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Characterization of porcine milk oligosaccharides over lactation between primiparous and multiparous female pigs.

ABSTRACT: Milk oligosaccharides (MOs) are complex carbohydrates with multifunctional health benefits for the neonate. Poor reproductive performance in primiparous gilts limits their productivity. Changes in the structure and abundance of porcine MO (PMOs) through lactation with parity remains unknown and may explain superior new-born growth in litters from multiparous sows relative to gilts. We report 55 PMOs structures, of which 25 are new (17 sialylated and 8 neutral). Their incidence in gilt and sow colostrum was almost identical (53 vs. 54), but not in transitional milk (48 vs. 53) nor mature milk (41 vs. 47). These PMOs including neutral-, sialyl- and fucosyl- MOs in colostrum were more abundant in the gilt than the sow, but always decreased during lactation. Structural diversity decreased, although fucosylated MO were conserved. In conclusion, high diversity and levels of MO in porcine milk is parity dependent. Given the similarity between porcine and human MO profiles, our findings may help define key roles for MOs as potential dietary additives to improve growth of neonates from first pregnancies in both human and sows.

SUBMITTER: Wei J

PROVIDER: S-EPMC5856818 | biostudies-literature | 2018 Mar

REPOSITORIES: biostudies-literature

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Characterization of porcine milk oligosaccharides over lactation between primiparous and multiparous female pigs.

Wei Jinhua J Wang Zhuo A ZA Wang Bing B Jahan Marefa M Wang Zhongfu Z Wynn Peter C PC Du Yuguang Y

Scientific reports 20180316 1

Milk oligosaccharides (MOs) are complex carbohydrates with multifunctional health benefits for the neonate. Poor reproductive performance in primiparous gilts limits their productivity. Changes in the structure and abundance of porcine MO (PMOs) through lactation with parity remains unknown and may explain superior new-born growth in litters from multiparous sows relative to gilts. We report 55 PMOs structures, of which 25 are new (17 sialylated and 8 neutral). Their incidence in gilt and sow co ...[more]

PMID: 29549280

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Project description:The composition of porcine milk oligosaccharides (PMO) was analyzed during early lactation and their relation to piglet gut microbiome was investigated. Pigs are considered ideal intestinal models to simulate humans because of the striking similarity in intestinal physiopathology to humans. The evolution of PMO was investigated in the milk from 3 healthy sows at prefarrowing, farrowing, and d 7 and 14 postpartum by Nano-LC Chip Quadrupole-Time-of-Flight mass spectrometer (Agilent Technologies, Santa Clara, CA). Previously sequenced metagenome libraries were reanalyzed to examine changes with specific gut bacterial populations. Over 30 oligosaccharides (OS) were identified in the milk, with 3'-sialyllactose, lacto-N-tetraose, α1-3,β1-4-d-galactotriose, 2'-fucosyllactose, and 6'-sialyllactose being the most abundant species (accounting for ~70% of the total OS). Porcine milk had lower OS diversity (number of unique structures) than human milk, and appeared closer to bovine and caprine milk. In agreement with previous studies, only 3 fucosylated OS were identified. Surprisingly, their contribution to total OS abundance was greater than in bovine milk (9 vs. 1%). Indeed, fucosylated PMO increased during lactation, mirroring a similar trend observed for neutral and type I OS content during early lactation. Taken together, these results suggest that, in terms of abundance, PMO are closer to human milk than other domestic species, such as bovine and caprine milks. Metagenomic sequencing revealed that fucose-consuming bacterial taxa in the gut microbiota of piglets were qualitatively but not quantitatively different between nursing and weaning stages, suggesting that both the composition and structure of dietary glycans may play a critical role in shaping the distal gut microbiome. The similarity of both intestinal physiopathology and milk OS composition in human and porcine species suggests similar effects on gastrointestinal development of early nutrition, reinforcing the use of the pig intestinal model to simulate human intestinal models in the clinical setting.

Project description:BackgroundPrevious studies have identified many immune pathways which are consistently altered in humans and model organisms as they age. Dairy cows are often culled at quite young ages due to an inability to cope adequately with metabolic and infectious diseases, resulting in reduced milk production and infertility. Improved longevity is therefore a desirable trait which would benefit both farmers and their cows. This study analysed the transcriptome derived from RNA-seq data of leukocytes obtained from Holstein cows in early lactation with respect to lactation number.ResultsSamples were divided into three lactation groups for analysis: i) primiparous (PP, n = 53), ii) multiparous in lactations 2-3 (MP 2-3, n = 121), and iii) MP in lactations 4-7 (MP > 3, n = 55). Leukocyte expression was compared between PP vs MP > 3 cows with MP 2-3 as background using DESeq2 followed by weighted gene co-expression network analysis (WGCNA). Seven modules were significantly correlated (r ≥ 0.25) to the trait lactation number. Genes from the modules which were more highly expressed in either the PP or MP > 3 cows were pooled, and the gene lists subjected to David functional annotation cluster analysis. The top three clusters from modules more highly expressed in the PP cows all involved regulation of gene transcription, particularly zinc fingers. Another cluster included genes encoding enzymes in the mitochondrial beta-oxidation pathway. Top clusters up-regulated in MP > 3 cows included the terms Glycolysis/Gluconeogenesis, C-type lectin, and Immunity. Differentially expressed candidate genes for ageing previously identified in the human blood transcriptome up-regulated in PP cows were mainly associated with T-cell function (CCR7, CD27, IL7R, CAMK4, CD28), mitochondrial ribosomal proteins (MRPS27, MRPS9, MRPS31), and DNA replication and repair (WRN). Those up-regulated in MP > 3 cows encoded immune defence proteins (LYZ, CTSZ, SREBF1, GRN, ANXA5, ADARB1).ConclusionsGenes and pathways associated with lactation number in cows were identified for the first time to date, and we found that many were comparable to those known to be associated with ageing in humans and model organisms. We also detected changes in energy utilization and immune responses in leukocytes from older cows.

Project description:The quantitation of human milk oligosaccharides (HMOs) is challenging because of the structural complexity and lack of standards.The objective of our study was to rapidly measure the absolute concentrations of HMOs in milk using LC-mass spectrometry (MS) and to determine the phenotypic secretor status of the mothers.This quantitative method for measuring HMO concentration was developed by using ultraperformance LC multiple reaction monitoring MS. It was validated and applied to milk samples from Malawi (88 individuals; 88 samples from postnatal month 6) and the United States (Davis, California; 45 individuals, mean age: 32 y; 103 samples collected on postnatal days 10, 26, 71, or 120, repeated measures included). The concentrations of ?(1,2)-fucosylated HMOs were used to determine the mothers' phenotypic secretor status with high sensitivity and specificity. We used Friedman's test and Wilcoxon's signed rank test to evaluate the change in HMO concentration during the course of lactation, and Student's t test was used to compare secretors and nonsecretors.A decrease (P < 0.05) in HMO concentration was observed during the course of lactation for the US mothers, corresponding to 19.3 ± 2.9 g/L for milk collected on postnatal day 10, decreasing to 8.53 ± 1.18 g/L on day 120 (repeated measures; n = 14). On postnatal day 180, the total concentration of HMOs in Malawi milk samples from secretors (6.46 ± 1.74 mg/mL) was higher (P < 0.05) than that in samples from nonsecretors (5.25 ± 2.55 mg/mL ). The same trend was observed for fucosylated species; the concentration was higher in Malawi milk samples from secretors (4.91 ± 1.22 mg/mL) than from nonsecretors (3.42 ± 2.27 mg/mL) (P < 0.05).HMOs significantly decrease during the course of lactation. Secretor milk contains higher concentrations of total and fucosylated HMOs than does nonsecretor milk. These HMO concentrations can be correlated to the health of breastfed infants in order to investigate the protective effects of milk components. The trials were registered at clinicaltrials.gov as NCT01817127 and NCT00524446.

Dataset Information

Characterization of porcine milk oligosaccharides over lactation between primiparous and multiparous female pigs.

Publications

Characterization of porcine milk oligosaccharides over lactation between primiparous and multiparous female pigs.

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