Estradiol mediates dendritic spine plasticity in the nucleus accumbens core through activation of mGluR5

Brain Structure and Function

Volumn 220, Issue 4, 2015, Pages 2415-2422

  Peterson, Brittni M ^a   Mermelstein, Paul G ^a   Meisel, Robert L ^a  

^a UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Drug addiction; Estrogen; Medium spiny neuron; mGluR

Indexed keywords

2 METHYL 6 (PHENYLETHYNYL)PYRIDINE; ESTRADIOL; GLUTAMATE RECEPTOR 5; AMINO ACID RECEPTOR BLOCKING AGENT; ESTROGEN; METABOTROPIC RECEPTOR 5;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DENDRITIC SPINE; DENDRITIC SPINE PLASTICITY; FEMALE; HIPPOCAMPAL CA1 REGION; MOLECULAR MECHANICS; NERVE CELL PLASTICITY; NONHUMAN; NUCLEUS ACCUMBENS; NUCLEUS ACCUMBENS CORE; NUCLEUS ACCUMBENS SHELL; OVARIECTOMY; PRIORITY JOURNAL; RAT; ANIMAL; CYTOLOGY; DRUG EFFECTS; METABOLISM; SPRAGUE DAWLEY RAT;

RATTUS; RODENTIA;

ANIMALS; DENDRITIC SPINES; ESTRADIOL; ESTROGENS; EXCITATORY AMINO ACID ANTAGONISTS; FEMALE; MICROSCOPY, CONFOCAL; NEURONAL PLASTICITY; NUCLEUS ACCUMBENS; OVARIECTOMY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, METABOTROPIC GLUTAMATE 5;

EID: 84933178578     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-014-0794-9     Document Type: Article

References (38)

1. Anker JJ, Carroll ME (2011) Females are more vulnerable to drug abuse than males: evidence from preclinical studies and the role of ovarian hormones. Curr Top Behav Neurosci 8:73–96. doi:10.1007/7854_2010_93
2. Asrar S, Jia Z (2013) Molecular mechanisms coordinating functional and morphological plasticity at the synapse: role of GluA2/N-cadherin interaction-mediated actin signaling in mGluR-dependent LTD. Cell Signal 25:397–402. doi:10.1016/j.cellsig.2012.11.007
3. Becker JB, Hu M (2008) Sex differences in drug abuse. Front Neuroendocrinol 29:36–47. doi:10.1016/j.yfrne.2007.07.003
4. Boulware MI, Mermelstein PG (2009) Membrane estrogen receptors activate metabotropic glutamate receptors to influence nervous system physiology. Steroids 74:608–613. doi:10.1016/j.steroids.2008.11.013
5. Boulware MI, Weick JP, Becklund BR et al (2005) Estradiol activates group I and II metabotropic glutamate receptor signaling, leading to opposing influences on cAMP response element-binding protein. J Neurosci 25:5066–5078. doi:10.1523/JNEUROSCI.1427-05.2005
6. Carroll ME, Anker JJ (2010) Sex differences and ovarian hormones in animal models of drug dependence. Horm Behav 58:44–56. doi:10.1016/j.yhbeh.2009.10.001
7. Christensen A, Dewing P, Micevych P (2011) Membrane-initiated estradiol signaling induces spinogenesis required for female sexual receptivity. J Neurosci 31:17583–17589. doi:10.1523/JNEUROSCI.3030-11.2011
8. Dumitriu D, Laplant Q, Grossman YS et al (2012) Subregional, dendritic compartment, and spine subtype specificity in cocaine regulation of dendritic spines in the nucleus accumbens. J Neurosci 32:6957–6966. doi:10.1523/JNEUROSCI.5718-11.2012
9. Duncan JR, Lawrence AJ (2012) The role of metabotropic glutamate receptors in addiction: evidence from preclinical models. Pharmacol Biochem Behav 100:811–824. doi:10.1016/j.pbb.2011.03.015
10. Festa ED, Quinones-Jenab V (2004) Gonadal hormones provide the biological basis for sex differences in behavioral responses to cocaine. Horm Behav 46:509–519. doi:10.1016/j.yhbeh.2004.04.009
11. Fujii R, Okabe S, Urushido T et al (2005) The RNA binding protein TLS is translocated to dendritic spines by mGluR5 activation and regulates spine morphology. Curr Biol CB 15:587–593. doi:10.1016/j.cub.2005.01.058
12. Gasparini F, Lingenhöhl K, Stoehr N et al (1999) 2-Methyl-6-(phenylethynyl)-pyridine (MPEP), a potent, selective and systemically active mGlu5 receptor antagonist. Neuropharmacology 38:1493–1503. doi:10.1016/S0028-3908(99)00082-9
13. Golden SA, Russo SJ (2012) Mechanisms of psychostimulant-induced structural plasticity. Cold Spring Harb Perspect Med. doi:10.1101/cshperspect.a011957
14. Grove-Strawser D, Boulware MI, Mermelstein PG (2010) Membrane estrogen receptors activate the metabotropic glutamate receptors mGluR5 and mGluR3 to bidirectionally regulate CREB phosphorylation in female rat striatal neurons. Neuroscience 170:1045–1055. doi:10.1016/j.neuroscience.2010.08.012
15. Hu M, Becker JB (2003) Effects of sex and estrogen on behavioral sensitization to cocaine in rats. J Neurosci 23:693–699
16. Huang GZ, Woolley CS (2012) Estradiol acutely suppresses inhibition in the hippocampus through a sex-specific endocannabinoid and mGluR-dependent mechanism. Neuron 74:801–808. doi:10.1016/j.neuron.2012.03.035
17. Ito R, Robbins TW, Everitt BJ (2004) Differential control over cocaine-seeking behavior by nucleus accumbens core and shell. Nat Neurosci 7:389–397. doi:10.1038/nn1217
18. Justice AJ, de Wit H (1999) Acute effects of d-amphetamine during the follicular and luteal phases of the menstrual cycle in women. Psychopharmacology 145:67–75
19. Lavreysen H, Wouters R, Bischoff F et al (2004) JNJ16259685, a highly potent, selective and systemically active mGlu1 receptor antagonist. Neuropharmacology 47:961–972. doi:10.1016/j.neuropharm.2004.08.007
20. Loweth JA, Tseng KY, Wolf ME (2013) Using metabotropic glutamate receptors to modulate cocaine’s synaptic and behavioral effects: mGluR1 finds a niche. Curr Opin Neurobiol 23:500–506. doi:10.1016/j.conb.2013.01.009
21. Mccance-katz EF, Hart CL, Boyarsky B et al (2005) Gender effects following repeated administration of cocaine and alcohol in humans. Subst Use Misuse 40:511–528
22. McEwen BS (2001) Invited review: estrogens effects on the brain: multiple sites and molecular mechanisms. J Appl Physiol 91:2785–2801
23. Meitzen J, Mermelstein PG (2011) Estrogen receptors stimulate brain region specific metabotropic glutamate receptors to rapidly initiate signal transduction pathways. J Chem Neuroanat 42:236–241. doi:10.1016/j.jchemneu.2011.02.002
24. Meredith GE, Baldo BA, Andrezjewski ME, Kelley AE (2008) The structural basis for mapping behavior onto the ventral striatum and its subdivisions. Brain Struct Funct 213:17–27. doi:10.1007/s00429-008-0175-3
25. Milner TA, McEwen BS, Hayashi S et al (2001) Ultrastructural evidence that hippocampal alpha estrogen receptors are located at extranuclear sites. J Comp Neurol 429:355–371
26. Mitrano DA, Smith Y (2007) Comparative analysis of the subcellular and subsynaptic localization of mGluR1a and mGluR5 metabotropic glutamate receptors in the shell and core of the nucleus accumbens in rat and monkey. J Comp Neurol 500:788–806. doi:10.1002/cne.21214
27. Olive MF (2010) Cognitive effects of Group I metabotropic glutamate receptor ligands in the context of drug addiction. Eur J Pharmacol 639:47–58. doi:10.1016/j.ejphar.2010.01.029
28. Olive MF, Cleva RM, Kalivas PW, Malcolm RJ (2012) Glutamatergic medications for the treatment of drug and behavioral addictions. Pharmacol Biochem Behav 100:801–810. doi:10.1016/j.pbb.2011.04.015
29. Ridenour TA, Maldonado-Molina M, Compton WM et al (2005) Factors associated with the transition from abuse to dependence among substance abusers: implications for a measure of addictive liability. Drug Alcohol Depend 80:1–14. doi:10.1016/j.drugalcdep.2005.02.005
30. Robinson TE, Kolb B (2004) Structural plasticity associated with exposure to drugs of abuse. Neuropharmacology 47(Suppl 1):33–46. doi:10.1016/j.neuropharm.2004.06.025
31. Roth ME, Cosgrove KP, Carroll ME (2004) Sex differences in the vulnerability to drug abuse: a review of preclinical studies. Neurosci Biobehav Rev 28:533–546. doi:10.1016/j.neubiorev.2004.08.001
32. Russo SJ, Dietz DM, Dumitriu D et al (2010) The addicted synapse: mechanisms of synaptic and structural plasticity in nucleus accumbens. Trends Neurosci 33:267–276. doi:10.1016/j.tins.2010.02.002
33. Segarra AC, Agosto-Rivera JL, Febo M et al (2010) Estradiol: a key biological substrate mediating the response to cocaine in female rats. Horm Behav 58:33–43. doi:10.1016/j.yhbeh.2009.12.003
34. Sircar R, Kim D (1999) Female gonadal hormones differentially modulate cocaine-induced behavioral sensitization in fischer, lewis, and Sprague–Dawley rats. J Pharmacol Exp Ther 289:54–65
35. Staffend NA, Loftus CM, Meisel RL (2011) Estradiol reduces dendritic spine density in the ventral striatum of female Syrian hamsters. Brain Struct Funct 215:187–194. doi:10.1007/s00429-010-0284-7
36. Wang X, Moussawi K, Knackstedt L et al (2013) Role of mGluR5 neurotransmission in reinstated cocaine-seeking. Addict Biol 18:40–49. doi:10.1111/j.1369-1600.2011.00432.x
37. Waselus M, Flagel SB, Jedynak JP et al (2013) Long-term effects of cocaine experience on neuroplasticity in the nucleus accumbens core of addiction-prone rats. Neuroscience 248C:571–584. doi:10.1016/j.neuroscience.2013.06.042
38. Woolley CS (1998) Estrogen-mediated structural and functional synaptic plasticity in the female rat hippocampus. Horm Behav 34:140–148. doi:10.1006/hbeh.1998.1466