Secondary neurogenesis in the brain of the African clawed frog, Xenopus laevis, as revealed by PCNA, Delta-1, Neurogenin-related-1, and NeuroD expression

Journal of Comparative Neurology

Volumn 489, Issue 3, 2005, Pages 387-402

  Wullimann, Mario F ^a,c   Rink, Elke ^b   Vernier, Philippe ^a   Schlosser, Gerhard ^b  

^a CNRS   (France)

^b UNIVERSITY OF BREMEN   (Germany)

^c CNRS   (France)

Author keywords

Basic helix loop helix genes; Mash; Neurogenic genes; Notch; Proneural genes; Zash

Indexed keywords

CYCLINE; HELIX LOOP HELIX PROTEIN; NEUROGENIC DIFFERENTIATION FACTOR;

ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL PROLIFERATION; CONTROLLED STUDY; DELTA 1 GENE; EMBRYO; EMBRYO DEVELOPMENT; GENE; GENE EXPRESSION; IN SITU HYBRIDIZATION; LARVA; NEUROANATOMY; NEUROD GENE; NGNR 1 GENE; NONHUMAN; PRIORITY JOURNAL; SPINAL CORD; XENOPUS LAEVIS; ZEBRA FISH;

ANIMALS; BRAIN; CELL DIFFERENTIATION; CELL PROLIFERATION; EMBRYO, NONMAMMALIAN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MEMBRANE PROTEINS; NERVE TISSUE PROTEINS; NEURONS; PROLIFERATING CELL NUCLEAR ANTIGEN; XENOPUS LAEVIS;

EID: 22644434977     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.20634     Document Type: Article

References (86)

1. Allende ML, Weinberg ES. 1994. The expression pattern of two zebrafish achaete-scute homolog (ash) genes is altered in the embryonic brain of the cyclops mutant. Dev Biol 166:509-530.
2. Anderson SA, Eisenstat DD, Rubenstein JL. 1997a. Interneuron migration from basal forebrain to neocortex: dependence on Dlx genes. Science 278:474-476.
3. Anderson SA, Qiu M, Bulfone A, Eisenstat DD, Meneses J, Pedersen R, Rubenstein JL. 1997b. Mutations of the homeobox genes Dlx-1 and Dlx-2 disrupt the striatal subventricular zone and differentiation of the late born striatal neurons. Neuron 19:27-37.
4. Anderson RB, Jackson SC, Fujiawa H, Key B. 2000. Expression and putative role of neuropilin-1 in the early scaffold of axon tracts in embryonic Xenopus brain. Dev Dyn 219:102-108.
5. Appel B, Eisen JS. 1998. Regulation of neuronal specification in the zebrafish spinal cord by Delta function. Development 125:371-380.
6. Appel B, Givan LA, Eisen LA. 2001. Delta-Notch signaling and lateral inhibition in zebrafish spinal cord development. BMC Dev Biol 1:13.
7. Bachy I, Vernier P, Rétaux S. 2001. The LIM-homeodomain gene family in the developing Xenopus brain: conservation and divergences with the mouse related to the evolution of the forebrain. J Neurosci 21:7620-7629.
8. Bachy I, Berthon J, Rétaux S. 2002. Defining pallial and subpallial divisions in the developing Xenopus forebrain. Mech Dev 117:163-172.
9. Bellefroid EJ, Bourguignon C, Hollemann T, Ma Q, Anderson DJ, Kintner C, Pieler T. 1996. X-Myt1, a Xenopus C2HC-type zinc finger protein with a regulatory function in neuronal differentiation. Cell 87:1191-1202.
10. 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.
11. Bierkamp C, Campos-Ortega JA. 1993. A zebrafish homologue of the Drosophila neurogenic gene Notch and its pattern of transcription during early embryogenesis. Mech Dev 43:87-100.
12. Blader P, Fischer N, Gradwohl G, Guillemot F, Strähle U. 1997. The activity of neurogenin1 is controlled by local cues in the zebrafish. Development 124:4557-4569.
13. Brox A, Puelles L, Ferreiro B, Medina L. 2003. Expression of the genes GAD67 and distal-less-4 in the forebrain of Xenopus laevis confirms a common pattern in tetrapods. J Comp Neurol 461:370-393.
14. Brox A, Puelles L, Ferreiro B, Medina L. 2004. Expression of the genes Emx1, Tbr1, Eomes (Tbr2) in the telencephalon of Xenopus laevis, confirms the existence of a ventral palliai division in all tetrapods. J Comp Neurol 474:562-577.
15. Casarosa S, Fode C, Guillemot F. 1999. Mash1 regulates neurogenesis in the ventral telencephalon. Development 126:525-534.
16. Chitnis AB. 1995. The role of Notch in latera inhibition and cell fate specification. Mol Cell Neurosci 6:311-322.
17. Chitnis AB. 1999. Control of neurogenesis - lessons from frogs, fish and flies. Curr Opin Neurobiol 9:18-25.
18. Chitnis AB, Dawid I. 1999. Neurogenesis in zebrafish embryos. Methods Cell Biol 59:367-386.
19. Chitnis A, Kintner C. 1996. Sensitivity of proneural genes to lateral inhibition affects the pattern of primary neurogenesis in Xenopus embryos. Development 122:2295-2301.
20. Chitnis AB, Kuwada JY. 1990. Axonogenesis in the brain of zebrafish embryos. J Neurosci 10:1892-1905.
21. Chitnis A, Henrique D, Lewis J, Ish-Horowicz D, Kintner C. 1995. Primary neurogenesis in Xenopus embryos regulated by a homologue of the Drosophila neurogeneic gene Delta. Nature 375:761-766.
22. Coffmann C, Harris W, Kintner C. 1990. Xotch, the Xenopus homolog of Drosophila notch. Science 249:1438-1441.
23. Coffmann CR, Skoglund P, Harris W, Kintner C. 1993. Expression of an extracellular deletion of Xotch diverts cell fate in Xenopus embryos. Cell 73:659-671.
24. Cornell E, Holt C. 1992. Precocious pathfinding: retinal axons can navigate in an axonless brain. Neuron 9:1001-1011.
25. Dorsky RI, Rapaport DH, Harris WA. 1995. Xotch inhibits cell differentiation in the Xenopus retina. Neuron 14:487-496.
26. Dorsky RI, Chang WS, Rapaport DH, Harris WA. 1997. Regulation of neuronal diversity in the Xenopus retina by Delta signaling. Nature 385:67-70.
27. Drapeau P, Saint-Amant L, Buss RR, Chong M, McDearmid J, Brustein E. 2002. Development of the locomotor network in zebrafish. Prog Neurobiol 68:85-111.
28. Dubois L, Bally-Cuif L, Crozatier M, Moreau J, Paquereau L, Vincent A. 1998. XCoe2, a transcription factor of the Col/Olf-1/EBF family involved in the specification of primary neurons in Xenopus. Curr Biol 8:199-209.
29. Eisenstat DD, Liu JK, Mione M, Zhong W, Yu G, Anderson SA, Ghattas I, Puelles P, Rubenstein JLR. 1999. DLX-1, DLX-2, and DLX-5 expression define distinct stages of basal forebrain differentiation. J Comp Neurol 414:217-237.
30. Englund C, Fink A, Lau C, Pham D, Daza RAM, Bulfone A, Kowalczyk T, Hevner RF. 2005. Pax6, Tbr2 and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells and postmitotic neurons in developing neocortex. J Neurosci 25:247-251.
31. Ferreiro B, Skoglund P, Bailey A, Dorsky R, Harris WA. 1993. XASH1, a Xenopus homolog of achaete-scute: a proneural gene in anterior regions of the vertebrate CNS. Mech Dev 40:25-36.
32. Fode C, Ma Q, Casarosa S, Ang S-L, Anderson DJ, Guillemot F. 2000. A role for neural determination genes in specifying the dorsoventral identity of telencephalic neurons. Genes Dev 14:67-80.
33. Guillemot G, Joyner AL. 1993. Dynamic expression of the murine Achaete-Scute homologue Mash-1 in the developing nervous system. Mech Dev 42:171-185.
34. Haddon C, Smithers L, Schneider-Maunoury S, Coche T, Henrique D, Lewis L. 1998. Multiple delta genes and lateral inhibition in zebrafish primary neurogenesis. Development 125:359-370.
35. Horton S, Meredith A, Richardson JA, Johnson JE. 1999. Correct coordination of neuronal differentiation events in ventral forebrain requires the bHLH factor Mash1. Mol Cell Neurosci 14:355-369.
36. Jasoni CL, Walker MB, Morris MD, Reh TA. 1994. A chicken acheate-scute homolog (CASH-1) is expressed in a temporally and spatially discrete manner in the developing nervous system. Development 120:769-783.
37. Key B, Anderson RB. 1999. Neuronal pathfinding during development of the rostral brain in Xenopus. Clin Exp Pharmacol Physiol 26:752-754.
38. Korzh V, Sleptsova I, Liao J, He J, Gong Z. 1998. Expression of zebrafish bHLH genes ngn1 and nrd defines distinct stages of neural differentiation. Dev Dyn 213:92-104.
39. Koyano-Nakagawa N, Wettstein D, Kintner C. 1999. Activation of Xenopus genes required for lateral inhibition and neuronal differentiation during primary neurogenesis. Mol Cell Neurosci 14:327-339.
40. Koyano-Nakagawa N, Kim J, Anderson D, Kintner C. 2000. Hes6 acts in a positive feedback loop with the neurogenins to promote neuronal differentiation. Development 127:4203-4216.
41. Lamborghini JE. 1980. Rohon-Beard cells and other large neurons in Xenopus embryos originate during gastrulation. J Comp Neurol 189:323-333.
42. Lamborghini JE. 1987. Dissappearance of Rohon-Beard neurons from the spinal cord of larval Xenopus laeavis. J Comp Neurol 264:47-55.
43. Lee JE. 1997. NeuroD and neurogenesis. Dev Neurosci 19:27-32.
44. Lee JE, Hollenberg SM, Snider L, Turner DL, Lipnick N, Weintraub H. 1995. Conversion of Xenopus ectoderm into neurons by NeuroD, a basic helix-loop-helix protein. Science 268:836-844.
45. Lewis J. 1998. Multiple delta genes and lateral inhibition in zebrafish primary neurogenesis. Development 125:359-370.
46. Liu KJ, Harland RM. 2003. Cloning and characterization of Xenopus Id4 reveals differing roles for Id genes. Dev Biol 264:339-351.
47. Lo L-C, Johnson JE, Wuenschell CW, Saito T, Anderson DJ. 1991. Mammalian achaete-scute homolog 1 is transiently expressed by spatially restricted subsets of early neuroepithelial and neural crest cells. Genes Dev 5:1524-1537.
48. Ma Q, Kintner C, Anderson DJ. 1996. Identification of neurogenin, a vertebrate neuronal determination gene. Cell 87:43-52.
49. Ma Q, Sommer L, Cserjesi P, Anderson DJ. 1997. Mash1 and neurogenin1 expression patterns define complementary domains of neuroepithelium in the developing CNS and are correlated with regions expressing Notch ligands. J Neurosci 17:3644-3652.
50. Marín O, Anderson SA, Rubenstein JLR. 2000. Origin and molecular specification of striatal interneurons. J Neurosci 20:6063-6076.
51. Milán FJ, Puelles L. 2000. Patterns of calretinin, calbindin, and tyrosine-hydroxylase expression are consistent with the prosomeric map of the frog diencephalon. J Comp Neurol 419:96-121.
52. Moreno N, Bachy I, Rétaux S, Gonzalez A. 2004. LIM-homeodomain genes as developmental and adult genetic markers of Xenopus forebrain functional subdivisions. J Comp Neurol 472:52-72.
53. Mueller T, Wullimann MF. 2002. BrdU-, neuroD-(nrd) and Hu-studies show unusual non-ventricular neurogenesis in the postembryonic zebrafish forebrain. Mech Dev 117:123-135.
54. Mueller T, Wullimann MF. 2003. Anatomy of neurogenesis in the zebrafish brain. Dev Brain Res 140:135-153.
55. Nieuwkoop PD, Faber J. 1967. Normal table of Xenopus laevis (Daudin). Amsterdam: North-Holland.
56. Pannese M, Lupo G, Kabla B, Boncinelli E, Barsacchi G, Vignali R. 1998. The Xenopus Emx genes identify presumptive dorsal telencephalon and are induced by head organizer signals. Mech Dev 73:73-83.
57. Park HC, Hong SK, Kim HS, Kim SH, Yoon EJ, Kim CH, Miki N, Huh TL. 2000. Structural comparison of zebrafish Elav/Hu and their differential expressions during neurogenesis. Neurosci Lett 79:81-84.
58. Perron M, Opdecamp K, Butler K, Harris WA, Bellefroid EJ. 1999. X-ngnr-1 and Xath3 promote ectopic expression of sensory neuron markers in the neurula ectoderm and have distinct inducing properties in the retina. Proc Nat Acad Sci U S A 96:14996-15001.
59. Puelles L, Rubensteir JLR. 1993. Expression patterns of homeobox and other putative regulatory genes in the embryonic mouse forebrain suggests a neuromeric organization., TINS 16:472-479.
60. Puelles L, Rubenstein JLR. 2003. Forebrain gene expression domains and the evolving prosomeric model. TINS 26:469-476.
61. Rétaux S, Rogard M, Bach I, Failli V, Besson Marie-Jo. 1999. Lhx9: a novel LIM-homeodomain gene epxressed in the developing forebrain. J Neurosci 19:783-793.
62. Reyes R, Haendel M, Grant D, Melancon E, Eisen JS. 2004. Slow degeneration of zebrafish Rohon-Beard neurons during programmed cell death. Dev Dyn 229:30-41.
63. Rink E, Wullimann MF. 2002. Development of the catecholaminergic system in the early zebrafish brain: an immunohistochemical study. Dev Brain Res 137:89-100.
64. Roberts A. 1989. The neurons that control axial movements in a frog embryo. Am Zool 29:53-63.
65. Roberts A. 2000. Early functional organization of spinal neurons in developing lower vertebrates. Brain Res Bull 53:585-593.
66. Schlosser G. 2003. Mosaic evolution of neural development in anurans: acceleration of spinal cord development in the direct developing frog Eleutherodactylus coqui. Anat Embryol 206:215-227.
67. Schlosser G, Ahrens K. 2004. Molecular anatomy of placode development in Xenopus laevis. Dev Biol 271:439-466.
68. Schlosser G, Northcutt RG. 2000. Development of neurogenic placodes in Xenopus laevis. J Comp Neurol 418:121-146.
69. Schlosser G, Koyano-Nakagama N, Kintner C. 2002. Thyroid hormone promotes neurogenesis in the Xenopus spinal cord. Dev Dyn 225:485-498.
70. Schuurmans C, Guillemot F. 2002. Molecular mechanisms underlying cell fate specification in the developing telencephalon. Curr Opin Neurobiol 12:26-34.
71. Slack J, Holland PW, Graham CF. 1993. The zootype and the phylotypic stage. Nature 361:490-492.
72. Smith-Fernandez A, Pieau C, Repérant J, Boncinelli E, Wassef M. 1998. Expression of the Emx-1 and Dlx-1 homeobox genes define three molecularly distinct domains in the telencephalon of the mouse, chick, turtle and frog embryos. Development 125:2099-2111.
73. Souopgui H, Solter M, Pieler T. 2002. XPak,3 promotes cell cycle withdrawal during primary neurogenesis in Xenopus laevis. EMBO J 21:6429-6439.
74. Taelman V, Opdecamp K, Avalosse B, Ryan K, Bellefroid EJ. 2001. Xath2, a bHLH gene expressed during a late transition stage of neurogenesis in the forebrain of Xenopus embryos. Mech Dev. 101:199-202.
75. Talikka M, Perez SE, Zimmermann K. 2002. Distinct patterns of downstream target activation are specified by the helix-loop-helix-domain of proneural basic helix-loop-helix transcription factors. Dev Biol 247:137-148.
76. Torii M-A, Matsuzaki F, Osumi N, Kaibuchi K, Nakamura S, Casarosa S, Guillemot F, Nakafuku M. 1999. Transcription factors Mash-1 and Prox-1 delineate early steps in differentiation of neural stem cells in the developing central nervous system. Development 126:443-456.
77. von Frowein J, Campbell K, Götz M. 2002. Expression of Ngn1, Ngn2, Cash1, Gsh2 and Sfrp1 in the developing chick telencephalon. Mech Dev 110:249-252.
78. Waseem NH, Lane DP. 1990. Monoclonal antibody analysis of the proliferating cell nuclear antigen (PCNA): structural conservation and the detection of a nucleolar form. J Cell Sci 96:121-129.
79. Westin J, Lardelli M. 1997. Three novel Notch genes in zebrafish: implication for vertebrate Notch gene evolution and function. Dev Genes Evol 207:51-63.
80. Wilson SW, Ross LS, Parrett T, Easter SS Jr. 1990. The development of a simple scaffold of axon tracts in the brain of the embryonic zebrafish, Brachydanio rerio. Development 108:121-145.
81. Wullimann MF, Knipp S. 2000. Proliferation pattern changes in the zebrafish brain from embryonic through early postembryonic stages. Anat Embryol 202:385-400.
82. Wullimann MF, Mueller T. 2002. Expression of Zash-1a in the postembryonic zebrafish brain allows comparison to mouse Mash1 domains. Gene Expr Patterns 1:187-192.
83. Wullimann MF, Mueller T. 2004a. Identification and morphogenesis of the eminentia thalami in the zebrafish. J Comp Neurol 471:37-48.
84. Wullimann MF, Mueller T. 2004b. Teleostean and mammalian forebrains contrasted: evidence from genes to behavior. J Comp Neurol 475:143-162.
85. Wullimann MF, Puelles L. 1999. Postembryonic neural proliferation in the zebrafish forebrain and its relationship to prosomeric domains. Anat Embryol 199:329-348.
86. Yun K, Fischman S, Johnson J, De Angelis MH, Weinmaster G, Rubenstein JLR. 2002. Modulation of the notch signaling by Mash1 and Dlx1/2 regulates sequential specification and differentiation of progenitor cell types in the subcortical telencephalon. Development 129:5029-5040.