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4. Phosphatases modified by LH signaling in ovarian follicles: testing their role in regulating the NPR2 guanylyl cyclase†

Author

Egbert, Jeremy R, Silbern, Ivan, Uliasz, Tracy F, Lowther, Katie M, Yee, Siu-Pok, Urlaub, Henning, and Jaffe, Laurinda A

Abstract

In response to luteinizing hormone (LH), multiple proteins in rat and mouse granulosa cells are rapidly dephosphorylated, but the responsible phosphatases remain to be identified. Because the phosphorylation state of phosphatases can regulate their interaction with substrates, we searched for phosphatases that might function in LH signaling by using quantitative mass spectrometry. We identified all proteins in rat ovarian follicles whose phosphorylation state changed detectably in response to a 30-min exposure to LH, and within this list, identified protein phosphatases or phosphatase regulatory subunits that showed changes in phosphorylation. Phosphatases in the phosphoprotein phosphatase (PPP) family were of particular interest because of their requirement for dephosphorylating the natriuretic peptide receptor 2 (NPR2) guanylyl cyclase in the granulosa cells, which triggers oocyte meiotic resumption. Among the PPP family regulatory subunits, PPP1R12A and PPP2R5D showed the largest increases in phosphorylation, with 4–10 fold increases in signal intensity on several sites. Although follicles from mice in which these phosphorylations were prevented by serine-to-alanine mutations in either Ppp1r12aor Ppp2r5dshowed normal LH-induced NPR2 dephosphorylation, these regulatory subunits and others could act redundantly to dephosphorylate NPR2. Our identification of phosphatases and other proteins whose phosphorylation state is rapidly modified by LH provides clues about multiple signaling pathways in ovarian follicles.Quantitative mass spectrometric analysis of phosphatases whose phosphorylation state is rapidly modified by LH provides clues about how LH signaling dephosphorylates NPR2 as well as a resource for future studies.Graphical Abstract

Published
2024
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7. Additional file 4 of A CRISPR toolbox for generating intersectional genetic mouse models for functional, molecular, and anatomical circuit mapping

Author

Lusk, Savannah J., McKinney, Andrew, Hunt, Patrick J., Fahey, Paul G., Patel, Jay, Chang, Andersen, Sun, Jenny J., Martinez, Vena K., Zhu, Ping Jun, Egbert, Jeremy R., Allen, Genevera, Jiang, Xiaolong, Arenkiel, Benjamin R., Tolias, Andreas S., Costa-Mattioli, Mauro, and Ray, Russell S.

Abstract

Additional file 4: Figure S4. Residual plots for independence testing of residuals from plethysmography analyses from Fig. 8. Description of data: Plot of residuals vs model predicted values of the dependent variable.

Published
2022
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8. Additional file 5 of A CRISPR toolbox for generating intersectional genetic mouse models for functional, molecular, and anatomical circuit mapping

Author

Lusk, Savannah J., McKinney, Andrew, Hunt, Patrick J., Fahey, Paul G., Patel, Jay, Chang, Andersen, Sun, Jenny J., Martinez, Vena K., Zhu, Ping Jun, Egbert, Jeremy R., Allen, Genevera, Jiang, Xiaolong, Arenkiel, Benjamin R., Tolias, Andreas S., Costa-Mattioli, Mauro, and Ray, Russell S.

Abstract

Additional file 5: Figure S5. QQplots for normal distribution testing of residuals from plethysmography analyses from Fig. 9. Plot of the empirical quantiles of the residual distributions vs the theoretical quantiles of gaussian distributions.

Published
2022
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9. Additional file 1 of A CRISPR toolbox for generating intersectional genetic mouse models for functional, molecular, and anatomical circuit mapping

Author

Lusk, Savannah J., McKinney, Andrew, Hunt, Patrick J., Fahey, Paul G., Patel, Jay, Chang, Andersen, Sun, Jenny J., Martinez, Vena K., Zhu, Ping Jun, Egbert, Jeremy R., Allen, Genevera, Jiang, Xiaolong, Arenkiel, Benjamin R., Tolias, Andreas S., Costa-Mattioli, Mauro, and Ray, Russell S.

Abstract

Additional file 1: Figure S1. Genetic schema for animals used to gather data for Figures 3 and 4. Vector diagrams for the transgenes present in mice used for anatomical fluorescence experiments in Figures 3 and 4. Demonstration of source of recombinase for animals from each panel in the figures.

Published
2022
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10. Additional file 3 of A CRISPR toolbox for generating intersectional genetic mouse models for functional, molecular, and anatomical circuit mapping

Author

Lusk, Savannah J., McKinney, Andrew, Hunt, Patrick J., Fahey, Paul G., Patel, Jay, Chang, Andersen, Sun, Jenny J., Martinez, Vena K., Zhu, Ping Jun, Egbert, Jeremy R., Allen, Genevera, Jiang, Xiaolong, Arenkiel, Benjamin R., Tolias, Andreas S., Costa-Mattioli, Mauro, and Ray, Russell S.

Abstract

Additional file 3: Figure S3. QQplots for normal distribution testing of residuals from plethysmography analyses from Fig. 8. Plot of the empirical quantiles of the residual distributions vs the theoretical quantiles of gaussian distributions.

Published
2022
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11. Additional file 6 of A CRISPR toolbox for generating intersectional genetic mouse models for functional, molecular, and anatomical circuit mapping

Author

Lusk, Savannah J., McKinney, Andrew, Hunt, Patrick J., Fahey, Paul G., Patel, Jay, Chang, Andersen, Sun, Jenny J., Martinez, Vena K., Zhu, Ping Jun, Egbert, Jeremy R., Allen, Genevera, Jiang, Xiaolong, Arenkiel, Benjamin R., Tolias, Andreas S., Costa-Mattioli, Mauro, and Ray, Russell S.

Abstract

Additional file 6: Figure S6. Residual plots for independence testing of residuals from plethysmography analyses from Fig. 9. Description of data: Plot of residuals vs model predicted values of the dependent variable.

Published
2022
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12. Additional file 2 of A CRISPR toolbox for generating intersectional genetic mouse models for functional, molecular, and anatomical circuit mapping

Author

Lusk, Savannah J., McKinney, Andrew, Hunt, Patrick J., Fahey, Paul G., Patel, Jay, Chang, Andersen, Sun, Jenny J., Martinez, Vena K., Zhu, Ping Jun, Egbert, Jeremy R., Allen, Genevera, Jiang, Xiaolong, Arenkiel, Benjamin R., Tolias, Andreas S., Costa-Mattioli, Mauro, and Ray, Russell S.

Abstract

Additional file 2: Figure S2. Breeding schema for animals used in Figures 7-9. Vector diagrams for animals used in e-physiology and whole animal physiology studies in Figures 7-9. Breeding paradigms indicated with arrows show recombinase and effector molecule source during derivation of used lines.

Published
2022
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13. A CRISPR toolbox for generating intersectional genetic mice for functional, molecular, and anatomical circuit mapping

Author

Lusk, Savannah J., primary, McKinney, Andrew, additional, Hunt, Patrick J., additional, Fahey, Paul G., additional, Patel, Jay, additional, Chang, Andersen, additional, Sun, Jenny J., additional, Martinez, Vena K., additional, Zhu, Ping Jun, additional, Egbert, Jeremy R., additional, Allen, Genevera, additional, Jiang, Xiaolong, additional, Arenkiel, Benjamin R., additional, Tolias, Andreas S., additional, Costa-Mattioli, Mauro, additional, and Ray, Russell S., additional

Published
2021
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14. Phosphatase inhibition by LB-100 enhances BMN-111 stimulation of bone growth

Author

Shuhaibar, Leia C., primary, Kaci, Nabil, additional, Egbert, Jeremy R., additional, Horville, Thibault, additional, Loisay, Léa, additional, Vigone, Giulia, additional, Uliasz, Tracy F., additional, Dambroise, Emilie, additional, Swingle, Mark R., additional, Honkanen, Richard E., additional, Duplan, Martin Biosse, additional, Jaffe, Laurinda A., additional, and Legeai-Mallet, Laurence, additional

Published
2021
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23. Dephosphorylation of the NPR2 guanylyl cyclase contributes to inhibition of bone growth by fibroblast growth factor

Author

Shuhaibar, Leia C, primary, Robinson, Jerid W, additional, Vigone, Giulia, additional, Shuhaibar, Ninna P, additional, Egbert, Jeremy R, additional, Baena, Valentina, additional, Uliasz, Tracy F, additional, Kaback, Deborah, additional, Yee, Siu-Pok, additional, Feil, Robert, additional, Fisher, Melanie C, additional, Dealy, Caroline N, additional, Potter, Lincoln R, additional, and Jaffe, Laurinda A, additional

Published
2017
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25. Author response: Dephosphorylation of the NPR2 guanylyl cyclase contributes to inhibition of bone growth by fibroblast growth factor

Author

Shuhaibar, Leia C, primary, Robinson, Jerid W, additional, Vigone, Giulia, additional, Shuhaibar, Ninna P, additional, Egbert, Jeremy R, additional, Baena, Valentina, additional, Uliasz, Tracy F, additional, Kaback, Deborah, additional, Yee, Siu-Pok, additional, Feil, Robert, additional, Fisher, Melanie C, additional, Dealy, Caroline N, additional, Potter, Lincoln R, additional, and Jaffe, Laurinda A, additional

Published
2017
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26. Dephosphorylation of the NPR2 guanylyl cyclase contributes to inhibition of bone growth by fibroblast growth factor

Author

Shuhaibar, Leia C., primary, Robinson, Jerid W., additional, Shuhaibar, Ninna P., additional, Egbert, Jeremy R., additional, Vigone, Giulia, additional, Baena, Valentina, additional, Kaback, Deborah, additional, Yee, Siu-Pok, additional, Feil, Robert, additional, Fisher, Melanie C., additional, Dealy, Caroline N., additional, Potter, Lincoln R., additional, and Jaffe, Laurinda A., additional

Published
2017
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28. Luteinizing Hormone Causes Phosphorylation and Activation of the cGMP Phosphodiesterase PDE5 in Rat Ovarian Follicles, Contributing, Together with PDE1 Activity, to the Resumption of Meiosis1

Author

Egbert, Jeremy R., primary, Uliasz, Tracy F., additional, Shuhaibar, Leia C., additional, Geerts, Andreas, additional, Wunder, Frank, additional, Kleiman, Robin J., additional, Humphrey, John M., additional, Lampe, Paul D., additional, Artemyev, Nikolai O., additional, Rybalkin, Sergei D., additional, Beavo, Joseph A., additional, Movsesian, Matthew A., additional, and Jaffe, Laurinda A., additional

Published
2016
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31. Dephosphorylation and inactivation of NPR2 guanylyl cyclase in granulosa cells contributes to the LH-induced decrease in cGMP that causes resumption of meiosis in rat oocytes

Author

Egbert, Jeremy R., primary, Shuhaibar, Leia C., additional, Edmund, Aaron B., additional, Van Helden, Dusty A., additional, Robinson, Jerid W., additional, Uliasz, Tracy F., additional, Baena, Valentina, additional, Geerts, Andreas, additional, Wunder, Frank, additional, Potter, Lincoln R., additional, and Jaffe, Laurinda A., additional

Published
2014
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34. Phosphatases modified by LH signaling in ovarian follicles: testing their role in regulating the NPR2 guanylyl cyclase.

Author

Egbert JR, Silbern I, Uliasz TF, Lowther KM, Yee SP, Urlaub H, and Jaffe LA

Abstract

In response to luteinizing hormone, multiple proteins in rat and mouse granulosa cells are rapidly dephosphorylated, but the responsible phosphatases remain to be identified. Because the phosphorylation state of phosphatases can regulate their interaction with substrates, we searched for phosphatases that might function in LH signaling by using quantitative mass spectrometry. We identified all proteins in rat ovarian follicles whose phosphorylation state changed detectably in response to a 30-minute exposure to LH, and within this list, identified protein phosphatases or phosphatase regulatory subunits that showed changes in phosphorylation. Phosphatases in the PPP family were of particular interest because of their requirement for dephosphorylating the natriuretic peptide receptor 2 (NPR2) guanylyl cyclase in the granulosa cells, which triggers oocyte meiotic resumption. Among the PPP family regulatory subunits, PPP1R12A and PPP2R5D showed the largest increases in phosphorylation, with 4-10 fold increases in signal intensity on several sites. Although follicles from mice in which these phosphorylations were prevented by serine-to-alanine mutations in either Ppp1r12a or Ppp2r5d showed normal LH-induced NPR2 dephosphorylation, these regulatory subunits and others could act redundantly to dephosphorylate NPR2. Our identification of phosphatases and other proteins whose phosphorylation state is rapidly modified by LH provides clues about multiple signaling pathways in ovarian follicles., Summary Sentence: Quantitative mass spectrometric analysis of phosphatases whose phosphorylation state is rapidly modified by luteinizing hormone provides clues about how LH signaling dephosphorylates NPR2 as well as a resource for future studies.

Published
2023
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