Proteomic analysis of chinook salmon (Oncorhynchus tshawytscha) ovarian fluid

PLoS ONE

Volumn 9, Issue 8, 2014, Pages

  Johnson, Sheri L ^a   Villarroel, Marsha ^a   Rosengrave, Patrice ^a   Carne, Alan ^a   Kleffmann, Torsten ^a   Mark Lokman, P ^a   Gemmell, Neil J ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ARTICLE; BODY FLUID; CHEMICAL COMPOSITION; EGG PRODUCTION; FEMALE; FERTILIZATION; GASTRULATION; GENE ONTOLOGY; HYPOXIA; JUVENILE ANIMAL; LIQUID CHROMATOGRAPHY; NONHUMAN; ONCORHYNCHUS TSHAWYTSCHA; OVARIAN FLUID; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN ANALYSIS; PROTEOMICS; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY; ANIMAL; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; OVARY FOLLICLE; PHYSIOLOGY; PROTEIN SYNTHESIS; REPRODUCTION; SALMONINE;

ANIMALS; BODY FLUIDS; FEMALE; GENE EXPRESSION REGULATION; OVARIAN FOLLICLE; PROTEIN BIOSYNTHESIS; PROTEOMICS; REPRODUCTION; SALMON; TANDEM MASS SPECTROMETRY;

EID: 84905460293     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0104155     Document Type: Article

References (76)

1. Rosengrave P, Gemmell NJ, Metcalf V, McBride K, Montgomerie R (2008) A mechanism for cryptic female choice in chinook salmon. Behav Ecol 19: 1179-1185.
2. Rosengrave P, Taylor H, Montgomerie R, Metcalf V, McBride K, et al. (2009) Chemical composition of seminal and ovarian fluids of chinook salmon (Oncorhynchus tshawytscha) and their effects on sperm motility traits. Comp Biochem Physiol A 152: 123-129.
3. Yeates SE, Diamond SE, Einum S, Emerson BC, Holt WV, et al. (2013) Cryptic choice of conspecific sperm controlled by the impact of ovarian fluid on sperm swimming behaviour. Evolution 67: 3523-3536.
4. Yanagimachi R, Cherr G, Matsubara T, Andoh T, Harumi T, et al. (2013) Sperm attractant in the micropyle region of fish and insect eggs I. Biol Reprod 88.
5. Litvak MK, Trippel EA (1998) Sperm motility patterns of Atlantic cod (Gadus morhua) in relation to salinity: effects of ovarian fluid and egg presence. Can J Fish Aquat Sci 55: 1871-1877. (Pubitemid 28554013)
6. Lahnsteiner F, Weismann T, Patzner R (1995) Composition of the ovarian fluid in 4 salmonid species: Oncorhynchus mykiss, Salmo trutta f lacustris, Salvelinus alpinus and Hucho hucho. Reprod Nutr Dev 35: 465.
7. Lahnsteiner F (2002) The influence of ovarian fluid on the gamete physiology in the Salmonidae. Fish Physiol Biochem 27: 49-59.
8. Hoar WS (1957) The gonads and reproduction. The Physiology of Fishes. New York: Academic Press. pp. 287-321.
9. Hirano T, Morisawa M, Suzuki K (1978) Changes in plasma and coelomic fluid composition of the mature salmon Oncorhynchus keta during freshwater adaptation. Comp Biochem Physiol A 61: 5-8. (Pubitemid 9015608)
10. Rime H, Guitton N, Pineau C, Bonnet E, Bobe J, et al. (2004) Post-ovulatory ageing and egg quality: a proteomic analysis of rainbow trout coelomic fluid. Reprod Biol Endocrinol 2.
11. Rosengrave PRP, Montgomerie RMR, Metcalf VJMVJ, McBride KMBK, Gemmell NJ (2009) Sperm traits in chinook salmon depend upon activation medium: implications for studies of sperm competition in fishes. Can J Zool 87: 920-927.
12. Turner E, Montgomerie R (2002) Ovarian fluid enhances sperm movement in Arctic charr. J Fish Biol 60: 1570-1579.
13. Urbach D, Folstad I, Rudolfsen G (2005) Effects of ovarian fluid on sperm velocity in Arctic charr (Salvelinus alpinus). Behav Ecol Sociobiol 57: 438-444. (Pubitemid 40383633)
14. Wojtczak M, Dietrich GJ, Słowińska M, Dobosz S, Kuźmiński H, et al. (2007) Ovarian fluid pH enhances motility parameters of rainbow trout (Oncorhynchus mykiss) spermatozoa. Aquaculture 270: 259-264. (Pubitemid 47223333)
15. Hugunin HA, Parsons JE, Nagler JJ (2008) The influence of coelomic fluid on in vitro fertilization success in rainbow trout Oncorhynchus mykiss. Aquaculture 281: 155-157.
16. Hatef A, Niksirat H, Alavi SMH (2009) Composition of ovarian fluid in endangered Caspian brown trout, Salmo trutta caspius, and its effects on spermatozoa motility and fertilizing ability compared to freshwater and a saline medium. Fish Physiol Biochem 35: 695-700.
17. Bahabadi MN, Shoae A, Lokman PM (2011) Effects of storage time, sex steroids and media composition on egg viability of rainbow trout (Oncorhynchus mykiss). Aquaculture 315: 306-311.
18. Bachan M, Fleming I, Trippel E (2012) Maternal allocation of lipid classes and fatty acids with seasonal egg production in Atlantic cod (Gadus morhua) of wild origin. Mar Biol 159: 2281-2297.
19. Dietrich MA, Dabrowski K, Arslan M, Ware K, Van Tassell J (2012) Quantifying quality attributes of walleye eggs prior to fertilization - Impact of time of ovulation and gametes storage. J Gt Lakes Res 38: 445-450.
20. Woolsey J, Holcomb M, Cloud JG, Ingermann RL (2006) Sperm motility in the steelhead Oncorhynchus mykiss (Walbaum): influence of the composition of the incubation and activation media. Aquac Res 37: 215-223.
21. Butts IA, Johnson K, Wilson CC, Pitcher TE (2012) Ovarian fluid enhances sperm velocity based on relatedness in lake trout, Salvelinus namaycush. Theriogenology 78: 2105-2109. e2101.
22. Galvano PM, Johnson K, Wilson CC, Pitcher TE, Butts IA (2013) Ovarian fluid influences sperm performance in lake trout, Salvelinus namaycush. Reprod Biol 13: 172-175.
23. Dietrich GJ, Wojtczak M, Słowińska M, Dobosz S, Kuźmiński H, et al. (2008) Effects of ovarian fluid on motility characteristics of rainbow trout (Oncorhynchus mykiss Walbaum) spermatozoa. J Appl Ichthyol 24: 503-507.
24. Elofsson H, Borg B, Mayer I (2003) Influence of salinity and ovarian fluid on sperm motility in the fifteen-spined stickleback. J Fish Biol 63: 1429-1438. (Pubitemid 38718014)
25. Elofsson H, McAllister B, Kime D, Mayer I, Borg B (2003) Long lasting stickleback sperm; is ovarian fluid a key to success in fresh water? J Fish Biol 63: 240-253. (Pubitemid 38592295)
26. Diogo P, Soares F, Dinis M, Cabrita E (2010) The influence of ovarian fluid on Solea senegalensis sperm motility. J Appl Ichthyol 26: 690-695.
27. Kanuga M, Drew R, Wilson-Leedy J, Ingermann R (2012) Subpopulation distribution of motile sperm relative to activation medium in steelhead (Oncorhynchus mykiss). Theriogenology 77: 916-925.
28. Evans JP, Rosengrave P, Gasparini C, Gemmell NJ (2013) Delineating the roles of males and females in sperm competition. Proc Roy Soc Lond B Biol 280: 20132047.
29. Skjæraasen JE, Mayer I, Meager JJ, Rudolfsen G, Karlsen O, et al. (2009) Sperm characteristics and competitive ability in farmed and wild cod. Mar Ecol Prog Ser 375: 219-228.
30. Gasparini C, Simmons LW, Beveridge M, Evans JP (2010) Sperm swimming velocity predicts competitive fertilization success in the green swordtail Xiphophorus helleri. PLoS ONE 5: e12146.
31. Boschetto C, Gasparini C, Pilastro A (2011) Sperm number and velocity affect sperm competition success in the guppy (Poecilia reticulata). Behav Ecol Sociobiol 65: 813-821.
32. Gage MJG, Macfarlane CP, Yeates S, Ward RG, Searle JB, et al. (2004) Spermatozoal traits and sperm competition in Atlantic salmon: Relative sperm velocity is the primary determinant of fertilization success. Curr Biol 14: 44-47. (Pubitemid 38069975)
33. Birkhead TR, Martinez JG, Burke T, Froman DP (1999) Sperm mobility determines the outcome of sperm competition in the domestic fowl. Proc Roy Soc Lond B Biol 266: 1759-1764. (Pubitemid 29433457)
34. Dziminski MA, Roberts JD, Beveridge M, Simmons LW (2009) Sperm competitiveness in frogs: slow and steady wins the race. Proc Roy Soc Lond B Biol 276: 3955-3961.
35. Lüpold S, Manier Mollie K, Berben Kirstin S, Smith Kyle J, Daley Bryan D, et al. (2012) How multivariate ejaculate traits determine competitive fertilization success in Drosophila melanogaster. Curr Biol 22: 1667-1672.
36. Gasparini G, Pilastro A (2011) Cryptic female preference for genetically unrelated males is mediated by ovarian fluid in the guppy. Proc Roy Soc Lond B Biol 278: 2495-2501.
37. Nynca J, Arnold GJ, Fröhlich T, Ciereszko A (2014) Shotgun proteomics of rainbow trout ovarian fluid. Reprod Fertil Dev /dx.doi.org/10.1071/RD13224.
38. Candiano G, Bruschi M, Musante L, Santucci L, Ghiggeri GM, et al. (2004) Blue silver: a very sensitive colloidal Coomassie G-250 staining for proteome analysis. Electrophoresis 25: 1327-1333. (Pubitemid 38801651)
39. Shevchenko A, Henrik Tomas JH, sbreve, Olsen JV, Mann M (2007) In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc 1: 2856-2860.
40. Eberhard WG (1996) Female control: sexual selection by cryptic female choice. Princeton, New Jersey: Princeton University Press.
41. Vacquier VD, Swanson WJ (2011) Selection in the rapid evolution of gamete recognition proteins in marine invertebrates. Cold Spring Harb Perspect Biol 3: a002931.
42. Swanson WJ, Vacquier VD (2002) The rapid evolution of reproductive proteins. Nat Rev Genet 3: 137-144. (Pubitemid 34506597)
43. Evans JP, Sherman CD (2013) Sexual selection and the evolution of egg-sperm interactions in broadcast-spawning invertebrates. Biol Bull 224: 166-183.
44. Palmer MR, Swanson WJ (2012) Evolution of sperm-egg interaction. In: Singh RS, J. Xu and R. J. Kulathinal, editor. Rapidly Evolving Genes & Genetic Systems: Oxford: Oxford University Press.
45. Simmons LW, Roberts JD, Dziminski MA (2009) Egg jelly influences sperm motility in the externally fertilizing frog, Crinia georgiana. J Evol Biol 22: 225-229.
46. Olson JH, Xiang X, Ziegert T, Kittelson A, Rawls A, et al. (2001) Allurin, a 21-kDa sperm chemoattractant from Xenopus egg jelly, is related to mammalian sperm-binding proteins. Proc Natl Acad Sci 98: 11205-11210. (Pubitemid 32928707)
47. Eisenbach M, Giojalas LC (2006) Sperm guidance in mammals - an unpaved road to the egg. Nat Rev Mol Cell Biol 7: 276-285.
48. Eisenbach M (1999) Sperm chemotaxis. Rev Reprod 4: 56-66.
49. Cherr GN, Morisawa M, Vines CA, Yoshida K, Smith EH, et al. (2008) Two egg-derived molecules in sperm motility initiation and fertilization in the Pacific herring (Clupea pallasi). Int J Dev Biol 52: 743.
50. Oda S, Igarashi Y, Manaka K-i, Koibuchi N, Sakai-Sawada M, et al. (1998) Sperm-activating proteins obtained from the herring eggs are homologous to trypsin inhibitors and synthesized in follicle cells. Dev Biol 204: 55-63. (Pubitemid 28563864)
51. Oda S, Igarashi Y, Ohtake H, Sakai K, Shimizu N, et al. (1995) Sperm-activating proteins from unfertilized eggs of the Pacific herring, Clupea pallasii. Dev Growth Differ 37: 257-261.
52. Ohtake H (2003) Sperm-activating proteins obtained from the herring eggs. Fish Physiol Biochem 28: 199-202.
53. Løvoll M, Kilvik T, Boshra H, Bøgwald J, Sunyer JO, et al. (2006) Maternal transfer of complement components C3-1, C3-3, C3-4, C4, C5, C7, Bf, and Df to offspring in rainbow trout (Oncorhynchus mykiss). Immunogenetics 58: 168-179.
54. Anderson DJ, Abbott AF, Jack RM (1993) The role of complement component C3b and its receptors in sperm-oocyte interaction. Proc Natl Acad Sci 90: 10051-10055. (Pubitemid 23328249)
55. Nynca J, Arnold GJ, Fröhlich T, Otte K, Flenkenthaler F, et al. (2014) Proteomic identification of rainbow trout seminal plasma proteins. Proteomics 14: 133-140.
56. Keyvanshokooh S, Vaziri B (2008) Proteome analysis of Persian sturgeon (Acipenser persicus) ova. Anim Reprod Sci 109: 287-297.
57. Benes P, Vetvicka V, Fusek M (2008) Cathepsin D - Many functions of one aspartic protease. Crit Rev Oncol Hematol 68: 12-28.
58. Carnevali O, Mosconi G, Cardinali M, Meiri I, Polzonetti-Magni A (2001) Molecular components related to egg viability in the gilthead sea bream, Sparus aurata. Mol Reprod Dev 58: 330-335. (Pubitemid 32121452)
59. Carnevali O, Centonze F, Brooks S, Marota I, Sumpter JP (1999) Molecular cloning and expression of ovarian cathepsin D in seabream, Sparus aurata. Biol Reprod 61: 785-791. (Pubitemid 29402640)
60. Saewu A, Asuvapongpatana S, Chotwiwatthanakun C, Tantiwongse A, Weerachatyanukul W, et al. (2012) Cathepsin D in human reproductive tissues: cellular localization in testis and epididymis and surface distribution in different sperm conditions. J Androl 33: 726-734.
61. Srivastava PN, Ninjoor V (1982) Isolation of rabbit testicular cathepsin D and its role in the activation of proacrosin. Biochem Biophys Res Commun 109: 63-69. (Pubitemid 13072672)
62. Moura AA, Chapman DA, Koc H, Killian GJ (2006) Proteins of the cauda epididymal fluid associated with fertility of mature dairy bulls. J Androl 27: 534-541. (Pubitemid 44126265)
63. Sharma R, Agarwal A, Mohanty G, Jesudasan R, Gopalan B, et al. (2013) Functional proteomic analysis of seminal plasma proteins in men with various semen parameters. Reprod Biol Endocrinol 11: 38.
64. Takayama S, Isogai A (2005) Self-incompatibility in plants. Annu Rev Plant Biol 56: 467-489. (Pubitemid 40802418)
65. Glass NL, Kaneko I (2003) Fatal attraction: nonself recognition and heterokaryon incompatibility in filamentous fungi. Eukaryot Cell 2: 1-8. (Pubitemid 36770370)
66. Kenoth R, Kamlekar RK, Simanshu DK, Gao Y, Malinina L, et al. (2011) Conformational folding and stability of the HET-C2 glycolipid transfer protein fold: does a molten globule-like state regulate activity? Biochemistry 50: 5163-5171.
67. Dobzhansky TG, Dobzhansky T (1937) Genetics and the Origin of Species: Columbia University Press.
68. Birkhead TR, Hosken DJ, Pitnick SS (2008) Sperm biology: an evolutionary perspective: Academic Press.
69. Howard DJ (1999) Conspecific sperm and pollen precedence and speciation. Annu Rev Ecol Syst 30: 109-132.
70. Yost JM, Kay KM (2009) The evolution of postpollination reproductive isolation in Costus. Sex Plant Reprod 22: 247-255.
71. Palumbi SR (1999) All males are not created equal: Fertility differences depend on gamete recognition polymorphisms in sea urchins. Proc Natl Acad Sci 96: 12632-12637.
72. Palumbi SR (2009) Speciation and the evolution of gamete recognition genes: pattern and process. Heredity (Edinb) 102: 66-76.
73. Levitan DR, Ferrell DL (2006) Selection on gamete recognition proteins depends on sex, density, and genotype frequency. Science 312: 267-269.
74. Neff BD, Garner SR, Heath JW, Heath DD (2008) The MHC and non-random mating in a captive population of chinook salmon. Heredity (Edinb) 101: 175-185.
75. Yeates SE, Einum S, Fleming IA, Megens HJ, Stet RJ, et al. (2009) Atlantic salmon eggs favour sperm in competition that have similar major histocompatibility alleles. Proc Roy Soc Lond B Biol 276: 559-566.
76. Consuegra S, Garcia de Leaniz C (2008) MHC-mediated mate choice increases parasite resistance in salmon. Proc Roy Soc Lond B Biol 275: 1397-1403. (Pubitemid 351653009)