An engineered zinc finger protein activator of the endogenous glial cell line-derived neurotrophic factor gene provides functional neuroprotection in a rat model of Parkinson's disease

Journal of Neuroscience

Volumn 30, Issue 49, 2010, Pages 16469-16474

  Laganiere, Josee ^a   Kells, Adrian P ^b   Lai, Jeffrey T ^a   Guschin, Dmitry ^a   Paschon, David E ^a   Meng, Xiangdong ^a   Fong, Lauren K ^a   Yu, Qi ^a   Rebar, Edward J ^a   Gregory, Philip D ^a   Bankiewicz, Krystof S ^b   Forsayeth, John ^b   Zhang, H Steve ^a  

^a SANGAMO BIOSCIENCES INC   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMPHETAMINE; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; OXIDOPAMINE; PARVOVIRUS VECTOR; ZINC FINGER PROTEIN;

AKINESIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CIRCLING BEHAVIOR; CONTROLLED STUDY; CORPUS STRIATUM; GENE ACTIVATION; GENE EXPRESSION; HUMAN; HUMAN CELL; NEUROPROTECTION; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN ENGINEERING; RAT; SEROTYPE; VIRAL GENE THERAPY;

AMPHETAMINE; ANIMALS; CELL LINE; DISEASE MODELS, ANIMAL; DOPAMINE AGENTS; ENZYME-LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION REGULATION; GENE THERAPY; GENETIC VECTORS; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTORS; GREEN FLUORESCENT PROTEINS; HAPLORHINI; HUMANS; LENTIVIRUS; MICE; MICROARRAY ANALYSIS; MOTOR ACTIVITY; NEUROPROTECTIVE AGENTS; OXIDOPAMINE; PARKINSON DISEASE; PROTEIN ENGINEERING; RATS; RNA, MESSENGER; TIME FACTORS; TRANSFECTION; TYROSINE 3-MONOOXYGENASE; ZINC FINGERS;

EID: 78650044247     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2440-10.2010     Document Type: Article

References (31)

1. Airaksinen MS, Titievsky A, Saarma M (1999) GDNF family neurotrophic factor signaling: four masters, one servant? Mol Cell Neurosci 13:313-325.
2. Christine CW, Starr PA, Larson PS, Eberling JL, Jagust WJ, Hawkins RA, VanBrocklin HF, Wright JF, Bankiewicz KS, Aminoff MJ (2009) Safety and tolerability of putaminal AADC gene therapy for Parkinson disease. Neurology 73:1662-1669.
3. Eberling JL, Jagust WJ, Christine CW, Starr P, Larson P, Bankiewicz KS, Aminoff MJ (2008) Results from a phase I safety trial of hAADC gene therapy for Parkinson disease. Neurology 70:1980-1983.
4. Eberling JL, Kells AP, Pivirotto P, Beyer J, Bringas J, Federoff HJ, Forsayeth J, Bankiewicz KS (2009) Functional effects of AAV2-GDNF on the dopaminergic nigrostriatal pathway in parkinsonian rhesus monkeys. Hum Gene Ther 20:511-518.
5. Engele J, Bohn MC (1991) The neurotrophic effects of fibroblast growth factors on dopaminergic neurons in vitro are mediated by mesencephalic glia. J Neurosci 11:3070-3078.
6. Fiandaca MS, Forsayeth JR, Dickinson PJ, Bankiewicz KS (2008) Image-guided convection-enhanced delivery platform in the treatment of neurological diseases. Neurotherapeutics 5:123-127.
7. Fitzsimmons DF, Moloney TC, Dowd E (2006) Further validation of the corridor task for assessing deficit and recovery in the hemi-Parkinsonian rat: restoration of bilateral food retrieval by dopamine receptor agonism. Behav Brain Res 169:352-355.
8. Gasmi M, Brandon EP, Herzog CD, Wilson A, Bishop KM, Hofer EK, Cunningham JJ, Printz MA, Kordower JH, Bartus RT (2007) 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 27:67-76.
9. Gill SS, Patel NK, Hotton GR, O'Sullivan K, McCarter R, Bunnage M, Brooks DJ, Svendsen CN, Heywood P (2003) Direct brain infusion of glial cell line-derived neurotrophic factor in Parkinson disease. Nat Med 9:589-595.
10. Grondin R, Cass WA, Zhang Z, Stanford JA, Gash DM, Gerhardt GA (2003) Glial cell line-derived neurotrophic factor increases stimulus-evoked dopamine release and motor speed in aged rhesus monkeys. J Neurosci 23:1974-1980.
11. Hovland DN Jr, Boyd RB, Butt MT, Engelhardt JA, Moxness MS, Ma MH, Emery MG, Ernst NB, Reed RP, Zeller JR, Gash DM, Masterman DM, Potter BM, Cosenza ME, Lightfoot RM (2007) Six-month continuous intraputamenal infusion toxicity study of recombinant methionyl human glial cell line-derived neurotrophic factor (r-metHuGDNF in rhesus monkeys. Toxicol Pathol 35:1013-1029.
12. Jamieson AC, Miller JC, Pabo CO (2003) Drug discovery with engineered zinc-finger proteins. Nat Rev Drug Discov 2:361-368.
13. Kells AP, Eberling J, Su X, Pivirotto P, Bringas J, Hadaczek P, Narrow WC, Bowers WJ, Federoff HJ, Forsayeth J, Bankiewicz KS (2010) Regeneration of the MPTP-lesioned dopaminergic system after convection-enhanced delivery of AAV2-GDNF. J Neurosci 30:9567-9577.
14. Lang AE, Gill S, Patel NK, Lozano A, Nutt JG, Penn R, Brooks DJ, Hotton G, Moro E, Heywood P, Brodsky MA, Burchiel K, Kelly P, Dalvi A, Scott B, Stacy M, Turner D, Wooten VG, Elias WJ, Laws ER, et al. (2006) Randomized controlled trial of intraputamenal glial cell line-derived neurotrophic factor infusion in Parkinson disease. Ann Neurol 59:459-466.
15. Lin LF, Doherty DH, Lile JD, Bektesh S, Collins F (1993) GDNF: a glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons. Science 260:1130-1132. (Pubitemid 23186789)
16. Liu PQ, Rebar EJ, Zhang L, Liu Q, Jamieson AC, Liang Y, Qi H, Li PX, Chen B, Mendel MC, Zhong X, Lee YL, Eisenberg SP, Spratt SK, Case CC, Wolffe AP (2001) Regulation of an endogenous locus using a panel of designed zinc finger proteins targeted to accessible chromatin regions. Activation of vascular endothelial growth factor A. J Biol Chem 276:11323-11334.
17. Manfredsson FP, Burger C, Rising AC, Zuobi-Hasona K, Sullivan LF, Lewin AS, Huang J, Piercefield E, Muzyczka N, Mandel RJ (2009a) Tight longterm dynamic doxycycline responsive nigrostriatal GDNF using a single rAAV vector. Mol Ther 17:1857-1867.
18. Manfredsson FP, Tumer N, Erdos B, Landa T, Broxson CS, Sullivan LF, Rising AC, Foust KD, Zhang Y, Muzyczka N, Gorbatyuk OS, Scarpace PJ, Mandel RJ (2009b) Nigrostriatal rAAV-mediated GDNF overexpression induces robust weight loss in a rat model of age-related obesity. Mol Ther 17:980-991.
19. Matsushita T, Elliger S, Elliger C, Podsakoff G, Villarreal L, Kurtzman GJ, Iwaki Y, Colosi P (1998) Adeno-associated virus vectors can be efficiently produced without helper virus. Gene Ther 5:938-945.
20. Moore M, Choo Y, Klug A (2001a) Design of polyzinc finger peptides with structured linkers. Proc Natl Acad Sci U S A 98:1432-1436.
21. Moore M, Klug A, Choo Y (2001b) Improved DNA binding specificity from polyzinc finger peptides by using strings of two-finger units. Proc Natl Acad Sci U S A 98:1437-1441.
22. Oiwa Y, Sanchez-Pernaute R, Harvey-White J, Bankiewicz KS (2003) Progressive and extensive dopaminergic degeneration induced by convection-enhanced delivery of 6-hydroxydopamine into the rat striatum: a novel rodent model of Parkinson disease. J Neurosurg 98:136-144.
23. Pascual A, Hidalgo-Figueroa M, Piruat JI, Pintado CO, Gómez-Díaz R, López-Barneo J (2008) Absolute requirement of GDNF for adult catecholaminergic neuron survival. Nat Neurosci 11:755-761.
24. Peterson AL, Nutt JG (2008) Treatment of Parkinson's disease with trophic factors. Neurotherapeutics 5:270-280.
25. Salvatore MF, Ai Y, Fischer B, Zhang AM, Grondin RC, Zhang Z, Gerhardt GA, Gash DM (2006) Point source concentration of GDNF may explain failure of phase II clinical trial. Exp Neurol 202:497-505.
26. Sariola H, Saarma M (2003) Novel functions and signalling pathways for GDNF. J Cell Sci 116:3855-3862.
27. Schallert T, Fleming SM, Leasure JL, Tillerson JL, Bland ST (2000) CNS plasticity and assessment of forelimb sensorimotor outcome in unilateral rat models of stroke, cortical ablation, parkinsonism and spinal cord injury. Neuropharmacology 39:777-787.
28. Slevin JT, Gerhardt GA, Smith CD, Gash DM, Kryscio R, Young B (2005) Improvement of bilateral motor functions in patients with Parkinson disease through the unilateral intraputaminal infusion of glial cell line-derived neurotrophic factor. J Neurosurg 102:216-222.
29. Su X, Kells AP, Huang EJ, Lee HS, Hadaczek P, Beyer J, Bringas J, Pivirotto P, Penticuff J, Eberling J, Federoff HJ, Forsayeth J, Bankiewicz KS (2009) Safety evaluation of AAV2-GDNF gene transfer into the dopaminergic nigrostriatal pathway in aged and parkinsonian rhesus monkeys. Hum Gene Ther 20:1627-1640.
30. Tiscornia G, Singer O, Verma IM (2006) Production and purification of lentiviral vectors. Nat Protoc 1:241-245.
31. Yokoi K, Zhang HS, Kachi S, Balaggan KS, Yu Q, Guschin D, Kunis M, Surosky R, Africa LM, Bainbridge JW, Spratt SK, Gregory PD, Ali RR, Campochiaro PA (2007) Gene transfer of an engineered zinc finger protein enhances the anti-angiogenic defense system. Mol Ther 15:1917-1923.