Transferrin Identification in Sterlet (Acipenser ruthenus) Reproductive System
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
LM2018099
the Ministry of Education, Youth and Sports of the Czech Republic - projects CENAKVA
CZ.02.1.01./0.0/0.0/16_025/0007370
Biodiversity
No. 125/2016/Z
the Grant Agency of the University of South Bohemia
16-02407Y
the Czech Science Foundation
LM2015055
the Czech research infrastructure for systems biology C4SYS
LM2015042
the Ministry of Education, Youth and Sports of the Czech Republic under the Projects CESNET
LM2015085
CERIT-Scientific Cloud
PubMed
31575042
PubMed Central
PMC6826671
DOI
10.3390/ani9100753
PII: ani9100753
Knihovny.cz E-zdroje
- Klíčová slova
- Wolffian duct, kidney, sperm, testes, transcriptome,
- Publikační typ
- časopisecké články MeSH
Transferrins are a superfamily of iron-binding proteins and are recognized as multifunctional proteins. In the present study, transcriptomic and proteomic methods were used to identify transferrins in the reproductive organs and sperm of out-of-spawning and spermiating sterlet (Acipenser ruthenus) males. The results showed that seven transferrin transcripts were identified in the transcriptome of sterlet, and these transcripts were qualified as two different transferrin genes, serotransferrin and melanotransferrin, with several isoforms present for serotransferrin. The relative abundance of serotransferrin isoforms was higher in the kidneys and Wolffian ducts in the spermiating males compared to out-of-spawning males. In addition, transferrin was immunodetected in sterlet seminal plasma, but not in sterlet spermatozoa extract. Mass spectrometry identification of transferrin in seminal plasma but not in spermatozoa corroborates immunodetection. The identification of transferrin in the reproductive organs and seminal plasma of sterlet in this study provides the potential function of transferrin during sturgeon male reproduction.
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Mackenzie E.L., Iwasaki K., Tsuji Y. Intracellular iron transport and storage: From molecular mechanisms to health implications. Antioxid. Redox Signal. 2014;10:997–1030. doi: 10.1089/ars.2007.1893. PubMed DOI PMC
Ellis A.E. Immunity to bacteria in fish. Fish. Shellfish Immunol. 1999;9:291–308. doi: 10.1006/fsim.1998.0192. DOI
Stafford J.L., Belosevic M. Transferrin and the innate immune response of fish: Identification of a novel mechanism of macrophage activation. Dev. Comp. Immunol. 2003;2:539–554. doi: 10.1016/S0145-305X(02)00138-6. PubMed DOI
Jurecka P., Irnazarow I., Stafford J.L., Ruszczyk A., Taverne N., Belosevic M. The induction of nitric oxide response of carp macrophages by transferrin is induced by the allelic diversity of the molecule. Fish. Shellfish Immunol. 2009;26:632–638. doi: 10.1016/j.fsi.2008.10.007. PubMed DOI
Li P., Hulak M., Koubek P., Sulc M., Dzyuba B., Boryshpolets S., Rodina M., Gela D., Manaskova-Postlerova P., Peknicova J., et al. Ice-age endurance: The effects of cryopreservation on proteins of sperm of common carp, Cyprinus carpio L. Theriogenology. 2010;74:413–423. doi: 10.1016/j.theriogenology.2010.02.024. PubMed DOI
Dietrich M.A., Żmijewski D., Karol H., Hejmej A., Bilińska B., Jurecka P., Irnazarow I., Słowińska M., Hliwa P., Ciereszko A. Isolation and characterization of transferrin from common carp (Cyprinus carpio L) seminal plasma. Fish. Shellfish Immunol. 2010;29:66–74. doi: 10.1016/j.fsi.2010.02.015. PubMed DOI
Dietrich M.A., Dietrich G.J., Hliwa P., Ciereszko A. Carp transferrin can protect spermatozoa against toxic effects of cadmium ions. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2011;153:422–429. doi: 10.1016/j.cbpc.2011.02.003. PubMed DOI
Wojtczak M., Dietrich G.J., Ciereszko A. Transferrin and antiproteases are major proteins of common carp seminal plasma. Fish. Shellfish Immunol. 2005;19:387–391. doi: 10.1016/j.fsi.2005.01.009. PubMed DOI
Barthelemy C., Khalfoun B., Guillaumin J.M., Lecomte P., Bardos P. Seminal fluid transferrin as an index of gonadal function in men. J. Reprod. Infertil. 1988;82:113–118. doi: 10.1530/jrf.0.0820113. PubMed DOI
Wojtczak M., Dietrich G.J., Irnazarow I., Jurecka P., Slowinska M., Ciereszko A. Polymorphism of transferrin of carp seminal plasma: Relationship to blood transferrin and sperm motility characteristics. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2007;148:426–431. doi: 10.1016/j.cbpb.2007.07.011. PubMed DOI
Nynca J., Arnold G.J., Froehlich 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. PubMed DOI
Nynca J., Dietrich M.A., Adamek M., Steinhagen D., Bilinska B., Hejmej A., Ciereszko A. Purification, characterization and expression of transferrin from rainbow trout seminal plasma. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 2017;208:38–46. doi: 10.1016/j.cbpb.2017.04.002. PubMed DOI
Skinner M.K., Griswold M.D. Secretion of testicular transferrin by cultured Sertoli cells is regulated by hormones and retinoids. Biol. Reprod. 1982;27:211–221. doi: 10.1095/biolreprod27.1.211. PubMed DOI
Skinner M.K., Griswold M.D. Sertoli cells synthesize and secrete transferrin-like protein. J. Biol. Chem. 1980;255:9523–9525. PubMed
Mudumana S.P., Wan H.Y., Singh M., Korzh V., Gong Z.Y. Expression analyses of zebrafish transferrin, ifabp, and elastaseB mRNAs as differentiation markers for the three major endodermal organs: Liver, intestine, and exocrine pancreas. Dev. Dyn. 2004;230:165–173. doi: 10.1002/dvdy.20032. PubMed DOI
Denovan-Wright E.M., Ramsey N.B., McCormick C.J., Lazier C.B., Wright J.M. Nucleotide sequence of transferrin cDNAs and tissue-specific of the transferrin gene in Atlantic cod (Gadus morhua) Physiol. B Biochem. Mol. Biol. 1996;113:269–273. doi: 10.1016/0305-0491(95)02023-3. PubMed DOI
Mikawa N., Hirono I., Aoki T. Structure of medaka transferrin gene and its 59-flanking region. Mol. Mar. Biol. Biotechnol. 1996;5:225–229. PubMed
Lee J.Y., Tange N., Yamashita H., Hirono I., Aoki T. Cloning and Characterization of Transferrin cDNA from Coho Salmon (Oncorhynchus kisutch) Fish. Pathol. 1995;30:271–277. doi: 10.3147/jsfp.30.271. DOI
Ford M.J. Molecular evolution of transferrin: Evidence for positive selection in salmonids. Mol. Biol. Evol. 2001;18:639–647. doi: 10.1093/oxfordjournals.molbev.a003844. PubMed DOI
Alavi S.M.H., Cosson J. Sperm motility in fishes. (II) Effects of ions and osmolality: A review. Cell Biol. Int. 2006;30:1–14. doi: 10.1016/j.cellbi.2005.06.004. PubMed DOI
Alavi S., Rodina M., Gela D., Linhart O. Sperm biology and control of reproduction in sturgeon: (I) testicular development, sperm maturation and seminal plasma characteristics. Rev. Fish. Biol. Fisher. 2012;22:695–717. doi: 10.1007/s11160-012-9268-4. DOI
Dzyuba B., Cosson J., Boryshpolets S., Bondarenko O., Dzyuba V., Prokopchuk G., Gazo I., Rodina M., Linhart O. In vitro sperm maturation in sterlet, Acipenser ruthenus. Reprod. Biol. 2014;14:160–163. doi: 10.1016/j.repbio.2014.01.003. PubMed DOI
Dzyuba B., Boryshpolets S., Cosson J., Dzyuba V., Fedorov P., Saito T., Psenicka M., Linhart O., Rodina M. Motility and fertilization ability of sterlet Acipenser ruthenus testicular sperm after cryopreservation. Cryobiology. 2014;69:339–341. doi: 10.1016/j.cryobiol.2014.07.008. PubMed DOI
Dzyuba B., Bondarenko O., Rodina M., Dzyuba V., Cosson J., Linhart O., Shelton W.L., Boryshpolets S., Fedorov P. Sperm maturation in sturgeon (Actinopterygii, Acipenseriformes): A review. Theriogenology. 2017;97:134–138. doi: 10.1016/j.theriogenology.2017.04.034. PubMed DOI
Bolger A.M., Lohse M., Usadel B. Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–2120. doi: 10.1093/bioinformatics/btu170. PubMed DOI PMC
Grabherr M.G., Haas B.J., Yassour M., Levin J.Z., Thompson D.A., Amit I., Adiconis X., Fan L., Raychowdhury R., Zeng Q.D., et al. Trinity: Reconstructing a full-length transcriptome without a genome from RNA-Seq data. Nature Biotechnol. 2011;29:644–652. doi: 10.1038/nbt.1883. PubMed DOI PMC
Gurevich A., Saveliev V., Vyahhi N., Tesler G. QUAST: Quality assessment tool for genome assemblies. Bioinformatics. 2013;29:1072–1075. doi: 10.1093/bioinformatics/btt086. PubMed DOI PMC
Waterhouse R.M., Seppey M., Simão F.A., Manni M., Ioannidis P., Klioutchnikov G., Kriventseva E.V., Zdobnov E.M. BUSCO applications from quality assessments to gene prediction and phylogenomics. Mol. Biol. Evol. 2017;35:543–548. doi: 10.1093/molbev/msx319. PubMed DOI PMC
Li B., Dewey C.N. RSEM: Accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform. 2011;12 doi: 10.1186/1471-2105-12-323. PubMed DOI PMC
Huang Y., Chain F.J., Panchal M., Eizaguirre C., Kalbe M., Lenz T.L., Samonte I.E., Stoll M., Bornberg-Bauer E., Reusch T.B., et al. Transcriptome profiling of immune tissues reveals habitat-specific gene expression between lake and river sticklebacks. Mol. Ecol. 2016;25:943–958. doi: 10.1111/mec.13520. PubMed DOI PMC
Robinson M.D., McCarthy D.J., Smyth G.K. edgeR: A Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2010;26:139–140. doi: 10.1093/bioinformatics/btp616. PubMed DOI PMC
Katoh K., Standley D.M. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol. Biol. Evol. 2013;30:772–780. doi: 10.1093/molbev/mst010. PubMed DOI PMC
Kalyaanamoorthy S., Minh B.Q., Wong T.K.F., von Haeseler A., Jermiin L.S. ModelFinder: Fast model selection for accurate phylogenetic estimates. Nat. Methods. 2017;14:587–589. doi: 10.1038/nmeth.4285. PubMed DOI PMC
Wang H.C., Minh B.Q., Susko E., Roger A.J. Modeling site heterogeneity with posterior mean site frequency profiles accelerates accurate phylogenomic estimation. Syst. Biol. 2017;67:216–235. doi: 10.1093/sysbio/syx068. PubMed DOI
Candiano G., Bruschi M., Musante L., Santucci L., Ghiggeri G.M., Carnemolla B., Orecchia P., Zardi L., Righetti P.G. Blue silver: A very sensitive colloidal Coomassie G-250 staining for proteome analysis. Electrophoresis. 2004;25:1327–1333. doi: 10.1002/elps.200305844. PubMed DOI
Shevchenko A., Tomas H., Havlis J., Olsen J.V., Mann M. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat. Protoc. 2006;1:2856–2860. doi: 10.1038/nprot.2006.468. PubMed DOI
Rehulka P., Zahradnikova M., Rehulkova H., Dvorakova P., Nenutil R., Valik D., Vojtesek B., Hernychova L., Novotny M.V. Microgradient separation technique for purification and fractionation of permethylated N-glycans before mass spectrometric analyses. J. Sep. Sci. 2018;41:1973–1982. doi: 10.1002/jssc.201701339. PubMed DOI
Dillies M.A., Rau A., Aubert J., Hennequet-Antier C., Jeanmougin M., Servant N., Keime C., Marot G., Castel D., Estelle J., et al. A comprehensive evaluation of normalization methods for Illumina high-throughput RNA sequencing data analysis. Brief. Bioinform. 2013;14:671–683. doi: 10.1093/bib/bbs046. PubMed DOI
Hughes A.L., Friedman R. Evolutionary diversification of the vertebrate transferrin multi-gene family. Immunogenetics. 2014;66:651–661. doi: 10.1007/s00251-014-0798-x. PubMed DOI PMC
Brière N., Ferrari J., Chailler P. Insulin and transferrin restore important cellular functions of human fetal kidney in serum-free organ culture. Biochem. Cell Biol. 1991;69:256–262. doi: 10.1139/o91-039. PubMed DOI
Zak O., Aisen P. A new method for obtaining human transferrin C-lobe in the native conformation: Preparation and properties. Biochemistry. 2002;41:1647–1653. doi: 10.1021/bi015868w. PubMed DOI
Sun Y., Zhu Z., Wang R., Sun Y., Xu T. Miiuy croaker transferrin gene and evidence for positive selection events reveal different evolutionary patterns. PLoS ONE. 2012;7:e43936. doi: 10.1371/journal.pone.0043936. PubMed DOI PMC
Ciuraszkiewicz J., Olczak M., Watorek W. Isolation and characterisation of crocodile and python ovotransferrins. Acta Biochim. Pol. 2007;54:175–182. PubMed
Siqueiros-Cendón T., Arévalo-Gallegos S., Iglesias-Figueroa B.F., García-Montoya I.A., Salazar-Martínez J., Rascón-Cruz Q. Immunomodulatory effects of lactoferrin. Acta Pharmacol. Sin. 2014;35:557–566. doi: 10.1038/aps.2013.200. PubMed DOI PMC
Gomme P.T., McCann K.B., Bertolini J. Transferrin: Structure, function and potential therapeutic actions. Drug Discov. Today. 2005;10:267–273. doi: 10.1016/S1359-6446(04)03333-1. PubMed DOI
Hevesy G., Lockner D., Sletten K. Iron metabolism and erythrocyte formation in fish. Acta Physiol. Scand. 1964;60:256–266. doi: 10.1111/j.1748-1716.1964.tb02887.x. PubMed DOI
Dunn L.L., Sekyere E.O., Rahmanto Y.S., Richardson D.R. The function of melanotransferrin: A role in melanoma cell proliferation and tumorigenesis. Carcinogenesis. 2006;27:2157–2169. doi: 10.1093/carcin/bgl045. PubMed DOI
Sekyere E.O., Dunn L.L., Rahmanto Y.S., Richardson D.R. Role of melanotransferrin in iron metabolism: Studies using targeted gene disruption in vivo. Blood. 2006;107:2599–2601. doi: 10.1182/blood-2005-10-4174. PubMed DOI
Kawamoto T., Pan H., Yan W.Q., Ishida H., Usui E., Oda R., Nakamasu K., Noshiro M., Kawashima-Ohya Y., Fujii M., et al. Expression of membrane-bound transferrin-like protein p97 on the cell surface of chondrocytes. Eur. J. Biochem. 1998;256:503–509. doi: 10.1046/j.1432-1327.1998.2560503.x. PubMed DOI
Brown J.P., Woodbury R.G., Hart C.E., Hellström I., Hellström K.E. Quantitative analysis of melanoma-associated antigen p97 in normal and neoplastic tissues. Proc. Natl. Acad. Sci. USA. 1981;78:539–543. doi: 10.1073/pnas.78.1.539. PubMed DOI PMC
Danielsen E.M., van Deurs B. A transferrin-like GPI-linked iron-binding protein in detergent-insoluble noncaveolar microdomains at the apical surface of fetal intestinal epithelial cells. J. Cell Biol. 1995;131:939–950. doi: 10.1083/jcb.131.4.939. PubMed DOI PMC
Rahmanto Y.S., Dunn L.L., Richardson D.R. Identification of distinct changes in gene expression after modulation of melanoma tumor antigen p97 (melanotransferrin) in multiple models in vitro and in vivo. Carcinogenesis. 2007;28:2172–2183. doi: 10.1093/carcin/bgm096. PubMed DOI
Ramirez-Gomez F., Ortiz-Pineda P.A., Rojas-Cartagena C., Suarez-Castillo E.C., Garcia-Ararras J.E. Immune-related genes associated with intestinal tissue in the sea cucumber Holothuria glaberrima. Immunogenetics. 2008;60:57–71. doi: 10.1007/s00251-007-0258-y. PubMed DOI
Rose T.M., Plowman G.D., Teplow D.B., Dreyer W.J., Hellström K.E., Brown J.P. Primary Structure of the Human Melanoma-Associated Antigen p97 (Melanotransferrin) Deduced from the mRNA Sequence. Proc. Natl. Acad. Sci. USA. 1986;83:1261–1265. doi: 10.1073/pnas.83.5.1261. PubMed DOI PMC
Hernandez-Pasos J., Valentin-Tirado G., Garcia-Arraras J.E. Melanotransferrin: New Homolog Genes and Their Differential Expression during Intestinal Regeneration in the Sea Cucumber Holothuria glaberrima. J. Exp. Zool. B Mol. Dev. Evol. 2017;328:259–274. doi: 10.1002/jez.b.22731. PubMed DOI PMC
Betancur-R R., Wiley E.O., Arratia G., Acero A., Bailly N., Miya M., Lecointre G., Orti G. Phylogenetic classification of bony fishes. BMC Evol. Biol. 2017;17:162. doi: 10.1186/s12862-017-0958-3. PubMed DOI PMC
Dietrich M.A., Arnold G.J., Nynca J., Fröhlich T., Otte K., Ciereszko A. Characterization of carp seminal plasma proteome in relation to blood plasma. J. Proteom. 2014;98:218–232. doi: 10.1016/j.jprot.2014.01.005. PubMed DOI
Papadimas I., Papadopoulou F., Ioannidis S., Katsavelir R., Tarlatzis B., Bontis I., Mantalenakis S. Seminal plasma transferrin in infertile men. Arch. Androl. 1992;28:125–133. doi: 10.3109/01485019208987690. PubMed DOI
De Smet H., Blust R., Moens L. Cadmium-binding to transferrin in the plasma of the common carp Cyprinus carpio. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2001;128:45–53. doi: 10.1016/S1532-0456(00)00171-X. PubMed DOI
Sylvester S.R., Griswold M.D. Localization of transferrin and transferrin receptors in rat testes. Biol. Reprod. 1984;31:195–203. doi: 10.1095/biolreprod31.1.195. PubMed DOI
Leichtmann-Bardoogo Y., Cohen L.A., Weiss A., Marohn B., Schubert S., Meinhardt A., Meyron-Holtz E.G. Compartmentalization and regulation of iron metabolism proteins protect male germ cells from iron overload. Am. J. Physiol. Endocrinol. Metab. 2012;302:E1519–E1530. doi: 10.1152/ajpendo.00007.2012. PubMed DOI