Patterns & Phenotypes
Localization and loss-of-function implicates ciliary proteins in early, cytoplasmic roles in left-right asymmetry
Article first published online: 29 JUL 2005
Copyright © 2005 Wiley-Liss, Inc.
Volume 234, Issue 1, pages 176–189, September 2005
How to Cite
Qiu, D., Cheng, S.-M., Wozniak, L., McSweeney, M., Perrone, E. and Levin, M. (2005), Localization and loss-of-function implicates ciliary proteins in early, cytoplasmic roles in left-right asymmetry. Dev. Dyn., 234: 176–189. doi: 10.1002/dvdy.20509
- Issue published online: 16 AUG 2005
- Article first published online: 29 JUL 2005
- Manuscript Accepted: 20 MAY 2005
- Manuscript Revised: 17 MAY 2005
- Manuscript Received: 14 DEC 2004
- American Cancer Society. Grant Number: RSG-02-046-01
- National Institute of Health. Grant Number: 1-R01-GM-06227
- National Center for Research Resources. Grant Number: CO6RR11244
- 2003. Elements of left-right patterning gap junctions, pH, and membrane voltage. Dev Biol 259: 482–483. , .
- 2005. The V-ATPase generates asymmetric H+ flux required for correct LR asymmetry in chick and frog embryos. (in press). , , , , , , , .
- 1999. Asymmetry of cilia and of mice and men. Int J Dev Biol 43: 283–286. .
- 1998. Phenotypic plasticity in the intercalated cell: the hensin pathway. Am J Physiol 275: F183–190. , , , , .
- 1996. Hensin: a matrix protein determinant of epithelial polarity. J Clin Invest 98: 2189–2190. .
- 2004. The T box transcription factor no tail in ciliated cells controls zebrafish left-right asymmetry. Curr Biol 14: 685–690. , .
- 1999. Cellular activation triggered by the autosomal dominant polycystic kidney disease gene product PKD2. Mol Cell Biol 19: 3423–3434. , , , , , , .
- 1998. Use of latrunculin-A, an actin monomer-binding drug. Methods Enzymol 298: 18–25. .
- 1999. Atlas of Xenopus development. Milan: Springer. , , , .
- 2001. Overexpression of the Xenopus tight-junction protein Claudin causes randomization of the left-right body axis. Dev Biol 230: 217–229. , , .
- 1990. The development of handedness in left/right asymmetry. Development 109: 1–9. , .
- 2001. Cilia propel the embryo in the right direction. Am J Med Genet 101: 339–344. .
- 2003. Fusicoccin signaling reveals 14-3-3 protein function as a novel step in left-right patterning during amphibian embryogenesis. Development 130: 4847–4858. , , .
- 2000. Conserved and divergent mechanisms in left-right axis formation. Genes Dev 14: 763–776. , .
- 2002. The ins and outs of polycystin-2 as a calcium release channel. Nature Cell Biol 4: E56–57. .
- 1999. Identification and characterization of polycystin-2, the PKD2 gene product. J Biol Chem 274: 28557–28565. , , , , , , , , , .
- 1989. The appearance of acetylated alpha-tubulin during early development and cellular differentiation in Xenopus. Dev Biol 136: 104–117. , .
- 2003. Role of cortical filamentous actin in the melanotrope cell of Xenopus laevis. Gen Comp Endocrinol 134: 95–102. , , , .
- 1996. Role of notochord in specification of cardiac left-right orientation in zebrafish and Xenopus. Dev Biol 177: 96–103. , .
- 2004. Expression of kinesin kif5c during chick development. Anat Embryol (Berl). , , .
- 1986. Microtubule dynamics during the cell cycle: the effects of taxol and nocodazole on the microtubule system of Pt K2 cells at different stages of the mitotic cycle. Int Rev Cytol 101: 215–274. , , , , , .
- 1989. Whole-mount analysis of cytoskeletal reorganization and function during oogenesis and early embryogenesis in Xenopus. In: ShattenH, ShattenG, editors. The cell biology of fertilization. New York: Academic Press. p 63–103. , .
- 2004. A perspective on inversin. Cell Biol Int 28: 119–124. , , , , , , , .
- 2002. Conserved function for embryonic nodal cilia. Nature 418: 37–38. , , , , , .
- 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. , , , , .
- 2005. Serotonin signaling is a very early step in patterning of the left-right axis in chick and frog embryos. Curr Biol 15: 794–803. , , .
- 2000. N-cadherin, a cell adhesion molecule involved in establishment of embryonic left-right asymmetry. Science 288: 1047–1051. , , .
- 1993. Confocal immunofluorescence microscopy of microtubules in amphibian oocytes and eggs. Methods Cell Biol 38: 241–264. .
- 1994. Gamma-tubulin is asymmetrically distributed in the cortex of Xenopus oocytes. Dev Biol 161: 131–140. .
- 1995. Axis formation during amphibian oogenesis: reevaluating the role of the cytoskeleton. Curr Topics Dev Biol 30: 215–252. .
- 1995a. Microtubule organization, acetylation, and nucleation in Xenopus laevis oocytes: II. A developmental transition in microtubule organization during early diplotene. Dev Biol 168: 189–201. , , .
- 1995b. F-actin is required for spindle anchoring and rotation in Xenopus oocytes: a re-examination of the effects of cytochalasin B on oocyte maturation. Zygote 3: 17–26. , , .
- 1995c. Confocal immunofluorescence microscopy of microtubules, microtubule-associated proteins, and microtubule-organizing centers during amphibian oogenesis and early development. Curr Topics Dev Biol 31: 383–431. , , .
- 2000. Expression and partial characterization of kinesin-related proteins in differentiating and adult skeletal muscle. Mol Biol Cell 11: 4143–4158. , .
- 2002. Voltage dependence and pH regulation of human polycystin-2-mediated cation channel activity. J Biol Chem 277: 24959–24966. , , , , , , , , .
- 1992. A series of normal stages in the development of the chick embryo. Dev Dyn 195: 231–272. , .
- 2000. Co-assembly of polycystin-1 and -2 produces unique cation-permeable currents. Nature 408: 990–994. , , , , , , , , .
- 1997. Unipolar microtubule array is directly involved in nurse cell-oocyte transport. Cell Motil Cytoskeleton 36: 355–362. , .
- 2000a. Determination of left-right asymmetry: Role of cilia and KIF3 motor proteins. News Physiol Sci 15: 56. .
- 2000b. Stirring up development with the heterotrimeric kinesin KIF3. Traffic 1: 29–34. .
- 1998. The left-right coordinator: the role of Vg1 in organizing left-right axis. Cell 93: 37–46. , .
- 2002. Polycystin-2 is an intracellular calcium release channel. Nat Cell Biol 4: 191–197. , , , , , , , .
- 2002. PKCgamma regulates syndecan-2 inside-out signaling during xenopus left-right development. Cell 111: 981–990. , , .
- 2005. Cilia-driven fluid flow in the zebrafish pronephros, brain and Kupffer's vesicle is required for normal organogenesis. Development 132: 1907–1921. , , , , , .
- 1997. Microtubule disruption reveals that Spemann's organizer is subdivided into two domains by the vegetal alignment zone. Development 124: 895–906. , .
- 1998. Role of xklp3, a subunit of the Xenopus kinesin II heterotrimeric complex, in membrane transport between the endoplasmic reticulum and the Golgi apparatus. J Cell Biol 143: 1559–1573. , , , , .
- 1991. Detection of acetylated alpha-tubulin by specific antibodies. Methods Enzymol 196: 264–274. , .
- 2003. Hypothesis: motor proteins and ion pumps, not ciliary motion, initiate LR asymmetry. BioEssays 25: 1002–1010. .
- 2004a. Embryonic origins of left-right asymmetry. Crit Rev Oral Biol Med 15: 197–206. .
- 2004b. A novel immunohistochemical method for evaluation of antibody specificity and detection of labile targets in biological tissue. J Biochem Biophys Methods 58: 85–96. .
- 2005. Left-right asymmetry in embryonic development: a comprehensive review. Mech Dev 122: 3–25. .
- 1998a. The compulsion of chirality: toward an understanding of left- right asymmetry. Genes Dev 12: 763–769. , .
- 1998b. Gap junctions are involved in the early generation of left right asymmetry. Dev Biol 203: 90–105. , .
- 1999. Gap junction-mediated transfer of left-right patterning signals in the early chick blastoderm is upstream of Shh asymmetry in the node. Development 126: 4703–4714. , .
- 1997. Two molecular models of initial left-right asymmetry generation. Med Hypotheses 49: 429–435. , .
- 2002. Asymmetries in H+/K+-ATPase and cell membrane potentials comprise a very early step in left-right patterning. Cell 111: 77–89. , , , , .
- 1996. Conserved left-right asymmetry of nodal expression and alterations in murine situs inversus. Nature 381: 158–161. , , , , , , , .
- 2003. Evidence for kinesin- and dynein-like protein function in circular nuclear migration in the green alga Pleurenterium tumidum: digital time lapse analysis of inhibitor effects. J Phycol 39: 106–114. .
- 1986. The acetylation of alpha-tubulin and its relationship to the assembly and disassembly of microtubules. J Cell Biol 103: 571–579. , , .
- 2003. Cilia are at the heart of vertebrate left-right asymmetry. Curr Opin Genet Dev 13: 385–392. , .
- 1998. Cloning of inv, a gene that controls left/right asymmetry and kidney development. Nature 395: 177–181. , , , , , , , , , , , , .
- 2002. Molecular cloning of a gene for inversion of embryo turning (inv) with cystic kidney. Nephrol Dial Transplant 17: 68–70. , , .
- 1991. Distribution of acetylated alpha-tubulin in brain. In situ localization and biochemical characterization. Cell Tissue Res 265: 415–423. , .
- 1998. Inversin, a novel gene in the vertebrate left-right axis pathway, is partially deleted in the inv mouse. Nature Genet 20: 149–156. , , , , , , , , , , , , , .
- 2002. The left-right determinant inversin has highly conserved ankyrin repeat and IQ domains and interacts with calmodulin. Human Genet 110: 377–384. , , , , , , , .
- 2000. The Oak Ridge Polycystic Kidney (orpk) disease gene is required for left-right axis determination. Development 127: 2347–2355. , , , , , .
- 1967. Normal Table of Xenopus laevis (Daudin). Amsterdam: North-Holland Publishing Company. , .
- 1997. Evidence for several roles of dynein in pigment transport in melanophores. Cell Motil Cytoskeleton 38: 397–409. , .
- 1996. Localization of kinesin and cytoplasmic dynein in cultured melanophores from Atlantic cod, Gadus morhua. Cell Motil Cytoskeleton 33: 183–196. , , .
- 1998. Randomization of left-right asymmetry due to loss of nodal cilia generating leftward flow of extraembryonic fluid in mice lacking KIF3B motor protein. Cell 95: 829–837. , , , , , , , .
- 2002. Determination of left-right patterning of the mouse embryo by artificial nodal flow. Nature 418: 96–99. , , , .
- 1986. A two-dimensional extracellular vibrating probe for the detection of trans-cellular ionic currents. J Cell Biol 103: A519–A519. .
- 2002. Inversin forms a complex with catenins and N-cadherin in polarized epithelial cells. Mol Biol Cell 13: 3096–3106. , , .
- 2004. The Invs gene encodes a microtubule-associated protein. J Am Soc Nephrol 15: 1700–1710. , , , , , .
- 2003. The vertebrate primary cilium is a sensory organelle. Curr Opin Cell Biol 15: 105–110. , .
- 2000. Chlamydomonas IFT88 and its mouse homologue, polycystic kidney disease gene tg737, are required for assembly of cilia and flagella. J Cell Biol 151: 709–718. , , , , , , .
- 2002. Polycystin-2 localizes to kidney cilia and the ciliary level is elevated in orpk mice with polycystic kidney disease. Curr Biol 12: R378–380. , , , , .
- 2002. The ion channel polycystin-2 is required for left-right axis determination in mice. Curr Biol 12: 938–943. , , , , , , , .
- 2001. The differential distribution of acetylated and detyrosinated alpha-tubulin in the microtubular cytoskeleton and primary cilia of hyaline cartilage chondrocytes. J Anat 199: 393–405. , , .
- 2004. Notch activity acts as a sensor for extracellular calcium during vertebrate left-right determination. Nature 427: 121–128. , , , , , , , , .
- 1991. Kinesin is responsible for centrifugal movement of pigment granules in melanophores. Proc Natl Acad Sci USA 88: 4956–4960. , , .
- 1994. Confocal microscopy of F-actin distribution in Xenopus oocytes. Zygote 2: 111–124. , .
- 1999. Monoclonal antibody ID5: epitope characterization and minimal requirements for the recognition of polyglutamylated alpha- and beta-tubulin. Eur J Cell Biol 78: 15–20. , , , .
- 1998. A marine natural product inhibitor of kinesin motors. Science 280: 292–295. , , , , , , .
- 1988. Distribution of acetylated alpha-tubulin in retina and in vitro-assembled microtubules. Cell Motil Cytoskeleton 9: 243–253. , , .
- 1995. Activin and its receptors during gastrulation and the later phases of mesoderm development in the chick embryo. Dev Biol 172: 192–205. , , , , , , , .
- 1997. Mutation of an axonemal dynein affects left-right asymmetry in inversus viscerum mice. Nature 389: 963–966. , , , .
- 1999a. Targeted deletion of the ATP binding domain of left-right dynein confirms its role in specifying development of left-right asymmetries. Development 126: 5495–5504. , , , , , , , .
- 1999b. Targeted deletion of the ATP binding domain of left-right dynein confirms its role in specifying development of left-right asymmetries. Development (Suppl) 126: 5495–5504. , , , , , , , .
- 2003. A two-cilia model for vertebrate left-right axis specification. Genes Dev 17: 1–6. , .
- 1999. Left-right asymmetry and kinesin superfamily protein KIF3A: new insights in determination of laterality and mesoderm induction by kif3A-/- mice analysis. J Cell Biol 145: 825–836. , , , , , .
- 1999. Hensin, the polarity reversal protein, is encoded by DMBT1, a gene frequently deleted in malignant gliomas. Am J Physiol 277: F277–289. , , , , , , .
- 2001. Polaris, a protein involved in left-right axis patterning, localizes to basal bodies and cilia. Mol Biol Cell 12: 589–599. , , , .
- 2001. Polycystin-2 is a novel cation channel implicated in defective intracellular Ca(2+) homeostasis in polycystic kidney disease. Biochem Biophys Res Commun 282: 341–350. , , , , , , , , , , , , .
- 1999. Hensin remodels the apical cytoskeleton and induces columnarization of intercalated epithelial cells: processes that resemble terminal differentiation. J Cell Biol 144: 1057–1067. , , , .
- 1999. A new spin on handed asymmetry. Nature 397: 295, 297–298. , .
- 1990. Distribution of microtubules containing post-translationally modified alpha-tubulin during Drosophila embryogenesis. Cell Motil Cytoskeleton 17: 34–45. , , , , .
- 1990. Detyrosination of alpha tubulin does not stabilize microtubules in vivo. J Cell Biol 111: 113–122. , , , .
- 2000. Formation of the avian primitive streak from spatially restricted blastoderm: evidence for polarized cell division in the elongating streak. Development 127: 87–96. , .
- 1994. Primary cilia in cultured mammalian cells: detection with an antibody against detyrosinated alpha-tubulin (ID5) and by electron microscopy. J Submicrosc Cytol Pathol 26: 91–102. , , , .
- 1997. Ortho-vanadate affects both the tyrosination/detyrosination state of spindle microtubules and the organization of XTH-2 spindles. Eur J Cell Biol 73: 306–315. , .
- 1993. Reversal of left-right asymmetry: a situs inversus mutation. Science 260: 679–682. , , , , , .
- 1991. Development of the left-right axis in amphibians. Ciba Found Symp 162: 165–176. .
- 2001. Establishment of left-right asymmetry. Int Rev Cytol 203: 357–381. .