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

PLoS Genetics

Volumn 9, Issue 1, 2013, Pages

  Hoang, Hieu D ^a   Prasain, Jeevan K ^b   Dorand, Dixon ^a   Miller, Michael A ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b University of Alabama at Birmingham   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARACHIDONIC ACID; CYTOCHROME P450; ICOSAPENTAENOIC ACID; OMEGA 3 FATTY ACID; OMEGA 6 FATTY ACID; PROSTAGLANDIN F; PROSTAGLANDIN F2 ALPHA; PROSTAGLANDIN SYNTHASE;

ANIMAL TISSUE; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; ELECTROSPRAY MASS SPECTROMETRY; FATTY ACID SYNTHESIS; GENETIC ANALYSIS; MALE; MALE GENITAL SYSTEM; MOUSE; NONHUMAN; PROSTAGLANDIN METABOLISM; PROSTAGLANDIN SYNTHESIS; SEQUENCE HOMOLOGY; SPECIES COMPARISON; SPERMATOZOON MOTILITY; STEREOISOMERISM; TANDEM MASS SPECTROMETRY;

ANIMALS; ARACHIDONIC ACIDS; CAENORHABDITIS ELEGANS; CYTOCHROME P-450 ENZYME SYSTEM; FATTY ACIDS, OMEGA-3; FATTY ACIDS, OMEGA-6; FEMALE; HUMANS; MALE; MICE; OOCYTES; PROSTAGLANDINS F; REPRODUCTION; SPERM MOTILITY; SPERMATOZOA;

EID: 84873503741     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003271     Document Type: Article

References (59)

1. Evans JP, Florman HM, (2002) The state of the union: the cell biology of fertilization. Nat Cell Biol 4 Suppl: s57-63.
2. Marcello MR, Singaravelu G, Singson A, (2013) Fertilization. Adv Exp Med Biol 757: 321-350.
3. Gadella BM, Evans JP, (2011) Membrane fusions during mammalian fertilization. Adv Exp Med Biol 713: 65-80.
4. Han SM, Cottee PA, Miller MA, (2010) Sperm and oocyte communication mechanisms controlling C. elegans fertility. Dev Dyn 239: 1265-1281.
5. Kaupp UB, Kashikar ND, Weyand I, (2008) Mechanisms of sperm chemotaxis. Annu Rev Physiol 70: 93-117.
6. Guerrero A, Wood CD, Nishigaki T, Carneiro J, Darszon A, (2010) Tuning sperm chemotaxis. Biochem Soc Trans 38: 1270-1274.
7. Chang H, Suarez SS, (2010) Rethinking the relationship between hyperactivation and chemotaxis in mammalian sperm. Biol Reprod 83: 507-513.
8. Eisenbach M, Giojalas LC, (2006) Sperm guidance in mammals- an unpaved road to the egg. Nat Rev Mol Cell Biol 7: 276-285.
9. Lishko PV, Botchkina IL, Kirichok Y, (2011) Progesterone activates the principal Ca2+ channel of human sperm. Nature 471: 387-391.
10. Strunker T, Goodwin N, Brenker C, Kashikar ND, Weyand I, et al. (2011) The CatSper channel mediates progesterone-induced Ca2+ influx in human sperm. Nature 471: 382-386.
11. Teves ME, Guidobaldi HA, Unates DR, Sanchez R, Miska W, et al. (2009) Molecular mechanism for human sperm chemotaxis mediated by progesterone. PLoS ONE 4: e8211 doi:10.1371/journal.pone.0008211.
12. Brenker C, Goodwin N, Weyand I, Kashikar ND, Naruse M, et al. (2012) The CatSper channel: a polymodal chemosensor in human sperm. EMBO J 31: 1654-1665.
13. Schuetz AW, Dubin NH, (1981) Progesterone and prostaglandin secretion by ovulated rat cumulus cell-oocyte complexes. Endocrinology 108: 457-463.
14. L'Hernault SW, (2009) The genetics and cell biology of spermatogenesis in the nematode C. elegans. Mol Cell Endocrinol 306: 59-65.
15. Stanfield GM, Villeneuve AM, (2006) Regulation of sperm activation by SWM-1 is required for reproductive success of C. elegans males. Curr Biol 16: 252-263.
16. Kim S, Spike C, Greenstein D, (2013) Control of Oocyte Growth and Meiotic Maturation in Caenorhabditis elegans. Adv Exp Med Biol 757: 277-320.
17. Hill KL, L'Hernault SW, (2001) Analyses of reproductive interactions that occur after heterospecific matings within the genus Caenorhabditis. Dev Biol 232: 105-114.
18. Kubagawa HM, Watts JL, Corrigan C, Edmonds JW, Sztul E, et al. (2006) Oocyte signals derived from polyunsaturated fatty acids control sperm recruitment in vivo. Nat Cell Biol 8: 1143-1148.
19. Ward S, Carrel JS, (1979) Fertilization and sperm competition in the nematode Caenorhabditis elegans. Dev Biol 73: 304-321.
20. Edmonds JW, Prasain JK, Dorand D, Yang Y, Hoang HD, et al. (2010) Insulin/FOXO signaling regulates ovarian prostaglandins critical for reproduction. Dev Cell 19: 858-871.
21. Edmonds JW, McKinney SL, Prasain JK, Miller MA, (2011) The gap junctional protein INX-14 functions in oocyte precursors to promote C. elegans sperm guidance. Dev Biol 359: 47-58.
22. Funk CD, (2001) Prostaglandins and leukotrienes: advances in eicosanoid biology. Science 294: 1871-1875.
23. Burr GO, Burr MM, (1929) A new deficiency disease produced by the rigid exclusion of fat from the diet. J Biol Chem 82: 345-367.
24. Burr GO, Burr MM, (1930) On the nature and role of the fatty acids essential for nutrition. J Biol Chem 86: 587-621.
25. Vane JR, Bakhle YS, Botting RM, (1998) Cyclooxygenases 1 and 2. Annu Rev Pharmacol Toxicol 38: 97-120.
26. Wathes DC, Abayasekara DR, Aitken RJ, (2007) Polyunsaturated fatty acids in male and female reproduction. Biology of reproduction 77: 190-201.
27. Bergstrom S, Danielsson H, Klenberg D, Samuelsson B, (1964) The enzymatic conversion of essential fatty acids into prostaglandins. J Biol Chem 239: PC4006-4008.
28. Hamberg M, Samuelsson B, (1967) On the mechanism of the biosynthesis of prostaglandins E-1 and F-1-alpha. J Biol Chem 242: 5336-5343.
29. Watanabe K, (2002) Prostaglandin F synthase. Prostaglandins Other Lipid Mediat 68-69: 401-407.
30. Milne GL, Yin H, Morrow JD, (2008) Human biochemistry of the isoprostane pathway. J Biol Chem 283: 15533-15537.
31. Watts JL, (2009) Fat synthesis and adiposity regulation in Caenorhabditis elegans. Trends Endocrinol Metab 20: 58-65.
32. Watts JL, Browse J, (2002) Genetic dissection of polyunsaturated fatty acid synthesis in Caenorhabditis elegans. Proc Natl Acad Sci U S A 99: 5854-5859.
33. Kahn-Kirby AH, Dantzker JL, Apicella AJ, Schafer WR, Browse J, et al. (2004) Specific polyunsaturated fatty acids drive TRPV-dependent sensory signaling in vivo. Cell 119: 889-900.
34. Grant B, Hirsh D, (1999) Receptor-mediated endocytosis in the Caenorhabditis elegans oocyte. Mol Biol Cell 10: 4311-4326.
35. Beanan MJ, Strome S, (1992) Characterization of a germ-line proliferation mutation in C. elegans. Development 116: 755-766.
36. Murphy RC, Barkley RM, Zemski Berry K, Hankin J, Harrison K, et al. (2005) Electrospray ionization and tandem mass spectrometry of eicosanoids. Anal Biochem 346: 1-42.
37. Masoodi M, Nicolaou A, (2006) Lipidomic analysis of twenty-seven prostanoids and isoprostanes by liquid chromatography/electrospray tandem mass spectrometry. Rapid Commun Mass Spectrom 20: 3023-3029.
38. Kingsley PJ, Rouzer CA, Saleh S, Marnett LJ, (2005) Simultaneous analysis of prostaglandin glyceryl esters and prostaglandins by electrospray tandem mass spectrometry. Anal Biochem 343: 203-211.
39. Watts JL, Browse J, (2000) A palmitoyl-CoA-specific delta9 fatty acid desaturase from Caenorhabditis elegans. Biochem Biophys Res Commun 272: 263-269.
40. Waugh RJ, Morrow JD, Roberts LJ 2nd, Murphy RC, (1997) Identification and relative quantitation of F2-isoprostane regioisomers formed in vivo in the rat. Free Radic Biol Med 23: 943-954.
41. Benenati G, Penkov S, Muller-Reichert T, Entchev EV, Kurzchalia TV, (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. Olson SK, Greenan G, Desai A, Muller-Reichert T, Oegema K, (2012) Hierarchical assembly of the eggshell and permeability barrier in C. elegans. J Cell Biol 198: 731-748.
43. Hsu MH, Savas U, Griffin KJ, Johnson EF, (2007) Human cytochrome p450 family 4 enzymes: function, genetic variation and regulation. Drug Metab Rev 39: 515-538.
44. Yin H, Gao L, Tai HH, Murphey LJ, Porter NA, 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. Whitten SJ, Miller MA, (2007) The role of gap junctions in Caenorhabditis elegans oocyte maturation and fertilization. Dev Biol 301: 432-446.
46. Yin H, Gao L, Tai HH, Murphey LJ, Porter NA, 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. Li A, Jiao X, Munier FL, Schorderet DF, Yao W, et al. (2004) Bietti crystalline corneoretinal dystrophy is caused by mutations in the novel gene CYP4V2. Am J Hum Genet 74: 817-826.
48. Nakano M, Kelly EJ, Wiek C, Hanenberg H, Rettie AE, (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. Kulas J, Schmidt C, Rothe M, Schunck WH, Menzel R, (2008) Cytochrome P450-dependent metabolism of eicosapentaenoic acid in the nematode Caenorhabditis elegans. Arch Biochem Biophys 472: 65-75.
50. Lishko PV, Kirichok Y, Ren D, Navarro B, Chung JJ, et al. (2012) The control of male fertility by spermatozoan ion channels. Annu Rev Physiol 74: 453-475.
51. Ren D, Navarro B, Perez G, Jackson AC, Hsu S, et al. (2001) A sperm ion channel required for sperm motility and male fertility. Nature 413: 603-609.
52. Quill TA, Ren D, Clapham DE, Garbers DL, (2001) A voltage-gated ion channel expressed specifically in spermatozoa. Proc Natl Acad Sci U S A 98: 12527-12531.
53. Aitken RJ, Kelly RW, (1985) Analysis of the direct effects of prostaglandins on human sperm function. J Reprod Fertil 73: 139-146.
54. Gottlieb C, Svanborg K, Eneroth P, Bygdeman M, (1988) Effect of prostaglandins on human sperm function in vitro and seminal adenosine triphosphate content. Fertil Steril 49: 322-327.
55. Timmons L, Fire A, (1998) Specific interference by ingested dsRNA. Nature 395: 854.
56. Kamath RS, Ahringer J, (2003) Genome-wide RNAi screening in Caenorhabditis elegans. Methods 30: 313-321.
57. Porta-de-la-Riva M, Fontrodona L, Villanueva A, Ceron J, (2012) Basic Caenorhabditis elegans methods: synchronization and observation. J Vis Exp pp. e4019.
58. McCarter J, Bartlett B, Dang T, Schedl T, (1999) On the control of oocyte meiotic maturation and ovulation in Caenorhabditis elegans. Dev Biol 205: 111-128.
59. Golovko MY, Murphy EJ, (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.