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© The Rockefeller University Press,
0021-9525/2000//915 $5.00
The Journal of Cell Biology, Volume 149, Number 4,
, 2000 915-930
Original Article |
Caenorhabditis elegans β-G Spectrin Is Dispensable for Establishment of Epithelial Polarity, but Essential for Muscular and Neuronal Function
benne012{at}mc.duke.edu
The Caenorhabditis elegans genome encodes one
spectrin subunit, a β spectrin subunit (β-G), and a β-H spectrin subunit. Our experiments show that the phenotype resulting from the loss of the C. elegans spectrin is reproduced by tandem depletion of both β-G and β-H spectrins. We propose that spectrin combines with the β-G and β-H subunits to form /β-G and /β-H heteromers that perform the entire repertoire of spectrin function in the nematode. The expression patterns of nematode β-G spectrin and vertebrate β spectrins exhibit three striking parallels including: (1) β spectrins are associated with the sites of cell–cell contact in epithelial tissues; (2) the highest levels of β-G spectrin occur in the nervous system; and (3) β spec-trin-G in striated muscle is associated with points of attachment of the myofilament apparatus to adjacent cells. Nematode β-G spectrin associates with plasma membranes at sites of cell–cell contact, beginning at the two-cell stage, and with a dramatic increase in intensity after gastrulation when most cell proliferation has been completed. Strikingly, depletion of nematode β-G spectrin by RNA-mediated interference to undetectable levels does not affect the establishment of structural and functional polarity in epidermis and intestine. Contrary to recent speculation, β-G spectrin is not associated with internal membranes and depletion of β-G spectrin was not associated with any detectable defects in secretion. Instead β-G spectrin-deficient nematodes arrest as early larvae with progressive defects in the musculature and nervous system. Therefore, C. elegans β-G spectrin is required for normal muscle and neuron function, but is dispensable for embryonic elongation and establishment of early epithelial polarity. We hypothesize that heteromeric spectrin evolved in metazoans in response to the needs of cells in the context of mechanically integrated tissues that can withstand the rigors imposed by an active organism.
Key Words: membrane skeleton • unc-70 • RNAi • cell–cell contact
© 2000 The Rockefeller University Press
S. Moorthy and L. Chen contributed equally to this work.Abbreviations used in this paper: β-G, C. elegans β spectrin; β-H, βHeavy; dsRNA, double-stranded RNA; ORF, open reading frame; PH, pleckstrin homology; RNAi, RNA-mediated interference; ssRNA, single-stranded RNA.
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