Liver metabolomics reveals increased oxidative stress and fibrogenic potential in Gfrp transgenic mice in response to ionizing radiation

Journal of Proteome Research

Volumn 13, Issue 6, 2014, Pages 3065-3074

  Cheema, Amrita K ^a   Pathak, Rupak ^b   Zandkarimi, Fereshteh ^a   Kaur, Prabhjit ^a   Alkhalil, Lynn ^a   Singh, Rajbir ^a   Zhong, Xiaogang ^a   Ghosh, Sanchita ^c   Aykin Burns, Nukhet ^b,d   Hauer Jensen, Martin ^b,d  

^a GEORGETOWN UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^c UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^d CENTRAL ARKANSAS VETERANS HEALTHCARE SYSTEM   (United States)

Author keywords

ionizing radiation; metabolomics; stress signaling

Indexed keywords

LIPID PEROXIDE; MALONALDEHYDE; PEROXIDE; PROTEIN GFRP; REGULATOR PROTEIN; TETRAHYDROBIOPTERIN; UNCLASSIFIED DRUG; CARRIER PROTEIN; GTP CYCLOHYDROLASE I FEEDBACK REGULATORY PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; GENE OVEREXPRESSION; GENOTYPE; IONIZING RADIATION; LIPID METABOLISM; LIPID PEROXIDATION; LIVER FIBROSIS; MASS SPECTROMETRY; METABOLOMICS; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RADIATION EXPOSURE; SIGNAL TRANSDUCTION; TRANSGENE; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; GENETICS; LIVER; LIVER CIRRHOSIS; MALE; METABOLISM; METABOLOME; RADIATION INJURY; RADIATION RESPONSE; TRANSGENIC MOUSE;

ANIMALS; CARRIER PROTEINS; FEMALE; LIPID METABOLISM; LIPID PEROXIDATION; LIVER; LIVER CIRRHOSIS; MALE; METABOLOME; METABOLOMICS; MICE, INBRED C57BL; MICE, TRANSGENIC; OXIDATIVE STRESS; RADIATION INJURIES, EXPERIMENTAL; RADIATION, IONIZING; SIGNAL TRANSDUCTION;

EID: 84902095879     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr500278t     Document Type: Article

References (46)

1. Kmiec, Z. Cooperation of liver cells in health and disease Adv. Anat. Embryol. Cell Biol. 2001, 161 (III-XIII) 1-151
2. Dawson, L. A.; Ten Haken, R. K.; Lawrence, T. S. Partial irradiation of the liver Semin. Radiat. Oncol. 2001, 11, 240-246
3. Lin, R. X.; Zhao, H. B.; Li, C. R.; Sun, Y. N.; Qian, X. H.; Wang, S. Q. Proteomic analysis of ionizing radiation-induced proteins at the subcellular level J. Proteome Res. 2009, 8, 390-399
4. Dawson, L. A.; Normolle, D.; Balter, J. M.; McGinn, C. J.; Lawrence, T. S.; Ten Haken, R. K. Analysis of radiation-induced liver disease using the Lyman NTCP model Int. J. Radiat. Oncol. Biol. Phys. 2002, 53, 810-821
5. Cheng, J. C.; Wu, J. K.; Huang, C. M. Radiation-induced liver disease after three-dimensional conformal radiotherapy for patients with hepatocellular carcinoma: dosimetric analysis and implication Int. J. Radiat. Oncol. Biol. Phys. 2002, 54, 156-162
6. Khan, A. R.; Rana, P.; Devi, M. M. Nuclear magnetic resonance spectroscopy-based metabonomic investigation of biochemical effects in serum of gamma-irradiated mice Int. J. Radiat. Biol. 2011, 87, 91-97
7. Lanz, C.; Patterson, A. D.; Slavik, J. Radiation metabolomics. 3. Biomarker discovery in the urine of gamma-irradiated rats using a simplified metabolomics protocol of gas chromatography-mass spectrometry combined with random forests machine learning algorithm Radiat. Res. 2009, 172, 198-212
8. Liu, H.; Wang, Z.; Zhang, X. Selection of candidate radiation biomarkers in the serum of rats exposed to gamma-rays by GC/TOFMS-based metabolomics Radiat. Prot. Dosimetry 2013, 154, 9-17
9. Varghese, R. S.; Cheema, A.; Cheema, P. Analysis of LC-MS data for characterizing the metabolic changes in response to radiation J. Proteome Res. 2010, 9, 2786-2793
10. Patterson, A. D.; Li, H.; Eichler, G. S. UPLC-ESI-TOFMS-based metabolomics and gene expression dynamics inspector self-organizing metabolomic maps as tools for understanding the cellular response to ionizing radiation Anal. Chem. 2008, 80, 665-674
11. Coy, S. L.; Cheema, A. K.; Tyburski, J. B.; Laiakis, E. C.; Collins, S. P.; Fornace, A. Radiation metabolomics and its potential in biodosimetry Int. J. Radiat. Biol. 2011, 87, 802-823
12. Patterson, A. D.; Lanz, C.; Gonzalez, F. J.; Idle, J. R. The role of mass spectrometry-based metabolomics in medical countermeasures against radiation Mass Spectrom. Rev. 2010, 29, 503-521
13. Thony, B.; Auerbach, G.; Blau, N. Tetrahydrobiopterin biosynthesis, regeneration and functions Biochem. J. 2000, 347 (Pt 1) 1-16
14. Yoneyama, T.; Wilson, L. M.; Hatakeyama, K. GTP cyclohydrolase I feedback regulatory protein-dependent and -independent inhibitors of GTP cyclohydrolase I Arch. Biochem. Biophys. 2001, 388, 67-73
15. Pathak, R.; Pawar, S. A.; Fu, Q. Characterization of transgenic Gfrp knock-in mice: implications for tetrahydrobiopterin in modulation of normal tissue radiation responses Antioxid. Redox Signaling 2014, 20, 1436-1446
16. Cohen, S. R.; Cohen, E. P. Chronic oxidative stress after irradiation: an unproven hypothesis Med. Hypotheses 2013, 80, 172-175
17. Berbee, M.; Fu, Q.; Boerma, M. Reduction of radiation-induced vascular nitrosative stress by the vitamin E analog gamma-tocotrienol: evidence of a role for tetrahydrobiopterin Int. J. Radiat. Oncol. Biol. Phys. 2011, 79, 884-891
18. Pathak, R.; Pawar, S. A.; Fu, Q. Characterization of transgenic Gfrp knock-in mice: implications for tetrahydrobiopterin in modulation of normal tissue radiation responses Antioxid. Redox Signaling 2014, 20, 1436-1446
19. Wang, S.; Lee, Y.; Kim, J. Potential role of Hedgehog pathway in liver response to radiation PLoS One 2013, 8, e74141
20. Kaur, P.; Sheikh, K.; Kirilyuk, A. Metabolomic profiling for biomarker discovery in pancreatic cancer Int. J. Mass Spectrom. 2012, 310, 44-51
21. Want, E. J.; Wilson, I. D.; Gika, H. Global metabolic profiling procedures for urine using UPLC-MS Nat. Protoc. 2010, 5, 1005-1018
22. 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
23. Ciappio, E. D.; Krausz, K. W.; Rochman, M. Metabolomics reveals a role for the chromatin-binding protein HMGN5 in glutathione metabolism PLoS One 2014, 9, e84583
24. Cheema, A. K.; Suman, S.; Kaur, P.; Singh, R.; Fornace, A. J., Jr.; Datta, K. Long-term differential changes in mouse intestinal metabolomics after gamma and heavy ion radiation exposure PLoS One 2014, 9, e87079
25. Tyburski, J. B.; Patterson, A. D.; Krausz, K. W. Radiation metabolomics. 2. Dose- and time-dependent urinary excretion of deaminated purines and pyrimidines after sublethal gamma-radiation exposure in mice Radiat. Res. 2009, 172, 42-57
26. Xia, J.; Mandal, R.; Sinelnikov, I. V.; Broadhurst, D.; Wishart, D. S. MetaboAnalyst 2.0 - a comprehensive server for metabolomic data analysis Nucleic Acids Res. 2012, 40, W127-W133
27. Zhou, B.; Wang, J.; Ressom, H. W. MetaboSearch: tool for mass-based metabolite identification using multiple databases PLoS One 2012, 7, e40096
28. Illig, T.; Gieger, C.; Zhai, G. A genome-wide perspective of genetic variation in human metabolism Nat. Genet. 2010, 42, 137-141
29. Römisch-Margl, W PC; Bogumil, R.; Röhring, C.; Suhre, K. Procedure for tissue sample preparation and metabolite extraction for high-throughput targeted metabolomics Metabolomics 2011, 1-10
30. Xia, J.; Wishart, D. S. Metabolomic data processing, analysis, and interpretation using MetaboAnalyst. Curr. Protoc. Bioinformatics 2011, 10.1002/0471250953.bi1410s34
31. Bulmer, A. C.; Verkade, H. J.; Wagner, K. H. Bilirubin and beyond: a review of lipid status in Gilbert's syndrome and its relevance to cardiovascular disease protection Prog. Lipid Res. 2013, 52, 193-205
32. Condezo-Hoyos, L.; Abderrahim, F.; Conde, M. V. Antioxidant activity of liver growth factor, a bilirubin covalently bound to albumin Free Radical Biol. Med. 2009, 46, 656-662
33. MacLean, P. D.; Drake, E. C.; Ross, L.; Barclay, C. Bilirubin as an antioxidant in micelles and lipid bilayers: its contribution to the total antioxidant capacity of human blood plasma Free Radical Biol. Med. 2007, 43, 600-609
34. Muchova, L.; Vanova, K.; Zelenka, J. Bile acids decrease intracellular bilirubin levels in the cholestatic liver: implications for bile acid-mediated oxidative stress J. Cell Mol. Med. 2011, 15, 1156-1165
35. Postic, C.; Dentin, R.; Girard, J. Role of the liver in the control of carbohydrate and lipid homeostasis Diabetes Metab. 2004, 30, 398-408
36. Ljubuncic, P.; Said, O.; Ehrlich, Y.; Meddings, J. B.; Shaffer, E. A.; Bomzon, A. On the in vitro vasoactivity of bile acids Br. J. Pharmacol. 2000, 131, 387-398
37. Le Quere, V.; Plee-Gautier, E.; Potin, P.; Madec, S.; Salaun, J. P. Human CYP4F3s are the main catalysts in the oxidation of fatty acid epoxides J. Lipid Res. 2004, 45, 1446-1458
38. Calder, P. C. n -3 polyunsaturated fatty acids, inflammation, and inflammatory diseases Am. J. Clin. Nutr. 2006, 83, 1505S-1519S
39. Fuchs, B.; Schiller, J.; Wagner, U.; Hantzschel, H.; Arnold, K. The phosphatidylcholine/lysophosphatidylcholine ratio in human plasma is an indicator of the severity of rheumatoid arthritis: investigations by 31P NMR and MALDI-TOF MS Clin. Biochem. 2005, 38, 925-933
40. Wymann, M. P.; Schneiter, R. Lipid signalling in disease Nat. Rev. Mol. Cell Biol. 2008, 9, 162-176
41. Tyburski, J. B.; Patterson, A. D.; Krausz, K. W. Radiation metabolomics. 1. Identification of minimally invasive urine biomarkers for gamma-radiation exposure in mice Radiat. Res. 2008, 170, 1-14
42. Negre-Salvayre, A.; Auge, N.; Ayala, V. Pathological aspects of lipid peroxidation Free Radical Res. 2010, 44, 1125-1171
43. Topal, G.; Brunet, A.; Millanvoye, E. Homocysteine induces oxidative stress by uncoupling of NO synthase activity through reduction of tetrahydrobiopterin Free Radical Biol. Med. 2004, 36, 1532-1541
44. Zhao, W.; Robbins, M. E. Inflammation and chronic oxidative stress in radiation-induced late normal tissue injury: therapeutic implications Curr. Med. Chem. 2009, 16, 130-143
45. Zhao, Y.; Cao, J.; Chen, Y. S. Detection of tetrahydrobiopterin by LC-MS/MS in plasma from multiple species Bioanalysis 2009, 1, 895-903
46. O'Sullivan, B.; Levin, W. Late radiation-related fibrosis: pathogenesis, manifestations, and current management Semin. Radiat. Oncol. 2003, 13, 274-289