A new severe congenital neutropenia syndrome associated with autosomal recessive <i>COPZ1</i> mutations

N Natalia Borbaran Bravo E Ekaterina Deordieva (2Department of Immunology, Dmitry Rogachev National Medical Research Center of Pediatric Hematology, Oncology and Immunology, Moscow, Russia) L Larissa Doll (1Department of Oncology, Hematology, Clinical Immunology, and Rheumatology, University Hospital Tuebingen, Tuebingen, Germany) M Mohammad ElGamacy (1Department of Oncology, Hematology, Clinical Immunology, and Rheumatology, University Hospital Tuebingen, Tuebingen, Germany) B Benjamin Dannenmann (1Department of Oncology, Hematology, Clinical Immunology, and Rheumatology, University Hospital Tuebingen, Tuebingen, Germany) J Joana Azevedo A Alberto Iannuzzo S Selket Delafontaine (7Department of Microbiology, Immunology, and Transplantation, Laboratory for Inborn Errors of Immunity, KU Leuven, Leuven, Belgium) M Moritz Lehners M Marius Kolodziej (10Natural and Medical Sciences Institute, University of Tuebingen, Reutlingen, Germany) B Birte Hernandez Alvarez A Anna-Sophia Hellmuth (1Department of Oncology, Hematology, Clinical Immunology, and Rheumatology, University Hospital Tuebingen, Tuebingen, Germany) M Malte Ritter (1University Hospital Tübingen, Translational Oncology, Tübingen, Germany) B Betül Findik (4Department of Hematology, Oncology, Immunology and Rheumatology, University Hospital Tübingen, Tübingen, Germany) V Viktoria Zakharova (11National Medical Research Center for Endocrinology, Clinical Data Analysis Department, National Medical Research Center for Endocrinology, Moscow, Russia) S Sandro Bräuning (1Department of Oncology, Hematology, Clinical Immunology, and Rheumatology, University Hospital Tuebingen, Tuebingen, Germany) S Sergey Kandabarau (1University Hospital Tübingen, Translational Oncology, Tübingen, Germany) C Claudia Lengerke R Robert Feil I Isabelle Meyts J Jérôme Delon M Markus Templin (10Natural and Medical Sciences Institute, University of Tuebingen, Reutlingen, Germany) M Marc Sturm O Olaf Riess (Institute of Medical Genetics and Applied Genomics, University of Tuebingen) C Cornelia Zeidler (5University of Tubingen, Tubingen, Germany) K Karl Welte (1University Hospital Tuebingen, Tuebingen, Germany) A Anna Shcherbina M Maksim Klimiankou (1University Hospital Tübingen, Translational Oncology, Tübingen, Germany) J Julia Skokowa

Abstract

Abstract We have identified a new inherited bone marrow failure syndrome with severe congenital neutropenia (CN) caused by autosomal recessive mutations in the coatomer protein complex I (COPI) subunit zeta 1 (COPZ1) gene. A stop-codon COPZ1 mutation and a missense (MS) mutation were found in 3 patients from 2 unrelated families. Although 2 affected siblings with a stop-codon COPZ1 mutation suffered from CN that involves other hematologic lineages and nonhematologic tissues, the patient with a MS COPZ1 mutation had isolated neutropenia. Both COPZ1 mutations were localized to a highly evolutionarily conserved region. The resulting truncated (TR) COPZ1 protein was predicted to display diminished interaction with its COPI complex partner, COPG1. These findings were consistent with the observed block in retrograde protein transport from the Golgi apparatus to the endoplasmic reticulum (ER) in human fibroblasts carrying TR COPZ1. Human CD34+ cells with TR or MS COPZ1 had significantly impaired granulocytic differentiation, and in zebrafish embryos, TR Copz1 also resulted in defective myelopoiesis. Intracellularly, TR COPZ1 downregulated JAK/STAT/CEBPE/G-CSFR signaling and hypoxia-responsive pathways, while inducing STING, interferon-stimulated genes, stimulating oxidative phosphorylation activity, and increasing reactive oxygen species levels in hematopoietic cells. MS COPZ1 deregulated interferon and JAK/STAT signaling but less than the TR protein. Finally, treatment with the small molecule HIF1α stabilizer IOX2 or transduction of cells with COPZ2 restored defective granulopoiesis in COPZ1-mutated human CD34+ cells, offering potential therapeutic options.

Article Details

Journal Blood
Volume / Issue Vol. 145, Issue 20
Published May 15, 2025
Pages 2317-2335
ISSN 0006-4971
Publisher Elsevier BV

Journal Info

Blood

Elsevier BV

ISSN: 0006-4971 Health Sciences

Authors (29)

N

Natalia Borbaran Bravo

E

Ekaterina Deordieva

2Department of Immunology, Dmitry Rogachev National Medical Research Center of Pediatric Hematology, Oncology and Immunology, Moscow, Russia

L

Larissa Doll

1Department of Oncology, Hematology, Clinical Immunology, and Rheumatology, University Hospital Tuebingen, Tuebingen, Germany

M

Mohammad ElGamacy

1Department of Oncology, Hematology, Clinical Immunology, and Rheumatology, University Hospital Tuebingen, Tuebingen, Germany

B

Benjamin Dannenmann

1Department of Oncology, Hematology, Clinical Immunology, and Rheumatology, University Hospital Tuebingen, Tuebingen, Germany

J

Joana Azevedo

A

Alberto Iannuzzo

S

Selket Delafontaine

7Department of Microbiology, Immunology, and Transplantation, Laboratory for Inborn Errors of Immunity, KU Leuven, Leuven, Belgium

M

Moritz Lehners

M

Marius Kolodziej

10Natural and Medical Sciences Institute, University of Tuebingen, Reutlingen, Germany

B

Birte Hernandez Alvarez

A

Anna-Sophia Hellmuth

1Department of Oncology, Hematology, Clinical Immunology, and Rheumatology, University Hospital Tuebingen, Tuebingen, Germany

M

Malte Ritter

1University Hospital Tübingen, Translational Oncology, Tübingen, Germany

B

Betül Findik

4Department of Hematology, Oncology, Immunology and Rheumatology, University Hospital Tübingen, Tübingen, Germany

V

Viktoria Zakharova

11National Medical Research Center for Endocrinology, Clinical Data Analysis Department, National Medical Research Center for Endocrinology, Moscow, Russia

S

Sandro Bräuning

1Department of Oncology, Hematology, Clinical Immunology, and Rheumatology, University Hospital Tuebingen, Tuebingen, Germany

S

Sergey Kandabarau

1University Hospital Tübingen, Translational Oncology, Tübingen, Germany

C

Claudia Lengerke

R

Robert Feil

I

Isabelle Meyts

J

Jérôme Delon

M

Markus Templin

10Natural and Medical Sciences Institute, University of Tuebingen, Reutlingen, Germany

M

Marc Sturm

O

Olaf Riess

Institute of Medical Genetics and Applied Genomics, University of Tuebingen

C

Cornelia Zeidler

5University of Tubingen, Tubingen, Germany

K

Karl Welte

1University Hospital Tuebingen, Tuebingen, Germany

A

Anna Shcherbina

M

Maksim Klimiankou

1University Hospital Tübingen, Translational Oncology, Tübingen, Germany

J

Julia Skokowa