Numb regulates Notch1, but not Notch3, during myogenesis

Mechanisms of Development

Volumn 128, Issue 5-6, 2011, Pages 247-257

  Beres, Brian J ^a   George, Rajani ^a,b   Lougher, Eric J ^a   Barton, Michael ^a   Verrelli, Brian C ^a,b   McGlade, C Jane ^c,d   Rawls, J Alan ^a,b   Wilson Rawls, Jeanne ^a  

^a ARIZONA STATE UNIVERSITY   (United States)

^b ARIZONA STATE UNIVERSITY   (United States)

^c HOSPITAL FOR SICK CHILDREN   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

Myogenesis; Notch; Numb; Ubiquitination

Indexed keywords

ADAPTOR PROTEIN; NOTCH1 RECEPTOR; NOTCH3 RECEPTOR; NUMB PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE INTERACTION; GENE TARGETING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MOUSE; MUSCLE DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN PROTEIN INTERACTION; TRANSCRIPTION REGULATION; UBIQUITINATION;

AMINO ACID SEQUENCE; ANIMALS; CELL DIFFERENTIATION; GENES, REPORTER; IMMUNOPRECIPITATION; LUCIFERASES; MEMBRANE PROTEINS; MICE; MOLECULAR SEQUENCE DATA; MUSCLE DEVELOPMENT; NERVE TISSUE PROTEINS; NIH 3T3 CELLS; PEPTIDE FRAGMENTS; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEIN STRUCTURE, TERTIARY; RECEPTOR, NOTCH1; RECEPTORS, NOTCH; RECOMBINANT FUSION PROTEINS; SEQUENCE ALIGNMENT; TRANSCRIPTIONAL ACTIVATION; UBIQUITINATION;

VERTEBRATA;

EID: 79959723262     PISSN: 09254773     EISSN: 18726356     Source Type: Journal    
DOI: 10.1016/j.mod.2011.02.002     Document Type: Article

References (64)

1. Amsen D., Blander J.M., Lee G.R., Tanigaki K., Honjo T., Flavell R.A. Instruction of distinct CD4 T helper cell fates by different Notch ligands on antigen-presenting cells. Cell 2004, 117:515-526.
2. Anderson A.C., Kitchens E.A., Chan S.W., St.Hill C., Jan Y.N., Zhong W., Robey E.A. The Notch regulator Numb links the Notch and TCR signaling pathways. J. Immunol. 2005, 174:890-897.
3. Artavanis-Tsakonis S., Rand M.D., Lake R.J. Notch signaling: cell fate control and signal integration in development. Science 1999, 288:770-776.
4. Bani-Yaghoub M., Kubu C.J., Cowling R., Rochira J., Nikopoulos G.N., Bellum S., Verdi J.M. A switch in numb isoforms is a critical step in cortical development. Dev. Dyn. 2007, 236:696-705.
5. Carmena A., Gisselbrecht S., Harrison J., Jiménez F., Michelson A.M. Combinatorial signaling codes for the progressive determination of cell fates in the Drosophila embryonic mesoderm. Genes Dev. 1998, 12:3910-3922.
6. Chastagner P., Israel A., Brou C. AIP4/Itch regulates Notch receptor degradation in the absence of ligand. PLoS One 2008, 3:e2735.
7. Cheng H.-T., Kim M., Valerius M.T., Surendran K., Schuster-Gossler K., Gossler A., McMahon A.P., Kopan R. Notch2, but not Notch1, is required for proximal fate acquisition in the mammalian nephron. Development 2007, 134:801-811.
8. Conboy I.M., Rando T.A. The regulation of Notch signaling controls satellite cell activation and cell fate determination in postnatal myogenesis. Dev. Cell 2002, 3:397-409.
9. Conlon R.A., Reaume A.G., Rossant J. Notch1 is required for the coordinate segmentation of somites. Development 1995, 121:1533-1545.
10. DiMarcotullio L., Ferretti E., Greco A., De Smaele E., Po A., Sico M.A., Alimandi M., Giannini G., Maroder M., Screpanti I., Gulino A. Numb is a suppressor of Hedgehog signalling and targets Gli1 for Itch-dependent ubiquitination. Nat. Cell Biol. 2006, 8:1415-1423.
11. Dho S.E., French M.B., Woods S.A., McGlade C.J. Characterization of four mammalian Numb protein isoforms. J. Biol. Chem. 1999, 274:33097-33104.
12. Franco Del Amo F., Smith D.E., Swiatek P.J., Gendron-Maguire M., Greenspan R.J., McMahon A.P., Gridley T. Expression pattern of Motch, a mouse homolog of Drosophila Notch, suggests an important role in early postimplantation mouse development. Development 1992, 115:737-744.
13. Guo M., Jan L.Y., Jan Y.N. Control of daughter cell fates during asymmetric division: interaction of Numb and Notch. Neuron 1996, 17:27-41.
14. Hamada Y., Kadokawa Y., Okabe M., Ikawa M., Coleman J.R., Tsujimoto Y. Mutation in ankyrin repeats of the mouse Notch2 gene induces early embryonic lethality. Development 1999, 126:3415-3424.
15. Han Z., Bodmer R. Myogenic cells fates are antagonized by Notch only in asymmetric lineages of the Drosophila heart, with or without cell division. Development 2003, 130:3039-3051.
16. Hansson E.M., Lendahl U., Chapman G. Notch signaling in development and disease. Sem. Cancer Biol. 2004, 14:320-328.
17. Hershko A., Ciechanover A. The ubiquitin system. Ann. Rev. Biochem. 1992, 67:425-479.
18. Holowacz T., Zeng L., Lassar A.B. Asymmetric localization of numb in the chick somite and the influence of myogenic signals. Dev. Dyn. 2006, 235:633-645.
19. Huang E.J., Li H., Tang A.A., Wiggins A.K., Neve R.L., Zhong W., Jan L.Y., Jan Y.N. Targeted deletion of numb and numblike in sensory neurons reveals their essential functions in axon arborization. Genes Dev. 2005, 19:138-151.
20. Huppert S.S., Le A., Schroeter E.H., Mumm J.S., Saxena M.T., Milner L.A., Kopan R. Embryonic lethality in mice homozygous for a processing-deficient allele of Notch1. Nature 2000, 405:966-970.
21. Iso T., Sartorelli V., Poizat C., Iezzi S., Wu H.Y., Chung G., Kedes L., Hamamori Y. HERP, a novel heterodimer partner of HES/E(spl) in Notch signaling. Mol. Cell. Biol. 2001, 21:6080-6089.
22. Jarriault S., Brou C., Logeat F., Schroeter E.H., Kopan R., Israel A. Signalling downstream of activated mammalian Notch. Nature 1995, 377:355-358.
23. Jarriault S., Le Bail O., Hirsinger E., Pourquie O., Logeat F., Strong C.F., Brou C., Seidah N.G., Israel A. Delta-1 activation of Notch-1 signaling results in HES-1 transactivation. Mol. Cell. Biol. 1998, 18:7423-7431.
24. Jia L., Yu G., Zhang Y., Wang M.M. Lysosome-dependent degradation of Notch3. Int. J. Biochem. Cell Biol. 2009, 41:2594-2598.
25. Johnson J., Espinoza T., McGaughey R.W., Rawls A., Wilson-Rawls J. Notch pathway genes are expressed in developing mammalian follicles. Mech. Dev. 2001, 109:355-361.
26. Kopan R., Schroeter E.H., Weintraub H., Nye J.S. Signal transduction by activated mNotch: importance of proteolytic processing and its regulation by the extracellular domain. Proc. Natl. Acad. Sci. USA 1996, 93:1683-1688.
27. Kopan R., Nye J.S., Weintraub H. The intracellular domain of mouse Notch: a constitutively activated repressor of myogenesis directed at the basic helix-loop-helix region of MyoD. Development 1994, 120:2385-2396.
28. Krebs L.T., Xue Y., Norton C.R., Sundberg J.P., Beatus P., Lendahl U., Joutel A., Gridley T. Characterization of Notch3-deficient mice: normal embryonic development and absence of genetic interactions with a Notch1 mutation. Genesis 2003, 37:139-143.
29. Kuo C.T., Mirzadeh Z., Soriano-Navarro M., Rasin M., Wang D., Shen J., Sestan N., Garcia-Verdugo J., Alvarez-Buylla A., Jan L.Y., Jan Y.-N. Postnatal deletion of Numb/Numblike reveals repair and remodeling capacity in the subventricular neurogenic niche. Cell 2006, 127:1253-1264.
30. Lammert E., Brown J., Melton D.A. Notch gene expression during pancreatic organogenesis. Mech. Dev. 2000, 94:199-203.
31. Lardelli M., Lendahl U. MotchA and MotchB - two mouse Notch homologues coexpressed in a wide variety of tissues. Exp. Cell Res. 1993, 204:364-372.
32. Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., Valentin F., Wallace I.M., Wilm A., Lopez R., Thompson J.D., Gibson T.J., Higgins D.G. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23:2947-2948.
33. Lu F.M., Lux S.E. Constitutively active human Notch1 binds to the transcription factor CBF1 and stimulates transcription through a promoter containing a CBF1-responsive element. Proc. Natl. Acad. Sci. USA 1996, 93:5663-5667.
34. + T cells. Immunity 2003, 19:549-559.
35. McCright B., Gao X., Shen L., Lozier J., Lan Y., Maguire M., Herzlinger D., Weinmaster G., Jiang R., Gridley T. Defects in development of the kidney, heart and eye vasculature in mice homozygous for a hypomorphic Notch2 mutation. Development 2001, 128:491-502.
36. McGill M.A., McGlade C.J. Mammalian Numb proteins promote Notch1 receptor ubiquitination and degradation of the Notch1 intracellular domain. J. Biol. Chem. 2003, 278:23196-23203.
37. McGill M.A., Dho S.E., Weinmaster G., McGlade C.J. Numb regulates post-endocytic trafficking and degradation of Notch1. J. Biol. Chem. 2009, 284:26427-26438.
38. Moloney D.J., Panin V.M., Johnston S.H., Chen J., Shao L., Wilson R., Wang Y., Stanley P., Irvine K.D., Haltiwanger R.S., Vogt T.F. Fringe is a glycosyltransferase that modifies Notch. Nature 2000, 406:369-375.
39. Mukhopadhyay D., Riezman H. Proteasome-independent functions of ubiquitin in endocytosis and signaling. Science 2007, 315:201-205.
40. Mumm J., Kopan R. Notch signaling: from the outside in. Dev. Biol. 2000, 228:151-165.
41. Mumm J.S., Schroeter E.H., Saxena M.T., Griesemer A., Tian X., Pan D.J., Ray W.J., Kopan R. A ligand-induced extracellular cleavage regulates γ-secretase-like proteolytic activation of Notch1. Mol. Cell 2000, 5:197-206.
42. Nye J.S., Kopan R., Axel R. An activated Notch suppresses neurogenesis and myogenesis but not gliogenesis in mammalian cells. Development 1994, 120:2421-2430.
43. Ong C.-T., Cheng H.-T., Chang L.-W., Ohtsuka T., Kageyama R., Stormo G.D., Kopan R. Target selectivity of vertebrate Notch proteins: collaboration between discrete domains and CSL-binding site architecture determine activation probability. J. Biol. Chem. 2006, 281:5106-5119.
44. Park M., Yaich L.E., Bodmer R. Mesodermal cell fate decisions in Drosophila are under the control of the lineage genes numb, Notch, and sanpodo. Mech. Dev. 1998, 75:117-126.
45. Pedersen W.A., Chan S.L., Zhu H., Abdur-Rahman L.A., Verdi J.M., Mattson M.P. Numb isoforms containing a short PTB domain promote neurotrophic factor-induced differentiation and neurotrophic factor withdrawal induced death of PC12 cells. J. Neurochem. 2002, 82:976-986.
46. Petersen P.H., Zou K., Hwang J.K., Jan Y.N., Zhong W. Progenitor cell maintenance requires numb and numblike during mouse neurogenesis. Nature 2002, 419:929-934.
47. Petersen P.H., Zou K., Krauss S., Zhong W. Continuing role for mouse Numb and Numbl in maintaining progenitor cells during cortical neurogenesis. Nat. Neurosci. 2004, 7:803-811.
48. Qiu L., Joazeiro C., Fang N., Wang H.-Y., Elly C., Altman Y., Fang D., Hunter T., Liu Y.-C. Recognition and ubiquitination of Notch by Itch, a Hect-type E3 Ubiquitin Ligase. J. Biol. Chem. 2000, 275:35734-35737.
49. Reaume A.G., Conlon R.A., Zirngibl R., Yamaguchi T.P., Rossant J. Expression analysis of a Notch homologue in the mouse embryo. Dev. Biol. 1992, 154:377-387.
50. Rhyu M.S., Jan L.Y., Jan Y.N. Asymmetric distribution of numb protein during division of the sensory organ precursor cell confers distinct fates to daughter cells. Cell 1994, 76:477-491.
51. Schroeter E.H., Kisslinger J.A., Kopan R. Notch-1 signalling requires ligand-induced proteolytic release of intracellular domain. Nature 1998, 393:382-386.
52. Shawber S.C., Nofziger D., Hsieh J.J., Lindsell C., Bögler O., Hayward D., Weinmaster G. Notch signaling inhibits muscle cell differentiation through a CBF1-independent pathway. Development 1996, 122:3765-3773.
53. Shimizu K., Chiba S., Saito T., Kumano K., Hamada Y., Hirai H. Functional diversity among Notch1, Notch2, and Notch3 receptors. Biochem. Biophys. Res. Commun. 2002, 291:775-779.
54. Swiatek P.J., Lindsell C.E., Franco Del Amo F., Weinmaster G., Gridley T. Notch1 is essential for postimplantation development in mice. Genes Dev. 1994, 8:707-719.
55. Venters S.J., Ordahl C.P. Asymmetric cell divisions are concentrated in the dermomyotome dorsomedial lip during epaxial primary myotome morphogenesis. Anat. Embryol. (Berl.) 2005, 209:449-460.
56. Verdi J.M., Bashirullah A., Goldhawk D.E., Kubu C.J., Jamali M., Meakin S.O., Lipshitz H.D. Distinct human NUMB isoforms regulate differentiation vs. proliferation in the neuronal lineage. Proc. Natl. Acad. Sci. USA 1999, 96:10472-10476.
57. Verdi J.M., Schmandt R., Bashirullah A., Jacob S., Salvino R., Craig C.G., Program A.E.S.T., Lipshitz H.D., McGlade C.J. Mammalian NUMB is an evolutionarily conserved signaling adapter protein that specifies cell fate. Curr. Biol. 1996, 6:1134-1145.
58. Wakamatsu Y., Maynard T.M., Jones S.U., Weston J.A. NUMB localizes in the basal cortex of mitotic avian neuroepithelial cells and modulates neuronal differentiation by binding to NOTCH-1. Neuron 1999, 23:71-81.
59. Williams R., Lendahl U., Lardelli M. Complementary and combinatorial patterns of Notch gene family expression during early mouse development. Mech. Dev. 1995, 53:357-368.
60. Wilson-Rawls J., Molkentin J.D., Black B.L., Olson E.N. Activated Notch inhibits myogenic activity of the MADS-box transcription factor myocyte enhancer factor 2C. Mol. Cell. Biol. 1999, 19:2853-2862.
61. Yoshida T., Tokunaga A., Nakao K., Okano H. Distinct expression patterns of splicing isoforms of mNumb in the endocrine lineage of developing pancreas. Differentiation 2003, 71:486-495.
62. Zhong W., Feder J.N., Jiang M.-M., Jan L.Y., Jan Y.N. Asymmetric localization of a mammalian Numb homolog during mouse cortical neurogenesis. Neuron 1996, 17:43-53.
63. Zhong W., Jiang M.M., Weinmaster G., Jan L.Y., Jan Y.N. Differential expression of mammalian Numb, Numblike and Notch1 suggests distinct roles during mouse cortical neurogenesis. Development 1997, 124:1887-1897.
64. Zilian O., Saner C., Hagedorn L., Lee H.-Y., Sauberli E., Suter U., Sommer L., Aguet M. Multiple roles of mouse Numb in tuning developmental cell fates. Curr. Biol. 2001, 11:494-501.