Segmental specificity and lateral asymmetry in the differentiation of developmentally homologous neurons during leech embryogenesis.
This paper describes the embryonic development of three leech neurons which undergo spatially regulated patterns of differentiation. In leeches, the nervous system arises from an iterated array of embryonic cell lineages, and each neuron is represented by a set of bilaterally symmetric and segmentally repeated homologs. Two of the cells discussed here, the neurons nz4 and mz3, stain with antibodies to the neuropeptides SCP and FMRFamide during the course of their embryonic differentiation, but only a subset of the initially immunoreactive homologs continue to express this immunoreactivity into postembryonic life. Those nz4 cells which retain immunoreactivity are referred to as RAS neurons, and the persistently immunoreactive mz3 cells referred to as CAS neurons. The subset of homologs which show persistent expression is segment specific, such that the mature RAS and CAS neurons occupy different segmental domains. In addition, both neurons display a final pattern of expression which is laterally asymmetric, with only one of the two homologs in each segment maintaining the RAS or CAS phenotype. Asymmetric differentiation can occur in either orientation for any given segment, although there is a very strong tendency for the persistently immunoreactive cells to lie on opposite sides of successive segments. The fate of the transiently immunoreactive homologs is unclear, but labeling with intracellular lineage tracers suggests that there are some mz3 neurons which survive late into postemobryonic life and never express detectable levels of immunoreactivity. Intracellular lineage tracers also allowed us to follow the development of a third neuron, mz4, which does not stain for either peptide. The mz4 neuron is initially paired, but undergoes an asymmetric pattern of cell death which also shows a strong tendency to alternate sides in successive segments. These spatially coordinated patterns of neuronal survival and/or differentiation suggest that cell interactions play a role in determining the developmental choices made by individual neurons, and a subsequent paper will characterize those interactions through experimental manipulation.
Department of Anatomy and Cellular Biology, Harvard Medical School, Boston, Massachusetts 02115.
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Shankland
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Martindale
D000818:Animals; D015415:Biomarkers / Q000032:analysis; D002454:Cell Differentiation; D002490:Central Nervous System / Q000166:cytology / Q000196:embryology; D004625:Embryo, Nonmammalian / Q000648:ultrastructure; D007839:Functional Laterality; D007865:Leeches / Q000196:embryology*; D009024:Morphogenesis; D009474:Neurons / Q000032:analysis / Q000166:cytology*; D013045:Species Specificity
D015415:Biomarkers