The neural RNA-binding protein musashi1 translationally regulates mammalian numb gene expression by interacting with its mRNA

Molecular and Cellular Biology

Volumn 21, Issue 12, 2001, Pages 3888-3900

  Imai, Takao ^a,b,c   Tokunaga, Akinori ^a,b   Yoshida, Tetsu ^a,b   Hashimoto, Mitsuhiro ^d   Mikoshiba, Katsuhiko ^d,e   Weinmaster, Gerry ^f,g   Nakafuku, Masato ^h,i   Okano, Hideyuki ^a,b,i  

^a KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c OSAKA UNIVERSITY   (Japan)

^d RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

^e UNIVERSITY OF TOKYO   (Japan)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

^h UNIVERSITY OF TOKYO   (Japan)

ⁱ JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GENE PRODUCT; MESSENGER RNA; PROTEIN MUSASHI1; PROTEIN NUMB; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; ASSAY; CONTROLLED STUDY; DOWN REGULATION; GENE EXPRESSION; GENE TARGETING; GENETIC TRANSCRIPTION; IN VITRO STUDY; MOUSE; NONHUMAN; PRECIPITATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; RNA BINDING; RNA TRANSLATION; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; STEM CELL; TRANSLATION REGULATION;

3T3 CELLS; ANIMALS; BASE SEQUENCE; DNA PRIMERS; DOWN-REGULATION; FUNGAL PROTEINS; GENES, REPORTER; LIGANDS; MEMBRANE PROTEINS; MICE; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; NERVE TISSUE PROTEINS; NEURONS; NUCLEIC ACID CONFORMATION; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; RECEPTORS, NOTCH; RNA; RNA, MESSENGER; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; STEM CELLS; TRANS-ACTIVATION (GENETICS);

ADENOVIRIDAE; ANIMALIA; MAMMALIA;

EID: 0035016795     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.21.12.3888-3900.2001     Document Type: Article

References (72)

1. Akamatsu, W., H. J. Okano, N. Osumi, T. Inoue, S. Nakamura, S. Sakakibara, M. Miura, N. Matsuo, R. B. Darnell, and H. Okano. 1999. Mammalian ELAV-like neuronal RNA-binding proteins HuB and HuC promote neuronal development in both the central and peripheral nervous systems. Proc. Natl. Acad. Sci. USA 96:9885-9890.
2. Antic, D., N. Lu, and J. D. Keene. 1999. ELAV tumor antigen, Hel-N1, increases translation of neurofilament M mRNA and induces formation of neurites in human teratocarcinoma cells. Genes Dev. 13:449-461.
3. Artavanis-Tsakonas, S., K. Matsuno, and M. F. Fortini. 1995. Notch signaling. Science 268:225-232.
4. Artavanis-Tsakonas, S., M. D. Rand, and R. J. Lake. 1999. Notch signaling: cell fate control and signal integration in development. Science 284:770-776.
5. Beatus, P., J. Lundkvist, C. Oberg, U. Lendahl. 1999. The Notch3 intracellular domain represses Notch1-mediated activation through Hairy/Enhancer of split (HES) promoters. Development 126:3925-3935.
6. Buckanovich, R. J., and R. B. Darnell. 1997. The neuronal RNA binding protein Nova-1 recognizes specific RNA targets in vitro and in vivo. Mol. Cell. Biol. 17:3194-3201.
7. Burd, C. G., and G. Dreyfuss. 1994. RNA binding specificity of hnRNP A1: significance of hnRNP A1 high affinity binding sites in pre-mRNA splicing. EMBO J. 13:1197-1204.
8. Burd, C. G., and G. Dreyfuss. 1994. Conserved structures and diversity of functions of RNA-binding protein. Science 263:615-621.
9. Carlesso, N., J. C. Aster, J. Sklar, and D. T. Scadden. 1999. Notch1-induced delay of human hematopoietic progenitor cell differentiation is associated with altered cell cycle kinetics. Blood 93:838-848.
10. Chung, C. N., Y. Hamaguchi, T. Honjo, and M. Kawaichi. 1994. Site-directed mutagenesis study on DNA binding regions of the mouse homologue of Suppressor of Hairless, RBP-J kappa. Nucleic Acids Res. 22:2938-2944.
11. Conne, B., A. Stutz, and J. D. Vassalli. 2000. The 3' untranslated region of messenger RNA: a molecular 'hotspot' for pathology? Nat. Med. 6:637-641.
12. Dho, S. E., M. B. French, S. T. Woods, and S. J. McGlade. 1999. Characterization of four mammalian Numb protein isoforms. J. Biol. Chem. 274: 33097-33104.
13. Fan, X. C., and J. A. Steitz. 1998. Overexpression of HuR, a nuclear-cytoplasmic shuttling protein, increases the in vivo stability of ARE-containing mRNAs. EMBO J. 17:3448-3460.
14. Frise, E., J. A. Knoblich, S. Younger-Shepherd, L. Y. Jan, and Y. N. Jan. 1996. The Drosophila Numb protein inhibits signaling of the Notch receptor during cell-cell interaction in sensory organ lineage. Proc. Natl. Acad. Sci. USA 93:11925-11932.
15. Good, P. J., Y. Akinori, S. Sakakibara, A. Yamamoto, T. Imai, H. Sawa, T. Ikeuti, S. Tsuji, H. Satoh, and H. Okano. 1998. The human Musashi homolog I (MSI1) encoding the homologue of Musashi/Nrp-1, a neural RNA-binding protein putatively expressed in CNS stem cell and neural progenitor cells. Genomics 52:382-384.
16. Gray, N. K., and M. Wickens. 1998. Control of translation initiation in animals. Annu. Rev. Cell Dev. Biol. 14:399-458.
17. Grosset, C., C. Y. Chen, N. Xu, N. Sonenberg, H. Jacquemin-Sablon, and A. B. Shyu. 2000. A mechanism for translationally coupled mRNA turnover: interaction between the poly(A) tail and a c-fos RNA coding determinant via a protein complex. Cell 103:29-40.
18. Guo, M., L. Y. Jan, and Y. N. Jan. 1996. Control of daughter cell fates during asymmetric division: interaction of Numb and Notch. Neuron 17:27-41.
19. Hashimoto, M., J. Aruga, Y. Hosoya, Y. Kanegae, I. Saito, and K. Mikoshiba. 1996. A neural cell-type-specific expression system using recombinant adenovirus vectors. Hum. Gene Ther. 7:149-158.
20. Heaphy, S., C. Dingwall, I. Ernberg, M. J. Gait, S. M. Green, J. Karn, A. D. Lowe, M. Singh, and M. A. Skinner. 1990. HIV-1 regulator of virion expression (Rev) protein binds to an RNA stem-loop structure located within the Rev response element region. Cell 60:685-693.
21. Hirota, Y., M. Okabe, T. Imai, M. Kurusu, A. Yamamoto, S. Miyao, M. Nakamura, K. Sawamoto, and H. Okano. 1999. Musashi and seven in absentia downregulate tramtrack through distinct mechanisms in Drosophila eye development. Mech. Dev. 87:93-101.
22. Hutton, M., C. L. Lendon, et al. 1998. Association of missense and 5'-splice-site mutations in tau with the inherited dementia FTDP-17. Nature 393:702-705.
23. Jan, Y. N., and L. Y. Jan. 1998. Asymmetric cell division. Nature 392:775-778.
24. Jarriault, S., C. Brou, F. Logeat, E. H. Schroeter, R. Kopan, and A. Israel. 1995. Signalling downstream of activated mammalian Notch. Nature 377: 355-358.
25. Jensen, K. B., B. K. Dredge, G. Stetani, R. Zhong, R. J. Buckanovich, H. J. Okano, Y. Y. Yang, and R. B. Daenell. 2000. Nova-1 regulates neuron-specific alternative splicing and is essential for neuronal viability. Neuron 25:359-371.
26. Joseph, B., M. Orlian, and H. Furneaux. 1998. p21(wafl) mRNA contains a conserved element in its 3'-untranslated region that is bound by the Elav-like mRNA-stabilizing proteins. J. Biol. Chem. 273:20511-20516.
27. Kajita, Y., J. Nakayama, M. Aizawa, and F. Ishikawa. 1995. The UUAG-specific RNA binding protein, heterogeneous nuclear ribonucleoprotein DO. J. Biol. Chem. 270:22168-22175.
28. Kaneko, Y., S. Sakakibara, T. Imai, A. Suzuki, Y. Nakamura, K. Sawamoto, Y. Ogawa, T. Toyama, and H. Okano. 2000. Musashil: evolutionarily conserved markers for CNS progenitor cells including neural stem cells. Dev. Neurosci. 22:138-152.
29. Kato, H., Y. Taniguchi, H. Kurooka, S. Minoguchi, T. Sakai, S. Nomura-Okazaki, K. Tamura, and T. Honjo. 1997. Involvement of RBP-J in biological functions of mouse Notch1 and its derivatives. Development 124:4133-4141.
30. Klausner, R. D., and J. B. Harford. 1989. cis-trans models for post-transcriptional gene regulation. Science 246:870-872.
31. Kurihara, Y., Y. Nagata, T. Imai, A. Hiwatasi, M. Horiuchi, S. Sakakibara, M. Katahira, H. Okano, and S. Uesugi. 1997. Structural properties and RNA-binding activities of two RNA recognition motifs of a mouse neural RNA-binding protein, mouse-Musashi-l. Gene 186:21-27.
32. Levine, T. D., F. Gao, P. H. King, L. G. Andrews, and J. D. Keene. 1993. Hel-Nl: an autoimmune RNA-binding protein with specificity tor 3' uridylate-rich untranslated regions of growth factor mRNAs. Mol. Cell. Biol. 13:3494-3504.
33. Lewis, H. A., K. Musunuru, K. B. Jensen, C. Edo, H. Chen, R. B. Darnell, and S. R. Burley. 2000. Sequence-specific RNA binding by Nova KH domain: implications for paraneoplastic disease and the fragile X. Cell 100: 323-332.
34. Liu, J., J. Dalmau, A. Szabo, M. Rosenfeld, J. Huber, and H. Furneaux. 1995. Paraneoplastic encephalomyelitis antigens bind to the AU-rich elements of mRNA. Neurology 45:544-550.
35. Myer, V. E., X. C. Fan, and J. A. Steitz. 1997. Identification of HuR as a protein implicated in AUUUA-mediated mRNA decay. EMBO J. 16:2130-2139.
36. Nagata, T., R. Kanno, Y. Kurihara, S. Uesugi, T. Imai, S. Sakakibara, H. Okano, and M. Katahira. 1999. Structural, backbone dynamics and interactions with RNA of the C-terminal RNA-binding domain of a mouse neural RNA-binding protein, Musashil. J. Mol. Biol. 287:315-330.
37. Nakafuku, M., and S. Nakamura. 1995. Establishment and characterization of a multipotential neural cell line that can conditionally generate neurons, astrocytes, and oligodendrocytes in vitro. J. Neurosci. Res. 41:153-168.
38. Nakamura, M., H. Okano, J. Blendy, and C. Montell. 1994. Musashi, a neural RNA-binding protein required for Drosophila adult external sensory organ development. Neuron 13:68-81.
39. Nakamura, Y., S. Sakakibara, T. Miyata, M. Ogawa, T. Shimazaki, S. Weiss, R. Kageyama, and H. Okano. 2000. The bHLH gene hesl as a repressor of the neuronal commitment of CNS stem cells. J. Neurosci. 20:283-293.
40. Niwa, H., K. Yamamura, and J. Miyazaki. 1991. Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108:193-200.
41. Nofziger, D., A. Miyamoto, K. M. Lyons, and G. Weinmaster. 1999. Notch signaling imposes two distinct blocks in the differentiation of C2C12 myoblasts. Development 126:1689-1702.
42. Ordentlich, P., A. Lin, C. P. Shen, C. Blaumueller, K. Matsuno, S. Artavanis-Tsakonas, and T. Kadesch. 1998. Notch inhibition of E47 supports the existence of a novel signaling pathway. Mol. Cell. Biol. 18:2230-2239.
43. Okabe, M., T. Imai, M. Kurusu, Y. Hiromi, and H. Okano. Translational repression determines a neuronal potential in Drosophila asymmetric cell division. Nature, in press.
44. Okano, H. 1995. Two major mechanisms regulating cell-fate decisions in the developing nervous system. Dev. Growth Differ. 37:619-629.
45. Okano, H. J., and R. B. Darnell. 1997. A hierarchy of Hu RNA binding proteins in developing and adult neurons. J. Neurosci. 17:3024-3037.
46. Oubridge, C., N. Ito, P. R. Evans, C. H. Teo, and K. Nagai. 1994. Crystal structure at 1.92 Å resolution ot the RNA-binding domain of the U1A spliceosomal protein complexed with an RNA hairpin. Nature 372:432-438.
47. Paris, M., and H. Lin. 2000. Translational repression: a duet of Nanos and Pumilio. Curr. Biol. 10:R81-R83.
48. Pengs, S. S., C. Y. Chen, N. Xu, and A. B. Shyu. RNA stabilization by AU-rich element binding protein. HuR, an ELAV protein. EMBO J. 17: 3461-3470.
49. Pincus, D. W., H. Keyoung, C. Restelli, R. R. Goodman, R. A. R. Fraser, M. Edgar, S. Sakakibara, H. Okano, M. Nedergaad, and S. A. Goldman. 1998. FGF2/BDNF-responsive neuronal progenitor cells in the adult human subependyma. Ann. Neurol. 43:576-585.
50. Rand, M. D., L. M. Grimm, S. Artavanis-Tsakonas, V. Patriub, S. C. Blacklow, J. Sklar, and J. C. Aster. 2000. Calcium depletion dissociates and activates heterodimeric notch receptors. Mol. Cell. Biol. 20:1825-1835.
51. Rao, P. K., M. Dorsch, T. Chickering, G. Zheng, C. Jiang, A. Goodearl, T. Kadesch, and S. McCarthy. 2000. Isolation and characterization of the notch ligand delta4. Exp. Cell Res. 260:379-386.
52. Sakakibara, S., T. Imai, K. Hamaguchi, M. Okabe, J. Aruga, K. Nakajima, D. Yasutomi, T. Nagata, Y. Kurihara, S. Uesugi, T. Miyata, M. Ogawa, K. Mikoshiba, and H. Okano. 1996. Mouse-musashi-l, neural RNA-binding protein highly enriched in the mammalian CNS stem cell. Dev. Biol. 176: 230-242.
53. Sakakibara, S., and H. Okano. 1997. Expression of neural RNA-binding proteins in the postnatal CNS: implication of their roles in neural and glial cell development. J. Neurosci. 17:8300-8312.
54. Sestan, N., S. Artavanis-Tsakonas, and P. Rakic. 1999. Contact-dependent inhibition of cortical neurite growth mediated by notch signaling. Science 286:741-746.
55. Shyu, A. B., and M. F. Wilkinson. 2000. The double lives of shuttling mRNA binding protein. Cell 102:135-138.
56. Siomi, H., M. C. Siomi, R. L. Nusshaum, and G. Dreyfuss. 1993. The protein product of lhe fragile X gene, FMR1, has characteristics of an RNA-binding protein. Cell 74:291-298.
57. Siomi, H., and G. Dreyfuss. 1997. RNA-binding proteins as regulators of gene expression. Curr. Opin. Genet. Dev. 7:345-353.
58. Siomi, M. C., Y. Zhang, H. Siomi, and G. Dreyfuss. 1996. Specific sequences in the fragile X syndrome protein FMR1 and the FXR proteins mediate their binding to 60S ribosomal subunits and the interactions among them. Mol. Cell. Biol. 16:3825-3832.
59. Steitz, J. A. 1989. Immunoprecipitation of ribonucleoproteins using autoantibodies. Methods Enzymol. 180:468-481.
60. Toda, M., Y. Iizuka, W.-J. Yu, E. Ikeda, K. Yoshida, T. Imai, T. Kawase, Y. Kawakami, H. Okano, and K. Uyemura. 2001. Expression of the neural RNA-binding protein Musashil in human gliomas. Glia 34:1-7.
61. Tsai, D. E., D. S. Harper, and J. D. Keene. 1991. Ul-snRNP-A protein selects a ten nucleotide consensus sequence from a degenerate RNA pool presented in various structural contexts. Nucleic Acids Res. 19:4931-4936.
62. Uemura, T., S. Shepherd, L. Ackerman, L. Y. Jan, and Y. N. Jan. 1989. numb, a gene required in determination of cell fate during sensory organ formation in Drosophila embryos. Cell 58:349-360.
63. Verdi, J. M., R. Schmandt, A. Bashirullah, S. Jacob, R. Salvino, C. G. Craig, A. E. Program, H. D. Lipshitz, and C. J. McGlade. 1996. Mammalian NUMB is an evolutionarily conserved signaling adapter protein that specifies cell fate. Curr. Biol. 6:1134-1145.
64. Wakamatsu, Y., and J. A. Weston. 1997. Sequential expression and role of Hu RNA-binding proteins during neurogenesis. Development 124:3449-3460.
65. Wakamatsu, Y., T. M. Maynard, S. U. Jones, and J. A. Weston. 1999. NUMB localizes in the basal cortex of mitotic avian neuroepithelial cells and modulates neuronal differentiation by binding to NOTCH-1. Neuron 23:71-81.
66. Wickens, M., J. Kimble, and S. Strickland. 1996. Translational control of developmental decisions, p. 411-450. In J. W. B. Hershey, M. B. Mathews, and N. Sonenberg (ed.), Translational control, vol. 30. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N. Y.
67. Wong, M. K., L. Prudovsky, C. Vary, C. Booth, L. Liaw, S. Mousa, D. Small, and T. Maciag. 2000. A non-transmembrane form of Jagged-1 regulates the formation of matrix-dependent chord-like structures. Biochem. Biophys. Res. Commun. 268:853-859.
68. Xu, N., C. Y. Chen, and A. B. Shyu. 1997. Modulation of the fate of cytoplasmic mRNA by AU-rich elements: key sequence features controlling mRNA deadenylation and decay. Mol. Cell. Biol. 17:4611-4621.
69. Yao, K. M., M. L. Samson, R. Reeves, and K. White. 1993. Gene elav of Drosophila melanogaster: a prototype for neuronal-specific RNA binding protein gene family that is conserved in flies and humans. J. Neurobiol. 24:723-739.
70. Zhong, W., J. H. Feder, M. M. Jiang, L. Y. Jan, and Y. N. Jan. 1996. Asymmetric localization of a mammalian Numb homolog during mouse cortical neurogenesis. Neuron 17:43-53.
71. Zhong, W., M. M. Jiang, G. Weinmaster, L. Y. Jan, and Y. N. Jan. 1997. Differential expression of mammalian Numb, Numblike and Notch I suggests distinct roles during mouse cortical neurogenesis. Development 124:1887-1897.
72. Zhong, W., M. M. Jiang, M. D. Schonemann, J. J. Meneses, R. A. Pedersen, L. Y. Jan, and Y. N. Jan. 2000. Mouse numb is an essential gene involved in cortical neurogenesis. Proc. Natl. Acad. Sci. USA 97:6844-6849.