IFN-α negatively regulates the expression of endothelial nitric oxide synthase and nitric oxide production: Implications for systemic lupus erythematosus

Journal of Immunology

Volumn 199, Issue 6, 2017, Pages 1979-1988

  Buie, Joy Jones ^a   Renaud, Ludivine L ^a   Muise Helmericks, Robin ^a   Oates, Jim C ^a,b  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^b RALPH H JOHNSON VA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; ENDOTHELIAL NITRIC OXIDE SYNTHASE; MESSENGER RNA; MICRORNA 155; MONOCYTE CHEMOTACTIC PROTEIN 1; NITRIC OXIDE; VASCULAR CELL ADHESION MOLECULE 1; AUTOANTIGEN; INSULIN; METAPHASE CHROMOSOME PROTEIN 1, HUMAN; MICRORNA; MIRN155 MICRORNA, HUMAN; NITRIC OXIDE SYNTHASE;

ARTICLE; CARDIOVASCULAR DISEASE; CELL ADHESION; CONTROLLED STUDY; ENDOTHELIAL DYSFUNCTION; ENZYME REGULATION; GENE EXPRESSION; GENETIC STABILITY; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUVEC CELL LINE; IMMUNOPATHOGENESIS; MOLECULAR PATHOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SYSTEMIC LUPUS ERYTHEMATOSUS; TRANSCRIPTION SUPPRESSION; UPREGULATION; ANIMAL; BLOOD VESSEL; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; MOUSE; NEUTROPHIL; PATHOLOGY; UMBILICAL VEIN ENDOTHELIAL CELL; VASCULAR ENDOTHELIUM;

ANIMALS; AUTOANTIGENS; BLOOD VESSELS; CELL ADHESION; ENDOTHELIUM, VASCULAR; GENE EXPRESSION REGULATION; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; INSULIN; INTERFERON-ALPHA; LUPUS ERYTHEMATOSUS, SYSTEMIC; MICE; MICRORNAS; NEUTROPHILS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; VASCULAR CELL ADHESION MOLECULE-1;

EID: 85028975317     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1600108     Document Type: Article

References (41)

1. Manzi, S., E. N. Meilahn, J. E. Rairie, C. G. Conte, T. A. Medsger, Jr., L. Jansen-McWilliams, R. B. D'Agostino, and L. H. Kuller. 1997. Age-specific incidence rates of myocardial infarction and angina in women with systemic lupus erythematosus: Comparison with the Framingham study. Am. J. Epidemiol. 145: 408-415.
2. Abu-Shakra, M., M. B. Urowitz, D. D. Gladman, and J. Gough. 1995. Mortality studies in systemic lupus erythematosus. Results from a single center. II. Predictor variables for mortality. J. Rheumatol. 22: 1265-1270.
3. Urowitz, M. B., A. A. Bookman, B. E. Koehler, D. A. Gordon, H. A. Smythe, and M. A. Ogryzlo. 1976. The bimodal mortality pattern of systemic lupus erythematosus. Am. J. Med. 60: 221-225.
4. Al Gadban, M. M., J. German, J. P. Truman, F. Soodavar, E. C. Riemer, W. O. Twal, K. J. Smith, D. Heller, A. F. Hofbauer, J. C. Oates, and S. M. Hammad. 2012. Lack of nitric oxide synthases increases lipoprotein immune complex deposition in the aorta and elevates plasma sphingolipid levels in lupus. Cell. Immunol. 276: 42-51.
5. Gilkeson, G. S., A. K. Mashmoushi, P. Ruiz, T. N. Caza, A. Perl, and J. C. Oates. 2013. Endothelial nitric oxide synthase reduces crescentic and necrotic glomerular lesions, reactive oxygen production, and MCP1 production in murine lupus nephritis. PLoS One 8: E64650.
6. Gómez-Guzmán, M., R. Jiménez, M. Romero, M. Sánchez, M. J. Zarzuelo, M. Gómez-Morales, F. O'Valle, A. J. López-Farré, F. Algieri, J. Gálvez, et al. 2014. Chronic hydroxychloroquine improves endothelial dysfunction and protects kidney in a mouse model of systemic lupus erythematosus. Hypertension 64: 330-337.
7. Ryan, M. J., and G. R. McLemore, Jr. 2007. Hypertension and impaired vascular function in a female mouse model of systemic lupus erythematosus. Am. J. Physiol. Regul. Integr. Comp. Physiol. 292: R736-R742.
8. Kahlenberg, J. M., and M. J. Kaplan. 2011. The interplay of inflammation and cardiovascular disease in systemic lupus erythematosus. Arthritis. Res. Ther. 13: 203
9. Hua, J., K. Kirou, C. Lee, and M. K. Crow. 2006. Functional assay of type I interferon in systemic lupus erythematosus plasma and association with anti-RNA binding protein autoantibodies. Arthritis Rheum. 54: 1906-1916.
10. Fischer, K. 2008. Risk factors of thickened intima-media and atherosclerotic plaque development in carotid arteries in patients with systemic lupus erythematosus. Ann. Acad. Med. Stetin. 54: 22-32.
11. Denny, M. F., S. Thacker, H. Mehta, E. C. Somers, T. Dodick, F. J. Barrat, W. J. McCune, and M. J. Kaplan. 2007. Interferon-alpha promotes abnormal vasculogenesis in lupus: A potential pathway for premature atherosclerosis. Blood 110: 2907-2915.
12. Thacker, S. G., W. Zhao, C. K. Smith, W. Luo, H. Wang, A. Vivekanandan-Giri, B. J. Rabquer, A. E. Koch, S. Pennathur, A. Davidson, et al. 2012. Type I interferons modulate vascular function, repair, thrombosis, and plaque progression in murine models of lupus and atherosclerosis. Arthritis Rheum. 64: 2975-2985.
13. Somers, E. C., W. Zhao, E. E. Lewis, L. Wang, J. J. Wing, B. Sundaram, E. A. Kazerooni, W. J. McCune, and M. J. Kaplan. 2012. Type I interferons are associated with subclinical markers of cardiovascular disease in a cohort of systemic lupus erythematosus patients. PLoS One 7: E37000.
14. Lee, P. Y., Y. Li, H. B. Richards, F. S. Chan, H. Zhuang, S. Narain, E. J. Butfiloski, E. S. Sobel, W. H. Reeves, and M. S. Segal. 2007. Type I interferon as a novel risk factor for endothelial progenitor cell depletion and endothelial dysfunction in systemic lupus erythematosus. Arthritis Rheum. 56: 3759-3769.
15. Thacker, S. G., C. C. Berthier, D. Mattinzoli, M. P. Rastaldi, M. Kretzler, and M. J. Kaplan. 2010. The detrimental effects of IFN-a on vasculogenesis in lupus are mediated by repression of IL-1 pathways: Potential role in atherogenesis and renal vascular rarefaction. J. Immunol. 185: 4457-4469.
16. Kamen, D. L., M. Barron, T. M. Parker, S. R. Shaftman, G. R. Bruner, T. Aberle, J. A. James, R. H. Scofield, J. B. Harley, and G. S. Gilkeson. 2008. Autoantibody prevalence and lupus characteristics in a unique African American population. Arthritis Rheum. 58: 1237-1247.
17. Doria, A., P. Vesco, F. Zulian, and P. F. Gambari. 1994. The 1982 ARA/ACR criteria for the classification of systemic lupus erythematosus in pediatric and adult patients. Clin. Exp. Rheumatol. 12: 689-690.
18. Wong, S. C., E. S. Lo, and M. T. Cheung. 2004. An optimised protocol for the extraction of non-viral mRNA from human plasma frozen for three years. J. Clin. Pathol. 57: 766-768.
19. Harvey, K. A., Z. Xu, T. M. Pavlina, G. P. Zaloga, and R. A. Siddiqui. 2015. Modulation of endothelial cell integrity and inflammatory activation by commercial lipid emulsions. Lipids Health Dis. 14: 9.
20. Kaiser, W. J., J. L. Kaufman, and M. K. Offermann. 2004. IFN-alpha sensitizes human umbilical vein endothelial cells to apoptosis induced by double-stranded RNA. J. Immunol. 172: 1699-1710.
21. Chen, J., J. Jin, M. Song, H. Dong, G. Zhao, and L. Huang. 2012. C-reactive protein down-regulates endothelial nitric oxide synthase expression and promotes apoptosis in endothelial progenitor cells through receptor for advanced glycation end-products. Gene 496: 128-135.
22. Shi, L., and I. Fleming. 2012. One miR level of control: MicroRNA-155 directly regulates endothelial nitric oxide synthase mRNA and protein levels. Hypertension 60: 1381-1382.
23. Zeng, G., F. H. Nystrom, L. V. Ravichandran, L. N. Cong, M. Kirby, H. Mostowski, and M. J. Quon. 2000. Roles for insulin receptor, PI3-kinase, and Akt in insulin-signaling pathways related to production of nitric oxide in human vascular endothelial cells. Circulation 101: 1539-1545.
24. Sugimoto, M., M. Nakayama, T. M. Goto, M. Amano, K. Komori, and K. Kaibuchi. 2007. Rho-kinase phosphorylates eNOS at threonine 495 in endothelial cells. Biochem. Biophys. Res. Commun. 361: 462-467.
25. Kaplan, M. J. 2009. Premature vascular damage in systemic lupus erythematosus: An imbalance of damage and repair? Transl. Res. 154: 61-69.
26. Crow, M. K. 2010. Interferon-alpha: A therapeutic target in systemic lupus erythematosus. Rheum. Dis. Clin. North Am. 36: 173-186, x.
27. Cates, A. M., V. I. Holden, E. M. Myers, C. K. Smith, M. J. Kaplan, and J. M. Kahlenberg. 2015. Interleukin 10 hampers endothelial cell differentiation and enhances the effects of interferon a on lupus endothelial cell progenitors. Rheumatology 54: 1114-1123.
28. Vallin, H., A. Perers, G. V. Alm, and L. Rönnblom. 1999. Anti-double-stranded DNA antibodies and immunostimulatory plasmid DNA in combination mimic the endogenous IFN-alpha inducer in systemic lupus erythematosus. J. Immunol. 163: 6306-6313.
29. Kahlenberg, J. M., and M. J. Kaplan. 2013. Mechanisms of premature atherosclerosis in rheumatoid arthritis and lupus. Annu. Rev. Med. 64: 249-263.
30. Thum, T., D. Fraccarollo, M. Schultheiss, S. Froese, P. Galuppo, J. D. Widder, D. Tsikas, G. Ertl, and J. Bauersachs. 2007. Endothelial nitric oxide synthase uncoupling impairs endothelial progenitor cell mobilization and function in diabetes. Diabetes 56: 666-674.
31. Bauersachs, J., and A. Schäfer. 2005. Tetrahydrobiopterin and eNOS dimer/ monomer ratio-a clue to eNOS uncoupling in diabetes? Cardiovasc. Res. 65: 768-769.
32. Alvarado-Vásquez, N., E. Zapata, S. Alcázar-Leyva, F. Massó, and L. F. Montaño. 2007. Reduced NO synthesis and eNOS mRNA expression in endothelial cells from newborns with a strong family history of type 2 diabetes. Diabetes Metab. Res. Rev. 23: 559-566.
33. Triggle, C. R., and H. Ding. 2010. A review of endothelial dysfunction in diabetes: A focus on the contribution of a dysfunctional eNOS. J. Am. Soc. Hypertens. 4: 102-115.
34. Baechler, E. C., F. M. Batliwalla, G. Karypis, P. M. Gaffney, W. A. Ortmann, K. J. Espe, K. B. Shark, W. J. Grande, K. M. Hughes, V. Kapur, et al. 2003. Interferon-inducible gene expression signature in peripheral blood cells of patients with severe lupus. Proc. Natl. Acad. Sci. USA 100: 2610-2615.
35. Ota, K., T. Matsumiya, H. Sakuraba, T. Imaizumi, H. Yoshida, S. Kawaguchi, S. Fukuda, and K. Satoh. 2010. Interferon-alpha2b induces p21cip1/waf1 degradation and cell proliferation in HeLa cells. Cell Cycle 9: 131-139.
36. Sun, H. X., D. Y. Zeng, R. T. Li, R. P. Pang, H. Yang, Y. L. Hu, Q. Zhang, Y. Jiang, L. Y. Huang, Y. B. Tang, et al. 2012. Essential role of microRNA-155 in regulating endothelium-dependent vasorelaxation by targeting endothelial nitric oxide synthase. Hypertension 60: 1407-1414.
37. Hartmann, P., A. Schober, and C. Weber. 2014. MicroRNA-155 and macrophages: A fatty liaison. Cardiovasc. Res. 103: 5-6.
38. Wang, R., L. D. Dong, X. B. Meng, Q. Shi, and W. Y. Sun. 2015. Unique microRNA signatures associated with early coronary atherosclerotic plaques. Biochem. Biophys. Res. Commun. 464: 574-579.
39. Wang, P., J. Hou, L. Lin, C. Wang, X. Liu, D. Li, F. Ma, Z. Wang, and X. Cao. 2010. Inducible microRNA-155 feedback promotes type I IFN signaling in antiviral innate immunity by targeting suppressor of cytokine signaling 1. J. Immunol. 185: 6226-6233.
40. Reynolds, J. A., D. W. Ray, L. A. Zeef, T. O'Neill, I. N. Bruce, and M. Y. Alexander. 2014. The effect of type 1 IFN on human aortic endothelial cell function in vitro: Relevance to systemic lupus erythematosus. J. Interferon. Cytokine. Res. 34: 404-412.
41. Xie, Q. W., H. J. Cho, J. Calaycay, R. A. Mumford, K. M. Swiderek, T. D. Lee, A. Ding, T. Troso, and C. Nathan. 1992. Cloning and characterization of inducible nitric oxide synthase from mouse macrophages. Science 256: 225-228.