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Induction of MCP1, CCR2, and Inos Expression in THP-1 Macrophages by Serum of Children Late After Kawasaki Disease

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Induction of MCP1, CCR2, and Inos Expression in THP-1 Macrophages by Serum of Children Late After Kawasaki Disease 0031-3998/05/5806-1306 PEDIATRIC RESEARCH Vol. 58, No. 6, 2005 Copyright © 2005 International Pediatric Research Foundation, Inc. Printed in U.S.A. Induction of MCP1, CCR2, and iNOS Expression in THP-1 Macrophages by Serum of Children Late After Kawasaki Disease YIU-FAI CHEUNG, KARMIN O, SIDNEY C. F. TAM, AND YAW L. SIOW Department of Paediatrics and Adolescent Medicine [Y.-F.C.], Grantham Hospital, The University of Hong Kong, Hong Kong, China; Departments of Animal Science and Physiology [K.O.], St. Boniface Hospital Research Centre, University of Manitoba, Winnipeg, Manitoba R2H 2A6, Canada; Department of Physiology [K.O., Y.L.S.], Centre for Research and Treatment of Atherosclerosis, University of Manitoba, Winnipeg, Manitoba R3E 0W3, Canada; Division of Clinical Biochemistry [S.C.F.T.], Queen Mary Hospital, Hong Kong, China ABSTRACT Evidence of premature atherosclerosis late after Kawasaki eurysms. The magnitude of induction of MCP-1, CCR2, and disease (KD) is accumulating. Given the potential roles of mono- iNOS or in combinations correlated positively with serum high- cyte chemoattractant protein-1 (MCP-1), chemokine receptor sensitivity C-reactive protein (hs-CRP), and low-density lipopro- CCR-2, and inducible nitric oxide synthase (iNOS) in atherogen- tein (LDL) cholesterol levels and negatively with high-density esis, we sought to determine whether serum obtained from lipoprotein (HDL) cholesterol level. In conclusion, the serum of children late after KD would induce expression of these genes in patients with a history of KD induces expression of MCP-1, macrophages in vitro. A total of 79 subjects were studied, which CCR2, and iNOS in THP-1 macrophages in vitro. Induction of comprised 57 KD patients, 33 of whom had coronary aneurysms, these genes in vivo may be related to chronic inflammation and and 22 age-matched controls. Expression of MCP-1, CCR2, and may have important implications for premature atherosclerosis. iNOS mRNA in THP-1 macrophages in the presence of patient (Pediatr Res 58: 1306–1310, 2005) and control serum was quantified as a ratio to ␤-actin mRNA and expressed as a percentage of control. MCP-1 expression was Abbreviations significantly increased in the presence of serum from patients hs-CRP, high-sensitivity C-reactive protein with coronary aneurysms. Expression of CCR2 and iNOS was iNOS, inducible nitric oxide synthase significantly increased when THP-1 macrophages were incu- KD, Kawasaki disease bated with serum from patients with and without coronary an- MCP-1, monocyte chemoattractant protein-1 KD is at present the most common acquired heart disease in atherosclerosis (8), has been found to be significantly increased children in developed countries (1). It has been more than 25 y in patients studied at about 10 y after the acute illness (9). since its first description and concerns have been raised regard- While there is growing evidence to suggest premature athero- ing the possibility of its predisposition to premature athero- sclerosis in patients with a history of KD, the underlying sclerosis later in life (2–6). We have previously reported on the mechanism remains unknown. adverse cardiovascular risk profile, as characterized by a Inflammatory processes play a pivotal role in atherogenesis proatherogenic alteration of lipid profile and increased periph- (10). Recently, we (11) and the others (12) have provided eral conduit arterial stiffness, in children with a history of KD evidence that low-grade chronic inflammation may continue (7). Furthermore, carotid intima-media thickness, a marker of unabated after the acute phase of KD. One of the important features of atherosclerosis is infiltration of monocytes into the injured arterial wall followed by their differentiation into mac- rophages (13). Recent evidence suggests that the inflammatory Received February 28, 2005; accepted April 29, 2005 response in vascular injury involves recruitment and activation Correspondence: Y.-F. Cheung, M.D., Division of Paediatric Cardiology, Department of monocytes through activation of the MCP-1 (10,14,15), a of Paediatrics and Adolescent Medicine, Grantham Hospital, The University of Hong potent chemotactic factor for monocytes. In both human and Kong, 125 Wong Chuk Hang Road, Hong Kong, China; e-mail: [email protected] Supported in part by the CRCG Research Grant, Faculty of Medicine, The University experimental animal models (16), expression of the MCP-1 of Hong Kong. mRNA and protein has been found to be markedly elevated in DOI: 10.1203/01.pdr.0000183360.79872.1c atherosclerotic lesions. MCP-1 exerts its action mainly through 1306 MCP1, CCR2, AND INOS EXPRESSION AFTER KD 1307 the interaction with the chemokine receptor CCR2 on the for 5 min at 95°C, 35 cycles of amplification (95°C for 45 s, 55°C for 50 s, and surface of monocytes (17). 72°C for 90 s), and an additional 10-min extension at 72°C. The PCR products were separated by 1.8% agarose gel (containing 0.5 ␮g/mL ethidium bromide) Apart from the MCP-1/CCR2 pathway, the possible role of electrophoresis. Bands corresponding to MCP-1 mRNA and ␤-actin were iNOS in atherogenesis has also been implicated (18). The visualized using autoradiography and analyzed using a gel documentation ␤ iNOS is expressed mainly in the macrophages. Prolonged system (Bio-Rad Gel Doc1000). The ratio of MCP-1 mRNA to -actin mRNA was calculated and values were expressed as a percentage of control. Similar production of nitric oxide at high levels upon iNOS induction experiments were carried out to determine the expression of CCR2 and iNOS may lead to cell injury in the vessels and may play a role in the mRNA in the THP-1 macrophages. The nucleotide sequences of primers for atherosclerotic process via mechanisms relating to enhance- CCR2 were 5=-ATG CTG TCC ACA TCT CGT TCT CG-3= and 5=-TTA TAA ACC AGC CGA GAC TTC CTG C-3=. The nucleotide sequences of primers ment of oxidative stress (19,20). Indeed, iNOS expression has for iNOS were 5=-CGG TGC TGT ATT TCC TTA CGA GGC GAA GAA been demonstrated in atheromatous plaque (21) and its expres- GG-3= and 5=-GGT GCT GCT TGT TAG GAG GTC AAG TAA AGG GC. Ϯ sion correlates with atherosclerotic intimal thickening (22). Statistical analysis. Data are presented as mean SEM. Differences in demographic data and serum lipid levels between patients and control subjects Given the growing evidence of premature atherosclerosis in were compared using unpaired t test. Patients with and without coronary patients with a history of KD and the potential roles of MCP-1, aneurysms were grouped together for comparison with control subjects as they CCR2, and iNOS in atherogenesis, we determined in the had no statistically significant differences in these variables. For the entire cohort, Pearson correlation analysis was used to assess for possible relation- present study whether the serum obtained from children late ships between gene expression levels and serum hs-CRP, cholesterol, and after KD would induce the expression of these genes in the triglyceride levels. High-sensitivity CRP levels in the patients and controls macrophages in vitro. We further determined the effects of were expressed as median and interquartile range and compared using Mann- Whitney U test. As hs-CRP levels showed a skewed distribution, logarithmi- serum hs-CRP and lipids, known to be altered in the long term cally transformed CRP values were used in correlation analysis. A p value after KD (7,11,12,23) and that may affect chemokine and Ͻ0.05 was considered statistically significant. All statistical analyses were chemokine receptor expression (24–27), on the magnitude of performed using SPSS version 10.0 (SPSS, Inc., Chicago, IL). gene expression. RESULTS METHODS Subjects. A total of 79 subjects were studied, comprising 57 patients after KD and 22 controls subjects. Of the 57 patients Subjects. Patients with a history of KD were recruited from the pediatric who all had received i.v. immunoglobulin during the acute cardiac clinic of Grantham Hospital. Patients diagnosed to have KD within 12 phase of the illness, 33 had coronary aneurysms. The patients mo of study were excluded to minimize potential confounding influence Ϯ relating to subacute inflammation (28). From the medical records, the follow- were studied at 7.0 0.4 y after KD. None were symptomatic ing data were collected: interval from disease onset to the time of study, and none required coronary arterial interventions. All of the coronary complications, and cardiac symptoms at the time of study. Coronary subjects were Chinese in origin. The demographic data of the aneurysms were documented by serial two-dimensional echocardiography. Healthy age-matched subjects were recruited as controls. These were healthy patients and controls are summarized in Table 1. There were no children previously discharged from our clinic with a diagnosis of a functional significant differences in age, sex distribution, and body mass heart murmur and their healthy siblings. The subjects presented for study after index between patients and controls. an overnight fast. Body weight and height were measured, and body mass index was calculated accordingly. The Institutional Review Board of the Effects of patient serum on gene expression. The effects of University of Hong Kong/Hospital Authority Hong Kong West Cluster ap- incubating THP-1 macrophages in the presence of serum from proved the study, and parents of all subjects gave written, informed consent. patients and controls on MCP-1, CCR2 and iNOS expression Blood investigations. Venous blood was withdrawn for measurement of fasting total cholesterol, HDL and LDL cholesterol and triglyceride levels. are shown in Figure 1. Serum total cholesterol level was determined enzymatically using a Hitachi MCP-1 expression in THP-1 macrophages was significantly 912 analyzer (Roche Diagnostics, GmbH, Mannheim, Germany). HDL cho- greater when incubated with serum from patients with coronary lesterol was measured using a homogeneous method with polyethylene glycol– Ϯ ϭ modified enzymes and sulfated ␣-cyclodextrin.
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