Altered Gut Microbiota and Its Metabolites in Hypertension of Developmental Origins: Exploring Differences between Fructose and Antibiotics Exposure
Gut microbiota-derived metabolites, in particular short chain fatty acids (SCFAs) and their receptors, are linked to hypertension. Fructose and antibiotics are commonly used worldwide, and they have a negative impact on the gut microbiota. Our previous study revealed that maternal high-fructose (HF)...
| Main Authors: | , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
MDPI AG
2021-03-01
|
| Series: | International Journal of Molecular Sciences |
| Subjects: | |
| Online Access: | https://www.mdpi.com/1422-0067/22/5/2674 |
| _version_ | 1797412842739073024 |
|---|---|
| author | Chien-Ning Hsu Julie Y. H. Chan Kay L. H. Wu Hong-Ren Yu Wei-Chia Lee Chih-Yao Hou You-Lin Tain |
| author_facet | Chien-Ning Hsu Julie Y. H. Chan Kay L. H. Wu Hong-Ren Yu Wei-Chia Lee Chih-Yao Hou You-Lin Tain |
| author_sort | Chien-Ning Hsu |
| collection | DOAJ |
| description | Gut microbiota-derived metabolites, in particular short chain fatty acids (SCFAs) and their receptors, are linked to hypertension. Fructose and antibiotics are commonly used worldwide, and they have a negative impact on the gut microbiota. Our previous study revealed that maternal high-fructose (HF) diet-induced hypertension in adult offspring is relevant to altered gut microbiome and its metabolites. We, therefore, intended to examine whether minocycline administration during pregnancy and lactation may further affect blood pressure (BP) programmed by maternal HF intake via mediating gut microbiota and SCFAs. Pregnant Sprague-Dawley rats received a normal diet or diet containing 60% fructose throughout pregnancy and lactation periods. Additionally, pregnant dams received minocycline (50 mg/kg/day) via oral gavage or a vehicle during pregnancy and lactation periods. Four groups of male offspring were studied (<i>n</i> = 8 per group): normal diet (ND), high-fructose diet (HF), normal diet + minocycline (NDM), and HF + minocycline (HFM). Male offspring were killed at 12 weeks of age. We observed that the HF diet and minocycline administration, both individually and together, causes the elevation of BP in adult male offspring, while there is no synergistic effect between them. Four groups displayed distinct enterotypes. Minocycline treatment leads to an increase in the F/B ratio, but decreased abundance of genera <i>Lactobacillus</i>, <i>Ruminococcus</i>, and <i>Odoribacter</i>. Additionally, minocycline treatment decreases plasma acetic acid and butyric acid levels. Hypertension programmed by maternal HF diet plus minocycline exposure is related to the increased expression of several SCFA receptors. Moreover, minocycline- and HF-induced hypertension, individually or together, is associated with the aberrant activation of the renin–angiotensin system (RAS). Conclusively, our results provide a new insight into the support of gut microbiota and its metabolite SCAFs in the developmental programming of hypertension and cast new light on the role of RAS in this process, which will help prevent hypertension programmed by maternal high-fructose and antibiotic exposure. |
| first_indexed | 2024-03-09T05:09:05Z |
| format | Article |
| id | doaj.art-6e24aed268234f10acbd0b6ea901f652 |
| institution | Directory Open Access Journal |
| issn | 1661-6596 1422-0067 |
| language | English |
| last_indexed | 2024-03-09T05:09:05Z |
| publishDate | 2021-03-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | International Journal of Molecular Sciences |
| spelling | doaj.art-6e24aed268234f10acbd0b6ea901f6522023-12-03T12:51:30ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672021-03-01225267410.3390/ijms22052674Altered Gut Microbiota and Its Metabolites in Hypertension of Developmental Origins: Exploring Differences between Fructose and Antibiotics ExposureChien-Ning Hsu0Julie Y. H. Chan1Kay L. H. Wu2Hong-Ren Yu3Wei-Chia Lee4Chih-Yao Hou5You-Lin Tain6Department of Pharmacy, Kaohsiung Chang Gung Memorial Hospital, Kaohsiung 833, TaiwanInstitute for Translational Research in Biomedicine, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung 833, TaiwanInstitute for Translational Research in Biomedicine, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung 833, TaiwanDepartment of Pediatrics, Kaohsiung Chang Gung Memorial Hospital, Chang Gung University College of Medicine, Kaohsiung 833, TaiwanDepartment of Urology, Kaohsiung Chang Gung Memorial Hospital, Chang Gung University College of Medicine, Kaohsiung 833, TaiwanDepartment of Seafood Science, National Kaohsiung University of Science and Technology, Kaohsiung 811, TaiwanInstitute for Translational Research in Biomedicine, Kaohsiung Chang Gung Memorial Hospital and Chang Gung University College of Medicine, Kaohsiung 833, TaiwanGut microbiota-derived metabolites, in particular short chain fatty acids (SCFAs) and their receptors, are linked to hypertension. Fructose and antibiotics are commonly used worldwide, and they have a negative impact on the gut microbiota. Our previous study revealed that maternal high-fructose (HF) diet-induced hypertension in adult offspring is relevant to altered gut microbiome and its metabolites. We, therefore, intended to examine whether minocycline administration during pregnancy and lactation may further affect blood pressure (BP) programmed by maternal HF intake via mediating gut microbiota and SCFAs. Pregnant Sprague-Dawley rats received a normal diet or diet containing 60% fructose throughout pregnancy and lactation periods. Additionally, pregnant dams received minocycline (50 mg/kg/day) via oral gavage or a vehicle during pregnancy and lactation periods. Four groups of male offspring were studied (<i>n</i> = 8 per group): normal diet (ND), high-fructose diet (HF), normal diet + minocycline (NDM), and HF + minocycline (HFM). Male offspring were killed at 12 weeks of age. We observed that the HF diet and minocycline administration, both individually and together, causes the elevation of BP in adult male offspring, while there is no synergistic effect between them. Four groups displayed distinct enterotypes. Minocycline treatment leads to an increase in the F/B ratio, but decreased abundance of genera <i>Lactobacillus</i>, <i>Ruminococcus</i>, and <i>Odoribacter</i>. Additionally, minocycline treatment decreases plasma acetic acid and butyric acid levels. Hypertension programmed by maternal HF diet plus minocycline exposure is related to the increased expression of several SCFA receptors. Moreover, minocycline- and HF-induced hypertension, individually or together, is associated with the aberrant activation of the renin–angiotensin system (RAS). Conclusively, our results provide a new insight into the support of gut microbiota and its metabolite SCAFs in the developmental programming of hypertension and cast new light on the role of RAS in this process, which will help prevent hypertension programmed by maternal high-fructose and antibiotic exposure.https://www.mdpi.com/1422-0067/22/5/2674developmental origins of health and disease (DOHaD)fructosegut microbiotahypertensionminocyclinenitric oxide |
| spellingShingle | Chien-Ning Hsu Julie Y. H. Chan Kay L. H. Wu Hong-Ren Yu Wei-Chia Lee Chih-Yao Hou You-Lin Tain Altered Gut Microbiota and Its Metabolites in Hypertension of Developmental Origins: Exploring Differences between Fructose and Antibiotics Exposure International Journal of Molecular Sciences developmental origins of health and disease (DOHaD) fructose gut microbiota hypertension minocycline nitric oxide |
| title | Altered Gut Microbiota and Its Metabolites in Hypertension of Developmental Origins: Exploring Differences between Fructose and Antibiotics Exposure |
| title_full | Altered Gut Microbiota and Its Metabolites in Hypertension of Developmental Origins: Exploring Differences between Fructose and Antibiotics Exposure |
| title_fullStr | Altered Gut Microbiota and Its Metabolites in Hypertension of Developmental Origins: Exploring Differences between Fructose and Antibiotics Exposure |
| title_full_unstemmed | Altered Gut Microbiota and Its Metabolites in Hypertension of Developmental Origins: Exploring Differences between Fructose and Antibiotics Exposure |
| title_short | Altered Gut Microbiota and Its Metabolites in Hypertension of Developmental Origins: Exploring Differences between Fructose and Antibiotics Exposure |
| title_sort | altered gut microbiota and its metabolites in hypertension of developmental origins exploring differences between fructose and antibiotics exposure |
| topic | developmental origins of health and disease (DOHaD) fructose gut microbiota hypertension minocycline nitric oxide |
| url | https://www.mdpi.com/1422-0067/22/5/2674 |
| work_keys_str_mv | AT chienninghsu alteredgutmicrobiotaanditsmetabolitesinhypertensionofdevelopmentaloriginsexploringdifferencesbetweenfructoseandantibioticsexposure AT julieyhchan alteredgutmicrobiotaanditsmetabolitesinhypertensionofdevelopmentaloriginsexploringdifferencesbetweenfructoseandantibioticsexposure AT kaylhwu alteredgutmicrobiotaanditsmetabolitesinhypertensionofdevelopmentaloriginsexploringdifferencesbetweenfructoseandantibioticsexposure AT hongrenyu alteredgutmicrobiotaanditsmetabolitesinhypertensionofdevelopmentaloriginsexploringdifferencesbetweenfructoseandantibioticsexposure AT weichialee alteredgutmicrobiotaanditsmetabolitesinhypertensionofdevelopmentaloriginsexploringdifferencesbetweenfructoseandantibioticsexposure AT chihyaohou alteredgutmicrobiotaanditsmetabolitesinhypertensionofdevelopmentaloriginsexploringdifferencesbetweenfructoseandantibioticsexposure AT youlintain alteredgutmicrobiotaanditsmetabolitesinhypertensionofdevelopmentaloriginsexploringdifferencesbetweenfructoseandantibioticsexposure |