Dose‐specific morphological changes in the Sertoli cell of the adult male Japanese quails testes exposed to di(n‐butyl)phthalate DBP prepubertally

Abstract

Di(n‐butyl) phthalates (DBP) are endocrine‐disrupting chemicals (EDCs) implicated in a number of reproductive disorders in humans and rodents. Previously, we have shown that DBP effects is anti‐androgenic and causing alterations in seminiferous tubular histology and impairment of Leydig cell steroidogenesis in the avian model. However, the ultrastructural changes on the Sertoli cell remain unclear. The present study was designed to assess, morphologically, the dose‐dependent toxic effect of pre‐pubertal exposure of the plasticizer‐DBP, on the histology and ultrastructure of the Sertoli cell. DBP was administered to 10‐week old male quail birds by oral gavage, with a control group given corn oil vehicle(1mL/kg) only, while the other five experimental groups were fed (1, 10, 50, 200– and 400mg/kgbwt/d DBP(dissolved in corn oil) , for a period of 30days. Testes were fixed in Bouin's liquid or in a mixture of 2.5% glutaraldehyde and 2% formaldehyde for analysis under light and electron microscopes(TEM), respectively. Histologically, the basal Sertoli cell cytoplasm in high DBP dosage levels (200mg and 400mg/kgbwt/d), increasingly displayed aggregations of lipid droplets, but only a few in the apical Sertoli cell cytoplasm. In addition, there was marked vacuolations in the lining germinal epithelium. Ultrastructurally, there were notable, dose‐dependent changes seen in the Sertoli cell in DBP‐treated birds, with low dosage groups displaying no obvious structural changes, while the DBP high‐dose resulted in a remarkable accumulation of numerous, scattered or usually, closely packed lipid droplets, found predominantly in the basal part of the Sertoli cell cytoplasm. In addition, there were several mis‐shaped or swollen mitochondria with electron lucent areas, indicative of early cellular degeneration. These degenerating mitochondria were characterized by swelling and deformation of the tubular cristae, resulting in a “moth‐eaten” appearance. These findings showed that high dose of DBP (200 and 400mg/kgbwt/d) administered daily for 30days significantly resulted in degenerative characteristics, such as the increase in lipid droplets, intra‐epithelial vacuolations and mitochondrial damage in the Sertoli cell. Thus, this study has provided a clear evidence that alterations in Sertoli cell morphology and function were involved in spermatogenic failure induced by DBP, in this specie.Support or Funding InformationThe research was supported by Ahmadu Bello University Board of Research and grants from the South African Veterinary/Novartis Wildlife Foundation.This abstract is from the Experimental Biology 2019 Meeting. There is no full text article associated with this abstract published in The FASEB Journal.

Changes in testicular histomorphometry and ultrastructure of Leydig cells in adult male Japanese quail exposed to di (n-butyl) phthalate (DBP) during the prepubertal period

“…It was previously demonstrated that PEs, including DBP, are anti-androgenic environmental contaminants that cause adverse biological effects on male reproductive health, growth, and development in both human and wildlife (Foster et al 2001 ; Oehlmann et al 2009 ; Alam et al 2010a ; Bello et al 2014 , 2019 ). Since reproductive development is a continuous process throughout ontogeny in vertebrate species, it is susceptible to changes in physiology due to exposure to environmental contaminants at different stages of development, including structural differentiation and hormonal synthesis (Diamanti-Kandarakis et al 2009 ).…”

“…This was expected since it has been established that spermatogenesis is particularly sensitive to several environmental toxicants in rats (Wong and Cheng 2011 ; Manfo et al 2014 ). The quail testis has also been shown to be susceptible to the effects of some environmental toxicants (Aire 2005 ; Bello et al 2014 , 2019 ). Furthermore, our present findings corroborate similar observations in rodents, showing that most phthalates adversely affect testicular differentiation; as well as adult spermatogenesis in the adult rodent by provoking germ cell loss, testicular atrophy, and altered Leydig cell function (Ge et al 2007 ; Spade et al 2015 ).…”

“…Exposure of adult male rats to high doses of certain phthalates resulted in rapid and severe changes in the testis (Dalgaard et al 2001 ). In testicular tissues, the primary cellular target of phthalate-induced exposure are Sertoli and/or Leydig cells, which exhibit biochemical and morphological changes (Moffit et al 2007 ; Shirai et al 2013 ; Wakui et al 2013 ; Bello et al 2014 ; 2019 ).…”

Effect of di(n‐butyl) phthalate on the blood–testis barrier during puberty onset

“…Exposure to DBP also alters the morphology of seminiferous tubule and impairs Leydig cell steroidogenesis (Bello et al, 2014;Zakariah et al, 2022). Although studies on the reproductive toxicological effects resulting from exposure to DBP have been conducted in the male Japanese quail (Bello et al, 2014(Bello et al, , 2019Ibrahim et al, 2021), there are no detailed reports on the effects of environmentally relevant concentrations of DBP on the Sertoli cell and junctional complexes of the BTB in the species. According to Tyler et al (2018), environmentally relevant concentrations of DBP are those in the low μg/L range, while Liu and Craig (2019) classified environmentally relevant levels of DBP as those between 10 and 100 μg/kg/day.…”

“…Exposure to phthalates transpires by intake of contaminated food, contact through the skin and inhalation of contaminated air (Heudorf et al, 2007; Olujimi et al, 2010). Previous studies have shown that phthalate exposure causes morphological and functional alterations in the male reproductive system of birds and mammals, with the Sertoli cell being the main cellular target for toxicants (Bao et al, 2011; Bello et al, 2019; Ibrahim et al, 2021; Kumar et al, 2015; Monsees et al, 2000).…”