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Segmentation and Neural Develolm' Nt in Vertebrates Roger J

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Segmentation and Neural Develolm' Nt in Vertebrates Roger J 220 11 ~,',S - Mav 198.' Segmentation and neural develolm' nt in vertebrates Roger J. Keynes and Claudio D. Stern A prominent feature of the development of most higher orgamsms ts the sub&wsion between antenor and postermr sclero- of the embryo into a series of repeating elements, or segments. In vertebrates, the tome halves, rotation experiments degree to which the nervous system ts involved m thts process ts uncertain, and has were carried out s. First, a portion of received lmle attention recently. It may be relevant, however, to an understanding of neural tube opposite 2 or 3 somites was the mechanisms underlying neural development rotated 180" antero-posteriorly (A-P) prior to axon outgrowth, so that neural Segmentation in the vertebrate embryo had Lehmann earher, that 'segmenta- tube previously opposite anterior half- is most obvious in the repeating pattern tion of the spinal cord and peripheral semite came to lie opposite posterior of the somites, and this ~s reflected in nerves is entirely subservient to meso- half After 2 days of further develop- the adult by the serial arrangement of dermic segmentation and that an ment axons had still grown out through the vertebrae and their associated tntnnsic segmentation is non-existent ' the anterior halves of those somltes muscles, nerves, labs and blood vessels opposite the rotated neural tube It is also visible m the nervous system. Peripheral nerve segmentation in the Second, a portion of segmental plate Morphological segments in the neural chick embryo mesoderm, 2-4 presumptive somltes tube were first noticed by yon Baer m In re-examimng these phenomena in long, was rotated 180 ° A-P, this time, 1828 I, and came to be called neuro- the chick embryo, we were interested after further development, axons had meres Subsequently some authors first to know how motor and sensory traversed the postenor (original anter- took them as evidence, additmnal to axons growing from the neural tube ior) halves of the grafted somltes the existence of somites, that verte- region are related to the somites, wluch Axons therefore grow through anter- brates evolved from a primitive seg- he in longitudinal senes adjacent to the ior half-sclerotome, regardless of its mented ancestor, and that the verte- neural tube Twenueth century text- position relative to the neural tube or to brate head has a segmental ongin 2_ books of embryology descnbe the the A-P axis of the whole embryo However, this was not generally ac- spinal nerves of lugher vertebrates as These expenments confirm Lehmann's cepted 3,4 In particular, it was never developing either opposite the middle and Detwder's conclusion that seg- agreed whether neuromeres, most of each semite, or between somites. It mented axonal outgrowth is due to the obvious m the region of the developing was therefore surprising to find, In zinc somites. In addition, they show that in hmdbrain (Fig 1), extend the full lodide-osmmm tetroxide stained, the chick segmentation is due to a rostro-caudal extent of the neural tube whole-mounted embryos, that axons difference between anterior and pos- In a review on the subject in 1918, actually traverse the anterior (rostral) terior sclerotome cells Axons do not NeaP pointed out that 'there is not the half of the sclerotome of each serrate s grow out simultaneously along the slightest evidence that the neuromeres (and it was less surprising to find that length of the neural tube and then of the spinal cord are other than the this had been descnbed in 1855 by become secondarily segmented by the passive result of the mechamcal pres- Remak 9) (Figs 2, 3) To test whether developing sclerotome. Rather, they sure of the adjacent mesodermlc this segmented outgrowth occurs be- grow out in a punctuated manner, first somites'. Kallen s later produced some cause of intrinsic neural tube segmenta- axons exit opposite antenor half- ewdence that they represent locahsed tmn or because of some difference sclerotome, while later axons do exit regions of mitotic activity While Neal's opposite posterior half-sclerotome but statement continues to be vahd, the fasclculate on previously outgrown possibility that neuromeres have rather axons so as to diverge towards antenor more developmental significance re- half-sclerotome on either side s mains. In the earliest experimental studies Neural crest cells on neural segmentation, Lehmarm Weston 1°, using [3H]thymidme auto- and Detwiler wanted to know how the radiography, originally descnbed the penpheral nerves become segmentally ventral pathway of migrating truncal arranged. Specifically, they wondered neural crest cells as being through whether this is because of external sclerotome, but later studies using the constraints imposed on the outgrowing quail-chick chunaera system n, or a axons by the somites, or because the monoclonal antibody 12, put the major neural tube is lntnnsically segmented pathway between adjacent somttes_ with respect to the position of out- More recently, lmmunohtstochemical growth. Lehmann found that removal studies have confirmed Weston's re- of several consecutive somites in sults Furthermore, they have shown urodele embryos leads to a loss of that neural crest cells share the segmentation of sensory ganglia in the Fig. 1. Neuromeres m an unfired, stage 21 chick pathway of motor axons by m~grating operated region Detwder then went embryo The hmdbram region of the neural tube pnmarily through the anterior half of was opened out by a dorsal cut along the mtdlme, on to show that grafting an addltmnal and ~everal segments (rhombomeres) are visible each sclerotome (Rickmann, M , semite produces an additional spinal on each vide Photographed with reflected hght, Duband, J L, Fawcett, J W. nerve and ganglion He concluded, as × 200 Keynes, R. 1 and Thiery. J P , unpub- ~) 1985 Elsewer Soenoe Pubhshers B V Amsterdam 0378 5912/85/$(12 (~) TINS -May1985 221 stage when few or no sclerotome cells are present, motor axons have been described as being either between myotomes (Xenopus) or opposite the middle of the myotome At later stages, though, both motor and sensory axons and sensory ganglia are found in the anterior half-sclerotome. In apodan amphibia*, reptiles, birds and mammals, axons grow out at a stage by which the sclerotome is well devel- oped, and it is hkely that in these higher vertebrate classes the A-P subdivision simultaneously determines axonal seg- mentation s One interesting feature of the A-P subdivision of the vertebrate somtte is its parallel with the insect segment Insect epidermal segments can be Fig. 2. Transverse semz-thm section of a late stage-16 chtck embryo, at the level of the wing somttes, subdivided into antenor and posterior stamed wtth toluldme blue By the stage of motor axon outgrowth (arrow), the somue has developed mto 'compartments 'I7 A compa,tment in dermatome, myotome (D, M, respecttvely presumpUve dermt~ and skeletal muscle) and selerotome (S, this sense has been defined as compris- presumpttve vertebral column) NT, neural tube, NC, notochord Scale bar, 100 wn Reproduced with ing all the surviving descendants of a permission from Ref 8 ) small group of founder cells 17.1s We do hshed observations) (Fig 4) Fibronec- which occurs between axial muscles not know whether the anterior and tin, which has been suggested as being and vertebrae, both of which develop posterior sclerotome halves are also the controlling factor in the guidance of from the somites, Remak introduced developmental compartments, and the crest cells, IS localized mainly at the the concept of 'neughederung', or re- similarity IS, at best, a superficial one somite borders, as previously des- segmentation, whereby on each side of In Drosophila, a number of 'homo- crlbed 13, there was no detectable varia- the embryo the anterior half of one eotlc' genes have been Identified 19,2° tion in the A-P distribution of this mol- sclerotome merges rostrally with the whtch are believed to play a controlling ecule wsthln the somite This lmphes posterior half of the next sclerotome to role in the specification of segment that fibronectln does not play a critical form a vertebra That cells from one identity and polarity. For example, the role in determining the route taken by somtte can contnbute to two adjacent homoeottc gene engraded is revolved m crest cells or axons_ vertebrae has been confirmed recently determining the distinction between Since crest ceils precede motor axons using the quail-chick chimaera techm- posterior and anterior compartments m m the anterior half-sclerotome, one que is. However, the original descrip- Drosophda epidermal segments 2°_ A possibility would be that axons grow on tions of re-segmentation are open to short DNA sequence assocmted with crest cells However, surgical removal criticism I6, and further experiments several of these genes, which is of the neural crest does not alter the will be needed to examine this phenom- conserved in the vertebrate genome, segmented outgrowth of motor axons. enon in more detail It would appear, then, that whatever Whether the A-P subdivision deter- differences exist between anterior and mines axonal segmentation in all * The order Apoda comprises a group of legless posterior sclerotome cells and/or their vertebrates is less certain In fishes and amphibians living in South America, tropical extracellular matrices, they can be amphibia, axons normally grow out at a Africa, the Seychelles and south east Asta detected independently by axons and neural crest cells_ Comparisons with other species Does an A-P subdivision of the somlte exist m all vertebrate classes? The answer is probably yes_ Since Remak's onginal description of the development of the vertebral column in the chick embryo 9, it has been con- firmed in all vertebrate classes that the sclerotome subdivides into anterior and postenor halves which subse- quently differ in cell density s In the chick, a boundary, first descnbed by von Ebner 14, can be seen separating the two halves of the sclerotome in the middle of each somtte_ This Won Fig.
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