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ACS omega2024; 9(6); 6505-6526; doi: 10.1021/acsomega.3c06647

New Pathophysiological Insights from Serum Proteome Profiling in Equine Atypical Myopathy.

Abstract: Equine atypical myopathy (AM) is a severe environmental intoxication linked to the ingestion of protoxins contained in seeds and seedlings of the sycamore maple () in Europe. The toxic metabolites cause a frequently fatal rhabdomyolysis syndrome in grazing horses. Since these toxic metabolites can also be present in cograzing horses, it is still unclear as to why, in a similar environmental context, some horses show signs of AM, whereas others remain clinically healthy. Label-free proteomic analyses on the serum of 26 diseased AM, 23 cograzers, and 11 control horses were performed to provide insights into biological processes and pathways. A total of 43 and 44 differentially abundant proteins between "AM vs cograzing horses" and "AM vs control horses" were found. Disease-linked changes in the proteome of different groups were found to correlate with detected amounts of toxins, and principal component analyses were performed to identify the 29 proteins representing a robust AM signature. Among the pathway-specific changes, the glycolysis/gluconeogenesis pathway, the coagulation/complement cascade, and the biosynthesis of amino acids were affected. Sycamore maple poisoning results in a combination of inflammation, oxidative stress, and impaired lipid metabolism, which is trying to be counteracted by enhanced glycolysis.
© 2024 The Authors. Published by American Chemical Society.
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Publication Date: 2024-01-29 PubMed ID: 38371826PubMed Central: PMC10870397DOI: 10.1021/acsomega.3c06647Google Scholar: Lookup
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Summary

This research summary has been generated with artificial intelligence and may contain errors and omissions. Refer to the original study to confirm details provided. Submit correction.

This research study focused on equine atypical myopathy (AM), a severe environmental illness affecting horses due to ingestion of protoxins found in sycamore maple seeds, and attempted to analyze the serum proteome profiles in affected equines, cograzers, and control horses to gain insights into this pathophysiological mechanism and establish a robust AM signature.

Study Design and Approach

  • The researchers carried out label-free proteomic analyses on the serum of 26 horses with AM, 23 cograzing horses (those grazing in the same area but not showing signs of AM), and 11 control horses (those not exposed to the toxin).
  • They sought to identify differentially abundant proteins, measure the toxic metabolites linked to AM in the serum, and calculate the correlation between these proteins and the toxin levels.
  • Through the use of principal component analysis, the team identified a set of 29 proteins that consistently appeared in high or low amounts in the diseased horses, thereby representing a robust signature for AM.

Key Findings

  • The researchers found 43 and 44 differentially abundant proteins when comparing affected horses to cograzers and to control horses, respectively.
  • Specific illnesses were found to correlate to certain alterations in protein amounts amongst each group of horses, and these alterations corresponded with the levels of sycamore maple toxins present in their blood.
  • Among the biological processes impacted by AM were the glycolysis/gluconeogenesis pathway (which pertains to how the body breaks down and forms glucose), the coagulation/complement cascade (a major part of the body’s immune response), and the biosynthesis of amino acids (required for protein formation).

Conclusion and Implications

  • The result of sycamore maple poisoning in affected horses is a combination of inflammation, oxidative stress (imbalances in the body’s ability to counteract the harmful effects of free radicals), and impaired lipid metabolism (the process by which fats are broken down in the body).
  • This toxic stress response triggers an enhanced glycolysis to counteract the effects, thus indicating a potential pathway for disease progression and symptoms.
  • The identification of a robust AM signature composed of 29 proteins offers new paths for understanding the disease, preparing predictive models, and focusing on potential therapies for horses exposed to toxic sycamore maple seeds.

Cite This Article

APA
Kruse CJ, Dieu M, Renaud B, Franu00e7ois AC, Stern D, Demazy C, Burteau S, Boemer F, Art T, Renard P, Votion DM. (2024). New Pathophysiological Insights from Serum Proteome Profiling in Equine Atypical Myopathy. ACS Omega, 9(6), 6505-6526. https://doi.org/10.1021/acsomega.3c06647

Publication

ACS omega
ISSN: 2470-1343
NlmUniqueID: 101691658
Country: United States
Language: English
Volume: 9
Issue: 6
Pages: 6505-6526

Researcher Affiliations

Kruse, Caroline-J
  • Department of Functional Sciences, Faculty of Veterinary Medicine, Physiology and Sport Medicine, Fundamental and Applied Research for Animals & Health (FARAH), University of Liu00e8ge, Sart Tilman, 4000 Liu00e8ge 1, Belgium.
Dieu, Marc
  • Namur Research Institute for Life Sciences (Narilis), University of Namur (UNamur), Namur 5000, Belgium.
  • MaSUN, Mass Spectrometry Facility, University of Namur (UNamur), Namur 5000, Belgium.
Renaud, Benou00eet
  • Department of Functional Sciences, Faculty of Veterinary Medicine, Pharmacology and Toxicology, Fundamental and Applied Research for Animals & Health (FARAH), University of Liu00e8ge, Sart Tilman, 4000 Liu00e8ge 1, Belgium.
Franu00e7ois, Anne-Christine
  • Department of Functional Sciences, Faculty of Veterinary Medicine, Pharmacology and Toxicology, Fundamental and Applied Research for Animals & Health (FARAH), University of Liu00e8ge, Sart Tilman, 4000 Liu00e8ge 1, Belgium.
Stern, David
  • GIGA Bioinformatics Platform, GIGA Institute, University of Liu00e8ge, Sart Tilman, 4000 Liu00e8ge, Belgium.
Demazy, Catherine
  • Namur Research Institute for Life Sciences (Narilis), University of Namur (UNamur), Namur 5000, Belgium.
  • MaSUN, Mass Spectrometry Facility, University of Namur (UNamur), Namur 5000, Belgium.
Burteau, Sophie
  • Namur Research Institute for Life Sciences (Narilis), University of Namur (UNamur), Namur 5000, Belgium.
  • MaSUN, Mass Spectrometry Facility, University of Namur (UNamur), Namur 5000, Belgium.
Boemer, Franu00e7ois
  • Biochemical Genetics Lab, Department of Human Genetics, CHU of Liu00e8ge, University of Liu00e8ge, Sart Tilman, 4000 Liu00e8ge, Belgium.
Art, Tatiana
  • Department of Functional Sciences, Faculty of Veterinary Medicine, Physiology and Sport Medicine, Fundamental and Applied Research for Animals & Health (FARAH), University of Liu00e8ge, Sart Tilman, 4000 Liu00e8ge 1, Belgium.
Renard, Patricia
  • Namur Research Institute for Life Sciences (Narilis), University of Namur (UNamur), Namur 5000, Belgium.
  • MaSUN, Mass Spectrometry Facility, University of Namur (UNamur), Namur 5000, Belgium.
Votion, Dominique-M
  • Department of Functional Sciences, Faculty of Veterinary Medicine, Pharmacology and Toxicology, Fundamental and Applied Research for Animals & Health (FARAH), University of Liu00e8ge, Sart Tilman, 4000 Liu00e8ge 1, Belgium.

Conflict of Interest Statement

The authors declare no competing financial interest.

References

This article includes 85 references
  1. Votion D.-M.; van Galen G.; Sweetman L.; Boemer F.; de Tullio P.; Dopagne C.; Lefu00e8re L.; Mouithys-Mickalad A.; Patarin F.; Rouxhet S.; van Loon G.; Serteyn D.; Sponseller B. T.; Valberg S. J. Identification of Methylenecyclopropyl Acetic Acid in Serum of European Horses with Atypical Myopathy. Equine Vet. J. 2014, 46 (2), 146u2013149. 10.1111/evj.12117.
    doi: 10.1111/evj.12117pubmed: 23773055google scholar: lookup
  2. Sander J.; Terhardt M.; Sander S.; Aboling S.; Janzen N. A New Method for Quantifying Causative and Diagnostic Markers of Methylenecyclopropylglycine Poisoning. Toxicol. Rep. 2019, 6, 803u2013808. 10.1016/j.toxrep.2019.08.002.
    doi: 10.1016/j.toxrep.2019.08.002pmc: PMC6699453pubmed: 31440457google scholar: lookup
  3. El-Khatib A. H.; Engel A. M.; Weigel S. Co-Occurrence of Hypoglycin A and Hypoglycin B in Sycamore and Box Elder Maple Proved by LC-MS/MS and LC-HR-MS. Toxins 2022, 14 (9), 608.10.3390/toxins14090608.
    doi: 10.3390/toxins14090608pmc: PMC9504185pubmed: 36136546google scholar: lookup
  4. Von Holt C.; Holt C. Methylenecyclopropaneacetic Acid, a Metabolite of Hypoglycin. Biochim. Biophys. Acta 1966, 125, 1u201310. 10.1016/0005-2760(66)90138-x.
    doi: 10.1016/0005-2760(66)90138-xpubmed: 5968592google scholar: lookup
  5. Melde K.; Buettner H.; Boschert W.; Wolf H. P. O.; Ghisla S. Mechanism of Hypoglycaemic Action of Methylenecyclopropylglycine. Biochem. J. 1989, 259 (3), 921u2013924. 10.1042/bj2590921.
    doi: 10.1042/bj2590921pmc: PMC1138607pubmed: 2730593google scholar: lookup
  6. Melde K.; Jackson S.; Bartlett K.; Sherratt H. S. A.; Ghisla S.; Ghisla S. Metabolic consequences of methylenecyclopropylglycine poisoning in rats. Biochem. J. 1991, 274, 395u2013400. 10.1042/bj2740395.
    doi: 10.1042/bj2740395pmc: PMC1150150pubmed: 2006907google scholar: lookup
  7. Sherratt H. S. A. Hypoglycin, the Famous Toxin of the Unripe Jamaican Ackee Fruit. Trends Pharmacol. Sci. 1986, 7 (C), 186u2013191. 10.1016/0165-6147(86)90310-X.
    doi: 10.1016/0165-6147(86)90310-Xgoogle scholar: lookup
  8. Dimou A.; Tsimihodimos V.; Bairaktari E. The Critical Role of the Branched Chain Amino Acids (BCAAs) Catabolism-Regulating Enzymes, Branched-Chain Aminotransferase (BCAT) and Branched-Chain u03b1-Keto Acid Dehydrogenase (BCKD), in Human Pathophysiology. Int. J. Mol. Sci. 2022, 23, 4022.10.3390/ijms23074022.
    doi: 10.3390/ijms23074022pmc: PMC8999875pubmed: 35409380google scholar: lookup
  9. Neinast M.; Murashige D.; Arany Z. Branched Chain Amino Acids. Annu. Rev. Physiol. 2019, 81, 139u2013164. 10.1146/annurev-physiol-020518-114455.
    doi: 10.1146/annurev-physiol-020518-114455pmc: PMC6536377pubmed: 30485760google scholar: lookup
  10. Von Holt C.; Chang J.; Von Holt M.; Bu00f6hm H. Metabolism and Metabolic Effects of Hypoglycin. Biochim. Biophys. Acta 1964, 90, 611u2013613. 10.1016/0304-4165(64)90242-9.
    doi: 10.1016/0304-4165(64)90242-9pubmed: 14237871google scholar: lookup
  11. Westermann C. M.; Dorland L.; van Diggelen O. P.; Schoonderwoerd K.; Bierau J.; Waterham H. R.; van der Kolk J. H. Decreased Oxidative Phosphorylation and PGAM Deficiency in Horses Suffering from Atypical Myopathy Associated with Acquired MADD. Mol. Genet. Metab. 2011, 104 (3), 273u2013278. 10.1016/j.ymgme.2011.07.022.
    doi: 10.1016/j.ymgme.2011.07.022pubmed: 21843962google scholar: lookup
  12. Lemieux H.; Boemer F.; van Galen G.; Serteyn D.; Amory H.; Baise E.; Cassart D.; van Loon G.; Marcillaud-Pitel C.; Votion D. M. Mitochondrial Function Is Altered in Horse Atypical Myopathy. Mitochondrion 2016, 30, 35u201341. 10.1016/j.mito.2016.06.005.
    doi: 10.1016/j.mito.2016.06.005pubmed: 27374763google scholar: lookup
  13. Cassart D.; Baise E.; Cherel Y.; Delguste C.; Antoine N.; Votion D.; Amory H.; Rollin F.; Linden A.; Coignoul F.; Desmecht D. Morphological Alterations in Oxidative Muscles and Mitochondrial Structure Associated with Equine Atypical Myopathy. Equine Vet. J. 2007, 39 (1), 26u201332. 10.2746/042516407X157765.
    doi: 10.2746/042516407X157765pubmed: 17228591google scholar: lookup
  14. Tanaka K.; Miller E. M.; Isselbacher K. J. Hypoglycin A: A Specific Inhibitor of Isovaleryl CoA Dehydrogenase. Proc. Natl. Acad. Sci. U.S.A. 1971, 68 (1), 20u201324. 10.1073/pnas.68.1.20.
    doi: 10.1073/pnas.68.1.20pmc: PMC391092pubmed: 5276292google scholar: lookup
  15. Renaud B.; Franu00e7ois A.-C.; Boemer F.; Kruse C.; Stern D.; Piot A.; Petitjean T.; Gustin P.; Votion D.-M. Grazing Mares on Pasture with Sycamore Maples: A Potential Threat to Suckling Foals and Food Safety through Milk Contamination. Animals 2021, 11 (1), 87.10.3390/ani11010087.
    doi: 10.3390/ani11010087pmc: PMC7824825pubmed: 33466424google scholar: lookup
  16. Baise E.; Habyarimana J. A.; Amory H.; Boemer F.; Douny C.; Gustin P.; Marcillaud-Pitel C.; Patarin F.; Weber M.; Votion D.-M. Samaras and Seedlings of Acer Pseudoplatanus Are Potential Sources of Hypoglycin A Intoxication in Atypical Myopathy without Necessarily Inducing Clinical Signs. Equine Vet. J. 2016, 48 (4), 414u2013417. 10.1111/evj.12499.
    doi: 10.1111/evj.12499pubmed: 26278545google scholar: lookup
  17. Bochnia M.; Ziegler J.; Sander J.; Uhlig A.; Schaefer S.; Vollstedt S.; Glatter M.; Abel S.; Recknagel S.; Schusser G. F.; Wensch-Dorendorf M.; Zeyner A. Hypoglycin a Content in Blood and Urine Discriminates Horses with Atypical Myopathy from Clinically Normal Horses Grazing on the Same Pasture. PLoS One 2015, 10 (9), e013678510.1371/journal.pone.0136785.
    doi: 10.1371/journal.pone.0136785pmc: PMC4574941pubmed: 26378918google scholar: lookup
  18. Renaud B.; Franu00e7ois A.-C.; Boemer F.; Macillaud-Pitel C.; Gustin P.; Votion D.-M.. Diagnostic and Prognostic Value of Hypoglycin A, Methylenecyclopropyl Acetic Acid-Carnitine and, Acylcarnitines Profile in Horses with Atypical Myopathy. In Proceedings of the 6th FARAH-Day; University of Liu00e8ge: Belgium, 2019.
  19. van Galen G.; Marcillaud Pitel C.; Saegerman C.; Patarin F.; Amory H.; Baily J. D.; Cassart D.; Gerber V.; Hahn C.; Harris P.; Keen J. A.; Kirschvink N.; Lefere L.; McGorum B.; Muller J. M. V.; Picavet M. T. J. E.; Piercy R. J.; Roscher K.; Serteyn D.; Unger L.; van der Kolk J. H.; van Loon G.; Verwilghen D.; Westermann C. M.; Votion D. M. European Outbreaks of Atypical Myopathy in Grazing Equids (2006u20132009): Spatiotemporal Distribution, History and Clinical Features. Equine Vet. J. 2012, 44 (5), 614u2013620. 10.1111/j.2042-3306.2012.00556.x.
    doi: 10.1111/j.2042-3306.2012.00556.xpubmed: 22448904google scholar: lookup
  20. Brandt K.; Hinrichs U.; Glitz F.; Landes E.; Schulze C.; Deegen E.; Pohlenz J.; Coenen M. Atypische Myoglobinurie Der Weidepferde. Pferdeheilkunde 1997, 13 (1), 27u201334. 10.21836/PEM19970104.
    doi: 10.21836/PEM19970104google scholar: lookup
  21. van Galen G.; Saegerman C.; Marcillaud Pitel C.; Patarin F.; Amory H.; Baily J. D.; Cassart D.; Gerber V.; Hahn C.; Harris P.; Keen J. A.; Kirschvink N.; Lefere L.; Mcgorum B.; Muller J. M. V.; Picavet M. T. J. E.; Piercy R. J.; Roscher K.; Serteyn D.; Unger L.; van der Kolk J. H.; van Loon G.; Verwilghen D.; Westermann C. M.; Votion D. M. European Outbreaks of Atypical Myopathy in Grazing Horses (2006u20132009): Determination of Indicators for Risk and Prognostic Factors. Equine Vet. J. 2012, 44 (5), 621u2013625. 10.1111/j.2042-3306.2012.00555.x.
    doi: 10.1111/j.2042-3306.2012.00555.xpubmed: 22413891google scholar: lookup
  22. Fabius L. S.; Westermann C. M. Evidence-Based Therapy for Atypical Myopathy in Horses. Equine Vet. Educ. 2018, 30, 616u2013622. 10.1111/eve.12734.
    doi: 10.1111/eve.12734google scholar: lookup
  23. Zhang Z.; Wu S.; Stenoien D. L.; Pau0161a-Toliu0107 L. High-Throughput Proteomics. Annu. Rev. Anal. Chem. 2014, 7, 427u2013454. 10.1146/annurev-anchem-071213-020216.
    doi: 10.1146/annurev-anchem-071213-020216pubmed: 25014346google scholar: lookup
  24. Chiaradia E.; Miller I. In Slow Pace towards the Proteome of Equine Body Fluids. J. Proteomics 2020, 225 (April), 103880.10.1016/j.jprot.2020.103880.
    doi: 10.1016/j.jprot.2020.103880pubmed: 32569818google scholar: lookup
  25. Aslam B.; Basit M.; Nisar M. A.; Khurshid M.; Rasool M. H. Proteomics: Technologies and Their Applications. J. Chromatogr. Sci. 2017, 55 (2), 182u2013196. 10.1093/chromsci/bmw167.
    doi: 10.1093/chromsci/bmw167pubmed: 28087761google scholar: lookup
  26. Votion D.-M.; Franu00e7ois A.-C.; Kruse C.; Renaud B.; Farinelle A.; Bouquieaux M.-C.; Marcillaud-Pitel C.; Gustin P. Answers to the Frequently Asked Questions Regarding Horse Feeding and Management Practices to Reduce the Risk of Atypical Myopathy. Animals 2020, 10 (2), 365.10.3390/ani10020365.
    doi: 10.3390/ani10020365pmc: PMC7071031pubmed: 32102384google scholar: lookup
  27. Boemer F.; Deberg M.; Schoos R.; Baise E.; Amory H.; Gault G.; Carlier J.; Gaillard Y.; Marcillaud-Pitel C.; Votion D. Quantification of hypoglycin A in serum using aTRAQu00ae assay. J. Chromatogr. B 2015, 997, 75u201380. 10.1016/j.jchromb.2015.06.004.
    doi: 10.1016/j.jchromb.2015.06.004pubmed: 26094208google scholar: lookup
  28. Votion D.-M. Analysing Hypoglycin A, Methylenecyclopropylacetic Acid Conjugates and Acylcarnitines in Blood to Confirm the Diagnosis and Improve Our Understanding of Atypical Myopathy. Equine Vet. Educ. 2018, 30 (1), 29u201330. 10.1111/eve.12617.
    doi: 10.1111/eve.12617google scholar: lookup
  29. Valberg S. J.; Sponseller B. T.; Hegeman A. D.; Earing J.; Bender J. B.; Martinson K. L.; Patterson S. E.; Sweetman L. Seasonal Pasture Myopathy/Atypical Myopathy in North America Associated with Ingestion of Hypoglycin A within Seeds of the Box Elder Tree. Equine Vet. J. 2013, 45 (4), 419u2013426. 10.1111/j.2042-3306.2012.00684.x.
    doi: 10.1111/j.2042-3306.2012.00684.xpubmed: 23167695google scholar: lookup
  30. Wiu015bniewski J. R.; Zougman A.; Nagaraj N.; Mann M. Universal Sample Preparation Method for Proteome Analysis. Nat. Methods 2009, 6 (5), 359u2013362. 10.1038/nmeth.1322.
    doi: 10.1038/nmeth.1322pubmed: 19377485google scholar: lookup
  31. Meier F.; Brunner A.-D.; Koch S.; Koch H.; Lubeck M.; Krause M.; Goedecke N.; Decker J.; Kosinski T.; Park M. A.; Bache N.; Hoerning O.; Cox J.; Ru00e4ther O.; Mann M. Online Parallel Accumulation-Serial Fragmentation (PASEF) with a Novel Trapped Ion Mobility Mass Spectrometer. Mol. Cell. Proteomics 2018, 17 (12), 2534u20132545. 10.1074/mcp.TIR118.000900.
    doi: 10.1074/mcp.TIR118.000900pmc: PMC6283298pubmed: 30385480google scholar: lookup
  32. Matzke M. M.; Waters K. M.; Metz T. O.; Jacobs J. M.; Sims A. C.; Baric R. S.; Pounds J. G.; Webb-robertson B. J. M. Improved Quality Control Processing of Peptide-Centric LC-MS Proteomics Data. Bioinformatics 2011, 27 (20), 2866u20132872. 10.1093/bioinformatics/btr479.
    doi: 10.1093/bioinformatics/btr479pmc: PMC3187650pubmed: 21852304google scholar: lookup
  33. Stanfill B. A.; Nakayasu E. S.; Bramer L. M.; Thompson A. M.; Ansong C. K.; Clauss T. R.; Gritsenko M. A.; Monroe M. E.; Moore R. J.; Orton D. J.; Piehowski P. D.; Schepmoes A. A.; Smith R. D.; Webb-Robertson B.-J. M.; Metz T. O. Quality Control Analysis in Real-Time (QC-ART): A Tool for Real-Time Quality Control Assessment of Mass Spectrometry-Based Proteomics Data. Mol. Cell. Proteomics 2018, 17 (9), 1824u20131836. 10.1074/mcp.RA118.000648.
    doi: 10.1074/mcp.RA118.000648pmc: PMC6126382pubmed: 29666158google scholar: lookup
  34. Lin H.; He L.; Ma B. A Combinatorial Approach to the Peptide Feature Matching Problem for Label-Free Quantification. Bioinformatics 2013, 29 (14), 1768u20131775. 10.1093/bioinformatics/btt274.
    doi: 10.1093/bioinformatics/btt274pubmed: 23665772google scholar: lookup
  35. Thomas P. D.; Ebert D.; Muruganujan A.; Mushayahama T.; Albou L. P.; Mi H. PANTHER: Making Genome-Scale Phylogenetics Accessible to All. Protein Sci. 2022, 31 (1), 8u201322. 10.1002/pro.4218.
    doi: 10.1002/pro.4218pmc: PMC8740835pubmed: 34717010google scholar: lookup
  36. Kanehisa M.; Furumichi M.; Tanabe M.; Sato Y.; Morishima K. KEGG: New Perspectives on Genomes, Pathways, Diseases and Drugs. Nucleic Acids Res. 2017, 45 (D1), D353u2013D361. 10.1093/nar/gkw1092.
    doi: 10.1093/nar/gkw1092pmc: PMC5210567pubmed: 27899662google scholar: lookup
  37. Kanehisa M.; Furumichi M.; Sato Y.; Kawashima M.; Ishiguro-Watanabe M. KEGG for Taxonomy-Based Analysis of Pathways and Genomes. Nucleic Acids Res. 2023, 51 (D1), D587u2013D592. 10.1093/nar/gkac963.
    doi: 10.1093/nar/gkac963pmc: PMC9825424pubmed: 36300620google scholar: lookup
  38. Votion D. M.; Linden A.; Delguste C.; Amory H.; Thiry E.; Engels P.; van Galen G.; Navet R.; Sluse F.; Serteyn D.; Saegerman C. Atypical Myopathy in Grazing Horses: A First Exploratory Data Analysis. Vet. J. 2009, 180 (1), 77u201387. 10.1016/j.tvjl.2008.01.016.
    doi: 10.1016/j.tvjl.2008.01.016pubmed: 18396430google scholar: lookup
  39. Schober P.; Boer C.; Schwarte L. A. Correlation Coefficients: Appropriate Use and Interpretation. Anesth. Analg. 2018, 126 (5), 1763u20131768. 10.1213/ANE.0000000000002864.
    doi: 10.1213/ANE.0000000000002864pubmed: 29481436google scholar: lookup
  40. PeaksTeam . PEAKS X User Manual; Bioinformatics Solutions Inc., 2018, p 243.
  41. Qu J.; Ko C. W.; Tso P.; Bhargava A. Apolipoprotein A-IV: A Multifunctional Protein Involved in Protection against Atherosclerosis and Diabetes. Cells 2019, 8 (4), 319.10.3390/cells8040319.
    doi: 10.3390/cells8040319pmc: PMC6523623pubmed: 30959835google scholar: lookup
  42. Yamamoto K.; Fukuda N.; Fukui M.; Kai Y.; Ikeda H.; Sakai T. Increased Secretion of Triglyceride and Cholesterol Following Inhibition of Long-Chain Fatty Acid Oxidation in Rat Liver. Ann. Nutr. Metab. 1996, 40 (3), 157u2013164. 10.1159/000177909.
    doi: 10.1159/000177909pubmed: 8862698google scholar: lookup
  43. Ge S. X.; Jung D.; Yao R. ShinyGO: A Graphical Gene-Set Enrichment Tool for Animals and Plants. Bioinformatics 2020, 36 (8), 2628u20132629. 10.1093/bioinformatics/btz931.
    doi: 10.1093/bioinformatics/btz931pmc: PMC7178415pubmed: 31882993google scholar: lookup
  44. Delguste C.; Cassart D.; Baise E.; Linden A.; Schwarzwald C.; Feige K.; Sandersen C.; Rollin F.; Amory H. Myopathies Atypiques Chez Les Chevaux Au Pru00e9: Une Su00e9rie de Cas En Belgique. Ann. Med. Vet. 2002, 146 (4), 231u2013243. 10.5167/uzh-61436.
    doi: 10.5167/uzh-61436google scholar: lookup
  45. Votion D.-M.; Linden A.; Saegerman C.; Engels P.; Erpicum M.; Thiry E.; Delguste C.; Rouxhet S.; Demoulin V.; Navet R.; Sluse F.; Serteyn D.; van Galen G.; Amory H. History and Clinical Features of Atypical Myopathy in Horses in Belgium (2000u20132005). J. Vet. Intern. Med. 2007, 21 (6), 1380.10.1892/07-053.1.
    doi: 10.1892/07-053.1pubmed: 18196750google scholar: lookup
  46. Boemer F.; Detilleux J.; Cello C.; Amory H.; Marcillaud-Pitel C.; Richard E.; van Galen G.; van Loon G.; Lefu00e8re L.; Votion D.-M. Acylcarnitines Profile Best Predicts Survival in Horses with At Myopathy. PLoS One 2017, 12 (8), e018276110.1371/journal.pone.0182761.
    doi: 10.1371/journal.pone.0182761pmc: PMC5573150pubmed: 28846683google scholar: lookup
  47. Mathis D.; Sass J. O.; Graubner C.; Schoster A. Diagnosis of Atypical Myopathy Based on Organic Acid and Acylcarnitine Profiles and Evolution of Biomarkers in Surviving Horses. Mol. Genet. Metab. Rep. 2021, 29, 100827.10.1016/j.ymgmr.2021.100827.
    doi: 10.1016/j.ymgmr.2021.100827pmc: PMC8639802pubmed: 34900597google scholar: lookup
  48. Harrison M. F. The Misunderstood Coagulopathy of Liver Disease: A Review for the Acute Setting. West. J. Emerg. Med. 2018, 19 (5), 863u2013871. 10.5811/westjem.2018.7.37893.
    doi: 10.5811/westjem.2018.7.37893pmc: PMC6123093pubmed: 30202500google scholar: lookup
  49. Mammen E. F. Coagulation Abnormalities in Liver Disease. Hematol./Oncol. Clin. North Am. 1992, 6 (6), 1247u20131257. 10.1016/S0889-8588(18)30273-9.
    doi: 10.1016/S0889-8588(18)30273-9pubmed: 1333467google scholar: lookup
  50. Holeu010dek M. Branched-Chain Amino Acids in Health and Disease: Metabolism, Alterations in Blood Plasma, and as Supplements. Nutr. Metab. (London) 2018, 15 (1), 33.10.1186/s12986-018-0271-1.
    doi: 10.1186/s12986-018-0271-1pmc: PMC5934885pubmed: 29755574google scholar: lookup
  51. Giannoglou G. D.; Chatzizisis Y. S.; Misirli G. The Syndrome of Rhabdomyolysis: Pathophysiology and Diagnosis. Eur. J. Intern. Med. 2007, 18, 90u2013100. 10.1016/j.ejim.2006.09.020.
    doi: 10.1016/j.ejim.2006.09.020pubmed: 17338959google scholar: lookup
  52. Wrogemann K.; Pena S. D. J. Mitochondrial Calcium Overloadu202f: A General Mechanism for Cell-Necrosis in Muscle Diseases. Lancet 1976, 307 (7961), 672u2013674. 10.1016/S0140-6736(76)92781-1.
    doi: 10.1016/S0140-6736(76)92781-1pubmed: 73643google scholar: lookup
  53. Rizzuto R.; Pinton P.; Ferrari D.; Chami M.; Szabadkai G.; Magalhu00e3es P. J.; Virgilio F. D.; Pozzan T. Calcium and Apoptosis: Facts and Hypotheses. Oncogene 2003, 22, 8619u20138627. 10.1038/sj.onc.1207105.
    doi: 10.1038/sj.onc.1207105pubmed: 14634623google scholar: lookup
  54. Zamzami N.; Hirsch T.; Dallaporta B.; Petit P. X.; Kroemer G. Mitochondrial Implication in Accidental and Programmed Cell Death: Apoptosis and Necrosis. J. Bioenerg. Biomembr. 1997, 29 (2), 185u2013193. 10.1023/A:1022694131572.
    doi: 10.1023/A:1022694131572pubmed: 9239543google scholar: lookup
  55. Brookes P. S.; Yoon Y.; Robotham J. L.; Anders M. W.; Sheu S.-S. Calcium, ATP, and ROS: A Mitochondrial Love-Hate Triangle. Am. J. Physiol.-Cell Physiol. 2004, 287, C817u2013C833. 10.1152/ajpcell.00139.2004.
    doi: 10.1152/ajpcell.00139.2004pubmed: 15355853google scholar: lookup
  56. Poels P. J. E.; Gabreels F. J. M. Rhabdomyolysis: A Review of the Literature. Clin. Neurol. Neurosurg. 1993, 95, 175u2013192. 10.1016/0303-8467(93)90122-W.
    doi: 10.1016/0303-8467(93)90122-Wpubmed: 8242960google scholar: lookup
  57. Lu00f6fberg M. Myosin Heavy-Chain Fragments and Cardiac Troponins in the Serum in Rhabdomyolysis. Arch. Neurol. 1995, 52 (12), 1210.10.1001/archneur.1995.00540360090020.
    doi: 10.1001/archneur.1995.00540360090020pubmed: 7492296google scholar: lookup
  58. Barrey E.; Mucher E.; Jeansoule N.; Larcher T.; Guigand L.; Herszberg B.; Chaffaux S.; Guu00e9rin G.; Mata X.; Benech P.; Canale M.; Alibert O.; Maltere P.; Gidrol X. Gene Expression Profiling in Equine Polysaccharide Storage Myopathy Revealed Inflammation, Glycogenesis Inhibition, Hypoxia and Mitochondrial Dysfunctions. BMC Vet. Res. 2009, 5 (1), 29.10.1186/1746-6148-5-29.
    doi: 10.1186/1746-6148-5-29pmc: PMC2741442pubmed: 19664222google scholar: lookup
  59. Valberg S. J.; Perumbakkam S.; McKenzie E. C.; Finno C. J. Proteome and Transcriptome Profiling of Equine Myofibrillar Myopathy Identifies Diminished Peroxiredoxin 6 and Altered Cysteine Metabolic Pathways. Physiol. Genomics 2018, 50 (12), 1036u20131050. 10.1152/physiolgenomics.00044.2018.
    doi: 10.1152/physiolgenomics.00044.2018pmc: PMC6337024pubmed: 30289745google scholar: lookup
  60. Finno C. J.; Valberg S. J.; Wu00fcnschmann A.; Murphy M. J. Seasonal Pasture Myopathy in Horses in the Midwestern United States: 14 Cases (1998u20132005). J. Am. Vet. Med. Assoc. 2006, 229 (7), 1134u20131141. 10.2460/javma.229.7.1134.
    doi: 10.2460/javma.229.7.1134pubmed: 17014363google scholar: lookup
  61. Mohammed H. O.; Divers T. J.; Kwak J.; Omar A. H.; White M. E.; de Lahunta A. Association of Oxidative Stress with Motor Neuron Disease in Horses. Am. J. Vet. Res. 2012, 73 (12), 1957u20131962. 10.2460/ajvr.73.12.1957.
    doi: 10.2460/ajvr.73.12.1957pubmed: 23176423google scholar: lookup
  62. de la Ru00faa-Domu00e8nech R.; Wiedmann M.; Mohammed H. O.; Cummings J. F.; Divers T. J.; Batt C. A. Equine Motor Neuron Disease Is Not Linked to Cu/Zn Superoxide Dismutase Mutations: Sequence Analysis of the Equine Cu/Zn Superoxide Dismutase CDNA. Gene 1996, 178 (1u20132), 83u201388. 10.1016/0378-1119(96)00339-3.
    doi: 10.1016/0378-1119(96)00339-3pubmed: 8921896google scholar: lookup
  63. Armstrong R. N. Glutathione Transferases. Compr. Toxicol. 2010, 4, 295u2013321. 10.1016/B978-0-08-046884-6.00416-4.
    doi: 10.1016/B978-0-08-046884-6.00416-4google scholar: lookup
  64. Gumulec J.; Raudenska M.; Hlavna M.; Stracina T.; Sztalmachova M.; Tanhauserova V.; Pacal L.; Ruttkay-Nedecky B.; Sochor J.; Zitka O.; Babula P.; Adam V.; Kizek R.; Novakova M.; Masarik M. Determination of Oxidative Stress and Activities of Antioxidant Enzymes in Guinea Pigs Treated with Haloperidol. Exp. Ther. Med. 2013, 5 (2), 479u2013484. 10.3892/etm.2012.822.
    doi: 10.3892/etm.2012.822pmc: PMC3570091pubmed: 23403848google scholar: lookup
  65. Huang J.; Tan P. H.; Tan B. K. H.; Bay B. H. GST-Pi Expression Correlates with Oxidative Stress and Apoptosis in Breast Cancer. Oncol. Rep. 2004, 12 (4), 921u2013925. 10.3892/or.12.4.921.
    doi: 10.3892/or.12.4.921pubmed: 15375523google scholar: lookup
  66. Tew K. D.; Townsend D. M. Glutathione-S-Transferases as Determinants of Cell Survival and Death. Antioxid. Redox Signaling 2012, 17 (12), 1728u20131737. 10.1089/ars.2012.4640.
    doi: 10.1089/ars.2012.4640pmc: PMC3474190pubmed: 22540427google scholar: lookup
  67. Barrey E.; Jayr L.; Mucher E.; Gospodnetic S.; Joly F.; Benech P.; Alibert O.; Gidrol X.; Mata X.; Vaiman A.; Guu00e9rin G. Transcriptome Analysis of Muscle in Horses Suffering from Recurrent Exertional Rhabdomyolysis Revealed Energetic Pathway Alterations and Disruption in the Cytosolic Calcium Regulation. Anim. Genet. 2012, 43 (3), 271u2013281. 10.1111/j.1365-2052.2011.02246.x.
    doi: 10.1111/j.1365-2052.2011.02246.xpubmed: 22486498google scholar: lookup
  68. Singer E.; Marku00f3 L.; Paragas N.; Barasch J.; Dragun D.; Mu00fcller D. N.; Budde K.; Schmidt-Ott K. M. Neutrophil Gelatinase-Associated Lipocalin: Pathophysiology and Clinical Applications. Acta Physiol. 2013, 207, 663u2013672. 10.1111/apha.12054.
    doi: 10.1111/apha.12054pmc: PMC3979296pubmed: 23375078google scholar: lookup
  69. Wasung M. E.; Chawla L. S.; Madero M. Biomarkers of Renal Function, Which and When?. Clin. Chim. Acta 2015, 438, 350u2013357. 10.1016/j.cca.2014.08.039.
    doi: 10.1016/j.cca.2014.08.039pubmed: 25195004google scholar: lookup
  70. Wouters C.Metabolomic/Lipidomic Investigations in Equine Atypical Myopathy and in Vitro Screening of Non-Pharmaceutical Compounds, Universitu00e9 de Liu00e8ge, 2021.
  71. Dunnett M.; Harris R. C.; Sewell D. A. Taurine Content and Distribution in Equine Skeletal Muscle. Scand. J. Clin. Lab. Invest. 1992, 52 (7), 725u2013730. 10.3109/00365519209115518.
    doi: 10.3109/00365519209115518pubmed: 1455166google scholar: lookup
  72. Valberg S.; Hu00e4ggendal J.; Lindholm A. Blood Chemistry and Skeletal Muscle Metabolic Responses to Exercise in Horses with Recurrent Exertional Rhabdomyolysis. Equine Vet. J. 1993, 25 (1), 17u201322. 10.1111/j.2042-3306.1993.tb02894.x.
    doi: 10.1111/j.2042-3306.1993.tb02894.xpubmed: 8422879google scholar: lookup
  73. Holloszy J. O.; Constable S. H.; Young D. A. Activation of Glucose Transport in Muscle by Exercise. Diabetes/Metab. Rev. 1986, 1 (4), 409u2013423. 10.1002/dmr.5610010405.
    doi: 10.1002/dmr.5610010405pubmed: 3522139google scholar: lookup
  74. Lacombe V. A.; Hinchcliff K. W.; Kohn C. W.; Devor S. T.; Taylor L. E. Effects of feeding meals with various soluble-carbohydrate content on muscle glycogen synthesis after exercise in horses. Am. J. Vet. Res. 2004, 65, 916u2013923. 10.2460/ajvr.2004.65.916.
    doi: 10.2460/ajvr.2004.65.916pubmed: 15281649google scholar: lookup
  75. Jose-Cunilleras E.; Hayes K. A.; Toribio R. E.; Mathes L. E.; Hinchcliff K. W. Expression of Equine Glucose Transporter Type 4 in Skeletal Muscle after Glycogen-Depleting Exercise. Am. J. Vet. Res. 2005, 66 (3), 379u2013385. 10.2460/ajvr.2005.66.379.
    doi: 10.2460/ajvr.2005.66.379pubmed: 15822579google scholar: lookup
  76. Huang C. K.; Sun Y.; Lv L.; Ping Y. ENO1 and Cancer. Mol. Ther.--Oncolytics 2022, 24, 288u2013298. 10.1016/j.omto.2021.12.026.
    doi: 10.1016/j.omto.2021.12.026pmc: PMC8987341pubmed: 35434271google scholar: lookup
  77. Khan F. Y. Rhabdomyolysis: A Review of the Literature. Neth. J. Med. 2009, 67 (9), 272u2013283.
    pubmed: 19841484
  78. Akmal M.; Massry S. G. Reversible Hepatic Dysfunction Associated with Rhabdomyolysis. Am. J. Nephrol. 1990, 10 (1), 49u201352. 10.1159/000168053.
    doi: 10.1159/000168053pubmed: 2343880google scholar: lookup
  79. Garcu00eda-Cau00f1averas J. C.; Peris-Du00edaz M. D.; Alcoriza-Balaguer M. I.; Cerdu00e1n-Calero M.; Donato M. T.; Lahoz A. A Lipidomic Cell-Based Assay for Studying Drug-Induced Phospholipidosis and Steatosis. Electrophoresis 2017, 38 (18), 2331u20132340. 10.1002/elps.201700079.
    doi: 10.1002/elps.201700079pubmed: 28512733google scholar: lookup
  80. Teresa Donato M.; Jose Gomez-Lechon M. Drug-Induced Liver Steatosis and Phospholipidosis: Cell-Based Assays for Early Screening of Drug Candidates. Curr. Drug Metab. 2012, 13 (8), 1160u20131173. 10.2174/138920012802850001.
    doi: 10.2174/138920012802850001pubmed: 22746303google scholar: lookup
  81. Muto-fujita A. A Novel Model for the Chemical Evolution of Metabolic Networks. Bull. Chem. Soc. Jpn. B Chem. Soc. Jpn. 2019, 37 (3), 57u201362. 10.11546/cicsj.37.57.
    doi: 10.11546/cicsj.37.57google scholar: lookup
  82. Valberg S. J.; Velez-Irizarry D.; Williams Z. J.; Henry M. L.; Iglewski H.; Herrick K.; Fenger C. Enriched Pathways of Calcium Regulation, Cellular/Oxidative Stress, Inflammation, and Cell Proliferation Characterize Gluteal Muscle of Standardbred Horses between Episodes of Recurrent Exertional Rhabdomyolysis. Genes (Basel) 2022, 13 (10), 1853.10.3390/genes13101853.
    doi: 10.3390/genes13101853pmc: PMC9601720pubmed: 36292738google scholar: lookup
  83. Avellini L.; Chiaradia E.; Gaiti A. Effect of Exercise Training, Selenium and Vitamin E on Some Free Radical Scavengers in Horses (Equus Caballus). Comp. Biochem. Physiol., Part B: Biochem. Mol. Biol. 1999, 123, 147u2013154. 10.1016/S0305-0491(99)00045-0.
    doi: 10.1016/S0305-0491(99)00045-0pubmed: 10425718google scholar: lookup
  84. Gomez D. E.; Valberg S. J.; Magdesian K. G.; Hanna P. E.; Lofstedt J. Acquired Multiple Acyl-CoA Dehydrogenase Deficiency and Marked Selenium Deficiency Causing Severe Rhabdomyolysis in a Horse. Can. Vet. J. 2015, 56 (11), 1166u20131171.
    pmc: PMC4608471pubmed: 26538673
  85. Koves T. R.; Ussher J. R.; Noland R. C.; Slentz D.; Mosedale M.; Ilkayeva O.; Bain J.; Stevens R.; Dyck J. R. B.; Newgard C. B.; Lopaschuk G. D.; Muoio D. M. Mitochondrial Overload and Incomplete Fatty Acid Oxidation Contribute to Skeletal Muscle Insulin Resistance. Cell Metab. 2008, 7 (1), 45u201356. 10.1016/j.cmet.2007.10.013.
    doi: 10.1016/j.cmet.2007.10.013pubmed: 18177724google scholar: lookup

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