From Entry to Early Dissemination- Initial Encounter With Its Host

Overview

Journal Front Cell Infect Microbiol

Specialties Cell Biology
Infectious Diseases
Microbiology

Date 2019 Mar 21

PMID 30891433

Citations 35

Authors

Estefania Delgado Betancourt

Benjamin Hamid

Benedikt T Fabian

Christian Klotz

Susanne Hartmann

Frank Seeber

Affiliations

Soon will be listed here.

Abstract

is a zoonotic intracellular parasite, able to infect any warm-blooded animal via ingestion of infective stages, either contained in tissue cysts or oocysts released into the environment. While immune responses during infection are well-studied, there is still limited knowledge about the very early infection events in the gut tissue after infection via the oral route. Here we briefly discuss differences in host-specific responses following infection with oocyst-derived sporozoites vs. tissue cyst-derived bradyzoites. A focus is given to innate intestinal defense mechanisms and early immune cell events that precede s dissemination in the host. We propose stem cell-derived intestinal organoids as a model to study early events of natural host-pathogen interaction. These offer several advantages such as live cell imaging and transcriptomic profiling of the earliest invasion processes. We additionally highlight the necessity of an appropriate large animal model reflecting human infection more closely than conventional infection models, to study the roles of dendritic cells and macrophages during early infection.

Citing Articles

Limited value of current and new predicted oocyst-specific proteins of for source-attributing serology.

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Recombinant SAG2A Protein from Modulates Immune Profile and Induces Metabolic Changes Associated with Reduced Tachyzoite Infection in Peritoneal Exudate Cells from Susceptible C57BL/6 Mice.

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CRISPR-based functional profiling of the Toxoplasma gondii genome during acute murine infection.

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Early immune response to lineage III isolates of different virulence phenotype.

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References

Kanatani S, Uhlen P, Barragan A . Infection by Toxoplasma gondii Induces Amoeboid-Like Migration of Dendritic Cells in a Three-Dimensional Collagen Matrix. PLoS One. 2015; 10(9):e0139104. PMC: 4583262. DOI: 10.1371/journal.pone.0139104. View

Cohen S, Denkers E . The gut mucosal immune response to Toxoplasma gondii. Parasite Immunol. 2014; 37(3):108-17. DOI: 10.1111/pim.12164. View

Nau J, Eller S, Wenning J, Spekker-Bosker K, Schroten H, Schwerk C . Experimental Porcine Infection as a Representative Model for Human Toxoplasmosis. Mediators Inflamm. 2017; 2017:3260289. PMC: 5572617. DOI: 10.1155/2017/3260289. View

Jennes M, De Craeye S, Devriendt B, Dierick K, Dorny P, Cox E . Strain- and Dose-Dependent Reduction of Burden in Pigs Is Associated with Interferon-Gamma Production by CD8 Lymphocytes in a Heterologous Challenge Model. Front Cell Infect Microbiol. 2017; 7:232. PMC: 5462990. DOI: 10.3389/fcimb.2017.00232. View

Roach J, Glusman G, Rowen L, Kaur A, Purcell M, Smith K . The evolution of vertebrate Toll-like receptors. Proc Natl Acad Sci U S A. 2005; 102(27):9577-82. PMC: 1172252. DOI: 10.1073/pnas.0502272102. View

Heo I, Dutta D, Schaefer D, Iakobachvili N, Artegiani B, Sachs N . Modelling Cryptosporidium infection in human small intestinal and lung organoids. Nat Microbiol. 2018; 3(7):814-823. PMC: 6027984. DOI: 10.1038/s41564-018-0177-8. View

Barragan A, Brossier F, Sibley L . Transepithelial migration of Toxoplasma gondii involves an interaction of intercellular adhesion molecule 1 (ICAM-1) with the parasite adhesin MIC2. Cell Microbiol. 2005; 7(4):561-8. DOI: 10.1111/j.1462-5822.2005.00486.x. View

Lu Y, Dong H, Feng Y, Wang K, Jiang Y, Zhang L . Avirulence and lysozyme secretion in Paneth cells after infection of BALB/c mice with oocysts of Toxoplasma gondii strains TgCatCHn2 (ToxoDB#17) and TgCatCHn4 (ToxoDB#9). Vet Parasitol. 2018; 252:1-8. DOI: 10.1016/j.vetpar.2018.01.016. View

Mair K, Sedlak C, Kaser T, Pasternak A, Levast B, Gerner W . The porcine innate immune system: an update. Dev Comp Immunol. 2014; 45(2):321-43. PMC: 7103209. DOI: 10.1016/j.dci.2014.03.022. View

10.

Zhang D, Zhang G, Hayden M, Greenblatt M, Bussey C, Flavell R . A toll-like receptor that prevents infection by uropathogenic bacteria. Science. 2004; 303(5663):1522-6. DOI: 10.1126/science.1094351. View

11.

Coombes J, Charsar B, Han S, Halkias J, Chan S, Koshy A . Motile invaded neutrophils in the small intestine of Toxoplasma gondii-infected mice reveal a potential mechanism for parasite spread. Proc Natl Acad Sci U S A. 2013; 110(21):E1913-22. PMC: 3666704. DOI: 10.1073/pnas.1220272110. View

12.

Blader I, Coleman B, Chen C, Gubbels M . Lytic Cycle of Toxoplasma gondii: 15 Years Later. Annu Rev Microbiol. 2015; 69:463-85. PMC: 4659696. DOI: 10.1146/annurev-micro-091014-104100. View

13.

Lilue J, Muller U, Steinfeldt T, Howard J . Reciprocal virulence and resistance polymorphism in the relationship between Toxoplasma gondii and the house mouse. Elife. 2013; 2:e01298. PMC: 3810784. DOI: 10.7554/eLife.01298. View

14.

Etheridge R, Alaganan A, Tang K, Lou H, Turk B, Sibley L . The Toxoplasma pseudokinase ROP5 forms complexes with ROP18 and ROP17 kinases that synergize to control acute virulence in mice. Cell Host Microbe. 2014; 15(5):537-50. PMC: 4086214. DOI: 10.1016/j.chom.2014.04.002. View

15.

Raetz M, Hwang S, Wilhelm C, Kirkland D, Benson A, Sturge C . Parasite-induced TH1 cells and intestinal dysbiosis cooperate in IFN-γ-dependent elimination of Paneth cells. Nat Immunol. 2012; 14(2):136-42. PMC: 3552073. DOI: 10.1038/ni.2508. View

16.

van Helden S, van den Dries K, Oud M, Raymakers R, Netea M, van Leeuwen F . TLR4-mediated podosome loss discriminates gram-negative from gram-positive bacteria in their capacity to induce dendritic cell migration and maturation. J Immunol. 2009; 184(3):1280-91. DOI: 10.4049/jimmunol.0900764. View

17.

Clevers H, Bevins C . Paneth cells: maestros of the small intestinal crypts. Annu Rev Physiol. 2013; 75:289-311. DOI: 10.1146/annurev-physiol-030212-183744. View

18.

Fritz H, Bowyer P, Bogyo M, Conrad P, Boothroyd J . Proteomic analysis of fractionated Toxoplasma oocysts reveals clues to their environmental resistance. PLoS One. 2012; 7(1):e29955. PMC: 3261165. DOI: 10.1371/journal.pone.0029955. View

19.

Guiton P, Sagawa J, Fritz H, Boothroyd J . An in vitro model of intestinal infection reveals a developmentally regulated transcriptome of Toxoplasma sporozoites and a NF-κB-like signature in infected host cells. PLoS One. 2017; 12(3):e0173018. PMC: 5376300. DOI: 10.1371/journal.pone.0173018. View

20.

Dubey J . Oocyst shedding by cats fed isolated bradyzoites and comparison of infectivity of bradyzoites of the VEG strain Toxoplasma gondii to cats and mice. J Parasitol. 2001; 87(1):215-9. DOI: 10.1645/0022-3395(2001)087[0215:OSBCFI]2.0.CO;2. View