Directed differentiation into neural lineages and therapeutic potential of porcine embryonic stem cells in rat parkinson's disease model

Cellular Reprogramming

Volumn 12, Issue 4, 2010, Pages 447-461

  Yang, Jenn Rong ^a,b   Liao, Chia Hsin ^c,d   Pang, Cheng Yoong ^c,d   Huang, Lynn Ling Huei ^e   Lin, Yu Ting ^a   Chen, Yi Ling ^a,b   Shiue, Yow Ling ^b   Chen, Lih Ren ^a,e,f  

^a FISHERIES RESEARCH INSTITUTE   (Taiwan)

^b NATIONAL SUN YAT SEN UNIVERSITY   (Taiwan)

^c BUDDHIST TZU CHI GENERAL HOSPITAL   (Taiwan)

^d TZU CHI UNIVERSITY   (Taiwan)

^e NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^f SOUTHERN TAIWAN UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; CHOLINE ACETYLTRANSFERASE; GREEN FLUORESCENT PROTEIN; TYROSINE 3 MONOOXYGENASE;

ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL LINEAGE; CONTROLLED STUDY; DOPAMINERGIC ACTIVITY; EMBRYONIC STEM CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; MALE; NERVE CELL; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; RAT; STEM CELL TRANSPLANTATION; SWINE;

ANIMALS; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; DISEASE MODELS, ANIMAL; DOPAMINE; EMBRYONIC STEM CELLS; GREEN FLUORESCENT PROTEINS; IMMUNOENZYME TECHNIQUES; INTERMEDIATE FILAMENT PROTEINS; MALE; NERVE TISSUE PROTEINS; NEURONS; PARKINSON DISEASE; RATS; RATS, SPRAGUE-DAWLEY; STEM CELL TRANSPLANTATION; SWINE;

ANIMALIA; RATTUS; SUS;

EID: 77955157760     PISSN: 21524971     EISSN: 21524998     Source Type: Journal    
DOI: 10.1089/cell.2009.0078     Document Type: Article

References (79)

1. Aberdam, D., Gambaro, K., Medawar, A., et al. (2007). Embryonic stem cells as a cellular model for neuroectodermal commitment and skin formation. C. R. Biol. 330, 479-484.
2. Assady, S., Maor, G., Amit, M., et al. (2001). Insulin production by human embryonic stem cells. Diabetes 50, 1691-1697.
3. Bain, G., Kitchens, D., Yao, M., et al. (1995). Embryonic stem cells express neuronal properties in vitro. Dev. Biol. 168, 342-357.
4. Barberi, T., Klivenyi, P., Calingasan, N.Y., et al. (2003). Neural subtype specification of fertilization and nuclear transfer embryonic stem cells and application in parkinsonian mice. Nat. Biotechnol. 21, 1200-1207.
5. Bjorklund, L.M., Sánchez-Pernaute, R., Chung, S., et al. (2002). Embryonic stem cells develop into functional dopaminergic neurons after transplantation in a Parkinson rat model. Proc. Natl. Acad. Sci. USA. 99, 2344-2349.
6. Brederlau, A., Correia, A.S., Anisimov, S.V., et al. (2006). 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. StemCells 24,1433-1440.
7. Brevini, T.A., Antonini, S., Cillo, F., et al. (2007). Porcine embryonic stem cells: facts, challenges and hopes. Theriogenol-ogy 68(Suppl 1), S206-S213.
8. Carpenter, M.K., Inokuma, M.S., Denham, J., et al. (2001). Enrichment of neurons and neural precursors from human embryonic stem cells. Exp. Neurol. 172, 383-397.
9. Cazillis, M., Lelièvre, V., and Gressens, P. (2005). Neural differentiation of murine embryonic stem cells ES. Med. Sci. (Paris). 21, 484-490.
10. Chen, L.R., Wang H.P., and Wu, M.C. (1991). In vitro culture of mammalian embryonic stem cells: II. In vitro culture of blas-tocyst-derived cells in mouse and pigs. J. Chin. Soc. Anim. Sci. 20, 326-339.
11. Chen, L.R., Shiue, Y.L., Bertolini, L., et al. (1999a). Establishment of pluripotent cell lines from porcine preimplantation embryos. Theriogenology 52, 195-212.
12. Chen, L. R., Shiue, Y.L., and Anderson, G.B. (1999b). Embryonic cell lines derived from morula to late hatched blastocyst stages in pigs. Taiwan Livestock Res. 32:169-181.
13. Chudakov, D.M., Lukyanov, S., and Lukyanov, K.A. (2005). Fluorescent proteins as a toolkit for in vivo imaging. Trends Biotechnol. 23, 605-613.
14. Drukker, M. (2008). Recent advancements towards the derivation of immune-compatible patient-specific human embryonic stem cell lines. Semin. Immunol. 20, 123-129.
15. Drukker, M., Katz, G., Urbach, A., et al. (2002). Characterization of the expression of MHC proteins in human embryonic stem cells. Proc. Natl. Acad. Sci. USA 99, 9864-9869.
16. Feletou, M., and Teisseire, B. (1992). Vascular pharmacology of the micropig: importance of the endothelium. In: Swine as Models in Biomedical Research. M.M. Swindle, ed. (Iowa State University Press, Ames, IA), pp. 74-95.
17. Ferguson, T.A., Green, D.R., and Griffith, T.S. (2002). Cell death and immune privilege. Int. Rev. Immunol. 21, 153-172.
18. Flye, M.W. (1992). Orthotopic liver transplantation in outbred and partially inbred swine. In: Swine as Models in Biomedical Research. M.M. Swindle, ed. (Iowa State University Press, Ames, IA), pp. 44-56.
19. Freed, C.R., Greene, P.E., Breeze, R.E., et al. (2001). Transplantation of embryonic dopamine neurons for severe Parkinson's disease. N. Engl. J. Med. 344, 710-719.
20. Guan, K., Chang, H., Rolletschek, A., et al. (2001). Embryonic stem cell-derived neurogenesis. Retinoic acid induction and lineage selection of neuronal cells. Cell Tissue Res. 305, 171-176.
21. Hadjantonakis, A.K., Macmaster, S., and Nagy, A. (2002). Embryonic stem cells and mice expressing different GFP variants for multiple non-invasive reporter usage within a single animal. BMC Biotechnol. 2, 11-19.
22. Hall, T.S., Stuart, R.S., Baumgarten, W.A., et al. (1986). Use of swine in heart transplantation research. In: Swine in Biomedical Research. M.E. Tumbleson, ed. (Plenum Press, New York), pp. 373-376.
23. Hoffman, R.M. (2008). A better fluorescent protein for whole-body imaging. Trends Biotechnol. 26, 1-4.
24. Hudson, J.L., Levin, D.R., and Hoffer, B.J. (1993). A 16-channel automated rotometer system for reliable measurement of turning behavior in 6-hydroxydopamine lesioned and transplanted rats. Cell Transplant. 2, 507-514.
25. Iacovitti, L., Donaldson, A.E., Marshall, C.E., et al. (2007). A protocol for the differentiation of human embryonic stem cells into dopaminergic neurons using only chemically defined human additives: Studies in vitro and in vivo. Brain Res. 1127, 19-25
26. Jü ngling, K., Nägler, K., Pfrieger, F.W., et al. (2003). Purification of embryonic stem cell-derived neurons by immunoisolation. FASEB J. 17, 2100-2102.
27. Kawasaki, H., Mizuseki, K., Nishikawa, S., et al. (2000). Induction of midbrain dopaminergic neurons from ES cells by stromal cell-derived inducing activity. Neuron 28, 31-40.
28. Kehat, I., Kenyagin-Karsenti, D., Snir, M., et al. (2001). Human embryonic stem cells can differentiate into myocytes with structural and functional properties of cardiomyocytes. J. Clin. Invest. 108, 407-414.
29. Kim, D.W., Chung, S., Hwang, M., et al. (2006). Stromal cell-derived inducing activity, Nurr1, and signaling molecules synergistically induce dopaminergic neurons from mouse embryonic stem cells. Stem Cells 24, 557-567.
30. Kim, J.H., Auerbach, J.M., Rodr?́guez-Gómez, J.A., et al. (2002). Dopamine neurons derived from embryonic stem cells function in an animal model of Parkinson's disease. Nature 418, 50-56.
31. Kurihara-Bergstrom, T., Woodworth, M., Feisullin, S., et al. (1986). Characterization of the Yucatan miniature pig skin and small intestine for pharmaceutical applications. Lab. Anim. Sci. 36, 396-399.
32. Lee, S.H., Lumelsky, N., Studer, L., et al. (2000). Efficient generation of midbrain and hindbrain neurons from mouse embryonic stem cells. Nat. Biotechnol. 18, 675-679.
33. Li, M., Zhang, D., Hou, Y., et al. (2003). Isolation and culture of embryonic stem cells from porcine blastocysts. Mol. Reprod. 65, 429-434.
34. Li, M., Li, Y.H., Hou, Y., et al. (2004). Isolation and culture of pluripotent cells from in vitro produced porcine embryos. Zygote 12, 43-48.
35. Li, X.J., Du, Z.W., Zarnowska, E.D., et al. (2005). Specification of motoneurons from human embryonic stem cells. Nat. Bio-technol. 23, 215-221.
36. Löscher, W., Richter, A., Nikkhah, G., et al. (1996). Behavioral and neurochemical dysfunction in the circling (ci) rat: a novel genetic animal model of a movement disorder. Neuroscience 74, 1135-1142.
37. Maden, M. (2002). Retinoid signalling in the development of the central nervous system. Nat. Rev. Neurosci. 3, 843-853.
38. Martinat, C., Bacci, J.J., Leete, T., et al. (2006). Cooperative transcription activation by Nurr1 and Pitx3 induces embryonic stem cell maturation to the midbrain dopamine neuron phe-notype. Proc. Natl. Acad. Sci. USA 103, 2874-2879.
39. Moritoh, Y., Yamato, E., Yasui, Y., et al. (2003). Analysis of insulin-producing cells during in vitro differentiation from feeder-free embryonic stem cells. Diabetes 52, 1163-1168.
40. Muramatsu, S.I., Okuno, T., Suzuki, Y., et al. (2009). Multitracer assessment of dopamine function after transplantation of embryonic stem cell-derived neural stem cells in a primate model of Parkinson's disease. Synapse 63, 541-548.
41. Nishimura, F., Yoshikawa, M., Kanda, S., et al. (2003). Potential use of embryonic stem cells for the treatment of mouse par-kinsonian models: improved behavior by transplantation of in vitro differentiated dopaminergic neurons from embryonic stem cells. Stem Cells 21, 171-180.
42. Olanow, C.W.,andTatton,W.G.(1999).Etiologyandpathogenesis of Parkinson's disease. Annu. Rev. Neurosci. 22, 123-144.
43. Park, C.H., Minn, Y.K., Lee, J.Y., et al. (2005). In vitro and in vivo analyses of human embryonic stem cell-derived dopamine neurons. J. Neurochem. 92, 1265-1276.
44. Paxinos, G., and Watson, C. (1986). The Rat Brain in Stereotaxic Coordinates, 2nd ed. (Academic Press, New York
45. Perrier, A.L., Tabar, V., Barberi, T., et al. (2004). Derivation of midbrain dopamine neurons from human embryonic stem cells. Proc. Natl. Acad. Sci. USA 101, 12543-12548.
46. Phillips, R.W., and Tumbleson, M.E. (1986). Models in "Swine in Biomedical Research," Vol. 1. M.E. Tumbleson, ed. (Plenum Press, New York), pp. 437-440.
47. Piccini, P., Brooks, D.J., Björklund, A., et al. (1999). Dopamine release from nigral transplants visualized in vivo in a Parkinson's patient. Neurosci. 2, 1137-1140.
48. Popova, E., Rentzsch, B., Bader, M., et al. (2008). Generation and characterization of a GFP transgenic rat line for embryological research. Transgenic Res. 17, 955-963.
49. Prelle, K., Vassiliev, I.M., Vassilieva, S.G., et al. (1999). Establishment of pluripotent cell lines from vertebrate species\Present status and future prospects. Cells Tissues Organs 165, 220-236.
50. Reubinoff, B.E., Pera, M.F., Fong, C.Y., et al. (2000). Embryonic stem cell lines from human blastocysts: somatic differentiation in vitro. Nat. Biotechnol. 18, 399-404.
51. Reubinoff, B.E., Itsykson, P., Turetsky, T., et al. (2001). Neural progenitors from human embryonic stem cells. Nat. Biotechnol. 19, 1134-1140.
52. Rodr?́guez-Gomez, J.A., Lu, J.Q., Velasco, I., et al. (2007). Persistent dopamine functions of neurons derived from embryonic stem cells in a rodent model of Parkinson disease. Stem Cells 25, 918-928.
53. m System for Windows. Release version 6.12. (SAS Institute Inc., Cary, NC
54. Schmidt, M.M., Guan, K., and Wobus, A.M. (2001). Lithium influences differentiation and tissue-specific gene expression of mouse embryonic stem (ES) cells in vitro. Int. J. Dev. Biol. 45, 421-429.
55. Schuldiner, M., Eiges, R., Eden, A., et al. (2001). Induced neuronal differentiation of human embryonic stem cells. Brain Res. 913, 201-205.
56. Schulz, T.C., Palmarini, G.M., Noggle, S.A., et al. (2003). Directed neuronal differentiation of human embryonic stem cells. BMC Neurosci. 4, 27-39.
57. Shim, J.W., Koh, H.C., Chang, M.Y., et al. (2004). Enhanced in vitro midbrain dopamine neuron differentiation, dopaminergic function, neurite outgrowth, and 1-methyl-4-phe-nylpyridium resistance in mouse embryonic stem cells overexpressing Bcl-XL. J. Neurosci. 24, 843-852.
58. Smukler, S.R., Runciman, S.B., Xu, S., et al. (2006). Embryonic stem cells assume a primitive neural stem cell fate in the absence of extrinsic influences. J. Cell Biol. 172, 79-90.
59. Strübing, C, Ahnert-Hilger, G., Shan, J., et al. (1995). Differentiation of pluripotent embryonic stem cells into the neuronal lineage in vitro gives rise to mature inhibitory and excitatory neurons. Mech. Dev. 53, 275-287.
60. Svendsen, C.N., ter Borg, M.G., Armstrong, R.J., et al. (1998). A new method for the rapid and long term growth of human neural precursor cells. J. Neurosci. Methods 85, 141-152.
61. Swindle, M.M., Thompson, R.P., Carabello, B.A., et al. (1992). Congenital cardiovascular disease. In: Swine as Models in Biomedical Research. M.M. Swindle, ed. (Iowa State University Press, Ames, IA), pp. 176-184.
62. Taylor, H., and Minger, S.L. (2005). Regenerative medicine in Parkinson's disease: generation of mesencephalic dopaminergic cells from embryonic stem cells. Curr. Opin. Biotechnol. 16, 487-492.
63. Thinyane, K., Baier, P.C., Schindehütte, J., et al. (2005). Fate of pre-differentiated mouse embryonic stem cells transplanted in unilaterally 6-hydroxydopamine lesioned rats: histological characterization of the grafted cells. Brain Res. 1045, 80-87.
64. Takagi, Y., Takahashi, J., Saiki, H., et al. (2005). Dopaminergic neurons generated from monkey embryonic stem cells function in a Parkinson primate model. J. Clin. Invest. 115, 102-109.
65. Thomson, J.A., Itskovitz-Eldor, J., Shapiro, S.S., et al. (1998). Embryonic stem cell lines derived from human blastocysts. Science 282, 1145-1147.
66. Tropepe, V., Hitoshi, S., Sirard, C, et al. (2001). Direct neural fate specification from embryonic stem cells: a primitive mammalian neural stem cell stage acquired through a default mechanism. Neuron 30, 65-78.
67. Vescovi, A.L., Parati, E.A., Gritti, A., et al. (1999). Isolation and cloning of multipotential stem cells from the embryonic human CNS and establishment of transplantable human neural stem cell lines by epigenetic stimulation. Exp. Neurol. 156, 71-83.
68. Wichterle, H., Lieberam, I., Porter, J.A., et al. (2002). Directed differentiation of embryonic stem cells into motor neurons. Cell 110, 385-397.
69. Winnard, P.T. Jr., Kluth, J.B., and Raman, V. (2006). Noninvasive optical tracking of red fluorescent protein-expressing cancer cells in a model of metastatic breast cancer. Neoplasia 8, 796-806.
70. Yan, Y., Yang, D., Zarnowska, E.D., et al. (2005). Directed differentiation of dopaminergic neuronal subtypes from human embryonic stem cells. Stem Cells 23, 781-790.
71. Yang, D., Zhang, Z.J., Oldenburg, M., et al. (2008). Human embryonic stem cell-derived dopaminergic neurons reverse functional deficit in Parkinsonian rats. Stem Cells 26, 55-63.
72. Yang, J.R., Shiue, Y.L., Liao, C.H., et al. (2009). Establishment and characterization of novel porcine embryonic stem cell lines expressing hrGFP. Cloning Stem Cells 11, 235-244.
73. Yang, M., Reynoso, J., Bouvet, M., et al. (2009). A transgenic red fluorescent protein-expressing nude mouse for color-coded imaging of the tumor microenvironment. J. Cell Biochem. 106, 279-284.
74. Ye, W., Shimamura, K., Rubenstein, J.L., et al. (1998). FGF and Shh signals control dopaminergic and serotonergic cell fate in the anterior neural plate. Cell 93, 755-766.
75. Yoshizaki, T., Inaji, M., Kouike, H., et al. (2004). Isolation and transplantation of dopaminergic neurons generated from mouse embryonic stem cells. Neurosci. Lett. 363, 33-37.
76. Zambraski, E.J., Thomas, G.D., and O'Hagan, K.P. (1992). DOCA-treated Yucatan miniature swine: a neurogenic model of essential hypertension. In: Swine as Models in Biomedical Research. M.M. Swindle, ed. (Iowa State University Press, Ames, IA), pp. 290-301.
77. Zeng, X., Cai, J., Chen, J., et al. (2004). Dopaminergic differentiation of human embryonic stem cells. Stem Cells 22, 925-940.
78. Zhang, S.C., Wernig, M., Duncan, I.D., et al. (2001). In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nat. Biotechnol. 19, 1129-1133.
79. Zhou, J.M., Xing, F.Y., Shi, J.J., et al. (2008). Quality of embryonic bodies and seeding density effects on neural differentiation of mouse embryonic stem cells. Cell Biol. Int. 32, 1169-1175.