Publications by authors named "Eric W Roubos"

69 Publications

Integration of stress and leptin signaling by CART producing neurons in the rodent midbrain centrally projecting Edinger-Westphal nucleus.

Front Neuroanat 2014 3;8. Epub 2014 Mar 3.

Department of Anatomy, Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen Medical Centre Nijmegen, Netherlands.

Leptin targets the brain to regulate feeding, neuroendocrine function and metabolism. The leptin receptor is present in hypothalamic centers controlling energy metabolism as well as in the centrally projecting Edinger-Westphal nucleus (EWcp), a region implicated in the stress response and in various aspects of stress-related behaviors. We hypothesized that the stress response by cocaine- and amphetamine-regulated transcript (CART)-producing EWcp-neurons would depend on the animal's energy state. To test this hypothesis, we investigated the effects of changes in energy state (mimicked by low, normal and high leptin levels, which were achieved by 24 h fasting, normal chow and leptin injection, respectively) on the response of CART neurons in the EWcp of rats subjected or not to acute restraint stress. Our data show that leptin treatment alone significantly increases CART mRNA expression in the rat EWcp and that in leptin receptor deficient (db/db) mice, the number of CART producing neurons in this nucleus is reduced. This suggests that leptin has a stimulatory effect on the production of CART in the EWcp under non-stressed condition. Under stressed condition, however, leptin blunts stress-induced activation of EWcp neurons and decreases their CART mRNA expression. Interestingly, fasting, does not influence the stress-induced activation of EWcp-neurons, and specifically EWcp-CART neurons are not activated. These results suggest that the stress response by the EWcp depends to some degree on the animal's energy state, a mechanism that may contribute to a better understanding of the complex interplay between obesity and stress.
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http://dx.doi.org/10.3389/fnana.2014.00008DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3939672PMC
March 2014

From frog integument to human skin: dermatological perspectives from frog skin biology.

Biol Rev Camb Philos Soc 2014 Aug 3;89(3):618-55. Epub 2013 Dec 3.

The Dermatology Centre, Salford Royal NHS Foundation Trust, Institute of Inflammation and Repair, University of Manchester, Oxford Road, Manchester, M13 9PT, U.K.

For over a century, frogs have been studied across various scientific fields, including physiology, embryology, neuroscience, (neuro)endocrinology, ecology, genetics, behavioural science, evolution, drug development, and conservation biology. In some cases, frog skin has proven very successful as a research model, for example aiding in the study of ion transport through tight epithelia, where it has served as a model for the vertebrate distal renal tubule and mammalian epithelia. However, it has rarely been considered in comparative studies involving human skin. Yet, despite certain notable adaptations that have enabled frogs to survive in both aquatic and terrestrial environments, frog skin has many features in common with human skin. Here we present a comprehensive overview of frog (and toad) skin ontogeny, anatomy, cytology, neuroendocrinology and immunology, with special attention to its unique adaptations as well as to its similarities with the mammalian integument, including human skin. We hope to provide a valuable reference point and a source of inspiration for both amphibian investigators and mammalian researchers studying the structural and functional properties of the largest organ of the vertebrate body.
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http://dx.doi.org/10.1111/brv.12072DOI Listing
August 2014

Effects of chronic administration of amitriptyline, gabapentin and minocycline on spinal brain-derived neurotrophic factor expression and neuropathic pain behavior in a rat chronic constriction injury model.

Reg Anesth Pain Med 2013 Mar-Apr;38(2):124-30

Department of Anesthesiology, Intensive Care, Emergency Care and Pain Therapy, Ziekenhuis Oost-Limburg, Genk, Belgium.

Background: In animal models of neuropathic pain (NP), promising results have been reported with the administration of minocycline, possibly through inhibition of spinal brain-derived neurotrophic factor (BDNF) expression. No data are available on the effect of amitriptyline and gabapentin on spinal BDNF expression. If the mechanism of action of the latter drugs does not involve brain-derived NP inhibition, further clinical research in BDNF is warranted.

Methods: In this placebo-controlled study, we investigated the effects of amitriptyline (5 mg/kg), gabapentin (50 mg/kg), and minocycline (25 mg/kg) twice a day on NP behavior in a sciatic chronic constriction injury (CCI) rat model. Drug treatment started 7 days after CCI and lasted 14 days. At postoperative day 21, spinal BDNF expression in laminae I and II was quantified using immunocytochemistry.

Results: Sciatic CCI resulted in NP behavior throughout the duration of the experiment in the placebo group. When administered for 2 weeks, minocycline (P ≤ 0.001) and amitriptyline (P ≤ 0.05), but not gabapentin, reduced thermal hyperalgesia. None of these drugs reduced mechanical allodynia. As opposed to amitriptyline and gabapentin, 2 weeks of treatment with minocycline reduced brain-derived, neurotrophic factor immunoreactivity (P ≤ 0.05) in the ipsilateral dorsal horn.

Conclusions: Minocycline and amitriptyline both reduce NP behavior in a sciatic CCI rat model, but only minocycline reduces spinal BDNF, indicating different modes of action of these 2 drugs. The observed actions of minocycline closely fit the clinical needs for the treatment of NP.
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http://dx.doi.org/10.1097/AAP.0b013e31827d611bDOI Listing
August 2013

Pituitary melanotrope cells of Xenopus laevis are of neural ridge origin and do not require induction by the infundibulum.

Gen Comp Endocrinol 2012 Aug 30;178(1):116-22. Epub 2012 Apr 30.

Dept. Cellular Animal Physiology, Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Faculty of Science, Heyendaalseweg 135, Nijmegen, The Netherlands.

Classical studies in amphibians have concluded that the endocrine pituitary and pars intermedia are derived from epithelial buccal epidermis and do not require the infundibulum for their induction. These studies also assumed that the pituitary is not subsequently determined by infundibular induction. Our extirpation, auto-transplantation and immunohistochemical studies with Xenopus laevis were initiated to investigate early presumptive pituitary development. These studies were conducted especially with reference to the pars intermedia melanotrope cell's induction, and its production and release of α-melanophore stimulating hormone (α-MSH) from the precursor protein proopiomelanocortin (POMC). Auto-transplantation studies demonstrated that the pituitary POMC-producing cells are determined at a stage prior to pituitary-infundibular contact. The results of experiments involving the extirpation of the presumptive infundibulum also indicated that the infundibulum is not essential for the differentiation of POMC-producing cells. We also demonstrated that early pituitary development involves adherence to the prechiasmatic area of the diencephalon with the pituitary placode growing in a posterior direction toward the infundibulum where contact occurs at Xenopus stage 39/40. Overall, our studies provide a model for early tissue relations among presumptive pituitary, suprachiasmatic nucleus, pars tuberalis and infundibulum during neurulation and later neural tube stages of development. It is hypothesized that the overlying chiasmatic area suppresses pituitary differentiation.
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http://dx.doi.org/10.1016/j.ygcen.2012.04.018DOI Listing
August 2012

Leptin and the hypothalamo-pituitary-adrenal stress axis.

Gen Comp Endocrinol 2012 May 28;177(1):28-36. Epub 2012 Jan 28.

Department of Cellular Animal Physiology, Faculty of Science, Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, PO Box 9010, 6500 GL Nijmegen, The Netherlands.

Leptin is a 16-kDa protein mainly produced and secreted by white adipose tissue and informing various brain centers via leptin receptor long and short forms about the amount of fat stored in the body. In this way leptin exerts a plethora of regulatory functions especially related to energy intake and metabolism, one of which is controlling the activity of the hypothalamo-pituitary-adrenal (HPA) stress axis. First, this review deals with the basic properties of leptin's structure and signaling at the organ, cell and molecule level, from lower vertebrates to humans but with emphasis on rodents because these have been investigated in most detail. Then, attention is given to the various interactions of adipose leptin with the HPA-axis, at the levels of the hypothalamus (especially the paraventricular nucleus), the anterior lobe of the pituitary gland (action on corticotropes) and the adrenal gland, where it releases corticosteroids needed for adequate stress adaptation. Also, possible local production and autocrine and paracrine actions of leptin at the hypothalamic and pituitary levels of the HPA-axis are being considered. Finally, a schematic model is presented showing the ways peripherally and centrally produced leptin may modulate, via the HPA-axis, stress adaptation in conjunction with the control of energy homeostasis.
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http://dx.doi.org/10.1016/j.ygcen.2012.01.009DOI Listing
May 2012

The role of brain-derived neurotrophic factor in the regulation of cell growth and gene expression in melanotrope cells of Xenopus laevis.

Gen Comp Endocrinol 2012 Jul 10;177(3):315-21. Epub 2012 Jan 10.

Department of Cellular Animal Physiology, Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Nijmegen, The Netherlands.

Brain-derived neurotrophic factor (BDNF) is, despite its name, also found outside the central nervous system (CNS), but the functional significance of this observation is largely unknown. This review concerns the expression of BDNF in the pituitary gland. While the presence of the neurotrophin in the mammalian pituitary gland is well documented its functional significance remains obscure. Studies on the pars intermedia of the pituitary of the amphibian Xenopus laevis have shown that BDNF is produced by the neuroendocrine melanotrope cells, its expression is physiologically regulated, and the melanotrope cells themselves express receptors for the neurotrophin. The neurotrophin has been shown to act as an autocrine factor on the melanotrope to promote cell growth and regulate gene expression. In doing so BDNF supports the physiological function of the cell to produce and release α-melanophore-stimulating hormone for the purpose of adjusting the animal's skin color to that of its background.
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http://dx.doi.org/10.1016/j.ygcen.2012.01.001DOI Listing
July 2012

Peptidergic Edinger-Westphal neurons and the energy-dependent stress response.

Gen Comp Endocrinol 2012 Jul 7;177(3):296-304. Epub 2011 Dec 7.

Department of Cellular Animal Physiology, Faculty of Science, Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, P.O. Box 9010, 6500 GL Nijmegen, The Netherlands.

The continuously changing environment demands for adequate stress responses to maintain the internal dynamic equilibrium of body and mind. A successful stress response requires energy, in an amount matching the severity of the stressor and the type of response ('fight, flight or freeze'). The stress response is generated by the central nervous system, which needs to be informed about both the threatening stressor and the availability of energy. In this review, evidence is considered for a role of the midbrain Edinger-Westphal centrally projecting neuron population (EWcp; synonym: non-preganglionic Edinger-Westphal nucleus) in the energy-dependent stress adaptation response. It deals with studies on the neurochemical organization of the EWcp with particular reference to the neuropeptides urocortin-1 and cocaine- and amphetamine-regulated transcript peptide, on the EWcp responses to different types of stressor (e.g., acute and chronic) and a changed energy state (e.g., fasting and leptin change), and on the sex-specificity of these responses. Finally, a model is presented for the way the EWcp might contribute to the coordination of the energy-dependent stress adaptation response.
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http://dx.doi.org/10.1016/j.ygcen.2011.11.039DOI Listing
July 2012

Chronic stress induces sex-specific alterations in methylation and expression of corticotropin-releasing factor gene in the rat.

PLoS One 2011 23;6(11):e28128. Epub 2011 Nov 23.

Department of Cellular Animal Physiology, Donders Institute for Brain, Cognition and Behaviour, Centre for Neuroscience, Radboud University Nijmegen, Nijmegen, The Netherlands.

Background: Although the higher prevalence of depression in women than in men is well known, the neuronal basis of this sex difference is largely elusive.

Methods: Male and female rats were exposed to chronic variable mild stress (CVMS) after which immediate early gene products, corticotropin-releasing factor (CRF) mRNA and peptide, various epigenetic-associated enzymes and DNA methylation of the Crf gene were determined in the hypothalamic paraventricular nucleus (PVN), oval (BSTov) and fusiform (BSTfu) parts of the bed nucleus of the stria terminalis, and central amygdala (CeA).

Results: CVMS induced site-specific changes in Crf gene methylation in all brain centers studied in female rats and in the male BST and CeA, whereas the histone acetyltransferase, CREB-binding protein was increased in the female BST and the histone-deacetylase-5 decreased in the male CeA. These changes were accompanied by an increased amount of c-Fos in the PVN, BSTfu and CeA in males, and of FosB in the PVN of both sexes and in the male BSTov and BSTfu. In the PVN, CVMS increased CRF mRNA in males and CRF peptide decreased in females.

Conclusions: The data confirm our hypothesis that chronic stress affects gene expression and CRF transcriptional, translational and secretory activities in the PVN, BSTov, BSTfu and CeA, in a brain center-specific and sex-specific manner. Brain region-specific and sex-specific changes in epigenetic activity and neuronal activation may play, too, an important role in the sex specificity of the stress response and the susceptibility to depression.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0028128PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3223222PMC
April 2012

Sex-dependent and differential responses to acute restraint stress of corticotropin-releasing factor-producing neurons in the rat paraventricular nucleus, central amygdala, and bed nucleus of the stria terminalis.

J Neurosci Res 2012 Jan 15;90(1):179-92. Epub 2011 Sep 15.

Department of Cellular Animal Physiology, Donders Institute for Brain, Cognition and Behaviour, Centre for Neuroscience, Radboud University Nijmegen, Nijmegen, The Netherlands.

Male and female rodents respond differently to acute stress. We tested our hypothesis that this sex difference is based on differences in stress sensitivity of forebrain areas, by determining possible effects of a single acute psychogenic stressor (1-hr restraint stress) on neuronal gene expression (c-Fos and FosB immunoreactivities), storage of corticotropin-releasing factor (CRF) immunoreactivity, and CRF production (CRF mRNA in situ hybridization) as well as the expression of genes associated with epigenetic processes (quantitative RT-PCR) in the rat paraventricular nucleus (PVN), the oval and fusiform subdivisions of the bed nucleus of the stria terminalis (BSTov and BSTfu, respectively), and the central amygdala (CeA), in both males and females. Compared with females, male rats responded to the stressor with a stronger rise in corticosterone titer and a stronger increase in neuronal contents of c-Fos, CRF mRNA, and CREB-binding protein mRNA in the PVN. In the BSTov, females but not males showed an increase in c-Fos, whereas the CRF mRNA content was increased in males only. In the BSTfu, males and females showed similar stress-induced increases in c-Fos and FosB, whereas in the CeA, both sexes revealed similar increases in c-Fos and in CRF mRNA. We conclude that male and female rats differ in their reactivity to acute stress with respect to possibly epigenetically mediated (particularly in the PVN) neuronal gene expression and neuropeptide dynamics (PVN and BSTov) and that this difference may contribute to the sex dependence of the animal's physiological and behavioral responses to an acute stressor.
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http://dx.doi.org/10.1002/jnr.22737DOI Listing
January 2012

Sex-dependent and differential responses to acute restraint stress of corticotropin-releasing factor-producing neurons in the rat paraventricular nucleus, central amygdala, and bed nucleus of the stria terminalis.

J Neurosci Res 2012 Jan 15;90(1):179-92. Epub 2011 Sep 15.

Department of Cellular Animal Physiology, Donders Institute for Brain, Cognition and Behaviour, Centre for Neuroscience, Radboud University Nijmegen, Nijmegen, The Netherlands.

Male and female rodents respond differently to acute stress. We tested our hypothesis that this sex difference is based on differences in stress sensitivity of forebrain areas, by determining possible effects of a single acute psychogenic stressor (1-hr restraint stress) on neuronal gene expression (c-Fos and FosB immunoreactivities), storage of corticotropin-releasing factor (CRF) immunoreactivity, and CRF production (CRF mRNA in situ hybridization) as well as the expression of genes associated with epigenetic processes (quantitative RT-PCR) in the rat paraventricular nucleus (PVN), the oval and fusiform subdivisions of the bed nucleus of the stria terminalis (BSTov and BSTfu, respectively), and the central amygdala (CeA), in both males and females. Compared with females, male rats responded to the stressor with a stronger rise in corticosterone titer and a stronger increase in neuronal contents of c-Fos, CRF mRNA, and CREB-binding protein mRNA in the PVN. In the BSTov, females but not males showed an increase in c-Fos, whereas the CRF mRNA content was increased in males only. In the BSTfu, males and females showed similar stress-induced increases in c-Fos and FosB, whereas in the CeA, both sexes revealed similar increases in c-Fos and in CRF mRNA. We conclude that male and female rats differ in their reactivity to acute stress with respect to possibly epigenetically mediated (particularly in the PVN) neuronal gene expression and neuropeptide dynamics (PVN and BSTov) and that this difference may contribute to the sex dependence of the animal's physiological and behavioral responses to an acute stressor.
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http://dx.doi.org/10.1002/jnr.22737DOI Listing
January 2012

The gray area between synapse structure and function-Gray's synapse types I and II revisited.

Synapse 2011 Nov 17;65(11):1222-30. Epub 2011 Jun 17.

Department of Cellular Animal Physiology, Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Nijmegen, The Netherlands.

On the basis of ultrastructural parameters, the concept was formulated that asymmetric Type I and symmetric Type II synapses are excitatory and inhibitory, respectively. This "functional Gray synapses concept" received strong support from the demonstration of the excitatory neurotransmitter glutamate in Type I synapses and of the inhibitory neurotransmitter γ-aminobutyric acid in Type II synapses, and is still frequently used in modern literature. However, morphological and functional evidence has accumulated that the concept is less tenable. Typical features of synapses like shape and size of presynaptic vesicles and synaptic cleft and presence of a postsynaptic density (PsD) do not always fit the postulated (excitatory/inhibitory) function of Gray's synapses. Furthermore, synapse function depends on postsynaptic receptors and associated signal transduction mechanisms rather than on presynaptic morphology and neurotransmitter type. Moreover, the notion that many synapses are difficult to classify as either asymmetric or symmetric has cast doubt on the assumption that the presence of a PsD is a sign of excitatory synaptic transmission. In view of the morphological similarities of the PsD in asymmetric synapses with membrane junctional structures such as the zonula adherens and the desmosome, asymmetric synapses may play a role as links between the postsynaptic and presynaptic membrane, thus ensuring long-term maintenance of interneuronal communication. Symmetric synapses, on the other hand, might be sites of transient communication as takes place during development, learning, memory formation, and pathogenesis of brain disorders. Confirmation of this idea might help to return the functional Gray synapse concept its central place in neuroscience.
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http://dx.doi.org/10.1002/syn.20962DOI Listing
November 2011

Acute ether stress differentially affects corticotropin-releasing factor and urocortin 1 in the Brattleboro rat.

Brain Res 2011 Jun 6;1398:21-9. Epub 2011 May 6.

Department of Cellular Animal Physiology, Donders Institute for Brain, Cognition and Behaviour, Centre for Neuroscience, Radboud University Nijmegen, PO Box 9010, 6500 GL Nijmegen, The Netherlands.

Arginine-vasopressin (AVP), corticotropin-releasing factor (CRF) and urocortin 1 (Ucn1) play a role in the stress response. The CRF-producing paraventricular nucleus of the hypothalamus (PVN), oval bed nucleus of the stria terminalis (BSTov) and central amygdala (CeA), and the Ucn1-expressing non-preganglionic Edinger-Westphal nucleus (npEW) all possess AVP receptors. We hypothesized that AVP is involved in the response of these four brain centers to acute physiological (ether) stress. To test this hypothesis, we studied AVP-deficient Brattleboro (BB) rats using quantitative immunocytochemistry. First, we showed that non-stressed wild-type (WT) and BB rats did not differ from each other in Fos contents, indicating similar (immediate early) gene expression activity, but that in BB rats CRF contents were lower in the PVN and higher in the CeA. Second, we found that stress induced Fos response in the PVN, CeA and npEW with strengths different for each center, but similar for BB and WT rats. Finally, no effects of stress on CRF and Ucn1 contents were seen in the WT rat brain, but in BB rats stress increased CRF contents in the PVN, and the CeA revealed more CRF in stressed BB than in WT rats. On the basis of these results we propose that during acute stress AVP interacts with, especially, the PVN and the CeA, to change their rates of biosynthesis and/or release of CRF.
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http://dx.doi.org/10.1016/j.brainres.2011.04.047DOI Listing
June 2011

ERK-regulated double cortin-like kinase (DCLK)-short phosphorylation and nuclear translocation stimulate POMC gene expression in endocrine melanotrope cells.

Endocrinology 2011 Jun 29;152(6):2321-9. Epub 2011 Mar 29.

Department of Cellular Animal Physiology, Donders Institute for Brain, Cognition, and Behaviour, Radboud University Nijmegen, NL-6525 AJ Nijmegen, The Netherlands.

We tested whether double cortin-like kinase-short (DCLK-short), a microtubule-associated Ser/Thr kinase predominantly expressed in the brain, is downstream of the ERK signaling pathway and is involved in proopiomelanocortin gene (POMC) expression in endocrine pituitary melanotrope cells of Xenopus laevis. Melanotropes form a well-established model to study physiological aspects of neuroendocrine plasticity. The amphibian X. laevis adapts its skin color to the background light intensity by the release of α-MSH from the melanotrope cell. In frogs on a white background, melanotropes are inactive but they are activated during adaptation to a black background. Our results show that melanotrope activation is associated with an increase in DCLK-short mRNA and with phosphorylation of DCLK-short at serine at position 30 (Ser-30). Upon cell activation phosphorylated Ser-30-DCLK-short was translocated from the cytoplasm into the nucleus, and the ERK blocker U0126 inhibited this process. The mutation of Ser-30 to alanine also inhibited the translocation and reduced POMC expression, whereas overexpression stimulated POMC expression. This is the first demonstration of DCLK-short in a native endocrine cell. We conclude that DCLK-short is physiologically regulated at both the level of its gene expression and protein phosphorylation and that the kinase is effectively regulating POMC gene expression upon its ERK-mediated phosphorylation.
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http://dx.doi.org/10.1210/en.2011-0067DOI Listing
June 2011

Gene expression profiling of pituitary melanotrope cells during their physiological activation.

J Cell Physiol 2012 Jan;227(1):288-96

Department of Cellular Animal Physiology, Donders Institute for Brain, Cognition and Behaviour, Centre for Neuroscience, Radboud University Nijmegen, Nijmegen, The Netherlands.

The pituitary melanotrope cells of the amphibian Xenopus laevis are responsible for the production of the pigment-dispersing peptide α-melanophore-stimulating hormone, which allows the animal to adapt its skin color to its environment. During adaptation to a dark background the melanotrope cells undergo remarkable changes characterized by dramatic increases in cell size and secretory activity. In this study we performed microarray mRNA expression profiling to identify genes important to melanotrope activation and growth. We show a strong increase in the expression of the immediate early gene (IEG) c-Fos and of the brain-derived neurotrophic factor gene (BDNF). Furthermore, we demonstrate the involvement of another IEG in the adaptation process, Nur77, and conclude from in vitro experiments that the expression of both c-Fos and Nur77 are partially regulated by the adenylyl cyclase system and calcium ions. In addition, we found a steady up-regulation of Ras-like product during the adaptation process, possibly evoked by BDNF/TrkB signaling. Finally, the gene encoding the 105-kDa heat shock protein HSPh1 was transiently up-regulated in the course of black-background adaptation and a gene product homologous to ferritin (ferritin-like product) was >100-fold up-regulated in fully black-adapted animals. We suggest that these latter two genes are induced in response to cellular stress and that they may be involved in changing the mode of mRNA translation required to meet the increased demand for de novo protein synthesis. Together, our results show that microarray analysis is a valuable approach to identify the genes responsible for generating coordinated responses in physiologically activated cells.
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http://dx.doi.org/10.1002/jcp.22734DOI Listing
January 2012

Together or alone?: foraging strategies in Caenorhabditis elegans.

Biol Rev Camb Philos Soc 2011 Nov 14;86(4):853-62. Epub 2011 Feb 14.

Department of Cellular Animal Physiology, Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, The Netherlands.

A central goal in Life Sciences is to understand how genes encode behaviour and how environmental factors influence the expression of the genes concerned. To reach this goal a combined ecological, molecular biological and physiological approach is required in combination with a suitable model organism. Such an approach allows the elucidation of all parts of the complicated chain of events that lead from induction of gene expression to behaviour, i.e. from environmental stimulus, sensory organs and extracellular and intracellular neuronal signal processing to activation of effector organs. A particularly good model species with which to take this approach is the nematode Caenorhabditis elegans, as it has been described in great detail at the genomic, cellular and behavioural levels. Different strains of C. elegans display prominent behavioural variation in foraging behaviour. Some strains will form social feeding groups when subjected to certain environmental stimuli, while others do not. This variation is due to the existence of just two isoforms of the gene npr-1, namely 215F and 215V. Here, we describe these behavioural variations at the molecular and cellular levels to attempt to determine the environmental inputs that cause aggregation of these small nematodes. As many different stimuli affect aggregation either positively or negatively, aggregation behaviour seems to be displayed when it improves survival chances. However, not much is known about the ecological context in which C. elegans lives. Investigation of the habitats of different strains of C. elegans would help us to understand why and how a specific foraging strategy enhances survival. The relatively well-understood molecular pathways that direct its social feeding behaviour make C. elegans a highly suitable model organism to test ecological and behavioural hypotheses about the mechanisms that differentiate between aggregation and solitary behaviours.
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http://dx.doi.org/10.1111/j.1469-185X.2011.00174.xDOI Listing
November 2011

Plasticity of melanotrope cell regulations in Xenopus laevis.

Eur J Neurosci 2010 Dec;32(12):2082-6

Department of Cellular Animal Physiology, Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, PO Box 9010, Nijmegen, the Netherlands.

This review focuses on the plasticity of the regulation of a particular neuroendocrine transducer cell, the melanotrope cell in the pituitary pars intermedia of the amphibian Xenopus laevis. This cell type is a suitable model to study the relationship between various external regulatory inputs and the secretion of an adaptive endocrine message, in this case the release of α-melanophore-stimulating hormone, which activates skin melanophores to darken when the animal is placed on a dark background. Information about the environmental conditions is processed by various brain centres, in the hypothalamus and elsewhere, that eventually control the activity of the melanotrope cell regarding hormone production and secretion. The review discusses the roles of these hypothalamic and extrahypothalamic nuclei, their neurochemical messengers acting on the melanotrope, and the external stimuli they mediate to control melanotrope cell functioning.
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http://dx.doi.org/10.1111/j.1460-9568.2010.07526.xDOI Listing
December 2010

Brain-derived neurotrophic factor stimulates growth of pituitary melanotrope cells in an autocrine way.

Gen Comp Endocrinol 2011 Jan 1;170(1):156-61. Epub 2010 Oct 1.

Department of Cellular Animal Physiology, Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Faculty of Science, Nijmegen, The Netherlands.

Brain-derived neurotrophic factor (BDNF) is expressed in the mammalian pituitary gland, in both the anterior and intermediate lobes, where its functional significance is unknown. Melanotrope cells in the intermediate pituitary lobe of the amphibian Xenopus laevis also produce BDNF, which co-exists in secretory granules with α-melanophore-stimulating hormone (α-MSH), a peptide that causes pigment dispersion in dermal melanophores during adaptation of the toad to a dark background. Xenopus melanotropes are highly plastic, undergoing very strong growth to support the high biosynthesis and release of α-MSH in black-adapted animals. In this study we have tested our hypothesis that this enhanced growth of the melanotrope is maintained by autocrine release of BDNF. Furthermore, since the extracellular-regulated kinase (ERK) pathway is a major component of BDNF signaling in neuronal plasticity, we investigated its involvement in melanotrope cell growth. For these purposes melanotropes were treated for 3 days in vitro, with either an anti-BDNF serum or a recombinant tropomyosin-receptor kinase B (TrkB) receptor fragment to eliminate released BDNF, or with the ERK inhibitor U0126. We also applied a novel inhibitor of the TrkB receptor, cyclotraxin-B, to test this receptor's involvement in melanotrope cell growth regulation. All treatments markedly reduced melanotrope cell growth. Therefore, we conclude that autocrine release of BDNF and subsequent TrkB-dependent ERK-mediated signaling is important for melanotrope cell growth during its physiologically induced activation.
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http://dx.doi.org/10.1016/j.ygcen.2010.09.020DOI Listing
January 2011

Analysis of the melanotrope cell neuroendocrine interface in two amphibian species, Rana ridibunda and Xenopus laevis: a celebration of 35 years of collaborative research.

Gen Comp Endocrinol 2011 Jan 1;170(1):57-67. Epub 2010 Oct 1.

Department of Cellular Animal Physiology, Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Nijmegen, The Netherlands.

This review gives an overview of the functioning of the hypothalamo-hypophyseal neuroendocrine interface in the pituitary neurointermediate lobe, as it relates to melanotrope cell function in two amphibian species, Rana ridibunda and Xenopus laevis. It primarily but not exclusively concerns the work of two collaborating laboratories, the Laboratory for Molecular and Cellular Neuroendocrinology (University of Rouen, France) and the Department of Cellular Animal Physiology (Radboud University Nijmegen, The Netherlands). In the course of this review it will become apparent that Rana and Xenopus have, for the most part, developed the same or similar strategies to regulate the release of α-melanophore-stimulating hormone (α-MSH). The review concludes by highlighting the molecular and cellular mechanisms utilized by thyrotropin-releasing hormone (TRH) to activate Rana melanotrope cells and the function of autocrine brain-derived neurotrophic factor (BDNF) in the regulation of Xenopus melanotrope cell function.
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http://dx.doi.org/10.1016/j.ygcen.2010.09.022DOI Listing
January 2011

BDNF stimulates Ca2+ oscillation frequency in melanotrope cells of Xenopus laevis: contribution of IP3-receptor-mediated release of intracellular Ca2+ to gene expression.

Gen Comp Endocrinol 2010 Nov 22;169(2):123-9. Epub 2010 Aug 22.

Department of Cellular Animal Physiology, Donders Institute for Brain, Cognition and Behaviour, Radboud University Nijmegen, Nijmegen, The Netherlands.

Pituitary melanotrope cells of the amphibian Xenopus laevis are neuroendocrine cells regulating the animal's skin color adaptation through secretion of α-melanophore-stimulating hormone (α-MSH). To fulfill this function optimally, the melanotrope cell undergoes plastic changes in structure and secretory activity in response to changed background light conditions. Xenopus melanotrope cells display Ca(2+) oscillations that are thought to drive α-MSH secretion and gene expression. They also produce brain-derived neurotrophic factor (BDNF), which stimulates in an autocrine way the biosynthesis of the α-MSH precursor, pro-opiomelanocortin (POMC). We have used this physiological adaptation mechanism as a model to investigate the role of BDNF in the regulation of Ca(2+) kinetics and Ca(2+)-dependent gene expression. By dynamic video imaging of isolated cultured melanotropes we demonstrated that BDNF caused a dose-dependent increase in Ca(2+) oscillation frequency up to 64.7±2.3% of control level. BDNF also induced a transient Ca(2+) peak in Ca(2+)-free medium, which was absent when calcium stores were blocked by thapsigargin and 2-aminoethoxydiphenyl borate, indicating that BDNF stimulates acute release of Ca(2+) from IP(3)-sensitive intracellular Ca(2+) stores. Moreover, we show that thapsigargin inhibits the expression of BDNF transcript IV (by 61.1±28.8%) but does not affect POMC transcript. We conclude that BDNF mobilizes Ca(2+) from IP(3)-sensitive intracellular Ca(2+) stores and propose the possibility that the resulting Ca(2+) oscillations selectively stimulate expression of the BDNF gene.
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http://dx.doi.org/10.1016/j.ygcen.2010.08.010DOI Listing
November 2010

Acute pain increases phosphorylation of DCLK-long in the Edinger-Westphal nucleus but not in the hypothalamic paraventricular nucleus of the rat.

J Pain 2010 Oct 24;11(10):930-40. Epub 2010 Apr 24.

Department of Cellular Animal Physiology, Donders Institute for Brain, Cognition and Behaviour, Center for Neuroscience, Radboud University Nijmegen, Nijmegen, The Netherlands.

Unlabelled: The doublecortin-like kinase (DCLK) gene is crucially involved in neuronal plasticity and microtubule-guided retrograde transport of signaling molecules. We have explored the possibility that DCLK is involved in pain-induced signaling events in adult male Wistar rats. Our results show that both DCLK-short and DCLK-long splice variants are present in the cell body and proximal dendrites of neurons in stress-related nuclei, ie, the paraventricular nucleus of the hypothalamus (PVN) and the non-preganglionic Edinger-Westphal nucleus (npEW) in the rostroventral periaqueductal grey. We found that DCLK-long but not DCLK-short is phosphorylated in its serine/proline-rich domain. Furthermore, we demonstrate that phosphorylation of DCLK-long in the npEW is increased by acute pain, whereas DCLK-long phosphorylation in the PVN remains unaffected. This is the first report revealing that DCLK isoforms in the PVN and npEW occur in the adult mammalian brain and that pain differentially affects DCLK-long-mediated neuronal plasticity in these 2 stress-sensitive brain centers.

Perspective: Pain is a burden for society and the individual, and although the mechanisms underlying pain are relatively well known, its treatment remains difficult and incomplete. Pain stress can lead to diseases like chronic pain and depression. The differential DCLK-phosphorylation in stress-sensitive brain areas is a potential novel therapeutic target in pain research.
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http://dx.doi.org/10.1016/j.jpain.2009.12.017DOI Listing
October 2010

A developmental analysis of periodic albinism in the amphibian Xenopus laevis.

Gen Comp Endocrinol 2010 Sep 21;168(2):302-6. Epub 2010 Feb 21.

Dept. Cellular Animal Physiology, Donders Institute for Brain, Cognition and Behaviour, European Graduate School of Neuroscience, Radboud University Nijmegen, Faculty of Science, Heyendaalseweg 135, 6525 AJ Nijmegen, The Netherlands.

The periodic albino of Xenopus laevis displays a transitory presence of black melanin pigment in the embryo but looses this during tadpole development. This mutation, involving a recessive allele, affects melanogenesis in dermal melanophore pigment cells. It has been suggested that the mutation is intrinsic to the melanophore cell itself or, alternatively, reflects malfunction in the neuroendocrine system that regulates melanophore cell function. This latter system, involving pituitary melanotrope cells which produces alpha-melanophore stimulating hormone (alpha-MSH), is responsible for stimulating the production and dispersion of melanin pigment in dermal melanophores. The purpose of the present study was to determine to which degree the albinism is intrinsic to the melanophore or involves neuroendocrine malfunction. Experiments involved transplantation of presumptive melanophores from wild-type to albino embryos, and vice versa, immunocytochemical analysis of the albino neuroendocrine system and the creation of wild-type/albino parabiotic animals to determine if the neuroendocrine system of the albino can support melanotrope cell function. We show that the albino has a functional neuroendocrine system and conclude that the defect in the albino primarily affects the melanophore cell, possibly rendering it incapable of responding to alpha-MSH. It is also apparent from our results that in later stages of development the cellular environment of the melanotrope cell does become important to its development, but the nature of the critical cellular factors involved remains to be determined.
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http://dx.doi.org/10.1016/j.ygcen.2010.02.017DOI Listing
September 2010

Ultrastructural and neurochemical architecture of the pituitary neural lobe of Xenopus laevis.

Gen Comp Endocrinol 2010 Sep 11;168(2):293-301. Epub 2010 Jan 11.

Department of Cellular Animal Physiology, Donders Institute for Brain, Cognition and Behaviour, EURON, Radboud University Nijmegen, P.O. Box 9010, Nijmegen, The Netherlands.

The melanotrope cell in the amphibian pituitary pars intermedia is a model to study fundamental aspects of neuroendocrine integration. They release alpha-melanophore-stimulating hormone (alphaMSH), under the control of a large number of neurochemical signals derived from various brain centers. In Xenopus laevis, most of these signals are produced in the hypothalamic magnocellular nucleus (Mg) and are probably released from neurohemal axon terminals in the pituitary neural lobe, to stimulate alphaMSH-release, causing skin darkening. The presence in the neural lobe of at least eight stimulatory factors implicated in melanotrope cell control has led us to investigate the ultrastructural architecture of this neurohemal organ, with particular attention to the diversity of neurohemal axon terminals and their neurochemical contents. Using regular electron microscopy, we here distinguish six types of neurohemal axon terminal, on the basis of the size, shape and electron-density of their secretory granule contents. Subsequently, we have identified the neurochemical contents of these terminal types by immuno-electron microscopy and antisera raised against not only the 'classical' neurohormones vasotocin and mesotocin but also brain-derived neurotrophic factor, cocaine- and amphetamine-regulated transcript peptide, corticotropin-releasing factor, metenkephalin, pituitary adenylyl cyclase-activating polypeptide, thyrotropin-releasing hormone and urocortin-1. This has revealed that each terminal type possesses a unique set of neurochemical messengers, containing at least four, but in some cases up to eight messengers. These results reveal the potential of the Mg/neural lobe system to release a wide variety of neurochemical messengers in a partly co-ordinated and partly differential way to control melanotrope cell activity as well as ion and water balance regulatory organs, in response to various, continuously changing, environmental stimuli.
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http://dx.doi.org/10.1016/j.ygcen.2010.01.008DOI Listing
September 2010

Restraint stress alters the secretory activity of neurons co-expressing urocortin-1, cocaine- and amphetamine-regulated transcript peptide and nesfatin-1 in the mouse Edinger-Westphal nucleus.

Brain Res 2010 Mar 4;1317:92-9. Epub 2010 Jan 4.

Department of Animal Biology, University of Modena and Reggio Emilia, Via Campi, 213/D, 41100 Modena, Italy.

Central stress regulatory pathways utilize various neuropeptides, such as urocortin-1 (Ucn1) and cocaine- and amphetamine-regulated transcript peptide (CART). Ucn1 is most abundantly expressed in the non-preganglionic Edinger-Westphal nucleus (npEW). In addition to Ucn1, CART and nesfatin-1 are highly expressed in neurons of the npEW, but the way these three neuropeptides act together in response to acute stress is not known. We hypothesized that Ucn1, CART and nesfatin-1 are colocalized in npEW neurons and that these neurons are recruited by acute stress. Using quantitative immunocytochemistry and the reverse transcriptase polymerase chain reaction (RT-PCR), we support this hypothesis, by showing in B6C3F1/Crl mice that Ucn1, CART and nesfatin-1 occur in the same neurons of the npEW nucleus. More specifically, Ucn1 and CART revealed a complete colocalization in the same perikarya, while 90% of these neurons are also nesfatin-1-immunoreactive. Furthermore, acute (restraint) stress stimulates the general secretory activity of these npEW neurons (increased presence of Fos) and the production of Ucn1, CART and nesfatin-1: Ucn1, CART and nesfatin-1(NUCB2) mRNAs have been increased compared to controls by x1.8, x2.0 and x2.6, respectively (p<0.01). We conclude that Ucn1, CART and nesfatin-1/NUCB2 are specifically involved in the response of npEW neurons to acute stress in the mouse.
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http://dx.doi.org/10.1016/j.brainres.2009.12.053DOI Listing
March 2010

About a snail, a toad, and rodents: animal models for adaptation research.

Front Endocrinol (Lausanne) 2010 20;1. Epub 2010 Oct 20.

Department of Cellular Animal Physiology, Faculty of Science, Donders Institute for Brain, Cognition and Behaviour, Centre for Neuroscience, Radboud University Nijmegen Nijmegen, Netherlands.

Neural adaptation mechanisms have many similarities throughout the animal kingdom, enabling to study fundamentals of human adaptation in selected animal models with experimental approaches that are impossible to apply in man. This will be illustrated by reviewing research on three of such animal models, viz. (1) the egg-laying behavior of a snail, Lymnaea stagnalis: how one neuron type controls behavior, (2) adaptation to the ambient light condition by a toad, Xenopus laevis: how a neuroendocrine cell integrates complex external and neural inputs, and (3) stress, feeding, and depression in rodents: how a neuronal network co-ordinates different but related complex behaviors. Special attention is being paid to the actions of neurochemical messengers, such as neuropeptide Y, urocortin 1, and brain-derived neurotrophic factor. While awaiting new technological developments to study the living human brain at the cellular and molecular levels, continuing progress in the insight in the functioning of human adaptation mechanisms may be expected from neuroendocrine research using invertebrate and vertebrate animal models.
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http://dx.doi.org/10.3389/fendo.2010.00004DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3355873PMC
August 2012

Sex differences in urocortin 1 dynamics in the non-preganglionic Edinger-Westphal nucleus of the rat.

Neurosci Res 2010 Jan 13;66(1):117-23. Epub 2009 Oct 13.

Department of Cellular Animal Physiology, Faculty of Science, EURON, Radboud University Nijmegen, Heyendaalseweg 135, 6525 AJ Nijmegen, The Netherlands.

Women have higher vulnerability to stress and stress-induced diseases than men. Estrogen may be involved in the control of sex-dependent stress adaptation via estrogen receptors alpha and beta (ERalpha/beta). Urocortin 1 (Ucn1) in the npEW plays an important role in stress adaptation. We hypothesize that the activity of npEW-Ucn1 neurons differs between sexes and is related to estrogen signalling. We here indicate by immunocytochemistry the absence of ERalpha and the presence of ERbeta in the npEW-Ucn1 neurons. Q-RT-PCR of the npEW confirmed this notion, demonstrating that in male rats ERbeta mRNA was almost 5 times higher than in females in di-estrus. Furthermore, Ucn1 mRNA in males was nearly 10 times and 1.6 times higher than in females in di- and pro-estrus, respectively, indicating a sex-dependent difference in Ucn1 biosynthetic activity. Since, at the same time, immunocytochemistry revealed that the amount of Ucn1 peptide stored in the cell bodies of the npEW-Ucn1 neurons did not differ between males and females, as judged on the basis of the number and immunosignal density of these neurons, we propose that the rate of axonal Ucn1 transport and, possibly, the strength of Ucn1 secretion, are dependent on sex to the same degree as is Ucn1 biosynthesis.
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http://dx.doi.org/10.1016/j.neures.2009.10.003DOI Listing
January 2010

Sex-specific expression of BDNF and CART in the midbrain non-preganglionic Edinger-Westphal nucleus in the rat.

Peptides 2009 Dec 13;30(12):2268-74. Epub 2009 Sep 13.

Department of Cellular Animal Physiology, Donders Institute for Brain, Cognition and Behaviour, EURON, Radboud University Nijmegen, PO Box 9010, 6500 GL Nijmegen, The Netherlands.

In mammals, females generally appear more vulnerable to stressors than males. The non-preganglionic Edinger-Westphal nucleus (npEW) has been implicated in regulation of the stress response. Brain-derived neurotrophic factor (BDNF) and cocaine- and amphetamine-related transcript peptide (CART) are sex-specifically involved in the stress response too, and are present in the human and rat npEW. We hypothesized that male and female rats would differ in the expression of BDNF and CART in the npEW. Using immunocytochemistry and in situ hybridization we found that BDNF, CART and the estrogen receptor beta (ERbeta) are colocalized in the npEW. Q-RT-PCR showed no differences in CART and BDNF coding mRNAs between males and females, but quantitative immunocytochemistry revealed a 16% lower number of BDNF-immunoreactive neurons, and 19% lower CART-immunoreactivity in females compared to males. Considering the fact that Ucn1, CART and BDNF are co-expressed in the npEW with ERbeta and their protein expression differs between males and females, we propose that the functioning of the npEW may contribute to the sex differences that exist in stress sensitivity.
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http://dx.doi.org/10.1016/j.peptides.2009.09.009DOI Listing
December 2009

Effects of maternal separation on dynamics of urocortin 1 and brain-derived neurotrophic factor in the rat non-preganglionic Edinger-Westphal nucleus.

Int J Dev Neurosci 2009 Aug 19;27(5):439-51. Epub 2009 May 19.

Department of Cellular Animal Physiology, Donders Centre for Neuroscience, EURON, Radboud University Nijmegen, Nijmegen, The Netherlands.

Although mood disorders are frequently genetically determined and to some degree gender-dependent, the concept of early life 'programming', implying a relation between perinatal environmental events and adult mood disorders, has recently gained considerable attention. In particular, maternal separation (MS) markedly affects various stress-sensitive brain centers. Therefore, MS is considered as a suitable experimental paradigm to study how early life events affect brain plasticity and, hence, cause psychopathologies like major depression. In adult mammals, the classical hypothalamo-pituitary-adrenal (HPA-) axis and the urocortin 1 (Ucn1)-containing non-preganglionic Edinger-Westphal nucleus (npEW) respond in opposite ways to chronic stressors. This raises the hypothesis that MS, which is known to increase vulnerability for adult mood disorders via the dysregulation of the HPA-axis, will affect npEW dynamics as well. We have tested this hypothesis and, moreover, studied a possible role of brain-derived neurotrophic factor (BDNF) in such npEW plasticity. By triple immunocytochemistry we show that BDNF and Ucn1 coexist in rat npEW-neurons that are c-Fos-positive upon acute stress. Quantitative immunocytochemistry revealed that MS increases the contents of Ucn1 and BDNF in these cells. Furthermore, in males and females, the c-Fos response of npEW-Ucn1 neurons upon restraint stress was blunted in animals with MS history, a phenomenon that was concomitant with dampening of the HPA corticosterone response in females but not in males. Based on these data we suggest that the BDNF-containing npEW-Ucn1 system might be affected by MS in a sex-specific manner. This supports the idea that the npEW would play a role in the appearance of sex differences in the pathogenesis of stress-induced mood disorders.
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http://dx.doi.org/10.1016/j.ijdevneu.2009.05.006DOI Listing
August 2009

Neurochemistry and plasticity of the median eminence and neural pituitary lobe in relation to background adaptation of Xenopus laevis.

Ann N Y Acad Sci 2009 Apr;1163:524-7

Department of Cellular Animal Physiology, Donders Institute for Brain, Cognition and Behaviour, European Graduate School of Neuroscience, Radboud University Nijmegen, Nijmegen, The Netherlands.

Using immunocytochemistry and morphometry we have supported our hypothesis that magnocellular neurons in the preoptic area of the brain of Xenopus laevis release identical sets of neuropeptides containing not only the previously identified vasotocin, mesotocin, corticotropin-releasing factor, thyrotropin-releasing hormone, brain-derived neurotrophic factor, urocortin 1, and pituitary adenylate cyclase-activating peptide but also mesotocin and met-enkephalin from both neurohemal areas in the pituitary neural lobe and in the median eminence. We also show that the external zone of the median eminence is plastic, depending in size on the state of background illumination.
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http://dx.doi.org/10.1111/j.1749-6632.2008.03666.xDOI Listing
April 2009

Dynamics of glucocorticoid and mineralocorticoid receptors in the Xenopus laevis pituitary pars intermedia.

Ann N Y Acad Sci 2009 Apr;1163:292-5

Department of Cellular Animal Physiology, Donders Centre for Neuroscience, European Graduate School of Neuroscience, University of Nijmegen, Nijmegen, The Netherlands.

We showed the presence of glucocorticoid (GR) and mineralocorticoid (MR) receptors in different populations of Xenopus laevis melanotrope cells and revealed their downregulation (MR) and upregulation (GR) during dark background adaptation. Corticosterone did not affect short-term intracellular calcium dynamics and alpha-melanophore-stimulating hormone secretion, suggesting a role for GR and MR in long-term processes in the melanotropes.
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http://dx.doi.org/10.1111/j.1749-6632.2008.03647.xDOI Listing
April 2009

Trends in comparative endocrinology and neurobiology. Preface.

Ann N Y Acad Sci 2009 Apr;1163:xiii-xiv

University of London, London, United Kingdom.

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http://dx.doi.org/10.1111/j.1749-6632.2009.04868.xDOI Listing
April 2009
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