Axonin-1/TAG-1 is required for pathfinding of granule cell axons in the developing cerebellum

Neural Development

Volumn 3, Issue 1, 2008, Pages

  Baeriswyl, Thomas ^a   Stoeckli, Esther T ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CONTACTIN 2; NERVE CELL ADHESION MOLECULE; UNCLASSIFIED DRUG;

ANIMAL; APOPTOSIS; ARTICLE; CEREBELLUM; CHICK EMBRYO; CHICKEN; CYTOLOGY; DOWN REGULATION; ELECTROPORATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NERVE FIBER; PHYSIOLOGY; PRENATAL DEVELOPMENT; RNA INTERFERENCE; SENSORY RECEPTOR; ULTRASTRUCTURE;

ANIMALS; APOPTOSIS; AXONS; CELL ADHESION MOLECULES, NEURONAL; CEREBELLUM; CHICK EMBRYO; CHICKENS; DOWN-REGULATION; ELECTROPORATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; RNA INTERFERENCE; SENSORY RECEPTOR CELLS;

EID: 42649105813     PISSN: None     EISSN: 17498104     Source Type: Journal    
DOI: 10.1186/1749-8104-3-7     Document Type: Article

References (73)

1. The axonally secreted cell adhesion molecule, axonin-1. Primary structure, immunoglobulin-like and fibronectin-type-III-like domains and glycosyl-phosphatidylinositol anchorage. RA Zuellig C Rader A Schroeder MB Kalousek F Von Bohlen und Halbach T Osterwalder C Inan ET Stoeckli HU Affolter A Fritz, Eur J Biochem 1992 204 453 463
2. The axonal glycoprotein TAG-1 is an immunoglobulin superfamily member with neurite outgrowth-promoting activity. AJ Furley SB Morton D Manalo D Karagogeos J Dodd TM Jessell, Cell 1990 61 157 170 10.1016/0092-8674(90)90223-2 2317872
3. Axonin-1, Nr-CAM, and Ng-CAM play different roles in the in vivo guidance of chick commissural neurons. ET Stoeckli LT Landmesser, Neuron 1995 14 1165 1179 10.1016/0896-6273(95)90264-3 7541632
4. Interference with axonin-1 and NrCAM interactions unmasks a floor-plate activity inhibitory for commissural axons. ET Stoeckli P Sonderegger GE Pollerberg LT Landmesser, Neuron 1997 18 209 221 10.1016/S0896-6273(00)80262-7 9052792
5. Distinct subpopulations of sensory afferents require F11 or axonin-1 for growth to their target layers within the spinal cord of the chick. FE Perrin FG Rathjen ET Stoeckli, Neuron 2001 30 707 723 10.1016/S0896-6273(01)00315-4 11430805
6. Changing patterns of gene expression define four stages of cerebellar granule neuron differentiation. SG Kuhar L Feng S Vidan ME Ross ME Hatten N Heintz, Development 1993 117 97 104 8223263
7. Distribution of TAG-1 and synaptophysin in the developing cerebellar cortex: relationship to Purkinje cell dendritic development. RW Stottmann RJ Rivas, J Comp Neurol 1998 395 121 135
8. Development of polarity in cerebellar granule neurons. SK Powell RJ Rivas E Rodriguez-Boulan ME Hatten, J Neurobiol 1997 32 223 236
9. Development and malformations of the cerebellum in mice. V Chizhikov KJ Millen, Mol Genet Metab 2003 80 54 65
10. Disorders of the cerebellum: ataxia, dysmetria of thought, and the cerebellar cognitive affective syndrome. JD Schmahmann, J Neuropsychiatry Clin Neurosci 2004 16 367 378 15377747
11. The cells and molecules that make a cerebellum. D Goldowitz K Hamre, Trends Neurosci 1998 21 375 382 10.1016/S0166-2236(98)01313-7 9735945
12. Central nervous system neuronal migration. ME Hatten, Annu Rev Neurosci 1999 22 511 539 10.1146/annurev.neuro.22.1.511 10202547
13. Genes involved in cerebellar cell specification and differentiation. ME Hatten J Alder K Zimmerman N Heintz, Curr Opin Neurobiol 1997 7 40 47 10.1016/S0959-4388(97)80118-3 9039803
14. Mechanisms of neural patterning and specification in the developing cerebellum. ME Hatten N Heintz, Annu Rev Neurosci 1995 18 385 408 7605067
15. Cellular and genetic regulation of the development of the cerebellar system. C Sotelo, Prog Neurobiol 2004 72 295 339 10.1016/j.pneurobio.2004.03.004 15157725
16. The chick/quail chimeric system: a model for early cerebellar development. M Hallonet RM Alvarado-Mallart, Perspect Dev Neurobiol 1997 5 17 31 9509515
17. Embryonic neural chimaeras in the study of brain development. NM Le Douarin, Trends Neurosci 1993 16 64 72 10.1016/0166-2236(93)90019-I 7680502
18. Early mesencephalon/metencephalon patterning and development of the cerebellum. M Wassef AL Joyner, Perspect Dev Neurobiol 1997 5 3 16 9509514
19. The rhombic lip and early cerebellar development. RJ Wingate, Curr Opin Neurobiol 2001 11 82 88 10.1016/S0959-4388(00)00177-X 11179876
20. Migration patterns of clonally related granule cells and their progenitors in the developing chick cerebellum. EF Ryder CL Cepko, Neuron 1994 12 1011 1028 10.1016/0896-6273(94)90310-7 8185941
21. Embryonic precursor cells from the rhombic lip are specified to a cerebellar granule neuron identity. J Alder NK Cho ME Hatten, Neuron 1996 17 389 399 10.1016/S0896-6273(00)80172-5 8816703
22. The role of the rhombic lip in avian cerebellum development. RJ Wingate ME Hatten, Development 1999 126 4395 4404 10498676
23. Generation of cerebellar interneurons from dividing progenitors in white matter. L Zhang JE Goldman, Neuron 1996 16 47 54 10.1016/S0896-6273(00)80022-7 8562089
24. Postnatal development of the murine cerebellar cortex: formation and early dispersal of basket, stellate and Golgi neurons. G Weisheit M Gliem E Endl PL Pfeffer M Busslinger K Schilling, Eur J Neurosci 2006 24 466 478 10.1111/j.1460-9568.2006.04915.x 16903854
25. Screening for gene function in chicken embryo using RNAi and electroporation. V Pekarik D Bourikas N Miglino P Joset S Preiswerk ET Stoeckli, Nat Biotechnol 2003 21 93 96 10.1038/nbt770 12496763
26. New tools for gene manipulation in chicken embryos. D Bourikas ET Stoeckli, Oligonucleotides 2003 13 411 419 10.1089/154545703322617096 15000832
27. In ovo RNAi opens new possibilities for temporal and spatial control of gene silencing during development of the vertebrate nervous system. T Baeriswyl ET Stoeckli, J RNAi Gene Silencing 2006 2 126 135
28. Longitudinal axon guidance. ET Stoeckli, Curr Opin Neurobiol 2006 16 35 39 10.1016/j.conb.2006.01.008 16418003
29. Neuronal specification in the spinal cord: inductive signals and transcriptional codes. TM Jessell, Nat Rev Genet 2000 1 20 29 10.1038/35049541 11262869
30. The morphogen sonic hedgehog is an axonal chemoattractant that collaborates with netrin-1 in midline axon guidance. F Charron E Stein J Jeong AP McMahon M Tessier-Lavigne, Cell 2003 113 11 23 10.1016/S0092-8674(03)00199-5 12679031
31. Sonic hedgehog guides commissural axons along the longitudinal axis of the spinal cord. D Bourikas V Pekarik T Baeriswyl A Grunditz R Sadhu M Nardo ET Stoeckli, Nat Neurosci 2005 8 297 304 10.1038/nn1396 15746914
32. A simple procedure for the long-term cultivation of chicken embryos. R Auerbach L Kubai D Knighton J Folkman, Dev Biol 1974 41 391 394 10.1016/0012-1606(74)90316-9 4452416
33. Overexpression of genes in Purkinje cells in the embryonic chicken cerebellum by in vivo electroporation. J Luo C Redies, J Neurosci Methods 2004 139 241 245 10.1016/j.jneumeth.2004.04.032 15488237
34. A complete culture system for the chick embryo. MM Perry, Nature 1988 331 70 72 10.1038/331070a0 3340149
35. Ex ovo electroporation for gene transfer into older chicken embryos. J Luo C Redies, Dev Dyn 2005 233 1470 1477 10.1002/dvdy.20454 15965981
36. A series of normal stages in the development of the chick embryo. V Hamburger HL Hamilton, J Morphol 1951 88 49 92 10.1002/jmor.1050880104
37. Cdh1-APC controls axonal growth and patterning in the mammalian brain. Y Konishi J Stegmuller T Matsuda S Bonni A Bonni, Science 2004 303 1026 1030 10.1126/science.1093712 14716021
38. Overlapping functions of the cell adhesion molecules Nr-CAM and L1 in cerebellar granule cell development. T Sakurai M Lustig J Babiarz AJ Furley S Tait PJ Brophy SA Brown LY Brown CA Mason M Grumet, J Cell Biol 2001 154 1259 1273 10.1083/jcb.200104122 11564762
39. Transgenic mice expressing F3/contactin from the TAG-1 promoter exhibit developmentally regulated changes in the differentiation of cerebellar neurons. A Bizzoca D Virgintino L Lorusso M Buttiglione L Yoshida A Polizzi M Tattoli R Cagiano F Rossi S Kozlov A Furley G Gennarini, Development 2003 130 29 43 10.1242/dev.00183 12441289
40. Ataxia and abnormal cerebellar microorganization in mice with ablated contactin gene expression. EO Berglund KK Murai B Fredette G Sekerkova B Marturano L Weber E Mugnaini B Ranscht, Neuron 1999 24 739 750 10.1016/S0896-6273(00)81126-5 10595523
41. A functional interaction between the neuronal adhesion molecules TAG-1 and F3 modulates neurite outgrowth and fasciculation of cerebellar granule cells. M Buttiglione JM Revest O Pavlou D Karagogeos A Furley G Rougon C Faivre-Sarrailh, J Neurosci 1998 18 6853 6870 9712656
42. Role of Pax6 in development of the cerebellar system. D Engelkamp P Rashbass A Seawright V van Heyningen, Development 1999 126 3585 3596 10409504
43. The axonally secreted protein axonin-1 is a potent substratum for neurite growth. ET Stoeckli TB Kuhn CO Duc MA Ruegg P Sonderegger, J Cell Biol 1991 112 449 455 10.1083/jcb.112.3.449 1991792
44. Clustering and functional cooperation of Ng-CAM and axonin-1 in the substratum-contact area of growth cones. ET Stoeckli U Ziegler AJ Bleiker P Groscurth P Sonderegger, Dev Biol 1996 177 15 29 10.1006/dbio.1996.0141 8660873
45. A direct interaction of axonin-1 with NgCAM-related cell adhesion molecule (NrCAM) results in guidance, but not growth of commissural axons. D Fitzli ET Stoeckli S Kunz K Siribour C Rader B Kunz SV Kozlov A Buchstaller RP Lane DM Suter WJ Dreyerc P Sonderegger, J Cell Biol 2000 149 951 968 10.1083/jcb.149.4.951 10811834
46. Efficient targeting of gene expression in chick embryos by microelectroporation. T Momose A Tonegawa J Takeuchi H Ogawa K Umesono K Yasuda, Dev Growth Differ 1999 41 335 344 10.1046/j.1440-169X.1999.413437.x 10400395
47. Comparison of three nonviral transfection methods for foreign gene expression in early chicken embryos in ovo. T Muramatsu Y Mizutani Y Ohmori J Okumura, Biochem Biophys Res Commun 1997 230 376 380 10.1006/bbrc.1996.5882 9016787
48. Introduction of DNA into chick embryos by in ovo electroporation. H Nakamura J Funahashi, Methods 2001 24 43 48 10.1006/meth.2001.1155 11327801
49. Targeted gene expression in the chicken eye by in ovo electroporation. YX Chen CE Krull LW Reneker, Mol Vis 2004 10 874 883 15570216
50. EphA4 constitutes a population-specific guidance cue for motor neurons. J Eberhart ME Swartz SA Koblar EB Pasquale CE Krull, Dev Biol 2002 247 89 101 10.1006/dbio.2002.0695 12074554
51. Efficient ectopic gene expression targeting chick mesoderm. KC Oberg CU Pira JP Revelli B Ratz E Aguilar-Cordova G Eichele, Dev Dyn 2002 224 291 302 10.1002/dvdy.10104 12112459
52. In ovo electroporation of avian somites. M Scaal J Gros C Lesbros C Marcelle, Dev Dyn 2004 229 643 650 10.1002/dvdy.10433 14991719
53. Sparking new frontiers: using in vivo electroporation for genetic manipulations. M Swartz J Eberhart GS Mastick CE Krull, Dev Biol 2001 233 13 21 10.1006/dbio.2001.0181 11319854
54. Functional knockdown of neuropilin-1 in the developing chick nervous system by siRNA hairpins phenocopies genetic ablation in the mouse. R Bron BJ Eickholt M Vermeren N Fragale J Cohen, Dev Dyn 2004 230 299 308 10.1002/dvdy.20043 15162508
55. Plasmid-based short-hairpin RNA interference in the chicken embryo. C Chesnutt L Niswander, Genesis 2004 39 73 78 10.1002/gene.20028 15170691
56. Gene silencing in chick embryos with a vector-based small interfering RNA system. T Katahira H Nakamura, Dev Growth Differ 2003 45 361 367 10.1046/j.1440-169X.2003.00705.x 12950277
57. Guidance of myocardial patterning in cardiac development by Sema6D reverse signalling. T Toyofuku H Zhang A Kumanogoh N Takegahara M Yabuki K Harada M Hori H Kikutani, Nat Cell Biol 2004 6 1204 1211 10.1038/ncb1193 15543137
58. Purkinje-cell-derived Sonic hedgehog regulates granule neuron precursor cell proliferation in the developing mouse cerebellum. VA Wallace, Curr Biol 1999 9 445 448 10.1016/S0960-9822(99)80195-X 10226030
59. Molecular markers of neuronal progenitors in the embryonic cerebellar anlage. D Morales ME Hatten, J Neurosci 2006 26 12226 12236 10.1523/JNEUROSCI. 3493-06.2006 17122047
60. The transmembrane semaphorin Sema6A controls cerebellar granule cell migration. G Kerjan J Dolan C Haumaitre S Schneider-Maunoury H Fujisawa KJ Mitchell A Chedotal, Nat Neurosci 2005 8 1516 1524 10.1038/nn1555 16205717
61. Netrin1 exerts a chemorepulsive effect on migrating cerebellar interneurons in a Dcc-independent way. P Guijarro S Simo M Pascual I Abasolo JA Del Rio E Soriano, Mol Cell Neurosci 2006 33 389 400 10.1016/j.mcn.2006.08.010 17029983
62. Axonal remodeling and synaptic differentiation in the cerebellum is regulated by WNT-7a signaling. AC Hall FR Lucas PC Salinas, Cell 2000 100 525 535 10.1016/S0092-8674(00)80689-3 10721990
63. Cadherins guide migrating Purkinje cells to specific parasagittal domains during cerebellar development. J Luo U Treubert-Zimmermann C Redies, Mol Cell Neurosci 2004 25 138 152 10.1016/j.mcn.2003.10.003 14962747
64. Genetic regulation of cerebellar development. VY Wang HY Zoghbi, Nat Rev Neurosci 2001 2 484 491 10.1038/35081558 11433373
65. F3/F11 cell surface molecule expression in the developing mouse cerebellum is polarized at synaptic sites and within granule cells. C Faivre-Sarrailh G Gennarini C Goridis G Rougon, J Neurosci 1992 12 257 267 1729438
66. F3 neuronal adhesion molecule controls outgrowth and fasciculation of cerebellar granule cell neurites: a cell-type-specific effect mediated by the Ig-like domains. M Buttiglione JM Revest G Rougon C Faivre-Sarrailh, Mol Cell Neurosci 1996 8 53 69 10.1006/mcne.1996.0043 8923455
67. The adhesion molecule TAG-1 is required for proper migration of the superficial migratory stream in the medulla but not of cortical interneurons. M Denaxa K Kyriakopoulou K Theodorakis G Trichas M Vidaki Y Takeda K Watanabe D Karagogeos, Dev Biol 2005 288 87 99 10.1016/j.ydbio.2005.09.021 16225856
68. TAG-1-deficient mice have marked elevation of adenosine A1 receptors in the hippocampus. F Fukamauchi O Aihara YJ Wang K Akasaka Y Takeda M Horie H Kawano K Sudo M Asano K Watanabe Y Iwakura, Biochem Biophys Res Commun 2001 281 220 226 10.1006/bbrc.2001.4334 11178983
69. Targeted ablation of NrCAM or ankyrin-B results in disorganized lens fibers leading to cataract formation. MI More FP Kirsch FG Rathjen, J Cell Biol 2001 154 187 196 10.1083/jcb.200104038 11449000
70. Cell-cell adhesion by homophilic interaction of the neuronal recognition molecule axonin-1. C Rader ET Stoeckli U Ziegler T Osterwalder B Kunz P Sonderegger, Eur J Biochem 1993 215 133 141 10.1111/j.1432-1033.1993.tb18015.x 8344273
71. Axonin-1/TAG-1 mediates cell-cell adhesion by a cis-assisted trans-interaction. B Kunz R Lierheimer C Rader M Spirig U Ziegler P Sonderegger, J Biol Chem 2002 277 4551 4557 10.1074/jbc.M109779200 11733523
72. Use of lipophilic dyes in studies of axonal pathfinding in vivo. FE Perrin ET Stoeckli, Microsc Res Tech 2000 48 25 31
73. Expression patterns of plexins and neuropilins are consistent with cooperative and separate functions during neural development. O Mauti R Sadhu J Gemayel M Gesemann ET Stoeckli, BMC Dev Biol 2006 6 32