Tumor Necrosis Factor-a Upregulates Angiopoietin-2
in Human Umbilical Vein Endothelial Cells
Injune Kim, Ji-Hye Kim, Young Shin Ryu, Mingzhu Liu, and Gou Young Koh
1
National Creative Research Initiatives Center for Cardiac Regeneration and Institute of Cardiovascular Research,
Chonbuk University School of Medicine, Chonju, Korea
Received January 11, 2000
The angiopoietin-Tie2 system is an important
regulator of vasculogenesis and vascular integrity.
Angiopoietin-2 (Ang2) disrupts blood vessel formation
in the developing embryo by antagonizing the effects
of angiopoietin-1 (Ang1) on the Tie2 receptor. In this
study, we examined the effect of a well-known proin-
flammatory cytokine, tumor necrosis factor-a (TNF-a),
on Ang2 expression in human umbilical vein endothe-
lial cells. Reverse transcriptase-polymerase chain re-
action and Northern blot analyses indicated that
TNF-a induced Ang2 mRNA expression in a time- and
dose-dependent manner. Western blot analyses re-
vealed that TNF-a treatment increased cellular Ang2
protein. TNF-a induced less Ang2 mRNA expression in
the presence of nuclear factor-kB (NF-kB) inhibitor.
These results suggest that TNF-a-induced inflamma-
tory angiogenesis might be facilitated by the induc-
tion of Ang2. © 2000 Academic Press
The recent discovery of Ang1 and Ang2 has provided
insight into the molecular and cellular mechanisms of
blood vessel formation (1, 2). Ang1 and Ang2 share
about 60% amino acid identity and bind with similar
affinity to the endothelial cell tyrosine kinase receptor,
Tie2 (1, 2). In vivo analysis by targeted gene inactiva-
tion reveals that Ang1 recruits and sustains periendo-
thelial support cells (3). Overexpression of Ang1 re-
sults in increased vascularization (4), whereas over-
expression of Ang2 disrupts blood vessel formation in
the developing embryo by antagonizing the effects of
Ang1 on Tie2 (2). Thus, Ang2 is a naturally occurring
antagonist of Ang1 that competes for binding to Tie2
and blocks Ang1-induced Tie2 autophosphorylation (2).
While Ang1 mRNA is mainly expressed in periendo-
thelial cells, including vascular smooth muscle (1, 3, 5),
Ang2 mRNA is selectively expressed in endothelial
cells (2). To date, the regulation of Ang1 mRNA expres-
sion is an unknown, but we do have some information
about the regulation of Ang2. Hypoxia, vascular endo-
thelial growth factor (VEGF) and basic fibroblast
growth factor upregulate Ang2 expression in endothe-
lial cells (6, 7). High levels of Ang2 mRNA are observed
in highly vascularized glioblastoma and hepatocellular
carcinoma (8, 9). Furthermore, histological analyses
indicate that Ang2 expression plays a key role in tumor
angiogenesis, both at early and later stages of vascular
activation (10). Angiogenesis is also an essential pro-
cess during inflammation (11). However, it is unknown
whether Ang2 is involved during inflammation.
In this study, we examined the effect of a well-known
proinflammatory cytokine, TNF-a, on Ang2 expression
in human umbilical vein endothelial cells (HUVECs).
The present results indicate that TNF-a induces Ang2
expression, at least in part, through intracellular
NF-kB activation. Our results suggest that TNF-a-
induced Ang2 expression might be involved in inflam-
matory angiogenesis.
MATERIALS AND METHODS
Materials and cell culture. Recombinant human TNF-a was pur-
chased from R&D systems (Minneapolis, MN). NF-kB SN50 and
NF-kB SN50M were purchased from Calbiochem (La Jolla, CA).
Media and sera were obtained from Life Technology, Inc (Gaithers-
burg, MD). Most other biochemical reagents were purchased from
Sigma (St. Louis, MO), unless otherwise specified. HUVECs were
prepared from human umbilical cords by collagenase digestion as
described previously (12). The endothelial origin of the cultures was
confirmed by immunofluorescent staining with an anti-von Wille-
brand factor antibody; acceptable cultures had .95% fluorescent
cells. These endothelial cells were maintained in M-199 medium
supplemented with 20% (vol/vol) heat-inactivated fetal bovine serum
at 37°C in 5% CO
2
. The primary cultured cells used in this study
were between passage 2 and 4.
Reverse transcriptase-polymerase chain reaction (RT-PCR) and
Northern blot analysis. Total RNA (100 ng) from HUVECs was
suspended in 100 ml of RT buffer (10 mM Tris-HCl, pH 8.3; 50 mM
1
To whom correspondence should be addressed at National Cre-
ative Research Initiatives Center for Cardiac Regeneration, Chon-
buk University School of Medicine, San 2-20, Keum-Am-Dong,
Chonju, 560-180, Republic of Korea. Fax: 82-652-270-4071. E-mail:
gykoh@moak.chonbuk.ac.kr.
Biochemical and Biophysical Research Communications 269, 361–365 (2000)
doi:10.1006/bbrc.2000.2296, available online at http://www.idealibrary.com on
361 0006-291X/00 $35.00
Copyright © 2000 by Academic Press
All rights of reproduction in any form reserved.