Inhibition of prolactin with bromocriptine for 28days increases blood-brain barrier permeability in the rat

Neuroscience

Volumn 301, Issue , 2015, Pages 61-70

  Rosas Hernandez, H ^a   Ramirez, M ^a   Ramirez Lee, M A ^a   Ali, S F ^b   Gonzalez, C ^a  

^a UNIVERSIDAD AUTÓNOMA DE SAN LUIS POTOSÍ   (Mexico)

^b NATIONAL CENTER FOR TOXICOLOGICAL RESEARCH   (United States)

Author keywords

Blood brain barrier; Lipopolysaccharide; Permeability; Prolactin; Tight junctions

Indexed keywords

BROMOCRIPTINE; CLAUDIN 5; GLIAL FIBRILLARY ACIDIC PROTEIN; MEMBRANE PROTEIN; OCCLUDIN; PROLACTIN; PROLACTIN RECEPTOR; SCAFFOLD PROTEIN; TIGHT JUNCTION PROTEIN; CLDN5 PROTEIN, RAT; DOPAMINE RECEPTOR STIMULATING AGENT; HORMONE ANTAGONIST; OCLN PROTEIN, RAT;

ANIMAL EXPERIMENT; ARTICLE; BLOOD BRAIN BARRIER; BLOOD VESSEL PERMEABILITY; BRAIN BLOOD VESSEL; BRAIN EDEMA; BRAIN FUNCTION; CONTROLLED STUDY; IN VITRO STUDY; IN VIVO STUDY; MALE; MICROPHOTOGRAPHY; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; TIGHT JUNCTION; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; CAPILLARY PERMEABILITY; METABOLISM; WISTAR RAT;

ANIMALS; BLOOD-BRAIN BARRIER; BRAIN EDEMA; BROMOCRIPTINE; CAPILLARY PERMEABILITY; CLAUDIN-5; DOPAMINE AGONISTS; HORMONE ANTAGONISTS; MALE; OCCLUDIN; PROLACTIN; RATS; RATS, WISTAR;

EID: 84931270125     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2015.05.066     Document Type: Article

References (60)

1. Arredondo Zamarripa D., Diaz-Lezama N., Melendez Garcia R., Chavez Balderas J., Adan N., Ledesma-Colunga M.G., Arnold E., Clapp C., Thebault S. Vasoinhibins regulate the inner and outer blood-retinal barrier and limit retinal oxidative stress. Front Cell Neurosci 2014, 8:333.
2. Barichello T., Fagundes G.D., Generoso J.S., Elias S.G., Simoes L.R., Teixeira A.L. Pathophysiology of neonatal acute bacterial meningitis. J Med Microbiol 2013, 62:1781-1789.
3. Bernacki J., Dobrowolska A., Nierwinska K., Malecki A. Physiology and pharmacological role of the blood-brain barrier. Pharmacol Rep 2008, 60:600-622.
4. Bole-Feysot C., Goffin V., Edery M., Binart N., Kelly P.A. Prolactin (PRL) and its receptor: actions, signal transduction pathways and phenotypes observed in PRL receptor knockout mice. Endocr Rev 1998, 19:225-268.
5. Bozzi Y., Borrelli E. The role of dopamine signaling in epileptogenesis. Front Cell Neurosci 2013, 7:157.
6. Burckard E., Patrigeon R.G., Felten D., Combourieu E., Escarment J. Convulsions due to a postpartum cerebral angiopathy associated with the administration of bromocriptine. Ann Fr Anesth Reanim 2003, 22:46-49.
7. Cardoso F.L., Brites D., Brito M.A. Looking at the blood-brain barrier: molecular anatomy and possible investigation approaches. Brain Res Rev 2010, 64:328-363.
8. Corbacho A.M., Martinez De La Escalera G., Clapp C. Roles of prolactin and related members of the prolactin/growth hormone/placental lactogen family in angiogenesis. J Endocrinol 2002, 173:219-238.
9. Cucullo L., Hallene K., Dini G., Dal Toso R., Janigro D. Glycerophosphoinositol and dexamethasone improve transendothelial electrical resistance in an in vitro study of the blood-brain barrier. Brain Res 2004, 997:147-151.
10. Daneman R., Zhou L., Agalliu D., Cahoy J.D., Kaushal A., Barres B.A. The mouse blood-brain barrier transcriptome: a new resource for understanding the development and function of brain endothelial cells. PLoS One 2010, 5:e13741.
11. Ebnet K. Organization of multiprotein complexes at cell-cell junctions. Histochem Cell Biol 2008, 130:1-20.
12. Flint D.J., Gardner M. Evidence that growth hormone stimulates milk synthesis by direct action on the mammary gland and that prolactin exerts effects on milk secretion by maintenance of mammary deoxyribonucleic acid content and tight junction status. Endocrinology 1994, 135:1119-1124.
13. Forster C. Tight junctions and the modulation of barrier function in disease. Histochem Cell Biol 2008, 130:55-70.
14. Freeman M.E., Kanyicska B., Lerant A., Nagy G. Prolactin: structure, function, and regulation of secretion. Physiol Rev 2000, 80:1523-1631.
15. Fresnoza S., Stiksrud E., Klinker F., Liebetanz D., Paulus W., Kuo M.F., Nitsche M.A. Dosage-dependent effect of dopamine D2 receptor activation on motor cortex plasticity in humans. J Neurosci 2014, 34:10701-10709.
16. Gomez R., Gonzalez-Izquierdo M., Zimmermann R.C., Novella-Maestre E., Alonso-Muriel I., Sanchez-Criado J., Remohi J., Simon C., Pellicer A. Low-dose dopamine agonist administration blocks vascular endothelial growth factor (VEGF)-mediated vascular hyperpermeability without altering VEGF receptor 2-dependent luteal angiogenesis in a rat ovarian hyperstimulation model. Endocrinology 2006, 147:5400-5411.
17. Gurney K.J., Estrada E.Y., Rosenberg G.A. Blood-brain barrier disruption by stromelysin-1 facilitates neutrophil infiltration in neuroinflammation. Neurobiol Dis 2006, 23:87-96.
18. Hawkins B.T., Davis T.P. The blood-brain barrier/neurovascular unit in health and disease. Pharmacol Rev 2005, 57:173-185.
19. Hollis J.H., Lightman S.L., Lowry C.A. Lipopolysaccharide has selective actions on sub-populations of catecholaminergic neurons involved in activation of the hypothalamic-pituitary-adrenal axis and inhibition of prolactin secretion. J Endocrinol 2005, 184:393-406.
20. 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.
21. Jangula A., Murphy E.J. Lipopolysaccharide-induced blood brain barrier permeability is enhanced by alpha-synuclein expression. Neurosci Lett 2013, 551:23-27.
22. Kang H.S., Ahn H.S., Kang H.J., Gye M.C. Effect of estrogen on the expression of occludin in ovariectomized mouse brain. Neurosci Lett 2006, 402:30-34.
23. Kasum M., Vrcic H., Stanic P., Jezek D., Oreskovic S., Beketic-Oreskovic L., Pekez M. Dopamine agonists in prevention of ovarian hyperstimulation syndrome. Gynecol Endocrinol 2014, 1-5.
24. Keep R.F., Hua Y., Xi G. Brain water content. A misunderstood measurement?. Translat Stroke Res 2012, 3:263-265.
25. Kletzky O.A., Rossman F., Bertolli S.I., Platt L.D., Mishell D.R. Dynamics of human chorionic gonadotropin, prolactin, and growth hormone in serum and amniotic fluid throughout normal human pregnancy. Am J Obstet Gynecol 1985, 151:878-884.
26. Kumlien E., Lundberg P.O. Seizure risk associated with neuroactive drugs: data from the WHO adverse drug reactions database. Seizure 2010, 19:69-73.
27. Liebner S., Corada M., Bangsow T., Babbage J., Taddei A., Czupalla C.J., Reis M., Felici A., Wolburg H., Fruttiger M., Taketo M.M., von Melchner H., Plate K.H., Gerhardt H., Dejana E. Wnt/beta-catenin signaling controls development of the blood-brain barrier. J Cell Biol 2008, 183:409-417.
28. Liebner S., Czupalla C.J., Wolburg H. Current concepts of blood-brain barrier development. Int J Dev Biol 2011, 55:467-476.
29. Lindh J. Short episode of seizures in a newborn of a mother treated with levodopa/carbidopa/entacapone and bromocriptine. Mov Disord 2007, 22:1515.
30. Linzell J.L., Peaker M., Taylor J.C. The effects of prolactin and oxytocin on milk secretion and on the permeability of the mammary epithelium in the rabbit. J Physiol 1975, 253:547-563.
31. Liu W.Y., Wang Z.B., Zhang L.C., Wei X., Li L. Tight junction in blood-brain barrier: an overview of structure, regulation, and regulator substances. CNS Neurosci Ther 2012, 18:609-615.
32. Marchi N., Angelov L., Masaryk T., Fazio V., Granata T., Hernandez N., Hallene K., Diglaw T., Franic L., Najm I., Janigro D. Seizure-promoting effect of blood-brain barrier disruption. Epilepsia 2007, 48:732-742.
33. Molitch M.E. Management of medically refractory prolactinoma. J Neurooncol 2014, 117:421-428.
34. Morales T., Lorenson M., Walker A.M., Ramos E. Both prolactin (PRL) and a molecular mimic of phosphorylated PRL, S179D-PRL, protect the hippocampus of female rats against excitotoxicity. Neuroscience 2014, 258:211-217.
35. Moreno-Smith M., Lee S.J., Lu C., Nagaraja A.S., He G., Rupaimoole R., Han H.D., Jennings N.B., Roh J.W., Nishimura M., Kang Y., Allen J.K., Armaiz G.N., Matsuo K., Shahzad M.M., Bottsford-Miller J., Langley R.R., Cole S.W., Lutgendorf S.K., Siddik Z.H., Sood A.K. Biologic effects of dopamine on tumor vasculature in ovarian carcinoma. Neoplasia 2013, 15:502-510.
36. Muresanu D.F., Sharma A., Sharma H.S. Diabetes aggravates heat stress-induced blood-brain barrier breakdown, reduction in cerebral blood flow, edema formation, and brain pathology: possible neuroprotection with growth hormone. Ann N Y Acad Sci 2010, 1199:15-26.
37. Nguyen D.A., Parlow A.F., Neville M.C. Hormonal regulation of tight junction closure in the mouse mammary epithelium during the transition from pregnancy to lactation. J Endocrinol 2001, 170:347-356.
38. Northrop N.A., Yamamoto B.K. Persistent neuroinflammatory effects of serial exposure to stress and methamphetamine on the blood-brain barrier. J Neuroimmune Pharmacol 2012, 7:951-968.
39. Nyberg F., Sharma H.S. Repeated topical application of growth hormone attenuates blood-spinal cord barrier permeability and edema formation following spinal cord injury: an experimental study in the rat using Evans blue, ([125])I-sodium and lanthanum tracers. Amino Acids 2002, 23:231-239.
40. Oby E., Janigro D. The blood-brain barrier and epilepsy. Epilepsia 2006, 47:1761-1774.
41. Peixoto E.B., Collares-Buzato C.B. Modulation of the epithelial barrier by dexamethasone and prolactin in cultured Madin-Darby canine kidney (MDCK) cells. Cell Biol Int 2006, 30:101-113.
42. Perez-Lloret S., Rascol O. Dopamine receptor agonists for the treatment of early or advanced Parkinson's disease. CNS Drugs 2010, 24:941-968.
43. Persidsky Y., Ramirez S.H., Haorah J., Kanmogne G.D. Blood-brain barrier: structural components and function under physiologic and pathologic conditions. J Neuroimmune Pharmacol 2006, 1:223-236.
44. Ramirez M., Wu Z., Moreno-Carranza B., Jeziorski M.C., Arnold E., Diaz-Lezama N., Martinez de la Escalera G., Colosi P., Clapp C. Vasoinhibin gene transfer by adenoassociated virus type 2 protects against VEGF- and diabetes-induced retinal vasopermeability. Invest Ophthalmol Vis Sci 2011, 52:8944-8950.
45. Rosas-Hernandez H., Cuevas E., Lantz S.M., Hamilton W.R., Ramirez-Lee M.A., Ali S.F., Gonzalez C. Prolactin and blood-brain barrier permeability. Curr Neurovasc Res 2013, 10:278-286.
46. Rosas-Hernandez H., Cuevas E., Lantz-McPeak S.M., Ali S.F., Gonzalez C. Prolactin protects against the methamphetamine-induced cerebral vascular toxicity. Curr Neurovasc Res 2013, 10:346-355.
47. Sadowska G.B., Malaeb S.N., Stonestreet B.S. Maternal glucocorticoid exposure alters tight junction protein expression in the brain of fetal sheep. Am J Physiol Heart Circ Physiol 2010, 298:H179-188.
48. Salvador E., Shityakov S., Forster C. Glucocorticoids and endothelial cell barrier function. Cell Tissue Res 2014, 355:597-605.
49. Sharma H.S., Ali S.F. Alterations in blood-brain barrier function by morphine and methamphetamine. Ann N Y Acad Sci 2006, 1074:198-224.
50. Stelwagen K., McFadden H.A., Demmer J. Prolactin, alone or in combination with glucocorticoids, enhances tight junction formation and expression of the tight junction protein occludin in mammary cells. Mol Cell Endocrinol 1999, 156:55-61.
51. Tam S.J., Watts R.J. Connecting vascular and nervous system development: angiogenesis and the blood-brain barrier. Annu Rev Neurosci 2010, 33:379-408.
52. Tejadilla D., Cerbon 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.
53. Tishkina O., Stepanichev M.Y., Lazareva N.A., Kulagina A.O., Gulyaeva N.V. The glial response in the rodent hippocampus to systemic administration of bacterial lipopolysaccharide. Neurochem J 2014, 8:144-147.
54. Ueda E.K., Huang K., Nguyen V., Ferreira M., Andre S., Walker A.M. Distribution of prolactin receptors suggests an intraductal role for prolactin in the mouse and human mammary gland, a finding supported by analysis of signaling in polarized monolayer cultures. Cell Tissue Res 2011, 346:175-189.
55. van Vliet E.A., da Costa Araujo S., Redeker S., van Schaik R., Aronica E., Gorter J.A. Blood-brain barrier leakage may lead to progression of temporal lobe epilepsy. Brain 2007, 130:521-534.
56. Virgintino D., Errede M., Robertson D., Capobianco C., Girolamo F., Vimercati A., Bertossi M., Roncali L. Immunolocalization of tight junction proteins in the adult and developing human brain. Histochem. Cell Biol. 2004, 122:51-59.
57. Weksler B.B., Subileau E.A., Perriere N., Charneau P., Holloway K., Leveque M., Tricoire-Leignel H., Nicotra A., Bourdoulous S., Turowski P., Male D.K., Roux F., Greenwood J., Romero I.A., Couraud P.O. Blood-brain barrier-specific properties of a human adult brain endothelial cell line. FASEB J 2005, 19:1872-1874.
58. Wu X.L., Wang P., Liu Y.H., Xue Y.X. Effects of poly (ADP-ribose) polymerase inhibitor 3-aminobenzamide on blood-brain barrier and dopaminergic neurons of rats with lipopolysaccharide-induced Parkinson's disease. J Mol Neurosc 2014, 53:1-9.
59. Zarei S., Frieden M., Rubi B., Villemin P., Gauthier B.R., Maechler P., Vischer U.M. Dopamine modulates von Willebrand factor secretion in endothelial cells via D2-D4 receptors. J Thromb Haemost 2006, 4:1588-1595.
60. Zhao Z., Hu J., Gao X., Liang H., Liu Z. Activation of AMPK attenuates lipopolysaccharide-impaired integrity and function of blood-brain barrier in human brain microvascular endothelial cells. Exp Mol Pathol 2014, 97:386-392.