Xenopus laevis nucleotide binding protein 1 (xNubp1) is important for convergent extension movements and controls ciliogenesis via regulation of the actin cytoskeleton

Developmental Biology

Volumn 380, Issue 2, 2013, Pages 243-258

  Ioannou, Andriani ^a   Santama, Niovi ^a   Skourides, Paris A ^a  

^a UNIVERSITY OF CYPRUS   (Cyprus)

Author keywords

Actin; Basal bodies; Ciliogenesis; Convergent extension; Nubp1; Xenopus

Indexed keywords

ACTIN; NUCLEOTIDE BINDING PROTEIN; NUCLEOTIDE BINDING PROTEIN 1; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AXONEME; CELL ELONGATION; CELL MATURATION; CELL MIGRATION; CELL MOTION; CELL STRUCTURE; CILIATED EPITHELIUM; CILIOGENESIS; CONTROLLED STUDY; DOWN REGULATION; EGG; EMBRYO; ENZYME ACTIVATION; EPIDERMIS; FEMALE; INTERCALATION COMPLEX; KINETOSOME; MOLECULAR CLONING; MOLECULAR DOCKING; NERVOUS TISSUE; NEURAL TUBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; REGULATORY MECHANISM; XENOPUS LAEVIS;

XENOPUS LAEVIS;

EID: 84879880339     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2013.05.004     Document Type: Article

References (72)

1. Antic D., Stubbs J.L., Suyama K., Kintner C., Scott M.P., Axelrod J.D. Planar cell polarity enables posterior localization of nodal cilia and left-right axis determination during mouse and Xenopus embryogenesis. PLoS One 2010, 5:e8999.
2. Baker K., Beales P.L. Making sense of cilia in disease: the human ciliopathies. Am. J. Med. Genet. C Semin. Med. Genet. 2009, 151C:281-295.
3. Blum M., Beyer T., Weber T., Vick P., Andre P., Bitzer E., Schweickert A. Xenopus, an ideal model system to study vertebrate left-right asymmetry. Dev. Dyn. 2009, 238:1215-1225.
4. Boisvieux-Ulrich E., Laine M.C., Sandoz D. The orientation of ciliary basal bodies in quail oviduct is related to the ciliary beating cycle commencement. Biol. Cell 1985, 55:147-150.
5. Boisvieux-Ulrich E., Laine M.C., Sandoz D. In vitro effects of colchicine and nocodazole on ciliogenesis in quail oviduct. Biol. Cell 1989, 67:67-79.
6. Boisvieux-Ulrich E., Laine M.C., Sandoz D. Cytochalasin D inhibits basal body migration and ciliary elongation in quail oviduct epithelium. Cell Tissue Res. 1990, 259:443-454.
7. Boisvieux-Ulrich E., Sandoz D., Allart J.-P. Determination of ciliary polarity precedes differentiation in the epithelial cells of quail oviduct. Biol. Cell 1991, 72:3-14.
8. Bowes J.B., Snyder K.A., Segerdell E., Jarabek C.J., Azam K., Zorn A.M., Vize P.D. Xenbase: gene expression and improved integration. Nucleic Acids Res. 2010, 38:D607-612.
9. Christodoulou A., Lederer C.W., Surrey T., Vernos I., Santama N. Motor protein KIFC5A interacts with Nubp1 and Nubp2, and is implicated in the regulation of centrosome duplication. J. Cell Sci. 2006, 119:2035-2047.
10. Chung M.-I., Peyrot S.M., LeBoeuf S., Park T.J., McGary K.L., Marcotte E.M., Wallingford J.B. RFX2 is broadly required for ciliogenesis during vertebrate development. Dev. Biol. 2012, 363:155-165.
11. Dawe H.R., Farr H., Gull K. Centriole/basal body morphogenesis and migration during ciliogenesis in animal cells. J. Cell Sci. 2007, 120:7-15.
12. Frisch D., Farbman A.I. Development of order during ciliogenesis. Anat. Rec. 1968, 162:221-231.
13. Frisch D., Farbman A.I. Development of order during ciliogenesis. Anat. Rec. 1968, 162:221-232.
14. Goetz S.C., Anderson K.V. The primary cilium: a signalling centre during vertebrate development. Nat. Rev. Genet. 2010, 11:331-344.
15. Gomperts B.N., Gong-Cooper X., Hackett B.P. Foxj1 regulates basal body anchoring to the cytoskeleton of ciliated pulmonary epithelial cells. J. Cell Sci. 2004, 117:1329-1337.
16. Gordon R.E. Three-dimensional organization of microtubules and microfilaments of the basal body apparatus of ciliated respiratory epithelium. Cell Motil. 1982, 2:385-391.
17. Habas R., Kato Y., He X. Wnt/frizzled activation of Rho regulates vertebrate gastrulation and requires a novel formin homology protein Daam1. Cell 2001, 107:843-854.
18. Hall A. Rho GTPases and the actin cytoskeleton. Science 1998, 279:509-514.
19. Hausmann A., Aguilar Netz D.J., Balk J., Pierik A.J., Muhlenhoff U., Lill R. The eukaryotic P loop NTPase Nbp35: an essential component of the cytosolic and nuclear iron-sulfur protein assembly machinery. Proc. Nat. Acad. Sci.U.S.A. 2005, 102:3266-3271.
20. Heisenberg C.P., Tada M., Rauch G.J., Saude L., Concha M.L., Geisler R., Stemple D.L., Smith J.C., Wilson S.W. Silberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation. Nature 2000, 405:76-81.
21. Hildebrandt F., Benzing T., Katsanis N. Ciliopathies. N. Engl. J. Med. 2011, 364:1533-1543.
22. Huang T., You Y., Spoor M.S., Richer E.J., Kudva V.V., Paige R.C., Seiler M.P., Liebler J.M., Zabner J., Plopper C.G., Brody S.L. Foxj1 is required for apical localization of ezrin in airway epithelial cells. J. Cell Sci. 2003, 116:4935-4945.
23. Kim H.Y., Davidson L.A. Punctuated actin contractions during convergent extension and their permissive regulation by the non-canonical Wnt-signaling pathway. J. Cell Sci. 2011, 124:635-646.
24. Klotz C., Bordes N., Laine M.C., Sandoz D., Bornens M. Myosin at the apical pole of ciliated epithelial cells as revealed by a monoclonal antibody. J. Cell Biol. 1986, 103:613-619.
25. Koonin E.V. A superfamily of ATPases with diverse functions containing either classical or deviant ATP-binding motif. J. Mol. Biol. 1993, 229:1165-1174.
26. Leipe D.D., Wolf Y.I., Koonin E.V., Aravind L. Classification and evolution of P-loop GTPases and related ATPases. J. Mol. Biol. 2002, 317:41-72.
27. Lemullois M., Klotz C., Sandoz D. Immunocytochemical localization of myosin during ciliogenesis of quail oviduct. Eur. J. Cell Biol. 1987, 43:429-437.
28. Lutkenhaus J., Sundaramoorthy M. MinD and role of the deviant Walker A motif, dimerization and membrane binding in oscillation. Mol. Microbiol. 2003, 48:295-303.
29. Mitchell B., Jacobs R., Li J., Chien S., Kintner C. A positive feedback mechanism governs the polarity and motion of motile cilia. Nature 2007, 447:97-101.
30. Mitchell B., Stubbs J.L., Huisman F., Taborek P., Yu C., Kintner C. The PCP pathway instructs the planar orientation of ciliated cells in the Xenopus larval skin. Curr. Biol. 2009, 19:924-929.
31. Nakashima H., Grahovac M.J., Mazzarella R., Fujiwara H., Kitchen J.R., Threat T.A., Ko M.S.H. Two novel mouse genes - Nubp2, mapped to the t-complex on chromosome 17, and Nubp1, mapped to chromosome 16 - establish a new gene family of nucleotide-binding proteins in eukaryotes. Genomics 1999, 60:152-160.
32. Netz D.J.A., Pierik A.J., Stumpfig M., Muhlenhoff U., Lill R. The Cfd1-Nbp35 complex acts as a scaffold for iron-sulfur protein assembly in the yeast cytosol. Nat. Chem. Biol. 2007, 3:278-286.
33. Nieuwkoop P.D.A.F., J. Normal Table of Xenopus laevis (Daudin) 1994, Garland, New York. first ed0.
34. Nishikawa S., Hirata J., Sasaki F. Fate of ciliated epidermal cells during early development of <i>Xenopus laevis</i> using whole-mount immunostaining with an antibody against chondroitin 6-sulfate proteoglycan and anti-tubulin: transdifferentiation or metaplasia of amphibian epidermis. Histochem. Cell Biol. 1992, 98:355-358.
35. Pan J., You Y., Huang T., Brody S.L. RhoA-mediated apical actin enrichment is required for ciliogenesis and promoted by Foxj1. J. Cell Sci. 2007, 120:1868-1876.
36. Park T.J., Haigo S.L., Wallingford J.B. Ciliogenesis defects in embryos lacking inturned or fuzzy function are associated with failure of planar cell polarity and Hedgehog signaling. Nat. Genet. 2006, 38:303-311.
37. Park T.J., Mitchell B.J., Abitua P.B., Kintner C., Wallingford J.B. Dishevelled controls apical docking and planar polarization of basal bodies in ciliated epithelial cells. Nat. Genet. 2008, 40:871-879.
38. Pazour G.J., Agrin N., Leszyk J., Witman G.B. Proteomic analysis of a eukaryotic cilium. J. Cell Biol. 2005, 170:103-113.
39. Pazour G.J., Witman G.B. The vertebrate primary cilium is a sensory organelle. Curr. Opin. Cell Biol. 2003, 15:105-110.
40. Pedersen L.B., Veland I.R., Schroder J.M., Christensen S.T. Assembly of primary cilia. Dev. Dyn. 2008, 237:1993-2006.
41. Rauzi M., Lenne P.F. Cortical forces in cell shape changes and tissue morphogenesis. Curr. Top. Dev. Biol. 2011, 95:93-144.
42. Roy S. The motile cilium in development and disease: emerging new insights. Bioessays 2009, 31:694-699.
43. Sandoz D., Chailley B., Boisvieux-Ulrich E., Lemullois M., Laine M.C., Bautista-Harris G. Organization and functions of cytoskeleton in metazoan ciliated cells. Biol. Cell 1988, 63:183-193.
44. Schlessinger K., Hall A., Tolwinski N. Wnt signaling pathways meet Rho GTPases. Genes. Dev. 2009, 23:265-277.
45. Schnatwinkel C., Niswander L. Nubp1 is required for lung branching morphogenesis and distal progenitor cell survival in mice. PLoS One 2012, 7:e44871.
46. Schweickert A., Weber T., Beyer T., Vick P., Bogusch S., Feistel K., Blum M. Cilia-driven leftward flow determines laterality in xenopus. Curr. Biol.: CB 2007, 17:60-66.
47. Shahrestanifar M., Saha D.P., Scala L.A., Basu A., Howells R.D. Cloning of a human cDNA encoding a putative nucleotide-binding protein related to Escherichia coli MinD. Gene 1994, 147:281-285.
48. Sive H.L., Grainger R.M., Richard M.H. Early Development of Xenopus laevis: A Laboratory Manual 2010, Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
49. Skoglund P., Rolo A., Chen X., Gumbiner B.M., Keller R. Convergence and extension at gastrulation require a myosin IIB-dependent cortical actin network. Development 2008, 135:2435-2444.
50. Smith J.C., Conlon F.L., Saka Y., Tada M. Xwnt11 and the regulation of gastrulation in Xenopus. Philos. Trans. R Soc. Lond B Biol. Sci. 2000, 355:923-930.
51. Smith W.C., Harland R.M. Injected Xwnt-8 RNA acts early in Xenopus embryos to promote formation of a vegetal dorsalizing center. Cell 1991, 67:753-765.
52. Sokol S.Y. Analysis of Dishevelled signalling pathways during Xenopus development. Curr. Biol. 1996, 6:1456-1467.
53. Sorokin S.P. Reconstructions of centriole formation and ciliogenesis in mammalian lungs. J. Cell Sci. 1968, 3:207-230.
54. Stehling O., Netz D.J., Niggemeyer B., Rosser R., Eisenstein R.S., Puccio H., Pierik A.J., Lill R. Human Nbp35 is essential for both cytosolic iron-sulfur protein assembly and iron homeostasis. Mol. Cell Biol. 2008, 28:5517-5528.
55. Steinman R.M. An electron microscopic study of ciliogenesis in developing epidermis and trachea in the embryo of Xenopus laevis. Am. J. Anat. 1968, 122:19-55.
56. Stubbs J.L., Oishi I., Izpisua Belmonte J.C., Kintner C. The forkhead protein Foxj1 specifies node-like cilia in Xenopus and zebrafish embryos. Nat. Genet. 2008, 40:1454-1460.
57. Tada M., Smith J.C. Xwnt11 is a target of Xenopus brachyury: regulation of gastrulation movements via dishevelled, but not through the canonical Wnt pathway. Development 2000, 127:2227-2238.
58. Tissir F., Qu Y., Montcouquiol M., Zhou L., Komatsu K., Shi D., Fujimori T., Labeau J., Tyteca D., Courtoy P., Poumay Y., Uemura T., Goffinet A.M. Lack of cadherins Celsr2 and Celsr3 impairs ependymal ciliogenesis, leading to fatal hydrocephalus. Nat. Neurosci. 2010, 13:700-707.
59. Vitale G., Fabre E., Hurt E.C. NBP35 encodes an essential and evolutionary conserved protein in Saccharomyces cerevisiae with homology to a superfamily of bacterial ATPases. Gene 1996, 178:97-106.
60. Wallingford J.B. Neural tube closure and neural tube defects: studies in animal models reveal known knowns and known unknowns. Am. J. Med. Genet C Semin. Med. Genet. 2005, 135C:59-68.
61. Wallingford J.B. Planar cell polarity, ciliogenesis and neural tube defects. Hum. Mol. Genet. 15 Spec No 2006, 2:R227-234.
62. Wallingford J.B. Planar cell polarity signaling, cilia and polarized ciliary beating. Curr. Opin. Cell Biol. 2010, 22:597-604.
63. Wallingford J.B., Fraser S.E., Harland R.M. Convergent extension: the molecular control of polarized cell movement during embryonic development. Dev. Cell 2002, 2:695-706.
64. Wallingford J.B., Habas R. The developmental biology of Dishevelled: an enigmatic protein governing cell fate and cell polarity. Development 2005, 132:4421-4436.
65. Wallingford J.B., Harland R.M. Xenopus dishevelled signaling regulates both neural and mesodermal convergent extension: parallel forces elongating the body axis. Development 2001, 128:2581-2592.
66. Wallingford J.B., Harland R.M. Neural tube closure requires dishevelled-dependent convergent extension of the midline. Development 2002, 129:5815-5825.
67. Wallingford J.B., Mitchell B. Strange as it may seem: the many links between Wnt signaling, planar cell polarity, and cilia. Genes Dev. 2011, 25:201-213.
68. Wallingford J.B., Rowning B.A., Vogeli K.M., Rothbacher U., Fraser S.E., Harland R.M. Dishevelled controls cell polarity during Xenopus gastrulation. Nature 2000, 405:81-85.
69. Werner M.E., Hwang P., Huisman F., Taborek P., Yu C.C., Mitchell B.J. Actin and microtubules drive differential aspects of planar cell polarity in multiciliated cells. J. Cell Biol. 2011, 195:19-26.
70. Ybot-Gonzalez P., Savery D., Gerrelli D., Signore M., Mitchell C.E., Faux C.H., Greene N.D., Copp A.J. Convergent extension, planar-cell-polarity signalling and initiation of mouse neural tube closure. Development 2007, 134:789-799.
71. Zariwala M.A., Knowles M.R., Omran H. Genetic defects in ciliary structure and function. Annu. Rev. Physiol. 2007, 69:423-450.
72. Zhou J., Kim H.Y., Davidson L.A. Actomyosin stiffens the vertebrate embryo during crucial stages of elongation and neural tube closure. Development 2009, 136:677-688.