Hoxc10 and Hoxd10 regulate mouse columnar, divisional and motor pool identity of lumbar motoneurons

Development

Volumn 135, Issue 1, 2008, Pages 171-182

  Wu, Yuanyuan ^a   Wang, Guoying ^a   Scott, Sheryl A ^a   Capecchi, Mario R ^a,b  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b HOWARD HUGHES MEDICAL INSTITUTE   (United States)

Author keywords

Hoxc10; Hoxd10; Motoneuron specification; Mouse; Spinal cord

Indexed keywords

COMPLEMENTARY DNA; HOX PROTEIN; TRANSCRIPTION FACTOR HOXC10; TRANSCRIPTION FACTOR HOXD10; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL DIVISION; CELL MIGRATION; CONTROLLED STUDY; DISEASE SEVERITY; HINDLIMB; INTERNEURON; LOCOMOTION; LUMBAR SPINAL CORD; MORPHOLOGY; MOTOR DYSFUNCTION; MOUSE; MUSCLE DEVELOPMENT; MUSCLE INNERVATION; NERVE CELL DIFFERENTIATION; NERVE PROJECTION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPIC VARIATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM; SPINAL CORD MOTONEURON; THORACIC SPINAL CORD;

ALLELES; ANIMALS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HINDLIMB; HOMEODOMAIN PROTEINS; LUMBAR VERTEBRAE; MICE; MICE, KNOCKOUT; MOTOR NEURONS; MUSCLES; MUTATION; SPINAL CORD; TRANSCRIPTION FACTORS;

VERTEBRATA;

EID: 38849182245     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.009225     Document Type: Article

References (53)

1. Arber, S., Han, B., Mendelsohn, M., Smith, M., Jessell, T. M. and Sockanathan, S. (1999). Requirement for the homeobox gene Hb9 in the consolidation of motor neuron identity. Neuron 23, 659-674.
2. Arber, S., Ladle D. R., Lin, J. H., Frank E. and Jessell, T. M. (2000). ETS gene Er81 controls the formation of functional connections between group la sensory afferents and motor neurons. Cell 101, 485-498.
3. Arenkiel, B. R., Tvrdik, R., Gaufo, G. O. and Capecchi, M. R. (2004). Hoxb1 functions in both motoneurons and in tissues of the periphery to establish and maintain the proper neuronal circuitry. Genes Dev. 18, 1539-1552.
4. Boulet, A. M. and Capecchi, M. R. (1996). Targeted disruption of hoxc-4 causes esophageal defects and vertebral transformations. Dev. Biol. 177, 232-249.
5. Briscoe, J., Sussel, L., Serup, P., Hartigan-O'Connor, D., Jessell, T. M., Rubenstein, J. L. and Ericson, J. (1999). Homeobox gene Nkx2.2 and specification of neuronal identity by graded Sonic hedgehog signalling. Nature 398, 622-627.
6. Bunting, M., Bernstein, K. E., Greer, J. M., Capecchi, M. R. and Thomas, K. R. (1999). Targeting genes for self-excision in the germ line. Genes Dev. 13, 1524-1528.
7. Carpenter, E. M. (2002). Hox genes and spinal cord development. Dev. Neurosci. 24, 24-34.
8. Carpenter, E. M., Goddard, J. M., Chisaka, O., Manley, N. R. and Capecchi, M. R. (1993). Loss of Hox-A1 (Hox-1.6) function results in the reorganization of the murine hindbrain. Development 118, 1063-1075.
9. Carpenter, E. M., Goddard, J. M., Davis, A. P., Nguyen, T. P. and Capecchi, M. R. (1997). Targeted disruption of Hoxd-10 affects mouse hindlimb development. Development 124, 4505-4514.
10. Choe, A., Phun, H. Q., Tieu, D. D., Hu, Y. H. and Carpenter, E. M. (2006). Expression patterns of Hox10 paralogous genes during lumbar spinal cord development. Gene Expr. Patterns 6, 730-737.
11. Dasen, J. S., Liu, J. P. and Jessell, T. M. (2003). Motor neuron columnar fate imposed by sequential phases of Hox-c activity. Nature 425, 926-933.
12. Dasen, J. S., Tice, B. C., Brenner-Morton, S. and Jessell, T. M. (2005). A Hox regulatory network establishes motor neuron pool identity and target-muscle connectivity. Cell 123, 477-491.
13. Duboule, D. and Morata, G. (1994). Colinearity and functional hierarchy among genes of the homeotic complexes. Trends Genet. 10, 358-364.
14. 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.
15. Ericson, J., Rashbass, R., Schedl, A., Brenner-Morton, S., Kawakarni, 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 190, 169-180.
16. Greene, E. C. (1935). Anatomy of the Rat. Philadelphia: American Philosophical Society.
17. Greer, J. M. and Capecchi, M. R. (2002). Hoxb8 is required for normal grooming behavior in the mouse. Neuron 33, 23-34.
18. Helmbacher, F., Schneider-Maunoury, S., Topilko, P., Tiret, L. and Charnay, P. (2000). Targeting of the EphA4 tyrosine kinase receptor affects dorsal/ventral pathfinding of limb motor axons. Development 127, 3313-3324.
19. Hostikka, S. L. and Capecchi, M. R. (1998). The mouse Hoxc11 gene: genomic structure and expression pattern. Mech. Dev. 70, 133-145.
20. Huber, A. B., Kania, A., Tran, T. S., Gu, C., De Marco Garcia, N., Lieberam, I., Johnson, D., Jessell, T. M., Ginty, D. D. and Kolodkin, A. L. (2005). Distinct roles for secreted semaphorin signaling in spinal motor axon guidance. Neuron 48, 949-964.
21. Jessell, T. M. (2000). Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev. Genet. 1, 20-29.
22. Kania, A., Johnson, R. L. and Jessell, T. M. (2000). Coordinate roles for LIM homeobox genes in directing the dorsoventral trajectory of motor axons in the vertebrate limb. Cell 102, 161-173.
23. Lance-Jones, C. (1982). Motoneuron cell death in the developing lumbar spinal cord of the mouse. Brain Res. 256, 473-479.
24. Lance-Jones, C., Omelchenko, N., Bailis, A., Lynch, S. and Sharma, K. (2001). Hoxd10 induction and regionalization in the developing lumbosacral spinal cord. Development 128, 2255-2268.
25. Landmesser, L. T. (2001). The acquisition of motoneuron subtype identity and motor circuit formation. Int. J. Dev. Neurosci. 19, 175-182.
26. Landmesser, L. T. and O'Donovan, M. J. (1984). The activation patterns of embryonic chick motoneurones projecting to inappropriate muscles. J. Physiol. 347, 205-224.
27. Lin, A. W. and Carpenter, E. M. (2003). Hoxa10 and Hoxd10 coordinately regulate lumbar motor neuron patterning. J. Neurobiol. 56, 328-337.
28. Lin, J. H., Saito, T., Anderson, D. J., Lance-Jones, C., Jessell, T. M. and Arber, S. (1998). Functionally related motor neuron pool and muscle sensory afferent subtypes defined by coordinate ETS gene expression. Cell 95, 393-407.
29. Livet, J., Sigrist, M., Stroebel, S., De Paola, V., Price, S. R., Henderson, C. E., Jessell, T. M. and Arber, S. (2002). ETS gene Pea3 controls the central position and terminal arborization of specific motor neuron pools. Neuron 35, 877-892.
30. Manley, N. R., Barrow, J. R., Zhang, T. and Capecchi, M. R. (2001). Hoxb2 and hoxb4 act together to specify ventral body wall formation. Dev. Biol. 237, 130-144.
31. Matise, M. P. and Lance-Jones, C. (1996). A critical period for the specification of motor pools in the chick lumbosacral spinal cord. Development 122, 659-669.
32. McHanwell, S. and Biscoe, T. J. (1981). The localization of motoneurons supplying the hindlimb muscles of the mouse. Philos. Trans. R. Soc. Lond. B Biol. Sci. 293, 477-508.
33. Messersmith, E. K., Leonardo, E. D., Shatz, C. J., Tessier-Lavigne, M., Goodman, C. S. and Kolodkin, A. L. (1995). Semaphorin III can function as a selective chemorepellent to pattern sensory projections in the spinal cord. Neuron 14, 949-959.
34. Misra, M., Shah, V., McCaffery, P. and Lance-Jones, C. (2005). Evidence that Hoxd10 and Hoxd11 have different roles in the development of lateral and medial motoneuron subtypes in the spinal cord of the chick embryo. Society for Neuroscience. Program No. 596.15. Washington DC.
35. Morgan, B. A. and Tabin, C. (1994). Hox genes and growth: early and late roles in limb bud morphogenesis. Dev. Suppl. 1994, 181-186.
36. Nelson, C. E., Morgan, B. A., Burke, A. C., Laufer, E., DiMarnbro, E., Murtaugh, L. C., Gonzales, E., Tessarollo, L., Parada, L. F. and Tabin, C. (1996). Analysis of Hox gene expression in the chick limb bud. Development 122, 1449-1466.
37. Price, S. R., De Marco Garcia, N. V., Ranscht, B. and Jessell, T. M. (2002). Regulation of motor neuron pool sorting by differential expression of type II cadherins. Cell 109, 205-216.
38. Rijli, F. M., Matyas, R., Pellegrini, M., Dierich, A., Gruss, P., Dolle, P. and Chambon, P. (1995). Cryptorchidism and homeotic transformations of spinal nerves and vertebrae in Hoxa-10 mutant mice. Proc. Natl. Acad. Sci. USA 92, 8185-8189.
39. Shah, V., Drill, E. and Lance-Jones, C. (2004). Ectopic expression of Hoxd10 in thoracic spinal segments induces motoneurons with a lumbosacral molecular profile and axon projections to the limb. Dev. Dyn. 231, 43-56.
40. Sharma, K., Sheng, H. Z., Lettieri, K., Li, H., Karavanov, A., Potter, S., Westphal, H. and Pfaff, S. L. (1998). LIM homeodomain factors Lhx3 and Lhx4 assign subtype identities for motor neurons. Cell 95, 817-828.
41. Sharma, K., Leonard, A. E., Lettieri, K. and Pfaff, S. L. (2000). Genetic and epigenetic mechanisms contribute to motor neuron pathfinding. Nature 406, 515-519.
42. Sockanathan, S. and Jessell, T. M. (1998). Motor neuron-derived retinoid signaling specifies the subtype identity of spinal motor neurons. Cell 94, 503-514.
43. Tarchini, B., Huynh, T. H., Cox, G. A. and Duboule, D. (2005). HoxD cluster scanning deletions identify multiple defects leading to paralysis in the mouse mutant Ironside. Genes Dev. 19, 2862-2876.
44. Thaler, J. P., Koo, S. J., Kania, A., Lettieri, K., Andrews, S., Cox, C., Jessell, T. M. and Pfaff, S. L. (2004). A postmitotic role for Isl-class LIM homeodomain proteins in the assignment of visceral spinal motor neuron identity. Neuron 41, 337-350.
45. Tiret, L., Le Mouellic, H., Maury, M. and Brulet, P. (1998). Increased apoptosis of motoneurons and altered somatotopic maps in the brachial spinal cord of Hoxc-8-deficient mice. Development 125, 279-291.
46. 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.
47. Vermot, J., Schuhbaur, B., Le Mouellic, H., McCaffery, P., Garnier, J. M., Hentsch, D., Brulet, P., Niederreither, K., Chambon, P., Dolle, P. et al. (2005). Retinaldehyde dehydrogenase 2 and Hoxc8 are required in the murine brachial spinal cord for the specification of Lim1+ motoneurons and the correct distribution of Islet1+ motoneurons. Development 132, 1611-1621.
48. Vogel, M. W. (1987). Activation patterns of embryonic chick lumbosacral motoneurones following large spinal cord reversals. J. Physiol. 389, 491-512.
49. Vrieseling, E. and Arber, S. (2006). Target-induced transcriptional control of dendritic patterning and connectivity in motor neurons by the ETS gene Pea3. Cell 127, 1439-1452.
50. Wahba, G. M., Hostikka, S. L. and Carpenter, E. M. (2001). The paralogous Hox genes Hoxa 10 and Hoxd 10 interact to pattern the mouse hindlimb peripheral nervous system and skeleton. Dev. Biol. 231, 87-102.
51. Wang, G. and Scott, S. A. (2004). An early broad competence of motoneurons to express ER81 is later sculpted by the periphery. J. Neurosci. 24, 9789-9798.
52. Wang, G. and Scott, S. A. (2007). Onset of ETS expression is not accelerated by premature exposure to signals from limb mesenchyme. Dev. Dyn. 236, 2109-2117.
53. Wellik, D. M. and Capecchi, M. R. (2003). Hox10 and Hox11 genes are required to globally pattern the mammalian skeleton. Science 301, 363-367.