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Department of Molecular and Cellular Biology Baylor College of Medicine Houston, Texas 77030
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONDISCUSSIONPROSPECTUSREFERENCES |
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONDISCUSSIONPROSPECTUSREFERENCES |
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). In brief, these
glycoprotein hormones bind ligandspecific, cell surface G
protein-coupled receptors (GPCRs) and activate adenylyl cyclase (AC)
leading to the production of cAMP. cAMP, first discovered as an
intracellular second messenger in 1959 (1), was by 1968 teamed up with
a protein kinase, cAMP-dependent protein kinase (2, 3, 4), establishing a
prototype for many intracellular signaling cascades. This
nucleotide-kinase pair has been universally accepted as a first tier of
reactions by which pituitary hormones control cell functions of
proliferation, differentiation, and cell survival. This model is so
well established that when one hears the word cAMP, protein kinase A
(PKA) or A-kinase immediately springs to mind. More recently, this
cascade has been expanded to include various isoforms of AC (5),
phosphodiesterases (PDEs)(6), and PKAs (7) as well as A-kinase anchor
proteins (AKAPs) (8, 9, 10). In addition, the nuclear transcription factor
cAMP regulatory element-binding protein (CREB) (11, 12, 13) and the
coregulatory molecule CREB-binding proteins (CBP/p300) (14, 15) have
been shown to mediate some of the effects of cAMP (Fig. 1A).
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, A and
B). CREB is not the only transcription factor activated by elevated
levels of intracellular cAMP. In the ovary, for example, stimulatory
protein 1 (Sp1), upstream stimulatory factor (USF), and estrogen
receptor
/ß (ER/ß) are activated (16, 17, 18, 19, 20). Others, such as
early growth response protein 1 (Egr-1), activator protein 1 (AP1)
factors (Fra2, JunD), and C/EBPß are induced and functionally active
based on promoter studies and gene knockout studies (21, 22).
Furthermore, CREB itself is phosphorylated and activated by kinases in
addition to PKA, such as calmodulin kinase IV and RSKB (11, 13, 23).
The coregulator CBP/p300 not only binds CREB but is highly promiscuous
and binds to a plethora of other transcription factors, including
members of the nuclear receptor superfamily (24), nuclear factor
B
(NFB) (25) and others (26, 27). PKA itself has now been shown to
activate as well as inhibit other cell signaling cascades such as the
mitogen-activated protein kinases (MAPKs) in a cell- specific manner
(28, 29, 30, 31). Even the G protein ß
-subunits have functions beyond the
regulation of Gs and the activation of AC (32, 33, 34, 35). Additionally, a
newly identified family of activators of G protein signaling (AGSs) can
stimulate G proteins in the absence of receptor activation (32, 33, 34, 35).
Conversely, regulators of GPCR signaling (RGSs) serve as negative
regulatory GTPase-activating proteins (GAPs) (36, 37, 38) for the specific
G-subunits, thereby turning off G protein activation. In this light,
the GPCRs may be viewed as a type of G guanine nucleotide exchange
factor (G-GEF) that is activated by external stimuli. These are just a few examples of the multiplicity of signaling by GPCR and cAMP. What is the moral of this? There is still more to know about cAMP, the proteins with which it interacts, and the cell functions that it controls. The linear model may give way to a mosaic with multiple intersecting lines of interactions (39). Furthermore, functions previously ascribed solely to cAMP activation of PKA may need to be reevaluated. This includes the transcriptional regulation of many genes.
The purpose of this minireview is to present some of the recent, novel evidence for how hormones and cAMP control such diverse functions as cell proliferation and differentiation in endocrine cells. Specifically, this minireview will focus on the activation of a second cAMP-dependent pathway and show how it may regulate hormone -induced signaling cascades in endocrine cells without the need for activation of PKA. Part of this alternative pathway is comprised of a new class of cAMP-binding proteins, the cAMP-guanine nucleotide exchange factors (cAMP-GEFs) or exchange protein activated by cAMP (Epac). This pathway appears to activate a phosphoinositide- regulated kinase cascade in which phosphoinositol 3-kinase (PI3-kinase) and phosphoinositide-dependent kinase (PDK1) have been identified and shown to mediate the activation of two downstream related kinases, protein kinase B (PKB/Akt) and serum and glucocorticoid induced kinase (Sgk). This cascade is a preeminent survival pathway involved in cell growth and metabolism and likely mediates some of the trophic effects of the gonadotropins. Due to space constraints, other parts of the pathway and other important pathways in endocrine cells are presented only briefly or not at all. This is not intended to show lack of interest or importance.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONDISCUSSIONPROSPECTUSREFERENCES |
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But how might cAMP impact PKB without a need for PKA? To address this
question, it is necessary to review what is known about the activation
of PKB (Fig. 2). It is well established
that PKB is expressed constitutively in all cell types examined.
However, the phosphorylation, activation, and cellular functions of PKB
remain an area of intense investigation (49). PKB is a terminal kinase
in a cascade that controls critical events in cell survival (50). It
has been best characterized as a downstream target of the insulin and
insulin-like growth factor I (IGF-I) pathways (50, 51) although the
downstream effects of these two hormones are not entirely identical
(52). In general, PI3-K generates specific phosphoinositides critical
for the activation of PDK1, which then phosphorylates PKB, p70S6K, Sgk
and other kinases (Fig. 2).
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Several conserved substrates for PKB have been identified. These include glycogen synthase kinase-3 (GSK-3), 6-phosphofructo 2-kinase, and other components (GLUT 1, 3, 4) of the glucose metabolic pathway. Other substrates are the forkhead transcription factor DAF 16, an orphan nuclear receptor DAF 12, and components of the apoptotic pathway such as BAD (50, 53, 58, 59). Members of the forkhead family have been shown to regulate transcription of p27KIP1, providing one link to the cell cycle (60, 61, 62) that may be relevant in endocrine cells as well (63, 64). Other pathways may control the levels of p27KIP1 protein (65). In mammalian cells PKB (via PDK1) appears to be phosphorylated and thereby activated not only in response to IGF-I and insulin but also in response to numerous growth factors (50) and other cell surface proteins, including integrins (66, 67). Importantly, the responses of cells to PKB may be cell cycle and stage specific, thus requiring cautious interpretations of data obtained with cell culture and in vivo experiments (68). These observations are consistent with a central role of PI3-K and PDK1 in controlling cell function and the response of cells to environmental and hormonal cues (53, 69, 70, 71).
Do the glycoprotein hormones and cAMP impact the PKB pathway? The
answer that is emerging from recent studies appears to be, yes—at
least in some cell types (Fig. 2). The pioneering studies of Meinkoth
and Dremier in thyroid cells have been confirmed in the ovary where FSH
leads to the rapid phosphorylation and activation of PKB in granulosa
cells (31). PKB may also be activated by MSH and the Ras pathway in
melanocytes (72). Are these effects of hormones and cAMP restricted to
endocrine cells? The answer to this is not yet known, but is probably
no. What is the mechanism and what are the factors that mediate this
alternate response of cells to glycoprotein hormones and cAMP? As
already mentioned, one pathway may be via the ß-subunits (32, 33, 34, 35).
However, cAMP itself can mediate specific effects.
New doors to the actions of cAMP sprang wide open in 1998 with papers
published by deRooij, Bos, and colleagues (73) and Kawasaki et
al. (74) (Fig. 3). Bos and
colleagues were searching the genomic database for additional genes
with cAMP binding domains. Kawasaki et al. isolated a novel
gene by differential display RT-PCR. Both groups identified genes
encoding proteins that bound cAMP with affinities similar to that of
the regulatory (RI) subunit of type I PKA. In addition, these papers
showed that the novel cAMP binding proteins had regions of homology and
functional activity corresponding to GEFs that exchange high-energy GTP
for GDP to activate Ras-related small GTPases. Hence they were called
cAMP-GEF or Exchange proteins activated by cAMP (Epac). These cAMP-GEFs
were first shown to be an exchange factor for the small GTPase, Rap1
(73, 74). GTP-bound Rap1 activates kinases (Raf-1, B-Raf or c-Raf)
leading into the ERK1/2 or p38MAPK pathways. Subsequent papers have
shown the cAMP-GEFI can activate Rap2 (75, 76) and possibly Ras (77).
The latter is particularly relevant to this review since Ras can
activate yet additional kinase cascades, such as PI3-K/PDK1 pathway.
Another structural feature of the cAMP-GEFs is that they also contain a
DEP (disheveled, Egl-10, Pleckstrin) domain that targets them to the
membrane (76), thus positioning them in proximity to other
membrane-localized enzymes such as PI3-K, PDK1, and PKB (78). cAMP
GEFII has recently been implicated in controlling exocytosis and
therefore may provide one means for the effects of cAMP in enhancing
secretion in specific cell types (79). cAMP-activated GEFs have also
been identified in C. elegans (74, 80) adding credence to
the universality of this pathway in mediating specific actions of
cAMP.
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Since the original studies by Meinkoth, Dremier, and their colleagues, other investigators have shown that cAMP can regulate the phosphorylation of PKB in normal cells. In particular, not only IGF-I but also FSH, forskolin, and 8-bromo-cAMP have been shown to increase rapidly PKB phosphorylation in ovarian granulosa cells (31, 82, 83, 84, 85). In rat granulosa cells, PKB phosphorylation in response to FSH is biphasic with an initial peak at 1–2 h followed by a decline at 6 h and then a secondary increase at 24–48 h. Inhibitors of PI3-K (LY294002 and wortmannin) antagonized FSH (and IGF-I)-induced phosphorylation of PKB whereas the PKA inhibitor, H89, caused a small but consistent increase. Interestingly, phorbol myristate acetate (PMA) failed to stimulate PKB phosphorylation and even blocked FSH (but not IGF-I)-stimulated phosphorylation of PKB. Thus, either C-kinase or the calcium-diacylglycerol-GEF (CalDAG-GEFs) (86) may block the activity of cAMP-GEFs. These observations suggest that FSH and cAMP activate signaling pathways that impact components of the IGF-I pathway, possibly IGF-I itself (85, 87), without the need for PKA activation.
In the ovary, the phosphorylation of PKB by FSH was associated with increased phosphorylation of GSK-3, a known substrate for PKB (31). It is likely that FSH via PKB alters the functional activity of other proteins, especially the inhibition of those involved in the apoptotic process. Alternatively, PKB may exert additional cell survival roles in granulosa cells including the regulation of steroidogenesis. It is of particular interest that FSH via PKB can mimic some actions of IGF-I whereas IGF-I cannot mimic the cAMP-mediated actions of FSH, such as the induction of genes involved in steroidogenesis (aromatase) (88, 89), the LH receptor (90), or the PKB-related kinase, Sgk (31). Conversely, IGF alone induces the expression of specific proteoglycans in the ovary (91, 92). Thus, each pathway brings distinct but also overlapping functions to ensure appropriate progression of proliferation and differentiation in granulosa cells of developing follicles. The distinct but overlapping functions of IGF-I and FSH are supported by phenotypes of IGF-I, IGF-R, IRS-2, and FSH-R knockout mice (93, 94). In each mutant mouse, follicles can grow to the small antral stage but never complete final differentiation.
As already indicated, FSH also induces Sgk (16, 95), a kinase first cloned by Webster et al. (96, 97) as a serum- and glucocorticoid-induced gene (96, 97). More recently, Sgk has been shown to be most closely related to PKB and can be phosphorylated by PDK1 (98). Thus, Sgk like PKB is a downstream target of PI3-K and PDK1. In this regard some functions previously ascribed to PKB may be mediated by one of the three known isoforms of Sgk (Sgk1–3) (99). This seems particularly important in cells where Sgk-1 is selectively expressed, induced, and phosphorylated. Despite the fact that PKB and Sgk-1 are both targets of PKD1, there are some important differences in these two terminal kinases. Sgk-1, but not Sgk3 (99), is inducible in many cell types by a variety of agonists, such as glucocorticoids (96), aldosterone (100, 101), serum (96), hyperosmotic stress (102), transforming growth factor-ß (TGF-ß) (103), and FSH (16). Sgk-2 is selectively expressed in a limited number of tissues examined (99). In contrast, PKB is constitutively expressed in all cells. Whereas PKB has a pleckstrin homology (PH) domain that targets it to the cell membrane, Sgk does not (98). Importantly, Sgk-1 is nuclear in proliferating cells and cytoplasmic in terminally differentiated nondividing cells. These observations on the nuclear to cytoplasmic localization of Sgk-1 during proliferation have been made in mammary epithelial cells (104) as well as granulosa cells (89, 95). Thus, although PKB and Sgk-1 have a common upstream activator and may have some overlapping functions, they appear to respond to different factors and, therefore, likely phosphorylate different substrates and control different functions. In support of these data, human Sgk-1, but not PKB or p70S6K, can substitute for mutated yeast kinases Ypk1and Ypk2 and restore viability to otherwise inviable yeast (54). Despite this critical role of Sgk-1 in yeast, its roles in mammalian cells are not yet clear. Sgk-1 has been shown to phosphorylate and activate an epithelial sodium channel (100) and has recently been proposed to regulate the translocation of the Na+ channels to the plasma membrane in a manner analogous to the translocation of GLUT4 (78) and thereby facilitate ion transport. Perhaps relevant to this is the presence of voltage-activated Na+-channels in ovarian cells (105). Most recently, Sgk-1 but not PKB, has been shown to transactivate a serum-response element in the promoter of the c-fos-luciferase transgene (106). In light of these observations, FSH via cAMP integrates multiple functions in granulosa cells such as the induction of Sgk-1 as well as the activation of PDK1, PKB, and Sgk-1 via a putative cAMP-GEF pathway (31).
And now we come full circle. Curiously, the catalytic subunit of PKA has recently been shown to be phosphorylated and activated by PDK1 in vitro, suggesting that the functional activity of PKA may be regulated by this pathway as well (59, 107). However, the cellular consequences of this PDK1-mediated phosphorylation are less clear. In embryonic stem cells lacking PDK1, PKA activity was normal whereas the activity of PKB was abolished and levels of PKC isoforms were markedly reduced (108, 109). Whether this relation of PDK1 to PKA, PKC, and PKB is true in all cell types is not yet known and could be cell specific. There is evidence that PDK1/PKB enhances the phosphorylation of CREB (78, 110) and that phospho-CREB is essential for cell survival because cotransfection of dominant-negative CREB decreased survival (46, 111, 112). Furthermore, in some situations phosphorylation of CREB on serine 133 is necessary but not sufficient for full activation of CREB (13, 113). Therefore, it is possible that in some cells both PKA-mediated phosphorylation of CREB as well as its phosphorylation by other kinases (PDK1, PKB, or MAPK) is obligatory for full activation. The presence of cAMP-GEFs as well as PKA would ensure that the cAMP signal goes in two directions in the cell.
Other evidence that we have come full circle is the identification of
intracellular proteins that can activate G-protein signaling (AGS
proteins). These factors activate G-proteins in manner not requiring
the GPCR (114). Furthermore, the ß-proteins can activate the
p110 isoform of PI3-K, thereby providing another link between GPCR
and the PI3-K, PDK1 pathway (32, 33, 34, 35). Lastly, there is evidence that
some glycoproteins such as FSH bind to receptors that are related to
growth factor type 1 receptors (115). Therefore, depending on the cell
types and levels of each of these intracellular signaling molecules in
these cells, numerous combinations can occur. It is clear the
PI3-K/PDK1/PKB pathway or the PI3-K/PDK1/Sgk pathway may mediate many
actions previously ascribed to PKA. These observations open exciting
new possibilities for controlling hormone action in endocrine
cells.
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PROSPECTUS |
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TOPABSTRACTINTRODUCTIONDISCUSSIONPROSPECTUSREFERENCES |
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).
These new divergent pathways for cAMP reveal that this nucleotide
should now be considered as a major coordinate integrator of cell
functions by at least three distinct pathways. By activating
cAMP-dependent protein kinases (PKAs), cAMP controls specific steps in
cell proliferation and differentiation by controlling cell
cycle-dependent protein kinase cascades (63, 116) as well as
transcriptional regulation of specific genes (117, 118). By activating
cAMP-GEFs, cAMP impacts small GTPases and their specific kinases (such
as Rap 1/2 and rafs) leading to the activation of other kinases such as
p38 MAPK (73, 74) and transcription factors such as the AP1 factors.
PKA can also impact this Rap-Raf-MAPK kinase pathway, at least in
certain cell types and stages of differentiation (28, 29, 30, 31). In addition,
the cAMP-GEFs via Ras-related GTPases (or other mechanisms) may
activate PI3-K and PDK1 leading to activation of other pathways that
control proliferation (p70S6K), differentiation (PKB, Sgk-1), and cell
survival (31, 43, 45, 84). In these pathways cAMP may act
synergistically with other GPCR-associated molecules such as the
ß-subunits that can also stimulate some forms of the PI3-K pathway
(32, 33, 34, 35). These observations may have clinical relevance in
characterizing polycystic ovarian syndrome (PCOS).
New GEFs (119), GTPases, and kinases in these cascades are likely to emerge. For example, Williams and Alessi and colleagues (108) have recently shown in PDK1-/- embryonic stem cells the phosphorylation of PKB on Ser473 may be mediated by a kinase distinct from PDK1. We need to know more about the function of the endogenous proteins in endocrine cells. We need to know which GEFs are present in specific cells, which GTPases they activate, and which kinases are their targets. Is Ras or another small GTPase activated by FSH or TSH via cAMP-GEF? What Sgk isoforms are expressed in the ovary and other endocrine tissues and what are the specific substrates for Sgk isoforms and PKB in these cells? Since Sgk-1, but not PKB, can reverse the lethal phenotype in yeast, the critical role of Sgk-1 and of the other Sgk isoforms in mammalian cells will no doubt emerge. For example, when granulosa cells cease dividing and become luteal cells, what signaling cascade(s) leads to the phosphorylation of Sgk-1 and PKB? What controls the movement of Sgk-1 from the nucleus to the cytoplasm, and is there an associated switch in activity of substrate specificity for this kinase? These and many other questions need to be answered before the specific roles of cAMP and its new targets of action are fully understood.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Supported, in part by NIH Grant HD-16272.
Received for publication October 20, 2000. Revision received November 29, 2000. Accepted for publication December 4, 2000.
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S. Paternot, J. E. Dumont, and P. P. Roger Differential Utilization of Cyclin D1 and Cyclin D3 in the Distinct Mitogenic Stimulations by Growth Factors and TSH of Human Thyrocytes in Primary Culture Mol. Endocrinol., December 1, 2006; 20(12): 3279 - 3292. [Abstract] [Full Text] [PDF]
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 F. Lang, C. Bohmer, M. Palmada, G. Seebohm, N. Strutz-Seebohm, and V. Vallon (Patho)physiological Significance of the Serum- and Glucocorticoid-Inducible Kinase Isoforms. Physiol Rev, October 1, 2006; 86(4): 1151 - 1178. [Abstract] [Full Text] [PDF]
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S. Lotfi, Z. Li, J. Sun, Y. Zuo, P. P. L. Lam, Y. Kang, M. Rahimi, D. Islam, P. Wang, H. Y. Gaisano, et al. Role of the Exchange Protein Directly Activated by Cyclic Adenosine 5'-Monophosphate (Epac) Pathway in Regulating Proglucagon Gene Expression in Intestinal Endocrine L Cells Endocrinology, August 1, 2006; 147(8): 3727 - 3736. [Abstract] [Full Text] [PDF]
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I. Hernandez-Gonzalez, I. Gonzalez-Robayna, M. Shimada, C. M. Wayne, S. A. Ochsner, L. White, and J. S. Richards Gene Expression Profiles of Cumulus Cell Oocyte Complexes during Ovulation Reveal Cumulus Cells Express Neuronal and Immune-Related Genes: Does this Expand Their Role in the Ovulation Process? Mol. Endocrinol., June 1, 2006; 20(6): 1300 - 1321. [Abstract] [Full Text] [PDF]
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M. Shimada, I. Hernandez-Gonzalez, I. Gonzalez-Robayna, and J. S. Richards 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., June 1, 2006; 20(6): 1352 - 1365. [Abstract] [Full Text] [PDF]
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M. Conti, M. Hsieh, J.-Y. Park, and Y.-Q. Su Role of the Epidermal Growth Factor Network in Ovarian Follicles Mol. Endocrinol., April 1, 2006; 20(4): 715 - 723. [Abstract] [Full Text] [PDF]
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V. K. Yadav and R. Medhamurthy Dynamic Changes in Mitogen-Activated Protein Kinase (MAPK) Activities in the Corpus Luteum of the Bonnet Monkey (Macaca radiata) during Development, Induced Luteolysis, and Simulated Early Pregnancy: A Role for p38 MAPK in the Regulation of Luteal Function Endocrinology, April 1, 2006; 147(4): 2018 - 2027. [Abstract] [Full Text] [PDF]
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B. N Friedrichsen, N. Neubauer, Y. C Lee, V. K Gram, N. Blume, J. S Petersen, J. H Nielsen, and A. Moldrup Stimulation of pancreatic {beta}-cell replication by incretins involves transcriptional induction of cyclin D1 via multiple signalling pathways. J. Endocrinol., March 1, 2006; 188(3): 481 - 492. [Abstract] [Full Text] [PDF]
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 M. Keller-Wood, M. J. Powers, J. A. Gersting, N. Ali, and C. E. Wood Genomic analysis of neuroendocrine development of fetal brain-pituitary-adrenal axis in late gestation Physiol Genomics, February 23, 2006; 24(3): 218 - 224. [Abstract] [Full Text] [PDF]
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V. Sriraman, M. D. Rudd, S. M. Lohmann, S. M. Mulders, and J. S. Richards Cyclic Guanosine 5'-Monophosphate-Dependent Protein Kinase II Is Induced by Luteinizing Hormone and Progesterone Receptor-Dependent Mechanisms in Granulosa Cells and Cumulus Oocyte Complexes of Ovulating Follicles Mol. Endocrinol., February 1, 2006; 20(2): 348 - 361. [Abstract] [Full Text] [PDF]
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C. Garcia-Jimenez, M. A. Zaballos, and P. Santisteban DARPP-32 (Dopamine and 3',5'-Cyclic Adenosine Monophosphate-Regulated Neuronal Phosphoprotein) Is Essential for the Maintenance of Thyroid Differentiation Mol. Endocrinol., December 1, 2005; 19(12): 3060 - 3072. [Abstract] [Full Text] [PDF]
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U. K. Misra and S. V. Pizzo Coordinate Regulation of Forskolin-induced Cellular Proliferation in Macrophages by Protein Kinase A/cAMP-response Element-binding Protein (CREB) and Epac1-Rap1 Signaling: EFFECTS OF SILENCING CREB GENE EXPRESSION ON Akt ACTIVATION J. Biol. Chem., November 18, 2005; 280(46): 38276 - 38289. [Abstract] [Full Text] [PDF]
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F. X. Donadeu and M. Ascoli The Differential Effects of the Gonadotropin Receptors on Aromatase Expression in Primary Cultures of Immature Rat Granulosa Cells Are Highly Dependent on the Density of Receptors Expressed and the Activation of the Inositol Phosphate Cascade Endocrinology, September 1, 2005; 146(9): 3907 - 3916. [Abstract] [Full Text] [PDF]
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Y. Omori, K. Nakamura, S. Yamashita, H. Matsuda, T. Mizutani, K. Miyamoto, and T. Minegishi Effect of Follicle-Stimulating Hormone and Estrogen on the Expression of Betaglycan Messenger Ribonucleic Acid Levels in Cultured Rat Granulosa Cells Endocrinology, August 1, 2005; 146(8): 3379 - 3386. [Abstract] [Full Text] [PDF]
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R. Ain, L. N Canham, and M. J Soares Dexamethasone-induced intrauterine growth restriction impacts the placental prolactin family, insulin-like growth factor-II and the Akt signaling pathway J. Endocrinol., May 1, 2005; 185(2): 253 - 263. [Abstract] [Full Text] [PDF]
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 L.-A. Li and P.-W. Wang PCB126 Induces Differential Changes in Androgen, Cortisol, and Aldosterone Biosynthesis in Human Adrenocortical H295R Cells Toxicol. Sci., May 1, 2005; 85(1): 530 - 540. [Abstract] [Full Text] [PDF]
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 W.-C. Huang, Z. Xie, H. Konaka, J. Sodek, H. E. Zhau, and L. W.K. Chung Human Osteocalcin and Bone Sialoprotein Mediating Osteomimicry of Prostate Cancer Cells: Role of cAMP-Dependent Protein Kinase A Signaling Pathway Cancer Res., March 15, 2005; 65(6): 2303 - 2313. [Abstract] [Full Text] [PDF]
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C. M. Bastida, A. Cremades, M. T. Castells, A. J. Lopez-Contreras, C. Lopez-Garcia, F. Tejada, and R. Penafiel Influence of Ovarian Ornithine Decarboxylase in Folliculogenesis and Luteinization Endocrinology, February 1, 2005; 146(2): 666 - 674. [Abstract] [Full Text] [PDF]
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H. Ashkenazi, X. Cao, S. Motola, M. Popliker, M. Conti, and A. Tsafriri Epidermal Growth Factor Family Members: Endogenous Mediators of the Ovulatory Response Endocrinology, January 1, 2005; 146(1): 77 - 84. [Abstract] [Full Text] [PDF]
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Y. Wu, S. Ghosh, Y. Nishi, T. Yanase, H. Nawata, and Y. Hu The Orphan Nuclear Receptors NURR1 and NGFI-B Modulate Aromatase Gene Expression in Ovarian Granulosa Cells: A Possible Mechanism for Repression of Aromatase Expression upon Luteinizing Hormone Surge Endocrinology, January 1, 2005; 146(1): 237 - 246. [Abstract] [Full Text] [PDF]
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R. Roberts, A. Iatropoulou, D. Ciantar, J. Stark, D. L. Becker, S. Franks, and K. Hardy Follicle-Stimulating Hormone Affects Metaphase I Chromosome Alignment and Increases Aneuploidy in Mouse Oocytes Matured in Vitro Biol Reprod, January 1, 2005; 72(1): 107 - 118. [Abstract] [Full Text] [PDF]
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M. Keiper, M. B. Stope, D. Szatkowski, A. Bohm, K. Tysack, F. vom Dorp, O. Saur, P. A. Oude Weernink, S. Evellin, K. H. Jakobs, et al. Epac- and Ca2+-controlled Activation of Ras and Extracellular Signal-regulated Kinases by Gs-coupled Receptors J. Biol. Chem., November 5, 2004; 279(45): 46497 - 46508. [Abstract] [Full Text] [PDF]
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P. I. Sadate-Ngatchou, D. J. Pouchnik, and M. D. Griswold Follicle-Stimulating Hormone Induced Changes in Gene Expression of Murine Testis Mol. Endocrinol., November 1, 2004; 18(11): 2805 - 2816. [Abstract] [Full Text] [PDF]
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E C Chin and D R E Abayasekara Progesterone secretion by luteinizing human granulosa cells: a possible cAMP-dependent but PKA-independent mechanism involved in its regulation J. Endocrinol., October 1, 2004; 183(1): 51 - 60. [Abstract] [Full Text] [PDF]
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K. M. H. Doyle, D. L. Russell, V. Sriraman, and J. S. Richards Coordinate Transcription of the ADAMTS-1 Gene by Luteinizing Hormone and Progesterone Receptor Mol. Endocrinol., October 1, 2004; 18(10): 2463 - 2478. [Abstract] [Full Text] [PDF]
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 C. P. Thomas, J. R. Campbell, P. J. Wright, and R. F. Husted cAMP-stimulated Na+ transport in H441 distal lung epithelial cells: role of PKA, phosphatidylinositol 3-kinase, and sgk1 Am J Physiol Lung Cell Mol Physiol, October 1, 2004; 287(4): L843 - L851. [Abstract] [Full Text] [PDF]
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A. Agoston, L. Kunz, A. Krieger, and A. Mayerhofer Two Types of Calcium Channels in Human Ovarian Endocrine Cells: Involvement in Steroidogenesis J. Clin. Endocrinol. Metab., September 1, 2004; 89(9): 4503 - 4512. [Abstract] [Full Text] [PDF]
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V. K. Yadav, P. Muraly, and R. Medhamurthy Identification of novel genes regulated by LH in the primate corpus luteum: insight into their regulation during the late luteal phase Mol. Hum. Reprod., September 1, 2004; 10(9): 629 - 639. [Abstract] [Full Text] [PDF]
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C. A. Nechamen, R. M. Thomas, B. D. Cohen, G. Acevedo, P. I. Poulikakos, J. R. Testa, and J. A. Dias Human Follicle-Stimulating Hormone (FSH) Receptor Interacts with the Adaptor Protein APPL1 in HEK 293 Cells: Potential Involvement of the PI3K Pathway in FSH Signaling Biol Reprod, August 1, 2004; 71(2): 629 - 636. [Abstract] [Full Text] [PDF]
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H. Morinaga, T. Yanase, M. Nomura, T. Okabe, K. Goto, N. Harada, and H. Nawata A Benzimidazole Fungicide, Benomyl, and Its Metabolite, Carbendazim, Induce Aromatase Activity in a Human Ovarian Granulose-Like Tumor Cell Line (KGN) Endocrinology, April 1, 2004; 145(4): 1860 - 1869. [Abstract] [Full Text] [PDF]
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 G. Y.-P. Ko, M. L. Ko, and S. E. Dryer Circadian Regulation of cGMP-Gated Channels of Vertebrate Cone Photoreceptors: Role of cAMP and Ras J. Neurosci., February 11, 2004; 24(6): 1296 - 1304. [Abstract] [Full Text] [PDF]
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P. Yang and S. K. Roy Follicle Stimulating Hormone-Induced DNA Synthesis in the Granulosa Cells of Hamster Preantral Follicles Involves Activation of Cyclin-Dependent Kinase-4 Rather Than Cyclin D2 Synthesis Biol Reprod, February 1, 2004; 70(2): 509 - 517. [Abstract] [Full Text] [PDF]
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D. M. Fass, J. E. F. Butler, and R. H. Goodman Deacetylase Activity Is Required for cAMP Activation of a Subset of CREB Target Genes J. Biol. Chem., October 31, 2003; 278(44): 43014 - 43019. [Abstract] [Full Text] [PDF]
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E. C. Lavelle, E. McNeela, M. E. Armstrong, O. Leavy, S. C. Higgins, and K. H. G. Mills Cholera Toxin Promotes the Induction of Regulatory T Cells Specific for Bystander Antigens by Modulating Dendritic Cell Activation J. Immunol., September 1, 2003; 171(5): 2384 - 2392. [Abstract] [Full Text] [PDF]
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R. Rusovici and H. A. LaVoie Expression and Distribution of AP-1 Transcription Factors in the Porcine Ovary Biol Reprod, July 1, 2003; 69(1): 64 - 74. [Abstract] [Full Text] [PDF]
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J. M. Suh, J. H. Song, D. W. Kim, H. Kim, H. K. Chung, J. H. Hwang, J. M. Kim, E. S. Hwang, J. Chung, J.-H. Han, et al. Regulation of the Phosphatidylinositol 3-Kinase, Akt/Protein Kinase B, FRAP/Mammalian Target of Rapamycin, and Ribosomal S6 Kinase 1 Signaling Pathways by Thyroid-stimulating Hormone (TSH) and Stimulating type TSH Receptor Antibodies in the Thyroid Gland J. Biol. Chem., June 6, 2003; 278(24): 21960 - 21971. [Abstract] [Full Text] [PDF]
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J. J. Tremblay and R. S. Viger Transcription Factor GATA-4 Is Activated by Phosphorylation of Serine 261 via the cAMP/Protein Kinase A Signaling Pathway in Gonadal Cells J. Biol. Chem., June 6, 2003; 278(24): 22128 - 22135. [Abstract] [Full Text] [PDF]
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J.-Y. Park, F. Richard, S.-Y. Chun, J.-H. Park, E. Law, K. Horner, S-L C. Jin, and M. Conti Phosphodiesterase Regulation Is Critical for the Differentiation and Pattern of Gene Expression in Granulosa Cells of the Ovarian Follicle Mol. Endocrinol., June 1, 2003; 17(6): 1117 - 1130. [Abstract] [Full Text] [PDF]
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S. K. Roy, J. Wang, and P. Yang Dexamethasone Inhibits Transforming Growth Factor-{beta} Receptor (T{beta}R) Messenger RNA Expression in Hamster Preantral Follicles: Possible Association with NF-YA Biol Reprod, June 1, 2003; 68(6): 2180 - 2188. [Abstract] [Full Text] [PDF]
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C. C. Johansson, M. K. Dahle, S. R. Blomqvist, L. M. Gronning, E. M. Aandahl, S. Enerback, and K. Tasken A Winged Helix Forkhead (FOXD2) Tunes Sensitivity to cAMP in T Lymphocytes through Regulation of cAMP-dependent Protein Kinase RIalpha J. Biol. Chem., May 2, 2003; 278(19): 17573 - 17579. [Abstract] [Full Text] [PDF]
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D. L. Russell, K. M. H. Doyle, I. Gonzales-Robayna, C. Pipaon, and J. S. Richards Egr-1 Induction in Rat Granulosa Cells by Follicle-Stimulating Hormone and Luteinizing Hormone: Combinatorial Regulation By Transcription Factors Cyclic Adenosine 3',5'-Monophosphate Regulatory Element Binding Protein, Serum Response Factor, Sp1, and Early Growth Response Factor-1 Mol. Endocrinol., April 1, 2003; 17(4): 520 - 533. [Abstract] [Full Text] [PDF]
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N. Y. Gevry, E. Lalli, P. Sassone-Corsi, and B. D. Murphy Regulation of Niemann-Pick C1 Gene Expression by the 3'5'-Cyclic Adenosine Monophosphate Pathway in Steroidogenic Cells Mol. Endocrinol., April 1, 2003; 17(4): 704 - 715. [Abstract] [Full Text] [PDF]
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C. Lukas-Croisier, C. Lasala, J. Nicaud, P. Bedecarras, T. R. Kumar, M. Dutertre, M. M. Matzuk, J.-Y. Picard, N. Josso, and R. Rey Follicle-Stimulating Hormone Increases Testicular Anti-Mullerian Hormone (AMH) Production through Sertoli Cell Proliferation and a Nonclassical Cyclic Adenosine 5'-Monophosphate-Mediated Activation of the AMH Gene Mol. Endocrinol., April 1, 2003; 17(4): 550 - 561. [Abstract] [Full Text] [PDF]
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P. A. Orihuela, A. Parada-Bustamante, P. P. Cortes, C. Gatica, and H. B. Croxatto Estrogen Receptor, Cyclic Adenosine Monophosphate, and Protein Kinase A Are Involved in the Nongenomic Pathway by Which Estradiol Accelerates Oviductal Oocyte Transport in Cyclic Rats Biol Reprod, April 1, 2003; 68(4): 1225 - 1231. [Abstract] [Full Text] [PDF]
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O. Dohan, A. De la Vieja, V. Paroder, C. Riedel, M. Artani, M. Reed, C. S. Ginter, and N. Carrasco The Sodium/Iodide Symporter (NIS): Characterization, Regulation, and Medical Significance Endocr. Rev., February 1, 2003; 24(1): 48 - 77. [Abstract] [Full Text] [PDF]
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Y. Wang and W. Ge Involvement of Cyclic Adenosine 3',5'-Monophosphate in the Differential Regulation of Activin {beta}A and {beta}B Expression by Gonadotropin in the Zebrafish Ovarian Follicle Cells Endocrinology, February 1, 2003; 144(2): 491 - 499. [Abstract] [Full Text] [PDF]
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R. M. Rao, Y. Jo, S. Leers-Sucheta, H. S. Bose, W. L. Miller, S. Azhar, and D. M. Stocco Differential Regulation of Steroid Hormone Biosynthesis in R2C and MA-10 Leydig Tumor Cells: Role of SR-B1-Mediated Selective Cholesteryl Ester Transport Biol Reprod, January 1, 2003; 68(1): 114 - 121. [Abstract] [Full Text] [PDF]
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G. W. Pearson and M. H. Cobb Cell Condition-dependent Regulation of ERK5 by cAMP J. Biol. Chem., December 6, 2002; 277(50): 48094 - 48098. [Abstract] [Full Text] [PDF]
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D. J. McLean, P. J. Friel, D. Pouchnik, and M. D. Griswold Oligonucleotide Microarray Analysis of Gene Expression in Follicle-Stimulating Hormone-Treated Rat Sertoli Cells Mol. Endocrinol., December 1, 2002; 16(12): 2780 - 2792. [Abstract] [Full Text] [PDF]
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J. Liu, T. Vanttinen, C. Hyden-Granskog, and R. Voutilainen Regulation of follistatin-related gene (FLRG) expression by protein kinase C and prostaglandin E2 in cultured granulosa-luteal cells Mol. Hum. Reprod., November 1, 2002; 8(11): 992 - 997. [Abstract] [Full Text] [PDF]
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H. Takemori, Y. Katoh, N. Horike, J. Doi, and M. Okamoto ACTH-induced Nucleocytoplasmic Translocation of Salt-inducible Kinase. IMPLICATION IN THE PROTEIN KINASE A-ACTIVATED GENE TRANSCRIPTION IN MOUSE ADRENOCORTICAL TUMOR CELLS J. Biol. Chem., October 25, 2002; 277(44): 42334 - 42343. [Abstract] [Full Text] [PDF]
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M. Paciga, A. J. Watson, G. E. DiMattia, and G. F. Wagner Ovarian Stanniocalcin Is Structurally Unique in Mammals and Its Production and Release Are Regulated through the Luteinizing Hormone Receptor Endocrinology, October 1, 2002; 143(10): 3925 - 3934. [Abstract] [Full Text] [PDF]
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J. J. Tremblay, F. Hamel, and R. S. Viger Protein Kinase A-Dependent Cooperation between GATA and CCAAT/Enhancer-Binding Protein Transcription Factors Regulates Steroidogenic Acute Regulatory Protein Promoter Activity Endocrinology, October 1, 2002; 143(10): 3935 - 3945. [Abstract] [Full Text] [PDF]
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K. Taki, T. Kogai, Y. Kanamoto, J. M. Hershman, and G. A. Brent A Thyroid-Specific Far-Upstream Enhancer in the Human Sodium/Iodide Symporter Gene Requires Pax-8 Binding and Cyclic Adenosine 3',5'-Monophosphate Response Element-Like Sequence Binding Proteins for Full Activity and Is Differentially Regulated in Normal and Thyroid Cancer Cells Mol. Endocrinol., October 1, 2002; 16(10): 2266 - 2282. [Abstract] [Full Text] [PDF]
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A. Bell, A. Gagnon, P. Dods, D. Papineau, M. Tiberi, and A. Sorisky TSH signaling and cell survival in 3T3-L1 preadipocytes Am J Physiol Cell Physiol, October 1, 2002; 283(4): C1056 - C1064. [Abstract] [Full Text] [PDF]
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J. A. Ehses, S. L. Pelech, R. A. Pederson, and C. H. S. McIntosh Glucose-dependent Insulinotropic Polypeptide Activates the Raf-Mek1/2-ERK1/2 Module via a Cyclic AMP/cAMP-dependent Protein Kinase/Rap1-mediated Pathway J. Biol. Chem., September 27, 2002; 277(40): 37088 - 37097. [Abstract] [Full Text] [PDF]
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V. M. Laurich, A. M. Trbovich, F. H. O'Neill, C. P. Houk, P. M. Sluss, A. H. Payne, P. K. Donahoe, and J. Teixeira Mullerian Inhibiting Substance Blocks the Protein Kinase A-Induced Expression of Cytochrome P450 17{alpha}-Hydroxylase/C17-20 Lyase mRNA in a Mouse Leydig Cell Line Independent of cAMP Responsive Element Binding Protein Phosphorylation Endocrinology, September 1, 2002; 143(9): 3351 - 3360. [Abstract] [Full Text] [PDF]
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S. Eimerl and J. Orly Regulation of Steroidogenic Genes by Insulin-Like Growth Factor-1 and Follicle-Stimulating Hormone: Differential Responses of Cytochrome P450 Side-Chain Cleavage, Steroidogenic Acute Regulatory Protein, and 3{beta}-Hydroxysteroid Dehydrogenase/Isomerase in Rat Granulosa Cells Biol Reprod, September 1, 2002; 67(3): 900 - 910. [Abstract] [Full Text] [PDF]
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L. Lou, J. Urbani, F. Ribeiro-Neto, and D. L. Altschuler cAMP Inhibition of Akt Is Mediated by Activated and Phosphorylated Rap1b J. Biol. Chem., August 30, 2002; 277(36): 32799 - 32806. [Abstract] [Full Text] [PDF]
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F. Liu, I. Usui, L. G. Evans, D. A. Austin, P. L. Mellon, J. M. Olefsky, and N. J. G. Webster Involvement of Both Gq/11 and Gs Proteins in Gonadotropin-releasing Hormone Receptor-mediated Signaling in Lbeta T2 Cells J. Biol. Chem., August 23, 2002; 277(35): 32099 - 32108. [Abstract] [Full Text] [PDF]
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T. Kamei, S. R. Jones, B. M. Chapman, K. L. MCGonigle, G. Dai, and M. J. Soares The Phosphatidylinositol 3-Kinase/Akt Signaling Pathway Modulates the Endocrine Differentiation of Trophoblast Cells Mol. Endocrinol., July 1, 2002; 16(7): 1469 - 1481. [Abstract] [Full Text] [PDF]
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D. Kovalovsky, D. Refojo, A. C. Liberman, D. Hochbaum, M. P. Pereda, O. A. Coso, G. K. Stalla, F. Holsboer, and E. Arzt Activation and Induction of NUR77/NURR1 in Corticotrophs by CRH/cAMP: Involvement of Calcium, Protein Kinase A, and MAPK Pathways Mol. Endocrinol., July 1, 2002; 16(7): 1638 - 1651. [Abstract] [Full Text] [PDF]
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J. S. Richards, S. C. Sharma, A. E. Falender, and Y. H. Lo Expression of FKHR, FKHRL1, and AFX Genes in the Rodent Ovary: Evidence for Regulation by IGF-I, Estrogen, and the Gonadotropins Mol. Endocrinol., March 1, 2002; 16(3): 580 - 599. [Abstract] [Full Text] [PDF]
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T. Hirakawa, C. Galet, and M. Ascoli MA-10 Cells Transfected with the Human Lutropin/Choriogonadotropin Receptor (hLHR): A Novel Experimental Paradigm to Study the Functional Properties of the hLHR Endocrinology, March 1, 2002; 143(3): 1026 - 1035. [Abstract] [Full Text] [PDF]
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