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Frontiers in Biology

ISSN 1674-7984

ISSN 1674-7992(Online)

CN 11-5892/Q

Front Biol    2013, Vol. 8 Issue (1) : 101-108    https://doi.org/10.1007/s11515-012-1201-7
REVIEW
Exercise-dependent regulation of glial cell line-derived neurotrophic factor (GDNF) expression in skeletal muscle and its importance for the neuromuscular system
John-Mary VIANNEY, Monica J. MCCULLOUGH, Amy M. GYORKOS, John M. SPITSBERGEN()
Department of Biological Sciences, Western Michigan University, Kalamazoo, MI 49008-5410, USA
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Abstract

The focus of this review is to highlight the importance of glial cell line-derived neurotrophic factor (GDNF) for the motor nervous system. GDNF is the most potent survival factor for motor neurons, where it enhances maintenance and survival of both developing and mature motor neurons in vivo and in vitro. GDNF aids in neuromuscular junction formation, maintenance, and plasticity, where skeletal muscle-derived GDNF may be responsible for this phenomenon. Increased levels of physical activity can increase GDNF protein levels in skeletal muscle, where alterations in acetylcholine and acetylcholine receptor activation may be involved in regulation of these changes observed. With inactivity and disuse, GDNF expression shows different patterns of regulation in the central and peripheral nervous systems. Due to its potent effects for motor neurons, GDNF is being extensively studied in neuromuscular diseases.

Keywords glial cell line-derived neurotrophic factor      neuromuscular junction      motor neurons      skeletal muscle     
Corresponding Author(s): SPITSBERGEN John M.,Email:john.spitsbergen@wmich.edu   
Issue Date: 01 February 2013
 Cite this article:   
John-Mary VIANNEY,Monica J. MCCULLOUGH,Amy M. GYORKOS, et al. Exercise-dependent regulation of glial cell line-derived neurotrophic factor (GDNF) expression in skeletal muscle and its importance for the neuromuscular system[J]. Front Biol, 2013, 8(1): 101-108.
 URL:  
https://academic.hep.com.cn/fib/EN/10.1007/s11515-012-1201-7
https://academic.hep.com.cn/fib/EN/Y2013/V8/I1/101
FactorEffectSiteReferences
Walk training--EDLMcCullough et al., 2011, Wehrwein et al. 2002
+SOL
StretchnoneEDLMcCullough et al., 2011
+--SOL
Electrical stimulation--EDLMcCullough et al., 2011
+SOL
Hindlimb suspension--SOLWehrwein et al. 2002
+pectoralis major
Cholinergic neurons--skeletal muscle cells in cultureVianney and Spitsbergen, 2011
nAChR activation--skeletal muscle cells in cultureVianney and Spitsbergen, 2011
Spinal cord injury+skeletal muscleLie and Weis, 1998; Suzuki et al., 1988a; Trupp et al., 1995; Naveilhan et al., 1997
+spinal cordHashimoto et al., 2005
Spinal cord injury and exercise+SOLDupont-Versteegden et al., 2004
+spinal cordCote et al., 2011
Aging--skeletal muscleNagano and Suzuki, 2003
Tab.1  Regulation of GDNF protein production
1 Adlard P A, Cotman C W (2004). Voluntary exercise protects against stress-induced decreases in brain-derived neurotrophic factor protein expression. Neuroscience , 124(4): 985-992
doi: 10.1016/j.neuroscience.2003.12.039 pmid:15026138
2 Airaksinen M S, Saarma M (2002). The GDNF family: signalling, biological functions and therapeutic value. Nat Rev Neurosci , 3(5): 383-394
doi: 10.1038/nrn812 pmid:11988777
3 Allen S J, Dawbarn D (2006). Clinical relevance of the neurotrophins and their receptors. Clin Sci (Lond) , 110(2): 175-191
doi: 10.1042/CS20050161 pmid:16411894
4 Andonian M H, Fahim M A (1987). Effects of endurance exercise on the morphology of mouse neuromuscular junctions during ageing. J Neurocytol , 16(5): 589-599
doi: 10.1007/BF01637652 pmid:3694234
5 Angka H E, Geddes A J, Kablar B (2008). Differential survival response of neurons to exogenous GDNF depends on the presence of skeletal muscle. Dev Dyn , 237(11): 3169-3178
doi: 10.1002/dvdy.21727 pmid:18816441
6 Bergman E, Kullberg S, Ming Y, Ulfhake B (1999). Upregulation of GFRalpha-1 and c-ret in primary sensory neurons and spinal motoneurons of aged rats. J Neurosci Res , 57(2): 153-165
doi: 10.1002/(SICI)1097-4547(19990715)57:2<153::AID-JNR1>3.0.CO;2-A pmid:10398293
7 Blum M, Weickert C S (1995). GDNF mRNA expression in normal postnatal development, aging, and in Weaver mutant mice. Neurobiol Aging , 16(6): 925-929
doi: 10.1016/0197-4580(95)02011-X pmid:8622783
8 Boger H A, Middaugh L D, Huang P, Zaman V, Smith A C, Hoffer B J, Tomac A C, Granholm A Ch (2006). A partial GDNF depletion leads to earlier age-related deterioration of motor function and tyrosine hydroxylase expression in the substantia nigra. Exp Neurol , 202(2): 336-347
doi: 10.1016/j.expneurol.2006.06.006 pmid:16889771
9 Caumont A S, Octave J N, Hermans E (2006). Amantadine and memantine induce the expression of the glial cell line-derived neurotrophic factor in C6 glioma cells. Neurosci Lett , 394(3): 196-201
doi: 10.1016/j.neulet.2005.10.027 pmid:16298481
10 Chen B M, Grinnell A D (1997). Kinetics, Ca2+ dependence, and biophysical properties of integrin-mediated mechanical modulation of transmitter release from frog motor nerve terminals. J Neurosci , 17(3): 904-916
pmid:8994045
11 Clemow D B, Spitsbergen J M, McCarty R, Steers W D, Tuttle J B (1999). Altered NGF regulation may link a genetic predisposition for hypertension with hyperactive voiding. J Urol , 161(4): 1372-1377
doi: 10.1016/S0022-5347(01)61686-0 pmid:10081910
12 Connor B, Dragunow M (1998). The role of neuronal growth factors in neurodegenerative disorders of the human brain. Brain Res Brain Res Rev , 27(1): 1-39
doi: 10.1016/S0165-0173(98)00004-6 pmid:9639663
13 Cote M P, Azzam G A, Lemay M A, Zhukareva V, Houlé J D (2011). Activity-dependent increase in neurotrophic factors is associated with an enhanced modulation of spinal reflexes after spinal cord injury. J Neurotrauma , 28(2): 299-309
doi: 10.1089/neu.2010.1594 pmid:21083432
14 Deschenes M R, Maresh C M, Crivello J F, Armstrong L E, Kraemer W J, Covault J (1993). The effects of exercise training of different intensities on neuromuscular junction morphology. J Neurocytol , 22(8): 603-615
doi: 10.1007/BF01181487 pmid:8229087
15 Dorl?chter M, Irintchev A, Brinkers M, Wernig A (1991). Effects of enhanced activity on synaptic transmission in mouse extensor digitorum longus muscle. J Physiol , 436: 283-292
pmid:1648130
16 Dudanova I, Gatto G, Klein R (2010). GDNF acts as a chemoattractant to support ephrinA-induced repulsion of limb motor axons. Curr Biol , 20(23): 2150-2156
doi: 10.1016/j.cub.2010.11.021 pmid:21109439
17 Dupont-Versteegden E E, Houlé J D, Dennis R A, Zhang J, Knox M, Wagoner G, Peterson C A (2004). Exercise-induced gene expression in soleus muscle is dependent on time after spinal cord injury in rats. Muscle Nerve , 29(1): 73-81
doi: 10.1002/mus.10511 pmid:14694501
18 Ebert A D, Barber A E, Heins B M, Svendsen C N (2010). Ex vivo delivery of GDNF maintains motor function and prevents neuronal loss in a transgenic mouse model of Huntington’s disease. Exp Neurol , 224: 155-162
19 Edstr?m E, Altun M, Bergman E, Johnson H, Kullberg S, Ramírez-León V, Ulfhake B (2007). Factors contributing to neuromuscular impairment and sarcopenia during aging. Physiol Behav , 92(1-2): 129-135
doi: 10.1016/j.physbeh.2007.05.040 pmid:17585972
20 Fabel K, Fabel K, Tam B, Kaufer D, Baiker A, Simmons N, Kuo C J, Palmer T D (2003). VEGF is necessary for exercise-induced adult hippocampal neurogenesis. Eur J Neurosci , 18(10): 2803-2812
doi: 10.1111/j.1460-9568.2003.03041.x pmid:14656329
21 Frostick S P, Yin Q, Kemp G J (1998). Schwann cells, neurotrophic factors, and peripheral nerve regeneration. Microsurgery , 18(7): 397-405
doi: 10.1002/(SICI)1098-2752(1998)18:7<397::AID-MICR2>3.0.CO;2-F pmid:9880154
22 Fu S Y, Gordon T (1997). The cellular and molecular basis of peripheral nerve regeneration. Mole Neurobiol 14 (1-2): 67-116
23 Funakoshi H, Belluardo N, Arenas E, Yamamoto Y, Casabona A, Persson H, Ibá?ez C F (1995). Muscle-derived neurotrophin-4 as an activity-dependent trophic signal for adult motor neurons. Science , 268(5216): 1495-1499
doi: 7770776" target="_blank">10.1126/science. pmid:7770776 pmid:7770776
24 Gómez-Pinilla F, Ying Z, Opazo P, Roy R R, Edgerton V R (2001). Differential regulation by exercise of BDNF and NT-3 in rat spinal cord and skeletal muscle. Eur J Neurosci , 13(6): 1078-1084
doi: 10.1046/j.0953-816x.2001.01484.x pmid:11285004
25 Gómez-Pinilla F, Ying Z, Roy R R, Molteni R, Edgerton V R (2002). Voluntary exercise induces a BDNF-mediated mechanism that promotes neuroplasticity. J Neurophysiol , 88(5): 2187-2195
doi: 10.1152/jn.00152.2002 pmid:12424260
26 Hashimoto M, Nitta A, Fukumitsu H, Nomoto H, Shen L, Furukawa S (2005). Involvement of glial cell line-derived neurotrophic factor in activation processes of rodent macrophages. J Neurosci Res , 79(4): 476-487
doi: 10.1002/jnr.20368 pmid:15635609
27 Henderson C E, Phillips H S, Pollock R A, Davies A M, Lemeulle C, Armanini M, Simpson L C, Moffet B, Vandlen R A, Koliatsos V E, Rosenthal A (1994). GDNF: a potent survival factor for motoneurons present in peripheral nerve and muscle. Science , 266: 1062-1064
doi: 7973664" target="_blank">10.1126/science. pmid:7973664 pmid:7973664
28 Houenou L J, Oppenheim R W, Li L, Lo A C, Prevette D (1996). Regulation of spinal motoneuron survival by GDNF during development and following injury. Cell Tissue Res , 286(2): 219-223
doi: 10.1007/s004410050690 pmid:8854890
29 Jacob J M (1998). Lumbar motor neuron size and number is affected by age in male F344 rats. Mech Ageing Dev , 106(1-2): 205-216
doi: 10.1016/S0047-6374(98)00117-1 pmid:9883984
30 Johnson F B, Sinclair D A, Guarente L (1999). Molecular biology of aging. Cell , 96(2): 291-302
doi: 10.1016/S0092-8674(00)80567-X pmid:9988222
31 Kanning K C, Kaplan A, Henderson C E (2010). Motor neuron diversity in development and disease. Annu Rev Neurosci , 33(1): 409-440
doi: 10.1146/annurev.neuro.051508.135722 pmid:20367447
32 Kaplan D R, Miller F D (2000). Neurotrophin signal transduction in the nervous system. Curr Opin Neurobiol , 10(3): 381-391
doi: 10.1016/S0959-4388(00)00092-1 pmid:10851172
33 Keller-Peck C R, Feng G, Sanes J R, Yan Q, Lichtman J W, Snider W D (2001). Glial cell line-derived neurotrophic factor administration in postnatal life results in motor unit enlargement and continuous synaptic remodeling at the neuromuscular junction. J Neurosci , 21(16): 6136-6146
pmid:11487637
34 Kramer E R, Knott L, Su F, Dessaud E, Krull C E, Helmbacher F, Klein R (2006). Cooperation between GDNF/Ret and ephrinA/EphA4 signals for motor-axon pathway selection in the limb. Neuron , 50(1): 35-47
doi: 10.1016/j.neuron.2006.02.020 pmid:16600854
35 Kullberg S, Ramírez-León V, Johnson H, Ulfhake B (1998). Decreased axosomatic input to motoneurons and astrogliosis in the spinal cord of aged rats. J Gerontol A Biol Sci Med Sci , 53A(5): B369-B379
doi: 10.1093/gerona/53A.5.B369 pmid:9754135
36 Lee R, Kermani P, Teng K K, Hempstead B L (2001). Regulation of cell survival by secreted proneurotrophins. Science , 294(5548): 1945-1948
doi: 10.1126/science.1065057 pmid:11729324
37 Li W, Brakefield D, Pan Y C, Hunter D, Myckatyn T M, Parsadanian A (2007). Muscle-derived but not centrally derived transgene GDNF is neuroprotective in G93A-SOD1 mouse model of ALS. Exp Neurol , 203(2): 457-471
doi: 10.1016/j.expneurol.2006.08.028 pmid:17034790
38 Lie D C, Weis J (1998). GDNF expression is increased in denervated human skeletal muscle. Neurosci Lett , 250(2): 87-90
doi: 10.1016/S0304-3940(98)00434-0 pmid:9697925
39 Lin L F, Doherty D H, Lile J D, Bektesh S, Collins F (1993). GDNF: a glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons. Science , 260(5111): 1130-1132
doi: 8493557" target="_blank">10.1126/science. pmid:8493557 pmid:8493557
40 McCullough M J, Peplinski N G, Kinnell K R, Spitsbergen J M (2011). Glial cell line-derived neurotrophic factor protein content in rat skeletal muscle is altered by increased physical activity in vivo and in vitro. Neuroscience , 174: 234-244
doi: 10.1016/j.neuroscience.2010.11.016 pmid:21081155
41 Michalski B, Bain J R, Fahnestock M (2008). Long-term changes in neurotrophic factor expression in distal nerve stump following denervation and reinnervation with motor or sensory nerve. J Neurochem , 105(4): 1244-1252
doi: 10.1111/j.1471-4159.2008.05224.x pmid:18194437
42 Moore M W, Klein R D, Fari?as I, Sauer H, Armanini M, Phillips H, Reichardt L F, Ryan A M, Carver-Moore K, Rosenthal A (1996). Renal and neuronal abnormalities in mice lacking GDNF. Nature , 382(6586): 76-79
doi: 10.1038/382076a0 pmid:8657308
43 Mussini I, Marchioro L (1991). Low frequency nerve stimulation of rat EDL muscle: morphology of myofibers and neuromuscular junctions. BAM , 1(1): 71-81
44 Nagano M, Suzuki H (2003). Quantitative analyses of expression of GDNF and neurotrophins during postnatal development in rat skeletal muscles. Neurosci Res , 45(4): 391-399
doi: 10.1016/S0168-0102(03)00010-5 pmid:12657452
45 Naveilhan P, ElShamy W M, Ernfors P (1997). Differential regulation of mRNAs for GDNF and its receptors Ret and GDNFR alpha after sciatic nerve lesion in the mouse. Eur J Neurosci , 9(7): 1450-1460
doi: 10.1111/j.1460-9568.1997.tb01499.x pmid:9240402
46 Nguyen Q T, Parsadanian A S, Snider W D, Lichtman J W (1998). Hyperinnervation of neuromuscular junctions caused by GDNF overexpression in muscle. Science , 279(5357): 1725-1729
doi: 10.1126/science.279.5357.1725 pmid:9497292
47 Niles L P, Armstrong K J, Rincón Castro L M, Dao C V, Sharma R, McMillan C R, Doering L C, Kirkham D L (2004). Neural stem cells express melatonin receptors and neurotrophic factors: colocalization of the MT1 receptor with neuronal and glial markers. BMC Neurosci , 5(1): 41
doi: 10.1186/1471-2202-5-41 pmid:15511288
48 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(6512): 344-346
doi: 10.1038/373344a0 pmid:7830769
49 Oppenheim R W, Houenou L J, Parsadanian A S, Prevette D, Snider W D, Shen L (2000). Glial cell line-derived neurotrophic factor and developing mammalian motoneurons: regulation of programmed cell death among motoneuron subtypes. J Neurosci , 20(13): 5001-5011
pmid:10864958
50 Pastor D, Viso-Leon M C, Jones J, Jaramillo-Merchan J, Toledo-Aral J J, Moraled J M, Martinez S (2011). Comparative effects between bone marrow and mesenchymal stem cell transplantation in GDNF expression and motor function recovery in a motorneuron degenerative mouse model. Sterm Cell Rec and Rep ,
pmid:21717132
51 Purves D, Snider W D, Voyvodic J T (1988). Trophic regulation of nerve cell morphology and innervation in the autonomic nervous system. Nature , 336(6195): 123-128
52 Reid B, Slater C R, Bewick G S (1999). Synaptic vesicle dynamics in rat fast and slow motor nerve terminals. J Neurosci , 19(7): 2511-2521
pmid:10087065
53 Ribchester R R, Thomson D, Haddow L J, Ushkaryov Y A (1998). Enhancement of spontaneous transmitter release at neonatal mouse neuromuscular junctions by the glial cell line-derived neurotrophic factor (GDNF). J Physiol , 512(3): 635-641
doi: 10.1111/j.1469-7793.1998.635bd.x pmid:9769409
54 Salvatore M F, Zhang J L, Large D M, Wilson P E, Gash C R, Thomas T C, Haycock J W, Bing G, Stanford J A, Gash D M, Gerhardt G A (2004). Striatal GDNF administration increases tyrosine hydroxylase phosphorylation in the rat striatum and substantia nigra. J Neurochem , 90(1): 245-254
doi: 10.1111/j.1471-4159.2004.02496.x pmid:15198683
55 Schatz D S, Kaufmann W A, Saria A, Humpel C (1999). Dopamine neurons in a simple GDNF-treated meso-striatal organotypic co-culture model. Exp Brain Res , 127(3): 270-278
doi: 10.1007/s002210050796 pmid:10452214
56 Sharma H S (2006). Post-traumatic application of brain-derived neurotrophic factor and glia-derived neurotrophic factor on the rat spinal cord enhances neuroprotection and improves motor function. Acta Neurochir Suppl (Wien) , 96: 329-334
doi: 10.1007/3-211-30714-1_69 pmid:16671480
57 Shneider N A, Brown M N, Smith C A, Pickel J, Alvarez F J (2009). Gamma motor neurons express distinct genetic markers at birth and require muscle spindle-derived GDNF for postnatal survival. Neural Dev , 4(1): 42
doi: 10.1186/1749-8104-4-42 pmid:19954518
58 Soler R M, Dolcet X, Encinas M, Egea J, Bayascas J R, Comella J X (1999). Receptors of the glial cell line-derived neurotrophic factor family of neurotrophic factors signal cell survival through the phosphatidylinositol 3-kinase pathway in spinal cord motoneurons. J Neurosci , 19(21): 9160-9169
pmid:10531419
59 Spitsbergen J M, Stewart J S, Tuttle J B (1995). Altered regulation of nerve growth factor secretion by cultured VSMCs from hypertensive rats. Am J Physiol , 269(2 Pt 2): H621-H628
pmid:7653626
60 Springer J E, Seeburger J L, He J, Gabrea A, Blankenhorn E P, Bergman L W (1995). cDNA sequence and differential mRNA regulation of two forms of glial cell line-derived neurotrophic factor in Schwann cells and rat skeletal muscle. Exp Neurol , 131(1): 47-52
doi: 10.1016/0014-4886(95)90006-3 pmid:7895811
61 Stoop R, Poo M M (1996). Synaptic modulation by neurotrophic factors: differential and synergistic effects of brain-derived neurotrophic factor and ciliary neurotrophic factor. J Neurosci , 16(10): 3256-3264
pmid:8627363
62 Suter-Crazzolara C, Unsicker K (1994). GDNF is expressed in two forms in many tissues outside the CNS. Neuroreport , 5(18): 2486-2488
doi: 10.1097/00001756-199412000-00020 pmid:7696586
63 Suzuki H, Hase A, Kim B Y, Miyata Y, Nonaka I, Arahata K, Akazawa C (1998a). Up-regulation of glial cell line-derived neurotrophic factor (GDNF) expression in regenerating muscle fibers in neuromuscular diseases. Neurosci Lett , 257(3): 165-167
doi: 10.1016/S0304-3940(98)00817-9 pmid:9870346
64 Suzuki H, Hase A, Miyata Y, Arahata K, Akazawa C (1998b). Prominent expression of glial cell line-derived neurotrophic factor in human skeletal muscle. J Comp Neurol , 402(3): 303-312
doi: 10.1002/(SICI)1096-9861(19981221)402:3<303::AID-CNE2>3.0.CO;2-I pmid:9853901
65 Trejo J L, Carro E, Torres-Aleman I (2001). Circulating insulin-like growth factor I mediates exercise-induced increases in the number of new neurons in the adult hippocampus. J Neurosci , 21(5): 1628-1634
pmid:11222653
66 Trupp M, Rydén M, J?rnvall H, Funakoshi H, Timmusk T, Arenas E, Ibá?ez C F (1995). Peripheral expression and biological activities of GDNF, a new neurotrophic factor for avian and mammalian peripheral neurons. J Cell Biol , 130(1): 137-148
doi: 10.1083/jcb.130.1.137 pmid:7790368
67 Ulfhake B, Bergman E, Edstrom E, Fundin B T, Johnson H, Kullberg S, Ming Y (2000). Regulation of neurotrophin signaling in aging sensory and motoneurons: dissipation of target support? Mol Neurobiol , 21(3): 109-136
doi: 10.1385/MN:21:3:109 pmid:11379795
68 Vianney J M, Spitsbergen J M (2011). Cholinergic neurons regulate secretion of glial cell line-derived neurotrophic factor by skeletal muscle cells in culture. Brain Res , 1390: 1-9
doi: 10.1016/j.brainres.2011.03.030 pmid:21420941
69 Wang C Y, Yang F, He X, Chow A, Du J, Russell J T, Lu B (2001). Ca(2+) binding protein frequenin mediates GDNF-induced potentiation of Ca(2+) channels and transmitter release. Neuron , 32(1): 99-112
doi: 10.1016/S0896-6273(01)00434-2 pmid:11604142
70 Wang C Y, Yang F, He X P, Je H S, Zhou J Z, Eckermann K, Kawamura D, Feng L, Shen L, Lu B (2002). Regulation of neuromuscular synapse development by glial cell line-derived neurotrophic factor and neurturin. J Biol Chem , 277(12): 10614-10625
doi: 10.1074/jbc.M106116200 pmid:11790765
71 Wehrwein E A, Roskelley E M, Spitsbergen J M (2002). GDNF is regulated in an activity-dependent manner in rat skeletal muscle. Muscle Nerve , 26(2): 206-211
doi: 10.1002/mus.10179 pmid:12210384
72 Wood S J, Slater C R (1997). The contribution of postsynaptic folds to the safety factor for neuromuscular transmission in rat fast- and slow-twitch muscles. J Physiol , 500(Pt 1): 165-176
pmid:9097941
73 Wu A, Ying Z, Gomez-Pinilla F (2008). Docosahexaenoic acid dietary supplementation enhances the effects of exercise on synaptic plasticity and cognition. Neurosci , 155 (30): 751-759
74 Yan Q, Matheson C, Lopez O T (1995). In vivo neurotrophic effects of GDNF on neonatal and adult facial motor neurons. Nature , 373(6512): 341-344
doi: 10.1038/373341a0 pmid:7830768
75 Yang F, He X, Feng L, Mizuno K, Liu X W, Russell J, Xiong W C, Lu B (2001). PI-3 kinase and IP3 are both necessary and sufficient to mediate NT3-induced synaptic potentiation. Nat Neurosci , 4(1): 19-28
doi: 10.1038/nn734 pmid:11135641
76 Yang L X, Nelson P G (2004). Glia cell line-derived neurotrophic factor regulates the distribution of acetylcholine receptors in mouse primary skeletal muscle cells. Neuroscience , 128(3): 497-509
doi: 10.1016/j.neuroscience.2004.06.067 pmid:15381279
77 Zhang L, Ma Z, Smith G M, Wen X, Pressman Y, Wood P M, Xu X M (2009). GDNF-enhanced axonal regeneration and myelination following spinal cord injury is mediated by primary effects on neurons. Glia , 57(11): 1178-1191
doi: 10.1002/glia.20840 pmid:19170182
78 Zhao Z Q, Alam S, Oppenheim R W, Prevette D M, Evenson A, Parsadanian A (2004). Overexpression of glial cell line-derived neurotrophic factor in the CNS rescues motoneurons from programmed cell death and promotes their long-term survival following axotomy. Exp Neurol , 190(2): 356-372
doi: 10.1016/j.expneurol.2004.06.015 pmid:15530875
79 Zhou H L, Yang H J, Li Y M, Wang Y, Yan L, Guo X L, Ba Y C, Liu S, Wang T H (2008). Changes in Glial cell line-derived neurotrophic factor expression in the rostral and caudal stumps of the transected adult rat spinal cord. Neurochem Res , 33(5): 927-937
doi: 10.1007/s11064-007-9536-1 pmid:18095158
80 Zwick M, Teng L, Mu X, Springer J E, Davis B M (2001). Overexpression of GDNF induces and maintains hyperinnervation of muscle fibers and multiple end-plate formation. Exp Neurol , 171(2): 342-350
doi: 10.1006/exnr.2001.7753 pmid:11573987
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