Cell-type-specific expression of NFIX in the developing and adult cerebellum

Brain Structure and Function

Volumn 222, Issue 5, 2017, Pages 2251-2270

  Fraser, James ^a   Essebier, Alexandra ^a   Gronostajski, Richard M ^b   Boden, Mikael ^a   Wainwright, Brandon J ^a   Harvey, Tracey J ^a   Piper, Michael ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b UNIVERSITY AT BUFFALO   (United States)

Author keywords

Cerebellum; External granular layer; Granule neuron; NFIX

Indexed keywords

NFIX TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; NFIX PROTEIN, MOUSE; NUCLEAR FACTOR I;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BERGMANN GLIA CELL; BIRTH; BRAIN DEVELOPMENT; BRAIN FUNCTION; CELL PROLIFERATION; CEREBELLUM; CONFOCAL MICROSCOPY; CONTROLLED STUDY; EMBRYO; FEMALE; GRANULE CELL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; INTERNEURON; MALE; MOUSE; NEURAL STEM CELL; NONHUMAN; PERINATAL PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PURKINJE CELL; SUBVENTRICULAR ZONE; TRANSCRIPTOMICS; WILD TYPE; AGING; ANIMAL; C57BL MOUSE; CELL DIFFERENTIATION; CYTOLOGY; GENE EXPRESSION REGULATION; GLIA; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NERVE CELL; NERVOUS SYSTEM DEVELOPMENT; PHYSIOLOGY;

AGING; ANIMALS; ASTROCYTES; CELL DIFFERENTIATION; CEREBELLUM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MICE, INBRED C57BL; NEURAL STEM CELLS; NEUROGENESIS; NEUROGLIA; NEURONS; NFI TRANSCRIPTION FACTORS;

EID: 84996644474     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-016-1340-8     Document Type: Article

References (79)

1. Akazawa C, Ishibashi M, Shimizu C, Nakanishi S, Kageyama R (1995) A mammalian helix-loop-helix factor structurally related to the product of Drosophila proneural gene atonal is a positive transcriptional regulator expressed in the developing nervous system. J Biol Chem 270(15):8730–8738
2. Alder J, Cho NK, Hatten ME (1996) Embryonic precursor cells from the rhombic lip are specified to a cerebellar granule neuron identity. Neuron 17(3):389–399
3. Alder J, Lee KJ, Jessell TM, Hatten ME (1999) Generation of cerebellar granule neurons in vivo by transplantation of BMP-treated neural progenitor cells. Nat Neurosci 2(6):535–540
4. Barry G, Piper M, Lindwall C, Moldrich R, Mason S, Little E, Sarkar A, Tole S, Gronostajski RM, Richards LJ (2008) Specific glial populations regulate hippocampal morphogenesis. J Neurosci 28(47):12328–12340
5. 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(6656):169–172
6. Betancourt J, Katzman S, Chen B (2014) Nuclear factor one B regulates neural stem cell differentiation and axonal projection of corticofugal neurons. J Comp Neurol 522(1):6–35
7. Bolduc ME, du Plessis AJ, Sullivan N, Guizard N, Zhang X, Robertson RL, Limperopoulos C (2012) Regional cerebellar volumes predict functional outcome in children with cerebellar malformations. Cerebellum 11(2):531–542
8. Buffo A, Rossi F (2013) Origin, lineage and function of cerebellar glia. Prog Neurobiol 109:42–63
9. Campbell CE, Piper M, Plachez C, Yeh YT, Baizer JS, Osinski JM, Litwack ED, Richards LJ, Gronostajski RM (2008) The transcription factor Nfix is essential for normal brain development. BMC Dev Biol 8:52
10. Chizhikov V, Millen KJ (2003) Development and malformations of the cerebellum in mice. Mol Genet Metab 80(1–2):54–65
11. Chow LM, Zhang J, Baker SJ (2008) Inducible Cre recombinase activity in mouse mature astrocytes and adult neural precursor cells. Transgenic Res 17(5):919–928
12. Chung SH, Kim CT, Jung YH, Lee NS, Jeong YG (2010) Early cerebellar granule cell migration in the mouse embryonic development. Anat Cell Biol 43(1):86–95
13. Corrales JD, Blaess S, Mahoney EM, Joyner AL (2006) The level of sonic hedgehog signaling regulates the complexity of cerebellar foliation. Development 133(9):1811–1821
14. 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(21):11946–11951
15. De Luca A, Parmigiani E, Tosatto G, Martire S, Hoshino M, Buffo A, Leto K, Rossi F (2015) Exogenous Sonic hedgehog modulates the pool of GABAergic interneurons during cerebellar development. Cerebellum 14(2):72–85
16. 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(6):953–968
17. Dohrmann GJ, Dunsmore RH (1975) Gliobastoma multiforme of the cerebellum. Surg Neurol 3(4):219–223
18. Dooley AL, Winslow MM, Chiang DY, Banerji S, Stransky N, Dayton TL, Snyder EL, Senna S, Whittaker CA, Bronson RT et al (2011) Nuclear factor I/B is an oncogene in small cell lung cancer. Genes Dev 25(14):1470–1475
19. Driller K, Pagenstecher A, Uhl M, Omran H, Berlis A, Grunder A, Sippel AE (2007) Nuclear factor I X deficiency causes brain malformation and severe skeletal defects. Mol Cell Biol 27(10):3855–3867
20. Englund C, Fink A, Lau C, Pham D, Daza RA, 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(1):247–251
21. Englund C, Kowalczyk T, Daza RA, Dagan A, Lau C, Rose MF, Hevner RF (2006) Unipolar brush cells of the cerebellum are produced in the rhombic lip and migrate through developing white matter. J Neurosci 26(36):9184–9195
22. Fink AJ, Englund C, Daza RA, Pham D, Lau C, Nivison M, Kowalczyk T, Hevner RF (2006) Development of the deep cerebellar nuclei: transcription factors and cell migration from the rhombic lip. J Neurosci 26(11):3066–3076
23. Fleming JT, He W, Hao C, Ketova T, Pan FC, Wright CC, Litingtung Y, Chiang C (2013) The Purkinje neuron acts as a central regulator of spatially and functionally distinct cerebellar precursors. Dev Cell 27(3):278–292
24. Fujita S, Shimada M, Nakamura T (1966) H3-thymidine autoradiographic studies on the cell proliferation and differentiation in the external and the internal granular layers of the mouse cerebellum. J Comp Neurol 128(2):191–208
25. 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(4):903–913
26. Genovesi LA, Ng CG, Davis MJ, Remke M, Taylor MD, Adams DJ, Rust AG, Ward JM, Ban KH, Jenkins NA et al (2013) Sleeping Beauty mutagenesis in a mouse medulloblastoma model defines networks that discriminate between human molecular subgroups. Proc Natl Acad Sci USA 110(46):E4325–E4334
27. 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(1–2):69–77
28. Grunder A, Qian F, Ebel TT, Mincheva A, Lichter P, Kruse U, Sippel AE (2003) Genomic organization, splice products and mouse chromosomal localization of genes for transcription factor Nuclear Factor One. Gene 304:171–181
29. Harris L, Genovesi LA, Gronostajski RM, Wainwright BJ, Piper M (2015) Nuclear factor one transcription factors: divergent functions in developmental versus adult stem cell populations. Dev Dyn 244(3):227–238
30. Harris L, Zalucki O, Piper M, Heng JI (2016) Insights into the biology and therapeutic applications of neural stem cells. Stem Cells Int 2016:9745315
31. Heng YH, Barry G, Richards LJ, Piper M (2012) Nuclear factor I genes regulate neuronal migration. Neurosignals 20(3):159–167
32. Heng YH, McLeay RC, Harvey TJ, Smith AG, Barry G, Cato K, Plachez C, Little E, Mason S, Dixon C et al (2014) NFIX regulates neural progenitor cell differentiation during hippocampal morphogenesis. Cereb Cortex 24(1):261–279
33. Hevner RF, Hodge RD, Daza RA, Englund C (2006) Transcription factors in glutamatergic neurogenesis: conserved programs in neocortex, cerebellum, and adult hippocampus. Neurosci Res 55(3):223–233
34. Joubert M, Eisenring JJ, Robb JP, Andermann F (1969) Familial agenesis of the cerebellar vermis. A syndrome of episodic hyperpnea, abnormal eye movements, ataxia, and retardation. Neurology 19(9):813–825
35. Kerjan G, Dolan J, Haumaitre C, Schneider-Maunoury S, Fujisawa H, Mitchell KJ, Chedotal A (2005) The transmembrane semaphorin Sema6A controls cerebellar granule cell migration. Nat Neurosci 8(11):1516–1524
36. Kruse U, Sippel AE (1994) The genes for transcription factor nuclear factor I give rise to corresponding splice variants between vertebrate species. J Mol Biol 238(5):860–865
37. Kumbasar A, Plachez C, Gronostajski RM, Richards LJ, Litwack ED (2009) Absence of the transcription factor Nfib delays the formation of the basilar pontine and other mossy fiber nuclei. J Comp Neurol 513(1):98–112
38. Laine J, Axelrad H (1998) Lugaro cells target basket and stellate cells in the cerebellar cortex. Neuroreport 9(10):2399–2403
39. Lastowska M, Al-Afghani H, Al-Balool HH, Sheth H, Mercer E, Coxhead JM, Redfern CP, Peters H, Burt AD, Santibanez-Koref M et al (2013) Identification of a neuronal transcription factor network involved in medulloblastoma development. Acta Neuropathol Commun 1:35
40. Lee HK, Lee DS, Park JC (2015) Nuclear factor I-C regulates E-cadherin via control of KLF4 in breast cancer. BMC Cancer 15:113
41. Lee HY, Greene LA, Mason CA, Manzini MC (2009) Isolation and culture of post-natal mouse cerebellar granule neuron progenitor cells and neurons. J Vis Exp(23)
42. Lee Y, Miller HL, Jensen P, Hernan R, Connelly M, Wetmore C, Zindy F, Roussel MF, Curran T, Gilbertson RJ et al (2003) A molecular fingerprint for medulloblastoma. Cancer Res 63(17):5428–5437
43. Leto K, Carletti B, Williams IM, Magrassi L, Rossi F (2006) Different types of cerebellar GABAergic interneurons originate from a common pool of multipotent progenitor cells. J Neurosci 26(45):11682–11694
44. Liu C, Duan P, Li B, Huang C, Jing Y, Yan W (2015) miR-29a activates Hes1 by targeting Nfia in esophageal carcinoma cell line TE-1. Oncol Lett 9(1):96–102
45. Lu W, Quintero-Rivera F, Fan Y, Alkuraya FS, Donovan DJ, Xi Q, Turbe-Doan A, Li QG, Campbell CG, Shanske AL et al (2007) NFIA haploinsufficiency is associated with a CNS malformation syndrome and urinary tract defects. PLoS Genet 3(5):e80
46. Machold R, Fishell G (2005) Math1 is expressed in temporally discrete pools of cerebellar rhombic-lip neural progenitors. Neuron 48(1):17–24
47. Machold R, Klein C, Fishell G (2011) Genes expressed in Atoh1 neuronal lineages arising from the r1/isthmus rhombic lip. Gene Expr Patterns 11(5–6):349–359
48. Martynoga B, Mateo JL, Zhou B, Andersen J, Achimastou A, Urban N, van den Berg D, Georgopoulou D, Hadjur S, Wittbrodt J et al (2013) Epigenomic enhancer annotation reveals a key role for NFIX in neural stem cell quiescence. Genes Dev 27(16):1769–1786
49. Mason S, Piper M, Gronostajski RM, Richards LJ (2009) Nuclear factor one transcription factors in CNS development. Mol Neurobiol 39(1):10–23
50. Mirabello L, Koster R, Moriarity BS, Spector LG, Meltzer PS, Gary J, Machiela MJ, Pankratz N, Panagiotou OA, Largaespada D et al (2015) A genome-wide scan identifies variants in NFIB associated with metastasis in patients with osteosarcoma. Cancer Discov 5(9):920–931
51. Mugnaini E, Floris A (1994) The unipolar brush cell: a neglected neuron of the mammalian cerebellar cortex. J Comp Neurol 339(2):174–180
52. Northcott PA, Korshunov A, Pfister SM, Taylor MD (2012) The clinical implications of medulloblastoma subgroups. Nat Rev Neurol 8(6):340–351
53. Packer RJ, Cogen P, Vezina G, Rorke LB (1999) Medulloblastoma: clinical and biologic aspects. Neuro Oncol 1(3):232–250
54. Piper M, Barry G, Harvey TJ, McLeay R, Smith AG, Harris L, Mason S, Stringer BW, Day BW, Wray NR et al (2014) NFIB-mediated repression of the epigenetic factor Ezh2 regulates cortical development. J Neurosci 34(8):2921–2930
55. Piper M, Barry G, Hawkins J, Mason S, Lindwall C, Little E, Sarkar A, Smith AG, Moldrich RX, Boyle GM et al (2010) NFIA controls telencephalic progenitor cell differentiation through repression of the Notch effector Hes1. J Neurosci 30(27):9127–9139
56. Piper M, Harris L, Barry G, Heng YH, Plachez C, Gronostajski RM, Richards LJ (2011) Nuclear factor one X regulates the development of multiple cellular populations in the postnatal cerebellum. J Comp Neurol 519(17):3532–3548
57. Piper M, Moldrich RX, Lindwall C, Little E, Barry G, Mason S, Sunn N, Kurniawan ND, Gronostajski RM, Richards LJ (2009) Multiple non-cell-autonomous defects underlie neocortical callosal dysgenesis in Nfib-deficient mice. Neural Dev 4:43
58. Pistocchi A, Gaudenzi G, Foglia E, Monteverde S, Moreno-Fortuny A, Pianca A, Cossu G, Cotelli F, Messina G (2013) Conserved and divergent functions of Nfix in skeletal muscle development during vertebrate evolution. Development 140(7):1528–1536
59. Plachez C, Lindwall C, Sunn N, Piper M, Moldrich RX, Campbell CE, Osinski JM, Gronostajski RM, Richards LJ (2008) Nuclear factor I gene expression in the developing forebrain. J Comp Neurol 508(3):385–401
60. Pouzat C, Hestrin S (1997) Developmental regulation of basket/stellate cell–>Purkinje cell synapses in the cerebellum. J Neurosci 17(23):9104–9112
61. Rossi G, Antonini S, Bonfanti C, Monteverde S, Vezzali C, Tajbakhsh S, Cossu G, Messina G (2016) Nfix regulates temporal progression of muscle regeneration through modulation of myostatin expression. Cell Rep 14(9):2238–2249
62. Singh SK, Wilczynska KM, Grzybowski A, Yester J, Osrah B, Bryan L, Wright S, Griswold-Prenner I, Kordula T (2011) The unique transcriptional activation domain of nuclear factor-I-X3 is critical to specifically induce marker gene expression in astrocytes. J Biol Chem 286(9):7315–7326
63. 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(4):557–568
64. 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(2):685–698
65. Steinlin M, Imfeld S, Zulauf P, Boltshauser E, Lovblad KO, Ridolfi Luthy A, Perrig W, Kaufmann F (2003) Neuropsychological long-term sequelae after posterior fossa tumour resection during childhood. Brain 126(Pt 9):1998–2008
66. Taniguchi H, He M, Wu P, Kim S, Paik R, Sugino K, Kvitsiani D, Fu Y, Lu J, Lin Y et al (2011) A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 71(6):995–1013
67. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc 7(3):562–578
68. Vidovic D, Harris L, Harvey TJ, Evelyn Heng YH, Smith AG, Osinski J, Hughes J, Thomas P, Gronostajski RM, Bailey TL et al (2015) Expansion of the lateral ventricles and ependymal deficits underlie the hydrocephalus evident in mice lacking the transcription factor NFIX. Brain Res 1616:71–87
69. Wang VY, Rose MF, Zoghbi HY (2005) Math1 expression redefines the rhombic lip derivatives and reveals novel lineages within the brainstem and cerebellum. Neuron 48(1):31–43
70. Wang W, Crandall JE, Litwack ED, Gronostajski RM, Kilpatrick DL (2010) Targets of the nuclear factor I regulon involved in early and late development of postmitotic cerebellar granule neurons. J Neurosci Res 88(2):258–265
71. Wang W, Mullikin-Kilpatrick D, Crandall JE, Gronostajski RM, Litwack ED, Kilpatrick DL (2007) Nuclear factor I coordinates multiple phases of cerebellar granule cell development via regulation of cell adhesion molecules. J Neurosci 27(23):6115–6127
72. 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(51):53491–53497
73. Weyer A, Schilling K (2003) Developmental and cell type-specific expression of the neuronal marker NeuN in the murine cerebellum. J Neurosci Res 73(3):400–409
74. Wilczynska KM, Singh SK, Adams B, Bryan L, Rao RR, Valerie K, Wright S, Griswold-Prenner I, Kordula T (2009) Nuclear factor I isoforms regulate gene expression during the differentiation of human neural progenitors to astrocytes. Stem Cells 27(5):1173–1181
75. Xu H, Yang Y, Tang X, Zhao M, Liang F, Xu P, Hou B, Xing Y, Bao X, Fan X (2013) Bergmann glia function in granule cell migration during cerebellum development. Mol Neurobiol 47(2):833–844
76. 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(16):3133–3144
77. Zhang X, Zhou Y, Pan C, Lei C, Dang R, Chen H, Lan X (2015) Novel alternative splice variants of NFIX and their diverse mRNA expression patterns in dairy goat. Gene 569(2):250–258
78. Zhou B, Osinski JM, Mateo JL, Martynoga B, Sim FJ, Campbell CE, Guillemot F, Piper M, Gronostajski RM (2015) Loss of NFIX transcription factor biases postnatal neural stem/progenitor cells toward oligodendrogenesis. Stem Cells Dev 24(18):2114–2126
79. Zhou Y, Cai H, Xu Y, Sun J, Lan X, Lei C, Chen H (2014) Novel isoforms of the bovine Nuclear factor I/X (CCAAT-binding transcription factor) transcript products and their diverse expression profiles. Anim Genet 45(4):581–584