Docosahexaenoic acid promotes dopaminergic differentiation in induced pluripotent stem cells and inhibits teratoma formation in rats with Parkinson-like pathology

Cell Transplantation

Volumn 21, Issue 1, 2012, Pages 313-332

  Chang, Yuh Lih ^a,b   Chen, Shih Jen ^a,b   Kao, Chung Lan ^a,b   Hung, Shih Chieh ^a,b   Ding, Dah Ching ^a,c   Yu, Cheng Chia ^a,d   Chen, Yi Jen ^a,b   Ku, Hung Hai ^a   Lin, Chin Po ^a   Lee, Kun Hsiung ^e   Chen, Yu Chih ^a,b   Wang, Jhi Joung ^f   Hsu, Chuan Chih ^f   Chen, Liang Kung ^a,b   Li, Hsin Yang ^a,b   Chiou, Shih Hwa ^a,b  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b TAIPEI VETERANS GENERAL HOSPITAL   (Taiwan)

^c BUDDHIST TZU CHI GENERAL HOSPITAL   (Taiwan)

^d CHUNG SHAN MEDICAL UNIVERSITY   (Taiwan)

^e ANIMAL TECHNOLOGY INSTITUTE TAIWAN   (Taiwan)

^f CHI MEI MEDICAL CENTER   (Taiwan)

Author keywords

3T MRI; Docosahexaenoic acid (DHA); Dopamine; Dopaminergic neurons; Induced pluripotent stem cells (iPS); Parkinson's disease

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; BRAIN DERIVED NEUROTROPHIC FACTOR; DOCOSAHEXAENOIC ACID; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GREEN FLUORESCENT PROTEIN; HETERODIMER; MESSENGER RNA; NUCLEAR RECEPTOR RELATED FACTOR 1; OCTAMER TRANSCRIPTION FACTOR 4; OXIDOPAMINE; PROTEIN BCL 2; PROTEIN BCL XL; RETINOID X RECEPTOR; TYROSINE 3 MONOOXYGENASE;

ANIMAL CELL; ANIMAL EXPERIMENT; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DOPAMINE RELEASE; DOPAMINERGIC NERVE CELL; DOWN REGULATION; EMBRYO; EMBRYONIC STEM CELL; EX VIVO STUDY; GENE EXPRESSION REGULATION; GENE FUNCTION; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NEUROPROTECTION; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEOTIDE SEQUENCE; ONCOGENE C MYC; PARKINSON DISEASE; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; RAT; TERATOMA; UPREGULATION;

1-METHYL-4-PHENYL-1,2,3,6-TETRAHYDROPYRIDINE; ANIMALS; APOPTOSIS; CELLS, CULTURED; DOCOSAHEXAENOIC ACIDS; DOPAMINE; DOPAMINERGIC NEURONS; GENE EXPRESSION REGULATION; INDUCED PLURIPOTENT STEM CELLS; MICE; MICE, INBRED C57BL; NEUROGENESIS; NUCLEAR RECEPTOR SUBFAMILY 4, GROUP A, MEMBER 2; OXIDOPAMINE; PARKINSONIAN DISORDERS; RATS; RATS, SPRAGUE-DAWLEY; RNA, MESSENGER; STEM CELL TRANSPLANTATION; TERATOMA; TYROSINE 3-MONOOXYGENASE;

ANIMALIA; IPS; RATTUS;

EID: 84863229446     PISSN: 09636897     EISSN: None     Source Type: Journal    
DOI: 10.3727/096368911X580572     Document Type: Article

References (55)

1. Arenas, E. Stem cells in the treatment of Parkinson's disease. Brain Res. Bull. 57(6):795-808; 2002.
2. Bjorklund, A.; Dunnett, S. B.; Brundin, P.; Stoessl, A. J.; Freed, C. R.; Breeze, R. E.; Levivier, M.; Peschanski, M.; Studer, L.; Barker, R. Neural transplantation for the treatment of Parkinson's disease. Lancet Neurol. 2(7):437-445; 2003.
3. 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.
4. 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 cellderived 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.
5. Calon, F.; Lim, G. P.; Yang, F.; Morihara, T.; Teter, B.; Ubeda, O.; Rostaing, P.; Triller, A.; Salem, Jr., N.; Ashe, K. H.; Frautschy, S. A.; Cole, G. M. Docosahexaenoic acid protects from dendritic pathology in an Alzheimer's disease mouse model. Neuron 43(5):633-645; 2004.
6. Carvey, P. M.; Punati, A.; Newman, M. B. Progressive dopamine neuron loss in Parkinson's disease: The multiple hit hypothesis. Cell Transplant. 15(3):239-250; 2006.
7. Castillo, S. O.; Baffi, J. S.; Palkovits, M.; Goldstein, D. S.; Kopin, I. J.; Witta, J.; Magnuson, M. A.; Nikodem, V. M. Dopamine biosynthesis is selectively abolished in substantia nigra/ventral tegmental area but not in hypothalamic neurons in mice with targeted disruption of the Nurrl gene. Mol. Cell. Neurosci. 11(1-2):36-46; 1998.
8. Cenci, M. A. Transcription factors involved in the pathogenesis of L-DOPA-induced dyskinesia in a rat model of Parkinson's disease. Amino Acids 23(1-3): 105-109; 2002.
9. Chen, S. J.; Chang, C. M.; Tsai, S. K.; Chang, Y. L.; Chou, S. J.; Huang, S. S.; Tai, L. K.; Chen, Y. C.; Ku, H. H.; Li, H. Y.; Chiou, S. H. Functional improvement of focal cerebral ischemia injury by subdural transplantation of induced pluripotent stem cells with fibrin glue. Stem Cells Dev. 19(11):1757-1767; 2010.
10. Chiou, S. H.; Kao, C. L.; Chang, Y. L.; Ku, H. H.; Tsai, Y. J.; Lin, H. T.; Yen, C. J.; Peng, C. H.; Chiu, J. H.; Tsai, T. H. Evaluation of anti-Fas ligand-induced apoptosis and neural differentiation of PC12 cells treated with nerve growth factor using small interfering RNA method and sampling by microdialysis. Anal. Biochem. 363(1):46-57; 2007.
11. Cui, Y. F.; Hargus, G.; Xu, J. C.; Schmid, J. S.; Shen, Y. Q.; Glatzel, M.; Schachner, M.; Bernreuther, C. Embryonic stem cell-derived L1 overexpressing neural aggregates enhance recovery in Parkinsonian mice. Brain 133(Pt. 1):189-204; 2010.
12. da Conceicao, F. S.; Ngo-Abdalla, S.; Houzel, J. C.; Rehen, S. K. Murine model for Parkinson's disease: From 6-OH dopamine lesion to behavioral test. J. Vis. Exp. 35: 1376; 2010.
13. Da Cunha, C.; Wietzikoski, E. C.; Ferro, M. M.; Martinez, G. R.; Vital, M. A.; Hipolide, D.; Tufik, S.; Canteras, N. S. Hemiparkinsonian rats rotate toward the side with the weaker dopaminergic neurotransmission. Behav. Brain Res. 189(2):364-372; 2008.
14. Deacon, T.; Schumacher, J.; Dinsmore, J.; Thomas, C.; Palmer, P.; Kott, S.; Edge, A.; Penney, D.; Kassissieh, S.; Dempsey, P.; Isacson, O. Histological evidence of fetal pig neural cell survival after transplantation into a patient with Parkinson's disease. Nat. Med. 3(3):350-353; 1997.
15. de la Presa Owens, S.; Innis, S. M. Docosahexaenoic and arachidonic acid prevent a decrease in dopaminergic and serotoninergic neurotransmitters in frontal cortex caused by a linoleic and alpha-linolenic acid deficient diet in formula-fed piglets. J. Nutr. 129(11):2088-2093; 1999.
16. Dyall, S. C.; Michael, G. J.; Michael-Titus, A. T. Omega3 fatty acids reverse age-related decreases in nuclear receptors and increase neurogenesis in old rats. J. Neurosci. Res. 88(10):2091-2102; 2010.
17. 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.
18. Glavaski-Joksimovic, A.; Virag, T.; Chang, Q. A.; West, N. C.; Mangatu, T. A.; McGrogan, M. P.; DugichDjordjevic, M.; Bohn, M. C. Reversal of dopaminergic degeneration in a parkinsonian rat following micrografting of human bone marrow-derived neural progenitors. Cell Transplant. 18(7):801-814; 2009.
19. Hashimoto, M.; Hossain, S.; Shimada, T.; Sugioka, K.; Yamasaki, H.; Fujii, Y.; Ishibashi, Y.; Oka, J.; Shido, O. Docosahexaenoic acid provides protection from impairment of learning ability in Alzheimer's disease model rats. J. Neurochem. 81(5):1084-1091; 2002.
20. 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.
21. Jo, A. Y.; Kim, M. Y.; Lee, H. S.; Rhee, Y. H.; Lee, J. E.; Baek, K. H.; Park, C. H.; Koh, H. C.; Shin, I.; Lee, Y. S.; Lee, S. H. Generation of dopamine neurons with improved cell survival and phenotype maintenance using a degradation-resistant nurr1 mutant. Stem Cells 27(9): 2238-2246; 2009.
22. Kao, C. L.; Tai, L. K.; Chiou, S. H.; Chen, Y. J.; Lee, K. H.; Chou, S. J.; Chang, Y. L.; Chang, C. M.; Chen, S. J.; Ku, H. H.; Li, H. Y. Resveratrol promotes osteogenic differentiation and protects against dexamethasone damage in murine induced pluripotent stem cells. Stem Cells Dev. 19(2):247-258; 2010.
23. Katakura, M.; Hashimoto, M.; Shahdat, H. M.; Gamoh, S.; Okui, T.; Matsuzaki, K.; Shido, O. Docosahexaenoic acid promotes neuronal differentiation by regulating basic helix-loop-helix transcription factors and cell cycle in neural stem cells. Neuroscience 160(3):651-660; 2009.
24. Lin, C. P.; Tseng, W. Y.; Cheng, H. C.; Chen, J. H. Validation of diffusion tensor magnetic resonance axonal fiber imaging with registered manganese-enhanced optic tracts. Neuroimage 14(5):1035-1047; 2001.
25. Lindvall, O.; Hagell, P. Cell therapy and transplantation in Parkinson's disease. Clin. Chem. Lab. Med. 39(4):356-361; 2001.
26. Lindvall, O.; Kokaia, Z.; Martinez-Serrano, A. Stem cell therapy for human neurodegenerative disorders-how to make it work. Nat. Med. 10 Suppl:S42-50; 2004.
27. Lukiw, W. J.; Cui, J. G.; Marcheselli, V. L.; Bodker, M.; Botkjaer, A.; Gotlinger, K.; Serhan, C. N.; Bazan, N. G. A role for docosahexaenoic acid-derived neuroprotectin D1 in neural cell survival and Alzheimer disease. J. Clin. Invest. 115(10):2774-2783; 2005.
28. Mahmoudi, S.; Samadi, P.; Gilbert, F.; Ouattara, B.; Morissette, M.; Gregoire, L.; Rouillard, C.; Di Paolo, T.; Levesque, D. Nur77 mRNA levels and L-Dopa-induced dyskinesias in MPTP monkeys treated with docosahexaenoic acid. Neurobiol. Dis. 36(1):213-222; 2009.
29. Mischoulon, D.; Fava, M. Docosahexanoic acid and omega-3 fatty acids in depression. Psychiatr. Clin. North Am. 23(4):785-794; 2000.
30. Miura, K.; Okada, Y.; Aoi, T.; Okada, A.; Takahashi, K.; Okita, K.; Nakagawa, M.; Koyanagi, M.; Tanabe, K.; Ohnuki, M.; Ogawa, D.; Ikeda, E.; Okano, H.; Yamanaka, S. Variation in the safety of induced pluripotent stem cell lines. Nat. Biotechnol. 27(8):743-745; 2009.
31. Monahan, A. J.; Warren, M.; Carvey, P. M. Neuroinflammation and peripheral immune infiltration in Parkinson's disease: An autoimmune hypothesis. Cell Transplant. 17(4):363-372; 2008.
32. Moretti, A.; Bellin, M.; Welling, A.; Jung, C. B.; Lam, J. T.; Bott-Flugel, L.; Dorn, T.; Goedel, A.; Hohnke, C.; Hofmann, F.; Seyfarth, M.; Sinnecker, D.; Schomig, A.; Laugwitz, K. L. Patient-specific induced pluripotent stemcell models for long-QT syndrome. N. Engl. J. Med. 363(15):1397-1409; 2010.
33. Mukherjee, P. K.; Marcheselli, V. L.; Serhan, C. N.; Bazan, N. G. Neuroprotectin D1: A docosahexaenoic acidderived docosatriene protects human retinal pigment epithelial cells from oxidative stress. Proc. Natl. Acad. Sci. USA 101(22):8491-8496; 2004.
34. Olanow, C. W.; Kordower, J. H.; Freeman, T. B. Fetal nigral transplantation as a therapy for Parkinson's disease. Trends Neurosci. 19(3):102-109; 1996.
35. Peng, C. H.; Chiou, S. H.; Chen, S. J.; Chou, Y. C.; Ku, H. H.; Cheng, C. K.; Yen, C. J.; Tsai, T. H.; Chang, Y. L.; Kao, C. L. Neuroprotection by Imipramine against lipopolysaccharide-induced apoptosis in hippocampusderived neural stem cells mediated by activation of BDNF and the MAPK pathway. Eur. Neuropsychopharmacol. 18(2):128-140; 2008.
36. Pruszak, J.; Sonntag, K. C.; Aung, M. H.; SanchezPernaute, R.; Isacson, O. Markers and methods for cell sorting of human embryonic stem cell-derived neural cell populations. Stem Cells 25(9):2257-2268; 2007.
37. Redmond, Jr., D. E.; Bjugstad, K. B.; Teng, Y. D.; Ourednik, V.; Ourednik, J.; Wakeman, D. R.; Parsons, X. H.; Gonzalez, R.; Blanchard, B. C.; Kim, S. U.; Gu, Z.; Lipton, S. A.; Markakis, E. A.; Roth, R. H.; Elsworth, J. D.; Sladek, Jr., J. R.; Sidman, R. L.; Snyder, E. Y. Behavioral improvement in a primate Parkinson's model is associated with multiple homeostatic effects of human neural stem cells. Proc. Natl. Acad. Sci. USA 104(29): 12175-12180; 2007.
38. 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.
39. Samadi, P.; Gregoire, L.; Rouillard, C.; Bedard, P. J.; Di Paolo, T.; Levesque, D. Docosahexaenoic acid reduces levodopa-induced dyskinesias in 1-methyl-4-phenyl-1,2, 3,6-tetrahydropyridine monkeys. Ann. Neurol. 59(2):282-288; 2006.
40. Samii, A.; Nutt, J. G.; Ransom, B. R. Parkinson's disease. Lancet 363(9423):1783-1793; 2004.
41. Saucedo-Cardenas, O.; Quintana-Hau, J. D.; Le, W. D.; Smidt, M. P.; Cox, J. J.; De Mayo, F.; Burbach, J. P.; Conneely, O. M. Nurrl is essential for the induction of the dopaminergic phenotype and the survival of ventral mesencephalic late dopaminergic precursor neurons. Proc. Natl. Acad. Sci. USA 95(7):4013-4018; 1998.
42. Schumacher, J. M.; Ellias, S. A.; Palmer, E. P.; Kott, H. S.; Dinsmore, J.; Dempsey, P. K.; Fischman, A. J.; Thomas, C.; Feldman, R. G.; Kassissieh, S.; Raineri, R.; Manhart, C.; Penney, D.; Fink, J. S.; Isacson, O. Transplantation of embryonic porcine mesencephalic tissue in patients with PD. Neurology 54(5):1042-1050; 2000.
43. Shim, J. W.; Park, C. H.; Bae, Y. C.; Bae, J. Y.; Chung, S.; Chang, M. Y.; Koh, H. C.; Lee, H. S.; Hwang, S. J.; Lee, K. H.; Lee, Y. S.; Choi, C. Y.; Lee, S. H. Generation of functional dopamine neurons from neural precursor cells isolated from the subventricular zone and white matter of the adult rat brain using Nurr1 overexpression. Stem Cells 25(5):1252-1262; 2007.
44. 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.
45. Song, Z.; Cai, J.; Liu, Y.; Zhao, D.; Yong, J.; Duo, S.; Song, X.; Guo, Y.; Zhao, Y.; Qin, H.; Yin, X.; Wu, C.; Che, J.; Lu, S.; Ding, M.; Deng, H. Efficient generation of hepatocyte-like cells from human induced pluripotent stem cells. Cell Res. 19(11):1233-1242; 2009.
46. Takahashi, K.; Tanabe, K.; Ohnuki, M.; Narita, M.; Ichisaka, T.; Tomoda, K.; Yamanaka, S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131(5):861-872; 2007.
47. Takahashi, K.; Yamanaka, S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126(4):663-676; 2006.
48. Tsuji, O.; Miura, K.; Okada, Y.; Fujiyoshi, K.; Mukaino, M.; Nagoshi, N.; Kitamura, K.; Kumagai, G.; Nishino, M.; Tomisato, S.; Higashi, H.; Nagai, T.; Katoh, H.; Kohda, K.; Matsuzaki, Y.; Yuzaki, M.; Ikeda, E.; Toyama, Y.; Nakamura, M.; Yamanaka, S.; Okano, H. Therapeutic potential of appropriately evaluated safe-induced pluripotent stem cells for spinal cord injury. Proc. Natl. Acad. Sci. USA 107(28):12704-12709; 2010.
49. Wallen, A.; Zetterstrom, R. H.; Solomin, L.; Arvidsson, M.; Olson, L.; Perlmann, T. Fate of mesencephalic AHD2-expressing dopamine progenitor cells in NURR1 mutant mice. Exp. Cell Res. 253(2):737-746; 1999.
50. Wernig, M.; Zhao, J. P.; Pruszak, J.; Hedlund, E.; Fu, D.; Soldner, F.; Broccoli, V.; Constantine-Paton, M.; Isacson, O.; Jaenisch, R. Neurons derived from reprogrammed fibroblasts functionally integrate into the fetal brain and improve symptoms of rats with Parkinson's disease. Proc. Natl. Acad. Sci. USA 105(15):5856-5861; 2008.
51. Wright, A. K.; Garcia-Munoz, M.; Arbuthnott, G. W. Slowly progressive dopamine cell loss-a model on which to test neuroprotective strategies for Parkinson's disease? Rev. Neurosci. 20(2):85-94; 2009.
52. Yamanaka, S. Induction of pluripotent stem cells from mouse fibroblasts by four transcription factors. Cell Prolif. 41(Suppl. 1):51-56; 2008.
53. Yang, D.; Zhang, Z. J.; Oldenburg, M.; Ayala, M.; Zhang, S.C. Human embryonic stem cell-derived dopaminergic neurons reverse functional deficit in parkinsonian rats. Stem Cells 26(l):55-63; 2008.
54. Zetterstrom, R. H.; Solomin, L.; Jansson, L.; Hoffer, B. J.; Olson, L.; Perlmann, T. Dopamine neuron agenesis in Nurrl-deficient mice. Science 276(5310):248-250; 1997.
55. Zuccato, C.; Cattaneo, E. Brain-derived neurotrophic factor in neurodegenerative diseases. Nat. Rev. Neurol. 5(6): 311-322; 2009.