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Vol. 17, Issue 8, 3625-3637, August 2006

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MARK2/EMK1/Par-1B Phosphorylation of Rab11-Family Interacting Protein 2 Is Necessary for the Timely Establishment of Polarity in Madin-Darby Canine Kidney Cells

Nicole A. Ducharme^*, Chadwick M. Hales, Lynne A. Lapierre^*, Amy-Joan L. Ham, Asli Oztan, Gerard Apodaca, and James R. Goldenring^*

*Departments of Surgery and Cell and Developmental Biology and Department of Biochemistry and Mass Spectrometry Research Center, Vanderbilt University School of Medicine, Vanderbilt-Ingram Cancer Center, and the Nashville VA Medical Center, Nashville, TN 37232; Institute of Molecular Medicine, Medical College of Georgia, Augusta, GA 30912; and Department of Cell Biology and Physiology, University of Pittsburgh School of Medicine, Pittsburgh, PA 15261

Submitted August 9, 2005; Revised May 31, 2006; Accepted June 1, 2006
Monitoring Editor: Asma Nusrat

Rab11a, myosin Vb, and the Rab11-family interacting protein 2 (FIP2) regulate plasma membrane recycling in epithelial cells. This study sought to characterize more fully Rab11-FIP2 function by identifying kinase activities modifying Rab11-FIP2. We have found that gastric microsomal membrane extracts phosphorylate Rab11-FIP2 on serine 227. We identified the kinase that phosphorylated Rab11-FIP2 as MARK2/EMK1/Par-1B (MARK2), and recombinant MARK2 phosphorylated Rab11-FIP2 only on serine 227. We created stable Madin-Darby canine kidney (MDCK) cell lines expressing enhanced green fluorescent protein-Rab11-FIP2 wild type or a nonphosphorylatable mutant [Rab11-FIP2(S227A)]. Analysis of these cell lines demonstrates a new role for Rab11-FIP2 in addition to that in the plasma membrane recycling system. In calcium switch assays, cells expressing Rab11-FIP2(S227A) showed a defect in the timely reestablishment of p120-containing junctional complexes. However, Rab11-FIP2(S227A) did not affect localization with recycling system components or the normal function of apical recycling and transcytosis pathways. These results indicate that phosphorylation of Rab11-FIP2 on serine 227 by MARK2 regulates an alternative pathway modulating the establishment of epithelial polarity.

Address correspondence to: James R. Goldenring ( jim.goldenring{at}vanderbilt.edu)

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