DOI QR코드

DOI QR Code

Effect of Neurotrophic Factors on Neuronal Stem Cell Death

  • Published : 2002.01.31

Abstract

Neural cell survival is an essential concern in the aging brain and many diseases of the central nervous system. Neural transplantation of the stem cells are already applied to clinical trials for many degenerative neurological diseases, including Huntington's disease, Parkinson's disease, and strokes. A critical problem of the neural transplantation is how to reduce their apoptosis and improve cell survival. Neurotrophic factors generally contribute as extrinsic cues to promote cell survival of specific neurons in the developing mammalian brains, but the survival factor for neural stem cell is poorly defined. To understand the mechanism controlling stem cell death and improve cell survival of the transplanted stem cells, we investigated the effect of plausible neurotrophic factors on stem cell survival. The neural stem cell, HiB5, when treated with PDGF prior to transplantation, survived better than cells without PDGF. The resulting survival rate was two fold for four weeks and up to three fold for twelve weeks. When transplanted into dorsal hippocampus, they migrated along hippocampal alveus and integrated into pyramidal cell layers and dentate granule cell layers in an inside out sequence, which is perhaps the endogenous pathway that is similar to that in embryonic neurogenesis. Promotion of the long term-survival and differentiation of the transplanted neural precursors by PDGF may facilitate regeneration in the aging adult brain and probably in the injury sites of the brain.

Keywords

References

  1. Alderson, R. F., Alterman, A. L., Barde, Y. A. and Lindsay, R. M. (1990) Brain-derived Neurotrophic Factor Increases Survival and Differentiated Functions of Rat Septal Cholinergic Neurons In Culture. Neuron 5, 297-306. https://doi.org/10.1016/0896-6273(90)90166-D
  2. Altman, J. and Bayer, S. A. (1990) Prolonged sojourn of developing pyramidal cells in the intermediate zone of the hippocampus and their settling in the stratum pyramidale. J. Camp. Neurol. 301, 343-364. https://doi.org/10.1002/cne.903010303
  3. Altman J. and Bayer. S. A. (1990) Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods. J. Camp. Neurol. 301, 365- 381. https://doi.org/10.1002/cne.903010304
  4. Altman J. and Das G. D. (1965) Post-natal origin of microneurones in the rat brain. Nature 28, 953-956.
  5. Benihoud, K., Yeh, P. and Perricaudet, M. (1999) Adenovirus vectors for gene delivery. Curr Opin. Biotech. 10, 440-447. https://doi.org/10.1016/S0958-1669(99)00007-5
  6. Bonni, A., Brunet, A., West A. E., Datta, S. R., Takasu, M. A. and Greenberg, M. E. (1999) Cell survival promoted by the Ras-MAPK signaling pathway by transcription-dependent and - independent mechanisms. Science 286, 1358-1362. https://doi.org/10.1126/science.286.5443.1358
  7. Brustle, O., Maskos, U. and McKay, R. D. (1995) Host-guided migration allows targeted introduction of neurons into the embryonic brain. Neuron 15, 1275-1285 https://doi.org/10.1016/0896-6273(95)90007-1
  8. Cheng, B. and Mattson, M. P. (1994) NT-3 and BDNF protect CNS neurons against metabolic/excitotoxic insults. Brain Res. 640,56-67. https://doi.org/10.1016/0006-8993(94)91857-0
  9. Choi, D. W. (2001) Excitotoxicity, apoptosis, and ischemic stroke. J. Biochem. Mol. BioI. 34, 8-14.
  10. Chung, J., Cho, S., Kwon, Y. K., Kim, D. H. and Kim, K. (2000) Activation of retinoic acid receptor g induces proliferation of immortalized hippocampal progenitor cells. Mol. Brain Res. 83, 52-62. https://doi.org/10.1016/S0169-328X(00)00196-0
  11. Collazo, D., Takahashi, H. and Mckay, R. D. G. (1992) Cellular Targets and Trophic Functions of neurotrophin-3 In the Developing Rat Hippocampus. Cell 9, 643-656.
  12. Creuzet, C., Loeb, J. and Barbin, G. (1995) Fibroblast growth factors stimulate protein tyrosine phosphorylation and mitogen-activated protein kinase activity in primary cultures of hippocampal neurons. J. Neurochem. 64, 1541-1547. https://doi.org/10.1046/j.1471-4159.1995.64041541.x
  13. Ernfors, P., Ibanez, C. F., Ebendal, T., Olson, L. and Persson, H. (1990) Molecular Cloning and Neurotrophic Activities of a Protein with Structural Similarities to Nerve Growth Factor: Developmental and Topographical Expression in the Brain. Proc. Natl. Acad. Sci. USA 87, 5454-5458. https://doi.org/10.1073/pnas.87.14.5454
  14. Frade, J. M., Rodriguez-Tebar, A. and Barde, Y.-A. (1996) Induction of cell death by endogenous nerve growth factor through its p75 receptor, Nature 383, 166-168. https://doi.org/10.1038/383166a0
  15. Gall, C. M. and Isackson, P. J. (1989) Limbic seizures increase neuronal production of messenger RNA for nerve growth factor. Science 245, 758-761. https://doi.org/10.1126/science.2549634
  16. Gao, H. and Hollyfield, Joe G. (1995) Basic Fibroblast Growth Factor in Retinal Development: Differential Levels of bFGF Expression and Content in Normal and Retinal Degeneration (rd) Mutant Mice. Dev. BioI. 169, 168-184. https://doi.org/10.1006/dbio.1995.1135
  17. Giger, R., Ziegler, U., Hermens, W., Kunz, B., Kunz, S. and Sonderegger, P. (1997) Adenovirus-mediated gene transfer in neurons: construction and characterization of a vector for heterologous expression of the axonal cell adhesion· molecule axonin-1. J. Neurosci. Methods 71, 99-111. https://doi.org/10.1016/S0165-0270(96)00130-6
  18. Hofer, M., Pagliusi, S. R., Hohn, A., Leibrock, J. and Barde, Y. A. (1990) Regional distribution of brain-derived neurotrophic factor mRNA in the adult mouse brain. EMBO J. 9, 2459- 2464.
  19. Hutchins J. B. and Jefferson V. E. (1992) Developmental distribution of platelet-derived growth factor in the mouse central nervous system. Dev. Brain. Res. 67, 121-135. https://doi.org/10.1016/0165-3806(92)90213-G
  20. Hyman, C., Hofer, M., Barde, Y. A., Juhasz, M., Yancopoulos, G. D., Squinto, S. P. and Lindsay, R. M. (1991) BDNF is a neurotrophic factor for dopaminergic neurons of the substantia nigra. Nature 350, 230-232. https://doi.org/10.1038/350230a0
  21. Johe, K. K., Hazel, T. G., Muller, T., Dugich-Djordjevic, M. M., and McKay, R. D. (1996) Single factors direct the differentiation of stem cells from the fetal and adult central nervous system. Genes & Dev. 15, 3129-3140.
  22. Johansson, C. B., Momma, S., Clarke, D. L., Risling, M., Lendahl, U. and Frisen, J. (1999) Identification of a neural stem cell in the adult mammalian central nervous system. Cell 96,25-34. https://doi.org/10.1016/S0092-8674(00)80956-3
  23. Joung, I., Kim, H. S., Hong, J. S., Kwon, H. and Kwon, Y. K. (2000) Effective gene transfer into regenerating sciatic nerves by adenoviral vectors: potentials for gene therapy of peripheral nerve injury. Mol. Cells. 10, 540-545. https://doi.org/10.1007/s10059-000-0540-4
  24. Klein, R., Nanduri, V., Jing, S., Lamballe, F., Tapley, P., Bryant, S., Cordon-Cardo, C., Jones, K. R., Reichardt, L. F. and Barbacid, M. (1991) The TrkB Tyrosine Protein Kinase Is a Receptor For Brain-derived Neurotrophic Factor and neurotrophin-3. Cell 66, 395-403. https://doi.org/10.1016/0092-8674(91)90628-C
  25. Kwon, H., Kim, K. S., Park, S. Y., Lee, D. K. and Yang, C. H. (2001) Inhibitory effect of paeoniflorin on Fos- Jun- DNA complex foemation and stimulation of apoptosis in HL-60 cells. J. Biochem. Mol. Biol. 34, 28-32.
  26. Kwon, Y. Kim (1997) Expression of brain-derived neutrophic factor mRNA stimulated by basic fibroblast growth factor and platelet-derived growth factor in rat hippocampal cell line. Mol. Cells 7, 320-325.
  27. Kwon, Y. Kim, Bhattacharyya, W. V., Cheon, K., Stiles, C. D. and Pomeroy, S. L. (1997) Activation of ErbB2 during wallerian degeneration of sciatic nerve. J. Neurosci. 17, 8293-8299. https://doi.org/10.1523/JNEUROSCI.17-21-08293.1997
  28. Lendahl, U. and McKay, R. D. G. (1990) The use of cell lines in neurobiology. Trends Neurosci. 13, 132-137. https://doi.org/10.1016/0166-2236(90)90004-T
  29. Lewin, G. R. and Barde, Y-A. (1996) Physiology of the neurotrophins. Annu. Rev. Neurosci. 19,289-317. https://doi.org/10.1146/annurev.ne.19.030196.001445
  30. Lindvall, O., Emfors, P., Bengzon, J., Kokaia, Z., Smith, M. L., Siesjo, B. K and Persson, H. (1992) Differential regulation of mRNAs for nerve growth factor, brain-derived neurotrophic factor, and neurotrophin 3 in the adult rat brain following cerebral ischemia and hypoglycemic coma. Proc. Natl. Acad. Sci. USA 89, 648-652. https://doi.org/10.1073/pnas.89.2.648
  31. Marsh, H. N., Scholz, W. K., Lamballe, F., Klein, R., Nanduri, V., Barbacid, M. and Palfrey, H. C. (1993) Signal transduction events mediated by the BDNF receptor gp 145trkB in primary hippocampal pyramidal cell culture. J. Neurosci. 13, 4281- 4292. https://doi.org/10.1523/JNEUROSCI.13-10-04281.1993
  32. Mattson, M. P., Murrain, M., Guthrie, P. B. and Kater, S. B. (1989) Fibroblast growth factor and glutamate: opposing roles in the generation and degeneration of hippocampal neuroarchitecture. J. Neurosci. 9, 3728-3740.
  33. McDonald, J. W., Liu, X. Z., Qu, Y., Liu, S., Mickey, S. K., Turetsky, D., Gottlieb, D. I. and Choi, D. W. (1999) Transplanted embryonic stem cells survive, differentiate and promote recovery in injured rat spinal cord. Nature Med. 5, 1410-1412. https://doi.org/10.1038/70986
  34. Olanow, C. W., Kordower, J. H. and Freeman, T. B. (1996) Fetal nigral transplantation as a therapy for Parkinson's disease. Trends Neurosci. 19, 102-109. https://doi.org/10.1016/S0166-2236(96)80038-5
  35. Park, C. M. and Hollenerg, M. J. (1989) Basic fibroblast growth factor induces retinal regeneration in vivo. Dev. Biol. 134, 201- 205. https://doi.org/10.1016/0012-1606(89)90089-4
  36. Park, C., Kang, M., Kwon, Y. K., Chung, J., Ahn, H. and Huh, Y. (2001) Inhibition of neuronal nitric oxide synthase enhances cell proliferation in the dentate gyrus of the adrenalectomized rat. Neurosci. Lett. 309, 9-12. https://doi.org/10.1016/S0304-3940(01)02003-1
  37. Renfranz, P., Cunningham, M. and Mckay, R. D. (1991) Region-specific differentiation of hippocampal stem cell line HiB5 upon implantation into the developing mammalian brain. Cell 66, 713-729. https://doi.org/10.1016/0092-8674(91)90116-G
  38. Reynolds, B. A. and Weiss, S. (1992) Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255, 1707-1710. https://doi.org/10.1126/science.1553558
  39. Ross, R. and Collins, T. (1991) PDGF B-chain in neurons of the central nervous system, posterior pituitary, and in a transgenic model. Cell 64, 217-227 https://doi.org/10.1016/0092-8674(91)90223-L
  40. Ryder, E. F., Snyder, E. Y. and Cepko, C. L. (1990) Establishment and characterization of multipotent neural cell lines using retrovirus vector-mediated oncogene transfer. J. Neurobiol. 21, 356-375. https://doi.org/10.1002/neu.480210209
  41. Sasahara, M., Fries, J. W., Raines, E. W., Gown, A. M., Westrum, L. E., Frosch, M. P., Bonthron, D. T., Sawai, H., Clarke, David B., Kittlerova, P., Bray, Garth M. and Aguayo, Albert J. (1996) Brain-Derived Neurotrophic Factor and Neurotrophin-4/5 Stimulate Growth of Axonal Branches from Regenerating Retinal Ganglion Cells. J. Neurosci. 16, 3887-3894. https://doi.org/10.1523/JNEUROSCI.16-12-03887.1996
  42. Segal, R. A., Goumnerova, L. C., Kwon, Yunhee Kim, Stiles, C. D. and Pomeroy, S. L. (1994) Expression of the neurotrophin receptor TrkC is linked to a favorable outcome in medulloblastoma,. Proc. Natl. Acad. Sci. USA 91, 12867- 12871. https://doi.org/10.1073/pnas.91.26.12867
  43. Segal, R. A. and Greenberg, M. E. (1996) Intracellular signaling pathways activated by neurotrophic factors. Annu. Rev. Neurosci. 19, 491-515. https://doi.org/10.1146/annurev.ne.19.030196.002423
  44. Shim, J. S., Lee, H. J., Park, S. S., Cha, B. G. and Chang, H. R. (2001) Curumin-induced apoptosis of A-431 cells involves caspase-3 activation. J. Biochem. Mol. Biol. 34, 189-193.
  45. Slack, R. and Miller, F. (1996) VIral vectors for modulating gene expression in neurons. Curr. Opin. Neurobiol. 6, 576-583. https://doi.org/10.1016/S0959-4388(96)80088-2
  46. Smits, A., Kato, M., Westerrnark, B., Nister, M., Heldin, C.-H. and Funa, K. (1991) Neurotrophic activity of platelet-derived growth factor (PDGF): Rat neuronal cells possess functional PDGF beta-type receptors and respond to PDGF. Proc. Natl. Acad. Sci. USA 88, 8159-8163. https://doi.org/10.1073/pnas.88.18.8159
  47. Sung, J. Y., Lee, S. Y., Min, D. S., Eom, T. Y., Ahn, Y. S., Choi, M., Kwon, Y. K. and Chung, K. C. (2001) Differential activation of phospholipases by mitogenic EGF and neurogenic PDGF in immortalized hippocampal stem cells lines. J. Neurochem. 78, 1044-1053. https://doi.org/10.1046/j.1471-4159.2001.00491.x
  48. Timmusk, T., Lendahl, U., Funakoshi, H., Arenas, E., Persson, H. and Metsis, M. (1995) Identification of brain-derived neurotrophic factor promoter regions mediating tissue-specific, axotomy-, and neuronal activity-induced expression in transgenic mice. J. Cell Biol. 128, 185-199. https://doi.org/10.1083/jcb.128.1.185
  49. VIcario-Abejon, C., Johe, Karl K., Hazel, Thomas G., Collazo, D. and McKay, D. G. (1995) Functions of basic fibroblast growth factor and neurotrophins in the differentiation of hippocampal neurons. Neuron 15, 105-114. https://doi.org/10.1016/0896-6273(95)90068-3
  50. Williams, B. P., Park, J. K., Alberta, J. A., Muhlebach, S.G., Hwang, G. Y., Roberts, T. M. and Stiles, C. D. (1997) A PDGF-regulated immediate early gene response initiates neuronal differentiation in ventricular zone progenitor cells. Neuron 18, 553-562. https://doi.org/10.1016/S0896-6273(00)80297-4
  51. Yao, R. and Cooper, G. M. (1995) Regulation of the Ras signaling pathway by GTPase-activating protein in PC12 cells. Oncogene. 11, 1607-1614.
  52. Yeh, H-J., Silo-Santiago, I., Wang, Y-X., George, R. J., Snider, W. D. and Deuel, T. F. (1993) Developmental expression of the platelet-derived growth factor alpha-receptor gene in mammalian central nervous system. Proc. Natl. Acad. Sci. USA 90, 1952-1956. https://doi.org/10.1073/pnas.90.5.1952
  53. Yuan, Junying and Yankner, Bruce A. (2000) Apoptosis in the nervous system. Nature 407, 802-809. https://doi.org/10.1038/35037739
  54. Zafra, F., Hengerer, B., Leibrock, J., Toenen, T. and Lindholm, L. (1990) Activity dependent regulation of BDNF and NGF mRNAs in the rat hippocampus is mediated by non-NMDA glutamate receptors. EMBO J. 9, 3545-3550.

Cited by

  1. Functions of neurotrophins and growth factors in neurogenesis and brain repair vol.83A, pp.1, 2013, https://doi.org/10.1002/cyto.a.22161
  2. Upregulation of TrkB by forskolin facilitated survival of MSC and functional recovery of memory deficient model rats vol.431, pp.4, 2013, https://doi.org/10.1016/j.bbrc.2012.12.122
  3. Neural stem cell differentiation is mediated by integrin β4 in vitro vol.41, pp.4, 2009, https://doi.org/10.1016/j.biocel.2008.09.001
  4. Autophagic Death of Adult Hippocampal Neural Stem Cells Following Insulin Withdrawal vol.26, pp.10, 2008, https://doi.org/10.1634/stemcells.2008-0153
  5. Incretin mimetics as pharmacologic tools to elucidate and as a new drug strategy to treat traumatic brain injury vol.10, pp.1, 2014, https://doi.org/10.1016/j.jalz.2013.12.011
  6. Autophagy for the quality control of adult hippocampal neural stem cells vol.1649, 2016, https://doi.org/10.1016/j.brainres.2016.02.048
  7. Mesencephalic human neural progenitor cells transplanted into the neonatal hemiparkinsonian rat striatum differentiate into neurons and improve motor behaviour vol.209, pp.6, 2006, https://doi.org/10.1111/j.1469-7580.2006.00654.x
  8. Adult hippocampal neurogenesis and aging vol.257, pp.5, 2007, https://doi.org/10.1007/s00406-007-0731-5
  9. Inhibition of Bcl-2 Stimulates Neural Stem Cell Proliferation in Organotypic Cultures of Mouse Hippocampus vol.45, pp.5, 2015, https://doi.org/10.1007/s11055-015-0104-x
  10. The role of neurotrophic factors in autism vol.16, pp.5, 2011, https://doi.org/10.1038/mp.2010.103
  11. Zuckerkandl's organ improves long-term survival and function of neural stem cell derived dopaminergic neurons in Parkinsonian rats vol.210, pp.2, 2008, https://doi.org/10.1016/j.expneurol.2007.12.016
  12. The application of platelet-rich plasma may be a novel treatment for central nervous system diseases vol.73, pp.6, 2009, https://doi.org/10.1016/j.mehy.2009.05.021
  13. Berberine Promotes Axonal Regeneration in Injured Nerves of the Peripheral Nervous System vol.15, pp.4, 2012, https://doi.org/10.1089/jmf.2011.2029
  14. Aucubin Promotes Neurite Outgrowth in Neural Stem Cells and Axonal Regeneration in Sciatic Nerves vol.23, pp.3, 2014, https://doi.org/10.5607/en.2014.23.3.238
  15. Mechanisms of cell death of neural progenitor cells caused by trophic support deprivation vol.548, pp.1-3, 2006, https://doi.org/10.1016/j.ejphar.2006.07.052
  16. Chitosan Channels Containing Spinal Cord-Derived Stem/Progenitor Cells for Repair of Subacute Spinal Cord Injury in the Rat vol.67, pp.6, 2010, https://doi.org/10.1227/NEU.0b013e3181f9af35
  17. Identification of aromatase-positive radial glial cells as progenitor cells in the ventricular layer of the forebrain in zebrafish vol.501, pp.1, 2007, https://doi.org/10.1002/cne.21222
  18. Extramedullary Chitosan Channels Promote Survival of Transplanted Neural Stem and Progenitor Cells and Create a Tissue Bridge After Complete Spinal Cord Transection vol.14, pp.5, 2008, https://doi.org/10.1089/tea.2007.0180