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© The Rockefeller University Press, 0021-9525/1998//697 $5.00
The Journal of Cell Biology, Volume 142, Number 3, , 1998 697-710

Apical Polarity of N-CAM and EMMPRIN in Retinal Pigment Epithelium Resulting from Suppression of Basolateral Signal Recognition

Alan D. Marmorstein^*, Yunbo C. Gan^*, Vera L. Bonilha^*, Silvia C. Finnemann^*, Karl G. Csaky, and Enrique Rodriguez-Boulan^*

^* Margaret M. Dyson Vision Research Institute, Department of Ophthalmology and Department of Cell Biology and Anatomy, Cornell University Medical College, New York 10021; and Laboratory of Immunology, National Eye Institute, Bethesda, Maryland 20892

Retinal pigment epithelial (RPE) cells apically polarize proteins that are basolateral in other epithelia. This reversal may be generated by the association of RPE with photoreceptors and the interphotoreceptor matrix, postnatal expansion of the RPE apical surface, and/or changes in RPE sorting machinery. We compared two proteins exhibiting reversed, apical polarities in RPE cells, neural cell adhesion molecule (N-CAM; 140-kD isoform) and extracellular matrix metalloproteinase inducer (EMMPRIN), with the cognate apical marker, p75-neurotrophin receptor (p75-NTR). N-CAM and p75-NTR were apically localized from birth to adulthood, contrasting with a basolateral to apical switch of EMMPRIN in developing postnatal rat RPE. Morphometric analysis demonstrated that this switch cannot be attributed to expansion of the apical surface of maturing RPE because the basolateral membrane expanded proportionally, maintaining a 3:1 apical/basolateral ratio. Kinetic analysis of polarized surface delivery in MDCK and RPE-J cells showed that EMMPRIN has a basolateral signal in its cytoplasmic tail recognized by both cell lines. In contrast, the basolateral signal of N-CAM is recognized by MDCK cells but not RPE-J cells. Deletion of N-CAM's basolateral signal did not prevent its apical localization in vivo. The data demonstrate that the apical polarity of EMMPRIN and N-CAM in mature RPE results from suppressed decoding of specific basolateral signals resulting in randomized delivery to the cell surface.

Key Words: adenovirus gene transfer • interphotoreceptor matrix • p75-NTR • polarity • RET-PE2

Abbreviations used in this paper: DAPI, 4',6-diamidino-2-phenylindole; EMMPRIN, extracellular matrix metalloproteinase inducer; IPM, interphotoreceptor matrix; MMP, matrix metalloproteinase; N-CAM, neural cell adhesion molecule; p75-NTR, p75-neurotrophin receptor; RPE, retinal pigment epithelium.

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