Metabolic phenotyping of the Crohn's disease-like IBD etiopathology in the TNF ΔARE/WT mouse model

Journal of Proteome Research

Volumn 10, Issue 12, 2011, Pages 5523-5535

  Baur, Pia ^a   Martin, François Pierre ^b   Gruber, Lisa ^a   Bosco, Nabil ^b   Brahmbhatt, Viral ^b   Collino, Sebastiano ^b   Guy, Philippe ^b   Montoliu, Ivan ^b   Rozman, Jan ^a   Klingenspor, Martin ^a   Tavazzi, Isabelle ^b   Thorimbert, Anita ^b   Rezzi, Serge ^b   Kochhar, Sunil ^b   Benyacoub, Jalil ^b   Kollias, George ^c   Haller, Dirk ^a  

^a TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^b NESTLÉ RESEARCH CENTER   (Switzerland)

^c BIOMEDICAL SCIENCES RESEARCH CENTER ALEXANDER FLEMING   (Greece)

Author keywords

chemometrics; Crohn's disease (CD); inflammatory bowel disease (IBD); LC MS; lipid metabolism; metabonomics; nuclear magnetic resonance (NMR) spectroscopy; tumor necrosis factor (TNF)

Indexed keywords

CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12P70; INTERLEUKIN 1BETA; INTERLEUKIN 6; KERATINOCYTE DERIVED CHEMOKINE; TUMOR NECROSIS FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY COMPOSITION; CHEMOMETRICS; CROHN DISEASE; ENTERITIS; HISTOLOGY; ILEITIS; ISOTOPE DILUTION ASSAY; LIPID METABOLISM; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; METABONOMICS; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; SCORING SYSTEM;

ADIPOSE TISSUE; ANIMALS; BODY COMPOSITION; CELL MEMBRANE; CHROMATOGRAPHY, LIQUID; CROHN DISEASE; DISEASE MODELS, ANIMAL; ENERGY METABOLISM; ILEITIS; INFLAMMATION MEDIATORS; INFLAMMATORY BOWEL DISEASES; LIPID METABOLISM; MAGNETIC RESONANCE SPECTROSCOPY; MASS SPECTROMETRY; METABOLOME; METABOLOMICS; MICE; MICE, INBRED C57BL; PHENOTYPE; TUMOR NECROSIS FACTOR-ALPHA; WEIGHT LOSS;

EID: 82755181915     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr2007973     Document Type: Article

References (56)

1. Kaser, A.; Zeissig, S.; Blumberg, R. S. Inflammatory bowel disease Annu. Rev. Immunol. 2010, 28, 573-621
2. Xavier, R. J.; Podolsky, D. K. Unravelling the pathogenesis of inflammatory bowel disease Nature 2007, 448 (7152) 427-34 (Pubitemid 47123518)
3. Cho, J. H.; Brant, S. R. Recent insights into the genetics of inflammatory bowel disease Gastroenterology 2011, 140 (6) 1704-12 e2
4. Clavel, T.; Haller, D. Molecular interactions between bacteria, the epithelium, and the mucosal immune system in the intestinal tract: implications for chronic inflammation Curr. Issues Intest. Microbiol. 2007, 8 (2) 25-43 (Pubitemid 46784297)
5. McGuckin, M. A.; Eri, R.; Simms, L. A.; Florin, T. H.; Radford-Smith, G. Intestinal barrier dysfunction in inflammatory bowel diseases Inflamm. Bowel Dis. 2009, 15 (1) 100-13
6. Shkoda, A.; Ruiz, P. A.; Daniel, H.; Kim, S. C.; Rogler, G.; Sartor, R. B.; Haller, D. Interleukin-10 blocked endoplasmic reticulum stress in intestinal epithelial cells: impact on chronic inflammation Gastroenterology 2007, 132 (1) 190-207 (Pubitemid 46108743)
7. Mizoguchi, A.; Mizoguchi, E. Inflammatory bowel disease, past, present and future: lessons from animal models J. Gastroenterol. 2008, 43 (1) 1-17 (Pubitemid 351324980)
8. Wirtz, S.; Neurath, M. F. Mouse models of inflammatory bowel disease Adv. Drug Delivery Rev. 2007, 59 (11) 1073-83 (Pubitemid 47615208)
9. Sartor, R. B. Review article: How relevant to human inflammatory bowel disease are current animal models of intestinal inflammation? Aliment. Pharmacol. Ther. 1997, 11 (Suppl 3) 89-96; discussion 96-7
10. Pizarro, T. T.; Arseneau, K. O.; Bamias, G.; Cominelli, F. Mouse models for the study of Crohn's disease Trends Mol. Med. 2003, 9 (5) 218-22 (Pubitemid 36713392)
11. Scaldaferri, F.; Correale, C.; Gasbarrini, A.; Danese, S. Mucosal biomarkers in inflammatory bowel disease: key pathogenic players or disease predictors? World J. Gastroenterol. 2010, 16 (21) 2616-25
12. Cosnes, J. Can we modulate the clinical course of inflammatory bowel diseases by our current treatment strategies? Dig Dis 2009, 27 (4) 516-21
13. Kontoyiannis, D.; Pasparakis, M.; Pizarro, T. T.; Cominelli, F.; Kollias, G. Impaired on/off regulation of TNF biosynthesis in mice lacking TNF AU-rich elements: implications for joint and gut-associated immunopathologies Immunity 1999, 10 (3) 387-98 (Pubitemid 29165293)
14. Apostolaki, M.; Manoloukos, M.; Roulis, M.; Wurbel, M. A.; Muller, W.; Papadakis, K. A.; Kontoyiannis, D. L.; Malissen, B.; Kollias, G. Role of beta7 integrin and the chemokine/chemokine receptor pair CCL25/CCR9 in modeled TNF-dependent Crohn's disease Gastroenterology 2008, 134 (7) 2025-35 (Pubitemid 351790742)
15. Kussmann, M.; Rezzi, S.; Daniel, H. Profiling techniques in nutrition and health research Curr. Opin. Biotechnol. 2008, 19 (2) 83-99
16. Nicholson, J. K.; Lindon, J. C.; Holmes, E. 'Metabonomics': understanding the metabolic responses of living systems to pathophysiological stimuli via multivariate statistical analysis of biological NMR spectroscopic data Xenobiotica 1999, 29 (11) 1181-9
17. Bjerrum, J. T.; Nielsen, O. H.; Wang, Y. L.; Olsen, J. Technology insight: metabonomics in gastroenterology-basic principles and potential clinical applications Nat. Clin. Pract. Gastroenterol. Hepatol. 2008, 5 (6) 332-43 (Pubitemid 351803604)
18. Martin, F. P.; Wang, Y.; Yap, I. K.; Sprenger, N.; Lindon, J. C.; Rezzi, S.; Kochhar, S.; Holmes, E.; Nicholson, J. K. Topographical variation in murine intestinal metabolic profiles in relation to microbiome speciation and functional ecological activity J. Proteome Res. 2009, 8 (7) 3464-74
19. Martin, F. P.; Montoliu, I.; Kochhar, S.; Rezzi, S. Chemometric strategy for modeling metabolic biological space along the gastrointestinal tract and assessing microbial influences Anal. Chem. 2010, 82 (23) 9803-11
20. Williams, H. R.; Cox, I. J.; Walker, D. G.; North, B. V.; Patel, V. M.; Marshall, S. E.; Jewell, D. P.; Ghosh, S.; Thomas, H. J.; Teare, J. P.; Jakobovits, S.; Zeki, S.; Welsh, K. I.; Taylor-Robinson, S. D.; Orchard, T. R. Characterization of inflammatory bowel disease with urinary metabolic profiling Am. J. Gastroenterol. 2009, 104 (6) 1435-44
21. Marchesi, J. R.; Holmes, E.; Khan, F.; Kochhar, S.; Scanlan, P.; Shanahan, F.; Wilson, I. D.; Wang, Y. Rapid and noninvasive metabonomic characterization of inflammatory bowel disease J. Proteome Res. 2007, 6 (2) 546-51 (Pubitemid 46340158)
22. Bezabeh, T.; Somorjai, R. L.; Smith, I. C. MR metabolomics of fecal extracts: applications in the study of bowel diseases Magn. Reson. Chem. 2009, 47 (Suppl 1) S54-61
23. Martin, F. P.; Rezzi, S.; Philippe, D.; Tornier, L.; Messlik, A.; Holzlwimmer, G.; Baur, P.; Quintanilla-Fend, L.; Loh, G.; Blaut, M.; Blum, S.; Kochhar, S.; Haller, D. Metabolic assessment of gradual development of moderate experimental colitis in IL-10 deficient mice J. Proteome Res. 2009, 8 (5) 2376-87
24. Schicho, R.; Nazyrova, A.; Shaykhutdinov, R.; Duggan, G.; Vogel, H. J.; Storr, M. Quantitative metabolomic profiling of serum and urine in DSS-induced ulcerative colitis of mice by (1)H NMR spectroscopy J. Proteome Res. 2010, 9 (12) 6265-73
25. Murdoch, T. B.; Fu, H.; MacFarlane, S.; Sydora, B. C.; Fedorak, R. N.; Slupsky, C. M. Urinary metabolic profiles of inflammatory bowel disease in interleukin-10 gene-deficient mice Anal. Chem. 2008, 80 (14) 5524-31
26. Lin, H. M.; Barnett, M. P.; Roy, N. C.; Joyce, N. I.; Zhu, S.; Armstrong, K.; Helsby, N. A.; Ferguson, L. R.; Rowan, D. D. Metabolomic analysis identifies inflammatory and noninflammatory metabolic effects of genetic modification in a mouse model of Crohn's disease J. Proteome Res. 2010, 9 (4) 1965-75
27. Otter, D.; Cao, M.; Lin, H. M.; Fraser, K.; Edmunds, S.; Lane, G.; Rowan, D. Identification of urinary biomarkers of colon inflammation in IL10-/- mice using Short-Column LCMS metabolomics J. Biomed. Biotechnol. 2011, 974701
28. Balasubramanian, K.; Kumar, S.; Singh, R. R.; Sharma, U.; Ahuja, V.; Makharia, G. K.; Jagannathan, N. R. Metabolism of the colonic mucosa in patients with inflammatory bowel diseases: an in vitro proton magnetic resonance spectroscopy study Magn. Reson. Imaging 2009, 27 (1) 79-86
29. Sharma, U.; Singh, R. R.; Ahuja, V.; Makharia, G. K.; Jagannathan, N. R. Similarity in the metabolic profile in macroscopically involved and un-involved colonic mucosa in patients with inflammatory bowel disease: an in vitro proton ((1)H) MR spectroscopy study Magn. Reson. Imaging 2010, 28 (7) 1022-9
30. Shiomi, Y.; Nishiumi, S.; Ooi, M.; Hatano, N.; Shinohara, M.; Yoshie, T.; Kondo, Y.; Furumatsu, K.; Shiomi, H.; Kutsumi, H.; Azuma, T.; Yoshida, M. GCMS-based metabolomic study in mice with colitis induced by dextran sulfate sodium Inflamm. Bowel Dis. 2011, 17 (11) 2261-74
31. Buhner, S.; Nagel, E.; Korber, J.; Vogelsang, H.; Linn, T.; Pichlmayr, R. Ileal and colonic fatty acid profiles in patients with active Crohn's disease Gut 1994, 35 (10) 1424-8 (Pubitemid 24310905)
32. Morita, H.; Nakanishi, K.; Dohi, T.; Yasugi, E.; Oshima, M. Phospholipid turnover in the inflamed intestinal mucosa: arachidonic acid-rich phosphatidyl/plasmenyl-ethanolamine in the mucosa in inflammatory bowel disease J. Gastroenterol. 1999, 34 (1) 46-53 (Pubitemid 29112335)
33. Katakura, K.; Lee, J.; Rachmilewitz, D.; Li, G.; Eckmann, L.; Raz, E. Toll-like receptor 9-induced type I IFN protects mice from experimental colitis J. Clin. Invest. 2005, 115 (3) 695-702 (Pubitemid 40322244)
34. Folch, J.; Lees, M.; Sloane Stanley, G. H. A simple method for the isolation and purification of total lipides from animal tissues J. Biol. Chem. 1957, 226 (1) 497-509
35. Siddiqui, N.; Sim, J.; Silwood, C. J.; Toms, H.; Iles, R. A.; Grootveld, M. Multicomponent analysis of encapsulated marine oil supplements using high-resolution 1H and 13C NMR techniques J. Lipid Res. 2003, 44 (12) 2406-27 (Pubitemid 38082500)
36. Oostendorp, M.; Engelke, U. F.; Willemsen, M. A.; Wevers, R. A. Diagnosing inborn errors of lipid metabolism with proton nuclear magnetic resonance spectroscopy Clin. Chem. 2006, 52 (7) 1395-405 (Pubitemid 43956033)
37. Römisch-Margl, W.; Prehn, C.; Bogumil, R.; Röhring, C.; Suhre, K.; Adamski, J. Procedure for tissue sample preparation and metabolite extraction for high-throughput targeted metabolomics. Metabolomics 2011, (doi:10.1007/s11306-011-0293-4).
38. Deems, R.; Buczynski, M. W.; Bowers-Gentry, R.; Harkewicz, R.; Dennis, E. A. Detection and quantitation of eicosanoids via high performance liquid chromatography-electrospray ionization-mass spectrometry Methods Enzymol. 2007, 432, 59-82
39. Trygg, J. O2-PLS for qualitative and quantitative analysis in multivariate calibration J. Chemom. 2002, 17, 53-64
40. Wiklund, S.; Johansson, E.; Sjostrom, L.; Mellerowicz, E. J.; Edlund, U.; Shockcor, J. P.; Gottfries, J.; Moritz, T.; Trygg, J. Visualization of GC/TOF-MS-based metabolomics data for identification of biochemically interesting compounds using OPLS class models Anal. Chem. 2008, 80 (1) 115-22 (Pubitemid 351448411)
41. Fisher, R. L. Wasting in chronic gastrointestinal diseases J. Nutr. 1999, 129 (1S Suppl) 252S-255S (Pubitemid 29035985)
42. Filipsson, S.; Hulten, L.; Lindstedt, G. Malabsorption of fat and vitamin B12 before and after intestinal resection for Crohn's disease Scand. J. Gastroenterol. 1978, 13 (5) 529-36 (Pubitemid 9003930)
43. Huybers, S.; Apostolaki, M.; van der Eerden, B. C.; Kollias, G.; Naber, T. H.; Bindels, R. J.; Hoenderop, J. G. Murine TNF(DeltaARE) Crohn's disease model displays diminished expression of intestinal Ca2+ transporters Inflamm. Bowel Dis. 2008, 14 (6) 803-11 (Pubitemid 351898065)
44. Bannerman, E.; Davidson, I.; Conway, C.; Culley, D.; Aldhous, M. C.; Ghosh, S. Altered subjective appetite parameters in Crohn's disease patients Clin. Nutr. 2001, 20 (5) 399-405 (Pubitemid 32916043)
45. Calder, P. C. Polyunsaturated fatty acids, inflammatory processes and inflammatory bowel diseases Mol. Nutr. Food Res. 2008, 52 (8) 885-97
46. Lambert, D.; O'Neill, C. A.; Padfield, P. J. Depletion of Caco-2 cell cholesterol disrupts barrier function by altering the detergent solubility and distribution of specific tight-junction proteins Biochem. J. 2005, 387 (Pt 2) 553-60 (Pubitemid 40571242)
47. Innis, S. M.; Dai, C.; Wu, X.; Buchan, A.M.; Jacobson, K. Perinatal lipid nutrition alters early intestinal development and programs the response to experimental colitis in young adult rats Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 299 (6) G1376-85
48. Li, Q.; Zhang, Q.; Wang, M.; Zhao, S.; Ma, J.; Luo, N.; Li, N.; Li, Y.; Xu, G.; Li, J. Interferon-gamma and tumor necrosis factor-alpha disrupt epithelial barrier function by altering lipid composition in membrane microdomains of tight junction Clin. Immunol. 2008, 126 (1) 67-80 (Pubitemid 350266450)
49. Rocha, R.; Santana, G. O.; Almeida, N.; Lyra, A. C. Analysis of fat and muscle mass in patients with inflammatory bowel disease during remission and active phase Br. J. Nutr. 2009, 101 (5) 676-9
50. Al-Jaouni, R.; Hebuterne, X.; Pouget, I.; Rampal, P. Energy metabolism and substrate oxidation in patients with Crohn's disease Nutrition 2000, 16 (3) 173-8 (Pubitemid 30114269)
51. Mingrone, G.; Greco, A. V.; Benedetti, G.; Capristo, E.; Semeraro, R.; Zoli, G.; Gasbarrini, G. Increased resting lipid oxidation in Crohn's disease Dig. Dis. Sci. 1996, 41 (1) 72-6 (Pubitemid 26064843)
52. Peyrin-Biroulet, L.; Chamaillard, M.; Gonzalez, F.; Beclin, E.; Decourcelle, C.; Antunes, L.; Gay, J.; Neut, C.; Colombel, J. F.; Desreumaux, P. Mesenteric fat in Crohn's disease: a pathogenetic hallmark or an innocent bystander? Gut 2007, 56 (4) 577-83 (Pubitemid 46580516)
53. Lee, C. W.; Lin, C. C.; Lee, I. T.; Lee, H. C.; Yang, C. M. Activation and induction of cytosolic phospholipase a(2) by TNF-alpha mediated through Nox2, MAPKs, NF-kappa B, and p300 in human tracheal smooth muscle cells J. Cell Physiol. 2010, 226 (8) 2103-2114
54. Hawkey, C. J.; Karmeli, F.; Rachmilewitz, D. Imbalance of prostacyclin and thromboxane synthesis in Crohn's disease Gut 1983, 24 (10) 881-5 (Pubitemid 13009570)
55. Sjoqvist, U.; Hertervig, E.; Nilsson, A.; Duan, R. D.; Ost, A.; Tribukait, B.; Lofberg, R. Chronic colitis is associated with a reduction of mucosal alkaline sphingomyelinase activity Inflamm. Bowel Dis. 2002, 8 (4) 258-63 (Pubitemid 34784978)
56. Bjerrum, J. T.; Nielsen, O. H.; Hao, F.; Tang, H.; Nicholson, J. K.; Wang, Y.; Olsen, J. Metabonomics in ulcerative colitis: diagnostics, biomarker identification, and insight into the pathophysiology J. Proteome Res. 2010, 9 (2) 954-62