Sains Malaysiana 47(8)(2018): 1827–1833

http://dx.doi.org/10.17576/jsm-2018-4708-22

Androgen Receptor and Ultrastructural Features of Nigella sativa Oil and Nicotine-Treated Male Rat Reproductive Glands

(Ciri-ciri Struktur Ultra dan Reseptor Androgen bagi Kelenjar Pembiakan Tikus yang Dirawat Nikotin dan Minyak Nigella sativa)

LINA, S¹., ELIZA, H²., HASHIDA, N.H.^3*, IBRAHIM, S.F⁴. & OSMAN, K⁵.

¹Institute of Graduate Studies, University of Malaya, 50603 Kuala Lumpur, Federal Territory, Malaysia

²Department of Anatomy, Faculty of Medicine, University of Malaya, 50603 Kuala Lumpur, Federal Territory, Malaysia

³Center for Foundation Studies in Science, University of Malaya, 50603 Kuala Lumpur, Federal Territory, Malaysia

⁴Department of Physiology, Faculty of Medicine, Universiti Kebangsaan Malaysia Medical Centre, Jalan Yaacob Latif, Bandar Tun Razak, 56000 Cheras, Kuala Lumpur, Federal Territory, Malaysia

⁵Faculty of Allied Health Sciences, Universiti Kebangsaan Malaysia, Jalan Raja Muda Abdul Aziz, 50300 Kuala Lumpur, Federal Territory, Malaysia

Diserahkan: 27 Januari 2017/Diterima: 19 Mac 2018

ABSTRACT

Nicotine is claimed to increase free radicals, DNA damage and lipid peroxidation in male reproductive organs. Nigella sativa has been identified to ameliorate these adverse effects due to nicotine intake. This study was conducted to evaluate potential protective effects of N. sativa oil on the adverse effects of nicotine on androgen receptors (AR) and ultrastructural features of rat seminal vesicles and prostate glands. Twenty four Sprague Dawley male rats, 7-9 weeks of age and 200-250 g body weight (BW) were randomly divided into; Group 1 Saline (S), forced fed with 0.1 mL/100 g BW of 0.9% normal saline; Group 2 Nicotine (N), intramuscularly injected with 0.5 mg/100 g BW of nicotine; Group 3 N. sativa (NS), forced fed with 6.0 μL/100 g BW of N. sativa and Group 4 Nicotine-N. sativa (NNS), co-administered with 0.5 mg/100 g BW of nicotine and 6.0 μL/100 g BW of N. sativa. The seminal vesicles and prostate glands were extracted after 100 days of treatment. The seminal vesicle and prostate gland were processed for ultrastructural study and androgen receptor detection. The epithelial cells in prostate gland and seminal vesicle of the N group showed weaker brown staining intensity as compared to that of in the NS and NNS groups. This was consistent with the presence of some ultracellular changes observed in the prostate gland and seminal vesicle tissues of the N group. Findings from this study suggest that administration of N. sativa results in ameliorating effects on both the prostate gland and seminal vesicle structures and functions of the nicotine-treated rats.

Keywords: Androgen receptor; nicotine; Nigella sativa; prostate gland; seminal vesicle

ABSTRAK

Nikotin didakwa meningkatkan radikal bebas, merosakkan DNA dan pengoksidaan lipid dalam organ pembiakan lelaki. Nigella sativa telah dikenal pasti untuk memperbaiki kesan buruk akibat pengambilan nikotin. Kajian ini telah dijalankan untuk menilai potensi kesan perlindungan minyak N. sativa pada kesan buruk nikotin kepada reseptor androgen (AR) dan ciri-ciri struktur ultra vesikel semen dan kelenjar prostat tikus. Dua puluh empat tikus jantan Sprague Dawley, berumur 7-9 minggu dan 200-250 g berat badan (BW) telah dibahagikan secara rawak kepada; Kumpulan 1 Salin (S), diberi makan secara paksaan dengan salin normal 0.9% 0.1 mL/100 g BW; Kumpulan 2 Nikotin (N), disuntik intraotot dengan nikotin 0.5 mg/100 g BW; Kumpulan 3 N. sativa (NS), diberi makan secara paksaan dengan N. sativa 6.0 uL/100 g BW dan Kumpulan 4 Nikotin-N. sativa (NNS), diberi bersama nikotin 0.5 mg/100 g BW dan N. sativa 6.0 uL/100 g BW. Vesikel semen dan kelenjar prostat telah diekstrak selepas 100 hari rawatan. Vesikel seminal dan kelenjar prostat telah diproses untuk kajian struktur ultra dan pengesanan reseptor androgen. Sel-sel epitelium dalam kelenjar prostat dan vesikel semen bagi kumpulan N menunjukkan keamatan pewarnaan coklat yang lemah berbanding dengan kumpulan NS dan NNS. Ini adalah konsisten dengan kehadiran beberapa perubahan sel ultra yang diperhatikan dalam kelenjar prostat dan tisu vesikel semen bagi kumpulan N. Penemuan daripada kajian ini mencadangkan bahawa pemberian N. sativa memberi kesan pemulihan kepada struktur dan fungsi kedua-dua kelenjar prostat dan vesikel semen tikus yang dirawat nikotin.

Kata kunci: Kelenjar prostat; Nigella sativa; nikotin; reseptor androgen; vesikel semen

RUJUKAN

Adedara, I.A., Lawal, T.A., Adesina, A.A., Oyebiyi, O.O., Ebokaiwe, A.P. & Farombi, E.O. 2014. Sperm functional parameters and erythrocytes oxidant-antioxidant imbalance during municipal landfill leachate treatment withdrawal in rats. Environmental Toxicology and Pharmacology 37(1): 460-467.

Aitken, R.J., Smith, T.B., Jobling, M.S., Baker, M.A. & De Iuliis, G.N. 2014. Oxidative stress and male reproductive health. Asian Journal of Andrology 16(1): 31.

Al-Malki, A.L. & Moselhy, S.S. 2013. Protective effect of vitamin E and epicatechin against nicotine-induced oxidative stress in rats. Toxicology and Industrial Health 29(2): 202-208.

Al-Sa’aidi, J.A.A., Al-Khuzai, A.L.D. & Al-Zobaydi, N.F.H. 2009. Effect of alcoholic extraction on Nigella sativa on fertility in male rats. Iraqi Journal of Veterinary Sciences 23: 123-128.

Al-Zahrani, S., Mohany, M., Kandeal, S. & Badr, G. 2012. Thymoquinone and vitamin E supplementation improve the reproductive characteristics of heat stressed male mice. Journal of Medicinal Plants Research 6(3): 493-499.

Ashraf, S.S., Rao, M.V., Kaneez, F.S., Qadri, S., Al-Marzouqi, A.H., Chandranath, I.S. & Adem, A. 2011. Nigella sativa extract as a potent antioxidant for petrochemical-induced oxidative stress. Journal of Chromatographic Science 49(4): 321-326.

Atanassova, M., Gerogieva, S. & Ivancheva, K. 2011. Total phenolic and total flavonoid contents: Antioxidant capacity and biological contaminants in medicinal herbs. Journal of the University of Chemical Technology and Metallurgy 46(1): 81-88.

Aumuller, G., Giers, K., Giers, U., Volk, A. & Seitz, J. 1981. p-Chlorophennylalanine-induced proliferation of the seminal vesicle epithelium. Cell and Tissue Research 219: 159-172.

Awah, F.M., Uzoegwu, P.N., Ifeonu, P., Oyugi, J.O., Rutherford, J., Yao, X., Fehrmann, F., Fowke, K.R. & Eze, M.O. 2012. Free radical scavenging activity: Phenolic contents and cytotoxicity of selected Nigerian medicinal plants. Food Chemistry 131(4): 1279-1286.

Banerjee, P.P., Banerjee, S. & Brown, T.R. 2001. Increased androgen receptor expression correlates with development of age-dependent, lobe-specific spontaneous hyperplasia of the Brown Norway rat prostate. Endocrinology 142: 4066-4075.

Burits, M. & Bucar, F. 2000. Antioxidant activity of Nigella sativa essential oil. Phytotherapy Research 14: 323-328.

Chen, M.T., Cheng, G.W., Lin, C.C., Chen, B.H. & Huang, Y.L. 2006. Effects of acute manganese chloride exposure on lipid peroxidation and alteration of trace metals in rat brain. Biological Trace Element Research 110: 163-177.

D’Cruz, S.C., Vaithinathna, S., Jubendradass, R. & Mathur, P.P. 2010. Effects of plants and plant products on the testis. Asian Journal of Andrology 12: 468.

Elbetieha, A., Bataineh, H., Darmani, H. & Al-Hamood, M. 2011. Effect of long-term exposure to manganese chloride on fertility of male and female mice. Toxicology Letters 119: 193-201.

Gamal, S.A.E., Magdy, O.E. & Raid, M.H. 2016. Protective effect of Eruca sativa seed oil against oral nicotine induced testicular damage in rats. Tissue and Cell 48: 340-348.

Ismail, M., Al-Naqeep, G. & Chan, K.W. 2010. Nigella sativa-thymoquinone-rich fraction greatly improves plasma antioxidant capacity and expression of antioxidant genes in hypercholesterolemic rats. Free Radical Biology and Medicine 48(5): 664-672.

Kiziler, A.R., Aydemir, B., Onaran, I., Alici, B., Ozkara, H., Gulyasar, T. & Akyolcu, M.C. 2007. High levels of cadmium and lead in seminal fluid and blood of smoking men are associated with high oxidative stress and damage in infertile subjects. Biological Trace Element Research 120(1-3): 82-91.

Kolahdooz, M., Nasri, S., Zadeh, M.S., Kianbakht, S. & Fallah, H.H. 2014. Effects of Nigella sativa L. oil on abnormal semen quality in infertile men: A randomized double-blind, placebo-controlled clinical trial. Phytomedicine 21: 901-905.

Lina, S., Hashida, N.H. & Eliza, H. 2014. Role of Habbatus sauda towards the histological features of nicotine treated male rats seminal vesicle and prostate gland. Biomedical Research 25(1): 11-18.

Madeha, N.A., Haddad, A.E.R., Amani, M.A. & Mazin, A.Z. 2018. Nigella sativa oil protects against tartrazine toxicity in male rats. Toxicology Reports 5: 146-155.

McDonald, A. 2004. A botanical perspective on the identity of Soma (Nelumbo nucifera Gaerin) based on scriptural and iconographic records. Economic Botany 58(sp1): S147-S173.

Meikle, A.W., Liu, X.H., Taylor, G.N. & Stringham, J.D. 1988. Nicotine and cotinine effects on 3-alpha hydroxysteroid dehydrogenase in canine prostate. Life Sciences 43: 1845- 1850.

Oyeyipo, I.P., Raji, Y. & Bolarinwa, A.F. 2015. Nitric oxide synthase inhibition ameliorates nicotine-induced sperm function decline in male rats. Asian Pacific Journal of Reproduction 4(3): 212-216.

Oyeyipo, I.P., Raji, Y., Emikpe, B.O. & Bolarinwa, A.F. 2011. Effects of nicotine on sperm characteristics and fertility profile in adult male rats: A possible role of cessation. Journal of Reproduction and Infertility 12(3): 201-207.

Oyeyipo, I.P., Raji, Y., Emikpe, B.O. & Bolarinwa, A.F. 2010. Effects of oral administration of nicotine on organ weight, serum testosterone level and testicular histology in adult male rats. Nigerian Journal of Physiological Sciences 25: 81-86.

Parveen, N. & Shadabig, G.G. 2011. Ameliorative action of Nigella sativa against iron induced chromosomal aberrations in rat bone marrow cells in vivo. International Journal of Pharmaceutical Biological Sciences 2: 470.

Reddy, S., Londonkar, R. & Patil, S.B. 1998. Testicular changes due to graded doses of nicotine in albino mice. Indian Journal of Physiology and Pharmacology 42: 276-280.

Reza, M., Javad, H. & Nazli, N. 2015. Effects of black seeds (Nigella sativa) on male infertility: A systematic review. Journal of Herbal Medicine 5: 133-139.

Safarinejad, M.R. & Safarinejad, S. 2012. The roles of omega-3 and omega-6 fatty acids in idiopathic male infertility. Asian Journal of Andrology 14: 514.

Sankako, M.K., Garcia, P.C., Piffer, R.C. & Pereira, O.M. 2013. Semen and reproductive parameters during some abstinence periods after cigarette smoke exposure in male rats. Brazilian Archives of Biology and Technology 56(1): 93-100.

Sayed Gabry, M., Dina, H.A.K., Maiada, M. & Asamaa, A.B.H.E. 2014. Effect of some antioxidants on the prostate of adult and aged albino rats: A histological and immunohistochemical study. Journal of Applied Pharmaceutical Sciences 4(2): 17-26.

Sunanda, P., Panda, B., Dash, C., Ray, P.K., Pahdy, R.N. & Routray, P. 2014. Prevalence of abnormal spermatozoa in tobacco chewing sub-fertile males. Journal of Human Reproductive Sciences 7(2): 136-142.

Tawfeek, F., Ahmed, S., Soulaf, J. & Kakel, S. 2006. Effect of Nigella sativa oil treatment on the sex organs and sperm charactors in rats exposed to hydrogen peroxide. Mesopotamia Journal of Agriculture 34: 1-7.

Thompson, S.A. & Heidger Jr., P.M. 1978. Synergistic effects of prolaction and testosterone in the restoration of rat prostatic epithelium following castration. Anatomical Record 191: 31-46.

Wright, A.S., Thomas, L.N., Douglas, R.C., Lazier, C.B. & Rittmaster, R.S. 1996. Relative potency of testosterone and dihydrotestosterone in preventing atrophy and apoptosis in the prostate of the castrated rat. The Journal of Clinical Investigation 98(11): 2558-2563.

Yeh, J., Barbieri, R.L. & Friedman, A.J. 1989. Nicotine and cotinine inhibit rat testis androgen biosynthesis in vitro. Journal of Steroid Biochemistry 33: 627-630.

Zahra, G., Shahrzad, M. & Hossein, B. 2016. Preclinical and clinical effects of Nigella sativa and its constituent, thymoquinone: A review. Journal of Ethnopharmacology 190: 372-386.

Zenzes, M.A. 2000. Smoking and reproduction: Gene damage to human gametes and embryos.Human Reproduction. Update 6(2): 122.

*Pengarang untuk surat-menyurat; email: nhhpasum@um.edu.my