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Erschienen in: Clinical Rheumatology 6/2019

12.02.2019 | Original Article

Macrophage migration inhibitory factor polymorphisms are a potential susceptibility marker in systemic sclerosis from southern Mexican population: association with MIF mRNA expression and cytokine profile

verfasst von: Christian Johana Baños-Hernández, José Eduardo Navarro-Zarza, Richard Bucala, Jorge Hernández-Bello, Isela Parra-Rojas, María Guadalupe Ramírez-Dueñas, Samuel García-Arellano, Luis Alexis Hernández-Palma, Andrea Carolina Machado-Sulbarán, José Francisco Muñoz-Valle

Erschienen in: Clinical Rheumatology | Ausgabe 6/2019

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Abstract

Introduction

Systemic sclerosis (SSc) is a complex autoimmune disease, characterized by microvascular lesions, autoimmunity, and fibrosis. It is suggested that MIF participates in the amplification of the proinflammatory process in SSc; moreover, the promoter polymorphisms − 794 CATT5–8 (rs5844572) and − 173G>C (rs755622) in the MIF gene have been associated with an increase in MIF serum levels in several autoimmune diseases. The aim of this study was to analyze the relationship of the − 794 CATT5–8 and − 173G>C MIF polymorphisms with mRNA expression, MIF serum levels, and the Th1/Th2/Th17 cytokine profile in SSc.

Materials and methods

A case-control study was carried out that included 50 patients with SSc and 100 control subjects (CS). Both polymorphisms were genotyped by PCR and PCR-RFLP. MIF levels were measured by ELISA kit. The cytokine profile and the MIF mRNA expression were quantified by BioPlex MagPix system and real-time PCR, respectively.

Results

An association between the − 794 CATT7 and − 173*C MIF alleles and the 7C haplotype with SSc susceptibility was found (p < 0.05). Also, the 7C haplotype was associated with increased MIF mRNA expression (p = 0.03) in SSc. In addition, an increase of IL-1β and IL-6 serum levels in SSc patients was found as well as a positive correlation between MIF serum levels and Th1 and Th17 cytokine profiles.

Conclusion

The MIF 7C haplotype is a susceptibility marker for SSc in the southern Mexican population and is associated with MIF mRNA expression. Moreover, there is a positive correlation between MIF serum levels and Th1 and Th17 inflammatory response in SSc.
Literatur
1.
Zurück zum Zitat Barsotti S, Stagnaro C, d'Ascanio A et al (2016) One year in review 2016: systemic sclerosis. Clin Exp Rheumatol 34 Suppl 100(5):3–13 Barsotti S, Stagnaro C, d'Ascanio A et al (2016) One year in review 2016: systemic sclerosis. Clin Exp Rheumatol 34 Suppl 100(5):3–13
2.
Zurück zum Zitat van den Hoogen F, Khanna D, Fransen J, Johnson SR, Baron M, Tyndall A, Matucci-Cerinic M, Naden RP, Medsger TA Jr, Carreira PE, Riemekasten G, Clements PJ, Denton CP, Distler O, Allanore Y, Furst DE, Gabrielli A, Mayes MD, van Laar JM, Seibold JR, Czirjak L, Steen VD, Inanc M, Kowal-Bielecka O, Müller-Ladner U, Valentini G, Veale DJ, Vonk MC, Walker UA, Chung L, Collier DH, Csuka ME, Fessler BJ, Guiducci S, Herrick A, Hsu VM, Jimenez S, Kahaleh B, Merkel PA, Sierakowski S, Silver RM, Simms RW, Varga J, Pope JE (2013) 2013 classification criteria for systemic sclerosis: an American College of Rheumatology/European league against rheumatism collaborative initiative. Arthritis Rheum 65(11):2737–2747CrossRefPubMedPubMedCentral van den Hoogen F, Khanna D, Fransen J, Johnson SR, Baron M, Tyndall A, Matucci-Cerinic M, Naden RP, Medsger TA Jr, Carreira PE, Riemekasten G, Clements PJ, Denton CP, Distler O, Allanore Y, Furst DE, Gabrielli A, Mayes MD, van Laar JM, Seibold JR, Czirjak L, Steen VD, Inanc M, Kowal-Bielecka O, Müller-Ladner U, Valentini G, Veale DJ, Vonk MC, Walker UA, Chung L, Collier DH, Csuka ME, Fessler BJ, Guiducci S, Herrick A, Hsu VM, Jimenez S, Kahaleh B, Merkel PA, Sierakowski S, Silver RM, Simms RW, Varga J, Pope JE (2013) 2013 classification criteria for systemic sclerosis: an American College of Rheumatology/European league against rheumatism collaborative initiative. Arthritis Rheum 65(11):2737–2747CrossRefPubMedPubMedCentral
3.
Zurück zum Zitat Katsumoto TR, Whitfield ML, Connolly MK (2011) The pathogenesis of systemic sclerosis. Annu Rev Pathol 6:509–537CrossRefPubMed Katsumoto TR, Whitfield ML, Connolly MK (2011) The pathogenesis of systemic sclerosis. Annu Rev Pathol 6:509–537CrossRefPubMed
4.
Zurück zum Zitat Stern EP, Denton CP (2015) The pathogenesis of systemic sclerosis. Rheum Dis Clin N Am 41(3):367–382CrossRef Stern EP, Denton CP (2015) The pathogenesis of systemic sclerosis. Rheum Dis Clin N Am 41(3):367–382CrossRef
5.
Zurück zum Zitat Selvi E, Tripodi SA, Catenaccio M, Lorenzini S, Chindamo D, Manganelli S, Romagnoli R, Ietta F, Paulesu L, Miracco C, Cintorino M, Marcolongo R (2003) Expression of macrophage migration inhibitory factor in diffuse systemic sclerosis. Ann Rheum Dis 62(5):460–464CrossRefPubMedPubMedCentral Selvi E, Tripodi SA, Catenaccio M, Lorenzini S, Chindamo D, Manganelli S, Romagnoli R, Ietta F, Paulesu L, Miracco C, Cintorino M, Marcolongo R (2003) Expression of macrophage migration inhibitory factor in diffuse systemic sclerosis. Ann Rheum Dis 62(5):460–464CrossRefPubMedPubMedCentral
8.
Zurück zum Zitat Mitchell RA, Liao H, Chesney J, Fingerle-Rowson G, Baugh J, David J, Bucala R (2002) Macrophage migration inhibitory factor (MIF) sustains macrophage proinflammatory function by inhibiting p53: regulatory role in the innate immune response. Proc Natl Acad Sci U S A 99(1):345–350CrossRefPubMed Mitchell RA, Liao H, Chesney J, Fingerle-Rowson G, Baugh J, David J, Bucala R (2002) Macrophage migration inhibitory factor (MIF) sustains macrophage proinflammatory function by inhibiting p53: regulatory role in the innate immune response. Proc Natl Acad Sci U S A 99(1):345–350CrossRefPubMed
9.
Zurück zum Zitat Kim JY, Kwok SK, Hur KH, Kim HJ, Kim NS, Yoo SA, Kim WU, Cho CS (2008) Up-regulated macrophage migration inhibitory factor protects apoptosis of dermal fibroblasts in patients with systemic sclerosis. Clin Exp Immunol 152(2):328–335CrossRefPubMedPubMedCentral Kim JY, Kwok SK, Hur KH, Kim HJ, Kim NS, Yoo SA, Kim WU, Cho CS (2008) Up-regulated macrophage migration inhibitory factor protects apoptosis of dermal fibroblasts in patients with systemic sclerosis. Clin Exp Immunol 152(2):328–335CrossRefPubMedPubMedCentral
10.
Zurück zum Zitat Llamas-Covarrubias MA, Valle Y, Bucala R, Navarro-Hernández RE, Palafox-Sánchez CA, Padilla-Gutiérrez JR, Parra-Rojas I, Bernard-Medina AG, Reyes-Castillo Z, Muñoz-Valle JF (2013) Macrophage migration inhibitory factor (MIF): genetic evidence for participation in early onset and early stage rheumatoid arthritis. Cytokine 61(3):759–765CrossRefPubMedPubMedCentral Llamas-Covarrubias MA, Valle Y, Bucala R, Navarro-Hernández RE, Palafox-Sánchez CA, Padilla-Gutiérrez JR, Parra-Rojas I, Bernard-Medina AG, Reyes-Castillo Z, Muñoz-Valle JF (2013) Macrophage migration inhibitory factor (MIF): genetic evidence for participation in early onset and early stage rheumatoid arthritis. Cytokine 61(3):759–765CrossRefPubMedPubMedCentral
11.
Zurück zum Zitat Morales-Zambrano R, Bautista-Herrera LA, De la Cruz-Mosso U et al (2014) Macrophage migration inhibitory factor (MIF) promoter polymorphisms (−794 CATT5-8 and −173 G>C): association with MIF and TNFalpha in psoriatic arthritis. Int J Clin Exp Med 7(9):2605–2614PubMedPubMedCentral Morales-Zambrano R, Bautista-Herrera LA, De la Cruz-Mosso U et al (2014) Macrophage migration inhibitory factor (MIF) promoter polymorphisms (−794 CATT5-8 and −173 G>C): association with MIF and TNFalpha in psoriatic arthritis. Int J Clin Exp Med 7(9):2605–2614PubMedPubMedCentral
12.
Zurück zum Zitat De la Cruz-Mosso U, Bucala R, Palafox-Sanchez CA et al (2014) Macrophage migration inhibitory factor: association of −794 CATT5-8 and −173 G>C polymorphisms with TNF-alpha in systemic lupus erythematosus. Hum Immunol 75(5):433–439CrossRefPubMedPubMedCentral De la Cruz-Mosso U, Bucala R, Palafox-Sanchez CA et al (2014) Macrophage migration inhibitory factor: association of −794 CATT5-8 and −173 G>C polymorphisms with TNF-alpha in systemic lupus erythematosus. Hum Immunol 75(5):433–439CrossRefPubMedPubMedCentral
13.
Zurück zum Zitat Castaneda-Moreno VA, De la Cruz-Mosso U, Torres-Carrillo N et al (2018) MIF functional polymorphisms (−794 CATT5-8 and −173 G>C) are associated with MIF serum levels, severity and progression in male multiple sclerosis from western Mexican population. J Neuroimmunol 320:117–124CrossRefPubMed Castaneda-Moreno VA, De la Cruz-Mosso U, Torres-Carrillo N et al (2018) MIF functional polymorphisms (−794 CATT5-8 and −173 G>C) are associated with MIF serum levels, severity and progression in male multiple sclerosis from western Mexican population. J Neuroimmunol 320:117–124CrossRefPubMed
14.
Zurück zum Zitat Baugh JA, Chitnis S, Donnelly SC, Monteiro J, Lin X, Plant BJ, Wolfe F, Gregersen PK, Bucala R (2002) A functional promoter polymorphism in the macrophage migration inhibitory factor (MIF) gene associated with disease severity in rheumatoid arthritis. Genes Immun 3(3):170–176CrossRefPubMed Baugh JA, Chitnis S, Donnelly SC, Monteiro J, Lin X, Plant BJ, Wolfe F, Gregersen PK, Bucala R (2002) A functional promoter polymorphism in the macrophage migration inhibitory factor (MIF) gene associated with disease severity in rheumatoid arthritis. Genes Immun 3(3):170–176CrossRefPubMed
15.
Zurück zum Zitat Yao J, Leng L, Sauler M, Fu W, Zheng J, Zhang Y, du X, Yu X, Lee P, Bucala R (2016) Transcription factor ICBP90 regulates the MIF promoter and immune susceptibility locus. J Clin Invest 126(2):732–744CrossRefPubMedPubMedCentral Yao J, Leng L, Sauler M, Fu W, Zheng J, Zhang Y, du X, Yu X, Lee P, Bucala R (2016) Transcription factor ICBP90 regulates the MIF promoter and immune susceptibility locus. J Clin Invest 126(2):732–744CrossRefPubMedPubMedCentral
16.
Zurück zum Zitat Gregersen PK, Bucala R (2003) Macrophage migration inhibitory factor, MIF alleles, and the genetics of inflammatory disorders: incorporating disease outcome into the definition of phenotype. Arthritis Rheum 48(5):1171–1176CrossRefPubMed Gregersen PK, Bucala R (2003) Macrophage migration inhibitory factor, MIF alleles, and the genetics of inflammatory disorders: incorporating disease outcome into the definition of phenotype. Arthritis Rheum 48(5):1171–1176CrossRefPubMed
17.
Zurück zum Zitat Wu SP, Leng L, Feng Z, Liu N, Zhao H, McDonald C, Lee A, Arnett FC, Gregersen PK, Mayes MD, Bucala R (2006) Macrophage migration inhibitory factor promoter polymorphisms and the clinical expression of scleroderma. Arthritis Rheum 54(11):3661–3669CrossRefPubMed Wu SP, Leng L, Feng Z, Liu N, Zhao H, McDonald C, Lee A, Arnett FC, Gregersen PK, Mayes MD, Bucala R (2006) Macrophage migration inhibitory factor promoter polymorphisms and the clinical expression of scleroderma. Arthritis Rheum 54(11):3661–3669CrossRefPubMed
18.
Zurück zum Zitat Bossini-Castillo L, Simeon CP, Beretta L, Vonk MC, Callejas-Rubio JL, Espinosa G, Carreira P, Camps MT, Rodríguez-Rodríguez L, Rodríguez-Carballeira M, García-Hernández FJ, López-Longo FJ, Hernández-Hernández V, Sáez-Comet L, Egurbide MV, Hesselstrand R, Nordin A, Hoffmann-Vold AM, Vanthuyne M, Smith V, de Langhe E, Kreuter A, Riemekasten G, Witte T, Hunzelmann N, Voskuyl AE, Schuerwegh AJ, Lunardi C, Airó P, Scorza R, Shiels P, van Laar JM, Fonseca C, Denton C, Herrick A, Worthington J, Koeleman BP, Rueda B, Radstake TRDJ, Martin J (2011) Confirmation of association of the macrophage migration inhibitory factor gene with systemic sclerosis in a large European population. Rheumatology 50(11):1976–1981CrossRefPubMed Bossini-Castillo L, Simeon CP, Beretta L, Vonk MC, Callejas-Rubio JL, Espinosa G, Carreira P, Camps MT, Rodríguez-Rodríguez L, Rodríguez-Carballeira M, García-Hernández FJ, López-Longo FJ, Hernández-Hernández V, Sáez-Comet L, Egurbide MV, Hesselstrand R, Nordin A, Hoffmann-Vold AM, Vanthuyne M, Smith V, de Langhe E, Kreuter A, Riemekasten G, Witte T, Hunzelmann N, Voskuyl AE, Schuerwegh AJ, Lunardi C, Airó P, Scorza R, Shiels P, van Laar JM, Fonseca C, Denton C, Herrick A, Worthington J, Koeleman BP, Rueda B, Radstake TRDJ, Martin J (2011) Confirmation of association of the macrophage migration inhibitory factor gene with systemic sclerosis in a large European population. Rheumatology 50(11):1976–1981CrossRefPubMed
19.
Zurück zum Zitat Becker H, Willeke P, Schotte H, Domschke W, Gaubitz M (2008) Macrophage migration inhibitory factor may contribute to vasculopathy in systemic sclerosis. Clin Rheumatol 27(10):1307–1311CrossRefPubMed Becker H, Willeke P, Schotte H, Domschke W, Gaubitz M (2008) Macrophage migration inhibitory factor may contribute to vasculopathy in systemic sclerosis. Clin Rheumatol 27(10):1307–1311CrossRefPubMed
20.
Zurück zum Zitat Ningyan G, Xu Y, Hongfei S, Jingjing C, Min C (2015) The role of macrophage migration inhibitory factor in mast cell-stimulated fibroblast proliferation and collagen production. PLoS One 10(3):e0122482CrossRefPubMedPubMedCentral Ningyan G, Xu Y, Hongfei S, Jingjing C, Min C (2015) The role of macrophage migration inhibitory factor in mast cell-stimulated fibroblast proliferation and collagen production. PLoS One 10(3):e0122482CrossRefPubMedPubMedCentral
21.
Zurück zum Zitat Miller SA, Dykes DD, Polesky HF (1988) A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 16(3):1215CrossRefPubMedPubMedCentral Miller SA, Dykes DD, Polesky HF (1988) A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 16(3):1215CrossRefPubMedPubMedCentral
22.
Zurück zum Zitat Radstake TR, Sweep FC, Welsing P et al (2005) Correlation of rheumatoid arthritis severity with the genetic functional variants and circulating levels of macrophage migration inhibitory factor. Arthritis Rheum 52(10):3020–3029CrossRefPubMed Radstake TR, Sweep FC, Welsing P et al (2005) Correlation of rheumatoid arthritis severity with the genetic functional variants and circulating levels of macrophage migration inhibitory factor. Arthritis Rheum 52(10):3020–3029CrossRefPubMed
23.
Zurück zum Zitat Makhija R, Kingsnorth A, Demaine A (2007) Gene polymorphisms of the macrophage migration inhibitory factor and acute pancreatitis. JOP 8(3):289–295PubMed Makhija R, Kingsnorth A, Demaine A (2007) Gene polymorphisms of the macrophage migration inhibitory factor and acute pancreatitis. JOP 8(3):289–295PubMed
24.
Zurück zum Zitat Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162(1):156–159CrossRefPubMed Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162(1):156–159CrossRefPubMed
25.
Zurück zum Zitat Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods 25(4):402–408CrossRefPubMed Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods 25(4):402–408CrossRefPubMed
26.
Zurück zum Zitat Shi YY, He L (2005) SHEsis, a powerful software platform for analyses of linkage disequilibrium, haplotype construction, and genetic association at polymorphism loci. Cell Res 15(2):97–98CrossRefPubMed Shi YY, He L (2005) SHEsis, a powerful software platform for analyses of linkage disequilibrium, haplotype construction, and genetic association at polymorphism loci. Cell Res 15(2):97–98CrossRefPubMed
27.
28.
Zurück zum Zitat Faul F, Erdfelder E, Buchner A, Lang AG (2009) Statistical power analyses using G*power 3.1: tests for correlation and regression analyses. Behav Res Methods 41(4):1149–1160CrossRefPubMed Faul F, Erdfelder E, Buchner A, Lang AG (2009) Statistical power analyses using G*power 3.1: tests for correlation and regression analyses. Behav Res Methods 41(4):1149–1160CrossRefPubMed
29.
Zurück zum Zitat Purcell S, Cherny SS, Sham PC (2003) Genetic power calculator: design of linkage and association genetic mapping studies of complex traits. Bioinformatics 19(1):149–150CrossRefPubMed Purcell S, Cherny SS, Sham PC (2003) Genetic power calculator: design of linkage and association genetic mapping studies of complex traits. Bioinformatics 19(1):149–150CrossRefPubMed
30.
Zurück zum Zitat Mayes MD, Bossini-Castillo L, Gorlova O, Martin JE, Zhou X, Chen WV, Assassi S, Ying J, Tan FK, Arnett FC, Reveille JD, Guerra S, Teruel M, Carmona FD, Gregersen PK, Lee AT, López-Isac E, Ochoa E, Carreira P, Simeón CP, Castellví I, González-Gay MÁ, Zhernakova A, Padyukov L, Alarcón-Riquelme M, Wijmenga C, Brown M, Beretta L, Riemekasten G, Witte T, Hunzelmann N, Kreuter A, Distler JHW, Voskuyl AE, Schuerwegh AJ, Hesselstrand R, Nordin A, Airó P, Lunardi C, Shiels P, van Laar JM, Herrick A, Worthington J, Denton C, Wigley FM, Hummers LK, Varga J, Hinchcliff ME, Baron M, Hudson M, Pope JE, Furst DE, Khanna D, Phillips K, Schiopu E, Segal BM, Molitor JA, Silver RM, Steen VD, Simms RW, Lafyatis RA, Fessler BJ, Frech TM, AlKassab F, Docherty P, Kaminska E, Khalidi N, Jones HN, Markland J, Robinson D, Broen J, Radstake TRDJ, Fonseca C, Koeleman BP, Martin J, Ortego-Centeno N, Ríos R, Callejas JL, Navarrete N, García Portales R, Camps MT, Fernández-Nebro A, González-Escribano MF, Sánchez-Román J, García-Hernández FJ, Castillo MJ, Aguirre MÁ, Gómez-Gracia I, Fernández-Gutiérrez B, Rodríguez-Rodríguez L, Vicente E, Andreu JL, Fernández de Castro M, García de la Peña P, López-Longo FJ, Martínez L, Fonollosa V, Espinosa G, Tolosa C, Pros A, Rodríguez Carballeira M, Narváez FJ, Rubio Rivas M, Ortiz Santamaría V, Díaz B, Trapiella L, Freire MC, Sousa A, Egurbide MV, Fanlo Mateo P, Sáez-Comet L, Díaz F, Hernández V, Beltrán E, Román-Ivorra JA, Grau E, Alegre Sancho JJ, Blanco García FJ, Oreiro N, Fernández Sueiro L (2014) Immunochip analysis identifies multiple susceptibility loci for systemic sclerosis. Am J Hum Genet 94(1):47–61CrossRefPubMedPubMedCentral Mayes MD, Bossini-Castillo L, Gorlova O, Martin JE, Zhou X, Chen WV, Assassi S, Ying J, Tan FK, Arnett FC, Reveille JD, Guerra S, Teruel M, Carmona FD, Gregersen PK, Lee AT, López-Isac E, Ochoa E, Carreira P, Simeón CP, Castellví I, González-Gay MÁ, Zhernakova A, Padyukov L, Alarcón-Riquelme M, Wijmenga C, Brown M, Beretta L, Riemekasten G, Witte T, Hunzelmann N, Kreuter A, Distler JHW, Voskuyl AE, Schuerwegh AJ, Hesselstrand R, Nordin A, Airó P, Lunardi C, Shiels P, van Laar JM, Herrick A, Worthington J, Denton C, Wigley FM, Hummers LK, Varga J, Hinchcliff ME, Baron M, Hudson M, Pope JE, Furst DE, Khanna D, Phillips K, Schiopu E, Segal BM, Molitor JA, Silver RM, Steen VD, Simms RW, Lafyatis RA, Fessler BJ, Frech TM, AlKassab F, Docherty P, Kaminska E, Khalidi N, Jones HN, Markland J, Robinson D, Broen J, Radstake TRDJ, Fonseca C, Koeleman BP, Martin J, Ortego-Centeno N, Ríos R, Callejas JL, Navarrete N, García Portales R, Camps MT, Fernández-Nebro A, González-Escribano MF, Sánchez-Román J, García-Hernández FJ, Castillo MJ, Aguirre MÁ, Gómez-Gracia I, Fernández-Gutiérrez B, Rodríguez-Rodríguez L, Vicente E, Andreu JL, Fernández de Castro M, García de la Peña P, López-Longo FJ, Martínez L, Fonollosa V, Espinosa G, Tolosa C, Pros A, Rodríguez Carballeira M, Narváez FJ, Rubio Rivas M, Ortiz Santamaría V, Díaz B, Trapiella L, Freire MC, Sousa A, Egurbide MV, Fanlo Mateo P, Sáez-Comet L, Díaz F, Hernández V, Beltrán E, Román-Ivorra JA, Grau E, Alegre Sancho JJ, Blanco García FJ, Oreiro N, Fernández Sueiro L (2014) Immunochip analysis identifies multiple susceptibility loci for systemic sclerosis. Am J Hum Genet 94(1):47–61CrossRefPubMedPubMedCentral
31.
Zurück zum Zitat Sreih A, Ezzeddine R, Leng L, LaChance A, Yu G, Mizue Y, Subrahmanyan L, Pons-Estel BA, Abelson AK, Gunnarsson I, Svenungsson E, Cavett J, Glenn S, Zhang L, Montgomery R, Perl A, Salmon J, Alarcón-Riquelme ME, Harley JB, Bucala R (2011) Dual effect of the macrophage migration inhibitory factor gene on the development and severity of human systemic lupus erythematosus. Arthritis Rheum 63(12):3942–3951CrossRefPubMedPubMedCentral Sreih A, Ezzeddine R, Leng L, LaChance A, Yu G, Mizue Y, Subrahmanyan L, Pons-Estel BA, Abelson AK, Gunnarsson I, Svenungsson E, Cavett J, Glenn S, Zhang L, Montgomery R, Perl A, Salmon J, Alarcón-Riquelme ME, Harley JB, Bucala R (2011) Dual effect of the macrophage migration inhibitory factor gene on the development and severity of human systemic lupus erythematosus. Arthritis Rheum 63(12):3942–3951CrossRefPubMedPubMedCentral
32.
Zurück zum Zitat Norton BJ, Strube MJ (2001) Understanding statistical power. J Orthop Sports Phys Ther 31(6):307–315CrossRefPubMed Norton BJ, Strube MJ (2001) Understanding statistical power. J Orthop Sports Phys Ther 31(6):307–315CrossRefPubMed
33.
Zurück zum Zitat Button KS, Ioannidis JP, Mokrysz C et al (2013) Power failure: why small sample size undermines the reliability of neuroscience. Nat Rev Neurosci 14(5):365–376CrossRefPubMed Button KS, Ioannidis JP, Mokrysz C et al (2013) Power failure: why small sample size undermines the reliability of neuroscience. Nat Rev Neurosci 14(5):365–376CrossRefPubMed
34.
Zurück zum Zitat Bryc K, Durand EY, Macpherson JM, Reich D, Mountain JL (2015) The genetic ancestry of African Americans, Latinos, and European Americans across the United States. Am J Hum Genet 96(1):37–53CrossRefPubMedPubMedCentral Bryc K, Durand EY, Macpherson JM, Reich D, Mountain JL (2015) The genetic ancestry of African Americans, Latinos, and European Americans across the United States. Am J Hum Genet 96(1):37–53CrossRefPubMedPubMedCentral
35.
Zurück zum Zitat Roy-Gagnon MH, Moreau C, Bherer C, St-Onge P, Sinnett D, Laprise C, Vézina H, Labuda D (2011) Genomic and genealogical investigation of the French Canadian founder population structure. Hum Genet 129(5):521–531CrossRefPubMed Roy-Gagnon MH, Moreau C, Bherer C, St-Onge P, Sinnett D, Laprise C, Vézina H, Labuda D (2011) Genomic and genealogical investigation of the French Canadian founder population structure. Hum Genet 129(5):521–531CrossRefPubMed
36.
Zurück zum Zitat Martinez-Cortes G, Salazar-Flores J, Fernandez-Rodriguez LG et al (2012) Admixture and population structure in Mexican-mestizos based on paternal lineages. J Hum Genet 57(9):568–574CrossRefPubMed Martinez-Cortes G, Salazar-Flores J, Fernandez-Rodriguez LG et al (2012) Admixture and population structure in Mexican-mestizos based on paternal lineages. J Hum Genet 57(9):568–574CrossRefPubMed
37.
Zurück zum Zitat Corallo C, Paulesu L, Cutolo M, Ietta F, Carotenuto C, Mannelli C, Romagnoli R, Nuti R, Giordano N (2015) Serum levels, tissue expression and cellular secretion of macrophage migration inhibitory factor in limited and diffuse systemic sclerosis. Clin Exp Rheumatol 33(4 Suppl 91):S98–S105PubMed Corallo C, Paulesu L, Cutolo M, Ietta F, Carotenuto C, Mannelli C, Romagnoli R, Nuti R, Giordano N (2015) Serum levels, tissue expression and cellular secretion of macrophage migration inhibitory factor in limited and diffuse systemic sclerosis. Clin Exp Rheumatol 33(4 Suppl 91):S98–S105PubMed
38.
Zurück zum Zitat Karres I, Kremer JP, Dietl I et al (1998) Chloroquine inhibits proinflammatory cytokine release into human whole blood. Am J Phys 274(4 Pt 2):R1058–R1064 Karres I, Kremer JP, Dietl I et al (1998) Chloroquine inhibits proinflammatory cytokine release into human whole blood. Am J Phys 274(4 Pt 2):R1058–R1064
39.
Zurück zum Zitat Church TS, Willis MS, Priest EL, LaMonte MJ, Earnest CP, Wilkinson WJ, Wilson DA, Giroir BP (2005) Obesity, macrophage migration inhibitory factor, and weight loss. Int J Obes 29(6):675–681CrossRef Church TS, Willis MS, Priest EL, LaMonte MJ, Earnest CP, Wilkinson WJ, Wilson DA, Giroir BP (2005) Obesity, macrophage migration inhibitory factor, and weight loss. Int J Obes 29(6):675–681CrossRef
40.
41.
Zurück zum Zitat Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW Jr (2003) Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112(12):1796–1808CrossRefPubMedPubMedCentral Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW Jr (2003) Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112(12):1796–1808CrossRefPubMedPubMedCentral
42.
Zurück zum Zitat Xu H, Barnes GT, Yang Q, Tan G, Yang D, Chou CJ, Sole J, Nichols A, Ross JS, Tartaglia LA, Chen H (2003) Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 112(12):1821–1830CrossRefPubMedPubMedCentral Xu H, Barnes GT, Yang Q, Tan G, Yang D, Chou CJ, Sole J, Nichols A, Ross JS, Tartaglia LA, Chen H (2003) Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 112(12):1821–1830CrossRefPubMedPubMedCentral
43.
Zurück zum Zitat Dandona P, Aljada A, Ghanim H, Mohanty P, Tripathy C, Hofmeyer D, Chaudhuri A (2004) Increased plasma concentration of macrophage migration inhibitory factor (MIF) and MIF mRNA in mononuclear cells in the obese and the suppressive action of metformin. J Clin Endocrinol Metab 89(10):5043–5047CrossRefPubMed Dandona P, Aljada A, Ghanim H, Mohanty P, Tripathy C, Hofmeyer D, Chaudhuri A (2004) Increased plasma concentration of macrophage migration inhibitory factor (MIF) and MIF mRNA in mononuclear cells in the obese and the suppressive action of metformin. J Clin Endocrinol Metab 89(10):5043–5047CrossRefPubMed
44.
Zurück zum Zitat Calandra T, Bernhagen J, Metz CN, Spiegel LA, Bacher M, Donnelly T, Cerami A, Bucala R (1995) MIF as a glucocorticoid-induced modulator of cytokine production. Nature 377(6544):68–71CrossRefPubMed Calandra T, Bernhagen J, Metz CN, Spiegel LA, Bacher M, Donnelly T, Cerami A, Bucala R (1995) MIF as a glucocorticoid-induced modulator of cytokine production. Nature 377(6544):68–71CrossRefPubMed
45.
Zurück zum Zitat Kamchybekov U, Figulla HR, Gerdes N, Jung C (2012) Macrophage migration inhibitory factor is elevated in obese adolescents. Arch Physiol Biochem 118(4):204–209CrossRefPubMed Kamchybekov U, Figulla HR, Gerdes N, Jung C (2012) Macrophage migration inhibitory factor is elevated in obese adolescents. Arch Physiol Biochem 118(4):204–209CrossRefPubMed
46.
Zurück zum Zitat Llamas-Covarrubias MA, Valle Y, Navarro-Hernandez RE et al (2012) Serum levels of macrophage migration inhibitory factor are associated with rheumatoid arthritis course. Rheumatol Int 32(8):2307–2311CrossRefPubMed Llamas-Covarrubias MA, Valle Y, Navarro-Hernandez RE et al (2012) Serum levels of macrophage migration inhibitory factor are associated with rheumatoid arthritis course. Rheumatol Int 32(8):2307–2311CrossRefPubMed
47.
Zurück zum Zitat Roger T, David J, Glauser MP, Calandra T (2001) MIF regulates innate immune responses through modulation of toll-like receptor 4. Nature 414(6866):920–924CrossRefPubMed Roger T, David J, Glauser MP, Calandra T (2001) MIF regulates innate immune responses through modulation of toll-like receptor 4. Nature 414(6866):920–924CrossRefPubMed
48.
Zurück zum Zitat Hong Z, Jiang Z, Liangxi W, Guofu D, Ping L, Yongling L, Wendong P, Minghai W (2004) Chloroquine protects mice from challenge with CpG ODN and LPS by decreasing proinflammatory cytokine release. Int Immunopharmacol 4(2):223–234CrossRefPubMed Hong Z, Jiang Z, Liangxi W, Guofu D, Ping L, Yongling L, Wendong P, Minghai W (2004) Chloroquine protects mice from challenge with CpG ODN and LPS by decreasing proinflammatory cytokine release. Int Immunopharmacol 4(2):223–234CrossRefPubMed
49.
Zurück zum Zitat Meloni F, Solari N, Cavagna L et al (2009) Frequency of Th1, Th2 and Th17 producing T lymphocytes in bronchoalveolar lavage of patients with systemic sclerosis. Clin Exp Rheumatol 27(5):765–772PubMed Meloni F, Solari N, Cavagna L et al (2009) Frequency of Th1, Th2 and Th17 producing T lymphocytes in bronchoalveolar lavage of patients with systemic sclerosis. Clin Exp Rheumatol 27(5):765–772PubMed
50.
Zurück zum Zitat Yoshizaki A, Yanaba K, Iwata Y, Komura K, Ogawa A, Akiyama Y, Muroi E, Hara T, Ogawa F, Takenaka M, Shimizu K, Hasegawa M, Fujimoto M, Tedder TF, Sato S (2010) Cell adhesion molecules regulate fibrotic process via Th1/Th2/Th17 cell balance in a bleomycin-induced scleroderma model. J Immunol 185(4):2502–2515CrossRefPubMed Yoshizaki A, Yanaba K, Iwata Y, Komura K, Ogawa A, Akiyama Y, Muroi E, Hara T, Ogawa F, Takenaka M, Shimizu K, Hasegawa M, Fujimoto M, Tedder TF, Sato S (2010) Cell adhesion molecules regulate fibrotic process via Th1/Th2/Th17 cell balance in a bleomycin-induced scleroderma model. J Immunol 185(4):2502–2515CrossRefPubMed
51.
Zurück zum Zitat Rodriguez-Reyna TS, Furuzawa-Carballeda J, Cabiedes J et al (2012) Th17 peripheral cells are increased in diffuse cutaneous systemic sclerosis compared with limited illness: a cross-sectional study. Rheumatol Int 32(9):2653–2660CrossRefPubMed Rodriguez-Reyna TS, Furuzawa-Carballeda J, Cabiedes J et al (2012) Th17 peripheral cells are increased in diffuse cutaneous systemic sclerosis compared with limited illness: a cross-sectional study. Rheumatol Int 32(9):2653–2660CrossRefPubMed
52.
Zurück zum Zitat O'Reilly S, Hugle T, van Laar JM (2012) T cells in systemic sclerosis: a reappraisal. Rheumatology 51(9):1540–1549CrossRefPubMed O'Reilly S, Hugle T, van Laar JM (2012) T cells in systemic sclerosis: a reappraisal. Rheumatology 51(9):1540–1549CrossRefPubMed
53.
Zurück zum Zitat Rolla G, Fusaro E, Nicola S, Bucca C, Peroni C, Parisi S, Cassinis MC, Ferraris A, Angelino F, Heffler E, Boita M, Brussino L (2016) Th-17 cytokines and interstitial lung involvement in systemic sclerosis. J Breath Res 10(4):046013CrossRefPubMed Rolla G, Fusaro E, Nicola S, Bucca C, Peroni C, Parisi S, Cassinis MC, Ferraris A, Angelino F, Heffler E, Boita M, Brussino L (2016) Th-17 cytokines and interstitial lung involvement in systemic sclerosis. J Breath Res 10(4):046013CrossRefPubMed
54.
Zurück zum Zitat Schmid AS, Hemmerle T, Pretto F, Kipar A, Neri D (2018) Antibody-based targeted delivery of interleukin-4 synergizes with dexamethasone for the reduction of inflammation in arthritis. Rheumatology 57(4):748–755CrossRefPubMed Schmid AS, Hemmerle T, Pretto F, Kipar A, Neri D (2018) Antibody-based targeted delivery of interleukin-4 synergizes with dexamethasone for the reduction of inflammation in arthritis. Rheumatology 57(4):748–755CrossRefPubMed
55.
Zurück zum Zitat Bautista-Herrera LA, De la Cruz-Mosso U, Morales-Zambrano R et al (2018) Expression of MIF and TNFA in psoriatic arthritis: relationship with Th1/Th2/Th17 cytokine profiles and clinical variables. Clin Exp Med 18(2):229–235CrossRefPubMed Bautista-Herrera LA, De la Cruz-Mosso U, Morales-Zambrano R et al (2018) Expression of MIF and TNFA in psoriatic arthritis: relationship with Th1/Th2/Th17 cytokine profiles and clinical variables. Clin Exp Med 18(2):229–235CrossRefPubMed
56.
Zurück zum Zitat De la Cruz-Mosso U, Garcia-Iglesias T, Bucala R et al (2018) MIF promotes a differential Th1/Th2/Th17 inflammatory response in human primary cell cultures: predominance of Th17 cytokine profile in PBMC from healthy subjects and increase of IL-6 and TNF-alpha in PBMC from active SLE patients. Cell Immunol 324:42–49CrossRefPubMed De la Cruz-Mosso U, Garcia-Iglesias T, Bucala R et al (2018) MIF promotes a differential Th1/Th2/Th17 inflammatory response in human primary cell cultures: predominance of Th17 cytokine profile in PBMC from healthy subjects and increase of IL-6 and TNF-alpha in PBMC from active SLE patients. Cell Immunol 324:42–49CrossRefPubMed
Metadaten
Titel
Macrophage migration inhibitory factor polymorphisms are a potential susceptibility marker in systemic sclerosis from southern Mexican population: association with MIF mRNA expression and cytokine profile
verfasst von
Christian Johana Baños-Hernández
José Eduardo Navarro-Zarza
Richard Bucala
Jorge Hernández-Bello
Isela Parra-Rojas
María Guadalupe Ramírez-Dueñas
Samuel García-Arellano
Luis Alexis Hernández-Palma
Andrea Carolina Machado-Sulbarán
José Francisco Muñoz-Valle
Publikationsdatum
12.02.2019
Verlag
Springer London
Erschienen in
Clinical Rheumatology / Ausgabe 6/2019
Print ISSN: 0770-3198
Elektronische ISSN: 1434-9949
DOI
https://doi.org/10.1007/s10067-019-04459-8

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