Systemic Inflammation and Normocytic Anemia in DOCK11 Deficiency

Jana Block, Christina Rashkova, Irinka Castanon, Samaneh Zoghi, Jessica Platon, Rico C. Ardy, Mitsuhiro Fujiwara, Beatriz Chaves, Rouven Schoppmeyer, Caspar I. van der Made, Raul Jimenez Heredia, Frederike L. Harms, Samin Alavi, Laia Alsina, Paula Sanchez Moreno, Rainiero Avila Polo, Rocio Cabrera-Perez, Sevgi Kostel Bal, Laurene Pfajfer, Bernhard RansmayrAnna-Katharina Mautner, Ryohei Kondo, Anna Tinnacher, Michael Caldera, Michael Schuster, Cecilia Dominguez Conde, Rene Platzer, Elisabeth Salzer, Thomas Boyer, Han G. Brunner, Judith E. Nooitgedagt-Frons, Estibaliz Iglesias, Angela Deya-Martinez, Marisol Camacho-Lovillo, Joerg Menche, Christoph Bock, Johannes B. Huppa, Winfried F. Pickl, Martin Distel, Jeffrey A. Yoder, David Traver, Karin R. Engelhardt, Tobias Linden, Leo Kager, J. Thomas Hannich, Alexander Hoischen, Sophie Hambleton, Sabine Illsinger, Lydie Da Costa, Kerstin Kutsche, K. Boztug*

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

Abstract

BackgroundIncreasing evidence links genetic defects affecting actin-regulatory proteins to diseases with severe autoimmunity and autoinflammation, yet the underlying molecular mechanisms are poorly understood. Dedicator of cytokinesis 11 (DOCK11) activates the small Rho guanosine triphosphatase (GTPase) cell division cycle 42 (CDC42), a central regulator of actin cytoskeleton dynamics. The role of DOCK11 in human immune-cell function and disease remains unknown. MethodsWe conducted genetic, immunologic, and molecular assays in four patients from four unrelated families who presented with infections, early-onset severe immune dysregulation, normocytic anemia of variable severity associated with anisopoikilocytosis, and developmental delay. Functional assays were performed in patient-derived cells, as well as in mouse and zebrafish models. ResultsWe identified rare, X-linked germline mutations in DOCK11 in the patients, leading to a loss of protein expression in two patients and impaired CDC42 activation in all four patients. Patient-derived T cells did not form filopodia and showed abnormal migration. In addition, the patient-derived T cells, as well as the T cells from Dock11-knockout mice, showed overt activation and production of proinflammatory cytokines that were associated with an increased degree of nuclear translocation of nuclear factor of activated T cell 1 (NFATc1). Anemia and aberrant erythrocyte morphologic features were recapitulated in a newly generated dock11-knockout zebrafish model, and anemia was amenable to rescue on ectopic expression of constitutively active CDC42. ConclusionsGermline hemizygous loss-of-function mutations affecting the actin regulator DOCK11 were shown to cause a previously unknown inborn error of hematopoiesis and immunity characterized by severe immune dysregulation and systemic inflammation, recurrent infections, and anemia. (Funded by the European Research Council and others.)DOCK11, Inflammation, and Normocytic AnemiaIn this study, DOCK11 was shown to regulate T-cell shape and migration and erythroid development. Inherited loss-of-function variants in DOCK11 led to early-onset severe immune dysregulation and normocytic anemia.
Original languageEnglish
Pages (from-to)527-539
Number of pages13
JournalNew England Journal of Medicine
Volume389
Issue number6
Early online date1 Jun 2023
DOIs
Publication statusPublished - 10 Aug 2023

Keywords

  • T-CELLS
  • CDC42
  • ACTIVATION
  • PROTEINS
  • RECEPTOR
  • CD4(+)

Fingerprint

Dive into the research topics of 'Systemic Inflammation and Normocytic Anemia in DOCK11 Deficiency'. Together they form a unique fingerprint.

Cite this