A possible contribution of lipocalin-2 to the development of dermal fibrosis, pulmonary vascular involvement and renal dysfunction in systemic sclerosis

Summary Background Lipocalin‐2 is an adipocytokine implicated in apoptosis, innate immunity, angiogenesis, and the development of chronic kidney disease. Objectives To investigate the role of lipocalin‐2 in systemic sclerosis (SSc). Materials and methods Serum lipocalin‐2 levels were determined by e...

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Published inBritish journal of dermatology (1951) Vol. 173; no. 3; pp. 681 - 689
Main Authors Takahashi, T., Asano, Y., Noda, S., Aozasa, N., Akamata, K., Taniguchi, T., Ichimura, Y., Toyama, T., Sumida, H., Kuwano, Y., Tada, Y., Sugaya, M., Kadono, T., Sato, S.
Format Journal Article
LanguageEnglish
Published England Blackwell Publishing Ltd 01.09.2015
Oxford University Press
Subjects
Acute-Phase Proteins - metabolism
Acute-Phase Proteins - physiology
Adult
Aged
Angiogenesis
Animals
Apoptosis
Apoptosis - physiology
Bleomycin
Blood pressure
Case-Control Studies
Endothelial cells
Female
Fibroblasts
Fibrosis
Fibrosis - etiology
Fibrosis - pathology
Fibrosis - physiopathology
Glomerular filtration rate
Glomerular Filtration Rate - physiology
Heart
Humans
Immunoblotting
Immunohistochemistry
Kidney diseases
Lipocalin
Lipocalin-2
Lipocalins - metabolism
Lipocalins - physiology
Lung diseases
Lung Diseases - etiology
Lung Diseases - physiopathology
Male
Matrix metalloproteinase
Metalloproteinase
Mice
Middle Aged
Polymerase chain reaction
Proto-Oncogene Proteins - metabolism
Proto-Oncogene Proteins - physiology
Pulmonary hypertension
Renal function
Renal Insufficiency, Chronic - etiology
RNA-directed DNA polymerase
Scleroderma
Scleroderma, Systemic - etiology
Scleroderma, Systemic - pathology
Scleroderma, Systemic - physiopathology
Sclerosis
Skin - pathology
Skin diseases
Skin Diseases, Vascular - etiology
Skin Diseases, Vascular - physiopathology
Systemic sclerosis
Vascular diseases
Vascular Diseases - etiology
Vascular Diseases - pathology
Vascular Diseases - physiopathology
Ventricle
Online AccessGet full text
ISSN0007-0963
1365-2133
1365-2133
DOI10.1111/bjd.13779

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Abstract Summary Background Lipocalin‐2 is an adipocytokine implicated in apoptosis, innate immunity, angiogenesis, and the development of chronic kidney disease. Objectives To investigate the role of lipocalin‐2 in systemic sclerosis (SSc). Materials and methods Serum lipocalin‐2 levels were determined by enzyme‐linked immunosorbent assay in 50 patients with SSc and 19 healthy subjects. Lipocalin‐2 expression was evaluated in the skin of patients with SSc and bleomycin (BLM)‐treated mice and in Fli1‐deficient endothelial cells by reverse transcriptase‐real time polymerase chain reaction, immunoblotting and/or immunohistochemistry. Results Although serum lipocalin‐2 levels were comparable between patients with SSc and healthy controls, the prevalence of scleroderma renal crisis was significantly higher in patients with SSc with elevated serum lipocalin‐2 levels than in those with normal levels. Furthermore, serum lipocalin‐2 levels inversely correlated with estimated glomerular filtration rate in patients with SSc with renal dysfunction. Among patients with SSc with normal renal function, serum lipocalin‐2 levels positively correlated with skin score in patients with diffuse cutaneous SSc with disease duration of < 3 years and inversely correlated with estimated right ventricular systolic pressure in total patients with SSc. Importantly, in SSc lesional skin, lipocalin‐2 expression was increased in dermal fibroblasts and endothelial cells. In BLM‐treated mice, lipocalin‐2 was highly expressed in dermal fibroblasts, but not in endothelial cells. On the other hand, the deficiency of transcription factor Fli1, which is implicated in SSc vasculopathy, induced lipocalin‐2 expression in cultivated endothelial cells. Conclusions Lipocalin‐2 may be involved in renal dysfunction and dermal fibrosis of SSc. Dysregulated matrix metalloproteinase‐9/lipocalin‐2‐dependent angiogenesis due to Fli1 deficiency may contribute to the development of pulmonary arterial hypertension associated with SSc. What's already known about this topic? Adipokines have been shown to play various important roles in systemic sclerosis (SSc). Lipocalin‐2 is a member of the adipokines, which are implicated in apoptosis, innate immunity, angiogenesis, and the development of chronic kidney disease. What does this study add? Lipocalin‐2 potentially contributes to the development of skin sclerosis, pulmonary arterial hypertension and renal damage in SSc, further supporting the critical roles of adipokines in the pathogenesis of this disease.
AbstractList Lipocalin-2 is an adipocytokine implicated in apoptosis, innate immunity, angiogenesis, and the development of chronic kidney disease. To investigate the role of lipocalin-2 in systemic sclerosis (SSc). Serum lipocalin-2 levels were determined by enzyme-linked immunosorbent assay in 50 patients with SSc and 19 healthy subjects. Lipocalin-2 expression was evaluated in the skin of patients with SSc and bleomycin (BLM)-treated mice and in Fli1-deficient endothelial cells by reverse transcriptase-real time polymerase chain reaction, immunoblotting and/or immunohistochemistry. Although serum lipocalin-2 levels were comparable between patients with SSc and healthy controls, the prevalence of scleroderma renal crisis was significantly higher in patients with SSc with elevated serum lipocalin-2 levels than in those with normal levels. Furthermore, serum lipocalin-2 levels inversely correlated with estimated glomerular filtration rate in patients with SSc with renal dysfunction. Among patients with SSc with normal renal function, serum lipocalin-2 levels positively correlated with skin score in patients with diffuse cutaneous SSc with disease duration of < 3 years and inversely correlated with estimated right ventricular systolic pressure in total patients with SSc. Importantly, in SSc lesional skin, lipocalin-2 expression was increased in dermal fibroblasts and endothelial cells. In BLM-treated mice, lipocalin-2 was highly expressed in dermal fibroblasts, but not in endothelial cells. On the other hand, the deficiency of transcription factor Fli1, which is implicated in SSc vasculopathy, induced lipocalin-2 expression in cultivated endothelial cells. Lipocalin-2 may be involved in renal dysfunction and dermal fibrosis of SSc. Dysregulated matrix metalloproteinase-9/lipocalin-2-dependent angiogenesis due to Fli1 deficiency may contribute to the development of pulmonary arterial hypertension associated with SSc.
Summary Background Lipocalin‐2 is an adipocytokine implicated in apoptosis, innate immunity, angiogenesis, and the development of chronic kidney disease. Objectives To investigate the role of lipocalin‐2 in systemic sclerosis (SSc). Materials and methods Serum lipocalin‐2 levels were determined by enzyme‐linked immunosorbent assay in 50 patients with SSc and 19 healthy subjects. Lipocalin‐2 expression was evaluated in the skin of patients with SSc and bleomycin (BLM)‐treated mice and in Fli1‐deficient endothelial cells by reverse transcriptase‐real time polymerase chain reaction, immunoblotting and/or immunohistochemistry. Results Although serum lipocalin‐2 levels were comparable between patients with SSc and healthy controls, the prevalence of scleroderma renal crisis was significantly higher in patients with SSc with elevated serum lipocalin‐2 levels than in those with normal levels. Furthermore, serum lipocalin‐2 levels inversely correlated with estimated glomerular filtration rate in patients with SSc with renal dysfunction. Among patients with SSc with normal renal function, serum lipocalin‐2 levels positively correlated with skin score in patients with diffuse cutaneous SSc with disease duration of < 3 years and inversely correlated with estimated right ventricular systolic pressure in total patients with SSc. Importantly, in SSc lesional skin, lipocalin‐2 expression was increased in dermal fibroblasts and endothelial cells. In BLM‐treated mice, lipocalin‐2 was highly expressed in dermal fibroblasts, but not in endothelial cells. On the other hand, the deficiency of transcription factor Fli1, which is implicated in SSc vasculopathy, induced lipocalin‐2 expression in cultivated endothelial cells. Conclusions Lipocalin‐2 may be involved in renal dysfunction and dermal fibrosis of SSc. Dysregulated matrix metalloproteinase‐9/lipocalin‐2‐dependent angiogenesis due to Fli1 deficiency may contribute to the development of pulmonary arterial hypertension associated with SSc. What's already known about this topic? Adipokines have been shown to play various important roles in systemic sclerosis (SSc). Lipocalin‐2 is a member of the adipokines, which are implicated in apoptosis, innate immunity, angiogenesis, and the development of chronic kidney disease. What does this study add? Lipocalin‐2 potentially contributes to the development of skin sclerosis, pulmonary arterial hypertension and renal damage in SSc, further supporting the critical roles of adipokines in the pathogenesis of this disease.
BackgroundLipocalin‐2 is an adipocytokine implicated in apoptosis, innate immunity, angiogenesis, and the development of chronic kidney disease.ObjectivesTo investigate the role of lipocalin‐2 in systemic sclerosis (SSc).Materials and methodsSerum lipocalin‐2 levels were determined by enzyme‐linked immunosorbent assay in 50 patients with SSc and 19 healthy subjects. Lipocalin‐2 expression was evaluated in the skin of patients with SSc and bleomycin (BLM)‐treated mice and in Fli1‐deficient endothelial cells by reverse transcriptase‐real time polymerase chain reaction, immunoblotting and/or immunohistochemistry.ResultsAlthough serum lipocalin‐2 levels were comparable between patients with SSc and healthy controls, the prevalence of scleroderma renal crisis was significantly higher in patients with SSc with elevated serum lipocalin‐2 levels than in those with normal levels. Furthermore, serum lipocalin‐2 levels inversely correlated with estimated glomerular filtration rate in patients with SSc with renal dysfunction. Among patients with SSc with normal renal function, serum lipocalin‐2 levels positively correlated with skin score in patients with diffuse cutaneous SSc with disease duration of < 3 years and inversely correlated with estimated right ventricular systolic pressure in total patients with SSc. Importantly, in SSc lesional skin, lipocalin‐2 expression was increased in dermal fibroblasts and endothelial cells. In BLM‐treated mice, lipocalin‐2 was highly expressed in dermal fibroblasts, but not in endothelial cells. On the other hand, the deficiency of transcription factor Fli1, which is implicated in SSc vasculopathy, induced lipocalin‐2 expression in cultivated endothelial cells.ConclusionsLipocalin‐2 may be involved in renal dysfunction and dermal fibrosis of SSc. Dysregulated matrix metalloproteinase‐9/lipocalin‐2‐dependent angiogenesis due to Fli1 deficiency may contribute to the development of pulmonary arterial hypertension associated with SSc.
Lipocalin-2 is an adipocytokine implicated in apoptosis, innate immunity, angiogenesis, and the development of chronic kidney disease.BACKGROUNDLipocalin-2 is an adipocytokine implicated in apoptosis, innate immunity, angiogenesis, and the development of chronic kidney disease.To investigate the role of lipocalin-2 in systemic sclerosis (SSc).OBJECTIVESTo investigate the role of lipocalin-2 in systemic sclerosis (SSc).Serum lipocalin-2 levels were determined by enzyme-linked immunosorbent assay in 50 patients with SSc and 19 healthy subjects. Lipocalin-2 expression was evaluated in the skin of patients with SSc and bleomycin (BLM)-treated mice and in Fli1-deficient endothelial cells by reverse transcriptase-real time polymerase chain reaction, immunoblotting and/or immunohistochemistry.MATERIALS AND METHODSSerum lipocalin-2 levels were determined by enzyme-linked immunosorbent assay in 50 patients with SSc and 19 healthy subjects. Lipocalin-2 expression was evaluated in the skin of patients with SSc and bleomycin (BLM)-treated mice and in Fli1-deficient endothelial cells by reverse transcriptase-real time polymerase chain reaction, immunoblotting and/or immunohistochemistry.Although serum lipocalin-2 levels were comparable between patients with SSc and healthy controls, the prevalence of scleroderma renal crisis was significantly higher in patients with SSc with elevated serum lipocalin-2 levels than in those with normal levels. Furthermore, serum lipocalin-2 levels inversely correlated with estimated glomerular filtration rate in patients with SSc with renal dysfunction. Among patients with SSc with normal renal function, serum lipocalin-2 levels positively correlated with skin score in patients with diffuse cutaneous SSc with disease duration of < 3 years and inversely correlated with estimated right ventricular systolic pressure in total patients with SSc. Importantly, in SSc lesional skin, lipocalin-2 expression was increased in dermal fibroblasts and endothelial cells. In BLM-treated mice, lipocalin-2 was highly expressed in dermal fibroblasts, but not in endothelial cells. On the other hand, the deficiency of transcription factor Fli1, which is implicated in SSc vasculopathy, induced lipocalin-2 expression in cultivated endothelial cells.RESULTSAlthough serum lipocalin-2 levels were comparable between patients with SSc and healthy controls, the prevalence of scleroderma renal crisis was significantly higher in patients with SSc with elevated serum lipocalin-2 levels than in those with normal levels. Furthermore, serum lipocalin-2 levels inversely correlated with estimated glomerular filtration rate in patients with SSc with renal dysfunction. Among patients with SSc with normal renal function, serum lipocalin-2 levels positively correlated with skin score in patients with diffuse cutaneous SSc with disease duration of < 3 years and inversely correlated with estimated right ventricular systolic pressure in total patients with SSc. Importantly, in SSc lesional skin, lipocalin-2 expression was increased in dermal fibroblasts and endothelial cells. In BLM-treated mice, lipocalin-2 was highly expressed in dermal fibroblasts, but not in endothelial cells. On the other hand, the deficiency of transcription factor Fli1, which is implicated in SSc vasculopathy, induced lipocalin-2 expression in cultivated endothelial cells.Lipocalin-2 may be involved in renal dysfunction and dermal fibrosis of SSc. Dysregulated matrix metalloproteinase-9/lipocalin-2-dependent angiogenesis due to Fli1 deficiency may contribute to the development of pulmonary arterial hypertension associated with SSc.CONCLUSIONSLipocalin-2 may be involved in renal dysfunction and dermal fibrosis of SSc. Dysregulated matrix metalloproteinase-9/lipocalin-2-dependent angiogenesis due to Fli1 deficiency may contribute to the development of pulmonary arterial hypertension associated with SSc.
Author Sumida, H.
Akamata, K.
Kuwano, Y.
Sugaya, M.
Asano, Y.
Aozasa, N.
Kadono, T.
Noda, S.
Ichimura, Y.
Sato, S.
Tada, Y.
Taniguchi, T.
Takahashi, T.
Toyama, T.
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  email: Yoshihide Asano., yasano-tky@umin.ac.jp
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Copyright 2015 British Association of Dermatologists
2015 British Association of Dermatologists.
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References Zhang J, Wu Y, Zhang Y et al. The role of lipocalin 2 in the regulation of inflammation in adipocytes and macrophages. Mol Endocrinol 2008; 22:1416-26.
van den Hoogen F, Khanna D, Fransen J et al. 2013 classification criteria for systemic sclerosis: an American College of Rheumatology/European League against Rheumatism collaborative initiative. Arthritis Rheum 2013; 65:2737-47.
Haase-Fielitz A, Bellomo R, Devarajan P et al. The predictive performance of plasma neutrophil gelatinase-associated lipocalin (NGAL) increases with grade of acute kidney injury. Nephrol Dial Transplant 2009; 24:3349-54.
Mishra J, Ma Q, Prada A et al. Identification of neutrophil gelatinase-associated lipocalin as a novel early urinary biomarker for ischemic renal injury. J Am Soc Nephrol 2003; 14:2534-43.
Liu JT, Song E, Xu A et al. Lipocalin-2 deficiency prevents endothelial dysfunction associated with dietary obesity: role of cytochrome P450 2C inhibition. Br J Pharmacol 2012; 165:520-31.
Masui Y, Asano Y, Akamata K et al. Serum resistin levels: a possible correlation with pulmonary vascular involvement in patients with systemic sclerosis. Rheumatol Int 2014; 34:1165-70.
Yoshizaki A, Iwata Y, Komura K et al. CD19 regulates skin and lung fibrosis via Toll-like receptor signaling in a model of bleomycin-induced scleroderma. Am J Pathol 2008; 172:1650-63.
Devarajan P. Emerging biomarkers of acute kidney injury. Contrib Nephrol 2007; 156:203-12.
Masui Y, Asano Y, Shibata S et al. A possible contribution of visfatin to t he resolution of skin sclerosis in patients with diffuse cutaneous systemic sclerosis via a direct anti-fibrotic effect on dermal fibroblasts and Th1 polarization of the immune response. Rheumatology (Oxford) 2013; 52:1239-44.
Li EM, Xu LY, Cai WJ et al. Functions of neutrophil gelatinase-associated lipocalin in the esophageal carcinoma cell line SHEEC. Sheng Wu Hua Xue Yu Sheng Wu Wu Li Xue Bao (Shanghai) 2003; 35:247-54.
Yan L, Borregaard N, Kjeldsen L et al. The high molecular weight urinary matrix metalloproteinase (MMP) activity is a complex of gelatinase B/MMP-9 and neutrophil gelatinase-associated lipocalin (NGAL). Modulation of MMP-9 activity by NGAL. J Biol Chem 2001; 276:37258-65.
Chung TW, Choi HJ, Kim CH et al. Lipocalin-2 elicited by advanced glycation end-products promotes the migration of vascular smooth muscle cells. Biochim Biophys Acta 2013; 1833:3386-95.
Kehrer JP. Lipocalin-2: pro- or anti-apoptotic? Cell Biol Toxicol 2010; 26:83-9.
van den Hoogen F, Khanna D, Fransen J et al. 2013 classification criteria for systemic sclerosis: an American College of Rheumatology/European League against Rheumatism collaborative initiative. Ann Rheum Dis 2013; 72:1747-55.
Flo TH, Smith KD, Sato S et al. Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron. Nature 2004; 432:917-21.
Kim JW, Lee SH, Jeong SH et al. Increased urinary lipocalin-2 reflects matrix metalloproteinase-9 activity in chronic hepatitis C with hepatic fibrosis. Tohoku J Exp Med 2010; 222:319-27.
Asano Y, Czuwara J, Trojanowska M. Transforming growth factor-beta regulates DNA binding activity of transcription factor Fli1 by p300/CREB-binding protein-associated factor-dependent acetylation. J Biol Chem 2007; 282:34672-83.
Giannelli G, Iannone F, Marinosci F et al. The effect of bosentan on matrix metalloproteinase-9 levels in patients with systemic sclerosis-induced pulmonary hypertension. Curr Med Res Opin 2005; 21:327-32.
Milner KL, van der Poorten D, Xu A et al. Adipocyte fatty acid binding protein levels relate to inflammation and fibrosis in nonalcoholic fatty liver disease. Hepatology 2009; 49:1926-34.
Toyama T, Asano Y, Takahashi T et al. Clinical significance of serum retinol binding protein-4 levels in patients with systemic sclerosis. J Eur Acad Dermatol Venereol 2013; 27:337-44.
Haase M, Bellomo R, Devarajan P et al. Accuracy of neutrophil gelatinase-associated lipocalin (NGAL) in diagnosis and prognosis in acute kidney injury: a systematic review and meta-analysis. Am J Kidney Dis 2009; 54:1012-24.
Yang J, Bielenberg DR, Rodig SJ et al. Lipocalin 2 promotes breast cancer progression. Proc Natl Acad Sci USA 2009; 106:3913-18.
Borkham-Kamphorst E, Drews F, Weiskirchen R. Induction of lipocalin-2 expression in acute and chronic experimental liver injury moderated by pro-inflammatory cytokines interleukin-1β through nuclear factor-κB activation. Liver Int 2011; 31:656-65.
Ko GJ, Grigoryev DN, Linfert D et al. Transcriptional analysis of kidneys during repair from AKI reveals possible roles for NGAL and KIM-1 as biomarkers of AKI-to-CKD transition. Am J Physiol Renal Physiol 2010; 298:F1472-83.
McReynolds MR, Taylor-Garcia KM, Greer KA et al. Renal medullary gene expression in aquaporin-1 null mice. Am J Physiol Renal Physiol 2005; 288:F315-21.
Matsushita T, Hasegawa M, Hamaguchi Y et al. Longitudinal analysis of serum cytokine concentrations in systemic sclerosis: association of interleukin 12 elevation with spontaneous regression of skin sclerosis. J Rheumatol 2006; 33:275-84.
Masui Y, Asano Y, Takahashi T et al. Clinical significance of monitoring serum adiponectin levels during intravenous pulse cyclophosphamide therapy in interstitial lung disease associated with systemic sclerosis. Mod Rheumatol 2013; 23:323-9.
Asano Y, Stawski L, Hant F et al. Endothelial Fli1 deficiency impairs vascular homeostasis: a role in scleroderma vasculopathy. Am J Pathol 2010; 176:1983-98.
Aozasa N, Asano Y, Akamata K et al. Serum apelin levels: clinical association with vascular involvements in patients with systemic sclerosis. J Eur Acad Dermatol Venereol 2013; 27:37-42.
Schermuly RT, Kreisselmeier KP, Ghofrani HA et al. Antiremodeling effects of iloprost and the dual-selective phosphodiesterase 3/4 inhibitor tolafentrine in chronic experimental pulmonary hypertension. Circ Res 2004; 94:1101-8.
Noda S, Asano Y, Aozasa N et al. Clinical significance of serum soluble Tie1 levels in patients with systemic sclerosis. Arch Dermatol Res 2013; 305:325-31.
Leng X, Ding T, Lin H et al. Inhibition of lipocalin 2 impairs breast tumorigenesis and metastasis. Cancer Res 2009; 69:8579-84.
Ichimura Y, Asano Y, Akamata K et al. Fli1 deficiency contributes to the suppression of endothelial CXCL5 expression in systemic sclerosis. Arch Dermatol Res 2014; 306:331-8.
Steen VD, Medsger TA Jr. Severe organ involvement in systemic sclerosis with diffuse scleroderma. Arthritis Rheum 2000; 43:2437-44.
Roy R, Louis G, Loughlin KR et al. Tumor-specific urinary matrix metalloproteinase fingerprinting: identification of high molecular weight urinary matrix metalloproteinase species. Clin Cancer Res 2008; 14:6610-17.
LeRoy E, Black C, Fleischmajer R et al. Scleroderma (systemic sclerosis): classification, subsets and pathogenesis. J Rheumatol 1988; 15:202-5.
Grigoryev DN, Mathai SC, Fisher MR et al. Identification of candidate genes in scleroderma-related pulmonary arterial hypertension. Transl Res 2008; 151:197-207.
Venkatesha S, Hanai J, Seth P et al. Lipocalin 2 antagonizes the proangiogenic action of ras in transformed cells. Mol Cancer Res 2006; 4:821-9.
Hanai J, Mammoto T, Seth P et al. Lipocalin 2 diminishes invasiveness and metastasis of Ras-transformed cells. J Biol Chem 2005; 280:13641-7.
Bauer M, Eickhoff JC, Gould MN et al. Neutrophil gelatinase-associated lipocalin (NGAL) is a predictor of poor prognosis in human primary breast cancer. Breast Cancer Res Treat 2008; 108:389-97.
Lin CW, Tseng SW, Yang SF et al. Role of lipocalin 2 and its complex with matrix metalloproteinase-9 in oral cancer. Oral Dis 2012; 18:734-40.
Feghali-Bostwick C, Medsger TA, Wright TM. Analysis of systemic sclerosis in twins reveals low concordance for disease and high concordance for the presence of antinuclear antibodies. Arthritis Rheum 2003; 48:1956-63.
Baraut J, Michel L, Verrecchia F et al. Relationship between cytokine profiles and clinical outcomes in patients with systemic sclerosis. Autoimmun Rev 2010; 10:65-73.
Song E, Fan P, Huang B et al. Deamidated lipocalin-2 induces endothelial dysfunction and hypertension in dietary obese mice. J Am Heart Assoc 2014; 3:e000837.
Wang Y, Fan PS, Kahaleh B. Association between enhanced type I collagen expression and epigenetic repression of the FLI1 gene in scleroderma fibroblasts. Arthritis Rheum 2006; 54:2271-9.
Asano Y. Future treatments in systemic sclerosis. J Dermatol 2010; 37:54-70.
Leng X, Lin H, Ding T et al. Lipocalin 2 is required for BCR-ABL-induced tumorigenesis. Oncogene 2008; 27:6110-19.
Lafyatis R, York M. Innate immunity and inflammation in systemic sclerosis. Curr Opin Rheumatol 2009; 21:617-22.
Masui Y, Asano Y, Shibata S et al. Serum adiponectin levels inversely correlate with the activity of progressive skin sclerosis in patients with diffuse cutaneous systemic sclerosis. J Eur Acad Dermatol Venereol 2012; 26:354-60.
Viau A, El Karoui K, Laouari D et al. Lipocalin 2 is essential for chronic kidney disease progression in mice and humans. J Clin Invest 2010; 120:4065-76.
Wang Y, Lam KS, Kraegen EW et al. Lipocalin-2 is an inflammatory marker closely associated with obesity, insulin resistance, and hyperglycemia in humans. Clin Chem 2007; 53:34-41.
Kjeldsen L, Johnsen AH, Sengeløv H et al. Isolation and primary structure of NGAL, a novel protein associated with human neutrophil gelatinase. J Biol Chem 1993; 268:10425-32.
Fernández CA, Yan L, Louis G et al. The matrix metalloproteinase-9/neutrophil gelatinase-associated lipocalin complex plays a role in breast tumor growth and is present in the urine of breast cancer patients. Clin Cancer Res 2005; 11:5390-5.
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Yang (10.1111/bjd.13779-BIB0026|bjd13779-cit-0026) 2009; 106
Asano (10.1111/bjd.13779-BIB0036|bjd13779-cit-0036) 2007; 282
Wang (10.1111/bjd.13779-BIB0041|bjd13779-cit-0041) 2006; 54
Feghali-Bostwick (10.1111/bjd.13779-BIB0040|bjd13779-cit-0040) 2003; 48
Asano (10.1111/bjd.13779-BIB0001|bjd13779-cit-0001) 2010; 37
McReynolds (10.1111/bjd.13779-BIB0014|bjd13779-cit-0014) 2005; 288
Masui (10.1111/bjd.13779-BIB0004|bjd13779-cit-0004) 2013; 52
Leng (10.1111/bjd.13779-BIB0031|bjd13779-cit-0031) 2008; 27
Roy (10.1111/bjd.13779-BIB0050|bjd13779-cit-0050) 2008; 14
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Hanai (10.1111/bjd.13779-BIB0025|bjd13779-cit-0025) 2005; 280
Song (10.1111/bjd.13779-BIB0051|bjd13779-cit-0051) 2014; 3
Flo (10.1111/bjd.13779-BIB0010|bjd13779-cit-0010) 2004; 432
Matsushita (10.1111/bjd.13779-BIB0045|bjd13779-cit-0045) 2006; 33
Ichimura (10.1111/bjd.13779-BIB0038|bjd13779-cit-0038) 2014; 306
Toyama (10.1111/bjd.13779-BIB0006|bjd13779-cit-0006) 2013; 27
Ko (10.1111/bjd.13779-BIB0015|bjd13779-cit-0015) 2010; 298
Li (10.1111/bjd.13779-BIB0030|bjd13779-cit-0030) 2003; 35
Bauer (10.1111/bjd.13779-BIB0029|bjd13779-cit-0029) 2008; 108
Steen (10.1111/bjd.13779-BIB0039|bjd13779-cit-0039) 2000; 43
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Hoogen (10.1111/bjd.13779-BIB0033|bjd13779-cit-0033) 2013; 65
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LeRoy (10.1111/bjd.13779-BIB0032|bjd13779-cit-0032) 1988; 15
Liu (10.1111/bjd.13779-BIB0053|bjd13779-cit-0053) 2012; 165
Mishra (10.1111/bjd.13779-BIB0019|bjd13779-cit-0019) 2003; 14
Chung (10.1111/bjd.13779-BIB0052|bjd13779-cit-0052) 2013; 1833
Masui (10.1111/bjd.13779-BIB0005|bjd13779-cit-0005) 2014; 34
Masui (10.1111/bjd.13779-BIB0002|bjd13779-cit-0002) 2012; 26
Masui (10.1111/bjd.13779-BIB0003|bjd13779-cit-0003) 2013; 23
Noda (10.1111/bjd.13779-BIB0035|bjd13779-cit-0035) 2013; 305
Zhang (10.1111/bjd.13779-BIB0011|bjd13779-cit-0011) 2008; 22
Borkham-Kamphorst (10.1111/bjd.13779-BIB0013|bjd13779-cit-0013) 2011; 31
References_xml – reference: Asano Y, Stawski L, Hant F et al. Endothelial Fli1 deficiency impairs vascular homeostasis: a role in scleroderma vasculopathy. Am J Pathol 2010; 176:1983-98.
– reference: Aozasa N, Asano Y, Akamata K et al. Serum apelin levels: clinical association with vascular involvements in patients with systemic sclerosis. J Eur Acad Dermatol Venereol 2013; 27:37-42.
– reference: Feghali-Bostwick C, Medsger TA, Wright TM. Analysis of systemic sclerosis in twins reveals low concordance for disease and high concordance for the presence of antinuclear antibodies. Arthritis Rheum 2003; 48:1956-63.
– reference: Fernández CA, Yan L, Louis G et al. The matrix metalloproteinase-9/neutrophil gelatinase-associated lipocalin complex plays a role in breast tumor growth and is present in the urine of breast cancer patients. Clin Cancer Res 2005; 11:5390-5.
– reference: Liu JT, Song E, Xu A et al. Lipocalin-2 deficiency prevents endothelial dysfunction associated with dietary obesity: role of cytochrome P450 2C inhibition. Br J Pharmacol 2012; 165:520-31.
– reference: Li EM, Xu LY, Cai WJ et al. Functions of neutrophil gelatinase-associated lipocalin in the esophageal carcinoma cell line SHEEC. Sheng Wu Hua Xue Yu Sheng Wu Wu Li Xue Bao (Shanghai) 2003; 35:247-54.
– reference: Milner KL, van der Poorten D, Xu A et al. Adipocyte fatty acid binding protein levels relate to inflammation and fibrosis in nonalcoholic fatty liver disease. Hepatology 2009; 49:1926-34.
– reference: Wang Y, Lam KS, Kraegen EW et al. Lipocalin-2 is an inflammatory marker closely associated with obesity, insulin resistance, and hyperglycemia in humans. Clin Chem 2007; 53:34-41.
– reference: Yang J, Bielenberg DR, Rodig SJ et al. Lipocalin 2 promotes breast cancer progression. Proc Natl Acad Sci USA 2009; 106:3913-18.
– reference: Leng X, Ding T, Lin H et al. Inhibition of lipocalin 2 impairs breast tumorigenesis and metastasis. Cancer Res 2009; 69:8579-84.
– reference: Yan L, Borregaard N, Kjeldsen L et al. The high molecular weight urinary matrix metalloproteinase (MMP) activity is a complex of gelatinase B/MMP-9 and neutrophil gelatinase-associated lipocalin (NGAL). Modulation of MMP-9 activity by NGAL. J Biol Chem 2001; 276:37258-65.
– reference: Schermuly RT, Kreisselmeier KP, Ghofrani HA et al. Antiremodeling effects of iloprost and the dual-selective phosphodiesterase 3/4 inhibitor tolafentrine in chronic experimental pulmonary hypertension. Circ Res 2004; 94:1101-8.
– reference: Grigoryev DN, Mathai SC, Fisher MR et al. Identification of candidate genes in scleroderma-related pulmonary arterial hypertension. Transl Res 2008; 151:197-207.
– reference: Flo TH, Smith KD, Sato S et al. Lipocalin 2 mediates an innate immune response to bacterial infection by sequestrating iron. Nature 2004; 432:917-21.
– reference: Baraut J, Michel L, Verrecchia F et al. Relationship between cytokine profiles and clinical outcomes in patients with systemic sclerosis. Autoimmun Rev 2010; 10:65-73.
– reference: Noda S, Asano Y, Aozasa N et al. Clinical significance of serum soluble Tie1 levels in patients with systemic sclerosis. Arch Dermatol Res 2013; 305:325-31.
– reference: Devarajan P. Emerging biomarkers of acute kidney injury. Contrib Nephrol 2007; 156:203-12.
– reference: Roy R, Louis G, Loughlin KR et al. Tumor-specific urinary matrix metalloproteinase fingerprinting: identification of high molecular weight urinary matrix metalloproteinase species. Clin Cancer Res 2008; 14:6610-17.
– reference: Leng X, Lin H, Ding T et al. Lipocalin 2 is required for BCR-ABL-induced tumorigenesis. Oncogene 2008; 27:6110-19.
– reference: Viau A, El Karoui K, Laouari D et al. Lipocalin 2 is essential for chronic kidney disease progression in mice and humans. J Clin Invest 2010; 120:4065-76.
– reference: Kim JW, Lee SH, Jeong SH et al. Increased urinary lipocalin-2 reflects matrix metalloproteinase-9 activity in chronic hepatitis C with hepatic fibrosis. Tohoku J Exp Med 2010; 222:319-27.
– reference: Masui Y, Asano Y, Akamata K et al. Serum resistin levels: a possible correlation with pulmonary vascular involvement in patients with systemic sclerosis. Rheumatol Int 2014; 34:1165-70.
– reference: Lin CW, Tseng SW, Yang SF et al. Role of lipocalin 2 and its complex with matrix metalloproteinase-9 in oral cancer. Oral Dis 2012; 18:734-40.
– reference: Steen VD, Medsger TA Jr. Severe organ involvement in systemic sclerosis with diffuse scleroderma. Arthritis Rheum 2000; 43:2437-44.
– reference: Giannelli G, Iannone F, Marinosci F et al. The effect of bosentan on matrix metalloproteinase-9 levels in patients with systemic sclerosis-induced pulmonary hypertension. Curr Med Res Opin 2005; 21:327-32.
– reference: Asano Y, Czuwara J, Trojanowska M. Transforming growth factor-beta regulates DNA binding activity of transcription factor Fli1 by p300/CREB-binding protein-associated factor-dependent acetylation. J Biol Chem 2007; 282:34672-83.
– reference: Bauer M, Eickhoff JC, Gould MN et al. Neutrophil gelatinase-associated lipocalin (NGAL) is a predictor of poor prognosis in human primary breast cancer. Breast Cancer Res Treat 2008; 108:389-97.
– reference: Yoshizaki A, Iwata Y, Komura K et al. CD19 regulates skin and lung fibrosis via Toll-like receptor signaling in a model of bleomycin-induced scleroderma. Am J Pathol 2008; 172:1650-63.
– reference: Haase-Fielitz A, Bellomo R, Devarajan P et al. The predictive performance of plasma neutrophil gelatinase-associated lipocalin (NGAL) increases with grade of acute kidney injury. Nephrol Dial Transplant 2009; 24:3349-54.
– reference: Ichimura Y, Asano Y, Akamata K et al. Fli1 deficiency contributes to the suppression of endothelial CXCL5 expression in systemic sclerosis. Arch Dermatol Res 2014; 306:331-8.
– reference: Hanai J, Mammoto T, Seth P et al. Lipocalin 2 diminishes invasiveness and metastasis of Ras-transformed cells. J Biol Chem 2005; 280:13641-7.
– reference: Zhang J, Wu Y, Zhang Y et al. The role of lipocalin 2 in the regulation of inflammation in adipocytes and macrophages. Mol Endocrinol 2008; 22:1416-26.
– reference: LeRoy E, Black C, Fleischmajer R et al. Scleroderma (systemic sclerosis): classification, subsets and pathogenesis. J Rheumatol 1988; 15:202-5.
– reference: Toyama T, Asano Y, Takahashi T et al. Clinical significance of serum retinol binding protein-4 levels in patients with systemic sclerosis. J Eur Acad Dermatol Venereol 2013; 27:337-44.
– reference: Kjeldsen L, Johnsen AH, Sengeløv H et al. Isolation and primary structure of NGAL, a novel protein associated with human neutrophil gelatinase. J Biol Chem 1993; 268:10425-32.
– reference: Matsushita T, Hasegawa M, Hamaguchi Y et al. Longitudinal analysis of serum cytokine concentrations in systemic sclerosis: association of interleukin 12 elevation with spontaneous regression of skin sclerosis. J Rheumatol 2006; 33:275-84.
– reference: van den Hoogen F, Khanna D, Fransen J et al. 2013 classification criteria for systemic sclerosis: an American College of Rheumatology/European League against Rheumatism collaborative initiative. Ann Rheum Dis 2013; 72:1747-55.
– reference: Chung TW, Choi HJ, Kim CH et al. Lipocalin-2 elicited by advanced glycation end-products promotes the migration of vascular smooth muscle cells. Biochim Biophys Acta 2013; 1833:3386-95.
– reference: Mishra J, Ma Q, Prada A et al. Identification of neutrophil gelatinase-associated lipocalin as a novel early urinary biomarker for ischemic renal injury. J Am Soc Nephrol 2003; 14:2534-43.
– reference: Haase M, Bellomo R, Devarajan P et al. Accuracy of neutrophil gelatinase-associated lipocalin (NGAL) in diagnosis and prognosis in acute kidney injury: a systematic review and meta-analysis. Am J Kidney Dis 2009; 54:1012-24.
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Snippet Summary Background Lipocalin‐2 is an adipocytokine implicated in apoptosis, innate immunity, angiogenesis, and the development of chronic kidney disease....
Lipocalin-2 is an adipocytokine implicated in apoptosis, innate immunity, angiogenesis, and the development of chronic kidney disease. To investigate the role...
BackgroundLipocalin‐2 is an adipocytokine implicated in apoptosis, innate immunity, angiogenesis, and the development of chronic kidney disease.ObjectivesTo...
Lipocalin-2 is an adipocytokine implicated in apoptosis, innate immunity, angiogenesis, and the development of chronic kidney disease.BACKGROUNDLipocalin-2 is...
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SubjectTerms Acute-Phase Proteins - metabolism
Acute-Phase Proteins - physiology
Adult
Aged
Angiogenesis
Animals
Apoptosis
Apoptosis - physiology
Bleomycin
Blood pressure
Case-Control Studies
Endothelial cells
Female
Fibroblasts
Fibrosis
Fibrosis - etiology
Fibrosis - pathology
Fibrosis - physiopathology
Glomerular filtration rate
Glomerular Filtration Rate - physiology
Heart
Humans
Immunoblotting
Immunohistochemistry
Kidney diseases
Lipocalin
Lipocalin-2
Lipocalins - metabolism
Lipocalins - physiology
Lung diseases
Lung Diseases - etiology
Lung Diseases - physiopathology
Male
Matrix metalloproteinase
Metalloproteinase
Mice
Middle Aged
Polymerase chain reaction
Proto-Oncogene Proteins - metabolism
Proto-Oncogene Proteins - physiology
Pulmonary hypertension
Renal function
Renal Insufficiency, Chronic - etiology
RNA-directed DNA polymerase
Scleroderma
Scleroderma, Systemic - etiology
Scleroderma, Systemic - pathology
Scleroderma, Systemic - physiopathology
Sclerosis
Skin - pathology
Skin diseases
Skin Diseases, Vascular - etiology
Skin Diseases, Vascular - physiopathology
Systemic sclerosis
Vascular diseases
Vascular Diseases - etiology
Vascular Diseases - pathology
Vascular Diseases - physiopathology
Ventricle
Title A possible contribution of lipocalin-2 to the development of dermal fibrosis, pulmonary vascular involvement and renal dysfunction in systemic sclerosis
URI https://api.istex.fr/ark:/67375/WNG-PF51HHXN-K/fulltext.pdf
https://onlinelibrary.wiley.com/doi/abs/10.1111%2Fbjd.13779
https://www.ncbi.nlm.nih.gov/pubmed/25781362
https://www.proquest.com/docview/2247343050
https://www.proquest.com/docview/1716935915
Volume 173
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