Muscle-specific cell ablation conditional upon Cre-mediated DNA recombination in transgenic mice leads to massive spinal and cranial motoneuron loss

Developmental Biology

Volumn 197, Issue 2, 1998, Pages 234-247

  Grieshammer, Uta ^a   Lewandoski, Mark ^a   Prevette, David ^b   Oppenheim, Ronald W ^b   Martin, Gail R ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Cell ablation; Cleft palate; Cre loxP; Diphtheria toxin A fragment (DTA); DNA recombination; Motoneuron survival; Muscle cells; Programmed cell death; Robin sequence

Indexed keywords

ANIMAL CELL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; DNA RECOMBINATION; EMBRYO; EMBRYO DEVELOPMENT; GENE EXPRESSION REGULATION; MOUSE; MUSCLE DEVELOPMENT; MUSCLE INNERVATION; NERVE CELL DIFFERENTIATION; NONHUMAN; PIERRE ROBIN SYNDROME; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SPINAL CORD MOTONEURON; TRANSGENIC MOUSE;

ANIMALIA; MAMMALIA; MUS MUSCULUS; RODENTIA;

EID: 0032523802     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1006/dbio.1997.8859     Document Type: Article

References (51)

1. Ashwell K., Watson C. The development of facial motoneurons in the mouse-neuronal death and the innervation of the facial muscles. J. Embryol. Exp. Morphol. 77:1983;117-141.
2. Breitman M. L., Clapoff S., Rossant J., Tsui L. C., Glode L. M., Maxwell I. H., Bernstein A. Genetic ablation: Targeted expression of a toxin gene causes microphthalmia in transgenic mice. Science. 238:1987;1563-1565.
3. Brennan T. J., Olsen E. N., Klein W. H., Winslow J. W. Extensive motoneuron survival in the absence of secondary skeletal muscle fiber formation. J. Neurosci. Res. 45:1996;57-68.
4. Carey J. C., Fineman R. M., Ziter F. A. The Robin sequence as a consequence of malformation, dysplasia, and neuromuscular syndromes. J. Pediatr. 101:1982;858-864.
5. Carraway K. L. III, Sliwkowski M., Akita R., Platko J., Guy P., Nuijens A., Diamonti A., Vandlen R., Cantley L., Cerione R. The erbB3 gene product is a receptor for heregulin. J. Biol. Chem. 269:1994;14303-14306.
6. Cheng T. C., Hanley T. A., Mudd J., Merlie J. P., Olson E. N. Mapping of myogenin transcription during embryogenesis using transgenes linked to the myogenin control region. J. Cell Biol. 119:1992;1649-1656.
7. Ciutat D., Caldero J., Oppenheim R., Esquerda J. Schwann cell apoptosis during normal development and after axonal degeneration induced by neurotoxins in the chick embryo. J. Neurosci. 16:1996;3979-3990.
8. Clark P. G. H., Oppenheim R. W. Neuron death in vertebrate development:In vivo. Methods in Cell Biology, Apoptosis. 1995;Academic Press, New York. p. 277-321.
9. Collier R. J. Diphtheria toxin: Mode of action and structure. Bacteriol. Rev. 39:1975;54-85.
10. Ferguson M. Palate development. Development. 103:1988;41-60.
11. Friedland D., Eden A., Laitman J. Naturally occurring motoneuron cell death in rat upper respiratory motor nuclei: A histological, fast D;I and immunocytochemical study in the hypoglossal nucleus. J. Neurobiol. 27:1995;520-534.
12. Gu H., Marth J. D., Orban P. C., Mossmann H., Rajewsky K. Deletion of a DNA polymerase beta gene segment in T cells using cell type-specific gene targeting. Science. 265:1994;103-106.
13. Hamburger V. Regression versus peripheral control of differentiation in motor hypoplasia. Am. J. Anat. 102:1958;365-410.
14. Hamburger V. Cell death in the development of the lateral motor column of the chick embryo. J. Comp. Neurol. 160:1975;535-546.
15. Hamburger V., Hamilton H. A series of normal stages in the development of the chick embyros. J. Morphol. 88:1951;49-92.
16. Henderson C., Phillips H., Pollock R., Davies A., Lemeulle C., Armani M., Simpson L., Moffet B., Vandlen R., Koliatsos V., Rosenthal A. GDNF: A potent survival factor for motoneurons present in peripheral nerve and muscle. Science. 266:1994;1062-1064.
17. Hogan B., Beddington R., Costantini F., Lacy E. Manipulating the Mouse Embryo. 1994;Cold Spring Harbor Laboratory Press, Cold Spring Harbor. p. 226-250.
18. Hollyday M., Hamburger V. Reduction of naturally occurring motoneuron loss by enlargement of the periphery. J. Comp. Neurol. 170:1976;311-320.
19. Kelly R., Alonso S., Tajbakhsh S., Cossu G., Buckingham M. Myosin light chain 3F regulatory sequences confer regionalized cardiac and skeletal muscle expression in transgenic mice. J. Cell Biol. 129:1995;383-396.
20. Kessel M., Gruss P. Homeotic transformations of murine vertebrae and concomitant alteration of Hox codes induced by retinoic acid. Cell. 67:1991;89-104.
21. Kjaer I., Bach-Petersen S., Graem N., Kjaer T. Changes in human palatine bone location and tongue position during prenatal palatal closure. J. Craniofac. Genet. Dev. Biol. 13:1993;18-23.
22. Lakso M., Sauer B., Mosinger B. Jr., Lee E. J., Manning R. W., Yu S. H., Mulder K. L., Westphal H. Targeted oncogene activation by site-specific recombination in transgenic mice. Proc. Natl. Acad. Sci. USA. 89:1992;6232-6236.
23. Lance-Jones C. Motoneuron cell death in the developing lumbar spinal cord of the mouse. Dev. Brain Res. 4:1982;473-479.
24. Lawson S. J., Davies H. J., Bennett J. P., Lowrie M. B. Evidence that spinal interneurons undergo programmed cell death postnatally. Eur. J. Neurosci. 9:1997;794-799.
25. Lewandoski M., Martin G. Cre-mediated chromosome loss in mice. Nat. Genet. 17:1997;223-225.
26. Lewandoski M., Meyers E. N., Martin G. R. Analysis ofFgf8. Cold Spring Harbor Symp. Quant. Biol. 62:1997;159-168.
27. Lin D. M., Auld V. J., Goodman C. S. Targeted neuronal cell ablation in the Drosophila embryo: Pathfinding by follower growth cones in the absence of pioneers. Neuron. 14:1995;707-715.
28. McKay S. E., Oppenheim R. W. Lack of evidence for cell death among avian spinal cord interneurons in the chick embryo. J. Neurobiol. 22:1991;721-733.
29. Oakley R., Lefcort F., Clary D., Reichardt L., Prevette D., Oppenheim R., Frank E. Neurotrophin-3 promotes the differentiation of muscle spindle afferents in the absence of peripheral targets. J. Neurosci. 17:1997;4262-4274.
30. Oppenheim R., Houenou L., Johnson J., Lin L., Li L., Lo A., Newsome A., Prevette D., Wang S. Developing motor neurons rescued from programmed and axotomy-induced cell death by GDNF. Nature. 373:1995;344-346.
31. Oppenheim R., Majors-Willard C. Neuronal cell death in the brachial spinal cord of the chick embryo is unrelated to the loss of polyneuronal innervation in wing muscle. Brain Res. 154:1978;148-152.
32. Oppenheim R. W. The absence of significant postnatal motoneuron death in the brachial and lumbar spinal cord of the rat. J. Comp. Neurol. 246:1986;281-286.
33. Oppenheim R. W. Cell death during development of the nervous system. Annu. Rev. Neurosci. 14:1991;453-501.
34. Oppenheim R. W. Neurotrophic survival molecules for motoneurons: An embarrassment of riches. Neuron. 17:1996;195-197.
35. Oppenheim R. W., Chu-Wang I. W., Maderdrut J. L. Cell death of motoneurons in the chick embryo spinal cord. III. Differentiation of motoneurons prior to their induced degeneration following limb bud removal. J. Comp. Neurol. 177:1978;87-112.
36. Oppenheim R. W., Prevette D., Haverkamp L. J., Houenou L., Yin Q. W., McManaman J. L. Biological studies of a putative avian muscle-derived neurotrophic factor that prevents naturally occurring motoneuron deathin vivo. J. Neurobiol. 24:1993;1065-1079.
37. Palmiter R. D., Behringer R. R., Quaife C. J., Maxwell F., Maxwell I. H., Brinster R. L. Cell lineage ablation in transgenic mice by cell-specific expression of a toxin gene. Cell. 50:1987;435-443.
38. Palmiter R. D., Brinster R. L. Germ-line transformation of mice. Annu. Rev. Genet. 20:1986;465-499.
39. Phelan K., Hollyday M. Embryonic development and survival of brachial motoneurons projecting to muscleless chick wings. J. Comp. Neurol. 311:1991;313-320.
40. Pinkas-Kramarski R., Shelly M., Glathe S., Ratzkin B., Yarden Y. Neu differentiation factor/neuregulin isoforms activate distinct receptor combinations. J. Biol. Chem. 27:1996;19029-19032.
41. Reithmacher D., Sonnenberg-Reithmacher E., Brinkmann V., Yamaai T., Lewin G., Birchmeier C. Severe neuropathies in mice with targeted mutations in the ErbB3 receptor. Nature. 398:1997;725-730.
42. Sanes J., Rubenstein J., Nicolas J. Use of a recombinant retrovirus to study post-implantation cell lineage in mouse embryos. EMBO J. 5:1986;3133-3142.
43. Sassoon D., Lyons G., Wright W. E., Lin V., Lassar A., Weintraub H., Buckingham M. Expression of two myogenic regulatory factors myogenin and MyoD1 during mouse embryogenesis. Nature. 341:1989;303-307.
44. Sliwkowski M., Schaefer G., Akita R., Lofgren J., Fitzpatrick V., Nuijens A., Fendly B., Cerione R., Vandlen R., Carraway K. R. Coexpression of erbB2 and erbB3 proteins reconstitutes a high affinity receptor for heregulin. J. Biol. Chem. 269:1994;14661-14665.
45. Tanaka H., Landmesser L. Cell death of lumbosacral motoneurons in chick, quail and chick-quail chimera embryos: A test of the quantitative matching hypothesis of neuronal cell death. J. Neurosci. 6:1986;2889-2899.
46. Tsien J. Z., Chen D. F., Gerber D., Tom C., Mercer E. H., Anderson D. J., Mayford M., Kandel E. R., Tonegawa S. Subregion- and cell type-restricted gene knockout in mouse brain. Cell. 87:1996;1317-1326.
47. Venuti J., Morris J., Vivian J., Olson E., Klein W. Myogenin is required for late but not early aspects of myogenesis during mouse development. J. Cell Biol. 128:1995;563-576.
48. Wright D., Zhou L., Kucera J., Snider W. Introduction of a neurotrophin-3 transgene into muscle selectively rescues proprioceptive neurons in mice lacking endogenous neurotrophin-3. Neuron. 19:1997;503-517.
49. Wright W., Sassoon D., Lin V. Myogenin, a factor regulating myogenesis, has a domain homologous to MyoD. Cell. 56:1989;607-617.
50. Yamaizumi M., Mekada E., Uchida T., Okada Y. One molecule of diphtheria toxin fragment A introduced into a cell can kill the cell. Cell. 15:1978;245-250.
51. Yee S. P., Rigby P. W. The regulation of myogenin gene expression during the embryonic development of the mouse. Genes Dev. 7:1993;1277-1289.