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Altered segmental identity and abnormal migration of motor neurons in mice lacking Hoxb-1

Abstract

SEGMENTATION of the vertebrate hindbrain into rhombomeres is important for the anterior–posterior arrangement of cranial motor nuclei and efferent nerves1. Underlying this reiterated organization, Hox genes display segmentally restricted domains of expression2–4, such as expression of Hoxb-1 (refs 5, 6) in rhombomere 4 (r4). Here we report that absence of Hoxb-1 leads to changes in r4 identity. In mutant mouse embryos, molecular markers indicate that patterning of r4 is initiated properly but not maintained. Cellular analysis by DiI tracing reveals that the r4-specific facial branchiomotor (FBM) and contralateral vestibuloacoustic efferent (CVA) neurons are incorrectly specified. In wild-type mice CVA neurons migrate from r4 into the contralateral side7, and we found in lineage analysis that FBM neurons migrate from r4 into r5. In mutants, motor neurons differentiate but the CVA and FBM neurons fail to migrate into their proper positions. Instead, they form a motor nucleus which migrates atypically, and there is a subsequent loss of the facial motor nerve. These results demonstrate that, as a part of its role in maintaining rhombomere identity, Hoxb-1 is involved in controlling migratory properties of motor neurons in the hindbrain.

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References

  1. Lumsden, A. & Keynes, R. Nature 337, 424–428 (1989).

    Article  ADS  CAS  Google Scholar 

  2. Hunt, P. et al. Nature 353, 891–864 (1991).

    Article  ADS  Google Scholar 

  3. Krumlauf, R. Cell 78, 191–201 (1994).

    Article  CAS  Google Scholar 

  4. Keynes, R. & Krumlauf, R. Annu. Rev. Neurosci. 17, 109–132 (1994).

    Article  CAS  Google Scholar 

  5. Murphy, P., Davidson, D. R. & Hill, R. E. Nature 341, 156–159 (1989).

    Article  ADS  CAS  Google Scholar 

  6. Wilkinson, D. G., Bhatt, S., Cook, M., Boncinelli, E. & Krumlauf, R. Nature 341, 405–409 (1989).

    Article  ADS  CAS  Google Scholar 

  7. Simon, H. & Lumsden, A. Neuron 11, 209–220 (1993).

    Article  CAS  Google Scholar 

  8. Carpenter, E. M., Goddard, J. M., Chisaka, O., Manley, N. R. & Capecchi, M. R. Development 118, 1063–1075 (1993).

    CAS  Google Scholar 

  9. Mark, M. et al. Development 119, 219–338 (1993).

    Google Scholar 

  10. Dollé, P. et al. Proc. Natl Acad. Sci. USA 90, 7666–7670 (1993).

    Article  ADS  Google Scholar 

  11. Alexandré, D. et al. Development 122, 723–746 (1996).

    Google Scholar 

  12. Zhang, M. et al. Development 120, 2431–2442 (1994).

    CAS  PubMed  Google Scholar 

  13. Pöpperl, H. et al. Cell 81, 1031–1042 (1995).

    Article  Google Scholar 

  14. Itasaki, N., Sharpe, J., Morrison, A. & Krumlauf, R. Neuron 16, 487–500 (1996).

    Article  CAS  Google Scholar 

  15. Wilkinson, D. G., Bhatt, S., Chavrier, P., Bravo, R. & Charnay, P. Nature 337, 461–464 (1989).

    Article  ADS  CAS  Google Scholar 

  16. Nieto, M. A., Gilardi-Hebenstreit, P., Charnay, P. & Wilkinson, D. Development 116, 1137–1150 (1992).

    CAS  Google Scholar 

  17. Cordes, S. P. & Barsh, G. S. Cell 79, 1025–1034 (1994).

    Article  CAS  Google Scholar 

  18. Ruiz, J. & Robertson, D. Mech. Dev. 46, 87–100 (1994).

    Article  CAS  Google Scholar 

  19. Becker, N. et al. Mech. Dev. 47, 3–18 (1994).

    Article  CAS  Google Scholar 

  20. Hume, C. R. & Dodd, J. Development 119, 1147–1160 (1993).

    CAS  PubMed  Google Scholar 

  21. Swiatek, P. J. & Gridley, T. Genes Dev. 7, 2071–2084 (1993).

    Article  CAS  Google Scholar 

  22. Ruberte, E., Friederich, V., Morriss-Kay, G. & Chambon, P. Development 115, 973–989 (1992).

    CAS  PubMed  Google Scholar 

  23. Maden, M. et al. Mech. Dev. 37, 13–23 (1992).

    Article  CAS  Google Scholar 

  24. Frasch, M., Chen. X. & Lufkin, T. Development 121, 957–974 (1995).

    CAS  PubMed  Google Scholar 

  25. Irving, C., Nieto, M., Das Gupta, R., Chamey, P. & Wilkinson, D. Dev. Biol. 173, 26–38 (1996).

    Article  CAS  Google Scholar 

  26. Marshall, H. et al. Nature 360, 737–741 (1992).

    Article  ADS  CAS  Google Scholar 

  27. McKay, I., Lewis, J. & Lumsden, A. Mol. Cell. Neurobiol. (in the press).

  28. Tsuchida, T. et al. Cell 79, 957–970 (1994).

    Article  CAS  Google Scholar 

  29. Pachnis, V., Mankoo, B. & Costantini, F. Development 119, 1005–1017 (1993).

    CAS  Google Scholar 

  30. Altman, J. & Bayer, S. Development of the Cranial Nerve Ganglia and Related Nuclei in the Rat (Springer, Berlin, 1982).

    Chapter  Google Scholar 

  31. Ramirez-Solis, R., Davis, A. & Bradley, A. in Guide to Techniques in Mouse Development (eds Wasserman, P. & DePamphilis, M.) 885–878 (Academic, 1993).

    Google Scholar 

  32. Wilkinson, D. & Green, J. in Postimplantation Mouse Embryos: a Practical Approach (eds Copp, A. J., Cockcroft, D. L & Hames, B. D.) 155–171 (IRL, Oxford, 1990).

    Google Scholar 

  33. Schaeren-Wiemers, N. & Gerfin-Moser, A. Histochemistry 100, 431–440 (1993).

    Article  CAS  Google Scholar 

  34. Studer, M., Pöpperl, H., Marshall, H., Kuroiwa, A. & Krumlauf, R. Science 265, 1728–1732 (1994).

    Article  ADS  CAS  Google Scholar 

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Studer, M., Lumsden, A., Ariza-McNaughton, L. et al. Altered segmental identity and abnormal migration of motor neurons in mice lacking Hoxb-1. Nature 384, 630–634 (1996). https://doi.org/10.1038/384630a0

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