Skip to main content
The American Journal of Pathology logoLink to The American Journal of Pathology
. 1989 Jan;134(1):115–132.

Neuroblastic Differentiation Potential of the Human Retinoblastoma Cell Lines Y-79 and WERI-Rb1 Maintained in an Organ Culture System

An Immunohistochemical, Electron Microscopic, and Biochemical Study

Mary M Herman, Elias Perentes, Christos D Katsetos, Françoise Darcel, Anthony Frankfurter, V Peter Collins, Larry A Donoso, Lawrence F Eng, Paul J Marangos, Allan F Wiechmann, Estelle E May, Christine B Thomas, Lucien J Rubinstein
PMCID: PMC1879546  PMID: 2643884

Abstract

The differentiation potential of the human retinoblastoma cell lines Y-79 and WERI-Rb 1 was evaluated in vitro for up to 120 days in a matrix system and in rotary suspension for 30 days. Matrix cultures were grown with 10% fetal calf serum (FCS), with and without differentiation-promoting agents. The latter were applied for a total of 5-45 days (usually 30 days) and included 7S nerve growth factor, dibutyryl cyclic AMP, sodium butyrate, retinoic acid, hydrocortisone, and ascorbic acid. Fully defined, serum-free medium and medium containing 5 or 15% FCS were also used for matrix cultures, and medium with 5 or 10% FCS for suspension cultures. By immunoperoxidase (performed on matrix cultures, both untreated and treated for 30 days with differentiation-promoting agents), the cells of both line were positive for neuron-specific enolase (NSE), microtubule-associated protein 2 (MAP2), class III β-tubulin (human hβ4) isotype, and synaptophysin. In addition, the WERI-Rb1 cells expressed 200 kd neurofilament protein (NFP-H) and retinal S-antigen. Both lines were invariably negative for glial fibrillary acidic (GFA) protein, myelin-associated glycoprotein, myelin basic protein, the epitope recognized by the Leu-7 monoclonal antibody, opsin, and hydroxyindole-0-methyltransferase. In the Y-79 line the presence of NSE and the absence of NF proteins-H, M and -L, of GFA protein, and of retinal S-antigen were confirmed biochemically. No differentiated features were found by electron microscopy in either line. Thus, in the matrix system employed, both lines exhibited solely a potential for neuroblastic differentiation, which was more advanced in the WERI-Rb1 line, as reflected by the antigenic expression of NFP-H and of retinal S-antigen.

Full text

PDF
115

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Artlieb U., Krepler R., Wiche G. Expression of microtubule-associated proteins, MAP-1 and MAP-2, in human neuroblastomas and differential diagnosis of immature neuroblasts. Lab Invest. 1985 Dec;53(6):684–691. [PubMed] [Google Scholar]
  2. BURTON K. A study of the conditions and mechanism of the diphenylamine reaction for the colorimetric estimation of deoxyribonucleic acid. Biochem J. 1956 Feb;62(2):315–323. doi: 10.1042/bj0620315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Barnes D., Sato G. Serum-free cell culture: a unifying approach. Cell. 1980 Dec;22(3):649–655. doi: 10.1016/0092-8674(80)90540-1. [DOI] [PubMed] [Google Scholar]
  4. Bennett G. S. Changes in intermediate filament composition during neurogenesis. Curr Top Dev Biol. 1987;21:151–183. doi: 10.1016/s0070-2153(08)60136-2. [DOI] [PubMed] [Google Scholar]
  5. Bernhardt R., Matus A. Initial phase of dendrite growth: evidence for the involvement of high molecular weight microtubule-associated proteins (HMWP) before the appearance of tubulin. J Cell Biol. 1982 Feb;92(2):589–593. doi: 10.1083/jcb.92.2.589. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bigner D. D., Bigner S. H., Pontén J., Westermark B., Mahaley M. S., Ruoslahti E., Herschman H., Eng L. F., Wikstrand C. J. Heterogeneity of Genotypic and phenotypic characteristics of fifteen permanent cell lines derived from human gliomas. J Neuropathol Exp Neurol. 1981 May;40(3):201–229. doi: 10.1097/00005072-198105000-00001. [DOI] [PubMed] [Google Scholar]
  7. Binder L. I., Frankfurter A., Kim H., Caceres A., Payne M. R., Rebhun L. I. Heterogeneity of microtubule-associated protein 2 during rat brain development. Proc Natl Acad Sci U S A. 1984 Sep;81(17):5613–5617. doi: 10.1073/pnas.81.17.5613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Bissell M. G., Eng L. F., Herman M. M., Bensch K. G., Miles L. E. Quantitative increase of neuroglia-specific GFA protein in rat C-6 glioma cells in vitro. Nature. 1975 Jun 19;255(5510):633–634. doi: 10.1038/255633a0. [DOI] [PubMed] [Google Scholar]
  9. Bottenstein J. E., Sato G. H. Growth of a rat neuroblastoma cell line in serum-free supplemented medium. Proc Natl Acad Sci U S A. 1979 Jan;76(1):514–517. doi: 10.1073/pnas.76.1.514. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Bäckström B., Collins V. P. Cytoskeletal changes in axons of rats exposed to 2,5-hexanediol, demonstrated using monoclonal antibodies. Neurotoxicology. 1987 Spring;8(1):85–96. [PubMed] [Google Scholar]
  11. Choux R., Tripier M. F., Bérard M., Hassoun J., Toga M. Ultrastructure d'une tumeur de la rétine. Bull Cancer. 1972 Apr-Jun;59(3):301–314. [PubMed] [Google Scholar]
  12. Craft J. L., Sang D. N., Dryja T. P., Brockhurst R. J., Robinson N. L., Albert D. M. Glial cell component in retinoblastoma. Exp Eye Res. 1985 May;40(5):647–659. doi: 10.1016/0014-4835(85)90134-4. [DOI] [PubMed] [Google Scholar]
  13. Cáceres A., Banker G. A., Binder L. Immunocytochemical localization of tubulin and microtubule-associated protein 2 during the development of hippocampal neurons in culture. J Neurosci. 1986 Mar;6(3):714–722. doi: 10.1523/JNEUROSCI.06-03-00714.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Dickson D. H., Ramsey M. S., Tonus J. G. Synapse formation in retinoblastoma tumours. Br J Ophthalmol. 1976 May;60(5):371–375. doi: 10.1136/bjo.60.5.371. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Donoso L. A., Felberg N. T., Augsburger J. J., Shields J. A. Retinal S-antigen and retinoblastoma: a monoclonal antibody and flow cytometric study. Invest Ophthalmol Vis Sci. 1985 Apr;26(4):568–571. [PubMed] [Google Scholar]
  16. Donoso L. A., Folberg R., Arbizo V. Retinal S antigen and retinoblastoma. A monoclonal antibody histopathologic study. Arch Ophthalmol. 1985 Jun;103(6):855–857. doi: 10.1001/archopht.1985.01050060115039. [DOI] [PubMed] [Google Scholar]
  17. Donoso L. A., Merryman C. F., Edelberg K. E., Naids R., Kalsow C. S-antigen in the developing retina and pineal gland: a monoclonal antibody study. Invest Ophthalmol Vis Sci. 1985 Apr;26(4):561–567. [PubMed] [Google Scholar]
  18. Dotti C. G., Banker G. A., Binder L. I. The expression and distribution of the microtubule-associated proteins tau and microtubule-associated protein 2 in hippocampal neurons in the rat in situ and in cell culture. Neuroscience. 1987 Oct;23(1):121–130. doi: 10.1016/0306-4522(87)90276-4. [DOI] [PubMed] [Google Scholar]
  19. Goto S., Matsukado Y., Mihara Y., Inoue N., Miyamoto E. An immunocytochemical demonstration of calcineurin in human nerve cell tumors. A comparison with neuron-specific enolase and glial fibrillary acidic protein. Cancer. 1987 Dec 15;60(12):2948–2957. doi: 10.1002/1097-0142(19871215)60:12<2948::aid-cncr2820601217>3.0.co;2-n. [DOI] [PubMed] [Google Scholar]
  20. Gould V. E., Lee I., Wiedenmann B., Moll R., Chejfec G., Franke W. W. Synaptophysin: a novel marker for neurons, certain neuroendocrine cells, and their neoplasms. Hum Pathol. 1986 Oct;17(10):979–983. doi: 10.1016/s0046-8177(86)80080-6. [DOI] [PubMed] [Google Scholar]
  21. Gould V. E., Wiedenmann B., Lee I., Schwechheimer K., Dockhorn-Dworniczak B., Radosevich J. A., Moll R., Franke W. W. Synaptophysin expression in neuroendocrine neoplasms as determined by immunocytochemistry. Am J Pathol. 1987 Feb;126(2):243–257. [PMC free article] [PubMed] [Google Scholar]
  22. Halks-Miller M., Henderson M., Eng L. F. Alpha tocopherol decreases lipid peroxidation, neuronal necrosis, and reactive gliosis in reaggregate cultures of fetal rat brain. J Neuropathol Exp Neurol. 1986 Jul;45(4):471–484. doi: 10.1097/00005072-198607000-00008. [DOI] [PubMed] [Google Scholar]
  23. Hart C. E., Nuckolls G. H., Wood J. G. Subcellular compartmentalization of phosphorylated neurofilament polypeptides in neurons. Cell Motil Cytoskeleton. 1987;7(4):393–403. doi: 10.1002/cm.970070411. [DOI] [PubMed] [Google Scholar]
  24. Herman M. M., Rubinstein L. J. Divergent glial and neuronal differentiation in a cerebellar medulloblastoma in an organ culture system: in vitro occurrence of synaptic ribbons. Acta Neuropathol. 1984;65(1):10–24. doi: 10.1007/BF00689823. [DOI] [PubMed] [Google Scholar]
  25. Hirokawa N., Glicksman M. A., Willard M. B. Organization of mammalian neurofilament polypeptides within the neuronal cytoskeleton. J Cell Biol. 1984 Apr;98(4):1523–1536. doi: 10.1083/jcb.98.4.1523. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Jiang Q., Lim R., Blodi F. C. Dual properties of cultured retinoblastoma cells: immunohistochemical characterization of neuronal and glial markers. Exp Eye Res. 1984 Aug;39(2):207–215. doi: 10.1016/0014-4835(84)90009-5. [DOI] [PubMed] [Google Scholar]
  27. Kivelä T., Tarkkanen A., Virtanen I. Intermediate filaments in the human retina and retinoblastoma. An immunohistochemical study of vimentin, glial fibrillary acidic protein, and neurofilaments. Invest Ophthalmol Vis Sci. 1986 Jul;27(7):1075–1084. [PubMed] [Google Scholar]
  28. Korf H. W., Foster R. G., Ekström P., Schalken J. J. Opsin-like immunoreaction in the retinae and pineal organs of four mammalian species. Cell Tissue Res. 1985;242(3):645–648. doi: 10.1007/BF00225432. [DOI] [PubMed] [Google Scholar]
  29. Kyritsis A. P., Tsokos M., Triche T. J., Chader G. J. Retinoblastoma--origin from a primitive neuroectodermal cell? Nature. 1984 Feb 2;307(5950):471–473. doi: 10.1038/307471a0. [DOI] [PubMed] [Google Scholar]
  30. Kyritsis A. P., Tsokos M., Triche T. J., Chader G. J. Retinoblastoma: a primitive tumor with multipotential characteristics. Invest Ophthalmol Vis Sci. 1986 Dec;27(12):1760–1764. [PubMed] [Google Scholar]
  31. Kyritsis A. P., Wiechmann A. F., Bok D., Chader G. J. Hydroxyindole-O-methyltransferase in Y-79 human retinoblastoma cells: effect of cell attachment. J Neurochem. 1987 May;48(5):1612–1616. doi: 10.1111/j.1471-4159.1987.tb05709.x. [DOI] [PubMed] [Google Scholar]
  32. Kyritsis A., Tsokos M., Chader G. Attachment culture of human retinoblastoma cells: long-term culture conditions and effects of dibutyryl cyclic AMP. Exp Eye Res. 1984 Apr;38(4):411–421. doi: 10.1016/0014-4835(84)90196-9. [DOI] [PubMed] [Google Scholar]
  33. LOWRY O. H., ROSEBROUGH N. J., FARR A. L., RANDALL R. J. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951 Nov;193(1):265–275. [PubMed] [Google Scholar]
  34. Lane J. C., Klintworth G. K. A study of astrocytes in retinoblastomas using the immunoperoxidase technique and antibodies to glial fibrillary acidic protein. Am J Ophthalmol. 1983 Feb;95(2):197–207. doi: 10.1016/0002-9394(83)90014-4. [DOI] [PubMed] [Google Scholar]
  35. Lee V., Trojanowski J. Q., Schlaepfer W. W. Induction of neurofilament triplet proteins in PC12 cells by nerve growth factor. Brain Res. 1982 Apr 22;238(1):169–180. doi: 10.1016/0006-8993(82)90779-x. [DOI] [PubMed] [Google Scholar]
  36. Liao C. L., Eng L. F., Herman M. M., Bensch K. G. Glial fibrillary acidic protein-solubility characteristics, relation to cell growth phases and cellular localization in rat C-6 glioma cells: an immunoradiometric and immunohistologic study. J Neurochem. 1978 May;30(5):1181–1186. doi: 10.1111/j.1471-4159.1978.tb12415.x. [DOI] [PubMed] [Google Scholar]
  37. Littauer U. Z., Zutra A., Rybak S., Ginzburg I. The expression of tubulin and various enzyme activities during neuroblastoma differentiation. Prog Clin Biol Res. 1985;175:193–208. [PubMed] [Google Scholar]
  38. MASTER R. W. POSSIBLE SYNTHESIS OF POLYRIBONUCLEOTIDES OF KNOWN BASE-TRIPLET SEQUENCES. Nature. 1965 Apr 3;206:93–93. doi: 10.1038/206093b0. [DOI] [PubMed] [Google Scholar]
  39. Marangos P. J., Schmechel D. E. Neuron specific enolase, a clinically useful marker for neurons and neuroendocrine cells. Annu Rev Neurosci. 1987;10:269–295. doi: 10.1146/annurev.ne.10.030187.001413. [DOI] [PubMed] [Google Scholar]
  40. Matus A., Bernhardt R., Hugh-Jones T. High molecular weight microtubule-associated proteins are preferentially associated with dendritic microtubules in brain. Proc Natl Acad Sci U S A. 1981 May;78(5):3010–3014. doi: 10.1073/pnas.78.5.3010. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. McFall R. C., Sery T. W., Makadon M. Characterization of a new continuous cell line derived from a human retinoblastoma. Cancer Res. 1977 Apr;37(4):1003–1010. [PubMed] [Google Scholar]
  42. Messmer E. P., Font R. L., Kirkpatrick J. B., Höpping W. Immunohistochemical demonstration of neuronal and astrocytic differentiation in retinoblastoma. Ophthalmology. 1985 Jan;92(1):167–173. doi: 10.1016/s0161-6420(85)34076-9. [DOI] [PubMed] [Google Scholar]
  43. Miettinen M., Rapola J. Synaptophysin--an immuno-histochemical marker for childhood neuroblastoma. Acta Pathol Microbiol Immunol Scand A. 1987 Jul;95(4):167–170. doi: 10.1111/j.1699-0463.1987.tb00026_95a.x. [DOI] [PubMed] [Google Scholar]
  44. Mirshahi M., Boucheix C., Dhermy P., Haye C., Faure J. P. Expression of the photoreceptor-specific S-antigen in human retinoblastoma. Cancer. 1986 Apr 15;57(8):1497–1500. doi: 10.1002/1097-0142(19860415)57:8<1497::aid-cncr2820570810>3.0.co;2-h. [DOI] [PubMed] [Google Scholar]
  45. Molnar M. L., Stefansson K., Marton L. S., Tripathi R. S., Molnar G. K. Immunohistochemistry of retinoblastomas in humans. Am J Ophthalmol. 1984 Mar;97(3):301–307. doi: 10.1016/0002-9394(84)90627-5. [DOI] [PubMed] [Google Scholar]
  46. Mørk S. J., May E. E., Papasozomenos S. C., Vinores S. A. Characteristics of human medulloblastoma cell line TE-671 under different growth conditions in vitro: a morphological and immunohistochemical study. Neuropathol Appl Neurobiol. 1986 May-Jun;12(3):277–289. doi: 10.1111/j.1365-2990.1986.tb00140.x. [DOI] [PubMed] [Google Scholar]
  47. Nakagawa Y., Perentes E., Rubinstein L. J. Immunohistochemical characterization of oligodendrogliomas: an analysis of multiple markers. Acta Neuropathol. 1986;72(1):15–22. doi: 10.1007/BF00687942. [DOI] [PubMed] [Google Scholar]
  48. Nishida T., Mukai N., Solish S. P., Pomeroy M. Effects of cyclic AMP on growth and differentiation of rat retinoblastoma-like tumor cells in vitro. Invest Ophthalmol Vis Sci. 1982 Feb;22(2):145–156. [PubMed] [Google Scholar]
  49. Parma A. M., Marangos P. J., Goodwin F. K. A more sensitive radioimmunoassay for neuron-specific enolase suitable for cerebrospinal fluid determinations. J Neurochem. 1981 Mar;36(3):1093–1096. doi: 10.1111/j.1471-4159.1981.tb01704.x. [DOI] [PubMed] [Google Scholar]
  50. Perentes E., Herbort C. P., Rubinstein L. J., Herman M. M., Uffer S., Donoso L. A., Collins V. P. Immunohistochemical characterization of human retinoblastomas in situ with multiple markers. Am J Ophthalmol. 1987 May 15;103(5):647–658. doi: 10.1016/s0002-9394(14)74324-7. [DOI] [PubMed] [Google Scholar]
  51. Perentes E., Rubinstein L. J. Immunohistochemical recognition of human nerve sheath tumors by anti-Leu 7 (HNK-1) monoclonal antibody. Acta Neuropathol. 1985;68(4):319–324. doi: 10.1007/BF00690835. [DOI] [PubMed] [Google Scholar]
  52. Perentes E., Rubinstein L. J. Recent applications of immunoperoxidase histochemistry in human neuro-oncology. An update. Arch Pathol Lab Med. 1987 Sep;111(9):796–812. [PubMed] [Google Scholar]
  53. Popoff N. A., Ellsworth R. M. The fine structure of retinoblastoma. In vivo and in vitro observations. Lab Invest. 1971 Nov;25(5):389–402. [PubMed] [Google Scholar]
  54. Reid T. W., Albert D. M., Rabson A. S., Russell P., Craft J., Chu E. W., Tralka T. S., Wilcox J. L. Characteristics of an established cell line of retinoblastoma. J Natl Cancer Inst. 1974 Aug;53(2):347–360. doi: 10.1093/jnci/53.2.347. [DOI] [PubMed] [Google Scholar]
  55. Rodrigues M. M., Wilson M. E., Wiggert B., Krishna G., Chader G. J. Retinoblastoma. A clinical, immunohistochemical, and electron microscopic case report. Ophthalmology. 1986 Aug;93(8):1010–1015. doi: 10.1016/s0161-6420(86)33630-3. [DOI] [PubMed] [Google Scholar]
  56. Rubinstein L. J., Herman M. M., Foley V. L. In vitro characteristics of human glioblastomas maintained in organ culture systems. Light microscopy observations. Am J Pathol. 1973 Apr;71(1):61–80. [PMC free article] [PubMed] [Google Scholar]
  57. Sawa H., Takeshita I., Kuramitsu M., Fukui M., Inomata H. Immunohistochemistry of retinoblastomas. J Neurooncol. 1987;5(4):351–355. doi: 10.1007/BF00148392. [DOI] [PubMed] [Google Scholar]
  58. Schwechheimer K., Wiedenmann B., Franke W. W. Synaptophysin: a reliable marker for medulloblastomas. Virchows Arch A Pathol Anat Histopathol. 1987;411(1):53–59. doi: 10.1007/BF00734514. [DOI] [PubMed] [Google Scholar]
  59. Sipe J. C., Rubinstein L. J., Herman M. M., Bignami A. Ethylnitrosourea-induced astrocytomas. Morphologic observations on rat tumors maintained in tissue and organ culture systems. Lab Invest. 1974 Dec;31(6):571–579. [PubMed] [Google Scholar]
  60. Steck A. J., Murray N., Vandevelde M., Zurbriggen A. Human monoclonal antibodies to myelin-associated glycoprotein. Comparison of specificity and use for immunocytochemical localisation of the antigen. J Neuroimmunol. 1983 Oct;5(2):145–156. doi: 10.1016/0165-5728(83)90005-x. [DOI] [PubMed] [Google Scholar]
  61. Sternberger L. A., Hardy P. H., Jr, Cuculis J. J., Meyer H. G. The unlabeled antibody enzyme method of immunohistochemistry: preparation and properties of soluble antigen-antibody complex (horseradish peroxidase-antihorseradish peroxidase) and its use in identification of spirochetes. J Histochem Cytochem. 1970 May;18(5):315–333. doi: 10.1177/18.5.315. [DOI] [PubMed] [Google Scholar]
  62. Subden R. E., Krizus A. Correction factors for the diphenylamine test for deoxyribonucleic acid in yeasts. Microbios. 1985;43(176S):233–243. [PubMed] [Google Scholar]
  63. Sullivan K. F., Cleveland D. W. Identification of conserved isotype-defining variable region sequences for four vertebrate beta tubulin polypeptide classes. Proc Natl Acad Sci U S A. 1986 Jun;83(12):4327–4331. doi: 10.1073/pnas.83.12.4327. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Sun C. N. Abnormal mitochondria in retinoblastoma. Experientia. 1976 May 15;32(5):630–632. doi: 10.1007/BF01990204. [DOI] [PubMed] [Google Scholar]
  65. Taylor H. R., Carroll N., Jack I., Crock G. W. A scanning electron microscopic examination of retinoblastoma in tissue culture. Br J Ophthalmol. 1979 Aug;63(8):551–559. doi: 10.1136/bjo.63.8.551. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Terenghi G., Polak J. M., Ballesta J., Cocchia D., Michetti F., Dahl D., Marangos P. J., Garner A. Immunocytochemistry of neuronal and glial markers in retinoblastoma. Virchows Arch A Pathol Anat Histopathol. 1984;404(1):61–73. doi: 10.1007/BF00704251. [DOI] [PubMed] [Google Scholar]
  67. Trojanowski J. Q., Friedman H. S., Burger P. C., Bigner D. D. A rapidly dividing human medulloblastoma cell line (D283 MED) expresses all three neurofilament subunits. Am J Pathol. 1987 Feb;126(2):358–363. [PMC free article] [PubMed] [Google Scholar]
  68. Ts'o M. O., Fine B. S., Zimmerman L. E. The Flexner-Wintersteiner rosettes in retinoblastoma. Arch Pathol. 1969 Dec;88(6):664–671. [PubMed] [Google Scholar]
  69. Ts'o M. O., Fine B. S., Zimmerman L. E. The nature of retinoblastoma. II. Photoreceptor differentiation: an electron microscopic study. Am J Ophthalmol. 1970 Mar;69(3):350–359. doi: 10.1016/0002-9394(70)92264-6. [DOI] [PubMed] [Google Scholar]
  70. Tsokos M., Kyritsis A. P., Chader G. J., Triche T. J. Differentiation of human retinoblastoma in vitro into cell types with characteristics observed in embryonal or mature retina. Am J Pathol. 1986 Jun;123(3):542–552. [PMC free article] [PubMed] [Google Scholar]
  71. VandenBerg S. R., May E. E., Rubinstein L. J., Herman M. M., Perentes E., Vinores S. A., Collins V. P., Park T. S. Desmoplastic supratentorial neuroepithelial tumors of infancy with divergent differentiation potential ("desmoplastic infantile gangliogliomas"). Report on 11 cases of a distinctive embryonal tumor with favorable prognosis. J Neurosurg. 1987 Jan;66(1):58–71. doi: 10.3171/jns.1987.66.1.0058. [DOI] [PubMed] [Google Scholar]
  72. Vinores S. A., Bonnin J. M., Rubinstein L. J., Marangos P. J. Immunohistochemical demonstration of neuron-specific enolase in neoplasms of the CNS and other tissues. Arch Pathol Lab Med. 1984 Jul;108(7):536–540. [PubMed] [Google Scholar]
  73. Virtanen I., Kivelä T., Bugnoli M., Mencarelli C., Pallini V., Albert D. M., Tarkkanen A. Expression of intermediate filaments and synaptophysin show neuronal properties and lack of glial characteristics in Y79 retinoblastoma cells. Lab Invest. 1988 Nov;59(5):649–656. [PubMed] [Google Scholar]
  74. Watanabe T., Raff M. C. Retinal astrocytes are immigrants from the optic nerve. Nature. 1988 Apr 28;332(6167):834–837. doi: 10.1038/332834a0. [DOI] [PubMed] [Google Scholar]
  75. Wiechmann A. F., Bok D., Horwitz J. Localization of hydroxyindole-O-methyltransferase in the mammalian pineal gland and retina. Invest Ophthalmol Vis Sci. 1985 Mar;26(3):253–265. [PubMed] [Google Scholar]
  76. Wiedenmann B., Franke W. W. Identification and localization of synaptophysin, an integral membrane glycoprotein of Mr 38,000 characteristic of presynaptic vesicles. Cell. 1985 Jul;41(3):1017–1028. doi: 10.1016/s0092-8674(85)80082-9. [DOI] [PubMed] [Google Scholar]
  77. Wiedenmann B., Franke W. W., Kuhn C., Moll R., Gould V. E. Synaptophysin: a marker protein for neuroendocrine cells and neoplasms. Proc Natl Acad Sci U S A. 1986 May;83(10):3500–3504. doi: 10.1073/pnas.83.10.3500. [DOI] [PMC free article] [PubMed] [Google Scholar]
  78. Willard M., Simon C. Antibody decoration of neurofilaments. J Cell Biol. 1981 May;89(2):198–205. doi: 10.1083/jcb.89.2.198. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Zackroff R. V., Idler W. W., Steinert P. M., Goldman R. D. In vitro reconstitution of intermediate filaments form mammalian neurofilament triplet polypeptides. Proc Natl Acad Sci U S A. 1982 Feb;79(3):754–757. doi: 10.1073/pnas.79.3.754. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The American Journal of Pathology are provided here courtesy of American Society for Investigative Pathology

RESOURCES