Supplementation of Freezing Medium with Alpha-Mangostin Improves Human Sperm Quality after Cryopreservation
Main Article Content
Abstract
Sperm cryopreservation, a routine technique in assisted reproductive technology (ART), is an efficient procedure to preserve sperm viability. Even though cryo-preservation has benefits on fertility preservation, it has a negative effect on sperm due to oxidative stress, causing damage and affecting sperm quality. The addition of antioxidants to the freezing media may protect the sperm quality after cryopreservation. Alpha-mangostin (α-MG) has been confirmed as having high potential antioxidant effects in several cell types. However, the protective effect of α-MG on sperm quality after cryopreservation has not yet been explored. This study aimed to investigate the effect of α-MG supplementation to a freezing media on motility, viability, malondialdehyde (MDA) level and catalase (CAT) activity in human sperm. Semen samples were obtained from 7 healthy men and divided into following groups (n=7 per group): control, freezing medium supplemented with 25 and 50 µM α-MG. Sperm samples were frozen by vitrification technique and stored at -196°C. After 2 weeks, the sperm samples were thawed and all parameters were evaluated. The results showed that supplementation with 25 and 50 µM α-MG in the freezing medium tended to increase the total sperm motility and progressive sperm motility. Furthermore, supplementation with 50 µM α-MG significantly increased sperm viability, CAT activity and decreased MDA level (p<0.05). Alpha-mangostin contains an antioxidant effect that could scavenge the reactive oxygen species (ROS) thus achieving a balance between ROS and the antioxidant activity. Therefore, α-MG may protect human sperm damage from cryopreservation.
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References
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2. Woods EJ, Benson JD, Agca Y, Critser JK. Fundamental cryobiology of reproductive cells and tissues. Cryobiology. 2004 Apr;48(2):146-56.
3. Royere D, Barthelemy C, Hamamah S, Lansac J. Cryopreservation of spermatozoa: a 1996 review. Hum Reprod Update. 1996 Nov-Dec;2(6):553-9.
4. Pena FJ, Johannisson A, Wallgren M, Rodriguez Martinez H. Antioxidant supplementation in vitro improves boar sperm motility and mitochondrial membrane potential after cryopreservation of different fractions of the ejaculate. Anim Reprod Sci. 2003 Sep 15;78(1-2):85-98.
5. 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 May-Jun;13(3):232-41.
6. Storey BT. Biochemistry of the induction and prevention of lipoperoxidative damage in human spermatozoa. Mol Hum Reprod. 1997 Mar;3(3):203-13.
7. Lenzi A, Picardo M, Gandini L, Dondero F. Lipids of the sperm plasma membrane: from polyunsaturated fatty acids considered as markers of sperm function to possible scavenger therapy. Hum Reprod Update. 1996 May-Jun;2(3):246-56.
8. Duru NK, Morshedi MS, Schuffner A, Oehninger S. Cryopreservation-thawing of fractionated human spermatozoa is associated with membrane phosphatidyl-serine externalization and not DNA fragmentation. J Androl. 2001 Jul-Aug;22(4): 646-51.
9. Baumber J, Ball BA, Linfor JJ, Meyers SA. Reactive oxygen species and cryopreservation promote DNA fragmentation in equine spermatozoa. J Androl. 2003 Jul-Aug;24(4):621-8.
10. Parks JE, Lynch DV. Lipid composition and thermotropic phase behavior of boar, bull, stallion, and rooster sperm membranes. Cryobiology. 1992 Apr;29(2): 255-66.
11. Kemal Duru N, Morshedi M, Oehninger S. Effects of hydrogen peroxide on DNA and plasma membrane integrity of human spermatozoa. Fertil Steril. 2000 Dec;74(6):1200-7.
12. Li P, Li Z-H, Dzyuba B, Hulak M, Rodina M, Linhart O. Evaluating the impacts of osmotic and oxidative stress on common carp (Cyprinus carpio, L.) sperm caused by cryopreservation techniques. Biol Reprod. 2010 Nov;83(5):852-8.
13. Nair SJ, Brar AS, Ahuja CS, Sangha SPS, Chaudhary KC. A comparative study on lipid peroxidation, activities of antioxidant enzymes and viability of cattle and buffalo bull spermatozoa during storage at refrigeration temperature. Anim Reprod Sci. 2006 Nov;96(1-2):21-9.
14. Taylor K, Roberts P, Sanders K, Burton P. Effect of antioxidant supplementation of cryopreservation medium on post-thaw integrity of human spermatozoa. Reprod BioMed Online. 2009 Feb;18(2):184-9.
15. Li Z, Lin Q, Liu R, Xiao W, Liu W. Protective effects of ascorbate and catalase on human spermatozoa during cryopreservation. J Androl. 2010 Sep-Oct;31(5): 437-44.
16. Zribi N, Chakroun NF, Ben Abdallah F, Elleuch H, Sellami A, Gargouri J, et al. Effect of freezing–thawing process and quercetin on human sperm survival and DNA integrity. Cryobiology. 2012 Dec;65(3):326-31.
17. Chairungsrilerd N, Takeuchi K, Ohizumi Y, Nozoe S, Ohta T. Mangostanol, a prenyl xanthone from Garcinia mangostana. Phytochemistry. 1996 Nov;43(5): 1099-1102.
18. Walker EB. HPLC analysis of selected xanthones in mangosteen fruit. J Sep Sci. 2007 Jun;30(9):1229-34.
19. Sanchez-Perez Y, Morales-Barcenas R, Garcia-Cuellar CM, Lopez-Marure R, Calderon-Oliver M, Pedraza-Chaverri J, et al. The alpha-mangostin prevention on cisplatin-induced apoptotic death in LLC-PK1 cells is associated to an inhibition of ROS production and p53 induction. Chem Biol Interact. 2010 Oct 6; 188(1):144-50.
20. Ibrahim MY, Hashim NM, Mariod AA, Mohan S, Abdulla MA, Abdelwahab SI, et al. α-Mangostin from Garcinia mangostana Linn: an updated review of its pharmacological properties. Arabian J Chem. 2016 May;9(3):317-29.
21. Gutierrez-Orozco F, Chitchumroonchokchai C, Lesinski GB, Suksamrarn S, Failla ML. α-Mangostin: anti-inflammatory activity and metabolism by human cells. J Agric Food Chem. 2013 Apr 24;61(16):3891-900.
22. Gupta SC, Tyagi AK, Deshmukh-Taskar P, Hinojosa M, Prasad S, Aggarwal BB. Downregulation of tumor necrosis factor and other proinflammatory biomarkers by polyphenols. Arch Biochem Biophys. 2014 Oct 1;559:91-9.
23. Upegui Y, Robledo SM, Gil Romero JF, Quinones W, Archbold R, Torres F, et al. In vivo Antimalarial activity of α-mangostin and the new xanthone -mangostin. Phytother Res. 2015 Aug;29(8):1195-201.
24. Nelli GB, K AS, Kilari EK. Antidiabetic effect of α-mangostin and its protective role in sexual dysfunction of streptozotocin induced diabetic male rats. Syst Biol Reprod Med. 2013 Dec;59(6):319-28.
25. World Health Organization. WHO laboratory manual for the examination and processing of human semen. 5th ed. Geneva: World Health Organization; 2007.
26. Beers RF, Jr., Sizer IW. A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem. 1952 Mar;195(1):133-40.
27. Mazzilli F, Rossi T, Sabatini L, Pulcinelli FM, Rapone S, Dondero F, et al. Human sperm cryopreservation and reactive oxygen species (ROS) production. Acta Eur Fertil. 1995 Jul-Aug;26(4):145-8.
28. Thomson LK, Fleming SD, Aitken RJ, De Iuliis GN, Zieschang JA, Clark AM. Cryopreservation-induced human sperm DNA damage is predominantly mediated by oxidative stress rather than apoptosis. Human Reprod. 2009 Sep;24(9):2061-70.
29. Parinaud J, Le Lannou D, Vieitez G, Griveau JF, Milhet P, Richoilley G. Enhancement of motility by treating spermatozoa with an antioxidant solution (Sperm-Fit) following ejaculation. Hum Reprod. 1997 Nov;12(11):2434-6.
30. Garcez ME, dos Santos Branco C, Lara LV, Pasqualotto FF, Salvador M. Effects of resveratrol supplementation on cryopreservation medium of human semen. Fertil Steril. 2010 Nov;94(6):2118-21.
31. Fontoura P, Mello MD, Gallo-Sá P, Erthal-Martins MC, Cardoso MCA, Ramos C. Leptin improves sperm cryopreservation via antioxidant defense. J Reprod Infertil. 2017 Jan-Mar;18(1):172-8.
32. Pedraza-Chaverrí J, Reyes-Fermín LM, Nolasco-Amaya EG, Orozco-Ibarra M, Medina-Campos ON, González-Cuahutencos O, et al. ROS scavenging capacity and neuroprotective effect of α-mangostin against 3-nitropropionic acid in cerebellar granule neurons. Exp Toxicol Pathol. 2009 Sep;61(5):491-501.
33. Martinez A, Galano A, Vargas R. Free radical scavenger properties of α-mangostin: thermodynamics and kinetics of HAT and RAF mechanisms. J Phys Chem B. 2011 Nov 3;115(43):12591-8.
34. Kosem N, Han Y-H, Moongkarndi P. Antioxidant and cytoprotective activities of methanolic extract from Garcinia mangostana hulls. ScienceAsia. 2007 Sep; 33:283-92.
35. Chen SC, Chao H, L Pan R, Wei Y-H. Hydroxyl radical-induced decline in motility and increase in lipid peroxidation and DNA modification in human sperm. Biochem Mol Biol Int. 1997 Oct; 43(2):291-303.
36. Devi Sampath P, Vijayaraghavan K. Cardioprotective effect of α-mangostin, a xanthone derivative from mangosteen on tissue defense system against isoproterenol-induced myocardial infarction in rats. J Biochem Mol Toxicol. 2007;21(6):336-9.
37. Buravlev EV, Shevchenko OG, Anisimov AA, Suponitsky KY. Novel Mannich bases of - and -mangostins: synthesis and evaluation of antioxidant and membrane-protective activity. Eur J Med Chem. 2018 May 25;152:10-20.
38. Lee D, Kim Y-M, Jung K, Chin Y-W, Kang KS. Alpha-mangostin improves insulin secretion and protects INS-1 cells from streptozotocin-induced damage. Int J Mol Sci. 2018;19(5):1484.
39. Tsai S-Y, Chung P-C, Owaga EE, Tsai IJ, Wang P-Y, Tsai J-I, et al. Alpha-mangostin from mangosteen (Garcinia mangostana Linn.) pericarp extract reduces high fat-diet induced hepatic steatosis in rats by regulating mitochondria function and apoptosis. Nutr Metab (Lond). 2016 Dec 1;13:88.
2. Woods EJ, Benson JD, Agca Y, Critser JK. Fundamental cryobiology of reproductive cells and tissues. Cryobiology. 2004 Apr;48(2):146-56.
3. Royere D, Barthelemy C, Hamamah S, Lansac J. Cryopreservation of spermatozoa: a 1996 review. Hum Reprod Update. 1996 Nov-Dec;2(6):553-9.
4. Pena FJ, Johannisson A, Wallgren M, Rodriguez Martinez H. Antioxidant supplementation in vitro improves boar sperm motility and mitochondrial membrane potential after cryopreservation of different fractions of the ejaculate. Anim Reprod Sci. 2003 Sep 15;78(1-2):85-98.
5. 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 May-Jun;13(3):232-41.
6. Storey BT. Biochemistry of the induction and prevention of lipoperoxidative damage in human spermatozoa. Mol Hum Reprod. 1997 Mar;3(3):203-13.
7. Lenzi A, Picardo M, Gandini L, Dondero F. Lipids of the sperm plasma membrane: from polyunsaturated fatty acids considered as markers of sperm function to possible scavenger therapy. Hum Reprod Update. 1996 May-Jun;2(3):246-56.
8. Duru NK, Morshedi MS, Schuffner A, Oehninger S. Cryopreservation-thawing of fractionated human spermatozoa is associated with membrane phosphatidyl-serine externalization and not DNA fragmentation. J Androl. 2001 Jul-Aug;22(4): 646-51.
9. Baumber J, Ball BA, Linfor JJ, Meyers SA. Reactive oxygen species and cryopreservation promote DNA fragmentation in equine spermatozoa. J Androl. 2003 Jul-Aug;24(4):621-8.
10. Parks JE, Lynch DV. Lipid composition and thermotropic phase behavior of boar, bull, stallion, and rooster sperm membranes. Cryobiology. 1992 Apr;29(2): 255-66.
11. Kemal Duru N, Morshedi M, Oehninger S. Effects of hydrogen peroxide on DNA and plasma membrane integrity of human spermatozoa. Fertil Steril. 2000 Dec;74(6):1200-7.
12. Li P, Li Z-H, Dzyuba B, Hulak M, Rodina M, Linhart O. Evaluating the impacts of osmotic and oxidative stress on common carp (Cyprinus carpio, L.) sperm caused by cryopreservation techniques. Biol Reprod. 2010 Nov;83(5):852-8.
13. Nair SJ, Brar AS, Ahuja CS, Sangha SPS, Chaudhary KC. A comparative study on lipid peroxidation, activities of antioxidant enzymes and viability of cattle and buffalo bull spermatozoa during storage at refrigeration temperature. Anim Reprod Sci. 2006 Nov;96(1-2):21-9.
14. Taylor K, Roberts P, Sanders K, Burton P. Effect of antioxidant supplementation of cryopreservation medium on post-thaw integrity of human spermatozoa. Reprod BioMed Online. 2009 Feb;18(2):184-9.
15. Li Z, Lin Q, Liu R, Xiao W, Liu W. Protective effects of ascorbate and catalase on human spermatozoa during cryopreservation. J Androl. 2010 Sep-Oct;31(5): 437-44.
16. Zribi N, Chakroun NF, Ben Abdallah F, Elleuch H, Sellami A, Gargouri J, et al. Effect of freezing–thawing process and quercetin on human sperm survival and DNA integrity. Cryobiology. 2012 Dec;65(3):326-31.
17. Chairungsrilerd N, Takeuchi K, Ohizumi Y, Nozoe S, Ohta T. Mangostanol, a prenyl xanthone from Garcinia mangostana. Phytochemistry. 1996 Nov;43(5): 1099-1102.
18. Walker EB. HPLC analysis of selected xanthones in mangosteen fruit. J Sep Sci. 2007 Jun;30(9):1229-34.
19. Sanchez-Perez Y, Morales-Barcenas R, Garcia-Cuellar CM, Lopez-Marure R, Calderon-Oliver M, Pedraza-Chaverri J, et al. The alpha-mangostin prevention on cisplatin-induced apoptotic death in LLC-PK1 cells is associated to an inhibition of ROS production and p53 induction. Chem Biol Interact. 2010 Oct 6; 188(1):144-50.
20. Ibrahim MY, Hashim NM, Mariod AA, Mohan S, Abdulla MA, Abdelwahab SI, et al. α-Mangostin from Garcinia mangostana Linn: an updated review of its pharmacological properties. Arabian J Chem. 2016 May;9(3):317-29.
21. Gutierrez-Orozco F, Chitchumroonchokchai C, Lesinski GB, Suksamrarn S, Failla ML. α-Mangostin: anti-inflammatory activity and metabolism by human cells. J Agric Food Chem. 2013 Apr 24;61(16):3891-900.
22. Gupta SC, Tyagi AK, Deshmukh-Taskar P, Hinojosa M, Prasad S, Aggarwal BB. Downregulation of tumor necrosis factor and other proinflammatory biomarkers by polyphenols. Arch Biochem Biophys. 2014 Oct 1;559:91-9.
23. Upegui Y, Robledo SM, Gil Romero JF, Quinones W, Archbold R, Torres F, et al. In vivo Antimalarial activity of α-mangostin and the new xanthone -mangostin. Phytother Res. 2015 Aug;29(8):1195-201.
24. Nelli GB, K AS, Kilari EK. Antidiabetic effect of α-mangostin and its protective role in sexual dysfunction of streptozotocin induced diabetic male rats. Syst Biol Reprod Med. 2013 Dec;59(6):319-28.
25. World Health Organization. WHO laboratory manual for the examination and processing of human semen. 5th ed. Geneva: World Health Organization; 2007.
26. Beers RF, Jr., Sizer IW. A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem. 1952 Mar;195(1):133-40.
27. Mazzilli F, Rossi T, Sabatini L, Pulcinelli FM, Rapone S, Dondero F, et al. Human sperm cryopreservation and reactive oxygen species (ROS) production. Acta Eur Fertil. 1995 Jul-Aug;26(4):145-8.
28. Thomson LK, Fleming SD, Aitken RJ, De Iuliis GN, Zieschang JA, Clark AM. Cryopreservation-induced human sperm DNA damage is predominantly mediated by oxidative stress rather than apoptosis. Human Reprod. 2009 Sep;24(9):2061-70.
29. Parinaud J, Le Lannou D, Vieitez G, Griveau JF, Milhet P, Richoilley G. Enhancement of motility by treating spermatozoa with an antioxidant solution (Sperm-Fit) following ejaculation. Hum Reprod. 1997 Nov;12(11):2434-6.
30. Garcez ME, dos Santos Branco C, Lara LV, Pasqualotto FF, Salvador M. Effects of resveratrol supplementation on cryopreservation medium of human semen. Fertil Steril. 2010 Nov;94(6):2118-21.
31. Fontoura P, Mello MD, Gallo-Sá P, Erthal-Martins MC, Cardoso MCA, Ramos C. Leptin improves sperm cryopreservation via antioxidant defense. J Reprod Infertil. 2017 Jan-Mar;18(1):172-8.
32. Pedraza-Chaverrí J, Reyes-Fermín LM, Nolasco-Amaya EG, Orozco-Ibarra M, Medina-Campos ON, González-Cuahutencos O, et al. ROS scavenging capacity and neuroprotective effect of α-mangostin against 3-nitropropionic acid in cerebellar granule neurons. Exp Toxicol Pathol. 2009 Sep;61(5):491-501.
33. Martinez A, Galano A, Vargas R. Free radical scavenger properties of α-mangostin: thermodynamics and kinetics of HAT and RAF mechanisms. J Phys Chem B. 2011 Nov 3;115(43):12591-8.
34. Kosem N, Han Y-H, Moongkarndi P. Antioxidant and cytoprotective activities of methanolic extract from Garcinia mangostana hulls. ScienceAsia. 2007 Sep; 33:283-92.
35. Chen SC, Chao H, L Pan R, Wei Y-H. Hydroxyl radical-induced decline in motility and increase in lipid peroxidation and DNA modification in human sperm. Biochem Mol Biol Int. 1997 Oct; 43(2):291-303.
36. Devi Sampath P, Vijayaraghavan K. Cardioprotective effect of α-mangostin, a xanthone derivative from mangosteen on tissue defense system against isoproterenol-induced myocardial infarction in rats. J Biochem Mol Toxicol. 2007;21(6):336-9.
37. Buravlev EV, Shevchenko OG, Anisimov AA, Suponitsky KY. Novel Mannich bases of - and -mangostins: synthesis and evaluation of antioxidant and membrane-protective activity. Eur J Med Chem. 2018 May 25;152:10-20.
38. Lee D, Kim Y-M, Jung K, Chin Y-W, Kang KS. Alpha-mangostin improves insulin secretion and protects INS-1 cells from streptozotocin-induced damage. Int J Mol Sci. 2018;19(5):1484.
39. Tsai S-Y, Chung P-C, Owaga EE, Tsai IJ, Wang P-Y, Tsai J-I, et al. Alpha-mangostin from mangosteen (Garcinia mangostana Linn.) pericarp extract reduces high fat-diet induced hepatic steatosis in rats by regulating mitochondria function and apoptosis. Nutr Metab (Lond). 2016 Dec 1;13:88.