Dysregulation of innate and adaptive serum mediators precedes systemic lupus erythematosus classification and improves prognostic accuracy of autoantibodies

Journal of Autoimmunity

Volumn 74, Issue , 2016, Pages 182-193

  Lu, Rufei ^a,b   Munroe, Melissa E ^a   Guthridge, Joel M ^a   Bean, Krista M ^a   Fife, Dustin A ^a   Chen, Hua ^a   Slight Webb, Samantha R ^a   Keith, Michael P ^c   Harley, John B ^d,e   James, Judith A ^a,b  

^a OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

^b UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^c WALTER REED ARMY MEDICAL CENTER   (United States)

^d CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^e VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Autoantibodies; Biomarkers; Cytokines; Disease progression; Forecasting; Systemic lupus erythematosus

Indexed keywords

APRIL PROTEIN; AUTOANTIBODY; B CELL ACTIVATING FACTOR; GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 12P70; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 2; INTERLEUKIN 21; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR RECEPTOR 1; TUMOR NECROSIS FACTOR RECEPTOR 2; BIOLOGICAL MARKER; CYTOKINE; TUMOR NECROSIS FACTOR;

ADAPTIVE IMMUNITY; ARTICLE; BLOOD SAMPLING; CONTROLLED STUDY; HIGH RISK PATIENT; HUMAN; IMMUNE DYSREGULATION; IMMUNOPATHOGENESIS; INNATE IMMUNITY; INTERVENTION STUDY; MAJOR CLINICAL STUDY; PRIORITY JOURNAL; PROGNOSIS; PROSPECTIVE STUDY; PROTEIN BLOOD LEVEL; SYSTEMIC LUPUS ERYTHEMATOSUS; TISSUE INJURY; BLOOD; CASE CONTROL STUDY; DISEASE EXACERBATION; IMMUNOLOGY; SIGNAL TRANSDUCTION; TIME FACTOR;

ADAPTIVE IMMUNITY; AUTOANTIBODIES; BIOMARKERS; CASE-CONTROL STUDIES; CYTOKINES; DISEASE PROGRESSION; HUMANS; IMMUNITY, INNATE; LUPUS ERYTHEMATOSUS, SYSTEMIC; PROGNOSIS; SIGNAL TRANSDUCTION; TIME FACTORS; TUMOR NECROSIS FACTORS;

EID: 84992568338     PISSN: 08968411     EISSN: 10959157     Source Type: Journal    
DOI: 10.1016/j.jaut.2016.06.001     Document Type: Article

References (85)

1. [1] Tsokos, G.C., Systemic lupus erythematosus. N. Engl. J. Med. 365 (2011), 2110–2121.
2. [2] Arbuckle, M.R., McClain, M.T., Rubertone, M.V., Scofield, R.H., Dennis, G.J., James, J.A., et al. Development of autoantibodies before the clinical onset of systemic lupus erythematosus. N. Engl. J. Med. 349 (2003), 1526–1533.
3. [3] McClain, M.T., Heinlen, L.D., Dennis, G.J., Roebuck, J., Harley, J.B., James, J.A., Early events in lupus humoral autoimmunity suggest initiation through molecular mimicry. Nat. Med. 11 (2005), 85–89.
4. [4] James, J.A., Kim-Howard, X.R., Bruner, B.F., Jonsson, M.K., McClain, M.T., Arbuckle, M.R., et al. Hydroxychloroquine sulfate treatment is associated with later onset of systemic lupus erythematosus. Lupus 16 (2007), 401–409.
5. [5] Li, Q.Z., Zhou, J., Lian, Y., Zhang, B., Branch, V.K., Carr-Johnson, F., et al. Interferon signature gene expression is correlated with autoantibody profiles in patients with incomplete lupus syndromes. Clin. Exp. Immunol. 159 (2010), 281–291.
6. [6] Bouwhuis, M.G., Gast, A., Figl, A., Eggermont, A.M., Hemminki, K., Schadendorf, D., et al. Polymorphisms in the CD28/CTLA4/ICOS genes: role in malignant melanoma susceptibility and prognosis?. Cancer Immunol. Immunother. CII 59 (2010), 303–312.
7. [7] Bruner, B.F., Guthridge, J.M., Lu, R., Vidal, G., Kelly, J.A., Robertson, J.M., et al. Comparison of autoantibody specificities between traditional and bead-based assays in a large, diverse collection of patients with systemic lupus erythematosus and family members. Arthritis Rheum. 64 (2012), 3677–3686.
8. [8] Satoh, M., Chan, E.K., Ho, L.A., Rose, K.M., Parks, C.G., Cohn, R.D., et al. Prevalence and sociodemographic correlates of antinuclear antibodies in the United States. Arthritis Rheum. 64 (2012), 2319–2327.
9. [9] Vila, L.M., Mayor, A.M., Valentin, A.H., Garcia-Soberal, M., Vila, S., Clinical outcome and predictors of disease evolution in patients with incomplete lupus erythematosus. Lupus 9 (2000), 110–115.
10. [10] Wandstrat, A.E., Carr-Johnson, F., Branch, V., Gray, H., Fairhurst, A.M., Reimold, A., et al. Autoantibody profiling to identify individuals at risk for systemic lupus erythematosus. J. Autoimmun. 27 (2006), 153–160.
11. [11] Kil, L.P., Hendriks, R.W., Aberrant B cell selection and activation in systemic lupus erythematosus. Int. Rev. Immunol. 32 (2013), 445–470.
12. [12] Datta, S.K., Production of pathogenic antibodies: cognate interactions between autoimmune T and B cells. Lupus 7 (1998), 591–596.
13. [13] Choi, J., Kim, S.T., Craft, J., The pathogenesis of systemic lupus erythematosus-an update. Curr. Opin. Immunol. 24 (2012), 651–657.
14. [14] Lee, S.K., Silva, D.G., Martin, J.L., Pratama, A., Hu, X., Chang, P.P., et al. Interferon-gamma excess leads to pathogenic accumulation of follicular helper T cells and germinal centers. Immunity 37 (2012), 880–892.
15. [15] Mari, N., Hercor, M., Denanglaire, S., Leo, O., Andris, F., The capacity of Th2 lymphocytes to deliver B-cell help requires expression of the transcription factor STAT3. Eur. J. Immunol. 43 (2013), 1489–1498.
16. [16] Peng, S.L., Szabo, S.J., Glimcher, L.H., T-bet regulates IgG class switching and pathogenic autoantibody production. Proc. Natl. Acad. Sci. U. S. A. 99 (2002), 5545–5550.
17. [17] Park, H.J., Kim, D.H., Lim, S.H., Kim, W.J., Youn, J., Choi, Y.S., et al. Insights into the role of follicular helper T cells in autoimmunity. Immune Netw. 14 (2014), 21–29.
18. [18] Munroe, M.E., Lu, R., Zhao, Y.D., Fife, D.A., Robertson, J.M., Guthridge, J.M., et al. Altered type II interferon precedes autoantibody accrual and elevated type I interferon activity prior to systemic lupus erythematosus classification. Ann. Rheum. Dis., 2016 In Press.
19. [19] Harigai, M., Kawamoto, M., Hara, M., Kubota, T., Kamatani, N., Miyasaka, N., Excessive production of IFN-gamma in patients with systemic lupus erythematosus and its contribution to induction of B lymphocyte stimulator/B cell-activating factor/TNF ligand superfamily-13B. J. Immunol. 181 (2008), 2211–2219.
20. [20] Lopez, P., Scheel-Toellner, D., Rodriguez-Carrio, J., Caminal-Montero, L., Gordon, C., Suarez, A., Interferon-alpha-induced B-lymphocyte stimulator expression and mobilization in healthy and systemic lupus erythematosus monocytes. Rheumatol. Oxf. 53 (2014), 2249–2258.
21. [21] Cancro, M.P., D'Cruz, D.P., Khamashta, M.A., The role of B lymphocyte stimulator (BLyS) in systemic lupus erythematosus. J. Clin. Invest. 119 (2009), 1066–1073.
22. [22] Munroe, M.E., Vista, E.S., Guthridge, J.M., Thompson, L.F., Merrill, J.T., James, J.A., Pro-inflammatory adaptive cytokines and shed tumor necrosis factor receptors are elevated preceding systemic lupus erythematosus disease flare. Arthritis & rheumatol. 66 (2014), 1888–1899.
23. [23] Munroe, M.E., James, J.A., Genetics of lupus nephritis: clinical implications. Seminars Nephrol. 35 (2015), 396–409.
24. [24] Stoll, T., Seifert, B., Isenberg, D.A., SLICC/ACR Damage Index is valid, and renal and pulmonary organ scores are predictors of severe outcome in patients with systemic lupus erythematosus. Br. J. Rheumatol. 35 (1996), 248–254.
25. [25] Rahman, P., Gladman, D.D., Urowitz, M.B., Hallett, D., Tam, L.S., Early damage as measured by the SLICC/ACR damage index is a predictor of mortality in systemic lupus erythematosus. Lupus 10 (2001), 93–96.
26. [26] Bruce, I.N., O'Keeffe, A.G., Farewell, V., Hanly, J.G., Manzi, S., Su, L., et al. Factors associated with damage accrual in patients with systemic lupus erythematosus: results from the Systemic Lupus International Collaborating Clinics (SLICC) Inception Cohort. Ann. Rheum. Dis. 74 (2015), 1706–1713.
27. [27] Urowitz, M.B., Gladman, D.D., Ibanez, D., Fortin, P.R., Bae, S.C., Gordon, C., et al. Evolution of disease burden over five years in a multicenter inception systemic lupus erythematosus cohort. Arthritis Care Res. 64 (2012), 132–137.
28. [28] Heinlen, L.D., McClain, M.T., Merrill, J., Akbarali, Y.W., Edgerton, C.C., Harley, J.B., et al. Clinical criteria for systemic lupus erythematosus precede diagnosis, and associated autoantibodies are present before clinical symptoms. Arthritis Rheum. 56 (2007), 2344–2351.
29. [29] Hochberg, M.C., Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum., 40, 1997, 1725.
30. [30] Tan, E.M., Cohen, A.S., Fries, J.F., Masi, A.T., McShane, D.J., Rothfield, N.F., et al. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 25 (1982), 1271–1277.
31. [31] Rosenberg-Hasson, Y., Hansmann, L., Liedtke, M., Herschmann, I., Maecker, H.T., Effects of serum and plasma matrices on multiplex immunoassays. Immunol. Res. 58 (2014), 224–233.
32. [32] Kumar, Y., Liang, C., Bo, Z., Rajapakse, J.C., Ooi, E.E., Tannenbaum, S.R., Serum proteome and cytokine analysis in a longitudinal cohort of adults with primary dengue infection reveals predictive markers of DHF. PLoS Negl. Trop. Dis., 6, 2012, e1887.
33. [33] Dossus, L., Becker, S., Achaintre, D., Kaaks, R., Rinaldi, S., Validity of multiplex-based assays for cytokine measurements in serum and plasma from “non-diseased” subjects: comparison with ELISA. J. Immunol. Methods 350 (2009), 125–132.
34. [34] Dupont, N.C., Wang, K., Wadhwa, P.D., Culhane, J.F., Nelson, E.L., Validation and comparison of luminex multiplex cytokine analysis kits with ELISA: determinations of a panel of nine cytokines in clinical sample culture supernatants. J. Reprod. Immunol. 66 (2005), 175–191.
35. [35] Heinlen, L.D., McClain, M.T., Ritterhouse, L.L., Bruner, B.F., Edgerton, C.C., Keith, M.P., et al. 60 kD Ro and nRNP A frequently initiate human lupus autoimmunity. PLoS One, 5, 2010, e9599.
36. [36] Akobeng, A.K., Understanding diagnostic tests 3: receiver operating characteristic curves. Acta Paediatr. 96 (2007), 644–647.
37. [37] Genuer, R., Poggi, J.M., Tuleau-Malot, C., Variable selection using random forests. Pattern Recogn. Lett. 31 (2010), 2225–2236.
38. [38] Fife, D.A., Package “fifer”. 2014 CRAN: CRAN.
39. [39] Ladd, B., Kenner, S., Information visualization and analytical data mining in pharmaceutical R&D. Curr. Opin. Drug Discov. Devel 3 (2000), 280–291.
40. [40] Gomez, D., Correa, P.A., Gomez, L.M., Cadena, J., Molina, J.F., Anaya, J.M., Th1/Th2 cytokines in patients with systemic lupus erythematosus: is tumor necrosis factor alpha protective?. Semin. Arthritis Rheum. 33 (2004), 404–413.
41. [41] Viallard, J.F., Taupin, J.L., Miossec, V., Pellegrin, J.L., Moreau, B.L., Analysis of interleukin-6, interleukin-10 and leukemia inhibitory factor (LIF) production by peripheral blood cells from patients with systemic lupus erythematosus identifies LIF as a potential marker of disease activity. Eur. Cytokine Netw. 10 (1999), 17–24.
42. [42] Ohtsuka, K., Gray, J.D., Stimmler, M.M., Horwitz, D.A., The relationship between defects in lymphocyte production of transforming growth factor-beta1 in systemic lupus erythematosus and disease activity or severity. Lupus 8 (1999), 90–94.
43. [43] Alvarado-Sanchez, B., Hernandez-Castro, B., Portales-Perez, D., Baranda, L., Layseca-Espinosa, E., Abud-Mendoza, C., et al. Regulatory T cells in patients with systemic lupus erythematosus. J. Autoimmun. 27 (2006), 110–118.
44. [44] Arbuckle, M.R., James, J.A., Dennis, G.J., Rubertone, M.V., McClain, M.T., Kim, X.R., et al. Rapid clinical progression to diagnosis among African-American men with systemic lupus erythematosus. Lupus 12 (2003), 99–106.
45. [45] Acosta-Rodriguez, E.V., Craxton, A., Hendricks, D.W., Merino, M.C., Montes, C.L., Clark, E.A., et al. BAFF and LPS cooperate to induce B cells to become susceptible to CD95/Fas-mediated cell death. Eur. J. Immunol. 37 (2007), 990–1000.
46. [46] Wong, C.K., Ho, C.Y., Li, E.K., Lam, C.W., Elevation of proinflammatory cytokine (IL-18, IL-17, IL-12) and Th2 cytokine (IL-4) concentrations in patients with systemic lupus erythematosus. Lupus 9 (2000), 589–593.
47. [47] Merrill, J.T., Neuwelt, C.M., Wallace, D.J., Shanahan, J.C., Latinis, K.M., Oates, J.C., et al. Efficacy and safety of rituximab in moderately-to-severely active systemic lupus erythematosus: the randomized, double-blind, phase II/III systemic lupus erythematosus evaluation of rituximab trial. Arthritis Rheum. 62 (2010), 222–233.
48. [48] Rovin, B.H., Furie, R., Latinis, K., Looney, R.J., Fervenza, F.C., Sanchez-Guerrero, J., et al. Efficacy and safety of rituximab in patients with active proliferative lupus nephritis: the Lupus Nephritis Assessment with Rituximab study. Arthritis Rheum. 64 (2012), 1215–1226.
49. [49] Slight-Webb, S., Lu, R., Ritterhouse, L.L., Munroe, M.E., Maecker, H.T., Fathman, C.G., et al. Autoantibody-positive healthy individuals display unique immune profiles that may regulate autoimmunity. Arthritis & rheumatol., 2016 In Press.
50. [50] Ritterhouse, L.L., Crowe, S.R., Niewold, T.B., Kamen, D.L., Macwana, S.R., Roberts, V.C., et al. Vitamin D deficiency is associated with an increased autoimmune response in healthy individuals and in patients with systemic lupus erythematosus. Ann. Rheum. Dis. 70:9 (2011), 1569–1574.
51. [51] Wahren-Herlenius, M., Dorner, T., Immunopathogenesis mechanisms of systemic autoimmune disease. Lancet 382 (2013), 819–831.
52. [52] Hughes-Austin, J.M., Deane, K.D., Derber, L.A., Kolfenbach, J.R., Zerbe, G.O., Sokolove, J., et al. Multiple cytokines and chemokines are associated with rheumatoid arthritis-related autoimmunity in first-degree relatives without rheumatoid arthritis: studies of the Aetiology of Rheumatoid Arthritis (SERA). Ann. Rheum. Dis. 72 (2013), 901–907.
53. [53] Deane, K.D., Striebich, C.C., Goldstein, B.L., Derber, L.A., Parish, M.C., Feser, M.L., et al. Identification of undiagnosed inflammatory arthritis in a community health fair screen. Arthritis Rheum. 61 (2009), 1642–1649.
54. [54] Deane, K.D., O'Donnell, C.I., Hueber, W., Majka, D.S., Lazar, A.A., Derber, L.A., et al. The number of elevated cytokines and chemokines in preclinical seropositive rheumatoid arthritis predicts time to diagnosis in an age-dependent manner. Arthritis Rheum. 62 (2010), 3161–3172.
55. [55] Yap, D.Y., Lai, K.N., Cytokines and their roles in the pathogenesis of systemic lupus erythematosus: from basics to recent advances. J. Biomed. Biotechnol., 2010, 2010, 365083.
56. [56] Charles, N., Hardwick, D., Daugas, E., Illei, G.G., Rivera, J., Basophils and the T helper 2 environment can promote the development of lupus nephritis. Nat. Med. 16 (2010), 701–707.
57. [57] Cash, H., Relle, M., Menke, J., Brochhausen, C., Jones, S.A., Topley, N., et al. Interleukin 6 (IL-6) deficiency delays lupus nephritis in MRL-Faslpr mice: the IL-6 pathway as a new therapeutic target in treatment of autoimmune kidney disease in systemic lupus erythematosus. J. Rheumatol. 37 (2010), 60–70.
58. [58] Linker-Israeli, M., Deans, R.J., Wallace, D.J., Prehn, J., Ozeri-Chen, T., Klinenberg, J.R., Elevated levels of endogenous IL-6 in systemic lupus erythematosus. A putative role in pathogenesis. J. Immunol. 147 (1991), 117–123.
59. [59] Eilertsen, G.O., Nikolaisen, C., Becker-Merok, A., Nossent, J.C., Interleukin-6 promotes arthritis and joint deformation in patients with systemic lupus erythematosus. Lupus 20 (2011), 607–613.
60. [60] Szodoray, P., Nakken, B., Barath, S., Csipo, I., Nagy, G., El-Hage, F., et al. Altered Th17 cells and Th17/regulatory T-cell ratios indicate the subsequent conversion from undifferentiated connective tissue disease to definitive systemic autoimmune disorders. Hum. Immunol. 74 (2013), 1510–1518.
61. [61] Mesquita, D., de Melo Cruvinel, W., Araujo, J., Pucci, F., Salmazi, K., Kallas, E., et al. Systemic lupus erythematosus exhibits a dynamic and continuum spectrum of effector/regulatory T cells. Scand. J. Rheumatol. 40 (2011), 41–50.
62. [62] Chen, X.Q., Yu, Y.C., Deng, H.H., Sun, J.Z., Dai, Z., Wu, Y.W., et al. Plasma IL-17A is increased in new-onset SLE patients and associated with disease activity. J. Clin. Immunol. 30 (2010), 221–225.
63. [63] Szodoray, P., Nakken, B., Barath, S., Gaal, J., Aleksza, M., Zeher, M., et al. Progressive divergent shifts in natural and induced T-regulatory cells signify the transition from undifferentiated to definitive connective tissue disease. Int. Immunol. 20 (2008), 971–979.
64. [64] Schroder, K., Hertzog, P.J., Ravasi, T., Hume, D.A., Interferon-gamma: an overview of signals, mechanisms and functions. J. Leukoc. Biol. 75 (2004), 163–189.
65. [65] Boghdadi, G., Elewa, E.A., Increased serum APRIL differentially correlates with distinct cytokine profiles and disease activity in systemic lupus erythematosus patients. Rheumatol. Int. 34 (2014), 1217–1223.
66. [66] Palanichamy, A., Bauer, J.W., Yalavarthi, S., Meednu, N., Barnard, J., Owen, T., et al. Neutrophil-mediated IFN activation in the bone marrow alters B cell development in human and murine systemic lupus erythematosus. J. Immunol. 192 (2014), 906–918.
67. [67] Moulton, V.R., Tsokos, G.C., T cell signaling abnormalities contribute to aberrant immune cell function and autoimmunity. J. Clin. Invest. 125 (2015), 2220–2227.
68. [68] Comte, D., Karampetsou, M.P., Tsokos, G.C., T cells as a therapeutic target in SLE. Lupus 24 (2015), 351–363.
69. [69] Niewold, T.B., Advances in lupus genetics. Curr. Opin. Rheumatol. 27 (2015), 440–447.
70. [70] Hedrich, C.M., Crispin, J.C., Tsokos, G.C., Epigenetic regulation of cytokine expression in systemic lupus erythematosus with special focus on T cells. Autoimmunity 47 (2014), 234–241.
71. [71] Poole, B.D., Scofield, R.H., Harley, J.B., James, J.A., Epstein-Barr virus and molecular mimicry in systemic lupus erythematosus. Autoimmunity 39 (2006), 63–70.
72. [72] Poole, B.D., Templeton, A.K., Guthridge, J.M., Brown, E.J., Harley, J.B., James, J.A., Aberrant Epstein-Barr viral infection in systemic lupus erythematosus. Autoimmun. Rev. 8 (2009), 337–342.
73. [73] Clancy, R.M., Markham, A.J., Buyon, J.P., Endosomal Toll-like receptors in clinically overt and silent autoimmunity. Immunol. Rev. 269 (2016), 76–84.
74. [74] van den Borne, B.E., Dijkmans, B.A., de Rooij, H.H., le Cessie, S., Verweij, C.L., Chloroquine and hydroxychloroquine equally affect tumor necrosis factor-alpha, interleukin 6, and interferon-gamma production by peripheral blood mononuclear cells. J. Rheumatol. 24 (1997), 55–60.
75. [75] Willis, R., Seif, A.M., McGwin, G. Jr., Martinez-Martinez, L.A., Gonzalez, E.B., Dang, N., et al. Effect of hydroxychloroquine treatment on pro-inflammatory cytokines and disease activity in SLE patients: data from LUMINA (LXXV), a multiethnic US cohort. Lupus 21 (2012), 830–835.
76. [76] Sacre, K., Criswell, L.A., McCune, J.M., Hydroxychloroquine is associated with impaired interferon-alpha and tumor necrosis factor-alpha production by plasmacytoid dendritic cells in systemic lupus erythematosus. Arthritis Res. Ther., 14, 2012, R155.
77. [77] Costedoat-Chalumeau, N., Dunogue, B., Morel, N., Le Guern, V., Guettrot-Imbert, G., Hydroxychloroquine: a multifaceted treatment in lupus. Presse medicale 43 (2014), e167–180.
78. [78] Tsang, A.S.M.W., Bultink, I.E., Systemic lupus erythematosus: review of synthetic drugs. Expert Opin. Pharmacother. 16 (2015), 2793–2806.
79. [79] Rainsford, K.D., Parke, A.L., Clifford-Rashotte, M., Kean, W.F., Therapy and pharmacological properties of hydroxychloroquine and chloroquine in treatment of systemic lupus erythematosus, rheumatoid arthritis and related diseases. Inflammopharmacology 23 (2015), 231–269.
80. [80] Catley, M.C., Coote, J., Bari, M., Tomlinson, K.L., Monoclonal antibodies for the treatment of asthma. Pharmacol. Ther. 132 (2011), 333–351.
81. [81] Shirota, Y., Yarboro, C., Fischer, R., Pham, T.H., Lipsky, P., Illei, G.G., Impact of anti-interleukin-6 receptor blockade on circulating T and B cell subsets in patients with systemic lupus erythematosus. Ann. Rheum. Dis. 72 (2013), 118–128.
82. [82] Thanarajasingam, U., Niewold, T.B., Sirukumab: a novel therapy for lupus nephritis?. Expert Opin. investigational drugs 23 (2014), 1449–1455.
83. [83] Chen, P., Vu, T., Narayanan, A., Sohn, W., Wang, J., Boedigheimer, M., et al. Pharmacokinetic and pharmacodynamic relationship of AMG 811, an anti-IFN-gamma IgG monoclonal antibody, in patients with systemic lupus erythematosus. Pharm. Res. 32:2 (2015), 640–653.
84. [84] Yellin, M., Paliienko, I., Balanescu, A., Ter-Vartanian, S., Tseluyko, V., Xu, L.A., et al. A phase II, randomized, double-blind, placebo-controlled study evaluating the efficacy and safety of MDX-1100, a fully human anti-CXCL10 monoclonal antibody, in combination with methotrexate in patients with rheumatoid arthritis. Arthritis Rheum. 64 (2012), 1730–1739.
85. [85] Zouali, M., Uy, E.A., Belimumab therapy in systemic lupus erythematosus. BioDrugs. Clin. Immunother. Biopharm. gene Ther. 27 (2013), 225–235.