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Molecular Medicine

Genetic Depletion or Hyperresponsiveness of Natural Killer Cells Do Not Affect Atherosclerosis DevelopmentNovelty and Significance

Wared Nour-Eldine, Jérémie Joffre, Kazem Zibara, Bruno Esposito, Andréas Giraud, Lynda Zeboudj, José Vilar, Megumi Terada, Patrick Bruneval, Eric Vivier, Hafid Ait-Oufella, Ziad Mallat, Sophie Ugolini, Alain Tedgui
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https://doi.org/10.1161/CIRCRESAHA.117.311743
Circulation Research. 2018;122:47-57
Originally published October 18, 2017
Wared Nour-Eldine
From the Institut National de la Santé et de la Recherche Médicale (Inserm), Unit 970, Paris-Cardiovascular Research Center, Université Paris-Descartes, France (W.N.-E., J.J., B.E., A.G., L.Z., J.V., P.B., H.A.-O., Z.M., A.T.); ER045, PRASE (W.N.-E., K.Z.) and Biology Department, Faculty of Sciences-I (K.Z.), Lebanese University, Beirut, Lebanon; Department of Anatomopathology, Hôpital Européen Georges Pompidou, Assistance Publique-Hopitaux de Paris, France (M.T., P.B.); Centre d’Immunologie de Marseille-Luminy, Aix Marseille University, CNRS, INSERM, France (E.V., S.U.); and Division of Cardiovascular Medicine, Department of Medicine, University of Cambridge, United Kingdom (Z.M.).
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Jérémie Joffre
From the Institut National de la Santé et de la Recherche Médicale (Inserm), Unit 970, Paris-Cardiovascular Research Center, Université Paris-Descartes, France (W.N.-E., J.J., B.E., A.G., L.Z., J.V., P.B., H.A.-O., Z.M., A.T.); ER045, PRASE (W.N.-E., K.Z.) and Biology Department, Faculty of Sciences-I (K.Z.), Lebanese University, Beirut, Lebanon; Department of Anatomopathology, Hôpital Européen Georges Pompidou, Assistance Publique-Hopitaux de Paris, France (M.T., P.B.); Centre d’Immunologie de Marseille-Luminy, Aix Marseille University, CNRS, INSERM, France (E.V., S.U.); and Division of Cardiovascular Medicine, Department of Medicine, University of Cambridge, United Kingdom (Z.M.).
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Kazem Zibara
From the Institut National de la Santé et de la Recherche Médicale (Inserm), Unit 970, Paris-Cardiovascular Research Center, Université Paris-Descartes, France (W.N.-E., J.J., B.E., A.G., L.Z., J.V., P.B., H.A.-O., Z.M., A.T.); ER045, PRASE (W.N.-E., K.Z.) and Biology Department, Faculty of Sciences-I (K.Z.), Lebanese University, Beirut, Lebanon; Department of Anatomopathology, Hôpital Européen Georges Pompidou, Assistance Publique-Hopitaux de Paris, France (M.T., P.B.); Centre d’Immunologie de Marseille-Luminy, Aix Marseille University, CNRS, INSERM, France (E.V., S.U.); and Division of Cardiovascular Medicine, Department of Medicine, University of Cambridge, United Kingdom (Z.M.).
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Bruno Esposito
From the Institut National de la Santé et de la Recherche Médicale (Inserm), Unit 970, Paris-Cardiovascular Research Center, Université Paris-Descartes, France (W.N.-E., J.J., B.E., A.G., L.Z., J.V., P.B., H.A.-O., Z.M., A.T.); ER045, PRASE (W.N.-E., K.Z.) and Biology Department, Faculty of Sciences-I (K.Z.), Lebanese University, Beirut, Lebanon; Department of Anatomopathology, Hôpital Européen Georges Pompidou, Assistance Publique-Hopitaux de Paris, France (M.T., P.B.); Centre d’Immunologie de Marseille-Luminy, Aix Marseille University, CNRS, INSERM, France (E.V., S.U.); and Division of Cardiovascular Medicine, Department of Medicine, University of Cambridge, United Kingdom (Z.M.).
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Andréas Giraud
From the Institut National de la Santé et de la Recherche Médicale (Inserm), Unit 970, Paris-Cardiovascular Research Center, Université Paris-Descartes, France (W.N.-E., J.J., B.E., A.G., L.Z., J.V., P.B., H.A.-O., Z.M., A.T.); ER045, PRASE (W.N.-E., K.Z.) and Biology Department, Faculty of Sciences-I (K.Z.), Lebanese University, Beirut, Lebanon; Department of Anatomopathology, Hôpital Européen Georges Pompidou, Assistance Publique-Hopitaux de Paris, France (M.T., P.B.); Centre d’Immunologie de Marseille-Luminy, Aix Marseille University, CNRS, INSERM, France (E.V., S.U.); and Division of Cardiovascular Medicine, Department of Medicine, University of Cambridge, United Kingdom (Z.M.).
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Lynda Zeboudj
From the Institut National de la Santé et de la Recherche Médicale (Inserm), Unit 970, Paris-Cardiovascular Research Center, Université Paris-Descartes, France (W.N.-E., J.J., B.E., A.G., L.Z., J.V., P.B., H.A.-O., Z.M., A.T.); ER045, PRASE (W.N.-E., K.Z.) and Biology Department, Faculty of Sciences-I (K.Z.), Lebanese University, Beirut, Lebanon; Department of Anatomopathology, Hôpital Européen Georges Pompidou, Assistance Publique-Hopitaux de Paris, France (M.T., P.B.); Centre d’Immunologie de Marseille-Luminy, Aix Marseille University, CNRS, INSERM, France (E.V., S.U.); and Division of Cardiovascular Medicine, Department of Medicine, University of Cambridge, United Kingdom (Z.M.).
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José Vilar
From the Institut National de la Santé et de la Recherche Médicale (Inserm), Unit 970, Paris-Cardiovascular Research Center, Université Paris-Descartes, France (W.N.-E., J.J., B.E., A.G., L.Z., J.V., P.B., H.A.-O., Z.M., A.T.); ER045, PRASE (W.N.-E., K.Z.) and Biology Department, Faculty of Sciences-I (K.Z.), Lebanese University, Beirut, Lebanon; Department of Anatomopathology, Hôpital Européen Georges Pompidou, Assistance Publique-Hopitaux de Paris, France (M.T., P.B.); Centre d’Immunologie de Marseille-Luminy, Aix Marseille University, CNRS, INSERM, France (E.V., S.U.); and Division of Cardiovascular Medicine, Department of Medicine, University of Cambridge, United Kingdom (Z.M.).
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Megumi Terada
From the Institut National de la Santé et de la Recherche Médicale (Inserm), Unit 970, Paris-Cardiovascular Research Center, Université Paris-Descartes, France (W.N.-E., J.J., B.E., A.G., L.Z., J.V., P.B., H.A.-O., Z.M., A.T.); ER045, PRASE (W.N.-E., K.Z.) and Biology Department, Faculty of Sciences-I (K.Z.), Lebanese University, Beirut, Lebanon; Department of Anatomopathology, Hôpital Européen Georges Pompidou, Assistance Publique-Hopitaux de Paris, France (M.T., P.B.); Centre d’Immunologie de Marseille-Luminy, Aix Marseille University, CNRS, INSERM, France (E.V., S.U.); and Division of Cardiovascular Medicine, Department of Medicine, University of Cambridge, United Kingdom (Z.M.).
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Patrick Bruneval
From the Institut National de la Santé et de la Recherche Médicale (Inserm), Unit 970, Paris-Cardiovascular Research Center, Université Paris-Descartes, France (W.N.-E., J.J., B.E., A.G., L.Z., J.V., P.B., H.A.-O., Z.M., A.T.); ER045, PRASE (W.N.-E., K.Z.) and Biology Department, Faculty of Sciences-I (K.Z.), Lebanese University, Beirut, Lebanon; Department of Anatomopathology, Hôpital Européen Georges Pompidou, Assistance Publique-Hopitaux de Paris, France (M.T., P.B.); Centre d’Immunologie de Marseille-Luminy, Aix Marseille University, CNRS, INSERM, France (E.V., S.U.); and Division of Cardiovascular Medicine, Department of Medicine, University of Cambridge, United Kingdom (Z.M.).
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Eric Vivier
From the Institut National de la Santé et de la Recherche Médicale (Inserm), Unit 970, Paris-Cardiovascular Research Center, Université Paris-Descartes, France (W.N.-E., J.J., B.E., A.G., L.Z., J.V., P.B., H.A.-O., Z.M., A.T.); ER045, PRASE (W.N.-E., K.Z.) and Biology Department, Faculty of Sciences-I (K.Z.), Lebanese University, Beirut, Lebanon; Department of Anatomopathology, Hôpital Européen Georges Pompidou, Assistance Publique-Hopitaux de Paris, France (M.T., P.B.); Centre d’Immunologie de Marseille-Luminy, Aix Marseille University, CNRS, INSERM, France (E.V., S.U.); and Division of Cardiovascular Medicine, Department of Medicine, University of Cambridge, United Kingdom (Z.M.).
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Hafid Ait-Oufella
From the Institut National de la Santé et de la Recherche Médicale (Inserm), Unit 970, Paris-Cardiovascular Research Center, Université Paris-Descartes, France (W.N.-E., J.J., B.E., A.G., L.Z., J.V., P.B., H.A.-O., Z.M., A.T.); ER045, PRASE (W.N.-E., K.Z.) and Biology Department, Faculty of Sciences-I (K.Z.), Lebanese University, Beirut, Lebanon; Department of Anatomopathology, Hôpital Européen Georges Pompidou, Assistance Publique-Hopitaux de Paris, France (M.T., P.B.); Centre d’Immunologie de Marseille-Luminy, Aix Marseille University, CNRS, INSERM, France (E.V., S.U.); and Division of Cardiovascular Medicine, Department of Medicine, University of Cambridge, United Kingdom (Z.M.).
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Ziad Mallat
From the Institut National de la Santé et de la Recherche Médicale (Inserm), Unit 970, Paris-Cardiovascular Research Center, Université Paris-Descartes, France (W.N.-E., J.J., B.E., A.G., L.Z., J.V., P.B., H.A.-O., Z.M., A.T.); ER045, PRASE (W.N.-E., K.Z.) and Biology Department, Faculty of Sciences-I (K.Z.), Lebanese University, Beirut, Lebanon; Department of Anatomopathology, Hôpital Européen Georges Pompidou, Assistance Publique-Hopitaux de Paris, France (M.T., P.B.); Centre d’Immunologie de Marseille-Luminy, Aix Marseille University, CNRS, INSERM, France (E.V., S.U.); and Division of Cardiovascular Medicine, Department of Medicine, University of Cambridge, United Kingdom (Z.M.).
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Sophie Ugolini
From the Institut National de la Santé et de la Recherche Médicale (Inserm), Unit 970, Paris-Cardiovascular Research Center, Université Paris-Descartes, France (W.N.-E., J.J., B.E., A.G., L.Z., J.V., P.B., H.A.-O., Z.M., A.T.); ER045, PRASE (W.N.-E., K.Z.) and Biology Department, Faculty of Sciences-I (K.Z.), Lebanese University, Beirut, Lebanon; Department of Anatomopathology, Hôpital Européen Georges Pompidou, Assistance Publique-Hopitaux de Paris, France (M.T., P.B.); Centre d’Immunologie de Marseille-Luminy, Aix Marseille University, CNRS, INSERM, France (E.V., S.U.); and Division of Cardiovascular Medicine, Department of Medicine, University of Cambridge, United Kingdom (Z.M.).
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Alain Tedgui
From the Institut National de la Santé et de la Recherche Médicale (Inserm), Unit 970, Paris-Cardiovascular Research Center, Université Paris-Descartes, France (W.N.-E., J.J., B.E., A.G., L.Z., J.V., P.B., H.A.-O., Z.M., A.T.); ER045, PRASE (W.N.-E., K.Z.) and Biology Department, Faculty of Sciences-I (K.Z.), Lebanese University, Beirut, Lebanon; Department of Anatomopathology, Hôpital Européen Georges Pompidou, Assistance Publique-Hopitaux de Paris, France (M.T., P.B.); Centre d’Immunologie de Marseille-Luminy, Aix Marseille University, CNRS, INSERM, France (E.V., S.U.); and Division of Cardiovascular Medicine, Department of Medicine, University of Cambridge, United Kingdom (Z.M.).
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Abstract

Rationale: Chronic inflammation is central in the development of atherosclerosis. Both innate and adaptive immunities are involved. Although several studies have evaluated the functions of natural killer (NK) cells in experimental animal models of atherosclerosis, it is not yet clear whether NK cells behave as protective or proatherogenic effectors. One of the main caveats of previous studies was the lack of specificity in targeting loss or gain of function of NK cells.

Objectives: We used 2 selective genetic approaches to investigate the role of NK cells in atherosclerosis: (1) Ncr1iCre/+R26lsl−DTA/+ mice in which NK cells were depleted and (2) Noé mice in which NK cells are hyperresponsive.

Methods and Results: No difference in atherosclerotic lesion size was found in Ldlr−/− (low-density lipoprotein receptor null) mice transplanted with bone marrow (BM) cells from Ncr1iCreR26Rlsl−DTA, Noé, or wild-type mice. Also, no difference was observed in plaque composition in terms of collagen content, macrophage infiltration, or the immune profile, although Noé chimera had more IFN (interferon)-γ–producing NK cells, compared with wild-type mice. Then, we investigated the NK-cell selectivity of anti–asialoganglioside M1 antiserum, which was previously used to conclude the proatherogenicity of NK cells. Anti–asialoganglioside M1 treatment decreased atherosclerosis in both Ldlr−/− mice transplanted with Ncr1iCreR26Rlsl−DTA or wild-type bone marrow, indicating that its antiatherogenic effects are unrelated to NK-cell depletion, but to CD8+ T and NKT cells. Finally, to determine whether NK cells could contribute to the disease in conditions of pathological NK-cell overactivation, we treated irradiated Ldlr−/− mice reconstituted with either wild-type or Ncr1iCreR26Rlsl−DTA bone marrow with the viral mimic polyinosinic:polycytidylic acid and found a significant reduction of plaque size in NK-cell–deficient chimeric mice.

Conclusions: Our findings, using state-of-the-art mouse models, demonstrate that NK cells have no direct effect on the natural development of hypercholesterolemia-induced atherosclerosis, but may play a role when an additional systemic NK-cell overactivation occurs.

  • atherosclerosis
  • immune system
  • inflammation
  • macrophages
  • mice
  • Received July 21, 2017.
  • Revision received October 12, 2017.
  • Accepted October 17, 2016.
  • © 2017 American Heart Association, Inc.

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January 5, 2018, Volume 122, Issue 1
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    Genetic Depletion or Hyperresponsiveness of Natural Killer Cells Do Not Affect Atherosclerosis DevelopmentNovelty and Significance
    Wared Nour-Eldine, Jérémie Joffre, Kazem Zibara, Bruno Esposito, Andréas Giraud, Lynda Zeboudj, José Vilar, Megumi Terada, Patrick Bruneval, Eric Vivier, Hafid Ait-Oufella, Ziad Mallat, Sophie Ugolini and Alain Tedgui
    Circulation Research. 2018;122:47-57, originally published October 18, 2017
    https://doi.org/10.1161/CIRCRESAHA.117.311743

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    Genetic Depletion or Hyperresponsiveness of Natural Killer Cells Do Not Affect Atherosclerosis DevelopmentNovelty and Significance
    Wared Nour-Eldine, Jérémie Joffre, Kazem Zibara, Bruno Esposito, Andréas Giraud, Lynda Zeboudj, José Vilar, Megumi Terada, Patrick Bruneval, Eric Vivier, Hafid Ait-Oufella, Ziad Mallat, Sophie Ugolini and Alain Tedgui
    Circulation Research. 2018;122:47-57, originally published October 18, 2017
    https://doi.org/10.1161/CIRCRESAHA.117.311743
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