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Possibilities and limitations of three-dimensional reconstruction and simulation techniques to identify patterns, rhythms and functions of apoptosis in the early developing neural tube

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Abstract

The now classical idea that programmed cell death (apoptosis) contributes to a plethora of developmental processes still has lost nothing of its impact. It is, therefore, important to establish effective three-dimensional (3D) reconstruction as well as simulation techniques to decipher the exact patterns and functions of such apoptotic events. The present study focuses on the question whether and how apoptosis promotes neurulation-associated processes in the spinal cord of Tupaia belangeri (Tupaiidae, Scandentia, Mammalia). Our 3D reconstructions demonstrate that at least two craniocaudal waves of apoptosis consecutively pass through the dorsal spinal cord. The first wave appears to be involved in neural fold fusion and/or in selection processes among premigratory neural crest cells. The second one seems to assist in establishing the dorsal signaling center known as the roof plate. In the hindbrain, in contrast, apoptosis among premigratory neural crest cells progresses craniocaudally but discontinuously, in a segment-specific manner. Unlike apoptosis in the spinal cord, these segment-specific apoptotic events, however, precede later ones that seemingly support neural fold fusion and/or postfusion remodeling. Arguing with Whitehead that biological patterns and rhythms differ in that biological rhythms depend “upon the differences involved in each exhibition of the pattern” (Whitehead in An enquiry concerning the principles of natural knowledge. Cambridge University Press, London, 1919, p. 198) we show that 3D reconstruction and simulation techniques can contribute to distinguish between (static) patterns and (dynamic) rhythms of apoptosis. By deciphering novel patterns and rhythms of developmental apoptosis, our reconstructions help to reconcile seemingly inconsistent earlier findings in chick and mouse embryos, and to create rules for computer simulations.

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Acknowledgments

The monoclonal anti-Pax3 antibody developed by Charles P. Ordahl was obtained from the Developmental Studies Hybridoma Bank, created by the NICHD of the NIH and maintained at The University of Iowa, Department of Biology, Iowa City, IA 52242.

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Author notes

  1. Stefan Washausen and Thomas Scheffel contributed equally to this work.

Authors and Affiliations

  1. Department Prosektur Anatomie, Westfälische Wilhelms-University, Vesaliusweg 2-4, 48149, Münster, Germany

    Stefan Washausen & Wolfgang Knabe

  2. Department of Psychiatry, Psychotherapy and Psychosomatics, Brandenburg Medical School, Campus Neuruppin, 16816, Neuruppin, Germany

    Thomas Scheffel

  3. Department of Informatics, Technical University, 09107, Chemnitz, Germany

    Guido Brunnett

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Washausen, S., Scheffel, T., Brunnett, G. et al. Possibilities and limitations of three-dimensional reconstruction and simulation techniques to identify patterns, rhythms and functions of apoptosis in the early developing neural tube. HPLS 40, 55 (2018). https://doi.org/10.1007/s40656-018-0222-1

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