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

被引:83
作者
Egbert, Jeremy R. [1 ]
Shuhaibar, Leia C. [1 ]
Edmund, Aaron B. [2 ]
Van Helden, Dusty A. [3 ]
Robinson, Jerid W. [3 ]
Uliasz, Tracy F. [1 ]
Baena, Valentina [1 ]
Geerts, Andreas [4 ]
Wunder, Frank [4 ]
Potter, Lincoln R. [2 ,3 ]
Jaffe, Laurinda A. [1 ]
机构
[1] Univ Connecticut, Ctr Hlth, Dept Cell Biol, Farmington, CT 06030 USA
[2] Univ Minnesota, Dept Biochem Mol Biol & Biophys, Minneapolis, MN 55455 USA
[3] Univ Minnesota, Dept Pharmacol, Minneapolis, MN 55455 USA
[4] Bayer Pharma AG, Pharma Res Ctr, D-42096 Wuppertal, Germany
来源
DEVELOPMENT | 2014年 / 141卷 / 18期
基金
美国国家卫生研究院;
关键词
Guanylyl cyclase; Luteinizing hormone; Meiosis; Natriuretic peptide receptor; Ovarian follicle; Phosphorylation; NATRIURETIC-PEPTIDE RECEPTOR; DEPENDENT PROTEIN-KINASE; MOUSE OVARIAN-FOLLICLES; MEIOTIC ARREST; CYCLIC-GMP; PHOSPHORYLATION SITES; SIGNALING MECHANISMS; B/GC-B; ACTIVATION; MATURATION;
D O I
10.1242/dev.112219
中图分类号
Q [生物科学];
学科分类号
07 ; 0710 ; 09 ;
摘要
In mammals, the meiotic cell cycle of oocytes starts during embryogenesis and then pauses. Much later, in preparation for fertilization, oocytes within preovulatory follicles resume meiosis in response to luteinizing hormone (LH). Before LH stimulation, the arrest is maintained by diffusion of cyclic (c)GMP into the oocyte from the surrounding granulosa cells, where it is produced by the guanylyl cyclase natriuretic peptide receptor 2 (NPR2). LH rapidly reduces the production of cGMP, but how this occurs is unknown. Here, using rat follicles, we show that within 10 min, LH signaling causes dephosphorylation and inactivation of NPR2 through a process that requires the activity of phosphoprotein phosphatase (PPP)-family members. The rapid dephosphorylation of NPR2 is accompanied by a rapid phosphorylation of the cGMP phosphodiesterase PDE5, an enzyme whose activity is increased upon phosphorylation. Later, levels of the NPR2 agonist C-type natriuretic peptide decrease in the follicle, and these sequential events contribute to the decrease in cGMP that causes meiosis to resume in the oocyte.
引用
收藏
页码:3594 / 3604
页数:11
相关论文
共 78 条
[1]   Lysophosphatidic acid inhibits C-type natriuretic peptide activation of guanylyl cyclase-B [J].
Abbey, SE ;
Potter, LR .
ENDOCRINOLOGY, 2003, 144 (01) :240-246
[2]   Vasopressin-dependent inhibition of the C-type natriuretic peptide receptor, NPR-B/GC-B, requires elevated intracellular calcium concentrations [J].
Abbey, SE ;
Potter, LR .
JOURNAL OF BIOLOGICAL CHEMISTRY, 2002, 277 (45) :42423-42430
[3]   Differential regulation of NPR-B/GC-B by protein kinase c and calcium [J].
Abbey-Hosch, SE ;
Smirnov, D ;
Potter, LR .
BIOCHEMICAL PHARMACOLOGY, 2005, 70 (05) :686-694
[4]   Epidermal growth factor family members: Endogenous mediators of the ovulatory response [J].
Ashkenazi, H ;
Cao, X ;
Motola, S ;
Popliker, M ;
Conti, M ;
Tsafriri, A .
ENDOCRINOLOGY, 2005, 146 (01) :77-84
[5]   Differential activation of natriuretic peptide receptors modulates cardiomyocyte proliferation during development [J].
Becker, Jason R. ;
Chatterjee, Sneha ;
Robinson, Tamara Y. ;
Bennett, Jeffrey S. ;
Panakova, Daniela ;
Galindo, Cristi L. ;
Zhong, Lin ;
Shin, Jordan T. ;
Coy, Shannon M. ;
Kelly, Amy E. ;
Roden, Dan M. ;
Lim, Chee Chew ;
MacRae, Calum A. .
DEVELOPMENT, 2014, 141 (02) :335-345
[6]   INVOLVEMENT OF CAMP-DEPENDENT PROTEIN-KINASE AND PROTEIN-PHOSPHORYLATION IN REGULATION OF MOUSE OOCYTE MATURATION [J].
BORNSLAEGER, EA ;
MATTEI, P ;
SCHULTZ, RM .
DEVELOPMENTAL BIOLOGY, 1986, 114 (02) :453-462
[7]   AUTORADIOGRAPHIC STUDY OF DISTRIBUTION OF LH(HCG) RECEPTORS IN OVARY OF UNTREATED AND GONADOTROPHIN-PRIMED IMMATURE RATS [J].
BORTOLUSSI, M ;
MARINI, G ;
DALLAGO, A .
CELL AND TISSUE RESEARCH, 1977, 183 (03) :329-342
[8]   Ovulation Involves the Luteinizing Hormone-Dependent Activation of Gq/11 in Granulosa Cells [J].
Breen, Shawn M. ;
Andric, Nebojsa ;
Ping, Tai ;
Xie, Fang ;
Offermans, Stefan ;
Gossen, Jan A. ;
Ascoli, Mario .
MOLECULAR ENDOCRINOLOGY, 2013, 27 (09) :1483-1491
[9]   Phosphorylation of the Eukaryotic Translation Initiation Factor 4E-Transporter (4E-T) by c-Jun N-Terminal Kinase Promotes Stress-Dependent P-Body Assembly [J].
Cargnello, Marie ;
Tcherkezian, Joseph ;
Dorn, Jonas F. ;
Huttlin, Edward L. ;
Maddox, Paul S. ;
Gygi, Steven P. ;
Roux, Philippe P. .
MOLECULAR AND CELLULAR BIOLOGY, 2012, 32 (22) :4572-4584
[10]   Reciprocal antagonism coordinates C-type natriuretic peptide and mitogen-signaling pathways in fibroblasts [J].
Chrisman, TD ;
Garbers, DL .
JOURNAL OF BIOLOGICAL CHEMISTRY, 1999, 274 (07) :4293-4299