#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

A Heterogeneous Mixture of F-Series Prostaglandins Promotes Sperm Guidance in the Reproductive Tract


The mechanisms that guide motile sperm through the female reproductive tract to oocytes are not well understood. We have shown that Caenorhabditis elegans oocytes synthesize sperm guiding F-series prostaglandins from polyunsaturated fatty acid (PUFA) precursors provided in yolk lipoprotein complexes. Here we use genetics and electrospray ionization tandem mass spectrometry to partially delineate F-series prostaglandin metabolism pathways. We show that omega-6 and omega-3 PUFAs, including arachidonic and eicosapentaenoic acids, are converted into more than 10 structurally related F-series prostaglandins, which function collectively and largely redundantly to promote sperm guidance. Disruption of omega-3 PUFA synthesis triggers compensatory up-regulation of prostaglandins derived from omega-6 PUFAs. C. elegans F-series prostaglandin synthesis involves biochemical mechanisms distinct from those in mammalian cyclooxygenase-dependent pathways, yet PGF stereoisomers are still synthesized. A comparison of F-series prostaglandins in C. elegans and mouse tissues reveals shared features. Finally, we show that a conserved cytochrome P450 enzyme, whose human homolog is implicated in Bietti's Crystalline Dystrophy, negatively regulates prostaglandin synthesis. These results support the model that multiple cyclooxygenase-independent prostaglandins function together to promote sperm motility important for fertilization. This cyclooxygenase-independent pathway for F-series synthesis may be conserved.


Vyšlo v časopise: A Heterogeneous Mixture of F-Series Prostaglandins Promotes Sperm Guidance in the Reproductive Tract. PLoS Genet 9(1): e32767. doi:10.1371/journal.pgen.1003271
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1003271

Souhrn

The mechanisms that guide motile sperm through the female reproductive tract to oocytes are not well understood. We have shown that Caenorhabditis elegans oocytes synthesize sperm guiding F-series prostaglandins from polyunsaturated fatty acid (PUFA) precursors provided in yolk lipoprotein complexes. Here we use genetics and electrospray ionization tandem mass spectrometry to partially delineate F-series prostaglandin metabolism pathways. We show that omega-6 and omega-3 PUFAs, including arachidonic and eicosapentaenoic acids, are converted into more than 10 structurally related F-series prostaglandins, which function collectively and largely redundantly to promote sperm guidance. Disruption of omega-3 PUFA synthesis triggers compensatory up-regulation of prostaglandins derived from omega-6 PUFAs. C. elegans F-series prostaglandin synthesis involves biochemical mechanisms distinct from those in mammalian cyclooxygenase-dependent pathways, yet PGF stereoisomers are still synthesized. A comparison of F-series prostaglandins in C. elegans and mouse tissues reveals shared features. Finally, we show that a conserved cytochrome P450 enzyme, whose human homolog is implicated in Bietti's Crystalline Dystrophy, negatively regulates prostaglandin synthesis. These results support the model that multiple cyclooxygenase-independent prostaglandins function together to promote sperm motility important for fertilization. This cyclooxygenase-independent pathway for F-series synthesis may be conserved.


Zdroje

1. EvansJP, FlormanHM (2002) The state of the union: the cell biology of fertilization. Nat Cell Biol 4 Suppl: s57–63.

2. MarcelloMR, SingaraveluG, SingsonA (2013) Fertilization. Adv Exp Med Biol 757: 321–350.

3. GadellaBM, EvansJP (2011) Membrane fusions during mammalian fertilization. Adv Exp Med Biol 713: 65–80.

4. HanSM, CotteePA, MillerMA (2010) Sperm and oocyte communication mechanisms controlling C. elegans fertility. Dev Dyn 239: 1265–1281.

5. KauppUB, KashikarND, WeyandI (2008) Mechanisms of sperm chemotaxis. Annu Rev Physiol 70: 93–117.

6. GuerreroA, WoodCD, NishigakiT, CarneiroJ, DarszonA (2010) Tuning sperm chemotaxis. Biochem Soc Trans 38: 1270–1274.

7. ChangH, SuarezSS (2010) Rethinking the relationship between hyperactivation and chemotaxis in mammalian sperm. Biol Reprod 83: 507–513.

8. EisenbachM, GiojalasLC (2006) Sperm guidance in mammals - an unpaved road to the egg. Nat Rev Mol Cell Biol 7: 276–285.

9. LishkoPV, BotchkinaIL, KirichokY (2011) Progesterone activates the principal Ca2+ channel of human sperm. Nature 471: 387–391.

10. StrunkerT, GoodwinN, BrenkerC, KashikarND, WeyandI, et al. (2011) The CatSper channel mediates progesterone-induced Ca2+ influx in human sperm. Nature 471: 382–386.

11. TevesME, GuidobaldiHA, UnatesDR, SanchezR, MiskaW, et al. (2009) Molecular mechanism for human sperm chemotaxis mediated by progesterone. PLoS ONE 4: e8211 doi:10.1371/journal.pone.0008211.

12. BrenkerC, GoodwinN, WeyandI, KashikarND, NaruseM, et al. (2012) The CatSper channel: a polymodal chemosensor in human sperm. EMBO J 31: 1654–1665.

13. SchuetzAW, DubinNH (1981) Progesterone and prostaglandin secretion by ovulated rat cumulus cell-oocyte complexes. Endocrinology 108: 457–463.

14. L'HernaultSW (2009) The genetics and cell biology of spermatogenesis in the nematode C. elegans. Mol Cell Endocrinol 306: 59–65.

15. StanfieldGM, VilleneuveAM (2006) Regulation of sperm activation by SWM-1 is required for reproductive success of C. elegans males. Curr Biol 16: 252–263.

16. KimS, SpikeC, GreensteinD (2013) Control of Oocyte Growth and Meiotic Maturation in Caenorhabditis elegans. Adv Exp Med Biol 757: 277–320.

17. HillKL, L'HernaultSW (2001) Analyses of reproductive interactions that occur after heterospecific matings within the genus Caenorhabditis. Dev Biol 232: 105–114.

18. KubagawaHM, WattsJL, CorriganC, EdmondsJW, SztulE, et al. (2006) Oocyte signals derived from polyunsaturated fatty acids control sperm recruitment in vivo. Nat Cell Biol 8: 1143–1148.

19. WardS, CarrelJS (1979) Fertilization and sperm competition in the nematode Caenorhabditis elegans. Dev Biol 73: 304–321.

20. EdmondsJW, PrasainJK, DorandD, YangY, HoangHD, et al. (2010) Insulin/FOXO signaling regulates ovarian prostaglandins critical for reproduction. Dev Cell 19: 858–871.

21. EdmondsJW, McKinneySL, PrasainJK, MillerMA (2011) The gap junctional protein INX-14 functions in oocyte precursors to promote C. elegans sperm guidance. Dev Biol 359: 47–58.

22. FunkCD (2001) Prostaglandins and leukotrienes: advances in eicosanoid biology. Science 294: 1871–1875.

23. BurrGO, BurrMM (1929) A new deficiency disease produced by the rigid exclusion of fat from the diet. J Biol Chem 82: 345–367.

24. BurrGO, BurrMM (1930) On the nature and role of the fatty acids essential for nutrition. J Biol Chem 86: 587–621.

25. VaneJR, BakhleYS, BottingRM (1998) Cyclooxygenases 1 and 2. Annu Rev Pharmacol Toxicol 38: 97–120.

26. WathesDC, AbayasekaraDR, AitkenRJ (2007) Polyunsaturated fatty acids in male and female reproduction. Biology of reproduction 77: 190–201.

27. BergstromS, DanielssonH, KlenbergD, SamuelssonB (1964) The enzymatic conversion of essential fatty acids into prostaglandins. J Biol Chem 239: PC4006–4008.

28. HambergM, SamuelssonB (1967) On the mechanism of the biosynthesis of prostaglandins E-1 and F-1-alpha. J Biol Chem 242: 5336–5343.

29. WatanabeK (2002) Prostaglandin F synthase. Prostaglandins Other Lipid Mediat 68–69: 401–407.

30. MilneGL, YinH, MorrowJD (2008) Human biochemistry of the isoprostane pathway. J Biol Chem 283: 15533–15537.

31. WattsJL (2009) Fat synthesis and adiposity regulation in Caenorhabditis elegans. Trends Endocrinol Metab 20: 58–65.

32. WattsJL, BrowseJ (2002) Genetic dissection of polyunsaturated fatty acid synthesis in Caenorhabditis elegans. Proc Natl Acad Sci U S A 99: 5854–5859.

33. Kahn-KirbyAH, DantzkerJL, ApicellaAJ, SchaferWR, BrowseJ, et al. (2004) Specific polyunsaturated fatty acids drive TRPV-dependent sensory signaling in vivo. Cell 119: 889–900.

34. GrantB, HirshD (1999) Receptor-mediated endocytosis in the Caenorhabditis elegans oocyte. Mol Biol Cell 10: 4311–4326.

35. BeananMJ, StromeS (1992) Characterization of a germ-line proliferation mutation in C. elegans. Development 116: 755–766.

36. MurphyRC, BarkleyRM, Zemski BerryK, HankinJ, HarrisonK, et al. (2005) Electrospray ionization and tandem mass spectrometry of eicosanoids. Anal Biochem 346: 1–42.

37. MasoodiM, NicolaouA (2006) Lipidomic analysis of twenty-seven prostanoids and isoprostanes by liquid chromatography/electrospray tandem mass spectrometry. Rapid Commun Mass Spectrom 20: 3023–3029.

38. KingsleyPJ, RouzerCA, SalehS, MarnettLJ (2005) Simultaneous analysis of prostaglandin glyceryl esters and prostaglandins by electrospray tandem mass spectrometry. Anal Biochem 343: 203–211.

39. WattsJL, BrowseJ (2000) A palmitoyl-CoA-specific delta9 fatty acid desaturase from Caenorhabditis elegans. Biochem Biophys Res Commun 272: 263–269.

40. WaughRJ, MorrowJD, RobertsLJ2nd, MurphyRC (1997) Identification and relative quantitation of F2-isoprostane regioisomers formed in vivo in the rat. Free Radic Biol Med 23: 943–954.

41. BenenatiG, PenkovS, Muller-ReichertT, EntchevEV, KurzchaliaTV (2009) Two cytochrome P450s in Caenorhabditis elegans are essential for the organization of eggshell, correct execution of meiosis and the polarization of embryo. Mech Dev 126: 382–393.

42. OlsonSK, GreenanG, DesaiA, Muller-ReichertT, OegemaK (2012) Hierarchical assembly of the eggshell and permeability barrier in C. elegans. J Cell Biol 198: 731–748.

43. HsuMH, SavasU, GriffinKJ, JohnsonEF (2007) Human cytochrome p450 family 4 enzymes: function, genetic variation and regulation. Drug Metab Rev 39: 515–538.

44. YinH, GaoL, TaiHH, MurpheyLJ, PorterNA, et al. (2007) Urinary prostaglandin F2alpha is generated from the isoprostane pathway and not the cyclooxygenase in humans. J Biol Chem 282: 329–336.

45. WhittenSJ, MillerMA (2007) The role of gap junctions in Caenorhabditis elegans oocyte maturation and fertilization. Dev Biol 301: 432–446.

46. YinH, GaoL, TaiHH, MurpheyLJ, PorterNA, et al. (2007) Urinary prostaglandin F2alpha is generated from the isoprostane pathway and not the cyclooxygenase in humans. J Biol Chem 282: 329–336.

47. LiA, JiaoX, MunierFL, SchorderetDF, YaoW, et al. (2004) Bietti crystalline corneoretinal dystrophy is caused by mutations in the novel gene CYP4V2. Am J Hum Genet 74: 817–826.

48. NakanoM, KellyEJ, WiekC, HanenbergH, RettieAE (2012) CYP4V2 in Bietti's Crystalline Dystrophy: Ocular Localization, Metabolism of omega-3-Polyunsaturated Fatty Acids, and Functional Deficit of the p.H331P Variant. Mol Pharmacol 82: 679–686.

49. KulasJ, SchmidtC, RotheM, SchunckWH, MenzelR (2008) Cytochrome P450-dependent metabolism of eicosapentaenoic acid in the nematode Caenorhabditis elegans. Arch Biochem Biophys 472: 65–75.

50. LishkoPV, KirichokY, RenD, NavarroB, ChungJJ, et al. (2012) The control of male fertility by spermatozoan ion channels. Annu Rev Physiol 74: 453–475.

51. RenD, NavarroB, PerezG, JacksonAC, HsuS, et al. (2001) A sperm ion channel required for sperm motility and male fertility. Nature 413: 603–609.

52. QuillTA, RenD, ClaphamDE, GarbersDL (2001) A voltage-gated ion channel expressed specifically in spermatozoa. Proc Natl Acad Sci U S A 98: 12527–12531.

53. AitkenRJ, KellyRW (1985) Analysis of the direct effects of prostaglandins on human sperm function. J Reprod Fertil 73: 139–146.

54. GottliebC, SvanborgK, EnerothP, BygdemanM (1988) Effect of prostaglandins on human sperm function in vitro and seminal adenosine triphosphate content. Fertil Steril 49: 322–327.

55. TimmonsL, FireA (1998) Specific interference by ingested dsRNA. Nature 395: 854.

56. KamathRS, AhringerJ (2003) Genome-wide RNAi screening in Caenorhabditis elegans. Methods 30: 313–321.

57. Porta-de-la-RivaM, FontrodonaL, VillanuevaA, CeronJ (2012) Basic Caenorhabditis elegans methods: synchronization and observation. J Vis Exp e4019.

58. McCarterJ, BartlettB, DangT, SchedlT (1999) On the control of oocyte meiotic maturation and ovulation in Caenorhabditis elegans. Dev Biol 205: 111–128.

59. GolovkoMY, MurphyEJ (2008) An improved LC-MS/MS procedure for brain prostanoid analysis using brain fixation with head-focused microwave irradiation and liquid-liquid extraction. J Lipid Res 49: 893–902.

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2013 Číslo 1
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Získaná hemofilie - Povědomí o nemoci a její diagnostika
nový kurz

Eozinofilní granulomatóza s polyangiitidou
Autori: doc. MUDr. Martina Doubková, Ph.D.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#