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[1]Lee HT, Shiao YM, Wu TH,Chen WS, Hsu YH, Tsai SF, and Tsai CY. Serum BLC/CXCL13 concentrations and renal expression of CXCL13/CXCR5 in patients with systemic lupus erythematosus and lupus nephritis. J. Rheumatol. 37:45-52 (2010)
[2]Su DL, Lu ZM, Shen MN, Li X, and Sun LY. Roles of pro-and anti-inflammatory cytokines in the pathogenesis of SLE. J. Biomed. Biotechnol. 347141 (2012)
[3]Ohl K, and Tenbrock K. Inflammatory cytokines in systemic lupus erythematosus. J. Biomed. Biotechnol. 432595 (2011)
[4]Lourenco EV, and la Cava A. Cytokines in systemic lupus erythematosus. Curr. Mol. Med. 9:242-254 (2009)
[5]Yu SL, Kuan WP, Wong CK, Li EK, and Tam LS. Immunopathological roles of cytokines, chemokines, signaling molecules, and pattern-recognition receptors in systemic lupus erythematosus. Clin. Dev. Immunol. 715190 (2012)
[6]Crow MK. Type I interferon in the pathogenesis of lupus. J. Immunol. 192:5459-5468 (2014)
[7]Dall’era MC, Cardarelli PM, Preston BT, Witte A, and Davis JC Jr. Type I interferon correlates with serological and clinical manifestations of SLE. Ann. Rheum. Dis. 64:1692-1697 (2005)
[8]Moore KW, de Waal Malefyt R, Coffman RL, and O’Garra A. Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19:683-765 (2001)
[9]Kasama T, Strieter RM, Lukacs NW, Burdick MD, and Kunkel SL. Regulation of neutrophil-derived chemokine expression by IL-10. J. Immunol. 152:3559-3569(1994)
[10]Schuetze N, Schoeneberger S, Mueller U, Freudenberg MA, Alber G, and Straubinger RK. IL-12 family members: differential kinetics of their TLR4-mediated induction by Salmonella enteritidis and the impact of IL-10 in bone marrow-derived macrophages. Int. Immunol. 17:649-659 (2005)
[11]Llorente L, Zou W, Levy Y, Wijdenes J, Alcocer-Varela J, Morel-Fourrier B, Brouet JC, Alarcon-Segovia D, Galanaud P, and Emilie D. Role of interleukin 10 in the B lymphocyte hyperactivity and autoantibody production of human systemic lupus erythematosus. J. Exp. Med. 181:839-844 (1995)
[12]Chun HY, Chung JW, Kim HA,Yun JM, Jeon JY, Ye YM, Kim SH, Park HS, and Suh CH. Cytokine IL-6 and IL-10 as biomarkers in systemic lupus erythematosus. J. Clin. Immunol. 27:461-466 (2007)
[13]Mills KH. Induction, function and regulation of IL-17-producing T cells. Eur. J. Immunol. 38:2636-2649 (2008)
[14]Jin W, and Dong C. IL-17 cytokines in immunity and inflammation. Emerg. Microbes Infect. 2:e60 (2013)
[15]Chen DY, Chen YM, Wen MC, Hsieh TY, Hung WT, and Lan JL. The potential role of Th17 cells and Th17-related cytokines in the pathogenesis of lupus nephritis. Lupus 21:1385-1396 (2012)
[16]Wong CK, Lit LC, Tam LS, Hsieh TY, Hung WT, and Lan JL. Hyperproduction of IL-23 and IL-17 in patients with systemic lupus erythematosus: implications for Th17-mediated inflammation in auto-immunity. Clin. Immunol. 127:385-393 (2008)
[17]Ronnblom L, Eloranta ML, and Alm GV. The type I interferon system in systemic lupus erythematosus. Arthritis Rheum. 54:408-420 (2006)
[18]Manoharan A, and Madaio MP. Biomarkers in lupus nephritis. Rheum. Dis. Clin. North Am. 36:131-143, ix (2010)
[19]Bennett M, and Brunner HI. Biomarkers and updates on pediatrics lupus nephritis. Rheum.Dis. Clin. North Am. 39:833-853 (2013)
[20]Abujam B, Cheekatla S, and Aggarwal A. Urinary CXCL-10/IP-10 and MCP-1 as markers to assess activity of lupus nephritis. Lupus 22:614-623 (2013)
[21]Morimoto S, Tokano Y, Nakano S,Watanabe T, Tamayama Y, Mitsuo A, Suzuki J, Kaneko H, Sekigawa I, and Takasaki Y. Chemoattractant mechanism of Th1 cells in class III and IV lupus nephritis. Autoimmunity42:143-149(2009)
[22]Watson L, Tullus K, Pilkington C, Chesters C, Marks SD, Newland P, Jones CA, and Beresford MW. Urine biomarkers for monitoring juvenile lupus nephritis: a prospective longitudinal study. Pediatr. Nephrol. 29:397-405 (2014)
[23]Shah D, Wanchu A, and Bhatnagar A. Interaction between oxidative stress and chemokines: possible pathogenic role in systemic lupus erythematosus and rheumatoid arthritis. Immunobiology 216:1010-1017 (2011)
[24]Shah D, Kiran R, Wanchu A, and Bhatnagar A. Oxidative stress in systemic lupus erythematosus: relationship to Th1 cytokine and disease activity. Immunol. Lett. 129:7-12 (2010)
[25]Perl A, Hanczko R, and Doherty E. Assessment of mitochondrial dysfunction in lymphocytes of patients with systemic lupus erythematosus. Meth. Mol. Biol. 900:61-89 (2012)
[26]Li KJ, Wu CH, Hsieh SC, Lu MC, Tsai CY, and Yu CL. Deranged bioenergetics and defective redox capacity in T lymphocytes and neutrophils are related to cellular dysfunction and increased oxidative stress in patients with active systemic lupus erythematosus. Clin. Dev. Immunol. 2012:548516 (2012)
[27]Domann FE. Aberrant free radical biology is a unifying theme in the etiology and pathogenesis of major human diseases. Int. J. Mol. Sci. 14:8491-8495 (2013)
[28]Lee HT, Lin CS, Lee CS, and Tsai CY, and Wei YH. Increased 8-hydroxy-2’-deoxyguanosine in plasma and decreased mRNA expression of human 8-oxoguanine DNA glycosylase 1, antioxidant enzymes, mitochondrial biogenesis-related proteins and glycolytic enzymes in leucocytes in patients with systemic lupus erythematosus. Clin. Exp. Immunol. 176:66-77 (2014)
[29]Lee HT, Lin CS, Chen WS, Liao HT, Tsai CY, and Wei YH. Leukocyte mitochondrial DNA alteration in systemic lupus erythematosus and its relevance to the susceptibility to lupus nephritis. Int. J. Mol. Sci. 13:8853-8868 (2012)
[30]Hochberg MC. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 40:1725 (1997)
[31]Petri M, Orbai AM, Alarcon GS,Gordon C, Merrill JT, Fortin PR, Bruce IN, Isenberg D, Wallace DJ, Nived O, Sturfelt G, Ramsey-Goldman R, Bae SC, Hanly JG, Sánchez-Guerrero J, Clarke A, Aranow C, Manzi S, Urowitz M, Gladman D, Kalunian K, Costner M, Werth VP, Zoma A, Bernatsky S, Ruiz-Irastorza G, Khamashta MA, Jacobsen S, Buyon JP, Maddison P, Dooley MA, van Vollenhoven RF, Ginzler E, Stoll T, Peschken C, Jorizzo JL, Callen JP, Lim SS, Fessler BJ, Inanc M, Kamen DL, Rahman A, Steinsson K, Franks AG Jr, Sigler L, Hameed S, Fang H, Pham N, Brey R, Weisman MH, McGwin G Jr, and Magder LS. Derivation and validation of the Systemic Lupus International Collaborating Clinics classification criteria for systemic lupus erythematosus. Arthritis Rheum. 64:2677-2686 (2012)
[32]Sato T, Takeda H, Otake S, Yokozawa J, Nishise S, Fujishima S, Orii T, Fukui T, Takano J, Sasaki Y, Nagino K, Iwano D, Yaoita T, and Kawata S. Increased plasma levels of 8-hydroxydeoxyguanosine are associated with development of colorectal tumors. J. Clin. Biochem. Nutr. 47:59-63 (2010)
[33]Wu CW, Yin PH, Hung WY, Li AF, Li SH, Chi CW, Wei YH, and Lee HC. Mitochondrial DNA mutations and mitochondrial DNA depletion in gastric cancer. Genes Chromosomes Cancer. 44:19-28(2005).
[34]Yu L, Zhou Y, Jiang Y, Tong W, Yang S, Gao F, Wang K, Li L, Xia T, Cheng Q, and Tong G. Construction and in vitro evaluation of a recombinant live attenuated PRRSV expressing GM-CSF. Virol. J. 11:201 (2014)
[35]Mok CC. Current role of rituximab in systemic lupus erythematosus. Int. J. Rheum. Dis.18:154-163 (2015)
[36]Carr MW, Roth SJ, Luther E, Rose SS, and Springer TA. Monocyte chemoattractant protein 1 acts as a T-lymphocyte chemoattractant. Proc. Natl. Acad. Sci. USA. 91:3652-3656 (1994)
[37]Xu LL, Warren MK, Rose WL, Gong W, and Wang JM. Human recombinant monocyte chemotactic protein and other C-C chemokines bind and induce directional migration of dendritic cells in vitro. J. Leuk. Biol. 6:365-371(1996)
[38]Dufour JH, Dziejman M, Liu MT, Leung JH, Lane TE, and Luster AD. IFN-gamma-inducible protein 10 (IP-10; CXCL10)-deficient mice reveal a role for IP-10 in effector T cell generation and trafficking. J. Immunol. 168:3195–3204 (2002)
[39]Angiolillo AL, Sgadari C, Taub DD, Liao F, Farber JM, Maheshwari S, Kleinman HK, Reaman GH, and Tosato G. Human interferon-inducible protein 10 is a potent inhibitor of angiogenesis in vivo. J. Exp. Med. 182:155–162(1995) is. Nephrol. Dial. Transplant. 26:3273-3280(2011)
[40]Adhya Z, Borozdenkova S, and Karim M.Y. The role of cytokines as biomarkersin systemic lupus erythematosus and lupus nephritis. Nephrol. Dial. Transplant. 26:3273-3280 (2011)
[41]Iwata Y, Furuichi K, Kaneko S, and Wada T. The role of cytokine in the lupus nephritis. J. Biomed. Biotechnol. 2011:594809 (2011)
[42]Mok MY, Wu HJ, Lo Y, and Lau CS. The relation of interleukin 17 (IL-17) and IL-23 to Th1/Th2 cytokines and disease activity in systemic lupus erythematosus. J. Rheumatol. 37:2046-2052 (2010)
[43]Park SJ, Kim JH, Ha TS, and Shin JI.The role ofinterleukin-23/interleukin-17 axis in coexisting anti-glomerular basement membrane disease and lupus nephritis. Saudi J. Kidney Dis. Transpl. 24:596-597 (2013)
[44]Zhang Z, Kyttaris VC, and Tsokos GC. The role of IL-23/IL-17 axis in lupus nephritis. J. Immunol. 183:3160-3169 (2009)
[45]Aggarwal S, and Gurney AL. IL-17: prototype member of an emerging cytokine family. J. Leuk. Biol. 71:1–8(2002)
[46]Gaffen SL. An overview of IL-17 function and signaling. Cytokine 43:402-407 (2008)
[47]Shah D, Sah S, Wanchu A, Wu MX, and Bhatnagar A. Altered redox state and apoptosis in the pathogenesis of systemic lupus erythematosus. Immunobiology 218:620-627 (2013)
[48]Mambo E, Gao X, Cohen Y, Guo Z, Talalay P, and Sidransky D. Electrophile and oxidant damage of mitochondrial DNA leading to rapid evolution of homoplasmic mutations. Proc. Natl. Acad. Sci. USA 100:1838-1843 (2003)
[49]Lee HC and Wei YH. Mitochondria and aging. Adv. Exp. Med. Biol. 942:311-327 (2012)
[50]Li X, Fang P, Mai J, Choi ET, Wang H, and Yang XF. Targeting mitochondrial reactive oxygen species as novel therapy for inflammatory diseases and cancers. J. Hematol. Oncol. 6:1-19 (2013)
[51]Sonoda J, Laganiere J, Mehl IR,Barish GD, Chong LW, Li X, Scheffler IE, Mock DC, Bataille AR, Robert F, Lee CH, Giguère V, and Evans RM. Nuclear receptor ERR α and coactivator PGC-1 β are effectors of IFN-γ-induced host defense. Genes Dev. 21:1909-1920 (2007)
[52]Perl A, Gergely P Jr, Nagy G, Koncz A, and Banki K. Mitochondrial hyperpolarization: a checkpoint of T-cell life, death and autoimmunity. Trends Immunol. 25:360-367 (2004)
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Frontiers in Bioscience-Landmark (FBL) is published by IMR Press from Volume 26 Issue 5 (2021). Previous articles were published by another publisher on a subscription basis, and they are hosted by IMR Press on imrpress.com as a courtesy and upon agreement with Frontiers in Bioscience.
Oxidative DNA and mitochondrial DNA change in patients with SLE
1 Division of Allergy, Immunology & Rheumatology, Department of Internal Medicine, Mackay Memorial Hospital, Taipei, Taiwan
2 Mackay Junior College of Medicine, Nursing, and Management, New Taipei City, Taiwan
3 Department of Medicine, Mackay Medical College, New Taipei City, Taiwan
4 Institute of Biochemistry and Molecular Biology, National Yang-Ming University, Taipei, Taiwan
5 Faculty of Medicine, National Yang-Ming University, Taipei, Taiwan
6 Division of Thoracic Surgery, Feng-Yuan Hospital, Ministry of Health and Welfare, Taichung City, Taiwan
7 Division of Nephrology, Taipei Veterans General Hospital, Taipei, Taiwan
8 Division of Allergy, Immunology and Rheumatology, Taipei Veterans General Hospital, Taipei, Taiwan
Abstract
We evaluated plasma IL-10, IFN-alpha, IL-23, IFN-gamma, IP-10, MCP-1, 8-OHdG, leukocyte mtDNA, serum anti-dsDNA antibodies and disease activity index (SLEDAI) in SLE patients. 93 patients (35 nephritis, 4 under dialysis, 5 under rituximab) and 50 healthy controls were recruited. Compared with healthy controls, SLE patients had higher IL-10, IFN-alpha, IL-23, IFN-γ, IP-10 and MCP-1 (p<0.05). High IFN-alpha (p=0.031) and IP-10 (p=0.026) correlated with high SLEDAI; high IFN-alpha (p<0.001), IL-23 (p=0.023) and IP-10 (p<0.001) correlated with high anti-dsDNA. High IL-10 (p=0.014), IL-23 (p<0.001), IFN-gamma (p<0.001) and MCP-1 (p=0.002) correlated with high 8-OHdG and high IL-23 (p<0.001), INF-gamma (p<0.001), IP-10 (p=0.023) and MCP-1 (p=0.002) correlated with low leukocyte mtDNA. mtDNA 4977 deletion correlated with high mtDNA (p=0.011) and low IL-10 (p=0.009). MCP-1 (p=0.043) decreased after rituximab therapy. 54 SLE patients without nephritis, 35 with nephritis but without dialysis, and 4 with nephritis under dialysis exhibited stepwise increases in IL-23 (p=0.009) and MCP-1 (p=0.015). These data suggest that oxidative DNA and mtDNA alterations and coordinate changes in cytokines/chemokines are implicated in progression of SLE and rituximab in amelioration of SLE.
Keywords
- Systemic Lupus Erythematosus
- Interleukin
- Interferon
- Chemokine
- Mitochondrial DNA
- Oxidative Stress
References
- [1] Lee HT, Shiao YM, Wu TH,Chen WS, Hsu YH, Tsai SF, and Tsai CY. Serum BLC/CXCL13 concentrations and renal expression of CXCL13/CXCR5 in patients with systemic lupus erythematosus and lupus nephritis. J. Rheumatol. 37:45-52 (2010)
- [2] Su DL, Lu ZM, Shen MN, Li X, and Sun LY. Roles of pro-and anti-inflammatory cytokines in the pathogenesis of SLE. J. Biomed. Biotechnol. 347141 (2012)
- [3] Ohl K, and Tenbrock K. Inflammatory cytokines in systemic lupus erythematosus. J. Biomed. Biotechnol. 432595 (2011)
- [4] Lourenco EV, and la Cava A. Cytokines in systemic lupus erythematosus. Curr. Mol. Med. 9:242-254 (2009)
- [5] Yu SL, Kuan WP, Wong CK, Li EK, and Tam LS. Immunopathological roles of cytokines, chemokines, signaling molecules, and pattern-recognition receptors in systemic lupus erythematosus. Clin. Dev. Immunol. 715190 (2012)
- [6] Crow MK. Type I interferon in the pathogenesis of lupus. J. Immunol. 192:5459-5468 (2014)
- [7] Dall’era MC, Cardarelli PM, Preston BT, Witte A, and Davis JC Jr. Type I interferon correlates with serological and clinical manifestations of SLE. Ann. Rheum. Dis. 64:1692-1697 (2005)
- [8] Moore KW, de Waal Malefyt R, Coffman RL, and O’Garra A. Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19:683-765 (2001)
- [9] Kasama T, Strieter RM, Lukacs NW, Burdick MD, and Kunkel SL. Regulation of neutrophil-derived chemokine expression by IL-10. J. Immunol. 152:3559-3569(1994)
- [10] Schuetze N, Schoeneberger S, Mueller U, Freudenberg MA, Alber G, and Straubinger RK. IL-12 family members: differential kinetics of their TLR4-mediated induction by Salmonella enteritidis and the impact of IL-10 in bone marrow-derived macrophages. Int. Immunol. 17:649-659 (2005)
- [11] Llorente L, Zou W, Levy Y, Wijdenes J, Alcocer-Varela J, Morel-Fourrier B, Brouet JC, Alarcon-Segovia D, Galanaud P, and Emilie D. Role of interleukin 10 in the B lymphocyte hyperactivity and autoantibody production of human systemic lupus erythematosus. J. Exp. Med. 181:839-844 (1995)
- [12] Chun HY, Chung JW, Kim HA,Yun JM, Jeon JY, Ye YM, Kim SH, Park HS, and Suh CH. Cytokine IL-6 and IL-10 as biomarkers in systemic lupus erythematosus. J. Clin. Immunol. 27:461-466 (2007)
- [13] Mills KH. Induction, function and regulation of IL-17-producing T cells. Eur. J. Immunol. 38:2636-2649 (2008)
- [14] Jin W, and Dong C. IL-17 cytokines in immunity and inflammation. Emerg. Microbes Infect. 2:e60 (2013)
- [15] Chen DY, Chen YM, Wen MC, Hsieh TY, Hung WT, and Lan JL. The potential role of Th17 cells and Th17-related cytokines in the pathogenesis of lupus nephritis. Lupus 21:1385-1396 (2012)
- [16] Wong CK, Lit LC, Tam LS, Hsieh TY, Hung WT, and Lan JL. Hyperproduction of IL-23 and IL-17 in patients with systemic lupus erythematosus: implications for Th17-mediated inflammation in auto-immunity. Clin. Immunol. 127:385-393 (2008)
- [17] Ronnblom L, Eloranta ML, and Alm GV. The type I interferon system in systemic lupus erythematosus. Arthritis Rheum. 54:408-420 (2006)
- [18] Manoharan A, and Madaio MP. Biomarkers in lupus nephritis. Rheum. Dis. Clin. North Am. 36:131-143, ix (2010)
- [19] Bennett M, and Brunner HI. Biomarkers and updates on pediatrics lupus nephritis. Rheum.Dis. Clin. North Am. 39:833-853 (2013)
- [20] Abujam B, Cheekatla S, and Aggarwal A. Urinary CXCL-10/IP-10 and MCP-1 as markers to assess activity of lupus nephritis. Lupus 22:614-623 (2013)
- [21] Morimoto S, Tokano Y, Nakano S,Watanabe T, Tamayama Y, Mitsuo A, Suzuki J, Kaneko H, Sekigawa I, and Takasaki Y. Chemoattractant mechanism of Th1 cells in class III and IV lupus nephritis. Autoimmunity42:143-149(2009)
- [22] Watson L, Tullus K, Pilkington C, Chesters C, Marks SD, Newland P, Jones CA, and Beresford MW. Urine biomarkers for monitoring juvenile lupus nephritis: a prospective longitudinal study. Pediatr. Nephrol. 29:397-405 (2014)
- [23] Shah D, Wanchu A, and Bhatnagar A. Interaction between oxidative stress and chemokines: possible pathogenic role in systemic lupus erythematosus and rheumatoid arthritis. Immunobiology 216:1010-1017 (2011)
- [24] Shah D, Kiran R, Wanchu A, and Bhatnagar A. Oxidative stress in systemic lupus erythematosus: relationship to Th1 cytokine and disease activity. Immunol. Lett. 129:7-12 (2010)
- [25] Perl A, Hanczko R, and Doherty E. Assessment of mitochondrial dysfunction in lymphocytes of patients with systemic lupus erythematosus. Meth. Mol. Biol. 900:61-89 (2012)
- [26] Li KJ, Wu CH, Hsieh SC, Lu MC, Tsai CY, and Yu CL. Deranged bioenergetics and defective redox capacity in T lymphocytes and neutrophils are related to cellular dysfunction and increased oxidative stress in patients with active systemic lupus erythematosus. Clin. Dev. Immunol. 2012:548516 (2012)
- [27] Domann FE. Aberrant free radical biology is a unifying theme in the etiology and pathogenesis of major human diseases. Int. J. Mol. Sci. 14:8491-8495 (2013)
- [28] Lee HT, Lin CS, Lee CS, and Tsai CY, and Wei YH. Increased 8-hydroxy-2’-deoxyguanosine in plasma and decreased mRNA expression of human 8-oxoguanine DNA glycosylase 1, antioxidant enzymes, mitochondrial biogenesis-related proteins and glycolytic enzymes in leucocytes in patients with systemic lupus erythematosus. Clin. Exp. Immunol. 176:66-77 (2014)
- [29] Lee HT, Lin CS, Chen WS, Liao HT, Tsai CY, and Wei YH. Leukocyte mitochondrial DNA alteration in systemic lupus erythematosus and its relevance to the susceptibility to lupus nephritis. Int. J. Mol. Sci. 13:8853-8868 (2012)
- [30] Hochberg MC. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 40:1725 (1997)
- [31] Petri M, Orbai AM, Alarcon GS,Gordon C, Merrill JT, Fortin PR, Bruce IN, Isenberg D, Wallace DJ, Nived O, Sturfelt G, Ramsey-Goldman R, Bae SC, Hanly JG, Sánchez-Guerrero J, Clarke A, Aranow C, Manzi S, Urowitz M, Gladman D, Kalunian K, Costner M, Werth VP, Zoma A, Bernatsky S, Ruiz-Irastorza G, Khamashta MA, Jacobsen S, Buyon JP, Maddison P, Dooley MA, van Vollenhoven RF, Ginzler E, Stoll T, Peschken C, Jorizzo JL, Callen JP, Lim SS, Fessler BJ, Inanc M, Kamen DL, Rahman A, Steinsson K, Franks AG Jr, Sigler L, Hameed S, Fang H, Pham N, Brey R, Weisman MH, McGwin G Jr, and Magder LS. Derivation and validation of the Systemic Lupus International Collaborating Clinics classification criteria for systemic lupus erythematosus. Arthritis Rheum. 64:2677-2686 (2012)
- [32] Sato T, Takeda H, Otake S, Yokozawa J, Nishise S, Fujishima S, Orii T, Fukui T, Takano J, Sasaki Y, Nagino K, Iwano D, Yaoita T, and Kawata S. Increased plasma levels of 8-hydroxydeoxyguanosine are associated with development of colorectal tumors. J. Clin. Biochem. Nutr. 47:59-63 (2010)
- [33] Wu CW, Yin PH, Hung WY, Li AF, Li SH, Chi CW, Wei YH, and Lee HC. Mitochondrial DNA mutations and mitochondrial DNA depletion in gastric cancer. Genes Chromosomes Cancer. 44:19-28(2005).
- [34] Yu L, Zhou Y, Jiang Y, Tong W, Yang S, Gao F, Wang K, Li L, Xia T, Cheng Q, and Tong G. Construction and in vitro evaluation of a recombinant live attenuated PRRSV expressing GM-CSF. Virol. J. 11:201 (2014)
- [35] Mok CC. Current role of rituximab in systemic lupus erythematosus. Int. J. Rheum. Dis.18:154-163 (2015)
- [36] Carr MW, Roth SJ, Luther E, Rose SS, and Springer TA. Monocyte chemoattractant protein 1 acts as a T-lymphocyte chemoattractant. Proc. Natl. Acad. Sci. USA. 91:3652-3656 (1994)
- [37] Xu LL, Warren MK, Rose WL, Gong W, and Wang JM. Human recombinant monocyte chemotactic protein and other C-C chemokines bind and induce directional migration of dendritic cells in vitro. J. Leuk. Biol. 6:365-371(1996)
- [38] Dufour JH, Dziejman M, Liu MT, Leung JH, Lane TE, and Luster AD. IFN-gamma-inducible protein 10 (IP-10; CXCL10)-deficient mice reveal a role for IP-10 in effector T cell generation and trafficking. J. Immunol. 168:3195–3204 (2002)
- [39] Angiolillo AL, Sgadari C, Taub DD, Liao F, Farber JM, Maheshwari S, Kleinman HK, Reaman GH, and Tosato G. Human interferon-inducible protein 10 is a potent inhibitor of angiogenesis in vivo. J. Exp. Med. 182:155–162(1995) is. Nephrol. Dial. Transplant. 26:3273-3280(2011)
- [40] Adhya Z, Borozdenkova S, and Karim M.Y. The role of cytokines as biomarkersin systemic lupus erythematosus and lupus nephritis. Nephrol. Dial. Transplant. 26:3273-3280 (2011)
- [41] Iwata Y, Furuichi K, Kaneko S, and Wada T. The role of cytokine in the lupus nephritis. J. Biomed. Biotechnol. 2011:594809 (2011)
- [42] Mok MY, Wu HJ, Lo Y, and Lau CS. The relation of interleukin 17 (IL-17) and IL-23 to Th1/Th2 cytokines and disease activity in systemic lupus erythematosus. J. Rheumatol. 37:2046-2052 (2010)
- [43] Park SJ, Kim JH, Ha TS, and Shin JI.The role ofinterleukin-23/interleukin-17 axis in coexisting anti-glomerular basement membrane disease and lupus nephritis. Saudi J. Kidney Dis. Transpl. 24:596-597 (2013)
- [44] Zhang Z, Kyttaris VC, and Tsokos GC. The role of IL-23/IL-17 axis in lupus nephritis. J. Immunol. 183:3160-3169 (2009)
- [45] Aggarwal S, and Gurney AL. IL-17: prototype member of an emerging cytokine family. J. Leuk. Biol. 71:1–8(2002)
- [46] Gaffen SL. An overview of IL-17 function and signaling. Cytokine 43:402-407 (2008)
- [47] Shah D, Sah S, Wanchu A, Wu MX, and Bhatnagar A. Altered redox state and apoptosis in the pathogenesis of systemic lupus erythematosus. Immunobiology 218:620-627 (2013)
- [48] Mambo E, Gao X, Cohen Y, Guo Z, Talalay P, and Sidransky D. Electrophile and oxidant damage of mitochondrial DNA leading to rapid evolution of homoplasmic mutations. Proc. Natl. Acad. Sci. USA 100:1838-1843 (2003)
- [49] Lee HC and Wei YH. Mitochondria and aging. Adv. Exp. Med. Biol. 942:311-327 (2012)
- [50] Li X, Fang P, Mai J, Choi ET, Wang H, and Yang XF. Targeting mitochondrial reactive oxygen species as novel therapy for inflammatory diseases and cancers. J. Hematol. Oncol. 6:1-19 (2013)
- [51] Sonoda J, Laganiere J, Mehl IR,Barish GD, Chong LW, Li X, Scheffler IE, Mock DC, Bataille AR, Robert F, Lee CH, Giguère V, and Evans RM. Nuclear receptor ERR α and coactivator PGC-1 β are effectors of IFN-γ-induced host defense. Genes Dev. 21:1909-1920 (2007)
- [52] Perl A, Gergely P Jr, Nagy G, Koncz A, and Banki K. Mitochondrial hyperpolarization: a checkpoint of T-cell life, death and autoimmunity. Trends Immunol. 25:360-367 (2004)
