Dynamics of T Cell, Antigen-presenting Cell, and Pathogen Interactions During Recall Responses in the Lymph Node

Overview

Journal Immunity

Publisher Cell Press

Specialty Allergy & Immunology

Date 2009 Aug 25

PMID 19699173

Citations 80

Authors

Tatyana Chtanova

Seong-Ji Han

Marie Schaeffer

Giel G van Dooren

Paul Herzmark

Boris Striepen

Ellen A Robey

Affiliations

Soon will be listed here.

Abstract

Memory T cells circulate through lymph nodes where they are poised to respond rapidly upon re-exposure to a pathogen; however, the dynamics of memory T cell, antigen-presenting cell, and pathogen interactions during recall responses are largely unknown. We used a mouse model of infection with the intracellular protozoan parasite, Toxoplasma gondii, in conjunction with two-photon microscopy, to address this question. After challenge, memory T cells migrated more rapidly than naive T cells, relocalized toward the subcapsular sinus (SCS) near invaded macrophages, and engaged in prolonged interactions with infected cells. Parasite invasion of T cells occurred by direct transfer of the parasite from the target cell into the T cell and corresponded to an antigen-specific increase in the rate of T cell invasion. Our results provide insight into cellular interactions during recall responses and suggest a mechanism of pathogen subversion of the immune response.

Citing Articles

Lymph Node-on-Chip Technology: Cutting-Edge Advances in Immune Microenvironment Simulation.

Wang Q, Yang Y, Chen Z, Li B, Niu Y, Li X Pharmaceutics. 2024; 16(5).

PMID: 38794327 PMC: 11124897. DOI: 10.3390/pharmaceutics16050666.

CD169 Expression in Lymph Nodes is Associated with Increased Infiltration of CD8 T Cells in Tumors: A Systematic Review and Meta-Analysis.

Wang Y, Wu X, Chen J J Immunol Res. 2024; 2024:8873767.

PMID: 38250298 PMC: 10798834. DOI: 10.1155/2024/8873767.

Animal Models for Toxoplasma gondii Infection.

Subauste C, Hubal A Curr Protoc. 2023; 3(9):e871.

PMID: 37695167 PMC: 10621533. DOI: 10.1002/cpz1.871.

Resolvin D1 prevents injurious neutrophil swarming in transplanted lungs.

Li W, Shepherd H, Terada Y, Shay A, Bery A, Gelman A Proc Natl Acad Sci U S A. 2023; 120(31):e2302938120.

PMID: 37487095 PMC: 10400944. DOI: 10.1073/pnas.2302938120.

Toxoplasma gondii Dissemination in the Brain Is Facilitated by Infiltrating Peripheral Immune Cells.

Schneider C, Velez D, Orchanian S, Shallberg L, Agalliu D, Hunter C mBio. 2022; 13(6):e0283822.

PMID: 36445695 PMC: 9765297. DOI: 10.1128/mbio.02838-22.

References

Fossum S . The architecture of rat lymph nodes. IV. Distribution of ferritin and colloidal carbon in the draining lymph nodes after foot-pad injection. Scand J Immunol. 1980; 12(5):433-41. DOI: 10.1111/j.1365-3083.1980.tb00087.x. View

Piguet V, Sattentau Q . Dangerous liaisons at the virological synapse. J Clin Invest. 2004; 114(5):605-10. PMC: 514595. DOI: 10.1172/JCI22812. View

Carrasco Y, Batista F . B cells acquire particulate antigen in a macrophage-rich area at the boundary between the follicle and the subcapsular sinus of the lymph node. Immunity. 2007; 27(1):160-71. DOI: 10.1016/j.immuni.2007.06.007. View

Kasper L, Courret N, Darche S, Luangsay S, Mennechet F, Minns L . Toxoplasma gondii and mucosal immunity. Int J Parasitol. 2004; 34(3):401-9. DOI: 10.1016/j.ijpara.2003.11.023. View

Lambert H, Hitziger N, Dellacasa I, Svensson M, Barragan A . Induction of dendritic cell migration upon Toxoplasma gondii infection potentiates parasite dissemination. Cell Microbiol. 2006; 8(10):1611-23. DOI: 10.1111/j.1462-5822.2006.00735.x. View

Phan T, Grigorova I, Okada T, Cyster J . Subcapsular encounter and complement-dependent transport of immune complexes by lymph node B cells. Nat Immunol. 2007; 8(9):992-1000. DOI: 10.1038/ni1494. View

Boissonnas A, Fetler L, Zeelenberg I, Hugues S, Amigorena S . In vivo imaging of cytotoxic T cell infiltration and elimination of a solid tumor. J Exp Med. 2007; 204(2):345-56. PMC: 2118741. DOI: 10.1084/jem.20061890. View

Witt C, Raychaudhuri S, Schaefer B, Chakraborty A, Robey E . Directed migration of positively selected thymocytes visualized in real time. PLoS Biol. 2005; 3(6):e160. PMC: 1088277. DOI: 10.1371/journal.pbio.0030160. View

Moudy R, Manning T, Beckers C . The loss of cytoplasmic potassium upon host cell breakdown triggers egress of Toxoplasma gondii. J Biol Chem. 2001; 276(44):41492-501. DOI: 10.1074/jbc.M106154200. View

10.

Persson E, Mpobela Agnarson A, Lambert H, Hitziger N, Yagita H, Chambers B . Death receptor ligation or exposure to perforin trigger rapid egress of the intracellular parasite Toxoplasma gondii. J Immunol. 2007; 179(12):8357-65. DOI: 10.4049/jimmunol.179.12.8357. View

11.

Szakal A, Holmes K, Tew J . Transport of immune complexes from the subcapsular sinus to lymph node follicles on the surface of nonphagocytic cells, including cells with dendritic morphology. J Immunol. 1983; 131(4):1714-27. View

12.

Labruyere E, Lingnau M, Mercier C, Sibley L . Differential membrane targeting of the secretory proteins GRA4 and GRA6 within the parasitophorous vacuole formed by Toxoplasma gondii. Mol Biochem Parasitol. 1999; 102(2):311-24. DOI: 10.1016/s0166-6851(99)00092-4. View

13.

Bousso P . T-cell activation by dendritic cells in the lymph node: lessons from the movies. Nat Rev Immunol. 2009; 8(9):675-84. DOI: 10.1038/nri2379. View

14.

Dzierszinski F, Pepper M, Stumhofer J, LaRosa D, Wilson E, Turka L . Presentation of Toxoplasma gondii antigens via the endogenous major histocompatibility complex class I pathway in nonprofessional and professional antigen-presenting cells. Infect Immun. 2007; 75(11):5200-9. PMC: 2168266. DOI: 10.1128/IAI.00954-07. View

15.

Khanna K, McNamara J, Lefrancois L . In situ imaging of the endogenous CD8 T cell response to infection. Science. 2007; 318(5847):116-20. PMC: 2846662. DOI: 10.1126/science.1146291. View

16.

Mrass P, Takano H, Ng L, Daxini S, Lasaro M, Iparraguirre A . Random migration precedes stable target cell interactions of tumor-infiltrating T cells. J Exp Med. 2006; 203(12):2749-61. PMC: 2118164. DOI: 10.1084/jem.20060710. View

17.

Junt T, Moseman E, Iannacone M, Massberg S, Lang P, Boes M . Subcapsular sinus macrophages in lymph nodes clear lymph-borne viruses and present them to antiviral B cells. Nature. 2007; 450(7166):110-4. DOI: 10.1038/nature06287. View

18.

Andrade R, Wessendarp M, Gubbels M, Striepen B, Subauste C . CD40 induces macrophage anti-Toxoplasma gondii activity by triggering autophagy-dependent fusion of pathogen-containing vacuoles and lysosomes. J Clin Invest. 2006; 116(9):2366-77. PMC: 1555650. DOI: 10.1172/JCI28796. View

19.

Plattner F, Soldati-Favre D . Hijacking of host cellular functions by the Apicomplexa. Annu Rev Microbiol. 2008; 62:471-87. DOI: 10.1146/annurev.micro.62.081307.162802. View

20.

Boothroyd J, Dubremetz J . Kiss and spit: the dual roles of Toxoplasma rhoptries. Nat Rev Microbiol. 2007; 6(1):79-88. DOI: 10.1038/nrmicro1800. View