Stem cell grafting improves both motor and cognitive impairments in a genetic model of parkinson'S disease, the aphakia (ak) mouse

Cell Transplantation

Volumn 22, Issue 7, 2013, Pages 1263-1279

  Moon, Jisook ^a,b   Lee, Hyun Seob ^b   Kang, Jun Mo ^b   Park, Junpil ^a   Leung, Amanda ^a   Hong, Sunghoi ^a,c   Chung, Sangmi ^a   Kim, Kwang Soo ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

^b CHA University   (South Korea)

^c Korea University   (South Korea)

Author keywords

4 dihydroxyphenylalanine (L DOPA); 6 hydroxydopamine (6 OHDA); Aphakia (ak) mouse; Dopaminergic neurons; Embryonic stem cells (ESCS); L 3; Parkinson's disease (PD); Tyrosine hydroxylase (TH)

Indexed keywords

TYROSINE 3 MONOOXYGENASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APHAKIA; ARTICLE; BASAL GANGLION; CELL DIFFERENTIATION; COGNITIVE DEFECT; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; EMBRYOID BODY; FUNCTIONAL STATUS; IN VITRO STUDY; MOTOR DYSFUNCTION; MOUSE; NEURAL STEM CELL; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; STEM CELL TRANSPLANTATION; SURVIVAL; TREATMENT RESPONSE;

ANIMALS; APHAKIA; CELL DIFFERENTIATION; COGNITION; DISEASE MODELS, ANIMAL; DOPAMINE; DOPAMINERGIC NEURONS; EMBRYONIC STEM CELLS; MESENCEPHALON; MICE; MODELS, GENETIC; MOTOR ACTIVITY; NEURAL STEM CELLS; PARKINSON DISEASE; TERATOMA; TYROSINE 3-MONOOXYGENASE;

ANIMALIA; MUS;

EID: 84879585928     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368912X657242     Document Type: Article

References (57)

1. Agid, Y.; Ruberg, M.; Dubois, B.; Pillon, B.; Cusimano, G.; Raisman, R.; Cash, R.; Lhermitte, F.; Javoy-Agid, F. Parkinson's disease and dementia. Clin. Neuropharmacol. 9 Suppl 2:S22-S36; 1986.
2. Ardayfio, P.; Moon, J.; Leung, K. K.; Youn-Hwang, D.; Kim, K. S. Impaired learning and memory in Pitx3 deficient aphakia mice: A genetic model for striatum-dependent cognitive symptoms in Parkinson'S disease. Neurobiol. Dis. 31(3):406-412; 2008.
3. Barberi, T.; Klivenyi, P.; Calingasan, N. Y.; Lee, H.; Kawamata, H.; Loonam, K.; Perrier, A. L.; Bruses, J.; Rubio, M. E.; Topf, N.; Tabar, V.; Harrison, N. L.; Beal, M. F.; Moore, M. A.; Studer, L. Neural subtype specification of fertilization and nuclear transfer embryonic stem cells and application in parkinsonian mice. Nat. Biotechnol. 21(10):1200-1207; 2003.
4. Beal, M. F. Experimental models of Parkinson'S disease. Nat. Rev. Neurosci. 2(5):325-334; 2001.
5. Beal, M. F. Parkinson'S disease: A model dilemma. Nature 466(7310):S8-S10; 2010.
6. Ben-Hur, T.; Idelson, M.; Khaner, H.; Pera, M.; Reinhartz, E.; Itzik, A.; Reubinoff, B. E. Transplantation of human embryonic stem cell-derived neural progenitors improves behavioral deficit in Parkinsonian rats. Stem Cells 22(7): 1246-1255; 2004.
7. Betarbet, R.; Sherer, T. B.; Greenamyre, J. T. Animal models of Parkinson'S disease. Bioessays 24(4):308-318; 2002.
8. Bjorklund, L. M.; Sanchez-Pernaute, R.; Chung, S.; Andersson, T.; Chen, I. Y.; McNaught, K. S.; Brownell, A. L.; Jenkins, B. G.; Wahlestedt, C.; Kim, K. S.; Isacson, O. Embryonic stem cells develop into functional dopaminergic neurons after transplantation in a Parkinson rat model. Proc. Natl. Acad. Sci. USA 99(4):2344-2349; 2002.
9. Blandini, F.; Cova, L.; Armentero, M. T.; Zennaro, E.; Levandis, G.; Bossolasco, P.; Calzarossa, C.; Mellone, M.; Giuseppe, B.; Deliliers, G. L.; Polli, E.; Nappi, G.; Silani, V. Transplantation of undifferentiated human mesenchymal stem cells protects against 6-hydroxydopamine neurotoxicity in the rat. Cell Transplant. 19(2):203-217; 2010.
10. Bosboom, J. L.; Stoffers, D.; Wolters, E. Cognitive dysfunction and dementia in Parkinson'S disease. J. Neural. Transm. 111(10-11):1303-1315; 2004.
11. Brederlau, A.; Correia, A. S.; Anisimov, S. V.; Elmi, M.; Paul, G.; Roybon, L.; Morizane, A.; Bergquist, F.; Riebe, I.; Nannmark, U.; Carta, M.; Hanse, E.; Takahashi, J.; Sasai, Y.; Funa, K.; Brundin, P.; Eriksson, P. S.; Li, J. Y. Transplantation of human embryonic stem cell-derived cells to a rat model of Parkinson'S disease: Effect of in vitro differentiation on graft survival and teratoma formation. Stem Cells 24(6):1433-1440; 2006.
12. Bronnick, K.; Aarsland, D.; Larsen, J. P. Neuropsychiatric disturbances in Parkinson'S disease clusters in five groups with different prevalence of dementia. Acta. Psychiatr. Scand. 112(3):201-207; 2005.
13. Chang, J. H.; Choi, J. Y.; Chang, J. W.; Park, Y. G.; Kim, T. S.; Chung, S. S. Chronic epidural hematoma with rapid ossification. Childs Nerv. Syst. 18(12):712-716; 2002.
14. Cho, M. S.; Lee, Y. E.; Kim, J. Y.; Chung, S.; Cho, Y. H.; Kim, D. S.; Kang, S. M.; Lee, H.; Kim, M. H.; Kim, J. H.; Leem, J. W.; Oh, S. K.; Choi, Y. M.; Hwang, D. Y.; Chang, J. W.; Kim, D. W. Highly efficient and large-scale generation of functional dopamine neurons from human embryonic stem cells. Proc. Natl. Acad. Sci. U S A 105(9):3392-3397; 2008.
15. Chung, S.; Shin, B. S.; Hedlund, E.; Pruszak, J.; Ferree, A.; Kang, U. J.; Isacson, O.; Kim, K. S. Genetic selection of sox1GFP-expressing neural precursors removes residual tumorigenic pluripotent stem cells and attenuates tumor formation after transplantation. J. Neurochem. 97(5):1467-1480; 2006.
16. Chung, S.; Shin, B. S.; Hwang, M.; Lardaro, T.; Kang, U. J.; Isacson, O.; Kim, K. S. Neural precursors derived from embryonic stem cells, but not those from fetal ventral mesencephalon, maintain the potential to differentiate into dopaminergic neurons after expansion in vitro. Stem Cells 24(6):1583-1593; 2006.
17. Chung, S.; Sonntag, K. C.; Andersson, T.; Bjorklund, L. M.; Park, J. J.; Kim, D. W.; Kang, U. J.; Isacson, O.; Kim, K. S. Genetic engineering of mouse embryonic stem cells by Nurr1 enhances differentiation and maturation into dopaminergic neurons. Eur. J. Neurosci. 16(10):1829-1838; 2002.
18. Dauer, W.; Przedborski, S. Parkinson'S disease: Mechanisms and models. Neuron 39(6):889-909; 2003.
19. Dyer, R. S.; Hammond, M. A.; Weldon, D. A.; Booker, T. C. Influence of enucleation upon two-way avoidance behavior of rats, hamsters, chinchillas and BALB/cJ mice. Physiol. Behav. 14(2):211-216; 1975.
20. Erdo, F.; Buhrle, C.; Blunk, J.; Hoehn, M.; Xia, Y.; Fleischmann, B.; Focking, M.; Kustermann, E.; Kolossov, E.; Hescheler, J.; Hossmann, K. A.; Trapp, T. Host-dependent tumorigenesis of embryonic stem cell transplantation in experimental stroke. J. Cereb. Blood Flow Metab. 23(7): 780-785; 2003.
21. Evans, M. J.; Kaufman, M. H. Establishment in culture of pluripotential cells from mouse embryos. Nature 292 (5819):154-156; 1981.
22. Farr, S. A.; Banks, W. A.; La Scola, M. E.; Morley, J. E. Blind mice are not impaired in T-maze footshock avoidance acquisition and retention. Physiol. Behav. 76(4-5):531-538; 2002.
23. Fleming, S. M.; Fernagut, P. O.; Chesselet, M. F. Genetic mouse models of parkinsonism: Strengths and limitations. NeuroRx. 2(3):495-503; 2005.
24. Fleming, S. M.; Salcedo, J.; Fernagut, P. O.; Rockenstein, E.; Masliah, E.; Levine, M. S.; Chesselet, M. F. Early and progressive sensorimotor anomalies in mice overexpressing wild-type human a-synuclein. J. Neurosci. 24(42):9434- 9440; 2004.
25. Franklin, K. B. J.; Paxinos, G. The Mouse brain in stereotaxic coordinates, 3rd ed. New York, NY: Academic Press/ Elsevier; 2008.
26. 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(10):710-719; 2001.
27. Hagell, P.; Schrag, A.; Piccini, P.; Jahanshahi, M.; Brown, R.; Rehncrona, S.; Widner, H.; Brundin, P.; Rothwell, J. C.; Odin, P.; Wenning, G. K.; Morrish, P.; Gustavii, B.; Bjorklund, A.; Brooks, D. J.; Marsden, C. D.; Quinn, N. P.; Lindvall, O. Sequential bilateral transplantation in Parkinson'S disease: Effects of the second graft. Brain 122(Pt 6):1121-1132; 1999.
28. Hedlund, E.; Pruszak, J.; Ferree, A.; Vinuela, A.; Hong, S.; Isacson, O.; Kim, K. S. Selection of embryonic stem cell-derived enhanced green fluorescent protein-positive dopamine neurons using the tyrosine hydroxylase promoter is confounded by reporter gene expression in immature cell populations. Stem Cells 25(5):1126-1135; 2007.
29. Hedlund, E.; Pruszak, J.; Lardaro, T.; Ludwig, W.; Vinuela, A.; Kim, K. S.; Isacson, O. Embryonic stem cell-derived Pitx3- enhanced green fluorescent protein midbrain dopamine neurons survive enrichment by fluorescence-activated cell sorting and function in an animal model of Parkinson'S disease. Stem Cells 26(6):1526-1536; 2008.
30. Hwang, D. Y.; Ardayfio, P.; Kang, U. J.; Semina, E. V.; Kim, K. S. Selective loss of dopaminergic neurons in the substantia nigra of Pitx3-deficient aphakia mice. Brain Res. Mol. Brain Res. 114(2):123-131; 2003.
31. Hwang, D. Y.; Fleming, S. M.; Ardayfio, P.; Moran-Gates, T.; Kim, H.; Tarazi, F. I.; Chesselet, M. F.; Kim, K. S. 3,4- dihydroxyphenylalanine reverses the motor deficits in Pitx3-deficient aphakia mice: Behavioral characterization of a novel genetic model of Parkinson'S disease. J. Neurosci. 25(8):2132-2137; 2005.
32. Kim, D. W.; Chung, S.; Hwang, M.; Ferree, A.; Tsai, H. C.; Park, J. J.; Chung, S.; Nam, T. S.; Kang, U. J.; Isacson, O.; Kim, K. S. Stromal cell-derived inducing activity, Nurr1, and signaling molecules synergistically induce dopaminergic neurons from mouse embryonic stem cells. Stem Cells 24(3):557-567; 2006.
33. Kim, J. H.; Auerbach, J. M.; Rodriguez-Gomez, J. A.; Velasco, I.; Gavin, D.; Lumelsky, N.; Lee, S. H.; Nguyen, J.; Sanchez-Pernaute, R.; Bankiewicz, K.; McKay, R. Dopamine neurons derived from embryonic stem cells function in an animal model of Parkinson'S disease. Nature 418(6893):50-56; 2002.
34. Lang, A. E.; Lozano, A. M. Parkinson'S disease. First of two parts. N. Engl. J. Med. 339(15):1044-1053; 1998.
35. Lang, A. E.; Lozano, A. M. Parkinson'S disease. Second of two parts. N. Engl. J. Med. 339(16):1130-1143; 1998.
36. Lee, S. H.; Lumelsky, N.; Studer, L.; Auerbach, J. M.; McKay, R. D. Efficient generation of midbrain and hindbrain neurons from mouse embryonic stem cells. Nat. Biotechnol. 18(6):675-679; 2000.
37. Lindvall, O.; Kokaia, Z. Prospects of stem cell therapy for replacing dopamine neurons in Parkinson'S disease. Trends Pharmacol. Sci. 30(5):260-267; 2009.
38. Lindvall, O.; Kokaia, Z. Stem cells for the treatment of neurological disorders. Nature 441(7097):1094-1096; 2006.
39. Martin, G. R. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc. Natl. Acad. Sci. USA 78(12):7634-7638; 1981.
40. Meredith, G. E.; Kang, U. J. Behavioral models of Parkinson'S disease in rodents: A new look at an old problem. Mov. Disord. 21(10):1595-1606; 2006.
41. Morizane, A.; Takahashi, J.; Shinoyama, M.; Ideguchi, M.; Takagi, Y.; Fukuda, H.; Koyanagi, M.; Sasai, Y.; Hashimoto, N. Generation of graftable dopaminergic neuron progenitors from mouse ES cells by a combination of coculture and neurosphere methods. J. Neurosci. Res. 83(6):1015-1027; 2006.
42. Nikkhah, G.; Rosenthal, C.; Falkenstein, G.; Roedter, A.; Papazoglou, A.; Brandis, A. Microtransplantation of dopaminergic cell suspensions: Further characterization and optimization of grafting parameters. Cell Transplant. 18(2): 119-133; 2009.
43. Nunes, I.; Tovmasian, L.T.; Silva, R. M.; Burke, R. E.; Goff, S. P. Pitx3 is required for development of substantia nigra dopaminergic neurons. Proc. Natl. Acad. Sci. USA 100(7):4245-4250; 2003.
44. Okabe, S.; Forsberg-Nilsson, K.; Spiro, A. C.; Segal, M.; McKay, R. D. Development of neuronal precursor cells and functional postmitotic neurons from embryonic stem cells in vitro. Mech. Dev. 59(1):89-102; 1996.
45. Olanow, C. W.; Goetz, C. G.; Kordower, J. H.; Stoessl, A. J.; Sossi, V.; Brin, M. F.; Shannon, K. M.; Nauert, G. M.; Perl, D. P.; Godbold, J.; Freeman, T. B. A double-blind controlled trial of bilateral fetal nigral transplantation in Parkinson'S disease. Ann. Neurol. 54(3):403-414; 2003.
46. Ono, Y.; Nakatani, T.; Sakamoto, Y.; Mizuhara, E.; Minaki, Y.; Kumai, M.; Hamaguchi, A.; Nishimura, M.; Inoue, Y.; Hayashi, H.; Takahashi, J.; Imai, T. Differences in neurogenic potential in floor plate cells along an anteroposterior location: Midbrain dopaminergic neurons originate from mesencephalic floor plate cells. Development 134(17):3213-3225; 2007.
47. Piccini, P.; Brooks, D. J.; Bjorklund, A.; Gunn, R. N.; Grasby, P. M.; Rimoldi, O.; Brundin, P.; Hagell, P.; Rehncrona, S.; Widner, H.; Lindvall, O. Dopamine release from nigral transplants visualized in vivo in a Parkinson'S patient. Nat. Neurosci. 2(12):1137-1140; 1999.
48. Rodriguez-Gomez, J. A.; Lu, J. Q.; Velasco, I.; Rivera, S.; Zoghbi, S. S.; Liow, J. S.; Musachio, J. L.; Chin, F. T.; Toyama, H.; Seidel, J.; Green, M. V.; Thanos, P. K.; Ichise, M.; Pike, V. W.; Innis, R. B.; McKay, R. D. Persistent dopamine functions of neurons derived from embryonic stem cells in a rodent model of Parkinson disease. Stem Cells 25(4):918-928; 2007.
49. Roy, N. S.; Cleren, C.; Singh, S. K.; Yang, L.; Beal, M. F.; Goldman, S. A. Functional engraftment of human ES cell-derived dopaminergic neurons enriched by coculture with telomerase-immortalized midbrain astrocytes. Nat. Med. 12(11):1259-1268; 2006.
50. Sedelis, M.; Schwarting, R. K.; Huston, J. P. Behavioral phenotyping of the MPTP mouse model of Parkinson'S disease. Behav. Brain Res. 125(1-2):109-125; 2001.
51. Siddique, J.; Belin, T. R. Using an approximate bayesian bootstrap to multiply impute nonignorable missing data. Comput. Stat. Data Anal. 53(2):405-415; 2008.
52. Smidt, M. P.; Smits, S. M.; Bouwmeester, H.; Hamers, F. P.; van der Linden, A. J.; Hellemons, A. J.; Graw, J.; Burbach, J. P. Early developmental failure of substantia nigra dopamine neurons in mice lacking the homeodomain gene Pitx3. Development 131(5):1145-1155; 2004.
53. Thomson, J. A.; Itskovitz-Eldor, J.; Shapiro, S. S.; Waknitz, M. A.; Swiergiel, J. J.; Marshall, V. S.; Jones, J. M. Embryonic stem cell lines derived from human blastocysts. Science 282(5391):1145-1147; 1998.
54. van den Munckhof, P.; Luk, K. C.; Ste-Marie, L.; Montgomery, J.; Blanchet, P. J.; Sadikot, A. F.; Drouin, J. Pitx3 is required for motor activity and for survival of a subset of midbrain dopaminergic neurons. Development 130(11):2535-2542; 2003.
55. Wolfinger, R.; O'Connell, M. Generalized linear mixed models: A pseudo-likelihood approach. J. Stat. Comput. Simul. 48:233-243; 1993.
56. Yi, S. H.; Jo, A. Y.; Park, C. H.; Koh, H. C.; Park, R. H.; Suh-Kim, H.; Shin, I.; Lee, Y. S.; Kim, J.; Lee, S. H. Mash1 and neurogenin 2 enhance survival and differentiation of neural precursor cells after transplantation to rat brains via distinct modes of action. Mol. Ther. 16(11):1873-1882; 2008.
57. Zgaljardic, D. J.; Foldi, N. S.; Borod, J. C. Cognitive and behavioral dysfunction in Parkinson'S disease: Neurochemical and clinicopathological contributions. J. Neural. Transm. 111(10-11):1287-1301; 2004.