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Published in: Clinical and Experimental Medicine 1/2019

01-02-2019 | Original Article

Association between IL-35 and coronary arterial lesions in children with Kawasaki disease

Authors: Ya Su, Siqi Feng, Li Luo, Ruixi Liu, Qijian Yi

Published in: Clinical and Experimental Medicine | Issue 1/2019

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Abstract

Kawasaki disease (KD) arises due to the acute inflammation and immune system dysfunction. This study investigated the relationship between the serum level of IL-35 and coronary artery lesions (CALs) in patients with KD. We obtained blood samples from 90 children with KD before intravenous immunoglobulin therapy. Levels of IL-35, IL-6, IL-17A, IL-10, MCP-1 and VEGF were measured in 190 cases, including 4 groups: KD with coronary arterial lesions (n = 46), KD without coronary arteries lesions (n = 44), febrile control group (FC, n = 40) and the normal control group (NC, n = 60). White blood cell counts (WBC), red blood cell counts (RBC), hemoglobin, platelet, C-reactive protein (CRP), erythrocyte sedimentation rate (ESR) and procalcitonin were tested in all subjects. Levels of IL-35, RBC and hemoglobin significantly decreased, and IL-6, IL-17A, IL-10, MCP-1 and VEGF were significantly elevated in the KD group compared with febrile and control groups. IL-35 serum level even decreased, and ESR, IL-6, MCP-1 and VEGF increased in the KD patients with CALs. Serum levels of IL-35 in KD patients were negatively associated with WBC, CRP, IL-6, IL-17A, IL-10, MCP-1 and VEGF in children with KD. IL-35 may have the effect on inhibiting inflammatory process in KD and further preventing KD patients from coronary artery lesion.
Literature
1.
go back to reference Kawasaki T, Kosaki F, Okawa S, et al. A new infantile acute febrile mucocutaneous lymph node syndrome (MCLS) prevailing in Japan. Pediatrics. 1974;54:271–6.PubMed Kawasaki T, Kosaki F, Okawa S, et al. A new infantile acute febrile mucocutaneous lymph node syndrome (MCLS) prevailing in Japan. Pediatrics. 1974;54:271–6.PubMed
2.
go back to reference Kato H, Koike S, Yamamoto M, et al. Coronary aneurysms in infants and young children with acute febrile mucocutaneous lymph node syndrome. J Pediatr. 1975;86:892–8.CrossRefPubMed Kato H, Koike S, Yamamoto M, et al. Coronary aneurysms in infants and young children with acute febrile mucocutaneous lymph node syndrome. J Pediatr. 1975;86:892–8.CrossRefPubMed
5.
go back to reference Guo MMH, Tseng WN, Ko CH, et al. Th17- and Treg-related cytokine and mRNA expression are associated with acute and resolving Kawasaki disease. Allergy. 2015;70:310–8.CrossRefPubMed Guo MMH, Tseng WN, Ko CH, et al. Th17- and Treg-related cytokine and mRNA expression are associated with acute and resolving Kawasaki disease. Allergy. 2015;70:310–8.CrossRefPubMed
6.
go back to reference Cumming C, McCartyh P, van Hoff J, et al. Kawasaki disease associated with reactive hemophagocytic lymphohistiocytosis. Pediatr Infect Dis J. 2008;27(12):1116–8.CrossRef Cumming C, McCartyh P, van Hoff J, et al. Kawasaki disease associated with reactive hemophagocytic lymphohistiocytosis. Pediatr Infect Dis J. 2008;27(12):1116–8.CrossRef
7.
go back to reference Collison LW, Workman CJ, Kuo TT, et al. The inhibitory cytokine IL-35 contributes to regulatory T-cell function. Nature. 2007;450:566–9.CrossRefPubMed Collison LW, Workman CJ, Kuo TT, et al. The inhibitory cytokine IL-35 contributes to regulatory T-cell function. Nature. 2007;450:566–9.CrossRefPubMed
9.
go back to reference Li X, Mai J, Virtue A, et al. IL-35 is a novel responsive antiinflammatory cytokine—a new system of categorizing anti-inflammatory cytokines. PLoS ONE. 2012;7:e33628.CrossRefPubMedPubMedCentral Li X, Mai J, Virtue A, et al. IL-35 is a novel responsive antiinflammatory cytokine—a new system of categorizing anti-inflammatory cytokines. PLoS ONE. 2012;7:e33628.CrossRefPubMedPubMedCentral
10.
go back to reference Bettini M, Castellaw AH, Lennon GP, et al. Prevention of autoimmune diabetes by ectopic pancreatic β-cell expression of interleukin-35. Diabetes. 2012;61:1519–26.CrossRefPubMedPubMedCentral Bettini M, Castellaw AH, Lennon GP, et al. Prevention of autoimmune diabetes by ectopic pancreatic β-cell expression of interleukin-35. Diabetes. 2012;61:1519–26.CrossRefPubMedPubMedCentral
11.
go back to reference Chaturvedi V, Collison LW, Guy CS, et al. Cutting edge: human regulatory T cells require IL-35 to mediate suppression and infectious tolerance. J Immunol. 2011;186:6661–6.CrossRefPubMedPubMedCentral Chaturvedi V, Collison LW, Guy CS, et al. Cutting edge: human regulatory T cells require IL-35 to mediate suppression and infectious tolerance. J Immunol. 2011;186:6661–6.CrossRefPubMedPubMedCentral
12.
go back to reference Niedbala W, Wei XQ, Cai B, et al. IL-35 is a novel cytokine with therapeutic effects against collagen-induced arthritis through the expansion of regulatory T cells and suppression of Th17 cells. Eur J Immunol. 2007;37:3021–9.CrossRefPubMed Niedbala W, Wei XQ, Cai B, et al. IL-35 is a novel cytokine with therapeutic effects against collagen-induced arthritis through the expansion of regulatory T cells and suppression of Th17 cells. Eur J Immunol. 2007;37:3021–9.CrossRefPubMed
13.
go back to reference Lin Y, Huang Y, Lu Z, et al. Decreased plasma IL-35 levels are related to the left ventricular ejection fraction in coronary artery diseases. PLoS ONE. 2012;7(12):e52490.CrossRefPubMedPubMedCentral Lin Y, Huang Y, Lu Z, et al. Decreased plasma IL-35 levels are related to the left ventricular ejection fraction in coronary artery diseases. PLoS ONE. 2012;7(12):e52490.CrossRefPubMedPubMedCentral
14.
go back to reference JCS Joint Working Group. Guidelines for diagnosis and management of cardiovascular sequelae in Kawasaki disease (JCS 2008). Circ J. 2010;74:1989–2020.CrossRef JCS Joint Working Group. Guidelines for diagnosis and management of cardiovascular sequelae in Kawasaki disease (JCS 2008). Circ J. 2010;74:1989–2020.CrossRef
15.
go back to reference Japan Kawasaki Disease Research Committee. Report of subcommittee on standardization of diagnostic criteria and reporting of coronary artery lesions in Kawasaki disease. Tokyo: Ministry of Health and Welfare; 1984. Japan Kawasaki Disease Research Committee. Report of subcommittee on standardization of diagnostic criteria and reporting of coronary artery lesions in Kawasaki disease. Tokyo: Ministry of Health and Welfare; 1984.
16.
go back to reference Wirtz S, Billmeier U, Mchedlidze T, et al. Interleukin-35 mediates mucosal immune responses that protect against T-cell-dependent colitis. Gastroenterology. 2011;141(5):1875–86.CrossRefPubMedPubMedCentral Wirtz S, Billmeier U, Mchedlidze T, et al. Interleukin-35 mediates mucosal immune responses that protect against T-cell-dependent colitis. Gastroenterology. 2011;141(5):1875–86.CrossRefPubMedPubMedCentral
17.
go back to reference Zandian M, Mott KR, Allen SJ, et al. Use of cytokine immunotherapy to block CNS demyelination induced by a recombinant HSV-1 expressing IL-2. Gene Ther. 2011;18:734–42.CrossRefPubMedPubMedCentral Zandian M, Mott KR, Allen SJ, et al. Use of cytokine immunotherapy to block CNS demyelination induced by a recombinant HSV-1 expressing IL-2. Gene Ther. 2011;18:734–42.CrossRefPubMedPubMedCentral
18.
go back to reference Huang CH, Loo EX, Kuo IC, et al. Airway inflammation and IgE production induced by dust mite allergen-specific memory/effector Th2 cell line can be effectively attenuated by IL-35. J Immunol. 2011;187:462–71.CrossRefPubMed Huang CH, Loo EX, Kuo IC, et al. Airway inflammation and IgE production induced by dust mite allergen-specific memory/effector Th2 cell line can be effectively attenuated by IL-35. J Immunol. 2011;187:462–71.CrossRefPubMed
19.
20.
go back to reference Crome SQ, Wang AY, Levings MK. Translational mini-review series on Th17 cells: function and regulation of human T helper 17 cells in health and disease. Clin Exp Immunol. 2010;159:109–19.CrossRefPubMedPubMedCentral Crome SQ, Wang AY, Levings MK. Translational mini-review series on Th17 cells: function and regulation of human T helper 17 cells in health and disease. Clin Exp Immunol. 2010;159:109–19.CrossRefPubMedPubMedCentral
21.
go back to reference Jia S, Li C, Wang G, et al. The T helper type 17/regulatory T cell imbalance in patients with acute Kawasaki disease. Clin Exp Immunol. 2010;162:131–7.CrossRefPubMedPubMedCentral Jia S, Li C, Wang G, et al. The T helper type 17/regulatory T cell imbalance in patients with acute Kawasaki disease. Clin Exp Immunol. 2010;162:131–7.CrossRefPubMedPubMedCentral
22.
go back to reference Laan M, Cui ZH, Hoshino H, et al. Neutrophil recruitment by human IL-17 via C-X-C chemokine release in the airways. J Immunol. 1999;162:2347–52.PubMed Laan M, Cui ZH, Hoshino H, et al. Neutrophil recruitment by human IL-17 via C-X-C chemokine release in the airways. J Immunol. 1999;162:2347–52.PubMed
23.
go back to reference Afzali B, Mitchell P, Lechler RI, et al. Translational mini-review series on Th17 cells: induction of interleukin-17 production by regulatory T cells. Clin Exp Immunol. 2010;159:120–30.CrossRefPubMedPubMedCentral Afzali B, Mitchell P, Lechler RI, et al. Translational mini-review series on Th17 cells: induction of interleukin-17 production by regulatory T cells. Clin Exp Immunol. 2010;159:120–30.CrossRefPubMedPubMedCentral
24.
go back to reference Nakano S, Morimoto S, Suzuki S, et al. Immunoregulatory role of IL-35 in T cells of patients with rheumatoid arthritis. Rheumatology (Oxford). 2015;54:1498–506.CrossRef Nakano S, Morimoto S, Suzuki S, et al. Immunoregulatory role of IL-35 in T cells of patients with rheumatoid arthritis. Rheumatology (Oxford). 2015;54:1498–506.CrossRef
25.
26.
go back to reference Lalani I, Bhol K, Ahmed AR. Interleukin-10: biology, role in inflammation and autoimmunity. Ann Allergy Asthma Immunol. 1997;79(6):469–83.CrossRefPubMed Lalani I, Bhol K, Ahmed AR. Interleukin-10: biology, role in inflammation and autoimmunity. Ann Allergy Asthma Immunol. 1997;79(6):469–83.CrossRefPubMed
27.
go back to reference Kochetkova I, Golden S, Holderness K, et al. IL-35 stimulation of CD39 + regulatory T cells confers protection against collagen II-induced arthritis via the production of IL-10. J Immunol. 2010;184:7144–53.CrossRefPubMedPubMedCentral Kochetkova I, Golden S, Holderness K, et al. IL-35 stimulation of CD39 + regulatory T cells confers protection against collagen II-induced arthritis via the production of IL-10. J Immunol. 2010;184:7144–53.CrossRefPubMedPubMedCentral
28.
go back to reference Leonard EJ, Yoshimura T. Human monocyte chemoattractant protein-1 (MCP-1). Immunol Today. 1990;11:97–101.CrossRefPubMed Leonard EJ, Yoshimura T. Human monocyte chemoattractant protein-1 (MCP-1). Immunol Today. 1990;11:97–101.CrossRefPubMed
29.
go back to reference Matsushima K, Larsen CG, Dubois GC, et al. Purification and characterization of a novel monocyte chemotactic and activating actor produced by a human myelomonocytic cell line. J Exp Med. 1985;169:1485–90.CrossRef Matsushima K, Larsen CG, Dubois GC, et al. Purification and characterization of a novel monocyte chemotactic and activating actor produced by a human myelomonocytic cell line. J Exp Med. 1985;169:1485–90.CrossRef
30.
go back to reference Terai M, Jibiki T, Harada A, et al. Dramatic decrease of circulating levels of monocyte chemoattractant protein-1 in kawasaki disease after gamma globulin treatment. J Leukoc Biol. 1999;65:566–72.CrossRefPubMed Terai M, Jibiki T, Harada A, et al. Dramatic decrease of circulating levels of monocyte chemoattractant protein-1 in kawasaki disease after gamma globulin treatment. J Leukoc Biol. 1999;65:566–72.CrossRefPubMed
31.
go back to reference Asano T, Ogawa S. Expression of monocyte chemoattractant protein-1 in Kawasaki disease: the anti-inflammatory effect of gamma globulin therapy. Scand J Immunol. 2000;51(1):98–103.CrossRefPubMed Asano T, Ogawa S. Expression of monocyte chemoattractant protein-1 in Kawasaki disease: the anti-inflammatory effect of gamma globulin therapy. Scand J Immunol. 2000;51(1):98–103.CrossRefPubMed
32.
go back to reference Filková M, Vernerová Z, Hulejová H, et al. Pro-inflammatory effects of interleukin-35 in rheumatoid arthritis. Cytokine. 2015;73:36–43.CrossRefPubMed Filková M, Vernerová Z, Hulejová H, et al. Pro-inflammatory effects of interleukin-35 in rheumatoid arthritis. Cytokine. 2015;73:36–43.CrossRefPubMed
33.
go back to reference Koyanagi H, Nakayama Y, Yanagawa H. Lower level of serum potassium and higher level of C-reactive protein as an independent risk factor for giant aneurysms in Kawasaki disease. Acta Paediatr. 1998;87:32–6.CrossRefPubMed Koyanagi H, Nakayama Y, Yanagawa H. Lower level of serum potassium and higher level of C-reactive protein as an independent risk factor for giant aneurysms in Kawasaki disease. Acta Paediatr. 1998;87:32–6.CrossRefPubMed
34.
go back to reference Connolly DT, Heuvelman DM, Nelson R, et al. Tumor vascular permeability factor stimulates endothelial cell growth and angiogenesis. J Clin Invest. 1989;84:1470–8.CrossRefPubMedPubMedCentral Connolly DT, Heuvelman DM, Nelson R, et al. Tumor vascular permeability factor stimulates endothelial cell growth and angiogenesis. J Clin Invest. 1989;84:1470–8.CrossRefPubMedPubMedCentral
35.
go back to reference Leung DYW, Cachianes G, Kuang W-J, et al. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science. 1989;246:1306–9.CrossRefPubMed Leung DYW, Cachianes G, Kuang W-J, et al. Vascular endothelial growth factor is a secreted angiogenic mitogen. Science. 1989;246:1306–9.CrossRefPubMed
36.
go back to reference Ohno T, Yuge T, Kariyazono H, et al. Serum hepatocyte growth factor combined with vascular endothelial growth factor as a predictive indicator for the occurrence of coronary artery lesions in Kawasaki disease. Eur J Pediatr. 2002;161:105–11.CrossRefPubMed Ohno T, Yuge T, Kariyazono H, et al. Serum hepatocyte growth factor combined with vascular endothelial growth factor as a predictive indicator for the occurrence of coronary artery lesions in Kawasaki disease. Eur J Pediatr. 2002;161:105–11.CrossRefPubMed
37.
go back to reference Hamamichi Y, Ichida F, Yu X, et al. Neutrophils and mononuclear cells express vascular endothelial growth factor in acute Kawasaki disease: its possible role in progression of coronary artery lesions. Pediatr Res. 2001;49:74–80.CrossRefPubMed Hamamichi Y, Ichida F, Yu X, et al. Neutrophils and mononuclear cells express vascular endothelial growth factor in acute Kawasaki disease: its possible role in progression of coronary artery lesions. Pediatr Res. 2001;49:74–80.CrossRefPubMed
38.
go back to reference Suqin W, Li Y, Li Y. Interleukin-35 attenuates collagen-induced arthritis through suppression of vascular endothelial growth factor and its receptors. Int Immunopharmacol. 2016;34:71–7.CrossRef Suqin W, Li Y, Li Y. Interleukin-35 attenuates collagen-induced arthritis through suppression of vascular endothelial growth factor and its receptors. Int Immunopharmacol. 2016;34:71–7.CrossRef
39.
go back to reference Jiang S, Li Y, Lin T, et al. IL-35 inhibits angiogenesis through VEGF/Ang2/Tie2 pathway in rheumatoid arthritis. Cell Physiol Biochem. 2016;40:1105–16.CrossRefPubMed Jiang S, Li Y, Lin T, et al. IL-35 inhibits angiogenesis through VEGF/Ang2/Tie2 pathway in rheumatoid arthritis. Cell Physiol Biochem. 2016;40:1105–16.CrossRefPubMed
Metadata
Title
Association between IL-35 and coronary arterial lesions in children with Kawasaki disease
Authors
Ya Su
Siqi Feng
Li Luo
Ruixi Liu
Qijian Yi
Publication date
01-02-2019
Publisher
Springer International Publishing
Published in
Clinical and Experimental Medicine / Issue 1/2019
Print ISSN: 1591-8890
Electronic ISSN: 1591-9528
DOI
https://doi.org/10.1007/s10238-018-0513-6

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