Ovarian steroids alter mu opioid receptor trafficking in hippocampal parvalbumin GABAergic interneurons

Experimental Neurology

Volumn 219, Issue 1, 2009, Pages 319-327

  Torres Reveron, Annelyn ^a   Williams, Tanya J ^a   Chapleau, Jeanette D ^a   Waters, Elizabeth M ^b   McEwen, Bruce S ^b   Drake, Carrie T ^a   Milner, Teresa A ^a,b  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Endogenous opioids; Estrogen; Estrous cycle; Hippocampus; Ovariectomy

Indexed keywords

ESTRADIOL BENZOATE; ESTROGEN; ESTROGEN DERIVATIVE; MU OPIATE RECEPTOR; OPIATE DERIVATIVE; PARVALBUMIN; SEX HORMONE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL LABELING; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DENDRITE; DENTATE GYRUS; DIESTRUS; ESTRUS; FEMALE; GABAERGIC SYSTEM; HIPPOCAMPUS; HORMONE ACTION; INTERNEURON; MALE; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE; NEUROMODULATION; NONHUMAN; PERIKARYON; PRIORITY JOURNAL; PROTEIN TRANSPORT; RAT;

ANIMALS; CELL MEMBRANE; DENDRITES; DENTATE GYRUS; ENDOCYTOSIS; ESTRADIOL; ESTROUS CYCLE; FEMALE; GAMMA-AMINOBUTYRIC ACID; GONADAL STEROID HORMONES; IMMUNOHISTOCHEMISTRY; INTERNEURONS; MICROSCOPY, IMMUNOELECTRON; OPIOID PEPTIDES; OVARIECTOMY; OVARY; PARVALBUMINS; PROTEIN TRANSPORT; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, OPIOID, MU;

EID: 68549109384     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2009.06.001     Document Type: Article

References (72)

1. Abbadie C., Pan Y.X., Drake C.T., and Pasternak G.W. Comparative immunohistochemical distributions of carboxy terminus epitopes from the mu-opioid receptor splice variants MOR-1D, MOR-1 and MOR-1C in the mouse and rat CNS. Neuroscience 100 1 (2000) 141-153
2. Akaishi T., Saito H., Ito Y., Ishige K., and Ikegaya Y. Morphine augments excitatory synaptic transmission in the dentate gyrus through GABAergic disinhibition. Neuroscience Research 38 4 (2000) 357-363
3. Arttamangkul S., Quillinan N., Low M.J., von Z.M., Pintar J., and Williams J.T. Differential activation and trafficking of micro-opioid receptors in brain slices. Molec. Pharmacol. 74 4 (2008) 972-979
4. Arvidsson U., Riedl M., Chakrabarti S., Lee J.H., Nakano A.H., Dado R.J., Loh H.H., Law P.Y., Wessendorf M.W., and Elde R. Distribution and targeting of a mu-opioid receptor (MOR1) in brain and spinal cord. J. Neurosci. 15 5 Pt 1 (1995) 3328-3341
5. Backstrom T. Epileptic seizures in women related to plasma estrogen and progesterone during the menstrual cycle. Acta Neurol. Scand. 54 4 (1976) 321-347
6. Becker J.B., and Hu M. Sex differences in drug abuse. Front Neuroendocrinol. 29 1 (2008) 36-47
7. Belanger A., Cusan L., Caron S., Barden N., and Dupont A. Ovarian progestins, androgens and estrogen throughout the 4-day estrous cycle in the rat. Biol. Reprod. 24 3 (1981) 591-596
8. Berke J.D., and Hyman S.E. Addiction, dopamine, and the molecular mechanisms of memory. Neuron 25 3 (2000) 515-532
9. Blurton-Jones M., and Tuszynski M.H. Estrogen receptor-beta colocalizes extensively with parvalbumin-labeled inhibitory neurons in the cortex, amygdala, basal forebrain, and hippocampal formation of intact and ovariectomized adult rats. J.Comp Neurol. 452 3 (2002) 276-287
10. Boudin H., Pélaprat D., Rostène W., Pickel V.M., and Beaudet A. Correlative ultrastructural distribution of neurotensin receptor proteins and binding sites in the rat substantia nigra. J. Neurosci. 18 20 (1998) 8473-8484
11. Bramham C.R. Opioid receptor dependent long-term potentiation: peptidergic regulation of synaptic plasticity in the hippocampus. Neurochem. Int. 20 (1992) 441-455
12. Bramham C.R., and Sarvey J.M. Endogenous activation of μ and δ-1 opioid receptors is required for long-term potentiation induction in the lateral perforant path: dependence on GABAergic inhibition. J. Neurosci. 16 (1996) 8123-8131
13. Celio M.R., Baier W., Scharer L., de Viragh P.A., and Gerday C. Monoclonal antibodies directed against the calcium binding protein parvalbumin. Cell Calcium 9 2 (1988) 81-86
14. Chan J., Aoki C., and Pickel V.M. Optimization of differential immunogold-silver and peroxidase labeling with maintenance of ultrastructure in brain sections before plastic embedding. J. Neurosci. Methods 33 (1990) 113-127
15. Chavkin C., Neumaier J.F., and Swearengen E. Opioid receptor mechanisms in the rat hippocampus. Natl. Inst. Drug Abuse Res. Monogr. Ser. 82 (1988) 94-117
16. Commons K.G., and Milner T.A. The ultrastructural relationships between leu-enkephalin and GABA containing neurons differ within the hippocampal formation. Brain Res. 724 (1996) 1-15
17. Cooke B.M., and Woolley C.S. Gonadal hormone modulation of dendrites in the mammalian CNS. J. Neurobiol. 64 1 (2005) 34-46
18. Cyr M., Ghribi O., Thibault C., Morissette M., Landry M., and Di Paolo T. Ovarian steroids and selective estrogen receptor modulators activity on rat brain NMDA and AMPA receptors. Brain Res. Brain Res. Rev. 37 1-3 (2001) 153-161
19. Derrick B.E., Rodriguez S.B., Lieberman D.N., and Martinez J.L. Mu opioid receptors are associated with the induction of hippocampal mossy fiber long-term potentiation. J. Pharmacol. Exper. Ther. 263 (1992) 725-733
20. Drake C.T., and Milner T.A. Mu opioid receptors are in somatodendritic and axonal compartments of GABAergic neurons in rat hippocampal formation. Brain Res. 849 1-2 (1999) 203-215
21. Drake C.T., and Milner T.A. Mu opioid receptors are extensively co-localized with parvalbumin, but not somatostatin, in the dentate gyrus. Neurosci. Lett. 403 1-2 (2006) 176-180
22. Drake C.T., Chang P.C., Harris J.A., and Milner T.A. Neurons with mu opioid receptors interact indirectly with enkephalin-containing neurons in the rat dentate gyrus. Exp. Neurol. 176 1 (2002) 254-261
23. Drake C.T., Aicher S.A., Montalmant F.L., and Milner T.A. Redistribution of mu-opioid receptors in C1 adrenergic neurons following chronic administration of morphine. Exp. Neurol. 196 (2005) 365-372
24. Drake C.T., Chavkin C., and Milner T.A. Opioid systems in the dentate gyrus. Prog. Brain Res. 163C (2007) 245-814
25. Dumas T.C., Powers E.C., Tarapore P.E., and Sapolsky R.M. Overexpression of calbindin D(28k) in dentate gyrus granule cells alters mossy fiber presynaptic function and impairs hippocampal-dependent memory. Hippocampus 14 6 (2004) 701-709
26. Eddy C.A. Experimental surgery of the genitalia system. In: Gay W.I., and Heavner J.E. (Eds). Methods of Animal Experimentation (1986), Academic Press, Orlando, FL 191
27. Gerrits M.A., Lesscher H.B., and van Ree J.M. Drug dependence and the endogenous opioid system. Eur. Neuropsychopharmacol. 13 6 (2003) 424-434
28. Herzog A.G., Harden C.L., Liporace J., Pennell P., Schomer D.L., Sperling M., Fowler K., Nikolov B., Shuman S., and Newman M. Frequency of catamenial seizure exacerbation in women with localization-related epilepsy. Ann. Neurol 56 3 (2004) 431-434
29. Hruby J., and Agnes R.S. Conformation-activity relationships of opioid peptides with selective activities at opioid receptors. Biopolymers 51 6 (1999) 391-410
30. Hsu S.M., Raine L., and Fanger H. Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J. Histochem. Cytochem 29 (1981) 557-580
31. Ishihara K., Mitsuno K., Ishikawa M., and Sasa M. Behavioral LTP during learning in rat hippocampal CA3. Behav. Brain Res. 83 (1997) 235-238
32. Janecka A., Fichna J., and Janecki T. Opioid receptors and their ligands. Curr. Top Med. Chem. 4 1 (2004) 1-17
33. Kim J.S., Kim H.Y., Kim J.H., Shin H.K., Lee S.H., Lee Y.S., and Son H. Enhancement of rat hippocampal long-term potentiation by 17 beta-estradiol involves mitogen-activated protein kinase-dependent and -independent components. Neurosci. Lett. 332 1 (2002) 65-69
34. Kreek M.J., Schluger J., Borg L., Gunduz M., and Ho A. Dynorphin A1-13 causes elevation of serum levels of prolactin through an opioid receptor mechanism in humans: gender differences and implications for modulation of dopaminergic tone in the treatment of addictions. J. Pharmacol. Exp. Ther. 288 1 (1999) 260-269
35. Leranth C., and Pickel V.M. Electron microscopic preembedding double-labeling methods. In: Heimer L., and Zaborszky L. (Eds). Neuroanatomical Tract-Tracing Methods 2 (1989), Plenum Press, New York 129-172
36. Lujan R., Nusser Z., Roberts J.D., Shigemoto R., and Somogyi P. Perisynaptic location of metabotropic glutamate receptors mGluR1 and mGluR5 on dendrites and dendritic spines in the rat hippocampus. Eur. J. Neurosci. 8 7 (1996) 1488-1500
37. Majewska M.D., Harrison N.L., Schwartz R.D., Barker J.L., and Paul S.M. Steroid hormone metabolites are barbiturate-like modulators of the GABA receptor. Science 232 4753 (1986) 1004-1007
38. Mansour A., Khachaturian H., Lewis M.E., Akil H., and Watson S.J. Anatomy of CNS opioid receptors. Trends Neurosci. 11 7 (1988) 308-314
39. McEwen B.S. Invited review: estrogens effects on the brain: multiple sites and molecular mechanisms. J. Appl. Physiol 91 6 (2001) 2785-2801
40. McLaughlin J.P., Marton-Popovici M., and Chavkin C. Kappa opioid receptor antagonism and prodynorphin gene disruption block stress-induced behavioral responses. J. Neurosci. 23 13 (2003) 5674-5683
41. Micevych P.E., Rissman E.F., Gustafsson J.A., and Sinchak K. Estrogen receptor-alpha is required for estrogen-induced mu-opioid receptor internalization. J. Neurosci. Res. 71 6 (2003) 802-810
42. Milner T.A., McEwen B.S., Hayashi S., Li C.J., Reagan L.P., and Alves S.E. Ultrastructural evidence that hippocampal alpha estrogen receptors are located at extranuclear sites. J. Compar. Neurol. 429 3 (2001) 355-371
43. Milner T.A., Ayoola K., Drake C.T., Herrick S.P., Tabori N.E., McEwen B.S., Warrier S., and Alves S.E. Ultrastructural localization of estrogen receptor beta immunoreactivity in the rat hippocampal formation. J. Comp. Neurol. 491 2 (2005) 81-95
44. Morris B.J., and Johnston H.M. A role for hippocampal opioids in long-term functional plasticity. Trends Neurosci. 18 (1995) 350-355
45. Nakamura N.H., and McEwen B.S. Changes in interneuronal phenotypes regulated by estradiol in the adult rat hippocampus: a potential role for neuropeptide Y. Neuroscience. 136 1 (2005) 357-369
46. Nestler E.J., Hyman S.E., and Malenka R.C. Neural Substrates of Drug Action (2001), McGraw-Hill Companies, Inc, New Yok 224
47. Paulsen O., and Moser E.I. A model of hippocampal memory encoding and retrieval: GABAergic control of synaptic plasticity. Trends Neurosci. 21 7 (1998) 273-278
48. Penovich P.E., and Helmers S. Catamenial epilepsy. Int. Rev. Neurobiol. 83 (2008) 79-90
49. Peters A., Palay S.L., and Webster H.d. The Fine Structure of the Nervous System, 3rd ed (1991), Oxford University Press, New York
50. Pierce J.P., Kurucz O., and Milner T.A. The morphometry of a peptidergic system before and after seizure. I. Dynorphin B-like immunoreactivity in the hippocampal mossy fiber system. Hippocampus 9 (1999) 255-276
51. Piva F., Limonta P., Dondi D., Pimpinelli F., Martini L., and Maggi R. Effects of steroids on the brain opioid system. J. Steroid Biochem. Molec. Biol. 53 1-6 (1995) 343-348
52. Plager M.D., and Vogt B.A. Mu- and delta-opioid receptor binding peaks and kappa-homogeneity in the molecular layers of rat hippocampal formation. Brain Res. 460 (1988) 150-154
53. Quinones-Jenab V., Jenab S., Ogawa S., Inturrisi C., and Pfaff D.W. Estrogen regulation of mu-opioid receptor mRNA in the forebrain of female rats. Brain Res. 47 1 (1997)
54. Sinchak K., and Micevych P.E. Progesterone blockade of estrogen activation of mu-opioid receptors regulates reproductive behavior. J. Neurosci. 21 15 (2001) 5723-5729
55. Slamberova R., Rimanoczy A., Schindler C.J., and Vathy I. Cortical and striatal mu-opioid receptors are altered by gonadal hormone treatment but not by prenatal morphine exposure in adult male and female rats. Brain Res. Bull. 62 1 (2003) 47-53
56. Smith C.C., and McMahon L.L. Estrogen-induced increase in the magnitude of long-term potentiation occurs only when the ratio of NMDA transmission to AMPA transmission is increased. J. Neurosci. 25 34 (2005) 7780-7791
57. Smith M.D., Jones L.S., and Wilson M.A. Sex differences in hippocampal slice excitability: role of testosterone. Neuroscience 109 3 (2002) 517-530
58. Swanson L.W. Brain Maps: Structure of the Rat Brain (1992), Elsevier, Amsterdam
59. Tanapat P., Hastings N.B., and Gould E. Ovarian steroids influence cell proliferation in the dentate gyrus of the adult female rat in a dose- and time-dependent manner. J. Comp. Neurol. 481 3 (2005) 252-265
60. Torres-Reveron A., Williams T.J., Prasad P., Drake C.T., and Milner T.A. Ovarian steroids affect the subcellular distribution of mu opioid receptors in parvalbumin interneurons of the dentate gyrus. Neuroscience Meeting Planner (2007), Society for Neuroscience, San Diego, CA (2007.Online 729.6)
61. Torres-Reveron A., Khalid S., Williams T.J., Waters E.M., Drake C.T., McEwen B., and Milner T.A. Ovarian steroids modulate leu-enkephalin levels and target leu-enkephalinergic profiles in the female hippocampal mossy fiber pathway. Brain Res. 1232 (2008) 70-84
62. Torres-Reveron A., Khalid S., Williams T.J., Waters E.M., Jacome L., Luine V.N., Drake C.T., McEwen B.S., and Milner T.A. Hippocampal dynorphin immunoreactivity increases in response to gonadal steroids and is positioned for direct modulation by ovarian steroid receptors. Neuroscience 159 1 (2009) 204-216
63. Towart L.A., Alves S.E., Znamensky V., and Hayashi S. Cholinergic terminals in rat hippocampal formation contain estrogen receptor a. Soc. Neurosci. Abstracts 28 (2002)
64. Turner C.D., and Bagnara J.T. General Endocrinology W.B (1971), Saunders, Philadelphia
65. Warren S.G., Humphreys A.G., Juraska J.M., and Greenough W.T. LTP varies across the estrous cycle: enhanced synaptic plasticity in proestrus rats. Brain Res. 703 (1995) 26-30
66. Wong M., and Moss R.L. Long-term and short-term electrophysiological effects of estrogen on the synaptic properties of hippocampal CA1 neurons. J. Neurosci. 12 (1992) 3217-3225
67. Woolley C.S. Estrogen-mediated structural and functional synaptic plasticity in the female rat hippocampus. Hormones Behav. 34 2 (1998) 140-148
68. Woolley C.S., and McEwen B.S. Estradiol regulates hippocampal dendritic spine density via an N-methyl-d-aspartate receptor-dependent mechanism. J. Neurosci. 14 (1994) 7680-7687
69. Woolley C.S., Gould E., Frankfurt M., and McEwen B.S. Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. J. Neurosci. 10 (1990) 4035-4039
70. Xie C.W., and Lewis D.V. Depression of LTP in rat dentate gyrus by naloxone is reversed by GABAA blockade. Brain Res. 688 (1995) 56-60
71. Xie C.W., Morrisett R.A., and Lewis D.V. Mu opioid receptor-mediated modulation of synaptic currents in dentate granule cells of rat hippocampus. J. Neurophysiol. 68 (1992) 1113-1120
72. Zurkovsky L., Brown S.L., Boyd S.E., Fell J.A., and Korol D.L. Estrogen modulates learning in female rats by acting directly at distinct memory systems. Neuroscience. 144 1 (2007) 26-37