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Uncoupling Histogenesis from Morphogenesis in the Vertebrate Embryo by Collapse of the Transneural Tube Potential

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Uncoupling Histogenesis from Morphogenesis in the Vertebrate Embryo by Collapse of the Transneural Tube Potential DEVELOPMENTAL DYNAMICS 203456467 (1995) Uncoupling Histogenesis From Morphogenesis in the Vertebrate Embryo by Collapse of the Transneural Tube Potential RICHARD B. BORGENS AND RIYI SHI Center for Paralysis Research, Department of Anatomy, School of Veterinary Medicine, Purdue University, West Lafayette, IN 4 7907-1244 ABSTRACT We have shown that unidirec- rostra1 end. This tube of presumptive neuroepithelium tional pumping of Na+ out of the neural tube’s is formed by a progressive infolding and dorsal fusion luminal fluids in amphibian embryos produces a of surface ectoderm. The neural tube forms a functional large potential difference (40-90 mV, lumen nega- epithelial syncytium, clearly possessing an energy de- tive to the abluminal surface). This transneural pendent polarized ion transporting capability (specifi- tube potential (TNTP) is analogous to the Na+ de- cally moving Na+ across itself from inside to outside). pendent transepithelial potential (TEP)that exists This same unidirectional movement of Na+ also pro- across surface ectoderm. This TEP is retained in duces a potential difference across embryonic surface ectoderm after it is internalized when the neural ectoderm of about 50 mV (inside positive with respect folds fuse to form the neural tube. The TNTP can to the outside). The embryonic transepithelial poten- be markedly reduced for several hours by injec- tial (TEP) resulting from the unidirectional ion trans- tion of the Na+ channel blockers amiloride or ben- port is established very early in development, as early zamil into the lumen by iontophoresis through mi- as the blastula stage (Regen and Steinhardt, 1986; croelectrodes. Here we describe the effect of Slack and Warner, 1973; McCaig and Robinson, 1982; TNTP modification on developmental anatomy. Robinson and Stump, 1984; Metcalf et al., 1994; Rob- Axolotl embryos possessing a fused and closed inson et al., 1991). The TEP is retained in surface ec- neural tube (stage 21-23) were injected with either toderm after fusion of the neural folds to form the neu- amiloride or benzamil and allowed to continue de- ral tube in both frog, Xenopus laeuis, and salamander, velopment for 36-52 hr. These were compared to Ambystoma mexicanum, embryos (Hotary and Robin- control embryos injected with vehicle alone, or to son, 1991; Shi and Borgens, 1994). We have further embryos in which amiloride or benzamil was ion- demonstrated that the polarity and Na + dependence of tophoresed just beneath surface ectoderm. All em- the potential expressed across the wall of the internal- bryos in which the TNTP was reduced were ized neural tube is retained from its predecessor. This grossly defective. These were characterized by a is reflected as a striking transneural tube potential disaggregation of the cells comprising the struc- (TNTP) ranging from 40-90 mV, inside (luminal do- tures that had already begun to form (otic primor- main) negative with respect to the extracellular envi- dia, brain, spinal cord, notochord) as well as a fail- ronment of the embryo (Shi and Borgens, 1994). More- ure in the development of new structures. over the TNTP is sensitive to the same specific Na+ Remarkably, some of these embryos displayed channel blocking agents (amiloride and benzamil) as continuing development of external form in the surface ectoderm (Sariban-Sohraby and Benos, 1986). complete absence of concomitant internal histoge- Application of these agents only to the apical surface of nesis. We discuss the ways in which a large endog- surface ectoderm results in a marked, yet temporary, enous voltage gradient associated with an epithe- suppression of the TEP. Since the lumen of the neural lial potential difference (the TNTP) may be tube was once the external environment of the embryo, required both for the structural integrity of the the former apical surface of the ectoderm becomes the early neuroepithelium, and a prerequisite for nor- luminal surface of the neural tube. Amiloride or ben- mal morphogenesis. o 1995 Wiley-Liss, Inc. zamil iontophoresed into the lumen through microelec- trodes (final concentration in CSF, approximately 5 Key words: Neural tube, Electric fields, Morpho- pM) also resulted in a temporary reduction (or col- genesis, Cranial development, So- lapse) of the TNTP. Na+ transport through epithelia dium potential can also be facilitated by application of the antibiotic INTRODUCTION Well before the differentiation of glia and neurons, Received December 22, 1994; accepted March 28, 1995. Address reprint requestsicorrespondence to Richard B. Borgens, the vertebrate brain and spinal cord are established as Center for Paralysis Research, School of Veterinary Medicine, 1244 a closed tube of embryonic epithelium, enlarged on the VCPR, Purdue University, West Lafayette, IN 47907-1244. 0 1995 WILEY-LISS, INC. EFFECT OF TNTP ON DEVELOPMENTAL ANATOMY 457 novobiocin (Johnson and Hoshiko, 1971; Rick et al., 1988) to the apical surface. This results in a modest wmai Vehicle increase in TEP, and in our studies, a modest (510%) boost in the TNTP (Shi and Borgens, 1994). Modulation of Na+ transport through the use of these agents re- veals the general physiological properties of this pre- sumptive neuroepithelium. Our laboratory has previously reported the existence of a three-dimensional coordinate system of extracellu- Amilorlde Benzamll lar voltages that appear at the beginning of neurula- tion and disappear at its climax (Shi and Borgens, 1995; see also Metcalf et al., 1994). These voltage gra- dients are produced by ionic currents driven through the embryo in predictable patterns by the TEP of sur- face ectoderm. Furthermore, these gradients not only partition the embryo into domains, but are required for normal morphogenesis. Interruption of internal elec- tric fields by precisely applied voltages causes predict- I1 able, and marked, abnormalities in later development (Metcalf and Borgens, 1994). We have further investi- gated if the voltage retained across the walls of the newly formed neural tube is required for subsequent morphogenesis and differentiation (Shi and Borgens, 1994). In this study we reduced the TNTP in order to test its relevance to ontogeny. Experimentally treated embryos were compared to controls that underwent iontophoresis of vehicle alone, or in which these agents Fig. 1. The effect of TNTP reduction on embryonic development. The were injected beneath the embryo's surface ectoderm. first two vertical bars show the normal TNTP (of about 80 mV) was unaffected by iontophoresis of vehicle (microelectrode filling solution: 100 Our preliminary evaluation revealed that severe devel- mM Na'CI) into the lumen of stage 21-23 axolotl embryos. A typical opmental abnormality resulted from reduction or col- stage 34 embryo is illustrated directly below these bars to show that such lapse of the TNTP (Shi and Borgens, 1994; Fig. 1). Here manipulation had no effect on subsequent embryonic development. Bars we describe the developmental anatomy of experimen- three and four show that the TNTP was reduced by more than 50% following iontophoresis of the Na + channel blockers amiloride or ben- tal and control embryos in detail and show that not zamil into the lumen of the neural tube shortly after its fusion. The result only is the TNTP required for normal histogenesis, of these manipulations produced grossly abnormal forms, many that re- morphogenesis, and development, but that its collapse mained viable for at least as long as control embryos which were killed at can lead to the uncoupling of the global controls of stage 34-36. Beneath the amiloride bar, a headless form is illustrated. pattern formation from the differentiation of the em- Such embryos were devoid of any cranial development. Beneath the benzamil bar an embryo is shown in which typical cranial structures were bryo's internal structures. Furthermore, we suggest observed to be missing (optic, otic, olfactory, or gill primordia) and the that the defective developmental anatomy results from neural tube had exvaginated along its dorsal surface. Both of these forms a disaggregation of cells-not their demise-and that were extreme examples of teratogenesis and were not viable. (This sum- this loss in neuroepithelial structure interrupts an mary figure reconstructs data presented in Shi and Borgens, 1994.) early step in morphogenesis, undermining the funda- mental organization of the developing embryo. vehicle lasted approximately 10 min, after which em- bryos were studied for varying times (36-52 hr) until RESULTS they were killed and evaluated histologically (Table 1). Experimental and Control Groups Equal populations of embryos in which benzamil and All embryos were manipulated experimentally fol- amiloride were iontophoresed into the lumen of the lowing complete closure of the neural folds forming the neural tube were studied. Amiloride treated embryos neural tube (stages 21-22; Bordzilovskaya et al., 1989). were affected most severely, however, and 4 of the 9 Three control populations were used for histological embryos viable past stage 30131 are described here, as comparison: animals in which (1) benzamil or (2) well as 10 of 13 viable benzamil treated embryos. The amiloride was injected beneath the rostra1 surface ec- balance were either grossly deformed individuals toderm, and (3) a group in which vehicle (see Methods) (many times completely lacking a cranial enlarge- was iontophoresed into the lumen of the neural tube. ment) or were not viable to stage 30131 (refer to their These were compared to two experimental groups description in Shi and Borgens, 1994). where either benzamil or amiloride was injected into It is important to emphasize that at the time of mi- the lumen of the neural tube. The methodology used for croelectrode impalement of the neural tube, all em- iontophoresis was identical in all cases. The procedures bryos possessed a stable TNTP. This TNTP indicated used for the iontophoresis of pharmacological agents or the formation of a distinct neural tube, closed and iso- 458 BORGENS AND SHI TABLE 1. Developmental Responses to Reduction of the Transneural Tube Potential Internal structuresa Embryo Abnormal/ Neural Application number totalb Optic Otic Olfac.
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