GDNF family ligands: A potential future for Parkinson's disease therapy

CNS and Neurological Disorders - Drug Targets

Volumn 10, Issue 6, 2011, Pages 703-711

  Mickiewicz, Amanda L ^a   Kordower, Jeffrey H ^a  

^a RUSH UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Gene therapy; Glial cell line derived neurotrophic factor; Glial cell line derived neurotrophic factor family ligands; Neuroprotection; Neurotrophic factors; Neurturin; Parkinson's disease

Indexed keywords

ADENOVIRUS VECTOR; APOMORPHINE; ARTEMIN; DOPAMINE; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; LACTOFERRIN; LENTIVIRUS VECTOR; LEVODOPA; LIATERMIN; NEURTURIN; OXIDOPAMINE; PERSEPHIN; PLACEBO;

AGING; ARTICLE; BRAIN LATERAL VENTRICLE; CELL LOSS; CLINICAL TRIAL; COGNITION; CORPUS STRIATUM; DOPAMINERGIC NERVE CELL; DRUG EFFECT; DRUG EFFICACY; DRUG SAFETY; ENZYME PHOSPHORYLATION; GENE EXPRESSION; GENE TARGETING; GENE THERAPY; HUMAN; IMMUNE RESPONSE; IMMUNOHISTOCHEMISTRY; MESENCEPHALON; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVE DEGENERATION; NEUROMODULATION; NEUROPATHOLOGY; NEUROPROTECTION; NONHUMAN; PARKINSON DISEASE; POSITRON EMISSION TOMOGRAPHY; PROTEIN FAMILY; PROTEIN ISOLATION; SUBSTANTIA NIGRA; TRANSCYTOSIS; VIRAL GENE DELIVERY SYSTEM;

EID: 80052849977     PISSN: 18715273     EISSN: 19963181     Source Type: Journal    
DOI: 10.2174/187152711797247876     Document Type: Article

References (89)

1. Kordower, J.H.; Goetz, C.G. The first miracle in neurodegenerative disease: the discovery of oral levodopa. Brain Res. Bull., 1999, 50(5-6), 377-378.
2. Miyasaki, J.M.; Martin, W.; Suchowersky, O.; Weiner, W.J.; Lang, A.E. Practice parameter: initiation of treatment for Parkinson's disease: an evidence-based review: report of the Quality Standards Subcommittee of the American Academy of Neurology. Neurology, 2002, 58(1), 11-17.
3. Chen, J.J.; Swope, D.M. Pharmacotherapy for Parkinson's disease. Pharmacotherapy, 2007, 27(12 Pt 2), 161S-173S.
4. Levi-Montalcini, R.; Hamburger, V. Selective growth stimulating effects of mouse sarcoma on the sensory and sympathetic nervous system of the chick embryo. J. Exp. Zool., 1951, 116(2), 321-361.
5. Ramaswamy, S.; Soderstrom, K.E.; Kordower, J.H. Trophic factors therapy in Parkinson's disease. Prog. Brain Res., 2009, 175, 201-216.
6. Rangasamy, S.B.; Soderstrom, K.; Bakay, R.A.; Kordower, J.H. Neurotrophic factor therapy for Parkinson's disease. Prog. Brain Res., 2010, 184, 237-264.
7. Diogenes, M.J.; Outeiro, T.F. Neurotrophic factors as a protective strategy in Parkinson's disease. CNS Neurol. Disord. Drug Targets, 2010, 9(6), 754-763.
8. Kotzbauer, P.T.; Lampe, P.A.; Heuckeroth, R.O.; Golden, J.P.; Creedon, D.J.; Johnson, E.M., Jr.; Milbrandt, J. Neurturin, a relative of glial-cell-line-derived neurotrophic factor. Nature, 1996, 384(6608), 467-470.
9. Baloh, R.H.; Tansey, M.G.; Lampe, P.A.; Fahrner, T.J.; Enomoto, H.; Simburger, K.S.; Leitner, M.L.; Araki, T.; Johnson, E.M., Jr.; Milbrandt, J. Artemin, a novel member of the GDNF ligand family, supports peripheral and central neurons and signals through the GFRalpha3-RET receptor complex. Neuron, 1998, 21(6), 1291-1302.
10. Milbrandt, J.; de Sauvage, F.J.; Fahrner, T.J.; Baloh, R.H.; Leitner, M.L.; Tansey, M.G.; Lampe, P.A.; Heuckeroth, R.O.; Kotzbauer, P.T.; Simburger, K.S.; Golden, J.P.; Davies, J.A.; Vejsada, R.; Kato, A.C.; Hynes, M.; Sherman, D.; Nishimura, M.; Wang, L.C.; Vandlen, R.; Moffat, B.; Klein, R.D.; Poulsen, K.; Gray, C.; Garces, A.; Johnson, E.M., Jr. Persephin, a novel neurotrophic factor related to GDNF and neurturin. Neuron 1998, 20(2), 245-253.
11. Airaksinen, M.S.; Titievsky, A.; Saarma, M. GDNF family neurotrophic factor signaling: four masters, one servant? Mol. Cell Neurosci., 1999, 13(5), 313-325.
12. Airaksinen, M.S.; Saarma, M. The GDNF family: signalling, biological functions and therapeutic value. Nat. Rev. Neurosci., 2002, 3(5), 383-394.
13. Saavedra, A.; Baltazar, G.; Duarte, E.P. Driving GDNF expression: the green and the red traffic lights. Prog. Neurobiol., 2008, 86(3), 186-215.
14. Worby, C.A.; Vega, Q.C.; Zhao, Y.; Chao, H.H.; Seasholtz, A.F.; Dixon, J.E. Glial cell line-derived neurotrophic factor signals through the RET receptor and activates mitogen-activated protein kinase. J. Biol. Chem., 1996, 271(39), 23619-23622.
15. van Weering, D.H.; Bos, J.L. Signal transduction by the receptor tyrosine kinase Ret. Rec. Res. Cancer Res., 1998, 154, 271-281.
16. Jing, S.; Wen, D.; Yu, Y.; Holst, P.L.; Luo, Y.; Fang, M.; Tamir, R.; Antonio, L.; Hu, Z.; Cupples, R.; Louis, J.C.; Hu, S.; Altrock, B.W.; Fox, G.M. GDNF-induced activation of the ret protein tyrosine kinase is mediated by GDNFR-alpha, a novel receptor for GDNF. Cell, 1996, 85(7), 1113-1124.
17. Treanor, J.J.; Goodman, L.; de, S.F.; Stone, D.M.; Poulsen, K.T.; Beck, C.D.; Gray, C.; Armanini, M.P.; Pollock, R.A.; Hefti, F.; Phillips, H.S.; Goddard, A.; Moore, M.W.; Buj-Bello, A.; Davies, A.M.; Asai, N.; Takahashi, M.; Vandlen, R.; Henderson, C.E.; Rosenthal, A. Characterization of a multicomponent receptor for GDNF. Nature, 1996, 382(6586), 80-83.
18. Baloh, R.H.; Tansey, M.G.; Golden, J.P.; Creedon, D.J.; Heuckeroth, R.O.; Keck, C.L.; Zimonjic, D.B.; Popescu, N.C.; Johnson, E.M., Jr.; Milbrandt, J. TrnR2, a novel receptor that mediates neurturin and GDNF signaling through Ret. Neuron, 1997, 18(5), 793-802.
19. Lindahl, M.; Poteryaev, D.; Yu, L.; Arumae, U.; Timmusk, T.; Bongarzone, I.; Aiello, A.; Pierotti, M.A.; Airaksinen, M.S.; Saarma, M. Human glial cell line-derived neurotrophic factor receptor alpha 4 is the receptor for persephin and is predominantly expressed in normal and malignant thyroid medullary cells. J. Biol. Chem., 2001, 276(12), 9344-9351.
20. Lin, L.F.; Doherty, D.H.; Lile, J.D.; Bektesh, S.; Collins, F. GDNF: a glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons. Science, 1993, 260(5111), 1130-1132.
21. Pascual, A.; Hidalgo-Figueroa, M.; Piruat, J.I.; Pintado, C.O.; Gomez-Diaz, R.; Lopez-Barneo, J. Absolute requirement of GDNF for adult catecholaminergic neuron survival. Nat. Neurosci., 2008, 11(7), 755-761.
22. Hoffer, B.J.; Hoffman, A.; Bowenkamp, K.; Huettl, P.; Hudson, J.; Martin, D.; Lin, L.F.; Gerhardt, G.A. Glial cell line-derived neurotrophic factor reverses toxin-induced injury to midbrain dopaminergic neurons in vivo. Neurosci. Lett., 1994, 182(1), 107-111.
23. Rosenblad, C.; Kirik, D.; Devaux, B.; Moffat, B.; Phillips, H.S.; Bjorklund, A. Protection and regeneration of nigral dopaminergic neurons by neurturin or GDNF in a partial lesion model of Parkinson's disease after administration into the striatum or the lateral ventricle. Eur. J. Neurosci., 1999, 11(5), 1554-1566.
24. Tomac, A.; Lindqvist, E.; Lin, L.F.; Ogren, S.O.; Young, D.; Hoffer, B.J.; Olson, L. Protection and repair of the nigrostriatal dopaminergic system by GDNF in vivo. Nature, 1995, 373(6512), 335-339.
25. Martin, D.; Miller, G.; Fischer, N.; Diz, D.; Cullen, T.; Russell, D. Glial cell line-derived neurotrophic factor: the lateral cerebral ventricle as a site of administration for stimulation of the substantia nigra dopamine system in rats. Eur. J. Neurosci., 1996, 8(6), 1249-1255.
26. Kirik, D.; Rosenblad, C.; Bjorklund, A. Preservation of a functional nigrostriatal dopamine pathway by GDNF in the intrastriatal 6-OHDA lesion model depends on the site of administration of the trophic factor. Eur. J. Neurosci., 2000, 12(11), 3871-3882.
27. Gash, D.M.; Zhang, Z.; Ovadia, A.; Cass, W.A.; Yi, A.; Simmerman, L.; Russell, D.; Martin, D.; Lapchak, P.A.; Collins, F.; Hoffer, B.J.; Gerhardt, G.A. Functional recovery in parkinsonian monkeys treated with GDNF. Nature, 1996, 380(6571), 252-255.
28. Jellinger, K. Overview of morphological changes in Parkinson's disease. Adv. Neurol., 1987, 45, 1-18.
29. Kish, S.J.; Shannak, K.; Hornykiewicz, O. Uneven pattern of dopamine loss in the striatum of patients with idiopathic Parkinson's disease. Pathophysiologic and clinical implications. N. Engl. J. Med., 1988, 318(14), 876-880.
30. Emborg, M.E.; Ma, S.Y.; Mufson, E.J.; Levey, A.I.; Taylor, M.D.; Brown, W.D.; Holden, J.E.; Kordower, J.H. Age-related declines in nigral neuronal function correlate with motor impairments in rhesus monkeys. J. Comp. Neurol., 1998, 401(2), 253-265.
31. Maswood, N.; Grondin, R.; Zhang, Z.; Stanford, J.A.; Surgener, S.P.; Gash, D.M.; Gerhardt, G.A. Effects of chronic intraputamenal infusion of glial cell line-derived neurotrophic factor(GDNF) in aged Rhesus monkeys. Neurobiol. Aging, 2002, 23(5), 881-889.
32. Grondin, R.; Zhang, Z.; Yi, A.; Cass, W.A.; Maswood, N.; Andersen, A.H.; Elsberry, D.D.; Klein, M.C.; Gerhardt, G.A.; Gash, D.M. Chronic, controlled GDNF infusion promotes structural and functional recovery in advanced parkinsonian monkeys. Brain 2002, 125(Pt 10), 2191-2201.
33. Nutt, J.G.; Burchiel, K.J.; Comella, C.L.; Jankovic, J.; Lang, A.E.; Laws, E.R., Jr.; Lozano, A.M.; Penn, R.D.; Simpson, R.K., Jr.; Stacy, M.; Wooten, G.F. Randomized, double-blind trial of glial cell line derived neurotrophic factor(GDNF) in PD. Neurology, 2003, 60(1), 69-73.
34. Kordower, J.H.; Palfi, S.; Chen, E.Y.; Ma, S.Y.; Sendera, T.; Cochran, E.J.; Cochran, E.J.; Mufson, E.J.; Penn, R.; Goetz, C.G.; Comella, C.D. Clinicopathological findings following intraventricular glial-derived neurotrophic factor treatment in a patient with Parkinson's disease. Ann. Neurol., 1999, 46(3), 419-424.
35. Gill, S.S.; Patel, N.K.; Hotton, G.R.; O'Sullivan, K.; McCarter, R.; Bunnage, M.; Brooks, D.J.; Svendsen, C.N.; Heywood, P. Direct brain infusion of glial cell line-derived neurotrophic factor in Parkinson disease. Nat. Med., 2003, 9(5), 589-595.
36. Patel, N.K.; Bunnage, M.; Plaha, P.; Svendsen, C.N.; Heywood, P.; Gill, S.S. Intraputamenal infusion of glial cell line-derived neurotrophic factor in PD: a two-year outcome study. Ann. Neurol., 2005, 57(2), 298-302.
37. Fuente-Fernandez, R.; Ruth, T.J.; Sossi, V.; Schulzer, M.; Calne, D.B.; Stoessl, A.J. Expectation and dopamine release: mechanism of the placebo effect in Parkinson's disease. Science, 2001, 293(5532), 1164-1166.
38. Goetz, C.G.; Leurgans, S.; Raman, R. Placebo-associated improvements in motor function: comparison of subjective and objective sections of the UPDRS in early Parkinson's disease. Mov. Disord., 2002, 17(2), 283-288.
39. Love, S.; Plaha, P.; Patel, N.K.; Hotton, G.R.; Brooks, D.J.; Gill, S.S. Glial cell line-derived neurotrophic factor induces neuronal sprouting in human brain. Nat. Med., 2005, 11(7), 703-704.
40. Slevin, J.T.; Gerhardt, G.A.; Smith, C.D.; Gash, D.M.; Kryscio, R.; Young, B. Improvement of bilateral motor functions in patients with Parkinson disease through the unilateral intraputaminal infusion of glial cell line-derived neurotrophic factor. J. Neurosurg., 2005, 102(2), 216-222.
41. Slevin, J.T.; Gash, D.M.; Smith, C.D.; Gerhardt, G.A.; Kryscio, R.; Chebrolu, H.; Walton, A.; Wagner, R.; Young, A.B. Unilateral intraputamenal glial cell line-derived neurotrophic factor in patients with Parkinson disease: response to 1 year of treatment and 1 year of withdrawal. J. Neurosurg., 2007, 106(4), 614-620.
42. Lang, A.E.; Gill, S.; Patel, N.K.; Lozano, A.; Nutt, J.G.; Penn, R.; Brooks, D.J.; Hotton, G.; Moro, E.; Heywood, P.; Brodsky, M.A.; Burchiel, K.; Kelly, P.; Dalvi, A.; Scott, B.; Stacy, M.; Turner, D.; Wooten, V.G.; Elias, W.J.; Laws, E.R.; Dhawan, V.; Stoessl, A.J.; Matcham, J.; Coffey, R.J.; Traub, M. Randomized controlled trial of intraputamenal glial cell line-derived neurotrophic factor infusion in Parkinson disease. Ann. Neurol., 2006, 59(3), 459-466.
43. Gash, D.M.; Zhang, Z.; Ai, Y.; Grondin, R.; Coffey, R.; Gerhardt, G.A. Trophic factor distribution predicts functional recovery in parkinsonian monkeys. Ann. Neurol., 2005, 58(2), 224-233.
44. Salvatore, M.F.; Ai, Y.; Fischer, B.; Zhang, A.M.; Grondin, R.C.; Zhang, Z.; Gerhardt, G.A.; Gash, D.M. Point source concentration of GDNF may explain failure of phase II clinical trial. Exp. Neurol., 2006, 202(2), 497-505.
45. Morrison, P.F.; Lonser, R.R.; Oldfield, E.H. Convective delivery of glial cell line-derived neurotrophic factor in the human putamen. J. Neurosurg., 2007, 107(1), 74-83.
46. Bjorklund, A.; Kirik, D.; Rosenblad, C.; Georgievska, B.; Lundberg, C.; Mandel, R.J. Towards a neuroprotective gene therapy for Parkinson's disease: use of adenovirus, AAV and lentivirus vectors for gene transfer of GDNF to the nigrostriatal system in the rat Parkinson model. Brain Res., 2000, 886(1-2), 82-98.
47. Choi-Lundberg, D.L.; Lin, Q.; Chang, Y.N.; Chiang, Y.L.; Hay, C.M.; Mohajeri, H.; Davidson, B.L.; Bohn, M.C. Dopaminergic neurons protected from degeneration by GDNF gene therapy. Science, 1997, 275(5301), 838-841.
48. Lapchak, P.A.; Araujo, D.M.; Hilt, D.C.; Sheng, J.; Jiao, S. Adenoviral vector-mediated GDNF gene therapy in a rodent lesion model of late stage Parkinson's disease. Brain Res., 1997, 777(1-2), 153-160.
49. Choi-Lundberg, D.L.; Lin, Q.; Schallert, T.; Crippens, D.; Davidson, B.L.; Chang, Y.N.; Chiang, Y.L.; Qian, J.; Bardwaj, L.; Bohn, M.C. Behavioral and cellular protection of rat dopaminergic neurons by an adenoviral vector encoding glial cell line-derived neurotrophic factor. Exp. Neurol., 1998, 154(2), 261-275.
50. Bilang-Bleuel, A.; Revah, F.; Colin, P.; Locquet, I.; Robert, J.J.; Mallet, J.; Horellou, P. Intrastriatal injection of an adenoviral vector expressing glial-cell-line-derived neurotrophic factor prevents dopaminergic neuron degeneration and behavioral impairment in a rat model of Parkinson disease. Proc. Natl. Acad. Sci. USA, 1997, 94(16), 8818-8823.
51. Naldini, L.; Blomer, U.; Gage, F.H.; Trono, D.; Verma, I.M. Efficient transfer, integration, and sustained long-term expression of the transgene in adult rat brains injected with a lentiviral vector. Proc. Natl. Acad. Sci. USA, 1996, 93(21), 11382-11388.
52. Naldini, L.; Blomer, U.; Gallay, P.; Ory, D.; Mulligan, R.; Gage, F.H.; Verma, I.M.; Trono, D. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science, 1996, 272(5259), 263-267.
53. Deglon, N.; Tseng, J.L.; Bensadoun, J.C.; Zurn, A.D.; Arsenijevic, Y.; Pereira de, A.L.; Zufferey, R.; Trono, D.; Aebischer, P. Self- inactivating lentiviral vectors with enhanced transgene expression as potential gene transfer system in Parkinson's disease. Hum. Gene Ther., 2000, 11(1), 179-190.
54. Bensadoun, J.C.; Deglon, N.; Tseng, J.L.; Ridet, J.L.; Zurn, A.D.; Aebischer, P. Lentiviral vectors as a gene delivery system in the mouse midbrain: cellular and behavioral improvements in a 6-OHDA model of Parkinson's disease using GDNF. Exp. Neurol., 2000, 164(1), 15-24.
55. Georgievska, B.; Kirik, D.; Bjorklund, A. Aberrant sprouting and downregulation of tyrosine hydroxylase in lesioned nigrostriatal dopamine neurons induced by long-lasting overexpression of glial cell line derived neurotrophic factor in the striatum by lentiviral gene transfer. Exp. Neurol., 2002, 177(2), 461-474.
56. Georgievska, B.; Kirik, D.; Rosenblad, C.; Lundberg, C.; Bjorklund, A. Neuroprotection in the rat Parkinson model by intrastriatal GDNF gene transfer using a lentiviral vector. Neuroreport, 2002, 13(1), 75-82.
57. Lo Bianco C.; Ridet, J.L.; Schneider, B.L.; Deglon, N.; Aebischer, P. Alpha-Synucleinopathy and selective dopaminergic neuron loss in a rat lentiviral-based model of Parkinson's disease. Proc. Natl. Acad. Sci. USA, 2002, 99(16), 10813-10818.
58. Lo Bianco C.; Deglon, N.; Pralong, W.; Aebischer, P. Lentiviral nigral delivery of GDNF does not prevent neurodegeneration in a genetic rat model of Parkinson's disease. Neurobiol. Dis., 2004, 17(2), 283-289.
59. Kordower, J.H.; Bloch, J.; Ma, S.Y.; Chu, Y.; Palfi, S.; Roitberg, B.Z.; Emborg, M.; Hantraye, P.; Deglon, N.; Aebischer, P. Lentiviral gene transfer to the nonhuman primate brain. Exp. Neurol., 1999, 160(1), 1-16.
60. Kordower, J.H.; Emborg, M.E.; Bloch, J.; Ma, S.Y.; Chu, Y.; Leventhal, L.; McBride, J.; Chen, E.Y.; Palfi, S.; Roitberg, B.Z.; Brown, W.D.; Holden, J.E.; Pyzalski, R.; Taylor, M.D.; Carvey, P.; Ling, Z.; Trono, D.; Hantraye, P.; Deglon, N.; Aebischer, P. Neurodegeneration prevented by lentiviral vector delivery of GDNF in primate models of Parkinson's disease. Science, 2000, 290(5492), 767-773.
61. Chu, Y.; Le, W.; Kompoliti, K.; Jankovic, J.; Mufson, E.J.; Kordower, J.H. Nurr1 in Parkinson's disease and related disorders. J. Comp. Neurol., 2006, 494(3), 495-514.
62. Mandel, R.J.; Spratt, S.K.; Snyder, R.O.; Leff, S.E. Midbrain injection of recombinant adeno-associated virus encoding rat glial cell line- derived neurotrophic factor protects nigral neurons in a progressive 6- hydroxydopamine-induced degeneration model of Parkinson's disease in rats. Proc. Natl. Acad. Sci. USA, 1997, 94(25), 14083-14088.
63. Kirik, D.; Rosenblad, C.; Bjorklund, A.; Mandel, R.J. Long-term rAAV-mediated gene transfer of GDNF in the rat Parkinson's model: intrastriatal but not intranigral transduction promotes functional regeneration in the lesioned nigrostriatal system. J. Neurosci., 2000, 20(12), 4686-4700.
64. Eslamboli, A.; Cummings, R.M.; Ridley, R.M.; Baker, H.F.; Muzyczka, N.; Burger, C.; Mandel, R.J.; Kirik, D.; Annett, L.E. Recombinant adeno-associated viral vector(rAAV) delivery of GDNF provides protection against 6-OHDA lesion in the common marmoset monkey(Callithrix jacchus). Exp. Neurol., 2003, 184(1), 536-548.
65. Eberling, J.L.; Kells, A.P.; Pivirotto, P.; Beyer, J.; Bringas, J.; Federoff, H.J.; Forsayeth, J.; Bankiewicz, K.S. Functional effects of AAV2- GDNF on the dopaminergic nigrostriatal pathway in parkinsonian rhesus monkeys. Hum. Gene Ther., 2009, 20(5), 511-518.
66. Widenfalk, J.; Nosrat, C.; Tomac, A.; Westphal, H.; Hoffer, B.; Olson, L. Neurturin and glial cell line-derived neurotrophic factor receptor- beta(GDNFR-beta), novel proteins related to GDNF and GDNFR-alpha with specific cellular patterns of expression suggesting roles in the developing and adult nervous system and in peripheral organs. J. Neurosci., 1997, 17(21), 8506-8519.
67. Burazin, T.C.; Gundlach, A.L. Localization of GDNF/neurturin receptor(c-ret, GFRalpha-1 and alpha-2) mRNAs in postnatal rat brain: differential regional and temporal expression in hippocampus, cortex and cerebellum. Brain Res. Mol. Brain Res., 1999, 73(1-2), 151-171.
68. Horger, B.A.; Nishimura, M.C.; Armanini, M.P.; Wang, L.C.; Poulsen, K.T.; Rosenblad, C.; Kirik, D.; Moffat, B.; Simmons, L.; Johnson E Jr; Milbrandt, J.; Rosenthal, A.; Bjorklund, A.; Vandlen, R.A.; Hynes, M.A.; Phillips, H.S. Neurturin exerts potent actions on survival and function of midbrain dopaminergic neurons. J. Neurosci., 1998, 18(13), 4929-4937.
69. Sanicola, M.; Hession, C.; Worley, D.; Carmillo, P.; Ehrenfels, C.; Walus, L.; Robinson, S.; Jaworski, G.; Wei, H.; Tizard, R.; Whitty, A.; Pepinsky, R.B.; Cate, R.L. Glial cell line-derived neurotrophic factor- dependent RET activation can be mediated by two different cell-surface accessory proteins. Proc. Natl. Acad. Sci. USA, 1997, 94(12), 6238-6243.
70. Tseng, J.L.; Bruhn, S.L.; Zurn, A.D.; Aebischer, P. Neurturin protects dopaminergic neurons following medial forebrain bundle axotomy. Neuroreport, 1998, 9(8), 1817-1822.
71. Oiwa, Y.; Yoshimura, R.; Nakai, K.; Itakura, T. Dopaminergic neuroprotection and regeneration by neurturin assessed by using behavioral, biochemical and histochemical measurements in a model of progressive Parkinson's disease. Brain Res., 2002, 947(2), 271-283.
72. Gasmi, M.; Herzog, C.D.; Brandon, E.P.; Cunningham, J.J.; Ramirez, G.A.; Ketchum, E.T.; Bartus, R.T. Striatal delivery of neurturin by CERE-120, an AAV2 vector for the treatment of dopaminergic neuron degeneration in Parkinson's disease. Mol. Ther., 2007, 15(1), 62-68.
73. Gasmi, M.; Brandon, E.P.; Herzog, C.D.; Wilson, A.; Bishop, K.M.; Hofer, E.K.; Cunningham, J.J.; Printz, M.A.; Kordower, J.H.; Bartus, R.T. AAV2-mediated delivery of human neurturin to the rat nigrostriatal system: long-term efficacy and tolerability of CERE-120 for Parkinson's disease. Neurobiol. Dis., 2007, 27(1), 67-76.
74. Herzog, C.D.; Dass, B.; Holden, J.E.; Stansell, J., III; Gasmi, M.; Tuszynski, M.H.; Bartus, R.T.; Kordower, J.H. Striatal delivery of CERE-120, an AAV2 vector encoding human neurturin, enhances activity of the dopaminergic nigrostriatal system in aged monkeys. Mov. Disord., 2007, 22(8), 1124-1132.
75. Collier, T.J.; Kanaan, N.M.; Kordower, J.H. Ageing as a primary risk factor for Parkinson's disease: evidence from studies of non-human primates. Nat. Rev. Neurosci., 2011, 12(6), 359-366.
76. Collier, T.J.; Lipton, J.; Daley, B.F.; Palfi, S.; Chu, Y.; Sortwell, C.; Bakay, R.A.; Sladek, J.R., Jr.; Kordower, J.H. Aging-related changes in the nigrostriatal dopamine system and the response to MPTP in nonhuman primates: diminished compensatory mechanisms as a prelude to parkinsonism. Neurobiol. Dis., 2007, 26(1), 56-65.
77. Kordower, J.H.; Herzog, C.D.; Dass, B.; Bakay, R.A.; Stansell, J., III; Gasmi, M.; Bartus, R.T. Delivery of neurturin by AAV2(CERE-120)- mediated gene transfer provides structural and functional neuroprotection and neurorestoration in MPTP-treated monkeys. Ann. Neurol., 2006, 60(6), 706-715.
78. Marks, W.J., Jr.; Ostrem, J.L.; Verhagen, L.; Starr, P.A.; Larson, P.S.; Bakay, R.A.; Taylor, R.; Cahn-Weiner, D.A.; Stoessl, A.J.; Olanow, C.W.; Bartus, R.T. Safety and tolerability of intraputaminal delivery of CERE-120(adeno-associated virus serotype 2-neurturin) to patients with idiopathic Parkinson's disease: an open-label, phase I trial. Lancet Neurol., 2008, 7(5), 400-408.
79. Marks, W.J., Jr.; Bartus, R.T.; Siffert, J.; Davis, C.S.; Lozano, A.; Boulis, N.; Vitek, J.; Stacy, M.; Turner, D.; Verhagen, L.; Bakay, R.; Watts, R.; Guthrie, B.; Jankovic, J.; Simpson, R.; Tagliati, M.; Alterman, R.; Stern, M.; Baltuch, G.; Starr, P.A.; Larson, P.S.; Ostrem, J.L.; Nutt, J.; Kieburtz, K.; Kordower, J.H.; Olanow, C.W. Gene delivery of AAV2-neurturin for Parkinson's disease: a double-blind, randomised, controlled trial. Lancet Neurol., 2010, 9(12), 1164-1172.
80. Ceregene, I. Ceregene presents additional clinical data from Phase 2 trial of CERE-120 for Parkinson's disease. 2011, http://www.drugs.com/clinical_trials/ceregene-presents-additional-clinical-data-phase-2-trial-cere-120-parkinson-s-7301.html
81. Ceregene, I. Ceregene has initiated a new Phase 1/2 trial of CERE-120 for Parkinson's disease. 2011, http://www.pdonlineresearch.org/news/2010-04/28/ceregene-hasinitiated-new-phase-12-trial-cere-120-parkinsons-disease
82. Biju, K.; Zhou, Q.; Li, G.; Imam, S.Z.; Roberts, J.L.; Morgan, W.W.; Clark, R.A.; Li, S. Macrophage-mediated GDNF delivery protects against dopaminergic neurodegeneration: a therapeutic strategy for Parkinson's disease. Mol. Ther., 2010, 18(8), 1536-1544.
83. Boado, R.J.; Zhang, Y.; Zhang, Y.; Wang, Y.; Pardridge, W.M. GDNF fusion protein for targeted-drug delivery across the human blood-brain barrier. Biotechnol. Bioeng., 2008, 100(2), 387-396.
84. Boado, R.J.; Pardridge, W.M. Comparison of blood-brain barrier transport of glial-derived neurotrophic factor(GDNF) and an IgGGDNF fusion protein in the rhesus monkey. Drug Metab. Dispos., 2009, 37(12), 2299-2304.
85. Zhou, Q.H.; Boado, R.J.; Lu, J.Z.; Hui, E.K.; Pardridge, W.M. Monoclonal antibody-glial-derived neurotrophic factor fusion protein penetrates the blood-brain barrier in the mouse. Drug Metab. Dispos., 2010, 38(4), 566-572.
86. Fu, A.; Zhou, Q.H.; Hui, E.K.; Lu, J.Z.; Boado, R.J.; Pardridge, W.M. Intravenous treatment of experimental Parkinson's disease in the mouse with an IgG-GDNF fusion protein that penetrates the blood-brain barrier. Brain Res., 2010, 1352, 208-213.
87. Pardridge, W.M.; Boado, R.J. Pharmacokinetics and safety in rhesus monkeys of a monoclonal antibody-GDNF fusion protein for targeted blood-brain barrier delivery. Pharm. Res., 2009, 26(10), 2227-2236.
88. Kratzer, I.; Wernig, K.; Panzenboeck, U.; Bernhart, E.; Reicher, H.; Wronski, R.; Windisch, M.; Hammer, A.; Malle, E.; Zimmer, A.; Sattler, W. Apolipoprotein A-I coating of protamine-oligonucleotide nanoparticles increases particle uptake and transcytosis in an in vitro model of the blood-brain barrier. J. Control. Release, 2007, 117(3), 301-311.
89. Huang, R.; Ke, W.; Liu, Y.; Jiang, C.; Pei, Y. The use of lactoferrin as a ligand for targeting the polyamidoamine-based gene delivery system to the brain. Biomaterials, 2008, 29(2), 238-246.