TIBS 19 - APRIL 1994
THE PROTEIN TYROSINE phos-
phatases (PTPs) are a growing family of
enzymes that function, in concert with
protein tyrosine kinases, to modulate
the tyrosine phosphorylation of cellular
proteins (for comprehensive reviews,
see Refs 1 and 2). Of the 30 or so PTPs
characterized to date, approximately a
third are transmembrane, receptor-like
molecules, while the majority are
cytoplasmic proteins. With such a large
number of potentially redundant en-
zymes located intracellularly, the ac-
tivity of the intracellular PTPs must
be highly regulated to prevent spurious,
nonspecific depbosphorylation of pro-
teins. Regulation of the activity of such
cellular enzymes can be accomplished
in various ways: (I) by modulating the
steady-state levels of the enzyme; (2)
by substrate specificity; (3) by post-
translational modification 0.e. phos-
phorylation, proteolytic cleavage, etc.);
and (4) by interaction with inhibitor/
activator molecules. We are just begin-
ning to understand how these regulat-
ory mechanisms might function to modu-
late PTP activity. In particular, controlling
substrate specificity by restricting sub-
strate availability could be an import-
ant means of regulating the intracellular
PTPs. Sequence analyses of the PTPs
have revealed an exquisite diversity of
protein sequences outside the highly
conserved catalytic domain. It has been
suggested that these noncatalytic se-
quences serve as 'zip codes' to 'ad-
dress' the PTPs to specific comp,~rt
ments within the ceil, thereby defining
and restricting their substrate speci-
ficity. Here we will discuss several
examples of intracellulax PTPs that could
he subjected to this mode of regulation.
The PTP family
The PTPs are multidomain proteins
whose structural features separate the
family into two main classes based on
their transmembrane or intracellular
location (Fig. 1). All PTPs, whether
transmembrane or cytoplasmic, pos-
sess at least one 230 amino acid cata-
lytic domain containing a highly cnn-
served active-site region with t!~e
consensus motif [I/V]HCXAGXXR[S/I IG
L. J. Maum and J. E. Dixon are at the
Departmentof BiologicalChemistry,
University of MichiganMedicalCenter, 5416
Medical Science I, Box 0606, Ann Arbor,
M148109, USA.
TALKING POINT
Illlllll
'Zip codes' direct intracellular
protein tyrosine phosphatases to
the correct cellular 'address'
[
Laura J. Mauro and Jack E. Dixon
The transmembrane and intracellular protein tyrosine phosphatases
(PTPs) play an essential role as signal transduction proteins involved in
various cellular processes including division, proliferation and differen-
tiation. As such, their activity must be strictly regulated to avoid nonspecific
tyrosine dephosphorylation of cellular proteins. The intracellular P]Ps pos-
sess a diversity of protein sequences outside the catalytic domain that
appear to serve as 'zip codes' specifically 'addressing' these proteins to
defined subceliular compartments. These localization strategies are pro-
posed to function as a regulatory mechanism, defining the substrate
specificity and function of the intracellular PTPs.
(where X is any amino acid). This
region is the signature sequence of
most PTPs. Site-directed mutagenesis
and trapping experiments have shown
that the cysteinyi residue within this
motif is essential for phosphatase ac-
tivity and forms a thiol-phosphate
intermediate during catalytic turnover1.
Interestingly, this catalytic domain
bears no resemblance to that of the
serine/threonine phosphatases or o(
the alkaline or acid phosphatases.
Transmembrane PTPs possess an
extracellular domain, a single trans-
membrane domain and norma, dy two
catalytic domains followed, by a short
carboxy-terminal segment. At present,
the human PTP[5 and tl'~e Drosophila
DPTPI0D are the only transmembrane
proteins that have a single catalytic
domain. Unlike the cytoplasmic tail, the
extracellular domains of these proteins
are highly divergent, with small glycosyl-
ated segments (human PTPa and e),
tandem repeats of immunoglobulin-like
and fibropectin type Ill domains similar
to N.CAM molecules [leucocyte com-
mon antigen related molecule OAR),
PTP,~], or alternately spliced lengths of
sequence containing N- and O.linked
carbohydrates (CD45). These extracellu-
lax features suggest that the activity of
these PTPs might be modulated by
ligands. Recently, it was shown that
the homophilic binding of PTPp~ can
mediate cell-cell aggregation 3,4. This
suggests theft the extracellular domain
of this PTP can serve as its own ligand
and could potentially function to regu-
late ceE-celi interactions.
Thr: distinguishing feature of the
intracellular PTPs is the diversity of
de, mains flanking a single catalytic
(iomain (Fig. 1). One of the principle
functions of these flanking sequences, or
zip codes, appears to be the targeting of
the enzyme to specific intracellular
locations. These include: (1) membrane-
association domains, (2) nucleax-
localization domains, (3) Src homology
2 (SH2) domains and (4) cytoskeletal-
association domains. A schematic
showing these intracellulax PTPs resid-
ing at their proven or hypothesized
subcellulax locations within a eukary-
otic cell is shown in Fig. 2. We will dis-
cuss each of the PTPs shown in the fol-
lowing sections.
Membrane and nuclear targeting
sequences fol PTPs
A number of intracellulax PTPs pos-
sess unique sequences downstream of
the catalytic domain, which might serve
to regulate the targeting of the protein
to a subcellular locale and, in some
cases, also modulate phosphatase
activity. Purification of PTP1B from the
human placenta yielded both soluble
and particulate forms of the enzyme,
© 1994, Elsevier Science Ltd 096~- 0004,/94/$~Z00 '15~"