Atypical Protein Kinase C Is Involved in the Evolutionarily Conserved PAR Protein Complex and Plays a Critical Role in Establishing Epithelia-specific Junctional Structures

doi:10.1083/jcb.152.6.1183

Published online 19 March 2001. doi:10.1083/jcb.152.6.1183

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© The Rockefeller University Press, 0021-9525/2001/3/1183/ $5.00
The Journal of Cell Biology, Volume 152, Number 6, March 19, 2001 1183-1196

Original Article

Atypical Protein Kinase C Is Involved in the Evolutionarily Conserved PAR Protein Complex and Plays a Critical Role in Establishing Epithelia-specific Junctional Structures

Atsushi Suzuki^a, Tomoyuki Yamanaka^a, Tomonori Hirose^a, Naoyuki Manabe^a, Keiko Mizuno^a, Miki Shimizu^a, Kazunori Akimoto^a, Yasushi Izumi^a, Tetsuo Ohnishi^a, and Shigeo Ohno^a
^a Department of Molecular Biology, Yokohama City University School of Medicine, Yokohama 236-0004, Japan

Correspondence to: Shigeo Ohno, Department of Molecular Biology, Yokohama City University School of Medicine, Kanazawa-ku, Yokohama 236, Japan. Tel:81-045-787-2596 Fax:81-045-785-4140 E-mail:ohnos{at}med.yokohama-cu.ac.jp.

We have previously shown that during early Caenorhabditis elegansembryogenesis PKC-3, a C. elegans atypical PKC (aPKC), playscritical roles in the establishment of cell polarity requiredfor subsequent asymmetric cleavage by interacting with PAR-3[Tabuse, Y., Y. Izumi, F. Piano, K.J. Kemphues, J. Miwa, andS. Ohno. 1998. Development (Camb.). 125:3607–3614]. Togetherwith the fact that aPKC and a mammalian PAR-3 homologue, aPKC-specificinteracting protein (ASIP), colocalize at the tight junctionsof polarized epithelial cells (Izumi, Y., H. Hirose, Y. Tamai,S.-I. Hirai, Y. Nagashima, T. Fujimoto, Y. Tabuse, K.J. Kemphues,and S. Ohno. 1998. J. Cell Biol. 143:95–106), this suggestsa ubiquitous role for aPKC in establishing cell polarity inmulticellular organisms. Here, we show that the overexpressionof a dominant-negative mutant of aPKC (aPKCkn) in MDCK II cellscauses mislocalization of ASIP/PAR-3. Immunocytochemical analyses,as well as measurements of paracellular diffusion of ions ornonionic solutes, demonstrate that the biogenesis of the tightjunction structure itself is severely affected in aPKCkn-expressingcells. Furthermore, these cells show increased interdomain diffusionof fluorescent lipid and disruption of the polarized distributionof Na⁺,K⁺-ATPase, suggesting that epithelial cell surface polarityis severely impaired in these cells. On the other hand, we alsofound that aPKC associates not only with ASIP/PAR-3, but alsowith a mammalian homologue of C. elegans PAR-6 (mPAR-6), andthereby mediates the formation of an aPKC-ASIP/PAR-3–PAR-6ternary complex that localizes to the apical junctional regionof MDCK cells. These results indicate that aPKC is involvedin the evolutionarily conserved PAR protein complex, and playscritical roles in the development of the junctional structuresand apico-basal polarization of mammalian epithelial cells.

Key Words: atypical PKC, tight junction, epithelial cell polarity, PAR-3,PAR-6

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