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Serotonin (5-HT) affects expression of liver metabolic enzymes and mammary gland glucose transporters during the transition from pregnancy to lactation.

Laporta J, Peters TL, Merriman KE, Vezina CM, Hernandez LL - PLoS ONE (2013)

Bottom Line: The aim of this experiment was to demonstrate the ability of feeding serotonin (5-HT; 5-hydroxytryptamine) precursors to increase 5-HT production during the transition from pregnancy to lactation and the effects this has on maternal energy metabolism in the liver and mammary gland.Feeding 5-HTP resulted in increased mRNA expression of key gluconeogenic and glycolytic enzymes in liver and glucose transporters 1 and 8 (GLUT-1, -8) in the mammary gland.Our results suggest that increasing 5-HT production during the transition from pregnancy to lactation increases mRNA expression of enzymes involved in energy metabolism in the liver, and mRNA abundance and distribution of glucose transporters within the mammary gland.

View Article: PubMed Central - PubMed

Affiliation: Department of Dairy Science, University of Wisconsin-Madison, Madison, Wisconsin, United States of America.

ABSTRACT
The aim of this experiment was to demonstrate the ability of feeding serotonin (5-HT; 5-hydroxytryptamine) precursors to increase 5-HT production during the transition from pregnancy to lactation and the effects this has on maternal energy metabolism in the liver and mammary gland. Pregnant rats (n = 45) were fed one of three diets: I) control (CON), II) CON supplemented with 0.2% 5-hydroxytryptophan (5-HTP) or III) CON supplemented with 1.35% L-tryptophan (L-TRP), beginning on d13 of pregnancy through d9 of lactation (d9). Serum (pre and post-partum), milk (daily), liver and mammary gland tissue (d9) were collected. Serum 5-HT was increased in the 5-HTP fed dams beginning on d20 of gestation and remained elevated through d9, while it was only increased on d9 in the L-TRP fed dams. 5-HT levels were increased in mammary gland and liver of both groups. Additionally, 5-HTP fed dams had serum and milk glucose levels similar to the CON, while L-TRP had decreased serum (d9) and milk glucose (all dates evaluated). Feeding 5-HTP resulted in increased mRNA expression of key gluconeogenic and glycolytic enzymes in liver and glucose transporters 1 and 8 (GLUT-1, -8) in the mammary gland. We demonstrated the location of GLUT-8 in the mammary gland both in the epithelial and vascular endothelial cells. Finally, phosphorylated 5' AMP-activated protein kinase (pAMPK), a known regulator of intracellular energy status, was elevated in mammary glands of 5-HTP fed dams. Our results suggest that increasing 5-HT production during the transition from pregnancy to lactation increases mRNA expression of enzymes involved in energy metabolism in the liver, and mRNA abundance and distribution of glucose transporters within the mammary gland. This suggests the possibility that 5-HT may be involved in regulating energy metabolism during the transition from pregnancy to lactation.

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Effects of feeding diets enriched in 5-HTP and L-TRP on serum 5-HT, insulin and glucose in rats.Serum 5-HT concentrations on d20 of gestation (d20-G), d1 and d9 of lactation (d1-L, d9-L) (A). 5-HT protein concentration and mRNA expression of TPH1 in the mammary gland (B-D) and liver (E-G) on d9-L. Serum insulin (H) and plasma glucose (I) concentrations on d20-G and d9-L, milk glucose concentrations at d1, d5 and d9 of lactation (J), in dams fed CON, 5-HTP, and L-TRP diets, and milk lactose concentrations at d1, d5, and d9 of lactation (I), in dams fed CON, 5-HTP, and L-TRP diets. Data are represented as mean ± SEM. Single asterisk (*) indicate statistical significance at P<0.05, two asterisks (**) at P<0.01, three (***) at P<0.001 and four (****) at P<0.0001.
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pone-0057847-g002: Effects of feeding diets enriched in 5-HTP and L-TRP on serum 5-HT, insulin and glucose in rats.Serum 5-HT concentrations on d20 of gestation (d20-G), d1 and d9 of lactation (d1-L, d9-L) (A). 5-HT protein concentration and mRNA expression of TPH1 in the mammary gland (B-D) and liver (E-G) on d9-L. Serum insulin (H) and plasma glucose (I) concentrations on d20-G and d9-L, milk glucose concentrations at d1, d5 and d9 of lactation (J), in dams fed CON, 5-HTP, and L-TRP diets, and milk lactose concentrations at d1, d5, and d9 of lactation (I), in dams fed CON, 5-HTP, and L-TRP diets. Data are represented as mean ± SEM. Single asterisk (*) indicate statistical significance at P<0.05, two asterisks (**) at P<0.01, three (***) at P<0.001 and four (****) at P<0.0001.

Mentions: We set out to determine if feeding precursors for 5-HT would not only increase circulating concentrations of 5-HT, but also whether the synthesis of 5-HT in the mammary gland and liver were also increased. It is a well-known fact that 5-HT is synthesized and secreted by various tissues throughout the body in addition to the circulating platelets, with the gut synthesizing approximately 95% of circulating 5-HT [26]. Serum 5-HT levels were greater in rats fed 5-HTP than CON for all times evaluated, and were only elevated in the L-TRP diet on d9 of lactation (P<0.01, Figure 2a). 5-HT concentrations were increased in mammary gland tissue of both 5-HTP and L-TRP dams compared to the CON (P<0.009, Figure 2b). In the liver, 5-HT was undetectable in the CON, but was increased in both the 5-HTP and L-TRP fed dams, with the 5-HTP fed dams exhibiting the highest levels of 5-HTP (P<0.04, Figure 2d). mRNA expression of TPH1 was increased in the 5-HTP group in both mammary gland and liver, and only in the liver of the L-TRP group (P<0.042, Figures 2c, e).


Serotonin (5-HT) affects expression of liver metabolic enzymes and mammary gland glucose transporters during the transition from pregnancy to lactation.

Laporta J, Peters TL, Merriman KE, Vezina CM, Hernandez LL - PLoS ONE (2013)

Effects of feeding diets enriched in 5-HTP and L-TRP on serum 5-HT, insulin and glucose in rats.Serum 5-HT concentrations on d20 of gestation (d20-G), d1 and d9 of lactation (d1-L, d9-L) (A). 5-HT protein concentration and mRNA expression of TPH1 in the mammary gland (B-D) and liver (E-G) on d9-L. Serum insulin (H) and plasma glucose (I) concentrations on d20-G and d9-L, milk glucose concentrations at d1, d5 and d9 of lactation (J), in dams fed CON, 5-HTP, and L-TRP diets, and milk lactose concentrations at d1, d5, and d9 of lactation (I), in dams fed CON, 5-HTP, and L-TRP diets. Data are represented as mean ± SEM. Single asterisk (*) indicate statistical significance at P<0.05, two asterisks (**) at P<0.01, three (***) at P<0.001 and four (****) at P<0.0001.
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Related In: Results  -  Collection

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pone-0057847-g002: Effects of feeding diets enriched in 5-HTP and L-TRP on serum 5-HT, insulin and glucose in rats.Serum 5-HT concentrations on d20 of gestation (d20-G), d1 and d9 of lactation (d1-L, d9-L) (A). 5-HT protein concentration and mRNA expression of TPH1 in the mammary gland (B-D) and liver (E-G) on d9-L. Serum insulin (H) and plasma glucose (I) concentrations on d20-G and d9-L, milk glucose concentrations at d1, d5 and d9 of lactation (J), in dams fed CON, 5-HTP, and L-TRP diets, and milk lactose concentrations at d1, d5, and d9 of lactation (I), in dams fed CON, 5-HTP, and L-TRP diets. Data are represented as mean ± SEM. Single asterisk (*) indicate statistical significance at P<0.05, two asterisks (**) at P<0.01, three (***) at P<0.001 and four (****) at P<0.0001.
Mentions: We set out to determine if feeding precursors for 5-HT would not only increase circulating concentrations of 5-HT, but also whether the synthesis of 5-HT in the mammary gland and liver were also increased. It is a well-known fact that 5-HT is synthesized and secreted by various tissues throughout the body in addition to the circulating platelets, with the gut synthesizing approximately 95% of circulating 5-HT [26]. Serum 5-HT levels were greater in rats fed 5-HTP than CON for all times evaluated, and were only elevated in the L-TRP diet on d9 of lactation (P<0.01, Figure 2a). 5-HT concentrations were increased in mammary gland tissue of both 5-HTP and L-TRP dams compared to the CON (P<0.009, Figure 2b). In the liver, 5-HT was undetectable in the CON, but was increased in both the 5-HTP and L-TRP fed dams, with the 5-HTP fed dams exhibiting the highest levels of 5-HTP (P<0.04, Figure 2d). mRNA expression of TPH1 was increased in the 5-HTP group in both mammary gland and liver, and only in the liver of the L-TRP group (P<0.042, Figures 2c, e).

Bottom Line: The aim of this experiment was to demonstrate the ability of feeding serotonin (5-HT; 5-hydroxytryptamine) precursors to increase 5-HT production during the transition from pregnancy to lactation and the effects this has on maternal energy metabolism in the liver and mammary gland.Feeding 5-HTP resulted in increased mRNA expression of key gluconeogenic and glycolytic enzymes in liver and glucose transporters 1 and 8 (GLUT-1, -8) in the mammary gland.Our results suggest that increasing 5-HT production during the transition from pregnancy to lactation increases mRNA expression of enzymes involved in energy metabolism in the liver, and mRNA abundance and distribution of glucose transporters within the mammary gland.

View Article: PubMed Central - PubMed

Affiliation: Department of Dairy Science, University of Wisconsin-Madison, Madison, Wisconsin, United States of America.

ABSTRACT
The aim of this experiment was to demonstrate the ability of feeding serotonin (5-HT; 5-hydroxytryptamine) precursors to increase 5-HT production during the transition from pregnancy to lactation and the effects this has on maternal energy metabolism in the liver and mammary gland. Pregnant rats (n = 45) were fed one of three diets: I) control (CON), II) CON supplemented with 0.2% 5-hydroxytryptophan (5-HTP) or III) CON supplemented with 1.35% L-tryptophan (L-TRP), beginning on d13 of pregnancy through d9 of lactation (d9). Serum (pre and post-partum), milk (daily), liver and mammary gland tissue (d9) were collected. Serum 5-HT was increased in the 5-HTP fed dams beginning on d20 of gestation and remained elevated through d9, while it was only increased on d9 in the L-TRP fed dams. 5-HT levels were increased in mammary gland and liver of both groups. Additionally, 5-HTP fed dams had serum and milk glucose levels similar to the CON, while L-TRP had decreased serum (d9) and milk glucose (all dates evaluated). Feeding 5-HTP resulted in increased mRNA expression of key gluconeogenic and glycolytic enzymes in liver and glucose transporters 1 and 8 (GLUT-1, -8) in the mammary gland. We demonstrated the location of GLUT-8 in the mammary gland both in the epithelial and vascular endothelial cells. Finally, phosphorylated 5' AMP-activated protein kinase (pAMPK), a known regulator of intracellular energy status, was elevated in mammary glands of 5-HTP fed dams. Our results suggest that increasing 5-HT production during the transition from pregnancy to lactation increases mRNA expression of enzymes involved in energy metabolism in the liver, and mRNA abundance and distribution of glucose transporters within the mammary gland. This suggests the possibility that 5-HT may be involved in regulating energy metabolism during the transition from pregnancy to lactation.

Show MeSH
Related in: MedlinePlus