Dual effect of the macrophage migration inhibitory factor gene on the development and severity of human systemic lupus erythematosus
Objective To study the effect of the innate cytokine macrophage migration inhibitory factor (MIF) on the susceptibility and severity of systemic lupus erythematosus (SLE) in a multinational population of 1,369 Caucasian and African American patients. Methods Two functional polymorphisms in the MIF g...
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| Published in | Arthritis & rheumatology (Hoboken, N.J.) Vol. 63; no. 12; pp. 3942 - 3951 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Hoboken
Wiley Subscription Services, Inc., A Wiley Company
01.12.2011
Wiley Wiley Subscription Services, Inc |
| Subjects | |
| Online Access | Get full text |
| ISSN | 0004-3591 2326-5191 1529-0131 1529-0131 2326-5205 |
| DOI | 10.1002/art.30624 |
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| Abstract | Objective
To study the effect of the innate cytokine macrophage migration inhibitory factor (MIF) on the susceptibility and severity of systemic lupus erythematosus (SLE) in a multinational population of 1,369 Caucasian and African American patients.
Methods
Two functional polymorphisms in the MIF gene, a −794 CATT5–8 microsatellite repeat (rs5844572) and a −173 G/C single‐nucleotide polymorphism (rs755622), were assessed for association with SLE in 3,195 patients and healthy controls. We also measured MIF plasma levels in relation to genotypes and clinical phenotypes, and assessed Toll‐like receptor 7 (TLR‐7)–stimulated MIF production in vitro.
Results
Both Caucasians and African Americans with the high‐expression MIF haplotype −794 CATT7/−173*C had a lower incidence of SLE (in Caucasians, odds ratio [OR] 0.63, 95% confidence interval [95% CI] 0.53–0.89, P = 0.001; in African Americans, OR 0.46, 95% CI 0.23–0.95, P = 0.012). In contrast, among patients with established SLE, reduced frequencies of low‐expression MIF genotypes (−794 CATT5) were observed in those with nephritis, those with serositis, and those with central nervous system (CNS) involvement when compared to patients without end‐organ involvement (P = 0.023, P = 0.005, and P = 0.04, respectively). Plasma MIF levels and TLR‐7–stimulated MIF production in vitro reflected the underlying MIF genotype of the studied groups.
Conclusion
These findings suggest that MIF, which has both proinflammatory properties and macrophage and B cell survival functions, exerts a dual influence on the immunopathogenesis of SLE. High‐expression MIF genotypes are associated with a reduced susceptibility to SLE and may contribute to an enhanced clearance of infectious pathogens. Once SLE develops, however, low‐expression MIF genotypes may protect from ensuing inflammatory end‐organ damage. |
|---|---|
| AbstractList | To study the effect of the innate cytokine macrophage migration inhibitory factor (MIF) on the susceptibility and severity of systemic lupus erythematosus (SLE) in a multinational population of 1,369 Caucasian and African American patients.OBJECTIVETo study the effect of the innate cytokine macrophage migration inhibitory factor (MIF) on the susceptibility and severity of systemic lupus erythematosus (SLE) in a multinational population of 1,369 Caucasian and African American patients.Two functional polymorphisms in the MIF gene, a -794 CATT(5-8) microsatellite repeat (rs5844572) and a -173 G/C single-nucleotide polymorphism (rs755622), were assessed for association with SLE in 3,195 patients and healthy controls. We also measured MIF plasma levels in relation to genotypes and clinical phenotypes, and assessed Toll-like receptor 7 (TLR-7)-stimulated MIF production in vitro.METHODSTwo functional polymorphisms in the MIF gene, a -794 CATT(5-8) microsatellite repeat (rs5844572) and a -173 G/C single-nucleotide polymorphism (rs755622), were assessed for association with SLE in 3,195 patients and healthy controls. We also measured MIF plasma levels in relation to genotypes and clinical phenotypes, and assessed Toll-like receptor 7 (TLR-7)-stimulated MIF production in vitro.Both Caucasians and African Americans with the high-expression MIF haplotype -794 CATT(7)/-173*C had a lower incidence of SLE (in Caucasians, odds ratio [OR] 0.63, 95% confidence interval [95% CI] 0.53-0.89, P = 0.001; in African Americans, OR 0.46, 95% CI 0.23-0.95, P = 0.012). In contrast, among patients with established SLE, reduced frequencies of low-expression MIF genotypes (-794 CATT(5)) were observed in those with nephritis, those with serositis, and those with central nervous system (CNS) involvement when compared to patients without end-organ involvement (P = 0.023, P = 0.005, and P = 0.04, respectively). Plasma MIF levels and TLR-7-stimulated MIF production in vitro reflected the underlying MIF genotype of the studied groups.RESULTSBoth Caucasians and African Americans with the high-expression MIF haplotype -794 CATT(7)/-173*C had a lower incidence of SLE (in Caucasians, odds ratio [OR] 0.63, 95% confidence interval [95% CI] 0.53-0.89, P = 0.001; in African Americans, OR 0.46, 95% CI 0.23-0.95, P = 0.012). In contrast, among patients with established SLE, reduced frequencies of low-expression MIF genotypes (-794 CATT(5)) were observed in those with nephritis, those with serositis, and those with central nervous system (CNS) involvement when compared to patients without end-organ involvement (P = 0.023, P = 0.005, and P = 0.04, respectively). Plasma MIF levels and TLR-7-stimulated MIF production in vitro reflected the underlying MIF genotype of the studied groups.These findings suggest that MIF, which has both proinflammatory properties and macrophage and B cell survival functions, exerts a dual influence on the immunopathogenesis of SLE. High-expression MIF genotypes are associated with a reduced susceptibility to SLE and may contribute to an enhanced clearance of infectious pathogens. Once SLE develops, however, low-expression MIF genotypes may protect from ensuing inflammatory end-organ damage.CONCLUSIONThese findings suggest that MIF, which has both proinflammatory properties and macrophage and B cell survival functions, exerts a dual influence on the immunopathogenesis of SLE. High-expression MIF genotypes are associated with a reduced susceptibility to SLE and may contribute to an enhanced clearance of infectious pathogens. Once SLE develops, however, low-expression MIF genotypes may protect from ensuing inflammatory end-organ damage. Objective To study the effect of the innate cytokine macrophage migration inhibitory factor (MIF) on the susceptibility and severity of systemic lupus erythematosus (SLE) in a multinational population of 1,369 Caucasian and African American patients. Methods. Two functional polymorphisms in the MIF gene, a -794 CATT5-8 microsatellite repeat (rs5844572) and a -173 G/C single-nucleotide polymorphism (rs755622), were assessed for association with SLE in 3,195 patients and healthy controls. We also measured MIF plasma levels in relation to genotypes and clinical phenotypes, and assessed Toll-like receptor 7 (TLR-7)-stimulated MIF production in vitro. Results. Both Caucasians and African Americans with the high-expression MIF haplotype -794 CATT(7)/ -173* C had a lower incidence of SLE (in Caucasians, odds ratio [OR] 0.63, 95% confidence interval [95% CI] 0.53-0.89, P = 0.001; in African Americans, OR 0.46, 95% CI 0.23-0.95, P = 0.012). In contrast, among patients with established SLE, reduced frequencies of low-expression MIF genotypes (-794 CATT(5)) were observed in those with nephritis, those with serositis, and those with central nervous system (CNS) involvement when compared to patients without end-organ involvement (P = 0.023, P = 0.005, and P = 0.04, respectively). Plasma MIF levels and TLR-7-stimulated MIF production in vitro reflected the underlying MIF genotype of the studied groups. Conclusion. These findings suggest that MIF, which has both proinflammatory properties and macrophage and B cell survival functions, exerts a dual influence on the immunopathogenesis of SLE. Highexpression MIF genotypes are associated with a reduced susceptibility to SLE and may contribute to an enhanced clearance of infectious pathogens. Once SLE develops, however, low-expression MIF genotypes may protect from ensuing inflammatory end-organ damage. To study the effect of the innate cytokine macrophage migration inhibitory factor (MIF) on the susceptibility and severity of systemic lupus erythematosus (SLE) in a multinational population of 1,369 Caucasian and African American patients. Two functional polymorphisms in the MIF gene, a -794 CATT(5-8) microsatellite repeat (rs5844572) and a -173 G/C single-nucleotide polymorphism (rs755622), were assessed for association with SLE in 3,195 patients and healthy controls. We also measured MIF plasma levels in relation to genotypes and clinical phenotypes, and assessed Toll-like receptor 7 (TLR-7)-stimulated MIF production in vitro. Both Caucasians and African Americans with the high-expression MIF haplotype -794 CATT(7)/-173*C had a lower incidence of SLE (in Caucasians, odds ratio [OR] 0.63, 95% confidence interval [95% CI] 0.53-0.89, P = 0.001; in African Americans, OR 0.46, 95% CI 0.23-0.95, P = 0.012). In contrast, among patients with established SLE, reduced frequencies of low-expression MIF genotypes (-794 CATT(5)) were observed in those with nephritis, those with serositis, and those with central nervous system (CNS) involvement when compared to patients without end-organ involvement (P = 0.023, P = 0.005, and P = 0.04, respectively). Plasma MIF levels and TLR-7-stimulated MIF production in vitro reflected the underlying MIF genotype of the studied groups. These findings suggest that MIF, which has both proinflammatory properties and macrophage and B cell survival functions, exerts a dual influence on the immunopathogenesis of SLE. High-expression MIF genotypes are associated with a reduced susceptibility to SLE and may contribute to an enhanced clearance of infectious pathogens. Once SLE develops, however, low-expression MIF genotypes may protect from ensuing inflammatory end-organ damage. Objective To study the effect of the innate cytokine macrophage migration inhibitory factor (MIF) on the susceptibility and severity of systemic lupus erythematosus (SLE) in a multinational population of 1,369 Caucasian and African American patients. Methods Two functional polymorphisms in the MIF gene, a −794 CATT5–8 microsatellite repeat (rs5844572) and a −173 G/C single‐nucleotide polymorphism (rs755622), were assessed for association with SLE in 3,195 patients and healthy controls. We also measured MIF plasma levels in relation to genotypes and clinical phenotypes, and assessed Toll‐like receptor 7 (TLR‐7)–stimulated MIF production in vitro. Results Both Caucasians and African Americans with the high‐expression MIF haplotype −794 CATT7/−173*C had a lower incidence of SLE (in Caucasians, odds ratio [OR] 0.63, 95% confidence interval [95% CI] 0.53–0.89, P = 0.001; in African Americans, OR 0.46, 95% CI 0.23–0.95, P = 0.012). In contrast, among patients with established SLE, reduced frequencies of low‐expression MIF genotypes (−794 CATT5) were observed in those with nephritis, those with serositis, and those with central nervous system (CNS) involvement when compared to patients without end‐organ involvement (P = 0.023, P = 0.005, and P = 0.04, respectively). Plasma MIF levels and TLR‐7–stimulated MIF production in vitro reflected the underlying MIF genotype of the studied groups. Conclusion These findings suggest that MIF, which has both proinflammatory properties and macrophage and B cell survival functions, exerts a dual influence on the immunopathogenesis of SLE. High‐expression MIF genotypes are associated with a reduced susceptibility to SLE and may contribute to an enhanced clearance of infectious pathogens. Once SLE develops, however, low‐expression MIF genotypes may protect from ensuing inflammatory end‐organ damage. Objective To study the effect of the innate cytokine macrophage migration inhibitory factor (MIF) on the susceptibility and severity of systemic lupus erythematosus (SLE) in a multinational population of 1,369 Caucasian and African American patients. Methods Two functional polymorphisms in the MIF gene, a -794 CATT5-8 microsatellite repeat (rs5844572) and a -173 G/C single-nucleotide polymorphism (rs755622), were assessed for association with SLE in 3,195 patients and healthy controls. We also measured MIF plasma levels in relation to genotypes and clinical phenotypes, and assessed Toll-like receptor 7 (TLR-7)-stimulated MIF production in vitro. Results Both Caucasians and African Americans with the high-expression MIF haplotype -794 CATT7/-173*C had a lower incidence of SLE (in Caucasians, odds ratio [OR] 0.63, 95% confidence interval [95% CI] 0.53-0.89, P = 0.001; in African Americans, OR 0.46, 95% CI 0.23-0.95, P = 0.012). In contrast, among patients with established SLE, reduced frequencies of low-expression MIF genotypes (-794 CATT5) were observed in those with nephritis, those with serositis, and those with central nervous system (CNS) involvement when compared to patients without end-organ involvement (P = 0.023, P = 0.005, and P = 0.04, respectively). Plasma MIF levels and TLR-7-stimulated MIF production in vitro reflected the underlying MIF genotype of the studied groups. Conclusion These findings suggest that MIF, which has both proinflammatory properties and macrophage and B cell survival functions, exerts a dual influence on the immunopathogenesis of SLE. High-expression MIF genotypes are associated with a reduced susceptibility to SLE and may contribute to an enhanced clearance of infectious pathogens. Once SLE develops, however, low-expression MIF genotypes may protect from ensuing inflammatory end-organ damage. [PUBLICATION ABSTRACT] |
| Author | Harley, John B. Pons‐Estel, Bernardo A. Abelson, Anna‐Karin Perl, Andras Alarcón‐Riquelme, Marta E. LaChance, Avery Subrahmanyan, Lakshman Cavett, Joshua Zhang, Lin Bucala, Richard Svenungsson, Elisabet Yu, Geraldine Mizue, Yuka Glenn, Stuart Montgomery, Ruth Salmon, Jane Sreih, Antoine Ezzeddine, Rana Gunnarsson, Iva Leng, Lin |
| AuthorAffiliation | 6 Arthritis and Clinical Immunology, Oklahoma Medical Research Foundation, 825 NE 13th St., MS #24 Oklahoma City, OK 73104 9 Center for Genomics and Oncological Research Pfizer-University of Granada.Junta de Andalucia, Avd de la Ilustración 114, 18007, Granada, Spain 8 Department of Medicine, Section of Rheumatology, Hospital for Special Surgery, 535 East 70th Street, New York, NY 10021 4 Department of Genetics and Pathology, Uppsala University, Dag Hammarskjölds väg 20, 751 85, Uppsala, Sweden 10 Department of Medicine, Section of Rheumatology, Cincinnati Children’s Hospital Medical Center. 3333 Burnet Ave, Cincinnati, OH 45229 5 Rheumatology unit, Department of Medicine, Karolinska Institutet, Stockholm, Sweden 2 Bristol-Myers-Squibb, Wallingford, CT 06492 3 Sanatorio Parque, Avenida Del Huerto 1375 P24, Rosario, Argentina 7 Department of Medicine, Section of Rheumatology, Upstate Medical University, 750 E Adams St Syracuse, NY 13210 1 Department of Medicine, Sections of Rheumatology and Card |
| AuthorAffiliation_xml | – name: 7 Department of Medicine, Section of Rheumatology, Upstate Medical University, 750 E Adams St Syracuse, NY 13210 – name: 8 Department of Medicine, Section of Rheumatology, Hospital for Special Surgery, 535 East 70th Street, New York, NY 10021 – name: 4 Department of Genetics and Pathology, Uppsala University, Dag Hammarskjölds väg 20, 751 85, Uppsala, Sweden – name: 6 Arthritis and Clinical Immunology, Oklahoma Medical Research Foundation, 825 NE 13th St., MS #24 Oklahoma City, OK 73104 – name: 2 Bristol-Myers-Squibb, Wallingford, CT 06492 – name: 10 Department of Medicine, Section of Rheumatology, Cincinnati Children’s Hospital Medical Center. 3333 Burnet Ave, Cincinnati, OH 45229 – name: 1 Department of Medicine, Sections of Rheumatology and Cardiology, Yale University School of Medicine, 300 Cedar St., New Haven, CT 06520 – name: 3 Sanatorio Parque, Avenida Del Huerto 1375 P24, Rosario, Argentina – name: 11 Department of Medicine, Section of Rheumatology, Rush University Medical Center, 1611 W. Harrison Street, Suite 510, Chicago, IL 60612 – name: 5 Rheumatology unit, Department of Medicine, Karolinska Institutet, Stockholm, Sweden – name: 9 Center for Genomics and Oncological Research Pfizer-University of Granada.Junta de Andalucia, Avd de la Ilustración 114, 18007, Granada, Spain |
| Author_xml | – sequence: 1 givenname: Antoine surname: Sreih fullname: Sreih, Antoine – sequence: 2 givenname: Rana surname: Ezzeddine fullname: Ezzeddine, Rana – sequence: 3 givenname: Lin surname: Leng fullname: Leng, Lin – sequence: 4 givenname: Avery surname: LaChance fullname: LaChance, Avery – sequence: 5 givenname: Geraldine surname: Yu fullname: Yu, Geraldine – sequence: 6 givenname: Yuka surname: Mizue fullname: Mizue, Yuka – sequence: 7 givenname: Lakshman surname: Subrahmanyan fullname: Subrahmanyan, Lakshman – sequence: 8 givenname: Bernardo A. surname: Pons‐Estel fullname: Pons‐Estel, Bernardo A. – sequence: 9 givenname: Anna‐Karin surname: Abelson fullname: Abelson, Anna‐Karin – sequence: 10 givenname: Iva surname: Gunnarsson fullname: Gunnarsson, Iva – sequence: 11 givenname: Elisabet surname: Svenungsson fullname: Svenungsson, Elisabet – sequence: 12 givenname: Joshua surname: Cavett fullname: Cavett, Joshua – sequence: 13 givenname: Stuart surname: Glenn fullname: Glenn, Stuart – sequence: 14 givenname: Lin surname: Zhang fullname: Zhang, Lin – sequence: 15 givenname: Ruth surname: Montgomery fullname: Montgomery, Ruth – sequence: 16 givenname: Andras surname: Perl fullname: Perl, Andras – sequence: 17 givenname: Jane surname: Salmon fullname: Salmon, Jane – sequence: 18 givenname: Marta E. surname: Alarcón‐Riquelme fullname: Alarcón‐Riquelme, Marta E. – sequence: 19 givenname: John B. surname: Harley fullname: Harley, John B. – sequence: 20 givenname: Richard surname: Bucala fullname: Bucala, Richard email: Richard.Bucala@yale.edu |
| BackLink | http://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=25330706$$DView record in Pascal Francis https://www.ncbi.nlm.nih.gov/pubmed/22127710$$D View this record in MEDLINE/PubMed https://urn.kb.se/resolve?urn=urn:nbn:se:uu:diva-258971$$DView record from Swedish Publication Index http://kipublications.ki.se/Default.aspx?queryparsed=id:123662822$$DView record from Swedish Publication Index |
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| Copyright | Copyright © 2011 by the American College of Rheumatology 2015 INIST-CNRS Copyright © 2011 by the American College of Rheumatology. |
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| Issue | 12 |
| Keywords | Human Immunopathology Connective tissue disease Skin disease Systemic lupus erythematosus Systemic disease Migration inhibitory factor Rheumatology Autoimmune disease Macrophage |
| Language | English |
| License | http://doi.wiley.com/10.1002/tdm_license_1.1 CC BY 4.0 Copyright © 2011 by the American College of Rheumatology. |
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| Notes | Dr. Bucala has received honoraria for service on the Carolus Therapeutics scientific advisory board (less than $10,000); he is a co‐inventor on a patent describing the diagnostic utility of genotype determination and anti‐MIF, which has been licensed to Baxter Healthcare, Inc. and for which Dr. Bucala receives royalties. Dr. Perl has received consulting fees, speaking fees, and/or honoraria from Ortho Diagnostics (less than $10,000). MIF ObjectType-Article-2 SourceType-Scholarly Journals-1 ObjectType-Feature-1 content type line 14 content type line 23 |
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| PublicationTitle | Arthritis & rheumatology (Hoboken, N.J.) |
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To study the effect of the innate cytokine macrophage migration inhibitory factor (MIF) on the susceptibility and severity of systemic lupus... To study the effect of the innate cytokine macrophage migration inhibitory factor (MIF) on the susceptibility and severity of systemic lupus erythematosus... Objective To study the effect of the innate cytokine macrophage migration inhibitory factor (MIF) on the susceptibility and severity of systemic lupus... |
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| SubjectTerms | Adult African Americans Autoimmune diseases Biological and medical sciences Black or African American - ethnology Case-Control Studies Confidence intervals Cross-Sectional Studies Diseases of the osteoarticular system Female Genetic Predisposition to Disease - genetics Genotype Humans Lupus Lupus Erythematosus, Systemic - blood Lupus Erythematosus, Systemic - ethnology Lupus Erythematosus, Systemic - genetics Macrophage Migration-Inhibitory Factors - blood Macrophage Migration-Inhibitory Factors - genetics Male Medical sciences Middle Aged Phenotype Polymorphism, Single Nucleotide - genetics Sarcoidosis. Granulomatous diseases of unproved etiology. Connective tissue diseases. Elastic tissue diseases. Vasculitis Severity of Illness Index Tumor Necrosis Factor-alpha - blood White People - ethnology |
| Title | Dual effect of the macrophage migration inhibitory factor gene on the development and severity of human systemic lupus erythematosus |
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