NCKAP1L defects lead to a novel syndrome combining immunodeficiency, lymphoproliferation, and hyperinflammation.


Journal

The Journal of experimental medicine
ISSN: 1540-9538
Titre abrégé: J Exp Med
Pays: United States
ID NLM: 2985109R

Informations de publication

Date de publication:
07 12 2020
Historique:
received: 03 12 2019
revised: 22 06 2020
accepted: 21 07 2020
entrez: 9 8 2020
pubmed: 9 8 2020
medline: 12 3 2021
Statut: ppublish

Résumé

The Nck-associated protein 1-like (NCKAP1L) gene, alternatively called hematopoietic protein 1 (HEM-1), encodes a hematopoietic lineage-specific regulator of the actin cytoskeleton. Nckap1l-deficient mice have anomalies in lymphocyte development, phagocytosis, and neutrophil migration. Here we report, for the first time, NCKAP1L deficiency cases in humans. In two unrelated patients of Middle Eastern origin, recessive mutations in NCKAP1L abolishing protein expression led to immunodeficiency, lymphoproliferation, and hyperinflammation with features of hemophagocytic lymphohistiocytosis. Immunophenotyping showed an inverted CD4/CD8 ratio with a major shift of both CD4+ and CD8+ cells toward memory compartments, in line with combined RNA-seq/proteomics analyses revealing a T cell exhaustion signature. Consistent with the core function of NCKAP1L in the reorganization of the actin cytoskeleton, patients' T cells displayed impaired early activation, immune synapse morphology, and leading edge formation. Moreover, knockdown of nckap1l in zebrafish led to defects in neutrophil migration. Hence, NCKAP1L mutations lead to broad immune dysregulation in humans, which could be classified within actinopathies.

Identifiants

pubmed: 32766723
pii: 152004
doi: 10.1084/jem.20192275
pmc: PMC7526481
pii:
doi:

Substances chimiques

Actins 0
Membrane Proteins 0
NCKAP1L protein, human 144351-15-5

Types de publication

Case Reports Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Wellcome Trust
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 108437/Z/15/Z
Pays : United Kingdom

Informations de copyright

© 2020 Castro et al.

Déclaration de conflit d'intérêts

Disclosures: The authors declare no competing interests exist.

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Auteurs

Carla Noemi Castro (CN)

Institute for Immunodeficiency, Center for Chronic Immunodeficiency, Medical Center-University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany.

Michelle Rosenzwajg (M)

Assistance Publique-Hôpitaux de Paris, Pitié-Salpêtrière Hospital, Biotherapy (Centre d'Investigation Clinique intégré en Biothérapies & immunologie; CIC-BTi) and Inflammation-Immunopathology-Biotherapy Department (i2B), Paris, France.
Sorbonne Université, Institut National de la Santé et de la Recherche Médicale UMR_S 959, Immunology-Immunopathology-Immunotherapy (i3), Paris, France.

Raphael Carapito (R)

Laboratoire d'ImmunoRhumatologie Moléculaire, Plateforme GENOMAX, Institut National de la Santé et de la Recherche Médicale UMR_S 1109, Faculté de Médecine, Fédération Hospitalo-Universitaire OMICARE, Fédération de Médecine Translationnelle de Strasbourg, Laboratory of Excellence TRANSPLANTEX, Université de Strasbourg, Strasbourg, France.
Service d'Immunologie Biologique, Plateau Technique de Biologie, Pôle de Biologie, Nouvel Hôpital Civil, Hôpitaux Universitaires de Strasbourg, Strasbourg, France.

Mohammad Shahrooei (M)

Specialized Immunology Laboratory of Dr. Shahrooei, Sina Medical Complex, Ahvaz, Iran.
Department of Microbiology and Immunology, University of Leuven, Leuven, Belgium.

Martina Konantz (M)

University of Basel and University Hospital Basel, Department of Biomedicine, Basel, Switzerland.

Amjad Khan (A)

Department of Pediatrics, King Abdulaziz Medical City, King Abdullah Specialized Children's Hospital, Riyadh, Saudi Arabia.
King Saud bin Abdulaziz University for Health Sciences, Riyadh, Saudi Arabia.
King Abdullah International Medical Research Center, Riyadh, Saudi Arabia.

Zhichao Miao (Z)

European Molecular Biology Laboratory, European Bioinformatics Institute, Wellcome Genome Campus, Hinxton, Cambridge, UK.
Shanghai Fourth People's Hospital Affiliated to Tongji University School of Medicine, Shanghai, Hongkou, China.

Miriam Groß (M)

Institute for Immunodeficiency, Center for Chronic Immunodeficiency, Medical Center-University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany.

Thibaud Tranchant (T)

Laboratoire d'ImmunoRhumatologie Moléculaire, Plateforme GENOMAX, Institut National de la Santé et de la Recherche Médicale UMR_S 1109, Faculté de Médecine, Fédération Hospitalo-Universitaire OMICARE, Fédération de Médecine Translationnelle de Strasbourg, Laboratory of Excellence TRANSPLANTEX, Université de Strasbourg, Strasbourg, France.

Mirjana Radosavljevic (M)

Laboratoire d'ImmunoRhumatologie Moléculaire, Plateforme GENOMAX, Institut National de la Santé et de la Recherche Médicale UMR_S 1109, Faculté de Médecine, Fédération Hospitalo-Universitaire OMICARE, Fédération de Médecine Translationnelle de Strasbourg, Laboratory of Excellence TRANSPLANTEX, Université de Strasbourg, Strasbourg, France.
Service d'Immunologie Biologique, Plateau Technique de Biologie, Pôle de Biologie, Nouvel Hôpital Civil, Hôpitaux Universitaires de Strasbourg, Strasbourg, France.

Nicodème Paul (N)

Laboratoire d'ImmunoRhumatologie Moléculaire, Plateforme GENOMAX, Institut National de la Santé et de la Recherche Médicale UMR_S 1109, Faculté de Médecine, Fédération Hospitalo-Universitaire OMICARE, Fédération de Médecine Translationnelle de Strasbourg, Laboratory of Excellence TRANSPLANTEX, Université de Strasbourg, Strasbourg, France.

Tristan Stemmelen (T)

Laboratoire d'ImmunoRhumatologie Moléculaire, Plateforme GENOMAX, Institut National de la Santé et de la Recherche Médicale UMR_S 1109, Faculté de Médecine, Fédération Hospitalo-Universitaire OMICARE, Fédération de Médecine Translationnelle de Strasbourg, Laboratory of Excellence TRANSPLANTEX, Université de Strasbourg, Strasbourg, France.

Fabien Pitoiset (F)

Assistance Publique-Hôpitaux de Paris, Pitié-Salpêtrière Hospital, Biotherapy (Centre d'Investigation Clinique intégré en Biothérapies & immunologie; CIC-BTi) and Inflammation-Immunopathology-Biotherapy Department (i2B), Paris, France.
Sorbonne Université, Institut National de la Santé et de la Recherche Médicale UMR_S 959, Immunology-Immunopathology-Immunotherapy (i3), Paris, France.

Aurélie Hirschler (A)

Laboratoire de Spectrométrie de Masse Bio-Organique, Institut Pluridisciplinaire Hubert Curien, UMR 7178, Université de Strasbourg, Centre National de la Recherche Scientifique, Strasbourg, France.

Benoit Nespola (B)

Service d'Immunologie Biologique, Plateau Technique de Biologie, Pôle de Biologie, Nouvel Hôpital Civil, Hôpitaux Universitaires de Strasbourg, Strasbourg, France.

Anne Molitor (A)

Laboratoire d'ImmunoRhumatologie Moléculaire, Plateforme GENOMAX, Institut National de la Santé et de la Recherche Médicale UMR_S 1109, Faculté de Médecine, Fédération Hospitalo-Universitaire OMICARE, Fédération de Médecine Translationnelle de Strasbourg, Laboratory of Excellence TRANSPLANTEX, Université de Strasbourg, Strasbourg, France.

Véronique Rolli (V)

Laboratoire d'ImmunoRhumatologie Moléculaire, Plateforme GENOMAX, Institut National de la Santé et de la Recherche Médicale UMR_S 1109, Faculté de Médecine, Fédération Hospitalo-Universitaire OMICARE, Fédération de Médecine Translationnelle de Strasbourg, Laboratory of Excellence TRANSPLANTEX, Université de Strasbourg, Strasbourg, France.
Service d'Immunologie Biologique, Plateau Technique de Biologie, Pôle de Biologie, Nouvel Hôpital Civil, Hôpitaux Universitaires de Strasbourg, Strasbourg, France.

Angélique Pichot (A)

Laboratoire d'ImmunoRhumatologie Moléculaire, Plateforme GENOMAX, Institut National de la Santé et de la Recherche Médicale UMR_S 1109, Faculté de Médecine, Fédération Hospitalo-Universitaire OMICARE, Fédération de Médecine Translationnelle de Strasbourg, Laboratory of Excellence TRANSPLANTEX, Université de Strasbourg, Strasbourg, France.

Laura Eva Faletti (LE)

Institute for Immunodeficiency, Center for Chronic Immunodeficiency, Medical Center-University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany.
Department of Pediatrics and Adolescent Medicine, Medical Center-University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany.

Bruno Rinaldi (B)

Laboratoire de Génétique Moléculaire, Génomique, Microbiologie, UMR7156/Université de Strasbourg, Centre National de la Recherche Scientifique, Strasbourg, France.

Sylvie Friant (S)

Laboratoire de Génétique Moléculaire, Génomique, Microbiologie, UMR7156/Université de Strasbourg, Centre National de la Recherche Scientifique, Strasbourg, France.

Mark Mednikov (M)

Integrated BioTherapeutics, Inc., Rockville, MD.

Hatice Karauzum (H)

Integrated BioTherapeutics, Inc., Rockville, MD.

M Javad Aman (MJ)

Integrated BioTherapeutics, Inc., Rockville, MD.

Christine Carapito (C)

Laboratoire de Spectrométrie de Masse Bio-Organique, Institut Pluridisciplinaire Hubert Curien, UMR 7178, Université de Strasbourg, Centre National de la Recherche Scientifique, Strasbourg, France.

Claudia Lengerke (C)

University of Basel and University Hospital Basel, Department of Biomedicine, Basel, Switzerland.

Vahid Ziaee (V)

Pediatric Rheumatology Research Group, Rheumatology Research Center, Tehran University of Medical Sciences, Tehran, Iran.
Department of Pediatrics, Tehran University of Medical Sciences, Tehran, Iran.

Wafaa Eyaid (W)

Department of Pediatrics, King Abdulaziz Medical City, King Abdullah Specialized Children's Hospital, Riyadh, Saudi Arabia.
King Saud bin Abdulaziz University for Health Sciences, Riyadh, Saudi Arabia.
King Abdullah International Medical Research Center, Riyadh, Saudi Arabia.

Stephan Ehl (S)

Institute for Immunodeficiency, Center for Chronic Immunodeficiency, Medical Center-University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany.
Department of Pediatrics and Adolescent Medicine, Medical Center-University of Freiburg, Faculty of Medicine, University of Freiburg, Freiburg, Germany.

Fayhan Alroqi (F)

Department of Pediatrics, King Abdulaziz Medical City, King Abdullah Specialized Children's Hospital, Riyadh, Saudi Arabia.
King Saud bin Abdulaziz University for Health Sciences, Riyadh, Saudi Arabia.
King Abdullah International Medical Research Center, Riyadh, Saudi Arabia.

Nima Parvaneh (N)

Division of Allergy and Clinical Immunology, Department of Pediatrics, Tehran University of Medical Sciences, Tehran, Iran.
Research Center for Immunodeficiencies, Tehran University of Medical Sciences, Tehran, Iran.

Seiamak Bahram (S)

Laboratoire d'ImmunoRhumatologie Moléculaire, Plateforme GENOMAX, Institut National de la Santé et de la Recherche Médicale UMR_S 1109, Faculté de Médecine, Fédération Hospitalo-Universitaire OMICARE, Fédération de Médecine Translationnelle de Strasbourg, Laboratory of Excellence TRANSPLANTEX, Université de Strasbourg, Strasbourg, France.
Service d'Immunologie Biologique, Plateau Technique de Biologie, Pôle de Biologie, Nouvel Hôpital Civil, Hôpitaux Universitaires de Strasbourg, Strasbourg, France.

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