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First published online 18 December 2002
doi: 10.1242/jcs.00260

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Journal of Cell Science 116, 655-663 (2003)
doi: 10.1242/jcs.00260

Research Article

Multiple cytoplasmic signals direct the intracellular trafficking of chicken kidney AE1 anion exchangers in MDCK cells

Tracy L. Adair-Kirk*, Frank C. Dorsey and John V. Cox{ddagger}

Department of Molecular Sciences, University of Tennessee Health Science Center, 858 Madison Avenue, Memphis, Tennessee 38163, USA
* Present address: Department of Medicine, Washington University School of Medicine at Barnes-Jewish Hospital, St Louis, MO 63110, USA

{ddagger} Author for correspondence (e-mail: jcox{at}utmem.edu)

Accepted 6 November 2002

AE1/Fc receptor chimeras have been used to define the sequences that direct the basolateral sorting, recycling and cytoskeletal association of the chicken AE1-4 anion exchanger in MDCK cells. These analyses revealed that amino acids 1-63 of AE1-4 were sufficient to redirect a cytoplasmic tailless murine IgG FcRII B2 receptor from the apical to the basolateral membrane of MDCK cells, where Fc1-63 associated with elements of the actin cytoskeleton. In contrast to Fc1-63, chimeras containing amino acids 1-37 (Fc1-37) or 38-63 (Fc38-63) of AE1-4 accumulated in intracellular membrane compartments that overlapped late endosomes and the trans-Golgi network (TGN), respectively. Internalization assays indicated that the patterns of localization observed for Fc1-37 and Fc38-63 resulted from the recycling of these chimeras from the cell surface. These assays further indicated that Fc1-37 and Fc38-63 each possess a basolateral sorting activity. Mutagenesis studies revealed that the endocytic and basolateral sorting activities in Fc1-37 are dependent upon serine 25, which is located in a sequence similar to a sorting signal in the polymeric immunoglobulin receptor. In addition, the sorting activities associated with Fc38-63 were dependent upon tyrosine 47 and leucine 50. These residues resided within the sequence, YVEL, which matches the YXX{Phi} motif (where X is any amino acid and {Phi} is a hydrophobic residue) that functions as an endocytic and TGN recycling signal for other membrane proteins. Our data indicate that amino acids 1-63 of AE1-4 contain sorting and cytoskeletal binding activities that account for most of the properties previously associated with AE1-4 in MDCK cells. Furthermore, the alternative localization patterns exhibited by chimeras containing various combinations of these activities suggest that interplay between these cytoplasmic activities is critical for specifying AE1-4 localization in epithelial cells.

Key words: Sorting signal, Actin, Recycling, TGN, Late endosomes




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