Bridging the Gap between GPCR activation and behaviour: Oxytocin and prolactin signalling in the hypothalamus

Journal of Molecular Neuroscience

Volumn 43, Issue 2, 2011, Pages 200-208

  Van Den Burg, Erwin H ^a   Neumann, Inga D ^a  

^a UNIVERSITY OF REGENSBURG   (Germany)

Author keywords

Anxiety; Intracellular signalling; Neuropeptides; Paraventricular nucleus; Stress

Indexed keywords

CORTICOTROPIN RELEASING FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; G PROTEIN COUPLED RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE; OXYTOCIN; PROLACTIN;

ANXIETY; ARTICLE; BEHAVIOR; FEMALE; HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS; MALE; NEUROENDOCRINE SYSTEM; NONHUMAN; RAT; STRESS; THALAMUS MIDLINE NUCLEUS; TRANQUILIZING ACTIVITY;

ANIMALS; ANTI-ANXIETY AGENTS; ANXIETY; HYPOTHALAMUS; MITOGEN-ACTIVATED PROTEIN KINASES; OXYTOCIN; PROLACTIN; RECEPTORS, G-PROTEIN-COUPLED; SECOND MESSENGER SYSTEMS; STRESS, PHYSIOLOGICAL;

RATTUS;

EID: 79951672730     PISSN: 08958696     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12031-010-9452-8     Document Type: Article

References (64)

1. JC Bakowska JI Morrell 1997 Atlas of the neurons that express mRNA for the long form of the prolactin receptor in the forebrain of the female rat J Comp Neurol 386 161 177 1:CAS:528:DyaK2sXlvF2itrs%3D 10.1002/(SICI)1096- 9861(19970922)386:2<161::AID-CNE1>3.0.CO;2-# 9295145 (Pubitemid 27392127)
2. JC Bakowska JI Morrell 2003 The distribution of mRNA for the short form of the prolactin receptor in the forebrain of the female rat Mol Brain Res 116 50 58 1:CAS:528:DC%2BD3sXms1ylsbo%3D 10.1016/S0169-328X(03)00213-4 12941460 (Pubitemid 36993696)
3. TL Bale AM Davis AP Auger DM Dorsa MM McCarthy 2001 CNS region-specific oxytocin receptor expression: importance in regulation of anxiety and sex behavior J Neurosci 21 2546 2552 1:CAS:528:DC%2BD3MXjslClsLo%3D 11264328 (Pubitemid 32240551)
4. A Blume OJ Bosch S Miklos, et al. 2008 Oxytocin reduces anxiety via ERK1/2 activation: local effect within the rat hypothalamic paraventricular nucleus Eur J Neurosci 27 1947 1956 10.1111/j.1460-9568.2008.06184.x 18412615 (Pubitemid 351521499)
5. A Blume L Torner Y Liu S Subburaju G Aguilera ID Neumann 2009a Prolactin activates mitogen-activated protein kinase signaling and corticotropin releasing hormone transcription in rat hypothalamic neurons Endocrinology 150 1841 1849 1:CAS:528:DC%2BD1MXktVWls7c%3D 10.1210/en.2008-1023
6. A Blume L Torner Y Liu S Subburaju G Aguilera ID Neumann 2009b Prolactin induces egr-1 gene expression in cultured hypothalamic cells and in the rat hypothalamus Brain Res 1302 34 41 1:CAS:528:DC%2BD1MXhtlyhtbzN 10.1016/j.brainres.2009.09.047
7. C Bole-Feysot V Goffin M Edery N Binart PA Kelly 1998 Prolactin (PRL) and its receptor: actions, signal transduction pathways and phenotypes observed in PRL receptor knockout mice Endocr Rev 19 225 268 1:CAS:528:DyaK1cXktVWhs7k%3D 10.1210/er.19.3.225 9626554 (Pubitemid 29117815)
8. RS Bridges M Numan PM Ronsheim PE Mann CE Lupini 1990 Central prolactin infusions stimulate maternal behavior in steroid-treated, nulliparous female rats Proc Natl Acad Sci USA 87 8003 8007 1:CAS:528:DyaK3cXmtVGisL0%3D 10.1073/pnas.87.20.8003 2236014
9. PJ Brunton JA Russell AJ Douglas 2008 Adaptive responses of the maternal hypothalamic-pituitary-adrenal axis during pregnancy and lactation J Neuroendocrinol 20 764 776 1:CAS:528:DC%2BD1cXnt1Cju78%3D 10.1111/j.1365-2826. 2008.01735.x 18601699 (Pubitemid 351858728)
10. C Clapp L Torner G Guttiérrez-Ospina, et al. 1994 The prolactin gene is expressed in the hypothalamic-neurohypophyseal system and the protein is processed into a 14-kDa fragment with activity like 16-kDa prolactin Proc Natl Acad Sci USA 91 10384 10388 1:CAS:528:DyaK2MXhslemurk%3D 10.1073/pnas.91.22. 10384 7937959 (Pubitemid 24329001)
11. WJ DeVito 1988 Distribution of immunoreactive prolactin in the male and female rat brain: effects of hypophysectomy and intraventricular administration of colchicines Neuroendocrinology 47 284 289 1:CAS:528:DyaL1cXovVegtg%3D%3D 10.1159/000124926 3374755
12. WJ DeVito S Stone C Avakian 1991 Stimulation of hypothalamic prolactin release by veratridine and angiotensin II in the female rat: effect of ovariectomy and estradiol administration Neuroendocrinology 54 391 398 1:CAS:528:DyaK3MXlt1Omtbk%3D 10.1159/000125919 1758581
13. D Devost ME Carrier HH Zingg 2008 Oxytocin-induced activation of eukaryotic elongation factor 2 in myometrial cells is mediated by protein kinase C Endocrinology 149 131 138 1:CAS:528:DC%2BD1cXjtVyhsQ%3D%3D 10.1210/en.2007-0548 17947356
14. B Ditzen M Schaer B Gabriel G Bodenmann U Ehlert M Heinrichs 2009 Intranasal oxytocin increases positive communication and reduces cortisol levels during couple conflict Biol Psychiatry 65 728 731 1:CAS:528: DC%2BD1MXktV2qsbw%3D 10.1016/j.biopsych.2008.10.011 19027101
15. N Donner R Bredewold R Maloumby ID Neumann 2007 Chronic intracerebral prolactin attenuates neuronal stress circuitries in virgin rats Eur J Neurosci 25 1804 1814 10.1111/j.1460-9568.2007.05416.x 17432967 (Pubitemid 46549997)
16. M Engelmann R Landgraf CT Wotjak 2004 The hypothalamic-neurohypophysial system regulates the hypothalamic-pituitary-adrenal axis under stress: an old concept revisited Front Neuroendocrinol 25 132 149 1:CAS:528: DC%2BD2cXhtVKltL%2FP 10.1016/j.yfrne.2004.09.001 15589266 (Pubitemid 39626771)
17. T Fujikawa H Soya KL Tamashiro, et al. 2004 Prolactin prevents acute stress-induced hypocalcemia and ulcerogenesis by acting in the brain of rat Endocrinology 145 2006 2013 1:CAS:528:DC%2BD2cXis1SisbY%3D 10.1210/en.2003-1446 14715716 (Pubitemid 38402410)
18. G Gimpl F Fahrenholz 2001 The oxytocin receptor system: structure, function, and regulation Phys Rev 81 629 683 1:CAS:528:DC%2BD3MXislCrsLk%3D (Pubitemid 32267075)
19. O Goupille J-V Barnier B Guibert J Paly J Djiane 2000 Effect of PRL on MAPK activation: negative regulatory role of the C-terminal part of the PRL receptor Mol Cell Endocrinol 159 133 146 1:CAS:528:DC%2BD3cXht1Gru7w%3D 10.1016/S0303-7207(99)00197-5 10687859 (Pubitemid 30067647)
20. M Gravati M Busnelli E Bulgheroni, et al. 2010 Dual modulation of inward rectifier potassium currents in olfactory neuronal cells by promiscuous G protein coupling of the oxytocin receptor J Neurochem 114 1424 1435 1:CAS:528:DC%2BC3cXhtFSlurfO 20557424
21. M Heinrichs G Meinlschmidt I Neumann, et al. 2001 Effects of suckling on hypothalamic-pituitary-adrenal axis responses to psychosocial stress in postpartum lactating women J Clin Endocrinol Metab 86 4798 4804 1:CAS:528:DC%2BD3MXptVarsL4%3D 10.1210/jc.86.10.4798 11600543 (Pubitemid 33020522)
22. M Heinrichs T Baumgartner C Kirschbaum U Ehlert 2003 Social support and oxytocin interact to suppress cortisol and subjective responses to psychosocial stress Biol Psychiatry 54 1389 1398 1:CAS:528:DC%2BD3sXpvVWqt7o%3D 10.1016/S0006-3223(03)00465-7 14675803 (Pubitemid 37522163)
23. S Hoare JA Copland Z Strakova, et al. 1999 The proximal portion of the COOH terminus of the oxytocin receptor is required for coupling to g(q), but not g(i). Independent mechanisms for elevating intracellular calcium concentrations from intracellular stores J Biol Chem 274 28682 28689 1:CAS:528: DyaK1MXmsFWns7w%3D 10.1074/jbc.274.40.28682 10497238 (Pubitemid 29473001)
24. D Huber P Veinante R Stoop 2005 Vasopressin and oxytocin excite distinct neuronal populations in the central amygdala Science 308 245 248 1:CAS:528:DC%2BD2MXivFCgsL0%3D 10.1126/science.1105636 15821089 (Pubitemid 40558858)
25. M Kosfeld M Heinrichs PJ Zak U Fischbacher E Fehr 2005 Oxytocin increases trust in humans Nature 435 673 676 1:CAS:528:DC%2BD2MXks1Ogur8%3D 10.1038/nature03701 15931222 (Pubitemid 40825511)
26. CY Ku A Qian Y Wen K Anwer BM Sanborn 1995 Oxytocin stimulates myometrial guanosine triphosphatase and phospholipase-C activities via coupling to G alpha q/11 Endocrinology 136 1509 1515 1:CAS:528:DyaK2MXks1Cisrg%3D 10.1210/en.136.4.1509 7895660
27. SR Ladyman RA Augustine GR Grattan 2010 Hormone interactions regulating energy balance during pregnancy J Neuroendocrinol 22 805 817 1:CAS:528:DC%2BC3cXovFejsbo%3D 20456605
28. R Landgraf ID Neumann 2004 Vasopressin and oxytocin release within the brain: a dynamic concept of multiple and variable modes of neuropeptide communication Front Neuroendocrinol 25 150 176 1:CAS:528:DC%2BD2cXhtVKltL%2FI 10.1016/j.yfrne.2004.05.001 15589267 (Pubitemid 39642188)
29. CM Larsen IC Kokay DR Grattan 2008 Male pheromones initiate prolactin-induced neurogenesis and advance maternal behavior in female mice Horm Behav 53 509 517 1:CAS:528:DC%2BD1cXjs1SksLw%3D 10.1016/j.yhbeh.2007.11.020 18258236
30. M Ludwig G Leng 2006 Dendritic peptide release and peptide-dependent behaviours Nat Rev Neurosci 7 126 136 1:CAS:528:DC%2BD28XlvV2qtQ%3D%3D 10.1038/nrn1845 16429122 (Pubitemid 43151599)
31. GK Mak EK Enwere C Gregg, et al. 2007 Male pheromone-stimulated neurogenesis in the adult female brain: possible role in mating behavior Nat Neurosci 10 1003 1011 1:CAS:528:DC%2BD2sXotFyktL8%3D 10.1038/nn1928 17603480 (Pubitemid 47185196)
32. LP Mangurian RJ Walsh BI Posner 1992 Prolactin enhancement of its own uptake at the choroid plexus Endocrinology 131 698 702 1:CAS:528: DyaK38XlsVertbw%3D 10.1210/en.131.2.698 1639017
33. SL Meddle VR Bishop E Gkoumassi FW van Leeuwen AJ Douglas 2007 Dynamic changes in oxytocin receptor expression and activation at parturition in the rat brain Endocrinology 148 5095 5104 1:CAS:528:DC%2BD2sXhtFWls7fK 10.1210/en.2007-0615 17628000 (Pubitemid 47481536)
34. G Muccioli C Ghe R Di Carlo 1991 Distribution and characterization of prolactin binding sites in the male and female rat brain: effects of hypophysectomy and ovariectomy Neuroendocrinology 53 47 53 1:CAS:528: DyaK3MXos1Q%3D 10.1159/000125696 2046861
35. ID Neumann 2001 Alterations in behavioral and neuroendocrine stress coping strategies in pregnant, parturient and lactating rats Prog Brain Res 133 143 152 1:CAS:528:DC%2BD3MXns1yqsr0%3D 10.1016/S0079-6123(01)33011-X 11589127 (Pubitemid 36987517)
36. ID Neumann 2007 Stimuli and consequences of dendritic release of oxytocin within the brain Biochem Soc Trans 35 1252 1257 1:CAS:528:DC%2BD2sXht1eru7nL 10.1042/BST0351252 17956324 (Pubitemid 350206473)
37. ID Neumann 2008 Brain oxytocin: a key regulator of emotional and social behaviours in both females and males J Neuroendocrinol 20 858 865 1:CAS:528:DC%2BD1cXnt1Cis7w%3D 10.1111/j.1365-2826.2008.01726.x 18601710 (Pubitemid 351858739)
38. ID Neumann 2009 The advantage of social living: brain neuropeptides mediate the beneficial consequences of sex and motherhood Front Neuroendocrinol 30 483 496 1:CAS:528:DC%2BD1MXhtFGksLjJ 10.1016/j.yfrne.2009.04.012 19416734
39. ID Neumann N Toschi 2000 Sequence design and practical implementation of antisense oligonucleotides in neuroendocrinology Methods Enzymol 314 223 238 1:CAS:528:DC%2BD3cXnt1ertA%3D%3D 10.1016/S0076-6879(99)14106-5 10565016
40. I Neumann JA Russell R Landgraf 1993 Oxytocin and vasopressin release within the supraoptic and paraventricular nuclei of pregnant, parturient and lactating rats: a microdialysis study Neuroscience 53 65 75 1:CAS:528: DyaK3sXitVGmu78%3D 10.1016/0306-4522(93)90285-N 8469313 (Pubitemid 23083308)
41. ID Neumann L Torner A Wigger 2000 Brain oxytocin: differential inhibition of neuroendocrine stress responses and anxiety-related behaviour in virgin, pregnant and lactating rats Neuroscience 95 567 575 1:CAS:528:DyaK1MXnslGlsrc%3D 10.1016/S0306-4522(99)00433-9 10658637
42. ID Neumann A Wigger L Torner F Holsboer R Landgraf 2000 Brain oxytocin inhibits basal and stress-induced activity of the hypothalamo-pituitary-adrenal axis in male and female rats: partial action within the paraventricular nucleus J Neuroendocrinol 12 235 243 1:CAS:528:DC%2BD3cXisVSgtr0%3D 10.1046/j.1365-2826. 2000.00442.x 10718919 (Pubitemid 30156515)
43. X-J Pi DR Grattan 1998 Differential expression of the two forms of prolactin receptor mRNA within microdissected hypothalamic nuclei of the rat Mol Brain Res 59 1 12 1:CAS:528:DyaK1cXkvFOksLc%3D 10.1016/S0169-328X(98)00109-0 9729233 (Pubitemid 28408441)
44. X-J Pi DR Grattan 1999 Expression of prolactin receptor mRNA is increased in the preoptic area of lactating rats Endocr 11 91 98 1:CAS:528: DyaK1MXns1eitLo%3D 10.1385/ENDO:11:1:91
45. X-J Pi DR Grattan 1999 Increased prolactin receptor immunoreactivity in the hypothalamus of lactating rats J Neuroendocrinol 11 693 705 1:CAS:528:DyaK1MXlvVGqsrk%3D 10.1046/j.1365-2826.1999.00386.x 10447808 (Pubitemid 29401529)
46. RH Ring JE Malberg L Potestio, et al. 2006 Anxiolytic-like activity of oxytocin in male mice: behavioral and autonomic evidence, therapeutic implications Psychopharmacology 185 218 225 1:CAS:528:DC%2BD28Xit1Cjt70%3D 10.1007/s00213-005-0293-z 16418825 (Pubitemid 43363618)
47. T Shingo C Gregg E Enwere, et al. 2003 Pregnancy-stimulated neurogenesis in the adult female forebrain mediated by prolactin Science 299 117 120 1:CAS:528:DC%2BD38XpvVensLk%3D 10.1126/science.1076647 12511652 (Pubitemid 36042416)
48. DA Slattery ID Neumann 2008 No stress please! Mechanisms of stress hyporesponsiveness of the maternal brain J Physio 586 2 377 385 1:CAS:528:DC%2BD1cXhsFSisL4%3D 10.1113/jphysiol.2007.145896
49. Z Strakova JA Copland SJ Lolait MS Soloff 1998 ERK2 mediates oxytocin-stimulated PGE2 synthesis Am J Physiol 274 E634 E641 1:CAS:528:DyaK1cXislyhtLw%3D 9575824
50. K Tomizawa I Norichika YF Lu, et al. 2003 Oxytocin improves long-lasting spatial memory during motherhood through MAP kinase cascade Nat Neurosci 6 384 390 1:CAS:528:DC%2BD3sXitlequ74%3D 10.1038/nn1023 12598900 (Pubitemid 36373984)
51. L Torner S Mejía FJ López-Gómez A Quintanar G Martínez de la Escalera C Clapp 1995 A 14-kilodalton prolactin-like fragment is secreted by the hypothalamo-neurohypophyseal system of the rat Endocrinology 136 5454 5460 1:CAS:528:DyaK2MXps1Kisr0%3D 10.1210/en.136.12.5454 7588295
52. L Torner N Toschi A Pohlinger R Landgraf ID Neumann 2001 Anxiolytic and anti-stress effects of brain prolactin: improved efficacy of antisense targeting of the prolactin receptor by molecular modeling J Neurosci 21 3207 3214 1:CAS:528:DC%2BD3MXjtFyqu7g%3D 11312305 (Pubitemid 32323502)
53. L Torner N Toschi G Nava C Clapp ID Neumann 2002 Increased hypothalamic expression of prolactin in lactation: involvement in behavioural and neuroendocrine stress responses Eur J Neurosci 15 1381 1389 10.1046/j.1460-9568. 2002.01965.x 11994132 (Pubitemid 35477999)
54. L Torner R Maloumby G Nava J Aranda C Clapp ID Neumann 2004 In vivo release and gene upregulation of brain prolactin in response to physiological stimuli Eur J Neurosci 19 1601 1608 10.1111/j.1460-9568.2004.03264.x 15066156 (Pubitemid 38437922)
55. L Torner S Karg A Blume, et al. 2009 Prolactin prevents chronic stress-induced decrease of adult hippocampal neurogenesis and promotes neuronal fate J Neurosci 29 1826 1833 1:CAS:528:DC%2BD1MXit1Witbc%3D 10.1523/JNEUROSCI. 3178-08.2009 19211889
56. AH Veenema ID Neumann 2008 Central vasopressin and oxytocin release: regulation of complex social behaviours Prog Brain Res 179 261 276 10.1016/S0079-6123(08)00422-6 (Pubitemid 352010234)
57. M Waldherr ID Neumann 2007 Centrally released oxytocin mediates mating-induced anxiolysis in male rats Proc Natl Acad Sci USA 104 16681 16684 1:CAS:528:DC%2BD2sXht1Wmu7zL 10.1073/pnas.0705860104 17925443 (Pubitemid 350211076)
58. RJ Walsh FJ Slaby BI Posner 1987 A receptor-mediated mechanism for the transport of prolactin from blood to cerebrospinal fluid Endocrinology 120 1846 1850 1:CAS:528:DyaL2sXitVyjtrY%3D 10.1210/endo-120-5-1846 3569115 (Pubitemid 17069213)
59. L Whitesell D Geselowitz C Chavany, et al. 1993 Stability, clearance, and disposition of intraventricularly administered oligodeoxynucleotides: implications for therapeutic application within the central nervous system Proc Natl Acad Sci USA 90 4665 4669 1:CAS:528:DyaK3sXks1agtLk%3D 10.1073/pnas.90.10. 4665 8506315 (Pubitemid 23148966)
60. RJ Windle N Shanks SL Lightman CD Ingram 1997 Central oxytocin administration reduces stress-induced corticosterone release and anxiety behaviour in rats Endocrinology 138 2829 2834 1:CAS:528:DyaK2sXktVKgsLg%3D 10.1210/en.138.7.2829 9202224 (Pubitemid 27258513)
61. RJ Windle YM Kershaw N Shanks SA Wood SL Lightman CD Ingram 2004 Oxytocin attenuates stress-induced c-fos mRNA expression in specific forebrain regions associated with modulation of hypothalamo-pituitary-adrenal activity J Neurosci 24 2974 2982 1:CAS:528:DC%2BD2cXjtFWmsr0%3D 10.1523/JNEUROSCI.3432-03.2004 15044536 (Pubitemid 38405745)
62. M Yoshida Y Takayanagi K Inoue, et al. 2009 Evidence that oxytocin exerts anxiolytic effects via oxytocin receptor expressed in serotonergic neurons in mice J Neurosci 29 2259 2271 1:CAS:528:DC%2BD1MXisV2gsrw%3D 10.1523/JNEUROSCI. 5593-08.2009 19228979
63. M Zhong M Yang BM Sanborn 2003 Extracellular signal-regulated kinase 1 / 2 activation by myometrial oxytocin receptor involves Galpha(q)Gbetagamma and epidermal growth factor receptor tyrosine kinase activation Endocrinology 144 2947 2956 1:CAS:528:DC%2BD3sXkvF2ktrk%3D 10.1210/en.2002-221039 12810550 (Pubitemid 36819897)
64. HH Zingg SA Laporte 2003 The oxytocin receptor Trends Endocrinol Metab 14 222 227 1:CAS:528:DC%2BD3sXkvVCmu70%3D 10.1016/S1043-2760(03)00080-8 12826328 (Pubitemid 36841480)