Effect of Methyl Farnesoate, Alone and in Combination with Other Hormones, on Ovarian Growth of the Red Swamp Crayfish, Procambarus clarkii, during Vitellogenesis

doi:10.1006/gcen.2001.7724

General and Comparative Endocrinology

Volume 125, Issue 1, January 2002, Pages 34-40

https://doi.org/10.1006/gcen.2001.7724 Get rights and content

Abstract

The effect of methyl farnesoate (MF) on the ovaries of female red swamp crayfish, Procambarus clarkii, undergoing vitellogenesis was determined both in vivo and in vitro. The in vivo assay showed a positive effect of MF on oocyte growth when injected alone and in combination with 17β-estradiol, but not in combination with JHIII or 17α-hydroxyprogesterone. A higher level of incorporation of labeled leucine was induced by MF on isolated pieces of ovary. The same effect was seen when ovary and mandibular organ (MO) were coincubated. These results suggest that MF stimulated the synthesis of vitellin in the ovary of crayfish. In vitro, 17α-hydroxyprogesterone completely suppressed the stimulatory action of the MO on the ovary, suggesting a competitive inhibition between 17α-hydroxyprogesterone and MF on the ovary and/or a negative feedback by that steroid on the MO.

References (39)

E.F. Couch et al.
Changes in estradiol and progesterone immunoactivities in tissues of the lobster, Homarus americanus, with developing and immature ovaries
Comp. Biochem. Physiol. A
(1987)
E. Homola et al.
Methyl farnesoate: Crustacean juvenile hormone in search of function
Comp. Biochem. Physiol. B
(1997)
H. Laufer et al.
Stimulation of ovarian maturation in the crayfish Procambarus clarkii by methyl farnesoate
Gen. Comp. Endocrinol.
(1998)
L. Liu et al.
A neurohormone regulating both methyl farnesoate synthesis and glucose metabolism in a crustacean
Biochem. Biophys. Res. Commun.
(1997)
E.T. Quinitio et al.
Changes in the steroid hormone and vitellogenin levels during the gametogenic cycle of the giant tiger shrimp, Penaeus monodon
Comp. Biochem. Physiol. C
(1994)
E.M. Rodríguez et al.
Inhibition of ovarian growth by cadmium, in the fiddler crab, Uca pugilator (Decapoda, Ocypodidae)
Ecotoxicol. Environ. Safety
(2000)
R. Sarojini et al.
Dopaminergic and enkephalinergic involvement in the regulation of blood glucose in the red swamp crayfish, Procambarus clarkii
Gen. Comp. Endocrinol.
(1995)
S.L. Tamone et al.
Methyl farnesoate stimulates ecdysteroid secretion from Y-organs in vitro
Gen. Comp. Endocrinol.
(1993)
B. Tsukimura et al.
In vitro stimulation of oocytes by presumptive mandibular organ secretions in the shrimp, Penaeus vannamei
Aquaculture
(1991)
I. Yano
Induced ovarian maturation and spawning in greasyback shrimp, Metapenaeus ensis, by progesterone
Aquaculture
(1985)

I. Yano

Effect of 17 α-hydroxy-progesterone on vitellogenin secretion in kuruma prawn, Penaeus japonicus

Aquaculture

(1987)

N.J. Young et al.

Progesterone metabolism in vitro in the decapod crustacean, Penaeus monodon

Gen. Comp. Endocrinol.

(1992)

E.S. Chang

Chemistry of crustacean hormones that regulate growth and reproduction

E.S. Chang

Comparative endocrinology of molting and reproduction: Insects and crustaceans

Annu. Rev. Entomol.

(1993)

G. Charmantier et al.

Hormonal regulation of growth and reproduction in crustaceans

S.B. Eastman-Reks et al.

In vitro synthesis of vitellin by the ovary of the fiddler crab Uca pugilator

J. Exp. Zool.

(1985)

M. Fingerman

Endocrine mechanisms in crayfish, with emphasis on reproduction and neurotransmitter regulation of hormone release

Am. Zool.

(1995)

M. Fingerman

Roles of neurotransmitters in regulating reproductive hormone release and gonadal maturation in decapod crustaceans

Invertebr. Reprod. Dev.

(1997)

M. Fingerman et al.

Vertebrate-type hormones in crustaceans: Localization, identification and functional significance

Zool. Sci.

(1993)

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Regular ArticleEffect of Methyl Farnesoate, Alone and in Combination with Other Hormones, on Ovarian Growth of the Red Swamp Crayfish, Procambarus clarkii, during Vitellogenesis

Abstract

Comp. Biochem. Physiol. A

Comp. Biochem. Physiol. B

Gen. Comp. Endocrinol.

Biochem. Biophys. Res. Commun.

Comp. Biochem. Physiol. C

Ecotoxicol. Environ. Safety

Gen. Comp. Endocrinol.

Gen. Comp. Endocrinol.

Aquaculture

Aquaculture

Aquaculture

Gen. Comp. Endocrinol.

Chemistry of crustacean hormones that regulate growth and reproduction

Comparative endocrinology of molting and reproduction: Insects and crustaceans

Annu. Rev. Entomol.

Hormonal regulation of growth and reproduction in crustaceans

In vitro synthesis of vitellin by the ovary of the fiddler crab Uca pugilator

J. Exp. Zool.

Endocrine mechanisms in crayfish, with emphasis on reproduction and neurotransmitter regulation of hormone release

Am. Zool.

Roles of neurotransmitters in regulating reproductive hormone release and gonadal maturation in decapod crustaceans

Invertebr. Reprod. Dev.

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Zool. Sci.

Regular Article
Effect of Methyl Farnesoate, Alone and in Combination with Other Hormones, on Ovarian Growth of the Red Swamp Crayfish, Procambarus clarkii, during Vitellogenesis