Right-Left Asymmetry of Cell Proliferation Predominates in Mouse Embryos Undergoing Clockwise Axial Rotation

Sue Ann Miller and Richard D. White
Department of Biology, Hamilton College, Clinton, New York


Anatomical Record 250:103-108 (1998)

Background: Differential growth is fundamental to most mechanisms proposed for axial rotation in amniotes. Other mechanisms, such as changes in cell shape are not consistently suggested by ultrastructure. Lateral asymmetries in cell proliferation exist in mouse and chick embryos undergoing normal, anti-clockwise axial rotation, but there has been no investigation of inverse, clockwise rotation, that could test the correlation.

Methods: We used the BALB/cHu - iv/iv, situs inversus mouse to test apparent correlation of lateral asymmetries with morphogenesis that we saw in cell division patterns of normally rotating mice. Proliferation indices were collected from tritium autoradiograms.

Results: Asymmetry of cell proliferation in inverse axial rotation is a mirror image of the pattern seen for normal axial rotation: right predominates over left. This asymmetry is statistically significant and correlates with morphology. Patterns of proliferation in constraining extraembryonic membranes, particularly visceral yolk sac, suggest that rotation could be pushed by uneven lateral growth as body and gut tubes form, for they are attached to these membranes.

Conclusions: Data from iv/iv mice provide additional evidence that differential growth, constrained by contiguous extraembryonic membranes, may drive closure of body and gut walls and contribute to axial rotation. Asymmetries of cell proliferation are likely consequences of genetic cascades, and will need to be incorporated with in situ information on gene activity.

Grant sponsor: Margaret Bundy Scott Fund; Grant sponsor: The Hamilton College Faculty Research Fund.

Summary Figure: Left-right asymmetry of cellular proliferation predominates at anti-clockwise axial rotation whereas right-left asymmetry of cellular proliferation predominates at clockwise axial rotation. Data represent 18 embryos from 10 litters of two randomly outbred stains of mice and 5 embryos from 4 litters of BALB/cHu - iv/iv. Data were collected from 50,089 cells in Theiler (1972) stages 12 to 15 (4 to 25 somite pairs). A. Schematics present composite data from somatopleure in rotating embryos. B. Statistical analyses of proliferation indices from somatopleure of the groups of embryos schematized in part A. Quantiles (90%, 75%, 50%, 25%, 10%) are shown by lines and boxes. Diamonds and circles indicate means with 95% confidence interval. Flatter diamonds and smaller comparison circles indicate greater confidence in a mean from a larger sample. Comparison circles that do not overlap indicate significantly different sets of data.

Normal mouse endoderm shows different asymmetries.

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Last Modified: 31 October 1999