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VEGFA165 gene therapy ameliorates blood-labyrinth barrier breakdown and hearing loss

Journal Article · · JCI Insight
 [1];  [2];  [3];  [2];  [2];  [2];  [2];  [2];  [4];  [4];  [5];  [6];  [2]
  1. Oregon Health & Science University, Portland, OR (United States). Dept. of Otolaryngology-Head & Neck Surgery. Oregon Hearing Research Center; OSTI
  2. Oregon Health & Science University, Portland, OR (United States). Dept. of Otolaryngology-Head & Neck Surgery. Oregon Hearing Research Center
  3. Oregon Health & Science University, Portland, OR (United States). Dept. of Otolaryngology-Head & Neck Surgery. Oregon Hearing Research Center; Harvard Medical School, Boston, MA (United States). Boston Children’s Hospital
  4. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Life Sciences Division
  5. Linköping Univ. (Sweden). Dept. of Biomedical and Clinical Sciences
  6. National Institutes of Health (NIH), Bethesda, MD (United States). National Inst. on Deafness and Other Communication Disorders (NIDCD). Auditory Development and Restoration Program

Millions of people are affected by hearing loss. Hearing loss is frequently caused by noise or aging and often associated with loss of pericytes. Pericytes populate the small vessels in the adult cochlea. However, their role in different types of hearing loss is largely unknown. Using an inducible and conditional pericyte depletion mouse model and noise-exposed mouse model, we show that loss of pericytes leads to marked changes in vascular structure, in turn leading to vascular degeneration and hearing loss. In vitro, using advanced tissue explants from pericyte fluorescence reporter models combined with exogenous donor pericytes, we show that pericytes, signaled by VEGF isoform A165 (VEGFA165), vigorously drive new vessel growth in both adult and neonatal mouse inner ear tissue. In vivo, the delivery of an adeno-associated virus serotype 1–mediated (AAV1–mediated) VEGFA165 viral vector to pericyte-depleted or noise-exposed animals prevented and regenerated lost pericytes, improved blood supply, and attenuated hearing loss. These studies provide the first clear-cut evidence that pericytes are critical for vascular regeneration, vascular stability, and hearing in adults. The restoration of vascular function in the damaged cochlea, including in noise-exposed animals, suggests that VEGFA165 gene therapy could be a new strategy for ameliorating vascular associated hearing disorders.

Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division; National Institutes of Health (NIH); Medical Research Foundation
Grant/Contract Number:
AC02-05CH11231
OSTI ID:
1815938
Journal Information:
JCI Insight, Journal Name: JCI Insight Journal Issue: 8 Vol. 6; ISSN 2379-3708
Publisher:
American Society for Clinical InvestigationCopyright Statement
Country of Publication:
United States
Language:
English

References (62)

Canalostomy as a Surgical Approach for Cochlear Gene Therapy in the Rat
  • Gassner, Davina; Durham, Dianne; Pfannenstiel, Susanna C.
  • The Anatomical Record: Advances in Integrative Anatomy and Evolutionary Biology, Vol. 295, Issue 11 https://doi.org/10.1002/ar.22593
journal October 2012
How is the highly positive endocochlear potential formed? The specific architecture of the stria vascularis and the roles of the ion-transport apparatus journal December 2009
Cytomegalovirus (CMV) Infection Causes Degeneration of Cochlear Vasculature and Hearing Loss in a Mouse Model journal December 2016
Platelet-Derived Growth Factor Subunit B Signaling Promotes Pericyte Migration in Response to Loud Sound in the Cochlear Stria Vascularis journal June 2018
Equal modulation of endothelial cell function by four distinct tissue-specific mesenchymal stem cells journal April 2012
Techniques for the observation and measurement of red blood cell velocity in vessels of the guinea pig cochlea journal January 1987
The effects of noise on histological measures of the cochlear vasculature and red blood cells: A review journal December 1987
Development and regression of cochlear blood vessels in fetal and newborn mice journal July 2000
Acoustic Trauma Causes Cochlear Pericyte-to-Myofibroblast–Like Cell Transformation and Vascular Degeneration, and Transplantation of New Pericytes Prevents Vascular Atrophy journal September 2020
Basic and Therapeutic Aspects of Angiogenesis journal September 2011
Vascular pathology and hearing disorders journal December 2020
Pericytes: Developmental, Physiological, and Pathological Perspectives, Problems, and Promises journal August 2011
Physiopathology of the cochlear microcirculation journal December 2011
Thin and open vessel windows for intra-vital fluorescence imaging of murine cochlear blood flow journal July 2014
Pathophysiology of the cochlear intrastrial fluid-blood barrier (review) journal August 2016
Tonotopy in calcium homeostasis and vulnerability of cochlear hair cells journal May 2019
Microvascular networks in the area of the auditory peripheral nervous system journal January 2019
Vascular regeneration in adult mouse cochlea stimulated by VEGF-A165 and driven by NG2-derived cells ex vivo journal June 2019
Tumor necrosis factor-α-stimulated brain pericytes possess a unique cytokine and chemokine release profile and enhance microglial activation journal August 2014
Pericytes: Blood-Brain Barrier Safeguards against Neurodegeneration? journal November 2010
Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis journal January 2007
Pericytes are required for blood–brain barrier integrity during embryogenesis journal October 2010
Capillary pericytes regulate cerebral blood flow in health and disease journal March 2014
Brain vessels squeezed to death journal March 2014
Pericyte-expressed Tie2 controls angiogenesis and vessel maturation journal July 2017
NIH Image to ImageJ: 25 years of image analysis journal June 2012
Pericytes of the neurovascular unit: key functions and signaling pathways journal May 2016
Isolation and culture of endothelial cells, pericytes and perivascular resident macrophage-like melanocytes from the young mouse ear journal March 2013
A role for pericytes in coronary no-reflow journal April 2014
Pericytes regulate VEGF-induced endothelial sprouting through VEGFR1 journal November 2017
NCK-dependent pericyte migration promotes pathological neovascularization in ischemic retinopathy journal August 2018
Improved TMC1 gene therapy restores hearing and balance in mice with genetic inner ear disorders journal January 2019
Endophilin-A2 dependent VEGFR2 endocytosis promotes sprouting angiogenesis journal May 2019
Pericyte loss leads to circulatory failure and pleiotrophin depletion causing neuron loss journal June 2019
Enhanced viral-mediated cochlear gene delivery in adult mice by combining canal fenestration with round window membrane inoculation journal February 2018
S1PR2 variants associated with auditory function in humans and endocochlear potential decline in mouse journal July 2016
Diversity Within Pericytes journal October 2000
Perivascular-resident macrophage-like melanocytes in the inner ear are essential for the integrity of the intrastrial fluid-blood barrier journal June 2012
Control of hearing sensitivity by tectorial membrane calcium journal March 2019
Pericytes enable effective angiogenesis in the presence of proinflammatory signals journal November 2019
The Cochlear Pericytes journal January 2008
VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia journal June 2003
Microenvironmental VEGF distribution is critical for stable and functional vessel growth in ischemia journal December 2006
Perivascular cells for regenerative medicine journal December 2012
Mechanical tuning and amplification within the apex of the guinea pig cochlea: Tuning and amplification in the cochlear apex journal May 2017
Tmc gene therapy restores auditory function in deaf mice journal July 2015
Vascular Endothelial Growth Factor (VEGF)-A165b Is a Weak In vitro Agonist for VEGF Receptor-2 Due to Lack of Coreceptor Binding and Deficient Regulation of Kinase Activity journal June 2008
Overexpression of Copper/Zinc- Superoxide Dismutase Protects from Kanamycin-Induced Hearing Loss journal January 2001
Mechanisms of Vessel Branching: Filopodia on Endothelial Tip Cells Lead the Way journal May 2009
Vascular Endothelial Growth Factor Promotes Pericyte Coverage of Brain Capillaries, Improves Cerebral Blood Flow During Subsequent Focal Cerebral Ischemia, and Preserves the Metabolic Penumbra journal June 2013
Sustained inflammation after pericyte depletion induces irreversible blood-retina barrier breakdown journal February 2017
Pericytes secrete pro-regenerative molecules in response to platelet-derived growth factor-BB journal July 2017
The role of pericytes in blood-vessel formation and maintenance journal October 2005
Origins of fibrosis: pericytes take centre stage journal September 2013
Lineage Analysis of the Late Otocyst Stage Mouse Inner Ear by Transuterine Microinjection of A Retroviral Vector Encoding Alkaline Phosphatase and an Oligonucleotide Library journal July 2013
The Role of Pericytes in Blood-Brain Barrier Function and Stroke journal August 2012
Pericyte Migration: A Novel Mechanism of Pericyte Loss in Experimental Diabetic Retinopathy journal June 2008
Bone Marrow Cell Recruitment Mediated by Inducible Nitric Oxide Synthase/Stromal Cell-Derived Factor-1α Signaling Repairs the Acoustically Damaged Cochlear Blood-Labyrinth Barrier journal December 2010
Strial Circulation Impairment due to Acoustic Trauma journal January 1991
Differential vulnerability of outer and inner hair cells during and after oxygen-glucose deprivation in organotypic cultures of newborn rats journal January 2009
Immune Regulation by Pericytes: Modulating Innate and Adaptive Immunity journal November 2016
Evaluating the role of connexin43 in congenital heart disease: Screening for mutations in patients with outflow tract anomalies and the analysis of knock-in mouse models journal October 2011

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