C60 Fullerenes Suppress Reactive Oxygen Species Toxicity Damage in Boar Sperm
Corresponding Author: Yafei Zhang
Nano-Micro Letters,
Vol. 11 (2019), Article Number: 104
Abstract
We report the carboxylated C60 improved the survival and quality of boar sperm during liquid storage at 4 °C and thus propose the use of carboxylated C60 as a novel antioxidant semen extender supplement. Our results demonstrated that the sperm treated with 2 μg mL−1 carboxylated C60 had higher motility than the control group (58.6% and 35.4%, respectively; P ˂ 0.05). Moreover, after incubation with carboxylated C60 for 10 days, acrosome integrity and mitochondrial activity of sperm increased by 18.1% and 34%, respectively, compared with that in the control group. Similarly, the antioxidation abilities and adenosine triphosphate levels in boar sperm treated with carboxylated C60 significantly increased (P ˂ 0.05) compared with those in the control group. The presence of carboxylated C60 in semen extender increases sperm motility probably by suppressing reactive oxygen species (ROS) toxicity damage. Interestingly, carboxylated C60 could protect boar sperm from oxidative stress and energy deficiency by inhibiting the ROS-induced protein dephosphorylation via the cAMP-PKA signaling pathway. In addition, the safety of carboxylated C60 as an alternative antioxidant was also comprehensively evaluated by assessing the mean litter size and number of live offspring in the carboxylated C60 treatment group. Our findings confirm carboxylated C60 as a novel antioxidant agent and suggest its use as a semen extender supplement for assisted reproductive technology in domestic animals.
Highlights:
1 Carboxylated C60 may be considered a novel antioxidant agent to be used as a semen extender supplement for assisted reproductive technology.
2 Carboxylated C60 could enhance the motility parameters and characteristics of boar spermatozoa during liquid storage at 4 °C and protect boar sperm from oxidative stress by inhibiting the reactive-oxygen-species–induced protein dephosphorylation.
3 Novel insights into the molecular mechanisms contributing to the protective effects of carboxylated C60 are provided.
Keywords
Download Citation
Endnote/Zotero/Mendeley (RIS)BibTeX
- D.A. Knight, J.A. Teprovich Jr., A. Summers, B. Peters, P.A. Ward, R.N. Compton, R. Zidan, Synthesis, characterization, and reversible hydrogen sorption study of sodium-doped fullerene. Nanotechnology 24(45), 455601 (2013). https://doi.org/10.1088/0957-4484/24/45/455601
- A.S. Shalabi, A.M. El Mahdy, H.O. Taha, The effect of c-vacancy on hydrogen storage and characterization of H2 modes on Ti functionalized C60 fullerene a first principles study. J. Mol. Model 19(3), 1211–1225 (2013). https://doi.org/10.1007/s00894-012-1615-9
- J.P. Martinez, M. Sola, A. Poater, On the reaction mechanism of the rhodium-catalyzed arylation of fullerene (C60) with organoboron compounds in the presence of water. ChemistryOpen 4(6), 774–778 (2015). https://doi.org/10.1002/open.201500093
- P. Piotrowski, J. Pawłowska, J.G. Sadło, R. Bilewicz, A. Kaim, Tempo functionalized C60 fullerene deposited on gold surface for catalytic oxidation of selected alcohols. J. Nanopart. Res. 19(5), 161 (2017). https://doi.org/10.1007/s11051-017-3857-z
- L. Bai, Y. Chen, Y. Bai, Y. Chen, J. Zhou, A. Huang, Fullerene-doped polyaniline as new redox nanoprobe and catalyst in electrochemical aptasensor for ultrasensitive detection of mycobacterium tuberculosis MP T64 antigen in human serum. Biomaterials 133, 11–19 (2017). https://doi.org/10.1016/j.biomaterials.2017.04.010
- M.B. Ballatore, J. Durantini, N.S. Gsponer, M.B. Suarez, M. Gervaldo, L. Otero, M.B. Spesia, M.E. Milanesio, E.N. Durantini, Photodynamic inactivation of bacteria using novel electrogenerated porphyrin-fullerene C60 polymeric films. Environ. Sci. Technol. 49(12), 7456–7463 (2015). https://doi.org/10.1021/acs.est.5b01407
- J.M. Ren, J. Subbiah, B. Zhang, K. Ishitake, K. Satoh, M. Kamigaito, G.G. Qiao, E.H. Wong, W.W. Wong, Fullerene peapod nanoparticles as an organic semiconductor-electrode interface layer. Chem. Commun. 52(16), 3356–3359 (2016). https://doi.org/10.1039/c5cc10444k
- Q. Tang, P. Bairi, R.G. Shrestha, J.P. Hill, K. Ariga, H. Zeng, Q. Ji, L.K. Shrestha, Quasi 2D mesoporous carbon microbelts derived from fullerene crystals as an electrode material for electrochemical supercapacitors. ACS Appl. Mater. Interfaces 9(51), 44458–44465 (2017). https://doi.org/10.1021/acsami.7b13277
- P.K. Brahman, L. Suresh, V. Lokesh, S. Nizamuddin, Fabrication of highly sensitive and selective nanocomposite film based on cunps/fullerene-C60/mwcnts: an electrochemical nanosensor for trace recognition of paracetamol. Anal. Chim. Acta 917, 107–116 (2016). https://doi.org/10.1016/j.aca.2016.02.044
- R. Gordon, I. Podolski, E. Makarova, A. Deev, E. Mugantseva, S. Khutsyan, F. Sengpiel, A. Murashev, V. Vorobyov, Intrahippocampal pathways involved in learning/memory mechanisms are affected by intracerebral infusions of amyloid-beta25-35 peptide and hydrated fullerene C60 in rats. J. Alzheimer’s Dis. 58(3), 711–724 (2017). https://doi.org/10.3233/jad-161182
- V. Vorobyov, V. Kaptsov, R. Gordon, E. Makarova, I. Podolski, F. Sengpiel, Neuroprotective effects of hydrated fullerene C60: cortical and hippocampal EEG interplay in an amyloid-infused rat model of Alzheimer’s disease. J. Alzheimer’s Dis. 45(1), 217–233 (2015). https://doi.org/10.3233/jad-142469
- A.B. Kraemer, G.M. Parfitt, D.D.S. Acosta, G.E. Bruch, M.F. Cordeiro, L.F. Marins, J. Ventura-Lima, J.M. Monserrat, D.M. Barros, Fullerene (C60) particle size implications in neurotoxicity following infusion into the hippocampi of Wistar rats. Toxicol. Appl. Pharmacol. 338, 197–203 (2018). https://doi.org/10.1016/j.taap.2017.11.022
- V.L. Voeikov, O.I. Yablonskaya, Stabilizing effects of hydrated fullerenes C60 in a wide range of concentrations on luciferase, alkaline phosphatase, and peroxidase in vitro. Electromagn. Biol. Med. 34(2), 160–166 (2015). https://doi.org/10.3109/15368378.2015.1036077
- J.J. Yin, F. Lao, P.P. Fu, W.G. Wamer, Y. Zhao et al., The scavenging of reactive oxygen species and the potential for cell protection by functionalized fullerene materials. Biomaterials 30(4), 611–621 (2009). https://doi.org/10.1016/j.biomaterials.2008.09.061
- R. Bal, G. Turk, M. Tuzcu, O. Yilmaz, I. Ozercan et al., Protective effects of nanostructures of hydrated C60 fullerene on reproductive function in streptozotocin-diabetic male rats. Toxicology 282(3), 69–81 (2011). https://doi.org/10.1016/j.tox.2010.12.003
- G.V. Andrievsky, V.I. Bruskov, A.A. Tykhomyrov, S.V. Gudkov, Peculiarities of the antioxidant and radioprotective effects of hydrated C60 fullerene nanostructures in vitro and in vivo. Free Radic. Biol. Med. 47(6), 786–793 (2009). https://doi.org/10.1016/j.freeradbiomed.2009.06.016
- A.A. Tykhomyrov, V.S. Nedzvetsky, V.K. Klochkov, G.V. Andrievsky, Nanostructures of hydrated C60 fullerene (Carboxylated C60) protect rat brain against alcohol impact and attenuate behavioral impairments of alcoholized animals. Toxicology 246(2–3), 158–165 (2008). https://doi.org/10.1016/j.tox.2008.01.005
- E.O. Etem, R. Bal, A.E. Akagac, T. Kuloglu, M. Tuzcu, G.V. Andrievsky, I. Buran, V.S. Nedzvetsky, G. Baydas, The effects of hydrated C(60) fullerene on gene expression profile of TRPM2 and TRPM7 in hyperhomocysteinemic mice. J. Recept. Signal Transduct. 34(4), 317–324 (2014). https://doi.org/10.3109/10799893.2014.896381
- N. Shershakova, E. Baraboshkina, S. Andreev, D. Purgina, I. Struchkova, O. Kamyshnikov, A. Nikonova, M. Khaitov, Anti-inflammatory effect of fullerene C60 in a mice model of atopic dermatitis. J. Nanobiotechnol. 14(1), 8 (2016). https://doi.org/10.1186/s12951-016-0159-z
- L.A. Johnson, K.F. Weitze, P. Fiser, W.M. Maxwell, Storage of boar semen. Anim. Reprod. Sci. 62(1–3), 143–172 (2000). https://doi.org/10.1016/S0378-4320(00)00157-3
- A.J. Michael, C. Alexopoulos, E.A. Pontiki, D.J. Hadjipavlou-Litina, P. Saratsis, H.N. Ververidis, C.M. Boscos, Quality and reactive oxygen species of extended canine semen after vitamin c supplementation. Theriogenology 70(5), 827–835 (2008). https://doi.org/10.1016/j.theriogenology.2008.05.043
- B. Didion, G. Braun, M. Duggan, Field fertility of frozen boar semen: a retrospective report comprising over 2600 ai services spanning a four year period. Anim. Reprod. Sci. 137(3–4), 189–196 (2013). https://doi.org/10.1016/j.anireprosci.2013.01.001
- I.G. White, Lipids and calcium uptake of sperm in relation to cold shock and preservation: a review. Reprod. Fertil. Dev. 5(6), 639–658 (1993). https://doi.org/10.1071/RD9930639
- B. Gadani, D. Bucci, M. Spinaci, C. Tamanini, G. Galeati, Resveratrol and Epigallocatechin-3-gallate addition to thawed boar sperm improves in vitro fertilization. Theriogenology 90, 88–93 (2017). https://doi.org/10.1016/j.theriogenology/2016.11.020
- K.T. Zhu, T. Umehara, S.A.M. Hoque, W. Zeng, M. Shimada, Negative effects of ROS generated during linear sperm motility on gene expression and ATP generation in boar sperm mitochondria. Free Radic. Biol. Med. 141, 159–171 (2019). https://doi.org/10.1016/j.freeradbiomed.2019.06.018
- X.G. Zhang, H. Li, L. Wang, Y.Y. Hao, G.D. Liang, Y.H. Ma, G.S. Yang, J.H. Hu, The effects of different levels of superoxide dismutase in Modena on boar semen quality during liquid preservation at 17 °C. Anim. Sci. J. 88(1), 55–62 (2017). https://doi.org/10.1111/asj.12574
- J. Fu, Q. Yang, Y. Li, P. Li, L. Wang, X. Li, A mechanism by which Astragalus polysaccharide protects against ROS toxicity through inhibiting the protein dephosphorylation of boar sperm preserved at 4 °C. J. Cell. Physiol. 233(7), 5267–5280 (2018). https://doi.org/10.1002/jcp.26321
- M. Shafiei, M. Forouzanfar, S.M. Hosseini, M.H.N. Esfahani, The effect of superoxide dismutase mimetic and catalase on the quality of postthawed goat semen. Theriogenology 83(8), 1321–1327 (2015). https://doi.org/10.1016/j.theriogenology.2015.01.018
- E. Tvrda, E. Tušimová, A. Kováčik, D. Paál, H. Greifova, A. Abdramanov, N. Lukáč, Curcumin has protective and antioxidant properties on bull spermatozoa subjected to induced oxidative stress. Anim. Reprod. Sci. 172, 10–20 (2016). https://doi.org/10.1016/j.anireprosci.2016.06.008
- F.A. Navarrete, F.A. García-Vázquez, A. Alvau, J. Escoffier, D. Krapf, C. Sánchez-Cárdenas, A.M. Salicioni, A. Darszon, P.E. Visconti, Biphasic role of calcium in mouse sperm capacitation signaling pathways. J. Cell. Physiol. 230(8), 1758–1769 (2015). https://doi.org/10.1002/jcp.24873
- A. Santiani, A. Ugarelli, S. Evangelista-Vargas, Characterization of functional variables in epididymal alpaca (vicugna pacos) sperm using imaging flow cytometry. Anim. Reprod. Sci. 173, 49–55 (2016). https://doi.org/10.1016/j.anireprosci.2016.08.010
- D. Shu, Y. Qing, Q. Tong, Y. He, Z. Xing et al., Deltonin isolated from dioscorea zingiberensis inhibits cancer cell growth through inducing mitochondrial apoptosis and suppressing akt and mitogen activated protein kinase signals. Biol. Pharm. Bull. 34(8), 1231–1239 (2011). https://doi.org/10.1248/bpb.34.1231
- W. Li, S. Nie, Y. Chen, Y. Wang, C. Li, M. Xie, Enhancement of cyclophosphamide-induced antitumor effect by a novel polysaccharide from ganoderma atrum in sarcoma 180-bearing mice. J. Agric. Food Chem. 59(8), 3707–3716 (2011). https://doi.org/10.1021/jf1049497
- Z. Zhu, X. Fan, Y. Pan, Y. Lu, W. Zeng, Trehalose improves rabbit sperm quality during cryopreservation. Cryobiology 75, 45–51 (2017). https://doi.org/10.1016/j.cryobiol.2017.02.006
- S.S. Du Plessis, A. Agarwal, J. Halabi, E. Tvrda, Contemporary evidence on the physiological role of reactive oxygen species in human sperm function. J. Assist. Reprod. Genet. 32(4), 509–520 (2015). https://doi.org/10.1007/s10815-014-0425-7
- P. Gogol, B. Szczęśniak-Fabiańczyk, A. Wierzchoś-Hilczer, The photon emission, atp level and motility of boar spermatozoa during liquid storage. Reprod. Biol. 9(1), 39–49 (2009). https://doi.org/10.1016/S1642-431X(12)60093-X
- S.-H. Lee, C.-K. Park, Antioxidative effects of magnetized extender containing bovine serum albumin on sperm oxidative stress during long-term liquid preservation of boar semen. Biochem. Biophys. Res. Commun. 464(2), 467–472 (2015). https://doi.org/10.1016/j.bbrc.2015.06.159
- B.J. Awda, M. Mackenzie-Bell, M.M. Buhr, Reactive oxygen species and boar sperm function. Biol. Reprod. 81(3), 553–561 (2009). https://doi.org/10.1095/biolreprod.109.076471
- I. Barranco, A. Tvarijonaviciute, C. Perez-Patiño, I. Parrilla, J.J. Ceron, E.A. Martinez, H. Rodriguez-Martinez, J. Roca, High total antioxidant capacity of the porcine seminal plasma (SP-TAC) relates to sperm survival and fertility. Sci. Rep. 5, 18538 (2015). https://doi.org/10.1038/srep18538
- D. González-Abreu, S. García-Martínez, V. Fernández-Espín, R. Romar, J. Gadea, Incubation of boar spermatozoa in viscous media by addition of methylcellulose improves sperm quality and penetration rates during in vitro fertilization. Theriogenology 92, 14–23 (2017). https://doi.org/10.1016/j.theriogenology.2017.01.016
- S. Ye, M. Chen, Y. Jiang, M. Chen, T. Zhou et al., Polyhydroxylated fullerene attenuates oxidative stress-induced apoptosis via a fortifying Nrf2-regulated cellular antioxidant defence system. Int. J. Nanomed. 29(9), 2073–2087 (2014). https://doi.org/10.2147/IJN.S56973.eCollection2014
- M.E. Bozdaganyan, P.S. Orekhov, A.K. Shaytan, K.V. Shaitan, Comparative computational study of interaction of C60-fullerene and tris-malonyl-C60-fullerene isomers with lipid bilayer: relation to their antioxidant effect. PLoS ONE 9(7), e102487 (2014). https://doi.org/10.1371/journal.pone.0102487
- K. Russ, P. Elvati, T. Parsonage, A. Dews, J. Jarvis et al., C60 fullerene localization and membrane interactions in raw 264.7 immortalized mouse macrophages. Nanoscale 8(7), 4134–4144 (2016). https://doi.org/10.1039/c5nr07003a
- I.Y. Podolski, Z. Podlubnaya, E. Kosenko, E. Mugantseva, E. Makarova et al., Effects of hydrated forms of C60 fullerene on amyloid β-peptide fibrillization in vitro and performance of the cognitive task. J. Nanosci. Nanotechnol. 7(4–5), 1479–1485 (2007). https://doi.org/10.1166/jnn.2007.330
- S.C. Sumner, R.W. Snyder, C. Wingard, N.P. Mortensen, N.A. Holland et al., Distribution and biomarkers of carbon-14-labeled fullerene C60 ([14C(U)] C60) in female rats and mice for up to 30 days after intravenous exposure. J. Appl. Toxicol. 35(12), 1452–1464 (2015). https://doi.org/10.1002/jat.3110
- S. Ye, T. Zhou, K. Cheng, M. Chen, Y. Wang, Y. Jiang, P. Yang, Carboxylic acid fullerene (C60) derivatives attenuated neuroinflammatory responses by modulating mitochondrial dynamics. Nanoscale Res. Lett. 10(1), 953 (2015). https://doi.org/10.1186/s11671-015-0953-9
- S.V. Prylutska, L.M. Skivka, G.V. Didenko, Y.I. Prylutskyy, M.P. Evstigneev et al., Complex of C60 fullerene with doxorubicin as a promising agent in antitumor therapy. Nanoscale Res. Lett. 10(1), 499 (2015). https://doi.org/10.1186/s11671-015-1206-7
- B. Srdjenovic, V. Milic-Torres, N. Grujic, K. Stankov, A. Djordjevic, V. Vasovic, Antioxidant properties of fullerenol C60 (OH) 24 in rat kidneys, testes, and lungs treated with doxorubicin. Toxicol. Mech. Methods 20(6), 298–305 (2010). https://doi.org/10.3109/15376516.2010.485622
- M.A. Murugan, B. Gangadharan, P. Mathur, Antioxidative effect of fullerenol on goat epididymal spermatozoa. Asian J. Androl. 4(2), 149–152 (2002)
- L. Zhen, L. Wang, J. Fu, Y. Li, N. Zhao, X. Li, Hexavalent chromium affects sperm motility by influencing protein tyrosine phosphorylation in the midpiece of boar spermatozoa. Reprod. Toxicol. 59, 66–79 (2016). https://doi.org/10.1016/j.reprotox.2015.11.001
- J.M. Nascimento, L.Z. Shi, J. Tam, C. Chandsawangbhuwana, B. Durrant, E.L. Botvinick, M.W. Berns, Comparison of glycolysis and oxidative phosphorylation as energy sources for mammalian sperm motility, using the combination of fluorescence imaging, laser tweezers, and real-time automated tracking and trapping. J. Cell. Physiol. 217(3), 745–751 (2008). https://doi.org/10.1002/jcp.21549
- M.A. Baker, Proteomics of post-translational modifications of mammalian spermatozoa. Cell Tissue Res. 363(1), 279–287 (2016). https://doi.org/10.1007/s00441-015-2249-x
- MathSciNet
- R.D. Brohi, L.J. Huo, Posttranslational modifications in spermatozoa and effects on male fertility and sperm viability. OMICS 21(5), 245–256 (2017). https://doi.org/10.1089/omi.2016.0173
- P. Li, Q. Yang, S. Li, H. Sun, H. Liu, B. Li, Q. Cui, X. Li, Candidates for reproductive biomarkers: protein phosphorylation and acetylation positively related to selected parameters of boar spermatozoa quality. Anim. Reprod. Sci. 197, 67–80 (2018). https://doi.org/10.1016/j.anireprosci.2018.08.010
- R.J. Aitken, M.A. Baker, The role of proteomics in understanding sperm cell biology. Int. J. Androl. 31(3), 295–302 (2008). https://doi.org/10.1111/j.1365-2605.2007.00851.x
- P. Leclerc, E. De Lamirande, C. Gagnon, Cyclic adenosine 3′, 5′ monophosphate-dependent regulation of protein tyrosine phosphorylation in relation to human sperm capacitation and motility. Biol. Reprod. 55(3), 684–692 (1996). https://doi.org/10.1095/biolreprod55.3.684
- R. Aitken, D. Harkiss, W. Knox, M. Paterson, D. Irvine, A novel signal transduction cascade in capacitating human spermatozoa characterised by a redox-regulated, camp-mediated induction of tyrosine phosphorylation. J. Cell Sci. 111(5), 645–656 (1998)
- F. Dimitriadis, D. Giannakis, N. Pardalidis, K. Zikopoulos, E. Paraskevaidis et al., Effects of phosphodiesterase 5 inhibitors on sperm parameters and fertilizing capacity. Asian J. Androl. 10(1), 115–133 (2008). https://doi.org/10.1111/j.1745-7262.2008.00373.x
- M. Avdeev, A. Khokhryakov, T. Tropin, G. Andrievsky, V. Klochkov et al., Structural features of molecular-colloidal solutions of C60 fullerenes in water by small-angle neutron scattering. Langmuir 20(11), 4363–4368 (2004). https://doi.org/10.1021/la0361969
- Q. Liu, Q. Cui, X.J. Li, L. Jin, The applications of buckminsterfullerene C60 and derivatives in orthopaedic research. Connect. Tissue Res. 55(2), 71–79 (2014). https://doi.org/10.3109/03008207.2013.877894
- K.L. Quick, S.S. Ali, R. Arch, C. Xiong, D. Wozniak, L.L. Dugan, A carboxyfullerene SOD mimetic improves cognition and extends the lifespan of mice. Neurobiol. Aging 29(1), 117–128 (2008). https://doi.org/10.1016/j.neurobiolaging.2006.09.014
References
D.A. Knight, J.A. Teprovich Jr., A. Summers, B. Peters, P.A. Ward, R.N. Compton, R. Zidan, Synthesis, characterization, and reversible hydrogen sorption study of sodium-doped fullerene. Nanotechnology 24(45), 455601 (2013). https://doi.org/10.1088/0957-4484/24/45/455601
A.S. Shalabi, A.M. El Mahdy, H.O. Taha, The effect of c-vacancy on hydrogen storage and characterization of H2 modes on Ti functionalized C60 fullerene a first principles study. J. Mol. Model 19(3), 1211–1225 (2013). https://doi.org/10.1007/s00894-012-1615-9
J.P. Martinez, M. Sola, A. Poater, On the reaction mechanism of the rhodium-catalyzed arylation of fullerene (C60) with organoboron compounds in the presence of water. ChemistryOpen 4(6), 774–778 (2015). https://doi.org/10.1002/open.201500093
P. Piotrowski, J. Pawłowska, J.G. Sadło, R. Bilewicz, A. Kaim, Tempo functionalized C60 fullerene deposited on gold surface for catalytic oxidation of selected alcohols. J. Nanopart. Res. 19(5), 161 (2017). https://doi.org/10.1007/s11051-017-3857-z
L. Bai, Y. Chen, Y. Bai, Y. Chen, J. Zhou, A. Huang, Fullerene-doped polyaniline as new redox nanoprobe and catalyst in electrochemical aptasensor for ultrasensitive detection of mycobacterium tuberculosis MP T64 antigen in human serum. Biomaterials 133, 11–19 (2017). https://doi.org/10.1016/j.biomaterials.2017.04.010
M.B. Ballatore, J. Durantini, N.S. Gsponer, M.B. Suarez, M. Gervaldo, L. Otero, M.B. Spesia, M.E. Milanesio, E.N. Durantini, Photodynamic inactivation of bacteria using novel electrogenerated porphyrin-fullerene C60 polymeric films. Environ. Sci. Technol. 49(12), 7456–7463 (2015). https://doi.org/10.1021/acs.est.5b01407
J.M. Ren, J. Subbiah, B. Zhang, K. Ishitake, K. Satoh, M. Kamigaito, G.G. Qiao, E.H. Wong, W.W. Wong, Fullerene peapod nanoparticles as an organic semiconductor-electrode interface layer. Chem. Commun. 52(16), 3356–3359 (2016). https://doi.org/10.1039/c5cc10444k
Q. Tang, P. Bairi, R.G. Shrestha, J.P. Hill, K. Ariga, H. Zeng, Q. Ji, L.K. Shrestha, Quasi 2D mesoporous carbon microbelts derived from fullerene crystals as an electrode material for electrochemical supercapacitors. ACS Appl. Mater. Interfaces 9(51), 44458–44465 (2017). https://doi.org/10.1021/acsami.7b13277
P.K. Brahman, L. Suresh, V. Lokesh, S. Nizamuddin, Fabrication of highly sensitive and selective nanocomposite film based on cunps/fullerene-C60/mwcnts: an electrochemical nanosensor for trace recognition of paracetamol. Anal. Chim. Acta 917, 107–116 (2016). https://doi.org/10.1016/j.aca.2016.02.044
R. Gordon, I. Podolski, E. Makarova, A. Deev, E. Mugantseva, S. Khutsyan, F. Sengpiel, A. Murashev, V. Vorobyov, Intrahippocampal pathways involved in learning/memory mechanisms are affected by intracerebral infusions of amyloid-beta25-35 peptide and hydrated fullerene C60 in rats. J. Alzheimer’s Dis. 58(3), 711–724 (2017). https://doi.org/10.3233/jad-161182
V. Vorobyov, V. Kaptsov, R. Gordon, E. Makarova, I. Podolski, F. Sengpiel, Neuroprotective effects of hydrated fullerene C60: cortical and hippocampal EEG interplay in an amyloid-infused rat model of Alzheimer’s disease. J. Alzheimer’s Dis. 45(1), 217–233 (2015). https://doi.org/10.3233/jad-142469
A.B. Kraemer, G.M. Parfitt, D.D.S. Acosta, G.E. Bruch, M.F. Cordeiro, L.F. Marins, J. Ventura-Lima, J.M. Monserrat, D.M. Barros, Fullerene (C60) particle size implications in neurotoxicity following infusion into the hippocampi of Wistar rats. Toxicol. Appl. Pharmacol. 338, 197–203 (2018). https://doi.org/10.1016/j.taap.2017.11.022
V.L. Voeikov, O.I. Yablonskaya, Stabilizing effects of hydrated fullerenes C60 in a wide range of concentrations on luciferase, alkaline phosphatase, and peroxidase in vitro. Electromagn. Biol. Med. 34(2), 160–166 (2015). https://doi.org/10.3109/15368378.2015.1036077
J.J. Yin, F. Lao, P.P. Fu, W.G. Wamer, Y. Zhao et al., The scavenging of reactive oxygen species and the potential for cell protection by functionalized fullerene materials. Biomaterials 30(4), 611–621 (2009). https://doi.org/10.1016/j.biomaterials.2008.09.061
R. Bal, G. Turk, M. Tuzcu, O. Yilmaz, I. Ozercan et al., Protective effects of nanostructures of hydrated C60 fullerene on reproductive function in streptozotocin-diabetic male rats. Toxicology 282(3), 69–81 (2011). https://doi.org/10.1016/j.tox.2010.12.003
G.V. Andrievsky, V.I. Bruskov, A.A. Tykhomyrov, S.V. Gudkov, Peculiarities of the antioxidant and radioprotective effects of hydrated C60 fullerene nanostructures in vitro and in vivo. Free Radic. Biol. Med. 47(6), 786–793 (2009). https://doi.org/10.1016/j.freeradbiomed.2009.06.016
A.A. Tykhomyrov, V.S. Nedzvetsky, V.K. Klochkov, G.V. Andrievsky, Nanostructures of hydrated C60 fullerene (Carboxylated C60) protect rat brain against alcohol impact and attenuate behavioral impairments of alcoholized animals. Toxicology 246(2–3), 158–165 (2008). https://doi.org/10.1016/j.tox.2008.01.005
E.O. Etem, R. Bal, A.E. Akagac, T. Kuloglu, M. Tuzcu, G.V. Andrievsky, I. Buran, V.S. Nedzvetsky, G. Baydas, The effects of hydrated C(60) fullerene on gene expression profile of TRPM2 and TRPM7 in hyperhomocysteinemic mice. J. Recept. Signal Transduct. 34(4), 317–324 (2014). https://doi.org/10.3109/10799893.2014.896381
N. Shershakova, E. Baraboshkina, S. Andreev, D. Purgina, I. Struchkova, O. Kamyshnikov, A. Nikonova, M. Khaitov, Anti-inflammatory effect of fullerene C60 in a mice model of atopic dermatitis. J. Nanobiotechnol. 14(1), 8 (2016). https://doi.org/10.1186/s12951-016-0159-z
L.A. Johnson, K.F. Weitze, P. Fiser, W.M. Maxwell, Storage of boar semen. Anim. Reprod. Sci. 62(1–3), 143–172 (2000). https://doi.org/10.1016/S0378-4320(00)00157-3
A.J. Michael, C. Alexopoulos, E.A. Pontiki, D.J. Hadjipavlou-Litina, P. Saratsis, H.N. Ververidis, C.M. Boscos, Quality and reactive oxygen species of extended canine semen after vitamin c supplementation. Theriogenology 70(5), 827–835 (2008). https://doi.org/10.1016/j.theriogenology.2008.05.043
B. Didion, G. Braun, M. Duggan, Field fertility of frozen boar semen: a retrospective report comprising over 2600 ai services spanning a four year period. Anim. Reprod. Sci. 137(3–4), 189–196 (2013). https://doi.org/10.1016/j.anireprosci.2013.01.001
I.G. White, Lipids and calcium uptake of sperm in relation to cold shock and preservation: a review. Reprod. Fertil. Dev. 5(6), 639–658 (1993). https://doi.org/10.1071/RD9930639
B. Gadani, D. Bucci, M. Spinaci, C. Tamanini, G. Galeati, Resveratrol and Epigallocatechin-3-gallate addition to thawed boar sperm improves in vitro fertilization. Theriogenology 90, 88–93 (2017). https://doi.org/10.1016/j.theriogenology/2016.11.020
K.T. Zhu, T. Umehara, S.A.M. Hoque, W. Zeng, M. Shimada, Negative effects of ROS generated during linear sperm motility on gene expression and ATP generation in boar sperm mitochondria. Free Radic. Biol. Med. 141, 159–171 (2019). https://doi.org/10.1016/j.freeradbiomed.2019.06.018
X.G. Zhang, H. Li, L. Wang, Y.Y. Hao, G.D. Liang, Y.H. Ma, G.S. Yang, J.H. Hu, The effects of different levels of superoxide dismutase in Modena on boar semen quality during liquid preservation at 17 °C. Anim. Sci. J. 88(1), 55–62 (2017). https://doi.org/10.1111/asj.12574
J. Fu, Q. Yang, Y. Li, P. Li, L. Wang, X. Li, A mechanism by which Astragalus polysaccharide protects against ROS toxicity through inhibiting the protein dephosphorylation of boar sperm preserved at 4 °C. J. Cell. Physiol. 233(7), 5267–5280 (2018). https://doi.org/10.1002/jcp.26321
M. Shafiei, M. Forouzanfar, S.M. Hosseini, M.H.N. Esfahani, The effect of superoxide dismutase mimetic and catalase on the quality of postthawed goat semen. Theriogenology 83(8), 1321–1327 (2015). https://doi.org/10.1016/j.theriogenology.2015.01.018
E. Tvrda, E. Tušimová, A. Kováčik, D. Paál, H. Greifova, A. Abdramanov, N. Lukáč, Curcumin has protective and antioxidant properties on bull spermatozoa subjected to induced oxidative stress. Anim. Reprod. Sci. 172, 10–20 (2016). https://doi.org/10.1016/j.anireprosci.2016.06.008
F.A. Navarrete, F.A. García-Vázquez, A. Alvau, J. Escoffier, D. Krapf, C. Sánchez-Cárdenas, A.M. Salicioni, A. Darszon, P.E. Visconti, Biphasic role of calcium in mouse sperm capacitation signaling pathways. J. Cell. Physiol. 230(8), 1758–1769 (2015). https://doi.org/10.1002/jcp.24873
A. Santiani, A. Ugarelli, S. Evangelista-Vargas, Characterization of functional variables in epididymal alpaca (vicugna pacos) sperm using imaging flow cytometry. Anim. Reprod. Sci. 173, 49–55 (2016). https://doi.org/10.1016/j.anireprosci.2016.08.010
D. Shu, Y. Qing, Q. Tong, Y. He, Z. Xing et al., Deltonin isolated from dioscorea zingiberensis inhibits cancer cell growth through inducing mitochondrial apoptosis and suppressing akt and mitogen activated protein kinase signals. Biol. Pharm. Bull. 34(8), 1231–1239 (2011). https://doi.org/10.1248/bpb.34.1231
W. Li, S. Nie, Y. Chen, Y. Wang, C. Li, M. Xie, Enhancement of cyclophosphamide-induced antitumor effect by a novel polysaccharide from ganoderma atrum in sarcoma 180-bearing mice. J. Agric. Food Chem. 59(8), 3707–3716 (2011). https://doi.org/10.1021/jf1049497
Z. Zhu, X. Fan, Y. Pan, Y. Lu, W. Zeng, Trehalose improves rabbit sperm quality during cryopreservation. Cryobiology 75, 45–51 (2017). https://doi.org/10.1016/j.cryobiol.2017.02.006
S.S. Du Plessis, A. Agarwal, J. Halabi, E. Tvrda, Contemporary evidence on the physiological role of reactive oxygen species in human sperm function. J. Assist. Reprod. Genet. 32(4), 509–520 (2015). https://doi.org/10.1007/s10815-014-0425-7
P. Gogol, B. Szczęśniak-Fabiańczyk, A. Wierzchoś-Hilczer, The photon emission, atp level and motility of boar spermatozoa during liquid storage. Reprod. Biol. 9(1), 39–49 (2009). https://doi.org/10.1016/S1642-431X(12)60093-X
S.-H. Lee, C.-K. Park, Antioxidative effects of magnetized extender containing bovine serum albumin on sperm oxidative stress during long-term liquid preservation of boar semen. Biochem. Biophys. Res. Commun. 464(2), 467–472 (2015). https://doi.org/10.1016/j.bbrc.2015.06.159
B.J. Awda, M. Mackenzie-Bell, M.M. Buhr, Reactive oxygen species and boar sperm function. Biol. Reprod. 81(3), 553–561 (2009). https://doi.org/10.1095/biolreprod.109.076471
I. Barranco, A. Tvarijonaviciute, C. Perez-Patiño, I. Parrilla, J.J. Ceron, E.A. Martinez, H. Rodriguez-Martinez, J. Roca, High total antioxidant capacity of the porcine seminal plasma (SP-TAC) relates to sperm survival and fertility. Sci. Rep. 5, 18538 (2015). https://doi.org/10.1038/srep18538
D. González-Abreu, S. García-Martínez, V. Fernández-Espín, R. Romar, J. Gadea, Incubation of boar spermatozoa in viscous media by addition of methylcellulose improves sperm quality and penetration rates during in vitro fertilization. Theriogenology 92, 14–23 (2017). https://doi.org/10.1016/j.theriogenology.2017.01.016
S. Ye, M. Chen, Y. Jiang, M. Chen, T. Zhou et al., Polyhydroxylated fullerene attenuates oxidative stress-induced apoptosis via a fortifying Nrf2-regulated cellular antioxidant defence system. Int. J. Nanomed. 29(9), 2073–2087 (2014). https://doi.org/10.2147/IJN.S56973.eCollection2014
M.E. Bozdaganyan, P.S. Orekhov, A.K. Shaytan, K.V. Shaitan, Comparative computational study of interaction of C60-fullerene and tris-malonyl-C60-fullerene isomers with lipid bilayer: relation to their antioxidant effect. PLoS ONE 9(7), e102487 (2014). https://doi.org/10.1371/journal.pone.0102487
K. Russ, P. Elvati, T. Parsonage, A. Dews, J. Jarvis et al., C60 fullerene localization and membrane interactions in raw 264.7 immortalized mouse macrophages. Nanoscale 8(7), 4134–4144 (2016). https://doi.org/10.1039/c5nr07003a
I.Y. Podolski, Z. Podlubnaya, E. Kosenko, E. Mugantseva, E. Makarova et al., Effects of hydrated forms of C60 fullerene on amyloid β-peptide fibrillization in vitro and performance of the cognitive task. J. Nanosci. Nanotechnol. 7(4–5), 1479–1485 (2007). https://doi.org/10.1166/jnn.2007.330
S.C. Sumner, R.W. Snyder, C. Wingard, N.P. Mortensen, N.A. Holland et al., Distribution and biomarkers of carbon-14-labeled fullerene C60 ([14C(U)] C60) in female rats and mice for up to 30 days after intravenous exposure. J. Appl. Toxicol. 35(12), 1452–1464 (2015). https://doi.org/10.1002/jat.3110
S. Ye, T. Zhou, K. Cheng, M. Chen, Y. Wang, Y. Jiang, P. Yang, Carboxylic acid fullerene (C60) derivatives attenuated neuroinflammatory responses by modulating mitochondrial dynamics. Nanoscale Res. Lett. 10(1), 953 (2015). https://doi.org/10.1186/s11671-015-0953-9
S.V. Prylutska, L.M. Skivka, G.V. Didenko, Y.I. Prylutskyy, M.P. Evstigneev et al., Complex of C60 fullerene with doxorubicin as a promising agent in antitumor therapy. Nanoscale Res. Lett. 10(1), 499 (2015). https://doi.org/10.1186/s11671-015-1206-7
B. Srdjenovic, V. Milic-Torres, N. Grujic, K. Stankov, A. Djordjevic, V. Vasovic, Antioxidant properties of fullerenol C60 (OH) 24 in rat kidneys, testes, and lungs treated with doxorubicin. Toxicol. Mech. Methods 20(6), 298–305 (2010). https://doi.org/10.3109/15376516.2010.485622
M.A. Murugan, B. Gangadharan, P. Mathur, Antioxidative effect of fullerenol on goat epididymal spermatozoa. Asian J. Androl. 4(2), 149–152 (2002)
L. Zhen, L. Wang, J. Fu, Y. Li, N. Zhao, X. Li, Hexavalent chromium affects sperm motility by influencing protein tyrosine phosphorylation in the midpiece of boar spermatozoa. Reprod. Toxicol. 59, 66–79 (2016). https://doi.org/10.1016/j.reprotox.2015.11.001
J.M. Nascimento, L.Z. Shi, J. Tam, C. Chandsawangbhuwana, B. Durrant, E.L. Botvinick, M.W. Berns, Comparison of glycolysis and oxidative phosphorylation as energy sources for mammalian sperm motility, using the combination of fluorescence imaging, laser tweezers, and real-time automated tracking and trapping. J. Cell. Physiol. 217(3), 745–751 (2008). https://doi.org/10.1002/jcp.21549
M.A. Baker, Proteomics of post-translational modifications of mammalian spermatozoa. Cell Tissue Res. 363(1), 279–287 (2016). https://doi.org/10.1007/s00441-015-2249-x
MathSciNet
R.D. Brohi, L.J. Huo, Posttranslational modifications in spermatozoa and effects on male fertility and sperm viability. OMICS 21(5), 245–256 (2017). https://doi.org/10.1089/omi.2016.0173
P. Li, Q. Yang, S. Li, H. Sun, H. Liu, B. Li, Q. Cui, X. Li, Candidates for reproductive biomarkers: protein phosphorylation and acetylation positively related to selected parameters of boar spermatozoa quality. Anim. Reprod. Sci. 197, 67–80 (2018). https://doi.org/10.1016/j.anireprosci.2018.08.010
R.J. Aitken, M.A. Baker, The role of proteomics in understanding sperm cell biology. Int. J. Androl. 31(3), 295–302 (2008). https://doi.org/10.1111/j.1365-2605.2007.00851.x
P. Leclerc, E. De Lamirande, C. Gagnon, Cyclic adenosine 3′, 5′ monophosphate-dependent regulation of protein tyrosine phosphorylation in relation to human sperm capacitation and motility. Biol. Reprod. 55(3), 684–692 (1996). https://doi.org/10.1095/biolreprod55.3.684
R. Aitken, D. Harkiss, W. Knox, M. Paterson, D. Irvine, A novel signal transduction cascade in capacitating human spermatozoa characterised by a redox-regulated, camp-mediated induction of tyrosine phosphorylation. J. Cell Sci. 111(5), 645–656 (1998)
F. Dimitriadis, D. Giannakis, N. Pardalidis, K. Zikopoulos, E. Paraskevaidis et al., Effects of phosphodiesterase 5 inhibitors on sperm parameters and fertilizing capacity. Asian J. Androl. 10(1), 115–133 (2008). https://doi.org/10.1111/j.1745-7262.2008.00373.x
M. Avdeev, A. Khokhryakov, T. Tropin, G. Andrievsky, V. Klochkov et al., Structural features of molecular-colloidal solutions of C60 fullerenes in water by small-angle neutron scattering. Langmuir 20(11), 4363–4368 (2004). https://doi.org/10.1021/la0361969
Q. Liu, Q. Cui, X.J. Li, L. Jin, The applications of buckminsterfullerene C60 and derivatives in orthopaedic research. Connect. Tissue Res. 55(2), 71–79 (2014). https://doi.org/10.3109/03008207.2013.877894
K.L. Quick, S.S. Ali, R. Arch, C. Xiong, D. Wozniak, L.L. Dugan, A carboxyfullerene SOD mimetic improves cognition and extends the lifespan of mice. Neurobiol. Aging 29(1), 117–128 (2008). https://doi.org/10.1016/j.neurobiolaging.2006.09.014