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Article ; Online: Treatment of human cardiac fibroblasts with the protein arginine deiminase inhibitor BB-Cl-amidine activates the Nrf2/HO-1 signaling pathway.

Stachowicz, Aneta / Sadiq, Alia / Walker, Brian / Sundararaman, Niveda / Fert-Bober, Justyna

Biomedicine & pharmacotherapy = Biomedecine & pharmacotherapie

2023 Volume 167, Page(s) 115443

Abstract: Background: Cardiac fibrosis contributes to end-stage extracellular matrix remodeling and heart failure (HF). Cardiac fibroblasts (CFs) differentiate into myofibroblasts (myoFbs) to preserve the structural integrity of the heart; however, the molecular ... ...

Abstract	Background: Cardiac fibrosis contributes to end-stage extracellular matrix remodeling and heart failure (HF). Cardiac fibroblasts (CFs) differentiate into myofibroblasts (myoFbs) to preserve the structural integrity of the heart; however, the molecular mechanisms regulating CF transdifferentiation remain poorly understood. Protein arginine deiminase (PAD), which converts arginine to citrulline, has been shown to play a role in myocardial infarction, fibrosis, and HF. This study aimed to investigate the role of PAD in CF differentiation to myoFbs and identify the citrullinated proteins that were associated with phenotypic changes in CFs. Results: Gene expression analysis showed that PAD1 and PAD2 isoforms, but not PAD4 isoforms, were abundant in both CFs and myoFbs, and PAD1 was significantly upregulated in myoFbs. The pan-PAD inhibitor BB-Cl-amidine (BB-Cl) downregulated the mRNA expression of PAD1 and PAD2 as well as the protein expression of the fibrosis marker COL1A1 in CFs and myoFbs. Interestingly, a proteomic approach pointed to the activation of the Nrf2/HO-1 signaling pathway upon BB-Cl treatment in CFs and myoFbs. BB-Cl administration resulted in the upregulation of HO-1 at both the gene and protein levels in CFs and myoFbs. Importantly, the protein citrullination landscape of CFs consisting of 86 novel citrullination sites associated with focal adhesion (FN1(R1054)), inflammation (TAGLN(R12)) and DNA replication (EEF2(R767)) pathways was identified. Conclusions: In summary, we revealed that BB-Cl treatment resulted in increased HO-1 expression via the Nrf2 pathway, which could prevent excessive tissue damage, thereby leading to substantial clinical benefits for the treatment of cardiac fibrosis.
Language	English
Publishing date	2023-09-11
Publishing country	France
Document type	Journal Article
ZDB-ID	392415-4
ISSN	1950-6007 ; 0753-3322 ; 0300-0893
ISSN (online)	1950-6007
ISSN	0753-3322 ; 0300-0893
DOI	10.1016/j.biopha.2023.115443
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Article ; Online: Role of protein deimination in cardiovascular diseases: potential new avenues for diagnostic and prognostic biomarkers.

Mao, Liqun / Mostafa, Rowann / Ibili, Esra / Fert-Bober, Justyna

Expert review of proteomics

2022 Volume 18, Issue 12, Page(s) 1059–1071

Abstract: Introduction: Arginine deimination (citrullination) is a post-translational modification catalyzed by a family of peptidyl arginine deiminase (PAD) enzymes. Cell-based functional studies and animal models have manifested the key role of PADs in various ... ...

Abstract	Introduction: Arginine deimination (citrullination) is a post-translational modification catalyzed by a family of peptidyl arginine deiminase (PAD) enzymes. Cell-based functional studies and animal models have manifested the key role of PADs in various cardiovascular diseases (CVDs). Area covered: This review summarizes the past 10 years of knowledge on the role of PADs in CVD pathogenesis. It focuses on the PAD functions and diverse citrullinated proteins in cardiovascular conditions like deep vein thrombosis, ischemia/reperfusion, and atherosclerosis. Identification of PAD isoforms and citrullinated targets are essential for directing diagnosis and clinical intervention. Finally, anti-citrullinated protein antibodies (ACPAs) are addressed as an independent risk factor for cardiovascular events. Expert opinion: PAD is an unique family of enzymes that permanently converts amino acid arginine to amino acid citrulline in protein . Overexpression or increased activity of PAD has been observed in various CVDs with acute and chronic inflammation as the background. Importantly, far beyond being simply involved in forming neutrophil extracellular traps (NETs), accumulating evidence indicated PAD activation as a trigger for numerous processes, such as transcriptional regulation, endothelial dysfunction, and thrombus formation. In summary, the findings so far have testified the important role of deimination in cardiovascular biology, while more basic and translational studies are essential for further exploration.
MeSH term(s)	Animals ; Biomarkers ; Cardiovascular Diseases ; Citrullination ; Prognosis ; Protein Processing, Post-Translational ; Protein-Arginine Deiminases/genetics ; Protein-Arginine Deiminases/metabolism
Chemical Substances	Biomarkers ; Protein-Arginine Deiminases (EC 3.5.3.15)
Language	English
Publishing date	2022-01-12
Publishing country	England
Document type	Journal Article ; Review
ZDB-ID	2299100-1
ISSN	1744-8387 ; 1478-9450
ISSN (online)	1744-8387
ISSN	1478-9450
DOI	10.1080/14789450.2021.2018303
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Article ; Online: An Update on Diagnostic Laboratory Biomarkers for Multiple Sclerosis.

Kaisey, Marwa / Lashgari, Ghazal / Fert-Bober, Justyna / Ontaneda, Daniel / Solomon, Andrew J / Sicotte, Nancy L

Current neurology and neuroscience reports

2022 Volume 22, Issue 10, Page(s) 675–688

Abstract: Purpose: For many patients, the multiple sclerosis (MS) diagnostic process can be lengthy, costly, and fraught with error. Recent research aims to address the unmet need for an accurate and simple diagnostic process through discovery of novel diagnostic ...

Abstract	Purpose: For many patients, the multiple sclerosis (MS) diagnostic process can be lengthy, costly, and fraught with error. Recent research aims to address the unmet need for an accurate and simple diagnostic process through discovery of novel diagnostic biomarkers. This review summarizes recent studies on MS diagnostic fluid biomarkers, with a focus on blood biomarkers, and includes discussion of technical limitations and practical applicability. Recent findings: This line of research is in its early days. Accurate and easily obtainable biomarkers for MS have not yet been identified and validated, but several approaches to uncover them are underway. Continue efforts to define laboratory diagnostic biomarkers are likely to play an increasingly important role in defining MS at the earliest stages, leading to better long-term clinical outcomes.
MeSH term(s)	Humans ; Multiple Sclerosis/diagnosis ; Biomarkers
Chemical Substances	Biomarkers
Language	English
Publishing date	2022-10-21
Publishing country	United States
Document type	Journal Article ; Review ; Research Support, Non-U.S. Gov't
ZDB-ID	2057363-7
ISSN	1534-6293 ; 1528-4042
ISSN (online)	1534-6293
ISSN	1528-4042
DOI	10.1007/s11910-022-01227-1
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Article ; Online: Insights into the study and origin of the citrullinome in rheumatoid arthritis.

Fert-Bober, Justyna / Darrah, Erika / Andrade, Felipe

Immunological reviews

2019 Volume 294, Issue 1, Page(s) 133–147

Abstract: The presence of autoantibodies and autoreactive T cells to citrullinated proteins and citrullinating enzymes in patients with rheumatoid arthritis (RA), together with the accumulation of citrullinated proteins in rheumatoid joints, provides substantial ... ...

Abstract	The presence of autoantibodies and autoreactive T cells to citrullinated proteins and citrullinating enzymes in patients with rheumatoid arthritis (RA), together with the accumulation of citrullinated proteins in rheumatoid joints, provides substantial evidence that dysregulated citrullination is a hallmark feature of RA. However, understanding mechanisms that dysregulate citrullination in RA has important challenges. Citrullination is a normal process in immune and non-immune cells, which is likely activated by different conditions (eg, inflammation) with no pathogenic consequences. In a complex inflammatory environment such as the RA joint, unique strategies are therefore required to dissect specific mechanisms involved in the abnormal production of citrullinated proteins. Here, we will review current models of citrullination in RA and discuss critical components that, in our view, are relevant to understanding the accumulation of citrullinated proteins in the RA joint, collectively referred to as the RA citrullinome. In particular, we will focus on potential caveats in the study of citrullination in RA and will highlight methods to precisely detect citrullinated proteins in complex biological samples, which is a confirmatory approach to mechanistically link the RA citrullinome with unique pathogenic pathways in RA.
MeSH term(s)	Animals ; Anti-Citrullinated Protein Antibodies/metabolism ; Arthritis, Rheumatoid/immunology ; Arthritis, Rheumatoid/metabolism ; Autoantibodies/metabolism ; Autoimmunity ; Citrullination ; Citrulline/metabolism ; Extracellular Traps/metabolism ; Female ; Humans ; Protein-Arginine Deiminases/metabolism
Chemical Substances	Anti-Citrullinated Protein Antibodies ; Autoantibodies ; Citrulline (29VT07BGDA) ; Protein-Arginine Deiminases (EC 3.5.3.15)
Language	English
Publishing date	2019-12-25
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	391796-4
ISSN	1600-065X ; 0105-2896
ISSN (online)	1600-065X
ISSN	0105-2896
DOI	10.1111/imr.12834
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Article ; Online: pH/Acetonitrile-Gradient Reversed-Phase Fractionation of Enriched Hyper-Citrullinated Library in Combination with LC-MS/MS Analysis for Confident Identification of Citrullinated Peptides.

Stachowicz, Aneta / Sundararaman, Niveda / Venkatraman, Vidya / Van Eyk, Jennifer / Fert-Bober, Justyna

Methods in molecular biology (Clifton, N.J.)

2021 Volume 2420, Page(s) 107–126

Abstract: Citrullination, the ... ...

Abstract	Citrullination, the Ca
MeSH term(s)	Acetonitriles ; Chromatography, Liquid ; Citrulline ; Hydrogen-Ion Concentration ; Peptides ; Proteome ; Proteomics ; Tandem Mass Spectrometry
Chemical Substances	Acetonitriles ; Peptides ; Proteome ; Citrulline (29VT07BGDA)
Language	English
Publishing date	2021-12-13
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ISSN	1940-6029
ISSN (online)	1940-6029
DOI	10.1007/978-1-0716-1936-0_9
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Article: Protein arginine deiminase 2 (PAD2) modulates the polarization of THP-1 macrophages to the anti-inflammatory M2 phenotype.

Stachowicz, Aneta / Pandey, Rakhi / Sundararaman, Niveda / Venkatraman, Vidya / Van Eyk, Jennifer E / Fert-Bober, Justyna

Journal of inflammation (London, England)

2022 Volume 19, Issue 1, Page(s) 20

Abstract: Background: Macrophages are effector cells of the innate immune system that undergo phenotypical changes in response to organ injury and repair. These cells are most often classified as proinflammatory M1 and anti-inflammatory M2 macrophages. Protein ... ...

Abstract	Background: Macrophages are effector cells of the innate immune system that undergo phenotypical changes in response to organ injury and repair. These cells are most often classified as proinflammatory M1 and anti-inflammatory M2 macrophages. Protein arginine deiminase (PAD), which catalyses the irreversible conversion of protein-bound arginine into citrulline, is expressed in macrophages. However, the substrates of PAD and its role in immune cells remain unclear. This study aimed to investigate the role of PAD in THP-1 macrophage polarization to the M1 and M2 phenotypes and identify the citrullinated proteins and modified arginines that are associated with this biological switch using mass spectrometry. Results: Our study showed that PAD2 and, to a lesser extent, PAD1 and PAD4 were predominantly expressed in M1 macrophages. We showed that inhibiting PAD expression with BB-Cl-amidine decreased macrophage polarization to the M1 phenotype (TNF-α, IL-6) and increased macrophage polarization to the M2 phenotype (MRC1, ALOX15). This process was mediated by the downregulation of proteins involved in the NF-κβ pathway. Silencing PAD2 confirmed the activation of M2 macrophages by increasing the antiviral innate immune response and interferon signalling. A total of 192 novel citrullination sites associated with inflammation, cell death and DNA/RNA processing pathways were identified in M1 and M2 macrophages. Conclusions: We showed that inhibiting PAD activity using a pharmacological inhibitor or silencing PAD2 with PAD2 siRNA shifted the activation of macrophages towards the M2 phenotype, which can be crucial for designing novel macrophage-mediated therapeutic strategies. We revealed a major citrullinated proteome and its rearrangement following macrophage polarization, which after further validation could lead to significant clinical benefits for the treatment of inflammation and autoimmune diseases.
Language	English
Publishing date	2022-11-18
Publishing country	England
Document type	Journal Article
ZDB-ID	2164385-4
ISSN	1476-9255
ISSN	1476-9255
DOI	10.1186/s12950-022-00317-8
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Article ; Online: BIRCH: An Automated Workflow for Evaluation, Correction, and Visualization of Batch Effect in Bottom-Up Mass Spectrometry-Based Proteomics Data.

Sundararaman, Niveda / Bhat, Archana / Venkatraman, Vidya / Binek, Aleksandra / Dwight, Zachary / Ariyasinghe, Nethika R / Escopete, Sean / Joung, Sandy Y / Cheng, Susan / Parker, Sarah J / Fert-Bober, Justyna / Van Eyk, Jennifer E

Journal of proteome research

2023 Volume 22, Issue 2, Page(s) 471–481

Abstract: Recent surges in large-scale mass spectrometry (MS)-based proteomics studies demand a concurrent rise in methods to facilitate reliable and reproducible data analysis. Quantification of proteins in MS analysis can be affected by variations in technical ... ...

Abstract	Recent surges in large-scale mass spectrometry (MS)-based proteomics studies demand a concurrent rise in methods to facilitate reliable and reproducible data analysis. Quantification of proteins in MS analysis can be affected by variations in technical factors such as sample preparation and data acquisition conditions leading to batch effects, which adds to noise in the data set. This may in turn affect the effectiveness of any biological conclusions derived from the data. Here we present Batch-effect Identification, Representation, and Correction of Heterogeneous data (BIRCH), a workflow for analysis and correction of batch effect through an automated, versatile, and easy to use web-based tool with the goal of eliminating technical variation. BIRCH also supports diagnosis of the data to check for the presence of batch effects, feasibility of batch correction, and imputation to deal with missing values in the data set. To illustrate the relevance of the tool, we explore two case studies, including an iPSC-derived cell study and a Covid vaccine study to show different context-specific use cases. Ultimately this tool can be used as an extremely powerful approach for eliminating technical bias while retaining biological bias, toward understanding disease mechanisms and potential therapeutics.
MeSH term(s)	Humans ; Proteomics/methods ; Betula ; Workflow ; COVID-19 Vaccines ; COVID-19 ; Mass Spectrometry/methods
Chemical Substances	COVID-19 Vaccines
Language	English
Publishing date	2023-01-25
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2078618-9
ISSN	1535-3907 ; 1535-3893
ISSN (online)	1535-3907
ISSN	1535-3893
DOI	10.1021/acs.jproteome.2c00671
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Article: Peptidyl arginine deiminase inhibition alleviates angiotensin II-induced fibrosis.

Ijichi, Takeshi / Sundararaman, Niveda / Martin, Thomas G / Pandey, Rakhi / Koronyo, Etai / Kirk, Jonathan A / Marbán, Eduardo / Van Eyk, Jennifer E / Fert-Bober, Justyna

American journal of translational research

2023 Volume 15, Issue 7, Page(s) 4558–4572

Abstract: Objectives: The conversion of protein arginine residues to citrulline by calcium-dependent peptidyl arginine deiminases (PADs) has been implicated in the pathogenesis of several diseases, indicating that PADs are therapeutic targets. A recent study ... ...

Abstract	Objectives: The conversion of protein arginine residues to citrulline by calcium-dependent peptidyl arginine deiminases (PADs) has been implicated in the pathogenesis of several diseases, indicating that PADs are therapeutic targets. A recent study indicated that PAD4 regulates age-related organ fibrosis and dysfunction; however, the specific role of this PAD and its citrullination substrate remains unclear. We investigated whether pharmacological inhibition of PAD activity could affect the progression of fibrosis and restore heart function. Methods: Cardiac hypertrophy was induced by chronic infusion of angiotensin (Ang) II. After 2 weeks of AngII infusion, a PAD inhibitor (Cl-amidine hydrochloride) or vehicle (saline) was injected every other day for the next 14 days together with the continued administration of AngII for a total of up to 28 days. Cardiac fibrosis and remodeling were evaluated by quantitative heart tissue histology, echocardiography, and mass spectrometry. Results: A reverse AngII-induced effect was observed in PAD inhibitor-treated mice (n=6) compared with AngII vehicle-treated mice, as indicated by a significant reduction in the heart/body ratio (AngII: 6.51±0.8 mg/g vs. Cl-amidine: 5.27±0.6 mg/g), a reduction in fibrosis (AngII: 2.1-fold increased vs. Cl-amidine: 1.8-fold increased), and a reduction in left ventricular posterior wall diastole (LWVPd) (AngII: 1.1±0.04 vs. Cl-amidine: 0.78±0.02 mm). Label-free quantitative proteomics analysis of heart tissue indicated that proteins involved in fibrosis (e.g., periostin), cytoskeleton organization (e.g., transgelin), and remodeling (e.g., myosin light chain, carbonic anhydrase) were normalized by Cl-amidine treatment. Conclusion: Our findings demonstrate that pharmacological inhibition of PAD may be an effective strategy to attenuate cardiac fibrosis.
Language	English
Publishing date	2023-07-15
Publishing country	United States
Document type	Journal Article
ZDB-ID	2471058-1
ISSN	1943-8141
ISSN	1943-8141
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Article ; Online: Proteomics of citrullination in cardiovascular disease.

Fert-Bober, Justyna / Sokolove, Jeremy

Proteomics. Clinical applications

2014 Volume 8, Issue 7-8, Page(s) 522–533

Abstract: Citrullination is an enzymatic posttranslational modification (PTM), which has become a topic of recent research due to its involvement in various physiologic and pathologic processes. This review will focus primarily on the cardiovascular pathology ... ...

Abstract	Citrullination is an enzymatic posttranslational modification (PTM), which has become a topic of recent research due to its involvement in various physiologic and pathologic processes. This review will focus primarily on the cardiovascular pathology associated to date with citrullination, including myocardial citrullination as well as the potential role of citrullination in atherosclerosis as a driver inflammation, especially in patients with rheumatoid arthritis (RA). There is extensive citrullination within normal and RA myocardium as well as the atherosclerotic plaque; and increased levels of antibodies to citrullinated proteins have been associated with increased cardiovascular burden in patients with RA. Given robust citrullination in both RA as well as non-RA patients, there also exists the potential for protein citrullination to contribute to cardiovascular pathology in the general population. However, to investigate this possibility will require development of improved biochemical and proteomic tools for the study of protein citrullination. The remainder of this review will discuss current and developing methodologies to study protein citrullination and discuss their applicability for the analysis of complex samples. The ability to identify and quantify citrullinated protein is a key to understanding the role of this PTM. Methodologies and limitations of current technology for the identification of citrullination are discussed.
MeSH term(s)	Amino Acid Sequence ; Animals ; Cardiovascular Diseases/metabolism ; Citrulline/metabolism ; Humans ; Molecular Sequence Data ; Protein Processing, Post-Translational ; Proteomics/methods
Chemical Substances	Citrulline (29VT07BGDA)
Language	English
Publishing date	2014-08
Publishing country	Germany
Document type	Journal Article ; Review
ZDB-ID	2261788-7
ISSN	1862-8354 ; 1862-8346
ISSN (online)	1862-8354
ISSN	1862-8346
DOI	10.1002/prca.201400013
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Article: Identification of retinal tau oligomers, citrullinated tau, and other tau isoforms in early and advanced AD and relations to disease status.

bioRxiv : the preprint server for biology

2024

Abstract: Importance: This study identifies and quantifies diverse pathological tau isoforms in the retina of both early and advanced-stage Alzheimer's disease (AD) and determines their relationship with disease status.: Objective: A case-control study was ... ...

Abstract	Importance: This study identifies and quantifies diverse pathological tau isoforms in the retina of both early and advanced-stage Alzheimer's disease (AD) and determines their relationship with disease status. Objective: A case-control study was conducted to investigate the accumulation of retinal neurofibrillary tangles (NFTs), paired helical filament (PHF)-tau, oligomeric tau (oligo-tau), hyperphosphorylated tau (p-tau), and citrullinated tau (Cit-tau) in relation to the respective brain pathology and cognitive dysfunction in mild cognitively impaired (MCI) and AD dementia patients versus normal cognition (NC) controls. Design setting and participants: Eyes and brains from donors diagnosed with AD, MCI (due to AD), and NC were collected (n=75 in total), along with clinical and neuropathological data. Brain and retinal cross-sections-in predefined superior-temporal and inferior-temporal (ST/IT) subregions-were subjected to histopathology analysis or Nanostring GeoMx digital spatial profiling. Main outcomes and measure: Retinal burden of NFTs (pretangles and mature tangles), PHF-tau, p-tau, oligo-tau, and Cit-tau was assessed in MCI and AD versus NC retinas. Pairwise correlations revealed associations between retinal and brain parameters and cognitive status. Results: Increased retinal NFTs (1.8-fold, p=0.0494), PHF-tau (2.3-fold, p<0.0001), oligo-tau (9.1-fold, p<0.0001), CitR Conclusions and relevance: This study reveals increases in immature and mature retinal tau isoforms in MCI and AD patients, highlighting their relationship with brain pathology and cognition. The data provide strong incentive to further explore retinal tauopathy markers that may be useful for early detection and monitoring of AD staging through noninvasive retinal imaging.
Language	English
Publishing date	2024-02-16
Publishing country	United States
Document type	Preprint
DOI	10.1101/2024.02.13.579999
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