Ankyrin-binding domain of CD44(GP85) is required for the expression of hyaluronic acid-mediated adhesion function

doi:10.1083/jcb.126.4.1099

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Ankyrin-binding domain of CD44(GP85) is required for the expression of hyaluronic acid-mediated adhesion function

VB Lokeshwar, N Fregien and LY Bourguignon
Department of Cell Biology and Anatomy, University of Miami School of Medicine, Florida 33101.

GP85 is one of the most common hemopoietic isoforms of the cell adhesion molecule, CD44. CD44(GP85) is known to contain at least one ankyrin-binding site within its 70 aa cytoplasmic domain and to bind hyaluronic acid (HA) with its extracellular domain. In this study we have mapped the ankyrin-binding domain of CD44(GP85) by deleting various portions of the cytoplasmic region followed by expression of these truncated cDNAs in COS cells. The results of these experiments indicate that the ankyrin-binding domain resides between amino acids 305 and 355. Biochemical analyses, using competition binding assays and a synthetic peptide (NGGNGT-VEDRKPSEL) containing 15 aa between aa 305 and aa 320, support the conclusion that this region is required for ankryin binding. Furthermore, we have constructed a fusion protein in which this 15 aa sequence of CD44(GP85) is transplanted onto another transmembrane protein which does not bind ankyrin. Our results show that this fusion protein acquires the ability to bind ankyrin confirming that the sequence (306NGGNGTVEDRKPSE320L) is a critical part of the ankryin-binding domain of CD44(GP85). In addition, we have demonstrated that deletion of this 15 aa ankyrin-binding sequence from CD44(GP85) results in a drastic reduction (> or = 90%) of HA-binding and HA-mediated cell adhesion. These findings strongly suggest that ankyrin binding to the cytoplasmic domain of CD44(GP85) plays a pivotal role in regulating hyaluronic acid-mediated cell-cell and cell- extracellular matrix interactions.
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Peck, D, Isacke, C. (1998). Hyaluronan-dependent cell migration can be blocked by a CD44 cytoplasmic domain peptide containing a phosphoserine at position 325. J. Cell Sci. 111: 1595-1601 [Abstract]
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Lokeshwar, V. B., Iida, N., Bourguignon, L. Y.W. (1996). The Cell Adhesion Molecule, GP116, Is a New CD44 Variant (ex14/v10) Involved in Hyaluronic Acid Binding and Endothelial Cell Proliferation. J. Biol. Chem. 271: 23853-23864 [Abstract] [Full Text]
Sheikh, H., Isacke, C. M. (1996). A Di-hydrophobic Leu-Val Motif Regulates the Basolateral Localization of CD44 in Polarized Madin-Darby Canine Kidney Epithelial Cells. J. Biol. Chem. 271: 12185-12190 [Abstract] [Full Text]
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Bourguignon, L. Y. W., Chu, A., Jin, H., Brandt, N. R. (1995). Ryanodine Receptor-Ankyrin Interaction Regulates Internal Ca[IMAGE] Release in Mouse T-lymphoma Cells. J. Biol. Chem. 270: 17917-17922 [Abstract] [Full Text]
Bourguignon, L. Y. W., Jin, H. (1995). Identification of the Ankyrin-binding Domain of the Mouse T-lymphoma Cell Inositol 1,4,5-Trisphosphate (IP(3)) Receptor and Its Role in the Regulation of IP(3)-mediated Internal Ca[IMAGE] Release. J. Biol. Chem. 270: 7257-7260 [Abstract] [Full Text]
Neame, S., Uff, C., Sheikh, H, Wheatley, S., Isacke, C. (1995). CD44 exhibits a cell type dependent interaction with triton X-100 insoluble, lipid rich, plasma membrane domains. J. Cell Sci. 108: 3127-3135 [Abstract]
Hudson, D., Sleeman, J, Watt, F. (1995). CD44 is the major peanut lectin-binding glycoprotein of human epidermal keratinocytes and plays a role in intercellular adhesion. J. Cell Sci. 108: 1959-1970 [Abstract]
Perschl, A, Lesley, J, English, N, Hyman, R, Trowbridge, I. (1995). Transmembrane domain of CD44 is required for its detergent insolubility in fibroblasts. J. Cell Sci. 108: 1033-1041 [Abstract]
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