Plasma proteome profiling of freshwater and seawater life stages of rainbow trout (Oncorhynchus mykiss)
Autoři:
Bernat Morro aff001; Mary K. Doherty aff002; Pablo Balseiro aff003; Sigurd O. Handeland aff003; Simon MacKenzie aff001; Harald Sveier aff004; Amaya Albalat aff001
Působiště autorů:
Institute of Aquaculture, University of Stirling, Stirling, Scotland, United Kingdom
aff001; Institute of Health Research and Innovation, Centre for Health Science, University of the Highlands and Islands, Inverness, Scotland, United Kingdom
aff002; NORCE AS, Universitetet i Bergen, Bergen, Norway
aff003; Lerøy Seafood Group ASA, Universitetet i Bergen, Bergen, Norway
aff004
Vyšlo v časopise:
PLoS ONE 15(1)
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pone.0227003
Souhrn
The sea-run phenotype of rainbow trout (Oncorhynchus mykiss), like other anadromous salmonids, present a juvenile stage fully adapted to life in freshwater known as parr. Development in freshwater is followed by the smolt stage, where preadaptations needed for seawater life are developed making fish ready to migrate to the ocean, after which event they become post-smolts. While these three life stages have been studied using a variety of approaches, proteomics has never been used for such purpose. The present study characterised the blood plasma proteome of parr, smolt and post-smolt rainbow trout using a gel electrophoresis liquid chromatography tandem mass spectrometry approach alone or in combination with low-abundant protein enrichment technology (combinatorial peptide ligand library). In total, 1,822 proteins were quantified, 17.95% of them being detected only in plasma post enrichment. Across all life stages, the most abundant proteins were ankyrin-2, DNA primase large subunit, actin, serum albumin, apolipoproteins, hemoglobin subunits, hemopexin-like proteins and complement C3. When comparing the different life stages, 17 proteins involved in mechanisms to cope with hyperosmotic stress and retinal changes, as well as the downregulation of nonessential processes in smolts, were significantly different between parr and smolt samples. On the other hand, 11 proteins related to increased growth in post-smolts, and also related to coping with hyperosmotic stress and to retinal changes, were significantly different between smolt and post-smolt samples. Overall, this study presents a series of proteins with the potential to complement current seawater-readiness assessment tests in rainbow trout, which can be measured non-lethally in an easily accessible biofluid. Furthermore, this study represents a first in-depth characterisation of the rainbow trout blood plasma proteome, having considered three life stages of the fish and used both fractionation alone or in combination with enrichment methods to increase protein detection.
Klíčová slova:
Blood plasma – Biomarkers – Proteomes – Serum proteins – Plasma proteins – Sea water – Fresh water – Trout
Zdroje
1. Fleming IA, Reynolds JD. Salmonid breeding systems. Evolution Illuminated: Salmon and Their Relatives. 2004: 264–294.
2. Quinn TP, Seamons TR, Vollestad LA, Duffy E. Effects of growth and reproductive history on the egg size-fecundity trade-off in steelhead. Trans Am Fish Soc. 2011;140: 45–51.
3. Quinn TP, McGinnity P, Reed TE. The paradox of “premature migration” by adult anadromous salmonid fishes: Patterns and hypotheses. Can J Fish Aquatic Sci. 2016;73: 1015–1030.
4. Kendall NW, McMillan JR, Sloat MR, Buehrens TW, Quinn TP, Pess GR, et al. Anadromy and residency in steelhead and rainbow trout (Oncorhynchus mykiss): A review of the Processes and Patterns. Can J Fish Aquatic Sci. 2015;72: 319–342.
5. Prunet P, Boeuf G, Bolton JP, Young G. Smoltification and seawater adaptation in Atlantic salmon (Salmo salar): Plasma prolactin, growth hormone, and thyroid hormones. Gen Comp Endocrinol. 1989;74: 355–364. doi: 10.1016/s0016-6480(89)80031-0 2545514
6. Hoar WS. The physiology of smolting salmonids. Fish Physiology. 1988;11 B: 275–343.
7. Björnsson BT, Stefansson SO, McCormick SD. Environmental endocrinology of salmon smoltification. Gen Comp Endocrinol. 2011;170: 290–298. doi: 10.1016/j.ygcen.2010.07.003 20627104
8. Mancera JM, McCormick SD. Role of prolactin, growth hormone, insulin-like growth factor and cortisol in teleost osmoregulation. Fish Osmoregulation. 2007: 497–515.
9. McCormick SD. Endocrine control of osmoregulation in teleost fish. Am Zool. 2001;41: 781–794.
10. Winans GA, Nishioka RS. A multivariate description of change in body shape of coho salmon (Oncorhynchus kisutch) during smoltification. Aquaculture. 1987;66: 235–245.
11. Riley WD, Ibbotson AT, Maxwell DL, Davison PI, Beaumont WRC, Ives MJ. Development of schooling behaviour during the downstream migration of Atlantic salmon Salmo salar smolts in a chalk stream. J Fish Biol. 2014;85: 1042–1059. doi: 10.1111/jfb.12457 25052817
12. Fontaine M, Hatey J. Variations of the liver glycogen in the young (Salmo salar L.) during smoltification. C R Seances Soc Biol Fil. 1950;144: 953–955. 14792810
13. Kobayashi R, yuki R. Differences in Catalase Activity in the Tissues and Blood between the Smolt and Parr of Masu, Oncorhynchus masou. Bulletin of The Faculty of Fisheries Hokkaido University. 1954;5: 223–230.
14. Ebbesson LOE, Björnsson BT, Ekström P, Stefansson SO. Daily endocrine profiles in parr and smolt Atlantic salmon. Comp Biochem Physiol A Mol Integr Physiol. 2008;151: 698–704. doi: 10.1016/j.cbpa.2008.08.017 18790069
15. Handeland SO, Imsland AK, Björnsson BT, Stefansson SO. Long-term effects of photoperiod, temperature and their interaction on growth, gill Na+, K+-ATPase activity, seawater tolerance and plasma growth-hormone levels in Atlantic salmon Salmo salar. J Fish Biol. 2013;83: 1197–1209. doi: 10.1111/jfb.12215 24580662
16. McCormick SD, Regish AM, Christensen AK. Distinct freshwater and seawater isoforms of Na+/K+-ATPase in gill chloride cells of Atlantic salmon. J Exp Biol. 2009;212: 3994–4001. doi: 10.1242/jeb.037275 19946077
17. Zaugg WS, Wagner HH. Gill ATPase activity related to parr-smolt transformation and migration in steelhead trout (Salmo gairdneri): Influence of photoperiod and temperature. Comparative Biochemistry and Physiology—Part B: Biochemistry and. 1973;45: 955–965.
18. Berthelot C, Brunet F, Chalopin D, Juanchich A, Bernard M, Noel B, et al. The rainbow trout genome provides novel insights into evolution after whole-genome duplication in vertebrates. Nat Commun. 2014;5: 3657. doi: 10.1038/ncomms4657 24755649
19. Davidson WS, Koop BF, Jones SJM, Iturra P, Vidal R, Maass A, et al. Sequencing the genome of the Atlantic salmon (Salmo salar). Genome Biol. 2010;11.
20. Johansson L, Timmerhaus G, Afanasyev S, Jørgensen SM, Krasnov A. Smoltification and seawater transfer of Atlantic salmon (Salmo salar L.) is associated with systemic repression of the immune transcriptome. Fish Shellfish Immunol. 2016;58: 33–41. doi: 10.1016/j.fsi.2016.09.026 27637733
21. Norman JD, Ferguson MM, Danzmann RG. An integrated transcriptomic and comparative genomic analysis of differential gene expression in Arctic charr (Salvelinus alpinus) following seawater exposure. J Exp Biol. 2014;217: 4029–4042. doi: 10.1242/jeb.107441 25278466
22. Norman JD, Ferguson MM, Danzmann RG. Transcriptomics of salinity tolerance capacity in Arctic charr (Salvelinus alpinus): a comparison of gene expression profiles between divergent QTL genotypes. American Journal of Physiology-Heart and Circulatory Physiology. 2013.
23. Baerwald MR, Meek MH, Stephens MR, Nagarajan RP, Goodbla AM, Tomalty KMH, et al. Migration-related phenotypic divergence is associated with epigenetic modifications in rainbow trout. Mol Ecol. 2016;25: 1785–1800. doi: 10.1111/mec.13231 25958780
24. Hecht BC, Thrower FP, Hale MC, Miller MR, Nichols KM. Genetic architecture of migration-related traits in rainbow and steelhead trout, Oncorhynchus mykiss. G3 (Bethesda). 2012;2: 1113–1127.
25. Hecht BC, Valle ME, Thrower FP, Nichols KM. Divergence in expression of candidate genes for the smoltification process between juvenile resident rainbow and anadromous steelhead trout. Mar Biotechnol (NY). 2014;16: 638–656.
26. Sutherland BJ, Hanson KC, Jantzen JR, Koop BF, Smith CT. Divergent immunity and energetic programs in the gills of migratory and resident Oncorhynchus mykiss. Mol Ecol. 2014;23: 1952–1964. doi: 10.1111/mec.12713 24612010
27. Hale MC, McKinney GJ, Thrower FP, Nichols KM. RNA-seq reveals differential gene expression in the brains of juvenile resident and migratory smolt rainbow trout (Oncorhynchus mykiss). Comparative Biochemistry and Physiology Part D: Genomics and Proteomics. 2016;20: 136–150.
28. Shimomura T, Nakajima T, Horikoshi M, Iijima A, Urabe H, Mizuno S, et al. Relationships between gill Na+,K+-ATPase activity and endocrine and local insulin-like growth factor-I levels during smoltification of masu salmon (Oncorhynchus masou). Gen Comp Endocrinol. 2012;178: 427–435. doi: 10.1016/j.ygcen.2012.06.011 22749841
29. Beckman BR, Shimizu M, Gadberry BA, Cooper KA. Response of the somatotropic axis of juvenile coho salmon to alterations in plane of nutrition with an analysis of the relationships among growth rate and circulating IGF-I and 41 kDa IGFBP. Gen Comp Endocrinol. 2004;135: 334–344. doi: 10.1016/j.ygcen.2003.10.013 14723885
30. Björnsson BT, Bradley TM. Epilogue: Past successes, present misconceptions and future milestones in salmon smoltification research. Aquaculture. 2007;273: 384–391.
31. Zhu W, Smith JW, Huang CM. Mass spectrometry-based label-free quantitative proteomics. J Biomed Biotechnol. 2010;2010: 840518. doi: 10.1155/2010/840518 19911078
32. Geromanos SJ, Vissers JP, Silva JC, Dorschel CA, Li G, Gorenstein MV, et al. The detection, correlation, and comparison of peptide precursor and product ions from data independent LC-MS with data dependant LC-MS/MS. Proteomics. 2009;9: 1683–1695. doi: 10.1002/pmic.200800562 19294628
33. Liumbruno G, D’Alessandro A, Grazzini G, Zolla L. Blood-related proteomics. Journal of proteomics. 2010;73: 483–507. doi: 10.1016/j.jprot.2009.06.010 19567275
34. Barnea E, Sorkin R, Ziv T, Beer I, Admon A. Evaluation of prefractionation methods as a preparatory step for multidimensional based chromatography of serum proteins. Proteomics. 2005;5: 3367–3375. doi: 10.1002/pmic.200401221 16047308
35. Fang Y, Gao X, Zha J, Ning B, Li X, Gao Z, et al. Identification of differential hepatic proteins in rare minnow (Gobiocypris rarus) exposed to pentachlorophenol (PCP) by proteomic analysis. Toxicol Lett. 2010;199: 69–79. doi: 10.1016/j.toxlet.2010.08.008 20732397
36. Corthals GL, Wasinger VC, Hochstrasser DF, Sanchez J. The dynamic range of protein expression: a challenge for proteomic research. Electrophoresis: An International Journal. 2000;21: 1104–1115.
37. Bandow JE. Comparison of protein enrichment strategies for proteome analysis of plasma. Proteomics. 2010;10: 1416–1425. doi: 10.1002/pmic.200900431 20127685
38. Millioni R, Tolin S, Puricelli L, Sbrignadello S, Fadini GP, Tessari P, et al. High abundance proteins depletion vs low abundance proteins enrichment: comparison of methods to reduce the plasma proteome complexity. PloS one. 2011;6: e19603. doi: 10.1371/journal.pone.0019603 21573190
39. De Bock M, De Seny D, Meuwis M, Servais A, Minh TQ, Closset J, et al. Comparison of three methods for fractionation and enrichment of low molecular weight proteins for SELDI-TOF-MS differential analysis. Talanta. 2010;82: 245–254. doi: 10.1016/j.talanta.2010.04.029 20685463
40. Jacobs JM, Adkins JN, Qian W, Liu T, Shen Y, Camp DG, et al. Utilizing human blood plasma for proteomic biomarker discovery. Journal of proteome research. 2005;4: 1073–1085. doi: 10.1021/pr0500657 16083256
41. Anderson NL, Anderson NG. The human plasma proteome: history, character, and diagnostic prospects. Mol Cell Proteomics. 2002;1: 845–867. doi: 10.1074/mcp.r200007-mcp200 12488461
42. Pernemalm M, Lehtiö J. Mass spectrometry-based plasma proteomics: state of the art and future outlook. Expert review of proteomics. 2014;11: 431–448. doi: 10.1586/14789450.2014.901157 24661227
43. Geyer PE, Holdt LM, Teupser D, Mann M. Revisiting biomarker discovery by plasma proteomics. Mol Syst Biol. 2017;13: 942. doi: 10.15252/msb.20156297 28951502
44. Hanash SM, Pitteri SJ, Faca VM. Mining the plasma proteome for cancer biomarkers. Nature. 2008;452: 571. doi: 10.1038/nature06916 18385731
45. Hye A, Lynham S, Thambisetty M, Causevic M, Campbell J, Byers H, et al. Proteome-based plasma biomarkers for Alzheimer’s disease. Brain. 2006;129: 3042–3050. doi: 10.1093/brain/awl279 17071923
46. Beckman BR. Perspectives on concordant and discordant relations between insulin-like growth factor 1 (IGF1) and growth in fishes. Gen Comp Endocrinol. 2011;170: 233–252. doi: 10.1016/j.ygcen.2010.08.009 20800595
47. Beckman BR, Fairgrieve W, Cooper KA, Mahnken CVW, Beamish RJ. Evaluation of endocrine indices of growth in individual postsmolt coho salmon. Trans Am Fish Soc. 2004;133: 1057–1067.
48. O’Loughlin A, McGee M, Doyle S, Earley B. Biomarker responses to weaning stress in beef calves. Res Vet Sci. 2014;97: 458–463. doi: 10.1016/j.rvsc.2014.06.003 24992823
49. Fast MD, Hosoya S, Johnson SC, Afonso LO. Cortisol response and immune-related effects of Atlantic salmon (Salmo salar Linnaeus) subjected to short-and long-term stress. Fish Shellfish Immunol. 2008;24: 194–204. doi: 10.1016/j.fsi.2007.10.009 18065240
50. Palermo F, Mosconi G, Angeletti M, Polzonetti-Magni A. Assessment of water pollution in the Tronto River (Italy) by applying useful biomarkers in the fish model Carassius auratus. Arch Environ Contam Toxicol. 2008;55: 295–304. doi: 10.1007/s00244-007-9113-2 18214578
51. Hiramatsu N, Matsubara T, Fujita T, Sullivan CV, Hara A. Multiple piscine vitellogenins: biomarkers of fish exposure to estrogenic endocrine disruptors in aquatic environments. Mar Biol. 2006;149: 35–47.
52. Barton C, Beck P, Kay R, Teale P, Roberts J. Multiplexed LC-MS/MS analysis of horse plasma proteins to study doping in sport. Proteomics. 2009;9: 3058–3065. doi: 10.1002/pmic.200800737 19526555
53. Morro B, Balseiro P, Albalat A, Pedrosa C, MacKenzie S, Nakamura S, et al. Effects of different photoperiod regimes on the smoltification and seawater adaptation of seawater-farmed rainbow trout (Oncorhynchus mykiss): Insights from Na+, K+–ATPase activity and transcription of osmoregulation and growth regulation genes. Aquaculture. 2019;507: 282–292.
54. McCormick SD. Methods for nonlethal gill biopsy and measurement of Na+,K+-ATPase activity. Can J Fish Aquat Sci. 1993;50: 656–658.
55. Madsen S, Naamansen E. Plasma ionic regulation and gill Na /K -ATPase changes during rapid transfer to sea water of yearling rainbow trout, Salmo gairdneri: time course and seasonal variation. J Fish Biol. 1989;34: 829–840.
56. Ewing R, Barratt D, Garlock D. Physiological changes related to migration tendency in rainbow trout (Oncorhynchus mykiss). Aquaculture. 1994;121: 277–287.
57. Zhang W, Carriquiry A, Nettleton D, Dekkers JC. Pooling mRNA in microarray experiments and its effect on power. Bioinformatics. 2007;23: 1217–1224. doi: 10.1093/bioinformatics/btm081 17344238
58. Weinkauf M, Hiddemann W, Dreyling M. Sample pooling in 2-D gel electrophoresis: A new approach to reduce nonspecific expression background. Electrophoresis. 2006;27: 4555–4558. doi: 10.1002/elps.200600207 17066383
59. Neubauer H, Clare SE, Kurek R, Fehm T, Wallwiener D, Sotlar K, et al. Breast cancer proteomics by laser capture microdissection, sample pooling, 54-cm IPG IEF, and differential iodine radioisotope detection. Electrophoresis. 2006;27: 1840–1852. doi: 10.1002/elps.200500739 16645950
60. Horgan GW. Sample size and replication in 2D gel electrophoresis studies. Journal of proteome research. 2007;6: 2884–2887. doi: 10.1021/pr070114a 17550277
61. Karp NA, Lilley KS. Design and analysis issues in quantitative proteomics studies. Proteomics. 2007;7: 42–50. doi: 10.1002/pmic.200700683 17893850
62. Karp NA, Spencer M, Lindsay H, O’Dell K, Lilley KS. Impact of replicate types on proteomic expression analysis. Journal of proteome research. 2005;4: 1867–1871. doi: 10.1021/pr050084g 16212444
63. Diz AP, Truebano M, Skibinski DO. The consequences of sample pooling in proteomics: an empirical study. Electrophoresis. 2009;30: 2967–2975. doi: 10.1002/elps.200900210 19676090
64. Zolg W. The proteomic search for diagnostic biomarkers: Lost in translation? Mol Cell Proteomics. 2006;5: 1720–1726. doi: 10.1074/mcp.R600001-MCP200 16546995
65. Karp NA, Lilley KS. Investigating sample pooling strategies for DIGE experiments to address biological variability. Proteomics. 2009;9: 388–397. doi: 10.1002/pmic.200800485 19105178
66. Shih JH, Michalowska AM, Dobbin K, Ye Y, Qiu TH, Green JE. Effects of pooling mRNA in microarray class comparisons. Bioinformatics. 2004;20: 3318–3325. doi: 10.1093/bioinformatics/bth391 15247103
67. Martínez-Fernández M, Rodríguez-Piñeiro AM, Oliveira E, Páez de la Cadena María, Rolán-Alvarez E. Proteomic comparison between two marine snail ecotypes reveals details about the biochemistry of adaptation. Journal of proteome research. 2008;7: 4926–4934. doi: 10.1021/pr700863e 18937509
68. Kendziorski C, Irizarry RA, Chen KS, Haag JD, Gould MN. On the utility of pooling biological samples in microarray experiments. Proc Natl Acad Sci U S A. 2005;102: 4252–4257. doi: 10.1073/pnas.0500607102 15755808
69. Paulo JA. Practical and Efficient Searching in Proteomics: A Cross Engine Comparison. Webmedcentral. 2013;4: doi: 10.9754/journal.wplus.2013.0052 25346847
70. Wickham H. ggplot2 Elegant Graphics for Data Analysis Introduction; 2009.
71. Li G, Vissers JP, Silva JC, Golick D, Gorenstein MV, Geromanos SJ. Database searching and accounting of multiplexed precursor and product ion spectra from the data independent analysis of simple and complex peptide mixtures. Proteomics. 2009;9: 1696–1719. doi: 10.1002/pmic.200800564 19294629
72. Bhatia VN, Perlman DH, Costello CE, McComb ME. Software tool for researching annotations of proteins: open-source protein annotation software with data visualization. Anal Chem. 2009;81: 9819–9823. doi: 10.1021/ac901335x 19839595
73. Vu VQ. ggbiplot: A ggplot2 based biplot. R package. 2011;342.
74. Adkins JN, Monroe ME, Auberry KJ, Shen Y, Jacobs JM, Camp DG II, et al. A proteomic study of the HUPO Plasma Proteome Project’s pilot samples using an accurate mass and time tag strategy. Proteomics. 2005;5: 3454–3466. doi: 10.1002/pmic.200401333 16052625
75. Simpson KL, Whetton AD, Dive C. Quantitative mass spectrometry-based techniques for clinical use: biomarker identification and quantification. Journal of Chromatography B. 2009;877: 1240–1249.
76. Nynca J, Arnold G, Fröhlich T, Ciereszko A. Proteomic identification of rainbow trout blood plasma proteins and their relationship to seminal plasma proteins. Proteomics. 2017;17: 1600460.
77. Medina-Gali R, Belló-Pérez M, Ciordia S, Mena MC, Coll J, Novoa B, et al. Plasma proteomic analysis of zebrafish following spring viremia of carp virus infection. Fish Shellfish Immunol. 2019;86: 892–899. doi: 10.1016/j.fsi.2018.12.035 30580041
78. Kültz D, Li J, Zhang X, Villarreal F, Pham T, Paguio D. Population-specific plasma proteomes of marine and freshwater three-spined sticklebacks (Gasterosteus aculeatus). Proteomics. 2015;15: 3980–3992. doi: 10.1002/pmic.201500132 26223892
79. Enerstvedt KS, Sydnes MO, Pampanin DM. Study of the plasma proteome of Atlantic cod (Gadus morhua): Changes due to crude oil exposure. Mar Environ Res. 2018;138: 46–54. doi: 10.1016/j.marenvres.2018.03.009 29692335
80. Kumar G, Hummel K, Razzazi-Fazeli E, El-Matbouli M. Proteome Profiles of Head Kidney and Spleen of Rainbow Trout (Oncorhynchus mykiss). Proteomics. 2018;18: 1800101.
81. Nynca J, Arnold GJ, Fröhlich T, Ciereszko A. Shotgun proteomics of rainbow trout ovarian fluid. Reproduction, Fertility and Development. 2015;27: 504–512.
82. Nynca J, Arnold GJ, Fröhlich T, Otte K, Flenkenthaler F, Ciereszko A. Proteomic identification of rainbow trout seminal plasma proteins. Proteomics. 2014;14: 133–140. doi: 10.1002/pmic.201300267 24174285
83. Murphy S, Dowling P. DIGE Analysis of ProteoMiner TM Fractionated Serum/Plasma Samples. In: Anonymous Difference Gel Electrophoresis. Springer; 2018. pp. 109–114.
84. Cunha SR, Mohler PJ. Ankyrin protein networks in membrane formation and stabilization. J Cell Mol Med. 2009;13: 4364–4376. doi: 10.1111/j.1582-4934.2009.00943.x 19840192
85. Tanaka Y, Akiyama H, Kuroda T, Jung G, Tanahashi K, Sugaya H, et al. A novel approach and protocol for discovering extremely low-abundance proteins in serum. Proteomics. 2006;6: 4845–4855. doi: 10.1002/pmic.200500774 16878292
86. Mohandas N, Evans E. Mechanical properties of the red cell membrane in relation to molecular structure and genetic defects. Annu Rev Biophys Biomol Struct. 1994;23: 787–818. doi: 10.1146/annurev.bb.23.060194.004035 7919799
87. Yasunaga M, Ipsaro JJ, Mondragón A. Structurally similar but functionally diverse ZU5 domains in human erythrocyte ankyrin. J Mol Biol. 2012;417: 336–350. doi: 10.1016/j.jmb.2012.01.041 22310050
88. Kuchta RD, Stengel G. Mechanism and evolution of DNA primases. Biochimica et Biophysica Acta (BBA)-Proteins and Proteomics. 2010;1804: 1180–1189.
89. Li C, Tan XF, Lim TK, Lin Q, Gong Z. Comprehensive and quantitative proteomic analyses of zebrafish plasma reveals conserved protein profiles between genders and between zebrafish and human. Scientific reports. 2016;6: 24329. doi: 10.1038/srep24329 27071722
90. Chi NC, Shaw RM, De Val S, Kang G, Jan LY, Black BL, et al. Foxn4 directly regulates tbx2b expression and atrioventricular canal formation. Genes Dev. 2008;22: 734–739. doi: 10.1101/gad.1629408 18347092
91. Li J, Yue Y, Dong X, Jia W, Li K, Liang D, et al. Zebrafish foxc1a plays a crucial role in early somitogenesis by restricting the expression of aldh1a2 directly. J Biol Chem. 2015;290: 10216–10228. doi: 10.1074/jbc.M114.612572 25724646
92. Watanabe K, Umeda T, Niwa K, Naguro I, Ichijo H. A PP6-ASK3 module coordinates the bidirectional cell volume regulation under osmotic stress. Cell reports. 2018;22: 2809–2817. doi: 10.1016/j.celrep.2018.02.045 29539411
93. Sullivan LS, Bowne SJ, Koboldt DC, Cadena EL, Heckenlively JR, Branham KE, et al. A novel dominant mutation in SAG, the arrestin-1 gene, is a common cause of retinitis pigmentosa in Hispanic families in the Southwestern United States. Invest Ophthalmol Vis Sci. 2017;58: 2774–2784. doi: 10.1167/iovs.16-21341 28549094
94. Renninger SL, Gesemann M, Neuhauss SC. Cone arrestin confers cone vision of high temporal resolution in zebrafish larvae. Eur J Neurosci. 2011;33: 658–667. doi: 10.1111/j.1460-9568.2010.07574.x 21299656
95. Murthy KR, Goel R, Subbannayya Y, Jacob HK, Murthy PR, Manda SS, et al. Proteomic analysis of human vitreous humor. Clinical proteomics. 2014;11: 29. doi: 10.1186/1559-0275-11-29 25097467
96. Dann SG, Allison WT, Levin DB, Hawryshyn CW. Identification of a unique transcript down-regulated in the retina of rainbow trout (Oncorhynchus mykiss) at smoltification. Comp Biochem Physiol B Biochem Mol Biol. 2003;136: 849–860. doi: 10.1016/s1096-4959(03)00262-8 14662307
97. Ebbesson LO, Ebbesson SO, Nilsen TO, Stefansson SO, Holmqvist B. Exposure to continuous light disrupts retinal innervation of the preoptic nucleus during parr–smolt transformation in Atlantic salmon. Aquaculture. 2007;273: 345–349.
98. Wang X, Liu Q, Xu S, Xiao Y, Wang Y, Feng C, et al. Transcriptome Dynamics During Turbot Spermatogenesis Predicting the Potential Key Genes Regulating Male Germ Cell Proliferation and Maturation. Scientific reports. 2018;8: 15825. doi: 10.1038/s41598-018-34149-5 30361543
99. Foote CJ, Mayer I, Wood CC, Clarke WC, Blackburn J. On the developmental pathway to nonanadromy in sockeye salmon, Oncorhynchus nerka. Can J Zool. 1994;72: 397–405.
100. Thorpe JE, Metcalfe NB. Is smolting a positive or a negative developmental decision? Aquaculture. 1998;168: 95–103.
101. Nichols KM, Edo AF, Wheeler PA, Thorgaard GH. The genetic basis of smoltification-related traits in Oncorhynchus mykiss. Genetics. 2008;179: 1559–1575. doi: 10.1534/genetics.107.084251 18562654
102. Tam S, Tsai M, Snouwaert JN, Kalesnikoff J, Scherrer D, Nakae S, et al. RabGEF1 is a negative regulator of mast cell activation and skin inflammation. Nat Immunol. 2004;5: 844. doi: 10.1038/ni1093 15235600
103. Epting D, Vorwerk S, Hageman A, Meyer D. Expression of rasgef1b in zebrafish. Gene expression patterns. 2007;7: 389–395. doi: 10.1016/j.modgep.2006.11.010 17239665
104. Fischer H, Esbjörnsson M, Sabina RL, Strömberg A, Peyrard-Janvid M, Norman B. AMP deaminase deficiency is associated with lower sprint cycling performance in healthy subjects. J Appl Physiol. 2007.
105. Coughlin DJ, Forry JA, McGlinchey SM, Mitchell J, Saporetti KA, Stauffer KA. Thyroxine induces transitions in red muscle kinetics and steady swimming kinematics in rainbow trout (Oncorhynchus mykiss). J Exp Zool. 2001;290: 115–124. doi: 10.1002/jez.1041 11471141
106. Martinez I, Bang B, Hatlen B, Blix P. Myofibrillar proteins in skeletal muscles of parr, smolt and adult atlantic salmon (Salmo salar l.). Comparison with another salmonid, the arctic charr Salvelinus alpinus (l.). Comparative Biochemistry and Physiology—Part B: Biochemistry and. 1993;106: 1021–1028.
107. Rousseau K, Martin P, Boeuf G, Dufour S. Salmonid smoltification. Metamorphosis in fish. CRC Press, Boca Raton. 2012: 167–215.
108. Millar JS, Maugeais C, Ikewaki K, Kolansky DM, Barrett PHR, Budreck EC, et al. Complete deficiency of the low-density lipoprotein receptor is associated with increased apolipoprotein B-100 production. Arterioscler Thromb Vasc Biol. 2005;25: 560–565. doi: 10.1161/01.ATV.0000155323.18856.a2 15637307
109. Innerarity TL, Mahley RW, Weisgraber KH, Bersot TP, Krauss RM, Vega GL, et al. Familial defective apolipoprotein B-100: a mutation of apolipoprotein B that causes hypercholesterolemia. J Lipid Res. 1990;31: 1337–1349. 2280177
110. Pankov R, Yamada KM. Fibronectin at a glance. J Cell Sci. 2002;115: 3861–3863. doi: 10.1242/jcs.00059 12244123
111. Wang J, Karra R, Dickson AL, Poss KD. Fibronectin is deposited by injury-activated epicardial cells and is necessary for zebrafish heart regeneration. Dev Biol. 2013;382: 427–435. doi: 10.1016/j.ydbio.2013.08.012 23988577
112. Rubin CI, Atweh GF. The role of stathmin in the regulation of the cell cycle. J Cell Biochem. 2004;93: 242–250. doi: 10.1002/jcb.20187 15368352
113. Tilli TM, da Silva Castro C, Tuszynski JA, Carels N. A strategy to identify housekeeping genes suitable for analysis in breast cancer diseases. BMC Genomics. 2016;17: 639. doi: 10.1186/s12864-016-2946-1 27526934
114. D’Avanzo N, Cheng WW, Doyle DA, Nichols CG. Direct and specific activation of human inward rectifier K+ channels by membrane phosphatidylinositol 4,5-bisphosphate. J Biol Chem. 2010;285: 37129–37132. doi: 10.1074/jbc.C110.186692 20921230
115. Zhou J, Li W, Kamei H, Duan C. Duplication of the IGFBP-2 gene in teleost fish: protein structure and functionality conservation and gene expression divergence. PloS one. 2008;3: e3926. doi: 10.1371/journal.pone.0003926 19081843
116. Duan C, Ding J, Li Q, Tsai W, Pozios K. Insulin-like growth factor binding protein 2 is a growth inhibitory protein conserved in zebrafish. Proc Natl Acad Sci U S A. 1999;96: 15274–15279. doi: 10.1073/pnas.96.26.15274 10611375
117. Selvaraju S, El Rassi Z. Reduction of protein concentration range difference followed by multicolumn fractionation prior to 2-DE and LC-MS/MS profiling of serum proteins. Electrophoresis. 2011;32: 674–685. doi: 10.1002/elps.201000606 21365658
118. Klingenberg R, Lebens M, Hermansson A, Fredrikson GN, Strodthoff D, Rudling M, et al. Intranasal immunization with an apolipoprotein B-100 fusion protein induces antigen-specific regulatory T cells and reduces atherosclerosis. Arterioscler Thromb Vasc Biol. 2010;30: 946–952. doi: 10.1161/ATVBAHA.109.202671 20167655
119. Kreuter J, Hekmatara T, Dreis S, Vogel T, Gelperina S, Langer K. Covalent attachment of apolipoprotein AI and apolipoprotein B-100 to albumin nanoparticles enables drug transport into the brain. J Controlled Release. 2007;118: 54–58.
120. Segrest JP, Jones MK, De Loof H, Dashti N. Structure of apolipoprotein B-100 in low density lipoproteins. J Lipid Res. 2001;42: 1346–1367. 11518754
Článok vyšiel v časopise
PLOS One
2020 Číslo 1
- Metamizol jako analgetikum první volby: kdy, pro koho, jak a proč?
- Nejasný stín na plicích – kazuistika
- Masturbační chování žen v ČR − dotazníková studie
- Těžké menstruační krvácení může značit poruchu krevní srážlivosti. Jaký management vyšetření a léčby je v takovém případě vhodný?
- Fixní kombinace paracetamol/kodein nabízí synergické analgetické účinky
Najčítanejšie v tomto čísle
- Psychometric validation of Czech version of the Sport Motivation Scale
- Comparison of Monocyte Distribution Width (MDW) and Procalcitonin for early recognition of sepsis
- Effects of supplemental creatine and guanidinoacetic acid on spatial memory and the brain of weaned Yucatan miniature pigs
- Accelerated sparsity based reconstruction of compressively sensed multichannel EEG signals