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RESEARCH ARTICLE

Active 3′–5′ cyclic nucleotide phosphodiesterases are present in detergent-resistant membranes of mural granulosa cells

Annick Bergeron A , Christine Guillemette A , Marc-André Sirard A and François J. Richard A B
+ Author Affiliations
- Author Affiliations

A Centre de Recherche en Biologie de la Reproduction, Département des Sciences Animales, Faculté des Sciences de l’Agriculture et de l’Alimentation, 2425 rue de l’Agriculture, Pavillon Paul-Comtois, Université Laval, Québec, G1V 0A6, Canada.

B Corresponding author. Email: francois.richard@fsaa.ulaval.ca

Reproduction, Fertility and Development 29(4) 778-790 https://doi.org/10.1071/RD15243
Submitted: 16 June 2015  Accepted: 26 November 2015   Published: 4 January 2016

Abstract

Lipids rafts are specialised membrane microdomains involved in cell signalling that can be isolated as detergent-resistant membranes (DRMs). The second messenger cyclic AMP (cAMP) has a central role in cell signalling in the ovary and its degradation is carried out by the phosphodiesterase (PDE) enzyme family. We hypothesised that PDEs could be functionally present in the lipid rafts of porcine mural granulosa cell membranes. PDE6C, PDE8A and PDE11A were detected by dot blot in the DRMs and the Triton-soluble fraction of the mural granulosa cells membrane and the cytosol. As shown by immunocytochemistry, PDEs showed clear immunostaining in mural granulosa cell membranes and the cytosol. Interestingly, cAMP–PDE activity was 18 times higher in the DRMs than in the Triton-soluble fraction of cell membranes and was 7.7 times higher in the cytosol than in the DRMs. cAMP–PDE activity in mural granulosa cells was mainly contributed by the PDE8 and PDE11 families. This study shows that PDEs from the PDE8 and PDE11 families are present in mural granulosa cells and that the cAMP–PDE activity is mainly contributed by the cytosol. In the cell membrane, the cAMP–PDE activity is mainly contributed by the DRMs. In addition, receptors for prostaglandin E2 and LH, two G-protein-coupled receptors, are present in lipid rafts and absent from the non-raft fraction of the granulosa cell membrane. These results suggest that in these cells, the lipid rafts exist as a cell-signalling platform and PDEs are one of the key enzyme families present in the raft.

Additional keywords: cAMP-PDE activity, DRMs, PDE8, PDE11, raft.


References

Adam, R. M., Yang, W., Di Vizio, D., Mukhopadhyay, N. K., and Steen, H. (2008). Rapid preparation of nuclei-depleted detergent-resistant membrane fractions suitable for proteomics analysis. BMC Cell Biol. 9, 30.
Rapid preparation of nuclei-depleted detergent-resistant membrane fractions suitable for proteomics analysis.Crossref | GoogleScholarGoogle Scholar | 18534013PubMed |

Agarwal, S. R., Yang, P. C., Rice, M., Singer, C. A., Nikolaev, V. O., Lohse, M. J., Clancy, C. E., and Harvey, R. D. (2014). Role of membrane microdomains in compartmentalisation of cAMP signalling. PLoS One 9, e95835.
Role of membrane microdomains in compartmentalisation of cAMP signalling.Crossref | GoogleScholarGoogle Scholar | 24752595PubMed |

Ahmad, F., Shen, W., Vandeput, F., Szabo-Fresnais, N., Krall, J., Degerman, E., Goetz, F., Klussmann, E., Movsesian, M., and Manganiello, V. (2015). Regulation of sarcoplasmic reticulum Ca2+ ATPase 2 (SERCA2) activity by phosphodiesterase 3A (PDE3A) in human myocardium: phosphorylation-dependent interaction of PDE3A1 with SERCA2. J. Biol. Chem. 290, 6763–6776.
Regulation of sarcoplasmic reticulum Ca2+ ATPase 2 (SERCA2) activity by phosphodiesterase 3A (PDE3A) in human myocardium: phosphorylation-dependent interaction of PDE3A1 with SERCA2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXktlGrs7w%3D&md5=8834b79adf98dfef58f4992866d04de0CAS | 25593322PubMed |

Baillie, G. S., Huston, E., Scotland, G., Hodgkin, M., Gall, I., Peden, A. H., MacKenzie, C., Houslay, E. S., Currie, R., Pettitt, T. R., Walmsley, A. R., Wakelam, M. J., Warwicker, J., and Houslay, M. D. (2002). TAPAS-1, a novel microdomain within the unique N-terminal region of the PDE4A1 cAMP-specific phosphodiesterase that allows rapid, Ca2+-triggered membrane association with selectivity for interaction with phosphatidic acid. J. Biol. Chem. 277, 28 298–28 309.
TAPAS-1, a novel microdomain within the unique N-terminal region of the PDE4A1 cAMP-specific phosphodiesterase that allows rapid, Ca2+-triggered membrane association with selectivity for interaction with phosphatidic acid.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlvFKnsrw%3D&md5=8542bd72e14cafbb3ce63f78bf1cd0acCAS |

Bajpai, M., Fiedler, S. E., Huang, Z., Vijayaraghavan, S., Olson, G. E., Livera, G., Conti, M., and Carr, D. W. (2006). AKAP3 selectively binds PDE4A isoforms in bovine spermatozoa. Biol. Reprod. 74, 109–118.
AKAP3 selectively binds PDE4A isoforms in bovine spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtlCjsrbP&md5=eb397ac012955a785b53f2afabbfe978CAS | 16177223PubMed |

Beavo, J. A. (1995). Cyclic nucleotide phosphodiesterases: functional implications of multiple isoforms. Physiol. Rev. 75, 725–748.
| 1:CAS:528:DyaK28XlvVyj&md5=1fa4fc8393708e13ff4912b92e5c0154CAS | 7480160PubMed |

Berger, K., Lindh, R., Wierup, N., Zmuda-Trzebiatowska, E., Lindqvist, A., Manganiello, V. C., and Degerman, E. (2009). Phosphodiesterase 3B is localised in caveolae and smooth ER in mouse hepatocytes and is important in the regulation of glucose and lipid metabolism. PLoS One 4, e4671.
Phosphodiesterase 3B is localised in caveolae and smooth ER in mouse hepatocytes and is important in the regulation of glucose and lipid metabolism.Crossref | GoogleScholarGoogle Scholar | 19262749PubMed |

Brown, K. M., Lee, L. C., Findlay, J. E., Day, J. P., and Baillie, G. S. (2012). Cyclic AMP-specific phosphodiesterase, PDE8A1, is activated by protein kinase A-mediated phosphorylation. FEBS Lett. 586, 1631–1637.
Cyclic AMP-specific phosphodiesterase, PDE8A1, is activated by protein kinase A-mediated phosphorylation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XntFaht7s%3D&md5=9b5509fe18ac4908a3182136be20d42aCAS | 22673573PubMed |

Brown, K. M., Day, J. P., Huston, E., Zimmermann, B., Hampel, K., Christian, F., Romano, D., Terhzaz, S., Lee, L. C., Willis, M. J., Morton, D. B., Beavo, J. A., Shimizu-Albergine, M., Davies, S. A., Kolch, W., Houslay, M. D., and Baillie, G. S. (2013). Phosphodiesterase-8A binds to and regulates Raf-1 kinase. Proc. Natl. Acad. Sci. USA 110, E1533–E1542.
Phosphodiesterase-8A binds to and regulates Raf-1 kinase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXnvVKhsrw%3D&md5=d7fdbb250145e19d98e35910926f562cCAS | 23509299PubMed |

Burke, R. W., Diamondstone, B. I., Velapoldi, R. A., and Menis, O. (1974). Mechanisms of the Liebermann–Burchard and Zak colour reactions for cholesterol. Clin. Chem. 20, 794–781.
| 1:CAS:528:DyaE2cXlsVOqsbg%3D&md5=e865316ca595c757f24146fe8233bd57CAS | 4835232PubMed |

Byrne, A. M., Elliott, C., Hoffmann, R., and Baillie, G. S. (2015). The activity of cAMP–phosphodiesterase 4D7 (PDE4D7) is regulated by protein kinase A-dependent phosphorylation within its unique N-terminus. FEBS Lett. 589, 750–755.
The activity of cAMP–phosphodiesterase 4D7 (PDE4D7) is regulated by protein kinase A-dependent phosphorylation within its unique N-terminus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXisl2rsL0%3D&md5=dabdfb1ad7cf33de61d3d1e41d7b783eCAS | 25680530PubMed |

Carlisle Michel, J. J., Dodge, K. L., Wong, W., Mayer, N. C., Langeberg, L. K., and Scott, J. D. (2004). PKA phosphorylation of PDE4D3 facilitates recruitment of the mAKAP signalling complex. Biochem. J. 381, 587–592.
PKA phosphorylation of PDE4D3 facilitates recruitment of the mAKAP signalling complex.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlvFGqtbY%3D&md5=522ab31e8f063a750641f8951fda0f36CAS | 15182229PubMed |

Conti, M. (2002). Specificity of the cyclic adenosine 3′,5′-monophosphate signal in granulosa cell function. Biol. Reprod. 67, 1653–1661.
Specificity of the cyclic adenosine 3′,5′-monophosphate signal in granulosa cell function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XptVelsrc%3D&md5=0f0b567a5b2d17c382d80d40e9a8e482CAS | 12444038PubMed |

Conti, M., and Beavo, J. (2007). Biochemistry and physiology of cyclic nucleotide phosphodiesterases: essential components in cyclic nucleotide signalling. Annu. Rev. Biochem. 76, 481–511.
Biochemistry and physiology of cyclic nucleotide phosphodiesterases: essential components in cyclic nucleotide signalling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVehtb%2FE&md5=20725f20f028453f949fe12f4f747df1CAS | 17376027PubMed |

Conti, M., Andersen, C. B., Richard, F., Mehats, C., Chun, S. Y., Horner, K., Jin, C., and Tsafriri, A. (2002). Role of cyclic nucleotide signalling in oocyte maturation. Mol. Cell. Endocrinol. 187, 153–159.
Role of cyclic nucleotide signalling in oocyte maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xjt1Sqtro%3D&md5=ea2884cfa93ed6e7b7971e301ecc73aaCAS | 11988323PubMed |

Conti, M., Mika, D., and Richter, W. (2014). Cyclic AMP compartments and signalling specificity: role of cyclic nucleotide phosphodiesterases. J. Gen. Physiol. 143, 29–38.
Cyclic AMP compartments and signalling specificity: role of cyclic nucleotide phosphodiesterases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXjtV2qtLY%3D&md5=663350733b9e623ee6035dcb3821500eCAS | 24378905PubMed |

Day, J. P., Dow, J. A., Houslay, M. D., and Davies, S. A. (2005). Cyclic nucleotide phosphodiesterases in Drosophila melanogaster. Biochem. J. 388, 333–342.
Cyclic nucleotide phosphodiesterases in Drosophila melanogaster.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXktVKntL0%3D&md5=45df1a6f3dd152a1ceb5ea0a8d9dca7fCAS | 15673286PubMed |

Folch, J., Lees, M., and Sloane Stanley, G. H. (1957). A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 226, 497–509.
| 1:STN:280:DyaG2s%2FnsFCjtw%3D%3D&md5=b92f7b65bbb4bd15d7ee84c7307ff606CAS | 13428781PubMed |

Gebska, M. A., Stevenson, B. K., Hemnes, A. R., Bivalacqua, T. J., Haile, A., Hesketh, G. G., Murray, C. I., Zaiman, A. L., Halushka, M. K., Krongkaew, N., Strong, T. D., Cooke, C. A., El-Haddad, H., Tuder, R. M., Berkowitz, D. E., and Champion, H. C. (2011). Phosphodiesterase-5A (PDE5A) is localised to the endothelial caveolae and modulates NOS3 activity. Cardiovasc. Res. 90, 353–363.
Phosphodiesterase-5A (PDE5A) is localised to the endothelial caveolae and modulates NOS3 activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlt1Gltrk%3D&md5=2c0554b9f1c517250603a428325e8506CAS | 21421555PubMed |

Girouard, J., Frenette, G., and Sullivan, R. (2011). Comparative proteome and lipid profiles of bovine epididymosomes collected in the intraluminal compartment of the caput and cauda epididymidis. Int. J. Androl. 34, e475–e486.
Comparative proteome and lipid profiles of bovine epididymosomes collected in the intraluminal compartment of the caput and cauda epididymidis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlOksr%2FJ&md5=2830f75cf1b93400943f571a61bf7aebCAS | 21875428PubMed |

Harder, T., and Simons, K. (1997). Caveolae, DIGs and the dynamics of sphingolipid–cholesterol microdomains. Curr. Opin. Cell Biol. 9, 534–542.
Caveolae, DIGs and the dynamics of sphingolipid–cholesterol microdomains.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXltVWgs70%3D&md5=6259ad2aeba9373d8b516a4e69a91cf5CAS | 9261060PubMed |

Hardman, J. G., Robison, G. A., and Sutherland, E. W. (1971). Cyclic nucleotides. Annu. Rev. Physiol. 33, 311–336.
Cyclic nucleotides.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE3MXhtlOns7o%3D&md5=a4ab33903865993f19d6c18e4335766cCAS | 4157117PubMed |

Head, B. P., Patel, H. H., and Insel, P. A. (2014). Interaction of membrane–lipid rafts with the cytoskeleton: impact on signalling and function: membrane–lipid rafts, mediators of cytoskeletal arrangement and cell signalling. Biochim. Biophys. Acta 1838, 532–545.
Interaction of membrane–lipid rafts with the cytoskeleton: impact on signalling and function: membrane–lipid rafts, mediators of cytoskeletal arrangement and cell signalling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXitVWntr%2FJ&md5=c643d5310458c7128ca238c6758f2903CAS | 23899502PubMed |

Houslay, M. D. (2010). Underpinning compartmentalised cAMP signalling through targeted cAMP breakdown. Trends Biochem. Sci. 35, 91–100.
Underpinning compartmentalised cAMP signalling through targeted cAMP breakdown.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhslWksL8%3D&md5=6805705277876703bf49d92ff8862d04CAS | 19864144PubMed |

Hunter, M. G., Robinson, R. S., Mann, G. E., and Webb, R. (2004). Endocrine and paracrine control of follicular development and ovulation rate in farm species. Anim. Reprod. Sci. 82–83, 461–477.
Endocrine and paracrine control of follicular development and ovulation rate in farm species.Crossref | GoogleScholarGoogle Scholar | 15271473PubMed |

Kotera, J., Sasaki, T., Kobayashi, T., Fujishige, K., Yamashita, Y., and Omori, K. (2004). Subcellular localisation of cyclic nucleotide phosphodiesterase type 10A variants and alteration of the localisation by cAMP-dependent protein kinase-dependent phosphorylation. J. Biol. Chem. 279, 4366–4375.
Subcellular localisation of cyclic nucleotide phosphodiesterase type 10A variants and alteration of the localisation by cAMP-dependent protein kinase-dependent phosphorylation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXps12nsA%3D%3D&md5=e244d11d9f7b94f6a3e76881a022e0c5CAS | 14604994PubMed |

Lingwood, D., and Simons, K. (2010). Lipid rafts as a membrane-organising principle. Science 327, 46–50.
Lipid rafts as a membrane-organising principle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1WksrfJ&md5=0808f590a3648b29b2b60165a8cfcd35CAS | 20044567PubMed |

Macphee, C. H., Reifsnyder, D. H., Moore, T. A., Lerea, K. M., and Beavo, J. A. (1988). Phosphorylation results in activation of a cAMP phosphodiesterase in human platelets. J. Biol. Chem. 263, 10 353–10 358.
| 1:CAS:528:DyaL1cXks1OlsLc%3D&md5=ba2f880aa63cf37eab250f4fa1d2b01fCAS |

Matthiesen, K., and Nielsen, J. (2011). Cyclic AMP control measured in two compartments in HEK293 cells: phosphodiesterase K(M) is more important than phosphodiesterase localisation. PLoS One 6, e24392.
Cyclic AMP control measured in two compartments in HEK293 cells: phosphodiesterase K(M) is more important than phosphodiesterase localisation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1Chsb3I&md5=cdcf41b5b0227f390010635516bd08a1CAS | 21931705PubMed |

Mika, D., Leroy, J., Vandecasteele, G., and Fischmeister, R. (2012). PDEs create local domains of cAMP signalling. J. Mol. Cell. Cardiol. 52, 323–329.
PDEs create local domains of cAMP signalling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtFGhtrs%3D&md5=96f4f179288b80db23c3aadf5b205054CAS | 21888909PubMed |

Nilsson, R., Ahmad, F., Sward, K., Andersson, U., Weston, M., Manganiello, V., and Degerman, E. (2006). Plasma membrane cyclic nucleotide phosphodiesterase 3B (PDE3B) is associated with caveolae in primary adipocytes. Cell. Signal. 18, 1713–1721.
Plasma membrane cyclic nucleotide phosphodiesterase 3B (PDE3B) is associated with caveolae in primary adipocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XosVOgsrY%3D&md5=48a1d0acbcbec671b23e6f88b3f746aeCAS | 16503395PubMed |

Noyama, K., and Maekawa, S. (2003). Localisation of cyclic nucleotide phosphodiesterase 2 in the brain-derived Triton-insoluble low-density fraction (raft). Neurosci. Res. 45, 141–148.
Localisation of cyclic nucleotide phosphodiesterase 2 in the brain-derived Triton-insoluble low-density fraction (raft).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXptFeltA%3D%3D&md5=a1f5f3d1651046962cc7e90669bb9eaaCAS | 12573460PubMed |

Otto, G. P., and Nichols, B. J. (2011). The roles of flotillin microdomains – endocytosis and beyond. J. Cell Sci. 124, 3933–3940.
The roles of flotillin microdomains – endocytosis and beyond.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsV2lu74%3D&md5=ad2d692cd4f561024916b28a3de8a0baCAS | 22194304PubMed |

Patel, H. H., Murray, F., and Insel, P. A. (2008). G-protein-coupled receptor signalling components in membrane raft and caveolae microdomains. In ‘Protein–Protein Interactions as New Drug Targets’. (Eds E. Klussmann and J. Scott.) pp. 167–184. (Springer: Berlin.)

Petersen, T. S., Kristensen, S. G., Jeppesen, J. V., Grondahl, M. L., Wissing, M. L., Macklon, K. T., and Andersen, C. Y. (2015). Distribution and function of 3′,5′-cyclic-AMP phosphodiesterases in the human ovary. Mol. Cell. Endocrinol. 403, 10–20.
Distribution and function of 3′,5′-cyclic-AMP phosphodiesterases in the human ovary.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtVWktLc%3D&md5=72d6fb3d449c622bd8fa34751a8a718cCAS | 25578602PubMed |

Petters, R. M., and Wells, K. D. (1993). Culture of pig embryos. J. Reprod. Fertil. Suppl. 48, 61–73.
| 1:STN:280:DyaK2c7psVCktQ%3D%3D&md5=f4caac82760b4e0a260217849d5e3cacCAS | 8145215PubMed |

Rajendran, L., and Simons, K. (2005). Lipid rafts and membrane dynamics. J. Cell Sci. 118, 1099–1102.
Lipid rafts and membrane dynamics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjs1Chs7s%3D&md5=8d609e52cff51f439199c8d3816a263dCAS | 15764592PubMed |

Richard, F. J., Tsafriri, A., and Conti, M. (2001). Role of phosphodiesterase type 3A in rat oocyte maturation. Biol. Reprod. 65, 1444–1451.
Role of phosphodiesterase type 3A in rat oocyte maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXnvVers7w%3D&md5=c5daf915a8318d9e163922f86845bb62CAS | 11673261PubMed |

Russell, D. L., and Robker, R. L. (2007). Molecular mechanisms of ovulation: co-ordination through the cumulus complex. Hum. Reprod. Update 13, 289–312.
Molecular mechanisms of ovulation: co-ordination through the cumulus complex.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmtlCisbc%3D&md5=1fcd8545d8404250224e58466399fc7aCAS | 17242016PubMed |

Sasseville, M., Cote, N., Guillemette, C., and Richard, F. J. (2006). New insight into the role of phosphodiesterase 3A in porcine oocyte maturation. BMC Dev. Biol. 6, 47.
New insight into the role of phosphodiesterase 3A in porcine oocyte maturation.Crossref | GoogleScholarGoogle Scholar | 17038172PubMed |

Sasseville, M., Cote, N., Vigneault, C., Guillemette, C., and Richard, F. J. (2007). 3′,5′-cyclic adenosine monophosphate-dependent upregulation of phosphodiesterase type 3A in porcine cumulus cells. Endocrinology 148, 1858–1867.
3′,5′-cyclic adenosine monophosphate-dependent upregulation of phosphodiesterase type 3A in porcine cumulus cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjvVOhtb8%3D&md5=543d24b1d4e720f2b1b336a54c31b1d3CAS | 17218408PubMed |

Sasseville, M., Cote, N., Gagnon, M. C., and Richard, F. J. (2008). Upregulation of 3′5′-cyclic guanosine monophosphate-specific phosphodiesterase in the porcine cumulus–oocyte complex affects steroidogenesis during in vitro maturation. Endocrinology 149, 5568–5576.
Upregulation of 3′5′-cyclic guanosine monophosphate-specific phosphodiesterase in the porcine cumulus–oocyte complex affects steroidogenesis during in vitro maturation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlWnsrjO&md5=5f387c058d2626698934c0d194deedebCAS | 18669600PubMed |

Sasseville, M., Albuz, F. K., Cote, N., Guillemette, C., Gilchrist, R. B., and Richard, F. J. (2009a). Characterisation of novel phosphodiesterases in the bovine ovarian follicle. Biol. Reprod. 81, 415–425.
Characterisation of novel phosphodiesterases in the bovine ovarian follicle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXptVaiurg%3D&md5=2a61e850c313c8d6d55743fe17593f4fCAS | 19357367PubMed |

Sasseville, M., Gagnon, M. C., Guillemette, C., Sullivan, R., Gilchrist, R. B., and Richard, F. J. (2009b). Regulation of gap junctions in porcine cumulus–oocyte complexes: contributions of granulosa cell contact, gonadotrophins and lipid rafts. Mol. Endocrinol. 23, 700–710.
Regulation of gap junctions in porcine cumulus–oocyte complexes: contributions of granulosa cell contact, gonadotrophins and lipid rafts.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXlsFCgtrk%3D&md5=64ac7f6d5bde34f76da03b037095ffd7CAS | 19228792PubMed |

Seno, K., Kishimoto, M., Abe, M., Higuchi, Y., Mieda, M., Owada, Y., Yoshiyama, W., Liu, H., and Hayashi, F. (2001). Light- and guanosine 5′-3-O-(thio)triphosphate-sensitive localisation of a G protein and its effector on detergent-resistant membrane rafts in rod photoreceptor outer segments. J. Biol. Chem. 276, 20 813–20 816.
Light- and guanosine 5′-3-O-(thio)triphosphate-sensitive localisation of a G protein and its effector on detergent-resistant membrane rafts in rod photoreceptor outer segments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXksFGlsr8%3D&md5=b87a818e4128bdbf52fe7a24212ec183CAS |

Shimada, M., Hernandez-Gonzalez, I., Gonzalez-Robayna, I., and Richards, J. S. (2006). Paracrine and autocrine regulation of epidermal growth factor-like factors in cumulus–oocyte complexes and granulosa cells: key roles for prostaglandin synthase 2 and progesterone receptor. Mol. Endocrinol. 20, 1352–1365.
Paracrine and autocrine regulation of epidermal growth factor-like factors in cumulus–oocyte complexes and granulosa cells: key roles for prostaglandin synthase 2 and progesterone receptor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XltlSrsb8%3D&md5=e41c09f03d28f3d25d51d0192351e9aeCAS | 16543407PubMed |

Shimizu-Albergine, M., Tsai, L. C., Patrucco, E., and Beavo, J. A. (2012). cAMP-specific phosphodiesterases 8A and 8B, essential regulators of Leydig cell steroidogenesis. Mol. Pharmacol. 81, 556–566.
cAMP-specific phosphodiesterases 8A and 8B, essential regulators of Leydig cell steroidogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XltVagsr4%3D&md5=3348e84708835b4a1b08a61c38744de0CAS | 22232524PubMed |

Shitsukawa, K., Andersen, C. B., Richard, F. J., Horner, A. K., Wiersma, A., van Duin, M., and Conti, M. (2001). Cloning and characterisation of the cyclic guanosine monophosphate-inhibited phosphodiesterase PDE3A expressed in mouse oocyte. Biol. Reprod. 65, 188–196.
Cloning and characterisation of the cyclic guanosine monophosphate-inhibited phosphodiesterase PDE3A expressed in mouse oocyte.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXkslWhtbo%3D&md5=3fae359abc7587d50120e39af867d426CAS | 11420239PubMed |

Smith, S. M., Lei, Y., Liu, J., Cahill, M. E., Hagen, G. M., Barisas, B. G., and Roess, D. A. (2006). Luteinising hormone receptors translocate to plasma membrane microdomains after binding of human chorionic gonadotrophin. Endocrinology 147, 1789–1795.
Luteinising hormone receptors translocate to plasma membrane microdomains after binding of human chorionic gonadotrophin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xjt1Oht7o%3D&md5=e253843b11a004485fd6cbdae438d9d9CAS | 16410308PubMed |

Soderling, S. H., Bayuga, S. J., and Beavo, J. A. (1998). Cloning and characterisation of a cAMP-specific cyclic nucleotide phosphodiesterase. Proc. Natl. Acad. Sci. USA 95, 8991–8996.
Cloning and characterisation of a cAMP-specific cyclic nucleotide phosphodiesterase.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXkvFaltbw%3D&md5=3884bb885290610d0f85c17235f997f0CAS | 9671792PubMed |

Thompson, W. J., Terasaki, W. L., Epstein, P. M., and Strada, S. J. (1979). Assay of cyclic nucleotide phosphodiesterase and resolution of multiple molecular forms of the enzyme. Adv. Cyclic Nucleotide Res. 10, 69–92.
| 1:CAS:528:DyaE1MXktlCmtr0%3D&md5=13c41a77c9f13ad5eedc21c5acca9b5dCAS | 222125PubMed |

Towbin, H., Staehelin, T., and Gordon, J. (1979). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76, 4350–4354.
Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1MXmtVKltLw%3D&md5=9a63ae993f243c65565e8d75c50c8b1aCAS | 388439PubMed |

Tsafriri, A., Chun, S. Y., Zhang, R., Hsueh, A. J., and Conti, M. (1996). Oocyte maturation involves compartmentalisation and opposing changes of cAMP levels in follicular somatic and germ cells: studies using selective phosphodiesterase inhibitors. Dev. Biol. 178, 393–402.
Oocyte maturation involves compartmentalisation and opposing changes of cAMP levels in follicular somatic and germ cells: studies using selective phosphodiesterase inhibitors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XlvVCksr0%3D&md5=553723758b5c3ac23f24d718c700a9caCAS | 8812137PubMed |

Wang, P., Wu, P., Egan, R. W., and Billah, M. M. (2001). Human phosphodiesterase 8A splice variants: cloning, gene organisation and tissue distribution. Gene 280, 183–194.
Human phosphodiesterase 8A splice variants: cloning, gene organisation and tissue distribution.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXovFCru74%3D&md5=5e39d4b483dd0718dceb03f5213c63ffCAS | 11738832PubMed |

Weninger, S., Van Craenenbroeck, K., Cameron, R. T., Vandeput, F., Movsesian, M. A., Baillie, G. S., and Lefebvre, R. A. (2014). Phosphodiesterase 4 interacts with the 5–HT4(b) receptor to regulate cAMP signalling. Cell. Signal. 26, 2573–2582.
Phosphodiesterase 4 interacts with the 5–HT4(b) receptor to regulate cAMP signalling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhsV2ltb3F&md5=5b1724a2e48032729317898482c38dc0CAS | 25101859PubMed |

Yang, G., Dong, Z., Xu, H., Wang, C., Li, H., Li, Z., and Li, F. (2015). Structural study of caveolin-1 intramembrane domain by circular dichroism and nuclear magnetic resonance. Biopolymers 104, 11–20.
Structural study of caveolin-1 intramembrane domain by circular dichroism and nuclear magnetic resonance.Crossref | GoogleScholarGoogle Scholar | 25471446PubMed |