Patterning of the vertebrate ventral spinal cord

International Journal of Developmental Biology

Volumn 46, Issue 4 SPEC., 2002, Pages 597-608

  Poh, Alisa ^a,b   Karunaratne, Asanka ^a   Kolle, Gabriel ^a   Huang, Ning ^a   Smith, Emma ^a   Starkey, Joanna ^a   Wen, Daying ^a   Wilson, Ian ^a   Yamada, Toshiya ^a   Hargrave, Murray ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Interneuron; Motor neuron; Patterning; Sonic hedgehog; Spinal cord

Indexed keywords

HOMEODOMAIN PROTEIN; MORPHOGEN; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR; TRANSACTIVATOR PROTEIN;

ANIMAL TISSUE; BRAIN DEVELOPMENT; CHICKEN; CONCENTRATION RESPONSE; CONTROLLED STUDY; EMBRYO; INHIBITION KINETICS; MOLECULAR DYNAMICS; MORPHOGENESIS; NERVE CELL NETWORK; NEURAL TUBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; SPINAL CORD VENTRAL HORN; VERTEBRATE; ANIMAL; BIOLOGICAL MODEL; CHICK EMBRYO; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; METABOLISM; NERVE CELL; PATHOLOGY; PHYSIOLOGY; PRENATAL DEVELOPMENT; PROTEIN TERTIARY STRUCTURE; SPINAL CORD; TIME;

ANIMALIA; ERINACEIDAE; GALLUS GALLUS; VERTEBRATA;

ANIMALS; CHICK EMBRYO; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; MODELS, BIOLOGICAL; NEURONS; PROTEIN STRUCTURE, TERTIARY; SIGNAL TRANSDUCTION; SPINAL CORD; TIME FACTORS; TRANS-ACTIVATORS; TRANSCRIPTION, GENETIC;

EID: 0036357186     PISSN: 02146282     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (92)

1. BARTH, K. A., KISHIMOTO, Y., ROHR, K. B., SEYDLER, C., SCHULTE-MERKER, S., and WILSON, S. W. (1999). Bmp activity establishes a gradient of positional information throughout the entire neural plate. Development 126: 4977-4987.
2. BELLONI, E., MUENKE, M., ROESSLER, E., TRAVERSO, G., SIEGEL-BARTELT, J., FRUMKIN, A., MITCHELL, H. F., H., D.-K., HELMS, C., HING, A. V., HENG, H. H., KOOP, B., MARTINDALE, D., ROMMENS, J. M., TSUI, L. C. and SCHERER, S. W. (1996). Identification of Sonic hedgehog as a candidate gene responsible for holoprosencephaly. Nat. Genet. 14: 353-356.
3. BINNS, W., JAMES, L. F., SHUPE, J. L., and EVERETT, G. (1963). A congenital cylcopian-type malformation in lambs induced by maternal ingestion of a range plant, Veratrum californicum. Am. J. Vet. Res. 24: 1164-1175.
4. BRISCOE, J., CHEN, Y., JESSELL, T. M., and STRUHL, G. (2001). A hedgehog-insensitive form of patched provides evidence for direct long-range morphogen activity of sonic hedgehog in the neural tube. Mol. Cell 7: 1279-1291.
5. BRISCOE, J., PIERANI, A., JESSELL, T. M. and ERICSON, J. (2000). A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell 101: 435-445.
6. 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.
7. BROWN, A. G. (1981). Organization in the spinal cord: the anatomy and physiology of identified neurones. Springer-Verlag, Berlin.
8. BRUNEAU, S., and ROSA, F. M. (1997). Dynamo, a new zebrafish DVR member of the TGF-beta superfamily is expressed in the posterior neural tube and is up-regulated by Sonic hedgehog. Mech. Dev. 61: 199-212.
9. + interneurons that require PAX6 for their development. Development 124: 4493-4503.
10. CHIANG, C., LITINGTUNG, Y., LEE, E., YOUNG, K. E., CORDEN, J. L., WESTPHAL, H. and BEACHY, P. A. (1996). Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383: 407-413.
11. COOPER, M. K., PORTER, J. A., YOUNG, K. E. and BEACHY, P. A. (1998). Teratogen-mediated inhibition of target tissue response to Shh signaling. Science 280: 1603-1607.
12. ENSINI, M., TSUCHIDA, T. N., BELTING, H. G., and JESSELL, T. M. (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.
13. ERICSON, J., RASHBASS, P., SCHEDL, A., BRENNER-MORTON, S., KAWAKAMI, A., VAN HEYNINGEN, V., JESSELL, T. M. and BRISCOE, J. (1997). Pax6 controls progenitor cell identity and neuronal fate in response to graded Shh signalling. Cell 90: 169-180.
14. ERICSON, J., MORTON, S., KAWAKAMI, A., ROELINK, H. and JESSELL, T. M. (1996). Two critical periods of Sonic Hedgehog signaling required for the specification of motor neuron identity. Cell 87: 661-673.
15. 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.
16. GOODRICH, L. V., JOHNSON, R. L., MILENKOVIC, L., MCMAHON, J. A. and SCOTT, M. P. (1996). Conservation of the hedgehog/patched signaling pathway from flies to mice: induction of a mouse patched gene by Hedgehog. Genes Dev. 10: 301-312.
17. GOULDING, M. (1998). Specifying motor neurons and their connections. Neuron 21: 943-946.
18. GOULDING, M. D., LUMSDEN, A. and GRUSS, P. (1993). Signals from the notochord and floor plate regulate the region-specific expression of two Pax genes in the developing spinal cord. Development 117: 1001-1016.
19. HAMBURGER, V. and HAMILTON, H. L. (1951). A series of normal stages in the development of the chick embryo. J. Morphol. 88: 49-92.
20. HARGRAVE, M., KARUNARATNE, A., COX, L., WOOD, S., KOOPMAN, P. and YAMADA, T. (2000). The HMG box transcription factor gene Sox14 marks a novel subset of ventral interneurons and is regulated by sonic hedgehog. Dev. Biol. 219: 142-153.
21. HYNES, M., YE, W., WANG, K., STONE, D., MURONE, M., SAUVAGE, F., and ROSENTHAL, A. (2000). The seven-transmembrane receptor smoothened cell-autonomously induces multiple ventral cell types. Nat. Neurosci. 3: 41-46.
22. INCARDONA, J. P., GAFFIELD, W., KAPUR, R. P. and ROELINK, H. (1998). The teratogenic Veratrum alkaloid cyclopamine inhibits sonic hedgehog signal transduction. Development 125: 3553-3562.
23. INGHAM, P. W. (2001) Hedgehog signalling: a tale of two lipids. Science 294: 1879-1881.
24. JESSELL, T. M. (2000). Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev. Genet. 1: 20-29.
25. JESSELL, T. M. and MELTON, D. A. (1992). Diffusible factors in vertebrate embryonic induction. Cell 68: 257-270.
26. JONES, C. M., LYONS, K. M., and HOGAN, B. L. (1991). Involvement of Bone Morphogenetic Protein-4 (BMP-4) and Vgr-1 in morphogenesis and neurogenesis in the mouse. Development 111: 531-542.
27. JUNGBLUTH, S., BELL, E., and LUMSDEN, A. (1999). Specification of distinct motor neuron identities by the singular activities of individual Hox genes. Development 126: 2751-2758.
28. KALDERON, D. (2000). Transducing the hedgehog signal. Cell 103: 371-374.
29. KARUNARATNE, A., HARGRAVE, M., POH, A. and YAMADA, T. GATA proteins identify a novel ventral interneuron subclass in the developing chick spinal cord. Manuscript submitted.
30. KEELER, R. F. (1969). Teratogenic compounds of Veratrum californicum (Durand). VII. The structure of the glycosidic alkaloid cycloposine. Steroids 13: 579-588.
31. KOLLE, G., GEORGAS, K., HOLMES, G. P., LITTLE, M. H., and YAMADA, T. (2000). CRIM1, a novel gene encoding a cysteine-rich repeat protein, is developmentally regulated and implicated in vertebrate CNS development and organogenesis. Mech. Dev. 90: 181-193.
32. LANGMAN, J., and HADEN, C. C. (1970). Formation and migration of neuroblasts in the spinal cord of the chick embryo. J. Comp. Neurol 138: 419-425.
33. LANGMAN, J., GUERRANT, R. L., and FREEMAN, B. G. (1966). Behavior of neuroepithelial cells during closure of the neural tube. J. Comp. Neurol 127: 399-411.
34. LEE, J. J., VON KESSLER, D. P., PARKS, S. and BEACHY, P. A. (1992). Secretion and localized transcription suggest a role in positional signaling for products of the segmentation gene hedgehog. Cell 71: 33-50.
35. LEE, K. J., DIETRICH, P. and JESSELL, T. M. (2000). Genetic ablation reveals that the roof plate is essential for dorsal interneuron specification. Nature 403: 734-740.
36. LEE, K. J., MENDELSOHN, M. and JESSELL, T. M. (1998). Neuronal patterning by BMPs: a requirement for GDF7 in the generation of a discrete class of commissural interneurons in the mouse spinal cord. Genes Dev. 12: 3394-3407.
37. LIEM, K. F., JR., JESSELL, T. M., and BRISCOE, J. (2000). Regulation of the neural patterning activity of sonic hedgehog by secreted BMP inhibitors expressed by notochord and somites. Development 127: 4855-4866.
38. LIEM, K. F. J., TREMML, G. and JESSELL, T. M. (1997). A role for the roof plate and its resident TGF-related proteins in neuronal patterning in the dorsal spinal cord. Cell 91: 127-138.
39. LIEM, K. F., JR., TREMML, G., ROELINK, H. and JESSELL, T. M. (1995). Dorsal differentiation of neural plate cells induced by BMP-mediated signals from epidermal ectoderm. Cell 82: 969-979.
40. LITINGTUNG, Y., and CHIANG, C. (2000). Specification of ventral neuron types is mediated by an antagonistic interaction between Shh and Gli3. Nat. Neurosci. 3: 979-985.
41. LUMSDEN, A. and KRUMLAUF, R. (1996). Patterning the vertebrate neuraxis. Science 274: 1109-1115.
42. MANSOURI, A. and GRUSS, P. (1998). Pax3 and Pax7 are expressed in commissural neurons and restrict ventral neuronal identity in the spinal cord. Mech. Dev. 78: 171-178.
43. MARIGO, V., and TABIN, C. J. (1996). Regulation of patched by sonic hedgehog in the developing neural tube. Proc. Natl Acad Sci. USA 93: 9346-9351.
44. MARTIN, V., CARRILLO, G., TORROJA, C., and GUERRERO, I. (2001). The sterol-sensing domain of Patched protein seems to control Smoothened activity through Patched vesicular trafficking. Curr. Biol. 11: 601-607.
45. MARQUARDT, T., and PFAFF, S. L. (2001). Cracking the transcriptional code for cell specification in the neural tube. Cell 106: 651-654.
46. MARTÍ, E., BUMCROT, D. A., TAKADA, R. and MCMAHON, A. P. (1995). Requirement of 19K form of Sonic hedgehog for induction of distinct ventral cell types in CNS explants. Nature 375: 322-325.
47. MATISE, M. P. and JOYNER, A. L. (1997). Expression patterns of developmental control genes in normal and Engrailed-1 mutant mouse spinal cord reveal early diversity in developing interneurons. J. Neurosci. 17: 7805-7816.
48. MCMAHON, J. A., TAKADA, S., ZIMMERMAN, L. B., FAN, C. M., HARLAND, R. M., and MCMAHON, A. P. (1998). Noggin-mediated antagonism of BMP signaling is required for growth and patterning of the neural tube and somite. Genes Dev. 12: 1438-1452.
49. MIZUGUCHI, R., SUGIMORI, M., TAKEBAYASHI, H., KOSAKO, H., NAGAO, M., YOSHIDA, S., NABESHIMA, Y., SHIMAMURA, K., and NAKAFUKU, M. (2001). Combinatorial roles of olig2 and neurogenin2 in the coordinated induction of panneuronal and subtype-specific properties of motoneurons. Neuron 31: 757-771.
50. MORAN-RIVARD, L., KAGAWA, T., SAUERESSIG, H., GROSS, M. K., BURRILL, J., and GOULDING, M. (2001). Evx1 is a postmitotic determinant of V0 interneuron identity in the spinal cord. Neuron 29: 385-399.
51. MUHR, J., ANDERSSON, E., PERSSON, M., JESSELL, T. M., and ERICSON, J. (2001). Groucho-mediated transcriptional repression establishes progenitor cell pattern and neuronal fate in the ventral neural tube. Cell 104: 861-873.
52. NGUYEN, V. H., TROUT, J., CONNORS, S. A., ANDERMANN, P., WEINBERG, E., and MULLINS, M. C. (2000). Dorsal and intermediate neuronal cell types of the spinal cord are established by a BMP signaling pathway. Development 127: 1209-1220.
53. NOVITCH, B. G., CHEN, A. I., and JESSELL, T. M. (2001). Coordinate regulation of motor neuron subtype identity and pan-neuronal properties by the bHLH repressor Olig2. Neuron 31: 773-89.
54. OPPENHEIM, R. W., SHNEIDERMAN, A., SHIMIZU, I. and YAGINUMA, H. (1988). Onset and development of intersegmental projections in the chick embryo spinal cord. J. Comp. Neurol. 275: 159-180.
55. PEPINSKY, R. B., ZENG, C., WEN, D., RAYHORN, P., BAKER, D. P., WILLIAMS, K. P., BIXLER, S. A., AMBROSE, C. M., GARBER, E. A., MIATKOWSKI, K., TAYLOR, F. R., WANG, E. A. and GLADES, A. (1998) Identification of a palmitic acid-modified form of human Sonic hedgehog. J. Biol. Chem. 273:14037-14045.
56. PFAFF, S. L., MENDELSOHN, M., STEWART, C. L., EDLUND, T. and JESSELL, T. M. (1996). Requirement for LIM homeobox gene Isl1 in motor neuron generation reveals a motor neuron-dependent step in intemeuron differentiation. Cell 84: 309-320.
57. PICCOLO, S., SASAI, Y., LU, B., and DE ROBERTIS, E. M. (1996). Dorsoventral patterning in Xenopus: inhibition of ventral signals by direct binding of chordin to BMP-4. Cell 86: 589-598.
58. PIERANI, A., MORAN-RIVARD, L., SUNSHINE, M. J., LITTMAN, D. R., GOULDING, M., and JESSELL, T. M. (2001). Control of interneuron fate in the developing spinal cord by the progenitor homeodomain protein Dbx1. Neuron 29: 367-384.
59. PIERANI, A., BRENNER-MORTON, S., CHIANG, C., and JESSELL, T. M. (1999). A sonic hedgehog-independent, retinoid-activated pathway of neurogenesis in the ventral spinal cord. Cell 97: 903-915.
60. PLACZEK, M., YAMADA, T., TESSIER-LAVIGNE, M., JESSELL, T. and DODD, J. (1991). Control of dorsoventral pattern in vertebrate neural development: induction and polarizing properties of the floor plate. Development 2: 105-122.
61. PORTER, J. A., EKKER, S. C., PARK, W. J., VON KESSLER, D. P., YOUNG, K. E., CHEN, C. H., MA, Y., WOODS, A. S., COTTER, R. J., KOONIN, E. V. and BEACHY, P. A. (1996a). Hedgehog patterning activity: role of a lipophilic modification mediated by the carboxy-terminal autoprocessing domain. Cell 86: 21-34.
62. PORTER, J. A., YOUNG, K. E. and BEACHY, P. A. (1996b). Cholesterol modification of hedgehog signaling proteins in animal development. Science 274: 255-259.
63. PORTER, J. A., VON KESSLER, D. P., EKKER, S. C., YOUNG, K. E., LEE, J. J., MOSES, K. and BEACHY, P. A. (1995). The product of hedgehog autoproteolytic cleavage active in local and long-range signalling. Nature 374: 363-366.
64. RAKIC, P. (1982). Early developmental events: cell lineages, acquisition of neuronal positions, and areal and laminar development. Neurosci. Res. Program Bull. 20: 439-451.
65. RICHARDSON, W. D., SMITH, H. K., SUN, T., PRINGLE, N. P., HALL, A., and WOODRUFF, R. (2000). Oligodendrocyte lineage and the motor neuron connection. Glia 29: 136-142.
66. ROELINK, H., PORTER, J. A., CHIANG, C., TANABE, Y., CHANG, D. T., BEACHY, P. A. and JESSELL, T. M. (1995). Floor plate and motor neuron induction by different concentrations of the amino-terminal cleavage product of sonic hedgehog autoproteolysis. Cell 81: 445-455.
67. ROELINK, H., AUGSBURGER, A., HEEMSKERK, J., KORZH, V., NORLIN, S., RUIZ I ALTABA, A., TANABE, Y., PLACZEK, M., EDLUND, T., JESSELL, T. M. and DODD, J. (1994). Floor plate and motor neuron induction by vhh-1, a vertebrate homolog of hedgehog expressed by the notochord. Cell 76: 761-775.
68. ROWITCH, D. H., B, S.-J., LEE, S. M., FLAX, J. D., SNYDER, E. Y. and MCMAHON, A. P. (1999). Sonic hedgehog regulates proliferation and inhibits differentiation of CNS precursor cells. J. Neurosci. 19: 8954-8965.
69. SANDER, M., PAYDAR, S., ERICSON, J., BRISCOE, J., BERBER, E., GERMAN, M., JESSELL, T. M., and RUBENSTEIN, J. L. (2000). Ventral neural patterning by Nkx homeobox genes: Nkx6.1 controls somatic motor neuron and ventral interneuron fates. Genes Dev. 14: 2134-2139.
70. SAUERESSIG, H., BURRILL, J. and GOULDING, M. (1999). Engrailed-1 and netrin-1 regulate axon pathfinding by association interneurons that project to motor neurons. Development 126: 4201-4212.
71. SCHOENWOLF, G. C. (1982). On the morphogenesis of the early rudiments of the developing central nervous system. Scan. Electron. Microsc. Part 1: 289-308.
72. SILOS-SANTIAGO, I. and SNIDER, W. D. (1994). Development of interneurons with ipsilateral projections in embryonic rat spinal cord. J. Comp. Neurol. 342: 221-231.
73. SILOS-SANTIAGO, I. and SNIDER, W. D. (1992). Development of commissural neurons in the embryonic rat spinal cord. J. Comp. Neurol. 325: 514-526.
74. SOCKANATHAN, S., and JESSELL, T. M. (1998). Motor neuron-derived retinoid signaling specifies the subtype identity of spinal motor neurons. Cell 94: 503-514.
75. SOULA, C., DANESIN, C., KAN, P., GROB, M., PONCET, C., and COCHARD, P. (2001). Distinct sites of origin of oligodendrocytes and somatic motoneurons in the chick spinal cord: oligodendrocytes arise from Nkx2.2-expressing progenitors by a Shh-dependent mechanism. Development 128: 1369-1379.
76. STONE, D., and ROSENTHAL, A. (2000). Achieving neuronal patterning by repression. Nat. Neurosci. 3: 967-969.
77. STREIT, A., LEE, K. J., WOO, I., ROBERTS, C., JESSELL, T. M., and STERN, C. D. (1998). Chordin regulates primitive streak development and the stability of induced neural cells, but is not sufficient for neural induction in the chick embryo. Development 125: 507-519.
78. STRUTT, H., THOMAS, C., NAKANO, Y., STARK, D., NEAVE, B., TAYLOR, A: M., and INGHAM, P. W. (2001). Mutations in the sterol-sensing domain of Patched suggest a role for vesicular trafficking in Smoothened regulation. Curr. Biol. 11: 608-613.
79. SUN, T., ECHELARD, Y., LU, R., YUK, D., KAING, S., STILES, C. D., and ROWITCH, D. H. (2001). Olig bHLH proteins interact with homeodomain proteinsto regulate cell fate acquisition in progenitors of the ventral neural tube. Curr. Biol. 11: 1413-1420.
80. TAIPALE, J., CHEN, J. K., COOPER, M. K., WANG, B., MANN, R. K., MILENKOVIC, L., SCOTT, M. P., and BEACHY, P. A. (2000). Effects of oncogenic mutations in Smoothened and Patched can be reversed by cyclopamine. Nature 406: 1005-1009.
81. TANAKA, H., MATSUI, T., AGATA, A., TOMURA, M., KUBOTA, I., MCFARLAND, K. C., KOHR, B., LEE, A., PHILLIPS, H. S. AND SHELTON, D. L. (1991). Molecular cloning and expression of a novel adhesion molecule, SC1. Neuron 7: 535-545.
82. TESTAZ, S., JAROV, A., WILLIAMS, K. P., LING, L. E., KOTELIANSKY, V. E., FOURNIER-THIBAULT, C., and DUBAND, J. L. (2001). Sonic hedgehog restricts adhesion and migration of neural crest cells independently of the Patched-Smoothened-Gli signaling pathway. Proc. Natl Acad. Sci. USA 98: 12521-12526.
83. TSUCHIDA, T., ENSINI, M., BRENNER-MORTON, S., 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.
84. VALLSTEDT, A., MUHR, J., PATTYN, A., PIERANI, A., MENDELSOHN, M., SANDER, M., JESSELL, T. M., and ERICSON, J. (2001). Different levels of repressor activity assign redundant and specific roles to Nkx6genes in motor neuron and interneuron specification. Neuron 31: 743-755.
85. WATANABE, Y., and NAKAMURA, H. (2000). Control of chick tectum territory along dorsoventral axis by Sonic hedgehog. Development 127: 1131-1140.
86. WENNER, P., O'DONOVAN, M. J., and MATISE, M. P. (2000). Topographical and physiological characterization of interneurons that express Engrailed-1 in the embryonic chick spinal cord. J. Neurophysiol. 84: 2651-2657.
87. WENNER, P., and O'DONOVAN, M. J. (1999). Identification of an interneuronal population that mediates recurrent inhibition of motoneurons in the developing chick spinal cord. J. Neurosci. 19: 7557-7567.
88. WICKING, C., and MCGLINN, E. (2001). The role of hedgehog signalling in tumorigenesis. Cancer Lett. 173: 1-7.
89. YAMADA, T., PFAFF, S. L., EDLUND, T. AND JESSELL, T. M. (1993). Control of cell pattern in the neural tube: motor neuron induction by diffusible factors from notochord and floor plate. Cell 73: 673-686.
90. YAMADA, T., PLACZEK, M., TANAKA, H., DODD, J. and JESSELL, T. M. (1991). Control of cell pattern in the developing nervous system: polarizing activity of the floor plate and notochord. Cell 64: 635-647.
91. ZHOU, Q., CHOI, G., and ANDERSON, D. J. (2001). The bHLH transcription factor Olig2 promotes oligodendrocyte differentiation in collaboration with Nkx2.2. Neuron 31: 791-807.
92. ZHOU, Y., YAMAMOTO, M., and ENGEL, J. D. (2000). GATA2 is required for the generation of V2 interneurons. Development 127: 3829-38.