Development in the absence of skeletal muscle results in the sequential ablation of motor neurons from the spinal cord to the brain

Developmental Biology

Volumn 208, Issue 1, 1999, Pages 93-109

  Kablar, Boris ^a   Rudnicki, Michael A ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

Apoptosis; Motor neuron; Myf 5; MyoD; Pyramidal cell; Type Ia afferent

Indexed keywords

MYOGENIC FACTOR;

APOPTOSIS; ARTICLE; FACIAL NERVE NUCLEUS; INTERNEURON; MOTONEURON; MOUSE; MUSCLE DEVELOPMENT; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; SENSORY NERVE CELL;

EID: 0033120177     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.1998.9184     Document Type: Article

References (71)

1. Abercrombie, M. (1946). Estimation of the nuclear population from microtome sections. Anat. Rec. 94, 239-247.
2. Brennan, T. J., Olson, E. N., Klein, W. H., and Winslow, J. W. (1996). Extensive motor neuron survival in the absence of secondary skeletal muscle fiber formation. J. Neurosci. Res. 45, 57-68.
3. Clarke, P. G. H. (1993). An unbiased correction factor for cell counts in histological sections. J. Neurosci. Methods 49, 133-140.
4. Cotran, R. S. (1994). In "Robbins Pathologic Basis of Disease" (R. S. Cotran, S. L. Robbins, and V. Kumar, Eds.), 5th ed., p. 1336. Saunders, Philadelphia.
5. Daunicht, W. J., Jaworski, E., and Eckmiller, R. (1985). Afferent innervation of extraocular muscles in the rat studied by retrograde and anterograde horseradish peroxidase transport. Neurosci. Lett. 56, 143-148.
6. Ericson, J., Thor, S., Edlund, T., Jessell, T. M., and Yamada, T. (1992). Early stages of motor neuron differentiation revealed by expression of homeobox gene Islet-1. Science 256, 1555-1560.
7. Ericson, J., Morton, S., Kawakami, A., Roelink, H., and Jessell, T. M. (1996). Two critical periods of Sonic hedgehog signaling required for the specification of motor neuron identity. Cell 87, 661-673.
8. Ericson, J., Rashbass, P., Schedl, A., Brenner-Morton, S., Kawakami, A., van Heyningen, V., Jessell, T. M., and Briscoe, J. (1997). Pax6 controls progenitor cell identity and neuronal fate in response to graded Shh signaling. Cell 90, 169-180.
9. Ernfors, P., and Persson, H. (1991). Developmentally regulated expression of HDNF/NT-3 mRNA in rat spinal cord motoneurons and detection of BDNF mRNA in embryonic dorsal root ganglion. Eur. J. Neurosci. 3, 953-961.
10. Ernfors, P., Lee, K.-F., Kucera, J., and Jaenish, R. (1994). Lack of neurotrophin-3 leads to deficiencies in the peripheral nervous system and loss of limb proprioceptive afferents. Cell 77, 503-512.
11. Fan, C. H., and Tessier-Lavigne, M. (1994). Patterning of mammalian somites by surface ectoderm and notochord: Evidence for sclerotome induction by a hedgehog homologue. Cell 79, 1175-1186.
12. Gavrieli, Y., Sherman, Y., and Ben-Sasson, S. A. (1992). Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. J. Cell Biol. 119, 493-501.
13. Grieshammer, U., Lewandoski, M., Prevette, D., Oppenheim, R. W., and Martin, G. R. (1998). Muscle-specific cell ablation conditional upon Cre-mediated DNA recombination in transgenic mice leads to massive spinal and cranial motoneuron loss. Dev. Biol. 197, 234-247.
14. Hamburger, V., and Oppenheim, R. W. (1982). Naturally-occurring neuronal death in vertebrates. Neurosci. Comment. 1, 38-55.
15. Hauschka, S. D. (1994). The Embryonic Origin of Muscle. In "Myology" (A. G. Engel and C. Franzini-Armstrong, Eds.), 2nd ed., pp. 3-73. McGraw-Hill, New York.
16. Henderson, C. E., Camu, W., Mettling, C., Govin, A., Poulsen, K., Karihaloo, M., Rullamas, J., Evans, T., McMahon, S. B., and Armanini, M. T. (1993). Neurotrophins promote motor neuron survival and are present in embryonic limb bud. Nature 363, 213-214.
17. Henderson, C. E., Phillips, H. S., Pollock, R. A., Davies, A. M., Lemeulle, C., Armanini, M., Simmons, L., Moffet, B., Vandlen, R. A., Koliatsos, V. E., and Rosenthal, A. (1994). GDNF: A potent survival factor for motoneurons present in peripheral nerve and muscle. Science 266, 1062-1064.
18. Hollyday, M., and Hamburger, V. (1977). An autoradiographic study of the formation of the lateral motor column in the chick embryo. Brain Res. 132, 197-208.
19. Hollyday, M. (1980). Motoneuron histogenesis and the development of limb innervation. Curr. Topics Dev. Biol. 15, 181-215.
20. Jacquin, T. D., Borday, V., Schneider-Maunoury, M., Topilko, P., Ghilini, G., Kato, F., Charnay, P., and Champagnat, J. (1996). Reorganization of pontine rhythmogenic neuronal networks in Krox-20 knockout mice. Neuron 17, 747-758.
21. Jessell, T. M., and Goodman, C. S. (1996). Neural development: Are there any surprises left? Curr. Opin. Neurobiol. 6, 1-2.
22. Kaufman, M. H. (1992). "The Atlas of Mouse Development." Academic Press, London.
23. Klein, R., Silos-Santiago, I., Smeyne, R. J., Lira, S. A., Brambilla, R., Bryant, S., Zhang, L., Snider, W. D., and Barbacid, M. (1994). Disruption of the neurotrophin-3 receptor gene trkC eliminates Ia muscle afferents and results in abnormal movements. Nature 368, 249-251.
24. 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.
25. Kucera, J., and Warlo, J. M. (1992). Superfluousness of motor innervation for the formation of muscle spindles in neonatal rats. Anat Embryol. (Berlin) 186, 301-309.
26. Laird, P. W., Zijderveld, A., Linders, K., Rudnicki, M. A., Jaenish, R., and Berns, A. (1991). Simplified mammalian DNA isolation procedure. Nucleic Acids Res. 19, 4293.
27. Lance-Jones, C. J. (1982). Motoneuron cell death in the developing lumbar spinal cord of the mouse. Dev. Brain Res. 4, 473-479.
28. Lance-Jones, C. J. (1986). Motoneuron projection patterns in chick embryonic limbs with a double complement of dorsal thigh musculature. Dev. Biol. 116, 387-406.
29. Lawson, S. J., Davies, H. J., Bennett, J. P., and Lowrie, M. B. (1997). Evidence that spinal interneurons undergo programmed cell death postnatally in the rat. Eur. J. Neurosci. 9, 794-799.
30. Lewis, J., Chevallier, A., Kieny, M., and Wolpert, L. (1981). Muscle nerve branches do not develop in chick wings devoid of muscle. Embryol. Exp. Morphol. 64, 211-232.
31. Lieberman, A. R. (1976). Sensory ganglia. In "The Peripheral Nerve" (D. N. Landon, Ed.), pp. 188-278. Chapman and Hall, London.
32. Lowe, J., and Cox, G. (1990). Neuropathological techniques. In "Theory and Practise of Histological Techniques" (J. O. Bancroft and A. Stevens, Eds.), pp. 343-378. Churchill Livingstone, Edinburgh.
33. Marin-Padilla, M. (1970). Prenatal and early postnatal ontogenesis of the human motor cortex: A Golgi study. I. The sequential development of the cortical layers. Brain Res. 23, 167-183.
34. Matise, M. P., and Joyner, A. L. (1997). Expression pattern of developmental control genes in normal and Engrailed-1 mutant mouse spinal cord reveals early diversity in developing interneurons. J. Neurosci. 17, 7805-7816.
35. McKay, S. E., and Oppenheim, R. W. (1991). Lack of evidence for cell death among avian spinal cord interneurons during normal development and following removal of targets and afferents. J. Neurobiol. 22, 721-733.
36. Megeney, L. A., and Rudnicki, M. A. (1995). Determination versus differentiation and the MyoD family of transcription factors. Biochem. Cell Biol. 73, 723-732.
37. Mettling, C., Camus, W., and Henderson, C. E. (1993). Embryonic wing and leg motoneurons have intrinsically different survival properties. Development 118, 1149-1156.
38. Oakley, R. A., Lefcort, F. B., Clary, D. O., Reichardt, L. F., Prevette, D., Oppenheim, R. W., and Frank, E. (1997). Neurotrophin-3 promotes the differentiation of muscle spindle afferents in the absence of peripheral targets. J. Neurosci. 17, 4246-4274.
39. Oppenheim, R. W. (1981). Cell death of motoneurons in the chick embryo spinal cord. V. Evidence on the role of cell death and neuromuscular function in the formation of specific peripheral connections. J. Neurosci. 1, 141-151.
40. Oppenheim, R. W., Houenou, L., Pincon-Raymond, M., Powell, J. A., Rieger, F., and Standish, L. J. (1986). The development of motoneurons in the embryonic spinal cord of the mouse mutant, muscular dysgenesis (mdg/mdg): Survival, morphology, and biochemical differentiation. Dev. Biol. 114, 426-436.
41. Oppenheim, R. W. (1991). Cell death during development of the nervous system. Annu. Rev. Neurosci. 14, 453-501.
42. Oppenheim, R. W., Prevette, D., Yin, Q.-W., Collins, F., and MacDonald, J. (1991). Control of embryonic motoneuron survival in vivo by ciliary neurotrophic factor. Science 251, 1616-1618.
43. Oppenheim, R. W., Yin, Q.-W., Prevette, D., and Yan, Q. (1992). Brain-derived neurotrophic factor rescues developing avian motoneurons from cell death. Nature 360, 755-757.
44. Oppenheim, R. W., Houenou, L. J., Johnson, J. E., Lin, L.-F. H., Li, L., Lo, A. C., Newsome, A. L., Prevette, D. M., and Wang, S. (1995). Developing motoneurons rescued from programmed and axotomy-induced cell death by GDNF. Nature 373, 344-346.
45. Oppenheim, R. W. (1996). Neurotrophic survival molecules for motoneurons: An embarrassment of riches. Neuron 17, 195-197.
46. Pettorossi, V. E., Ferraresi, A., Draicchio, F., Errico, P., Santarelli, R., and Manni, E. (1995). Extraocular muscle proprioception and eye position. Acta Otolaryngol. (Stockholm) 115, 137-140.
47. Pfaff, S. L., Mendelsohn, M., Stewart, C. L., Edlund, T., and Jessell, T. M. (1996). Requirement for LIM homeobox gene Isll in motor neuron generation reveals a motor neuron-dependent step in interneuron differentiation. Cell 84, 309-320.
48. Phelan, K. A., and Hollyday, M. (1990). Axon guidance in muscleless chick wings: The role of muscle cells in motoneuronal pathway selection and muscle nerve formation. J. Neurosci. 10, 2699-2716.
49. Ringstedt, T., Kucera, J., Lendahl, U., Ernfors, P., and Ibáñez, C. F. (1997). Limb proprioceptive deficits without neuronal loss in transgenic mice overexpressing neurotrophin-3 in the developing nervous system. Development 124, 2603-2613.
50. Roelink, H., Porter, J. A., Chiang, C., Tanabe, Y., Chang, D. T., Beachy, P. A., and Jessell, T. M. (1995). Floor plate and motor neuron induction by different concentrations of the amino-terminal cleavage product of Sonic hedgehog autoproteolysis. Cell 81, 445-455.
51. Roelink, H. (1996). Tripartite signaling of pattern: Interactions between hedgehogs, MBPs and Wnts in the control of vertebrate development. Curr. Opin. Neurobiol. 6, 33-40.
52. Rudnicki, M. A., Schnegelsberg, P. N. J., Stead, R. H., Braun, T., Arnold, H. H., and Jaenish, R. (1993). MyoD or Myf-5 is required for the formation of skeletal muscle. Cell 75, 1351-1359.
53. Rudnicki, M. A., and Jaenish, R. (1995). The MyoD family of transcription factors and skeletal myogenesis. BioEssays 17, 203-209.
54. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989). "Molecular Cloning: A Laboratory Manual" (C. Nolan, Ed.). Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
55. 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, 757-759.
56. Sendtner, M., Schmalbruch, H., Stockli, K. A., Carroll, P., Kreutzberg, G. W., and Thoenen, H. (1992b). Ciliary neurotrophic factor prevents degeneration of motor neurons in mouse mutant progressive motor neuronopathy. Nature 358, 502-504.
57. Snider, W. D., Zhang, L., Yusoof, S., Gorukanti, N., and Tsering, C. (1992). Interactions between dorsal root axons and their target motor neurons in developing mammalian spinal cord. /. Neurosci. 12, 3494-3508.
58. Tanabe, Y., Roelnik, H., and Jessell, T. M. (1995). Induction of motor neurons by Sonic hedgehog is independent of floor plate differentiation. Curr. Biol. 5, 651-658.
59. Tanabe, Y., and Jessell, T. M. (1996). Diversity and pattern in the developing spinal cord. Science 274, 1115-1123.
60. Tosney, K. W. (1987). Proximal tissues and patterned neurite outgrowth at the lumbosacral level of the chick embryo: Deletion of the dermamyotome. Dev. Biol. 122, 540-558.
61. Tosney, K. W. (1988). Proximal tissues and patterned neurite outgrowth at the lumbosacral level of the chick embryo: Partial and complete deletion of the somite. Dev. Biol. 127, 266-286.
62. Tosney, K. W., Hotary, K. B., and Lance-Jones, C. (1995). Specifying the target identity of motoneurons. BioEsseys 17, 379-382.
63. Tsien, J. Z., Chen, D.-F., Gerber, D., Tom, C., Mercer, E. H., Anderson, D. J., Mayford, M., Kandel, E. R., and Tonegawa, S. (1996). Subregion-and cell type-restricted gene knockout in mouse brain. Cell 87, 1317-1326.
64. Tsuchida, T., Ensini, M., Morton, S. B., Baldassare, M., Edlund, T., Jessell, T. M., and Pfaff, S. L. (1994). Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes. Cell 79, 957-970.
65. Wright, D. E., Zhou, L., Kucera, J., and Snider, W. D. (1997). Introduction of a neurotrophin-3 transgene into muscle selectively rescues proprioceptive neurons in mice lacking endogenous neurotrophin-3. Neuron 19, 503-517.
66. Yamada, T., Placzek, M., Tanaka, H., Dodd, J., and Jessell, T. M. (1991). Control of cell pattern in the developing nervous system: Polarizing activity of the floor plate and notochord. Cell 64, 635-647.
67. Yamada, T., Pfaff, S. L., Edlund, T., and Jessell, T. M. (1993). Control of cell pattern in the neural tube: Motor neuron induction by diffusible factors from notochord and floor plate. Cell 73, 673-686.
68. Yan, Q., Elliot, J., and Snider, W. D. (1992). Brain-derived neurotrophic factor rescues spinal motor neurons from axotomy-induced cell death. Nature 360, 753-755.
69. Yan, Q., Elliott, J. L., Matheson, C., Sun, J., Zhang, L., Mu, X., Rex, K. L., and Snider, W. D. (1993). Influences of neurotrophins on mammalian motoneurons in vivo. J. Neurobiol. 24, 1555-1577.
70. Yan, Q., Matheson, C., Lopez, O. T., and Miller, J. A. (1994). The biological responses of axotomized adult motoneurons to brain-derived neurotrophic factor. J. Neurosci. 14, 5281-5291.
71. Yan, Q., Matheson, C., and Lopez, O. T. (1995). In vivo neurotrophic effects of GDNF on neonatal and adult facial motor neurons. Nature 373, 342-344.