Variability in the protein profiles in spermatozoa of two sturgeon species
Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection
Typ dokumentu časopisecké články, validační studie
PubMed
29077704
PubMed Central
PMC5659609
DOI
10.1371/journal.pone.0186003
PII: PONE-D-17-15094
Knihovny.cz E-zdroje
- MeSH
- druhová specificita MeSH
- fertilita MeSH
- motilita spermií MeSH
- proteom metabolismus MeSH
- ryby klasifikace metabolismus MeSH
- spermie metabolismus MeSH
- zvířata MeSH
- Check Tag
- mužské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- validační studie MeSH
- Názvy látek
- proteom MeSH
Conventional sperm analysis (i.e., motility and fertility) has been used to evaluate sperm quality. Understanding the quality of sperm on the molecular level in the sturgeons, Acipenser baerii and A. schrenckii, is essential for the improvement of the conservation of genetic resources and farming performance. In this study, we used the iTRAQ proteomics approach to perform proteomic profiling of spermatozoa associated with sperm quality in sturgeons (Data are available via ProteomeXchange with identifier PXD006108). The results showed 291 and 359 differentially expressed proteins in A. baerii and A. schrenckii, respectively, of which 72 were common to both species and all were upregulated in high quality compared with low quality samples. The differentially expressed proteins were mainly categorized into the generation of precursor metabolites and energy and oxidation, and they were localized to the mitochondria. Three distinguishing pathways, Arginine and proline metabolism, Pyruvate metabolism and the Citrate cycle (TCA cycle) were found to play an important role in energy metabolism, and some substrates could be used in the sperm medium for storage and cryopreservation. The quantity levels of two proteins, CKMT1 and LDHB, were verified by western blot analysis. Moreover, other potential biomarkers involved in oxidation reduction, ubiquitin-proteasome-dependent proteolysis, chaperones and binding activity were also discussed. Our study is the first to use the iTRAQ-based proteomics approach to analyse the sturgeon spermatozoa proteome, and the results that we obtained are valuable for the prediction of sperm quality and reproduction management in these threatened species.
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Birstein VJ, Bemis WE, Waldman JR. The threatened status of acipenseriform species: a summary In: Birstein VJ, Bemis WE, Waldman JR, editors. Sturgeon Biodiversity and Conservation. Netherlands: Springer; 1997. pp. 427–435.
Alavi SM, Rodina M, Policar T, Kozak P, Psenicka M, Linhart O. Semen of Perca fluviatilis L.: sperm volume and density, seminal plasma indices and effects of dilution ratio, ions and osmolality on sperm motility. Theriogenology. 2007; 68(2): 276–283. doi: 10.1016/j.theriogenology.2007.05.045 PubMed DOI
Li P, Hulak M, Linhart O. Sperm proteins in teleostean and chondrostean (sturgeon) fishes. Fish Physiol Biochem. 2009; 35(4): 567–581. doi: 10.1007/s10695-008-9261-y PubMed DOI
Li P, Wei Q, Liu L. DNA integrity of Polyodon spathula cryopreserved sperm. J Appl Ichthy. 2008; 24: 121–125.
Watson PF. The causes of reduced fertility with cryopreserved semen. Anim Reprod Sci. 2000; 60–61: 481–492. PubMed
Pesch S, Hoffmann B. Cryopreservation of spermatozoa in veterinary medicine. J Reprod Med Endocrin. 2007; 4: 101–105.
Tomar AK, Saraswat M, Chhikara N, Kumar S, Yadav VK, Sooch BS, et al. Differential proteomics of sperm: insights, challenges and future prospects. Biomarkers Med. 2010; 4(6): 905–910. PubMed
Aitken RJ, Baker MA. The role of proteomics in understanding sperm cell biology. Int J Androl. 2008; 31: 295–302. doi: 10.1111/j.1365-2605.2007.00851.x PubMed DOI
Oliva R, de Mateo S, Estanyol JM. Sperm cell proteomics. Proteomics. 2009; 9: 1004–1017. doi: 10.1002/pmic.200800588 PubMed DOI
McCauley TC, Zhang H, Bellin ME, Ax RL. Purification and characterization of fertility-associated antigen (FAA) in bovine seminar fluid. Mol Reprod Rev. 1999; 54: 145–153. PubMed
Erikson DW, Way AL, Chapman DA, Killian GJ. Detection of osteopontin on Holstein bull spermatozoa, in cauda epididymal fluid and testis homogenates, and its potential role in bovine fertilization. Reproduction. 2007; 133: 909–917. doi: 10.1530/REP-06-0228 PubMed DOI
D’Amours O, Frenette G, Fortier M, Leclerc P, Sullivan R. Proteomic comparison of detergent-extracted sperm proteins from bulls with different fertility indexes. Reproduction. 2010; 139: 545–556. doi: 10.1530/REP-09-0375 PubMed DOI
Gamboa S, Ramalho-Santos J. SNARE proteins and caveolin-1 in stallion spermatozoa: possible implications for fertility. Theriogenology. 2005; 64: 275–291. doi: 10.1016/j.theriogenology.2004.11.021 PubMed DOI
Novak S, Ruiz-Sanchez A, Dixon WT, Foxcroft GR, Dyck MK. Seminal plasma proteins as potential markers of relative fertility in boars. J Androl. 2010; 31: 188–200. doi: 10.2164/jandrol.109.007583 PubMed DOI
Griveau FJ, Le Lannou D. Reactive oxygen species and human spermatozoa: physiology and pathology. Int J Androl. 1997; 20(2): 61–69. PubMed
Karp G. Cell and Molecular Biology, Fifth edition Hoboken, NJ: John Wiley & Sons; 2008.
Meyers SA. Cryostorage and oxidative stress in mammalian spermatozoa In: Agarwal AAJ, Alvarez J, editors. Studies on Men’s Health and Fertility, Oxidative Stress in Applied Basic Research and Clinical Practice. New York: Springer; 2012. pp. 41–56.
du Plessis SS, Agarwal A, Mohanty G, van der Linde M. Oxidative phosphorylation versus glycolysis: what fuel do spermatozoa use. Asian J Androl. 2015; 17: 230–235. doi: 10.4103/1008-682X.135123 PubMed DOI PMC
Ruiz-Pesini E, Díez-Sánchez C, López-Pérez MJ, Enríquez JA. The role of the mitochondrion in sperm function: is there a place for oxidative phosphorylation or is this a purely glycolytic process? Curr Top Dev Biol. 2007; 77: 3–19. doi: 10.1016/S0070-2153(06)77001-6 PubMed DOI
Hoshi K, Tsukikawa S, Sato A. Importance of Ca2+, K+ and glucose in the medium for sperm penetration through the human zona pellucida. Tohoku J Exp Med. 1991; 165: 99–104. PubMed
Williams AC, Ford WC. The role of glucose in supporting motility and capacitation in human spermatozoa. J Androl. 2001; 22: 680–695. PubMed
Mukai C, Okuno M. Glycolysis plays a major role for adenosine triphosphate supplementation in mouse sperm flagellar movement. Biol Reprod. 2004; 71: 540–547. doi: 10.1095/biolreprod.103.026054 PubMed DOI
Ferramosca A, Zara V. Bioenergetics of mammalian sperm capacitation. Biomed Res Int. 2014; 2014: 902–953. PubMed PMC
Lahnsteiner F, Berger B, Weismann T. Sperm metabolism of the teleost fishes Chalcalburnus chalcoides and Oncorhynchus mykiss and its relation to motility and viability. J exp zool. 1999; 284: 454–465. PubMed
Qiu JH, Li YW, Xie HL, Li Q, Dong HB, Sun MJ, et al. Effects of glucose metabolism pathways on sperm motility and oxidative status during long-term liquid storage of goat semen. Theriogenology. 2016; 86: 839–849. doi: 10.1016/j.theriogenology.2016.03.005 PubMed DOI
Darr CR, Varner DD, Teague S, Cortopassi GA, Datta S, Meyers SA. Lactate and pyruvate are major sources of energy for stallion sperm with dose effects on mitochondrial function, motility, and ROS production. Biol Reprod. 2016; 95(2): 34, 1–11. doi: 10.1095/biolreprod.116.140707 PubMed DOI
Storey BT. Mammalian sperm metabolism: oxygen and sugar, friend and foe. Int J Dev Biol. 2008; 52: 427–437. doi: 10.1387/ijdb.072522bs PubMed DOI
Lahnsteiner F. The role of free amino acids in semen of rainbow trout Oncorhynchus mykiss and carp Cyprinus carpio. J Fish Biol. 2009; 75: 816–833. doi: 10.1111/j.1095-8649.2009.02317.x PubMed DOI
Sangeeta S, Arangasamy A, Kulkarni S, Selvaraju S. Role of amino acids as additives on sperm motility, plasma membrane integrity and lipid peroxidation levels at pre-freeze and post-thawed ram semen. Anim Reprod Sci. 2015; 161: 82–88. doi: 10.1016/j.anireprosci.2015.08.008 PubMed DOI
Barett GC. Chemistry and Biochemistry of the Amino Acids. London: Chapman & Hall; 1985.
Patel AB, Srivastava S, Phadke RS, Govil G. Arginine activates glycolysis of goat epididymal spermatozoa: an NMR study. Biophys J. 1998; 75: 1522–1528. doi: 10.1016/S0006-3495(98)74071-8 PubMed DOI PMC
Randany EW, Atherton RW. Arginine induced stimulation of rabbit sperm motility. Arch Androl. 1981; 7: 351–355. PubMed
Keller DW, Polakoski KL. L-Arginine stimulation of human sperm motility in vitro. Biol Reprod. 1975; 13: 154–157. PubMed
Srivastava S, Agarwal A. Effect of anion channel blockers on L-arginine action in spermatozoa from asthenospermic men. Andrologia. 2009; 42: 76–82. PubMed
O’Flaherty C, Rodriguez P, Srivastava S. L-Arginine promotes capacitation and acrosome reaction in cryopreserved bovine spermatozoa. Biochim Biophys Acta. 2004; 1674: 215–221. doi: 10.1016/j.bbagen.2004.06.020 PubMed DOI
Crowe JH, Crowe LH. Stabilization of membranes anhydrobiotic organism In: Leopold AC, editor. Membranes, Metabolism and Dry Organisms. Ithaca and London: Comstock Publishing Associates; 1986. pp. 188–209.
Scanchez-Partidata LG, Maxwell WMC, Setchell BP. Effect of compatible solutes and diluents composition on the post-thaw motility of ram sperm. Reprod Fertil Dev. 1998; 10: 347–357. PubMed
Sangeeta S, Kulkarni S, Arangasamy A, Selvaraju S. Effect of amino acids on sperm motility, velocity parameters, plasma membrane integrity and lipid peroxidation levels at cooled and post-thawed ram epididymal semen. Indian J Anim Sci. 2015; 85(7): 729–735. PubMed
Smirnoff N, Cumbes QJ. Hydroxyl radical scavenging activity of compatible solutes. Phytochemistry.1989; 28: 1057–1060.
Morita M, Nakajima A, Takemura A, Okuno M. Involvement of redox- and phosphorylation-dependent pathways in osmotic adaptation in sperm cells of euryhaline tilapia. J Exp Biol. 2011; 214: 2096–2104. doi: 10.1242/jeb.053405 PubMed DOI
Peeker R,Abramsson L,Marklund SL. Superoxide dismutase isoenzymes in human seminal plasma and spermatozoa. Mol Hum Reprod. 1997; 3(12): 1061–1066. PubMed
Inazu N, Ruepp B, Wirth H, Wermuth B. Carbonyl reductase from human testis: purification and comparison with carbonyl reductase from human brain and rat testis. Biochim Biophys Acta. 1992; 1116: 50–56. PubMed
Adams SH, Esser V, Brown NF, Ing NH, Larry J, Foster DW, et al. Expression and possible role of muscle-type carnitine palmitoyltransferase I during sperm development in the rat. Biol Reprod. 1998; 59(6): 1399–1405. PubMed
Fujii J, Iuchi Y, Okada F. Fundamental roles of reactive oxygen species and protective mechanisms in the female reproductive system. Reprod Biol Endocrin. 2005; 3(1): 1–10. PubMed PMC
Baarends WM, Roest HP, Grootegoed JA. The ubiquitin system in gametogenesis. Mol Cell Endocrinol. 1999; 151: 5–16. PubMed
Bebington C, Doherty FJ, Fleming SD. The possible biological and reproductive functions of ubiquitin. Hum Reprod Update. 2001; 7: 102–111. PubMed
Sutovsky P. Ubiquitin-dependent proteolysis in mammalian spermatogenesis, fertilization, and sperm quality control: killing three birds with one stone. Microsc Res Tech. 2003; 61: 88–102. doi: 10.1002/jemt.10319 PubMed DOI
Baska KM, Sutovsky P. Protein modification by ubiquitination and is consequences for spermatogenesis, sperm maturation, fertilization and preimplantation embryonic development In: Tokumoto T, editor. New Impact on Protein Modifications in the Regulation of Reproductive System. Kerala: Research Signpost; 2005. pp. 83–114.
Hershko A, Ciechanover A. The ubiquitin system for protein degradation. Annu Rev Biochem. 1992; 61: 761–807. doi: 10.1146/annurev.bi.61.070192.003553 PubMed DOI
Yi YJ, Manandhar G, Sutovsky M, Li R, Jonáková V, Oko R, et al. Ubiquitin C-Terminal Hydrolase-Activity is involved in sperm acrosomal function and anti-polyspermy defense during porcine fertilization. Biol Reprod. 2007; 77: 780–793. doi: 10.1095/biolreprod.107.061275 PubMed DOI
Dietrich MA, Dietrich GJ, Mostek A, Ciereszko A. Motility of carp spermatozoa is associated with profound changes in the sperm proteome. J Proteomics. 2016; 138: 124–135. doi: 10.1016/j.jprot.2016.02.029 PubMed DOI
Eggert-Kruse W, Neuer A, Clussmann C, Boit R, Geissler W, Rohr G, et al. Seminal antibodies to human 60kd heat shock protein (HSP 60) in male partners of subfertile couples. Hum Reprod. 2002; 17(3): 726–735. PubMed
Asquith KL, Baleato RM, McLaughlin EA, Nixon B, Aitken RJ. Tyrosine phosphorylation activates surface chaperones facilitating sperm-zona recognition. J Cell Sci. 2004; 117: 3645–3657. doi: 10.1242/jcs.01214 PubMed DOI
Walsh A, Whelan D, Bielanowicz A, Skinner B, Aitken RJ, O’Bryan MK, et al. Identification of the molecular chaperone, heat shock protein 1 (Chaperonin 10), in the reproductive tract and in capacitating spermatozoa in the male mouse. Biol Reprod. 2008; 78: 983–993. doi: 10.1095/biolreprod.107.066860 PubMed DOI
Sun S, Wong EWP, Li MWM, Lee WM, Cheng CY. 14-3-3 and its binding partners are regulators of protein–protein interactions during spermatogenesis. J Endocrinol. 2009; 202(3): 327–336. doi: 10.1677/JOE-09-0041 PubMed DOI PMC
Arangasamy A, Kasimanickam VR, DeJarnette JM, Kasimanickam RK. Association of CRISP2, CCT8, PEBP1 mRNA abundance in sperm and sire conception rate in Holstein bulls. Theriogenology. 2011; 76: 570–577. doi: 10.1016/j.theriogenology.2011.03.009 PubMed DOI
Tubb B, Mulholland DJ, Vogl W, Lan ZJ, Niederberger C, Cooney A, et al. Testis fascin (FSCN3): a novel paralog of the actin-bundling protein fascin expressed specifically in the elongate spermatid head. Exp Cell Res. 2002; 275(1): 92–109. doi: 10.1006/excr.2002.5486 PubMed DOI