The Journal of Rheumatology 2003; 30:2 326
2002-238-1
From the Orthopaedic Research Laboratory and the Division of
Orthopaedic Surgery, Stanford University School of Medicine, Stanford;
and the RR&D Center, Veterans Affairs Palo Alto Health Care System,
Palo Alto, California, USA.
Supported by NIH Grant AR45788.
M.S. Lee, MD, Assistant Professor, Chang Gung Memorial Hospital,
Taiwan, ROC; M.C.D. Trindade, MS, Medical Student; T. Ikenoue, MD,
Postdoctoral fellow; R.L. Smith, PhD, Professor (Research), Orthopaedic
Research Laboratory; D.J. Schurman, MD, Professor; S.B. Goodman,
MD, PhD, Professor, Division of Orthopaedic Surgery.
Address reprint requests to Dr. R.L. Smith, Orthopaedic Research
Laboratory, Stanford University School of Medicine,
300 Pasteur Drive, R144, Stanford, CA, 94305-5341, USA.
E-mail: smith@rrdmail.stanford.edu
Submitted March 14, 2002; revision accepted June 4, 2002.
Articular chondrocytes respond to mechanical stimuli by
altered matrix macromolecule expression and release of
soluble mediators, including nitric oxide (NO)
1-4
. NO serves
as multifunctional cellular messenger for an array of biolog-
ical processes and is implicated in rheumatological
diseases
5-7
. In bovine articular chondrocytes, induction of
NO by shear stress modulates matrix metabolism
8
. Other
types of mechanical loads may exert differential effects on
articular chondrocyte metabolism through NO
9,10
. We tested
effects of intermittent hydrostatic pressure (IHP) on NO
release by human osteoarthritic chondrocytes induced by
shear stress and matrix macromolecule gene expression
following exposure to shear stress or an NO donor.
MATERIALS AND METHODS
Cell culture. Human osteoarthritic chondrocytes were isolated from carti-
lage samples of 9 patients receiving total joint replacements as described
2
.
Chondrocytes were plated at a density of 5 × 10
4
/cm
2
, maintained in
DMEM/F12 supplemented with fetal bovine serum and antibiotics and
placed in serum-free medium 24 h prior to loading, as described
11
. The cells
were then exposed to mechanical loading in the presence of fresh serum-
free medium. Each experiment was carried out in duplicate and repeated
with 6 individual samples. To test the response of chondrocytes to IHP after
preconditioning with an NO donor, sodium nitroprusside (SNP) (Sigma
Chemical, St. Louis, MO, USA) was added to the cultures at concentrations
of 20 μM or 2000 μM, prior to mechanical loading. To test the response of
chondrocytes to IHP after treatment with shear stress, the cells were
exposed to shear stress for 2 h (200 rpm; 1.6 Pa) followed by transfer to a
pressure vessel for application of IHP.
Mechanical loading. IHP (10 MPa at 1 Hz) was applied to confluent cell
monolayers by placing the culture plates in heat-sealed bags filled with
serum-free medium, as described
2
. The loading of IHP included test periods
of 4 h per day for 1, 2 or 4 days.
NO release. Nitrite, the stable end product of NO oxidation, was used as an
indicator of NO synthesis. Nitrite concentration in the culture medium was
measured using the Griess reaction with sodium nitrite as the standard, as
described
8
.
Analysis of mRNA expression. Following loading, the cells were maintained
Intermittent Hydrostatic Pressure Inhibits Shear Stress-
Induced Nitric Oxide Release in Human Osteoarthritic
Chondrocytes in Vitro
MEL S. LEE, MICHAEL C.D. TRINDADE, TAKASHI IKENOUE, DAVID J. SCHURMAN, STUART B. GOODMAN,
and R. LANE SMITH
ABSTRACT. Objective. To test the effects of intermittent hydrostatic pressure (IHP) on nitric oxide (NO) release
induced by shear stress and matrix macromolecule gene expression in human osteoarthritic chon-
drocytes in vitro.
Methods. Chondrocytes isolated from cartilage samples from 9 patients with osteoarthritis were
cultured and exposed to either shear stress or an NO donor. Nitrite concentration was measured
using the Griess reaction. Matrix macromolecule mRNA signal levels were determined using
reverse-transcriptase polymerase chain reaction and quantified by imaging analysis software.
Results. Exposure to shear stress upregulated NO release in a dose and time-dependent manner.
Application of IHP inhibited shear stress induced NO release but did not alter NO release from
chondrocytes not exposed to shear stress. Shear stress induced NO or addition of an NO donor
(sodium nitroprusside) was associated with decreased mRNA signal levels for the cartilage matrix
proteins, aggrecan, and type II collagen. Intermittent hydrostatic pressure blocked the inhibitory
effects of sodium nitroprusside but did not alter the inhibitory effects of shear stress on cartilage
macromolecule gene expression.
Conclusion. Our data show that shear stress and IHP differentially alter chondrocyte metabolism
and suggest that a balance of effects between different loading forces preserve cartilage extracel-
lular matrix in vivo. (J Rheumatol 2003;30:326–8)
Key Indexing Terms:
NITRIC OXIDE MECHANICAL LOADS OSTEOARTHRITIS
CHONDROCYTES AGGRECAN COLLAGEN
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