268
Views
13
CrossRef citations to date
0
Altmetric
Original Article

Selenium supplementation suppresses immunological and serological features of lupus in B6.Sle1b mice

, , , , &
Pages 57-68 | Received 09 Nov 2018, Accepted 01 Apr 2019, Published online: 22 Apr 2019

References

  • Kaul A, Gordon C, Crow MK, et al. Systemic lupus erythematosus. Nat Rev Dis Primers. 2016;2:16039.
  • Pisetsky DS. Anti-DNA antibodies-quintessential biomarkers of SLE. Nat Rev Rheumatol. 2016;12:102–110.
  • Christensen SR, Shlomchik MJ. Regulation of lupus-related autoantibody production and clinical disease by Toll-like receptors. Semin Immunol. 2007;19:11–23.
  • Shlomchik MJ. Sites and stages of autoreactive B cell activation and regulation. Immunity. 2008;28:18–28.
  • Suurmond J, Calise J, Malkiel S, et al. DNA-reactive B cells in lupus. Curr Opin Immunol. 2016;43:1–7.
  • Jackson SW, Kolhatkar NS, Rawlings DJ. B cells take the front seat: dysregulated B cell signals orchestrate loss of tolerance and autoantibody production. Curr Opin Immunol. 2015;33:70–77.
  • Coutant F, Miossec P. Altered dendritic cell functions in autoimmune diseases: distinct and overlapping profiles. Nat Rev Rheumatol. 2016;12:703–715.
  • Ganguly D, Haak S, Sisirak V, et al. The role of dendritic cells in autoimmunity. Nat Rev Immunol. 2013;13:566–577.
  • Sisirak V, Ganguly D, Lewis KL, et al. Genetic evidence for the role of plasmacytoid dendritic cells in systemic lupus erythematosus. J Exp Med. 2014;211:1969–1976.
  • Soni C, Wong EB, Domeier PP, et al. B cell-intrinsic TLR7 signaling is essential for the development of spontaneous germinal centers. J Immunol. 2014;193:4400–4414.
  • Shlomchik MJ, Marshak-Rothstein A, Wolfowicz CB, et al. The role of clonal selection and somatic mutation in autoimmunity. Nature. 1987;328:805–811.
  • Meffre E, Wardemann H. B-cell tolerance checkpoints in health and autoimmunity. Curr Opin Immunol. 2008;20:632–638.
  • Wong EB, Khan TN, Mohan C, et al. The lupus-prone NZM2410/NZW strain-derived Sle1b sublocus alters the germinal center checkpoint in female mice in a B cell-intrinsic manner. J Immunol. 2012;189:5667–5681.
  • Domeier PP, Schell SL, Rahman ZS. Spontaneous germinal centers and autoimmunity. Autoimmunity. 2017;50:4–18.
  • Furie R, Petri M, Zamani O, et al. A phase III, randomized, placebo-controlled study of belimumab, a monoclonal antibody that inhibits B lymphocyte stimulator, in patients with systemic lupus erythematosus. Arthritis Rheum. 2011;63:3918–3930.
  • Navarra SV, Guzman RM, Gallacher AE, et al. Efficacy and safety of belimumab in patients with active systemic lupus erythematosus: a randomised, placebo-controlled, phase 3 trial. Lancet. 2011;377:721–731.
  • Isenberg DA, Petri M, Kalunian K, et al. Efficacy and safety of subcutaneous tabalumab in patients with systemic lupus erythematosus: results from ILLUMINATE-1, a 52-week, phase III, multicenter, randomised, double-blind, placebo-controlled study. Ann Rheum Dis. 2016;75:323–331.
  • Merrill JT, van Vollenhoven RF, Buyon JP, et al. Efficacy and safety of subcutaneous tabalumab, a monoclonal antibody to B-cell activating factor, in patients with systemic lupus erythematosus: results from ILLUMINATE-2, a 52-week, phase III, multicentre, randomised, double-blind, placebo-controlled study. Ann Rheum Dis. 2016;75:332–340.
  • Furie RA, Leon G, Thomas M, et al. A phase 2, randomised, placebo-controlled clinical trial of blisibimod, an inhibitor of B cell activating factor, in patients with moderate-to-severe systemic lupus erythematosus, the PEARL-SC study. Ann Rheum Dis. 2015;74:1667–1675.
  • Ruiz-Irastorza G, Danza A, Khamashta M. Glucocorticoid use and abuse in SLE. Rheumatology (Oxford). 2012;51:1145–1153.
  • Kasturi S, Sammaritano LR. Corticosteroids in lupus. Rheum Dis Clin North Am. 2016;42:47–62.
  • Schrauzer GN. Nutritional selenium supplements: product types, quality, and safety. J Am Coll Nutr. 2001;20:1–4.
  • Yang X, Tian Y, Ha P, et al. Determination of the selenomethionine content in grain and human blood. Wei Sheng Yan Jiu. 1997; 26:113–116.
  • Vinceti M, Filippini T, Del Giovane C, et al. Selenium for preventing cancer. Cochrane Database Syst Rev. 2018;1:CD005195.
  • Sinha R, Unni E, Ganther HE, et al. Methylseleninic acid, a potent growth inhibitor of synchronized mouse mammary epithelial tumor cells in vitro. Biochem Pharmacol. 2001;61:311–317.
  • Unni E, Koul D, Yung WK, et al. Se-methylselenocysteine inhibits phosphatidylinositol 3-kinase activity of mouse mammary epithelial tumor cells in vitro. Breast Cancer Res. 2005;7:R699–R707.
  • Ip C, Dong Y. Methylselenocysteine modulates proliferation and apoptosis biomarkers in premalignant lesions of the rat mammary gland. Anticancer Res 2001; 21:863–867.
  • Wang L, Bonorden MJ, Li GX, et al. Methyl-selenium compounds inhibit prostate carcinogenesis in the transgenic adenocarcinoma of mouse prostate model with survival benefit. Cancer Prev Res (Phila). 2009;2:484–495.
  • Sinha I, Allen JE, Pinto JT, et al. Methylseleninic acid elevates REDD1 and inhibits prostate cancer cell growth despite AKT activation and mTOR dysregulation in hypoxia. Cancer Med. 2014;3:252–264.
  • Huang Z, Rose AH, Hoffmann PR. The role of selenium in inflammation and immunity: from molecular mechanisms to therapeutic opportunities. Antioxid Redox Signal. 2012;16:705–743.
  • Vega L, Rodriguez-Sosa M, Garcia-Montalvo EA, et al. Non-optimal levels of dietary selenomethionine alter splenocyte response and modify oxidative stress markers in female mice. Food Chem Toxicol. 2007;45:1147–1153.
  • Verma S, Hoffmann FW, Kumar M, et al. Selenoprotein K knockout mice exhibit deficient calcium flux in immune cells and impaired immune responses. J Immunol. 2011;186:2127–2137.
  • Hawkes WC, Richter D, Alkan Z. Dietary selenium supplementation and whole blood gene expression in healthy North American men. Biol Trace Elem Res. 2013;155:201–208.
  • Hawkes WC, Hwang A, Alkan Z. The effect of selenium supplementation on DTH skin responses in healthy North American men. J Trace Elem Med Biol. 2009;23:272–280.
  • Richie JP, Jr., Das A, Calcagnotto AM, et al. Comparative effects of two different forms of selenium on oxidative stress biomarkers in healthy men: a randomized clinical trial. Cancer Prev Res (Phila). 2014;7:796–804.
  • Bentley-Hewitt KL, Chen RK, Lill RE, et al. Consumption of selenium-enriched broccoli increases cytokine production in human peripheral blood mononuclear cells stimulated ex vivo, a preliminary human intervention study. Mol Nutr Food Res. 2014;58:2350–2357.
  • Sahebari M, Abrishami-Moghaddam M, Moezzi A, et al. Association between serum trace element concentrations and the disease activity of systemic lupus erythematosus. Lupus. 2014;23:793–801.
  • O'Dell JR, McGivern JP, Kay HD, et al. Improved survival in murine lupus as the result of selenium supplementation. Clin Exp Immunol. 1988;73:322–327.
  • Sinha I, Karagoz K, Fogle RL, et al. "Omics" of selenium biology: a prospective study of plasma proteome network before and after selenized-yeast supplementation in healthy men. Omics. 2016;20:202–213.
  • Kumar KR, Li L, Yan M, et al. Regulation of B cell tolerance by the lupus susceptibility gene Ly108. Science. 2006;312:1665–1669.
  • Wandstrat AE, Nguyen C, Limaye N, et al. Association of extensive polymorphisms in the SLAM/CD2 gene cluster with murine lupus. Immunity. 2004;21:769–780.
  • Wong EB, Soni C, Chan AY, et al. B cell-intrinsic CD84 and Ly108 maintain germinal center B cell tolerance. J Immunol. 2015;194:4130–4143.
  • Morel L, Croker BP, Blenman KR, et al. Genetic reconstitution of systemic lupus erythematosus immunopathology with polycongenic murine strains. Proc Natl Acad Sci USA. 2000;97:6670–6675.
  • Morel L, Wakeland EK. Lessons from the NZM2410 model and related strains. Int Rev Immunol. 2000;19:423–446.
  • Nguyen C, Limaye N, Wakeland EK. Susceptibility genes in the pathogenesis of murine lupus. Arthritis Res. 2002;4(3):S255–S263.
  • Morel L, Blenman KR, Croker BP, et al. The major murine systemic lupus erythematosus susceptibility locus, Sle1, is a cluster of functionally related genes. Proc Natl Acad Sci USA. 2001;98:1787–1792.
  • Notidis E, Heltemes L, Manser T. Dominant, hierarchical induction of peripheral tolerance during foreign antigen-driven B cell development. Immunity. 2002;17:317–327.
  • Heltemes-Harris L, Liu X, Manser T. Progressive surface B cell antigen receptor down-regulation accompanies efficient development of antinuclear antigen B cells to mature, follicular phenotype. J Immunol. 2004;172:823–833.
  • Li GX, Lee HJ, Wang Z, et al. Superior in vivo inhibitory efficacy of methylseleninic acid against human prostate cancer over selenomethionine or selenite. Carcinogenesis. 2008;29:1005–1012.
  • Rahman ZS, Shao WH, Khan TN, et al. Impaired apoptotic cell clearance in the germinal center by Mer-deficient tingible body macrophages leads to enhanced antibody-forming cell and germinal center responses. J Immunol. 2010;185:5859–5868.
  • Goronzy JJ, Weyand CM. T-cell co-stimulatory pathways in autoimmunity. Arthritis Res Ther. 2008;10(1):S3.
  • Navegantes KC, de Souza Gomes R, Pereira PAT, et al. Immune modulation of some autoimmune diseases: the critical role of macrophages and neutrophils in the innate and adaptive immunity. J Transl Med. 2017;15:36.
  • Crow MK. Collaboration, genetic associations, and lupus erythematosus. N Engl J Med. 2008;358:956–961.
  • Hom G, Graham RR, Modrek B, et al. Association of systemic lupus erythematosus with C8orf13-BLK and ITGAM-ITGAX. N Engl J Med. 2008;358:900–909.
  • Buyon JP, Shadick N, Berkman R, et al. Surface expression of Gp 165/95, the complement receptor CR3, as a marker of disease activity in systemic lupus erythematosus. Clin Immunol Immunopathol. 1988;46:141–149.
  • Austyn JM, Gordon S. F4/80, a monoclonal antibody directed specifically against the mouse macrophage. Eur J Immunol. 1981;11:805–815.
  • Hirsch S, Austyn JM, Gordon S. Expression of the macrophage-specific antigen F4/80 during differentiation of mouse bone marrow cells in culture. J Exp Med. 1981;154:713–725.
  • Folzenlogen D, Hofer MF, Leung DY, et al. Analysis of CD80 and CD86 expression on peripheral blood B lymphocytes reveals increased expression of CD86 in lupus patients. Clin Immunol Immunopathol. 1997;83:199–204.
  • Nagafuchi H, Shimoyama Y, Kashiwakura J, et al. Preferential expression of B7.2 (CD86), but not B7.1 (CD80), on B cells induced by CD40/CD40L interaction is essential for anti-DNA autoantibody production in patients with systemic lupus erythematosus. Clin Exp Rheumatol. 2003; 21:71–77.
  • Relle M, Schwarting A. Role of MHC-linked susceptibility genes in the pathogenesis of human and murine lupus. Clin Dev Immunol. 2012;2012:584374.
  • Kim HJ, Park JW, Cho YS, et al. Pathogenic role of HIF-1alpha in prostate hyperplasia in the presence of chronic inflammation. Biochim Biophys Acta. 2013;1832:183–194.
  • Pastor F, Dumas K, Barthelemy MA, et al. Implication of REDD1 in the activation of inflammatory pathways. Sci Rep. 2017;7:7023.
  • Cho SH, Raybuck AL, Stengel K, et al. Germinal centre hypoxia and regulation of antibody qualities by a hypoxia response system. Nature. 2016;537:234–238.
  • Abbott RK, Thayer M, Labuda J, et al. Germinal center hypoxia potentiates immunoglobulin class switch recombination. J Immunol. 2016;197:4014–4020.
  • Khan TN, Wong EB, Soni C, et al. Prolonged apoptotic cell accumulation in germinal centers of Mer-deficient mice causes elevated B cell and CD4+ Th cell responses leading to autoantibody production. J Immunol. 2013;190:1433–1446.
  • Rahman ZS. Impaired clearance of apoptotic cells in germinal centers: implications for loss of B cell tolerance and induction of autoimmunity. Immunol Res. 2011;51:125–133.
  • Yan L, DeMars LC. Dietary supplementation with methylseleninic acid, but not selenomethionine, reduces spontaneous metastasis of Lewis lung carcinoma in mice. Int J Cancer. 2012;131:1260–1266.
  • Leffler J, Bengtsson AA, Blom AM. The complement system in systemic lupus erythematosus: an update. Ann Rheum Dis. 2014;73:1601–1606.
  • Wardemann H, Nussenzweig MC. B-cell self-tolerance in humans. Adv Immunol. 2007;95:83–110.
  • Mahieu MA, Strand V, Simon LS, et al. A critical review of clinical trials in systemic lupus erythematosus. Lupus. 2016;25:1122–1140.
  • Dorner T, Lipsky PE. Beyond pan-B-cell-directed therapy - new avenues and insights into the pathogenesis of SLE. Nat Rev Rheumatol. 2016;12:645–657.
  • Victora GD, Nussenzweig MC. Germinal centers. Annu Rev Immunol. 2012;30:429–457.
  • Lemke G, Burstyn-Cohen T. TAM receptors and the clearance of apoptotic cells. Ann N Y Acad Sci. 2010;1209:23–29.
  • Baumann I, Kolowos W, Voll RE, et al. Impaired uptake of apoptotic cells into tingible body macrophages in germinal centers of patients with systemic lupus erythematosus. Arthritis Rheum. 2002;46:191–201.
  • Wenes M, Shang M, Di Matteo M, et al. Macrophage metabolism controls tumor blood vessel morphogenesis and metastasis. Cell Metab. 2016;24:701–715.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.