Caenorhabditis elegans num-1 negatively regulates endocytic recycling

Genetics

Volumn 179, Issue 1, 2008, Pages 375-387

  Nilsson, Lars ^a   Conradt, Barbara ^b   Ruaud, Anne Francxoise ^c,d   Chen, Carlos Chih Hsiung ^e   Hatzold, Julia ^b   Bessereau, Jean Louis ^c,d   Grant, Barth D ^e   Tuck, Simon ^a  

^a UMEÅ UNIVERSITY   (Sweden)

^b DARTMOUTH MEDICAL SCHOOL   (United States)

^c ECOLE NORMALE SUPÉRIEURE   (France)

^d INSERM   (France)

^e RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; HELMINTH PROTEIN; HYBRID PROTEIN; PROTEIN NUM 1A; PROTEIN RAB 10; PROTEIN RME 1; UNCLASSIFIED DRUG; CAENORHABDITIS ELEGANS PROTEIN; NUM 1 PROTEIN, C ELEGANS; NUM-1 PROTEIN, C ELEGANS; PRIMER DNA; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ARTICLE; BASOLATERAL MEMBRANE; CAENORHABDITIS ELEGANS; CELL STRUCTURE; CELL SURFACE; CELL VACUOLE; CONTROLLED STUDY; ENDOCYTOSIS; EPITHELIUM CELL; GENE FUNCTION; GENE LOCUS; GENE MUTATION; GENETIC EPISTASIS; INTESTINE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SEQUENCE HOMOLOGY; SUBCUTANEOUS TISSUE; ANIMAL; COMPARATIVE STUDY; GENETICS; INTESTINE MUCOSA; METABOLISM; PHYSIOLOGY; TRANSMISSION ELECTRON MICROSCOPY; TRANSPORT VESICLE; ULTRASTRUCTURE;

CAENORHABDITIS ELEGANS; MAMMALIA;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; DNA PRIMERS; ENDOCYTOSIS; GREEN FLUORESCENT PROTEINS; INTESTINAL MUCOSA; MICROSCOPY, ELECTRON, TRANSMISSION; TRANSPORT VESICLES;

EID: 52049099207     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.108.087247     Document Type: Article

References (54)

1. APODACA, G., C. ENRICH and K. E. MOSTOV, 1994 The calmodulin antagonist, W-13, alters transcytosis, recycling, and the morphology of the endocytic pathway in Madin-Darby canine kidney cells. J. Biol. Chem. 269: 19005-19013.
2. BALKLAVA, Z., S. PANT, H. FARES and B. D. GRANT, 2007 Genome-wide analysis identifies a general requirement for polarity proteins in endocytic traffic. Nat. Cell Biol. 9: 1066-1073.
3. BERDNIK, D., T. TOROK, M. GONZALEZ- GAITAN and J. A. KNOBLICH, 2002 The endocytic protein α-Adaptin is required for numb-mediated asymmetric cell division in Drosophila. Dev. Cell 3: 221-231.
4. BRENNER, S., 1974 The genetics of Caenorhabditis elegans. Genetics 77: 71-94.
5. BRODSKY, F. M., C. Y. CHEN, C. KNUEHL, M. C. TOWLER and D. E. WAKEHAM, 2001 Biological basket weaving: formation and function of clathrin-coated vesicles. Annu. Rev. Cell Dev. Biol. 17: 517-568.
6. CAPLAN, S., N. NASLAVSKY, L. M. HARTNELL, R. LODGE, R. S. POLISHCHUK et al., 2002 A tubular EHD1-containing compartment involved in the recycling of major histocompatibility complex class I molecules to the plasma membrane. EMBO J. 21: 2557-2567.
7. CHEN, C. C., P. J. SCHWEINSBERG, S. VASHIST, D. P. MAREINISS, E. J. LAMBIE et al., 2006 RAB-10 is required for endocytic recycling in the Caenorhabditis elegans intestine. Mol. Biol. Cell 17: 1286-1297.
8. EDGLEY, M., A. D'SOUZA, G. MOULDER, S. MCKAY, B. SHEN et al., 2002 Improved detection of small deletions in complex pools of DNA. Nucleic Acids Res. 30: e52.
9. FARES, H., and I. GREENWALD, 2001a Genetic analysis of endocytosis in Caenorhabditis elegans: coelomocyte uptake defective mutants. Genetics 159: 133-145.
10. FARES, H., and I. GREENWALD, 2001b Regulation of endocytosis by CUP-5, the Caenorhabditis elegans mucolipin-1 homolog. Nat. Genet. 28: 64-68.
11. GRANT, B., and D. HIRSH, 1999 Receptor-mediated endocytosis in the Caenorhabditis elegans oocyte. Mol. Biol. Cell 10: 4311-4326.
12. GRANT, B., Y. ZHANG, M. C. PAUPARD, S. X. LIN, D. H. HALL et al., 2001 Evidence that RME-1, a conserved C. elegans EH-domain protein, functions in endocytic recycling. Nat. Cell Biol. 3: 573-579.
13. GREENWALD, I., 2005 LIN-12/Notch signaling in C. elegans (August 4, 2005), in WormBook, edited by THE C. ELEGANS RESEARCH COMMUNITY. WormBook, http://www.wormbook.org.
14. 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.
15. HAO, M., and F. R. MAXFIELD, 2000 Characterization of rapid membrane internalization and recycling. J. Biol. Chem. 275: 15279-15286.
16. HARTENSTEIN, V., and J. W. POSAKONY, 1990 A dual function of the Notch gene in Drosophila sensillum development. Dev. Biol. 142: 13-30.
17. HERMANN, G. J., L. K. SCHROEDER, C. A. HIEB, A. M. KERSHNER, B. M. RABBITTS et al., 2005 Genetic analysis of lysosomal trafficking in Caenorhabditis elegans. Mol. Biol. Cell 16: 3273-3288.
18. HOPKINS, C. R., 1983 Intracellular routing of transferrin and transferrin receptors in epidermoid carcinoma A431 cells. Cell 35: 321-330.
19. HUANG, E. J., H. LI, A. A. TANG, A. K. WIGGINS, R. L. NEVE et al., 2005 Targeted deletion of numb and numblike in sensory neurons reveals their essential functions in axon arborization. Genes Dev. 19: 138-151.
20. HURD, D. D., and K. J. KEMPHUES, 2003 PAR-1 is required for morphogenesis of the Caenorhabditis elegans vulva. Dev. Biol. 253: 54-65.
21. HUTTERER, A., and J. A. KNOBLICH, 2005 Numb and α-Adaptin regulate Sanpodo endocytosis to specify cell fate in Drosophila external sensory organs. EMBO Rep. 6: 836-842.
22. JAN, Y. N., and L. Y. JAN, 1998 Asymmetric cell division. Nature 392: 775-778.
23. KOSTICH, M., A. FIRE and D. M. FAMBROUGH, 2000 Identification and molecular-genetic characterization of a LAMP/CD68-like protein from Caenorhabditis elegans. J. Cell Sci. 113(Pt. 14): 2595-2606.
24. KRAUSE, M., and D. HIRSH, 1987 A trans-spliced leader sequence on actin mRNA in C. elegans. Cell 49: 753-761.
25. LE BORGNE, R., 2006 Regulation of Notch signalling by endocytosis and endosomal sorting. Curr. Opin. Cell Biol. 18: 213-222.
26. LEUNG, B., G. J. HERMANN and J. R. PRIESS, 1999 Organogenesis of the Caenorhabditis elegans intestine. Dev. Biol. 216: 114-134.
27. LIEGEOIS, S., A. BENEDETTO, J. M. GARNIER, Y. SCHWAB and M. LABOUESSE, 2006 The V0-ATPase mediates apical secretion of exosomes containing Hedgehog-related proteins in Caenorhabditis elegans. J. Cell Biol. 173: 949-961.
28. LIN, S. X., B. GRANT, D. HIRSH and F. R. MAXFIELD, 2001 Rme-1 regulates the distribution and function of the endocytic recycling compartment in mammalian cells. Nat. Cell Biol. 3: 567-572.
29. MADURO, M., and D. PILGRIM, 1996 Conservation of function and expression of unc-119 from two Caenorhabditis species despite divergence of non-coding DNA. Gene 183: 77-85.
30. MAXFIELD, F. R., and T. E. MCGRAW, 2004 Endocytic recycling. Nat. Rev. Mol. Cell Biol. 5: 121-132.
31. MCMAHON, L., R. LEGOUIS, J. L. VONESCH and M. LABOUESSE, 2001 Assembly of C. elegans apical junctions involves positioning and compaction by LET-413 and protein aggregation by the MAGUK protein DLG-1. J. Cell Sci. 114: 2265-2277.
32. NISHIMURA, T., and K. KAIBUCHI, 2007 Numb controls integrin endocytosis for directional cell migration with aPKC and PAR-3. Dev. Cell 13: 15-28.
33. O'CONNOR-GILES, K. M., and J. B. SKEATH, 2003 Numb inhibits membrane localization of Sanpodo, a four-pass transmembrane protein, to promote asymmetric divisions in Drosophila. Dev. Cell 5: 231-243.
34. POLO, S., and P. P. DI FIORE, 2006 Endocytosis conducts the cell signaling orchestra. Cell 124: 897-900.
35. POSAKONY, J. W., 1994 Nature versus nurture: asymmetric cell divisions in Drosophila bristle development. Cell 76: 415-418.
36. ROUDIER, N., C. LEFEBVRE and R. LEGOUIS, 2005 CeVPS-27 is an endosomal protein required for the molting and the endocytic trafficking of the low-density lipoprotein receptor-related protein 1 in Caenorhabditis elegans. Traffic 6: 695-705.
37. SALCINI, A. E., S. CONFALONIERI, M. DORIA, E. SANTOLINI, E. TASSI et al., 1997 Binding specificity and in vivo targets of the EH domain, a novel protein-protein interaction module. Genes Dev. 11: 2239-2249.
38. SANTOLINI, E., C. PURI, A. E. SALCINI, M. C. GAGLIANI, P. G. PELICCI et al., 2000 Numb is an endocytic protein. J. Cell Biol. 151: 1345-1352.
39. SATO, M., K. SATO, P. FONAREV, C. J. HUANG, W. LIOU et al., 2005 Caenorhabditis elegans RME-6 is a novel regulator of RAB-5 at the clathrin-coated pit. Nat. Cell Biol. 7: 559-569.
40. SIMMER, F., M. TIJSTERMAN, S. PARRISH, S. P. KOUSHIKA, M. L. NONET et al., 2002 Loss of the putative RNA-directed RNA polymerase RRF-3 makes C. elegans hypersensitive to RNAi. Curr. Biol. 12: 1317-1319.
41. SMITH, C. A., S. E. DHO, J. DONALDSON, U. TEPASSAND C. J. MCGLADE, 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.
42. SPANA, E. P., and C. Q. DOE, 1996 Numb antagonizes Notch signaling to specify sibling neuron cell fates. Neuron 17: 21-26.
43. TANG, H., S. B. ROMPANI, J. B. ATKINS, Y. ZHOU, T. OSTERWALDER et al., 2005 Numb proteins specify asymmetric cell fates via an endocytosis-and proteasome-independent pathway. Mol. Cell. Biol. 25: 2899-2909.
44. TREUSCH, S., S. KNUTH, S. A. SLAUGENHAUPT, E. GOLDIN, B. D. GRANT et al., 2004 Caenorhabditis elegans functional orthologue of human protein h-mucolipin-1 is required for lysosome biogenesis. Proc. Natl. Acad. Sci. USA 101: 4483-4488.
45. UHLIK, M. T., B. TEMPLE, S. BENCHARIT, A. J. KIMPLE, D. P. SIDEROVSKI et al., 2005 Structural and evolutionary division of phosphotyrosine binding (PTB) domains. J. Mol. Biol. 345: 1-20.
46. VAN WEERT, A. W., H. J. GEUZE, B. GROOTHUIS and W. STOORVOGEL, 2000 Primaquine interferes with membrane recycling from endosomes to the plasma membrane through a direct interaction with endosomes which does not involve neutralisation of endosomal pH nor osmotic swelling of endosomes. Eur. J. Cell Biol. 79: 394-399.
47. WANG, E., P. S. BROWN, B. AROETI, S. J. CHAPIN, K. E. MOSTOV et al., 2000 Apical and basolateral endocytic pathways of MDCK cells meet in acidic common endosomes distinct from a nearly-neutral apical recycling endosome. Traffic 1: 480-493.
48. WEIMER, R. M., 2006 Preservation of C. elegans tissue via high-pressure freezing and freeze-substitution for ultrastructural analysis and immunocytochemistry. Methods Mol. Biol. 351: 203-221.
49. WISSLER, F., and M. LABOUESSE, 2007 PARtners for endocytosis. Nat. Cell Biol. 9: 1027-1029.
50. WU, L. G., 2004 Kinetic regulation of vesicle endocytosis at synapses. Trends Neurosci. 27: 548-554.
51. YAMASHIRO, D. J., B. TYCKO, S. R. FLUSS and F. R. MAXFIELD, 1984 Segregation of transferrin to a mildly acidic (pH 6.5) para-Golgi compartment in the recycling pathway. Cell 37: 789-800.
52. ZHANG, L., S. L. WU and C. S. RUBIN, 2001a A novel adapter protein employs a phosphotyrosine binding domain and exceptionally basic N-terminal domains to capture and localize an atypical protein kinase C: characterization of Caenorhabditis elegans C kinase adapter 1, a protein that avidly binds protein kinase C3. J. Biol. Chem. 276: 10463-10475.
53. ZHANG, L., S. L. WU and C. S. RUBIN, 2001b Structural properties and mechanisms that govern association of C kinase adapter 1 with protein kinase C3 and the cell periphery. J. Biol. Chem. 276: 10476-10484.
54. ZHANG, Y., B. GRANT and D. HIRSH, 2001 RME-8, a conserved J-domain protein, is required for endocytosis in Caenorhabditis elegans. Mol. Biol. Cell 12: 2011-2021.