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Convergence of model systems for peroxisome biogenesis
Suresh Subramani
Receptors for the two peroxisomal targeting signals PTS1
and PTS2 have recently been identified in yeasts. The
disparate subcellular locations of PTS receptor homologs
have led to proposals of receptor shuttling between the
cytosol and the peroxisomal membrane, and to the suggestion
that some of these molecules may even reside normally in
the peroxisomal matrix. A peroxisomal membrane protein
that interacts with the PTS1 receptor in Saccharomyces
cerevisiae may serve as the receptor-docking site on
the organelle. The conservation of the PTS1 receptor in
several yeasts has led to the cloning and characterization
of the gene encoding its human homolog, PTS1 R, which is
mutated in a group of patients afflicted with fatal peroxisomal
disorders. The identification of peroxisome assembly
genes in yeasts is likely to lead to the cloning of additional
human genes responsible for other generalized peroxisomal
disorders. Protein unfolding is not a prerequisite for import
of peroxisomal matrix proteins, suggesting novel mechanisms
for the translocation of polypeptides across the peroxisomal
membrane.
Address
Department of Biology, University of California at San Diego,
Rm 4314 Bonner Hall, 9500 Gilman Drive, La Jolla, CA 92093-0322,
USA; e-mail: ssubramani@ucsd.edu
Current Opinion in Cell Biology 1996, 8:513-518
© Current Biology Ltd ISSN 0955-06?4
Abbreviations
GFP
hsp
mPTS
PAF
Pas
Peb
Per
PMP
Pp
PTS
PTS1 R
PXR
RCDP
Sc
YIPay
green fluorescent protein
heat shock protein
peroxisomal membranetargeting signal
peroxisome assembly factor
peroxisome assembly
peroxisome biogenesis
peroxisome
peroxisomal membrane protein
Pichia pastoris
peroxisomaltargeting signal
PTS1 receptor
peroxisometargeting signal receptor
rhizomelic chondrodysplasiapunctata
Saccharomyces cerevisiae
peroxisome assemblyin Yarrowia lipolytica
Introduction: multiple model systems for the
study of peroxisome biogenesis
Understanding the mechanism of peroxisomal protein
import is germane to the mechanism of protein trans-
location across biological membranes and to human
disease. Patients who succumb to any one of several
fatal peroxisomal disorders -- Zellweger syndrome, neo-
natal adrenoleukodystrophy, infantile Refsum's disease;
hyperpipecolic acidemia or rhizomelic chondrodysplasia
punctata (RCDP)--are impaired in their ability to import
peroxisomal matrix proteins into the lumen of the
organelle [1-3,4"]. Cell lines derived from such patients
have been propagated and exploited in cell fusion studies,
and at least 10 different complementation groups affecting
peroxisomal protein import and biogenesis in humans have
been defined [5].
This rich genetic resource of mutant cells deficient in
peroxisome assembly has been expanded significantly by
the development of several yeast model systems in which
peroxisomal import and/or biogenesis is compromised
[6-14]. The success of these studies stems in large
measure from the fact that peroxisomes are apparently dis-
pensable under certain conditions, allowing the isolation of
non-conditional mutants (known as pas, per, pat, or peb).
A close parallel exists among the general classes of
import-deficient phenotypes observed in mutant yeast
and human cells. The evolutionary conservation of perox-
isomal targeting signals (PTSs) and peroxisome biogenesis
genes has led to a convergence of model systems that
promises to yield new insights into peroxisome function
and biogenesis and the role of these processes in human
disease. In this review, I focus primarily on new results
published in 1995 and 1996.
Targeting signals
Peroxisomal matrix, in addition to membrane, proteins
are necessarily encoded by the nuclear genome, and are
imported post-translationally to the organelle. None of the
peroxisomal profeins studied to date are glycosylated, nor
are they burdened by any modifications that are sometimes
necessary for import into organelles [5].
Peroxisomes are no exception to the recurring theme that
multiple import pathways are involved in the targeting of
proteins to a specific subcellular organelle. Several signals
direct protein traffic to the peroxisome. Prominent among
these is PTS1, a conserved, carboxy-terminal tripeptide
(with the amino acid sequence SKL or a variant thereof)
that constitutes the major targeting signal for polypeptides
that are en route to the peroxisomal matrix [5]. A second
sequence, PTS2, is composed of a conserved nonapeptide
with the sequence (R/K)(L/V/I)(Xs)(H/Q)(L/A), and it
is used by a smaller subset of matrix proteins [5].
Although naturally located at the amino terminus of
proteins, the PTS2 sequence also functions at internal
locations in passenger proteins (KN Faber, S Subramani,
unpublished data). Other sequences, located internally
within peroxisomai matrix proteins such as Candida
tropicalis acyl CoA oxidase [15] and Saccharomyces cerevisiae
catalase [16] and carnitine acetyl transferase [17]; have
been described but their generality is undocumented.
Recently, another PTS has been described that is near