The caenorhabditis elegans excretory system: A model for tubulogenesis, cell fate specification, and plasticity

Genetics

Volumn 203, Issue 1, 2016, Pages 35-63

  Sundaram, Meera V ^a   Buechner, Matthew ^b  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF KANSAS   (United States)

Author keywords

Caenorhabditis elegans; Excretory secretory system; Tubulogenesis; WormBook

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; RAS PROTEIN; TRANSCRIPTION FACTOR; VASCULOTROPIN;

ARTICLE; AXON; BASEMENT MEMBRANE; CAENORHABDITIS ELEGANS; CELL DIFFERENTIATION; CELL FATE; CELL MIGRATION; CELL PLASTICITY; CELL SHAPE; CELL ULTRASTRUCTURE; CYTOSKELETON; EXOCRINE GLAND; ION TRANSPORT; LARVAL DEVELOPMENT; NONHUMAN; OSMOREGULATION; PHENOTYPE; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ANIMAL; ANTIBODY SPECIFICITY; CYTOLOGY; PHYSIOLOGY; SECRETORY PATHWAY;

ANIMALS; CAENORHABDITIS ELEGANS; CELL PLASTICITY; EXOCRINE GLANDS; ORGAN SPECIFICITY; SECRETORY PATHWAY;

EID: 84979917597     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.116.189357     Document Type: Article

References (271)

1. Abdus-Saboor, I., V. P. Mancuso, J. I. Murray, K. Palozola, C. Norris et al., 2011 Notch and Ras promote sequential steps of excretory tube development in C. elegans. Development 138: 3545–3555.
2. Abdus-Saboor, I., C. E. Stone, J. I. Murray, and M. V. Sundaram, 2012 The Nkx5/HMX homeodomain protein MLS-2 is required for proper tube cell shape in the C. elegans excretory system. Dev. Biol. 366: 298–307.
3. Achilleos, A., A. M. Wehman, and J. Nance, 2010 PAR-3 mediates the initial clustering and apical localization of junction and polarity proteins during C. elegans intestinal epithelial cell polarization. Development 137: 1833–1842.
4. Adlimoghaddam, A., D. Weihrauch, and M. J. O’Donnell, 2014 Localization of K+, H+, Na+ and Ca2+ fluxes to the excretory pore in Caenorhabditis elegans: application of scanning ion-selective microelectrodes. J. Exp. Biol. 217: 4119–4122.
5. Alessi, D. R., J. Zhang, A. Khanna, T. Hochdorfer, Y. Shang et al., 2014 The WNK-SPAK/OSR1 pathway: master regulator of cation-chloride cotransporters. Sci. Signal. 7: re3.
6. Altun, Z. F., B. Chen, Z. W. Wang, and D. H. Hall, 2009 High resolution map of Caenorhabditis elegans gap junction proteins. Dev. Dyn. 238: 1936–1950.
7. Altun-Gultekin, Z., Y. Andachi, E. L. Tsalik, D. Pilgrim, Y. Kohara et al., 2001 A regulatory cascade of three homeobox genes, ceh-10, ttx-3 and ceh-23, controls cell fate specification of a defined interneuron class in C. elegans. Development 128: 1951–1969.
8. Andrini, O., M. Keck, R. Briones, S. Lourdel, R. Vargas-Poussou et al., 2015 ClC-K chloride channels: emerging pathophysiology of Bartter syndrome type 3. Am. J. Physiol. Renal Physiol. 308: F1324–F1334.
9. Armenti, S. T., E. Chan, and J. Nance, 2014 Polarized exocyst-mediated vesicle fusion directs intracellular lumenogenesis within the C. elegans excretory cell. Dev. Biol. 394: 110–121.
10. Armstrong, K. R., and H. M. Chamberlin, 2010 Coordinate regulation of gene expression in the C. elegans excretory cell by the POU domain protein CEH-6. Mol. Genet. Genomics 283: 73–87.
11. Aue, A., C. Hinze, K. Walentin, J. Ruffert, Y. Yurtdas et al., 2015 A Grainyhead-Like 2/Ovo-Like 2 pathway regulates renal epithelial barrier function and lumen expansion. J. Am. Soc. Nephrol. 26: 2704–2715.
12. Bai, Z., and B. D. Grant, 2015 A TOCA/CDC-42/PAR/WAVE functional module required for retrograde endocytic recycling. Proc. Natl. Acad. Sci. USA 112: E1443–E1452.
13. 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.
14. Bär, T., F. H. Guldner, and J. R. Wolff, 1984 “Seamless” endothelial cells of blood capillaries. Cell Tissue Res. 235: 99–106.
15. Bastian, H. C., 1866 On the anatomy and physiology of the nematoids, parasitic and free; with observations on their zoological position and affinities to the echinoderms. Philos. Trans. R. Soc. Lond. 156: 545–638.
16. Baum, P. D., and G. Garriga, 1997 Neuronal migrations and axon fasciculation are disrupted in ina-1 integrin mutants. Neuron 19: 51–62.
17. Beitel, G. J., S. Tuck, I. Greenwald, and H. R. Horvitz, 1995 The Caenorhabditis elegans gene lin-1 encodes an ETS-domain protein and defines a branch in the vulval induction pathway. Genes Dev. 9: 3149–3162.
18. Bennett, V., and J. Healy, 2008 Organizing the fluid membrane bilayer: diseases linked to spectrin and ankyrin. Trends Mol. Med. 14: 28–36.
19. Bergeron, M. J., B. Clemencon, M. A. Hediger, and D. Markovich, 2013 SLC13 family of Na(+)-coupled di- and tri-carboxylate/ sulfate transporters. Mol. Aspects Med. 34: 299–312.
20. Berry, K. L., and O. Hobert, 2006 Mapping functional domains of chloride intracellular channel (CLIC) proteins in vivo. J. Mol. Biol. 359: 1316–1333.
21. Berry, K. L., H. E. Bulow, D. H. Hall, and O. Hobert, 2003 A C. elegans CLIC-like protein required for intracellular tube formation and maintenance. Science 302: 2134–2137.
22. Bhat, J. M., J. Pan, and H. Hutter, 2015 PLR-1, a putative E3 ubiquitin ligase, controls cell polarity and axonal extensions in C. elegans. Dev. Biol. 398: 44–56.
23. Bird, A. F., and B. M. Zuckerman, 1989 Studies on the surface coat (glycocalyx) of the dauer larva of Anguina agrostis. Int. J. Parasitol. 19: 235–240.
24. Bird, J., and A. F. Bird, 1991 Secretory-Excretory System, pp. 167–182 in The Structure of Nematodes. Academic Press, San Diego.
25. Blaxter, M. L., A. P. Page, W. Rudin, and R. M. Maizels, 1992 Nematode surface coats: actively evading immunity. Parasitol. Today 8: 243–247.
26. Borthwick, K. J., and F. E. Karet, 2002 Inherited disorders of the H+-ATPase. Curr. Opin. Nephrol. Hypertens. 11: 563–568.
27. Bossinger, O., A. Klebes, C. Segbert, C. Theres, and E. Knust, 2001 Zonula adherens formation in Caenorhabditis elegans requires dlg-1, the homologue of the Drosophila gene discs large. Dev. Biol. 230: 29–42.
28. Breton, S., and D. Brown, 2013 Regulation of luminal acidification by the V-ATPase. Physiology (Bethesda) 28: 318–329.
29. Brohawn, S. G., 2015 How ion channels sense mechanical force: insights from mechanosensitive K2P channels TRAAK, TREK1, and TREK2. Ann. N. Y. Acad. Sci. 1352: 20–32.
30. Bronicki, L. M., and B. J. Jasmin, 2013 Emerging complexity of the HuD/ELAVl4 gene; implications for neuronal development, function, and dysfunction. RNA 19: 1019–1037.
31. Brose, N., 2009 Synaptogenic proteins and synaptic organizers: “Many hands make light work. Neuron 61: 650–652.
32. Brown, D., R. Bouley, T. G. Paunescu, S. Breton, and H. A. Lu, 2012 New insights into the dynamic regulation of water and acid-base balance by renal epithelial cells. Am. J. Physiol. Cell Physiol. 302: C1421–C1433.
33. Brown, E. J., J. S. Schlondorff, D. J. Becker, H. Tsukaguchi, S. J. Tonna et al., 2010 Mutations in the formin gene INF2 cause focal segmental glomerulosclerosis. Nat. Genet. 42: 72–76.
34. Buechner, M., 2002 Tubes and the single C. elegans excretory cell. Trends Cell Biol. 12: 479–484.
35. Buechner, M., D. H. Hall, H. Bhatt, and E. M. Hedgecock, 1999 Cystic canal mutants in Caenorhabditis elegans are defective in the apical membrane domain of the renal (excretory). Cell. Dev Biol 214: 227–241.
36. Burglin, T. R., 1996 Warthog and groundhog, novel families related to hedgehog. Curr. Biol. 6: 1047–1050.
37. Burglin, T. R., and G. Ruvkun, 2001 Regulation of ectodermal and excretory function by the C. elegans POU homeobox gene ceh-6. Development 128: 779–790.
38. Carberry, K., T. Wiesenfahrt, R. Windoffer, O. Bossinger, and R. E. Leube, 2009 Intermediate filaments in Caenorhabditis elegans. Cell Motil. Cytoskeleton 66: 852–864.
39. Caviglia, S., and S. Luschnig, 2014 Tube fusion: making connections in branched tubular networks. Semin. Cell Dev. Biol. 31: 82–90.
40. Caviston, J. P., and E. L. Holzbaur, 2006 Microtubule motors at the intersection of trafficking and transport. Trends Cell Biol. 16: 530–537.
41. Chang, C., N. A. Hopper, and P. W. Sternberg, 2000 Caenorhabditis elegans SOS-1 is necessary for multiple RAS-mediated developmental signals. EMBO J. 19: 3283–3294.
42. Chitwood, M. B., and B. G. Chitwood, 1974 The excretory system, pp. 126–135 in Introduction to Nematology, edited by B. G. Chitwood, and M. G. Chitwood. University Park Press, Baltimore.
43. Choe, K. P., and K. Strange, 2007 Molecular and genetic characterization of osmosensing and signal transduction in the nematode Caenorhabditis elegans. FEBS J. 274: 5782–5789.
44. Chou, S. Y., K. S. Hsu, W. Otsu, Y. C. Hsu, Y. C. Luo et al., 2016 CLIC4 regulates apical exocytosis and renal tube lumino-genesis through retromer- and actin-mediated endocytic trafficking. Nat. Commun. 7: 10412.
45. Colman, D. R., 1999 Neuronal polarity and the epithelial metaphor. Neuron 23: 649–651.
46. D’Agati, V. D., F. J. Kaskel, and R. J. Falk, 2011 Focal segmental glomerulosclerosis. N. Engl. J. Med. 365: 2398–2411.
47. D’Angelo, G., T. Matusek, S. Pizette, and P. P. Therond, 2015 Endocytosis of Hedgehog through dispatched regulates long-range signaling. Dev. Cell 32: 290–303.
48. Datta, A., D. M. Bryant, and K. E. Mostov, 2011 Molecular regulation of lumen morphogenesis. Curr. Biol. 21: R126–R136.
49. Davis, G. E., and C. W. Camarillo, 1996 An a2b1 integrin-dependent pinocytic mechanism involving intracellular vacuole formation and coalescence regulates capillary lumen and tube formation in three-dimensional collagen matrix. Exp. Cell Res. 224: 39–51.
50. de Baaij, J. H. F., J. G. J. Hoenderop, and R. J. M. Bindels, 2015 Magnesium in man: Implications for health and disease. Physiol. Rev. 95: 1–46.
51. de Grisse, A. T., 1977 De ultrastructuur van het zenuwstelsel in de kop van 22 soorten plantenparasitaire nematoden, behorende tot 19 genera (nematode: Tylenchida), Rijksuniversiteit Gent, Gent, Belgium.
52. Delague, V., A. Jacquier, T. Hamadouche, Y. Poitelon, C. Baudot et al., 2007 Mutations in FGD4 encoding the Rho GDP/GTP exchange factor FRABIN cause autosomal recessive Charcot-Marie-Tooth type 4H. Am. J. Hum. Genet. 81: 1–16.
53. Denker, E., I. Bocina, and D. Jiang, 2013 Tubulogenesis in a simple cell cord requires the formation of bi-apical cells through two discrete Par domains. Development 140: 2985–2996.
54. Denning, D. P., V. Hatch, and H. R. Horvitz, 2012 Programmed elimination of cells by caspase-independent cell extrusion in C. elegans. Nature 488: 226–230.
55. Dent, E. W., S. L. Gupton, and F. B. Gertler, 2011 The growth cone cytoskeleton in axon outgrowth and guidance. Cold Spring Harb. Perspect. Biol. 3: a001800.
56. Denton, J., K. Nehrke, X. Yin, R. Morrison, and K. Strange, 2005 GCK-3, a newly identified Ste20 kinase, binds to and regulates the activity of a cell cycle-dependent ClC anion channel. J. Gen. Physiol. 125: 113–125.
57. Donowitz, M., C. Ming Tse, and D. Fuster, 2013 SLC9/NHE gene family, a plasma membrane and organellar family of Na+/H+ exchangers. Mol. Aspects Med. 34: 236–251.
58. Draheim, K. M., O. S. Fisher, T. J. Boggon, and D. A. Calderwood, 2014 Cerebral cavernous malformation proteins at a glance. J. Cell Sci. 127: 701–707.
59. Eaton, S., and F. Martin-Belmonte, 2014 Cargo sorting in the endocytic pathway: a key regulator of cell polarity and tissue dynamics. Cold Spring Harb. Perspect. Biol. 6: a016899.
60. Everett, L. A., B. Glaser, J. C. Beck, J. R. Idol, A. Buchs et al., 1997 Pendred syndrome is caused by mutations in a putative sulphate transporter gene (PDS). Nat. Genet. 17: 411–422.
61. Feihl, F., L. Liaudet, B. I. Levy, and B. Waeber, 2008 Hypertension and microvascular remodelling. Cardiovasc. Res. 78: 274–285.
62. Fidalgo, M., M. Fraile, A. Pires, T. Force, C. Pombo et al., 2010 CCM3/PDCD10 stabilizes GCKIII proteins to promote Golgi assembly and cell orientation. J. Cell Sci. 123: 1274–1284.
63. Flower, D. R., 1996 The lipocalin protein family: structure and function. Biochem. J. 318(Pt 1): 1–14.
64. Folkman, J., and C. Haudenschild, 1980 Angiogenesis by capillary endothelial cells in culture. Trans. Ophthalmol. Soc. U. K. 100: 346–353.
65. Forrester, W. C., and G. Garriga, 1997 Genes necessary for C. elegans cell and growth cone migrations. Development 124: 1831–1843.
66. Forrester, W. C., E. Perens, J. A. Zallen, and G. Garriga, 1998 Identification of Caenorhabditis elegans genes required for neuronal differentiation and migration. Genetics 148: 151–165.
67. Forrester, W. C., M. Dell, E. Perens, and G. Garriga, 1999 A C. elegans Ror receptor tyrosine kinase regulates cell motility and asymmetric cell division. Nature 400: 881–885.
68. Freeman, M. R., 2015 Drosophila central nervous system glia. Cold Spring Harb. Perspect. Biol. 7: a020552.
69. Fujita, M., D. Hawkinson, K. V. King, D. H. Hall, H. Sakamoto et al., 2003 The role of the ELAV homologue EXC-7 in the development of the Caenorhabditis elegans excretory canals. Dev. Biol. 256: 290–301.
70. Gao, J., L. Estrada, S. Cho, R. E. Ellis, and J. L. Gorski, 2001 The Caenorhabditis elegans homolog of FGD1, the human Cdc42 GEF gene responsible for faciogenital dysplasia, is critical for excretory cell morphogenesis. Hum. Mol. Genet. 10: 3049–3062.
71. Geering, K., 1997 Na,K-ATPase. Curr. Opin. Nephrol. Hypertens. 6: 434–439.
72. Geitmann, A., 2010 How to shape a cylinder: pollen tube as a model system for the generation of complex cellular geometry. Sex. Plant Reprod. 23: 63–71.
73. Gervais, L., and J. Casanova, 2010 In vivo coupling of cell elongation and lumen formation in a single cell. Curr. Biol. 20: 359–366.
74. Gervais, L., G. Lebreton, and J. Casanova, 2012 The making of a fusion branch in the Drosophila trachea. Dev. Biol. 362: 187–193.
75. Gettner, S. N., C. Kenyon, and L. F. Reichardt, 1995 Characterization of bPAT-3 heterodimers, a family of essential integrin receptors in C. elegans. J. Cell Biol. 129: 1127–1141.
76. Ghosh, S., and P. W. Sternberg, 2014 Spatial and molecular cues for cell outgrowth during C. elegans uterine development. Dev. Biol. 396: 121–135.
77. Gissendanner, C. R., and A. E. Sluder, 2000 nhr-25, the Caenorhabditis elegans ortholog of ftz-f1, is required for epidermal and somatic gonad development. Dev. Biol. 221: 259–272.
78. Gobel, V., P. L. Barrett, D. H. Hall, and J. T. Fleming, 2004 Lumen morphogenesis in C. elegans requires the membrane-cytoskeleton linker erm-1. Dev. Cell 6: 865–873.
79. Govani, F. S., and C. L. Shovlin, 2009 Hereditary haemorrhagic telangiectasia: a clinical and scientific review. Eur. J. Hum. Genet. 17: 860–871.
80. Greenwald, I. S., P. W. Sternberg, and H. R. Horvitz, 1983 The lin-12 locus specifies cell fates in Caenorhabditis elegans. Cell 34: 435–444.
81. Guerrero-Esteo, M., T. Sanchez-Elsner, A. Letamendia, and C. Bernabeu, 2002 Extracellular and cytoplasmic domains of endoglin interact with the transforming growth factor-beta receptors I and II. J. Biol. Chem. 277: 29197–29209.
82. Haffner, C., R. Malik, and M. Dichgans, 2016 Genetic factors in cerebral small vessel disease and their impact on stroke and dementia. J. Cereb. Blood Flow Metab. 36: 158–171.
83. Hahn-Windgassen, A., and M. R. Van Gilst, 2009 The Caenorhabditis elegans HNF4a Homolog, NHR-31, mediates excretory tube growth and function through coordinate regulation of the vacuolar ATPase. PLoS Genet. 5: e1000553.
84. Hao, L., R. Johnsen, G. Lauter, D. Baillie, and T. R. Burglin, 2006 Comprehensive analysis of gene expression patterns of hedgehog-related genes. BMC Genomics 7: 280.
85. Harris, J. E., and H. D. Crofton, 1957 Structure and function in the nematodes: internal pressure and cuticular structure in ascaris. J. Exp. Biol. 34: 116–130.
86. Harris, K. P., and U. Tepass, 2010 Cdc42 and vesicle trafficking in polarized cells. Traffic 11: 1272–1279.
87. Hayes, G. D., A. R. Frand, and G. Ruvkun, 2006 The mir-84 and let-7 paralogous microRNA genes of Caenorhabditis elegans direct the cessation of molting via the conserved nuclear hormone receptors NHR-23 and NHR-25. Development 133: 4631–4641.
88. Hedgecock, E. M., and J. G. White, 1985 Polyploid tissues in the nematode Caenorhabditis elegans. Dev. Biol. 107: 128–133.
89. Hedgecock, E. M., J. G. Culotti, D. H. Hall, and B. D. Stern, 1987 Genetics of cell and axon migrations in Caenorhabditis elegans. Development 100: 365–382.
90. Hempel, A., and S. J. Kuhl, 2014 Comparative expression analysis of cysteine-rich intestinal protein family members crip1, 2 and 3 during Xenopus laevis embryogenesis. Int. J. Dev. Biol. 58: 841–849.
91. Herwig, L., Y. Blum, A. Krudewig, E. Ellertsdottir, A. Lenard et al., 2011 Distinct cellular mechanisms of blood vessel fusion in the zebrafish embryo. Curr. Biol. 21: 1942–1948.
92. Hewitson, J. P., J. R. Grainger, and R. M. Maizels, 2009 Helminth immunoregulation: the role of parasite secreted proteins in modulating host immunity. Mol. Biochem. Parasitol. 167: 1–11.
93. Hisamoto, N., T. Moriguchi, S. Urushiyama, S. Mitani, H. Shibuya et al., 2008 Caenorhabditis elegans WNK-STE20 pathway regulates tube formation by modulating ClC channel activity. EMBO Rep. 9: 70–75.
94. Hobert, O., K. Tessmar, and G. Ruvkun, 1999 The Caenorhabditis elegans lim-6 LIM homeobox gene regulates neurite outgrowth and function of particular GABAergic neurons. Development 126: 1547–1562.
95. Howard, J., 2008 The IRG proteins: a function in search of a mechanism. Immunobiol. 213: 367–375.
96. Howard, R. M., and M. V. Sundaram, 2002 C. elegans EOR-1/ PLZF and EOR-2 positively regulate Ras and Wnt signaling and function redundantly with LIN-25 and the SUR-2 Mediator complex. Genes Dev. 16: 1815–1827.
97. Howell, K., S. Arur, T. Schedl, and M. V. Sundaram, 2010 EOR-2 is an obligate binding partner of the BTB-zinc finger protein EOR-1 in Caenorhabditis elegans. Genetics 184: 899–913.
98. Huang, C. G., T. Lamitina, P. Agre, and K. Strange, 2007 Functional analysis of the aquaporin gene family in Caenorhabditis elegans. Am. J. Physiol. Cell Physiol. 292: C1867–C1873.
99. Hunt-Newbury, R., R. Viveiros, R. Johnsen, A. Mah, D. Anastas et al., 2007 High-throughput in vivo analysis of gene expression in Caenorhabditis elegans. PLoS Biol. 5: e237.
100. Huveneers, S., and J. de Rooij, 2013 Mechanosensitive systems at the cadherin-F-actin interface. J. Cell Sci. 126: 403–413.
101. Hwang, J., and D. C. Pallas, 2014 STRIPAK complexes: structure, biological function, and involvement in human diseases. Int. J. Biochem. Cell Biol. 47: 118–148.
102. Imbrici, P., C. Altamura, M. Pessia, R. Mantegazza, J. F. Desaphy et al., 2015 ClC-1 chloride channels: state-of-the-art research and future challenges. Front. Cell. Neurosci. 9: 156.
103. Iruela-Arispe, M. L., and G. E. Davis, 2009 Cellular and molecular mechanisms of vascular lumen formation. Dev. Cell 16: 222–231.
104. Iruela-Arispe, M. L., and G. J. Beitel, 2013 Tubulogenesis. Development 140: 2851–2855.
105. Jacobs, D., G. J. Beitel, S. G. Clark, H. R. Horvitz, and K. Kornfeld, 1998 Gain-of-function mutations in the Caenorhabditis elegans lin-1 ETS gene identify a C-terminal regulatory domain phosphorylated by ERK MAP kinase. Genetics 149: 1809–1822.
106. Jarriault, S., Y. Schwab, and I. Greenwald, 2008 A Caenorhabditis elegans model for epithelial-neuronal transdifferentiation. Proc. Natl. Acad. Sci. USA 105: 3790–3795.
107. JayaNandanan, N., R Mathew, and M Leptin, 2014 Guidance of subcellular tubulogenesis by actin under the control of a synaptotagmin-like protein and Moesin. Nat. Commun. 5: 3036.
108. Jazwinska, A., C. Ribeiro, and M. Affolter, 2003 Epithelial tube morphogenesis during Drosophila tracheal development requires Piopio, a luminal ZP protein. Nat. Cell Biol. 5: 895–901.
109. Jessen, K. R., R. Mirsky, and A. C. Lloyd, 2015 Schwann cells: development and role in nerve repair. Cold Spring Harb. Perspect. Biol. 7: a020487.
110. Jiang, L., J. M. Phang, J. Yu, S. J. Harrop, A. V. Sokolova et al., 2014 CLIC proteins, ezrin, radixin, moesin and the coupling of membranes to the actin cytoskeleton: A smoking gun? Biochim. Biophys. Acta 1838: 643–657.
111. Johansson, M. E., H. Sjovall, and G. C. Hansson, 2013 The gastrointestinal mucus system in health and disease. Nat. Rev. Gastroenterol. Hepatol. 10: 352–361.
112. Johnson, A. D., D. Fitzsimmons, J. Hagman, and H. M. Chamberlin, 2001 EGL-38 Pax regulates the ovo-related gene lin-48 during Caenorhabditis elegans organ development. Development 128: 2857–2865.
113. Jones, S. J., and D. L. Baillie, 1995 Characterization of the let-653 gene in Caenorhabditis elegans. Mol. Gen. Genet. 248: 719–726.
114. Kalluri, R., and R. A. Weinberg, 2009 The basics of epithelial-mesenchymal transition. J. Clin. Invest. 119: 1420–1428.
115. Karabinos, A., E. Schulze, J. Schunemann, D. A. Parry, and K. Weber, 2003 In vivo and in vitro evidence that the four essential intermediate filament (IF) proteins A1, A2, A3 and B1 of the nematode Caenorhabditis elegans form an obligate heteropolymeric IF system. J. Mol. Biol. 333: 307–319.
116. Katidou, M., N. Tavernarakis, and D. Karagogeos, 2013 The contactin RIG-6 mediates neuronal and non-neuronal cell migration in Caenorhabditis elegans. Dev. Biol. 373: 184–195.
117. Kato, Y., 2011 The multiple roles of Notch signaling during left-right patterning. Cell. Mol. Life Sci. 68: 2555–2567.
118. Kean, M. J., D. F. Ceccarelli, M. Goudreault, M. Sanches, S. Tate et al., 2011 Structure-function analysis of core STRIPAK proteins: a signaling complex implicated in Golgi polarization. J. Biol. Chem. 286: 25065–25075.
119. Khan, L. A., H. Zhang, N. Abraham, L. Sun, J. T. Fleming et al., 2013 Intracellular lumen extension requires ERM-1-dependent apical membrane expansion and AQP-8-mediated flux. Nat. Cell Biol. 15: 143–156.
120. King, L. S., D. Kozono, and P. Agre, 2004 From structure to disease: the evolving tale of aquaporin biology. Nat. Rev. Mol. Cell Biol. 5: 687–698.
121. Knight, A. J., N. M. Johnson, and C. A. Behm, 2012 VHA-19 is essential in Caenorhabditis elegans oocytes for embryogenesis and is involved in trafficking in oocytes. PLoS One 7: e40317.
122. Kolotuev, I., Y. Schwab, and M. Labouesse, 2010 A precise and rapid mapping protocol for correlative light and electron microscopy of small invertebrate organisms. Biol. Cell 102: 121–132.
123. Kolotuev, I., V. Hyenne, Y. Schwab, D. Rodriguez, and M. Labouesse, 2013 A pathway for unicellular tube extension depending on the lymphatic vessel determinant Prox1 and on osmoregulation. Nat. Cell Biol. 15: 157–168.
124. Koppen, M., J. S. Simske, P. A. Sims, B. L. Firestein, D. H. Hall et al., 2001 Cooperative regulation of AJM-1 controls junctional integrity in Caenorhabditis elegans epithelia. Nat. Cell Biol. 3: 983–991.
125. Kostrouchova, M., M. Krause, Z. Kostrouch, and J. E. Rall, 2001 Nuclear hormone receptor CHR3 is a critical regulator of all four larval molts of the nematode Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 98: 7360–7365.
126. Kouns, N. A., J. Nakielna, F. Behensky, M. W. Krause, Z. Kostrouch et al., 2011 NHR-23-dependent collagen and hedgehog-related genes required for molting. Biochem. Biophys. Res. Commun. 413: 515–520.
127. Kurogane, Y., M. Miyata, Y. Kubo, Y. Nagamatsu, R. K. Kundu et al., 2012 FGD5 mediates proangiogenic action of vascular endothelial growth factor in human vascular endothelial cells. Arterioscler. Thromb. Vasc. Biol. 32: 988–996.
128. Kwon, T.H., J. Nielsen, H.B. Moller, R.A. Fenton, S. Nielsen et al., 2009 Aquaporins in the kidney. Handb. Exp. Pharmacol. 95–132.
129. Labouesse, M., S. Sookhareea, and H. R. Horvitz, 1994 The Caenorhabditis elegans gene lin-26 is required to specify the fates of hypodermal cells and encodes a presumptive zinc-finger transcription factor. Development 120: 2359–2368.
130. Labouesse, M., E. Hartwieg, and H. R. Horvitz, 1996 The Caenorhabditis elegans LIN-26 protein is required to specify and/or maintain all non-neuronal ectodermal cell fates. Development 122: 2579–2588.
131. Lambie, E. J., and J. Kimble, 1991 Two homologous regulatory genes, lin-12 and glp-1, have overlapping functions. Development 112: 231–240.
132. Lanningham-Foster, L., C. L. Green, B. Langkamp-Henken, B. A. Davis, K. T. Nguyen et al., 2002 Overexpression of CRIP in transgenic mice alters cytokine patterns and the immune response. Am. J. Physiol. Endocrinol. Metab. 282: E1197–E1203.
133. Lant, B., B. Yu, M. Goudreault, D. Holmyard, J. D. Knight et al., 2015 CCM-3/STRIPAK promotes seamless tube extension through endocytic recycling. Nat. Commun. 6: 6449.
134. Lassiter, R. N., M. R. Stark, T. Zhao, and C. J. Zhou, 2014 Signaling mechanisms controlling cranial placode neurogenesis and delamination. Dev. Biol. 389: 39–49.
135. Lee, D. L., 1970 The fine structure of the excretory system in adult Nippostrongylus brasiliensis (Nematoda) and a suggested function for the ‘excretory glands’. Tissue Cell 2: 225–231.
136. Lee, S. K., W. Li, S. E. Ryu, T. Rhim, and J. Ahnn, 2010 Vacuolar (H+)-ATPases in Caenorhabditis elegans: What can we learn about giant H+ pumps from tiny worms? Biochim. Biophys. Acta 1797: 1687–1695.
137. Lenard, A., E. Ellertsdottir, L. Herwig, A. Krudewig, L. Sauteur et al., 2013 In vivo analysis reveals a highly stereotypic morphoge-netic pathway of vascular anastomosis. Dev. Cell 25: 492–506.
138. Lenard, A., S. Daetwyler, C. Betz, E. Ellertsdottir, H. G. Belting et al., 2015 Endothelial cell self-fusion during vascular pruning. PLoS Biol. 13: e1002126.
139. Li, M., J. Jiang, and L. Yue, 2006 Functional characterization of homo- and heteromeric channel kinases TRPM6 and TRPM7. J. Gen. Physiol. 127: 525–537.
140. Liegeois, S., A. Benedetto, J. M. Garnier, Y. Schwab, and M. Labouesse, 2006 The V0-ATPase mediates apical secretion of exo-somes containing Hedgehog-related proteins in Caenorhabditis elegans. J. Cell Biol. 173: 949–961.
141. Liegeois, S., A. Benedetto, G. Michaux, G. Belliard, and M. Labouesse, 2007 Genes required for osmoregulation and apical secretion in Caenorhabditis elegans. Genetics 175: 709–724.
142. Lillehoj, E. P., K. Kato, W. Lu, and K. C. Kim, 2013 Cellular and molecular biology of airway mucins. Int. Rev. Cell Mol. Biol. 303: 139–202.
143. Littler, D. R., S. J. Harrop, S. C. Goodchild, J. M. Phang, A. V. Mynott et al., 2010 The enigma of the CLIC proteins: Ion channels, redox proteins, enzymes, scaffolding proteins? FEBS Lett. 584: 2093–2101.
144. Liu, J., and W. Guo, 2012 The exocyst complex in exocytosis and cell migration. Protoplasma 249: 587–597.
145. Lubarsky, B., and M. A. Krasnow, 2003 Tube morphogenesis: making and shaping biological tubes. Cell 112: 19–28.
146. Lundquist, E. A., P. W. Reddien, E. Hartwieg, H. R. Horvitz, and C. I. Bargmann, 2001 Three C. elegans Rac proteins and several alternative Rac regulators Control axon guidance, cell migration, and apoptotic cell phagocytosis. Development 128: 4475–4488.
147. Luschnig, S., T. Batz, K. Armbruster, and M. A. Krasnow, 2006 Serpentine and vermiform encode matrix proteins with chitin binding and deacetylation domains that limit tracheal tube length in Drosophila. Curr. Biol. 16: 186–194.
148. MacQueen, A. J., J. J. Baggett, N. Perumov, R. A. Bauer, T. Januszewski et al., 2005 ACT-5 is an essential Caenorhabditis elegans actin required for intestinal microvilli formation. Mol. Biol. Cell 16: 3247–3259.
149. Maggenti, A. R., 1962 The production of the gelatinous matrix and its taxonomic significance in Tylenchulus (Nematoda: Tylenchulinae). Proc. Helminthol. Soc. Wash. 29: 139–144.
150. Mah, A. K., K. R. Armstrong, D. S. Chew, J. S. Chu, D. K. Tu et al., 2007 Transcriptional regulation of AQP-8, a Caenorhabditis elegans aquaporin exclusively expressed in the excretory system, by the POU homeobox transcription factor CEH-6. J. Biol. Chem. 282: 28074–28086.
151. Mancuso, V. P., J. M. Parry, L. Storer, C. Poggioli, K. C. Nguyen et al., 2012 Extracellular leucine-rich repeat proteins are required to organize the apical extracellular matrix and maintain epithelial junction integrity in C. elegans. Development 139: 979–990.
152. Manser, J., and W. B. Wood, 1990 Mutations affecting embryonic cell migrations in Caenorhabditis elegans. Dev. Genet. 11: 49–64.
153. Marcus-Gueret, N., K. L. Schmidt, and E. G. Stringham, 2012 Distinct cell guidance pathways controlled by the Rac and Rho GEF domains of UNC-73/TRIO in Caenorhabditis elegans. Genetics 190: 129–142.
154. Maruyama, R., and D. J. Andrew, 2012 Drosophila as a model for epithelial tube formation. Dev. Dyn. 241: 119–135.
155. Mathis, S., B. Funalot, O. Boyer, C. Lacroix, P. Marcorelles et al., 2014 Neuropathologic characterization of INF2-related Charcot-Marie-Tooth disease: evidence for a Schwann cell actinopathy. J. Neuropathol. Exp. Neurol. 73: 223–233.
156. Mattingly, B. C., and M. Buechner, 2011 The FGD homologue EXC-5 regulates apical trafficking in C. elegans tubules. Dev. Biol. 359: 59–72.
157. McAllister, K. A., K. M. Grogg, D. W. Johnson, C. J. Gallione, M. A. Baldwin et al., 1994 Endoglin, a TGFb binding protein of endothelial cells, is the gene for hereditary haemorrhagic telangiectasia type 1. Nat. Genet. 8: 345–351.
158. McCormick, J. A., and D. H. Ellison, 2011 The WNKs: atypical protein kinases with pleiotropic actions. Physiol. Rev. 91: 177–219.
159. McShea, M. A., K. L. Schmidt, M. L. Dubuke, C. E. Baldiga, M. E. Sullender et al., 2013 Abelson interactor-1 (ABI-1) interacts with MRL adaptor protein MIG-10 and is required in guided cell migrations and process outgrowth in C. elegans. Dev. Biol. 373: 1–13.
160. Menezes, L. F., F. Zhou, A. D. Patterson, K. B. Piontek, K. W. Krausz et al., 2012 Network analysis of a Pkd1-mouse model of autosomal dominant polycystic kidney disease identifies HNF4a as a disease modifier. PLoS Genet. 8: e1003053.
161. Menoret, D., M. Santolini, I. Fernandes, R. Spokony, J. Zanet et al., 2013 Genome-wide analyses of Shavenbaby target genes reveals distinct features of enhancer organization. Genome Biol. 14: R86.
162. Merline, R., R. M. Schaefer, and L. Schaefer, 2009 The matricellular functions of small leucine-rich proteoglycans (SLRPs). J. Cell Commun. Signal. 3: 323–335.
163. Merris, M., W. G. Wadsworth, U. Khamrai, R. Bittman, D. J. Chitwood et al., 2003 Sterol effects and sites of sterol accumulation in Caenorhabditis elegans: Developmental requirement for 4a-methyl sterols. J. Lipid Res. 44: 172–181.
164. Metzstein, M. M., M. O. Hengartner, N. Tsung, R. E. Ellis, and H. R. Horvitz, 1996 Transcriptional regulator of programmed cell death encoded by Caenorhabditis elegans gene ces-2. Nature 382: 545–547.
165. Mohamed, A. M., and I. D. Chin-Sang, 2011 The C. elegans nck-1 gene encodes two isoforms and is required for neuronal guidance. Dev. Biol. 354: 55–66.
166. Moreno, Y., J. F. Nabhan, J. Solomon, C. D. Mackenzie, and T. G. Geary, 2010 Ivermectin disrupts the function of the excretory-secretory apparatus in microfilariae of Brugia malayi. Proc. Natl. Acad. Sci. USA 107: 20120–20125.
167. Moskowitz, I. P., and J. H. Rothman, 1996 Lin-12 and glp-1 are required zygotically for early embryonic cellular interactions and are regulated by maternal GLP-1 signaling in Caenorhabditis elegans. Development 122: 4105–4117.
168. Murray, J. I., T. J. Boyle, E. Preston, D. Vafeados, B. Mericle et al., 2012 Multidimensional regulation of gene expression in the C. elegans embryo. Genome Res. 22: 1282–1294.
169. Nakai, S., Y. Sugitani, H. Sato, S. Ito, Y. Miura et al., 2003 Crucial roles of Brn1 in distal tubule formation and function in mouse kidney. Development 130: 4751–4759.
170. Narang, H. K., 1972 The excretory system of nematodes: structure and ultrastructure of the excretory system of Panagrellus redivivus, Ditylenchus myceliophagus with some observations on D. dipsaci and Heterodera rostochiensis. Parasitology 64: 253–268.
171. Nedvetsky, P.I., G. Tamma, S. Beulshausen, G. Valenti, W. Rosenthal et al., 2009 Regulation of aquaporin-2 trafficking. Handb. Exp. Pharmacol. 133–157.
172. Nehrke, K., and J. E. Melvin, 2002 The NHX family of Na+-H+ exchangers in Caenorhabditis elegans. J. Biol. Chem. 277: 29036–29044.
173. Neisch, A. L., and R. G. Fehon, 2011 Ezrin, Radixin and Moesin: key regulators of membrane-cortex interactions and signaling. Curr. Opin. Cell Biol. 23: 377–382.
174. Nelson, F. K., and D. L. Riddle, 1984 Functional study of the Caenorhabditis elegans secretory-excretory system using laser microsurgery. J. Exp. Zool. 231: 45–56.
175. Nelson, F. K., P. S. Albert, and D. S. Riddle, 1983 Fine structure of the Caenorhabditis elegans secretory-excretory system. J. Ultrastruct. Res. 82: 156–171.
176. Neves, A., and J. R. Priess, 2005 The REF-1 family of bHLH transcription factors pattern C. elegans embryos through Notch-dependent and Notch-independent pathways. Dev. Cell 8: 867–879.
177. Noble, L. M., A. S. Chang, D. McNelis, M. Kramer, M. Yen et al., 2015 Natural variation in plep-1 causes male-male copulatory behavior in C. elegans. Curr. Biol. 25: 2730–2737.
178. Oka, T., R. Yamamoto, and M. Futai, 1997 Three vha genes encode proteolipids of Caenorhabditis elegans vacuolar-type ATPase. Gene structures and preferential expression in an H-shaped excretory cell and rectal cells. J. Biol. Chem. 272: 24387–24392.
179. Olson, M. F., N. G. Pasteris, J. L. Gorski, and A. Hall, 1996 Faciogenital dysplasia protein (FGD1) and Vav, two related proteins required for normal embryonic development, are upstream regulators of Rho GTPases. Curr. Biol. 6: 1628–1633.
180. Oosterveen, T., D. Y. Coudreuse, P. T. Yang, E. Fraser, J. Bergsma et al., 2007 Two functionally distinct Axin-like proteins regulate canonical Wnt signaling in C. elegans. Dev. Biol. 308: 438–448.
181. Page, A. P., A. J. Hamilton, and R. M. Maizels, 1992a Toxocara canis: monoclonal antibodies to carbohydrate epitopes of secreted (TES) antigens localize to different secretion-related structures in infective larvae. Exp. Parasitol. 75: 56–71.
182. Page, A. P., W. Rudin, E. Fluri, M. L. Blaxter, and R. M. Maizels, 1992b Toxocara canis: a labile antigenic surface coat overlying the epicuticle of infective larvae. Exp. Parasitol. 75: 72–86.
183. Paragas, N., A. Qiu, M. Hollmen, T. L. Nickolas, P. Devarajan et al., 2012 NGAL-Siderocalin in kidney disease. Biochim. Biophys. Acta 1823: 1451–1458.
184. Park, S. Y., J. S. Yang, A. B. Schmider, R. J. Soberman, and V. W. Hsu, 2015 Coordinated regulation of bidirectional COPI transport at the Golgi by CDC42. Nature 521: 529–532.
185. Parry, J. M., and M. V. Sundaram, 2014 A non-cell-autonomous role for Ras signaling in C. elegans neuroblast delamination. Development 141: 4279–4284.
186. Pasti, G., and M. Labouesse, 2014 Epithelial junctions, cytoskeleton, and polarity. WormBook 4: 1–35.
187. Patel, N., D. Thierry-Mieg, and J. R. Mancillas, 1993 Cloning by insertional mutagenesis of a cDNA encoding Caenorhabditis elegans kinesin heavy chain. Proc. Natl. Acad. Sci. USA 90: 9181– 9185.
188. Perens, E. A., and S. Shaham, 2005 C. elegans daf-6 encodes a patched-related protein required for lumen formation. Dev. Cell 8: 893–906.
189. Perry, R. N., 1977 The water dynamics of stages of Ditylenchus dipsaci and D. myceliophagus during desiccation and rehydration. Parasitology 75: 45–70.
190. Petkova, D. S., C. Viret, and M. Faure, 2012 IRGM in autophagy and viral infections. Front. Immunol. 3: 426.
191. Plattner, H., 2015 The contractile vacuole complex of protists: new cues to function and biogenesis. Crit. Rev. Microbiol. 41: 218–227.
192. Plaza, S., H. Chanut-Delalande, I. Fernandes, P. M. Wassarman, and F. Payre, 2010 From A to Z: apical structures and zona pellucida-domain proteins. Trends Cell Biol. 20: 524–532.
193. Podbilewicz, B., and J. G. White, 1994 Cell fusions in the developing epithelia of C. elegans. Dev. Biol. 161: 408–424.
194. Polanska, U. M., E. Edwards, D. G. Fernig, and T. K. Kinnunen, 2011 The cooperation of FGF receptor and Klotho is involved in excretory canal development and regulation of metabolic homeostasis in Caenorhabditis elegans. J. Biol. Chem. 286: 5657–5666.
195. Praitis, V., E. Ciccone, and J. Austin, 2005 SMA-1 spectrin has essential roles in epithelial cell sheet morphogenesis in C. elegans. Dev. Biol. 283: 157–170.
196. Premachandran, D., N. Von Mende, R. S. Hussey, and M. A. McClure, 1988 A method for staining nematode secretions and structures. J. Nematol. 20: 70–78.
197. Priess, J. R., 2005 Notch signaling in the C. elegans embryo. WormBook 25: 1–16.
198. Rampoldi, L., F. Scolari, A. Amoroso, G. Ghiggeri, and O. Devuyst, 2011 The rediscovery of uromodulin (Tamm-Horsfall protein): from tubulointerstitial nephropathy to chronic kidney disease. Kidney Int. 80: 338–347.
199. Rasmussen, J. P., K. English, J. R. Tenlen, and J. R. Priess, 2008 Notch signaling and morphogenesis of single-cell tubes in the C. elegans digestive tract. Dev. Cell 14: 559–569.
200. Ribeiro, C., M. Neumann, and M. Affolter, 2004 Genetic control of cell intercalation during tracheal morphogenesis in Drosophila. Curr. Biol. 14: 2197–2207.
201. Roca, H., J. Hernandez, S. Weidner, R. C. McEachin, D. Fuller et al., 2013 Transcription factors OVOL1 and OVOL2 induce the mesenchymal to epithelial transition in human cancer. PLoS One 8: e76773.
202. Ross, B., A. Leaf, P. Silva, and F. H. Epstein, 1974 Na-K-ATPase in sodium transport by the perfused rat kidney. Am. J. Physiol. 226: 624–629.
203. Rumsey, D. M., and D. A. Mallory, 2013 GIL: a blood group system review. Immunohematology 29: 141–144.
204. Sacharidou, A., A. N. Stratman, and G. E. Davis, 2012 Molecular mechanisms controlling vascular lumen formation in three-dimensional extracellular matrices. Cells Tissues Organs 195: 122–143.
205. Salkoff, L., A. Butler, G. Fawcett, M. Kunkel, C. McArdle et al., 2001 Evolution tunes the excitability of individual neurons. Neuroscience 103: 853–859.
206. Samakovlis, C., N. Hacohen, G. Manning, D. C. Sutherland, K. Guillemin et al., 1996 Development of the Drosophila tracheal system occurs by a series of morphologically distinct but genetically coupled branching events. Development 122: 1395–1407.
207. Sapir, A., J. Choi, E. Leikina, O. Avinoam, C. Valansi et al., 2007 AFF-1, a FOS-1-regulated fusogen, mediates fusion of the anchor cell in C. elegans. Dev. Cell 12: 683–698.
208. Sawa, H., and H. C. Korswagen, 2013 Wnt signaling in C. elegans. WormBook 9: 1–30.
209. Schmidt, K. L., N. Marcus-Gueret, A. Adeleye, J. Webber, D. Baillie et al., 2009 The cell migration molecule UNC-53/NAV2 is linked to the ARP2/3 complex by ABI-1. Development 136: 563–574.
210. Schneider, A., 1866 Monographie der Nematoden, G. Reiner, Berlin.
211. Schottenfeld, J., Y. Song, and A. S. Ghabrial, 2010 Tube continued: morphogenesis of the Drosophila tracheal system. Curr. Opin. Cell Biol. 22: 633–639.
212. Schriever, A. M., T. Friedrich, M. Pusch, and T. J. Jentsch, 1999 CLC chloride channels in Caenorhabditis elegans. J. Biol. Chem. 274: 34238–34244.
213. Shaham, S., 2015 Glial development and function in the nervous system of Caenorhabditis elegans. Cold Spring Harb. Perspect. Biol. 7: a020578.
214. Shaye, D. D., and I. Greenwald, 2015 The disease-associated formin INF2/EXC-6 organizes lumen and cell outgrowth during tubulogenesis by regulating F-actin and microtubule cytoskeletons. Dev. Cell 32: 743–755.
215. Sherman, T., M. N. Chernova, J. S. Clark, L. Jiang, S. L. Alper et al., 2005 The abts and sulp families of anion transporters from Caenorhabditis elegans. Am. J. Physiol. Cell Physiol. 289: C341–C351.
216. Siekmann, A. F., M. Affolter, and H. G. Belting, 2013 The tip cell concept 10 years after: new players tune in for a common theme. Exp. Cell Res. 319: 1255–1263.
217. Sigurbjornsdottir, S., R. Mathew, and M. Leptin, 2014 Molecular mechanisms of de novo lumen formation. Nat. Rev. Mol. Cell Biol. 15: 665–676.
218. Simone, L. E., and J. D. Keene, 2013 Mechanisms coordinating ELAV/Hu mRNA regulons. Curr. Opin. Genet. Dev. 23: 35–43.
219. Simons, M., and J. Trotter, 2007 Wrapping it up: the cell biology of myelination. Curr. Opin. Neurobiol. 17: 533–540.
220. Singh, R. N., and J. E. Sulston, 1978 Some observations on moulting in Cænorhabditis elegans. Nematologica 24: 63–71.
221. Soleimani, M., 2015 The multiple roles of pendrin in the kidney. Nephrol. Dial. Transplant. 30: 1257–1266.
222. Song, Y., M. Eng, and A. S. Ghabrial, 2013 Focal defects in single-celled tubes mutant for cerebral cavernous malformation 3, GCKIII, or NSF2. Dev. Cell 25: 507–519.
223. Spencer, W. C., G. Zeller, J. D. Watson, S. R. Henz, K. L. Watkins et al., 2011 A spatial and temporal map of C. elegans gene expression. Genome Res. 21: 325–341.
224. Srivastava, A., 2014 Progressive familial intrahepatic cholestasis. J. Clin. Exp. Hepatol. 4: 25–36.
225. Stephenson, W., 1942 On the culturing of Rhabditis terrestris n.sp. Parasitology 34: 246–252.
226. Stone, C. E., D. H. Hall, and M. V. Sundaram, 2009 Lipocalin signaling controls unicellular tube development in the Caenorhabditis elegans excretory system. Dev. Biol. 329: 201–211.
227. Stringham, E., N. Pujol, J. Vandekerckhove, and T. Bogaert, 2002 unc-53 controls longitudinal migration in C. elegans. Development 129: 3367–3379.
228. Sulston, J. E., and H. R. Horvitz, 1977 Post-embryonic cell lineages of the nematode, Cænorhabditis elegans. Dev. Biol. 56: 110–156.
229. Sulston, J. E., E. Schierenberg, J. G. White, and J. N. Thomson, 1983 The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol. 100: 64–119.
230. Sumida, G. M., and S. Yamada, 2013 Self-contact elimination by membrane fusion. Proc. Natl. Acad. Sci. USA 110: 18958–18963.
231. Sumida, G. M., and S. Yamada, 2015 Rho GTPases and the downstream effectors actin-related protein 2/3 (Arp2/3) complex and myosin II induce membrane fusion at self-contacts. J. Biol. Chem. 290: 3238–3247.
232. Sun, H., and R. Kawaguchi, 2011 The membrane receptor for plasma retinol-binding protein, a new type of cell-surface receptor. Int. Rev. Cell Mol. Biol. 288: 1–41.
233. Sundaram, M. V., 2005 The love-hate relationship between Ras and Notch. Genes Dev. 19: 1825–1839.
234. Suzuki, N., M. Buechner, K. Nishiwaki, D. H. Hall, H. Nakanishi et al., 2001 A putative GDP-GTP exchange factor is required for development of the excretory cell in Caenorhabditis elegans. EMBO Rep. 2: 530–535.
235. Suzuki, T., T. Toyohara, Y. Akiyama, Y. Takeuchi, E. Mishima et al., 2011 Transcriptional regulation of organic anion transporting polypeptide SLCO4C1 as a new therapeutic modality to prevent chronic kidney disease. J. Pharm. Sci. 100: 3696–3707.
236. Svendsen, P. C., and J. D. McGhee, 1995 The C. elegans neuronally expressed homeobox gene ceh-10 is closely related to genes expressed in the vertebrate eye. Development 121: 1253–1262.
237. Takano, K., D. Liu, P. Tarpey, E. Gallant, A. Lam et al., 2012 An X-linked channelopathy with cardiomegaly due to a CLIC2 mutation enhancing ryanodine receptor channel activity. Hum. Mol. Genet. 21: 4497–4507.
238. Tamura, A., S. Kikuchi, M. Hata, T. Katsuno, T. Matsui et al., 2005 Achlorhydria by ezrin knockdown: defects in the formation/expansion of apical canaliculi in gastric parietal cells. J. Cell Biol. 169: 21–28.
239. Technau, G. M., C. Berger, and R. Urbach, 2006 Generation of cell diversity and segmental pattern in the embryonic central nervous system of Drosophila. Dev. Dyn. 235: 861–869.
240. Teramoto, T., L. A. Sternick, E. Kage-Nakadai, S. Sajjadi, J. Siembida et al., 2010 Magnesium excretion in C. elegans requires the activity of the GTL-2 TRPM channel. PLoS One 5: e9589.
241. Tong, X., and M. Buechner, 2008 CRIP homologues maintain apical cytoskeleton to regulate tubule size in C. elegans. Dev. Biol. 317: 225–233.
242. Tonning, A., J. Hemphala, E. Tang, U. Nannmark, C. Samakovlis et al., 2005 A transient luminal chitinous matrix is required to model epithelial tube diameter in the Drosophila trachea. Dev. Cell 9: 423–430.
243. Tukachinsky, H., R. P. Kuzmickas, C. Y. Jao, J. Liu, and A. Salic, 2012 Dispatched and scube mediate the efficient secretion of the cholesterol-modified hedgehog ligand. Cell Reports 2: 308–320.
244. Turpeenniemi, T. A., and H. Hyvarinen, 1996 Structure and role of the Renette cell and caudal glands in the nematode Sphaerolaimus gracilis (Monhysterida). J. Nematol. 28: 318–327.
245. Ulmasov, B., J. Bruno, N. Gordon, M. E. Hartnett, and J. C. Edwards, 2009 Chloride intracellular channel protein-4 functions in angiogenesis by supporting acidification of vacuoles along the intracellular tubulogenic pathway. Am. J. Pathol. 174: 1084–1096.
246. Vallat, J. M., S. Mathis, and B. Funalot, 2013 The various Charcot Marie-Tooth diseases. Curr. Opin. Neurol. 26: 473–480.
247. van de Velde, M. C., and A. Coomans, 1987 Ultrastructure of the excretory system of the marine nematode Monhystera disjuncta. Tissue Cell 19: 713–725.
248. Walton, T., E. Preston, G. Nair, A. L. Zacharias, A. Raj et al., 2015 The Bicoid class homeodomain factors ceh-36/OTX and unc-30/PITX cooperate in C. elegans embryonic progenitor cells to regulate robust development. PLoS Genet. 11: e1005003.
249. Wang, B. B., M. M. Muller-Immergluck, J. Austin, N. T. Robinson, A. Chisholm et al., 1993 A homeotic gene cluster patterns the anteroposterior body axis of C. elegans. Cell 74: 29–42.
250. Wang, X., and H. M. Chamberlin, 2002 Multiple regulatory changes contribute to the evolution of the Caenorhabditis lin-48 ovo gene. Genes Dev. 16: 2345–2349.
251. Wang, X., and H. M. Chamberlin, 2004 Evolutionary innovation of the excretory system in Caenorhabditis elegans. Nat. Genet. 36: 231–232.
252. Wang, X., H. Jia, and H. M. Chamberlin, 2006 The bZip proteins CES-2 and ATF-2 alter the timing of transcription for a cell-specific target gene in C. elegans. Dev. Biol. 289: 456–465.
253. Wang, X., C. W. Piccolo, B. M. Cohen, and E. A. Buttner, 2014a Transient receptor potential melastatin (TRPM) channels mediate clozapine-induced phenotypes in Caenorhabditis elegans. J. Neurogenet. 28: 86–97.
254. Wang, Z., Q. Chi, and D. R. Sherwood, 2014b MIG-10 (lamellipodin) has netrin-independent functions and is a FOS-1A transcriptional target during anchor cell invasion in C. elegans. Development 141: 1342–1353.
255. Wharton, D. A., and R. I. Sommerville, 1984 The structure of excretory system of the infective larva of Haemonchus contortus. Int. J. Parasitol. 14: 591–600.
256. Wharton, D. A., C. M. Preston, J. Barrett, and R. N. Perry, 1988 Changes in cuticular permeability associated with recovery from anhydrobiosis in the plant parasitic nematode, Ditylenchus dipsaci. Parasitology 97: 317–330.
257. White, J. G., E. Southgate, J. N. Thomson, and S. Brenner, 1986 The structure of the nervous system of the nematode Caenorhabditis elegans. Philos. Trans. R. Soc. Lond. B Biol. Sci. 314: 1–340.
258. Wigle, J. T., and G. Oliver, 1999 Prox1 function is required for the development of the murine lymphatic system. Cell 98: 769–778.
259. Wolff, J. R., and T. Bar, 1972 ‘Seamless’ endothelia in brain capillaries during development of the rat’s cerebral cortex. Brain Res. 41: 17–24.
260. Woo, W. M., A. Goncharov, Y. Jin, and A. D. Chisholm, 2004 Intermediate filaments are required for C. elegans epidermal elongation. Dev. Biol. 267: 216–229.
261. Wright, D. J., 2004 Osmoregulatory and excretory behaviour, pp. 177–196 in Nematode Behaviour, edited by R. Gaugler and A. L. Bilgrami. CABI Publishing, Wallingford, UK.
262. Wright, D. J., and D. R. Newall, 1976 Nitrogen excretion, osmotic and ionic regulation in nematodes, pp. 163–210 in The Organisation of Nematodes, edited by N. A. Croll, Academic Press, New York.
263. Yanowitz, J. L., M. A. Shakir, E. Hedgecock, H. Hutter, A. Z. Fire et al., 2004 UNC-39, the C. elegans homolog of the human myotonic dystrophy-associated homeodomain protein Six5, regulates cell motility and differentiation. Dev. Biol. 272: 389–402.
264. Yochem, J., M. Sundaram, and M. Han, 1997 Ras is required for a limited number of cell fates and not for general proliferation in Caenorhabditis elegans. Mol. Cell. Biol. 17: 2716–2722.
265. Yoshida, S., H. Yamamoto, T. Tetsui, Y. Kobayakawa, R. Hatano et al., 2016 Effects of ezrin knockdown on the structure of gastric glandular epithelia. J. Physiol. Sci. 66: 53–65.
266. Yoshimura, S., J. I. Murray, Y. Lu, R. H. Waterston, and S. Shaham, 2008 mls-2 and vab-3 control glia development, hlh-17/Olig expression and glia-dependent neurite extension in C. elegans. Development 135: 2263–2275.
267. Yu, J. A., D. Castranova, V. N. Pham, and B. M. Weinstein, 2015 Single-cell analysis of endothelial morphogenesis in vivo. Development 142: 2951–2961.
268. Zacharias, A. L., T. Walton, E. Preston, and J. I. Murray, 2015 Quantitative differences in nuclear b-catenin and TCF pattern embryonic cells in C. elegans. PLoS Genet. 11: e1005585.
269. Zhao, Z., L. Fang, N. Chen, R. C. Johnsen, L. Stein et al., 2005 Distinct regulatory elements mediate similar expression patterns in the excretory cell of Caenorhabditis elegans. J. Biol. Chem. 280: 38787–38794.
270. Zheng, Y., M. K. Jung, and B. R. Oakley, 1991 Gamma-tubulin is present in Drosophila melanogaster and Homo sapiens and is associated with the centrosome. Cell 65: 817–823.
271. Zuryn, S., T. Daniele, and S. Jarriault, 2012 Direct cellular reprogramming in Caenorhabditis elegans: facts, models, and promises for regenerative medicine. Wiley Interdiscip. Rev. Dev. Biol. 1: 138–152.