Differential ontogenetic exposure to obesogenic environment induces hyperproliferative status and nuclear receptors imbalance in the rat prostate at adulthood

Pytlowanciv, Eloísa Zanin; Pinto-Fochi, Maria Etelvina; Reame, Vanessa; Gobbo, Marina Guimarães; Ribeiro, Daniele Lisboa; Taboga, Sebastião Roberto; Góes, Rejane Maira

doi:10.1002/pros.23158

Cited by 11 publications

(7 citation statements)

References 95 publications

(150 reference statements)

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“…Indeed, in a recent study comparing the effects of an obesogenic environment caused by HFD consumption at different stages of development, our group showed that the sperm damage was proportional to the metabolic impairment and the decline in circulating testosterone levels (Reame et al 2014). In addition, we also demonstrated that HFD exposure during different periods of ontogenetic development leads to prostate hypertrophy (Pytlowanciv et al 2016). It is thus relevant to compare the mechanisms underlying this steroidogenic impairment during different life periods as a result of exposure to excessive dietary fat.…”

Section: Introductionmentioning

confidence: 57%

A high-fat diet fed during different periods of life impairs steroidogenesis of rat Leydig cells

Pinto-Fochi¹,

Pytlowanciv²,

Reame³

et al. 2016

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This study evaluated the impact of a high-fat diet (HFD) during different stages of rat life, associated or not with maternal obesity, on the content of sex steroid hormones and morphophysiology of Leydig cells. The following periods of development were examined: gestation (O1), gestation and lactation (O2), from weaning to adulthood (O3), from lactation to adulthood (O4), gestation to adulthood (O5), and after sexual maturation (O6). The HFD contained 20% unsaturated fat, whereas the control diet had 4% fat. Maternal obesity was induced by feeding HFD 15 weeks before mating. All HFD groups presented increased body weight, hyperinsulinemia and reduced insulin sensitivity. Except for O1, all HFD groups exhibited a higher adiposity index, hyperleptinemia, reduced testosterone and estradiol testicular levels, and decreased testicular 17β-HSD enzyme . Morphometrical analyses indicated atrophy of Leydig cells in the O2 group. Myelin vesicles were observed in the mitochondrial matrix of Leydig cells in O3, O4, O5 and O6, and autophagosomes containing mitochondria were found in O5 and O6. In conclusion, HFD feeding, before or after sexual maturation, reduces the functional capacity of rat Leydig cells. Maternal obesity associated with HFD during pregnancy/lactation prejudices Leydig cell steroidogenesis and induces its atrophy in adulthood, even if it is replaced by a conventional diet at later stages of life. Regardless of the life period of exposure to HFD, deregulation of leptin is the main factor related to steroidogenic impairment of Leydig cells, and, in groups exposed for longer periods (O3, O4, O5 and O6), this is worsened by structural damage and mitochondrial degeneration of these cells.

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Section: Introductionmentioning

confidence: 57%

A high-fat diet fed during different periods of life impairs steroidogenesis of rat Leydig cells

Pinto-Fochi¹,

Pytlowanciv²,

Reame³

et al. 2016

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“…Aging can lead to a more disordered orientation of SMC in mice prostate (Bianchi-Frias et al, 2010), which may be associated with a decrease in androgen levels, as described after castration (Antonioli et al, 2004). If androgen levels from rats in adulthood (at least 19 weeks old) were compared to ours, a twofold decrease is noted (Pytlowanciv et al, 2016;Ribeiro et al, 2012a). This is of particular interest because MLT, despite the deregulation of sexual steroids by aging or diet, preserved SML and then prostate stroma.…”

Section: Discussionmentioning

confidence: 64%

“…In the present study, we evaluated the consequences for the prostate morphology and the antioxidant system of a long-term high-fat feeding (38 weeks) provided during aging to Wistar rats, which are a suitable preclinical model for investigations of prostatic aging-related disorders (Campolina-Silva et al, 2020). We observed that the high-fat diet raised estrogen serum levels, led to acinar atrophy, and in- The long-term high-fat diet caused several metabolic alterations already described for shorter periods of feeding (Nascimento et al, 2008;Pytlowanciv et al, 2016;Ribeiro et al, 2012a), as the increase of body weight gain, hyperglycemia, abdominal circumference, retroperitoneal fatness, and circulating estrogen levels. This indicated that our protocol led to obesity-like changes as expected, in addition to raising systemic oxidative stress.…”

Section: Discussionmentioning

confidence: 87%

“…The long‐term high‐fat diet caused several metabolic alterations already described for shorter periods of feeding (Nascimento et al, 2008; Pytlowanciv et al, 2016; Ribeiro et al, 2012a), as the increase of body weight gain, hyperglycemia, abdominal circumference, retroperitoneal fatness, and circulating estrogen levels. This indicated that our protocol led to obesity‐like changes as expected, in addition to raising systemic oxidative stress.…”

Section: Discussionmentioning

confidence: 92%

“…High‐fat diet and aging have been implicated in several deleterious effects in the prostate, including cancer, but the underlying mechanisms are not fully understood (Labbé et al, 2019; Pytlowanciv et al, 2016; Ribeiro et al, 2012a,b; Silva et al, 2015). In the present study, we evaluated the consequences for the prostate morphology and the antioxidant system of a long‐term high‐fat feeding (38 weeks) provided during aging to Wistar rats, which are a suitable preclinical model for investigations of prostatic aging‐related disorders (Campolina‐Silva et al, 2020).…”

Section: Discussionmentioning

confidence: 99%

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Melatonin ameliorates degenerative alterations caused by age in the rat prostate and mitigates high‐fat diet damages

Tamarindo

Gobbo

Taboga

et al. 2020

Cell Biology International

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Imbalance of sexual steroids milieu and oxidative stress are often observed during aging and correlated to prostate disorders. Likewise, high‐fat intake has been related to prostate damage and tumor development. Melatonin (MLT) is an antioxidant whose secretion decreases in elderly and is also suggested to protect the gland. This study evaluated the impact of a long‐term high‐fat diet during aging on prostate morphology and antioxidant system of rats and tested the effects of MLT supplementation under these conditions. Male rats were assigned into four groups: control, treated with MLT, high‐fat diet and high‐fat diet treated with MLT. The high‐fat diet was provided from the 24th week of age, MLT from the 48th (100 μg/kg/day) and rats were euthanized at the 62nd week. The high‐fat diet increased body weight, retroperitoneal fatness, glycaemia, and circulating estrogen levels. It aggravated the aging effects, leading to epithelial atrophy (∼32% reduction of epithelial height) and collagen fibers increase (83%). MLT alone did not alter biometric and physiological parameters, except for the prostate weight decrease, whereas it alleviated biometric as well as ameliorated acinar atrophy induced by high‐lipid intake. Systemic oxidative stress increased, and prostatic glutathione peroxidase activity decreased fivefold with the high‐fat diet despite the indole. Regardless of the diet, MLT triggered epithelial desquamation, reduced androgen receptor‐positive cells, increased smooth muscle layer thickness (12%), decreased at least 50% corpora amylacea formation, and stimulated prostatic gluthatione‐S‐transferase activity. In conclusion, MLT partially recovered prostate damage induced by aging and the long‐term high‐fat diet and ameliorated degenerative prostate alterations.

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Docosahexaenoic acid differentially modulates the cell cycle and metabolism- related genes in tumor and pre-malignant prostate cells

Tamarindo

Góes

2020

Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biolog

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Differential ontogenetic exposure to obesogenic environment induces hyperproliferative status and nuclear receptors imbalance in the rat prostate at adulthood

Abstract: OE leads to prostate hypertrophy regardless of the period of development and, except when restricted to gestation, leads to a hyperproliferative status which was correlated to downregulation of AR and LXRα and upregulation of ERα and PPARγ signaling.

Cited by 11 publications

References 95 publications

A high-fat diet fed during different periods of life impairs steroidogenesis of rat Leydig cells

A high-fat diet fed during different periods of life impairs steroidogenesis of rat Leydig cells

Melatonin ameliorates degenerative alterations caused by age in the rat prostate and mitigates high‐fat diet damages

Docosahexaenoic acid differentially modulates the cell cycle and metabolism- related genes in tumor and pre-malignant prostate cells

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