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Originally published In Press as doi:10.1074/jbc.M009203200 on November 7, 2000

J. Biol. Chem., Vol. 276, Issue 8, 5924-5931, February 23, 2001
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Translation Rate of Human Tyrosinase Determines Its N-Linked Glycosylation Level*

Andrea ÚjváriDagger §, Rebecca AronDagger §, Thomas EisenhaureDagger , Elaine Cheng, Hadas A. ParagDagger , Yoel Smicun, Ruth Halaban, and Daniel N. HebertDagger ||

From the Dagger  Department of Biochemistry and Molecular Biology, Program in Molecular and Cellular Biology, University of Massachusetts, Amherst, Massachusetts 01003 and the  Department of Dermatology, Yale University School of Medicine, New Haven, Connecticut 06520

Tyrosinase is a type I membrane glycoprotein essential for melanin synthesis. Mutations in tyrosinase lead to albinism due, at least in part, to aberrant retention of the protein in the endoplasmic reticulum and subsequent degradation by the cytosolic ubiquitin-proteasomal pathway. A similar premature degradative fate for wild type tyrosinase also occurs in amelanotic melanoma cells. To understand critical cotranslational events, the glycosylation and rate of translation of tyrosinase was studied in normal melanocytes, melanoma cells, an in vitro cell-free system, and semi-permeabilized cells. Site-directed mutagenesis revealed that all seven N-linked consensus sites are utilized in human tyrosinase. However, glycosylation at Asn-290 (Asn-Gly-Thr-Pro) was suppressed, particularly when translation proceeded rapidly, producing a protein doublet with six or seven N-linked core glycans. The inefficient glycosylation of Asn-290, due to the presence of a proximal Pro, was enhanced in melanoma cells possessing 2-3-fold faster (7.7-10.0 amino acids/s) protein translation rates compared with normal melanocytes (3.5 amino acids/s). Slowing the translation rate with the protein synthesis inhibitor cycloheximide increased the glycosylation efficiency in live cells and in the cell-free system. Therefore, the rate of protein translation can regulate the level of tyrosinase N-linked glycosylation, as well as other potential cotranslational maturation events.

* This work was supported by grants from the Medical Foundation, Edward Mallinckrodt, Jr. Foundation, and United States Public Health Service Grant CA79864 (to D. N. H.) and by United States Public Health Service Grants AR39848 (to R. H.) and AR41942 (Yale Skin Diseases Research Center; R. E. Tigelaar, Program Investigator).The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

§ These authors contributed equally to this work.

|| To whom correspondence should be addressed. E-mail: dhebert@biochem.umass.edu.

Copyright © 2001 by The American Society for Biochemistry and Molecular Biology, Inc.
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