Integrated omics profiling reveals systemic dysregulation and potential biomarkers in the blood of patients with neuromyelitis optica spectrum disorders
Abstract Background Neuromyelitis optica spectrum disorders (NMOSD) are autoimmune conditions that affect the central nervous system. The contribution of peripheral abnormalities to the disease's pathogenesis is not well understood. Methods To investigate this, we employed a multi-omics approac...
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BMC
2024-11-01
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| Series: | Journal of Translational Medicine |
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| Online Access: | https://doi.org/10.1186/s12967-024-05801-8 |
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| author | Zuoquan Xie Qinming Zhou Jin Hu Lu He Huangyu Meng Xiaoni Liu Guangqiang Sun Zhiyu Luo Yuan Feng Liang Li Xingkun Chu Chen Du Dabing Yang Xinying Yang Jing Zhang Changrong Ge Xiang Zhang Sheng Chen Meiyu Geng |
| author_facet | Zuoquan Xie Qinming Zhou Jin Hu Lu He Huangyu Meng Xiaoni Liu Guangqiang Sun Zhiyu Luo Yuan Feng Liang Li Xingkun Chu Chen Du Dabing Yang Xinying Yang Jing Zhang Changrong Ge Xiang Zhang Sheng Chen Meiyu Geng |
| author_sort | Zuoquan Xie |
| collection | DOAJ |
| description | Abstract Background Neuromyelitis optica spectrum disorders (NMOSD) are autoimmune conditions that affect the central nervous system. The contribution of peripheral abnormalities to the disease's pathogenesis is not well understood. Methods To investigate this, we employed a multi-omics approach analyzing blood samples from 52 NMOSD patients and 46 healthy controls (HC). This included mass cytometry, cytokine arrays, and targeted metabolomics. We then analyzed the peripheral changes of NMOSD, and features related to NMOSD's disease severity. Furthermore, an integrative analysis was conducted to identify the distinguishing characteristics of NMOSD from HC. Additionally, we unveiled the variations in peripheral features among different clinical subgroups within NMOSD. An independent cohort of 40 individuals with NMOSD was utilized to assess the serum levels of fibroblast activation protein alpha (FAP). Results Our analysis revealed a distinct peripheral immune and metabolic signature in NMOSD patients. This signature is characterized by an increase in monocytes and a decrease in regulatory T cells, dendritic cells, natural killer cells, and various T cell subsets. Additionally, we found elevated levels of inflammatory cytokines and reduced levels of tissue-repair cytokines. Metabolic changes were also evident, with higher levels of bile acids, lactates, triglycerides, and lower levels of dehydroepiandrosterone sulfate, homoarginine, octadecadienoic acid (FA[18:2]), and sphingolipids. We identified distinctive biomarkers differentiating NMOSD from HC and found blood factors correlating with disease severity. Among these, fibroblast activation protein alpha (FAP) was a notable marker of disease progression. Conclusions Our comprehensive blood profile analysis offers new insights into NMOSD pathophysiology, revealing significant peripheral immune and metabolic alterations. This work lays the groundwork for future biomarker identification and mechanistic studies in NMOSD, highlighting the potential of FAP as a marker of disease progression. |
| format | Article |
| id | doaj-art-e3952ee527f34a49be4aefe9a3a8f255 |
| institution | OA Journals |
| issn | 1479-5876 |
| language | English |
| publishDate | 2024-11-01 |
| publisher | BMC |
| record_format | Article |
| series | Journal of Translational Medicine |
| spelling | doaj-art-e3952ee527f34a49be4aefe9a3a8f2552025-08-20T02:18:25ZengBMCJournal of Translational Medicine1479-58762024-11-0122111810.1186/s12967-024-05801-8Integrated omics profiling reveals systemic dysregulation and potential biomarkers in the blood of patients with neuromyelitis optica spectrum disordersZuoquan Xie0Qinming Zhou1Jin Hu2Lu He3Huangyu Meng4Xiaoni Liu5Guangqiang Sun6Zhiyu Luo7Yuan Feng8Liang Li9Xingkun Chu10Chen Du11Dabing Yang12Xinying Yang13Jing Zhang14Changrong Ge15Xiang Zhang16Sheng Chen17Meiyu Geng18State Key Laboratory of Drug Research, Shanghai Institute of Materia Medica, Chinese Academy of SciencesDepartment of Neurology, Ruijin Hospital, Shanghai Jiaotong University School of MedicineDepartment of Neurology, Affiliated Hospital of Jiaxing UniversityDepartment of Neurology, Ruijin Hospital, Shanghai Jiaotong University School of MedicineDepartment of Neurology, Ruijin Hospital, Shanghai Jiaotong University School of MedicineDepartment of Neurology, Huashan Hospital Fudan University and Institute of Neurology, Fudan UniversityShanghai Green Valley Pharmaceutical Co., LtdShanghai Green Valley Pharmaceutical Co., LtdShanghai Green Valley Pharmaceutical Co., LtdShanghai Green Valley Pharmaceutical Co., LtdShanghai Green Valley Pharmaceutical Co., LtdShanghai Green Valley Pharmaceutical Co., LtdShanghai Green Valley Pharmaceutical Co., LtdShanghai Green Valley Pharmaceutical Co., LtdShanghai Green Valley Pharmaceutical Co., LtdShanghai Green Valley Pharmaceutical Co., LtdDepartment of Neurology, Huashan Hospital Fudan University and Institute of Neurology, Fudan UniversityDepartment of Neurology, Ruijin Hospital, Shanghai Jiaotong University School of MedicineState Key Laboratory of Drug Research, Shanghai Institute of Materia Medica, Chinese Academy of SciencesAbstract Background Neuromyelitis optica spectrum disorders (NMOSD) are autoimmune conditions that affect the central nervous system. The contribution of peripheral abnormalities to the disease's pathogenesis is not well understood. Methods To investigate this, we employed a multi-omics approach analyzing blood samples from 52 NMOSD patients and 46 healthy controls (HC). This included mass cytometry, cytokine arrays, and targeted metabolomics. We then analyzed the peripheral changes of NMOSD, and features related to NMOSD's disease severity. Furthermore, an integrative analysis was conducted to identify the distinguishing characteristics of NMOSD from HC. Additionally, we unveiled the variations in peripheral features among different clinical subgroups within NMOSD. An independent cohort of 40 individuals with NMOSD was utilized to assess the serum levels of fibroblast activation protein alpha (FAP). Results Our analysis revealed a distinct peripheral immune and metabolic signature in NMOSD patients. This signature is characterized by an increase in monocytes and a decrease in regulatory T cells, dendritic cells, natural killer cells, and various T cell subsets. Additionally, we found elevated levels of inflammatory cytokines and reduced levels of tissue-repair cytokines. Metabolic changes were also evident, with higher levels of bile acids, lactates, triglycerides, and lower levels of dehydroepiandrosterone sulfate, homoarginine, octadecadienoic acid (FA[18:2]), and sphingolipids. We identified distinctive biomarkers differentiating NMOSD from HC and found blood factors correlating with disease severity. Among these, fibroblast activation protein alpha (FAP) was a notable marker of disease progression. Conclusions Our comprehensive blood profile analysis offers new insights into NMOSD pathophysiology, revealing significant peripheral immune and metabolic alterations. This work lays the groundwork for future biomarker identification and mechanistic studies in NMOSD, highlighting the potential of FAP as a marker of disease progression.https://doi.org/10.1186/s12967-024-05801-8Neuromyelitis optica spectrum disordersBlood immune cells phenotypingPlasma cytokine arrayPlasma metabolomicsBiomarker |
| spellingShingle | Zuoquan Xie Qinming Zhou Jin Hu Lu He Huangyu Meng Xiaoni Liu Guangqiang Sun Zhiyu Luo Yuan Feng Liang Li Xingkun Chu Chen Du Dabing Yang Xinying Yang Jing Zhang Changrong Ge Xiang Zhang Sheng Chen Meiyu Geng Integrated omics profiling reveals systemic dysregulation and potential biomarkers in the blood of patients with neuromyelitis optica spectrum disorders Journal of Translational Medicine Neuromyelitis optica spectrum disorders Blood immune cells phenotyping Plasma cytokine array Plasma metabolomics Biomarker |
| title | Integrated omics profiling reveals systemic dysregulation and potential biomarkers in the blood of patients with neuromyelitis optica spectrum disorders |
| title_full | Integrated omics profiling reveals systemic dysregulation and potential biomarkers in the blood of patients with neuromyelitis optica spectrum disorders |
| title_fullStr | Integrated omics profiling reveals systemic dysregulation and potential biomarkers in the blood of patients with neuromyelitis optica spectrum disorders |
| title_full_unstemmed | Integrated omics profiling reveals systemic dysregulation and potential biomarkers in the blood of patients with neuromyelitis optica spectrum disorders |
| title_short | Integrated omics profiling reveals systemic dysregulation and potential biomarkers in the blood of patients with neuromyelitis optica spectrum disorders |
| title_sort | integrated omics profiling reveals systemic dysregulation and potential biomarkers in the blood of patients with neuromyelitis optica spectrum disorders |
| topic | Neuromyelitis optica spectrum disorders Blood immune cells phenotyping Plasma cytokine array Plasma metabolomics Biomarker |
| url | https://doi.org/10.1186/s12967-024-05801-8 |
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