Nuclear factor I coordinates multiple phases of cerebellar granule cell development via regulation of cell adhesion molecules

Journal of Neuroscience

Volumn 27, Issue 23, 2007, Pages 6115-6127

  Wang, Wei ^a   Mullikin Kilpatrick, Debra ^a   Crandall, James E ^a,b   Gronostajski, Richard M ^c   Litwack, E David ^d   Kilpatrick, Daniel L ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c UNIVERSITY AT BUFFALO   (United States)

^d UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

Author keywords

Axon; Dendrite; Differentiation; Migration; Neuron; Transcription

Indexed keywords

CELL ADHESION MOLECULE; EPHRIN B1; NERVE CELL ADHESION MOLECULE; NUCLEAR FACTOR I; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ARTICLE; CELL CULTURE; CELL MATURATION; CEREBELLAR GRANULE NEURON; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; DENDRITIC CELL; EMBRYO; GENE TARGETING; GERM LAYER; GRANULE CELL; MOUSE; NERVE CELL DIFFERENTIATION; NERVE FIBER MEMBRANE; NONHUMAN; PRIORITY JOURNAL; TRANSCRIPTION REGULATION;

ANIMALS; CELL ADHESION MOLECULES; CELL MOVEMENT; CELLS, CULTURED; CEREBELLUM; DROSOPHILA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; NFI TRANSCRIPTION FACTORS; RATS;

EID: 34250015228     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0180-07.2007     Document Type: Article

References (68)

1. Altman J (1972) Postnatal development of the cerebellar cortex in the rat. 3. Maturation of the components of the granular layer. J Comp Neurol 145:465-513.
2. Arregui C, Pathre P, Lilien J, Balsamo J (2000) The nonreceptor tyrosine kinase fer mediates cross-talk between N-cadherin and beta1-integrins. J Cell Biol 149:1263-1274.
3. Aruga J, Minowa O, Yaginuma H, Kuno J, Nagai T, Noda T, Mikoshiba K (1998) Mouse Zic1 is involved in cerebellar development. J Neurosci 18:284-293.
4. Aruga J, Inoue T, Hoshino J, Mikoshiba K (2002) Zic2 controls cerebellar development in cooperation with Zic1. J Neurosci 22:218-225.
5. Barami K, Kirschenbaum B, Lemmon V, Goldman SA (1994) N-cadherin and Ng-CAM/8D9 are involved serially in the migration of newly generated neurons into the adult songbird brain. Neuron 13:567-582.
6. Ben-Arie N, Bellen HJ, Armstrong DL, McCall AE, Gordadze PR, Guo Q, Matzuk MM, Zoghbi HY (1997) Math1 is essential for genesis of cerebellar granule neurons. Nature 390:169-172.
7. Berglund EO, Murai KK, Fredette B, Sekerkova G, Marturano B, Weber L, Mugnaini E, Ranscht B (1999) Ataxia and abnormal cerebellar microorganization in mice with ablated contactin gene expression. Neuron 24:739-750.
8. Bix GJ, Clark GD (1998) Platelet-activating factor receptor stimulation disrupts neuronal migration in vitro. J Neurosci 18:307-318.
9. Blaess S, Graus-Porta D, Belvindrah R, Radakovits R, Pons S, Littlewood-Evans A, Senften M, Guo H, Li Y, Miner JH, Reichardt LF, Muller U (2004) β1-integrins are critical for cerebellar granule cell precursor proliferation. J Neurosci 24:3402-3412.
10. Chaudhry AZ, Lyons GE, Gronostajski RM (1997) Expression patterns of the four nuclear factor I genes during mouse embryogenesis indicate a potential role in development. Dev Dyn 208:313-325.
11. das Neves L, Duchala CS, Tolentino-Silva F, Haxhiu MA, Colmenares C, Macklin WB, Campbell CE, Butz KG, Gronostajski RM (1999) Disruption of the murine nuclear factor I-A gene (Nfia) results in perinatal lethality, hydrocephalus, and agenesis of the corpus callosum. Proc Natl Acad Sci USA 96:11946-11951.
12. Davis S, Gale NW, Aldrich TH, Maisonpierre PC, Lhotak V, Pawson T, Goldfarb M, Yancopoulos GD (1994) Ligands for EPH-related receptor tyrosine kinases that require membrane attachment or clustering for activity. Science 266:816-819.
13. Deneen B, Ho R, Lukaszewicz A, Hochstim CJ, Gronostajski RM, Anderson DJ (2006) The transcription factor NFIA controls the onset of gliogenesis in the developing spinal cord. Neuron 52:953-968.
14. Doherty P, Rowett LH, Moore SE, Mann DA, Walsh FS (1991) Neurite outgrowth in response to transfected N-CAM and N-cadherin reveals fundamental differences in neuronal responsiveness to CAMs. Neuron 6:247-258.
15. Fannon AM, Colman DR (1996) A model for central synaptic junctional complex formation based on the differential adhesive specificities of the cadherins. Neuron 17:423-434.
16. Fishman RB, Hatten ME (1993) Multiple receptor systems promote CNS neural migration. J Neurosci 13:3485-3495.
17. Galipeau J, Li H, Paquin A, Sicilia F, Karpati G, Nalbantoglu J (1999) Vesicular stomatitis virus G pseudotyped retrovector mediates effective in vivo suicide gene delivery in experimental brain cancer. Cancer Res 59:2384-2394.
18. Gao PP, Yue Y, Cerretti DP, Dreyfus C, Zhou R (1999) Ephrin-dependent growth and pruning of hippocampal axons. Proc Natl Acad Sci USA 96:4073-4077.
19. Gao WO, Heintz N, Hatten ME (1991) Cerebellar granule cell neurogenesis is regulated by cell-cell interactions in vitro. Neuron 6:705-715.
20. Gao WQ, Hatten ME (1993) Neuronal differentiation rescued by implantation of Weaver granule cell precursors into wild-type cerebellar cortex. Science 260:367-369.
21. Gazit R, Krizhanovsky V, Ben-Arie N (2004) Math1 controls cerebellar granule cell differentiation by regulating multiple components of the Notch signaling pathway. Development 131:903-913.
22. Gronostajski RM (2000) Roles of the NFI/CTF gene family in transcription and development. Gene 249:31-45.
23. Grunder A, Ebel TT, Mallo M, Schwarzkopf G, Shimizu T, Sippel AE, Schrewe H (2002) Nuclear factor I-B (Nfib) deficient mice have severe lung hypoplasia. Mech Dev 112:69-77.
24. Halloran MC, Wolman MA (2006) Repulsion or adhesion: receptors make the call. Curr Opin Cell Biol 18:533-540.
25. Hirotsune S, Fleck MW, Gambello MJ, Bix GJ, Chen A, Clark GD, Ledbetter DH, McBain CJ, Wynshaw-Boris A (1998) Graded reduction of Pafah1b1 (Lis1) activity results in neuronal migration defects and early embryonic lethality. Nat Genet 19:333-339.
26. Huynh-Do U, Vindis C, Liu H, Cerretti DP, McGrew JT, Enriquez M, Chen J, Daniel TO (2002) Ephrin-B1 transduces signals to activate integrinmediated migration, attachment and angiogenesis. J Cell Sci 115:3073-3081.
27. Jensen P, Smeyne R, Goldowitz D (2004) Analysis of cerebellar development in math1 null embryos and chimeras. J Neurosci 24:2202-2211.
28. Lauro C, Catalano M, Trettel F, Mainiero F, Ciotti MT, Eusebi F, Limatola C (2006) The chemokine CX3CL1 reduces migration and increases adhesion of neurons with mechanisms dependent on the beta1 integrin subunit. J Immunol 177:7599-7606.
29. Li H, Leung TC, Hoffman S, Balsamo J, Lilien J (2000) Coordinate regulation of cadherin and integrin function by the chondroitin sulfate proteoglycan neurocan. J Cell Biol 149:1275-1288.
30. Li S, Qiu F, Xu A, Price SM, Xiang M (2004) Barhl1 regulates migration and survival of cerebellar granule cells by controlling expression of the neurotrophin-3 gene. J Neurosci 24:3104-3114.
31. Lu Q, Sun EE, Flanagan JG (2004) Analysis of PDZ-RGS3 function in ephrin-B reverse signaling. Methods Enzymol 390:120-128.
32. Ma Q, Jones D, Springer TA (1999) The chemokine receptor CXCR4 is required for the retention of B lineage and granulocytic precursors within the bone marrow microenvironment. Immunity 10:463-471.
33. Marquardt T, Shirasaki R, Ghosh S, Andrews SE, Carter N, Hunter T, Pfaff SL (2005) Coexpressed EphA receptors and ephrin-A ligands mediate opposing actions on growth cone navigation from distinct membrane domains. Cell 121:127-139.
34. Marrs GS, Honda T, Fuller L, Thangavel R, Balsamo J, Lilien J, Dailey ME, Arregui C (2006) Dendritic arbors of developing retinal ganglion cells are stabilized by beta 1-integrins. Mol Cell Neurosci 32:230-241.
35. Mathis C, Collin L, Borrelli E (2003) Oligodendrocyte ablation impairs cerebellum development. Development 130:4709-4718.
36. Mercado ML, Nur-e-Kamal A, Liu HY, Gross SR, Movahed R, Meiners S (2004) Neurite outgrowth by the alternatively spliced region of human tenascin-C is mediated by neuronal α7β1 integrin. J Neurosci 24:238-247.
37. Millen KJ, Hui CC, Joyner AL (1995) A role for En-2 and other murine homologues of Drosophila segment polarity genes in regulating positional information in the developing cerebellum. Development 121:3935-3945.
38. Miyata T, Maeda T, Lee JE (1999) NeuroD is required for differentiation of the granule cells in the cerebellum and hippocampus. Genes Dev 13:1647-1652.
39. Moreno-Flores MT, Martin-Aparicio E, Avila J, Diaz-Nido J, Wandosell F (2002) Ephrin-B1 promotes dendrite outgrowth on cerebellar granule neurons. Mol Cell Neurosci 20:429-446.
40. Nakai Y, Kamiguchi H (2002) Migration of nerve growth cones requires detergent-resistant membranes in a spatially defined and substrate-dependent manner. J Cell Biol 159:1097-1108.
41. Nakamoto T, Kain KH, Ginsberg MH (2004) Neurobiology: new connections between integrins and axon guidance. Curr Biol 14:R121-R123.
42. Palmer A, Klein R (2003) Multiple roles of ephrins in morphogenesis, neuronal networking, and brain function. Genes Dev 17:1429-1450.
43. Powell SK, Rivas RJ, Rodriguez-Boulan E, Hatten ME (1997) Development of polarity in cerebellar granule neurons. J Neurobiol 32:223-236.
44. Riehl R, Johnson K, Bradley R, Grunwald GB, Cornel E, Lilienbaum A, Holt CE (1996) Cadherin function is required for axon outgrowth in retinal ganglion cells in vivo. Neuron 17:837-848.
45. Ronn LC, Ralets I, Hartz BP, Bech M, Berezin A, Berezin V, Moller A, Bock E (2000) A simple procedure for quantification of neurite outgrowth based on stereological principles. J Neurosci Methods 100:25-32.
46. Schwartz PM, Borghesani PR, Levy RL, Pomeroy SL, Segal RA (1997) Abnormal cerebellar development and foliation in BDNF-/-mice reveals a role for neurotrophins in CNS patterning. Neuron 19:269-281.
47. Shan WS, Tanaka H, Phillips GR, Arndt K, Yoshida M, Colman DR, Shapiro L (2000) Functional cis-heterodimers of N- and R-cadherins. J Cell Biol 148:579-590.
48. Shu T, Butz KG, Plachez C, Gronostajski RM, Richards LJ (2003) Abnormal development of forebrain midline glia and commissural projections in Nfia knock-out mice. J Neurosci 23:203-212.
49. Soha JM, Kim S, Crandall JE, Vogel MW (1997) Rapid growth of parallel fibers in the cerebella of normal and staggerer mutant mice. J Comp Neurol 389:642-654.
50. Solecki DJ, Liu XL, Tomoda T, Fang Y, Hatten ME (2001) Activated Notch2 signaling inhibits differentiation of cerebellar granule neuron precursors by maintaining proliferation. Neuron 31:557-568.
51. Steele Perkins G, Butz KG, Lyons GE, Zeichner-David M, Kim HJ, Cho MI, Gronostajski RM (2003) Essential role for NFI-C/CTF transcription-replication factor in tooth root development. Mol Cell Biol 23:1075-1084.
52. Steele Perkins G, Plachez C, Butz KG, Yang G, Bachurski CJ, Kinsman SL, Litwack ED, Richards LJ, Gronostajski RM (2005) The transcription factor gene Nfib is essential for both lung maturation and brain development. Mol Cell Biol 25:685-698.
53. Swanson DJ, Tong Y, Goldowitz D (2005) Disruption of cerebellar granule cell development in the Pax6 mutant, Sey mouse. Brain Res Dev Brain Res 160:176-193.
54. Takeda H, Shimoyama Y, Nagafuchi A, Hirohashi S (1999) E-cadherin functions as a cis-dimer at the cell-cell adhesive interface in vivo. Nat Struct Biol 6:310-312.
55. Thelen K, Kedar V, Panicker AK, Schmid RS, Midkiff BR, Maness PF (2002) The neural cell adhesion molecule L1 potentiates integrin-dependent cell migration to extracellular matrix proteins. J Neurosci 22:4918-4931.
56. Tomoda T, Bhatt RS, Kuroyanagi H, Shirasawa T, Hatten ME (1999) A mouse serine/threonine kinase homologous to C. elegans UNC51 functions in parallel fiber formation of cerebellar granule neurons. Neuron 24:833-846.
57. Volk T, Geiger B (1984) A 135-kd membrane protein of intercellular adherens junctions. EMBO J 3:2249-2260.
58. Wang W, Stock RE, Gronostajski RM, Wong YW, Schachner M, Kilpatrick DL (2004) A role for nuclear factor I in the intrinsic control of cerebellar granule neuron gene expression. J Biol Chem 279:53491-53497.
59. Wang W, Qu Q, Smith FI, Kilpatrick DL (2005) Self-inactivating lentiviruses: versatile vectors for quantitative transduction of cerebellar granule neurons and their progenitors. J Neurosci Methods 149:144 -153.
60. Weyer A, Schilling K (2003) Developmental and cell type-specific expression of the neuronal marker NeuN in the murine cerebellum. J Neurosci Res 73:400-409.
61. Williams E, Williams G, Gour BJ, Blaschuk OW, Doherty P (2000a) A novel family of cyclic peptide antagonists suggests that N-cadherin specificity is determined by amino acids that flank the HAV motif. J Biol Chem 275:4007- 4012.
62. Williams EJ, Williams G, Gour B, Blaschuk O, Doherty P (2000b) INP, a novel N-cadherin antagonist targeted to the amino acids that flank the HAV motif. Mol Cell Neurosci 15:456-464.
63. Yamasaki T, Kawaji K, Ono K, Bito H, Hirano T, Osumi N, Kengaku M (2001) Pax6 regulates granule cell polarization during parallel fiber formation in the developing cerebellum. Development 128:3133-3144.
64. Yang XW, Wynder C, Doughty ML, Heintz N (1999) BAC-mediated genedosage analysis reveals a role for Zipro1 (Ru49/Zfp38) in progenitor cell proliferation in cerebellum and skin. Nat Genet 22:327-335.
65. Yin Y, Yamashita Y, Noda H, Okafuji T, Go MJ, Tanaka H (2004) EphA receptor tyrosine kinases interact with co-expressed ephrin-A ligands in cis. Neurosci Res 48:285-296.
66. Zhang L, Goldman JE (1996) Generation of cerebellar interneurons from dividing progenitors in white matter. Neuron 16:47-54.
67. Zheng T, Santi MR, Bovolin P, Marlier LN, Grayson DR (1993) Developmental expression of the alpha 6 GABAA receptor subunit mRNA occurs only after cerebellar granule cell migration. Brain Res Dev Brain Res 75:91-103.
68. Zhu H, Luo L (2004) Diverse functions of N-cadherin in dendritic and axonal terminal arborization of olfactory projection neurons. Neuron 42:63-75.