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Article ; Online: OA susceptibility in mice is partially mediated by the gut microbiome, is transferrable via microbiome transplantation and is associated with immunophenotype changes.

Prinz, Emmaline / Schlupp, Leoni / Dyson, Gabby / Barrett, Montana / Szymczak, Aleksander / Velasco, Cassandra / Izda, Vladislav / Dunn, Christopher M / Jeffries, Matlock A

Annals of the rheumatic diseases

2024 Volume 83, Issue 3, Page(s) 382–393

Abstract: Objectives: The Murphy Roths Large (MRL)/MpJ 'superhealer' mouse strain is protected from post-traumatic osteoarthritis (OA), although no studies have evaluated the microbiome in the context of this protection. This study characterised microbiome ... ...

Abstract	Objectives: The Murphy Roths Large (MRL)/MpJ 'superhealer' mouse strain is protected from post-traumatic osteoarthritis (OA), although no studies have evaluated the microbiome in the context of this protection. This study characterised microbiome differences between MRL and wild-type mice, evaluated microbiome transplantation and OA and investigated microbiome-associated immunophenotypes. Methods: Cecal material from mixed sex C57BL6/J (B6) or female MRL/MpJ (MRL) was transplanted into B6 and MRL mice, then OA was induced by disruption of the medial meniscus surgery (DMM). In other experiments, transplantation was performed after DMM and transplantation was performed into germ-free mice. Transplanted mice were bred through F2. OARSI, synovitis and osteophyte scores were determined blindly 8 weeks after DMM. 16S microbiome sequencing was performed and metagenomic function was imputed. Immunophenotypes were determined using mass cytometry. Results: MRL-into-B6 transplant prior to DMM showed reduced OA histopathology (OARSI score 70% lower transplant vs B6 control), synovitis (60% reduction) and osteophyte scores (30% reduction) 8 weeks after DMM. When performed 48 hours after DMM, MRL-into-B6 transplant improved OA outcomes but not when performed 1-2 weeks after DMM. Protection was seen in F1 (60% reduction) and F2 progeny (30% reduction). Several cecal microbiome clades were correlated with either better (eg, Conclusion: The gut microbiome is responsible in part for OA protection in MRL mice and is transferrable by microbiome transplantation. Transplantation induces resting systemic immunophenotyping changes that correlate with OA protection.
MeSH term(s)	Mice ; Female ; Animals ; Gastrointestinal Microbiome ; Osteophyte/pathology ; Immunophenotyping ; Microbiota ; Synovitis/pathology ; Disease Models, Animal ; Mice, Inbred C57BL ; Cartilage, Articular/pathology
Language	English
Publishing date	2024-02-15
Publishing country	England
Document type	Journal Article
ZDB-ID	7090-7
ISSN	1468-2060 ; 0003-4967
ISSN (online)	1468-2060
ISSN	0003-4967
DOI	10.1136/ard-2023-224907
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Article ; Online: COVID-19: A review of therapeutic strategies and vaccine candidates.

Izda, Vladislav / Jeffries, Matlock A / Sawalha, Amr H

Clinical immunology (Orlando, Fla.)

2020 Volume 222, Page(s) 108634

Abstract: The world is engulfed by one of the most widespread and significant public health crises in decades as COVID-19 has become among the leading causes of death internationally. The novel SARS-CoV-2 coronavirus which causes COVID-19 has unified the ... ...

Abstract	The world is engulfed by one of the most widespread and significant public health crises in decades as COVID-19 has become among the leading causes of death internationally. The novel SARS-CoV-2 coronavirus which causes COVID-19 has unified the scientific community in search of therapeutic and preventative solutions. The top priorities at the moment are twofold: first, to repurpose already-approved pharmacologic agents or develop novel therapies to reduce the morbidity and mortality associated with the ever-spreading virus. Secondly, the scientific and larger pharmaceutical community have been tasked with the development, testing, and production of a safe and effective vaccine as a longer-term solution to prevent further spread and recurrence throughout the populace. The purpose of this article is to review the most up-to-date published data regarding both the leading pharmacological therapies undergoing clinical trials and vaccine candidates in development to stem the threat of COVID-19.
MeSH term(s)	Adrenal Cortex Hormones/therapeutic use ; Antiviral Agents/therapeutic use ; COVID-19/prevention & control ; COVID-19 Vaccines/immunology ; Complement Inactivating Agents/therapeutic use ; Humans ; SARS-CoV-2 ; COVID-19 Drug Treatment
Chemical Substances	Adrenal Cortex Hormones ; Antiviral Agents ; COVID-19 Vaccines ; Complement Inactivating Agents
Keywords	covid19
Language	English
Publishing date	2020-11-17
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Review
ZDB-ID	1459903-x
ISSN	1521-7035 ; 1521-6616
ISSN (online)	1521-7035
ISSN	1521-6616
DOI	10.1016/j.clim.2020.108634
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Article ; Online: DNA methylation and noncoding RNA in OA: Recent findings and methodological advances.

Izda, Vladislav / Martin, Jake / Sturdy, Cassandra / Jeffries, Matlock A

Osteoarthritis and cartilage open

2021 Volume 3, Issue 4

Abstract: Introduction: Osteoarthritis (OA) is a chronic musculoskeletal disease characterized by progressive loss of joint function. Historically, it has been characterized as a disease caused by mechanical trauma, so-called 'wear and tear'. Over the past two ... ...

Abstract	Introduction: Osteoarthritis (OA) is a chronic musculoskeletal disease characterized by progressive loss of joint function. Historically, it has been characterized as a disease caused by mechanical trauma, so-called 'wear and tear'. Over the past two decades, it has come to be understood as a complex systemic disorder involving gene-environmental interactions. Epigenetic changes have been increasingly implicated. Recent improvements in microarray and next-generation sequencing (NGS) technologies have allowed for ever more complex evaluations of epigenetic aberrations associated with the development and progression of OA. Methods: A systematic review was conducted in the Pubmed database. We curated studies that presented the results of DNA methylation and noncoding RNA research in human OA and OA animal models since 1985. Results: Herein, we discuss recent findings and methodological advancements in OA epigenetics, including a discussion of DNA methylation, including microarray and NGS studies, and noncoding RNAs. Beyond cartilage, we also highlight studies in subchondral bone and peripheral blood mononuclear cells, which highlight widespread and potentially clinically important alterations in epigenetic patterns seen in OA patients. Finally, we discuss epigenetic editing approaches in the context of OA. Conclusions: Although a substantial body of literature has already been published in OA, much is still unknown. Future OA epigenetics studies will no doubt continue to broaden our understanding of underlying pathophysiology and perhaps offer novel diagnostics and/or treatments for human OA.
Language	English
Publishing date	2021-08-14
Publishing country	England
Document type	Journal Article
ISSN	2665-9131
ISSN (online)	2665-9131
DOI	10.1016/j.ocarto.2021.100208
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Article ; Online: Sex-Linked Discrepancies in C57BL6/J Mouse Osteoarthritis are Associated With the Gut Microbiome and are Transferrable by Microbiome Transplantation.

Schlupp, Leoni / Prinz, Emmaline / Dyson, Gabriella / Barrett, Montana / Izda, Vladislav / Dunn, Christopher M / Jeffries, Matlock A

Arthritis & rheumatology (Hoboken, N.J.)

2023 Volume 76, Issue 2, Page(s) 231–237

Abstract: Objective: Females have reduced osteoarthritis (OA) in surgical models. The objective of the current study was to evaluate a sex-linked gut microbiome in the pathogenesis of OA.: Methods: We induced OA via destabilization of the medial meniscus ... ...

Abstract	Objective: Females have reduced osteoarthritis (OA) in surgical models. The objective of the current study was to evaluate a sex-linked gut microbiome in the pathogenesis of OA. Methods: We induced OA via destabilization of the medial meniscus surgery in adult male and female C57BL6/J mice with and without opposite-sex microbiome transplantation. Eight weeks later, animals were euthanized, and OA severity, synovitis, and osteophyte scores were determined. Serum lipopolysaccharide was measured chromogenically, and serum cytokines were quantified via multiplex immunoassay. Cecal microbiome profiles were generated using 16S deep sequencing. Results: Males had worse OA histology (3.5x, P = 6 × 10 Conclusion: Sex-linked differences in the mouse gut microbiome are associated with OA outcomes, are reversible by opposite-sex microbiome transplantation, and are associated with serum cytokine changes.
MeSH term(s)	Male ; Female ; Mice ; Animals ; Gastrointestinal Microbiome ; Osteophyte/etiology ; Osteoarthritis/pathology ; Mice, Inbred C57BL ; Synovitis/pathology ; Cytokines ; Cartilage, Articular/pathology
Chemical Substances	Cytokines
Language	English
Publishing date	2023-12-12
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	2756371-6
ISSN	2326-5205 ; 2326-5191
ISSN (online)	2326-5205
ISSN	2326-5191
DOI	10.1002/art.42687
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Article ; Online: Murine cartilage microbial DNA deposition occurs rapidly following the introduction of a gut microbiome and changes with obesity, aging, and knee osteoarthritis.

Izda, Vladislav / Schlupp, Leoni / Prinz, Emmaline / Dyson, Gabby / Barrett, Montana / Dunn, Christopher M / Nguyen, Emily / Sturdy, Cassandra / Jeffries, Matlock A

GeroScience

2023 Volume 46, Issue 2, Page(s) 2317–2341

Abstract: Cartilage microbial DNA patterns have been recently characterized in osteoarthritis (OA). The objectives of this study were to evaluate the gut origins of cartilage microbial DNA, to characterize cartilage microbial changes with age, obesity, and OA in ... ...

Abstract	Cartilage microbial DNA patterns have been recently characterized in osteoarthritis (OA). The objectives of this study were to evaluate the gut origins of cartilage microbial DNA, to characterize cartilage microbial changes with age, obesity, and OA in mice, and correlate these to gut microbiome changes. We used 16S rRNA sequencing performed longitudinally on articular knee cartilage from germ-free (GF) mice following oral microbiome inoculation and cartilage and cecal samples from young and old wild-type mice with/without high-fat diet-induced obesity (HFD) and with/without OA induced by destabilization of the medial meniscus (DMM) to evaluate gut and cartilage microbiota. Microbial diversity was assessed, groups compared, and functional metagenomic profiles reconstructed. Findings were confirmed in an independent cohort by clade-specific qPCR. We found that cartilage microbial patterns developed at 48 h and later timepoints following oral microbiome inoculation of GF mice. Alpha diversity was increased in SPF mouse cartilage samples with age (P = 0.013), HFD (P = 5.6E-4), and OA (P = 0.029) but decreased in cecal samples with age (P = 0.014) and HFD (P = 1.5E-9). Numerous clades were altered with aging, HFD, and OA, including increases in Verrucomicrobia in both cartilage and cecal samples. Functional analysis suggested changes in dihydroorotase, glutamate-5-semialdehyde dehydrogenase, glutamate-5-kinase, and phosphoribosylamine-glycine ligase, in both cecum and cartilage, with aging, HFD, and OA. In conclusion, cartilage microbial DNA patterns develop rapidly after the introduction of a gut microbiome and change in concert with the gut microbiome during aging, HFD, and OA in mice. DMM-induced OA causes shifts in both cartilage and cecal microbiome patterns independent of other factors.
MeSH term(s)	Humans ; Animals ; Mice ; Osteoarthritis, Knee ; Gastrointestinal Microbiome ; RNA, Ribosomal, 16S/genetics ; Obesity ; Cartilage, Articular ; DNA ; Aging
Chemical Substances	RNA, Ribosomal, 16S ; DNA (9007-49-2)
Language	English
Publishing date	2023-11-09
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2886586-8
ISSN	2509-2723 ; 2509-2715
ISSN (online)	2509-2723
ISSN	2509-2715
DOI	10.1007/s11357-023-01004-z
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Article ; Online: COVID-19

Izda, Vladislav / Jeffries, Matlock A. / Sawalha, Amr H.

Clinical Immunology

A review of therapeutic strategies and vaccine candidates

2020 , Page(s) 108634

Keywords	Immunology ; Immunology and Allergy ; covid19
Language	English
Publisher	Elsevier BV
Publishing country	us
Document type	Article ; Online
ZDB-ID	1459903-x
ISSN	1521-7035 ; 1521-6616
ISSN (online)	1521-7035
ISSN	1521-6616
DOI	10.1016/j.clim.2020.108634
Database	BASE - Bielefeld Academic Search Engine (life sciences selection)

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Article ; Online: A Pilot Analysis of Genome-Wide DNA Methylation Patterns in Mouse Cartilage Reveals Overlapping Epigenetic Signatures of Aging and Osteoarthritis.

Izda, Vladislav / Dunn, Christopher M / Prinz, Emmaline / Schlupp, Leoni / Nguyen, Emily / Sturdy, Cassandra / Jeffries, Matlock A

ACR open rheumatology

2022 Volume 4, Issue 12, Page(s) 1004–1012

Abstract: Objective: Cartilage epigenetic changes are strongly associated with human osteoarthritis (OA). However, the influence of individual environmental OA risk factors on these epigenetic patterns has not been determined; herein we characterize cartilage DNA ...

Abstract	Objective: Cartilage epigenetic changes are strongly associated with human osteoarthritis (OA). However, the influence of individual environmental OA risk factors on these epigenetic patterns has not been determined; herein we characterize cartilage DNA methylation patterns associated with aging and OA in a mouse model. Methods: Murine knee cartilage DNA was extracted from healthy young (16-week, n = 6), old (82-week, n = 6), and young 4-week post-destabilization of the medial meniscus (DMM) OA (n = 6) C57BL6/J mice. Genome-wide DNA methylation patterns were determined via Illumina BeadChip. Gene set enrichment analysis was performed by Ingenuity Pathway Analysis. The top seven most differentially methylated positions (DMPs) were confirmed by pyrosequencing in an independent animal set. Results were compared to previously published human OA methylation data. Results: Aging was associated with 20,940 DMPs, whereas OA was associated with 761 DMPs. Merging these two conditions revealed 279 shared DMPs. All demonstrated similar directionality and magnitude of change (Δβ 1.0% ± 0.2%, mean methylation change ± SEM). Shared DMPs were enriched in OA-associated pathways, including RhoA signaling (P = 1.57 × 10 Conclusion: Aging and early OA following DMM surgery induce similar DNA methylation changes within a murine OA model, suggesting that aging may induce pro-OA epigenetic "poising" within articular cartilage. Future research should focus on confirming and expanding these findings to other environmental OA risk factors, including obesity, as well as determining late OA changes in mice.
Language	English
Publishing date	2022-10-17
Publishing country	United States
Document type	Journal Article
ISSN	2578-5745
ISSN (online)	2578-5745
DOI	10.1002/acr2.11506
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Article: COVID-19: A review of therapeutic strategies and vaccine candidates

Izda, Vladislav Jeffries Matlock A. / Sawalha, Amr H.

Clinical Immunology

Abstract: The world is engulfed by one of the most widespread and significant public health crises in decades as COVID-19 has become among the leading causes of death internationally The novel SARS-CoV-2 coronavirus which causes COVID-19 has unified the scientific ...

Abstract	The world is engulfed by one of the most widespread and significant public health crises in decades as COVID-19 has become among the leading causes of death internationally The novel SARS-CoV-2 coronavirus which causes COVID-19 has unified the scientific community in search of therapeutic and preventative solutions The top priorities at the moment are twofold: first, to repurpose already-approved pharmacologic agents or develop novel therapies to reduce the morbidity and mortality associated with the ever-spreading virus Secondly, the scientific and larger pharmaceutical community have been tasked with the development, testing, and production of a safe and effective vaccine as a longer-term solution to prevent further spread and recurrence throughout the populace The purpose of this article is to review the most up-to-date published data regarding both the leading pharmacological therapies undergoing clinical trials and vaccine candidates in development to stem the threat of COVID-19
Keywords	covid19
Publisher	WHO
Document type	Article
Note	WHO #Covidence: #927708
Database	COVID19

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Article ; Online: Ear wound healing in MRL/MpJ mice is associated with gut microbiome composition and is transferable to non-healer mice via microbiome transplantation.

Velasco, Cassandra / Dunn, Christopher / Sturdy, Cassandra / Izda, Vladislav / Martin, Jake / Rivas, Alexander / McNaughton, Jeffrey / Jeffries, Matlock A

PloS one

2021 Volume 16, Issue 7, Page(s) e0248322

Abstract: Objective: Adult elastic cartilage has limited repair capacity. MRL/MpJ (MRL) mice, by contrast, are capable of spontaneously healing ear punctures. This study was undertaken to characterize microbiome differences between healer and non-healer mice and ... ...

Abstract	Objective: Adult elastic cartilage has limited repair capacity. MRL/MpJ (MRL) mice, by contrast, are capable of spontaneously healing ear punctures. This study was undertaken to characterize microbiome differences between healer and non-healer mice and to evaluate whether this healing phenotype can be transferred via gut microbiome transplantation. Methods: We orally transplanted C57BL/6J (B6) mice with MRL/MpJ cecal contents at weaning and as adults (n = 57) and measured ear hole closure 4 weeks after a 2.0mm punch and compared to vehicle-transplanted MRL and B6 (n = 25) and B6-transplanted MRL (n = 20) mice. Sex effects, timing of transplant relative to earpunch, and transgenerational heritability were evaluated. In a subset (n = 58), cecal microbiomes were profiled by 16S sequencing and compared to ear hole closure. Microbial metagenomes were imputed using PICRUSt. Results: Transplantation of B6 mice with MRL microbiota, either in weanlings or adults, improved ear hole closure. B6-vehicle mice healed ear hole punches poorly (0.25±0.03mm, mm ear hole healing 4 weeks after a 2mm ear hole punch [2.0mm-final ear hole size], mean±SEM), whereas MRL-vehicle mice healed well (1.4±0.1mm). MRL-transplanted B6 mice healed roughly three times as well as B6-vehicle mice, and half as well as MRL-vehicle mice (0.74±0.05mm, P = 6.9E-10 vs. B6-vehicle, P = 5.2E-12 vs. MRL-vehicle). Transplantation of MRL mice with B6 cecal material did not reduce MRL healing (B6-transplanted MRL 1.3±0.1 vs. MRL-vehicle 1.4±0.1, p = 0.36). Transplantation prior to ear punch was associated with the greatest ear hole closure. Offspring of transplanted mice healed significantly better than non-transplanted control mice (offspring:0.63±0.03mm, mean±SEM vs. B6-vehicle control:0.25±0.03mm, n = 39 offspring, P = 4.6E-11). Several microbiome clades were correlated with healing, including Firmicutes (R = 0.84, P = 8.0E-7), Lactobacillales (R = 0.65, P = 1.1E-3), and Verrucomicrobia (R = -0.80, P = 9.2E-6). Females of all groups tended to heal better than males (B6-vehicle P = 0.059, MRL-transplanted B6 P = 0.096, offspring of MRL-transplanted B6 P = 0.0038, B6-transplanted MRL P = 1.6E-6, MRL-vehicle P = 0.0031). Many clades characteristic of female mouse cecal microbiota vs. males were the same as clades characteristic of MRL and MRL-transplanted B6 mice vs. B6 controls, including including increases in Clostridia and reductions in Verrucomicrobia in female mice. Conclusion: In this study, we found an association between the microbiome and tissue regeneration in MRL mice and demonstrate that this trait can be transferred to non-healer mice via microbiome transplantation. We identified several microbiome clades associated with healing.
MeSH term(s)	Animals ; Female ; Gastrointestinal Microbiome ; Male ; Mice ; Wound Healing
Language	English
Publishing date	2021-07-20
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Research Support, U.S. Gov't, Non-P.H.S.
ISSN	1932-6203
ISSN (online)	1932-6203
DOI	10.1371/journal.pone.0248322
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Article ; Online: Peripheral Blood DNA Methylation-Based Machine Learning Models for Prediction of Knee Osteoarthritis Progression: Biologic Specimens and Data From the Osteoarthritis Initiative and Johnston County Osteoarthritis Project.

Dunn, Christopher M / Sturdy, Cassandra / Velasco, Cassandra / Schlupp, Leoni / Prinz, Emmaline / Izda, Vladislav / Arbeeva, Liubov / Golightly, Yvonne M / Nelson, Amanda E / Jeffries, Matlock A

Arthritis & rheumatology (Hoboken, N.J.)

2022 Volume 75, Issue 1, Page(s) 28–40

Abstract: Objective: The lack of accurate biomarkers to predict knee osteoarthritis (OA) progression is a key unmet need in OA clinical research. The objective of this study was to develop baseline peripheral blood epigenetic biomarker models to predict knee OA ... ...

Abstract	Objective: The lack of accurate biomarkers to predict knee osteoarthritis (OA) progression is a key unmet need in OA clinical research. The objective of this study was to develop baseline peripheral blood epigenetic biomarker models to predict knee OA progression. Methods: Genome-wide buffy coat DNA methylation patterns from 554 individuals from the Osteoarthritis Biomarkers Consortium (OABC) were determined using Illumina Infinium MethylationEPIC 850K arrays. Data were divided into model development and validation sets, and machine learning models were trained to classify future OA progression by knee pain, radiographic imaging, knee pain plus radiographic imaging, and any progression (pain, radiographic, or both). Parsimonious models using the top 13 CpG sites most frequently selected during development were tested on independent samples from participants in the Johnston County Osteoarthritis (JoCo OA) Project (n = 128) and a previously published Osteoarthritis Initiative (OAI) data set (n = 55). Results: Full models accurately classified future radiographic-only progression (mean ± SEM accuracy 87 ± 0.8%, area under the curve [AUC] 0.94 ± 0.004), pain-only progression (accuracy 89 ± 0.9%, AUC 0.97 ± 0.004), pain plus radiographic progression (accuracy 72 ± 0.7%, AUC 0.79 ± 0.006), and any progression (accuracy 78 ± 0.4%, AUC 0.86 ± 0.004). Pain-only and radiographic-only progressors were not distinguishable (mean ± SEM accuracy 58 ± 1%, AUC 0.62 ± 0.001). Parsimonious models showed similar performance and accurately classified future radiographic progressors in the OABC cohort and in both validation cohorts (mean ± SEM accuracy 80 ± 0.3%, AUC 0.88 ± 0.003 [using JoCo OA Project data], accuracy 80 ± 0.8%, AUC 0.89 ± 0.002 [using previous OAI data]). Conclusion: Our data suggest that pain and structural progression share similar early systemic immune epigenotypes. Further studies should focus on evaluating the pathophysiologic consequences of differential DNA methylation and peripheral blood cell epigenotypes in individuals with knee OA.
MeSH term(s)	Humans ; Osteoarthritis, Knee/diagnostic imaging ; Osteoarthritis, Knee/genetics ; DNA Methylation ; Knee Joint ; Pain/etiology ; Biomarkers ; Biological Products ; Disease Progression
Chemical Substances	Biomarkers ; Biological Products
Language	English
Publishing date	2022-11-21
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	2756371-6
ISSN	2326-5205 ; 2326-5191
ISSN (online)	2326-5205
ISSN	2326-5191
DOI	10.1002/art.42316
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