Intracellular lumen extension requires ERM-1-dependent apical membrane expansion and AQP-8-mediated flux

Nature Cell Biology

Volumn 15, Issue 2, 2013, Pages 143-156

  Khan, Liakot A ^a   Zhang, Hongjie ^a   Abraham, Nessy ^a   Sun, Lei ^c,d   Fleming, John T ^a   Buechner, Matthew ^b   Hall, David H ^c   Gobel, Verena ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b UNIVERSITY OF KANSAS   (United States)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^d INSTITUTE OF BIOPHYSICS   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; AQUAPORIN 8; CELL MEMBRANE PROTEIN; MERCURY; PROTEIN ERM 1; UNCLASSIFIED DRUG;

APICAL MEMBRANE; ARTICLE; CAENORHABDITIS ELEGANS; CELL MEMBRANE TRANSPORT; CYTOSKELETON; EXOCRINE GLAND; INTRACELLULAR LUMEN EXPANSION; INTRACELLULAR MEMBRANE; INTRACELLULAR SPACE; MEMBRANE STRUCTURE; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SINGLE CELL ANALYSIS;

ACTIN CYTOSKELETON; ANIMALS; ANIMALS, GENETICALLY MODIFIED; AQUAPORINS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CYTOSKELETAL PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENOTYPE; MERCURIC CHLORIDE; MORPHOGENESIS; MUTATION; OSMOTIC PRESSURE; PHENOTYPE; PROTEIN BINDING; PROTEIN TRANSPORT; RNA INTERFERENCE; TIME FACTORS; WATER; WATER-ELECTROLYTE BALANCE;

CAENORHABDITIS ELEGANS;

EID: 84873398008     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2656     Document Type: Article

References (76)

1. Lubarsky, B. & Krasnow, M. A. Tube morphogenesis: making and shaping biological tubes. Cell 112, 19-28 (2003).
2. Bryant, D. M. & Mostov, K. E. From cells to organs: building polarized tissue. Nat Rev. Mol. Cell Biol. 9, 887-901 (2008).
3. Nelson, F. K., Albert, P. S. & Riddle, D. L. Fine structure of the Caenorhabditis elegans secretory-excretory system. J. Ultrastruct. Res. 82, 156-171 (1983).
4. Buechner, M., Hall, D. H., Bhatt, H. & Hedgecock, E. M. Cystic canal mutants in Caenorhabditis elegans are defective in the apical membrane domain of the renal (excretory) cell. Dev. Biol. 214, 227-241 (1999).
5. Hall, D. H. & Altun, Z. F. C. elegans Atlas (Cold Spring Harbor Laboratory Press, 2008).
6. Abdus-Saboor, I. et al. Notch and Ras promote sequential steps of excretory tube development in C. elegans. Development 138, 3545-3555 (2011).
7. Kolotuev, I., Hyenne, V., Schwab, Y., Rodriguez, D. & Labouesse, M. A pathway for unicellulartube extension dependingon the lymphatic vessel determinant Prox1 and on osmoregulation. Nat Cell Biol. http://dx.doi.org/10. 1038/ncb2662 (2013).
8. Jones, S. J. & Baillie, D. L. Characterization of the let-653 gene in Caenorhabditis elegans. Mol. Gen. Genet. 248, 719-726 (1995).
9. Suzuki, N. et al. A putative GDP-GTP exchange factor is required for development of the excretory cell in Caenorhabditis elegans. EMBO Rep. 2, 530-535 (2001).
10. Berry, K. L., Bulow, H. E., Hall, D. H. & Hobert, O.A C. elegans CLIC-like protein required for intracellular tube formation and maintenance. Science 302, 2134-2137 (2003).
11. Fujita, M. et al. The role of the ELAV homologue EXC-7 in the development of the Caenorhabditis elegans excretory canals. Dev. Biol. 256, 290-301 (2003).
12. Perens, E.A. & Shaham, S. C. elegans daf-6 encodes a patched-related protein required for lumen formation. Dev. Cell 8, 893-906 (2005).
13. Gobel, V., Barrett, P. L., Hall, D. H. & Fleming, J. T. Lumen morphogenesis in C. elegans requires the membrane-cytoskeleton linker erm-1. Dev. Cell 6, 865-873 (2004).
14. Saotome, I., Curto, M. & McClatchey, A. I. Ezrin is essential for epithelial organization and villus morphogenesis in the developing intestine. Dev. Cell 6, 855-864 (2004).
15. Fehon, R. G., McClatchey, A. I. & Bretscher, A. Organizing the cell cortex: the role of ERM proteins. Nat Rev. Mol. Cell Biol. 11, 276-287 (2010).
16. Ten Klooster, J. P. et al. Mst4 and Ezrin induce brush borders downstream of the Lkb1/Strad/Mo25 polarization complex. Dev. Cell 16, 551-562 (2009).
17. Zhu, L., Crothers, J. Jr, Zhou, R. & Forte, J. G. A possible mechanism for ezrin to establish epithelial cell polarity. Am. J. Physiol. Cell Physiol. 299, C431-C443 (2010).
18. Kerman, B. E., Cheshire, A. M., Myat, M. M. & Andrew, D. J. Ribbon modulates apical membrane during tube elongation through Crumbs and Moesin. Dev. Biol. 320, 278-288 (2008).
19. Gervais, L. & Casanova, J. In vivo coupling of cell elongation and lumen formation in a single cell. Curr. Biol. 20, 359-366 (2010).
20. Wang, Y. et al. Moesin1 and Ve-cadherin are required in endothelial cells during in vivotubulogenesis. Development 137,3119-3128(2010).
21. King, L. S., Kozono, D. & Agre, P. From structure to disease: the evolving tale of aquaporin biology. Nat Rev. Mol. Cell Biol. 5, 687-698 (2004).
22. Preston, G. M., Jung, J. S., Guggino, W. B. & Agre, P. The mercury-sensitive residue at cysteine 189 in the CHIP28 water channel. J. Biol. Chem. 268, 17-20 (1993).
23. Hachez, C. & Chaumont, F. Aquaporins: a family of highly regulated multifunctional channels. Adv. Exp. Med. Biol. 679, 1-17 (2010).
24. Huang, C. G., Lamitina, T., Agre, P. & Strange, K. Functional analysis of the aquaporin gene family in Caenorhabditis elegans. Am. J. Physiol. Cell Physiol. 292, C1867-C1873 (2007).
25. Buechner, M. Tubes and the single C. elegans excretory cell. Trends Cell Biol. 12, 479-484 (2002).
26. Koppen, M. et al. Cooperative regulation of AJM-1 controls junctional integrity in Caenorhabditis elegans epithelia. Nat Cell Biol. 3, 983-991 (2001).
27. MacQueen, A. J. et al. ACT-5 is an essential Caenorhabditis elegans actin required for intestinal microvilli formation. Mol. Biol. Cell 16, 3247-3259 (2005).
28. Mah, A. K. et al. Transcriptional regulation of AQP-8, a Caenorhabditis elegans aquaporin exclusively expressed in the excretory system, by the POU homeobox transcription factorCEH-6. J. Biol. Chem. 282, 28074-28086 (2007).
29. Mattingly, B. C. & Buechner, M. The FGD homologue EXC-5 regulates apical trafficking in C. elegans tubules. Dev. Biol. 359, 59-72 (2011).
30. Hahn-Windgassen, A. & Van Gilst, M. R. The Caenorhabditis elegansHNF4α homolog, NHR-31, mediates excretory tube growth and function through coordinate regulation of the vacuolar ATPase. PLoS Genet. 5, e1000553 (2009).
31. Liu, J., Xu, J., Gu, S., Nicholson, B. J. & Jiang, J. X. Aquaporin 0 enhances gap junction coupling via its cell adhesion function and interaction with connexin 50. J. CellSci. 124, 198-206 (2011).
32. Agre, P., Bonhivers, M. & Borgnia, M.J. The aquaporins, blueprints for cellular plumbingsystems. J. Biol. Chem. 273, 14659-14662 (1998).
33. Cheong, H.I. et al. Two novel mutations in the aquaporin 2 gene in a girl with congenital nephrogenic diabetes insipidus. J. Korean Med. Sci. 20, 1076-1078 (2005).
34. Folkman, J. & Haudenschild, C. Angiogenesis in vitro. Nature 288, 551-556 (1980).
35. Kamei, M. et al. Endothelial tubes assemble from intracellular vacuoles in vivo. Nature 442, 453-456 (2006).
36. Herwig, L. et al. Distinct cellular mechanisms of blood vessel fusion in the zebrafish embryo. Curr. Biol. 21, 1942-1948 (2011).
37. Schottenfeld-Roames, J. & Ghabrial, A. S. Whacked and Rab35 polarize dynein-motor-complex-dependent seamless tube growth. Nat Cell Biol. 14, 386-393 (2012).
38. Deretic, D. et al. Phosphoinositides, ezrin/moesin, and rac1 regulate fusion of rhodopsin transport carriers in retinal photoreceptors. Mol. Biol. Cell 15, 359-370 (2004).
39. Balklava, Z., Pant, S., Fares, H. & Grant, B. D. Genome-wide analysis identifies a general requirement for polarity proteins in endocytic traffic. Nat Cell Biol. 9, 1066-1073 (2007).
40. Chirivino, D. et al. The ERM proteins interact with the HOPS complex to regulate the maturation of endosomes. Mol. Biol. Cell 22, 375-385 (2011).
41. Kaksonen, M., Toret, C. P. & Drubin, D. G. A modular design for the clathrin-and actin-mediated endocytosis machinery. Cell 123, 305-320 (2005).
42. Lamprecht, G., Weinman, E. J. & Yun, C. H. The role of NHERF and E3KARP in the cAMP-mediated inhibition of NHE3. J. Biol. Chem. 273, 29972-29978 (1998).
43. Denker, S. P., Huang, D. C., Orlowski, J., Furthmayr, H. & Barber, D. L. Direct binding of the Na-H exchanger NHE1 to ERM proteins regulates the cortical cytoskeleton and cell shape independently of H(+) translocation. Mol. Cell 6, 1425-1436 (2000).
44. Zhou, R. et al. Characterization of protein kinaseA-mediated phosphorylation of ezrin in gastric parietal cell activation. J. Biol. Chem. 278, 35651-35659 (2003).
45. Tamura, A. et al. Achlorhydria by ezrin knockdown: defects in the forma-tion/expansion of apical canaliculi in gastric parietal cells. J. Cell Biol. 169, 21-28 (2005).
46. Cha, B. et al. The NHE3 juxtamembrane cytoplasmic domain directly binds ezrin: dual role in NHE3 trafficking and mobility in the brush border. Mol. Biol. Cell 17, 2661-2673 (2006).
47. Tamma, G. et al. Actin remodeling requires ERM function to facilitate AQP2 apical targeting. J. CellSci. 118, 3623-3630 (2005).
48. Desmond, M. E. & Jacobson, A. G. Embryonic brain enlargement requires cerebrospinal fluid pressure. Dev. Biol. 57, 188-198 (1977).
49. Stewart, M. P. et al. Hydrostatic pressure and the actomyosin cortex drive mitotic cell rounding. Nature 469, 226-230 (2011).
50. Vasilyev, A. et al. Collective cell migration drives morphogenesis of the kidney nephron. PLoS Biol. 7, e1000009 (2009).
51. Bagnat, M., Cheung, I. D., Mostov, K. E. & Stainier, D. Y. Genetic control of single lumen formation in the zebrafish gut. Nat Cell Biol. 9, 954-960 (2007).
52. Krupinski, T. & Beitel, G.J. Unexpected roles of the Na-K-ATPase and other ion transporters in cell junctions and tubulogenesis. Physiology (Bethesda) 24, 192-201 (2009).
53. Bagnat, M. et al. Cse1l is a negative regulator of CFTR-dependent fluid secretion. Curr. Biol. 20, 1840-1845 (2010).
54. Maurel, C.,Verdoucq, L., Luu, D. T. & Santoni, V. Plant aquaporins: membrane chan-nelswith multiple integrated functions. Annu. Rev. PlantBiol. 59, 595-624 (2008).
55. Morishita, Y. et al. Disruption of aquaporin-11 produces polycystic kidneys following vacuolization of the proximal tubule. Mol. Cell Biol. 25, 7770-7779 (2005).
56. Saadoun, S., Papadopoulos, M. C., Hara-Chikuma, M. & Verkman, A. S. Impairment of angiogenesis and cell migration by targeted aquaporin-1 gene disruption. Nature 434, 786-792 (2005).
57. Chen, Y. et al. Aquaporin 2 promotes cell migration and epithelial morphogenesis. J. Am. Soc. Nephrol. 23, 1506-1517 (2012).
58. Tatsumi, K. et al. Drosophila big brain does not act as a waterchannel, but mediates cell adhesion. FEBS Lett. 583, 2077-2082 (2009).
59. Wang, Z. & Schey, K. L. Aquaporin-0 interacts with the FERM domain of ezrin/radixin/moesin proteins in the ocular lens. Invest. Ophthalmol. Vis. Sci. 52, 5079-5087 (2011).
60. Gonen, T., Sliz, P., Kistler, J., Cheng, Y. & Walz, T. Aquaporin-0 membranejunctions reveal the structure of a closed water pore. Nature 429, 193-197 (2004).
61. Cho, S. J. et al. Aquaporin 1 regulatesGTP-induced rapidgatingofwater in secretory vesicles. Proc. NatlAcad. Sci. USA 99, 4720-4724 (2002).
62. Brown, D. The ins and outs of aquaporin-2 trafficking. Am. J. Physiol. Renal Physiol. 284, F893-F901 (2003).
63. Nozaki, K., Ishii, D. & Ishibashi, K. Intracellular aquaporins: clues for intracellular water transport? PfíugersArch. 456, 701-707 (2008).
64. Sugiya, H., Matsuki-Fukushima, M. & Hashimoto, S. Role of aquaporins and regulation of secretory vesicle volume in cell secretion. J. Cell Mol. Med. 12, 1486-1494 (2008).
65. Tung, J. J., Hobert, O., Berryman, M. & Kitajewski, J. Chloride intracellular channel 4 is involved in endothelial proliferation and morphogenesis in vitro. Angiogenesis 12, 209-220 (2009).
66. Brenner, S. The genetics of Caenorhabditis elegans. Genetics 77, 71-94 (1974).
67. Timmons, L., Court, D. L. & Fire, A. Ingestion of bacterially expressed dsRNAs can produce specific and potent genetic interference in Caenorhabditis elegans. Gene 263, 103-112 (2001).
68. Fire, A., Harrison, S. W. & Dixon, D. A modularsetof lacZ fusion vectors forstudying gene expression in Caenorhabditis elegans. Gene 93, 189-198 (1990).
69. Stinchcomb, D. T., Shaw, J. E., Carr, S. H. & Hirsh, D. Extrachromosomal DNA transformation of Caenorhabditis elegans. Mol. Cell Biol. 5, 3484-3496 (1985).
70. Mello, C. C., Kramer,J. M., Stinchcomb, D. & Ambros, V. Efficientgene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J. 10, 3959-3970 (1991).
71. Hadwiger, G., Dour, S., Arur, S., Fox, P. & Nonet, M. L. A monoclonal antibody toolkit for C. elegans. PLoS One 5, e10161 (2010).
72. Harlow, E. & Lane, D. Antibodies: A Laboratory Manual (Cold Spring Harbor Laboratory Press, 1988).
73. Weimer, R. M. Preservation of C. elegans tissue via high-pressure freezing and freeze-substitution for ultrastructural studies and immunocytochemistry. Methods Mol. Biol. 351, 203-221 (2006).
74. Winkler, H. & Taylor, K.A. Accurate marker-free alignment with simultaneous geometry determination and reconstruction of tilt series in electron tomography. Ultramicroscopy 106, 240-254 (2006).
75. Mastronarde, D. N. Dual-axis tomography: an approach using alignment methods that preserve resolution. J. Struct. Biol. 120, 343-352 (1997).
76. Kremer, J. R., Mastronarde, D. N. & McIntosh, J. R. Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 116, 71-76 (1996).