Ectopic expression of Hoxd10 in thoracic spinal segments induces motoneurons with a lumbosacral molecular profile and axon projections to the limb

Developmental Dynamics

Volumn 231, Issue 1, 2004, Pages 43-56

  Shah, Veeral ^a   Drill, Emily ^a   Lance Jones, Cynthia ^a  

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

Author keywords

AP patterning; Axon guidance; Chick embryo; Hox genes; Hoxd10; Lumbosacral spinal cord; Motorneuron identity; Spinal cord

Indexed keywords

GENE PRODUCT; PROTEIN LIM1; PROTEIN RALDH2; UNCLASSIFIED DRUG;

ANIMAL TISSUE; BACK; CELL INTERACTION; CENTRAL NERVOUS SYSTEM; CHICK EMBRYO; CONFERENCE PAPER; ELECTROPORATION; EMBRYO; GENE EXPRESSION; GENE FUNCTION; GONAD; HOX GENE; HOXD10 GENE; LIMB; MESODERM; MOTONEURON; NERVE CELL DIFFERENTIATION; NERVE PROJECTION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; THORACIC SPINE;

ALDEHYDE OXIDOREDUCTASES; ANIMALS; AXONS; CHICK EMBRYO; EXTREMITIES; GREEN FLUORESCENT PROTEINS; HOMEODOMAIN PROTEINS; IN SITU HYBRIDIZATION; MOTOR NEURONS; RETINAL DEHYDROGENASE; SPINAL CORD; THORAX;

EID: 4143123157     PISSN: 10588388     EISSN: None     Source Type: Journal    
DOI: 10.1002/dvdy.20103     Document Type: Conference Paper

References (75)

1. Akam M. 1987. The molecular basis for metameric pattern in the Drosophila embryo. Development 101:1-22.
2. Alexandre D, Clarke JD, Oxtoby E, Yan YL, Jowett T, Holder N. 1996. Ectopic expression of Hoxa-1 in the zebrafish alters the fate of the mandibular arch neural crest and phenocopies a retinoic acid-induced phenotype. Development 122:735-746.
3. Barrow JR, Stadler HS, Capecchi MR. 2000. Roles of Hoxa1 and Hoxa2 in patterning the early hindbrain of the mouse. Development 127:933-944.
4. Bell E, Wingate RJ, Lumsden A. 1999. Homeotic transformation of rhombomere identity after localized Hoxb1 misexpression. Science 284:2168-2171.
5. Bello BC, Hirth F, Gould AP. 2003. A pulse of the Drosophila Hox protein Abdominal-A schedules the end of neural proliferation via neuroblast apoptosis. Neuron 37:209-219.
6. Berggren K, McCaffery P, Drager U, Forehand CJ. 1999. Differential distribution of retinoic acid synthesis in the chicken embryo as determined by immunolocalization of the retinoic acid synthetic enzyme, RALDH-2. Dev Biol 210:288-304.
7. Burke AC, Tabin CJ. 1996. Virally mediated misexpression of Hoxc-6 in the cervical mesoderm results in spinal nerve truncations. Dev Biol 178:192-197.
8. Burke AC, Nelson CE, Morgan BA, Tabin C. 1995. Hox genes and the evolution of vertebrate axial morphology. Development 121:333-346.
9. Capdevila J, Tsukui T, Rodriquez Esteban C, Zappavigna V, Izpisua Belmonte JC, 1999. Control of vertebrate limb outgrowth by the proximal factor Meis2 and distal antagonism of BMPs by Gremlin. Mol Cell 4:839-849.
10. Capecchi MR. 1997. The role of Hox genes in hindbrain development. New York: Oxford University Press. p 334-355.
11. Carton N, Pizant J, Stahl A. 1983. Mesonephric origin of the gonadal primitive medulla in chick embryos. Anat Embryol (Berl) 166:399-414.
12. Carpenter EM. 2002. Hox genes and spinal cord development. Dev Neurosci 24:24-34.
13. Carpenter EM, Goddard JM, Davis AP, Nguyen TP, Capecchi MR. 1997. Targeted disruption of Hoxd-10 affects mouse hindlimb development. Development 124:4505-4514.
14. Carpenter EM, Hollyday M. 1992. The location and distribution of neural crest-derived Schwann cells in developing peripheral nerves in the chick forelimb. Dev Biol 150:144-159.
15. Dasen JS, Liu JP, Jessell TM. 2003. Motor neuron columnar fate imposed by sequential phases of Hox-c activity. Nature 425:926-933.
16. de la Cruz CC, Der-Avakian A, Spyropoulos DD, Tieu DD, Carpenter EM. 1999. Targeted disruption of Hoxd9 and Hoxd10 alters locomotor behavior, vertebral identity, and peripheral nervous system development. Dev Biol 216:595-610.
17. Ebens A, Brose K, Leonardo ED, Hanson MG Jr, Bladt F, Birchmeier C, Barres BA, Tessier-Lavigne M. 1996. Hepatocyte growth factor/scatter factor is an axonal chemoattractant and a neurotrophic factor for spinal motor neurons. Neuron 17:1157-1172.
18. Eberhart J, Swartz M, Koblar SA, Pasquale EB, Tanaka H, Krull CE. 2000. Expression of EphA4, ephrin-A2 and ephrin-A5 during axon outgrowth to the hindlimb indicates potential roles in pathfinding. Dev Neurosci 22:237-250.
19. Eberhart J, Swartz ME, Koblar SA, Pasquale EB, Krull CE. 2002. EphA4 constitutes a population-specific guidance cue for motor neurons. Dev Biol 247:89-101.
20. Economides KD, Zeltser L, Capecchi MR, 2003. Hoxb13 mutations cause overgrowth of caudal spinal cord and tail vertebrae. Dev Biol 266:317-330.
21. Ensini M, Tsuchida TN, Belting HG, Jessell TM. 1998. The control of rostrocaudal pattern in the developing spinal cord: specification of motor neuron subtype identity is initiated by signals from paraxial mesoderm. Development 125:969-982.
22. Feng G, Laskowski MB, Feldheim DA, Wang H, Lewis R, Frisen J, Flanagan JG, Sanes JR. 2000. Roles for ephrins in positionally selective synaptogenesis between motor neurons and muscle fibers. Neuron 25:295-306.
23. Fukushima M, Nakamura M, Ohta K, Okamura R, Negi A. 1996. Regional specification of motoneurons along the anterior-posterior axis is independent of the notochord. Development 122:905-914.
24. Gaufo GO, Thomas KR, Capecchi MR. 2003. Hox3 genes coordinate mechanisms of genetic suppression and activation in the generation of branchial and somatic motoneurons. Development 130:5191-5201.
25. Gaunt SJ. 2000. Evolutionary shifts of vertebrate structures and Hox expression up and down the axial series of segments: a consideration of possible mechanisms. Int J Dev Biol 44:109-117.
26. Goodman FR, Scambler PJ. 2001. Human HOX gene mutations. Clin Genet 59:1-11.
27. Guidato S, Prin F, Guthrie S. 2003. Somatic motoneurone specification in the hindbrain: the influence of somite-derived signals, retinoic acid and Hoxa3. Development 130:2981-2996.
28. Gutman CR, Ajmera MK, Hollyday M. 1993. Organization of motor pools supplying axial muscles in the chicken. Brain Res 609:129-136.
29. Hamburger V, Hamilton HL. 1951. A series of normal stages in the development of the chick embryo. J Morphol 88:49-92.
30. Hamburger V, Oppenheim RW. 1982. Naturally occurring neuronal death in vertebrates. Neurosci Comment 1:39-55.
31. Helmbacher F, Pujades C, Desmarquet C, Frain M, Rijii FM, Chambon P, Charnay P. 1998. Hoxa1 and Krox-20 synergize to control the development of rhombomere3. Development 125:4739-4748.
32. Helmbacher F, Schneider-Maunoury S, Topilko P, Tiret L, Charnay P. 2000. Targeting of the EphA4 tyrosine kinase receptor affects dorsal/ventral pathfinding of limb motor axons. Development 127:3313-3324.
33. Hollyday M, Hamburger V. 1977. An autoradiographic study of the formation of the lateral motor column in the chick embryo. Brain Res 132:197-208.
34. Hollyday M, Jacobson RD. 1990. Location of motor pools innervating chick wing. J Comp Neurol 302:575-588.
35. Itasaki N, Bel-Vialar S, Krumlauf R. 1999. 'Shocking' developments in chick embryology: electroporation and in ovo gene expression. Nat Cell Biol 1:E203-207.
36. Iwamasa H, Ohta K, Yamada T, Ushijima K, Terasaki H, Tanaka H. 1999. Expression of Eph receptor tyrosine kinases and their ligands in chick embryonic motor neurons and hindlimb muscles. Dev Growth Differ 41:685-698.
37. James RG, Schultheiss TM. 2003. Patterning of the avion intermediate mesoderm by lateral plate and axial tissues. Dev Biol 253:109-124.
38. Johnson RL, Tabin CJ. 1997. Molecular models for vertebrate limb development. Cell 90:979-990.
39. Jungbluth S, Bell E, Lumsden A. 1999. Specification of distinct motor neuron identities by the singular activities of individual Hox genes. Development 126:2751-2758.
40. Kania A, Jessell TM. 2003. Topographic motor projections in the limb imposed by LIM homeodomain protein regulation of ephrin-A:EphA interactions. Neuron 38:581-596.
41. Kania A, Johnson RL, Jessell TM. 2000. Coordinate roles for LIM homeobox genes in directing the dorsoventral trajectory of motor axons in the vertebrate limb. Cell 102:161-173.
42. Kilpatrick TJ, Brown A, Lai C, Gassmann M, Goulding M, Lemke G. 1996. Expression of the Tyro4/Mek4/Cek4 gene specifically marks a subset of embryonic motor neurons and their muscle targets. Mol Cell Neurosci 7:62-74.
43. Kobayashi A, Behringer RR. 2003. Developmental genetics of the female reproductive tract in mammals. Nat Rev Genet 4:969-980.
44. Krumlauf R. 1994. Hox genes in vertebrate development. Cell 78:191-201.
45. Lance-Jones C, Landmesser L. 1981. Pathway selection by embryonic chick motoneurons in an experimentally altered environment. Proc R Soc Lond B Biol Sci 214:19-52.
46. Lance-Jones C, Omelchenko N, Bailis A, Lynch S, Sharma K. 2001. Hoxd10 induction and regionalization in the developing lumbosacral spinal cord. Development 128:2255-2268.
47. Landmesser L. 1978. The distribution of motoneurons supplying chick hind limb muscles. J Physiol 284:371-389.
48. Lin AW, Carpenter EM. 2003. Hoxa10 and Hoxd10 coordinately regulate lumbar motor neuron patterning. J Neurobiol 50:328-337.
49. Liu JP, Laufer E, Jessell TM. 2001. Assigning the positional identity of spinal motor neurons. Rostrocaudal patterning of Hox-c expression by FGFs, Gdf11, and retinoids. Neuron 32:997-1012.
50. Lumsden A, Krumlauf R. 1996. Patterning the vertebrate neuraxis. Science 274:1109-1115.
51. Matise MP, Lance-Jones C. 1996. A critical period for the specification of motor pools in the chick lumbosacral spinal cord. Development 122:659-669.
52. Mauch TJ, Yang G, Wright M, Smith D, Schoenwolf GC. 2000. Signals from trunk paraxial mesoderm induce pronephros formation in chick intermediate mesoderm. Dev Biol 220:62-75.
53. McGinnis W, Krumlauf R. 1992. Homeobox genes and axial patterning. Cell 68:283-302.
54. Mercader N, Leonardo E, Azpiazu N, Serrano A, Morata G, Martinez C, Torres M. 1999. Conserved regulation of proximodistal limb axis development by Meis1/Hth. Nature 402:425-429.
55. Nelson CE, Morgan BA, Burke AC, Laufer E, DiMambro E, Murtaugh LC, Gonzales E, Tessarollo L, Parada LF, Tabin C. 1996. Analysis of Hox gene expression in the chicklimb bud. Development 122:1449-1466.
56. Nieto MA, Patel K, Wilkinson DG. 1996. In situ hybridization analysis of chick embryos in whole mount and tissue sections. Methods Cell Biol 51:219-235.
57. Nowicki JL, Burke AC. 2000. Hox genes and morphological identity: axial versus lateral patterning in the vertebrate mesoderm. Development 127:4265-4275.
58. O'Brien MK, Oppenheim RW. 1990. Development and survival of thoracic motoneurons and hindiimb musculature following transplantation of the thoracic neural tube to the lumbar region in the chick embryo: anatomical aspects. J Neurobiol 21:313-340.
59. Omelchenko N, Lance-Jones C. 2003. Programming neural Hoxd10: in vivo evidence that early node-associated signals predominate over paraxial mesoderm signals at posterior spinal levels. Dev Biol 261:99-115.
60. Patterson LT, Potter SS. 2003. Hox genes and kidney patterning. Curr Opin Nephrol Hypertens 12:19-23.
61. Prasad A, Hollyday M. 1991. Development and migration of avian sympathetic preganglionic neurons. J Comp Neurol 307:237-258.
62. Rijli FM, Matyas R, Pellegrini M, Dierich A, Gruss P, Dolle P, Chambon P. 1995. Cryptorchidism and homeotic transformations of spinal nerves and vertebrae in Hoxa-10 mutant mice. Proc Natl Acad Sci U S A 92:8185-8189.
63. Rodemer ES, Ihmer A, Wartenberg H. 1986. Gonadal development of the chick embryo following microsurgically caused agenesis of the mesonephros and using interspecific quail-chick chimaeras. J Embryol Exp Morphol 98:269-285.
64. Saltis J, Rush RA. 1995. The development of normal and peripherally deprived sympathetic neurons in the chick. J Auton Nerv Syst 51:117-127.
65. Sariola H, Holm-Sainio K, Henke-Fahle S. 1989. The effect of neuronal cells on kidney differentiation. Int J Dev Biol 33:149-155.
66. Schaeren-Wiemers N, Gerfin-Moser A. 1993. A single protocol to detect transcripts of various types and expression levels in neural tissue and cultured cells: in situ hybridization using digoxigenin-labelled cRNA probes. Histochemistry 100:431-440.
67. Scott MP. 1993. A rational nomenclature for vertebrate homeobox (HOX) genes. Nucleic Acids Res 21:1687-1688.
68. Sockanathan S, Jessell TM. 1998. Motor neuron-derived retinoid signaling specifies the subtype identity of spinal motor neurons. Cell 94:503-514.
69. Swartz M, Eberhart J, Mastick GS, Krull CE. 2001. Sparking new frontiers: using in vivo electroporation for genetic manipulations. Dev Biol 233:13-21.
70. Tiret L, Le Mouellic H, Maury M, 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.
71. Tosney KW. 1992. Growth cone navigation in the proximal environment of the chick embryo. In: Letourneau PC, Kater SB, Macagno ER, editors. The nerve growth cone. New York: Raven Press, Ltd. p 387-403.
72. Tsuchida T, Ensini M, Morton SB, Baldassare M, Edlund T, Jessell TM, Pfaff SL. 1994. Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes (see comments). Cell 79:957-970.
73. Wahba GM, Hostikka SL, Carpenter EM. 2001. The paralogous Hox genes Hoxa10 and Hoxd10 interact to pattern the mouse hindlimb peripheral nervous system and skeleton. Dev Biol 231:87-102.
74. Wellik DM, Capecchi MR. 2003. Hox10 and Hox11 genes are required to globally pattern the mammalian skeleton. Science 301:363-367.
75. Zakany J, Duboule D. 1999. Hox genes in digit development and evolution. Cell Tissue Res 296:19-25.