Encapsulated GDNF-producing C2C12 cells for Parkinson's disease: A pre-clinical study in chronic MPTP-treated baboons

Neurobiology of Disease

Volumn 16, Issue 2, 2004, Pages 428-439

  Kishima, Haruhiko ^a   Poyot, Thomas ^a   Bloch, Jocelyne ^b   Dauguet, Julien ^a   Condé, Francoise ^a   Dollé, Frédéric ^a   Hinnen, Francoise ^a   Pralong, William ^b   Palfi, Stéphane ^a,c   Déglon, Nicole ^b   Aebischer, Patrick ^b   Hantraye, Philippe ^a  

^a SERVICE HOSPITALIER FRÉDÉRIC JOLIOT   (France)

^b EPFL   (Switzerland)

^c HENRI MONDOR HOSPITAL   (France)

Author keywords

1 methyl 4 phenyl 1,2,3,6 tetrahydropyridine; Baboon; Glial cell line derived neurotrophic factor; Macroencapsulation; Neurotrophic factor; Parkinson disease

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; NEUROTROPHIC FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BABOON; CAUDATE NUCLEUS; CELL LINE; CONTROLLED STUDY; CONVALESCENCE; DOPAMINERGIC SYSTEM; DRUG CAPSULE; DRUG INFUSION; ENCAPSULATION; GENETIC ENGINEERING; HYPOKINESIA; IMPLANTATION; MALE; MOTOR DYSFUNCTION; NEUROPROTECTION; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; STRIATE CORTEX; SUBSTANTIA NIGRA;

ANIMALS; CAPSULES; DIHYDROXYPHENYLALANINE; FLUORINE RADIOISOTOPES; GENE THERAPY; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; LATERAL VENTRICLES; MAGNETIC RESONANCE IMAGING; MALE; MOTOR ACTIVITY; NERVE GROWTH FACTORS; NEUROGLIA; NEURONS; PAPIO; PARKINSONIAN DISORDERS; RECOVERY OF FUNCTION; SUBSTANTIA NIGRA; TOMOGRAPHY, EMISSION-COMPUTED; TYROSINE 3-MONOOXYGENASE;

EID: 2942555115     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2004.03.012     Document Type: Article

References (53)

1. Adam L.E., Zaers J., Ostertag H., Trojan H., Belleman M.E., Brix G. Performance evaluation of the whole-body PET scanner ECAT EXACT HR+ following the IEC standard. IEEE Trans. Nucl. Sci. 44:1997;1172-1179
2. Aebischer P., Pralong W. Gene therapy approaches for Parkinson's disease. J. Neurochem. 85(Suppl 2:8):2003
3. Aebischer P., Schluep M., Deglon N., Joseph J.M., Hirt L., Heyd B., Goddard M., Hammang J.P., Zurn A.D., Kato A.C., Regli F., Baetge E.E. Intrathecal delivery of CNTF using encapsulated genetically modified xenogeneic cells in amyotrophic lateral sclerosis patients. Nat. Med. 2:1996;696-699
4. Bachoud-Levi A.C., Deglon N., Nguyen J.P., Bloch J., Bourdet C., Winkel L., Remy P., Goddard M., Lefaucheur J.P., Brugieres P., Baudic S., Cesaro P., Peschanski M., Aebischer P. Neuroprotective gene therapy for Huntington's disease using a polymer encapsulated BHK cell line engineered to secrete human CNTF. Hum. Gene Ther. 11:2000;23-29
5. Banknieder A.R., Phillips J.M., Jackson K.T., Vinal S.I. Jr. Comparison of ketmine with the combination of ketamine and xylazine for effective anesthesia in the rhesus monkey (Macaca mulatta). Lab. Anim. Sci. 28:1978;742-745
6. Beck K.D., Valverde J., Alexi T., Poulsen K., Moffat B., Vandlen R.A., Rosenthal A., Hefti F. Mesencephalic dopaminergic neurons protected by GDNF from axotomy-induced degeneration in the adult brain. Nature. 373:1995;339-341
7. Betarbet R., Turner R., Chockkan V., DeLong M.R., Allers K.A., Walters J., Levey A.I., Greenamyre J.T. Dopaminergic neurons intrinsic to the primate striatum. J. Neurosci. 17:1997;6761-6768
8. Björklund A., Rosenblad C., Winkler C., Kirik D. Studies on neuroprotective and regenerative effects of GDNF in a partial lesion model of Parkinson's disease. Neurobiol. Dis. 4:1997;186-200
9. Björklund 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. 886:2000;82-98
10. Blanchet P.J., Konitsiotis S., Mochizuki H., Pluta R., Emerich D.F., Chase T.N., Mouradian M.M. Complications of a trophic xenotransplant approach in parkinsonian monkeys. Prog. Neuro-Psychopharmacol. Biol. Psychiatry. 27:2003;607-612
11. Deglon N., Heyd B., Tan S.A., Joseph J.M., Zurn A.D., Aebischer P. Central nervous system delivery of recombinant ciliary neurotrophic factor by polymer encapsulated differentiated C2C12 myoblasts. Hum. Gene Ther. 7:1996;2135-2146
12. Dollé F., Demphel S., Hinnen F., Fournier D., Vaufrey F., Crouzel C. 6-[18F]Fluoro-L-DOPA by radiofluorodestannylation: a short and simple synthesis of a new labeling precursor. J. Labelled Compd. Radiopharm. 41:1998;105-114
13. Dubach M., Schmidt R., Kunkel D., Bowden D.M., Martin R., German D.C. Primate neostriatal neurons containing tyrosine hydroxylase: immunohistochemical evidence. Neurosci. Lett. 75:1987;205-210
14. Freed C.R., Greene P.E., Breeze R.E., Tsai W.Y., DuMouchel W., Kao R., Dillon S., Winfield H., Culver S., Trojanowski J.Q., Eidelberg D., Fahn S. Transplantation of embryonic dopamine neurons for severe Parkinson's disease. N. Engl. J. Med. 344:2001;710-719
15. Friston K.J., Frith C.D., Liddle P.F., Frackowiak R.S. Comparing functional (PET) images: the assessment of significant change. J. Cereb. Blood Flow Metab. 11:1991;690-699
16. Friston K.J., Ashburner J., Poline J.B., Frith C.D., Heather J.D., Frackowiak R.S.J. Spatial registration and normalization of images. Hum. Brain Mapp. 2:1995;165-189
17. Friston K.J., Holmes A.P., Worsley K.J., Poline J.P., Frith C.D., Frackowiak R.S.J. Statistical parametric maps in functional imaging: a general linear approach. Hum. Brain Mapp. 2:1995;189-210
18. 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. 21:1996;252-255
19. 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. 13:2002;75-82
20. 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. 9:2003;589-595
21. 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. 125:2002;2191-2201
22. Hantraye P., Varastet M., Peschanski M., Riche D., Cesaro P., Willer J.C., Maziere M. Stable parkinsonian syndrome and uneven loss of striatal dopamine fibres following chronic MPTP administration in baboons. Neuroscience. 53:1993;169-178
23. Hsu S.M., Raine L., Fanger H. Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabeled antibody (PAP) procedures. J. Histochem. Cytochem. 29:1981;577-580
24. 18F-DOPA PET shows bilaterally reduced striatal and nigral dopaminergic function in early Parkinson's disease. J. Neurol., Neurosurg. Psychiatry. 66:1999;754-758
25. 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. 46:1999;419-424
26. 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. 290:2000;767-773
27. Kumar R., Lozano A.M., Kim Y.J., Hutchison W.D., Sime E., Halket E., Lang A.E. Double-blind evaluation of subthalamic nucleus deep brain stimulation in advanced Parkinson's disease. Neurology. 51:1998;850-855
28. Kumar K., Kelly M., Toth C. Deep brain stimulation of the ventral intermediate nucleus of the thalamus for control of tremors in Parkinson's disease and essential tremor. Stereotact. Funct. Neurosurg. 72:1999;47-61
29. Lanotte M.M., Rizzone M., Bergamasco B., Faccani G., Melcarne A., Lopiano L. Deep brain stimulation of the subthalamic nucleus: anatomical, neurophysiological, and outcome correlations with the effects of stimulation. J. Neurol., Neurosurg. Psychiatry. 72:2002;53-58
30. 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. 21:1993;1130-1132
31. Lindvall O., Brundin P., Widner H., Rehncrona S., Gustavii B., Frackowiak R., Leenders K.L., Sawle G., Rothwell J.C., Marsden C.D., Bjorklund A. Grafts of fetal dopamine neurons survive and improve motor function in Parkinson's disease. Science. 247:1990;574-577
32. Mittoux V., Joseph J.M., Conde F., Palfi S., Dautry C., Poyot T., Bloch J., Deglon N., Ouary S., Nimchinsky E.A., Brouillet E., Hof P.R., Peschanski M., Aebischer P., Hantraye P. Restoration of cognitive and motor functions by ciliary neurotrophic factor in a primate model of Huntington's disease. Hum. Gene Ther. 11:2000;1177-1187
33. Moens K., Heimberg H., Flamez D., Huypens P., Quartier E., Ling Z., Pipeleers D., Gremlich S., Thorens B., Schuit F. Expression and functional activity of glucagon, glucagon-like peptide I, and glucose-dependent insulinotropic peptide receptors in rat pancreatic islet cells. Diabetes. 45:1996;257-261
34. Namavari M., Bishop A., Satyamurthy N., Bida G., Barrio J.R. Regioselective radiofluorodestannylation with [18F]F2 and [18F]CH3COOF: a high yield synthesis of 6-[18F]Fluoro-L-DOPA. Int. J. Appl. Radiat. Isot. 43:1992;989-996
35. Palfi S., Leventhal L., Chu Y., Ma S.Y., Emborg M., Bakay R., Deglon N., Hantraye P., Aebischer P., Kordower J.H. Lentivirally delivered glial cell line-derived neurotrophic factor increases the number of striatal dopaminergic neurons in primate models of nigrostriatal degeneration. J. Neurosci. 22:2002;4942-4954
36. Patlak C.S., Blasberg R.G. Graphical evaluation of blood-to-brain transfer constants from multiple-time uptake data. Generalizations. J. Cereb. Blood Flow Metab. 5:1985;584-590
37. Peschanski M., Defer G., N'Guyen J.P., Ricolfi F., Monfort J.C., Remy P., Geny C., Samson Y., Hantraye P., Jeny R., Gaston A., Keravel Y., Degos J.D., Césaro P. Bilateral motor improvement and alteration of L-dopa effect in two patients with Parkinson's disease following intrastriatal transplantation of foetal ventral mesencephalon. Brain. 117:1994;487-499
38. Pollak P., Fraix V., Krack P., Moro E., Mendes A., Chabardes S., Koudsie A., Benabid A.L. Treatment results: Parkinson's disease. Mov. Disord. 17:2002;S75-S83
39. Porritt M.J., Batchelor P.E., Hughes A.J., Kalnins R., Donnan G.A., Howells D.W. New dopaminergic neurons in Parkinson's disease striatum. Lancet. 356:2000;44-45
40. Remy P., Samson Y., Hantraye P., Fontaine A., Defer G., Mangin J.-F., Fenelon G., Geny C., Ricolfi F., Frouin V., N'guyen J.P., Jeny R., Degos J.D., Peschanski M., Cesaro P. Clinical correlates of (18F)Fluorodopa uptake in five grafted Parkinsonian patients. Ann. Neurol. 38:1995;580-588
41. Riche D., Christolomme A., Bert J., Naquet R. Atlas stéré otaxique du cerveau de babouin. 1968;Editions du Centre National de la Recherche Scientifique, Paris VII, France
42. Rinsch C., Regulier E., Deglon N., Dalle B., Beuzard Y., Aebischer P. A gene therapy approach to regulated delivery of erythropoietin as a function of oxygen tension. Hum. Gene Ther. 8:1997;1881-1889
43. Sautter J., Tseng J.L., Braguglia D., Aebischer P., Spenger C., Seiler R.W., Widmer H.R., Zurn A.D. Implants of polymer-encapsulated genetically modified cells releasing glial cell line-derived neurotrophic factor improve survival, growth, and function of fetal dopaminergic grafts. Exp. Neurol. 149:1998;230-236
44. Shingo T., Date I., Yoshida H., Ohmoto T. Neuroprotective and restorative effects of intrastriatal grafting of encapsulated GDNF-producing cells in a rat model of Parkinson's disease. J. Neurosci. Res. 69:2002;946-954
45. 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. 373:1995;335-339
46. Tseng J.L., Aebischer P. Encapsulated neural transplants. Prog. Brain Res. 127:2000;189-202
47. Varastet M., Riche D., Maziere M., Hantraye P. Chronic MPTP treatment reproduces in baboons the differential vulnerability of mesencephalic dopaminergic neurons observed in Parkinson's disease. Neuroscience. 63:1994;47-56
48. Wang L., Muramatsu S., Lu Y., Ikeguchi K., Fujimoto K., Okada T., Mizukami H., Hanazono Y., Kume A., Urano F., Ichinose H., Nagatsu T., Nakano I., Ozawa K. Delayed delivery of AAV-GDNF prevents nigral neurodegeneration and promotes functional recovery in a rat model of Parkinson's disease. Gene Ther. 9:2002;381-389
49. West M.J., Slomianka L., Gundersen H.J. Unbiased stereological estimation of the total number of neurons in the subdivisions of the rat hippocampus using the optical fractionator. Anat. Rec. 231:1991;482-497
50. West M.J., Ostergaard K., Andreassen O.A., Finsen B. Estimation of the number of somatostatin neurons in the striatum: an in situ hybridization study using the optical fractionator method. J. Comp. Neurol. 70:1996;11-22
51. Wullner U., Pakzaban P., Brownell A.L., Hantraye P., Burns L., Shoup T., Elmaleh D., Petto A.J., Spealman R.D., Brownell G.L., Isacson O. Dopamine terminal loss and onset of motor symptoms in MPTP-treated monkeys: a positron emission tomography study with 11C-CFT. Exp. Neurol. 126:1994;305-309
52. Zurn A.D., Henry H., Schluep M., Aubert V., Winkel L., Eilers B., Bachmann C., Aebischer P. Evaluation of an intrathecal immune response in amyotrophic lateral sclerosis patients implanted with encapsulated genetically engineered xenogeneic cells. Cell Transplant. 9:2000;471-484
53. Zurn A.D., Widmer H.R., Aebischer P. Sustained delivery of GDNF: towards a treatment for Parkinson's disease. Brain Res. Brain Res. Rev. 36:2001;222-229