Skip to main content
Biochemical Journal logoLink to Biochemical Journal
. 1994 Jul 15;301(Pt 2):361–366. doi: 10.1042/bj3010361

Oestradiol-induced changes in the composition of phospholipid classes of quail oviduct: specific replacement of arachidonic acid by docosahexaenoic acid in alkenylacyl-glycerophosphoethanolamine.

B E Felouati 1, J F Pageaux 1, J M Fayard 1, M Lagarde 1, C Laugier 1
PMCID: PMC1137088  PMID: 8042978

Abstract

The phospholipid composition and the molecular species of the major subclasses of ethanolamine and choline glycerophospholipids were determined during the natural or oestradiol-induced development of the quail oviduct. The phospholipid concentration increased significantly during oviduct development, and the proportion of ethanolamine glycerophospholipids (EPL) remained constant while that of choline glycerophospholipids increased. The immature oviduct contained the majority of its endogenous arachidonic acid mass (71%) in EPL, mainly in alkenylacyl-glycerophosphoethanolamine (alkenylacyl-GPE) (49% of the total). Oestrogen treatment induced the depletion of 20:4,n-6 specifically from this pool, which indicates the biological importance of 20:4,n-6 molecular species in alkenylacyl-GPE as substrates for the oviduct phospholipases activated by oestradiol, and suggests that this EPL subclass is involved in the oestrogen-induced cell proliferation. Another striking result was the marked increase in 22:6,n-3 EPL molecular species following the oestradiol treatment and more particularly the strict substitution of 20:4,n-6 by 22:6,n-3 in alkenylacyl-GPE. We speculate that alkenylacyl-GPE molecular species containing 22:6,n-3 may participate in the arrest of oestrogen-induced proliferation.

Full text

PDF
361

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Albert D. H., Snyder F. Release of arachidonic acid from 1-alkyl-2-acyl-sn-glycero-3-phosphocholine, a precursor of platelet-activating factor, in rat alveolar macrophages. Biochim Biophys Acta. 1984 Oct 24;796(1):92–101. doi: 10.1016/0005-2760(84)90242-x. [DOI] [PubMed] [Google Scholar]
  2. Angle M. J., Jones M. A., McManus L. M., Pinckard R. N., Harper M. J. Platelet-activating factor in the rabbit uterus during early pregnancy. J Reprod Fertil. 1988 Jul;83(2):711–722. doi: 10.1530/jrf.0.0830711. [DOI] [PubMed] [Google Scholar]
  3. Blank M. L., Robinson M., Fitzgerald V., Snyder F. Novel quantitative method for determination of molecular species of phospholipids and diglycerides. J Chromatogr. 1984 Aug 31;298(3):473–482. doi: 10.1016/s0021-9673(01)92744-x. [DOI] [PubMed] [Google Scholar]
  4. Boisvieux-Ulrich E., Laugier C., Sandoz D. Opposite effects of glucocorticoid on estrogen-induced growth and differentiation of quail oviduct: demonstration by sequential treatments. Biol Cell. 1984;51(3):335–346. doi: 10.1111/j.1768-322x.1984.tb00312.x. [DOI] [PubMed] [Google Scholar]
  5. Bonney R. C., Qizilbash S. T., Franks S. Endometrial phospholipase A2 enzymes and their regulation by steroid hormones. J Steroid Biochem. 1987;27(4-6):1057–1064. doi: 10.1016/0022-4731(87)90190-7. [DOI] [PubMed] [Google Scholar]
  6. Braquet P., Touqui L., Shen T. Y., Vargaftig B. B. Perspectives in platelet-activating factor research. Pharmacol Rev. 1987 Jun;39(2):97–145. [PubMed] [Google Scholar]
  7. Brown M. L., Jakubowski J. A., Leventis L. L., Deykin D. Ionophore-induced metabolism of phospholipids and eicosanoid production in porcine aortic endothelial cells: selective release of arachidonic acid from diacyl and ether phospholipids. Biochim Biophys Acta. 1987 Sep 25;921(2):159–166. doi: 10.1016/0005-2760(87)90014-2. [DOI] [PubMed] [Google Scholar]
  8. Croset M., Bayon Y., Lagarde M. Incorporation and turnover of eicosapentaenoic and docosahexaenoic acids in human blood platelets in vitro. Biochem J. 1992 Jan 15;281(Pt 2):309–316. doi: 10.1042/bj2810309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Croset M., Lagarde M. In vitro incorporation and metabolism of icosapentaenoic and docosahexaenoic acids in human platelets--effect on aggregation. Thromb Haemost. 1986 Aug 20;56(1):57–62. [PubMed] [Google Scholar]
  10. Croset M., Sala A., Folco G., Lagarde M. Inhibition by lipoxygenase products of TXA2-like responses of platelets and vascular smooth muscle. 14-Hydroxy from 22:6n-3 is more potent than 12-HETE. Biochem Pharmacol. 1988 Apr 1;37(7):1275–1280. doi: 10.1016/0006-2952(88)90782-4. [DOI] [PubMed] [Google Scholar]
  11. Daniel L. W., King L., Waite M. Source of arachidonic acid for prostaglandin synthesis in Madin-Darby canine kidney cells. J Biol Chem. 1981 Dec 25;256(24):12830–12835. [PubMed] [Google Scholar]
  12. Dey S. K., Hoversland R. C., Johnson D. C. Phospholipase A2 activity in the rat uterus: modulation by steroid hormones. Prostaglandins. 1982 May;23(5):619–630. doi: 10.1016/s0090-6980(82)80002-6. [DOI] [PubMed] [Google Scholar]
  13. Eldering J. A., Nay M. G., Hoberg L. M., Longcope C., McCracken J. A. Hormonal regulation of prostaglandin production by rhesus monkey endometrium. J Clin Endocrinol Metab. 1990 Sep;71(3):596–604. doi: 10.1210/jcem-71-3-596. [DOI] [PubMed] [Google Scholar]
  14. Fischer S., von Schacky C., Siess W., Strasser T., Weber P. C. Uptake, release and metabolism of docosahexaenoic acid (DHA, c22:6 omega 3) in human platelets and neutrophils. Biochem Biophys Res Commun. 1984 May 16;120(3):907–918. doi: 10.1016/s0006-291x(84)80193-x. [DOI] [PubMed] [Google Scholar]
  15. Ford D. A., Gross R. W. Plasmenylethanolamine is the major storage depot for arachidonic acid in rabbit vascular smooth muscle and is rapidly hydrolyzed after angiotensin II stimulation. Proc Natl Acad Sci U S A. 1989 May;86(10):3479–3483. doi: 10.1073/pnas.86.10.3479. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Grove R. I., Korach K. S. Estrogen stimulation of phosphatidylinositol metabolism in mouse uterine tissue. Endocrinology. 1987 Sep;121(3):1083–1088. doi: 10.1210/endo-121-3-1083. [DOI] [PubMed] [Google Scholar]
  17. Imagawa W., Bandyopadhyay G. K., Wallace D., Nandi S. Phospholipids containing polyunsaturated fatty acyl groups are mitogenic for normal mouse mammary epithelial cells in serum-free primary cell culture. Proc Natl Acad Sci U S A. 1989 Jun;86(11):4122–4126. doi: 10.1073/pnas.86.11.4122. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Juaneda P., Rocquelin G. Rapid and convenient separation of phospholipids and non phosphorus lipids from rat heart using silica cartridges. Lipids. 1985 Jan;20(1):40–41. doi: 10.1007/BF02534360. [DOI] [PubMed] [Google Scholar]
  19. Kerr M. B., Marshall K., Senior J. The effects of thromboxane receptor antagonists on oestrogen-induced uterotrophic responses in the spontaneously hypertensive rat. Br J Pharmacol. 1991 Jun;103(2):1363–1366. doi: 10.1111/j.1476-5381.1991.tb09794.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kudolo G. B., Harper M. J. Characterization of platelet-activating factor binding sites on uterine membranes from pregnant rabbits. Biol Reprod. 1989 Oct;41(4):587–603. doi: 10.1095/biolreprod41.4.587. [DOI] [PubMed] [Google Scholar]
  21. Loeb L. A., Gross R. W. Identification and purification of sheep platelet phospholipase A2 isoforms. Activation by physiologic concentrations of calcium ion. J Biol Chem. 1986 Aug 15;261(23):10467–10470. [PubMed] [Google Scholar]
  22. Nakagawa Y., Horrocks L. A. Separation of alkenylacyl, alkylacyl, and diacyl analogues and their molecular species by high performance liquid chromatography. J Lipid Res. 1983 Sep;24(9):1268–1275. [PubMed] [Google Scholar]
  23. Nakayama R., Yasuda K., Okumura T., Saito K. Effect of 17 beta-estradiol on PAF and prostaglandin levels in oophorectomized rat uterus. Biochim Biophys Acta. 1991 Sep 11;1085(2):235–240. doi: 10.1016/0005-2760(91)90099-4. [DOI] [PubMed] [Google Scholar]
  24. Pageaux J. F., Laugier C., Pal D., D'Almeida M. A., Sandoz D., Pacheco H. Magnum morphogenesis during the natural development of the quail oviduct: analysis of egg white proteins and progesterone receptor concentration. Biol Reprod. 1986 Oct;35(3):657–666. doi: 10.1095/biolreprod35.3.657. [DOI] [PubMed] [Google Scholar]
  25. Pageaux J. F., Laugier C., Pal D., Pacheco H. Development of the oviduct in quail during sexual maturation in relation to plasma concentrations of oestradiol and progesterone. J Endocrinol. 1984 Feb;100(2):167–173. doi: 10.1677/joe.0.1000167. [DOI] [PubMed] [Google Scholar]
  26. Pakrasi P. L., Cheng H. C., Dey S. K. Prostaglandins in the uterus: modulation by steroid hormones. Prostaglandins. 1983 Dec;26(6):991–1009. doi: 10.1016/0090-6980(83)90160-0. [DOI] [PubMed] [Google Scholar]
  27. Patton G. M., Fasulo J. M., Robins S. J. Separation of phospholipids and individual molecular species of phospholipids by high-performance liquid chromatography. J Lipid Res. 1982 Jan;23(1):190–196. [PubMed] [Google Scholar]
  28. Patton G. M., Robins S. J. Extraction of phospholipids and analysis of phospholipid molecular species. Methods Enzymol. 1990;187:195–215. doi: 10.1016/0076-6879(90)87025-x. [DOI] [PubMed] [Google Scholar]
  29. Rittenhouse-Simmons S., Russell R. A., Deykin D. Transfer of arachidonic acid to human platelet plasmalogen in response to thrombin. Biochem Biophys Res Commun. 1976 May 3;70(1):295–301. doi: 10.1016/0006-291x(76)91141-4. [DOI] [PubMed] [Google Scholar]
  30. Rose D. P., Connolly J. M. Effects of fatty acids and eicosanoid synthesis inhibitors on the growth of two human prostate cancer cell lines. Prostate. 1991;18(3):243–254. doi: 10.1002/pros.2990180306. [DOI] [PubMed] [Google Scholar]
  31. Rose D. P., Connolly J. M. Effects of fatty acids and inhibitors of eicosanoid synthesis on the growth of a human breast cancer cell line in culture. Cancer Res. 1990 Nov 15;50(22):7139–7144. [PubMed] [Google Scholar]
  32. Spaargaren M., Wissink S., Defize L. H., de Laat S. W., Boonstra J. Characterization and identification of an epidermal-growth-factor-activated phospholipase A2. Biochem J. 1992 Oct 1;287(Pt 1):37–43. doi: 10.1042/bj2870037. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Stacey K., Beasley B., Wilce P. A., Martin L. Effects of female sex hormones on lipid metabolism in the uterine epithelium of the mouse. Int J Biochem. 1991;23(3):371–376. doi: 10.1016/0020-711x(91)90121-3. [DOI] [PubMed] [Google Scholar]
  34. Tóth M., Hertelendy F. Differential effect of progesterone on the labeling of phosphatidylinositol with [3H]inositol and [32P]phosphate in the uterus of the estrogen-treated ovariectomized rat. J Steroid Biochem. 1987 Dec;28(6):629–635. doi: 10.1016/0022-4731(87)90390-6. [DOI] [PubMed] [Google Scholar]
  35. Wolf R. A., Gross R. W. Identification of neutral active phospholipase C which hydrolyzes choline glycerophospholipids and plasmalogen selective phospholipase A2 in canine myocardium. J Biol Chem. 1985 Jun 25;260(12):7295–7303. [PubMed] [Google Scholar]
  36. Yasuda K., Satouchi K., Saito K. Platelet-activating factor in normal rat uterus. Biochem Biophys Res Commun. 1986 Aug 14;138(3):1231–1236. doi: 10.1016/s0006-291x(86)80414-4. [DOI] [PubMed] [Google Scholar]
  37. Yee G. M., Squires P. M., Cejic S. S., Kennedy T. G. Lipid mediators of implantation and decidualization. J Lipid Mediat. 1993 Mar-Apr;6(1-3):525–534. [PubMed] [Google Scholar]
  38. van Corven E. J., Groenink A., Jalink K., Eichholtz T., Moolenaar W. H. Lysophosphatidate-induced cell proliferation: identification and dissection of signaling pathways mediated by G proteins. Cell. 1989 Oct 6;59(1):45–54. doi: 10.1016/0092-8674(89)90868-4. [DOI] [PubMed] [Google Scholar]

Articles from Biochemical Journal are provided here courtesy of The Biochemical Society

RESOURCES