Olfactory mucosa: a rich source of cell therapy for central nervous system repair

References

Agrawal, A.K., Shukla, S., Chaturvedi, R.K., Seth, K., Srivastava, N., Ahmad, A., and Seth, P.K. (2004). Olfactory ensheathing cell transplantation restores functional deficits in rat model of Parkinson’s disease: a cotransplantation approach with fetal ventral mesencephalic cells. Neurobiol. Dis. 16, 516–526.10.1016/j.nbd.2004.04.014Search in Google Scholar

Amariglio, N., Hirshberg, A., Scheithauer, B.W., Cohen, Y., Loewenthal, R., Trakhtenbrot, L., Paz, N., Koren-Michowitz, M., Waldman, D., Leider-Trejo, L., et al. (2009). Donor-derived brain tumor following neural stem cell transplantation in an ataxia telangiectasia patient. PLoS Med. 6, e1000029.10.1371/journal.pmed.1000029Search in Google Scholar

Ambasudhan, R., Dolatabadi, N., Nutter, A., Masliah, E., Mckercher, S.R., and Lipton, S.A. (2014). Potential for cell therapy in Parkinson’s disease using genetically programmed human embryonic stem cell-derived neural progenitor cells. J. Comp. Neurol. 522, 2845–2856.10.1002/cne.23617Search in Google Scholar

Aoki, M., Kishima, H., Yoshimura, K., Ishihara, M., Ueno, M., Hata, K., Yamashita, T., Iwatsuki, K., and Yoshimine, T. (2010). Limited functional recovery in rats with complete spinal cord injury after transplantation of whole-layer olfactory mucosa: laboratory investigation. J. Neurosurg. Spine 12, 122–130.10.3171/2009.9.SPINE09233Search in Google Scholar

Barnett, S.C. and Chang, L. (2004). Olfactory ensheathing cells and CNS repair: going solo or in need of a friend. Trends Neurosci. 27, 54–60.10.1016/j.tins.2003.10.011Search in Google Scholar

Barraud, P., Seferiadis, A.A., Tyson, L.D., Zwart, M.F., Szabo-Rogers, H.L., Ruhrberg, C., Liu, K.J., and Baker, C.V. (2010). Neural crest origin of olfactory ensheathing glia. Proc. Natl. Acad. Sci. USA 107, 21040–21045.10.1073/pnas.1012248107Search in Google Scholar

Beites, C.L., Kawauchi, S., Crocker, C.E., and Calof, A.L. (2005). Identification and molecular regulation of neural stem cells in the olfactory epithelium. Exp. Cell. Res. 306, 309–316.10.1016/j.yexcr.2005.03.027Search in Google Scholar

Boone, N., Loriod, B., Bergon, A., Sbai, O., Formisano-Tréziny, C., Gabert, J., Khrestchatisky, M., Nguyen, C., Féron, F., Axelrod, F.B., et al. (2010). Olfactory stem cells, a new cellular model for studying molecular mechanisms underlying familial dysautonomia. PLoS One 5, e15590.10.1371/journal.pone.0015590Search in Google Scholar

Caggiano, M., Kauer, J.S., and Hunter, D.D. (1994). Globose basal cells are neuronal progenitors in the olfactory epithelium: a lineage analysis using a replication-incompetent retrovirus. Neuron 13, 339–352.10.1016/0896-6273(94)90351-4Search in Google Scholar

Carter, L.A., MacDonald, J.L., and Roskams, A.J. (2004). Olfactory horizontal basal cells demonstrate a conserved multipotent progenitor phenotype. J. Neurosci. 24, 5670–5683.10.1523/JNEUROSCI.0330-04.2004Search in Google Scholar PubMed PubMed Central

Centenaro, L.A., Jaeger Mda, C., Ilha, J., de Souza, M.A., Kalil-Gaspar, P.I., Cunha, N.B., Marcuzzo, S., and Achaval, M. (2011). Olfactory and respiratory lamina propria transplantation after spinal cord transection in rats: effects on functional recovery and axonal regeneration. Brain Res. 1426, 54–72.10.1016/j.brainres.2011.09.054Search in Google Scholar PubMed

Centenaro, L.A., da Cunha Jaeger, M., Ilha, J., de Souza, M.A., Balbinot, L.F., do Nascimento, P.S., Marcuzzo, S., and Achaval, M. (2013). Implications of olfactory lamina propria transplantation on hyperreflexia and myelinated fiber regeneration in rats with complete spinal cord transection. Neurochem. Res. 38, 371–381.10.1007/s11064-012-0928-5Search in Google Scholar PubMed

Chen, X., Fang, H., and Schwob, J.E. (2004). Multipotency of purified, transplanted globose basal cells in olfactory epithelium. J. Comp. Neurol. 469, 457–474.10.1002/cne.11031Search in Google Scholar PubMed

Chen, M., Tian, S., Yang, X., Reed, R.R., and Liu, H. (2014). Wnt-responsive Lgr5⁺ globose basal cells function as multipotent olfactory epithelium progenitor cells. J. Neurosci. 34, 8268–8276.10.1523/JNEUROSCI.0240-14.2014Search in Google Scholar PubMed PubMed Central

Chernykh, E.R., Shevela, E.Y., Leplina, O.Y., Tikhonova, M.A., Ostanin, A.A., Kulagin, A.D., Pronkina, N.V., Muradov, Zh.M., Stupak, V.V., and Kozlov, V.A. (2006). Characteristics of bone marrow cells under conditions of impaired innervation in patients with spinal trauma. Bull. Exp. Biol. Med. 141, 117–120.10.1007/s10517-006-0109-0Search in Google Scholar PubMed

Delorme, B., Nivet, E., Gaillard, J., Häupl, T., Ringe, J., Devèze, A., Magnan, J., Sohier, J., Khrestchatisky, M., Roman, F.S., et al. (2010). The human nose harbors a niche of olfactory ectomesenchymal stem cells displaying neurogenic and osteogenic properties. Stem Cells Dev. 19, 853–866.10.1089/scd.2009.0267Search in Google Scholar PubMed

Diaz-Solano, D., Wittig, O., Ayala-Grosso, C., Pieruzzini, R., and Cardier, J.E. (2012). Human olfactory mucosa multipotent mesenchymal stromal cells promote survival, proliferation, and differentiation of human hematopoietic cells. Stem Cells Dev. 21, 3187–3196.10.1089/scd.2012.0084Search in Google Scholar PubMed PubMed Central

Dlouhy, B.J., Awe, O., Rao, R.C., Kirby, P.A., and Hitchon, P.W. (2014). Autograft-derived spinal cord mass following olfactory mucosal cell transplantation in a spinal cord injury patient. J. Neurosurg. Spine 21, 618–622.10.3171/2014.5.SPINE13992Search in Google Scholar PubMed

Doucette, R. (1990). Glial influences on axonal growth in the primary olfactory system. Glia. 3, 433–449.10.1002/glia.440030602Search in Google Scholar PubMed

Duan, D., Rong, M., Zeng, Y., Teng, X., Zhao, Z., Liu, B., Tao, X., Zhou, R., Fan, M., Peng, C., et al. (2011). Electrophysiological characterization of NSCs after differentiation induced by OEC conditioned medium. Acta Neurochir. (Vienna) 153, 2085–2090.10.1007/s00701-011-0955-zSearch in Google Scholar PubMed

Duggan, C.D. and Ngai, J. (2007). Scent of a stem cell. Nat. Neurosci. 10, 673–674.10.1038/nn0607-673Search in Google Scholar PubMed

Féron, F., Perry, C., Cochrane, J., Licina, P., Nowitzke, A., Urquhart, S., Geraghty, T., and Mackay-Sim, A. (2005). Autologous olfactory ensheathing cell transplantation in human spinal cord injury. Brain 128, 2951–2960.10.1093/brain/awh657Search in Google Scholar PubMed

Fletcher, R.B., Prasol, M.S., Estrada, J., Baudhuin, A., Vranizan, K., Choi, Y.G., and Ngai, J. (2011). p63 regulates olfactory stem cell self-renewal and differentiation. Neuron 72, 748–759.10.1016/j.neuron.2011.09.009Search in Google Scholar PubMed PubMed Central

García-Escudero, V., García-Gómez, A., Langa, E., Martín-Bermejo, M.J., Ramírez-Camacho, R., García-Berrocal, J.R., Moreno-Flores, M.T., Avila, J., and Lim, F. (2012). Patient-derived olfactory mucosa cells but not lung or skin fibroblasts mediate axonal regeneration of retinal ganglion neurons. Neurosci. Lett. 509, 27–32.10.1016/j.neulet.2011.12.037Search in Google Scholar PubMed

Girard, S.D., Devéze, A., Nivet, E., Gepner, B., Roman, F.S., and Féron, F. (2011). Isolating nasal olfactory stem cells from rodents or humans. J. Vis. Exp. pii: 2762.Search in Google Scholar

Goldstein, B.J. and Schwob, J.E. (1996). Analysis of the globose basal cell compartment in rat olfactory epithelium using GBC-1, a new monoclonal antibody against globose basal cells. J. Neurosci. 16, 4005–4016.10.1523/JNEUROSCI.16-12-04005.1996Search in Google Scholar

Goldstein, B.J., Hare, J.M., Lieberman, S., and Casiano, R. (2013). Adult human nasal mesenchymal stem cells have an unexpected broad anatomic distribution. Int. Forum Allergy Rhinol. 3, 550–555.10.1002/alr.21153Search in Google Scholar PubMed

Goni, V.G., Chhabra, R., Gupta, A., Marwaha, N., Dhillon, M.S., Pebam, S., Gopinathan, N.R., and Kantharajanna, S. (2014). Safety profile, feasibility and early clinical outcome of cotransplantation of olfactory mucosa and bone marrow stem cells in chronic spinal cord injury patients. Asian Spine J. 8, 484–490.10.4184/asj.2014.8.4.484Search in Google Scholar PubMed PubMed Central

Gordon, M.K., Mumm, J.S., Davis, R.A., Holcomb, J.D., and Calof, A.L. (1995). Dynamics of MASH1 expression in vitro and in vivo suggest a non-stem cell site of MASH1 action in the olfactory receptor neuron lineage. Mol. Cell. Neurosci. 6, 363–379.10.1006/mcne.1995.1028Search in Google Scholar PubMed

Gorrie, C.A., Hayward, I., Cameron, N., Kailainathan, G., Nandapalan, N., Sutharsan, R., Wang, J., Mackay-Sim, A., and Waite, P.M. (2010). Effects of human OEC-derived cell transplants in rodent spinal cord contusion injury. Brain Res. 1337, 8–20.10.1016/j.brainres.2010.04.019Search in Google Scholar PubMed

Granger, N., Blamires, H., Franklin, R.J., and Jeffery, N.D. (2012). Autologous olfactory mucosal cell transplants in clinical spinal cord injury: a randomized double-blinded trial in a canine translational model. Brain 135, 3227–3237.10.1093/brain/aws268Search in Google Scholar PubMed PubMed Central

Guérout, N., Derambure, C., Drouot, L., Bon-Mardion, N., Duclos, C., Boyer, O., and Marie, J.P. (2010). Comparative gene expression profiling of olfactory ensheathing cells from olfactory bulb and olfactory mucosa. Glia 58, 1570–1580.10.1002/glia.21030Search in Google Scholar

Guérout, N., Paviot, A., Bon-Mardion, N., Duclos, C., Genty, D., Jean, L., Boyer, O., and Marie, J.P. (2011). Co-transplantation of olfactory ensheathing cells from mucosa and bulb origin enhances functional recovery after peripheral nerve lesion. PLoS One 6, e22816.10.1371/journal.pone.0022816Search in Google Scholar

Han, Q., Xiang, J., Zhang, Y., Qiao, H., Shen, Y., and Zhang, C. (2014). Enhanced neuroprotection and improved motor function in traumatized rat spinal cords by rAAV2-mediated glial-derived neurotrophic factor combined with early rehabilitation training. Chin. Med. J. (Engl.) 127, 4220–4225.Search in Google Scholar

Holbrook, E.H., Szumowski, K.E., and Schwob, J.E. (1995). An immunochemical, ultrastructural, and developmental characterization of the horizontal basal cells of rat olfactory epithelium. J. Comp. Neurol. 363, 129–146.10.1002/cne.903630111Search in Google Scholar

Huard, J.M., Youngentob, S.L., Goldstein, B.J., Luskin, M.B., and Schwob, J.E. (1998). Adult olfactory epithelium contains multipotent progenitors that give rise to neurons and non-neural cells. J. Comp. Neurol. 400, 469–486.10.1002/(SICI)1096-9861(19981102)400:4<469::AID-CNE3>3.0.CO;2-8Search in Google Scholar

Hubbard, I.J., Carey, L.M., Budd, T.W., Levi, C., McElduff, P., Hudson, S., Bateman, G., and Parsons, M.W. (2014). A randomized controlled trial of the effect of early upper-limb training on stroke recovery and brain activation. Neurorehabil. Neural. Repair. Epub ahead of print.Search in Google Scholar

Ibrahim, A., Li, D., Collins, A., Tabakow, P., Raisman, G., and Li, Y. (2014). Comparison of olfactory bulbar and mucosal cultures in a rat rhizotomy model. Cell Transplant. 23, 1465–1470.10.3727/096368913X676213Search in Google Scholar

Ishihara, M., Mochizuki-Oda, N., Iwatsuki, K., Kishima, H., Ohnishi, Y., Moriwaki, T., Umegaki, M., and Yoshimine, T. (2014). Primary olfactory mucosal cells promote axonal outgrowth in a three-dimensional assay. J. Neurosci. Res. 92, 847–855.10.1002/jnr.23367Search in Google Scholar

Iwai, N., Zhou, Z., Roop, D.R., and Behringer, R.R. (2008). Horizontal basal cells are multipotent progenitors in normal and injured adult olfactory epithelium. Stem Cells 26, 1298–1306.10.1634/stemcells.2007-0891Search in Google Scholar

Jang, W., Youngentob, S.L., and Schwob, J.E. (2003). Globose basal cells are required for reconstitution of olfactory epithelium after methyl bromide lesion. J. Comp. Neurol. 460, 123–140.10.1002/cne.10642Search in Google Scholar

Johnson, T.S., O’Neill, A.C., Motarjem, P.M., Nazzal, J., Randolph, M., and Winograd, J.M. (2008). Tumor formation following murine neural precursor cell transplantation in a rat peripheral nerve injury model. J. Reconstr. Microsurg. 24, 545–550.10.1055/s-0028-1088228Search in Google Scholar

Kachramanoglou, C., Law, S., Andrews, P., Li, D., and Choi, D. (2013). Culture of olfactory ensheathing cells for central nerve repair: the limitations and potential of endoscopic olfactory mucosal biopsy. Neurosurgery 72, 170–178.10.1227/NEU.0b013e31827b99beSearch in Google Scholar

Kalincik, T., Jozefcikova, K., Sutharsan, R., Mackay-Sim, A., Carrive, P., and Waite, P.M. (2010). Selected changes in spinal cord morphology after T4 transection and olfactory ensheathing cell transplantation. Auton. Neurosci. 158, 31–38.10.1016/j.autneu.2010.05.011Search in Google Scholar PubMed

Katoh, H., Shibata, S., Fukuda, K., Sato, M., Satoh, E., Nagoshi, N., Minematsu, T., Matsuzaki, Y., Akazawa, C., Toyama, Y., et al. (2011). The dual origin of the peripheral olfactory system: placode and neural crest. Mol. Brain 4, 34.10.1186/1756-6606-4-34Search in Google Scholar PubMed PubMed Central

Krolewski, R.C., Packard, A., and Schwob, J.E. (2013). Global expression profiling of globose basal cells and neurogenic progression within the olfactory epithelium. J. Comp. Neurol. 521, 833–859.10.1002/cne.23204Search in Google Scholar PubMed PubMed Central

Kueh, J.L., Raisman, G., Li, Y., Stevens, R., and Li, D. (2011). Comparison of bulbar and mucosal olfactory ensheathing cells using FACS and simultaneous antigenic bivariate cell cycle analysis. Glia 59, 1658–1671.10.1002/glia.21213Search in Google Scholar PubMed

Lakatos, A., Smith, P.M., Barnett, S.C., and Franklin, R.J. (2003). Meningeal cells enhance limited CNS remyelination by transplanted olfactory ensheathing cells. Brain 126, 598–609.10.1093/brain/awg055Search in Google Scholar PubMed

Leung, C.T., Coulombe, P.A., and Reed, R.R. (2007). Contribution of olfactory neural stem cells to tissue maintenance and regeneration. Nat. Neurosci. 10, 720–726.10.1038/nn1882Search in Google Scholar PubMed

Li, Y., Field, P.M., and Raisman, G. (2005). Olfactory ensheathing cells and olfactory nerve fibroblasts maintain continuous open channels for regrowth of olfactory nerve fibres. Glia 52, 245–251.10.1002/glia.20241Search in Google Scholar PubMed

Lim, H., Sharoukhov, D., Kassim, I., Zhang, Y., Salzer, J.L., and Melendez-Vasquez, C.V. (2014). Label-free imaging of Schwann cell myelination by third harmonic generation microscopy. Proc. Natl. Acad. Sci. USA 111, 18025–18030.10.1073/pnas.1417820111Search in Google Scholar PubMed PubMed Central

Lima, C., Pratas-Vital, J., Escada, P., Hasse-Ferreira, A., Capucho, C., and Peduzzi, J.D. (2006). Olfactory mucosa autografts in human spinal cord injury, a pilot clinical study. J. Spinal Cord Med. 29, 191–203.10.1080/10790268.2006.11753874Search in Google Scholar PubMed PubMed Central

Lima, C., Escada, P., Pratas-Vital, J., Branco, C., Arcangeli, C.A., Lazzeri, G., Maia, C.A., Capucho, C., Hasse-Ferreira, A., and Peduzzi, J.D. (2010). Olfactory mucosal autografts and rehabilitation for chronic traumatic spinal cord injury. Neurorehabil, Neural Repair 24, 10–22.10.1177/1545968309347685Search in Google Scholar PubMed

Lindsay, S.L., Riddell, J.S., and Barnett, S.C. (2010). Olfactory mucosa for transplant-mediated repair: a complex tissue for a complex injury. Glia 58, 125–134.10.1002/glia.20917Search in Google Scholar

Lindsay, S.L., Johnstone, S.A., Mountford, J.C., Sheikh, S., Allan, D.B., Clark, L., and Barnett, S.C. (2013). Human mesenchymal stem cells isolated from olfactory biopsies but not bone enhance CNS myelination in vitro. Glia 61, 368–382.10.1002/glia.22440Search in Google Scholar

Lu, Q.R., Yuk, D., Alberta, J.A., Zhu, Z., Pawlitzky, I., Chan, J., McMahon, A.P., Stiles, C.D., and Rowitch, D.H. (2000). Sonic hedgehog – regulated oligodendrocyte lineage genes encoding bHLH proteins in the mammalian central nervous system. Neuron 25, 317–329.10.1016/S0896-6273(00)80897-1Search in Google Scholar

Mackay-Sim, A., Féron, F., Cochrane, J., Bassingthwaighte, L., Bayliss, C., Davies, W., Fronek, P., Gray, C., Kerr, G., Licina, P., et al. (2008). Autologous olfactory ensheathing cell transplantation in human paraplegia: a 3-year clinical trial. Brain 131, 2376–2386.10.1093/brain/awn173Search in Google Scholar

Marshall, C.A., Novitch, B.G., and Goldman, J.E. (2005). Olig2 directs astrocyte and oligodendrocyte formation in postnatal subventricular zone cells. J. Neurosci. 25, 7289–7298.10.1523/JNEUROSCI.1924-05.2005Search in Google Scholar

Mayeur, A., Duclos, C., Honoré, A., Gauberti, M., Drouot, L., do Rego, J.C., Bon-Mardion, N., Jean, L., Vérin, E., Emery, E., et al. (2013). Potential of olfactory ensheathing cells from different sources for spinal cord repair. PLoS One 8, e62860.10.1371/journal.pone.0062860Search in Google Scholar

Mendoza, A.S., Breipohl, W., and Miragall, F. (1982). Cell migration from the chick olfactory placode: a light and electron microscopic study. J. Embryol. Exp. Morphol. 69, 47–59.10.1242/dev.69.1.47Search in Google Scholar

Miragall, F., Kadmon, G., Husmann, M., and Schachner M. (1988). Expression of cell adhesion molecules in the olfactory system of the adult mouse: presence of the embryonic form of N-CAM. Dev. Biol. 129, 516–531.10.1016/0012-1606(88)90397-1Search in Google Scholar

Miragall, F., Kadmon, G., and Schachner, M. (1989). Expression of L1 and N-CAM cell adhesion molecules during development of the mouse olfactory system. Dev. Biol. 135, 272–286.10.1016/0012-1606(89)90179-6Search in Google Scholar

Moriwaki, T., Iwatsuki, K., Mochizuki-Oda, N., Ohnishi, Y., Ishihara, M., Umegaki, M., Ninomiya, K., and Yoshimine, T. (2014). Presence of trans-synaptic neurons derived from olfactory mucosa transplanted after spinal cord injury. Spine (Phila Pa 1976). 39, 1267–1273.10.1097/BRS.0000000000000386Search in Google Scholar PubMed

Murrell, W., Féron, F., Wetzig, A., Cameron, N., Splatt, K., Bellette, B., Bianco, J., Perry, C., Lee, G., and Mackay-Sim, A. (2005). Multipotent stem cells from adult olfactory mucosa. Dev. Dyn. 233, 496–515.10.1002/dvdy.20360Search in Google Scholar PubMed

Murrell, W., Wetzig, A., Donnellan, M., Féron, F., Burne, T., Meedeniya, A., Kesby, J., Bianco, J., Perry, C., Silburn, P., et al. (2008). Olfactory mucosa is a potential source for autologous stem cell therapy for Parkinson’s disease. Stem Cells 26, 2183–2192.10.1634/stemcells.2008-0074Search in Google Scholar PubMed

Nivet, E., Vignes, M., Girard, S.D., Pierrisnard, C., Baril, N., Devèze, A., Magnan, J., Lanté, F., Khrestchatisky, M., Féron, F., et al. (2011). Engraftment of human nasal olfactory stem cells restores neuroplasticity in mice with hippocampal lesions. J. Clin. Invest. 121, 2808–2820.10.1172/JCI44489Search in Google Scholar PubMed PubMed Central

Novikova, L.N., Lobov, S., Wiberg, M., and Novikov, L.N. (2011). Efficacy of olfactory ensheathing cells to support regeneration after spinal cord injury is influenced by method of culture preparation. Exp. Neurol. 229, 132–142.10.1016/j.expneurol.2010.09.021Search in Google Scholar PubMed

Ohnishi, Y., Iwatsuki, K., Shinzawa, K., Ishihara, M., Moriwaki, T., Umegaki, M., Kishima, H., and Yoshimine, T. (2013). Adult olfactory sphere cells are a source of oligodendrocyte and Schwann cell progenitors. Stem Cell Res. 11, 1178–1190.10.1016/j.scr.2013.08.005Search in Google Scholar PubMed

Ould-Yahoui, A., Sbai, O., Baranger, K., Bernard, A., Gueye, Y., Charrat, E., Clément, B., Gigmes, D., Dive, V., Girard, S.D., et al. (2013). Role of matrix metalloproteinases in migration and neurotrophic properties of nasal olfactory stem and ensheathing cells. Cell Transplant. 22, 993–1010.10.3727/096368912X657468Search in Google Scholar PubMed

Packard, A., Giel-Moloney, M., Leiter, A., and Schwob, J.E. (2011a). Progenitor cell capacity of NeuroD1-expressing globose basal cells in the mouse olfactory epithelium. J. Comp. Neurol. 519, 3580–3596.10.1002/cne.22726Search in Google Scholar PubMed PubMed Central

Packard, A., Schnittke, N., Romano, R.A., Sinha, S., and Schwob, J.E. (2011b). DeltaNp63 regulates stem cell dynamics in the mammalian olfactory epithelium. J. Neurosci. 31, 8748–8759.10.1523/JNEUROSCI.0681-11.2011Search in Google Scholar PubMed PubMed Central

Paviot, A., Guérout, N., Bon-Mardion, N., Duclos, C., Jean, L., Boyer, O., and Marie, J.P. (2011). Efficiency of laryngeal motor nerve repair is greater with bulbar than with mucosal olfactory ensheathing cells. Neurobiol. Dis. 41, 688–694.10.1016/j.nbd.2010.12.004Search in Google Scholar PubMed

Petrelli, A., Kaesberg, S., Barbe, M.T., Timmermann, L., Rosen, J.B., Fink, G.R., Kessler, J., and Kalbe, E. (2014). Cognitive training in Parkinson’s disease reduces cognitive decline in the long term. Eur. J. Neurol. Epub ahead of print.Search in Google Scholar

Radtke, C., Redeker, J., Jokuszies, A., and Vogt, P.M. (2010). In vivo transformation of neural stem cells following transplantation in the injured nervous system. J. Reconstr. Microsurg. 26, 211–212.10.1055/s-0029-1238221Search in Google Scholar PubMed

Raisman, G. (2001). Olfactory ensheathing cells – another miracle cure for spinal cord injury. Nat. Rev. Neurosci. 2, 369–375.10.1038/35072576Search in Google Scholar PubMed

Rao, Y., Zhu, W., Liu, H., Jia, C., Zhao, Q., and Wang, Y. (2013). Clinical application of olfactory ensheathing cells in the treatment of spinal cord injury. J. Int. Med. Res. 41, 473–481.10.1177/0300060513476426Search in Google Scholar PubMed

Rao, Y.J., Zhu, W.X., Du, Z.Q., Jia, C.X., Du, T.X., Zhao, Q.A., Cao, X.Y., and Wang, Y.J. (2014). Effectiveness of olfactory ensheathing cell transplantation for treatment of spinal cord injury. Genet. Mol. Res. 13, 4124–4129.10.4238/2014.May.30.7Search in Google Scholar PubMed

Richter, M.W., Fletcher, P.A., Liu, J., Tetzlaff, W., and Roskams, A.J. (2005). Lamina propria and olfactory bulb ensheathing cells exhibit differential integration and migration and promote differential axon sprouting in the lesioned spinal cord. J. Neurosci. 25, 10700–10711.10.1523/JNEUROSCI.3632-05.2005Search in Google Scholar PubMed PubMed Central

Rizek, P.N. and Kawaja, M.D. (2006). Cultures of rat olfactory ensheathing cells are contaminated with Schwann cells. Neuroreport 17, 459–462.10.1097/01.wnr.0000209000.32857.1bSearch in Google Scholar PubMed

Schwob, J.E., Youngentob, S.L., and Mezza, R.C. (1995). Reconstitution of the rat olfactory epithelium after methyl bromide-induced lesion. J. Comp. Neurol. 359, 15–37.10.1002/cne.903590103Search in Google Scholar PubMed

Seminatore, C., Polentes, J., Ellman, D., Kozubenko, N., Itier, V., Tine, S., Tritschler, L., Brenot, M., Guidou, E., Blondeau, J., et al. (2010). The postischemic environment differentially impacts teratoma or tumor formation after transplantation of human embryonic stem cell-derived neural progenitors. Stroke 41, 153–159.10.1161/STROKEAHA.109.563015Search in Google Scholar PubMed

Shafiee, A., Kabiri, M., Ahmadbeigi, N., Yazdani, S.O., Mojtahed, M., Amanpour, S., and Soleimani, M. (2011). Nasal septum-derived multipotent progenitors: a potent source for stem cell-based regenerative medicine. Stem Cells Dev. 20, 2077–2091.10.1089/scd.2010.0420Search in Google Scholar PubMed

Shukla, S., Chaturvedi, R.K., Seth, K., Roy, N.S., and Agrawal, A.K. (2009). Enhanced survival and function of neural stem cells-derived dopaminergic neurons under influence of olfactory ensheathing cells in parkinsonian rats. J. Neurochem. 109, 436–451.10.1111/j.1471-4159.2009.05983.xSearch in Google Scholar PubMed

Srivastava, N., Seth, K., Khanna, V.K., Ansari, R.W., and Agrawal, A.K. (2009). Long-term functional restoration by neural progenitor cell transplantation in rat model of cognitive dysfunction: co-transplantation with olfactory ensheathing cells for neurotrophic factor support. Int. J. Dev. Neurosci. 27, 103–110.10.1016/j.ijdevneu.2008.08.002Search in Google Scholar PubMed

Stamegna, J.C., Felix, M.S., Roux-Peyronnet, J., Rossi, V., Féron, F., Gauthier, P., and Matarazzo, V. (2011). Nasal OEC transplantation promotes respiratory recovery in a subchronic rat model of cervical spinal cord contusion. Exp. Neurol. 229, 120–131.10.1016/j.expneurol.2010.07.002Search in Google Scholar PubMed

Stamegna, J.C., Girard, S.D., Veron, A., Sicard, G., Khrestchatisky, M., Feron, F., and Roman, F.S. (2014). A unique method for the isolation of nasal olfactory stem cells in living rats. Stem Cell Res. 12, 673–679.10.1016/j.scr.2014.02.010Search in Google Scholar PubMed

Suzuki, J., Yoshizaki, K., Kobayashi, T., and Osumi, N. (2013). Neural crest-derived horizontal basal cells as tissue stem cells in the adult olfactory epithelium. Neurosci. Res. 75, 112–120.10.1016/j.neures.2012.11.005Search in Google Scholar PubMed

Tabakow, P., Jarmundowicz, W., Czapiga, B., Fortuna, W., Miedzybrodzki, R., Czyz, M., Huber, J., Szarek, D., Okurowski, S., Szewczyk, P., et al. (2013). Transplantation of autologous olfactory ensheathing cells in complete human spinal cord injury. Cell Transplant. 22, 1591–1612.10.3727/096368912X663532Search in Google Scholar PubMed

Thakur, A., Muniswami, D., Tharion, G., and Kanakasabapathy, I. (2013). Isolating globose basal stem cells from albino Wistar rats using a highly specific monoclonal antibody. J. Clin. Diagn. Res. 7, 2419–2422.10.7860/JCDR/2013/6372.3562Search in Google Scholar PubMed PubMed Central

Thakur, A., Muniswami, D., Tharion, G., and Kanakasabapathy, I. (2014). Immunohistological and electrophysiological characterization of globose basal stem cells. Iran J. Basic Med. Sci. 17, 278–286.Search in Google Scholar

Tharion, G., Indirani, K., Durai, M., Meenakshi, M., Devasahayam, S.R., Prabhav, N.R., Solomons, C., and Bhattacharji, S. (2011). Motor recovery following olfactory ensheathing cell transplantation in rats with spinal cord injury. Neurol. India 59, 566–572.10.4103/0028-3886.84339Search in Google Scholar PubMed

Toft, A., Tomé, M., Lindsay, S.L., Barnett, S.C., and Riddell, J.S. (2012). Transplant-mediated repair properties of rat olfactory mucosal OM-I and OM-II sphere-forming cells. J. Neurosci. Res. 90, 619–631.10.1002/jnr.22789Search in Google Scholar PubMed

Tomé, M., Lindsay, S.L., Riddell, J.S., and Barnett, S.C. (2009). Identification of nonepithelial multipotent cells in the embryonic olfactory mucosa. Stem Cells 27, 2196–2208.10.1002/stem.130Search in Google Scholar PubMed

Urdzíková, L.M., Růžička, J., LaBagnara, M., Kárová, K., Kubinová, Š., Jiráková, K., Murali, R., Syková, E., Jhanwar-Uniyal, M., and Jendelová, P. (2014). Human mesenchymal stem cells modulate inflammatory cytokines after spinal cord injury in rat. Int. J. Mol. Sci. 15, 11275–11293.10.3390/ijms150711275Search in Google Scholar PubMed PubMed Central

Wakeman, D.R., Redmond, D.E. Jr., Dodiya, H.B., Sladek, J.R. Jr., Leranth, C., Teng, Y.D., Samulski, R.J., and Snyder, E.Y. (2014). Human neural stem cells survive long term in the midbrain of dopamine-depleted monkeys after GDNF overexpression and project neurites toward an appropriate target. Stem Cells Transl. Med. 3, 692–701.10.5966/sctm.2013-0208Search in Google Scholar PubMed PubMed Central

Wang, G., Ao, Q., Gong, K., Zuo, H., Gong, Y., and Zhang, X. (2010). Synergistic effect of neural stem cells and olfactory ensheathing cells on repair of adult rat spinal cord injury. Cell Transplant. 19, 1325–1337.10.3727/096368910X505855Search in Google Scholar PubMed

Wang, Y.Z., Yamagami, T., Gan, Q., Wang, Y., Zhao, T., Hamad, S., Lott, P., Schnittke, N., Schwob, J.E., and Zhou, C.J. (2011). Canonical Wnt signaling promotes the proliferation and neurogenesis of peripheral olfactory stem cells during postnatal development and adult regeneration. J Cell Sci. 124, 1553–1563.10.1242/jcs.080580Search in Google Scholar PubMed PubMed Central

Wang, M., Lu, C., and Roisen, F. (2012). Adult human olfactory epithelial-derived progenitors: a potential autologous source for cell-based treatment for Parkinson’s disease. Stem Cells Transl. Med. 1, 492–450.10.5966/sctm.2012-0012Search in Google Scholar PubMed PubMed Central

Wang, Y.C., Xia, Q.J., Ba, Y.C., Wang, T.Y., Lin, N., Zou, Y., Shang, F.F., Zhou, X.F., Wang, T.H., Fu, X.M., et al. (2014). Transplantation of olfactory ensheathing cells promotes the recovery of neurological functions in rats with traumatic brain injury associated with downregulation of Bad. Cytotherapy 16, 1000–1010.10.1016/j.jcyt.2013.12.009Search in Google Scholar PubMed

Wegener, A., Deboux, C., Bachelin, C., Frah, M., Kerninon, C., Seilhean, D., Weider, M., and Wegner, M. (2015). Gain of Olig2 function in oligodendrocyte progenitors promotes remyelination. Brain 138, 120–135.10.1093/brain/awu375Search in Google Scholar PubMed PubMed Central

Witheford, M., Westendorf, K., and Roskams, A.J. (2013). Olfactory ensheathing cells promote corticospinal axonal outgrowth by a L1 CAM-dependent mechanism. Glia 61, 1873–1889.10.1002/glia.22564Search in Google Scholar PubMed

Wright, K.T., El Masri, W., Osman, A., Chowdhury, J., and Johnson, W.E. (2011). Concise review: bone marrow for the treatment of spinal cord injury: mechanisms and clinical applications. Stem Cells 29, 169–178.10.1002/stem.570Search in Google Scholar PubMed PubMed Central

Xie, S.T., Lu, F., Zhang, X.J., Shen, Q., He, Z., Gao, W.Q., Hu, D.H., and Yang, H. (2013). Retinoic acid and human olfactory ensheathing cells cooperate to promote neural induction from human bone marrow stromal stem cells. Neuromolecular Med. 15, 252–264.10.1007/s12017-012-8215-9Search in Google Scholar PubMed

Yeung, T.Y., Seeberger, K.L., Kin, T., Adesida, A., Jomha, N., Shapiro, A.M., and Korbutt, G.S. (2012). Human mesenchymal stem cells protect human islets from pro-inflammatory cytokines. PLoS One 7, e38189.10.1371/journal.pone.0038189Search in Google Scholar PubMed PubMed Central

Yin, F., Guo, L., Meng, C.Y., Liu, Y.J., Lu, R.F., Li, P., and Zhou, Y.B. (2014). Transplantation of mesenchymal stem cells exerts anti-apoptotic effects in adult rats after spinal cord ischemia-reperfusion injury. Brain Res. 1561, 1–10.10.1016/j.brainres.2014.02.047Search in Google Scholar PubMed

Ziege, S., Baumgärtner, W., and Wewetzer, K. (2013). Toward defining the regenerative potential of olfactory mucosa: establishment of Schwann cell-free adult canine olfactory ensheathing cell preparations suitable for transplantation. Cell Transplant. 22, 355–367.10.3727/096368912X656108Search in Google Scholar PubMed