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J. Biol. Chem., Vol. 278, Issue 38, 36707-36717, September 19, 2003

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Characterization of Periphilin, a Widespread, Highly Insoluble Nuclear Protein and Potential Constituent of the Keratinocyte Cornified Envelope^*

Shideh Kazerounian and Sirpa Aho 

From the Department of Dermatology and Cutaneous Biology, Thomas Jefferson University, Philadelphia, Pennsylvania 19107

While keratinocytes go through the terminal differentiation and move toward the outer layers of epidermis, multiple proteins become sequentially incorporated into the cornified cell envelope. We have identified through yeast two-hybrid screening a novel protein, periphilin, interacting with periplakin, which is known as a precursor of the cornified cell envelope. Periphilin gene at chromosome 12q12 gives rise to multiple alternatively spliced transcripts. A monoclonal antibody detected the keratinocyte-specific periphilin isoform in undifferentiated keratinocytes in speckle-type nuclear granules and at the nuclear membrane, but in differentiated keratinocytes periphilin localized to the cell periphery and at cell-cell junctions, colocalizing there with periplakin. From cultured keratinocytes, periphilin was solubilized only after urea extraction, indicating the highly insoluble character of this protein. The nuclear localization, mediated through the N-terminal sequences of periphilin protein, is a prerequisite for the formation of insoluble complexes. Although the globular N terminus of periphilin was necessary for the interaction with the periplakin tail, the keratinocyte-specific C terminus was responsible for the homodimerization. The C-terminal helical domain, composed of multiple heptad repeats, serves as a substrate for cross-linking by transglutaminases but also was specifically cleaved by caspase-5 in vitro. In conclusion, the localization pattern and insolubility of periphilin indicate that this novel protein is potentially involved in epithelial differentiation and contributes to epidermal integrity and barrier formation.

Received for publication, April 14, 2003 , and in revised form, July 1, 2003.

The nucleotide sequence(s) reported in this paper has been submitted to the GenBank^TM/EBI Data Bank with accession number(s) AY157850.

^* This work was supported by Grant RO1-33588 from NIAMS, National Institutes of Health. The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

To whom correspondence should be addressed: Dept. of Dermatology and Cutaneous Biology, Thomas Jefferson University, 233 S. 10th St., BLSB 422, Philadelphia, PA 19107. Tel.: 215-503-2018; Fax: 215-503-5788; E-mail: Sirpa.Aho{at}jefferson.edu.

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