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The Effects of Methyl Tert-Butyl Ether (MTBE) on the Male Rat Reproductive System

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The Effects of Methyl Tert-Butyl Ether (MTBE) on the Male Rat Reproductive System Food and Chemical Toxicology 46 (2008) 2402–2408 Contents lists available at ScienceDirect Food and Chemical Toxicology journal homepage: www.elsevier.com/locate/foodchemtox The effects of methyl tert-butyl ether (MTBE) on the male rat reproductive system Dongmei Li a,b, Chuntao Yuan a,b, Yi Gong a,b, Yufeng Huang c, Xiaodong Han a,b,* a Immunology and Reproduction Biology Laboratory, Medical School, Nanjing University, Nanjing, Jiangsu 210093, China b Jiangsu Key Laboratory of Molecular Medicine, Nanjing University, Nanjing, Jiangsu 210093, China c Department of Biochemistry, Jinling Hospital, Clinical School of Medicine, Nanjing University, Nanjing, Jiangsu 210002, China article info abstract Article history: Methyl tert-butyl ether (MTBE) is an oxygenated compound, which has been widely used in Asia, Europe Received 15 October 2007 and North America. Although numerous in vitro and in vivo studies have demonstrated the carcinogenic- Accepted 23 March 2008 ity and the toxicity of MTBE, there is still a lack of data on reproductive system exposure of MTBE in male rodent animals. We studied subacute exposure of MTBE on the reproductive systems of male Sprague– Dawley rats. MTBE was administered to rats at dose levels of 0, 400, 800 and 1600 mg/kg/day. After 2 Keywords: or 4 weeks of treatments, the rats were euthanized, and their serum, epididymis and testes were col- Methyl tert-butyl ether (MTBE) lected. Significant adverse effects in their reproductive system were observed including: a significant Reproductive system increase in the percentage of abnormal sperm; an irregular and disordered arrangement of the seminif- Toxicity Oxidative stress erous epithelium indicated by a histopathological examination; changed serum levels of testosterone (T), luteinizing hormone (LH) and follicle stimulating hormone (FSH); and decreased levels of mRNA and of androgen binding protein (ABP). In the oxidative stress study, results indicated an increased maleic dial- dehyde (MDA) content, implying a raised peroxide level, and that the total antioxidant ability in serum was significantly increased. This finding was especially strong at 1600 mg/kg/day MTBE. In the 2-week treatment, at 1600 mg/kg/day, the mRNA level of 8-oxoguanine DNA glycosidase (OGG1) was signifi- cantly decreased, and the mRNA level of the extra-cellular form of superoxide dismutase (SODEX) was sig- nificantly increased. Our experiments suggest that relatively high doses of MTBE can exert reproductive system toxicity of male rats and disturb the secretions of T, LH and FSH, possibly due to oxidative stress induced by MTBE. Ó 2008 Elsevier Ltd. All rights reserved. 1. Introduction (Mehlman, 2000; Faulk and Gray, 2001). In view of this, a thorough understanding the characteristics of MTBE remains a priority. Methyl tert-butyl ether (MTBE) is commonly used as an octane Existing studies focused on the carcinogenicity of MTBE (Bel- booster and oxygenate additive in reformulated gasoline. MTBE in- poggi et al., 1997; Borghoff and Williams, 2000; Swenberg and Leh- creases the oxygen content of fuel, decreases carbon monoxide and man-McKeeman, 1999; Zhou et al., 2000). These studies have other hydrocarbon emissions, and reduces air pollution (USEPA, shown that the incidence of renal tubular adenomas and carcino- 1988). In the US, over 200,000 barrels (8 Â 106 l) of MTBE are pro- mas increased in MTBE-exposed male rats. The US environmental duced everyday and more than 1/3 of them are used (Energy Infor- protection agency (EPA), therefore, has listed MTBE as a potential mation Administration (EIA), 2003). In China, more than 1 billion human carcinogen (USEPA, 1998). Few research studies have been kilograms of MTBE are produced annually. However, a report made conducted to figure out the influence of MTBE on the reproductive by US Geological Survey stated that MTBE is the second most fre- systems of rodents. In both inhalation studies and gavage dosages, quently detected chemical in shallow urban monitoring wells it was found that MTBE induces interstitial cell tumors of the testes due to the physicochemical properties of MTBE (Simmons, 1996). in rats. (Belpoggi et al., 1995; Bird et al., 1997; Clegg et al., 1997). For this reason some states in US have either restricted or banned There were other studies on changes in testosterone (T), luteinizing using MTBE, though it is still widely used in Europe and Asia hormone (LH) levels in MTBE-exposed rats (Williams et al., 2000). Our previous studies indicated that a relatively high dose MTBE is directly toxic to spermatogenic cells of mice or rats (Li et al., * Corresponding author. Address: Immunology and Reproduction Biology Labo- 2006, 2007). However, there is still little knowledge on the mech- ratory, Medical School, Nanjing University, Nanjing, Jiangsu 210093, China. Tel./fax: +86 25 83686497. anism through which MTBE influences the male reproductive E-mail address: [email protected] (X. Han). system. 0278-6915/$ - see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.fct.2008.03.024 D. Li et al. / Food and Chemical Toxicology 46 (2008) 2402–2408 2403 Recently, Krayl et al. (2003) revealed that the energy conserva- Medicine, Nanjing University, according to the manufacturer’s instructions. The ser- tion system involving oxidative stress was very sensitive in the um from group A was first collected and stocked at À80 °C at the Two week mark. Two weeks later, the serum from group B was collected and measured together presence of MTBE by using the model organism Pseudomonas Put- with that from group A. Because commercially available kits are designed for hu- ida KT2440. In mammals, seminiferous epithelium is composed of man serum, the absolute levels of testosterone, FSH and LH could not be qualified two basic cell types: spermatogenic cells and Sertoli cells. It was but the comparative levels of these hormones could be ascertained. found that spermatogenesis, per se, required extensive tissue restructuring in the seminiferous epithelium, resulting in the pro- 2.3. Serum antioxidant and peroxide level determination duction of reactive oxygen species (ROS) and reactive nitrogen spe- The serum antioxidant ability and peroxide level determination including total cies (RNS). An extra-cellular form of superoxide dismutase (SODEX) antioxidant ability and Maleic Dialdehyde (MDA) content were analyzed with the synthesized and secreted by both spermatogenic cells and Sertoli assay kit. Many antioxidants can deoxidize Fe3+ to Fe2+, and the total antioxidant cells acts as an important member of antioxidant defense systems ability of serum was determined by colorimetry at 520 nm. Lipid peroxidation Thio- in rat testes to protect themselves from cellular damage and death barbituric acid-reactive species (TBARS) were determined according to Uchiyama and Mihara (1978), in which malondialdehyde (MDA), an end-product of fatty acid caused by free radicals (Mruk et al., 2002). peroxidation, reacts with thiobarbituric acid (TBA) to form a colored complex. The In this study, we measured the effects of a 2-or-4-week expo- amount of TBARS was measured at 532 nm. sure to MTBE on the reproductive system of male Sprague–Dawley rats, including measurements of the reproductive hormone level in 2.4. Sperm count and the semina deformity ratio serum, sperm count, semina deformity ratio, pathological observa- tion of testes, and the mRNA expression of androgen binding pro- One epididymis of each animal was isolated and cleared of adhering tissues. The cauda epididymis was chopped into small pieces (about 1 mm3) and incubated in tein (ABP) in the testes. We hypothesized that MTBE influences 10 ml of Ham’s F-12 medium at 32 °C for 1 h (Chitra et al., 2002). Then, 1 ml of male reproductive system through oxidative stress, and thus mea- the above solution was diluted with 9 ml Ham’s F-12 medium. The diluted solution sured the antioxidant and peroxide levels in the serum and testes, was transferred into each chamber of the haemocytometer, and sperm number was including the MDA content and total antioxidant ability in the ser- counted. To minimize subjective errors, all operations were performed by one per- son blinded to the group assignment of animals. Then 7–10 ll of suspended sperm um, mRNA expression of 8-oxoguanine DNA glycosidase (OGG1), was smeared on a slide and dyed with Wright Stain for microscopic examination. and extracellular form of superoxide dismutase (SODEX) in testes. 200 sperm of every animal were observed by recording 10–15 slides with an optical microscope (Nikon Corporation, Chiyoda-ku, Tokyo, Japan). The abnormal sperm 2. Materials and methods was observed and the percent of abnormal sperm was counted. Methyl tert-butyl ether (MTBE), CAS No. 1634-04-4, 99.8% of purity was pur- 2.5. Pathological observation chased from Tedia Company Inc. (Fairfield, OH, USA). Total antioxidant ability test kits and maleic dialdehyde (MDA) test kits were obtained from Nanjing Jiancheng Testicular tissue blocks were fixed in Bouin ’s Fluid (Zhen, 1978). Then, samples Bioengineering Inc. (Nanjing, China). testosterone (T), luteinizing hormone (LH) were sectioned by routine methods and this procedure was followed by H&E stain- and follicle stimulating hormone (FSH) Radioimmunoassay (RIA) kits were pur- ing. Sections were observed with an optical microscope (Nikon Corporation, chased from Beijing Furui Bioengineering Inc. (Beijing, China). Trizol, M–MLV Re- Chiyoda-ku, Tokyo, Japan). verse Transcriptase, dNTP mix and Ribonuclease Inhibitors were purchased from Promega. (Madison, WI, USA). 2ÂTaq PCR MasterMix was obtained from Tiangen Bio- 2.6. Expression of androgen binding protein (ABP), 8-oxoguanine DNA glycosidase tech (Beijing) Co. Ltd. (Beijing, China). All other chemicals were of analytical grade. (OGG1), extracellular form of superoxide dismutase (SODEX) mRNA in testes by RT–PCR 2.1. Animals and housing Total RNAs were extracted from testes with Trizol method. 2 lg RNA was rever- sely transcribed into cDNAs using 5 lg of oligo (dT)18 and an M-MLV reverse trans- Rats were utilized in accordance with federal guidelines for the humane care criptase kit (Promega, Madison, WI) in a final reaction volume of 20 ll.
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