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3. High-dimensional mass cytometry identified circulating natural killer T-cell subsets associated with protection from cytomegalovirus infection in kidney transplant recipients

Author

Donadeu, Laura, Jouve, Thomas, Bin, Sofia, Hartzell, Susan, Crespo, Elena, Torija, Alba, Jarque, Marta, Kervella, Delphine, Zúñiga, José, Zhang, Weijia, Sun, Zeguo, Verlato, Alberto, Martínez-Gallo, Mónica, Font-Miñarro, Cristina, Meneghini, Maria, Toapanta, Nestor, Torres, Irina B., Sellarés, Joana, Perelló, Manel, Kaminski, Hannah, Couzi, Lionel, Loupy, Alexandre, La Manna, Gaetano, Moreso, Francesc, Cravedi, Paolo, and Bestard, Oriol

Published
2024
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5. A Comprehensive Phenotypic and Functional Immune Analysis Unravels Circulating Anti–Phospholipase A2 Receptor Antibody Secreting Cells in Membranous Nephropathy Patients

Author

Cantarelli, Chiara, Jarque, Marta, Angeletti, Andrea, Manrique, Joaquin, Hartzell, Susan, O’Donnell, Timothy, Merritt, Elliot, Laserson, Uri, Perin, Laura, Donadei, Chiara, Anderson, Lisa, Fischman, Clara, Chan, Emilie, Draibe, Juliana, Fulladosa, Xavier, Torras, Joan, Riella, Leonardo V., La Manna, Gaetano, Fiaccadori, Enrico, Maggiore, Umberto, Bestard, Oriol, and Cravedi, Paolo

Published
2020
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6. The impact of dupilumab treatment on SARS-CoV-2 T cell responses in atopic dermatitis patients

Author

Icahn School of Medicine at Mount Sinai, Sanofi, Sanofi España, National Institute of Allergy and Infectious Diseases (US), National Institutes of Health (US), Ungar, Benjamin, Hartzell, Susan, Lozano-Ojalvo, Daniel, Ghalili, Sabrina, Bose, Swaroop, Golant, Alexandra K., Tan, Kathryn, Estrada, Yeriel D., Singer, Giselle K., Pavel, Ana B., Cravedi, Paolo, Guttman-Yassky, Emma, Icahn School of Medicine at Mount Sinai, Sanofi, Sanofi España, National Institute of Allergy and Infectious Diseases (US), National Institutes of Health (US), Ungar, Benjamin, Hartzell, Susan, Lozano-Ojalvo, Daniel, Ghalili, Sabrina, Bose, Swaroop, Golant, Alexandra K., Tan, Kathryn, Estrada, Yeriel D., Singer, Giselle K., Pavel, Ana B., Cravedi, Paolo, and Guttman-Yassky, Emma

Published
2023

7. Blood Transcriptomes of SARS-CoV-2–Infected Kidney Transplant Recipients Associated with Immune Insufficiency Proportionate to Severity

Author

Sun, Zeguo, primary, Zhang, Zhongyang, additional, Banu, Khadija, additional, Azzi, Yorg Al, additional, Reghuvaran, Anand, additional, Fredericks, Samuel, additional, Planoutene, Marina, additional, Hartzell, Susan, additional, Kim, Yesl, additional, Pell, John, additional, Tietjen, Gregory, additional, Asch, William, additional, Kulkarni, Sanjay, additional, Formica, Richard, additional, Rana, Meenakshi, additional, Maltzman, Jonathan S., additional, Zhang, Weijia, additional, Akalin, Enver, additional, Heeger, Peter S., additional, Cravedi, Paolo, additional, and Menon, Madhav C., additional

Published
2022
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8. The impact of dupilumab treatment on SARS‐CoV ‐2 T cell responses in atopic dermatitis patients

Author

Ungar, Benjamin, primary, Hartzell, Susan, additional, Lozano‐Ojalvo, Daniel, additional, Ghalili, Sabrina, additional, Bose, Swaroop, additional, Golant, Alexandra K., additional, Tan, Kathryn, additional, Estrada, Yeriel D., additional, Singer, Giselle K., additional, Pavel, Ana B., additional, Cravedi, Paolo, additional, and Guttman‐Yassky, Emma, additional

Published
2022
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9. Differences in Humoral and Cellular Vaccine Responses to SARS-CoV-2 in Kidney and Liver Transplant Recipients

Author

Furian, Lucrezia, primary, Russo, Francesco Paolo, additional, Zaza, Gianluigi, additional, Burra, Patrizia, additional, Hartzell, Susan, additional, Bizzaro, Debora, additional, Di Bello, Marianna, additional, Di Bella, Caterina, additional, Nuzzolese, Erica, additional, Agnolon, Clara, additional, Florman, Sander, additional, Rana, Meenakshi, additional, Lee, Jar-How, additional, Kim, Yesl, additional, Maggiore, Umberto, additional, Maltzman, Jonathan S., additional, and Cravedi, Paolo, additional

Published
2022
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11. Blood transcriptomes of SARS-CoV-2 infected kidney transplant recipients demonstrate immune insufficiency

Author

Sun, Zeguo, primary, Zhang, Zhongyang, additional, Banu, Khadija, additional, Azzi, Yorg Al, additional, Reghuvaran, Anand, additional, Fredericks, Samuel, additional, Planoutene, Marina, additional, Hartzell, Susan, additional, Pell, John, additional, Tietjen, Gregory, additional, Asch, William, additional, Kulkarni, Sanjay, additional, Formica, Richard, additional, Rana, Meenakshi, additional, Zhang, Weijia, additional, Akalin, Enver, additional, Cravedi, Paolo, additional, Heeger, Peter S., additional, and Menon, Madhav C., additional

Published
2022
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15. The impact of dupilumab treatment on SARS‐CoV‐2 T cell responses in atopic dermatitis patients.

Author

Ungar, Benjamin, Hartzell, Susan, Lozano‐Ojalvo, Daniel, Ghalili, Sabrina, Bose, Swaroop, Golant, Alexandra K., Tan, Kathryn, Estrada, Yeriel D., Singer, Giselle K., Pavel, Ana B., Cravedi, Paolo, and Guttman‐Yassky, Emma

Subjects
*T cells, *SARS-CoV-2, *ATOPIC dermatitis, *DUPILUMAB, *MONONUCLEAR leukocytes, *THYMIC stromal lymphopoietin
Abstract

Overall, this study suggests that Th2-inhibition with dupilumab does not hinder, and may possibly even improve, Th1-specific T cell responses to COVID-19 infection and mRNA vaccination. Fifty-five samples from patients with prior SARS-CoV-2 infection confirmed by positive anti-SARS-CoV-2 Spike IgG (unvaccinated at the time of sample collection), and 125 post-vaccination samples from different subjects were analyzed. Spike antigens were used to provide comparisons between treatment groups as a measure of T cell responses for both post-infection and post-vaccination samples (the vaccine contains only spike antigen of SARS-CoV-2). [Extracted from the article]

Published
2023
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17. Delayed Kinetics of IgG, but Not IgA, Antispike Antibodies in Transplant Recipients following SARS-CoV-2 Infection

Author

Cravedi, Paolo, primary, Ahearn, Patrick, additional, Wang, Lin, additional, Yalamarti, Tanuja, additional, Hartzell, Susan, additional, Azzi, Yorg, additional, Menon, Madhav C., additional, Jain, Aditya, additional, Billah, Marzuq, additional, Fernandez-Vina, Marcelo, additional, Gebel, Howard M., additional, Woodle, E. Steve, additional, Haddad, Natalie S., additional, Morrison-Porter, Andrea, additional, Lee, F. Eun-Hyung, additional, Sanz, Ignacio, additional, Akalin, Enver, additional, Girnita, Alin, additional, and Maltzman, Jonathan S., additional

Published
2021
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18. Erythropoietin Reduces Auto- and Alloantibodies by Inhibiting T Follicular Helper Cell Differentiation

Author

Guglielmo, Chiara, primary, Bin, Sofia, additional, Cantarelli, Chiara, additional, Hartzell, Susan, additional, Angeletti, Andrea, additional, Donadei, Chiara, additional, Cumpelik, Arun, additional, Anderson, Lisa, additional, Cody, Evan, additional, Sage, Peter T., additional, La Manna, Gaetano, additional, Fiaccadori, Enrico, additional, Heeger, Peter S., additional, and Cravedi, Paolo, additional

Published
2021
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21. Kidney Failure Associates With T Cell Exhaustion and Imbalanced Follicular Helper T Cells

Author

Hartzell, Susan, primary, Bin, Sofia, additional, Cantarelli, Chiara, additional, Haverly, Meredith, additional, Manrique, Joaquin, additional, Angeletti, Andrea, additional, Manna, Gaetano La, additional, Murphy, Barbara, additional, Zhang, Weijia, additional, Levitsky, Josh, additional, Gallon, Lorenzo, additional, Yu, Samuel Mon-Wei, additional, and Cravedi, Paolo, additional

Published
2020
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22. Loss of decay-accelerating factor triggers podocyte injury and glomerulosclerosis

Author

Angeletti, Andrea, primary, Cantarelli, Chiara, additional, Petrosyan, Astgik, additional, Andrighetto, Sofia, additional, Budge, Kelly, additional, D’Agati, Vivette D., additional, Hartzell, Susan, additional, Malvi, Deborah, additional, Donadei, Chiara, additional, Thurman, Joshua M., additional, Galešić-Ljubanović, Danica, additional, He, John Cijiang, additional, Xiao, Wenzhen, additional, Campbell, Kirk N., additional, Wong, Jenny, additional, Fischman, Clara, additional, Manrique, Joaquin, additional, Zaza, Gianluigi, additional, Fiaccadori, Enrico, additional, La Manna, Gaetano, additional, Fribourg, Miguel, additional, Leventhal, Jeremy, additional, Da Sacco, Stefano, additional, Perin, Laura, additional, Heeger, Peter S., additional, and Cravedi, Paolo, additional

Published
2020
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23. Pneumococcal Polysaccharide Vaccine Ameliorates Murine Lupus

Author

Cantarelli, Chiara, primary, Guglielmo, Chiara, additional, Hartzell, Susan, additional, Salem, Fadi El, additional, Andrighetto, Sofia, additional, Gazivoda, Victor P., additional, Fiaccadori, Enrico, additional, La Manna, Gaetano, additional, Zaza, Gianluigi, additional, Leventhal, Jeremy, additional, Tassiulas, Ioannis, additional, and Cravedi, Paolo, additional

Published
2019
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24. Erythropoietin inhibits SGK1-dependent Th17 cell induction and Th17 cell–dependent kidney disease

Author

Donadei, Chiara, primary, Angeletti, Andrea, additional, Cantarelli, Chiara, additional, D’Agati, Vivette D., additional, La Manna, Gaetano, additional, Fiaccadori, Enrico, additional, Horwitz, Julian K., additional, Xiong, Huabao, additional, Guglielmo, Chiara, additional, Hartzell, Susan, additional, Madsen, Joren C., additional, Maggiore, Umberto, additional, Heeger, Peter S., additional, and Cravedi, Paolo, additional

Published
2019
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27. Erythropoietin administration expands regulatory T cells in patients with autoimmune hepatitis

Author

Elisa McEachern, Miguel Fribourg, Paolo Cravedi, Susan Hartzell, Allison M. Carroll, Thomas D. Schiano, Sofia Bin, Josh Levitsky, McEachern, Elisa, Carroll, Allison M, Fribourg, Miguel, Schiano, Thomas D, Hartzell, Susan, Bin, Sofia, Cravedi, Paolo, and Levitsky, Josh

Subjects
0301 basic medicine, Adult, Male, Regulatory T cell, medicine.medical_treatment, T cell, Immunology, chemical and pharmacologic phenomena, Autoimmune hepatitis, Autoimmune hepatiti, Chronic liver disease, Lymphocyte Activation, T-Lymphocytes, Regulatory, Immunophenotyping, Immunomodulation, 03 medical and health sciences, 0302 clinical medicine, hemic and lymphatic diseases, medicine, Immunology and Allergy, Humans, Lymphocyte Count, Erythropoietin, Aged, 030203 arthritis & rheumatology, Duration of Therapy, business.industry, Immunosuppression, hemic and immune systems, Middle Aged, medicine.disease, Treg, Hepatitis, Autoimmune, 030104 developmental biology, medicine.anatomical_structure, Treatment Outcome, Cytokines, Female, business, Ex vivo, CD8, Biomarkers, medicine.drug, EPO
Abstract

Objective Autoimmune hepatitis (AIH) is a chronic liver disease associated with impaired regulatory T cell (Treg) number and function. Erythropoietin (EPO) is a kidney-produced erythropoietic hormone that has known immune-modulating effects, including Treg induction. Whether EPO administration increases Treg in patients with AIH is unknown. Methods We treated six stable AIH patients with a single 1000 IU dose of EPO and comprehensively characterized changes in Treg overall and in Treg subsets before and at 4 and 12 weeks after treatment using mass cytometry (CyTOF) combined with an unbiased clustering approach (Phenograph) based on 22 Treg-relevant cell-surface markers. Results EPO was well-tolerated and no patients showed significant changes in hematological parameters, liver enzymes, or IgG levels from baseline to 12 weeks following EPO administration. Total Treg and Treg/CD8+ T cell ratios significantly increased at 4 weeks and returned to baseline levels at 12 weeks after EPO injection. We identified 17 Treg subsets of which CD4+CD25HICD127NEG HLADR+ Treg had the highest increase and the most favorable Treg/CD8+ ratio upon EPO treatment. At 12 weeks after EPO administration, the HLADR+ Treg subset also returned to values comparable to those at baseline. Ex vivo assays documented that Treg were functional and the ones isolated at 12 weeks after EPO injection were significantly more suppressive than the ones isolated at baseline. In Treg-depleted assays, EPO did not show a significant effect on IFN-γ+, IL-2+, and IL-17+ CD4+ T cells. Conclusion In stable AIH patients, EPO increases overall Treg and particularly those expressing the high function marker HLA-DR. These results provide the rationale for future studies testing the hypothesis that EPO or EPO analogues improve outcomes of AIH patients by increasing Treg.

Published
2021

28. Erythropoietin inhibits SGK1-dependent TH17 induction and TH17-dependent kidney disease

Author

Paolo Cravedi, Susan Hartzell, Chiara Cantarelli, Chiara Donadei, Huabao Xiong, Vivette D. D'Agati, Julian K. Horwitz, Andrea Angeletti, Umberto Maggiore, Joren C. Madsen, Enrico Fiaccadori, Peter S. Heeger, Gaetano La Manna, Chiara Guglielmo, Donadei, Chiara, Angeletti, Andrea, Cantarelli, Chiara, D'Agati, Vivette D, La Manna, Gaetano, Fiaccadori, Enrico, Horwitz, Julian K, Xiong, Huabao, Guglielmo, Chiara, Hartzell, Susan, Madsen, Joren C, Maggiore, Umberto, Heeger, Peter S, and Cravedi, Paolo

Subjects
0301 basic medicine, Male, Mice, Inbred MRL lpr, medicine.disease_cause, Severity of Illness Index, T-Lymphocytes, Regulatory, Autoimmunity, Mice, 0302 clinical medicine, hemic and lymphatic diseases, Receptors, Erythropoietin, Phosphorylation, Receptor, Cells, Cultured, Chemistry, Interleukin-17, Glomerulonephritis, General Medicine, Acquired immune system, Lupus Nephritis, Nephrology, 030220 oncology & carcinogenesis, Aristolochic Acids, Female, medicine.drug, Research Article, Adaptive immunity, Immunology, Primary Cell Culture, Mice, Transgenic, Protein Serine-Threonine Kinases, Immediate-Early Proteins, 03 medical and health sciences, Downregulation and upregulation, medicine, Animals, Humans, Erythropoietin, T cell, Receptors, Interleukin, medicine.disease, Epoetin Alfa, Disease Models, Animal, 030104 developmental biology, Cancer research, SGK1, Nephritis, Interstitial, Th17 Cells, Tolerance, Kidney disease
Abstract

IL-17–producing CD4(+) (Th17) cells are pathogenically linked to autoimmunity and, specifically, to autoimmune kidney disease. The newly recognized immunoregulatory functions of erythropoietin (EPO) and its predominant intrarenal source suggested that EPO physiologically regulates Th17 cell differentiation, thereby serving as a barrier to development of autoimmune kidney disease. Using in vitro studies of human and murine cells and in vivo models, we show that EPO ligation of its receptor (EPO-R) on CD4(+) T cells directly inhibits Th17 cell generation and promotes transdifferentiation of Th17 cells into IL-17(–)FOXP3(+)CD4(+) T cells. Mechanistically, EPO/EPO-R ligation abrogates upregulation of SGK1 gene expression and blocks p38 activity to prevent SGK1 phosphorylation, thereby inhibiting RORC-mediated transcription of IL17 and IL23 receptor genes. In a murine model of Th17 cell–dependent aristolochic acid–induced interstitial kidney disease associated with reduced renal EPO production, we demonstrate that transgenic EPO overexpression or recombinant EPO (rEPO) administration limits Th17 cell formation and clinical/histological disease expression. EPO/EPO-R ligations on CD4(+) T cells abrogate, while absence of T cell–expressed EPO-R augments, Th17 cell induction and clinical/histological expression of pristane-induced glomerulonephritis (associated with decreased intrarenal EPO). rEPO prevents spontaneous glomerulonephritis and Th17 cell generation in MRL-lpr mice. Together, our findings indicate that EPO physiologically and therapeutically modulates Th17 cells to limit expression of Th17 cell–associated autoimmune kidney disease.

Published
2019

29. Blood transcriptomes of SARS-CoV-2 infected kidney transplant recipients demonstrate immune insufficiency.

Author

Sun Z, Zhang Z, Banu K, Azzi YA, Reghuvaran A, Fredericks S, Planoutene M, Hartzell S, Pell J, Tietjen G, Asch W, Kulkarni S, Formica R, Rana M, Zhang W, Akalin E, Cravedi P, Heeger PS, and Menon MC

Abstract

Background: Kidney transplant recipients (KTRs) with COVID-19 have poor outcomes compared to non-KTRs. To provide insight into management of immunosuppression during acute illness, we studied immune signatures from the peripheral blood during and after COVID-19 infection from a multicenter KTR cohort.□., Methods: Clinical data were collected by chart review. PAXgene blood RNA was poly-A selected and RNA sequencing was performed to evaluate transcriptome changes., Results: A total of 64 cases of COVID-19 in KTRs were enrolled, including 31 acute cases (< 4 weeks from diagnosis) and 33 post-acute cases (>4 weeks). In the blood transcriptome of acute cases, we identified differentially expressed genes (DEGs) in positive or negative association COVID-19 severity scores. Functional enrichment analyses showed upregulation of neutrophil and innate immune pathways, but downregulation of T-cell and adaptive immune-activation pathways proportional to severity score. This finding was independent of lymphocyte count and despite reduction in immunosuppression (IS) in most KTRs. Comparison with post-acute cases showed "normalization" of these enriched pathways after >4 weeks, suggesting recovery of adaptive immune system activation despite reinstitution of IS. The latter analysis was adjusted for COVID-19 severity score and lymphocyte count. DEGs associated with worsening disease severity in a non-KTR cohort with COVID-19 (GSE152418) showed significant overlap with KTRs in these identified enriched pathways., Conclusion: Blood transcriptome of KTRs affected by COVID-19 shows decrease in T-cell and adaptive immune activation pathways during acute disease that associate with severity despite IS reduction and show recovery after acute illness., Significance Statement: Kidney transplant recipients (KTRs) are reported to have worse outcomes with COVID-19, and empiric reduction of maintenance immunosuppression is pursued. Surprisingly, reported rates of acute rejection have been low despite reduced immunosuppression. We evaluated the peripheral blood transcriptome of 64 KTRs either during or after acute COVID-19. We identified transcriptomic signatures consistent with suppression of adaptive T-cell responses which significantly associated with disease severity and showed evidence of recovery after acute disease, even after adjustment for lymphocyte number. Our transcriptomic findings of immune-insufficiency during acute COVID-19 provide an explanation for the low rates of acute rejection in KTRs despite reduced immunosuppression. Our data support the approach of temporarily reducing T -cell-directed immunosuppression in KTRs with acute COVID-19.

Published
2022
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30. Erythropoietin inhibits SGK1-dependent TH17 induction and TH17-dependent kidney disease.

Author

Donadei C, Angeletti A, Cantarelli C, D'Agati VD, La Manna G, Fiaccadori E, Horwitz JK, Xiong H, Guglielmo C, Hartzell S, Madsen JC, Maggiore U, Heeger PS, and Cravedi P

Subjects
Animals, Aristolochic Acids toxicity, Cells, Cultured, Disease Models, Animal, Epoetin Alfa administration & dosage, Erythropoietin genetics, Female, Humans, Interleukin-17 immunology, Interleukin-17 metabolism, Lupus Nephritis diagnosis, Lupus Nephritis drug therapy, Male, Mice, Mice, Inbred MRL lpr, Mice, Transgenic, Nephritis, Interstitial chemically induced, Phosphorylation immunology, Primary Cell Culture, Receptors, Erythropoietin metabolism, Receptors, Interleukin metabolism, Severity of Illness Index, T-Lymphocytes, Regulatory immunology, T-Lymphocytes, Regulatory metabolism, Th17 Cells metabolism, Erythropoietin metabolism, Immediate-Early Proteins metabolism, Lupus Nephritis immunology, Nephritis, Interstitial immunology, Protein Serine-Threonine Kinases metabolism, Th17 Cells immunology
Abstract

IL-17-producing CD4+ cells (TH17) are pathogenically linked to autoimmunity including to autoimmune kidney disease. Erythropoietin's (EPO) newly recognized immunoregulatory functions and its predominant intra-renal source suggested that EPO physiologically regulates TH17 differentiation, thereby serving as a barrier to the development of autoimmune kidney disease. Using in vitro studies of human and murine cells and in vivo models, we show that EPO ligation of its receptor (EPO-R) on CD4+ T cells directly inhibits TH17 generation and promotes trans-differentiation of TH17 into IL-17-FOXP3+CD4+ T cells. Mechanistically, EPO/EPO-R ligation abrogates upregulation of SGK1 gene expression and blocks p38 activity to prevent SGK1 phosphorylation, thereby inhibiting RORC-mediated transcription of IL-17 and IL-23 receptor genes. In a murine model of TH17-dependent aristolochic acid (ArA)-induced, interstitial kidney disease associated with reduced renal EPO production, we demonstrate that transgenic EPO overexpression or recombinant EPO (rEPO) administration limits TH17 formation and clinical/histological disease expression. EPO/EPO-R ligations on CD4+ T cells abrogate, while absence of T cell-expressed EPO-R augments, TH17 induction and clinical/histological expression of pristane-induced glomerulonephritis (associated with decreased intrarenal EPO). rEPO prevents spontaneous glomerulonephritis and TH17 generation in MRL-lpr mice. Together, our findings indicate that EPO physiologically and therapeutically modulate TH17 cells to limit expression of TH17-associated autoimmune kidney disease.

Published
2019
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