Verbascoside attenuates experimental varicocele-induced damage to testes and sperm levels through up-regulation of the hypothalamus-pituitary-gonadal (HPG) axis

References

• Agarwal A, Esteves SC. 2016. Varicocele and male infertility: current concepts and future perspectives. Asian J Androl. 18(2):161–162.
   PubMed Web of Science ®Google Scholar
• Alipieva K, Korkina L, Orhan IE, Georgiev MI. 2014. Verbascoside-a review of its occurrence, (bio)synthesis and pharmacological significance. Biotechnol Adv. 32(6):1065–1076.
   PubMed Web of Science ®Google Scholar
• Alsaikhan B, Alrabeeah K, Delouya G, Zini A. 2016. Epidemiology of varicocele. Asian J Androl. 18(2):179–181.
   PubMed Web of Science ®Google Scholar
• Amin B, Poureshagh E, Hosseinzadeh H. 2016. The effect of verbascoside in neuropathic pain induced by chronic constriction injury in rats. Phytother Res. 30(1):128–135.
   PubMed Web of Science ®Google Scholar
• Attia YM, El-Kersh DM, Wagdy HA, Elmazar MM. 2018. Verbascoside: identification, quantification, and potential sensitization of colorectal cancer cells to 5-FU by targeting PI3K/AKT pathway. Sci Rep. 8(1):16939.
   PubMedGoogle Scholar
• Blevrakis E, Chatzidarellis E, Anyfantakis D, Sakellaris G, Raissaki M, Zoras O, Mamoulakis C, Sofras F, Chrysos E. 2016. Impact of varicocele on biological markers of gonadal function. Hernia. 20(3):435–439.
   PubMed Web of Science ®Google Scholar
• Burow S, Fontaine R, von Krogh K, Mayer I, Nourizadeh-Lillabadi R, Hollander-Cohen L, Cohen Y, Shpilman M, Levavi-Sivan B, Weltzien FA. 2019. Medaka follicle-stimulating hormone (Fsh) and luteinizing hormone (Lh): developmental profiles of pituitary protein and gene expression levels. Gen Comp Endocrinol. 272:93–108.
   PubMed Web of Science ®Google Scholar
• Chiba K, Ramasamy R, Lamb DJ, Lipshultz LI. 2016. The varicocele: diagnostic dilemmas, therapeutic challenges and future perspectives. Asian J Androl. 18(2):276–281.
   PubMed Web of Science ®Google Scholar
• Cho CL, Esteves SC, Agarwal A. 2019. Indications and outcomes of varicocele repair. Panminerva Med. 61(2):152–163.
   PubMed Web of Science ®Google Scholar
• De Martino MU, Pastore R, Caprio M, Frajese G, Fabbri A. 2003. Dynamic testing in the evaluation of male gonadal function. J Endocrinol Invest. 26(7 Suppl):107–113.
   PubMedGoogle Scholar
• Dehghani F, Sotoude N, Bordbar H, Panjeshahin MR, Karbalay-Doust S. 2019. The use of platelet-rich plasma (PRP) to improve structural impairment of rat testis induced by busulfan. Platelets. 30(4):513–520.
   PubMed Web of Science ®Google Scholar
• Etemad L, Zafari R, Moallem SA, Vahdati-Mashhadian N, Skouei Shirvan Z, Hosseinzadeh H. 2016. Teratogenic effect of verbascoside, main constituent of Lippia citriodora leaves, in mice. Iran J Pharm Res. 15(2):521–525.
   PubMed Web of Science ®Google Scholar
• Fischer S, Ehlert U, Amiel Castro R. 2019. Hormones of the hypothalamic-pituitary-gonadal (HPG) axis in male depressive disorders – a systematic review and meta-analysis. Front Neuroendocrinol. 55:100792.
   PubMed Web of Science ®Google Scholar
• Galli A, Marciani P, Marku A, Ghislanzoni S, Bertuzzi F, Rossi R, Di Giancamillo A, Castagna M, Perego C. 2020. Verbascoside protects pancreatic β-cells against ER-stress. Biomedicines. 8(12):582.
   PubMed Web of Science ®Google Scholar
• Gan SD, Patel KR. 2013. Enzyme immunoassay and enzyme-linked immunosorbent assay. J Invest Dermatol. 133(9):e12.
   PubMed Web of Science ®Google Scholar
• Hassani-Bafrani H, Najaran H, Razi M, Rashtbari H. 2019. Berberine ameliorates experimental varicocele-induced damages at testis and sperm levels; evidences for oxidative stress and inflammation. Andrologia. 51(2):e13179.
   PubMed Web of Science ®Google Scholar
• Ivell R, Heng K, Anand-Ivell R. 2014. Insulin-like factor 3 and the HPG axis in the male. Front Endocrinol. 5:6.
   PubMed Web of Science ®Google Scholar
• Jin F, Xie T, Huang X, Zhao X. 2018. Berberine inhibits angiogenesis in glioblastoma xenografts by targeting the VEGFR2/ERK pathway. Pharm Biol. 56(1):665–671.
   PubMed Web of Science ®Google Scholar
• Johnsen SG. 1970. Testicular biopsy score count-a method for registration of spermatogenesis in human testes: normal values and results in 335 hypogonadal males. Hormones. 1(1):2–25.
   PubMedGoogle Scholar
• Karna KK, Choi BR, Kim MJ, Kim HK, Park JK. 2019. The effect of Schisandra chinensis baillon on cross-talk between oxidative stress, endoplasmic reticulum stress, and mitochondrial signaling pathway in testes of varicocele-induced SD rat. Int J Mol Sci. 20:5785.
   PubMed Web of Science ®Google Scholar
• Kathrins M. 2017. The varicocele as related to fertility. Fertil Steril. 107(1):72–73.
   PubMed Web of Science ®Google Scholar
• Kathrins M. 2018. Historical investigations into varicocele pathophysiology and sperm migration. Fertil Steril. 109(1):75–76.
   PubMed Web of Science ®Google Scholar
• Maquiaveli CC, Lucon-Júnior JF, Brogi S, Campiani G, Gemma S, Vieira PC, Silva ER. 2016. Verbascoside inhibits promastigote growth and arginase activity of Leishmania amazonensis. J Nat Prod. 79(5):1459–1463.
   PubMed Web of Science ®Google Scholar
• Maquiaveli CDC, Rochetti AL, Fukumasu H, Vieira PC, da Silva ER. 2017. Antileishmanial activity of verbascoside: selective arginase inhibition of intracellular amastigotes of Leishmania (leishmania) amazonensis with resistance induced by LPS plus IFN-γ. Biochem Pharmacol. 127:28–33.
   PubMed Web of Science ®Google Scholar
• Migone FF, Hung PH, Cowan RG, Selvaraj V, Suarez SS, Quirk SM. 2017. Overactivation of hedgehog signaling in the developing Müllerian duct interferes with duct regression in males and causes subfertility. Reproduction. 153(4):481–492.
   PubMed Web of Science ®Google Scholar
• Mohammadi H, Rezaei M, Faghihi F, Khazaie H. 2019. Hypothalamic-pituitary-gonadal activity in paradoxical and psychophysiological insomnia. J Med Signals Sens. 9(1):59–67.
   PubMedGoogle Scholar
• National Research Council (US) Institute for Laboratory Animal Research. 1996. Guide for the care and use of laboratory animals. Washington (DC): National Academies Press (US).
   Google Scholar
• Nevoux P, Mitchell V, Chevallier D, Rigot JM, Marcelli F. 2011. Varicocele repair: does it still have a role in infertility treatment? Curr Opin Obstet Gynecol. 23(3):151–157.
   PubMed Web of Science ®Google Scholar
• Pagani RL, Ohlander SJ, Niederberger CS. 2019. Microsurgical varicocele ligation: surgical methodology and associated outcomes. Fertil Steril. 111(3):415–419.
   PubMed Web of Science ®Google Scholar
• Paoletti F, Mocali A. 1990. Determination of superoxide dismutase activity by purely chemical system based on NAD(P)H oxidation. Methods Enzymol. 186:209–220.
   PubMed Web of Science ®Google Scholar
• Pastuszak AW, Wang R. 2015. Varicocele and testicular function. Asian J Androl. 17(4):659–667.
   PubMed Web of Science ®Google Scholar
• Peper JS, Brouwer RM, van Leeuwen M, Schnack HG, Boomsma DI, Kahn RS, Hulshoff Pol HE. 2010. HPG-axis hormones during puberty: a study on the association with hypothalamic and pituitary volumes. Psychoneuroendocrinology. 35(1):133–140.
   PubMed Web of Science ®Google Scholar
• Reed-Maldonado AB, Madden KC. 2019. Infertility and the military male. Semin Reprod Med. 37(1):5–11.
   PubMed Web of Science ®Google Scholar
• Roque M, Esteves SC. 2018. Effect of varicocele repair on sperm DNA fragmentation: a review. Int Urol Nephrol. 50(4):583–603.
   PubMed Web of Science ®Google Scholar
• Rotker K, Sigman M. 2016. Recurrent varicocele. Asian J Androl. 18(2):229–233.
   PubMed Web of Science ®Google Scholar
• Sand E, Bergvall M, Ekblad E, D'Amato M, Ohlsson B. 2013. Expression and distribution of GnRH, LH, and FSH and their receptors in gastrointestinal tract of man and rat. Regul Pept. 187:24–28.
   PubMedGoogle Scholar
• Sohrabipour S, Jafari A, Kamalinejad M, Sarrafnejd A, Shahrestany T, Sadeghipour HR. 2013. The role of flaxseed and vitamin E on oxidative stress in prepubertal rats with experimental varicocele: an experimental study. Iran J Reprod Med. 11(6):459–466.
   PubMedGoogle Scholar
• Soni KK, Zhang LT, Choi BR, Karna KK, You JH, Shin YS, Lee SW, Kim CY, Zhao C, Chae HJ, Kim HK, et al. 2018. Protective effect of MOTILIPERM in varicocele-induced oxidative injury in rat testis by activating phosphorylated inositol requiring kinase 1α (p-IRE1α) and phosphorylated c-Jun N-terminal kinase (p-JNK) pathways. Pharm Biol. 56(1):94–103.
   PubMed Web of Science ®Google Scholar
• Türk G, Çeribaşı S, Sönmez M, Çiftçi M, Yüce A, Güvenç M, Kaya ŞÖ, Çay M, Aksakal M. 2016. Ameliorating effect of pomegranate juice consumption on carbon tetrachloride-induced sperm damages, lipid peroxidation, and testicular apoptosis. Toxicol Ind Health. 32(1):126–137.
   PubMed Web of Science ®Google Scholar
• Wan Y, Zou B, Zeng H, Zhang L, Chen M, Fu G. 2016. Inhibitory effect of verbascoside on xanthine oxidase activity. Int J Biol Macromol. 93(Pt A):609–614.
   PubMedGoogle Scholar
• Zhang L, Zhao X, Wang F, Lin Q, Wang W. 2016. Effects of Morinda officinalis polysaccharide on experimental varicocele rats. Evid Based Complement Alternat Med. 2016:5365291.
   PubMed Web of Science ®Google Scholar
• Zhu M, Zhu H, Tan N, Wang H, Chu H, Zhang C. 2016. Central anti-fatigue activity of verbascoside. Neurosci Lett. 616:75–79.
   PubMed Web of Science ®Google Scholar