Splenic Priming of Virus-specific CD8 T Cells Following Influenza Virus Infection

Overview

Journal J Virol

Publisher American Society for Microbiology

Date 2013 Feb 8

PMID 23388712

Citations 19

Authors

Damian L Turner

Kara L Bickham

Donna L Farber

Leo Lefrancois

Affiliations

Soon will be listed here.

Abstract

In healthy individuals, influenza virus (IAV) infection generally remains localized to the epithelial cells of the respiratory tract. Previously, IAV-specific effector CD8 T cells found systemically during the course of IAV infection were thought to have been primed in lung-draining lymph nodes with subsequent migration to other tissues. However, little is known about whether other lymphoid sites participate in the generation of virus-specific CD8 T cells during localized IAV infection. Here, we present evidence of early CD8 T cell priming in the spleen following respiratory IAV infection independent of lung-draining lymph node priming of T cells. Although we found early indications of CD8 T cell activation in the lymph nodes draining the respiratory tract, we also saw evidence of virus-specific CD8 T cell activation in the spleen. Furthermore, CD8 T cells primed in the spleen differentiated into memory cells of equivalent longevity and with similar recall capacity as CD8 T cells primed in the draining lymph nodes. These data showed that the spleen contributes to the virus-specific effector and memory CD8 T cell populations that are generated in response to respiratory infection.

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References

Togashi T, Matsuzono Y, Narita M, Morishima T . Influenza-associated acute encephalopathy in Japanese children in 1994-2002. Virus Res. 2004; 103(1-2):75-8. DOI: 10.1016/j.virusres.2004.02.016. View

Lee Y, Suarez-Ramirez J, Wu T, Redman J, Bouchard K, Hadley G . Environmental and antigen receptor-derived signals support sustained surveillance of the lungs by pathogen-specific cytotoxic T lymphocytes. J Virol. 2011; 85(9):4085-94. PMC: 3126261. DOI: 10.1128/JVI.02493-10. View

Lawrence C, Braciale T . Activation, differentiation, and migration of naive virus-specific CD8+ T cells during pulmonary influenza virus infection. J Immunol. 2004; 173(2):1209-18. DOI: 10.4049/jimmunol.173.2.1209. View

Khanna K, Blair D, Vella A, McSorley S, Datta S, Lefrancois L . T cell and APC dynamics in situ control the outcome of vaccination. J Immunol. 2010; 185(1):239-52. PMC: 2997353. DOI: 10.4049/jimmunol.0901047. View

Masopust D, Vezys V, Marzo A, Lefrancois L . Preferential localization of effector memory cells in nonlymphoid tissue. Science. 2001; 291(5512):2413-7. DOI: 10.1126/science.1058867. View

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

Yoo J, Galligan C, Virtanen C, Fish E . Identification of a novel antigen-presenting cell population modulating antiinfluenza type 2 immunity. J Exp Med. 2010; 207(7):1435-51. PMC: 2901068. DOI: 10.1084/jem.20091373. View

Moskophidis D, Kioussis D . Contribution of virus-specific CD8+ cytotoxic T cells to virus clearance or pathologic manifestations of influenza virus infection in a T cell receptor transgenic mouse model. J Exp Med. 1998; 188(2):223-32. PMC: 2212460. DOI: 10.1084/jem.188.2.223. View

Teijaro J, Turner D, Pham Q, Wherry E, Lefrancois L, Farber D . Cutting edge: Tissue-retentive lung memory CD4 T cells mediate optimal protection to respiratory virus infection. J Immunol. 2011; 187(11):5510-4. PMC: 3221837. DOI: 10.4049/jimmunol.1102243. View

10.

Masopust D . Developing an HIV cytotoxic T-lymphocyte vaccine: issues of CD8 T-cell quantity, quality and location. J Intern Med. 2008; 265(1):125-37. DOI: 10.1111/j.1365-2796.2008.02054.x. View

11.

Wherry E, Barber D, Kaech S, Blattman J, Ahmed R . Antigen-independent memory CD8 T cells do not develop during chronic viral infection. Proc Natl Acad Sci U S A. 2004; 101(45):16004-9. PMC: 524220. DOI: 10.1073/pnas.0407192101. View

12.

Kim T, Hufford M, Sun J, Fu Y, Braciale T . Antigen persistence and the control of local T cell memory by migrant respiratory dendritic cells after acute virus infection. J Exp Med. 2010; 207(6):1161-72. PMC: 2882836. DOI: 10.1084/jem.20092017. View

13.

Mempel T, Henrickson S, von Andrian U . T-cell priming by dendritic cells in lymph nodes occurs in three distinct phases. Nature. 2004; 427(6970):154-9. DOI: 10.1038/nature02238. View

14.

Hogquist K, Jameson S, Heath W, Howard J, Bevan M, Carbone F . T cell receptor antagonist peptides induce positive selection. Cell. 1994; 76(1):17-27. DOI: 10.1016/0092-8674(94)90169-4. View

15.

Wu H, Kumar A, Miao H, Holden-Wiltse J, Mosmann T, Livingstone A . Modeling of influenza-specific CD8+ T cells during the primary response indicates that the spleen is a major source of effectors. J Immunol. 2011; 187(9):4474-82. PMC: 3197949. DOI: 10.4049/jimmunol.1101443. View

16.

Salonen O, Koshkiniemi M, Saari A, Myllyla V, Pyhala R, Airaksinen L . Myelitis associated with influenza A virus infection. J Neurovirol. 1997; 3(1):83-5. DOI: 10.3109/13550289709015797. View

17.

Eichelberger M . Virus-specific antigen presentation by different subsets of cells from lung and mediastinal lymph node tissues of influenza virus-infected mice. J Virol. 1995; 69(10):6359-66. PMC: 189535. DOI: 10.1128/JVI.69.10.6359-6366.1995. View

18.

Legge K, Braciale T . Accelerated migration of respiratory dendritic cells to the regional lymph nodes is limited to the early phase of pulmonary infection. Immunity. 2003; 18(2):265-77. DOI: 10.1016/s1074-7613(03)00023-2. View

19.

Yap K, Ada G . Cytotoxic T cells in the lungs of mice infected with an influenza A virus. Scand J Immunol. 1978; 7(1):73-80. DOI: 10.1111/j.1365-3083.1978.tb00428.x. View

20.

Pinschewer D, Ochsenbein A, Odermatt B, Brinkmann V, Hengartner H, Zinkernagel R . FTY720 immunosuppression impairs effector T cell peripheral homing without affecting induction, expansion, and memory. J Immunol. 2000; 164(11):5761-70. DOI: 10.4049/jimmunol.164.11.5761. View