Nutrition affects Sertoli cell function but not Sertoli cell numbers in sexually mature male sheep

Guan, Yongjuan; Liang, Guanxiang; Hawken, Penny; Meachem, Sarah J; Malecki, Irek; Ham, Seungmin; Stewart, Tom; Guan, Le Luo; Martin, Graeme B.

doi:10.1071/rd14368

Cited by 18 publications

(23 citation statements)

References 57 publications

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“…Zonula occludens protein 1 (ZO1), also referred to as tight junction protein 1, is involved in blood-testis barrier function. Expression of ZO1 was found to be decreased in undernourished mature rams (Guan et al 2014(Guan et al , 2015. However, in contrast, in our calves, all of which were in positive energy balance, we did not observe an effect of either stage of maturity or plane of nutrition (within calves) on transcript abundance for ZO1.…”

Section: Figurecontrasting

confidence: 90%

Role of early life nutrition on the hypothalamic-pituitary-testicular axis of the bull

et al. 2018

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The objective of this study was to examine the effect of nutrition during the first 18 weeks of life on the physiological and transcriptional functionality of the hypothalamic (arcuate nucleus region), anterior pituitary and testes in Holstein–Friesian bull calves. Holstein–Friesian bull calves with a mean (±s.d.) age and bodyweight of 19 (±8.2) days and 47.5 (±5.3) kg, respectively, were assigned to either a HIGH (n = 10) or LOW (n = 10) plane of nutrition, to achieve an overall target growth rate of 1.2 or 0.5 kg/day, respectively. At 126 ± 1.1 days of age, all calves were euthanised. Animal performance (weekly) and systemic concentrations of metabolic (monthly) and reproductive hormones (fortnightly) were assessed. Testicular histology, targeted gene and protein expression of the arcuate nucleus region, anterior pituitary and testes were also assessed using qPCR and immunohistochemistry, respectively. The expression of candidate genes in testicular tissue from post pubertal 19-month-old Holstein–Friesian bulls (n = 10) was compared to that of the 18-week-old calves. Metabolite and metabolic hormone profiles generally reflected the improved metabolic status of the calves on the HIGH (P < 0.001). Calves offered a HIGH plane of nutrition were heavier at slaughter (P < 0.001), had larger testes (P < 0.001), larger seminiferous tubule diameter (P < 0.001), more mature spermatogenic cells (P < 0.001) and more Sertoli cells (P < 0.05) in accordance with both morphological and transcriptional data. Overall, testicular gene expression profiles suggested a more mature stage of development in HIGH compared with LOW and were more closely aligned to that of mature bulls. Ghrelin receptor was the only differentially expressed gene between LOW and HIGH calves in either the anterior pituitary (P < 0.05) or arcuate nucleus region of the hypothalamus (P < 0.10) and was upregulated in LOW for both tissues. This study indicates that an enhanced plane of nutrition during early calfhood favourably alters the biochemical regulation of the hypothalamus–anterior pituitary–testicular axis, advancing testicular development and hastening spermatogenesis.

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confidence: 90%

Role of early life nutrition on the hypothalamic-pituitary-testicular axis of the bull

et al. 2018

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“…In sexually mature sheep, we have shown that Sertoli cell function is clearly affected by nutritional treatment (Guan et al 2014a), as evidenced by changes in molecular regulators of critical processes that are specific to Sertoli cells. Underfeeding-induced testis regression was associated with: (a) disrupted distribution of the tight junction protein CLDN11, increased expression of CLDN11 and decreased expression of zonula occludens protein 1 (ZO1); (b) reduced expression of GATA1, a marker for mature Sertoli cells (Beau et al 2000), but an increase in the expression of AMH, a marker for immature Sertoli cells (Rey 1998), (Kliesch et al 1998, Steger et al 1999, Sharpe et al 2003; (c) reduced expression of three Sertoli cell-specific genes (KLM, SOX9, MSI1).…”

Section: The Effect Of Nutrition On Sertoli Cell Functionmentioning

confidence: 99%

“…These observations were extended in a subsequent study (Guan et al 2014a) that included the Johnsen Score, an indicator of spermatogenesis, again showing that spermatogenesis was impaired in underfed rams (testes regressing), but normal in both maintenance-fed (testes stable) and well-fed rams (testes growing). The number of Leydig cells per testis was not affected by diet, but the total volume of Leydig cells was, indicating changes in the volume of individual cells.…”

Section: The Effect Of Nutrition On Testis Morphologymentioning

confidence: 99%

“…We found that there was no effect of nutritional treatment on Sertoli cell numbers, so the earlier observations of Hötzel and coworkers (1998) can be attributed to histological artefact, perhaps caused by effects of nutrition on Sertoli cell functionality (see below) that affected the ease and accuracy with which their nuclei could be counted. Interestingly, about 1% of Sertoli cells in all animals appeared to retain their ability to proliferate (Guan et al 2014a). The possibility that Sertoli cells can proliferate after puberty suggests that, in future we might find ways to replenish damaged testes and restore germ cell production.…”

Section: R135mentioning

confidence: 99%

“…This finding might seem logical considering the differences in sperm production, but it contradicts the dogma that Sertoli cells stop proliferating at puberty, leaving the number fixed during adult life (Kluin et al 1984, Monet-Kuntz et al 1984, Hochereau-de Reviers et al 1987. We therefore decided to repeat the study by using modern techniques (Guan et al 2014a). We adopted GATA4 as a marker for Sertoli cells (Ketola et al 2000) and combined stereological cell counts with the assessment of Sertoli cell activity by analysis of immunoreactivity to proliferation cell ) per testis 120 ± 5 77 ± 6.7* These data have been selected from the full set presented by Hötzel et al (1998).…”

Section: The Effect Of Nutrition On Sertoli Cell Numbermentioning

confidence: 99%

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Cellular and molecular responses of adult testis to changes in nutrition: novel insights from the sheep model

Guan¹,

Martin²

2017

Reproduction

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This review explores the cellular and molecular mechanisms that regulate spermatogenesis in the post-pubertal testis that is regressing in response to mild undernutrition, using the sexually mature male sheep as a model. Testis regression leads to reductions in daily sperm production and in the quality of ejaculated spermatozoa (poorer movement, DNA damage). There is also a reduction in spermatogenic efficiency that appears to be caused, at least partially, by increases in germ cell apoptosis. Sertoli cell number does not change with testis regression, although about 1% of Sertoli cells do appear to retain proliferative ability after puberty. On the other hand, Sertoli cell function is disrupted during testis regression, as evidenced by a disorganization of tight junctions and indications that cell differentiation and maturation are reversed. Disrupted Sertoli cell function can explain, at least partially, the increase in germ cell apoptosis and any decrease in the rate of spermatogenesis, the two major contributors to spermatogenic efficiency. These outcomes seem to be mediated by changes in two RNA-based processes: (i) the expression of small non-coding RNAs that are involved in the regulation of Sertoli cell function, spermatogenesis and germ cell apoptosis and (ii) alternative pre-mRNA splicing that affects the regulation of spermatogenesis but does not appear to affect germ cell apoptosis, at least during testis progression induced by undernutrition in the male sheep. These research outcomes can be extended to other animal models and are relevant to issues in human male fertility.Reproduction (2017) 154 R133-R141

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Sertoli cell survival and barrier function are regulated by miR-181c/d-Pafah1b1 axis during mammalian spermatogenesis

Feng

Chen

Wang

et al. 2022

Cell. Mol. Life Sci.

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Sertoli cells contribute to the formation of the blood-testis barrier (BTB), which is necessary for normal spermatogenesis. Recently, microRNAs (miRNAs) have emerged as posttranscriptional regulatory elements in BTB function during spermatogenesis. Our previous study has shown that miR-181c or miR-181d (miR-181c/d) is highly expressed in testes from boars at 60 days old compared with at 180 days old. Herein, we found that overexpression of miR-181c/d via miR-181c/d mimics in murine Sertoli cells (SCs) or through injecting miR-181c/d-overexpressing lentivirus in murine testes perturbs BTB function by altering BTB-associated protein distribution at the Sertoli cell–cell interface and F-actin organization, but this in vivo perturbation disappears approximately 6 weeks after the final treatment. We also found that miR-181c/d represses Sertoli cell proliferation and promotes its apoptosis. Moreover, miR-181c/d regulates Sertoli cell survival and barrier function by targeting platelet-activating factor acetylhydrolase 1b regulatory subunit 1 (Pafah1b1) gene. Furthermore, miR-181c/d suppresses PAFAH1B1 expression, reduces the complex of PAFAH1B1 with IQ motif-containing GTPase activating protein 1, and inhibits CDC42/PAK1/LIMK1/Cofilin pathway which is required for F-actin stabilization. In total, our results reveal the regulatory axis of miR-181c/d-Pafah1b1 in cell survival and barrier function of Sertoli cells and provide additional insights into miRNA functions in mammalian spermatogenesis.

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Nutrition affects Sertoli cell function but not Sertoli cell numbers in sexually mature male sheep

Cited by 18 publications

References 57 publications

Role of early life nutrition on the hypothalamic-pituitary-testicular axis of the bull

Role of early life nutrition on the hypothalamic-pituitary-testicular axis of the bull

Cellular and molecular responses of adult testis to changes in nutrition: novel insights from the sheep model

Sertoli cell survival and barrier function are regulated by miR-181c/d-Pafah1b1 axis during mammalian spermatogenesis

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