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      Lowered dietary phosphorus affects intestinal and renal gene expression to maintain mineral homeostasis with immunomodulatory implications in weaned piglets

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          Abstract

          Background

          In monogastric animals, phosphorus (P) homeostasis is maintained by regulating intestinal absorption, bone mobilization, and renal excretion. Since P is a non-renewable resource, a shortage is imminent due to widespread over-usage in the farming and animal husbandry industries. As a consequence, P efficiency should be improved in pig production. We sought to characterize the transcriptional response in re−/absorbing and excreting tissues in pigs to diets varying in calcium: phosphorus ratios. Weaned piglets were assigned to one of three groups fed diets varying in digestible P content for a period of five weeks. Gene expression profiles were analyzed in jejunum, colon, and kidney.

          Results

          Transcriptome analysis revealed that reduced dietary P intake affects gene expression in jejunum and kidney, but not in colon. The regulation of mineral homeostasis was reflected via altered mRNA abundances of CYP24A1, CYP27A1, TRPM6, SPP1, and VDR in jejunum and kidney. Moreover, lowered abundances of transcripts associated with the classical complement system pathway were observed in the jejunum. In kidney, shifted transcripts were involved in phospholipase C, calcium signaling, and NFAT signaling, which may have immunomodulatory implications.

          Conclusions

          Our results revealed local transcriptional consequences of variable P intake in intestinal and renal tissues. The adaptive responses are the result of organismal efforts to maintain systemic mineral homeostasis while modulating immune features at local tissue sites. Therefore, the deviation from the currently recommended dietary P supply must be carefully considered, as the endogenous mechanisms that respond to low P diets may impact important adaptive immune responses.

          Electronic supplementary material

          The online version of this article (10.1186/s12864-018-4584-2) contains supplementary material, which is available to authorized users.

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          Most cited references51

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          The immune system and kidney disease: basic concepts and clinical implications.

          Christian Kurts, Ulf Panzer, Hans-Joachim Anders … (2013)
          The kidneys are frequently targeted by pathogenic immune responses against renal autoantigens or by local manifestations of systemic autoimmunity. Recent studies in rodent models and humans have uncovered several underlying mechanisms that can be used to explain the previously enigmatic immunopathology of many kidney diseases. These mechanisms include kidney-specific damage-associated molecular patterns that cause sterile inflammation, the crosstalk between renal dendritic cells and T cells, the development of kidney-targeting autoantibodies and molecular mimicry with microbial pathogens. Conversely, kidney failure affects general immunity, causing intestinal barrier dysfunction, systemic inflammation and immunodeficiency that contribute to the morbidity and mortality of patients with kidney disease. In this Review, we summarize the recent findings regarding the interactions between the kidneys and the immune system.
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            Vitamin D controls T cell antigen receptor signaling and activation of human T cells.

            Niels Ødum, Peter Schjerling, Marina Rode von Essen … (2010)
            Phospholipase C (PLC) isozymes are key signaling proteins downstream of many extracellular stimuli. Here we show that naive human T cells had very low expression of PLC-gamma1 and that this correlated with low T cell antigen receptor (TCR) responsiveness in naive T cells. However, TCR triggering led to an upregulation of approximately 75-fold in PLC-gamma1 expression, which correlated with greater TCR responsiveness. Induction of PLC-gamma1 was dependent on vitamin D and expression of the vitamin D receptor (VDR). Naive T cells did not express VDR, but VDR expression was induced by TCR signaling via the alternative mitogen-activated protein kinase p38 pathway. Thus, initial TCR signaling via p38 leads to successive induction of VDR and PLC-gamma1, which are required for subsequent classical TCR signaling and T cell activation.
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              Mammalian phospholipase C.

              Ganesh Kadamur, Kirstin E. Ross (2012)
              Phospholipase C (PLC) converts phosphatidylinositol 4,5-bisphosphate (PIP(2)) to inositol 1,4,5-trisphosphate (IP(3)) and diacylglycerol (DAG). DAG and IP(3) each control diverse cellular processes and are also substrates for synthesis of other important signaling molecules. PLC is thus central to many important interlocking regulatory networks. Mammals express six families of PLCs, each with both unique and overlapping controls over expression and subcellular distribution. Each PLC also responds acutely to its own spectrum of activators that includes heterotrimeric G protein subunits, protein tyrosine kinases, small G proteins, Ca(2+), and phospholipids. Mammalian PLCs are autoinhibited by a region in the catalytic TIM barrel domain that is the target of much of their acute regulation. In combination, the PLCs act as a signaling nexus that integrates numerous signaling inputs, critically governs PIP(2) levels, and regulates production of important second messengers to determine cell behavior over the millisecond to hour timescale.
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                Author and article information

                Contributors
                Franziska Just: just@fbn-dummerstorf.de
                Michael Oster: oster@fbn-dummerstorf.de
                Kirsten Büsing: kirsten.buesing@uni-rostock.de
                Luisa Borgelt: luisa.borgelt@uni-rostock.de
                Eduard Murani: murani@fbn-dummerstorf.de
                Siriluck Ponsuksili: ponsuksili@fbn-dummerstorf.de
                Petra Wolf: petra.wolf@uni-rostock.de
                Klaus Wimmers:
                ORCID: http://orcid.org/0000-0002-9523-6790
                wimmers@fbn-dummerstorf.de
                Journal
                Journal ID (nlm-ta): BMC Genomics
                Journal ID (iso-abbrev): BMC Genomics
                Title: BMC Genomics
                Publisher: BioMed Central (London )
                ISSN (Electronic): 1471-2164
                Publication date (Electronic): 20 March 2018
                Publication date PMC-release: 20 March 2018
                Publication date Collection: 2018
                Volume: 19
                Electronic Location Identifier: 207
                Affiliations
                [1 ]Leibniz Institute for Farm Animal Biology (FBN), Institute for Genome Biology, Wilhelm-Stahl-Allee 2, 18196 Dummerstorf, Germany
                [2 ]ISNI 0000000121858338, GRID grid.10493.3f, Faculty of Agricultural and Environmental Sciences, , University Rostock, ; 18059 Rostock, Germany
                Author information
                http://orcid.org/0000-0002-9523-6790
                Article
                Publisher ID: 4584
                DOI: 10.1186/s12864-018-4584-2
                PMC ID: 5859397
                SO-VID: ea6abd8e-8800-4c04-a62f-1fa75e247ac9
                Copyright © © The Author(s). 2018
                License:

                Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

                History
                Date received : 2 May 2017
                Date accepted : 7 March 2018
                Funding
                Funded by: LeibnizScienceCampus Phosphorus Research Rostock
                Award ID: n.a.
                Award ID: n.a.
                Award Recipient :
                Funded by: FP7 EU-project ECO-FCE
                Award ID: 311794
                Award Recipient :
                Categories
                Subject: Research Article
                Custom metadata
                issue-copyright-statement © The Author(s) 2018

                ScienceOpen disciplines: Genetics
                Keywords: calcium: phosphorus ratio,pig,gene expression,immune response,diet
                Data availability:
                ScienceOpen disciplines: Genetics
                Keywords: calcium: phosphorus ratio, pig, gene expression, immune response, diet

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