Sex-Specific Differences in Extracellular Vesicle Protein Cargo in Synovial Fluid of Patients with Osteoarthritis
Women are at a significantly higher risk of developing osteoarthritis (OA) compared to males. The pathogenesis of osteoarthritis (OA) in women is poorly understood. Extracellular vesicles (EVs) have been shown to play an essential role in numerous signaling processes during the pathogenesis of age-r...
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Published in | Life (Basel, Switzerland) Vol. 10; no. 12; p. 337 |
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Main Authors | , , , , , , , , , , , |
Format | Journal Article |
Language | English |
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10.12.2020
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Abstract | Women are at a significantly higher risk of developing osteoarthritis (OA) compared to males. The pathogenesis of osteoarthritis (OA) in women is poorly understood. Extracellular vesicles (EVs) have been shown to play an essential role in numerous signaling processes during the pathogenesis of age-related diseases via paracrine signaling. Molecular profiling of the synovial fluid-derived EVs cargo in women may help in the discovery of novel biomarkers and therapeutics for the treatment of OA in women. Previously, we reported that synovial fluid-derived EV miRNA cargo differs in a sex-specific manner. This study aims to characterize synovial fluid-derived EV protein cargo in OA patients. Our data showed sex-specific EVs protein content in OA. We found haptoglobin, orosomucoid, and ceruloplasmin significantly up-regulated, whereas apolipoprotein down-regulated in female OA EVs. In males, we discovered β-2-glycoprotein, and complement component 5 proteins significantly up-regulated and Spt-Ada-Gcn5 acetyltransferase (SAGA)-associated factor 29 down-regulated in male OA EVs. Database for Annotation, Visualization, and Integrated Discovery (DAVID) and QuickGO analysis revealed OA-specific protein involvement in several biological, molecular, and cellular pathways, specifically in inflammatory processes. In conclusion, synovial fluid EV protein content is altered in a sex-specific manner with OA, explaining the increased prevalence and severity of OA in women. |
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AbstractList | Women are at a significantly higher risk of developing osteoarthritis (OA) compared to males. The pathogenesis of osteoarthritis (OA) in women is poorly understood. Extracellular vesicles (EVs) have been shown to play an essential role in numerous signaling processes during the pathogenesis of age-related diseases via paracrine signaling. Molecular profiling of the synovial fluid-derived EVs cargo in women may help in the discovery of novel biomarkers and therapeutics for the treatment of OA in women. Previously, we reported that synovial fluid-derived EV miRNA cargo differs in a sex-specific manner. This study aims to characterize synovial fluid-derived EV protein cargo in OA patients. Our data showed sex-specific EVs protein content in OA. We found haptoglobin, orosomucoid, and ceruloplasmin significantly up-regulated, whereas apolipoprotein down-regulated in female OA EVs. In males, we discovered β-2-glycoprotein, and complement component 5 proteins significantly up-regulated and Spt-Ada-Gcn5 acetyltransferase (SAGA)-associated factor 29 down-regulated in male OA EVs. Database for Annotation, Visualization, and Integrated Discovery (DAVID) and QuickGO analysis revealed OA-specific protein involvement in several biological, molecular, and cellular pathways, specifically in inflammatory processes. In conclusion, synovial fluid EV protein content is altered in a sex-specific manner with OA, explaining the increased prevalence and severity of OA in women. |
Author | Kolhe, Ravindra Mondal, Ashis K Fulzele, Sadanand Isales, Carlos M Ghilzai, Umar Hunter, Monte Hamrick, Mark W Owens, Virgenal Liu, Yutao Sharma, Ashok Lee, Tae Jin Zhi, Wenbo |
AuthorAffiliation | 7 Institute of Healthy Aging, Augusta University, Augusta, GA 30912, USA 3 Department of Orthopaedic Surgery, Carolinas Medical Center, Charlotte, NC 28203, USA 5 Cell Biology and Anatomy, Augusta University, Augusta, GA 30912, USA; YUTLIU@augusta.edu 4 Center for Biotechnology and Genomic Medicine, Augusta University, Augusta, GA 30912, USA; ASSHARMA@augusta.edu (A.S.); TALEE@augusta.edu (T.J.L.); WZHI@augusta.edu (W.Z.) 1 Department of Pathology, Augusta University, Augusta, GA 30912, USA; rkolhe@augusta.edu (R.K.); AMONDAL@augusta.edu (A.K.M.); cisales@augusta.edu (C.M.I.); mhamrick@augusta.edu (M.W.H.) 6 Department of Medicine, Augusta University, Augusta, GA 30912, USA 2 Department of Orthopaedic Surgery, Augusta University, Augusta, GA 30912, USA; virgenal.owens@atriumhealth.org (V.O.); UGHILZAI@augusta.edu (U.G.); MOHUNTER@augusta.edu (M.H.) |
AuthorAffiliation_xml | – name: 3 Department of Orthopaedic Surgery, Carolinas Medical Center, Charlotte, NC 28203, USA – name: 7 Institute of Healthy Aging, Augusta University, Augusta, GA 30912, USA – name: 4 Center for Biotechnology and Genomic Medicine, Augusta University, Augusta, GA 30912, USA; ASSHARMA@augusta.edu (A.S.); TALEE@augusta.edu (T.J.L.); WZHI@augusta.edu (W.Z.) – name: 6 Department of Medicine, Augusta University, Augusta, GA 30912, USA – name: 2 Department of Orthopaedic Surgery, Augusta University, Augusta, GA 30912, USA; virgenal.owens@atriumhealth.org (V.O.); UGHILZAI@augusta.edu (U.G.); MOHUNTER@augusta.edu (M.H.) – name: 5 Cell Biology and Anatomy, Augusta University, Augusta, GA 30912, USA; YUTLIU@augusta.edu – name: 1 Department of Pathology, Augusta University, Augusta, GA 30912, USA; rkolhe@augusta.edu (R.K.); AMONDAL@augusta.edu (A.K.M.); cisales@augusta.edu (C.M.I.); mhamrick@augusta.edu (M.W.H.) |
Author_xml | – sequence: 1 givenname: Ravindra orcidid: 0000-0002-8283-2403 surname: Kolhe fullname: Kolhe, Ravindra organization: Department of Pathology, Augusta University, Augusta, GA 30912, USA – sequence: 2 givenname: Virgenal surname: Owens fullname: Owens, Virgenal organization: Department of Orthopaedic Surgery, Carolinas Medical Center, Charlotte, NC 28203, USA – sequence: 3 givenname: Ashok orcidid: 0000-0001-9597-4374 surname: Sharma fullname: Sharma, Ashok organization: Center for Biotechnology and Genomic Medicine, Augusta University, Augusta, GA 30912, USA – sequence: 4 givenname: Tae Jin surname: Lee fullname: Lee, Tae Jin organization: Center for Biotechnology and Genomic Medicine, Augusta University, Augusta, GA 30912, USA – sequence: 5 givenname: Wenbo surname: Zhi fullname: Zhi, Wenbo organization: Center for Biotechnology and Genomic Medicine, Augusta University, Augusta, GA 30912, USA – sequence: 6 givenname: Umar orcidid: 0000-0003-2207-074X surname: Ghilzai fullname: Ghilzai, Umar organization: Department of Orthopaedic Surgery, Augusta University, Augusta, GA 30912, USA – sequence: 7 givenname: Ashis K surname: Mondal fullname: Mondal, Ashis K organization: Department of Pathology, Augusta University, Augusta, GA 30912, USA – sequence: 8 givenname: Yutao surname: Liu fullname: Liu, Yutao organization: Cell Biology and Anatomy, Augusta University, Augusta, GA 30912, USA – sequence: 9 givenname: Carlos M orcidid: 0000-0002-4480-3484 surname: Isales fullname: Isales, Carlos M organization: Institute of Healthy Aging, Augusta University, Augusta, GA 30912, USA – sequence: 10 givenname: Mark W surname: Hamrick fullname: Hamrick, Mark W organization: Institute of Healthy Aging, Augusta University, Augusta, GA 30912, USA – sequence: 11 givenname: Monte surname: Hunter fullname: Hunter, Monte organization: Department of Orthopaedic Surgery, Augusta University, Augusta, GA 30912, USA – sequence: 12 givenname: Sadanand surname: Fulzele fullname: Fulzele, Sadanand organization: Institute of Healthy Aging, Augusta University, Augusta, GA 30912, USA |
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Cites_doi | 10.1097/GME.0000000000001280 10.1016/j.cger.2014.08.019 10.1159/000489739 10.1371/journal.pone.0057645 10.1186/ar4679 10.1186/s12891-016-1059-y 10.1515/bmc-2019-0014 10.1371/journal.pone.0005606 10.1167/iovs.17-23434 10.1016/j.eurger.2017.07.008 10.1038/s41598-017-01386-z 10.1111/imm.12125 10.1074/jbc.M112.353771 10.1155/2017/4814987 10.1097/01.NAJ.0000412646.80054.21 10.3233/BMR-181294 10.3390/ijms18030538 10.1186/ar1706 10.1007/s00264-018-4093-6 10.1002/hep.29732 10.1177/2053369118757537 10.1016/j.clnu.2019.01.019 10.1055/s-0038-1660791 10.5435/00124635-200700001-00007 10.1093/bioinformatics/btp536 10.1186/1471-2407-14-44 10.1046/j.1365-2613.2003.00336.x 10.3109/1354750X.2016.1171907 10.1038/srep23978 10.1007/s12178-013-9164-0 10.1007/s12020-010-9392-7 10.1371/journal.pone.0041387 10.18632/aging.101874 10.1016/j.jprot.2016.11.012 10.1189/jlb.0208100 10.1038/emm.2017.307 10.1186/ar2791 10.3390/nu12020574 10.1038/s41598-017-01905-y 10.1007/s12031-020-01526-7 10.1093/nar/gkn923 10.1373/clinchem.2005.055442 10.1186/s13287-017-0632-0 10.1038/nprot.2008.211 10.1007/s13224-019-01213-7 10.1002/art.23176 10.1007/s13105-015-0389-9 10.1371/journal.pone.0170628 10.1093/molehr/7.8.747 10.1016/j.joca.2011.10.003 |
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References | Sharma (ref_24) 2018; 59 Wang (ref_20) 2017; 8 ref_12 Largo (ref_49) 2009; 11 Kato (ref_54) 2014; 16 Zhao (ref_53) 2018; 42 Menashe (ref_6) 2012; 20 ref_16 Huang (ref_27) 2009; 37 Munjal (ref_29) 2019; 10 Berkova (ref_36) 2001; 7 Magid (ref_43) 2005; 51 Liao (ref_13) 2015; 8 Lawrence (ref_2) 2008; 58 Binns (ref_28) 2009; 25 Luo (ref_45) 2015; 71 Stagno (ref_10) 2020; 33 Iolascon (ref_7) 2017; 8 ref_22 Hame (ref_3) 2013; 6 Smeets (ref_39) 2003; 84 Kolhe (ref_15) 2017; 7 Eitan (ref_31) 2017; 7 Park (ref_42) 2013; 140 Rider (ref_23) 2016; 12 Dasari (ref_25) 2020; 70 ref_35 Damiani (ref_9) 2020; 32 Komori (ref_47) 2012; 287 ref_30 Jung (ref_50) 2019; 26 Piva (ref_5) 2015; 31 Mabey (ref_14) 2016; 21 Withrow (ref_17) 2016; 18 Tang (ref_37) 2020; 39 Saha (ref_33) 2018; 67 Huntoon (ref_38) 2008; 84 Sammour (ref_34) 2010; 38 Fulzele (ref_32) 2019; 11 Domenis (ref_18) 2017; 2017 ref_46 Calamia (ref_41) 2017; 152 Khadilkar (ref_52) 2019; 69 ref_44 Berckmans (ref_19) 2005; 7 ref_40 Santilli (ref_11) 2018; 6 Sun (ref_48) 2018; 50 Watt (ref_51) 2018; 24 (ref_4) 2007; 15 Huang (ref_26) 2009; 4 Murphy (ref_1) 2012; 112 ref_8 Silvestre (ref_21) 2018; 47 |
References_xml | – volume: 26 start-page: 598 year: 2019 ident: ref_50 article-title: Knee osteoarthritis and menopausal hormone therapy in postmenopausal women publication-title: Menopause doi: 10.1097/GME.0000000000001280 contributor: fullname: Jung – volume: 31 start-page: 67 year: 2015 ident: ref_5 article-title: Links between osteoarthritis and diabetes: Implications for management from a physical activity perspective publication-title: Clin. Geriatr. Med. doi: 10.1016/j.cger.2014.08.019 contributor: fullname: Piva – volume: 47 start-page: 11 year: 2018 ident: ref_21 article-title: Microvesicles from Human Adipose Tissue-Derived Mesenchymal Stem Cells as a New Protective Strategy in Osteoarthritic Chondrocytes publication-title: Cell. Physiol. Biochem. doi: 10.1159/000489739 contributor: fullname: Silvestre – volume: 32 start-page: 327 year: 2020 ident: ref_9 article-title: Trade-Offs with rehabilitation Effectiveness (REs) and Efficiency (REy) in a sample of Italian disabled persons in a in post-acuity rehabilitation unit publication-title: Ann. Ig. contributor: fullname: Damiani – ident: ref_46 doi: 10.1371/journal.pone.0057645 – volume: 16 start-page: R163 year: 2014 ident: ref_54 article-title: Exosomes from IL-1β stimulated synovial fibroblasts induce osteoarthritic changes in articular chondrocytes publication-title: Arthritis Res. Ther. doi: 10.1186/ar4679 contributor: fullname: Kato – ident: ref_40 doi: 10.1186/s12891-016-1059-y – volume: 10 start-page: 111 year: 2019 ident: ref_29 article-title: Advances in Molecular biomarker for early diagnosis of Osteoarthritis publication-title: Biomol. Concepts doi: 10.1515/bmc-2019-0014 contributor: fullname: Munjal – ident: ref_35 doi: 10.1371/journal.pone.0005606 – volume: 59 start-page: 2635 year: 2018 ident: ref_24 article-title: Proteomic Alterations in Aqueous Humor From Patients With Primary Open Angle Glaucoma publication-title: Investig. Opthalmol. Vis. Sci. doi: 10.1167/iovs.17-23434 contributor: fullname: Sharma – volume: 8 start-page: 383 year: 2017 ident: ref_7 article-title: Early osteoarthritis: How to define, diagnose, and manage. A systematic review publication-title: Eur. Geriatr. Med. doi: 10.1016/j.eurger.2017.07.008 contributor: fullname: Iolascon – volume: 7 start-page: 1 year: 2017 ident: ref_31 article-title: Age-Related Changes in Plasma Extracellular Vesicle Characteristics and Internalization by Leukocytes publication-title: Sci. Rep. doi: 10.1038/s41598-017-01386-z contributor: fullname: Eitan – volume: 140 start-page: 133 year: 2013 ident: ref_42 article-title: Identification of a specific haptoglobin C-terminal fragment in arthritic synovial fluid and its effect on interleukin-6 expression publication-title: Immunology doi: 10.1111/imm.12125 contributor: fullname: Park – volume: 287 start-page: 30688 year: 2012 ident: ref_47 article-title: α1-Acid Glycoprotein Up-regulates CD163 via TLR4/CD14 Protein Pathway publication-title: J. Biol. Chem. doi: 10.1074/jbc.M112.353771 contributor: fullname: Komori – volume: 2017 start-page: 4814987 year: 2017 ident: ref_18 article-title: Characterization of the pro-inflammatory profile of synovial fluid-derived exosomes of patients with osteoarthritis publication-title: Mediat. Inflamm. doi: 10.1155/2017/4814987 contributor: fullname: Domenis – volume: 112 start-page: 13 year: 2012 ident: ref_1 article-title: The impact of osteoarthritis in the United States: A population-health perspective publication-title: Am. J. Nurs. doi: 10.1097/01.NAJ.0000412646.80054.21 contributor: fullname: Murphy – volume: 33 start-page: 347 year: 2020 ident: ref_10 article-title: Long-term effects of intra-articular oxygen-ozone therapy versus hyaluronic acid in older people affected by knee osteoarthritis: A randomized single-blind extension study publication-title: J. Back Musculoskelet Rehabil. doi: 10.3233/BMR-181294 contributor: fullname: Stagno – ident: ref_16 doi: 10.3390/ijms18030538 – volume: 7 start-page: R536 year: 2005 ident: ref_19 article-title: Synovial microparticles from arthritic patients modulate chemokine and cytokine release by synoviocytes publication-title: Arthritis Res. Ther. doi: 10.1186/ar1706 contributor: fullname: Berckmans – volume: 42 start-page: 2865 year: 2018 ident: ref_53 article-title: Synovial fluid-derived exosomal lncRNA PCGEM1 as biomarker for the different stages of osteoarthritis publication-title: Int. Orthop. doi: 10.1007/s00264-018-4093-6 contributor: fullname: Zhao – volume: 67 start-page: 1986 year: 2018 ident: ref_33 article-title: Extracellular vesicles from mice with alcoholic liver disease carry a distinct protein cargo and induce macrophage activation through heat shock protein 90 publication-title: Hepatology doi: 10.1002/hep.29732 contributor: fullname: Saha – volume: 24 start-page: 34 year: 2018 ident: ref_51 article-title: Musculoskeletal pain and menopause publication-title: Post Reprod. Health doi: 10.1177/2053369118757537 contributor: fullname: Watt – volume: 39 start-page: 225 year: 2020 ident: ref_37 article-title: Haptoglobin phenotype influences the effectiveness of diet-induced weight loss in middle-age abdominally obese women with metabolic abnormalities publication-title: Clin. Nutr. doi: 10.1016/j.clnu.2019.01.019 contributor: fullname: Tang – volume: 6 start-page: 131 year: 2018 ident: ref_11 article-title: Comment on Early Efficacy of Intra-Articular HYADD® 4 (Hymovis®) Injections for Symptomatic Knee Osteoarthritis publication-title: Joints doi: 10.1055/s-0038-1660791 contributor: fullname: Santilli – volume: 15 start-page: S22 year: 2007 ident: ref_4 article-title: Sex Differences in Osteoarthritis of the Hip and Knee publication-title: J. Am. Acad. Orthop. Surg. doi: 10.5435/00124635-200700001-00007 – volume: 25 start-page: 3045 year: 2009 ident: ref_28 article-title: QuickGO: A web-based tool for Gene Ontology searching publication-title: Bioinformatics doi: 10.1093/bioinformatics/btp536 contributor: fullname: Binns – ident: ref_30 doi: 10.1186/1471-2407-14-44 – volume: 84 start-page: 69 year: 2003 ident: ref_39 article-title: The acute phase protein haptoglobin is locally expressed in arthritic and oncological tissues publication-title: Int. J. Exp. Pathol. doi: 10.1046/j.1365-2613.2003.00336.x contributor: fullname: Smeets – volume: 21 start-page: 639 year: 2016 ident: ref_14 article-title: Plasma and synovial fluid inflammatory cytokine profiles in primary knee osteoarthritis publication-title: Biomarkers doi: 10.3109/1354750X.2016.1171907 contributor: fullname: Mabey – volume: 12 start-page: 23978 year: 2016 ident: ref_23 article-title: ExtraPEG: A Polyethylene Glycol-Based Method for Enrichment of Extracellular Vesicles publication-title: Sci. Rep. doi: 10.1038/srep23978 contributor: fullname: Rider – volume: 6 start-page: 182 year: 2013 ident: ref_3 article-title: Knee osteoarthritis in women publication-title: Curr. Rev. Musculoskelet. Med. doi: 10.1007/s12178-013-9164-0 contributor: fullname: Hame – volume: 38 start-page: 303 year: 2010 ident: ref_34 article-title: Haptoglobin phenotype in women with preeclampsia publication-title: Endocrine doi: 10.1007/s12020-010-9392-7 contributor: fullname: Sammour – ident: ref_44 doi: 10.1371/journal.pone.0041387 – volume: 8 start-page: 9975 year: 2015 ident: ref_13 article-title: Proteomic analysis of synovial fluid as an analytical tool to detect candidate biomarkers for knee osteoarthritis publication-title: Int. J. Clin. Exp. Pathol. contributor: fullname: Liao – volume: 11 start-page: 1791 year: 2019 ident: ref_32 article-title: Muscle-derived miR-34a increases with age in circulating extracellular vesicles and induces senescence of bone marrow stem cells publication-title: Aging doi: 10.18632/aging.101874 contributor: fullname: Fulzele – volume: 152 start-page: 216 year: 2017 ident: ref_41 article-title: Multiplexed mass spectrometry monitoring of biomarker candidates for osteoarthritis publication-title: J. Proteom. doi: 10.1016/j.jprot.2016.11.012 contributor: fullname: Calamia – volume: 84 start-page: 170 year: 2008 ident: ref_38 article-title: The acute phase protein haptoglobin regulates host immunity publication-title: J. Leukoc. Biol. doi: 10.1189/jlb.0208100 contributor: fullname: Huntoon – volume: 50 start-page: e463 year: 2018 ident: ref_48 article-title: Estrogen weakens muscle endurance via estrogen receptor-p38 MAPK-mediated orosomucoid (ORM) suppression publication-title: Exp. Mol. Med. doi: 10.1038/emm.2017.307 contributor: fullname: Sun – volume: 11 start-page: 241 year: 2009 ident: ref_49 article-title: Osteoarthritis associated with estrogen deficiency publication-title: Arthritis Res. Ther. doi: 10.1186/ar2791 contributor: fullname: Largo – ident: ref_8 doi: 10.3390/nu12020574 – volume: 7 start-page: 1 year: 2017 ident: ref_15 article-title: Gender-specific differential expression of exosomal miRNA in synovial fluid of patients with osteoarthritis publication-title: Sci. Rep. doi: 10.1038/s41598-017-01905-y contributor: fullname: Kolhe – volume: 70 start-page: 1186 year: 2020 ident: ref_25 article-title: A Combined Proteomics and Bioinformatics Approach Reveals Novel Signaling Pathways and Molecular Targets After Intracerebral Hemorrhage publication-title: J. Mol. Neurosci. doi: 10.1007/s12031-020-01526-7 contributor: fullname: Dasari – ident: ref_12 – volume: 37 start-page: 1 year: 2009 ident: ref_27 article-title: Bioinformatics enrichment tools: Paths toward the comprehensive functional analysis of large gene lists publication-title: Nucleic Acids Res. doi: 10.1093/nar/gkn923 contributor: fullname: Huang – volume: 51 start-page: 2052 year: 2005 ident: ref_43 article-title: Monitoring Urinary Orosomucoid in Acute Inflammation: Observations on Urinary Excretion of Orosomucoid, Albumin, α1-Microglobulin, and IgG publication-title: Clin. Chem. doi: 10.1373/clinchem.2005.055442 contributor: fullname: Magid – volume: 8 start-page: 1 year: 2017 ident: ref_20 article-title: Exosomes from embryonic mesenchymal stem cells alleviate osteoarthritis through balancing synthesis and degradation of cartilage extracellular matrix publication-title: Stem Cell Res. Ther. doi: 10.1186/s13287-017-0632-0 contributor: fullname: Wang – volume: 4 start-page: 44 year: 2009 ident: ref_26 article-title: Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources publication-title: Nat. Protoc. doi: 10.1038/nprot.2008.211 contributor: fullname: Huang – volume: 69 start-page: 99 year: 2019 ident: ref_52 article-title: Musculoskeletal Disorders and Menopause publication-title: J. Obstet. Gynecol. India doi: 10.1007/s13224-019-01213-7 contributor: fullname: Khadilkar – volume: 58 start-page: 26 year: 2008 ident: ref_2 article-title: Estimates of the prevalence of arthritis and other rheumatic conditions in the United States: Part II publication-title: Arthritis Rheum. doi: 10.1002/art.23176 contributor: fullname: Lawrence – volume: 71 start-page: 329 year: 2015 ident: ref_45 article-title: Orosomucoid, an acute response protein with multiple modulating activities publication-title: J. Physiol. Biochem. doi: 10.1007/s13105-015-0389-9 contributor: fullname: Luo – ident: ref_22 doi: 10.1371/journal.pone.0170628 – volume: 18 start-page: 1 year: 2016 ident: ref_17 article-title: Extracellular vesicles in the pathogenesis of rheumatoid arthritis and osteoarthritis publication-title: Arthritis Res. contributor: fullname: Withrow – volume: 7 start-page: 747 year: 2001 ident: ref_36 article-title: Haptoglobin is present in human endometrium and shows elevated levels in the decidua during pregnancy publication-title: Mol. Hum. Reprod. doi: 10.1093/molehr/7.8.747 contributor: fullname: Berkova – volume: 20 start-page: 13 year: 2012 ident: ref_6 article-title: The diagnostic performance of MRI in osteoarthritis: A systematic review and meta-analysis publication-title: Osteoarthr. Cartil. doi: 10.1016/j.joca.2011.10.003 contributor: fullname: Menashe |
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Title | Sex-Specific Differences in Extracellular Vesicle Protein Cargo in Synovial Fluid of Patients with Osteoarthritis |
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