Ero1L, a thiol oxidase, is required for Notch signaling through cysteine bridge formation of the Lin12-Notch repeats in Drosophila melanogaster

Journal of Cell Biology

Volumn 182, Issue 6, 2008, Pages 1113-1125

  Tien, An Chi ^a   Rajan, Akhila ^a   Schulze, Karen L ^a   Hyung, Don Ryoo ^b,c   Acar, Melih ^a   Steller, Hermann ^c   Bellen, Hugo J ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; NOTCH RECEPTOR; PROTEIN ERO1L; PROTEIN LIN 12 NOTCH REPEAT; THIOL OXIDASE; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CELL COMMUNICATION; CELL FATE; CLONE; CONTROLLED STUDY; DISULFIDE BOND; DROSOPHILA MELANOGASTER; ENDOPLASMIC RETICULUM; ERO1L GENE; GENE; GENETIC SCREENING; MOSAICISM; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FAMILY; PROTEIN FOLDING; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM;

ANIMALS; CYSTEINE; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENDOPLASMIC RETICULUM; MORPHOGENESIS; MUTATION; OXIDOREDUCTASES ACTING ON SULFUR GROUP DONORS; PHENOTYPE; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION;

DROSOPHILA MELANOGASTER;

EID: 52249103998     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200805001     Document Type: Article

References (88)

1. Acar, M., H. Jafar-Nejad, N. Giagtzoglou, S. Yallampalli, G. David, Y. He, C. Delidakis, and H.J. Bellen. 2006. Senseless physically interacts with proneural proteins and functions as a transcriptional co-activator. Development. 133:1979-1989.
2. Acar, M., H. Jafar-Nejad, H. Takeuchi, A. Rajan, D. Ibrani, N.A. Rana, H. Pan, R.S. Haltiwanger, and H.J. Bellen. 2008. Rumi is a CAP10 domain glycosyltransferase that modifies Notch and is required for Notch signaling. Cell. 132:247-258.
3. 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.
4. Bardin, A.J., R. Le Borgne, and F. Schweisguth. 2004. Asymmetric localization and function of cell-fate determinants: a fly's view. Curr. Opin. Neurobiol. 14:6-14.
5. Benham, A.M., A. Cabibbo, A. Fassio, N. Bulleid, R. Sitia, and I. Braakman. 2000. The CXXCXXC motif determines the folding, structure and stability of human Ero1-Lalpha. EMBO J. 19:4493-4502.
6. Berdnik, D., T. Torok, M. Gonzalez-Gaitan, and J.A. Knoblich. 2002. The endocytic protein alpha-Adaptin is required for numb-mediated asymmetric cell division in Drosophila. Dev. Cell. 3:221-231.
7. Berry, L.W., B. Westlund, and T. Schedl. 1997. Germ-line tumor formation caused by activation of glp-1, a Caenorhabditis elegans member of the Notch family of receptors. Development. 124:925-936.
8. Blochlinger, K., R. Bodmer, L.Y. Jan, and Y.N. Jan. 1990. Patterns of expression of cut, a protein required for external sensory organ development in wild-type and cut mutant Drosophila embryos. Genes Dev. 4:1322-1331.
9. Boldt, H.B., K. Kjaer-Sorensen, M.T. Overgaard, K. Weyer, C.B. Poulsen, L. Sottrup-Jensen, C.A. Conover, L.C. Giudice, and C. Oxvig. 2004. The Lin12-notch repeats of pregnancy-associated plasma protein-A bind calcium and determine its proteolytic specificity. J. Biol. Chem. 279:38525-38531.
10. Brand, A.H., and N. Perrimon. 1993. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development. 118:401-415.
11. Bray, S. 1998. Notch signalling in Drosophila: three ways to use a pathway. Semin. Cell Dev. Biol. 9:591-597.
12. Bray, S.J. 2006. Notch signalling: a simple pathway becomes complex. Nat. Rev. Mol. Cell Biol. 7:678-689.
13. Brook, W.J., and S.M. Cohen. 1996. Antagonistic interactions between wingless and decapentaplegic responsible for dorsal-ventral pattern in the Drosophila Leg. Science. 273:1373-1377.
14. Cabibbo, A., M. Pagani, M. Fabbri, M. Rocchi, M.R. Farmery, N.J. Bulleid, and R. Sitia. 2000. ERO1-L, a human protein that favors disulfide bond formation in the endoplasmic reticulum. J. Biol. Chem. 275:4827-4833.
15. Calleja, M., E. Moreno, S. Pelaz, and G. Morata. 1996. Visualization of gene expression in living adult Drosophila. Science. 274:252-255.
16. Chintapalli, V.R., J. Wang, and J.A. Dow. 2007. Using FlyAtlas to identify better Drosophila melanogaster models of human disease. Nat. Genet. 39:715-720.
17. Clemens, J.C., C.A. Worby, N. Simonson-Leff, M. Muda, T. Maehama, B.A. Hemmings, and J.E. Dixon. 2000. Use of double-stranded RNA interference in Drosophila cell lines to dissect signal transduction pathways. Proc. Natl. Acad. Sci. USA. 97:6499-6503.
18. Culi, J., and R.S. Mann. 2003. Boca, an endoplasmic reticulum protein required for wingless signaling and trafficking of LDL receptor family members in Drosophila. Cell. 112:343-354.
19. de Celis, J.F., and S. Bray. 1997. Feed-back mechanisms affecting Notch activation at the dorsoventral boundary in the Drosophila wing. Development. 124:3241-3251.
20. de Celis, J.F., and A. Garcia-Bellido. 1994. Modifications of the notch function by Abruptex mutations in Drosophila melanogaster. Genetics. 136:183-194.
21. de Celis, J.F., A. Garcia-Bellido, and S.J. Bray. 1996. Activation and function of Notch at the dorsal-ventral boundary of the wing imaginal disc. Development. 122:359-369.
22. De Strooper, B., W. Annaert, P. Cupers, P. Saftig, K. Craessaerts, J.S. Mumm, E.H. Schroeter, V. Schrijvers, M.S. Wolfe, W.J. Ray, et al. 1999. A presenilin-1-dependent gamma-secretase-like protease mediates release of Notch intracellular domain. Nature. 398:518-522.
23. Diederich, R.J., K. Matsuno, H. Hing, and S. Artavanis-Tsakonas. 1994. Cytosolic interaction between deltex and Notch ankyrin repeats implicates deltex in the Notch signaling pathway. Development. 120:473-481.
24. Dietzl, G., D. Chen, F. Schnorrer, K.C. Su, Y. Barinova, M. Fellner, B. Gasser, K. Kinsey, S. Oppel, S. Scheiblauer, et al. 2007. A genome-wide transgenic RNAi library for conditional gene inactivation in Drosophila. Nature. 448:151-156.
25. Downing, A.K., V. Knott, J.M. Werner, C.M. Cardy, I.D. Campbell, and P.A. Handford. 1996. Solution structure of a pair of calcium-binding epidermal growth factor-like domains: implications for the Marfan syndrome and other genetic disorders. Cell. 85:597-605.
26. Elefant, F., and K.B. Palter. 1999. Tissue-specific expression of dominant negative mutant Drosophila HSC70 causes developmental defects and lethality. Mol. Biol. Cell. 10:2101-2117.
27. Ellgaard, L., and L.W. Ruddock. 2005. The human protein disulphide isomerase family: substrate interactions and functional properties. EMBO Rep. 6:28-32.
28. Fehon, R.G., P.J. Kooh, I. Rebay, C.L. Regan, T. Xu, M.A. Muskavitch, and S. Artavanis-Tsakonas. 1990. Molecular interactions between the protein products of the neurogenic loci Notch and Delta, two EGF-homologous genes in Drosophila. Cell. 61:523-534.
29. Frand, A.R., and C.A. Kaiser. 1998. The ERO1 gene of yeast is required for oxidation of protein dithiols in the endoplasmic reticulum. Mol. Cell. 1:161-170.
30. Frand, A.R., and C.A. Kaiser. 1999. Ero1p oxidizes protein disulfide isomerase in a pathway for disulfide bond formation in the endoplasmic reticulum. Mol. Cell. 4:469-477.
31. Freedman, R.B. 1989. Protein disulfide isomerase: multiple roles in the modification of nascent secretory proteins. Cell. 57:1069-1072.
32. Gallagher, C.M., and J.A. Knoblich. 2006. The conserved c2 domain protein lethal (2) giant discs regulates protein trafficking in Drosophila. Dev. Cell. 11:641-653.
33. Gho, M., Y. Bellaiche, and F. Schweisguth. 1999. Revisiting the Drosophila microchaete lineage: a novel intrinsically asymmetric cell division generates a glial cell. Development. 126:3573-3584.
34. Ghysen, A., C. Dambly-Chaudiere, L.Y. Jan, and Y.N. Jan. 1993. Cell interactions and gene interactions in peripheral neurogenesis. Genes Dev. 7:723-733.
35. Gordon, W.R., D. Vardar-Ulu, G. Histen, C. Sanchez-Irizarry, J.C. Aster, and S.C. Blacklow. 2007. Structural basis for autoinhibition of Notch. Nat. Struct. Mol. Biol. 14:295-300.
36. Greenwald, I., and G. Seydoux. 1990. Analysis of gain-of-function mutations of the lin-12 gene of Caenorhabditis elegans. Nature. 346:197-199.
37. Gross, E., D.B. Kastner, C.A. Kaiser, and D. Fass. 2004. Structure of Ero1p, source of disulfide bonds for oxidative protein folding in the cell. Cell. 117:601-610.
38. Haines, N., and K.D. Irvine. 2003. Glycosylation regulates Notch signalling. Nat. Rev. Mol. Cell Biol. 4:786-797.
39. Hambleton, S., N.V. Valeyev, A. Muranyi, V. Knott, J.M. Werner, A.J. McMichael, P.A. Handford, and A.K. Downing. 2004. Structural and functional properties of the human notch-1 ligand binding region. Structure. 12:2173-2183.
40. Harrison, S.D., N. Solomon, and G.M. Rubin. 1995. A genetic analysis of the 63E-64A genomic region of Drosophila melanogaster: identification of mutations in a replication factor C subunit. Genetics. 139:1701-1709.
41. Hartenstein, V., and J.W. Posakony. 1990. A dual function of the Notch gene in Drosophila sensillum development. Dev. Biol. 142:13-30.
42. Hoober, K.L., N.M. Glynn, J. Burnside, D.L. Coppock, and C. Thorpe. 1999a. Homology between egg white sulfhydryl oxidase and quiescin Q6 defines a new class of flavin-linked sulfhydryl oxidases. J. Biol. Chem. 274:31759-31762.
43. Hoober, K.L., S.L. Sheasley, H.F. Gilbert, and C. Thorpe. 1999b. Sulfhydryl oxidase from egg white. A facile catalyst for disulfide bond formation in proteins and peptides. J. Biol. Chem. 274:22147-22150.
44. Jafar-Nejad, H., H.K. Andrews, M. Acar, V. Bayat, F. Wirtz-Peitz, S.Q. Mehta, J.A. Knoblich, and H.J. Bellen. 2005. Sec15, a component of the exocyst, promotes notch signaling during the asymmetric division of Drosophila sensory organ precursors. Dev. Cell. 9:351-363.
45. Jafar-Nejad, H., A.C. Tien, M. Acar, and H.J. Bellen. 2006. Senseless and Daughterless confer neuronal identity to epithelial cells in the Drosophila wing margin. Development. 133:1683-1692.
46. Jan, Y.N., and L.Y. Jan. 1993. HLH proteins, fly neurogenesis, and vertebrate myogenesis. Cell. 75:827-830.
47. Jessop, C.E., S. Chakravarthi, N. Garbi, G.J. Hammerling, S. Lovell, and N.J. Bulleid. 2007. ERp57 is essential for efficient folding of glycoproteins sharing common structural domains. EMBO J. 26:28-40.
48. Kidd, S., and T. Lieber. 2002. Furin cleavage is not a requirement for Drosophila Notch function. Mech. Dev. 115:41-51.
49. Kobayashi, T., S. Kishigami, M. Sone, H. Inokuchi, T. Mogi, and K. Ito. 1997. Respiratory chain is required to maintain oxidized states of the DsbA-DsbB disulfide bond formation system in aerobically growing Escherichia coli cells. Proc. Natl. Acad. Sci. USA. 94:11857-11862.
50. Kuhnlein, R.P., G. Frommer, M. Friedrich, M. Gonzalez-Gaitan, A. Weber, J.F. Wagner-Bernholz, W.J. Gehring, H. Jackle, and R. Schuh. 1994. spalt encodes an evolutionarily conserved zinc finger protein of novel structure which provides homeotic gene function in the head and tail region of the Drosophila embryo. EMBO J. 13:168-179.
51. Lai, E.C. 2004. Notch signaling: control of cell communication and cell fate. Development. 131:965-973.
52. Lee, T., and L. Luo. 2001. Mosaic analysis with a repressible cell marker (MARCM) for Drosophila neural development. Trends Neurosci. 24:251-254.
53. Lesokhin, A.M., S.Y. Yu, J. Katz, and N.E. Baker. 1999. Several levels of EGF receptor signaling during photoreceptor specification in wild-type, Ellipse, and null mutant Drosophila. Dev. Biol. 205:129-144.
54. Lieber, T., S. Kidd, E. Alcamo, V. Corbin, and M.W. Young. 1993. Antineurogenic phenotypes induced by truncated Notch proteins indicate a role in signal transduction and may point to a novel function for Notch in nuclei. Genes Dev. 7:1949-1965.
55. Lieber, T., S. Kidd, and M.W. Young. 2002. kuzbanian-mediated cleavage of Drosophila Notch. Genes Dev. 16:209-221.
56. Lopez-Schier, H., and D. St Johnston. 2001. Delta signaling from the germ line controls the proliferation and differentiation of the somatic follicle cells during Drosophila oogenesis. Genes Dev. 15:1393-1405.
57. Maattanen, P., G. Kozlov, K. Gehring, and D.Y. Thomas. 2006. ERp57 and PDI: multifunctional protein disulfide isomerases with similar domain architectures but differing substrate-partner associations. Biochem. Cell Biol. 84:881-889.
58. Modolell, J. 1997. Patterning of the adult peripheral nervous system of Drosophila. Perspect. Dev. Neurobiol. 4:285-296.
59. Motzny, C.K., and R. Holmgren. 1995. The Drosophila cubitus interruptus protein and its role in the wingless and hedgehog signal transduction pathways. Mech. Dev. 52:137-150.
60. Nakao, A., E. Roijer, T. Imamura, S. Souchelnytskyi, G. Stenman, C.H. Heldin, and P. ten Dijke. 1997. Identification of Smad2, a human Mad-related protein in the transforming growth factor beta signaling pathway. J. Biol. Chem. 272:2896-2900.
61. Newsome, T.P., B. Asling, and B.J. Dickson. 2000. Analysis of Drosophila photoreceptor axon guidance in eye-specific mosaics. Development. 127:851-860.
62. Nolo, R., L.A. Abbott, and H.J. Bellen. 2000. Senseless, a Zn finger transcription factor, is necessary and sufficient for sensory organ development in Drosophila. Cell. 102:349-362.
63. Okajima, T., A. Xu, L. Lei, and K.D. Irvine. 2005. Chaperone activity of protein O-fucosyltransferase 1 promotes notch receptor folding. Science. 307:1599-1603.
64. Okochi, M., H. Steiner, A. Fukumori, H. Tanii, T. Tomita, T. Tanaka, T. Iwatsubo, T. Kudo, M. Takeda, and C. Haass. 2002. Presenilins mediate a dual intramembranous gamma-secretase cleavage of Notch-1. EMBO J. 21:5408-5416.
65. Pagani, M., M. Fabbri, C. Benedetti, A. Fassio, S. Pilati, N.J. Bulleid, A. Cabibbo, and R. Sitia. 2000. Endoplasmic reticulum oxidoreductin 1-lbeta (ERO1-Lbeta), a human gene induced in the course of the unfolded protein response. J. Biol. Chem. 275:23685-23692.
66. Pollard, M.G., K.J. Travers, and J.S. Weissman. 1998. Ero1p: a novel and ubiquitous protein with an essential role in oxidative protein folding in the endoplasmic reticulum. Mol. Cell. 1:171-182.
67. Robinow, S., and K. White. 1991. Characterization and spatial distribution of the ELAV protein during Drosophila melanogaster development. J. Neurobiol. 22:443-461.
68. Rubin, G.M., L. Hong, P. Brokstein, M. Evans-Holm, E. Frise, M. Stapleton, and D.A. Harvey. 2000. A Drosophila complementary DNA resource. Science. 287:2222-2224.
69. Ryoo, H.D., P.M. Domingos, M.J. Kang, and H. Steller. 2007. Unfolded protein response in a Drosophila model for retinal degeneration. EMBO J. 26:242-252.
70. Sanchez-Irizarry, C., A.C. Carpenter, A.P. Weng, W.S. Pear, J.C. Aster, and S.C. Blacklow. 2004. Notch subunit heterodimerization and prevention of ligand-independent proteolytic activation depend, respectively, on a novel domain and the LNR repeats. Mol. Cell. Biol. 24:9265-9273.
71. Schroder, M., and R.J. Kaufman. 2005. ER stress and the unfolded protein response. Mutat. Res. 569:29-63.
72. Schuster, C.M., G.W. Davis, R.D. Fetter, and C.S. Goodman. 1996. Genetic dissection of structural and functional components of synaptic plasticity. I. Fasciclin II controls synaptic stabilization and growth. Neuron. 17:641-654.
73. Schweisguth, F. 2004. Regulation of notch signaling activity. Curr. Biol. 14:R129-R138.
74. Sevier, C.S., and C.A. Kaiser. 2006. Conservation and diversity of the cellular disulfide bond formation pathways. Antioxid. Redox Signal. 8:797-811.
75. Stowers, R.S., and T.L. Schwarz. 1999. A genetic method for generating Drosophila eyes composed exclusively of mitotic clones of a single genotype. Genetics. 152:1631-1639.
76. Struhl, G., and I. Greenwald. 1999. Presenilin is required for activity and nuclear access of Notch in Drosophila. Nature. 398:522-525.
77. Tanimoto, H., S. Itoh, P. ten Dijke, and T. Tabata. 2000. Hedgehog creates a gradient of DPP activity in Drosophila wing imaginal discs. Mol. Cell. 5:59-71.
78. Tepass, U., and E. Knust. 1993. Crumbs and stardust act in a genetic pathway that controls the organization of epithelia in Drosophila melanogaster. Dev. Biol. 159:311-326.
79. Thorpe, C., and D.L. Coppock. 2007. Generating disulfides in multicellular organisms: emerging roles for a new flavoprotein family. J. Biol. Chem. 282:13929-13933.
80. Travers, K.J., C.K. Patil, L. Wodicka, D.J. Lockhart, J.S. Weissman, and P. Walter. 2000. Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell. 101:249-258.
81. Tu, B.P., S.C. Ho-Schleyer, K.J. Travers, and J.S. Weissman. 2000. Biochemical basis of oxidative protein folding in the endoplasmic reticulum. Science. 290:1571-1574.
82. Vardar, D., C.L. North, C. Sanchez-Irizarry, J.C. Aster, and S.C. Blacklow. 2003. Nuclear magnetic resonance structure of a prototype Lin12-Notch repeat module from human Notch1. Biochemistry. 42:7061-7067.
83. Wang, Q.T., and R.A. Holmgren. 1999. The subcellular localization and activity of Drosophila cubitus interruptus are regulated at multiple levels. Development. 126:5097-5106.
84. Wang, W., and G. Struhl. 2004. Drosophila Epsin mediates a select endocytic pathway that DSL ligands must enter to activate Notch. Development. 131:5367-5380.
85. Weng, A.P., A.A. Ferrando, W. Lee, J.P. Morris IV, L.B. Silverman, C. Sanchez-Irizarry, S.C. Blacklow, A.T. Look, and J.C. Aster. 2004. Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia. Science. 306:269-271.
86. Williams, J.A., J.B. Bell, and S.B. Carroll. 1991. Control of Drosophila wing and haltere development by the nuclear vestigial gene product. Genes Dev. 5:2481-2495.
87. Xu, T., L.A. Caron, R.G. Fehon, and S. Artavanis-Tsakonas. 1992. The involvement of the Notch locus in Drosophila oogenesis. Development. 115:913-922.
88. Zhai, R.G., P.R. Hiesinger, T.W. Koh, P. Verstreken, K.L. Schulze, Y. Cao, H. Jafar-Nejad, K.K. Norga, H. Pan, V. Bayat, et al. 2003. Mapping Drosophila mutations with molecularly defined P element insertions. Proc. Natl. Acad. Sci. USA. 100:10860-10865.