Enhanced early-life nutrition upregulates cholesterol biosynthetic gene expression and Sertoli cell maturation in testes of pre-pubertal Holstein bulls

Johnson, Chinju; Dance, Alysha; Kovalchuk, Igor; Kastelic, John P.; Thundathil, Jacob C.

doi:10.1038/s41598-019-42686-w

Cited by 13 publications

(8 citation statements)

References 45 publications

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“…There was a significant increase in cholesterol concentration in the early-weaned groups from day 70 to day 140 of this trial (p = 0.011), which reflected that the liver was unable to produce as much cholesterol in the young, early-weaned calves on account of later production when they were more mature. A higher energy supply enhanced cholesterol biosynthesis in 16-week-old bull calves [36], which is in line with our findings in late-weaned female calves that received more energy through MR and a higher concentrate feed intake (Figure 1). Moreover, the MR is a nutritional source for cholesterol, which is no longer available after weaning.…”

Section: Blood Metabolitessupporting

confidence: 91%

Weaning Holstein Calves at 17 Weeks of Age Enables Smooth Transition from Liquid to Solid Feed

Schwarzkopf

Kinoshita

Kluess

et al. 2019

Animals

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Simple Summary: Weaning calves from liquid to solid feed can be a stressful event in their life and can affect growth, development and welfare. It is commonly done at the age of 7 to 8 weeks on dairy farms, but weaning at a greater age could potentially reduce the associated stress. Therefore, it might improve growth rates and enable a smooth transition to an adult liver metabolism. To confirm this hypothesis this study evaluated the effect of two different weaning ages (7 vs. 17 weeks of age) on female Holstein calves. Furthermore, the effect of mothers' parity was analyzed (primiparous vs. multiparouos). Primiparous cows were often immature and still developing during their first pregnancy. This can lead to negative intrauterine conditions and result in long-term changes in the calf's metabolism. Late-weaned calves consumed high amounts of concentrate feed before weaning despite their high milk replacer intake, indicating the maturation of their rumen. In addition, they experienced a smooth transition to an adult liver metabolism as reflected by steady plasma glucose and cholesterol concentrations. Later weaning corrected the reduced growth of calves born to primiparous cows as well, indicating that those particularly benefitted from late weaning. All benefits were indicated by slower changes of blood metabolites and higher growth rates, which might lead to better health and productivity in their subsequent lifetime.Abstract: Development of calves depends on prenatal and postnatal conditions. Primiparous cows were still maturing during pregnancy, which can lead to negative intrauterine conditions and affect the calf's metabolism. It is hypothesized that weaning calves at higher maturity has positive effects due to reduced metabolic stress. We aimed to evaluate effects of mothers' parity and calves' weaning age on growth performance and blood metabolites. Fifty-nine female Holstein calves (38.8 ± 5.3 kg birth weight, about 8 days old) were used in a 2 × 2 factorial experiment with factors weaning age (7 vs. 17 weeks) and parity of mother (primiparous vs. multiparous cows). Calves were randomly assigned one of these four groups. Live weight, live weight gain and morphometry increased over time and were greater in calves weaned later. Metabolic indicators except total protein were interactively affected by time and weaning age. Leptin remained low in early-weaned calves born to primiparous cows, while it increased in the other groups. The results suggest that weaning more mature calves has a positive effect on body growth, and calves born to primiparous cows particularly benefit from this weaning regimen. It also enables a smooth transition from liquid to solid feed, which might reduce the associated stress of weaning.

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Section: Blood Metabolitessupporting

confidence: 91%

Weaning Holstein Calves at 17 Weeks of Age Enables Smooth Transition from Liquid to Solid Feed

Schwarzkopf

Kinoshita

Kluess

et al. 2019

Animals

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“…Thus, the effect of enhanced metabolic status on steroid and fatty acid synthesis and testicular development may be mediated through CDH13 expression. Proteins related to fatty acid synthesis and cholesterol biosynthesis that CDH13 was interacting with were also previously identified as differentially expressed at the transcript level in the testes data of English et al 7 ( AACS, ACLY, ACSS2 ) and Johnson et al 9 ( TM7SF2 ). Moreover, in our earlier evaluation of the metabolic control of enhanced early life nutrition, we observed a tendency for greater systemic concentrations of cholesterol in HI compared with MOD calves, consistent with the higher concentrations of testosterone in the same calves used for the current study 10 .…”

Section: Discussionmentioning

confidence: 80%

“…2 ) derived through IPA and depicted genes involved in cellular movement, lipid metabolism and small molecular biochemistry. Furthermore, other differentially expressed genes within this network were previously implicated in testicular development following enhanced early life plane of nutrition up to 18 weeks of age ( TF, NTRK1, SEMA5B ) 7 as well as both 16 and 24 weeks of age ( TF, MCF2 , PLEKHD1 ) 9 . The genes listed above ( TF, NTRK1, SEMA5B, MCF2 and PLEKHD1 ) that were also differentially expressed in similar studies play important roles in testicular, spermatogenic and overall sexual development.…”

Section: Discussionmentioning

confidence: 97%

“…While we 7 and others 9 have investigated aspects of the impact of early life nutrition on global mRNA transcriptomic profiles of testicular tissue, an evaluation of both miRNA transcriptomic and global proteomics in relation to this phenotype is lacking. Therefore, the objective of this study was to examine the effect of enhanced nutritional status during early calfhood on (i) the global testicular transcriptome (miRNA and mRNA) and (ii) the testicular proteome in bull calves coincident with the early transient gonadotrophin rise (12 weeks).…”

Section: Introductionmentioning

confidence: 99%

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Early life nutrition affects the molecular ontogeny of testicular development in the young bull calf

Coen

Keogh

Lonergan

et al. 2023

Sci Rep

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Enhanced early life nutrition accelerates sexual development in the bull calf through neuroendocrine-signalling mediated via the hypothalamic–pituitary–testicular axis. Our aim was to assess the impact of contrasting feeding regimes in bull calves during the first 12 weeks of life on the testes transcriptome and proteome. Holstein–Friesian bull calves were offered either a high (HI) or moderate (MOD) plane of nutrition, designed to support target growth rates of 1.0 and 0.5 kg/day, respectively. At 12 weeks of age all calves were euthanized, testicular parenchyma sampled, and global transcriptome (miRNAseq and mRNAseq) and proteome analyses undertaken. Bioinformatic analyses revealed 7 differentially expressed (DE) miRNA and 20 DE mRNA. There were no differentially abundant proteins between the two dietary groups. Integration of omics results highlighted a potential role for the cadherin gene, CDH13, in earlier reproductive development. Furthermore, co-regulatory network analysis of the proteomic data revealed CDH13 as a hub protein within a network enriched for processes related to insulin, IGF-1, androgen and Sertoli cell junction signalling pathways as well as cholesterol biosynthesis. Overall, results highlight a potential role for CDH13 in mediating earlier reproductive development as a consequence of enhanced early life nutrition in the bull calf.

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“…Quantitative real-time polymerase chase reaction (RT-PCR). RT-PCR was performed as described previously 7 . In brief, reverse transcription and subsequently PCR with SYBR Green (Fast SYBR ® Green Master Mix; Applied Biosystems, Foster City, CA, USA) was done to validate mRNA expression of five differentially expressed genes: TJP2, COX5B, ATP5J, ATP5G1 and CRHR1.…”

Section: Discussionmentioning

confidence: 99%

Enhanced pre-pubertal nutrition upregulates mitochondrial function in testes and sperm of post-pubertal Holstein bulls

Johnson

Dance

Kovalchuk

et al. 2020

Sci Rep

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Supplemental energy and protein during calf-hood (2-30 wk) in dairy bulls hastened puberty (~1 mo), upregulated steroid biosynthesis, concentrations of reproductive hormones and Sertoli cell maturation, with larger testes and greater sperm production (~25%) in mature bulls. The objective was to evaluate effects of feeding high (20.0% crude protein [CP], 67.9% total digestible nutrients [TDN]), control/ medium (17.0% CP, 66.0% TDN) and low (12.2% CP, 62.9% TDN) diets from 2 to 30 wk on post-pubertal testes of Holstein bulls. Based on RNA sequencing, 497 and 2961 genes were differentially expressed (p < 0.1) in high-vs low-and high-vs medium-diet groups, respectively. According to KEGG analysis, oxidative phosphorylation and ribosome pathways were upregulated in high-vs medium-and low-diet groups, with majority of upregulated genes encoding for essential subunits of complex I, III, IV and V of OXYPHOS pathway. In addition, mitochondrial translation, mitotic nuclear division and cell division were enriched in high-vs medium-diet groups. Consistent with these results, a greater percentage of sperm from high-diet bulls were progressively motile and had normal mitochondrial function compared to medium-diet sperm (p < 0.1). Thus, enhanced early life nutrition upregulated mitochondrial function in testes and sperm of post-pubertal Holstein bulls.Enhanced early-life nutrition hastens puberty, with ~25% increases in testis size and sperm production in dairy and beef bulls 1,2 . The underlying endocrine basis is profound increases in luteinizing hormone (LH) pulse frequency and insulin like growth factor (IGF-I) concentrations in blood 3,4 . In a cohort-based study in Sweden, low nutrition during the pre-pubertal period in men reduced susceptibility to heart disease in their offspring 5 , consistent with developmental programming in male germ cells that extends well into early post-natal life 6 . Therefore, nutritional modulation during early life affects testicular development, with apparent epigenetic effects on post-pubertal sperm function.We reported increased cholesterol/steroid biosynthesis and Sertoli cell maturation in testicular tissues of high-diet bulls at 16 and 24 wk, respectively 7 . Although a wide range in pre-pubertal diets had no significant effects on routine analyses of sperm morphology and function 8 , molecular-level analyses should be done, to ensure no deleterious effects are transmitted to the next generation. Our objective was to determine effects of pre-pubertal dietary modulations on post-pubertal testes of Holstein bulls. ResultsmRNA profile of testes. Approximately 340 × 10 6 reads were obtained from the 24 libraries sequenced. On average, 14,357,890 (SD = 2,267,076) reads were obtained per library and 13,565,597 (SD = 2,148,261) mapped to the Ensemble gene annotation database. On average 13,710,936 (SD = 3,098,630), 13,120,341 (SD = 1,219,498) and 13,865,513 (SD = 1,929,109) reads were mapped from HD, MD and LD groups respectively. A total of 18,288 genes were detected in testicular tissue and...

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Enhanced early-life nutrition upregulates cholesterol biosynthetic gene expression and Sertoli cell maturation in testes of pre-pubertal Holstein bulls

Cited by 13 publications

References 45 publications

Weaning Holstein Calves at 17 Weeks of Age Enables Smooth Transition from Liquid to Solid Feed

Weaning Holstein Calves at 17 Weeks of Age Enables Smooth Transition from Liquid to Solid Feed

Early life nutrition affects the molecular ontogeny of testicular development in the young bull calf

Enhanced pre-pubertal nutrition upregulates mitochondrial function in testes and sperm of post-pubertal Holstein bulls

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