Chapter Six Hox Networks and the Origins of Motor Neuron Diversity

Current Topics in Developmental Biology

Volumn 88, Issue , 2009, Pages 169-200

  Dasen, Jeremy S ^a   Jessell, Thomas M ^b  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HOMEODOMAIN PROTEIN; TRANSCRIPTION FACTOR;

ANIMAL; BIOLOGICAL MODEL; CYTOLOGY; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; GROWTH, DEVELOPMENT AND AGING; HINDLIMB; METABOLISM; MOTONEURON; MOTOR ACTIVITY; PHYSIOLOGY; PRENATAL DEVELOPMENT; REVIEW;

ANIMALS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REGULATORY NETWORKS; HINDLIMB; HOMEODOMAIN PROTEINS; MODELS, BIOLOGICAL; MOTOR ACTIVITY; MOTOR NEURONS; TRANSCRIPTION FACTORS;

EID: 67949095557     PISSN: 00702153     EISSN: None     Source Type: Book Series    
DOI: 10.1016/S0070-2153(09)88006-X     Document Type: Review

References (109)

1. Agalliu D., Takada S., Agalliu I., McMahon A.P., and Jessell T.M. Motor neurons with axial muscle projections specified by Wnt4/5 signaling. Neuron 61 (2009) 708-720
2. Alvares L.E., Schubert F.R., Thorpe C., Mootoosamy R.C., Cheng L., Parkyn G., Lumsden A., and Dietrich S. Intrinsic, Hox-dependent cues determine the fate of skeletal muscle precursors. Dev. Cell 5 (2003) 379-390
3. Appel B., Korzh V., Glasgow E., Thor S., Edlund T., Dawid I.B., and Eisen J.S. Motoneuron fate specification revealed by patterned LIM homeobox gene expression in embryonic zebrafish. Development 121 (1995) 4117-4125
4. Arber S., Han B., Mendelsohn M., Smith M., Jessell T.M., and Sockanathan S. Requirement for the homeobox gene Hb9 in the consolidation of motor neuron identity. Neuron 23 (1999) 659-674
5. Belting H.G., Shashikant C.S., and Ruddle F.H. Multiple phases of expression and regulation of mouse Hoxc8 during early embryogenesis. J. Exp. Zool. 282 (1998) 196-222
6. Bel-Vialar S., Itasaki N., and Krumlauf R. Initiating Hox gene expression: In the early chick neural tube differential sensitivity to FGF and RA signaling subdivides the HoxB genes in two distinct groups. Development 129 (2002) 5103-5115
7. Borodinsky L.N., Root C.M., Cronin J.A., Sann S.B., Gu X., and Spitzer N.C. Activity-dependent homeostatic specification of transmitter expression in embryonic neurons. Nature 429 (2004) 523-530
8. Briscoe J., Pierani A., Jessell T.M., and Ericson J. A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell 101 (2000) 435-445
9. Brohmann H., Jagla K., and Birchmeier C. The role of Lbx1 in migration of muscle precursor cells. Development 127 (2000) 437-445
10. Carpenter E.M. Hox genes and spinal cord development. Dev. Neurosci. 24 (2002) 24-34
11. Choe A., Phun H.Q., Tieu D.D., Hu Y.H., and Carpenter E.M. Expression patterns of Hox10 paralogous genes during lumbar spinal cord development. Gene Expr. Patterns 6 (2006) 730-737
12. Chopra V.S., and Mishra R.K. "Mir"acles in Hox gene regulation. Bioessays 28 (2006) 445-448
13. Cohn M.J., Izpisua-Belmonte J.C., Abud H., Heath J.K., and Tickle C. Fibroblast growth factors induce additional limb development from the flank of chick embryos. Cell 80 (1995) 739-746
14. Cohn M.J., Patel K., Krumlauf R., Wilkinson D.G., Clarke J.D., and Tickle C. Hox9 genes and vertebrate limb specification. Nature 387 (1997) 97-101
15. Dasen J.S., Liu J.P., and Jessell T.M. Motor neuron columnar fate imposed by sequential phases of Hox-c activity. Nature 425 (2003) 926-933
16. Dasen J.S., Tice B.C., Brenner-Morton S., and Jessell T.M. A Hox regulatory network establishes motor neuron pool identity and target-muscle connectivity. Cell 123 (2005) 477-491
17. Dasen J.S., De Camilli A., Wang B., Tucker P.W., and Jessell T.M. Hox repertoires for motor neuron diversity and connectivity gated by a single accessory factor, FoxP1. Cell 134 (2008) 304-316
18. De Marco Garcia N.V., and Jessell T.M. Early motor neuron pool identity and muscle nerve trajectory defined by postmitotic restrictions in Nkx6.1 activity. Neuron 57 (2008) 217-231
19. Dessaud E., McMahon A.P., and Briscoe J. Pattern formation in the vertebrate neural tube: A sonic hedgehog morphogen-regulated transcriptional network. Development 135 (2008) 2489-2503
20. Diez del Corral R., and Storey K.G. Opposing FGF and retinoid pathways: A signalling switch that controls differentiation and patterning onset in the extending vertebrate body axis. Bioessays 26 (2004) 857-869
21. Duboule D., and Morata G. Colinearity and functional hierarchy among genes of the homeotic complexes. Trends Genet. 10 (1994) 358-364
22. Dubrulle J., and Pourquie O. fgf8 mRNA decay establishes a gradient that couples axial elongation to patterning in the vertebrate embryo. Nature 427 (2004) 419-422
23. Eberhart J., Swartz M.E., Koblar S.A., Pasquale E.B., and Krull C.E. EphA4 constitutes a population-specific guidance cue for motor neurons. Dev. Biol. 247 (2002) 89-101
24. Elowitz M.B., and Leibler S. A synthetic oscillatory network of transcriptional regulators. Nature 403 (2000) 335-338
25. Ensini M., Tsuchida T.N., Belting H.G., and Jessell T.M. 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 (1998) 969-982
26. Fetcho J.R. A review of the organization and evolution of motoneurons innervating the axial musculature of vertebrates. Brain Res. 434 (1987) 243-280
27. Fetcho J.R. The spinal motor system in early vertebrates and some of its evolutionary changes. Brain Behav. Evol. 40 (1992) 82-97
28. Force A., Amores A., and Postlethwait J.H. Hox cluster organization in the jawless vertebrate Petromyzon marinus. J. Exp. Zool. 294 (2002) 30-46
29. Freitas R., Zhang G., and Cohn M.J. Evidence that mechanisms of fin development evolved in the midline of early vertebrates. Nature 442 (2006) 1033-1037
30. Funakoshi K., and Nakano M. The sympathetic nervous system of anamniotes. Brain Behav. Evol. 69 (2007) 105-113
31. Gavalas A., Davenne M., Lumsden A., Chambon P., and Rijli F.M. Role of Hoxa-2 in axon pathfinding and rostral hindbrain patterning. Development 124 (1997) 3693-3702
32. Gebelein B., McKay D.J., and Mann R.S. Direct integration of Hox and segmentation gene inputs during Drosophila development. Nature 431 (2004) 653-659
33. Glover J.C., Renaud J.S., and Rijli F.M. Retinoic acid and hindbrain patterning. J. Neurobiol. 66 (2006) 705-725
34. Gross M.K., Moran-Rivard L., Velasquez T., Nakatsu M.N., Jagla K., and Goulding M. Lbx1 is required for muscle precursor migration along a lateral pathway into the limb. Development 127 (2000) 413-424
35. Guthrie S. Patterning and axon guidance of cranial motor neurons. Nat. Rev. Neurosci. 8 (2007) 859-871
36. Gutman C.R., Ajmera M.K., and Hollyday M. Organization of motor pools supplying axial muscles in the chicken. Brain Res. 609 (1993) 129-136
37. Haase G., Dessaud E., Garces A., de Bovis B., Birling M., Filippi P., Schmalbruch H., Arber S., and deLapeyriere O. GDNF acts through PEA3 to regulate cell body positioning and muscle innervation of specific motor neuron pools. Neuron 35 (2002) 893-905
38. Hollyday M. Motoneuron histogenesis and the development of limb innervation. Curr. Top. Dev. Biol. 15 (1980) 181-215
39. Hollyday M. Organization of motor pools in the chick lumbar lateral motor column. J. Comp. Neurol. 194 (1980) 143-170
40. Hollyday M. Chick wing innervation. I. Time course of innervation and early differentiation of the peripheral nerve pattern. J. Comp. Neurol. 357 (1995) 242-253
41. Hollyday M., and Jacobson R.D. Location of motor pools innervating chick wing. J. Comp. Neurol. 302 (1990) 575-588
42. Izpisua-Belmonte J.C., and Duboule D. Homeobox genes and pattern formation in the vertebrate limb. Dev. Biol. 152 (1992) 26-36
43. Jegalian B.G., and De Robertis E.M. Homeotic transformations in the mouse induced by overexpression of a human Hox3.3 transgene. Cell 71 (1992) 901-910
44. Jessell T.M. Neuronal specification in the spinal cord: Inductive signals and transcriptional codes. Nat. Rev. Genet. 1 (2000) 20-29
45. Joshi R., Passner J.M., Rohs R., Jain R., Sosinsky A., Crickmore M.A., Jacob V., Aggarwal A.K., Honig B., and Mann R.S. Functional specificity of a Hox protein mediated by the recognition of minor groove structure. Cell 131 (2007) 530-543
46. Kania A., and Jessell T.M. Topographic motor projections in the limb imposed by LIM homeodomain protein regulation of ephrin-A:EphA interactions. Neuron 38 (2003) 581-596
47. Kania A., Johnson R.L., and Jessell T.M. Coordinate roles for LIM homeobox genes in directing the dorsoventral trajectory of motor axons in the vertebrate limb. Cell 102 (2000) 161-173
48. Klausberger T., and Somogyi P. Neuronal diversity and temporal dynamics: The unity of hippocampal circuit operations. Science 321 (2008) 53-57
49. Kmita M., and Duboule D. Organizing axes in time and space; 25 years of colinear tinkering. Science 301 (2003) 331-333
50. Kong J.H., Fish D.R., Rockhill R.L., and Masland R.H. Diversity of ganglion cells in the mouse retina: Unsupervised morphological classification and its limits. J. Comp. Neurol. 489 (2005) 293-310
51. Kusakabe R., and Kuratani S. Evolution and developmental patterning of the vertebrate skeletal muscles: Perspectives from the lamprey. Dev. Dyn. 234 (2005) 824-834
52. Lance-Jones C., and Landmesser L. Motoneurone projection patterns in embryonic chick limbs following partial deletions of the spinal cord. J. Physiol. 302 (1980) 559-580
53. Lance-Jones C., Omelchenko N., Bailis A., Lynch S., and Sharma K. Hoxd10 induction and regionalization in the developing lumbosacral spinal cord. Development 128 (2001) 2255-2268
54. Landgraf M., and Thor S. Development of Drosophila motoneurons: Specification and morphology. Semin. Cell Dev. Biol. 17 (2006) 3-11
55. Landmesser L. The development of motor projection patterns in the chick hind limb. J. Physiol. 284 (1978) 391-414
56. Landmesser L. The distribution of motoneurones supplying chick hind limb muscles. J. Physiol. 284 (1978) 371-389
57. Landmesser L.T. The acquisition of motoneuron subtype identity and motor circuit formation. Int. J. Dev. Neurosci. 19 (2001) 175-182
58. Lemons D., and McGinnis W. Genomic evolution of Hox gene clusters. Science 313 (2006) 1918-1922
59. Lewis J., Chevallier A., Kieny M., and Wolpert L. Muscle nerve branches do not develop in chick wings devoid of muscle. J. Embryol. Exp. Morphol. 64 (1981) 211-232
60. Lin J.H., Saito T., Anderson D.J., Lance-Jones C., Jessell T.M., and Arber S. Functionally related motor neuron pool and muscle sensory afferent subtypes defined by coordinate ETS gene expression. Cell 95 (1998) 393-407
61. Liu J.P. The function of growth/differentiation factor 11 (Gdf11) in rostrocaudal patterning of the developing spinal cord. Development 133 (2006) 2865-2874
62. Liu J.P., Laufer E., and Jessell T.M. Assigning the positional identity of spinal motor neurons: Rostrocaudal patterning of Hox-c expression by FGFs, Gdf11, and retinoids. Neuron 32 (2001) 997-1012
63. Livet J., Sigrist M., Stroebel S., De Paola V., Price S.R., Henderson C.E., Jessell T.M., and Arber S. ETS gene Pea3 controls the central position and terminal arborization of specific motor neuron pools. Neuron 35 (2002) 877-892
64. Mann R.S., and Affolter M. Hox proteins meet more partners. Curr. Opin. Genet. Dev. 8 (1998) 423-429
65. McIntyre D.C., Rakshit S., Yallowitz A.R., Loken L., Jeannotte L., Capecchi M.R., and Wellik D.M. Hox patterning of the vertebrate rib cage. Development 134 (2007) 2981-2989
66. McPherron A.C., Lawler A.M., and Lee S.J. Regulation of anterior/posterior patterning of the axial skeleton by growth/differentiation factor 11. Nat. Genet. 22 (1999) 260-264
67. Milner L.D., and Landmesser L.T. Cholinergic and GABAergic inputs drive patterned spontaneous motoneuron activity before target contact. J. Neurosci. 19 (1999) 3007-3022
68. Moens C.B., and Selleri L. Hox cofactors in vertebrate development. Dev. Biol. 291 (2006) 193-206
69. Narayanan C.H., and Hamburger V. Motility in chick embryos with substitution of lumbosacral by brachial and brachial by lumbosacral spinal cord segments. J. Exp. Zool. 178 (1971) 415-431
70. Nonchev S., Maconochie M., Gould A., Morrison A., and Krumlauf R. Cross-regulatory interactions between Hox genes and the control of segmental expression in the vertebrate central nervous system. Cold Spring Harb. Symp. Quant. Biol. 62 (1997) 313-323
71. Nordstrom U., Maier E., Jessell T.M., and Edlund T. An early role for WNT signaling in specifying neural patterns of Cdx and Hox gene expression and motor neuron subtype identity. PLoS Biol. 4 (2006) e252
72. Novitch B.G., Chen A.I., and Jessell T.M. Coordinate regulation of motor neuron subtype identity and pan-neuronal properties by the bHLH repressor Olig2. Neuron 31 (2001) 773-789
73. O'Brien M.K., and Oppenheim R.W. Development and survival of thoracic motoneurons and hindlimb musculature following transplantation of the thoracic neural tube to the lumbar region in the chick embryo: Anatomical aspects. J. Neurobiol. 21 (1990) 313-340
74. O'Brien M.K., Landmesser L., and Oppenheim R.W. Development and survival of thoracic motoneurons and hindlimb musculature following transplantation of the thoracic neural tube to the lumbar region in the chick embryo: Functional aspects. J. Neurobiol. 21 (1990) 341-355
75. Pfaff S.L., Mendelsohn M., Stewart C.L., Edlund T., and Jessell T.M. Requirement for LIM homeobox gene Isl1 in motor neuron generation reveals a motor neuron-dependent step in interneuron differentiation. Cell 84 (1996) 309-320
76. Phelan K.A., and Hollyday M. Axon guidance in muscleless chick wings: The role of muscle cells in motoneuronal pathway selection and muscle nerve formation. J. Neurosci. 10 (1990) 2699-2716
77. Phelan K.A., and Hollyday M. Embryonic development and survival of brachial motoneurons projecting to muscleless chick wings. J. Comp. Neurol. 311 (1991) 313-320
78. Prasad A., and Hollyday M. Development and migration of avian sympathetic preganglionic neurons. J. Comp. Neurol. 307 (1991) 237-258
79. Price S.R., De Marco Garcia N.V., Ranscht B., and Jessell T.M. Regulation of motor neuron pool sorting by differential expression of type II cadherins. Cell 109 (2002) 205-216
80. Prud'homme B., Gompel N., and Carroll S.B. Emerging principles of regulatory evolution. Proc. Natl. Acad. Sci. USA 104 Suppl 1 (2007) 8605-8612
81. Romanes G.J. The development and significance of the cell columns in the ventral horn of the cervical and upper thoracic spinal cord of the rabbit. J. Anat. Lond. 76 (1942) 112-130
82. Rousso D.L., Gaber Z.B., Wellik D., Morrisey E.E., and Novitch B.G. Coordinated actions of the forkhead protein Foxp1 and Hox proteins in the columnar organization of spinal motor neurons. Neuron 59 (2008) 226-240
83. Saueressig H., Burrill J., and Goulding M. Engrailed-1 and netrin-1 regulate axon pathfinding by association interneurons that project to motor neurons. Development 126 (1999) 4201-4212
84. Shah V., Drill E., and Lance-Jones C. Ectopic expression of Hoxd10 in thoracic spinal segments induces motoneurons with a lumbosacral molecular profile and axon projections to the limb. Dev. Dyn. 231 (2004) 43-56
85. Sharma K., Sheng H.Z., Lettieri K., Li H., Karavanov A., Potter S., Westphal H., and Pfaff S.L. LIM homeodomain factors Lhx3 and Lhx4 assign subtype identities for motor neurons. Cell 95 (1998) 817-828
86. Sharma K., Leonard A.E., Lettieri K., and Pfaff S.L. Genetic and epigenetic mechanisms contribute to motor neuron pathfinding. Nature 406 (2000) 515-519
87. Sherrington C.S. The Integrative Action of the Nervous System. (1906), C. Scribner's sons, New York
88. Shieh P. The neofomation of cells of preganglionic type in the cervical spinal cord of the chick embryo following its transplantation to the thoracic level. J. Exp. Zool. 117 (1951) 359-395
89. Shimizu T., Bae Y.K., and Hibi M. Cdx-Hox code controls competence for responding to Fgfs and retinoic acid in zebrafish neural tissue. Development 133 (2006) 4709-4719
90. Shirasaki R., and Pfaff S.L. Transcriptional codes and the control of neuronal identity. Annu. Rev. Neurosci. 25 (2002) 251-281
91. Shu W., Yang H., Zhang L., Lu M.M., and Morrisey E.E. Characterization of a new subfamily of winged-helix/forkhead (Fox) genes that are expressed in the lung and act as transcriptional repressors. J. Biol. Chem. 276 (2001) 27488-27497
92. Shubin N., Tabin C., and Carroll S. Fossils, genes and the evolution of animal limbs. Nature 388 (1997) 639-648
93. Skromne I., Thorsen D., Hale M., Prince V.E., and Ho R.K. Repression of the hindbrain developmental program by Cdx factors is required for the specification of the vertebrate spinal cord. Development 134 (2007) 2147-2158
94. Sockanathan S., and Jessell T.M. Motor neuron-derived retinoid signaling specifies the subtype identity of spinal motor neurons. Cell 94 (1998) 503-514
95. Stirling R.V., and Summerbell D. Specific guidance of motor axons to duplicated muscles in the developing amniote limb. Development 103 (1988) 97-110
96. Takio Y., Kuraku S., Murakami Y., Pasqualetti M., Rijli F.M., Narita Y., Kuratani S., and Kusakabe R. Hox gene expression patterns in Lethenteron japonicum embryos-insights into the evolution of the vertebrate Hox code. Dev. Biol. 308 (2007) 606-620
97. Tamura S., Morikawa Y., Iwanishi H., Hisaoka T., and Senba E. Expression pattern of the winged-helix/forkhead transcription factor Foxp1 in the developing central nervous system. Gene Expr. Patterns 3 (2003) 193-197
98. Thaler J., Harrison K., Sharma K., Lettieri K., Kehrl J., and Pfaff S.L. Active suppression of interneuron programs within developing motor neurons revealed by analysis of homeodomain factor HB9. Neuron 23 (1999) 675-687
99. Thaler J.P., Koo S.J., Kania A., Lettieri K., Andrews S., Cox C., Jessell T.M., and Pfaff S.L. A postmitotic role for Isl-class LIM homeodomain proteins in the assignment of visceral spinal motor neuron identity. Neuron 41 (2004) 337-350
100. Tosney K.W., and Landmesser L.T. Development of the major pathways for neurite outgrowth in the chick hindlimb. Dev. Biol. 109 (1985) 193-214
101. Tosney K.W., and Landmesser L.T. Growth cone morphology and trajectory in the lumbosacral region of the chick embryo. J. Neurosci. 5 (1985) 2345-2358
102. Trainor P.A., and Krumlauf R. Patterning the cranial neural crest: Hindbrain segmentation and Hox gene plasticity. Nat. Rev. Neurosci. 1 (2000) 116-124
103. Tsuchida T., Ensini M., Morton S.B., Baldassare M., Edlund T., Jessell T.M., and Pfaff S.L. Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes. Cell 79 (1994) 957-970
104. Turney B.W., Rowan-Hull A.M., and Brown J.M. The innervation of FGF-induced additional limbs in the chick embryo. J. Anat. 202 (2003) 83-92
105. Vallstedt A., Muhr J., Pattyn A., Pierani A., Mendelsohn M., Sander M., Jessell T.M., and Ericson J. Different levels of repressor activity assign redundant and specific roles to Nkx6 genes in motor neuron and interneuron specification. Neuron 31 (2001) 743-755
106. Vermot J., Schuhbaur B., Le Mouellic H., McCaffery P., Garnier J.M., Hentsch D., Brulet P., Niederreither K., Chambon P., and Dolle P. 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 (2005) 1611-1621
107. Vrieseling E., and Arber S. Target-induced transcriptional control of dendritic patterning and connectivity in motor neurons by the ETS gene Pea3. Cell 127 (2006) 1439-1452
108. William C.M., Tanabe Y., and Jessell T.M. Regulation of motor neuron subtype identity by repressor activity of Mnx class homeodomain proteins. Development 130 (2003) 1523-1536
109. Zhou Q., and Anderson D.J. The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell 109 (2002) 61-73