Eicosanomic profiling reveals dominance of the epoxygenase pathway in human amniotic fluid at term in spontaneous labor

FASEB Journal

Volumn 28, Issue 11, 2014, Pages 4835-4846

  Maddipati, Krishna Rao ^a,b   Romero, Roberto ^c,d,e   Chaiworapongsa, Tinnakorn ^a,c   Zhou, Sen Lin ^a,b   Xu, Zhonghui ^f   Tarca, Adi L ^f   Kusanovic, Juan Pedro ^c,g,h   Munoz, Hernan ⁱ   Honn, Kenneth V ^a  

^a WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

^c EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^d UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^e MICHIGAN STATE UNIVERSITY   (United States)

^f Wayne State University   (United States)

^g PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^h HOSPITAL DR SÓTERO DEL RÍO   (Chile)

ⁱ UNIVERSITY OF CHILE   (Chile)

Author keywords

Epoxy fatty acids; Hydroxy fatty acids; LC MS; Lipidomics; Parturition

Indexed keywords

11 HYDROXYICOSATETRAENOIC ACID; 12 HYDROXYICOSATETRAENOIC ACID; 5 HYDROXYICOSATETRAENOIC ACID; 8 HYDROXYICOSATETRAENOIC ACID; 9 HYDROXYICOSATETRAENOIC ACID; ARACHIDONIC ACID; EPOXYGENASE; HYDROXYICOSATETRAENOIC ACID; ICOSANOID; LIPOXIN B; LIPOXYGENASE; OXYGENASE; POLYUNSATURATED FATTY ACID; PROSTAGLANDIN E2; UNCLASSIFIED DRUG; OXIDOREDUCTASE;

ADULT; AMNION FLUID; ARACHIDONIC ACID METABOLISM; ARTICLE; CHIRAL CHROMATOGRAPHY; CLINICAL ARTICLE; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; EMBRYO; FEMALE; HUMAN; LABOR; LIMIT OF DETECTION; LIPID HYDROLYSIS; LIPIDOMICS; MASS SPECTROMETRY; RETROSPECTIVE STUDY; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; STEREOCHEMISTRY; LIPID METABOLISM; METABOLISM; PHYSIOLOGY; PREGNANCY; TERM BIRTH;

ADULT; AMNIOTIC FLUID; ARACHIDONIC ACID; EICOSANOIDS; FEMALE; HUMANS; LABOR, OBSTETRIC; LIPID METABOLISM; OXIDOREDUCTASES; PREGNANCY; TERM BIRTH;

EID: 84912071097     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.14-254383     Document Type: Article

References (81)

1. Mitchell, M. D. (1981) Prostaglandins during pregnancy and the perinatal period. J. Reprod. Fertil. 62, 305-315
2. Romero, R., Gonzalez, R., Baumann, P., Behnke, E., Rittenhouse, L., Barberio, D., Cotton, D. B., and Mitchell, M. D. (1994) Topographic differences in amniotic fluid concentrations of prostanoids in women in spontaneous labor at term. Prostaglandins Leukot. Essent. Fatty Acids 50, 97-104
3. Romero, R., Munoz, H., Gomez, R., Parra, M., Polanco, M., Valverde, V., Hasbun, J., Garrido, J., Ghezzi, F., Mazor, M., Tolosa, J. E., and Mitchell, M. D. (1996) Increase in prostaglandin bioavailability precedes the onset of human parturition. Prostaglandins Leukot. Essent. Fatty Acids. 54, 187-191
4. Mitchell, M. D., Romero, R. J., Edwin, S. S., and Trautman, M. S. (1995) Prostaglandins and parturition. Reprod. Fertil. Dev. 7, 623-632
5. Lee, S. E., Romero, R., Park, I. S., Seong, H. S., Park, C. W., and Yoon, B. H. (2008) Amniotic fluid prostaglandin concentrations increase before the onset of spontaneous labor at term. J. Matern. Fetal Neonatal Med. 21, 89-94
6. Vidaeff, A. C., and Ramin, S. M. (2008) Potential biochemical events associated with initiation of labor. Curr. Med. Chem. 15, 614-619
7. Slater, D., Berger, L., Newton, R., Moore, G., and Bennett, P. (1994) The relative abundance of type 1 to type 2 cyclooxygenase mRNA in human amnion at term. Biochem. Biophys. Res. Commun. 198, 304-308
8. Olson, D. M., and Ammann, C. (2007) Role of the prostaglandins in labour and prostaglandin receptor inhibitors in the prevention of preterm labour. Front. Biosci. 12, 1329-1343
9. Kelly, A. J., Malik, S., Smith, L., Kavanagh, J., and Thomas, J. (2009) Vaginal prostaglandin (PGE2 and PGF2a) for induction of labour at term. Cochrane Database Syst. Rev. CD003101
10. Austin, S. C., Sanchez-Ramos, L., and Adair, C. D. (2010) Labor induction with intravaginal misoprostol compared with the dinoprostone vaginal insert: a systematic review and metaanalysis. Am. J. Obstet. Gynecol. 202, 624.e1-9
11. Berryman, G. K., Strickland, D. M., Hankins, G. D. V., and Mitchell, M. D. (1987) Amniotic fluid prostaglandin D2 in spontaneous and augmented labor. Life Sci. 41, 1611-1614
12. Romero, R., Wu, Y. K., Mazor, M., Hobbins, J. C., and Mitchell, M. D. (1988) Increased amniotic fluid leukotriene C4 concentration in term human parturition. Am. J. Obstet. Gynecol. 159, 655-657
13. Romero, R., Wu, Y. K., Mazor, M., Hobbins, J. C., and Mitchell, M. D. (1989) Amniotic fluid concentration of 5-hydroxyeicosatetraenoic acid is increased in human parturition at term. Prostaglandins Leukot. Essent. Fatty Acids 35, 81-83
14. Edwin, S. S., Romero, R. J., Munoz, H., Branch, D. W., and Mitchell, M. D. (1996) 5-Hydroxyeicosatetraenoic acid and human parturition. Prostaglandins 51, 403-412
15. Glass, M., Hong, J., Sato, T. A., and Mitchell, M. D. (2005) Misidentification of prostamides as prostaglandins. J. Lipid Res. 46, 1364-1368
16. Rosner, W., Auchus, R. J., Azziz, R., Sluss, P. M., and Raff, H. (2007) Utility, limitations, and pitfalls in measuring testosterone: an endocrine society position statement. J. Clin. Endocrinol. Metab. 92, 405-413
17. Wenk, M. R. (2010) Lipidomics: new tools and applications. Cell 143, 888-895
18. Ricciotti, E., and Fitzgerald, G. A. (2011) Prostaglandins and inflammation. Arterioscler. Thromb. Vasc. Biol. 31, 986-1000
19. McKirdy, N. C., Rice, G. E., and Mitchell, M. D. (2013) Eicosanoids as diagnostics for preterm labor. Reprod. Biol. Insights 6, 1-10
20. Romero, R., Quintero, R., Nores, J., Avila, C., Mazor, M., Hanaoka, S., Hagay, Z., Merchant, L., and Hobbins, J. C. (1991) Amniotic fluid white blood cell count: a rapid and simple test to diagnose microbial invasion of the amniotic cavity and predict preterm delivery. Am. J. Obstet. Gynecol. 165, 821-830
21. Romero, R., Jimenez, C., Lohda, A. K., Nores, J., Hanaoka, S., Avila, C., Callahan, R., Mazor, M., Hobbins, J. C., and Diamond, M. P. (1990) Amniotic fluid glucose concentration: a rapid and simple method for the detection of intraamniotic infection in preterm labor. Am. J. Obstet. Gynecol. 163, 968-974
22. Romero, R., Emamian, M., Quintero, R., Wan, M., Hobbins, J. C., Mazor, M., and Edberg, S. (1988) The value and limitations of the Gram stain examination in the diagnosis of intraamniotic infection. Am. J. Obstet. Gynecol. 159, 114-119
23. Maddipati, K. R., and Zhou, S. L. (2011) Stability and analysis of eicosanoids and docosanoids in tissue culture media. Prostaglandins Other Lipid Mediat. 94, 59-72
24. Benjamini, Y., and Hochberg, Y. (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57, 289-300
25. Henningsen, A. (2011) censReg: censored regression (tobit) models. R package, Version 0.5. R Project for Statistical Computing, Vienna, Austria; http://CRAN.R-project.org/package- censReg
26. Fulton, D., Falck, J. R., McGiff, J. C., Carroll, M. A., and Quilley, J. (1998) A method for the determination of 5, 6-EET using the lactone as an intermediate in the formation of the diol. J. Lipid Res. 39, 1713-1721
27. Ylikorkala, O., Makila, U. M., and Viinikka, L. (1981) Amniotic fluid prostacyclin and thromboxane in normal, preeclamptic, and some other complicated pregnancies. Am. J. Obstet. Gynecol. 141, 487-490
28. Mitchell, M. D., Chang, M. C., Chaiworapongsa, T., Lan, H.-Y., Helliwell, R. J. A., Romero, R., and Sato, T. A. (2005) Identification of 9α, 11β-prostaglandin F2 in human amniotic fluid and characterization of its production by human gestational tissues. J. Clin. Endocrinol. Metab. 90, 4244-4248
29. Romero, R., Emamian, M., Wan, M., Grzyboski, C., Hobbins, J. C., and Mitchell, M. D. (1987) Increased concentrations of arachidonic acid lipoxygenase metabolites in amniotic fluid during parturition. Obstet. Gynecol. 70, 849-851
30. Bennett, P. R., Elder, M. G., and Myatt, L. (1987) The effects of lipoxygenase metabolites of arachidonic acid on human myometrial contractility. Prostaglandins 33, 837-844
31. Fitzpatrick, F. A., and Wynalda, M. A. (1981) Albumin-lipid interactions: prostaglandin stability as a probe for characterizing binding sites on vertebrate albumins. Biochemistry 20, 6129-6134
32. Mitchell, M. D., Kraemer, D. L., and Strickland, D. M. (1982) The human placenta: a major source of prostaglandin D2. Prostaglandins Leukot. Med. 8, 383-387
33. Maxey, K. M., Maddipati, K. R., and Birkmeier, J. (1992) Interference in enzyme immunoassays. J Clin. Immunoassay 15, 116-120
34. Templeton, A. A., Cooper, I., and Kelly, R. W. (1978) Prostaglandin concentrations in the semen of fertile men. J. Reprod. Fertil. 52, 147-150
35. Quayle, A. J., Kelly, R. W., Hargreave, T. B., and James, K. (1989) Immunosuppression by seminal prostaglandins. Clin. Exp. Immunol. 75, 387-391
36. Skibinski, G., Kelly, R. W., Harrison, C. M., McMillan, L. A., and James, K. (1992) Relative immunosuppressive activity of human seminal prostaglandins. J. Reprod. Immunol. 22, 185-195
37. James, K., and Hargreave, T. B. (1984) Immunosuppression by seminal plasma and its possible clinical significance. Immunol. Today 5, 357-363
38. Woodward, D. F., Protzman, C. E., Krauss, A. H., and Williams, L. S. (1993) Identification of 19 (R)-OH prostaglandin E2 as a selective prostanoid EP2-receptor agonist. Prostaglandins 46, 371-383
39. Senior, J., Marshall, K., Sangha, R., and Clayton, J. K. (1993) In vitro characterization of prostanoid receptors on human myometrium at term pregnancy. Br. J. Pharmacol. 108, 501-506
40. Brodt-Eppley, J., and Myatt, L. (1999) Prostaglandin receptors in lower segment myometrium during gestation and labor. Obstet. Gynecol. 93, 89-93
41. Arulkumaran, S., Kandola, M. K., Hoffman, B., Hanyaloglu, A. C., Johnson, M. R., and Bennett, P. R. (2012) The roles of prostaglandin EP 1 and 3 receptors in the control of human myometrial contractility. J. Clin. Endocrinol. Metab. 97, 489-498
42. Senior, J., Marshall, K., Sangha, R., Baxter, G. S., and Clayton, J. K. (1991) In vitro characterization of prostanoid EP-receptors in the non-pregnant human myometrium. Br. J. Pharmacol. 102, 747-753
43. Menon, R., Fortunato, S. J., Milne, G. L., Brou, L., Carnevale, C., Sanchez, S. C., Hubbard, L., Lappas, M., Drobek, C. O., and Taylor, R. N. (2011) Amniotic fluid eicosanoids in preterm and term births: effects of risk factors for spontaneous preterm labor. Obstet. Gynecol. 118, 121-134
44. Smith, W. L., Urade, Y., and Jakobsson, P.-J. (2011) Enzymes of the cyclooxygenase pathways of prostanoid biosynthesis. Chem. Rev. 111, 5821-5865
45. Furstenberger, G., Marks, F., and Krieg, P. (2002) Arachidonate 8(S)-lipoxygenase. Prostaglandins Other Lipid Mediat. 68-69, 235-243
46. Schweiger, D., Fürstenberger, G., and Krieg, P. (2007) Inducible expression of 15-lipoxygenase-2 and 8-lipoxygenase inhibits cell growth via common signaling pathways. J. Lipid Res. 48, 553-564
47. Walther, M., Roffeis, J., Jansen, C., Anton, M., Ivanov, I., and Kuhn, H. (2009) Structural basis for pH-dependent alterations of reaction specificity of vertebrate lipoxygenase isoforms. Biochim. Biophys. Acta 1791, 827-835
48. Krishnamoorthy, S., and Honn, K. V. (2006) Inflammation and disease progression. Cancer Metastasis Rev. 25, 481-491
49. Marcus, A. J., Broekman, M. J., Safier, L. B., Ullman, H. L., Islam, N., Serhan, C. N., Rutherford, L. E., Korchak, H. M., and Weissmann, G. (1982) Formation of leukotrienes and other hydroxy acids during platelet-neutrophil interactions in vitro. Biochem. Biophys. Res. Commun. 109, 130-137
50. Borgeat, P., Fruteau de Laclos, B., Picard, S., Drapeau, J., Vallerand, P., and Corey, E. J. (1982) Studies on the mechanism of formation of the 5S, 12S-dihydroxy-6, 8, 10, 14(E, Z, E, Z)-icosatetraenoic acid in leukocytes. Prostaglandins 23, 713-724
51. Von Schacky, C., Marcus, A. J., Safier, L. B., Ullman, H. L., Islam, N., Broekman, M. J., and Fischer, S. (1990) Plateletneutrophil interactions. 12S, 20- and 5S, 12S-dihydroxyeicosapentaenoic acids: two novel neutrophil metabolites from plateletderived 12S-hydroxyeicosapentaenoic acid. J. Lipid Res. 31, 801-810
52. Osman, I., Young, A., Jordan, F., Greer, I. A., and Norman, J. E. (2006) Leukocyte density and proinflammatory mediator expression in regional human fetal membranes and decidua before and during labor at term. J. Soc. Gynecol. Investig. 13, 97-103
53. Osman, I., Young, A., Ledingham, M. A., Thomson, A. J., Jordan, F., Greer, I. A., and Norman, J. E. (2003) Leukocyte density and pro-inflammatory cytokine expression in human fetal membranes, decidua, cervix and myometrium before and during labour at term. Mol. Hum. Reprod. 9, 41-45
54. Kiel, D., Zipkin, R. E., and Feinmark, S. J. (1991) Desensitization of the leukotriene B4 receptor by partial agonists. Adv. Prostaglandin Thromboxane Leukot. Res. 21A, 403-406
55. Serhan, C. N., and Petasis, N. A. (2011) Resolvins and protectins in inflammation resolution. Chem. Rev. 111, 5922-5943
56. Serhan, C. N., and Savill, J. (2005) Resolution of inflammation: the beginning programs the end. Nat. Immunol. 6, 1191-1197
57. Zeldin, D. C. (2001) Epoxygenase pathways of arachidonic acid metabolism. J. Biol. Chem. 276, 36059-36062
58. Zeldin, D. C., Dubois, R. N., Falck, J. R., and Capdevila, J. H. (1995) Molecular cloning, expression and characterization of an endogenous human cytochrome P450 arachidonic acid epoxygenase isoform. Arch. Biochem. Biophys. 322, 76-86
59. Keeney, D. S., Skinner, C., Wei, S., Friedberg, T., and Waterman, M. R. (1998) A keratinocyte-specific epoxygenase, CYP2B12, metabolizes arachidonic acid with unusual selectivity, producing a single major epoxyeicosatrienoic acid. J. Biol. Chem. 273, 9279-9284
60. Patel, L., Sullivan, M. H., and Elder, M. G. (1989) Production of epoxygenase metabolite by human reproductive tissues. Prostaglandins 38, 615-624
61. Imig, J. D. (2012) Epoxides and soluble epoxide hydrolase in cardiovascular physiology. Physiol. Rev. 92, 101-130
62. Morisseau, C., and Hammock, B. D. (2013) Impact of soluble epoxide hydrolase and epoxyeicosanoids on human health. Annu. Rev. Pharmacol. Toxicol. 53, 37-58
63. Catella, F., Lawson, J. A., Fitzgerald, D. J., and FitzGerald, G. A. (1990) Endogenous biosynthesis of arachidonic acid epoxides in humans: increased formation in pregnancy-induced hypertension. Proc. Natl. Acad. Sci. U. S. A. 87, 5893-5897
64. Jiang, H., McGiff, J. C., Fava, C., Amen, G., Nesta, E., Zanconato, G., Quilley, J., and Minuz, P. (2013) Maternal and fetal epoxyeicosatrienoic acids in normotensive and preeclamptic pregnancies. Am. J. Hypertens. 26, 271-278
65. Pearson, T., Zhang, J., Arya, P., Warren, A. Y., Ortori, C., Fakis, A., Khan, R. N., and Barrett, D. A. (2010) Measurement of vasoactive metabolites (hydroxyeicosatetraenoic and epoxyeicosatrienoic acids) in uterine tissues of normal and compromised human pregnancy. J. Hypertens. 28, 2429-2437
66. Herse, F., Lamarca, B., Hubel, C. A., Kaartokallio, T., Lokki, A. I., Ekholm, E., Laivuori, H., Gauster, M., Huppertz, B., Sugulle, M., Ryan, M. J., Novotny, S., Brewer, J., Park, J. K., Kacik, M., Hoyer, J., Verlohren, S., Wallukat, G., Rothe, M., Luft, F. C., Muller, D. N., Schunck, W. H., Staff, A. C., and Dechend, R. (2012) Cytochrome P450 subfamily 2J polypeptide 2 expression and circulating epoxyeicosatrienoic metabolites in preeclampsia. Circulation 126, 2990-2999
67. Node, K., Huo, Y., Ruan, X., Yang, B., Spiecker, M., Ley, K., Zeldin, D. C., and Liao, J. K. (1999) Anti-inflammatory properties of cytochrome P450 epoxygenase-derived eicosanoids. Science 285, 1276-1279
68. Fisslthaler, B., Popp, R., Kiss, L., Potente, M., Harder, D. R., Fleming, I., and Busse, R. (1999) Cytochrome P450 2C is an EDHF synthase in coronary arteries. Nature 401, 493-497
69. Campbell, W. B., and Falck, J. R. (2007) Arachidonic acid metabolites as endothelium-derived hyperpolarizing factors. Hypertension 49, 590-596
70. Earley, S., Heppner, T. J., Nelson, M. T., and Brayden, J. E. (2005) TRPV4 forms a novel Ca2+ signaling complex with ryanodine receptors and BKCa channels. Circ. Res. 97, 1270-1279
71. Spiecker, M., and Liao, J. (2006) Cytochrome P450 epoxygenase CYP2J2 and the risk of coronary artery disease. Trends Cardiovasc. Med. 16, 204-208
72. Gonzalez, E., Jawerbaum, A., Novaro, V., and Gimeno, M. A. (1997) Influence of epoxyeicosatrienoic acids on uterine function. Prostaglandins Leukot. Essent. Fatty Acids 56, 57-61
73. Roman, R. J., Maier, K. G., Sun, C.-W., Harder, D. R., and Alonso-Galicia, M. (2000) Renal and cardiovascular actions of 20-hydroxyeicosatetraenoic acid and epoxyeicosatrienoic acids. Clin. Exp. Pharmacol. Physiol. 27, 855-865
74. Pearson, T., Warren, A. Y., Barrett, D. A., and Khan, R. N. (2009) Detection of EETs and HETE-generating cytochrome P-450 enzymes and the effects of their metabolites on myometrial and vascular function. Am. J. Physiol. Endocrinol. Metab. 297, E647-E656
75. Enayetallah, A. E., French, R. A., Thibodeau, M. S., and Grant, D. F. (2004) Distribution of soluble epoxide hydrolase and of cytochrome P450 2C8, 2C9, and 2J2 in human tissues. J. Histochem. Cytochem. 52, 447-454
76. Zhang, J.-H., Pearson, T., Matharoo-Ball, B., Ortori, C. A., Warren, A. Y., Khan, R., and Barrett, D. A. (2007) Quantitative profiling of epoxyeicosatrienoic, hydroxyeicosatetraenoic, and dihydroxyeicosatetraenoic acids in human intrauterine tissues using liquid chromatography/electrospray ionization tandem mass spectrometry. Anal. Biochem. 365, 40-51
77. Gaedigk, A., Baker, D. W., Totah, R. A., Gaedigk, R., Pearce, R. E., Vyhlidal, C. A., Zeldin, D. C., and Leeder, J. S. (2006) Variability of CYP2J2 expression in human fetal tissues. J. Pharmacol. Exp. Ther. 319, 523-532
78. Strickland, D. M., Saeed, S. A., Casey, M. L., and Mitchell, M. D. (1983) Stimulation of prostaglandin biosynthesis by urine of the human fetus may serve as a trigger for parturition. Science 220, 521-522
79. MacDonald, P. C., and Casey, M. L. (1993) The accumulation of prostaglandins (PG) in amniotic fluid is an aftereffect of labor and not indicative of a role for PGE2 or PGF2 alpha in the initiation of human parturition. J. Clin. Endocrinol. Metab. 76, 1332-1339
80. Kinoshita, K., Satoh, K., and Sakamoto, S. (1977) Prostaglandin F2α and E1 in plasma and amniotic fluid during human pregnancy and labor. Endocrinol. Jpn. 24, 155-162
81. Satoh, K., Yasumizu, T., Fukuoka, H., Kinoshita, K., Kaneko, Y., Tsuchiya, M., and Sakamoto, S. (1979) Prostaglandin F2 alpha metabolite levels in plasma, amniotic fluid, and urine during pregnancy and labor. Am. J. Obstet. Gynecol. 133, 886-890