NMR metabolomics analysis of the effects of 5-lipoxygenase inhibitors on metabolism in glioblastomas

Journal of Proteome Research

Volumn 12, Issue 5, 2013, Pages 2165-2176

  Morin, Pier Jr ^a   Ferguson, Dean ^a   Leblanc, Luc M ^a   Hébert, Martin J G ^a   Paré, Aurélie F ^a   Jean François, Jacques ^a   Surette, Marc E ^a   Touaibia, Mohamed ^a   Cuperlovic Culf, Miroslava ^a,b  

^a UNIVERSITÉ DE MONCTON   (Canada)

^b NATIONAL RESEARCH COUNCIL CANADA   (Canada)

Author keywords

5 lipoxygenase inhibitors; Antioxidant and antiradical activity; Caffeic acid phenethyl ester; Drug discovery; Glioblastoma multiforme; NMR Metabolomics

Indexed keywords

CAFFEIC ACID; CAFFEIC ACID CYCLOHEXETHYL ESTER; CAFFEIC ACID PHENETHYL ESTER; LIPOXYGENASE INHIBITOR; UNCLASSIFIED DRUG; ZILEUTON;

ANTIOXIDANT ACTIVITY; ARTICLE; CANCER CELL CULTURE; DRUG MECHANISM; GLIOBLASTOMA; HIGH THROUGHPUT SCREENING; METABOLISM; METABOLOMICS; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL;

ANTINEOPLASTIC AGENTS; ARACHIDONATE 5-LIPOXYGENASE; CAFFEIC ACIDS; CELL LINE, TUMOR; DRUG SCREENING ASSAYS, ANTITUMOR; FREE RADICAL SCAVENGERS; GLIOBLASTOMA; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; HYDROXYUREA; LEUKOTRIENES; LIPID METABOLISM; LIPOXYGENASE INHIBITORS; MAGNETIC RESONANCE SPECTROSCOPY; METABOLOME; METABOLOMICS; PHENYLETHYL ALCOHOL; PRINCIPAL COMPONENT ANALYSIS;

EID: 84877104135     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr400026q     Document Type: Article

References (46)

1. Kanu, O. O.; Mehta, A.; Di, C.; Lin, N.; Bortoff, K.; Binger, D. D. Glioblastoma multiforme: a review of therapeutic targets Expert Opin. Ther. Targets 2009, 13, 701-18
2. Stupp, R.; Hegi, M. E.; Mason, W. P.; van den Bent, M. J.; Taphoorn, M. J.; Janzer, R. C. Effects of radiotherapy with concomitant and adjuvant Temozolomide versus radiotherapy alone on survival in glioblastoma in a randomized phase III study: 5-year analysis of the EORTC-NCIC trial Lancet Oncol. 2009, 10, 459-466
3. Tennant, D. A.; Durán, R. V.; Gottlieb, E. Targeting metabolic transformation for cancer therapy Nat. Rev. Cancer 2010, 10, 267-277
4. Cairns, R.; Harris, I. S.; Mak, T. W. Regulation of cancer cell metabolism Nat. Rev. Cancer 2011, 11, 85-95
5. Kroemer, G.; Pouyssegur, J. Tumor cell metabolism: cancer's Achilles' heel Cancer Cell 2008, 13, 472
6. Hanahan, D.; Weinberg, R. A. Hallmarks of cancer: the next generation Cell 2011, 144, 646-74
7. Cuperlovic-Culf, M.; Ferguson, D.; Culf, A.; Morin, P.; Touaibia, M. 1H NMR metabolomics analysis of glioblastoma subtypes: correlation between metabolomics and gene expression characteristics J. Biol. Chem. 2012, 287, 20164-20175
8. Ding, X.-Z.; Hennig, R.; Adrian, T E. Lipoxygenase and cyclooxygenase metabolism: new insights in treatment and chemoprevention of pancreatic cancer Mol. Cancer 2003, 2, 10
9. Samuelsson, B. Leukotrienes: mediators of immediate hypersensitivity reactions and inflammation Science 1983, 220, 568-575
10. Chen, M.; Lam, B. K.; Kanaoka, Y.; Nigrovic, P. A.; Audoly, L. P. Neutrophil-derived leukotriene B4 is required for inflammatory arthritis J. Exp. Med. 2006, 203, 837-842
11. Gupta, S.; Srivastava, M.; Ahmad, N.; Sakamoto, K.; Bostwick, D. G. Lipoxygenase-5 is overexpressed in prostate adenocarcinoma Cancer 2001, 91, 737-743
12. Banoglu, E.; CalIşkan, B.; Luderer, S.; Eren, G.; Ozkan, Y.; Altenhofen, W. Identification of novel benzimidazole derivatives as inhibitors of leukotriene biosynthesis by virtual screening targeting 5-lipoxygenase- activating protein (FLAP) Bioorg. Med. Chem. 2012, 20, 3728-3741
13. Rossi, A.; Pergola, C.; Koeberle, A.; Hoffmann, M.; Dehm, F.; Bramanti, P.; Cuzzocrea, S. The 5-lipoxygenase inhibitor, zileuton, suppresses prostaglandin biosynthesis by inhibition of arachidonic acid release in macrophages Br. J. Pharmacol. 2010, 161, 555-570
14. Ishii, K.; Zaitsu, M.; Yonemitsu, N.; Kan, Y.; Hamasaki, Y.; Matsuo, M. 5-lipoxygenase pathway promotes cell proliferation in human glioma cell lines Clin. Neuropathol. 2009, 28, 445-452
15. Lim, J. Y.; Oh, J. H.; Jung, J. R.; Kim, S. M.; Ryu, C. H.; Kim, H. T.; Jeun, S. S. MK886-induced apoptosis depends on the 5-LO expression level in human malignant glioma cells J. Neurooncol. 2010, 97, 339-46
16. Magro, A. M.; Magro, A. D.; Cunningham, C.; Miller, M. R. Down-regulation of vinculin upon MK886-induced apoptosis in LN18 glioblastoma cells Neoplasma 2007, 54, 517-26
17. Boudreau, L. H.; Maillet, J.; LeBlanc, L. M.; Jean-Francois, J.; Touaibia, M.; Flamand, N.; Surette, M. E. Caffeic acid phenethyl ester and its amide analogue are potent inhibitors of leukotriene biosynthesis in human polymorphonuclear leukocytes PLoS One 2012, 7, e31833
18. Liégeois, C.; Lermusieau, G.; Collin, C. Measuring antioxidant efficiency of wort, malt and hop against 2,2′-azobis(2-amidopropane)- dihydrochloride-induced oxidation of an aqueous dispersion of linoleic acid J. Agric. Food Chem. 2000, 48, 1129-1134
19. Tiziani, S.; Kang, Y.; Choi, J. S.; Roberts, W.; Paternostro, G. Metabolic high-content nuclear magnetic resonance-based drug screening of a kinase inhibitor library Nat. Commun. 2011, 2, 545
20. Touaibia, M.; Guay, M. Natural product total synthesis in the organic laboratory: Total synthesis of caffeic acid phenethyl ester (CAPE), a potent 5-lipoxygenase inhibitor from honeybee hives J. Chem. Educ. 2011, 88, 473
21. Cano, K. E.; Li, Y. J.; Chen, Y. NMR metabolomic profiling reveals new roles of SUMOylation in DNA damage response J. Proteome Res. 2010, 9, 5382-5388
22. Hwang, T.; Shaka, A. J. Water suppression that works. Excitation sculpting using arbitrary waveforms and pulse field gradients J Magn Res A 1995, 112, 275-279
23. Savorani, F.; Tomasi, G.; Engelsen, S. B. icoshift: A versatile tool for the rapid alignment of 1D NMR spectra J. Magn. Reson. 2010, 202, 190-202
24. Cuperlovic-Culf, M.; Belacel, N.; Chute, I.; Culf, A.; Burton, I. Walter, NMR metabolic analysis of samples using fuzzy K-means clustering J. Magn. Res. Chem. 2009, 47, S96
25. Tusher, V. G.; Tibshirani, R.; Chu, G. Significance analysis of microarrays applied to the ionizing radiation response Proc. Natl. Acad. Sci. U.S.A. 2001, 98, 5116
26. Wishart, D. S.; Knox, C.; Guo, A. C.; Eisner, R.; Young, N.; Gautam, B. HMDB: a knowledgebase for the human metabolome Nucleic Acids Res. 2009, 37 (Database) D603
27. Markley, J. L.; Anderson, M. E.; Cui, Q.; Eghbalnia, H. R.; Lewis, I. A.; Hegeman, A. D.; Li, J.; Schulte, C. F.; Sussman, M. R.; Westler, W. M.; Ulrich, E. L.; Zolnai, Z. New bioinformatics resources for metabolomics Pac. Symp. Biocomput. 2007, 168, 157-68
28. Tulpan, D.; Leger, S.; Belliveau, L.; Culf, A.; Cuperlovic-Culf, M. MetaboHunter: an automatic approach for identification of metabolites from 1H-NMR spectra of complex mixtures BMC Bioinf. 2011, 12, 400
29. Morin, P., Jr.; Ni, Z.; McMullen, D. C.; Storey, K. B. Expression of Nrf2 and its downstream gene targets in hibernating 13-lined ground squirrels, Spermophilus tridecemlineatus Mol. Cell. Biochem. 2008, 312, 121-129
30. Flamand, N.; Mancuso, P.; Serezani, C. H.; Brock, T. G. Leukotrienes: mediators that have been typecast as villains Cell. Mol. Life Sci. 2007, 64, 2657-2670
31. Barretina, J.; Caponigro, G.; Stransky, N.; Venkatesan, K.; Margolin, A. A.; Kim, S. The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity Nature 2012, 483, 603-607
32. Ishii, K.; Zaitsu, M.; Yonemitsu, N.; Kan, Y.; Hamasaki, Y.; Matsuo, M. 5-Lipoxygenase pathway promotes cell proliferation in human glioma cell lines Clin. Neuropathol. 2009, 28, 445-452
33. Greenhough, A.; Smartt, H. J.; Moore, A. E.; Roberts, H. R.; Williams, A. C.; Paraskeva, C.; Kaidi, A. The COX-2/PGE2 pathway: key roles in the hallmarks of cancer and adaptation to the tumour microenvironment Carcinogenesis 2009, 30, 377-386
34. Harmon, G. S.; Lam, M. T.; Glass, C. K. PPARs and lipid ligands in inflammation and metabolism Chem. Rev. 2011, 111, 6321-6340
35. Devaraj, S.; Jialal, I. Alpha-tocopherol decreases tumor necrosis factor-alpha mRNA and protein from activated human monocytes by inhibition of 5-lipoxygenase Free Radic. Biol. Med. 2005, 38, 1212-1220
36. Kozawa, O.; Suzuki, A.; Kaida, T.; Tokuda, H.; Uematsu, T. Tumor necrosis factor-alpha autoregulates interleukin-6 synthesis via activation of protein kinase C. Function of sphingosine 1-phosphate and phosphatidylcholine-specific phospholipase C J. Biol. Chem. 1997, 272, 25099-25104
37. Plo, I.; Lautier, D.; Levade, T.; Sekouri, H.; Jaffrézou, J. P.; Laurent, G.; Bettaïeb, A. Phosphatidylcholine-specific phospholipaseC and phospholipaseD are respectively implicated in mitogen-activated protein kinase and nuclear factor kappaB activation in tumour-necrosis-factor-alpha-treated immature acute-myeloid-leukaemia cells Biochem. J. 2000, 351, 459-467
38. Regueira, T.; Lepper, P. M.; Brandt, S.; Ochs, M.; Vuda, M.; Takala, J.; Jakob, S. M.; Djafarzadeh, S. Hypoxia inducible factor-1 alpha induction by tumour necrosis factor-alpha, but not by toll-like receptor agonists, modulates cellular respiration in cultured human hepatocytes Liver Int. 2009, 29, 1582-1592
39. Pufahl, L.; Katryniok, C.; Schnur, N.; Sorg, B. L.; Metzner, J.; Grez, M.; Steinhilber, D J. Trichostatin A induces 5-lipoxygenase promoter activity and mRNA expression via inhibition of histone deacetylase 2 and 3 J. Cell. Mol. Med. 2012, 16, 1461-1467
40. Watanabe, C.; Shu, G. L.; Zheng, T. S.; Flavell, R. A.; Clark, E. A. Caspase 6 regulates B cell activation and differentiation into plasma cells J. Immunol. 2008, 181, 6810-6819
41. Battelino, T.; Goto, M.; Krzisnik, C.; Zeller, W. P. Tumor necrosis factor-alpha alters glucose metabolism in suckling rats J. Lab. Clin. Med. 1999, 133, 583-589
42. Kim, Y. J.; Stringfield, T. M.; Chen, Y.; Broxmeyer, H. E. Modulation of cord blood CD8+ T-cell effector differentiation by TGF-beta1 and 4-1BB costimulation Blood 2005, 105, 274-281
43. Schneider, C.; Pozzi, A. Cyclooxygenases and lipoxygenases in cancer Cancer Metastat. Rev. 2011, 30, 277-294
44. Ishibashi, M.; Bottone, F. G., Jr; Taniura, S.; Kamitani, H.; Watanabe, T.; Eling, T. E. The cyclooxygenase inhibitor indomethacin modulates gene expression and represses the extracellular matrix protein laminin gamma1 in human glioblastoma cells Exp. Cell Res. 2005, 302, 244-252
45. Gottschalk, M.; Ivanova, G.; Collins, D. M.; Eustace, A.; Connor, R. O.; Brougham, D. F. Metabolomic studies of human lung carcinoma cell lines using in vitro 1 H NMR of whole cells and cellular extracts NMR Biomed. 2008, 21, 809-819
46. Schulte, A.; Günther, H. S.; Phillips, H. S.; Kemming, D. A distinct subset of glioma cell lines with stem cell-like properties reflects the transcriptional phenotype of glioblastomas and overexpresses CXCR4 as therapeutic target Glia 2011, 59, 590-602