Effects of Manganese Exposure on Testicular Histomorphology, Serum Hormones Level and Biochemical Marker Parameters in Wistar Rats
Abstract
Manganese is an essential trace element that can elicit a variety of toxic responses upon prolonged exposure. The aim of the present study was to elucidate the toxic effects of manganese chloride (MnCl2) exposure on testicular histomorphology, reproductive hormone levels and oxidative stress parameters in Wistar rats. Adult, colony bred male rats were divided into four groups each having eight animals. Group I served as control and received normal saline (0.5 ml/rat) as vehicle while Group II, III and IV received 50, 100 and 150 mg/kg b.wt. MnCl2/day orally, respectively for 60 days. The present study revealed thatthe body andrelative weight of testes, serum follicle stimulating hormone, luteinizing hormone and testosterone levels were significantly declined in MnCl2 exposed rats when compared with control rats. The level of testicular thiobarbituric acid reactive substance (TBARs) was increased with concomitant decline in superoxide dismutase activity, glutathione and ascorbic acid levels. Histomorphological study of the testis in MnCl2 exposed rats revealed dose dependent degenerative and atrophic changes, exfoliation of germ cells, shrinkage of seminiferous tubules and Leydig cell nucleus. Thus, the findings of the present study suggested that exposure of MnCl2 at high doses had significant adverse impact on male reproductive endpoints.
References
Abd-Aleh SO, Rahim SA, Radi NK (2017) The effect of manganese poisoning on the histological structure of testis in male Swiss mice. Mesopo Environ Special Issue C,44-53
Abercrombie M (1946) Estimation of nuclear population from microtome sections. Anat Rec 94(2):239-247
Adaramoye OA, Akanni OO (2016) Protective effects of Artocarpus altilis (Moraceae) on cadmiumâ€induced changes in sperm characteristics and testicular oxidative damage in rats. Andrologia 48(2):152-163
Adedara IA, Abolaji AO, Awogbindin IO, Farombi, EO (2017) Suppression of the brain-pituitary-testicular axis function following acute arsenic and manganese co-exposure and withdrawal in rats. J Trace Elem Med Biol 39:21-29
Agarwal A, Virk G, Ong C, Plessis S S (2014) Effect of Oxidative Stress on Male Reproduction. World J Mens Health 32(1):1-17
Agrawal M, Sharma P, Kushwaha S (2011) Antifertility efficacy of 50% ethanolic extract of Calendula officinalis in male rats. Int J Pharm Pharm Sci 5:192-196
Aitkin RJ, Roman SD (2008) Antioxidant systems and oxidative stress in the testis. Oxid Med Cell Longev 1:15-24
Ajibade, AJ, Fakunle, PB, Fatoba, OO, Olayemi OT (2011) Some effects of manganese dichloride administration on the body weight, Purkinje cell population, brain, and cerebellar weights of adult Wistar rats. J Neurosci Behav Health 3(7):87-90
Aschner, M, Guilarte, TR, Schneider JS, Zheng W (2007) Manganese: recent advances in understanding its transport and neurotoxicity Toxicol Appl Pharmacol 221(2):131-147
Boudou F, Aldi DEH, Slimani M, Berroukche A (2014) The impact of chronic exposure to manganese on testiculaire tissue and sperm parameters in rat Wistar. International Journal of Natural Sciences Research 3:12-19
Cai XL, Wang GX, Guo H (2010) Effect of manganese on Caspase-3 mRNA regulation in spermatogenic cell and the expression of vimentin on sertoli cell in rats. Acta Anat Sin 41(3):0529-1356
Chaki SP, Misro MM, Gautam DK, Kaushik M, Ghosh D, Chainy GB (2006) Estradiol treatment induces testicular oxidative stress and germ cell apoptosis in rats. Apoptosis 11(8):1427-1437
Chandel M, Jain GC (2014) Toxic effects of transition metals on male reproductive system: A review. J Environ Occup Sci 3(4):204-213
Chandel M, Jain GC (2016) Manganese-induced hematological alteration in Wistar rats. J Environ Occup Sci 5:77-81
Chandra AK, Chatterjee A, Ghosh R, Sarkar M (2010) Vitamin E-supplementation protect chromium (VI)-induced spermatogenic and steroidogenic disorders in testicular tissues of rats. Food Chem Toxicol 48(3):972-979
Chen P, Chakraborty S, Mukhopadhyay S, Lee E, Paoliello M, Bowman AB, Aschner M (2015) Manganese homeostasis in the nervous system. J Neurochem 134(4):601-610
Cheng J, Fu J L, Zhou ZC (2003) The inhibitory effects of manganese on steroidogenesis in rat primary Leydig cells by disrupting steroidogenic acute regulatory (StAR) protein expression. Toxicology 187(2):139-148
Creasy DM (2001) Pathogenesis of male reproductive toxicity. Toxicol Pathol 29(1):64-76
Dorman DC, Struve MF, Marshall MW, Parkinson CU, James RA, Wong BA (2006) Tissue manganese concentrations in young male rhesus monkeys following subchronic manganese sulfate inhalation. Toxicol Sci 92(1):201-210
Elbetieha A, Bataineh H, Darmani H, Al-Hamood MH (2001) Effects of long-term exposure to manganese chloride on fertility of male and female mice. Toxicol Lett 119(3):193-201
Farombi EO, Adedara IA, Akinrinde SA, Ojo OO, Eboh AS (2012) Protective effects of kolaviron and quercetin on cadmiumâ€induced testicular damage and endocrine pathology in rats. Andrologia 44(4):273-284
França LR, Silva Jr VA, Chiarini-Garcia H, Garcia SK, Debeljuk L (2000) Cell Proliferation and Hormonal Changes During Postnatal Development of the Testis in the Pig 1 Biol Reprod 63(6):1629-1636
Galal AAA, Alam RTM, Abd Elâ€Aziz RM (2016) Adverse effects of longâ€term administration of fluvoxamine on haematology, blood biochemistry and fertility in male albino rats: a possible effect of cessation. Andrologia 48(9):914-922
Gunter TE, Gavi CE, Aschner M, Gunter KK (2006) Speciation of manganese in cells and mitochondria: a search for the proximal cause of manganese neurotoxicity. Neurotoxicol 27(5):765-776
Gupta G, Rajalakshmi M, Prasad MRN, Moudgal NR (1974) Alteration of epididymal function and its relation to maturation of spermatozoa. Andrologia 6(1):35-44
Hu H (2002) Human health and heavy metals exposure. In: McCally M (ed) Life Support: The Environment and Human Health, MIT press. Chapter: 4
Hu J, Zhang Z, Shen WJ, Azhar S (2010) Cellular cholesterol delivery, intracellular processing and utilization for biosynthesis of steroid hormones. Nutr Metab 7:47
Huang YL, Tseng WC, Lin TH (2001) In vitro effects of metal ions (Fe2+, Mn2+, Pb2+) on sperm motility and lipid peroxidation in human semen. J Toxicol Environ Health A 62(4):259-267
Imam Z, Chandra SV (1975) Histochemical alterations in rabbit testis produced by manganese chloride. Toxicol Appl Pharmacol 32(3):534-544
Jablonska-Czapla M (2015) Manganese and its speciation in environmental samples using hyphenated techniques: A review. J Elementol 20(4):1061-1075
Jana K, Jana S, Samanta PK (2006) Effects of chronic exposure to sodium arsenite on hypothalamo-pituitary-testicular activities in adult rats: possible an estrogenic mode of action. Reprod Biol Endocrinol 4:9. doi:10.1186/1477-7827-4-9
Jiang Y, Zheng W (2005) Cardiovascular toxicities upon manganese exposure. Cardiovasc Toxicol 5(4):345-354
Juberg DR, Mudra DR, Hazelton GA, Parkinson A (2006) The effect of fenbuconazole on cell proliferation and enzyme induction in the liver of female CD1 mice. Toxicol Appl Pharmacol 214(2):178-187
Kamtchouing P, Fandio GM, Dimo T, Jatsa HB (2002) Evaluation of androgenic activity of Zingiber officinale and Pentadiplandra brazzeana in male rats. Asian J Androl 4(4):299-302
Khan KN, Andress JM, Smith PF (1997) Toxicity of subacute intravenous manganese chloride administration in beagle dogs. Toxicol Pathol 25(4):344-350
Kostić T, Andrić S, KovaÄević R, Marić D (1998) The involvement of nitric oxide in stress-impaired testicular steroidogenesis. Eur J Pharmacol 346(2):267-273
Lauwerys R, Roels H, Genet P, Toussaint G, Bouckaert A, De Cooman S (1985) Fertility of male workers exposed to mercury vapor or to manganese dust: A questionnaire study. Am J Ind Med 7(2):171-176
Lebda MA, El-Neweshy MS, El-Sayed YS (2012) Neurohepatic toxicity of subacute manganese chloride exposure and potential chemoprotective effects of lycopene. Neurotoxicology 33(1):98-104
Leblond CP, Clermont Y (1952) Definition of the stages of the cycle of the seminiferous epithelium in the rat. Ann N Y Acad Sci 55(1):548-573
Lee B, Pine M, Johnson L, Rettori V, Hiney JK, Les Dees W (2006) Manganese acts centrally to activate reproductive hormone secretion and pubertal development in male rats. Reprod Toxicol 22(4):580-585
Liu XF, Zhang LM, Guan HN, Zhang ZW, Xu SW (2013) Effects of oxidative stress on apoptosis in manganese-induced testicular toxicity in cocks. Food Chem Toxicol 60:168-176
Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193(1):265-275
Marklund S, Marklund G (1974) Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem 47(3):469-474
Martinez-Finley EJ, Gavin CE, Aschner M, Gunter TE (2013) Manganese neurotoxicity and the role of reactive oxygen species. Free Radic Biol Med 62:65-75
McLachlan RI, Wreford NG, De Kretser DM, Robertson DM (1995) The effects of recombinant follicle-stimulating hormone on the restoration of spermatogenesis in the gonadotropin-releasing hormone-immunized adult rat. Endocrinology 136(9):4035-4043
Milatovic D, Gupta RC, Yu Y, Zaja-Milatovic S, Aschner M (2011) Protective effects of antioxidants and anti-inflammatory agents against manganese-induced oxidative damage and neuronal injury. Toxicol Appl Pharmacol 256(3):219-226
Montgomery R (1957) Determination of glycogen. Arch Biochem Biophys 67(2):378-386
Morakinyo AO, Achema PU, Adegoke OA (2010) Effect of Zingiber officinale (Ginger) on sodium arsenite-induced reproductive toxicity in male rats. Afr J Biomed Res 13(1):39-45
Moron MS, Depierre JW, Mannervik B (1979) Levels of glutathione, glutathione reductase and glutathione S-transferase activities in rat lung and liver. Biochim Biophys Acta 582(1): 67-78
Mourao Jr CA, Schmidt SL, Manhães AC (2003) Testosterone and free thyroxin blood in congenitally acallosal male BALB/cCF mice. Neuro Endocrinol Lett 24(6):459-462
Murthy RC, Srivastava RS, Gupta SK, Chandra SV (1980) Manganese induced testicular changes in monkeys. Exp Pathol 18(4):240-244
Nuha AL-Harbi Y (2014) Histological Alteration Induced by Manganese chloride in the Male Testes, Epididymis and Kidney of the Albino Rats. International Research Journal of Natural Sciences 3:12-19
Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95(2):351-358
Pandey G, Jain GC (2015) Assessment of Molybdenum Induced Alteration in Oxidative Indices Biochemical Parameters and Sperm Quality in Testis of Wistar Male Rats. Asian J Biochem 10 (6):267-280
Pandey G, Jain GC (2015) Molybdenum induced histopathological and histomorphometric alterations in testis of male wistar rats. International Journal of Current Microbiology and Applied Sciences 4(1):150-61
Ponnapakkam TP, Bailey KS, Graves KA, Iszard MB (2003) Assessment of male reproductive system in the CD-1 mice following oral manganese exposure. Reprod Toxicol 17(5):547-551
Rawi SM, Seif Al Nassr FM (2015) Zinc sulphate and vitamin E alleviate reproductive toxicity caused by aluminium sulphate in male albino rats. Toxicol Ind Health 31(3):221-234
Resenberg A, (1999) Biochemistry and Role of Sialic Acid. In: Resenberg A (ed) Biology of Sialic Acid, Plenum Press, New York, pp. 7-67
Roe J, Kuether C (1943) Estimation of ascorbic acid. J Biol Chem 147:3999
Rojanasakul A, Udomsubpayakul U, Chinsomboon S (1994) Chemiluminescence immunoassay versus radioimmunoassay for the measurement of reproductive hormones. Int J Gynaecol Obstet 45(2):141-146
Roth J, Zuber C, Park S, Jang I, Lee Y, Kysela KG, Cho JW (2010) Protein N-glycosylation, protein folding, and protein quality control. Mol Cell 30(6):497-506
Sakr SA, Nooh HZ (2013) Effect of Ocimum basilicum extract on cadmium-induced testicular histomorphometric and immunohistochemical alterations in albino rats. Anat Cell Biol 46(2):122-130
Sánchez DJ, Domingo J, Llobet JM, Keen CL (1993) Maternal and developmental toxicity of manganese in the mouse. Toxicol Lett 69(1):45-52
Santamaria AB (2008) Manganese exposure, essentiality toxicity. Indian J Med Res 128(4):484-500
Saxena DK, Husain R, Chandra SV, Seth PK (1976) Manganese induced biochemical alterations in rat seminiferous tubules. Ind Health 14(1-2):15-20
Sharpe RM (1994) Regulation of spermatogenesis. The Physiology of Reproduction, 1363-1434
Warren L (1959) The thiobarbituric acid assay of sialic acids. J Biol Chem 234(8):1971-1975
Weinbauer GF, Luetjens CM, Simoni M, Nieschlag E (2010) Physiology of testicular function. In Andrology. Springer Berlin Heidelberg, pp. 11-59
Weiping W (1992) Effects on testis reproductive function of male workers exposed to manganese. Industrial Health and Occupational Diseases, 5, 011
Williams M, Todd GD, Roney N, Crawford J et al. (2012) Relevance to public health. In: Toxicological profile for manganese, Agency for toxic substances and disease registry, United States Department of Health and Human Services, Public health service, Atlanta, GA. https://www.ncbi.nlm.nih.gov/books/NBK158871/
Wirth JJ, Rossano MG, Daly DC, Paneth N, Puscheck E, Potter RC, Diamond MP (2007) Ambient manganese exposure is negatively associated with human sperm motility and concentration. Epidemiology 18(2):270-273
Wooley A (2003) Determination–general and reproductive toxicology. A Guide to Practical Toxicology Evaluation, Prediction and Risk, 80-106
World Health Organization, Manganese in drinking-water (2011) Background document for development of WHO guidelines for drinking-water quality. WHO/SDE/WSH/03.04/104/Rev/1
Xuejun L, Jifang L, Libo L et al. (1998) Pathological changes of testis in rabbits induced by manganese bichloride. Journal of Norman Bethune University of Medical Science. 02
Yueming J, Jipei L, Peiyi X (2000) Effects of manganese on gonadal hormone level in male exposed workers. Journal of Guangxi Medical University, 1:008
Zhai XW, Zhang YL, Qi Q, Bai Y, Chen XL, Jin LJ, Liu FJ (2013) Effects of molybdenum on sperm quality and testis oxidative stress. Syst Biol Reprod Med 59(5):251-255
Zlatkis A, Zak B, Boyle AJ (1953) A new method for the direct determination of serum cholesterol. J Lab Clin Med 41:486-492
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