Cited by 228Systemic Lupus Erythematosus ResearchAutophagy in Disease and Therapyinterferon and immune responses

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Erythroid mitochondrial retention triggers myeloid-dependent type I interferon in human SLE

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Caielli, Simone, Cardenas, Jacob, de Jesus, Adriana Almeida, Baisch, Jeanine, Walters, Lynnette, Blanck, Jean Philippe, Balasubramanian, Preetha, Stagnar, Cristy, Ohouo, Marina, Hong, Seunghee, Nassi, Lorien, Stewart, Katie, Fuller, Julie, Gu, Jinghua, Banchereau, Jacques F., Wright, Tracey, Goldbach-Mansky, Raphaela, Pascual, Virginia·2021·Cell

DOI 10.1016/j.cell.2021.07.021PMC PMC8380737

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Abstract

Emerging evidence supports that mitochondrial dysfunction contributes to systemic lupus erythematosus (SLE) pathogenesis. Here we show that programmed mitochondrial removal, a hallmark of mammalian erythropoiesis, is defective in SLE. Specifically, we demonstrate that during human erythroid cell maturation, a hypoxia-inducible factor (HIF)-mediated metabolic switch is responsible for the activation of the ubiquitin-proteasome system (UPS), which precedes and is necessary for the autophagic removal of mitochondria. A defect in this pathway leads to accumulation of red blood cells (RBCs) carrying mitochondria (Mito+ RBCs) in SLE patients and in correlation with disease activity. Antibody-mediated internalization of Mito+ RBCs induces type I interferon (IFN) production through activation of cGAS in macrophages. Accordingly, SLE patients carrying both Mito+ RBCs and opsonizing antibodies display the highest levels of blood IFN-stimulated gene (ISG) signatures, a distinctive feature of SLE.

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Authors: Caielli, S., Cardenas, J., de Jesus, A. A., Baisch, J., Walters, L., Blanck, J. P., Balasubramanian, P., Stagnar, C., Ohouo, M., Hong, S., Nassi, L., Stewart, K., Fuller, J., Gu, J., Banchereau, J. F., Wright, T., Goldbach-Mansky, R., & Pascual, V.
Affiliations: Weill Cornell Medicine (US)
Texas Scottish Rite Hospital for Children (US)
The Jackson Laboratory for Genomic Medicine (US)
Corresponding author: Caielli, Simone
Pascual, Virginia
ORCID: Caielli, Simone
Cardenas, Jacob
Baisch, Jeanine
Walters, Lynnette
Stagnar, Cristy
Ohouo, Marina
Hong, Seunghee
Nassi, Lorien
Banchereau, Jacques F.
Wright, Tracey
Pascual, Virginia
Venue: Cell
Publisher: Elsevier BV
Published: 2021-08
Volume: 184
Issue: 17
Pages: 4464-4479.e19
ISSN: 0092-8674 (ISSN-L)
DOI: 10.1016/j.cell.2021.07.021
PMC: PMC8380737
OpenAlex: W3189265697
Cited by: 228
References: 88
Citations by year: 2026: 36 · 2025: 53 · 2024: 60 · 2023: 40 · 2022: 33 · 2021: 6
FWCI: 26.18
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 384 d)
doi.org/10.15223/policy-017 (stm-asf)
doi.org/10.15223/policy-037 (stm-asf)
doi.org/10.15223/policy-012 (stm-asf)
doi.org/10.15223/policy-029 (stm-asf)
doi.org/10.15223/policy-004 (stm-asf)
Locations: Cell (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
The Mouseion at the JAXlibrary (Jackson Laboratory) (submittedVersion)
Funders: NIH (U19 AI082715)
Sanofi
AstraZeneca
Weill Cornell Medical College
National Institute of Allergy and Infectious Diseases
Lupus Research Alliance
National Institute of Arthritis and Musculoskeletal and Skin Diseases
Topics: Health Sciences › Medicine › Rheumatology › Systemic Lupus Erythematosus Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Autophagy in Disease and Therapy
Life Sciences › Immunology and Microbiology › Immunology › interferon and immune responses
Keywords: systemic lupus erythematosus, erythropoiesis, autophagy, hypoxia-inducible factor, ubiquitin-proteasome system, mitochondrial dysfunction, type I interferon, cGAS, macrophages, opsonic antibodies, interferon-stimulated genes, disease activity
MeSH terms: Endothelial PAS Domain-Containing Protein 1, Adolescent, Child, Child, Preschool, Erythroblasts, Erythrocytes, Erythropoiesis, Humans, Interferon Type I, Lupus Erythematosus, Systemic, Mitochondria, Myeloid Cells, Ubiquitin, Proteasome Endopeptidase Complex, Basic Helix-Loop-Helix Transcription Factors, Basic Helix-Loop-Helix Proteins, Mitophagy

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Erythroid mitochondrial retention triggers myeloid-dependent type I interferon in human SLE

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