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Ross Granville Harrison on the Origin of Embryonic Polarity MARTINA Bruecknern Dept

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Ross Granville Harrison on the Origin of Embryonic Polarity MARTINA Bruecknern Dept JOURNAL OF EXPERIMENTAL ZOOLOGY 301A:549–551 (2004) What Comes First: the Structure or the Egg? Ross Granville Harrison on the Origin of Embryonic Polarity MARTINA BRUECKNERn Dept. Pediatrics/Cardiology, Yale University School of Medicine, New Haven, Connecticut 06520 Ross Granville Harrison’s paper ‘‘ On relations independent analysis of Harrison’s experiments of symmetry in transplanted limbs,’’ published in just based on the raw data in the manuscript, and JEZ in 1921 investigated the mechanism govern- for that reader to form independent conclusions ing the development of embryonic axes through not influenced by those Harrison himself pre- systematic transplantation experiments on the sented later in the paper. forelimb of the salamander, Amblystoma puncta- The conclusions that Harrison did draw from tum. The questions these experiments addressed his experiments far outlasted the experiments remain as fundamental, and largely unanswered, themselves, however. The experiments were today as they were over 80 years ago: how does an sparked by a discrepancy in observations between embryo establish its three axes, and how is this two notable embryologists of that time, Streeter positional information conveyed to developing and Spemann, regarding the equipotentiality of organs? The experiments themselves exemplified the ear placode. Although the discrepancy turned the transition from embryology as a purely des- out to be spurious, the questions raised by those criptive field, to modern experimental embryology. observations lead Harrison to search for other Harrison’s interest in embryology began while equipotential developmental systems. The limb he was working towards his Ph.D., when he visited bud of Amblystoma presented a manipulable and Germany and studied the development of fins in observable model for the development of embryo- teleost fishes with Nussbaum. At that time in nic axes. The limb bud could be transplanted Germany, Wihelm Roux established a new journal either in its entirety, or in parts, both to the ‘‘Archiv fur Entwicklungsmechanik,’’ designed for normal location, and to a location which does not the study of mechanisms of development, as normally give rise to a limb. The degree to which opposed to mere description of developmental symmetry was pre-patterned in the limb bud could processes. It is highly likely that this shift in then be investigated by transplanting it to the approach to problems in developmental biology same or to the opposite side of the embryo, and by had a significant impact on Harrison also. Harri- positioning the transplanted limb with its dorsal- son was clearly an outstanding observer, and the ventral axis preserved or inverted. The outcome of care which he applied to the descriptive aspects of these experiments showed that limb buds can embryology becomes apparent in the JEZ paper. regulate their development in some respects: The experiments are systematic, and the docu- halved or doubled buds gave rise to a normal mentation of the experimental results is detailed limb. Thus, with regard to size regulation the limb and totally objective. The beautiful line drawings bud behaves as an equipotential system, which along with the detailed experimental histories can respond to information from the rest of the convey the actual experimental results more embryo and re-set its developmental program. accurately than many multicolor photoshop Development of asymmetry, however, presented a images in the current scientific literature. The more complex picture. data is presented exactly as Harrison saw it, not as he predicted it to be. For example, in figure 37, the nCorrespondence to: Martina Brueckner, Dept. Pediatrics/Cardiol- ogy, Yale University School of Medicine, 333 Cedar Street, Fitkin 430, transplanted limb is incidentally covered by the New Haven, CT 06520. gills, and Harrison does not alter the drawing to E-mail: [email protected] Received 29 March 2004; Accepted 30 March 2004 ‘‘move’’ the gills and make his observation more Published online in Wiley Interscience (www.interscience.wiley. obvious. It would be possible for a reader to do an com). DOI: 10.1002/jez.a.82 r 2004 WILEY-LISS, INC. 550 HARRISON AND EMBRYONIC POLARITY Harrison asks two predominating questions the ‘‘Existence of an equipotential system neces- here: when is the adult form established in the sitates, in fact, the assumption of some sort of primordium, and what is the nature of the signal molecular hypothesis for the representation of that shapes the undifferentiated limb bud into the adult form in the germ.’’ Since each elementary adult limb? His experiments provided a partial unit comprising the limb bud is able to assume a answer to the first question, leading to the range of adult fates, depending on the environ- conclusion that ‘‘the posture and asymmetry of ment in which it develops, determination of form the limb is determined neither by the limb itself, must reside in the elementary unit itself, rather nor by its surroundings exclusively.’’ At the stage than in the arrangement of elementary units at of the transplants described in this manuscript, the time of transplantation. He then goes on to the anteroposterior axial differentiation is already describe a hypothetical carbon molecule, showing determined, while the dorsoventral specification is how progressive modification of the four side imposed on the limb bud by the surrounding chains leads to an asymmetric, chiral structure. tissue. To this day, the precise timing during This structure could provide the internal refer- development when a limb bud is specified remains ence found in each cell of the limb bud that would an area of active investigation (Tickle, 2003). For permit alignment along the anteroposterior axis, example, there are currently two differing models and thus determine the correct dorsoventral and describing the timing of specification of the left-right axes. Childs raised some major objec- proximo-distal axis of the limb, the ‘‘progress zone tions to the ‘‘molecular’’ approach. In particular, model’’ and the ‘‘early specification model’’ he suggested that ‘‘ protoplasms in general have (Dudley et al., 2002). In the progress zone model, not yet been shown to posses any structure that the different parts of the limb are progressively might serve as a basis for developmental pattern,’’ specified as the limb extends. In contrast, in the and advocated instead that the site of attachment early specification model, the fate of limb seg- of the egg established a metabolic gradient that ments along the proximo-distal axis is already formed the basis for the development of future encoded in the very early limb bud. Of note is that asymmetry. Harrison and the crystallographer recent experiments designed to address these W.T. Astbury went on to search for the molecular questions employed some of the same basic structures underlying developmental asymmetry experimental methods used by Harrison, the through the use of X-ray crystallography of air- transplantation of chick limb buds to other sites dried specimens of A. punctatum. These experi- of the embryo. The analysis today is guided by the ments were unsuccessful, largely not because the use of molecular markers, but the question idea would turn out to be wrong, but because of Harrison at least partially addressed using only the technical limitations of the experiments. careful observation has still not been definitively Harrison does not deny that gradients may have answered. a role in developing embryonic symmetry. For The second question, namely the nature of the example, he wrote that ‘‘It seems to the present embryonic signal specifying adult form, is the writer that such gradients may well be an principal subject of the discussion in his 1921 JEZ expression of polarity rather than its cause.’’ In paper, and was one that Harrison spent consider- other words, something, such as inherent mole- able time on in his subsequent scientific endea- cular asymmetry must initiate organismal asym- vors. At the time of Harrison’s experiments, a metry. The initial asymmetry can then be vigorous debate was ongoing between Harrison converted to a gradient. and Childs regarding the nature of this signal. What has been learned about development of Child and others espoused the idea that the embryonic symmetry since Harrison’s publica- phenomena of axial differentiation are the result tion? Strikingly, both gradients and underlying of gradients, which were thought to be metabolic molecular asymmetry have been shown to govern in nature. Harrison, on the other hand, questioned the formation of the 3 embryonic axes. In the existence of such gradients as the origin of Drosophila, a gradient of the bicoid molecule is embryonic axes, believing that there is a molecular one of the first steps in the creation of anteropos- basis underlying the development of asymmetry. terior axis. Notably, the bicoid gradient is regu- In the 1921 JEZ paper, the argument for a lated by cytoskeletal elements, which Harrison molecular determination of form arises from the alluded to when he stated that ‘‘in the egg, such an observation that the limb bud is, at least partially, arrangement of protein molecules would form a an equipotential system. Harrison concludes that lattice or framework in which substances could be M. BRUECKNER 551 differentially distributed.’’ The recent observa- biology, mouse knockouts, or genomics, but tions that provide the greatest support for Harri- through careful, thoughtful experimentation and son’s hypothesis of an underlying molecular observation alone. asymmetry are those concerning the development of the left-right axis. In this instance, the asym- LITERATURE CITED metric macromolecular structure has been identi- Abercrombie M. 1961. Ross Greenville Harrison, 1870–1959. fied. It is the axoneme of the cilium, which is a Biographical memoirs of fellows of the royal society 7:111–126. large, highly asymmetric macromolecular struc- Dudley AT, Ross MA, Tabin CJ. 2002. A re-examination of ture (McGrath and Brueckner, 2003). The cilium proximodistal patterning during vertebrate limb develop- is aligned relative to the anteroposterior and ment.
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