Click here to close
Hello! We notice that you are using Internet Explorer, which is not supported by Xenbase and may cause the site to display incorrectly.
We suggest using a current version of Chrome,
FireFox, or Safari.
???displayArticle.abstract???
Consistently-biased left-right (LR) patterning is required for the proper placement of organs including the heart and viscera. The LR axis is especially fascinating as an example of multi-scale pattern formation, since here chiral events at the subcellular level are integrated and amplified into asymmetric transcriptional cascades and ultimately into the anatomical patterning of the entire body. In contrast to the other two body axes, there is considerable controversy about the earliest mechanisms of embryonic laterality. Many molecular components of asymmetry have not been widely tested among phyla with diverse bodyplans, and it is unknown whether parallel (redundant) pathways may exist that could reverse abnormal asymmetry states at specific checkpoints in development. To address conservation of the early steps of LR patterning, we used the Xenopus laevis (frog) embryo to functionally test a number of protein targets known to direct asymmetry in plants, fruit fly, and rodent. Using the same reagents that randomize asymmetry in Arabidopsis, Drosophila, and mouse embryos, we show that manipulation of the microtubule and actin cytoskeleton immediately post-fertilization, but not later, results in laterality defects in Xenopus embryos. Moreover, we observed organ-specific randomization effects and a striking dissociation of organ situs from effects on the expression of left side control genes, which parallel data from Drosophila and mouse. Remarkably, some early manipulations that disrupt laterality of transcriptional asymmetry determinants can be subsequently "rescued" by the embryo, resulting in normal organ situs. These data reveal the existence of novel corrective mechanisms, demonstrate that asymmetric expression of Nodal is not a definitive marker of laterality, and suggest the existence of amplification pathways that connect early cytoskeletal processes to control of organ situs bypassing Nodal. Counter to alternative models of symmetry breaking during neurulation (via ciliary structures absent in many phyla), our data suggest a widely-conserved role for the cytoskeleton in regulating left-right axis formation immediately after fertilization of the egg. The novel mechanisms that rescue organ situs, even after incorrect expression of genes previously considered to be left-side master regulators, suggest LR patterning as a new context in which to explore multi-scale redundancy and integration of patterning from the subcellular structure to the entire bodyplan.
Abe,
Microtubule defects and cell morphogenesis in the lefty1lefty2 tubulin mutant of Arabidopsis thaliana.
2004, Pubmed
Abe,
Microtubule defects and cell morphogenesis in the lefty1lefty2 tubulin mutant of Arabidopsis thaliana.
2004,
Pubmed
Agata,
[Evolution of the genetic program controlling brain development].
1999,
Pubmed
Applegate,
plusTipTracker: Quantitative image analysis software for the measurement of microtubule dynamics.
2011,
Pubmed
Armakolas,
Left-right dynein motor implicated in selective chromatid segregation in mouse cells.
2007,
Pubmed
Bangs,
Generation of mice with functional inactivation of talpid3, a gene first identified in chicken.
2011,
Pubmed
Basu,
Cilia multifunctional organelles at the center of vertebrate left-right asymmetry.
2008,
Pubmed
,
Xenbase
Bearce,
TIPsy tour guides: how microtubule plus-end tracking proteins (+TIPs) facilitate axon guidance.
2015,
Pubmed
Bunney,
Fusicoccin signaling reveals 14-3-3 protein function as a novel step in left-right patterning during amphibian embryogenesis.
2003,
Pubmed
,
Xenbase
Burn,
Disturbance of morphological laterality in humans.
1991,
Pubmed
Campione,
The homeobox gene Pitx2: mediator of asymmetric left-right signaling in vertebrate heart and gut looping.
1999,
Pubmed
,
Xenbase
Chen,
Left-right symmetry breaking in tissue morphogenesis via cytoskeletal mechanics.
2012,
Pubmed
Cota,
Mice with mutations in Mahogunin ring finger-1 (Mgrn1) exhibit abnormal patterning of the left-right axis.
2006,
Pubmed
Coutelis,
Left-right asymmetry in Drosophila.
2008,
Pubmed
Danilchik,
Intrinsic chiral properties of the Xenopus egg cortex: an early indicator of left-right asymmetry?
2006,
Pubmed
,
Xenbase
Davison,
Formin Is Associated with Left-Right Asymmetry in the Pond Snail and the Frog.
2016,
Pubmed
,
Xenbase
Frasnelli,
Left-right asymmetries of behaviour and nervous system in invertebrates.
2012,
Pubmed
Fuller,
Rab23 regulates Nodal signaling in vertebrate left-right patterning independently of the Hedgehog pathway.
2014,
Pubmed
Gardner,
Normal bias in the direction of fetal rotation depends on blastomere composition during early cleavage in the mouse.
2010,
Pubmed
Géminard,
The myosin ID pathway and left-right asymmetry in Drosophila.
2014,
Pubmed
Gros,
Cell movements at Hensen's node establish left/right asymmetric gene expression in the chick.
2009,
Pubmed
,
Xenbase
Guerra,
Functional conservation between mammalian MGRN1 and plant LOG2 ubiquitin ligases.
2013,
Pubmed
Harland,
In situ hybridization: an improved whole-mount method for Xenopus embryos.
1991,
Pubmed
,
Xenbase
Hashimoto,
Molecular genetic analysis of left-right handedness in plants.
2002,
Pubmed
Heacock,
Clockwise growth of neurites from retinal explants.
1977,
Pubmed
Hoffman,
The incidence of congenital heart disease.
2002,
Pubmed
Hozumi,
An unconventional myosin in Drosophila reverses the default handedness in visceral organs.
2006,
Pubmed
Ishida,
An Arabidopsis thaliana tubulin mutant with conditional root-skewing phenotype.
2007,
Pubmed
Ishida,
Helical microtubule arrays in a collection of twisting tubulin mutants of Arabidopsis thaliana.
2007,
Pubmed
Janke,
Post-translational regulation of the microtubule cytoskeleton: mechanisms and functions.
2011,
Pubmed
Jiao,
Transgenic analysis of the physiological functions of Mahogunin Ring Finger-1 isoforms.
2009,
Pubmed
Jones,
The mouse neurological mutant flailer expresses a novel hybrid gene derived by exon shuffling between Gnb5 and Myo5a.
2000,
Pubmed
Kamura,
Pkd1l1 complexes with Pkd2 on motile cilia and functions to establish the left-right axis.
2011,
Pubmed
Klar,
Support for the selective chromatid segregation hypothesis advanced for the mechanism of left-right body axis development in mice.
2008,
Pubmed
Kondratova,
Poliovirus protein 3A binds and inactivates LIS1, causing block of membrane protein trafficking and deregulation of cell division.
2005,
Pubmed
Kuroda,
Canonical Wnt signaling in the visceral muscle is required for left-right asymmetric development of the Drosophila midgut.
2012,
Pubmed
Kuroda,
Chiral blastomere arrangement dictates zygotic left-right asymmetry pathway in snails.
2009,
Pubmed
Levin,
Left-right patterning from the inside out: widespread evidence for intracellular control.
2007,
Pubmed
Levin,
Asymmetries in H+/K+-ATPase and cell membrane potentials comprise a very early step in left-right patterning.
2002,
Pubmed
,
Xenbase
Levin,
Two molecular models of initial left-right asymmetry generation.
1997,
Pubmed
,
Xenbase
Levin,
A molecular pathway determining left-right asymmetry in chick embryogenesis.
1995,
Pubmed
Levin,
Gap junctions are involved in the early generation of left-right asymmetry.
1998,
Pubmed
,
Xenbase
Lobikin,
Early, nonciliary role for microtubule proteins in left-right patterning is conserved across kingdoms.
2012,
Pubmed
,
Xenbase
Logan,
The transcription factor Pitx2 mediates situs-specific morphogenesis in response to left-right asymmetric signals.
1998,
Pubmed
Lohr,
Left-right asymmetry of a nodal-related gene is regulated by dorsoanterior midline structures during Xenopus development.
1997,
Pubmed
,
Xenbase
Lowery,
Neural Explant Cultures from Xenopus laevis.
2012,
Pubmed
,
Xenbase
Lowery,
Growth cone-specific functions of XMAP215 in restricting microtubule dynamics and promoting axonal outgrowth.
2013,
Pubmed
,
Xenbase
Männer,
Does an equivalent of the "ventral node" exist in chick embryos? A scanning electron microscopic study.
2001,
Pubmed
McDowell,
Non-canonical ubiquitylation: mechanisms and consequences.
2013,
Pubmed
McGrath,
Two populations of node monocilia initiate left-right asymmetry in the mouse.
2003,
Pubmed
Meno,
Left-right asymmetric expression of the TGF beta-family member lefty in mouse embryos.
1996,
Pubmed
Meno,
Two closely-related left-right asymmetrically expressed genes, lefty-1 and lefty-2: their distinct expression domains, chromosomal linkage and direct neuralizing activity in Xenopus embryos.
1997,
Pubmed
,
Xenbase
Monsoro-Burq,
A rapid protocol for whole-mount in situ hybridization on Xenopus embryos.
2007,
Pubmed
,
Xenbase
Naganathan,
Active torque generation by the actomyosin cell cortex drives left-right symmetry breaking.
2014,
Pubmed
Nakamura,
Generation of robust left-right asymmetry in the mouse embryo requires a self-enhancement and lateral-inhibition system.
2006,
Pubmed
Nakamura,
Reduced cell number in the hindgut epithelium disrupts hindgut left-right asymmetry in a mutant of pebble, encoding a RhoGEF, in Drosophila embryos.
2013,
Pubmed
Nakamura,
A mutation in the Arabidopsis gamma-tubulin-containing complex causes helical growth and abnormal microtubule branching.
2009,
Pubmed
Okumura,
The development and evolution of left-right asymmetry in invertebrates: lessons from Drosophila and snails.
2008,
Pubmed
Okumura,
Class I myosins have overlapping and specialized functions in left-right asymmetric development in Drosophila.
2015,
Pubmed
Palmer,
From symmetry to asymmetry: phylogenetic patterns of asymmetry variation in animals and their evolutionary significance.
1996,
Pubmed
Palmer,
Symmetry breaking and the evolution of development.
2004,
Pubmed
Peeters,
Human laterality disorders.
2006,
Pubmed
Petzoldt,
DE-Cadherin regulates unconventional Myosin ID and Myosin IC in Drosophila left-right asymmetry establishment.
2012,
Pubmed
Pohl,
Left-right patterning in the C. elegans embryo: Unique mechanisms and common principles.
2011,
Pubmed
Pramparo,
Global developmental gene expression and pathway analysis of normal brain development and mouse models of human neuronal migration defects.
2011,
Pubmed
Prokopenko,
Tissue distribution of PEBBLE RNA and pebble protein during Drosophila embryonic development.
2000,
Pubmed
Ramsdell,
Left-right asymmetry and congenital cardiac defects: getting to the heart of the matter in vertebrate left-right axis determination.
2005,
Pubmed
Raya,
Notch activity induces Nodal expression and mediates the establishment of left-right asymmetry in vertebrate embryos.
2003,
Pubmed
Rebagliati,
Zebrafish nodal-related genes are implicated in axial patterning and establishing left-right asymmetry.
1998,
Pubmed
,
Xenbase
Reller,
Prevalence of congenital heart defects in metropolitan Atlanta, 1998-2005.
2008,
Pubmed
Sampath,
Functional differences among Xenopus nodal-related genes in left-right axis determination.
1997,
Pubmed
,
Xenbase
Schonegg,
Timing and mechanism of the initial cue establishing handed left–right asymmetry in Caenorhabditis elegans embryos.
2014,
Pubmed
Schumacher-Bass,
Role for myosin-V motor proteins in the selective delivery of Kv channel isoforms to the membrane surface of cardiac myocytes.
2014,
Pubmed
Schweickert,
The nodal inhibitor Coco is a critical target of leftward flow in Xenopus.
2010,
Pubmed
,
Xenbase
Shibazaki,
Body handedness is directed by genetically determined cytoskeletal dynamics in the early embryo.
2004,
Pubmed
Sipe,
Lis1 mediates planar polarity of auditory hair cells through regulation of microtubule organization.
2013,
Pubmed
Sitaram,
Regulation of dynein localization and centrosome positioning by Lis-1 and asunder during Drosophila spermatogenesis.
2012,
Pubmed
Somers,
A RhoGEF and Rho family GTPase-activating protein complex links the contractile ring to cortical microtubules at the onset of cytokinesis.
2003,
Pubmed
Spéder,
Type ID unconventional myosin controls left-right asymmetry in Drosophila.
2006,
Pubmed
Spéder,
Strategies to establish left/right asymmetry in vertebrates and invertebrates.
2007,
Pubmed
Srivastava,
Mahogunin-mediated α-tubulin ubiquitination via noncanonical K6 linkage regulates microtubule stability and mitotic spindle orientation.
2014,
Pubmed
Stout,
Using plusTipTracker software to measure microtubule dynamics in Xenopus laevis growth cones.
2014,
Pubmed
,
Xenbase
Sumigray,
Lis1 is essential for cortical microtubule organization and desmosome stability in the epidermis.
2011,
Pubmed
Sun,
The novel functions of ubiquitination in signaling.
2004,
Pubmed
Supp,
Mutation of an axonemal dynein affects left-right asymmetry in inversus viscerum mice.
1997,
Pubmed
Tabin,
Do we know anything about how left-right asymmetry is first established in the vertebrate embryo?
2005,
Pubmed
Taniguchi,
Chirality in planar cell shape contributes to left-right asymmetric epithelial morphogenesis.
2011,
Pubmed
Tee,
Cellular chirality arising from the self-organization of the actin cytoskeleton.
2015,
Pubmed
Thitamadee,
Microtubule basis for left-handed helical growth in Arabidopsis.
2002,
Pubmed
Tingler,
Symmetry breakage in the frog Xenopus: role of Rab11 and the ventral-right blastomere.
2014,
Pubmed
,
Xenbase
Upadhyay,
Mahogunin Ring Finger-1 (MGRN1), a Multifaceted Ubiquitin Ligase: Recent Unraveling of Neurobiological Mechanisms.
2016,
Pubmed
Vandenberg,
It's never too early to get it Right: A conserved role for the cytoskeleton in left-right asymmetry.
2013,
Pubmed
,
Xenbase
Vandenberg,
A unified model for left-right asymmetry? Comparison and synthesis of molecular models of embryonic laterality.
2013,
Pubmed
Vandenberg,
Laterality defects are influenced by timing of treatments and animal model.
2012,
Pubmed
,
Xenbase
Vandenberg,
Far from solved: a perspective on what we know about early mechanisms of left-right asymmetry.
2010,
Pubmed
Vandenberg,
Normalized shape and location of perturbed craniofacial structures in the Xenopus tadpole reveal an innate ability to achieve correct morphology.
2012,
Pubmed
,
Xenbase
Vandenberg,
Perspectives and open problems in the early phases of left-right patterning.
2009,
Pubmed
Vick,
Flow on the right side of the gastrocoel roof plate is dispensable for symmetry breakage in the frog Xenopus laevis.
2009,
Pubmed
,
Xenbase
Wan,
Micropatterned mammalian cells exhibit phenotype-specific left-right asymmetry.
2011,
Pubmed
Wynshaw-Boris,
Lissencephaly and LIS1: insights into the molecular mechanisms of neuronal migration and development.
2007,
Pubmed
Xu,
Polarity reveals intrinsic cell chirality.
2007,
Pubmed
Yin,
The Talpid3 gene (KIAA0586) encodes a centrosomal protein that is essential for primary cilia formation.
2009,
Pubmed
Zhang,
Left-right asymmetry in the chick embryo requires core planar cell polarity protein Vangl2.
2009,
Pubmed
Zimdahl,
Lis1 regulates asymmetric division in hematopoietic stem cells and in leukemia.
2014,
Pubmed