Metabolomics reveals altered lipid metabolism in a mouse model of endometriosis

Journal of Proteome Research

Volumn 15, Issue 8, 2016, Pages 2626-2633

  Dutta, Mainak ^a,c   Anitha, Mallappa ^a   Smith, Philip B ^b   Chiaro, Christopher R ^a   Maan, Meenu ^d   Chaudhury, Koel ^c   Patterson, Andrew D ^a,b  

^a Department of Veterinary and Biomedical Sciences   (United States)

^b PENNSYLVANIA STATE UNIVERSITY   (United States)

^c INDIAN INSTITUTE OF TECHNOLOGY   (India)

^d JAWAHARLAL NEHRU UNIVERSITY   (India)

Author keywords

endometriosis; metabolomics; phosphatidylcholine; phosphatidylethanolamine

Indexed keywords

PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; PHOSPHATIDYLETHANOLAMINE METHYLTRANSFERASE; PHOSPHATIDYLINOSITOL; SPHINGOMYELIN; TRIACYLGLYCEROL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CONTROLLED STUDY; DISEASE COURSE; ENDOMETRIOSIS; ESTRUS CYCLE; EXPERIMENTAL PERITONITIS; FEMALE; GENE EXPRESSION; LIPID BLOOD LEVEL; LIPID METABOLISM; LIPIDOMICS; METABOLOMICS; MOUSE; NONHUMAN; PERITONEUM; PERITONEUM MACROPHAGE; PHOSPHOLIPID METABOLISM; PRIORITY JOURNAL; QUADRUPOLE MASS SPECTROMETRY; TIME OF FLIGHT MASS SPECTROMETRY; TRIACYLGLYCEROL BLOOD LEVEL; ULTRA PERFORMANCE LIQUID CHROMATOGRAPHY; ANIMAL; BLOOD; METABOLISM;

ANIMALS; ENDOMETRIOSIS; FEMALE; LIPID METABOLISM; METABOLOMICS; MICE; PHOSPHATIDYLCHOLINES; PHOSPHATIDYLETHANOLAMINES; SPHINGOMYELINS; TRIGLYCERIDES;

EID: 84981297755     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/acs.jproteome.6b00197     Document Type: Article

References (36)

1. Sampson, J. A. Metastatic or Embolic Endometriosis, due to the Menstrual Dissemination of Endometrial Tissue into the Venous Circulation Am. J. Pathol. 1927, 3 (2) 93-110.43
2. Van Langendonckt, A.; Casanas-Roux, F.; Donnez, J. Oxidative stress and peritoneal endometriosis Fertil. Steril. 2002, 77 (5) 861-70 10.1016/S0015-0282(02)02959-X
3. Lebovic, D. I.; Mueller, M. D.; Taylor, R. N. Immunobiology of endometriosis Fertil. Steril. 2001, 75 (1) 1-10 10.1016/S0015-0282(00)01630-7
4. Rizner, T. L. Estrogen metabolism and action in endometriosis Mol. Cell. Endocrinol. 2009, 307 (1-2) 8-18 10.1016/j.mce.2009.03.022
5. Takahashi, K.; Nagata, H.; Kitao, M. Clinical usefulness of determination of estradiol level in the menstrual blood for patients with endometriosis Nihon Sanka Fujinka Gakkai Zasshi 1989, 41 (11) 1849-50
6. Gschwind, A.; Prenzel, N.; Ullrich, A. Lysophosphatidic acid-induced squamous cell carcinoma cell proliferation and motility involves epidermal growth factor receptor signal transactivation Cancer Res. 2002, 62 (21) 6329-36
7. Coussens, L. M.; Werb, Z. Inflammation and cancer Nature 2002, 420 (6917) 860-7 10.1038/nature01322
8. Gibellini, F.; Smith, T. K. The Kennedy pathway - De novo synthesis of phosphatidylethanolamine and phosphatidylcholine IUBMB Life 2010, 62 (6) 414-28 10.1002/iub.354
9. Kennedy, E. P.; Weiss, S. B. The function of cytidine coenzymes in the biosynthesis of phospholipides J. Biol. Chem. 1956, 222 (1) 193-214
10. DeLong, C. J.; Shen, Y. J.; Thomas, M. J.; Cui, Z. Molecular distinction of phosphatidylcholine synthesis between the CDP-choline pathway and phosphatidylethanolamine methylation pathway J. Biol. Chem. 1999, 274 (42) 29683-8 10.1074/jbc.274.42.29683
11. Byers, S. L.; Wiles, M. V.; Dunn, S. L.; Taft, R. A. Mouse estrous cycle identification tool and images PLoS One 2012, 7 (4) e35538 10.1371/journal.pone.0035538
12. Hirata, T.; Osuga, Y.; Yoshino, O.; Hirota, Y.; Harada, M.; Takemura, Y.; Morimoto, C.; Koga, K.; Yano, T.; Tsutsumi, O.; Taketani, Y. Development of an experimental model of endometriosis using mice that ubiquitously express green fluorescent protein Hum. Reprod. 2005, 20 (8) 2092-6 10.1093/humrep/dei012
13. Argyris, B. F. Role of macrophages in antibody production. Immune response to sheep red blood cells J. Immunol 1967, 99 (4) 744-50
14. Zhang, X.; Goncalves, R.; Mosser, D. M. The isolation and characterization of murine macrophages Curr. Protoc Immunol 2008, 83, 14.1.1-14 10.1002/0471142735.im1401s83
15. Zhang, L.; Hatzakis, E.; Nichols, R. G.; Hao, R.; Correll, J.; Smith, P. B.; Chiaro, C. R.; Perdew, G. H.; Patterson, A. D. Metabolomics Reveals that Aryl Hydrocarbon Receptor Activation by Environmental Chemicals Induces Systemic Metabolic Dysfunction in Mice Environ. Sci. Technol. 2015, 49 (13) 8067-77 10.1021/acs.est.5b01389
16. Kind, T.; Liu, K. H.; Lee, D. Y.; DeFelice, B.; Meissen, J. K.; Fiehn, O. LipidBlast in silico tandem mass spectrometry database for lipid identification Nat. Methods 2013, 10 (8) 755-8 10.1038/nmeth.2551
17. Fahy, E.; Sud, M.; Cotter, D.; Subramaniam, S. LIPID MAPS online tools for lipid research Nucleic Acids Res. 2007, 35 (Web Server) W606-12 10.1093/nar/gkm324
18. Schmelzer, K.; Fahy, E.; Subramaniam, S.; Dennis, E. A. The lipid maps initiative in lipidomics Methods Enzymol. 2007, 432, 171-83 10.1016/S0076-6879(07)32007-7
19. Bolton, E. E.; Wang, Y.; Thiessen, P. A.; Bryant, S. H.; Ralph, A. W.; David, C. S. Integrated Platform of Small Molecules and Biological Activities. In Annual Reports in Computational Chemistry; Elsevier, 2008; Vol. 4, pp 217-241.
20. Barupal, D. K.; Haldiya, P. K.; Wohlgemuth, G.; Kind, T.; Kothari, S. L.; Pinkerton, K. E.; Fiehn, O. MetaMapp: mapping and visualizing metabolomic data by integrating information from biochemical pathways and chemical and mass spectral similarity BMC Bioinf. 2012, 13, 99 10.1186/1471-2105-13-99
21. Eyster, K. M.; Klinkova, O.; Kennedy, V.; Hansen, K. A. Whole genome deoxyribonucleic acid microarray analysis of gene expression in ectopic versus eutopic endometrium Fertil. Steril. 2007, 88 (6) 1505-33 10.1016/j.fertnstert.2007.01.056
22. Ulukus, M.; Arici, A. Immunology of endometriosis Minerva Ginecol. 2005, 57 (3) 237-48
23. Vouk, K.; Hevir, N.; Ribic-Pucelj, M.; Haarpaintner, G.; Scherb, H.; Osredkar, J.; Moller, G.; Prehn, C.; Rizner, T. L.; Adamski, J. Discovery of phosphatidylcholines and sphingomyelins as biomarkers for ovarian endometriosis Hum. Reprod. 2012, 27 (10) 2955-65 10.1093/humrep/des152
24. Lee, Y. H.; Tan, C. W.; Venkatratnam, A.; Tan, C. S.; Cui, L.; Loh, S. F.; Griffith, L.; Tannenbaum, S. R.; Chan, J. K. Dysregulated sphingolipid metabolism in endometriosis J. Clin. Endocrinol. Metab. 2014, 99 (10) E1913-21 10.1210/jc.2014-1340
25. Dutta, M.; Joshi, M.; Srivastava, S.; Lodh, I.; Chakravarty, B.; Chaudhury, K. A metabonomics approach as a means for identification of potential biomarkers for early diagnosis of endometriosis Mol. BioSyst. 2012, 8 (12) 3281-7 10.1039/c2mb25353d
26. Nowak, N. M.; Fischer, O. M.; Gust, T. C.; Fuhrmann, U.; Habenicht, U. F.; Schmidt, A. Intraperitoneal inflammation decreases endometriosis in a mouse model Hum. Reprod. 2008, 23 (11) 2466-74 10.1093/humrep/den189
27. Cook, A. D.; Braine, E. L.; Hamilton, J. A. The phenotype of inflammatory macrophages is stimulus dependent: implications for the nature of the inflammatory response J. Immunol. 2003, 171 (9) 4816-23 10.4049/jimmunol.171.9.4816
28. Hrabak, A.; Bajor, T.; Csuka, I. The effect of various inflammatory agents on the alternative metabolic pathways of arginine in mouse and rat macrophages Inflammation Res. 2006, 55 (1) 23-31 10.1007/s00011-005-0004-6
29. Watkins, S. M.; Zhu, X.; Zeisel, S. H. Phosphatidylethanolamine-N-methyltransferase activity and dietary choline regulate liver-plasma lipid flux and essential fatty acid metabolism in mice J. Nutr. 2003, 133 (11) 3386-91
30. da Costa, K. A.; Sanders, L. M.; Fischer, L. M.; Zeisel, S. H. Docosahexaenoic acid in plasma phosphatidylcholine may be a potential marker for in vivo phosphatidylethanolamine N-methyltransferase activity in humans Am. J. Clin. Nutr. 2011, 93 (5) 968-74 10.3945/ajcn.110.011064
31. Resseguie, M.; Song, J.; Niculescu, M. D.; da Costa, K. A.; Randall, T. A.; Zeisel, S. H. Phosphatidylethanolamine N-methyltransferase (PEMT) gene expression is induced by estrogen in human and mouse primary hepatocytes FASEB J. 2007, 21 (10) 2622-32 10.1096/fj.07-8227com
32. Noga, A. A.; Vance, D. E. A gender-specific role for phosphatidylethanolamine N-methyltransferase-derived phosphatidylcholine in the regulation of plasma high density and very low density lipoproteins in mice J. Biol. Chem. 2003, 278 (24) 21851-9 10.1074/jbc.M301982200
33. Young, D. L. Estradiol- and testosterone-induced alterations in phosphatidylcholine and triglyceride synthesis in hepatic endoplasmic reticulum J. Lipid Res. 1971, 12 (5) 590-5
34. Obeid, R.; Herrmann, W. Homocysteine and lipids: S-adenosyl methionine as a key intermediate FEBS Lett. 2009, 583 (8) 1215-25 10.1016/j.febslet.2009.03.038
35. Aidrus, A.; Natadisastra, M.; Jacoeb, T. Z. Homocysteine Level in the Blood and Follicular Fluid is Higher in Infertile Women with Endometriosis Indonesian Journal of Obstetrics and Gynecology 2013, 37 (2) 92-98
36. Ebisch, I. M.; Peters, W. H.; Thomas, C. M.; Wetzels, A. M.; Peer, P. G.; Steegers-Theunissen, R. P. Homocysteine, glutathione and related thiols affect fertility parameters in the (sub)fertile couple Hum. Reprod. 2006, 21 (7) 1725-33 10.1093/humrep/del081