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Ly49C Impairs NK Cell Memory in Mouse Cytomegalovirus Infection

Catherine A. Forbes, Anthony A. Scalzo, Mariapia A. Degli-Esposti and Jerome D. Coudert
J Immunol May 27, 2016, 1600199; DOI: https://doi.org/10.4049/jimmunol.1600199
Catherine A. Forbes
Centre for Experimental Immunology, Lions Eye Institute, Nedlands, Western Australia 6009, Australia; and
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Anthony A. Scalzo
Centre for Experimental Immunology, Lions Eye Institute, Nedlands, Western Australia 6009, Australia; and
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Mariapia A. Degli-Esposti
Centre for Experimental Immunology, Lions Eye Institute, Nedlands, Western Australia 6009, Australia; andCentre for Ophthalmology and Vision Science, University of Western Australia, Crawley, Western Australia 6009, Australia
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Jerome D. Coudert
Centre for Experimental Immunology, Lions Eye Institute, Nedlands, Western Australia 6009, Australia; andCentre for Ophthalmology and Vision Science, University of Western Australia, Crawley, Western Australia 6009, Australia
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Abstract

NK cells possess inhibitory receptors that are responsible for self-MHC class I recognition; beyond their inhibitory function, accumulating evidence indicates that such receptors confer NK cell functional competence through an unclear process termed “licensing.” Ly49C is the main self-specific inhibitory Ly49 receptor in H-2b C57BL/6 (B6) mice. We used B6 Ly49C-transgenic and B6 β2 microglobulin (β2m)-knockout Ly49C-transgenic mice to investigate the impact of licensing through this inhibitory receptor in precursor and mature NK cells. We found that self-specific inhibitory receptors affected NK cell precursor survival and proliferation at particular developmental stages in an MHC class I–dependent manner. The presence of Ly49C impacted the NK cell repertoire in a β2m-dependent manner, with reduced Ly49A+, Ly49G2+, and Ly49D+ subsets, an increased DNAM-1+ subset, and higher NKG2D expression. Licensed NK cells displayed a skewed distribution of the maturation stages, which was characterized by differential CD27 and CD11b expression, toward the mature phenotypes. We found that Ly49C-mediated licensing induced a split effect on NK cell functions, with increased cytokine-production capabilities following engagement of various activating receptors while cytotoxicity remained unchanged. Analysis of licensed NK cell functions in vivo, in a system of mouse CMV infection, indicated that licensing did not play a major role in the NK cell antiviral response during acute infection, but it strongly impaired the generation and/or persistence of memory NK cells. This study unravels multifaceted effects of licensing on NK cell populations and their functions.

Footnotes

  • This work was supported by the National Health and Medical Research Council of Australia. J.D.C. was supported by National Health and Medical Research Council of Australia Project Grant 1011489, by the Lions Eye Institute, and by the University of Western Australia. M.A.D.-E. is a National Health and Medical Research Council of Australia Principal Research Fellow.

  • The online version of this article contains supplemental material.

  • Received February 2, 2016.
  • Accepted May 3, 2016.
  • Copyright © 2016 by The American Association of Immunologists, Inc.
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The Journal of Immunology: 203 (12)
The Journal of Immunology
Vol. 203, Issue 12
15 Dec 2019
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Ly49C Impairs NK Cell Memory in Mouse Cytomegalovirus Infection
Catherine A. Forbes, Anthony A. Scalzo, Mariapia A. Degli-Esposti, Jerome D. Coudert
The Journal of Immunology May 27, 2016, 1600199; DOI: 10.4049/jimmunol.1600199

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Ly49C Impairs NK Cell Memory in Mouse Cytomegalovirus Infection
Catherine A. Forbes, Anthony A. Scalzo, Mariapia A. Degli-Esposti, Jerome D. Coudert
The Journal of Immunology May 27, 2016, 1600199; DOI: 10.4049/jimmunol.1600199
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Print ISSN 0022-1767        Online ISSN 1550-6606