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The beneficial role of vitamin D in systemic lupus erythematosus (SLE)

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Abstract

Patients with systemic lupus erythematosus (SLE) have a high prevalence of abnormal bone metabolism and vitamin D deficiency. Genetic studies have provided the opportunity to determine the specific proteins linking vitamin D to SLE pathology [i.e., major histocompatibility complex (MHC) class II molecules, the vitamin D receptor (VDR), microRNAs (miRNAs), the renin–angiotensin system (RAS), apolipoprotein E (ApoE), liver X receptor (LXR), and toll-like receptors (TLRs)]. Vitamin D also exerts protective effects against SLE through non-genomic factors, such as ultraviolet radiation (UV) exposure, matrix metalloproteinase (MMPs), heme oxygenase-1 (HO-1), the prostaglandins (PGs), cyclooxygenase-2 (COX-2), and oxidative stress. Thus, vitamin D may play a beneficial role in SLE. Moreover, the use of calcitriol or 1α,25-dihydroxyvitamin D3 is optimal for the treatment of SLE patients because this active form of the vitamin D3 metabolite can modulate inflammatory cytokine production. However, further investigation into the effects of calcitriol with SLE is warranted.

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REFERENCES

  1. Fragoso TS, Dantas AT, Marques CD, Rocha Junior LF, Melo JH et al (2012) 25-Hydroxyvitamin D3 levels in patients with systemic lupus erythematosus and its association with clinical parameters and laboratory tests. Rev Bras Reumatol 52:60–5

    PubMed  Google Scholar 

  2. López-Robles C, Rios-Fernández R, Callejas-Rubio JL, Ortego-Centeno N (2011) Vitamin D deficiency in a cohort of patients with systemic lupus erythematosus from the South of Spain. Lupus 20:330–1

    PubMed  Google Scholar 

  3. Hamza RT, Awwad KS, Ali MK, Hamed AI (2011) Reduced serum concentrations of 25-hydroxy vitamin D in Egyptian patients with systemic lupus erythematosus: relation to disease activity. Med Sci Monit 17:CR711–8

    PubMed  CAS  Google Scholar 

  4. Becker A, Fischer R, Schneider M (2001) Bone density and 25-OH vitamin D serum level in patients with systemic lupus erythematosus. Z Rheumatol 60:352–8 [Article in German]

    PubMed  CAS  Google Scholar 

  5. Amital H, Szekanecz Z, Szücs G, Dankó K, Nagy E et al (2010) Serum concentrations of 25-OH vitamin D in patients with systemic lupus erythematosus (SLE) are inversely related to disease activity: is it time to routinely supplement patients with SLE with vitamin D? Ann Rheum Dis 69:1155–7

    PubMed  CAS  Google Scholar 

  6. Müller K, Kriegbaum NJ, Baslund B, Sørensen OH, Thymann M, Bentzen K (1995) Vitamin D3 metabolism in patients with rheumatic diseases: low serum levels of 25-hydroxyvitamin D3 in patients with systemic lupus erythematosus. Clin Rheumatol 14:397–400

    PubMed  Google Scholar 

  7. Toloza SM, Cole DE, Gladman DD, Ibañez D, Urowitz MB (2010) Vitamin D insufficiency in a large female SLE cohort. Lupus 19:13–9

    PubMed  CAS  Google Scholar 

  8. Kim HA, Sung JM, Jeon JY, Yoon JM, Suh CH (2011) Vitamin D may not be a good marker of disease activity in Korean patients with systemic lupus erythematosus. Rheumatol Int 31:1189–94

    PubMed  CAS  Google Scholar 

  9. Cutillas-Marco E, Morales-Suárez-Varela M, Marquina-Vila A, Grant W (2010) Serum 25-hydroxyvitamin D levels in patients with cutaneous lupus erythematosus in a Mediterranean region. Lupus 19:810–4

    PubMed  CAS  Google Scholar 

  10. Borba VZ, Vieira JG, Kasamatsu T, Radominski SC, Sato EI, Lazaretti-Castro M (2009) Vitamin D deficiency in patients with active systemic lupus erythematosus. Osteoporos Int 20:427–33

    PubMed  CAS  Google Scholar 

  11. Wenzel J, Henze S, Brähler S, Bieber T, Tüting T (2005) The expression of human leukocyte antigen-DR and CD25 on circulating T cells in cutaneous lupus erythematosus and correlation with disease activity. Exp Dermatol 14:454–9

    PubMed  CAS  Google Scholar 

  12. Viallard JF, Bloch-Michel C, Neau-Cransac M, Taupin JL, Garrigue S et al (2001) HLA-DR expression on lymphocyte subsets as a marker of disease activity in patients with systemic lupus erythematosus. Clin Exp Immunol 125:485–91

    PubMed  CAS  Google Scholar 

  13. Jacobi AM, Mei H, Hoyer BF, Mumtaz IM, Thiele K et al (2010) HLA-DRhigh/CD27high plasmablasts indicate active disease in patients with systemic lupus erythematosus. Ann Rheum Dis 69:305–8

    PubMed  CAS  Google Scholar 

  14. Rashtak S, Marietta E, Cheng S, Camilleri M, Pittelkow M et al (2010) Spontaneous lupus-like syndrome in HLA-DQ2 transgenic mice with a mixed genetic background. Lupus 19:815–29

    PubMed  CAS  Google Scholar 

  15. Pan CF, Wu CJ, Chen HH, Dang CW, Chang FM et al (2009) Molecular analysis of HLA-DRB1 allelic associations with systemic lupus erythematosus and lupus nephritis in Taiwan. Lupus 18:698–704

    PubMed  CAS  Google Scholar 

  16. Fojtíková M, Novota P, Cejková P, Pešičková S, Tegzová D, Cerná M (2011) HLA class II, MICA and PRL gene polymorphisms: the common contribution to the systemic lupus erythematosus development in Czech population. Rheumatol Int 31:1195–201

    PubMed  Google Scholar 

  17. Vasconcelos C, Carvalho C, Leal B, Pereira C, Bettencourt A et al (2009) HLA in Portuguese systemic lupus erythematosus patients and their relation to clinical features. Ann N Y Acad Sci 1173:575–80

    PubMed  CAS  Google Scholar 

  18. Siriboonrit U, Tsuchiya N, Sirikong M, Kyogoku C, Bejrachandra S et al (2003) Association of Fcgamma receptor IIb and IIIb polymorphisms with susceptibility to systemic lupus erythematosus in Thais. Tissue Antigens 61:374–83

    PubMed  CAS  Google Scholar 

  19. Ayed K, Gorgi Y, Ayed-Jendoubi S, Bardi R (2004) The involvement of HLA-DRB1*, DQA1*, DQB1* and complement C4A loci in diagnosing systemic lupus erythematosus among Tunisians. Ann Saudi Med 24:31–5

    PubMed  Google Scholar 

  20. Smikle M, Christian N, DeCeulaer K, Barton E, Roye-Green K et al (2002) HLA-DRB alleles and systemic lupus erythematosus in Jamaicans. South Med J 95:717–9

    PubMed  Google Scholar 

  21. Lee HS, Chung YH, Kim TG, Kim TH, Jun JB et al (2003) Independent association of HLA-DR and FCgamma receptor polymorphisms in Korean patients with systemic lupus erythematosus. Rheumatology (Oxford) 42:1501–7

    CAS  Google Scholar 

  22. Mosaad YM, Hammad A, Youssef HM, Elhanbly S (2010) HLA-DRB1*15 confers susceptibility to juvenile SLE but is not associated with disease presentation: an Egyptian study. Immunol Invest 39:235–44

    PubMed  CAS  Google Scholar 

  23. Endreffy E, Kovács A, Kovács L, Pokorny G (2003) HLA class II allele polymorphism in Hungarian patients with systemic lupus erythematosus. Ann Rheum Dis 62:1017–8

    PubMed  CAS  Google Scholar 

  24. Reveille JD, Moulds JM, Ahn C, Friedman AW, Baethge B et al (1998) Systemic lupus erythematosus in three ethnic groups: I. The effects of HLA class II, C4, and CR1 alleles, socioeconomic factors, and ethnicity at disease onset. LUMINA Study Group. Lupus in minority populations, nature versus nurture. Arthritis Rheum 41:1161–72

    PubMed  CAS  Google Scholar 

  25. Cortes LM, Baltazar LM, Lopez-Cardona MG, Olivares N, Ramos C et al (2004) HLA class II haplotypes in Mexican systemic lupus erythematosus patients. Hum Immunol 65:1469–76

    PubMed  CAS  Google Scholar 

  26. Stevens AM, Tsao BP, Hahn BH, Guthrie K, Lambert NC et al (2005) Maternal HLA class II compatibility in men with systemic lupus erythematosus. Arthritis Rheum 52:2768–73

    PubMed  CAS  Google Scholar 

  27. Sebastiani GD, Galeazzi M, Tincani A, Scorza R, Mathieu A et al (2003) HLA-DPB1 alleles association of anticardiolipin and anti-beta2GPI antibodies in a large series of European patients with systemic lupus erythematosus. Lupus 12:560–3

    PubMed  CAS  Google Scholar 

  28. Miyagawa S, Shinohara K, Fujita T, Kidoguchi K, Fukumoto T et al (1997) Neonatal lupus erythematosus: analysis of HLA class II alleles in mothers and siblings from seven Japanese families. J Am Acad Dermatol 36:186–90

    PubMed  CAS  Google Scholar 

  29. Paisansinsup T, Vallejo AN, Luthra H, David CS (2001) HLA-DR modulates autoantibody repertoire, but not mortality, in a humanized mouse model of systemic lupus erythematosus. J Immunol 167:4083–90

    PubMed  CAS  Google Scholar 

  30. Tokuda N, Mizuki N, Kasahara M, Levy RB (1992) 1,25-Hydroxyvitamin D3 down-regulation of HLA-DR on human peripheral blood monocytes. Immunol 75:349–54

    CAS  Google Scholar 

  31. Tokuda N, Levy R (1996) 1,25-Hydroxyvitamin D3 stimulates phagocytosis but suppresses HLA-DR and CD13 antigen expression in human mononuclear phagocytes. Proc Soc Exp Biol Med 211:244–50

    PubMed  CAS  Google Scholar 

  32. Xu H, Soruri A, Gieseler RK, Peters JH (1993) 1,25-Dihydroxyvitamin D3 exerts opposing effects to IL-4 on MHC class-II antigen expression, accessory activity, and phagocytosis of human monocytes. Scand J Immunol 38:535–60

    PubMed  CAS  Google Scholar 

  33. Rigby W, Waugh M, Graziano R (1990) Regulation of human monocyte HLA-DR and CD4 antigen expression, and antigen presentation by 1,25-dihydroxyvitamin D3. Blood 76:189–97

    PubMed  CAS  Google Scholar 

  34. Tamaki K, Saitoh A, Kubota Y (1990-1991) 1,25-Hydroxyvitamin D3 decreases the interferon-gamma (IFN-gamma) induced HLA-DR expression but not intercellular adhesion molecule 1 (ICAM-1) on human keratinocytes. Reg Immunol 3:223–7

    Google Scholar 

  35. Tone T, Eto H, Katsuoka K, Nishioka K, Nishiyama S (1991) Suppression of gamma-interferon induced HLA-DR antigen expression on normal and transformed keratinocytes by 1,25 (OH)2 vitamin D3. Nippon Hifuka Gakkai Zasshi 101:519–25 [Article in Japanese]

    PubMed  CAS  Google Scholar 

  36. Tone T, Eto H, Katou T, Otani F, Nishiyama S (1993) 1 Alpha,25-dihydroxyvitamin D3 modulation of HLA-DR mRNA induced by gamma-interferon in cultured epithelial tumor cell lines. J Dermatol 20:581–4

    PubMed  CAS  Google Scholar 

  37. Scherberich J, Kellermeyer M, Ried C, Hartinger A (2005) 1-Alpha-calcidol modulates major human monocyte antigens and toll-like receptors TRL2 and TRL4 in vitro. Eur J Med Res 10:179–82

    PubMed  CAS  Google Scholar 

  38. Ozaki Y, Nomura S, Nagahama M, Yoshimura C, Kagawa H, Fukuhara S (2000) Vitamin-D receptor genotype and renal disorder in Japanese patients with systemic lupus erythematosus. Nephron 85:86–91

    PubMed  CAS  Google Scholar 

  39. Huang CM, Wu MC, Wu JY, Tsai FJ (2002) Association of vitamin D receptor gene Bsml polymorphisms in Chinese patients with systemic lupus erythematosus. Lupus 11:31–4

    PubMed  CAS  Google Scholar 

  40. Luo XY, Yang MH, Wu FX, Wu JY, Chen L et al (2012) Vitamin D receptor gene BsmI polymorphism B allele, but not BB genotype, is associated with systemic lupus erythematosus in a Han Chinese population. Lupus 21:53–9

    PubMed  CAS  Google Scholar 

  41. Sakulpipatsin W, Verasertniyom O, Nantiruj K, Totemchokchyakarn K, Lertsrisatit P, Janwityanujit S (2006) Vitamin D receptor gene BsmI polymorphisms in Thai patients with systemic lupus erythematosus. Arthritis Res Ther 8:R48

    PubMed  Google Scholar 

  42. Abbasi M, Rezaieyazdi Z, Afshari JT, Hatef M, Sahebari M, Saadati N (2010) Lack of association of vitamin D receptor gene BsmI polymorphisms in patients with systemic lupus erythematosus. Rheumatol Int. 30:1537–9

    Google Scholar 

  43. Luo XY, Wu LJ, Yang MH, Liu NT, Liao T et al (2011) Relationship of vitamin D receptor gene FokI polymorphism with systemic lupus erythematosus. Xi Bao Yu Fen Mian Yi Xue Za Zhi 27:901–5 [Article in Chinese]

    CAS  Google Scholar 

  44. Huang CM, Wu MC, Wu JY, Tsai FJ (2002) No association of vitamin D receptor gene start codon fok 1 polymorphisms in Chinese patients with systemic lupus erythematosus. J Rheumatol 29:1211–3

    PubMed  CAS  Google Scholar 

  45. Lee YH, Bae SC, Choi SJ, Ji JD, Song GG (2011) Associations between vitamin D receptor polymorphisms and susceptibility to rheumatoid arthritis and systemic lupus erythematosus: a meta-analysis. Mol Biol Rep 38:3643–51

    PubMed  CAS  Google Scholar 

  46. Lu HJ, Li HL, Hao P, Li JM, Zhou LF (2003) Association of the vitamin D receptor gene start codon polymorphism with vitamin D deficiency rickets. Zhonghua Er Ke Za Zhi 41:493–6 [Article in Chinese]

    PubMed  Google Scholar 

  47. Wu SH, Yu SD, Yan CH, Shen LX, Yu XG et al (2006) Association between vitamin D receptor gene polymorphism and vitamin D deficiency rickets. Zhongguo Dang Dai Er Ke Za Zhi 8:121–4 [Article in Chinese]

    PubMed  CAS  Google Scholar 

  48. Gilad S, Meiri E, Yogev Y, Benjamin S, Lebanony D et al (2008) Serum microRNAs are promising novel biomarkers. PLoS One 3:e3148

    PubMed  Google Scholar 

  49. Pauley KM, Cha S, Chan EK (2009) MicroRNA in autoimmunity and autoimmune diseases. J Autoimmun 32:189–94

    PubMed  CAS  Google Scholar 

  50. Lu LF, Liston A (2009) MicroRNA in the immune system, microRNA as an immune system. Immunology 127:291–8

    PubMed  CAS  Google Scholar 

  51. Dai Y, Huang YS, Tang M, Lv TY, Hu CX et al (2007) Microarray analysis of microRNA expression in peripheral blood cells of systemic lupus erythematosus patients. Lupus 16:939–46

    PubMed  CAS  Google Scholar 

  52. Dai Y, Sui W, Lan H, Yan Q, Huang H, Huang Y (2009) Comprehensive analysis of microRNA expression patterns in renal biopsies of lupus nephritis patients. Rheumatol Int 29:749–54

    PubMed  CAS  Google Scholar 

  53. Hai-yan W, Yang L, Mei-hong C, Hui Z (2011) Expression of microRNA-146a in peripheral blood mononuclear cells in patients with systemic lupus erythematosus. Zhongguo Yi Xue Ke Xue Yuan Xue Bao 33:185–8

    PubMed  Google Scholar 

  54. Tang Y, Luo X, Cui H, Ni X, Yuan M et al (2009) MicroRNA-146A contributes to abnormal activation of the type I interferon pathway in human lupus by targeting the key signaling proteins. Arthritis Rheum 60:1065–75

    PubMed  CAS  Google Scholar 

  55. Luo X, Yang W, Ye DQ, Cui H, Zhang Y et al (2011) A functional variant in microRNA-146a promoter modulates its expression and confers disease risk for systemic lupus erythematosus. PLoS Genet 7:e1002128

    PubMed  CAS  Google Scholar 

  56. Zhang J, Yang B, Ying B, Li D, Shi Y et al (2011) Association of pre-microRNAs genetic variants with susceptibility in systemic lupus erythematosus. Mol Biol Rep 38:1463–8

    PubMed  CAS  Google Scholar 

  57. Wang G, Tam LS, Li EK, Kwan BC, Chow KM et al (2011) Serum and urinary free microRNA level in patients with systemic lupus erythematosus. Lupus 20:493–500

    PubMed  CAS  Google Scholar 

  58. Wang G, Tam LS, Kwan BC, Li EK, Chow KM, et al (2012) Expression of miR-146a and miR-155 in the urinary sediment of systemic lupus erythematosus. Clin Rheumatol 31:435–40

    Google Scholar 

  59. Pan YZ, Gao W, Yu AM (2009) MicroRNAs regulate CYP3A4 expression via direct and indirect targeting. Drug Metab Dispos 37:2112–7

    PubMed  CAS  Google Scholar 

  60. Komagata S, Nakajima M, Takagi S, Mohri T, Taniya T, Yokoi T (2009) Human CYP24 catalyzing the inactivation of calcitriol is post-transcriptionally regulated by miR-125b. Mol Pharmacol 76:702–9

    PubMed  CAS  Google Scholar 

  61. Wang WL, Chatterjee N, Chittur SV, Welsh J, Tenniswood MP (2011) Effects of 1α,25 dihydroxyvitamin D3 and testosterone on miRNA and mRNA expression in LNCaP cells. Mol Cancer 10:58

    PubMed  CAS  Google Scholar 

  62. Essa S, Denzer N, Mahlknecht U, Klein R, Collnot EM et al (2010) VDR microRNA expression and epigenetic silencing of vitamin D signaling in melanoma cells. J Steroid Biochem Mol Biol 121:110–3

    PubMed  CAS  Google Scholar 

  63. Johnston CI (1994) Tissue angiotensin converting enzyme in cardiac and vascular hypertrophy, repair, and remodeling. Hypertension 23:258–68

    PubMed  CAS  Google Scholar 

  64. Tareeva IE, Shvetsov MIu, Kutyrina IM, Gerasimenko OI (1998) Hemodynamic mechanisms of lupus nephritis progression. Ter Arkh 70:11–4 [Article in Russian]

    PubMed  CAS  Google Scholar 

  65. Bugrova OV, Kutyrina IM, Bagirova VV, Morozova EV, Gromova MM (2001) Effects of acute pharmacological blockade of the renin–angiotensin system on intrarenal hemodynamics in patients with systemic lupus erythematosus and systemic scleroderma. Ter Arkh 73:20–5 [Article in Russian]

    PubMed  CAS  Google Scholar 

  66. Ryan MJ (2009) The pathophysiology of hypertension in systemic lupus erythematosus. Am J Physiol Regul Integr Comp Physiol 296:R1258–67

    PubMed  CAS  Google Scholar 

  67. Venegas-Pont M, Mathis KW, Iliescu R, Ray WH, Glover PH, Ryan MJ (2011) Blood pressure and renal hemodynamic responses to acute angiotensin II infusion are enhanced in a female mouse model of systemic lupus erythematosus. Am J Physiol Regul Integr Comp Physiol 301:R1286–92

    PubMed  CAS  Google Scholar 

  68. Kanda H, Kubo K, Tateishi S, Sato K, Yonezumi A et al (2005) Antiproteinuric effect of ARB in lupus nephritis patients with persistent proteinuria despite immunosuppressive therapy. Lupus 14:288–92

    PubMed  CAS  Google Scholar 

  69. Molad Y, Gal E, Magal N, Sulkes J, Mukamel M et al (2000) Renal outcome and vascular morbidity in systemic lupus erythematosus (SLE): lack of association with the angiotensin-converting enzyme gene polymorphism. Semin Arthritis Rheum 30:132–7

    PubMed  CAS  Google Scholar 

  70. Al-Awadhi AM, Haider MZ, Sharma PN, Hasan EA, Botaiban F et al (2007) Angiotensin-converting enzyme gene polymorphism in Kuwaiti patients with systemic lupus erythematosus. Clin Exp Rheumatol 25:437–42

    PubMed  CAS  Google Scholar 

  71. Pullmann R Jr, Lukác J, Skerenová M, Rovensky J, Hybenová J et al (1999) Association between systemic lupus erythematosus and insertion/deletion polymorphism of the angiotensin converting enzyme (ACE) gene. Clin Exp Rheumatol 17:593–6

    PubMed  Google Scholar 

  72. Prkacin I, Novak B, Sertić J, Mrzljak A (2001) Angiotensin-converting enzyme gene polymorphism in patients with systemic lupus. Acta Med Croatica 55:73–6

    PubMed  CAS  Google Scholar 

  73. Sprovieri SR, Sens YA, Martini Filho D (2005) Association between polymorphisms of the renin–angiotensin system and more severe histological forms of lupus nephritis. Clin Nephrol 64:20–7

    PubMed  CAS  Google Scholar 

  74. Guan T, Liu Z, Chen Z (1997) Angiotensin-converting enzyme gene polymorphism and the clinical pathological features and progression in lupus nephritis. Zhonghua Nei Ke Za Zhi 36:461–4 [Article in Chinese]

    PubMed  CAS  Google Scholar 

  75. Uhm WS, Lee HS, Chung YH, Kim TH, Bae SC et al (2002) Angiotensin-converting enzyme gene polymorphism and vascular manifestations in Korean patients with SLE. Lupus 11:227–33

    PubMed  CAS  Google Scholar 

  76. Akai Y, Sato H, Iwano M, Kurumatani N, Kurioka H et al (1999) Association of an insertion polymorphism of angiotensin-converting enzyme gene with the activity of lupus nephritis. Nephrol 51:141–6

    CAS  Google Scholar 

  77. Parsa A, Lovett DH, Peden EA, Zhu L, Seldin MF, Criswell LA (2005) Renin–angiotensin system gene polymorphisms predict the progression to renal insufficiency among Asians with lupus nephritis. Genes Immun 6:217–24

    PubMed  CAS  Google Scholar 

  78. Rabbani MA, Mahmood MS, Mekan SF, Frossard PM (2008) Association of angiotensin-converting enzyme gene dimorphisms with severity of lupus disease. Saudi J Kidney Dis Transpl 19:761–6

    PubMed  Google Scholar 

  79. Lee YH, Rho YH, Choi SJ, Ji JD, Song GG (2006) Angiotensinconverting enzyme insertion/deletion polymorphism and systemic lupus erythematosus: a metaanalysis. J Rheumatol 33:698–702

    PubMed  CAS  Google Scholar 

  80. Ravenell RL, Kamen DL, Spence JD, Hollis BW, Fleury TJ, et al (2012) Premature Atherosclerosis Is Associated With Hypovitaminosis D and Angiotensin-Converting Enzyme Inhibitor Non-use in Lupus Patients. Am J Med Sci. doi:10.1097/MAJ.0b013e31823fa7d9

  81. Pérez-Castrillón JL, Justo I, Sanz A, De Luis D, Dueñas A (2006) Effect of angiotensin converting enzyme inhibitors on 1,25(OH)2 D levels of hypertensive patients. Relationship with ACE polymorphisms. Horm Metab Res 38:812–6

    PubMed  Google Scholar 

  82. Kulah E, Dursun A, Aktunc E, Acikgoz S, Aydin M et al (2007) Effects of angiotensin-converting enzyme gene polymorphism and serum vitamin D levels on ambulatory blood pressure measurement and left ventricular mass in Turkish hypertensive population. Blood Press Monit 12:207–13

    PubMed  Google Scholar 

  83. Xiang W, Kong J, Chen S, Cao L, Qiao G et al (2005) Cardiac hypertrophy in vitamin D receptor knockout mice: role of the systemic and cardiac renin–angiotensin systems. Am J Phys Endocrinol Met 288:E125–32

    CAS  Google Scholar 

  84. Yuan W, Pan W, Kong J, Zheng W, Szeto F et al (2007) 1,25-Dihydroxyvitamin D3 suppresses renin gene transcription by blocking the activity of the cyclic AMP response element in the renin gene promoter. J Biol Chem 282:29821–30

    PubMed  CAS  Google Scholar 

  85. Higiwara H, Furuhashi H, Nakaya K, Nakamura Y (1988) Effects of vitamin D3 and related compounds on angiotensin converting activity of endothelial cells and on release of plasminogen activator from them. Chem Pharm Bull 36:4858–64

    Google Scholar 

  86. Juárez-Rojas J, Medina-Urrutia A, Posadas-Sánchez R, Jorge-Galarza E, Mendoza-Pérez E et al (2008) High-density lipoproteins are abnormal in young women with uncomplicated systemic lupus erythematosus. Lupus 17:981–7

    PubMed  Google Scholar 

  87. Chong YB, Yap DY, Tang CS, Chan TM (2011) Dyslipidaemia in patients with lupus nephritis. Nephrology (Carlton) 16:511–7

    Google Scholar 

  88. Olusi SO, George S (2011) Prevalence of LDL atherogenic phenotype in patients with systemic lupus erythematosus. Vasc Health Risk Manag 7:75–80

    PubMed  Google Scholar 

  89. Bassi N, Zampieri S, Ghirardello A, Tonon M, Zen M, Beggio S et al (2009) oxLDL/beta2GPI complex and anti-oxLDL/beta2GPI in SLE: prevalence and correlates. Autoimmunity 42:289–91

    PubMed  CAS  Google Scholar 

  90. Lin BF, Huang CH, Chiang BL, Jeng SJ (1996) Dietary fat influences Ia antigen expression, cytokines and prostaglandin E2 production of immune cells in autoimmune-prone NZB x NZW F1 mice. Br J Nutr 75:711–22

    PubMed  CAS  Google Scholar 

  91. O’Neill SG, Giles I, Lambrianides A, Manson J, D’Cruz D et al (2010) Antibodies to apolipoprotein A-I, high-density lipoprotein, and C-reactive protein are associated with disease activity in patients with systemic lupus erythematosus. Arthritis Rheum 62:845–54

    PubMed  Google Scholar 

  92. Ma Z, Choudhury A, Kang SA, Monestier M, Cohen PL, Eisenberg RA (2006) Accelerated atherosclerosis in ApoE deficient lupus mouse models. J Immunol 177:7444–50

    PubMed  CAS  Google Scholar 

  93. Pullmann R Jr, Skerenová M, Hybenová J, Lukác J, Rovenský J, Pullmann R (2004) Apolipoprotein E polymorphism in patients with neuropsychiatric SLE. Clin Rheumatol 23:97–101

    PubMed  Google Scholar 

  94. Orlacchio A, Bruce IN, Rahman P, Kawarai T, Bernardi G et al (2008) The apolipoprotein E2 isoform is associated with accelerated onset of coronary artery disease in systemic lupus erythematosus. Med Sci Monit 14:CR233–7

    PubMed  Google Scholar 

  95. A-Gonzalez N, Bensinger SJ, Hong C, Beceiro S, Bradley MN et al (2009) Apoptotic cells promote their own clearance and immune tolerance through activation of the nuclear receptor LXR. Immunity 31:245–58

    PubMed  CAS  Google Scholar 

  96. Woo JM, Lin Z, Navab M, Van Dyck C, Trejo-Lopez Y et al (2010) Treatment with apolipoprotein A-1 mimetic peptide reduces lupus-like manifestations in a murine lupus model of accelerated atherosclerosis. Arthritis Res Ther 12:R93

    PubMed  Google Scholar 

  97. Shiraki M, Shiraki Y, Aoki C, Hosoi T, Inoue S et al (1997) Association of bone mineral density with apolipoprotein E phenotype. J Bone Miner Res 12:1438–45

    PubMed  CAS  Google Scholar 

  98. Gerdes LU, Vestergaard P, Hermann AP, Mosekilde L (2001) Regional and hormone-dependent effects of apolipoprotein E genotype on changes in bone mineral in perimenopausal women. J Bone Miner Res 16:1906–16

    PubMed  CAS  Google Scholar 

  99. Jouni ZE, McNamara DJ (1991) Lipoprotein receptors of HL-60 macrophages. Effect of differentiation with tetramyristic phorbol acetate and 1,25-didroxyvitamin D3. Arterioscler Thromb 11:995–1006

    PubMed  CAS  Google Scholar 

  100. Husain K, Suarez E, Isidro A, Ferder L (2010) Effects of paricalcitol and analapril on atherosclerotic injury in mouse aortas. Am J Nephrol 32:296–304

    PubMed  CAS  Google Scholar 

  101. Becker LE, Koleganova N, Piecha G, Noronha IL, Zeier M et al (2011) Effects of paricalcitol and calcitriol on aortic wall remodeling in uninephrectomized ApoE knockout mice. Am J Physiol Renal Physiol 300:F772–82

    PubMed  CAS  Google Scholar 

  102. Huebbe P, Nebel A, Siegert S, Moehring J, Boesch-Saadatmandi C et al (2011) APOE ε4 is associated with higher vitamin D levels in targeted replacement mice and humans. FASEB J 25:3262–70

    PubMed  CAS  Google Scholar 

  103. John WG, Noonan K, Mannan N, Boucher BJ (2005) Hypovitamin D is associated with reductions in serum apolipoprotein A-1 but not with fasting lipids in British Bangladeshis. Am J Clin Nutr 82:517–22

    PubMed  CAS  Google Scholar 

  104. Auwerx J, Bouillon R, Kesteloot H (1992) Relation between 25-hydroxyvitamin D3, apolipoprotein A-1, and high density lipoprotein cholesterol. Arterioscler Thromb 12:671–4

    PubMed  CAS  Google Scholar 

  105. Jorde R, Figenschau Y, Hutchinson M, Emaus N, Grimnes G (2010) High serum 25-hydroxyvitamin D concentrations are associated with a favorable serum lipid profile. Eur J Clin Nutr 64:1457–64

    PubMed  CAS  Google Scholar 

  106. Karhapää P, Pihlajamäki J, Pörsti I, Kastarinen M, Mustonen J et al (2010) Diverse associations of 25-hydroxyvitamin D and 1,25-dihydroxy-vitamin D with dyslipidaemias. J Intern Med 268:604–10

    PubMed  Google Scholar 

  107. Riek AE, Oh J, Bernal-Mizrachi C (2010) Vitamin D regulates macrophage cholesterol metabolism in diabetes. J Steroid Biochem Mol Biol 121:430–3

    PubMed  CAS  Google Scholar 

  108. Gupta AK, Sexton RC, Rudney H (1989) Effect of vitamin D3 derivatives on cholesterol synthesis and HMG-CoA reductase activity in cultured cells. J Lipid Res 30:379–386

    PubMed  CAS  Google Scholar 

  109. Wang J-H, Keisala T, Salakivi T, Minasyan A, Kalueff AV, Tuohimaa P (2009) Serum cholesterol and expression of ApoAI, LXRbeta and SREBP2 in vitamin D receptor knock-out mice. J Steroid Biochem Mol Biol 113:222–6

    PubMed  CAS  Google Scholar 

  110. Jiang W, Miyamoto T, Kakizawa T, Nishio S-I, Oiwa A et al (2006) Inhibition of LXRα signaling by vitamin D receptor: possible role of VDR in bile acid synthesis. Biochem Biophys Res Commun 351:176–84

    PubMed  CAS  Google Scholar 

  111. Papadimitraki ED, Choulaki C, Koutala E, Bertsias G, Tsatsanis C et al (2006) Expansion of toll-like receptor 9-expressing B cells in active systemic lupus erythematosus: implications for the induction and maintenance of the autoimmune process. Arthritis Rheum 54:3601–11

    PubMed  CAS  Google Scholar 

  112. Migita K, Miyashita T, Maeda Y, Nakamura M, Yatsuhashi H et al (2007) Toll-like receptor expression in lupus peripheral blood mononuclear cells. J Rheumatol 34:493–500

    PubMed  CAS  Google Scholar 

  113. Nakano S, Morimoto S, Suzuki J, Nozawa K, Amano H et al (2008) Role of pathogenic auto-antibody production by toll-like receptor 9 of B cells in active systemic lupus erythematosus. Rheumatology (Oxford) 47:145–9

    CAS  Google Scholar 

  114. Komatsuda A, Wakui H, Iwamoto K, Ozawa M, Togashi M et al (2008) Up-regulated expression of toll-like receptors mRNAs in peripheral blood mononuclear cells from patients with systemic lupus erythematosus. Clin Exp Immunol 152:482–7

    PubMed  CAS  Google Scholar 

  115. Patole PS, Pawar RD, Lech M, Zecher D, Schmidt H et al (2006) Expression and regulation of toll-like receptors in lupus-like immune complex glomerulonephritis of MRL-Fas(lpr) mice. Nephrol Dial Transplant 21:3062–73

    PubMed  CAS  Google Scholar 

  116. Lee YH, Lee HS, Choi SJ, Ji JD, Song GG (2012) Associations between TLR polymorphisms and systemic lupus erythematosus: a systematic review and meta-analysis. Clin Exp Rheumatol 30:262–5

    Google Scholar 

  117. Capolunghi F, Rosado MM, Cascioli S, Girolami E, Bordasco S et al (2010) Pharmacological inhibition of TLR9 activation blocks autoantibody production in human B cells from SLE patients. Rheumatology (Oxford) 49:2281–9

    CAS  Google Scholar 

  118. Pawar RD, Ramanjaneyulu A, Kulkarni OP, Lech M, Segerer S, Anders HJ (2007) Inhibition of toll-like receptor-7 (TLR-7) or TLR-7 plus TLR-9 attenuates glomerulonephritis and lung injury in experimental lupus. J Am Soc Nephrol 18:1721–31

    PubMed  CAS  Google Scholar 

  119. Barrat FJ, Meeker T, Chan JH, Guiducci C, Coffman RL (2007) Treatment of lupus-prone mice with a dual inhibitor of TLR7 and TLR9 leads to reduction of autoantibody production and amelioration of disease symptoms. Eur J Immunol 37:3582–6

    PubMed  CAS  Google Scholar 

  120. Roth CL, Elfers CT, Figlewicz DP, Melhorn SJ, Morton GJ, et al (2012) Vitamin D deficiency in obese rats exacerbates nonalcoholic fatty liver disease and increases hepatic resistin and Toll-like receptor activation. Hepatology 55:1103–11

    Google Scholar 

  121. Sadeghi K, Wessner B, Laggner U, Ploder M, Tamandl D et al (2006) Vitamin D3 down-regulates monocyte TLR expression and triggers hyporesponsiveness to pathogen-associated molecular patterns. Eur J Immunol 36:361–70

    PubMed  CAS  Google Scholar 

  122. Dickie L, Church L, Coulthard L, Mathews R, Emery P, McDermott M (2010) Vitamin D3 downregulates intracellular toll-like receptor 9 expression and toll-like receptor 9-induced IL-6 production in human monocytes. Rheumatol 48:1466–71

    Google Scholar 

  123. Liu PT, Stenger S, Li H, Wenzel L, Tan BH, Krutzik SR et al (2006) Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response. Science 311:1770–3

    PubMed  CAS  Google Scholar 

  124. Yim S, Dhawan P, Ragunath C, Christakos S, Diamond G (2007) Induction of cathelicidin in normal and CF bronchial epithelial cells by 1,25-dihydroxyvitamin D3. J Cys Fibros 6:403–410

    CAS  Google Scholar 

  125. Rivas-Santiago B, Hernandez-Pando R, Carranza C, Juarez E, Contreras JL et al (2008) Expression of cathelicidin LL-37 during Mycobacterium tuberculosis infection in human alveolar macrophages, monocytes, neutrophils, and epithelial cells. Infect Immun 76:935–41

    PubMed  CAS  Google Scholar 

  126. Sun CL, Zhang FZ, Li P, Bi LQ (2011) LL-37 expression in the skin in systemic lupus erythematosus. Lupus 20:904–11

    PubMed  CAS  Google Scholar 

  127. Ritterhouse LL, Crowe SR, Niewold TB, Kamen DL, Macwana SR et al (2011) Vitamin D deficiency is associated with an increased autoimmune response in healthy individuals and in patients with systemic lupus erythematosus. Ann Rheum Dis 70:1569–74

    PubMed  CAS  Google Scholar 

  128. Bogaczewicz J, Sysa-Jedrzejowska A, Arkuszewska C, Zabek J, Kontny E et al (2012) Vitamin D status in systemic lupus erythematosus patients and its association with selected clinical and laboratory parameters. Lupus 21:477–84

    Google Scholar 

  129. Reynolds JA, Haque S, Berry JL, Pemberton P, Teh LS et al (2012) 25-Hydroxyvitamin D deficiency is associated with increased aortic stiffness in patients with systemic lupus erythematosus. Rheumatology (Oxford) 51:544–51

    CAS  Google Scholar 

  130. Szodoray P, Tarr T, Bazso A, Poor G, Szegedi G, Kiss E (2011) The immunopathological role of vitamin D in patients with SLE: data from a single centre registry in Hungary. Scand J Rheumatol 40:122–6

    PubMed  CAS  Google Scholar 

  131. Bonakdar ZS, Jahanshahifar L, Jahanshahifar F, Gholamrezaei A (2011) Vitamin D deficiency and its association with disease activity in new cases of systemic lupus erythematosus. Lupus 20:1155–60

    PubMed  CAS  Google Scholar 

  132. Wright TB, Shults J, Leonard MB, Zemel BS, Burnham JM (2009) Hypovitaminosis D is associated with greater body mass index and disease activity in pediatric systemic lupus erythematosus. J Pediatr 155:260–5

    PubMed  CAS  Google Scholar 

  133. Chen S, Sims GP, Chen XX, Gu YY, Chen S, Lipsky PE (2007) Modulatory effects of 1,25-dihydroxyvitamin D3 on human B cell differentiation. J Immunol 179:1634–47

    PubMed  CAS  Google Scholar 

  134. Lemire JM, Archer DC (1991) 1,25-Dihydroxyvitamin D3 prevents the in vivo induction of murine experimental autoimmune encephalomyelitis. J Clin Invest 87:1103–7

    PubMed  CAS  Google Scholar 

  135. Cantorna MT, Hayes CE, DeLuca HF (1996) 1,25-Dihydroxyvitamin D3 reversibly blocks the progression of relapsing encephalomyelitis, a model of multiple sclerosis. Proc Natl Acad Sci U S A 93:7861–4

    PubMed  CAS  Google Scholar 

  136. Mathieu C, Waer M, Laureys J, Rutgeerts O, Bouillon R (1994) Prevention of autoimmune diabetes in NOD mice by 1,25 dihydroxyvitamin D3. Diabetologia 37:552–8

    PubMed  CAS  Google Scholar 

  137. Lemire JM, Ince A, Takashima M (1992) 1,25-Dihydroxyvitamin D3 attenuates the expression of experimental murine lupus of MRL/l mice. Autoimmunity 12:143–8

    PubMed  CAS  Google Scholar 

  138. Linker-Israeli M, Elstner E, Klinenberg JR, Wallace DJ, Koeffler HP (2001) Vitamin D3 and its synthetic analogs inhibit the spontaneous in vitro immunoglobulin production by SLE-derived PBMC. Clin Immunol 99:82–93

    PubMed  CAS  Google Scholar 

  139. Chong PJ, Matzner WL, Wallace DJ, Klinenberg JR, Toyoda M, Jordan SC (1989) 1,25 Dihydroxyvitamin-D3 regulation of immunoglobulin production in peripheral blood mononuclear cells of patients with systemic lupus erythematosus. J Autoimmun 2:861–7

    PubMed  CAS  Google Scholar 

  140. Lerman M, Burnham J, Behrens E (2011) 1,25 Dihydroxyvitamin D3 limits monocyte maturation in lupus sera. Lupus 20:749–53

    PubMed  CAS  Google Scholar 

  141. Abe J, Nakamura K, Takita Y, Nakano T, Irie H, Nishii Y (1990) Prevention of immunological disorders in MRL/l mice by a new synthetic analogue of vitamin D3: 22-oxa-1 alpha,25-dihydroxyvitamin D3. J Nutr Sci Vitaminol (Tokyo) 36:21–31

    CAS  Google Scholar 

  142. Ben-Zvi I, Aranow C, Mackay M, Stanevsky A, Kamen DL et al (2010) The impact of vitamin D on dendritic cell function in patients with systemic lupus erythematosus. PLoS One 5:e9193

    PubMed  Google Scholar 

  143. Hasan T, Pertovaara M, Yli-Kerttula U, Luukkaala T, Korpela M (2004) Seasonal variation of disease activity of systemic lupus erythematosus in Finland: a 1 year follow up study. Ann Rheum Dis 63:1498–500

    PubMed  CAS  Google Scholar 

  144. Haga HJ, Brun JG, Rekvig OP, Wetterberg L (1999) Seasonal variations in activity of systemic lupus erythematosus in a subarctic region. Lupus 8:269–73

    PubMed  CAS  Google Scholar 

  145. Léone J, Pennaforte JL, Delhinger V, Detour J, Lefondre K et al (1997) Influence of seasons on risk of flare-up of systemic lupus: retrospective study of 66 patients. Rev Med Interne 18:286–91 [Article in French]

    PubMed  Google Scholar 

  146. Terao C, Ohmura K, Yamamoto K, Yukawa N, Kawabata D et al (2012) Serum IgG levels demonstrate seasonal change in connective tissue diseases: a large-scale, 4-year analysis in Japanese. Mod Rheumatol 22:426–30

    Google Scholar 

  147. Van Nguyen H, Di Girolamo N, Jackson N, Hampartzoumian T, Bullpitt P et al (2011) Ultraviolet radiation-induced cytokines promote mast cell accumulation and matrix metalloproteinase production: potential role in cutaneous lupus erythematosus. Scand J Rheumatol 40:197–204

    PubMed  CAS  Google Scholar 

  148. Krause I, Shraga I, Molad Y, Guedj D, Weinberger A (1997) Seasons of the year and activity of SLE and Behcet’s disease. Scand J Rheumatol 26:435–9

    PubMed  CAS  Google Scholar 

  149. Szeto CC, Mok HY, Chow KM, Lee TC, Leung JY et al (2008) Climatic influence on the prevalence of noncutaneous disease flare in systemic lupus erythematosus in Hong Kong. J Rheumatol 35:1031–7

    PubMed  Google Scholar 

  150. Schlesinger N, Schlesinger M, Seshan SV (2005) Seasonal variation of lupus nephritis: high prevalence of class V lupus nephritis during the winter and spring. J Rheumatol 32:1053–7

    PubMed  Google Scholar 

  151. Hua-Li Z, Shi-Chao X, De-Shen T, Dong L, Hua-Feng L (2011) Seasonal distribution of active systemic lupus erythematosus and its correlation with meteorological factors. Clinics (Sao Paulo) 66:1009–13

    Google Scholar 

  152. Hanada K, Sawamura D, Hashimoto I (1995) Possible role of 1,25-dihydroxyvitamin D3-induced metallothionein in photoprotection against UVB injury in mouse skin and cultured rat keratinocytes. J Dermatol Sci 9:203–8

    PubMed  CAS  Google Scholar 

  153. Youn JI, Park BS, Chung JH, Lee JH (1997) Photoprotective of calcipotriol upon skin photoreaction to UVA and UVB. Photodermatol Photoimmunol Photo Med 13:109–14

    CAS  Google Scholar 

  154. Koshiishi I, Mitani H, Sumita T, Imanari T (2001) 1,25-Dihydroxyvitamin D3 prevents the conversion of adipose tissue into fibrous tissue in skin exposed to chronic UV irradiation. Toxicol Appl Pharmacol 173:99–104

    PubMed  CAS  Google Scholar 

  155. Damian DL, Kim YJ, Dixon KM, Halliday GM, Javeri A, Mason RS (2009) Topical calcitriol protects from UV-induced genetic damage but suppresses cutaneous immunity in humans. Exp Dermatol 19:e23–e30

    Google Scholar 

  156. Jiang Z, Sui T, Wang B (2010) Relationships between MMP-2, MMP-9, TIMP-1 and TIMP-2 levels and their pathogenesis in patients with lupus nephritis. Rheumatol Int 30:1219–26

    PubMed  CAS  Google Scholar 

  157. Chang YH, Lin IL, Tsay GJ, Yang SC, Yang TP et al (2008) Elevated circulatory MMP-2 and MMP-9 levels and activities in patients with rheumatoid arthritis and systemic lupus erythematosus. Clin Biochem 41:955–9

    PubMed  CAS  Google Scholar 

  158. Cai G, Chen X, Wang Z, Tian Y, Shi S (2002) Aging changes of gelatinase activity in kidney tissue of autoimmune MRL/lpr mice. Zhonghua Bing Li Xue Za Zhi 31:432–5 [Article in Chinese]

    PubMed  Google Scholar 

  159. Faber-Elmann A, Sthoeger Z, Tcherniack A, Dayan M, Mozes E (2002) Activity of matrix metalloproteinase-9 is elevated in sera of patients with systemic lupus erythematosus. Clin Exp Immunol 127:393–8

    PubMed  CAS  Google Scholar 

  160. Makowski GS, Ramsby ML (2003) Concentrations of circulating matrix metalloproteinase 9 inversely correlate with autoimmune antibodies to double stranded DNA: implications for monitoring disease activity in systemic lupus erythematosus. Mol Pathol 56:244–7

    PubMed  CAS  Google Scholar 

  161. Trysberg E, Blennow K, Zachrisson O, Tarkowski A (2004) Intrathecal levels of matrix metalloproteinases in systemic lupus erythematosus with central nervous system engagement. Arthritis Res Ther 6:R551–6

    PubMed  CAS  Google Scholar 

  162. Ainiala H, Hietaharju A, Dastidar P, Loukkola J, Lehtimäki T et al (2004) Increased serum matrix metalloproteinase 9 levels in systemic lupus erythematosus patients with neuropsychiatric manifestations and brain magnetic resonance imaging abnormalities. Arthritis Rheum 50:858–65

    PubMed  CAS  Google Scholar 

  163. Kotajima L, Aotsuka S, Fujimani M, Okawa-Takatsuji M et al (1998) Increased levels of matrix metalloproteinase-3 in sera from patients with active lupus nephritis. Clin Exp Rheumatol 16:409–15

    PubMed  CAS  Google Scholar 

  164. Cauwe B, Martens E, Sagaert X, Dillen C, Geurts N et al (2011) Deficiency of gelatinase B/MMP-9 aggravates lpr-induced lymphoproliferation and lupus-like systemic autoimmune disease. J Autoimmun 36:239–52

    PubMed  CAS  Google Scholar 

  165. Lee YJ, Woo M, Nam JH, Baek J, Im CH et al (2008) Matrix metalloproteinase-9 promoter polymorphisms in Korean patients with systemic lupus erythematosus. Hum Immunol 69:374–9

    PubMed  CAS  Google Scholar 

  166. Lesiak A, Narbutt J, Sysa-Jedrzejowska A, Lukamowicz J, McCauliffe DP, Wózniacka A (2010) Effect of chloroquine phosphate treatment on serum MMP-9 and TIMP-1 levels in patients with systemic lupus erythematosus. Lupus 19:683–8

    PubMed  CAS  Google Scholar 

  167. Faber-Elmann A, Eilat E, Zinger H, Mozes E (2002) A peptide based on an anti-DNA autoantibody downregulates matrix metalloproteinases in murine models of lupus. Clin Immunol 105:223–32

    PubMed  CAS  Google Scholar 

  168. Zhang HY, Bao SM, Shou WL, Luan HX, Zhang Y et al (2009) Expression of matrix metalloproteinase-1 mRNA in peripheral blood mononuclear cells of systemic lupus erythematosus patients and its relationship with atherosclerosis. Chin Med J (Engl) 122:2593–7

    CAS  Google Scholar 

  169. Bahrehmand F, Vaisi-Raygani A, Kiani A, Rahimi Z, Tavilani H, et al (2012) Matrix metalloproteinase-2 functional promoter polymorphism G1575A is associated with elevated circulatory MMP-2 levels and increased risk of cardiovascular disease in systemic lupus erythematosus patients. Lupus 21:616–24

    Google Scholar 

  170. Järvinen TM, Kanninen P, Jeskanen L, Koskenmies S, Panelius J et al (2007) Matrix metalloproteinases as mediators of tissue injury in different forms of cutaneous lupus erythematosus. Br J Dermatol 157:970–80

    PubMed  Google Scholar 

  171. Sundar I, Hwang J, Wu S, Sun J, Rahman I (2011) Deletion of vitamin D receptor leads to premature emphysema/COPD by increased matrix metalloproteinase and lymphoid aggregates formation. Biochem Biophys Res Commun 406:127–33

    PubMed  CAS  Google Scholar 

  172. Timms PM, Mannan N, Hitman GA, Noonan K, Mills PG et al (2002) Circulating MMP9, vitamin D and variation in the TIMP-1 response with VDR genotype: mechanisms for inflammatory damage in chronic disorders? Q J Med 95:787–96

    CAS  Google Scholar 

  173. Dean DD, Schwartz Z, Schmitz J, Muniz OE, Lu Y et al (1996) Vitamin D regulation of metalloproteinase activity in matrix vesicles. Connect Tissue Res 35:331–6

    PubMed  CAS  Google Scholar 

  174. Bahar-Shany K, Ravid A, Koren R (2010) Upregulation of MMP-production by TNFalpha in keratinocytes and its attenuation by vitamin D. J Cell Physiol 222:729–37

    PubMed  CAS  Google Scholar 

  175. Lacraz S, Dayer J, Nicod L, Welgus H (1994) 1,25-Dihydroxyvitamin D3 dissociates production of interstitial collagenase and 92-kDa gelatinase in human mononuclear phagocytes. J Biol Chem 269:6485–90

    PubMed  CAS  Google Scholar 

  176. Nakagawa K, Sasaki Y, Kato S, Kubodera N, Okano T (2005) 22-Oxa-1α,25-dihydroxyvitamin D3 inhibits metastasis and angiogenesis in lung cancer. Carcinogenesis 26:1044–54

    PubMed  CAS  Google Scholar 

  177. Coussens A, Timms P, Boucher B, Venton T, Ashcroft A et al (2009) 1α,25-Dihydroxyvitamin D3 inhibits matrix metalloproteinases induced by Mycobacterium tuberculosis infection. Immunology 127:539–48

    PubMed  CAS  Google Scholar 

  178. Anand S, Selvaraj P (2009) Effect of 1, 25 dihydroxyvitamin D3 on matrix metalloproteinases MMP-7, MMP-9 and the inhibitor TIMP-1 in pulmonary tuberculosis. Clin Immunol 133:126–31

    Google Scholar 

  179. Tetlow L, Woolley D (2001) Expression of vitamin D receptors and matrix metalloproteinases in osteoarthritic cartilage and human articular chondrocytes in vitro. Osteoarthr Cartil 9:423–31

    PubMed  CAS  Google Scholar 

  180. Takahashi T, Morita K, Akagi R, Sassa S (2004) Protective role of heme oxygenase-1 in renal ischemia. Antioxid Redox Signal 6:867–77

    PubMed  CAS  Google Scholar 

  181. Takahashi A, Mori M, Naruto T, Nakajima S, Miyamae T et al (2009) The role of heme oxygenase-1 in systemic-onset juvenile idiopathic arthritis. Mod Rheumatol 19:302–8

    PubMed  CAS  Google Scholar 

  182. Avihingsanon Y, Benjachat T, Tassanarong A, Sodsai P, Kittikovit V, Hirankarn N (2009) Decreased renal expression of vascular endothelial growth factor in lupus nephritis is associated with worse prognosis. Kidney Int 75:1340–8

    PubMed  CAS  Google Scholar 

  183. Datta PK, Koukouritaki SB, Hopp KA, Lianos EA (1999) Heme oxygenase-1 induction attenuates inducible nitric oxide synthase expression and proteinuria in glomerulonephritis. J Am Soc Nephrol 10:2540–50

    PubMed  CAS  Google Scholar 

  184. Takeda Y, Takeno M, Iwasaki M, Kobayashi H, Kirino Y et al (2004) Chemical induction of HO-1 suppresses lupus nephritis by reducing local iNOS expression and synthesis of anti-dsDNA antibody. Clin Exp Immunol 138:237–44

    PubMed  CAS  Google Scholar 

  185. Shih PK, Chen YC, Huang YC, Chang YT, Chen JX, Cheng CM (2011) Pretreatment of vitamin D3 ameliorates lung and muscle injury induced by reperfusion of bilateral femoral vessels in a rat model. J Surg Res 171:323–8

    PubMed  CAS  Google Scholar 

  186. Oermann E, Bidmon H-J, Witte O-W, Zilles K (2004) Effects of 1α,25-didroxyvitamin D3 on the expression of HO-1 and GFAP in glial cells of the photothrombotically lesioned cerebral cortex. J Chem Neuroanat 28:225–38

    PubMed  CAS  Google Scholar 

  187. Tomasoni S, Noris M, Zappella S, Gotti E, Casiraghi F et al (1998) Upregulation of renal and systemic cyclooxygenase-2 in patients with active lupus nephritis. J Am Soc Nephrol 9:1202–12

    PubMed  CAS  Google Scholar 

  188. Menè P, Pecci G, Cinotti GA, Pugliese G, Pricci F, Pugliese F (1998) Eicosanoid synthesis in peripheral blood monocytes: a marker of disease activity in lupus nephritis. Am J Kidney Dis 32:778–84

    PubMed  Google Scholar 

  189. Habib A, Martinuzzo ME, Carreras LO, Lévy-Toledano S, Maclouf J (1995) Increased expression of inducible cyclooxygenase-2 in human endothelial cells by antiphospholipid antibodies. Thromb Haemost 74:770–7

    PubMed  CAS  Google Scholar 

  190. Yang P, Zhang Y, Ping L, Gao XM (2007) Apoptosis of murine lupus T cells induced by the selective cyclooxygenase-2 inhibitor celecoxib: molecular mechanisms and therapeutic potential. Int Immunopharmacol 7:1414–21

    PubMed  CAS  Google Scholar 

  191. Zhang L, Bertucci AM, Smith KA, Xu L, Datta SK (2007) Hyperexpression of cyclooxygenase 2 in the lupus immune system and effect of cyclooxygenase 2 inhibitor diet therapy in a murine model of systemic lupus erythematosus. Arthritis Rheum 56:4132–41

    PubMed  CAS  Google Scholar 

  192. Kimberly RP, Gill JR Jr, Bowden RE, Keiser HR, Plotz PH (1978) Elevated urinary prostaglandins and the effects of aspirin on renal function in lupus erythematosus. Ann Intern Med 89:336–41

    PubMed  CAS  Google Scholar 

  193. Fan PY, Ruiz P, Pisetsky DS, Spurney RF (1995) The effects of short-term treatment with the prostaglandin E1 (PGE1) analog misoprostol on inflammatory mediator production in murine lupus nephritis. Clin Immunol Immunopathol 75:125–30

    PubMed  CAS  Google Scholar 

  194. Ambrus JL Jr, Contractor V, Joseph A, Long J, Blumenthal D (1995) A potential role for PGE and IL-14 (HMW-BCGF) in B-cell hyperactivity of patients with systemic lupus erythematosus. Am J Ther 2:933–942

    PubMed  Google Scholar 

  195. Nagayama Y, Namura Y, Tamura T, Muso R (1988) Beneficial effect of prostaglandin E1 in three cases of lupus nephritis with nephrotic syndrome. Ann Allergy 61:289–95

    PubMed  CAS  Google Scholar 

  196. Moreno J, Krishnan AV, Swami S, Nonn L, Peehl DM, Feldman D (2005) Regulation of prostaglandin metabolism by calcitriol attenuates growth stimulation in prostate cancer cells. Cancer Res 65:7917–25

    PubMed  CAS  Google Scholar 

  197. Aparna R, Subhashini J, Roy KR, Reddy GS, Robinson M et al (2008) Selective inhibition of cyclooxygenase-2 (COX-2) by 1alpha,25-dihydroxy16-ene-yne-vitamin D3, a less calcemic vitamin D analog. J Cell Biochem 104:1832–42

    PubMed  CAS  Google Scholar 

  198. Thill M, Hoellen F, Becker S, Dittmer C, Fischer D et al (2012) Expression of prostaglandin- and vitamin D-metabolising enzymes in benign and malignant breast cells. Anticancer Res 32:367–72

    PubMed  CAS  Google Scholar 

  199. Cordes T, Hoellen F, Dittmer C, Salehin D, Kümmel S et al (2012) Correlation of prostaglandin metabolizing enzymes and serum PGE2 levels with vitamin D receptor and serum 25(OH)2D3 levels in breast and ovarian cancer. Anticancer Res 32:351–7

    PubMed  CAS  Google Scholar 

  200. Zhang Q, Ye DQ, Chen GP, Zheng Y (2010) Oxidative protein damage and antioxidant status in systemic lupus erythematosus. Clin Exp Dermatol 35:287–94

    PubMed  CAS  Google Scholar 

  201. Shingu M, Oribe M, Todoroki T, Tatsukawa K, Tomo-oka K et al (1983) Serum factors from patients with systemic lupus erythematosus enhancing superoxide generation by normal neutrophils. J Invest Dermatol 81:212–5

    PubMed  CAS  Google Scholar 

  202. Sato T (1991) Role of active oxygen on the progression of murine lupus nephritis. Nihon Jinzo Gakkai Shi 33:239–46

    PubMed  CAS  Google Scholar 

  203. Jiang X, Chen F (1992) The effect of lipid peroxides and superoxide dismutase on systemic lupus erythematosus: a preliminary study. Clin Immunol Immunopathol 63:39–44

    PubMed  CAS  Google Scholar 

  204. Belmont HM, Levartovsky D, Goel A, Amin A, Giorno R et al (1997) Increased nitric oxide production accompanied by the up-regulation of inducible nitric oxide synthase in vascular endothelium from patients with systemic lupus erythematosus. Arthritis Rheum 40:1810–6

    PubMed  CAS  Google Scholar 

  205. Cohen MS, Mesler DE, Snipes RG, Gray TK (1986) 1α-Dihydroxyvitamin D3 activates secretion of hydrogen peroxide by human monocytes. J Immunol 136:1049–53

    PubMed  CAS  Google Scholar 

  206. Levy R, Malech H (1991) Effect of 1α-dihydroxyvitamin D3, lipoxysaccharide, or lipoteichoic acid on the expression of NADPH oxidase components in cultured human monocytes. J Immunol 147:3066–71

    PubMed  CAS  Google Scholar 

  207. Bao BY, Ting HJ, Hsu JW, Lee YF (2008) Protective role of 1α-dihydroxyvitamin D3 against oxidative stress in nonmalignant human prostate epithelial cells. Int J Cancer 122:2699–706

    PubMed  CAS  Google Scholar 

  208. Somjen D, Katzburg S, Grafi-Cohen M, Knoll E, Sharon O, Posner GH (2011) Vitamin D metabolites and analogs induce lipoxygenase mRNA expression and as well as reactive oxygen species (ROS) production in human bone cell line. J Steroid Biochem Mol Biol 123:85–9

    PubMed  CAS  Google Scholar 

  209. Sardar S, Chakraborty A, Chatterjee M (1996) Comparative effectiveness of vitamin D3 and dietary vitamin E on peroxidation of lipids and enzymes of the hepatic antioxidant system in Sprague-Dawley rats. Int J Vitam Nutr Res 66:39–45

    PubMed  CAS  Google Scholar 

  210. Chang J, Kuo M, Kuo H, Hwang S, Tsai J et al (2004) 1 Alpha,25-hydroxyvitamin D3 regulates inducible nitric oxide synthase messenger RNA expression and nitric oxide release in macrophage-like RAW 264.7 cells. J Lab Clin Med 143:14–22

    PubMed  CAS  Google Scholar 

  211. Equils O, Naiki Y, Shapiro AM, Michelsen K, Lu D et al (2005) 1,25-Hydroxyvitamin D3 inhibits liposaccharide-induced immune activation in human endothelial cells. Clin Exp Immunol 143:58–64

    Google Scholar 

  212. Garcion E, Sindji L, Leblondel G, Brachet P, Darcy F (1999) 1,25-Hydroxyvitamin D3 regulates the synthesis of γ-glutamyl transpeptidase and glutathione levels in rat primary astrocytes. J Neurochem 73:859–66

    PubMed  CAS  Google Scholar 

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    Khanh vinh quốc Lương & Lan Thi Hoàng Nguyễn

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vinh quốc Lương, K., Nguyễn, L.T.H. The beneficial role of vitamin D in systemic lupus erythematosus (SLE). Clin Rheumatol 31, 1423–1435 (2012). https://doi.org/10.1007/s10067-012-2033-1

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