Salt-Sensitive Ileal Microbiota Plays a Role in Atrial Natriuretic Peptide Deficiency-Induced Cardiac Injury

Atrial natriuretic peptide (ANP) activity deficiency contributes to salt-sensitive hypertension in humans and mice. However, the role of ileal microbiota in salt sensitivity in ANP deficiency-related cardiac injury has not been investigated yet. This study used ANP−/− mice to analyze the role of the...

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Veröffentlicht in:Nutrients 2022-07, Vol.14 (15), p.3129
Hauptverfasser: Li, Siqi, Chen, Sishuo, Nie, Min, Wen, Lijing, Zou, Bin, Zhang, Lingyu, Xie, Jingzhou, Ser, Hooi-Leng, Lee, Learn-Han, Wang, Shunyi, Lin, Caixia, Pathak, Janak L., Zhou, Weijie, Miao, Ji, Wang, Lijing, Zheng, Lingyun
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container_issue 15
container_start_page 3129
container_title Nutrients
container_volume 14
creator Li, Siqi
Chen, Sishuo
Nie, Min
Wen, Lijing
Zou, Bin
Zhang, Lingyu
Xie, Jingzhou
Ser, Hooi-Leng
Lee, Learn-Han
Wang, Shunyi
Lin, Caixia
Pathak, Janak L.
Zhou, Weijie
Miao, Ji
Wang, Lijing
Zheng, Lingyun
description Atrial natriuretic peptide (ANP) activity deficiency contributes to salt-sensitive hypertension in humans and mice. However, the role of ileal microbiota in salt sensitivity in ANP deficiency-related cardiac injury has not been investigated yet. This study used ANP−/− mice to analyze the role of the salt-sensitive ileal microbiome on cardiac injury. ANP−/− mice showed an increase in blood pressure (BP), the heart weight/body weight (HW/BW) ratio, and cardiac hypertrophy compared with wild-type (WT) mice. ANP deficiency did not impact the histological structure but reduced occludin expression in the ileum. Antibiotics significantly relieved BP and cardiac hypertrophy in ANP−/− mice. A high-salt diet (HSD) increased BP, the HW/BW ratio, and cardiac hypertrophy/fibrosis in WT and ANP−/− mice, and an HSD treatment in ANP−/− mice exacerbated these cardiac parameters. The HSD markedly decreased muscularis layer thickening, villus length, and numbers of Paneth and goblet cells in the ileum of WT and ANP−/− mice. Furthermore, the HSD increased the level of TLR4 and IL-1β in ANP−/− mice ileum compared with WT mice. Antibiotics reduced the HW/BW ratio, cardiac hypertrophy/fibrosis, and the level of TLR4 and IL-1β in the ileum, and rescued the muscularis layer thickening, villus length, and numbers of Paneth and goblet cells in the ileum of HSD-ANP−/− mice. Importantly, ANP deficiency induced the colonization of Burkholderiales bacterium YL45, Lactobacillus johnsonii, and Lactobacillus reuteri in the ileum on the NSD diet, which was only observed in HSD-induced WT mice but not in WT mice on the NSD. Besides, the HSD significantly enhanced the sum of the percentage of the colonization of Burkholderiales bacterium YL45, Lactobacillus johnsonii, and Lactobacillus reuteri in the ileum of ANP−/− mice. Ileal microbiota transfer (IMT) from ANP−/− mice to healthy C57BL/6J mice drove Lactobacillus johnsonii and Lactobacillus reuteri colonization in the ileum, which manifested an increase in BP, the HW/BW ratio, cardiac hypertrophy, and ileal pathology compared with IMT from WT mice. The HSD in C57BL/6J mice with IMT from ANP−/− mice drove the colonization of Burkholderiales bacterium YL45, Lactobacillus johnsonii, and Lactobacillus reuteri in the ileum and further exacerbated the cardiac and ileal pathology. Our results suggest that salt-sensitive ileal microbiota is probably related to ANP deficiency-induced cardiac injury.
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However, the role of ileal microbiota in salt sensitivity in ANP deficiency-related cardiac injury has not been investigated yet. This study used ANP−/− mice to analyze the role of the salt-sensitive ileal microbiome on cardiac injury. ANP−/− mice showed an increase in blood pressure (BP), the heart weight/body weight (HW/BW) ratio, and cardiac hypertrophy compared with wild-type (WT) mice. ANP deficiency did not impact the histological structure but reduced occludin expression in the ileum. Antibiotics significantly relieved BP and cardiac hypertrophy in ANP−/− mice. A high-salt diet (HSD) increased BP, the HW/BW ratio, and cardiac hypertrophy/fibrosis in WT and ANP−/− mice, and an HSD treatment in ANP−/− mice exacerbated these cardiac parameters. The HSD markedly decreased muscularis layer thickening, villus length, and numbers of Paneth and goblet cells in the ileum of WT and ANP−/− mice. Furthermore, the HSD increased the level of TLR4 and IL-1β in ANP−/− mice ileum compared with WT mice. Antibiotics reduced the HW/BW ratio, cardiac hypertrophy/fibrosis, and the level of TLR4 and IL-1β in the ileum, and rescued the muscularis layer thickening, villus length, and numbers of Paneth and goblet cells in the ileum of HSD-ANP−/− mice. Importantly, ANP deficiency induced the colonization of Burkholderiales bacterium YL45, Lactobacillus johnsonii, and Lactobacillus reuteri in the ileum on the NSD diet, which was only observed in HSD-induced WT mice but not in WT mice on the NSD. Besides, the HSD significantly enhanced the sum of the percentage of the colonization of Burkholderiales bacterium YL45, Lactobacillus johnsonii, and Lactobacillus reuteri in the ileum of ANP−/− mice. Ileal microbiota transfer (IMT) from ANP−/− mice to healthy C57BL/6J mice drove Lactobacillus johnsonii and Lactobacillus reuteri colonization in the ileum, which manifested an increase in BP, the HW/BW ratio, cardiac hypertrophy, and ileal pathology compared with IMT from WT mice. The HSD in C57BL/6J mice with IMT from ANP−/− mice drove the colonization of Burkholderiales bacterium YL45, Lactobacillus johnsonii, and Lactobacillus reuteri in the ileum and further exacerbated the cardiac and ileal pathology. Our results suggest that salt-sensitive ileal microbiota is probably related to ANP deficiency-induced cardiac injury.</description><identifier>ISSN: 2072-6643</identifier><identifier>EISSN: 2072-6643</identifier><identifier>DOI: 10.3390/nu14153129</identifier><identifier>PMID: 35956306</identifier><language>eng</language><publisher>Basel: MDPI AG</publisher><subject>Antibiotics ; Atrial natriuretic peptide ; Bacteria ; Blood pressure ; Body weight ; Burkholderiales ; Colon ; Colonization ; Diet ; Drinking water ; Experiments ; Feces ; Fibrosis ; Goblet cells ; Heart ; histology ; Homeostasis ; Hypertension ; Hypertrophy ; IL-1β ; Ileum ; Injury analysis ; Laboratory animals ; Lactobacillus johnsonii ; Lactobacillus reuteri ; microbiome ; Microbiomes ; Microbiota ; occludins ; Pathology ; Peptides ; Rodents ; Salt ; Salts ; Small intestine ; Thickening ; TLR4 protein ; Toll-like receptors ; villi ; Villus</subject><ispartof>Nutrients, 2022-07, Vol.14 (15), p.3129</ispartof><rights>2022 by the authors. 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However, the role of ileal microbiota in salt sensitivity in ANP deficiency-related cardiac injury has not been investigated yet. This study used ANP−/− mice to analyze the role of the salt-sensitive ileal microbiome on cardiac injury. ANP−/− mice showed an increase in blood pressure (BP), the heart weight/body weight (HW/BW) ratio, and cardiac hypertrophy compared with wild-type (WT) mice. ANP deficiency did not impact the histological structure but reduced occludin expression in the ileum. Antibiotics significantly relieved BP and cardiac hypertrophy in ANP−/− mice. A high-salt diet (HSD) increased BP, the HW/BW ratio, and cardiac hypertrophy/fibrosis in WT and ANP−/− mice, and an HSD treatment in ANP−/− mice exacerbated these cardiac parameters. The HSD markedly decreased muscularis layer thickening, villus length, and numbers of Paneth and goblet cells in the ileum of WT and ANP−/− mice. Furthermore, the HSD increased the level of TLR4 and IL-1β in ANP−/− mice ileum compared with WT mice. Antibiotics reduced the HW/BW ratio, cardiac hypertrophy/fibrosis, and the level of TLR4 and IL-1β in the ileum, and rescued the muscularis layer thickening, villus length, and numbers of Paneth and goblet cells in the ileum of HSD-ANP−/− mice. Importantly, ANP deficiency induced the colonization of Burkholderiales bacterium YL45, Lactobacillus johnsonii, and Lactobacillus reuteri in the ileum on the NSD diet, which was only observed in HSD-induced WT mice but not in WT mice on the NSD. Besides, the HSD significantly enhanced the sum of the percentage of the colonization of Burkholderiales bacterium YL45, Lactobacillus johnsonii, and Lactobacillus reuteri in the ileum of ANP−/− mice. Ileal microbiota transfer (IMT) from ANP−/− mice to healthy C57BL/6J mice drove Lactobacillus johnsonii and Lactobacillus reuteri colonization in the ileum, which manifested an increase in BP, the HW/BW ratio, cardiac hypertrophy, and ileal pathology compared with IMT from WT mice. The HSD in C57BL/6J mice with IMT from ANP−/− mice drove the colonization of Burkholderiales bacterium YL45, Lactobacillus johnsonii, and Lactobacillus reuteri in the ileum and further exacerbated the cardiac and ileal pathology. Our results suggest that salt-sensitive ileal microbiota is probably related to ANP deficiency-induced cardiac injury.</description><subject>Antibiotics</subject><subject>Atrial natriuretic peptide</subject><subject>Bacteria</subject><subject>Blood pressure</subject><subject>Body weight</subject><subject>Burkholderiales</subject><subject>Colon</subject><subject>Colonization</subject><subject>Diet</subject><subject>Drinking water</subject><subject>Experiments</subject><subject>Feces</subject><subject>Fibrosis</subject><subject>Goblet cells</subject><subject>Heart</subject><subject>histology</subject><subject>Homeostasis</subject><subject>Hypertension</subject><subject>Hypertrophy</subject><subject>IL-1β</subject><subject>Ileum</subject><subject>Injury analysis</subject><subject>Laboratory animals</subject><subject>Lactobacillus johnsonii</subject><subject>Lactobacillus reuteri</subject><subject>microbiome</subject><subject>Microbiomes</subject><subject>Microbiota</subject><subject>occludins</subject><subject>Pathology</subject><subject>Peptides</subject><subject>Rodents</subject><subject>Salt</subject><subject>Salts</subject><subject>Small intestine</subject><subject>Thickening</subject><subject>TLR4 protein</subject><subject>Toll-like receptors</subject><subject>villi</subject><subject>Villus</subject><issn>2072-6643</issn><issn>2072-6643</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><sourceid>BENPR</sourceid><recordid>eNqNkU9r3DAQxUVpaUKSSz-BoJdQcCtpbNm-FMLmTxeSJiTtWYzlcatFK28lObDfPl4S2iSnzuUNzI_H8B5jH6T4DNCKL2GSpaxAqvYN21eiVoXWJbx9tu-xo5RWYje1qDW8Z3tQtZUGofeZv0OfizsKyWV3T3zpCT2_cjaOnRsz8huP28SR346euAv8JEc3E99x1ilSdpbf0Ca7nvgpDc46CnZbLEM_Wer5AmPv0PJlWE1xe8jeDegTHT3pAft5fvZj8a24vL5YLk4uC1tKnYtODdQoSdjXehBU6V5jTxIVDaQ6Qg3QaCUVQtWUCF1TYU2tElRbadEOcMC-Pvpupm5NvaWQI3qziW6NcWtGdOblJbjf5td4b1qYE2pgNjh-Mojjn4lSNmuXLHmPgcYpGVXLBrRulPgPVCjZCC3LGf34Cl2NUwxzEjtK1GWpQc3Up0dqriClSMPfv6Uwu8rNv8rhAdbinYQ</recordid><startdate>20220729</startdate><enddate>20220729</enddate><creator>Li, Siqi</creator><creator>Chen, Sishuo</creator><creator>Nie, Min</creator><creator>Wen, Lijing</creator><creator>Zou, Bin</creator><creator>Zhang, Lingyu</creator><creator>Xie, Jingzhou</creator><creator>Ser, Hooi-Leng</creator><creator>Lee, Learn-Han</creator><creator>Wang, Shunyi</creator><creator>Lin, Caixia</creator><creator>Pathak, Janak L.</creator><creator>Zhou, Weijie</creator><creator>Miao, Ji</creator><creator>Wang, Lijing</creator><creator>Zheng, Lingyun</creator><general>MDPI AG</general><general>MDPI</general><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7TS</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BENPR</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>K9.</scope><scope>M0S</scope><scope>M1P</scope><scope>PIMPY</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-3815-7436</orcidid><orcidid>https://orcid.org/0000-0002-3199-084X</orcidid><orcidid>https://orcid.org/0000-0003-2576-443X</orcidid><orcidid>https://orcid.org/0000-0002-8589-7456</orcidid><orcidid>https://orcid.org/0000-0001-9243-9923</orcidid><orcidid>https://orcid.org/0000-0003-0869-4492</orcidid></search><sort><creationdate>20220729</creationdate><title>Salt-Sensitive Ileal Microbiota Plays a Role in Atrial Natriuretic Peptide Deficiency-Induced Cardiac Injury</title><author>Li, Siqi ; Chen, Sishuo ; Nie, Min ; Wen, Lijing ; Zou, Bin ; Zhang, Lingyu ; Xie, Jingzhou ; Ser, Hooi-Leng ; Lee, Learn-Han ; Wang, Shunyi ; Lin, Caixia ; Pathak, Janak L. ; Zhou, Weijie ; Miao, Ji ; Wang, Lijing ; Zheng, Lingyun</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c416t-b2fe821ead76f0e56d6ade1a2efe2bea63386212a3584a3b85a7e920e7c1cacf3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Antibiotics</topic><topic>Atrial natriuretic peptide</topic><topic>Bacteria</topic><topic>Blood pressure</topic><topic>Body weight</topic><topic>Burkholderiales</topic><topic>Colon</topic><topic>Colonization</topic><topic>Diet</topic><topic>Drinking water</topic><topic>Experiments</topic><topic>Feces</topic><topic>Fibrosis</topic><topic>Goblet cells</topic><topic>Heart</topic><topic>histology</topic><topic>Homeostasis</topic><topic>Hypertension</topic><topic>Hypertrophy</topic><topic>IL-1β</topic><topic>Ileum</topic><topic>Injury analysis</topic><topic>Laboratory animals</topic><topic>Lactobacillus johnsonii</topic><topic>Lactobacillus reuteri</topic><topic>microbiome</topic><topic>Microbiomes</topic><topic>Microbiota</topic><topic>occludins</topic><topic>Pathology</topic><topic>Peptides</topic><topic>Rodents</topic><topic>Salt</topic><topic>Salts</topic><topic>Small intestine</topic><topic>Thickening</topic><topic>TLR4 protein</topic><topic>Toll-like receptors</topic><topic>villi</topic><topic>Villus</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Li, Siqi</creatorcontrib><creatorcontrib>Chen, Sishuo</creatorcontrib><creatorcontrib>Nie, Min</creatorcontrib><creatorcontrib>Wen, Lijing</creatorcontrib><creatorcontrib>Zou, Bin</creatorcontrib><creatorcontrib>Zhang, Lingyu</creatorcontrib><creatorcontrib>Xie, Jingzhou</creatorcontrib><creatorcontrib>Ser, Hooi-Leng</creatorcontrib><creatorcontrib>Lee, Learn-Han</creatorcontrib><creatorcontrib>Wang, Shunyi</creatorcontrib><creatorcontrib>Lin, Caixia</creatorcontrib><creatorcontrib>Pathak, Janak L.</creatorcontrib><creatorcontrib>Zhou, Weijie</creatorcontrib><creatorcontrib>Miao, Ji</creatorcontrib><creatorcontrib>Wang, Lijing</creatorcontrib><creatorcontrib>Zheng, Lingyun</creatorcontrib><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Physical Education Index</collection><collection>Health &amp; 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However, the role of ileal microbiota in salt sensitivity in ANP deficiency-related cardiac injury has not been investigated yet. This study used ANP−/− mice to analyze the role of the salt-sensitive ileal microbiome on cardiac injury. ANP−/− mice showed an increase in blood pressure (BP), the heart weight/body weight (HW/BW) ratio, and cardiac hypertrophy compared with wild-type (WT) mice. ANP deficiency did not impact the histological structure but reduced occludin expression in the ileum. Antibiotics significantly relieved BP and cardiac hypertrophy in ANP−/− mice. A high-salt diet (HSD) increased BP, the HW/BW ratio, and cardiac hypertrophy/fibrosis in WT and ANP−/− mice, and an HSD treatment in ANP−/− mice exacerbated these cardiac parameters. The HSD markedly decreased muscularis layer thickening, villus length, and numbers of Paneth and goblet cells in the ileum of WT and ANP−/− mice. Furthermore, the HSD increased the level of TLR4 and IL-1β in ANP−/− mice ileum compared with WT mice. Antibiotics reduced the HW/BW ratio, cardiac hypertrophy/fibrosis, and the level of TLR4 and IL-1β in the ileum, and rescued the muscularis layer thickening, villus length, and numbers of Paneth and goblet cells in the ileum of HSD-ANP−/− mice. Importantly, ANP deficiency induced the colonization of Burkholderiales bacterium YL45, Lactobacillus johnsonii, and Lactobacillus reuteri in the ileum on the NSD diet, which was only observed in HSD-induced WT mice but not in WT mice on the NSD. Besides, the HSD significantly enhanced the sum of the percentage of the colonization of Burkholderiales bacterium YL45, Lactobacillus johnsonii, and Lactobacillus reuteri in the ileum of ANP−/− mice. Ileal microbiota transfer (IMT) from ANP−/− mice to healthy C57BL/6J mice drove Lactobacillus johnsonii and Lactobacillus reuteri colonization in the ileum, which manifested an increase in BP, the HW/BW ratio, cardiac hypertrophy, and ileal pathology compared with IMT from WT mice. The HSD in C57BL/6J mice with IMT from ANP−/− mice drove the colonization of Burkholderiales bacterium YL45, Lactobacillus johnsonii, and Lactobacillus reuteri in the ileum and further exacerbated the cardiac and ileal pathology. Our results suggest that salt-sensitive ileal microbiota is probably related to ANP deficiency-induced cardiac injury.</abstract><cop>Basel</cop><pub>MDPI AG</pub><pmid>35956306</pmid><doi>10.3390/nu14153129</doi><orcidid>https://orcid.org/0000-0003-3815-7436</orcidid><orcidid>https://orcid.org/0000-0002-3199-084X</orcidid><orcidid>https://orcid.org/0000-0003-2576-443X</orcidid><orcidid>https://orcid.org/0000-0002-8589-7456</orcidid><orcidid>https://orcid.org/0000-0001-9243-9923</orcidid><orcidid>https://orcid.org/0000-0003-0869-4492</orcidid><oa>free_for_read</oa></addata></record>
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source MDPI - Multidisciplinary Digital Publishing Institute; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; PubMed Central; PubMed Central Open Access
subjects Antibiotics
Atrial natriuretic peptide
Bacteria
Blood pressure
Body weight
Burkholderiales
Colon
Colonization
Diet
Drinking water
Experiments
Feces
Fibrosis
Goblet cells
Heart
histology
Homeostasis
Hypertension
Hypertrophy
IL-1β
Ileum
Injury analysis
Laboratory animals
Lactobacillus johnsonii
Lactobacillus reuteri
microbiome
Microbiomes
Microbiota
occludins
Pathology
Peptides
Rodents
Salt
Salts
Small intestine
Thickening
TLR4 protein
Toll-like receptors
villi
Villus
title Salt-Sensitive Ileal Microbiota Plays a Role in Atrial Natriuretic Peptide Deficiency-Induced Cardiac Injury
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-02T22%3A02%3A59IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Salt-Sensitive%20Ileal%20Microbiota%20Plays%20a%20Role%20in%20Atrial%20Natriuretic%20Peptide%20Deficiency-Induced%20Cardiac%20Injury&rft.jtitle=Nutrients&rft.au=Li,%20Siqi&rft.date=2022-07-29&rft.volume=14&rft.issue=15&rft.spage=3129&rft.pages=3129-&rft.issn=2072-6643&rft.eissn=2072-6643&rft_id=info:doi/10.3390/nu14153129&rft_dat=%3Cproquest_pubme%3E2702180614%3C/proquest_pubme%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=2700744632&rft_id=info:pmid/35956306&rfr_iscdi=true