TY - JOUR
T1 - Mirror-imaged doublets of Tetmemena pustulata
T2 - Implications for the development of left-right asymmetry
AU - Bell, Aaron J.
AU - Satir, Peter
AU - Grimes, Gary W.
N1 - Funding Information:
This paper is dedicated to the memory of Dr. Gary W. Grimes, who died while this work was being completed. He was an exceptional scientist, friend and mentor. We thank Pauline Gould for help in generating the cell line used in this study. Special thanks to Dr. Joseph Frankel for critical reading and editing of this manuscript. We also thank Dr. Robert Hammersmith for species identification as well as Dr. Wilhelm Foissner and Dr. Laura Landweber. Finally, we thank the imaging facility at AECOM for assistance with some of the image preparation. The work is based in part on a thesis submitted by Aaron Bell for partial fulfillment of the requirements for an M.S. degree at Hofstra University. Aaron Bell is a fellow at Sue Golding Graduate Department at Albert Einstein College of Medicine. The work was partially funded by grants from NCI and NIDDK.
PY - 2008/2/1
Y1 - 2008/2/1
N2 - Ciliated protozoa possess cellular axes reflected in the arrangement of their ciliature. Upon transverse fission, daughter cells develop an identical ciliary pattern, ensuring perpetuation of the cellular phenotype. Experimentally manipulated cells can be induced to form atypical phenotypes, capable of intraclonal propagation and regeneration after encystment. One such phenotype in the ciliate Tetmemena pustulata (formerly Stylonychia pustulata) is the mirror-imaged doublet. These cells possess two distinct sets of ciliature, juxtaposed on the surfaces in mirror image symmetry, with a common anterior-posterior axis. We have examined whether individual ciliary components of Tetmemena mirror-image doublets are mirror imaged. Ultrastructural analysis indicates that despite global mirror imaging of the ciliature, detailed organization of the membranelles is reversed in the mirror-image oral apparatus (OA), such that the ciliary effective stroke propels food away from the OA. Assembly of compound ciliary structures of both OAs starts out identically, but as the structures associated with the mirror-image OA continue to form, the new set of membranelles undergoes a 180° planar rotation on the ventral surface relative to the same structures in the typical OA. The overall symmetry of the OA thus appears to be separable from the more localized assembly of individual basal bodies. True mirror imagery of the membranelles would require new enantiomorphic forms of the individual ciliary components, particularly the basal bodies, which is never observed. These observations suggest a mechanistic hypothesis with implications for the development of left-right asymmetry not only in ciliates, but perhaps also in development of left-right asymmetry in general.
AB - Ciliated protozoa possess cellular axes reflected in the arrangement of their ciliature. Upon transverse fission, daughter cells develop an identical ciliary pattern, ensuring perpetuation of the cellular phenotype. Experimentally manipulated cells can be induced to form atypical phenotypes, capable of intraclonal propagation and regeneration after encystment. One such phenotype in the ciliate Tetmemena pustulata (formerly Stylonychia pustulata) is the mirror-imaged doublet. These cells possess two distinct sets of ciliature, juxtaposed on the surfaces in mirror image symmetry, with a common anterior-posterior axis. We have examined whether individual ciliary components of Tetmemena mirror-image doublets are mirror imaged. Ultrastructural analysis indicates that despite global mirror imaging of the ciliature, detailed organization of the membranelles is reversed in the mirror-image oral apparatus (OA), such that the ciliary effective stroke propels food away from the OA. Assembly of compound ciliary structures of both OAs starts out identically, but as the structures associated with the mirror-image OA continue to form, the new set of membranelles undergoes a 180° planar rotation on the ventral surface relative to the same structures in the typical OA. The overall symmetry of the OA thus appears to be separable from the more localized assembly of individual basal bodies. True mirror imagery of the membranelles would require new enantiomorphic forms of the individual ciliary components, particularly the basal bodies, which is never observed. These observations suggest a mechanistic hypothesis with implications for the development of left-right asymmetry not only in ciliates, but perhaps also in development of left-right asymmetry in general.
KW - Cilia
KW - Cortical inheritance
KW - Global patterning
KW - Local assembly
KW - Spirotrichs
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U2 - 10.1016/j.ydbio.2007.11.020
DO - 10.1016/j.ydbio.2007.11.020
M3 - Article
C2 - 18164285
AN - SCOPUS:38349102189
SN - 0012-1606
VL - 314
SP - 150
EP - 160
JO - Developmental Biology
JF - Developmental Biology
IS - 1
ER -