A gestational high protein diet affects the abundance of muscle transcripts related to cell cycle regulation throughout development in porcine progeny

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Abstract

Background: In various animal models pregnancy diets have been shown to affect offspring phenotype. Indeed, the underlying programming of development is associated with modulations in birth weight, body composition, and continual diet-dependent modifications of offspring metabolism until adulthood, producing the hypothesis that the offspring's transcriptome is permanently altered depending on maternal diet. Methodology/Principal Findings: To assess alterations of the offspring's transcriptome due to gestational protein supply, German Landrace sows were fed isoenergetic diets containing protein levels of either 30% (high protein - HP) or 12% (adequate protein - AP) throughout their pregnancy. Offspring muscle tissue (M. longissimus dorsi) was collected at 94 days post conception (dpc), and 1, 28, and 188 days post natum (dpn) for use with Affymetrix GeneChip Porcine Genome Arrays and subsequent statistical and Ingenuity pathway analyses. Numerous transcripts were found to have altered abundance at 94 dpc and 1 dpn; at 28 dpn no transcripts were altered, and at 188 dpn only a few transcripts showed a different abundance between diet groups. However, when assessing transcriptional changes across developmental time points, marked differences were obvious among the dietary groups. Depending on the gestational dietary exposure, short- and long-term effects were observed for mRNA expression of genes related to cell cycle regulation, energy metabolism, growth factor signaling pathways, and nucleic acid metabolism. In particular, the abundance of transcripts related to cell cycle remained divergent among the groups during development. Conclusion: Expression analysis indicates that maternal protein supply induced programming of the offspring's genome; early postnatal compensation of the slight growth retardation obvious at birth in HP piglets resulted, as did a permanently different developmental alteration and responsiveness to the common environment of the transcriptome. The transcriptome modulations are interpreted as the molecular equivalent of developmental plasticity of the offspring that necessitates adaptation and maintenance of the organismal phenotype. © 2012 Oster et al.

Figures

  • Figure 1. Number of probe sets showing a significantly altered abundance in muscle tissue. The number of altered probe sets between adjacent developmental stages in AP or HP offspring are indicated at horizontal arrows; the number of commonly altered probe sets between stages in AP and HP offspring are indicated at intersections; the number of probe sets showing a different abundance between HP and AP offspring at the same developmental stage are indicated at vertical arrows; small arrows at the numbers indicate a higher or lower probe set abundance, respectively. doi:10.1371/journal.pone.0034519.g001
  • Figure 2. Affected pathways in muscle tissue between developmental stages and diets. Listed pathways between AP stages (white boxes) indicate shifts during development that are not found in HP offspring (black boxes) at the corresponding period. Pathways between HP stages indicate alterations that occur in HP offspring but not in AP offspring in the corresponding period. (Arrows between boxes show direction of comparison; small arrows indicate higher and lower transcript abundance, respectively. OXPHOS, oxidative phosphorylation; PLK, Polo-like kinase; mTOR, mammalian target of rapamycin; AMPK, AMP-activated protein kinase; IGF1, insulin-like growth factor 1; FA, Fatty acid; RAN, Ras-related nuclear protein). doi:10.1371/journal.pone.0034519.g002
  • Table 1. Functional annotation of muscle transcripts showing altered abundance depending on the dietary group (HP vs. AP) within different developmental stages (Ingenuity Pathway Analysis).
  • Table 2. Functional annotation of muscle transcripts showing altered abundance between two developmental stages within either dietary group HP or AP (Ingenuity Pathway Analysis).
  • Table 2. Cont.
  • Figure 3. Experimental design. Fetuses and offspring of divergently fed sows were collected at 4 developmental stages. Fetuses were derived from 3 sows per dietary group. Offspring were full sibs of six litters per dietary group collected at 3 consecutive postnatal stages; HP = high protein, CP = crude protein, AP = adequate protein. doi:10.1371/journal.pone.0034519.g003

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Oster, M., Murani, E., Metges, C. C., Ponsuksili, S., & Wimmers, K. (2012). A gestational high protein diet affects the abundance of muscle transcripts related to cell cycle regulation throughout development in porcine progeny. PLoS ONE, 7(4). https://doi.org/10.1371/journal.pone.0034519

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