Maturation of Postnatally Generated Olfactory Bulb Granule Cells Depends on Functional γ-protocadherin Expression

Overview

Journal Sci Rep

Specialty Science

Date 2013 Mar 22

PMID 23515096

Citations 17

Authors

Julia Ledderose

Sandra Dieter

Martin K Schwarz

Affiliations

Soon will be listed here.

Abstract

γ-protocadherins (γ-pcdhs) are transmembrane receptor proteins ubiquitously expressed in the postnatal and adult mouse brain. γ-pcdhs are required for normal neuronal development as shown for spinal cord interneurons, retinal ganglion cells and cortical neurons. To test the role of γ-pcdhs during development of subventricular zone progenitor cells and their subsequent differentiation into olfactory granule cells we generated a conditional γ-pcdh(lox/lox) allele (γ-pcdh(lox/lox)) allowing for functional γ-pcdh inactivation upon lentivirus-mediated Cre-recombinase expression selectively in subventricular zone progenitor cells. While γ-pcdh loss did not alter the proliferation of subventricular zone progenitors, γ-pcdh ko progenitors that reached the main olfactory bulb showed a significant reduction in dendritic arborization and failed to develop dendritic spines. Our results suggest that olfactory bulb granule cell maturation necessitates functional γ-pcdh expression.

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References

Garrett A, Schreiner D, Lobas M, Weiner J . γ-protocadherins control cortical dendrite arborization by regulating the activity of a FAK/PKC/MARCKS signaling pathway. Neuron. 2012; 74(2):269-76. PMC: 3582349. DOI: 10.1016/j.neuron.2012.01.028. View

Andreu-Agullo C, Maurin T, Thompson C, Lai E . Ars2 maintains neural stem-cell identity through direct transcriptional activation of Sox2. Nature. 2011; 481(7380):195-8. PMC: 3261657. DOI: 10.1038/nature10712. 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

Consiglio A, Gritti A, Dolcetta D, Follenzi A, Bordignon C, Gage F . Robust in vivo gene transfer into adult mammalian neural stem cells by lentiviral vectors. Proc Natl Acad Sci U S A. 2004; 101(41):14835-40. PMC: 522006. DOI: 10.1073/pnas.0404180101. View

Clements M, Godfrey A, Crossley J, Wilson S, Takeuchi Y, Boshoff C . Lentiviral manipulation of gene expression in human adult and embryonic stem cells. Tissue Eng. 2006; 12(7):1741-51. DOI: 10.1089/ten.2006.12.1741. View

Gotts J, Chesselet M . Migration and fate of newly born cells after focal cortical ischemia in adult rats. J Neurosci Res. 2005; 80(2):160-71. DOI: 10.1002/jnr.20434. View

Kelsch W, Lin C, Lois C . Sequential development of synapses in dendritic domains during adult neurogenesis. Proc Natl Acad Sci U S A. 2008; 105(43):16803-8. PMC: 2567906. DOI: 10.1073/pnas.0807970105. View

Jang E, Goldman J . Pax6 expression is sufficient to induce a neurogenic fate in glial progenitors of the neonatal subventricular zone. PLoS One. 2011; 6(6):e20894. PMC: 3117849. DOI: 10.1371/journal.pone.0020894. View

Murata Y, Hamada S, Morishita H, Mutoh T, Yagi T . Interaction with protocadherin-gamma regulates the cell surface expression of protocadherin-alpha. J Biol Chem. 2004; 279(47):49508-16. DOI: 10.1074/jbc.M408771200. View

10.

Hambsch B, Grinevich V, Seeburg P, Schwarz M . {gamma}-Protocadherins, presenilin-mediated release of C-terminal fragment promotes locus expression. J Biol Chem. 2005; 280(16):15888-97. DOI: 10.1074/jbc.M414359200. View

11.

Lledo P, Alonso M, Grubb M . Adult neurogenesis and functional plasticity in neuronal circuits. Nat Rev Neurosci. 2006; 7(3):179-93. DOI: 10.1038/nrn1867. View

12.

Kirschenbaum B, Doetsch F, Lois C, Alvarez-Buylla A . Adult subventricular zone neuronal precursors continue to proliferate and migrate in the absence of the olfactory bulb. J Neurosci. 1999; 19(6):2171-80. PMC: 6782582. View

13.

Whitman M, Greer C . Adult neurogenesis and the olfactory system. Prog Neurobiol. 2009; 89(2):162-75. PMC: 2748178. DOI: 10.1016/j.pneurobio.2009.07.003. View

14.

Carleton A, Petreanu L, Lansford R, Alvarez-Buylla A, Lledo P . Becoming a new neuron in the adult olfactory bulb. Nat Neurosci. 2003; 6(5):507-18. DOI: 10.1038/nn1048. View

15.

Wu Q, Maniatis T . A striking organization of a large family of human neural cadherin-like cell adhesion genes. Cell. 1999; 97(6):779-90. DOI: 10.1016/s0092-8674(00)80789-8. View

16.

Yagi T . Clustered protocadherin family. Dev Growth Differ. 2008; 50 Suppl 1:S131-40. DOI: 10.1111/j.1440-169X.2008.00991.x. View

17.

Doetsch F . A niche for adult neural stem cells. Curr Opin Genet Dev. 2003; 13(5):543-50. DOI: 10.1016/j.gde.2003.08.012. View

18.

Saura C, Servian-Morilla E, Scholl F . Presenilin/γ-secretase regulates neurexin processing at synapses. PLoS One. 2011; 6(4):e19430. PMC: 3084856. DOI: 10.1371/journal.pone.0019430. View

19.

Lefebvre J, Zhang Y, Meister M, Wang X, Sanes J . gamma-Protocadherins regulate neuronal survival but are dispensable for circuit formation in retina. Development. 2008; 135(24):4141-51. PMC: 2644426. DOI: 10.1242/dev.027912. View

20.

Dittgen T, Nimmerjahn A, Komai S, Licznerski P, Waters J, Margrie T . Lentivirus-based genetic manipulations of cortical neurons and their optical and electrophysiological monitoring in vivo. Proc Natl Acad Sci U S A. 2004; 101(52):18206-11. PMC: 539748. DOI: 10.1073/pnas.0407976101. View