Two Distinct Pathways for Targeting Proteins from the Cytoplasm to the Vacuole/Lysosome

doi:10.1083/jcb.139.7.1687

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© The Rockefeller University Press, 0021-9525/1997//1687 $5.00
The Journal of Cell Biology, Volume 139, Number 7, , 1997 1687-1695

Article

Two Distinct Pathways for Targeting Proteins from the Cytoplasm to the Vacuole/Lysosome

Misuzu Baba^*^,, Masako Osumi, Sidney V. Scott, Daniel J. Klionsky, and Yoshinori Ohsumi^*

^* Department of Cell Biology, National Institute for Basic Biology, Okazaki 444, Japan; Department of Chemical and Biological Sciences, Faculty of Science, Japan Women's University, Mejirodai, Tokyo 112, Japan; and Section of Microbiology, University of California, Davis, California 95616

Stress conditions lead to a variety of physiological responsesat the cellular level. Autophagy is an essential process usedby animal, plant, and fungal cells that allows for both recyclingof macromolecular constituents under conditions of nutrientlimitation and remodeling the intracellular structure for celldifferentiation. To elucidate the molecular basis of autophagic protein transport to the vacuole/lysosome, we have undertakena morphological and biochemical analysis of this pathway inyeast.

Using the vacuolar hydrolase aminopeptidase I (API) as a marker,we provide evidence that the autophagic pathway overlaps withthe biosynthetic pathway, cytoplasm to vacuole targeting (Cvt),used for API import. Before targeting, the precursor form ofAPI is localized mostly in restricted regions of the cytosolas a complex with spherical particles (termed Cvt complex). During vegetative growth, the Cvt complex is selectively wrappedby a membrane sac forming a double membrane-bound structureof $~$ 150 nm diam, which then fuses with the vacuolar membrane.This process is topologically the same as macroautophagy inducedunder starvation conditions in yeast (Baba, M., K. Takeshige,N. Baba, and Y. Ohsumi. 1994. J. Cell Biol. 124:903–913).However, in contrast with autophagy, API import proceeds constitutivelyin growing conditions. This is the first demonstration of theuse of an autophagy-like mechanism for biosynthetic deliveryof a vacuolar hydrolase. Another important finding is that when cells are subjected to starvation conditions, the Cvtcomplex is now taken up by an autophagosome that is much largerand contains other cytosolic components; depending on environmentalconditions, the cell uses an alternate pathway to sequesterthe Cvt complex and selectively deliver API to the vacuole.Together these results indicate that two related but distinctautophagy-like processes are involved in both biogenesis ofvacuolar resident proteins and sequestration of substrates tobe degraded.

Address all correspondence to Yoshinori Ohsumi, Department ofCell Biology, National Institute for Basic Biology, Okazaki444, Japan. Tel.: (81) 564-55-7515. Fax: (81) 564-55-7516.E-mail: yohsumi{at}nibb.ac.jp

1. Abbreviation used in this paper: API, aminopeptidase I.

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