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Vol. 19, Issue 10, 4492-4505, October 2008

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Piecemeal Microautophagy of the Nucleus Requires the Core Macroautophagy Genes

R. Krick^*,, Y. Muehe^*,, T. Prick^*,, S. Bremer^*, P. Schlotterhose^*, E.-L. Eskelinen, J. Millen, D. S. Goldfarb, and M. Thumm^*

*Center of Biochemistry and Molecular Cell Biology, Georg-August University, D-37073 Göttingen, Germany; Department of Biological and Environmental Sciences, University of Helsinki, FI-00014 Helsinki, Finland; and Biology Department, University of Rochester, Rochester, NY 14627-0211

Submitted April 8, 2008; Revised July 22, 2008; Accepted August 4, 2008
Monitoring Editor: Suresh Subramani

Autophagy is a diverse family of processes that transport cytoplasm and organelles into the lysosome/vacuole lumen for degradation. During macroautophagy cargo is packaged in autophagosomes that fuse with the lysosome/vacuole. During microautophagy cargo is directly engulfed by the lysosome/vacuole membrane. Piecemeal microautophagy of the nucleus (PMN) occurs in Saccharomyces cerevisiae at nucleus-vacuole (NV) junctions and results in the pinching-off and release into the vacuole of nonessential portions of the nucleus. Previous studies concluded macroautophagy ATG genes are not absolutely required for PMN. Here we report using two biochemical assays that PMN is efficiently inhibited in atg mutant cells: PMN blebs are produced, but vesicles are rarely released into the vacuole lumen. Electron microscopy of arrested PMN structures in atg7, atg8, and atg9 mutant cells suggests that NV-junction–associated micronuclei may normally be released from the nucleus before their complete enclosure by the vacuole membrane. In this regard PMN is similar to the microautophagy of peroxisomes (micropexophagy), where the side of the peroxisome opposite the engulfing vacuole is capped by a structure called the "micropexophagy-specific membrane apparatus" (MIPA). The MIPA contains Atg proteins and facilitates terminal enclosure and fusion steps. PMN does not require the complete vacuole homotypic fusion genes. We conclude that a spectrum of ATG genes is required for the terminal vacuole enclosure and fusion stages of PMN.

These authors contributed equally to this work.

Address correspondence to: M. Thumm (mthumm{at}uni-goettingen.de)

Abbreviations used: Atg, autophagy; PAS, preautophagosomal structure; PMN, piecemeal microautophagy of the nucleus; PMSF, phenylmethylsulfonyl fluoride.

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