Identification of a Novel Antigen-presenting Cell Population Modulating Antiinfluenza Type 2 Immunity

Overview

Journal J Exp Med

Specialties Allergy & Immunology
General Medicine

Date 2010 Jun 16

PMID 20547825

Citations 15

Authors

Jae-Kwang Yoo

Carole L Galligan

Carl Virtanen

Eleanor N Fish

Affiliations

Soon will be listed here.

Abstract

Antiinfluenza type 2 (T2) immunity contributes to both immunopathology and immunoprotection, yet the underlying mechanisms modulating T2 immunity remain ill defined. We describe a novel mouse antigen (Ag)-presenting cell (APC), designated late-activator APC (LAPC). After pulmonary influenza A (H1N1) virus infection, LAPCs enter the lungs, capture viral Ag, and subsequently migrate to the draining lymph node (DLN) and spleen, with delayed kinetics relative to dendritic cells (DCs). In the DLN, influenza virus-activated LAPCs present Ag and selectively induce T helper type 2 (Th2) effector cell polarization by cell-cell contact-mediated modulation of GATA-3 expression. In adoptive transfer experiments, influenza virus-activated LAPCs augmented Th2 effector T cell responses in the DLN, increased production of circulating antiinfluenza immunoglobulin, and increased levels of T2 cytokines in bronchoalveolar lavage fluid in recipient influenza virus-infected mice. LAPC-recipient mice exhibited exacerbated pulmonary pathology, with delayed viral clearance and enhanced pulmonary eosinophilia. Collectively, our results identify and highlight the importance of LAPCs as immunomodulators of T2 immunity during influenza A virus infection.

Citing Articles

Identifying Active Compounds and Targets of against Influenza-Associated Inflammation by Network Pharmacology Analysis and Molecular Docking.

Kim M, Park K, Kim Y Molecules. 2020; 25(17).

PMID: 32854331 PMC: 7504253. DOI: 10.3390/molecules25173853.

Kinetics and Phenotype of the CD4 T Cell Response to Influenza Virus Infections.

Hornick E, Zacharias Z, Legge K Front Immunol. 2019; 10:2351.

PMID: 31632414 PMC: 6783515. DOI: 10.3389/fimmu.2019.02351.

IL-21 promotes late activator APC-mediated T follicular helper cell differentiation in experimental pulmonary virus infection.

Yoo J, Braciale T PLoS One. 2014; 9(9):e105872.

PMID: 25251568 PMC: 4175070. DOI: 10.1371/journal.pone.0105872.

Mucosal immunization and adjuvants.

Hasegawa H, van Reit E, Kida H Curr Top Microbiol Immunol. 2014; 386:371-80.

PMID: 25015787 PMC: 7120566. DOI: 10.1007/82_2014_402.

CD301b⁺ dermal dendritic cells drive T helper 2 cell-mediated immunity.

Kumamoto Y, Linehan M, Weinstein J, Laidlaw B, Craft J, Iwasaki A Immunity. 2013; 39(4):733-43.

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References

Marshall D, Sealy R, SANGSTER M, Coleclough C . TH cells primed during influenza virus infection provide help for qualitatively distinct antibody responses to subsequent immunization. J Immunol. 1999; 163(9):4673-82. View

Cox N, Subbarao K . Global epidemiology of influenza: past and present. Annu Rev Med. 2000; 51:407-21. DOI: 10.1146/annurev.med.51.1.407. View

Amsen D, Antov A, Jankovic D, Sher A, Radtke F, Souabni A . Direct regulation of Gata3 expression determines the T helper differentiation potential of Notch. Immunity. 2007; 27(1):89-99. PMC: 2062505. DOI: 10.1016/j.immuni.2007.05.021. View

Hurst S, Muchamuel T, Gorman D, Gilbert J, Clifford T, Kwan S . New IL-17 family members promote Th1 or Th2 responses in the lung: in vivo function of the novel cytokine IL-25. J Immunol. 2002; 169(1):443-53. DOI: 10.4049/jimmunol.169.1.443. View

Zheng W, Flavell R . The transcription factor GATA-3 is necessary and sufficient for Th2 cytokine gene expression in CD4 T cells. Cell. 1997; 89(4):587-96. DOI: 10.1016/s0092-8674(00)80240-8. View

Carding S, Allan W, McMickle A, Doherty P . Activation of cytokine genes in T cells during primary and secondary murine influenza pneumonia. J Exp Med. 1993; 177(2):475-82. PMC: 2190883. DOI: 10.1084/jem.177.2.475. View

Kaech S, Wherry E, Ahmed R . Effector and memory T-cell differentiation: implications for vaccine development. Nat Rev Immunol. 2002; 2(4):251-62. DOI: 10.1038/nri778. View

McGill J, van Rooijen N, Legge K . Protective influenza-specific CD8 T cell responses require interactions with dendritic cells in the lungs. J Exp Med. 2008; 205(7):1635-46. PMC: 2442641. DOI: 10.1084/jem.20080314. View

Belz G, Bedoui S, Kupresanin F, Carbone F, Heath W . Minimal activation of memory CD8+ T cell by tissue-derived dendritic cells favors the stimulation of naive CD8+ T cells. Nat Immunol. 2007; 8(10):1060-6. DOI: 10.1038/ni1505. View

10.

Baboonian C, Davies M, BOOTH J, McKenna W . Coxsackie B viruses and human heart disease. Curr Top Microbiol Immunol. 1997; 223:31-52. DOI: 10.1007/978-3-642-60687-8_3. View

11.

Dawson T, Beck M, Kuziel W, Henderson F, Maeda N . Contrasting effects of CCR5 and CCR2 deficiency in the pulmonary inflammatory response to influenza A virus. Am J Pathol. 2000; 156(6):1951-9. PMC: 1850091. DOI: 10.1016/S0002-9440(10)65068-7. View

12.

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

13.

Kondo M, Wagers A, Manz M, Prohaska S, Scherer D, Beilhack G . Biology of hematopoietic stem cells and progenitors: implications for clinical application. Annu Rev Immunol. 2003; 21:759-806. DOI: 10.1146/annurev.immunol.21.120601.141007. View

14.

Irizarry R, Hobbs B, Collin F, Beazer-Barclay Y, Antonellis K, Scherf U . Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics. 2003; 4(2):249-64. DOI: 10.1093/biostatistics/4.2.249. View

15.

Yoon H, Legge K, Sung S, Braciale T . Sequential activation of CD8+ T cells in the draining lymph nodes in response to pulmonary virus infection. J Immunol. 2007; 179(1):391-9. DOI: 10.4049/jimmunol.179.1.391. View

16.

La Gruta N, Kedzierska K, Stambas J, Doherty P . A question of self-preservation: immunopathology in influenza virus infection. Immunol Cell Biol. 2007; 85(2):85-92. DOI: 10.1038/sj.icb.7100026. View

17.

DeKruyff R, Rizzo L, Umetsu D . Induction of immunoglobulin synthesis by CD4+ T cell clones. Semin Immunol. 1993; 5(6):421-30. DOI: 10.1006/smim.1993.1048. View

18.

Brehin A, Mouries J, Frenkiel M, Dadaglio G, Despres P, Lafon M . Dynamics of immune cell recruitment during West Nile encephalitis and identification of a new CD19+B220-BST-2+ leukocyte population. J Immunol. 2008; 180(10):6760-7. DOI: 10.4049/jimmunol.180.10.6760. View

19.

McKenna H, Stocking K, Miller R, Brasel K, De Smedt T, Maraskovsky E . Mice lacking flt3 ligand have deficient hematopoiesis affecting hematopoietic progenitor cells, dendritic cells, and natural killer cells. Blood. 2000; 95(11):3489-97. View

20.

Palladino G, Mozdzanowska K, Washko G, GERHARD W . Virus-neutralizing antibodies of immunoglobulin G (IgG) but not of IgM or IgA isotypes can cure influenza virus pneumonia in SCID mice. J Virol. 1995; 69(4):2075-81. PMC: 188873. DOI: 10.1128/JVI.69.4.2075-2081.1995. View