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7α-Hydroxypregnenolone, a key neuronal modulator of locomotion, stimulates upstream migration by means of the dopaminergic system in salmon.

Haraguchi S, Yamamoto Y, Suzuki Y, Hyung Chang J, Koyama T, Sato M, Mita M, Ueda H, Tsutsui K - Sci Rep (2015)

Bottom Line: We first identified 7α-OH PREG and cytochrome P450 7α-hydroxylase (P4507α), a steroidogenic enzyme producing 7α-OH PREG, in the salmon brain and then found that 7α-OH PREG synthesis in the brain increases during upstream migration.We further found that 7α-OH PREG acts on dopamine neurons in the magnocellular preoptic nucleus during upstream migration.These findings provide new insights into the molecular mechanisms of fish upstream migration.

View Article: PubMed Central - PubMed

Affiliation: 1] Department of Biology and Center for Medical Life Science, Waseda University, Tokyo, Japan [2] Department of Biology, Tokyo Gakugei University, Tokyo, Japan.

ABSTRACT
Salmon migrate upstream against an opposing current in their natal river. However, the molecular mechanisms that stimulate upstream migratory behavior are poorly understood. Here, we show that 7α-hydroxypregnenolone (7α-OH PREG), a newly identified neuronal modulator of locomotion, acts as a key factor for upstream migration in salmon. We first identified 7α-OH PREG and cytochrome P450 7α-hydroxylase (P4507α), a steroidogenic enzyme producing 7α-OH PREG, in the salmon brain and then found that 7α-OH PREG synthesis in the brain increases during upstream migration. Subsequently, we demonstrated that 7α-OH PREG increases upstream migratory behavior of salmon. We further found that 7α-OH PREG acts on dopamine neurons in the magnocellular preoptic nucleus during upstream migration. Thus, 7α-OH PREG stimulates upstream migratory behavior through the dopaminergic system in salmon. These findings provide new insights into the molecular mechanisms of fish upstream migration.

No MeSH data available.


Changes in 7α-OH PREG synthesis and concentration, and Cyp7b mRNA expression in the brain of chum salmon Oncorhynchus keta during homing migration.(a,b) Salmon of both sexes were captured at the Bering Sea at the beginning of homing migration (a); Ishikari Bay, the entrance of upstream migration just prior to upstream migration (b); the pre-spawning ground during upstream migration (b); and the Chitose salmon hatchery, the goal of upstream migration just after upstream migration (b), Hokkaido, Japan. Canvas software (ACD Systems) was used to create the maps. (c) Changes in Cyp7b mRNA expression in the salmon brain during homing migration. (d) Changes in 7α-OH PREG synthesis in the salmon brain during homing migration. (e) Changes in 7α-OH PREG concentration in the salmon brain during homing migration. Each column and vertical line represent the mean ± s.e.m. of six independent samples. *P < 0.05 or **P < 0.01 versus Bering Sea.
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f2: Changes in 7α-OH PREG synthesis and concentration, and Cyp7b mRNA expression in the brain of chum salmon Oncorhynchus keta during homing migration.(a,b) Salmon of both sexes were captured at the Bering Sea at the beginning of homing migration (a); Ishikari Bay, the entrance of upstream migration just prior to upstream migration (b); the pre-spawning ground during upstream migration (b); and the Chitose salmon hatchery, the goal of upstream migration just after upstream migration (b), Hokkaido, Japan. Canvas software (ACD Systems) was used to create the maps. (c) Changes in Cyp7b mRNA expression in the salmon brain during homing migration. (d) Changes in 7α-OH PREG synthesis in the salmon brain during homing migration. (e) Changes in 7α-OH PREG concentration in the salmon brain during homing migration. Each column and vertical line represent the mean ± s.e.m. of six independent samples. *P < 0.05 or **P < 0.01 versus Bering Sea.

Mentions: To understand the physiological role of 7α-OH PREG during upstream migration, we examined changes in 7α-OH PREG synthesis and concentration, and Cyp7b mRNA expression in the salmon brain during homing migration that comprises upstream migration. Sexually mature adult chum salmon were collected from the Bering Sea to the Chitose salmon hatchery, Hokkaido, Japan during their homing migration (Fig. 2a,b). Fish of both sexes were captured from (i) the Bering Sea at the beginning of homing migration; (ii) the Ishikari Bay, the entrance of upstream migration just prior to upstream migration; (iii) the pre-spawning ground during upstream migration; and (iv) the Chitose salmon hatchery, the goal of upstream migration just after upstream migration (Fig. 2a,b). As shown in Fig. 2c, Cyp7b mRNA expression in the salmon brain of both sexes markedly changed at these different places during homing migration. Cyp7b mRNA was highly expressed in the brain of both sexes from the Ishikari Bay to the Chitose salmon hatchery compared with the Bering Sea (Fig. 2c). Similar changes in 7α-OH PREG synthesis in the brain of both sexes were detected (Fig. 2d). 7α-OH PREG concentration in the brain of both sexes also increased from the Ishikari Bay to the pre-spawning ground (Fig. 2e). However, 7α-OH PREG concentration in the brain was low at the Chitose salmon hatchery (Fig. 2e). These results indicate that 7α-OH PREG synthesis and concentration, and Cyp7b mRNA expression in the salmon brain increase just before and during upstream migration. In contrast to the brain, we did not detect a significant level of 7α-OH PREG in the plasma from the Bering Sea to the Chitose salmon hatchery during homing migration (Supplementary Fig. S2).


7α-Hydroxypregnenolone, a key neuronal modulator of locomotion, stimulates upstream migration by means of the dopaminergic system in salmon.

Haraguchi S, Yamamoto Y, Suzuki Y, Hyung Chang J, Koyama T, Sato M, Mita M, Ueda H, Tsutsui K - Sci Rep (2015)

Changes in 7α-OH PREG synthesis and concentration, and Cyp7b mRNA expression in the brain of chum salmon Oncorhynchus keta during homing migration.(a,b) Salmon of both sexes were captured at the Bering Sea at the beginning of homing migration (a); Ishikari Bay, the entrance of upstream migration just prior to upstream migration (b); the pre-spawning ground during upstream migration (b); and the Chitose salmon hatchery, the goal of upstream migration just after upstream migration (b), Hokkaido, Japan. Canvas software (ACD Systems) was used to create the maps. (c) Changes in Cyp7b mRNA expression in the salmon brain during homing migration. (d) Changes in 7α-OH PREG synthesis in the salmon brain during homing migration. (e) Changes in 7α-OH PREG concentration in the salmon brain during homing migration. Each column and vertical line represent the mean ± s.e.m. of six independent samples. *P < 0.05 or **P < 0.01 versus Bering Sea.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4518220&req=5

f2: Changes in 7α-OH PREG synthesis and concentration, and Cyp7b mRNA expression in the brain of chum salmon Oncorhynchus keta during homing migration.(a,b) Salmon of both sexes were captured at the Bering Sea at the beginning of homing migration (a); Ishikari Bay, the entrance of upstream migration just prior to upstream migration (b); the pre-spawning ground during upstream migration (b); and the Chitose salmon hatchery, the goal of upstream migration just after upstream migration (b), Hokkaido, Japan. Canvas software (ACD Systems) was used to create the maps. (c) Changes in Cyp7b mRNA expression in the salmon brain during homing migration. (d) Changes in 7α-OH PREG synthesis in the salmon brain during homing migration. (e) Changes in 7α-OH PREG concentration in the salmon brain during homing migration. Each column and vertical line represent the mean ± s.e.m. of six independent samples. *P < 0.05 or **P < 0.01 versus Bering Sea.
Mentions: To understand the physiological role of 7α-OH PREG during upstream migration, we examined changes in 7α-OH PREG synthesis and concentration, and Cyp7b mRNA expression in the salmon brain during homing migration that comprises upstream migration. Sexually mature adult chum salmon were collected from the Bering Sea to the Chitose salmon hatchery, Hokkaido, Japan during their homing migration (Fig. 2a,b). Fish of both sexes were captured from (i) the Bering Sea at the beginning of homing migration; (ii) the Ishikari Bay, the entrance of upstream migration just prior to upstream migration; (iii) the pre-spawning ground during upstream migration; and (iv) the Chitose salmon hatchery, the goal of upstream migration just after upstream migration (Fig. 2a,b). As shown in Fig. 2c, Cyp7b mRNA expression in the salmon brain of both sexes markedly changed at these different places during homing migration. Cyp7b mRNA was highly expressed in the brain of both sexes from the Ishikari Bay to the Chitose salmon hatchery compared with the Bering Sea (Fig. 2c). Similar changes in 7α-OH PREG synthesis in the brain of both sexes were detected (Fig. 2d). 7α-OH PREG concentration in the brain of both sexes also increased from the Ishikari Bay to the pre-spawning ground (Fig. 2e). However, 7α-OH PREG concentration in the brain was low at the Chitose salmon hatchery (Fig. 2e). These results indicate that 7α-OH PREG synthesis and concentration, and Cyp7b mRNA expression in the salmon brain increase just before and during upstream migration. In contrast to the brain, we did not detect a significant level of 7α-OH PREG in the plasma from the Bering Sea to the Chitose salmon hatchery during homing migration (Supplementary Fig. S2).

Bottom Line: We first identified 7α-OH PREG and cytochrome P450 7α-hydroxylase (P4507α), a steroidogenic enzyme producing 7α-OH PREG, in the salmon brain and then found that 7α-OH PREG synthesis in the brain increases during upstream migration.We further found that 7α-OH PREG acts on dopamine neurons in the magnocellular preoptic nucleus during upstream migration.These findings provide new insights into the molecular mechanisms of fish upstream migration.

View Article: PubMed Central - PubMed

Affiliation: 1] Department of Biology and Center for Medical Life Science, Waseda University, Tokyo, Japan [2] Department of Biology, Tokyo Gakugei University, Tokyo, Japan.

ABSTRACT
Salmon migrate upstream against an opposing current in their natal river. However, the molecular mechanisms that stimulate upstream migratory behavior are poorly understood. Here, we show that 7α-hydroxypregnenolone (7α-OH PREG), a newly identified neuronal modulator of locomotion, acts as a key factor for upstream migration in salmon. We first identified 7α-OH PREG and cytochrome P450 7α-hydroxylase (P4507α), a steroidogenic enzyme producing 7α-OH PREG, in the salmon brain and then found that 7α-OH PREG synthesis in the brain increases during upstream migration. Subsequently, we demonstrated that 7α-OH PREG increases upstream migratory behavior of salmon. We further found that 7α-OH PREG acts on dopamine neurons in the magnocellular preoptic nucleus during upstream migration. Thus, 7α-OH PREG stimulates upstream migratory behavior through the dopaminergic system in salmon. These findings provide new insights into the molecular mechanisms of fish upstream migration.

No MeSH data available.