Key of mechanisms of action antioxidants used in cryopreservation sperm stallions
DOI:
https://doi.org/10.35172/rvz.2017.v24.277Keywords:
free radicals, antioxidants, semen, equineAbstract
The use of sperm cryopreservation in equine reproduction represented a major breakthrough
for the development of the species. However the use of biotechnologies such as refrigeration
and freezing sperm prints on the physical and chemical damage cells that result in increased
levels of reactive oxygen species (ROS), oxidative stress and irreversible injury to sperm.
Aiming to mitigate the consequences of oxidative stress, different substances with antioxidant
properties are added to extenders for cryopreservation, despite this, most of the time the
mechanism of action triggered by these antioxidants is not well understood. In view of this,
the aim with this study reference the main antioxidants used in cryopreservation stallions and
their mechanisms of action.
References
1. Nouri H, Towhidi A, Zhandi M, Sadeghi R. The effects of centrifuged egg yolk used with
INRA plus soybean lecithin extender on semen quality to freeze miniature caspian horse
semen. J Equine Vet Sci. 2013;33:1050-3.
2. Morillo-Rodríguez A, Macías-García B, Tapia JA, Ortega-Ferrusola C, Peña FJ.
Consequences of butylated hydroxytoluene in the freezing extender on post-thaw
characteristics of stallion spermatozoa in vitro. Andrologia. 2012;44:688-95.
3. Ortega-Ferrusola C, Gonzalez FL, Morrell JM, Salazar SC, Macías-García B, RodriguezMartinez H, et al. Lipid peroxidation, assessed with BODIPY-C11, increases after
cryopreservation of stallion spermatozoa, is stallion-dependent and is related to apoptoticlike changes. Reproduction. 2009;138:55-63.
4. García BM, Fernández LG, Ferrusola CO, Rodríguez AM, Bolaños JMG, Martinez HR, et
al. Fatty acids and plasmalogens of the phospholipids of the sperm membranes and their
relation with the post-thaw quality of stallion spermatozoa. Theriogenology. 2011;75:811-
18.
5. Aitken RJ, Harkiss D, Knox W, Paterson M, Irvine DS. A novel signal transduction
cascade in capacitating human spermatozoa characterised by a redox-regulated, cAMPmediated induction of tyrosine phosphorylation. J Cell Sci. 1998;111:645-56.
6. Lenzi A, Gandini L, Lombardo F, Picardo M, Maresca V, Panfili E, et al. Polyunsaturated
fatty acids of germ cell membranes, glutathione and blutathione-dependent enzymePHGPx: from basic to clinic. Contraception. 2002;65:301-4.
7. Ford WCL. Regulation of sperm function by reactive oxygen species. Hum Reprod
Update. 2004;10:387-99.
8. Kothari S, Thompson A, Agarwal A, Du Plessis SS. Free radicals: their beneficial and
detrimental effects on sperm function. Indian J Exp Biol. 2010;48:425-35.
9. Cocchia N, Pasolini MP, Mancini R, Petrazzuolo O, Cristofaro I, Rosapane I, et al. Effect
of sod (superoxide dismutase) protein supplementation in semen extenders on motility,
viability, acrosome status and ERK (extracellular signal-regulated kinase) protein
phosphorylation of chilled stallion spermatozoa. Theriogenology. 2011;75:1201-10.
10. Oliveira RA, Wolf CA, Oliveira MA, Gambarini ML. Addition of glutathione to na
extender for frozen equine sêmen. J Equine Vet Sci. 2013;33:1148-52.
11. Aurich JE, Schönherr U, Hoppe H, Aurich C. Effects of antioxidants on motility and
membrane integrity of chilled-stored stallion semen. Theriogenology. 1997;48:185-92.
12. Ball BA, Medina V, Gravance CG, Baumber J. Effect of antioxidants on preservation of
motility,viability and acrosomal integrity of equine spermatozoa during storage at 5°C.
Theriogenology. 2001;56:577-89.
13. Almeida J, Ball BA. Effect of α-tocopherol and tocopherol succinate on lipid
peroxidation in equine spermatozoa. Anim Reprod Sci. 2005;87:321-37.
14. Franco JSV, Chaveiro A, Góis A, Silva FMS. Effects of α-tocopherol and ascorbic acid
on equine semen quality after cryopreservation. J Equine Vet Sci. 2013;33:787-93.
15. Yousefian I, Zare-Shahneh A, Zhandi M. The effect of coenzyme q10 and α-tocopherol
in skim milk–based extender for preservation of caspian stallion semen in cool condition.
J Equine Vet Sci. 2014;34:949-54.
16. McNiven MA, Richardson GF. Chilled storage of stallion semen using
perfluorochemicals and antioxidants. Cell Preserv Technol. 2003;1:165-74.
17. Gibb Z, Butler TJ, Morris LH , Maxwell WM, Grupen CG. Quercetin improves the
postthaw characteristics of cryopreserved sex-sorted and nonsorted stallion sperm.
Theriogenology. 2013;79:1001-9.
18. Varner DDD, Gibb Z, Aitken RJ. Stallion fertility: a focus on the spermatozoon. Equine
Vet J. 2015;47:16-24.
19. Varner D, Johnson L. From a sperm’s view – revisiting our perception of this intriguing
cell. AEEP Proceedings. 2007;53:104-77.
20. Nelson DL, Cox MM. Lehninger princípios da bioquímica. 6a ed. Porto Alegre: Artmed;
2014.
21. Venditti P, Di Stefano L, Di Meo S. Mitochondrial metabolism of reactive oxygen
species. Mitochondrion. 2013;13:71-82.
22. Lenaz G, Fato R, Formiggini G, Genova ML. The role of coenzyme Q in mitochondrial
electron transport. Mitochondrion. 2007;7:S8-33.
23. Turrens JF. Mitochondrial formation of reactive oxygen species. J Physiol.
2003;552:335-44.
24. Kussmaul L, Hirst J. The mechanism of superoxide production by NADH: ubiquinone
oxidoreductase (complex I) from bovine heart mitochondria. Proc Natl Acad Sci U S A.
2006;103:7607-12.
25. Lenzi A, Gandini L, Picardo M, Tramer F, Sandri G, Panfili E. Lipoperoxidation damage
of spermatozoa polyunsaturated fatty acids (PUFA): scavenger mechanisms and possible
scavenger therapies. Front Biosci. 2000;5:1-15.
26. Maia MS, Bicudo SD. Radicais livres, antioxidantes e função espermática em mamíferos:
uma revisão. Rev Bras Reprod Anim. 2009;33:183-93.
27. Lenaz G. The mitochondrial production of reactive oxygen species: mechanisms and
implications in human pathology. IUBMB Life. 2001;52:159-64.
28. Nogueira BG, Bitencourt JL, Sampaio BFB, Bender ESC, Costa e Silva EV, Zúccari
CESN. Peroxidação lipídica e agentes antioxidantes no sêmen de mamíferos. Rev
Eletronica Vet. 2013;15:1-15.
29. Lambert AJ, Brand MD. Superoxide production by NADH: ubiquinone oxidoreductase
(complex I) depends on the pH gradient across the mitochondrial inner membrane.
Biochem J. 2004;382:511-7.
30. Griveau JF, Le Lannou D. Reactive oxygen species and human spermatozoa: physiology
and pathology. Int J Androl. 1997;20:61-9.
31. Barreiros ALBS, David JM, David JP. Estresse oxidativo: relação entre geração de
espécies reativas e defesa do organismo. Quim Nova. 2006;29:113-23.
32. Salmani H, Nabi MM, Vaseghi-Dodaran H, Rahman MB, Mohammadi-Sangcheshmeh
A, Shakeri M, et al. Effect of glutathione in soybean lecithin-based semen extender on
goat semen quality after freeze-thawing. Small Rumin Res. 2013;112:123-7.
33. Halliwell B. Oxidative stress and neurodegeneration. Where are we now? J Neurochem.
2006;97:1634-58.
34. Catala A. An overview of lipid peroxidation with emphasis in outer segments of
photoreceptors and the chemiluminescence assay. Int J Biochem Cell Biol.
2006;38:1482-95.
35. Schober D, Aurich C, Nohl H, Gille L. Influence of cryopreservation on mitochondrial
functions in equine spermatozoa. Theriogenology. 2007;68:745-54.
36. Alvarez JG, Storey BT. Evidence for increased lipid peroxidative damage and loss of
superoxide dismutase activity as a mode of sublethal cryodamage to human sperm during
cryopreservation. J Androl. 1992;13:232-41.
37. Silva ECB, Guerra MMP. Terapias antioxidantes na criopreservação espermática. Rev
Port Cienc Vet. 2012;107:143-9.
38. Andreyev AY, Kushnareva YE, Starkov AA. Mitochondrial metabolism of reactive
oxygen species. Biochemistry. 2005;70:200-14.
39. Nogueira BG, Bitencourt JL, Sampaio BFB, Bender ESC, Costa e Silva EV, Zúccari
CESN. Peroxidação lipídica e agentes antioxidantes no sêmen de mamíferos. Rev
Eletronica Vet. 2013;15:1-15.
40. Kankofer M, Kolm G, Aurich J, Aurich C. Activity of glutathione peroxidase, superoxide
dismutase and catalase and lipid peroxidation intensity in stallion semen during storage at
5°C. Theriogenology. 2005;63:1354-65.
41. Alvarez G, Storey BT. Role of glutathione peroxidase in protecting mammalian
spermatozoa from loss of motility caused by spontaneous lipid peroxidation. Gamete Res.
1989;23:77-90.
42. Andrade ER, Melo-Sterza FA, Seneda MM, Alfieri AA. Consequências da produção das
espécies reativas de oxigênio na reprodução e principais mecanismos antioxidantes. Rev
Bras Reprod Anim. 2010;34:79-85.
43. Wright JS, Johnson ER, Dilabio GA. Predicting the activity of phenolic antioxidants:
theoretical method, analysis of substituent effects, and application to major families of
antioxidants. J Am Chem Soc. 2001;123:1173-83.
44. Stojanovic S, Sprinz H, Brede O. Efficiency and mechanism of the antioxidant action of
trans-resveratrol and its analogues in the radical liposome oxidation. Arch Biochem
Biophys. 2001;391:79-89.
45. Aitken RJ, Clarkson JS. Cellular basis of defective sperm function and its association
with the genesis of reactive oxygen species by human spermatozoa. J Reprod Fertil.
1988;81:459-69.
46. Ijaz A, Hussain A, Aleem M, Yousaf MS, Rehman H. Butylated hydroxytoluene
inclusion in semen extender improves the post-thawed semen quality of Nili-Ravi buffalo
(Bubalus bubalis). Theriogenology. 2009;71:1326-9.
47. Ansari MS, Rakha BR, Akhter S. Effect of butylated hydroxytoluene supplementation in
extender on motility, plasmalemma and viability of sahiwal bull spermatozoa. Pak J Zool.
2011;43:311-4.
48. Neagu VR, García BM, Sandoval CS, Rodríguez AM, Ferrusola CO, Fernández LG, et
al. Freezing dog semen in presence of the antioxidant butylated hydroxytoluene improves
postthaw sperm membrane integrity. Theriogenology. 2010;73:645-50.
49. Trzcińska M, Bryła M, Gajda B, Gogol P. Fertility of boar semen cryopreserved in
extender supplemented with butylated hydroxytoluene. Theriogenology. 2015;83:307-13.
50. Alrawaiq NS, Abdullah A. A review of flavonoid quercetin: metabolism, bioactivity and
antioxidant properties. Int J PharmTech Res. 2014;6:933-41.
51. Afanas'ev IB, Dorozhko AI, Brodskii AV, Kostyuk VA, Potapovitch AI. Chelating and
free radical scavenging mechanisms of inhibitory action of rutin and quercetin in lipid
peroxidation. Biochem Pharmacol. 1989;38:1763-9.
52. Chen Y, Zheng R, Jia Z, Ju Y. Flavonoids as superoxide scavengers and antioxidants.
Free Radic Biol Med. 1990;9:19-21.
53. Gülçin I. Antioxidant activity of food constituents: an overview. Arch Toxicol.
2012;86:345-91.
INRA plus soybean lecithin extender on semen quality to freeze miniature caspian horse
semen. J Equine Vet Sci. 2013;33:1050-3.
2. Morillo-Rodríguez A, Macías-García B, Tapia JA, Ortega-Ferrusola C, Peña FJ.
Consequences of butylated hydroxytoluene in the freezing extender on post-thaw
characteristics of stallion spermatozoa in vitro. Andrologia. 2012;44:688-95.
3. Ortega-Ferrusola C, Gonzalez FL, Morrell JM, Salazar SC, Macías-García B, RodriguezMartinez H, et al. Lipid peroxidation, assessed with BODIPY-C11, increases after
cryopreservation of stallion spermatozoa, is stallion-dependent and is related to apoptoticlike changes. Reproduction. 2009;138:55-63.
4. García BM, Fernández LG, Ferrusola CO, Rodríguez AM, Bolaños JMG, Martinez HR, et
al. Fatty acids and plasmalogens of the phospholipids of the sperm membranes and their
relation with the post-thaw quality of stallion spermatozoa. Theriogenology. 2011;75:811-
18.
5. Aitken RJ, Harkiss D, Knox W, Paterson M, Irvine DS. A novel signal transduction
cascade in capacitating human spermatozoa characterised by a redox-regulated, cAMPmediated induction of tyrosine phosphorylation. J Cell Sci. 1998;111:645-56.
6. Lenzi A, Gandini L, Lombardo F, Picardo M, Maresca V, Panfili E, et al. Polyunsaturated
fatty acids of germ cell membranes, glutathione and blutathione-dependent enzymePHGPx: from basic to clinic. Contraception. 2002;65:301-4.
7. Ford WCL. Regulation of sperm function by reactive oxygen species. Hum Reprod
Update. 2004;10:387-99.
8. Kothari S, Thompson A, Agarwal A, Du Plessis SS. Free radicals: their beneficial and
detrimental effects on sperm function. Indian J Exp Biol. 2010;48:425-35.
9. Cocchia N, Pasolini MP, Mancini R, Petrazzuolo O, Cristofaro I, Rosapane I, et al. Effect
of sod (superoxide dismutase) protein supplementation in semen extenders on motility,
viability, acrosome status and ERK (extracellular signal-regulated kinase) protein
phosphorylation of chilled stallion spermatozoa. Theriogenology. 2011;75:1201-10.
10. Oliveira RA, Wolf CA, Oliveira MA, Gambarini ML. Addition of glutathione to na
extender for frozen equine sêmen. J Equine Vet Sci. 2013;33:1148-52.
11. Aurich JE, Schönherr U, Hoppe H, Aurich C. Effects of antioxidants on motility and
membrane integrity of chilled-stored stallion semen. Theriogenology. 1997;48:185-92.
12. Ball BA, Medina V, Gravance CG, Baumber J. Effect of antioxidants on preservation of
motility,viability and acrosomal integrity of equine spermatozoa during storage at 5°C.
Theriogenology. 2001;56:577-89.
13. Almeida J, Ball BA. Effect of α-tocopherol and tocopherol succinate on lipid
peroxidation in equine spermatozoa. Anim Reprod Sci. 2005;87:321-37.
14. Franco JSV, Chaveiro A, Góis A, Silva FMS. Effects of α-tocopherol and ascorbic acid
on equine semen quality after cryopreservation. J Equine Vet Sci. 2013;33:787-93.
15. Yousefian I, Zare-Shahneh A, Zhandi M. The effect of coenzyme q10 and α-tocopherol
in skim milk–based extender for preservation of caspian stallion semen in cool condition.
J Equine Vet Sci. 2014;34:949-54.
16. McNiven MA, Richardson GF. Chilled storage of stallion semen using
perfluorochemicals and antioxidants. Cell Preserv Technol. 2003;1:165-74.
17. Gibb Z, Butler TJ, Morris LH , Maxwell WM, Grupen CG. Quercetin improves the
postthaw characteristics of cryopreserved sex-sorted and nonsorted stallion sperm.
Theriogenology. 2013;79:1001-9.
18. Varner DDD, Gibb Z, Aitken RJ. Stallion fertility: a focus on the spermatozoon. Equine
Vet J. 2015;47:16-24.
19. Varner D, Johnson L. From a sperm’s view – revisiting our perception of this intriguing
cell. AEEP Proceedings. 2007;53:104-77.
20. Nelson DL, Cox MM. Lehninger princípios da bioquímica. 6a ed. Porto Alegre: Artmed;
2014.
21. Venditti P, Di Stefano L, Di Meo S. Mitochondrial metabolism of reactive oxygen
species. Mitochondrion. 2013;13:71-82.
22. Lenaz G, Fato R, Formiggini G, Genova ML. The role of coenzyme Q in mitochondrial
electron transport. Mitochondrion. 2007;7:S8-33.
23. Turrens JF. Mitochondrial formation of reactive oxygen species. J Physiol.
2003;552:335-44.
24. Kussmaul L, Hirst J. The mechanism of superoxide production by NADH: ubiquinone
oxidoreductase (complex I) from bovine heart mitochondria. Proc Natl Acad Sci U S A.
2006;103:7607-12.
25. Lenzi A, Gandini L, Picardo M, Tramer F, Sandri G, Panfili E. Lipoperoxidation damage
of spermatozoa polyunsaturated fatty acids (PUFA): scavenger mechanisms and possible
scavenger therapies. Front Biosci. 2000;5:1-15.
26. Maia MS, Bicudo SD. Radicais livres, antioxidantes e função espermática em mamíferos:
uma revisão. Rev Bras Reprod Anim. 2009;33:183-93.
27. Lenaz G. The mitochondrial production of reactive oxygen species: mechanisms and
implications in human pathology. IUBMB Life. 2001;52:159-64.
28. Nogueira BG, Bitencourt JL, Sampaio BFB, Bender ESC, Costa e Silva EV, Zúccari
CESN. Peroxidação lipídica e agentes antioxidantes no sêmen de mamíferos. Rev
Eletronica Vet. 2013;15:1-15.
29. Lambert AJ, Brand MD. Superoxide production by NADH: ubiquinone oxidoreductase
(complex I) depends on the pH gradient across the mitochondrial inner membrane.
Biochem J. 2004;382:511-7.
30. Griveau JF, Le Lannou D. Reactive oxygen species and human spermatozoa: physiology
and pathology. Int J Androl. 1997;20:61-9.
31. Barreiros ALBS, David JM, David JP. Estresse oxidativo: relação entre geração de
espécies reativas e defesa do organismo. Quim Nova. 2006;29:113-23.
32. Salmani H, Nabi MM, Vaseghi-Dodaran H, Rahman MB, Mohammadi-Sangcheshmeh
A, Shakeri M, et al. Effect of glutathione in soybean lecithin-based semen extender on
goat semen quality after freeze-thawing. Small Rumin Res. 2013;112:123-7.
33. Halliwell B. Oxidative stress and neurodegeneration. Where are we now? J Neurochem.
2006;97:1634-58.
34. Catala A. An overview of lipid peroxidation with emphasis in outer segments of
photoreceptors and the chemiluminescence assay. Int J Biochem Cell Biol.
2006;38:1482-95.
35. Schober D, Aurich C, Nohl H, Gille L. Influence of cryopreservation on mitochondrial
functions in equine spermatozoa. Theriogenology. 2007;68:745-54.
36. Alvarez JG, Storey BT. Evidence for increased lipid peroxidative damage and loss of
superoxide dismutase activity as a mode of sublethal cryodamage to human sperm during
cryopreservation. J Androl. 1992;13:232-41.
37. Silva ECB, Guerra MMP. Terapias antioxidantes na criopreservação espermática. Rev
Port Cienc Vet. 2012;107:143-9.
38. Andreyev AY, Kushnareva YE, Starkov AA. Mitochondrial metabolism of reactive
oxygen species. Biochemistry. 2005;70:200-14.
39. Nogueira BG, Bitencourt JL, Sampaio BFB, Bender ESC, Costa e Silva EV, Zúccari
CESN. Peroxidação lipídica e agentes antioxidantes no sêmen de mamíferos. Rev
Eletronica Vet. 2013;15:1-15.
40. Kankofer M, Kolm G, Aurich J, Aurich C. Activity of glutathione peroxidase, superoxide
dismutase and catalase and lipid peroxidation intensity in stallion semen during storage at
5°C. Theriogenology. 2005;63:1354-65.
41. Alvarez G, Storey BT. Role of glutathione peroxidase in protecting mammalian
spermatozoa from loss of motility caused by spontaneous lipid peroxidation. Gamete Res.
1989;23:77-90.
42. Andrade ER, Melo-Sterza FA, Seneda MM, Alfieri AA. Consequências da produção das
espécies reativas de oxigênio na reprodução e principais mecanismos antioxidantes. Rev
Bras Reprod Anim. 2010;34:79-85.
43. Wright JS, Johnson ER, Dilabio GA. Predicting the activity of phenolic antioxidants:
theoretical method, analysis of substituent effects, and application to major families of
antioxidants. J Am Chem Soc. 2001;123:1173-83.
44. Stojanovic S, Sprinz H, Brede O. Efficiency and mechanism of the antioxidant action of
trans-resveratrol and its analogues in the radical liposome oxidation. Arch Biochem
Biophys. 2001;391:79-89.
45. Aitken RJ, Clarkson JS. Cellular basis of defective sperm function and its association
with the genesis of reactive oxygen species by human spermatozoa. J Reprod Fertil.
1988;81:459-69.
46. Ijaz A, Hussain A, Aleem M, Yousaf MS, Rehman H. Butylated hydroxytoluene
inclusion in semen extender improves the post-thawed semen quality of Nili-Ravi buffalo
(Bubalus bubalis). Theriogenology. 2009;71:1326-9.
47. Ansari MS, Rakha BR, Akhter S. Effect of butylated hydroxytoluene supplementation in
extender on motility, plasmalemma and viability of sahiwal bull spermatozoa. Pak J Zool.
2011;43:311-4.
48. Neagu VR, García BM, Sandoval CS, Rodríguez AM, Ferrusola CO, Fernández LG, et
al. Freezing dog semen in presence of the antioxidant butylated hydroxytoluene improves
postthaw sperm membrane integrity. Theriogenology. 2010;73:645-50.
49. Trzcińska M, Bryła M, Gajda B, Gogol P. Fertility of boar semen cryopreserved in
extender supplemented with butylated hydroxytoluene. Theriogenology. 2015;83:307-13.
50. Alrawaiq NS, Abdullah A. A review of flavonoid quercetin: metabolism, bioactivity and
antioxidant properties. Int J PharmTech Res. 2014;6:933-41.
51. Afanas'ev IB, Dorozhko AI, Brodskii AV, Kostyuk VA, Potapovitch AI. Chelating and
free radical scavenging mechanisms of inhibitory action of rutin and quercetin in lipid
peroxidation. Biochem Pharmacol. 1989;38:1763-9.
52. Chen Y, Zheng R, Jia Z, Ju Y. Flavonoids as superoxide scavengers and antioxidants.
Free Radic Biol Med. 1990;9:19-21.
53. Gülçin I. Antioxidant activity of food constituents: an overview. Arch Toxicol.
2012;86:345-91.
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Published
2017-09-29
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Merces Chaves Silva LF, Adonis Braga de Araujo E, Nunes de Oliveira S, Morales Dalanezi F, Pena de Andrade Júnior LR, Ferreira de Souza F, Maciel Crespilho A, Dell’Aqua Junior JA, Ozanam Papa F. Key of mechanisms of action antioxidants used in cryopreservation sperm stallions. RVZ [Internet]. 2017 Sep. 29 [cited 2024 Jul. 22];24(3):418-34. Available from: https://rvz.emnuvens.com.br/rvz/article/view/277
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