Neurotrophin and GDNF family ligands promote survival and alter excitotoxic vulnerability of neurons derived from murine embryonic stem cells

Experimental Neurology

Volumn 191, Issue 1, 2005, Pages 65-76

  Lee, Chul Sang ^a   Tee, Lee Y ^a   Dusenbery, Susan ^a   Takata, Toshihiro ^a   Golden, Judith P ^a   Pierchala, Brian A ^a   Gottlieb, David I ^a   Johnson Jr , Eugene M ^a   Choi, Dennis W ^a   Joy Snider, B ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Calcium; Neurturin; NMDA; NT 3; NT 4; Persephin; Ret; Trk receptor

Indexed keywords

GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GROWTH FACTOR RECEPTOR; LIGAND; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEUROTROPHIN; NEUROTROPHIN 3; PROTEIN DERIVATIVE; PROTEIN SUBUNIT; RECOMBINANT PROTEIN;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CELL DIVISION; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; DRUG MECHANISM; EMBRYO; EMBRYO CELL; IN VITRO STUDY; MOUSE; NERVE CELL CULTURE; NERVE CELL GROWTH; NERVE CELL NECROSIS; NERVE CELL STIMULATION; NEUROPROTECTION; NEUROTOXICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PREMEDICATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL;

ANIMALS; CELL LINE; CELL SURVIVAL; CELLS, CULTURED; EMBRYO; EXCITATORY AMINO ACID AGONISTS; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; LIGANDS; MICE; N-METHYLASPARTATE; NERVE GROWTH FACTORS; NEURONS; RECEPTORS, NERVE GROWTH FACTOR; STEM CELLS;

EID: 10044254089     PISSN: 00144886     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.expneurol.2004.08.025     Document Type: Article

References (65)

1. K. Abe Therapeutic potential of neurotrophic factors and neural stem cells against ischemic brain injury J. Cereb. Blood Flow Metab. 20 2000 1393 1408
2. P. Akerud, J. Alberch, S. Eketjall, J. Wagner, and E. Arenas Differential effects of glial cell line-derived neurotrophic factor and neurturin on developing and adult substantia nigra dopaminergic neurons J. Neurochem. 73 1999 70 78
3. J. Alberch, E. Perez-Navarro, and J.M. Canals Neuroprotection by neurotrophins and GDNF family members in the excitotoxic model of Huntington's disease Brain Res. Bull. 57 2002 817 822
4. G. Bain, D. Kitchens, M. Yao, J.E. Huettner, and D.I. Gottlieb Embryonic stem cells express neuronal properties in vitro Dev. Biol. 168 1995 342 357
5. R.H. Baloh, M.G. Tansey, J.P. Golden, D.J. Creedon, R.O. Heuckeroth, C.L. Keck, D.B. Zimonjic, N.C. Popescu, E.M. Johnson Jr., and J. Milbrandt TrnR2, a novel receptor that mediates neurturin and GDNF signaling through Ret Neuron 18 1997 793 802
6. M. Barbacid Structural and functional properties of the TRK family of neurotrophin receptors Ann. N. Y. Acad. Sci. 766 1995 442 458
7. P.A. Barker, C. Lomen-Hoerth, E.M. Gensch, S.O. Meakin, D.J. Glass, and E.M. Shooter Tissue-specific alternative splicing generates two isoforms of the trkA receptor J. Biol. Chem. 268 1993 15150 15157
8. B. Bates, L. Hirt, S.S. Thomas, S. Akbarian, D. Le, S. Amin-Hanjani, M. Whalen, R. Jaenisch, and M.A. Moskowitz Neurotrophin-3 promotes cell death induced in cerebral ischemia, oxygen-glucose deprivation, and oxidative stress: possible involvement of oxygen free radicals Neurobiol. Dis. 9 2002 24 37
9. M.M. Behrens, U. Strasser, and D.W. Choi Gö 6976 is a potent inhibitor of neurotrophin-receptor intrinsic tyrosine kinase J. Neurochem. 72 1999 919 924
10. M.M. Bilak, D.A. Shifrin, A.M. Corse, S.R. Bilak, and R.W. Kuncl Neuroprotective utility and neurotrophic action of neurturin in postnatal motor neurons: comparison with GDNF and persephin Mol. Cell. Neurosci. 13 1999 326 336
11. A. Blesch, P. Lu, and M.H. Tuszynski Neurotrophic factors, gene therapy, and neural stem cells for spinal cord repair Brain Res. Bull. 57 2002 833 838
12. C. Bonde, B.W. Kristensen, M. Blaabjerg, T.E. Johansen, J. Zimmer, and M. Meyer GDNF and neublastin protect against NMDA-induced excitotoxicity in hippocampal slice cultures NeuroReport 11 2000 4069 4073
13. J.E. Bottenstein, and G.H. Sato Growth of a rat neuroblastoma cell line in serum-free supplemented medium Proc. Natl. Acad. Sci. U. S. A. 76 1979 514 517
14. J. Bottenstein, I. Hayashi, S. Hutchings, H. Masui, J. Mather, D.B. McClure, S. Ohasa, A. Rizzino, G. Sato, G. Serrero, R. Wolfe, and R. Wu The growth of cells in serum-free hormone-supplemented media Methods Enzymol. 58 1979 94 109
15. K. Cairns, and S.P. Finklestein Growth factors and stem cells as treatments for stroke recovery Phys. Med. Rehabil. Clin. North Am. 14 2003 S135 S142
16. C.C. Chao, and E.H. Lee Neuroprotective mechanism of glial cell line-derived neurotrophic factor on dopamine neurons: role of antioxidation Neuropharmacology 38 1999 913 916
17. H. Cheng, Y.S. Fu, and J.W. Guo Ability of GDNF to diminish free radical production leads to protection against kainate-induced excitotoxicity in hippocampus Hippocampus 14 2004 77 86
18. P. Chomczynski, and N. Sacchi Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction Anal. Biochem. 162 1987 156 159
19. A.M. Corse, M.M. Bilak, S.R. Bilak, M. Lehar, J.D. Rothstein, and R.W. Kuncl Preclinical testing of neuroprotective neurotrophic factors in a model of chronic motor neuron degeneration Neurobiol. Dis. 6 1999 335 346
20. D.J. Creedon, M.G. Tansey, R.H. Baloh, P.A. Osborne, P.A. Lampe, T.J. Fahrner, R.O. Heuckeroth, J. Milbrandt, and E.M. Johnson Jr. Neurturin shares receptors and signal transduction pathways with glial cell line-derived neurotrophic factor in sympathetic neurons Proc. Natl. Acad. Sci. U. S. A. 94 1997 7018 7023
21. P. Dubus, M. Parrens, Y. El-Mokhtari, J. Ferrer, A. Groppi, and J.P. Merlio Identification of novel trkA variants with deletions in leucine-rich motifs of the extracellular domain J. Neuroimmunol. 107 2000 42 49
22. S. Dusenbery, B.J. Snider, L.Y. Tee, A. St Clair, L. Adams, D.I. Gottlieb, S. Liu, J.W. McDonald, and D.W. Choi Neurotrophin pretreatment enhances excitotoxic death in neurons derived from embryonic stem cells Abstr. - Soc. Neurosci. 27 2001 (Program 865.12)
23. M.J. Evans, and M.H. Kaufman Establishment in culture of pluripotential cells from mouse embryos Nature 292 1981 154 156
24. A. Fraichard, O. Chassande, G. Bilbaut, C. Dehay, P. Savatier, and J. Samarut In vitro differentiation of embryonic stem cells into glial cells and functional neurons J. Cell Sci. 108 1995 3181 3188
25. G.W. Glazner, and M.P. Mattson Differential effects of BDNF, ADNF9, and TNFa on levels of NMDA receptor subunits, calcium homeostasis, and neuronal vulnerability to excitotoxicity Exp. Neurol. 161 2000 442 452
26. J.P. Golden, J. Milbrandt, and E.M. Johnson Jr. Neurturin and persephin promote the survival of embryonic basal forebrain cholinergic neurons in vitro Exp. Neurol. 184 2003 447 455
27. E. Gratacos, E. Perez-Navarro, E. Tolosa, E. Arenas, and J. Alberch Neuroprotection of striatal neurons against kainate excitotoxicity by neurotrophins and GDNF family members J. Neurochem. 78 2001 1287 1296
28. 2+ indicators with greatly improved fluorescence properties J. Biol. Chem. 260 1985 3440 3450
29. B.J. Gwag, J.-Y. Koh, M.M. Chen, L.L. Dugan, M.M. Behrens, D. Lobner, and D.W. Choi BDNF or IGF-I potentiates free radical-mediated injury in cortical cell cultures NeuroReport 7 1995 93 96
30. T.W. Ho, L.A. Bristol, C. Coccia, Y. Li, J. Milbrandt, E. Johnson, L. Jin, O. Bar-Peled, J.W. Griffin, and J.D. Rothstein TGFβ trophic factors differentially modulate motor axon outgrowth and protection from excitotoxicity Exp. Neurol. 161 2000 664 675
31. C.R. Jarvis, Z.G. Xiong, J.R. Plant, D. Churchill, W.Y. Lu, B.A. MacVicar, and J.F. MacDonald Neurotrophin modulation of NMDA receptors in cultured murine and isolated rat neurons J. Neurophysiol. 78 1997 2363 2371
32. D.R. Kaplan, K. Matsumoto, E. Lucarelli, and C.J. Thiele Induction of TrkB by retinoic acid mediates biologic responsiveness to BDNF and differentiation of human neuroblastoma cells. Eukaryotic Signal Transduction Group Neuron 11 1993 321 331
33. H.J. Kim, J.J. Hwang, M.M. Behrens, B.J. Snider, D.W. Choi, and J.Y. Koh TrkB mediates BDNF-induced potentiation of neuronal necrosis in cortical culture Neurobiol. Dis. 14 2003 110 119
34. R. Klein, D. Conway, L.F. Parada, and M. Barbacid The trkB tyrosine protein kinase gene codes for a second neurogenic receptor that lacks the catalytic kinase domain Cell 61 1990 647 656
35. M. Kobayashi, K. Kurihara, and I. Matsuoka Retinoic acid induces BDNF responsiveness of sympathetic neurons by alteration of Trk neurotrophin receptor expression FEBS Lett. 356 1994 60 65
36. J.-Y. Koh, B.J. Gwag, D. Lobner, and D.W. Choi Potentiated necrosis of cultured cortical neurons by neurotrophins Science 268 1995 573 575
37. S.H. Lee, N. Lumelsky, L. Studer, J.M. Auerbach, and R.D. McKay Efficient generation of midbrain and hindbrain neurons from mouse embryonic stem cells Nat. Biotechnol. 18 2000 675 679
38. C.-S. Lee, L.Y. Tee, T. Takata, J.P. Golden, B.A. Tsui-Pierchala, E.M. Johnson Jr., and B.J. Snider GDNF supports survival and attenuates NMDA-mediated neuronal death in neurons derived from murine embryonic stem cells Abstr. - Soc. Neurosci. 2003 (Program 355.4)
39. M. Li, L. Pevny, R. Lovell-Badge, and A. Smith Generation of purified neural precursors from embryonic stem cells by lineage selection Curr. Biol. 8 1998 971 974
40. M. Lindahl, T. Timmusk, J. Rossi, M. Saarma, and M.S. Airaksinen Expression and alternative splicing of mouse Gfrα4 suggest roles in endocrine cell development Mol. Cell. Neurosci. 15 2000 522 533
41. G.R. Martin Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells Proc. Natl. Acad. Sci. U. S. A. 78 1981 7634 7638
42. K. McCarthy, and J. deVellis Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue J. Cell Biol. 85 1980 890 902
43. S.J. Morrison Neuronal potential and lineage determination by neural stem cells Curr. Opin. Cell Biol. 13 2001 666 672
44. O. Nicole, C. Ali, F. Docagne, L. Plawinski, E.T. MacKenzie, D. Vivien, and A. Buisson Neuroprotection mediated by glial cell line-derived neurotrophic factor: involvement of a reduction of NMDA-induced calcium influx by the mitogen-activated protein kinase pathway J. Neurosci. 21 2001 3024 3033
45. S. Okabe, K. Forsberg-Nilsson, A.C. Spiro, M. Segal, and R.D. McKay Development of neuronal precursor cells and functional postmitotic neurons from embryonic stem cells in vitro Mech. Dev. 59 1996 89 102
46. M.J. Perez-Garcia, V. Cena, Y. de Pablo, M. Llovera, J.X. Comella, and R.M. Soler Glial cell line-derived neurotrophic factor increases intracellular calcium concentration. Role of calcium/calmodulin in the activation of the phosphatidylinositol 3-kinase pathway J. Biol. Chem. 279 2004 6132 6142
47. J.H.M. Prehn Marked diversity in the action of growth factors on N-methyl-d-aspartate-induced neuronal degeneration Eur. J. Pharmacol. 306 1996 81 88
48. Y. Qu, S. Vadivelu, L. Choi, S. Liu, A. Lu, B. Lewis, R. Girgis, C.S. Lee, B.J. Snider, D.I. Gottlieb, and J.W. McDonald Neurons derived from embryonic stem (ES) cells resemble normal neurons in their vulnerability to excitotoxic death Exp. Neurol. 184 2003 326 336
49. M.C. Raff, R.H. Miller, and M. Noble A glial progenitor cell that develops in vitro into an astrocyte or an oligodendrocyte depending on culture medium Nature 303 1983 390 396
50. Y. Renoncourt, P. Carroll, P. Filippi, V. Arce, and S. Alonso Neurons derived in vitro from ES cells express homeoproteins characteristic of motoneurons and interneurons Mech. Dev. 79 1998 185 197
51. J.T. Rifkin, V.J. Todd, L.W. Anderson, and F. Lefcort Dynamic expression of neurotrophin receptors during sensory neuron genesis and differentiation Dev. Biol. 227 2000 465 480
52. A. Rodriguez-Tébar, and H. Rohrer Retinoic acid induces NGF-dependent survival response and high-affinity NGF receptors in immature chick sympathetic neurons Development 112 1991 813 820
53. K. Rose, D.W. Choi, and M.P. Goldberg Cytotoxicity in murine neocortical cell culture C. Tyson J. Frazier In Vitro Biological Methods Methods Toxicol. vol. 1A 1993 Academic Press San Diego, CA 46 60
54. M. Sanicola, C. Hession, D. Worley, P. Carmillo, C. Ehrenfels, L. Walus, S. Robinson, G. Jaworski, H. Wei, R. Tizard, A. Whitty, R.B. Pepinsky, and R.L. Cate Glial cell line-derived neurotrophic factor-dependent RET activation can be mediated by two different cell-surface accessory proteins Proc. Natl. Acad. Sci. U. S. A. 94 1997 6238 6243
55. R.J. Scheibe, and J.A. Wagner Retinoic acid regulates both expression of the nerve growth factor receptor and sensitivity to nerve growth factor J. Biol. Chem. 267 1992 17611 17616
56. M.J. Shamblott, J. Axelman, S. Wang, E.M. Bugg, J.W. Littlefield, P.J. Donovan, P.D. Blumenthal, G.R. Huggins, and J.D. Gearhart Derivation of pluripotent stem cells from cultured human primordial germ cells Proc. Natl. Acad. Sci. U. S. A. 95 1998 13726 13731
57. C. Strubing, G. Ahnert-Hilger, J. Shan, B. Wiedenmann, J. Hescheler, and A.M. Wobus Differentiation of pluripotent embryonic stem cells into the neuronal lineage in vitro gives rise to mature inhibitory and excitatory neurons Mech. Dev. 53 1995 275 287
58. J. Takahashi, T.D. Palmer, and F.H. Gage Retinoic acid and neurotrophins collaborate to regulate neurogenesis in adult-derived neural stem cell cultures J. Neurobiol. 38 1999 65 81
59. X.Q. Tang, Y. Wang, J.S. Han, and Y. Wan Adenovirus-mediated GDNF protects cultured motoneurons from glutamate injury NeuroReport 12 2001 3073 3076
60. J.A. Thomson, J. Itskovitz-Eldor, S.S. Shapiro, M.A. Waknitz, J.J. Swiergiel, V.S. Marshall, and J.M. Jones Embryonic stem cell lines derived from human blastocysts Science 282 1998 1145 1147
61. A.C. Tomac, A.D. Agulnick, N. Haughey, C.F. Chang, Y. Zhang, C. Backman, M. Morales, M.P. Mattson, Y. Wang, H. Westphal, and B.J. Hoffer Effects of cerebral ischemia in mice deficient in persephin Proc. Natl. Acad. Sci. U. S. A. 99 2002 9521 9526
62. B.A. Tsui-Pierchala, R.C. Ahrens, R.J. Crowder, J. Milbrandt, and E.M. Johnson Jr. The long and short isoforms of Ret function as independent signaling complexes J. Biol. Chem. 277 2002 34618 34625
63. W.G. van Inzen, M.P. Peppelenbosch, M.W. van den Brand, L.G. Tertoolen, and S.W. de Laat Neuronal differentiation of embryonic stem cells Biochim. Biophys. Acta 1312 1996 21 26
64. A. von Holst, A. Rodriguez-Tébar, J.J. Michaille, D. Dhouailly, A. Backstrom, T. Ebendal, and H. Rohrer Retinoic acid-mediated increase in TrkA expression is sufficient to elicit NGF-dependent survival of sympathetic neurons Mol. Cell. Neurosci. 6 1995 185 198
65. Y. Wang, S.Z. Lin, A.L. Chiou, L.R. Williams, and B.J. Hoffer Glial cell line-derived neurotrophic factor protects against ischemia-induced injury in the cerebral cortex J. Neurosci. 17 1997 4341 4348