Abstract
Possible roles of brain-derived signals in the regulation of embryogenesis are unknown. Here we use an amputation assay in Xenopus laevis to show that absence of brain alters subsequent muscle and peripheral nerve patterning during early development. The muscle phenotype can be rescued by an antagonist of muscarinic acetylcholine receptors. The observed defects occur at considerable distances from the head, suggesting that the brain provides long-range cues for other tissue systems during development. The presence of brain also protects embryos from otherwise-teratogenic agents. Overexpression of a hyperpolarization-activated cyclic nucleotide-gated ion channel rescues the muscle phenotype and the neural mispatterning that occur in brainless embryos, even when expressed far from the muscle or neural cells that mispattern. We identify a previously undescribed developmental role for the brain and reveal a non-local input into the control of early morphogenesis that is mediated by neurotransmitters and ion channel activity.
Highlights
Possible roles of brain-derived signals in the regulation of embryogenesis are unknown
To determine whether the brain is required for the onset and/or patterning of myotomes, we evaluated the muscle phenotype at two relevant time points, corresponding to the different myogenic waves: early- and late- stages after brain removal, respectively
Soon after brain removal, animals developing without a brain (BR−) began to display a notable decrease (−43 ± 7%) in the collagen density of the myotomes, compared to the control animals (Ctrl) (OD mean value of 64 ± 8 units for BR− group compared to 113 ± 13 units for Ctrl group; t-test P < 0.01; n = 79) (Fig. 1c, d, turquoise and magenta short arrows)
Summary
Possible roles of brain-derived signals in the regulation of embryogenesis are unknown. We use an amputation assay in Xenopus laevis to show that absence of brain alters subsequent muscle and peripheral nerve patterning during early development. We identify a previously undescribed developmental role for the brain and reveal a non-local input into the control of early morphogenesis that is mediated by neurotransmitters and ion channel activity. The brain and central nervous system (CNS) generate information that controls muscle activity to implement behavior in adult organisms. The CNS may provide an instructive influence over the behavior of multiple cell types during the establishment, repair and maintenance of complex anatomical patterns in vivo. Pattern regulation during regeneration requires neural signals. Possible roles of the brain (or brain-derived signals) for early patterning, long before behavior begins, remain unknown. Given the tandem physiology of nerves and muscles, might innervation help orchestrate the symphony of signals that leads to somitogenesis? Does the presumptive nervous system release instructive signals that might be involved in somitogenesis and muscle development? Is there any element of this process co-opted into muscle regeneration? the peripheral innervation forms a stereotypic and complex neural network, which must be precisely patterned in a way that integrates size and positional information across the whole body[24]
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