Deep Brain Stimulation of the Medial Septal Nucleus Induces Expression of a Virally Delivered Reporter Gene in Dentate Gyrus.

deep brain stimulation gene expression hippocampus medial septal nucleus neuromodulation viral vector

Journal

Frontiers in neuroscience
ISSN: 1662-4548
Titre abrégé: Front Neurosci
Pays: Switzerland
ID NLM: 101478481

Informations de publication

Date de publication:
2020
Historique:
received: 17 10 2019
accepted: 15 04 2020
entrez: 2 6 2020
pubmed: 2 6 2020
medline: 2 6 2020
Statut: epublish

Résumé

Mechanisms of deep brain stimulation (DBS) remain controversial, and spatiotemporal control of brain-wide circuits remains elusive. Adeno-associated viral (AAV) vectors have emerged as vehicles for spatiotemporal expression of exogenous transgenes in several tissues, including specific nuclei in the brain. Coupling DBS with viral vectors to modulate exogenous transgene expression remains unexplored. This study examines whether DBS of the medial septal nucleus (MSN) can regulate gene expression of AAV-transduced neurons in a brain region anatomically remote from the stimulation target: the hippocampal dentate gyrus. Rats underwent unilateral hippocampal injection of an AAV vector with c-Fos promoter-driven expression of TdTomato (TdT), followed by MSN electrode implantation. Rodents received no stimulation, 7.7 Hz (theta), or 130 Hz (gamma) DBS for 1 h one week after surgery. In a repeat stimulation experiment, rodents received either no stimulation, or two 1 h MSN DBS over 2 weeks. No significant differences in hippocampal TdT expression between controls and acute MSN DBS were found. With repeat DBS we found c-Fos protein expression was induced and we could detect increased TdT with either gamma or theta stimulation. We demonstrate that viral vector-mediated gene expression can be regulated spatially and temporally using DBS. Control of gene expression by DBS warrants further investigation into stimulation-responsive promoters for clinical applications.

Sections du résumé

BACKGROUND BACKGROUND
Mechanisms of deep brain stimulation (DBS) remain controversial, and spatiotemporal control of brain-wide circuits remains elusive. Adeno-associated viral (AAV) vectors have emerged as vehicles for spatiotemporal expression of exogenous transgenes in several tissues, including specific nuclei in the brain. Coupling DBS with viral vectors to modulate exogenous transgene expression remains unexplored.
OBJECTIVE OBJECTIVE
This study examines whether DBS of the medial septal nucleus (MSN) can regulate gene expression of AAV-transduced neurons in a brain region anatomically remote from the stimulation target: the hippocampal dentate gyrus.
METHODS METHODS
Rats underwent unilateral hippocampal injection of an AAV vector with c-Fos promoter-driven expression of TdTomato (TdT), followed by MSN electrode implantation. Rodents received no stimulation, 7.7 Hz (theta), or 130 Hz (gamma) DBS for 1 h one week after surgery. In a repeat stimulation experiment, rodents received either no stimulation, or two 1 h MSN DBS over 2 weeks.
RESULTS RESULTS
No significant differences in hippocampal TdT expression between controls and acute MSN DBS were found. With repeat DBS we found c-Fos protein expression was induced and we could detect increased TdT with either gamma or theta stimulation.
CONCLUSION CONCLUSIONS
We demonstrate that viral vector-mediated gene expression can be regulated spatially and temporally using DBS. Control of gene expression by DBS warrants further investigation into stimulation-responsive promoters for clinical applications.

Identifiants

pubmed: 32477058
doi: 10.3389/fnins.2020.00463
pmc: PMC7235415
doi:

Types de publication

Journal Article

Langues

eng

Pagination

463

Informations de copyright

Copyright © 2020 Fomenko, Lee, McKinnon, Lee, de Snoo, Gondard, Neudorfer, Hamani, Lozano, Kalia and Kalia.

Références

Cerebellum. 2017 Apr;16(2):398-410
pubmed: 27435250
PLoS One. 2013 Sep 27;8(9):e76310
pubmed: 24086725
J Chem Neuroanat. 2013 Sep;52:20-4
pubmed: 23660497
Brain Stimul. 2015 Nov-Dec;8(6):1058-64
pubmed: 26321354
Science. 1978 Jul 14;201(4351):160-3
pubmed: 663646
J Neurosci. 1998 Jan 1;18(1):388-98
pubmed: 9412515
Nat Neurosci. 2013 Feb;16(2):130-8
pubmed: 23354386
Neuron. 2019 Mar 6;101(5):839-862
pubmed: 30844402
Acta Neuropathol Commun. 2017 Sep 6;5(1):68
pubmed: 28877758
Nature. 1984 Dec 20-1985 Jan 2;312(5996):716-20
pubmed: 6334806
Curr Opin Neurol. 2013 Aug;26(4):374-80
pubmed: 23817213
Curr Gene Ther. 2010 Oct;10(5):319-340
pubmed: 20712583
Annu Rev Neurosci. 2017 Jul 25;40:453-477
pubmed: 28772097
Neuromodulation. 2008 Jul;11(3):187-95
pubmed: 22151095
Brain Stimul. 2018 Mar - Apr;11(2):435-444
pubmed: 29246746
Ann Clin Transl Neurol. 2018 Nov 08;6(1):174-185
pubmed: 30656196
Hum Gene Ther. 2007 Mar;18(3):195-206
pubmed: 17343566
EMBO Mol Med. 2019 Apr;11(4):
pubmed: 30862663
J Chem Neuroanat. 2011 Nov;42(3):210-7
pubmed: 21855627
Prog Neuropsychopharmacol Biol Psychiatry. 2017 Feb 6;73:1-10
pubmed: 27644164
J Neurosci. 2010 Nov 24;30(47):15951-61
pubmed: 21106833
J Neuroendocrinol. 2008 Jun;20(6):665-72
pubmed: 18601687
Neuroscience. 2006;138(4):1377-85
pubmed: 16460881

Auteurs

Anton Fomenko (A)

Krembil Research Institute, University Health Network, Toronto, ON, Canada.

Darrin J Lee (DJ)

Department of Neurological Surgery and USC Neurorestoration Center, Keck School of Medicine of USC, Los Angeles, CA, United States.

Chris McKinnon (C)

Krembil Research Institute, University Health Network, Toronto, ON, Canada.

Eun Jung Lee (EJ)

Krembil Research Institute, University Health Network, Toronto, ON, Canada.

Mitchell L de Snoo (ML)

Krembil Research Institute, University Health Network, Toronto, ON, Canada.

Elise Gondard (E)

Krembil Research Institute, University Health Network, Toronto, ON, Canada.

Clemens Neudorfer (C)

Krembil Research Institute, University Health Network, Toronto, ON, Canada.

Clement Hamani (C)

Division of Neurosurgery, Sunnybrook Health Sciences Centre, University of Toronto, Toronto, ON, Canada.

Andres M Lozano (AM)

Krembil Research Institute, University Health Network, Toronto, ON, Canada.
Division of Neurosurgery, Department of Surgery, Toronto Western Hospital, University of Toronto, Toronto, ON, Canada.

Lorraine V Kalia (LV)

Krembil Research Institute, University Health Network, Toronto, ON, Canada.
Division of Neurosurgery, Department of Surgery, Toronto Western Hospital, University of Toronto, Toronto, ON, Canada.

Suneil K Kalia (SK)

Krembil Research Institute, University Health Network, Toronto, ON, Canada.
Department of Neurological Surgery and USC Neurorestoration Center, Keck School of Medicine of USC, Los Angeles, CA, United States.

Classifications MeSH