تأثیر تمرین هوازی و کاندیشن مدیای سلولهای سرتولی بر وضعیت آنتیاکسیدانی و هیستومورفومتری در آسیب بیضه ناشی از مصرف کافئین در موشهای صحرایی نر بالغ
محورهای موضوعی :
آسیب شناسی درمانگاهی دامپزشکی
داود رحیمی
1
,
جبار بشیری
2
,
میرعلیرضا نورآذر
3
,
رقیه پوزش جدیدی
4
,
داریوش مهاجری
5
1 - دانشجوی دکترای فیزیولوژی ورزشی، گروه علوم ورزشی، واحد تبریز، دانشگاه آزاد اسلامی، تبریز، ایران.
2 - دانشیار گروه علوم ورزشی، دانشکده علوم انسانی و تربیتی تبریز، دانشگاه آزاد اسلامی، تبریز، ایران.
3 - استادیار گروه علوم پایه، دانشکده دامپزشکی، علوم پزشکی تبریز، دانشگاه آزاد اسلامی، تبریز، ایران.
4 - استادیار گروه علوم ورزشی، دانشکده علوم انسانی و تربیتی تبریز، دانشگاه آزاد اسلامی، تبریز، ایران.
5 - استاد گروه پاتوبیولوژی، دانشکده دامپزشکی، علوم پزشکی تبریز، دانشگاه آزاد اسلامی، تبریز، ایران.
تاریخ دریافت : 1402/02/20
تاریخ پذیرش : 1402/06/01
تاریخ انتشار : 1402/05/01
کلید واژه:
بیضه موش,
کافئین,
وضعیت آنتیاکسیدانی,
تمرین هوازی,
کاندیشن مدیا,
چکیده مقاله :
با توجه به مصرف کافئین به عنوان مکمل مورد اقبال ورزشکاران و اثبات اثرات سوء مصرف طولانیمدت آن بر باروری افراد مذکر، هدف از مطالعه حاضر، تعیین تأثیر تمرین هوازی توأم با کاندیشن مدیای سلولهای سرتولی بر آسیب بیضه ناشی از مصرف کافئین در موشهای صحرایی نر بالغ بود. بدین منظور30 سر موش صحرایی نر بالغ نژاد ویستار به طور تصادفی در 5 گروه برابر مورد آزمون واقع شدند. موش های گروه شاهد فقط آب مقطر و موش های چهار گروه دیگر شامل: گروه های بدون انجام تیمار، تیمار با تمرین هوازی، تیمار با کاندیشن مدیوم و تیمار با تمرین هوازی توأم با کاندیشن مدیا، به مدت 4 هفته کافئین را با دوز mg/kg 200 بهصورت خوراکی دریافت کردند. 42 روز بعد، کاندیشن مدیای سلولهای سرتولی به درون مجاری وابران موشهای گروه های تیمار تزریق شد. پس از 8 هفته، از بیضه موشها نمونه بافتی اخذ شده و مورد مطالعه هیستومورفومتری قرار گرفت. همچنین فعالیت آنزیم های سوپراکسید دیسموتاز (SOD) و گلوتاتیون پراکسیداز (GPX) و مقدار مالون دی آلدئید (MDA) در بافت بیضه و ظرفیت تام آنتیاکسیدانی سرم موش ها مورد سنجش قرار گرفت. در موش های گروه آسیب دیده با کافئین نسبت به گروه سالم، قطر لوله های منیساز، ارتفاع اپیتلیوم مجاری منی ساز و ضخامت بافت بینابینی بیضه و فعالیت آنزیم های SOD و GPX و میزان TAC به طور معنیداری کمتر و مقدار MDA بالاتر بود (01/0>p). همه گروه های آسیب دیده باکافئین توأم با دریافت تیمار، نسبت به گروه آسیبدیده با کافئین دارای مقادیر بالاتری از قطر لوله های منی ساز، ارتفاع اپیتلیوم مجاری منی ساز و ضخامت بافت بینابینی بیضه و فعالیت آنزیم های SOD و GPX و میزان TAC بودند و مقادیر MDA پایینتری داشتند. در گروه تیمارشده با کاندیشن مدیا توام با تمرین هوازی، میزان کاهش و افزایش در پارامترهای ذکرشده، در مقایسه با دو گروه تیماری دیگر، بیشتر بوده و تفاوت آماری معنیداری داشت (05/0>p). نتایج مطالعه نشان داد مصرف کاندیشن مدیای سلولهای سرتولی و انجام همزمان تمرین هوازی، با اثرات همافزایی باعث بهبود شاخصهای دفاع آنتیاکسیدانی و کاهش اثرات مخرب کافئین در بافت بیضه موشهای صحرایی میشود.
چکیده انگلیسی:
Considering the consumption of caffeine as a supplement favored by theathletes and the proof of its long-term abuse effects on male fertility, the purpose of this study was to investigate the effect of moderate aerobic training combined with the conditioning of Sertoli cell media in testicular damage caused by caffeine consumption.For this purpose,30male Wistar rats were tested in5groups.For4weeks, the groups received caffeine at a dose of200 mg/kg orally and group1received of distilled water.42days after that, the conditioned media of Sertoli cells was injected into the efferent ducts of the rats in the treatment group.After8 weeks, mice were sampled.Tissue samples were studied by histomorphometry andSOD,,GPX, TACand MDA.The group under the influence of caffeine compared to the healthy group, significantly(p<0.01).had lower values of seminiferous tubule diameter, epithelium height, interstitial thickness,TAC, SODandGPXand higher values ofMDA. Respectively, the three groups affected by caffeine along with exercise treatment, treatment with media conditioning and exercise along with media conditioning compared to the group affected with caffeine, have higher values of seminiferous tubule diameter, epithelium height, interstitial thickness,TAC, SODandGPX,and MDA values were lower.In the treatment group with media conditioning and exercise, there was a significant difference in the amount of decrease and increase in the mentioned parameters compared to the other two treatment groups (p<0.05).The results of the present study showed that the use of Sertoli cell media conditioning and aerobic exercise at the same time, with synergistic effects, improves the antioxidant defense indices and reduces the harmful effects of caffeine in the testicular tissue of rats..
منابع و مأخذ:
Afzalpour, M.E., Chadorneshin, H.T., Foadoddini, M. and Eivari, H.A. (2015). Comparing interval and continuous exercise training regimens on neurotrophic factors in rat brain. Physiology Behavior, 147(1): 78-83.
Agarwal, A., Ikemotom I. and Loughlin, K.R. (1994). Relationship of sperm parameters with levels of reactive oxygen species in semen specimens. Journal of Urology, 152(1): 107-110.
Aitken, R.J., De Iuliis, G.N., Finnie, J.M., Hedges, A. and McLachlan, R.I. (2010). Analysis of the relationships between oxidative stresses, DNA damage and sperm vitality in a patient population: development of diagnostic criteria. Human Reproduction, 25(10): 2415-2426.
Akomolafe, S.F., Olasehinde, T.A., Ogunsuyi, O.B., Oyeleye, S.I. and Oboh, G. (2019). Revealed that caffeine (5 and 25 mg/kg) improved sperm quality, increased steroidogenic enzyme activities and attenuated oxidative damage in testis and epididymis of rats treated with scopolamine. Journal of Pharmacy and Pharmacology, 71(10): 1565-1575.
Alihemmati, A., Ebadi, F., Moghadaszadeh, M., Asadi, M., Zare, P. and Badalzadeh, R. (2019). Effects of high-intensity interval training on the expression of microRNA-499 and pro-and anti-apoptotic genes in doxorubicin-cardiotoxicity in rats. Journal of Electrocardiology, 55(1): 9-15.
Armstrong, J.S., Rajasekaran, M., Chamulitrat, W., Gatti, P., Hellstrom, W.J. and Sikka, S.C. (1999). Characterization of reactive oxygen species induced effects on human spermatozoa movement and energy metabolism. Free Radical Biology & Medicine 26(7-8): 869-880.
Bassey, R.B., Yama, O.E., Osinubi, A.A., Noronha, C.C. and Okanlawon, A. (2011). Effects of Tahitian Noni dietary supplement on caffeine-induced testicular histo-pathological alterations in adult Sprague-Dawley rats. Middle East Fertility Society Journal, 16(1): 61-66.
Bartosz, G. (2003). Total antioxidant capacity. Advances in Clinical Chemistry, 37(8): 219-229.
Dias, T.R., Alves, M.G., Bernardino, R.L., Martins, A.D., Moreira, A.C., Silva, J., et al. (2015). Dose-dependent effects of caffeine in human Sertoli cells metabolism and oxidative profile: Relevance for male fertility. Toxicology, 328(3): 12-20.
Dorostghoal, M., Majd, N.E. and Nooraei, P. (2012). Maternal caffeine consumption has irreversible effects on reproductive parameters and fertility in male offspring rats. Clinical and Experimental Reproductive Medicine, 39(4): 144-152.
Ekaluo, U., Ikpeme, E., Etta, S., Erem, F. and Daniel, I. (2014). Protective role of soursop (Annona muricata L.) fruit on testicular toxicity induced by caffeine in albino rats. Journal of Life Sciences Research and Discovery, 22(1): 150-157.
Galardo, M., Riera, M., Pellizzari, E., Sobarzo, C., Scarcelli, R., Denduchis, B., et al. (2010). Adenosine regulates Sertoli cell function by activating AMPK. Molecular and Cell Endocrinology, 330(1-2): 49-58.
Gaskins, A.J., Mendiola, J., Afeiche, M., Jørgensen, N., Swan, S.H. and Chavarro, J.E., (2015). Physical activity and television watching in relation to semen quality in young men. British Journal of Sports Medicine, 49(4): 265-270.
Gołembiowska, K. and Dziubina, A. (2012). The Effect of Adenosine A2A Receptor Antagonists on Hydroxyl Radical, Dopamine, and Glutamate in the Striatum of Rats with Altered Function of VMAT2. Neurotoxicity Research, 22(2): 150-157.
Grandys, M., Majerczak, J., Duda, K., Zapart-Bukowska, J., Kulpa, J. and Zoladz, J.A. (2009). Endurance training of moderate intensity increases testosterone concentration in young, healthy men. International. Journal of Sports Medicine, 30(7): 489-495
Grucka-Mamczar, E., Zalejska-Fiolka, J., Chlubek, D., Kasperczyk, S., Blaszczyk, U., Kasperczyk, A. (2009). The influence of sodium fluoride and caffeine on the activity of antioxidative enzymes and the concentration of malondialdehyde in rat liver. Fluoride, 42(2): 105-109.
Hajizadeh Maleki, B., Tartibian, B. and Chehrazi, M. (2017). The effects of three different exercise modalities on markers of male reproduction in healthy subjects: a randomized controlled trial. Reproduction, 153(2): 157-74.
Hajizadeh Maleki, B. and Tartibian, B. (2020). High-intensity interval training modulates male factor infertility through anti-inflammatory and antioxidative mechanisms in infertile men: A randomized controlled trial. Cytokine, 125(1): 154861.
Huang, Z.L., Qu, W.M., Eguchi, N., Chen, J.N., Schwarzschild, M.A. and Fredholm, B.B. (2005). Adenosine A2A, but not A1, receptors mediate the arousal effect of caffeine. Nature Neurosciense, 8(7): 858-859.
Husain, K. and Somani, S.M. (1998). Interaction of exercise training and chronic ethanol ingestion on testicular antioxidant system in rat. Journal of Applied Toxicology, 18(6): 421-9.
Sohrabvand, F., Ansari, Sh. and Bagheri, M. (2006). Efficacy of combined metformin-letrozole in comparison with metforminclomiphenecitrate in clomiphene-resistant infertile women with polycystic ovarian disease. Human Reproduction, 21(6): 1432-1435.
Kalantari, A., Saremi, A., Shavandi, N. and Foroutan Nia, A. (2017). Impact of four week swimming exercise with alpha-tocopherol supplementation on fertility potential in healthy rats. Urology Journal, 14(5): 5023-5026.
Liu, A.G., Arceneaux, K.P., Chu, J.T., Jacob, G., Schreiber, A.L., Tipton, R.C., Yu, Y., Johnson, W.D., Greenway, F.L., Primeaux, S.D., 2015. The effect of caffeine and albuterol on body composition and metabolic rate. Obesity (Silver Spring Md), 23(9): 1830-1835.
Makker, K., Agarwal, A. and Sharma, R. (2009). Oxidative stress and male infertility. Indian Journal of Medical Research, 129(4): 357-367.
Marques-Aleixo, I., Santos-Alves, E., Oliveira, P.J., Moreira, P.I., Magalhães, J. and Ascensão, A. (2018). The beneficial role of exercise in mitigating doxorubicin-induced Mitochondrionopathy. Biochimical Biophysiology Acta(BBA) Reviews on Cancer, 1869(2): 189-199.
Matos, B., Howl, J., Ferreira, R. and Fardilha, M. (2019). Exploring the effect of exercise training on testicular function. European Journal of Applied Physiology, 119(1): 1-8.
Mombeyni, A., Bahmanzade, M., Sarami, A., Changizi-Ashtiyani, S. and Parastesh, M. (2018). The Effect of Increasing Resistance Training on Testicular Oxidative Stress and Quality of Spermatogenesis in Male Rats. Journal of Arak University Medical Sciense, 21(4): 86-97. [In Persian]
Monfared, M.H., Minaee, B., Rastegar, T., Khrazinejad, E. and Barbarestani, M. (2016). Sertoli cell condition media can induce germ like cells from bone marrow derived mesenchymal stem cells. Iranian Journal of Basic Medical Sciences, 19(11): 1186-1192.
Mora-Esteves, C. and Shin, D. (2013). Nutrient Supplementation: Improving Male Fertility Fourfold. Seminars in Reproductive Medicine, 31(4): 293-
Nehlig, A., Daval, J.L. and Debry, G. (1992). Caffeine and the central nervous system: mechanisms of action, biochemical, metabolic and psychostimulant effects. Brain Reserch, 17(2): 139-170.
Ojuka, E.O., Jones, T.E., Nolte, L.A., Chen, M., Wamhoff, B.R., Sturek, M., et al. (2002). Regulation of GLUT4 biogenesis in muscle: evidence for involvement of AMPK and Ca2+. American Journal of Physiology, Endocrinology and Metabolism, 282(5): 1008-1013.
Oluwole, O.F., Salami, S.A., Ogunwole, E. and Raji, Y. (2016). Implication of caffeine consumption and recovery on the reproductive functions of adult male Wistar rats. Journal of Basic and Clinical Physiology and Pharmacology, 27(5): 483-491.
Pizziol, A., Tikhonoff, V., Paleari, C., Russo, E., Mazza, A., Ginocchio, G., et al. (1998). Effects of caffeine on glucose tolerance: a placebo-controlled study. European Journal of Clinical Nutriation, 52(11): 846-849.
Priskorn, L., Jensen, T.K., Bang, A.K., Nordkap, L., Joensen, U.N., Lassen, T.H., et al. (2016). Is Sedentary Lifestyle Associated with Testicular Function? A Cross-Sectional Study of 1,210. American Journal of Epidemiology, 184(4): 284-294
Radak, Z., Ishihara, K., Tekus, E., Varga, C., Posa, A. and Balogh, L. (2017). Exercise, oxidants, and antioxidants change the shape of the bell-shaped hormesis curve. Redox Biology, 12(1): 285-290.
Rato, L., Alves, M.G., Socorro, S., Duarte, A.I., Cavaco, J.E. and Oliveira, P.F. (2012). Metabolic regulation is important for spermatogenesis. Nature Reviews. Urology, 9(6): 330-338.
Ricci, E., Viganò, P., Cipriani, S., Somigliana, E., Chiaffarino, F., Bulfoni, A. and Parazzini, F. (2017). Coffee and caffeine intake and male infertility: a systematic review. Nutrition Journal., 16(1): 37.
Rotruck, J.T., Pope, A.L., Ganther, H.E., Swanson, A.B., Hafeman, D.G. and Hoekstra, W.G. (1973). Selenium: biochemical role as a component of glutathione peroxidase. Science, 179(4073): 588-590.
Salem, M., Mirzapour, T., Bayrami, A., Sagha, M. and Asadi, A. (2017). The Effects of Sertoli Cells Condition Media and Retinoic Acid on the Number of Colonies of Bone Marrow Mesenchymal Stem Cells. Journal of Ardabil University of Medical Scienses, 17(1): 7-21. [In Persian]
Shi, X., Dalal, N. and Jain, A. (1991). Antioxidant behavior of caffeine: efficient scavenging of hydroxyl radicals. Food and Chemical Toxicology, 29(1): 1-6.
Svartberg, J., Midtby, M., Bonaa, K., Sundsfjord, J., Joakimsen, R. and Jorde, R. (2003). The associations of age, lifestyle factors and chronic disease with testosterone in men: the Tromso Study. European Journal of Endocrinology. 149(2): 145-152.
Tiwari, K.K., Chu, C., Couroucli, X., Moorthy, B. and Lingappan, K. (2014). Differential concentration-specific effects of caffeine on cell viability, oxidative stress, and cell cycle in pulmonary oxygen toxicity in vitro. Biochemical and Biophysical Research Communications, 450(4): 1345-1350.
Vaamonde, D., Da Silva-Grigoletto, M.E., García-Manso, J.M., Barrera, N. and Vaamonde-Lemos, R. (2012). Physically active men show better semen parameters and hormone values than sedentary men. European Journal of Applied Physiology., 112(9): 3267-3273.
Yokogoschi, H., Mochizuki, S., Takahata, M., Quazi, S. and Yoshida, A. (1983). Hypercholesterolemic effects of caffeine-containing beverages and xanthine-derivatives in rats. Food Additives and Contaminants, 28(12): 805-814.
_||_
Afzalpour, M.E., Chadorneshin, H.T., Foadoddini, M. and Eivari, H.A. (2015). Comparing interval and continuous exercise training regimens on neurotrophic factors in rat brain. Physiology Behavior, 147(1): 78-83.
Agarwal, A., Ikemotom I. and Loughlin, K.R. (1994). Relationship of sperm parameters with levels of reactive oxygen species in semen specimens. Journal of Urology, 152(1): 107-110.
Aitken, R.J., De Iuliis, G.N., Finnie, J.M., Hedges, A. and McLachlan, R.I. (2010). Analysis of the relationships between oxidative stresses, DNA damage and sperm vitality in a patient population: development of diagnostic criteria. Human Reproduction, 25(10): 2415-2426.
Akomolafe, S.F., Olasehinde, T.A., Ogunsuyi, O.B., Oyeleye, S.I. and Oboh, G. (2019). Revealed that caffeine (5 and 25 mg/kg) improved sperm quality, increased steroidogenic enzyme activities and attenuated oxidative damage in testis and epididymis of rats treated with scopolamine. Journal of Pharmacy and Pharmacology, 71(10): 1565-1575.
Alihemmati, A., Ebadi, F., Moghadaszadeh, M., Asadi, M., Zare, P. and Badalzadeh, R. (2019). Effects of high-intensity interval training on the expression of microRNA-499 and pro-and anti-apoptotic genes in doxorubicin-cardiotoxicity in rats. Journal of Electrocardiology, 55(1): 9-15.
Armstrong, J.S., Rajasekaran, M., Chamulitrat, W., Gatti, P., Hellstrom, W.J. and Sikka, S.C. (1999). Characterization of reactive oxygen species induced effects on human spermatozoa movement and energy metabolism. Free Radical Biology & Medicine 26(7-8): 869-880.
Bassey, R.B., Yama, O.E., Osinubi, A.A., Noronha, C.C. and Okanlawon, A. (2011). Effects of Tahitian Noni dietary supplement on caffeine-induced testicular histo-pathological alterations in adult Sprague-Dawley rats. Middle East Fertility Society Journal, 16(1): 61-66.
Bartosz, G. (2003). Total antioxidant capacity. Advances in Clinical Chemistry, 37(8): 219-229.
Dias, T.R., Alves, M.G., Bernardino, R.L., Martins, A.D., Moreira, A.C., Silva, J., et al. (2015). Dose-dependent effects of caffeine in human Sertoli cells metabolism and oxidative profile: Relevance for male fertility. Toxicology, 328(3): 12-20.
Dorostghoal, M., Majd, N.E. and Nooraei, P. (2012). Maternal caffeine consumption has irreversible effects on reproductive parameters and fertility in male offspring rats. Clinical and Experimental Reproductive Medicine, 39(4): 144-152.
Ekaluo, U., Ikpeme, E., Etta, S., Erem, F. and Daniel, I. (2014). Protective role of soursop (Annona muricata L.) fruit on testicular toxicity induced by caffeine in albino rats. Journal of Life Sciences Research and Discovery, 22(1): 150-157.
Galardo, M., Riera, M., Pellizzari, E., Sobarzo, C., Scarcelli, R., Denduchis, B., et al. (2010). Adenosine regulates Sertoli cell function by activating AMPK. Molecular and Cell Endocrinology, 330(1-2): 49-58.
Gaskins, A.J., Mendiola, J., Afeiche, M., Jørgensen, N., Swan, S.H. and Chavarro, J.E., (2015). Physical activity and television watching in relation to semen quality in young men. British Journal of Sports Medicine, 49(4): 265-270.
Gołembiowska, K. and Dziubina, A. (2012). The Effect of Adenosine A2A Receptor Antagonists on Hydroxyl Radical, Dopamine, and Glutamate in the Striatum of Rats with Altered Function of VMAT2. Neurotoxicity Research, 22(2): 150-157.
Grandys, M., Majerczak, J., Duda, K., Zapart-Bukowska, J., Kulpa, J. and Zoladz, J.A. (2009). Endurance training of moderate intensity increases testosterone concentration in young, healthy men. International. Journal of Sports Medicine, 30(7): 489-495
Grucka-Mamczar, E., Zalejska-Fiolka, J., Chlubek, D., Kasperczyk, S., Blaszczyk, U., Kasperczyk, A. (2009). The influence of sodium fluoride and caffeine on the activity of antioxidative enzymes and the concentration of malondialdehyde in rat liver. Fluoride, 42(2): 105-109.
Hajizadeh Maleki, B., Tartibian, B. and Chehrazi, M. (2017). The effects of three different exercise modalities on markers of male reproduction in healthy subjects: a randomized controlled trial. Reproduction, 153(2): 157-74.
Hajizadeh Maleki, B. and Tartibian, B. (2020). High-intensity interval training modulates male factor infertility through anti-inflammatory and antioxidative mechanisms in infertile men: A randomized controlled trial. Cytokine, 125(1): 154861.
Huang, Z.L., Qu, W.M., Eguchi, N., Chen, J.N., Schwarzschild, M.A. and Fredholm, B.B. (2005). Adenosine A2A, but not A1, receptors mediate the arousal effect of caffeine. Nature Neurosciense, 8(7): 858-859.
Husain, K. and Somani, S.M. (1998). Interaction of exercise training and chronic ethanol ingestion on testicular antioxidant system in rat. Journal of Applied Toxicology, 18(6): 421-9.
Sohrabvand, F., Ansari, Sh. and Bagheri, M. (2006). Efficacy of combined metformin-letrozole in comparison with metforminclomiphenecitrate in clomiphene-resistant infertile women with polycystic ovarian disease. Human Reproduction, 21(6): 1432-1435.
Kalantari, A., Saremi, A., Shavandi, N. and Foroutan Nia, A. (2017). Impact of four week swimming exercise with alpha-tocopherol supplementation on fertility potential in healthy rats. Urology Journal, 14(5): 5023-5026.
Liu, A.G., Arceneaux, K.P., Chu, J.T., Jacob, G., Schreiber, A.L., Tipton, R.C., Yu, Y., Johnson, W.D., Greenway, F.L., Primeaux, S.D., 2015. The effect of caffeine and albuterol on body composition and metabolic rate. Obesity (Silver Spring Md), 23(9): 1830-1835.
Makker, K., Agarwal, A. and Sharma, R. (2009). Oxidative stress and male infertility. Indian Journal of Medical Research, 129(4): 357-367.
Marques-Aleixo, I., Santos-Alves, E., Oliveira, P.J., Moreira, P.I., Magalhães, J. and Ascensão, A. (2018). The beneficial role of exercise in mitigating doxorubicin-induced Mitochondrionopathy. Biochimical Biophysiology Acta(BBA) Reviews on Cancer, 1869(2): 189-199.
Matos, B., Howl, J., Ferreira, R. and Fardilha, M. (2019). Exploring the effect of exercise training on testicular function. European Journal of Applied Physiology, 119(1): 1-8.
Mombeyni, A., Bahmanzade, M., Sarami, A., Changizi-Ashtiyani, S. and Parastesh, M. (2018). The Effect of Increasing Resistance Training on Testicular Oxidative Stress and Quality of Spermatogenesis in Male Rats. Journal of Arak University Medical Sciense, 21(4): 86-97. [In Persian]
Monfared, M.H., Minaee, B., Rastegar, T., Khrazinejad, E. and Barbarestani, M. (2016). Sertoli cell condition media can induce germ like cells from bone marrow derived mesenchymal stem cells. Iranian Journal of Basic Medical Sciences, 19(11): 1186-1192.
Mora-Esteves, C. and Shin, D. (2013). Nutrient Supplementation: Improving Male Fertility Fourfold. Seminars in Reproductive Medicine, 31(4): 293-
Nehlig, A., Daval, J.L. and Debry, G. (1992). Caffeine and the central nervous system: mechanisms of action, biochemical, metabolic and psychostimulant effects. Brain Reserch, 17(2): 139-170.
Ojuka, E.O., Jones, T.E., Nolte, L.A., Chen, M., Wamhoff, B.R., Sturek, M., et al. (2002). Regulation of GLUT4 biogenesis in muscle: evidence for involvement of AMPK and Ca2+. American Journal of Physiology, Endocrinology and Metabolism, 282(5): 1008-1013.
Oluwole, O.F., Salami, S.A., Ogunwole, E. and Raji, Y. (2016). Implication of caffeine consumption and recovery on the reproductive functions of adult male Wistar rats. Journal of Basic and Clinical Physiology and Pharmacology, 27(5): 483-491.
Pizziol, A., Tikhonoff, V., Paleari, C., Russo, E., Mazza, A., Ginocchio, G., et al. (1998). Effects of caffeine on glucose tolerance: a placebo-controlled study. European Journal of Clinical Nutriation, 52(11): 846-849.
Priskorn, L., Jensen, T.K., Bang, A.K., Nordkap, L., Joensen, U.N., Lassen, T.H., et al. (2016). Is Sedentary Lifestyle Associated with Testicular Function? A Cross-Sectional Study of 1,210. American Journal of Epidemiology, 184(4): 284-294
Radak, Z., Ishihara, K., Tekus, E., Varga, C., Posa, A. and Balogh, L. (2017). Exercise, oxidants, and antioxidants change the shape of the bell-shaped hormesis curve. Redox Biology, 12(1): 285-290.
Rato, L., Alves, M.G., Socorro, S., Duarte, A.I., Cavaco, J.E. and Oliveira, P.F. (2012). Metabolic regulation is important for spermatogenesis. Nature Reviews. Urology, 9(6): 330-338.
Ricci, E., Viganò, P., Cipriani, S., Somigliana, E., Chiaffarino, F., Bulfoni, A. and Parazzini, F. (2017). Coffee and caffeine intake and male infertility: a systematic review. Nutrition Journal., 16(1): 37.
Rotruck, J.T., Pope, A.L., Ganther, H.E., Swanson, A.B., Hafeman, D.G. and Hoekstra, W.G. (1973). Selenium: biochemical role as a component of glutathione peroxidase. Science, 179(4073): 588-590.
Salem, M., Mirzapour, T., Bayrami, A., Sagha, M. and Asadi, A. (2017). The Effects of Sertoli Cells Condition Media and Retinoic Acid on the Number of Colonies of Bone Marrow Mesenchymal Stem Cells. Journal of Ardabil University of Medical Scienses, 17(1): 7-21. [In Persian]
Shi, X., Dalal, N. and Jain, A. (1991). Antioxidant behavior of caffeine: efficient scavenging of hydroxyl radicals. Food and Chemical Toxicology, 29(1): 1-6.
Svartberg, J., Midtby, M., Bonaa, K., Sundsfjord, J., Joakimsen, R. and Jorde, R. (2003). The associations of age, lifestyle factors and chronic disease with testosterone in men: the Tromso Study. European Journal of Endocrinology. 149(2): 145-152.
Tiwari, K.K., Chu, C., Couroucli, X., Moorthy, B. and Lingappan, K. (2014). Differential concentration-specific effects of caffeine on cell viability, oxidative stress, and cell cycle in pulmonary oxygen toxicity in vitro. Biochemical and Biophysical Research Communications, 450(4): 1345-1350.
Vaamonde, D., Da Silva-Grigoletto, M.E., García-Manso, J.M., Barrera, N. and Vaamonde-Lemos, R. (2012). Physically active men show better semen parameters and hormone values than sedentary men. European Journal of Applied Physiology., 112(9): 3267-3273.
Yokogoschi, H., Mochizuki, S., Takahata, M., Quazi, S. and Yoshida, A. (1983). Hypercholesterolemic effects of caffeine-containing beverages and xanthine-derivatives in rats. Food Additives and Contaminants, 28(12): 805-814.