Early Responding Dendritic Cells Direct the Local NK Response To Control Herpes Simplex Virus 1 Infection within the Cornea

Journal of Immunology - Tập 188 Số 3 - Trang 1350-1359 - 2012
Gregory M. Frank1,2, Kristine-Ann Buela1,2, D. Maker2, S. Harvey2, Robert L. Hendricks3,2,4
1*Graduate Program in Immunology, University of Pittsburgh School of Medicine, Pittsburgh, PA 15213;
2Department of Ophthalmology, University of Pittsburgh School of Medicine, Pittsburgh, PA 15213
3§Department of Molecular Genetics and Biochemistry, University of Pittsburgh School of Medicine, Pittsburgh, PA 15213
4‡Department of Immunology, University of Pittsburgh School of Medicine, Pittsburgh, PA 15213; and

Tóm tắt

Abstract Dendritic cells (DCs) regulate both innate and adaptive immune responses. In this article, we exploit the unique avascularity of the cornea to examine a role for local or very early infiltrating DCs in regulating the migration of blood-derived innate immune cells toward HSV-1 lesions. A single systemic diphtheria toxin treatment 2 d before HSV-1 corneal infection transiently depleted CD11c+ DCs from both the cornea and lymphoid organs of CD11c-DTR bone marrow chimeric mice for up to 24 h postinfection. Transient DC depletion significantly delayed HSV-1 clearance from the cornea through 6 d postinfection. No further compromise of viral clearance was observed when DCs were continuously depleted throughout the first week of infection. DC depletion did not influence extravasation of NK cells, inflammatory monocytes, or neutrophils into the peripheral cornea, but it did significantly reduce migration of NK cells and inflammatory monocytes, but not neutrophils, toward the HSV-1 lesion in the central cornea. Depletion of NK cells resulted in similar loss of viral control to transient DC ablation. Our findings demonstrate that resident corneal DCs and/or those that infiltrate the cornea during the first 24 h after HSV-1 infection contribute to the migration of NK cells and inflammatory monocytes into the central cornea, and are consistent with a role for NK cells and possibly inflammatory monocytes, but not polymorphonuclear neutrophils, in clearing HSV-1 from the infected cornea.

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Tài liệu tham khảo

Kaisho, 2001, Dendritic-cell function in Toll-like receptor- and MyD88-knockout mice., Trends Immunol., 22, 78, 10.1016/S1471-4906(00)01811-1

Kaisho, 2001, Toll-like receptors and their signaling mechanism in innate immunity., Acta Odontol. Scand., 59, 124, 10.1080/000163501750266701

Bedoui, 2009, Cross-presentation of viral and self antigens by skin-derived CD103+ dendritic cells., Nat. Immunol., 10, 488, 10.1038/ni.1724

Knickelbein, 2009, Stratification of antigen-presenting cells within the normal cornea., Ophthalmol. Eye Dis., 1, 45, 10.4137/OED.S2813

Eidsmo, 2009, Differential migration of epidermal and dermal dendritic cells during skin infection., J. Immunol., 182, 3165, 10.4049/jimmunol.0802950

Lucas, 2007, Dendritic cells prime natural killer cells by trans-presenting interleukin 15., Immunity, 26, 503, 10.1016/j.immuni.2007.03.006

Kassim, 2006, In vivo ablation of CD11c-positive dendritic cells increases susceptibility to herpes simplex virus type 1 infection and diminishes NK and T-cell responses., J. Virol., 80, 3985, 10.1128/JVI.80.8.3985-3993.2006

Kassim, 2009, Dendritic cells are required for optimal activation of natural killer functions following primary infection with herpes simplex virus type 1., J. Virol., 83, 3175, 10.1128/JVI.01907-08

Liu, 1996, Inflammatory infiltration of the trigeminal ganglion after herpes simplex virus type 1 corneal infection., J. Virol., 70, 264, 10.1128/jvi.70.1.264-271.1996

Heiligenhaus, 1999, CD4+ T-cell type 1 and type 2 cytokines in the HSV-1 infected cornea., Graefes Arch. Clin. Exp. Ophthalmol., 237, 399, 10.1007/s004170050251

Ghiasi, 2000, The role of natural killer cells in protection of mice against death and corneal scarring following ocular HSV-1 infection., Antiviral Res., 45, 33, 10.1016/S0166-3542(99)00075-3

Carr, 2001, The immune response to ocular herpes simplex virus type 1 infection., Exp. Biol. Med. (Maywood), 226, 353, 10.1177/153537020122600501

Daley, 2008, Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice., J. Leukoc. Biol., 83, 64, 10.1189/jlb.0407247

Wojtasiak, 2010, Depletion of Gr-1+, but not Ly6G+, immune cells exacerbates virus replication and disease in an intranasal model of herpes simplex virus type 1 infection., J. Gen. Virol., 91, 2158, 10.1099/vir.0.021915-0

Wojtasiak, 2010, Gr-1+ cells, but not neutrophils, limit virus replication and lesion development following flank infection of mice with herpes simplex virus type-1., Virology, 407, 143, 10.1016/j.virol.2010.08.001

Quinnan, 1979, The role of natural killer cells and antibody-dependent cell-mediated cytotoxicity during murine cytomegalovirus infection., J. Exp. Med., 150, 1549, 10.1084/jem.150.6.1549

Welsh, 1986, Regulation of virus infections by natural killer cells. A review., Natural Immunity and Cell Growth Regulation, 5, 169

Ferlazzo, 2004, The abundant NK cells in human secondary lymphoid tissues require activation to express killer cell Ig-like receptors and become cytolytic., J. Immunol., 172, 1455, 10.4049/jimmunol.172.3.1455

Ferlazzo, 2004, Distinct roles of IL-12 and IL-15 in human natural killer cell activation by dendritic cells from secondary lymphoid organs., Proc. Natl. Acad. Sci. USA, 101, 16606, 10.1073/pnas.0407522101

Kobayashi, 2005, Role of trans-cellular IL-15 presentation in the activation of NK cell-mediated killing, which leads to enhanced tumor immunosurveillance., Blood, 105, 721, 10.1182/blood-2003-12-4187

Hochweller, 2008, A novel CD11c.DTR transgenic mouse for depletion of dendritic cells reveals their requirement for homeostatic proliferation of natural killer cells., Eur. J. Immunol., 38, 2776, 10.1002/eji.200838659

Zhao, 2003, Vaginal submucosal dendritic cells, but not Langerhans cells, induce protective Th1 responses to herpes simplex virus-2., J. Exp. Med., 197, 153, 10.1084/jem.20021109

Miller, 1993, Corneal Langerhans cell dynamics after herpes simplex virus reactivation., Invest. Ophthalmol. Vis. Sci., 34, 2282

Chen, 1998, B7 costimulatory requirements of T cells at an inflammatory site., J. Immunol., 160, 5045, 10.4049/jimmunol.160.10.5045

Ambati, 2006, Corneal avascularity is due to soluble VEGF receptor-1., Nature, 443, 993, 10.1038/nature05249

Tang, 1997, Proinflammatory functions of IL-2 in herpes simplex virus corneal infection., J. Immunol., 158, 1275, 10.4049/jimmunol.158.3.1275

Zammit, 2005, Dendritic cells maximize the memory CD8 T cell response to infection., Immunity, 22, 561, 10.1016/j.immuni.2005.03.005

Chinnery, 2008, Turnover of bone marrow-derived cells in the irradiated mouse cornea., Immunology, 125, 541, 10.1111/j.1365-2567.2008.02868.x

Yan, 1998, Role of MIP-2 in neutrophil migration and tissue injury in the herpes simplex virus-1-infected cornea., Invest. Ophthalmol. Vis. Sci., 39, 1854

Bursch, 2007, Identification of a novel population of Langerin+ dendritic cells., J. Exp. Med., 204, 3147, 10.1084/jem.20071966

Kaplan, 2005, Epidermal Langerhans cell-deficient mice develop enhanced contact hypersensitivity., Immunity, 23, 611, 10.1016/j.immuni.2005.10.008

Brissette-Storkus, 2002, Identification of a novel macrophage population in the normal mouse corneal stroma., Invest. Ophthalmol. Vis. Sci., 43, 2264

Vollstedt, 2006, The long-term but not the short-term antiviral effect of IFN-alpha depends on Flt3 ligand and pDC., Eur. J. Immunol., 36, 1231, 10.1002/eji.200535759

Hochrein, 2004, Herpes simplex virus type-1 induces IFN-alpha production via Toll-like receptor 9-dependent and -independent pathways., Proc. Natl. Acad. Sci. USA, 101, 11416, 10.1073/pnas.0403555101

Sapoznikov, 2007, Organ-dependent in vivo priming of naive CD4+, but not CD8+, T cells by plasmacytoid dendritic cells., J. Exp. Med., 204, 1923, 10.1084/jem.20062373

Bukowski, 1986, The role of natural killer cells and interferon in resistance to acute infection of mice with herpes simplex virus type 1., J. Immunol., 136, 3481, 10.4049/jimmunol.136.9.3481

Sciammas, 1997, T cell receptor-gamma/delta cells protect mice from herpes simplex virus type 1-induced lethal encephalitis., J. Exp. Med., 185, 1969, 10.1084/jem.185.11.1969

Vance, 1998, Mouse CD94/NKG2A is a natural killer cell receptor for the nonclassical major histocompatibility complex (MHC) class I molecule Qa-1(b)., J. Exp. Med., 188, 1841, 10.1084/jem.188.10.1841

Bourquin, 2009, Immunostimulatory RNA oligonucleotides induce an effective antitumoral NK cell response through the TLR7., J. Immunol., 183, 6078, 10.4049/jimmunol.0901594

Martinez, 2010, Direct TLR2 signaling is critical for NK cell activation and function in response to vaccinia viral infection., PLoS Pathog., 6, e1000811, 10.1371/journal.ppat.1000811

Zitvogel, 2002, Dendritic and natural killer cells cooperate in the control/switch of innate immunity., J. Exp. Med., 195, F9, 10.1084/jem.20012040

Tang, 1996, Interferon gamma regulates platelet endothelial cell adhesion molecule 1 expression and neutrophil infiltration into herpes simplex virus-infected mouse corneas., J. Exp. Med., 184, 1435, 10.1084/jem.184.4.1435

Saito, 1996, Nitric oxide production by peritoneal macrophages of Mycobacterium bovis BCG-infected or non-infected mice: regulatory role of T lymphocytes and cytokines., J. Leukoc. Biol., 59, 908, 10.1002/jlb.59.6.908

Molesworth-Kenyon, 2008, IL-17 receptor signaling influences virus-induced corneal inflammation., J. Leukoc. Biol., 83, 401, 10.1189/jlb.0807571

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Journal of Immunology

Tập 188 Số 3

1350-1359

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