Inactivation of bcl-2 results in progressive degeneration of motoneurons, sympathetic and sensory neurons during early postnatal development

Neuron

Volumn 17, Issue 1, 1996, Pages 75-89

  Michaelidis, T M ^a   Sendtner, M ^b   Cooper, J D ^a   Airaksinen, M S ^a   Holtmann, B ^a   Meyer, M ^a   Thoenen, H ^a  

^a MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

^b UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; CILIARY NEUROTROPHIC FACTOR; DNA; ONCOPROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL SURVIVAL; EMBRYO; GENE ACTIVATION; GENE DISRUPTION; GENE EXPRESSION; GENE LOCUS; MOTONEURON; MOUSE; NERVE CELL DEGENERATION; NERVE CELL NECROSIS; NERVE FIBER TRANSECTION; NEUROPROTECTION; NEWBORN; NONHUMAN; PHENOTYPE; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTO ONCOGENE; SENSORY NERVE CELL; SYMPATHETIC NERVE CELL; TRANSGENIC MOUSE;

EID: 1842456916     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(00)80282-2     Document Type: Article

References (92)

1. Abe-Dohmae, S., Harada, N., Yamada, K., and Tanaka, R. (1993). Bcl-2 gene is highly expressed during neurogenesis in the central nervous system. Biochem. Biophys. Res. Commun. 191, 915-921.
2. Allsopp, T.E., Wyatt, S., Paterson, H.F., and Davies A.M. (1993). The proto-oncogene bcl-2 can selectively rescue neurotrophic factor-dependent neurons from apoptosis. Cell 73, 295-307.
3. Allsopp, T.E., Kiselev S., Wyatt S., and Davies, A.M. (1995). Role of Bcl-2 in the brain-derived neurotrophic factor survival response. Eur. J. Neurosci. 7, 1266-1272.
4. Ashwell, K.W. (1982). The adult mouse facial nerve nucleus: morphology and musculotopic organization. J. Anat. 135, 531-538.
5. Ashwell, K.W., and Watson, C.R.R. (1983). The development of facial motoneurons in the mouse: neuronal death and the innervation of the facial muscle cells. J. Embryol. Exp. Morph. 77, 117-141.
6. Bakhshi, A., Jensen, J.P., Goldman, P., Wright, J.J., McBride, O.W., Epstein, A.L., and Korsmeyer, S.J. (1985). Cloning the chromosomal breakpoint of t(14;18) human lymphomas: clustering around JH on chromosome 14 and near a transcriptional unit on 18. Cell 41, 899-906.
7. Barde, Y.-A. (1989). Trophic factors and neuronal survival. Neuron 2, 1525-1534.
8. Boise, L.H., Gonzalez-Garcia, M., Postema, C.E., Ding, L., Lindsten, T., Turka, L.A., Mao, X., Nuñez, G., and Thompson, C.B. (1993). bcl-x a bcl-2-related gene that functions as a dominant regulator of apoptotic cell death. Cell 74, 597-608.
9. Borasio, G.D., Markus, A., Wittinghofer, A., Barde, Y.-A, and Heumann, R. (1993). Involvement of ras p21 in neurotrophin-induced response of sensory but not sympathetic neurons. J. Cell Biol. 121, 665-672.
10. Bothwell, M. (1995). Functional interactions of neurotrophins and neurotrophin receptors. Annu. Rev. Neurosci. 18, 223-253.
11. Bradford, M.M. (1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72, 248-254.
12. Chao, M.V. (1992). Neurotrophin receptors: a window into neuronal differentiation. Neuron 9, 583-593.
13. Chao, M.V., and Hempstead, B.L. (1995). p75 and Trk: a two-receptor system. Trends Neurosci. 18, 321-326.
14. Chleq-Deschamps, C.M., LeBrun, D.P., Bensier, D.P., Warnke, R.A., Sibley, R.K., and Cleary, M.L. (1993). Topographical dissociation of bcl-2 messenger RNA and protein expression in human lymphoid tissues. Blood 81, 293-298.
15. Cleary, M.L., Smith, S.D., and Sklar, J. (1986). Cloning and structural analysis of cDNAs for bcl-2 and a hybrid bcl-2 immunoglobulintranscript resulting from the t(14;18) translocation. Cell 47, 19-28.
16. Crews, L.L., and Wigston, D.J. (1990). The dependence of motoneurons on their target muscle during postnatal development of the mouse. J. Neurosci. 10, 1643-1653.
17. Coggeshall, R.E., Pover, C.M., and Fitzgerald, M. (1994). Dorsal root ganglion cell death and surviving cell numbers in relation to the development of sensory innervation in the rat hindlimb. Dev. Brain Res. 82, 193-212.
18. Conover, J.C., Erickson, J.T., Katz, D.M., Bianchi, L.M., Poueymirou, W.T., McClain, J., Pan, L., Helgren, M., Ip, N.Y., Boland, P., Friedman, B., Wiegand, S., Vejsada, R., Kato, A.C., DeChiara, T.M., and Yancopoulos, G.D. (1995). Neuronal deficits, not involving motor neurons, in mice lacking BDNF and/or NT4. Nature 375, 235-238.
19. Crowley, C., Spencer, S.D., Nishimura, M.C., Chen, K.S., Pitts-Meek, S., Armanini, M.P., Ling, L.H., McMahon, S.B., Shelton, D.L., Levinson, A.D., and Phillips, H.S. (1994). Mice lacking nerve growth factor display perinatal loss of sensory and sympathetic neurons yet develop basal forebrain cholinergic neurons. Cell 76, 1001-1011.
20. Davies, A.M. (1994). The role of neurotrophins in the developing nervous system. J. Neurobiol. 25, 1334-1348.
21. De Bilbao, F., and Dubois-Dauphin, M. (1996). Time course of axotomy-induced apoptotic cell death in facial motoneurons of neonatal wild-type and bcl-2 transgenic mice. Neuroscience, 71, 1111-1119.
22. Dubois-Dauphin, M., Frankowski, H., Tsujimoto, Y., Huarte, J., and Martinou, J.C. (1994). Neonatal motoneurons overexpressing the bcl-2 protooncogene in transgenic mice are protected from axotomy-induced cell death. Proc. Natl. Acad. Sci. USA 97, 3309-3313.
23. Ellis, R.E., Yuan, J., and Horvitz, H.R. (1991). Mechanisms and functions of cell death. Annu. Rev. Cell Biol. 7, 663-698.
24. Ernfors, P., Lee, K.-F., Kucera, J., and Jaenisch, R. (1994). Lack of neurotrophin-3 leads to deficiencies in the peripheral nervous system and loss of limb proprioceptive afferents. Cell 77, 503-512.
25. Fariñas, I., Jones, K.R., Backus, C., Wang, X.-Y., and Reichardt, L.F. (1994). Severe sensory and sympathetic deficits in mice lacking neurotrophin-3. Nature 369, 658-661.
26. Farlie, P.G., Dringen, R., Rees, S.M., Kannourakis, G., and Bernard O. (1995). bcl-2 transgene expression can protect neurons against developmental and induced cell death. Proc. Natl. Acad. Sci. USA 92, 4397-4401.
27. Frankowski, H., Missotten, M., Fernandez, P.-A., Michel, P., Sadoul, R., and Martinou J.-C. (1995). Function and expression of the Bcl-x gene in the developing and adult nervous system. Neuroreport 6, 1917-1921.
28. Garcia, I., Martinou, I., Tsujimoto, Y., and Martinou, J.C. (1992). Prevention of programmed cell death of sympathetic neurons by the bcl-2 proto-oncogene. Science 258, 302-304.
29. Gillardon, F., Wickert, H., and Zimmermann, M. (1995). Up-regulation of bax and down-regulation of bcl-2 is associated with kainate-induced apoptosis in mouse brain. Neurosci. Lett. 192, 85-88.
30. Gonzáles-García, M., García, I., Ding, L., O'Shea S., Boise, L.H., Thompson, C.B., and Nuñez, G. (1995). bcl-x is expressed in embryonic and postnatal neural tissues and functions to prevent neuronal cell death. Proc. Natl. Acad. Sci. USA 92, 4304-4308.
31. Greenlund, L.J. S, Korsmeyer, S.J., and Johnson, E.M., Jr. (1995). Role of Bcl-2 in the survival and function of developing and mature sympathetic neurons. Neuron 15, 649-661.
32. Hara, A., Iwai, T., Niwa, M., Uematsu, T., Yoshimi, N., Tanaka, T., and Mori, H. (1996). Immunohistochemical detection of Bax and Bcl-2 proteins in gerbil hippocampus following transient forebrain ischemia. Brain Res. 711, 249-253.
33. Hefti, F. (1994). Neurotrophic factor therapy for nervous system degenerative diseases. J. Neurobiol. 25, 1418-1435.
34. Henderson, C.E., Camu, W., Mettling, C., Gouin, A., Poulson, K., Karihaloo, M., Rullamas, J., Evans, T., McMahon, S.B., Armanini, M.P., Berkemeier, L.R., Phillips, H.S., and Rosenthal, A. (1993). Neurotrophins promote motor neuron survival and are present in embryonic limb bud. Nature 363, 266-270.
35. Hockenbery, D., Nuñes, G., Milliman, C., Schreiber, R.D., and Korsmeyer, S.J. (1990). Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature 348, 334-336.
36. Hockenbery, D.M., Zutter, M., Hickey, W., Nahm, M., and Korsmeyer, S. J. (1991). BCL2 protein is topographically restricted in tissues characterized by apoptotic cell death. Proc. Natl. Acad. Sci. USA 88, 6961-6965.
37. Hughes, R.A., Sendtner, M., and Thoenen, H. (1993). Members of several gene families influence survival of rat motoneurons in vitro and in vivo. Neurosci. Res. 36, 663-671.
38. Johnson, E.M., Jr., and Deckwerth, T.L. (1993). Molecular mechanisms of developmental neuronal death. Annu. Rev. Neurosci. 16, 31-46.
39. Jones, K.R., Fariñas, Backus C., and Reichardt, L.F. (1994). Targeted disruption of the BDNF gene perturbs brain and sensory neuron development but not motor neuron development. Cell 76, 989-999.
40. Koliatsos, V.E., Clatterbuck, R.E., Winslow, J.W., Cayouette, M.H., and Price, D.L. (1993). Evidence that brain-derived neurotrophic factor is a trophic factor for motor neurons in vivo. Neuron 10, 359-367.
41. Koliatsos, V.E., Cayouette, M.H., Berkemeier, L.F., Clatterbuck, R.E., Price D.L., and Rosenthal, A. (1994). Neurotrophin 4/5 is a trophic factor for mammalian facial motoneurons. Proc. Natl. Acad. Sci. USA 91, 3304-3308.
42. Kondo, E., Nakamura, S., Onoue, H., Matsuo, Y., Yoshito, T., Aoki, H., Hayashi, K., Takahashi, K., Minowada, J., Nomura, S., and Akagi, T. (1992). Detection of bcl-2 protein and bcl-2 messenger RNA in normal and neoplastic lymphoid tissues by immunohistochemistry and in situ hybridization. Blood 80, 2044-2051.
43. Kou, S.-Y., Chiu, A.Y., and Patterson, P.H. (1995). Differential regulation of motor neuron survival and choline acetyltransferase expression following axotomy. J. Neurobiol. 27, 561-572.
44. Kozopas, K.M., Yang, T., Buchan, H.L., Zhou, P., and Earnshaw, W.C. (1993). MCL1, a gene expressed in programmed myeloid cell differentiation, has sequence similarity to BCL2. Proc. Natl. Acad. Sci. USA 90, 3516-3520.
45. Krajewski, S., Krajewska, M., Shabaik, A., Miyashita, T., Wang, H.G., and Reed, J.C. (1994). Immunohistochemical determination of in vivo distribution of Bax, a dominant inhibitor of Bcl-2. Am. J. Pathol. 145, 1323-1336.
46. Krajewski, S., Mai, J.K., Krajewska, M., Sikorska, M., Mossakowski, M.J., and Reed, J.C. (1995). Upregulation of Bax protein levels in neurons following cerebral ischemia. J. Neurosci. 15, 6364-6376.
47. Kreutzberg, G.W. (1986). The Facial Nerve, M. May, ed. (New York: Thieme), pp. 75-83.
48. Laemmli, U.K. (1970). Cleavage of structural proteins during assembly of the head of bacteriophage T4. Nature 227, 680-685.
49. Lawson, S.N. (1992). Morphological and biochemical cell types of sensory neurons. In Sensory Neurons: Diversity, Development, and Plasticity, S.A. Scott, ed. (New York: Oxford University Press), pp. 27-59.
50. Le Mouellic, H., Lallemand, Y., and Brûlet, P. (1992). Homeosis in the mouse induced by a null mutation in the Hox-3.1 gene. Cell 69, 251-264.
51. Levi-Montalcini, R. (1987). The nerve growth factor 35 years later. Science 237, 1154-1162.
52. Lewin, G.R., and Barde, Y.-A. (1996). Physiology of the neurotrophins. Annu. Rev. Neurosci. 19, 289-317.
53. Li, L., Oppenheim, R.W., Lei, M., and Houenou, L.J. (1994). Neurotrophic agents prevent motoneuron death following sciatic nerve section in the neonatal mouse. J. Neurobiol. 25, 759-766.
54. Lin, E.Y., Orlofsky, A., Berger, M.S., and Prystowski, M.B. (1993). Characterization of A1, a novel hemopoietic-specific early response gene with sequence similarity to Bcl-2. J. Immunol. 151, 1979-1988.
55. Lindsay, R.M., Wiegand, S.J., Altar, C.A., and DiStefano, P.S. (1994). Neurotrophic factors: from molecule to man. Trends Neurosci. 17, 182-189.
56. Liu, X., Ernfors, P., Wu, H., and Jaenisch, R. (1995). Sensory but not motor neuron deficits in mice lacking NT4 and BDNF. Nature 375, 238-241.
57. Mah, S.P., Zhong, L.T., Liu, Y., Roghani, A., Edwards, R.H., and Bredesen, D.E. (1993). The protooncogene bcl-2 inhibits apoptosis in PC12 cells. J. Neurochem. 60, 1183-1186.
58. Martinou, J.C., Dubois-Dauphin, M., Staple, J.K., Rodriguez, I., Frankowski, H., Missotten, M., Albertini, P., Talabot, D., Catsicas, S., Pietra, C., and Huarte, J. (1994). Overexpression of BCL-2 in transgenic mice protects neurons from naturally occurring cell death and experimental ischemia. Neuron 13, 1017-1030.
59. Meakin, S.O., and Shooter, E.M. (1992). The nerve growth factor family of receptors. Trends Neurosci. 15, 323-331.
60. 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.
61. Motoyama, N., Wang, F., Roth, K.A., Sawa, H., Nakayama, K.-i., Nakayama, K., Negishi, I., Senju, S., Zhang, Q., Fujii, S., and Loh, D.Y. (1995). Massive cell death of immature hematopoietic cells and neurons in Bcl-x-deficient mice. Science 267, 1506-1510.
62. Nakayama, K., Nakayama, K.-i., Negishi, I., Keisuke K., Sawa H., and Loh, D.Y. (1994). Targeted disruption of Bcl-2αβ in mice: occurrence of gray hair, polycystic kidney disease, and lymphocytopenia. Proc. Natl. Acad. Sci. USA 97, 3700-3704.
63. Negrini, M., Silini, E., Kozak, C., Tsujimoto, Y., and Croce, C.M. (1987). Molecular analysis of mbcl-2: structure and expression of the murine gene homologous to the human gene involved in follicular lymphoma. Cell 49, 455-463.
64. Nobes, C.D., and Tolkovsky, A.M. (1995). Neutralising Anti-p21ras Fabs suppress rat sympathetic neuron survival induced by NGF, LIF, CNTF and cAMP. Eur. J. Neurosci. 7, 344-350.
65. Nobes, C.D., Reppas, J.B., Markus, A., and Tolkovsky, A.M. (1996). Active p21RAS is sufficient for rescue of NGF-dependent rat sympathetic neurons. Neuroscience 70, 1067-1079.
66. Nuñez, G., London, L., Hockenbery, D., Alexander, M., McKearn, J.P., and Korsmeyer, S.J. (1990). Deregulated Bcl-2 gene expression selectively prolongs survival of growth factor deprived hematopoietic cell lines. J. Immunol. 144, 3602-3610.
67. Ohga, Y., Zirrgiebel, U., Hamnér, S., Michaelidis, M.T., Cooper, J., Thoenen, H., and Lindholm, D. (1996). Cell density increases Bcl-2 and Bcl-x expression in addition to survival of cultured cerebellar granule neurons. Neuroscience 73, 913-917.
68. Oltvai, Z.N., Milliman, C.L., and Korsmeyer, S.J. (1993). Bcl-2 heterodimerizes in vivo with a conserved homolog, bax, that accelerates programed cell death. Cell 74, 609-619.
69. Oppenheim, R.W., Haverkamp, L.J., Prevette, D., McManaman, J.L., and Appel, S.H. (1988). Reduction of naturally occuring motoneuron death in vivo by a target-derived neurotrophic factor. Science 240, 919-921.
70. Oppenheim, R.W. (1991). Cell death during development of the nervous system. Annu. Rev. Neurosci. 14, 453-501.
71. Oppenheim, R.W., Qin-Wei, Y., Prevette, D., and Yan, Q. (1992). Brain-derived neurotrophic factor rescues developing avian motoneurons from cell death. Nature 360, 755-757.
72. Pollin, M.M., McHanwell, S., and Slater, C.R. (1991). The effect of age on motor neurone death following axotomy in the mouse. Development 112, 83-89.
73. Raff, M.C. (1992). Social controls on cell survival and death: an extreme view. Nature 356, 397-400.
74. Rudnicki, M.A., Braun, T., Hinuma, S., and Jaenisch, R. (1992). Inactivation of MyoD in mice leads to up-regulation of the myogenic HLH gene Myf-5 and results in apparently normal muscle development. Cell 71, 383-390.
75. Sambrook, J., Frisch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, Second Edition (Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press).
76. Schmalbruch, H. (1984). Motoneuron death after sciatic nerve section in newborn rats. J. Comp. Neurol. 224, 252-258.
77. Sendtner, M., Kreutzberg, G.W., and Thoenen, H. (1990). Ciliary neurotrophic factor prevents the degeneration of motor neurons after axotomy. Nature 345, 440-441.
78. Sendtner, M., Holtmann, B., Kolbeck, R., Thoenen, H., and Barde, Y.-A. (1992a). Brain-derived neurotrophic factor prevents the death of motoneurons in newborn rats after nerve section. Nature 360, 757-758.
79. Siegel, R.M., Katsumata, M., Miyashita, T., Louie, D.C., Green, M.I., and Reed, J.C. (1992). Inhibition of thymocyte apoptosis and negative antigenic selection in Bcl-2 transgenic mice. Proc. Natl. Acad. Sci. USA 89, 7003-7007.
80. Silos-Santiago, I., Molliver, D.C., Ozaki, S., Smeyne, R.J., Fagan, A.M., Barbacid, M., and Snider, W.D. (1995). Non-TrkA-expressing small DRG neurons are lost in TrkA deficient mice. J. Neurosci. 15, 5929-5942.
81. Snider, W.D., Elliott, J.L., and Yan, Q. (1992). Axotomy-induced neuronal death during development. J. Neurobiol. 23, 1231-1246.
82. Snider, W.D. (1994). Functions of the neurotrophins during nervous system development: what the knockouts are teaching us. Cell 77, 627-638.
83. Southern, E.M. (1975). Detection of specific sequences among DNA fragments separated by gel electrophoresis. J. Mol. Biol. 98, 503-517.
84. Thoenen, H., Castrén, E., Berzaghi, M., Blöchl, A., and Lindholm, D. (1994). Neurotrophic factors: possibilities and limitations in the treatment of neurodegenerative disorders. In Acad. Biomed. Drug Res. Volume 7 (Basel: Karger), pp. 197-203.
85. Thoenen, H., Hughes, R.A., and Sendtner, M. (1993). Trophic support of motoneurons: physiological, pathophysiological, and therapeutic implications. Exp. Neurol. 724, 47-55.
86. Tsujimoto, Y., Finger, L.R., Tunis, J., Nowell, P.C., and Croce, C.M. (1984). Cloning of the chromosomic breakpoint of neoplastic B cells with the t(14;18) chromosome translocation. Science 226, 1097-1099.
87. Tzimagiorgis, G., Michaelidis, T.M., Lindholm, D., and Thoenen, H. (1996). Introduction of the negative selection marker into replacement by a single ligation step. Nucl. Acids Res., in press.
88. Veis, D.J., Sorenson, C.M., Shutter, J.R., and Korsmeyer, S.J. (1993). Bcl-2-deficient mice demonstrate fulminant lymphoid apoptosis, polycystic kidneys, and hypopigmented hair. Cell 75, 229-240.
89. Wright, L.L., Cunninham, T.J., and Smolen, A.J. (1983). Developmental neuron death in the rat superior cervical sympathetic ganglion: cell counts and ultrastructure. J. Neurocytol. 12, 727-738.
90. Yan, Q., Elliott, J., and Snider, W.D. (1992). Brain-derived neurotrophic factor rescues spinal motor neurons from axotomy-induced cell death. Nature 360, 753-755.
91. L and Bcl-2, displaces Bax and promotes cell death. Cell 80, 285-291.
92. Young, R.L., and Korsmeyer, S.J. (1993). A negative regulatory element in the bcl-2 5′-untranslated region inhibits expression from an upstream promoter. Mol. Cell. Biol. 13, 3686-3697.