71:324-327. 357797, 13306703.
16. Puchkov EO, Pinchukova VA, Ivanov SA. [The characteristics of potassium ion transport across the bacterial membranes in a vaccinal culture of Francisella tularensis]. Zh Mikrobiol Epidemiol Immunobiol 1991, 11-13.
17. Teusink B, Wiersma A, Molenaar D, Francke C, de Vos WM, Siezen RJ, Smid EJ. Analysis of growth of Lactobacillus plantarum WCFS1 on a complex medium using a genome-scale metabolic model. J Biol Chem 2006, 281:40041-40048. 10.1074/jbc.M606263200, 17062565.
18. Lee DS, Burd H, Liu J, Almaas E, Wiest O, Barabasi AL, Oltvai ZN, Kapatral V. Comparative genome-scale metabolic reconstruction and flux balance analysis of multiple Staphylococcus aureus genomes identify novel antimicrobial drug targets. J Bacteriol 2009, 191:4015-4024. 10.1128/JB.01743-08, 2698402, 19376871.
19. Santiago AE, Cole LE, Franco A, Vogel SN, Levine MM, Barry EM. Characterization of rationally attenuated Francisella tularensis vaccine strains that harbor deletions in the guaA and guaB genes. Vaccine 2009, 27:2426-2436. 10.1016/j.vaccine.2009.02.073, 2716139, 19368784.
20. Alkhuder K, Meibom KL, Dubail I, Dupuis M, Charbit A. Glutathione provides a source of cysteine essential for intracellular multiplication of Francisella tularensis. PLoS Pathog 2009, 5:e1000284. 10.1371/journal.ppat.1000284, 2629122, 19158962.
21. Pechous RD, McCarthy TR, Mohapatra NP, Soni S, Penoske RM, Salzman NH, Frank DW, Gunn JS, Zahrt TC. A Francisella tularensis Schu S4 purine auxotroph is highly attenuated in mice but offers limited protection against homologous intranasal challenge. PLoS One 2008, 3:e2487. 10.1371/journal.pone.0002487, 2429968, 18575611.
22. Maier TM, Casey MS, Becker RH, Dorsey CW, Glass EM, Maltsev N, Zahrt TC, Frank DW. Identification of Francisella tularensis Himar1-based transposon mutants defective for replication in macrophages. Infect Immun 2007, 75:5376-5389. 10.1128/IAI.00238-07, 2168294, 17682043.
23. Lindgren H, Shen H, Zingmark C, Golovliov I, Conlan W, Sjostedt A. Resistance of Francisella tularensis strains against reactive nitrogen and oxygen species with special reference to the role of KatG. Infect Immun 2007, 75:1303-1309. 10.1128/IAI.01717-06, 1828546, 17210667.
24. Raynaud C, Meibom KL, Lety MA, Dubail I, Candela T, Frapy E, Charbit A. Role of the wbt locus of Francisella tularensis in lipopolysaccharide O-antigen biogenesis and pathogenicity. Infect Immun 2007, 75:536-541. 10.1128/IAI.01429-06, 1828372, 17030571.
25. LoVullo ED, Sherrill LA, Perez LL, Pavelka MSJ. Genetic tools for highly pathogenic Francisella tularensis subsp. tularensis. Microbiology 2006, 152:3425-3435. 10.1099/mic.0.29121-0, 17074911.
26. Bakshi CS, Malik M, Regan K, Melendez JA, Metzger DW, Pavlov VM, Sellati TJ. Superoxide dismutase B gene (sodB)-deficient mutants of Francisella tularensis demonstrate hypersensitivity to oxidative stress and attenuated virulence. J Bacteriol 2006, 188:6443-6448. 10.1128/JB.00266-06, 1595384, 16923916.
27. Gil H, Platz GJ, Forestal CA, Monfett M, Bakshi CS, Sellati TJ, Furie MB, Benach JL, Thanassi DG. Deletion of TolC orthologs in Francisella tularensis identifies roles in multidrug resistance and virulence. Proc Natl Acad Sci USA 2006, 103:12897-12902. 10.1073/pnas.0602582103, 1568944, 16908853.
28. Sullivan JT, Jeffery EF, Shannon JD, Ramakrishnan G. Characterization of the siderophore of Francisella tularensis and role of fslA in siderophore production. J Bacteriol 2006, 188:3785-3795. 10.1128/JB.00027-06, 1482922, 16707671.
29. Thomas RM, Titball RW, Oyston PC, Griffin K, Waters E, Hitchen PG, Michell SL, Grice ID, Wilson JC, Prior JL. The immunologically distinct O antigens from Francisella tularensis subspecies tularensis and Francisella novicida are both virulence determinants and protective antigens. Infect Immun 2007, 75:371-378. 10.1128/IAI.01241-06, 1828428, 17074846.
30. Twine S, Bystrom M, Chen W, Forsman M, Golovliov I, Johansson A, Kelly J, Lindgren H, Svensson K, Zingmark C, Conlan W, Sjostedt A. A mutant of Francisella tularensis strain SCHU S4 lacking the ability to express a 58-kilodalton protein is attenuated for virulence and is an effective live vaccine. Infect Immun 2005, 73:8345-8352. 10.1128/IAI.73.12.8345-8352.2005, 1307091, 16299332.
31. Wang X, Ribeiro AA, Guan Z, Abraham SN, Raetz CR. Attenuated virulence of a Francisella mutant lacking the lipid A 4'-phosphatase. Proc Natl Acad Sci USA 2007, 104:4136-4141. 10.1073/pnas.0611606104, 1820721, 17360489.
32. Richards MI, Michell SL, Oyston PC. An intracellularly inducible gene involved in virulence and polyphosphate production in Francisella. J Med Microbiol 2008, 57:1183-1192. 10.1099/jmm.0.2008/001826-0, 18809544.
33. Milne TS, Michell SL, Diaper H, Wikstrom P, Svensson K, Oyston PC, Titball RW. A 55 kDa hypothetical membrane protein is an iron-regulated virulence factor of Francisella tularensis subsp. novicida U112. J Med Microbiol 2007, 56:1268-1276. 10.1099/jmm.0.47190-0, 17893160.
34. Brotcke A, Weiss DS, Kim CC, Chain P, Malfatti S, Garcia E, Monack DM. Identification of MglA-regulated genes reveals novel virulence factors in Francisella tularensis. Infect Immun 2006, 74:6642-6655. 10.1128/IAI.01250-06, 1698089, 17000729.
35. Nano FE, Zhang N, Cowley SC, Klose KE, Cheung KK, Roberts MJ, Ludu JS, Letendre GW, Meierovics AI, Stephens G, Elkins KL. A Francisella tularensis pathogenicity island required for intramacrophage growth. J Bacteriol 2004, 186:6430-6436. 10.1128/JB.186.19.6430-6436.2004, 516616, 15375123.
36. Deng K, Blick RJ, Liu W, Hansen EJ. Identification of Francisella tularensis genes affected by iron limitation. Infect Immun 2006, 74:4224-4236. 10.1128/IAI.01975-05, 1489736, 16790797.
37. Lenco J, Link M, Tambor V, Zakova J, Cerveny L, Stulik AJ. iTRAQ quantitative analysis of Francisella tularensis ssp. holarctica live vaccine strain and Francisella tularensis ssp. tularensis SCHU S4 response to different temperatures and stationary phases of growth. Proteomics 2009, 9:2875-2882. 10.1002/pmic.200700820, 19415661.
38. Becker SA, Feist AM, Mo ML, Hannum G, Palsson BO, Herrgard MJ. Quantitative prediction of cellular metabolism with constraint-based models: the COBRA Toolbox. Nat Protoc 2007, 2:727-738. 10.1038/nprot.2007.99, 17406635.
39. Gyuranecz M, Erdelyi K, Fodor L, Janosi K, Szepe B, Fuleki M, Szoke I, Denes B, Makrai L. Characterization of Francisella tularensis Strains, Comparing Their Carbon Source Utilization. Zoonoses Public Health 2009,
40. Nagle SCJ, Anderson RE, Gary ND. Chemically defined medium for the growth of Pasteurella tularensis. J Bacteriol 1960, 79:566-571. 278733, 14425793.
41. Scharer JM, Klein F, Lincoln RE. Growth and metabolism of live vaccine strain of Pasteurella tularensis. Appl Microbiol 1968, 16:855-861. 547543, 5664109.
42. Han YH, Smibert RM, Krieg NR. Wolinella recta, Wolinella curva, Bacteroides ureolyticus, and Bacteroides gracilis are microaerophiles, not anaerobes. Int J Syst Bacteriol 1991, 41:218-222. 10.1099/00207713-41-2-218, 1854636.
43. Verdoni N, Aon MA, Lebeault JM. Metabolic and energetic control of Pseudomonas mendocina growth during transitions from aerobic to oxygen-limited conditions in chemostat cultures. Appl Environ Microbiol 1992, 58:3150-3156. 183062, 1444429.
44. Munoz-Elias EJ, McKinney JD. Carbon metabolism of intracellular bacteria. Cell Microbiol 2006, 8:10-22. 10.1111/j.1462-5822.2005.00648.x, 16367862.
45. Tramonti A, De Canio M, Delany I, Scarlato V, De Biase D. Mechanisms of transcription activation exerted by GadX and GadW at the gadA and gadBC gene promoters of the glutamate-based acid resistance system in Escherichia coli. J Bacteriol 2006, 188:8118-8127. 10.1128/JB.01044-06, 1698215, 16980449.
46. Chong A, Wehrly TD, Nair V, Fischer ER, Barker JR, Klose KE, Celli J. The early phagosomal stage of Francisella tularensis determines optimal phagosomal escape and Francisella pathogenicity island protein expression. Infect Immun 2008, 76:5488-5499. 10.1128/IAI.00682-08, 2583578, 18852245.
47. Nogales J, Palsson BO, Thiele I. A genome-scale metabolic reconstruction of Pseudomonas putida KT2440: iJN746 as a cell factory. BMC Syst Biol 2008, 2:79. 10.1186/1752-0509-2-79, 2569920, 18793442.
48. Dougherty MJ, Boyd JM, Downs DM. Inhibition of fructose-1,6-bisphosphatase by aminoimidazole carboxamide ribotide prevents growth of Salmonella enterica purH mutants on glycerol. J Biol Chem 2006, 281:33892-33899. 10.1074/jbc.M604429200, 16987812.
49. Raman K, Rajagopalan P, Chandra N. Flux balance analysis of mycolic acid pathway: targets for anti-tubercular drugs. PLoS Comput Biol 2005, 1:e46. 10.1371/journal.pcbi.0010046, 1246807,1246807, 16261191.
50. Schuetz R, Kuepfer L, Sauer U. Systematic evaluation of objective functions for predicting intracellular fluxes in Escherichia coli. Mol Syst Biol 2007, 3:119. 10.1038/msb4100162, 1949037, 17625511.
51. Tamilselvam B, Daefler S. Francisella targets cholesterol-rich host cell membrane domains for entry into macrophages. J Immunol 2008, 180:8262-8271.