Growth stimulation and chemotropic attraction of rat retinal ganglion cell axons in vitro by co-cultured optic nerves, astrocytes and astrocyte conditioned medium

International Journal of Developmental Neuroscience

Volumn 14, Issue 4, 1996, Pages 387-398

  Lucius, Ralph ^a   Young, Hans Peter ^a   Tidow, Susanne ^a   Sievers, Jobst ^a  

^a Kiel and Lungen Clinic Grosshansdorf   (Germany)

Author keywords

Axonal regeneration; Neurotrophic activity

Indexed keywords

NERVE GROWTH FACTOR;

ANIMAL CELL; ARTICLE; ASTROCYTE; BRAIN CORTEX; CELL CULTURE; CONTROLLED STUDY; CULTURE MEDIUM; EXPLANT; NERVE CELL CULTURE; NERVE CELL GROWTH; NERVE FIBER; NERVE FIBER GROWTH; NERVE FIBER REGENERATION; NONHUMAN; ONTOGENY; OPTIC NERVE; PRIORITY JOURNAL; RAT; RETINA GANGLION CELL;

EID: 0030198831     PISSN: 07365748     EISSN: None     Source Type: Journal    
DOI: 10.1016/0736-5748(96)00031-7     Document Type: Article

References (86)

1. 1. Allcutt D., Berry M. and Sievers J. (1984) A qualitative comparison of the reaction of retinal ganglion cells to optic nerve crush in neonatal and adult mice. Dev. Brain Res. 16, 231-240.
2. 2. Allcutt D., Berry M. and Sievers J. (1984) A quantitative comparison of the reaction of retinal ganglion cells to optic nerve crush in neonatal and adult mice. Dev. Brain Res. 16, 219-230.
3. 3. Bähr M., Eschweiler G. W. and Wolburg H. (1992) Precrushed sciatic nerve grafts enhance the survival and axonal regrowth of retinal ganglion cells in adult rats. Exp. Neurol. 116, 13-22.
4. 4. Bamberger C., Debus O. and Sievers J. (1990) Fetal and early postnatal but not late postnatal and adult optic nerves induce axon regeneration from the transected optic nerve of adult rats. Anat. Anzeiger 83, 195-196.
5. 5. Banker G. A. (1980) Trophic interactions between astroglial and hippocampal neurons in culture. Science 209, 809-810.
6. 6. Barnstable C. J. and Drager U. C. (1984) Thy-1 antigen: a ganglion specific cell marker in rodent retina. Neuroscience 11, 847-855.
7. 7. Bauer H. C. and Tontsch U. (1990) Glia-conditioned medium and attachment to ConA are essential for long-term culture of cortical neurons. Int. J. Devl Neurosci. 8, 151-158.
8. 8. Beckh S., Müller H. W. and Seifert W. (1987) Neurotrophic and neurite promoting activities in astroglial conditioned medium. In Glial-neuronal Communication in Development and Regeneration. NATO ASI Series H: Cell Biology. Vol. 2. (eds Althaus H. H. and Seifert W.), pp. 385-406. Springer, Heidelberg.
9. 9. Berry M. (1979) Regeneration in the central nervous system. In Recent Advances in Neuropathology. Vol. 1. (eds Smith W. T. and Cavanagh J. B.), pp. 67-111. Churchill Livingstone, Edinburgh.
10. 10. Berry M. (1983) Regeneration of axons in the central nervous system. Prog. Anat. 3, 213-233.
11. 11. Berry M., Rees L. and Sievers J. (1986) Regeneration of axons in the mammalian visual system. Exp. Brain Res. (Suppl.) 13, 18-33.
12. 12. Berry M., Rees L. and Sievers J. (1986b) Unequivocal regeneration of rat optic axons into sciatic nerve isografts. In Neural Tissue Transplantation Research. (eds Wallace R. and Das G. D.), pp. 63-79. Springer, New York.
13. 13. Berry M., Hall S., Rees L. and Sievers J. (1987) Role of basal lamina in axon regeneration. In Mesenchymal-epithelial Interactions in Neural Development, (eds Wolff J. R., Sievers J. and Berry M.), pp. 361-383. Springer, Berlin, New York.
14. 14. Berry M., Rees L., Hall S., Yiu P. and Sievers J. (1988) Optic axons regenerate into sciatic nerve isografts only in the presence of Schwann cells. Brain Res. Bull. 20, 223-231.
15. 15. Berry M., Hall S., Rees J., Carlile J. and Wyse J. P.H. (1992) Regeneration of axons in the optic nerve of the adult Browman-Wyse (BW) mutant rat. J. Neurocytol. 21, 426-448.
16. 16. Björklund A. and Stenevi U. (eds.) (1985) Neural Grafting in the Mammalian CNS. Elsevier, Amsterdam.
17. 17. Boehlen P. (1989) Fibroblast growth factor. Cytokines 1, 204-228.
18. 18. Brook G. A., Lawrence J. M. and Raisman G. (1993) Morphology and migration of cultured Schwann cells into the fimbria and hippocampus of adult rats. Glia 9, 292-304.
19. 19. Brown J. O. and McCough G. P. (1947) Abortive regeneration of the transected spinal cord. J. comp. Neurol. 87, 131-137.
20. 20. Caroni P. and Schwab M. E. (1988) Two membrane protein fractions from rat central myelin with inhibitory properties for neurite growth and fibroblast spreading. J. Cell Biol. 106, 1281-1288.
21. 21. Clemente C. D. (1964) Regeneration in the vertebrate central nervous system. Int. Rev. Neurobiol. 6, 257-301.
22. 22. David S. and Aguayo A. J. (1981) Axonal elongation into peripheral nervous system "bridges" after central nervous system injury in adult rats. Science 214, 931-933.
23. 23. Dentinger M. P., Barron K. D. and Csiza C. K. (1985) Glial and axonal development in optic nerve of myelin deficient rat mutant. Brain Res. 344, 255-266.
24. 24. Fallon J. R. (1985) Preferential outgrowth of CNS neurites on astrocytes and Schwann cells as compared with nonglial cells in vitro. J. Cell Biol. 100, 198-207.
25. 25. Ferrara N., Ousley F. and Gospodarowicz D. (1988) Bovine brain astrocytes express basic fibroblast growth factor, a neurotrophic protein and angiogenic mitogen. Brain Res. 462, 223-232.
26. 26. Fischer P. (1992) Untersuchung über den Einfluss des basischen Fibroblasten Wachstumsfaktors und von Basallamina auf die axonale Regeneration im Fasciculus Opticus der Ratte in vivo. MD Thesis, Universität Kiel.
27. 27. Friedmann B. and Aguayo A. J. (1985) Injured neurons in the olfactory bulb of the adult rat grow axons along grafts of peripheral nerve. J. Neurosci. 5, 1616-1625.
28. 28. Gower H. J., Barton C. H., Elsom V. L., Thompson J., Moore S. E., Dickson G. and Walsh F. S. (1988) Alternative splicing generates a secreted form of N-CAM in muscle and brain. Cell 55, 955-964.
29. 29. Hagg T., Manthorpe M., Vahlsing H. L. and Varon S. (1990) Nerve growth factor roles for cholinergic axonal regeneration in the adult mammalian central nervous system. Comments Dev. Neurobiol. 1, 157-175.
30. 30. Hall A. K. and Rao M. S. (1992) Cytokines and neurokines: related ligands and receptors. Trends Neurosci. 15, 35-37.
31. 31. Hasan S. J., Keirstead H. S., Muir G. D. and Steeves J. D. (1993) Axonal regeneration contributes to repair of injured brainstem-spinal neurons in embryonic chick. J. Neurosci. 13, 492-507.
32. 32. Hausmann B., Sievers J., Hermanns J. and Berry M. (1989) Regeneration of axons from the adult rat optic nerve: influence of fetal brain grafts, laminin and artificial basement membrane. J. comp. Neurol. 281, 447-466.
33. 33. Heumann R., Korsching S., Bandtlow C. and Thoenen H. (1987) Changes in nerve growth factor synthesis in nonneuronal cells in response to sciatic nerve transection. J. Cell Biol. 104, 1623-1631.
34. 34. Jackson K. F. and Duncan D. (1988) Cell kinetics and cell death in the optic nerve of the myclin deficient rat. J. Neurocytol. 17, 657-670.
35. 35. Kao C. C., Chang L. W. and Bloodworth J. M.B. (1977) Axonal regeneration across transected mammalian spinal cords: an electron microscopic study of delayed microsurgical nerve grafting. Exp. Neurol. 54, 591-615.
36. 36. Keirstead H. S., Hasan S. J., Muir G. D. and Steeves J. D. (1992) Suppression of the onset of myelination extends the permissive period for the functional repair of embryonic spinal cord. Proc. natn. Acad. Sci. U.S.A. 89, 11664-11668.
37. 37. Kennedy T. E., Serafini T., de la Torre J. R. and Tessier-Lavigne M. (1994) Netrins are diffusible chemotropic factors for commissural axons in the embryonic spinal cord. Cell 78, 425-435.
38. 38. Kiernan J. A. (1978) An explanation of axonal regeneration in peripheral nerves and its failure in the central nervous system. Med. Hypoth. 4, 15-26.
39. 39. Kromer L. F. and Cornbrooks C. J. (1985) Transplants of Schwann cell cultures promote axonal regeneration in the adult mammalian brain. Proc. natn. Acad. Sci. U.S.A. 82, 6330-6334.
40. 40. Kucherer-Ehret A., Pottgiesser J., Kreutzberg G. W., Thoenen H. and Edgar D. (1990) Developmental loss of laminin from the interstitial extracellular matrix correlates with decreased laminin gene expression. Development 110, 1285-1293.
41. 41. Letourneau P. C. (1978) Chemotactic response of nerve fiber elongation to nerve growth factor. Dev. Biol. 66, 183-196.
42. 42. Liesi P., Dahl D. and Vaheri A. (1983) Laminin is produced by early rat astrocytes in primary culture. J. Cell Biol. 96, 920-924.
43. 43. Liesi P., Kirkwood T. and Vaheri A. (1986) Fibronectin is expressed by astrocytes cultured from embryonic and early postnatal rat brain. Exp. Cell Res. 163, 175-185.
44. 44. Lindsay R. M. (1979) Adult rat brain astrocytes support survival of both NGF-dependent and NGF-insensitive neurons. Nature 282, 80-82.
45. 45. Logan A., Frautschy S. A., Gonzales A.-M. and Baird A. (1992) A time course for the focal elevation of synthesis of basic fibroblast growth factor and one of its high-affinity receptors (flg) following a localized cortical brain injury. J. Neurosci. 12, 3828-3837.
46. 46. Lucius R. and Sievers J. (1992) Regeneration of retinal ganglion cell axons in vitro: influence of astroglia-released stimulatory and inhibitory activities. Biol. Chem. Hoppe-Seyler 372, 954-955.
47. 47. Lucius R., Sievers J. and Mentlein R. (1995) Enkephalin metabolism by microglia ammopeptidase N (CD 13). J. Neurochem. 64, 1841-1847.
48. 48. Lumsden A. G.S. and Davies A. M. (1983) Earliest sensory nerve fibres are guided to peripheral targets by attractants other than nerve growth factor. Nature 306, 786-788.
49. 49. Lund R. D. (1978) Development and Plasticity of the Brain. Oxford University Press, New York.
50. 50. McCarthy K. D. and de Vellis J. (1980) Preparation of separate astroglial and oligodendroglial cell cultures from rat cerebral tissue. J. Cell Biol. 85, 890-902.
51. 51. Menesini-Chen M. G., Chen J. S. and Levi-Montalcini R. (1978) Sympathetic nerve fibers ingrowth in the central nervous system of neonatal rodent upon intracerebral NGF injections. Arch. Ital. Biol. 116, 53-84.
52. 52. Müller H. W., Beckh S. and Seifert W. (1984) Neurotrophic factor for central neurons. Proc. natn. Acad. Sci. U.S.A. 81, 1248-1252.
53. 53. Noble M., Fok-Seang J. and Cohen J. (1984) Glia are a unique substrate for the in vitro growth of central nervous system neurons. J. Neurosci. 4, 1892-1903.
54. 54. Ogawa H., Sato Y., Takeshita I., Tateishi J. and Kitamura K. (1985) Transient expression of glial fibrillary acidic protein in developing oligodendrocytes in vitro. Dev. Brain Res. 18, 133-141.
55. 55. Oorschot D. E. and Jones D. G. (1990) Axonal regeneration in the mammalian central nervous system. Adv. Anat. Embryol. Cell Biol. 119, 1-118.
56. 56. Parwaresch R., Radzun H. J., Kreipe H., Hausmann M. L. and Barth J. (1986) Monocyte/macrophage reactive monoclonal antibody Ki-M6 recognizes an intracytoplasmic antigen. Am. J. Pathol. 125, 141-151.
57. 57. Pini A. (1993) Chemorepulsion of axons in the developing mammalian central nervous system. Science 261, 95-98.
58. 58. Price J. and Hynes R. O. (1985) Astrocytes in culture synthesize and secret a variant form of fibronectin. J. Neurosci. 5, 2205-2211.
59. 59. Ramon y Cajal, S. (1928) Degeneration and Regeneration of the Nervous System. Oxford Press, London.
60. 60. Richardson A., Hao C. and Fedoroff S. (1993) Microglia progenitor cells: a subpopulation of mouse neopallial astroglia. Glia 7, 25-33.
61. 61. Rieske E., Graeber M. B., Tetzlaff W., Czlonkowska A., Streit W. and Kreutzberg G. W. (1989) Microglia and microglia-derived brain macrophages in culture: generation from axotomized rat facial nuclei, identification and characterisation in vitro. Brain Res. 492, 1-14.
62. 62. Rifkin D. B. and Moscatelli D. (1989) Recent developments in the cell biology of basic fibroblast growth factor. J. Cell Biol. 109, 1-6.
63. 63. Schwab M. E. and Caroni P. (1988) Oligodendrocytes and CNS myelin are nonpermissive substrates for neurite growth and fibroblast spreading in vitro. J. Neurosci. 8, 2381-2393.
64. 64. Serafini T., Kennedy T. E., Galko M. J., Mirzayan C., Jessell T. M. and Tessier-Lavigne M. (1994) The netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6. Cell 78, 409-424.
65. 65. Shewan D., Berry M., Bedi K. and Cohen J. (1993) Embryonic optic nerve tissue fails to support neurite outgrowth by central and peripheral neurons in vitro. Eur. J. Neurosci. 5, 809-817.
66. 66. Shimizu I., Oppenheim R. W., O'Brien M. and Shneiderman A. (1990) Anatomical and functional recovery following spinal cord transection in the chick embryo. J. Neurobiol. 21, 918-937.
67. 67. Sievers J., Hausmann B., Unsicker K. and Berry M. (1987) Fibroblast growth factors promote the survival of adult rat retinal ganglion cells after transection of the optic nerve. Neurosci. Lett. 76, 157-162.
68. 68. Sievers J., deGroot H., Meyer J. P. and Young P. (1991) Dual actions of astrocytes on regeneration of retinal axons in vitro. Third IBRO world congress of neuroscience, Abstracts, p. 33.
69. 69. Sievers J., Parwaresch R. and Wottge H. U. (1994) Blood monocytes and spleen macrophages differentiate into microglia-like cells on monolayers of astrocytes: morphology. Glia 12, 245-258.
70. 70. Sievers J., Bamberger C., Debus O. M. and Lucius R. (1995) Regeneration in the optic nerve of adult rats: influences of cultured astrocytes and optic nerve grafts of different ontogenetic stages. J. Neurocytol. 24, 783-793.
71. 71. Skoff R. P., Price D. L. and Stocks A. (1976) Electron microscopic autoradiographic studies of gliogenesis in rat optic nerve. J. comp. Neurol. 169, 291-312.
72. 72. Skoff R. P., Price D. L. and Stocks A. (1976) Electron microscopic autoradiographic studies of gliogenesis in rat optic nerve. J. comp. Neurol. 169, 313-334.
73. 73. Smith G. M., Miller R. H. and Silver J. (1986) Changing role of forebrain astrocytes during development, regenerative failure, and induced regeneration upon transplantation. J. comp. Neurol. 251, 23-43.
74. 74. Smith G. M., Rutishauser U., Silver J. and Miller R. H. (1990) Maturation of astrocytes in vitro alters the extent and molecular basis of neurite outgrowth. Dev. Biol. 138, 377-390.
75. 75. Sunde N. A. and Zimmer J. (1983) Cellular, histochemical and connective organization of the hippocampus and fascia dentata transplanted to different regions of immature and adult rat brains. Dev. Brain Res. 8, 165-191.
76. 76. Tessier-Lavigne M., Placzek M., Lumsden A. G. S., Dodd J. and Jessel T. M. (1988) Chemotropic guidance of developing axons in the mammalian nervous system. Nature 336, 775-778.
77. 77. Thanos S., Bähr M., Barde Y. and Vanselow J. (1989) Survival and axonal elongation of adult rat retinal ganglion cells. In vitro effects of lesioned sciatic nerve and brain derived neurotrophic factor. Eur. J. Neurosci. 1, 19-26.
78. 78. Tidow S., Struckhoff G., Mentlein R. and Sievers J. (1988) Growth of neuntes from retinal expiants of different ages: effects of media, substrates and the neurite elongation factor S-100β. In Sense Organs. (Abstr.) (eds Elsner N. and Barth F. G.), p. 347. Thieme, Stuttgart.
79. 79. Tidow S., Struckhoff G., Mentlein R. and Sievers J. (1989) Brain derived neurotrophic factor (BDNF) promotes the survival of adult retinal ganglion cells and stimulates the outgrowth of neurites from postnatal retinal explants. In Dynamics and Plasticity in the Neuronal Systems. (Abstr.) (eds Elsner N. and Singer W.), p. 203. Thieme, Stuttgart.
80. 80. Tidow S., Struckhoff G., Mentlein R. and Sievers J. (1990) Effect of cocultured astrocytes and astrocyte-conditioned media (ACM) on the regeneration of retinal axons in vitro. In Brain-Perception-Cognition. (Abstr.) (eds Elsner N. and Roth G.), p. 384. Thieme, Stuttgart.
81. 81. Tomaselli K. J., Reichardt L. F. and Bixby J. L. (1986) Distinct molecular interactions mediate neuronal process outgrowth on non-neuronal cell surfaces and extracellular matrices. J. Cell Biol. 103, 2659-2672.
82. 82. Unsicker K., Blottner D., Dreyer D., Grothe C., Lagrange A., Otto D. and Westermann R. (1990) Basic FGF and its implications for physiological and lesion-induced neuron death. In Regulation of Gene Expression in the Nervous System. (ed. Giuffrida-Stella A. M.), pp. 31-47. Wiley-Liss, New York.
83. 83. Vahlsing H. L., Hagg T., Spencer M., Conner J. M., Manthorpe M. and Varon S. (1991) Dose-dependent responses to nerve growth factor by adult rat cholinergic medial septum and neostriatum neurons. Brain Res. 552, 320-329.
84. 84. Varon S. and Bunge R. P. (1978) Trophic mechanisms in the peripheral nervous system. A. Rev. Neurosci. 1, 327-361.
85. 85. Varon S., Skaper S. D., Barbin G., Selak I. and Manthorpe M. (1984) Low molecular weight agents support survival of cultured neurons from the central nervous system. J. Neurosci. 4, 654-658.
86. 86. Xu X. M. and Martin G. F. (1991) Evidence for new growth and regeneration of cut axons in developmental plasticity of the rubrospinal tract in the North American opossum. J. comp. Neurol. 313, 103-112.