Biogenesis of Porin of the Outer Mitochondrial Membrane Involves an Import Pathway via Receptors and the General Import Pore of the TOM Complex

doi:10.1083/jcb.152.2.289

Published online 16 January 2001. doi:10.1083/jcb.152.2.289

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© The Rockefeller University Press, 0021-9525/2001/1/289/ $5.00
The Journal of Cell Biology, Volume 152, Number 2, January 22, 2001 289-300

Original Article

Biogenesis of Porin of the Outer Mitochondrial Membrane Involves an Import Pathway via Receptors and the General Import Pore of the TOM Complex

Thomas Krimmer^a,b, Doron Rapaport^c, Michael T. Ryan^a, Chris Meisinger^a, C. Kenneth Kassenbrock^d, Elizabeth Blachly-Dyson^e, Michael Forte^e, Michael G. Douglas^d, Walter Neupert^c, Frank E. Nargang^f, and Nikolaus Pfanner^a
^a Institute for Biochemistry and Molecular Biology, University of Freiburg, D-79104 Freiburg, Germany
^b Faculty for Biology, University of Freiburg, D-79104 Freiburg, Germany
^c Institute for Physiological Chemistry, Munich University, D-80336 Munich, Germany
^d Department of Biochemistry and Biophysics, University of North Carolina, Chapel Hill, North Carolina 27599
^e Oregon Health Sciences University, Portland, Oregon 97201
^f Department of Biological Sciences, University of Alberta, Edmonton, Alberta, T6G 2E9, Canada

Correspondence to: Frank E. Nargang, Department of Biological Sciences, University of Alberta, Edmonton, Alberta, T6G 2F0 Canada. Tel:(780) 492-5375 Fax:(780) 492-1903 E-mail:frank.nargang{at}ualberta.ca.

Porin, also termed the voltage-dependent anion channel, is themost abundant protein of the mitochondrial outer membrane. Theprocess of import and assembly of the protein is known to bedependent on the surface receptor Tom20, but the requirementfor other mitochondrial proteins remains controversial. We haveused mitochondria from Neurospora crassa and Saccharomyces cerevisiaeto analyze the import pathway of porin. Import of porin intoisolated mitochondria in which the outer membrane has been openedis inhibited despite similar levels of Tom20 as in intact mitochondria.A matrix-destined precursor and the porin precursor competefor the same translocation sites in both normal mitochondriaand mitochondria whose surface receptors have been removed,suggesting that both precursors utilize the general import pore.Using an assay established to monitor the assembly of in vitro–importedporin into preexisting porin complexes we have shown that besidesTom20, the biogenesis of porin depends on the central receptorTom22, as well as Tom5 and Tom7 of the general import pore complex(translocase of the outer mitochondrial membrane [TOM] corecomplex). The characterization of two new mutant alleles ofthe essential pore protein Tom40 demonstrates that the importof porin also requires a functional Tom40. Moreover, the porinprecursor can be cross-linked to Tom20, Tom22, and Tom40 onits import pathway. We conclude that import of porin does notproceed through the action of Tom20 alone, but requires an intactouter membrane and involves at least four more subunits of theTOM machinery, including the general import pore.

Key Words: mitochondria, protein sorting, porin, Neurospora crassa, Saccharomycescerevisiae

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