Skip to main content
NCBI home page
Genetics logoLink to Genetics
. 2001 Sep;159(1):133–145. doi: 10.1093/genetics/159.1.133

Genetic analysis of endocytosis in Caenorhabditis elegans: coelomocyte uptake defective mutants.

H Fares 1, I Greenwald 1
PMCID: PMC1461804  PMID: 11560892

Abstract

The coelomocytes of Caenorhabditis elegans are scavenger cells that continuously and nonspecifically endocytose fluid from the pseudocoelom (body cavity). Green fluorescent protein (GFP) secreted into the pseudocoelom from body wall muscle cells is endocytosed and degraded by coelomocytes. We show that toxin-mediated ablation of coelomocytes results in viable animals that fail to endocytose pseudocoelomic GFP, indicating that endocytosis by coelomocytes is not essential for growth or survival of C. elegans under normal laboratory conditions. We examined known viable endocytosis mutants, and performed RNAi for other known endocytosis genes, for coelomocyte uptake defective (Cup) phenotypes. We also screened for new genes involved in endocytosis by isolating viable mutants with Cup defects; this screen identified 14 different genes, many with multiple alleles. A variety of Cup terminal phenotypes were observed, consistent with defects at various steps in the endocytic pathway. Available molecular information indicates that the Cup mutant screen has identified novel components of the endocytosis machinery that are conserved in mammals but not in Saccharomyces cerevisiae, the only other organism for which large-scale genetic screens for endocytosis mutants have been performed.

Full Text

The Full Text of this article is available as a PDF (246.7 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aalto M. K., Ruohonen L., Hosono K., Keränen S. Cloning and sequencing of the yeast Saccharomyces cerevisiae SEC1 gene localized on chromosome IV. Yeast. 1991 Aug-Sep;7(6):643–650. doi: 10.1002/yea.320070613. [DOI] [PubMed] [Google Scholar]
  2. Achstetter T., Franzusoff A., Field C., Schekman R. SEC7 encodes an unusual, high molecular weight protein required for membrane traffic from the yeast Golgi apparatus. J Biol Chem. 1988 Aug 25;263(24):11711–11717. [PubMed] [Google Scholar]
  3. Backer J. M. Phosphoinositide 3-kinases and the regulation of vesicular trafficking. Mol Cell Biol Res Commun. 2000 Apr;3(4):193–204. doi: 10.1006/mcbr.2000.0202. [DOI] [PubMed] [Google Scholar]
  4. Bacon R. A., Cohen C. J., Lewin D. A., Mellman I. Dictyostelium discoideum mutants with temperature-sensitive defects in endocytosis. J Cell Biol. 1994 Oct;127(2):387–399. doi: 10.1083/jcb.127.2.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bargal R., Avidan N., Ben-Asher E., Olender Z., Zeigler M., Frumkin A., Raas-Rothschild A., Glusman G., Lancet D., Bach G. Identification of the gene causing mucolipidosis type IV. Nat Genet. 2000 Sep;26(1):118–123. doi: 10.1038/79095. [DOI] [PubMed] [Google Scholar]
  6. Bassi M. T., Manzoni M., Monti E., Pizzo M. T., Ballabio A., Borsani G. Cloning of the gene encoding a novel integral membrane protein, mucolipidin-and identification of the two major founder mutations causing mucolipidosis type IV. Am J Hum Genet. 2000 Sep 29;67(5):1110–1120. doi: 10.1016/s0002-9297(07)62941-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Baumert M., Maycox P. R., Navone F., De Camilli P., Jahn R. Synaptobrevin: an integral membrane protein of 18,000 daltons present in small synaptic vesicles of rat brain. EMBO J. 1989 Feb;8(2):379–384. doi: 10.1002/j.1460-2075.1989.tb03388.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Becker M., Matzner M., Gerisch G. Drainin required for membrane fusion of the contractile vacuole in Dictyostelium is the prototype of a protein family also represented in man. EMBO J. 1999 Jun 15;18(12):3305–3316. doi: 10.1093/emboj/18.12.3305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Bossinger O., Schierenberg E. The use of fluorescent marker dyes for studying intercellular communication in nematode embryos. Int J Dev Biol. 1996 Feb;40(1):431–439. [PubMed] [Google Scholar]
  10. Brenner S. The genetics of Caenorhabditis elegans. Genetics. 1974 May;77(1):71–94. doi: 10.1093/genetics/77.1.71. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Chalfie M., Tu Y., Euskirchen G., Ward W. W., Prasher D. C. Green fluorescent protein as a marker for gene expression. Science. 1994 Feb 11;263(5148):802–805. doi: 10.1126/science.8303295. [DOI] [PubMed] [Google Scholar]
  12. Chavrier P., Parton R. G., Hauri H. P., Simons K., Zerial M. Localization of low molecular weight GTP binding proteins to exocytic and endocytic compartments. Cell. 1990 Jul 27;62(2):317–329. doi: 10.1016/0092-8674(90)90369-p. [DOI] [PubMed] [Google Scholar]
  13. Chen H., Fre S., Slepnev V. I., Capua M. R., Takei K., Butler M. H., Di Fiore P. P., De Camilli P. Epsin is an EH-domain-binding protein implicated in clathrin-mediated endocytosis. Nature. 1998 Aug 20;394(6695):793–797. doi: 10.1038/29555. [DOI] [PubMed] [Google Scholar]
  14. Choy R. K., Thomas J. H. Fluoxetine-resistant mutants in C. elegans define a novel family of transmembrane proteins. Mol Cell. 1999 Aug;4(2):143–152. doi: 10.1016/s1097-2765(00)80362-7. [DOI] [PubMed] [Google Scholar]
  15. Chvatchko Y., Howald I., Riezman H. Two yeast mutants defective in endocytosis are defective in pheromone response. Cell. 1986 Aug 1;46(3):355–364. doi: 10.1016/0092-8674(86)90656-2. [DOI] [PubMed] [Google Scholar]
  16. Clark S. G., Shurland D. L., Meyerowitz E. M., Bargmann C. I., van der Bliek A. M. A dynamin GTPase mutation causes a rapid and reversible temperature-inducible locomotion defect in C. elegans. Proc Natl Acad Sci U S A. 1997 Sep 16;94(19):10438–10443. doi: 10.1073/pnas.94.19.10438. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Colbaugh P. A., Kao C. Y., Shia S. P., Stookey M., Draper R. K. Three new complementation groups of temperature-sensitive Chinese hamster ovary cell mutants defective in the endocytic pathway. Somat Cell Mol Genet. 1988 Sep;14(5):499–507. doi: 10.1007/BF01534715. [DOI] [PubMed] [Google Scholar]
  18. Conboy M. J., Cyert M. S. Luv1p/Rki1p/Tcs3p/Vps54p, a yeast protein that localizes to the late Golgi and early endosome, is required for normal vacuolar morphology. Mol Biol Cell. 2000 Jul;11(7):2429–2443. doi: 10.1091/mbc.11.7.2429. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Creutz C. E., Harrison J. R. Clathrin light chains and secretory vesicle binding proteins are distinct. Nature. 1984 Mar 8;308(5955):208–210. doi: 10.1038/308208a0. [DOI] [PubMed] [Google Scholar]
  20. Creutz C. E., Tomsig J. L., Snyder S. L., Gautier M. C., Skouri F., Beisson J., Cohen J. The copines, a novel class of C2 domain-containing, calcium-dependent, phospholipid-binding proteins conserved from Paramecium to humans. J Biol Chem. 1998 Jan 16;273(3):1393–1402. doi: 10.1074/jbc.273.3.1393. [DOI] [PubMed] [Google Scholar]
  21. DeLange R. J., Williams L. C., Drazin R. E., Collier R. J. The amino acid sequence of fragment A, an enzymically active fragment of diphtheria toxin. III. The chymotryptic peptides, the peptides derived by cleavage at tryptophan residues, and the complete sequence of the protein. J Biol Chem. 1979 Jul 10;254(13):5838–5842. [PubMed] [Google Scholar]
  22. Fares H., Greenwald I. Regulation of endocytosis by CUP-5, the Caenorhabditis elegans mucolipin-1 homolog. Nat Genet. 2001 May;28(1):64–68. doi: 10.1038/ng0501-64. [DOI] [PubMed] [Google Scholar]
  23. Fire A. Integrative transformation of Caenorhabditis elegans. EMBO J. 1986 Oct;5(10):2673–2680. doi: 10.1002/j.1460-2075.1986.tb04550.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Fire A., Xu S., Montgomery M. K., Kostas S. A., Driver S. E., Mello C. C. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature. 1998 Feb 19;391(6669):806–811. doi: 10.1038/35888. [DOI] [PubMed] [Google Scholar]
  25. Fitzgerald K., Greenwald I. Interchangeability of Caenorhabditis elegans DSL proteins and intrinsic signalling activity of their extracellular domains in vivo. Development. 1995 Dec;121(12):4275–4282. doi: 10.1242/dev.121.12.4275. [DOI] [PubMed] [Google Scholar]
  26. Grant B., Greenwald I. Structure, function, and expression of SEL-1, a negative regulator of LIN-12 and GLP-1 in C. elegans. Development. 1997 Feb;124(3):637–644. doi: 10.1242/dev.124.3.637. [DOI] [PubMed] [Google Scholar]
  27. Grant B., Hirsh D. Receptor-mediated endocytosis in the Caenorhabditis elegans oocyte. Mol Biol Cell. 1999 Dec;10(12):4311–4326. doi: 10.1091/mbc.10.12.4311. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Grant B., Zhang Y., Paupard M. C., Lin S. X., Hall D. H., Hirsh D. Evidence that RME-1, a conserved C. elegans EH-domain protein, functions in endocytic recycling. Nat Cell Biol. 2001 Jun;3(6):573–579. doi: 10.1038/35078549. [DOI] [PubMed] [Google Scholar]
  29. Harris T. W., Hartwieg E., Horvitz H. R., Jorgensen E. M. Mutations in synaptojanin disrupt synaptic vesicle recycling. J Cell Biol. 2000 Aug 7;150(3):589–600. doi: 10.1083/jcb.150.3.589. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Henley J. R., Krueger E. W., Oswald B. J., McNiven M. A. Dynamin-mediated internalization of caveolae. J Cell Biol. 1998 Apr 6;141(1):85–99. doi: 10.1083/jcb.141.1.85. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Hill E., van Der Kaay J., Downes C. P., Smythe E. The role of dynamin and its binding partners in coated pit invagination and scission. J Cell Biol. 2001 Jan 22;152(2):309–323. doi: 10.1083/jcb.152.2.309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Hobbie L., Fisher A. S., Lee S., Flint A., Krieger M. Isolation of three classes of conditional lethal Chinese hamster ovary cell mutants with temperature-dependent defects in low density lipoprotein receptor stability and intracellular membrane transport. J Biol Chem. 1994 Aug 19;269(33):20958–20970. [PubMed] [Google Scholar]
  33. Hoekstra D., van IJzendoorn S. C. Lipid trafficking and sorting: how cholesterol is filling gaps. Curr Opin Cell Biol. 2000 Aug;12(4):496–502. doi: 10.1016/s0955-0674(00)00122-8. [DOI] [PubMed] [Google Scholar]
  34. Huang K. M., D'Hondt K., Riezman H., Lemmon S. K. Clathrin functions in the absence of heterotetrameric adaptors and AP180-related proteins in yeast. EMBO J. 1999 Jul 15;18(14):3897–3908. doi: 10.1093/emboj/18.14.3897. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Jantsch-Plunger V., Glotzer M. Depletion of syntaxins in the early Caenorhabditis elegans embryo reveals a role for membrane fusion events in cytokinesis. Curr Biol. 1999 Jul 15;9(14):738–745. doi: 10.1016/s0960-9822(99)80333-9. [DOI] [PubMed] [Google Scholar]
  36. Jones D., Russnak R. H., Kay R. J., Candido E. P. Structure, expression, and evolution of a heat shock gene locus in Caenorhabditis elegans that is flanked by repetitive elements. J Biol Chem. 1986 Sep 15;261(26):12006–12015. [PubMed] [Google Scholar]
  37. Kimble J., Sharrock W. J. Tissue-specific synthesis of yolk proteins in Caenorhabditis elegans. Dev Biol. 1983 Mar;96(1):189–196. doi: 10.1016/0012-1606(83)90322-6. [DOI] [PubMed] [Google Scholar]
  38. Konzok A., Weber I., Simmeth E., Hacker U., Maniak M., Müller-Taubenberger A. DAip1, a Dictyostelium homologue of the yeast actin-interacting protein 1, is involved in endocytosis, cytokinesis, and motility. J Cell Biol. 1999 Jul 26;146(2):453–464. doi: 10.1083/jcb.146.2.453. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Kostich M., Fire A., Fambrough D. M. Identification and molecular-genetic characterization of a LAMP/CD68-like protein from Caenorhabditis elegans. J Cell Sci. 2000 Jul;113(Pt 14):2595–2606. doi: 10.1242/jcs.113.14.2595. [DOI] [PubMed] [Google Scholar]
  40. Krieger M. Isolation of somatic cell mutants with defects in the endocytosis of low-density lipoprotein. Methods Enzymol. 1986;129:227–237. doi: 10.1016/0076-6879(86)29072-2. [DOI] [PubMed] [Google Scholar]
  41. Lander E. S., Linton L. M., Birren B., Nusbaum C., Zody M. C., Baldwin J., Devon K., Dewar K., Doyle M., FitzHugh W. Initial sequencing and analysis of the human genome. Nature. 2001 Feb 15;409(6822):860–921. doi: 10.1038/35057062. [DOI] [PubMed] [Google Scholar]
  42. Lee J., Jongeward G. D., Sternberg P. W. unc-101, a gene required for many aspects of Caenorhabditis elegans development and behavior, encodes a clathrin-associated protein. Genes Dev. 1994 Jan;8(1):60–73. doi: 10.1101/gad.8.1.60. [DOI] [PubMed] [Google Scholar]
  43. Lemmon S. K., Traub L. M. Sorting in the endosomal system in yeast and animal cells. Curr Opin Cell Biol. 2000 Aug;12(4):457–466. doi: 10.1016/s0955-0674(00)00117-4. [DOI] [PubMed] [Google Scholar]
  44. Lin S. X., Grant B., Hirsh D., Maxfield F. R. Rme-1 regulates the distribution and function of the endocytic recycling compartment in mammalian cells. Nat Cell Biol. 2001 Jun;3(6):567–572. doi: 10.1038/35078543. [DOI] [PubMed] [Google Scholar]
  45. Lundquist E. A., Herman R. K., Shaw J. E., Bargmann C. I. UNC-115, a conserved protein with predicted LIM and actin-binding domains, mediates axon guidance in C. elegans. Neuron. 1998 Aug;21(2):385–392. doi: 10.1016/s0896-6273(00)80547-4. [DOI] [PubMed] [Google Scholar]
  46. Maniak M., Rauchenberger R., Albrecht R., Murphy J., Gerisch G. Coronin involved in phagocytosis: dynamics of particle-induced relocalization visualized by a green fluorescent protein Tag. Cell. 1995 Dec 15;83(6):915–924. doi: 10.1016/0092-8674(95)90207-4. [DOI] [PubMed] [Google Scholar]
  47. Matyash V., Geier C., Henske A., Mukherjee S., Hirsh D., Thiele C., Grant B., Maxfield F. R., Kurzchalia T. V. Distribution and transport of cholesterol in Caenorhabditis elegans. Mol Biol Cell. 2001 Jun;12(6):1725–1736. doi: 10.1091/mbc.12.6.1725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. McKim K. S., Matheson C., Marra M. A., Wakarchuk M. F., Baillie D. L. The Caenorhabditis elegans unc-60 gene encodes proteins homologous to a family of actin-binding proteins. Mol Gen Genet. 1994 Feb;242(3):346–357. doi: 10.1007/BF00280425. [DOI] [PubMed] [Google Scholar]
  49. Mello C., Fire A. DNA transformation. Methods Cell Biol. 1995;48:451–482. [PubMed] [Google Scholar]
  50. Mukherjee S., Ghosh R. N., Maxfield F. R. Endocytosis. Physiol Rev. 1997 Jul;77(3):759–803. doi: 10.1152/physrev.1997.77.3.759. [DOI] [PubMed] [Google Scholar]
  51. Nehrke K., Begenisich T., Pilato J., Melvin J. E. Into ion channel and transporter function. Caenorhabditis elegans ClC-type chloride channels: novel variants and functional expression. Am J Physiol Cell Physiol. 2000 Dec;279(6):C2052–C2066. doi: 10.1152/ajpcell.2000.279.6.C2052. [DOI] [PubMed] [Google Scholar]
  52. Nonet M. L., Grundahl K., Meyer B. J., Rand J. B. Synaptic function is impaired but not eliminated in C. elegans mutants lacking synaptotagmin. Cell. 1993 Jul 2;73(7):1291–1305. doi: 10.1016/0092-8674(93)90357-v. [DOI] [PubMed] [Google Scholar]
  53. Nonet M. L., Holgado A. M., Brewer F., Serpe C. J., Norbeck B. A., Holleran J., Wei L., Hartwieg E., Jorgensen E. M., Alfonso A. UNC-11, a Caenorhabditis elegans AP180 homologue, regulates the size and protein composition of synaptic vesicles. Mol Biol Cell. 1999 Jul;10(7):2343–2360. doi: 10.1091/mbc.10.7.2343. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Otsuka A. J., Jeyaprakash A., García-Añoveros J., Tang L. Z., Fisk G., Hartshorne T., Franco R., Born T. The C. elegans unc-104 gene encodes a putative kinesin heavy chain-like protein. Neuron. 1991 Jan;6(1):113–122. doi: 10.1016/0896-6273(91)90126-k. [DOI] [PubMed] [Google Scholar]
  55. Pearson A. M. Scavenger receptors in innate immunity. Curr Opin Immunol. 1996 Feb;8(1):20–28. doi: 10.1016/s0952-7915(96)80100-2. [DOI] [PubMed] [Google Scholar]
  56. Qualmann B., Roos J., DiGregorio P. J., Kelly R. B. Syndapin I, a synaptic dynamin-binding protein that associates with the neural Wiskott-Aldrich syndrome protein. Mol Biol Cell. 1999 Feb;10(2):501–513. doi: 10.1091/mbc.10.2.501. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Rappleye C. A., Paredez A. R., Smith C. W., McDonald K. L., Aroian R. V. The coronin-like protein POD-1 is required for anterior-posterior axis formation and cellular architecture in the nematode caenorhabditis elegans. Genes Dev. 1999 Nov 1;13(21):2838–2851. doi: 10.1101/gad.13.21.2838. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Reddien P. W., Horvitz H. R. CED-2/CrkII and CED-10/Rac control phagocytosis and cell migration in Caenorhabditis elegans. Nat Cell Biol. 2000 Mar;2(3):131–136. doi: 10.1038/35004000. [DOI] [PubMed] [Google Scholar]
  59. Richmond J. E., Davis W. S., Jorgensen E. M. UNC-13 is required for synaptic vesicle fusion in C. elegans. Nat Neurosci. 1999 Nov;2(11):959–964. doi: 10.1038/14755. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Robbins A. R., Peng S. S., Marshall J. L. Mutant Chinese hamster ovary cells pleiotropically defective in receptor-mediated endocytosis. J Cell Biol. 1983 Apr;96(4):1064–1071. doi: 10.1083/jcb.96.4.1064. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Robinson M. S., Watts C., Zerial M. Membrane dynamics in endocytosis. Cell. 1996 Jan 12;84(1):13–21. doi: 10.1016/s0092-8674(00)80988-5. [DOI] [PubMed] [Google Scholar]
  62. Saifee O., Wei L., Nonet M. L. The Caenorhabditis elegans unc-64 locus encodes a syntaxin that interacts genetically with synaptobrevin. Mol Biol Cell. 1998 Jun;9(6):1235–1252. doi: 10.1091/mbc.9.6.1235. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Seki N., Muramatsu M., Sugano S., Suzuki Y., Nakagawara A., Ohhira M., Hayashi A., Hori T., Saito T. Cloning, expression analysis, and chromosomal localization of HIP1R, an isolog of huntingtin interacting protein (HIP1). J Hum Genet. 1998;43(4):268–271. doi: 10.1007/s100380050087. [DOI] [PubMed] [Google Scholar]
  64. Sever S., Damke H., Schmid S. L. Dynamin:GTP controls the formation of constricted coated pits, the rate limiting step in clathrin-mediated endocytosis. J Cell Biol. 2000 Sep 4;150(5):1137–1148. doi: 10.1083/jcb.150.5.1137. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Shibata Y., Fujii T., Dent J. A., Fujisawa H., Takagi S. EAT-20, a novel transmembrane protein with EGF motifs, is required for efficient feeding in Caenorhabditis elegans. Genetics. 2000 Feb;154(2):635–646. doi: 10.1093/genetics/154.2.635. [DOI] [PMC free article] [PubMed] [Google Scholar]
  66. Simpson F., Peden A. A., Christopoulou L., Robinson M. S. Characterization of the adaptor-related protein complex, AP-3. J Cell Biol. 1997 May 19;137(4):835–845. doi: 10.1083/jcb.137.4.835. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Singleton D. R., Wu T. T., Castle J. D. Three mammalian SCAMPs (secretory carrier membrane proteins) are highly related products of distinct genes having similar subcellular distributions. J Cell Sci. 1997 Sep;110(Pt 17):2099–2107. doi: 10.1242/jcs.110.17.2099. [DOI] [PubMed] [Google Scholar]
  68. Steeg P. S., Bevilacqua G., Kopper L., Thorgeirsson U. P., Talmadge J. E., Liotta L. A., Sobel M. E. Evidence for a novel gene associated with low tumor metastatic potential. J Natl Cancer Inst. 1988 Apr 6;80(3):200–204. doi: 10.1093/jnci/80.3.200. [DOI] [PubMed] [Google Scholar]
  69. Steven R., Kubiseski T. J., Zheng H., Kulkarni S., Mancillas J., Ruiz Morales A., Hogue C. W., Pawson T., Culotti J. UNC-73 activates the Rac GTPase and is required for cell and growth cone migrations in C. elegans. Cell. 1998 Mar 20;92(6):785–795. doi: 10.1016/s0092-8674(00)81406-3. [DOI] [PubMed] [Google Scholar]
  70. Sun M., Goldin E., Stahl S., Falardeau J. L., Kennedy J. C., Acierno J. S., Jr, Bove C., Kaneski C. R., Nagle J., Bromley M. C. Mucolipidosis type IV is caused by mutations in a gene encoding a novel transient receptor potential channel. Hum Mol Genet. 2000 Oct 12;9(17):2471–2478. doi: 10.1093/hmg/9.17.2471. [DOI] [PubMed] [Google Scholar]
  71. Swan K. A., Severson A. F., Carter J. C., Martin P. R., Schnabel H., Schnabel R., Bowerman B. cyk-1: a C. elegans FH gene required for a late step in embryonic cytokinesis. J Cell Sci. 1998 Jul 30;111(Pt 14):2017–2027. doi: 10.1242/jcs.111.14.2017. [DOI] [PubMed] [Google Scholar]
  72. Tabara H., Grishok A., Mello C. C. RNAi in C. elegans: soaking in the genome sequence. Science. 1998 Oct 16;282(5388):430–431. doi: 10.1126/science.282.5388.430. [DOI] [PubMed] [Google Scholar]
  73. Tan M. W., Ausubel F. M. Caenorhabditis elegans: a model genetic host to study Pseudomonas aeruginosa pathogenesis. Curr Opin Microbiol. 2000 Feb;3(1):29–34. doi: 10.1016/s1369-5274(99)00047-8. [DOI] [PubMed] [Google Scholar]
  74. Tcherepanova I., Bhattacharyya L., Rubin C. S., Freedman J. H. Aspartic proteases from the nematode Caenorhabditis elegans. Structural organization and developmental and cell-specific expression of asp-1. J Biol Chem. 2000 Aug 25;275(34):26359–26369. doi: 10.1074/jbc.M000956200. [DOI] [PubMed] [Google Scholar]
  75. TerBush D. R., Maurice T., Roth D., Novick P. The Exocyst is a multiprotein complex required for exocytosis in Saccharomyces cerevisiae. EMBO J. 1996 Dec 2;15(23):6483–6494. [PMC free article] [PubMed] [Google Scholar]
  76. Venter J. C., Adams M. D., Myers E. W., Li P. W., Mural R. J., Sutton G. G., Smith H. O., Yandell M., Evans C. A., Holt R. A. The sequence of the human genome. Science. 2001 Feb 16;291(5507):1304–1351. doi: 10.1126/science.1058040. [DOI] [PubMed] [Google Scholar]
  77. Wang S. S., Devuyst O., Courtoy P. J., Wang X. T., Wang H., Wang Y., Thakker R. V., Guggino S., Guggino W. B. Mice lacking renal chloride channel, CLC-5, are a model for Dent's disease, a nephrolithiasis disorder associated with defective receptor-mediated endocytosis. Hum Mol Genet. 2000 Dec 12;9(20):2937–2945. doi: 10.1093/hmg/9.20.2937. [DOI] [PubMed] [Google Scholar]
  78. Wendland B., McCaffery J. M., Xiao Q., Emr S. D. A novel fluorescence-activated cell sorter-based screen for yeast endocytosis mutants identifies a yeast homologue of mammalian eps15. J Cell Biol. 1996 Dec;135(6 Pt 1):1485–1500. doi: 10.1083/jcb.135.6.1485. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Williams B. D., Schrank B., Huynh C., Shownkeen R., Waterston R. H. A genetic mapping system in Caenorhabditis elegans based on polymorphic sequence-tagged sites. Genetics. 1992 Jul;131(3):609–624. doi: 10.1093/genetics/131.3.609. [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. Wu Y. C., Horvitz H. R. C. elegans phagocytosis and cell-migration protein CED-5 is similar to human DOCK180. Nature. 1998 Apr 2;392(6675):501–504. doi: 10.1038/33163. [DOI] [PubMed] [Google Scholar]
  81. Yeung B. G., Phan H. L., Payne G. S. Adaptor complex-independent clathrin function in yeast. Mol Biol Cell. 1999 Nov;10(11):3643–3659. doi: 10.1091/mbc.10.11.3643. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Zipkin I. D., Kindt R. M., Kenyon C. J. Role of a new Rho family member in cell migration and axon guidance in C. elegans. Cell. 1997 Sep 5;90(5):883–894. doi: 10.1016/s0092-8674(00)80353-0. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES