Sex and estrogen receptor expression influence opioid peptide levels in the mouse hippocampal mossy fiber pathway

Neuroscience Letters

Volumn 552, Issue , 2013, Pages 66-70

  Van Kempen, Tracey A ^a   Kahlid, Sana ^a   Gonzalez, Andreina D ^a   Spencer Segal, Joanna L ^b,c   Tsuda, Mumeko C ^d   Ogawa, Sonoko ^d   McEwen, Bruce S ^b   Waters, Elizabeth M ^b   Milner, Teresa A ^a,b  

^a FEIL FAMILY BRAIN AND MIND RESEARCH INSTITUTE   (United States)

^b ROCKEFELLER UNIVERSITY   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF TSUKUBA   (Japan)

Author keywords

CA3 region; Dentate gyrus; Opioids; Synaptic plasticity

Indexed keywords

DYNORPHIN; ENKEPHALIN; ESTRADIOL BENZOATE; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; OPIATE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENTATE GYRUS; DRUG BRAIN LEVEL; DRUG EFFECT; ESTRUS CYCLE; FEMALE; HIPPOCAMPAL MOSSY FIBER; IMMUNOCYTOCHEMISTRY; KNOCKOUT MOUSE; MALE; MOUSE; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SEX DIFFERENCE; SIGNAL TRANSDUCTION; SPECIES DIFFERENCE; WILD TYPE;

AERKO; BDNF; BERKO; BOVINE SERUM ALBUMIN; BRAIN DERIVED NEUROTROPHIC FACTOR; BSA; CA1; CA3; CA3 REGION; CORNU AMMONIS 1 REGION; CORNU AMMONIS 3 REGION; DENTATE GYRUS; DG; DYN; DYNORPHIN; EB; ER; ESTRADIOL BENZOATE; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA KNOCK OUT MICE; ESTROGEN RECEPTOR BETA KNOCK OUT MICE; G-PROTEIN-COUPLED ESTROGEN RECEPTOR 1; GLC; GPER1; GRANULE CELL LAYER; HIL; HILUS OF THE DENTATE GYRUS; IGG; IMMUNOGLOBULIN; IMMUNOREACTIVITY; IR; L-ENK; LEU-ENKEPHALIN; LONG TERM POTENTIATION; LTP; OPIOIDS; OVARIECTOMY; OVX; PB; PCL; PHOSPHATE BUFFER; PYRAMIDAL CELL LAYER; SLU; SR; STRATUM LUCIDUM; STRATUM RADIATUM; SYNAPTIC PLASTICITY; TRIS-SALINE; TS; WILD-TYPE MICE; WT;

ANIMALS; CA3 REGION, HIPPOCAMPAL; DENTATE GYRUS; DYNORPHINS; ENKEPHALINS; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; ESTROUS CYCLE; FEMALE; MALE; MICE; MICE, KNOCKOUT; MOSSY FIBERS, HIPPOCAMPAL; SEX CHARACTERISTICS;

EID: 84884261298     PISSN: 03043940     EISSN: 18727972     Source Type: Journal    
DOI: 10.1016/j.neulet.2013.07.048     Document Type: Article

References (37)

1. Akama K.T., Thompson L.I., Milner T.A., McEwen B.S. Post-synaptic density-95 (PSD-95) binding capacity of G-protein-coupled receptor 30 (GPR30), an estrogen receptor that can be identified in hippocampal dendritic spines. J. Biol. Chem. 2013, 288:6438-6450.
2. Bruchas M.R., Xu M., Chavkin C. Repeated swim stress induces kappa opioid-mediated activation of extracellular signal-regulated kinase 1/2. Neuroreport 2008, 19:1417-1422.
3. Burstein S.R., Williams T.J., Lane D.A., Knudsen M.G., Pickel V.M., McEwen B.S., Waters E.M., Milner T.A. The influences of reproductive status and acute stress on the levels of phosphorylated delta opioid receptor immunoreactivity in rat hippocampus. Brain Res. 2013, 1518:71-81.
4. Carroll M.E., Lynch W.J., Roth M.E., Morgan A.D., Cosgrove K.P. Sex and estrogen influence drug abuse. Trends Pharmacol. Sci. 2004, 25:273-279.
5. Chang P.C., Aicher S.A., Drake C.T. Kappa opioid receptors in rat spinal cord vary across the estrous cycle. Brain Res. 2000, 861:168-172.
6. Commons K.G., Milner T.A. Ultrastructural heterogeneity of enkephalin-containing neurons in the rat hippocampal formation. J. Comp. Neurol. 1995, 358:324-342.
7. Day M., Sung A., Logue S., Bowlby M., Arias R. Beta estrogen receptor knockout (BERKO) mice present attenuated hippocampal CA1 long-term potentiation and related memory deficits in contextual fear conditioning. Behav. Brain Res. 2005, 164:128-131.
8. Foy M.R. Ovarian hormones, aging and stress on hippocampal synaptic plasticity. Neurobiol. Learn. Mem. 2011, 95:134-144.
9. Fugger H.N., Foster T.C., Gustafsson J.Å., Rissman E.F. Novel effects of estradiol and estrogen receptor α and β on cognitive function. Brain Res. 2000, 883:258-264.
10. Gall C. Seizures induce dramatic and distinctly different changes in enkephalin, dynorphin, and CCK immunoreactivities in mouse hippocampal mossy fibers. J. Neurosci. 1988, 8:1852-1862.
11. Gonzales K.L., Chapleau J.D., Pierce J.P., Kelter D.T., Williams T.J., Torres-Reveron A., McEwen B.S., Waters E.M., Milner T.A. The influences of reproductive status and acute stress on the levels of phosphorylated mu opioid recetpor immunoreactivity in rat hippocampus. Front. Neuroendocrinol. 2011, 2:1-10.
12. Han X., Aenlle K.K., Bean L.A., Rani A., Semple-Rowland S.L., Kumar A., Foster T.C. Role of estrogen receptor alpha and beta in preserving hippocampal function during aging. J. Neurosci. 2013, 33:2671-2683.
13. Harte-Hargrove L.C., MacLusky N.J., Scharfman H.E. Brain-derived neurotrophic factor-estrogen interactions in the hippocampal mossy fiber pathway: implications for normal brain function and disease. Neuroscience 2013, 239:46-66.
14. Kobayashi K. Targeting the hippocampal mossy fiber synapse for the treatment of psychiatric disorders. Mol. Neurobiol. 2009, 39:24-36.
15. Ledoux V.A., Smejkalova T., May R.M., Cooke B.M., Woolley C.S. Estradiol facilitates the release of neuropeptide Y to suppress hippocampus-dependent seizures. J. Neurosci. 2009, 29:1457-1468.
16. Lee S.H., Kim K.R., Ryu S.Y., Son S., Hong H.S., Mook-Jung I., Lee S.H., Ho W.K. Impaired short-term plasticity in mossy fiber synapses caused by mitochondrial dysfunction of dentate granule cells is the earliest synaptic deficit in a mouse model of Alzheimer's disease. J. Neurosci. 2012, 32:5953-5963.
17. Luo A.H., Tahsili-Fahadan P., Wise R.A., Lupica C.R., Aston-Jones G. Linking context with reward: a functional circuit from hippocampal CA3 to ventral tegmental area. Science 2011, 333:353-357.
18. McEwen B.S. Stress and hippocampal plasticity. Annu. Rev. Neurosci. 1999, 22:105-122.
19. Meilandt W.J., Yu G.Q., Chin J., Roberson E.D., Palop J.J., Wu T., Scearce-Levie K., Mucke L. Enkephalin elevations contribute to neuronal and behavioral impairments in a transgenic mouse model of Alzheimer's disease. J. Neurosci. 2008, 28:5007-5017.
20. Milner T.A., Ayoola K., Drake C.T., Herrick S.P., Tabori N.E., McEwen B.S., Warrier S., Alves S.E. Ultrastructural localization of estrogen receptor beta immunoreactivity in the rat hippocampal formation. J. Comp. Neurol. 2005, 491:81-95.
21. Milner T.A., McEwen B.S., Hayashi S., Li C.J., Reagan L.P., Alves S.E. Ultrastructural evidence that hippocampal alpha estrogen receptors are located at extranuclear sites. J. Comp. Neurol. 2001, 429:355-371.
22. Milner T.A., Pickel V.M., Reis D.J. Ultrastructural basis for interactions between central opioids and catecholamines: I. Rostral ventrolateral medulla. J. Neurosci. 1989, 9:2114-2130.
23. Milner T.A., Waters E.M., Robinson D.C., Pierce J.P. Degenerating processes identified by electron microscpic immunocytochemical methods. Neurodegeneration, Methods and Protocols 2011, 23-59. Springer, New York. G. Manfredi, H. Kawamata (Eds.).
24. Mitterling K.L., Spencer J.L., Dziedzic N., Shenoy S., McCarthy K., Waters E.M., McEwen B.S., Milner T.A. Cellular and subcellular localization of estrogen and progestin receptor immunoreactivities in the mouse hippocampus. J. Comp. Neurol. 2010, 518:2729-2743.
25. Nestler E.J. Molecular basis of long-term plasticity underlying addiction. Nat. Rev. Neurosci. 2001, 2:119-128.
26. Nicoll R.A., Schmitz D. Synaptic plasticity at hippocampal mossy fibre synapses. Nat. Rev. Neurosci. 2005, 6:863-876.
27. Pallud J., Haussler U., Langlois M., Hamelin S., Devaux B., Deransart C., Depaulis A. Dentate gyrus and hilus transection blocks seizure propagation and granule cell dispersion in a mouse model for mesial temporal lobe epilepsy. Hippocampus 2011, 21:334-343.
28. Pierce J.P., Kurucz O., Milner T.A. The morphometry of a peptidergic transmitter system before and after seizure. I. Dynorphin B-like immunoreactivity in the hippocampal mossy fiber system. Hippocampus 1999, 9:255-276.
29. Rissman E.F., Heck A.L., Leonard J.E., Shupnik M.A., Gustafsson J.A. Disruption of estrogen receptor beta gene impairs spatial learning in female mice. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:3996-4001.
30. Smith S.S., Woolley C.S. Cellular and molecular effects of steroid hormones on CNS excitability. Cleve. Clin. J. Med. 2004, 71(Suppl. 2):S4-S10.
31. Spencer J.L., Waters E.M., Romeo R.D., Wood G.E., Milner T.A., McEwen B.S. Uncovering the mechanisms of estrogen effects on hippocampal function. Front. Neuroendocrinol. 2008, 29:219-237.
32. Spencer-Segal J.L., Tsuda M.C., Mattei L., Waters E.M., Romeo R.D., Milner T.A., McEwen B.S., Ogawa S. Estradiol acts via estrogen receptors alpha and beta on pathways important for synaptic plasticity in the mouse hippocampal formation. Neuroscience 2012, 202:131-146.
33. Spencer-Segal J.L., Waters E.M., Bath K.G., Chao M.V., McEwen B.S., Milner T.A. Distribution of phosphorylated TrkB receptor in the mouse hippocampal formation depends on sex and estrous cycle stage. J. Neurosci. 2011, 31:6780-6790.
34. Svingos A.L., Colago E.E.O., Pickel V.M. Cellular sites for dynorphin activation of kappa-opioid receptors in the rat nucleus accumbens shell. J. Neurosci. 1999, 19:1804-1813.
35. Torres-Reveron A., Khalid S., Williams T.J., Waters E.M., Drake C.T., McEwen B.S., Milner T.A. Ovarian steroids modulate leu-enkephalin levels and target leu-enkephalinergic profiles in the female hippocampal mossy fiber pathway. Brain Res. 2008, 1232(70-84):70-84.
36. Torres-Reveron A., Khalid S., Williams T.J., Waters E.M., Jacome L., Luine V.N., Drake C.T., McEwen B.S., Milner T.A. Hippocampal dynorphin immunoreactivity increases in response to gonadal steroids and is positioned for direct modulation by ovarian steroid receptors. Neuroscience 2009, 159:204-216.
37. Weisskopf M.G., Zalutsky R.A., Nicoll R.A. The opioid peptide dynorphin mediates heterosynaptic depression of hippocampal mossy fibre synapses and modulates long-term potentiation. Nature 1993, 362:423-427.