Perinatal Propionate Supplementation Protects Adult Male Offspring from Maternal Chronic Kidney Disease-Induced Hypertension
Emerging evidence supports that early-life disturbance of gut microbiota has an impact on adult disease in later life. Offspring hypertension can be programmed by maternal chronic kidney disease (CKD). Conversely, perinatal use of gut microbiota-targeted therapy has been implemented to reverse progr...
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MDPI AG
2022-08-01
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| Series: | Nutrients |
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| Online Access: | https://www.mdpi.com/2072-6643/14/16/3435 |
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| author | You-Lin Tain Chih-Yao Hou Guo-Ping Chang-Chien Su-Fan Lin Chien-Ning Hsu |
| author_facet | You-Lin Tain Chih-Yao Hou Guo-Ping Chang-Chien Su-Fan Lin Chien-Ning Hsu |
| author_sort | You-Lin Tain |
| collection | DOAJ |
| description | Emerging evidence supports that early-life disturbance of gut microbiota has an impact on adult disease in later life. Offspring hypertension can be programmed by maternal chronic kidney disease (CKD). Conversely, perinatal use of gut microbiota-targeted therapy has been implemented to reverse programming processes and prevent hypertension. Short-chain fatty acids (SCFAs), the major gut microbiota-derived metabolites, can be applied as postbiotics. Propionate, one of predominant SCFAs, has been shown to have antihypertensive property. We examined whether perinatal propionate supplementation can prevent offspring hypertension induced by maternal CKD. CKD was induced by chow supplemented with 0.5% adenine for 3 weeks before pregnancy. Propionate (P) was supplemented at 200 mmol/L in drinking water during pregnancy and lactation. Male offspring were divided into four groups (<i>n</i> = 7–8/group): control, CKD, control+propionate (CP), and CKD+propionate (CKDP). Maternal CKD-induced offspring hypertension was reversed by perinatal propionate supplementation. The protective effects of perinatal propionate treatment were related to increased propionate-generating bacteria <i>Clostridium</i> spp. and plasma propionate level, increased expression of renal G protein-coupled receptor 41 (GPR41, a SCFA receptor), augmentation of α-diversity, and shifts in gut microbiota composition. In summary, our results highlight that maternal CKD-induced offspring hypertension can be prevented by the use of gut microbial metabolite SCFAs in early life, which could shed light on the prevention of the current hypertension pandemic. |
| first_indexed | 2024-03-09T09:50:58Z |
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| institution | Directory Open Access Journal |
| issn | 2072-6643 |
| language | English |
| last_indexed | 2024-03-09T09:50:58Z |
| publishDate | 2022-08-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Nutrients |
| spelling | doaj.art-6fa9c18d2dd340e1a9266ed92ef22fe92023-12-02T00:07:42ZengMDPI AGNutrients2072-66432022-08-011416343510.3390/nu14163435Perinatal Propionate Supplementation Protects Adult Male Offspring from Maternal Chronic Kidney Disease-Induced HypertensionYou-Lin Tain0Chih-Yao Hou1Guo-Ping Chang-Chien2Su-Fan Lin3Chien-Ning Hsu4Department of Pediatrics, Kaohsiung Chang Gung Memorial Hospital, Kaohsiung 833, TaiwanDepartment of Seafood Science, National Kaohsiung University of Science and Technology, Kaohsiung 811, TaiwanInstitute of Environmental Toxin and Emerging-Contaminant, Cheng Shiu University, Kaohsiung 833, TaiwanInstitute of Environmental Toxin and Emerging-Contaminant, Cheng Shiu University, Kaohsiung 833, TaiwanDepartment of Pharmacy, Kaohsiung Chang Gung Memorial Hospital, Kaohsiung 833, TaiwanEmerging evidence supports that early-life disturbance of gut microbiota has an impact on adult disease in later life. Offspring hypertension can be programmed by maternal chronic kidney disease (CKD). Conversely, perinatal use of gut microbiota-targeted therapy has been implemented to reverse programming processes and prevent hypertension. Short-chain fatty acids (SCFAs), the major gut microbiota-derived metabolites, can be applied as postbiotics. Propionate, one of predominant SCFAs, has been shown to have antihypertensive property. We examined whether perinatal propionate supplementation can prevent offspring hypertension induced by maternal CKD. CKD was induced by chow supplemented with 0.5% adenine for 3 weeks before pregnancy. Propionate (P) was supplemented at 200 mmol/L in drinking water during pregnancy and lactation. Male offspring were divided into four groups (<i>n</i> = 7–8/group): control, CKD, control+propionate (CP), and CKD+propionate (CKDP). Maternal CKD-induced offspring hypertension was reversed by perinatal propionate supplementation. The protective effects of perinatal propionate treatment were related to increased propionate-generating bacteria <i>Clostridium</i> spp. and plasma propionate level, increased expression of renal G protein-coupled receptor 41 (GPR41, a SCFA receptor), augmentation of α-diversity, and shifts in gut microbiota composition. In summary, our results highlight that maternal CKD-induced offspring hypertension can be prevented by the use of gut microbial metabolite SCFAs in early life, which could shed light on the prevention of the current hypertension pandemic.https://www.mdpi.com/2072-6643/14/16/3435gut microbiotashort-chain fatty aciddevelopmental origins of health and disease (DOHaD)propionatehypertensionchronic kidney disease |
| spellingShingle | You-Lin Tain Chih-Yao Hou Guo-Ping Chang-Chien Su-Fan Lin Chien-Ning Hsu Perinatal Propionate Supplementation Protects Adult Male Offspring from Maternal Chronic Kidney Disease-Induced Hypertension Nutrients gut microbiota short-chain fatty acid developmental origins of health and disease (DOHaD) propionate hypertension chronic kidney disease |
| title | Perinatal Propionate Supplementation Protects Adult Male Offspring from Maternal Chronic Kidney Disease-Induced Hypertension |
| title_full | Perinatal Propionate Supplementation Protects Adult Male Offspring from Maternal Chronic Kidney Disease-Induced Hypertension |
| title_fullStr | Perinatal Propionate Supplementation Protects Adult Male Offspring from Maternal Chronic Kidney Disease-Induced Hypertension |
| title_full_unstemmed | Perinatal Propionate Supplementation Protects Adult Male Offspring from Maternal Chronic Kidney Disease-Induced Hypertension |
| title_short | Perinatal Propionate Supplementation Protects Adult Male Offspring from Maternal Chronic Kidney Disease-Induced Hypertension |
| title_sort | perinatal propionate supplementation protects adult male offspring from maternal chronic kidney disease induced hypertension |
| topic | gut microbiota short-chain fatty acid developmental origins of health and disease (DOHaD) propionate hypertension chronic kidney disease |
| url | https://www.mdpi.com/2072-6643/14/16/3435 |
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