#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

TRY-5 Is a Sperm-Activating Protease in Seminal Fluid


Seminal fluid proteins have been shown to play important roles in male reproductive success, but the mechanisms for this regulation remain largely unknown. In Caenorhabditis elegans, sperm differentiate from immature spermatids into mature, motile spermatozoa during a process termed sperm activation. For C. elegans males, sperm activation occurs during insemination of the hermaphrodite and is thought to be mediated by seminal fluid, but the molecular nature of this activity has not been previously identified. Here we show that TRY-5 is a seminal fluid protease that is required in C. elegans for male-mediated sperm activation. We observed that TRY-5::GFP is expressed in the male somatic gonad and is transferred along with sperm to hermaphrodites during mating. In the absence of TRY-5, male seminal fluid loses its potency to transactivate hermaphrodite sperm. However, TRY-5 is not required for either hermaphrodite or male fertility, suggesting that hermaphrodite sperm are normally activated by a distinct hermaphrodite-specific activator to which male sperm are also competent to respond. Within males, TRY-5::GFP localization within the seminal vesicle is antagonized by the protease inhibitor SWM-1. Together, these data suggest that TRY-5 functions as an extracellular activator of C. elegans sperm. The presence of TRY-5 within the seminal fluid couples the timing of sperm activation to that of transfer of sperm into the hermaphrodite uterus, where motility must be rapidly acquired. Our results provide insight into how C. elegans has adopted sex-specific regulation of sperm motility to accommodate its male-hermaphrodite mode of reproduction.


Vyšlo v časopise: TRY-5 Is a Sperm-Activating Protease in Seminal Fluid. PLoS Genet 7(11): e32767. doi:10.1371/journal.pgen.1002375
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1002375

Souhrn

Seminal fluid proteins have been shown to play important roles in male reproductive success, but the mechanisms for this regulation remain largely unknown. In Caenorhabditis elegans, sperm differentiate from immature spermatids into mature, motile spermatozoa during a process termed sperm activation. For C. elegans males, sperm activation occurs during insemination of the hermaphrodite and is thought to be mediated by seminal fluid, but the molecular nature of this activity has not been previously identified. Here we show that TRY-5 is a seminal fluid protease that is required in C. elegans for male-mediated sperm activation. We observed that TRY-5::GFP is expressed in the male somatic gonad and is transferred along with sperm to hermaphrodites during mating. In the absence of TRY-5, male seminal fluid loses its potency to transactivate hermaphrodite sperm. However, TRY-5 is not required for either hermaphrodite or male fertility, suggesting that hermaphrodite sperm are normally activated by a distinct hermaphrodite-specific activator to which male sperm are also competent to respond. Within males, TRY-5::GFP localization within the seminal vesicle is antagonized by the protease inhibitor SWM-1. Together, these data suggest that TRY-5 functions as an extracellular activator of C. elegans sperm. The presence of TRY-5 within the seminal fluid couples the timing of sperm activation to that of transfer of sperm into the hermaphrodite uterus, where motility must be rapidly acquired. Our results provide insight into how C. elegans has adopted sex-specific regulation of sperm motility to accommodate its male-hermaphrodite mode of reproduction.


Zdroje

1. PitnickSWolfnerMFSuarezS 2009 Ejaculate-female and sperm-female interactions. BirkheadTRHoskenDJPitnickS Sperm Biology: An Evolutionary Perspective Amsterdam; London Elsevier/Academic Press 247 304

2. PoianiA 2006 Complexity of seminal fluid: a review. Behav Ecol Sociobiol 60 289 310

3. YoshidaMKawanoNYoshidaK 2008 Control of sperm motility and fertility: diverse factors and common mechanisms. Cell Mol Life Sci 65 3446 3457

4. AvilaFWSirotLKLaFlammeBARubinsteinCDWolfnerMF 2011 Insect seminal fluid proteins: identification and function. Annu Rev Entomol 56 21 40

5. WolfnerMF 2009 Battle and Ballet: Molecular Interactions between the Sexes in Drosophila. J Hered 100 399 410

6. WardSCarrelJS 1979 Fertilization and sperm competition in the nematode Caenorhabditis elegans. Dev Biol 73 304 321

7. WardS 1977 The use of nematode behavioral mutants for analysis of neural function and development. CowanWMFerrendelliJA Neurosciences Research Symposium II: Approaches to the cell biology of neurons Bethesda, MD Society for Neurosciences 1 61

8. JustineJ-L 2002 Male and female gametes and fertilisation. LeeDL The biology of nematodes London Taylor & Francis 162 244

9. SmithHE 2006 Sperm motility and MSP. In: WormBook, ed. The C. elegans Research Community, WormBook, doi/10.1895/wormbook.1.68.1, http://www.wormbook.org

10. NelsonGAWardS 1980 Vesicle fusion, pseudopod extension and amoeboid motility are induced in nematode spermatids by the ionophore monensin. Cell 19 457 464

11. WardSHoganENelsonGA 1983 The initiation of spermiogenesis in the nematode Caenorhabditis elegans. Dev Biol 98 70 79

12. ShakesDCWardS 1989 Initiation of spermiogenesis in C. elegans: a pharmacological and genetic analysis. Dev Biol 134 189 200

13. MachacaKDeFeliceLJL'HernaultSW 1996 A novel chloride channel localizes to Caenorhabditis elegans spermatids and chloride channel blockers induce spermatid differentiation. Dev Biol 176 1 16

14. L'HernaultSWShakesDCWardS 1988 Developmental genetics of chromosome I spermatogenesis-defective mutants in the nematode Caenorhabditis elegans. Genetics 120 435 452

15. MinnitiANSadlerCWardS 1996 Genetic and molecular analysis of spe-27, a gene required for spermiogenesis in Caenorhabditis elegans hermaphrodites. Genetics 143 213 223

16. NanceJMinnitiANSadlerCWardS 1999 spe-12 encodes a sperm cell surface protein that promotes spermiogenesis in Caenorhabditis elegans. Genetics 152 209 220

17. NanceJDavisEBWardS 2000 spe-29 encodes a small predicted membrane protein required for the initiation of sperm activation in Caenorhabditis elegans. Genetics 156 1623 1633

18. MuhlradPJWardS 2002 Spermiogenesis initiation in Caenorhabditis elegans involves a casein kinase 1 encoded by the spe-6 gene. Genetics 161 143 155

19. GeldzilerBChatterjeeISingsonA 2005 The genetic and molecular analysis of spe-19, a gene required for sperm activation in Caenorhabditis elegans. Dev Biol 283 424 436

20. StanfieldGMVilleneuveAM 2006 Regulation of sperm activation by SWM-1 is required for reproductive success of C. elegans males. Curr Biol 16 252 263

21. Marchler-BauerAAndersonJBChitsazFDerbyshireMKDeWeese-ScottC 2009 CDD: specific functional annotation with the Conserved Domain Database. Nucleic Acids Res 37 D205 210

22. Di CeraE 2009 Serine proteases. IUBMB Life 61 510 515

23. PeronaJJCraikCS 1995 Structural basis of substrate specificity in the serine proteases. Protein Sci 4 337 360

24. VarkeyJPJansmaPLMinnitiANWardS 1993 The Caenorhabditis elegans spe-6 gene is required for major sperm protein assembly and shows second site non-complementation with an unlinked deficiency. Genetics 133 79 86

25. WardSMiwaJ 1978 Characterization of temperature-sensitive, fertilization-defective mutants of the nematode Caenorhabditis elegans. Genetics 88 285 303

26. L'HernaultSW 2006 Spermatogenesis. In: WormBook, ed. The C. elegans Research Community, WormBook, doi/10.1895/wormbook.1.85.1, http://www.wormbook.org

27. ChenFHershBMConradtBZhouZRiemerD 2000 Translocation of C. elegans CED-4 to nuclear membranes during programmed cell death. Science 287 1485 1489

28. Frokjaer-JensenCDavisMWHopkinsCENewmanBJThummelJM 2008 Single-copy insertion of transgenes in Caenorhabditis elegans. Nat Genet 40 1375 1383

29. LintsRHallDH 2009 Male reproductive system, somatic gonad. WormAtlas doi:10.3908/wormatlas.2.15. Accessed 1 May 2011

30. KimbleJHirshD 1979 The postembryonic cell lineages of the hermaphrodite and male gonads in Caenorhabditis elegans. Dev Biol 70 396 417

31. BarrMMGarciaLR 2006 Male mating behavior. In: WormBook, ed. The C. elegans Research Community, WormBook, doi/10.1895/wormbook.1.78.1, http://www.wormbook.org

32. SchindelmanGWhittakerAJThumJYGharibSSternbergPW 2006 Initiation of male sperm-transfer behavior in Caenorhabditis elegans requires input from the ventral nerve cord. BMC Biol 4 26

33. BaldiCChoSEllisRE 2009 Mutations in two independent pathways are sufficient to create hermaphroditic nematodes. Science 326 1002 1005

34. FoorWEMcMahonJT 1973 Role of the glandular vas deferens in the development of Ascaris spermatozoa. J Parasitol 59 753 758

35. BurghardtRCFoorWE 1978 Membrane fusion during spermiogenesis in Ascaris. J Ultrastruct Res 62 190 202

36. PampalakisGSotiropoulouG 2007 Tissue kallikrein proteolytic cascade pathways in normal physiology and cancer. Biochim Biophys Acta 1776 22 31

37. OvaerePLippensSVandenabeelePDeclercqW 2009 The emerging roles of serine protease cascades in the epidermis. Trends Biochem Sci 34 453 463

38. GillottC 2003 Male accessory gland secretions: Modulators of female reproductive physiology and behavior. Annu Rev Entomol 48 163 184

39. WolfnerMF 2007 “S.P.E.R.M.” (seminal proteins (are) essential reproductive modulators): the view from Drosophila. Soc Reprod Fertil Suppl 65 183 199

40. HodgkinJDoniachT 1997 Natural variation and copulatory plug formation in Caenorhabditis elegans. Genetics 146 149 164

41. PalopoliMFRockmanMVTinMaungARamsayCCurwenS 2008 Molecular basis of the copulatory plug polymorphism in Caenorhabditis elegans. Nature 454 1019 1022

42. GattiJLCastellaSDacheuxFEcroydHMetayerS 2004 Post-testicular sperm environment and fertility. Anim Reprod Sci 82-83 321 339

43. CornwallGAvan HorstenHH 2007 Sperm maturation in the epididymis: Role of segment-specific microenvironments. CarrellDT The genetics of male infertility Totowa, N.J. Humana Press 211 231

44. KiontkeKGavinNPRaynesYRoehrigCPianoF 2004 Caenorhabditis phylogeny predicts convergence of hermaphroditism and extensive intron loss. Proc Natl Acad Sci U S A 101 9003 9008

45. ChoSJinSWCohenAEllisRE 2004 A phylogeny of Caenorhabditis reveals frequent loss of introns during nematode evolution. Genome Res 14 1207 1220

46. LaMunyonCWWardS 1995 Sperm precedence in a hermaphroditic nematode (Caenorhabditis elegans) is due to competitive superiority of male sperm. Experientia 51 817 823

47. BrennerS 1974 The genetics of Caenorhabditis elegans. Genetics 77 71 94

48. HodgkinJHorvitzHRBrennerS 1979 Nondisjunction mutants of the nematode Caenorhabditis elegans. Genetics 91 67 94

49. Wood and the Community of C. elegans Researchers 1988 The nematode Caenorhabditis elegans Cold Spring Harbor, N.Y. Cold Spring Harbor Laboratory

50. MaduroMPilgrimD 1995 Identification and cloning of unc-119, a gene expressed in the Caenorhabditis elegans nervous system. Genetics 141 977 988

51. AhringerJ 2006 Reverse genetics. In: WormBook, ed. The C. elegans Research Community, WormBook, doi/10.1895/wormbook.1.47.1, http://www.wormbook.org

52. FraserAGKamathRSZipperlenPMartinez-CamposMSohrmannM 2000 Functional genomic analysis of C. elegans chromosome I by systematic RNA interference. Nature 408 325 330

53. KamathRSFraserAGDongYPoulinGDurbinR 2003 Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421 231 237

54. RasbandWS 1997–2009 ImageJ Bethesda, Maryland, US U.S. National Institutes of Health

55. SambrookJFritschEFManiatisT 1989 Molecular Cloning: A Laboratory Manual Cold Spring Harbor, New York Cold Spring Harbor Laboratory Press

56. MerrittCRasolosonDKoDSeydouxG 2008 3′ UTRs are the primary regulators of gene expression in the C. elegans germline. Curr Biol 18 1476 1482

57. HobertO 2002 PCR fusion-based approach to create reporter gene constructs for expression analysis in transgenic C. elegans. Biotechniques 32 728 730

58. MelloCCKramerJMStinchcombDAmbrosV 1991 Efficient gene transfer in C.elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J 10 3959 3970

59. WormBase http://www.wormbase.org, release WS224. Accessed 6 June 2011

60. BendtsenJDNielsenHvon HeijneGBrunakS 2004 Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340 783 795

Štítky
Genetika Reprodukčná medicína

Článok vyšiel v časopise

PLOS Genetics


2011 Číslo 11
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#