Lymph Node Colonization Dynamics after Oral Salmonella Typhimurium Infection in Mice

PLoS Pathogens

Volumn 9, Issue 9, 2013, Pages

  Kaiser, Patrick ^a   Slack, Emma ^a   Grant, Andrew J ^b   Hardt, Wolf Dietrich ^a   Regoes, Roland R ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

REACTIVE OXYGEN METABOLITE; BACTERIAL PROTEIN; CCR7 PROTEIN, MOUSE; CHEMOKINE RECEPTOR CCR7; CYBB PROTEIN, MOUSE; MEMBRANE PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; VIRULENCE FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL CLEARANCE; BACTERIAL COLONIZATION; BACTERIAL TRANSMISSION; CELL DIVISION; CELL MIGRATION; COLONY FORMING UNIT; CONTROLLED STUDY; INFLAMMATION; INNATE IMMUNITY; LYMPH NODE; MATHEMATICAL MODEL; MOUSE; NONHUMAN; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SALMONELLA TYPHIMURIUM; SALMONELLOSIS; TYPE III SECRETION SYSTEM; ANIMAL; BACTERIAL TRANSLOCATION; C57BL MOUSE; CECUM; COMPARATIVE STUDY; DENDRITIC CELL; DISEASE MODEL; GENETICS; GERMFREE ANIMAL; HOST PATHOGEN INTERACTION; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; MICROBIOLOGY; MUTATION; PATHOGENICITY; PHYSIOLOGY; SALMONELLA ENTERICA SUBSP. ENTERICA SEROVAR TYPHIMURIUM; SALMONELLA FOOD POISONING; VIRULENCE;

ANIMALS; BACTERIAL PROTEINS; BACTERIAL TRANSLOCATION; CECUM; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; HOST-PATHOGEN INTERACTIONS; IMMUNITY, INNATE; LYMPH NODES; MEMBRANE GLYCOPROTEINS; MICE, INBRED C57BL; MICE, KNOCKOUT; MUTATION; NADPH OXIDASE; REACTIVE OXYGEN SPECIES; RECEPTORS, CCR7; SALMONELLA FOOD POISONING; SALMONELLA TYPHIMURIUM; SPECIFIC PATHOGEN-FREE ORGANISMS; VIRULENCE; VIRULENCE FACTORS;

EID: 84884687854     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003532     Document Type: Article

References (45)

1. Haase AT, (2005) Perils at mucosal front lines for HIV and SIV and their hosts. Nat Rev Immunol 5: 783-92.
2. Shankarappa R, Margolick JB, Gange SJ, Rodrigo AG, Upchurch D, et al. (1999) Consistent viral evolutionary changes associated with the progression of human immunodeficiency virus type 1 infection. J Virol 73: 10489-502.
3. Keele BF, Giorgi EE, Salazar-Gonzalez JF, Decker JM, Pham KT, et al. (2008) Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc Natl Acad Sci U S A 105: 7552-7.
4. Schmitz JE, Kuroda MJ, Santra S, Sasseville VG, Simon MA, et al. (1999) Control of viremia in simian immunodeficiency virus infection by CD8(+) lymphocytes. Science 283: 857-860.
5. Regoes RR, Antia R, Garber DA, Silvestri G, Feinberg MB, et al. (2004) Roles of target cells and virus-specific cellular immunity in primary simian immunodeficiency virus infection. J Virol 78: 4866-4875.
6. Fernandez CS, Stratov I, De Rose R, Walsh K, Dale CJ, et al. (2005) Rapid viral escape at an immunodominant simian-human immunodeficiency virus cytotoxic T-lymphocyte epitope exacts a dramatic fitness cost. J Virol 79: 5721-31.
7. Mandl JN, Regoes RR, Garber DA, Feinberg MB, (2007) Estimating the effectiveness of SIV specific CD8+ T cells from the dynamics of viral immune escape. J Virol 81: 11982-11991.
8. Goonetilleke N, Liu MKP, Salazar-Gonzalez JF, Ferrari G, Giorgi E, et al. (2009) The first T cell response to transmitted/founder virus contributes to the control of acute viremia in HIV-1 infection. J Exp Med 206: 1253-72.
9. Lay MD, Petravic J, Gordon SN, Engram J, Silvestri G, et al. (2009) Is the gut the major source of virus in early simian immunodeficiency virus infection? J Virol 83: 7517-23.
10. Baccam P, Beauchemin C, Macken CA, Hayden FG, Perelson AS, (2006) Kinetics of influenza A virus infection in humans. J Virol 80: 7590-9.
11. Bull RA, Luciani F, McElroy K, Gaudieri S, Pham ST, et al. (2011) Sequential bottlenecks drive viral evolution in early acute hepatitis C virus infection. PLoS Pathog 7: e1002243.
12. Meynell GG, (1957) The applicability of the hypothesis of independent action to fatal infections in mice given Salmonella typhimurium by mouth. J Gen Microbiol 16: 396-404.
13. Meynell GG, Stocker BA, (1957) Some hypotheses on the aetiology of fatal infections in partially resistant hosts and their application to mice challenged with Salmonella paratyphi-B or Salmonella typhimurium by intraperitoneal injection. J Gen Microbiol 16: 38-58.
14. Moxon ER, Murphy PA, (1978) Haemophilus inuenzae bacteremia and meningitis resulting from survival of a single organism. Proc Natl Acad Sci USA 75: 1534-6.
15. Levin BR, Lipsitch M, Bonhoeffer S, (1999) Population biology, evolution, and infectious disease: convergence and synthesis. Science 283: 806-9.
16. Margolis E, Levin BR, (2007) Within-host evolution for the invasiveness of commensal bacteria: an experimental study of bacteremias resulting from Haemophilus inuenzae nasal carriage. J Infect Dis 196: 1068-75.
17. Barnes PD, Bergman MA, Mecsas J, Isberg RR, (2006) Yersinia pseudotuberculosis disseminates directly from a replicating bacterial pool in the intestine. J Exp Med 203: 1591-601.
18. Grant AJ, Restif O, McKinley TJ, Sheppard M, Maskell DJ, et al. (2008) Modelling within-host spatiotemporal dynamics of invasive bacterial disease. PLoS Biol 6: e74.
19. Barthel M, Hapfelmeier S, Quintanilla-Martinez L, Kremer M, Rohde M, et al. (2003) Pretreatment of mice with streptomycin provides a Salmonella enterica serovar Typhimurium colitis model that allows analysis of both pathogen and host. Infect Immun 71: 2839-58.
20. Kaiser P, Diard M, Stecher B, Hardt WD, (2012) The streptomycin mouse model for Salmonella diarrhea: functional analysis of the microbiota, the pathogen's virulence factors, and the host's mucosal immune response. Immunol Rev 245: 56-83.
21. Kaniga K, Bossio JC, Galán JE, (1994) The Salmonella typhimurium invasion genes invF and invG encode homologues of the AraC and PulD family of proteins. Mol Microbiol 13: 555-68.
22. Hapfelmeier S, Stecher B, Barthel M, Kremer M, Müller AJ, et al. (2005) The Salmonella pathogenicity island (SPI)-2 and SPI-1 type III secretion systems allow Salmonella serovar typhimurium to trigger colitis via MyD88-dependent and MyD88-independent mechanisms. J Immunol 174: 1675-85.
23. Martinoli C, Chiavelli A, Rescigno M, (2007) Entry route of Salmonella typhimurium directs the type of induced immune response. Immunity 27: 975-84.
24. Ackermann M, Stecher B, Freed NE, Songhet P, Hardt WD, et al. (2008) Self-destructive cooperation mediated by phenotypic noise. Nature 454: 987-90.
25. Macpherson AJ, Uhr T, (2004) Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science 303: 1662-5.
26. Hapfelmeier S, Müller AJ, Stecher B, Kaiser P, Barthel M, et al. (2008) Microbe sampling by mucosal dendritic cells is a discrete, MyD88-independent step in DeltainvG S. Typhimurium colitis. J Exp Med 205: 437-50.
27. Müller AJ, Kaiser P, Dittmar KEJ, Weber TC, Haueter S, et al. (2012) Salmonella gut invasion involves TTSS-2-dependent epithelial traversal, basolateral exit, and uptake by epithelium-sampling lamina propria phagocytes. Cell Host Microbe 11: 19-32.
28. Förster R, Schubel A, Breitfeld D, Kremmer E, Renner-Müller I, et al. (1999) CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell 99: 23-33.
29. Niess JH, Brand S, Gu X, Landsman L, Jung S, et al. (2005) CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science 307: 254-8.
30. Diehl GE, Longman RS, Zhang JX, Breart B, Galan C, et al. (2013) Microbiota restricts traffcking of bacteria to mesenteric lymph nodes by CX(3)CR1(hi) cells. Nature 494: 116-20.
31. Helaine S, Thompson JA, Watson KG, Liu M, Boyle C, et al. (2010) Dynamics of intracellular bacterial replication at the single cell level. Proc Natl Acad Sci USA 107: 3746-51.
32. Brown SP, Cornell SJ, Sheppard M, Grant AJ, Maskell DJ, et al. (2006) Intracellular demography and the dynamics of Salmonella enterica infections. PLoS Biol 4: e349.
33. Gog JR, Murcia A, Osterman N, Restif O, McKinley TJ, et al. (2012) Dynamics of Salmonella infection of macrophages at the single cell level. J R Soc Interface 9: 2696-707.
34. Druett HA, (1952) Bacterial invasion. Nature 170: 288.
35. Halvorson HO, (1935) The effect of chance on the mortality of experimentally infected animals. J Bact 30: 330-331.
36. Levin BR, Bull JJ, (1994) Short-sighted evolution and the virulence of pathogenic microorganisms. Trends Microbiol 2: 76-81.
37. Hoiseth SK, Stocker BA, (1981) Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 291: 238-9.
38. Hapfelmeier S, Ehrbar K, Stecher B, Barthel M, Kremer M, et al. (2004) Role of the Salmonella pathogenicity island 1 effector proteins SipA, SopB, SopE, and SopE2 in Salmonella enterica subspecies 1 serovar Typhimurium colitis in streptomycin-pretreated mice. Infect Immun 72: 795-809.
39. Suar M, Periaswamy B, Songhet P, Misselwitz B, Müller A, et al. (2009) Accelerated type III secretion system 2-dependent enteropathogenesis by a Salmonella enterica serovar enteritidis PT4/6 strain. Infect Immun 77: 3569-77.
40. Pollock JD, Williams DA, Gifford MA, Li LL, Du X, et al. (1995) Mouse model of X-linked chronic granulomatous disease, an inherited defect in phagocyte superoxide production. Nat Genet 9: 202-9.
41. Karlin S, Taylor HM (1975) A first course in stochastic processes, Academic Press, chapter 4. Second edition.
42. Debnath L (2012) Nonlinear Partial Differential Equations for Scientists and Engineers. Birkhäuser Boston, third edition.
43. Read T, Cressie N (1988) Goodness-of-Fit Statistics for Discrete Multivariate Data. Springer Series in Statistics. Springer.
44. R Development Core Team (2010) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. URL http://www.R-project.org. ISBN 3-900051-07-0.
45. Pineda-Krch M (2010) GillespieSSA: a stochastic simulation package for R.