Numb independently antagonizes Sanpodo membrane targeting and Notch signaling in Drosophila sensory organ precursor cells

Molecular Biology of the Cell

Volumn 21, Issue 5, 2010, Pages 802-810

  Tong, Xin ^a,b   Zitserman, Diana ^a   Serebriiskii, Ilya ^a   Andrake, Mark ^a   Dunbrack, Roland ^a   Roegiers, Fabrice ^a  

^a FOX CHASE CANCER CENTER   (United States)

^b UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; NOTCH RECEPTOR; SANPODO; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL FATE; CELL MEMBRANE; DROSOPHILA; GENE DELETION; IMMUNOHISTOCHEMISTRY; IN VIVO STUDY; MITOSIS; MOLECULAR MODEL; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN TARGETING; REGULATORY MECHANISM; SENSE ORGAN; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; STEM CELL; STRUCTURE ACTIVITY RELATION; TRANSGENE;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; CELL MEMBRANE; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; JUVENILE HORMONES; MICROFILAMENT PROTEINS; MITOSIS; MOLECULAR SEQUENCE DATA; NEURONS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, NOTCH; SEQUENCE HOMOLOGY, AMINO ACID;

HEXAPODA; VERTEBRATA;

EID: 77649135481     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E09-09-0831     Document Type: Article

References (37)

1. Berdnik, D., Torok, T., Gonzalez-Gaitan, M., and Knoblich, J. A. (2002). The endocytic protein alpha-Adaptin is required for numb-mediated asymmetric cell division in Drosophila. Dev. Cell 3, 221-231.
2. Borg, J. P., Ooi, J., Levy, E., and Margolis, B. (1996). The phosphotyrosine interaction domains of X11 and FE65 bind to distinct sites on the YENPTY motif of amyloid precursor protein. Mol. Cell. Biol. 16, 6229-6241.
3. Brand, A. H., and Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415.
4. Calderwood, D. A., Fujioka, Y., de Pereda, J. M., Garcia-Alvarez, B., Nakamoto, T., Margolis, B., McGlade, C. J., Liddington, R. C., and Ginsberg, M. H. (2003). Integrin beta cytoplasmic domain interactions with phosphotyrosine-binding domains: a structural prototype for diversity in integrin signaling. Proc. Natl. Acad. Sci. USA 100, 2272-2277.
5. Canutescu, A. A., Shelenkov, A. A., and Dunbrack, R. L., Jr. (2003). A graph-theory algorithm for rapid protein side-chain prediction. Protein Sci. 12, 2001-2014.
6. Cayouette, M., and Raff, M. (2002). Asymmetric segregation of Numb: a mechanism for neural specification from Drosophila to mammals. Nat. Neurosci. 5, 1265-1269.
7. Chen, W. J., Goldstein, J. L., and Brown, M. S. (1990). NPXY, a sequence often found in cytoplasmic tails, is required for coated pit-mediated internalization of the low density lipoprotein receptor. J. Biol. Chem. 265, 3116-3123.
8. Clamp, M., Cuff, J., Searle, S. M., and Barton, G. J. (2004). The Jalview Java alignment editor. Bioinformatics 20, 426-427.
9. Fischer, J. A., Eun, S.H., and Doolan, B. T. (2006). Endocytosis, endosome trafficking, and the regulation of Drosophila development. Annu. Rev. Cell Dev. Biol. 22, 181-206.
10. Frise, E., Knoblich, J. A., Younger-Shepherd, S., Jan, L. Y., and Jan, Y. N. (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.
11. Garcia-Alvarez, B., de Pereda, J. M., Calderwood, D. A., Ulmer, T. S., Critchley, D., Campbell, I. D., Ginsberg, M. H., and Liddington, R. C. (2003). Structural determinants of integrin recognition by talin. Mol. Cell 11, 49-58.
12. Guo, M., Jan, L. Y., and Jan, Y. N. (1996). Control of daughter cell fates during asymmetric division: interaction of Numb and Notch. Neuron 17, 27-41.
13. Hsu, D., Knudson, P. E., Zapf, A., Rolband, G. C., and Olefsky, J. M. (1994). NPXY motif in the insulin-like growth factor-I receptor is required for efficient ligand-mediated receptor internalization and biological signaling. Endocrinology 134, 744-750.
14. Hutterer, A., and Knoblich, J. A. (2005). Numb and alpha-Adaptin regulate Sanpodo endocytosis to specify cell fate in Drosophila external sensory organs. EMBO Rep. 6, 836-842.
15. Jafar-Nejad, H., Andrews, H. K., Acar, M., Bayat, V., Wirtz-Peitz, F., Mehta, S. Q., Knoblich, J. A., and Bellen, H. J. (2005). Sec15, a component of the exocyst, promotes Notch signaling during the asymmetric division of Drosophila sensory organ precursors. Dev Cell. 9, 351-363.
16. Justice, N., Roegiers, F., Jan, L. Y., and Jan, Y. N. (2003). Lethal giant larvae acts together with numb in notch inhibition and cell fate specification in the Drosophila adult sensory organ precursor lineage. Curr. Biol. 13, 778-783.
17. Knoblich, J. A. (2008). Mechanisms of asymmetric stem cell division. Cell 132, 583-597.
18. Kyriazis, G. A., Wei, Z., Vandermey, M., Jo, D. G., Xin, O., Mattson, M. P., and Chan, S. L. (2008). Numb endocytic adapter proteins regulate the transport and processing of the amyloid precursor protein in an isoform-dependent manner: implications for Alzheimer disease pathogenesis. J. Biol. Chem. 283, 25492-25502.
19. Langevin, J., Le Borgne, R., Rosenfeld, F., Gho, M., Schweisguth, F., and Bellaiche, Y. (2005). Lethal giant larvae controls the localization of notchsignaling regulators numb, neuralized, and Sanpodo in Drosophila sensoryorgan precursor cells. Curr. Biol. 15, 955-962.
20. Lee, T., and Luo, L. (2001). Mosaic analysis with a repressible cell marker (MARCM) for Drosophila neural development. Trends Neurosci. 24, 251-254.
21. McGill, M. A., Dho, S. E., Weinmaster, G., and McGlade, C. J. (2009). Numb regulates post-endocytic trafficking and degradation of Notch1. J. Biol. Chem. 284, 26427-26438.
22. McGill, M. A., and McGlade, C. J. (2003). Mammalian numb proteins promote Notch1 receptor ubiquitination and degradation of the Notch1 intracellular domain. J. Biol. Chem. 278, 23196-23203.
23. Nilsson, L., Conradt, B., Ruaud, A. F., Chen, C. C., Hatzold, J., Bessereau, J. L., Grant, B. D., and Tuck, S. (2008). Caenorhabditis elegans num-1 negatively regulates endocytic recycling. Genetics 179, 375-387.
24. Nishimura, T., and Kaibuchi, K. (2007). Numb controls integrin endocytosis for directional cell migration with aPKC and PAR-3. Dev. Cell 13, 15-28.
25. O'Connor-Giles, K. M., and Skeath, J. B. (2003). Numb inhibits membrane localization of Sanpodo, a four-pass transmembrane protein, to promote asymmetric divisions in Drosophila. Dev. Cell 5, 231-243.
26. Petersen, P. H., Tang, H., Zou, K., and Zhong, W. (2006). The enigma of the numb-Notch relationship during mammalian embryogenesis. Dev. Neurosci. 28, 156-168.
27. Rhyu, M. S., Jan, L. Y., and Jan, Y. N. (1994). Asymmetric distribution of numb protein during division of the sensory organ precursor cell confers distinct fates to daughter cells. Cell 76, 477-491.
28. Roegiers, F., Jan, L. Y., and Jan, Y. N. (2005). Regulation of membrane localization of Sanpodo by lethal giant larvae and neuralized in asymmetrically dividing cells of Drosophila sensory organs. Mol. Biol. Cell 16, 3480-3487.
29. Roegiers, F., and Jan, Y. N. (2004). Asymmetric cell division. Curr. Opin. Cell Biol. 16, 195-205.
30. Roegiers, F., Younger-Shepherd, S., Jan, L. Y., and Jan, Y. N. (2001). Two types of asymmetric divisions in the Drosophila sensory organ precursor cell lineage. Nat. Cell Biol. 3, 58-67.
31. Santolini, E., Puri, C., Salcini, A. E., Gagliani, M. C., Pelicci, P. G., Tacchetti, C., and Di Fiore, P. P. (2000). Numb is an endocytic protein. J. Cell Biol. 151, 1345-1352.
32. Smith, C. A., Dho, S. E., Donaldson, J., Tepass, U., and McGlade, C. J. (2004). The cell fate determinant numb interacts with EHD/Rme-1 family proteins and has a role in endocytic recycling. Mol. Biol. Cell 15, 3698-3708.
33. Stolt, P. C., Jeon, H., Song, H. K., Herz, J., Eck, M. J., and Blacklow, S. C. (2003). Origins of peptide selectivity and phosphoinositide binding revealed by structures of disabled-1 PTB domain complexes. Structure 11, 569-579.
34. Thompson, J. D., Higgins, D. G., and Gibson, T. J. (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22, 4673-4680.
35. Uhlik, M. T., Temple, B., Bencharit, S., Kimple, A. J., Siderovski, D. P., and Johnson, G. L. (2005). Structural and evolutionary division of phosphotyrosine binding (PTB) domains. J. Mol. Biol. 345, 1-20.
36. Wang, Q., Canutescu, A. A., and Dunbrack, R. L., Jr. (2008). SCWRL and MolIDE: computer programs for side-chain conformation prediction and homology modeling. Nat. Protoc. 3, 1832-1847.
37. Zwahlen, C., Li, S. C., Kay, L. E., Pawson, T., and Forman-Kay, J. D. (2000). Multiple modes of peptide recognition by the PTB domain of the cell fate determinant Numb. EMBO J. 19, 1505-1515.