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Interactions between eosinophils and IL-5Rα-positive mast cells in nonadvanced systemic mastocytosis.
Lefèvre, Guillaume; Gibier, Jean-Baptiste; Bongiovanni, Antonino; Lhermitte, Ludovic; Rossignol, Julien; Anglo, Emilie; Dendooven, Arnaud; Dubois, Romain; Terriou, Louis; Launay, David; Barete, Stéphane; Esnault, Stéphane; Frenzel, Laurent; Gourguechon, Clément; Ballul, Thomas; Dezoteux, Frédéric; Staumont-Salle, Delphine; Copin, Marie-Christine; Rignault-Bricard, Rachel; Maciel, Thiago Trovati; Damaj, Gandhi; Tardivel, Meryem; Crinquette-Verhasselt, Marie; Dubreuil, Patrice; Maouche-Chrétien, Leila; Bruneau, Julie; Lortholary, Olivier; Duployez, Nicolas; Behal, Hélène; Molina, Thierry Jo; Hermine, Olivier.
Affiliation
  • Lefèvre G; University of Lille, Institut National de la Santé et de la Recherche Médicale (INSERM), Centre Hospitalier Universitaire (CHU) Lille, and Institute for Translational Research in Inflammation (INFINITE), Lille, France; Institut d'Immunologie, CHU Lille, Lille, France; National Reference Center for H
  • Gibier JB; University of Lille, Institut de Pathologie, Centre de Biopathologie, CHU Lille, Lille, France.
  • Bongiovanni A; Centre National de la Recherche Scientifique (CNRS), INSERM, CHU Lille, University of Lille, Institut Pasteur de Lille, Lille, France.
  • Lhermitte L; Laboratoire d'Onco-Hématologie, Hôpital Necker-Enfants Malades, Assistance Publique-Hôpitaux de Paris (AP-HP), Paris, France; University of Paris, Institut Imagine, INSERM, Paris, France; French Reference Center for Mastocytosis (CEREMAST), Hôpital Necker-Enfants Malades, AP-HP, Paris, France.
  • Rossignol J; University of Paris, Institut Imagine, INSERM, Paris, France; French Reference Center for Mastocytosis (CEREMAST), Hôpital Necker-Enfants Malades, AP-HP, Paris, France; Department of Hematology, Hôpital Necker-Enfants Malades, AP-HP, Paris, France.
  • Anglo E; University of Lille, Institut National de la Santé et de la Recherche Médicale (INSERM), Centre Hospitalier Universitaire (CHU) Lille, and Institute for Translational Research in Inflammation (INFINITE), Lille, France; Institut d'Immunologie, CHU Lille, Lille, France.
  • Dendooven A; University of Lille, Institut National de la Santé et de la Recherche Médicale (INSERM), Centre Hospitalier Universitaire (CHU) Lille, and Institute for Translational Research in Inflammation (INFINITE), Lille, France; Institut d'Immunologie, CHU Lille, Lille, France.
  • Dubois R; University of Lille, Institut de Pathologie, Centre de Biopathologie, CHU Lille, Lille, France.
  • Terriou L; University of Lille, Institut National de la Santé et de la Recherche Médicale (INSERM), Centre Hospitalier Universitaire (CHU) Lille, and Institute for Translational Research in Inflammation (INFINITE), Lille, France; National Reference Center for Hypereosinophilic Syndromes (CEREO); Département de
  • Launay D; University of Lille, Institut National de la Santé et de la Recherche Médicale (INSERM), Centre Hospitalier Universitaire (CHU) Lille, and Institute for Translational Research in Inflammation (INFINITE), Lille, France; National Reference Center for Hypereosinophilic Syndromes (CEREO); Département de
  • Barete S; CEREMAST, AP-HP, Groupe Hospitalier Pitié-Salpêtrière, Unit de Dermatologie, Sorbonne Université Paris, Paris, France.
  • Esnault S; University of Lille, Institut National de la Santé et de la Recherche Médicale (INSERM), Centre Hospitalier Universitaire (CHU) Lille, and Institute for Translational Research in Inflammation (INFINITE), Lille, France; Institut d'Immunologie, CHU Lille, Lille, France; Department of Medicine, Divisio
  • Frenzel L; University of Paris, Institut Imagine, INSERM, Paris, France; French Reference Center for Mastocytosis (CEREMAST), Hôpital Necker-Enfants Malades, AP-HP, Paris, France; Department of Hematology, Hôpital Necker-Enfants Malades, AP-HP, Paris, France.
  • Gourguechon C; Department of Hematology, CHU Amiens, Amiens, France.
  • Ballul T; University of Paris, Institut Imagine, INSERM, Paris, France; French Reference Center for Mastocytosis (CEREMAST), Hôpital Necker-Enfants Malades, AP-HP, Paris, France; Department of Hematology, Hôpital Necker-Enfants Malades, AP-HP, Paris, France.
  • Dezoteux F; University of Lille, Institut National de la Santé et de la Recherche Médicale (INSERM), Centre Hospitalier Universitaire (CHU) Lille, and Institute for Translational Research in Inflammation (INFINITE), Lille, France; National Reference Center for Hypereosinophilic Syndromes (CEREO); Department of
  • Staumont-Salle D; University of Lille, Institut National de la Santé et de la Recherche Médicale (INSERM), Centre Hospitalier Universitaire (CHU) Lille, and Institute for Translational Research in Inflammation (INFINITE), Lille, France; National Reference Center for Hypereosinophilic Syndromes (CEREO); Department of
  • Copin MC; Department of Pathology, CHU Angers, University of Angers, INSERM, CNRS, CRCI(2)NA, Angers, France.
  • Rignault-Bricard R; University of Paris, Institut Imagine, INSERM, Paris, France.
  • Maciel TT; University of Paris, Institut Imagine, INSERM, Paris, France.
  • Damaj G; Institut d'Hématologie, University of Caen Normandie, Caen, France.
  • Tardivel M; Centre National de la Recherche Scientifique (CNRS), INSERM, CHU Lille, University of Lille, Institut Pasteur de Lille, Lille, France.
  • Crinquette-Verhasselt M; University of Lille, Institut de Pathologie, Centre de Biopathologie, CHU Lille, Lille, France.
  • Dubreuil P; Signaling, Hematopoiesis, and Mechanism of Oncogenesis (CRCM), CEREMAST, and Association Française pour les Initiatives de Recherche sur le Mastocyte et les Mastocytose (AFIRMM) studies, INSERM U1068; Institut Paoli-Calmettes; UM105, Aix-Marseille University; and CNRS, UMR7258, Marseille, France.
  • Maouche-Chrétien L; University of Paris, Institut Imagine, INSERM, Paris, France.
  • Bruneau J; University of Paris, Institut Imagine, INSERM, Paris, France; French Reference Center for Mastocytosis (CEREMAST), Hôpital Necker-Enfants Malades, AP-HP, Paris, France; Department of Pathology, Hôpital Necker-Enfants Malades, AP-HP, Paris, France.
  • Lortholary O; University of Paris, Institut Imagine, INSERM, Paris, France; French Reference Center for Mastocytosis (CEREMAST), Hôpital Necker-Enfants Malades, AP-HP, Paris, France.
  • Duployez N; CNRS, INSERM, CHU Lille, Cancer Heterogeneity, Plasticity, and Resistance to Therapies (CANTHER), University of Lille, Institut d'Hématologie, CHU Lille, Lille, France.
  • Behal H; University of Lille, CHU Lille, Evaluation des Technologies de Santé et des Pratiques Médicales (METRICS), Lille, France.
  • Molina TJ; University of Paris, Institut Imagine, INSERM, Paris, France; Signaling, Hematopoiesis, and Mechanism of Oncogenesis (CRCM), CEREMAST, and Association Française pour les Initiatives de Recherche sur le Mastocyte et les Mastocytose (AFIRMM) studies, INSERM U1068; Institut Paoli-Calmettes; UM105, Aix-
  • Hermine O; University of Paris, Institut Imagine, INSERM, Paris, France; French Reference Center for Mastocytosis (CEREMAST), Hôpital Necker-Enfants Malades, AP-HP, Paris, France; Department of Hematology, Hôpital Necker-Enfants Malades, AP-HP, Paris, France. Electronic address: olivier.hermine@aphp.fr.
J Allergy Clin Immunol ; 2024 Aug 14.
Article in En | MEDLINE | ID: mdl-39151478
ABSTRACT

BACKGROUND:

Bidirectional interactions between eosinophils and mast cells (MCs) have been reported in various allergic diseases. Bone marrow (BM) eosinophilia, and to a lesser extent blood eosinophilia, is common in systemic mastocytosis (SM), but its significance remains unknown.

OBJECTIVE:

We described blood and BM eosinophil characteristics in SM.

METHODS:

A large collection of BM biopsy samples was analyzed using immunohistochemical staining and whole-slide imaging. Eosinophil and extracellular granules were detected by eosinophil peroxidase (EPX) staining and MCs by KIT staining. Complementary analyses were conducted using flow cytometry and immunofluorescence.

RESULTS:

Eosinophil infiltrates and large areas of eosinophil degranulation were observed within or around BM MC infiltrates in SM. EPX staining surface, highlighting intact eosinophils and eosinophil degranulation, was higher in nonadvanced SM (n = 37 BM biopsy samples) compared with both controls (n = 8, P = .0003) and advanced SM (n = 24, P = .014). In nonadvanced SM, positive correlations were observed between serum tryptase levels and percentages of eosinophil counts in BM aspirations (Spearman r coefficient r = 0.38, P = .038), eosinophils count in BM biopsy samples (r = 0.45, P = .007), EPX staining (r = 0.37, P = .035), and eosinophil degranulation (r = 0.39, P = .023). Eosinophil counts in BM biopsy samples also correlated with MC counts (r = 0.47, P = .006) and KIT staining surface (r = 0.49, P = .003). BM MCs expressed IL-5 receptor and other usual eosinophil cytokine/chemokine receptors, and blood eosinophils displayed several increased surface markers compared with controls, suggesting an activated state.

CONCLUSION:

Our data suggest possible cross talk between MCs and eosinophils, supporting MC tryptase release and MC activation-related symptoms. This suggests a rationale for targeting eosinophils in nonadvanced SM not fully controlled by other therapies.
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Full text: 1 Collection: 01-internacional Database: MEDLINE Language: En Journal: J Allergy Clin Immunol Year: 2024 Document type: Article Country of publication:
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Full text: 1 Collection: 01-internacional Database: MEDLINE Language: En Journal: J Allergy Clin Immunol Year: 2024 Document type: Article Country of publication: