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Left-Right Asymmetry in Vertebrate Embryogenesis

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Left-Right Asymmetry in Vertebrate Embryogenesis Michael Levin Summary Embryonic development results in animals whose body plans exhibit a variety of symmetry types. While significant progress has been made in understanding the molecular events underlying the early specification of the antero-posterior and dorso-ventral axes, little information has been available regarding the basis for left-right (LR) differences in animal morphogenesis. Recently however, important advances have been made in uncovering the molecular mechanisms responsible for LR patterning. A number of genes (including well-known signaling molecules such as Sonic hedgehog and activin) are asymmetrically expressed in early chick embryos, well before the appearance of morphological asymmetries. One of these, nodal, is asymmetrically expressed in frogs and mice as well, and its expression is altered in mouse mutants exhibiting defects in laterality. In the chick, these genes regulate each other in a sequential cascade, which Accepted independently determines the situs of the heart and other organs. 20 December 1996 Introduction ferences between the left and right sides of an animal’s mor- The geometrical invariance known as symmetry is a striking phology. This specifically excludes pseudo-random charac- feature of developmental morphology during embryogen- teristics such as coat colors, and minor stochastic deviations esis. There are several types, such as translational symme- due to developmental noise. Thus, to count as true LR asym- try (resulting in repeated units, such as embryonic somites or metry, a feature has to appear consistently in all normal indi- millipede segments) and reflectional symmetry (resulting viduals. Here, I also purposefully neglect behavioral/sensory from two or more sections of an organism looking the same asymmetries (such as lobster claws, which are determined to some level of detail on either side of a symmetry line). Ani- by neurological activity) and morphological/structural brain mal body plans occur in a wide variety of symmetries: spher- lateralization phenomena (reviewed in ref. 1). I avoid these ical (volvox), radial (starfish), chiral (snails, ciliates), bilateral issues because they are likely to be secondary (develop- (drosophila) and pseudo-bilateral(man). Vertebrates have a mentally) to basic body situs; also, they are confounded by generally bilaterally symmetrical body plan, but this sym- environmental influences, making them less tractable. metry is broken further into a pseudo-symmetryby the consis- The LR axis itself follows automatically from the definition tently asymmetric placement of various internal organs such of the antero-posteroir (AP) and dorso-ventral (DV) axes, as as the heart, liver, spleen and gut, or an asymmetric develop- it is perpendicular to both; however, consistently imposed ment of paired organs (such as brain hemispheres or lungs). asymmetry across it is fundamentally different from pattern- Symmetries are repeatedly broken during development. ing along the other two axes. Firstly, while the AP and DV For example, the radial symmetry of the early chick blasto- axes can be set by exogenous cues such as gravity or derm is broken into a bilateral symmetry by the appearance sperm entry point, there is no independent way to pick out of Kohler’s sickle and then the primitive streak. This is fur- ther broken into a definitive pseudo-symmetry by the right- the left (or right) direction, since no obvious macroscopic sided looping of the heart tube. In contrast, the sea-urchin aspect of nature differentiates left from right. One possible develops from a bilaterally symmetric larva into an adult with way to use a fundamental force to orientate the LR axis rela- a fivefold radial symmetry. tive to the other two axes was suggested by Huxley and Arguably, the most interesting asymmetry in vertebrate deBeer(*).They proposed that LR asymmetry was oriented development is that along the left-right (LR) axis. In this dis- during embryonic development by an electric current run- cussion, I limit LR asymmetry to include only invariant (i.e. ning down the length of the notochord, which would gener- consistent among all normal individuals of a given type) dif- ate a magnetic field pointing right or left, if measured at the dorsal or ventral sides. There is, however, no good evidence under the other, many crustaceans have specialized right for such a mechanism. and left fore-limbs, some flatfish consistently settle on and Secondly,all normal members of a given species are asym- undergo eye migration to one side, and there is even a metrical in the direction. However, animals with com- species of parasite (the arthropod Bopyrus) which lives only plete mirror reversal of internal organs can arise (situsinver- on one side of host prawn and shrimp. Meanwhile, there has sus) and are otherwise phenotypically unimpaired. Thus, while been little information shedding light on the mechanisms it is possible to come up with plausible evolutionary reasons for determining the sidedness of the asymmetries. Selection for why organisms might be asymmetric in the first place (optimal LR asymmetries in Drosophila, in the hopes of generating a packing of viscera, etc.), there is no obvious reason for why genetically tractable mutant, failed(13). they should all be asymmetric to the same direction. It is, after Several experiments have shed light on the timing of LR all, much easier to imagine a developmental mechanism for asymmetry specification. Chick heart sidedness has been generating asymmetry (such as positive-feedbackand amplifi- experimentally demonstrated to be determined during gas- cation of stochastic biochemical differences) than for biasing it trulation(14);studies on LR inversions induced by drugs like- to a given direction. The left-right axis thus presents several wise suggest that in mammals, a critical period in LR biasing unique and deeply interesting theoretical issues. occurs before late gastrulation(15). Besides the intrinsic interest to those working on funda- Several kinds of molluscs undergo spiral cleavage and mental morphogenetic mechanisms, LR asymmetry is also secrete an exoskeleton shaped like a conical spiral. In 3-D relevant to medical considerations of several fairly common space, such spirals can have two possible variants: a left- human birth defects: syndromes such as Kartagener’s and handed and a right-handed helix (which are otherwise identi- Ivemark’d3),dextrocardia, situs inversus (a complete mirror- cal). Each particular species of snail has invariant (consis- image reversal of the sidedness of asymmetrically posi- tent) chirality, but there are species which utilize each type of tioned organs and asymmetric paired organs), heterotaxia coiling. Murray and Clarke(16)found that the direction of coil- (where each organ makes an independent decision as to its ing of /? suturalis is maternally inherited and sinistrality is situs), and right or left isomerism (where the organism dominant to dextrality. Freeman and L~ndelius(’~),studying a is completely symmetrical, for example, polysplenia or different species, found that dextrality is dominant; interest- asplenia).Of these, only the complete (and rare) situs inversus ingly, the dextral gene apparently functions via a cytoplasmic is not associated with physiological difficulties. The rest, espe- product since it is possible to transfer (by micropipette) cyto- cially heterotaxia, often result in serious health problems for plasm from the dextral variant of the snail into the sinistral the patient. Laterality defects can arise in a single individual variety, and thus rescue the phenotype. The biochemical but are especially associated with monozygotic t~inning(~-~).nature of this activity has not yet been identified. There are a variety of drugs which, within defined dose Pre-molecular data windows, cause defects in a LR-asymmetric manner or ran- While molecular mechanisms underlying antero-posterior domize asymmetry (Table 1). These form a basically unre- and dorso-ventral asymmetry have been studied in detail, lated group, which includes even such simple substances as the mechanistic basis for LR asymmetry was, until recently, cadmium. The drugs which cause worse limb defects on completely unknown. The bilateral body plan is thought to one side were suggested(18)to be due to a differential blood have originated with the eumetazoa, the evolution of an- supply to the two limbs (due to asymmetry in blood vessels terior-posterior body axis, unidirectional movement and exiting the heart). This is made somewhat unlikely by the cephalization probably occurring together, followed closely fact that cadmium causes opposite-sided defects in rats and by the triploblastic architecture of the body pland6).The LR mi~e(’~-~O),while cardiac anatomy and relative vessel size of axis is probably specified after the anterior-posterior (AP) both species are extremely similar (no known differences and dorso-ventral (DV) axes, and is determined with respect exist between rats and mice in this respect; W. Scott and M. to them(7-8).Echinoderms possess well-defined LR asym- Fujinaga, personal communication). This suggests a funda- metries, and amphioxus, considered to be the ancestor of mental difference between left and right limbs. The pharma- vertebrates, exhibits many LR a~ymmetries(~).Currently, cology of these drugs has not yet suggested anything about several morphological markers of LR asymmetry are appar- the normal mechanisms of LR patterning, except that an ent in vertebrates: heart, direction of embryo rotation,
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