Engrailed-1 expression marks a primitive class of inhibitory spinal interneuron

Journal of Neuroscience

Volumn 24, Issue 25, 2004, Pages 5827-5839

  Higashijima, Shin Ichi ^a   Masino, Mark A ^a   Mandel, Gail ^a   Fetcho, Joseph R ^a  

^a STONY BROOK UNIVERSITY   (United States)

Author keywords

Circuitry; Inhibition; Interneuron; Spinal cord; Transcription factor; Zebrafish

Indexed keywords

CARRIER PROTEIN; ENGRAILED 1 PROTEIN; GLYCINE RECEPTOR; STRYCHNINE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CELL FUNCTION; CELL TYPE; CIRCUMFERENTIAL ASCENDING INTERNEURON; EMBRYO; EVOLUTION; GENE; GENE EXPRESSION; GLYCINE TRANSPORTER 2 GENE; INHIBITORY NEUROTRANSMISSION; INTERNEURON; LARVA; MONOSYNAPTIC REFLEX; MOTONEURON; MOTOR SYSTEM; NERVE PROJECTION; NERVOUS SYSTEM DEVELOPMENT; NEUROTRANSMISSION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSORY SYSTEM; SPINAL CORD; SPINAL CORD VENTRAL HORN; SWIMMING; ZEBRA FISH;

AMINO ACID TRANSPORT SYSTEMS, NEUTRAL; ANIMALS; EMBRYO, NONMAMMALIAN; GLYCINE; GLYCINE PLASMA MEMBRANE TRANSPORT PROTEINS; IN SITU HYBRIDIZATION; INTERNEURONS; LARVA; MICROSCOPY, CONFOCAL; NERVE TISSUE PROTEINS; PATCH-CLAMP TECHNIQUES; SPINAL CORD; TIME FACTORS; TRANSCRIPTION FACTORS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 3042817387     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5342-03.2004     Document Type: Article

References (51)

1. Alvarez FJ, Jonas P, Sapir T, Gieman EJ, Hartley R, Todd AJ, Goulding M (2003) Postnatal phenotype and localization of spinal cord V1 derived interneurons. Soc Neurosci Abstr 29:39.3.
2. Antal M, Berki AC, Horvath L, O'Donovan MJ (1994) Developmental changes in the distribution of gamma-aminobutyric acid-immunoreactive neurons in the embryonic chick lumbosacral spinal cord. J Comp Neurol 343:228-236.
3. Baldissera F, Hultborn H, Illert M (1981) Integration in spinal neuronal systems. In: Handbook of physiology, Sec 1, The nervous system, Vol II, Motor control (Brooks VB, ed), pp 509 -595. Bethesda, MD: American Physiological Society.
4. Berki AC, O'Donovan MJ, Antal M (1995) Developmental expression of glycine immunoreactivity and its colocalization with GABA in the embryonic chick lumbosacral spinal cord. J Comp Neurol 362:583-596.
5. Bernhardt RR, Chitnis AB, Lindamer L, Kuwada JY (1990) Identification of spinal neurons in the embryonic and larval zebrafish. J Comp Neurol 302:603-616.
6. Briscoe J, Pierani A, Jessell TM, Ericson J (2000) A homeodomain protein code specifies progenitor cell identity and neuronal fate in the ventral neural tube. Cell 101:435-445.
7. Burke RE, Fleshman JW (1986) Strategies to identify interneurons involved in locomotor pattern generation in the mammalian spinal cord. In: Neurobiology of vertebrate locomotion (Grillner S, Stein PSG, Forssberg H, Herman RM, eds), pp 245-267. London: Macmillian.
8. Burrill JD, Moran L, Goulding MD, Saueressig H (1997) PAX2 is expressed in multiple spinal cord interneurons, including a population of EN1+ interneurons that require PAX6 for their development. Development 124:4493-4503.
9. Davis CA, Holmyard DP, Millen KJ, Joyner AL (1991) Examining pattern formation in mouse, chicken and frog embryos with an En-specific antiserum. Development 111:287-298.
10. Drapeau P, Ali DW, Buss RR, Saint-Amant L (1999) In vivo recording from identifiable neurons of the locomotor network in the developing zebrafish. J Neurosci Methods 88:1-13.
11. Ekker M, Wegner J, Akimenko MA, Westerfield M (1992) Coordinate embryonic expression of three zebrafish engrailed genes. Development 116:1001-1010.
12. Fetcho JR (1990) Morphological variability, segmental relationships, and functional role of a class of commissural interneurons in the spinal cord of goldfish. J Comp Neurol 299:283-298.
13. Fetcho JR (2001) Optical and genetic approaches toward understanding spinal circuits. In: Motor neurobiology of the spinal cord (Cope TC, ed), pp 3-20. Boca Raton, FL.: CRC.
14. Fetcho JR, O'Malley DM (1995) Visualization of active neural circuitry in the spinal-cord of intact zebrafish. J Neurophysiol 73:399-406.
15. Fjose A, Njolstad PR, Nornes S, Molven A, Krauss S (1992) Structure and early embryonic expression of the zebrafish engrailed-2 gene. Mech Dev 39:51-62.
16. Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151:1531-1545.
17. Gleason MR, Higashijima S, Dallman J, Liu K, Mandel G, Fetcho JR (2003) Translocation of CaM kinase II to synaptic sites in vivo. Nat Neurosci 6:217-218.
18. Goulding M, Lanuza G, Sapir T, Narayan S (2002) The formation of sensorimotor circuits. Curr Opin Neurobiol 12:508-515.
19. Grillner S (1981) Control of locomotion in bipeds, tetrapods, and fish. In: Handbook of physiology, Sect I, The nervous system II (Brooks VB, ed), pp 1179-1236. Washington, DC: American Physiological Society.
20. Hale ME, Ritter DA, Fetcho JR (2001) A confocal study of spinal interneurons in living larval zebrafish. J Comp Neurol 437:1-16.
21. Halloran MC, Sato-Maeda M, Warren JT, Su F, Lele Z, Krone PH, Kuwada JY, Shoji W (2000) Laser-induced gene expression in specific cells of transgenic zebrafish. Development 127:1953-1960.
22. Hatta K, Bremiller R, Westerfield M, Kimmel CB (1991) Diversity of expression of engrailed-like antigens in zebrafish. Development 112:821-832.
23. Hieber V, Dai X, Foreman M, Goldman D (1998) Induction of alpha1-tubulin gene expression during development and regeneration of the fish central nervous system. J Neurobiol 37:429-440.
24. Higashijima S, Okamoto H, Ueno N, Hotta Y, Eguchi G (1997) High-frequency generation of transgenic zebrafish which reliable express GFP in whole muscles or the whole body by using promoters of zebrafish origin. Dev Biol 192:289-299.
25. Higashijima SI, Masino MA, Mandel G, Fetcho JR (2003) Imaging neuronal activity during zebrafish behavior with a genetically encoded calcium indicator. J Neurophysiol 90:3986-3997.
26. Holland PW, Williams NA (1990) Conservation of engrailed-like homeobox sequences during vertebrate evolution. FEBS Lett 277:250-252.
27. Jankowska E, Hammar I (2002) Spinal interneurones; how can studies in animals contribute to the understanding of spinal interneuronal systems in man? Brain Res Rev 40:19-28.
28. Jessell TM (2000) Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat Rev Genet 1:20-29.
29. Jessen JR, Meng A, McFarlane RJ, Paw BH, Zon LI, Smith GR, Lin S (1998) Modification of bacterial artificial chromosomes through chi-stimulated homologous recombination and its application in zebrafish transgenesis. Proc Natl Acad Sci USA 95:5121-5126.
30. Joyner AL, Martin GR (1987) En-1 and En-2, two mouse genes with sequence homology to the Drosophila engrailed gene: expression during embryogenesis. Genes Dev 1:29-38.
31. Kiehn O, Kjaerulff O (1998) Distribution of central pattern generators for rhythmic motor outputs in the spinal cord of limbed vertebrates. Ann NY Acad Sci 860:110-129.
32. Kiehn O, Kullander K (2004) Central pattern generators deciphered by molecular genetics. Neuron 41:317-321.
33. Kuwada JY, Bernhardt RR, Nguyen N (1990) Development of spinal neurons and tracts in the zebrafish embryo. J Comp Neurol 302:617-628.
34. Legendre P, Korn H (1994) Glycinergic inhibitory synaptic currents and related receptor channels in the zebrafish brain. Eur J Neurosci 6:1544-1557.
35. Li WC, Soffe SR, Roberts A (2002) Spinal inhibitory neurons that modulate cutaneous sensory pathways during locomotion in a simple vertebrate. J Neurosci 22:10924-10934.
36. Li W-C, Higashijima S, Parry DM, Roberts A, Soffe SR (2004) Primitive roles for inhibitory interneurons in developing frog spinal cord. J Neurosci 24:5840-5848.
37. Martin SC, Heinrich G, Sandell JH (1998) Sequence and expression of glutamic acid decarboxylase isoforms in the developing zebrafish. J Comp Neurol 396:253-266.
38. Miyawaki A, Llopis J, Heim R, McCaffery JM, Adams JA, Ikura M, Tsien RY (1997) Fluorescent indicators for Ca2+ based on green fluorescent proteins and calmodulin. Nature 388:882-887.
39. Moran-Rivard L, Kagawa T, Saueressig H, Gross MK, Burrill J, Goulding M (2001) Evx1 is a postmitotic determinant of v0 interneuron identity in the spinal cord. Neuron 29:385-399.
40. Nakayama K, Nishimaru H, Kudo N (2002) Basis of changes in left-right coordination of rhythmic motor activity during development in the rat spinal cord. J Neurosci 22:10388-10398.
41. Park HC, Kim CH, Bae YK, Yeo SY, Kim SH, Hong SK, Shin J, Yoo KW, Hibi M, Hirano T, Miki N, Chitnis AB, Huh TL (2000) Analysis of upstream elements in the HuC promoter leads to the establishment of transgenic zebrafish with fluorescent neurons. Dev Biol 227:279-293.
42. Pierani A, Moran-Rivard L, Sunshine MJ, Littman DR, Goulding M, Jessell TM (2001) Control of interneuron fate in the developing spinal cord by the progenitor homeodomain protein Dbx1. Neuron 29:367-384.
43. Ritter DA, Bhatt DH, Fetcho JR (2001) In vivo imaging of zebrafish reveals differences in the spinal networks for escape and swimming movements. J Neurosci 21:8956-8965.
44. Sapir T, Geiman EJ, Wang Z, Velasquez T, Mitsui S, Yoshihara Y, Frank E, Alvarez FJ, Goulding M (2004) Pax6 and engrailed1 regulate two distinct aspects of renshaw cell development. J Neurosci 24:1255-1264.
45. Saueressig H, Burrill J, Goulding M (1999) Engrailed-1 and netrin-1 regulate axon pathfinding by association interneurons that project to motor neurons. Development 126:4201-4212.
46. Sharma K, Peng CY (2001) Spinal motor circuits: merging development and function. Neuron 29:321-324.
47. Sillar KT, Roberts A (1988) A neuronal mechanism for sensory gating during locomotion in a vertebrate. Nature 331:262-265.
48. Sillar KT, Roberts A (1992a) The role of premotor interneurons in phase-dependent modulation of a cutaneous reflex during swimming in Xenopus laevis embryos. J Neurosci 12:1647-1657.
49. Sillar KT, Roberts A (1992b) Phase-dependent modulation of a cutaneous sensory pathway by glycinergic inhibition from the locomotor rhythm generator in Xenopus embryos. Eur J Neurosci 4:1022-1034.
50. Wenner P, O'Donovan MJ (1999) Identification of an interneuronal population that mediates recurrent inhibition of motoneurons in the developing chick spinal cord. J Neurosci 19:7557-7567.
51. Wenner P, O'Donovan MJ, Matise MP (2000) Topographical and physiological characterization of interneurons that express engrailed-1 in the embryonic chick spinal cord. J Neurophysiol 84:2651-2657.