The Activity of Ellagic Acid in Male Reproduction: A mini-review

Document Type : Mini Review

Authors

1 Área Académica de Medicina, Instituto de Ciencias de la Salud, Universidad Autónoma del Estado de Hidalgo. Ex hacienda la Concepción, Tilcuautla, C.P. 42160 Pachuca de Soto Hidalgo, México.

2 1 Área Académica de Medicina, Instituto de Ciencias de la Salud, Universidad Autónoma del Estado de Hidalgo. Ex hacienda la Concepción, Tilcuautla, C.P. 42160 Pachuca de Soto Hidalgo, México.

Abstract

Ellagic Acid (EA), is a naturally occurring phenolic found in some fruits and nuts. It has a great variety of biological activities, including properties antioxidant, anti-inflammatory, anti-thrombotic, anti-atherogenic, neuroprotective, hepatoprotective, anti-mutagenic, and anti-carcinogenic agent recently. This review aims to summarize experimental research carried out in vivo and in vitro that evaluated the EA treatment in male reproduction and discussed the mechanisms of action. For this purpose, PubMed and SCOPUS databases were searched to identify publications in this regard.

Keywords


1. Li A-N, Li S, Zhang Y-J, Xu X-R, Chen Y-M, Li H-B. Resources and Biological Activities of Natural Polyphenols. Nutrients. 2014; 6(12):6020–6047. doi: 10.3390/nu6126020.
2. Zhou Y, Zheng J, Li Y, Xu D-P, Li S, Chen Y-M, Li H-B. Natural Polyphenols for Prevention and Treatment of Cancer. Nutrients. 2016;8(8):pii: E515. doi: 10.3390/nu8080515.
3. Lipińska L, Klewicka E, Sójka M. The structure, occurrence and biological activity of ellagitannins: a general review. Acta Sci Pol Technol Aliment. 2014;13(3):289–299. doi:10.17306/J.AFS.2014.3.7
4. Rossi M, Erlebacher J, Zacharias DE, Carrell HL, Iannucci B. The crystal and molecular structure of ellagic acid dihydrate: a dietary anti-cancer agent. Carcinogenesis. 1991;12(12):2227–2232. doi:10.1093/carcin/12.12.2227
5. Priyadarsini KI, Khopde SM, Kumar SS, Mohan H. Free radical studies of ellagic acid, a natural phenolic antioxidant. J Agric Food Chem. 2002;50(7):2200–2206. doi:10.1021/jf011275g
6. Ríos J-L, Giner RM, Marín M, Recio MC. A Pharmacological Update of Ellagic Acid. Planta Med. 2018;84(15):1068–1093. doi: 10.1055/a-0633-9492.
7. Ceci C, Lacal PM, Tentori L, De Martino MG, Miano R, Graziani G. Experimental Evidence of the Antitumor, Antimetastatic and Antiangiogenic Activity of Ellagic Acid. Nutrients. 2018;10(11): 1756-1779. doi: 10.3390/nu10111756
8. Ahmed T, Setzer WN, Nabavi SF, Orhan IE, Braidy N, Sobarzo-Sanchez E, Nabavi SM. Insights Into Effects of Ellagic Acid on the Nervous System: A Mini Review. Curr Pharm Des. 2016;22(10): 1350–1360. doi:10.2174/1381612822666160125114503
9. Larrosa M, García-Conesa MT, Espín JC, Tomás-Barberán FA. Ellagitannins, ellagic acid and vascular health. Mol Aspects Med. 2010;31(6):513–539. doi: 10.1016/j.mam.2010.09.005.
10. Fedder MDK, Jakobsen HB, Giversen I, Christensen LP, Parner ET, Fedder J. An extract of pomegranate fruit and galangal rhizome increases the numbers of motile sperm: a prospective, randomised, controlled, double-blinded trial. PloS One. 2014;9(9):e108532. doi: 10.1371/journal.pone.0108532.
11. Yamada H, Wakamori S, Hirokane T, Ikeuchi K, Matsumoto S. Structural Revisions in Natural Ellagitannins. Mol J Synth Chem Nat Prod Chem. 2018;23(8). pii:E1901. doi: 10.3390/molecules23081901
12. Ismail T, Calcabrini C, Diaz AR, Fimognari C, Turrini E, Catanzaro E, Akhtar S, Sestili P. Ellagitannins in Cancer Chemoprevention and Therapy. Toxins. 2016;8(5):151. doi: 10.3390/toxins8050151.
13. Aguilera-Carbo A, Augur C, Prado-Barragan LA, Favela-Torres E, Aguilar CN. Microbial production of ellagic acid and biodegradation of ellagitannins. Appl Microbiol Biotechnol. 2008;78(2):189–199. doi:10.1007/s00253-007-1276-2
14. González-Barrio R, Borges G, Mullen W, Crozier A. Bioavailability of anthocyanins and ellagitannins following consumption of raspberries by healthy humans and subjects with an ileostomy. J Agric Food Chem. 2010;58(7):3933–3939. doi: 10.1021/jf100315d.
15. Mao X, Wu L-F, Zhao H, Liang W-Y, Chen W-J, Han S-X, et al. Transport of Corilagin, Gallic Acid, and Ellagic Acid from Fructus Phyllanthi Tannin Fraction in Caco-2 Cell Monolayers. Evid Based Complement Alternat Med. 2016; Article ID 9205379. doi:10.1155/2016/9205379
16. Selma MV, Espín JC, Tomás-Barberán FA. Interaction between phenolics and gut microbiota: role in human health. J Agric Food Chem. 2009;57(15):6485–6501. doi:10.1021/jf902107d
17. Espín JC, González-Barrio R, Cerdá B, López-Bote C, Rey AI, Tomás-Barberán FA. Iberian pig as a model to clarify obscure points in the bioavailability and metabolism of ellagitannins in humans. J Agric Food Chem. 2007;55(25):10476–10485. doi:10.1021/jf0723864
18. García-Villalba R, Beltrán D, Espín JC, Selma MV, Tomás-Barberán FA. Time course production of urolithins from ellagic acid by human gut microbiota. J Agric Food Chem. 2013;61(37):8797–8806. doi: 10.1021/jf402498b.
19. Cerdá B, Tomás-Barberán FA, Espín JC. Metabolism of antioxidant and chemopreventive ellagitannins from strawberries, raspberries, walnuts, and oak-aged wine in humans: identification of biomarkers and individual variability. J Agric Food Chem. 2005;53(2):227–235. doi:10.1021/jf049144d
20. Tulipani S, Urpi-Sarda M, García-Villalba R, Rabassa M, López-Uriarte P, Bulló M, et al. Urolithins are the main urinary microbial-derived phenolic metabolites discriminating a moderate consumption of nuts in free-living subjects with diagnosed metabolic syndrome. J Agric Food Chem. 2012;60(36) :8930–8940. doi:10.1021/jf301509w
21. Mora-Cubillos X, Tulipani S, Garcia-Aloy M, Bulló M, Tinahones FJ, Andres-Lacueva C. Plasma metabolomic biomarkers of mixed nuts exposure inversely correlate with severity of metabolic syndrome. Mol Nutr Food Res. 2015;59(12):2480–2490. doi: 10.1002/mnfr.201500549.
22. Truchado P, Larrosa M, García-Conesa MT, Cerdá B, Vidal-Guevara ML, Tomás-Barberán FA, et al. Strawberry processing does not affect the production and urinary excretion of urolithins, ellagic acid metabolites, in humans. J Agric Food Chem. 2012;60(23):5749–5754. doi: 10.1021/jf203641r.
23. González-Sarrías A, Giménez-Bastida JA, García-Conesa MT, Gómez-Sánchez MB, García-Talavera NV, Gil-Izquierdo A, et al. Occurrence of urolithins, gut microbiota ellagic acid metabolites and proliferation markers expression response in the human prostate gland upon consumption of walnuts and pomegranate juice. Mol Nutr Food Res. 2010;54(3):311–322. doi: 10.1002/mnfr.200900152.
24. Tomás-Barberán FA, García-Villalba R, González-Sarrías A, Selma MV, Espín JC. Ellagic acid metabolism by human gut microbiota: consistent observation of three urolithin phenotypes in intervention trials, independent of food source, age, and health status. J Agric Food Chem. 2014;62(28):6535–6538. doi: 10.1021/jf5024615.
25. Piwowarski JP, Granica S, Kiss AK. Influence of gut microbiota-derived ellagitannins’ metabolites urolithins on pro-inflammatory activities of human neutrophils. Planta Med. 2014;80(11):887–895. doi:10.1055/s-0034-1368615.
26. Ceribaşi AO, Türk G, Sönmez M, Sakin F, Ateşşahin A. Toxic effect of cyclophosphamide on sperm morphology, testicular histology and blood oxidant-antioxidant balance, and protective roles of lycopene and ellagic acid. Basic Clin Pharmacol Toxicol. 2010;107(3):730–736. doi: 10.1111/j.1742-7843.2010.00571.x.
27. Türk G, Ceribaşi AO, Sakin F, Sönmez M, Ateşşahin A. Antiperoxidative and anti-apoptotic effects of lycopene and ellagic acid on cyclophosphamide-induced testicular lipid peroxidation and apoptosis. Reprod Fertil Dev. 2010;22(4):587–596. doi: 10.1071/RD09078.
28. Ateşşahin A, Türk G, Yilmaz S, Sönmez M, Sakin F, Ceribasi AO. Modulatory effects of lycopene and ellagic acid on reproductive dysfunction induced by polychlorinated biphenyl (Aroclor 1254) in male rats. Basic Clin Pharmacol Toxicol. 2010;106(6):479–489. doi: 10.1111/j.1742-7843.2009.00529.x.
29. Çeribaşı AO, Sakin F, Türk G, Sönmez M, Ateşşahin A. Impact of ellagic acid on adriamycin-induced testicular histopathological lesions, apoptosis, lipid peroxidation and sperm damages. Exp Toxicol Pathol. 2012;64(7–8):717–724. doi: 10.1016/j.etp.2011.01.006.
30. Georgy GS, Maher OW. Ellagic acid and rosmarinic acid attenuate doxorubicin-induced testicular injury in rats. J Biochem Mol Toxicol. 2017;31(9). doi: 10.1002/jbt.21937.
31. Sönmez M, Türk G, Çeribaşı AO, Sakin F, Ateşşahin A. Attenuating effect of lycopene and ellagic acid on 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced spermiotoxicity and testicular apoptosis. Drug Chem Toxicol. 2011;34(4):347–356. doi: 10.3109/01480545.2011.557382.
32. Türk G, Sönmez M, Ceribaşi AO, Yüce A, Ateşşahin A. Attenuation of cyclosporine A-induced testicular and spermatozoal damages associated with oxidative stress by ellagic acid. Int Immunopharmacol. 2010;10(2):177–182. doi: 10.1016/j.intimp.2009.10.013.
33. Türk G, Ateşşahin A, Sönmez M, Ceribaşi AO, Yüce A. Improvement of cisplatin-induced injuries to sperm quality, the oxidant-antioxidant system, and the histologic structure of the rat testis by ellagic acid. Fertil Steril. 2008;89(5 Suppl):1474–1481. doi:10.1016/j.fertnstert.2007.04.059
34. Türk G, Ceribaşı AO, Sahna E, Ateşşahin A. Lycopene and ellagic acid prevent testicular apoptosis induced by cisplatin. Phytomedicine Int J Phytother Phytopharm. 2011;18(5):356–361. doi: 10.1016/j.phymed.2010.07.008.
35. Girish C, Shweta O, Raj V, Balakrishnan S, Varghese RG. Ellagic acid modulates sodium valproate induced reproductive toxicity in male Wistar rats. Indian J Physiol Pharmacol.2014;58(4):416–422.
36. Mehrzadi S, Bahrami N, Mehrabani M, Motevalian M, Mansouri E, Goudarzi M. Ellagic acid: A promising protective remedy against testicular toxicity induced by arsenic. Biomed Pharmacother Biomedecine Pharmacother.2018;103:1464–1472. doi: 10.1016/j.biopha.2018.04.194.
37. Guvvala PR, Ravindra JP, Selvaraju S, Arangasamy A, Venkata KM. Ellagic and ferulic acids protect arsenic-induced male reproductive toxicity via regulating Nfe2l2, Ppargc1a and StAR expressions in testis. Toxicology.2019;413:1–12. doi: 10.1016/j.tox.2018.11.012.
38. Bucak MN, Bodu M, Başpınar N, Güngör Ş, İli P, Acibaeva B, et al. Influence of Ellagic Acid and Ebselen on Sperm and Oxidative Stress Parameters during Liquid Preservation of Ram Semen. Cell J. 2019;21(1):7–13. doi:10.22074/cellj.2019.5593.
39. Najafi A, Taheri RA, Mehdipour M, Martínez-Pastor F, Rouhollahi AA, Nourani MR. Improvement of post-thawed sperm quality in broiler breeder roosters by ellagic acid-loaded liposomes. Poult Sci. 2019;98(1):440–446. doi: 10.3382/ps/pey353.
40. Mehdipour M, Daghigh Kia H, Nazari M, Najafi A. Effect of lecithin nanoliposome or soybean lecithin supplemented by pomegranate extract on post-thaw flow cytometric, microscopic and oxidative parameters in ram semen. Cryobiology.2017; 78:34–40. doi:10.1016/j.cryobiol.2017.07.005.
41. Kilic I, Yeşiloğlu Y, Bayrak Y. Spectroscopic studies on the antioxidant activity of ellagic acid. Spectrochim Acta A Mol Biomol Spectrosc. 2014;130:447–452. doi:10.1016/j.saa.2014.04.052.
42. Dalvi LT, Moreira DC, Andrade R, Ginani J, Alonso A, Hermes-Lima M. Ellagic acid inhibits iron-mediated free radical formation. Spectrochim Acta A Mol Biomol Spectrosc. 2017;173:910–917. doi: 10.1016/j.saa.2016.10.034.