Dynamic regulation of caveolin-1 trafficking in the germ line and embryo of Caenorhabditis elegans

Molecular Biology of the Cell

Volumn 17, Issue 7, 2006, Pages 3085-3094

  Sato, Ken ^a,b   Sato, Miyuki ^a,b   Audhya, Anjon ^c   Oegema, Karen ^c   Schweinsberg, Peter ^a   Grant, Barth D ^a  

^a RUTGERS UNIVERSITY   (United States)

^b GUNMA UNIVERSITY   (Japan)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CAVEOLIN 1; CLATHRIN; DYNAMIN; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; RAB PROTEIN;

ANAPHASE; ANIMAL CELL; ARTICLE; CAENORHABDITIS ELEGANS; CAVEOLA; CELL CYCLE; CELL MEMBRANE; CONTROLLED STUDY; EMBRYO DEVELOPMENT; ENDOCYTOSIS; EXOCYTOSIS; FERTILIZATION; GERM LINE; GOLGI COMPLEX; NONHUMAN; OVULATION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; RNA INTERFERENCE;

ADP-RIBOSYLATION FACTOR 1; ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CAVEOLIN 1; CELL CYCLE; CELL MEMBRANE; EMBRYO, NONMAMMALIAN; ENDOCYTOSIS; FEMALE; GOLGI APPARATUS; GREEN FLUORESCENT PROTEINS; MEMBRANE FUSION; OOCYTES; RAB5 GTP-BINDING PROTEINS; RNA INTERFERENCE;

CAENORHABDITIS ELEGANS; CHICKEN ANEMIA VIRUS;

EID: 33745612093     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E06-03-0211     Document Type: Article

References (61)

1. Abbott, A. L., and Ducibella, T. (2001). Calcium and the control of mammalian cortical granule exocytosis. Front Biosci. 6, D792-D806.
2. Anderson, R. G. (1998). The caveolae membrane system. Annu. Rev. Biochem. 67, 199-225.
3. Audhya, A., Hyndman, F., McLeod, I. X., Maddox, A. S., Yates, J. R., 3rd, Desai, A., and Oegema, K. (2005). A complex containing the Sm protein CAR-1 and the RNA helicase CGH-1 is required for embryonic cytokinesis in Caenorhabditis elegans. J. Cell Biol. 171, 267-279.
4. Bonifacino, J. S. (2004). The GGA proteins: adaptors on the move. Nat. Rev. Mol. Cell Biol. 5, 23-32.
5. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
6. Brodsky, F. M., Chen, C. Y., Knuehl, C., Towler, M. C., and Wakeham, D. E. (2001). Biological basket weaving: formation and function of clathrin-coated vesicles. Annu. Rev. Cell Dev. Biol. 17, 517-568.
7. del Pozo, M. A., Balasubramanian, N., Alderson, N. B., Kiosses, W. B., Grande-Garcia, A., Anderson, R. G., and Schwartz, M. A. (2005). Phosphocaveolin-1 mediates integrin-regulated membrane domain internalization. Nat. Cell Biol. 7, 901-908.
8. Donaldson, J. G., and Honda, A. (2005). Localization and function of Arf family GTPases. Biochem. Soc. Trans. 33, 639-642.
9. Donaldson, J. G., Honda, A., and Weigert, R. (2005). Multiple activities for Arf1 at the Golgi complex. Biochim. Biophys. Acta 2744, 364-373.
10. Drab, M. et al. (2001). Loss of caveolae, vascular dysfunction, and pulmonary defects in caveolin-1 gene-disrupted mice. Science 293, 2449-2452.
11. Fernandez, I., Ying, Y., Albanesi, J., and Anderson, R. G. (2002). Mechanism of caveolin filament assembly. Proc. Natl. Acad. Sci. USA 99, 11193-11198.
12. Fisher, G. W., and Rebhun, L. I. (1983). Sea urchin egg cortical granule exocytosis is followed by a burst of membrane retrieval via uptake into coated vesicles. Dev. Biol. 99, 456-472.
13. Glenney, J. R., Jr., and Soppet, D. (1992). Sequence and expression of caveolin, a protein component of caveolae plasma membrane domains phosphorylated on tyrosine in Rous sarcoma virus-transformed fibroblasts. Proc. Natl. Acad. Sci. USA 89, 10517-10521.
14. Golden, A., Sadler, P. L., Wallenfang, M. R., Schumacher, J. M., Hamill, D. R., Bates, G., Bowerman, B., Seydoux, G., and Shakes, D. C. (2000). Metaphase to anaphase (mat) transition-defective mutants in Caenorhabditis elegans. J. Cell Biol. 151, 1469-1482.
15. Grant, B., and Hirsh, D. (1999). Receptor-mediated endocytosis in the Caenorhabditis elegans oocyte. Mol. Biol. Cell 10, 4311-4326.
16. Grant, B., Zhang, Y., Paupard, M. C., Lin, S. X., Hall, D. H., and Hirsh, D. (2001). Evidence that RME-1, a conserved C. elegans EH-domain protein, functions in endocytic recycling. Nat. Cell Biol. 3, 573-579.
17. Grant, B. D., and Sato, M. (2006). Intracellular trafficking. In: WormBook, ed. The C. elegans Research Community, WormBook, doi/10.1895/wormbook. 1.77.1, http://www.wormbook.org.
18. Herman, T., and Horvitz, H. R. (1999). Three proteins involved in Caenorhabditis elegans vulval invagination are similar to components of a glycosylation pathway. Proc. Natl. Acad. Sci. USA 96, 974-979.
19. Hicke, L., and Dunn, R. (2003). Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu. Rev. Cell Dev. Biol. 19, 141-172.
20. Huet, C., Ash, J. F., and Singer, S. J. (1980). The antibody-induced clustering and endocytosis of HLA antigens on cultured human fibroblasts. Cell 22, 429-438.
21. Jackson, C. L., and Casanova, J. E. (2000). Turning on ARF: the Sec7 family of guanine-nucleotide-exchange factors. Trends Cell Biol. 20, 60-67.
22. Kadandale, P., and Singson, A. (2004). Oocyte production and sperm utilization patterns in semi-fertile strains of Caenorhabditis elegans. BMC Dev. Biol. 4, 3.
23. Kamath, R. S., and Ahringer, J. (2003). Genome-wide RNAi screening in Caenorhabditis elegans. Methods 30, 313-321.
24. Le Lay, S., and Kurzchalia, T. V. (2005). Getting rid of caveolins: phenotypes of caveolin-deficient animals. Biochim. Biophys. Acta 1746, 322-333.
25. Lipardi, C., Mora, R., Colomer, V., Paladino, S., Nitsch, L., Rodriguez-Boulan, E., and Zurzolo, C. (1998). Caveolin transfection results in caveolae formation but not apical sorting of glycosylphosphatidylinositol (GPI)-anchored proteins in epithelial cells. J. Cell Biol. 240, 617-626.
26. Maduro, M., and Pilgrim, D. (1995). Identification and cloning of unc-119, a gene expressed in the Caenorhabditis elegans nervous system. Genetics 242, 977-988.
27. Matveev, S., Li, X., Everson, W., and Smart, E. J. (2001). caveolae and caveolin in vesicle-dependent and vesicle-independent trafficking. Adv. Drug Delivery Rev. 49, 237-250.
28. Matyash, V., Geier, C., Henske, A., Mukherjee, S., Hirsh, D., Thiele, C., Grant, B., Maxfield, F. R., and Kurzchalia, T. V. (2001). Distribution and transport of cholesterol in Caenorhabditis elegans. Mol. Biol. Cell 22, 1725-1736.
29. 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.
30. Miller, M. A., Nguyen, V. Q., Lee, M. H., Kosinski, M., Schedl, T., Caprioli, R. M., and Greenstein, D. (2001). A sperm cytoskeletal protein that signals oocyte meiotic maturation and ovulation. Science 292, 2144-2147.
31. Murata, M., Peranen, J., Schreiner, R., Wieland, F., Kurzchalia, T. V., and Simons, K. (1995). VIP21/caveolin is a cholesterol-binding protein. Proc. Natl. Acad. Sci. USA 92, 10339-10343.
32. Nie, Z., Hirsch, D. S., and Randazzo, P. A. (2003). Arf and its many interactors. Curr. Opin. Cell Biol. 25, 396-404.
33. Parton, R. G. (1996). Caveolae and caveolins. Curr. Opin. Cell Biol. 8, 542-548.
34. Parton, R. G., Joggerst, B., and Simons, K. (1994). Regulated internalization of caveolae. J. Cell Biol. 127, 1199-1215.
35. Parton, R. G., and Richards, A. A. (2003). Lipid rafts and caveolae as portals for endocytosis: new insights and common mechanisms. Traffic 4, 724-738.
36. Pelkmans, L., Burli, T., Zerial, M., and Helenius, A. (2004). Caveolin-stabilized membrane domains as multifunctional transport and sorting devices in endocytic membrane traffic. Cell 118, 767-780.
37. Pelkmans, L., Fava, E., Grabner, H., Hannus, M., Habermann, B., Krausz, E., and Zerial, M. (2005). Genome-wide analysis of human kinases in clathrin-and caveolae/raft-mediated endocytosis. Nature 436, 78-86.
38. Pelkmans, L., Kartenbeck, J., and Helenius, A. (2001). Caveolar endocytosis of simian virus 40 reveals a new two-step vesicular-transport pathway to the ER. Nat. Cell Biol. 3, 473-483.
39. Pelkmans, L., Puntener, D., and Helenius, A. (2002). Local actin polymerization and dynamin recruitment in SV40-induced internalization of caveolae. Science 296, 535-539.
40. Pelkmans, L., and Zerial, M. (2005). Kinase-regulated quantal assemblies and kiss-and-run recycling of caveolae. Nature 436, 128-133.
41. Pellettieri, J., Reinke, V., Kim, S. K., and Seydoux, G. (2003). Coordinate activation of maternal protein degradation during the egg-to-embryo transition in C. elegans. Dev. Cell 5, 451-462.
42. Pol, A., Martin, S., Fernandez, M. A., Ferguson, C., Carozzi, A., Luetterforst, R., Enrich, C., and Parton, R. G. (2004). Dynamic and regulated association of caveolin with lipid bodies: modulation of lipid body motility and function by a dominant negative mutant. Mol. Biol. Cell 25, 99-110.
43. Praitis, V., Casey, E., Collar, D., and Austin, J. (2001). Creation of low-copy integrated transgenic lines in Caenorhabditis elegans. Genetics 257, 1217-1226.
44. Raiborg, C., Rusten, T. E., and Stenmark, H. (2003). Protein sorting into multivesicular endosomes. Curr. Opin. Cell Biol. 25, 446-455.
45. Robinson, M. S. (2004). Adaptable adaptors for coated vesicles. Trends Cell Biol. 74, 167-174.
46. Rothberg, K. G., Heuser, J. E., Donzell, W. C., Ying, Y. S., Glenney, J. R., and Anderson, R. G. (1992). Caveolin, a protein component of caveolae membrane coats. Cell 68, 673-682.
47. Roy, S., Luetterforst, R., Harding, A., Apolloni, A., Etheridge, M., Stang, E., Rolls, B., Hancock, J. F., and Parton, R. G. (1999). Dominant-negative caveolin inhibits H-Ras function by disrupting cholesterol-rich plasma membrane domains. Nat. Cell Biol. 7, 98-105.
48. Sato, M., Sato, K., Fonarev, P., Huang, C. J., Liou, W., and Grant, B. D. (2005). Caenorhabditis elegans RME-6 is a novel regulator of RAB-5 at the clathrin-coated pit. Nat. Cell Biol. 7, 559-569.
49. Schedl, T., and Kimble, J. (1988). fog-2, a germ-line-specific sex determination gene required for hermaphrodite spermatogenesis in Caenorhabditis elegans. Genetics 229, 43-61.
50. Scheel, J., Srinivasan, J., Honnert, U., Henske, A., and Kurzchalia, T. V. (1999). Involvement of caveolin-1 in meiotic cell-cycle progression in Caenorhabditis elegans. Nat. Cell Biol. 2, 127-129.
51. Singson, A., Mercer, K. B., and L'Hernault, S. W. (1998). The C. elegans spe-9 gene encodes a sperm transmembrane protein that contains EGF-like repeats and is required for fertilization. Cell 93, 71-79.
52. Srayko, M., Buster, D. W., Bazirgan, O. A., McNally, F. J., and Mains, P. E. (2000). MEI-1/MEI-2 katanin-like microtubule severing activity is required for Caenorhabditis elegans meiosis. Genes Dev. 14, 1072-1084.
53. Stearns, T., Willingham, M. C., Botstein, D., and Kahn, R. A. (1990). ADP-ribosylation factor is functionally and physically associated with the Golgi complex. Proc. Natl. Acad. Sci. USA 87, 1238-1242.
54. Tagawa, A., Mezzacasa, A., Hayer, A., Longatti, A., Pelkmans, L., and Helenius, A. (2005). Assembly and trafficking of caveolar domains in the cell: caveolae as stable, cargo-triggered, vesicular transporters. J. Cell Biol. 370, 769-779.
55. Takei, K., Yoshida, Y., and Yamada, H. (2005). Regulatory mechanisms of dynamin-dependent endocytosis. J Biochem. (Tokyo) 237, 243-247.
56. Tang, Z., Okamoto, T., Boontrakulpoontawee, P., Katada, T., Otsuka, A. J., and Lisanti, M. P. (1997). Identification, sequence, and expression of an invertebrate caveolin gene family from the nematode Caenorhabditis elegnns. Implications for the molecular evolution of mammalian caveolin genes. J. Biol. Chem. 272, 437-2445.
57. Thomsen, P., Roepstorff, K., Stahlhut, M., and van Deurs, B. (2002). Caveolae are highly immobile plasma membrane microdomains, which are not involved in constitutive endocytic trafficking. Mol. Biol. Cell 13, 238-250.
58. Timmons, L., Court, D. L., and Fire, A. (2001). Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 263, 103-112.
59. Togawa, A., Morinaga, N., Ogasawara, M., Moss, J., and Vaughan, M. (1999). Purification and cloning of a brefeldin A-inhibited guanine nucleotide-exchange protein for ADP-ribosylation factors. J. Biol. Chem. 274, 12308-12315.
60. Yamaji, R., Adamik, R., Takeda, K., Togawa, A., Pacheco-Rodriguez, G., Ferrans, V. J., Moss, J., and Vaughan, M. (2000). Identification and localization of two brefeldin A-inhibited guanine nucleotide-exchange proteins for ADP-ribosylation factors in a macromolecular complex. Proc. Natl. Acad. Sci. USA 97, 2567-2572.
61. Zerial, M., and McBride, H. (2001). Rab proteins as membrane organizers. Nat. Rev. Mol. Cell Biol. 2, 107-117.