ANTIOXIDANTS & REDOX SIGNALING
Volume 10, Number 6, 2008
© Mary Ann Liebert, Inc.
DOI: 10.1089/ars.2007.2011
Forum Review
Novel Role of Protein Disulfide Isomerase in the Regulation
of NADPH Oxidase Activity: Pathophysiological Implications
in Vascular Diseases
FRANCISCO R. M. LAURINDO,
1
DENISE C. FERNANDES,
1
ANGÉLICA M. AMANSO,
1
LUCIA R. LOPES,
2
and CÉLIO X. C. SANTOS
1
ABSTRACT
Vascular cell NADPH oxidase complexes are key sources of signaling reactive oxygen species (ROS) and con-
tribute to disease pathophysiology. However, mechanisms that fine-tune oxidase-mediated ROS generation
are incompletely understood. Besides known regulatory subunits, upstream mediators and scaffold platforms
reportedly control and localize ROS generation. Some evidence suggest that thiol redox processes may coor-
dinate oxidase regulation. We hypothesized that thiol oxidoreductases are involved in this process. We focused
on protein disulfide isomerase (PDI), a ubiquitous dithiol disulfide oxidoreductase chaperone from the endo-
plasmic reticulum, given PDI’s unique versatile role as oxidase/isomerase. PDI is also involved in protein traf-
fic and can translocate to the cell surface, where it participates in cell adhesion and nitric oxide internaliza-
tion. We recently provided evidence that PDI exerts functionally relevant regulation of NADPH oxidase activity
in vascular smooth muscle and endothelial cells, in a thiol redox-dependent manner. Loss-of-function exper-
iments indicate that PDI supports angiotensin II-mediated ROS generation and Akt phosphorylation. In ad-
dition, PDI displays confocal co-localization and co-immunoprecipitates with oxidase subunits, indicating close
association. The mechanisms of such interaction are yet obscure, but may involve subunit assembling stabi-
lization, assistance with traffic, and subunit disposal. These data may clarify an integrative view of oxidase
activation in disease conditions, including stress responses. Antioxid. Redox Signal. 10, 1101–1113.
1101
INTRODUCTION
R
EDOX PATHWAYS ADD AN IMPORTANT DIMENSION to cell sig-
naling networks regulating physiological and pathologi-
cal events, particularly cardiovascular disorders such as hyper-
tension (16, 99). However, mechanisms providing fine-tuning
of redox equilibrium are complex and yet incompletely under-
stood. Indeed, it has been shown that redox signaling can oc-
cur in the absence of overall changes in redox status of the ma-
jor intracellular reductants glutathione or thioredoxin (37), and
thus can be separated from oxidative stress, which is a disrup-
tion of redox signaling requiring some type of cellular adapta-
tion (49). Accordingly, most intra- and extracellular redox
buffer pairs are not in equilibrium, suggesting their indepen-
dent regulation (49), and further indicating that oxidative stress
is more complex than a simple overall imbalance between ox-
idants and antioxidants in favor of the former. In turn, oxida-
tive stress activates vicious signaling circuits in several disease
conditions, not only as a result of direct free radical-mediated
damage to biomolecules, but—perhaps mostly—from disor-
dered activation and/or expression of subcellular signaling tar-
gets due to excessive, uncompensated, or decompartmentalized
1
Vascular Biology Laboratory, Heart Institute (InCor), University of São Paulo School of Medicine; and
2
Department of Pharmacology,
Biomedical Sciences Institute, University of São Paulo, Brazil.