Regulation of nuclear binding of the avian oviduct progesterone receptor. Changes during estrogen-induced oviduct development, withdrawal, and secondary stimulation

P. Boyd-Leinen, B. Gosse, K. Rasmussen, G. Martin-Dani, T. C. Spelsberg

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38 Scopus citations

Abstract

The progesterone receptors from various stages of estrogen induced oviduct development, estrogen withdrawal, and secondary stimulation with estrogen were examined. The progesterone receptors were characterized for their biological function (i.e. capacity for nuclear translocation, nuclear binding, and effects on RNA polymerase II activity) as well as certain physical properties. The progesterone receptors from the undeveloped or partially developed oviducts (0 to 8 days of estrogen treatment) displayed litte or no nuclear translocation and binding in vivo and in vitro. Similarly, progesterone showed little or no effect in vivo on RNA polymerase II activity at the early stages of development. As development progressed from 8 to 12 days of estrogen treatment, the above parameters rapidly increased to maximal levels and plateaued through day 23 of estrogen treatment. A marked decrease in these parameters occurred within 1 day of estrogen withdrawal. The reverse series of events occurred during secondary estrogen stimulation of 10-day-old withdrawn chicks. While the receptor concentrations increase rapidly to maximum values by 2 days of restimulation, receptor function did not return untill day 4. Similarly, the effects of progesterone on RNA polymerase II activity reached maximal values by day 4. The progesterone receptor isolated from oviducts during development, estrogen withdrawal, and restimulation, displayed similar patterns of cell-free binding to chromatin and nucleoacidic protein as that observed in vivo supporting the nativeness of the in vitro binding assay. In contrast, the cell-free binding of these same progesterone receptor to pure DNA were not similar to the in vivo binding, i.e. no patterns (differences) in progesterone receptor binding were observed. These data support that protein DNA complexes and not pure DNA represent the native acceptors sites for oviduct progesterone receptor. Comparison of the progesterone receptor between the functional and nonfunctional states revealed no differences in the steroid affinity for the receptor, in the apparent pI of the species, or in the sedimentation of the receptor under high salt conditions. However, the nonfunctional receptors consistently displayed a deficiency in one of the two monomer molecular species (the B species) as determined by isoelectric focusing. These results suggest that both monomer species of progesterone receptor are required for biological activity. Interestingly, the 7S 'aggregate' species of the progesterone receptor was constantly detected even when only one of the monomer species was present. The data suggest that a possible indirect action of progesterone on gene expression in the estrogen withdrawn chicks, e.g. formation of metabolites of progesterone, such as estrogen and hydrocortisone, which in turn may regulate genes. These studies also show that estrogen regulates not only the concentration, but more profoundly, the biological activity of the progesterone receptor. The existence of another level of regulation of steroid action in animals, represented by a differential responsiveness of a target tissue to vascular steroids, is indicated.

Original languageEnglish (US)
Pages (from-to)2411-2421
Number of pages11
JournalJournal of Biological Chemistry
Volume259
Issue number4
StatePublished - 1984

ASJC Scopus subject areas

  • Biochemistry
  • Molecular Biology
  • Cell Biology

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