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Cancer Immunology Research
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Research Article

CD16+NKG2Ahigh Natural Killer cells infiltrate breast cancer draining lymph nodes

Alexandra Frazao, Meriem Messaoudene, Nicolas Núñez, Nicolas Dulphy, France Roussin, Christine Sedlik, Laurence Zitvogel, Eliane Piaggio, Antoine Toubert and Anne Caignard
Alexandra Frazao
1Institut Universitaire d'Hématologie, INSERM UMRS1160
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Meriem Messaoudene
2Research, CRCHUM
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Nicolas Núñez
3SiRIC TransImm «Translational Immunotherapy Team», Translational Research Department, Research Center, PSL Research University, INSERM U932, Institut Curie, F-75005
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Nicolas Dulphy
4Institut Universitaire d'Hematologie, Universite Paris Diderot
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France Roussin
5Service Anesthésie et Réanimation, CHU Saint-Louis-Lariboisière
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Christine Sedlik
6SiRIC TransImm «Translational Immunotherapy Team», Translational Research Department, Centre d'Investigation Clinique Biothérapie, Research Center - Institut Curie,PSL Research University, INSERM U932, F-75005
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Laurence Zitvogel
7INSERM-CIC Institut Gustave Roussy
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Eliane Piaggio
3SiRIC TransImm «Translational Immunotherapy Team», Translational Research Department, Research Center, PSL Research University, INSERM U932, Institut Curie, F-75005
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Antoine Toubert
8Institut Universitaire d'Hematologie, INSERM UMRS1160
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Anne Caignard
8Institut Universitaire d'Hematologie, INSERM UMRS1160
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  • For correspondence: anne.caignard@inserm.fr
DOI: 10.1158/2326-6066.CIR-18-0085
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Abstract

Tumor-draining lymph nodes (TD-LNs) are the first site of metastasis of breast cancer (BC). Natural killer (NK) cells that infiltrate TD-LNs (including non-invaded (NI) or metastatic (M)-LNs from BC patients) and NK cells from healthy donor (HD)-LN were characterized, and their phenotype analyzed by flow cytometry. Low percentages of tumor cells invaded M-LNs, and these cells expressed ULBP2 and HLA class I molecules. Although NK cells from paired NI and M-LNs were similar, they expressed different markers compared to HD-LN NK cells. Compared to HD-LNs, TD-LN NK cells expressed activating DNAM-1, NKG2C and inhibitory NKG2A receptors, and exhibited elevated CXCR3 expression. CD16, NKG2A, and NKp46 expression were shown to be increased in stage IIIA BC patients. TD-LNs contained a large proportion of activated CD56brightCD16+ NK cells with high expression of NKG2A. We also showed that a subset of LN NK cells expressed PD-1, expression of which was correlated with NKp30 and NKG2C expression. LN NK cell activation status was evaluated by degranulation potential and lytic capacity towards BC cells. NK cells from TD-LNs degranulated after coculture with BC cell lines. Cytokine-activated TD-LN NK cells exerted greater lysis of BC cell lines than HD-LN NK cells and preferentially lysed the HLA class Ilow MCF-7 BC cell line. TD-LNs from BC patients, thus, contained activated lytic NK cells. The expression of inhibitory receptor NKG2A and checkpoint PD-1 by NK cells infiltrating BC-draining LNs supports their potential as targets for immunotherapies using anti-NKG2A and/or anti-PD-1.

  • Received February 14, 2018.
  • Revision received July 3, 2018.
  • Accepted November 27, 2018.
  • Copyright ©2018, American Association for Cancer Research.
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This OnlineFirst version was published on December 4, 2018
doi: 10.1158/2326-6066.CIR-18-0085

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CD16+NKG2Ahigh Natural Killer cells infiltrate breast cancer draining lymph nodes
Alexandra Frazao, Meriem Messaoudene, Nicolas Núñez, Nicolas Dulphy, France Roussin, Christine Sedlik, Laurence Zitvogel, Eliane Piaggio, Antoine Toubert and Anne Caignard
Cancer Immunol Res December 4 2018 DOI: 10.1158/2326-6066.CIR-18-0085

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CD16+NKG2Ahigh Natural Killer cells infiltrate breast cancer draining lymph nodes
Alexandra Frazao, Meriem Messaoudene, Nicolas Núñez, Nicolas Dulphy, France Roussin, Christine Sedlik, Laurence Zitvogel, Eliane Piaggio, Antoine Toubert and Anne Caignard
Cancer Immunol Res December 4 2018 DOI: 10.1158/2326-6066.CIR-18-0085
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