Paternal dietary ratio of n-6: n-3 polyunsaturated fatty acids programs offspring leptin expression and gene imprinting in mice
BackgroundThis study determined the effects of the paternal dietary ratio of n-6: n-3 polyunsaturated fatty acids (PUFAs) on leptin expression in the offspring and associated gene imprinting in a mouse model.MethodsThree- to four-week-old male C57BL/6J mice (F0) were fed an n-3 PUFA-deficient (n-3 D...
| Main Authors: | , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Frontiers Media S.A.
2022-12-01
|
| Series: | Frontiers in Nutrition |
| Subjects: | |
| Online Access: | https://www.frontiersin.org/articles/10.3389/fnut.2022.1043876/full |
| _version_ | 1828088483201155072 |
|---|---|
| author | Qiaoyu Shi Xuanyi Liu Xiuqin Fan Rui Wang Kemin Qi |
| author_facet | Qiaoyu Shi Xuanyi Liu Xiuqin Fan Rui Wang Kemin Qi |
| author_sort | Qiaoyu Shi |
| collection | DOAJ |
| description | BackgroundThis study determined the effects of the paternal dietary ratio of n-6: n-3 polyunsaturated fatty acids (PUFAs) on leptin expression in the offspring and associated gene imprinting in a mouse model.MethodsThree- to four-week-old male C57BL/6J mice (F0) were fed an n-3 PUFA-deficient (n-3 D) diet, a diet with normal n-3 PUFA content (n-3 N; n-6: n-3 = 4.3:1), or a diet with a high n-3 PUFA content (n-3 H; n-6: n-3 = 1.5:1) for 8 weeks. Two subsequent generations were generated by mating F0 and F1 male mice with 10-week-old virgin female C57 BL/6J mice, to produce F1 and F2 offspring.ResultsCompared to the paternal n-3 D diet, paternal n-3 N and n-3 H diets reduced adipose mRNA expression of leptin (Lep) and its plasma concentrations in juvenile F1 male and female offspring, and adult F1 male and F2 female offspring, with upregulated Lep receptor mRNA expression in the hypothalamus. Meanwhile, paternal n-3 N and n-3 H diets altered the expression of the imprinted genes H19, Igf2, Igf2r, Plagl1, Cdkn1c, Kcnq1ot1, Peg3, and Grb10 in the adipose tissue of juvenile and adult F1 males, with almost no effects on F1 females, while more effects were observed in the adult F2 females than F2 males. Principal component analysis verified that Plagl1, Cdkn1c, and Kcnq1ot1 contributed the most to variation in adipose tissue expression in all offspring. Some of these genes (Plagl1, Cdkn1c, Kcnq1ot1, Peg3, and Grb10) were altered by the paternal n-3 N and n-3 H diets in the F1 and F2 generation testes as well. Furthermore, adipose Lep expression was positively correlated with expressions of H19, Igf2r, Plagl1, and Kcnq1ot1 in juvenile F1 males and females, negatively correlated with the Kcnq1ot1 expression in adult F1 males, and positively correlated with the Plagl1 expression in adult F2 females.ConclusionThese data imply that paternal Plagl1, Cdkn1c, and Kcnq1ot1 might be part of the pathways involved in offspring leptin programming. Therefore, a lower ratio of n-6: n-3 PUFAs, with higher intake of n-3 PUFAs in paternal pre-conception, may help maintain the offspring’s optimal leptin pattern in a sex-specific manner through multiple generations, and thereby, be beneficial for the offspring’s long-term health. |
| first_indexed | 2024-04-11T05:27:29Z |
| format | Article |
| id | doaj.art-bc5b941fd1ac44ddb91542d2322751cb |
| institution | Directory Open Access Journal |
| issn | 2296-861X |
| language | English |
| last_indexed | 2024-04-11T05:27:29Z |
| publishDate | 2022-12-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Nutrition |
| spelling | doaj.art-bc5b941fd1ac44ddb91542d2322751cb2022-12-23T06:19:34ZengFrontiers Media S.A.Frontiers in Nutrition2296-861X2022-12-01910.3389/fnut.2022.10438761043876Paternal dietary ratio of n-6: n-3 polyunsaturated fatty acids programs offspring leptin expression and gene imprinting in miceQiaoyu ShiXuanyi LiuXiuqin FanRui WangKemin QiBackgroundThis study determined the effects of the paternal dietary ratio of n-6: n-3 polyunsaturated fatty acids (PUFAs) on leptin expression in the offspring and associated gene imprinting in a mouse model.MethodsThree- to four-week-old male C57BL/6J mice (F0) were fed an n-3 PUFA-deficient (n-3 D) diet, a diet with normal n-3 PUFA content (n-3 N; n-6: n-3 = 4.3:1), or a diet with a high n-3 PUFA content (n-3 H; n-6: n-3 = 1.5:1) for 8 weeks. Two subsequent generations were generated by mating F0 and F1 male mice with 10-week-old virgin female C57 BL/6J mice, to produce F1 and F2 offspring.ResultsCompared to the paternal n-3 D diet, paternal n-3 N and n-3 H diets reduced adipose mRNA expression of leptin (Lep) and its plasma concentrations in juvenile F1 male and female offspring, and adult F1 male and F2 female offspring, with upregulated Lep receptor mRNA expression in the hypothalamus. Meanwhile, paternal n-3 N and n-3 H diets altered the expression of the imprinted genes H19, Igf2, Igf2r, Plagl1, Cdkn1c, Kcnq1ot1, Peg3, and Grb10 in the adipose tissue of juvenile and adult F1 males, with almost no effects on F1 females, while more effects were observed in the adult F2 females than F2 males. Principal component analysis verified that Plagl1, Cdkn1c, and Kcnq1ot1 contributed the most to variation in adipose tissue expression in all offspring. Some of these genes (Plagl1, Cdkn1c, Kcnq1ot1, Peg3, and Grb10) were altered by the paternal n-3 N and n-3 H diets in the F1 and F2 generation testes as well. Furthermore, adipose Lep expression was positively correlated with expressions of H19, Igf2r, Plagl1, and Kcnq1ot1 in juvenile F1 males and females, negatively correlated with the Kcnq1ot1 expression in adult F1 males, and positively correlated with the Plagl1 expression in adult F2 females.ConclusionThese data imply that paternal Plagl1, Cdkn1c, and Kcnq1ot1 might be part of the pathways involved in offspring leptin programming. Therefore, a lower ratio of n-6: n-3 PUFAs, with higher intake of n-3 PUFAs in paternal pre-conception, may help maintain the offspring’s optimal leptin pattern in a sex-specific manner through multiple generations, and thereby, be beneficial for the offspring’s long-term health.https://www.frontiersin.org/articles/10.3389/fnut.2022.1043876/fullgene imprintingpaternal programmingn-3 fatty acidsleptinoffspring |
| spellingShingle | Qiaoyu Shi Xuanyi Liu Xiuqin Fan Rui Wang Kemin Qi Paternal dietary ratio of n-6: n-3 polyunsaturated fatty acids programs offspring leptin expression and gene imprinting in mice Frontiers in Nutrition gene imprinting paternal programming n-3 fatty acids leptin offspring |
| title | Paternal dietary ratio of n-6: n-3 polyunsaturated fatty acids programs offspring leptin expression and gene imprinting in mice |
| title_full | Paternal dietary ratio of n-6: n-3 polyunsaturated fatty acids programs offspring leptin expression and gene imprinting in mice |
| title_fullStr | Paternal dietary ratio of n-6: n-3 polyunsaturated fatty acids programs offspring leptin expression and gene imprinting in mice |
| title_full_unstemmed | Paternal dietary ratio of n-6: n-3 polyunsaturated fatty acids programs offspring leptin expression and gene imprinting in mice |
| title_short | Paternal dietary ratio of n-6: n-3 polyunsaturated fatty acids programs offspring leptin expression and gene imprinting in mice |
| title_sort | paternal dietary ratio of n 6 n 3 polyunsaturated fatty acids programs offspring leptin expression and gene imprinting in mice |
| topic | gene imprinting paternal programming n-3 fatty acids leptin offspring |
| url | https://www.frontiersin.org/articles/10.3389/fnut.2022.1043876/full |
| work_keys_str_mv | AT qiaoyushi paternaldietaryratioofn6n3polyunsaturatedfattyacidsprogramsoffspringleptinexpressionandgeneimprintinginmice AT xuanyiliu paternaldietaryratioofn6n3polyunsaturatedfattyacidsprogramsoffspringleptinexpressionandgeneimprintinginmice AT xiuqinfan paternaldietaryratioofn6n3polyunsaturatedfattyacidsprogramsoffspringleptinexpressionandgeneimprintinginmice AT ruiwang paternaldietaryratioofn6n3polyunsaturatedfattyacidsprogramsoffspringleptinexpressionandgeneimprintinginmice AT keminqi paternaldietaryratioofn6n3polyunsaturatedfattyacidsprogramsoffspringleptinexpressionandgeneimprintinginmice |