The development of handedness in left/right asymmetry

Nigel A. Brown; Lewis Wolpert

doi:10.1242/dev.109.1.1

journal article May 01, 1990

The development of handedness in left/right asymmetry

Nigel A. Brown Lewis Wolpert

Development Vol. 109 No. 1 pp. 1-9 · The Company of Biologists

View at Publisher Save 10.1242/dev.109.1.1

Abstract

ABSTRACT
The development of handed asymmetry requires a special mechanism for consistently specifying a difference between left and right sides. This is to be distinguished from both random asymmetry, and from those left/right differences that are mirror symmetrical. We propose a model for the development of handedness in bilateral animals, comprising three components. (I) A process termed conversion, in which a molecular handedness is converted into handedness at the cellular level. A specific model for this process is put forward, based on cell polarity and transport of cellular constituents by a handed molecule. (Ii) A mechanism for random generation of asymmetry, which could involve a reaction-diffusion process, so that the concentration of a molecule is higher on one side than the other. The handedness generated by conversion could consistently bias this mechanism to one side. (iii) A tissue-specific interpretation process which responds to the difference between the two sides, and results in the development of different structures on the left and right. There could be direct genetic control of the direction of handedness in this model, most probably through the conversion process. Experimental evidence for the model is considered, particularly the iv mutation in the mouse, which appears to result in loss-of-function in biasing, and so asymmetry is random. The model can explain the abnormal development of handedness observed in bisected embryos of some mammalian, amphibian and sub-vertebrate species. Spiral asymmetry, as seen in spiral cleavage and in ciliates, involves only conversion of molecular asymmetry to the cellular and multicellular level, with no separate interpretation step.

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References

50

[1]

Afzelius "A human syndrome caused by immotile cilia" Science (1976) 10.1126/science.1084576

[2]

Almirantes "Morphogenesis in an asymmetric medium" Bull. Math. Biol (1987) 10.1016/s0092-8240(87)90001-2

[3]

Anett "Genetic and nongenetic influences on handedness" Behav. Genet (1978) 10.1007/bf01072826

[4]

Boycott "On the inheritance of sinistrality in hmnaea peregra" Proc. Roy. Soc. (B) (1923)

[5]

Breitenbrecker "The inheritance of sex-limited bilateral asymmetry in Bruchus" Generics (1925)

[6]

Brown "The development of asymmetry: the sidedness of drug induced limb abnormalities is reversed in situs i11versus mice" Development (1989) 10.1242/dev.107.3.637

[7]

Brown "The development of handed asymmetry’ in aggregation chimeras of situs inversus mutant and wild-type mice" (1990)

[8]

Bruckner "Linkage mapping of a mouse gene, iv, that controls left-right asymmetry of the heart and viscera" Proc. nam. Acad. Sci. U.S.A (1989) 10.1073/pnas.86.13.5035

[9]

Collins "When left-handed mice live in right-handed worlds" Science (1975) 10.1126/science.1111097

[10]

Corballis "On the biological basis of human laterality" (1978)

[11]

Deuchar "The mechanism of axial rotation in the rat embryo: an experimental study in vitro" J. Embryo/. exp. Morph (1971)

[12]

Diver "Sinistrality in Limnaea peregra (Mollusca, Pulmonata); the problem of mixed broods" J. Genet (1938) 10.1007/bf02982368

[13]

Freeman "The developmental genetics of dextrality and sinistrality in the gastropod hymnea peregra" Willhelm Roux Arch. devl Biol (1982) 10.1007/bf00848443

[14]

Galloway "Evolution of helicity" Nature (1987) 10.1038/330204a0

[15]

Galloway "Reflections on the ambilaent helix" Experienria (1989) 10.1007/bf01954060

[16]

Govind "Critical period for determining claw asymmetry in developing lobsters. /" exp. Zoo/ (1989) 10.1002/jez.1402490107

[17]

Gustafson "Studies on the cellular basis of morphogenesis. Formation of the coelom, the mouth and the primary pore-canal" Expl Cell Res (1963) 10.1016/s0014-4827(63)80017-8

[18]

Handel "Situs inversus in homozygous mice without immotile cilia. /" Hered (1984) 10.1093/oxfordjournals.jhered.a109995

[19]

Horstadius

[20]

Hummel "Visceral inversion and associated anomalies in the mouse.l" Hered (1959)

[21]

Huxley (1963) 10.5962/bhl.title.6433

[22]

Kauffman "Control of sequential compartment formation in Drosophila" Science (1978) 10.1126/science.413193

[23]

Layton "Random determination of a developmental process. L" Hered (1976) 10.1093/oxfordjournals.jhered.a108749

[24]

Layton "Heart malformations in mice homozygous for a gene causing situs inversus" Binh Defects (1978)

[25]

Leporj "Orientation et situs viscerium et cordis chez les embryons jumeaux de cane" Mo11itore Zoo/. Ital (1967)

[26]

Mangold situs inversus bei Triton. Arch. Entwicklungsmech (1921)

[27]

Mckusick (1988)

[28]

Mcmanus "Hand clasping and arm folding: a review and a genetic model" All. Human Biol (1979) 10.1080/03014467900003931

[29]

Mellon "Limb morphology and function are transformed by contralateral nerve section in snapping shrimp" Nature (1978) 10.1038/272246a0

[30]

Morgan "Embryology and inheritance of asymmetry" (1977) 10.1016/b978-0-12-325750-5.50018-x

[31]

Morgan "On the biological basis of human laterality II. The mechanism of inheritance" Behav. Brain Sci (1978) 10.1017/s0140525x00074483

[32]

Nelsen "Maintenance and regulation of cellular handedness in Tetrahymena" Development (1989) 10.1242/dev.105.3.457

[33]

Nelsen "Non-genie inheritance of cellular handedness" Development (1989) 10.1242/dev.105.3.447

[34]

Neville (1976)

[35]

Oppenheimer "Asymmetry revisited" Amu. Zoo/ (1974) 10.1093/icb/14.3.867

[36]

Palmblad "Ultrastructural, cellular and clinicul features of the immotile-cilia syndrome" Ann. Rev. Med (1984) 10.1146/annurev.me.35.020184.002405

[37]

Policansky "Flatfish and the inheritance of asymmetries" Behav. Brain Sci (1982) 10.1017/s0140525x0001181x

[38]

Cellular interactions in early C. elegans embryos

James R. Priess, J.Nichol Thomson

Cell 1987 10.1016/0092-8674(87)90427-2

[39]

Purnell "Selection for asymmetrical bias in a behavioural character of D. Melanogaster" Heredity (1973) 10.1038/hdy.1973.94

[40]

Satin "Development of cardiac beat rate in early chick embryos is regulated by regional cues" Devi Biol (1988) 10.1016/0012-1606(88)90165-0

[41]

Schterenberg "Cytoplasmic determination and distribution of developmental potential in the embryo of Caenorhabditis elegans" BioEssays (1989) 10.1002/bies.950100402

[42]

Siebert "Anatomic findings in dicephalic conjoined twins: implications for morphogenesis" Teratology (1989) 10.1002/tera.1420400402

[43]

Smith "The genetics of a pattern" Genetics (1960) 10.1093/genetics/45.8.1039

[44]

Spemann "Uber asymmetriche Entwicklung und situs inversus viscerum be Zwillingen und Doppelbildungen" Arch. Entwicklungsmech (1919) 10.1007/bf02554405

[45]

Stalsberg "Mechanism of dextral looping of the embryonic heart" Am. J. Cardiol (1970) 10.1016/s0002-9149(70)80002-9

[46]

Sturtevant "The effects of unequal crossing over at the bar locus in Drosophila" Genetics (1925) 10.1093/genetics/10.2.117

[47]

Sui..Ston "Neuronal cell lineages in the nematode Caenorhabditis elegans" Cold Spring Harbour quant. Biol (1983) 10.1101/sqb.1983.048.01.049

[48]

The embryonic cell lineage of the nematode Caenorhabditis elegans

J.E. Sulston, E. Schierenberg, J.G. White et al.

Developmental Biology 1983 10.1016/0012-1606(83)90201-4

[49]

Wehrmaker "Right-left asymmetry and situs inversus in Triturus alpestria" Willhelm Roux Arch1v. devl Biol (1969) 10.1007/bf00576984

[50]

Wilhelmi "Experimentelle Untersuchungen uber situs inversus viscerum" Arch. Entwicklungmech (1921) 10.1007/bf02554577

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Metrics

344

Citations

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References

Details

Published: May 01, 1990
Vol/Issue: 109(1)
Pages: 1-9
License: View

Authors

N

Nigel A. Brown

1 MRC Experimental Embryology and Teratology Unit, St George’s Hospital Medical School, Cranmer Terrace, London, SW17 ORE, UK

L

Lewis Wolpert

University College and Middlesex Hospital School of Medicine 2 Department of Anatomy and Developmental Biology , , Windeyer Building, Cleveland Street, London, WIP 6D8, UK

Cite This Article

Nigel A. Brown, Lewis Wolpert (1990). The development of handedness in left/right asymmetry. Development, 109(1), 1-9. https://doi.org/10.1242/dev.109.1.1

The development of handedness in left/right asymmetry

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