A Urinary Metabolic Signature for Multiple Sclerosis and Neuromyelitis Optica

Journal of Proteome Research

Volumn 15, Issue 2, 2016, Pages 659-666

  Gebregiworgis, Teklab ^a   Nielsen, Helle H ^b   Massilamany, Chandirasegaran ^a   Gangaplara, Arunakumar ^a   Reddy, Jay ^a   Illes, Zsolt ^b   Powers, Robert ^a  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^b ODENSE UNIVERSITY HOSPITAL   (Denmark)

Author keywords

metabolomics; multiple sclerosis; multivariate statistics; neuromyelitis optica spectrum disorder; NMR; urine biomarkers

Indexed keywords

3 HYDROXYBUTYRIC ACID; AZATHIOPRINE; BIOLOGICAL MARKER; CREATININE; GLATIRAMER; HIPPURIC ACID; INTERFERON BETA SERINE; KETONE BODY; MALONIC ACID; NATALIZUMAB; OXALOACETIC ACID; PROPIONIC ACID; PYRUVIC ACID; TRICARBOXYLIC ACID; TRIMETHYLAMINE OXIDE;

AMINO ACID SYNTHESIS; ARTICLE; CITRIC ACID CYCLE; CLINICAL ARTICLE; DEGRADATION; ENERGY METABOLISM; FATTY ACID METABOLISM; GLYCOLYSIS; HUMAN; INTESTINE FLORA; KETOGENESIS; LIPID DEGRADATION; METABOLISM; METABOLITE; MITOCHONDRION; MULTIPLE SCLEROSIS; MYELOOPTIC NEUROPATHY; PRIORITY JOURNAL; URINALYSIS; ADULT; AGED; DIFFERENTIAL DIAGNOSIS; FEMALE; MALE; METABOLOME; METABOLOMICS; MIDDLE AGED; MULTIVARIATE ANALYSIS; NEUROMYELITIS OPTICA; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PROCEDURES; REPRODUCIBILITY; SENSITIVITY AND SPECIFICITY; URINE; YOUNG ADULT;

ADULT; AGED; BIOMARKERS; DIAGNOSIS, DIFFERENTIAL; FEMALE; HUMANS; MAGNETIC RESONANCE SPECTROSCOPY; MALE; METABOLOME; METABOLOMICS; MIDDLE AGED; MULTIPLE SCLEROSIS; MULTIVARIATE ANALYSIS; NEUROMYELITIS OPTICA; REPRODUCIBILITY OF RESULTS; SENSITIVITY AND SPECIFICITY; YOUNG ADULT;

EID: 84957710743     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/acs.jproteome.5b01111     Document Type: Article

References (43)

1. Sospedra, M.; Martin, R. Immunology of multiple sclerosis Annu. Rev. Immunol. 2005, 23, 683-747 10.1146/annurev.immunol.23.021704.115707
2. Trebst, C.; Jarius, S.; Berthele, A.; Paul, F.; Schippling, S.; Wildemann, B.; Borisow, N.; Kleiter, I.; Aktas, O.; Kumpfel, T. Update on the diagnosis and treatment of neuromyelitis optica: recommendations of the Neuromyelitis Optica Study Group (NEMOS) J. Neurol. 2014, 261 (1) 1-16 10.1007/s00415-013-7169-7
3. Wingerchuk, D. M.; Banwell, B.; Bennett, J. L.; Cabre, P.; Carroll, W.; Chitnis, T.; de Seze, J.; Fujihara, K.; Greenberg, B.; Jacob, A.; Jarius, S.; Lana-Peixoto, M.; Levy, M.; Simon, J. H.; Tenembaum, S.; Traboulsee, A. L.; Waters, P.; Wellik, K. E.; Weinshenker, B. G. International consensus diagnostic criteria for neuromyelitis optica spectrum disorders Neurology 2015, 85 (2) 177-89 10.1212/WNL.0000000000001729
4. Wingerchuk, D. M.; Lennon, V. A.; Pittock, S. J.; Lucchinetti, C. F.; Weinshenker, B. G. Revised diagnostic criteria for neuromyelitis optica Neurology 2006, 66 (10) 1485-9 10.1212/01.wnl.0000216139.44259.74
5. Carroll, W. M.; Saida, T.; Kim, H. J.; Kira, J.; Kermode, A. G.; Tsai, C. P.; Fujihara, K.; Kusunoki, S.; Tanaka, M.; Kim, K. K.; Bates, D. A guide to facilitate the early treatment of patients with idiopathic demyelinating disease (multiple sclerosis and neuromyelitis optica) Mult Scler 2013, 19 (10) 1371-80 10.1177/1352458512471092
6. Schnackenberg, L. K.; Beger, R. D. Metabolomic biomarkers: their role in the critical path Drug Discovery Today: Technol. 2007, 4 (1) 13-16 10.1016/j.ddtec.2007.10.012
7. Fiehn, O. Metabolomics - the link between genotypes and phenotypes Plant Mol. Biol. 2002, 48 (1-2) 155-71 10.1023/A:1013713905833
8. Kruger, N. J.; Troncoso-Ponce, M. A.; Ratcliffe, R. G. 1H NMR metabolite fingerprinting and metabolomic analysis of perchloric acid extracts from plant tissues Nat. Protoc. 2008, 3 (6) 1001-12 10.1038/nprot.2008.64
9. Gebregiworgis, T.; Powers, R. Application of NMR metabolomics to search for human disease biomarkers Comb. Chem. High Throughput Screening 2012, 15 (8) 595-610 10.2174/138620712802650522
10. Ray, P.; Manach, Y. L.; Riou, B.; Houle, T. T. Statistical evaluation of a biomarker Anesthesiology 2010, 112 (4) 1023-40 10.1097/ALN.0b013e3181d47604
11. Pisitkun, T.; Johnstone, R.; Knepper, M. A. Discovery of urinary biomarkers Mol. Cell. Proteomics 2006, 5 (10) 1760-1771 10.1074/mcp.R600004-MCP200
12. Powers, R. The current state of drug discovery and a potential role for NMR metabolomics J. Med. Chem. 2014, 57 (14) 5860-70 10.1021/jm401803b
13. Worley, B.; Powers, R. Multivariate analysis in metabolomics Curr. Metabolomics 2013, 1 (1) 92-107 10.2174/2213235X11301010092
14. Reinke, S. N.; Broadhurst, D. L.; Sykes, B. D.; Baker, G. B.; Catz, I.; Warren, K. G.; Power, C. Metabolomic profiling in multiple sclerosis: insights into biomarkers and pathogenesis Mult Scler 2014, 20 (10) 1396-400 10.1177/1352458513516528
15. Moussallieh, F. M.; Elbayed, K.; Chanson, J. B.; Rudolf, G.; Piotto, M.; De Seze, J.; Namer, I. J. Serum analysis by 1H nuclear magnetic resonance spectroscopy: a new tool for distinguishing neuromyelitis optica from multiple sclerosis Mult Scler 2014, 20 (5) 558-65 10.1177/1352458513504638
16. Dobson, R. Urine: An under-studied source of biomarkers in multiple sclerosis? Mult. Scler. Relat. Disord. 2012, 1 (2) 76-80 10.1016/j.msard.2012.01.002
17. Gebregiworgis, T.; Massilamany, C.; Gangaplara, A.; Thulasingam, S.; Kolli, V.; Werth, M. T.; Dodds, E. D.; Steffen, D.; Reddy, J.; Powers, R. Potential of urinary metabolites for diagnosing multiple sclerosis ACS Chem. Biol. 2013, 8 (4) 684-90 10.1021/cb300673e
18. Pandit, L.; Asgari, N.; Apiwattanakul, M.; Palace, J.; Leite, M. I.; Paul, F.; Kleiter, I.; Chitnis, T. Demographic and clinical features of neuromyelitis optica: A review Mult Scler 2015, 21 (7) 845-53 10.1177/1352458515572406
19. Polman, C. H.; Reingold, S. C.; Banwell, B.; Clanet, M.; Cohen, J. A.; Filippi, M.; Fujihara, K.; Havrdova, E.; Hutchinson, M.; Kappos, L.; Lublin, F. D.; Montalban, X.; O'Connor, P.; Sandberg-Wollheim, M.; Thompson, A. J.; Waubant, E.; Weinshenker, B.; Wolinsky, J. S. Diagnostic criteria for multiple sclerosis: 2010 revisions to the McDonald criteria Ann. Neurol. 2011, 69 (2) 292-302 10.1002/ana.22366
20. Worley, B.; Powers, R. MVAPACK: a complete data handling package for NMR metabolomics ACS Chem. Biol. 2014, 9 (5) 1138-44 10.1021/cb4008937
21. RCoreTeam R: A language and environment for statistical computing.; R Foundation for Statistical Computing: Vienna, Austria, 2013.
22. Miller, R. G. J. Simultaneous Statistical Inference; Springer-Verlag: New York, 1981; p 299.
23. Benjamini, Y.; Hochberg, Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing J. R. Stat. Soc. Series B Stat. Methodol. 1995, 57 (1) 289-300
24. Saccenti, E.; Hoefsloot, H. C. J.; Smilde, A. K.; Westerhuis, J. A.; Hendriks, M. M. W. B. Reflections on univariate and multivariate analysis of metabolomics data Metabolomics 2014, 10 (3) 361-374 10.1007/s11306-013-0598-6
25. Hecht, S. S. Human urinary carcinogen metabolites: biomarkers for investigating tobacco and cancer Carcinogenesis 2002, 23 (6) 907-922 10.1093/carcin/23.6.907
26. Dobson, R. Urine: an under-studied source of biomarkers in multiple sclerosis? Mult. Scler. Relat. Disord. 2012, 1 (2) 76-80 10.1016/j.msard.2012.01.002
27. Mathur, D.; Lopez-Rodas, G.; Casanova, B.; Marti, M. B. Perturbed glucose metabolism: insights into multiple sclerosis pathogenesis Front. Neurol. 2014, 5, 250 10.3389/fneur.2014.00250
28. Tavazzi, B.; Batocchi, A. P.; Amorini, A. M.; Nociti, V.; D'Urso, S.; Longo, S.; Gullotta, S.; Picardi, M.; Lazzarino, G. Serum metabolic profile in multiple sclerosis patients Mult. Scler. Int. 2011, 2011, 167156 10.1155/2011/167156
29. Mao, P.; Reddy, P. H. Is multiple sclerosis a mitochondrial disease? Biochim. Biophys. Acta, Mol. Basis Dis. 2010, 1802 (1) 66-79 10.1016/j.bbadis.2009.07.002
30. Witte, M. E.; Bo, L.; Rodenburg, R. J.; Belien, J. A.; Musters, R.; Hazes, T.; Wintjes, L. T.; Smeitink, J. A.; Geurts, J. J.; De Vries, H. E.; van der Valk, P.; van Horssen, J. Enhanced number and activity of mitochondria in multiple sclerosis lesions J. Pathol. 2009, 219 (2) 193-204 10.1002/path.2582
31. Yoon, H. J.; Kim, J. H.; Jeon, T. Y.; Yoo, S.-Y.; Eo, H. Devastating metabolic brain disorders of newborns and young infants Radiographics 2014, 34 (5) 1257-72 10.1148/rg.345130095
32. Wyss, M.; Kaddurah-Daouk, R. Creatine and creatinine metabolism Physiol. Rev. 2000, 80 (3) 1107-213
33. Matsuishi, T.; Stumpf, D. A.; Seliem, M.; Eguren, L. A.; Chrislip, K. Propionate mitochondrial toxicity in liver and skeletal muscle: acyl CoA levels Biochem. Med. Metab. Biol. 1991, 45 (2) 244-53 10.1016/0885-4505(91)90027-I
34. Fenton, W. A.; Gravel, R. A.; Rosenblatt, D. S. Disorders of Propionate and Methylmalonate Metabolism. In OMMBID-The Online Metabolic and Molecular Bases of Inherited Disease; Valle, D., Ed.; McGraw-Hill: New York, 2001; pp 2165-2193.
35. Corthals, A. P. Multiple sclerosis is not a disease of the immune system Q. Rev. Biol. 2011, 86 (4) 287-321 10.1086/662453
36. Collins, S. M.; Surette, M.; Bercik, P. The interplay between the intestinal microbiota and the brain Nat. Rev. Microbiol. 2012, 10 (11) 735-742 10.1038/nrmicro2876
37. Cantarel, B. L.; Waubant, E.; Chehoud, C.; Kuczynski, J.; DeSantis, T. Z.; Warrington, J.; Venkatesan, A.; Fraser, C. M.; Mowry, E. M. Gut Microbiota in Multiple Sclerosis: Possible Influence of Immunomodulators J. Invest. Med. 2015, 63 (5) 729-734 10.1097/JIM.0000000000000192
38. Williams, H. R.; Cox, I. J.; Walker, D. G.; Cobbold, J. F.; Taylor-Robinson, S. D.; Marshall, S. E.; Orchard, T. R. Differences in gut microbial metabolism are responsible for reduced hippurate synthesis in Crohn's disease BMC Gastroenterol. 2010, 10, 108 10.1186/1471-230X-10-108
39. Singh, V.; Stingl, C.; Stoop, M. P.; Zeneyedpour, L.; Neuteboom, R. F.; Smitt, P. S.; Hintzen, R. Q.; Luider, T. M. Proteomics Urine Analysis of Pregnant Women Suffering from Multiple Sclerosis J. Proteome Res. 2015, 14 (5) 2065-2073 10.1021/pr501162w
40. Vafaeyan, H.; Alavijeh, S. K.; Madadi, A.; Rad, H. S.; Faeghi, F.; Ebrahimzadeh, S. A.; Rahimian, N.; Harirchian, M. H. Quantification of diagnostic biomarkers to detect multiple sclerosis lesions employing (1)H-MRSI at 3T Australas. Phys. Eng. Sci. Med. 2015, 38, 611 10.1007/s13246-015-0390-1
41. Kroksveen, A. C.; Jaffe, J. D.; Aasebo, E.; Barsnes, H.; Bjorlykke, Y.; Franciotta, D.; Keshishian, H.; Myhr, K.-M.; Opsahl, J. A.; van Pesch, V.; Teunissen, C. E.; Torkildsen, O.; Ulvik, R. J.; Vethe, H.; Carr, S. A.; Berven, F. S. Quantitative proteomics suggests decrease in the secretogranin-1 cerebrospinal fluid levels during the disease course of multiple sclerosis Proteomics 2015, 15 (19) 3361-3369 10.1002/pmic.201400142
42. Jurynczyk, M.; Leite, I.; Palace, J.; Selmaj, K.; Weinshenker, B.; Akman-Demir, G.; Asgari, N.; Barnes, D.; Wren, D.; Boggild, M.; Chaudhuri, A.; D'Hooghe, M.; Evangelou, N.; Tanasescu, R.; Geraldes, R.; Illes, Z.; Jacob, A.; Kim, H. J.; Kleiter, I.; Levy, M.; Marignier, R.; Vukusic, S.; McGuigan, C.; Murray, K.; Nakashima, I.; Pandit, L.; Paul, F.; Pittock, S.; de Seze, J.; Siva, A.; Wingerchuk, D. Status of diagnostic approaches to AQP4-IgG seronegative NMO and NMO/MS overlap syndromes J. Neurol. 2016, 263, 140 10.1007/s00415-015-7952-8
43. Tremlett, H.; Dai, D. L. Y.; Hollander, Z.; Kapanen, A.; Aziz, T.; Wilson-McManus, J. E.; Tebbutt, S. J.; Borchers, C. H.; Oger, J.; Cohen Freue, G. V. Serum proteomics in multiple sclerosis disease progression J. Proteomics 2015, 118, 2-11 10.1016/j.jprot.2015.02.018