New functions for a vertebrate Rho guanine nucleotide exchange factor in ciliated epithelia

Development

Volumn 134, Issue 5, 2007, Pages 921-931

  Panizzi, Jennifer R ^a   Jessen, Jason R ^b   Drummond, Iain A ^c   Solnica Krezel, Lilianna ^a  

^a VANDERBILT UNIVERSITY   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

Arhgef11; Cell polarity; Left right asymmetry; Otoliths; PDZ RhoGEF; Pronephros; Zebrafish

Indexed keywords

ADENOSINE TRIPHOSPHATASE (POTASSIUM SODIUM); ANTISENSE OLIGONUCLEOTIDE; F ACTIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHO GUANINE NUCLEOTIDE EXCHANGE FACTOR; RHO GUANINE NUCLEOTIDE EXCHANGE FACTOR 11; UNCLASSIFIED DRUG; ACTIN; ARHGEF11 PROTEIN, HUMAN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; ZEBRAFISH PROTEIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BLASTULA; BRAIN VENTRICLE; CELL CULTURE; CELL VACUOLE; CHROMOSOME DELETION; CILIATED EPITHELIUM; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; GASTRULATION; GENE LOCUS; GENE OVEREXPRESSION; HUMAN; KIDNEY CYST; MARKER GENE; NERVOUS TISSUE; NONHUMAN; NUCLEOTIDE SEQUENCE; OTOLITH; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA SPLICING; RNA TRANSLATION; STRESS FIBER; VERTEBRATE; ZEBRA FISH; ANIMAL; BRAIN; CONGENITAL MALFORMATION; EPITHELIUM; EUKARYOTIC FLAGELLUM; GASTRULA; GENETICS; KIDNEY; METABOLISM; MORPHOGENESIS; PHYSIOLOGY; PRENATAL DEVELOPMENT; VESTIBULE;

DANIO RERIO; VERTEBRATA;

ACTINS; ANIMALS; BLASTULA; BODY PATTERNING; BRAIN; CELLS, CULTURED; CILIA; EPITHELIUM; GASTRULA; GUANINE NUCLEOTIDE EXCHANGE FACTORS; KIDNEY; NA(+)-K(+)-EXCHANGING ATPASE; OTOLITHIC MEMBRANE; STRESS FIBERS; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 34248570697     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.02776     Document Type: Article

References (62)

1. Aurandt, J., Vikis, H. G., Gutkind, J. S., Ahn, N. and Guan, K. L. (2002). The semaphorin receptor plexin-B1 signals through a direct interaction with the Rho-specific nucleotide exchange factor, LARG. Proc. Natl. Acad. Sci. USA 99, 12085-12090.
2. Banerjee, J. and Wedegaertner, P. B. (2004). Identification of a novel sequence in PDZ-RhoGEF that mediates interaction with the actin cytoskeleton. Mol. Biol. Cell 15, 1760-1775.
3. Barac, A., Basile, J., Vazquez-Prado, J., Gao, Y., Zheng, Y. and Gutkind, J. S. (2004). Direct interaction of p21-activated kinase 4 with PDZ-RhoGEF a G protein-linked Rho guanine exchange factor. J. Biol. Chem. 279, 6182-6189.
4. Barrett, K., Leptin, M. and Settleman, J. (1997). The Rho GTPase and a putative RhoGEF mediate a signaling pathway for the cell shape changes in Drosophila gastrulation. Cell 91, 905-915.
5. Bisgrove, B. W., Snarr, B. S., Emrazian, A. and Yost, H. J. (2005). Polaris and Polycystin-2 in dorsal forerunner cells and Kupffer's vesicle are required for specification of the zebrafish left-right axis. Dev. Biol. 287, 274-288.
6. Cerione, R. A. and Zheng, Y. (1996). The Dbl family of oncogenes. Curr. Opin. Cell Biol. 8, 216-222.
7. Chikumi, H., Barac, A., Behbahani, B., Gao, Y., Teramoto, H., Zheng, Y. and Gutkind, J. S. (2004). Homo- and hetero-oligomerization of PDZ-RhoGEF, LARG and p115RhoGEF by their C-terminal region regulates their in vivo Rho GEF activity and transforming potential. Oncogene 23, 233-240.
8. Cooper, M. S. and D'Amico, L. A. (1996). A cluster of noninvoluting endocytic cells at the margin of the zebrafish blastoderm marks the site of embryonic shield formation. Dev. Biol. 180, 184-198.
9. Corbit, K. C., Aanstad, P., Singla, V., Norman, A. R., Stainier, D. Y. and Reiter, J. F. (2005). Vertebrate Smoothened functions at the primary cilium. Nature 437, 1018-1021.
10. Danos, M. C. and Yost, H. J. (1996). Role of notochord in specification of cardiac left-right orientation in zebrafish and Xenopus. Dev. Biol. 177, 96-103.
11. Drummond, I. A. (2000). The zebrafish pronephros: a genetic system for studies of kidney development. Pediatr. Nephrol. 14, 428-435.
12. Drummond, I. A., Majumdar, A., Hentschel, H., Eiger, M., Solnica-Krezel, L., Schier, A. F., Neuhauss, S. C., Stemple, D. L., Zwartkruis, F., Rangini, Z. et al. (1998). Early development of the zebrafish pronephros and analysis of mutations affecting pronephric function. Development 125, 4655-4667.
13. Essner, J. J., Amack, J. D., Nyholm, M. K., Harris, E. B. and Yost, H. J. (2005). Kupffer's vesicle is a ciliated organ of asymmetry in the zebrafish embryo that initiates left-right development of the brain, heart and gut. Development 132, 1247-1260.
14. Fukuhara, S., Murga, C., Zohar, M., Igishi, T. and Gutkind, J. S. (1999). A novel PDZ domain containing guanine nucleotide exchange factor links heterotrimeric G proteins to Rho. J. Biol. Chem. 274, 5868-5879.
15. Fukuhara, S., Chikumi, H. and Gutkind, J. S. (2001). RGS-containing RhoGEFs: the missing link between transforming G proteins and Rho? Oncogene 20, 1661-1668.
16. Hacker, U. and Perrimon, N. (1998). DRhoGEF2 encodes a member of the Dbl family of oncogenes and controls cell shape changes during gastrulation in Drosophila. Genes Dev. 12, 274-284.
17. Hart, M. J., Roscoe, W. and Bollag, G. (2000). Activation of Rho GEF activity by G alpha 13. Meth. Enzymol. 325, 61-71.
18. Huangfu, D. and Anderson, K. V. (2005). Cilia and Hedgehog responsiveness in the mouse. Proc. Natl. Acad. Sci. USA 102, 11325-11330.
19. Hubbard, T., Andrews, D., Caccamo, M., Cameron, G., Chen, Y., Clamp, M., Clarke, L., Coates, G., Cox, T., Cunningham, F. et al. (2005). Ensembl 2005. Nucleic Acids Res. 33, D447-D453.
20. -, and pH dependence of the human choline transporter (hCHT) in Xenopus oocytes: the proton inactivation hypothesis of hCHT in synaptic vesicles. J. Neurosci. 26, 9851-9859.
21. Jessen, J. R., Topczewski, J., Bingham, S., Sepich, D. S., Marlow, F., Chandrasekhar, A. and Solnica-Krezel, L. (2002). Zebrafish trilobite identifies new roles for Strabismus in gastrulation and neuronal movements. Nat. Cell Biol. 4, 610-615.
22. Kane, D. A. and Kimmel, C. B. (1993). The zebrafish midblastula transition. Development 119, 447-456.
23. Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B. and Schilling, T. F. (1995). Stages of embryonic development of the zebrafish. Dev. Dyn. 203, 253-310.
24. Kramer-Zucker, A. G., Olale, E, Haycraft, C. J., Yoder, B. K., Schier, A. F. and Drummond, I. A. (2005). Cilia-driven fluid flow in the zebrafish pronephros, brain and Kupffer's vesicle is required for normal organogenesis. Development 132, 1907-1921.
25. Kuner, R., Swiercz, J. M., Zywietz, A., Tappe, A. and Offermanns, S. (2002). Characterization of the expression of PDZ-RhoGEF, LARG and G(alpha)12/G(alpha)13 proteins in the murine nervous system. Eur. J. Neurosci. 16, 2333-2341.
26. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
27. Levin, M. (2005). Left-right asymmetry in embryonic development: a comprehensive review. Mech. Dev. 122, 3-25.
28. Long, S., Ahmad, N. and Rebagliati, M. (2003). The zebrafish nodal-related gene southpaw is required for visceral and diencephalic left-right asymmetry. Development 130, 2303-2316.
29. Marlow, F, Zwartkruis, F., Malicki, J., Neuhauss, S. C., Abbas, L., Weaver M., Driever, W. and Soinica-Krezel, L. (1998). Functional interactions of genes mediating convergent extension, knypek and trilobite, during the partitioning of the eye primordium in zebrafish. Dev. Biol. 203, 382-399.
30. Marlow, F., Topczewski, J., Sepich, D. and Solnica-Krezel, L. (2002). Zebrafish Rho kinase 2 acts downstream of Wnt11 to mediate cell polarity and effective convergence and extension movements. Curr. Biol. 12, 876-884.
31. Matsui, T., Raya, A., Kawakami, Y., Callol-Massot, C., Capdevila, J., Rodriguez-Esteban, C. and Izpisua Belmonte, J. C. (2005). Noncanonical Wnt signaling regulates midline convergence of organ primordia during zebrafish development. Genes Dev. 19, 164-175.
32. Milewski, W. M., Duguay, S. J., Chan, S. J. and Steiner, D. F. (1998). Conservation of PDX-1 structure, function, and expression in zebrafish. Endocrinology 139, 1440-1449.
33. Murphy, J. T., Duffy, S. L., Hybki, D. L. and Kamm, K. (2001). Thrombin-mediated permeability of human microvascular pulmonary endothelial cells is calcium dependent. J. Trauma 50, 213-222.
34. Nagase, T., Ishikawa, K., Nakajima, D., Ohira, M., Seki, N., Miyajima, N., Tanaka, A., Kotani, H., Nomura, N. and Ohara, O. (1997). Prediction of the coding sequences of unidentified human genes. VII. The complete sequences of 100 new cDNA clones from brain which can code for large proteins in vitro. DNA Res. 4, 141-150.
35. Nasevicius, A. and Ekker, S. C. (2000). Effective targeted gene 'knockdown' in zebrafish. Nat. Genet 26, 216-220.
36. Nikolaidou, K. K. and Barrett, K. (2004). A Rho GTPase signaling pathway is used reiteratively in epithelial folding and potentially selects the outcome of Rho activation. Curr. Biol. 14, 1822-1826.
37. Oleksy, A., Opalinski, L., Derewenda, U., Derewenda, Z. S. and Otlewski, J. (2006). The molecular basis of RhoA specificity in the guanine nucleotide exchange factor PDZ-RhoGEF. J. Biol. Chem. 281, 32891-32897.
38. Otto, E. A., Schermer, B., Obara, T., O'Toole, J. F., Hiller, K. S., Mueller, A. M., Ruf R. G., Hoefele, J., Beekmann, E, Landau, D. et al. (2003). Mutations in INVS encoding inversin cause nephronophthisis type 2, linking renal cystic disease to the function of primary cilia and left-right axis determination. Nat. Genet. 34, 413-420.
39. Padash Barmchi, M., Rogers, S. and Hacker, U. (2005). DRhoGEF2 regulates actin organization and contractility in the Drosophila blastoderm embryo. J. Cell Biol. 168, 575-585.
40. Panizzi, P., Boxrud, P. D., Verhamme, I. M. and Bock, P. E. (2006). Binding of the COOH-terminal lysine residue of streptokinase to plasmin(ogen) kringles enhances formation of the streptokinase plasmin(ogen) catalytic complexes. J. Biol. Chem. 281, 26774-26778.
41. Perrot, V., Vazquez-Prado, J. and Gutkind, J. S. (2002). Plexin B regulates Rho through the guanine nucleotide exchange factors leukemia-associated Rho GEF (LARG) and PDZ-RhoGEF. J. Biol. Chem. 277, 43115-43120.
42. Popper, A. N. and Lu, Z. (2000). Structure-function relationships in fish otolith organs. Fish. Res. 46, 15-25.
43. Rajasekaran, S. A., Barwe, S. P. and Rajasekaran, A. K. (2005). Multiple functions of Na,K-ATPase in epithelial cells. Semin. Nephrol. 25, 328-334.
44. Riley, B. B., Zhu, C., Janetopoulos, C. and Aufderheide, K. J. (1997). A critical period of ear development controlled by distinct populations of ciliated cells in the zebrafish. Dev. Biol. 191, 191-201.
45. Rogers, S. L., Wiedemann, U., Hacker, U., Turck, C. and Vale, R. D. (2004). Drosophila RhoGEF2 associates with microtubule plus ends in an EB1-dependent manner. Curr. Biol. 14, 1827-1833.
46. Rossman, K. L., Der, C. J. and Sondek, J. (2005). GEF means go: turning on RHO GTPases with guanine nucleotide-exchange factors. Nat. Rev. Mol. Cell Biol. 6, 167-180.
47. Rumenapp, U., Blomquist A., Schworer, G., Schablowski, H., Psoma, A. and Jakobs, K. H. (1999). Rho-specific binding and guanine nucleotide exchange catalysis by KIAA0380, a dbl family member. FEBS Lett. 459, 313-318.
48. Rupp, R. A., Snider, L. and Weintraub, H. (1994). Xenopus embryos regulate the nuclear localization of XMyoD. Genes Dev. 8, 1311-1323.
49. Schmidt, A. and Hall, A. (2002). Guanine nucleotide exchange factors for Rho GTPases: turning on the switch. Genes Dev. 16, 1587-1609.
50. Schneider, L., Clement C. A., Teilmann, S. C., Pazour, G. J., Hoffmann, E. K., Satir, P. and Christensen, S. T. (2005). PDGFRalphaalpha signaling is regulated through the primary cilium in fibroblasts. Curr. Biol. 15, 1861-1866.
51. Simoes, S., Denholm, B., Azevedo, D., Sotillos, S., Martin, P., Skaer, H., Hombria, J. C. and Jacinto, A. (2006). Compartmentalisation of Rho regulators directs cell invagination during tissue morphogenesis. Development 133, 4257-4267.
52. Solnica-Krezel, L., Schier, A. F. and Driever, W. (1994). Efficient recovery of ENU-induced mutations from the zebrafish germline. Genetics 136, 1401-1420.
53. Sun, Z., Amsterdam, A., Pazour, G. J., Cole, D. G., Miller, M. S. and Hopkins, N. (2004). A genetic screen in zebrafish identifies cilia genes as a principal cause of cystic kidney. Development 131, 4085-4093.
54. Swiercz, J. M., Kuner, R., Behrens, J. and Offermanns, S. (2002). Plexin-B1 directly interacts with PDZ-RhoGEF/LARG to regulate RhoA and growth cone morphology. Neuron 35, 51-63.
55. Tatusova, T. A. and Madden, T. L. (1999). BLAST 2 Sequences, a new tool for comparing protein and nucleotide sequences. FEMS Microbiol. Lett. 174, 247-250.
56. Thisse, C. and Thisse, B. (1998). High resolution whole-mount in situ hybridization. Zebrafish Science Monitor 5, 8-9.
57. Topczewska, J. M., Topczewski, J., Shostak, A., Kume, T., Solnica-Krezel, L. and Hogan, B. L. (2001). The winged helix transcription factor Foxc1 a is essential for somitogenesis in zebrafish. Genes Dev. 15, 2483-2493.
58. Tsujikawa, M. and Malicki, J. (2004). Intraflagellar transport genes are essential for differentiation and survival of vertebrate sensory neurons. Neuron 42, 703-716.
59. Isukui, T., Capdevila, J., Tamura, K., Ruiz-Lozano, P., Rodriguez-Esteban, C., Yonei-Tamura, S., Magallon, J., Chandraratna, R. A., Chien, K., Blumberg, B. et al. (1999). Multiple left-right asymmetry defects in Shh(-/-) mutant mice unveil a convergence of the shh and retinoic acid pathways in the control of Lefty-1. Proc. Natl. Acad. Sci. USA 96, 11376-11381.
60. Wei, L., Roberts, W., Wang, L., Yamada, M., Zhang, S., Zhao, Z., Rivkees, S. A., Schwartz, R. J. and Imanaka-Yoshida, K. (2001). Rho kinases play an obligatory role in vertebrate embryonic organogenesis. Development 128, 2953-2962.
61. Yelon, D., Horne, S. A. and Stainier, D. Y. (1999). Restricted expression of cardiac myosin genes reveals regulated aspects of heart tube assembly in zebrafish. Dev. Biol. 214, 23-37.
62. Zhu, S., Liu, L., Korzh, V., Gong, Z. and Low, B. C. (2006). RhoA acts downstream of Wnt5 and Wnt11 to regulate convergence and extension movements by involving effectors Rho kinase and Diaphanous: use of zebrafish as an in vivo model for GTPase signaling. Cell. Signal. 18, 359-372.