Syngeneic Transplantation of Rat Olfactory Stem Cells in a Vein Conduit Improves Facial Movements and Reduces Synkinesis after Facial Nerve Injury.
Animals
Behavior Observation Techniques
Disease Models, Animal
Electromyography
Facial Nerve
/ physiopathology
Facial Nerve Injuries
/ complications
Facial Paralysis
/ diagnosis
Female
Femoral Vein
/ transplantation
Humans
Nerve Regeneration
/ physiology
Olfactory Mucosa
/ cytology
Rats
Recovery of Function
Stem Cell Transplantation
/ methods
Synkinesis
/ diagnosis
Transplantation, Isogeneic
/ methods
Vascular Grafting
/ methods
Vibrissae
/ innervation
Video Recording
Journal
Plastic and reconstructive surgery
ISSN: 1529-4242
Titre abrégé: Plast Reconstr Surg
Pays: United States
ID NLM: 1306050
Informations de publication
Date de publication:
12 2020
12 2020
Historique:
entrez:
25
11
2020
pubmed:
26
11
2020
medline:
16
1
2021
Statut:
ppublish
Résumé
Posttraumatic facial paralysis is a disabling condition. Current surgical management by faciofacial nerve suture provides limited recovery. To improve the outcome, the authors evaluated an add-on strategy based on a syngeneic transplantation of nasal olfactory stem cells in a rat model of facial nerve injury. The main readouts of the study were the recording of whisking function and buccal synkinesis. Sixty rats were allocated to three groups. Animals with a 2-mm facial nerve loss were repaired with a femoral vein, filled or not with olfactory stem cells. These two groups were compared to similarly injured rats but with a faciofacial nerve suture. Olfactory stem cells were purified from rat olfactory mucosa. Three months after surgery, facial motor performance was evaluated using video-based motion analysis and electromyography. Synkinesis was assessed by electromyography, using measure of buccal involuntary movements during blink reflex, and double retrograde labeling of regenerating motoneurons. The authors' study reveals that olfactory stem cell transplantation induces functional recovery in comparison to nontransplanted and faciofacial nerve suture groups. They significantly increase (1) maximal amplitude of vibrissae protraction and retraction cycles and (2) angular velocity during protraction of vibrissae. They also reduce buccal synkinesis, according to the two techniques used. However, olfactory stem cell transplantation did not improve axonal regrowth of the facial nerve, 3 months after surgery. The authors show here that the adjuvant strategy of syngeneic transplantation of olfactory stem cells improves functional recovery. These promising results open the way for a phase I clinical trial based on the autologous engraftment of olfactory stem cells in patients with a facial nerve paralysis.
Sections du résumé
BACKGROUND
Posttraumatic facial paralysis is a disabling condition. Current surgical management by faciofacial nerve suture provides limited recovery. To improve the outcome, the authors evaluated an add-on strategy based on a syngeneic transplantation of nasal olfactory stem cells in a rat model of facial nerve injury. The main readouts of the study were the recording of whisking function and buccal synkinesis.
METHODS
Sixty rats were allocated to three groups. Animals with a 2-mm facial nerve loss were repaired with a femoral vein, filled or not with olfactory stem cells. These two groups were compared to similarly injured rats but with a faciofacial nerve suture. Olfactory stem cells were purified from rat olfactory mucosa. Three months after surgery, facial motor performance was evaluated using video-based motion analysis and electromyography. Synkinesis was assessed by electromyography, using measure of buccal involuntary movements during blink reflex, and double retrograde labeling of regenerating motoneurons.
RESULTS
The authors' study reveals that olfactory stem cell transplantation induces functional recovery in comparison to nontransplanted and faciofacial nerve suture groups. They significantly increase (1) maximal amplitude of vibrissae protraction and retraction cycles and (2) angular velocity during protraction of vibrissae. They also reduce buccal synkinesis, according to the two techniques used. However, olfactory stem cell transplantation did not improve axonal regrowth of the facial nerve, 3 months after surgery.
CONCLUSIONS
The authors show here that the adjuvant strategy of syngeneic transplantation of olfactory stem cells improves functional recovery. These promising results open the way for a phase I clinical trial based on the autologous engraftment of olfactory stem cells in patients with a facial nerve paralysis.
Identifiants
pubmed: 33234960
doi: 10.1097/PRS.0000000000007367
pii: 00006534-202012000-00016
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1295-1305Références
Ichihara S, Inada Y, Nakamura T. Artificial nerve tubes and their application for repair of peripheral nerve injury: An update of current concepts. Injury. 2008; 39Suppl 429–39
Murrell W, Féron F, Wetzig A, et al. Multipotent stem cells from adult olfactory mucosa. Dev Dyn. 2005; 233:496–515
Huard JM, Youngentob SL, Goldstein BJ, Luskin MB, Schwob JE. Adult olfactory epithelium contains multipotent progenitors that give rise to neurons and non-neural cells. J Comp Neurol. 1998; 400:469–486
Girard SD, Devéze A, Nivet E, Gepner B, Roman FS, Féron F. Isolating nasal olfactory stem cells from rodents or humans. J Vis Exp. 2011; 54:2762
Féron F, Perry C, Girard SD, Mackay-Sim A. Isolation of adult stem cells from the human olfactory mucosa. Methods Mol Biol. 2013; 1059:107–114
Ould-Yahoui A, Sbai O, Baranger K, et al. Role of matrix metalloproteinases in migration and neurotrophic properties of nasal olfactory stem and ensheathing cells. Cell Transplant. 2013; 22:993–1010
Delorme B, Nivet E, Gaillard J, et al. The human nose harbors a niche of olfactory ectomesenchymal stem cells displaying neurogenic and osteogenic properties. Stem Cells Dev. 2010; 19:853–866
Xiao M, Klueber KM, Zhou J, et al. Human adult olfactory neural progenitors promote axotomized rubrospinal tract axonal reinnervation and locomotor recovery. Neurobiol Dis. 2007; 26:363–374
Murrell W, Wetzig A, Donnellan M, et al. Olfactory mucosa is a potential source for autologous stem cell therapy for Parkinson’s disease. Stem Cells. 2008; 26:2183–2192
Doyle KL, Kazda A, Hort Y, McKay SM, Oleskevich S. Differentiation of adult mouse olfactory precursor cells into hair cells in vitro. Stem Cells. 2007; 25:621–627
Pandit SR, Sullivan JM, Egger V, Borecki AA, Oleskevich S. Functional effects of adult human olfactory stem cells on early-onset sensorineural hearing loss. Stem Cells. 2011; 29:670–677
Nivet E, Vignes M, Girard SD, et al. Engraftment of human nasal olfactory stem cells restores neuroplasticity in mice with hippocampal lesions. J Clin Invest. 2011; 121:2808–2820
Neely JG, Neufeld PS. Defining functional limitation, disability, and societal limitations in patients with facial paresis: Initial pilot questionnaire. Am J Otol. 1996; 17:340–342
Volk GF, Pantel M, Guntinas-Lichius O. Modern concepts in facial nerve reconstruction. Head Face Med. 2010; 6:25
Placheta E, Wood MD, Lafontaine C, et al. Enhancement of facial nerve motoneuron regeneration through cross-face nerve grafts by adding end-to-side sensory axons. Plast Reconstr Surg. 2015; 135:460–471
Kaya Y, Ozsoy U, Turhan M, Angelov DN, Sarikcioglu L. Hypoglossal-facial nerve reconstruction using a Y-tube-conduit reduces aberrant synkinetic movements of the orbicularis oculi and vibrissal muscles in rats. Biomed Res Int. 2014; 2014:543020
Ozsoy U, Demirel BM, Hizay A, et al. Manual stimulation of the whisker pad after hypoglossal-facial anastomosis (HFA) using a Y-tube conduit does not improve recovery of whisking function. Exp Brain Res. 2014; 232:2021–2033
Hizay A, Ozsoy U, Demirel BM, et al. Use of a Y-tube conduit after facial nerve injury reduces collateral axonal branching at the lesion site but neither reduces polyinnervation of motor endplates nor improves functional recovery. Neurosurgery. 2012; 70:1544–1556. discussion 1556
Guntinas-Lichius O, Glowka TR, Angelov DN, Irintchev A, Neiss WF. Improved functional recovery after facial nerve reconstruction by temporary denervation of the contralateral mimic musculature with botulinum toxin in rats. Neurorehabil Neural Repair. 2011; 25:15–23
Bischoff A, Grosheva M, Irintchev A, et al. Manual stimulation of the orbicularis oculi muscle improves eyelid closure after facial nerve injury in adult rats. Muscle Nerve. 2009; 39:197–205
Sinis N, Horn F, Genchev B, et al. Electrical stimulation of paralyzed vibrissal muscles reduces endplate reinnervation and does not promote motor recovery after facial nerve repair in rats. Ann Anat. 2009; 191:356–370
Angelov DN, Ceynowa M, Guntinas-Lichius O, et al. Mechanical stimulation of paralyzed vibrissal muscles following facial nerve injury in adult rat promotes full recovery of whisking. Neurobiol Dis. 2007; 26:229–242
Guntinas-Lichius O, Irintchev A, Streppel M, et al. Factors limiting motor recovery after facial nerve transection in the rat: Combined structural and functional analyses. Eur J Neurosci. 2005; 21:391–402
Tomov TL, Guntinas-Lichius O, Grosheva M, et al. An example of neural plasticity evoked by putative behavioral demand and early use of vibrissal hairs after facial nerve transection. Exp Neurol. 2002; 178:207–218
Batioglu-Karaaltin A, Karaaltin MV, Oztel ON, et al. Human olfactory stem cells for injured facial nerve reconstruction in a rat model. Head Neck. 2016; 38XXXSuppl 1E2011–E2020
Rivera A, Raymond M, Grobman A, Abouyared M, Angeli SI. The effect of n-acetyl-cysteine on recovery of the facial nerve after crush injury. Laryngoscope Investig Otolaryngol. 2017; 2:109–112
Byrne PJ, Stuart RM, Fakhry C, Lehar M, Flint PW. An electrophysiologic model for functional assessment of effects of neurotrophic factors on facial nerve reinnervation. Arch Facial Plast Surg. 2005; 7:114–118
Yasui G, Yamamoto Y, Shichinohe R, et al. Neuregulin-1 released by biodegradable gelatin hydrogels can accelerate facial nerve regeneration and functional recovery of traumatic facial nerve palsy. J Plast Reconstr Aesthet Surg. 2016; 69:328–334
Ono K, Yamamoto Y, Shichinohe R, et al. Exploration of more effective neurorrhaphy in facial nerve reconstruction: A comparison focusing on the difference of neural window size and condition of the neurorrhaphy site. J Plast Reconstr Aesthet Surg. 2016; 69:1072–1079
Guérout N, Paviot A, Bon-Mardion N, et al. Co-transplantation of olfactory ensheathing cells from mucosa and bulb origin enhances functional recovery after peripheral nerve lesion. PLoS One. 2011; 6:e22816
Guntinas-Lichius O, Streppel M, Stennert E. Postoperative functional evaluation of different reanimation techniques for facial nerve repair. Am J Surg. 2006; 191:61–67
Boyd JG, Gordon T. Neurotrophic factors and their receptors in axonal regeneration and functional recovery after peripheral nerve injury. Mol Neurobiol. 2003; 27:277–324
Gravel C, Götz R, Lorrain A, Sendtner M. Adenoviral gene transfer of ciliary neurotrophic factor and brain-derived neurotrophic factor leads to long-term survival of axotomized motor neurons. Nat Med. 1997; 3:765–770
Hood B, Levene HB, Levi AD. Transplantation of autologous Schwann cells for the repair of segmental peripheral nerve defects. Neurosurg Focus. 2009; 26:E4
Radtke C, Aizer AA, Agulian SK, Lankford KL, Vogt PM, Kocsis JD. Transplantation of olfactory ensheathing cells enhances peripheral nerve regeneration after microsurgical nerve repair. Brain Res. 2009; 1254:10–17
Guérout N, Duclos C, Drouot L, et al. Transplantation of olfactory ensheathing cells promotes axonal regeneration and functional recovery of peripheral nerve lesion in rats. Muscle Nerve. 2011; 43:543–551
Ge L, Jiang M, Duan D, et al. Secretome of olfactory mucosa mesenchymal stem cell, a multiple potential stem cell. Stem Cells Int. 2016; 2016:1243659
Girard SD, Virard I, Lacassagne E, et al. From blood to lesioned brain: An in vitro study on migration mechanisms of human nasal olfactory stem cells. Stem Cells Int. 2017; 2017:1478606
Di Trapani M, Bassi G, Ricciardi M, et al. Comparative study of immune regulatory properties of stem cells derived from different tissues. Stem Cells Dev. 2013; 22:2990–3002
Rui K, Zhang Z, Tian J, et al. Olfactory ecto-mesenchymal stem cells possess immunoregulatory function and suppress autoimmune arthritis. Cell Mol Immunol. 2016; 13:401–408
Forni PE, Wray S. Neural crest and olfactory system: New prospective. Mol Neurobiol. 2012; 46:349–360
Duan D, Lu M. Olfactory mucosa: A rich source of cell therapy for central nervous system repair. Rev Neurosci. 2015; 26:281–293
Alvites RD, Caseiro AR, Pedrosa SS, Branquinho ME, Varejão ASP, Mauricio AC. The nasal cavity of the rat and mouse: Source of mesenchymal stem cells for treatment of peripheral nerve injury. Anat Rec (Hoboken). 2018; 301:1678–1689
Young E, Westerberg B, Yanai A, Gregory-Evans K. The olfactory mucosa: A potential source of stem cells for hearing regeneration. Regen Med. 2018; 13:581–593
Harrell CR, Jovicic N, Djonov V, Arsenijevic N, Volarevic V. Mesenchymal stem cell-derived exosomes and other extracellular vesicles as new remedies in the therapy of inflammatory diseases. Cells. 2019; 8:1605
Clark K, Zhang S, Barthe S, et al. Placental mesenchymal stem cell-derived extracellular vesicles promote myelin regeneration in an animal model of multiple sclerosis. Cells. 2019; 8:1497
Bonafede R, Brandi J, Manfredi M, et al. The anti-apoptotic effect of ASC-exosomes in an in vitro ALS model and their proteomic analysis. Cells. 2019; 8:1087
Galieva LR, James V, Mukhamedshina YO, Rizvanov AA. Therapeutic potential of extracellular vesicles for the treatment of nerve disorders. Front Neurosci. 2019; 13:163
Otero-Ortega L, Gómez de Frutos MC, Laso-García F, et al. Exosomes promote restoration after an experimental animal model of intracerebral hemorrhage. J Cereb Blood Flow Metab. 2018; 38:767–779
Alvarez-Erviti L, Seow Y, Yin H, Betts C, Lakhal S, Wood MJ. Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat Biotechnol. 2011; 29:341–345
Kooijmans SAA, Aleza CG, Roffler SR, van Solinge WW, Vader P, Schiffelers RM. Display of GPI-anchored anti-EGFR nanobodies on extracellular vesicles promotes tumour cell targeting. J Extracell Vesicles. 2016; 5:31053