Detection of metabolic alterations in non-tumor gastrointestinal tissue of the ApcMin/+ mouse by1H mas NMR spectroscopy

Journal of Proteome Research

Volumn 8, Issue 3, 2009, Pages 1423-1430

  Backshall, Alexandra ^a   Alferez, Denis ^b   Teichert, Friederike ^c   Wilson, Ian D ^d   Wilkinson, Robert W ^d   Goodlad, Robert A ^b,e   Keun, Hector C ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^c UNIVERSITY OF LEICESTER   (United Kingdom)

^d ASTRAZENECA   (United Kingdom)

^e HAMMERSMITH HOSPITAL   (United Kingdom)

Author keywords

Aberrant crypt; APC; Colorectal cancer; Familial adenomatous polyposis; Field cancerization; Gastrointestinal cancer; Metabolomics; Metabonomics; Min mouse

Indexed keywords

APC PROTEIN; DIMETHYLAMINE; GLYCEROPHOSPHORYLCHOLINE; INOSITOL; LACTIC ACID; PHOSPHATIDYLCHOLINE; PHOSPHOLIPASE A2; PHOSPHORYLCHOLINE;

ADENOMATOUS POLYP; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CARCINOGENESIS; COLORECTAL CANCER; CONTROLLED STUDY; EPITHELIUM CELL; FEMALE; GASTROINTESTINAL TRACT; GENETIC VARIABILITY; IMMUNE SYSTEM; INTESTINE BIOPSY; LAMINA PROPRIA; MASS SPECTROMETRY; METABOLIC DISORDER; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; TUMOR SUPPRESSOR GENE; TUMOR VOLUME; WILD TYPE;

ADENOMATOUS POLYPOSIS COLI PROTEIN; ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; COLON; DIMETHYLAMINES; EPITHELIAL CELLS; GASTROINTESTINAL NEOPLASMS; INOSITOL; INTESTINE, SMALL; LACTIC ACID; MAGNETIC RESONANCE SPECTROSCOPY; METABOLOMICS; MICE; MICE, INBRED C57BL; MUCOUS MEMBRANE; PHOSPHORYLCHOLINE; PRECANCEROUS CONDITIONS;

ANIMALIA; MUS;

EID: 65249128032     PISSN: 15353893     EISSN: None     Source Type: Journal    
DOI: 10.1021/pr800793w     Document Type: Article

References (47)

1. Ilyas, M.; Straub, J.; Tomlinson, I. P.; Bodmer, W. F. Genetic pathways in colorectal and other cancers. Eur. J. Cancer 1999, 35 (14), 1986-2002.
2. Fodde, R.; Smits, R.; Clevers, H. APC, signal transduction and genetic instability in colorectal cancer. Nat. Rev. Cancer 2001, 1 (1), 55-67.
3. Fodde, R.; Smits, R. Disease model: familial adenomatous polyposis. Trends Mol. Med. 2001, 7 (8), 369-73.
4. Moser, A. R.; Pitot, H. C.; Dove, W. F. A dominant mutation that predisposes to multiple intestinal neoplasia in the mouse. Science 1990, 247 (4940), 322-4.
5. Shoemaker, A. R.; Gould, K. A.; Luongo, C.; Moser, A. R.; Dove, W. F. Studies of neoplasia in the Min mouse. Biochim. Biophys. Acta 1997, 1332 (2), F25-48.
6. Aoki, K.; Taketo, M. M. Adenomatous polyposis coli (APC): a multifunctional tumor suppressor gene. J. Cell Sci. 2007, 120 (Pt 19),3327-35.
7. Clarke, A. R. Wnt signalling in the mouse intestine. Oncogene 2006, 25 (57), 7512-21.
8. Beckonert, O.; Keun, H. C.; Ebbels, T. M. D.; Bundy, J.; Holmes, E.; Lindon, J. C.; Nicholson, J. K. Metabolic profiling, metabolomic and metabonomic procedures for NMR spectroscopy of urine, plasma, serum and tissue extracts. Nat. Protocols 2007, 2 (11), 2692-2703.
9. Fan, T. W.-M. Metabolite profiling by one- and two-dimensional NMR analysis of complex mixtures. Prog. Nucl. Magn. Reson. Spectrosc. 1996, 28 (2), 161-219.
10. 13C NMR spectroscopy of human blood plasma. Anal. Chem. 1995, 67 (5), 793-811.
11. 1H NMR spectroscopy of human blood plasma. Prog. Nucl. Magn. Reson. Spectrosc. 1995, 27 (5-6), 475-554.
12. Griffin, J. L.; Kauppinen, R. A. Tumour metabolomics in animal models of human cancer. J. Proteome Res. 2007, 6 (2), 498-505.
13. Teichert, F.; Verschoyle, R. D.; Greaves, P.; Edwards, R. E.; Teahan, O.; Jones, D. J.; Wilson, I. D.; Farmer, P. B.; Steward, W. P.; Gant, T. W.; Gescher, A. J.; Keun, H. C. Metabolic profiling of transgenic adenocarcinoma of mouse prostate (TRAMP) Tissue by (1)H-NMR analysis: evidence for unusual phospholipid metabolism. Prostate 2008, 68 (10), 1035-47.
14. Liotta, L. A.; Kohn, E. C. The microenvironment of the tumour- host interface. Nature 2001, 411 (6835), 375-9.
15. Gatenby, R. A.; Gillies, R. J. Why do cancers have high aerobic glycolysis. Nat. Rev. Cancer 2004, 4 (11), 891-9.
16. Braakhuis, B. J. M.; Tabor, M. P.; Kummer, J. A.; Leemans, C. R.; Brakenhoff, R. H. A Genetic Explanation of Slaughter's Concept of Field Cancerization: Evidence and Clinical Implications. Cancer Res. 2003, 63 (8), 1727-1730.
17. Nicholson, J. K.; Holmes, E.; Wilson, I. D. Gut microorganisms, mammalian metabolism and personalized health care. Nat. Rev. Microbiol. 2005, 3 (5), 431-8.
18. 1H NMR spectroscopy and multivariate data analysis. J. Proteome Res. 2005, 4 (4), 13249.
19. Wang, Y.; Cloarec, O.; Tang, H.; Lindon, J. C.; Holmes, E.; Kochhar, S.; Nicholson, J. K. Magic Angle Spinning NMR and (1)H-(31)P Heteronuclear Statistical Total Correlation Spectroscopy of Intact Human Gut Biopsies. Anal. Chem. 2008, 80 (4), 1058-1066.
20. 1H NMR spectroscopy. J. Proteome Res. 2007, 6 (10), 3944-51.
21. Tugnoli, V.; Mucci, A.; Schenetti, L.; Righi, V.; Calabrese, C.; Fabbri, A.; Di Febo, G.; Tosi, M. R. Ex vivo HR-MAS Magnetic Resonance Spectroscopy of human gastric adenocarcinomas: a comparison with healthy gastric mucosa. Oncol. Rep. 2006, 16 (3), 543-53.
22. 1H NMR spectroscopy of colon tumors and normal mucosal biopsies; elevated taurine levels and reduced polyethyleneglycol absorption in tumors may have diagnostic significance. NMR Biomed. 1993, 6 (2), 111-8.
23. M[nl+ mouse model of early intestinal cancer. Carcinogenesis 2006, 27 (10), 2133-9.
24. Rudling, R.; Hassan, A. B.; Kitau, J.; Mandir, N.; Goodlad, R. A. A simple device to rapidly prepare whole mounts of murine intestine. CellProlif. 2006, 39 (5), 415-20.
25. Dieterle, F.; Ross, A.; Schlotterbeck, G.; Senn, H. Probabilistic quotient normalization as robust method to account for dilution of complex biological mixtures. Application in 1H NMR metabo- nomics. Anal. Chem. 2006, 78 (13), 4281-90.
26. Westerhuis, J. Assessment of PLSDA cross validation. Metabolomics 2008, 4 (1), 81-89.
27. Alferez, D.; Goodlad, R. A. To best measure cell proliferation in samples from the intestine. Cell Prolif. 2007, 40 (2), 231-40.
28. Orner, G. A.; Dashwood, W. M.; Blum, C. A.; Diaz, G. D.; Li, Q.; AlFageeh, M.; Tebbutt, N.; Heath, J. K.; Ernst, M.; Dashwood, R. H. Response of Apc(min) and A33 (delta N beta-cat) mutant mice to treatment with tea, sulindac, and 2-amino-1-methyl-6-phenylimi- dazo[4,5-b]pyridine (PhIP). Mutat. Res. 2002, 506-507, 121-7.
29. Swanson, M. G.; Zektzer, A. S.; Tabatabai, Z. L.; Simko, J.; Jarso, S.; Keshari, K. R.; Schmitt, L.; Carroll, P. R.; Shinohara, K.; Vigneron, D. B.; Kurhanewicz, J. Quantitative analysis of prostate metabolites using 1H HR-MAS spectroscopy. Magn. Reson. Med. 2006, 55 (6), 1257-64.
30. Halestrap, A. P.; Price, N. T. The proton-linked monocarboxylate transporter (MCT) family: structure, function and regulation. Biochem. J. 1999, 343 Pt 2, 281-99.
31. Ackerstaff, E.; Glunde, K.; Bhujwalla, Z. M. Choline phospholipid metabolism: a target in cancer cells. J. Cell Biochem. 2003, 90 (3), 525-33.
32. Glunde, K.; Jacobs, M. A.; Bhujwalla, Z. M. Choline metabolism in cancer: implications for diagnosis and therapy. Expert Rev. Mol. Diagn. 2006, 6 (6), 821-9.
33. Podo, F. Tumour phospholipid metabolism. NMR Biomed. 1999, 12 (7), 413-39.
34. Glunde, K.; Jie, C.; Bhujwalla, Z. M. Molecular causes of the aberrant choline phospholipid metabolism in breast cancer. Cancer Res. 2004, 64 (12), 4270-6.
35. Iorio, E.; Mezzanzanica, D.; Alberti, P.; Spadaro, F.; Ramoni, C.; D'Ascenzo, S.; Millimaggi, D.; Pavan, A.; Dolo, V.; Canevari, S.; Podo, F. Alterations of choline phospholipid metabolism in ovarian tumor progression. Cancer Res. 2005, 65 (20), 9369-76.
36. Chan, E. C. Y.; Koh, P. K.; Mal, M.; Cheah, P. Y.; Eu, K. W.; Backshall, A.; Cavill, R.; Nicholson, J. K.; Keun, H. C. Metabolic profiling of human colorectal cancer using high-resolution magic angle spinning nuclear magnetic resonance (HR-MAS NMR) spectroscopy and gas chromatography mass spectrometry (GClMS). J. Proteome Res. 2008, 10.1021lpr8006232.
37. Nakagami, K.; Uchida, T.; Ohwada, S.; Koibuchi, Y.; Suda, Y.; Sekine, T.; Morishita, Y. Increased choline kinase activity and elevated phosphocholine levels in human colon cancer. Jpn. J. Cancer Res. 1999, 90 (4), 419-24.
38. Minl+ Mom1S mice. Proc. Natl. Acad. Sci. U.S.A. 2005, 102 (8), 2868-73.
39. MacPhee, M.; Chepenik, K. P.; Liddell, R. A.; Nelson, K. K.; Siracusa, L. D.; Buchberg, A. M. The secretory phospholipase A2 gene is a candidate for the Mom1 locus, a major modifier of ApcMin- induced intestinal neoplasia. Cell 1995, 81 (6), 957-66.
40. Zeisel, S. H.; daCosta, K. A.; Youssef, M.; Hensey, S. Conversion of Dietary Choline to Trimethylamine and Dimethylamine in Rats: Dose-Response Relationship. J. Nutr. 1989, 119 (5), 800-804.
41. al-Waiz, M.; Mikov, M.; Mitchell, S. C.; Smith, R. L. The exogenous origin of trimethylamine in the mouse. Metabolism 1992, 41 (2), 135-6.
42. Chen, L. C.; Hao, C. Y.; Chiu, Y. S.; Wong, P.; Melnick, J. S.; Brotman, M.; Moretto, J.; Mendes, F.; Smith, A. P.; Bennington, J. L.; Moore, D.; Lee, N. M. Alteration of gene expression in normal- appearing colon mucosa of APC(min) mice and human cancer patients. Cancer Res. 2004, 64 (10), 3694-700.
43. Hull, M. A.; Booth, J. K.; Tisbury, A.; Scott, N.; Bonifer, C.; Markham, A. F.; Coletta, P. L. Cyclooxygenase 2 is up-regulated and localized to macrophages in the intestine of Min mice. Br. J. Cancer 1999, 79 (9-10), 1399-405.
44. Inaba, T.; Sano, H.; Kawahito, Y.; Hla, T.; Akita, K.; Toda, M.; Yamashina, I.; Inoue, M.; Nakada, H. Induction of cyclooxyge- nase-2 in monocyte/macrophage by mucins secreted from colon cancer cells. Proc. Natl. Acad. Sci. U.S.A. 2003, 100 (5), 2736-41.
45. Min mice is associated with only regional effects on tumori- genesis. Carcinogenesis 2008, 29, 1825-1830.
46. Lamlum, H.; Papadopoulou, A.; Ilyas, M.; Rowan, A.; Gillet, C.; Hanby, A.; Talbot, I.; Bodmer, W.; Tomlinson, I. APC mutations are sufficient for the growth of early colorectal adenomas. Proc. Natl. Acad. Sci. U.S.A. 2000, 97 (5), 2225-8.
47. Humphries, A.; Wright, N. A. Colonic crypt organization and tumorigenesis. Nat. Rev. Cancer 2008, 8 (6), 415-24.