Skip to main content
SpringerLink
Log in

Iprodione and/or chlorpyrifos exposure induced testicular toxicity in adult rats by suppression of steroidogenic genes and SIRT1/TERT/PGC-1α pathway

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

There is cumulative evidence that iprodione (IPR) fungicide and chlorpyrifos (CPF) insecticide are endocrine disruptors that can evoke reproductive toxicity. Yet, the underlying mechanisms are still unclear. Besides, the outcomes of their co-exposure to male sexual behavior and male fertility are still unknown. The effects of IPR (200 mg/kg b.wt) and CPF (7.45 mg/kg b.wt) single or mutual exposure for 65 days on sexual behavior, sex hormones, testicular enzymes, testis, and accessory sex gland histomorphometric measurements, apoptosis, and oxidative stress biomarkers were investigated. In addition, expression of nuclear receptor subfamily group A (NR5A1), 17β-hydroxysteroid dehydrogenase (HSD17B3), silent information regulator type-1 (SIRT1), telomerase reverse transcriptase (TERT), and peroxisome proliferator-activated receptor gamma coactivator 1-alpha (PGC-1α) genes has been assessed. Our results revealed that the individual or concurrent IPR and CPF exposure significantly disturb the sexual behavior, semen characteristics, testicular enzymes, and male hormones level. Oxidative stress caused by IPR and CPF activates apoptosis by inducing Caspase-3 and reducing Bcl-2. Downregulation of HSD17B3, NR5A1, and SIRT1/TERT/PGC-1α pathway was evident. Of note, most of these disturbances were exaggerated in rats co-exposed to IPR and CPF compared to IPR or CPF alone. Conclusively, our findings verified that IPR and CPF possibly damage the male reproductive system, and concurrent exposure should be avoided.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Data availability

The datasets used and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  • Adedara IA, Alake SE, Adeyemo MO, Olajide LO, Ajibade TO, Farombi EO (2018a) Taurine enhances spermatogenic function and antioxidant defense mechanisms in testes and epididymis of L-NAME-induced hypertensive rats. Biomed Pharmacother 97:181–189

    Article  CAS  Google Scholar 

  • Adedara IA, Owoeye O, Ajayi BO, Awogbindin IO, Rocha JBT, Farombi EO (2018b) Diphenyl diselenide abrogates chlorpyrifos-induced hypothalamic-pituitary-testicular axis impairment in rats. Biochem Biophys Res Commun 503:171–176

    Article  CAS  Google Scholar 

  • Ågmo A (1997) Male rat sexual behavior. Brain Res Protocol 1:203–209

    Article  Google Scholar 

  • Akhtar N, Srivastava M, Raizada R (2009) Assessment of chlorpyrifos toxicity on certain organs in rat, Rattus norvegicus. J Environ Biol 30:1047–1053

    CAS  Google Scholar 

  • Ambali SF, Akanbi DO, Oladipo OO, Yaqub LS, Kawu MU (2011) Subchronic chlorpyrifos-induced clinical, hematological and biochemical changes in Swiss albino mice: protective effect of vitamin E. Int J Biol Med Res 2(2):497–503

    Google Scholar 

  • Anamthathmakula P, Miryala CSJ, Moreci RS, Kyathanahalli C, Hassan SS, Condon JC, Jeyasuria P (2019) Steroidogenic factor 1 (Nr5a1) is required for sertoli cell survival post sex determination. Sci Rep 9:4452

    Article  CAS  Google Scholar 

  • Angioni A, Dedola F, Garau A, Sarais G, Cabras P, Caboni P (2011) Chlorpyrifos residues levels in fruits and vegetables after field treatment. J Environ Sci Health B 46:544–549

    CAS  Google Scholar 

  • Arisha AH, Moustafa A (2019) Potential inhibitory effect of swimming exercise on the Kisspeptin–GnRH signaling pathway in male rats. Theriogenology 133:87–96

    Article  CAS  Google Scholar 

  • Awobajo FO, Raji Y, Akinloye AK (2010) Histomorphometric changes in the testes and epididymis of Wistar strain Albino rats following fourteen days oral administration of therapeutic doses of some antibiotics. Int J Morphol 28:1281–1287

    Article  Google Scholar 

  • Babazadeh M, Najafi G (2017) Effect of chlorpyrifos on sperm characteristics and testicular tissue changes in adult male rats. Vet Res Forum 8:319–326

    Google Scholar 

  • Bai J-P, Shi Y-L (2002) Inhibition of Ca2+ channels in mouse spermatogenic cells by male antifertility compounds from Tripterygium wilfordii Hook. f. Contraception 65:441–445

    Article  CAS  Google Scholar 

  • Beutler E, Duron O, Kelly BM (1963) Improved method for the determination of blood glutathione. J Lab Clin Med 61:882–888

    CAS  Google Scholar 

  • Bletsou AA, Hanafi AH, Dasenaki ME, Thomaidis NS (2013) Development of specific LC-ESI-MS/MS methods to determine bifenthrin, lufenuron, and iprodione residue levels in green beans, peas, and chili peppers under Egyptian field conditions. Food Anal Methods 6:1099–1112

    Article  Google Scholar 

  • Blystone CR, Lambright CS, Furr J, Wilson VS, Gray LE Jr (2007a) Iprodione delays male rat pubertal development, reduces serum testosterone levels, and decreases ex vivo testicular testosterone production. Toxicol Lett 174:74–81

    Article  CAS  Google Scholar 

  • Blystone CR, Lambright CS, Furr J, Wilson VS, Gray LE (2007b) Iprodione delays male rat pubertal development, reduces serum testosterone levels, and decreases ex vivo testicular testosterone production. Toxicol Lett 174:74–81

    Article  CAS  Google Scholar 

  • Burke RD, Todd SW, Lumsden E, Mullins RJ, Mamczarz J, Fawcett WP, Gullapalli RP, Randall WR, Pereira EF, Albuquerque EX (2017) Developmental neurotoxicity of the organophosphorus insecticide chlorpyrifos: from clinical findings to preclinical models and potential mechanisms. J Neurochem 142:162–177

    Article  CAS  Google Scholar 

  • Callahan CL, Hamad LA, Olson JR, Ismail AA, Abdel-Rasoul G, Hendy O, Rohlman DS, Bonner MR (2017) Longitudinal assessment of occupational determinants of chlorpyrifos exposure in adolescent pesticide workers in Egypt. Int J Hyg Environ Health 220:1356–1362

    Article  CAS  Google Scholar 

  • Celeiro M, Llompart M, Lamas JP, Lores M, Garcia-Jares C, Dagnac T (2014) Determination of fungicides in white grape bagasse by pressurized liquid extraction and gas chromatography tandem mass spectrometry. J Chromatogr A 1343:18–25

    Article  CAS  Google Scholar 

  • Chaufan G, Galvano C, Nieves M, Mudry MD, Ríos de Molina MDC, Andrioli NB (2019) Oxidative response and micronucleus centromere assay in HEp-2 cells exposed to fungicide iprodione. Chem Res Toxicol 32:745–752

    Article  CAS  Google Scholar 

  • Clermont Y (1972) Kinetics of spermatogenesis in mammals: seminiferous epithelium cycle and spermatogonial renewal. Physiol Rev 52:198–236

    Article  CAS  Google Scholar 

  • Coussens M, Maresh JG, Yanagimachi R, Maeda G, Allsopp R (2008) Sirt1 deficiency attenuates spermatogenesis and germ cell function. PLoS One 3:e1571

    Article  CAS  Google Scholar 

  • Dai W, Chen H, Yu R, He L, Chen B, Chen X (2010) Effects of cadmium on telomerase activity, expressions of TERT, c-myc and P53, and apoptosis of rat hepatocytes. J Huazhong Univ Sci Technol [Medical Sciences] 30:709–713

  • Docea AO, Goumenou M, Calina D, Arsene AL, Dragoi CM, Gofita E, Pisoschi CG, Zlatian O, Stivaktakis PD, Nikolouzakis TK (2019) Adverse and hormetic effects in rats exposed for 12 months to low dose mixture of 13 chemicals: RLRS part III. Toxicol Lett 310:70–91

    Article  CAS  Google Scholar 

  • Dogheim SM, Gad Alla SA, El-Marsafy AM (2001) Monitoring of pesticide residues in Egyptian fruits and vegetables during 1996. J AOAC Int 84(2):519–531

  • El-Tawil MF (2014) Toxicological effects of short-term feeding with chlorpyrifos and chlorpyrifos-methyl insecticides on adult albino rats. Middle East J Agric Res 3:208–220

    Google Scholar 

  • Esterbauer H, Cheeseman KH, Dianzani MU, Poli G, Slater TF (1982) Separation and characterization of the aldehydic products of lipid peroxidation stimulated by ADP-Fe2+ in rat liver microsomes. Biochem J 208:129–140

    Article  CAS  Google Scholar 

  • European Food Safety Authority (2018) The 2016 European Union report on pesticide residues in food. EFSA J 16:e05348

    Article  Google Scholar 

  • Ezzi L, Salah IB, Haouas Z, Sakly A, Grissa I, Chakroun S, Kerkeni E, Hassine M, Mehdi M, Cheikh HB (2016) Histopathological and genotoxic effects of chlorpyrifos in rats. Environ Sci Pollut Res 23:4859–4867

    Article  CAS  Google Scholar 

  • Farag AT, Radwan AH, Sorour F, El Okazy A, El-Agamy E-S, El-Sebae AE-K (2010) Chlorpyrifos induced reproductive toxicity in male mice. Reprod Toxicol 29:80–85

  • Filler R (1993) Methods for evaluation of rat epididymal sperm morphology. Methods Toxicol 3:334–343

    Google Scholar 

  • Foong SY, Ma NL, Lam SS, Peng W, Low F, Lee BH, Alstrup AK, Sonne C (2020) A recent global review of hazardous chlorpyrifos pesticide in fruit and vegetables: prevalence, remediation and actions needed. J Hazard Mater 400:123006

    Article  CAS  Google Scholar 

  • González-Rodríguez RM, Rial-Otero R, Cancho-Grande B, Simal-Gándara J (2008) Occurrence of fungicide and insecticide residues in trade samples of leafy vegetables. Food Chem 107:1342–1347

    Article  CAS  Google Scholar 

  • Grabke A, Fernández-Ortuño D, Amiri A, Li X, Peres NA, Smith P, Schnabel G (2014) Characterization of iprodione resistance in Botrytis cinerea from strawberry and blackberry. Phytopathology 104:396–402

    Article  CAS  Google Scholar 

  • Guido C, Santoro M, De Amicis F, Perrotta I, Panza S, Rago V, Cesario MG, Lanzino M, Aquila S (2014) Human sperm anatomy and endocrinology in varicocele: role of androgen receptor. Reproduction 147:589–598

    Article  CAS  Google Scholar 

  • Hafez E (1970) Rabbits. Reproduction and breeding techniques for laboratory animals, pp 273–315

    Google Scholar 

  • Hallal N, El Sabbouri HEK, Salami A, Ramadan W, Khachfe H, Moustafa ME, Khalil M, Joumaa WH (2019) Impacts of prolonged chlorpyrifos exposure on locomotion and slow-and fast-twitch skeletal muscles contractility in rats. Toxicol Rep 6:598–606

    Article  CAS  Google Scholar 

  • Hassan MA, El Bohy KM, El Sharkawy NI, Imam TS, El-Metwally AE, Hamed Arisha A, Mohammed HA, Abd-Elhakim YM (2021) Iprodione and chlorpyrifos induce testicular damage, oxidative stress, apoptosis and suppression of steroidogenic-and spermatogenic-related genes in immature male albino rats. Andrologia 53:e13978

    Article  CAS  Google Scholar 

  • He X, Wu C, Cui Y, Zhu H, Gao Z, Li B, Hua J, Zhao B (2017) The aldehyde group of gossypol induces mitochondrial apoptosis via ROS-SIRT1-p53-PUMA pathway in male germline stem cell. Oncotarget 8:100128–100140

    Article  Google Scholar 

  • Heikal TM, Mossa A, Ibrahim AW, Abdel-Hamid HF (2014) Oxidative damage and reproductive toxicity associated with cyromazine and chlorpyrifos in male rats: the protective effects of green tea extract. Res J Environ Toxicol 8:53–67

    Article  CAS  Google Scholar 

  • Hernández AH, Curi R, Salazar LA (2015) Selection of reference genes for expression analyses in liver of rats with impaired glucose metabolism. Int J Clin Exp Patho 8:3946

  • Hull EM, Wood RI, McKenna KE (2006) Neurobiology of male sexual behavior. Knobil Neill’s Physiol Reprod 3:1729–1824

  • Hussein RM, Mohamed WR, Omar HA (2018) A neuroprotective role of kaempferol against chlorpyrifos-induced oxidative stress and memory deficits in rats via GSK3β-Nrf2 signaling pathway. Pestic Biochem Physiol 152:29–37

    Article  CAS  Google Scholar 

  • Ibrahim MA, Abd-El-Rahman HMA, M RZ, Abeer EE-M (2016) Studies on some biochemical, hormonal, histopathological and seminal characters in relation to rutting and non-rutting season in camels. Alex J Vet Sci 49:189–202

    Google Scholar 

  • Jaiswal C, Verma Y (2012) Effect of α-tocopherol on haematological alteration induced by chlorpyrifos in albino rats. Haryana Vet 51:108–110

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Justulin LA Jr, Ureshino RP, Zanoni M, Felisbino SL (2006) Differential proliferative response of the ventral prostate and seminal vesicle to testosterone replacement. Cell Biol Int 30:354–364

    Article  CAS  Google Scholar 

  • Khawar MB, Liu C, Gao F, Gao H, Liu W, Han T, Wang L, Li G, Jiang H, Li W (2021) Sirt1 regulates testosterone biosynthesis in Leydig cells via modulating autophagy. Protein & Cell 12:67–75

    Article  CAS  Google Scholar 

  • Kolthur-Seetharam U, Teerds K, de Rooij DG, Wendling O, McBurney M, Sassone-Corsi P, Davidson I (2009) The histone deacetylase SIRT1 controls male fertility in mice through regulation of hypothalamic-pituitary gonadotropin signaling. Biol Reprod 80:384–391

    Article  CAS  Google Scholar 

  • Koracevic D, Koracevic G, Djordjevic V, Andrejevic S, Cosic V (2001) Method for the measurement of antioxidant activity in human fluids. J Clin Pathol 54:356–361

    Article  CAS  Google Scholar 

  • Kumar A, Margekar SL, Margekar P, Margekar V (2018) Recent advances in management of organophosphate & carbamate poisoning. Indian J Med Spec 9:154–159

    Article  Google Scholar 

  • Laporte B, Gay-Quéheillard J, Bach V, Villégier A-S (2018) Developmental neurotoxicity in the progeny after maternal gavage with chlorpyrifos. Food Chem Toxicol 113:66–72

    Article  CAS  Google Scholar 

  • Lehrer RI, Lu W (2012) α-Defensins in human innate immunity. Immunol Rev 245:84–112

    Article  CAS  Google Scholar 

  • Li J, Liu X, Ren C, Li J, Sheng F, Hu Z (2009) In vitro study on the interaction between thiophanate methyl and human serum albumin. J Photochem Photobiol B Biol 94:158–163

    Article  CAS  Google Scholar 

  • Li J, Ren F, Li Y, Luo J, Pang G (2019) Chlorpyrifos induces metabolic disruption by altering levels of reproductive hormones. J Agric Food Chem 67:10553–10562

    Article  CAS  Google Scholar 

  • Li R, He L, Wei W, Hao L, Ji X, Zhou Y, Wang Q (2015) Chlorpyrifos residue levels on field crops (rice, maize and soybean) in China and their dietary risks to consumers. Food Control 51:212–217

    Article  CAS  Google Scholar 

  • Lin CH, Li NT, Cheng HS, Yen ML (2018) Oxidative stress induces imbalance of adipogenic/osteoblastic lineage commitment in mesenchymal stem cells through decreasing SIRT1 functions. J Cell Mol Med 22:786–796

    CAS  Google Scholar 

  • Lin S-Y, Elledge SJ (2003) Multiple tumor suppressor pathways negatively regulate telomerase. Cell 113:881–889

    Article  CAS  Google Scholar 

  • Liu C, Song Z, Wang L, Yu H, Liu W, Shang Y, Xu Z, Zhao H, Gao F, Wen J (2017) Sirt1 regulates acrosome biogenesis by modulating autophagic flux during spermiogenesis in mice. Development 144:441–451

    CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods (San Diego, Calif) 25:402–408

    Article  CAS  Google Scholar 

  • Loutfy N, Malhat F, Kamel E, Saber A (2015) Residual pattern and dietary intake of iprodione on grapes under Egyptian field conditions: a prelude to risk assessment profile. Hum Ecol Risk Assess 21:265–279

    Article  CAS  Google Scholar 

  • Ma M, Chen C, Yang G, Wang Y, Wang T, Li Y, Qian Y (2019) Combined anti-androgenic effects of mixtures of agricultural pesticides using in vitro and in silico methods. Ecotoxicol Environ Saf 186:109652

    Article  CAS  Google Scholar 

  • Mansour SA (2004) Pesticide exposure—Egyptian scene. Toxicology 198(1–3):91–115

  • Meggs WJ, Brewer KL (2007) Weight gain associated with chronic exposure to chlorpyrifos in rats. J Med Toxicol 3:89–93

    Article  Google Scholar 

  • Mehrpour O, Karrari P, Zamani N, Tsatsakis AM, Abdollahi M (2014) Occupational exposure to pesticides and consequences on male semen and fertility: a review. Toxicol Lett 230:146–156

    Article  CAS  Google Scholar 

  • Morgan AM, El-Aty AA (2008) Reproductive toxicity evaluation of Pestban insecticide exposure in male and female rats. Toxicol Res 24:137–150

    Article  CAS  Google Scholar 

  • Nakayama A, Okawa H, Zheng M, Pu S, Watanabe G, Ohta R. Kawaguchi M (2018) Male Hatano low-avoidance rats show more active sexual behavior with lower plasma testosterone than high-avoidance rats. J Vet Med Sci 17-0668

  • Omirou M, Vryzas Z, Papadopoulou-Mourkidou E, Economou A (2009) Dissipation rates of iprodione and thiacloprid during tomato production in greenhouse. Food Chem 116:499–504

    Article  CAS  Google Scholar 

  • Pascual P, Martinez-Lara E, Barcena JA, Lopez-Barea J, Toribio F (1992) Direct assay of glutathione peroxidase activity using high-performance capillary electrophoresis. J Chromatogr 581:49–56

    Article  CAS  Google Scholar 

  • Payne A (1996) Structure, function and regulation of steroidogenic enzymes in the Leydig cell. Leydig Cell:259–268

  • Peiris DC, Dhanushka T (2017) Low doses of chlorpyrifos interfere with spermatogenesis of rats through reduction of sex hormones. Environ Sci Pollut Res 24:20859–20867

    Article  CAS  Google Scholar 

  • Perez-Fernandez C, Morales-Navas M, Aguilera-Sáez LM, Abreu AC, Guardia-Escote L, Fernández I, Garrido-Cárdenas JA, Colomina MT, Giménez E, Sánchez-Santed F (2020) Medium and long-term effects of low doses of Chlorpyrifos during the postnatal, preweaning developmental stage on sociability, dominance, gut microbiota and plasma metabolites. Environ Res 184:109341

    Article  CAS  Google Scholar 

  • Pisani C, Voisin S, Arafah K, Durand P, Perrard M-H, Guichaoua M-R, Bulet P, Prat O (2016) Ex vivo assessment of testicular toxicity induced by carbendazim and iprodione, alone or in a mixture. ALTEX-Altern Anim Exp 33:393–413

    Google Scholar 

  • Radice S, Marabini L, Gervasoni M, Ferraris M, Chiesara E (1998) Adaptation to oxidative stress: effects of vinclozolin and iprodione on the HepG2 cell line. Toxicology 129:183–191

    Article  CAS  Google Scholar 

  • Radice S, Ferraris M, Marabini L, Grande S, Chiesara E (2001) Effect of iprodione, a dicarboximide fungicide, on primary cultured rainbow trout (Oncorhynchus mykiss) hepatocytes. Aquat Toxicol 54:51–58

    Article  CAS  Google Scholar 

  • Rato L, Alves MG, Duarte AI, Santos MS, Moreira PI, Cavaco JE, Oliveira PF (2015) Testosterone deficiency induced by progressive stages of diabetes mellitus impairs glucose metabolism and favors glycogenesis in mature rat Sertoli cells. Int J Biochem Cell Biol 66:1–10

    Article  CAS  Google Scholar 

  • Rizzati V, Briand O, Guillou H, Gamet-Payrastre L (2016) Effects of pesticide mixtures in human and animal models: an update of the recent literature. Chem Biol Interact 254:231–246

    Article  CAS  Google Scholar 

  • Robbins A (1996) Androgens and male sexual behavior from mice to men. Trends Endocrinol Metab 7:345–350

    Article  CAS  Google Scholar 

  • Rone MB, Fan J, Papadopoulos V (2009) Cholesterol transport in steroid biosynthesis: role of protein–protein interactions and implications in disease states. Biochim Biophys Acta Mol Cell Biol Lipids 1791:646–658

    Article  CAS  Google Scholar 

  • Röpke A, Tewes A-C, Gromoll J, Kliesch S, Wieacker P, Tüttelmann F (2013) Comprehensive sequence analysis of the NR5A1 gene encoding steroidogenic factor 1 in a large group of infertile males. Eur J Hum Genet 21:1012–1015

    Article  CAS  Google Scholar 

  • Rose G, Lane S, Jordan R (2009) The fate of fungicide and insecticide residues in Australian wine grape by-products following field application. Food Chem 117:634–640

    Article  CAS  Google Scholar 

  • Sahin E, Colla S, Liesa M, Moslehi J, Müller FL, Guo M, Cooper M, Kotton D, Fabian AJ, Walkey C (2011) Telomere dysfunction induces metabolic and mitochondrial compromise. Nature 470:359–365

    Article  CAS  Google Scholar 

  • Sakr SA, Mahran HA, Nofal AE (2012) Effect of selenium on carbimazole-induced histopathological and histochemical alterations in prostate of albino rats. Am J Med Med Sci 2:5–11

    Article  Google Scholar 

  • Seed J, Chapin RE, Clegg ED, Dostal LA, Foote RH, Hurtt ME, Klinefelter GR, Makris SL, Perreault SD, Schrader S (1996) Methods for assessing sperm motility, morphology, and counts in the rat, rabbit, and dog: a consensus report. Reprod Toxicol 10:237–244

    Article  CAS  Google Scholar 

  • Seo S, Lee M-S, Chang E, Shin Y, Oh S, Kim I-H, Kim Y (2015) Rutin increases muscle mitochondrial biogenesis with AMPK activation in high-fat diet-induced obese rats. Nutrients 7:8152–8169

  • Sharma A, Shukla A, Attri K, Kumar M, Kumar P, Suttee A, Singh G, Barnwal RP, Singla N (2020) Global trends in pesticides: a looming threat and viable alternatives. Ecotoxicol Environ Saf 201:110812

    Article  CAS  Google Scholar 

  • Sharma P, Huq AU, Singh R (2014) Cypermethrin-induced reproductive toxicity in the rat is prevented by resveratrol. J Hum Reprod Sci 7:99

    Article  CAS  Google Scholar 

  • Shittu M, Ayo J, Ambali S, Fatihu M, Onyeanusi B, Kawu M (2012) Chronic chlorpyrifos-induced oxidative changes in the testes and pituitary gland of Wistar rats: ameliorative effects of vitamin C. Pestic Biochem Physiol 102:79–85

    Article  CAS  Google Scholar 

  • Stensvand A, Christiansen A (2000) Investigation on fungicide residues in greenhouse-grown strawberries. J Agric Food Chem 48:917–920

    Article  CAS  Google Scholar 

  • Suvarna KS, Layton C, Bancroft JD (2018) Bancroft's theory and practice of histological techniques E-Book. Elsevier Health Sciences

  • Vachharajani VT, Liu T, Wang X, Hoth JJ, Yoza BK, McCall CE (2016) Sirtuins link inflammation and metabolism. J Immunol Res 2016:1–10

    Article  CAS  Google Scholar 

  • Visalakshmi V, Raju M, Rao AU, Kumar KM, Satyanarayana NH (2016) Compatibility and efficacy of insecticide and fungicide combinations on major pests and sheath blight of paddy. Nat Environ Pollut Technol 15:233

    CAS  Google Scholar 

  • Wang X-l, Wu L-y, Zhao L, L-n S, H-y L, Liu G, Guan G-j (2016) SIRT1 activator ameliorates the renal tubular injury induced by hyperglycemia in vivo and in vitro via inhibiting apoptosis. Biomed Pharmacother 83:41–50

    Article  CAS  Google Scholar 

  • Wang X, Xu G, Wang F, Sun H, Li Y (2012) Iprodione residues and dissipation rates in tobacco leaves and soil. Bull Environ Contam Toxicol 89:877–881

    Article  CAS  Google Scholar 

  • Wang Z, Cang T, Qi P, Zhao X, Xu H, Wang X, Zhang H, Wang X (2015) Dissipation of four fungicides on greenhouse strawberries and an assessment of their risks. Food Control 55:215–220

    Article  CAS  Google Scholar 

  • Watts M (2012) Chlorpyrifos as a possible global POP. Pesticide Action Network North America, Oakland, CA. https://scholar.google.com.eg/scholar?hl=en&as_sdt=0%2C5&q=Watts%2C+M.%282012%29%3A+Chlorpyrifos+as+a+possible+global+POP.+Pesticide+Action+Network+North+America%2C+Oakland%2C+CA.+www.+paneurope.+info%2FNews%2FPR%2F121009_Chlorpyrifos_as_POP_final.+pdf.&btnG=

  • Weikert S, Christoph F, Schulze W, Krause H, Kempkensteffen C, Schostak M, Miller K, Schrader M (2006) Testicular expression of survivin and human telomerase reverse transcriptase (hTERT) associated with spermatogenic function in infertile patients. Asian J Androl 8:95–100

    Article  CAS  Google Scholar 

  • Wood MA, Mukherjee P, Toocheck CA, Walker WH (2011) Upstream stimulatory factor induces Nr5a1 and Shbg gene expression during the onset of rat Sertoli cell differentiation. Bio Reprod 85:965–976

  • Wu X, Guo X, Wang H, Zhou S, Li L, Chen X, Wang G, Liu J, Ge H-S, Ge R-S (2017) A brief exposure to cadmium impairs Leydig cell regeneration in the adult rat testis. Sci Rep 7:1–11

  • Xu L, Luo G, Sun Y, Huang S, Xu D, Xu G, Han Z, Gu Z, Zhang Y (2020) Multiple down-regulated cytochrome P450 monooxygenase genes contributed to synergistic interaction between chlorpyrifos and imidacloprid against Nilaparvata lugens. J Asia-Pac Entomol 23:44–50

    Article  Google Scholar 

  • Xu M-Y, Wang P, Sun Y-J, Wu Y-J (2017) Metabolomic analysis for combined hepatotoxicity of chlorpyrifos and cadmium in rats. Toxicology 384:50–58

    Article  CAS  Google Scholar 

  • Xu M-Y, Wang P, Sun Y-J, Wu Y-J (2018) Disruption of kidney metabolism in rats after subchronic combined exposure to low-dose cadmium and chlorpyrifos. Chem Res Toxicol 32:122–129

    Article  CAS  Google Scholar 

  • Yang X, Luo J, Li S, Liu C (2016) Evaluation of nine pesticide residues in three minor tropical fruits from southern China. Food Control 60:677–682

    Article  CAS  Google Scholar 

  • Yang YY, Lai CT (2019) Synergistic effect and field control efficacy of the binary mixture of permethrin and chlorpyrifos to brown planthopper (Nilaparvata lugens). J Asia-Pac Entomol 22:67–76

    Article  Google Scholar 

  • Zhang X, Cui W, Wang K, Chen R, Chen M, Lan K, Wei Y, Pan C, Lan X (2020) Chlorpyrifos inhibits sperm maturation and induces a decrease in mouse male fertility. Environ Res 188:109785

    Article  CAS  Google Scholar 

  • Zidan N (2009) Evaluation of the reproductive toxicity of chlorpyrifos methyl, diazinon and profenofos pesticides in male rats. Int J Pharmacol 5:51–57

    Article  CAS  Google Scholar 

  • Zimmer KE, Montaño M, Olsaker I, Dahl E, Berg V, Karlsson C, Murk AJ, Skaare JU, Ropstad E, Verhaegen S (2011) In vitro steroidogenic effects of mixtures of persistent organic pollutants (POPs) extracted from burbot (Lota lota) caught in two Norwegian lakes. Sci Total Environ 409:2040–2048

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank all members of Forensic Medicine and Toxicology, Faculty of Veterinary Medicine, Zagazig University for their technical support during the study.

Author information

Authors and Affiliations

  1. Department of Forensic Medicine and Toxicology, Faculty of Veterinary Medicine, Zagazig University, Zagazig, Egypt

    Yasmina M. Abd-Elhakim, Nabela I. El Sharkawy, Khlood M. El Bohy, Mona A. Hassan & Tamer S. Imam

  2. Department of Veterinary Public Health, Faculty of Veterinary Medicine, Zagazig University, Zagazig, Egypt

    Heba S. A. Gharib

  3. Department of Pathology, Animal Reproduction Research Institute, Giza, Egypt

    Abeer E. El-Metwally

  4. Department of Animal Physiology and Biochemistry, Faculty of Veterinary Medicine, Badr University in Cairo (BUC), Badr City, Cairo, Egypt

    Ahmed Hamed Arisha

  5. Department of Physiology, Faculty of Veterinary Medicine, Zagazig University, Sharkia, Zagazig, Egypt

    Ahmed Hamed Arisha

Authors
  1. Yasmina M. Abd-Elhakim
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Nabela I. El Sharkawy
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Khlood M. El Bohy
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Mona A. Hassan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Heba S. A. Gharib
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Abeer E. El-Metwally
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ahmed Hamed Arisha
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Tamer S. Imam
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization: Yasmina M. Abd-Elhakim, Nabela I. El Sharkawy, and Khlood M. El Bohy. Data Curation: Mona A. Hassan and Yasmina M. Abd-Elhakim. Formal Analysis: Mona A. Hassan. Methodology: Mona A. Hassan, Yasmina M. Abd-Elhakim, and Tamer S. Imam. Histopathology: Abeer E. El-Metwally. Sexual behavior assassment: Heba S.A. Gharib. Gene expression analysis: Ahmed Hamed Arisha .Writing Original draft: Yasmina M. Abd-Elhakim and Mona A. Hassan. Review and Editing: Yasmina M. Abd-Elhakim and Tamer S. Imam.

Corresponding author

Correspondence to Mona A. Hassan.

Ethics declarations

Ethics approval

The authors of the current study confirm that all the experimental procedures were conducted in strict compliance with the ethical standards of the NIH guidelines on the care and use of laboratory animals to minimize the suffering of the experimental animals throughout the acclimatization, experimentation, and sampling. The ethical standards were approved by the Institutional Animal Care and Use Committee of Zagazig University, Egypt (ZU-IACUC/2/F/41/2019).

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Conflict of interest

The authors declare no competing interests.

Additional information

Responsible Editor: Ludek Blaha

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Abd-Elhakim, Y.M., El Sharkawy, N.I., El Bohy, K.M. et al. Iprodione and/or chlorpyrifos exposure induced testicular toxicity in adult rats by suppression of steroidogenic genes and SIRT1/TERT/PGC-1α pathway. Environ Sci Pollut Res 28, 56491–56506 (2021). https://doi.org/10.1007/s11356-021-14339-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-021-14339-x

Keywords

Search

Navigation