{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,9]],"date-time":"2025-10-09T19:10:47Z","timestamp":1760037047388,"version":"build-2065373602"},"reference-count":60,"publisher":"MDPI AG","issue":"19","license":[{"start":{"date-parts":[[2025,10,7]],"date-time":"2025-10-07T00:00:00Z","timestamp":1759795200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Medical Practice Plan (MPP) granted to Nada Lawand at the American University of Beirut Faculty of Medicine","award":["MPP-NL-19"],"award-info":[{"award-number":["MPP-NL-19"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["IJMS"],"abstract":"<jats:p>Rheumatoid arthritis (RA) is a chronic inflammatory autoimmune disease affecting the joints, with neurogenic inflammation involving the nervous system being a hallmark of the condition. Treatments include medications such as disease-modifying antirheumatic drugs (DMARDs), corticosteroids, and biologics targeting inflammatory pathways. Yet, these treatments are not curative for RA. Heat Shock Proteins (HSPs) are molecular chaperones with immunoregulatory properties; however, their role is not yet fully understood, as these molecules may play a dual, pro- and anti-inflammatory role. In this study, we evaluated the protein expression levels of HSPs 27, 60, 70, and 90 in the synovial membrane and spinal cord of the RA rats\u2019 model to determine their roles during the disease course, both on the neurological and immunological levels. Furthermore, HSP levels have been evaluated in the spinal cord of control and RA rats\u2019 model after high and low doses of ketamine injection. Significant changes in Hsp60, 70, and 90 expression levels were observed only in the spinal cord of RA rats. We demonstrated that blocking N-methyl-D-aspartate receptors with ketamine can modulate spinal cord HSPs expression in RA rats and subsequently impact neurogenic inflammation and adult neurogenesis. This suggests that HSPs may be a promising target for RA treatment due to their complex immunomodulatory effects and potential interactions with the nervous system. Further research is needed to explore their therapeutic potential and develop effective interventions for RA.<\/jats:p>","DOI":"10.3390\/ijms26199743","type":"journal-article","created":{"date-parts":[[2025,10,7]],"date-time":"2025-10-07T10:48:07Z","timestamp":1759834087000},"page":"9743","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Exploring the Role of Heat Shock Proteins in Neuroimmune Modulation in Rheumatoid Arthritis: Insights from a Rat Model"],"prefix":"10.3390","volume":"26","author":[{"given":"Malak","family":"Fouani","sequence":"first","affiliation":[{"name":"Department of Neurology, Duke University, Durham, NC 27710, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Federica","family":"Scalia","sequence":"additional","affiliation":[{"name":"Department of Biomedicine, Neurosciences and Advanced Diagnostics, University of Palermo, 90127 Palermo, Italy"},{"name":"Department of Medicine and Surgery, University of Enna \u201cKore\u201d, 94100 Enna, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Giuseppe Donato","family":"Mangano","sequence":"additional","affiliation":[{"name":"Department of Medicine and Surgery, University of Enna \u201cKore\u201d, 94100 Enna, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6610-5268","authenticated-orcid":false,"given":"Francesca","family":"Rappa","sequence":"additional","affiliation":[{"name":"Department of Biomedicine, Neurosciences and Advanced Diagnostics, University of Palermo, 90127 Palermo, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-9719-9324","authenticated-orcid":false,"given":"Wassim","family":"Abou-Kheir","sequence":"additional","affiliation":[{"name":"Department of Anatomy, Cell Biology and Physiological Sciences, Faculty of Medicine, American University of Beirut, Beirut 1107 2020, Lebanon"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6904-5141","authenticated-orcid":false,"given":"Angelo","family":"Leone","sequence":"additional","affiliation":[{"name":"Department of Biomedicine, Neurosciences and Advanced Diagnostics, University of Palermo, 90127 Palermo, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Nada","family":"Lawand","sequence":"additional","affiliation":[{"name":"Ivy Tech Community College, Indianapolis, IN 46208, USA"}],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6491-3640","authenticated-orcid":false,"given":"Rosario","family":"Barone","sequence":"additional","affiliation":[{"name":"Department of Biomedicine, Neurosciences and Advanced Diagnostics, University of Palermo, 90127 Palermo, Italy"}],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"1968","published-online":{"date-parts":[[2025,10,7]]},"reference":[{"key":"ref_1","first-page":"136","article-title":"What Is the Global Prevalence of Rheumatoid Arthritis (RA) Among Different Age Groups and Ethnicities","volume":"1","author":"Smith","year":"2020","journal-title":"Medscape"},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Fouani, M., Basset, C.A., Mangano, G.D., Leone, L.G., Lawand, N.B., Leone, A., and Barone, R. (2022). Heat Shock Proteins Alterations in Rheumatoid Arthritis. Int. J. Mol. Sci., 23.","DOI":"10.3390\/ijms23052806"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"220","DOI":"10.1186\/ar2292","article-title":"Cells of the Synovium in Rheumatoid Arthritis. Chondrocytes","volume":"9","author":"Otero","year":"2007","journal-title":"Arthritis Res. Ther."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"v3","DOI":"10.1093\/rheumatology\/kes113","article-title":"Understanding the Dynamics: Pathways Involved in the Pathogenesis of Rheumatoid Arthritis","volume":"51","author":"Choy","year":"2012","journal-title":"Rheumatology"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"3537","DOI":"10.1172\/JCI36389","article-title":"Evidence That Cytokines Play a Role in Rheumatoid Arthritis","volume":"118","author":"Brennan","year":"2008","journal-title":"J. Clin. Investig."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"12","DOI":"10.3904\/kjim.2019.271","article-title":"Roles of Mast Cells in Rheumatoid Arthritis","volume":"35","author":"Min","year":"2020","journal-title":"Korean J. Intern. Med."},{"key":"ref_7","doi-asserted-by":"crossref","unstructured":"Yap, H.-Y., Tee, S., Wong, M., Chow, S.-K., Peh, S.-C., and Teow, S.-Y. (2018). Pathogenic Role of Immune Cells in Rheumatoid Arthritis: Implications in Clinical Treatment and Biomarker Development. Cells, 7.","DOI":"10.3390\/cells7100161"},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"64","DOI":"10.1186\/s13075-020-2138-x","article-title":"Cytotoxic T Lymphocyte-Associated Antigen-4-Ig (CTLA-4-Ig) Suppresses Staphylococcus Aureus-Induced CD80, CD86, and pro-Inflammatory Cytokine Expression in Human B Cells","volume":"22","author":"Liu","year":"2020","journal-title":"Arthritis Res. Ther."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"198","DOI":"10.1093\/rheumatology\/kew266","article-title":"Heat Shock Proteins and Their Immunomodulatory Role in Inflammatory Arthritis","volume":"56","author":"Spierings","year":"2017","journal-title":"Rheumatology"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"323","DOI":"10.1177\/1947603518790075","article-title":"Circulating and Synovial Fluid Heat Shock Protein 70 Are Correlated with Severity in Knee Osteoarthritis","volume":"11","author":"Ngarmukos","year":"2020","journal-title":"CARTILAGE"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"357","DOI":"10.3389\/fnins.2014.00357","article-title":"New Insights into the Impact of Neuro-Inflammation in Rheumatoid Arthritis","volume":"8","author":"Fuggle","year":"2014","journal-title":"Front. Neurosci."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"285","DOI":"10.1177\/19714009231187340","article-title":"Autoimmune Diseases of the Spine and Spinal Cord","volume":"37","author":"Biddle","year":"2024","journal-title":"Neuroradiol. J."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"R41","DOI":"10.1186\/ar2399","article-title":"Extracellular Heat Shock Protein 70 Inhibits Tumour Necrosis Factor-\u03b1 Induced Proinflammatory Mediator Production in Fibroblast-like Synoviocytes","volume":"10","author":"Luo","year":"2008","journal-title":"Arthritis Res. Ther."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"3712","DOI":"10.1002\/art.20635","article-title":"Inhibition of Adjuvant-Induced Arthritis by DNA Vaccination with the 70-Kd or the 90-Kd Human Heat-Shock Protein: Immune Cross-Regulation with the 60-Kd Heat-Shock Protein","volume":"50","author":"Quintana","year":"2004","journal-title":"Arthritis Rheum."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"27","DOI":"10.1186\/s12974-016-0486-x","article-title":"HSP60 Plays a Regulatory Role in IL-1\u03b2-Induced Microglial Inflammation via TLR4-P38 MAPK Axis","volume":"13","author":"Swaroop","year":"2016","journal-title":"J. Neuroinflamm."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1186\/ar2674","article-title":"Heat Shock Protein 60 Reactive T Cells in Juvenile Idiopathic Arthritis: What Is New?","volume":"11","author":"Vercoulen","year":"2009","journal-title":"Arthritis Res. Ther."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"138","DOI":"10.3389\/fncel.2017.00138","article-title":"Evidence of a Cell Surface Role for Hsp90 Complex Proteins Mediating Neuroblast Migration in the Subventricular Zone","volume":"11","author":"Miyakoshi","year":"2017","journal-title":"Front. Cell. Neurosci."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"16006","DOI":"10.1073\/pnas.1516131112","article-title":"Exogenous Hsp70 Delays Senescence and Improves Cognitive Function in Aging Mice","volume":"112","author":"Bobkova","year":"2015","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_19","first-page":"359","article-title":"Central Control of Peripheral Joint Inflammation and Heat Hyperalgesia","volume":"2","author":"Sluka","year":"1994","journal-title":"Prog. Pain Res. Manag."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"365","DOI":"10.1016\/0306-4522(93)90069-R","article-title":"Ultrastructural Studies on Peptides in the Dorsal Horn of the Spinal Cord\u2014I. Co-Existence of Galanin with Other Peptides in Primary Afferents in Normal Rats","volume":"57","author":"Zhang","year":"1993","journal-title":"Neuroscience"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/978-1-4939-7321-7_1","article-title":"NMDA Receptors in the Central Nervous System","volume":"1677","author":"Hansen","year":"2017","journal-title":"Methods Mol. Biol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1016\/j.ejphar.2006.02.009","article-title":"Effect of Glutamate Receptor Antagonists and Antirheumatic Drugs on Proliferation of Synoviocytes In Vitro","volume":"535","author":"Rzeski","year":"2006","journal-title":"Eur. J. Pharmacol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"958","DOI":"10.1111\/j.1476-5381.2009.00586.x","article-title":"Substance P and Glutamate Receptor Antagonists Improve the Anti-Arthritic Actions of Dexamethasone in Rats: Combined Therapy on Experimental Arthritis","volume":"159","author":"Lam","year":"2010","journal-title":"Br. J. Pharmacol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"108","DOI":"10.1016\/j.neuroscience.2018.01.028","article-title":"HSP70 Facilitates Memory Consolidation of Fear Conditioning through MAPK Pathway in the Hippocampus","volume":"375","author":"Porto","year":"2018","journal-title":"Neuroscience"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1897","DOI":"10.1038\/jcbfm.2013.144","article-title":"Neuroprotective Effects of Geranylgeranylacetone in Experimental Traumatic Brain Injury","volume":"33","author":"Zhao","year":"2013","journal-title":"J. Cereb. Blood Flow Metab."},{"key":"ref_26","first-page":"e44909","article-title":"Outpatient Ketamine Infusions for the Treatment of Fibromyalgia and Chronic Pain Syndrome: A Case Report","volume":"15","author":"Sharma","year":"2023","journal-title":"Cureus"},{"key":"ref_27","first-page":"e2609","article-title":"Measuring Motor Coordination in Mice","volume":"29","author":"Deacon","year":"2013","journal-title":"J. Vis. Exp."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"920","DOI":"10.3389\/fphar.2019.00920","article-title":"Heat-Shock Proteins in Neuroinflammation","volume":"10","author":"Dukay","year":"2019","journal-title":"Front. Pharmacol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"429","DOI":"10.1093\/rheumatology\/kex308","article-title":"Divergent Roles of Immune Cells and Their Mediators in Pain","volume":"57","author":"Raoof","year":"2018","journal-title":"Rheumatology"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"667","DOI":"10.1007\/s00011-010-0179-3","article-title":"Sensory and Vascular Changes in a Rat Monoarthritis Model: Prophylactic and Therapeutic Effects of Meloxicam","volume":"59","author":"Hashmi","year":"2010","journal-title":"Inflamm. Res."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"302","DOI":"10.1172\/JCI2465","article-title":"Enhanced Expression of Heat Shock Protein 70 (Hsp70) and Heat Shock Factor 1 (HSF1) Activation in Rheumatoid Arthritis Synovial Tissue. Differential Regulation of Hsp70 Expression and Hsf1 Activation in Synovial Fibroblasts by Proinflammatory Cytokines, Shear Stress, and Antiinflammatory Drugs","volume":"102","author":"Schett","year":"1998","journal-title":"J. Clin. Investig."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"17","DOI":"10.1080\/08916930802227466","article-title":"Cell Surface and Relative mRNA Expression of Heat Shock Protein 70 in Human Synovial Cells","volume":"42","author":"Sedlackova","year":"2009","journal-title":"Autoimmunity"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"283","DOI":"10.1007\/s12192-018-0951-9","article-title":"Autoantibodies to Heat Shock Proteins 60, 70, and 90 in Patients with Rheumatoid Arthritis","volume":"24","author":"Mantej","year":"2019","journal-title":"Cell Stress Chaperones"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"1105","DOI":"10.1007\/s12192-020-01114-z","article-title":"Autologous Extracellular Hsp70 Exerts a Dual Role in Rheumatoid Arthritis","volume":"25","author":"Tukaj","year":"2020","journal-title":"Cell Stress Chaperones"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"1018800","DOI":"10.3389\/fpain.2022.1018800","article-title":"Macrophages and Glial Cells: Innate Immune Drivers of Inflammatory Arthritic Pain Perception from Peripheral Joints to the Central Nervous System","volume":"3","author":"Malange","year":"2022","journal-title":"Front. Pain Res."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"960","DOI":"10.1161\/ATVBAHA.110.217877","article-title":"Heat Shock Protein 60 and Immune Inflammatory Responses in Atherosclerosis","volume":"31","author":"Grundtman","year":"2011","journal-title":"Arterioscler. Thromb. Vasc. Biol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"135941","DOI":"10.1016\/j.neulet.2021.135941","article-title":"Role of Innate Immunity in Chemotherapy-Induced Peripheral Neuropathy","volume":"755","author":"Uhelski","year":"2021","journal-title":"Neurosci. Lett."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"378","DOI":"10.1016\/j.expneurol.2007.06.009","article-title":"Inflammation and Its Role in Neuroprotection, Axonal Regeneration and Functional Recovery after Spinal Cord Injury","volume":"209","author":"Donnelly","year":"2008","journal-title":"Exp. Neurol."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"8564215","DOI":"10.1155\/2018\/8564215","article-title":"Chronic Pain in Inflammatory Arthritis: Mechanisms, Metrology, and Emerging Targets\u2014A Focus on the JAK-STAT Pathway","volume":"2018","author":"Salaffi","year":"2018","journal-title":"Pain Res. Manag."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1002\/cpmb.13","article-title":"Detection of Cell Proliferation Markers by Immunofluorescence Staining and Microscopy Imaging in Paraffin-Embedded Tissue Sections","volume":"115","author":"Eminaga","year":"2016","journal-title":"Curr. Protoc. Mol. Biol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"799","DOI":"10.1007\/s00702-014-1180-8","article-title":"Glutamate as a Neurotransmitter in the Healthy Brain","volume":"121","author":"Zhou","year":"2014","journal-title":"J. Neural Transm."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"379","DOI":"10.1586\/ecp.11.17","article-title":"Targeting N-Methyl-D-Aspartate Receptors for Treatment of Neuropathic Pain","volume":"4","author":"Zhou","year":"2011","journal-title":"Expert Rev. Clin. Pharmacol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"895","DOI":"10.1016\/j.jpain.2009.06.012","article-title":"Central Sensitization: A Generator of Pain Hypersensitivity by Central Neural Plasticity","volume":"10","author":"Latremoliere","year":"2009","journal-title":"J. Pain"},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/S0006-8993(96)00842-6","article-title":"Memantine Induces Heat Shock Protein HSP70 in the Posterior Cingulate Cortex, Retrosplenial Cortex and Dentate Gyrus of Rat Brain","volume":"740","author":"Tomitaka","year":"1996","journal-title":"Brain Res."},{"key":"ref_45","first-page":"844502","article-title":"The Effect of Low Dose Intra-Articular S(+) Ketamine on Osteoarthritis in Rats: An Experimental Study","volume":"74","author":"Neto","year":"2024","journal-title":"Braz. J. Anesthesiol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"5013","DOI":"10.3892\/mmr.2016.5164","article-title":"Ketamine Attenuates Osteoarthritis of the Knee via Modulation of Inflammatory Responses in a Rabbit Model","volume":"13","author":"Lu","year":"2016","journal-title":"Mol. Med. Rep."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"970242","DOI":"10.1155\/2015\/970242","article-title":"HSP90 and HSP70: Implication in Inflammation Processes and Therapeutic Approaches for Myeloproliferative Neoplasms","volume":"2015","author":"Sevin","year":"2015","journal-title":"Mediat. Inflamm."},{"key":"ref_48","doi-asserted-by":"crossref","unstructured":"Singh, M.K., Shin, Y., Han, S., Ha, J., Tiwari, P.K., Kim, S.S., and Kang, I. (2024). Molecular Chaperonin HSP60: Current Understanding and Future Prospects. Int. J. Mol. Sci., 25.","DOI":"10.3390\/ijms25105483"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"474","DOI":"10.1016\/j.bbi.2009.12.002","article-title":"Spinally Applied Ketamine or Morphine Attenuate Peripheral Inflammation and Hyperalgesia in Acute and Chronic Phases of Experimental Arthritis","volume":"24","author":"Boettger","year":"2010","journal-title":"Brain Behav. Immun."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"147","DOI":"10.1007\/s00011-018-1202-3","article-title":"Intravenous Anesthetic Ketamine Attenuates Complete Freund\u2019s Adjuvant-Induced Arthritis in Rats via Modulation of MAPKs\/NF-\u03baB","volume":"68","author":"Lin","year":"2019","journal-title":"Inflamm. Res."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1016\/B978-0-12-381298-8.00001-0","article-title":"Constitutive Activity at the Cannabinoid CB1 Receptor and Behavioral Responses","volume":"Volume 484","author":"Hanlon","year":"2010","journal-title":"Methods in Enzymology"},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"e0260423","DOI":"10.1371\/journal.pone.0260423","article-title":"Effects of Different Doses of Complete Freund\u2019s Adjuvant on Nociceptive Behaviour and Inflammatory Parameters in Polyarthritic Rat Model Mimicking Rheumatoid Arthritis","volume":"16","author":"Noh","year":"2021","journal-title":"PLoS ONE"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"e2506","DOI":"10.21769\/BioProtoc.2506","article-title":"Assessment of Thermal Pain Sensation in Rats and Mice Using the Hargreaves Test","volume":"7","author":"Cheah","year":"2017","journal-title":"Bio-Protocol"},{"key":"ref_54","doi-asserted-by":"crossref","unstructured":"Notartomaso, S., Scarselli, P., Di Pietro, P., Battaglia, G., Llebaria, A., Ciruela, F., and Nicoletti, F. (2018). Mechanical Allodynia Assessment in a Murine Neuropathic Pain Model. Bio-Protocol, 8.","DOI":"10.21769\/BioProtoc.2671"},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"172","DOI":"10.4103\/0974-8490.129041","article-title":"Anti-Allodynic and Anti-Hyperalgesic Effects of an Ethanolic Extract and Xylopic Acid from the Fruits of Xylopia Aethiopica in Murine Models of Neuropathic Pain","volume":"6","author":"Woode","year":"2014","journal-title":"Pharmacogn. Res."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"101","DOI":"10.1016\/j.brs.2015.09.006","article-title":"Thalamic Stimulation in Awake Rats Induces Neurogenesis in the Hippocampal Formation","volume":"9","author":"Chamaa","year":"2016","journal-title":"Brain Stimul."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"19781","DOI":"10.1038\/srep19781","article-title":"Skeletal Muscle Heat Shock Protein 60 Increases after Endurance Training and Induces Peroxisome Proliferator-Activated Receptor Gamma Coactivator 1 A1 Expression","volume":"6","author":"Barone","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"1086","DOI":"10.1002\/jcp.25511","article-title":"Effects of Conjugated Linoleic Acid Associated With Endurance Exercise on Muscle Fibres and Peroxisome Proliferator-Activated Receptor \u03b3 Coactivator 1 \u03b1 Isoforms","volume":"232","author":"Barone","year":"2017","journal-title":"J. Cell. Physiol."},{"key":"ref_59","first-page":"4153","article-title":"Comparative Analysis of Hsp10 and Hsp90 Expression in Healthy Mucosa and Adenocarcinoma of the Large Bowel","volume":"34","author":"Rappa","year":"2014","journal-title":"Anticancer Res."},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"927","DOI":"10.1007\/s12192-016-0721-5","article-title":"Quantitative Patterns of Hsps in Tubular Adenoma Compared with Normal and Tumor Tissues Reveal the Value of Hsp10 and Hsp60 in Early Diagnosis of Large Bowel Cancer","volume":"21","author":"Rappa","year":"2016","journal-title":"Cell Stress Chaperones"}],"container-title":["International Journal of Molecular Sciences"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/1422-0067\/26\/19\/9743\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,9]],"date-time":"2025-10-09T18:49:58Z","timestamp":1760035798000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/1422-0067\/26\/19\/9743"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2025,10,7]]},"references-count":60,"journal-issue":{"issue":"19","published-online":{"date-parts":[[2025,10]]}},"alternative-id":["ijms26199743"],"URL":"https:\/\/doi.org\/10.3390\/ijms26199743","relation":{},"ISSN":["1422-0067"],"issn-type":[{"type":"electronic","value":"1422-0067"}],"subject":[],"published":{"date-parts":[[2025,10,7]]}}}