Sex-biased protein expression in threespine stickleback, Gasterosteus aculeatus

Journal of Proteome Research

Volumn 10, Issue 9, 2011, Pages 4033-4040

  Viitaniemi, Heidi Marja ^a   Leder, Erica Helen ^a  

^a UNIVERSITY OF TURKU   (Finland)

Author keywords

gasterosteus; label free; liver; proteomics; sexual dimorphism; stickleback

Indexed keywords

AMINO ACID METABOLISM; ANIMAL TISSUE; ARTICLE; ENERGY METABOLISM; FEMALE; FISH; GASTEROSTEUS ACULEATUS; LIPID METABOLISM; LIVER FUNCTION; MALE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; SEX CHROMOSOME; SEX DIFFERENCE; SEXUAL BEHAVIOR;

ANIMALS; CHROMATOGRAPHY, LIQUID; CLUSTER ANALYSIS; FEMALE; FISH PROTEINS; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORKS; LIVER; MALE; PROTEOME; PROTEOMICS; SEX FACTORS; SMEGMAMORPHA; TANDEM MASS SPECTROMETRY;

GASTEROSTEUS; GASTEROSTEUS ACULEATUS;

EID: 80052502624     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr200234a     Document Type: Article

References (66)

1. Kodric-Brown, A. Sexual dichromatism and temporary color changes in the reproduction of fishes Am. Zool. 1998, 38 (1) 70-81 (Pubitemid 128058924)
2. Rubenik, G. A. Seosonal regulation of deer reproduction as related to the antler cycle-a review Vet. Arhiv. 2006, S275-S285
3. Kitano, J.; Mori, S.; Peichel, C. L. Sexual dimorphism in the external morphology of the threespine stickleback (Gasterosteus aculeatus) Copeia 2007, 2, 336-349 (Pubitemid 47164604)
4. Fleming, I. A.; Gross, M. R. Breeding competition in a pacific salmon (coho, Oncorhyncyus kisutch) - measures of natural and sexual selection Evolution 1994, 48 (3) 637-657
5. Fleming, I. A.; Reynolds, J. D. Salmonid breeding systems. Evolution Illuminated, Salmon and Their Relatives; Oxford University Press: New York, 2003.
6. Bhattacharya, S. Endocrine control of fish reproduction Curr. Sci. India 1992, 63 (3) 135-139
7. Mode, A.; Gustafsson, J. A. Sex and the liver-A journey through five decades Drug Metab. Rev. 2006, 38 (1-2) 197-207 (Pubitemid 43739007)
8. Waxman, D. J.; Holloway, M. G. Sex differences in the expression of hepatic drug metabolizing enzymes Mol. Pharmacol. 2009, 76 (2) 215-228
9. Toppo, S.; Vanin, S.; Bosello, V.; Tosatto, S. C. Evolutionary and structural insights into the multifaceted glutathione peroxidase (Gpx) superfamily Antioxid. Redox Signal. 2008, 10 (9) 1501-1514
10. Yamazaki, H.; Shimada, T. Progesterone and testosterone hydroxylation by cytochromes P450 2C19, 2C9, and 3A4 in human liver microsomes Arch. Biochem. Biophys. 1997, 346, 161-169 (Pubitemid 27415307)
11. Gustaffsson, J. A.; Mode, A.; Norstedt, G.; Skett, P. Sex steroid induced changes in hepatic enzymes Annu. Rev. Physiol. 1983, 45, 51-60
12. Roy, A. K.; Chatterjee, B. Sexual dimorphism in liver Annu. Rev. Physiol. 1983, 45, 37-50
13. Ahluwalia, A.; Clodfelter, K. H.; Waxman, D. J. Sexual dimorphism of rat liver gene expression: regulatory role of growth hormone revealed by deoxyribonucleid acid microarray analysis Mol. Endocrinol. 2004, 18 (3) 747-760 (Pubitemid 38328217)
14. Yang, X.; Schadt, E. E.; Wang, S.; Wang, H.; Arnold, A. P.; Ingram-Drake, L.; Drake, T. A.; Lusis, A. J. Tissue-specific expression and regulation of sexually dimorphic genes in mice Genome Res. 2006, 16 (8) 995-1004 (Pubitemid 44162259)
15. Goetz, F. W.; Rise, M. L.; Rise, M.; Goetz, G. W.; Binkowski, F.; Shepherd, B. S. Stimulation of growth and changes in the hepatic transcriptome by 17β-estradiol in the yellow perch (Perca flavescens) Physiol. Genomics 2009, 38, 261-280
16. Leder, E. H.; Cano, J. M.; Leinonen, T.; O'Hara, R. B.; Nikinmaa, M.; Primmer, C. R.; Merila, J. Female-Biased Expression on the X Chromosome as a Key Step in Sex Chromosome Evolution in Threespine Sticklebacks Mol. Biol. Evol. 2010, 27 (7) 1495-1503
17. Prohaska, J. R.; Sunde, R. A. Comparison of liver glutathione peroxidase activity and mRNA in female and male mice and rats Comp. Biochem. Physiol. B 1993, 105 (1) 111-116 (Pubitemid 23136871)
18. Liang, Q.; Sheng, Y.; Jiang, P.; Ji, L.; Xia, Y.; Min, Y.; Wang, Z. The gender-dependent difference of liver GSH antioxidant system in mice and its influence on isoline-induced liver injury Toxicology 2010, 280, 61-69
19. Ramirez, M. C.; Luque, G. M.; Ornstein, A. M.; Becu-Villalobos, D. Differential neonatal testosterone imprinting of GH-dependent liver proteins and genes in female mice J. Endocrinol. 2010, 207, 301-308
20. Barnett, A.; Bellwood, D. R. Sexual dimorphism in the buccal cavity of paternal mouthbrooding cardinalfishes (Pisces: Apogonidae) Mar. Biol. 2005, 148 (1) 205-212 (Pubitemid 41605647)
21. Eibner, C.; Pittlik, S.; Meyer, A.; Begemann, G. An organizer controls the development of the "sword," a sexually selected trait in swordtail fish Evol. Dev. 2008, 10 (4) 403-412 (Pubitemid 351991475)
22. Devlin, R. H.; Nagahama, Y. Sex determination and sex specific differentiation in fish Aquaculture 2002, 208, 191-364
23. Tinbergen, N. The study of instinct; Oxford University Press: New York, 1951.
24. Schluter, D. The ecology of adaptive radiation; Oxford University Press: New York, 2000.
25. Foster, S. A.; Shaw, K. A.; Robert, K. L.; Baker, J. A. Benthic, limnetic and oceanic threespine stickleback: profiles of reproductive behaviour Behaviour 2008, 145, 485-508 (Pubitemid 351445633)
26. Peichel, C. L.; Ross, J. A.; Matson, C. K.; Dickson, M.; Grimwood, J.; Schmutz, J.; Myers, R. M.; Mori, S.; Schluter, D.; Kingsley, D. M. The master sex-determination locus in threespine sticklebacks is on a nascent Y chromosome Curr. Biol. 2004, 14 (16) 1416-1424 (Pubitemid 39123739)
27. Leinonen, T.; Cano, J. M.; Merila, J. Genetic basis of sexual dimorphism in the threespine stickleback Gasterosteus aculeatus Heredity 2011, 106 (2) 218-227
28. Sanchez, W.; Ait-Aissa, S.; Palluel, O.; Ditche, J. M.; Porcher, J. M. Preliminary investigation of multi-biomarker responses in three-spined stickleback (Gasterosteus aculeatus L.) sampled in contaminated streams Ecotoxicology 2007, 16 (2) 279-287 (Pubitemid 46295254)
29. Sanchez, W.; Piccini, B.; Ditche, J. M.; Porcher, J. M. Assessment of seasonal variability of biomarkers in three-spined stickleback (Gasterosteus aculeatus L.) from a low contaminated stream: Implication for environmental biomonitoring Environ. Intl. 2008, 34 (6) 791-798
30. Michiel, G. P. An examination of two reported protein polymorphisms in threespine sticklaback, Gasterosteus aculeatus; Masters thesis, University of British Colombia, 1974.
31. Gstaiger, M.; Aebersold, R. Applying mass spectrometry-based proteomics to genetics, genomics and network biology Nat. Rev. Genet. 2009, 10, 617-627
32. Paoletti, A. C.; Parmely, T. J.; Tomomori-Sato, C.; Sato, S.; Zhu, D.; Conaway, R. C.; Conaway, J. W.; Florens, L.; Washburn, M. P. Quantitative proteomic analysis of distinct mammalian Mediator complexes using normalized spectral abundance factors Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 18928-18933 (Pubitemid 350002805)
33. Keller, A.; Nesvizhskii, A. I.; Kolker, E.; Aebersold, R. Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search Anal. Chem. 2002, 74 (20) 5383-5392 (Pubitemid 35215372)
34. Nesvizhskii, A. I.; Keller, A.; Kolker, E.; Aebersold, R. A statistical model for identifying proteins by tandem mass spectrometry Anal. Chem. 2003, 75 (17) 4646-4658 (Pubitemid 37082259)
35. Craig, R.; Beavis, R. C. TANDEM: matching proteins with tandem mass spectra Bioinformatics 2004, 20, 1466-1467 (Pubitemid 38931421)
36. Zybailov, B.; Mosley, A. L.; Sardiu, M. E.; Coleman, M. K.; Florens, L.; Washburn, M. P. Statistical analysis of membrane proteome expression changes in Saccharomyces cerevisiae J. Proteome Res. 2006, 5 (9) 2339-2347 (Pubitemid 44330827)
37. Mosley, A. L.; Florens, L.; Wen, Z.; Washburn, M. P. A label free quantitative proteomic analysis of the Saccharomyces cerevisiae nucleus J. Proteomics 2009, 72, 110-120
38. Asara, J. M.; Christofk, H. R.; Freimark, L. M.; Cantley, L. C. A label-free quantification method by MS/MS TIC compared to SILAC and spectral counting in a proteomics screen Proteomics 2008, 8 (5) 994-999 (Pubitemid 351441438)
39. Elo, L. L.; Hiissa, J.; Tuimala, J.; Kallio, A.; Korpelainen, E.; Aittokallio, T. Optimized detection of differential expression in global profiling experiments: case studies in clinical transcriptomic and quantitative proteomic datasets Brief Bioinform. 2009, 10, 547-555
40. Smyth, G. K. Linear models and empirical bayes methods for assessing differential expression in microarray experiments Stat. Appl. Genet. Mol. Biol. 2004, 3 (1 Article 3
41. Shannon, P.; Markiel, A.; Ozier, O.; Baliga, N. S.; Wang, J. T.; Ramage, D.; Amin, N.; Schwikowski, B.; Ideker, T. Cytoscape: A software environment for integrated models of interaction networks Genome Res. 2003, 13, 2498-2504 (Pubitemid 37428274)
42. Bindea, G.; Mlecnik, B.; Hackl, H.; Charoentong, P.; Tosolini, M.; Kirilovsky, A.; Fridman, W. H.; Pages, F.; Trajanoski, Z.; Galon, J. ClueGO: A Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks Bioinformatics 2009, 25, 1091-1093
43. Gebhardt, R. Metabolic zonation of the liver: regulation and implications for liver function Pharmacol. Ther. 1992, 53, 275-354
44. McFarland, V. A.; Inouye, L. S.; Lutz, C. H.; Jarvis, A. S.; Clarke, J. U.; McCant, D. D. Biomarkers of oxidative stress and genotoxicity in livers of field-collected brown bullhead, Ameiurus nebulosus Arch. Environ. Contam. Toxicol. 1999, 37, 236-241 (Pubitemid 29357895)
45. Bize, P.; Devevey, G.; Monaghan, P.; Doligez, B.; Christe, P. Fecundity and survival in relation to resistance to oxidative stress in a free-living bird Ecology 2008, 89 (9) 2584-2593
46. Wang, Y.; Salmon, A. B.; Harsham, L. G. A cost of reproduction: oxidative stress susceptibility is associated with increased egg production in Drosophila melanogaster Exp. Gerontol. 2001, 36, 1349-1359 (Pubitemid 32707872)
47. O'Donohue, M. F.; Choesmel, V.; Faubladier, M.; Fichant, G.; Gleizes, P. E. Functional dichotomy of ribosomal proteins during the synthesis of mammalian 40S ribosomal subunits J. Cell Biol. 2010, 190, 853-866
48. Lian, Z.; Liu, J.; Li, L.; Li, X.; Tufan, N. L.; Wu, M. C.; Wang, H. Y.; Arbuthnot, P.; Kew, M.; Feitelson, M. A. Human S15a expression is upregulated by hepatitis B virus X protein Mol. Carcinog. 2004, 40 (1) 34-46 (Pubitemid 38581661)
49. Chai, G.; Brewer, J. M.; Lovelace, L. L.; Aoki, T.; Minor, W.; Lebioda, L. Expression, purification and the 1.8 angstroms resolution crystal structure of human neuron specific enolase J. Mol. Biol. 2004, 341, 1015-1021 (Pubitemid 39037361)
50. Glatt, H. Sulfotransferases in the bioactivation of xenobiotics Chem. Biol. Interact. 2000, 129, 141-170 (Pubitemid 32061058)
51. Alnouti, Y.; Klaassen, C. D. Mechanisms of gender-specific regulation of mouse sulfotransferases (Sults) Xenobiotica 2011, 41 (3) 187-197
52. Nagata, K.; Ozawa, S.; Miyata, M.; Shimada, M.; Gong, D. W.; Yamazoe, Y.; Kato, R. Isolation and expression of a cDNA encoding a male-specific rat sulfotransferase that catalyzes activation of N-hydroxy-2-acetylaminofluorene J. Biol. Chem. 1993, 268 (33) 24720-24725 (Pubitemid 23335482)
53. DeBaun, J. R.; Smith, J. Y.; Miller, E. C.; Miller, J. A. Reactivity in vivo of the carcinogen N-hydroxy-2-acetylaminofluorene: increase by sulfate ion Science 1970, 167 (915) 184-186
54. Day, I. N.; Thompson, R. J. UCHL1 (PGP 9.5): neuronal biomarker and ubiquitin system protein Prog. Neurobiol. 2009, 90, 327-362
55. Esteban, F. J.; Jimenez, A.; Barroso, J. B.; Pedrosa, J. A.; del Moral, M. L.; Rodrigo, J.; Peinado, M. A. The innervation of rainbow trout (Oncorhynchus mykiss) liver: protein gene product 9.5 and neuronal nitric oxide synthase immunoreactivities J. Anat. 1998, 193 (2) 241-249 (Pubitemid 28479048)
56. Wilson, C. M.; Roebuck, Q.; High, S. Ribophorin I regulates substrate delivery to the oligosaccharyltransferase core Proc. Natl. Acad. Sci. U.S.A. 2008, 105, 9534-9539 (Pubitemid 352031336)
57. Lu, Y.; O'Dowd, B. F.; Orrego, H.; Israel, Y. Cloning and nucleotide sequence of human liver cDNA encoding for cystathionine gamma-lyase Biochem. Biophys. Res. Commun. 1992, 189, 749-758 (Pubitemid 23032436)
58. Okuno, T.; Ueno, H.; Nakamuro, K. Cystathionine gamma-lyase contributes to selenomethionine detoxification and cytosolic glutathione peroxidase biosynthesis in mouse liver Biol. Trace. Elem. Res. 2006, 109, 155-171 (Pubitemid 43162266)
59. Wibe, A. E.; Rosenqvist, G.; Jenssen, B. M. Disruption of male reproductive behavior in threespine stickleback Gasterosteus aculeatus exposed to 17β-estradiol Environ. Res. 2002, 90 (2) 136-141 (Pubitemid 35191495)
60. Mazzoni, C.; Torella, M.; Petrera, A.; Palermo, V.; Falcone, C. PGK1, the gene encoding the glycolitic enzyme phosphoglycerate kinase, acts as a multicopy suppressor of apoptotic phenotypes in S. cerevisiae Yeast 2009, 26, 31-37
61. Lindblad, B.; Lindstedt, S.; Steen, G. On the enzymic defects in hereditary tyrosinemia Proc. Natl. Acad. Sci. U.S.A. 1977, 74 (10) 4641-4645 (Pubitemid 8225182)
62. Williams, T. D.; Diab, A. M.; George, S. G.; Sabine, V.; Chipman, J. K. Gene expression responses of European flounder (Platichthys flesus) to 17-β estradiol Toxicol. Lett. 2007, 168, 236-248 (Pubitemid 46097342)
63. Katsiadakia, I.; Williams, T. D.; Ball, J. C.; Beana, T. P.; Sanders, M. B.; Wub, H.; Santos, E. M.; Margaret, M.; Brown, M. M.; Baker, P.; Ortega, F.; Falciani, F.; Craft, J. A.; Tyler, C. R.; Viant, M. R.; Chipman, J. K. Hepatic transcriptomic and metabolomic responses in the Stickleback (Gasterosteus aculeatus) exposed to ethinyl-estradiol Aquat. Toxicol. 2010, 97, 174-187
64. Cox, J.; Mann, M. Is proteomics the new genomics? Cell 2007, 130, 395-398 (Pubitemid 47198310)
65. Cox, B.; Kislinger, T.; Emili, A. Integrating gene and protein expression data: pattern analysis and profile mining Methods 2005, 35, 303-314 (Pubitemid 40255595)
66. Tyers, M.; Mann, M. From genomics to proteomics Nature 2003, 422, 193-197 (Pubitemid 36362756)