Ultrastructural localization of extranuclear progestin receptors in the rat hippocampal formation

Journal of Comparative Neurology

Volumn 511, Issue 1, 2008, Pages 34-46

  Waters, Elizabeth M ^a   Torres Reveron, Annelyn ^b   McEwen, Bruce S ^a   Milner, Teresa A ^a,b  

^a ROCKEFELLER UNIVERSITY   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Estrogen inducible progestin receptors; Extranuclear; Progesterone

Indexed keywords

ESTROGEN; MESSENGER RNA; PROGESTERONE RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL LABELING; CELL STRUCTURE; CONTROLLED STUDY; DENDRITE; DENDRITIC SPINE; DENTATE GYRUS; EXCITATORY POSTSYNAPTIC POTENTIAL; FEMALE; HIPPOCAMPUS; HORMONAL REGULATION; IMMUNOREACTIVITY; MICROSCOPY; NERVE CONDUCTION; NEUROMUSCULAR SYNAPSE; NONHUMAN; OVARIECTOMY; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; ULTRASTRUCTURE; ANIMAL; CHEMISTRY; GLIA; HUMAN; SPRAGUE DAWLEY RAT; SYNAPSE; SYNAPTOSOME;

ANIMALS; DENDRITES; FEMALE; HIPPOCAMPUS; HUMANS; NEUROGLIA; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, PROGESTERONE; SYNAPSES;

EID: 56149116410     PISSN: 00219967     EISSN: 10969861     Source Type: Journal    
DOI: 10.1002/cne.21826     Document Type: Article

References (80)

1. Adams MM, Fink SF, Janssen WGM, Shah RA, Morrison, HJ. 2004. Estrogen modulates synaptic N-methyl-D-asparatate receptor subunit distribution in the aged hippocampus. J Comp Neurol 474:419-426.
2. Aoki C, Miko I, Oviedo H, Mikeladze-Dvali T, Alexandre L, Sweeney N, Bredt DS. 2001. Electron microscopic immunocytochemical detection of PSD-95, PSD-93, SAP-102, and SAP-97 at postsynaptic, presynaptic, and nonsynaptic sites of adult and neonatal rat visual cortex. Synapse 40:239-257.
3. Ballare C, Vallejo G, Vicent GP, Saragueta P, Beato M. 2006. Progesterone signaling in breast and endometrium. J Steroid Biochem Mol Biol 102:2-10.
4. Camacho-Arroyo I, Guerra-Araiza C, Cerbón MA. 1998. Progesterone receptor isoforms are differentially regulated by sex steroids in the rat forebrain. Neuroreport 9:3993-3996.
5. Cammarata PR, Chu S, Moor A, Wang Z, Yang SH, Simpkins JW. 2004. Subcellular distribution of native estrogen receptor alpha and beta subtypes in cultured human lens epithelial cells. Exp Eye Res 78:861-871.
6. Carlin RK, Grab DJ, Cohen RS, Siekevitz P. 1980. Isolation and characterization of postsynaptic densities from various brain regions: enrichment of different types of postsynaptic densities. J Cell Biol 86:831-845.
7. Chan J, Aoki C, Pickel VM. 1990. Optimization of differential immunogold-silver and peroxidase labeling with maintenance of ultrastructure in brain sections before plastic embedding. J Neurosci Methods 33:113-127.
8. De Nicola AF, Gonzalez SL, Labombarda F, Deniselle MC, Garay L, Guennoun R, Schumacher M. 2006. Progesterone treatment of spinal cord injury: effects on receptors, neurotrophins, and myelination. J Mol Neurosci 28:3-15.
9. Djebaili M, Hoffman SW, Stein DG. 2004. Allopregnanolone and progesterone decrease cell death and cognitive deficits after a contusion of the rat pre-frontal cortex. Neuroscience 123:349-359.
10. Drake CT, Chavlin C, Milner TA. 2007. Opioid systems in the dentate gyrus. Prog Brain Res 163:245-263.
11. Edwards HE, Epps T, Carlen PL, N JM. 2000. Progestin receptors mediate progesterone suppression of epileptiform activity in tetanized hippocampal slices in vitro. Neuroscience 101:895-906.
12. Fitzpatrick SL, Berrodin TJ, Jenkins SF, Sindoni DM, Deecher DC, Frail DE. 1999. Effect of estrogen agonists and antagonists on induction of progesterone receptor in a rat hypothalamic cell line. Endocrinology 140:3928-3937.
13. Foy MR, Xu J, Xie X, Brinton RD, Thompson RF, Berger TW. 1999. 17Beta-estradiol enhances NMDA recceptor-mediated EPSPs and long-term potentiation. J Neurophysiol 81:925-929.
14. Frye CA, Rhodes ME. 2005. Estrogen-priming can enhance progesterone's anti-seizure effects in part by increasing hippocampal levels of allopregnanolone. Pharmacol Biochem Behav 81:907-916.
15. Gazzaley AH, Weiland NG, McEwen BS, Morrison JH. 1996. Differential regulation of NMDAR1 mRNA and protein by estradiol in the rat hippocampus. J Neurosci 16:6830-6838.
16. Garcia-Segura LM, Melcangi RC. 2006. Steroids and glial cell function. Glia 54:485-498.
17. Ghoumari AM, Dusart I, El-Etr M, Tronche F, Sotelo C, Schumacher M, Baulieu EE. 2003. Mifepristone (RU486) protects Purkinje cells from cell death in organotypic slice cultures of postnatal rat and mouse cerebellum. Proc Natl Acad Sci U S A 100:7953-7958.
18. Ghoumari AM, Wehrle R, Sotelo C, Dusart I. 2005. Bcl-2 protection of axotomized Purkinje cells in organotypic culture is age dependent and not associated with an enhancement of axonal regeneration. Prog Brain Res 148:37-44.
19. Giangrande PH, McDonnell DP. 1999. The A and B isoforms of the human progesterone receptor: two functionally different transcription factors encoded by a single gene. Rec Prog Horm Res 54:291-313; discussion 313-294.
20. Giangrande PH, Pollio G, McDonnell DP. 1997. Mapping and characterization of the functional domains responsible for the differential activity of the A and B isoforms of the human progesterone receptor. J Biol Chem 272:32889-32900.
21. Guerra-Araiza C, Cerbón MA, Morimoto S, Camacho-Arroyo I. 2000. Progesterone receptor isoforms expression pattern in the rat brain during the estrous cycle. Life Sci 66:1743-1752.
22. Guerra-Araiza C, Coyoy-Salgado A, Camacho-Arroyo I. 2002. Sex differences in the regulation of progesterone receptor isoforms expression in the rat brain. Brain Res Bull 59:105-109.
23. Guerra-Araiza C, Villamar-Cruz O, Gonzalez-Arenas A, Chavira R, Camacho-Arroyo I. 2003. Changes in progesterone receptor isoforms content in the rat brain during the oestrous cycle and after oestradiol and progesterone treatments. J Neuroendocrinol 15:984-990.
24. Hammes SR, Levin ER. 2007. Extranuclear steroid receptors: nature and actions. Endocrine Rev 28:726-741.
25. Hanekamp EE, Kuhne LM, Grootegoed JA, Burger CW, Blok LJ. 2004. Progesterone receptor A and B expression and progestagen treatment in growth and spread of endometrail cancer cells in nude mice. Endocrine Rel Cancer 11:831-841.
26. Haywood SA, Simonian SX, van der Beek EM, Bicknell RJ, Herbison AE. 1999. Fluctuating estrogen and progesterone receptor expression in brainstem norepinephrine neurons through the rat estrous cycle. Endocrinology 140:3255-3263.
27. Herrick SP, Waters EM, Drake CT, McEwen BS, Milner TA. 2006. Extranuclear estrogen receptor beta immunoreactivity is on doublecortincontaining cells in the adult and neonatal rat dentate gyrus. Brain Res 1121:46-58.
28. Hsu SM, Raine L, Fanger H. 1981. Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J Histochem Cytochem 29: 577-580.
29. Jung-Testas I, Renoir M, Bugnard H, Greene GL, Baulieu EE. 1992. Demonstration of steroid hormone receptors and steroid action in primary cultures of rat glial cells. J Steroid Biochem Mol Biol 41:621-631.
30. Kastner P, Krust A, Turcotte B, Stropp U, Tora L, Gronemeyer H, Chambon P. 1990. Two distinct estrogen-regulated promoters generate transcripts encoding the two functionally different human progesterone receptor forms A and B. EMBO J 9:1603-1614.
31. Kipp M, Karakaya S, Johann S, Kampmann E, Mey J, Beyer C. 2007. Oestrogen and progesterone reduce lipopolysaccharide-induced expression of tumour necrosis factor-alpha and interleukin-18 in midbrain astrocytes. J Neuroendocrinology 19:819-822.
32. Kurita T, Young P, Brody JR, Lydon JP, O'Malley BW, Cunha GR. 1998. Stromal progesterone receptors mediate the inhibitory effects of progesterone on estrogen-induced uterine epithelial cell deoxyribonucleic acid synthesis. Endocrinology 139:4708-4713.
33. Lacroix-Fralish ML, Tawkif VL, Nutlie-McMenemy N, Harris BT, Deleo JA. 2006. Differential regulation of neuregulin 1 expression by progesterone in astrocytes and neurons. Neuron Glia Biol. 2:227-34.
34. Lange CA, Gioeli D, Hammes SR, Marker PC. 2007. Integration of rapid signaling events with steroid hormone receptor action in breast and prostate cancer. Annu Rev Physiol 69:171-199.
35. Levin ER. 2005. Integration of the extranuclear and nuclear actions of estrogen. Mol Endocrinol 19:1951-1959.
36. MacLusky NJ, McEwen BS. 1978. Oestrogen modulates progestin receptor concentrations in some rat brain regions but not in others. Nature 274:276-278.
37. MacLusky NJ, McEwen BS. 1980. Progestin receptors in rat brain: distribution and properties of cytoplasmic progestin-binding sites. Endocrinology 106:192-202.
38. Milner TA, McEwen BS, Hayashi S, Li CJ, Reagan LP, Alves SE. 2001. Ultrastructural evidence that hippocampal alpha estrogen receptors are located at extranuclear sites. J Comp Neurol 429:355-371.
39. Milner TA, Ayoola K, Drake CT, Herrick SP, Tabori NE, McEwen BS, Warrier S, Alves SE. 2005. Ultrastructural localization of estrogen receptor beta immunoreactivity in the rat hippocampal formation. J Comp Neurol 491:81-95.
40. Milner TA, Mitterling K, Iadecola C, Waters EM. 2007. Ultrastructural localization of extranuclear progestin receptors relative to C1 neurons in the rostral ventrolateral medulla. Neurosci Lett (in press).
41. Nilsen J, Brinton RD. 2002. Impact of progestins on estradiol potentiation of the glutamate calcium response. Neuroreport 13:825-830.
42. Nishida H, Okabe S. 2007. Direct astrocytic contacts regulate local maturation of dendritic spines. J Neurosci 27:331-340.
43. O'Connor CA, Cernak I, Johnson F, Vink R. 2007. Effects of progesterone on neurologic and morphologic outcome following diffuse traumatic brain injury in rats. Exp Neurol 205:145-153.
44. Parsons B, Rainbow TC, MacLusky NJ, McEwen BS. 1982. Progestin receptor levels in rat hypothalamic and limbic nuclei. J Neurosci 2:1446-1452.
45. Perea G, Araque A. 2007. Astrocytes potentiate transmitter release at single hippocampal synapses. Science 317:1083-1086.
46. Peters A, Palay SL, Webster HD. 1991. The fine structure of the nervous system. New York: Oxford University Press.
47. Quadros PS, Pfau JL, Goldstein AY, De Vries GJ, Wagner CK. 2002. Sex differences in progesterone receptor expression: a potential mechanism for estradiol-mediated sexual differentiation. Endocrinology 143:3727-3739.
48. Quadros PS, Pfau JL, Wagner CK. 2007. Distribution of progesterone receptor immunoreactivity in the fetal and neonatal rat forebrain. J Comp Neurol 504:42-56.
49. Robertson CL, Puskar A, Hoffman GE, Murphy AZ, Saraswati M, Fiskum G. 2006. Physiologic progesterone reduces mitochondrial dysfunction and hippocampal cell loss after traumatic brain injury in female rats. Exp Neurol 197:235-243.
50. Rosario ER, Ramsden M, Pike CJ. 2006. Progestins inhibit the neuroprotective effects of estrogen in rat hippocampus. Brain Res 1099:206-210.
51. Sandstrom NJ, Williams CL. 2001. Memory retention is modulated by acute estradiol and progesterone replacement. Behav Neurosci 115: 384-393.
52. Sayeed I, Wali B, Stein DG. 2007. Progesterone inhibits ischemic brain injury in a rat model of permanent middle cerebral artery occlusion. Restor Neurol Neurosci 25:151-159.
53. Scharfman HE, Mercurio TC, Goodman JH, Wilson MA, MacLusky NJ. 2003. Hippocampal excitability increases during the estrous cycle in the rat: a potential role for brain-derived neurotrophic factor. J Neurosci 23:11641-11652.
54. Schumacher M, Guennoun R, Ghoumari A, Massaad C, Robert F, El-Etr M, Akwa Y, Rajkowski K, Baulieu EE. 2007. Novel perspectives for progesterone in hormone replacement therapy, with special reference to the nervous system. Endocrine Rev 28:387-439.
55. Sierra A, Gottfried-Blackmore A, Milner TA, McEwen BS, Bulloch K. 2008. Steroid hormone receptor expression and function in microglia. Glia (in press).
56. Sinchak K, Micevych PE. 2001. Progesterone blockade of estrogen activation of μ-opioid receptors regulates reproductive behavior. J Neurosci 21:5723-5729.
57. Smith CC, McMahon LL. 2005. 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 25:2650-2659.
58. Smith CC, McMahon LL. 2006. Estrogen-induced increase in the magnitude of long-term potentiation is prevented by blocking NR2B-containing receptors. J Neurosci 26:8517-8522.
59. Stein DG. 2007. Progesterone exerts neuroprotective effects after brain injury. Brain Res Rev (in press).
60. Sternberger LA. 1979. Immunohistchemistry. New York: Wiley.
61. Sul JY, Orosz G, Givens RS, Haydon PG. 2004. Astrocytic connectivity in the hippocampus. Neuron Glia Biol 1:3-11.
62. Swanson LW. 2000. Brain maps: structure of the rat brain. San Diego: Academic Press.
63. Tabori NE, Stewart LS, Znamensky V, Romeo RD, Alves SE, McEwen BS, Milner TA. 2005. Ultrastructural evidence that androgen receptors are located at extranuclear sites in the rat hippocampal formation. Neuroscience 130:151-163.
64. Tibbetts TA, DeMayo F, Rich S, Conneely OM, O'Malley BW. 1999. Progesterone receptors in the thymus are required for thymic involution during pregnancy and for normal fertility. Proc Natl Acad Sci U S A 96:12021-12026.
65. Tournell CE, Bergstrom RA, Ferreira A. 2006. Progesterone-induced agrin expression in astrocytes modulates glia-neuron interactions leading to synapse formation. Neuroscience 141:1327-1338.
66. Traish AM, Wotiz HH. 1990. Monoclonal and polyclonal antibodies to human progesterone receptor peptide-(533-547) recognize a specific site in unactivated (8S) and activated (4S) progesterone receptor and distinguish between intact and proteolyzed receptors. Endocrinology 127:1167-1175.
67. Turner CD, Bagnara JT. 1971. General endocrinology. Philadelphia: W.B. Saunders.
68. Venkatesan C, Song XZ, Go CG, Kurose H, Aoki C. 1996. Cellular and subcellular distribution of alpha 2A-adrenergic receptors in the visual cortex of neonatal and adult rats. J Comp Neurol 365:79-95.
69. Villamar-Cruz O, Manjarrez-Marmolejo J, Alvarado R, Camacho-Arroyo I. 2006. Regulation of the content of progesterone and estrogen receptors, and their cofactors SRC-1 and SMRT by the 26S proteasome in the rat brain during the estrous cycle. Brain Res Bull 69:276 -281.
70. Villoslada P, Genain CP. 2004. Role of nerve growth factor and other trophic factors in brain inflammation. Prog Brain Res 146:403-414.
71. Wang G, Drake CT, Rozenblit M, Zhou P, Alves SE, Herrick SP, Hayashi S, Warrier S, Iadecola C, Milner TA. 2006. Evidence that estrogen directly and indirectly modulates C1 adrenergic bulbospinal neurons in the rostral ventrolateral medulla. Brain Res 1094:163-178.
72. Williams TJ, Torres-Reveron A, Gore AC, McEwen BS, Milner TA. 2007. Estrogen differentially affects leu-enkephalin and dynorphin immunoreactivity in the dorsal hippocampus of young, mature and old female rats. Annu Meeting Soc Neurosci 625.3.
73. Woolley CS. 2007. Acute effects of estrogen on neuronal physiology. Annu Rev Pharmacol Toxicol 47:657-680.
74. Woolley CS, McEwen BS. 1993. Roles of estradiol and progesterone in regulation of hippocampal dendritic spine density during the estrous cycle in the rat. J Comp Neurol 336:293-306.
75. Woolley CS, McEwen BS. 1994. Estradiol regulates hippocampal dendritic spine density via an N-methyl-D-aspartate receptor-dependent mechanism. J Neurosci 14:7680-7687.
76. Woolley CS, Gould E, Frankfurt M, McEwen BS. 1990. Naturally occurring fluctuation in dendritic spine density on adult hippocampal pyramidal neurons. J Neurosci 10:4035-4039.
77. Woolley CS, Weiland NG, McEwen BS, Schwartzkroin PA. 1997. Estradiol increases the sensitivity of hippocampal CA1 pyramidal cells to NMDA receptor-mediated synaptic input: correlation with dendritic spine density. J Neurosci 17:1848-1859.
78. Yang SH, Liu R, Perez EJ, Wen Y, Stevens SM Jr, Valencia T, Brun-Zinkernagel AM, Prokai L, Will Y, Dykens J, Koulen P, Simpkins JW. 2004. Mitochondrial localization of estrogen receptor beta. Proc Natl Acad Sci U S A 101:4130-4135.
79. Yuste R, Bonhoeffer T. 2001. Morphological changes in dendritic spines associated with long-term synaptic plasticity. Annu Rev Neurosci 24: 1071-1089.
80. Zaborszky L, Wouterlood, FG, Lanciego JL, editors. 2006. Neuroanatomical tract-tracing 3: molecules, neurones, systems. New York: Springer.