Both prolactin (PRL) and a molecular mimic of phosphorylated PRL, S179D-PRL, protect the hippocampus of female rats against excitotoxicity

Neuroscience

Volumn 258, Issue , 2014, Pages 211-217

  Morales, T ^a   Lorenson, M ^b   Walker, A M ^b   Ramos, E ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Amygdala; ERK1 2; Hippocampus; Kainate; Prolactin; STAT5

Indexed keywords

ASPARTIC ACID; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHORYLATED PROLACTIN; PROLACTIN; PROLACTIN DERIVATIVE; SERINE; STAT5 PROTEIN; UNCLASSIFIED DRUG;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN NUCLEUS; CONTROLLED STUDY; DENTATE HILUS; ENZYME ACTIVATION; EXCITOTOXICITY; FEMALE; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPUS; LACTATION; LATERAL BRAIN VENTRICLE; MICRO-OSMOTIC PUMP; NERVE CELL EXCITABILITY; NEUROPROTECTION; NONHUMAN; OSMOTIC PUMP; OVARIECTOMY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; SEIZURE; SIGNAL TRANSDUCTION;

AMYGDALA; ERK; ERK1/2; EXTRACELLULAR-REGULATED KINASE; HIPPOCAMPUS; HPRL; HUMAN PROLACTIN; HUMAN PROLACTIN IN WHICH THE NORMALLY PHOSPHORYLATED SERINE AT POSITION 179 IS REPLACED WITH AN ASPARTATE; KA; KAINATE; KAINIC ACID; NEU-N; NEURONAL NUCLEI; OPRL; OVARIECTOMIZED; OVINE PROLACTIN; OVX; PRL; PROLACTIN; S179D-PRL; SIGNAL TRANSDUCER AND ACTIVATION OF TRANSCRIPTION 5; STAT5;

AMYGDALA; ANIMALS; ARCUATE NUCLEUS; CELL DEATH; EXCITATORY AMINO ACID AGONISTS; FEMALE; HIPPOCAMPUS; HUMANS; KAINIC ACID; MAP KINASE SIGNALING SYSTEM; MOTOR ACTIVITY; NEURONS; NEUROPROTECTIVE AGENTS; PROLACTIN; RATS; RATS, WISTAR; SEIZURES; STAT5 TRANSCRIPTION FACTOR;

EID: 84890242338     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2013.11.015     Document Type: Article

References (52)

1. Bakowska J.C., Morrell J.I. 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 1997, 386:161-177.
2. Ben-Ari Y. Limbic seizure and brain damage produced by kainic acid: mechanisms and relevance to human temporal lobe epilepsy. Neuroscience 1985, 14:375-403.
3. Ben-Ari Y., Cossart R. Kainate, a double agent that generates seizures: two decades of progress. Trends Neurosci 2000, 23:580-587.
4. Ben-Jonathan N., Mershon J.L., Allen D.L., Steinmetz R.W. Extrapituitary prolactin: distribution, regulation, functions, and clinical aspects. Endocr Rev 1996, 17:639-669.
5. Brown R.S., Piet R., Herbison A.E., Grattan D.R. Differential actions of prolactin on electrical activity and intracellular signal transduction in hypothalamic neurons. Endocrinology 2012, 153:2375-2384.
6. Brown RS, Banks WA, Binart N, Grattan DR. Saturable transport of prolactin across the blood-brain barrier is independent of the prolactin receptor. ENDO 2013, The Endocrine Society; 2013 MON-135.
7. Cabrera V., Cantú D., Ramos E., Vanoye-Carlo A., Cerbón M., Morales T. Lactation is a natural model of hippocampus neuroprotection against excitotoxicity. Neurosci Lett 2009, 461:136-139.
8. Cabrera V., Ramos E., González-Arenas A., Cerbón M., Camacho-Arroyo I., Morales T. Lactation reduces glial activation induced by excitotoxicity in the rat hippocampus. J Neuroendocrinol 2013, 25:519-527.
9. Chen T.J., Kuo C.B., Tsai K.F., Liu J.W., Chen D.Y., Walker A.M. Development of recombinant human prolactin receptor antagonists by molecular mimicry of the phosphorylated hormone. Endocrinology 1998, 139:609-616.
10. Chiu S., Wise P.M. Prolactin receptor mRNA localization in the hypothalamus by in situ hybridization. J Neuroendocrinol 1994, 6:191-199.
11. DeVito W.J., Avakian C., Stone S., Ace C.I. Estradiol increases prolactin synthesis and prolactin messenger ribonucleic acid in selected brain regions in the hypophysectomized female rat. Endocrinology 1992, 131:2154-2160.
12. DeVito W.J., Okulicz W.C., Stone S., Avakian C. Prolactin-stimulated mitogenesis of cultured astrocytes. Endocrinology 1992, 130:2549-2556.
13. DeVito W.J., Stone S., Shamgochian M. Prolactin induced expression of glial fibrillary acidic protein and tumor necrosis factor-alpha at a wound site in the rat brain. Mol Cell Endocrinol 1995, 108:125-130.
14. Donner N., Bredewold R., Maloumby R., Neumann I.D. Chronic intracerebral prolactin attenuates neuronal stress circuitries in virgin rats. Eur J Neurosci 2007, 25:1804-1814.
15. Doretto M.C., Oliveira-e-Silva M., Ferreira-Alves D.L., Pires S.G., Garcia-Cairasco N., Reis A.M. Effect of lactation on the expression of audiogenic seizures: association with plasma prolactin profiles. Epilepsy Res 2003, 54:109-121.
16. Durand D., Pampillo M., Caruso C., Lasaga M. Role of metabotropic glutamate receptors in the control of neuroendocrine function. Neuropharmacology 2008, 55:577-583.
17. Gregg C., Shikar V., Larsen P., Mak G., Chojnacki A., Yong V.W., Weiss S. White matter plasticity and enhanced remyelination in the maternal CNS. J Neurosci 2007, 27:1812-1823.
18. Haraguchi S., Koyama T., Hasunuma I., Vaudry H., Tsutsui K. Prolactin increases the synthesis of 7alpha-hydroxypregnenolone, a key factor for induction of locomotor activity, in breeding male Newts. Endocrinology 2010, 151:2211-2222.
19. Huang K., Ueda E., Chen Y., Walker A.M. Paradigm-shifters: phosphorylated prolactin and short prolactin receptors. J Mammary Gland Biol Neoplasia 2008, 13:69-79.
20. Kemppainen S., Pitkänen A. Damage to the amygdalo-hippocampal projection in temporal lobe epilepsy: a tract-tracing study in chronic epileptic rats. Neuroscience 2004, 126:485-501.
21. Kinsley C.H., Lambert K.G. Reproduction-induced neuroplasticity: natural behavioural and neuronal alterations associated with the production and care of offspring. J Neuroendocrinol 2008, 20:515-525.
22. Kokay I.C., Petersen S.L., Grattan D.R. Identification of prolactin-sensitive GABA and kisspeptin neurons in regions of the rat hypothalamus involved in the control of fertility. Endocrinology 2011, 152:526-535.
23. Larriva-Sahd J. Some contributions of Rafael Lorente de Nó to neuroscience: a reminiscence. Brain Res Bull 2002, 59:1-11.
24. Leff M.A., Buckley D.J., Krumenacker J.S., Reed J.C., Miyashita T., Buckley A.R. Rapid modulation of the apoptosis regulatory genes, bcl-2 and bax by prolactin in rat Nb2 lymphoma cells. Endocrinology 1996, 137:5456-5462.
25. Leuner B., Mirescu C., Noiman L., Gould E. Maternal experience inhibits the production of immature neurons in the hippocampus during the postpartum period through elevations in adrenal steroids. Hippocampus 2007, 17:434-442.
26. Mak G.K., Weiss S. Paternal recognition of adult offspring mediated by newly generated CNS neurons. Nat Neurosci 2010, 13:753-758.
27. Mann P.E., Bridges R.S. Lactogenic hormone regulation of maternal behavior. Prog Brain Res 2001, 133:251-262.
28. McNeilly A.S. Lactational control of reproduction. Reprod Fertil Dev 2001, 13:583-590.
29. Moderscheim T.A., Gorba T., Pathipati P., Kokay I.C., Grattan D.R., Williams C.E., Scheepens A. Prolactin is involved in glial responses following a focal injury to the juvenile rat brain. Neuroscience 2007, 145:963-973.
30. Morales T. Recent findings on neuroprotection against excitotoxicity in the hippocampus of female rats. J Neuroendocrinol 2011, 23:994-1001.
31. Munasinghe J.P., Banerjee M., Acosta M.T., Banks M., Heffer A., Silva A.C., Koretsky A., Theodore W.H. Arterial spin labeling demonstrates that focal amygdalar glutamatergic agonist infusion leads to rapid diffuse cerebral activation. Acta Neurol Scand 2010, 121:209-216.
32. Nagano M., Kelly P.A. Tissue distribution and regulation of rat prolactin receptor gene expression. Quantitative analysis by polymerase chain reaction. J Biol Chem 1994, 269:13337-13345.
33. Naylor M.J., Oakes S.R., Gardiner-Garden M., Harris J., Blazek K., Ho T.W., Li F.C., Wynick D., Walker A.M., Ormandy C.J. Transcriptional changes underlying the secretory activation phase of mammary gland development. Mol Endocrinol 2005, 19:1868-1883.
34. Nephew B.C., Amico J., Cai H.M., Walker A.M., Bridges R.S. Intracerebroventricular administration of the prolactin (PRL) receptor antagonist, S179D PRL, disrupts parturition in rats. Reproduction 2007, 134:155-160.
35. Pawluski J.L., Brummelte S., Barha C.K., Crozier T.M., Galea L.A. Effects of steroid hormones on neurogenesis in the hippocampus of the adult female rodent during the estrous cycle, pregnancy, lactation and aging. Front Neuroendocrinol 2009, 30:343-357.
36. Pi X.J., Grattan D.R. Increased prolactin receptor immunoreactivity in the hypothalamus of lactating rats. J Neuroendocrinol 1999, 11:693-705.
37. Pitkänen A. Connectivity of the rat amygdaloid complex. The amygdala: a functional analysis 2000, 31-115. Oxford University Press, New York. J.P. Aggleton (Ed.).
38. Sapsford T.J., Kokay I.C., Ostberg L., Bridges R.S., Grattan D.R. Differential sensitivity of specific neuronal populations of the rat hypothalamus of prolactin action. J Comp Neurol 2012, 520:1062-1077.
39. Sawchenko P.E., Cuningham E.T., Mortrud M.T., Pfeiffer S.W., Gerfen C.R. Phaseolus vulgaris leucoagglutinin anterograde axonal transport technique. Methods in neurosciences 1990, vol. 3. Academic Press, New York.
40. Schroeder M.D., Brockman J.L., Walker A.M., Schuler L.A. Inhibition of prolactin (PRL)-induced proliferative signals in breast cancer cells by a molecular mimic of phosphorylated PRL, S179D-PRL. Endocrinology 2003, 144:5300-5307.
41. Shingo T., Gregg C., Enwere E., Fujikawa H., Hassam R., Geary C., Cross J.C., Weiss S. Pregnancy-stimulated neurogenesis in the adult female forebrain mediated by prolactin. Science 2003, 299:117-120.
42. Siniscalchi A., Gallelli L., Mercuri N.B., De Sarro G. Serum prolactin levels in repetitive temporal epileptic seizures. Eur Rev Med Pharmacol Sci 2008, 12:365-368.
43. Sirzen-Zelenskaya A., Gonzalez-Iglesias A.E., Boutet de Monvel J., Bertram R., Freeman M.E., Gerber U., Egli M. Prolactin induces a hyperpolarising current in rat paraventricular oxytocinergic neurones. J Neuroendocrinol 2011, 23:883-893.
44. Swanson L.W. Brain maps: structure of the rat brain 1998, Elsevier, New York.
45. Tejadilla D., Cerbón M., Morales T. Prolactin reduces the damaging effects of excitotoxicity in the dorsal hippocampus of the female rat independently of ovarian hormones. Neuroscience 2010, 169:1178-1185.
46. Torner L., Neumann I.D. The brain prolactin system: involvement in stress response adaptations in lactation. Stress 2002, 5:249-257.
47. Torner L., Karg S., Blume A., Kandasamy M., Kuhn H.G., Winkler J., Aigner L., Neumann I.D. Prolactin prevents chronic stress-induced decrease of adult hippocampal neurogenesis and promotes neuronal fate. J Neurosci 2009, 29:1826-1833.
48. Vanoye-Carlo A., Morales T., Aguilar E., Mendoza-Rodríguez A., Cerbón M.A. Neuroprotective effects of lactation against kainic acid treatment in the dorsal hippocampus of the rat. Horm Behav 2008, 53:112-123.
49. Walker A.M. S179D prolactin: antagonistic agony!. Mol Cell Endocrinol 2007, 276:1-9.
50. Walsh R.J., Slaby F.J., Posner B.I. A receptor-mediated mechanism for the transport of prolactin from blood to cerebrospinal fluid. Endocrinology 1987, 120:1846-1850.
51. Wu W., Coss D., Lorenson M.Y., Kuo C.B., Xu X., Walker A.M. Different biological effects of unmodified prolactin and a molecular mimic of phosphorylated prolactin involve different signaling pathways. Biochemistry 2003, 42:7561-7570.
52. Zhang X., Gelowitz D., Lai C., Boulton A., Yu P. Gradation of kainic acid-induced rat limbic seizures and expression of hippocampal heat shock protein-70. Eur J Neurosci 1997, 9:760-769.