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J. Biol. Chem., Vol. 278, Issue 5, 3489-3496, January 31, 2003

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Translocation of the C Terminus of a Tail-anchored Protein across the Endoplasmic Reticulum Membrane in Yeast Mutants Defective in Signal Peptide-driven Translocation^*

Monica Yabal^§, Silvia Brambillasca^¶, Paolo Soffientini^¶, Emanuela Pedrazzini^¶, Nica Borgese^¶**, and Marja Makarow^§§§

From the  Program of Cellular Biotechnology, Institute of Biotechnology, University of Helsinki, Viikinkaari 9, 00710 Helsinki, Finland, ^¶ Consiglio Nazionale delle Ricerche Institute of Neuroscience, Cellular and Molecular Pharmacology Section, Via Vanvitelli 32-20129 Milano, Italy, and the ^** Faculty of Pharmacy, University of Catanzaro "Magna Graecia," 8021 Roccelletta di Borgia (Catanzaro), Italy

C-tail-anchored proteins are defined by an N-terminal cytosolic domain followed by a transmembrane anchor close to the C terminus. Their extreme C-terminal polar residues are translocated across membranes by poorly understood post-translational mechanism(s). Here we have used the yeast system to study translocation of the C terminus of a tagged form of mammalian cytochrome b₅, carrying an N-glycosylation site in its C-terminal domain (b₅-Nglyc). Utilization of this site was adopted as a rigorous criterion for translocation across the ER membrane of yeast wild-type and mutant cells. The C terminus of b₅-Nglyc was rapidly glycosylated in mutants where Sec61p was defective and incapable of translocating carboxypeptidase Y, a well known substrate for post-translational translocation. Likewise, inactivation of several other components of the translocon machinery had no effect on b₅-Nglyc translocation. The kinetics of translocation were faster for b₅-Nglyc than for a signal peptide-containing reporter. Depletion of the cellular ATP pool to a level that retarded Sec61p-dependent post-translational translocation still allowed translocation of b₅-Nglyc. Similarly, only low ATP concentrations (below 1 µM), in addition to cytosolic protein(s), were required for in vitro translocation of b₅-Nglyc into mammalian microsomes. Thus, translocation of tail-anchored b₅-Nglyc proceeds by a mechanism different from that of signal peptide-driven post-translational translocation.

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