Skip to main content
SpringerLink
Log in

Class I MHC Antigens and the Control of Virus Infections by NK Cells

  • Chapter
Cytotoxic Cells: Recognition, Effector Function, Generation, and Methods

Abstract

Due to their ability to lyse virus-infected cells before the release of mature virions, cytotoxic lymphocytes are among the most important host defense mechanisms against viral infections. The two major forms of cytotoxic lymphocytes are the natural killer (NK) cells and the cytotoxic T lymphocytes (CTL), which peak in response at early and late stages of infection, respectively. Mouse NK cells, defined here as CD3−, TCR−, NK1.1+, asialo GM1 + lymphocytes, are normally slowly dividing cells that lyse a limited range of “NKsensitive” targets, but the interferon (IFN)-α/β induced during virus infection augments their cytolytic potential, enabling them to lyse most types of targets, and, most likely in concordance with other growth factors, stimulates their proliferation (Welsh, 1986). NK cells accumulate at sites of virus infection and may represent up to 20% of the infiltrating leukocyte population by 3 days postinfection (McIntyre and Welsh, 1986; Natuk and Welsh, 1987). Concomitantly, clones of CTL precursors recognizing viral peptides displayed on class I major histocompatibility complex (MHC) antigens proliferate and differentiate in response to IL-2 and IFN-γ and become detectable at later (day 6–10) stages of infection (Welsh, 1986; Townsend and Bodmer, 1989). At this later time the NK cell response diminishes, due both to a decrease in the levels of virus, which stimulate the IFN-α/β response, and due to suppressive effects of transforming growth factor-β produced predominantly by activated macrophages (Su et al., 1991).

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 39.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Andersson M, Paabo S, Nilsson T, Peterson PA (1985): Impaired intracellular transport of class I MHC antigens as a possible means for adenovirus to evade immune surveillance. Cell 43: 215–222

    Article  Google Scholar 

  • Arora DJS, Houde M, Justewicz DM, Mandeville R (1984): In vitro enhancement of human natural killer cell mediated cytotoxicity by purified influenza virus glycoproteins. J Virol 52: 839–845

    Google Scholar 

  • Biron CA, Byron KS, Sullivan JS (1989): Severe herpes virus infections in an adolescent without natural killer cells. New Engl J Med 320: 1731–1735

    Article  Google Scholar 

  • Borysiewicz LK, Rodgers B, Morris S, Graham S, Sissons JGP (1985): Lysis of human cytomegalovirus infected fibroblasts by natural killer cells: Demonstration of an interferon-dependent component requiring expression of early viral proteins and characterization of effector cells. J Immunol 134: 2695–2701

    Google Scholar 

  • Browne H, Smith G, Beck S, Minson T (1990): A complex between the MHC class I homologue encoded by human cytomegalovirus and ß, microglobulin. Nature 347: 770–772

    Article  Google Scholar 

  • Bukowski JF, Welsh RM (1985a): Interferon enhances the susceptibility of virus-infected fibroblasts to cytotoxic T cells. J Exp Med 161: 257–262

    Article  Google Scholar 

  • Bukowski JF, Welsh RM (19856): Susceptibility of virus-infected targets to natural killer cell-mediated lysis in vitro correlates with natural killer cell-mediated antiviral effects in vivo. J Immunol 135: 3537–3541

    Google Scholar 

  • Bukowski JF, Welsh RM (1986): Enhanced susceptibility to cytotoxic T lymphocytes of target cells isolated from virus-infected or interferon-treated mice. J Virol 59: 735–739

    Google Scholar 

  • Bukowski JF, Warner JR, Dennert G, Welsh RM (1985): Adoptive transfer studies demonstrating the antiviral effect of NK cells in vivo. J Exp Med 161: 40–52

    Article  Google Scholar 

  • Bukowski JF, Yang IT Welsh RM (1988): The antiviral effect of lymphokine activated killer (LAK) cells. 1. Characterization of the effector cells mediating prophylaxis. J Virol 62: 3642–3648

    Google Scholar 

  • Casali P, Sissons JGP, Buchmeier MJ, Oldstone MBA (1981): In vitro generation of human cytotoxic lymphocytes by virus. Viral glycoproteins induce nonspecific cell-mediated cytotoxicity without release of interferon. J Exp Med 154: 840–855

    Article  Google Scholar 

  • Chadwick BS, Sambhara SR, Roder JC, Miller RG (1991): Effect of MHC-class-l-binding peptides on recognition by NK cells. Nat Immun Cell Growth Regul 10: 127 (abstract)

    Google Scholar 

  • Cook JL, May DL, Lewis AM, Walker TA (1987): Adenovirus EIA gene induction of susceptibility to lysis by natural killer cells and infected macrophages in infected rodent cells. J Virol 61: 3510–3520

    Google Scholar 

  • Dawson JR, Storkus WJ, Patterson EB, Cresswell P (1989): Adenovirus inversely modulates target cell class I MHC antigen expression and sensitivity to natural killing. In: Natural Killer Cells and Host Defense, Ades EW, Lopez C, eds. Basel: S Karger, pp. 156–159

    Google Scholar 

  • Flyer DC, Burakoff SJ, Faller DV (1985): Retrovirusinduced changes in major histocompatibility complex antigen expression influence susceptibility to lysis by cytotoxic T lymphocytes. J Immunol 135: 2287–2292

    Google Scholar 

  • Friedman DJ, Ricciardi RP (1988): Adenovirus type 12 EIA gene represses accumulation of MHC class I mRNAs at the level of transcription. Virology 165: 303–305

    Article  Google Scholar 

  • Hansson M, Kiessling R, Andersson B, Welsh RM (1980): Effect of interferon and interferon inducers on the NK sensitivity of normal mouse thymocytes. J Immunol 125: 2225–2231

    Google Scholar 

  • Harfast B, Orvell C, Alsheikhly A, Andersson T, Perlmann P, Norrby E (1980): The role of viral glycoproteins in mumps virus-dependent lymphocyte-mediated cytotoxicity in vitro. Scand J Immunol 11: 391–400

    Article  Google Scholar 

  • Hecht TT, Summers DF (1972): Effect of vesicular stoma-titis virus infection on histocompatibility antigens of L cells. J Virol 10: 578–585

    Google Scholar 

  • Hoglund P, Glas R, Ohlen C, Ljunggren H-G, Karre K (1991): Alteration of the natural killer cell repertoire in H-2 transgenic mice: Specificity of rapid lymphoma cell clearance determined by the H-2 phenotype of the cell. J Exp Med 174: 327–334

    Article  Google Scholar 

  • Jennings SR, Rice PL, Kloszewski ED, Anderson RW, Thompson DL, Tevethia SS (1985): Effect of herpes simplex virus types 1 and 2 on surface expression of class I major histocompatibility complex antigens on infected cells. J Virol 56: 757–766

    Google Scholar 

  • Kiessling R, Welsh RM (1980): Killing of normal cells by natural killer cells: Evidence for two patterns of genetic regulation of lysis. In! J Cancer 25: 611–615

    Article  Google Scholar 

  • Liao N-S, Bix M, Zilstra M, Jaenisch R, Raulet D (1991): MHC class I deficiency: Susceptibility to natural killer (NK) cells and impaired NK activity. Science 253: 199–202

    Article  Google Scholar 

  • Ljunggren H-G, Karre K (1990): In search of the `missing se1P: MHC molecules and NK cell recognition. Immuno! Today 11: 237–244

    Article  Google Scholar 

  • Ljunggren H-G, Sturmhofel K, Wolpert E, Hammerling G, Karre K (1990): Transfection of ß2-microglobulin restores IFN-mediated protection from natural killer cell lysis in YAC-1 lymphoma variants. J Immunol 145: 380–386

    Google Scholar 

  • Lopez C, Kirkpatrick D, Reid SE, Fitzgerald PA, Pitt J, Pahwa S, Ching CY, Smithwick EM (1983): Correlation between low natural killing of fibroblasts infected with herpes simplex virus type 1 and susceptibility to herpesvirus infections. J Infect Dis 147: 1030–1035

    Article  Google Scholar 

  • McIntyre KW, Welsh RM (1986): Accumulation of natural killer and cytotoxic T large granular lymphocytes during virus infection. J Exp Med 164: 1677–1681

    Article  Google Scholar 

  • Mellencamp MW, O’Brien PCM, Stevenson JR (1991): Pseudorabies virus-induced suppression of major histocompatibility complex class I antigen expression. J Virol 65: 3365–3368

    Google Scholar 

  • Natuk RJ, Welsh RM (1987): Accumulation and chemotaxis of natural killer/large granular lymphocytes to sites of virus replication. J Immunol 138: 877–883

    Google Scholar 

  • Quinnan GV, Kirmani N, Rook AH, Manischewitz JF, Jackson L, Moreschi G, Santos GW, Sarai R, Burns WH (1982): Cytotoxic T cells in cytomegalovirus infection: HLA-restricted T-lymphocyte and non-Tlymphocyte cytotoxic responses correlate with recovery from cytomegalovirus infection in bone marrow transplant recipients. New Engl J Med 307: 7–13

    Article  Google Scholar 

  • Rich RF, Gaffney KJ, White HD, Green WR (1990): Differential up-regulation of H-2D versus H-2K class I major histocompatibility expression by interferon-gamma: Evidence against a trans-acting factor. J Interferon Res 10: 505–514

    Article  Google Scholar 

  • Scalzo AA, Fitzgerald NA, Simmons A, LaVista AB, Shellam GR (1990): CMV-1, a genetic locus that controls murine cytomegalovirus replication in the spleen. J Exp Med 171: 1469–1483

    Article  Google Scholar 

  • Scheppler JA, Nicholson JKA, Swan DC, Ahmed-Ansari A, McDougal JS (1989): Down-modulation of MHC-I in a CD4+ T cell line, CEM-E5, after HIV-1 infection. J Immunol 143: 2858–2866

    Google Scholar 

  • Storkus WJ, Salter RD, Alexander J, Ward FE, Ruiz RE, Cresswell P, Dawson JR (1991): Class I-induced resistance to natural killing: Identification of nonpermissive residues in HLA-A2. Proc Nall Acad Sci USA 88: 5989–5992

    Article  Google Scholar 

  • Su HC, Ishikawa R, Leite-Morris KA, Braun L, Biron CA (1991): Role of TGF-beta in regulating NK cell proliferation. Nat Immun Cell Growth Regul 10: 147–148 (abstract)

    Google Scholar 

  • Townsend A, Bodmer H (1989): Antigen recognition by class I-restricted T lymphocytes. Annu Rev Immunol 7: 601–624

    Article  Google Scholar 

  • Trinchieri G, Santoli D (1978): Antiviral activity induced by culturing lymphocytes with tumor derived or virus-transformed cells. Enhancement of natural killer activity by interferon and antagonistic inhibition of susceptibility of target cells to lysis. J Exp Med 147: 1314–1333

    Article  Google Scholar 

  • Versteeg R, Noodermeer IA, Kruse-Walters M, Reiter DJ, Schrier P (1988): c-myc down-regulates class I HLA expression in human melanomas. EMBO J 7: 1023–1029

    Google Scholar 

  • Versteeg R, Peltenburg LTC, Plomp AC, Schrier PI (1989): High expression of the c-myc oncogene renders melanoma cells prone to lysis by natural killer cells. J Immunol 143: 4331–4337

    Google Scholar 

  • Welsh RM (1978): Cytotoxic cells induced during lymphocytic choriomenigitis virus infection of mice: 1. Characterization of natural killer cell induction. J Exp Med 148: 163–181

    Article  Google Scholar 

  • Welsh RM (1986): Regulation of virus infections by natural killer cells. Nat Immun Cell Growth Regul 5: 169–199

    Google Scholar 

  • Welsh RM, Hallenbeck LA (1980): Effect of virus infections on target cell susceptibility to natural killer cell-mediated lysis. J Immunol 124: 2491–2497

    Google Scholar 

  • Welsh RM, Vargas-Cortes M (1992): Natural killer cells in virus infection. In: The Natural Immune System: The Natural Killer Cell, Lewis CE, Gee JOM, eds. Oxford University Press, pp. 108–150

    Google Scholar 

  • Welsh RM, Brubaker JO, Vargas-Cortes M, O’Donnell CL (1991): Natural killer (NK) cell response to virus infections in mice with severe combined immunodeficiency. The stimulation of NK cells and the NK cell-dependent control of virus infections occur independently of T and B cell function. J Exp Med 173: 1053–1063

    Article  Google Scholar 

  • Welsh RM, Dundon PL, Eynon EE, Brubaker JO, Koo GC, O’Donnell CL (1990): Demonstration of the antiviral role of natural killer cells in vivo with a natural killer cell-specific monoclonal antibody (NK 1.1). Nat Immun Cell Growth Regul 9: 112–120

    Google Scholar 

  • Welsh RM, Karre K, Hansson M, Kunkel LA, Kiessling RW (1981): Interferon-mediated protection of normal and tumor target cells against lysis by mouse natural killer cells. J Immunol 126: 219–225

    Google Scholar 

  • Welsh RM, Zinkernagel RM, Hallenbeck LA (1979): Cytotoxic cells induced during lymphocytic choriomeningitis virus infection of mice. II. Specificities of the natural killer cells. J Immunol 122: 475–481

    Google Scholar 

Download references

Authors
  1. Raymond M. Welsh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Paul R. Rogers
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Randy R. Brutkiewicz
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Laboratory of Immunology, Biochemistry and Immunopharmacology Unit, NIH-NIAID, 20892, Bethesda, Maryland, USA

    Michail V. Sitkovsky

  2. Experimental Immunology Branch, National Cancer Institute, National Institutes of Health, 20892, Bethesda, Maryland, USA

    Pierre A. Henkart

Rights and permissions

Reprints and permissions

Copyright information

© 1993 Birkhäuser Boston

About this chapter

Cite this chapter

Welsh, R.M., Rogers, P.R., Brutkiewicz, R.R. (1993). Class I MHC Antigens and the Control of Virus Infections by NK Cells. In: Sitkovsky, M.V., Henkart, P.A. (eds) Cytotoxic Cells: Recognition, Effector Function, Generation, and Methods. Birkhäuser Boston. https://doi.org/10.1007/978-1-4684-6814-4_40

Download citation

  • DOI: https://doi.org/10.1007/978-1-4684-6814-4_40

  • Publisher Name: Birkhäuser Boston

  • Print ISBN: 978-1-4684-6816-8

  • Online ISBN: 978-1-4684-6814-4

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation