CDNF Protects the Nigrostriatal Dopamine System and Promotes Recovery After MPTP Treatment in Mice

Cell Transplantation

Volumn 21, Issue 6, 2012, Pages 1213-1223

  Airavaara, Mikko ^a   Harvey, Brandon K ^a   Voutilainen, Merja H ^b   Shen, Hui ^a   Chou, Jenny ^a   Lindholm, Päivi ^c   Lindahl, Maria ^c   Tuominen, Raimo K ^b   Saarma, Mart ^c   Hoffer, Barry ^a   Wang, Yun ^a  

^a NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

^b UNIVERSITY OF HELSINKI   (Finland)

^c UNIVERSITY OF HELSINKI   (Finland)

Author keywords

1 methyl 4 phenyl 1,2,3,6 tetrahydropyridine (MPTP); Cerebral dopamine neurotrophic factor (CDNF); Mesencephalic astrocyte derived neurotrophic factor (MANF); Parkinson's disease

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; CEREBRAL DOPAMINE NEUROTROPHIC FACTOR; NEUROPROTECTIVE AGENT; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL FUNCTION; CELL SURVIVAL; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC NERVE CELL; DOPAMINERGIC SYSTEM; IMMUNOREACTIVITY; LOCOMOTION; MALE; MOUSE; NEUROPROTECTION; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; PRIORITY JOURNAL; SUBSTANTIA NIGRA PARS COMPACTA; SUBSTANTIA NIGRA PARS RETICULATA;

ANIMALS; DISEASE MODELS, ANIMAL; DOPAMINE; MALE; MICE; MICE, INBRED C57BL; MOTOR ACTIVITY; MPTP POISONING; NERVE GROWTH FACTORS; NERVE TISSUE PROTEINS; NEURITES; NEUROPROTECTIVE AGENTS; NUCLEAR PROTEINS; RATS; RATS, WISTAR; SUBSTANTIA NIGRA; TYROSINE 3-MONOOXYGENASE;

ANIMALIA; MUS; PARKINSONIA; RODENTIA;

EID: 84865493751     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368911X600948     Document Type: Article

References (44)

1. Airavaara, M.; Chiocco, M. J.; Howard, D. B.; Zuchowoski, K. L.; Peränen, J.; Liu, C.; Fang, S.; Hoffer, B. J.; Wang, Y.; Harvey, B. J. Widespread cortical expression of MANF by AAV serotype 7: Localization and protection against ischemic brain injury. Exp. Neurol. 225(1):104-113; 2010.
2. Airavaara, M.; Shen, H.; Kuo, C. C.; Peränen, J.; Saarma, M.; Hoffer, B.; Wang, Y. Mesencephalic astrocyte-derived neurotrophic factor reduces ischemic brain injury and promotes behavioral recovery in rats. J. Comp. Neurol. 515(1):116-124; 2009.
3. Anderson, D. W.; Neavin, T.; Smith, J. A.; Schneider, J. S. Neuroprotective effects of pramipexole in young and aged MPTP-treated mice. Brain Res. 905(1-2):44-53; 2001.
4. Apostolou, A.; Shen, Y.; Liang, Y.; Luo, J.; Fang, S. Armet, a UPR-upregulated protein, inhibits cell proliferation and ER stress-induced cell death. Exp. Cell Res. 314(13):2454-2467; 2008.
5. Bespalov, M. M.; Saarma, M. GDNF family receptor complexes are emerging drug targets. Trends Pharmacol. Sci. 28(2):68-74; 2007.
6. Cannon, J. R.; Greenamyre, J. T. NeuN is not a reliable marker of dopamine neurons in rat substantia nigra. Neurosci. Lett. 464(1):14-17; 2009.
7. Chen, Y. H.; Harvey, B. K.; Hoffman, A. F.; Wang, Y.; Chiang, Y. H.; Lupica, C. R. MPTP-induced deficits in striatal synaptic plasticity are prevented by glial cell line-derived neurotrophic factor expressed via an adeno-associated viral vector. FASEB J. 22(1):261-275; 2008.
8. Cheng, F. C.; Ni, D. R.; Wu, M. C.; Kuo, J. S.; Chia, L. G. Glial cell line-derived neurotrophic factor protects against 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-induced neurotoxicity in C57BL/6 mice. Neurosci. Lett. 252(2):87-90; 1998.
9. Chiocco, M. J.; Harvey, B. K.; Wang, Y.; Hoffer, B. J. Neurotrophic factors for the treatment of Parkinson's disease. Parkinsonism Relat. Disord. 13(Suppl. 3):S321-S328; 2007.
10. Chou, J.; Greig, N. H.; Reiner, D.; Hoffer, B. J.; Wang, Y. Enhanced survival of dopaminergic neuronal transplants in hemiparkinsonian rats by the p53 inactivator PFT-α. Cell Transplant. 20(9):1351-1359; 2011.
11. Chou, J.; Luo, Y.; Kuo, C. C.; Powers, K.; Shen, H.; Harvey, B. K.; Hoffer, B. J.; Wang, Y. Bone morphogenetic protein-7 reduces toxicity induced by high doses of methamphetamine in rodents. Neuroscience 151(1):92-103; 2008.
12. Date, I.; Yoshimoto, Y.; Imaoka, T.; Miyoshi, Y.; Gohda, Y.; Furuta, T.; Asari, S.; Ohmoto, T. Enhanced recovery of the nigrostriatal dopaminergic system in MPTP-treated mice following intrastriatal injection of basic fibroblast growth factor in relation to aging. Brain Res. 621(1):150-154; 1993.
13. Eberhardt, O.; Coelln, R. V.; Kugler, S.; Lindenau, J.; Rathke-Hartlieb, S.; Gerhardt, E.; Haid, S.; Isenmann, S.; Gravel, C.; Srinivasan, A.; Bahr, M.; Weller, M.; Dichgans, J.; Schulz, J. B. Protection by synergistic effects of adenovirus-mediated X-chromosome-linked inhibitor of apoptosis and glial cell line-derived neurotrophic factor gene transfer in the 1-methyl-4-phenyl1,2,3,6-tetrahydropyridine model of Parkinson's disease. J. Neurosci. 20(24):9126-9134; 2000.
14. Garrido-Gil, P.; Belzunegui, S.; San Sebastian, W.; Izal-Azcarate, A.; Lopez, B.; Marcilla, I.; Luquin, M. R. 1Methyl-4-phenyl-1,2,3,6-tetrahydropyridine exposure fails to produce delayed degeneration of substantia nigra neurons in monkeys. J. Neurosci. Res. 87(2):586-597; 2009.
15. 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(5):589-595; 2003.
16. Grondin, R.; Zhang, Z.; Ai, Y.; Ding, F.; Walton, A. A.; Surgener, S. P.; Gerhardt, G. A.; Gash, D. M. Intraputamenal infusion of exogenous neurturin protein restores motor and dopaminergic function in the globus pallidus of MPTP-lesioned rhesus monkeys. Cell Transplant. 17(4): 373-381; 2008.
17. Heikkilä, R. E.; Hess, A.; Duvoisin, R. C. Dopaminergic neurotoxicity of 1-methyl-4-phenyl-1,2,5,6-tetrahydropyridine in mice. Science 224(4656):1451-1453; 1984.
18. Hellman, M.; Arumäe, U.; Yu, L. Y.; Lindholm, P.; Peränen, J.; Saarma, M.; Permi, P. Mesencephalic astrocyte-derived neurotrophic factor (MANF) has a unique mechanism to rescue apoptotic neurons. J. Biol. Chem. 286(4):2675-2680; 2011.
19. 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. 182(1):107-111; 1994.
20. Hsu, Y. C.; Lee, D. C.; Chiu, I. M. Neural stem cells, neural progenitors, and neurotrophic factors. Cell Transplant. 16(2):133-150; 2007.
21. Jackson-Lewis, V.; Jakowec, M.; Burke, R. E.; Przedborski, S. Time course and morphology of dopaminergic neuronal death caused by the neurotoxin 1-methyl-4-phenyl1,2,3,6-tetrahydropyridine. Neurodegeneration 4(3):257-269; 1995.
22. Jackson-Lewis, V.; Przedborski, S. Protocol for the MPTP mouse model of Parkinson's disease. Nat. Protoc. 2(1): 141-151; 2007.
23. Kojima, H.; Abiru, Y.; Sakajiri, K.; Watabe, K.; Ohishi, N.; Takamori, M.; Hatanaka, H.; Yagi, K. Adenovirus-mediated transduction with human glial cell line-derived neurotrophic factor gene prevents 1-methyl-4-phenyl1,2,3,6-tetrahydropyridine-induced dopamine depletion in striatum of mouse brain. Biochem. Biophys. Res. Commun. 238(2):569-573; 1997.
24. Kowsky, S.; Poppelmeyer, C.; Kramer, E. R.; Falkenburger, B. H.; Kruse, A.; Klein, R.; Schulz, J. B. RET signaling does not modulate MPTP toxicity but is required for regeneration of dopaminergic axon terminals. Proc. Natl. Acad. Sci. USA 104(50):20049-20054; 2007.
25. Krasnova, I. N.; Bychkov, E. R.; Lioudyno, V. I.; Zubareva, O. E.; Dambinova, S. A. Intracerebroventricular administration of substance P increases dopamine content in the brain of 6-hydroxydopamine-lesioned rats. Neuroscience 95(1):113-117; 2000.
26. 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. 59(3):459-466; 2006.
27. Lee, A. H.; Iwakoshi, N. N.; Glimcher, L. H. XBP-1 regulates a subset of endoplasmic reticulum resident chaperone genes in the unfolded protein response. Mol. Cell. Biol. 23(21):7448-7459; 2003.
28. Leenders, K. L.; Salmon, E. P.; Tyrrell, P.; Perani, D.; Brooks, D. J.; Sager, H.; Jones, T.; Marsden, C. D.; Frackowiak, R. S. The nigrostriatal dopaminergic system assessed in vivo by positron emission tomography in healthy volunteer subjects and patients with Parkinson's disease. Arch. Neurol. 47(12):1290-1298; 1990.
29. Lim, S. T.; Airavaara, M.; Harvey, B. K. Viral vectors for neurotrophic factor delivery: A gene therapy approach for neurodegenerative diseases of the CNS. Pharmacol. Res. 61(1):14-26; 2010.
30. Lindholm, P.; Peränen, J.; Andressoo, J. O.; Kalkkinen, N.; Kokaia, Z.; Lindvall, O.; Timmusk, T.; Saarma, M. MANF is widely expressed in mammalian tissues and differently regulated after ischemic and epileptic insults in rodent brain. Mol. Cell. Neurosci. 39(3):356-371; 2008.
31. Lindholm, P.; Voutilainen, M. H.; Laurén, J.; Peränen, J.; Leppänen, V. M.; Andressoo, J. O.; Lindahl, M.; Janhunen, S.; Kalkkinen, N.; Timmusk, T. Tuominen, R. K.; Saarma, M. Novel neurotrophic factor CDNF protects and rescues midbrain dopamine neurons in vivo. Nature 448(7149): 73-77; 2007.
32. Mizobuchi, N.; Hoseki, J.; Kubota, H.; Toyokuni, S.; Nozaki, J.; Naitoh, M.; Koizumi, A.; Nagata, K. ARMET is a soluble ER protein induced by the unfolded protein response via ERSE-II element. Cell Struct. Funct. 32(1): 41-50; 2007.
33. Palgi, M.; Lindström, R.; Peränen, J.; Piepponen, T. P.; Saarma, M.; Heino, T. I. Evidence that DmMANF is an invertebrate neurotrophic factor supporting dopaminergic neurons. Proc. Natl. Acad. Sci. USA 106(7):2429-2434; 2009.
34. Parkash, V.; Lindholm, P.; Peränen, J.; Kalkkinen, N.; Oksanen, E.; Saarma, M.; Leppanen, V. M.; Goldman, A. The structure of the conserved neurotrophic factors MANF and CDNF explains why they are bifunctional. Protein Eng. Des. Sel. 22(4):233-241; 2009.
35. Petroske, E.; Meredith, G. E.; Callen, S.; Totterdell, S.; Lau, Y. S. Mouse model of parkinsonism: A comparison between subacute MPTP and chronic MPTP/probenecid treatment. Neuroscience 106(3):589-601; 2001.
36. Petrova, P.; Raibekas, A.; Pevsner, J.; Vigo, N.; Anafi, M.; Moore, M. K.; Peaire, A. E.; Shridhar, V.; Smith, D. I.; Kelly, J.; Durocher, Y.; Commissiong, J. W. MANF: A new mesencephalic, astrocyte-derived neurotrophic factor with selectivity for dopaminergic neurons. J. Mol. Neurosci. 20(2):173-188; 2003.
37. Ricaurte, G. A.; Langston, J. W.; Delanney, L. E.; Irwin, I.; Peroutka, S. J.; Forno, L. S. Fate of nigrostriatal neurons in young mature mice given 1-methyl-4-phenyl1,2,3,6-tetrahydropyridine: A neurochemical and morphological reassessment. Brain Res. 376(1):117-124; 1986.
38. 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. 102(2):216-222; 2005.
39. Soderstrom, K.; O'Malley, J.; Steece-Collier, K.; Kordower, J. H. Neural repair strategies for Parkinson's disease: Insights from primate models. Cell Transplant. 15(3):251-265; 2006.
40. Sundström, E.; Stromberg, I.; Tsutsumi, T.; Olson, L.; Jönsson, G. Studies on the effect of 1-methyl-4-phenyl1,2,3,6-tetrahydropyridine (MPTP) on central catecholamine neurons in C57BL/6 mice. Comparison with three other strains of mice. Brain Res. 405(1):26-38; 1987.
41. Tadimalla, A.; Belmont, P. J.; Thuerauf, D. J.; Glassy, M. S.; Martindale, J. J.; Gude, N.; Sussman, M. A.; Glembotski, C. C. Mesencephalic astrocyte-derived neurotrophic factor is an ischemia-inducible secreted endoplasmic reticulum stress response protein in the heart. Circ. Res. 103(11): 1249-1258; 2008.
42. 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(6512):335-339; 1995.
43. Voutilainen, M. H.; Bäck, S.; Peränen, J.; Lindholm, P.; Raasmaja, A.; Männisto, P. T.; Saarma, M.; Tuominen, R. K. Chronic infusion of CDNF prevents 6-OHDAinduced deficits in a rat model of Parkinson's disease. Exp. Neurol. 228(1):99-108; 2011.
44. Voutilainen, M. H.; Bäck, S.; Pörsti, E.; Toppinen, L.; Lindgren, L.; Lindholm, P.; Peranen, J.; Saarma, M.; Tuominen, R. K. Mesencephalic astrocyte-derived neurotrophic factor is neurorestorative in rat model of Parkinson's disease. J. Neurosci. 29(30):9651-9659; 2009.