Model of hostpathogen interaction dynamics links in vivo optical imaging and immune responses

Infection and Immunity

Volumn 85, Issue 1, 2017, Pages

  Ale, Angelique ^a   Crepin, Valerie F ^a   Collins, James W ^a   Constantinou, Nicholas ^a   Habibzay, Maryam ^a   Babtie, Ann C ^a   Frankel, Gad ^a   Stumpf, Michael P H ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Antibiotic therapy; Bioluminescent bacteria; Citrobacter rodentium; Dynamic modeling; EspO mutant; In vivo imaging

Indexed keywords

CHLORAMPHENICOL; CIPROFLOXACIN; ANTIINFECTIVE AGENT; ESCHERICHIA COLI PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBIOTIC THERAPY; ARTICLE; BACTERIAL IMMUNITY; CITROBACTER RODENTIUM; CONTROLLED STUDY; DISEASE COURSE; ENTEROBACTERIACEAE INFECTION; ENTEROPATHOGENIC ESCHERICHIA COLI; FEMALE; FLUORESCENCE IMAGING; HOST PATHOGEN INTERACTION; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IN VIVO STUDY; MOUSE; MOUSE MODEL; NONHUMAN; OPTICAL TOMOGRAPHY; PRIORITY JOURNAL; X-RAY COMPUTED TOMOGRAPHY; ANIMAL; C57BL MOUSE; COLON; DISEASE MODEL; DRUG EFFECTS; ENTEROBACTERIACEAE INFECTIONS; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; PHYSIOLOGY; PROCEDURES;

ANIMALS; ANTI-BACTERIAL AGENTS; CITROBACTER RODENTIUM; COLON; DISEASE MODELS, ANIMAL; ENTEROBACTERIACEAE INFECTIONS; ENTEROPATHOGENIC ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FEMALE; HOST-PATHOGEN INTERACTIONS; MICE; MICE, INBRED C57BL; OPTICAL IMAGING; TOMOGRAPHY, X-RAY COMPUTED;

EID: 85009083762     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00606-16     Document Type: Article

References (40)

1. Chen HD, Frankel G. 2005. Enteropathogenic Escherichia coli: unravelling pathogenesis. FEMS Microbiol Rev 29:83-98. https://doi.org/10.1016/j.femsre.2004.07.002.
2. Wong AR, Pearson JS, Bright MD, Munera D, Robinson KS, Lee SF, Frankel G, Hartland EL. 2011. Enteropathogenic and enterohaemorrhagic Escherichia coli: even more subversive elements. Mol Microbiol 80: 1420-1438. https://doi.org/10.1111/j.1365-2958.2011.07661.x.
3. Hemrajani C, Berger CN, Robinson KS, Marchès O, Mousnier A, Frankel G. 2010 NleH effectors interact with Bax inhibitor-1 to block apoptosis during enteropathogenic Escherichia coli infection. Proc Natl Acad Sci U S A 107:3129-3134. https://doi.org/10.1073/pnas.0911609106.
4. Pearson JS, Giogha C, Ong SY, Kennedy CL, Kelly M, Robinson KS, Lung TW, Mansell A, Riedmaier P, Oates CV, Zaid A, Mühlen S, Crepin VF, Marches O, Ang CS, Williamson NA, O'Reilly LA, Bankovacki A, Nachbur U, Infusini G, Webb AI, Silke J, Strasser A, Frankel G, Hartland EL. 2013. A type III effector antagonizes death receptor signalling during bacterial gut infection. Nature 501:247-251. https://doi.org/10.1038/nature12524.
5. Li S, Zhang L, Yao Q, Li L, Dong N, Rong J, Gao W, Ding X, Sun L, Chen X, Chen S, Shao F. 2013. Pathogen blocks host death receptor signalling by arginine GlcNAcylation of death domains. Nature 501:242-246. https://doi.org/10.1038/nature12436.
6. Collins JW, Keeney KM, Crepin VF, Rathinam VAK, Fitzgerald KA, Finlay BB, Frankel G. 2014. Citrobacter rodentium: infection, inflammation and the microbiota. Nat Rev Microbiol 12:612-623. https://doi.org/10.1038/nrmicro3315.
7. Basu R, O'Quinn DB, Silberger DJ, Schoeb TR, Fouser L, Ouyang W, Hatton RD, Weaver CT. 2012. Th22 cells are an important source of IL-22 for host protection against enteropathogenic bacteria. Immunity 37: 1061-1075. https://doi.org/10.1016/j.immuni.2012.08.024.
8. Zheng Y, Valdez PA, Danilenko DM, Hu Y, Sa SM, Gong Q, Abbas AR, Modrusan Z, Ghilardi N, de Sauvage FJ, Ouyang W. 2008. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat Med 14:282-289. https://doi.org/10.1038/nm1720.
9. Hoffmann C, Hill DA, Minkah N, Kirn T, Troy A, Artis D, Bushman F. 2009. Community-wide response of the gut microbiota to enteropathogenic Citrobacter rodentium infection revealed by deep sequencing. Infect Immun 77:4668-4678. https://doi.org/10.1128/IAI.00493-09.
10. Willing BP, Vacharaksa A, Croxen M, Thanachayanont T, Finlay BB. 2011. Altering host resistance to infections through microbial transplantation. PLoS One 6:e26988. https://doi.org/10.1371/journal.pone.0026988.
11. Ivanov II, Atarashi K, Manel N, Brodie EL, Shima T, Karaoz U, Wei D, Goldfarb KC, Santee CA, Lynch SV, Tanoue T, Imaoka A, Itoh K, Takeda K, Umesaki Y, Honda K, Littman DR. 2009. Induction of intestinal TH17 cells by segmented filamentous bacteria. Cell 139:485-498. https://doi.org/10.1016/j.cell.2009.09.033.
12. Kamada N, Sakamoto K, Seo SU, Zeng MY, Kim YG, Cascalho M, Vallance BA, Puente JL, Núñez G. 2015. Humoral immunity in the gut selectively targets phenotypically virulent attaching-and-effacing bacteria for intraluminal elimination. Cell Host Microbe 17:617-627. https://doi.org/10.1016/j.chom.2015.04.001.
13. Wiles S, Robertson BD, Frankel G, Kerton A. 2009. Bioluminescent monitoring of in vivo colonization and clearance dynamics by light-emitting bacteria. Methods Mol Biol 574:137-153. https://doi.org/10.1007/978-1-60327-321-3_12.
14. Wiles S, Pickard KM, Peng K, MacDonald TT, Frankel G. 2006. In vivo bioluminescence imaging of the murine pathogen citrobacter rodentium. Infect Immun 74:5391-5396. https://doi.org/10.1128/IAI.00848-06.
15. Hall LJ, Murphy CT, Hurley G, Quinlan A, Shanahan F, Nally K, Melgar S. 2013 Natural killer cells protect against mucosal and systemic infection with the enteric pathogen citrobacter rodentium. Infect Immun 81: 460-469. https://doi.org/10.1128/IAI.00953-12.
16. Kherlopian AR, Song T, Duan Q, Neimark MA, Po MJ, Gohagan JK, Laine AF. 2008. A review of imaging techniques for systems biology. BMC Syst Biol 2:74. https://doi.org/10.1186/1752-0509-2-74.
17. Ntziachristos V. 2010. Going deeper than microscopy: the optical imag-ing frontier in biology. Nat Methods 7:603-614. https://doi.org/10.1038/nmeth.1483.
18. Mei Y, Abedi V, Carbo A, Zhang X, Lu P, Philipson C, Hontecillas R, Hoops S, Liles N, Bassaganya-Riera J. 2015. Multiscale modeling of mucosal immune responses. BMC Bioinformatics 16(Suppl 12):S2. https://doi.org/10.1186/1471-2105-16-S14-S2.
19. Wendelsdorf KV, Alam M, Bassaganya-Riera J, Bisset K, Eubank S, Hontecillas R, Hoops S, Marathe M. 2012. ENteric Immunity SImulator: a tool for in silico study of gastroenteric infections. IEEE Trans Nanobioscience 11:273-288. https://doi.org/10.1109/TNB.2012.2211891.
20. Kirk PD, Babtie AC, Stumpf MP. 2015. Systems biology (un)certainties. Science 350:386-388. https://doi.org/10.1126/science.aac9505.
21. Hastings WK. 1970. Monte Carlo sampling methods using Markov chains and their applications. Biometrika 57:97-109. https://doi.org/10.1093/biomet/57.1.97.
22. Wilkinson DJ. 2012. Stochastic modelling for systems biology. CRC Press, Boca Raton, FL.
23. Rasmussen CE, Williams CKI. 2006. Gaussian processes for machine learning. MIT Press, Cambridge, MA.
24. Kirk PD, Stumpf MP. 2009. Gaussian process regression bootstrapping: exploring the effects of uncertainty in time course data. Bioinformatics 25:1300-1306. https://doi.org/10.1093/bioinformatics/btp139.
25. Liepe J, Filippi S, Komorowski M, Stumpf MP. 2013. Maximizing the information content of experiments in systems biology. PLoS Comput Biol 9:e1002888. https://doi.org/10.1371/journal.pcbi.1002888.
26. Silk D, Kirk PD, Barnes CP, Toni T, Stumpf MP. 2014. Model selection in systems biology depends on experimental design. PLoS Comput Biol 10:e1003650. https://doi.org/10.1371/journal.pcbi.1003650.
27. Lebeis SL, Bommarius B, Parkos CA, Sherman MA, Kalman D. 2007. TLR signaling mediated by MyD88 is required for a protective innate immune response by neutrophils to citrobacter rodentium. J Immunol 179:566-577. https://doi.org/10.4049/jimmunol.179.1.566.
28. + T cells in immunity to infection by the attaching and effacing pathogen citrobacter rodentium. Infect Immun 71:5077-5086. https://doi.org/10.1128/IAI.71.9.5077-5086.2003.
29. Ogawa M, Fujita Y, Yoshikawa Y, Nagai T, Koyama T, Nagai S, Lange A, Fässler R, Sasakawa C. 2009. Bacteria hijack integrin-linked kinase to stabilize focal adhesions and block cell detachment. Nature 459: 578-582. https://doi.org/10.1038/nature07952.
30. Morita-Ishihara T, Miura M, Iyoda S, Izumiya H, Watanabe H, Ohnishi M, Terajima J. 2013. EspO1-2 regulates EspM2-mediated RhoA activity to stabilize formation of focal adhesions in enterohemorrhagic Escherichia coli-infected host cells. PLoS One 8:e55960. https://doi.org/10.1371/journal.pone.0055960.
31. Crepin VF, Habibzay M, Glegola-Madejska I, Guenot M, Collins JW, Frankel G. 2015. Tir triggers expression of CXCL1 in enterocytes and neutrophil recruitment during Citrobacter rodentium infection. Infect Immun 83:3342-3354. https://doi.org/10.1128/IAI.00291-15.
32. Collins JW, Akin AR, Kosta A, Zhang N, Tangney M, Francis KP, Frankel G. 2012 Pre-treatment with Bifidobacterium breve UCC2003 modulates Citrobacter rodentium-induced colonic inflammation and organ specificity. Microbiology 158:2826-2834. https://doi.org/10.1099/mic.0.060830-0.
33. Ale A, Ermolayev V, Herzog E, Cohrs C, Hrabe de Angelis M, Ntziachristos V. 2012. FMT-XCT: in vivo animal studies with hybrid fluorescence molecular tomography-X-ray computed tomography. Nat Methods 9:615-620. https://doi.org/10.1038/nmeth.2014.
34. Cronin M, Akin AR, Collins SA, Meganck J, Kim JB, Baban CK, Joyce SA, van Dam GM, Zhang N, van Sinderen D, O'Sullivan GC, Kasahara N, Gahan CG, Francis KP, Tangney M. 2012. High resolution in vivo bioluminescent imaging for the study of bacterial tumour targeting, PLoS One 7:e30940. https://doi.org/10.1371/journal.pone.0030940.
35. Fallahi-Sichani M, El-Kebir M, Marino S, Kirschner DE, Linderman JJ. 2011. Multiscale computational modeling reveals a critical role for TNF-α receptor 1 dynamics in tuberculosis granuloma formation. J Immunol 186:3472-3483. https://doi.org/10.4049/jimmunol.1003299.
36. Wiles S, Clare S, Harker J, Huett A, Young D, Dougan G, Frankel G. 2004. Organ specificity, colonization and clearance dynamics in vivo following oral challenges with the murine pathogen citrobacter rodentium. Cell Microbiol 6:963-972. https://doi.org/10.1111/j.1462-5822.2004.00414.x.
37. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97:6640-6645. https://doi.org/10.1073/pnas.120163297.
38. Dziva F, Vlisidou I, Crepin VF, Wallis TS, Frankel G, Stevens MP. 2007. Vaccination of calves with EspA, a key colonisation factor of Escherichia coli O157:H7, induces antigen-specific humoral responses but does not confer protection against intestinal colonisation. Vet Microbiol 123: 254-261. https://doi.org/10.1016/j.vetmic.2007.02.016.
39. Collins JW, Meganck JA, Kuo C, Francis KP, Frankel G. 2013. 4D multimodality imaging of Citrobacter rodentium infections in mice. J Vis Exp 78:50450. https://doi.org/10.3791/50450.
40. Rasmussen CE, Nickisch H. 2010. Gaussian processes for machine learning (GPML) toolbox. J Mach Learn Res 11:3011-3015.