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July 2019; 6 (4) ArticleOpen Access

Harmful neutrophil subsets in patients with ischemic stroke

Association with disease severity

David Weisenburger-Lile, Yuan Dong, Marion Yger, Gaëlle Weisenburger, Giulia Frasca Polara, Thomas Chaigneau, Riccardo Zapata Ochoa, Beatrice Marro, Bertrand Lapergue, Sonia Alamowitch, Carole Elbim
First published May 15, 2019, DOI: https://doi.org/10.1212/NXI.0000000000000571
David Weisenburger-Lile
From the Sorbonne Universités (D.W.-L., Y.D., T.C., R.Z.O., S.A., C.E.), UPMC Univ Paris 06, UMRS 938, CdR Saint-Antoine, Hôpital Saint-Antoine; INSERM (D.W.-L., Y.D., T.C., R.Z.O., S.A., C.E.), UMRS 938, CdR Saint- Antoine, Team “Immune System, Neuroinflammation and Neurodegenerative Diseases,” Hôpital St-Antoine; Service de Neurologie et d'Urgences Neurovasculaires (D.W.-L., M.Y., S.A.), Assistance Publique-Hôpitaux de Paris, Hôpital Saint-Antoine; Division of Pneumology (G.W.), Foch Hospital, F-92150, Suresnes; Division of Neurology (G.F.P.), Stroke Center, Assistance Publique-Hôpitaux de Paris, Pitié-Salpêtrière Hospital; Division of Radiology (B.M.), Assistance Publique-Hôpitaux de Paris, Hôpital Saint-Antoine; and Division of Neurology (B.L.), Stroke Center, Foch Hospital, F-92150, Suresnes.
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Yuan Dong
From the Sorbonne Universités (D.W.-L., Y.D., T.C., R.Z.O., S.A., C.E.), UPMC Univ Paris 06, UMRS 938, CdR Saint-Antoine, Hôpital Saint-Antoine; INSERM (D.W.-L., Y.D., T.C., R.Z.O., S.A., C.E.), UMRS 938, CdR Saint- Antoine, Team “Immune System, Neuroinflammation and Neurodegenerative Diseases,” Hôpital St-Antoine; Service de Neurologie et d'Urgences Neurovasculaires (D.W.-L., M.Y., S.A.), Assistance Publique-Hôpitaux de Paris, Hôpital Saint-Antoine; Division of Pneumology (G.W.), Foch Hospital, F-92150, Suresnes; Division of Neurology (G.F.P.), Stroke Center, Assistance Publique-Hôpitaux de Paris, Pitié-Salpêtrière Hospital; Division of Radiology (B.M.), Assistance Publique-Hôpitaux de Paris, Hôpital Saint-Antoine; and Division of Neurology (B.L.), Stroke Center, Foch Hospital, F-92150, Suresnes.
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Marion Yger
From the Sorbonne Universités (D.W.-L., Y.D., T.C., R.Z.O., S.A., C.E.), UPMC Univ Paris 06, UMRS 938, CdR Saint-Antoine, Hôpital Saint-Antoine; INSERM (D.W.-L., Y.D., T.C., R.Z.O., S.A., C.E.), UMRS 938, CdR Saint- Antoine, Team “Immune System, Neuroinflammation and Neurodegenerative Diseases,” Hôpital St-Antoine; Service de Neurologie et d'Urgences Neurovasculaires (D.W.-L., M.Y., S.A.), Assistance Publique-Hôpitaux de Paris, Hôpital Saint-Antoine; Division of Pneumology (G.W.), Foch Hospital, F-92150, Suresnes; Division of Neurology (G.F.P.), Stroke Center, Assistance Publique-Hôpitaux de Paris, Pitié-Salpêtrière Hospital; Division of Radiology (B.M.), Assistance Publique-Hôpitaux de Paris, Hôpital Saint-Antoine; and Division of Neurology (B.L.), Stroke Center, Foch Hospital, F-92150, Suresnes.
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Gaëlle Weisenburger
From the Sorbonne Universités (D.W.-L., Y.D., T.C., R.Z.O., S.A., C.E.), UPMC Univ Paris 06, UMRS 938, CdR Saint-Antoine, Hôpital Saint-Antoine; INSERM (D.W.-L., Y.D., T.C., R.Z.O., S.A., C.E.), UMRS 938, CdR Saint- Antoine, Team “Immune System, Neuroinflammation and Neurodegenerative Diseases,” Hôpital St-Antoine; Service de Neurologie et d'Urgences Neurovasculaires (D.W.-L., M.Y., S.A.), Assistance Publique-Hôpitaux de Paris, Hôpital Saint-Antoine; Division of Pneumology (G.W.), Foch Hospital, F-92150, Suresnes; Division of Neurology (G.F.P.), Stroke Center, Assistance Publique-Hôpitaux de Paris, Pitié-Salpêtrière Hospital; Division of Radiology (B.M.), Assistance Publique-Hôpitaux de Paris, Hôpital Saint-Antoine; and Division of Neurology (B.L.), Stroke Center, Foch Hospital, F-92150, Suresnes.
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Giulia Frasca Polara
From the Sorbonne Universités (D.W.-L., Y.D., T.C., R.Z.O., S.A., C.E.), UPMC Univ Paris 06, UMRS 938, CdR Saint-Antoine, Hôpital Saint-Antoine; INSERM (D.W.-L., Y.D., T.C., R.Z.O., S.A., C.E.), UMRS 938, CdR Saint- Antoine, Team “Immune System, Neuroinflammation and Neurodegenerative Diseases,” Hôpital St-Antoine; Service de Neurologie et d'Urgences Neurovasculaires (D.W.-L., M.Y., S.A.), Assistance Publique-Hôpitaux de Paris, Hôpital Saint-Antoine; Division of Pneumology (G.W.), Foch Hospital, F-92150, Suresnes; Division of Neurology (G.F.P.), Stroke Center, Assistance Publique-Hôpitaux de Paris, Pitié-Salpêtrière Hospital; Division of Radiology (B.M.), Assistance Publique-Hôpitaux de Paris, Hôpital Saint-Antoine; and Division of Neurology (B.L.), Stroke Center, Foch Hospital, F-92150, Suresnes.
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Thomas Chaigneau
From the Sorbonne Universités (D.W.-L., Y.D., T.C., R.Z.O., S.A., C.E.), UPMC Univ Paris 06, UMRS 938, CdR Saint-Antoine, Hôpital Saint-Antoine; INSERM (D.W.-L., Y.D., T.C., R.Z.O., S.A., C.E.), UMRS 938, CdR Saint- Antoine, Team “Immune System, Neuroinflammation and Neurodegenerative Diseases,” Hôpital St-Antoine; Service de Neurologie et d'Urgences Neurovasculaires (D.W.-L., M.Y., S.A.), Assistance Publique-Hôpitaux de Paris, Hôpital Saint-Antoine; Division of Pneumology (G.W.), Foch Hospital, F-92150, Suresnes; Division of Neurology (G.F.P.), Stroke Center, Assistance Publique-Hôpitaux de Paris, Pitié-Salpêtrière Hospital; Division of Radiology (B.M.), Assistance Publique-Hôpitaux de Paris, Hôpital Saint-Antoine; and Division of Neurology (B.L.), Stroke Center, Foch Hospital, F-92150, Suresnes.
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Riccardo Zapata Ochoa
From the Sorbonne Universités (D.W.-L., Y.D., T.C., R.Z.O., S.A., C.E.), UPMC Univ Paris 06, UMRS 938, CdR Saint-Antoine, Hôpital Saint-Antoine; INSERM (D.W.-L., Y.D., T.C., R.Z.O., S.A., C.E.), UMRS 938, CdR Saint- Antoine, Team “Immune System, Neuroinflammation and Neurodegenerative Diseases,” Hôpital St-Antoine; Service de Neurologie et d'Urgences Neurovasculaires (D.W.-L., M.Y., S.A.), Assistance Publique-Hôpitaux de Paris, Hôpital Saint-Antoine; Division of Pneumology (G.W.), Foch Hospital, F-92150, Suresnes; Division of Neurology (G.F.P.), Stroke Center, Assistance Publique-Hôpitaux de Paris, Pitié-Salpêtrière Hospital; Division of Radiology (B.M.), Assistance Publique-Hôpitaux de Paris, Hôpital Saint-Antoine; and Division of Neurology (B.L.), Stroke Center, Foch Hospital, F-92150, Suresnes.
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Beatrice Marro
From the Sorbonne Universités (D.W.-L., Y.D., T.C., R.Z.O., S.A., C.E.), UPMC Univ Paris 06, UMRS 938, CdR Saint-Antoine, Hôpital Saint-Antoine; INSERM (D.W.-L., Y.D., T.C., R.Z.O., S.A., C.E.), UMRS 938, CdR Saint- Antoine, Team “Immune System, Neuroinflammation and Neurodegenerative Diseases,” Hôpital St-Antoine; Service de Neurologie et d'Urgences Neurovasculaires (D.W.-L., M.Y., S.A.), Assistance Publique-Hôpitaux de Paris, Hôpital Saint-Antoine; Division of Pneumology (G.W.), Foch Hospital, F-92150, Suresnes; Division of Neurology (G.F.P.), Stroke Center, Assistance Publique-Hôpitaux de Paris, Pitié-Salpêtrière Hospital; Division of Radiology (B.M.), Assistance Publique-Hôpitaux de Paris, Hôpital Saint-Antoine; and Division of Neurology (B.L.), Stroke Center, Foch Hospital, F-92150, Suresnes.
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Bertrand Lapergue
From the Sorbonne Universités (D.W.-L., Y.D., T.C., R.Z.O., S.A., C.E.), UPMC Univ Paris 06, UMRS 938, CdR Saint-Antoine, Hôpital Saint-Antoine; INSERM (D.W.-L., Y.D., T.C., R.Z.O., S.A., C.E.), UMRS 938, CdR Saint- Antoine, Team “Immune System, Neuroinflammation and Neurodegenerative Diseases,” Hôpital St-Antoine; Service de Neurologie et d'Urgences Neurovasculaires (D.W.-L., M.Y., S.A.), Assistance Publique-Hôpitaux de Paris, Hôpital Saint-Antoine; Division of Pneumology (G.W.), Foch Hospital, F-92150, Suresnes; Division of Neurology (G.F.P.), Stroke Center, Assistance Publique-Hôpitaux de Paris, Pitié-Salpêtrière Hospital; Division of Radiology (B.M.), Assistance Publique-Hôpitaux de Paris, Hôpital Saint-Antoine; and Division of Neurology (B.L.), Stroke Center, Foch Hospital, F-92150, Suresnes.
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Sonia Alamowitch
From the Sorbonne Universités (D.W.-L., Y.D., T.C., R.Z.O., S.A., C.E.), UPMC Univ Paris 06, UMRS 938, CdR Saint-Antoine, Hôpital Saint-Antoine; INSERM (D.W.-L., Y.D., T.C., R.Z.O., S.A., C.E.), UMRS 938, CdR Saint- Antoine, Team “Immune System, Neuroinflammation and Neurodegenerative Diseases,” Hôpital St-Antoine; Service de Neurologie et d'Urgences Neurovasculaires (D.W.-L., M.Y., S.A.), Assistance Publique-Hôpitaux de Paris, Hôpital Saint-Antoine; Division of Pneumology (G.W.), Foch Hospital, F-92150, Suresnes; Division of Neurology (G.F.P.), Stroke Center, Assistance Publique-Hôpitaux de Paris, Pitié-Salpêtrière Hospital; Division of Radiology (B.M.), Assistance Publique-Hôpitaux de Paris, Hôpital Saint-Antoine; and Division of Neurology (B.L.), Stroke Center, Foch Hospital, F-92150, Suresnes.
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Carole Elbim
From the Sorbonne Universités (D.W.-L., Y.D., T.C., R.Z.O., S.A., C.E.), UPMC Univ Paris 06, UMRS 938, CdR Saint-Antoine, Hôpital Saint-Antoine; INSERM (D.W.-L., Y.D., T.C., R.Z.O., S.A., C.E.), UMRS 938, CdR Saint- Antoine, Team “Immune System, Neuroinflammation and Neurodegenerative Diseases,” Hôpital St-Antoine; Service de Neurologie et d'Urgences Neurovasculaires (D.W.-L., M.Y., S.A.), Assistance Publique-Hôpitaux de Paris, Hôpital Saint-Antoine; Division of Pneumology (G.W.), Foch Hospital, F-92150, Suresnes; Division of Neurology (G.F.P.), Stroke Center, Assistance Publique-Hôpitaux de Paris, Pitié-Salpêtrière Hospital; Division of Radiology (B.M.), Assistance Publique-Hôpitaux de Paris, Hôpital Saint-Antoine; and Division of Neurology (B.L.), Stroke Center, Foch Hospital, F-92150, Suresnes.
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Citation
Harmful neutrophil subsets in patients with ischemic stroke
Association with disease severity
David Weisenburger-Lile, Yuan Dong, Marion Yger, Gaëlle Weisenburger, Giulia Frasca Polara, Thomas Chaigneau, Riccardo Zapata Ochoa, Beatrice Marro, Bertrand Lapergue, Sonia Alamowitch, Carole Elbim
Neurol Neuroimmunol Neuroinflamm Jul 2019, 6 (4) e571; DOI: 10.1212/NXI.0000000000000571

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    Figure 1 Hyperactivation of circulating neutrophils from patients with ischemic stroke

    (A–E) Adhesion molecules expression, polymorphonuclear neutrophil (PMN) elastase, and ROS production were studied in patients with IS at inclusion. Expression of CD62L (A) and CD11b (B) at the surface of resting PMNs was studied on whole-blood samples kept on ice and incubeted with anti-CD62L and anti-CD11b monoclonal antibodies. Results are expressed as mean fluorescence intensity (MFI). (C) Circulating levels of PMN elastase were quantified by ELISA; results are expressed as ng/mL. (D and E) ROS production by unstimulated PMNs was studied after treatment of whole-blood samples for 50 minutes with PBS; results are expressed as MFI (D). ROS production by stimulated PMNs was measured after pretreatment of whole-blood samples for 45 minutes with PBS, Pam3CSK4 (TLR1/2 agonist, 1 μg/mL), or LPS (TLR4 agonist, 10 ng/mL), or TNF-α (TNF, 5 ng/mL) and incubation for 5 minutes with fMLP (10−6 M); results are expressed as MFI (E). (F–J) Follow-up of surface expression of CD62L (F), surface expression of CD11b (G), circulating levels of PMN elastase (H), and ROS production by unstimulated (I) and stimulated PMNs (J) during the first week after IS symptoms. All samples came from age-matched HCs, (n = 22) and patients with IS at day 0 (n = 27), day 2 (n = 14), and day 7 (n = 14). Values are mean ± SEM. *Significantly different from controls p < 0.05, **p < 0.01, ***p < 0.001, adjusted for age. D0 = day 0; D2 = day 2; D7 = day 7; fMLP = N-formylmethionyl-leucyl-phenylalanine; HC = healthy control; IS = ischemic stroke; LPS = lipopolysaccharide; ROS = reactive oxygen species; SEM = standard error of mean; TLR = Toll-like receptor; TNF = tumor necrosis factor.

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    Figure 2 Deregulation of neutrophil death in patients with ischemic stroke

    (A–D) Polymorphonuclear neutrophil (PMN) death was measured immediately after sampling by staining with annexin V and 7-AAD. Results are expressed as the percentages of apoptotic (A and B) and necrotic (C and D) PMNs. (A and C) Values of PMN death in patients with IS at inclusion. (B and D) Follow-up of PMN death during the first week after IS symptoms. (E and F) Circulating NETs were quantified by MPO-DNA complex ELISA; results are expressed as ng/μL DNA. Values of circulating NETs in patients with IS at inclusion (E). Follow-up of intravascular NETosis during the first week after IS symptoms (F). All samples came from age-matched healthy controls (HCs, n = 22) and patients with IS at day 0 (n = 27), day 2 (n = 14), and day 7 (n = 14). Values are mean ± SEM. *Significantly different from controls p < 0.05, **p < 0.01, ***p < 0.001, adjusted for age. AAD = amino-actinomycin D; D0 = day 0; D2 = day 2; D7 = day 7; HC = healthy control; IS = ischemic stroke; MPO = myeloperoxidase; NET = neutrophil extracellular trap; SEM = standard error of mean.

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    Figure 3 Impaired homeostasis of the circulating neutrophils in patients with ischemic stroke

    (A–E) Analysis of senescent and immunosuppressive polymorphonuclear neutrophil (PMN) subsets in patients with IS at inclusion. Whole-blood samples were incubated for 45 minutes at 4°C with Pe-Cy7-anti-human CXCR4, PE-anti-human CD11b, and APC-antihuman CD62L (A and B) or with FITC-anti-human CD16, PE-anti-human CD11c, Pe-Cy7-antihuman CD11b, and APC-anti-human CD62L (C and D) antibodies. (A) Representative dot plots of the PMN phenotype according to CXCR4 and CD62L expression in a HC (left) and a patient with IS (right). (B) Representative dot plots of the PMN phenotype according to CD16 and CD62L expression in an HC (left) and a patient with IS (right). (C) Percentages of the CXCR4bright/CD62Ldim senescent PMN subset. (D) Percentages of the CD16bright/CD62Ldim immunosuppressive PMN subset. (E) Ratio between the senescent and the immunosuppressive PMN subsets. (F–H) Follow-up of senescent PMN subset (F), immunosuppressive PMN subset (G), and ratio between the senescent and the immunosuppressive PMN subsets (H) during the first week after IS symptoms. All samples came from age-matched HCs, (n = 22) and patients with IS at day 0 (n = 27), day 2 (n = 14), and day 7 (n = 14). Values are mean ± SEM. *Significantly different from controls p < 0.05, **p < 0.01, ***p < 0.001, adjusted for age. D0 = day 0; D2 = day 2; D7 = day 7; HC = healthy control; IS = ischemic stroke; SEM = standard error of mean.

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    Figure 4 Patients with ischemic stroke have higher levels of soluble JAM-C and of PMN reverse transmigration

    (A and B) sJAM-C was quantified by ELISA; results are expressed as pg/mL. (A) Values of sJAM-C in age-matched HCs, (n = 22) and patients with IS at inclusion (n = 27) (patients included in set 1). (B) Follow-up of sJAM-C levels during the first week after IS symptoms in 10 patients. (C) Correlation between the levels of sJAM-C and of circulating PMN elastase. (D and E) Quantification of rTEM PMNs in patients with IS included in set 2. Whole-blood samples were incubated for 45 minutes at 4°C with FITCanti-human CD181 and PE-anti-human CD54 antibodies. (D) Representative dot plots of the PMN phenotype according to CXCR4 and CD62L expression in an HC (left) and a patient with IS (right). (E) Percentages of the rTEM PMN subset (CD54high, CXCR1low) in age-matched HCs (n = 17) and patients with IS at inclusion (n = 14). (F) Correlation between the percentage of rTEM PMN subset and the level of sJAM-C in patients with IS included in the set 2. *Significantly different from controls p < 0.05, **p < 0.01, ***p < 0.001, adjusted for age. D0 = day 0; D2 = day 2; D7 = day 7; HC = healthy control; IS = ischemic stroke; PMN = polymorphonuclear neutrophil; rTEM = reverse transendothelial migration; sJAM-C = soluble JAM-C.

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    Figure 5 Neutrophil hyperactivation is associated with disease severity

    (A and B) Expression of CD62L (A) and CD11b (B) at the surface of resting polymorphonuclear neutrophils (PMNs). Results are expressed as MFI. (C) Circulating levels of neutrophil elastase were quantified by ELISA. (D) ROS production by unstimulated PMNs; results are expressed in MFI. (E) Percentages of the CXCR4bright/CD62Ldim senescent PMN subset. (F) Percentages of the CD16bright/CD62Ldim immunosuppressive PMN subset. (G) sJAM-C was quantified by ELISA; results are expressed as pg/mL (H) PMN apoptosis was measured immediately after sampling by staining with annexin V and 7-AAD. Results are expressed as percentages of apoptotic PMNs. All measurements came from patients with minor-to-moderate stroke (IS NHISS ≤ 12, n = 17) and patients with severe stroke (IS NHISS > 12, n = 10) at the inclusion. Values are mean ± SEM. Statistical significance as determined by the nonparametric Mann-Whitney test is indicated. *Significantly different p < 0.05, **p < 0.01, ***p < 0.001. Correlation between the NIHSS score at inclusion and CD62L expression at the PMN surface (I), ROS production by unstimulated PMNs (J), ROS production by LPS-stimulated PMNs (K), percentage of the CXCR4bright/CD62Ldim senescent PMN subset (L), sJAM-C level (M), and percentage of rTEM PMNs (N). AAD = amino-actinomycin D; D0 = day 0; IS = ischemic stroke; LPS = lipopolysaccharide; MFi = mean fluorescence intensity; NIHSS = NIH Stroke Scale; PMN = polymorphonuclear neutrophil; ROS = reactive oxygen species; SEM = standard error of mean; sJAM-C = soluble JAM-C.

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    Figure 6 Proinflammatory mediators in patients with ischemic stroke

    (A) Circulating levels of pro- and anti-inflammatory cytokines were measured with Luminex assays in samples from controls (HCs, n = 22) and patients with IS at day 0 (n = 27). (B and C) Circulating levels of HMGB1 were measured in serum by ELISA. (B) Comparative analysis of circulating levels of HMGB1 between age-matched HCs (n = 22) and patients with IS (IS) at day 0 (n = 27). (C) Follow-up of circulating levels of HMGB1 in patients with IS at day 0, 2, and 7. Values are mean ± SEM. *Significantly different from controls p < 0.05, **p < 0.01, ***p < 0.001, adjusted for age. Correlation between circulating levels of HMGB1 at day 0 and the NIHSS score at day 0 (D). (E–G) Correlation between circulating levels of HMGB1 at day 0 and PMN activation markers at day 0: PMN surface expression of CD62L (E) and of CD11b (F) and ROS production by LPS-stimulated PMNs (G). D0 = day 0; D2 = day 2; D7 = day 7; HC = healthy control; HMGB = high-mobility group box; IS = ischemic stroke; LPS = lipopolysaccharide; NIHSS = NIH Stroke Scale; PMN = polymorphonuclear neutrophil; ROS = reactive oxygen species; SEM = standard error of mean.

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Neurology - Neuroimmunology Neuroinflammation: 10 (3)

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Neurology: Neuroimmunology & Neuroinflammation
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