Dental pulp cells provide neurotrophic support for dopaminergic neurons and differentiate into neurons in vitro ; implications for tissue engineering and repair in the nervous system
dc.contributor.author | Nosrat, Irina V. | en_US |
dc.contributor.author | Smith, Christopher A. | en_US |
dc.contributor.author | Mullally, Patrick | en_US |
dc.contributor.author | Olson, Lars | en_US |
dc.contributor.author | Nosrat, Christopher A. | en_US |
dc.date.accessioned | 2010-06-01T18:36:26Z | |
dc.date.available | 2010-06-01T18:36:26Z | |
dc.date.issued | 2004-05 | en_US |
dc.identifier.citation | Nosrat, Irina V.; Smith, Christopher A.; Mullally, Patrick; Olson, Lars; Nosrat, Christopher A. (2004). "Dental pulp cells provide neurotrophic support for dopaminergic neurons and differentiate into neurons in vitro ; implications for tissue engineering and repair in the nervous system." European Journal of Neuroscience 19(9): 2388-2398. <http://hdl.handle.net/2027.42/71809> | en_US |
dc.identifier.issn | 0953-816X | en_US |
dc.identifier.issn | 1460-9568 | en_US |
dc.identifier.uri | https://hdl.handle.net/2027.42/71809 | |
dc.identifier.uri | http://www.ncbi.nlm.nih.gov/sites/entrez?cmd=retrieve&db=pubmed&list_uids=15128393&dopt=citation | en_US |
dc.description.abstract | Glial cell line-derived neurotrophic factor (GDNF) mRNA is highly expressed by dental pulp cells (DPCs) prior to the initiation of dental pulp innervation. We show that radioactively labelled exogenous GDNF is retrogradely transported from neonatal teeth and vibrissae to the trigeminal neurons, indicating that GDNF acts as a classical neurotrophic factor in the trigeminal system. We also show that DPCs from both rats and humans produce nerve growth factor (NGF), brain-derived neurotrophic factor (BDNF) and GDNF mRNAs in vitro , promote the survival and phenotypic characteristics of embryonic dopaminergic (DA) neurons and protect DA neurons against the neurotoxin 6-hydroxy-dopamine (6-OHDA) in vitro . By using inhibitory antibodies to NGF, BDNF and GDNF, we show that the promotion of DA neuron survival relates to the production and release of neurotrophic proteins by DPCs in vitro . We suggest that in vivo production of neurotrophic factors by DPCs play roles in tooth innervation. However, continued production of neurotrophic factors by the DPCs might have wider implications. We propose that the dental pulp is a viable source of easily attainable cells with possible potential for development of autologous cell transplantation therapies. We also show that a population of neural crest-derived dental pulp cells acquire clear neuronal morphology and protein expression profile in vitro , indicating the presence of a cell population in the dental pulp with neuronal differentiation capacity that might provide additional benefits when grafted into the CNS. | en_US |
dc.format.extent | 467878 bytes | |
dc.format.extent | 3109 bytes | |
dc.format.mimetype | application/pdf | |
dc.format.mimetype | text/plain | |
dc.publisher | Blackwell Science Ltd | en_US |
dc.rights | © Federation of European Neuroscience Societies | en_US |
dc.subject.other | BDNF | en_US |
dc.subject.other | Dopamine | en_US |
dc.subject.other | GDNF | en_US |
dc.subject.other | Neurotrophic Factors | en_US |
dc.subject.other | NGF | en_US |
dc.subject.other | Tooth Innervation | en_US |
dc.title | Dental pulp cells provide neurotrophic support for dopaminergic neurons and differentiate into neurons in vitro ; implications for tissue engineering and repair in the nervous system | en_US |
dc.type | Article | en_US |
dc.subject.hlbsecondlevel | Neurosciences | en_US |
dc.subject.hlbtoplevel | Health Sciences | en_US |
dc.description.peerreviewed | Peer Reviewed | en_US |
dc.contributor.affiliationum | Laboratory of Oral Neurobiology, Department of Biologic and Materials Sciences, Room 3218, School of Dentistry, University of Michigan, Ann Arbor, MI 48109–1078, USA | en_US |
dc.contributor.affiliationother | Department of Neuroscience, Karolinska Institutet, Stockholm, Sweden | en_US |
dc.identifier.pmid | 15128393 | en_US |
dc.description.bitstreamurl | http://deepblue.lib.umich.edu/bitstream/2027.42/71809/1/j.0953-816X.2004.03314.x.pdf | |
dc.identifier.doi | 10.1111/j.0953-816X.2004.03314.x | en_US |
dc.identifier.source | European Journal of Neuroscience | en_US |
dc.identifier.citedreference | About, I., Laurent-Maquin, D., Lendahl, U. & Mitsiadis, T. A. ( 2000 ) Nestin expression in embryonic and adult human teeth under normal and pathological conditions. Am. J. Pathol., 157, 287 – 295. | en_US |
dc.identifier.citedreference | Ai, Y., Markesbery, W., Zhang, Z., Grondin, R., Elseberry, D., Gerhardt, G. A. & Gash, D. M. ( 2003 ) Intraputamenal infusion of GDNF in aged rhesus monkeys: distribution and dopaminergic effects. J. Comp. Neurol., 461, 250 – 261. | en_US |
dc.identifier.citedreference | Amano, O., Bringas, P., Takahashi, I., Takahashi, K., Yamane, A., Chai, Y., Nuckolls, G. H., Shum, L. & Slavkin, H. C. ( 1999 ) Nerve growth factor (NGF) supports tooth morphogenesis in mouse first branchial arch explants. Dev. Dyn., 216, 299 – 310. | en_US |
dc.identifier.citedreference | Arenas, E. & Persson, H. ( 1994 ) Neurotrophin-3 prevents the death of adult central noradrenergic neurons in vivo. Nature, 367, 368 – 371. | en_US |
dc.identifier.citedreference | Arenas, E., Trupp, M., Åkerud, P. & IbÁÑez, D. ( 1995 ) GDNF prevents degeneration and promotes the phenotype of brain noradrenergic neuros in vivo. Neuron, 15, 1465 – 1473. | en_US |
dc.identifier.citedreference | Bixby, S., Kruger, G. M., Mosher, J. T., Joseph, N. M. & Morrison, S. J. ( 2002 ) Cell-intrinsic differences between stem cells from different regions of the peripheral nervous system regulate the generation of neural diversity. Neuron, 35, 643 – 656. | en_US |
dc.identifier.citedreference | BjÖrklund, A. & Lindvall, O. ( 2000 ) Cell replacement therapies for central nervous system disorders. Nat. Neurosci., 3, 537 – 544. | en_US |
dc.identifier.citedreference | Borlongan, C. V., Sanberg, P. R. & Freeman, T. B. ( 1999 ) Neural transplantation for neurodegenerative disorders. Lancet, 353, SI 29 - 30. | en_US |
dc.identifier.citedreference | Borlongan, C. V., Zhou, F. C., Hayashi, T., Su, T. P., Hoffer, B. J. & Wang, Y. ( 2001 ) Involvement of GDNF in neuronal protection against 6-OHDA-induced parkinsonism following intracerebral transplantation of fetal kidney tissues in adult rats. Neurobiol. Dis., 8, 636 – 646. | en_US |
dc.identifier.citedreference | Bottner, M., Krieglstein, K. & Unsicker, K. ( 2000 ) The transforming growth factor-betas: structure, signaling, and roles in nervous system development and functions. J. Neurochem., 75, 2227 – 2240. | en_US |
dc.identifier.citedreference | Brundin, P., Karlsson, J., Emgard, M., Schierle, G. S., Hansson, O., Petersen, A. & Castilho, R. F. ( 2000 ) Improving the survival of grafted dopaminergic neurons: a review over current approaches. Cell Transplant., 9, 179 – 195. | en_US |
dc.identifier.citedreference | Byers, M. R., O'Neill, P. C., Nishimura, M. C., Philips, H. S. & Albers, K. M. ( 1997 ) Dependence of dental innervation on NGF: comparison of hetero- and homozygous mice lacking NGF with k14NGF transgenic or hybrid rescued TKO mice. Soc. Neurosci. Abstr., 23, 1704. | en_US |
dc.identifier.citedreference | Byers, M. R., Wheeler, E. F. & Bothwell, M. ( 1992 ) Altered expression of NGF and P75 NGF-receptor by fibroblasts of injured teeth precedes sensory nerve sprouting. Growth Factors, 6, 41 – 52. | en_US |
dc.identifier.citedreference | Carrasco, E. & Werner, P. ( 2002 ) Selective destruction of dopaminergic neurons by low concentrations of 6-OHDA and MPP+: protection by acetylsalicylic acid aspirin. Parkinsonism Relat. Disord., 8, 407 – 411. | en_US |
dc.identifier.citedreference | Choi-Lundberg, D. & Rosenthal, A. ( 1999 ) Autotransplantation for Parkinson's disease goes a step further. Neuron, 22, 635 – 636. | en_US |
dc.identifier.citedreference | Davies, A. M. ( 1994a ) Neurotrophic factors. Switching neurotrophin dependence. Current Biol., 4, 273 – 276. | en_US |
dc.identifier.citedreference | Davies, A. M. ( 1994b ) The role of neurotrophins in the developing nervous system. J. Neurobiol., 25, 1334 – 1348. | en_US |
dc.identifier.citedreference | Dunnett, S. B. & BjÖrklund, A. ( 1992 ) Staging and dissection of rat embryos. In Dunnett, S. B. & Bjorklund, A. (eds), Neural Transplantation, a Practical Approach. Oxford University Press, New York, pp. 1 – 20. | en_US |
dc.identifier.citedreference | Engele, J. & Bohn, M. C. ( 1991 ) The neurotrophic effects of fibroblast growth factors on dopaminergic neurons in vitro are mediated by mesencephalic glia. J. Neurosci., 11, 3070 – 3078. | en_US |
dc.identifier.citedreference | Engele, J., Rieck, H., Choi-Lundberg, D. & Bohn, M. C. ( 1996 ) Evidence for a novel neurotrophic factor for dopaminergic neurons secreted from mesencephalic glial cell lines. J. Neurosci. Res., 43, 576 – 586. | en_US |
dc.identifier.citedreference | Ernfors, P., Lee, K. F. & Jaenisch, R. ( 1994 ) Mice lacking brain-derived neurotrophic factor develop with sensory deficits. Nature, 368, 147 – 150. | en_US |
dc.identifier.citedreference | Espejo, E. F., Montoro, R. J., Armengol, J. A. & Lopez-Barneo, J. ( 1998 ) Cellular and functional recovery of Parkinsonian rats after intrastriatal transplantation of carotid body cell aggregates. Neuron, 20, 197 – 206. | en_US |
dc.identifier.citedreference | Farkas, L. M., Dunker, N., Roussa, E., Unsicker, K. & Krieglstein, K. ( 2003 ) Transforming growth factor-beta (s) are essential for the development of midbrain dopaminergic neurons in vitro and in vivo. J. Neurosci., 23, 5178 – 5186. | en_US |
dc.identifier.citedreference | Fried, K., Nosrat, C., Lillesaar, C. & Hildebrand, C. ( 2000 ) Molecular signaling and pulpal nerve development. Crit. Rev. Oral Biol. Med., 11, 318 – 332. | en_US |
dc.identifier.citedreference | Gash, D., Zhang, Z., Ovadia, A., Cass, W., Yi, A., Simmerman, L., Russell, D., Martin, D., Lapchak, P., Collins, F., Hoffer, B. & Gerhardt, G. ( 1996 ) Functional recovery in parkinsonian monkeys treated with GDNF. Nature, 380, 252 – 255. | en_US |
dc.identifier.citedreference | Granholm, A. C., Henry, S., Hebert, M. A., Eken, S., Gerhardt, G. A. & Vanhorne, C. ( 1998 ) Kidney cografts enhance fiber outgrowth from ventral mesencephalic grafts to the 6-OHDA-lesioned striatum, and improve behavioral recovery. Cell Transplantation, 7, 197 – 212. | en_US |
dc.identifier.citedreference | Granholm, A., Srivastava, N., Mott, J., Henry, S., Henry, M., Westphal, H., Pichel, J., Shen, L. & Hoffer, B. J. ( 1997 ) Morphological alterations in the peripheral and central nervous system of mice lacking glial cell line-derived neurotrophic factor (GDNF): Immunohistochemical studies. J. Neurosci., 17, 1168 – 1178. | en_US |
dc.identifier.citedreference | Gronthos, S., Brahim, J., Li, W., Fisher, L. W., Cherman, N., Boyde, A., DenBesten, P., Robey, P. G. & Shi, S. ( 2002 ) Stem cell properties of human dental pulp stem cells. J. Dent. Res., 81, 531 – 535. | en_US |
dc.identifier.citedreference | Gronthos, S., Mankani, M., Brahim, J., Robey, P. G. & Shi, S. ( 2000 ) Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. Proc. Natl Acad. Sci. USA, 97, 13625 – 13630. | en_US |
dc.identifier.citedreference | Hefti, F. ( 1986 ) Nerve growth factor promotes survival of septal cholinergic neurons after fimbrial transections. J. Neurosci., 6, 2155 – 2162. | en_US |
dc.identifier.citedreference | Henderson, C. E., Phillips, H. S., Pollock, R. A., Davies, A. M., Lemeulle, C., Armanini, M., Simmons, L., Moffet, B., Vandlen, R. A., Simpson, L. C., Koliatsos, V.E. & Rosenthal, A. ( 1994 ) GDNF: a potent survival factor for motoneurons present in peripheral nerve and muscle. Science, 266, 1062 – 1064. | en_US |
dc.identifier.citedreference | Hofstetter, C. P., Schwarz, E. J., Hess, D., Widenfalk, J., El Manira, A., Prockop, D. J. & Olson, L. ( 2002 ) Marrow stromal cells form guiding strands in the injured spinal cord and promote recovery. Proc. Natl Acad. Sci. USA, 99, 2199 – 2204. | en_US |
dc.identifier.citedreference | Jones, K. R. I., Backus, C. & Reichardt, L. F. ( 1994 ) Targeted disruption of the BDNF gene perturbs brain and sensory neuron development but not motor neuron development. Cell, 76, 989 – 999. | en_US |
dc.identifier.citedreference | Karavanov, A., Sainio, K., Palgi, J., Saarma, M., Saxen, L. & Sariola, H. ( 1995 ) Neurotrophin 3 rescues neuronal precursors from apoptosis and promotes neuronal differentiation in the embryonic metanephric kidney. Proc. Natl Acad. Sci. USA, 92, 11279 – 11283. | en_US |
dc.identifier.citedreference | Kruger, G. M., Mosher, J. T., Bixby, S., Joseph, N., Iwashita, T. & Morrison, S. J. ( 2002 ) Neural crest stem cells persist in the adult gut but undergo changes in self-renewal, neuronal subtype potential, and factor responsiveness. Neuron, 35, 657 – 669. | en_US |
dc.identifier.citedreference | Lillesaar, C., Eriksson, C. & Fried, K. ( 2001 ) Rat tooth pulp cells elicit neurite growth from trigeminal neurones and express mRNAs for neurotrophic factors in vitro. Neurosci. Lett., 308, 161 – 164. | en_US |
dc.identifier.citedreference | Luquin, M. R., Montoro, R. J., Guillen, J., Saldise, L., Insausti, R., Del Rio, J. & Lopez-Barneo, J. ( 1999 ) Recovery of chronic parkinsonian monkeys by autotransplants of carotid body cell aggregates into putamen. Neuron, 22, 743 – 750. | en_US |
dc.identifier.citedreference | Luukko, K., Arumae, U., Karavanov, A., Moshnyakov, M., Sainio, K., Sariola, H., Saarma, M. & Thesleff, I. ( 1997a ) Neurotrophin mRNA expression in the developing tooth suggests multiple roles in innervation and organogenesis. Dev. Dynamics, 210, 117 – 129. | en_US |
dc.identifier.citedreference | Luukko, K., Suvanto, P., Saarma, M. & Thesleff, I. ( 1997b ) Expression of GDNF and its receptors in developing tooth is developmentally regulated and suggests multiple roles in innervation and organogenesis. Devel. Dynam., 210, 463 – 471. | en_US |
dc.identifier.citedreference | Matsuo, S., Ichikawa, H., Henderson, T. A., Silos-Santiago, I., Barbacid, M., Arends, J. J. & Jacquin, M. F. ( 2001 ) trkA modulation of developing somatosensory neurons in oro-facial tissues: tooth pulp fibers are absent in trkA knockout mice. Neuroscience, 105, 747 – 760. | en_US |
dc.identifier.citedreference | Miura, M., Gronthos, S., Zhao, M., Lu, B., Fisher, L. W., Robey, P. G. & Shi, S. ( 2003 ) SHED: Stem cells from human exfoliated deciduous teeth. Proc. Natl Acad. Sci. USA, 25, 25. | en_US |
dc.identifier.citedreference | Mohamed, S. S. & Atkinson, M. E. ( 1983 ) A histological study of the innervation of developing mouse teeth. J. Anat., 136, 735 – 749. | en_US |
dc.identifier.citedreference | Nosrat, C. A., Fang, M., Kuszpit, K. K. & Nosrat, I. V. ( 2002a ) Dental pulp cells promote the survival of dopaminergic neurons in vitro. Program No. 635.5.2002. Abstract Viewer/Itinerary planner, Society for Neuroscience, Washington, DC. On line. | en_US |
dc.identifier.citedreference | Nosrat, C. A., Fried, K., Ebendal, T. & Olson, L. ( 1998 ) NGF, BDNF, NT-3, NT-4 and GDNF in tooth development. Eur. J. Oral Sci., 106, 94 – 99. | en_US |
dc.identifier.citedreference | Nosrat, C. A., Fried, K., Lindskog, S. & Olson, L. ( 1997a ) Cellular expression of neurotrophin mRNAs during tooth development. Cell Tissue Res., 290, 569 – 580. | en_US |
dc.identifier.citedreference | Nosrat, I., Seiger, A., Olson, L. & Nosrat, C. A. ( 2002b ) Expression patterns of neurotrophic factor mRNAs in developing human teeth. Cell Tissue Res., 310, 177 – 187. | en_US |
dc.identifier.citedreference | Nosrat, C. A., Tomac, A., Hoffer, B. J. & Olson, L. ( 1997b ) Cellular and developmental patterns of expression of Ret and GDNFR-α mRNAs. Exp. Brain Res., 115, 410 – 422. | en_US |
dc.identifier.citedreference | Nosrat, C. A., Tomac, A., Lindqvist, E., Lindskog, S., Humpel, C., Stromberg, I., Ebendal, T., Hoffer, B. J. & Olson, L. ( 1996 ) Cellular expression of GDNF mRNA suggests multiple functions inside and outside the nervous system. Cell Tiss. Res., 286, 191 – 207. | en_US |
dc.identifier.citedreference | Nosrat, I. V., Widenfalk, J., Olson, L. & Nosrat, C. A. ( 2001 ) Dental pulp cells produce neurotrophic factors, interact with trigeminal neurons in vitro and rescue motoneurons after spinal cord injury. Devel. Biol., 238, 120 – 132. | en_US |
dc.identifier.citedreference | Olson, L. ( 1997 ) Regeneration in the adult central nervous system: experimental repair strategies. Nat. Med., 3, 1329 – 1335. | en_US |
dc.identifier.citedreference | Olson, L., Seiger, Å. & StrÖmberg, I. ( 1983 ) Intraocular transplantation in rodents. A detailed account of the procedure and examples of its use in neurobiology with special reference to brain tissue grafting. In Federoff, S. & Hertz, L. (eds), Advances in Cellular Neurobiology, Vol. 4. Academic, New York, pp. 407 – 442. | en_US |
dc.identifier.citedreference | Oppenheim, R. W., Houenou, L. J., Johnson, J. E., Lin, L. F., Li, L., Lo, A. C., Newsome, A. L., Prevette, D. M. & Wang, S. ( 1995 ) Developing motor neurons rescued from programmed and axotomy-induced cell death by GDNF. Nature, 373, 344 – 346. | en_US |
dc.identifier.citedreference | Oppenheim, R. W., Yin, Q. W., Prevette, D. & Yan, Q. ( 1992 ) Brain-derived neurotrophic factor rescues developing avian motoneurons from cell death. Nature, 360, 755 – 757. | en_US |
dc.identifier.citedreference | Othberg, A. I., Willing, A. E., Cameron, D. F., Anton, A., Saporta, S., Freeman, T. B. & Sanberg, P. R. ( 1998 ) Trophic effect of porcine Sertoli cells on rat and human ventral mesencephalic cells and hNT neurons in vitro. Cell Transplantation, 7, 157 – 164. | en_US |
dc.identifier.citedreference | Pichel, J. G., Shen, L. Y., Sheng, H. Z., Granholm, A. C., Drago, J., Grinberg, A., Lee, E. J., Huang, S. P., Saarma, M., Hoffer, B. J., Sariola, H. & Westphal, H. ( 1996 ) Defects in enteric innervation and kidney development in mice lacking GDNF. Nature, 382, 73 – 76. | en_US |
dc.identifier.citedreference | Prockop, D. J., Azizi, S. A., Phinney, D. G., Kopen, G. C. & Schwarz, E. J. ( 2000 ) Potential use of marrow stromal cells as therapeutic vectors for diseases of the central nervous system. Prog. Brain Res., 128, 293 – 297. | en_US |
dc.identifier.citedreference | Qian, X. B. & Naftel, J. P. ( 1994 ) The effects of anti-nerve growth factor on retrograde labelling of superior cervical ganglion neurones projecting to the molar pulp in the rat. Arch. Oral Biol., 39, 1041 – 1047. | en_US |
dc.identifier.citedreference | Qian, X. B. & Naftel, J. P. ( 1996 ) Effects of neonatal exposure to anti-nerve growth factor on the number and size distribution of trigeminal neurones projecting to the molar dental pulp in rats. Arch. Oral Biol., 41, 359 – 367. | en_US |
dc.identifier.citedreference | Ramon-Cueto, A., Plant, G. W., Avila, J. & Bunge, M. B. ( 1998 ) Long-distance axonal regeneration in the transected adult rat spinal cord is promoted by olfactory ensheathing glia transplants. J. Neurosci., 18, 3803 – 3815. | en_US |
dc.identifier.citedreference | Rochlin, M. W., O'Connor, R., Giger, R. J., Verhaagen, J. & Farbman, A. I. ( 2000 ) Comparison of neurotrophin and repellent sensitivities of early embryonic geniculate and trigeminal axons. J. Comp. Neurol., 422, 579 – 593. | en_US |
dc.identifier.citedreference | Rosenthal, A. ( 1998 ) Auto transplants for Parkinson's disease? Neuron, 20, 169 – 172. | en_US |
dc.identifier.citedreference | Sanberg, P. R., Borlongan, C. V., Othberg, A. I., Saporta, S., Freeman, T. B. & Cameron, D. F. ( 1997 ) Testis-derived Sertoli cells have a trophic effect on dopamine neurons and alleviate hemiparkinsonism in rats. Nature Med., 3, 1129 – 1132. | en_US |
dc.identifier.citedreference | Sautter, J., Meyer, M., Spenger, C., Seiler, R. W. & Widmer, H. R. ( 1998 ) Effects of combined BDNF and GDNF treatment on cultured dopaminergic midbrain neurons. Neuroreport, 20, 1093 – 1096. | en_US |
dc.identifier.citedreference | Sendtner, M., Holtmann, B., Kolbeck, R., Thoenen, H. & Barde, Y. A. ( 1992 ) Brain-derived neurotrophic factor prevents the death of motoneurons in newborn rats after nerve section. Nature, 360, 757 – 759. | en_US |
dc.identifier.citedreference | Skinner, M. K. ( 1993 ) Secretion of growth factors and other regulatory factors. In Russell, L. D. & Griswold, M. D. (Eds), The Sertoli Cell. Cache River Press, Clearwater, FL, pp. 237 – 248. | en_US |
dc.identifier.citedreference | Terling, C., Rass, A., Mitsiadis, T. A., Fried, K., Lendahl, U. & Wroblewski, J. ( 1995 ) Expression of the intermediate filament nestin during rodent tooth development. Int. J. Dev. Biol., 39, 947 – 956. | en_US |
dc.identifier.citedreference | Toledo-Aral, J. J., Mendez-Ferrer, S., Pardal, R., Echevarria, M. & Lopez-Barneo, J. ( 2003 ) Trophic restoration of the nigrostriatal dopaminergic pathway in long-term carotid body-grafted parkinsonian rats. J. Neurosci., 23, 141 – 148. | en_US |
dc.identifier.citedreference | Toma, J. G., Akhavan, M., Fernandes, K. J., Barnabe-Heider, F., Sadikot, A., Kaplan, D. R. & Miller, F. D. ( 2001 ) Isolation of multipotent adult stem cells from the dermis of mammalian skin. Nat. Cell Biol., 3, 778 – 784. | en_US |
dc.identifier.citedreference | Tomac, A., Lindqvist, E., Lin, L. F., Ogren, S. O., Young, D., Hoffer, B. J. & Olson, L. ( 1995a ) Protection and repair of the nigrostriatal dopaminergic system by GDNF in vivo. Nature, 373, 335 – 339. | en_US |
dc.identifier.citedreference | Tomac, A., Widenfalk, J., Lin, L., Kohno, T., Ebendal, T., Hoffer, B. & Olson, L. ( 1995b ) Retrograde axonal transport of glial cell line-derived neurotrohic factor in the adult nigrostriatal system suggests a trophic role in the adult. Proc. Natl Acad. Sci. USA, 92, 8274 – 8278. | en_US |
dc.identifier.citedreference | Unsicker, K. & Krieglstein, K. ( 2000 ) Co-activation of TGF-ss and cytokine signaling pathways are required for neurotrophic functions. Cytokine Growth Factor Rev., 11, 97 – 102. | en_US |
dc.identifier.citedreference | de Vicente, J. C., Cabo, R., Ciriaco, E., Laura, R., Naves, F. J., Silos-Santiago, I. & Vega, J. A. ( 2002 ) Impaired dental cytodifferentiation in glial cell-line derived growth factor (GDNF) deficient mice. Ann. Anat, 184, 85 – 92. | en_US |
dc.identifier.citedreference | Widenfalk, J., Lundstromer, K., Jubran, M., Brene, S. & Olson, L. ( 2001 ) Neurotrophic factors and receptors in the immature and adult spinal cord after mechanical injury or kainic acid. J. Neurosci., 21, 3457 – 3475. | en_US |
dc.identifier.citedreference | Williams, L. R., Varon, S., Peterson, G. M., Wictorin, K., Fischer, W., BjÖrklund, A. & Gage, F. H. ( 1986 ) Continuous infusion of nerve growth factor prevents basal forebrain neuronal death after fimbria fornix transection. Proc. Natl Acad. Sci. USA, 83, 9231 – 9235. | en_US |
dc.identifier.citedreference | Yan, Q., Elliott, J. & Snider, W. D. ( 1992 ) Brain-derived neurotrophic factor rescues spinal motor neurons from axotomy-induced cell death. Nature, 360, 753 – 755. | en_US |
dc.identifier.citedreference | Zhang, J., Geula, C., Lu, C., Koziel, H., Hatcher, L. M. & Roisen, F. J. ( 2003 ) Neurotrophins regulate proliferation and survival of two microglial cell lines in vitro. Exp. Neurol., 183, 469 – 481. | en_US |
dc.owningcollname | Interdisciplinary and Peer-Reviewed |
Files in this item
Remediation of Harmful Language
The University of Michigan Library aims to describe library materials in a way that respects the people and communities who create, use, and are represented in our collections. Report harmful or offensive language in catalog records, finding aids, or elsewhere in our collections anonymously through our metadata feedback form. More information at Remediation of Harmful Language.
Accessibility
If you are unable to use this file in its current format, please select the Contact Us link and we can modify it to make it more accessible to you.