Alteration in sperm characteristics, endocrine balance and redox status in rats rendered diabetic by streptozotocin treatment: attenuating role of Loranthus micranthus

References

• Osadebe PO, Okide GB, Akabogu IC. Study on antidiabetic activities of crude methanolic extracts of Loranthus micranthus (Linn.) sourced from five different host trees. J Ethnopharmacol. 2004;95:133–138. doi: 10.1016/j.jep.2004.06.029
   PubMed Web of Science ®Google Scholar
• Griffin S, Tittikpina NK, Al-Marby A, et al. Turning waste into value: nanosized natural plant materials of Solanum incanum L. and Pterocarpus erinaceus Poir with promising antimicrobial activities. Pharmaceutics. 2016;19(2):8.
   Google Scholar
• Lee SH, Jeon YJ. Anti-diabetic effects of brown algae derived phlorotannins, marine polyphenols through diverse mechanisms. Fitoterapia. 2013;86:129–136. doi: 10.1016/j.fitote.2013.02.013
   PubMed Web of Science ®Google Scholar
• Yeh GY, Eisenberg DM, Kaptchuk TJ, et al. Systematic review of herbs and dietary supplements for glycemic control in diabetes. Diabetes Care. 2003;26(4):1277–1294. doi: 10.2337/diacare.26.4.1277
   PubMed Web of Science ®Google Scholar
• Osadebe PO, Omeje EO, Uzor PF, et al. Seasonal variation for the antidiabetic activity of Loranthus micranthus methanol extract. Asian Pac J Trop Med. 2010;3(3):196–199. doi: 10.1016/S1995-7645(10)60008-9
   Web of Science ®Google Scholar
• Griggs P. Mistletoe, myth, magic and medicine. Biochem (Lond). 1991;13:3–4.
   Google Scholar
• Moghadamtousi SZ, Hajrezaei M, Abdul Kadir H, et al. Loranthus micranthus Linn: biological activities and phytochemistry. Evid Based Complement Alternat Med. 2013;12:27–37. doi:10.1155/2013/273712
   Google Scholar
• Adesina SK, Illoh HC, Imoh JI, et al. African mistletoes (loranthaceae); ethnopharmacology, chemistry and medicinal values: an update. Afr J Tradit Complement Altern Med. 2013;10(3):161–170.
   PubMedGoogle Scholar
• Orji FA, Nwachukwu NC, Onyia AU, et al. Phytochemical and antimicrobial properties of leaves of African mistletoe (Loranthus micranthus) on some selected microbial pathogens in Abia State, Nigeria. Global Adv Res J Microbiol. 2013;2(1):011–016.
   Google Scholar
• Ramachandran V, Baojun X. Antidiabetic properties of dietary flavonoids: a cellular mechanism review. Nut Met. 2015;12:60. doi: 10.1186/s12986-015-0057-7
   PubMed Web of Science ®Google Scholar
• Arts IC, Hollman PC. Polyphenols and disease risk in epidemiologic studies. Am J Clin Nutr. 2005;81:317S–325S. doi: 10.1093/ajcn/81.1.317S
   PubMed Web of Science ®Google Scholar
• Duncan BB, Schmidt MI, Pankow JS, et al. Low-grade systemic inflammation and the development of type 2 diabetes: The atherosclerosis risk in communities study. Diabetes. 2003;52:1799–1805. doi: 10.2337/diabetes.52.7.1799
   PubMed Web of Science ®Google Scholar
• Pickup JC. Inflammation and activated innate immunity in the pathogenesis of type 2 diabetes. Diabetes Care. 2004;27:813–823. doi: 10.2337/diacare.27.3.813
   PubMed Web of Science ®Google Scholar
• Rice-Evans CA, Miller NJ, Paganga G. Structure-antioxidant activity relationships of flavonoids and phenolic acids. Free Radic Biol Med. 1996;20:933–956. doi: 10.1016/0891-5849(95)02227-9
   PubMed Web of Science ®Google Scholar
• Kandaswami C, Middleton E. Free radical scavenging and antioxidant activity of plant flavonoids. Adv Exp Med Biol. 1994;366:351–376. doi: 10.1007/978-1-4615-1833-4_25
   PubMedGoogle Scholar
• Pandey KB, Rizvi SI. Plant polyphenols as dietary antioxidants in human health and disease. Oxid Med Cell Longev. 2009;2:270–278. doi: 10.4161/oxim.2.5.9498
   PubMed Web of Science ®Google Scholar
• Bahadoran Z, Mirmiran P, Azizi F. Dietary polyphenols as potential nutraceuticals in management of diabetes: A review. J Diabetes Metab Disord. 2013;12:43. doi: 10.1186/2251-6581-12-43
   PubMedGoogle Scholar
• Adedara IA, Awogbindin IO, Anamelechi JP, et al. Garcinia kola seed ameliorates renal, hepatic, and testicular oxidative damage in streptozotocin-induced diabetic rats. Pharm Biol. 2014. DOI: 10.3109/13880209.2014.937504.
   PubMed Web of Science ®Google Scholar
• Rato L, Alves M, Dias G, et al. Testicular metabolic reprogramming in neonatal streptozotocin-induced type 2 diabetic rats impairs glycolytic flux and promotes glycogen synthesis. J Diabetes Res. 2015. DOI:10.1155/2015/973142.
   PubMed Web of Science ®Google Scholar
• Vignera SL, Condorelli R, Vicari E, et al. Diabetes mellitus and sperm parameters. J Androl. 2012;33:145–153. doi: 10.2164/jandrol.111.013193
   PubMedGoogle Scholar
• Lutz W, Leridon H, Aitken RJ. Fertility rates and future population trends:Will Europe’s birth rate recover or continue to decline? Int J Androl. 2006;29:25–33. doi: 10.1111/j.1365-2605.2005.00639.x
   PubMedGoogle Scholar
• Hamilton BE, Hoyert DL, Martin JA, et al. Annual summary of vital statistics: 2010-2011. Pediatrics. 2013;131:548–558. doi: 10.1542/peds.2012-3769
   PubMed Web of Science ®Google Scholar
• Gillot I, Jehl-Pietr C, Gounon P. Germ cells and fatty acids induce translocation of CD36 scavenger receptor to the plasma membrane of Sertoli cells. J. Cell Sci. 2005;118:3027–3035. doi: 10.1242/jcs.02430
   PubMed Web of Science ®Google Scholar
• Rato L, Alves MG, Dias TR. High-energy diets may induce a pre-diabetic state altering testicular glycolytic metabolic profile and male reproductive parameters. Andrology. 2013;1(3):495–504. doi: 10.1111/j.2047-2927.2013.00071.x
   PubMed Web of Science ®Google Scholar
• Rato L, Alves MG, Socorro S, et al. Metabolic modulation induced by oestradiol and DHT in immature rat Sertoli cells cultured in vitro. Biosci Rep. 2012;32(1):61–69. doi: 10.1042/BSR20110030
   PubMed Web of Science ®Google Scholar
• Alves MG, Martins AD, Rato L, et al. Molecular mechanisms beyond glucose transport in diabetes-related male infertility. Biochim Biophys Acta. 2013;1832(5):626–635. doi: 10.1016/j.bbadis.2013.01.011
   PubMed Web of Science ®Google Scholar
• Rato L, Alves M, Socorro GS, et al. Metabolic regulation is important for spermatogenesis. Nat Rev Urol. 2012;9(6):330–338. doi: 10.1038/nrurol.2012.77
   PubMed Web of Science ®Google Scholar
• Rato L, Duarte AI, Tom GD. Pre-diabetes alters testicular PGC1-α/SIRT3 axismodulating mitochondrial bioenergetics and oxidative stress. Biochim Biophys Acta. 2014;1837(3):335–344. doi: 10.1016/j.bbabio.2013.12.008
   PubMed Web of Science ®Google Scholar
• Rato L, Alves MG, Cavaco JE, et al. High energy diets: a threat for male fertility? Obes Rev. 2014;15(12):996–1007. doi: 10.1111/obr.12226
   PubMed Web of Science ®Google Scholar
• Zemjanis R. Collection and evaluation of semen. In: Zemjanis R, editor. Diagnostic and therapeutic technique in animal reproduction. 2nd ed. Baltimore, MD: William and Wilkins Company; 1970. p. 139–153.
   Google Scholar
• Pant N, Srivastava SP. Testicular and spermatotoxic effects of quinalphos in rats. J Appl Toxicol. 2003;23:271–274. doi: 10.1002/jat.919
   PubMed Web of Science ®Google Scholar
• Lowry OH, Rosenbrough NJ, Farr AL. Protein measurement with folin phenol reagent. J Biol Chem. 1951;193:265–275.
   PubMed Web of Science ®Google Scholar
• Misra HP, Fridovich I. The role of superoxide anion in the autooxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem. 1972;247:3170–3175.
   PubMed Web of Science ®Google Scholar
• Clairborne A. Catalase activity. In: Greewald AR, editor. Handbook of methods for oxygen radical research. Boca Raton, FL: CRC; 1995. p. 237–242.
   Google Scholar
• Jollow DJ, Mitchell JR, Zampaglione N. Bromobenzene induced liver necrosis: protective role of glutathione and evidence for 3, 4 bromobenzene oxide as the hepatotoxic metabolite. Pharmacology. 1974;11:151–169. doi: 10.1159/000136485
   PubMed Web of Science ®Google Scholar
• Rotruck JT, Pope AL, Ganther HE. Selenium: biochemical role as a component of glutathione peroxidase. Science. 1973;179:588–590. doi: 10.1126/science.179.4073.588
   PubMed Web of Science ®Google Scholar
• Farombi EO, Tahnteng JG, Agboola AO. Chemoprevention of 2 acetylaminofluorene-induced hepatotoxicity and lipid peroxidation in rats by kolaviron-a Garcinia kola seed extract. Food Chem Toxicol. 2000;38:535–541. doi: 10.1016/S0278-6915(00)00039-9
   PubMed Web of Science ®Google Scholar
• Bergmeyer HU. β-Hydroxysteroid dehydrogenase. In: Bergmeyer HU, editor. Methods of enzymatic analysis, vol. 1. New York: Academic Press; 1974. p. 447–489.
   Google Scholar
• Branstrup N, Krik JE, Bruni C. The hexokinase and phosphoglucoisomerase activities of aorta and pulmonary artery tissue in individuals of various ages. J Gerontol. 1957;12:166–171. doi: 10.1093/geronj/12.2.166
   PubMedGoogle Scholar
• Dawson RCM, Elliott DC, Elliott WH, et al. Data For biockemical research. 2nd ed. Oxford: Clarendon Press; 1969; p.483–498.
   Google Scholar
• Tuominen VJ, Ruotoistenmäki S, Viitanen A, et al. Immunoratio: a publicly available web application for quantitative image analysis of estrogen receptor (ER), progesterone receptor (PR), and Ki-67. Breast Cancer Res 2010;12(4):56. doi: 10.1186/bcr2615
   PubMed Web of Science ®Google Scholar
• Elham G, Vahid N, Mozafar K. Antioxidant and protective effects of Royal jelly on histopathological changes in testis of diabetic rats. Int J Reprod Biomed. 2016;14(8):519–526. doi: 10.29252/ijrm.14.8.519
   PubMed Web of Science ®Google Scholar
• Atalay UB, Ilhan F, Gulyuz F, et al. The effects of sildenafil citrate and vitamins A. C and E on testicular damage in alloxan-diabetic rats. J Anim Vet Adv. 2012;11:56–63. doi: 10.3923/javaa.2012.56.63
   Google Scholar
• Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227:680–685. doi: 10.1038/227680a0
   PubMed Web of Science ®Google Scholar
• Rambir S, Priyanka B, Poonam S. Antioxidant and toxicological evaluation of Cassia sopherain streptozotocin-induced diabetic Wistar rats. Pharmacognosy Res. 2013;5(4):225–232. doi: 10.4103/0974-8490.118767
   PubMedGoogle Scholar
• Al-Maghrebi M, Waleed MR. Altered expression profile of glycolytic enzymes during testicular ischemia reperfusion injury is associated with the p53/TIGAR pathway: effect of fructose 1,6-diphosphate. PeerJ. 2016;4:e2195. DOI10.7717/peerj.2195.
   PubMed Web of Science ®Google Scholar
• Oliveira PF, Martins AD, Moreira AC, et al. The Warburg effect revisited—lesson from the Sertoli cell. Med Res Rev. 2015;35:126–151. doi: 10.1002/med.21325
   PubMed Web of Science ®Google Scholar
• Boussouar F, Benahmed M. Lactate and energy metabolism in male germ cells. Trends Endocrinol Metab. 2004;15:345–350. doi: 10.1016/j.tem.2004.07.003
   PubMed Web of Science ®Google Scholar
• Miki K. Energy metabolism and sperm function. Soc Reprod Fertil Suppl. 2007;65:309–325.
   PubMedGoogle Scholar
• Mukai C, Okuno M. Glycolysis plays a major role for adenosine triphosphate supplementation in mouse sperm flagellar movement. Biol Reprod. 2004;71:540–547. doi: 10.1095/biolreprod.103.026054
   PubMed Web of Science ®Google Scholar
• Travis AJ, Tutuncu L, Jorgez CJ. Requirements for glucose beyond sperm capacitation during in vitro fertilization in the mouse. Biol Reprod. 2004;71:139–145. doi: 10.1095/biolreprod.103.025809
   PubMed Web of Science ®Google Scholar
• Williams AC, Ford WC. The role of glucose in supporting motility and capacita- tion in human spermatozoa. J Androl. 2001;22:680–695.
   PubMedGoogle Scholar
• Rao PM, Kelly DM, Jones TH. Testosterone and insulin resistance in the metabolic syndrome and T2DM in men. Nat Rev Endocrinol. 2013;9(8):479–493. doi: 10.1038/nrendo.2013.122
   PubMed Web of Science ®Google Scholar
• Alberts B, Johnson A, Lewis J, et al. Molecular biology of the cell. 4th ed. New York: Garland Science; 2002.
   Google Scholar
• Pitteloud N, Hardin M, Dwyer AA. Increasing insulin resistance is associated with a decrease in Leydig cell testosterone secretion in men. J Clin Endocrinol Metab. 2005;90(5):2636–2641. doi: 10.1210/jc.2004-2190
   PubMed Web of Science ®Google Scholar
• Amaral S, Mota PC, Lacerda B, et al. Testicular mitochondrial alterations in untreated streptozotocin-induced diabetic rats. Mitochondrion. 2009;9:41–50. doi: 10.1016/j.mito.2008.11.005
   PubMed Web of Science ®Google Scholar
• Khaneshi F, Nasrolahi O, Azizi S, et al. Sesame effects on testicular damage in streptozotocin-induced diabetes rats. Avicenna J Phytomed. 2013;3(4):347–355.
   PubMedGoogle Scholar
• Navarro-Casado L, Juncos-Tobarra MA, Chafer-Rudilla M, et al. Effect of experimental diabetes and STZ on male fertility capacity study in rats. J Androl. 2010;31:584–592. doi: 10.2164/jandrol.108.007260
   PubMedGoogle Scholar
• Ballester J, Munoz MC, Dominguez J, et al. Insulin-dependent diabetes affects testicular function by FSH- and LH-linked mechanisms. J Androl. 2004;25:706–719. doi: 10.1002/j.1939-4640.2004.tb02845.x
   PubMedGoogle Scholar
• Yadav R, Goel A, Sankhwar SN, et al. Incidentally detected bilaterally symmetrical seminal and vas calcification in young infertile male: a case report, literature review and algorithm for diagnosis. Can Urol Assoc J. 2012;6(5):206–208. doi: 10.5489/cuaj.12009
   Web of Science ®Google Scholar
• González OFJ, Duque F, Vega S, et al. Bilateral calcification of seminal vesicles and vas deferens. Actas Urol Esp. 2009;33:216. doi: 10.1016/S0210-4806(09)74129-4
   PubMed Web of Science ®Google Scholar
• Culver GJ, Tannenhaus J. Calcification of the vas deferens in diabetes. J Am Med Assoc. 1960;173:648–651. doi: 10.1001/jama.1960.03020240036006
   PubMed Web of Science ®Google Scholar
• Guvel S, Pourbagher MA, Torun DT, et al. Calcification of the epididymis and the tunica albuginea of the corpora cavernosa in patients on maintenance hemodialysis. J Androl. 2004;25:752–756. doi: 10.1002/j.1939-4640.2004.tb02851.x
   PubMed Web of Science ®Google Scholar
• Richenberg J, Belfield J, Ramchandani P, et al. Testicular microlithiasis imaging and follow-up: guidelines of the ESUR scrotal imaging subcommittee. Eur Radiol. 2015;25:323–330. doi: 10.1007/s00330-014-3437-x
   PubMed Web of Science ®Google Scholar