Microbial community shifts elicit inflammation in the caecal mucosa via the GPR41/43 signalling pathway during subacute ruminal acidosis

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Abstract

Background

Dietary structure in ruminants is closely connected with the composition of gastrointestinal microbiota. Merging study has shown that dietary induced SARA causes the alteration of microbial community in the cecum leading to the local inflammation. However, the mechanisms of cecum inflammation elicited by the shift of microbial flora in ruminants are largely unknown, and whether the development of this inflammation is modified by epigenetic modifications.

Results

Ten multiparous lactating goats were randomly seperated into two groups and received either a low concentrate diet (LC, 40% concentrate, n = 5) or a high concentrate diet (HC, 60% concentrate) to induce subacute ruminal acidosis (SARA). Compared with LC, HC-induced SARA altered the predominant phyla and genera, thereby increasing the concentration of lipopolysaccharide (LPS) and short chain fatty acids (SCFAs). Meanwhile, HC-induced SARA enhanced the mRNA expression of cytokines and chemokines and the expression of mRNA and protein of GPR41, GPR43, p38 and ERK1/2, while HC-induced SARA had no effect on TLR4 and p65. Furthermore, HC-induced SARA decreased the percentage of chromatin compaction and DNA methylation at the area of the promoters of GPR41 and GPR43.

Conclusion

This study indicated that HC diet induced SARA resulted in the alteration in the composition of cecal microbiota. This alteration increased the concentration of LPS, but failing to activate TLR4 signaling pathway due to the tolerance effect of intestinal epithelial cell to certain level of LPS, as well as elevated the concentration of SCFAs, thereby activating GPR41 and GPR43 signaling pathway to produce cytokines and chemokins and cause the cecal inflammation. And epigenetic mechanisms contributed to the development of this inflammation in the lactating goats suffering from SARA.

Electronic supplementary material

The online version of this article (10.1186/s12917-019-2031-5) contains supplementary material, which is available to authorized users.

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Most cited references 26

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Toll-like receptors: critical proteins linking innate and acquired immunity.

S Akira, K Takeda, T Kaisho (2001)

Recognition of pathogens is mediated by a set of germline-encoded receptors that are referred to as pattern-recognition receptors (PRRs). These receptors recognize conserved molecular patterns (pathogen-associated molecular patterns), which are shared by large groups of microorganisms. Toll-like receptors (TLRs) function as the PRRs in mammals and play an essential role in the recognition of microbial components. The TLRs may also recognize endogenous ligands induced during the inflammatory response. Similar cytoplasmic domains allow TLRs to use the same signaling molecules used by the interleukin 1 receptors (IL-1Rs): these include MyD88, IL-1R--associated protein kinase and tumor necrosis factor receptor--activated factor 6. However, evidence is accumulating that the signaling pathways associated with each TLR are not identical and may, therefore, result in different biological responses.

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Functional characterization of human receptors for short chain fatty acids and their role in polymorphonuclear cell activation.

Emmanuel Le Poul, Cécile Loison, Sofie Struyf … (2003)

Short chain fatty acids (SCFAs), including acetate, propionate, and butyrate, are produced at high concentration by bacteria in the gut and subsequently released in the bloodstream. Basal acetate concentrations in the blood (about 100 microm) can further increase to millimolar concentrations following alcohol intake. It was known previously that SCFAs can activate leukocytes, particularly neutrophils. In the present work, we have identified two previously orphan G protein-coupled receptors, GPR41 and GPR43, as receptors for SCFAs. Propionate was the most potent agonist for both GPR41 and GPR43. Acetate was more selective for GPR43, whereas butyrate and isobutyrate were more active on GPR41. The two receptors were coupled to inositol 1,4,5-trisphosphate formation, intracellular Ca2+ release, ERK1/2 activation, and inhibition of cAMP accumulation. They exhibited, however, a differential coupling to G proteins; GPR41 coupled exclusively though the Pertussis toxin-sensitive Gi/o family, whereas GPR43 displayed a dual coupling through Gi/o and Pertussis toxin-insensitive Gq protein families. The broad expression profile of GPR41 in a number of tissues does not allow us to infer clear hypotheses regarding its biological functions. In contrast, the highly selective expression of GPR43 in leukocytes, particularly polymorphonuclear cells, suggests a role in the recruitment of these cell populations toward sites of bacterial infection. The pharmacology of GPR43 matches indeed the effects of SCFAs on neutrophils, in terms of intracellular Ca2+ release and chemotaxis. Such a neutrophil-specific SCFA receptor is potentially involved in the development of a variety of diseases characterized by either excessive or inefficient neutrophil recruitment and activation, such as inflammatory bowel diseases or alcoholism-associated immune depression. GPR43 might therefore constitute a target allowing us to modulate immune responses in these pathological situations.

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Subacute ruminal acidosis in dairy cows: the physiological causes, incidence and consequences.

J. C. Plaizier, D Krause, G N Gozho … (2008)

During subacute ruminal acidosis (SARA) rumen pH is depressed for several hours per day due to accumulation of volatile fatty acids and insufficient rumen buffering. Surveys suggested an incidence of SARA of between 19% and 26% in early and mid-lactation dairy cows. Causes of SARA include feeding excessive amounts of non-structural carbohydrates and highly fermentable forages, and insufficient dietary coarse fiber. Consequences of SARA include feed intake depression, reduced fiber digestion, milk fat depression, diarrhea, laminitis, liver abscesses, increased production of bacterial endotoxin and inflammation characterized by increases in acute phase proteins. The increase in endotoxin is similar among methods for SARA induction, but depends on the diet fed before induction. Increases in acute phase proteins vary among methods of SARA induction, even when the methods result in similar rumen pH depressions. This suggests that the inflammatory response might not be solely due to bacterial endotoxin in the rumen.

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Author and article information

Contributors

Guangjun Chang: changguangjun@njau.edu.cn

Huanmin Zhang: 2015107105@njau.edu.cn

Yan Wang: 2015107104@njau.edu.cn

Nana Ma: 2017207035@njau.edu.cn

Roy Animesh Chandra: royanimeshvet98@yahoo.com

Gengping Ye: ygphappy@163.com

Su Zhuang: zhuangsu@njau.edu.cn

Weiyun Zhu: zhuweiyun@njau.edu.cn

Xiangzhen Shen:

ORCID: http://orcid.org/0000-0002-3020-5010

xzshen@njau.edu.cn

Journal

Journal ID (nlm-ta): BMC Vet Res

Journal ID (iso-abbrev): BMC Vet. Res

Title: BMC Veterinary Research

Publisher: BioMed Central (London )

ISSN (Electronic): 1746-6148

Publication date (Electronic): 19 August 2019

Publication date PMC-release: 19 August 2019

Publication date Collection: 2019

Volume: 15

Electronic Location Identifier: 298

Affiliations

[1 ]ISNI 0000 0000 9750 7019, GRID grid.27871.3b, College of Veterinary Medicine, , Nanjing Agricultural University, ; Nanjing, Jiangsu China

[2 ]Ranch Management Department, Bright Farming Co.,Ltd, Shanghai, China

[3 ]ISNI 0000 0000 9750 7019, GRID grid.27871.3b, College of Animal Science and Technology, , Nanjing Agricultural University, ; Nanjing, Jiangsu China

Author information

Xiangzhen Shen http://orcid.org/0000-0002-3020-5010

Article

Publisher ID: 2031

DOI: 10.1186/s12917-019-2031-5

PMC ID: 6700796

PubMed ID: 31426783

SO-VID: 94b1e17d-ebe2-4715-8006-2b6d5d536222

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 : 3 October 2018

Date accepted : 30 July 2019

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;

Award ID: 31702301 and 31672618

Award Recipient : Guangjun Chang

Funded by: FundRef http://dx.doi.org/10.13039/501100010031, Postdoctoral Research Foundation of China;

Award ID: 2016M590471

Award Recipient : Guangjun Chang

Funded by: Fundamental Research Funds for the Central Universities

Award ID: KJQN201828

Award Recipient : Guangjun Chang

Funded by: the Priority Academic Program Development of Jiangsu Higher Education Institutions

Award ID: PAPD

Award Recipient : Guangjun Chang

Custom metadata

ScienceOpen disciplines: Veterinary medicine

Keywords: caecal microbiota,scfas,lps,gpr41/gpr43,signalling pathway,tlr4

Data availability:

ScienceOpen disciplines: Veterinary medicine

Keywords: caecal microbiota, scfas, lps, gpr41/gpr43, signalling pathway, tlr4

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Microbial community shifts elicit inflammation in the caecal mucosa via the GPR41/43 signalling pathway during subacute ruminal acidosis

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Abstract

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Microbial Genomics

Most cited references 26

Toll-like receptors: critical proteins linking innate and acquired immunity.

Functional characterization of human receptors for short chain fatty acids and their role in polymorphonuclear cell activation.

Subacute ruminal acidosis in dairy cows: the physiological causes, incidence and consequences.

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Cited by 5

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