Down-Regulation–Resistant STAT4 Risk Haplotype Contributes to Lupus Nephritis Through CD4+ T Cell Interferon-? Production


Por: Madera-Salcedo I.K., Ramírez-Sánchez A.L., Rodríguez-Rodríguez N., García-Quintero R., Rubio R.M., Morales-Montes de Oca G., Dávalos E., Cuervo R., Furuzawa-Carballeda J., Alcocer-Varela J., Gómez-Martín D., González-Yáñez M., de la Cruz A., Albarrán-Godínez A., Suárez-Rojas G., Romero-Díaz J., Uribe-Uribe N.O., Alarcón-Riquelme M., Furlan-Magaril M., Mejía-Vilet J.M., Crispín J.C., Rosetti F.

Publicada: 1 ene 2023
Resumen:
Objective: Variants in STAT4 are associated with systemic lupus erythematosus (SLE) and other autoimmune diseases. We undertook this study to investigate how disease-associated variants affect STAT4 expression, in particular in CD4+ T cells where STAT4 plays an essential role. Methods: We compared Th1 differentiation between naive CD4+ T cells from healthy donors homozygous for the risk (R/R) or nonrisk (NR/NR) alleles. We analyzed epigenetic marks in STAT4 and evaluated the relevance of its third intron, assessed the consequences of Stat4 overexpression in vivo in mice, and analyzed the effects of the STAT4 genotype in patients with lupus nephritis. Results: Naive CD4+ T cells from NR/NR healthy donors down-regulated STAT4 in response to interleukin-12 (IL-12). In contrast, cells from R/R healthy donors maintained high levels. R/R cells exhibited a higher abundance of transcriptionally active STAT4 and increased interferon-? production. Accordingly, R/R healthy donors exhibited a stronger induction of local active enhancer marks. Genetic editing confirmed the presence of a negative regulatory region in the STAT4 third intron, where most of the SLE-associated STAT4 single-nucleotide polymorphisms (SNPs) are located. In vivo forced expression demonstrated that increases in Stat4 levels in T cells enhanced glomerulonephritis in mice. Accordingly, the R/R genotype was associated with suboptimal response to treatment and with worse clinical outcomes in patients with proliferative lupus nephritis. Conclusion: The SLE-associated STAT4 haplotype correlates with an abnormal IL-12–mediated STAT4 transcriptional regulation. Carriers of the risk variant exhibit exaggerated CD4+ proinflammatory capacities that, in the context of SLE, contribute to more severe disease. R/R patients may benefit from blockade of the IL-12/STAT4 pathway. (Figure presented.). © 2022 American College of Rheumatology.

Filiaciones:
Madera-Salcedo I.K.:
 Department of Immunology and Rheumatology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico

Ramírez-Sánchez A.L.:
 Department of Immunology and Rheumatology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico

Rodríguez-Rodríguez N.:
 Department of Immunology and Rheumatology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico

García-Quintero R.:
 Department of Internal Medicine, Instituto Nacional de Ciencias Medicas y Nutricion Salvador Zubiran, Mexico City, Mexico

Rubio R.M.:
 Department of Immunology and Rheumatology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico

 Department of Immunology and Rheumatology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico, and Tecnologico de Monterrey, Escuela de Medicina y Ciencias de la Salud, Monterrey, Mexico

Morales-Montes de Oca G.:
 Department of Immunology and Rheumatology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico

Dávalos E.:
 Department of Immunology and Rheumatology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico

Cuervo R.:
 Department of Immunology and Rheumatology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico

Furuzawa-Carballeda J.:
 Department of Immunology and Rheumatology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico

Alcocer-Varela J.:
 Department of Immunology and Rheumatology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico

Gómez-Martín D.:
 Department of Immunology and Rheumatology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico

González-Yáñez M.:
 Animal Research Facility, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico

de la Cruz A.:
 Department of Immunology and Rheumatology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, and Plan de Estudios Combinados en Medicina (PECEM), Facultad de Medicina, UNAM, Mexico City, Mexico

Albarrán-Godínez A.:
 Department of Immunology and Rheumatology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, and Programa de Doctorado en Ciencias Biomédicas, Universidad Nacional Autónoma de México, Ciudad Universitaria, Mexico City, Mexico

Suárez-Rojas G.:
 Department of Immunology and Rheumatology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, and Programa de Doctorado en Ciencias Biomédicas, Universidad Nacional Autónoma de México, Ciudad Universitaria, Mexico City, Mexico

Romero-Díaz J.:
 Department of Immunology and Rheumatology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico

Uribe-Uribe N.O.:
 Department of Pathology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico

Alarcón-Riquelme M.:
 Medical Genomics, GENYO. Centre for Genomics and Oncological Research: Pfizer/University of Granada/Andalusian Regional Government, Granada, Spain, and Unit of Inflammatory Chronic Diseases, Institute of Environmental Medicine, Karolinska Institutet, Solna, Sweden

Furlan-Magaril M.:
 Department of Molecular Genetics, Instituto de Fisiología Celular, Universidad Nacional Autónoma de México, Mexico City, Mexico

Mejía-Vilet J.M.:
 Department of Nephrology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán Mexico City, Mexico

Crispín J.C.:
 Department of Immunology and Rheumatology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico

 Department of Immunology and Rheumatology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico, and Tecnologico de Monterrey, Escuela de Medicina y Ciencias de la Salud, Monterrey, Mexico

Rosetti F.:
 Department of Immunology and Rheumatology, Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán, Mexico City, Mexico
ISSN: 23265191
Editorial
WILEY-BLACKWELL, 111 RIVER ST, HOBOKEN 07030-5774, NJ USA, Estados Unidos America
Tipo de documento: Article
Volumen: 75 Número: 6
Páginas: 961-972
WOS Id: 000957978300001
ID de PubMed: 36575804

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