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Mediated Cochlear Gene Transfer

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Mediated Cochlear Gene Transfer Gene Therapy (2000) 7, 377–383 2000 Macmillan Publishers Ltd All rights reserved 0969-7128/00 $15.00 www.nature.com/gt VIRAL TRANSFER TECHNOLOGY RESEARCH ARTICLE Transduction of the contralateral ear after adenovirus- mediated cochlear gene transfer T Sto¨ver1,2, M Yagi1,3 and Y Raphael1 1Kresge Hearing Research Institute, Department of Otolaryngology, The University of Michigan Medical School, Ann Arbor, MI, USA; 2Department of Otolaryngology, Medizinische Hochschule Hannover, Hannover, Germany; and 3Department of Otolaryngology, Kansai Medical University, Osaka, Japan Cochlear gene transfer is a promising new approach for cochleae, whereas virus inoculation into the bloodstream did inner ear therapy. Previous studies have demonstrated hair not. The cochlear aqueduct was identified as the most likely cell protection with cochlear gene transfer not only in the route of virus spread to the contralateral cochlea. These data inoculated, but also in the uninoculated ear. To characterize enhance our understanding of the kinetics of virus-mediated the kinetics of viral spread, we investigated the extent of transgene expression in the inner ear, and assist in the transgene expression in the contralateral (uninoculated) development of clinical applications for inner ear gene ther- cochlea after unilateral adenoviral cochlear gene transfer. apy. Our results showed a functional communication We used a lacZ reporter gene vector, and demonstrated between the CSF and the perilymphatic space of the inner spread of the adenovirus into the cerebrospinal fluid (CSF) ear, that is not only of importance for otological gene trans- after cochlear inoculation of 25 ␮l viral vector. Direct virus fer, but also for CNS gene transfer. Gene Therapy (2000) 7, application into the CSF resulted in transduction of both 377–383. Keywords: adenovirus; gene transfer; cochlea; guinea pig Introduction low. In contrast, viral vectors have been shown to be effective vehicles for gene transfer. Several viral vectors A variety of pathological processes may lead to cochlear have been used for experimental inner ear gene transfer.4 and vestibular impairments. Prevention or correction of Among the most promising are the adenovirus,5,6 the such pathological processes is, thus far, clinically restric- adeno-associated virus,7 the herpes simplex virus,8 and ted to the systemic application of substances. Cochlear the retrovirus.9 Cochlear gene transfer for over- gene transfer provides both an opportunity for localized expression of glial cell line-derived neurotrophic factor administration and the potential for molecular-based (GDNF) and brain-derived neurotrophic factor (BDNF) interventions. Such intervention may facilitate over- showed protective effects on hair cells and spiral expression of certain gene products that may influence ganglion cells.10,11 These studies also demonstrated the repair and regeneration in the inner ear epithelia. For potential for cochlear gene therapy for therapeutic instance, manipulating levels of retinoic acid in cultured applications. Kip1 developing cochleae and knocking out the p27 gene Following unilateral adeno-associated virus gene trans- 1–3 have been shown to lead to overproduction of hair cells. fer into guinea pig cochlea, Lalwani et al12,13 observed The former example deals with a secreted (diffusible) transduction of vestibular cells of the uninoculated gene product and can be done in the mature cochlea. The (contralateral) cochlea. They speculated that the viral vec- Kip1 latter example, p27 knock out, can presently be tor was transferred to the uninoculated ear via the blood- accomplished only at the germline intervention level. stream, the bone marrow, or the CSF. Contralateral trans- However, once gene therapy in somatic cells shuts down gene expression following virus-mediated gene transfer the expression of specific genes, similar results can be has not been reported elsewhere. However, a trend for accomplished in a tissue-specific manner. Such inter- the contralateral protective effects of GDNF has been ventions are particularly exciting for clinical applications observed.10 If the contralateral effect is true, protection as they would provide a treatment of inner ear experiments based on a comparison between the inocu- pathologies that currently have no cure. lated and contralateral sides could underestimate the There are several possible ways to deliver transgenes degree of protection, since the contralateral ear might into tissues. Nonviral vectors pose little or no risk of also have been treated and protected. The mechanism for immune response, but their transduction efficiency is the contralateral protection is unclear. Therefore, the first goal of this study was to characterize the contralateral effects after unilateral cochlear gene transfer. Specifically, Correspondence: Y Raphael, MSRB 3, Room 9303, 1150 W. Medical we wished to determine if contralateral transgene Center Drive, Ann Arbor, MI 48109–0648, USA expression can occur after adenovirus inoculation of the Received 29 July 1999; accepted 28 October 1999 guinea pig ear and, if so, to elucidate the route of migration of the viral particles to the contralateral ear. Transduction of the contralateral cochlea T Sto¨ver et al 378 We chose an adenoviral vector system, encoding the Transduced cochlear cells are detectable 6 h after gene reporter gene lacZ, to address these questions. Inner ear transfer inoculation with the adenoviral vector is well estab- Time-course experiments were performed with cochlear lished5,14 and it has been demonstrated to be therapeuti- inoculations of 25 ␮l adenoviral vector into the left coch- cally effective on hair cells.10 As third-generation adeno- lea. Transfected cochlear cells could be detected 6 h after virus vectors are being developed with reduced inoculation. None of the animals killed from 30 min to immunogenicity and increased duration of gene 5.5 h after cochlear gene transfer showed lacZ-positive expression, these vectors are potential candidates for cells. In animals killed 6 h and 10 h after inoculation, cochlear gene transfer in clinical trials. lacZ-positive cells were identified in the scala tympani of The second goal of this study was to determine other both ears. Histological sections obtained from these speci- important features of virus-mediated cochlear gene trans- mens identified lacZ-positive cells predominantly in con- fer in the cochlea. Without doubt, clinical application will nective tissue cells within the spiral ligament, mesothelial require detailed information on the possible side-effects cells beneath the organ of Corti, and fibrocyctes lining of viral vehicles used for cochlear gene transfer. Determi- the perilymphatic fluid spaces (Figure 1D). Furthermore, nation of the transgene distribution after inoculation with in some specimens, we found lacZ-staining in Hensen increased amounts of viral vector is of great interest as cells and pillar cells (Figure 1E) and also in the region of no information is currently available on the maximal vol- Rosenthal’s canal. The transfected cells in Rosenthal’s umes of virus solution applicable to the inner ear as a canal were predominantly Schwann cells, lying between bolus injection. Evaluation of the resulting transgene dis- spiral ganglion cells (Figure 1F). Six (and 10) h after virus tribution and identification of the cell types susceptible inoculation into the scala tympani, we also observed to the viral vector after inoculation with increased vol- staining of the middle ear mucosa in the inoculated side umes of vector have to occur before gene transfer can (data not shown). be practically used in clinical trials. Other issues to be addressed include unintended transfection of nontar- The transduction of the contralateral cochlea is geted tissues with increased virus volume and possible mediated by the cochlear aqueduct changes in vector cell specificity. To determine if the route of transduction for the contrala- We demonstrate that cochlear expression of lacZ was teral cochlear cells was via the blood or CSF mediation, detectable as soon as 6 h after virus inoculation. Contrala- 25 ␮l of adenoviral solution was injected directly into the teral transgene expression was volume dependent. It was jugular vein or into the CSF space of the skull. No lacZ- observed after an inoculation with 25 ␮l, but not after a positive cells were found on the brain surface or in coch- 5 ␮l inoculation into the cochlea. No systemic transgene lear tissue of any systemically inoculated animal (n = 4). expression was found after cochlear inoculation even In contrast, lacZ-positive cells were identified in both with the increased volume of the viral vector, whereas cochleae, mostly in the basal and the second cochlear expression in liver and spleen was observed after inocu- turns, and on the brain surface in all animals inoculated lation into the bloodstream and the CSF. Inoculation into via the CSF (n = 6). Careful inspection of the cochlear the cranial CSF resulted in detection of lacZ-positive cells tissue revealed a predominant cluster region of lacZ-posi- in the cochlear opening of the cochlear aqueduct bilater- tive cells close to the ‘hook’ region of the cochlea ally, implicating the CSF aqueduct as the route for ear to (Figure 3A and B). This region represents anatomically ear vector transfer. Finally, application of the viral vector the opening of the cochlear aqueduct that connects the into the lumbar region of the CSF space was also ident- CSF space with the perilymphatic space of the scala tym- ified as a potential route for delivering vectors into the pani. While 5 ␮l of the viral vector applied to the cochlea cochlea. were not sufficient to induce a contralateral gene transfer effect, 25 ␮l of the virus solution applied to the cochlea or the CSF space induced a response. Results To investigate further viral passage through the coch- lear aqueduct in guinea pigs, we injected 200 ␮l of the adenoviral vector into the CSF space of the lumbar region Cochlear inoculation of increased vector volume results via a lumbar puncture (n = 2). We found that one of the in transduction of the contralateral ear animals showed lacZ-positive cells in both cochleae.
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