Lipocalin signaling controls unicellular tube development in the Caenorhabditis elegans excretory system

Developmental Biology

Volumn 329, Issue 2, 2009, Pages 201-211

  Stone, Craig E ^a   Hall, David H ^b   Sundaram, Meera V ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

Excretory; Intercellular signaling; Lipocalin; lpr 1; Tubulogenesis

Indexed keywords

LIPOCALIN; SIGNAL PEPTIDE;

APICAL MEMBRANE; ARTICLE; CAENORHABDITIS ELEGANS; CAPILLARY PROLIFERATION; CELL FUNCTION; CONTROLLED STUDY; GENETIC MODEL; LIPOPHILICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN SECRETION; RENAL SYSTEM PARAMETERS;

CAENORHABDITIS ELEGANS;

EID: 67349242376     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2009.02.030     Document Type: Article

References (66)

1. Andreeva A., Howorth D., Chandonia J.M., Brenner S.E., Hubbard T.J., Chothia C., and Murzin A.G. Data growth and its impact on the SCOP database: new developments. Nucleic Acids Res. 36 (2008) D419-D425
2. Bar T., Guldner F.H., and Wolff J.R. "Seamless" endothelial cells of blood capillaries. Cell & Tissue Res. 235 (1984) 99-106
3. Berger T., Togawa A., Duncan G.S., Elia A.J., You-Ten A., Wakeham A., Fong H.E., Cheung C.C., and Mak T.W. Lipocalin 2-deficient mice exhibit increased sensitivity to Escherichia coli infection but not to ischemia-reperfusion injury. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 1834-1839
4. Berry K.L., Bulow H.E., Hall D.H., and Hobert O. A C. elegans CLIC-like protein required for intracellular tube formation and maintenance. Science 302 (2003) 2134-2137
5. Blaner W.S. STRA6, a cell-surface receptor for retinol-binding protein: the plot thickens. Cell Metabolism 5 (2007) 164-166
6. Blum Y., Belting H.G., Ellertsdottir E., Herwig L., Luders F., and Affolter M. Complex cell rearrangements during intersegmental vessel sprouting and vessel fusion in the zebrafish embryo. Dev. Biol. 316 (2008) 312-322
7. Buechner M. Tubes and the single C. elegans excretory cell. Trends Cell Biol. 12 (2002) 479-484
8. Buechner M., Hall D.H., Bhatt H., and Hedgecock E.M. Cystic canal mutants in Caenorhabditis elegans are defective in the apical membrane domain of the renal (excretory) cell. Dev. Biol. 214 (1999) 227-241
9. Chamero P., Marton T.F., Logan D.W., Flanagan K., Cruz J.R., Saghatelian A., Cravatt B.F., and Stowers L. Identification of protein pheromones that promote aggressive behaviour. Nature 450 (2007) 899-902
10. Davis G.E., and Camarillo C.W. An alpha 2 beta 1 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 (1996) 39-51
11. Devireddy L.R., Gazin C., Zhu X., and Green M.R. A cell-surface receptor for lipocalin 24p3 selectively mediates apoptosis and iron uptake. Cell 123 (2005) 1293-1305
12. Flo T.H., Smith K.D., Sato S., Rodriguez D.J., Holmes M.A., Strong R.K., Akira S., and Aderem A. Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron. Nature 432 (2004) 917-921
13. Flower D.R. Beyond the superfamily: the lipocalin receptors. Biochim. Biophys. Acta 1482 (2000) 327-336
14. Flower D.R., North A.C., and Attwood T.K. Structure and sequence relationships in the lipocalins and related proteins. Protein Sci. 2 (1993) 753-761
15. Flower D.R., North A.C., and Sansom C.E. The lipocalin protein family: structural and sequence overview. Biochim. Biophys. Acta 1482 (2000) 9-24
16. Folkman J., and Haudenschild C. Angiogenesis by capillary endothelial cells in culture. Trans. Ophthalmol. Soc. U.K. 100 (1980) 346-353
17. Forrester W.C., Perens E., Zallen J.A., and Garriga G. Identification of Caenorhabditis elegans genes required for neuronal differentiation and migration. Genetics 148 (1998) 151-165
18. Fujita M., Hawkinson D., King K.V., Hall D.H., Sakamoto H., and Buechner M. The role of the ELAV homologue EXC-7 in the development of the Caenorhabditis elegans excretory canals. Dev. Biol. 256 (2003) 290-301
19. Ganfornina M.D., Gutierrez G., Bastiani M., and Sanchez D. A phylogenetic analysis of the lipocalin protein family. Mol. Biol. Evol. 17 (2000) 114-126
20. Gilleard J.S., Barry J.D., and Johnstone I.L. cis regulatory requirements for hypodermal cell-specific expression of the Caenorhabditis elegans cuticle collagen dpy-7. Mol. Cell Biol. 17 (1997) 2301-2311
21. Gobel V., Barrett P.L., Hall D.H., and Fleming J.T. Lumen morphogenesis in C. elegans requires the membrane-cytoskeleton linker erm-1. Dev. Cell 6 (2004) 865-873
22. Goodman A.B. Retinoid receptors, transporters, and metabolizers as therapeutic targets in late onset Alzheimer disease. J. Cell. Physiol. 209 (2006) 598-603
23. Graham P.L., Johnson J.J., Wang S., Sibley M.H., Gupta M.C., and Kramer J.M. Type IV collagen is detectable in most, but not all, basement membranes of Caenorhabditis elegans and assembles on tissues that do not express it. J. Cell Biol. 137 (1997) 1172-1183
24. Gwira J.A., Wei F., Ishibe S., Ueland J.M., Barasch J., and Cantley L.G. Expression of neutrophil gelatinase-associated lipocalin regulates epithelial morphogenesis in vitro. J. Biol. Chem. 280 (2005) 7875-7882
25. Hulo N., Bairoch A., Bulliard V., Cerutti L., Cuche B.A., de Castro E., Lachaize C., Langendijk-Genevaux P.S., and Sigrist C.J. The 20 years of PROSITE. Nucleic Acids Res. 36 (2008) D245-D249
26. Johnson A.D., Fitzsimmons D., Hagman J., and Chamberlin H.M. EGL-38 Pax regulates the ovo-related gene lin-48 during Caenorhabditis elegans organ development. Development 128 (2001) 2857-2865
27. Kamath R.S., Fraser A.G., Dong Y., Poulin G., Durbin R., Gotta M., Kanapin A., Le Bot N., Moreno S., Sohrmann M., Welchman D.P., Zipperlen P., and Ahringer J. Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421 (2003) 231-237
28. Kamei M., Saunders W.B., Bayless K.J., Dye L., Davis G.E., and Weinstein B.M. Endothelial tubes assemble from intracellular vacuoles in vivo. Nature 442 (2006) 453-456
29. Kawaguchi R., Yu J., Honda J., Hu J., Whitelegge J., Ping P., Wiita P., Bok D., and Sun H. A membrane receptor for retinol binding protein mediates cellular uptake of vitamin A. Science 315 (2007) 820-825
30. Koppen M., Simske J.S., Sims P.A., Firestein B.L., Hall D.H., Radice A.D., Rongo C., and Hardin J.D. Cooperative regulation of AJM-1 controls junctional integrity in Caenorhabditis elegans epithelia. Nature Cell Biol. 3 (2001) 983-991
31. Liegeois S., Benedetto A., Michaux G., Belliard G., and Labouesse M. Genes required for osmoregulation and apical secretion in Caenorhabditis elegans. Genetics 175 (2007) 709-724
32. Lubarsky B., and Krasnow M.A. Tube morphogenesis: making and shaping biological tubes. Cell 112 (2003) 19-28
33. Mello C., and Fire A. DNA transformation. Methods Cell Biol. 48 (1995) 451-482
34. Michaux G., Gansmuller A., Hindelang C., and Labouesse M. CHE-14, a protein with a sterol-sensing domain, is required for apical sorting in C. elegans ectodermal epithelial cells. Curr. Biol. 10 (2000) 1098-1107
35. Mishra J., Dent C., Tarabishi R., Mitsnefes M.M., Ma Q., Kelly C., Ruff S.M., Zahedi K., Shao M., Bean J., Mori K., Barasch J., and Devarajan P. Neutrophil gelatinase-associated lipocalin (NGAL) as a biomarker for acute renal injury after cardiac surgery. Lancet 365 (2005) 1231-1238
36. Mishra J., Ma Q., Prada A., Mitsnefes M., Zahedi K., Yang J., Barasch J., and Devarajan P. Identification of neutrophil gelatinase-associated lipocalin as a novel early urinary biomarker for ischemic renal injury. J. Am. Soc. Nephrol. 14 (2003) 2534-2543
37. Myers T.R., and Greenwald I. lin-35 Rb acts in the major hypodermis to oppose ras-mediated vulval induction in C. elegans. Dev. Cell 8 (2005) 117-123
38. Nangaku M., and Fujita T. Activation of the renin-angiotensin system and chronic hypoxia of the kidney. Hypertens. Res. 31 (2008) 175-184
39. Nelson F.K., Albert P.S., and Riddle D.L. Fine structure of the C. elegans secretory-excretory system. J. Ultrastruct. Res. 82 (1983) 156-171
40. Nelson F.K., and Riddle D.L. Functional study of the C. elegans secretory-excretory system using laser microsurgery. J. Exptl. Zool. 231 (1984) 45-56
41. Oka T., Yamamoto R., and Futai M. 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 (1997) 24387-24392
42. Okkema P.G., Harrison S.W., Plunger V., Aryana A., and Fire A. Sequence requirements for myosin gene expression and regulation in Caenorhabditis elegans. Genetics 135 (1993) 385-404
43. Perens E.A., and Shaham S. C. elegans daf-6 encodes a patched-related protein required for lumen formation. Dev. Cell 8 (2005) 893-906
44. Perkins L.A., Hedgecock E.M., Thomson J.N., and Culotti J.G. Mutant sensory cilia in the nematode Caenorhabditis elegans. Dev. Biol. 117 (1986) 456-487
45. Pulak R., and Anderson P. mRNA surveillance by the Caenorhabditis elegans smg genes. Genes Dev. 7 (1993) 1885-1897
46. Quadro L., Blaner W.S., Salchow D.J., Vogel S., Piantedosi R., Gouras P., Freeman S., Cosma M.P., Colantuoni V., and Gottesman M.E. Impaired retinal function and vitamin A availability in mice lacking retinol-binding protein. EMBO J. 18 (1999) 4633-4644
47. Rasmussen J.P., English K., Tenlen J.R., and Priess J.R. Notch signaling and morphogenesis of single-cell tubes in the C. elegans digestive tract. Dev. Cell 14 (2008) 559-569
48. Redondo C., Burke B.J., and Findlay J.B. The retinol-binding protein system: a potential paradigm for steroid-binding globulins?. Horm. Metab. Res. 38 (2006) 269-278
49. Ribeiro C., Neumann M., and Affolter M. Genetic control of cell intercalation during tracheal morphogenesis in Drosophila. Curr. Biol. 14 (2004) 2197-2207
50. Rost B., Yachdav G., and Liu J. The PredictProtein server. Nucleic Acids Res. 32 (2004) W321-W326
51. Samakovlis C., Hacohen N., Manning G., Sutherland D.C., Guillemin K., and Krasnow M.A. Development of the Drosophila tracheal system occurs by a series of morphologically distinct but genetically coupled branching events. Development 122 (1996) 1395-1407
52. Sanchez D., Lopez-Arias B., Torroja L., Canal I., Wang X., Bastiani M.J., and Ganfornina M.D. Loss of glial lazarillo, a homolog of apolipoprotein D, reduces lifespan and stress resistance in Drosophila. Curr. Biol. 16 (2006) 680-686
53. Sapir A., Choi J., Leikina E., Avinoam O., Valansi C., Chernomordik L.V., Newman A.P., and Podbilewicz B. AFF-1, a FOS-1-regulated fusogen, mediates fusion of the anchor cell in C. elegans. Dev. Cell 12 (2007) 683-698
54. Schmidt-Ott K.M., Mori K., Kalandadze A., Li J.Y., Paragas N., Nicholas T., Devarajan P., and Barasch J. Neutrophil gelatinase-associated lipocalin-mediated iron traffic in kidney epithelia. Curr. Opin. Nephrol. Hypertens 15 (2006) 442-449
55. Schmidt-Ott K.M., Mori K., Li J.Y., Kalandadze A., Cohen D.J., Devarajan P., and Barasch J. Dual action of neutrophil gelatinase-associated lipocalin. J. Am. Soc. Nephrol. 18 (2007) 407-413
56. Schultz J., Milpetz F., Bork P., and Ponting C.P. SMART, a simple modular architecture research tool: identification of signaling domains. Proc. Natl. Acad. Sci. U. S. A. 95 (1998) 5857-5864
57. Sulston J.E., and Horvitz H.R. Post-embryonic cell lineages of the nematode Caenorhabditis elegans. Dev. Biol. 56 (1977) 110-156
58. Sulston J.E., Scheirenberg E., White J.G., and Thomson J.N. The embryonic cell lineage of the nematode Caenorhabditis elegans. Dev. Biol. 100 (1983) 64-119
59. Wang C.X., and Shuaib A. Critical role of microvasculature basal lamina in ischemic brain injury. Prog. Neurobiol. 83 (2007) 140-148
60. Ward S., Thomson N., White J.G., and Brenner S. Electron microscopical reconstruction of the anterior sensory anatomy of the nematode Caenorhabditis elegans. J. Comp. Neurol. 160 (1975) 313-337
61. Weimer R.M. Preservation of C. elegans tissue via high-pressure freezing and freeze-substitution for ultrastructural analysis and immunocytochemistry. Methods Mol. Biol. (2006) 203-221
62. Whitehead K.F., Chan A.C., Navankasattusas S., Koh W., London N.R., Ling J., Mayo A.H., Drakos S.G., Marchuk D.A., Davis G.E., and Li D.Y. The cerebral cavernous malformation signaling pathway promotes vascular integrity via Rho GTPases. Nat. Med. 15 (2009) 177-184
63. Wilkinson H.A., and Greenwald I. Spatial and temporal patterns of lin-12 expression during C. elegans hermaphrodite development. Genetics 141 (1995) 513-526
64. Yang J., Goetz D., Li J.Y., Wang W., Mori K., Setlik D., Du T., Erdjument-Bromage H., Tempst P., Strong R., and Barasch J. An iron delivery pathway mediated by a lipocalin. Mol. Cell 10 (2002) 1045-1056
65. Yang J., Mori K., Li J.Y., and Barasch J. Iron, lipocalin, and kidney epithelia. Am. J. Physiol. Renal Physiol. 285 (2003) F9-F18
66. Yochem J., Sundaram M., and Han M. Ras is required for a limited number of cell fates and not for general proliferation in Caenorhabditis elegans. Mol. Cell Biol. 17 (1997) 2716-2722