Nuclear Pore Composition Regulates Neural Stem/Progenitor Cell Differentiation in the Mouse Embryo

Developmental Cell

Volumn 14, Issue 6, 2008, Pages 831-842

  Lupu, Floria ^a   Alves, Annabelle ^b,c   Anderson, Kathryn ^a   Doye, Valérie ^b,c   Lacy, Elizabeth ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^b INSTITUT CURIE   (France)

^c CNRS   (France)

Author keywords

CELLBIO; DEVBIO; STEMCELL

Indexed keywords

ALKALINE PHOSPHATASE; CYCLIN D1; CYCLIN D2; CYCLIN DEPENDENT KINASE INHIBITOR 1B; FIBROBLAST GROWTH FACTOR 5; NUCLEOPORIN; NUCLEOPORIN 133; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR OTX2;

ALLELE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ACTIVITY; CELL COMMUNICATION; CELL DIFFERENTIATION; CELL DIVISION; CELL NUCLEUS; CELL TYPE; CONTROLLED STUDY; CYTOPLASM; DEVELOPMENTAL STAGE; ECTODERM; EMBRYO; EMBRYO DEVELOPMENT; EMBRYO PATTERN FORMATION; EMBRYONIC STEM CELL; MAMMAL; MOUSE; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; NUCLEAR PORE COMPLEX; PLURIPOTENT STEM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; STEM CELL;

ALLELES; ANIMALS; BIOLOGICAL MARKERS; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; CHROMOSOME MAPPING; CROSSES, GENETIC; EMBRYO, MAMMALIAN; GASTRULA; GENE EXPRESSION REGULATION, DEVELOPMENTAL; IN SITU HYBRIDIZATION; MICE; MICE, CONGENIC; MICE, INBRED C3H; MICE, INBRED C57BL; MUTATION; NEURONS; NUCLEAR PORE; NUCLEAR PORE COMPLEX PROTEINS; STEM CELLS; TRANSCRIPTION, GENETIC;

MAMMALIA;

EID: 44449129923     PISSN: 15345807     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.devcel.2008.03.011     Document Type: Article

References (70)

1. Akhtar A., and Gasser S. The nuclear envelope and transcriptional control. Nat. Rev. Genet. 8 (2007) 507-517
2. Alber F., Dokudovskaya S., Veenhoff L., Zhang W., Kipper J., Devos D., Suprapto A., Karni-Schmidt O., Williams R., Chait B., et al. The molecular architecture of the nuclear pore complex. Nature 450 (2007) 695-701
3. Ang S., Conlon R., Jin O., and Rossant J. Positive and negative signals from mesoderm regulate the expression of mouse Otx2 in ectoderm explants. Development 120 (1994) 2979-2989
4. Aoto T., Saitoh N., Ichimura T., Niwa H., and Nakao M. Nuclear and chromatin reorganization in the MHC-Oct3/4 locus at developmental phases of embryonic stem cell differentiation. Dev. Biol. 298 (2006) 354-367
5. Babu J., Jeqanathan K., Baker D., Wu X., Kang-Decker N., and van Deursen J. Rae1 is an essential mitotic checkpoint regulator that cooperates with Bub3 to prevent chromosome missegregation. J. Cell Biol. 160 (2003) 341-353
6. Bai S., Rouquette J., Umeda M., Faigle W., Loew D., Sazer S., and Doye V. The fission yeast Nup107-120 complex functionally interacts with the small GTPase Ran/Spi1 and is required for mRNA export, nuclear pore distribution, and proper cell division. Mol. Cell. Biol. 24 (2004) 6379-6392
7. Belgareh N., Rabut G., Bai S., van Overbeek M., Beaudouin J., Daigle N., Zatsepina O., Pasteau F., Labas V., Fromont-Racine M., et al. An evolutionarily conserved NPC subcomplex, which redistributes in part to kinetochores in mammalian cells. J. Cell Biol. 154 (2001) 1147-1160
8. Berke I., Boehmer T., Blobel G., and Schwartz T. Structural and functional analysis of Nup133 domains reveals modular building blocks of the nuclear pore complex. J. Cell Biol. 167 (2004) 591-597
9. Bertrand N., Castro D., and Guillemot F. Proneural genes and the specification of neural cell types. Nat. Rev. Neurosci. 3 (2002) 517-530
10. Boehmer T., and Schwartz T. Purification, crystallization and preliminary X-ray analysis of a Nup107-Nup133 heterodimeric nucleoporin complex. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 63 (2007) 816-818
11. Boehmer T., Enninga J., Dales S., Blobel G., and Zhong H. Depletion of a single nucleoporin, Nup107, prevents the assembly of a subset of nucleoporins into the nuclear pore complex. Proc. Natl. Acad. Sci. USA 100 (2003) 981-985
12. Bradley A., and Robertson E. Embryo-derived stem cells: a tool for elucidating the developmental genetics of the mouse. Curr. Top. Dev. Biol. 20 (1986) 357-371
13. Burdon T., Smith A., and Savatier P. Signalling, cell cycle and pluripotency in embryonic stem cells. Trends Cell Biol. 12 (2002) 432-438
14. Chambers I., and Smith A. Self-renewal of teratocarcinoma and embryonic stem cells. Oncogene 23 (2004) 7150-7160
15. Do H.-J., Lim H.-Y., Kim J.-H., Song H., Chung H.-M., and Kim J.-H. An intact homeobox domain is required for complete nuclear localization of human Nanog. Biochem. Biophys. Res. Commun. 353 (2007) 770-775
16. Doye V., Wepf R., and Hurt E. A novel nuclear pore protein Nup133p with distinct roles in poly(A)+ RNA transport and nuclear pore distribution. EMBO J. 13 (1994) 6062-6075
17. Eggenschwiler J., and Anderson K. Dorsal and lateral fates in the mouse neural tube require the cell-autonomous activity of the open brain gene. Dev. Biol. 227 (2000) 648-660
18. Faria A., Levay A., Wang Y., Kamphorst A., Rosa M., Nussenzveig D., Balkan W., Chook Y., Levy D., and Fontoura B. The nucleoporin Nup96 is required for proper expression of interferon-regulated proteins and functions. Immunity 24 (2006) 283-290
19. Galy V., Mattaj I., and Askjaer P. Caenorhabditis elegans nucleoporins Nup93 and Nup205 determine the limit of nuclear pore complex size exclusion in vivo. Mol. Biol. Cell 14 (2003) 5104-5115
20. Garcia-Garcia M., Eggenschwiler J., Caspary T., Alcorn H., Wyler M., Huangfu D., Rakeman A., Lee J., Feinberg E., Timmer J., et al. Analysis of mouse embryonic patterning and morphogenesis by forward genetics. Proc. Natl. Acad. Sci. USA 102 (2005) 5913-5919
21. Gotz M., and Huttner W. The cell biology of neurogenesis. Nat. Rev. Mol. Cell Biol. 6 (2005) 777-788
22. Guan T., Kehlenbach R., Schirmer A., Kehlenbach A., Fan F., Clurman B., Arnheim N., and Gerace L. Nup50, a nucleoplasmically oriented nucleoporin with a role in nuclear protein export. Mol. Cell. Biol. 20 (2000) 5619-5630
23. Harel A., Orjalo A., Vincent T., Lachish-Zalait A., Vasu S., Shah S., Zimmerman E., Elbaum M., and Forbes D. Removal of a single pore subcomplex results in vertebrate nuclei devoid of nuclear pores. Mol. Cell 11 (2003) 853-864
24. Hebert J., Boyle M., and Martin G. mRNA localization studies suggest that murine FGF-5 plays a role in gastrulation. Development 112 (1991) 407-415
25. Hetzer M., Walther T., and Mattaj I. Pushing the envelope: structure, function, and dynamics of the nuclear periphery. Annu. Rev. Cell Dev. Biol. 21 (2005) 347-380
26. Hochedlinger K., Yamada Y., Beard C., and Jaenisch R. Ectopic expression of Oct-4 blocks progenitor-cell differentiation and causes dysplasia in epithelial tissues. Cell 121 (2005) 465-477
27. Hogan B., Beddington R., Costantini F., and Lacy E. Manipulating the Mouse Embryo: A Laboratory Manual (1994), Cold Spring Harbor Laboratory Press, Cold Spring Habor
28. Jen Y., Manova K., and Benezra R. Expression patterns of Id1, Id2, and Id3 are highly related but distinct from that of Id4 during mouse embryogenesis. Dev. Dyn. 207 (1996) 235-252
29. Jen Y., Manova K., and Benezra R. Each member of the Id gene family exhibits a unique expression pattern in mouse gastrulation and neurogenesis. Dev. Dyn. 208 (1997) 92-106
30. Jessell T. Neuronal specification in the spinal cord: inductive signals and transcriptional codes. Nat. Rev. Genet. 1 (2000) 20-29
31. Kalverda B., and Fornerod M. The nuclear life of nucleoporins. Dev. Cell 13 (2007) 164-165
32. Kanamori N., Madsen L., Radutoiu S., Frantescu M., Quistgaard E., Miwa H., Downie J., James E., Felle H., Haaning L., et al. A nucleoporin is required for induction of Ca2+ spiking in legume nodule development and essential for rhizobial and fungal symbiosis. Proc. Natl. Acad. Sci. USA 103 (2006) 359-364
33. Kouzarides T. Chromatin modifications and their function. Cell 128 (2007) 693-705
34. Lee J., Hart S., and Skalnik D. Histone deacetylase activity is required for embryonic stem cell differentiation. Genesis 38 (2004) 32-38
35. Loiodice I., Alves A., Rabut G., van Overbeek M., Ellenberg J., Sibarita J., and Doye V. The entire Nup107-160 complex, including three new members, is targeted as one entity to kinetochores in mitosis. Mol. Biol. Cell 15 (2004) 3333-3344
36. Moore M. Npap60: a new player in nuclear protein import. Trends Cell Biol. 13 (2003) 61-64
37. Okita K., Kiyonari H., Nobuhisa N., Aizawa S., and Taga T. Targeted disruption of the mouse ELYS gene results in embryonic death at peri-implantation development. Genes Cells 9 (2004) 1083-1091
38. Orjalo A., Amaotov A., Shen Z., Boyarchuk Y., Zeitlin S., Fontura B., Briggs S., Dasso M., and Forbes D. The Nup107-160 nucleoporin complex is required for correct bipolar spindle assembly. Mol. Biol. Cell 17 (2006) 3806-3818
39. Osmani A., Davies J., Liu H., Nile A., and Osmani S. Systematic deletion and mitotic localization of the nuclear pore complex proteins of Aspergillus nidulans. Mol. Biol. Cell 17 (2006) 4946-4961
40. Pan G., Qin B., Liu N., Scholer H., and Pei D. Identification of a nuclear localization signal in OCT4 and generation of a dominant negative mutant by its ablation. J. Biol. Chem. 279 (2004) 37013-37020
41. Pevny L., Lovell-Badge R., and Smith A. Generation of purified neural precursors from embryonic stem cells by lineage selection. Curr. Biol. 8 (1998) 971-974
42. Pfister S., Steiner K., and Tam P. Gene expression pattern and progression of embryogenesis in the immediate post-implantation period of mouse development. Gene Expr. Patterns 7 (2007) 558-573
43. Ralston A., and Rossant J. Genetic regulation of stem cell origins in the mouse embryo. Clin. Genet. 68 (2005) 106-112
44. Rhinn M., Dierich A., Shawlot W., Behringer R., Le Meur M., and Ang S. Sequential roles for Otx2 in visceral endoderm and neuroectoderm for forebrain and midbrain induction and specification. Development 125 (1998) 845-856
45. Ruzinova M., and Benezra R. Id proteins in development, cell cycle and cancer. Trends Cell Biol. 13 (2003) 410-418
46. Sabri N., Roth P., Xylourgidis F., Sadeghifar F., Adler J., and Samakovlis C. Distinct functions of the Drosophila Nup153 and Nup214 FG domains in nuclear protein transport. J. Cell Biol. 178 (2007) 557-565
47. Savatier P., Lapillonne H., van Grunsven L., Rudkin B., and Samarut J. Withdrawal of differentiation inhibitory activity/leukemia inhibitory factor up-regulates D-type cyclins and cyclin-dependent kinase inhibitors in mouse embryonic stem cells. Oncogene 12 (1996) 309-322
48. Scholer H., Dressler G., Balling R., Rohdewohld H., and Gruss P. Oct-4: a germline-specific transcription factor mapping to the mouse t-complex. EMBO J. 9 (1990) 2185-2195
49. Sjöblom T., Jones S., Wood L., Parsons D., Lin J., Barber T., Mandelker D., Leary R., Ptak J., Silliman N., et al. The consensus coding sequences of human breast and colorectal cancers. Science 314 (2006) 268-274
50. Smitherman M., Lee K., Swanger J., Kapur R., and Clurman B. Characterization and targeted disruption of murine Nup50, a p27(Kip1)-interacting component of the nuclear pore complex. Mol. Cell. Biol. 20 (2000) 5631-5642
51. Stern C. Neural induction: 10 years on since the 'default model'. Curr. Opin. Cell Biol. 18 (2006) 692-697
52. Taddei A. Active genes at the nuclear pore complex. Curr. Opin. Cell Biol. 19 (2007) 305-310
53. Tam P., and Rossant J. Mouse embryonic chimeras: tools for studying mammalian development. Development 130 (2003) 6155-6163
54. Tam P., and Loebel D. Gene function in mouse embryogenesis: get set for gastrulation. Nat. Rev. Genet. 8 (2007) 368-381
55. Tam P., Loebel D., and Tanaka S. Building the mouse gastrula: signals, asymmetry and lineages. Curr. Opin. Genet. Dev. 16 (2006) 419-425
56. Terry L., and Wente S. Nuclear mRNA export requires specific FG nucleoporins for translocation through the nuclear pore complex. J. Cell Biol. 178 (2007) 1121-1132
57. Tran E., and Wente S. Dynamic nuclear pore complexes: life on the edge. Cell 125 (2006) 1041-1053
58. van Deursen J., Boer J., Kasper L., and Grosveld G. G2 arrest and impaired nucleocytoplasmic transport in mouse embryos lacking the proto-oncogene CAN/Nup214. EMBO J. 15 (1996) 5574-5583
59. Vasu S., Shah S., Orjalo A., Park M., Fischer W., and Forbes D. Novel vertebrate nucleoporins Nup133 and Nup160 play a role in mRNA export. J. Cell Biol. 155 (2001) 339-354
60. Walther T., Alves A., Pickersgill H., Loiodice I., Hetzer M., Galy V., Hulsmann B., Kocher T., Wilm M., Allen T., et al. The conserved Nup107-160 complex is critical for nuclear pore complex assembly. Cell 113 (2003) 195-206
61. Wianny F., Real F., Mummery C., Van Rooijen M., Lahti J., Samarut J., and Savatier P. G1-phase regulators, cyclin D1, cyclin D2, and cyclin D3: up-regulation at gastrulation and dynamic expression during neurulation. Dev. Dyn. 212 (1998) 49-62
62. Wichterle H., Lieberam I., Porter J., and Jessell T. Directed differentiation of embryonic stem cells into motor neurons. Cell 110 (2002) 385-397
63. Williams R., Azuara V., Perry P., Sauer S., Dvorkina M., Jørgensen H., Roix J., McQueen P., Misteli T., Merkenschlager M., et al. Neural induction promotes large-scale chromatin reorganisation of the Mash1 locus. J. Cell Sci. 119 (2006) 132-140
64. Winnier G., Blessing M., Labosky P., and Hogan B. Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev. 9 (1995) 2105-2116
65. Wood L.D., Parsons D.W., Jones S., Lin J., Sjoblom T., Leary R.J., Shen D., Boca S.M., Barber T., Ptak J., et al. The genomic landscapes of human breast and colorectal cancers. Science 318 (2007) 1108-1113
66. Wu X., Kasper L., Mantcheva R., Mantchev G., Springett M., and van Deursen J. Disruption of the FG nucleoporin NUP98 causes selective changes in nuclear pore complex stoichiometry and function. Proc. Natl. Acad. Sci. USA 98 (2001) 3191-3196
67. Xu L., and Massague J. Nucleocytoplasmic shuttling of signal transducers. Nat. Rev. Mol. Cell Biol. 5 (2004) 209-219
68. Yasuhara N., Shibazaki N., Tanaka S., Nagai M., Kamikawa Y., Oe S., Asally M., Kamachi Y., Kondoh H., and Yoneda Y. Triggering neural differentiation of ES cells by subtype switching of importin-alpha. Nat. Cell Biol. 9 (2007) 72-79
69. Ying Q., Nichols J., Chambers I., and Smith A. BMP induction of Id proteins suppresses differentiation and sustains embryonic stem cell self-renewal in collaboration with STAT3. Cell 115 (2003) 281-292
70. Zuccolo M., Alves A., Galy V., Bolhy S., Formstecher E., Racine V., Sibarita J.-B., Fukagawa T., Shiekhattar R., Yen T., et al. The human Nup107-160 nuclear pore subcomplex contributes to proper kinetochore functions. EMBO J. 26 (2007) 1853-1864