Testosterone-driven seasonal regulation of vasopressin and galanin in the bed nucleus of the stria terminalis of the Djungarian hamster (Phodopus sungorus)

Neuroscience

Volumn 157, Issue 1, 2008, Pages 174-187

  Rasri, K ^b   Mason, P ^a   Govitrapong, P ^b,c   Pevet, P ^a   Klosen, P ^a  

^a Hopitaux Universitaires de Strasbourg   (France)

^b MAHIDOL UNIVERSITY   (Thailand)

^c MAHIDOL UNIVERSITY   (Thailand)

Author keywords

neuropeptides; photoperiod; plasticity; sex steroids

Indexed keywords

GALANIN; MESSENGER RNA; NEUROPEPTIDE; TESTOSTERONE; VASOPRESSIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN NERVE CELL; BRAIN REGION; HAMSTER; HYPOTHALAMUS; IMMUNOREACTIVITY; MALE; NERVE ENDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REPRODUCTION; STRIA TERMINALIS;

ANIMALS; CELL COUNT; CRICETINAE; GALANIN; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; MELATONIN; PHODOPUS; PHOTOPERIOD; RECEPTORS, ANDROGEN; RNA, MESSENGER; SEASONS; SEPTAL NUCLEI; TESTOSTERONE; VASOPRESSINS;

EID: 54549085356     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2008.08.058     Document Type: Article

References (58)

1. Amaya F., Tanaka M., Tamada Y., Tanaka Y., Nilaver G., and Ibata Y. The influence of salt loading on vasopressin gene expression in magno- and parvocellular hypothalamic neurons: an immunocytochemical and in situ hybridization analysis. Neuroscience 89 (1999) 515-523
2. Arendt T., Stieler J., Strijkstra A.M., Hut R.A., Rüdiger J., Van der Zee E.A., Harkany T., Holzer M., and Härtig W. Reversible paired helical filament-like phosphorylation of tau is an adaptive process associated with neuronal plasticity in hibernating animals. J Neurosci 23 (2003) 6972-6981
3. Auger C.J., and De Vries G.J. Progestin receptor immunoreactivity within steroid-responsive vasopressin-immunoreactive cells in the male and female rat brain. J Neuroendocrinol 14 (2002) 561-567
4. Axelson J.F., and van Leeuwen F.W. Differential localization of estrogen receptors in various vasopressin synthesizing nuclei of the rat brain. J Neuroendocrinol 2 (1990) 209-216
5. Bittman E.L., Jetton A.E., Villalba C., and De Vries G.J. Effects of photoperiod and androgen on pituitary function and neuropeptide staining in Siberian hamsters. Am J Physiol 271 (1996) R64-R72
6. Bittman E.L., Ehrlich D.A., Ogdahl J.L., and Jetton A.E. Photoperiod and testosterone regulate androgen receptor immunostaining in the Siberian hamster brain. Biol Reprod 69 (2003) 876-884
7. Buijs R.M., Swaab D.F., Dogterom J., and Van Leeuwen F.W. Seasonal variation in vasopressin innervation in the brain of the European hamster (Cricetus cricetus). Brain Res 371 (1986) 193-196
8. Carter D.A., and Murphy D. Regulation of vasopressin (VP) gene expression in the bed nucleus of the stria terminalis: Gonadal steroid-dependent changes in VP mRNA accumulation are associated with alterations in mRNA poly (A) tail length but are independent of the rate of VP gene transcription. J Neuroendocrinol 5 (1993) 509-515
9. Chiba T., and Murata Y. Afferent and efferent connections of the medial preoptic area in the rat: a WGA-HRP study. Brain Res Bull 14 (1985) 261-272
10. Cortes R., Ceccatelli S., Schalling M., and Hökfelt T. Differential effects of intracerebroventricular colchicine administration on the expression of mRNAs for neuropeptides and neurotransmitter enzymes, with special emphasis on galanin: an in situ hybridization study. Synapse 6 (1990) 369-391
11. de Bree F.M., and Burbach J.P.H. Structure-function relationships of the vasopressin prohormone domains. Cell Mol Neurobiol 15 (1998) 173-191
12. De Vries G.J., Best W., and Sluiter A.A. The influence of androgens on the development of a sex difference in the vasopressinergic innervation of the rat lateral septum. Dev Brain Res 8 (1983) 377-380
13. De Vries G.J., Buijs R.M., and Sluiter A.A. Gonadal hormone actions on the morphology of the vasopressinergic innervation of the adult rat brain. Brain Res 298 (1984) 141-145
14. De Vries G.J., Buijs R.M., Van Leeuwen F.W., Caffe A.R., and Swaab D.F. The vasopressinergic innervation of the brain in normal and castrated rats. J Comp Neurol 233 (1985) 236-254
15. De Vries G.J., Duetz W., Buijs R.M., Van Heerikhuize J., and Vreeburg J.T.M. Effects of androgens and estrogens on the vasopressin and oxytocin innervation of the adult rat brain. Brain Res 399 (1986) 296-302
16. De Vries G.J., Wang Z., Bullock N.A., and Numan S. Sex differences in the effects of testosterone and its metabolites on vasopressin messenger RNA levels in the bed nucleus of the stria terminalis of rats. J Neurosci 14 (1994) 1789-1794
17. Fliers E., De Vries G.J., and Swaab D.F. Changes with aging in the vasopressin and oxytocin innervation of the rat brain. Brain Res 348 (1985) 1-8
18. Goodson J.L., and Bass A.H. Social behaviour functions and related anatomical characteristics of vasotocin/vasopressin systems in vertebrates. Brain Res Rev 35 (2001) 246-265
19. Goudsmit E., Fliers E., and Swaab D.F. Testosterone supplementation restores vasopressin innervation in the senescent rat brain. Brain Res 473 (1988) 306-313
20. Han T.M., and De Vries G.J. Neurogenesis of galanin cells in the bed nucleus of the stria terminalis and centromedial amygdala in rats: A model for sexual differentiation of neuronal phenotype. J Neurobiol 38 (1999) 491-498
21. Hermes M.L., Buijs R.M., Masson-Pévet M., van der Woude T.P., Pévet P., Brenklé R., and Kirsch R. Central vasopressin infusion prevents hibernation in the European hamster (Cricetus cricetus). Proc Natl Acad Sci U S A 86 (1989) 6408-6411
22. Hermes M.L.H.J., Buijs R.M., Masson-Pévet M., and Pévet P. Seasonal changes in vasopressin in the brain of the garden dormouse (Eliomys quercinus L.). J Comp Neurol 363 (1990) 15-27
23. Hermes M.L., Kalsbeek A., Kirsch R., Buijs R.M., and Pévet P. Induction of arousal in hibernating European hamsters (Cricetus cricetus L.) by vasopressin infusion in the lateral septum. Brain Res 631 (1993) 313-316
24. Howard G., Peng L., and Hyde J.F. An estrogen receptor binding site within the human galanin gene. Endocrinology 138 (1997) 4649-4656
25. Klein S., Jurkevich A., and Grossmann R. Sexually dimorphic immunoreactivity of galanin and colocalization with arginine vasotocin in the chicken brain (Gallus gallus domesticus). J Comp Neurol 499 (2006) 828-839
26. Klosen P., Maessen X., and van den Bosch de Aguilar P. PEG embedding for immunocytochemistry: application to the analysis of immunoreactivity loss during histological processing. J Histochem Cytochem 41 (1993) 455-463
27. Laflamme N., Nappi R.E., Drolet G., Labrie C., and Rivest S. Expression and neuropeptidergic characterization of estrogen receptors (ERα and ERβ) throughout the rat brain: Anatomical evidence of distinct roles of each subtype. J Neurobiol 36 (1998) 357-378
28. Lakhdar-Ghazal N., Dubois-Dauphin M., Hermes M.L.H.J., Buijs R.M., Bengelloun W.A., and Pévet P. Vasopressin in the brain of a desert hibernator, the jerboa (Jaculus orientalis): Presence of sexual dimorphism and seasonal variation. J Comp Neurol 358 (1995) 499-517
29. Landry M., Vila-Porcile E., Hökfelt T., and Calas A. Differential routing of coexisting neuropeptides in vasopressin neurons. Eur J Neurosci 17 (2003) 579-589
30. Lee W., Watanabe M., and Glass J.D. Photoperiod affects the expression of neural cell adhesion molecule and polysialic acid in the hypothalamus of the Siberian hamster. Brain Res 690 (1995) 64-72
31. Lerchl A., and Nieschlag E. Diurnal variations of serum and testicular testosterone and dihydrostestosterone (DHT) in Djungarian hamsters (Phodopus sungorus): Testes are the main source for circulating DHT. Gen Comp Endocrinol 98 (1995) 129-136
32. Ma W., and Bisby M.A. Differential expression of galanin immunoreactivities in the primary sensory neurons following partial and complete sciatic nerve injuries. Neuroscience 79 (1997) 1183-1195
33. Magarinos A.M., McEwen B.S., Saboureau M., and Pevet P. Rapid reversible changes in intrahippocampal connectivity during the course of hibernation in European hamsters. Proc Natl Acad Sci U S A 103 (2006) 18775-18780
34. Merchenthaler I., Hoffman G.E., and Lane M.V. Estrogen and estrogen receptor-β (ERβ)-selective ligands induce galanin expression within gonadotropin hormone-releasing hormone-immunoreactive neurons in the female rat brain. Endocrinology 146 (2005) 2760-2765
35. Miller M.A., Urban J.H., and Dorsa D.M. Steroid dependency of vasopressin neurons in the bed nucleus of the stria terminalis by in situ hybridization. Endocrinology 125 (1989) 2335-2340
36. Miller M.A., De Vries G.J., Al-Shamma H.A., and Dorsa D.M. Decline of vasopressin immunoreactivity and mRNA levels in the bed nucleus of the stria terminalis following castration. J Neurosci 12 (1992) 2881-2887
37. Miller M.A., Kolb P.E., and Raskind M.A. Extra-hypothalamic vasopressin neurons coexpress galanin messenger RNA as shown by double in situ hybridization histochemistry. J Comp Neurol 329 (1993) 378-384
38. Miller M.A., Kolb P.E., and Raskind M.A. Testosterone regulates galanin gene expression in the bed nucleus of the stria terminalis. Brain Res 611 (1993) 338-341
39. Ouarour A., Kirsch R., and Pévet P. Expression of daily torpor in the Djungarian hamster (Phodopus sungorus) is correlated with the testosterone-driven vasopressin content in the lateral septum. Biol Signals 4 (1995) 42-50
40. Pak T.R., Wilson C.J.C., Hinds L.R., and Handa R.J. Estrogen receptor-β mediates dihydrotestosterone-induced stimulation of the arginine vasopressin promoter in neuronal cells. Endocrinology 148 (2007) 3371-3382
41. Perez S.E., Wynick D., Steiner R.A., and Mufson E.J. Distribution of galaninergic immunoreactivity in the brain of the mouse. J Comp Neurol 434 (2001) 158-185
42. Pittman Q.J., Malkinson T.J., Kasting N.W., and Veale W.L. Enhanced fever following castration: possible involvement of brain arginine vasopressin. Am J Physiol 254 (1988) R513-R517
43. Pittman Q.T., Chen X., Mouihate A., Hirasawa M., and Martin S. Arginine vasopressin, fever and temperature regulation. Prog Brain Res 119 (1998) 383-392
44. Planas B., Kolb P.E., Raskind M.A., and Miller M.A. Activation of galanin pathways across puberty in the male rat: Galanin gene expression in the bed nucleus of the stria terminalis and medial amygdala. Neuroscience 63 (1994) 851-858
45. Planas B., Kolb P.E., Raskind M.A., and Miller M.A. Sex difference in coexpression by galanin neurons accounts for sexual dimorphism of vasopressin in the bed nucleus of the stria terminalis. Endocrinology 136 (1995) 727-733
46. Plumari L., Viglietti-Panzica C., Allieri F., Honda S., Harada N., Absil P., Balthazart J., and Panzica G.C. Changes in the arginine-vasopressin immunoreactive systems in male mice lacking a functional aromatase gene. J Neuroendocrinol 14 (2002) 971-978
47. Rajendren G., Levenkova N., and Gibson M.J. Galanin immunoreactivity in mouse basal forebrain: Sex differences and discrete projections of galanin-containing cells beyond the blood-brain barrier. Neuroendocrinology 71 (2000) 27-33
48. Schlatt S., De Geyter M., Kliesch S., Nieschlag E., and Bergmann M. Spontaneous recrudescence of spermatogenesis in the photoinhibited male Djungarian hamster, Phodopus sungorus. Biol Reprod 53 (1995) 1169-1177
49. Shapiro R.A., Xu C., and Dorsa D.M. Differential transcriptional regulation of rat vasopressin gene expression by estrogen receptor α and β. Endocrinology 141 (2000) 4056-4064
50. Shen E.S., Meade E.H., Perez M.C., Deecher D.C., Negro-Vilar A., and Lopez F.J. Expression of functional estrogen receptors and galanin messenger ribonucleic acid in immortalized luteinizing hormone-releasing hormone neurons: Estrogenic control of galanin gene expression. Endocrinology 139 (1998) 939-948
51. Shen E.S., Hardenburg J.M., Meade E.H., Arey B.J., Merchenthaler I., and Lopez F.J. Estradiol induces galanin gene expression in the pituitary of the mouse in an estrogen receptor α-dependent manner. Endocrinology 140 (1999) 2628-2631
52. Shughrue P.J., Scrimo P.J., and Merchenthaler I. Evidence for the colocalisation of estrogen receptor-mRNA and estrogen receptor-immunoreactivity in neurons of the rat forebrain. Endocrinology 139 (1998) 5267-5270
53. Simerly R.B. Wired for reproduction: Organization and development of sexually dimorphic circuits in the mammalian forebrain. Annu Rev Neurosci 25 (2002) 507-536
54. Villar M.J., Cortes R., Theodorsson E., Wiesenfeld-Hallin Z., Schalling M., Fahrenkrug J., Emson P.C., and Hökfelt T. Neuropeptide expression in rat dorsal root ganglion cells and spinal cord after peripheral nerve injury with special reference to galanin. Neuroscience 33 (1989) 587-604
55. von der Ohe C.G., Darian-Smith C., Garner C.G., and Heller H.C. Ubiquitous and temperature dependent neural plasticity in hibernators. J Neurosci 26 (2006) 10590-10598
56. Wang Z., Bullock N.A., and De Vries G.J. Sexual differentiation of vasopressin projections of the bed nucleus of the stria terminalis and medial amygdaloid nucleus in rats. Endocrinology 132 (1993) 2299-2306
57. Wang Z., and De Vries G.J. Androgen and estrogen effects on vasopressin messenger RNA expression in the medial amygdaloid nucleus in male and female rats. J Neuroendocrinol 7 (1995) 827-831
58. Zhou L., Blaustein J.D., and De Vries G.J. Distribution of androgen receptor immunoreactivity in vasopressin- and oxytocin-immunoreactive neurons in the male rat brain. Endocrinology 134 (1994) 2622-2627