Nanofibrous scaffolds for the guidance of stem cell-derived neurons for auditory nerve regeneration
Impairment of spiral ganglion neurons (SGNs) of the auditory nerve is a major cause for hearing loss occurring independently or in addition to sensory hair cell damage. Unfortunately, mammalian SGNs lack the potential for autonomous regeneration. Stem cell based therapy is a promising approach for a...
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| Published in | PloS one Vol. 12; no. 7; p. e0180427 |
|---|---|
| Main Authors | , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
03.07.2017
Public Library of Science (PLoS) |
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| Online Access | Get full text |
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| Abstract | Impairment of spiral ganglion neurons (SGNs) of the auditory nerve is a major cause for hearing loss occurring independently or in addition to sensory hair cell damage. Unfortunately, mammalian SGNs lack the potential for autonomous regeneration. Stem cell based therapy is a promising approach for auditory nerve regeneration, but proper integration of exogenous cells into the auditory circuit remains a fundamental challenge. Here, we present novel nanofibrous scaffolds designed to guide the integration of human stem cell-derived neurons in the internal auditory meatus (IAM), the foramen allowing passage of the spiral ganglion to the auditory brainstem. Human embryonic stem cells (hESC) were differentiated into neural precursor cells (NPCs) and seeded onto aligned nanofiber mats. The NPCs terminally differentiated into glutamatergic neurons with high efficiency, and neurite projections aligned with nanofibers in vitro. Scaffolds were assembled by seeding GFP-labeled NPCs on nanofibers integrated in a polymer sheath. Biocompatibility and functionality of the NPC-seeded scaffolds were evaluated in vivo in deafened guinea pigs (Cavia porcellus). To this end, we established an ouabain-based deafening procedure that depleted an average 72% of SGNs from apex to base of the cochleae and caused profound hearing loss. Further, we developed a surgical procedure to implant seeded scaffolds directly into the guinea pig IAM. No evidence of an inflammatory response was observed, but post-surgery tissue repair appeared to be facilitated by infiltrating Schwann cells. While NPC survival was found to be poor, both subjects implanted with NPC-seeded and cell-free control scaffolds showed partial recovery of electrically-evoked auditory brainstem thresholds. Thus, while future studies must address cell survival, nanofibrous scaffolds pose a promising strategy for auditory nerve regeneration. |
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| AbstractList | Impairment of spiral ganglion neurons (SGNs) of the auditory nerve is a major cause for hearing loss occurring independently or in addition to sensory hair cell damage. Unfortunately, mammalian SGNs lack the potential for autonomous regeneration. Stem cell based therapy is a promising approach for auditory nerve regeneration, but proper integration of exogenous cells into the auditory circuit remains a fundamental challenge. Here, we present novel nanofibrous scaffolds designed to guide the integration of human stem cell-derived neurons in the internal auditory meatus (IAM), the foramen allowing passage of the spiral ganglion to the auditory brainstem. Human embryonic stem cells (hESC) were differentiated into neural precursor cells (NPCs) and seeded onto aligned nanofiber mats. The NPCs terminally differentiated into glutamatergic neurons with high efficiency, and neurite projections aligned with nanofibers in vitro. Scaffolds were assembled by seeding GFP-labeled NPCs on nanofibers integrated in a polymer sheath. Biocompatibility and functionality of the NPC-seeded scaffolds were evaluated in vivo in deafened guinea pigs (Cavia porcellus). To this end, we established an ouabain-based deafening procedure that depleted an average 72% of SGNs from apex to base of the cochleae and caused profound hearing loss. Further, we developed a surgical procedure to implant seeded scaffolds directly into the guinea pig IAM. No evidence of an inflammatory response was observed, but post-surgery tissue repair appeared to be facilitated by infiltrating Schwann cells. While NPC survival was found to be poor, both subjects implanted with NPC-seeded and cell-free control scaffolds showed partial recovery of electrically-evoked auditory brainstem thresholds. Thus, while future studies must address cell survival, nanofibrous scaffolds pose a promising strategy for auditory nerve regeneration. Impairment of spiral ganglion neurons (SGNs) of the auditory nerve is a major cause for hearing loss occurring independently or in addition to sensory hair cell damage. Unfortunately, mammalian SGNs lack the potential for autonomous regeneration. Stem cell based therapy is a promising approach for auditory nerve regeneration, but proper integration of exogenous cells into the auditory circuit remains a fundamental challenge. Here, we present novel nanofibrous scaffolds designed to guide the integration of human stem cell-derived neurons in the internal auditory meatus (IAM), the foramen allowing passage of the spiral ganglion to the auditory brainstem. Human embryonic stem cells (hESC) were differentiated into neural precursor cells (NPCs) and seeded onto aligned nanofiber mats. The NPCs terminally differentiated into glutamatergic neurons with high efficiency, and neurite projections aligned with nanofibers in vitro . Scaffolds were assembled by seeding GFP-labeled NPCs on nanofibers integrated in a polymer sheath. Biocompatibility and functionality of the NPC-seeded scaffolds were evaluated in vivo in deafened guinea pigs ( Cavia porcellus ). To this end, we established an ouabain-based deafening procedure that depleted an average 72% of SGNs from apex to base of the cochleae and caused profound hearing loss. Further, we developed a surgical procedure to implant seeded scaffolds directly into the guinea pig IAM. No evidence of an inflammatory response was observed, but post-surgery tissue repair appeared to be facilitated by infiltrating Schwann cells. While NPC survival was found to be poor, both subjects implanted with NPC-seeded and cell-free control scaffolds showed partial recovery of electrically-evoked auditory brainstem thresholds. Thus, while future studies must address cell survival, nanofibrous scaffolds pose a promising strategy for auditory nerve regeneration. Impairment of spiral ganglion neurons (SGNs) of the auditory nerve is a major cause for hearing loss occurring independently or in addition to sensory hair cell damage. Unfortunately, mammalian SGNs lack the potential for autonomous regeneration. Stem cell based therapy is a promising approach for auditory nerve regeneration, but proper integration of exogenous cells into the auditory circuit remains a fundamental challenge. Here, we present novel nanofibrous scaffolds designed to guide the integration of human stem cell-derived neurons in the internal auditory meatus (IAM), the foramen allowing passage of the spiral ganglion to the auditory brainstem. Human embryonic stem cells (hESC) were differentiated into neural precursor cells (NPCs) and seeded onto aligned nanofiber mats. The NPCs terminally differentiated into glutamatergic neurons with high efficiency, and neurite projections aligned with nanofibers in vitro. Scaffolds were assembled by seeding GFP-labeled NPCs on nanofibers integrated in a polymer sheath. Biocompatibility and functionality of the NPC-seeded scaffolds were evaluated in vivo in deafened guinea pigs (Cavia porcellus). To this end, we established an ouabain-based deafening procedure that depleted an average 72% of SGNs from apex to base of the cochleae and caused profound hearing loss. Further, we developed a surgical procedure to implant seeded scaffolds directly into the guinea pig IAM. No evidence of an inflammatory response was observed, but post-surgery tissue repair appeared to be facilitated by infiltrating Schwann cells. While NPC survival was found to be poor, both subjects implanted with NPC-seeded and cell-free control scaffolds showed partial recovery of electrically-evoked auditory brainstem thresholds. Thus, while future studies must address cell survival, nanofibrous scaffolds pose a promising strategy for auditory nerve regeneration.Impairment of spiral ganglion neurons (SGNs) of the auditory nerve is a major cause for hearing loss occurring independently or in addition to sensory hair cell damage. Unfortunately, mammalian SGNs lack the potential for autonomous regeneration. Stem cell based therapy is a promising approach for auditory nerve regeneration, but proper integration of exogenous cells into the auditory circuit remains a fundamental challenge. Here, we present novel nanofibrous scaffolds designed to guide the integration of human stem cell-derived neurons in the internal auditory meatus (IAM), the foramen allowing passage of the spiral ganglion to the auditory brainstem. Human embryonic stem cells (hESC) were differentiated into neural precursor cells (NPCs) and seeded onto aligned nanofiber mats. The NPCs terminally differentiated into glutamatergic neurons with high efficiency, and neurite projections aligned with nanofibers in vitro. Scaffolds were assembled by seeding GFP-labeled NPCs on nanofibers integrated in a polymer sheath. Biocompatibility and functionality of the NPC-seeded scaffolds were evaluated in vivo in deafened guinea pigs (Cavia porcellus). To this end, we established an ouabain-based deafening procedure that depleted an average 72% of SGNs from apex to base of the cochleae and caused profound hearing loss. Further, we developed a surgical procedure to implant seeded scaffolds directly into the guinea pig IAM. No evidence of an inflammatory response was observed, but post-surgery tissue repair appeared to be facilitated by infiltrating Schwann cells. While NPC survival was found to be poor, both subjects implanted with NPC-seeded and cell-free control scaffolds showed partial recovery of electrically-evoked auditory brainstem thresholds. Thus, while future studies must address cell survival, nanofibrous scaffolds pose a promising strategy for auditory nerve regeneration. |
| Audience | Academic |
| Author | Corey, Joseph M. White, Christina Prieskorn, Diane M. Chan, Che He, Long Rastogi, Arjun Duncan, R. Keith Hackelberg, Sandra Loomis, Benjamin R. Miller, Josef M. Miller, Ryan J. Liu, Liqian Tuck, Samuel J. |
| AuthorAffiliation | 2 Geriatrics Research, Education, and Clinical Center (GRECC), VA Ann Arbor Healthcare Center (VAAAHC), Ann Arbor, MI, United States of America University of Pennsylvania, UNITED STATES 4 Departments of Otorhinolaryngology, Guangzhou First Peoples' Hospital and First Affiliated Hospital, School of Medicine, Jinan University, Guangdong, China 1 Kresge Hearing Research Institute, Department of Otolaryngology-Head & Neck Surgery, University of Michigan, Ann Arbor, MI, United States of America 6 Department of Neurology, University of Michigan, Ann Arbor, MI, United States of America 5 Department of Materials Science and Engineering, University of Michigan, Ann Arbor, MI, United States of America 3 Department of Biomedical Engineering, University of Michigan, Ann Arbor, MI, United States of America |
| AuthorAffiliation_xml | – name: University of Pennsylvania, UNITED STATES – name: 1 Kresge Hearing Research Institute, Department of Otolaryngology-Head & Neck Surgery, University of Michigan, Ann Arbor, MI, United States of America – name: 3 Department of Biomedical Engineering, University of Michigan, Ann Arbor, MI, United States of America – name: 2 Geriatrics Research, Education, and Clinical Center (GRECC), VA Ann Arbor Healthcare Center (VAAAHC), Ann Arbor, MI, United States of America – name: 4 Departments of Otorhinolaryngology, Guangzhou First Peoples' Hospital and First Affiliated Hospital, School of Medicine, Jinan University, Guangdong, China – name: 6 Department of Neurology, University of Michigan, Ann Arbor, MI, United States of America – name: 5 Department of Materials Science and Engineering, University of Michigan, Ann Arbor, MI, United States of America |
| Author_xml | – sequence: 1 givenname: Sandra orcidid: 0000-0003-2387-5451 surname: Hackelberg fullname: Hackelberg, Sandra – sequence: 2 givenname: Samuel J. surname: Tuck fullname: Tuck, Samuel J. – sequence: 3 givenname: Long surname: He fullname: He, Long – sequence: 4 givenname: Arjun surname: Rastogi fullname: Rastogi, Arjun – sequence: 5 givenname: Christina surname: White fullname: White, Christina – sequence: 6 givenname: Liqian surname: Liu fullname: Liu, Liqian – sequence: 7 givenname: Diane M. surname: Prieskorn fullname: Prieskorn, Diane M. – sequence: 8 givenname: Ryan J. surname: Miller fullname: Miller, Ryan J. – sequence: 9 givenname: Che surname: Chan fullname: Chan, Che – sequence: 10 givenname: Benjamin R. surname: Loomis fullname: Loomis, Benjamin R. – sequence: 11 givenname: Joseph M. surname: Corey fullname: Corey, Joseph M. – sequence: 12 givenname: Josef M. surname: Miller fullname: Miller, Josef M. – sequence: 13 givenname: R. Keith surname: Duncan fullname: Duncan, R. Keith |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/28672008$$D View this record in MEDLINE/PubMed |
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| Copyright | COPYRIGHT 2017 Public Library of Science 2017 Hackelberg et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2017 Hackelberg et al 2017 Hackelberg et al |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Conceptualization: RKD JMC JMM.Data curation: SH RKD LH AR DMP.Formal analysis: SH SJT LH AR LL DMP LH RJM BRL.Funding acquisition: RKD.Investigation: SH SJT LH AR CW LL DMP RJM CC BRL RKD.Methodology: SH SJT LH AR CW LL DMP RJM CC BRL JMC JMM RKD.Project administration: RKD SH.Resources: RKD.Supervision: RKD JMC JMM.Validation: SH RKD JMM JMC.Visualization: RKD SH SJT AR RJM BRL LH.Writing – original draft: SH RKD DMP.Writing – review & editing: SH RKD AR JMC JMM. Current address: Ken & Ruth Davee Department of Neurology, Feinberg School of Medicine, Northwestern University, Chicago, IL, United States of America Competing Interests: The authors have declared that no competing interests exist. |
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| Snippet | Impairment of spiral ganglion neurons (SGNs) of the auditory nerve is a major cause for hearing loss occurring independently or in addition to sensory hair... |
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| SubjectTerms | Alignment Animals Auditory nerve Biocompatibility Biocompatible Materials Biology and Life Sciences Biomedical engineering Biomedical materials Brain stem Brain Stem - physiology Cell Differentiation Cell survival Cell Transplantation Cellulose Circuit design Cochlear Nerve - physiology Deafness - therapy Education Embryo cells Embryonic Stem Cells - cytology Engineering and Technology Female Ganglion cells Gene expression Genetic aspects Geriatrics Glutamatergic transmission Green Fluorescent Proteins - genetics Guinea Pigs Hair Health aspects Hearing loss Humans In vitro methods and tests Inflammation Inflammatory response Integration Male Mammals Mats Medical imaging Medicine and Health Sciences Mineralization Nanofibers Nerve regeneration Nerve Regeneration - physiology Neurogenesis Neurons Neurons - cytology Otolaryngology Ouabain Physical Sciences Physiological aspects Polymers Regeneration Research and Analysis Methods Risk factors Scaffolds Schwann cells Spiral ganglion Stem cell transplantation Stem cells Surgery Surgical implants Survival Therapy Thresholds Tissue Engineering Transplants & implants |
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| Title | Nanofibrous scaffolds for the guidance of stem cell-derived neurons for auditory nerve regeneration |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/28672008 https://www.proquest.com/docview/1915544744 https://www.proquest.com/docview/1915876549 https://pubmed.ncbi.nlm.nih.gov/PMC5495534 https://doaj.org/article/6df7ef99e9354d7abb3dfe18dc7ac024 http://dx.doi.org/10.1371/journal.pone.0180427 |
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