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Vol. 9, Issue 3, 685-699, March 1998
and
*Department of Molecular and Cellular Physiology, Stanford
University School of Medicine, Stanford, California 94305; and
In nonpolarized epithelial cells, microtubules originate from a
broad perinuclear region coincident with the distribution of the Golgi
complex and extend outward to the cell periphery (perinuclear [PN]
organization). During development of epithelial cell polarity,
microtubules reorganize to form long cortical filaments parallel to the
lateral membrane, a meshwork of randomly oriented short filaments
beneath the apical membrane, and short filaments at the base of the
cell; the Golgi becomes localized above the nucleus in the subapical
membrane cytoplasm (apiconuclear [AN] organization). The AN-type
organization of microtubules is thought to be specialized in polarized
epithelial cells to facilitate vesicle trafficking between the
trans-Golgi Network (TGN) and the plasma membrane. We describe two
clones of MDCK cells, which have different microtubule distributions:
clone II/G cells, which gradually reorganize a PN-type distribution of
microtubules and the Golgi complex to an AN-type during development of
polarity, and clone II/J cells which maintain a PN-type organization.
Both cell clones, however, exhibit identical steady-state polarity of
apical and basolateral proteins. During development of cell surface
polarity, both clones rapidly establish direct targeting pathways for
newly synthesized gp80 and gp135/170, and E-cadherin between the TGN
and apical and basolateral membrane, respectively; this occurs before
development of the AN-type microtubule/Golgi organization in clone II/G
cells. Exposure of both clone II/G and II/J cells to low temperature
and nocodazole disrupts >99% of microtubules, resulting in: 1)
25-50% decrease in delivery of newly synthesized gp135/170 and
E-cadherin to the apical and basolateral membrane, respectively, in
both clone II/G and II/J cells, but with little or no missorting to the
opposite membrane domain during all stages of polarity development; 2)
~40% decrease in delivery of newly synthesized gp80 to the apical
membrane with significant missorting to the basolateral membrane in
newly established cultures of clone II/G and II/J cells; and 3)
variable and nonspecific delivery of newly synthesized gp80 to both
membrane domains in fully polarized cultures. These results define
several classes of proteins that differ in their dependence on intact
microtubules for efficient and specific targeting between the Golgi and
plasma membrane domains.
Division of Nephrology, Indiana University School of
Medicine, Indianapolis, Indiana 46236
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