GPER1 Signaling Initiates Migration of Female V-SVZ-Derived Cells

Overview

Journal iScience

Publisher Cell Press

Date 2020 May 4

PMID 32361597

Citations 4

Authors

Iris Haumann

Muriel Anne Sturm

Max Anstotz

Gabriele M Rune

Affiliations

Soon will be listed here.

Abstract

In the rodent ventricular-subventricular zone (V-SVZ) neurons are generated throughout life. They migrate along the rostral migratory stream (RMS) into the olfactory bulb before their final differentiation into interneurons and integration into local circuits. Estrogen receptors (ERs) are steroid hormone receptors with important functions in neurogenesis and synaptic plasticity. In this study, we show that the ER GPER1 is expressed in subsets of cells within the V-SVZ of female animals and provide evidence for a potential local estrogen source from aromatase-positive astrocytes surrounding the RMS. Blocking of GPER1 in Matrigel cultures of female animals significantly impairs migration of V-SVZ-derived cells. This outgrowth is accompanied by regulation of phosphorylation of the actin-binding protein cofilin by GPER1 signaling including an involvement of the p21-Ras pathway. Our results point to a prominent role of GPER1 in the initiation of neuronal migration from the V-SVZ to the olfactory bulb.

Citing Articles

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The Impact of Estrogen and Estrogen-Like Molecules in Neurogenesis and Neurodegeneration: Beneficial or Harmful?.

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Does GPER1 Play a Role in Sexual Dimorphism?.

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References

Vierk R, Glassmeier G, Zhou L, Brandt N, Fester L, Dudzinski D . Aromatase inhibition abolishes LTP generation in female but not in male mice. J Neurosci. 2012; 32(24):8116-26. PMC: 6703647. DOI: 10.1523/JNEUROSCI.5319-11.2012. View

Saldanha C, Remage-Healey L, Schlinger B . Synaptocrine signaling: steroid synthesis and action at the synapse. Endocr Rev. 2011; 32(4):532-49. PMC: 3369574. DOI: 10.1210/er.2011-0004. View

Doetsch F, Garcia-Verdugo J, Alvarez-Buylla A . Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci. 1997; 17(13):5046-61. PMC: 6573289. View

Young W, Goy R, Phoenix C . HORMONES AND SEXUAL BEHAVIOR. Science. 1964; 143(3603):212-8. DOI: 10.1126/science.143.3603.212. View

Luskin M . Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron. 1993; 11(1):173-89. DOI: 10.1016/0896-6273(93)90281-u. View

McEwen B, Milner T . Understanding the broad influence of sex hormones and sex differences in the brain. J Neurosci Res. 2016; 95(1-2):24-39. PMC: 5120618. DOI: 10.1002/jnr.23809. View

Mak G, Enwere E, Gregg C, Pakarainen T, Poutanen M, Huhtaniemi I . Male pheromone-stimulated neurogenesis in the adult female brain: possible role in mating behavior. Nat Neurosci. 2007; 10(8):1003-11. DOI: 10.1038/nn1928. View

Li Y, Jia Y, Bian Y, Tong H, Qu J, Wang K . Autocrine motility factor promotes endometrial cancer progression by targeting GPER-1. Cell Commun Signal. 2019; 17(1):22. PMC: 6402158. DOI: 10.1186/s12964-019-0336-4. View

Martinez-Cerdeno V, Noctor S, Kriegstein A . Estradiol stimulates progenitor cell division in the ventricular and subventricular zones of the embryonic neocortex. Eur J Neurosci. 2007; 24(12):3475-88. DOI: 10.1111/j.1460-9568.2006.05239.x. View

10.

Lennington J, Yang Z, Conover J . Neural stem cells and the regulation of adult neurogenesis. Reprod Biol Endocrinol. 2003; 1:99. PMC: 293430. DOI: 10.1186/1477-7827-1-99. View

11.

Du G, Zhou L, Chen X, Wan X, He Y . The G protein-coupled receptor GPR30 mediates the proliferative and invasive effects induced by hydroxytamoxifen in endometrial cancer cells. Biochem Biophys Res Commun. 2012; 420(2):343-9. DOI: 10.1016/j.bbrc.2012.02.161. View

12.

Prange-Kiel J, Rune G . Direct and indirect effects of estrogen on rat hippocampus. Neuroscience. 2005; 138(3):765-72. DOI: 10.1016/j.neuroscience.2005.05.061. View

13.

Fester L, Ribeiro-Gouveia V, Prange-Kiel J, von Schassen C, Bottner M, Jarry H . Proliferation and apoptosis of hippocampal granule cells require local oestrogen synthesis. J Neurochem. 2006; 97(4):1136-44. DOI: 10.1111/j.1471-4159.2006.03809.x. View

14.

Hoyk Z, Varga C, Parducz A . Estrogen-induced region specific decrease in the density of 5-bromo-2-deoxyuridine-labeled cells in the olfactory bulb of adult female rats. Neuroscience. 2006; 141(4):1919-24. DOI: 10.1016/j.neuroscience.2006.05.053. View

15.

Lim D, Alvarez-Buylla A . Adult neural stem cells stake their ground. Trends Neurosci. 2014; 37(10):563-71. PMC: 4203324. DOI: 10.1016/j.tins.2014.08.006. View

16.

Gohla A, Birkenfeld J, Bokoch G . Chronophin, a novel HAD-type serine protein phosphatase, regulates cofilin-dependent actin dynamics. Nat Cell Biol. 2004; 7(1):21-9. DOI: 10.1038/ncb1201. View

17.

Vivacqua A, Bonofiglio D, Grazia Recchia A, Musti A, Picard D, Ando S . The G protein-coupled receptor GPR30 mediates the proliferative effects induced by 17beta-estradiol and hydroxytamoxifen in endometrial cancer cells. Mol Endocrinol. 2005; 20(3):631-46. DOI: 10.1210/me.2005-0280. View

18.

Zhong W, Feder J, Jiang M, Jan L, Jan Y . Asymmetric localization of a mammalian numb homolog during mouse cortical neurogenesis. Neuron. 1996; 17(1):43-53. DOI: 10.1016/s0896-6273(00)80279-2. View

19.

Dixon K, Turbic A, Turnley A, Liebl D . Explant Methodology for Analyzing Neuroblast Migration. Bio Protoc. 2017; 7(9). PMC: 5512276. DOI: 10.21769/BioProtoc.2249. View

20.

Marino M, Ascenzi P, Acconcia F . S-palmitoylation modulates estrogen receptor alpha localization and functions. Steroids. 2005; 71(4):298-303. DOI: 10.1016/j.steroids.2005.09.011. View