Evolution of patterning systems and circuit elements for locomotion

Developmental Cell

Volumn 32, Issue 4, 2015, Pages 408-422

  Jung, Heekyung ^a   Dasen, Jeremy S ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

NEUROTRANSMITTER;

BILATERIA; CELL FATE; GAIT; HOX GENE; INTERNEURON; LOCOMOTION; MOTOR SYSTEM; MUSCLE INNERVATION; NEUROMODULATION; NONHUMAN; PRIORITY JOURNAL; REVIEW; SPINAL CORD; ANIMAL; EVOLUTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; MORPHOGENESIS; NERVOUS SYSTEM; PHYSIOLOGY; SIGNAL TRANSDUCTION; VERTEBRATE;

ANIMALIA; BILATERIA;

ANIMALS; BIOLOGICAL EVOLUTION; BODY PATTERNING; HUMANS; LOCOMOTION; NERVOUS SYSTEM; SIGNAL TRANSDUCTION; VERTEBRATES;

EID: 84923239753     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2015.01.008     Document Type: Review

References (107)

1. Ampatzis K., Song J., Ausborn J., El Manira A. Pattern of innervation and recruitment of different classes of motoneurons in adult zebrafish. J.Neurosci. 2013, 33:10875-10886.
2. Andersson L.S., Larhammar M., Memic F., Wootz H., Schwochow D., Rubin C.J., Patra K., Arnason T., Wellbring L., Hjälm G., et al. Mutations in DMRT3 affect locomotion in horses and spinal circuit function in mice. Nature 2012, 488:642-646.
3. Appel B., Korzh V., Glasgow E., Thor S., Edlund T., Dawid I.B., Eisen J.S. Motoneuron fate specification revealed by patterned LIM homeobox gene expression in embryonic zebrafish. Development 1995, 121:4117-4125.
4. Arber S. Motor circuits in action: specification, connectivity, and function. Neuron 2012, 74:975-989.
5. Arber S., Han B., Mendelsohn M., Smith M., Jessell T.M., Sockanathan S. Requirement for the homeobox gene Hb9 in the consolidation of motor neuron identity. Neuron 1999, 23:659-674.
6. Arendt D., Nübler-Jung K. Inversion of dorsoventral axis?. Nature 1994, 371:26.
7. Azim E., Jiang J., Alstermark B., Jessell T.M. Skilled reaching relies on a V2a propriospinal internal copy circuit. Nature 2014, 508:357-363.
8. Baek M., Enriquez J., Mann R.S. Dual role for Hox genes and Hox co-factors in conferring leg motoneuron survival and identity in Drosophila. Development 2013, 140:2027-2038.
9. Bagnall M.W., McLean D.L. Modular organization of axial microcircuits in zebrafish. Science 2014, 343:197-200.
10. Begemann G., Schilling T.F., Rauch G.J., Geisler R., Ingham P.W. The zebrafish neckless mutation reveals a requirement for raldh2 in mesodermal signals that pattern the hindbrain. Development 2001, 128:3081-3094.
11. Bernhardt N.R., Memic F., Kullander K. Genetic analysis of left-right coordination of locomotion. Front. Biosci. (Landmark Ed.) 2013, 18:21-35.
12. Berni J., Pulver S.R., Griffith L.C., Bate M. Autonomous circuitry for substrate exploration in freely moving Drosophila larvae. Curr. Biol. 2012, 22:1861-1870.
13. Bertrand S., Camasses A., Somorjai I., Belgacem M.R., Chabrol O., Escande M.L., Pontarotti P., Escriva H. Amphioxus FGF signaling predicts the acquisition of vertebrate morphological traits. Proc. Natl. Acad. Sci. USA 2011, 108:9160-9165.
14. Bronner M.E., LeDouarin N.M. Development and evolution of the neural crest: an overview. Dev. Biol. 2012, 366:2-9.
15. Cho H.H., Cargnin F., Kim Y., Lee B., Kwon R.J., Nam H., Shen R., Barnes A.P., Lee J.W., Lee S., Lee S.K. Isl1 directly controls a cholinergic neuronal identity in the developing forebrain and spinal cord by forming cell type-specific complexes. PLoS Genet. 2014, 10:e1004280.
16. Crone S.A., Zhong G., Harris-Warrick R., Sharma K. In mice lacking V2a interneurons, gait depends on speed of locomotion. J.Neurosci. 2009, 29:7098-7109.
17. Dasen J.S., Jessell T.M. Hox networks and the origins of motor neuron diversity. Curr. Top. Dev. Biol. 2009, 88:169-200.
18. Dasen J.S., Liu J.P., Jessell T.M. Motor neuron columnar fate imposed by sequential phases of Hox-c activity. Nature 2003, 425:926-933.
19. Dasen J.S., Tice B.C., Brenner-Morton S., Jessell T.M. A Hox regulatory network establishes motor neuron pool identity and target-muscle connectivity. Cell 2005, 123:477-491.
20. Dasen J.S., De Camilli A., Wang B., Tucker P.W., Jessell T.M. Hox repertoires for motor neuron diversity and connectivity gated by a single accessory factor, FoxP1. Cell 2008, 134:304-316.
21. De Robertis E.M. Evo-devo: variations on ancestral themes. Cell 2008, 132:185-195.
22. De Robertis E.M., Sasai Y. A common plan for dorsoventral patterning in Bilateria. Nature 1996, 380:37-40.
23. Demireva E.Y., Shapiro L.S., Jessell T.M., Zampieri N. Motor neuron position and topographic order imposed by β- and γ-catenin activities. Cell 2011, 147:641-652.
24. Deneris E.S., Hobert O. Maintenance of postmitotic neuronal cell identity. Nat. Neurosci. 2014, 17:899-907.
25. Denes A.S., Jékely G., Steinmetz P.R., Raible F., Snyman H., Prud'homme B., Ferrier D.E., Balavoine G., Arendt D. Molecular architecture of annelid nerve cord supports common origin of nervous system centralization in bilateria. Cell 2007, 129:277-288.
26. Dixit R., Vijayraghavan K., Bate M. Hox genes and the regulation of movement in Drosophila. Dev. Neurobiol. 2008, 68:309-316.
27. Droge M.H., Leonard R.B. Organization of spinal motor nuclei in the stingray, Dasyatis sabina. Brain Res. 1983, 276:201-211.
28. Esposito M.S., Capelli P., Arber S. Brainstem nucleus MdV mediates skilled forelimb motor tasks. Nature 2014, 508:351-356.
29. Esteves F.F., Springhorn A., Kague E., Taylor E., Pyrowolakis G., Fisher S., Bier E. BMPs regulate msx gene expression in the dorsal neuroectoderm of Drosophila and vertebrates by distinct mechanisms. PLoS Genet. 2014, 10:e1004625.
30. Fetcho J.R. A review of the organization and evolution of motoneurons innervating the axial musculature of vertebrates. Brain Res. 1987, 434:243-280.
31. Fetcho J.R. The spinal motor system in early vertebrates and some of its evolutionary changes. Brain Behav. Evol. 1992, 40:82-97.
32. Flames N., Hobert O. Gene regulatory logic of dopamine neuron differentiation. Nature 2009, 458:885-889.
33. Gehring W.J. The evolution of vision. Wiley Interdiscip. Rev. Dev. Biol. 2014, 3:1-40.
34. Goulding M., Pfaff S.L. Development of circuits that generate simple rhythmic behaviors in vertebrates. Curr. Opin. Neurobiol. 2005, 15:14-20.
35. Grillner S., Jessell T.M. Measured motion: searching for simplicity in spinal locomotor networks. Curr. Opin. Neurobiol. 2009, 19:572-586.
36. Halder G., Callaerts P., Gehring W.J. Induction of ectopic eyes by targeted expression of the eyeless gene in Drosophila. Science 1995, 267:1788-1792.
37. Hirasawa T., Kuratani S. A new scenario of the evolutionary derivation of the mammalian diaphragm from shoulder muscles. J.Anat. 2013, 222:504-517.
38. Hirth F., Kammermeier L., Frei E., Walldorf U., Noll M., Reichert H. An urbilaterian origin of the tripartite brain: developmental genetic insights from Drosophila. Development 2003, 130:2365-2373.
39. Hobert O. Regulation of terminal differentiation programs in the nervous system. Annu. Rev. Cell Dev. Biol. 2011, 27:681-696.
40. Holland N.D. Early central nervous system evolution: an era of skin brains?. Nat. Rev. Neurosci. 2003, 4:617-627.
41. Holland L.Z., Holland N.N., Schubert M. Developmental expression of AmphiWnt1, an amphioxus gene in the Wnt1/wingless subfamily. Dev. Genes Evol. 2000, 210:522-524.
42. Holley S.A., Jackson P.D., Sasai Y., Lu B., De Robertis E.M., Hoffmann F.M., Ferguson E.L. A conserved system for dorsal-ventral patterning in insects and vertebrates involving sog and chordin. Nature 1995, 376:249-253.
43. Imai K.S., Stolfi A., Levine M., Satou Y. Gene regulatory networks underlying the compartmentalization of the Ciona central nervous system. Development 2009, 136:285-293.
44. Irimia M., Piñeiro C., Maeso I., Gómez-Skarmeta J.L., Casares F., Garcia-Fernàndez J. Conserved developmental expression of Fezf in chordates and Drosophila and the origin of the Zona Limitans Intrathalamica (ZLI) brain organizer. Evodevo 2010, 1:7.
45. Jessell T.M. Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev. Genet. 2000, 1:20-29.
46. Jung H., Lacombe J., Mazzoni E.O., Liem K.F., Grinstein J., Mahony S., Mukhopadhyay D., Gifford D.K., Young R.A., Anderson K.V., et al. Global control of motor neuron topography mediated by the repressive actions of a single hox gene. Neuron 2010, 67:781-796.
47. Jung H., Mazzoni E.O., Soshnikova N., Hanley O., Venkatesh B., Duboule D., Dasen J.S. Evolving Hox activity profiles govern diversity in locomotor systems. Dev. Cell 2014, 29:171-187.
48. Kammermeier L., Leemans R., Hirth F., Flister S., Wenger U., Walldorf U., Gehring W.J., Reichert H. Differential expression and function of the Drosophila Pax6 genes eyeless and twin of eyeless in embryonic central nervous system development. Mech. Dev. 2001, 103:71-78.
49. Kao T.J., Law C., Kania A. Eph and ephrin signaling: lessons learned from spinal motor neurons. Semin. Cell Dev. Biol. 2012, 23:83-91.
50. Karlsson D., Baumgardt M., Thor S. Segment-specific neuronal subtype specification by the integration of anteroposterior and temporal cues. PLoS Biol. 2010, 8:e1000368.
51. King B.L., Gillis J.A., Carlisle H.R., Dahn R.D. A natural deletion of the HoxC cluster in elasmobranch fishes. Science 2011, 334:1517.
52. Kjaerulff O., Kiehn O. Distribution of networks generating and coordinating locomotor activity in the neonatal rat spinal cord invitro: a lesion study. J.Neurosci. 1996, 16:5777-5794.
53. Kohwi M., Doe C.Q. Temporal fate specification and neural progenitor competence during development. Nat. Rev. Neurosci. 2013, 14:823-838.
54. Kratsios P., Stolfi A., Levine M., Hobert O. Coordinated regulation of cholinergic motor neuron traits through a conserved terminal selector gene. Nat. Neurosci. 2012, 15:205-214.
55. Kullander K., Butt S.J., Lebret J.M., Lundfald L., Restrepo C.E., Rydström A., Klein R., Kiehn O. Role of EphA4 and EphrinB3 in local neuronal circuits that control walking. Science 2003, 299:1889-1892.
56. Lacin H., Zhu Y., Wilson B.A., Skeath J.B. Transcription factor expression uniquely identifies most postembryonic neuronal lineages in the Drosophila thoracic central nervous system. Development 2014, 141:1011-1021.
57. Lacombe J., Hanley O., Jung H., Philippidou P., Surmeli G., Grinstein J., Dasen J.S. Genetic and functional modularity of Hox activities in the specification of limb-innervating motor neurons. PLoS Genet. 2013, 9:e1003184.
58. Landgraf M., Thor S. Development of Drosophila motoneurons: specification and morphology. Semin. Cell Dev. Biol. 2006, 17:3-11.
59. Lanuza G.M., Gosgnach S., Pierani A., Jessell T.M., Goulding M. Genetic identification of spinal interneurons that coordinate left-right locomotor activity necessary for walking movements. Neuron 2004, 42:375-386.
60. Lee S., Lee B., Joshi K., Pfaff S.L., Lee J.W., Lee S.K. A regulatory network to segregate the identity of neuronal subtypes. Dev. Cell 2008, 14:877-889.
61. Lee S., Cuvillier J.M., Lee B., Shen R., Lee J.W., Lee S.K. Fusion protein Isl1-Lhx3 specifies motor neuron fate by inducing motor neuron genes and concomitantly suppressing the interneuron programs. Proc. Natl. Acad. Sci. USA 2012, 109:3383-3388.
62. Liu J.P., Laufer E., Jessell T.M. Assigning the positional identity of spinal motor neurons: rostrocaudal patterning of Hox-c expression by FGFs, Gdf11, and retinoids. Neuron 2001, 32:997-1012.
63. Livet J., Sigrist M., Stroebel S., De Paola V., Price S.R., Henderson C.E., Jessell T.M., Arber S. ETS gene Pea3 controls the central position and terminal arborization of specific motor neuron pools. Neuron 2002, 35:877-892.
64. Lopes R., Verhey van Wijk N., Neves G., Pachnis V. Transcription factor LIM homeobox 7 (Lhx7) maintains subtype identity of cholinergic interneurons in the mammalian striatum. Proc. Natl. Acad. Sci. USA 2012, 109:3119-3124.
65. Lowe C.J., Wu M., Salic A., Evans L., Lander E., Stange-Thomann N., Gruber C.E., Gerhart J., Kirschner M. Anteroposterior patterning in hemichordates and the origins of the chordate nervous system. Cell 2003, 113:853-865.
66. Lowe C.J., Terasaki M., Wu M., Freeman R.M., Runft L., Kwan K., Haigo S., Aronowicz J., Lander E., Gruber C., et al. Dorsoventral patterning in hemichordates: insights into early chordate evolution. PLoS Biol. 2006, 4:e291.
67. Ma L.H., Gilland E., Bass A.H., Baker R. Ancestry of motor innervation to pectoral fin and forelimb. Nat. Commun. 2010, 1:49.
68. Macesic L.J., Kajiura S.M. Comparative punting kinematics and pelvic fin musculature of benthic batoids. J.Morphol. 2010, 271:1219-1228.
69. Masland R.H. Neuronal cell types. Curr. Biol. 2004, 14:R497-R500.
70. Maxwell E.E., Fröbisch N.B., Heppleston A.C. Variability and conservation in late chondrichthyan development: ontogeny of the winter skate (Leucoraja ocellata). Anat. Rec. (Hoboken) 2008, 291:1079-1087.
71. McGinnis W., Krumlauf R. Homeobox genes and axial patterning. Cell 1992, 68:283-302.
72. Menelaou E., McLean D.L. A gradient in endogenous rhythmicity and oscillatory drive matches recruitment order in an axial motor pool. J.Neurosci. 2012, 32:10925-10939.
73. Miyamoto N., Wada H. Hemichordate neurulation and the origin of the neural tube. Nat. Commun. 2013, 4:2713.
74. Mizutani C.M., Bier E. EvoD/Vo: the origins of BMP signalling in the neuroectoderm. Nat. Rev. Genet. 2008, 9:663-677.
75. Murakami Y., Tanaka M. Evolution of motor innervation to vertebrate fins and limbs. Dev. Biol. 2011, 355:164-172.
76. Murata Y., Tamura M., Aita Y., Fujimura K., Murakami Y., Okabe M., Okada N., Tanaka M. Allometric growth of the trunk leads to the rostral shift of the pelvic fin in teleost fishes. Dev. Biol. 2010, 347:236-245.
77. Myers P.Z. Spinal motoneurons of the larval zebrafish. J.Comp. Neurol. 1985, 236:555-561.
78. Narayanan C.H., Hamburger V. Motility in chick embryos with substitution of lumbosacral by brachial and brachial by lumbosacral spinal cord segments. J.Exp. Zool. 1971, 178:415-431.
79. Nomaksteinsky M., Röttinger E., Dufour H.D., Chettouh Z., Lowe C.J., Martindale M.Q., Brunet J.F. Centralization of the deuterostome nervous system predates chordates. Curr. Biol. 2009, 19:1264-1269.
80. Pani A.M., Mullarkey E.E., Aronowicz J., Assimacopoulos S., Grove E.A., Lowe C.J. Ancient deuterostome origins of vertebrate brain signalling centres. Nature 2012, 483:289-294.
81. Parker H.J., Bronner M.E., Krumlauf R. A Hox regulatory network of hindbrain segmentation is conserved to the base of vertebrates. Nature 2014, 514:490-493.
82. Philippe H., Brinkmann H., Copley R.R., Moroz L.L., Nakano H., Poustka A.J., Wallberg A., Peterson K.J., Telford M.J. Acoelomorph flatworms are deuterostomes related to Xenoturbella. Nature 2011, 470:255-258.
83. Philippidou P., Dasen J.S. Hox genes: choreographers in neural development, architects of circuit organization. Neuron 2013, 80:12-34.
84. Philippidou P., Walsh C.M., Aubin J., Jeannotte L., Dasen J.S. Sustained Hox5 gene activity is required for respiratory motor neuron development. Nat. Neurosci. 2012, 15:1636-1644.
85. Price S.R., De Marco Garcia N.V., Ranscht B., Jessell T.M. Regulation of motor neuron pool sorting by differential expression of type II cadherins. Cell 2002, 109:205-216.
86. Rabe N., Gezelius H., Vallstedt A., Memic F., Kullander K. Netrin-1-dependent spinal interneuron subtypes are required for the formation of left-right alternating locomotor circuitry. J.Neurosci. 2009, 29:15642-15649.
87. Rousso D.L., Gaber Z.B., Wellik D., Morrisey E.E., Novitch B.G. Coordinated actions of the forkhead protein Foxp1 and Hox proteins in the columnar organization of spinal motor neurons. Neuron 2008, 59:226-240.
88. Seredick S.D., Van Ryswyk L., Hutchinson S.A., Eisen J.S. Zebrafish Mnx proteins specify one motoneuron subtype and suppress acquisition of interneuron characteristics. Neural Dev. 2012, 7:35.
89. Serrano-Saiz E., Poole R.J., Felton T., Zhang F., De La Cruz E.D., Hobert O. Modular control of glutamatergic neuronal identity in C. elegans by distinct homeodomain proteins. Cell 2013, 155:659-673.
90. Sharma K., Leonard A.E., Lettieri K., Pfaff S.L. Genetic and epigenetic mechanisms contribute to motor neuron pathfinding. Nature 2000, 406:515-519.
91. Shim S., Kwan K.Y., Li M., Lefebvre V., Sestan N. Cis-regulatory control of corticospinal system development and evolution. Nature 2012, 486:74-79.
92. Shimeld S.M. The evolution of the hedgehog gene family in chordates: insights from amphioxus hedgehog. Dev. Genes Evol. 1999, 209:40-47.
93. Sillar K.T., Combes D., Ramanathan S., Molinari M., Simmers J. Neuromodulation and developmental plasticity in the locomotor system of anuran amphibians during metamorphosis. Brain Res. Brain Res. Rev. 2008, 57:94-102.
94. Steinmetz P.R., Kostyuchenko R.P., Fischer A., Arendt D. The segmental pattern of otx, gbx, and Hox genes in the annelid Platynereis dumerilii. Evol. Dev. 2011, 13:72-79.
95. Straznicky K. Function of Heterotopic Spinal Cord Segments Investigation in the Chick. Acta. Biol. Acad. Sci. Hung. 1963, 14:143-153.
96. Sürmeli G., Akay T., Ippolito G.C., Tucker P.W., Jessell T.M. Patterns of spinal sensory-motor connectivity prescribed by a dorsoventral positional template. Cell 2011, 147:653-665.
97. Takatori N., Satou Y., Satoh N. Expression of hedgehog genes in Ciona intestinalis embryos. Mech. Dev. 2002, 116:235-238.
98. Takio Y., Kuraku S., Murakami Y., Pasqualetti M., Rijli F.M., Narita Y., Kuratani S., Kusakabe R. Hox gene expression patterns in Lethenteron japonicum embryos-insights into the evolution of the vertebrate Hox code. Dev. Biol. 2007, 308:606-620.
99. Talpalar A.E., Bouvier J., Borgius L., Fortin G., Pierani A., Kiehn O. Dual-mode operation of neuronal networks involved in left-right alternation. Nature 2013, 500:85-88.
100. Thaler J., Harrison K., Sharma K., Lettieri K., Kehrl J., Pfaff S.L. Active suppression of interneuron programs within developing motor neurons revealed by analysis of homeodomain factor HB9. Neuron 1999, 23:675-687.
101. Thor S., Thomas J.B. Motor neuron specification in worms, flies and mice: conserved and 'lost' mechanisms. Curr. Opin. Genet. Dev. 2002, 12:558-564.
102. Tsuchida T., Ensini M., Morton S.B., Baldassare M., Edlund T., Jessell T.M., Pfaff S.L. Topographic organization of embryonic motor neurons defined by expression of LIM homeobox genes. Cell 1994, 79:957-970.
103. Uemura O., Okada Y., Ando H., Guedj M., Higashijima S., Shimazaki T., Chino N., Okano H., Okamoto H. Comparative functional genomics revealed conservation and diversification of three enhancers of the isl1 gene for motor and sensory neuron-specific expression. Dev. Biol. 2005, 278:587-606.
104. Vallstedt A., Kullander K. Dorsally derived spinal interneurons in locomotor circuits. Ann. N Y Acad. Sci. 2013, 1279:32-42.
105. Zarin A.A., Asadzadeh J., Labrador J.P. Transcriptional regulation of guidance at the midline and in motor circuits. Cell. Mol. Life Sci. 2014, 71:419-432.
106. Zhang Y., Narayan S., Geiman E., Lanuza G.M., Velasquez T., Shanks B., Akay T., Dyck J., Pearson K., Gosgnach S., et al. V3 spinal neurons establish a robust and balanced locomotor rhythm during walking. Neuron 2008, 60:84-96.
107. Zhang F., Bhattacharya A., Nelson J.C., Abe N., Gordon P., Lloret-Fernandez C., Maicas M., Flames N., Mann R.S., Colón-Ramos D.A., Hobert O. The LIM and POU homeobox genes ttx-3 and unc-86 act as terminal selectors in distinct cholinergic and serotonergic neuron types. Development 2014, 141:422-435.