Enhanced efficacy of the CDNF/MANF family by combined intranigral overexpression in the 6-OHDA rat model of parkinson's disease

Molecular Therapy

Volumn 23, Issue 2, 2015, Pages 244-254

  Cordero Llana, Óscar ^a   Houghton, Benjamin C ^a   Rinaldi, Federica ^a   Taylor, Hannah ^a   Yáñez Muñoz, Rafael J ^b   Uney, James B ^a   Wong, Liang Fong ^a   Caldwell, Maeve A ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CEREBRAL DOPAMINE NEUROTROPHIC FACTOR; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GROWTH FACTOR; LENTIVIRUS VECTOR; MESENCEPHALIC ASTROCYTE DOPAMINE NEUROTROPHIC FACTOR; NEUROTROPHIC FACTOR; UNCLASSIFIED DRUG; CDNF PROTEIN, RAT; HYBRID PROTEIN; MANF PROTEIN, RAT; NERVE GROWTH FACTOR; OXIDOPAMINE; TYROSINE 3 MONOOXYGENASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DENSITY; CELL PROTECTION; CIRCLING BEHAVIOR; CONTROLLED STUDY; DRUG EFFICACY; DRUG POTENTIATION; INTRANIGRAL DRUG ADMINISTRATION; INTRASTRIATAL DRUG ADMINISTRATION; NEUROPROTECTION; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; PARKINSON DISEASE; RAT; SUBSTANTIA NIGRA; ADMINISTRATION AND DOSAGE; ANIMAL; ANIMAL BEHAVIOR; CELL LINE; DISEASE MODEL; GENE EXPRESSION; GENE ORDER; GENE VECTOR; GENETIC TRANSDUCTION; GENETICS; HUMAN; IMMUNOHISTOCHEMISTRY; LENTIVIRINAE; METABOLISM; NERVE CELL; PATHOLOGY;

RATTUS;

ANIMALS; BEHAVIOR, ANIMAL; CELL LINE; DISEASE MODELS, ANIMAL; GENE EXPRESSION; GENE ORDER; GENETIC VECTORS; HUMANS; IMMUNOHISTOCHEMISTRY; LENTIVIRUS; NERVE GROWTH FACTORS; NEURONS; OXIDOPAMINE; PARKINSON DISEASE; RATS; RECOMBINANT FUSION PROTEINS; SUBSTANTIA NIGRA; TRANSDUCTION, GENETIC; TYROSINE 3-MONOOXYGENASE;

EID: 84922221939     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2014.206     Document Type: Article

References (42)

1. Maetzler W, Liepelt I and Berg D. (2009). Progression of Parkinson's disease in the clinical phase: potential markers. Lancet Neurol 8: 1158-1171
2. Evans JR and Barker RA. (2008). Neurotrophic factors as a therapeutic target for Parkinson's disease. Expert Opin Ther Targets 12: 437-447
3. Li H, He, Z, Su, T, Ma Y, Lu, S, Dai C., et al. (2003). Protective action of recombinant neurturin on dopaminergic neurons in substantia nigra in a rhesus monkey model of Parkinson's disease. Neurol Res 25: 263-267
4. Kordower JH, Herzog CD, Dass B, Bakay RA, Stansell J 3rd, Gasmi M., et al. (2006). Delivery of neurturin by AAV2 (CERE-120)-mediated gene transfer provides structural and functional neuroprotection and neurorestoration in MPTP-treated monkeys. Ann Neurol 60: 706-715
5. Gasmi M, Brandon EP, Herzog CD, Wilson A, Bishop KM, Hofer EK., et al. (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
6. Gill SS, Patel NK, Hotton GR, O'Sullivan K, McCarter R, Bunnage M., et al. (2003). Direct brain infusion of glial cell line-derived neurotrophic factor in Parkinson disease. Nat Med 9: 589-595
7. Nutt JG, Burchiel KJ, Comella CL, Jankovic J, Lang AE, Laws ER Jr., et al.; ICV GDNF Study Group. Implanted intracerebroventricular. Glial cell line-derived neurotrophic factor. (2003). Randomized double-blind trial of glial cell line-derived neurotrophic factor (GDNF) in PD. Neurology 60: 69-73
8. Lang AE, Gill S, Patel NK, Lozano A, Nutt JG, Penn R., et al. (2006). Randomized controlled trial of intraputamenal glial cell line-derived neurotrophic factor infusion in Parkinson disease. Ann Neurol 59: 459-466
9. Marks WJ Jr, Bartus RT, Siffert J, Davis CS, Lozano A, Boulis N., et al. (2010). Gene delivery of AAV2-neurturin for Parkinson's disease: a double-blind randomised controlled trial. Lancet Neurol 9: 1164-1172
10. Marks WJ Jr, Ostrem JL, Verhagen L, Starr PA, Larson PS, Bakay RA., et al. (2008). 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 7: 400-408
11. Decressac M, Ulusoy A, Mattsson B, Georgievska B, Romero-Ramos M, Kirik D., et al. (2011). GDNF fails to exert neuroprotection in a rat a-synuclein model of Parkinson's disease. Brain 134(Pt 8): 2302-2311
12. Lo Bianco C, Déglon N, Pralong W and Aebischer P. (2004). Lentiviral nigral delivery of GDNF does not prevent neurodegeneration in a genetic rat model of Parkinson's disease. Neurobiol Dis 17: 283-289
13. Lindholm P, Voutilainen MH, Laurén J, Peränen J, Leppänen VM, Andressoo JO., et al. (2007). Novel neurotrophic factor CDNF protects and rescues midbrain dopamine neurons in vivo. Nature 448: 73-77
14. Petrova P, Raibekas A, Pevsner J, Vigo N, Anafi M, Moore MK., et al. (2003). MANF: a new mesencephalic astrocyte-derived neurotrophic factor with selectivity for dopaminergic neurons. J Mol Neurosci 20: 173-188
15. Lindholm P, Peränen J, Andressoo JO, Kalkkinen N, Kokaia Z, Lindvall O., et al. (2008). MANF is widely expressed in mammalian tissues and differently regulated after ischemic and epileptic insults in rodent brain. Mol Cell Neurosci 39: 356-371
16. Palgi M, Lindström R, Peränen J, Piepponen TP, Saarma M and Heino TI. (2009). Evidence that DmMANF is an invertebrate neurotrophic factor supporting dopaminergic neurons. Proc Natl Acad Sci USA 106: 2429-2434
17. Ren X, Zhang T, Gong X, Hu G, Ding W and Wang X. (2013). AAV2-mediated striatum delivery of human CDNF prevents the deterioration of midbrain dopamine neurons in a 6-hydroxydopamine induced parkinsonian rat model. Exp Neurol 248: 148-156
18. Voutilainen MH, Bäck S, Pörsti E, Toppinen L, Lindgren L, Lindholm P., et al. (2009). Mesencephalic astrocyte-derived neurotrophic factor is neurorestorative in rat model of Parkinson's disease. J Neurosci 29: 9651-9659
19. Airavaara M, Harvey BK, Voutilainen MH, Shen H, Chou J, Lindholm P., et al. (2012). CDNF protects the nigrostriatal dopamine system and promotes recovery after MPTP treatment in mice. Cell Transplant 21: 1213-1223
20. Lundberg C, Björklund T, Carlsson T, Jakobsson J, Hantraye P, Déglon N., et al. (2008). Applications of lentiviral vectors for biology and gene therapy of neurological disorders. Curr Gene Ther 8: 461-473
21. Sun ZP, Gong L, Huang SH, Geng Z, Cheng L and Chen ZY. (2011). Intracellular trafficking and secretion of cerebral dopamine neurotrophic factor in neurosecretory cells. J Neurochem 117: 121-132
22. Kirik D, Rosenblad C and Björklund A. (1998). Characterization of behavioral and neurodegenerative changes following partial lesions of the nigrostriatal dopamine system induced by intrastriatal 6-hydroxydopamine in the rat. Exp Neurol 152: 259-277
23. Voutilainen MH, Bäck S, Peränen J, Lindholm P, Raasmaja A, Männistö PT., et al. (2011). Chronic infusion of CDNF prevents 6-OHDA-induced deficits in a rat model of Parkinson's disease. Exp Neurol 228: 99-108
24. Kirik D, Rosenblad C, Bjorklund A and Mandel RJ. (2000). 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 20: 4686-4700
25. Szymczak AL, Workman CJ, Wang Y, Vignali KM, Dilioglou S, Vanin EF., et al. (2004). Correction of multi-gene deficiency in vivo using a single 'self-cleaving' 2A peptide-based retroviral vector. Nat Biotechnol 22: 589-594
26. Kordower JH and Bjorklund A. (2013). Trophic factor gene therapy for Parkinson's disease. Mov Disord 28: 96-109
27. Airaksinen MS and Saarma M. (2002). The GDNF family: signalling biological functions and therapeutic value. Nat Rev Neurosci 3: 383-394
28. Kirik D, Georgievska B and Björklund A. (2004). Localized striatal delivery of GDNF as a treatment for Parkinson disease. Nat Neurosci 7: 105-110
29. Georgievska B, Kirik D, Rosenblad C, Lundberg C and Björklund A. (2002). Neuroprotection in the rat Parkinson model by intrastriatal GDNF gene transfer using a lentiviral vector. Neuroreport 13: 75-82
30. Bäck S, Peränen J, Galli E, Pulkkila P, Lonka-Nevalaita L, Tamminen T., et al. (2013). Gene therapy with AAV2-CDNF provides functional benefits in a rat model of Parkinson's disease. Brain Behav 3: 75-88
31. Cheng L, Liu Y, Zhao H, Zhang W, Guo YJ and Nie L. (2013). Lentiviralmediated transfer of CDNF promotes nerve regeneration and functional recovery after sciatic nerve injury in adult rats. Biochem Biophys Res Commun 440: 330-335
32. Cheng HC, Ulane CM and Burke RE. (2010). Clinical progression in Parkinson disease and the neurobiology of axons. Ann Neurol 67: 715-725
33. Kim SR, Chen X, Oo, TF, Kareva T, Yarygina O, Wang C., et al. (2011). Dopaminergic pathway reconstruction by Akt/Rheb-induced axon regeneration. Ann Neurol 70: 110-120
34. Lindström R, Lindholm P, Kallijärvi J, Yu, LY, Piepponen TP, Arumäe U., et al. (2013). Characterization of the structural and functional determinants of MANF/CDNF in Drosophila in vivo model. PLoS ONE 8: e73928
35. Yáñez-Muñoz RJ, Balaggan KS, MacNeil A, Howe SJ, Schmidt M, Smith AJ., et al. (2006). Effective gene therapy with nonintegrating lentiviral vectors. Nat Med 12: 348-353
36. Wanisch K and Yáñez-Muñoz RJ. (2009). Integration-deficient lentiviral vectors: a slow coming of age. Mol Ther 17: 1316-1332
37. Lu-Nguyen NB, Broadstock M, Schliesser MG, Bartholomae CC, von Kalle C, Schmidt M., et al. (2014). Transgenic expression of human glial cell line-derived neurotrophic factor from integration-deficient lentiviral vectors is neuroprotective in a rodent model of Parkinson's disease. Hum Gene Ther 25: 631-641
38. Lindholm P and Saarma M. (2010). Novel CDNF/MANF family of neurotrophic factors. Dev Neurobiol 70: 360-371
39. Gonzalez-Aparicio R, Flores JA and Fernandez-Espejo E. (2010). Antiparkinsonian trophic action of glial cell line-derived neurotrophic factor and transforming growth factor ß1 is enhanced after co-infusion in rats. Exp Neurol 226: 136-147
40. Sun M, Kong L, Wang X, Lu, XG, Gao Q and Geller AI. (2005). Comparison of the capability of GDNF BDNF or both to protect nigrostriatal neurons in a rat model of Parkinson's disease. Brain Res 1052: 119-129
41. Mitrophanous K, Yoon S, Rohll J, Patil D, Wilkes F, Kim V., et al. (1999). Stable gene transfer to the nervous system using a non-primate lentiviral vector. Gene Ther 6: 1808-1818
42. Cordero-Llana O, Rinaldi F, Brennan PA, Wynick D and Caldwell MA. (2014). Galanin promotes neuronal differentiation from neural progenitor cells in vitro and contributes to the generation of new olfactory neurons in the adult mouse brain. Exp Neurol 256: 93-104