Journal of Neurochemistry
Lippincott—Raven Publishers, Philadelphia
© 1998 International Society for Neurochemistry
Peripherin Is Tyrosine-Phosphorylated
at Its Carboxyl-Terminal Tyrosine
James M. Angelastro, Chung-Liang Ho, Thierry Frappier, Ronald K. H. Liem,
and Lloyd A. Greene
Department of Pathology and Center for Neurobiology and Behavior, College of Physicians and Surgeons
of Columbia University, New York, New York, U.S.A.
Abstract: Peripherin is a type Ill intermediate filament
present in peripheral and certain CNS neurons. We report
here that peripherin contains a phosphotyrosine residue
and, as such, is the only identified intermediate filament
protein known to be modified in this manner. Antiserum
specific for phosphotyrosine recognizes peripherin pres-
ent in Pci 2 cells (with or without nerve growth factor
treatment) and in rat sciatic nerve as well as that ex-
pressed in Sf-9 cells and SW-13 cl. 2 vim cells. The
identity of peripherin as a tyrosine-phosphorylated pro-
tein in PC12 cells was confirmed by immunoprecipitation,
two-dimensional isoelectric focusing/sodium dodecyl
sulfate—polyacrylamide gel electrophoresis gels, and
phosphoamino acid analysis. Unlike serine/threonine
phosphorylation, tyrosine phosphorylation of peripherin
is not regulated by depolarization or nerve growth factor
treatment. To identify the site of tyrosine phosphorylation,
rat peripherin was mutated at several tyrosine residues
and expressed in SW-13 cl. 2 vim~ cells. Tyrosine phos-
phorylation was selectively lost only for peripherin mu-
tants in which the carboxy-terminal tyrosine (Y474) was
mutated. Indirect immunofluorescence staining indicated
that both wild-type peripherin and peripherin Y474F form
a filamentous network in SW-13 cI. 2 vim~ cells. This
indicates that tyrosine phosphorylation of the peripherin
c-terminal residue is not required for assembly and
leaves open the possibility that this modification serves
other functions. Key Words: Intermediate filament—Pe-
ripherin—Phosphotyrosine.
J. Neurochem. 70, 540—549 (1998).
understood (Troy et a!., 1992), but in light of its pres-
ence in early postmitotic neurons (Escurat et al., 1990;
Troy et al., 1990a) and up-regulation in axotomized
peripheral nerve cells (Oblinger et al., 1989; Troy et
al., 199Db), it has been suggested to play a role in
axon growth and stabilization (Troy et al., 1992).
Like other IFs, peripherin is heavily phosphorylated.
Huc et al. (1989) showed that in cultured mouse neuro-
blastoma cells and in sympathetic neurons, peripherin
is mainly phosphorylated in its amino-terminal half,
similar to vimentin and desmin type III IFs (Evans,
1988; Geisler et al., 1989; Kitamura et al., 1989; Chou
et a!., 1990). Regulation of peripherin expression and
phosphorylation has been studied in PC12 pheochro-
mocytoma cells. Peripherin levels are induced by expo-
sure to nerve growth factor (NGF), and peripherin
phosphorylation can be rapidly increased by various
stimuli, including NGF, K ± depolarization, and activa-
tors of protein kinase A or C (Aletta et al., 1988).
The role of phosphorylation in regulation of peripherin
function is presently unknown, but this modification
can affect the behavior of other IF proteins. For in-
stance, phosphorylation at the carboxyl-terminal tail
KSP motifs of the high-molecular-weight neurofila-
ment is thought to control the caliber of the axon (Car-
den et al., 1987; Inagaki et al., 1987; Shaw, 1991). In
addition, several lines of evidence suggest that phos-
phorylation of vimentin and desmin inhibits their as-
sembly into filaments (Inagaki et al., 1987; Evans,
Peripherin is a type III intermediate filament (IF)
protein that is expressed by neurons that give rise to
peripheral and certain cranial nerves as well as by
enteric neurons and by neurons that comprise several
midbrain nuclei (Portier et al., 1983—1984; Greene,
1989). Like all IF proteins, peripherin is synthesized
as subunits that spontaneously self-assemble into fil-
aments. Each subunit consists of a central a-helical
rod domain flanked by nonhelical N- and C-terminal
domains (Leonard et al., 1988; Thompson and Ziff,
1989). The functional roles of peripherin are not well
Received August 20, 1997; revised manuscript received Septem-
ber 19, 1997; accepted September 22, 1997.
Address correspondence and reprint requests to Dr. J. M. Ange-
lastro at Department of Pathology and Center for Neurobiology and
Behavior, College of Physicians and Surgeons of Columbia Univer-
sity, 630 West 168th Street, New York, NY 10032, U.S.A.
Abbreviations used: BSA, bovine serum albumin; DMEM, Dul-
becco’s modified Eagle’s medium; ECL, enhanced chemilumines-
cence; FITC, fluorescein isothiocyanate; HRP, horseradish peroxi-
dase; IEF, isoelectric focusing; IF, intermediate filament; NGF, nerve
growth factor; PAGE, polyacrylamide gel electrophoresis; PBS,
phosphate-buffered saline; PCR, polymerase chain reaction; SDS,
sodium dodecyl sulfate.
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