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Effect of Single Growth Factor and Growth Factor Combinations on Differentiation of Neural Stem Cells

  • Choi, Kyung-Chul (Department of Neurosurgery, Uijeongbu St. Mary's Hospital, The Catholic University of Korea College of Medicine) ;
  • Yoo, Do-Sung (Department of Neurosurgery, Uijeongbu St. Mary's Hospital, The Catholic University of Korea College of Medicine) ;
  • Cho, Kyung-Sock (Department of Neurosurgery, Uijeongbu St. Mary's Hospital, The Catholic University of Korea College of Medicine) ;
  • Huh, Pil-Woo (Department of Neurosurgery, Uijeongbu St. Mary's Hospital, The Catholic University of Korea College of Medicine) ;
  • Kim, Dal-Soo (Department of Neurosurgery, Uijeongbu St. Mary's Hospital, The Catholic University of Korea College of Medicine) ;
  • Park, Chun-Kun (Department of Neurosurgery, Kangnam St. Mary's Hospital, The Catholic University of Korea College of Medicine)
  • 발행 : 2008.12.31

초록

Objective : The effects on neural proliferation and differentiation of neural stem cells (NSC) of basic fibroblast growth factor-2 (bFGF). insulin growth factor-I (IGF-I). brain-derived neurotrophic factor (BDNF). and nerve growth factor (NGF) were assessed. Also, following combinations of various factors were investigated : bFGF+IGF-I, bFGF+BDNF, bFGF+NGF, IGF-I+BDNF, IGF-I+NGF, and BDNF+NGF. Methods : Isolated NSC of Fisher 344 rats were cultured with individual growth factors, combinations of factors, and no growth factor (control) for 14 days. A proportion of neurons was analyzed using $\beta$-tubulin III and NeuN as neural markers. Results : Neural differentiations in the presence of individual growth factors for $\beta$-tubulin III-positive cells were : BDNF, 35.3%; IGF-I, 30.9%; bFGF, 18.1%; and NGF, 15.1%, and for NeuN-positive cells was : BDNF, 34.3%; bFGF, 32.2%; IGF-I, 26.6%; and NGF, 24.9%. However, neural differentiations in the absence of growth factor was only 2.6% for $\beta$-tubulin III and 3.1% for NeuN. For $\beta$-tubulin III-positive cells, neural differentiations were evident for the growth factor combinations as follows : bFGF+IGF-I, 73.1 %; bFGF+NGF, 65.4%; bFGF+BDNF, 58.7%; BDNF+IGF-I, 52.2%; NGF+IGF-I, 40.6%; and BDNF+NGF, 40.0%. For NeuN-positive cells : bFGF+IGF-I, 81.9%; bFGF+NGF, 63.5%; bFGF+BDNF, 62.8%; NGF+IGF-I, 62.3%; BDNF+NGF, 56.3%; and BDNF+IGF-I, 46.0%. Significant differences in neural differentiation were evident for single growth factor and combination of growth factors respectively (p<0.05). Conclusion : Combinations of growth factors have an additive effect on neural differentiation. The most prominent neural differentiation results from growth factor combinations involving bFGF and IGF-I. These findings suggest that the combination of a mitogenic action of bFGF and post-mitotic differentiation action of IGF-I synergistically affects neural proliferation and NSC differentiation.

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참고문헌

  1. Altman J, Das GD : Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124 : 319-335, 1965 https://doi.org/10.1002/cne.901240303
  2. Arsenijevic Y, Weiss S : Insulin-like growth factor-I is a differentiation factor for postmitotic CNS stem cell-derived neuronal precursors : distinct actions from those of brain-derived neurotrophic factor. J Neurosci 18 : 2118-2128, 1998 https://doi.org/10.1523/JNEUROSCI.18-06-02118.1998
  3. Arsennijevic Y, Weiss S, Schneider B, Aebischer P : Insulin-like growth factor-I is necessary for neural stem cell proliferation and demonstrates distinct actions of epidermal growth factor and fibroblast growth factor-2. J Neurosci 21 : 7194-7202, 2001 https://doi.org/10.1523/JNEUROSCI.21-18-07194.2001
  4. Bartlett WP, Li XS, Williams M, Benkovic S : Localization of insulin-like growth factor-1 mRNA in murine central nervous system during postnatal development. Dev Biol 147 : 239-250, 1991 https://doi.org/10.1016/S0012-1606(05)80021-1
  5. Beck KD, Knüsel B, Hefti F : The nature of the trophic action of brain-derived neurotrophic factor, des(1-3)-insulin-like growth factor-1, and basic fibroblast growth factor on mesencephalic dopaminergic neurons developing in culture. Neuroscience 52 : 855-866, 1993 https://doi.org/10.1016/0306-4522(93)90534-M
  6. Bondy CA, Werner H, Roberts CT Jr, LeRoith D : Cellular pattern of insulin-like growth factor-I (IGF-I) and type I IGF receptor gene expression in early organogenesis : comparison with IGF-II gene expression. Mol Endocrinol 4 : 1386-1398, 1990 https://doi.org/10.1210/mend-4-9-1386
  7. Cao QL, Zhang YP, Howard RM, Walters WM, Tsoulfas P, Whittemore SR : Pluripotent stem cells engrafted into the normal or lesioned adult rat spinal cord are restricted to a glial lineage. Exp Neurol 167 : 48-58, 2001 https://doi.org/10.1006/exnr.2000.7536
  8. Chen J, Li Y, Chopp M : Intracerebral transplantation of bone marrow with BDNF after MCAo in rat. Neuropharmacology 39 : 711-716, 2000 https://doi.org/10.1016/S0028-3908(00)00006-X
  9. Chen X, Li Y, Wang L, Katakowski M, Zhang L, Chen J, et al : Ischemic rat brain extracts induce human marrow stromal cell growth factor production. Neuropathology 22 : 275-279, 2002 https://doi.org/10.1046/j.1440-1789.2002.00450.x
  10. Drago J, Murphy M, Carroll SM, Harvey RP, Bartlett PF : Fibroblast growth factor-mediated proliferation of central nervous system precursors depends on endogenous production of insulin-like growth factor I. Proc Natl Acad Sci U S A 88 : 2199-2203, 1991
  11. Gage FH : Mammalian neural stem cells. Science 287 : 1433-1438, 2000 https://doi.org/10.1126/science.287.5457.1433
  12. Gage FH, Armstrong DM, Williams LR, Varon S : Morphological response of axotomized septal neurons to nerve growth factor. J Comp Neurol 269 : 147-155, 1988 https://doi.org/10.1002/cne.902690112
  13. Gage FH, Coates PW, Palmer TD, Kuhn HG, Fisher LJ, Suhonen JO, et al : Survival and differentiation of adult neuronal progenitor cells transplanted to the adult brain. Proc Natl Acad Sci U S A 92 : 11879-11883, 1995
  14. Gao WQ, Zheng JL, Karihaloo M : Neurotrophin-4/5 (NT-4/5) and brain-derived neurotrophic factor (BDNF) act at later stages of cerebellar granule cell differentiation. J Neurosci 15 : 2656-2667, 1995 https://doi.org/10.1523/JNEUROSCI.15-04-02656.1995
  15. Ghosh A, Carnahan J, Greenberg ME : Requirement for BDNF in activity-dependent survival of cortical neurons. Science 263 : 1618- 1623, 1994 https://doi.org/10.1126/science.7907431
  16. Gritti A, Parati EA, Cova L, Frolichsthal P, Galli R, Wanke E, et al : Multipotential stem cells from the adult mouse brain proliferate and self-renew in response to basic fibroblast growth factor. J Neurosci 16 : 1091-1100, 1996 https://doi.org/10.1523/JNEUROSCI.16-03-01091.1996
  17. Hanson MG Jr, Shen S, Wiemelt AP, McMorris FA, Barres BA : Cyclic AMP elevation is sufficient to promote the survival of spinal motor neurons in vitro. J Neurosci 18 : 7361-7371, 1998 https://doi.org/10.1523/JNEUROSCI.18-18-07361.1998
  18. Hefti F : Nerve growth factor promotes survival of septal cholinergic neurons after fimbrial transections. J Neurosci 6 : 2155-2162, 1986 https://doi.org/10.1523/JNEUROSCI.06-08-02155.1986
  19. Hohn A, Leibrock J, Bailey K, Barde YA : Identification and characterization of a novel member of the nerve growth factor/brainderived neurotrophic factor family. Nature 344 : 339-341, 1990 https://doi.org/10.1038/344339a0
  20. Kim JH, Auerbach JM, Rodríguez-Gómez JA, Velasco I, Gavin D, Lumelsky N, et al : Dopamine neurons derived from embryonic stem cells function in an animal model of Parkinson's disease. Nature 418 : 50-56, 2002 https://doi.org/10.1038/nature00900
  21. Kim JT, Yoo DS, Woo JH, Huh PH, Cho KS, Kim DS : The cell survival and differentiation after transplantation, which harvest from adult rat brain by high-speed centrifugation method. J Korean Neurosurg Soc 38 : 121-125, 2005
  22. Kirschenbaum B, Goldman SA : Brain-derived neurotrophic factor promotes the survival of neurons arising from the adult rat forebrain subependymal zone. Proc Natl Acad Sci U S A 92 : 210-214, 1995
  23. Klein R, Nanduri V, Jing SA, Lamballe F, Tapley P, Bryant S, et al : The trkB tyrosine protein kinase is a receptor for brain-derived neurotrophic factor and neurotrophin-3. Cell 66 : 395-403, 1991 https://doi.org/10.1016/0092-8674(91)90628-C
  24. Kolb B, Cote S, Ribeiro-da-Silva A, Cuello AC : Nerve growth factor treatment prevents dendritic atrophy and promotes recovery of function after cortical injury. Neuroscience 76 : 1139-1151, 1997 https://doi.org/10.1016/S0306-4522(96)00448-4
  25. Kromer LF : Nerve growth factor treatment after brain injury prevents neuronal death. Science 235 : 214-216, 1987 https://doi.org/10.1126/science.3798108
  26. Kuhn HG, Winkler J, Kempermann G, Thal LJ, Gage FH : Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain. J Neurosci 17 : 5820-5829, 1997 https://doi.org/10.1523/JNEUROSCI.17-15-05820.1997
  27. Kwon HJ, Lee KY, Park IK, Park MS, Lee MY, Kim MK : Expression of tyrosine kinase A in the cerebral cortex of postnatal developing rat. J Vet Sci 6 : 185-189, 2005
  28. Leonard DG, Ziff EB, Greene LA : Identification and characterization of mRNAs regulated by nerve growth factor in PC12 cells. Mol Cell Biol 7 : 3156-3167, 1987 https://doi.org/10.1128/MCB.7.9.3156
  29. LeRoith D, Werner H, Beitner-Johnson D, Roberts CT Jr : Molecular and cellular aspects of the insulin-like growth factor I receptor. Endocr Rev 16 : 143-163, 1995 https://doi.org/10.1210/edrv-16-2-143
  30. Li L, Oppenheim RW, Lei M, Houenou LJ : Neurotrophic agents prevent motoneuron death following sciatic nerve section in the neonatal mouse. J Neurobiol 25 : 759-766, 1994 https://doi.org/10.1002/neu.480250702
  31. Lois C, Alvarez-Buylla A : Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc Natl Acad Sci U S A 90 : 2074-2077, 1993
  32. Murer MG, Yan Q, Raisman-Vozari R : Brain-derived neurotrophic factor in the control human brain, and in Alzheimer's disease and Parkinson's disease. Prog Neurobiol 63 : 71-124, 2001 https://doi.org/10.1016/S0301-0082(00)00014-9
  33. Ng NF, Shooter EM : Activation of p21ras by nerve growth factor in embryonic sensory neurons and PC12 cells. J Biol Chem 268 : 25329-25333, 1993
  34. Onifer SM, Cannon AB, Whittemore SR : Altered differentiation of CNS neural progenitor cells after transplantation into the injured adult rat spinal cord. Cell Transplant 6 : 327-338, 1997 https://doi.org/10.1016/S0963-6897(97)00037-7
  35. Palmer TD, Markakis EA, Willhoite AR, Safar F, Gage FH : Fibroblast growth factor-2 activates a latent neurogenic program in neural stem cells from diverse regions of the adult CNS. J Neurosci 19 : 8487-8497, 1999 https://doi.org/10.1523/JNEUROSCI.19-19-08487.1999
  36. Palmer TD, Takahashi J, Gage FH : The adult rat hippocampus contains primordial neural stem cells. Mol Cell Neurosci 8 : 389- 404, 1997 https://doi.org/10.1006/mcne.1996.0595
  37. Robinson LJ, Leitner W, Draznin B, Heidenreich KA : Evidence that p21ras mediates the neurotrophic effects of insulin and insulinlike growth factor I in chick forebrain neurons. Endocrinology 135 : 2568-2573, 1994 https://doi.org/10.1210/en.135.6.2568
  38. Sugita N : Comparative studies on the growth of the cerebral cortex. J Comp Neurol 1918 : 61-117

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