[en] The objective of this study was to compare the blood metabolomic profiles of horses with AM clinical signs with those of healthy co-grazing (Co-G) horses.
Research Center/Unit :
FARAH - Fundamental and Applied Research for Animals and Health - ULiège
Renaud, Benoît ; Université de Liège - ULiège > Département des sciences fonctionnelles (DSF) > Département des sciences fonctionnelles (DSF)
François, Anne-Christine ; Université de Liège - ULiège > Pharmacologie, pharmacothérapie et toxicologie
Fortier-Guillaume, Justine
Marcillaud-Pitel, Christel
BOEMER, François ; Centre Hospitalier Universitaire de Liège - CHU > Unilab > Laboratoire Biochimie Génétique
De Tullio, Pascal ; Université de Liège - ULiège > Département de pharmacie > Chimie pharmaceutique
Richard, Eric
Votion, Dominique ; Université de Liège - ULiège > Scientifiques attachés au Doyen (F MV)
Language :
English
Title :
Metabolomic Signatures Discriminate Horses with Clinical Signs of Atypical Myopathy from Healthy Co-grazing Horses
Alternative titles :
[fr] Les signatures métabolomiques permettent de distinguer les chevaux présentant des signes cliniques de myopathie atypique de leur compagnons de pâture
Publication date :
2021
Journal title :
Journal of Proteome Research
ISSN :
1535-3893
eISSN :
1535-3907
Publisher :
American Chemical Society, United States - District of Columbia
Peer reviewed :
Peer Reviewed verified by ORBi
Funders :
DGA - Région wallonne. Direction générale de l'Agriculture IFCE - Institut Français du Cheval et de l'Équitation Pommier Nutrition SARL
Votion, D.-M.; van Galen, G.; Sweetman, L.; Boemer, F.; Tullio, P.; Dopagne, C.; Lefère, L.; Mouithys-mickalad, A. A.; Patarin, F.; Rouxhet, S.; van Loon, G.; Serteyn, D.; Sponseller, B. T.; Valberg, S. Identification of Methylenecyclopropyl Acetic Acid in Serum of European Horses with Atypical Myopathy. Equine Vet. J. 2014, 46, 146-149, 10.1111/evj.12117
Fowden, L.; Pratt, H. M. Cyclopropylamino Acids of the Genus Acer: Distribution and Biosynthesis. Phytochemistry 1973, 12, 1677-1681, 10.1016/0031-9422(73)80387-5
Sherratt, H. S. A. Hypoglycin, the Famous Toxin of the Unripe Jamaican Ackee Fruit. Trends Pharmacol. Sci. 1986, 7, 186-191, 10.1016/0165-6147(86)90310-X
Melde, K.; Jackson, S.; Bartlett, K.; Sherratt, H.; Ghisla, S. Metabolic Consequences of Methylenecyclopropylglycine Poisoning in Rats. Biochem. J 1991, 274, 395-400, 10.1042/bj2740395
Bochnia, M.; Sander, J.; Ziegler, J.; Terhardt, M.; Sander, S.; Janzen, N.; Cavalleri, J. V.; Zuraw, A.; Wensch-dorendorf, M.; Zeyner, A. Detection of MCPG Metabolites in Horses with Atypical Myopathy. PLoS One 2019, 96, e0211698 10.1371/journal.pone.0211698
Osmundsen, H.; Sherratt, H. S. A. A Novel Mechanism for Inhibition of β-Oxidation by Methylenecyclopropylacetyl-CoA, a Metabolite of Hypoglycin. FEBS Lett. 1975, 55, 38-41, 10.1016/0014-5793(75)80951-3
Ikeda, Y.; Tanaka, K. Selective Inactivation of Various Acyl-CoA Dehydrogenases by (Methylenecyclopropyl)acetyl-CoA. Biochim. Biophys. Acta, Protein Struct. Mol. Enzymol. 1990, 1038, 216-221, 10.1016/0167-4838(90)90208-W
Lai, M.; L D; Oh, E.; Liu, H. Inactivation of Medium-Chain Acyl-CoA Dehydrogenase by a Metabolite of Hypoglycin: Characterization of the Major Turnover Product and Evidence Suggesting an Alternative Flavin Modification Pathway. J. Am. Chem. Soc. 1993, 115, 1619-1628, 10.1021/ja00058a001
Li, D.; Agnihotri, G.; Dakoji, S.; Oh, E.; Lantz, M.; Liu, H. W. The Toxicity of Methylenecyclopropylglycine: Studies of the Inhibitory Effects of (Methylenecyclopropyl)formyl-CoA on Enzymes Involved in Fatty Acid Metabolism and the Molecular Basis of Its Inactivation of Enoyl-CoA Hydratases. J. Am. Chem. Soc. 1999, 121, 9034-9042, 10.1021/ja991908w
Westermann, C. M.; Dorland, L.; Votion, D. M.; de Sain-van der Velden, M. G. M.; Wijnberg, I. D.; Wanders, R. J. A.; Spliet, W. G. M.; Testerink, N.; Berger, R.; Ruiter, J. P. N.; van der Kolk, J. H. Acquired Multiple Acyl-CoA Dehydrogenase Deficiency in 10 Horses with Atypical Myopathy. Neuromuscul. Disord. 2008, 18, 355-364, 10.1016/j.nmd.2008.02.007
Boemer, F.; Detilleux, J.; Cello, C.; Amory, H.; Marcillaud-pitel, C.; Richard, E.; van Galen, G.; van Loon, G.; Votion, D.-M. Acylcarnitines Profile Best Predicts Survival in Horses with Atypical Myopathy. PLoS One 2017, 12, e0182761 10.1371/journal.pone.0182761
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 (2006-2009): Spatiotemporal Distribution, History and Clinical Features. Equine Vet. J. 2012, 44, 614-620, 10.1111/j.2042-3306.2012.00556.x
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 aTRAQ Assay. J. Chromatogr. B 2015, 997, 75-80, 10.1016/j.jchromb.2015.06.004
Rudolph, W.; Remane, D.; Wissenbach, D. K.; Klein, C.; Barnewitz, D.; Peters, F. T. Development and Validation of an Ultrahigh Performance Liquid Chromatography-High Resolution Tandem Mass Spectrometry Quantification Method for Hypoglycin A and Methylene Cyclopropyl Acetic Acid Carnitine in Horse Serum in Cases of Atypical Myopathy. Drug Test. Anal. 2018, 10, 814-820, 10.1002/dta.2337
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, 803-808, 10.1016/j.toxrep.2019.08.002
González-Medina, S.; Hyde, C.; Lovera, I.; Piercy, R. J. Detection of Hypoglycin A and MCPA-Carnitine in Equine Serum and Muscle Tissue: Optimisation and Validation of a LC-MS-based Method without Derivatisation. Equine Vet. J. 2021, 53, 558-568, 10.1111/evj.13303
Wimmer-Scherr, C.; Taminiau, B.; Renaud, B.; van Loon, G.; Palmers, K.; Votion, D.; Amory, H.; Daube, G.; Cesarini, C. Comparison of Fecal Microbiota of Horses Suffering from Atypical Myopathy and Healthy Co-Grazers. Animals 2021, 11, 506, 10.3390/ani11020506
González-Medina, S.; Ireland, J. L.; Piercy, R. J.; Newton, J. R.; Votion, D.-M. Equine Atypical Myopathy in the UK: Epidemiological Characteristics of Cases Reported from 2011 to 2015 and Factors Associated with Survival. Equine Vet. J. 2018, 12, 3218-3221, 10.1111/evj.12694
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 (2000-2005). J. Vet. Intern. Med. 2007, 21, 1380-1391, 10.1111/j.1939-1676.2007.tb01962.x
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, e0136785 10.1371/journal.pone.0136785
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, 414-417, 10.1111/evj.12499
Gröndahl, G. et al. Detection of the Toxin Hypoglycin A in Pastured Horses and in the European Sycamore Maple Tree (Acer Pseudoplatanus) during Two Outbreaks of Atypical Myopathy in Sweden. Equine Vet. J. 2015, 47, 22, 10.1111/evj.12486_49
Renaud, B.; François, A.-C.; Marcillaud-pitel, C.; Gustin, P.; Votion, D.-M. In Proceedings of the 6th FARAH-Day' Diagnostic and Prognostic Value Of Hypoglycin A, Methylenecyclopropyl Acetic Acid-carnitine and, Acylcarnitines Profile in Horses with Atypical Myopathy, Liège, Belgium, 2019; p 25.
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, 77-87, 10.1016/j.tvjl.2008.01.016
Karlíková, R.; Široká, J.; Jahn, P.; Friedecký, D.; Gardlo, A.; Janečková, H.; Hrdinová, F.; Drábková, Z.; Adam, T. Equine Atypical Myopathy: A Metabolic Study. Vet. J. 2016, 216, 125-132, 10.1016/j.tvjl.2016.07.015
Valberg, S.; Sponseller, B. T.; Hegele, R. A.; 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, 419-426, 10.1111/j.2042-3306.2012.00684.x
Giacomoni, F.; Le Corguillé, G.; Monsoor, M.; Landi, M.; Pericard, P.; Pétéra, M.; Duperier, C.; Tremblay-Franco, M.; Martin, J. F.; Jacob, D.; Goulitquer, S.; Thévenot, E. A.; Caron, C. Workflow4Metabolomics: A Collaborative Research Infrastructure for Computational Metabolomics. Bioinformatics 2015, 31, 1493-1495, 10.1093/bioinformatics/btu813
Smith, C. A.; Want, E. J.; O'Maille, G.; Abagyan, R.; Siuzdak, G. XCMS: Processing Mass Spectrometry Data for Metabolite Profiling Using Nonlinear Peak Alignment, Matching, and Identification. Anal. Chem. 2006, 78, 779-787, 10.1021/ac051437y
Cleveland, W. S.; Grosse, E. Computational Methods for Local Regression. Stat. Comput. 1991, 1, 47-62, 10.1007/BF01890836
Van Der Kloet, F. M.; Bobeldijk, I.; Verheij, E. R.; Jellema, R. H. Analytical Error Reduction Using Single Point Calibration for Accurate and Precise Metabolomic Phenotyping. J. Proteome Res. 2009, 8, 5132-5141, 10.1021/pr900499r
Dunn, W. B.; Broadhurst, D.; Begley, P.; Zelena, E.; Francis-Mcintyre, S.; Anderson, N.; Brown, M.; Knowles, J. D.; Halsall, A.; Haselden, J. N.; Nicholls, A. W.; Wilson, I. D.; Kell, D. B.; Goodacre, R. Procedures for Large-Scale Metabolic Profiling of Serum and Plasma Using Gas Chromatography and Liquid Chromatography Coupled to Mass Spectrometry. Nat. Protoc. 2011, 6, 1060-1083, 10.1038/nprot.2011.335
Thévenot, E. A.; Roux, A.; Xu, Y.; Ezan, E.; Junot, C. Analysis of the Human Adult Urinary Metabolome Variations with Age, Body Mass Index, and Gender by Implementing a Comprehensive Workflow for Univariate and OPLS Statistical Analyses. J. Proteome Res. 2015, 14, 3322-3335, 10.1021/acs.jproteome.5b00354
Kowarik, A.; Templ, M. Imputation with the R Package VIM. J. Stat. Software 2016, 74, 5842 10.18637/jss.v074.i07
Do, K. T.; Wahl, S.; Raffler, J.; Molnos, S.; Laimighofer, M.; Adamski, J.; Suhre, K.; Strauch, K.; Peters, A.; Gieger, C.; Langenberg, C.; Stewart, I. D.; Theis, F. J.; Grallert, H.; Kastenmüller, G.; Krumsiek, J. Characterization of Missing Values in Untargeted MS-Based Metabolomics Data and Evaluation of Missing Data Handling Strategies. Metabolomics 2018, 14, 128 10.1007/s11306-018-1420-2
Galindo-Prieto, B.; Eriksson, L.; Trygg, J. Variable Influence on Projection (VIP) for Orthogonal Projections to Latent Structures (OPLS). J. Chemom. 2014, 28, 623-632, 10.1002/cem.2627
Wang, M.; Carver, J. J.; Phelan, V. V.; Sanchez, L. M.; Garg, N.; Peng, Y.; Nguyen, D. D.; Watrous, J.; Kapono, C. A.; Luzzatto-Knaan, T.; Porto, C.; Bouslimani, A.; Melnik, A. V.; Meehan, M. J.; Liu, W.-T.; Crüsemann, M.; Boudreau, P. D.; Esquenazi, E.; Sandoval-Calderón, M.; Kersten, R. D.; Pace, L. A.; Quinn, R. A.; Duncan, K. R.; Hsu, C.-C.; Floros, D. J.; Gavilan, R. G.; Kleigrewe, K.; Northen, T.; Dutton, R. J.; Parrot, D.; Carlson, E. E.; Aigle, B.; Michelsen, C. F.; Jelsbak, L.; Sohlenkamp, C.; Pevzner, P.; Edlund, A.; McLean, J.; Piel, J.; Murphy, B. T.; Gerwick, L.; Liaw, C.-C.; Yang, Y.-L.; Humpf, H.-U.; Maansson, M.; Keyzers, R. A.; Sims, A. C.; Johnson, A. R.; Sidebottom, A. M.; Sedio, B. E.; Klitgaard, A.; Larson, C. B.; Boya, P. C. A.; Torres-Mendoza, D.; Gonzalez, D. J.; Silva, D. B.; Marques, L. M.; Demarque, D. P.; Pociute, E.; O'Neill, E. C.; Briand, E.; Helfrich, E. J. N.; Granatosky, E. A.; Glukhov, E.; Ryffel, F.; Houson, H.; Mohimani, H.; Kharbush, J. J.; Zeng, Y.; Vorholt, J. A.; Kurita, K. L.; Charusanti, P.; McPhail, K. L.; Nielsen, K. F.; Vuong, L.; Elfeki, M.; Traxler, M. F.; Engene, N.; Koyama, N.; Vining, O. B.; Baric, R.; Silva, R. R.; Mascuch, S. J.; Tomasi, S.; Jenkins, S.; Macherla, V.; Hoffman, T.; Agarwal, V.; Williams, P. G.; Dai, J.; Neupane, R.; Gurr, J.; Rodríguez, A. M. C.; Lamsa, A.; Zhang, C.; Dorrestein, K.; Duggan, B. M.; Almaliti, J.; Allard, P.-M.; Phapale, P.; Nothias, L.-F.; Alexandrov, T.; Litaudon, M.; Wolfender, J.-L.; Kyle, J. E.; Metz, T. O.; Peryea, T.; Nguyen, D.-T.; VanLeer, D.; Shinn, P.; Jadhav, A.; Müller, R.; Waters, K. M.; Shi, W.; Liu, X.; Zhang, L.; Knight, R.; Jensen, P. R.; Palsson, B. Ø.; Pogliano, K.; Linington, R. G.; Gutiérrez, M.; Lopes, N. P.; Gerwick, W. H.; Moore, B. S.; Dorrestein, P. C.; Bandeira, N. Sharing and Community Curation of Mass Spectrometry Data with Global Natural Products Social Molecular Networking. Nat. Biotechnol. 2016, 34, 828-837, 10.1038/nbt.3597
Sumner, L. W.; Amberg, A.; Barrett, D.; Beale, M. H.; Beger, R.; Daykin, C. A.; Fan, T. W.-M.; Fiehn, O.; Goodacre, R.; Griffin, J. L.; Hankemeier, T.; Hardy, N.; Harnly, J.; Higashi, R.; Kopka, J.; Lane, A. N.; Lindon, J. C.; Marriott, P.; Nicholls, A. W.; Reily, M. D.; Thaden, J. J.; Viant, M. R. Proposed Minimum Reporting Standards for Chemical Analysis. Metabolomics 2007, 3, 211-221, 10.1007/s11306-007-0082-2
Kanehisa, M.; Goto, S.; Sato, Y.; Kawashima, M.; Furumichi, M.; Tanabe, M. Data, Information, Knowledge and Principle: Back to Metabolism in KEGG. Nucleic Acids Res. 2014, 42, D199-D205, 10.1093/nar/gkt1076
Xia, J.; Wishart, D. S. MSEA: A Web-Based Tool to Identify Biologically Meaningful Patterns in Quantitative Metabolomic Data. Nucleic Acids Res. 2010, 38, W71-W77, 10.1093/nar/gkq329
Chong, J.; Soufan, O.; Li, C.; Caraus, I.; Li, S.; Bourque, G.; Wishart, D. S.; Xia, J. MetaboAnalyst 4.0: towards more transparent and integrative metabolomics analysis. Nucleic Acids Res. 2018, 46, 486-494, 10.1093/nar/gky310
Otasek, D.; Morris, J. H.; Bouças, J.; Pico, A. R.; Demchak, B. Cytoscape Automation: Empowering Workflow-Based Network Analysis. Genome Biol. 2019, 20, 185 10.1186/s13059-019-1758-4
Westermann, C. M.; Dorland, L.; Wijnberg, I. D.; van der Kolk, J. H. Equine Metabolic Myopathies with Emphasis on the Diagnostic Approach Comparison with Human Myopathies a Review. Vet. Q. 2007, 29, 42-59, 10.1080/01652176.2007.9695227
Foulon, V.; Sniekers, M.; Huysmans, E.; Asselberghs, S.; Mahieu, V.; Mannaerts, G. P.; Van Veldhoven, P. P.; Casteels, M. Breakdown of 2-Hydroxylated Straight Chain Fatty Acids via Peroxisomal 2-Hydroxyphytanoyl-CoA Lyase: A Revised Pathway for the α-Oxidation of Straight Chain Fatty Acids. J. Biol. Chem. 2005, 280, 9802-9812, 10.1074/jbc.M413362200
Van Veldhoven, P. P. Biochemistry and Genetics of Inherited Disorders of Peroxisomal Fatty Acid Metabolism. J. Lipid Res. 2010, 51, 2863-2895, 10.1194/jlr.r005959
Kondo, N.; Ohno, Y.; Yamagata, M.; Obara, T.; Seki, N.; Kitamura, T.; Naganuma, T.; Kihara, A. Identification of the Phytosphingosine Metabolic Pathway Leading to Odd-Numbered Fatty Acids. Nat. Commun. 2014, 5, 5338 10.1038/ncomms6338
Jenkins, B.; West, J. A.; Koulman, A. A Review of Odd-Chain Fatty Acid Metabolism and the Role of Pentadecanoic Acid (C15:0) and Heptadecanoic Acid (C17:0) in Health and Disease. Molecules 2015, 20, 2425-2444, 10.3390/molecules20022425
Oizumi, J.; Giudici, T. A.; Ng, W. G.; Shaw, K. N. F.; Donnell, G. N. Propionate Metabolism by Cultured Skin Fibroblasts from Normal Individuals and Patients with Methylmalonicaciduria and Propionicacidemia. Biochem. Med. 1981, 26, 28-40, 10.1016/0006-2944(81)90027-2
Pfeuffer, M.; Jaudszus, A. Pentadecanoic and Heptadecanoic Acids: Multifaceted Odd-Chain Fatty Acids. Adv. Nutr. 2016, 7, 730-734, 10.3945/an.115.011387
Sander, J.; Terhardt, M.; Janzen, N. Study on the Metabolic Effects of Repeated Consumption of Canned Ackee. J. Agric. Food Chem. 2020, 68, 14603-14609, 10.1021/acs.jafc.0c06235
Long, B.; Koyfman, A.; Gottlieb, M. An Evidence-Based Narrative Review of the Emergency Department Evaluation and Management of Rhabdomyolysis. Am. J. Emerg. Med. 2019, 37, 518-523, 10.1016/j.ajem.2018.12.061
Dunnett, M.; Harris, R. C. Carnosine and Taurine Contents of Type I, IIA and IIB Fibres in the Middle Gluteal Muscle. Equine Vet. J. 1995, 27, 214-217, 10.1111/j.2042-3306.1995.tb04922.x
Dunnett, M.; Harris, R. C.; Dunnett, C. E.; Harris, P. A. Plasma Carnosine Concentration: Diurnal Variation and Effects of Age, Exercise and Muscle Damage. Equine Vet. J. Suppl. 2002, 34, 283-287, 10.1111/j.2042-3306.2002.tb05434.x
Sewell, D. A.; Harris, R. C.; Marlin, D. J.; Dunnett, M. Estimation of the Carnosine Content of Different Fibre Types in the Middle Gluteal Muscle of the Thoroughbred Horse. J. Physiol. 1992, 97, 447-453, 10.1113/jphysiol.1992.sp019310
Rivero, J. L.; Serrano, A. L.; Henckel, P.; Aguera, E. Muscle Fiber Type Composition and Fiber Size in Successfully and Unsuccessfully Endurance-Raced Horses. J. Appl. Physiol. 1993, 75, 1758-1766, 10.1152/jappl.1993.75.4.1758
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, 26-32, 10.2746/042516407X157765
Dunnett, M. Carnosine Metabolism and Function in the Thoroughbred Horse. PhD thesis, 1996.
Verheyen, T.; Decloedt, A.; de Clercq, D.; van Loon, G. Cardiac Changes in Horses with Atypical Myopathy. J. Vet. Intern. Med. 2012, 26, 1019-1026, 10.1111/j.1939-1676.2012.00945.x
Leys, D.; Basran, J.; Scrutton, N. S. Channelling and Formation of "Active" Formaldehyde in Dimethylglycine Oxidase. EMBO J. 2003, 22, 4038-4048, 10.1093/emboj/cdg395
Wenz, A.; Thorpe, C.; Ghisla, S. Inactivation of General Acyl-CoA Dehydrogenase from Pig Kidney by a Metabolite of Hypoglycin A. J. Biol. Chem. 1981, 256, 9809-9812, 10.1016/S0021-9258(19)68697-7
Zeller, S.; Ghisla, H.-D. On the Inactivation of General Acyl-CoA Dehydrogenase from Pig Kidney by Methylenecyclopropyl-Acetyl-CoA, a Metabolite of Hypoglycin. In Flavins and Flavoproteins; De Gruyter, 1984; pp 447-450.
KRAUTH-SIEGEL, R. L.; SCHIRMER, R. H.; GHISLA, S. {FAD} Analogues as Prosthetic Groups of Human Glutathione Reductase. Properties of the Modified Enzyme Species and Comparisons with the Active Site Structure. Eur. J. Biochem. 1985, 148, 335-344, 10.1111/j.1432-1033.1985.tb08844.x
Varwell Marsh, M.; Caldwell, J.; Smith, R. L.; Horner, M. W.; Houghton, E.; Moss, M. S. Metabolic Conjugation of Some Carboxylic Acids in the Horse. Xenobiotica 1981, 11, 655-663, 10.3109/00498258109049085
Sander, J.; Terhardt, M.; Sander, S.; Janzen, N. Quantification of Methylenecyclopropyl Compounds and Acyl Conjugates by UPLC-MS/MS in the Study of the Biochemical Effects of the Ingestion of Canned Ackee (Blighia Sapida) and Lychee (Litchi Chinensis). J. Agric. Food Chem. 2017, 65, 2603-2608, 10.1021/acs.jafc.7b00224