Potential role of green tea catechins in the management of oxidative stress-associated infertility

Reproductive BioMedicine Online

Volumn 34, Issue 5, 2017, Pages 487-498

  Roychoudhury, Shubhadeep ^a,b   Agarwal, Ashok ^a   Virk, Gurpriya ^a   Cho, Chak Lam ^c  

^a LERNER RESEARCH INSTITUTE   (United States)

^b ASSAM UNIVERSITY   (India)

^c KWONG WAH HOSPITAL   (Hong Kong)

Author keywords

Epigallocatechin 3 gallate (GCG); fertility; green tea catechins; oxidative stress; reactive oxygen species (ROS); reproduction

Indexed keywords

ANTIOXIDANT; CATECHIN; EPICATECHIN; EPIGALLOCATECHIN; EPIGALLOCATECHIN GALLATE; GREEN TEA CATECHIN; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

ANTIOXIDANT ACTIVITY; DRUG BIOAVAILABILITY; EMBRYO DEVELOPMENT; FEMALE INFERTILITY; HUMAN; MALE INFERTILITY; OOCYTE MATURATION; OXIDATIVE STRESS; REPRODUCTIVE HEALTH; REVIEW; SPERMATOZOON MOTILITY; TEA; CHEMISTRY; DRUG EFFECTS; FEMALE; MALE; METABOLISM;

CATECHIN; FEMALE; HUMANS; INFERTILITY, FEMALE; INFERTILITY, MALE; MALE; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; TEA;

EID: 85014744862     PISSN: 14726483     EISSN: 14726491     Source Type: Journal    
DOI: 10.1016/j.rbmo.2017.02.006     Document Type: Review

References (145)

1. Abshenas, J., Babaei, H., Zare, M.-H., Allahbakhshi, A., Sharififar, F., The effects of green tea (Camellia sinensis) extract on mouse semen quality after scrotal heat stress. Vet. Res. Forum, 2012, 242–247.
2. Agarwal, A., Said, T.M., Carnitines and male infertility. Reprod. Biomed. Online 8 (2004), 376–384.
3. Agarwal, A., Allamaneni, S.S., Nallella, K.P., George, A.T., Mascha, E., Correlation of reactive oxygen species levels with the fertilization rate after in vitro fertilization: a qualified meta-analysis. Fertil. Steril 84 (2005), 228–231.
4. Agarwal, A., Gupta, S., Abdel-Razek, H., Krajcir, N., Athayde, K., Impact of oxidative stress on gametes and embryos in an ART laboratory. Clin. Embryol 9 (2006), 5–22.
5. Agarwal, A., Said, T.M., Bedaiwy, M.A., Banerjee, J., Alvarez, J.G., Oxidative stress in an assisted reproductive techniques setting. Fertil. Steril 86 (2006), 503–512.
6. Agarwal, A., Gupta, S., Sekhon, L., Shah, R., Redox considerations in female reproductive function and assisted reproduction: from molecular mechanisms to health implications. Antioxid. Redox Signal 10 (2008), 1375–1404.
7. Aitken, R.J., Paterson, M., Fisher, H., Buckingham, D.W., Van Duin, M., Redox regulation of tyrosine phosphorylation in human spermatozoa and its role in the control of human sperm function. J. Cell Sci 108:Pt 5 (1995), 2017–2025.
8. Askoxylaki, M., Siristatidis, C., Chrelias, C., Vogiatzi, P., Creatsa, M., Salamalekis, G., Vrantza, T., Vrachnis, N., Kassanos, D., Reactive oxygen species in the follicular fluid of subfertile women undergoing in vitro fertilization: a short narrative review. J. Endocrinol. Invest 36 (2013), 1117–1120.
9. Awoniyi, D.O., Aboua, Y.G., Marnewick, J., Brooks, N., The effects of Rooibos (Aspalathus linearis), Green tea (Camellia sinensis) and commercial Rooibos and Green tea supplements on epididymal sperm in oxidative stress-induced rats. Phytother. Res 26 (2012), 1231–1239.
10. Azam, S., Hadi, N., Khan, N.U., Hadi, S.M., Prooxidant property of green tea polyphenols epicatechin and epigallocatechin-3-gallate: implications for anticancer properties. Toxicol. In Vitro 18 (2004), 555–561.
11. Aziz, N., Saleh, R.A., Sharma, R.K., Lewis-Jones, I., Esfandiari, N., Thomas, A.J. Jr., Agarwal, A., Novel association between sperm reactive oxygen species production, sperm morphological defects, and the sperm deformity index. Fertil. Steril 81 (2004), 349–354.
12. Balentine, D.A., Wiseman, S.A., Bouwens, L.C., The chemistry of tea flavonoids. Crit. Rev. Food Sci. Nutr 37 (1997), 693–704.
13. Bansal, A.K., Bilaspuri, G.S., Impacts of oxidative stress and antioxidants on semen functions. Vet. Med. Int, 2010, 2010, 10.4061/2011/686137.
14. Barakat, I.A., Al-Himaidi, A.R., Rady, A.M., Antioxidant effect of green tea leaves extract on in vitro production of sheep embryos. Pak. J. Zool 46 (2014), 167–175.
15. Basu, A., Lucas, E.A., Mechanisms and effects of green tea on cardiovascular health. Nutr. Rev 65 (2007), 361–375.
16. Beecher, G.R., Warden, B.A., Merken, H., Analysis of tea polyphenols. Exp. Biol. Med 220 (1999), 267–270.
17. Behrman, H.R., Kodaman, P.H., Preston, S.L., Gao, S., Oxidative stress and the ovary. J. Soc. Gynecol. Investig 8 (2001), S40–S42.
18. Blondin, P., Guilbault, L.A., Sirard, M.A., The time interval between FSH-P administration and slaughter can influence the developmental competence of beef heifer oocytes. Theriogenology 48 (1997), 803–813.
19. Bokuchava, M.A., Skobeleva, N.I., The biochemistry and technology of tea manufacture. Crit. Rev. Food Sci. Nutr 12 (1980), 303–370.
20. Bose, M., Hao, X., Ju, J., Husain, A., Park, S., Lambert, J.D., Yang, C.S., Inhibition of tumorigenesis in Apc Min/+ mice by a combination of (–)-epigallocatechin-3-gallate and fish oil. J. Agric. Food Chem 55 (2007), 7695–7700.
21. Cabrera, C., Giménez, R., López, M.C., Determination of tea components with antioxidant activity. J. Agric. Food Chem 51 (2003), 4427–4435.
22. Cabrera, C., Artacho, R., Gimenez, R., Beneficial effects of green tea–a review. J. Am. Coll. Nutr 25 (2006), 79–99.
23. Camlin, N.J., Sobinoff, A.P., Sutherland, J.M., Beckett, E.L., Jarnicki, A.G., Vanders, R.L., Hansbro, P.M., Mclaughlin, E.A., Holt, J.E., Maternal smoke exposure impairs the long-term fertility of female offspring in a murine model. Biol. Reprod, 94, 2016, 39.
24. Cao, H., Hininger-Favier, I., Kelly, M.A., Benaraba, R., Dawson, H.D., Coves, S., Roussel, A.M., Anderson, R.A., Green tea polyphenol extract regulates the expression of genes involved in glucose uptake and insulin signaling in rats fed a high fructose diet. J. Agric. Food Chem 55 (2007), 6372–6378.
25. Cengiz, H., Dagdeviren, H., Kanawati, A., Suzen Çaypinar, S., Yesil, A., Ekin, M., Yasar, L., Ischemia-modified albumin as an oxidative stress biomarker in early pregnancy loss. J. Matern. Fetal. Neonatal. Med 29 (2016), 1754–1757.
26. Chandra, A.K., Choudhury, S.R., De, N., Sarkar, M., Effect of green tea (Camellia sinensis L.) extract on morphological and functional changes in adult male gonads of albino rats. Indian J. Exp. Biol 49 (2011), 689–697.
27. Chen, D., Green Tea Polyphenols Prevent Parkinson's Disease: In Vitro and In Vivo Studies. Graduate Theses Dissertation. 2013, Iowa State University, 1–136.
28. Chen, S., Osaki, N., Shimotoyodome, A., Green tea catechins enhance norepinephrine-induced lipolysis via a protein kinase A-dependent pathway in adipocytes. Biochem. Biophys. Res. Commun 461 (2015), 1–7.
29. Chow, H.H., Cai, Y., Hakim, I.A., Crowell, J.A., Shahi, F., Brooks, C.A., Dorr, R.T., Hara, Y., Alberts, D.S., Pharmacokinetics and safety of green tea polyphenols after multiple-dose administration of epigallocatechin gallate and polyphenon E in healthy individuals. Clin. Cancer Res 9 (2003), 3312–3319.
30. Chow, H.H., Hakim, I.A., Vining, D.R., Crowell, J.A., Cordova, C.A., Chew, W.M., Xu, M.J., Hsu, C.H., Ranger-Moore, J., Alberts, D.S., Effects of repeated green tea catechin administration on human cytochrome P450 activity. Cancer Epidemiol. Biomarkers Prev 15 (2006), 2473–2476.
31. Cia, D., Jacquemot, N., Vergnaud, J., Doly, M., Protective effects of epigallocatechin gallate (EGCG) against oxidative stress in cultured retinal pigment epithelial cells. Invest. Ophthalmol. Vis. Sci, 52, 2011, 4437.
32. Cocuzza, L., Sikka, S.C., Athayde, K.S., Agarwal, A., Clinical relevance of oxidative stress and sperm chromatin damage in male infertility: an evidence based analysis. Int. Braz. J. Urol 33 (2007), 603–621.
33. Coimbra, S., Castro, E., Rocha-Pereira, P., Rebelo, I., Rocha, S., Santos-Silva, A., The effect of green tea in oxidative stress. Clin. Nutr 25 (2006), 790–796.
34. de Castro, L.S., De Assis, P.M., Siqueira, A.F., Hamilton, T.R., Mendes, C.M., Losano, J.D., Nichi, M., Visintin, J.A., Assumpcao, M.E., Sperm oxidative stress is detrimental to embryo development: a dose-dependent study model and a new and more sensitive oxidative status evaluation. Oxid. Med. Cell. Longev, 2016, 2016, 8213071.
35. de Lamirande, E., Gagnon, C., Human sperm hyperactivation and capacitation as parts of an oxidative process. Free Radic. Biol. Med 14 (1993), 157–166.
36. Dada, R., Mahfouz, R.Z., Kumar, R., Venkatesh, S., Shamsi, M.B., Agarwal, A., Talwar, P., Sharma, R.K., A comprehensive work up for an asthenozoospermic man with repeated intracytoplasmic sperm injection (ICSI) failure. Andrologia 43 (2011), 368–372.
37. Daglar, K., Biberoglu, E., Kirbas, A., Dirican, A.O., Genc, M., Avci, A., Biberoglu, K., The cellular immunity and oxidative stress markers in early pregnancy loss. J. Matern. Fetal. Neonatal. Med 29 (2016), 1840–1843.
38. Das, S.K., Karmakar, S.N., Effect of green tea (Camelia sinensis L.) leaf extract on reproductive system of adult male albino rats. Int. J. Physiol. Pathophysiol. Pharmacol 7 (2015), 178–184.
39. De Amicis, F., Santoro, M., Guido, C., Russo, A., Aquila, S., Epigallocatechin gallate affects survival and metabolism of human sperm. Mol. Nutr. Food Res 56 (2012), 1655–1664.
40. Del Rio, D., Calani, L., Cordero, C., Salvatore, S., Pellegrini, N., Brighenti, F., Bioavailability and catabolism of green tea flavan-3-ols in humans. Nutrition 26 (2010), 1110–1116.
41. Ding, J., Wang, H., Wu, Z.-B., Zhao, J., Zhang, S., Li, W., Protection of murine spermatogenesis against ionizing radiation-induced testicular injury by a green tea polyphenol. Biol. Reprod, 114, 2015, 122333.
42. Elbling, L., Weiss, R.-M., Teufelhofer, O., Uhl, M., Knasmueller, S., Schulte-Hermann, R., Berger, W., Micksche, M., Green tea extract and (–)-epigallocatechin-3-gallate, the major tea catechin, exert oxidant but lack antioxidant activities. FASEB J. 19 (2005), 807–809.
43. Esfandiari, N., Falcone, T., Agarwal, A., Attaran, M., Nelson, D.R., Sharma, R.K., Protein supplementation and the incidence of apoptosis and oxidative stress in mouse embryos. Obstet. Gynecol 105 (2005), 653–660.
44. Fang, M.Z., Wang, Y., Ai, N., Hou, Z., Sun, Y., Lu, H., Welsh, W., Yang, C.S., Tea polyphenol (−)-epigallocatechin-3-gallate inhibits DNA methyltransferase and reactivates methylation-silenced genes in cancer cell lines. Cancer Res 63 (2003), 7563–7570.
45. Fraga, C.G., Oteiza, P.I., Dietary flavonoids: role of (−)-epicatechin and related procyanidins in cell signaling. Free Radic. Biol. Med 51 (2011), 813–823.
46. Gale, I., Gil, L., Malo, C., González, N., Martínez, F., Effect of Camellia sinensis supplementation and increasing holding time on quality of cryopreserved boar semen. Andrologia 47 (2015), 505–512.
47. Galleano, M., Verstraeten, S.V., Oteiza, P.I., Fraga, C.G., Antioxidant actions of flavonoids: thermodynamic and kinetic analysis. Arch. Biochem. Biophys 501 (2010), 23–30.
48. Garcia-Cortes, M., Robles-Diaz, M., Ortega-Alonso, A., Medina-Caliz, I., Andrade, R.J., Hepatotoxicity by dietary supplements: a tabular listing and clinical characteristics. Int. J. Mol. Sci, 17, 2016 pii: E537.
49. González-Fernández, R., Hernandez, J., Martin-Vasallo, P., Puopolo, M., Palumbo, A., Avila, J., Expression levels of the oxidative stress response gene ALDH3A2 in granulosa-lutein cells are related to female age and infertility diagnosis. Reprod. Sci 23 (2016), 604–609.
50. Graham, H.N., Green tea composition, consumption, and polyphenol chemistry. Prev. Med 21 (1992), 334–350.
51. Guerin, P., El Mouatassim, S., Menezo, Y., Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum. Reprod. Update 7 (2001), 175–189.
52. Gupta, J., Siddique, Y., Beg, T., Ara, G., Afzal, M., A review on the beneficial effects of tea polyphenols on human health. Int. J. Pharmacol 4 (2008), 314–338.
53. Guthrie, H.D., Welch, G.R., Effects of reactive oxygen species on sperm function. Theriogenology 78 (2012), 1700–1708.
54. Hampl, R., Drábková, P., Kand'ár, R., Stěpán, J., [Impact of oxidative stress on male infertility]. Ceska Gynekol 77 (2012), 241–245.
55. Hara, Y., Physiological functions of tea polyphenols: part 2. Am. Biotechnol. Lab, 12, 1994, 18.
56. Harvey, A.J., Kind, K.L., Thompson, J.G., REDOX regulation of early embryo development. Reproduction 123 (2002), 479–486.
57. Henning, S.M., Fajardo-Lira, C., Lee, H.W., Youssefian, A.A., Go, V.L.W., Heber, D., Catechin content of 18 teas and a green tea extract supplement correlates with the antioxidant capacity. Nutr. Cancer 45 (2003), 226–235.
58. Henning, S.M., Niu, Y., Liu, Y., Lee, N.H., Hara, Y., Thames, G.D., Minutti, R.R., Carpenter, C.L., Wang, H., Heber, D., Bioavailability and antioxidant effect of epigallocatechin gallate administered in purified form versus as green tea extract in healthy individuals. J. Nutr. Biochem 16 (2005), 610–616.
59. Hijazi, M.M., Khatoon, N., Azmi, M.A., Rajput, M.T., Zaidi, S.I., Azmi, M.A., Perveen, R., Naqvi, S.N., Rashid, M., Report: effects of Camellia sinensis L. (green tea) extract on the body and testicular weight changes in adult Wistar rate. Pak. J. Pharm. Sci 28 (2015), 249–253.
60. Hong, J., Lambert, J.D., Lee, S.H., Sinko, P.J., Yang, C.S., Involvement of multidrug resistance-associated proteins in regulating cellular levels of (-)-epigallocatechin-3-gallate and its methyl metabolites. Biochem. Biophys. Res. Commun 310 (2003), 222–227.
61. Hyung, S.-J., Detoma, A.S., Brender, J.R., Lee, S., Vivekanandan, S., Kochi, A., Choi, J.-S., Ramamoorthy, A., Ruotolo, B.T., Lim, M.H., Insights into antiamyloidogenic properties of the green tea extract (−)-epigallocatechin-3-gallate toward metal-associated amyloid-β species. Proc. Natl. Acad. Sci. U.S.A. 110 (2013), 3743–3748.
62. Isbrucker, R.A., Edwards, J.A., Wolz, E., Davidovich, A., Bausch, J., Safety studies on epigallocatechin gallate (EGCG) preparations. Part 3: teratogenicity and reproductive toxicity studies in rats. Food Chem. Toxicol 44 (2006), 651–661.
63. Isozaki, T., Tamura, H., Epigallocatechin gallate (EGCG) inhibits the sulfation of 1-naphthol in a human colon carcinoma cell line, Caco-2. Biol. Pharm. Bull 24 (2001), 1076–1078.
64. Jaganathan, S.K., Mandal, M., Involvement of non-protein thiols, mitochondrial dysfunction, reactive oxygen species and p53 in honey-induced apoptosis. Invest. New Drugs 28 (2010), 624–633.
65. Jana, S.K., Babu, N., Chattopadhyay, R., Chakravarty, B., Chaudhury, K., Upper control limit of reactive oxygen species in follicular fluid beyond which viable embryo formation is not favorable. Reprod. Toxicol 29 (2010), 447–451.
66. Jung, H.A., Jung, M.J., Kim, J.Y., Chung, H.Y., Choi, J.S., Inhibitory activity of flavonoids from Prunus davidiana and other flavonoids on total ROS and hydroxyl radical generation. Arch. Pharm. Res 26 (2003), 809–815.
67. Katiyar, S.K., Raman, C., Green tea: a new option for the prevention or control of osteoarthritis. Arthritis Res. Ther, 13, 2011, 121.
68. Kim, H.S., Kim, M.H., Jeong, M., Hwang, Y.S., Lim, S.H., Shin, B.A., Ahn, B.W., Jung, Y.D., EGCG blocks tumor promoter-induced MMP-9 expression via suppression of MAPK and AP-1 activation in human gastric AGS cells. Anticancer Res 24 (2004), 747–754.
69. Kim, H.S., Quon, M.J., Kim, J.A., New insights into the mechanisms of polyphenols beyond antioxidant properties; lessons from the green tea polyphenol, epigallocatechin 3-gallate. Redox Biol 2 (2014), 187–195.
70. Kim, J.-A., Mechanisms underlying beneficial health effects of tea catechins to improve insulin resistance and endothelial dysfunction. Endocr. Metab. Immune Disord. Drug Targets 8 (2008), 82–88.
71. Kim, J.E., Shin, M.H., Chung, J.H., Epigallocatechin-3-gallate prevents heat shock-induced MMP-1 expression by inhibiting AP-1 activity in human dermal fibroblasts. Arch. Dermatol. Res 305 (2013), 595–602.
72. Konishi, Y., Kobayashi, S., Shimizu, M., Tea polyphenols inhibit the transport of dietary phenolic acids mediated by the monocarboxylic acid transporter (MCT) in intestinal Caco-2 cell monolayers. J. Agric. Food Chem 51 (2003), 7296–7302.
73. Kothari, S., Thompson, A., Agarwal, A., Du Plessis, S.S., Free radicals: their beneficial and detrimental effects on sperm function. Indian J. Exp. Biol 48 (2010), 425–435.
74. Kwiecien, S., Jasnos, K., Magierowski, M., Sliwowski, Z., Pajdo, R., Brzozowski, B., Mach, T., Wojcik, D., Brzozowski, T., Lipid peroxidation, reactive oxygen species and antioxidative factors in the pathogenesis of gastric mucosal lesions and mechanism of protection against oxidative stress-induced gastric injury. J. Physiol. Pharmacol 65 (2014), 613–622.
75. Lackner, J.E., Agarwal, A., Mahfouz, R., Du Plessis, S.S., Schatzl, G., The association between leukocytes and sperm quality is concentration dependent. Reprod. Biol. Endocrinol, 8, 2010, 12.
76. Laschke, M.W., Schwender, C., Scheuer, C., Vollmar, B., Menger, M.D., Epigallocatechin-3-gallate inhibits estrogen-induced activation of endometrial cells in vitro and causes regression of endometriotic lesions in vivo. Hum. Reprod 23 (2008), 2308–2318.
77. Li, M.J., Yin, Y.C., Wang, J., Jiang, Y.F., Green tea compounds in breast cancer prevention and treatment. World J. Clin. Oncol 5 (2014), 520–528.
78. Li, Y., Zhang, C., Gao, Y., Zhang, Y., Sui, L., Zhang, X., Zhang, Y., Effect of epigallocatechin-3-gallate on the in vitro developmental potential of porcine oocytes and embryos obtained parthenogenetically and by somatic cell nuclear transfer. Ital. J. Anim. Sci, 13, 2014.
79. Lombardo, F., Fiducia, M., Lunghi, R., Marchetti, L., Palumbo, A., Rizzo, F., Koverech, A., Lenzi, A., Gandini, L., Effects of a dietary supplement on chronic pelvic pain syndrome (Category IIIA), leucocytospermia and semen parameters. Andrologia 44 (2012), 672–678.
80. Luderer, U., Ovarian toxicity from reactive oxygen species. Vitam. Horm 94 (2014), 99–127.
81. Mahfouz, R., Sharma, R., Thiyagarajan, A., Kale, V., Gupta, S., Sabanegh, E., Agarwal, A., Semen characteristics and sperm DNA fragmentation in infertile men with low and high levels of seminal reactive oxygen species. Fertil. Steril 94 (2010), 2141–2146.
82. Mandel, S.A., Amit, T., Kalfon, L., Reznichenko, L., Weinreb, O., Youdim, M.B., Cell signaling pathways and iron chelation in the neurorestorative activity of green tea polyphenols: special reference to epigallocatechin gallate (EGCG). J. Alzheimers Dis 15 (2008), 211–222.
83. Manohar, M., Fatima, I., Saxena, R., Chandra, V., Sankhwar, P.L., Dwivedi, A., (−)-Epigallocatechin-3-gallate induces apoptosis in human endometrial adenocarcinoma cells via ROS generation and p38 MAP kinase activation. J. Nutr. Biochem 24 (2013), 940–947.
84. Matsuzaki, S., Darcha, C., Antifibrotic properties of epigallocatechin-3-gallate in endometriosis. Hum. Reprod 29 (2014), 1677–1687.
85. Mazzanti, G., Di Sotto, A., Vitalone, A., Hepatotoxicity of green tea: an update. Arch. Toxicol 89 (2015), 1175–1191.
86. Nakagawa, T., Yokozawa, T., Sano, M., Takeuchi, S., Kim, M., Minamoto, S., Activity of (-)-epigallocatechin 3-O-gallate against oxidative stress in rats with adenine-induced renal failure. J. Agric. Food Chem 52 (2004), 2103–2107.
87. Naumovski, N., Blades, B.L., Roach, P.D., Food inhibits the oral bioavailability of the major green tea antioxidant epigallocatechin gallate in humans. Antioxidants (Basel) 4 (2015), 373–393.
88. Nguyen, M.M., Ahmann, F.R., Nagle, R.B., Hsu, C.H., Tangrea, J.A., Parnes, H.L., Sokoloff, M.H., Gretzer, M.B., Chow, H.H., Randomized, double-blind, placebo-controlled trial of polyphenon E in prostate cancer patients before prostatectomy: evaluation of potential chemopreventive activities. Cancer Prev. Res. (Phila.) 5 (2012), 290–298.
89. Nozaki, A., Hori, M., Kimura, T., Ito, H., Hatano, T., Interaction of polyphenols with proteins: binding of (-)-epigallocatechin gallate to serum albumin, estimated by induced circular dichroism. Chem. Pharm. Bull 57 (2009), 224–228.
90. Oliva, J., Bardag-Gorce, F., Tillman, B., French, S.W., Protective effect of quercetin, EGCG, catechin and betaine against oxidative stress induced by ethanol in vitro. Exp. Mol. Pathol 90 (2011), 295–299.
91. Oyawoye, O., Abdel Gadir, A., Garner, A., Constantinovici, N., Perrett, C., Hardiman, P., Antioxidants and reactive oxygen species in follicular fluid of women undergoing IVF: relationship to outcome. Hum. Reprod 18 (2003), 2270–2274.
92. Pahune, P.P., Choudhari, A.R., Muley, P.A., The total antioxidant power of semen and its correlation with the fertility potential of human male subjects. J. Clin. Diagn. Res 7 (2013), 991–995.
93. Pan, T., Jankovic, J., Le, W., Potential therapeutic properties of green tea polyphenols in Parkinson's disease. Drugs Aging 20 (2003), 711–721.
94. Park, J.-H., Bae, J.-H., Im, S.-S., Song, D.-K., Green tea and type 2 diabetes. Integr. Med. Res 3 (2014), 4–10.
95. Pasqualotto, F.F., Sharma, R.K., Nelson, D.R., Thomas, A.J., Agarwal, A., Relationship between oxidative stress, semen characteristics, and clinical diagnosis in men undergoing infertility investigation. Fertil. Steril 73 (2000), 459–464.
96. Patel, S.S., Beer, S., Kearney, D.L., Phillips, G., Carter, B.A., Green tea extract: a potential cause of acute liver failure. World J. Gastroenterol 19 (2013), 5174–5177.
97. Perron, N.R., Brumaghim, J.L., A review of the antioxidant mechanisms of polyphenol compounds related to iron binding. Cell Biochem. Biophys 53 (2009), 75–100.
98. Pirker, K.F., Baratto, M.C., Basosi, R., Goodman, B.A., Influence of pH on the speciation of copper (II) in reactions with the green tea polyphenols, epigallocatechin gallate and gallic acid. J. Inorg. Biochem 112 (2012), 10–16.
99. Pisters, K.M.W., Newman, R.A., Coldman, B., Shin, D.M., Khuri, F.R., Hong, W.K., Glisson, B.S., Lee, J.S., Phase I trial of oral green tea extract in adult patients with solid tumors. J. Clin. Oncol 19 (2001), 1830–1838.
100. Rahmani, A.H., Al. Shabrmi, F.M., Allemailem, K.S., Aly, S.M., Khan, M.A., Implications of green tea and its constituents in the prevention of cancer via the modulation of cell signalling pathway. Biomed Res. Int, 2015, 2015, 925640.
101. Reygaert, W.C., The antimicrobial possibilities of green tea. Front. Microbiol, 5, 2014, 434.
102. Ricci, A., Olivares, C., Bilotas, M., Bastón, J., Singla, J., Meresman, G., Barañao, R., Natural therapies assessment for the treatment of endometriosis. Hum. Reprod 28 (2013), 178–188.
103. Roth, Z., Aroyo, A., Yavin, S., Arav, A., The antioxidant epigallocatechin gallate (EGCG) moderates the deleterious effects of maternal hyperthermia on follicle-enclosed oocytes in mice. Theriogenology 70 (2008), 887–897.
104. Roychoudhury, S., Sharma, R., Sikka, S., Agarwal, A., Diagnostic application of total antioxidant capacity in seminal plasma to assess oxidative stress in male factor infertility. J. Assist. Reprod. Genet 2016 (2016), 627–635.
105. Rozeboom, K., Composition for preserving reproductive cells and method of using. Google Patents, 2012.
106. Saalu, L.C., The incriminating role of reactive oxygen species in idiopathic male infertility: an evidence based evaluation. Pak. J. Biol. Sci 13 (2010), 413–422.
107. Sang, S., Cheng, X., Stark, R.E., Rosen, R.T., Yang, C.S., Ho, C.-T., Chemical studies on antioxidant mechanism of tea catechins: analysis of radical reaction products of catechin and epicatechin with 2, 2-diphenyl-1-picrylhydrazyl. Bioorg. Med. Chem 10 (2002), 2233–2237.
108. Sang, S., Hou, Z., Lambert, J.D., Yang, C.S., Redox properties of tea polyphenols and related biological activities. Antioxid. Redox Signal 7 (2005), 1704–1714.
109. Sang, S., Lee, M.J., Yang, I., Buckley, B., Yang, C.S., Human urinary metabolite profile of tea polyphenols analyzed by liquid chromatography/electrospray ionization tandem mass spectrometry with data-dependent acquisition. Rapid Commun. Mass Spectrom 22 (2008), 1567–1578.
110. Sato, K., Sueoka, K., Tanigaki, R., Tajima, H., Nakabayashi, A., Yoshimura, Y., Hosoi, Y., Green tea extracts attenuate doxorubicin-induced spermatogenic disorders in conjunction with higher telomerase activity in mice. J. Assist. Reprod. Genet 27 (2010), 501–508.
111. Schramm, L., Going green: the role of the green tea component EGCG in chemoprevention. J. Carcinog. Mutagen, 4, 2013, 1000142.
112. Severino, J.F., Goodman, B.A., Kay, C.W., Stolze, K., Tunega, D., Reichenauer, T.G., Pirker, K.F., Free radicals generated during oxidation of green tea polyphenols: electron paramagnetic resonance spectroscopy combined with density functional theory calculations. Free Radic. Biol. Med 46 (2009), 1076–1088.
113. Shapiro, H., Lev, S., Cohen, J., Singer, P., Polyphenols in the prevention and treatment of sepsis syndromes: rationale and pre-clinical evidence. Nutrition 25 (2009), 981–997.
114. Sheldon, R., Kochi, J.K., Metal-catalyzed Oxidations of Organic Compounds. Mechanistic Principles and Synthetic Methodology including Biochemical Processes. 2016, Academic Press, Elsevier, 424.
115. Shi, X., Ye, J., Leonard, S., Ding, M., Vallyathan, V., Castranova, V., Rojanasakul, Y., Dong, Z., Antioxidant properties of (-)-epicatechin-3-gallate and its inhibition of Cr (VI)-induced DNA damage and Cr (IV)-or TPA-stimulated NF-κB activation. Mol. Cell. Biochem 206 (2000), 125–132.
116. Shiota, S., Shimizu, M., Mizushima, T., Ito, H., Hatano, T., Yoshida, T., Tsuchiya, T., Marked reduction in the minimum inhibitory concentration (MIC) of. BETA.-lactams in methicillin-resistant staphylococcus aureus produced by epicatechin gallate, an ingredient of green tea (Camellia sinensis). Biol. Pharm. Bull 22 (1999), 1388–1390.
117. Simbula, G., Columbano, A., Ledda-Columbano, G., Sanna, L., Deidda, M., Diana, A., Pibiri, M., Increased ROS generation and p53 activation in α-lipoic acid-induced apoptosis of hepatoma cells. Apoptosis 12 (2007), 113–123.
118. Siristatidis, C., Askoxylaki, M., Varounis, C., Kassanos, D., Chrelias, C., E-selectin, resistin and reactive oxygen species levels in GnRH-agonist and-antagonist protocols in IVF/ICSI: a prospective cohort study. J. Assist. Reprod. Genet 32 (2015), 959–967.
119. Sirk, T.W., Brown, E.F., Friedman, M., Sum, A.K., Molecular binding of catechins to biomembranes: relationship to biological activity. J. Agric. Food Chem 57 (2009), 6720–6728.
120. Someya, S., Yoshiki, Y., Okubo, K., Antioxidant compounds from bananas (Musa Cavendish). Food Chem 79 (2002), 351–354.
121. Spinaci, M., Volpe, S., De Ambrogi, M., Tamanini, C., Galeati, G., Effects of epigallocatechin-3-gallate (EGCG) on in vitro maturation and fertilization of porcine oocytes. Theriogenology 69 (2008), 877–885.
122. Suh, K.S., Chon, S., Oh, S., Kim, S.W., Kim, J.-W., Kim, Y.S., Woo, J.-T., Prooxidative effects of green tea polyphenol (−)-epigallocatethin-3-gallate on the HIT-T15 pancreatic beta cell line. Cell Biol. Toxicol 26 (2010), 189–199.
123. Tamura, H., Matsui, M., Inhibitory effects of green tea and grape juice on the phenol sulfotransferase activity of mouse intestines and human colon carcinoma cell line, Caco-2. Biol. Pharm. Bull 23 (2000), 695–699.
124. Uekusa, Y., Kamihira, M., Nakayama, T., Dynamic behavior of tea catechins interacting with lipid membranes as determined by NMR spectroscopy. J. Agric. Food Chem 55 (2007), 9986–9992.
125. Ullmann, U., Haller, J., Decourt, J.D., Girault, J., Spitzer, V., Weber, P., Plasma-kinetic characteristics of purified and isolated green tea catechin epigallocatechin gallate (EGCG) after 10 days repeated dosing in healthy volunteers. Int. J. Vitam. Nutr. Res 74 (2004), 269–278.
126. Vahedi, V., Zeinoaldini, S., Kohram, H., Farahavar, A., Retinoic acid effects on nuclear maturation of bovine oocytes in vitro. Afr. J. Biotechnol, 8, 2009.
127. Valcic, S., Burr, J.A., Timmermann, B.N., Liebler, D.C., Antioxidant chemistry of green tea catechins. New oxidation products of (-)-epigallocatechin gallate and (-)-epigallocatechin from their reactions with peroxyl radicals. Chem. Res. Toxicol 13 (2000), 801–810.
128. Van Acker, S.A., Tromp, M.N., Griffioen, D.H., Van Bennekom, W.P., Van Der Vijgh, W.J., Bast, A., Structural aspects of antioxidant activity of flavonoids. Free Radic. Biol. Med 20 (1996), 331–342.
129. Vergote, D., Cren-Olivé, C., Chopin, V., Toillon, R.-A., Rolando, C., Hondermarck, H., Le Bourhis, X., (−)-Epigallocatechin (EGC) of green tea induces apoptosis of human breast cancer cells but not of their normal counterparts. Breast Cancer Res. Treat 76 (2002), 195–201.
130. Vittal, R., Selvanayagam, Z.E., Sun, Y., Hong, J., Liu, F., Chin, K.-V., Yang, C.S., Gene expression changes induced by green tea polyphenol (−)-epigallocatechin-3-gallate in human bronchial epithelial 21BES cells analyzed by DNA microarray. Mol. Cancer Ther 3 (2004), 1091–1099.
131. Wang, T.-Y., Li, Q., Li, Q., Li, H., Zhu, J., Cui, W., Jiao, G.-Z., Tan, J.-H., Non-frozen preservation protocols for mature mouse oocytes dramatically extend their developmental competence by reducing oxidative stress. Mol. Hum. Reprod 20 (2014), 318–329.
132. Wang, Z.-G., Yu, S.-D., Xu, Z.-R., Improvement in bovine embryo production in vitro by treatment with green tea polyphenols during in vitro maturation of oocytes. Anim. Reprod. Sci 100 (2007), 22–31.
133. Warden, B.A., Smith, L.S., Beecher, G.R., Balentine, D.A., Clevidence, B.A., Catechins are bioavailable in men and women drinking black tea throughout the day. J. Nutr 131 (2001), 1731–1737.
134. Williams, A.C., Ford, W.L., Relationship between ROS production and lipid peroxidation in human sperm suspensions and their association with sperm function. Fertil. Steril 83 (2005), 929–937.
135. Wittayarat, M., Ito, A., Kimura, T., Namula, Z., Luu, V.V., Do, L.T.K., Sato, Y., Taniguchi, M., Otoi, T., Effects of green tea polyphenol on the quality of canine semen after long-term storage at 5 C. Reprod. Biol 13 (2013), 251–254.
136. Wright, C., Milne, S., Leeson, H., Sperm DNA damage caused by oxidative stress: modifiable clinical, lifestyle and nutritional factors in male infertility. Reprod. Biomed. Online 28 (2014), 684–703.
137. Xu, H., Lui, W., Chu, C., Ng, P., Wang, C., Rogers, M., Anti-angiogenic effects of green tea catechin on an experimental endometriosis mouse model. Hum. Reprod 24 (2009), 608–618.
138. Xu, H., Becker, C.M., Lui, W.T., Chu, C.Y., Davis, T.N., Kung, A.L., Birsner, A.E., D'amato, R.J., Man, G.C.W., Wang, C.C., Green tea epigallocatechin-3-gallate inhibits angiogenesis and suppresses vascular endothelial growth factor C/vascular endothelial growth factor receptor 2 expression and signaling in experimental endometriosis in vivo. Fertil. Steril 96 (2011), 1021–1028 e1.
139. Yang, C.S., Chen, L., Lee, M.J., Balentine, D., Kuo, M.C., Schantz, S.P., Blood and urine levels of tea catechins after ingestion of different amounts of green tea by human volunteers. Cancer Epidemiol. Biomarkers Prev 7 (1998), 351–354.
140. Yang, C.S., Lambert, J.D., Sang, S., Antioxidative and anti-carcinogenic activities of tea polyphenols. Arch. Toxicol 83 (2009), 11–21.
141. Yang, G.-Z., Wang, Z.-J., Bai, F., Qin, X.-J., Cao, J., Lv, J.-Y., Zhang, M.-S., Epigallocatechin-3-gallate protects HUVECs from PM2. 5-induced oxidative stress injury by activating critical antioxidant pathways. Molecules 20 (2015), 6626–6639.
142. Yassa, H.A., George, S.M., Refaiy Ael, R., Moneim, E.M., Camellia sinensis (green tea) extract attenuate acrylamide induced testicular damage in albino rats. Environ. Toxicol 29 (2014), 1155–1161.
143. Yavari, M., Naoi, H., Kaedei, Y., Tanihara, F., Namula, Z., Viet, V.L., Otoi, T., Effects of epigallocatechin-3-gallate (EGCG) on the developmental competence of parthenogenetic embryos in pig. Ital. J. Anim. Sci, 9, 2010, 73.
144. Zanchi, M.M., Manfredini, V., Dos Santos Brum, D., Vargas, L.M., Spiazzi, C.C., Soares, M.B., Izaguirry, A.P., Santos, F.W., Green tea infusion improves cyclophosphamide-induced damage on male mice reproductive system. Toxicol. Rep 2 (2015), 252–260.
145. Zhu, N., Huang, T.-C., Yu, Y., Lavoie, E.J., Yang, C.S., Ho, C.-T., Identification of oxidation products of (-)-epigallocatechin gallate and (-)-epigallocatechin with H2O2. J. Agric. Food Chem 48 (2000), 979–981.