Receptor-mediated endocytosis in the Caenorhabditis elegans oocyte

Molecular Biology of the Cell

Volumn 10, Issue 12, 1999, Pages 4311-4326

  Grant, Barth ^a   Hirsh, David ^a  

^a Dept Biochem and Molec Biophys ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; LOW DENSITY LIPOPROTEIN RECEPTOR; RNA; VITELLOGENIN;

ARTICLE; CAENORHABDITIS ELEGANS; EGG YOLK; ENDOCYTOSIS; GENETIC CONSERVATION; NONHUMAN; OOCYTE; PRIORITY JOURNAL; REPORTER GENE; SEQUENCE HOMOLOGY; TRANSGENIC ANIMAL;

ANIMALIA; CAENORHABDITIS ELEGANS; VERTEBRATA;

EID: 0032734242     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.10.12.4311     Document Type: Article

References (77)

1. Baker, M.E. (1988). Is vitellogenin an ancestor of apolipoprotein B-100 of human low-density lipoprotein and human lipoprotein lipase. Biochem. J. 255, 1057-1060.
2. Bettinger, J.C., Lee, K., and Rougvie, A.E. (1996). Stage-specific accumulation of the terminal differentiation factor LIN-29 during Caenorhabditis elegans development. Development 122, 2517-2527.
3. Bossinger, O., and Schierenberg, E. (1992). Cell-cell communication in the embryo of Caenorhabditis elegans. Dev. Biol. 151, 401-409.
4. Bossinger, O., and Schierenberg, E. (1996). The use of fluorescent marker dyes for studying intercellular communication in nematode embryos. Int. J. Dev. Biol. 40, 431-439.
5. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
6. Bucci, C., Parton, R.G., Mather, I.H., Stunnenberg, H., Simons, K., Hoflack, B., and Zerial, M. (1992). The small GTPase rab5 functions as a regulatory factor in the early endocytic pathway. Cell 70, 715-728.
7. Chalfie, M., Tu, Y., Euskirchen, G., Ward, W.W., and Prasher, D.C. (1994). Green fluorescent protein as a marker for gene expression. Science 263, 802-804.
8. 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.
9. Clandinin, T.R., DeModena, J.A., and Sternberg, P.W. (1998). Inositol trisphosphate mediates a RAS-independent response to LET-23 receptor tyrosine kinase activation in C. elegans. Cell 92, 523-533.
10. Clark, S.G., Shurland, D.L., Meyerowitz, E.M., Bargmann, C.I., and van der Bliek, A.M. (1997). A dynamin GTPase mutation causes a rapid and reversible temperature-inducible locomotion defect in C. elegans. Proc. Natl. Acad. Sci. USA 94, 10438-10443.
11. Czekay, R.P., Orlando, R.A., Woodward, L., Lundstrom, M., and Farquhar, M.G. (1997). Endocytic trafficking of megalin/RAP complexes: dissociation of the complexes in late endosomes. Mol. Biol. Cell 8, 517-532.
12. Daro, E., Sheff, D., Gomez, M., Kreis, T., and Mellman, I. (1997). Inhibition of endosome function in CHO cells bearing a temperature-sensitive defect in the coatomer (COPI) component epsilon-COP. J. Cell Biol. 239, 1747-1759.
13. de Camilli, P., Takei, K., and McPherson, P.S. (1995). The function of dynamin in endocytosis. Curr. Opin. Neurobiol. 5, 559-565.
14. De Stasio, E., Lephoto, C., Azuma, L., Holst, C., Stanislaus, D., and Uttam, J. (1997). Characterization of revertants of unc-93(e1500) in Caenorhabditis elegans induced by N-ethyl-N-nitrosourea. Genetics 147, 597-608.
15. Dell'Angelica, E.C., Shotelersuk, V., Aguilar, R.C., Gahl, W.A., and Bonifacino, J.S. (1999). Altered trafficking of lysosomal proteins in Hermansky-Pudlak syndrome due to mutations in the beta 3A subunit of the AP-3 adaptor. Mol. Cell 3, 11-21.
16. Doniach, T., and Hodgkin, J. (1984). A sex determining gene, fem-1, required for both male and hermaphrodite development in Caenorhabditis elegans. Dev. Biol. 106, 223-235.
17. Esser, V., Limbird, L.E., Brown, M.S., Goldstein, J.L., and Russell, D.W. (1988). Mutational analysis of the ligand binding domain of the low density lipoprotein receptor. J. Biol. Chem. 263, 13282-13290.
18. Feig, L.A. (1999). Tools of the trade: use of dominant-inhibitory mutants of Ras-family GTPases. Nat. Cell Biol. 1, E25-E27.
19. Feng, Y., Press, B., and Wandinger-Ness, A. (1995). Rab 7: an important regulator of late endocytic membrane traffic. J. Cell Biol. 131, 1435-1452.
20. Ferguson, E.L., and Horvitz, H.R. (1985). Identification and characterization of 22 genes that affect the vulval cell lineages of the nematode Caenorhabditis elegans. Genetics 110, 17-72.
21. Fire, A. (1986). Integrative transformation of Caenorhabditis elegans. EMBO J. 5, 2673-2680.
22. Fire, A., Xu, S., Montgomery, M.K., Kostas, S.A., Driver, S.E., and Mello, C.C. (1998). Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391, 806-811.
23. Gafvels, M.E., Caird, M., Britt, D., Jackson, C.L., Patterson, D., and Strauss, J.F.d. (1993). Cloning of a cDNA encoding a putative human very low density lipoprotein/apolipoprotein E receptor and assignment of the gene to chromosome 9pter-p23. Somat. Cell Mol. Genet. 29, 557-569.
24. Gaynor, E.C., Graham, T.R., and Emr, S.D. (1998). COPI in ER/Golgi and intraGolgi transport: do yeast COPI mutants point the way? Biochim. Biophys. Acta 1404, 33-51.
25. Goldstein, J.L., Brown, M.S., Anderson, R.G., Russell, D.W., and Schneider, W.J. (1985). Receptor-mediated endocytosis: concepts emerging from the LDL receptor system. Annu. Rev. Cell Biol. 1, 1-39.
26. Grant, B., and Greenwald, I. (1997). Structure, function, and expression of SEL-1, a negative regulator of LIN-12 and GLP-1 in C. elegans. Development 124, 637-644.
27. Gu, J., Stephenson, C.G., and Iadarola, M.J. (1994). Recombinant proteins attached to a nickel-NTA column: use in affinity purification of antibodies. Biotechniques 17, 257-262.
28. Hall, D.H., Winfrey, V.P., Blaeuer, G., Hoffman, L.H., Furuta, T., Rose, K.L., Hobert, O., and Greenstein, D. (1999). Ultrastructural features of the adult hermaphrodite gonad of Caenorhabditis elegans: relations between the germ line and soma. Dev. Biol. 212, 101-123.
29. Herz, J., Hamann, U., Rogne, S., Myklebost, D., Gausepohl, H., and Stanley, K.K. (1988). Surface localization and high affinity for calcium for a 500-kd liver membrane protein closely related to the LDL-receptor suggest a physiological role as lipoprotein receptor. EMBO J. 7, 4119-4127.
30. Horiuchi, H., et al. (1997). A novel rab5 GDP/GTP exchange factor complexed to rabaptin-5 links nucleotide exchange to effector recruitment and function. Cell 90, 1149-1159.
31. Iwasaki, K., McCarter, J., Francis, R., and Schedl, T. (1996). emo-1, a Caenorhabditis elegans Sec61p gamma homologue, is required for oocyte development and ovulation. J. Cell Biol. 134, 699-714.
32. Jones, A.R., Francis, R., and Schedl, T. (1996). GLD-1, a cytoplasmic protein essential for oocyte differentiation, shows stage-and sex-specific expression during Caenorhabditis elegans germline development. Dev. Biol. 180, 165-183.
33. Jorgensen, E.M., Hartwieg, E., Schuske, K., Nonet, M.L., Jin, Y., and Horvitz, H.R. (1995). Defective recycling of synaptic vesicles in synaptotagmin mutants of Caenorhabditis elegans. Nature 378, 196-199.
34. Kimble, J., and Sharrock, W.J. (1983). Tissue-specific synthesis of yolk proteins in C. elegans. Dev. Biol. 96, 189-196.
35. Kramer, J.M., and Johnson, J.J. (1993). Analysis of mutations in the sqt-1 and rol-6 collagen gene of Caenorhabditis elegans. Genetics 135, 1035-1045.
36. Lee, J., Jongeward, G.D., and Sternberg, P.W. (1994). unc-101, a gene required for many aspects of Caenorhabditis elegans development and behavior, encodes a clathrin-associated protein. Genes & Dev. 8, 60-73.
37. Levy, A.D., Yang, J., and Kramer, J.M. (1993). Molecular genetic analysis of the Caenorhabditis elegans dpy-2 and dpy-10 collagen genes: a variety of molecular alterations affect organismal morphology. Mol. Biol. Cell 4, 803-817.
38. Lowe, M., and Kreis, T.E. (1998). Regulation of membrane traffic in animal cells by COPI. Biochim. Biophys. Acta 1404, 53-66.
39. McCarter, J., Bartlett, B., Dang, T., and Schedl, T. (1999). On the control of oocyte meiotic maturation and ovulation in Caenorhabditis elegans. Dev. Biol. 205, 111-128.
40. McLauchlan, H., Newell, J., Morrice, N., Osborne, A., West, M., and Smythe, E. (1998). A novel role for Rab5-GDI in ligand sequestration into clathrin-coated pits. Curr. Biol. 8, 34-45.
41. Mellman, I. (1996). Endocytosis and molecular sorting. Annu. Rev. Cell Dev. Biol. 12, 575-625.
42. Mello, C.C., Kramer, J.M., Stinchcomb, D., and Ambros, V. (1991). Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J. 10, 3959-3970.
43. Montgomery, M.K., Xu, S., and Fire, A. (1998). RNA as a target of double-stranded RNA-mediated genetic interference in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 95, 15502-15507.
44. Mukherjee, S., Ghosh, R.N., and Maxfield, F.R. (1997). Endocytosis. Physiol. Rev. 77, 759-803.
45. Nonet, M.L., Grundahl, K., Meyer, B.J., and Rand, J.B. (1993). Synaptic function is impaired but not eliminated in C elegans mutants lacking synaptotagmin. Cell 73, 1291-1305.
46. Nigon, V. (1949). Les modalites de la reproduction et le determinisme du sexe chez quelques nematodes libres. Ann. Sci. Nat. 11, 1-132.
47. Ohno, H., Aguilar, R.C., Yeh, D., Taura, D., Saito, T., and Bonifacino, J.S. (1998). The medium subunits of adaptor complexes recognize distinct but overlapping sets of tyrosine-based sorting signals. J. Biol. Chem. 273, 25915-25921.
48. Ohno, H., Stewart, J., Fournier, M.C., Bosshart, H., Rhee, I., Miyatake, S., Saito, T., Gallusser, A., Kirchhausen, T., and Bonifacino, J.S. (1995). Interaction of tyrosine-based sorting signals with clathrin-associated proteins. Science 269, 1872-1875.
49. Okkema, P.G., Harrison, S.W., Plunger, V., Aryana, A., and Fire, A. (1993). Sequence requirements for myosin gene-expression and regulation in Caenorhabditis elegans. Genetics 135, 385-404.
50. Page, L.J., Darmon, A.J., Uellner, R., and Griffiths, G.M. (1998). L is for lytic granules: lysosomes that kill. Biochim. Biophys. Acta 1401, 146-156.
51. Pearse, B.M., and Robinson, M.S. (1990). Clathrin, adaptors, and sorting. Annu. Rev. Cell Biol. 6, 151-171.
52. Pfeffer, S.R. (1994). Rab GTPases: master regulators of membrane trafficking. Curr. Opin. Cell Biol. 6, 522-526.
53. Press, B., Feng, Y., Hoflack, B., and Wandinger-Ness, A. (1998). Mutant Rab7 causes the accumulation of cathepsin D and cation-independent mannose 6-phosphate receptor in an early endocytic compartment. J. Cell Biol. 140, 1075-1089.
54. Roth, T.F., and Porter, K.R. (1964). Yolk protein uptake in the oocyte of the mosquito Aedes aegypti. J. Cell Biol. 20, 313-332.
55. Rothman, J.E., and Wieland, F.T. (1996). Protein sorting by transport vesicles. Science 272, 227-234.
56. Sappington, T.W., and Raikhel, A.S. (1998). Molecular characteristics of insect vitellogenins and vitellogenin receptors. Insect Biochem. Mol. Biol. 28, 277-300.
57. Sawamura, T., et al. (1997). An endothelial receptor for oxidized low-density lipoprotein. Nature 386, 73-77.
58. Schekman, R., and Orci, L. (1996). Coat proteins and vesicle budding. Science 271, 1526-1533.
59. Schneider, W.J. (1996). Vitellogenin receptors: oocyte-specific members of the low-density lipoprotein receptor supergene family. Int. Rev. Cytol. 166, 103-137.
60. Schonbaum, C.P., Lee, S., and Mahowald, A.P. (1995). The Drosophila yolkless gene encodes a vitellogenin receptor belonging to the low density lipoprotein receptor superfamily. Proc. Natl. Acad. Sci. USA 92, 1485-1489.
61. Sharrock, W.J. (1983). Yolk proteins of C. elegans. Dev. Biol. 96, 182-188.
62. Sharrock, W.J., Sutherlin, M.E., Leske, K., Cheng, T.K., and Kim, T.Y. (1990). Two distinct yolk lipoprotein complexes from Caenorhabditis elegans. J. Biol. Chem. 265, 14422-14431.
63. Shen, X., Steyrer, E., Retzek, H., Sanders, E.J., and Schneider, W.J. (1993). Chicken oocyte growth: receptor-mediated yolk deposition. Cell Tissue Res. 272, 459-471.
64. Spieth, J., Nettleton, M., Zucker-Aprison, E., Lea, K., and Blumenthal, T. (1991). Vitellogenin motifs conserved in nematodes and vertebrates. J. Mol. Evol. 32, 429-438.
65. Springer, T.A. (1998). An extracellular beta-propeller module predicted in lipoprotein and scavenger receptors, tyrosine kinases, epidermal growth factor precursor, and extracellular matrix components. J. Mol. Biol. 283, 837-862.
66. Stifani, S., Barber, D.L., Nimpf, J., and Schneider, W.J. (1990). A single chicken oocyte plasma membrane protein mediates uptake of very low density lipoprotein and vitellogenin. Proc. Natl. Acad. Sci. USA 87, 1955-1959.
67. Sudhof, T.C., Goldstein, J.L., Brown, M.S., and Russell, D.W. (1985). The LDL receptor gene: a mosaic of exons shared with different proteins. Science 228, 815-822.
68. Ullrich, O., Reinsch, S., Urbe, S., Zerial, M., and Parton, R.G. (1996). Rab11 regulates recycling through the pericentriolar recycling endosome. J. Cell Biol. 135, 913-924.
69. van der Sluijs, P., Hull, M., Webster, P., Male, P., Goud, B., and Mellman, I. (1992). The small GTP-binding protein rab4 controls an early sorting event on the endocytic pathway. Cell 70, 729-740.
70. van Luenen, H.G.A.M., and Plasterk, R.H.A. (1997). Transposons. In: C. elegans, vol. II, ed. T. Blumenthal, D.L. Riddle, B.J. Meyer, and J.R. Priess, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 97-116.
71. von Heijne, G. (1986). A new method for predicting signal sequence cleavage sites. Nucleic Acids Res. 14, 4683-4690.
72. Wang, L.H., Sudhof, T.C., and Anderson, R.G. (1995). The appendage domain of alpha-adaptin is a high affinity binding site for dynamin. J. Biol. Chem. 270, 10079-10083.
73. Wen, C., and Greenwald, I. (1999). p24 proteins and quality control of LIN-12 and GLP-1 trafficking in Caenorhabditis elegans. J. Cell Biol. 145, 1165-1175.
74. Wendland, B., Emr, S.D., and Riezman, H. (1998). Protein traffic in the yeast endocytic and vacuolar protein sorting pathways. Curr. Opin. Cell Biol. 10, 513-522.
75. Williams, B.D. (1995). Genetic mapping with polymorphic sequence-tagged sites. Methods Cell Biol. 48, 81-96.
76. Yochem, J., and Greenwald, I. (1993). A gene for a low density lipoprotein receptor-related protein in the nematode Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 90, 4572-4576.
77. Yochem, J., Tuck, S., Greenwald, I., and Han, M. (1999). A gp330/ megalin-related protein is required in the major epidermis of Caenorhabditis elegans for completion of molting. Development 126, 597-606.