Abstract
Astroglial cells play an important role in orchestrating the migration and positioning of neurons during central nervous system development. Primary astroglia, as well as astrocytoma cells will extend long stable processes when co-cultured with granule neurons. In order to determine the function of the glial fibrillary acidic protein (GFAP), the major intermediate filament protein in astroglia and astrocytoma cells, we suppressed the expression of GFAP by stable transfection of an anti- sense GFAP construct in human astrocytoma U251MG cells. The resulting AS2-U251 cells can no longer extend stable processes in the presence of granule neurons. To show that this effect is due specifically to the absence of GFAP, we reintroduced a fully encoding rat brain GFAP cDNA into these AS2-U251 cells. The resulting rat GFAP appeared as a filamentous network and the reexpression of GFAP rescued the ability of these astrocytoma cells to form stable processes when co-cultured with neurons. From these results, it is clear that the glial specific intermediate filament protein, GFAP, is required for process extension of these astrocytoma cells in response to granule neurons.
Full Text
The Full Text of this article is available as a PDF (2.7 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Aletta J. M., Greene L. A. Growth cone configuration and advance: a time-lapse study using video-enhanced differential interference contrast microscopy. J Neurosci. 1988 Apr;8(4):1425–1435. doi: 10.1523/JNEUROSCI.08-04-01425.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Amaducci L., Forno K. I., Eng L. F. Glial fibrillary acidic protein in cryogenic lesions of the rat brain. Neurosci Lett. 1981 Jan 1;21(1):27–32. doi: 10.1016/0304-3940(81)90052-5. [DOI] [PubMed] [Google Scholar]
- Antonicek H., Persohn E., Schachner M. Biochemical and functional characterization of a novel neuron-glia adhesion molecule that is involved in neuronal migration. J Cell Biol. 1987 Jun;104(6):1587–1595. doi: 10.1083/jcb.104.6.1587. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Backhovens H., Gheuens J., Slegers H. Expression of glial fibrillary acidic protein in rat C6 glioma relates to vimentin and is independent of cell-cell contact. J Neurochem. 1987 Aug;49(2):348–354. doi: 10.1111/j.1471-4159.1987.tb02872.x. [DOI] [PubMed] [Google Scholar]
- Baorto D. M., Mellado W., Shelanski M. L. Astrocyte process growth induction by actin breakdown. J Cell Biol. 1992 Apr;117(2):357–367. doi: 10.1083/jcb.117.2.357. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bovolenta P., Liem R. K., Mason C. A. Development of cerebellar astroglia: transitions in form and cytoskeletal content. Dev Biol. 1984 Mar;102(1):248–259. doi: 10.1016/0012-1606(84)90189-1. [DOI] [PubMed] [Google Scholar]
- Bovolenta P., Liem R. K., Mason C. A. Glial filament protein expression in astroglia in the mouse visual pathway. Brain Res. 1987 May;430(1):113–126. doi: 10.1016/0165-3806(87)90181-7. [DOI] [PubMed] [Google Scholar]
- Browning E. T., Ruina M. Glial fibrillary acidic protein: norepinephrine stimulated phosphorylation in intact C-6 glioma cells. J Neurochem. 1984 Mar;42(3):718–726. doi: 10.1111/j.1471-4159.1984.tb02742.x. [DOI] [PubMed] [Google Scholar]
- Bulinski J. C., Borisy G. G. Immunofluorescence localization of HeLa cell microtubule-associated proteins on microtubules in vitro and in vivo. J Cell Biol. 1980 Dec;87(3 Pt 1):792–801. doi: 10.1083/jcb.87.3.792. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Caceres A., Kosik K. S. Inhibition of neurite polarity by tau antisense oligonucleotides in primary cerebellar neurons. Nature. 1990 Feb 1;343(6257):461–463. doi: 10.1038/343461a0. [DOI] [PubMed] [Google Scholar]
- Chen W. J., Liem R. K. The endless story of the glial fibrillary acidic protein. J Cell Sci. 1994 Aug;107(Pt 8):2299–2311. doi: 10.1242/jcs.107.8.2299. [DOI] [PubMed] [Google Scholar]
- Chin S. S., Liem R. K. Transfected rat high-molecular-weight neurofilament (NF-H) coassembles with vimentin in a predominantly nonphosphorylated form. J Neurosci. 1990 Nov;10(11):3714–3726. doi: 10.1523/JNEUROSCI.10-11-03714.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ching G. Y., Liem R. K. Assembly of type IV neuronal intermediate filaments in nonneuronal cells in the absence of preexisting cytoplasmic intermediate filaments. J Cell Biol. 1993 Sep;122(6):1323–1335. doi: 10.1083/jcb.122.6.1323. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ching G. Y., Liem R. K. Structure of the gene for the neuronal intermediate filament protein alpha-internexin and functional analysis of its promoter. J Biol Chem. 1991 Oct 15;266(29):19459–19468. [PubMed] [Google Scholar]
- Choi B. H., Lapham L. W. Radial glia in the human fetal cerebrum: a combined Golgi, immunofluorescent and electron microscopic study. Brain Res. 1978 Jun 16;148(2):295–311. doi: 10.1016/0006-8993(78)90721-7. [DOI] [PubMed] [Google Scholar]
- Chomczynski P., Sacchi N. Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem. 1987 Apr;162(1):156–159. doi: 10.1006/abio.1987.9999. [DOI] [PubMed] [Google Scholar]
- Dale R. M., McClure B. A., Houchins J. P. A rapid single-stranded cloning strategy for producing a sequential series of overlapping clones for use in DNA sequencing: application to sequencing the corn mitochondrial 18 S rDNA. Plasmid. 1985 Jan;13(1):31–40. doi: 10.1016/0147-619x(85)90053-8. [DOI] [PubMed] [Google Scholar]
- Edmondson J. C., Hatten M. E. Glial-guided granule neuron migration in vitro: a high-resolution time-lapse video microscopic study. J Neurosci. 1987 Jun;7(6):1928–1934. doi: 10.1523/JNEUROSCI.07-06-01928.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Edmondson J. C., Liem R. K., Kuster J. E., Hatten M. E. Astrotactin: a novel neuronal cell surface antigen that mediates neuron-astroglial interactions in cerebellar microcultures. J Cell Biol. 1988 Feb;106(2):505–517. doi: 10.1083/jcb.106.2.505. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fedoroff S., Ahmed I., Opas M., Kalnins V. I. Organization of microfilaments in astrocytes that form in the presence of dibutyryl cyclic AMP in cultures, and which are similar to reactive astrocytes in vivo. Neuroscience. 1987 Jul;22(1):255–266. doi: 10.1016/0306-4522(87)90216-8. [DOI] [PubMed] [Google Scholar]
- Feinstein D. L., Weinmaster G. A., Milner R. J. Isolation of cDNA clones encoding rat glial fibrillary acidic protein: expression in astrocytes and in Schwann cells. J Neurosci Res. 1992 May;32(1):1–14. doi: 10.1002/jnr.490320102. [DOI] [PubMed] [Google Scholar]
- Felgner P. L., Ringold G. M. Cationic liposome-mediated transfection. Nature. 1989 Jan 26;337(6205):387–388. doi: 10.1038/337387a0. [DOI] [PubMed] [Google Scholar]
- Gao W. Q., Hatten M. E. Neuronal differentiation rescued by implantation of Weaver granule cell precursors into wild-type cerebellar cortex. Science. 1993 Apr 16;260(5106):367–369. doi: 10.1126/science.8469990. [DOI] [PubMed] [Google Scholar]
- Gasser U. E., Hatten M. E. Central nervous system neurons migrate on astroglial fibers from heterotypic brain regions in vitro. Proc Natl Acad Sci U S A. 1990 Jun;87(12):4543–4547. doi: 10.1073/pnas.87.12.4543. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gasser U. E., Hatten M. E. Neuron-glia interactions of rat hippocampal cells in vitro: glial-guided neuronal migration and neuronal regulation of glial differentiation. J Neurosci. 1990 Apr;10(4):1276–1285. doi: 10.1523/JNEUROSCI.10-04-01276.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Goldberg D. J., Burmeister D. W. Microtubule-based filopodium-like protrusions form after axotomy. J Neurosci. 1992 Dec;12(12):4800–4807. doi: 10.1523/JNEUROSCI.12-12-04800.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Goldman J. E., Abramson B. Cyclic AMP-induced shape changes of astrocytes are accompanied by rapid depolymerization of actin. Brain Res. 1990 Oct 1;528(2):189–196. doi: 10.1016/0006-8993(90)91657-3. [DOI] [PubMed] [Google Scholar]
- Goldman J. E., Chiu F. C. Dibutyryl cyclic AMP causes intermediate filament accumulation and actin reorganization in astrocytes. Brain Res. 1984 Jul 23;306(1-2):85–95. doi: 10.1016/0006-8993(84)90358-5. [DOI] [PubMed] [Google Scholar]
- Goldmuntz E. A., Brosnan C. F., Chiu F. C., Norton W. T. Astrocytic reactivity and intermediate filament metabolism in experimental autoimmune encephalomyelitis: the effect of suppression with prazosin. Brain Res. 1986 Nov 5;397(1):16–26. doi: 10.1016/0006-8993(86)91365-x. [DOI] [PubMed] [Google Scholar]
- Harada A., Oguchi K., Okabe S., Kuno J., Terada S., Ohshima T., Sato-Yoshitake R., Takei Y., Noda T., Hirokawa N. Altered microtubule organization in small-calibre axons of mice lacking tau protein. Nature. 1994 Jun 9;369(6480):488–491. doi: 10.1038/369488a0. [DOI] [PubMed] [Google Scholar]
- Harrison B. C., Mobley P. L. Phorbol ester-induced change in astrocyte morphology: correlation with protein kinase C activation and protein phosphorylation. J Neurosci Res. 1990 Jan;25(1):71–80. doi: 10.1002/jnr.490250109. [DOI] [PubMed] [Google Scholar]
- Hatten M. E., Liem R. K., Mason C. A. Two forms of cerebellar glial cells interact differently with neurons in vitro. J Cell Biol. 1984 Jan;98(1):193–204. doi: 10.1083/jcb.98.1.193. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hatten M. E., Liem R. K., Mason C. A. Weaver mouse cerebellar granule neurons fail to migrate on wild-type astroglial processes in vitro. J Neurosci. 1986 Sep;6(9):2676–2683. doi: 10.1523/JNEUROSCI.06-09-02676.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hatten M. E., Mason C. A. Mechanisms of glial-guided neuronal migration in vitro and in vivo. Experientia. 1990 Sep 15;46(9):907–916. doi: 10.1007/BF01939383. [DOI] [PubMed] [Google Scholar]
- Hatten M. E. Neuronal inhibition of astroglial cell proliferation is membrane mediated. J Cell Biol. 1987 May;104(5):1353–1360. doi: 10.1083/jcb.104.5.1353. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hatten M. E. Neuronal regulation of astroglial morphology and proliferation in vitro. J Cell Biol. 1985 Feb;100(2):384–396. doi: 10.1083/jcb.100.2.384. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hatten M. E. Riding the glial monorail: a common mechanism for glial-guided neuronal migration in different regions of the developing mammalian brain. Trends Neurosci. 1990 May;13(5):179–184. doi: 10.1016/0166-2236(90)90044-b. [DOI] [PubMed] [Google Scholar]
- Kalnins V. I., Opas M., Ahmet I., Fedoroff S. Astrocyte cell lineage. IV. Changes in the organization of microfilaments and adhesion patterns during astrocyte differentiation in culture. J Neurocytol. 1984 Dec;13(6):867–882. doi: 10.1007/BF01148590. [DOI] [PubMed] [Google Scholar]
- Kretzschmar H. A., DeArmond S. J., Forno L. S. Measurement of GFAP in hepatic encephalopathy by ELISA and transblots. J Neuropathol Exp Neurol. 1985 Sep;44(5):459–471. doi: 10.1097/00005072-198509000-00002. [DOI] [PubMed] [Google Scholar]
- Lee K. F., Li E., Huber L. J., Landis S. C., Sharpe A. H., Chao M. V., Jaenisch R. Targeted mutation of the gene encoding the low affinity NGF receptor p75 leads to deficits in the peripheral sensory nervous system. Cell. 1992 May 29;69(5):737–749. doi: 10.1016/0092-8674(92)90286-l. [DOI] [PubMed] [Google Scholar]
- Levitt P., Rakic P. Immunoperoxidase localization of glial fibrillary acidic protein in radial glial cells and astrocytes of the developing rhesus monkey brain. J Comp Neurol. 1980 Oct 1;193(3):815–840. doi: 10.1002/cne.901930316. [DOI] [PubMed] [Google Scholar]
- Lewis S. A., Balcarek J. M., Krek V., Shelanski M., Cowan N. J. Sequence of a cDNA clone encoding mouse glial fibrillary acidic protein: structural conservation of intermediate filaments. Proc Natl Acad Sci U S A. 1984 May;81(9):2743–2746. doi: 10.1073/pnas.81.9.2743. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Liem R. K., Yen S. H., Salomon G. D., Shelanski M. L. Intermediate filaments in nervous tissues. J Cell Biol. 1978 Dec;79(3):637–645. doi: 10.1083/jcb.79.3.637. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lim R., Mitsunobu K., Li W. K. Maturation-stimulating effect of brain extract and dibutyryl cyclic AMP on dissociated embryonic brain cells in culture. Exp Eye Res. 1973 Apr;79(1):243–246. [PubMed] [Google Scholar]
- Mason C. A., Edmondson J. C., Hatten M. E. The extending astroglial process: development of glial cell shape, the growing tip, and interactions with neurons. J Neurosci. 1988 Sep;8(9):3124–3134. doi: 10.1523/JNEUROSCI.08-09-03124.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Mason C. A., Gregory E. Postnatal maturation of cerebellar mossy and climbing fibers: transient expression of dual features on single axons. J Neurosci. 1984 Jul;4(7):1715–1735. doi: 10.1523/JNEUROSCI.04-07-01715.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- McCarthy K. D., Prime J., Harmon T., Pollenz R. Receptor-mediated phosphorylation of astroglial intermediate filament proteins in cultured astroglia. J Neurochem. 1985 Mar;44(3):723–730. doi: 10.1111/j.1471-4159.1985.tb12875.x. [DOI] [PubMed] [Google Scholar]
- Melton D. A., Krieg P. A., Rebagliati M. R., Maniatis T., Zinn K., Green M. R. Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing a bacteriophage SP6 promoter. Nucleic Acids Res. 1984 Sep 25;12(18):7035–7056. doi: 10.1093/nar/12.18.7035. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Messens J., Slegers H. Synthesis of glial fibrillary acidic protein in rat C6 glioma in chemically defined medium: cyclic AMP-dependent transcriptional and translational regulation. J Neurochem. 1992 Jun;58(6):2071–2080. doi: 10.1111/j.1471-4159.1992.tb10948.x. [DOI] [PubMed] [Google Scholar]
- Mission J. P., Takahashi T., Caviness V. S., Jr Ontogeny of radial and other astroglial cells in murine cerebral cortex. Glia. 1991;4(2):138–148. doi: 10.1002/glia.440040205. [DOI] [PubMed] [Google Scholar]
- Murphy S., Pearce B. Functional receptors for neurotransmitters on astroglial cells. Neuroscience. 1987 Aug;22(2):381–394. doi: 10.1016/0306-4522(87)90342-3. [DOI] [PubMed] [Google Scholar]
- Napolitano E. W., Chin S. S., Colman D. R., Liem R. K. Complete amino acid sequence and in vitro expression of rat NF-M, the middle molecular weight neurofilament protein. J Neurosci. 1987 Aug;7(8):2590–2599. [PMC free article] [PubMed] [Google Scholar]
- Pinto-Lord M. C., Evrard P., Caviness V. S., Jr Obstructed neuronal migration along radial glial fibers in the neocortex of the reeler mouse: a Golgi-EM analysis. Brain Res. 1982 Aug;256(4):379–393. doi: 10.1016/0165-3806(82)90181-x. [DOI] [PubMed] [Google Scholar]
- Pollenz R. S., McCarthy K. D. Analysis of cyclic AMP-dependent changes in intermediate filament protein phosphorylation and cell morphology in cultured astroglia. J Neurochem. 1986 Jul;47(1):9–17. doi: 10.1111/j.1471-4159.1986.tb02824.x. [DOI] [PubMed] [Google Scholar]
- Pustell J., Kafatos F. C. A convenient and adaptable package of computer programs for DNA and protein sequence management, analysis and homology determination. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 2):643–655. doi: 10.1093/nar/12.1part2.643. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rakic P. Neuron-glia relationship during granule cell migration in developing cerebellar cortex. A Golgi and electronmicroscopic study in Macacus Rhesus. J Comp Neurol. 1971 Mar;141(3):283–312. doi: 10.1002/cne.901410303. [DOI] [PubMed] [Google Scholar]
- Rakic P., Sidman R. L. Sequence of developmental abnormalities leading to granule cell deficit in cerebellar cortex of weaver mutant mice. J Comp Neurol. 1973 Nov 15;152(2):103–132. doi: 10.1002/cne.901520202. [DOI] [PubMed] [Google Scholar]
- Rakic P., Stensas L. J., Sayre E., Sidman R. L. Computer-aided three-dimensional reconstruction and quantitative analysis of cells from serial electron microscopic montages of foetal monkey brain. Nature. 1974 Jul 5;250(461):31–34. doi: 10.1038/250031a0. [DOI] [PubMed] [Google Scholar]
- Sanger F., Coulson A. R., Barrell B. G., Smith A. J., Roe B. A. Cloning in single-stranded bacteriophage as an aid to rapid DNA sequencing. J Mol Biol. 1980 Oct 25;143(2):161–178. doi: 10.1016/0022-2836(80)90196-5. [DOI] [PubMed] [Google Scholar]
- Sariola H., Saarma M., Sainio K., Arumäe U., Palgi J., Vaahtokari A., Thesleff I., Karavanov A. Dependence of kidney morphogenesis on the expression of nerve growth factor receptor. Science. 1991 Oct 25;254(5031):571–573. doi: 10.1126/science.1658930. [DOI] [PubMed] [Google Scholar]
- Schnitzer J., Franke W. W., Schachner M. Immunocytochemical demonstration of vimentin in astrocytes and ependymal cells of developing and adult mouse nervous system. J Cell Biol. 1981 Aug;90(2):435–447. doi: 10.1083/jcb.90.2.435. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shafit-Zagardo B., Kume-Iwaki A., Goldman J. E. Astrocytes regulate GFAP mRNA levels by cyclic AMP and protein kinase C-dependent mechanisms. Glia. 1988;1(5):346–354. doi: 10.1002/glia.440010507. [DOI] [PubMed] [Google Scholar]
- Shain W., Forman D. S., Madelian V., Turner J. N. Morphology of astroglial cells is controlled by beta-adrenergic receptors. J Cell Biol. 1987 Nov;105(5):2307–2314. doi: 10.1083/jcb.105.5.2307. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sidman R. L., Rakic P. Neuronal migration, with special reference to developing human brain: a review. Brain Res. 1973 Nov 9;62(1):1–35. doi: 10.1016/0006-8993(73)90617-3. [DOI] [PubMed] [Google Scholar]
- Silver J., Lorenz S. E., Wahlsten D., Coughlin J. Axonal guidance during development of the great cerebral commissures: descriptive and experimental studies, in vivo, on the role of preformed glial pathways. J Comp Neurol. 1982 Sep 1;210(1):10–29. doi: 10.1002/cne.902100103. [DOI] [PubMed] [Google Scholar]
- Smith M. E., Eng L. F. Glial fibrillary acidic protein in chronic relapsing experimental allergic encephalomyelitis in SJL/J mice. J Neurosci Res. 1987;18(1):203–208. doi: 10.1002/jnr.490180129. [DOI] [PubMed] [Google Scholar]
- Smith M. E., Somera F. P., Eng L. F. Immunocytochemical staining for glial fibrillary acidic protein and the metabolism of cytoskeletal proteins in experimental allergic encephalomyelitis. Brain Res. 1983 Apr 4;264(2):241–253. doi: 10.1016/0006-8993(83)90822-3. [DOI] [PubMed] [Google Scholar]
- Stitt T. N., Hatten M. E. Antibodies that recognize astrotactin block granule neuron binding to astroglia. Neuron. 1990 Nov;5(5):639–649. doi: 10.1016/0896-6273(90)90218-5. [DOI] [PubMed] [Google Scholar]
- Streit A., Nolte C., Rásony T., Schachner M. Interaction of astrochondrin with extracellular matrix components and its involvement in astrocyte process formation and cerebellar granule cell migration. J Cell Biol. 1993 Feb;120(3):799–814. doi: 10.1083/jcb.120.3.799. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tardy M., Fages C., Rolland B., Bardakdjian J., Gonnard P. Effect of prostaglandins and dibutyryl cyclic AMP on the morphology of cells in primary astroglial cultures and on metabolic enzymes of GABA and glutamate metabolism. Experientia. 1981 Jan 15;37(1):19–21. doi: 10.1007/BF01965545. [DOI] [PubMed] [Google Scholar]
- Teng K. K., Greene L. A. Depolarization maintains neurites and priming of PC12 cells after nerve growth factor withdrawal. J Neurosci. 1993 Jul;13(7):3124–3135. doi: 10.1523/JNEUROSCI.13-07-03124.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tomaselli K. J., Neugebauer K. M., Bixby J. L., Lilien J., Reichardt L. F. N-cadherin and integrins: two receptor systems that mediate neuronal process outgrowth on astrocyte surfaces. Neuron. 1988 Mar;1(1):33–43. doi: 10.1016/0896-6273(88)90207-3. [DOI] [PubMed] [Google Scholar]
- Torres-Aleman I., Rejas M. T., Pons S., Garcia-Segura L. M. Estradiol promotes cell shape changes and glial fibrillary acidic protein redistribution in hypothalamic astrocytes in vitro: a neuronal-mediated effect. Glia. 1992;6(3):180–187. doi: 10.1002/glia.440060305. [DOI] [PubMed] [Google Scholar]
- Wang E., Cairncross J. G., Liem R. K. Identification of glial filament protein and vimentin in the same intermediate filament system in human glioma cells. Proc Natl Acad Sci U S A. 1984 Apr;81(7):2102–2106. doi: 10.1073/pnas.81.7.2102. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Weinstein D. E., Shelanski M. L., Liem R. K. C17, a retrovirally immortalized neuronal cell line, inhibits the proliferation of astrocytes and astrocytoma cells by a contact-mediated mechanism. Glia. 1990;3(2):130–139. doi: 10.1002/glia.440030207. [DOI] [PubMed] [Google Scholar]
- Weinstein D. E., Shelanski M. L., Liem R. K. Suppression by antisense mRNA demonstrates a requirement for the glial fibrillary acidic protein in the formation of stable astrocytic processes in response to neurons. J Cell Biol. 1991 Mar;112(6):1205–1213. doi: 10.1083/jcb.112.6.1205. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Westermark B. The deficient density-dependent growth control of human malignant glioma cells and virus-transformed glia-like cells in culture. Int J Cancer. 1973 Sep 15;12(2):438–451. doi: 10.1002/ijc.2910120215. [DOI] [PubMed] [Google Scholar]
- Williams R. W., Rakic P. Dispersion of growing axons within the optic nerve of the embryonic monkey. Proc Natl Acad Sci U S A. 1985 Jun;82(11):3906–3910. doi: 10.1073/pnas.82.11.3906. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Woolf T. M., Melton D. A., Jennings C. G. Specificity of antisense oligonucleotides in vivo. Proc Natl Acad Sci U S A. 1992 Aug 15;89(16):7305–7309. doi: 10.1073/pnas.89.16.7305. [DOI] [PMC free article] [PubMed] [Google Scholar]