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J Biol Chem, Vol. 274, Issue 24, 17275-17283, June 11, 1999

Early Steps in Assembly of the Yeast Vacuolar H⁺-ATPase

From the Department of Biochemistry and Molecular Biology, State University of New York Health Science Center, Syracuse, New York 13210

Vacuolar proton-translocating ATPases are composed of a complex of integral membrane proteins, the V_o sector, attached to a complex of peripheral membrane proteins, the V₁ sector. We have examined the early steps in biosynthesis of the yeast vacuolar ATPase by biosynthetically labeling wild-type and mutant cells for varied pulse and chase times and immunoprecipitating fully and partially assembled complexes under nondenaturing conditions. In wild-type cells, several V₁ subunits and the 100-kDa V_o subunit associate within 3-5 min, followed by addition of other V_o subunits with time. Deletion mutants lacking single subunits of the enzyme show a variety of partial complexes, including both complexes that resemble intermediates in the assembly pathway of wild-type cells and independent V₁ and V_o sectors that form without any apparent V₁V_o subunit interaction. Two yeast sec mutants that show a temperature-conditional block in export from the endoplasmic reticulum accumulate a complex containing several V₁ subunits and the 100-kDa V_o subunit during incubation at elevated temperature. This complex can assemble with the 17-kDa V_o subunit when the temperature block is reversed. We propose that assembly of the yeast V-ATPase can occur by two different pathways: a concerted assembly pathway involving early interactions between V₁ and V_o subunits and an independent assembly pathway requiring full assembly of V₁ and V_o sectors before combination of the two sectors. The data suggest that in wild-type cells, assembly occurs predominantly by the concerted assembly pathway, and V-ATPase complexes acquire the full complement of V_o subunits during or after exit from the endoplasmic reticulum.

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