Chronic VEGFR-3 signaling preserves dendritic arborization and sensitization under stress.
Arborization
Dendrite
Neuroprotection
VEGF-C
VEGF-D
Journal
Brain, behavior, and immunity
ISSN: 1090-2139
Titre abrégé: Brain Behav Immun
Pays: Netherlands
ID NLM: 8800478
Informations de publication
Date de publication:
11 2021
11 2021
Historique:
received:
30
11
2020
revised:
15
07
2021
accepted:
05
08
2021
pubmed:
15
8
2021
medline:
15
12
2021
entrez:
14
8
2021
Statut:
ppublish
Résumé
Dendritic arborization is critical for the establishment and maintenance of precise neural circuits. Vascular endothelial growth factor D (VEGF-D), well-characterized as a "lymphangiogenic" growth factor, reportedly maintains dendritic arborization and synaptic strength in the hippocampus of adult mice through VEGF receptor (VEGFR-3) signaling. Here, we investigated the effect of chronic VEGFR-3-specific activation on adipose arbor morphometry using the Adipo-VD mouse, a model of inducible, adipose-specific VEGF-D overexpression. We examined whether adipose tissue innervation was preserved or functionally different in Adipo-VD mice during stress in vivo and if VEGFR-3 signaling afforded neuroprotection to challenged neurons in vitro. Chronic VEGFR-3 signaling in Adipo-VD subcutaneous adipose tissue resulted in a reduction in the dendrite length, dendritic terminal branches (filament length), and dendritic terminal branch volume (filament volume), but increased dendrite branching. We also identified reduced stimulus-evoked excitatory sympathetic nerve activity in Adipo-VD mice. Following 6-hydroxydopamine (6-OHDA) denervation, Adipo-VD dendritic arbors were preserved, including improved dendritic branch volume, length, and dendritic branches than in wildtype tissues. In vitro, we found that chronic elevation of VEGFR-3 signaling in developing mVC neurons changes the dendritic arbor complexity and improves stress-induced structure remodeling. Developing neurons are conferred neuroprotection against stress, potentially by upregulation of proteolytic conversion of pro-BDNF to mature BDNF. Mature neurons, however, display improved dendritic arbor complexity, and unaltered dendritic structural remodeling and improved resistance to stress with VEGFR-3 signaling. Overall, chronically increasing VEGFR-3 signaling in neurons has a synergistic impact on neurosensitization and neuroprotection during stress.
Identifiants
pubmed: 34389489
pii: S0889-1591(21)00296-8
doi: 10.1016/j.bbi.2021.08.007
pmc: PMC8511130
mid: NIHMS1735952
pii:
doi:
Substances chimiques
Vascular Endothelial Growth Factor D
0
Vascular Endothelial Growth Factor Receptor-3
EC 2.7.10.1
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
219-233Subventions
Organisme : NINDS NIH HHS
ID : R01 NS106907
Pays : United States
Informations de copyright
Copyright © 2021 Elsevier Inc. All rights reserved.
Références
Elife. 2019 Dec 23;8:
pubmed: 31868584
Eur J Neurosci. 2016 Aug;44(3):2028-39
pubmed: 27285957
PLoS One. 2019 Sep 11;14(9):e0221766
pubmed: 31509546
J Neurosci. 2020 Sep 30;40(40):7578-7589
pubmed: 32998955
Am J Pathol. 2019 Apr;189(4):924-939
pubmed: 30878136
Exp Biol Med (Maywood). 2017 Apr;242(8):884-895
pubmed: 28346012
Neuroscience. 2011 Sep 29;192:550-63
pubmed: 21767614
Mol Ther Methods Clin Dev. 2019 Dec 25;17:281-299
pubmed: 32055648
J Neurosci. 2012 May 16;32(20):6795-807
pubmed: 22593049
Nat Neurosci. 2006 Mar;9(3):340-8
pubmed: 16462734
Int J Mol Sci. 2020 Feb 24;21(4):
pubmed: 32102377
Stem Cells Transl Med. 2013 Nov;2(11):862-70
pubmed: 24113065
Cell Rep. 2018 Aug 21;24(8):2063-2074
pubmed: 30134168
Neuroscience. 2018 Sep 15;388:330-346
pubmed: 30076998
Mol Cell Neurosci. 2016 Mar;71:66-79
pubmed: 26705735
Endocrinology. 2015 Oct;156(10):3485-7
pubmed: 26380935
Stem Cells Int. 2019 Nov 19;2019:8502370
pubmed: 31827536
Organogenesis. 2010 Apr-Jun;6(2):107-14
pubmed: 20885857
Cell Rep. 2015 Feb 24;10(7):1158-72
pubmed: 25704818
Mol Cell Biol. 2005 Mar;25(6):2441-9
pubmed: 15743836
PLoS One. 2014 Aug 07;9(8):e104458
pubmed: 25101983
Genes Dev. 2016 Aug 1;30(15):1776-89
pubmed: 27542831
Obesity (Silver Spring). 2012 Jul;20(7):1355-64
pubmed: 22513494
Cell. 2020 Jul 23;182(2):270-296
pubmed: 32707093
J Neurosci. 2007 Jul 25;27(30):7911-20
pubmed: 17652582
Mol Metab. 2017 Oct;6(10):1081-1091
pubmed: 29031710
Cell Tissue Res. 2015 Jan;359(1):267-78
pubmed: 25080065
Development. 2005 Oct;132(19):4285-98
pubmed: 16141221
Am J Physiol Heart Circ Physiol. 2016 Aug 1;311(2):H384-94
pubmed: 27342876
Methods Mol Biol. 2013;997:57-72
pubmed: 23546748
Mol Cell Neurosci. 2000 Feb;15(2):170-82
pubmed: 10673325
Mol Cell Biol. 2018 Oct 29;38(22):
pubmed: 30126894
Front Physiol. 2020 Jul 15;11:831
pubmed: 32760294
Curr Diab Rep. 2016 Mar;16(3):29
pubmed: 26897744
Neuroscience. 2020 Nov 10;448:28-42
pubmed: 32920043
Mol Cell Endocrinol. 2010 Apr 29;318(1-2):34-43
pubmed: 19747957
J Extracell Vesicles. 2020 Aug 26;9(1):1809064
pubmed: 32944193
Annu Rev Neurosci. 2012;35:369-89
pubmed: 22715882
Annu Rev Cell Dev Biol. 2015;31:779-805
pubmed: 26436703
J Neurosci Res. 2012 Jul;90(7):1367-81
pubmed: 22535492
Annu Rev Neurosci. 2010;33:349-78
pubmed: 20367247
Front Neuroanat. 2016 Jun 28;10:75
pubmed: 27445713
Neuron. 2011 Jul 14;71(1):117-30
pubmed: 21745642
Endocrinology. 2015 Oct;156(10):3680-94
pubmed: 26132918
Proc Natl Acad Sci U S A. 2020 Apr 14;117(15):8616-8623
pubmed: 32229571
Behav Pharmacol. 2017 Jun;28(4):285-293
pubmed: 28134661
Front Cell Neurosci. 2020 Jan 22;13:570
pubmed: 32038171
Free Radic Biol Med. 2013 Oct;63:421-31
pubmed: 23732519
J Vis Exp. 2013 Dec 19;(82):e51212
pubmed: 24378519
Neuropharmacology. 2008 Dec;55(7):1081-94
pubmed: 18755202
Curr Protoc Neurosci. 2001 May;Chapter 7:Unit7.18
pubmed: 18428528
Front Physiol. 2020 Apr 22;11:363
pubmed: 32390866
Ann Anat. 2011 Jul;193(4):347-53
pubmed: 21514121
Nat Rev Neurosci. 2006 Nov;7(11):873-81
pubmed: 17053811
Exp Neurol. 1991 Oct;114(1):11-22
pubmed: 1717307
PLoS One. 2013 Sep 30;8(9):e75877
pubmed: 24098736
Trends Neurosci. 2014 Jun;37(6):343-55
pubmed: 24833289
Cell Res. 2018 Aug;28(8):803-818
pubmed: 29844583
Cytometry A. 2004 Apr;58(2):167-76
pubmed: 15057970
BMC Res Notes. 2016 Feb 11;9:82
pubmed: 26864470
Sci Rep. 2020 Jul 24;10(1):12409
pubmed: 32710087
Cell Metab. 2016 Sep 13;24(3):420-433
pubmed: 27626200
Toxicol In Vitro. 2019 Oct;60:400-411
pubmed: 31247335
Pain Res Manag. 2016;2016:2487924
pubmed: 27445603
Cell Rep. 2019 Jun 4;27(10):3081-3096.e5
pubmed: 31167149
Methods Enzymol. 2014;537:199-225
pubmed: 24480348
Proc Natl Acad Sci U S A. 2020 Jul 14;117(28):16096-16099
pubmed: 32581125
Genes Dev. 2011 Apr 15;25(8):831-44
pubmed: 21498572
J Neurosci. 2008 Oct 15;28(42):10451-9
pubmed: 18923022
Eur J Neurosci. 2004 Mar;19(5):1119-32
pubmed: 15016071
Cell. 2003 May 2;113(3):285-99
pubmed: 12732138