Retinoic acid induces apoptosis-associated neural differentiation of a murine teratocarcinoma cell line

Journal of Neurochemistry

Volumn 70, Issue 1, 1998, Pages 47-58

  Herget, Thomas ^a   Specht, Heike ^a   Esdar, Christina ^a   Oehrlein, Silke A ^a   Maelicke, Alfred ^a  

^a JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

Apoptosis; Neurogenesis; Protein kinase C; Retinoic acid; Stem cells

Indexed keywords

BENZYLOXYCARBONYL VALINYL ALANINYL ASPARTYL FLUOROMETHYL KETONE; CASPASE INHIBITOR; CISPLATIN; GLUTAMIC ACID; MESYLIC ACID ETHYL ESTER; NEUROMODULIN; PROTEIN KINASE C; RETINOIC ACID; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DIFFERENTIATION; CHROMATIN CONDENSATION; CONTROLLED STUDY; DNA DEGRADATION; EMBRYO; GENE EXPRESSION REGULATION; GENE INDUCTION; MOUSE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TERATOCARCINOMA;

ANIMALIA; MURINAE;

EID: 0031972626     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1998.70010047.x     Document Type: Article

References (66)

1. Alnemri E. S., Livingston D. J., Nicholson D. W., Salvesen G., Thornberry N. A., Wong W. W., and Yuan J. (1996) Human ICE/CED-3 protease nomenclature. Cell 87, 171.
2. Arenas E. and Persson P. (1994) Neurotrophin-3 prevents the death of adult central noradrenergic neurons in vivo. Nature 367, 368-370.
3. Batistatou A. and Greene L. A. (1991) Aurintricarboxylic acid rescues PC12 cells and sympathetic neurons from cell death caused by nerve growth factor deprivation: correlation with suppression of endonuclease activity. J. Cell Biol. 115, 461-471.
4. Behrens M. M., Martinez J. C., Moratilla C., and Renart J. (1995) Apoptosis induced by protein kinase C inhibition in a neuroblastoma cell line. Cell Growth Diff. 6, 1375-1380.
5. Berger C., Reinhardt S., Rentrop M., Bachmann M., Weiser T., Link E., Wienrich M., Jahn R., and Maelicke A. (1997) De novo acquisition of neuronal polarity. Eur. J. Cell Biol. (in press).
6. Blaschke A. J., Staley K., and Chun J. (1996) Widespread programmed cell death in proliferative and postmitotic regions of the fetal cerebral cortex. Development 122, 1165-1174.
7. Bredesen D. E. (1995) Neural apoptosis. Ann. Neurol. 38, 839-851.
8. Cano E. and Mahadevan L. (1995) Parallel signal processing among mammalian MAPKs. Trends Biochem. Sci. 20, 117-122.
9. Clifford J., Chiba H., Sobieszczuk D., Metzger D., and Chambon P. (1996) RXRalpha-null F9 embryonal carcinoma cells are resistant to the differentiation, anti-proliferative and apoptotic effects of retinoids. EMBO J. 15, 4142-4155.
10. Cohen J. J. (1993) Apoptosis. Immunol. Today 14, 126-130.
11. Couldwell W. T., Hinton D. R., He S., Chen T. C., Sebat I., Weiss M. H., and Law R. E. (1994) Protein kinase C inhibitors induce apoptosis in human malignant glioma cell lines. FEBS Lett. 345, 43-46.
12. Dolle P., Fraulob P., Kastner P., and Chambon P. (1994) Developmental expression of murine retinoid X receptor (RXR) genes. Mech. Dev. 45, 91-104.
13. Edwards S. N., Buckmaster A. E., and Tolkovsky A. M. (1991) The death programme in cultured sympathetic neurones can be suppressed at the posttranslational level by nerve growth factor, cyclic AMP, and depolarization. J. Neurochem. 57, 2140-2143.
14. Faucheau C., Diu A., Chan A. W., Blanchet A.-M., Miossec C., Herve F., Collard-Dutilleul V., Gu Y., Aldape R. A., Lippke J. A., Rocher C., Su M. S.-S., Livingston D. J., Hercend T., and Lalanne J.-L. (1995) A novel human protease similar to the interleukin-1 beta converting enzyme induces apoptosis in transfected cells. EMBO J. 14, 1914-1922.
15. Gavrieli Y., Sherman Y., and Ben-Sasson S. A. (1992) Identification of programmed cell death in situ via specific labeling of nuclear DNA fragments. J. Cell Biol. 119, 493-501.
16. Goslin K. and Banker G. (1990) Rapid changes in the distribution of GAP-43 correlate with the expression of neuronal polarity during normal development and under experimental conditions. J. Cell Biol. 110, 1331-1339.
17. Gschwendt M., Dieterich S., Rennecke J., Kittstein W., Mueller H.-J. and Johannes F.-J. (1996) Inhibition of protein kinase C μ by various inhibitors. Differentiation from protein kinase C isoenzymes. FEBS Lett. 392, 77-80.
18. Gurfinkel N., Unger T., Givol D., and Mushinsi J. F. (1987) Expression of the bcl-2 gene in mouse B lymphocytic cell lines is differentiation stage specific. Eur. J. Immunol. 17, 567-570.
19. Hanada M., Krajewski S., Tanaka S., Cazals-Hatem D., Spengler B. A., Ross R. A., Biedler J. L., and Reed J. C. (1993) Regulation of Bcl-2 oncoprotein levels with differentiation of human neuroblastoma cells. Cancer Res. 53, 4978-4986.
20. Heiermann R., Lang E., Rentrop M., and Maelicke A. (1992) Expression of retinoic acid nuclear receptors in the mouse embryonal carcinoma cell line PCC7-Mz1. FEBS Lett. 312, 75-79.
21. Herget T. and Rozengurt E. (1994) Bombesin, endothelin, and platelet-derived growth factor induce rapid translocation of the myristoylated alanine-rich C-kinase substrate 80K/MARCKS in Swiss 3T3 cells. Eur. J. Biochem. 225, 539-548.
22. Herget T., Reich M., Stüber K., and Starzinski-Powitz A. (1986) Regulated expression of repetitive sequences including the identifier sequence during myotube formation in culture. EMBO J. 5, 659-664.
23. 0. Proc. Natl. Acad. Sci. USA 90, 2945-2949.
24. Herget T., Oehrlein S. A., Pappin D. J. C., Rozengurt E., and Parker P. J. (1995) The myristoylated alanine-rich C kinase substrate (MARCKS) is sequentially phosphorylated by conventional, novel and atypical isotypes of protein kinase C. Eur. J. Biochem. 233, 448-457.
25. Hogan B. L. M., Thaller C., and Eichele G. (1992) Evidence that Hensen's node is a site of retinoic acid synthesis. Nature 359, 237-241.
26. Ikemoto H., Tani E., Matsumoto T., Nakano A., and Furuyama J. (1995) Apoptosis of human glioma cells in response to calphostin C, a specific protein kinase C inhibitor. J. Neurosurg. 83, 1008-1016.
27. Ishizaki Y., Burne J. F., and Raff M. C. (1994) Autocrine signals enable chondrocytes to survive in culture. J. Cell Biol. 126, 1069-1077.
28. Jacobson M. D., Weil M., and Raff M. C. (1996) Role of Ced-3/ICE-family proteases in staurosporine-induced programmed cell death. J. Cell Biol. 133, 1041-1051.
29. Jacobson M. D., Weil M., and Raff M. C. (1997) Programmed cell death in animal development. Cell 88, 347-354.
30. Kaufmann S. H., Desnoyers S., Ottaviano Y., Davidson N. E., and Poirier G. G. (1993) Specific proteolytic cleavage of poly (ADP-ribose) polymerase: an early marker of chemotherapy-induced apoptosis. Cancer Res. 53, 3976-3985.
31. Kumar S. (1995) ICE-like proteases in apoptosis. Trends Biochem. Sci. 20, 198-202.
32. Kure S., Tominaga T., Yoshimoto T., Tada K., and Narisawa K. (1991) Glutamate triggers internucleosomal DNA cleavage in neuronal cells. Biochem. Biophys. Res. Commun. 179, 39-45.
33. Kyriakis J. M., App H., Zhang X. F., Banerjee P., Brautigan D. L., Rapp U. R., and Avruch J. (1992) Raf-1 activates MAP kinase-kinase. Nature 358, 417-421.
34. Lang E., Mazauric-Stüker M.-L., and Maelicke A. (1989) States of developmental commitments of a mouse embryonal carcinoma cell line differentiating along a neural pathway. J. Cell Biol. 109, 2481-2493.
35. Leithäuser F., Dhein J., Mechtersheimer G., Koretz K., Brüderlein S., Henne C. Schmidt A., Debatin K.-M., Krammer P. H., and Müller P. (1993) Constitutive and induced expression of APO-1, a new member of the nerve growth factor/tumor necrosis factor receptor superfamily, in normal and neoplastic cells. Lab. Invest. 69, 415-429.
36. Loo D. T., Copani A., Pike C. J., Whittemore E. R., Walencewicz A. J., and Cotman C. W. (1993) Apoptosis is induced by β-amyloid in cultured central nervous system neurons. Proc. Natl. Acad. Sci. USA 90, 7951-7955.
37. Lucas M. and Sanchez-Margalet V. (1995) Protein kinase C involvement in apoptosis. Gen. Pharmacol. 26, 881-887.
38. Mailhos C., Howard M. K., and Latchman D. S. (1994) A common pathway mediates retinoic acid and PMA-dependent programmed cell death (apoptosis) of neuronal cells. Brain Res. 644, 7-12.
39. Marshall N. J., Goodwin C. J., and Holt S. J. (1995) A critical assessment of the use of microculture tetrazolium assays to measure cell growth and function. Growth Regul. 5, 69-84.
40. Martin S. J. and Green D. R. (1995) Protease activation during apoptosis: death by a thousand cuts? Cell 82, 349-352.
41. Martiny-Baron G., Kazanietz M. G., Mischak H., Blumberg P. M., Kochs G., Hug H., Marme D., and Schächtele C. (1993) Selective inhibition of protein kinase C isozymes by the indolocarbazole Gö 6976. J. Biol. Chem. 268, 9194-9197.
42. Merry D. E., Veis D. J., Hickey W. F., and Korsmeyer S. J. (1994) Bcl-2 protein expression is widespread in the developing nervous system and retained in the adult PNS. Development 120, 301-311.
43. Mesner P. W., Winters T. R., and Green S. H. (1992) Nerve growth factor withdrawal-induced cell death in neuronal PC12 cells resembles that in sympathetic neurons. J. Cell Biol. 119, 1669-1680.
44. Mosmann T. (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods 65, 55-63.
45. Müller-Husmann G., Reinhardt S., Stähle M., Lang E., and Maelicke A. (1994) EX-1, a cell surface antigen of mouse neuronal progenitor cells and mature neurons. Dev. Brain Res. 83, 262-277.
46. Nagata S. (1997) Apoptosis by death factor. Cell 88, 355-365.
47. Nishizuka Y. (1992) Intracellular signaling by hydrolysis of phospholipids and activation of protein kinase C. Science 258, 607-614.
48. Oehrlein S. A., Parker P. J., and Herget T. (1996) Phosphorylation of GAP-43 (growth-associated protein of 43 kDa) by conventional, novel and atypical isotypes of the protein kinase C gene family: differences between oligopeptide and polypeptide phosphorylation. Biochem. J. 317, 219-224.
49. Ojeda F., Folch H., Guarda M. I., Jastorff B., and Diehl H. A. (1995) Induction of apoptosis in thymocytes: new evidence for an interaction of PKC and PKA pathways. Biol. Chem. Hoppe Seyler 376, 389-393.
50. Okazawa H., Shimizu J., Kamei M., Imafuku I., Hamada H., and Kanazawa I. (1996) Bcl-2 inhibits retinoic acid-induced apoptosis during the neural differentiation of embryonal stem cells. J. Cell Biol. 132, 955-968.
51. Oppenheim R. W. (1991) Cell death during development of the nervous system. Annu. Rev. Neurosci. 14, 453-501.
52. Paulin D., Jakob H., Jacob F., Weber K., and Osborn M. (1982) In vitro differentiation of mouse teratocarcinoma cells monitored by intermediate filament expression. Differentiarion 22, 90-99.
53. Pfeiffer S. E., Jakob H., Mikoshiba K., Dubois P., Guenet J. L., Nicolas J.-F., Gaillard J., Chevance G., and Jacob F. (1981) Differentiation of a teratocarcinoma line: preferential development of cholinergic neurons. J. Cell Biol. 88, 57-66.
54. Raff M. C. (1992) Social controls on cell survival and cell death. Nature 356, 397-400.
55. Raff M. C., Barres B. A., Burne J. F., Cole H. S., Ishizaki Y., and Jacobson M. D. (1993) Programmed cell death and the control of cell survival: lessons from the nervous system. Science 262, 695-700.
56. Reed J. C. (1994) Bcl-2 and the regulation of programmed cell death. J. Cell Biol. 124, 1-6.
57. Ruberte E., Friedrich V., Chambon P., and Morriss-Kay G. (1993) Retinoic acid receptors and cellular retinoid binding proteins. III. Their differential transcript distribution during mouse nervous system development. Development 118, 267-282.
58. Schnell L., Schneider R., Kolbeck R., Barde Y.-A., and Schwab M. E. (1994) Neurotrophin-3 enhances sprouting of corticospinal tract during development and after adult spinal cord lesion. Nature 367, 170-172.
59. Selvakumaran M., Lin H. K., Miyashita T., Wang H. G., Krajewski S., Reed J. C., Hoffman B., and Liebermann D. (1994) Immediate early up-regulation of bax expression by p53 but not TGF beta 1: a paradigm for distinct apoptotic pathways. Oncogene 9, 1791-1798.
60. Shortman K., Egerton M., Spangrude G. J., and Scollay R. (1990) The generation and fate of thymocytes. Semin. Immunol. 2, 3-12.
61. Smith C. A., Williams G. T., Kingston R., Jenkinson E. J., and Owen J. J. T. (1989) Antibodies to CD3/T-cell receptor complex induce death by apoptosis in immature T cells in thymic cultures. Nature 337, 181-184.
62. Surh C. D. and Sprent J. (1994) T-cell apoptosis detected in situ during positive and negative selection in the thymus. Nature 372, 100-103.
63. Vekrellis K., McCarthy M. J., Watson A., Whitfield J., Rubin L. L., and Ham J. (1997) Bax promotes neural cell death and is down-regulated during the development of the nervous system. Development 124, 1239-1249.
64. White E. (1996) Life, death, and the pursuit of apoptosis. Genes Dev. 10, 1-15.
65. Yan Q., Elliott J., and Snider W. D. (1992) Brain-derived neurotrophic factor rescues spinal motor neurons from axotomy-induced cell death. Nature 360, 753-754.
66. Zhang K.-Z., Westberg J. A., Hölttä E., and Andersson L. C. (1996) BCL2 regulates neural differentiation. Proc. Natl. Acad. Sci. USA 93, 4504-4508.